Marine Ecology: Processes, Systems, and Impacts

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 •
aline co 0
Processes, Systems, and Impacts
SECOND EDITION

Michel J. Kaiser • Martin J.Attrill • Simon Jennings

David N.Thomas • David K.A. Barnes • Andrew S. Brierley • Jan Geert Hiddink
Hermanni Kaartokallio • Nicholas V. C. Polunin • David G. Raffaelli

With contributions from

Peter J. Ie B.Williams • Gareth Johnson • Kerry Howell

Coleen Suckling • Anne Berit Skiftesvik

OXFORD
UNIVERS ITY PRESS
 OXFORD
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I 3 5 7 9 10 8 5 4 2
'It is likely that much present day published science depends on "fa ct"which has not been sufficiently
checked. James Elroy Flecker, in his play Hassan, wrote: "Men who think themselves wise believe
nothing until the proof. Men who are wise believe anything until the disproof." Perhaps in this com-
plicated world, one should steer a careful path between Flecker's two extremes.'
G. E. (Tony) Fogg (1919-2005)
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Preface
Marine ecology: an introduction
Approximately 2.2 billion people live within 100 Ian of a
coastline. This figure is set to double by 2025. While the
average population density along coastlines is currently
80 people krrr-, this increases to up to 1000 krrr- in coun-
tries such as Egypt and Bangladesh. Many of these coastal
inhabitants depend directly upon marine resources for their
subsistence or income. The world's oceans provide a wealth
of goods and services. and are used as repositories for our
waste products, yield renewable (wind and tidal energy)
and non-renewable (oil and gas) forms of energy, provide
important bulk transportation routes, provide a source of
food, yield mined commodities (diamonds, heavy metals),
and provide recreational benefits that support important
tourism industries. Technological advances have enabled
us to use areas of the oceans that previously were inacces-
sible to humans, and many marine resources are either fully
or over-exploited. However. with technical advances. the
increase in knowledge and material riches is often accom-
panied by increased consequences of technical failures, as
seen in the Gulf of Mexico Deep Horizon blowout in 2010.
Despite our growing use of the oceans and major efforts to
catalogue the diversity and distribution. such as the Cen-
sus of Marine Life. much of the marine realm has never
been viewed by the human eye. Indeed, it is sobering to
think that we probably know more about the surface of the
moon than we do about the marine environment ofour own
planet. Understanding marine ecological processes and
systems are urgent research priorities if we are to compre-
hend the ecological effects of human activities that impact
upon them and more widely on global systems. This under-
standing is essential to help society find ways of achieving
sustainable use of marine resources. Thus marine ecology
remains an exciting and pivotal subject that has matured
into an integrated science that encapsulates biological.
chemical, and physical processes from the microscopic to
the global scale.
Nearly 40Ofo of the world's population live close to the
coastline.
The world's oceans are heavily exploited for mineral and
biological resources even though much of the ocean
remains unexplored.
The evolution of marine ecology
The development of marine ecology can be charted through
three major eras. Early naturalists worked in an age when
seafarers' stories of sea monsters abounded and authors
such as Jules Verne romanticized exploration of the deep
and the battle with the leviathan. The observations of early
naturalists, such as Darwin, were mostly restricted to the
shoreline, while scientific sampling of the abyss was per-
formed by lowering crude sampling devices to the distant
seabed. This must have been (and remains) an incred-
ibly exciting time. as every sample probably contained an
organism viewed for the first time by human eyes. Explora-
tion of the oceans continues to be an ongoing task, with the
discovery ofa new phylum in the last few decades (Chapter
1) . Then in the early to mid-twentieth century, ecologists
such as Petersen and Thorson began to consider ecological
rules that determined the distribution and abundance of
marine species and communities (Chapters 3, 7,8, and 13).
This coincided with the early beginnings offisheries science
and concerted efforts to understand the processes affecting
population variability in fish populations.
The history of marine ecology can be divided into three
main eras: (1) exploration and description; (2) experi-
mental manipulation; (3) integration and application.
The second era of marine ecology began in the late
1960s and early 1970s, when ecologists such as Connell
and Paine undertook their seminal research on the effects
of disturbance and competition in ecology. using marine
systems as models fortheir studies (Chapter 6) . Their work
had a pivotal role in the development of general ecologi-
cal theory, which then springboarded into the more easily
studied terrestrial systems. This theme has developed to
the present day, and spawned many manipulative studies
of the role of predators and grazers in marine systems and
long-term studies of food-web dynamics. Technological
advances have enabled us to understand better the pro-
cesses of primary and microbial production; the advent of
stable isotope analysis has provided a common means to
assess the trophic status (i.e. top predator. forage species,
detritivore, secondary producer) of species in marine com-
munities from around the world (Chapters 7, 8, and 10) and
the development of remote sensing methods to describe the
distribution and dynamics of primaryproduetion on global
scales provided unprecedented insights into the ecology
 Preface
of the global oceans. Novel molecular tools have offered
new insights into the diversity of species complexes that
previously were the source of debate amongst taxonomists
(Chapter 1).
While we still have a lot to learn about marine ecosys-
tem processes, we have entered a new phase (the third era)
in which research has become more urgently focused on
the ecological ramifications of an ever-increas ing list of
human impacts (Chapters 13, 14, and 15). This new focus
still firmly relies upon ecological theory (Chapters 1, 3, 4,
7, 13, and 15) to understand how communities respond to
exploitation and disturbance. These impacts occur against
a background of climate change that is occurring at a rate
faster than previously recorded in our time. Changes in
water temperature, storm activity, and precipitation are
now compounded by the potential of ocean acidification
altering biochemical processes in the ocean. Activities such
as comme rcial fishing have occurred for hundreds of years,
but have sometimes reached such intensive levels that they
Ecosystem goods and services
The concept of ecosystem goods is fairly easy to grasp
in tangible economic terms; for example, the value (US$)
of fish or other commodi ties extracted or farmed in the
ocean. Perhaps less obvious are the values attributed to
the regulat ing functions, such as flood control and coastal
defence, and the cultural non-material benefits derived
have driven fundamental changes in ecosystem status . An
increasingly complex range of contaminants is pouring into
many coastal waters, and their pernicious sub-lethal effects
may cause reduced survival of larval stages and alteration
ofsexual characteristics in adult organisms . The incidences
ofdeoxygenation in coastal waters have increased in recent
years with catastrophic implications for the associated fish-
eries and aquaculture activities, not to mention degrada-
tion of ecosystem fun ctioning, goods, and services (see box
below). The latter provide a clue to the direction of marine
ecology of the future. While there are still many gaps to be
filled, the latest exciting advances are being made by stud-
ies that are multidisciplinary, combining oceanography,
biogeochemistry, and sedime ntology together with marine
ecology, a trend that is set to continue into the future.
Human impacts on the marine environment are set
against a background of an increasing rate of global
climate change.
from marine ecosystems. Cultural values are ofte n deeply
embedded within human society, as typified by the bless-
ing of the fleet by the local Roman Catholic Bishop in
Provincetown Harbour, New England (inset), where
a large proportion of the fishing commu nity can trace
their roots to Portugal or the Azores. (Photographs: M. J.
Kaiser.)
,
. ,.
-
•,
 Preface
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Provisioning Regulating Cultural

Products obtained from : Benefi ts obtained from: Non-material benefits obtained from :
ecosystems regulati on of ecosystem processes ecosystems
food climate regulation spirit ual
freshwater disease co ntro l recreational
fuel flood con trol aesthetic
biochemicals detoxification inspirational
genetic reso urces po llinat ion ed ucat ional
communal
symbolic
• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Supporting
Services necessary for th e pro duct ion of all oth er ecosystem serv ices
Soil form ation
Nutrient cycli ng
Eco log ical processes/fu nctioni ng

These are exciting times, but even the multidisciplinary good example would be the loss of the cultural services that
approach is constrained within the boundaries of' marine sci- occurs when a pristine flora and fauna is degraded (e.g. loss
ence'. This has been the typical approach of scientists , to offe r of w hales from Arctic waters deprives Inuit peoples of the
up our findings to the wider public and governmental bodies, cultural aspect of hunting whales, regardless of the practical
at which point we have fulfilled our duty. This approach is need to acquire food) (see box above) . Different biodivers ity
rapidly being replaced by the realization that marine eco- change scenarios (e.g. habitat fragmentation, contamination,
syste ms have tangible value to society, not only in terms of over-exploitation) are likely to affect processes to a varying
the goods (fis h, aggregate, oil) that are yielded, but also in exte nt, because different kinds of taxa (large or small, pri-
terms of the services that they provide (carbo n sequestration, mary producers or top predators) are lost under the different
coastal defence, waste repositories). Degradation of biodi- scenarios. A good example of the latter is the over-harves ting
versity is thought to reduce the capacity of the ecosyste ms of bottom-dwelling fish and incidental removal of other sea-
to deliver goods and services, thus biodiversity loss has real bed animals (b ent h os) on the Scotian Shelf off Canada. This
economic, societal, and cultural costs for human society. has led to a decoupling of the ecosystem link between water
For example, living m arine syste ms, such as coral reefs and column and seabed processes (b en th o p ela gic coupling)
mangrove forests, provide an important buffer between the and ultimately resulted in a syste m dominated by mid-water
ocean and the land. This role was brought sharply into focus (pela gic) fishes. In addition, specific goods and services may
w ith the 2004 tsunami that struck the Indian Ocean leaving be supported by several different processes , further convolut-
over SOOO dead in Thailand alone, with the exte nt of damage ing their relationship w ith biodivers ity.
often correlating with the exte nt of coastal defence.
While ecosystem goods are reasonably simple concepts
Marine ecology is beginning to break out of traditional to grasp, e.g. the acquisition of food or minerals, the
scientific boundaries and is beginning to interface with cultural value of biodiversity is a more abstract concept.
economics and the social sciences to understand the wider
societal importance of marine biodiversity.

Most experimental m anipulations of biodiversity indicate

Using this book to study marine
some relationship between biodivers ity and ecosystem
ecology
processes; however, few have drawn out the links between Marine Eco logy: Processes, Systems, and Imp acts h as been
biodiversity change and the output of goods and services. A written to address the current need to understand the appli-
 Preface
cation of marine ecology in a marine environment strongly
influenced by human activities. The structure of the book
reflects the integrated approach to marine ecology that is
necessary to answer many of today's key marine environ-
mental and conservation problems. which form the focus of
the last section of the book. The bookis divided into 16 chap-
ters arranged in four distinct sections. The opening chapter
deals with the processes that affect patterns at a variety of
spatial and temporal scales, diversity. community organi-
zation, and structuring processes. and provides a palaeo-
ecological perspective on present-day marine systems. As a
marine ecologist, it is important to have a grasp of the rel-
evant time-scales that impact upon the systems in which we
work. While much of the ecology we encounter deals with
either instantaneous or relatively short-term (1-3 years in
duration) processes. evolutionary ecologists think in terms
of thousands to millions of years. Some environments. such
as the deep sea, have remained relatively stable on an evolu-
tionary time-scale. whereas coastal and shelf habitats have
experienced far more frequent changes. This dynamic flux
in the near coastal habitat is brought into focus by present-
day findings, at sites currently 40 m beneath the sea to the
west of Florida in the Gulf of Mexico, of human artefacts
and animal bones from the early Holocene with evidence of
butcher cuts and other implement shaping.
Processes contains three chapters that address the fun-
damental global processes of primary and microbial pro-
duction that fuel marine systems and the ecology of the
organisms responsible. Chapter two describes primary pro-
cesses. while Chapter three has been revised extensively to
better convey its biological context. These two chapters lead
into a new chapter that deals with secondary production.
Systems then addresses in more detail estuaries. rocky and
sandy shores, the pelagic environment. continental shelf
seabed. the deep sea, mangroves. and seagrass meadows,
coral reefs. and polar seas. Impacts tackles some ofthe most
pressing environmental issues relevant to the marine envi-
ronment that span the systems described beforehand, with
chapters on fisheries. aquaculture. disturbance, pollution,
and climate change. and finally marine conservation. The
penultimate chapter also includes a consideration of the
experimental approach needed to determine the effects of
human impacts and deals with common pitfalls made by stu-
dents undertaking field and laboratory projects.
This second edition has been revised extensively
throughout and the feedback from users of the first edition
has helped us identify new areas for inclusion. As requested,
we have supplemented the online supporting materials with
worked examples (e .g. how to calculate secondary produc-
tion) and advice on improving exam performance.
Other textbooks have traditionally dealt with key physi-
cal and chemical environmental processes as a discrete unit,
usually towards the beginning of the book. This section can
be overlooked or its importance not appreciated at the time
of reading or forgotten by the time it becomes relevant in the
text. In Marine Ecology: Processes. Systems, and Impacts, we
have integrated the environmental processes at key points
that are cross-referenced throughout the text. so that their
relevance is immediate and the learning process enhanced.
Some of these key processes are reiterated from a slightly
different perspective or even repeated in a number of chap-
ters so that learning is reinforced. Key words and concepts
are highlighted in bold throughout the text to aid learning
and revision. In addition to the definitions and explanations
given in the text. an excellent online glossary of important
marine biological terms can be found at the website of the
Marine Life Information Network for Britain and Ireland
(MARLIN; see www.marlin.ac.uk for more information) .
Boxes are used to expand specific points, and offer interest-
ing examples and case studies that illuminate the concepts
being introduced. In this second edition we have highlighted
in each chapter key techniques that are important to the
contemporary marine ecologist and current focus boxes
that we feel are likely to be of major interest in coming years.
Finally, we have provided a short list offurther reading, try-
ing wherever possible to recommend widely accessible lit-
erature and have provided a list of websites that will enable
you to learn more about specific subjects or disciplines. Full
citations for all references given in the chapters can be found
at the end of the book.
Marine ecology is a highly relevant and challenging sub-
ject that is fascinating to amateur. student. and professional
alike. We hope that students using this textbook will gain a
real feeling for the excitement of marine ecology as a sub-
ject of interest, a hobby, and a potential career.
Michel Kaiser
Online Resource Centre
Marine Ecology: Processes, Systems, and Impacts is supported
by an Online Resource Centre, which holds various supple-
mentary materials for students and registered adopters,
including figures from the book available to download,
videos, and a web link library including all the URLs cited
in the book. Visit: www.oxfordtextbooks.co.uk/orc/kai-
ser2e/.
New to this Edition
This 2nd edition has been revised by 30%, including an
entirely new chapter on secondary production. Two new
authors have been added to the team, and all chapters
have been updated to include key works, issues, and topics
published since 2005 . Coverage of socioeconomic issues
and climate change has been enhanced in this edition and
two new box types-Current Focus and Techniques-have
been introduced to highlight important issues facing ecolo-
gists today and showcase contemporary research methods.
respectively.
Acknowledgements
As with any large project, this book could only be brought to
fruition with the help and goodwill of many others.
The authors thank the following for their collaboration
and help with the reproduction of illustrative materials:
Alice Alldredge, Ann-Margret Amui-Vedel, Kirsty Ander-
son, Emmanuel Arand, Peter Auster, Phillip Assay, Tim
Atack, Riitta Autio, Nick Baker, Ole Johan Brett, Gen Broad,
Tracey Bryant, Andrew Butko, Blaise Bullimore, S. C. Cary,
Patrice Ceisel, Chelsea Instruments, Kris Chmielewski,
David Clausen, Joey Comiso, Finlo Cottier, John O. Dabiri,
Paul Dando, Bruno Danis, Meg Daly, Gerhard Dieckmann,
Beatriz Diez, Emily Downes, Nick Dulvy, Kurt Fedra, Kevin
Fitzsimmons, Sarah Foster, Peter Fretwell, Jo Gasgoigne,
David Gillikin, Brett Glencross, Ronnie Glud, Charles
Greenlaw, Sonnke Grossmann, Julian Gutt, Jason Hall-
Spencer, Christian Hamm, Heinz Walz GmbH, IFREMER,
Joachim Henjes, Hilmar Hinz, Keith Hiscock, Rohan Holt,
James Hrynyshyn, Atsushi Ishirnatsu, Emma Jackson, Greg
Jenkins, David Samuel Johnson, Matt Johnson, Mandy
Joye, Johanna Junback, Paul Kay, Gunter Kirst, Christo-
pher Krembs, Christoph Kuhne, HaITi Kuosa, Ruben Lara,
Chris Leakey, Eva Leu, Lewis LeVay, Alan Longhurst, Ian
Lucas, Ian Macintyre, Michal Mafias, Sophie McCully, lain
McGaw, Jan Michels, Peter Miller, Craig Mills, Daniel Mos-
quin, NASA, Simon Neill, NOM, Ylva Olsen, Stathys Papad-
imitriou, James Perrins, Lasse Pettersson, Jarone Pinhassi,
Lubas Polerecky, Joao Quaresma, Ivor Rees, Marcus Reck-
ermann, David Roberts, Riccardo Rodolfo-Metalpa, Craig
Rose, Royal Society for the Protection of Birds, George
Russell, SAHFOS, Bill Sanderson, Ricardo Serrao Santos,
Sedgewick Geology Museum Cambridge University, Sig-
rid Schiel, Shedd Aquarium, Sir Alistair Hardy Foundation
for Ocean Science, Mariano Sironi, Smithsonian Institute,
Wayne P. Sousa, South Australian Research and Develop-
ment Institute, Michael Stachowitsch, Kare Telnes, The
Hawaii Ocean Time Series Programme, Toru Takita, Jim
Treasurer, Andreas Trepte, Paul Tucker, Tuna Boat Own-
ers of South Australia!Australia and Fishing Management
Authority, U.S. Fish and Wildlife Service, Katrien van Lan-
deghem, Dolors Vaque, AnoukVerheyden, Amanda Vincent
(Project Seahorse), Janet Voight, Stephen C Votier, Tom
Webb, WHO! Graphics, Alan D. Wilson, Keith Wilson, Rory
Wilson, Matthew Witt, Richard Woodcock, Boris Worm,
Jeremy Young, Kakani Katija Young. The opening quote is
from an article by Professor G.E. Fogg who died in 2005.
The authors are grateful to the family of Professor Fogg for
permission to reproduce his thoughts that remain as rel-
evant as ever.
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Outline Contents

1 Patterns in the Marine Environment 1

Part 1 PROCESSES

2 Primary Production Processes 33

3 Microbial Ecology: Production and the Decomposition
of Organic Material 89
4 Secondary Production 126

Part 2 SYSTEMS

5 Estuaries 143
6 Rocky and Sandy Shores 172
7 Pelagic Ecosystems 194
8 Continental Shelf Seabed 217
9 The Deep Sea 251
10 Mangrove Forests and Seagrass Meadows 277
11 Coral Reefs 305
12 Polar Regions 325

Part 3 IMPACTS

13 Fisheries 357
14 Aquaculture 377
15 Disturbance, Pollution, and Climate Change 401
16 Conservation 429

References 450
Weblinks 485
Index 489
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Detailed Contents

1 Patterns in the Marine Environment I

1.1 Introduction I
1.2 Biogeography 9
1.3 Biodiversity 15
1.4 Abundance and size 23
Further reading 29

Part 1 PROCESSES
2 Primary Production Processes 33
2.1 Introduction 33
2.2 Photosynthesis 36
2.3 Respiration 42
2.4 Heterotrophic metabolism 43
2.5 Light in water 44
2.6 Light and photosynthesis 46
2.7 Supply of inorganic nutrients 49
2.8 The main limiting nutrients for growth 53
2.9 Algal growth 64
2.10 Seasonal trends in primary production 69
2.11 Global trend in primary production 69
2.12 Primary production in seaweeds 76
2.13 Measurement of primary production 78
Further reading 87
3 Microbial Ecology: Production and the Decomposition of Organic
Material 89
3.1 Introduction 89
3.2 The microbial powerhouse 89
3.3 The ecological context in which the marine microbes are embedded 91
3.4 The decomposition process 93
3.5 Key organism groups in the oceanic microbial food webs 97
3.6 The dynamics of bacterial growth and its measurement 115
3.7 The seasonal cycle of production and consumption 118
3.8 Oceanic microbes in global carbon and nutrient cycles 123
Further reading 125
4 Secondary Production 126
4.1 Introduction 126
4.2 Measuring secondary production 129
4.3 Drivers of secondary production 134
4.4 Size structuring in marine food-webs 136
Detailed Contents

4.5 Human impacts on secondary production 136

Further reading 140

Part 2 SYSTEMS
5 Estuaries 143
5.1 Introduction 143
5.2 Estuarine organisms 151
5.3 Productivity and food webs 159
5.4 Diversity patterns in estuaries 165
5.5 Other 'brackish-water' systems 168
Further reading 171
6 Rocky and Sandy Shores 172
6.1 Introduction 172
6.2 What is the shore? 173
6.3 Environmental gradients and the shore 174
6.4 Causes of zonation 179
6.5 The organization of shore communities 181
6.6 The shore network 190
6.7 The future of rocky and sandy shores 192
Further reading 193
7 Pelagic Ecosystems 194
7.1 Introduction 194
7.2 Definitions and environmental features 195
7.3 Pelagic inhabitants: consequences of size 198
7.4 Temporal and spatial variability in pelagic ecosystems 200
7.5 Sampling the open ocean 208
7.6 Pelagic fisheries 212
7.7 Regime shifts in pelagic marine ecosystems 213
7.8 The future for pelagic marine ecosystems 214
Further reading 216
8 Continental Shelf Seabed 217
8.1 Introduction 217
8.2 Definitions and environmental features 218
8.3 The seabed habitat and biota 224
8.4 Functional roles of the biota 231
8.5 Food webs in shelf systems 235
8.6 Characterization of seabed communities 239
8.7 Specific habitats 241
Further reading 250
9 The Deep Sea 251
9.1 Introduction 251
9.2 Definitions and environmental features 252
 Detailed Contents
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9.3 Food supply to the deep sea 260

9.4 The organisms of the deep sea 263
9.5 Hydrothermal vents - islands in the deep sea 271
Further reading 275
10 Mangrove Forests and Seagrass Meadows 277
10.1 Introduction 277
10.2 Mangrove forests 278
10.3 Seagrass meadows 290
Further reading 304
11 Coral Reefs 305
11.1 Introduction 305
11.2 Reef development and distribution 305
11.3 Corals and coral communities 309
11.4 Coral reef productivity and food chains 311
11.5 Reef fauna 313
11.6 Threats to coral reefs 314
11.7 Reef growth and bioerosion 318
11.8 Dynamics of reef animals 320
11.9 Reefs and human society 322
Further reading 323
12 Polar Regions 325
12.1 Introduction 325
12.2 What is pack ice? 329
12.3 Arctic vs Antarctic pack ice 331
12.4 Life in a block of ice 332
12.5 Sea-ice edges 337
12.6 Polar benthos 341
12.7 Polar bentho-pelagic coupling 343
12.8 Endemism in polar benthos 343
12.9 Gigantism in polar waters 344
12.10 Birds and mammals 345
Further reading 352

Part 3 IMPACTS
13 Fisheries 357
13.1 Introduction 357
13.2 Global fisheries 357
13.3 Fish production 361
13.4 Fished species and their fisheries 361
13.5 Fish population biology 362
13.6 Fishing methods 363
13.7 Fish stock assessment 366
13.8 The management process 368
13.9 Environmental impacts of fishing 370
Detailed Contents

13.10 Ecosystem-based fishery management 375

13.11 The future of fisheries 376
Further reading 376

14 Aquaculture 377
14.1 Introduction 377
14.2 Aquaculture past and present 378
14.3 How do we produce food from the sea? 381
14.4 What is cultivated and where? 383
14.5 Food requirements and constraints 385
14.6 The role of biotechnology 386
14.7 Negative effects of biotechnology 386
14.8 Cultivation systems 387
14.9 Cultivation of fish in cages 387
14.10 Cage cultivation: a lousy system? 389
14.11 Breaking away from the coastal margin 391
14.12 Shrimp cultivation: the gold rush 393
14.13 Shrimp farming and mangroves 394
14.14 Cultivation of molluscs 395
14.15 Ranching at sea 397
14.16 A conservation role for aquaculture? 398
Further reading 400

15 Disturbance, Pollution, and Climate Change 401

15.1 Introduction 401
15.2 Ecological role of disturbance 402
15.3 Measuring the effects of human activities 406
15.4 Agents of change 413
15.5 Climate change 421
15.6 Interaction of multiple factors 426
Further reading 428

16 Conservation 429
16.1 Introduction 429
16.2 Why conserve? 431
16.3 What to conserve 432
16.4 Economics of conservation 435
16.5 Conservation policy and legislation 439
16.6 Conservation in action 442
16.7 Evidence-based conservation 447
16.8 Life-cycle analysis 448
16.9 The future 448
Further reading 449

References 450
Weblinks 485
Index 489
Patterns in the Marine
Environment
Chapter Summary
Most space for li fe on Earth is in the vast oceans and seas.
Li fe began in the oceans and remained confined to thi s
environment for hund reds of mi llions of years. Most maj or
gro ups (ph yla) of animals never left it. The wid e expanse
of th e oceanscape changes dramati cally, from und ersea
mountain ranges to sedi ment plains and coral reefs, to for-
ests of kelp. Pattern s of organisms, so obvious at th e shore,
are also evide nt from the po les to the trop ics, from coasts
to ocean cent res, from th e shallows to the deep abyss,
1.1 Introduction
Humans are a land-living species and consequently most
familiar w it h the terrestrial environme nt, yet the Earth is a
blue planet and the oceans cover > 70% of its surface . Close
to the continents this aquatic ecosystem takes the form of
shallow seas just a few hundred metres deep known as the
continental shelf. However, around Antarctica the mass
of the huge (3-km thick) icecap has depressed the shelf to
be as deep as 1000 m in places. Most of the oceanic habitat
(and 51% of the earth's surface) is nearly 4000 m deep.
This three-dimensional environme nt is populated through-
out its depth by many organisms. The steep rises up to the
continental shelf contrast with the large sedime nt-covered
basins that span tens of thousands of square kilome tres,
broken only by the undersea mountain ranges of mid-
ocean ridges. At these locations oceanic crust is formed
and gradually moves outwards, pushing continents apart,
and eventually disappears down beneath continental crust,
forming deep oceanic trenches. Considering its volume ,
and from millions of years ago to th e present day. Pat-
terns occur in species' richness, abundance, ancientness, or
size, all of w hich are indicators of powerful changes o n th e
planet surfac e in t ime and space. Oceans have wid ened or
been co mpressed, risen and fallen , heated and cool ed, and
remain dyna mic places; most will have changed drastically
in j ust the lifes pan of the reader of this book. Examining
som e of the maj or pattern s in organisms and their bio logy
gives a strong insight into the processes that determine
success and evol uti on of li fe on Earth.
the vast majority (c.99%) of the Earth's habitat is marine,
where most major types of animal (phyla) have evolved
and continue to live exclusively. Most of the vast water
column and seabed (ben thic) habitat remain unobserved
by human eyes. The first biological samples were only col-
lected from the continental shelf of the Amundsen Sea
0
(whic h spans 40 longitude- equivalent to the Med iter-
ranean) in 2008. New species are still routinely found in
deep-sea samples and even some of the larger animals on
Eart h which live there, megamouth sharks and giant squid,
have only recently been seen alive in their natural habitat.
Our impoverished knowledge of the ocean 's inhabitants
is emphasized by the fact that it is not just new species
that are described , but that even some of those that are
high-profile and common , such as the crown-of-thorns
starfish, now appear to be several species (like giraffes
on land). Furthermore, entirely new classes or phyla (the
highest taxonomic levels of animal types) have been dis-
covered in just the last couple of decades.
 Chapter 1 Patterns in the Marine Environment
Box 1.1: A new phylum
In 1995 an entire new phylum of tiny animals, the
Cycliopho ra, was repo rted from a discovery two
years earlier. As it is only 350 u rn in size and super-
ficially resembles individuals of several other phyla
of small animals (Gastrotricha, Rotifera, and Ento-
procta) , it could be considered unsurprisi ng that
such animals are still being discovered. Surprisingly,
though, the single species (Symbion pandora) lives
on the mouthparts of Nephrops norvegicus-a very
common, well studied, and widely consu med species,
ofte n referred to as scampi. S. pandora, or the 'Pan-
dora', attaches to its host using a sucker and suspen-
sion feeds on particles in the water, a small parasitic
male (whose sole purpose seems to be for breedi ng)
is also shown attached in the picture below.
Feeding tentodes - - - -
'------ Anached male
'------ Stalk
-/--7"----- Sucker
Standing at the edge of a forest looking out over a prai-
rie, lake, or into the tree canopy, it is easy to see how
fragmented the land can be. Furthermore, even a simple
climb up a mountain can reveal altitudinal changes and,
though few have experienced it, most people understand
that polar regions are deserts compared to the generally
species-rich tropics. In contrast, the water column and wide
ocean basins might be envisaged as fairly monotonous, uni-
form ecosystems. However, there are many features that
punctuate them abruptly or gradually into many different
environme nts . Changes in time, topography, chemis try,
and oceanography allow for the development of patterns
across a wide range of scales in time and space, and form
the subject of this first chapter and are themes that reoccur
throughout this book.
1.1.1 Zonation
Patterns in the marine environme nt are often beyond our
immediate perception; we cannot always see them. Often,
patterns are only revealed through sampling and subse-
quent interpretation. The number and size of samples col-
lected and the type of equipme nt used will have a profound
effect on what is found. Strong differences in opinion exist
about even the most basic marine biotic patterns, each
defined by evidence from a discrete set of samples (see also
sampling in Chapter 8) . In many respects, patterns in the
sea resemble those on land; for example, at a large scale
along grad ients of solar radiation (latitudinal gradients),
altitudinal (which in the marine environment is depth, thus
bathymetry), from the coast to ocean/continent centres,
and from young to old areas (e.g. from the mid-Atlantic
ridge (new) to the far eastern or western Atlantic sea-floor
(oldest)) . In the shallowest parts of the sea there are plenty
of places where the type or nature of the organisms changes
over tens of centimetres or metres, which we term zona-
tion (Chapter 6). In warm tropical waters, the type and
dominance of corals changes quickly with depth (Chapter
11). In polar seas the abundance and richness of marine
life alters equally sharply in response to decreasing physi-
cal disturbance by floating icebergs that scour the seabed
(Chapter 12). In certain types of environment, such as estu-
aries (Chapter 5) , rapid changes in biological constituents
occur along the length of the estuary in response to a suite
of changing environme ntal vari ables; patterns that are
repeated at virtually all latitudes. Zonation is most appar-
ent where the land meets the sea and it is here that it has
been studied in most detail (Fig. 1.la). Zonation is not just
driven by tolerance to physical conditions (though this is
most important at the high shore level) . Connell's (1961a,
1961b) wo rk on barnacles demonstrated that interspecific
competition and differential predation pressures strongly
influence the location where species survive. In temper-
ate regions across the globe different species and colours
of algae and lichens indicate the grad ient of immersion on
the lower and upper regions of the shore. Shore zonation
is equally apparent in some muddy shores in changing salt-
marsh vegetation or, at tropical latitudes, in mangrove trees
and their associated fauna. Only towards the polar regions
does shore zonation become increasingly constrained and
ultimately disappear altogether at very high latitudes (Fig.
1.1b). At high polar latitudes (Fig. 1.1c), very few organ-
isms can survive the constant abrasion by floating ice dur-
ing the summe r, coupled with encaseme nt in winter ice
 1.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

as the sea surface freezes . Conversely this phenomenon
causes zonation in the sublittoral zone as the frequency of
ice scour (Chapter 12) decreases with depth and distance
from the shore.
In many ways, patterns in the sea resemble those on
land with large-scale gradients in solar radiation , altitude
(depth), and geological age.
Zonation is driven at the land/sea interface by a com-
bination of physiolog ical tolerance and competition for
space and predation pressure. See Chapter 6 for a dia-
grammatic explanation of different zones in the intertidal
and near-shore zone.
The littoral zone has gradients of immersion, exposure,
shade, roughness (rugosity), topography, and many others.
With such a variety of micro-environmental variation it is
easy to understand why the littoral zone is species' rich. Spe-
cies specialize in response to different tolerances. exposure,
food, and feeding methods (as well as to other factors), so
there is potential for many species to co-occur when many
environmental factors interact. Examples of this on a rocky
shore include those species specialized to living on exposed
rock face, in crevices, on the undersides or tops of boulders.
overhangs, and in pools. But what about the variability of
conditions away from the seabed, i.e, in the water column?
In this seemingly uniform environment. many species also
occur in close proximity. Hutchinson (1961) referred to this
as the 'paradox of the plankton' (see Current Focus box in

40 50 60 70
Latitude "S

(el

Figure 1.1 Shore zonation. (a) Bands of barnacles, algae, and mussels in Tierra del Fuego (54°5), southern Argentina.
(b) Intensity of zonation in relation to latitude and the position of t he Polar Frontal Zone (PFZ). Diagram is a schematic
suggesting manner of change of intensity of zonation based on strength of littoral macrobiota patterns at sites at
latitudes ind icated by (1) Tristan da Cunha, (2) Gough Island, (3) Prince Edward Archipelago, (4) Falkland Islands, (S)
South Georgia, (6) Signy Island, (7) South Sandwich archipelago, (8) Haswell Island, (9) Adelaide Island, (10) Vestfold
Hills, (1 1) McMurdo Sound. (Sa) Is Tierra del Fuego, which is actually north of the PFZ. Adapted from Barnes &
Brockington (2003). (c) A denuded polar shore (Adelaide Island).
 Chapter 1 Patterns in the Marine Environment
Box 1.2: Determinants of zonation
patterns
Sessile, arm o ured, ci rri ped crustaceans (com monly
known as barnacles) are very abun dant and are even
the dom inant organisms on hard surfaces on temper-
ate rocky shores. Connell (19 61 a) studied the dis-
tribut ion of one speci es (Chtham alu5 stellatus (see
fig ure, below left), w hich occu rs in a dist inct vertical
zone. Relative to most other marine organisms in the
littoral, this zone is high up, so C. stellatus ind ividu-
als have to wit hstand high ly variable temperat ures,
dessicati on, and longe r periods wi t hou t foo d. This
zone is not , however, of th eir choosing. C. stellatus
larv ae settle cons iderably be low (and even above)
this level on t he shore. Other factors, principally com -
petition w ith oth er organisms, such as the barnacle
Semibalanus balanoides (below right) , red uce the
surv ival of recruits on t he lower shore to near zero.
The more heavily armoured plates of S. balanoides
crush C. stellatus individ uals w hen space becomes
limit ing. The compet itors (and many of the preda-
tors) of C. stellatus fi nd the harsh con ditions hig her
up on t he shore too d ifficult to endure so only at this
level can C. stellatus prosper.
Chapter 7). The plankton contains many permanent repre-
sentatives, but also many transient constituents, such as the
larvae of seabed animals (b ent h os) . Larvae of individual
species may diffe r in their time of release. residence time in
the plankton, whet her they are feeding (p la nktotroph ic) ,
or have their own yolk sacs (lecithotrophic), and behav-
iour. The water column, like the land and seabed, has many
sh arply changing physical features that effectively form
environmental barriers that constrain the organisms that
live there (Chapters 2, 3, and 7) .
Benthic organisms are those that live in , on , or are
anchored to the seabed , whereas those that move freely
in the water column are known as pelagic organisms.
1.1.2 Oceanography
On a larger scale the water column has a strong pattern of
zonation that occurs across its full depth range. similar to
that found in the littoral zone. Most importantly, in the top
few to 200 metres of the water column there is enough light
(during the day) fo r primary producers to photosynthesize,
termed the euphotic zone (Chapters 2 and 7) . As a result,
the top 100- 200 m of open ocean water and 1-50 m of
coastal water is a very different environment to that found
below. Of course, even w ithin the euphotic zone there is
a strong gradient of light intensity and wavelength with
depth. Beyond a depth of 1000 m (most ofthe world's ocean
volume) the ocean is effectively lightless, wit h a few small-
scale exceptions, such as the bioluminescence produced by
bacteria found in the light organs of deep-sea biota. Light
striking the surface of the marine environment also imparts
heat. thus the surface layers are the warmest and hence
have lower density than the cold water beneath. Globally
the temperature of deep water is relatively uniform at just
a few degrees Celsius, in contrast with shallower water
temperatures that fluctuate w ith latitude and season. In
the polar regions, surface water is near freezing point at
- 1.8So C in the winter, and just positive in summer. How-
ever, the water in polar regions is well mixed, as dense cold
water sinks and wave height and wind speed are greatest at
a latitude of 50- 60" (Fig. 1.2). Moving away from the polar
regions, wit h a few exceptions, such as regions of upwell-
ing, the global ocean is stratified into a warm upper layer, a
rapidly cooling zone. and a lower cold zone. The n ature of
thermoclines ch anges from place to place but in general
the thermoclines in the tropics are more than 10°C warmer
than those in temperate regions, and they are permanent
rather than seasonal. Such stratification is important as
organisms require nutrients and minerals, as well as light
and respiratory gases. Thus away from permanently mixed
areas, such as polar seas or upwelling zones, the surface
layers of the sea also have strong changes in molecules used
or produced by organ isms, such as nitrates. Locally other
gradients, e.g. haloclines (salin ity) or pycnoclines (dens-
ity), may also stratify water layers. The salinity of seawater
is typically about 35 psu . Generally, changes in salinity that
occur with eit her latitude or longitude across oceans are
small, but are a little greater in the tropics (due to increased
evapora tion of surface water) and lower close to continents
and in the Arctic due to the influence of greater fresh water
run-off (Chapter 5).
 1.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Thermoclines are a vertical zone of rapid temperature

change in t he water column . Haloclines occur where two Table 1.1 Example of changes in the marine
water masses of different salinity interact, e.g. in an estu- environment wit h time-scale.
ary or towards the head of a fjord , where freshwater
meets seawater. Both changes in salinity and tempera-
ture will affect water density. Time-scale Feature

Hours High to low tides

psu-practical salinity units (see 5.1.4.).
Days Spring to neap tides
There are many features that partition the ocean environ- Months Seasonal temperature/ salinity/
ment, and the positions of continents, islands, and sub- currents
surface marine mountain chains form obvious physical
Years EI Nino Southern Oscillation
barriers. In the open ocean, differences in water density,
currents, and fronts provide the conditions that lead to dis- Decades Climate warming, ice sheet retreat
tinct water m asses. Centuries to Ice ages, Milankovitch cycles,
millennia sea-level fluctuations, sea floo r
See Chapter 9 to understand more about the physical spreading
and biological processes around sea mounts and Chap-
ter 7 to understand how fronts form in the ocean .

Although current d irection and velocity of water m asses II

(.)
and patterns of wind across the globe are complex, there Atlantic
10
are general large-scale patterns th at occur, m ost obviously 0 Podfic
1-
• lrdlun
in water flow. Most deep (seabed) water is derived from
the Southern Ocean . Cooled dense w ater (termed Antarc- -
.~
c

~
• Mean global

tic Bottom Water, AABW) sinks in the Southern Ocean and

flows away from Ant arctica, well into t he northern hemi- -- ,
,S

••~
sphere abyssal regions. There m ay be seve ral curren ts
that occur at diffe rent depths betwee n the deep AABW
'. c

0
0
•c
a nd surface water. For example , cool north ern water
0
c
e
•
~

flows sout hwards in the mid-region of the water colum n 5

in the Atlantic. At the sea surface, the world's oceans are 700 N 5~N 300 N lOoN ,., W5 70°$

dom inated by a series of gyres rotating clockwise in the Latitude(degre&s)

northern hemisphere and ant iclockw ise in the southern 5r.:-:-- - - - - - - - - - - - - - -----,
(b)
hemisphere. Where these meet in the equ atorial region,
strong curren ts flowin g westwa rds occur (as well as
smaller countercurrents flowing eas twards). The current
system of t he Southern Ocea n is dom inated by the circum -
polar curre nt, wh ich flows around the continent in a clock-
w ise direction. This is bot h the fastest m ajor curre nt in the t
world (flowing at 10 em s') and the only one that spans -a
i
the entire water column from surface to the abyssal seabed •
•
o
•
(5 km down) . Surface currents are particularly important J!
in mixing the water layers, which is a powerful agent t hat
counters stratification, at least in the sh allower layers of
the water column . As well as these large- and small-scale Latitude(degre&s)

spat ial variations, the m arine environm ent changes over a Figure 1.2 The di stribution of mean wind speed and
variety of time-scales (Ta ble 1.1 ). wave action in the marine environment with ocean basin
and latitude. Plotted from data from Bentamy et al. 1996.
 Chapter 1 Patterns in the Marine Environment
Surface currents are particularly important in mixing
the water layers due to the frictional stress that occurs
between two moving bodies of water (also see Chapter
8 to understand laminar flow and boundary layer effects
of flow at the seabed and how this affects biology).
1.1.3 Climate
There is now much concern about accelerating climate
change and the extent to which human activities are linked
to this phenomenon (Chapter 14). The climate ofthe Earth,
however, has been in a state of constant change; only the
magnitude of the rate of change has varied with time (Fig.
1.3) . The most familiar environmental variable associated
with climate is temperature. While air or land temperatures
fluctuate more dramatically, sea surface temperature (SSn
changes are more subtle due to the huge volume and high
latent heat of water, which give it a strong buffering effect.
It is important to understand what a change in t he rate of
change means. The following is illust rat ive only: if global
ocean temperatures were increasing at a rate of 0.1 °C
every 10 years then th is is a constant rate of change;
however, if global ocean temperature changed O.1 °C from
year 1-10 and then 0.2°C from year 11-20, this is an
increasing mag nitude of rate of change. In other words
the world ocean would be heating up faste r and faster.
When global temperatures are high, sea-levels rise through
thermal expansion and the melting of ice. There is great
connectivity between many environmental variables, such
that when SSTs rise. other environmental parameters
change concomitantly. For example. warmer water is able
to hold less gas and hence the oxygen needed for respira-
tion (Chapter 14) . At present. icecaps occur over the two
polar regions. which is a relatively unusual condition in
palaeontological time-scales. Ice area expansions occur
every winter (the geographical extent, but not the volume,
of Antarctic sea ice doubles from summer to winter) . On a
very much larger scale, each ice age spreads the icecap to
lower latitudes from the poles, then retreats in interglacial
periods. The rise and fall of sea-level has clear and impor-
tant implications forthe marine habitat (Fig. 1.4) : the shal-
low sloping continental shelf is one of the most important
habitats formost organisms with 90%ofthe World's marine
primary production (Jennings & Kaiser 1998) . The extent
of the continental shelf changes considerably with just a
50 m change in mean global sea-level (Chapters 5 and 8) .
Changes in ice extent, which occur simultaneously with
those in sea-level, are also important. literally scraping
away entire habitats and thereby open up new space for
colonists.
20 , -- - - - - - - - - - - - - - ---,
--,\0 -40 - 20 0
Millions of yeors ogo
Figure 1.3 Sea temperature change with time in the
Southern Ocean (Adapted from Clarke et al. 1992).
The effects of sea-level rise inevitably mean that near-
shore communit ies and continental-shelf comm unities
are the most recently establ ished when measured in
geological time-scales.
Strong signals of climate change have been found in the
last century, particularly from 1916 to 1945 and from
1976 to the present. Earth's mean surface air tempera-
ture has increased by 0.6°C in a century. but some regions.
such as the Arctic and west Antarctic air and soil tempera-
tures. have warmed more than this in a decade (Walther
et al. 2002) . Most recently, significant climate-related sea
temperature increases have been measured in the Scotia
and Bellingshausen seas of West Antarctica (Chapter 12) .
There have. however, been drastic and rapid changes in
the Earth's surface temperature before. even in the sea.
These changes occurred in response to massive methane
clathrate releases from below the seabed, major volcanic
events. and after meteorite collisions (such as that near
the Yucatan at the end of the Cretaceous period) (see Box
1.3) . Other prominent aspects of recent climate change
have included increasing CO2 levels and changes in strato-
spheric ozone thickness. The first of these is strongly
related to temperature changes through heat trapping and
is referred to as 'the greenhouse effect'. Seasonal thinning
of the upper atmosphere ozone (ozone holes) permits
increased penetration of the ultraviolet wavelengths of
light with their potential damaging effects to organisms.
UV penetration of water is limited to just a few metres of
the sea surface. so although potentially a serious issue in
terrestrial, littoral, and very shallow aquatic habitats. it
does not affect the majority of the volume of the global
ocean environment. Aside from a strong signal of season-
ality in the oceans and climate change. there are various
other longer term but cyclical events such as Milankovitch
cycles (which concern solar activity. such as solar flares)
and the El Niiio Southern Oscillation (ENSO) . ENSO has
been the subject of considerable scientific discussion after
 1.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

(0)
250
200
150 ~~ <:
m 100
50
o
v
r\JV'V\JI y,v
r
1~
HI
65 60 55 50 45 40 35 30 25 20 15 10 5 o
Me

(b)

Figure 1.4 Sea level change with time. Global sea level change from the Mesozoic to present (a) and the coastline of
NW Europe (b) and Australasia (c) c.18 thousand years ago (in light green) and now (in dark green).

major events in 1972, 1982/1 983, and the early 1990s. An

ENSO event centres around raised equatorial Pacific sea
surface temperatures, raised coastal rainfall, and flood-
ing in the western Americas but is also associated with
knock-on global climatic anomalies. One example of such
an anomaly is the weakening of ocean cu rrents such as
the Gulf Stream (which takes warm water to north-west-
ern Eu ro pe) , resulting in colder climatic cond iti ons and
changes in rainfall patterns. The phenomenon of ENSO
has be en recorded for more than a hundred ye ars and dis-
crete events h ave been traced back ne arly 500 years. ENSO
a nd ot her ele men ts of climate change, as well as physi-
cal and chem ical oceanography, h ave a strong influence
on the magnitude of productivity in the oceans (below) .
This has consequences for higher predators, such as fish,
mamm als, and seabirds, as well as fisheries (Grant ham et
al. 2004).
Although the penetration of UV light affects only the
upper few metres of seawater, it has the potential to
adversely affect fish larvae and other biota that form
the shallow nekton and neuston (i.e. those animals that
live at the sea/air interface, such as the Portuguese Man
o'War (Physalia physalis)).
Box 1.3: Methane clathrate
Methane clathrate is a type of ice that has met hane
(CH 3 ) bound wi thin its crystalli ne struct ure. Build-
ups of this hydrate are probably created by gases
moving along geological fault lines where they crys-
tallize on mixi ng wi th col d water. Methane clathrate
has long been thought to be common in the outer
solar system but more recent ly it has been discov-
ered in considerable quantities below some oceanic
sediments. This is importantfor several reasons: first,
it is a maj or source of fossil fuel (maybe > 9 0 % of
nat ural gas reserves) and, second, release of overly-
ing pressure on these deposi ts could result in large-
scale discharges of methane through the ocean into
the at mosphere. Such releases are thought to have
occurred rapidly, on various occasions and may have
been responsible fo r sudd en clim ate w arming. For
example, some of t he rapid increases in the tem pera-
ture of the Southern Ocean (Fig. 1.3) seem li kely
to be caused by methane clathrate chang ing from
storage in ice crystals to atmospheric gas and then
having a profound effect as a greenho use gas.
 Chapter 1 Patterns in the Marine Environment

1.1.4 Productivity
Unlike on land, true plants generate little of global marine
production (except in intertidal saltmarshes, seagrass
meadows, and mangrove swamps) . In cool, shallow,
coastal waters, macroalgae such as subtidal kelps, or inter-
tidal green, brown, and red macroalgae, are highly pro-
ductive and can grow rapidly (Fig . 1.5). The productivity
of the sea mostly depends on microscopic free-living, sin-
gle-celled algae collectively referred to as phytoplankton
(see Chapter 2) . Although phytoplankton are individual
(or aggregations of) single cells, they vary in size from
large (200-20 11m diameter), diatoms (microplankton) to
tiny (2-D.2I1m diameter) bacteria (picop la n kt on) or even
smaller cells (see Chapters 2 and 3) . In tropical coral reef
systems much of the primary productivity is associated
with microscopic algae that occur as symbionts within
the tissues of animals, such as corals (Chapter 11) . Pri-
mary productivity in the marine environment varies over
several orders of magnitude from grams of carbon rrr? d?
to just tens of mg carbon m-2 do' . Total annual global phy-
toplankton primary productivity is patchy in space but is
typically highest around continental shelves and lowest
in the centre of ocean gyres (Fig. 1.6) (Chapter 2). Sec-
ondary production (mainly by zooplankton Fig. 1.5) is
linked directly to phytoplankton production though often
appears to have a higher biomass because the turnover of
primary productivity is 50 rapid.

Figure 1.5 Macro- and micro-phytoplankton and zooplankton. Examples of macro-primary producers are subtidal kelp
(a), intertidal red and brown macrophytes (b), and a seagrass meadow (c). Examples of micro-primary producers are a
diatom (Coconeis) (d), a silico-flagellate (e), and a radiolarian (t). Foraminiferans are protoctist (protist) micro-consumers
(g). Examples of zooplankton (h) include a jellyfish, a polychaete worm, a euphausid crustacean, and a ctenophore
(comb jelly), and various invertebrate larvae (i). Photographs: (a, b, and c) David Barnes, (d and e) Sandra Wilks, British
Antarctic Survey, (I) Claire Allen, British Antarctic Survey, (g) Mark Williams, (h) Simon Brockington, (i) David Bowden.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
_ > 500 _ _ 1250-500 1_ _1100-250
Figure 1.6 Patterns of annual phytoplankton productivity in the global oceanic environment expressed as 9
cm-2 year" (adapted from Barnes & Hughes 1999).
Turnover describes the process whereby cells are eaten
or die almost as quickly as new ones are produced.
The rate of primary production varies along gradients of
light and nutrient availability. As a result, productivity var-
ies across the tropics, temperate, and polar regions, with
depth, with the proximity to the coast, and to other features
such as upwellings. Pelagic productivity is typically more
than an order ofmagnitude lower than for benthic systems.
The majority of benthic production is, however, restricted
to only a tiny proportion of the global marine environment
on the continental shelf (Chapter 8). The lowest levels of
total annual productivity are concentrated around the cen-
tre of oceanic gyres such as the Pacific Ocean basins north
and south of the equator. Seasonally, high productivity is
associated with much of the shallow polar or high-temper-
ate coastline and high annual productivity is particularly
notable across the tropics of much of the coastal Indo-West
Pacific. Patterns of high and low productivity have a largely
predictable distribution and are likely to be a major cause
in the way other marine organisms are arranged globally.
The process of primary production is dealt with in detail in
Chapters 2 and 3.
Patterns of high and low productivity have a largely pre-
dictable distribution and are likely to be a major cause in
the way other marine organisms are arranged globally.
This first chapter examines large-scale patterns in the dis-
tribution of marine organisms. The emerging discipline
of macro-ecology has grown to quantify. analyse, and
1.2 Biogeography
__ I <100
explain the patterns of organism groups on large scales
(Brown 1995) . Biogeography is the science of geographi-
cal and historical relationships between and among differ-
ent organisms (taxa), and is a natural starting point for the
examination of large-scale patterns in the marine environ-
ment. Later chapters consider patterns and processes that
occur in specific systems.
1.2 Biogeography
Biogeography explores the distribution of species, how
groupings of such species form distinct ecosystems, and
their geographical limits. Individual species (and in some
cases higher taxa) each occur across a certain geographic
range. Under experimental conditions. many species can
endure environmental conditions (e.g. temperature. salin-
ity, sedimentation. and pressure) far in excess of the con-
ditions in which their populations naturally are found .
There are many reasons why species are not found across
the entire range of their physiological tolerance. At the
edge of their geographical range. species are much more
susceptible to local extinctions that occur with changing
environmental conditions. hence the presence of a species
along a gradient may simply reflect the time since the last
local extinction event. At a larger scale, there is evidence
in some groups of animals that the geographic ranges of
species alter along major gradients. and ultimately influ-
ence biodiversity (Box 1.4). Species and higher taxa tend
to form characteristic groupings by regions around the
globe, as well as in particular habitats. The major theme
 Chapter 1 Patterns in the Marine Environment

of biogeography has been to identify and characterize the
geographic groupings of species and the biogeochemical
conditions that make them differ (Longhurst 2006) . Key to
the advancement of biogeography h as been the application
of molecular genetics to elucidate genetic variability and
relationships in space (see Technique application).
At the edge of their geographical range , species are
much more susceptible to local extinctions that occur
with changing environmental conditions.
Biogeography has been of interest to both terrestrial and
marine biologists for more than a century, since early bota-
nists began to match vegetation structures to regional cli-
mate types. A succession of pioneering botanists classified
groupings of vegetation structures by climate into a series
of life zones, biomes, or eco-regions according to environ-
mental characteristics such as precipitation, temperature,
and humidity. Similar advances were not easy in the m arine
environment whe re mismatches in different as pects of bio-
geograph ic knowledge occurred, even in the most acces-
sible systems. In the last few decades, underwater scientific
instrumentation, advances in marine sampling platforms
(ships and autonomous underwater vehicles), and analysis
of high-quality oceanographic data (Coastal Zone Colour
Scanner, CZCS) from the NIMBUS satellite have revolution-
ized our understanding of ocean surface biogeochemistry.
In terms of marine climate, the global m arine enviro nment
has been cons idered to consist of three broad domains:
polar, temperate, and tropical. In contrast, the early zoolo-
gists divided the globe into six broad realms in terms of their
fauna: Nearctic (North America) and the sim ilar Palearctic
(most of Euras ia and Northwest Africa ), Neotropical (Cen-
tral and South America) , Ethiopian (Africa), Oriental, and
Australian . Boundaries and subdivisions have gone through
many subsequent refinements. Although designed around
terrestrial biology, theories of island biogeography repre-
sent a good introduction to many of the important factors
that determine the distributions of organisms.
1.2.1 Island biogeography
The global terrestrial enviro nment is formed of a series
of islands that vary in size, age, isolation, nature, and his-
tory. The fauna of islands reflects these factors. The larger,
older, and closer to a continent an island is, the greater the

Box 1.4: Variability in latitudinal ranges of North American

gastropod mollusc species
Each species occurs across a certain range of latitude (see figu re). Roy et al. (1998) compared the number of gas-
tropod species with latitude along the Pacific (blue line) and Atlantic (red li ne) coasts of North America (i nsert plot) .
They then investigated whether these species' richness patterns could be explained by species at lower latitude having
narrower latitudi nal ranges (Rapoport's rule). They found, however, no obvious link and, furthermore, latitudinal ranges
of many trop ical gastropod molluscs were higher than those at high latitudes. Roy et al.'s (1998) study was the most
serious test of Rapoport's rule and one of the strongest data sets for latitudinal ranges of species for any marine group.

1000

60 ••
.-
800

600
0

"--
~
~
~

= 50 -
z
0: 400
E
0

200
~
=

~
c
0

0
c
- 40
0
ON ION 20N 30N 40N SON
latitude (degrees)
60N IO N SO N
0

0
c
0
-
.~

30
~
~

'"
20

ON 10N 20 N JO N 40 N Sll N 60 N 70 N 80 N
Latitude Idegrees)

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
number of taxa present. MacArthur and Wilson's (1967)
theories of island biogeography explained many of these
concepts. Whether marine or terrestrial, animals or plants,
the number of species (S) (or higher taxa) increases pro-
portionally to the area of the island (A) according to the
Arrhenius relationship:
Log S = c + z (log A),
where the values of the constants are:
c = c.0.3 and z = c.0. 16.
Thus on a plot with log scales on both axes, the relation-
ship approximates to a straight line-shown, for example,
by plant numbers on Australian islands or even (approxi-
mately) for species on continents. At the other end of the
spatial scale a number ofauthors have immersed settlement
panels of various sizes into the sea and demonstrated simi-
1ar increases of species with area of these miniature islands
(see e.g, Jackson 1979) . There are a number of causes of
species-area relationships, such as higher numbers of
samples (the more samples you take the more species you
encounter). more habitats, immigration and extinction
rates, and greater ratios ofspeciation to extinction. Smaller
islands are less likely to be encountered by would-be colo-
nizers because they represent a smaller target than a larger
land mass (likewise younger islands represent a smaller tar-
get in time for potential colonizers) . Similarly, the more iso-
lated an island, the smaller the pool of organisms that are
capable of reaching it. A water- or airborne organism would
take a long time to reach Bouvet Island in the Southern
Ocean, which is thousands of kilometres from the nearest
land of any kind. Of course prevailing winds, currents, and
chance playa major role in determining which organisms
arrive. where and when, which in part explains why there
is often much 'noise' in species-area plots of sample data.
There are all sorts of islands in the marine environment
varying from enclosed coastal lagoons, sea lochs, and fjords
to seamounts or hydrothermal vents in deep water (Chap-
ter 9) . The same principals of colonization and dynamics
of fauna apply to these environments. However. species-
area relationships tend to be complicated by other factors :
some regions have richer regional species' pools than oth-
ers. For example, Jamaica contains many more species of
most organisms than the Falkland Islands, even though
their land masses are ofsimilar size and distance from their
adjacent continental land mass. Jamaica and the Falkland
Islands are situated in very different regions (Caribbean d .
Southern Atlantic Ocean), which explains the differences
we observe in their species' complement.
Island size, age, and isolation are important determin-
ants of species' richness.
1.2 Biogeography
1.2.2 Local versus regional patterns
Some regions are richer in taxa than others. Japanese
coastal waters are, for example, particularly rich in bra-
chiopods and the Antarctic continental shelves are rich in
sea spiders (pycnogonids) . Overall the Indo-West Pacific
region, in particular around Indonesia. has higher numbers
ofspecies of fish, corals, molluscs, and probably many other
marine animals than elsewhere. On land there are typically
more plant species (per unit area) in the neotropics than
in other tropical regions, which are in turn more speciose
than nearctic or palearctic regions. Thus small areas. orvol-
umes (though these are rarely measured). in species-rich
regions will contain more species than similar sized areas
in species-poor regions. So, in addition to effects such as
species-area relationships, there is typically a positive rela-
tionship between local and regional diversity. This relation-
ship is useful as it enables prediction ofchanges at one scale
from observations at another. To date, examples of this
regional local species relationship principally have been
from terrestrial systems (Caley & Schluter 1997) . In order
to appreciate the relationship of a local parameter with a
larger scale unit. the unit in question needs to be defined.
Although we have already considered a very brief history
of the partitioning of the terrestrial and marine realms into
smaller areas or units (1.2). it is appropriate to consider
this in more depth due to the importance of this issue to
biogeography.
Generally, there is a strong positive relationship between
local and regional diversity, although to date t his has
been demonstrated best in terrestrial systems.
1.2.3 Biomes, oceans, and provinces
Using a small set offactors, it is possible to predict a series of
community types or 'biomes' on land. Using high-resolution
CZCS images of phytoplankton 'greenness' (a proxy for the
biomass of a phytoplankton bloom), an analogous series of
biomes can be generated for the marine environment. Thus
four primary biomes are recognizable from characteristic
patterns of phytoplanktonic algal growth, the environ-
mental forcing agents (wind. currents). and fauna at other
trophic levels. Longhurst (2006) details these as the (1)
Trades, (2) Westerlies, (3) Polar, and (4) Coastal biomes.
These are all defined by the agent that determines the depth
of the mixed layer ofseawater: wind acting over large-scale
distances (Trades), local wind speed and light intensity
(Westerlies), surface-reduced salinity water (Polar), or a
complex of processes (Coastal) . With the exception of the
Trades biorne, all include several disjunetwater masses. For
example, the Polar biome occurs (at high latitude) in each
 Chapter 1 Patterns in the Marine Environment

hemisphere and can be split into Antarctic, North Atlantic,
and North Pacific secondary associated biomes.
The t rophic level of an organism in acommunitydescribes
its position in a foodweb relative to the organisms upon
which it preys and t he predators th at feed upon it (see
Chapter 4 and 7).
As biomes are defined largely on the basis of physical ocean-
ographic conditions a nd the response of phytoplankton, the
exact boundaries are prone to alter with seasonal, ENSO, or
other climatic alterations that have even longer cycles. The
extent and shape of biomes and their subdivision into prov-
inces are very much dependent on geographic positioning
ofcontinents, features ofcoastlines, and oceanic circulation
patterns. As coastlines and even oceanic frontal zones are
approximately fractal, a serial subdivision of units could be
argued as a valid concept, however. this would require pro-
gressively more and more detailed data from which to con-
struct them. The establishment of provinces has followed
similar biogeochemical steps to those for the designation of
biomes (climatology of mixed layer depth, water transpar-
ency, and surface nutrient status). but at a high resolution.
The designation of biomes and provinces is very useful for
examining many aspects of large-scale patterns in organ-
ism ecology and evolution (Fig. 1.7) . This is particularly
the case for the investigation of the relationship of species-
groupings in one area to those in others. One of the most
fundamental areas ofbiogeographic research is the study of
the degree of endemism. i.e, how many species (or h igher
taxa) are unique to a particular area?
The Trades, Westerlies, Polar, and Coastal biomes are all
defined by the environmental factors that determine the
depth of mixed layer of the water column.
The definition of provinces has followed similar biogeo-
chemical steps to those for the designation of biomes
(climatology of mixed layer depth, water transparency,
and surface nutrient status).
1.2.4 Endemism
At a global scale all species are endemic, at a whole-ocean
scale many taxa are likely to be endemic but decrease at
smaller spatial scales. Typically endemism is used in the
context of countries, archipelagos. or islands and seas,
but also between different sorts of organisms (e. g. while
all but one of the marine lizards in the Galapagos Islands
are endemic, less than 20% of the fish are endemic) . As

, PIGIWI ,PIG lEI

PNE(
WARM
PEQD

,PSG
SAIL

;:::~ "NG ~::::;:~ SST(

~-.I"";---1 '<-__--=SA;;;" -I
:; ANTA

APLR

Figure 1.7 Longhurst's (1998) biogeographic divisions of the marine environment. The oceanic boundaries of biomes
(-) and provinces (-) are shown. The biomes (and provinces within) are Antarctic Polar (ANTA, APLR), Antarctic
Westerly Winds (SANT, SSTCj, Atlantic Coastal (BENG, BRAl, CNRY, FKLD, GUIA, GUIN, NECS, NWCS), Atlantic Polar (ARCT,
BPLR, SARCj, Atlantic Trade Wind (CARB, ETRA, NATR, SATL, WTRA), Atlant ic Westerly Wind (GFST, MEDI, NADR, NAST),
Indian Ocean Coastal (ARAB, AUSW, EAFR, INDE, INDW, REDS), Indian Ocean Trade Wind (ISSG, MONS), Pacific Coastal
(ALSK, AUSE, CALC, CAMR, CHIN, HUMB, NEWl, SUND), Pacific Polar (BERS), Pacific Trade Wind (ARCH, NPTG, PEQD,
PNEC, SPSG, WARM), and Pacific Westerly Winds (KURO, NPPF, PSAG, TASM). (See also Chapter 8).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
wit h most aspects of biogeography and biodiversity, terres-
trial d ata are considerably more advanced compared w it h
that for the marine environment, and the values for many
marine invertebrate taxa are simply rough estimates. Table
1.2 shows the similarity in endemism (except in polar archi-
pelagos) of two of the better-known marine and terrestrial
taxa at example islands. Care is needed in the interpreta-
tion of such d ata; animals with long-lived planktonic lar-
vae (e.g. crabs) are likely to have lower rates of endemism
than those with only limited opportunities for dispersal,
such as an imals that brood their young (e.g. amphipods) .
Nevertheless, levels and patterns of endemism provide a
powerful insight into the evolutionary history of areas.
Isolation prevents taxa evolving locally and then spre ad-
ing into other regions, thus the more extreme and longer
the isolation, the more intense the tendency to endemism.
TECHNIQUES: Phylogeography
so
I
rerrent
,8";..[- 7 't:;c-..J
. , ' ,:::.
, »:
•
• I
5%
• Survey sites
•
BIOCUM suitability
o N01suitoble •
0 100% Palumo
0 98%
_ 95%
Relatedness of land snails in different areas within
tropical rainforest in Queensland , Australia. Scale is
shown top-left and key to differing levels of habitat
suitability is shown bottom-left. The x-axis of the
't ree' (far right) shows level of similarity (relatedness)
of mitochondrial DNA in the land snail Gnarosophia
beJlendenkerensis (Hugall et al. 2002 © National
Academy of Sciences, U.S.A.).
1.2 Biogeography
During the fragmentation of the supercontinent of Gond-
wana, many of the resulting fragments became isolated.
Some of the resulting islands, such as Aus tralia, Madagas-
car, and New Zealand , are famous for their endemic ter-
restrial vertebrates. Geographically isolated islands such
as Hawaii and, on a continental scale, Aus tralia h ave very
high levels of endemism in marine, freshwater, and ter-
restrial faunas. Anot her island, Antarctica, became even
more oceanograph ically and climatologically isolated,
and a high proportion of the species of marine phyla are
endemic (Arntz et al. 1997). A prolific decade of polar sci-
entific research since Arntz et a1.'s (1997) review has found
that Antarctic species endemism may be closer to 60% than
80% in a number of groups, but new and ongoing phylo-
geograph ic analyses should provide much more powerful
estimates (see Technique application) .
One of the major recent advances to influence ecology is
the applicat ion of molecular ecologi cal methods to inves-
t igate t he di stributi on of closely related species. This
involves sampling t iny t issue sampl es from organisms
and extracting their genomic DNA. Genetic sequences,
once amplified , can be examined and compared across
ind ividuals wi thin and between species. One such appli-
cat ion is phylogeography- the interact ion of geneti c
and spatial relationship s. Phylogeography can be a very
powerful tool, particularly if genet ic sequences from the
nucleus and mitochondria can be sampled thro ughout a
known geographic range. Mitochon drial genes evolve at
a more rapid rate compared w ith nuclear genes, allowing
related ness between organisms to be examined across a
wi de variety of t ime-scales. Mitochon drial coding genes
have bee n traditionally used in phy logeographic st ud-
ies, but it is important to realize that the mitochondrion
I ,
represents multip le genes that are united into a singl e
non-recombining locus, and is usually only inherited from
one parent. The incl usion of nuclear genes in a st udy
int roduces independent replicat ion that increases the reli-
ab il ity that the results represent the w hole organism, not
j ust one sex or a mo lecu le.
An advantage of spatially exp li cit genet ic analysis is in
the identif icat ion and characterizat ion of crypt ic species.
Recent highlights have included separat ion of giraffes into
six or more geog raphic species and crow n of thorns sea-
stars into four species. The info rmat ion stored in DNA
sequences also allows the timing of divergence events to
be estim ated , such as the invasion of the deep sea fro m
the Antarctic shelf. This tool is being successfully and
w idely app lied to investi gate crypt ic speciati on and to
infer historical processes important to pop ulation history
and speciat ion. Crucially, phylogeographic stu dies dem-
 Chapter 1 Patterns in the Marine Environment

onstrate that we tend to underestima te genetic diversity
and local scale endemism. Further they are shedding new
light on dispersal potential and any relationship of this to
li festyle an d repro ductive strategies. The latter is particu-
larly important in the context of designing netwo rks of
marine protected areas, which are dealt with later in this
boo k. As it becomes more widely used, the information
on sequences for differing genes and species are being
rapidly built up into freely available databases, such that
the context and comparisons that can be made from any
given study are similarly increasi ng.
On land, Garrick et al. (200 6) have shown how phy-
logeog raphy can be hugely beneficial to conserva tion
potential and strategy, within and aw ay f rom nat ure
reserves. Over the next decade it seems li kely that it will
have similar impacts on marine conservation. Phylogeog-
raphy has altered our perception of what constitutes a
species, w hich has had considerable ramificat ions for our
perception of the current status of biodiversity loss.
New studies of marine biodiversity, b iogeography, and
ecology are now being designed around using phylo-
geog raphy on specimens sampled. For phylogeographic
studies to have maximum rigour they require careful plan-
ning, which implies sufficient funding to thoroug hly and
evenly sample a species across its ent ire geographic dis-
tribution and to screen individuals wi th mult iple unlin ked
genetic sequence markers.

Antarctica's marine fauna has few genera and even fewer
families that are endemic, which contrasts sh arply wit h
patterns in the Australasian and Mad agascan vertebrates.
Young islands, such as Ascension Island (tropical, mid
Atlantic) or regions, such as the Arctic basin, h ave few
endemics . Before comparisons of endemism can be made
between locations, considerations of the principles of island
biogeography must be remembered. Ascension Island is
tiny and young, and even the Arctic basin is small in com-
parison with the Southern Ocean (which covers c.l 0% of
the surface of the globe) . In one sense, the use of similar-
sized areas would be ideal for comparisons of endemism,
but what size would be meaningful and would this be con-
sistent from place to place? In the marine environment
biomes and provinces are obvious starting points but so are
the coastal zones of islands, as they are often geograph i-
cally distinct. The degree of endemism is often an important
va riable, particularl y in the consideration of conservation
issues. However, comparisons between distinct regions are
often based on either species' richness or diversity per unit
area, but so are the coastal zones of islands as they are often
geogr aphically distinct.

Table 1.2 Endemi sm in marine and terrestrial archipelagos (modified from Myers 1997). Shallow water
amphipods and vascular plants are used as example taxa from the two realms. For each local ity the island size,
total number of species, and percentage of endemics is given. The one polar locality, South Georgia, is show n in
italics.

Land area x 100 km' Shallow amphipods Terrestrial plants

No. species 0;0 endemics No. species 0;0 endemics

New Caledon ia 160 17 2 70 2700 95
New Zealand 2680 1 13 66 16 18 81
Madag ascar 5877 3 14 ? 10000 80
Fiji 18 3 80 41 1628 50
Japan 3800 300 40 4022 34
Galapagos 80 51 33 701 41
Tristan da Cunha 1.0 24 33 70 29
Society Is. 6.4 32 31 623 44
Ber muda 0.5 51 12 165 9
Ireland 820 263 <1 121 0 <1
South Georgia 36 152 35 25 4

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Australia and North America lost most of their indig-
enous animals c.1 00 000 years ago, and Madagascar
and New Zealand have lost an even greater proportion in
the last 10000 years. Before comparisons of endemism
can be made between locations, the principles of island
biogeography must be remembered .
1.3 Biodiversity
1.3.1 Whatis it?
Since the Convention on Biological Diversity (CBD) held
in the city of Rio de Janeiro, Brazil in 1992, the abbrevi-
ated term biod iversity has become an accepted and much
used term. Interpretations of what the term means vary,
but effectively it re fers to the life on the planet, and is
used to encompass extinct and living organisms (Box 1.5).
There are three m ain threads of biodivers ity: ecological
(e.g. biomes, ecosystems, and habitats), organismal (e .g.
kingdoms, phyla, and species) , and genet ic (popu lations,
individuals, and genes ). Some of these components, such
as genes, are unambiguous; while ot hers, such as popu-
lations or t axonomic ranks, are difficult to define w ith
precision. Species is probably the unit of m ost com mon
reference and species' richness one of the most com monly
used methods of quantifying divers ity. As with any t axo-
nomic rank (o r indeed biodiversity) , the term 's pecies '
does not have a single definition. One defi nition of a 'spe-
cies' is: 'a group of organ isms that are able to generate
reproductively via ble young'. However, it is somewhat dif-
ficult to demonstrate the latter for fossil spe cies ! Thus the
term morpho-species h as been widely used (those wit h
observable distinct structural differences, e.g. the colou r
and shape of a gastropod shell)-but genetic stud ies have
demonst rated that some morpho-sp ecies actually com-
prise m any cryptic species.
Biodiversity comprises ecological , organ ismal, and
genetic components.
Even sm all (0 .1 m-) samples of species' assemblages in
the marine environment can contain anything from 1 to 10
000 individuals, representing from 1 to 150 species. In most
cases there will be from 20 to SO species within the sample,
but a few species will account for most of the individuals.
This means that many different species within a sample are
likely to have similar functional roles within the assemblage.
Th is raises the ecological question of 'what is the purpose
of so much duplication of sim ilar ecological roles within
an assemblage?' Perhaps more intriguing is the notion that
some species are redundant suc h that their extirpation from
a defined area would have no consequences for local ecosys-
1.3 Biodiversity
Box 1.5: Biodiversity
This term, a combination of the words 'b iological' and
'diversity', essentially refers to 'the variety of life' (see
Gaston & Spicer 2004). The CBD used the defini-
tion 'the variability among living organisms from all
sources including, inter alia, terrestrial, marine and
other aquatic ecosystems and the ecological com-
plexes of which they are part; this includes diversity
within species, between species and of ecosystems. '
Gaston and Spicer (2004) suggested that, amongst
the many defini tions, this is a good general one if
'living' is altered to ' living and all those that have
ever lived' to take into account past forms (the vast
majority of life).
tern function (Chapter 6) . Hence the prevalence ofrare spe-
cies, which share sim ilar functional roles, m ay explain, to an
extent, the resilience of m arine ecosystems to environmen-
tal and anthropogenic influences. As a result, species-poor
systems are expected to be those that are most vulnerable
to external forcing factors, as the elim inatio n of one or two
species may have a proportionately much greater effect on
ecosystem functioning.
Species-poor systems are expected to be those that are
most vulnerable to external forcing factors.
The realization that the functional diversity of benthic
assemblages m ay differ considerably from the diversity
ascertained from the quantification of separate species
(e.g. species' richness) has led to the development of new
techniques that describe community structure and compo-
sition . Taxonomic diversity (~) and taxonomic distinct-
ness (~*) are proposed to be more sensitive to variation in
environmental stress than tradition al diversity indices, as
they use information de rived from the hierarchical taxo-
nomic tree upon which species' identities are based (Chap-
ter 15). Taxonomic diversity is de fined as the average pat h
length between every pair of individual organisms identified
from with in a sample. Individuals derived from the same
genus have a shorter average path length than individuals
within the same family. Taxonomic distinctness is defined
as the average path length between every pair of individu-
als, ignoring those between individuals of the same species
(Fig. 1.8). These indices circumvent two problems that nor-
mally confound detection of more subtle responses to stress
by standard diversity indices, such as Shannon-Wiener
(H') and Margalef's (d) . For example, in stressed environ-
ments, such as those subjected to severe organic pollution,
the dominant species include polychaetes in the Capitella
capitata complex of species and the genus Ophryotrocha.
 Chapter 1 Patterns in the Marine Environment

This group contains related species that have a similar tro-
phic role or function . Hence, despite the presence of a high
number of species from within this group. the weighting
given to these species is down-weighted compared with a
less perturbed assemblage comprising only a few individuals
of these closely related species but greater numbers of taxo-
nomically less related species (Fig. 1.8) . In addition, these
indices incorporate a multivariate component by retaining
the information derived from species' identity. whereas
standard indices give no weighting to species' identity such
that two assemblages with an entirely different species' com-
position could have the same index of diversity.
Standard indices of diversity do not incorporate any con-
sideration of species' identity; hence two samples wit h
an entirely different comp lement of species can generate
the same value fo r the diversity index in question.
A principal issue with the quantification of biodiversity is
the scale at which measurement or sampling is undertaken.
5. Phylum
4. Closs / 1""
/\
3.0rde r
There are vast numbers of studies of biodiversity whose
scale in time and space varies over many orders of magni-
tude according to the types of organisms under investiga-
tion. For a specific community, there is a standard method
for estimating how representative sampling has been. Sam-
ples are repeatedly taken, and the number of new species
from each successive sample is plotted against the cumula-
tive number of samples. When species' numbers no longer
increase (the curve reaches an asymptote), the sampling
is gauged as sufficient (though this does make a number
of assumptions) . This is known as a species' accumulation
curve. The problem is that different scales are appropriate
for sampling different organisms, communities, and ecosys-
tems. While a I_m2 sample would be too large as a unit to
assess the richness and abundance of tiny infauna, the same
scale would be far too small to assess their wading-bird or
fish predators, which are far less abundant and much more
mobile (Kaiser 2003) . So the time or spatial scale to be used
to measure biodiversity has to be specifically geared to the
ecosystem, community, trophic level, and lifespan oforgan-
isms, and even the type of sampling apparatus and proto-
col (Chapter 15) . Given such differences in the method of
measurement, comparison of biodiversity values in time
and space is not straightforward. Certainly when making
or evaluating comparisons that have been made, it is vital
to consider the implications and bias due to scale effects.

2. Family Sampling needs to be undertaken in proportion to the

1. Genus -. / abundance and mobility of biota; t here is no point t rying

t o sample fish communities at a scale of < 1 m 2 •
O.Species
/1\ I
ABCD EFG ACE W I tt
Sample A Sample B
Calculating a· 1.3.2 Biodiversity through time
Sample A Sample B By measuring biodiversity of particular types of habitats
BCDEFG CEWIYl or particular groups of organisms, it is easy to see that
A 1 I 1 2 2 2 9 A I 2 5 5 5 5 23 biodiversity is not static in time or space. The number of
B 1 1 2 2 2 B C 2 5 5 5 5 22
C 1 2 2 2 7 E 5 5 5 5 2D
lower taxonomic units (species, genera, families, etc.)
D 2 2 2 6 W 5 4 4 13 has increased many-fold over the approximately 570-600
E 1 1 2 I 3 5 B million years for which we have a fossil record of macro-
F I 1 Y 5 5 organisms (Fig. 1.9A). This represents less than 5% of
TOIol pcth longth (P) 33 91 living species, past and present. However, we can only esti-
Number of linkoges (LJ 21 21 mate the number of species that may have existed at any
one time, as for many species the fossil record is poor or
157 4.33
absent. For every one species for which we have fossil evi-
dence, there may be a thousand whose existence remains
Figure 1.8 An example of the method of calculating unknown. To complicate matters further, the duration of
t;. for two different samples: A, typical of a polluted site the existence of a species can vary from approximately 1
and, B, typical of an unpolluted area The hierarchical million to 10 million years. From the limited evidence we
linkages are shown with the path length at each level. The have of fossil taxa (Fig. 1.9), the overall increase in num-
species' (A, B, C, D, E, F; G, W, X, Y, Z) matrix shows how bers of animal families has been uneven, punctuated by a
the path lengths between each species are calculated. 1:1'" series of sudden decreases. These decreases are referred to
is the product of the total path length divided by the total as extinctions, and the largest occurrences as mass extinc-
number of linkages. tions, which themselves have interesting patterns in time.
 1.3 Biodiversity
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

The rate of speciation also appears to have been variable,
and major radiations have generally occurred 'soon' after
the occurrence of extinctions.
The pattern shown in Figure 1.9A: a shows the trend in the
numberofanimal families across time and uses data pooled
from all animal families. Such general figures mask the dif-
ferent patterns that occur for each ofthe component animal
groupings. For example, trilobites (Fig. 1.9A: b) were one of
the more abundant and species-rich benthic anima l types
found in Palaeozoic seas, but it seems that none survived
the biggest mass extinction that occurred at the end of the
Permian period. The patterns of increase and decrease in
speciation differed with both the taxonomic level consid-
ered and between different specific taxa. For example, in
the bryozoan orders Cheilostomatida and Cyclostomatida,
contrasts in patterns can be seen both among and within
representatives of these orders. Furthermore. family and
genus level patterns contrast strongly. particularly in rela-
tion to the KT mass extinction 65 million years ago (Fig.
1.9A: c, d; Box 1.6).
One theory to explain sudden radiation after an extinc-
tion event is I barrel filling', a term used to refer to the
rapid diversification of biota to fill the many empty
niches following an extinction event.
Bryozoans are benthic, colon ial, suspension-feeding
organisms (Fig 1.9 B).

(A)
1000
(-I (b)

SOD

-..."
c

~
0
-500 -400 -200
•
~

z
c• 80
«j
350
(d) I
JOO~
60 I-
250 I-
/
200 ~
V
40 I-
150 l-
20 ~ 100 ~ I/'
50 I- J
0 , , , , ,
0
-200 -150 -100 -SO 0 -200 -150 -100 -SO 0
Time (millions of jeers agol

(B) Figure 1.9 (A) Changes in taxon

richness with time (millions of
years): (a) overall numbers of
famil ies; (b) foss il trilobites, an
extinct phylum; (c) numbers
of bryozoan families; and (d)
numbers of bryozoan genera
The blue line codes for th e order
Cheilostomatida and th e red line
for the order Cyciostomatida. Plot
(a) redrawn from Jablonski (1999)
and plots (c) and (d) redrawn from
Sepkoski et al. (2000). (B) Inset
image: a range of d iverse different
types of bryozoan colonies.
Photograph: David Barnes.
 Chapter 1 Patterns in the Marine Environment
While overall patterns of lower taxonomic levels indi-
cate a substantial increase with time, this may not be the
case for the higher taxonomic levels, such as phylum. Ste -
phen J . Gould popularized the work of several scientists
that investigated a particularly fossiliferous and ancient
out-crop of rock called the Burgess Shale (Gould 1989).
The fossil organisms revealed in these rocks were not overly
speciose but they were very different from each other. Most
of the phyla known today are represented in early Cam-
brian rocks but in addition there were many oddities that
could not be assigned easily to existing phyla and resulted
in many early misinterpretations of body form and func-
tion. The number of taxa present in this early fauna has
attracted considerable debate, but there is undoubtedly
an almost unprecedented diversity of body types (d is-
parity) . Whether different organisms are 'lumped' into
existing groups or 'split' into new taxa are two extre mes
of approaches taken by taxonomists. Since the dominance
of the enigmatic Marella (Box 1. 7) in mid-Cambrian rocks
there has been a sequential series of dominance by higher
taxa, such as trilobites and brachiopods in the Palaeozoic
or ammonites and marine reptiles in the Mesozoic. Since
the Cretaceous, the cheilostome bryozoans (Fig. 1.9A: c,
d) , gastro pod molluscs, and teleost fish have dramatically
radiated in richness and disparity, a pattern also reflected
in the radiation of land mammals. Some taxa, such as the
corals and sponges, h ave been speciose and abundant
throughout their fossil record to the present day. Other
groups, such as the priapulan worms, exhibit remark-
ably few morphological changes over nearly 600 million
years, and remain a minor group in terms of disparity
and richness. Based on evidence from only the Cambrian
period, or even that from the whole Palaeozoic, it would
be difficult to predict wh ich of the higher taxa would be
Box 1.6: The KT mass extinction
The KT mass extinction refers to the sudden decline
of organisms at the boundary of the Cretaceous and
Tertiary periods. In the KT mass exti nction (K is for
Kreide , meaning 'chalk' in German, which describes
the chalky sediment layer from that ti me; T is for
Tertiary, the next geologic period), all land animals
over about 25 kg went exti nct, as did many smaller
organisms. In total, 1 1 % of marine families were lost
(which compares with other mass exti nctions, except
the Permian-Triassic in which 52% of marine families
went exti nct). The KT mass extinction is famously
linked wi th several events: fi rst, it was approximately
at this time that a large meteorite collided wi th earth
in the Caribbean near the Yucatan Peninsula; second,
the remaining dinosau rs perished at this time.
successful today or to predict which phyla might come to
dominate in 50-100 million years time. While palaeon-
tologists are primarily interested in the pattern of species
through time, for biologistswho workwith present-day taxa,
patterns in space have attracted most attention and debate.
Based on evidence from only the Cambrian period , or
even that from the whole Palaeozoic, it would be difficult
to predict which of the higher taxa would be successful
today or to predict which phyla might come to dominate
at some point in the future .
1.3.3 Biodiversity in space
How many species are alive in the global marine environ-
ment today? In total about 2 million species of organism
have been described to date from all habit ats, of which
most h ave been terrestrial insects or plants. Terrestrial
organisms and habitats have been much better sampled,
but many believe that they will still dominate global spe-
cies' richness, even when marine habitats are better stud-
ied. Nevert heless, it is important to remember that the seas
are much richer in higher taxonomic levels (e.g. phyla and
classes). At present, providing estimates of the total num-
ber of species in the ocean is problematic for the follow-
ing reasons: most of the oceanic environment is so poorly
studied; some taxa, e.g. nematodes, may be very rich in
species but there are few taxonomists to describe the spe-
cies; and some previously well-studied taxa appear to be
a complex of m any crypt ic species, whose identification
will require extensive genetic studies. Along a spatial scale
grad ient, biodiversity is essentially cons idered at point
(a diversity), habitat ( ~ d ive rs i ty), or re gional (y diversity)
levels. Discussions of large-scale patterns of biodiversity
almost invariably deal with 't level data. For about two cen-
turies scientists h ave considered the species' richness of
organisms to increase from the poles to the tropics. This
is supported by robust data sets from the terrestrial envi-
ronment for plants, insects, birds, reptiles, and mammals.
However, cons iderable debate exists as to the cause of
such a cline (trend) or whether it is real or partly an arte-
fact of confounding factors (e .g. land area; the land mass
in the southern hemisphere is less than in the northern
hemisphere ). Data from the marine environment are even
patchier, but sim ilar debates occur over the global latitu-
dinal pattern of increasing species' richness towards the
equator. To date only a few marine data sets cover entire
hemispheres or even just multiple oceans. Even the most
ro bust data sets cover only the northern hemisphere and,
even then, only the American or Atlantic coasts. One of the
best-known species' latitude d ata series is that reported
by Roy et al. (1998) for North American gastro pods. Gas-
tropod species' richness is considerably depressed at high

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Box 1.7: Typical Cambrian fauna
Marella (see figure: A) , an enigmatic species belonging to an unknown phylum, was the most common in Burgess
Shale rocks (Cambrian mudstone). Early representatives of extant phyla, such as the priapulan Ottoia (B) and poly-
chaetes (C) crawled on these muds together with strange forms like Hallucigenia (D) , Wiwaxia (E) , and Burgessia
(F). Other strange forms were
stalked, such as Dinomischus
(G) , or were large swimmi ng
predators, such as Anomlacaris
(H). Anomlacaris (whose name
means strange shrimp) was
origi nally described from just
the curled front-most append-
ages- they were thought to be
shrimps. Its circular mouth and
main body we re also described
as separate species until all
three fossils were realized as
belonging to one larger organ-
ism. Other common animals at
this t ime (and well before this -
pe riod through to present day)
we re cnidarians, such as the jel-
lyfish (I) and sponges (J).
latitudes (Fig. 1.10a) but equatorial values are also signifi-
cantly lower than those at latitudes from 15 to 30 0N. North
Atlantic data for bryozoans and sea-weeds also decrease
in richness towards the North Pole, but studies elsewhere
suggest that Atlantic t axon richness levels are not repre-
sentative and thus wide-scale generalizations should not
be based on suc h data alone. Patterns of coastal decapod
crustace an (e.g. crabs and lobsters) richness h ave now
been described across the Americas (Fig. 1.10b), and dem-
onstrate a strong decrease in richness towards the Arctic
and a weaker decrease towards higher sout he rn latitudes.
Approximately 2 million species have been described to
date, but these are mostly terrestrial insects and plants.
Clines in species ' richness from the poles to the tropics
could be caused by artefacts such as differences in land
area.
The only truly global data series are those for the bivalve
molluscs (Fig. 1.lOd) and estimates for the reef-building
(hermatypic) corals (Fig. 1.lOe ). Both of these groups
show distinct latitudinal grad ients, but longitudinal gradi-
ents appear equally strong. Basically both patterns radiate
out from an Indo-West Pacific 'hotspot' (in contras t to
terrestrial plants, which are richest in the American trop-
1.3 Biodiversity
H
G
D~_0
0-
-B---
ics) . Clarke (1992) suggested that, while there was a clear
northern cline in species' richness, evidence for a similar
pattern in the southern hemisphere was at best inconclu-
sive, and remains so today. New data reinforce the exis-
tence of the northern trend; but while some studies have
supported a sou thern decrease for decapod crustaceans
and bivalve molluscs, other studies demonstrate that gas-
tropod molluscs increase in richness towards the pole. The
Sout he rn Ocean has disproportionately high numbers of
some m arine taxa, notably the Pycnogona, Polychaeta,
Brachiopoda, and Bryozoa. Very rare ly have biodiversity
patterns been cons ide re d across organism types (in other
words scient ists h ave looked for patterns within one group
of organisms, e.g. the Mollusca). The established paradigm
for decades has been of a rich East Indian/West Pacific cen-
tre decreas ing outwards to lowest levels in the south and
north polar regions. The first inventory of (macroscopic)
animals at a polar archipelago (the South Orkney Islands
in Antarctica; see Barnes et al. 2009) found much higher
biodiversity than reported for many temperate or even sub-
tropical islands- with a species' richness compara ble to the
Galapagos Islands.
The debate on the causes of a global pattern of species'
richness in the sea would seem premature given uncertain-
ties surrounding the evidence for consistent patterns in the
southe rn hemisphere. One such explanation for both the
latitudin al and longitudin al patterns of richness in the sea is
 Chapter 1 Patterns in the Marine Environment

o 100 200 300 400 500 600 700 BOO 900 1000 0 100 200 300 400 500 600 700 BOO 900 1000 1100 0 10 20 30 40 50 60 70 80 90 100 110

180 ~ ~ ~ ~ ~ ~ ~ ~ 1000 1100 1200 o 10 15 20 30 40 50

Figure 1.10 Latitudinal and longitudinal patterns of taxon richness. Numbers of. (a) species of gastropod molluscs, (b)
species of decapod crustaceans, (e) species of sabellid polychaetes, (d) species of bivalve molluscs, and (e) genera of
hermatypic corals. Plots redrawn from data in Royet al. (1998), Boschi (2000), Giangrande & Licciano (2004), Crame
(2000), and Stehli & Wells (1971), respectively.

focused on sea basin age, which might explain why latitudi-
nal trends are strong towards the young Arctic (it is still in the
process ofbeing invaded) but weak towards older Antarctica.
Part of the problem of discerning gradients in diversity
is the patchy coverage of major animal and plant groups
in the marine environment.
The Southern Ocean has disproportionately high num-
bers of Pycnogona, Polychaeta, Brachiopoda, and Bryo-
zoa.
In the deep sea. a latitudinal cline in species' richness
is also evident in the north but not in the southern hemi-
sphere. A recent high-profile study (Brandt et at. 2007)
described a remarkable richness of undescribed species,
especially of isopod crustaceans. in the Southern Ocean
deep sea. There have also been suggestions of a decrease in
richness from the shallow waters (continental shelf) down
into deeper waters . Support for this came from early abys-
sal samples, but sampling elsewhere (e .g. off Norway) has
cast doubts on the generality of a trend (Gray 2001) . Very
shallow faunas are young (major changes occurred at the
last ice age berween 14 000 to 10000 years ago) as sea-
level changes require constant reinvasions and ice-sheet
maxima have repeatedly bulldozed colonists to the shelf
edges (Chapter 8) . The deep-sea fauna also must be quite
young as the flow of oxygen-laden cold water from Antarc-
tica is relatively recent (older than shallow shelf environ-
ments, but maybe only a million years old) . Thus the oldest
and richest fauna might be expected in the vicinity of the
shelf edge, presently at a depth of about 200 to 300 m (but
deeper in the polar regions) . The richness oflarge (mega-)
benthos and fish increases towards and away from shelf-
edge depths. Any bathymetric cline is unlikely to be as sharp
or directional as the altitudinal richness clines in the ter-
restrial environment.
The oldest and hence richest fauna might be expected
to occur at the margin of the continental shelf. The con-
tinental shelf edge occurs at a depth of 200 m.
 1.3 Biodiversity
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

•
CURRENT FOCUS: Why does manne grabbed so much of the attention because the rest of the
biodiversity matter? science in the paper was much more important. Drawi ng
on a wide range of case studies, and some meta-ana-
Whenever you hear biodiversity mentioned on the televi- lytical techniques, Worm et al. demonstrated consistent
sion or on the radio it is an almost given fact that biodi- patterns in the relationship between key ecosystem func-
versity is inherently 'good' and that 'more' b io diversity is t ion ing and biodiversity.
better than 'less' biodiversity. However, it is rare tha t com- In the figu re below, (a) and (b) show the response
mentators explore what evidence underlies this 'belief'. ratios (taki ng the rat io of high:low diversity treatment
Furthermore, some of the early experiments that sought respo nses in experiments) (+95% (I) of ecosystem
to unde rstand the relationship between biodiversity and processes of experimental manipulations of species
the provision of ecosystem services reported results diversity of (a) prima ry producers (such as phytoplank-
that were complex or idiosyncratic (e.g. Emmerson et ton or macroalgae) and (b) consumers (e.g. herbivores
al. 2001). Clearly the relationship is not that simple to or carnivores). The dashed line through 0 would indicate
understand. More recently, a paper published by Worm et no difference, hence it is clear tha t higher biodiversity
al. (2006) provided some compelli ng evidence of the link treat ments consistently have posi tive effects on these pro-
between biodiversity loss and declines in ocean ecosys- cesses. In (c), increasing seagrass genotypes increased
tem services. This paper became somewhat infamous due the density of seagrass shoots in recovery experiments
to the much publicized prediction that there would be 'no subjected to grazi ng t reatments. In (d) a more diverse
more fish in the sea by 2048', which was hotly contested diet increased the production of copepod eggs. In (e),
by the wider marine fisheries science commu nity. It is well catch p roductivity in wild capture fisheries (excludi ng
worth studying the complete debate and subsequent fol- those tha t were considered in a state of collapse) was
low-on paper Boris Worm co-authored with Ray Hilborn. highest in systems with greater fish species diversity in
It was a pity that Worm et al.'s fisheries extrapolation large marine ecosystems.

(oj (b) «J
0.8, -- - - - - - - - - .- - - - - - - -----,
70
0.7
0.6 65

~ 0.5
e• D.•
.
]
~
•• 60
55
a@ •
~•
0.3
0.7 .x•-
~ 50
45

0.1
_____________ Jl +_ 40

D.' ----------------------
(5) 131 114) 151 (6) (9) (8)
35

•
~' a
••
0
~ ~ .- 1 2 3 4 5 6 7
• i~
Number of genotype5
,h l ! j !
Producer diversity Consumerdiversity

(d) 1400 (,) 80

1200 70
r = 0.57
P < 0.0001 •
•.-
•
~ 1000
•
;r
~
60
.*
• •
•
• s:••• ~.
50
800
0
•
.. a
600

•
.~
s•
40
30
.s 400 ~

~.
• ••
••
700 "
10
0 0 •
Average
Monorultures
8.. Mixed die!
45pe<ies
1 7 3
(log) Species ndmess
•
Meta-analysis is a p rocess in w hich mul t iple ind ep end ent published stud ies are drawn t o geth er t o provide a
global synthesis (see www.cebc.bangor.ac.uk).

Referen ce: Worm et al. 2006 Impacts of Biodiversity loss on ocean ecosystem services. Science, 3 14 : 787-790 .
 Chapter 1 Patterns in the Marine Environment

1.3.4 Biodiversity and ecosystem
functioning
The species that constitute ecosystems can be assigned to
functional types, such as pioneer encrusting suspension
feeders (e.g. some polychaetes and bryozoans), competi-
tively dominant encrusting suspension feeders (e.g. some
sponges and aseidians ), benthic zooplankto n feeders (e.g.
some anemones), deposit feeders (e.g. echiuran worms),
scavenge rs (e.g. arnphipods) , mobile carnivores, and oth-
ers . The concept of biodiversity can also be used in the con-
text of the number of functional groups within a system.
Thus the functional diversity of an ecosystem is higher
if the number of functional groups is higher and/ or the
number of members of each functional group is higher.
Higher functional divers ity should mean that ecosystems
are more robust to change and environmental stress. This
is currently an important area of research, which seeks to
answer the qu estion 'if the number of species in an eco-
system decreases does this affect its ability to respond to
change?' (See Curre nt Focus box and also Chapters 6, 8,
and 15. ).
One of the key questions in ecology is the role of func-
tional diversity in ecosystem resilience.
Some species have been described as 'keystone' with in
their communities (Chapters 6 and 8) . Such species, when
experimentally removed, can h ave major ecological conse-
quences for the other species wit hin the system (Pace et
a1. 1999). Few species, even those considered as 'keystone',
have been demonstrated to h ave a pivotal role in their
community. Some simple hypotheses have been generated,
however, to predict change in ecosys tem functionality wit h
species number (i.e. what h appens following removal of
any random species). Examples of experimental diversity-
ecosystem function studies in low richness (estu arine)
systems are given in Chapters 5 and 6. The redundancy
hypothesis predicts that an increasing number of species
increases ecosystem functionality proportionally less as
the number of species rises to a point when further addi-
tions have no net effect (a curve towards an asymptote). If
(rivet hypothesis) or that functionality is driven by spe-
cies interactions rather than the species perse (Box 1.8 ). All
of these hypotheses suggest that biodiversity is intricately
linked to ecosys tem stability. Intrinsic to the ideas of ecosys-
tem functionality, ecosys tem trophic, and food-web struc-
ture are the numbers of individu als of each species present
wit hin the system . The latter also exhibit large-scale pat-
terns in time and space.
In species-rich systems, ecosystem functionality is
unlikely to be adversely affected by the loss of one or
two species.
Box 1.8: Species'richness and
ecosystem function: the rivet and
redundancy hypotheses
Erhlich and Erhlich (198 1) described the rivet-
redundancy hypothesis. They use the analogy of the
structure of a plane wi ng to describe the response
of ecosystem functioning to species loss. The spe-
cies are equivalent to the rivets in the wing. If one
or two rivets are lost this will have little effect on
the performance of the wi ng (decreasing species
numberfrom A to B on our figure). However, as more
and more rivets (species) are lost, the performance
of the wi ng will reach a critical point whereupon a
rapid decline in function will occur (from point C to
D on our figure).
Ehrlich, P.R. and A. Eh rlich. 19 81. Extinction: The
Causes and Consequences of the Disappearance of
Species. Random House, New York. 305pp.
A
l- Redundancy theory
e B
..n
-."
0
e
l- D

, I-
this is correct, species could be lost from species-rich eco- -0

•Es ,
systems wit hout any loss of functions. This is termed the -- l-
e
functional redundancy hypothesis. Support for such an idea ~
~

comes from the response of many coral reefs to herbivore

l-
losses. In the Caribbean, losses of herbivorous, manatees,
turtles, and fish have occurred, but major system deteriora-
tion only occurred when the last big herbivore populations , , , , , ,
(sea urchins) crashed and resulted in overgrowth of coral o s 10 1\ 20 2\ 30 35
Species richness
by algae. Other hypotheses suggest that any speeies' addi-
tion or subtraction changes the level ofecosystem functions
 1.4 Abundance and size
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

1908
1.4 Abundance and size 40
70
A
0
1.4.1 Scale, time, and space 40 1909
Some animals are very abundant and some are not. Abun-
70
0
./
dant animals are often very small, such that billions would 1910
j
weigh less than a single individual of some of the rare larger 0
ones. Many low-diversity habitats are instead characterized 1911
by huge numbers of a few species (e .g. Hydrobia snails on ,\
0
intertidal mudflats, capitellid worms in marine sediments, 1912
or sea cucumbers in deep ocean trenches) . The abundance
}\
0
of most organisms is very dynamic at certain scales in time
and space. Thus, it is possible for one species to be super-
abundant one year and almost absent the next, while it is
0
./ .. 1913

1914
not uncommon to encounter thousands ofindividuals in one
0
sample and hardly any in an adjacent sample. Despite long
1915
being considered fairly uniform. this is just as apparent in
0 /'- } \.
the deep sea (see Kaiser et aI., 2007) . The abundance of a
1916
taxon so far has only been considered as an aid to quantify-
ing diversity. but many large-scale patterns in the sea occur 0
/' /~
,, 1917
not between, but within taxa. On land, seasonal changes in /
/ ,\.
the abundance of many species are obvious, and in the sea 0
,, 1918
this is most clearlyseen in terms ofseasonal blooms ofphyto- 40
70
, / ,\
plankton. Annual changes in the abundance oforganisms are 0
often due to differential survival of year-classes (co h o r ts) 40 ;,. 1919
of young that are related to environmental conditions (e.g.
70 / ' -\,,-
0
, 1920
~
temperature), abundance of predators. and competitors. 40
,,
70
There are a number of long-term data sets that demonstrate 0
,, 1921
~
major inter-annual differences in the abundance of animals 40
70
across the world's oceans. Long-term data sets of fisheries' 0
landings demonstrate the cyclical nature of 'good' and 'bad' 4 6 8 10 12 14 16 18 20
Age (years)
year-classes in various fish species. such as salmon, cod, and
herring (Fig. 1.11). Cyclical patterns have also been observed Figure 1.11 An example of inter-annual variabil ity in
at interdecadal scales or linked to ENSO events, such as sea recruitment. A major recruitment event of Herring (Clupea
stars (crown-of-thomsAcanthasteron coral reefs) or temper- harengus) in 1904 dominates a Norweg ian fis hery for
ate North American sea urchins (Strongylocentrotus in mac- more t han a decade. Adapted from Cushing (1975).
roalgal beds) (Chapters 8 and 11) .

Low-diversity habitats are typified by high abundances
of single species, which are themselves highly variable
in space and t ime.
Interdecadal cyclic fluctuations in the abundance of
invertebrates, such as starfishes and sea urchins, have a
strong influence on the ecology of the systems in which
they occur.
We can gain a much longer time-scale perspective by ref-
erence to the fossil record. which enables us to compare
patterns in the abundance of taxa. as well as species' rich-
ness. Changes in the abundance levels of species form the
patterns of mass extinction in the fossil record. Patterns
of abundance are often decoupled from patterns of spe-
cies' richness. 'IWo examples that illustrate this are the
present-day Antarctic shallow benthic fauna and in the fossil
record (Mesozoic to present-day) of cyclostome bryozoans.
In terms of the numbers of taxa. many benthic groups of
animals found in the Antarctic are dominated by those that
brood their young (e.g. sea urchins or gastropod molluscs;
see Fig. 1.12) . However. the most abundant species in these
groups are broadcast-spawners (animals that release their
gametes directly into the water column). Studying the fossil
record, McKinney et al. (1998) found that the proportion of
global bryozoan genera and species in the order Cyclosto-
matida, has steadily decreased relative to the order Chei-
lostomatida over the last 100 million years (Fig. 1.13a) .
Prior to the end-Cretaceous mass extinction (KT bound-
ary), the same pattern was evident in abundance. that is
cheilostomes became progressively dominant in terms of
bryozoan abundance. However. immediately after the KT
boundary. the cyclostomes became very abundant again
(Fig. 1.13b) . This recovery lasted only a few million years,
 Chapter 1 Patterns in the Marine Environment

I,) (b)
~ -0
100
.€o -;;F 80 "' , ~~-
100
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o ~ ~

e · 0~ 60
Q.

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[ ~ 60
: ; : 40 E .E 40
E <, ~~\ .e-"
.go ~ 20
-l:.. = 0
~."
~
~
--
~ ..; 20
';:;-0
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-150 -100 -50 0 -150 -100 -50 0

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100
Figure 1.12 Dominant fauna of Antarctic shallow
waters: (a) the echinoid Sterechinus neumayeri; (b)
~
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t he limpet Nocella concinna; (c) spirorbid polychaete

~

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worms; (d) the nemertean worm, Parbolasia corrugatus. ~

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Photographs: British Antarctic Survey. 0
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'E • Fossil assemblages
9
but is a clear illustration that historical abundance and 0
20 0
~

richness can be quite separate. Both cyclostomes and
cheilostomes are similar types of organisms (encrusting.
benthic suspension feeders) which occur in the same
J
habitats. Competition for resources (space in the case of
bryozoans) is thought to be the main driving force that
underpins major temporal patterns that are repeated in
• •
many co-occurrmg orgarusm groups.
Patterns of abundance are often decoupled from pat-
terns of species' richness.
1.4.2 Competition
Competition for resources can take many forms (Chapter
5) and can drive large-scale biogeographic and biodiver-
sity patterns. Many consider that one of the fundamental
changes that occurred in Cambrian oceans c.5S0+ million
years ago was the initiation of competition driven by the
rapid increase in the abundance and diversity of marine
organisms. Investigation of past evidence for competition
is problematical. McKinney (1995) measured the outcomes
ofspatial interference competition between cyclostome and
cheilostome bryozoans preserved in fossils (Fig . 1.13c) .
Cheilostomes consistently out-competed the cyclostomes in
c.66% ofencounters. This suggests that one of these groups
of bryozoans has had a clear, but not increasing, competi-
tive advantage. Both of these organism types are extant
(alive in the present day), hence Barnes and Dick (2000)
were able to look for similar patterns across the world, but
found no such constancy in the outcome of competition
e o Living essernhlejes
~
0
0
-100 -80 -60 -40 -20 0
Time (millions years)
Figure 1.1 3 Cyclostome and cheilostome bryozoans:
(a) taxonom ic richness and (b) relative abundance over
the last 140 million years, trend lines plotted from data
in McKinney et al. (1998). Arrow shows timi ng of KT
mass extinction, dashed blue line is species' num ber, and
cont inuous red line is genus number. Photographs show
compet ition for space between the two groups. McKinney's
(1995) data from fossi l assemblages (blue circles) suggest
cheilostomes w in c.66Ofo of competitive encounters (c).
Compet ition in living assemblages (white circles) shows
much more variability; data from Barnes and Dick (2000).
Photographs: David Barnes.
(Fig. 1.13c) . There are two possible explanations of this
discrepancy: greater variation in competition in modern
assemblages or constancy of outcome within the type of
environment that preserves well in the fossil record (warm
shallow continental shelf) . The latter seems more likely
and as such makes it difficult to interpret the implication
of McKinney's (1995) long-term pattern of competition, as
the dominance of cheilostomes would then depend on the
proportion of warm shallow shelf compared to other suit-
able habitats, which are unknown.
Competition driven by the rapid increase in the abun-
dance and diversity of marine organisms may have exac-
erbated the rate of diversification in Cambrian oceans.
 1.4 Abundance and size
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Reconstructing the outcome of competition between 100 (0) = Brachiopods

- Bivalves
biota in the fossi l record is complicated by potential arte-
facts, such as the likelihood of preservation in particular
types of habitat. 50

Perhaps the most famous example of inferred competi- -

S
."
~
c
0
600
Families

tion is that between (articulate) brachiopods and bivalve ~

E
molluscs. Both of these taxa are superficially similar, both z=
400
have a shell composed of two valves, and they are benthic
and suspension-feeding animals. The brachiopods were
200 l'. ~.
initially more abundant and diverse than bivalves, but this
trend was reversed following the biggest of the mass extinc-
tions, at the end-Permian (Fig. 1.14a, b) . Brachiopods are -500 -400 -300 -200 -100 o
presently most abundant and speciose in the deep sea and Millions af years
polar regions, two of the few areas where bivalves are not
200 (e) 0
dominant. More than a hundred years ago the match of the
o
two patterns was held-up as a 'classic' example of competi- Palaeozoic data
tion driving the gradual replacement ofone group oforgan-
isms by another superior competitor. Modern bivalves and
o
brachiopods compete for resources in some environments.
notably in New Zealand fjords. In these situations bivalves
seem to be generally superior but the outcomes of competi-
tion are complicated by predation and other factors. Gould 50 o 0 Post-palaeozoic data c9
and Calloway (1980) re-analysed the fossil data and found 0 · 0. - - -0-0. - - 00- - - - -r::n::tiJ -----
0

that. except at the end-Permian extinction, there was no o

negative relationship between the species' richness of the
two groups (Fig. 1.14c). Furthermore, they actually found
a weak positive correlation, so that there were more bra-
chiopod species when there were more bivalve species.
The positive relationships were, as the authors acknowl-
edged, probably not causal. The possibility that competition
explains the patterns of richness in these two co-occurring
animals is still debated.
The pattern of occurrence of bivalves and brachiopods
was previously viewed as a classic example of the out-
come of species that compete for the same resources.
o 100 200 300 400
Bivalve genera
Figure 1.14 Patterns of, and between, brachiopod and
bivalve (mollusc) richness: (a) numbers of families with
time over the last 600 million years; (b) numbers of
genera over the same period; and (c) generic richness of
brachiopods vs. that of bivalves, before and after the end-
Permian extinction event. Data from Gould and Calloway
(1980). The photograph illustrates abundant fossil
spiriferid brachiopods.

Competition has been investigated in many different
regions, habitats. and among and within a wide variety of
marine organisms. Relatively few large-scale spatial and
taxonomic patterns have emerged. One of the few patterns
that has emerged is that of shallow encrusting (bryozoan)
communities that are typically much more hierarchical at
high latitude (polar seas) (Fig. 1.15) . This means that the
dominance hierarchy in polar regions is more pronounced:
the top competitor wins virtually all encounters with any
other species. The next highest ranked competitor wins all
encounters except those with the most dominant. and so
on down the dominance hierarchy. If it were not for the
influence of disturbance. one species would ultimately
monopolize all the available space. In this system, dis-
turbance, through wave action (Fig. 1.2) and ice scour, is
important for the maintenance of biodiversity. as has been
described for some low-latitude communities. In contrast.
on Jamaican coral reefs, Jackson (1979) found that in many
interactions between species' pairs there was no definitive
winner. A number of studies have reported similar findings
in the competition for space among corals or sponges. In
these situations many species seem to be able to exist in
close proximity to each other and biodiversity is maintained
through biological interactions rather than by physical dis-
turbance. Most investigations of competition have been
between closely related competitors. often among species
belonging to the same genus. Intuitively this makes sense,
as similar species are likely to have the most similar require-
ments and methods of resources acquisition. In addition.
very different species compete for the same resources; for
 Chapter 1 Patterns in the Marine Environment

for space than between congenerics (two species from the

-•e
c
0.9
Hiemnhies 0 ••
same genus), which in turn was less likely than those in
the same family but from different genera. Furthermore,
,•"
- .~ O:·
~

0
•e the more distantly related the two competitors, the more
.e- /,,(fj'6 °c uneven the outcome of competition. Trends in the out-
::E
'"5;
c 0.7 • c. "• • 0 comes of competition, abundance, and richness could be
-- 0
c
"
c Networks 0 considered as patterns of success. This means that it is pos-
\
-s
,c
S-
0 • sible to measure the success of different taxa.
•"c
~

c
0.5
••
'"
0 10 10 30 40
lemude (degree~)
Figure 1.15 Changes in the structure of marine
competition with latitude. Data are how hierarchical
'pecking orders' of bryozoan communities are in the
Northern (0) and Southern hemispheres (.), scored using
Tanaka and Nandakumar's (1994) transitivity formu la. Plot
redrawn from Barnes (2002b) with additional data
example, humans, seals, and seabirds compete for sand eels
(Ammodytes spp.). Barnes (2003) examined how the inten-
sity of competition varied with relatedness in two groups
of marine organisms (e.g. bryozoans and ascidians) in two
regions of matching latitude (north-western Europe and
the Antarctic Peninsula) . The outcomes of competition
were as asymmetrical between organisms from different
kingdoms (e.g. algae and ascidians) as they were between
animals of different families (Fig. 1.16) . This study showed
that intraspecific competition (two competitors of the same
species) was less likely to result in aggressive competition
At high latitudes, diversity is maintained by disturbance
compared to biological interactions at lower lat itudes.
50 60 70 80
The more distantly related the two competitors t he more
uneven the outcome of competition .
1.4.3 Success
To measure success. we first need a standardized definition
ofthis term. In evolutionary terms, insects are considered a
successful taxon because they have radiated to a high level
of species' richness. Alternatively, higher taxonomic levels
could be considered (genus, phylum), as could the abun-
dance of taxa. Copepod crustaceans and nematodes have
been described as the most numerous animals on Earth.
and are therefore considered to be 'successful'. As we have
seen already, large-scale trends exist both in species' rich-
ness and the abundance of organisms. but these do not
necessarily coincide (Fig. 1.13). There are, however, many
more potential measures of success, which show strong
trends in space and time . Along a bathymetric gradient.
echinoderms (sea cucumbers in particular) occur across a

(oj (bJ (II

=
c

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l.0"
•
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-'="5
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~

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•I ~

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-
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,
-•• - ~
, , , 0

o ' ,
"
,
"
, -,
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= = ~- -
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0
~

~
=
'I
=
=
~

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1.a (Kaled by Nei'sgenetic identity)
j
Iemncmk divergon(e of rempetlters

Figure 1.16 Competition asymmetry with taxon d ivergence in shallow seas. Proportion of spatial competitors
demonstrating mutual aggression decreases w ith increasing relatedness in temperate bryozoans (red filled circles) (a).
Scaled by Nei's genetic index (0.273 = within fam ily, 0 .54 = within genus, and 0.96 = within species), the relationship
seems robust: it also holds true for Antarctic bryozoans (white circles) and temperate ascidians (squares). (b) Plot
modified from Barnes (2003).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
much wider depth range than other taxa and numerically
dominate the megafauna deep sea (Chapter 9) .
Nematodes are considered to be 'successful' because
they are among the most numerous animals on Earth.
Crustaceans, molluscs, and some other phyla occur in
marine, freshwater, and terrestrial systems. so an analysis
of occupancy of the available habitats in these systems with
time could be considered as an analysis of success. A fre-
quently used proxy of success is the evolution of advanced
features or complexity. Organism evolution has produced
progressively more complex designs with time or the num-
ber ofevolutionarysteps that have occurred. However, some
organisms (e.g. sharks) show evidence of over-evolution
and consequent reverse evolution from complex to simpler
reproductive strategies (Dulvy & Reynolds 1997) . There is
some debate about whether the development of complex
organisms from simple ones is directional or random. but it
is clear that the vast majority of organisms are still simple in
structure. At this point we should perhaps consider whether
more complex organisms are more successful? In many
examples this depends on the time-scale under consider-
ation. Some of the more speciose and abundant groups in
today's seas (e.g, molluscs and crustaceans) were relatively
unspecialized in Cambrian seas. Trilobites and brachiopods.
in contrast. were more specialized and for considerable peri-
ods of evolutionary time were more speciose and abundant
(see Fig. 1.10), though not since the Palaeozoic.
A frequently used proxy of success is the evolution of
advanced features or complexity.
On smaller (but still large) time-scales, increased complex-
ity has made some animal types more abundant and speci-
ose but more prone to extinction on larger time-scales. A
Figure 1.17 Complexity in suture lines of Jurassic ammonites. Four ammonite species with suture line boundaries
coloured to illustrate evolving complexity from simple (left) to progressively more complexly folded ones (right).
Photograph: David Barnes.
1.4 Abundance and size
good example is the evolution of a group of Mesozoic mol-
luscs (ammonites) that resembled the shelled cephalopod
Nautilus in today's seas. Over tens of millions of years. fam-
ilies and genera of ammonites with complex suture lines in
their shells became more speciose and abundant than sim-
pler forms (Fig. 1.17) . Despite this, those that survived the
mass extinctions were mostly the ammonites with the sim-
pler shell form, which illustrates that selection pressures for
evolutionary and ecological success can be very different.
Ammonite evolution also illustrated another major trend
with time. change in body size.
Ammonites with complex suture lines in their shells
became more speciose and abundant than simpler forms,
but it was the latter that survived the mass extinctions.
1.4.4 Size
Body size has a key role in the function, ecology, physiol-
ogy. and evolution of individual organisms. Contrasts in
animal size surround us; many are simply between organ-
ism types: all nematode worms are, for example. smaller
than brachiopods, which are all smaller than marine rep-
tiles. However, contrasting representatives of some taxa
span more than four orders of magnitude in size (e.g, for
molluscs, while many snails are just a few millimetres in
length, giant squid can measure nearly 30 m) . Other animal
types, such as sponges and colonial forms. do not have defi-
nite limits to body size, much like many fungi, lichens, and
mosses. There are strong trends in time and space for organ-
ism size. In the Precambrian (c.570 million years ago), all
known animals were fairly small. While in the Mesozoic.
we find the largest known ocean 'predator' (Liopleurodon) .
Nevertheless the largest organisms ever to have occurred
are found in today's seas, i.e. fin (Balaenoptera physalus)
 Chapter 1 Patterns in the Marine Environment
and blue (B. muscufus) whales. Within taxa, many types
of animals (mostly those with calcareous skeletons) have
tended to get larger with time (Cope's rule) . It may be that
this reflects evolution awayfrom small rather than towards
large size and is an artefact ofincreased specialization. The
increasingly complex ammonites also tended to become
larger (Fig. 1.13) . For nearly all animals, an increase in
volume will change their surface area-to-volume ratio.
This is crucial to functions such as gas exchange and feed-
ing. There has been much discussion (and little generally
accepted conclusion) on whether: (1) there have been more
opportunities for new roles (empty niches) for small or
large animals; (2) rates of evolution of body size vary with
population size or reproductive mode; and (3) oxygen. tem-
perature, or other factors were responsible for the within-
fauna size variability seen in modern faunas . For example.
amphipods, isopods, pycnogonids, and some other taxa in
the deep sea and polar regions can achieve very large size
(sometimes referred to as polar gigantism) . Analysing
amphipod sizes from around the world, Chapelle and Peck
(1999) found that size spectra of not only marine, but also
freshwater faunas showed a strong correlation to oxygen.
They later tested this hypothesis by investigating amphipod
size in a high-altitude lake (Lake Titicaca), which confirmed
their predictions (they were mainly very small) . New stud-
ies (such as Brandt et at. 2007) have revealed many previ-
ously undescribed small polar species, so it is likely that the
true extent of polar gigantism will be revisited.
Many types of animals have tended to increase in size
with time, this is known as Cope's rule. However, some
organisms (particularly colony forming biota) can shrink
in response to negative environmental or feeding condi-
tions.
The link to oxygen explains gigantism (e.g. in dragonflies)
during the Carbon iferous period when atmospheric oxy-
gen levels were higher.
Usually terrestrial fauna on islands change in size relative
to mainland counterparts, but there can be decreases as
well as increases. On islands. certain animal types (most
famously large mammals. such as carnivores or mam-
moths) become dwarfs, while others (such as rodents)
tend to increase in size. For the sea, we know of far fewer
size changes due to isolation or along resource-limitation
gradients. There is evidence of decreases in size for some
Radiolaria (Fig. 1.3f). but conversely increases in others.
Many estuarine animals seem to be smaller than their fully
marine equivalent species (Chapter 5), but any conclusions
about either reduced growth or maximum size are usually
confounded by their shorter life history. There have been
many explanations for why animals should increase in size
(such as reduction ofpredation or increasing food availabil-
ity or feeding efficiency), but there has been little consensus
of the importance of dwarfism, other than in the formation
ofcolonial modular units. One effective method ofescaping
surface area-to-volume constraints on respiratory or feed-
ing surfaces is coloniality. In virtually all cases of colonial
taxa (e.g. many ascidians, bryozoans, many corals), the
colonial modules are smaller than similar solitary/unitary
species, but the colony may be unlimited in size.
Colonies of organisms can increase in size without the
same constraints that apply to unitary organisms. This is
because there is no change in the surface area of respira-
tory or feeding surfaces, because the individual modules
of a colony remain fixed in size.
The current interest in global biodiversity means that there
is intense interest in the relative extinction rates of small-
versus large-bodied animals. In recent time the extinction
ofmanyofthe large vertebrates from continents and islands
coincided with human inhabitation. Far less is known about
size-related extinctions further back in time, most notably
in the largest extinction at the end-Permian. Predictions
based on organismal energetics alone have suggested that
larger mammals have higher extinction probabilities. Vari-
ous lines of evidence suggest that adaptive breakthroughs
in faunas occurred at small body size. This set the scene for
rapid increases in size as well as the number of species at
the start of the Cambrian and after the various Mesozoic
extinctions.
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Chapter Summary
• The mari ne environment accounts for 99Ofo of the Eart h's living space and it is where nearly all
major types of animal (phyla) evolved. Most of these animals remain endem ic (uniq ue) to the marine
environment. Mass extinctions and radiat ions of species affected marine organisms most d ramati-
cally. As marine organisms tend to be better preserved than those on land, most of our perception
of past life comes from marine fossils.
• New evidence, such as satellite imagery, has revealed that the oceans and seas are more compart-
mentalized than we once thought. Broadly, marine life seems spatially d ivided into twelve major
biogeographic biomes, each w ith different patterns of productivity and their own specific biotas.
• It has long been recogn ized that terrestrial organisms exhibit distinct trends in endemism, diversity,
abundance, size, and other characters with physical environmental characteristics. Intense wo rk on
marine organisms during the last co uple of decades has revealed some similarities and striki ng
d ifferences wit h such patterns on land.
• With more extreme and longer isolat ion of geographic regions, the tendency towards endemism
is greater. Continental shelf margins around islands, such as Hawaii or as big as An tarctica, can
contain the majority of species found nowhere else. How many depends very much on the scale at
which we look for such species.
• Biodiversity is much discussed but often poorly understood. It can be measured using a variety
of methods at various t axo nomic levels (though usually species). There is very good evidence that
richness (the number of taxa) has changed t hroug h time and differs with latitude, longitude, and
other factors.
• Other major aspects of ecology also change drastically along time and space gradients. This chapter
d iscussed the evidence for j ust a few, including how competition appears t o be more hierarchical at
the poles than at lower latitudes and how it changes w ith the taxonomic relatedness of competitors.
• Success can be measured in many ways: some organ ism types have become successful eco logically
(abundance, ubiquity) and evolutionari ly (great geological age, many taxa), though not always at
the same time. Many ot hers have had some ecological or evolutionary success, w hilst some may
always have been rare-but was this through design o r chance?
• Finally, evidence t o date suggests the largest organisms that ever lived are alive t oday, but the
largest land animals died tens of millions of years ago and the largest insects lived even earlier.
Gigantism and dwarfism occurs in certain environments even now (deep sea and polar regions).
The evolution of body size is complex and depends on many factors.

Further Reading
• Gaston and Spicer (2004) provide an excellent treatme nt of biodiversity and current topical issues,
w hile McShea (1996) provides a detailed treatment of trends between metazoan complexity and
evolution.
• Gaston, K. J. and J. I. Spicer 2004. Biodiversity: an Introduction (2 nd edition) . Blackwell Science, Oxford.
• McShea, D. W. 199 6 . Metazoan complexity and evolution: Is there a trend? Evolution 50: 477-92 .
• For an introduction to the wider impl ications of body size, see laBarbera ( 1986) for one of the best
reviews of this subject.
• laBarbera, M. 198 6. The evolutio n and eco logy of body size. In D.M . Raup and D. Jablonski (eds) ,
Patterns and Processes in the History of Life . Springer-Verlag, Berlin, pp. 69-98.
This page intentionally left blank
This page intentionally left blank
 Primary Production
Processes

Chapter Summary
Primary produ ction is the starting poi nt of all other life in
marine systems. Primary producers in the oceans span
many orders of magnitude in size from bacteria less than a
micron (u rn) in diameter through to > 50-m long giant kelps
that grow up to 0 .5 m a day. Production is measured using
bottled incubati ons or, increasingl y, from space using satel-
lite-borne ocean colour sensors that detect photosynthetic
pigments in surface waters. The conversion of inorgan ic
carbon into biomass, its subseq uent sinking to th e seabed,
and sequestration over thousands of years are fundamental
for our understanding of the ocean as a potenti al si nk for
increasing levels of atmospheric carbon dioxide. About 5 5%
of the total 'carbon captured' on Earth through the process
of photosynthesis and production of biomass takes place in
marine systems, and over 90% of the earth's CO2 is cycled
and stored through marine systems. This chapter introduces
the maj or factors that control primary production , and how
to measure it.

2.1 Introduction
The photosynthetic organisms of the ocean, as on land, are for
the most part the fundamental food source on which marine
ecosys tems are based (Field et al. 1998; Falkowski et al. 2000;
Nellemann et al. 2009). In coastal waters , the large stands of
seaweeds exposed at low tide, submerged kelp beds, or gently
wafting meadows of seagrasses that fill coastal lagoons, are
the obvious plants. These primary producers grow in much
the same way as their terrestrial counterparts: assimilating
carbon through photosynt hes is, and growing by taking up
nitrogen, phosphorus, and a host of necessary ot her minerals
and trace substances to generate new biomass.
When considering photosynthesis and the production of
new biomass we need to consider both production and loss
processes, and both are important for this chapter (Fig. 2.2) .
In the most simplistic terms, light energy is trapped and used Figure 2 .1 Sun light is the energy source for the primary
to produce organic matter through photosynthesis, and this producti on in the wo rld 's oceans, and is therefore the
organic matter is broken down through respiration to release fundamental limiting factor co nt roll ing ocean productivity
energy and heat. (photograph David Thomas).
 Chapter 2 Primary Production Processes

The global scale of this cycle is m assive and the annual cycle
There is a large body of information on primary produc-
of production and consumption has been calculated to have
tion processes in aquatic systems, and for this chapter,
the same energy production of about 1.5 x 10 14 watts per
rather than an extensive list of citations and reference list
year, equivalent to the annu al output of around 150 000
(as used by other chapters), readers are rather encour-
nuclear power stations . It is also a relatively efficient pro-
aged to use the extended reading list at the end of the
cess, with 40% of the solar rad iation absorbed converted
chapter. These have been selected for the overviews they
into organic material, which is slightly better than the best
give and the synthesis of the primary scientific literature.
modern power station . See Kolber (2007) for an excelle nt
Citations are used for more specialized points, possibly
description of the microbial ene rgy cycle of the oceans, in
not so widely covered in the more generalized texts.
a way that forms a brief synops is of much that is covered in
this chapter.
Phorosynthesit I :I Respiration
Primary production is the formation of organic matter
Organic
meienel & through the trapping of light energy and assimilation of
oxygen
Liqht
~ inorganic elements.
(visible
radiation)
,, .::
o
, ~"
~- - . _ - - - - - - - ~ - - - - - - - _ . .- - - - - o
•E
,
,, Heat (infrared ! 2.1.1 Marine plants and algae
rto;l
radialio n)
J Mangroves, salt m arsh systems, and seagrass beds (see
~ Chapter 10 for detailed cover of these systems) cover less
IFlowofenergy I - - - IFlowof material I than 0.5% of the global marine system , although it has been
estimated that they account for between 50 and 71 % of all
carbon storage in m arine sed iments. Although they are only
Figure 2.2 The massive biological cycle. The energy about 0.05% of the plant biomass on land, they still rep-
of light, inorganic nutrients, CO 2 , water, and salts are resent a considerable carbon store when looked upon on
co nvert ed to a complex mix of organic compounds and global terms (Table 2.1; Laffoley & Grirnsditch 20 09; Nel-
oxygen by photosynthetic organisms. Respiration releases lemann et a1. 2009) .
CO 2 and energy, at the expense of oxygen and recycles
nutrients to the inorganic state (image: Peter J. Ie B.
Williams).

Table 2.1. Comparison of global carbon storage by mangroves, seagrass meadows, kelp forests, and
comparative terrestrial systems (extracted from Laffoley & Grimsditch 2009).

Ecosystem Type Standing stock carbon Global carbon stocks

(gC m-Z ) (PgC)*

Plants Soil Plants Soil

Mangroves 7990 1.2

Seag rass beds 18 4 7000 0.06 2. 1

Ke lp forests 120 -720 na 0.0 1-0.02 na
Croplands 18 8 8000 3 128
Boreal forest 6423 34380 88 4 71
Temperate forest 5673 96 15 59 100
Tro pical forest 1204 5 12 2 73 2 12 2 16

.. P = peta and 1 Pg is equivalent to 10 15 g.

 2.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Figure 2.3 (a) Mangroves, li ke these in the Philippines, are hotspots of primary production in many coastal regions
(photograph: David Thomas). (b) Seagrasses are the only true marine plants and form extensive beds of high
productivity in temperate and tropical coastal waters (photograph: Ylva Olsen).

Looks can be deceptive-while the seagrasses and man- (a)

groves, and many of the species inhabiting salt marshes.
are true flowering plants (Fig. 2.3), the seaweeds are not.
Seaweeds are algae and, although they are photosynthetic
organisms, in contrast to the terrestrial plants, they are non-
flowering and do not have roots. leafy shoots, or sophisti-
cated tissues for transporting water, sugars. and nutrients.
Their major evolutionary lineages remain controversial,
although recent molecular advances clearly indicate that,
apart from a few of the green algal species, the algae are
only remotely linked to land plants.

Seaweeds, seagrasses, and microscopic algae and bac-

teria are the primary producers in the oceans.

Seaweeds, or rather macroalgae, are a diverse group. rang-

(b)
ing from mere encrustations on rock surfaces. to giant
brown algae such as Macroeystis prolifera and Neroeystis
leutkaena, which reach lengths over 50 m long (Fig. 2.4) .
The latter species is an annual. and grows taller than a
mature oak tree in a single year.
Macroalgae are easily seen by the human observer,
but we need the assistance of a microscope to observe the
microalgae that generate most of the primary production
in the oceans (Fig. 2.4) . We may not be able to see these
individual phytoplankton cells, but we can certainly see
their effects : clear waters can be turned brown almost
overnight. when light, temperature. and nutrient condi-
tions in the water are favourable. such that phytoplankton
are induced to grow at such a rapid rate that they form an Figure 2.4 The primary producers of marine systems
algal bloom. range from large seaweeds (macroalgae) that grow
attached to t he sea floor (a), down to microscopic
phytoplankton (b). Note the x1 0000 difference in scale
Phytoplankton can bloom rap idly given enoug h light and
between t he two images (photographs: Ian Lucas/Gerhard
a sufficient supply of inorganic nut rients.
Dieckmann).
 Chapter 2 Primary Production Processes
2.1.2 The phytoplankton
The microalgae vary considerably in size ranging from
about 2 urn in diameter to over 200 urn. They are very var-
ied in form, some of the most elaborate being the silicate
(glass) encased diatoms that have beguiled naturalists since
the first microscope lenses became available (Armbrust
2009; Box 2 .1) . However, these microphytoplankton are
not the only photosynthetic organisms to be found in the
phytoplankton. Since the 1980s, a host of much smaller
prokaryotic photosynthetic organisms have been shown
to be an important component of the phytoplankton. These
include cyano-baeteria such as those from the genus Syn-
echococcus, cells about 1 urn in diameter, which are found
in all waters except the polar oceans. Pelagic prochloro-
phytes in the genus ProchlorococclLS (cells of O.7 I'm diam-
eter) were discovered in the late-1980s. These very small
picoplankton are thought to be found in most waters
around the globe, and contribute a high percentage of the
total primaryproducrion ofopen waters (Figs 2.5 and 2 .6) .
However, we are only just beginning to understand their
role in global primary production, and in many oceano-
graphic studies these tiny organisms remain overlooked
(Binder et al. 1996; Fuhrman & Capone 2001; Karl 2002;
Scanlan & West 2002) .
Femtoplankton: 0 .02 to 0 .2 I'm.
Picoplankton: 0 .2 to 2.0 I'm.
Nanoplankton: 2.0 to 20 prn,
Microplankton: 20 to 200 prn,
Mesoplankton: 0.2 to 200 prn,
Picoplankton, 0 .2 to 2 IJm in d iameter, are important
contributors to plankton primary production.
This chapter describes production processes in marine
systems with a focus on photosynthetic organisms and
the constraints acting on this process. while in Chapter 3
we explore the role of non-photosynthetic organisms. The
growth ofall photosynthetic organisms is restricted primarily
by the supply of light, carbon dioxide, oxygen, and the main
macro-nutrients (phosphate. silicate. and nitrate) . However,
even when all these factors are adequate, the lack of trace
elements can be enough to restrict growth (see Box 2.6).
There are many other mechanisms for utilizing energy
sources other than light, as well as different sources of car-
bon for the generation ofnew biomass. Itis only proper that
at least some mention is given to the diversity of metabo-
lism. especially since this variety is fundamental for the
microbial ecology (Chapter 3) and biogeochemical pro-
cesses found within marine systems.
2.2 Photosynthesis
Algae (micro- and macroalgae) and cyanobacteria, such as
Synechocccus and Prochlorococcus, are photoautotrophs,
as they use light for their energy source and carbon dioxide
(or one of its various forms in the water; see 2.2.1) to pro-
duce new organic matter.
The photosynthetic reaction can be divided into a light
reaction and a dark reaction. The light reaction converts
light into metabolic energy and reducing power. The dark
reaction utilizes these to convert (fix) carbon dioxide and
form organic material. The overall reactions are :
Light reaction 2H20 + light => 4[H+]
+ metabolic energy + 0 2
Dark reaction-HH" l + metabolic energy + CO2 =>
[CH,D] + H 20,
where [CH 20 ] is used as a general symbol for organic
material.
Photoautotrophs use light as an energy source and car-
bon dioxide to produce new organic matter.
Figure 2.5 The advent of
satellite-borne ocean colour
sensors enables scientists to look
at the global distributions of
phytoplankton in surface waters.
This image shows the SeaWiFS
average chlorophyll concentration
collected from January 1997 to
July 2005 (image: SeaWiFS Project,
NASA/Goddard Space Flight Center
and ORBIMAGE).
 2.2 Photosynthesis
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 2.6 A co ncent rated w ater samp le f rom th e Arabian Sea, Indian Ocean, stai ned by t he fluorescent DNA stai n
DAPI , and viewed by ep ifluo rescence microscopy. Left: under exc itat ion by UV light, individual bacteria and flagell ates
are v isible by th eir DAPI-induced blue flu orescence. Ri ght: the same preparati on under blu e light excit at ion. Yellow
(Synechococcus sp.) and even smaller red flu orescing pi coplan kton cells (Prochlorococcus sp.) are v isible. Unlike in th e
upper pi cture, only th e auto-flu orescence of the natural p hotosynt hetic pigments can be seen. Th e large, very bright cell
is a dinoflagellate (Gymnodinium sp., about zopm in d iameter) (p hotog rap hs: Marcus Reckermann).

Photosynthetic organisms contain specialized light-sen-
sitive pigments, such as chlorophylls, to absorb light energy,
which is subsequently transferred to reduce CO2 to organic
compounds. CO, is fixed w ithin the Calvin cycle, and the
first step of the reduction of CO, in t his cycle is catalysed by
the enzyme ribulose bisphosphate carboxylase/oxygen-
ase (RUBISCO). It is important that there is a high supply
of CO, at the active site of RUBI SCO. Many species ofcyano-
bacteria and algae have active carbon-concentrating
mechanisms (CCMs) that m aintain t he required high lev-
els of CO, within the cells (Box 2.3).

Box 2.1: THE DIATOM FRUSTULE The strength of the diatom frustule seems to be a most
remarkable feature of these algae. Although diatoms are
Diatoms, a group of microalgae, are major contributors grazed, they are clearly not an easy food sou rce to break
to the phytoplankton of marine and fresh water. There into. The unique architectures and design of the frustules
are also many diatom species that live within and on top give them immense mechanical strength, and the dia-
of sedi ments, as well as species that grow as epiphytes tom silica has material properties co mparable to cortical
on the surfaces of animals, plants, and macroalgae (for bone wi th greater elasticity tha n glass. In fact, the grazers
comprehensive review see: Arm brust 2009). The charac- must exert t remendous force, and therefore expend extra
terist ic of all diatoms is that they produce cell walls made energy, to break the frustules open and get to t he cell
of silicate, which are not only very beautiful to look at, but
also apparently very strong (Brownlee and Taylor 2002). 10)
Diatoms can form dense blooms in coastal wate rs, and
are an important food source for protozoan and zooplan k-
ton grazers. However, once formed, the diato m cases, or
frustules, dissolve only slowly, and in some regions of the
world's oceans, the sediments are characterized by diatom-
ataceous or siliceous oozes: massive accumulations of
diatom frustules that have sunk from the surface waters
over eons of t ime.
Many diatom species have h igh ly ornate f rustules,
with spines, spi kes, hooks, and other protrusions. Many
of these adaptations are thought to resist sinking and
aid colony/chain formation, but also deter grazers from Sophi sticated mod el s of diatom frustules, such as
attempting to eat them. The spines of diatoms have even th is co mp uter-generated p ennate diatom, are helping
been known to clog fish gills and pierce delicate mem- researchers understand how th e st ructures of the silica
branes in gill t issues. cell w alls are related t o th eir ecol o gy and evo lut ion
(image: Christian Hamm , Alfred Wegener Institute).
 Chapter 2 Primary Production Processes

Ib)
contents. Recent studies using microscopi c crash tests ,
as well as computer-based simulations, suggest that the
diatom frustu les have arisen from an evolutionary arms
race in w hich the capability of graz ing organisms to break
open its prey has been pitched against the evolution of
very strong elastic diatom fr ustules (Hamm et al. 2003) .
Both copepods and eup hausiids, major consumers of
diatoms, have sil ica-edged mandibles an d gizzards lined
with sharp crushing structures that function like teeth . It is
likely that these structures have co-evolved w ith the devel- Scanning electron micrographs of the mandibular
opment of the diatom frustu le, j ust as the anti-grazing gnathobases of the copepod Calanoides acutus. The
sil ica spicules in grasses have co-evolved with the evolu- gnathobases of this species have strong tooth-like
t ion of teet h in animals that g raze on land. structures that consist of a different material from the
rest of the gnathobases. These structures are very suit-
able for cracking hard diatom frustules (photograph:
Jan Michels, Alfred Wegener Institute).

The strength of diatom frustules is possibly linked to an

that is primarily governed by the acidity (pH) , salinity, and
anti-grazing strategy.
temperature of the water:
HCO; + H+ ¢'> H 2 CO, ¢'> H 20 + cal.
Carbon-concentrating mechanisms maintain high carbon
dioxide levels at the RUBISCO enzyme.
pH, temperature , and salinity govern the form of inor-
ganic carbon in marine systems.

2.2.1 Carbon dioxide and
photosynthesis in the sea
Dissolved inorganic carbon occurs as several forms in sea-
water: carbon dioxide (CO,) gas, carbonic acid (H,C0 ,l ,
bicarbonate ions (HCO; ), and carbonate ions (CO:-). The
proportions of these forms in seawater are in an equilibrium
In seawater with a salinity of 35 and a 'typ ical' pH of 8.1
to 8.3 (Box 2.4; Fig. 2.5) approximately 90% of the inor-
ganic carbon occurs as HCO; . wit h 2 mmol L-l of HCO;
and only about 10 umol L-1 in the form of CO, (Fig. 2.7) .
RUBISCO requires CO, as a substrate . CO, is taken up
directly by marine algae, but this is dependent on diffu -

Range of seawater
.. ..

-
o
.~
~ 10-1
e
-
§
=
o
o
o

.J!" 10-
o
2

Figure 2 .7 Relationship between pH and the relative

proportions of dissolved inorganic carbon species in
seawater. Note the relative concentrations are plotted on a
10-' L-_---'--_~"---_--'--_ ____'_---'---'--_---': - _..J
4 5 6 7 8 9 10 II logarithmic scale (from Raven et al. 2005).
pH
 2.2 Photosynthesis
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

sion from low external concentrations compared with the
high amount of carbon present in the Ilea; pool (Box 2.2).
Surprisingly, there is still debate as to which inorgan ic car-
bon form is the predominant form used by marine algae
(Burkhardt et al. 2001 ). He O; is t aken up by some algal
species and this is converted wit hin the cell to CO 2 by the
enzyme carbon ic anhydrase (Raven 199 5; Elzenga et al.
2000) . In m any algae, carbonic anhydrase act ivity has also
been measured on the outer cell surfaces converting HCO;
to CO 2 , which is then taken up into the cells.
Note that in chemistry we talk about a substrate, whereas
later in this book we discuss seabed habitats: the sub-
stratum.
The enzyme carbonic anhydrase converts HCO~ to CO 2
within and on the outside of some cells.
Generally photosynthesis (both light and dark reactio ns)
is represented by the following equation:
6e0 2 + 6H,o + 48 photons of light es 602 + C6H 1,o6.
This highly simplified equ atio n masks the great complex-
ity of the photosynthetic process. However, it does show
that for these organisms water is used as an electron donor
to produce the reducing power in the overall metabolism,
with oxygen produced as an end product. Because oxygen
is produced, these organisms are referred to as being oxy-
genic photoautotrophs.

Box 2.2: RUBISCO of the cell. It is the most abundant protein on the planet
RUBISCO is an enzyme of very high molecu lar weight (estimates of 40 million tonnes) . Given this estim ate, an d
and in planktonic algae amounts to 50% of the protei n taking global produ ctivity at 100 x 10 9 tonnes per year,

light

,...-- HoNF ' --'<,

I,-AOP /
30
r"cl~¥.-
t -'i CO,
reer tens

IPhase 1:(arMnfi xation I

Rubisco

6 0 'C <:'()-<
Ribulose bisp osphute ].phospho ~cer·~otO-e_ - _ 6@
(RuBPI
,li;---- 6AOP
3AOP- ~_'
Colvin
cycle

L.-- - 61NAOPH I
(' - - 6NAOP '
------- 6@
Phase3: I P
Regenerationof ~::::~l~;,:;~G~IY~
Ceralde~Yde J.phosphate Phase 2:
( 0 acceptor (G3PI
2 Redudion
(RoBP)

I o-o-o-®____
G3P - _ .. Glucose and
(0 sugar) otherorganic
«mpeunds
Output

The Calvin cycle. Central to the making of biomass following photosynthetic capture of light.
Copyright © Pearson Education, Inc., publishing as Benjamin Cummings
 Chapter 2 Primary Production Processes
1 9 of RUBISCO fixes about 2500 9 C per year, i.e. about
10 9 per day, which is equivalent to 70 CO2 molecules
per RUBISCO molecule per second (enzymes characteris-
t ically are much mo re reactive, catalysing 10 0 0 0 to 100
000 molecular reactions per second).
The carboxylase reaction catalysed by RUBISCO is as
follows in the Calvin cycle:
6 Ri bulose- 1, 5-Bisphosphate + 6 CO, =>
12 (3-Phosphoglycerate).
Then follows a complex sequence of reactions, from w hich
the sugars glucose (C6 H 12 0 6) and sucrose (C1zHzzO l 1)
are common initial products.
RUBISCO is unusual as an enzyme in that it has a sec-
ond and quite different function as an oxygenase. In this
reaction, rather than adding carbon dioxide on to ribu-
lose- 1, 5-bisphosphate, oxygen is added:
Ribulose- 1, 5-Bisphosphate + 0, =>
3-phosphoglycerate + phosphoglycolate.
This reaction, known as photorespiration, results
eventually in the loss of carbon and the fo rmation of CO 2,
RUBISCO is an en zyme-ri b ulose b isphosphat e
carboxylase/oxygenase.
Box 2.3: Photosynthesis and stable
carbon isotopes
Carbon is present in nat ure in various isotopic fo rms: the
radioactive isotope 14C and the stable carbon isotopes,
12C and Be. Photosynthetic carbon assi milation results in
discrimination agai nst 13C, and as a result the produced
biomass becomes enriched in 12C whereas the remaini ng
total dissolved inorganic carbon pool becomes relatively
enriched in 13C (Bu rkhardt et al. 19 9 9a, 1999b; Riebesell
et al. 2000b).
This is reflected in their stable isotope ratio, which is
com monly reported on a eroo (parts per thousand) basis in
the 0 notation relat ive to the international standard Vie nna
Pee Dee Belemnite (VPDB) as, li 13 C = 1000((R/RVPDB ) -
1), with R = 13C/ 12e. Negative values indicate 12C enrich-
ment and more positive values indicate BC enrichment.
The isotope effect attributable to RUBISCO is about
- 2 70/00 in photosynthetic algae. In other words, the
RUBISCO effect alone will result in a li 13C of the pho-
It is an important loss react ion in pla nts, especially tropical
plants. The balance b etw een the two alternative react ions
is controlled by the ratio of 02 and CO 2 concentrations
at the enzyme:
Carboxylase (CO, fixi ng) reaction is high at high
CO 2/0 2 ratios.
Oxygenase (C0 2 re leasing) reaction is high at low
CO 2/ 0 2 ratios.
Therefore:
At high CO 2/ 0 2 retlee ee carboxylase function
:::::} CO 2 fixation & 02 production.
At low COi02 retlcs ee oxygenase function
:::::} CO 2 production & 02 utilization.
By having carbon-concentrating mechanisms (CCMs;
see above) the algae mai ntain high concentrations of
CO, inside the cells where RUBISCO is situated, thereby
ensuring that the carboxylase function dominates (Raven
1997) .
Corbon
e- _
- 13 e
12e
Ratio, 13e112e
Expressed cs 013C1% 0)
More positive = greoter proportion 13C
More negative = lesser proportion13 C
Sche matic illustrat ing th e relative proportions (not t o
scale) of t he stable carbon isot opes 13C and 12C.
tosynt hetically assi milated o rganic carbon (OBCPQC) that
is more en riched in 12C (i.e. isotopically lighter) than the
CO 2 available for assimilation by an equivalent amount.
This can be observed during growth in CO 2- replete condi-
 2.2 Photosynthesis
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

tions. However, the overall (net) biological isotope frac-
t ionat ion during photosynthe sis and, hence, the fi nal 3 1 3 C
values are a complex fu nction of a number of factors,
such as the dissolved CO 2 concentration, passive and /or
active dissolved inorganic carbon transport into the cell,
growth rate, cell size, and cell geometry. The departure
from the chemical equi librium value has been used by
geochemists and palaeobiologists to identify the earliest
ev idence for life on the planet.
The 0 13 e signat ures have become a valuable tool for
researchers interested in food webs (see later chapters) .
The signat ure tends to be conservative and maintained.
Therefore an organism eati ng the primary producer will
tend to assimilate carbon w ith the same isotopic signat ure
(in line w ith the proverb 'You are what you eat' ) . By mea-
suring the isotope signat ures valuable informat ion can
therefore be gleaned for determining food web dynamics.

2.2.2 Photosynthetic pigments 1·1

There are groups of photosynthetic bacteria that use other Chlorophyll a

reductants, such as hydrogen, hydrogen sulphide, and fer-
•
rous iron, and do not produce oxygen. Oxygen can inhibit •-
-"o
photosynthesis in these organ isms, which include purple .ao
sulphur bacteria, purple non-sulphur bacteria, and green ••
.~

o
sulphur bacteria, among ot hers. ~

Some types of photosynthetic bacteria only photosyn-

thesize in anoxic conditions.
, , \ ,
There is a great variety of chlorophylls and other light- 300 400 500 600 700
Wavelength (nm)
absorbing pigments in photoautotrophs. Chlorophy ll-a
(Chla) , is the m ajor chlorophyll of the algae, and is green Ibl
because it absorbs blue (maximally at 430 nm) and red
wavelengths (maximally at 680 nm) of light and reflects
green wavelengths (Fig. 2 .8) . Be cause Chla is such a
e
ubiquitous pigment in a w ide diversity of photosynthetic -""
-
organisms it is used as a measure of algal biomass in water
samples, and when photosynthetic rates are calculated (see
-
o

a
a
•
.<

2.1 3) they are often referred to the amount of chloro phyll

present in the sample.
'"
A wide range of pigments, including chlorophylls, are
used by photosynthetic organisms to trap light. 350 400 450 500 550 600 650 700
Wavelength (nm)
- Solar radiation
Carotenoids such as ~-carotine and fucoxanthin, as well Chlorophyll a
Phycocyanin
as chlorophyll-b, absorb in the green part of the light spec- Phycoerythrin
trum (400 to 5 20 nm), w hereas phycoerythrin absorbs in ~- (Orlltin e

a different range of the green region (490 to 570 nm) (Fig.

2.8b). Phycocyanins and allophycocyanins absorb light in
the green-yellow (550 to 630 nm) and orange-red (650 to
670 nm) parts ofthe spectrum, respectively. These pigments
are examples of accessory pigments. The wavelengths of
light that range from 400 to 700 nm are called the photo-
synthetically active radiation (PAR) , and photosynthetic
organisms adjust their light-harvesting pigments to absorb
various components of this spectrum of light which varies
w it h wate r depth.
Figure 2.8 (a) The absorption spectra of chlorophyll-a.
(b) Absorption spectra of chlorophyll-a (green) and some
accessory pigments: Phycocyanin (blue), Phycoerythrin
(red) and [f-carotene (yellow). The spectrum of
photosynthetically active radiation (PAR) is overlain.
Photosynthetically active radiation is the wavelengths
400 to 700 nm.
 Chapter 2 Primary Production Processes

Among the prokaryotes, the cyano bacteria have ChIa, as carbohydra tes (hence their value as storage m aterial and
as in eukaryo tic photoautotrophs. However, ot her photo- their occu rrence in the eggs of m ost animals).
trophs, such as the pu r ple and green bacteria, contain an y of
a large number of bacteriochlorophylls. These have d iffer- The oxidation of fats yields far more energy than the
ent absorption characteristics than the algal chlorophylls, oxidation of the same amount of simple sugars.
e .g. bacteriochlorophyll-a absorbs m aximally between 830
to 925 nm, whereas algal Chla absorbs m aximally at 430 Where oxygen does not occu r in sufficien t concen tra-
and 680 n m . tions for normal aerobic respiration, some organisms (not
algae or plan ts) can use anaerobic respiration, and use
nitrate , sulphate, carbonate , and organic com pou nds as
2.3 Respiration electron acceptors. When oxygen is depleted , a number of
other proton acceptors m ay replace oxygen, the list of w hich
The ot her major metabolic pathway that needs to be intro - is quite long with 14 compounds identified to date. Some
duced here is aerobic respiration. When oxygen is present, of the proton acceptors are well-known, such as n itrate and
compounds are oxidized using 0 2 as an electron acceptor sulphate, but others are m ore obscure and in m any respects
to produce CO, and adenos ine triphosphate (ATP). All surprising; for example, u ranium, perchlorate, and arsenic
organisms respire and, unlike photosynthesis that can only can also be used by m icro-organisms (see King 2005) . There
take place in t he light , resp iration takes place con tin uously. is a broad ge neralization t hat if a reaction is thermodynami-
Effectively the process of respiration can be exem plified by cally favourable , some m icr o-organisms w ill eventually
the reverse of the equation given for photosynthesis above: exploit it (see Table 2.2 for examples) .
Nitrate respiration is key to the denitrification process
60, + C6H 1206 -> 6CO, + 6H,o + energy*. (Chapter 3) , in which denitrifying bacteria reduce nitrate
(*When glucose is oxid ized d u ri ng respiration, 2870 kJ and nitrite to nitrous oxide or dinitrogen gas:
m ol-' of energy is produced.)
The amou n t of energy produced is dependent on the
nature o f the star ting m aterial : one m ole of fat (e.g. pal-
mitic acid) results in the production of 9959 kJ of energy Un til recen tly nitrate respiration was thought to be only
com pared to t he production of 2870 kJ when the same car ried ou t by bacteria. However, Pina-Ochoa et al (2010)
amoun t of glucose (a carbohydrate) is respired. For a given have shown that ben th ic foraminters are able to store and
weight of m aterial, fats yield at least twice as much energy resp ire n itrates.

Table 2.2 The basic reacti on s of the some proton donors and acceptor reactions involved in respiration. [CH20]
as symbolism for o rganic material , for simplicity of presentation all compounds are shown in their non-ionized
form.

Proton Proton acceptor Respiration Respiration Specific bacteria group responsible

donor end product(s) by-product
Aerobi c metabolism
[CH,Oj + 0, -> CO, + H,O No specific group

Anoxic metabolism- alternative proton acceptors to oxygen

[CH,Oj + 2 HN0 3 -> CO, + H,O + 2 HNO, Denitrify ing bacteria
[CH,Oj + HNO, -> CO, + NH 3 Denitrify in g bacteria
1
+ 1 -> CO, + H,O + 2 H,5 Su lphate-reducing bacteria
[CH,Oj 2 H,S04 -> CO, + H,O 2 H,5
• •• ••• •• •• •• ••• • • • • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• •• •• • •• •• •• • •• •• •• •• • • • • • •• •• •• •• •• •• •• •• •• •• • •• • • •• • • • •• • • •• • • •• • • •• • • •• • • •• • • •• • • •• • • • •• • • •• • • ••
Chemoautotrophic metabolism-additional proton donors to organic material
HN0 2 02 +; ~ HN0 3 Nitrite-oxidizing nitrifying bacteria
NH 3 + 0z ~ H20 + HNOz Ammonia-oxidizing nit ri fying bacteria
HzS + 202 ~ H2S04 Su lphur bacteria
 2.4 Heterotrophic metabolism
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Sulphur-reducing bacteria use sulphate, thiosulphate,
and elemental sulphur as electron acceptors in respiration.
The metabolism produces sulphide or hydrogen sulphide,
the rotten egg smell. characteristic of many anoxic waters
and sediments. Methanogenic bacteria use CO2 as an elec-
tron acceptor, producing methane (CH4 ) as an end product.
Anaerobic respi ration can resu lt in the production of
potentially toxic products, such as hydrogen sulphide
and methane.
Many of the products of anaerobic respiration are toxic
(e.g, H2S, which is even more toxic than hydrogen cyanide) .
This toxicity has very great ecological significance in water
management, since plankton. zooplankton, and higher
organisms (e.g. fish) are particularly susceptible to this
toxicity and are at risk in environments that are prone to
produce these compounds. Oxygen is always the preferred
electron acceptor, and, providing there is oxygen in the
water, these toxic compounds will not be produced.
Heterot rophic organisms obtain their carbon from the
oxidat ion of organic matter, whereas autotrophic organ-
isms obtain carbon from CO 2 ,
There are other groups of prokaryotes that use inorganic
chemicals as their energy source (ch emo lit h o trop hs) .
Most of these organisms obtain their carbon from CO 2, and
so are autotrophs. There are many sources ofinorganic elec-
tron donor used by these prokaryotes, which include both
bacteria and archaea. These include hydrogen sulphide,
sulphur. ammonium, nitrite. and ferrous iron. Again some
ofthese organisms can only survive in anaerobic conditions
whereas others are tolerant of oxygen.

There are alternative proton acceptors to oxygen.

2.4 Heterotrophic metabolism

Organisms that use chemical compounds as an energy
source, rather than light, are called chemotrophs. The
chemo-organotrophs include those bacteria and fungi
that live via the oxidation oforganic compounds and in oxy-
genated habitats; they catabolize organic matter via aerobic
respiration. Because these organisms do not get their car-
bon from CO2 , but rather from the oxidation oforganic mat-
ter, they are called heterotrophs. Those species that live
in aerobic conditions use oxygen (oxygenic heterotrophs)
as the external electron acceptor, whereas other species in
anaerobic conditions (anoxygenic heterotrophs) can use
other oxidized substrates. such as nitrate and sulphate.
instead of oxygen as the terminal electron acceptor. The
anaerobic heterotrophs are particularly important in anoxic
sediments and the biogeochemical transformations that
take place within these. These bacteria and fungi assimi-
late low molecular weight organic compounds, such as
sugars, amino acids. pyruvate. ethanol, and acetate, which
are transported directly into the cells. These organisms
release hydrolytic enzymes to break down larger organic
compounds into low molecular weight substrates that can
then be transported into the cell and then respired and built
up into new biomass.
Heterotrophic organisms assimilate carbon derived from
the oxidat ion of organic matter.
Figure 2.9 Beggiataa form filaments that twine together
to form the white mats shown here. Beggiatoa is found
in habitats that have high levels of hydrogen sulphide,
including deep hydrothermal vents, su lphur springs,
sewage-contaminated water, and mud layers (photo:
Samantha Joye, University of Georgia (www.marsci.uga.
ed u/Facu ItyPages/Joye/index.htmI).
Examples of chemolithrophic bacteria include the
sulphur-oxidizing bacteria, which grow in the tissues of
hydrothermal vent organisms where sulphides are intro-
duced into well-oxygenated seawater. Mats of Beggiatoa
also grow on the reduced sulphur from the vents (Fig. 2.9) .
Purple sulphur bacteria are another example oforganisms
that oxidize H 2S and elemental sulphur:
H,S + 20 , => SO ~- + 2W
S + H,D + 3 / 20, => SO ~- + 2W
Nitrifying bacteria are vital for nitrogen cycling and
the regeneration of nitrogen forms that can be utilized
for growth in other organisms (Chapter 3) . Two groups
of chemolithotrophic nitrifying bacteria exist: one group

~----'--'---------)
(including Nitrosomonas) oxidizing ammonium to nitrite
( Anoxic means wit hout oxygen.
and another group (including Nitrobacter) oxidizing nitrite
 Chapter 2 Primary Production Processes
to nitrate. The reactions in this vitally important process of
nitrification are:
NH: + 0 , => NO; + 4W + 2e-
NO; + H20 => NO; + 2W + 2e-
Box 2.4: Switching metabolism
There are groups of organisms that can also swi tch
metabolism. Good examples are the anoxygenic pho-
totrophic bacteria. These bacteria are capable of uti-
lizing organic carbon when it is available, but capable
of photosynthe tic light utilization and CO 2 metabolism
when organic carbon sources are low. These organisms
are abundant in the upper oceans and are estima ted to
make up to 11% of the microbial community.
There are also organisms, mixotrophs, which combi ne
the use of phototrophic and heterotrophic nutrition (e.g.
Stoecker 199 9). Many phytoplankton species, phago-
trophs, have been shown to be able to ingest particulate
organic material to meet part of their nutritional require-
ments. These range from small nanoflagellates that ingest
bacteria and cyanobacterial sized particles th rough to
photosynthetic dinoflagellates that can consume phyto-
plankton and small ciliates more than 10 urn in diameter.
Many phagotrophic algae increase their rates of particle
inges tion in response to nutrient limited conditions in
order to obtain growth limiting compounds and elements.
Some marine organisms, including some molluscs,
forami niferans, helizoa, ciliates, and dinoflagellates retain
chlo roplasts that they have ingested when grazing on
photosynthetic organisms. The chloroplasts, although
not fully integrated into the metabolism, can be a useful
source of energy. In general the chloroplasts do not func-
tion for long periods of time in the new 'host', and their
function gradually declines and they are lost. However,
in some species, such as the ciliate fv1esodinium rubrum,
which is a major species in some 'red tides', are truly
photosynthetic organisms (Dolan & Perez 2000).
One of the best-known symbiotic relationships in the
marine world is that between photosynthetic dinofla-
Symbiotic relationships are vital for coral species, but
also for planktonic radiolarians, foraminifers, turbellar-
ians, molluscs, and siphonophores.
Nitrifying bacteria are important for nitrate regeneration
in marine systems.
Mixotrophs use both phototrophic and heterotrophic
means for assimilating energy.
Bloom of the autotrophic ciliate Mesodinium rubrum
in surface waters of the North Sea. This is an obligate
phototrophic ciliate that contains endosymbiotic crypto-
phyte chloroplasts. (b) The relationship between corals
and zooxanthellae is one of the best-known symbiotic
relationships in marine systems (photographs: David
Thomas).
gellates (zooxanthellae) and benthic corals. However,
symbiotic relat ionships are also widespread in marine
pelagic com munities. A variety of algal species from
several classes have been observed to fo rm symbiotic
associations wi th protozoans, medusae, turbellarians,
and siphonopho res. In most cases these relationships
are highly species specific, most hosts only having one
species as a symbiont. Certain species of heterotrophic
dinoflagellates have cyanobacteria attached to their sur-
faces that sometimes reside within specialized pockets
of the host's cell wall. Planktonic radiolarians and foram-
inifers can contain up to tens of thousands of symbiotic
algae per individual.
It is clearly not an easy task to unravel the complexi-
ties of the metabolic pathways that are vital for the prod-
uctivity in the oceans. With ever-i ncreasing analytical
tools the current trend for the discovery of new micro-
bial co mponents of the marine microbial wo rld is likely
to continue.
2.5 Light in water
Although many factors interact to determine the net pri-
mary production of photoautotrophs in the oceans, natur-
ally it is light that is the dominant factor that determines
the rate and extent of photosynthetic activity (Kirk 1994).
It is both the quality of the light and the quantity of the light
that reaches the chloroplasts w it hin the cells that control
 2.5 Light in water
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

these reactions. As anybody who has dived or snorkelled
in open waters can testify, the penetration of light can vary
greatly (Fig . 2 .10a) . In clear waters, light can penetrate
many hundreds of metres; but in waters heavily laden with
sediment or particulate matter, it can be difficult to see a
few metres. No matter how clear the water, below 1000 m
water depth, essentially no light penetrates and hence most
of the world's oceans with an average depth of 4000 mare
permanently in total darkness (t h e aphotic zone, Chapter
9) . In general the photic zone (e u ph otic zone) seldom
extends down to 200 m water depth, and in coastal waters
light penetrates to depths of between 1 and 50 m.
Much of the light incident on the water is reflected at the
surface, and the transmission of light is then dependent on
the quantity ofparticulate matter and also dissolved organic
matter (DOM) in the water. There is an exponential loss of
light as it passes through the water (called attenuation)
due to absorbance of the light by the water itself, photosyn-
thetic organisms. particles in the water, and humic material
and various other DOM compounds that colour the water
(Fig.2.10c) .
Coloured water has very different optical properties than
non-coloured waters.

Without light, photosynthesis cannot take place. Particles in the water, such as bacteria. plankton. and
sediment, all contribute to the scattering of light in the
water. which causes the attenuation of light. Therefore
In the clearest of waters light seldom penetrates below
the distribution of such particles is intimately linked to
200 m.
the transmission of light through the water. Even bubbles,

Figure 2.10 (a) Light decreases exponentially with water depth, and as light passes through a body of water, it is
not just the amount of light, but also the spectral quality of light that changes. (b) Light quality structures zones of
submerged algae, such as these in a Baltic Sea rock pool (photograph: David Thomas.). (c) River waters often contain
high amounts of dissolved organic matter (DOM). In humic-rich rivers, the DOM turns the waters brown. Where they mix
w ith seawater, the coloured waters can greatly infl uence the optical properties of coastal waters (photograph: David
Thomas).
 Chapter 2 Primary Production Processes
ripples ofwater on the surface, and waves will have dramatic
effects on the underwater light regime. These features may
result in short-term fluctuations in irradiance, with focus-
ing and defocusing of the light. This will produce a light
regime more akin to a flashing light, which has been shown
to enhance the photosynthesis of some phytoplankton
species.
Bubbles, particles, and surface ripples all great ly alter the
lig ht field underwater.
It is notjust the transmission of light itself that is affected by
the scattering and absorption oflight, but also the spectral
quality of the light (Fig. 2.10a) . Water absorbs strongly in
the red and infrared part of the spectrum, and so at deeper
water depths the light is reduced in this part of the spec-
trum and effectively enriched in the blue and blue-green
wavelengths. Water looks blue because of this differen-
tial absorption of the blue and red parts of the spectrum.
Coastal waters have a large input of DOM. These reflect in
the yellow-red part of the spectrum, hence the character-
istic yellow/brown colour of some river and coastal waters
(Fig. 2.lOc) . This matter is referred to in the literature as
coloured (or chromophoric) dissolved organic matter or
eDOM. As the DOM pool in natural waters consists ofa com-
plex mixture ofcompounds, its absorption spectrum repre-
sents the sum of the different overlapping absorption peaks.
eDOM absorbs light strongly in the UV and blue region of
the light spectrum ( < 450 nanometres) and its absorption
decreases in intensity with increasing wavelength . When
present in high concentrations. eDOM therefore gives
water a yellow-brown colour. The eDOM in oceanic waters
is a mixture of matter derived from both autochthonous
(marine) and allocthonous (terrestrial) sources (Fig. 2 .11),
and the fluorescent and absorbtion characteristics of the
colour in a water sample enable researchers to use eDOM
as a tracer to work out the origin of a specific water mass
within the water column.
Humic-rich coloured d issolved organic matter (CDOM)
can significantly colour coastal waters.
2.6 Light and photosynthesis
The relationship between photosynthesis and irradiance is
described by the characteristic P/E curve (Fig. 2.12) . At
low irradiance the photosynthetic rate is linearly propor-
tional to increases in irradiance. At a particular irradiance
the photosynthetic rate is equal to the respiration rate, the
compensation irradiance, E c . This irradiance is species-
30,----------------,
25 Marine derived CDOM
-
-t
.§. 20
Mountain river
Streom draining ogrirulruralland
s Estuarine eDOM
~ Peatland drainage (,10')
-"c 15
s'"
~
10
5
500 600
Wavelength (nm)
Figure 2.11 The absorption of light by different water
types influenced by the chromophoric dissolved organic
matter (CDOM) within it. (Redrawn from Sendergaard and
Thomas 2004).
specific. and within a single species can vary with season
and even on shorter time-scales. As irradiance increases.
the trend becomes gradually non-linear and a point is
reached where further increases in irradiance do not result
in increases in the photosynthetic rate. In other words, the
rate of photosynthesis is light saturated (Pm~) ' The slope of
the linear part oftheP/E curve is denoted by the symbol a.
The saturation irradiance, Ek, is calculated from the inter-
cept between a and Pmax. In some organisms, there can be
a decrease in photosynthetic rates at high irradiances. This
decrease is a result of photoinhibition. This results from
damage to components of the photosystems, such as cel-
lular membranes or electron-transport proteins.
At hi gh li ght levels maximum rates of photosynt hesis can
be inhibited, this is called photoinhibition.
Just as in the terminology used for primary production.
gross photosynthesis is equivalent to the total photosyn-
thesis, and net photosynthesis is equal to gross photosyn-
thesis minus respiration (Fig. 2.13) .
The characteristics Pmax' Ee, Ek, and a are all species-
dependent, and also vary within a particular species.
depending on environmental conditions of light, nutrient
status. and temperature . Generally. Pmax increases with
increasing temperature (up to physiological limits) and
is higher in organisms that grow at high rates in nutrient-
replete conditions. compared with growth-limited cells in
poor nutrient conditions.
 2.6 Light and photosynthesis
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

(0) P (b)
, ,, 2.0
, Pmox -r
--------- If---- - ~
c

,,",
~
~
1.0
a- ,, -r
=
--
'0;
Phofoinhibilion = §:
~
='-
•
-
~ 0
c ~

Po .sa
~
~
~
p. •-
'0
0
0
0.4
=
0
-e
0
, Compensationpoint
0
~
---=
I
~

~-... 0.2
E, Ek =
~

Irrodiance (£)

o 50 100 150
Irradiance umcl m·2 sec- 1

Figure 2.12 (a) The response to photosynthesis (I') in response to changes in irradiance (E}-a PIE curve. With
increasing light, photosynthesis increases linearly and the slope of the increase is a. At the compensation irradiance
Ec the photosynthetic rate is equal to the respiration rate (R). With increasing irradiance the linear trend ceases, and at
the saturation irradiance (Ek) the rate of photosynthesis is saturated (Pmax). In some organisms, there can be a decrease
in photosynthetic rates at high irradiances (photoinhibition). Respiration typically does not change with increasing
irradiance, and gross photosynthesis is indicated by P, and net photosynthesis by P, (after Lalli & Parsons 2004).
(b) PIE curves for phytoplankton cells grown in high (0) and low light (0). In the top set the rate of photosynthetic
carbon assimilation are expressed as a function of chlorophyll concentration of the phytoplankton. In the bottom set,
the same data are expressed on a per cell basis. The low-light algae have acclimated to the low light by increasing
cellular concentrations of chlorophyll , and on a per cell basis reach the same Pmax as the high-light acclimated algae,
although their value of a is greater (i.e. more efficiently utilizing the lower irradiances).

Time course of oxygen concentrotion mation, and in low light conditions the Chlorophyll:Carbon
(Chla:C) ratio can be considerably greater than that for the
-
' il
~
same organism acclimated at higher light levels (i.e. in the

.- -•
~
0
." ~
low light cells there is more chlorophyll per cell than in
the cells at high light) . Under nitrogen, phosphorus, and
-• . ~
~
~
0
trace metal (e.g, iron) limitation the Chla:C ratio of a par-
'" - ~
~
ticular photosynthetic organism tends to decrease. Likewise
- 0

'" in lower temperature acclimated cells, the Chla:C ratio is

lower than in cells acclimated at higher temperatures. The
Respiration changing pigment concentrations of cells obviously have
significant effects on the P/ E characteristics of a particular
nme--- algal species (Fig. 2.12b) .

Figure 2.1 3 The relationship between gross
photosynthesis (gross primary production), net
photosynthesis (net primary production), and respiration.
2.6.1 Light acclimation
Within certain limits, most photosynthetic organisms are
able to acclimate to a given light regime (Macintyre et at.
2002; Raven & Geider 2003), mostly by altering the con-
centration of chlorophyll and/or accessory pigments per
cell or per unit cell area. This process is called photoaccli-
By chang ing pigment content algae can photoacclimate
to changing light regimes.
A Chla:C ratio of 0.02 :1 is often cited in the literature
and used in models describing phytoplankton dynam-
ics. However, because chlorophyll concentrations within
phytoplankton cells can be altered due to external stimuli
(temperature, irradiance, and the growth status of the
algae) within time periods of hours, the utility of this ratio
is rather dubious. Furthermore, ratios in the order of0.0 1:1
to 0.005 :1 are not uncommon in field populations (Lefevre
et at. 2003) .
 Chapter 2 Primary Production Processes
Another feature, exhibited by some algal cells w hen
exposed to changing light conditions, is an obvious move-
ment of the chlorophyll-containing chloroplasts wit hin the
cells. The chloroplasts move along cytoplasmic strands in a
process known as karyostrophy. Generally chloroplasts are
distributed within the cell so that efficie nt light abso rption
can t ake place. However, in high light, clumping of chloro-
plasts, often around the nucleus, is frequently observed,
and is thought to be associated with mechanisms to protect
cell organelles from damaging light effects. Although not
universal within aquatic photosynthetic organisms, such
Box 2.5: Compensation and critical
depths
The euphoti c zone is the upper part of the water column
that supports photosynthes is. The bottom of th is zone is
generall y defined as the depth at wh ich 1% of the surface
irradiance is measured. However, a better representation
of the bottom of the euphotic zone is the compensation
depth. This is the depth at which the gross photosyn-
thetic carbon assimilati on by phytoplankton equals th e
respiratory carbon losses, or when the net photosynthesis
is O.
A B
Photosynthesis(PJ
- -- -- -o(«mpensctlcndepth
E( compensationlight intensity
- - - - - - - - - - - - Omdepthof mixing
mechanisms are known from terrestrial higher plants. It is
likely that chloroplast-moveme nt processes are important
for coping with rapidly changing light environme nts in tur-
bulent surface waters or diurnal changes in light.
Karyostrophy is a process by which chloroplasts move in
reaction to changes in light conditions.
Compensation depth is the depth in a water column at
which net photosynthesis is O.
It is worth noti ng that there is often a reducti on in the
photosynthesis rates measured at t he surface of the
w ater. This represents an often observed lowering of the
photosynthetic rate due to photoi nhibition in the very top-
most metres of the water column.
Of co urse phytoplankton cells are not at a stat ic depth
as they and/ or the water may move. In fact they are mixed
either through out the wh ole water column or, w here w ater
strat ificat ion takes place, wi thin surface mixed w ater lay-
e rs (Chapter 7). Becau se of this, phytoplankton cells wi ll
be mixed above and below the compensat ion depth, to
depths as deep as the mixed layer depth. When cons id-
eri ng net phytoplankton growth it is therefore more pert i-
nent to relate the daily integrated photosynt het ic gains to
E
the integrated respiration losses over the w ater column
(day and nig ht) to the mixed layer depth.
The critical depth is the water d epth w here the inte-
grated daily photosynthetic carbon assimilati on is bal-
At the compensat ion depth (0,) the phytoplankton pho-
tosynthesi s is equal to the respirati on, i.e. the compen-
sat ion light intensity Ec• Phytoplankton is mixed in the
water column, above and below the compen sation depth,
down t o the depth of mixing (D m) . The criti cal depth is
the water depth w here the integrated water-column pho-
t o synthesis is equal to the integrated wat er-column res-
piration . In this diagram the area bounded by the points
A , B, C, &. D represents respiration, and the area A , C, &. E
represents the photosynthesis. At the crit ical depth these
two areas are equal. When the depth of mixing is deeper
than the crit ical depth, no net growth takes place. When ,
however, the depth of mixing is shallow er than the crit i-
ca l depth net phytoplankton growth occurs. (After Lalli
and Parsons 2004.)
 2.7 Supply of inorganic nutrients
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Data from the Norwegian Sea in

• Phytoplankton
\0,000 • Zooplankton 1949 showing the relationship
40,000 ~ Critical depth between mixed layer depth, crit-
ical depth , and phytoplankton
30,000 I Thickness mixed layer
and zooplankton abundance.
20,000
Growth occurs only when the
10,000
depth of mixing is consistently
• • -...- I above the critical depth. (Illus-
N tration adapted from Sverdrup

-- 100 ~ 1953,)

t
E
" ~'
0-rlI' ~ /' I'.
Q 200 I ~ :" -i-

s 10 1\ 20 21 30 4 9 14 19 24 29 4 9 14 19 24 29
March April May

anced by the integrated daily respiratory carbon losses.
As long as suffic ient nutrients are present, net phyto-
plankton growth occurs when the mixed layer depth is
shallower than the critical depth . When the mixed layer
extends be low the critical depth algal growth is limited by
lig ht, and there is no net phytop lankton growth (Sverdrup
1953 ; Smetacek & Passow 1990),
The critical depth theory was first proposed by Sver-
dru p in 19 53. In this theory the respiratio n losses are
not j ust the algal respiration losses, but also losses due
to grazin g organisms and the respiration of bacteria and
other heterotrophic organisms. Interestin gly it led to a
major advance in the design of freshwater reservoirs,
w here preventin g algal blooms is an impor tant part of
their management.
The seasonal changes of mixed layer depth an d inci-
dent light playa key role in th e seasonal dynamics of
phytoplankton (see be low) , These are discussed be low in
conj unction w ith the inorganic nutrient demands of grow-
ing phytop lankton po pul ations,

The critical depth is the water depth where the inte- have high concentrations of nutrients, and generally sup-
grated daily carbon assimilation is balanced by daily port high levels of primary production. Waters between the
respiratory carbon loss. two states are referred to as mesotrophic waters, and these
sustain intermediate levels of primary production.
Most marine systems are classified on the basis of the
annual primar y production, whic h is anot her way of
2.7 Supply of inorganic express ing the supply or production of organic matter in
nutrients the wate r body:

In addition to carbon , oxygen, an d hydrogen, the plant Organic Carbon Supply

must incorporate other eleme nts into organic material, This Oligotrophic: < 100 g carbon m-2 year - 1
arises as a consequence of the eleme ntal composition of Mesotrophic: 100 to 300 g carbon m- 2 yea r-'
the various macromolecules, notably proteins and nucleic Eutrophic: 300 to sao g carbon m- 2 year- 1
acids. The principal add itional requirements are nitrogen Hypertrophic: > sao g carbon m-2 year - 1
and phosphorus, and in aqu atic ecology, these eleme nts are
commonly referred to as nutrients or inorganic nutrients. The process ofeutrophication can be defined as an increase
in the rate of supply of organic matter to an ecosystem.
This occurs when there is a change in the concentration of a
2.7.1 Nutrient status of water factor (can be more than one) that limits algal growth , This
Waters that have low concentrations of essential nutrients is often an increase in inorganic nutrients, such as nitrogen
for algal growth are called oligotrophic and are regions or phosphorus, often associated with the run-off of artificial
of low primar y productivity. In contrast, eutrophic waters fertilizers from agricultural land (Chapter IS), The res ulting
 Chapter 2 Primary Production Processes
Figure 2.14 Increased inorganic nutrient supply can
result in excessive algal growth as shown by the mass
of U1va spp. supported by nutrient-rich run-off from
agricultural land in Ireland (photograph: David Thomas).
increase in algal growth (both phytoplankton and!or mac-
roalgae), if excessive (Fig. 2.14), can have deleterious effects
for the whole ecosystem (Skei et al. 2000) .
It is important to stress that eutrophication is a process
of change and is not a trophic state. For example, an estuary
may have been mesotrophic and is now classified as eutro-
phic, but it is not necessarily undergoing further eutrophi-
cation. Although eutrophication is generally perceived as a
detrimental process. it is also important to stress that it can
be a reversible process. There are also instances when low
levels of eutrophication can even be considered as being a
positive state for increasing the productivity of a specific
water body.
Eutrophicat ion can be defined as an increase in t he rate
of supply of organic matter to an ecosystem .
Eutrophication is a revers ible process and not always
detrimental.
Strictly speaking eutrophication is a process by which
the productivity of an aquatic system is increased. and can
therefore be caused by factors other than nutrient input.
These factors include reducing the suspended material in
a water body and therefore increasing the light levels avail-
able for photosynthesis, or changing the residence time of
water within a particular system. Therefore, eutrophica-
tion is also a natural phenomenon, and is not always asso-
ciated with anthropogenic activities. Coastal regions can
receive high dosages of nutrients both directly via marine
outfalls and by discharges from estuaries. This, coupled
with their relatively long residence time. makes coastal
ecosystems especially vulnerable to eutrophication (Chap-
ters 8 and 15) .
2.7.2 Supply of nutrients
Photoautotrophs require a diverse range of elements for
balanced growth. These include nitrogen, phosphorus, sili-
con, sulphur, potassium, and sodium (all known as macro-
nutrients) . Many trace elements (micro-nutrients) are also
required, including iron. zinc, copper. and manganese. as
well as vitamins such as B12 (cyanocobalamin), biotin, and
thiamine.
A wide range of macro- and micro-nutrients are needed
for algal g rowth.
Although each nutrient has the potential to limit the
growth of photoautotrophs, in most marine environments it
is either nitrogen or phosphorus that is generally the limit-
ing element (cf. Box 2.6 and Boyd et al. 2010) . It is actually
the supply of the nutrient to the organism that is critical.
A nutrient can be present in low concentrations. but if the
uptake rate by the organism is low, only a low supply rate
is required. Naturally growth can be limited by the supply
of more than one nutrient at anyone time: nutrients can be
either biomass-limiting or rate-limiting. In the case ofthe for-
mer. the nutrients are exhausted so that no more biomass can
be produced. In contrast. rate-limiting nutrients simply limit
the rate of new biomass production by their rate of supply.
Resupply of nutrients primarily takes place by molecular
diffusion.
When a nutrient is taken up by an organism, there is
immediately a reduction in that nutrient in the micro-envi-
ronment surrounding the cell or organism. The resupply
of nutrients takes place primarily by molecular diffusion
from the bulk medium of water (Wolf-Gladrow & Riebesell
1997) . Surrounding each cell or surface in water is a diffu-
sive boundary layer (DBL) in which water movement and
molecular diffusion is restricted. The thickness of the DBL
surrounding the organism is therefore critical to determin-
ing the rate at which nutrients are transported to cell sur-
faces. The smaller the organism, the smaller the DBL due
to the surface area:volume relationship (Chapter 3) . This
gives smaller organisms a physiological advantage at low
nutrient concentrations and is presumed to be why small
species of phytoplankton prevail in oligotrophic waters.
Small phytoplankton species have a greater surface
area:volume ratio than larger species.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Box 2.6: Iron and high-nutrient, low-
chlorophyll regions
In some areas of the world's oceans the supply and
assimilation of ni trogen, phosphorus, and carbon appear
not to be linked. In these waters the phytoplankton stand-
ing stocks are never large enough to assimilate the N and
P in the surface waters fast enoug h to deplete them at
any tim e throughout the year. These are the 'high-nut rient ,
low-chlorophyll' (HNLC) waters of the subarctic Pacific,
the Sou thern Ocean, and the equatorial Pacific.
Several hypotheses have been proposed to explain
HNLC regions, including suggestions that in these regions
light (either low or damaging high light intensity) limits
production to a degree that inorganic nutrients are not uti-
lized or that grazi ng pressure limits the standing stocks of
phytoplankton. Whereas these factors clearly do playa ro le
to varyi ng degrees, the most compelli ng explanation is that
the rate of supply of iron, an essential trace element for
phytoplankton growth, is limited.
Dissolved iron concentrations in offshore areas are
extremely low, since the primary source of iron to the
surface waters of the oceans is from the land, either via
atmospheric dust deposition in offshore areas or di rect
depositions from land masses. Atmospheric dust depo-
sition in the two major HNLC areas- the Antarctic and
equatorial Pacific Oceans-are the lowest in the world.
Conversely, in the equatorial North Atlantic, which receives
large amounts of dust from the Sahara, iron concentra-
tions are sufficient for the complete assimilation of available
nitrates and phosphates.
. -- ...
....... ~e:S N.E~ .......
/ ~ -- . .
....... - ,
,
1
'..-. ....
• I
2.7 Supply of inorganic nutrients
In the late-1980s, John Martin developed the idea that a
lack of iron is the cause and laboratory experiments con-
firmed how vital iron is for phytoplankton growth. A series
of experiments in the Equatorial Pacific Ocean, where large
areas of the ocean (hundreds of square kilometres) were
seeded with iron, led to substantial increases in phyto-
plan kton growth. In particular, diatoms grew and it appears
that not all phytoplankton species are equally iron-limited
(Martin et al. 2002). Several oceanographic expeditions
showed that , during spring in the Southern Ocean, phyto-
plankton bloom in iron-rich waters but do not in waters with
limited iron reserves (de Baar et al.1995). It was pertinent
to therefore extend the Pacific iron-fertilization experime nts
to the Southern Ocean. Several studies have now 'fertil-
ized' Antarctic water bodies and in all of these diatoms
did bloom in response to the added iron. This growth was
in turn responsible for the absorption of significant quanti-
ties of carbon dioxide from the water during the experi-
ment (Boyd et al. 2000; Buesseler et al. 2004; Coale et
al. 2004). Much of this work is synthesized by Boyd et
al. (2007). An extension of this work has been to investi-
gate regions w here natural upwelling water into iron-poor
surface waters is responsible fo r enhanced phytoplan kton
activity, such as on the Kerguelen Plateau in the Southern
Ocean (Blain et al. 2007; Pollard et al 2009).
It is this link between the phytoplankton growth and draw-
down of atmospheric carbon dioxide that fuels a vigorous
debate about these experiments. There is a concern that
these results may be viewed as providing a simple answer
for mopping up excess carbon dioxide, thereby curbi ng
the effects of increasing greenhouse gases. It is thought
A satellite image of an iron-fer-
tilized patch during the Eisenex
expedition to the Southern Ocean
in 2000. The sparse phytoplank-
ton outside of the patch is strik-
ing compared with the abundant
growth of phytoplankton within
the patch following fertilization.
The satellite image shows the
increase in chlorophyll (orange/
red) compared to the waters sur-
rounding the patch (blue). (Image:
Philipp Assmy & Joachim Henjes,
AWl Alfred Wegener Institute.)
 Chapter 2 Primary Production Processes

by some that by spreading iron over huge swathes of the
ocean, enhanced phytoplankton growth would effectively
trap carbon dioxide. Such ideas about large-scale ecological
engineering have little to do with the work of the scientists
conducting the experiments. Iron fertilization is in fact a poor
way to tackle greenhouse gas problems. Calculations show
that iron fertilization of the Southern Ocean would not in
fact be an effective mechanism fo r carbon dioxide removal.
Levels of carbon dioxide are increasing at such a rate that ,
even by maximizing biological uptake in these oceans by
addi ng iron, there would still be a net increase in atmos-
pheric carbon dioxide (Chishol m et al. 200 1; Buesseler et
al. 2004). Much of this de bate is add ressed in a special
issue of the journal Oceanus (volume 46 published in Janu-
ary 2008).
The real interest of th is work co mes fro m the implica-
ti ons for the understandi ng of the atmospheric carbon
dioxide levels in past cli mate history. This new evidence
supports the theory that low amou nts of atmospheric
carbon dioxide (measu red in ice cores taken in the Arctic
and Antarctic) during past ice ages may be linked to high
amounts of iron in Antarctic waters that suppo rted large
standi ng crops of phytoplankton.

( HNLC = high-nutrient, low-chlorophyll.
Lack of iron may limit the growth of phytoplankton in
HNLC regions.
Iron-fertilization experiments have resulted in increased
phytoplankton growth within the fertilized patches.
Fertilization of the oceans with iron is not in any wayan
easy fix for combating rising atmospheric carbon dioxide
concentrations.
) It has been estimated that for cells less than 1 urn in
diameter, molecular diffu sion is adequate for the resup-
ply of nutrients, but for larger organisms it is a major lim-
iting factor. Therefo re mechanisms for reducing the DBL
around the organism are key to the nutrient metabolism
of aquatic organisms. Movement through the water, eit her
by sinking or swimming, means that the nutrient-depleted
bound ary layer is dragged with the organism, causing fluid
from the layer to be she ared away. This can then be replaced
by nutrient-replete water. Clearly the velocity and magni-
tude of distance travelled will affect the degree of replace-
ment. However, it is estimated that swimming significantly
reduces d iffusion-limitation only in organisms greater

(I) 131

151

Figure 2.15 An y property of an organism that alters the organism 's size and/or shape w ill alter the properties of the
diffu se boundary layer (DBL). Therefore the variety of shapes and form s of phytoplankton shown here will have very
different sinking rates as well as different characterist ics of the DBL surrounding the cells, co lo nies, o r chains. Starting
from t op-left and moving clockwise the images are: (1) Dity/um brightwellii, (2) Ceratium tripos & Rhizoso/enia sp.,
(3) Eucampia zodiacus, (4) Guinardia flaccida , (5) Chaetoceros s ocia/is, (6) Coscinodiscus sp. (photographs: Ian Lucas).
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

than 100 urn diame ter. In many of the organisms between

-- -
1 and 100 urn diame ter, movement is a means of relocating
into regions of higher nutrient concentration, rather than
address ing diffusion-limitation by altering DBL properties.
Any property of an organism that alters the organ ism's size
and/or shape will alter the properties of the DBL. The re-
fore, organisms that form colonies or chains, such as the
diatoms, change their shape and therefore sinking rate, and
also the characteristics of the DBL surround ing the colony
or chain (Fig. 2. 15) .

The diffusive boundary layer is key to determining nutri-

ent supply to a cell, or surface of a macroalga.
In the case of macroalgae and seagrasses, relief or struc-
tures on the thallus or frond surface will cause eddy forma-
tion and turbulent motion of water passing over the surface
(see also Chapter 8). This will have the effect of reducing
DBLs and therefore enhancing nutrient exchange. As mac-
ro algae and seagrasses cannot move in the water column
by swimming or sinking, they rely on modification of the
water movement across their surfaces to enhance nutrient
exchange (Fig. 2. 16) . Seagrasses are also able to t ake up
nutrients from the sed ime nts throu gh their root and rhi-
zome systems.
Ridges and structures on the surface of a macroalga can
increase the rate of exchange of nutrients and dissolved
gasses.
Naturally on exposed and turbulent wave-infl uenced
waters, water exchange is never going to be a problem. In
sheltered waters with little water movement, diffusion-lim-
itation of nutrients becomes more of an issue. For example,
the giant Pacific brown seaweed (Nereocystis luetkeana)
has smooth blades in rapidly moving water, but in more
sheltered waters its fronds are ruffled . The ruffled blades
serve to increase the turbulence as water passes over them,
thereby increasing nutrient supply and gas exchange to the
fronds. In faster moving waters the ruffled blades would
increase the risk of tearing because of their increased drag;
instead the seaweed's smooth blades tend to form stream-
lined bundles that are not so easily damaged.
Figure 2.16 Structures o n the surfaces of macroalgae ,
such as the ripples on thi s Macrocystis pyrifera, can cau se
turbulent water movements over the surface of the frond s.
This will increase the exchange of gases and inorgan ic
nutrients compared with when undisturbed lamina flow
passes over the surface (photograph: David Thomas).
2.8 The main limiting nutrients
for growth
The main products of photosynthesis are sugars, reductant
(t he product of reducing enzymes), ATP, and oxygen, which
are themselves substrates in further biosynthetic pathways
(Table 2.2). The other m ajor inorganic nutrients needed
for the myriad of molecules that make up a living organism
occur in seawater as different chemical species :
Nitrogen: N0 3, NO l , NH: , NH3 , Nz' and urea.
Phosphorus : HPO'.;", PO';, and, H,PO•.
Sulphur: 50'.;", H, 5.
Particular nutrients are critical for certain organisms,
alt ho ugh not limiting for photoautotrophs in general.
An example is silicate, for diatoms and silica-scaled
prymnesiophytes (and some cysts of some dinoflagellate
species) , which is present in several forms as well: H4 Si0 4 ,
H3 SiO. , and H3 SiO•.
Nitrogen and phosphorus are the main growth-limiting
nutrients in marine systems.

Table 2.3 Typical percentage biochemical and elemental composition of algal cell s.

Biochemical "!o of an algal cell "!oC "!oH "!o0 "!oN "!oP "!oS
Carbohydrate 40 44 6 49
Protein 40 53 7 23 16 1
Li pids 15 69 10 18 1 2
Nucleic acid & nucleotides 5 36 4 33 17 10
 Chapter 2 Primary Production Processes

The balance of these forms of anyone element is highly

,
.....'. o
,• • ·.'•• •-
•
•
--• 0

• ... .
o 0
•
dependent on many complex biogeochemical processes.
'.
•• ••
'. •• • -'If • •
'. ,:
• . ' • • #~ • • , ,
• It ~ . ... ..
'.
....
•
~ • "•
f,.
- •
o

,'. - -.
Many of the trace nutrients are actually only mostly found • 0 "
o r
! ' . .. • , •
,." •
. ~
in complexed forms wit h organic compounds in seawater •, • • , • •
• • " ,••
(Table 2.3). The nutrient demands of individual species . -, , '..
• • I . ••• • I , ••
•
• •
•

are n aturally a reflection of its biochemical demands and

composition. Clea rly the proportion of the relative macro- •
• .0•.
• •• • ,
•
'.. , 1
. ..., -,... .
•
..
' ..
• 0 •

•
-: ' '!. •
'
•

molecules, e.g. lipid (cf, nucleic acid) , will determine the

elemental composition of the cell and the relative demands
• 0
••
•
• •
• • • •
• ., . •
. ' 0 -

•I . .
•

•
'J
•
~
to ... "~ •
, I
o .

• :.'•
• ••
· •
for C, N, and P for growth. Although there is great variation
in the composition of the cell, the functioning of the cell
• ·.. . .
"
.
'
-':,
. '.
.
'
•
• "-
:-
•
:
•
" o•

(i.e, the requirements for metabolism (enzymes-proteins)

and reproduction (nucleic acid), sets constraints on the rel-
ative proportions of the various macromolecules, and con -
sequently the relative requ ire ments for carbon, nitrogen,
and phosphorus during photosynt hesis.
2.8.1 Elemental composition of algae
There are obvious nutrient demands that are virtually uni-
versal, and these will be discussed here. However, it must be
stressed that in many instances it is not the major ino rganic
nutrients (Table 2.4) that may limit growth, but rather the
rate of supply of trace elements that restrict the growth
rates (Box 2.6) .
A typical algal cell is 400;0 protein , 400;0 carbohydrate ,
15% lipid , and 5% nucleic acids.
Typically, marine phytoplankton are comprised of more
than 40% protein, 5% nucleic acids and nucleotides, 40%
carbohydrates, and 15% lipids. These proportions can vary
greatly depending on the inorganic nutrient supply, age of
the organ ism, temperature, and irradi ance cond itions. In
particular the lipid fraction can vary cons idera bly during
the lifetime of a phytoplankton cell, being < 10% in expo-
nentially growing cells and increasing to > 25 % in cells in
the station ary phase of growt h, where nutrients are lim-
Figure 2.17 Epifluorescent photom icrographs of Nile-red
st ained diatoms that sh ow the lipid droplets within the
cells v ery clearl y (from Pri scu et at. 1990).
ited. In some cases there can be so much lipid production
that the lipids can be seen as oil droplets with in the cells,
and is one of the reasons algae have been the recent focus
as possible biofuel sources (Fig 2.17 and also see Current
Focus: Us ing algae for carbon sequestration and algal bio-
fuel production) .
It is straightforward to categorize the average composi-
tion of the organic materials within the phytoplankto n. If
we rewrite the simplified photosynthesis equation to take
into account the need for nitrogen (mostly supplied as
nitrate) and phosphorus (sup plied as phosphate) we get:
106CO, + 16NO, + HPO~- + 122H,o + 18W
=> CI06H 2630 n oN16P + 13 8 0 2
Typically from the equ ation a bove , the ratio of
carbon:nitrogen:phosphorus in healthy, actively growing
algal cells is 106:16:1 . This ratio is referred to as t he Red-
field ratio, after the oceanographer A. C. Redfield. There-
fore the typical C:N ratio is 6.6 :1. This is a commo nly used
parameter to measure the physiological status of algae,
since when nitrogen is limited, or the algal cells are senes-
cent or dying, the ratio increases considerably (Burkhardt &

Table 2.4 The major function s o f so m e select ed inorganic nutrients.

Nutrient Examples of functions

Nitrogen Major metabolic impor tance, structural ami no acid, p rotei n metabolism
Phosphorus Structural in pa r ticular membranes and energy metabolism
Potassium Osmotic re gulat io n, protein stability
Calcium Ion transport, enzyme activation, stru ctural function
Magnesium Ion transp ort, enzyme activation, pigments such as ch lorop hy ll
Sulphur Stru ctu ral function, active in enzyme activity
Iron Active in enzyme activity
Sodiu m Ion transp ort , osmoregulation , enzyme activation
Manganese Electron t ransport and membrane structu re
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
Riebesell1997; Lenton & Watson 2000; Geider & la Roche
2002).
The Redfield rat io, carbon:nitrogen:phosphorus
106:16:1.
The quotient of CO 2 to 0 2 from the above equation is
1.3. This is known as the photosynthetic quotient (PQ)
(Williams 1998) . This quotient is highly dependent on the
state of oxidation/reduction of the nitrogen source. When
nitrate is taken up by an algal cell it has to be reduced within
the cell to ammonium before it can be utilized in cellular
metabolism (Fig. 2.22) . Algae can also take up ammonium
(NHt) directly as a nitrogen source. avoiding the energy in
the reduction stage when nitrate is assimilated (see below) .
Therefore growth on ammonium is about 19% more effi-
cient on comparing the PQ values. The resulting PQ is lower
at around 1.09.
Ocean ode allile and death
CO, -Althe balance poinl-
I
CO2 + nutrients • Organic maUer
Primary productian
106 CO, + 122 H,O + 16 HNO,+ H,PO, - [((H,OIi" +INH,I" +H,PO,] + 138 0,
CO2 + nutrients Organic metter
Organic (
Bauam
Figure 2.18 Primary production and decomposition
(respiration) are driving the biogeochemical pathways
w ithin marine systems in an almost closed 'grand cycle'
(from Cullen et al. 2007).
PQ = the moles of 0 2 evolved per moles of CO 2 assimi-
lated.
It must be stressed that this discussion of elemental
ratios and typical cell composition is oversimplified. The
cell composition (and therefore elemental ratios) will vary
greatly at different life-history stages, and with changes in
the prevailing temperature, light, and nutrient status. For
example, in older phytoplankton cells there is a marked
switch from carbohydrate production to the accumulation
of lipid reserves. When there is a lack of nitrogen in the
surrounding water, protein synthesis is suppressed and the
IS relative proportion of lipid and carbohydrates increases.
2.8.2 Carbon
The supply ofinorganic carbon for photosynthesis and algal
growth is seldom (if ever) limiting in marine systems. How-
ever, the role of oceans in the global carbon cycle has been
the focus of intense study in the past decades, especially in
relation to increasing carbon dioxide in the atmosphere as
a result of anthropogenic activity (Box 2.3) .
The biggest pool ofcarbon in the oceans is that locked up
in the sediments, which is, globally, about 10 million Giga-
tonnes (Giga is x 10 9 ) . In comparison there are about 39
000 Gigatonnes ofdissolved inorganic carbon in the various
forms discussed above. The next largest pool is that con-
tained within the dissolved organic carbon (DOC) pool at
about 700 Gigatonnes. It is striking to compare these num-
berswith the 30 Gigatonnes ofcarbon contained within the
particulate organic carbon (POC) pool, which contains all
of the organisms from bacteria to blue whales within the
world's oceans (Fig. 2.19) .
30 Gigatonnes of carbon is contained in all of the partic-
ulate phase biology compared to 700 Gigatonnes in the
dissolved organic carbon pool and 39 000 Gigatonnes
in the inorganic carbon pool.
Carbon expressed as
C Atmasphere 750 ~
Gigatonnes
Oissolved orgonic
carbon (Ooq Inorganic
carbon
- 700
-39000
Partiwlate organic
"rhan (Poq
- 30
(living -3)
Biogenic (arbon in surface marine sediments - 3000
Figure 2.1 g Schematic to show the major pool of
carbon within the oceans. Particu late organic carbon
(poq includes all organisms from bacteria-sized particles
to whales. Dissolved organic carbon (DOC) is generally
considered to be all carbon that can pass through a 0 .2
urn fi lter. (Image: Ruben Lara)
 Chapter 2 Primary Production Processes
There are many algae that deposit calcium carbon-
ate (CaCO,) in their cell walls, sometimes together with
smaller amounts of magnesium and strontium carbonates.
In the phytoplankton, the most conspicuous group of algae
to exhibit calcification are the coccolithophorids that pro-
duce external 'shells' composed ofcalcium carbonate plates
called coccoliths (Brownlee & Taylor 2002) . These small
phytoplankton species are common in all seas, although
not as abundant in polar oceans. They can form extensive
blooms where the ocean surface turns a milky white. One
of the better-known species ofcoccolithophorid is Emiliana
huxleyi, which can form blooms in the North Atlantic cov-
ering an area of the ocean equivalent to the size of Great
Britain (Fig. 2.20) . The coccoliths sink and are incorpor-
ated into sediments. where they can accumulate in huge
amounts locking up CaCO, (Young & Ziveri 2000) .
Some microalgal and macroalgal species have calcified
cell walls.
Normally when phytoplankton bloom there is a draw-
down of CO 2 due to the assimilation through photosyn-
thesis. However, the production of calcium carbonate
structures by coccolithophorids can actually result in CO 2
being released to the atmosphere due to the formation of
the calcium carbonate:
Ca2+ + 2HCO, => CaCO, + CO2 + H,o.
There are also many examples of calcareous brown, red,
and green macroalgae, i.e. species that have deposited cal-
cium carbonate in the form of calcite or aragonite crystals
within their tissue. This can be so extensive that these spe-
cies can be important in the formation oftropical atolls and
help to cement coral reefs together (Chapter 11) . Calcite
and aragonite never occur together in the same alga. and
there is still some debate as to the metabolic processes that
acrually lead to the deposition. In some calcifying species
the crystals are laid down outside the cells, such as in the
green Halimeda, which causes aragonite crystals to pre-
cipitate in the spaces between the cells. In the fan-shaped
brownPadina. aragonite is precipitated in concentric bands
on the outer surface of the thallus. The corallines such
as Lithothamnion and Lithophyllum, on the other hand,
deposit calcite within their cell walls to the extent that the
cells become encased, except for the cellular connections
(Fig. 2.20) .
In some coral reef systems over 70Ofo of the reef can
be made from calcified macroalgae.
Calcification is related to photosynthetic activity and, in
particular, the effects of pH on the dynamics ofcalcium and
carbonate and bicarbonate in seawater. Certain polysaccha-
rides in algal cell walls can actually block crystal growth
and stop calcification taking place. The ability to produce
these polysaccharides in the cell walls is the likely reason
why calcification is not ubiquitous in marine algae and that
relatively so few species are calcified.
Figure 2.20 (a) Planktonic coccolithophorids ('round-
stone-bearers'), such as this Coccolithus pelagicus,
synthesize exquisitely sculptured calcium carbonate cell
walls known as coccoliths (photograph: Jeremy Young,
Natural History Museum, London). (b) This MODIS
satellite true-colour image shows the blues and greens
of phytoplankton blooms occurring around Denmark, in
the North Sea on the left, and within the Baltic Sea on
the right. The bright blue colour of the North Sea bloom
is thought to be a coccolithophore-bloom reflecting blue/
white due to t he reflection of li ght by the coccoliths
(image: Jacques Descloitres, MODIS Land Rapid Response
Team. NASA/Goddard Space Flig ht Center, Visible Earth).
(c) Several species of macroalgae have calcified cell walls,
such as those comprising this maerl bed. Several species
of coralline algae form maerl beds, which are often found
at depths of 0-35 m, although in some parts of the world
free-living calcified macroalgae have been found at depths
down to 200 m (photograph: Bill Sanderson). (d) More
commonly seen calcified macroalgae are the encrusting
red species (with lichen-like growth forms) and articulated
Corollina offlcinalis combining here to form a vivid pink
fringe surrounding an intertidal rockpool (photograph:
David Roberts).
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

CURRENT FOCUS: Oceans as carbon 2 . As more CO2 is absorbed by the oceans, there w ill be
sinks and ocean acidification reduction in the pH of the seawater and a correspond-
ing decrease in the carbonate ion concentrat ion (see
Seawater is undersaturated with CO2 compared with the figure be low) , which results in the process commonly
atmosphere and so there is a continual process by which referred to as ocean acidification.
CO2 diffuses acro ss the air-ocean surface and dissolves to
for the dissolved inorganic carb on (DIC) pool. The solubil- Since the Industrial Revolution in the 1700s it is esti-
ity of CO 2 in seaw ater increases as temperat ure decreases mated that the oceans have dropped in pH by about 0 ,1
and so a greater amount of CO2 dissolves in the Arctic and pH unit and it is pred icted that by 21 00 the w orld 's oceans
Southern Oceans than in temperate and tropical waters may have undergone a further decrease of about 0 .4 p H
(Takahash i et al. 2009), units (Zeebe et al. 2009),
Coupled to this 'solubility pump ', the oceans also 'take
A!nmpllere 5urfo(e «eon [C01(oq)I COt l
up ' CO 2 due to photosynthetic assimilation. Ultimately this pro,
(ppm) pH (p mol l-' )
assimilated carbon is transported to the deep oceans as
700 8.3 ss 300
par ticulate matter sinks to the depths, although of course pH
30 250
600 8,'
a con siderable amount of the organic matter produced is ~b~iness OS" u~uol~ [COt ] 25
500 8,1 '00
respired through microbial activity (see Chapter 3 ) . The 15920scenario 10 150
400 (IP(( 1995) 8,0 15
uptake of CO2 by the biology of the oceans and removal to 100
7,9 10
300 [(O!" II \0
deep waters is referred to as the 'b iological pump '. In par t 5
'00 7,8 0 0
the oceans are mitigating against the well-recorded increas- 1850 1900 19511 2000 1050 2100 18511 1900 19511 2000 2050 2100
ing atmospheric CO2 concentrat ions, primarily driven by Year y~,

anthropogenic greenhouse gas release, by absorbing CO2

Predicted changes in atmospheric CO2 to the year 2100
through both th e solubi lity and biolog ical pum ps. However,
and associated changes in ocean pH and carbon chem-
there are two obvious problems ident ified in future global
istry, Adapted from Wolf-Glad row et al. 1999,
climate change scenarios (IPCC 200 7a, b, c) :

1. As oceans warm , they will absorb less CO2 from the At th e moment, th e surface of th e oceans is saturated
atmosphere since the so lubility of CO2 is less in warmer in the vari ous mineral fo rm s of calcium carbonate (e.g.
water.

10' '" 60' 80' 100' 110' 140' 160' 180'1 60' 140' 110' 100' SO' 60' '" 10' 0' 10'

60' 60'
\0' '/'.. \0'
",;e~ ~'0
40'
]0' ./-'-""'-" , ]0'

10' ?/'.:;, 10'

10' 10'
0' 0'
10' 10'
10' -T..h'-4;#'f 10'
]0 ' ]0 '

,,' \0' \0'

,,'
~
60'

10' '" 60' SO' 100' 110'140' 160' 180' 160' 140' 110' 100' SO' 60' '" 10' 0' 10'
@ill 2008 Apr I 13:42:53 1

- 108 - 96 - 84 - 72 - 60 -48 - 36 - 24 - 12 0 12 24 36 48 60 72 84 96 108

Net Flux {arums(m- 2 vear- 1)

Climatological mean annual sea-air CO 2 flux (g carbon m-2 year'] for the reference year 2000 (non-EI Nino condi-
tions). The map is based on 3.0 million surface water pC0 2 measurements obtained since 1970. Thi s yields a net
global air to sea flux of 1.42 Pg carbon year: ". Adapted from Takahashi et al. 2009.
 Chapter 2 Primary Production Processes

calcite and aragonite) and these minerals do not dissolve;
whereas in deeper waters, where the waters are under-
saturated in calcium carbonate minerals, they do dissolve.
Because of the lowering of pH of ocean waters and the
parallel reduction of carbonate ions, the surface waters
are becoming less satu rated in calcium carbonate and it
is predicted that in the next 150 years the carbonate-
saturated surface waters in some regions, especially cold
polar waters, may disappear altogether (Feely et al. 2004;
Raven et al. 2005).
Such changes will bri ng about considerable change to
all organisms that utilize calcium carbonate as part of their
body skeleton or external structures. This clearly includes
the corals and molluscs, but also planktonic forami nfers and
calcareous phytoplankton such as the coccolithophores
(section 2.8.2). The poten tial effects of such changes are
well reviewed by Orr et al. (2005), Fabry (2008), Fabry
et al. (2008), and Browman et al. (2008).
A very good example of the debate about what the
effects of ocean acidification may have on marine organ-
isms is exemplified by work carried out using coccolitho-
phores. Riebesell et al. (2000a) produced some highly
convincing results that showed that there was very reduced
calcification in Emifiana huxfeyi grown in response to
increased CO 2 loadi ng in laboratory cultures. They also
showed that in the more acidic conditions, the coccoliths
(calcium carbonate plates) were more deformed than in
those formed in normal pH conditions.
This culture work was followed up by Iglesias-Rodriguez
et al. (2008) who showed that calcification and primary
production of E. huxfeyi were increased in cultures grown
in more acidic waters and they interpreted their results
as showing that already populations of E. huxfeyi were
already respondi ng to decreased pH surface waters. They
also backed this up with addi tional field evidence to show
how the average coccolith mass has increased over the
past 220 years.
The apparent discrepancy between the Riebesell et al.
and Iglesias-Rodriguez et al. results is an excellent example
of the difficulties in trying to answer a pote ntial simple
question such as: what do increased CO2 conditions do to
calcification in a species of coccolithophore? As described
by Fabry (2008), there are several explanations for the
discrepancies, including methodological issues on how to
realist ically change CO2 conditions in laboratory cultures
(also see Riebesell et al. 20 10). Maybe the most compel-
ling explanation is that both groups were actually experi-
menting on different species of algae, or at least different
populations of a single species with very different physi-
ological properties.

(a), (b) , (d), and (e) Emiliania huxleyi; (c) and (I) Gephyracapsa oceanica collected fram cultures incubated at [CO,I
12 pmol 1-1 (a-c) and at [CO,] 30-33 pmol 1-1 (d-I) , corresponding to Pcoa levels of about 300 p.p.m .v. and 780
to 850 p.p.m.v., respectively. Scale bars represent 1 I-Im. Note the difference in the coccolith structure (including
distinct malformations) and in the degree of calcification of cells grown at normal and elevated CO 2 levels. (From
Riebesell et al. 2000a.)
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

2.8.3 Nitrogen
Nitrogen is present in seawater as dissolved molecular
N" ammonium (NH.i), nitrite (NO,), nitrate (NO,), and
as organic forms such as urea, amino acids, and a diverse
range of complex dissolved organic nitrogen (DON) com-
pounds (Fig. 2.21) . In seawater, ammonia (NH,J exists as
a mixture of the ammonium ion (NHt ) and NH 3 " At sea-
water pHs (approx. 8) over 95% is in the form ofNHr, With
increasing pH, the relative contribution of NH3 increases
(e.g. at pH 9, NH: is about 75%) .
Nitrogen is the element that most frequently limits pri-
mary production in the oceans. Only some cyanobacteria,
such as Trichodesmium species can reduce (fix) nitrogen
gas, and these species thrive in waters where other forms
of nitrogen are limited and thus re strict the growth of
other phytoplankton (Berman-Frank et al. 2001) . How-
ever, they still need sources of other nutrients, such as
phosphate.
Nitrate is the primary form of nitrogen assimilated by
marine primary producers.

, -_ _ Regenerated Fishand _ Blooms of nitrogen-fixing cyanobacteria are a feature

NH. + ethers of oligotrophic waters (particularly oceanic tropical coast-
=-c-t---,-,- lines), where nitrogen is present in the water in very low
I,.,"'h.m'""I concentrations, thereby restricting the algal growth. Other
Phytoplankton nitrogen fixers are also found growing on and in sediments
II in coastal regions, saltmarshes, and estuaries, as well as in
the roots of seagrasses and other saltmarsh grasses (e.g.

Rjv~
c
o
..•- Spartino spp.), where the nitrogen fixed by the cyanobac-
teria also supports the growth of the plants. In general, Nq-

-"
•• .~
z is the primary source of nitrogen utilized by algae, although
NO, and NH: can also be taken up (Fig. 2.17) . Whatever

~-~-~--L~~~J
the original source of nitrogen, NHt is the form utilized in
Newnltrogen • Biota
cell metabolism and NO, and NO, have to be reduced by the
enzymes nitrate reductase and nitrite reductase within

"
Oenltrificllfion
the cell:
N0 3 ---t nitrate reductase ~ N02 nitrate reductase
I
NOl" ===ni1rificolion
NO£ - N~ - NH. + ~ NHt

More recently reported for marine systems is the Anam-

Figure 2.21 Schematic of nitrogen in the ocean including
input, transformation, and loss terms.
Only some species of cyanobacteria can fix nitrogen gas
directly.
mox process (Anaerobic ammonium oxidation) which is
thought to account for large amounts of the Nz production
in sediments and other suboxic systems (Fig 2.23 and Ward
et al. 2007) . In this process, NH: and NO, are converted
by the anammox bacteria into Nz. This is an important
pathway in the marine nitrogen cycle, since it may account
for why most of the NH1, which should theoretically be

NO -
, 3
Nitrate redudnse
,
NO -

Urea Urea Cell wall -

- Nitrite reductase
llrecse

Figure 2 .22 Highly simplified schematic of

-CO,
_ _ _ _ NH/ / Aminoacids ~
major routes of nitrogen uptake and cellular
Ie)
transformation of inorganic nitrogen into ,
NH + Aminoacids

amino acids by algae. -.. Amino acids

 Chapter 2 Primary Production Processes
,
NO ~
_I \ ;,-,.
,
NO ~
4
N,O
N,
1 2.8.4 Phosphorus
Primary - ....- Heteronepbs
NH'
. ~
.....1 - -
producers
Assimilation
Figure 2.23 Principal features of the marine nitrogen
cycle: 1, Anammox, invo lving the generat ion of N2
from inorganic constituents by autotrophic microbes.
2 , Nitrogen fixation . 3, Nitrification. 4 , Heterotrophic
denitrification, in which N2 is produced from N0 3 - used
in microbial respiration of organic substrates; th is
process also results in the production of NH/ and
CO 2 (not shown). 5, Dissimilatory nitrate reduction to
ammonium (DNRA). N0 3- :::; nitrate; N02 - :::; nitrite;
N20, ::: nitrous oxide; NH4 + :::; ammonium (from Voss and
Montoya 2009).
produced from the remineralization oforganic matter in the
oceans, is unaccounted for (summarized by Arrigo 2005) .
As previously stated, changes in PQ indicate that pro-
duction based on ammonium is 19% more efficient than
production based on nitrate. In fact, in some algal spe-
cies nitrate uptake is inhibited when there are significant
ammonium concentrations in the water. This inhibition is
thought to be brought about by the inhibition of the nitrate
reductase activity within the cells.
Primary production based on nitrate is referred to as
new production. The breakdown, decomposition, and
respiration of organic matter (Chapter 3) releases a range
of other nitrogen species, ammonium, nitrite, and urea,
and even amino acids that can be used as nitrogen sources
for primary production. Primary production based on non-
nitrate nitrogen sources is called recycled production.
The ratio of new production to total (new and recycled)
production is called the f-ratio . The average global value is
between 0.3 and 0.5. However, in oligotrophic deep ocean
sites, where there is little input of fresh ni trate into the
upper mixed layer from below, the values can be well below
0.1 (Chapter 9) . In contrast, in coastal regions or sites of
coastal upwelling, where input of nitrate can be high, t he
f-ratio can be up to 0.8 (Chapters 7 and 8) . The inverse of
the f-ratio gives th e number of times the element recycles
per year, i.e, an f-ratio of 0.3 implies that an average nitro-
gen atom cycles around 3 times per year.
The f-ratio is the ratio of new production to total (new
and recycled) production.
3
Following nitrogen, phosphorus is the second most com-
• mon limiting nutrient in marine systems. However,
<:» NH '
• in phosphorus-limited systems there is evidence that at
Exuetion least cyanobacteria adapt their metabolism to produce
higher proportions of sulphur and sugar-based membrane
lipids instead of phospholipids in order to decrease the
cellular demand for phosphorus (Dyhrman et al. 2007) .
Phosphate occurs in several inorganic forms in seawater,
HPO~~, PO;, and H2PO<, although at pH 8 and a tempera-
ture of 20°C HPO~- accounts for 97% of the free ions and
it is inorganic phosphorus tha t is most bioavailable for cell
uptake and metabolism. Phosphorus is also present in a
diverse range of organic compounds (organic phosphates),
and these are generally classified together within th e dis-
solved organic phosphorus (DOP) pool. These can be bro-
ken down by enzymes (phosphatases) that are located in
the membranes of many algal species. Phosphate limitation
may also result in algae releasing alkaline phosphatases
into the surrounding water to break down nop. When
external concentrations of inorganic phosphate are high,
th e production of alkaline phosphatases is repressed (see
review of Dyhrman et al. 2007) .
Phosphorus can also limit primary production in some
marine systems.
2.8.5 Sulphur
Sulphur is rarely a limiting nutrient as seawater is rich in
sulphate, but it is a vital nutrient, primarily for amino acid
and protein synthesis (Sievert et al. 2007) . Curiously, in
some macroalgae, such as th e brown Desmarestia, the cells
contain such high concentrations of sulphuric acid within
their vacuoles that the low pH of the tissues deters grazers.
Many species of macroalgae also contain large quantities of
sulphated polysaccharides in their cell walls.
Several phytoplankton species, as well as red and green
macroalgae, produce a specialized compound, dimethylsul-
phonioproprionate (DMSP), which is used as an osmolyte
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

in osmoregulation, a storage product, and possibly an anti-
freeze compound (Fig. 2.24) .
DMSP is cleaved into DMS and acrylic acid.
Intracellular DMSP is released into the water either
directly orthrough grazing activity (Fig 2.18) . In the water
column the fate of the DMSP is varied depending on micro-
bial dynamics. but a certain amount produces dimethyl
sulphide (DMS) . Most of the DMS in the water is converted
to DMSO (dimethyl sulphoxide), SO~-, and S, only < 5%
being exported to the atmosphere, but still DMS released
from phytoplankton and macroalgae accounts for most of
the no n-marine salt sulphate in the atmosphere. The subse-
quent oxidation ofDMS to sulphur dioxide and subsequent
formation of aerosol particles and cloud condensation
nuclei is part of a complex system of localized and global
climate control (Stefels et al. 2007) . High concentrations
of DMSP are also known to deter grazing of phytoplankton
by protozoans (Wolfe 2000) .
DMS is important in the production of cloud condensa-
tion nuclei.
The most prolific producer of DMSP in coastal waters is
the planktonic colonial alga, Phaeocystis (Box 2.7) and in

~ud albe!V

- - \
••
, -• -
Direct - -
__< IDMSO algae I release r-.-: -
;-::_ _
-. -'-\~9ical axidatian/~)-L-:~:::::::::-/
Photochemicalan I
DMSOdiss I

YXidati~ IDMS I ~ Q edumo.v

DMSP algae Excretion
DOMmerel thial
, & lysis Enzymatic cleavage Bialngical
•• complexes
, -"'-"', consumption
: Salinity
Light DMSP bacteria
Temperature r0gesti~
Bacterial amino
Nutrients MeSH
ocids & proteins

DMSP grazers Excretion Demethylation

Elimination

Figure 2.24 Schematic representation of the processes and pools involved in the marine biogeochemical cycling
of DMSP and DMS. Dominant ro le of functional groups in the different processes is indicated by coloured ellipses:
green, phyto plankton; blue, zooplankton; red, bacteria; black, abiotic factors. eeN, cloud-condensation nuclei; DOM,
dissolved organic material; DMSO, dimethyl sulphoxide; MeSH, methanethiol; MPA, mercaptopropionate; MMPA,
met hylmercaptopropionate; MSA, methanesul phonic acid. Dimethyl sulphide released from phyto pla nkton and
macroalgae accounts for most of the non-marine salt sulphate in the atmosphere, and the oxidation of OMS to sulphur
dioxide and the subsequent format ion of aerosol particles and cl oud condensation nuclei is part of a comp lex system
of localized and global climate control (from Stefels et a l. 2007).
 Chapter 2 Primary Production Processes

ocean ic waters Emiliana huxley i (Stefels et al, 2007) . When now includes the species previously called Enteromorpha )
these algae bloom, there is a characteristic stench of DMS have high concentrations of DMSP. and following a rain
in the air, resulting from the breakdown of DMSP to DMS. shower during low tide, t he DMS released from t he Viva
Likewise intertidal green macroalgal species of Ulva (which spp. ca n be quite pungent.

Box 2.7: Phaeocystis a foam producing
alga
In the North Sea in late spri ng/early summer, a curious
event takes place where considerable quantities of foam
are washed up on the shore, which normally result in
repor ts of pollution spills. Nothing could be further from
the trut h, since the foam is the natural result of the break-
down of the colo nial stage of the one of the Phaeocystis
spp.
Any marine b iologist or biological oceanographer who
has had to filter water samples taken during a Phaeocys-
tis bloom will animatedly curse the stuff, since tryi ng to
filter even just a few millili tres of seawa ter laden wi th the
colonies of this prymnesiophyte (haptophyte) is a very
slow process indeed.
Phaeocystis spp. have two phases: a free-livi ng motile
stage and a colonial stage. It is the latte r tha t is the surge
of any fil tration exercise. The colonies (up to 10 mm in
diameter) are embedded in a gelatinous matrix surround-
ing a hollow centre and the whole colony is covered in
a tough me mbrane (Hamm 2000). The membrane has
po res less than 5 nm and this effectively protects the
colonies from viruses, bacteria, and/or protists.
After a bloom of Phaeocystis, when the gelati nous
material of the colonies breaks down, a considerable
amount of organic matter is released into the water. When
th is organic 'soup' is agitated by tu rbulence and wave
action, it fo rms a foam that gets washed up on the shore.
It has been estimated that Phaeocystis spp. contri bute up
to 10% of the global marine primary production or around
4 b illion tonnes of carbon. Up to 50% of this carbon is
in the fo rm of the colonial gel matrix and so up to 2 bil-
lion tonnes of gel (or rather extracellular polymeric sub-
stances, see Chapter 3) are released into coastal waters
from this one genus of algae (Schoemann et al. 2005;
Verity et al. 2007).
Phaeocystis spp. are not only notorious for their gels,
but also for being prolific producers of DMSP and there-
fo re DMS to the atmosphere (Stefels et al. 2007; Verity
et al. 2007) .

(a) Phaeocystis is a cosmopolit an group of species that have a colonial phase of th eir life history (Photograph
Dolors Vaqu e), (b) When Phaeocystis bloom s end, th e colonial st ages break up releasing large quantiti es of di s-
solved organic matter into coastal wat ers. When mi xed up by w ave acti on this is transformed into co p ious amounts
of foam that can wash up on beaches, causing unnecessary public co ncern (p hotograp h: Dav id Thomas).
 2.8 The main limiting nutrients for growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 2.8: Ultraviolet radiation damage

Ultraviolet radiation is able to penetrate into the surface waters, and in regions where there is seasonal ozone
depletion , damaging amounts of UVR can result in macroalgae and m icroalgae having to repair cell damage and
change their physiology to produce screening compounds (photograph: David Thomas).

Ultraviolet radiation (UV: UV-A wavelength 320-400 nm
and UV-B 280--320 nm) can damage RNA transcription
and DNA replication, and, in particular, UVB radiation
can damage the photosystem II of photosynthetic organ-
isms, severely limiting photosynthetic carbon assimilation
and therefore growth (Buma et al. 200 1; Helbling et al.
2001). Some accessory pigments have a photoprotective
role, and these are used to protect cells from damagi ng
high light levels and also harmful UV radiation . Concentra-
tions of these are usually low in light-limi ted algae, but
fo rm rapidly when the algae are transported into high
light environments or high levels of UV radiation .
The effect of UV stress on many phytoplankton and
macroalgal species is to produce UV screening agents
such as f3-carotene, mycosporine-like amino acids
(MAAs), and photoprotective carotenoids (Hannach &
Siglo 1998). These effectively act as sunscreens pre-
venting damage to cell structures and DNA (Aguilera et
al. 2002; Hoyer et al. 2002). The general response to
increased UV radia tion is a combination of a complex
suite of cellular mechanisms, including protection, repair,
cell size, growth rates, and photo-acclimation. Interspe-
cific differences in response to this complex of factors will
dictate any changes in phytoplankton composi tion. There-
fore, the most likely scenario due to this environmental
change is a shift in species composi tion or successional
patterns (Vincen t & Roy 1993).
One of the few generalizations that seem to be pos-
sible to make is tha t small cells are more vul nerable to
UV radiation damage (Karentz et al. 199 1; Buma et
al. 2001). This is due to t heir surface area to volume
ratios and the low effectiveness of screening pigments
in small cells, al though Helb ing et al. (1992) fou nd
that UV radiation inhi bited microplankton more than the
nanoplankton.
It is not simply the amount of UV radiation that is
damaging. This is because extremely low-light adapted
algae are more susceptible to UV damage than algae
grown in high light environments. Therefore, algae grow-
ing in shade or low-light habitats suddenly exposed to
high levels of UV radiat ions are highly susceptible to UV
radiation damage. This may occur when subtidal stands
of macroalgae are exposed on very low spring t ides or
phytoplankton cells are transported from deep waters to
surface waters.
To complicate our understanding about UV effects on
primary production there are some reports that indicate
that U~ especially UV-A, can actually enhance photosyn-
thesis in some species of phytoplankton, and Gao et al.
(2007) have calculated that, by ignoring the positive
effects of UV radiat ion on primary production, estimates
of primary production in tropical regions may have been
underestimated by as much as 13%.
 Chapter 2 Primary Production Processes

2.9 Algal growth
The ultimate growth of an organism is a result of the bal-
ance between the energy input and the necessary energetic
costs for cell processes to take place and of course repro-
duction to maintain the following generation (Fig. 2.25) .
The energetic gains, investments, and losses of individual
organisms include the following :
• Material and energy gains: photosynthesis or chemo-
synthesis.
• Material investments: skeleton formation, production
of energy storage compounds, and formation of repro-
ductive material.
• Energy and material losses: movement, buoyancy,
excretion, osmoregulation, nutrient uptake, and respir-
ation .
A range of UV-absorbing compounds are produced by
algae in high UV conditions to prevent cell damage.
Growth is the expression ofthe integration ofall ofthese
losses and gains, within an organism. Thus, in general form:
Growth = Material and energy gains - Material and
energy losses .
This growth can be measured in material (mass) terms,
e.g. dry weight, wet weight, or in energy terms, kJ.
One of the striking features of algal growth is that sig-
nificant amounts of the carbon assimilated during pho-
tosynthesis are released as excreted organic matter (see
dissolved organic matter, Chapter 3) . This varies greatly
in composition from organic acids, such as glycollate, to
vitamins, polysaccharides, fatty acids, amino acids, pro-
teins, and simple carbohydrates. There are reports that up
to 70%of carbon assimilated during photosynthesis can be
excreted, but in general most values lie between 0 and 20%.
Up to 20% of the carbon assimilated during photo-
synthesis can be excreted as dissolved organic carbon
(DOC).
Some algal species increase the excretion of organic
matter towards the end of a bloom, or when light and!or
nutrients become limited. In contrast, laboratory experi-
ments have also shown that excretion of organic matter
continues at a constant rate of about 10%. This excretion
also continues during darkness and so is uncoupled from
photosynthetic activity (Fig. 2.26) .
2.9.1 Nutrients and growth
Algae can grow at high rates, given an adequate supply of
light and no limitation in nutrient supply. Phytoplankton
growth is usually expressed as the rate of cell division or
increase in biomass per unit of time. In ideal conditions,
small picoplankton can divide to produce up to 3 generations
per day (ct. bacteria growing in ideal conditions can divide
every 20 minutes, or 72 generations per day) . For most phy-
toplankton maximum growth rates of 0.3 to 1 generation
per day are more usual. However, in natural conditions the
growth rate is better reflected by the net rate of change in
numbers or biomass including the gains due to reproduction
and losses due to mortality or export from the system.
Typically phytoplankton divide at 0 .3 to 1 generation
per day depending on the temperature and nutrients
available.

Photosyntheti( ,,
(orban ,,
assimilotion ,,
,
Portirulate = :Algal biomass

~
•
:,, '-...... .. •
'
.' •

Energy in ,, I .........

Energy
or losses
.>: respiration
ond other
,,, ~
,.J ............
.' ,
.........
." 1

in exuetory metebelk
, .. ,,
......... 1 Filtrafe ,l= Excretion
,
products demands ,• • .'•
'
,,, ,,
..'
.. ' .",
,, ,, ,,
,
•

Growthl Ught Dark light Dark

production
Figure 2.25 The net carbon used for growth or
production of a primary producer is a product of the
photosynthetic assimilation minus several loss terms (c.f.
Chapter 3).
Figure 2.26 Carbon assimilation by phytoplankton during
light and dark periods. In the light, carbon is assimilated
by the cells (particulate fraction) , but not during the dark.
In contrast, carbon continues to be excreted by the cells
(collected in the filtrate) in both the light and dark.
 2.9 Algal growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

The growth of phytoplankton can be expressed by the

following equation (from Richmond 2004) :
N t =N2"
0

where No is the starting number of cells. Nt is the number

of cells after time t (the original No + the cells produced
and n is number of doublings or generations) . Therefore
the time needed for the cells to double is given using the
following equation (where td is doubling time,) :
N t =N0 2"" d

Rearranging the equation:

NINo =2"" d

or using the natural logarithm: 100

In (NINo) = (ln2) t/td

Time -
or:
(bJ
In (NINo)lt = 0 .693/t d Growth phases
The term Ji is called the specific growth rate (which is spe- lao Exponentiol Stotionary Death
cies-specific and depends on temperature, irradiance levels, ,, ,,
and nutrient concentrations) :
=
I- , I
Ji = 0 .693/t d· ...•
~
Therefore if the growth rate (Ji) is 0.69 per day, the doubl-
ing time (r) would be 1 doubling per day.
When growth is described by the equation: I

Time •
the growth of the population is exponential, and if natur-
allogarithms of both sides of the equation are taken, the (eJ
equation describes a straight line (Fig. 2.27a), the slope of
which is u:

InN, = fit + InNo • :;: 11,,, - - - - - - - - - - - - - ~~~~~:':':~==~1

However. no population can continue growing exponen-
tiallyfor an indefinite period. Typically, exponential growth l=
ends following the utilization of one or another essential = ~

j "iJ1
l
nutrient. When this happens a stationary phase is reached MOI ----
,,
where there is no net increase or decrease in cell numbers ,,
(Fig. 2.27b) . It is important to note that, although there ,,
is no growth of the algal population, the cells continue to
,,
,,
metabolize and produce and/or turnover cellularproduets.
There may even be some cell division (growth), which is K, Nutrient concentration (N) •
balanced by the numbers of cells dying during this phase.
Figure 2.27 (a) The growth rate of a phytoplankton
Ultimately, as the stationary phase extends. the percentage
culture expressed on both arithmetic and logarithmic
of the cells dying increases and thereafter the population
scales. (b) Idealized growth curve for a phytoplankton
enters a death phase.
population. (c) Relationship between nutrient
concentration (N) and the growth rate of a primary
Typically phytoplankton divide at 0 .3 to 1 generation
producer. flmlJJf, is the maximum growth rate, KN the nutrient
per day depending on the temperature and nutrients
concentration at which growth rate is half the maximum
available.
(0.5 Jlmur-the half-saturation constant.
 Chapter 2 Primary Production Processes

If light and temperature conditions remain unchanged,
and losses due to grazing are not important, growth of algae
is mostly limited by the availability of nutrients. The effect
of nutrients on algal growth is described by the following
equation :
where S is the concentration of the nutrient and KN is the
half-saturation constant, or the concentration of the nutri-
ent at which:
J1 = Jimax / 2.
This is a Michaelis-Menten relationship (as was the
relationship between photosynthesis and irradiance, see
above) , and so whe n at low nutrient concentrations, the
rate of increase in growth rate increases rapidly with ris-
ing external nutrient concentration (Fig. 2.27c). At higher
concentrations, increases in nutrient concentration add
progressively less to the growth rate until the maximum
growth rate is reached and further increases in nutrients
do not affect the growt h rate.
Each species of phytoplankton present in a body of water
(may be many tens to hundreds of species at any one time)
has a species-specific growth rate (J1 and J1 max ) ' and also a
species-specific half-saturation constant (K N ) for all of the
nutrients it needs to assimilate. This is one of the reasons
why many different species of phytoplankton can coexist in
a water body (Box 2.9) .
Previously in the ch apter it was described that small
algae, such as the picoplankton, most efficiently take up
nutrients because of diffusive boundary effects. Small pho-
toautotrophs such as these also tend to grow at faster rates.
Therefore why isn't there anything else but the picoplank-
ton? The answer is that in the discussions here, we have
ignored a major controlling factor limiting algal stand ing
stocks, namely, grazing by protozoans and zooplankton. In
aquatic systems, grazing pressure exerts a major control on
the dynamics and distribution of photosynthetic organ isms.
Photosynthesis provides the organic material for respira-
tion , while for its part respiration provides the inorganic
nutrients for photosynthesis.

Box 2.9: Nutrient dynamics and

In the first examp le (a) , species 1 has a hig her J1 max than
phytoplankton growth
spec ies 2, but both have the same KN• In th is case both
species grow at the same rate unt il a certain level of
1'1
nutrients, after which speci es 1 continues to grow further
until it reaches its maximum growth rate. In this case spe-
cies 1 w ill dominate at nutrient concentrat ions greater
than those at KN .

11.... 51 > 52 In (b) , both species 1 and 2 have the same value of
J1 max ' However, spec ies 1 has a lower value of KN t han
KH constant
species 2 . In th is case, species 1 reaches its maximum
(bl growth rate at lower nutrient concent rat ions than spec ies
--cs, 2. Therefo re, in low nut rient concentrat ions, species 1

-
--•
~

~
w ill dominate, altho ugh at higher nut rient conditions both
spec ies will grow equally.
-=-
0
=
·0
In the third example (c), spec ies 1 has a higher J1 ma x
than speci es 2, but the latter has a lower KN t han species
~ II .... constant
=
~
1. At lower nutrient concen trations species 2 grows faster
K,51 < 52
and dominates because it reache s its maximum growth
('I rate at lower nut rient concentrat ions. However, at higher
52 dominates - :- 51 dominates
, nutrient concentrations, species 1 dominates because of
,,, 51
its greater maxi mu m growth rate.
.....-- 7"' - - - - - 52
Examples of possible variations In nutrient growth
p .... 51 > 52 curves of competing pairs of phytoplankton with dif-
ferent specific growth rates (,Li) , maximum growth rates
(,Limax) and half saturation constants (~) for nutrient
• uptake (from Lalli & Parsons 2004).
Nutrient
 2.9 Algal growth
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 2.10: Definition of productivity
terms
There is a set of definitions used in ecology that derive
basically from th ree physiological processes, namely:
1 = P.
Photosynth esis
2 Algal respiration = Ra •
3 Whole community respiration = Rc '
The pri mary photosynthetic event is termed Gross
Production = P.
The difference between productio n and respiration in
the algal community is te rmed Net Primary Production
(also Net Photosynthesis) = P - Ra '
The difference between production and respiration
within the whole community is termed Net Community
Production (also Net Ecosystem Production) = P-R c '
Net Primary Production tells us how much energy
and organic materi al is available to the heterotrophi c com-
munity, whe reas Net Community Production tells us
about the balance wi thi n the community as a whole, i.e.
whether the community is g rowi ng o r contract ing. It is
important not to confuse these terms and the use of net
production, w hich is co mmonly fo und in the literatu re and
could refer to either, is to be avo ided.
Fo r a number of reasons the two processes of pho-
tosynthesis (P) and respiratio n (R) are out of phase, so
there will be places and times when and where P > R
and R > R The difference between these two processes
(P) - (R) is te rmed net community production (NCP)
(see Box 2.5 regarding the critical depth). Unlike photo-
synthesis and respi ration, net community production is
not a process in its own right: there is not a dedicated
set of enzymes or a single metabolic pathway tha t gives
rise to NCP; rat her it is an arithmetic difference. Never-
theless it is arguably the most valuable plan ktoni c rate
measurement we can make, and is the best descrip tor of
the waxing and waning of the population. Net community
production should be distinguished from the similar te rm
net primary production (NPP; also referred to as net
photosynthesis: see 2.8), which is photosynthesis minus
autotrophic respi ration. Ari thmetically NPP > NCR

CURRENT FOCUS: Using algae for carbon sequestration and algal biofuel
production
Under ideal conditions of light and replete nutrients, micro-
algae can grow at high rates and achieve high biomass.
For several decades there have been numerous industrial
driven research initiatives desig ned to intensively cult ivate
microalgal cultures on a large scale. This has successfully
been done in b ioreactors and shallow ponds/ raceways for
the cultivation of algae for the nutraceut ical industry and
fo r biomass pri marily for aquaculture feeds (http: / /www.
algae.wu r.nl / UK/Welcome/). In the past ten years there
has been renewed vigor in research into the large-scale
growth of algae as a potential source of lipids that can be
converted into biof uels and/or as a way of sequestering
CO 2 from industrial processes.
The case fo r the latter is a co mpelling one, since from
a basic knowledge of Redfield ratio and the equations
for photosynthesis and respirat ion it can be calcul ated
that for 0.8 tonnes of algal b io mass produced, 1.8 tonne
of CO2 will be assimilated. For this amou nt of algal b io-
mass to be produced there would need to be about Large-scale cultures of algae can be grown in bioreac-
45 kg of nitrogen and 4 kg of phosphorus added to the tors s uch as these, which ca n be expanded to fill large
system, as well as lower amounts of othe r maj or and areas of land or in greenhouses. The key is to keep the
trace nutrients. This addi tional requi rement for nutrients tubing narrow enough to maximize the light penetra-
besides CO2 is one of the key factors to be considered in tion (photograph: David Thomas).
 Chapter 2 Primary Production Processes
any economic analysis as to the viability of growing algae
in a sustainable way. Using industrial fertilizers clearly
adds a considerable cost to the product (algal biomass)
and generates no greater benefit than growing normal
efficient terrestrial crop species. However, if the algae
can be grown utilizing nutrient-rich waters from industrial,
municipal waste outlets, then of course the whole process
becomes more tenable.
In terms of carbon sequestration, of course, just pro-
ducing biomass is not enough, but something has to
be done with the biomass. As pointed out earlier in the
chapter, algae do produce lipids and in several species
at various stages of growth and/or under specific envi-
ronmen tal conditions, lipid content can increase over 20%
of the biomass. The attraction of easily growing lipid-rich,
high-biomass 'crops' of algae for biofuel production has
achieved much attention. However, it should be stressed
that in exponentially growing cultures of the vast majority
of algal species, the lipid content is relatively low « 10% of
the total biomass). As compelling as the concept is, w hen
all the costs of production, includi ng cost of nutrient addi-
tions, energy to remove the water from the cell suspension,
energy to extract lipids from the biomass, and the costs of
The potential use of large-scale cultivation of algae is hardly a new idea. Over 50 years ago this image was a
rather fanciful idea about how massive algal farms could be set up in space to satisfy a future demand for human
nutrition (Image from the journal Mechanix Illustrated, May 1954).
processi ng the remaining biomass, it appears difficult to
see how biofuel production from algae can be competitive
compared to the intensive cultivation of oil-rich terrestrial
plants. See debate between Reijnders (2008) and Christi
(2008) and further insight by Weyer et al. (2009).
In any design for a facility for growing on the industrial-
scale, it is important that light does not become limiting
to growth. This nat urally dictates where on th e planet
such systems are viable wi thout th e additional cost for
ar tificial lighting. The cell cul tures will become dense and
th erefore 'shelf shadi ng ' will prevent even illumination of
all cells in a suspension. This effect can be minimized in
one of two ways:
1. Growing t he cell suspensions In shallow ponds in
which the algae are well mixed to ensure that they do
not settle.
2. Growing the cell suspensions flowing through trans-
parent t ub ing narrow enough to ensure th at light can
penetrate to the middle of the tube, even when the
cell suspension is very dense, but not so narrow that
the shear stress acting on the cells actually causes the
cells to be damaged (Richmond 2004).
 2.11 Global trend in primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

2.10 Seasonal trends in ,/ , \ ·L

~
primary production j~ 11
.. ~
In nature it is impossible simply to consider the limitation of ~
• L I
algal growth in terms of a single factor, as in the examples ~
~ 100 j~ -,
given above (Jickells 1998). Although only one nutrient :i• L .~~
1'"
~
•
may limit the growth of an alga at anyone time, whether or d j~
r
-g
not an alga will grow will depend also on other growth-lim- :U J j~~ .~
iting factors of which the most important is light. No matter "?e ~l ~ , -- ,
what the nutrient concentration, if there is not enough light ~ /' /\
"

I
.
E! .i. ' ,/ - ~ ~
..:!I.t:; I I
I \

.S! .~
_ 1 I ' ,

to reach maximum photosynthetic rates. growth rates will -ci I I ' , ',
::B1
~

be compromised. By contrast, if there is plenty of light to

z
'y , I
I \
I

\~,
I
I I

:: ,,-\ J
I ,
I I
I,
'\ .
...

saturate photosynthetic systems. but there are no nutrients. ,,,

II " \ ,
, I,
I, I
' ,I , I \ ,
growth will not take place. This is most vividly shown in
,,
I, I 1
I,
, ",I \
I I \

the seasonal phytoplankton growth dynamics in temperate ,II

(mid to h igh latitude) waters in which seasonal thermal
stratification of the water column takes place that is pre-
sented in Chapter 3 .
2.10.1 Succession of phytoplankton
• years (from Barnes & Hughes 1999).
species
When we measure phytoplankton dynamics in terms of
increases in chlorophyll or particulate organic carbon
concentrations in the water, there is the great danger in
forgetting that these changes are the result of the growth
through cell division of a number of phytoplankton spe-
cies. Different phytoplankton species dominate at different
times of the year. and this succession of dominant phyto-
plankton species is thought to be controlled by a complex
mosaic of factors. such as temperature, irradiance, growth
rates, and nutrient supply (Box 2.9; Fig. 2.29) . Added
to this is the influence of grazing by protozoan a nd zoo-
plankton species, which can have a major role. It is impor-
tant to note that this succession is not the same as that
Sea 5Urf,re
--• Ihermedlne
Nutrient limitation
- N.
c
,
,
,
J FMAMJ JA SOND
Month
Figure 2 .29 Seasonal succession of dom inant
phytoplankton species in t he Irish Sea averaged over 14
described for terrestrial systems. where species' succession
results in a climax community (Sommer 1989; Roelke &
Buyukates 2002; Worm et al. 2002) .
Many species make up the phytoplankton, and there is a
succession of species throughout a bloom or from one
season to the next.
Even within a 'bloom' event. there is a succession of spe-
cies, even though blooms normally start by the explosive
growth of an individual species. During the course of a
diatom bloom, silicate is taken up by the diatoms to build
silicate frustules (Brownlee & Taylor 2002) . As the concen-
trations of silicate fall in the water due to this uptake. there
can be a progression from large diatom species to small dia-

'E
Nutrient tom species that have less demanding silicate requirements
~
~
c
~
flux

<,
I
Chlorophyll moximum
for growth.

I
Ugh! llmitollcn
I production
Figure 2 .28 In stratified waters nut rients may become
limiting in the surface waters. However, nutrients may
diffuse from deeper waters upwards across a thermocli ne.
If this layer is in the euphot ic zone (above the critical
dept h) phytoplankton growth can occur, lead ing to the
formation of sub-surface chlorophyll layers.
2.11 Global trend in primary
When considering primary production on a global scale.
the advent of satellite colour images ofchlorophyll distribu-
tion around the globe have been very successful in showing
us that primary production is far from uniform at a large
scale (McClain 2009) . Indeed, large-scale patterns in pri-
mary production are partly used to define distinct regions
or biomes of the world's seas (see Chapter 8) . Ultimately
there are four major factors that govern primary production
in marine systems (Falkowski et al. 1998) :
 Chapter 2 Primary Production Processes
• Ught-only available in the upper part of the water col-
umn (max 200 m) .
• Nutrients- that can be exhausted in upper water lay-
ers, but are generally available in the deeper part of the
water column.
• Stability- to allow algal growth in surface water layers.
• Mixing- to replenish used nutrients from lower water
layers to surface.
Ultimately it is the physics of a water body that controls
the primary production.
These controlling factors are somewhat conflicting, and
in areas of high primary production it is the physics of the
water body that gives rise to circumstances that enable
these conflicting requirements to be met.
There are many ocean processes that influence nutrient
supply to surface waters. which vary greatlyin time and size
scale. These range from storm events that effectively mix
stratifiedwaters in shallow waters through to global thermo-
haline circulation patterns (Chapters 7, 8, and 12) that mix
deep ocean waters to the surface after about SOD years or
more. These are also significantly influenced by cyclical
oceanic events, such as EI Nino Southern Oscillation and
North Atlantic Oscillation events (Chapter 7) .
In tropical and subtropical waters, there is normally
permanent thermal stratification due to the high degree
of solar heating of the surface waters. Irradiances in these
_ > 500 L--...J1250-500 1_ _ 1100-250
Figure 2.30 The annual primary production as g carbon m-2 year:' of the oceans from a global perspective (see also
Chapter 1).
waters are high, and the clear waters result in light passing
deep into the water column (>200 m) . These conditions
are of course conducive to high primary production, but
because of the lack of mixing of inorganic nutrients from
the deeper waters, tropical waters generally only support
low primary production, although at a rather constant level
throughout the year. When storm events do mix surface and
deeper waters, phytoplankton blooms can result from the
input of nutrients. Likewise tropical waters are sensitive to
eutrophication processes, since when nutrients are intro-
duced, the high light levels support a rapid build-up of pri-
mary producers.
Tropical waters have generally low primary production
due to low surface water nutrient concentrations.
In contrast, in the polar oceans there is significant mix-
ing of nutrient-rich lower waters with the surface waters.
However, these regions are characterized by long times of
the year when day length is short and sun angles shallow.
Therefore, primary production in these waters is limited
by irradiance, and generally there is a single peak of pri-
mary production when light is high enough to support net
gain in algal growth. There are differences in the nutrient
status of the Arctic and Southern Oceans. In the latter, the
major nutrients (nitrogen and phosphate) are in excess, but
primary production is restricted due to limitation of iron.
In the Arctic, nutrient limitation does occur following the
annual late-spring/summer plankton bloom.
__I < 100
 2.11 Global trend in primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Upwelling of nutrients in nutrient-rich waters is charac-

Primary production in polar waters is restricted to short
teristic of several coastal regions. Offshore winds give rise
seasonal windows when light is available.
to offshore transport of nutrient-depleted surface water
that is replaced by upwelling nutrient-rich water, sup-
As described above, temperate waters are character-
porting high rates of primary production. Upwelling also
ized by a suite of complex seasonal dynamics of light and
occurs at major ocean frontal systems in the open oceans,
thermal stratification. These seasonal variations impart a
such as the equatorial regions where north-east and south-
distinctive seasonality in primary productivity: spring and
east trade winds generate two westerly flowing surface
autumn blooms of phytoplankton, with low standing stocks
currents: the North and South Equatorial Currents. The
of phytoplankton in summer and winter.
Coriolis effect causes the currents to be deflected north-
Large oceanic gyres are a conspicuous feature of the
wards in the northern hemisphere and southwards in the
Atlantic, Pacific, Indian, and Southern Oceans. In the
southern hemisphere. The divergent flow of these surface
northern hemisphere these gyres move in a clockwise direc-
waters from the equator promotes nutrient-rich water
tion and anticlockwise in the southern hemisphere. These
upwelling, supporting higher rates of primary production
anticyclonic gyres tend to deepen the thermocline, mov-
(Fig 2.32 and also see Chapter 7).
ing water towards the centre ofthe gyre. Therefore nutrient
replenishment into surface waters does not take place, and
these anticyclonic gyres tend to be regions of low primary
productivity (Chapter 7) .

Figure 2.31 A large gyre off the east coast of Japan
in this SeaWiFS image shows the concentration of
phytoplankton associated with the physical structure
(image provided by the SeaWiFS Project, NASA/Goddard
Space Flig ht Center, and GeoEye).
Anticyclonic gyres are regions of low primary production
whereas cyclonic gyres sustain higher rates of primary
production.
However. cyclonic gyres (anticlockwise in northern
hemisphere and clockwise in southern hemisphere) actu-
ally result in water being mixed from below the thermo-
cline into surface waters, due to water being transported
outwards from the centre of the gyre. Therefore. in such
gyres, higher rates of primary production are supported,
due to the mixing of nutrient rich water into surface waters
(Fig 2.31) .
Figure 2.32 Upwelling of nutrient-rich water resu lts in
phytoplankton blooms to the west and south of South
Africa (image provided by the SeaWiFS Project, NASAl
Goddard Space Flight Center, and GeoEye).
Regions of upwelling are important sites of high primary
production.
Coastal waters and waters overlying continental
shelves ( < 200 m) supportthe greatest primary productiv-
ity. This is because many coastal waters are shallower than
the critical depth (see Box 2.5) and also because coastal
waters receive large amounts of growth-limiting nutrients
from river inputs into the coastal zone (Jickells 1998) .
There are many different types of frontal systems in shelf
seas, and these tend to be associated with increased pri-
mary production, e.g, fronts associated with river plumes
and shelf-sea fronts (tidal fronts), where the water column
 Chapter 2 Primary Production Processes

(a) (bl

Figure 2.33 (a) Fronts can be zones where concentrations of biology are found, either as a result of physical
concentration or by increased growth of organisms. Here there is a huge concentration of photosynthetic ciliate
Mesodinium rubrum in the surface waters of a front in the North Sea, as well as bird feathers and green macroalgae
concentrated on the water's surface (photograph: David Thomas). (b) Frontal systems are enhanced zones of biological
activity, as seen here by the whales and birds feeding on planktivorous fish at a front (photograph: Michel Kaiser).

changes from being tidally mixed to being stratified. 1YJli-
cally the dense accumulations of plankton that occur at
fronts attract feeding aggregations offish, birds, cetaceans,
and fishers (Fig. 2.33; Chapters 7 and 8).
Frontal systems tend to be regions of enhanced biologi-
cal activity, either from increased primary production or a
concentration of organisms through physical processes.
The high standing stocks of plankton at tidal fronts may
simply result from physical concentration by the water
dynamics in the frontal zone. However, the conjunction
of two separate water bodies can result in an exchange of
nutrients (or other components) from one body of water
to the other.
2.11. 1 Global ocean primary
productivity
Global ocean net primary productivity estimates are numer-
ous and varied (Geider et at. 2001) . Most of the variability
is largely to do with the methods used to measure ocean
primary production. and the different metabolic processes
that these methods quantify. The most recent estimates
based on satellite images of phytoplankton biomass in sur-
face waters tend to range between 40 and 50 Pg carbon
year-' . Recent estimates of terrestrial primary production
are between 50 and 60 Pg carbon year" which, combined
with the oceanic primary production. gives a total primary
production on Earth of c.lO' 6 g carbon year' (Box 2.11 &
Table 2.5).
Marine and terrestrial primary production are roughly the
same at approximately 50 Pg C 'f'.
We can measure the distribution of phytoplankton from
satellites in space (McClain 2009; Fig. 2.3) . Like all pho-
tosynthesizing organisms, the algae contain chlorophyll.
With modern-day satellites, it is possible to estimate the
chlorophyll concentrations in the surface waters of the
world's oceans and therefore monitor the growth of the
phytoplankton.
Macroalgae can produce up to 14 kg carbon m- 2 r '.
Although phytoplankton productivity is much less than
that of macroalgae per unit area, on a global scale total
phytoplankton productivity is far greater than that con-
tributed by macroalgae.
 2.11 Global trend in primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 2.11: Comparison of terrestrial

and aquatic primary production
The amou nt of bacterial, algal, or plant biomass (p r im a ry
producers) built up over t ime th rough the process of
photosynthesis is generally referred to as primary prow
duction . This is normally expressed as the amou nt of
carbon fixed by photosynthesis, per unit area of space or
volume, per unit of time. Most estima tes are expressed
as net primary production, which takes into account the
costs of respiration as well.

Net primary production = Total photosynthetic carbon

assimilation - respiration carbon losses.

The production per square metre of seaweeds and

seagrasses is equal to, or in many cases greater than,
that of terrestrial plant based systems. For instance Lami-
naria spp. dominated communities have annual produc-
t ivity rates of approximately 2 kg carbon m 2 year'. and
the macroalgal sea palm Postefsia has been estimated to
produce up to 14 kg carbon m- 2 year 1 . These estimates
contrast with those for mature rainforests and intensive
alfalfa crop production ( 1 to 2 kg carbon m- 2 year").
and temperate tree plantations or grasslands and prairies,
which are generally less than 1 kg carbon m- 2 year: ".
Coastal phytoplankton annual production is also gener-
ally less than 1 kg carbon m- 2 year: ". One study estimated
the annual productivity of all the seaweeds in a 1-m wide
strip of shoreline, 360 m long, was c.600 kg carbon year".
Macroalgae can be very productive, and Laminaria spp.
dominated communities have annual productivity rates
of approximately 2 kg carbon m- 2 yea r' (photograph:
David Roberts).
An equivalent productivity by the phytoplankton in a l -m
wide strip of the adjacent seawater would requi re a stretch
of water extendi ng out 3.4 km from the shore. From fig-
ures like these it would be easy to think that the seaweed
production is more important than that of phytoplankton
production to the overall productivity of the oceans. How-
ever, compared to the vast area of the globe covered by the
oceans (80%) in which phytoplankton grow, the seaweed
covered strips of coastlines are rather small and at best can
be viewed as sites of intense localized production.

Table 2 .5 Comparison of annual primary production between marine and terrestrial systems. It must be
stressed that at best these values are good estimates, but they do allow a comparison of the magnitudes of
primary production from various components of the biosphere.

Domain Global annual roduction

Marine
Tempe rate westerly winds 16 .3
Tropical & subtropical trade winds 13.0
Coastal waters 10 .7
Polar 6.4
Marshes/estuaries/macrophytes 1.2
Coral reefs 0.7
Terrestrial
Tropical rainforests 1 7 .8
Savannas 16.8
Cultivation 8.0
Mixed broadleaf & needle leaf 3. 1
Needle leaf evergreen forest 3.1
Perennial grasslands 2.4
Broadleaf deciduous forests 1.5
Needleleaf deciduous forest 1.4
Broadleaf shrubs wi th bare soil 1.0
Tundra 0.8
Desert 0.5
*P = peta, and 1 Pg is equivalent to 10 15 g.
 Chapter 2 Primary Production Processes
2.11.2 Are the oceans net
heterotrophic or net autotrophic
There is still a tendency to regard great areas of the ocean
as biological deserts. This particularly applies to the c.4000
m of water that lies between the base of the euphotic zone
and the deep-sea sediments, which is often seen as merely a
transit zone. As there is no photosynthesis beyond about 200
m, metabolism at these depths must be supported primar-
ily by transport of organic material out of the euphotic
zone. and marine snow (Chapter 3) plays an important role
in this transfer. The organic content of these settling par-
ticles is depleted during their descent, so we may expect a
general decrease in activity with time and therefore depth.
Conventionally the oceans are divided into five depth
zones (Chapters 6 to 8) :
1. Epipelagic zone, from the surface to 150 m, for all
intents and purposes synonymous with the euphotic
zone.
2. Mesopelagic zone (150 to 1000 m) .
3. Bathypelagic zone (1000 to 4000 m) .
4. Abyssopelagic (4000 to 6000 m) .
5. Hadal zone (6000 to 10000 m) .
We have no information of the rates of respiration in the
two latter zones but we are beginning to build up a picture
of the upper three zones (Aristegui et al. 2005; Robinson
and Williams 2005) . A summary of rates for these three
oceanic zones, the oceanic sediments, as well as the coastal
90 uni~ recycled Primary production
in surface ~
y lflllunits
water
...- - 1000 --- - - - - - - - - - - - - - - - - - - - - - - - - - - - - -
7-9 units recycled in
10 units sink aut of photic zane
mid-depth, , -
~ <I unit preserved in sediments
Figure 2.34 Very little of the carbon assim ilated in the
euphotic zone through primary production actually gets
sequestered in the sediments, since most of it is respired
as it sinks; see Chapter 3 (redrawn from Cockell et al.
2007).
zone is given in Table 2.6. Not surprisingly. close to 90% of
metabolism occurs in the epipelagic zone of the open ocean,
of the 10% or so that passes out of the epipelagic zone, all
but a small fraction is respired away during its transit to the
sediments (Fig 2.34) .
The amount accumulating in the sediments is minute
by comparison: 1 and 12 Tmol carbon year', in the oce-
anic and coastal sediments, respectively; onlyO.1% of the
total oceanic carbon flux. Moving from the surface into the
deep water, there appears to be a shift in the balance of
metabolism between the micro-organisms and the larger
organisms. The present estimates are that in the euphotic
zone. the respiration associated with the metazoans as a
whole is about 10% of the heterotrophic micro-organisms.
whereas in the mesopelagic and bathypelagic zones the
fraction is nearer 30%. This perhaps at first is surpris-
ing as these zones would seem to the zone of the detriti-
vores, until one realizes that, unlike the micro-organisms.
the metazoans (the fish, copepods, and the euphausids)
are highly mobile and are not confined to this zone but
undertake extensive vertical migrations. in many cases on
a diel frequency (Chapter 7), so they are able to visit the
rich feeding areas of the upper ocean during their nightly
excursions. As they will defecate and lose organic material
by other routes during their time in deep water, the zoo-
plankton are a vector for transport oforganic material
from the surface to depths, thus supplementing the pas-
sive rain of organic particles.
Respiration rate (as mmal 0 2 m-' 11-1)
Epipel,gi, 0.005 0.01 0
zane -T::-:--:=:'~;:~;::;:~~=====:2:===]
Mesopelagic zane
_ 2000 --
oS
""=
e- Bathypelagic zane
3000 --
4000
Abyssapelagic zane
Figure 2.35 The vertical distribution of respiration in the
dark ocean. Redrawn from the equation given in Aristegu i
et al. (2005).
 2.11 Global trend in primary production
••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •••••••••••••••••••••••••••••••••••• •••••••••• ••••••••• •

Table 2.6 Estimates of respiration for major zones of the oceans. Data f rom del Giorgio and Williams (200 5).

Depth zone Depth Global annual respiration (T' mol carbon yea....') Contribution to open
range (m) ...... .... ..... .... ..... .... ..... .... .... ..... .... ..... .... .... ..... .. ocean respiration (~o) *

Coastal zone Open ocean

Epipelagic 0- 150 1200 9000-12000 88
Mesopelagic 1 50-100 0 600-1400 8.5
Bathypelagic 1000-4000 160 - 2 30 2
Sediments 12 1 30- 18 0 1.5

Total 1200 10 000-1 4 000

"T _ tera _ 10 12 ,
• Number s rounded off.

Beyond a depth of about 200 m, metabolism must be
supported primarily by transport of organic material
from the euphotic zone.
Zooplankton are a vector for the transport of organic
material.
The oceans are not closed as they receive organic mate-
rial from land and freshwater ecosystems, via the rivers,
and they lose material to the marine sed iments. There
are also exchanges with the atmosphere but t hey are very
small and can be ignored. The loss to the sed iments is small
compared to overall turnover, the input from the rivers is
greater (curre nt estimates give a figure of 34 Tmol carbon
year'), but still remains a small component (c.0 .3%) of
the overall cycle. The diffe rence between the inp ut along
w ith the rivers and loss to t he sediments (c.20 Tmol car-
bon year') , i.e, the net supply, represents t he extent to
which ocean ic respiration and photosynthesis can be out
of balance. We can assess t he overall gains and losses to the
oceans from the outside qu ite simply and wit h mo re than
adequate accuracy. This simple so-called mass balance cal-
culation (see Table 2.7) leads us to the conclusion that there
is a net input of about 20 Tmol carbon year-' to the oceans.
So, if the oceanic system is in some form of equilibrium, as
we believe it to be, then res piration will exceed photosyn -
thesis by this amount, as this net import of material, along
with marine photosynthesis, has to be consumed within the
ocea nic system. Thus, the oceans are most probably net
heterotrophic wit h respiration exceeding photosynthesis
by about 0 .2%.
What we find , when we compare t he consens us est i-
mates of oceanic photosynthetic production of 50 to 60 Pg
carbon year! (4000 to 5000 Tmol carbon year!) wit h the
estimated sum of the respiration (10 000 to 15 000 Tmol
carbon year'), is a very different story: a massive differ-
ence between estimates of photosynthesis and respiration.
To some small extent we are not comparing like with like,
as the estimate of respiration (the total removal of organic
material) should be compared with the to tal production
of organ ic material (gross production), whereas the esti-
mate of production from 14 C techn ique is of net primary
production (i.e, gross photosynthesis minus autotrophic
respira tion). Thus we need to add on the material lost by
autotrophic respiration to the net primary production esti-
mate in order to derive an estimate of gross production. We
ca n make a fairly safe assumpt ion that this form of respira-
tory loss is no more than 40% of net primary production so
we need to add this amount on to the figures from 4000 to
5000 Tmol carbon year' , to give 5000 to 7000 Tmol carbon
year! (see Table 2 .7) . This still, however, leaves a deficit of
almost a factor of two. There is almost certainly no over-
Table 2.7 Bud get sheet for the o rg anic fluxes
into, o ut of, and w it hin th e oc eans (t aken from d el
Giorgio and Willi ams 200 5). All fluxes are in T mol
carbo n yea r' (T = 10 12 ) .
Sources and Inputs Outputs
sinks
External
Rivers 34
Sedi ments 14
• •••• ••••• ••••• •••• •••• ••• •••••••••• ••• •••••••• ••••• •••• ••••• •••• •••
Internal
Photosynthesis 3000-5000
Photosynthesis 5000-7000
(corrected t)
Respiration 10 000- 1 5 000
tCorrected for algal respiration-see text.
 Chapter 2 Primary Production Processes

looked source of carbon to the oceans of a scale that would
bridge the gap. so we have to acknowledge massive errors
in one, or more likely both, of our global estimates of the
processes of oceanic production and respiration. The basis
of this discrepancy is currently a matter of active debate
among biological oceanographers and biogeochemists.
2.12 Primary production in
seaweeds
Much of this chapter has concentrated on primary produc-
tion in planktonic photoautotrophs, since these contribute
the greatest proportion to the primary production in the
oceans. However, in coastal waters, the intertidal sea-
grasses and macroalgae are a very dominant feature. These
have a huge influence on the dynamics of coastal inorganic
nutrients and cycling of organic matter (Chapter 10). More
general discussions about the ecology of macroalgae and
seagrasses will be found in later chapters (Chapters 6, 8,
and 10).
Nevertheless, seaweeds on a shore can grow at impres-
sive rates, amassing large biomass (Fig. 2.36a) . The pro-
ductivityofseaweeds and seagrasses is equal to. or in many
cases greater than. that of terrestrial plant systems. For
instance. Laminaria-dominated communities have annual
productivity rates of approximately 2 kg carbon m-2year1•
Seagrass meadows are extremely productive with annual
production rates up to 6 kg carbon m-Zyear1 measured at
some tropical sites, far exceeding estimates for even tropical
rain forests and monocultures of crops (Chapter 10).
The annual primary production of seaweed and seagrass
meadows can be in excess of rainforest or crop species.
In water, seaweeds obtain the carbon needed for photo-
synthesis from CO 2 or from HC03. When they are exposed
to air, there is no bicarbonate and photosynthesis can only
take place by the uptake of carbon dioxide from the air. As
long as the seaweeds do not dry out, many species photo-
synthesize in air at rates similar to those measured when
they are fully submerged. However, when they begin to
dry out there are considerable differences in capacities
for photosynthesis. Photosynthesis in the low shore kelps,
such as Laminaria, even when mildly desiccated, is greatly
reduced, whereas the green alga Ulva, often found in inter-
tidal zones, continues photosynthesis down to 35% water
loss. Fucusvesiculosus, F. serratus. and F. spiralis can all pho-
tosynthesize even when desiccated down to a point where
the remaining tissue water content is less than 30% (Dring
& Brown 1982) .
Macroalgae continue to photosynthesize when exposed
to air, and some species even when harshly desiccated.
When submerged. considerable energy is expended
in maximizing the amount of light getting to the chloro-
plasts. This is especially important in turbid coastal waters
full of plankton and suspended particles that reduce light
penetration to a few metres or less. There are several mor-
phological features common to many species of seaweed
that help to address this problem. The first is the stipe
that supports the bulk of the photosynthetic tissue at the

I,j (b)

Figure 2.36 (a) Infrared image enabling a comparison to be made of terrestrial and intertidal primary producers. The
trees in the background show up red in the image, as do the large standing stock of macroalgae on the shore in the
foreground (photograph: David Roberts). (b) Air bladders at the end of each Macrocystis pyrifera blade help to support
the giant algae in the water, and maximize exposure to the incident light (photograph: David Thomas).
 2.12 Primary production in seaweeds
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
surface of the water where incident light is at a maximum.
Nereocystis luetkena is a superb example of this, with a
stipe of over 30 m long supporting up to 100 blades, each
several metres long. In species growing in deep waters,
such as the giant kelp species, the stipes act very much
like the trunks of canopy species of trees in a rain forest,
getting the maximum surface area of photosynthetic cells
as close to the incident light as possible (Figs 2.36b and
2.3 7) .
The long stipe of Nereocystis is rather flexible, and the
blades only sit on the surface because the apex of the stipe
terminates in an approximately IS-em diameter float, or
pneumatocyst. This large gas-filled bladder ensures that
the blades are floating as high in the water as possible. In
contrast, the giant kelp (Macrocystis pyrifera) has a differ-
ent arrangement with a small gas bladder at the base of
each of its thousands of blades, which connects them to
the highly branched stipe (Figs 2.36 & 2.37) .
Figure 2.37 (a & b) The massive gas-filled air bladder of
t he bull kelp, Nereocystis luetkeana. Specimen washed up
on the shore in California (photographs: David Thomas).
Gas-filled bladders are important in many macroalgal
species for maintaining photosynthetic t issues as close
to the incident light as possible.
Although not as impressively large. many other species
use gas-filled bladders in a similar fashion, e.g. Ascophyl-
lum, Sargassum, Fucus, and the bead-like Hormosira . The
gases within the bladders contain oxygen and nitrogen in
roughly the same proportion as in air. and varying amounts
of carbon dioxide. Curiously, the huge pneumatocysts of
Nereocystis contain up to 10% carbon monoxide. although
why this should be remains unclear.
As in trees that form terrestrial forests, the stipes of the
seaweeds also act as surfaces for epiphytes to grow on.
These can vary from other macroalgal fronds through to
biofilms made from bacterial and/or microalgal assem-
blages. Colonial animals, such as Bryozoa. can also form
dense cover on the outside of large macroalgal species.
both on the stipe and blades. Epiphytic growth can reach
such densities that they restrict the exchange of gases and
inorganic nutrients and cut down on light that reaches the
photosynthetic cells of the host. They can also increase drag
to such an extent that they make their hosts more prone to
being washed away in strong water currents (Fig. 2.38) . To
avoid such problems, 'skin shedding' is widespread among
large seaweed species (Russell & Veltkamp 1984) . Layers
of cell walls are shed from the outer surfaces of the sea-
weed carrying any attached epiphytes along with them
(Fig. 2.39) .
Epiphytes growing on the surfaces of seaweeds restrict
gas exchange and the supply of ino rganic nutrients, as
well as increasing drag.
Figure 2 .38 Macroalgae, like many other structures, can
quickly become host to other algae and sessile animals
Fucus serratus
that grow on their surface. Here a frond of
is nearly overgrown by the epiphytic brown Ectocarpus sp.
(photograph: David Roberts).
 Chapter 2 Primary Production Processes
Figure 2.39 One of the mechanisms by which several
seaweed species overcome problems derived from
epiphyte growth on their surfaces, is the periodic
shedding of outer layers of cell walls. In this scanning
electron microscope image, the outer layer of cell walls of
the brown alga Himanthalia elongata can be seen lifting
off, with the pattern of the underlying cells imprint ed
(photograph: George Russell).
Seagrass blades are also renowned for supporting dense
epiphytic growth. The biomass ofepiphytes can range from
25 to 80% and production from 50 to 100% thatofthe sea-
grasses. Skin shedding is not carried out by seagrass spe-
cies, but rather they produce large numbers of shoots, and
blades heavily laden with epiphytes break off and are lost.
2.13 Measurement of primary
production
The act ofobservation alters the object being observed (crude
interpretation of Schr6dinger's Cat thought experiment) .
One of the key issues facing biological oceanographers try-
ing to get good measurements of primary production rates
is how to translate the measurements they can make to the
conditions from where their field samples are taken. For the
past 50 years the key techniques to measure primary pro-
duction have been to measure directly the carbon assimila-
tion during photosynthesis and/or the oxygen production
and oxygen uptake during photosynthesis and respiration,
respectively.
Primary production is mainly estimated by measures of
the fluxes of carbon dioxide and/or oxygen.
The amount of carbon or oxygen flux per unit of time is
then related to the biomass of the photosynthetic organ-
isms creating the fluxes. Commonly used biomass terms are
amount of chlorophyll or the weight/concentration of the
organic carbon contained within the photosynthetic organ-
isms. Therefore the production is expressed as: change in
concentration of 0 2 or CO 2 per unit of time per unit of
mass or concentration of algae.
The combinations of units are diverse. depending on
the types of measurements being made and/or whether it
is phytoplankton or macroalgae/seagrasses that are under
investigation. For phytoplankton. rates of gas flux are often
expressed per unit of chlorophyll or particulate organic car-
bon (POC) . Measurements with macroalgae and seagrasses
are normally expressed on the basis of fresh or dry weight,
since these are easy to determine.
Rates of primary production are usually based per unit
of chlorophyll, particulate organic carbon or in seaweeds
on a dry or wet weight basis.
To be most realistic. the incubations during which the
fluxes of gas are measured should be made under the exact
light regime that would be experienced in nature (Fig.
2.34) . In a few instances it is possible to take a sample of
phytoplankton, or macroalgae, from a particular water
depth, put it in a container, and then perform the incuba-
tions back at the same depth and then subsequently mea-
sure the gases produced or consumed over the incubation.
However. the simple act of using a closed vessel introduces
changes to the system that some researchers claim result in
unrealistic measurements.
How realistic 'bottle incubations' are is open to debate.
It is logistically difficult to deploy in situ incubations,
especially if incubations are made throughout the euphotic
zone. which may extend down to 200 m in the open ocean.
It is also preferable to make incubations last for whole diur-
nal periods. so that the carbon and/or oxygen changes can
be integrated over daily periods, thereby including periods
of darkness where photosynthesis is absent, but respiration
continues. These measurements are onerous; hence com-
promise is necessary, as discussed below.
Although ideal, in situ incubations are often difficult to
employ.
2.13.1 Radiocarbon labelling-the ' 14C
method'
Primary production is basically the measure of the amount
of inorganic carbon that is assimilated through photosyn-
thesis to create new organic matter over a period of time
and over a specified area. Intuitively. therefore, direct mea-
surements of the decrease in the external inorganic carbon
pool or the increase in the organic carbon pool would seem
the most obvious way to measure primary production.
 2.13 Measurement of primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
In the1950s the Danish scientist, Einer Steemann Nielsen,
introduced the use of radiolabelled isotope 14C for measuring
carbon assimilation in phytoplankton. Since then, the '14C
method', as it is often referred to, has become probably the
most standard technique for measuring primary production
in both phytoplankton and macroalgal studies.
14C, in the fOITO of NaH14C03 , is added to the incubation
water surrounding a macroalgal sample or into a sample of
phytoplankton. The photoautotrophs assimilate the 14C dur-
ing photosynthesis and at the end of an incubation period
the quantity of radioisotope within the photoautotrophs is
measured. This is directly converted into the amount of car-
bon that has been photosynthetically assimilated during the
incubation.
Uptake of radioactive 14 C is a widely used way to esti-
mate primary production, althoug h it is not clear whether
net or gross production is being measured.
Technically the method is rather straightforward; how-
ever. there is still much controversy about what it actually
measures in terms of net or gross production. The other
major disadvantage of the method is that it is not possible
to measure dark respiration rates and. therefore. estimate
gross primary production.
2.13.2 Oxygen determinations
It is possible to measure both photosynthetic oxygen produc-
tion and respiratory oxygen consumption during incuba-
tions. The most widely used accurate oxygen determination
method is based on Winkler titrations for determining the
oxygen concentration of water. When performed with care.
this chemical titration determination method is able to mea-
sure precisely very small changes in oxygen concentration.
vital where respiration and photosynthetic rates are low.
By measuring oxygen fluxes both photosynthesis and
respiration can be measured, enabling bot h gross and
net photosynthesis to be estimated.
The method involves measuring the increase in oxygen
concentration in glass bottles (ranging in size from 10 to
200 ml) in which photosynthesis has taken place and the
decrease in oxygen concentration in darkened bottles in
which only respiration has taken place. One major differ-
ence between this and the '1 4C method' is that the oxygen
fluxes due to bacterial. protozoan. and zooplankton respi-
ration present in the sample will be included, because in
reality it is impossible to screen these out of field samples
without completely disrupting the photoautotrophs. There-
fore. the oxygen methods tend to measure community
metabolism. whereas in general the 14C method is measur-
ing activity of only the photoautotrophs.
The advantage of the oxygen system for the estimation
of primary production is that both rates of respiration and
photosynthesis can be directly measured, and so there is no
ambiguity about whether or not net or gross production is
being measured. The major difficulty comes in the conver-
sion of the oxygen measurements into carbon terms. The
photosynthetic quotient (PQ) is the term that describes
the moles of oxygen evolved per moles of CO, assimilated,
and is often quoted as 1.3. However, as described above,
the PQ varies with different nitrogen and/or phosphorus
supply. Iflipids are being predominantly produced, the PQ
is significantly different than ifcarbohydrates are being pro-
duced. Respiratory quotients (RQ) are the inverse of the PQ
and describe the respiratory relationships between oxygen
consumption and CO2 production. and are typically taken to
be 1.0 . Although less variable than PQ values, there will be
variations around this value, making standardized conver-
sions less certain.
Photosynthetic and respiratory quotients are important
to convert oxygen fluxes into units of carbon in primary
production studies.
2.13.3 Electrodes
There is an increasing array of electrodes that can mea-
sure pH. 0 2' CO 2, as well as sulphur and nitrogen species
(de Beer 2000) . These are not typically used to measure
the fluxes of 0 2 or CO2 in incubations, as described above.
but rather are used in field deployments to measure tem-
poral trends and estimate fluxes . Since the 1980s there
have been great advances in technology that have enabled
reliable electrodes with tip diameters ofless than 50 I'm to
be constructed. These have been revolutionary in measur-
ing small-scale fluxes in photosynthesis and respiration at
surfaces such as biofilms and sediments. Estimates of pri-
mary production using these techniques have been greatly
enhanced by the engineering of miniature light sensors
with tip diameters of approximately 100 I'm. Therefore,
the prevailing light regime can be measured at the same
time as the chemical fluxes (Figs 2.40 & 2.41) .
Increasingly electrodes are used to measure pH and gas
fl uxes, especially for fine-scale work on the surfaces of
sediments.
The latest generation of equipment capable of measuring
small-scale fluxes are the micro-optodes. In these, light of a
specific wavelength is conducted via fine glass fibres to the
measuring tip, which can be less than 20 urn, The tip contains
a fluorescent dye that fluoresces at a different wavelength to
the exciting light. The intensity of fluorescence depends on
the concentration of the substance being measured. Some
 Chapter 2 Primary Production Processes

of the most insightful data on the gas fluxes associated with
biofilms and sediment surfaces has come with the use ofpla-
nar optodes (Fig 2.41; Fenchel and Glud 2000; Glud et al.
1998, 2001) . In the planar optodes the dye that reacts with
the substance beingmeasured is spread on thin sheets placed
in contact with the surface ofinterest. The fluorescent signal
created by the reaction with the dye is then captured by a
charged couple device (CCD) camera. The camera converts
brightness into an electrical signal, thereby enabling the
signal to be quantified. More recently ultrathin layers of 0 2
indicator have been sprayed on to glass coverslips and then
these used to considerable effect for investigating bacterial
activity in biofilms in flow chambers on microscope stages
(Kiihl et aI. 2007). It is quite remarkable the level of precision
that can be achieved with these new technologies and the
quest for simultaneous light, pH. 0 2' and CO2 measurements
on the micro-scale are achievable and will revolutionize the
way we perceive production processes.

(oj (bJ

(e) Figure 2.40 (a) Micro-electrodes are now available for several parameters, including
oxygen and carbon dioxide. These have incredibly small diameter tips (insert),
enabling scientists to profile mi ni-scale (J.tM) differences in primary production
and respiration, in particular in benthic systems. The image shows a 'lander'
eq uipped with several electrodes, which it automatically pushes into the sediments.
It logs the chemical data measured by the electrodes for downloading when the
lander is retrieved (photographs: Dirk de Beer, Microsensor Group, Max Planck
Institute for Marine Microbiology, Bremen and Christian Lett, Hydra institute). (b)
In situ fluoromete r (window in centre) that can be dep loyed for lo ng pe ri ods of
time (months) to measure concentrations of chlorophyll in the water. Note that
instruments left in the sea become fouled by growth of sessile organisms, requ iring
the antifouling washing arm shown to clean the fluorometer window periodically
(photograph: David Thomas). (c) Measuring photosynthetic activity on algae, corals,
and s ponges (symbiotic algae) in the Red Sea with the in situ chlorophyll fluorometer
DIVING-PAM (photograph: Camillo Weis, Heinz Walz GmbH, Germany, www.walz.com).

02 Jlmol L- l
o 700 > 1400
Figure 2.41 Two planar o ptode 02
images (in li g ht an d da rk) of a diatom-
covered sediment. The white line
indicates the position of the sediment
surface. Notice the much deeper 02
penetration into the sediment in the
light, and t he very patchy distributio n
of the photosynthetic activity in the
light (image: Ronn ie Gl ud , see Fenchel
and Glud 2000).
 2.13 Measurement of primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
2.13.4 Fluorescence measurements
The measurement of changes in biomass is one route to
estimate primary production. One of the most commonly
employed methods for measuring chlorophyll is by mea-
suring its fluorescence, either within the cells directly or
after extraction from the organism by a solvent. The chloro-
phyll is excited by carefully defined wavelengths of light
and the resulting fluorescence measured directly (Krause
& Weis 1991). Since the 1970s, reliable instruments have
been available for measuring the chlorophyll fluorescence
in open waters. These send out pulses oflight and the fluo-
rescence generated is measured. Many systems that pro-
file for salinity (con du ctivity), temperature, and pressure
(depth) (CfD sensors) can also be easily adapted to have
in vivo chlorophyll fluorescence sensors attached and this
information relayed backto the ship, together with the tem-
perature and salinity data. Such instruments have become
invaluable for determining the distribution profiles of phy-
toplankton through the water column. For instance, such
profiles often help scientists determine from which depths
they should take water bottle samples for their oxygen or
14C incubations for primary production determinations.
Fluorescence sensors are used for the determination of
in situ concentrations of chlorophyll, and therefore phy-
toplankton biomass.
Such sensors can also be deployed for the long-term
measurement of fluorescence on moorings, automated
underwater vehicles (AUVs), or on seabed platforms (see
below) . These can be left for periods of over a year and the
data logged to allow the seasonal dynamics of phytoplank-
ton biomass to be elucidated in fine detail for that particular
site (Chapter 6) .
It is possible to derive more information from the fluores-
cent characteristics of a photoautotroph than from the sim-
ple measures of in vivo chlorophyll concentrations. Pulse
Amplitude Modulated (PAM) fluorometry is becoming a
widespread tool for measuring in situ photosynthesis (Fig.
2.33) . PAM fluorometers use a range of flashing (pulsed)
lights to measure the photosynthesis from the fluorescence
induced by the flashes oflight (e.g. Glud et al. 2002) . Gen-
erally, the fluorescence is excited at high repetition rates by
microsecond pulses of different wavelengths of light from
light emitting diodes (LED) .
Fluorometric methods are used for direct measurements
of primary production.
The accurate measurement of the variable fluorescence
characteristics of phytoplankton is the basis of profiling
devices that can measure 'real time' primary production
as they are lowered through the water. These are known
as Fast Repetition Rate Fluorometers (FRRF). The fluo-
rescence excitation system generates excitation flashes at
rates exceeding 200 kHz. The stimulated fluorescence and
excitation flashes, as well as the photosynthetically active
radiation, are all measured simultaneously. These mea-
surements are then used to calculate various biophysical
parameters that allow rates ofphotosynthesis and therefore
primary production to be calculated (Suggett et al. 2003) .
2.13.5 Remote sensing
Probably one of the most significant changes in biologi-
cal oceanography over the past twenty years has been the
development and deployment ofsatellite and aircraft-borne
colour sensors that can record the colour of water masses
and, using sophisticated algorithms, can allocate the
colour to concentrations of dissolved constituents, such as
coloured dissolved organic matter (CDOM), suspended sol-
ids, and (most importantly for primary production) chloro-
phyll and other algal pigment concentrations. Such satellite
ocean colour sensors provide the only means we have for
looking at the large-scale distributions of phytoplankton, so
that monthly and annual distribution patterns can be cre-
ated (McClain 2009) .
Increasingly sensors on satellites provide information on
primary production on a global scale.
These large-scale distribution studies are fundamental
to our understanding of the large-scale processes in the
oceans and how these affect primary production, e.g, the
inter-annual variability due to massive cyclical phenom-
ena, such as the North Atlantic Oscillation (NAO) or the
El Nino Southern Ocean Oscillation (ENSO) . Naturally,
as more satellites are deployed carrying such sensors, and
more years of information are collected, these methodolo-
gies will greatly enhance our understanding of large-scale
ocean processes.
Ocean colour sensors can also be deployed on aircraft
and have been used successfully to record the dynamics of
phytoplankton blooms, especially in coastal waters within
the operational ranges of the aircraft. tight Detection and
Ranging (UDAR) flights use a variety of pulsed lasers to
stimulate phytoplankton chlorophyll and other pigments to
fluoresce, and the fluorescent signals are then detected by
sensors on the aircraft.
Surveys of water bodies using aircraft give rapid informa-
tion about phytoplankton distribution in surface waters.
One advantage of such data is that they can be collated
rapidly by scientists on board the aircraft and relayed to
colleagues on the ground or on research vessels. In this
way, the research vessels can be directed to particular areas
 Chapter 2 Primary Production Processes
of research interest, such as developing phytoplankton
blooms or phytoplankton dynamics associated with water
frontal systems. Increasingly, research expeditions will
rely on information such as this, as well as 'online' satellite
information to plan and modify cruise tracks to conserve
expensive ship time.
The major disadvantage of ocean colour sensors, either
aircraft- or satellite-borne, is that it is only the colour of the
very top few metres of the oceans that is measured. As has
been discussed above (section 2.10), this is unlikely to be
a reflection of much of the phytoplankton biomass in any
one body of water. In particular, features such as sub-sur-
face chlorophyll maxima and accumulations of chlorophyll
associated with sub-surface processes are not accounted for
using these sensors.
Many remote sensing methods only give info rmat io n in
surface waters, t hey cannot give information about sub-
surface phytoplankton distribution.
2.13.6 Automatic measuring devices
Naturally, such ground truth exercises are limited to the
rather restricted activities of research vessels. Although
many millions of dollars are spent each year on maintain-
ing research ships at sea, the coverage of global oceans at
anyone moment of time is minimal. Many research vessels
now have the technology to measure the chlorophyll con-
tent of surface waters continually during the whole of their
cruise track by pumping surface waters past a sensor that
measures the fluorescence, which can then be converted to
phytoplankton biomass. This technology is robust enough
to deploy on other ships, such as commercial freighters,
container ships, and ferries . These vessels tend to keep to
well-defined routes, and so information can be collected
that will document seasonal changes with high precision.
The typical daily cost of an ocean going research vessel
is between $US20 000 and $USSO 000, depending on
size and sophistication.
As well as chlorophyll concentrations, automated measur-
ing systems are being developed for measuring temperature,
salinity, and inorganic nutrients, such as nitrate, phosphate,
and silicate, as well as dissolved gases. Increasingly, such
devices will be deployed on a variety of ships (including fer-
ries and commercial shipping), together with fluorescent
sensors for phytoplankton determination (e.g, Cooper et al.
1998) . This will enable the determination ofseasonal biolog-
ical and chemical dynamics along specific routes to be well
defined. Naturally these measurements still suffer from the
limitation that they are only measuring surface waters, since
the water is normally pumped from seawater inlets in the
keel of the ships, only a few metres below the water surface.
Coupled biological and chemical sensors are deployed
on ships that have regu lar routes, enabling large-scale
collection of data over long periods of time.
The opportunity to profile the concentrations of phyto-
plankton and the parameters that determine primary pro-
ductivity over greater water depths is clearly the next step.
Very important information may be gained using towed
platforms that undulate during towing from the surface
to depths of 500 m (Fig. 2.42) . These undulators can be
towed at speeds up to 12 knots (c.6 ms- I ) and their 'flight-
paths' can be set by the operators. These platforms can
support a multitude of sensors, such as fluorescent chloro-
phyll sensors, light sensors, salinity, temperature, pressure,
nitrate and nitrite, and particle concentration sensors. The
data from the sensors can be sent to the operators by the
connecting cable, giving the scientists on board 'real time'
data about a whole suite of information.
Figure 2.42 Various profilers are now
available that can be towed from a ship.
They are designed to undulate over a water
column , profiling a range of parameters
using a range of sensors (insert) carried on
the vehicle. Data can either be logged on the
profiler or, more normally, can be sent back
through cables so that scientists get real-time
data on board the ship (photographs: Chelsea
Techno logies Group, www.chelsea.co.uk).
 2.13 Measurement of primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

) ) ) ) )

I
••
,
,"~.! - - -
,,
"••
I

!l
I

Figure 2.43 Conceptual image of the components of an ocean observing system, including research vessels, satellites,
moorings, autonomous underwater vehicles, moorings. The image was supplied by OceanSITES (http://www.oceansites.
org!), a worldwide system of long-term, deepwater reference stations measuring dozens of variables and monitoring
the full depth of the ocean from air-sea interactions down to 5,000 m. (Image: Jack Cook and E. Paul Oberlander, WHOI
Graphics).

devices are designed to 'roam' pre-programmed tracks over

Towed instrument platforms that undulate between the
surface and depths of 500 m can provide valuable infor-
mation about the biological and chemical characteristics
of a water body.
These technologies are still restricted to the places that
ships travel and, therefore, a large part of the worlds' oceans
will be visited only infrequently, if at alL What is needed are
roaming platforms that are able to measure physical, bio-
logical. and chemical parameters across depths and for long
transects . A whole range of Autonomous Underwater Vehi-
cles (AUV), gliders, and floaters have been under develop-
ment since the late 1990s (Fig 2.43; and see reviews: Paul
et al. 2007; Benfield et aL 2007) , These battery-powered
large regions of the ocean, collecting data, Periodically
these devices surface to send the collated data to satellites,
which then transfer the data to base stations from where
scientists can download the information . To date. many of
these devices carry sensors for salinity, temperature, and
pressure among others. However, as technology progresses
fluorescent and nutrient sensors will be routinely deployed
on such platforms.
In the future Autonomous Underwater Vehicles will be
used to roam the oceans sending information about pri-
mary production and chemistry to satellites and back to
researchers at their desks.
 Chapter 2 Primary Production Processes

Box 2.12: The need for long-term data support the analyses. It is clearer than ever before that
sets long-term monitoring of basic parameters is absolutely vital
There is understandable debate about the impacts of if we are to understand changes taking place and make
global climate change on primary production of the world's predictions fo r the future (Richardson et al. 2006).
oceans, in particular coastal waters and the resulting effects There are too many long-term series to mention here,
on fisheries (IPee 2007a, b, c). Rising sea temperat ures, but as examples it is worth mentioning two quite different
increased freshwater input to coastal waters, increased sampling programmes.
sediment, and inorganic nutrient loadings due to increased
Continuous plankton recorder survey
run-off from land, will all impact the basic factors control-
(1930s to present)
ling photosynthesis and the balance between gross and net
Sir Alister Hardy is arguably one of the most inspirational
community production.
of marine biologists to have transformed the way biological
Despite all of our sophistication of methods we
oceanog raphy and plankton research is done. His books
use to measure, or rather estimate, primary production,
The Open Sea (in 2 parts) and Great Waters are still some
and the development of elaborate biogeochemical models
of the most remarkable writings in marine biology and are
to help predict futu re trends in phytoplankton dynamics,
recommended to anyone consideri ng a career in marine
we still have a rud imentary knowledge that allows us to
biology/biological oceanography.
determi ne trends from natural annual or decadal varia-
Hardy invented the continuous plankton recorder, a
tions (Smetacek & Cloem 2008). There is only one real-
device towed by a ship, at a depth of about 10m, that
istic way to do this and that is the analyses of long-term
collects the plankton onto a silk ribbon. The ribbons are
data series. Fortunately many of the marine laboratories
retu rned to the Sir Alister Hardy Foundation for Ocean Sci-
established regular water sampling of basic parameters
ence in Plymouth, U.K. (http://www.sahfos.ac.ukl) where
such as salinity, temperature, chlorophyll concentra-
the plankton on the ribbon are analysed in blocks of ribbon
t ion , species composition, and nutrient concentrations.
representing a tow distance of about 10 nautical miles.
Some of these have been maintained with no interruptions,
The routine parameters measured and phytoplankton and
whereas some have long periods where data are missing.
zooplan kton species abundance and a colour measure for
Sadly many have been stopped due to lack of funding to
the density of plankton.

70'W 60'W SO'W 40'W 30'W 20'W 10'W O' 10' E

6S'N 6S'N

6O'N 60' N

SS'N SS'N

SO'N SO' N

4S'N 4S'N

40'N 40'N

3S'N 3S'N

30'N
70'W SO'W 40'W 30'W 20'W 10'W O' IO' E

Th e Si r Aliste r Hardy Found ation for Ocean Science (SAH FOS) run th e CPR prog ra mme t o monitor the near-
su rface plankto n of t he North Atlanti c and North Sea o n a monthly bas is, usin g co nt inuous plankton record ers
o n a network of shippi ng routes. Th e map shows the full network of routes t hat have been t ow ed ove r th e last
75 years. Th ese ro utes we re not all used at th e same tim e (© SAHFOS Ecol o g ical Stat us Report 2008).
 2.13 Measurement of primary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

200000 Partial pressure of COl

180000 •• atmosphere (Mauna loa)
160000
140000 • • •
• •
••cc
~
120000
~
3year runningmean ~
~
100000 • =
=
- -
c
ts • ~

80000
60000
• •
•• •
•
. •
• 8- ~

- - - - - - -•- - -
• • • .,
40000
20000
• • .. •
.'
0
1958 1966 1974 1982 1990 1998 2006
Yea"
Lon g-term data sets are vital if we a re to interpret eco-
logical change. This example s hows the trends in num- The Hawaii Ocean Time series (HOT) has been co llecting
bers of Ceratium sp p. in th e North Sea samples f rom an extensive series of oceanograp hic measurement at
the co nt inuous plankton record er (C PR) su rveys ove r o ne stat ion si nce 19 8 8 fund ed by th e Nati onal Sci-
50 yea rs. Ceratium s pecies a re known t o be sens it ive ence Foundati on , USA. Here the pC0 2 of surface w aters
to t em perature change and it is possible that the very are co mpared t o th e atm osph eric trend s in CO2 mea-
low numbers in recent years are du e t o this (image from su red at Maun a Loa. The large seaso nal changes are
Edw ards et al 2009 and w it h pe rmission of SAHFOS) clearly v isible, but th e lon g-term increases are very clear
(© SA HFOS Eco lo gical Statu s Report 2008). (image w it h permi ssion of HOT pro gramm e, http:/ /hah-
ana.soest .hawaii.edu).

The first tow was in 19 31 from Hull, UK to Bremen,

Germany and since then more than 275 vessels have been HOT 1-21 SFluoromelric Chlorophyll a(mg nr'I
used to tow CPRs and the North Sea and North Atlantic 20
have been routinely sampled by using a series of shipping
40
routes since the 19 40 s to the present (Richardson et al
60
2006). In a single year there can be over 3 80 tows cover-
ing distances of more than 130 000 naut ical miles. " 80
~ 100
~

Hawaii Ocean Time series, HOT (1988 to

~

• 120
present) •.>:: 140
Research cruises are made one a month to a deep-water 160
Station ALOHA (A Long-Term Oligotrophic Habitat Assess-
180
ment ; 22 0 45 'N, 158 0 OOW) located 100 km north of
200
Oahu , Haw aii (http ://hahana.soest.hawaii.edu / hot/ M90919293~95%9 798990001~~M~M0 7~

hotjgofs.html). The teams of scien tists on board make

detailed measurements of both physical and biogeochemi-
cal parameters down to 1000 rn. These include tempera-
ture, sali nity, major inorganic nutrients, gas content of the
water, pH, chlorophyll , bacteria and phytoplan kton produc-
tivity, among othe rs. This is a quite remarkable time series
reflecting a considerable investment of resources and sci-
entist effort.
These data, together with the results of a sister-project
in the Atlantic, the Bermuda Atlantic Time Series (BATS,
see: http:/ /bats.bios.edul) , have been fundamental to our
understanding of seasonal changes in gas and nutrient bio-
geochemial processes, and in parti cular the changes due
to atmospheric loads of CO2 ,
0.05 0.1 0.15 0.2 0.25 0.3
Lon g-term trend s in cho ro p hyll a in th e HOT d ata set .
Larg e inter- annual variatio n is dearly seen wit h peak
values in 19 8 9 , 19 9 9 , and si nce 200 5 bein g greater
th an th e ot he r years. NB Thi s is an o ligotrop hic site
and th e maximum Chl-a values are ve ry mu ch less than
peak values measured in more nutrient-ri ch systems.
Al so note that th e maximum st anding stoc k of algae
is between 60 and 140 m water depth and not at the
surface (see Fig. 2.28) (image w it h perm ission of HOT
pro gramme, http:/ /hahana.so est.haw aii.edu).
 Chapter 2 Primary Production Processes

Of course the long-term t rends at anyone site may be
unique to that site and a synthesis of results from several
sites is a key to understanding controlling factors th at force
results. This was attempted by Cloern and Jassby (2008)
who searched 11 4 databases from around the world for
seasonal trends in phytoplankton biomass in te rms of
chlorophyll concentration. Their analyses showed that
there was much greater variability between and within the
systems they looked at (estuaries, lagoons, shallow inland
seas, coastal waters) compared to the terrestrial and true
oceanic sites for which seasonal variation in phytoplankton
standing stock are recurrent and synchronous over large
geographic regions. As a conclusion of their work th ey
posed two fundamental ecological questions: ' ( 1) how do
estuari ne and coastal consumers adapt to an irregular and
unpredictable food supply, and (2) how can we extract
signals of cli mate change from phytoplankton observa-
tions in coastal ecosystems where local-scale processes
can mask responses to changing climate?'. These are key
ecological questions facing marine bio logists/b io logical
oceanog raphers working with planktonic systems in the
co ming decades.

Figure 2.44 In this st riking pi cture, th e import ance of primary produ cti on p rocesses for th e marin e ecosystem can b e
su mmed up: from th e microbes t o th e w hales th e energy harvested throu gh ph oto synth esis is th e basis of it all. This is
a sout hern ri ght w hale mother wit h her calf swimming along the shores of Peninsula Valdes in Argentina. As they move
their t ail s, a g reen t id e of phytop lankto n swirls b ehind th em . Algal blooms are becomin g more frequent in th e bays of
Peninsula Va ldes, w here so ut hern right w hales gat her each year t o g ive b irth and nurse the ir calves (photog raph by
Mariano Sironi, Instituto d e Conservac i6 n d e Ball enas, Bu enos Aires, Argentina. http:/ / www.icb.org.ar).
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Chapter Summary
• Abou t half of the global primary production takes place in marine systems. Most of the primary prod uc-
tion in the world's oceans is d ue to microscopic phytoplankton, si nce macroalgae are restricted to a rather
narrow band on coastlines.
• Photosynthetic algae can vary in size from just a few urn to giant macroalgae > 50 m long. Growth of
primary producers is the difference between the gains from photosynt hesis and losses to respirati o n,
excretion , and the construct ion of skeletal material and storage products.

• Rates of primary production are mainly controlled by light and inorganic nutrient supply. The amount of
light available for photosynthesis depends upon water depth, and the amount of lig ht-scattering particles
that occur in the water:
• The main limiting inorganic nutrients are nitrogen and phosphorus, while in certain marine systems trace
elements such as iron are limiting.
• Seasonal dynam ics of algal growth are controlled by a complicated suite of interactions between irradi-
ance and nutrient supply, ultimately driven by the physical dynamics of the system.
• Eutrophication of a water body is a reversible process and can be caused by factors other than solely
increased inorganic nutrient loading of a system.
• Frontal systems, gyres, river plumes, and coastal upwelling all influence the rate of primary production,
as they influence the transport of nutrient-rich waters to the sea surface.
• Primary production in polar oceans is restricted to a short summer season, in contrast to temperate waters
where two peaks in production are often observed. Primary production of tropical waters is generally
consistently low.
• The measurement of small-scale primary production can be made using oxygen and carbon dioxide trac-
ers, or electrodes and various fluo rometric techniques. On a global scale primary production is measured
using satellite-borne colour sensors that are used to estimate the concentrations of plankton in the water:

Further Reading
A classic introduction to phytoplankton dynamics and constraints on growth is presented by Fogg (199 1) as
well as short essays by Smetacek (1999, 200 1, 2002), The evolutio n of modern phytoplankton is discussed
by Falkowski et al. (2004),
Both Falkowski and Raven (2007) and Williams et al. (2002) give comprehensive overviews of primary pro-
duction in aquatic systems, whereas del Giorgio and Wi lliams (2005) deal specifically with respiration. However,
these primarily deal with phytoplankton, while Lobban and Harrison ( 1997), Lee (2008) , and Graham and Wilcox
(2008) give good overviews of factors influencing primary production of macroalgae. Microbial processes and
the underlying biochemistry of photosynthesis, respiration, and associated metabolism is given by Mad igan et al.
(2008) , who also give a good overview of microbial physio logy and ecology, Bacterial metabolism and ecology
is comprehensively covered by Dyer (2003) , as is general marine microbial dynamics by Kirchmann (2008),
The influence of physical processes on primary production is dealt with by Mann and Lazier (2005), Bigg
(2003) summarizes many of the large-scale ocean processes that infl uence primary prod uction.
It is important to set the topics covered by this chapter into a wider context of biological oceanography, and
Lalli and Parsons (2004), Libes (2009) , Mann and Lazier (2005) , Stumm and Morgan, 199 5, Millar (2004) ,
Cockell et al. (2007) , and Millero (2005) comprehensively link aspects of physics, chemistry, and biology. There
are three excellent books published by The Open University (1995, 2000, & 2005) , that together make a superb
companion text to discussions about issues re lated to marine primary production.
For a more global consideration of primary prod uction and its role in global biogech emical cycles, comprehen-
sive overviews are given by Andrews et al. (2003) , Black and Shimm ield (2003), Emersen & Hedges (2008) ,
Longhurst (2006) , Sar miento & Gruber (2006), and Schulz and label (2000), Broecker (2009) gives a com-
prehensive overvi ew of the oceans in terms of climate change.
Arrigo (200 5) gives a comprehensive overview of the ro le of microorganisms, nutrient cycles, and biogeo-
chemical cycling in marine systems.
Chapter 2 Primary Production Processes

One of the best resources for informed short essays on many of the issues raised in this chapter can
be found in Oceanus, a popular forum pub lished by the Woods Hole Oceanograph ic Inst itute. (http:/ /www.
whoi.edu/oceanus/i ndex.do) .
• Andrews, J, E" Brimblecom be, P., Jickell s, T. D., Liss, P. S., & Reid, B. J. 2003 . An Introduction to Environ-
mental Chemistry. Wiley-Blackwell.
• Arrigo, K. R. 200S. Marine microorganisms and global nutrient cycles. Nature, 437 : 3 49-355.
• Bigg, G, 2003. The Oceans and Climate. Cambridge Univers ity Press,
• Black, K. D. & Shimm ield, G, B. 2003. Biogeochemistry of Marine Systems. Wiley-Blackwell .
• Broecker, W. 2009. Wally 's quest to understand the oceans CaC0 3 cycle. Annual Review of Marine
Science, 1: 1- 18.
• Broecker, W. 2010. The Great Ocean Conveyor: Discovering the Trigger for Abrupt Climate Change,
Princeton University Press,
• Cockell, C; Corfield, R. , Edwards, N., & Harris, N. 2007 . An Introduction to the Earth-Life System.
Cambridge University Press,
• Del Giorg io, P. & Williams, P. J. Ie B. 2005. Respirotion in Aquatic Systems, Oxford University Press.
• Dyer, B. D, 2003. A Field Guide to Bacteria. Comstock/Cornell paperbacks, Cornell University Press.
• Emerson , S, R. & Hedges, J. I. 2008, Chemical Oceanogrophy and the Marine Carbon Cycle. Cambridge
University Press.
• Falkowski, P. G, & Raven, J. A. 2007 . Aquatic Photosynthesis 2nd edn. Princeton University Press,
• Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A. , & Raven, J. A. 2004 . The evol ution of modern
eukaryotic phytoplankton, Science 305: 354-360.
• Fogg, G, E. 1991, Tansley Review No. 30, The phytoplankton ways of life. New Phytologist 1 18 :
19 1- 2 3 2 .
• Graham, L. E. & Wi lcox, L W, 2008, Algae. Benjemin Cumm ings,
• Kirchman, D. L, 2008. Microbial Ecology of the Oceans 2nd edn . Wiley Blackwell.
• Lal li, C. M. & Parsons, T. R. 2004, Biological Oceanogrophy. An Introduction 2nd edn . Butterworth -
Heinemann.
• Lee, R. E. 2008. Phycology 4 t h edn. Cambridge University Press, Cambridge,
• Libes, S, M. 2009. An Introduction to Marine Biogeochemistry 2nd edn. Academ ic Press.
• Lobban, C. S, & Harrison, P. J. 1997. Seaweed Ecology and Physiology. Cambridge University Press,
• Longhurst, A. 2006. Ecological Geography of the Sea 2nd ed n. Academ ic Press,
• Mad igan , M. T., Martinko, J. M., & Parker, J. 2008, Brock Biology of Microorganisms 12th edn. Pearson
Education.
• Mann, K. H. & Lazier, J. R. N. 2005. Dynamics of Marine Ecasystems: Biological-physicallnteroctions in
the Oceans 3 rd edn. Wiley Blackwell.
• Miller, C. B, 2004, Biological Oceanography. Wiley Blackwell.
• Millero, FJ. 2005. Chemical Oceanography 3 rd edn. CRC Press, Florida, USA.
• Open Un iversity. 1995. Seawater, its Composition, Properties and Behaviour. Butterworth -Heinemann.
• Open Un iversity. 2000. Waves, Tides and Shaffow-Water Processes. Butterworth -Heinemann.
• Open Un iversity. 2005. Marine Biogeochemical Cycles. Butterworth-Heinemann.
• Sarmiento, J. L. & Gruber, N. 2006. Ocean Biogeochemical Dynamics. Princeton University Press.
• Schulz, H. D. & Zabel, M. 2000. Marine Geochemistry. Springer Verlag,
• Smetacek, V. 2002 . The ocean's veil. Nature 419: 565.
• Srnetacek, V. 2001 . A watery arms race. Nature 41 1: 745.
• Srnetacek, V. 19 9 9 . Revo lution in the ocean. Nature 40 1: 647 .
• Stumm, W. & Morgan , JJ, 19 9 5. Aquatic Chemistry-Chemical Equilibria and Rates in Natural Waters
3rd edn. Wiley Blackwell, Oxford, UK,
• Williams, P. J, Ie B" Thomas, D. N., & Reynolds, C. S. 2002. Phytoplankton Productivity: Carbon Assimila-
tion in Marine and Freshwater Ecosystems. Wiley Blackwell.
Microbial Ecology:
Production and the
Decomposition of
Organic Material
Chapter Summary
Micro-organisms have the most important role in the recy-
cl ing, decompositi on, and remineralization of organic mate-
rial. This chapter will reveal how they play such a do minant
role and introduce the most important organ ism groups in
oceanic microb ial food webs. The ecological context into
which these micro-organisms are embedded is developed
and leads to a view that the microbial food web may be seen
as having two origins: photosynthes is and detrital organic
matter. Th e production and composit ion of dissolved and
3.1 Introduction
All sustainable systems are cyclic. In Chapters 1 and 2 the
production of organic material by marine algae was con-
sidered. The production process utilizes energy in the form
of light. water. and inorganic nutrients, suc h as nitrates,
phosphates, and carbon dioxide. For the cycle of nature
to be completed. t his energy must be rele ased as heat and
the ele men ts ass im ilated into organic m aterial du ring
photosynthesis, and then recycled back to their inorganic
state. Th is process. the complement to photosynthes is. is
respiration. In its n arrowest meaning. respiration is sim-
ply the biological oxidation of organic material, typically
by oxygen. and the formation of water and carbon dioxide;
the reformation of the inorganic nutrients is an intimately
associated process. known by a number of synonyms: min-
eralization and remineralization (Chapte r 2) . As the
process also results in the breakdown of organic m aterial it
also carries the name decomposition. All living organisms
respire; however. in the oceans this process is dom inated
by the prokaryotic m icro-organisms (shortly m icrobes).
notably the bacteria and archaea.
particulate organi c matter is explored, as is the basic pro-
cess of decomposition. The organi sms that comprise the
mi crobial communi ty are introduced together with the ir re la-
tive abu ndances and interactions. The complex chall enge of
how we measure microbial diversity and activ ity, and count
micro-organisms in the oceans, leads to a consideration of
the dynami cs of bacterial growth. Fi nally, the chapter con-
cl udes by discussing the seasonal cycle of production and
consumpti on a nd the role of marine mi crobes in the global
carbon cycle and cli mate system.
Prokaryotic organisms are micro-organisms (bacteria
and archaea) that do not, unlike eukaryotes (e.g. plants,
animals), have separate organelles like a nucleus (Greek
karyon), in their cells.
3.2 The microbial powerhouse
We can readily perceive larger organisms as whales, fish, and
large invertebrates in the seas since they occupy the same
spatial scales (centimetres to tens of metres) as humans. In
contrast, microbes can be seen and studied only w ith the
help of sophisticated technology, but the same also holds
true for most of the life in the dark abyssal layers of ocean.
Temporal, spatial, and bod y-size scale issues, and t he
necessary observational techniques and devices to study
m icrobes, distinguish them from othe r organisms. Under-
standing the properties of the miniature scales inhabited by
m icrobes is required if we are to really understand t he m and
how they fun ction (see Box 3.2) . Although the oceans are
mainly (99.99999%) water; the biota occupy only approxi-
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

mately O.0 000 1 % of the total volume. From the organism's
point of view the environment is very dilute and empty. To
examine marine microbes, the first step is always to con-
centrate them from water samples. most often by collecting
them on fine filters . The consequences for organisms ofliv-
ing in a dilute environment and the adaptations needed to
cope with it will be discussed later in the chapter.
It is difficult to convince even expert marine scientists
that the biomass of micro-organisms is comparable to that
of whales or fish, and that their activity, as we shall see,
exceeds that of the combined metabolism of vertebrates
many times. But whyis this 50, and why are marine microbes
50 important in the turnover oforganic material in the sea?
Besides their qualitative importance in organic material
cycling. prokaryotic microbes are very important in other
aspects. Their genetic and metabolic diversity far exceeds
the diversity of other groups of organisms. The estimated
total number of all eukaryotic marine species. including
all phyla of plants, algae, animals, and micro-organisms, in
the seas and oceans is 230 000, ofwhich approximately 140
000 are known (world register of marine species at http:/ /
www.marinespecies.org/) .
Eukaryotic organisms have complex membrane-bound
structures, like a nucleus, mitochondria, and chloroplasts
in their cells. Eukaryotic organisms include plants, ani-
mals, fungi , and protists.
In contrast. the number ofbaeterial species is estimated
to be from 1 000000 to 1 000000000 (Curtis et a1. 2002;
Pedros-Alio 2006), of which only a tiny fraction is currently
known. Metabolic versatility allows bacteria to carry out
multiple fundamental biogeochemical processes vital for
ecosystem functioning in the ocean. such as the decompo-
sition and utilization of dissolved organic matter. nitrogen
fixation, denitrification, and nitrification.
Body size has a major consequence for metabolism
(Fenchel 2005) . All free-living organisms take in the
metabolites necessary for their growth and dispose of their
waste products through the body wall. This transfer is the
principal limitation to maximum growth. thus surface area.
rather than biomass, is ultimately the main determinant of
metabolic rate : If an organism, such as a whale, were to
achieve a metabolic rate comparable to a bacteria cell, the
metabolic heat it produced would be so difficult to dissipate
that its body temperature would rise to 1500°C-it would
be white hot.
We can explore the consequences of this simply by con-
sidering the organism as a simple sphere:
S 4.,., 3
- -
V r3 rx
r
where r is the radius. S is the surface area (which will
reflect metabolism), and V is volume (which is directly
related to biomass) . Thus. in the case of our simplistic
organism, the specific metabolic rate (metabolism/bio-
mass = S/V) is proportional to l /r, i.e . inversely pro-
portional to the organism's linear dimensions. If we take
our end members of the marine community (the marine
bacterial cell and the whale) to have linear dimensions of
0 .5 I'm (0.5 x 10-6 m) and 10 m, then if this simple rule
is applied, the metabolic rate of a given mass of bacteria
would be 2 x 10-', i.e. about 10 million times greater than
the same biomass of a whale. The results of this simple cal-
culation are shown in Fig. 3.1 . Now clearly the calculation
is simplistic, as organisms, particularly larger ones. are not
spheres; further they overcome the S/V limitation in part
by increasing the surface areas available for exchange, by
convoluted structures such as gills and lungs. Nonethe-
less there is a limit to this and so we end up with a broad
compliance to the S/V rule. but it is not as simple or exact
as the formula above.

125
3.2.1 Small organisms are important - Surfo(e area/volume
-3- I 000000000
- Volume
Why are small organisms so important? There are broadly
two answers to this question. First. the primary production
-~

E
~
- Areo 10
~
E
~

of organic material in the seas is associated with micro-

scopic organisms (see Chapter 2 and section 3.8) and the
-e-
11
0
1000000 75
--
11
0
~

usually large number ofsteps between the primary produc- --

"-
0
~
S -""-
0
~

ers and the marine vertebrates results in the loss of almost

all the organic material produced by photosynthesis such
-""-
~
~
0
~
1000

25
~

tharthere is very little forlarge organisms to live on (3.3.2).

Second. and related to this. is the consequence of size. 0
10.1 1 10 100 1000 10000
The marine pelagic community spans a range of size from
Diameter (J.lm)
marine bacteria (c.0.1 pg = 0.1 X 10- 12 g), arguably the
smallest free-living organisms, to the whales (c.100 tonnes
= 108 g), the largest ofanimals. This means that biological Figure 3.1 The relationship between diameter, volume,
biomass spans 21 orders of magnitude. and surface area for a sphere.
 3.3 The ecological context in which the marine microbes are embedded
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

3.2.2 How is metabolic activity In Fig. 3.3 the distributions of activity and biomass given
distributed and which are the in Figs 3.1 and 3.2 are combined. Because the change of
important organisms? metabolism with size (Fig. 3.2) is much less than biomass
(Fig. 3 .1), the resultant line is very similar to the surface-
Metabolic activity is constrained by metabolic capability to-volume relationship given in Fig. 3.1. Thus we have a
and abundance . A surprising observation made by Sheldon basis for understanding the major part played by micro-
et al. (1972) is that if estimates of biomass are assembled in organisms in the plankton.
logarithmic categories, there is comparatively little change
with body size. Food-web theory suggests that a small Specific metabolic rate (metabolism/biomass) is inversely
decrease in biomass occurs with an increase in the size frac- proportional to an organism's linear dimensions.
tion, which is broadly upheld by field observations. Models
that give the distribution of biomass through logarithmic
increments of size (as length) suggest a small decrease with
body size, which complies with the following relationship: 3.3 The ecological context in
biomass = k x (Size)-O·22 which the marine microbes are
A plot of the above relationship is given in Fig. 3.2, along embedded
with the planktonic groupings that are mainly associated
with the various size categories (see also Chapters 4 and 7) . Before we can explore the role and functioning ofthe micro-
bial community. we need to understand the theoretical eco-
1.0 logical context into which it is embedded. As microbes play
!
!• a central role in the metabolism of organic material in the
•
a
' .9
, :~ ••
~ .s•• . ~
oceans. as in most other ecosystems, it is logical to outline
~
E
.2
•
••-.>; ' .8 ~
•
-
•
j
~
•
!
l
• ~
•
-•
!
•
~
~
0
~
•• - .
~
•
•
~
~
~ the rationalizations surrounding the flow of organic mate-
rial through an ecosystem. The flow oforganic material can
•• ~

•
,
~

••
,•
~
, .7 be treated in the context of feeding interactions between
• •
••
a organisms sharing the same habitat and forming food
0.6;;
-- .- §
- -- .-
§ § § §
chains and food webs.

--
§ §
Size (length in 11m)
- Trophic levels indicate the position of an organism in a
food chain or food web, hence primary producers make
Figure 3.2 The red line shows the theoretical distribution up the lowest trophic level, with the largest predators
of biomass with size. The approximate size bands at the top.
occupied by various planktonic groups are shown.

125 100 --
E
-a
Aquatic food webs are typically size-structured (e.g.
Loeuille & Loreau 2005), meaning that body size is an
•a ~
a
~

~
1;; important trait (although not the only one) explaining feed-
~
• l' Distribution of metabolism with size E
• 8' ing interactions between organisms (see also Chapter 7) .
'0
N

a
ca= 75
Inueose intumuletlve metobcllsm
with size
a

0-
>;

'j
6' "it'
--
a 3.3.1 The concept and consequence of
."--•
E E
5.' 4' -a .~
growth yield
~
~
a
.e
E ~ An organism cannot grow (convert food into body tissue)
25
-a 2' •>
with 100o/n efficiency. The laws of thermodynamics show
'" \ ~
-"
~
E that work must be done to create new tissue and that this
'-d - -
= =
-
= =
=
= =
=
= =
=
= =
=
=
='
=
=
8
- -
= =
-= = 8=
requires energy. This energy derives from respiration.
Size (in I'mJ -
8
-= which occurs at the expense of some of the energy derived
from assimilated food or photosynthetic assimilation (see
Figure 3.3 The size distribution of metabolism and its Chapter 2 and Fig. 3.4). In addition some of the food is lost
progressive integral, with size. The rates are determined via excretion. Respiration and excretion both represent
as the product of the size distribution of specific metabolic losses that result from converting food into new
metabolic activity (Figure 3.1) and biomass (Figure 3.2) organism tissue, i.e. growth. Excretion encompasses both
with size. The figure shows that most of the metabolism is particulate (like zooplankton faecal pellets) and dissolved
associated with organisms less than 100 urn, waste products. This introduces the notion ofthe efficiency
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

ofgrowth, usually expressed as a growth yield or, since it is In this way we may link together the type of flow diagram
often expressed as a percentage, growth efficiency. shown in Fig. 3.4 into a string of trophic yields (see Fig.
3.5) .
. growth G G
Growth yield = Y" = food intake = G + R + E or G + M Given this as a concept we may calculate the overall yield
of our simple food chain as:
where G = growth, R = respiration. E = excretion. and
overall efficiency = Yt = 2 X Yt = 3 X Yt = 4 X •••
M = metabolism.
There is no fixed value for the term Yg, it varies with where Yt = 2' Yt = 3' etc.• are the yields at the various trophic
organism type (unicellular, multicellular), level ofcomplex- levels.
ity, behaviour (motile or non-motile), and stage of devel- If we make the further simplifying assumption that in a
opment (larva, juvenile, adult) . Typically values lie in the given food web the values of Y can be treated as the same.
range of 10 to 30% (Chapters 12 and 13). then the above equation simplifies to:
overall efficiency = (1';)"
Growth
G where Yt is a simple representative trophic yield and n is
Food intake Y" growth yield = G/(G+M) the number of steps (note. one less than the number of tro-

~~
phic levels) in the food chain. This simple concept was the
M Metabolism basis of the early work to predict the fishery potential of the
oceans (Ryther 1969) . This concept allows us to explore the
significance of growth (trophic) yield and the number of
Figure 3.4 Schematic of the apportionment of overall steps in the food chain.
metabolism of a heterotroph into metabolism (M) and This sort of analysis can be extended to more realistic
growth (G). branched and interlinked complex food webs, with differ-
entyields at various trophic levels. but the broad outcome is
much the same, and at this level the additional complexity
is not justified. The point made by these calculations (Table
3.3.2 Trophic yield and food chain 3.1) is that both properties have a profound effect upon the
efficiency overall efficiency of the food web, and most natural food
chains (and in particular food webs) are, and need to be,
One organism's growth is another organism's meal. If we energetically inefficient. This inefficiencyis a consequence
consider a simple linear food chain, comprised of physio- of the very large fraction respired and recycled back (rem-
logically similar organisms within each trophic grouping, ineralized) to form the inorganic carbon and, more impor-
we can extend the growth yield concept to a trophic yield. tantly. inorganic nitrogen and phosphorus, originally used
In this case the production (growth) at one level is taken as during phytoplankton production. Without this efficient
the food intake for the subsequent one (Chapters 4 and 7) . recycling of nutrients. the food webs in the oceans, as in
production at trophic level. + 1 any other ecosystem. would rapidly stagnate. We may now
fu~k~W=Y= . . ' build recycling of nutrients into our developing conceptual
t production at trophic level.
model ofthe food chain.

Ett.....
Growlh

Growlh Food intoke

G
Food intake Y. = growthyield = GI(G+M) Metabolitm

• Metabolitm

Metabolism
Trophic level 3
Trophic level 2
Trophi( level I

Figure 3.5 The simple scheme shown in Figure 3.4 embedded in a linear heterotrophic food chain. Photosynthetic
primary production (the green ellipse) is taken to be the starting point.
 3.4 The decomposition process
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 3 .1 Ca lculat ion of the effect of trophic yie ld and the number of trophic levels o n overall losses
and yields in a simplifi ed food chain.

Trophic yield (%j Number of trophic levels in the food chain

2 5
Yield offood chain (as %)
10 I 0.001
30 9 0.24
• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Loss through the trophi c levels (%)

10 99 99.999
30 91 99.76

Yield from I tonne of phytoplankton production

10 10kg 10 9
30 90 kg 2.4 kg

3.4 The decomposition and growt h, it is conven ient to consider the decomposition
process as starting from particulate material. Biological
process particulate material mostly consists of organic macromol-
ecules as cellulose, proteins, ch itin, and fats. Protein- and
So far we have explored a simple linear food chain, sup- carbohydrate-like components are most biodegrad able,
ported by photosynthetic production. The losses due to w ith turnover times from months to years in the surface
respiration have been built into this sequence in Fig. 3.6. ocean, whereas other biological macromolecules, such as
We now need to consider the organic losses-the forma- the components of bacterial cell walls themselves, as well
tion and decomposition of organic detritus. This leads to as other molecules of bacterial origin, are mo re resistant
a realization that there is a second base to the food we b: a to enzymatic attack and can persist in the environment
food chain leading from detrital organic material. Although even thousands of years (Loh et aI. 2004; Nagata 2008) .
decomposition is seen to be the prerogative of the microbes The initial stage of the whole degrad ation process is the
(the group referred to by ecologists as the decomposers), it conversion of the insoluble, non-diffusible material to low
is a process to which all heterotrophic organisms contribute , molecular weight (LMW) dissolved material by extracel-
from bacteria to whales, although for the reasons discussed lular hydrolytic enzymes (digestive enzymes) . In principle,
in 3.2.1, bacteria and the protists play the dominant role. the first stage must occur outside the cell, in the gu t, in
vesicles, or in the external environment. Bacteria are obli-
Decomposition of organic material back into energy and gate osmotrophs, i.e. capable of taking only dissolved
inorganic material is a process to which all heterotro- substrates into the cell. They must eit her secre te extracel-
phic organisms contribute, although the microbes play lular enzymes or use enzymes attached to their cell surface
a dominant role. structures.
The low molecular weight products (amino acids, sug-
Decomposition, the breakdown of organ ic material by ars, fatty acids) may now diffuse or be actively transported
heterotrophic metabolism as a consequence of respiration, into the cell, through the cell membrane in single-celled
results in the production of ino rgan ic carbon (as CO2 ) , organisms (bacteria, protists) or the gut wall in the case of
nitrogen (as ammonium) , and phosphorus (as phosphate) ; most metazoans. The subsequent stages of metabolism, and
the process is collectively referred to as remineralization in particular the very final stages (respiration) , are complex
(or sometimes simply as mineralization) . biochemical processes that require a high level of organi-
zation that can only occur w it hin the cell (Chapter 2) . As
the biochemical basis of respiration is rather universal in
3.4.1 Marine detritus all heterotrophic organisms, we can now se parate the first
Although, as we will see later, there is direct release of solu- stage in Fig. 3.4 into these two steps (see Fig. 3. 7).
ble organic material from marine organisms during feeding No food chain is entirely closed, there is always some
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
Trophic level 2
Irephk level I
Food intake
PhatOiynthesii
Reminerolizotion of
C, N, and P
Figure 3.6 The flow of respired nutrients has been added to Figure 3.5.
Growth
Particulate & high
Food intake
MW material
Metabolism
Figure 3.7 An extended version of Figure 3.4, showing
the two stages in decomposition.
wastage of food along the way. Wastage may occur through
faeces. from incomplete digestion, release of soluble
organic material from the algae or heterotrophic organisms
(exud ates), or damage of, or incomplete feeding upon, the
prey (so called 'sloppy feeding') . All of these sources of
wastage are included in the loss term 'excretion' in the food
web model developed in this chapter. Dead organisms are
also part of decaying particulate organic matter. In addi-
tion organic matter is transported from terrestrial ecosys-
tems via rivers to estuaries. coastal waters, and continental
shelf regions. This (both soluble and particulate material)
is collectively known as marine detritus (see Fig. 3.8), the
nature and origins of which are dealt with in the following
section.
3.4.2 The nature and production of
marine detritus
Marine organic detritus is partly composed of the scraps left
over from the various 'meals' of the marine heterotrophs.
As such it has no particular composition and thus will vary
with the type offood organism and the feeding mechanism.
Although organic detritus may be of poor nutritional value
to the organism giving rise to its production. the micro-
organisms have the metabolic and nutritional versatility to
make a meal out ofit. In addition to the uneaten remains
and dead organisms. there are two additional sources
of marine detritus. Various marine organisms. including
Ircphk level3
Ett.....
Growth
Growlh Food intoke
Metabolitm
Metabolitm
the microbes. secrete mucilage or various classes of poly-
saccharide material (exopolymeric substances abbrevi-
ated to EPS; we revisit this in Chapter 8) during their
growth and development; for example, coral are a rich
source of mucilaginous material. Appendicularians (a
class of chordates also known as larvaceans) surround
themselves with a mucilaginous 'house'. which contains
filtering apparatus with which food is garnered. When
the filters become blocked they discard the 'house' and
construct a new one; this process takes a few minutes
and can be repeated up to a dozen times per day.
A quite different source of organic detritus comes
from the algae themselves. The mechanism and causes
of release ofthis dissolved organic material are far from
clear. It occurs in active as well as moribund cells, so it
may be regarded as a 'normal' part of the metabolism
of the algae. The release of dissolved organic material
would appear to be high when the cells are under high
irradiances and in such situations a metabolic pathway
(photo-respiration), closely associated with the primary
CO2 fixation, is known to produce compounds such as
glycolic acid (glycolate) , and amino acids (serine and
glycine) as by-products. However, this is probably only
one of a series of processes giving rise to the release of
these compounds. The extent of release in actively grow-
ing, unstressed cells, is probably in the range of 5 to
15% of photosynthetic production (Chapter 2), but may
rise to 50 to 80% if the algae are stressed by high light or
low nutrient conditions.
Because of its multiplicity of sources and formation
mechanisms, marine detritus is a heterogeneous mix of
compounds and not readily amenable to detailed chemi-
cal analysis. The organic matter in the ocean forms a size
continuum from millimetre to nanometre scales. For prac-
tical reasons the organic matter is typically divided into
two categories based primarily on size. using fine filters,
into so-called dissolved and particulate organic material
(DOM and POM) . The point of separation is not exact but
 3.4 The decomposition process
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Organicdetritus
<,
-, , /' Growth
ElL..

~
Growth Foodinlllke ~ = growth yield = G/(G+ Ml
-, .Y'
Poololynthl.'lil
/'
~ Growth Food inlll ke
,,'
Y =g rowth yield= G/(G+Ml

At ......... Metobolilrn
At .......

/
Metobolilrn

.... Metobolilm /
/
Reminerclizution of
-:
/
/
C, N,a nd P /
Figure 3.8 Incorporation of remineralization and detritu s formation into the diagram in Figure 3.6.

lies in the region 0.2 to 1 urn, determined by the nature,

properties, and loading of the filter used, as we ll as the Tabl e 3 .2 Major organic carbon poo ls' sizes in
morphology of the particles themselves. The distinction the biosphere.
into DOM and POM pools is ecologically relevant, as only
osmotrophs (mainly prokar yotic microbes) can take up
DOM direc tly from seawater, while larger organisms have Pool Pool s iz e
to seek for particulate meals that can be ingested. The dis- (as mol C)
solved organic carbon CDOC) fraction constitutes by far
Ocean ic pools
the largest orga nic pool in the sea, and one of the largest
Dissolved organic material 1 X 10 17
on the planet (see : Box 3.1 figure; Table 3.2). DOC has
Particu late organic material 3 x 10 15
been the subj ect of detailed chemical examination and
Marine plankton 1 X 10 14
yet we have been able to characterize only 5 to 10% as
Fish 5 x 10 12
simple molecules such as amino acids and simple sugars
(hexoses) . The remaining 90% of DOC has been identified
only into broad categories (Ben ner 2002) . While some of Terrestial pool s
the DOC cycles rapidly within the upper part of the water Terrestial plants 5 x 10 16
column, a substantial proportion of the DOC is resistant Soil 2 x 10 18
to d ecay. 14C dating of the resistant material gives it a
half-life of approximately 6000 years. It was previous ly Globa l pools
thought that this recalcitrant material cons isted of com- Foss il fue ls 5x 10 17
plex high molecular weight material and was given the
name 'm ar ine humus', but recent work has shown that
the material has a low molecular weight (be low 1000 d aI- metry) and is commonly referred to as 'm ar in e snow'.
tons) and thus d oes not conform to these earlier notions Early bat hysphere explo rers of the ocean dept hs reported
(Na gata 2008 ) . A major challenge facing the marine marine snow to occur at the scale of a terrestrial snow
chemis t and microbiologists is the chemical nature of this blizzard on occasions . The first step in the creation of
material, it is res istant to decay, and the mechanism of marine snow particles is the agglutination by shear forces
its even tual decay rema ins unknown. The curre nt view of hydrated mucilaginous fibril s released from the plank-
is that its d ecomposition involves photoc hemical and ton to form transparent exopolymer particles or TEPs
microbiological reactions wo rking in consort, but wit h- (Wotton 2004) . The marine snowflakes arise by random
out doubt there is a lot to be learned about this aspect of collis ion of TEPs. In the northern Adriatic these fl akes can
carbon flow in the oceans. reach massive size (Fig. 3.10). As discussed later in this
The particulate organic fraction comprises a melange chapter (Box 3.1 and 3.5 .4) they are a habitatfor marine
of small living organisms , bits and pieces left over from micro-organisms and oases in an otherwise nutritional
the various meals, and particulate material created by desert. It is thought that these flakes are the main vehicle
physicoche mical processes from solu ble detritus. The for the transport of organic matter from the upper ocean to
material (Fig. 3.9) has the general overall appearance the ocean floor and, as such, a vital step in the carbon cycle
of snowflakes (although it lacks their characteristic sym- of the oceans . The fate of marine snow and the rate at which
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

it is decomposed by its bacterial hitchhikers are critical to
the behaviour of the oceans as a potential sink for carbon.
In a simplified form, Fig. 3 .11 builds on Fig. 3 .7 to show
how this 'waste' material will feed back into the food chain.
As shown in Fig. 3 .12 (3.4.3) the flows to the detrital sec-
tion are multiple. They would appear to be equal to 50% of
the primary photosynthetic formation of organic material.

3.4.3 The utilization and recycling of

marine detritus

Detrital material is potentially a valuable food resource.

Detrital material is potentially a valuable food resource

that is utilized by a complex of organisms (t h e decompos-
ers) . To fit this into our developing model of the marine
plankton community and explore the consequences of the
recycling of organic material. we need to depart from our
simple linear food chain, with a single starting point (the
photosynthetic autotrophs), to rwo initially parallel food
chains with separate starting points : one based on pho-
Figure 3.9 Marine snow particle (photograph: Alice tosynthesis, and the other starting from detritus, which
Alldredge). involves the microbial community. In Fig. 3.12 these sepa-
rate food chains are shown to merge at one point; the reality
is more like that depicted in Fig. 3 .19 in which the whole
system is more of a complex network of feeding and nutri-
tional interactions.
Whereas organic material can only pass through respira-
tion once, a single carbon atom (also a nitrogen or phos-
phate atom) in organic material can be taken up by marine
organisms several times before it is respired. This intro-
duces the concept of organic recycling within the plank-
ton community. The consequence of recycling is that the
organic material used by the planktonic. or any. community
will be greater than the primary introduction of organic
material. If we know the fraction recycled (let us call this
Ydet) it is a simple matter to calculate the total amount of
material passing through the food web. If we take a com-
Figure 3.10 A massive marine 'snowflake' in the northern monly estimated figure ofabout 50% recycled through each
Adriatic (photograph: Michael Stachowitsch). cycle (Nagata 2000), then of the original amount, 50% will
be recycled on the first pass, 50% of that (25% of the origi-
POM recyrling nal) on the second pass. etc., and the total amount passing
through will be in this case:
Growth

Partculote & high low MW diffusible

-> 1 + 0 .5 + 0.25 + 0 .125 .. .
or 0.5 0 + 0.5' + 0.5 2 + 0.5' + ... ,
MelDbol i~m
MW malerial material
or expressed more generally:
<, Dissolved organic
malerial
Y ~et + Y 1et + Y ~et + Y ~et + K
I
DOM recycling This is a mathematical series with a surprisingly simple
solution:
1
Figure 3.11 Extension of Figure 3.7, showing the
1- Ydet
recycling of particulate and dissolved organic material Thus ifYdet = 0 .5, then the total amount of organic material
back into the food chain. passing through is 1/(l-Q.5} = 2.
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

<,
-, G
<,
G,"",
<,
-,
Food intoke r
G-I G_

growlhyie ld = &(G+ Ml
Ell ....

W
"\ <, r growlh yield &(G+Ml
"'-, ....... •
Melcbolhm

.
Grcwlh Food intoke
.> •

<: ~ Metabolilm
Photmyn!h~~

------...
-." Metabolim.

--
~ .ISbaled load th'in
pno\OS'fn,hIlS -
c

"'
e•
0
-;
.-
a
'e

-a
c
0

l! <, '<,

Q
-, -, <,
G..... G,o. h" Food intake
G"
,•
Growth

grllwlh yield GlIG+M)

EIt.....

\
~ Growth
'<,

Food intake ,• grllwth yield G/(G+ Ml • Metabolism

Detr~al
meterial '. growllJ yield GI(G+M) • Metabolilm
/'
,/

~
Metabolism
oetti,us-basedtood thain
/ /
/
/

Figure 3.12 The dual food chain, showing the two starting bases: photosynthesis (the green ellipse) and organic
detritus (the red ellipse). The detritus-based food chain can start from bacteria (capable of consuming both POM and
DOM) or other organisms (consuming POM). Arrows from "metabolism" boxes to the detritus pool represent excretion,
exudation, and sloppy feeding (3.4.1 and figure 2.25).

3.5 Key organism groups in
the oceanic microbial food
webs
We will now set the organismal biology on the conceptual
background presented earlier in this chapter. Marine plank-
tonic microbial communities discussed in this chapter are
very diverse and can be classified and divided into different
categories according to the approach chosen.
From a taxonomic point ofview, life on Earth is classified
into three major phylogenetic groups: prokaryotic bacteria.
archaea, and eukaryotes. Prokaryotes have no membrane-
bound organelles such as nucleii (karyon) in their cells,
from which the name emerges. Eukaryotes comprise all
macroscopic organisms like animals. plants, and fungi ;
whereas all prokaryotes are microscopic, single-celled
organisms. Viruses do not have their own metabolism. are
not considered living organisms. and have a separate clas-
sification (Tree of life project at http:/ /tolweb .orgltree/
phylogeny.html) . All these taxonomic groups are well rep-
resented in the marine plankton.
Another approach to marine microbial diversity is to
look at functional groups that are (from the ecological point
of view) rather uniform, although most often comprise
phylogenetically distant species. The ecologically relevant
grouping of these organisms is based on the function of
the organism as a part of the microbial food web. The most
important criteria for functional grouping are size of the
organism and the way it acquires its energy. For example.
body size together with some other morphological features
determine the possible range of prey available to a gra z-
ing or predatory organism. In the following section we will
present the major features offive of the most important eco-
logical groups present in the marine plankton and compris-
ing the oceanic food webs, these are : marine prokaryotes
(bacteria and archaea), viruses. algae, protozoa. and mul-
ticellular zooplankton. We will also discuss the microbial
food web they form in the pelagic realm of the oceans.
3.5.1 Marine prokaryotic microbes
Marine prokaryotic microbes belonging to phyla Eubocte-
ria (bacteria) andArchaea (archaea) are central in organic
matter degradation and nutrient remineralization in the
oceans. Because of their importance. we discuss their diver-
sity, ecology, and techniques used in their study in the fol-
lowing subchapter in depth. l\vo major physiological types
of prokaryotes are discussed: organotrophs and nitrifying
chemolithotrophs.
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
Chemolithotrophs are autotrophic prokaryotic microbes
deriving their energy for growth from inorganic reduced
compounds and capable of fixing atmospheric carbon
dioxide for their carbon demand.
Organotrophs are heterot roph ic prokaryotic microbes
deriving their energy and carbon from decomposition
and respiration of organic material produced by auto-
trophic organisms.
Although they appear identical under the microscope,
bacteria and archaea form two deeply distinct evolution-
ary lineages, indeed in phylogenetic terms they are as dis-
tant from each other as they are from eukaryotes. They
are minute in size (typically below Iurn I 0 .001 mm),
and reproduce by binary fission in which the cell divides
into two identical daughter cells at a certain point in its
growth. Archaea have been found to be important compo-
nents of marine microbial communities, especially deep-
water habitats. However. these discoveries have occurred
only during the last 10 years and therefore they are less
well-known compared to bacteria. In the following text
we will use the terms marine prokaryote or marine pro-
karyotic microbe referring to both bacteria and archaea.
However, at present most of the available research con-
cerns marine bacteria.
Organotrophic marine prokaryotic microbes. or simply
organotrophs, are mainly responsible for the degradation
of organic matter. These organisms gain energy for their
growth from the respiration (Chapter 2) of organic mate-
rial. They are also defined as heterotrophs because they
rely on organic carbon fixed by other organisms (ultimately
autotrophic organisms. i.e, primary producers. as discussed
in Chapter 2) . Because of their genomic and metabolic
diversity they are able to break down nearly all naturally
produced organic material and many synthetic chemicals,
which is usually not the case with other groups of organ-
isms that degrade organic matter. In addition, they are
osmotrophs, i.e, able to take up dissolved organic matter
from their environment and thus have access to the vast
pool of dissolved organic matter in the ocean that is mostly
unavailable for larger organisms.
Another important group of marine prokaryotes dis-
cussed in this chapter are chemolithotrophic nitrify-
ing prokaryotes (also both bacteria and archaea) (Ward
2000) . They are autotrophic as they acquire their energy
for growth solely by oxidizing reduced inorganic nitrogen
compounds and their carbon. from which they create new
biomass. by synthesizing organic carbon from CO 2 with
chemical energy.
Identifying marine prokaryotes
Taxonomic classification of an organism is based on its
distinguishable morphological, metabolic, or genetic char-
acteristics that solely. or in combination, separate it from
other species of organisms. The concept of 'species' in
the sexually reproducing organisms. such as animals and
plants, is also defined by interbreeding ability that leads to
viable offspring capable of reproduction. Distinguishable
morphology or metabolism are difficult to use in classifica-
tion of marine prokaryotes (see below), and interbreeding
ability as a basis for species identification is not applicable
as they reproduce by binary fission .
Marine prokaryotes most often lack decisive morpholog-
ical characteristics that could be used in their classification.
There are only two broad morphological categories: cocci
(spherical cells) and rods (elongated cells) . These catego-
ries can be divided into a few further subcategories, like
straight or curved rods. In addition. there are some specific
cell shapes that are not common, like corkscrew-shaped
spirilli (Fig. 13.3 A) and stalked bacteria, which are able to
attach to surfaces with an elongated stalk. Cell size varies
(Fig. 3.13. A-C) according to nutritional status of the cell,
as well as the phase of the cell cycle (near division cells are
larger, and daughter cells correspondingly smaller) .
In order to study the metabolic characteristics of an
organism it is necessary to isolate it from its environment.
and from other organisms that share the same environ-
ment. and to then maintain it in culture. Such separation
and establishment oflaboratorycultures for the vast major-
ity of the marine microbes has not been possible so far. This
is because traditional microbiological culturing on nutrient
rich media is only successful for a few groups that are able
to grow in high-nutrient environments and respond rapidly
to an increased availability of resources. e.g. those organ-
isms associated with estuarine environments or decaying
algal blooms. Culturing of oligotrophic bacteria, i.e . bac-
teria adapted to a low availability of substrate. nutrient, or
'food' in seawater, has only been successful with one bacte-
rial group. the SARlI Cluster. with one strain maintained
in long-term culture (Giovannoni et al. 2005) .
Due to their lack of morphological characteristics and dif-
ficulties in culturing marine prokaryotes discussed above.
we need other methods to describe and study marine pro-
karyotic microbial diversity and ecology. Most contempo-
rary studies of microbial community composition are based
on use of molecular markers (either DNA or RNA-based),
avoiding the cultivation process that inevitably misses most
of the marine microbes (Fuhrman 2009) . Use of molecular
methods in the study of marine prokaryotes is an example
of how molecular ecology enables us to expand our views
beyond the horizon of traditional (based on morphology
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
Figure 3.13 Seawater samples filtered on membrane
filters, stained with fluorescent Acridine Orange stain and
viewed with epifluorescence microscopy (at
x 1250 magnification). (a) Various bacterial morphotypes,
including cocci (round cells), rods (elongated cells), and
one corkscrew-like spirillum in the lower centre of the
photograph. (b) Cyanobacterial filament being converted
from living organism to detrital POM and DOM. At the left
end of the filament, cells are still intact but the other end
is rapidly decaying. Attached bacteria (arrows) can be seen
on the surface of the filament. (c) Very large bacterial cells
and a small marine ciliate (photographs: Riitta Autio).
and metabolic characteristics) methods. Molecular ecology
is a field ofbiology that applies molecular population genet-
ics. phylogenetics, and genomics (see Current Focus) to
answer ecological questions. Molecular methods are appli-
cable to the study of the ecology and diversity of various
organism groups (both pro- and eukaryotes) and are widely
used in modern marine ecology. Culture-independent
genetic analysis is a particularly powerful tool for obtaining
knowledge of marine microbes. their community compo-
sition. and ecology. Culture-independent genetic analysis
requires the extraction of nucleic acids (DNA or RNA) from
biomass (obtained from environmental samples or cultured
organisms) followed by the determination of their nucleic
acid sequence. Single or multiple genes, or even a complete
genome, of an organism (Current Focus) can be targeted.
Identification and classification of microbes is typically
based on gene regions that are conserved. i.e. there is little
variation in their nucleotide sequence with time. There are
two key genes involved in identification of microbes: the
165 rRNA gene that encodes the small subunit of ribosomal
RNA in prokaryotic cells, and the IT5 regions (Internal
Transcribed Spacer region between prokaryotic 16S and
235 rRNA genes) . The 165 rRNA gene is highly conserved
as it forms an essential part ofa cell's basic protein synthesis
machinery. The species concept in prokaryotic organisms in
general is subject to ongoing discussion. One suggestion for
the definition of a prokaryotic species is: a coherent cluster
of individual organisms with uniform evolutionary origin
that have a high degree of overall similarity in many inde-
pendent characteristics that can be separated from other
species (Rossello-Mora & Amann 2001) . For practical
purposes species are often defined based on the percent-
age similarity of nucleotide sequence investigated, with
97%similarity representing a commonly used cut-off for a
boundary between species. Another way to express this is
to consider a speciation to occur when a dissimilarity of 3%
occurs in the nucleotide sequence. A scientific description
ofnew prokaryotic species necessitates that the organism is
cultured to enable the description ofits phenotypic (observ-
able) physiological and morphological characteristics.
Major organic-matter degrading prokaryotic
microbes in seawater
Organotrophs are, in principle, capable of breaking down
nearly all natural organic matter. The availability oforganic
matter is one of the main factors that regulates bacterial
growth. biomass, and also community structure in the
ocean. For those bacteria that degrade organic matter.
the ocean is an extremely challenging environment. The
introduction of new organic matter into the system (either
allochthonous. i.e. entering from the land via rivers or
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

autochthonous, i.e. produced within the marine envi-
ronment) is extremely variable in time and space in scales
relevant to us and even more variable in scales relevant to
microbes (think about the variation in organic loading that
occurs during a winter flood versus a summer drought)
(Box 3.1) . Other factors that regulate community composi-
tion are the availability ofinorganic nutrients and trace ele-
ments, physical and chemical conditions (e.g. temperature,
pH), predation, viruses (see below), and competition. The
relative importance of these different ecological factors for
microbial communities is currently unknown (Fuhrman &
Hagstrom 2008) .
As is the case for other organism groups (e.g. planktonic
algae and zooplankton) in the marine pelagic environment.
marine prokaryotes also have typical major taxonomic
groups that characterize their communities. The majority
of heterotrophic and chemolithotrophic marine prokary-
otes occur in about a dozen major phylogenetic divisions
(Phyla or Kingdoms), which are commonly found world-
wide (Fuhrman & Hagstrom 2008). The most ubiquitous
groups among the planktonic prokaryotes are the groups
Proteobacteria, Bacteroidetes, Planktobaeteria, and marine
Actinobacteria, as well as the archaean groups Creanar-
chaeota and Euryarchaeota (Fig. 3.14) . Some groups can
be easily cultivated and studied in the laboratory, whereas
others do not thrive in culture and are only known by their
DNA sequences found in environmental samples.
Although the ecological niches of marine bacterial
groups are still not well-understood, recent research sug-
gests that some marine bacterial groups have defined
niches in organic matter degradation. Bacteroidetes have
been associated with degradation of protein and chitin,
whereas some subgroups of y-Proteobacteria seem to be
specialized in the utilization of simple sugars or amino

Archaea
Crenarchaeota Euryarchaeota
Group IArcheeu Group II Armeen
Group III Archeeu
Group IV Archoeo

a-Proteobocteria
"SARTI - Pefagibaderia ubique
"Roseobaderclade
0(1116
Chloroll,,;
SAR202 ---J.. fl-Proteobocteria
' OM43

~
~::::::::-_ _- - IJ-Proteobocterio
IARB6
'OMGaod,
"Vibrionaeceae
"Pseudoafteromonas
Fibrobacter "Marinomonas
SAR406 *Halomonadacae
Bacteroidetes '(olw,lIio
"Oceanaspirillum
Marine Actinobacteria
3·Proteobocterio
Cyanobacteria
"Morine duster A
Lentisphaerae ISy,,,h,,occus)
"Lenfisphaera araneosa
"Prochlorococcus sp.

Bacteria

Figure 3.14 Schematic illustration of the phylogenetic relationships of the major marine planktonic prokaryote clades
(groups with a common ancestor). Black letters indicate ubiquitous microbial groups in seawater. Green colour ind icates
microbial groups associated with coastal ocean ecosystems, grey groups found in t he photic zone and blue groups
confined to the mesopelagic and surface waters during polar winters. (Illustration: Giovannoni & Stingl 2005.)
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
acid monomers that occur in high concentrations. Marine
a -Proteobacteria (SARI l) are particularly well-adapted to
take up dissolved amino acids at very low concentrations
in pelagic environments (Cottre ll & Kirchman 2000; Eilers
et al. 2000; Church 2008) and can comprise up to 25- 33%
of total abundance of many pelagic prokaryote communi-
ties (Morris et al. 2005) . The specialized role of different
microbes in organic matter degradation in the ocean under-
lines the need for better recognition of these microbes and
an improved understanding of their ecological role in regu -
lating important oceanic biogeochemical cycles.
Nitrifying prokaryotic microbes
In the process of nitrification, inorganic nitrogen from
reduced ammonium is oxidized into nitrate (see Chapter 2).
Nitrification is the biological oxidation of ammonia with
oxygen to nitrite and further to nitrate.
Ammonium is a common nitrogenous waste product of
heterotrophic metabolism .
The nitrification process is exclus ively biological,
whereby ammon ium is conve rted to nitrate, which is used
rapidly by phytoplankton in the photic zone but accumu-
lates in the deeper water layers. It is because of the nitrifi-
cation process that the major pool of fixed nitrogen in the
world's oceans occurs in the form of nitrate (Ward 2000).
Nitrification is performed by two different functional
groups of marine prokaryotic microbes in two separate
CURRENT FOCUS: Marine microbial
• As many of the marine microbes are difficult, or so far
genomlcs
Genomics is t he study of an organism's complete
genetic information that is encoded in its DNA nucleotide
sequence. Because prokaryotic (bacterial and archaean)
genomes are considerably smaller and simpler t han
eukaryote genomes, they have been the focus of much
research in the last 10 years. Metagenomics (also referred
to as 'environmental genomics' or 'community genomics')
is defined as the cult ure-independent genomic analysis
of microb ial assemblages or populations, i.e. analysis
of genomic information obtained directly from a sample
taken from t he environment (Moran 2008; Fuhrman
2009). Cultu red organisms provide complete genome
sequences and access to organism physiology, while
metagenomic sequences show the abundance and distri-
bution of genes and genome fragments from organisms
that have not been cultures (Moran & Armbrust 2007).
steps : in the first ste p, am mon ium is oxidized to nitrite
by ammonium-oxidizing bacteria and then subsequently
nitrite is oxidized to nitrate by nitrite-oxidizing bacteria
(Treusch et a1. 20 05). Ammonium oxidizers are chemoli-
thotrophic organisms that use carbon dioxide as their m ain
carbon source. They are typically slow-growing and gain
their energy for growth by the oxidation of ammonium to
nitrite. Both reactions use oxygen as an electron acceptor. In
most environments both organisms occur together, yielding
nitrate as the final end-product. Oxidation of ammonium to
nitrite is usually the rate-limiting step of nitrification. Nitri-
fying prokaryotes have limited diversity compared to pro-
karyotes that degrade organic-matter, and m ainly belong to
Proteobacteria (Purkhold et al. 2000) and Cren archaeota
(Lein inger et al. 20 06; Wuchter et al. 2006).
Individual species of nitrifiers represent approximately
0. 1 % of the total bacterial assemblage and have their maxi-
mum abundance near the bottom of the photic zone (Ward
2000). In open oceanic waters the highest nitrification rates
are measured near the base of the photic zone in the upper
100 m of the ocean, where conditions are optimal for nitri-
fication, and also competition for ammonium and nitrate
from autotrophic phytoplankton is less intense. It is a com-
bination of light and the availability of substrate that are the
major factors that determine the magnitude and location
of nitrification rates in both vertical and horizontal scales.
As ammonium concentrations in water are partly the result
of the intensity of organic m atter production and degrada-
tion, highly productive systems such as upwelling areas
have high nitrification rates (Ward 2000).
impossible, to maintain in laborato ry cultu re for tradit ional
microbiological studies, culture-i ndependent techniques,
including environ mental genomics, are an important tool
for studyi ng the diversity and metabolic capa bili ties of
uncultured organisms and thei r possible roles in marine
ecosystems.
The development of molecular methods has made
marine microbial genomics possible only recently. In 2007
there we re approximately 30 complete marine bacterial
or archaeal genomes available for study (Moran & Arm-
brust 2007; Moran 2008), whereas by 2009 hundreds
of whole or draft bacterial genomes we re available in
public databases (Delong 2009) . In addition to complete
genomes, the metagenomic data obtained directly from
natural marine microbial assemblages is growi ng rapidly.
Although microbial geno mes are small compared to
eukaryote genomes, they still contain millions of nucle-
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
otid e base pairs and thousands of genes. Genes are
defined genome regions that contain the necessary infor-
mation to maintain cell functions and reproduce from th e
code in the sequence of DNA nucleotides. To study the
genetic inform atio n stored in the nucleotide sequence, it
must be decoded. In practice this is done by processi ng
short DNA pieces (fragments) in automa tic sequencing
machines that produce the DNA sequence information
found in each f ragment Sequence information is then
assembled like a puzzle into a complete genome by
automated computer prog rams that find the correct place
for each short piece of code by identifying overlappi ng
sequence regions in the different frag ments. Assem bly
of the code cor respo nds to the construction of the circle
seen in figu re A. Afte r assembly, the genome needs to
be annotated. The location and identity of genes wi thin
the genome are determined from the annotation, which
can be undertaken by automated computer prog rams.
Annotation corresponds to the coloured lines and their
locations along the ci rcle in figu re a. Once annotated,
putative genes can be searched fo r from the genome.
Putative gene sequences can then be compared to exist-
ing sequences in gene-sequence databases and thei r
possible function determined. This correspo nds to finding
the right colou r for each of the coloured lines in figu re a.
Genome mort of
onorganic motter·degrading
= marinebacterium --
4010 pr,tein gen es
IIRNA gen..
(a) Genome chart of an o rganic-matte r deg radi ng
marin e y-Prot eo bact eriu m. The ci rcular form co rre-
sponds t o the bacterial ge no me st ructure, t he size of
the genome in thousands of base pairs (kb) of DNA
sequence is shown in t he outer rim. Each co lo ured lin e
represents a po ssibl e gene ident ificatio n, w hile t he
co lours represent various functional classes of genes,
e.g. 'protein synt hesis' or 'ion (nut rie nt) transport'.
Management and analysis of massive amounts of genetic
informa tion is demandi ng and constitutes a separate field
of science called bioinformatics. The advent of novel
sequencing tech niques (e.g. shotgun sequencing and
pyrosequencing) has made the production of massive
amounts of new genomic information possible. Func-
t ional genomics attempts to describe gene and protein
interactions and, ulti mately, function of organisms in their
envi ronment Importa nt areas in functional genomics are
transcriptomics (analysis of gene expression) and pro-
teomics (analysis of protei n expression), which can be
studied in cultured organisms, envi ronmental samples, or
both.
Two key initiatives that have advanced availability of
marine microbial genomic data in the recent years are
J. Craig Vente r Inst it ute's Global Ocean Sampling (GaS)
Expedition, and the Gordon and Betty Moore foundation's
Marine Mic robial Genome Sequencing project (http://
www.jcvi.orgl). Venter (also known from his maj or con-
tribution to the human genome sequenci ng project) and
his team have made several majo r voyages throughout
the world's Oceans, wi th Sorcerer II, a 100-ft sailing
yacht fitted wi th the scientific equipment necessary to
obtain the microb ial samples from oceanic w aters. The
samples are then processed and sequenced using tech-
niques developed for the human genome project Sor-
cere r II conducted a world ci rcum navigation between
2003 and 2006, followed by a sampling voyage arou nd
North America and in Southern Ocean waters in 2007 to
2008, and finally in 2009 to 2010 samples in the North
Sea, the Baltic Sea, the Mediterranean, and the Black Sea
were collected (see figure b) . The fi rst part of the global
ci rcumnavigation expedition alone pro duced 6.3 million
base pairs of new environmental marine DNA, w hich was
pu blished by Rusch et al. (2007). The GaS dataset has
expanded significantly our unde rstanding of the diversity
and function of oceanic microb ial and viral community
diversity and thei r possi ble functions.
In the Gordo n and Betty Moore Foundation's Marine
Microbial Genome Sequencing project, the J. Craig Ven-
ter Institute is sequencing, and making publicly available,
the genom es of 16 5 cul tivated marine microbes. The
microbes sequenced are contri buted by 79 scien tific col-
laborators wo rldwide, and represent the major mari ne
taxa. These organisms embody an array of physiological
diversity including: carbon fixers, photoautotrop hs, pho-
toheterotrophs, nitrif iers, and methanotrophs. Both GOS
and the Marine Microbial Sequencing project make their
genomic data available thro ugh CAMERA (The Community
Cyberinfrast ructu re for Advanced Marine Microbial Ecol-
ogy Research and Analysis) that is an onli ne database
and high-speed computational service, as well as an infor-
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
(b) Routes of Sorcerer II sampling voyages in 2003-10 (image from : http://www.jcvi.org /cms/research/projectsj
gos/overview/).
mation resource developed for marine microbial genomi c
analysis (http:/ /camera.calitZ.netl).
A genome consists of genes with different functions that
are vital for an organism's cellular functions. Genes can
be assigned to multiple functio nal categories according
to major cellular functions. Figure A shows the genome of
a marine bacterium that degrades organic matter, where
each coloured strip presents a putative gene and each
colour represents a functional category. A concept ual divi-
sion between the 'core' genome and accessory 'flexible'
genome can be made. The core genome tends to perform
central housekeeping fu nctions, such as DNA and protei n
synthesis. These core genes (e.g. the 16 5 rRNA gene) are
typically also used to identify organisms and to construct
the phylogenetic relationships between them. The flexible
genome encodes the accessory functions, such as trans-
port of nutrients and cell surface properties, which con trol
the niche adaptations, i.e. define where the organisms can
th rive. The flexible genome is more variable than the core
genome and enables organisms to adapt to new envi ron-
ments (Fuhrman 2009). For example, the marine cyano-
bacterium Prochlorococcus, one of th e best-known marine
prokaryotes, contains approximately 1200 core genes and
4000 flexible genes. The high proportion of flexible genes
ensures efficient adaptation to changes in the environ-
ment. Although more variable, the flexible genome seems
to be typically congruent with the core genome, w hich
suggests the existence of stable ecotypes whose distribu-
tion can be predi cted from environmental factors.
- 2003 - 2008 Routes - 2009 -2010Routes
Genomics can reveal the complete genetic informa-
tion of an organism , from which the genes responsible
for basic or novel biogeochemical processes in the sea
can be traced. One goal of metagenomics is to link par-
ticular ecosystem fu nctions (e.g. specific nitrogen cycle
processes) to parti cular organisms (Fuhrman 2009) .
Genetics-based hypotheses, e.g. regardi ng the function
of a particular gene or organism in its environment, can
be created and subsequently tested , either in enviro n-
mental or laboratory studies. Marine microbial genom-
ics has led to unprecedented discoveries in rece nt years;
for example, based on genomic data from an uncultu red
marine bacte ria, a novel way to obtain energy from light
via a proton pump was revealed and found widespread in
heterot roph ic oceanic bacterioplankton (Beja et al. 2000,
2001) . This discovery could ultimately alter our view on
energy assimilation in th e surface ocean.
The future challenges for marine microbial genomics lie
in the meaningful integ ration of genomi c information into
process and ecosystem studies (see figure c). At present
we are only slowly deciphering the identity and genomic
diversity of marine prokaryotic microbes responsible for
major ecosystem and processes in the ocea ns (see figure
c). The next steps will req uire bridgi ng th e gaps between
genomics, metageno mics, microbial physiology, biogeo-
chemistry, ecology, and physical oceanography to create a
clearer picture of microbial systems that drive energy and
matter flux in the ocean ecosystems (Fuhrman 2009).
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

Community composition
andinteractions

I CommunityDNAI
1EcosystemfunctionsI
Diatoms
Dinoflagellates
Climatic
~iates feedback co,
Gosemissions
r'---'-"

'te Jc9 Dimethyl sulphide t I

~Cyanobacteria
Bacteria CO 2 .. Oceon microbiome .... DOC
Archoea
Viruses Cyonophoge
~~o I
P, N, I cycling
LI POC
ICommunity metabolism I t
{arbon
fixation
Methene
metabolism
Redudive Sulphur
carboxylate metabolism
cycle

Nitrogen
Oxidative metabolism
phosphorylation

(c) The network instructions enco ded in microbial gen om es drive ecosystem processes. This schemat ic s hows
hypothetical linkages between th e ge no mic information of th e mi cro bial assemblage a nd the co llect ive ecological
interaction s and com munity metabolism that in part regulate and sustain bio geo ch emical and eco system p ro-
cesses. Each DNA circle in th e left panel represents a g enome derived from a marine bacterioplankton species.
Co-occur ring m icro-organi sms that inhabit the same enviro nment co llectively form the pool of genes sam pled in
metagen omi c st udies. These inst ructions modulate co mmunity interactions, metabolism, and ecosystem function.
(Ill ust rat io n and fi gure capt ion f rom : D elong 2009 .)

Marine bacterial populations

Bacterial cells in a given environme nt belonging to t he
same species form a population. Cells in a population have
variable physiological states (dead, alive, healthy, ill), as
is typical also fo r higher organisms (like humans) in their
populations. Bacteria have, however, also other possible
physiological states as a result of their small size and versa-
tile metabolic capabilities (del Giorgio & GasoI2008) . Some
bacterial cells observed in a population are actually already
dead but still intact, because the bacterial envelope and cell
wall components are refractory (diffic ult to decay). Some
cells are dormant (analogo us to hibernation) but capable
of growt h after a certain period, whereas some are starved
(analogo us to hunger), i.e, suffe ring lack of food but the
metabolism only partially shut down. Only a fraction of the
population is active and growing, of which only the most
active cells are capable of reproduction by division. Larger
bacteria are generally more active than smaller bacteria,
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

which often are starved cells that have become 'miniatur-
ized' to enhance their survival.
There are multiple factors that regulate bacterial popu-
lations in the ocean but th e two basic categories of control-
ling factors are :
1. Control of growth rates, which includes substrate
(organic or inorganic) type and its availability, nutri-
ent availability, temperature, salinity, and pressure, all
factors that affect the rate new cells enter into a given
population.
2. Mortality-controlling factors. such as protozoan preda-
tion, viral mortality. competition, and starvation, which
determine cell activity or its removal from the popula-
tion.
When growth exceeds mortality, th e population grows, or
alternatively diminishes when mortality exceeds growth.
The most important adaptive trait for biodiversity a nd
the function of marine bacteria is the persistence of a pop-
ulation despite long periods of unfavourable conditions.
Persistence of a population is achieved through adaptation
to starvation and dormancy strategies that allow survival
and growth of species through untypical environmental
fluctuations. Different species have variable general eco-
logical strategies to survive and flourish in their environ-
ment, which, in terms of substrate or 'food' availability, is
dil ute and unpredictable in time and space.
Bacteria can be divided between two general ecological
strategies: those that exploit patchiness in the environment.
and those that compete efficiently at low ambient nutri-
ent levels (Giovannoni & Stingl 2005) . Patch exploiters,
also known as r-ecotypes (Fuhrman & Hagstrom 2008),
are species that can respond to a sudden increase in 'food'
availability, and grow and multiply rapidly. Their popula-
tion size can vary widely in response to favourable growth
conditions. i.e. they can become dominant in the bacterial
community following the onset of favourable conditions,

101 Ibl
Globol
Extinction dispersal Molecular techniques Pure culture techniques

- • -:-- -
• • -
-...,-=
c
-...,-=
c
•
• • •
• •
•
• • • •
•
•
•
•
• •
c c
Death Immigration
~

::E
~
c
Predation,
-sa
~
.~
c
•
virallysis

Abundont ~.---- Taxon ronk -----. Rore Abundant ~.---- Toxon rank - - - - - . Rore

Figure 3.15 Plots of number of individuals versus taxon, with taxa ranked according to their respective abundance.
(a) The total curve represents biodive rs ity and is postulated to be composed of two sections: (i) diversity (red), which
contains the abundant taxa that have an active role in carbon and energy flow in a given ecosystem . These taxa are
maintained by active growth and suffer losses because of predation and viral lysis. The insert shows two autotrophic
flagellates (with red autofluorescence of chloroplasts), one heterotrophic flagellate (large green shape), and bacteria
(small green dots), and corresponds to a winter sample from the Beaufort Sea (photograph by Dolors Vaque). (ii) The
blue section of the curve corresponds to rare taxa, w hich survive in the ecosystem at low abundance, perhaps with
resting stages or spores. This 'seed bank' recruits new species through immigrat ion. Because of the easy dispersal of
micro-organisms, it is li kely that essentially all micro-organisms reach t his ecosystem periodically. One advantage of
being rare is that these micro-organisms eminimize viral attack and predation ; thus, extinction can occur only as a result
of cell deat h. Because extinction can be expected to be low while immigration is probably high, this part of the curve
might be long and perhaps include the whole biodiversity of micro-organisms. (b) The same curve il lust rates which
port ions of biodiversity can be retrieved with different techniques. Molecular techniques can presumably access most
taxa in the diversity part of the curve (solid arrows) but the biodiversity tail is usually not accessible. The left-hand
insert shows RFLP patterns of 185 rDNA clones from a library constructed from a coastal Mediterranean sample of
pico-eukaryotes (photograph by Beatriz Diez). Pure cult ure techniques can only retrieve a few of the taxa present in the
environment (broken arrows). However, these techniques have the potential to retrieve bot h abundant and rare taxa. The
rig ht-hand insert shows Petri dishes wit h ZoBell's medium inoculated with a sample from the coastal Mediterranean
and incubated in the dark. Yellow and orange colonies correspond to Bacteroidetes, small light-pink colonies are
Roseobacter species and the large whi te colonies are y-proteobacteria (photograph by Jarone Pin hassi, il lust ration and
figure caption from Ped r6s-Al i6 2006).
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
but rapidly become scarce when the conditions deterio-
rate . These organisms often have a colony-forming mode
of growth and typically can be associated with high pro-
ductivity habitats, e.g, estuaries or offshore algal blooms,
or marine snow plumes (Box 3 .1; Azam & Long 2001) .
Typical bacterial groups belonging to r-ecotypes are some
culturable y-Proteobacteria and the Roseobacter group of
n-Proteobacteria (see above) .
Species that are able to effectively compete for scarce
resources are called K-ecotypes (Fuhrman & Hagstrom
2008) or oligotrophs, They favour a single-celled growth
mode and are well-adapted to oligotrophic (low-nutrient)
conditions in open pelagic waters; they are often unable to
respond to nutrient inputs but can utilize scarce resources
efficiently. In contrast to r-ecotypes they typically have rela-
tively stable population sizes that fluctuate near the car-
rying capacity of their environment. Examples of bacteria
considered to be K-ecotypes are organisms belonging to
SARlI cluster of the a-Proteobacteria.
Bacterial communities
Organic matter-degrading prokaryotes form distinct com-
munities that consist of populations of bacterial species.
Typically a community consists of a few abundant species
and numerous rare species with low abundance, forming
a 'long tail' in species rank abundance plots (Pedr6s-Ali6
2006; Pommier et al. 2007) . Such a relationship is also
common in communities of higher organisms.
Abundant species (marked red in Fig. 3.15 on the pre-
vious page) change according to the changes in the envi-
ronment. and community assembly rules with seasonality.
availability, and quality of organic matter contributing to
the former, and viral attack, competition, and community
history to the latter (Fuhrman 2009) . Persistence in a pop-
ulation, despite long periods of unfavourable conditions
(rare species, marked blue in Fig. 3 .15), is an important
adaptive trait for biodiversity and the function of marine
bacteria, as it allows the survival and growth of species
adapted to changes in the environment that occur sporadi-
cally.
Abacterial community in any given environment is com-
posed of bacterial populations with different physiological
profiles that form a mosaic of activities within the com-
munity. The proportion of active cells increases along with
overall system productivity, but these active cells are also
those that are most effectively removed by predation and
viral attack (del Giorgio & Gasol 2008). In general, bac-
terial communities are highly dynamic with high species
turnover and most species have narrowniches and compete
for the same resources (Pommier et al. 2007) . A bacterial
community, seen as a whole, is suggested to be always capa-
ble of utilizing resources, i.e . organic matter, in an optimal
way because well-adapted species, although present in pro-
portionally low numbers. are always present.
In the euphotic zone bacteria generally have average dou-
bling times of the order of a few days, so it is reasonable to
expect community changes on similartime-scales. Bacterial
community composition can change by up to 10-20% per
day in extreme circumstances (Hewson et a1. 2006); how-
ever, typically. community composition is rather stable over
daily and weekly time-scales and possibly for months (Rie-
mann & Middelboe 2002) . The rate of community change
depends upon the prevailing environmental conditions
and stability. On seasonal time-scales succession resem-
bling that of overall plankton dynamics can be expected for
stable bacterioplankton communities. Seasonal studies of
succession are rare but suggest that bacteria have repeat-
able seasonal patterns in the North Atlantic (Morris et a1.
2005), the Pacific (Brown et al. 2005; Fuhrman et al. 2006),
and the Baltic Sea (Pinhassi & Hagstrom 2000). Since envi-
ronmental factors exert control over community composi-
tion, repeated seasonal patterns in the bacterial community
composition indicate both a strong forcing by the environ-
mental factors and well-defined ecological niches for the
dominating bacterial species (Fuhrman & Hagstrom 2008).
In terms ofspatial scales. bacterial community composition
is highly variable at a microscale (l x 10.6 L of seawater
typically harbours 1000 bacteria), especially when con-
sidering the differences in bacterial composition between
free water and communities attached to particles, such as
marine snow (Box 3.1) . However. microscale variations are
integrated at scales from litres (the size ofa typical environ-
mental sample) to the kilometre scale (Hewson et al. 2006) .
Again, at larger scales of a few to <50 km, the variation in
community composition increases, probably reflecting dif-
ferences in water masses created by the large-scale oceano-
graphic forcing (Hewson et al. 2006; see also Chapter 7) .
Independent patterns of large-scale community com-
position patchiness, probably governed by currents and
production history (creating different amounts of marine
snowfall), can be found at depths between 300 and 500 m
(Hewson et al. 2006) . On a global scale a latitudinal gra-
dient in species richness in marine bacterioplankton has
been found such that species' richness increases towards
the equator. as in some animal and plant groups (Pommier
et al. 2007, Fuhrman et al. 2008, see also Chapter 1) .
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
TECHNIQUES: Microbial community
studies: fingerprinting methods
In addition to obtai ning direct nucleic acid sequence
inform ation from oceanic samples (Marine Microbi al
Genomics, Current Focus), nat ural microbial commu-
nities are often studied with molecular methods called
w hol e-com munity fingerp rinting. These meth ods allow the
detection of org anisms present within an environmental
sample based on the differences found in the nucleotide
sequences of selected regions of genes. It is typical to
target conserved gene regions for mari ne bacteria, e.g.
riboso mal RNA gene or functional genes responsible for
the processes under study (e.g. genes encodi ng enzymes
in nitrogen cycle processes).
Nucleot ide sequence differences are visualized, pro-
ducing a unique 'fingerprint' for each sample. Visualiza-
t ion can be don e based on target frag ment nucleotide
sequence differences in differen t Operational Taxc-
nomic Unit (OTU) or by di rectly meas uring target DNA
Information on bacterial commun ity structure can be
used to understand basic patterns in microbial distribu-
tions, such as unique geog raph ical occurrence (endemism)
vs. global occurrence (cosmopolitanism), rarity vs. ubiquity
and dispersion patterns. Patterns of co-occurrence of spe-
cies helps to define potentially interacting organisms and
interaction networks that provide insights into a greater
understanding of ecological and biogeoche m ical processes
in oceans (Fuhrman 2009) .
Interactions between bacterial populations
As discussed later in this ch apter (3.5.4) , bacteria in normal
seawater concentrations occur on average 200 bacterial
body lengths apart (co rresponds to approximately 0.5 km
on a human scale) . It is natural to assume that interactions,
i.e. signalling or direct chemical attacks, between m arine
bacteria are important when bacterial densities exceed the
seawater concentrat ions, i.e , on marine snow particles
(Long & Azam 2001). Interactions between marine bacte -
rial populations include ant agonistic interactions (or alle-
Iopathy) and quorum sensing. Antagon istic interactions
refer to the prevention of the growth of anothe r bacterium
by the production of certa in bactericidal compounds. Such
frag ment length polymorp hism. Each detected unique tar-
get sequence in the fingerp rint represents an OTU that can
represent a strain, a species, a higher taxon, or functional
group of microbes, depending on the desi red reso lution
of the process. The most co mmon fingerp rinti ng meth ods
are Terminal Restriction Fragment Length Polymer-
phism (TRFLP). Denaturing Gel Gradient Electropho-
resis (DGGE) , and Automated Ribosomal Intergenic
Spacer Analysis (ARls A). These methods have different
sensitivity and can only give a partial pictu re of commu-
nity diversity. For example, ARISA can visualize organisms
that represent 0. 1% of the bacterial population but more
rare OTUs are ignored. This incomplete detection of diver-
sity is a common problem in all fields of ecology and can
be imputed using statistical methods (i.e. how many spe-
cies did we fail to find?). However, th e comparative study
of standardized fi ngerp rints provides valuable information
about co mmunity composition, changes in time or space
as well as the co-occu rrence of patterns of different spe-
cies (Fuhrman 2009).
antago nist ic abilities h ave been found to occur w idely
among marine bacteria and they are more common in parti-
cle-associated than free-living bacterial populations (Long
& Azam 2001 ). In particular, y-Proteobacteria are prolifi c
producers of inhibitory compounds (and also most resilient
to them), whereas Bacteroidetes are the least produc tive
and most vulnera ble to antagonistic interactions with other
bacteria (Long &Azam 2001) .
Bacteria can coordinate their gene expression by qu o-
rum se ns ing. For example, this occu rs when bacter ia
that have colon ized the same m arine snow particle (Box
3 .1) regu late, by leakin g a nd detectin g sign alling mol-
ecules, the timing of their production of costly extracel-
lular en zymes needed to solubilize marine snow particles
in to DOM (Gra m et a1. 2002) . There is a low likelihood
that a bacte ria ce ll would detect its ow n sign a lling
molecules and the cell thu s needs to detect m ole cules
secreted by other cells in the immediate vicin ity. Quorum
sensing allows single-celled bacteria to regulate their gene
expression, which ultimately benefits the individu al cells
by, for example, reducing the cost of extracellular en zyme
synthesis.
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

Box 3. 1: Marine snow plumes as oases
for marine heterotrophic bacteria
Marine snow particles, flakes, or accumulations of organic
matter (Fig. 3.9), are a major vehicle for transporting
organic matter from the ocean surface to depths and the
seafloor. A marine snow particle is colonized by bacteria
that produce extracellular enzymes converti ng POM to
DOM. Because bacteria produce DOM faster than they
can consume it, a sinking particle leaves a rich plume
of organic matter in its wake. Thus marine snow forms
an important source of organic matter in intermediate
depths. Many marine bacteria are motile and can actively
swim around instead of j ust passively floating in the water.
In addi tion, there is clear evidence that seawater bacteria
sense chemical gradients and are attracted towards nutri-
ent or organic molecules. Bacteria swimming in the water
surrou nding the DOM-rich marine snow plume could
therefore actively sense the DOM gradient at th e edge of
the plume when entering it and change their swimming
behaviour to stay in the plume.
Bacteria swim by rotary movemen t of a flagellum (or mul-
tiple flagellae), which are attached to the bacterial cell wall,
typically at the end of the cell. They can modify the flagellar
rotation speed and direction and thus regulate speed and
also direction of their movement to some extent. Flagellae
are left-handed corkscrew-like helices, so counterclockwise
rotation makes the flagellae move in synchrony and pushes
the cell forward . When a bacterium occasionally reverses
th e rotation to clockwise, the forward movement stops
and it starts 'tumbling'-staying in one place but chang-
ing its orientation. The occurrence of clockwise rotation
of a flagellum is suppressed by favourable low molecular
weight DOM molecules (e.g. amino acids) resulting in a
lower frequency of 't umbling', w hen the concentration of
these molecules increases. Bacteria then swim straight
when enteri ng and staying in the plume but start tumbling
when they are about to swim out of the plume and sense
decreasing concentration of favourable molecules.

•
•
( Fe

~ ( Phytoplankton
Ii
(
,-' ('
Fe '""Ill Source Phytoplankton
N(
~
particles delritus

~
Metazoa Bacteria

The marine snow particle colonized by bacteria, which turn particulate organic matter into DOM. Plume of excess
DOM trailing behind the particle as it sinks contains carbon (C) and mineral nutrients (N, Fe, Si). Free-living bacteria
(red) are attracted to the plume by their chemokinetic ability and grow rapidly. Particle colonizers may also release
their progeny (blue) into the plume. High concentrations of bacteria attract protozoa, which attract larger animals
(metazoa). Marine snow particles and their plumes may thus become focal points for the upper ocean microbial
food webs (illustration and figure caption from Azam & Long 2001).
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
The swimming speed of a bacterium , the time inter-
val between successive t urn s, and its chem ical sensit ivity
(ability to sense t he organ ic matter molecules) are traits
that cont ri bute to its chemokinetic behaviour. In addition,
the abi lity to effectively produ ce ext racell ular enzymes is
important for bacteria colonizing the part icles.
The study by Kiorboe and Jackson (200 1) is a theoreti-
cal modelling st udy in which a previously pub lished physi -
cal mod el of the flow and concentration fields around a
sinki ng part icle and a mod el of the chemokinetic behav-
io ur of bacteria are co mbined to pro duce est imates of
the o ptimal behaviour of bacteria col onizing marine snow
par ticle s and pl umes. In model simulat ions performed for
large and small marine snow particles separately, bacterial
swimmi ng characterist ics and chemosensory behaviour
were varied to define optimal values for bot h traits. In
colonizing and sol ubilizi ng a marine snow par ticle th ere
are t hree critical phases from th e bacteri al poi nt of view:
( 1) encounter wit h th e particle, (2 ) growth on the marine
snow particle and ectoenzym e pro duct ion to sol ub ilize
PO M into DO M, and (3) pl ume uti li zation for growth as
describ ed above.
In phase 1, the smallest possib le t umbling frequency
(0 .1 to 1 second betwee n tumblings) combi ned wi th high
chemical sensit ivity yi elds the best result for col oniza-
t ion. Once th e aggreg ate has been found , the bacteri a
need to prod uce ectoenzymes to sol ubil ize it into a usab le
form . Ectoenzyme produ ction is a costly process such
that bacteri a colonizi ng the same particle may be able to
keep the ectoenzyme pro duct ion at an opti mal level by
3.5.2 Viruses
Vir uses are submicroscopic biological entities of size about
20 to 200 nm (from 0 .00002 to 0.0002 mm) that replicate
by infecting cellular life and using the cellular machinery of
the host cell. They contain genetic material in the form of
RNA or DNA but are not organisms since they have no inde-
pendent metabolism or reproduction capacity. Although
not organ isms , they form an important functional gro up
as they are capable of infecting marine organ isms from
prokaryotes to whales (Fuhrman 1999; Suttle 2005) and
occur in very high numbers. There are typically ten billion
viruses in a millilitre of seawater, which makes viruses the
most abundant biological entities on Eart h, exceeding the
number of bacteria by an order of m agnitude. It has been
estimate d that there are several hundreds of thousands
of marine viral species, and diversity is highest in low lati-
tudes and decreases toward s the polar areas (Angly et al.
leaking sig nal molecu les th at influence prox imate bacte-
rial cells. In phase 3 only the fast-swimm ing bacteria are
able to remai n wit hin th e plumes of DOM. Once again, the
lowest po ssib le tumb ling frequency and high est chem ical
sensitiv ity lead to optimal pl ume uti lizati on. Overa ll , the
st udy suggests that chemo kinet ic behaviour can have a
significant effect o n bacterial growth in marine snow par-
ti cles and pl umes, and that opt imal tumb ling fre quency
and chemical sensitiv ity predicted by th e mode ls are pos-
sible, i.e. they co rrespond to previously reported values.
It is not known w hether the same spec ies colon ize
the particles and pl ume, wi th parti cle dwell ers releas-
in g the ir progeny into the pl ume (Azam & Long 200 1)
or w hether there are d ifferent spec ies that specialize in
living on particl es or wi thi n plumes . Optimal chemo ki-
net ic behavio ur can increase the growth rate of bacteria
in a pl ume by a factor of ten compared to a sit uati on
w it h an absence of chemo kinetic behavi our. Plumes are
favourab le for bacterial growth and are ubiquitous and
predictable enough to per mit co nstant colon ization and
utili zatio n by bacteri a. As not on ly the par ti cle itse lf but
also th e DOM -rich plum e can become colonized by bac-
teria, the marine snow pl umes are hot spots for bacterial
pro duction in the oceans and are responsib le for a large
part of the pro ducti on, even th o ugh they occ upy a minor
fraction of the w ater vol ume. Parti cle col onizat ion and
pl ume utili zatio n have conseq uences for carbon flow in
the upper ocean and beco me the focus of a compl ex
and partly independ ent food web (Box 3.1 fi gure; Azam
& Lo ng 200 1) .
2006; see Chapter 1 for sim ilar trends in other gro ups of
organisms) .
Viruses have an important regulating function w it h
respect to marine prokaryotes by infecting and killing them.
Viruses also have a significant influence on the fate of marine
primary and secondar y production. The importance of
viruses for the pelagic m arine ecosyste ms have been under-
stood for just the last 15 to 20 years and our knowledge on
viral diversity and the role of vir uses within marine microbial
food webs is accumulating at a rapid pace.
Most marine viruses contain DNA and probably infect
prokaryotes. Viruses that infect bacteria are called bacte-
riophages. In the surface oceans there are also very large
spherical (diameter from 130 to 200 nm) viruses that infect
phytoplankton cells. Viruses infect their host by finding spe-
cific receptors on the cell surface and then injecting their
DNA or RNA into the cell, where it takes control of the host
cellular machinery. Some viruses are very host-specific and
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

can only infect one particular strain or species, whereas
others seem to have a wider host range. It is possible that
each bacterial strain has at least one virus capable of infect-
ing it (Breitbart et al. 2008) . A key factor in infection is the
host-virus contact rate. which is a function of the amount
of host cells and viral particles in the water. It has been sug-
gested that viruses limit the abundance of bacterial species
that become dominant in the microbial community since
the viral infection rate increases as the concentration of host
cells increases. This is termed the 'kill-the-winner' hypoth-
esis and may be an important mechanism that controls both
prokaryote and algal populations.
Viruses are always dependent upon their host cells. This
means that it is necessary to isolate both the virus and the
host cell if they are to be srudied under laboratoryconditions.
Most prokaryote viral hosts have not been culrured, which
further complicates the study of viruses (see marine pro-
karyotes) . However. as for marine prokaryotes, viruses that
cannot be produced in the laboratory can be srudied using
culture independent-methods based on genes found exclu-
sively on viruses or environmental viral genomics . Viruses
typicallyhave genomes that are 40 times smallerthanmarine
prokaryotes, which makes it easier to study their genomes.
Viruses have different replication cycles, ofwhich the two
most important types are the lytic cycle and the lysogenic
or latent cycle (Fig. 3.16) . In the lytic cycle, viruses infect
cells. replicate, and release themselves into the environ-
ment through lysis of the host cell. In the lysogenic cycle,
viruses infect the cell and insert their genome into the host
genome, staying latent and replicating with the host until
some external factor (e.g. ultraviolet radiation) triggers the
lytic cycle (induction) . Viruses can remain in a dormant con-
dition for long periods of time until favourable conditions
activate the lytic cycle. Parts of the host genome can accom-
pany viral genetic material and can be subsequently trans-
ferred to another host organism and become inserted into
its genome. This feature makes viruses important vectors for
the lateral exchange of genetic material. i.e. from one organ-
ism species or strain to another. Ithas been suggested that in
highly productive waters (with a high abundance of hosts)

IVirus Ufe Cycles I

Virus attachment to host Virus encrhment to hcsr

ILysogenit I
• MTemperate"phage
•
Nucleic acid injected into host Virus nucleic acid injected

• Host with viral nucleic acid integrated into

•
~ genome or as extrachromosomal element II
Host makes copies of viral
\~_.......
I Normal division......-c---....
\
Host makes tuples of viral
nucleic acid and coat proteins nucleic acid and coat proteins

• II •
I
Normal division mnllnues unless induction occurs
\ I \ 1: II I
Viruses self-asscmble within host Host releeses progeny viruses without

• II
lysing· by budding or extrusion
I Normal \
di,ilion ---- ~

III I II I
H05llyses to release progeny viruses
---------
Host progeny continue to release viruses unless "cured"

Figure 3.16 Virus life cycles (illustration from Fuhrman 2000).

 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
the lytic cycle is dominant, whereas in low-productivity sys-
tems lysogeny is more prevalent (Weinbauer et al. 2003) . In
addition to the lytic and lysogenic cycles, a chronic life-cycle
is possible (Fig. 3.16), whereby an infected host cell and its
progeny constantly produce and release new viral particles
without completely lysing.
3.5.3 Protozoa
Protists are unicellular eukaryotes that can occur as indi-
vidual cells or colonies. They can be either auto- or hetero-
trophic. The autotrophic species include most eukaryotic
microscopic single-celled planktonic algae. Permanently
heterotrophic, non-pigmented motile protists are called
protozoa. Some species, especially flagellated algae, can
have both auto- and heterotrophic forms that are persis-
tent or change their mode of energy acquisition according
to the prevalent environmental conditions. Some species
are capable ofobtaining energy simultaneously from photo-
synthesis and through the use of organic compounds from
outside the cell, or by alternating between the auto- and
heterotrophic mode of nutrition. These species are termed
mixotrophs (See Chapter 2) . As neither the taxonomic
classification nor the size of protozoa determines their eco-
logical function, protozoa are classified here by the nature
of their food, although this will also reflect their size indi-
rectly. Protists can feed across several size-classes of food
particles and in some cases they can ingest prey that is
larger than themselves . Protitsts can typically reproduce
asexually by binary fission or sexually, when two cells
conjugate. The species concept in protists is based on the
morpho-species concept, whereby species are defined by
their morphological characters (Caron et al. 2009) . Pro-
tistan communities in the oceanic pelagic zones share the
same characteristics worldwide (Jurgens & Massana 2008) .
The diversity of protists seems to be very high, with thou-
sands of species anticipated even in a single group (Von
der Heyden & Cavalier-Smith 2005) . The genomic study of
eukaryotes is much more challenging than for prokaryotes
because of their larger genomes. For instance, the dinofla-
gellate genome size varies from 1 to 70 times the size of
the human genome (Hackettet al. 2004) . Despite the chal-
lenges, several marine protist genomes are currently being
sequenced (Caron et al. 2009).
Flagellated bacterivores comprise a very diverse range
of protists with representatives from all major protistan
lineages. They are collectively known as the heterotro-
phic nanoflagellates (HNF), and span a size range of 2
to 20 um. Flagellates are characterized by 1 to 4 flagellae
that are whip-like, motile, flexible organelles that consist
of microtubules. The flagellae serve multiple functions by
providing propulsion for movement and as a device to gen-
erate feeding currents (see below) or are used for sensing
the environment. Flagellates are the only grazers that can
survive on a pure diet of bacteria in the marine pelagic
zone (Jurgens & Massana 2008). They generate feeding
currents by undulating their flagellum and collect the prey
particles through contact with the flagellum or by using
filter structures.
Flagellates have specific adaptations to enable them to
operate in both a dilute and very viscous environment and
they can process 100 000 times their body volume ofwater
per hour (Boenigk & Arndt 2002) . Flagellate grazing is an
important limiting factor for bacterial production and is a
selective force in marine bacterial assemblages, as large-
sized bacteria are more vulnerable to grazing.
Protist microzooplankton characteristically fall into the
body-size range of 20 to 200 urn, They include major sub-
groups such as the ciliates and the larger dinoflagellates.
Ciliates are characterized by hair-like organelles called cilia,
which are identical in structure to a flagellum, but they
occur in largernumbers on the cell surface (Fig. 3.13) . Cili-
ates can be bacterivorous, herbivorous, predatory (preying
also on other ciliates), or mixotrophic (using chloroplasts
captured from algal prey to supply them photosynthetic
products) .
Large non-pigmented dinoflagellates are also an impor-
tant part of the microzooplankton. They are flagellated
cells that have two differentiated flagellae, one of which is
used for motility and another for grazing. Together ciliates
and large dinoflagellates are considered as the main preda-
tors of smaller phytoplankton in the oceanic pelagic zones.
Dinoflagellates have versatile feeding habits and can prey
upon significantly larger organisms by extending a pseudo-
pod (highly plastic membrane-like organ) around the prey
cell (Jacobson & Anderson 1986) . Although many dinofla-
gellates are covered by an armour of cellulose plates, they
are capable of extracellular feeding (Fig. 3.17) .
3.5.4 Metazoan zooplankton
Metazoan (multicellular) larval zooplankton include
crustaceans that are taxonomically very distinct from the
microzooplankton protists. However, the larval stages of
many metazoan plankton belong to the same size-class as
microzooplankton and are functionally similar (see also
Chapter 7) .
3.5.5 Algae
Organisms comprising the planktonic microscopic algae
(phytoplankton) have been presented in more detail
already in Chapter 2 . In the context of this chapter, the
categorization of algae is mainly presented in relation to
their function as a part of the microbial food web. Algae as
a functional group are taxonomically diverse, containing
both prokaryotic and eukaryotic organisms. Prokaryotic
autotrophic primary producers belong to cyanobacteria
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

Q b
o 30 50s

50~m

Figure 3.17 Image sequences on three species of heterotrophic armoured dinoflagellates feeding on diatom s (a and c)
and a small flagellate (b) by extending a pseudopod over them (modified from Jacobson &. Anderson 1986).

(also called blue-green algae) , and these can be either uni-
cellular, filamentous (Fig. 3.13) , or colon ial. In contrast,
eukaryotic algae are taxonomically and morphologically
more diverse (Chapter 2). All organisms grouped here into
algae are , however, autotrophic primary producers, and
produce new organic carbon from inorganic substances by
using light energy.
The size range of planktonic algae spans more than two
orders of magnitude from tum single-celled cyanobacterial
(picoplankton) to large diatoms (200 urn in diameter!). It
is in this size-range that the combination of fluid dynam-
ics and size has a cons ide rable bearing on the mechanisms
used to collect food. In the case of the smaller algae and pro-
karyotes, we enter a realm characterized by a value known
as Reynolds' number (Box 3.2), where the behaviour of
particles gives the impression that the water is very viscous;
although it is important to stress that this is in appearance
only, as it is a feature of their lack of momentum rather
than any change in the viscos ity of water. This means that
feeding mechanisms that rely upon straining or collecting
the particles by sweeping them into funnel-shaped gul-
lets simply do not work for algal fl agellates and bacteria;
whe reas for larger algae it is a very effect ive feeding mecha-
nism. Predators that operate at smaller scales typically rely
on the generation of feeding curre nts by fl agellar move-
ment (see above) .

Box 3.2: Life at low Reynolds'numbers5--'where our intuitions fail

The Reynol ds' number is a coeffic ient that gives us a scale that allows us to ant icipate how a moving organism will
exp erience the fluid physics of its envi ronment. It is calculated from the size of the organism, its rate of movement,
and a property known as the kinematic v iscos ity, w hich is the normal viscosity t imes the density of the fluid . We occupy
high Reynolds' numbers, e.g. 10 6 , whereas micro-organisms occupy low numbers, e.g. 10 -5 . Our everyday experi ence
gives us a poor understanding of the circumstances at low Reyno lds' number and our intu itions can be very misleading.
If we were to experience life at the scale of micro-organ isms we would be in for big surprises. Consider the basic
component of Reynolds' number- the kinematic viscosity. The kinematic viscosity of air is greater than water, thus it
means that a part icle the size of a bacterium falling through the atmosphere into the ocean would settle faster once
 3.5 Key organism groups in the oceanic microbial food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

it entered th e water, not slower as we would experience in our scale. At low Reynolds' numbers, the fluid gives the
appearance that it is highly viscous, and if we look at organisms under a high-powered microscope (when we enter the
world of low Reynolds' numbers) we can actually see this phenomenon. Scaled up to the human scale, the environment
has a viscosity somewh ere between molasses and tarm ac. In truth the viscosity is the same, but the organisms have
vi rtually no momentum. This lack of momentum means tha t w hen micro-organisms cease swimming, they stop almost
immediately; a bacterium coasts for 10 microseconds, only the length of a hydrog en bond (0. 1 nm). On our scale
such a deceleration would be lethal, many orders of magnitude worse than driving a Formula One car at full speed
into a concrete w all. These properties at small scales have a controlli ng influence on the mechanisms for the mot ility
and feeding of organisms living at these scales. A delightfully entertaini ng account of life at low Reynolds' numbers
is given by Purcell (1977).

3.5.6 How much do we find?

75

In Fig. 3.2, we produced profiles of biomass and activity

developed extensively from t heory. However theory can
--
0
0
~

=
only take us so far. Field observations of biomass and cal- -
0
c
culated surface area are broadly consistent with the theo- -
~
~

= 50
~
• Biomass
retical distribution given in Fig. 3 .2 (Fig. 3. 18 and Table
3.3) . The biomass profile shows that there is not a marked
-
0
E
0
• Surfote oreo

~
d ifference in biomass between the small and large forms, ~
c
and t he h igh biomass of phytoplankton is probably in part 0

an artefact as much of the sampling from which these com- -

0
~

0
~
25
pilations are derived, as have been made during t he bloom
period. The strikin g feature is t he span of surface areas, --
~
~
~
0

dominated by the bacteria (Table 3.3).

Figure 3.18 The typ ical di stributi on of surface area and

biomass of th e maj or planktoni c grouping s.

Table 3 .3 Typical values for abundance and biomass and su rface area of the major planktonic types.

Number Biomass Biomass Surface Surface

(per m 3 ) (mmol e /m 3 ) (%) area (m 2 /m 3 ) area (%)
Viruses C. 10 16
Bacteria C. 10 12 _ 10 13 1.5 16 1.00 73
Phytoplankton c. 10 8 _ 10 9 5.0 52 0.30 22
Bacterivorous c. 10 1O 1.0 10 0.05 4
protozoans
Herbivorous c. 10 6 0.2 2 0.01 1
protozoans
Larval zoopl ankton c. 10 5 0.3 3 0.005 0 .4
Adult zooplankton c. 10 3 1.5 16 0.01 1
9.5 1.37
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
3.5.7 Trophic structure of the oceanic
microbial food webs
We now need to put the pieces together. Fig. 3.19 summa-
rizes our current understanding of the major flows within
the oceanic microbial food web and provides a pictorial
summary of the statements in 3.5. This diagram can be
reorganized to give the twin source food chains developed
in 3.4.3. As the intensity of the various flows will vary with
the location and time of year. no attempt is made to gen-
eralize on them here; this will be done in 3.7. The relative
distribution of the biomasses is summarized in Table 3.3,
but again these figures vary spatially and temporally and
the numbers may only be taken as guides.
3.5.8 Spatial and phase distribution
Popular accounts of the plankton give the impression that a
drop of water is teeming with life. Without doubt there are
many thousands ofindividual organisms in a drop ofwater.
Bacteria are present in numbers of a million or more per
cubic centimetre. in other words they occur about 100 um
apart. Hence, if a drop of seawater is viewed under a high-
powered microscope, there is less than a 1 in 50 chance ofa
bacteria cell occurring in the field of view. For that reason.
bacteria and other micro-organisms most often are concen-
trated on fine filters and stained with fluorescent dyes for
microscopic examination.
Micro-organisms are certainly not homogenously dis-
persed though the water. The simple dichotomy of organic
material into 'dissolved' and 'particulate', as used in chemi-
cal analysis. is a poor representation of the reality in seawa-
Diatoms
'"
~
.~
S
-e-
~
o
~
o
Heterotrophic flagellates
:->. ~
Dissolved and particulate organic material
ter, where there is a continuum ofsizes oforganic material.
Microbes are found attached to living algae, where they
are thought to playa key role by 'pruning' mucus from the
surface of the algal cell thereby reducing its stickiness,
inhibiting aggregation and the consequent enhancement
of settling of the algae out of the illuminated part of the
ocean. Bacteria and other microbes colonize all forms of
detritus, including fragments of body parts and faecal pel-
lets. thereby facilitating their decomposition. Marine snow
(3.4.2) evidently is a rich habitat for micro-organisms ofall
types, including a range of bacteria, and autotrophic and
heterotrophic protists (Azam 1998; Azam & Long 2001;
Box 3.1) . The benefits and negative aspects of colonizing
particles are complex. The particle may provide a source
of organic material for microbial growth if the basic matrix
is organic. but less so if it is primarily an inorganic matrix;
for example, a diatom frustule . The physical chemistry of
adsorption leads us to expect that the availability oforganic
material will be lower in the vicinity ofa surface than in the
surrounding water (Box 3.3) . The potential disadvantages
of being attached to particles are very real: the presence
of the protist community will increase the threat due to
grazing by these forms; further, the large size and the rich
microbial community on marine snowflakes make them
choice food-items; these attached organisms are now avail-
able to metazoans, which would not have the capability to
feed on individual microbial cells. Finally, hitching a ride on
a rapidly sinking particle on its way to the cold organically
sparse ocean depths would not seem a strategy that benefits
the attached organisms.
-
f!;\------'
Figure 3.19 The trophic connections
within the microbial network.
 3.6 The dynamics of bacterial growth and its measurement
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Box 3.3: Adsorption and the
concept of activity
A common misunderstand ing is that as many sur-
faces adsorb organi c material, they are areas that
are favourab le for microb ial growth. However, an
understandi ng of the basi s of adsorption indicates
the opposite. The physical chemi st defi nes a prop-
erty 'a ctivity', which is the fraction of the molecu les
present that are reactive. It is only the active mol-
ecules that can engage in chemical and biochemical
reactions and set up diffu sion grad ients. Adsorption
occurs because the adsorb ing surface reduces the
activity of the absorbed mo lecu le below that in t he
bulk water. This sets up a diffusion gradient, w hich
decreases towards the surfac e (in contrast to the
concentrati on wh ich increases) . The consequence
of this is that material diffuses tow ards the surface,
hence the elevated concent rat ion at the surface (con-
centrati ons at surfaces however is a questi onable
concept) . Thus, the availab ility of the compound for
a micro-organ ism to assim ilate is less at the surface,
becau se its activity is lower than in the bulk medium.
This not ion w as resisted for some considerable tim e
but now it has been shown tha t bacteria grow more
slow ly on surfac es, which is consist ent with these
arguments. On the other hand, bacteria coloniz ing
marine snow par ti cles may be well-adapted to life
on particles (3.5. 2) and/ or gain benefit by releasing
their progeny in the blqh-Dofvl plume trailing behind
the particle (Box 3.1).
3.6 The dynamics of bacterial
growth and its measurement
The l /diameter rule (see 3. 2.1), developed from the sur-
face-to-volume relationship to account for the relationship
between metabolism and size , applies equally to microbial
growth and the consequence is that bacteria can have very
rapid growth rates. The record is a division every 10 min,
the norm for cultures is 20 min to an hour, and for natural
populat ions from one to a few days. Binary division gives
rise to exponential growt h : 1,2,4, 8,16, etc., thus growth
is literally explos ive. Simply expressed, the change in cell
numbers after 'n' divisions is 2 TI • The consequence of this
is impressive. An organ ism that divides at a rate of once
every 10 min, wo uld result in 24 x 60/ 10 = 144 divisions
after 24 h. Fro m an initial single cell, this would give rise
to 2 144 = 2.2 X 1043 cells. They would occupy a space of
1.S x 10 15 km", 1000 times the volume of the Earth ! One has
to be honest that the outco me of the calcula tion is highly
dependent upon the growth rates assumed and the time-
scale cons idered. Even in the case of more slow-growing
bacteria that occur in the sea, we would arrive at the same
position in less than a year.
3.6.1 The measurement of bacterial
growth and biomass
In a natural population , whe re organ isms are constantly
being grazed or eaten by predators, one cannot, as in a
culture, simply measure growth from an increase in num-
bers, i.e. changes in standing biomass; instead, growth rate
needs to be quantified . 'IWo of the most commonly used
approaches used to m easure bacterial growt h are pre-
sented in the following section.
Both methods are based on recording the uptake of radio-
actively labelled precursors of DNA or protein that exclu-
sively bacteria are able to take up from their environment.
Whe n heterotrophic bacteria are offe red the re ady-made
precursors at high enough concentrations (in the micromo-
lar range), they shut down their own precursor synthes is
and use only radioactively labelled precursors. By measur-
ing the uptake rate of these labelled precursors it is possible
to estimate the rate of bacterial production, i.e, the synthe-
sis of new bacterial biomass. The first method employs the
incorporation into DNA of ' H (tritium)-labelled thymi-
dine (a nucleotide; Fuhrm an &Azam 1980,1982). Labelled
thymidine is added to a seawater sample and incubated in
ambient conditions . Subseque nt to the incubation, which
can be as short as 30 min, the cells are lysed and the sample
is filtered through a fine filter (typically with a pore size
of 0.2 ~m) that retains radioacti vely labelled DNA synthe-
sized by the bacteria during the incubation. The amount of
radioactivity in the filter is then measured by scintillat ion
counting. Information from the radioacti vity retained on
the filter (assum ing that the incubation time and volume
are known) provides a rate of incorporation of thymidine
into DNA. As thymidine represents close to 25% of the bases
in DNA, it is a very simple matter to calculate the qu antity
of DNA produced. Given the assumption over the total DNA
content of a single bacterial cell and the mass of the cell, one
can calculate the rate of formation of new bacterial biomass.
Nevert he less, it is important to note that the validity of the
technique is intimately linked to the validity of the assump-
tions, which often need to be verified for new environments
with separate methodological testing.
The second approach follows the incorporation of 3H_
or He-labelled leucine (am ino acid) into protein (Kirch-
m an et aJ. 19 85). The basic approach is much the same:
the calculation in this case requires knowledge of the ratio
between cell biomass and its leucine content (or the per-
centage ofleucine in proteins and the percentage protein in
the cell) . Again the uncertainties in these assumptions limit
the accuracy of the techniques. The two techniques measure
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material
fundamentally diffe re nt properties: the [3H]-thymi dine
technique is associated with the rate of cell productio n, the
leucine technique with the rate of biomass produc tio n. Any
attempt to compare the two methods requires an accurate
knowledge of the biomass of a single bacterial cell, which
in a n atural population is an extre mely difficult property to
determine (Duc klow 2000) .
The biomass of marine bacteria and ot her microbes can
be estimated using a host of methods that can be di vided
into three categories. Most often cell-counting methods are
used where microbial cells are directly counted and their
biovolume measured eit her by epifl uoresce nce microscopy
(e.g. Hobbie et al. 1977) or, increasingly, by flow cytometry.
Biovolume or cell numbers can be transformed to carbon
values by suitable empirical correction factors. Direct mea-
surement of microbial carbon can be done by removing
larger organ isms and ot her particles by pre-filtration and
then collecting microbial cells on fine filters (again typi-
cally 0.2 - ~m pore-sized filters are used) for direct carbon
analysis. A third alternative is to use a proxy for microbial
biomass. Proxies can be che mical (e .g. the concentration of
bacterial cell wall compone nts or fatty acids) or molecular
(e .g. number of 165 rRNA genes), which then can be trans-
lated to biomass with known correction factors.
Table 3.4 conta ins a summary of data for bacterial bio-
mass, produc tio n, and growth rates in the euphotic zone of
the major zones of the oceans, along with comparable d ata
for the phytoplankton. At low latitudes, bacterial and algal
biomasses are comparable; but in cold waters, the bacterial
biomass may dominate. This m ay represent a community
shift to compensate for reduced rates of bacterial metabo-
lism at low temperatures. Cons istent with this, in the warm
water of low latitudes, bacteria grow much faster than the
phytoplankton. The production rates draw attention to a
major contemporary problem in biological oceanography:
Table 3.4 Bacterial and phytoplankton production and growth rates in the euphotic zone of various oceanic
areas (recalculated from Ducklow, 2000).
Equatorial
Zone
Euphotic zone depth (m) 1 20
Average biomass (as mg C m-3 )
Phytoplankton 11
Bacteria
Average production rate (mg C m- 3 d:')
Phytop lankton
Bacteria 11
Average grawth rate (d")
Phytop lankton 0 .1
Bacteria 0 .7
balancing the books. As a consequence of recycling (3.4.3),
organic material can pass through the bacteria more than
once, so in principle bacterial production can exceed pri-
mary production ; this can only occur to a limited extent
and the heterotrophic processes in the water column can-
not exceed production by large amounts. However, whe n
attempts a re m ade to produce a budget for the oceans, most
frequently we end up w it h a presently unexplained deficit
of organic material (see also 3.7). This is curre ntly a m atter
of active debate and without doubt there are some issues
related to the errors related to temporal and spatial averag-
ing, as well as questions over the accuracy of the methods
for measuring both photosynthetic and heterotrophic rates
of production.
3.6.2 Food web dynamics and growth
control in oceanic microbial food webs
Given the potential for explosive growth, changes in bacte-
rial numbers through the seasons are surprisingly muted
(Fig. 3.20) . In the case of bacteria, three m ajor factors con-
strain bacterial growth in the oceanic water column: (1 )
control by flagellate or ciliate grazing, (2) resource limita-
tion, and (3) viral mortality. In the following, the major
growth-regulating mechanisms, which apply not only for
bacteria but throughout the ocean ic m icrobial food webs
in the oceans , are discussed.
Grazing and viral mortality: top-down control
Bacteria are grazed by small protozoa, in particular hetero-
trophic nanoflagellates (HNF) . The grazing control on prey
populations (e.g. bacteria) is termed top-down control, as
predators (that are higher in graz ing chains) control the
abundance of their prey (McQueen et al. 1989 ; Thingstad
2000). Top-down control also includes the effects of para-
Subtropical Temperate Polar (Ross
Gyre (N. Atlantic) Sea)
14 0 50 45
2 20 5
9 4 90 2 54
2 1 6 0
3 22 28
0 .1 0.3 0 .3
0 .8 0 .3 0 .1
 3.6 The dynamics of bacterial growth and its measurement
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

20
to select the larger bacterial cells preferentially, so the size
~
Flagellate distribution of the bacterial population, when it is grazed.
e
~

-
-;;
~
I5
Bacteria is shifted down from a modal diameter of 0 .75 to 0.5 I'm,
resulting in a threefold reduction in cell volume from 0.22
'"
=
-- to 0.065 I'm' .
~

c
"
-;;
= I0
Bacteria do also have mechanisms to escape size-
=-
c /\ selective grazing. e.g. miniaturization of cells and colony
.--.,
c
I~ formation. Marine viruses occur at abundances of about

.~
-• 5
IJV \1\
c
.lI
0
/ W\i1
160
120 140 180 7110
Day of the year
2211
'"
Figure 3.20 Seasonal changes in the abundance of
bacteria and heterotrophic nanoflagellates in a shallow
marine fjord. Redrawn from Strom (2000), original
material from Anderson and Sorensen (1986).
sites and viruses that are other major sources of mortality.
The dynamics between the bacteria-protozoan predator-
prey relationship and that of the phytoplankton-meso-
zooplankton coupling are different and a critical factor in
the determination of the dynamics of the various plank-
ton communities. In the latter case. the growth rates are
very different; the zooplankton reproductive rate is about
tenfold slower than that of phytoplankton. This mismatch
allows the phytoplankton to bloom before their predators
can increase in numbers or size sufficient to graze down
the bloom. In the case of the bacteria-protozoan coupling,
their growth rates are more comparable (a pproximately a
day) so the bacteria have no opportunity to bloom, at least
for any extended period, as their increase in abundance is
quickly followed by an increase in the numbers of the pro-
tozoans. The latter graze down the bacteria again. giving
rise to Latka-Volterra limit cycle oscillations (Fig. 3.20) .
Abundance or biomass control caused by predation or
virus mortal ity is termed top-down control.
As an extension to one-level oscillation (with two func-
tional groups involved), trophic cascades are typical in
planktonic microbial food webs. In a trophic cascade a
predator (e .g. zooplankton) suppresses the abundance of
its prey (ciliates) and thereby releases predation pressure
on the next lower level (flagellates), increasing its abun-
dance and further suppressing their prey (b acteria). The
top-down effects that are mediated in trophic cascades are
complex and explain how. for example. increase in zoo-
plankton abundance can lower the abundance of bacteria.
There is a secondary feature of the control by grazing that is
related to prey-size selection. The protozoan predators tend
10 7 crrr-', i.e, about 10 viruses for every bacterial cell. and
kill and infect bacteria (3.5.3) . We have a great deal to learn
J of the impact ofviruses on marine biota: it is estimated that
V"" they may account for 5 to 40% of the mortality of bacteria.
,OJ
' 60
Resource limitation: bottom-up control
Another important cate gory of bacterial abundance-
controlling factors are related to resource availability. i.e .
growth, and are termed bottom-up control. because they
are defined by factors lower in the food chains (Thingstad
2000) . The seas are an organically dilute environment.
Characteristically. the concentration of individual mol-
ecules is in the region of 10-7 molar (10 grains of sugar per
ton of seawater would give a similar concentration) . Also
availability of inorganic nutrients (N. P) or trace elements
can be limiting bacterial growth in the upper ocean. This
dilute environment constrains both the rate and extent
of bacterial growth. Resource limitation is governed by
the law of minimum (discovered by the famous German
chemist Justus von Liebig (1842) and hence is known as
Liebig's law of the minimum), stating that availability of
the scarcest resource limits the abundance or standing
biomass of an organism (see also Hiddink & Kaiser 2005) .
Typical biomass-limiting factors in ocean pelagic zones can
be considered to be nutrients (nitrogen). or trace elements
(e.g . iron) for planktonic algae. and organic carbon com-
pounds or phosphorus for heterotrophic bacteria. Another
type of limitation is termed Blackman limitation (named
after British plant physiologist F.F. Blackman (1905), who
discovered the two-step nature of the photosynthesis),
where resource limits population growth or metabolism
rate, instead of directly limiting standing biomass. Black-
man limitation can be light for phytoplankton or the type
or relative lability ofavailable organic matter for heterotro-
phic bacteria (3.4.3) . Specific limitation type or substrate
characterization for marine microbes in oceanic environ-
ments is complex and difficult. Multiple co-limiting fac-
tors. both of the major limitation types specified above
and complex physiological or species-specific limitation
patterns. can act simultaneously in a microbial community
in the sea (Arrigo 2005) . Bottom-up or resource control
can thus manifest itself, e.g, through shortage of chemical
substrates (pa M/Da M for heterotrophic bacteria) or also
shortage of prey organism for a predator. Bottom-up control
might be expected to lead to competition between bacte-
ria for the same limiting resources, leading to changes in
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

bacterial community composition. In addition to top-down
and bottom-up controls on bacterial populations, a third
type-'sid eways' control-can be postulated (Fuhrman &
Hagstrom 2008) . Sideways control refers to resource com-
petition between bacterial populations and the active nega-
tive effects they can direct towards each other (allelopathy,
see 3.5.1) .
Resource limitation, meaning shortage of an essential
growth factors limiting growth rate or standing biomass
of an organism , is termed bottom-up control and is gov-
erned by the Law of the Minimum or Blackman limitation .
acteristic situations seen elsewhere in the surface oceans.
Seasonal changes of solar angle and subsequent changes in
amount of solar energy entering the oceans are especially
important in temperate areas, just because of the thermal
stratification patterns they evoke in the upper water-col-
umn. Another important role in the seasonal production
cycle is in direct light-limitation on phytoplankton growth.
In the following we shortly go through the seasonal temper-
ate stratification and phytoplankton productivity patterns,
also depicted in Fig. 3.21, which are then elaborated more
in the paragraphs from 3.7.1 to 3.7.4.
The thermocline is the boundary between dense, cooler
bottom water and warmer, less dense surface water.

3.7 The seasonal cycle of • Winter: The sun is low in the sky, days are short, and
production and consumption due to low solar angle much of the radiation energy is
reflected from the ocean surface. Winds tend to mix
We now have all the pieces in place to look at the dyoam- surface waters deep into the water column. With no
ics of the microbial food webs in the context of seasonal thermocline, the water column is fully mixed (isot h er-
and larger biogeochemical cycles and terms of matter and mal) and the inorganic nutrients are evenly distributed
energy flow. In this and the following section we consider throughout the water column. Although phytoplank-
the seasonal changes in a temperate marine ecosystem and ton are present throughout the water they do not grow
explore the changes that occur with time and in space. The because short days and the low angle of the sun mean
seasonal cycle of temperate waters, in which seasonal ther- that light levels are too low to support high rates of pho-
mal stratification of the water column takes place, gives the tosyothesis and growth.
best example to consider as it encompasses most of the char-
• Spring: In spring the sun is higher in the sky and day
Phuse IV (<0,1.) Ph", I jhese II Phose III Phase IV length increases. This results in more solar energy
0
0
0 0
0
0
0
absorption by the water and the development of a ther-
nof:° <,
0
0

\: 0
,
0
- Nutrient5
- Phytoplonkton
mocline, which effectively traps phytoplankton in the
surface waters. If the mixed layer depth is shallower than
, 0 - Zooplankton
0

- 0 anit detritu the critical depth (see Chapter 2), phytoplankton will
0
0 , 0

0
0
/,, :--.. bloom, since there are abundant nutrients and adequate
0 0

0 , 0 0
0
light to support maximal growth rates. This is termed
,,
0 0 0
0
0
0
0
new production.
0
0 , 0 0
0
• Summer: The sun is high in the sky and day length is
0 0 0
0 0 0

:; long. This results in the surface waters warming even

Jon
\..
Feb Mar Apr Moy Jon
0

i' " lui Aug Sept Oct Nov Dec

o
o o
1 phosphate) phytoplankton growth ceases, despite the
Winter Spring Summer
Figure 3.21 The relative seasonal fluctuations of
inorganic nitrogen, phytoplankton , zooplankton , and
organic detritus (dissolved and particulate organic
material) in temperate waters in relation to the seasonal
thermal stratification of the water column . The phases (1-
IV) are described in the text.
more and the development of a strong thermocline that
prevents any mixing between the surface and waters
below the thermocline. Once the nutrients in the sur-
face waters have been used up (typically nitrate and/or
fact that light conditions are good enough for maximum
photosyothetic rates to take place. Some growth will
continue based on regenerated nutrients. This is termed
Autumn Winter recycled production.
• Autumn: The sun is lower in the sky and day length
shortens. The surface waters begin to cool again and
autumn winds tend to mix surface waters deeper lead-
ing to a breakdown in the thermocline. This results in
nutrients from deeper waters mixing above the thermo-
cline and this supports an autumn bloom of phytoplank-
ton while light levels are still high enough to support
 3.7 The seasonal cycle of production and consumption
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
photosynthesis. The autumn bloom is not as great as
the spring bloom, because of lower light levels and also
because concentrations ofnutrients are not as great as at
the beginning ofspring. This is termed new production.
The depletion of nutrients in surface-mixed water layers
results in the establishment of a nutricline between the
surface waters and deeper water: a gradient of low to high
nutrients with increasing depth. There is therefore a poten-
tial flux of nutrients from below to above, and the maxi-
mum flux will be in the region of the nutracline.
This biological cycle of seasons is embedded in the over-
all biogeochemical cycle, introduced in Chapter 2 is shown
again in Fig. 3 .22 . The cycle involves a throughput of
energy, entering as visible radiation and departing as heat
in the form oflong-wave radiation. and a cycle ofnutrients.
Thus. whereas an atom of say C. N. or P can cycle round
indefinitely. perhaps a number of times in one season (the
reciprocal of thef-ratio, see 2.8.3, gives the number of times
a nitrogen atom is cycled per year). energy passes through
the system once only, to be lost eventually as heat to outer
space. Although all energy eventually passes through the
system and elements are recycled, both can be also stored
in the seafloor for geological times (e.g. in fossil fuels), re-
entering the biosphere through geological processes or dur-
ing the short industrial history also by human actions.
As we treat a cycle of production and consumption here,
we could begin anywhere, but it is logical to begin at the
point of photosynthetic formation of organic material,
where solar energy is directly transformed into chemi-
cal energy. This event, and the circumstances initiating
it. is discussed in Chapter 2. The photosynthetic process
involves the absorption oflight and the splitting ofwater to
provide the reductants (a proton and an electron) needed
for the reduction of carbon dioxide. The reductants are also
used to reduce nitrate to ammonium, prior to their incor-
Photosynthesis
Ught
(visible
radiationj
Heat (infrared
radiation)
IFlow of energy I - - - IFlow of material I
poration into organic molecules as amino acids. About 20
to 25% of the energy used in photosynthesis can be spent
on reducing nitrate to ammonium; small amounts are also
used for the reduction of sulphate and other minor ele-
ments . Oxygen is appropriately viewed as a toxic waste
product of the photosynthetic reaction. Phosphate is also
incorporated into organic material at this stage, but unlike
C, N. and S there is no change in the oxidation state and for
this reason it is not included in Fig. 3.22.
Some of the formed organic material will be used to fuel
algal respiration, but by far the major part will pass into,
and cycle round, the food web (Fig. 3 .19) . As it flows and
cycles through the food web, it is respired. The principal
respiration products are carbon dioxide, water, and ammo-
nium. To complete the cycle. the ammonium needs to be
oxidized back to nitrate by the nitrifying bacteria (the lower
right-hand quadrant in Fig. 3.22). However, this does not
automatically occur for there is a short circuit. as the algae
may use ammonium; indeed. for energetic reasons they use
it in preference to nitrate. This gives a cycle (the two upper
quadrants in Fig. 3.22) within the overall cycle. As we shall
see. the flows through the four quadrants vary in intensity
through the season.
The broad temporal sequence of events in the seasonal
cycle of the plankton is shown in Fig. 3.21 and the primary
driving forces are discussed in Chapter 2. It is convenient to
consider the seasonal events as four phases:
Phase I- the initial development of the spring phytoplank-
ton bloom.
Phase II- the demise of the phytoplankton bloom.
Phase III- a mid-summer recycling phase.
Phase IV- the regenerative period, lasting until the bloom
the following spring.
Figure 3.22 A simple schematic of the
principal reactants of the photosynthesis-
respiration cycle. The broad, multicoloured
arrow depicts the flow of energy through
the system , entering as short-wavelength,
high-energy, visible radiation , and leaving as
long-wavelength, low-energy heat or infrared
radiation . The cycles of elements are shown
in the middle. The cycle of nitrogen shows
the intermediate production of ammonium
and the short-circuiting of the nitrogen
part of the cycle. The left-hand sector of
the diagram represents the photosynthetic
process, the right respiration. The food web
interactions are not shown. (To simplify the
diagram nitrate (NOJ and ammonium are not
shown in their charged form .)
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

This sequence ignores the autumn bloom. This is done for
the sake of simplicity, the autumn bloom can be considered
as a brief rerun of Phases I and II. The relative flows over
the seasons of the various biological and chemical pools are
shown as a mandala in Fig. 3.23.
3 .7.1 Phase I:the initiation and growth
of the phytoplankton bloom
The warming ofthe upper water-column. the development
of the thermocline, and the consequent shallowing of the
mixed layer, along w ith the concomitant deepening of the
compensation and therefore the critical depth, trigger the
initiation of the phytoplankton bloom. This results in an
initially uncontrolled burst of algal growth (Figs 3.23a
and 3.21) . The bloom is characteristically dominated by
diatoms, as the high levels of nutrients present favour
their growth. Their predators, traditionally thought to be
the calanoid copepods, do not have the metabolic capac-
ity to respond to the banquet offered to them; hence the
bloom initially is uncontro lled. There will be, as a con-
sequence of the algal growth, some release of dissolved

(a) (b)
Phase I:Spring bloom development Phase II:Spring bloom demise
t
/ <, /' / <, / <,
Diatoms Iepepeds Diotoms Iepepeds
<, / -, / <,
.••.-- _
/ .r-,
AutotrophIC: _
/'
I I

Gliates
-••-=
.••-= Autotrophic~
/. /
t
, Illictes
.= = f1agellales :/ flagellales
= = y
c
=
c-= 1 -r-J 1
=
c
c
-= , /'
/" t
- 'erotrop~i( _ ',erolrophiC }_ - , ~.,
eterotrop I(
, 'terotrophic
- ,,-bacteria> ~agellales -, bacte~ia y ~agellal"

II I
Dissolved and particulate Dissolved and particulate
organic material orgonic materiol

(d)
t
Phase IV:Autumn/winter regeneration period
(eJ
Phase III: Mid-summer re-cyt:ling period
I t
/ <, <, /' -, / <,
~

<,
Diatoms
./
~ Icpepcds - -,
Diatoms
/' <,
Iepepeds
./
,
-.=-•= , t
--•= t
-== 'A'ulalroph >- /'
-=='0
"A'ulalroph0
/ <,

c
=
-= ~agellate5
, >--
Ciliates
.... -= =
c
~agellate:,;
/"
OIiates

•= /Heteretrcchk
:.x
, j •= /. '
I
~lerotrophiC ~
,:,< / /
Heterotrop~i(
, Heterotrophic
-, barte~io flagellates -, bacte!ia ~agellate5
, >
I
Dissolved and particulate Dissolved and particulate
organic material organic material

~
Dominant flow
__
I Signifi(ant flow
-_. Minor flow
Insignifimnt flow

Figure 3.23 The variations in the flows of material throug h the microbial network shown in Figure 3.19 through the
four phases of the year shown in Figure 3.22. The width of the arrows indicates the intensity of the flow.
 3.7 The seasonal cycle of production and consumption
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
organic detritus and some particulate detritus as a con-
sequence of zooplankton activities. This will result in an
increase of the pool of non-living organic matter and con-
sequent bacterial growth. In this phase, the autotrophic
phase, the left-hand quadrants of Fig. 3.22 dominate (see
Fig. 3.25a) . As a result of the assimilation of the organic
matter released by the algae. the flow of organic material
through the microbial sector of the food web increases.
Through this phase, the major part of the respiration is
associated with the algae; that associated with the het-
erotrophic population is minor. This is a period of positive
net community production, as depicted in Fig. 3 .24. The
algal growth results in a drawdown of the pool of inor-
ganic nutrients and this. coupled with the consequential
growth of the zooplankton, eventually results in a slowing
down of the rate of phytoplankton growth leading onto to
the next phase.
3.7.2 Phase II: the demise of the spring
bloom
The combination of the events above results in the demise
of the spring bloom and a progressive growth of the het-
erotrophic parts of the community, especially the microbial
sector. the bacteria, the heterotrophic nanoflagellates, and
the microzooplankton (see Fig. 3 .25b) . There is, during
this period, a change in the balance between production
and respiration, and a consequent fall in net community
production, becoming negative on occasions (Fig. 3.24) .
Importantly there is a downward shift in size of the primary
producers from the diatoms to the autotrophic flagellates.
This is driven in part by selective grazing of the larger forms
by the zooplankton, but more importantly by the fall in
nutrient concentration. The smaller-sized algae have a nar-
rower diffusion boundary layer (see 2.7.2) and so are able
to out-compete the diatoms for nutrients when the concen-
trations are low. This drives the whole centre of metabo-
lism downwards in size (Fig. 3.25b) and so the growth in
emphasis of the microbial network. In many respects this
is a transitional phase leading to the establishment of the
next phase.
As a result of the assimilation of the organic matter
released by the spring bloom algae the flow of organic
material through the microbial compartment of the food
web increases in spring.
3.7.3 Phase III: the mid-summer
recycling period
As the nutrients fall in concentration and the recycled
nutrients become more important. we enter a phase ofvery
closely coupled metabolism and a food web tightly con-
Phose IV(<ont.) Phose I Phose II Phose III Phose IV
Photosyntflesis
1- - Respiration
1- - Nel mmrnunits production
.e
e
Jon Feb Mor Ajlr May Jun Jul Aug Sep Od Noy Dec
Figure 3.24 The distribution of respiration and
photosynthesis rates through the season. Also shown
is net community production (the difference between
photosynthesis and respiration).
trolled by grazing. The reason for this is that the organisms
that now constitute the main hub of metabolism all have
comparable growth rates and so. as one group increases in
abundance. so its predator responds by increased grazing
and its abundance increases. Eventually the prey becomes
diminished and so the grazing activity ofits predator is cur-
tailed. There are two further layers ofinteraction. First. the
growth of the predator gives rise to an increase of its own
predator and so its own demise. To give a concrete example:
the increase in abundance of the bacteria will give rise to
an increase in the abundance of the heterotrophic nano-
flagellates, which pin down the bacteria. The subsequent
increase in the nanoflagellates gives rise to an increase in
the microzooplankton, which will graze down the nano-
flagellates, releasing the control on the bacteria (a trophic
cascade; 3.6.2), which then can flourish a second time. This
gives rise to the sort of perturbations seen in Fig. 3.20.
As the nutrients fall in concentration and the recycled
nutrients become more important in summer we enter
a phase of very closely coupled metabolism and a food
web t ightly controlled by grazing.
The second form ofinteraction derives from the fact that
much of the organic detritus the bacteria use (e.g. muci-
lage) is nitrogen-deficient and therefore nutritionally poor.
Bacteria, however, have the facility to assimilate inorganic
nitrogen and incorporate it into organic material. thereby
making up this deficiency and enriching the food quality.
This gives rise to a further level of control. As the bacte-
ria compete with the autotrophic flagellates for inorganic
nitrogen, these in turn are controlled by the microzoo-
plankton. Thus, the development of the microzooplankton
can favour the bacteria in two ways as the microzooplank-
ton predate on the two groups of organisms that control
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

bacterial growth: the autotrophic flagellates (a) Autotrophic phase

(that compete with them for inorganic nitro-

Photosynthesis Respiration
gen) and the heterotrophic nanoflagellates
(that graze upon them) . The system is locked
in a rather loose equilibrium and will tend to
Light
meander (as in Fig. 3.20) from one state to {visible
the other. There will be a tendency to swing radialion)
from a net autotrophic state to a net hetero- :@ - ~.........
---_.
trophic one, thus NCP will shift from positive
Heal (infrared
to negative.
radialion)
The system, shown as the upper fWO quad-
rants in Fig. 3.25b, is self-sustaining and in
principle could cycle and oscillate in this man-
ner indefinitely. It is in fact the basic structure IFlow of energy I - - _ . IFlowof materiall
of many low latitude oligotrophic plank-
tonic communities. This is a stable situation
and will persist until some external force (Ii) Re<y<ling phase
disturbs it sufficiently to break down the con-
trols (see also alternative stable states and Photosynthesis Respiration
phase shifts in Chapter 8) . Part of this stabil-
ity derives from the recycling of ammonium.
Light
There is a three-way competition for
(visible
ammonium in the plankton as the plank- radialion)
tonic autotrophs, the heterotrophic bacteria,
and the nitrifying bacteria all compete with
~ ---_ . ......
one another for ammonium. The competition Heal (infrared
radialion)
between the bacteria and the autotrophs is
part of the self-sustaining mechanism; how-
ever, the nitrifiers will produce nitrate and
its production would move the system out of IFlow of energy I - - _ . IFlowof materiall
this state. The growth of the nitrifying bacte-
ria is inhibited by light, whereas that of the
photo-autotrophs is of course light-depen- (e) Heterotrophic phase
dent, and thus light may provide the basis
of the switch. In the mid-summer period, I Photosynthesis Respiration
when the sun is high. the nitrifiers compete
poorly against the microalgae for ammo-
nium (the short circuit in Fig. 3.25b) . As the Light
autumn period is entered and the sun angle (visible
radialion)
decreases. the balance between the nitrifiers
and the algae shifts in favour of the nitrifiers, ~ ---_ . ......
and the ammonium produced by the micro- Heal (infrared
heterotrophs is not recycled but converted to radialion)
nitrate. Nitrate has to be reduced first before
it can be incorporated into organic material.
as this is an energy-consuming reaction it is a
less satisfactory nitrogen source for the bac-
IFlow of energy I - - _ . IFlowof materiall

teria and to a large extent also the algae. This

is probably one of a number of mechanisms
that jerk the community out of its tightly
coupled structure. Another will be the break-
down of the thermocline and the formation
of the autumn bloom, essentially a re-run of
Phase I. When the autumn bloom wanes, the
Figure 3.25 Figure 3.22 redrawn to show the changes in the dominant
flows during three phases of the year: the autotrophic phase (Phase I),
the recycling phase (Phase fII), and the regeneration phase (Phase IV).
Phase 11 is not depicted as it is transitional between Phases J and III.
 3.8 Oceanic microbes in global carbon and nutrient cycles
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
circumstances may no longer favour the re-establishment
of the structure seen in mid-summer. Thus, for a number of
reasons the planktonic community enters the last phase of
the seasonal cycle : the heterotrophic phase of regeneration.
3.7.4 Phase IV: the final regeneration
of nutrients
Whereas, as one enters the autumn period, phytoplankton
activity decreases, the particulate and especially the dis-
solved organic detritus, left as a result of their growth. per-
sists and is a source of food for the microbial heterotrophic
community. Phosphate regeneration is essentially a one-
step process as it is produced in its final form by respiration.
As we have seen, the case of nitrogen is more complex,
as ammonium, the immediate product of respiration. in
the presence of oxygen is a potential source of energy that
the nitrifiers can utilize. The conversion back to nitrate is
a two-step process (see the lower third of Table 2.2), car-
ried out by two different types of nitrifying bacteria and the
intermediate, nitrite. shows a temporary rise in concentra-
tion in the autumn period prior to its conversion to nitrate.
Slowly, through the late autumn and the winter period, the
heterotrophs use up the detrital material and regenerate
the nutrients. eventually reinstating the circumstances
that existed at the onset of the spring bloom.
Throug h the late autumn and the winter period, the het-
erotrophs use up the detrital material and regenerate
the nut rients.
This (the upper and lower right-hand quadrants in Fig.
3 .25c) is a period of predominant heterotrophy and a sus-
tained period of negative net community production (Fig.
3 .24) . Thus, by the time winter gives place to spring, the
great cycle of the plankton is complete and ready to start
again.
During the summer recycling period the system is self-
sustaining and in principle could oscillate in this manner
indefinitely.
3.8 Oceanic microbes in
global carbon and nutrient
cycles
Oceanic microbes playa central role in the global carbon
cycle and subsequently climate regulation. Approximately
half of the daily photosynthetic production of organic mat-
ter on Earth takes place in the upper 100 m of the marine
environment, exclusively produced by marine microbes
(Bowler et at. 2009) . The distribution of carbon in the sea is
governed by two fundamentally distinct processes (termed
'pumps') that have independent controls (Fig. 3.26) . The
solubility carbon pump, which transports mostly dissolved
inorganic carbon, is controlled by CO, dissolubility and
large-scale ocean circulation. The other is the biological
carbon pump that is driven by microbial production and
consumption of organic matter and is currently not well
understood (Bowler et at. 2009) . The biological transfer of
particulate carbon from near surface habitats, where it is
produced by primary producers, to great depths, where the
majority ofdecomposition takes place (Chapter 2), sustains
the CO, depth profile in the open oceans with highest con-
centrations below 1000 m depth (Chisholm 2001; Bowleret
a1. 2009) . Microbial processes in the ocean thus sequester
carbon from the atmosphere and store it in the deep sea over
time-scales that range from centuries to millennia. As phy-
toplankton production is an important driver of the biologi-
cal pump, it has been suggested that by releasing prevalent
iron limitation (3.6.2) in parts of the world ocean, carbon
sequestration into the deep ocean water layers would
increase. helping to combat increasing atmospheric CO2 ,
Functioning of oceanic microbial food webs powering the
biological carbon pump are currently not well understood
and large-scale fertilization could lead to unprecedented
side effects such as deoxygenating the deep ocean and the
generation of greenhouse gases that are more potent than
CO, (Chisholm 2001) .
Because of their central role in global primary produc-
tivity. as well as their capacity for rapid growth, marine
microbes are a major component of global nutrient cycles.
In the nitrogen cycle marine microbes also mediate complex
biogeochemical processes, such as nitrogen fixation from
atmospheric N2, nitrification, and denitrification (microbial
conversion of nitrates into N2 gas). Global biogeochemical
cycles of elements have been shaped by the forces of evolu-
tion over geological time-scales and they are important fac-
tors in the functioning ofthe Earth System (Chisholm 2001) .
Marine microbes can modulate the coupling between the
cycles of nutrient and carbon on global scales (Arrigo 2005) .
Microbial oceanography is a relatively new scientific dis-
cipline that focuses on the ocean as a habitat for the evolu-
tion and regulation of microbial-based processes and their
ecological consequences. It combines observation, experi-
mentation, and models. and strives to integrate the prin-
ciples of several otherwise unrelated disciplines (Bowler et
at. 2009) . Microbial oceanography bears great promises for
improved understanding of the Earth System but is also con-
fronted by great challenges, including development of sam-
pling strategies for the highly dynamic and complex habitat,
development ofconceptual and theoretical ecological mod-
els and better understanding of marine microbial diversity
and its connections to global biogeochemical cycles (Bowler
et at. 2009) .
 Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material

Lorge ""'.~ -
phytoplankton- _ _~~_ , --= 7 .....

?:J)~ ""
~ Small 1
phytoplankton ~~
1:.'~ ~~
E

'. :. ~..
:,.
<,
~
J Zooplankton g
-
• : " ~',,:: , ... - ' fl!1 Microlooplonkton c
•
-=
.-
o
o
c
~

Sea floor

Figure 3.26 The biological pump is a collective property of phytoplankton-based food webs. Together with the solubility
pump (right), which is driven by chemical and biological processes, it maintains a sharp gradient of CO2 between the
atmosphere and deep oceans, where carbon is stored. Most of the phytoplankton POM production is decomposed
into CO 2 in the upper water layers, from where it re-enters t he atmosp here. Part of the produced POM is exported into
deeper water layers, decomposed into CO 2 and stays d issolved in deep water. The net resu lt is transpo rt of CO 2 from t he
atmosphere to the deep ocean. The food web structure, relative abundance of species, and production control influence
how much CO, w ill be pumped into the deep ocean (illustration and figure caption from Chisholm 200 1).

Chapter Summary
• The small size and large surface-to-volume ratio of micro-organisms endows them with extraordi-
nary hig h metabo lic rates.
• Due to the high o rgan ic losses at each troph ic step, marine food-chains transfer a minute amount
of primary production t o the top predato rs.
• Marine microbial food-chains interlink and form complex, highly dynam ic microbial food-webs that
are the engine of oceanic biogeochemical cycles.
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

• Ecosystems consequently are hig hly efficient at recycl ing organic matter and nutrients. Most of the
metabolism in the ocean plankton is associated with single-celled organisms.
• The utilization of 'waste' organ ic detritus by the micro-organisms provides the basis of a second
food chain that o riginates from marine bacteria.
• The seasonal cycle of the trophic metabolism may be considered in four phases:
• Phase I-the in itial development of the sp ring p hytoplankton bloom.
• Phase II-the demise of the p hytoplankton bloom.
• Phase III-a mid-summer recycling p hase.
• Phase IV-the rege nerat ive period , last ing until the bloom the following spring.
• The Oceanic microbes playa central ro le in the global carbon cycle and subsequently climate regu la-
tion.
• Microbial oceanography is a relatively new scientific discipl ine that focuses on the ocean as a habitat
fo r the evolution and reg ulation of microbial-based processes and their ecological consequences.

Further Reading
Books
• del Giorgio. P. A. & P. J. le B, Williams 2005. The global significance of respirat ion in aquatic ecosystems :
from single cells to the b iosphere. In P. A. del Giorgio & P. J. Ie B. Will iams (eds) Respiration in Aquatic
Ecosystems. Oxford University Press. Oxford, pp, 267-303 .
• Hansell. D, A. & C. A. Carlson 2002 . Biogeochemistry of Morine Dissolved Organic Matter. Academ ic
Press, Amsterdam.
• Kirchman. D, l . (ed.) 2000. Micrabial Ecology of the Oceans. John Wiley & Sons. Inc. New York.
• Kirchman. D. L (ed.) 2008. Micrabial Ecology of the Oceans (2nd edn) . John Wiley & Sons. Inc. New
York,

Key papers and reviews

• Arrigo K. 2005. Marine micro-organisms and global nut rient cycles . Nature 437: 349-355.
• Bowler. c., Karl, D, M" & Colwell, R. R. 2009. Microbial oceanography in the sea of oppo rtu nity, Nature,
4 5 9 : 18 0-1 84.
• Caron. D. A. , Worden, A. Z .• Counlway, P. D.• Demir. E" & Heidelberg, K, B, 2009. Protists are microbes
too: a perspective. ISME Journal. 3: 4- 12.
• Delong. E. F. 2009. The microbial ocean from genomes to biomes. Nature 4 5 9 : 200-206.
• Delong. E. F. & D, M. Karl 2005. Genom ic perspect ives in microbial oceanog raphy. Nature. 437 :
336-3 42.
• Fuhrman J. A. 2009. Microbial community structure and its functional implications. Nature 459: 19 3-
19 9 .
• Giovannoni. S, J. & U. St ingl 2005. Molecular diversity and eco logy of microbial plankton. Nature, 4 37:
3 43-348.
• Legendre, L & Rassoulzadegan, F. 199 5. Plankton and nutrient dynamics in marine waters. Ophelia 4 1:
15 3- 7 2 .
• Moran, M. A. & Armbrust, E, V. 2007. Genomes of Sea Microbes. Oceanography, 20: 47-55.
• Pomeroy, L R. 19 74 . The ocean's food we b. a changi ng paradigm , Bioscience 24 : 4 9 9- 504.
• Suttle. C. A. 2005. Viruses in t he sea. Nature, 4 3 7: 356-36 1.
Secondary Production
Chapter Summary
Secon dary production is the production of biomass by het-
erotrophic organisms and is measured as the increase in
biomass over time. In food we bs, secondary production can
be defined as the total amoun t of biomass tha t becomes
available to be consumed by the next t rophic level. Second-
ary production of a population depends on the growth and
mortality rates of the population and it is, therefore, tightly
4.1 Introduction
Secondary production is the production of biomass by het-
erotrophic organisms, and this includes all production by
animals, fun gi, and some bacteria. A large fraction of the
primary production of micro- and macroalgae is consumed
by multicellular heterotrophic organisms and converted
into secondary production. The amount of secondary pro-
duction in an ecosystem, therefore, defines how much of
the primar y production is converted into heterotrophic bio-
mass. The amount of secondary production by a particular
trophic level also determines how much food is available
for higher trophic levels. For example, the second ary pro-
duction of a fish population will define what the maximum
sustainable yield is for this population, and determines how
much food this population needs to maintain its rate of
growth (see also Chapter 13) . Therefore, the quantification
of secondary production is an important step in enabling
us to understand the flow of energy in food webs and the
carrying capacity of ecosystems. Secondary production
has also been used as an indicator of ecosystem health
(Murawski 2000; Rochet & TrenkeI2003). This means that
the quantification of secondary production is of great inter-
est to marine and fisheries ecologists.
linked to the life history of organisms. As a result, the pro-
duction to b iomass ratio of small organisms is generally
higher than that of larger organisms. This chapter introduces
how secondary production is measured and the major fac-
tors that control it. Human impacts, such as fisheries, eutro-
phication, and climate change, generally have a negative
impact on secondary production.
This chapter discusses what secondary production is,
how it is measured, what determines the amount of second-
ary production and how secondary production is affected
by human activities. This chapter is focused on the second-
ar y production of marine benthic invertebrates and fish.
Techniques to estimate energy flow in microbial food webs
are discussed in Chapter 3.
The carrying capacity of a species is the population size
or biomass that an ecosystem can support in the long
term . The trophic level of an organism is their position in
the food chain . Plants form the first trophic level , animals
that feed on plants (herbivores) are the second trophic
level. Carnivores that feed on these herbivores form the
third trophic level.
4.1.1 What is secondary production?
It would seem logical to call production by herbivores sec-
ondary production and production by carnivores tertiary
production, and this terminology is sometimes used. How-
ever, in general all production by heterotrophs is summa-
rized under the term secondary production and that is how
 4.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

we will use the term secondary production in this chapter.

Secondary production is defined as the production of
biomass by heterotrophic organisms and is measured as the
change in biomass with time . In food webs, secondary pro- June
duction can be defined as the total amount of biomass that
is available to be consumed by the next trophic level over
some time period. While biomass is measured as a density
(e.g. g m"), production is measured as a rate (e.g. g rrr-y' ). July
To illustrate what secondary production is, consider the
following analogy. A fish farmer starts with fish eggs, and
raises these through the larval and juvenile stages until the
fish reaches a marketable size. During this period. which August
can last several years. the fish will increase in size, but at
the same time many eggs, larvae, and fish will die. The
production of this fish farm is the sum of the biomass of

Figure 4.2 (a) Production of the encrusting bryozoan

Figure 4.1 Siphon cropping of the clam
by a juvenile plaice Pleuronectes platessa.
Membranipora membranacea. This colonial bryozoan
typically lives on fronds of kelp such as Laminaria digitata
and can grow very fast. This image illustrates the size of
the colony over three subsequent months. The production
of this colony in July (1 month, production measured in
this case as mm 2 month") is equal to the surface area of
the colony in July, minus the surface area that was already
present in June. Similarly, the production of this colony in
August is equal to the surface area of the colony in August,
minus the surface area that was already present in July_(b)
The nudibranch Limacia c1avigeria feed ing on Membranipora
Macoma balthica membranacea. (c) Light microscope image of Membranipora
membranacea, Galway Bay, Ireland (A.-M. Amui-Vedel).
 Chapter 4 Secondary Production

all fish when they are harvested when marketable, minus
the biomass of all fish when they entered the farm (in this
case the negligible weight ofthe eggs). To calculate the pro-
duction of fish per year, the biomass of fish at h arvesting is
divided by the time over which the fish grew, which gives
the biomass produced per year (e .g. tons fish y ' ). A farmer
will aim to maximize this production, rather than the bio-
mass present on the farm, as the number of animals that
leave the farm determine his income (see also Fig. 4.2). In
ecological stud ies, the meat produced by animals that died
before harvesting is also included in the secondary produc-
tion estimate.
Secondary production cons ists of two components :
somatic and gonad production. Somatic production is the
production of tissues, such as muscle, brain, skin, scales,
shell, but not gonads . Gonad production is the production
of reproduc tive tissue, suc h as sperm and eggs. Most sci-
ent ific studies of secondary product ion focus on somatic
production a lone and ignore go nad production. In this
chapter we will focus on somatic produc tion. Ecologists
and the fishery biologists are m ost interested in somatic
produc tion because this represents the quantity of m atter
and energy that is available as food for the organisms in the
next trophic level, suc h as natural predators, and for human
consumpt ion in the case of commercially exploited species
(see Chapter 13). Secondary production also includes body
parts that are lost and regenerated . For example, a sign ifi-
cant part of the production of bivalve populations on inter-
tidal mudflats is due to the regeneration of siphons that are
cropped by fish and shrimp predators (Fig. 4.1) (De Vlas
1979). In this example, this component of production can
be difficult to quantify because it requires knowledge of the
frequency of siphon cro pping by predators.
Production changes according to the life-stage (egg,
juvenile, adult), season, and availability of food .

Box 4.1 Effect of the development

of a cohort on production

Secon dary prod uct ion of a pop ulat ion depend s

on the growth and mortality rates of th e po pula- (o) ec ••
tion . Production th erefore changes w ith life stage, e •••
season, and food supply. The producti on of an • c ••
e c ••
ind ividual organis m is equal to th e increase in the ce.e
bod y mass of thi s ind ivid ual over a year. The popula-
300- , - - - - - - - - - - - - - , - - - , - 12
tion production is th e sum of the pro duction of all
ind ividuals in a popu lation. To ill ust rate th is, let us
consider a popu lation of clams Nucula nitidosa, and
250 10
-=
8 ..s
:E
wi thin th is popu lation a single cohort. A cohort is a =
• Density 6 ~
group of plants or animals born more or less at the • Weigbt
same time. Cl ear co horts can be found in popula-
tion s where reproduction is seaso nal. Species that
reproduce throughout th e year w ill not have defined
cohorts and spec ies that have life cycl es that are 1968 1970 1972 1974
shorter than one year can have several co horts in a Year
year that may be indisti nguishable. When th e larv ae (b) 800 , -- - - - - - - - - - - - ----,
of the clams settle, the larvae are abundant and
700
small. Over th e perio d of several years, the indivi dual
clams increase in mass, while at the same time many 600
indivi dual clam s die, until after about 8 years the last ~= 500
large clam dies (fig ure a). The tota l biom ass of this -E
400
300
is
The populati on development of the 1968 cohort a 200
of Nucula nitidosa in Swan sea bay based on
.::
100
data from Warwi ck & George (1980): (a) density 0+----,- ,-----,- --,- .----.- ,--- ,----1
and average weight (AFDW), (b) cohort biomass 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976
(AFDW). Year
 4.2 Measuring secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
population at any ti me can be calculated by multiplying
the abundance by the average weight of the clams. The
total biomass of cl ams increases from near zero in 1968
to a maximum in 19 7 1, and then decreases agai n to near
zero in 19 75. Biomass is therefore add ed to the cohort by
the gro wth of individual organisms, while biomass is lost
from the cohort due to mortality of individuals. Mortality
occurs due to predation, disease, senescence or changing
environmental conditions such as hypoxia.
Second ary production of a population thus depends
on the growth and mortality rates of the population.
4.1.2 The production to biomass ratio
(PIB)
When trying to understand patterns in production, a use-
ful concept is the production to biomass ratio (P/B) .
This ratio describes how much biomass is produced by the
standing stock of biomass, usually per year. For example,
the PIB of macrobenthic invertebrates is around 1.5; this
means that the annual production of macrobenthic inver-
tebrates is about 1.5 times its average biomass.
Growt h and mortality are two important life-history
parameters, and as with most life-history parameters, both
growth and mortality are correlated to the body size of
organisms. Because of this, the PIB of species and popu-
lations is also closely correlated to their body size. Small
species generally have high growth rates and high mortality
rates. This results in a low biomass but a high production
and therefore small organ isms have a high PIB. Large spe-
cies have low growth rates and low mortality rates. This
results in a high biomass but a low production and therefore
large organisms have a low PIB (Box 4.1) . The general rule
of a higher PI B for smaller organ isms is also valid within
Table 4.1 Typical PIB values for some groups of
marine organisms. Small organisms generally have
higher production to biomass ratios than larger
organIsms.
Group PIS
Bacteri a 26~292
Micro-alg ae 7-24
Meiofauna 3-19
Sm all benthic invertebrates 1-6
Large benthic invertebrates 0.2-2
Fish 0.5-0.8
Sources: Jenn ings et al. (2001 a); Schwing hamer et al. (1986).
A species with equivalent growth but a lower mortality
rate will reach a h igher population b iomass maximum
and will therefore have a higher production. A species
wi th equivalent mortali ty rate but a lower growth rate
will reach a lower popul ation biom ass maximum and
will therefo re have a lower p roduction. Obv iously, t he
com bi nation of hig h growth and low mortality results in
highest production.
We explain in Section 4.2 how to calculate the produc-
tion of the clam population.
species; a cohort of l -year-old juvenile clams will have a
higher PIB than a cohort of 5-year-old adult clams. Again,
this is due to the relatively higher growth rates of smaller
and younger organ isms.
Because PI B ratios va ry widely between different groups
of second ary producers, even groups that seem less impor-
tant in terms of biomass can contribute sign ificantly to eco-
system production when they have a high PIB ratio (Table
4.1). For example, nematodes in soft sediments generally
have a lower biomass than macrofaunal invertebrates, but
because their P/B is higher, their production is generally
higher than that of macrofaunal invertebrates (Schwing-
hamer et al. 1986).
4.2 Measuring secondary
production
Production can be reported in many different units. For
example, production has been reported as wet weight/
mass (WWI W M ), ash free dry weight/mass (AFDWI
AFDM), organic carbon (e ) , and joules (J) , all per year, and
for different areas or volumes (e.g. m·2 , km', m-'). When
comparing production estimates from different sources, it
is therefore important to ensure that comparable units are
used. If different units are used, conversion factors can be
used to recalculate all measurements to a single unit (Brey
2008) .
4.2.1 Cohort-based methods
Secondary production is most easily estimated for rec-
ognizable cohorts of species. To measure the secondary
production of a cohort, we have to examine the growt h of
individu al organisms and the population mortality. 'IWo
different approaches are possible when estimating second-
ary production using cohort-based methods: measurement
of production of biomass due to growth, or the measure-
ment of the elimination of biomass due to mortality.
 Chapter 4 Secondary Production

Measurement of the elimination of biomass as a measure and fish, one has to separate these cohorts from each other
of production may seem counter-intuitive, but one has to before the analysis. For bivalves such as Nucula nitidosa,
realize that all biomass that is lost by a cohort due to mor- individual cohorts are usually recognized by counting the
tality must have been added previously due to production number of year-rings on the shell. Fish cohorts can be rec-
by growth . Therefore, at the cohort level, whe n the last an i- ognized by counting year-rings on the otoliths or scales.
mal in the cohort dies, the amount of biomass eliminated However, unlike fish and clams, many organisms leave no
exactly equals the amount of biomass produced (a lthough easily discernable record of their age in growth structures.
this argument is less robust when considering organisms The production of a population with identifiable cohorts
that can regenerate body parts or those that grow and can be estimated using the increment summation method
senesce). The biomass that was produced by an organism (Table 4.2) . The 19 68 cohort of Nucu la nitidosa was sam-
only becomes available for higher trophic levels when it dies pled each year in summer to estimate the density and aver-
(for whatever reason: predation, parasitism, disease , harsh age body mass ofthis cohort. The density of clams decreased
abiotic conditions) and therefore the biomass eliminated is over time to reach zero in 1976, while the average body
a logical way to estimate secondary production in foodweb mass increased at the same time (Box 4.1 , figure a). The
studies. Furthermore, measuring the production of biomass total population biomass (= density x average body mass)
due to growth and the measurement of the elimination of reached a maximum in 1971 (Box 4 .1, figure b) . The incre-
biomass due to mortality can be mathematically equivalent. ment summation method calculates how much the average
As described in the example of the clam Nucula nitidosa clam increased in weight over each sampling period, in this
(Box 4.1) , a cohort starts at birth with m any eggs with a low case a year. Because some clams died over the period of a
body mass and finishes with the death of the last old and year, we have to use the average density over the examined
large individual. Biomass is added to this cohort by growth period to get a representative estimate of the abundance of
of the body mass of individual organisms, while biomass is the clams in that year and therefore a good production esti-
lost from the cohort by the death of individual organisms. mate. This method means that the increment summation
To estimate production of a cohort, it is necessary to repeat- method estimates the area under the curve when density is
edly measure the abundance and body mass of the cohort plotted against average body mass, and such a plot has been
(Box 4.1). When more than one cohort is present in the named the Allen plot (Fig. 4.3 ) . The actual calculat ions are
population, as is usually the case for benthic invertebrates straightforward and illustrated in Table 4.2. To estimate

Table 4.2. Calculation of the production of the 1968 cohort of Nucula nitidosa in Swansea Bay using the
increment summation method .

Year Density Body mass Body mass Average of Production Average PIB
(n m- Z) (mg) difference density in two (mg m-z y-') population ratio
between years (n m- Z ) biomass
years (mg) (mg m- Z)

1968 248 0.149

1.0 71 206 (A) 221 1 19 1.8 6
1969 16 4 1.2 20
2.529 144.5 365 334 1.0 9
1970 125 3.749
2. 195 121.5 267 585 0.46
197 1 1 18 5.944
2.23 1 83 185 547 0.34
1972 48 8.175
1.4 4 5 29 (B) 42 244 0.17
1973 10 9.620
0.709 8.5 6 84 0.07
1974 7 10.329
0.910 6.5 6 70 0.08
1975 6 1 1.239
2.783 3 8 34 0.25
1976 0 14.022
• • • •• •• •• • •• •• • •• • •• • •• • •• • • •• • • • •• • • • • •• • • • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • • • • •• • • • •• • • • •• • • • •• • •• • •• •• •• • •• •• • •• •• •• •• •• •• •• ••• •

Total 1 10 0 mg m- 2

A and B refer to the areas under the fitted line in figure 4 .3 that corresponds to these values. Biomass is reported as mg ash free dry
we ight. Modified from Warw ick & George ( 19 8 0 ). An excel spreadsheet of these calculat ions is available on the Online Resource Centre.
 4.2 Measuring secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

300 -,---- - - - - - - - - - - - - - ,
production over the 1968-69 period, it is necessary to cal-
culate the difference in body mass for the average animal
between the two years (i.e, the increase in body mass over 250 1968
this period, 1.071 mg) and the average of the densities in
the two years (206 nr-) . Production over this period is then
200
simply the product of the increase in body mass and the
'1
average number of animals present: 1.071 mg x 206 m-2
= 221 mg m-2 y l. This amount is equivalent to the area of -"
~
~

150
A in Fig. 4.3. This method requires repeated sampling of
the same population and the precision of the production
0"
~

100
estimate will increase with increasing sampling frequency.
A
Ideally, the population should be sampled several times a
year. Infrequent sampling leads to an underestimation of 50
secondary production rates (Morin et aI. 1987). The last 1973
1974 1975 1976
column ofTable 4.2 presents the P/B ratio ofthis cohort. As 0
expected, P/B decreases with the increasing age and body- 0 2 4 6 8 10 12 14 16
size of this cohort. 80dy mass Imy)
If cohorts cannot be identified and separated, cohort-
based methods such as the increment summation method Figure 4.3 Allen plot of Nucula nitidosa. Over time,
cannot be applied. Some complicated mathematical meth- the dens ity of clams decreases while their body mass
ods can be used to estimate production, but these are increases. Production is the product of the increase in
beyond the scope ofthis book (see Van der Meer 2005) . body mass over a period and the average number of
organ ims present in this period. The area under the curve
therefore represents the production of this cohort over
4.2.2 Allometric relationships its lifetime. Areas A and B refer to the production of the
It is easy to appreciate that estimating the production ofjust years 1968-69 and 1972-73, respectively.
a single cohort of a species requires a substantial amount
of field work to repeatedly collect samples and laboratory
analysis to quantify, age, and weigh all organisms. How-
ever. often the production of a whole community, rather
than a single species. needs to be estimated. Sampling of
marine organisms can be time-consuming and expensive,
particularly when research vessels need to be used to sam-
ple offshore ecosystems. Methods to estimate production
that only require a single sampling campaign and no ageing
of the organisms are therefore much less time-consuming
and therefore cheaper. As we have shown above. a correla-
tion exists between the body size of organisms and their
P/B ratio. The relationship between P/B and the body size
of individual organisms can be used to estimate produc-
tion of communities when the body size of the organisms
in this community is known. For example. Jennings et al.
(2001b) developed an allometric relationship between
body mass and the P/B ofmarine invertebrates, which they Figure 4.4 A 2-m beam trawl sample from gravelly
used to estimate the production of benthic invertebrate ground in the Long forties in the northern North Sea.
communities in the North Sea. Theyweighed all individual Weighing every individual animal from a sample like this is
organisms in their beam trawl and anchor dredge samples. a labour intensive activity. Photo: J.G. Hiddink.
and used these weights to estimate the PIB ratio for each
of these organisms (Figs 4.4 and 4.5) . By multiplying P/B ment, as well as the body size of the organisms, to estimate
with the body mass of each individual organism, the pro- production. This is particularly useful when large spatial
duction for this organism is estimated. The sum of all these scales are considered. where the environmental conditions
individual production estimates then gives the production vary considerably. Tumbiolo and Downing (1994) devel-
of the whole community. oped a marine benthos production model that accounts for
Alternative approaches use information on the environ- worldwide variation in benthic production based on bio-
 Chapter 4 Secondary Production
1,----------------,
1 Wm (mg dry mass). the annual mean surface temperature
0 10gP = 0 .24 + 0.96 10g B -0.21l0gWm
=-
15
0.;
0 + 0 .03 T, - 0. 16 l og (Z + 1).
...
,;;
0
•
-I
• •
-1 + - - - - - , - - - - - - r - - - - - - - - - 1
-4 -1 0 1
10910 bodymoss
Figure 4 .5 The relation ship between the body mass
(9 AFDW) of North Sea benthic invertebrates and their
production-to-biomass (PIS) ratio. Larger organism s have
a lower PIS ratio. The fitted relationship is described by
109 10 PIS = 0.233 109 10 B + 0 .197. Source: Jenning s et al.
(2001 b).
TECHNIQUES: Using meta-analysis
to examine global patterns of macro-
invertebrate production in marine
benthic habitats
A meta-analysis combines the results of multip le stu dies
that address similar research questions, and provides a
powerful tool to generate general trends or responses
at global scal es. In a meta-analysis, data are integ rated
and summ arized from ind ivid ual st ud ies to generate a
single estim at e for an effect. The advantage of doing this
is that the results of the meta-analysis w ill be more gen-
erally appl icable than the results of the ind ividual stu d-
ies and that a meta-analysis w ill be more powerful than
single st udies (essent ially each individual stu dy becomes
a single rep licate). Meta-analysis is wi dely used in epi-
demiology and evidence-based medicine today. For a
detailed descri pti on of how meta-analysis can be used
in a systemat ic review process in conservation and envi-
ronmental management, please refer to the Guidelines
for Systematic Review of Effectiveness of Interventions
in Conservation and Environmen tal Management (htt p:/ /
www.cebc.bangor.ac.uk/Doc uments/Review guid elines-
version3.0JI NAL_OOO. pdf).
mass, individu al body mass, water temperature, and depth.
Accord ing to their study, production P (mg dry mass y l)
depends on body m ass of the organism B (mg dry mass),
the maximum ind ividual body mass that a species can reach
T, ('C) , and depth Z (m) for m arine be nthic invertebrates :
This equation explains 86% of the observed large-scale
worldwide variability in the production of benthic marine
inverteb rates. The effect of temperature is pos itive, indicat-
ing that production is higher in warmer seas. The effect of
depth is negative, suggest ing that food quantity or qu ality
are lower at greater water dept h.
The predictions of production by allometric relation-
ships are only correct for average populations. The pro-
duction that is estimated by these models for individual
populat ions can be wrong by as much as factor 2.5 (Bre y
2008). Prediction error diminishes rapidly when estimates
of several populations in a commun ity are pooled. There-
fore, allometric relationships can be used to estimate the
production of whole communities (i.e. the combination of
many populations), but should not be used to estimate the
production for individual species.
Large-scale patterns of benthic production and produc-
t ion to bi omass ratios (PIB ) are a function of life-history
characteristics of populat ions (such as populat ion bio-
mass, body size, and maximum age) and the environment.
Using a meta-analysis of data published in 15 marine
ecology journals, Cusson and Bourget (200 5) examined
global patte rns in the production of marine benthic inver-
tebrates and in relation to envi ronmental vari ables such
as substrate ty pe, wa ter depth, and seawater tempera-
ture. Their database contained 54 7 datasets that related
the second ary production of benth ic invertebrates to
environmenta l variables from 14 7 papers. The datasets
included information on 207 taxa from 170 study sites,
ranging from 0 to 930 m depth. From each dataset,
they collected information about secon dary production
and environmental parameters. The relationship between
environmental variables, life-history variables, and PIB
ratios was examined for the dominant taxonomic groups
of benthic invertebrates (annelids, arthropods, echino-
derm s, and mo ll uscs).
The meta-analysis s howed that hi gh values of PIB
ratios were observed in temperate zones w hile low val-
ues of PIB ratios we re observed in polar regions (8 0
 4.2 Measuring secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

to 60 0 5) and (sub) trop ical zones (4 0 0 5 to 20 0 N)
(see fi gure). The highest production was observed on
hard substrata, for filterfeedi ng molluscs. The highest Pia
ratios were observed for org anisms that feed on algae
including sed iment with hi gh organic enrichment, omni-
vores, and arthropods (see table) . Production and Pia
ratios we re lower in deeper waters an d higher at higher
temperatures. This can be expl ai ned from the decreas-
ing food avail ability with depth an d increasi ng potential
for growth with increasing temperatures. However, these
abiotic vari abl es did not greatly improve the predictions of
production by biotic variables such as life span an d mean
body mass alone.

Table Outputs of the meta-analysis of 147 studies. Mean annual production (+SE) and PIS for the
dominant taxonomic groups, functional groups, and subst rata (Cusson & Bourget 2005).

Group Mean production Mean P/B ratio (y,.-')

(109 10; kJ m-Zy,.-1)
Taxonomic group
Mollusca 1.9 4 + 0.08 (n= 227) 1.77 + 0. 14 (n= 230)
Annelida 1.42 + 0.09 (n = 12 3) 3.37 + 0.38 (n = 120 )
Arthropoda 1.30 + 0.08 (n = 140 ) 4.85 + 0.3 1 (n = 140 )
Echinodermata 1.34 + 0.23 (n = 27) 0.3 4 + 0.06 (n = 28)

Functional guild
Deposit feeders 1.47 + 0.09 (n = 175) 2.54 + 0. 15 (n = 175)
Fi Iter feed ers 1.9 6 + 0. 11 (n = 134 ) 1.8 2 + 0.20 (n = 136)
Grazers 1.64 + 0.08 (n = 8 1) 2.81 + 0 .43 (n = 82)
Omnivores 1.2 5 + 0.1 1 (n = 96) 4 .94 + 0.54 (n = 95)
Predator 1.3 7 + 0. 13 (n = 4 5) 3.41 + 0 .49 (n = 4 2)

Substratum type
Alg ae = 65)
1.10 + 0. 15 (n = 62)
4 .1 8 + 0 .48 (n
Hard 2.2 1 + 0. 16 (n = 69) 1.09 + 0.18 (n = 70)
Muddy 1.46 + 0.07 (n = 219) 3.25 + 0.21 (n = 216)
Sandy 1.67 + 0.08 (n = 18 4 ) 2.90 + 0.30 (n = 188 )

4-,---- - - - - - - - - - - - -----,

I
1

0 1----._ • ,----,-_ -,------,_ -,-------,_ ---,----\

 Chapter 4 Secondary Production
4.3 Drivers of secondary
production
Table 4.3 presents some typical values of secondary pro-
duction from different marine ecosystems. There exists
a large variation in the magnitude of secondary produc-
tion between different ecosystems and different groups of
organisms . In this section we w ill discuss w hat factors are
responsible for these differences.
In the preced ing text (Section 4.2.2), the empirical rela-
tionship between production and environmental factors
indicates that secondary production of benthic inverte-
brates relates to temperature and water depth. In general,
secondary production of a population is affected by the
amo unt of food that is available for this population. This
in turn depends on local primary production, bottom tem-
perature, water depth, the troph ic level of the o rganism,
and the trophic efficiency of the organisms in the fo od web.
Ecosystems that have a high primary production can
support more secondary production. For example , a strong
large -scale correlation exists between the amount of pri-
mary production by phytoplankto n and the production of
fish and squid (Iverson 1990 ; Frank et aI. 2007) . Such eco-
sys tems, in which the abundance of organisms at higher tro -
phic levels is positively related to primary production, are
said to be governed by bottom-up control. Top-down con-
trol occurs when, for example, the grazing of filter-feeding
benthos on phytoplankton is so strong that they deplete the
phytoplankton, such that a neg ative correlation between
the abundance of the filter feeders and the phytoplankton
exists (see also Chapter 7) .
Table 4.3. Typical values of secondary production for a set of ecosystem s and groups of organisms. 1 g C
repre sents approximatel y 13 g wet weight ti ssue (Brey 2008) . Secondary production is high for organisms
at low trophi c level s, and for producti ve ecosystems in shallow coastal seas. Production is lower for deep sea
ecosystems and for high trophic level organisms.
Ecosystem type Area
Deep sea
Shelf sea North Sea
Tropical coral reefs
Deep sea Rockall Trough
Shelf sea Bay of Fundy
Tidal flats Wadden Sea
Shelf sea Bay of Fundy
Shelf sea North Sea
Upwelling zones
Sources: Cush ing (1 9 6 9); Beukema & Cadee ( 1986); Emerson ( 1989); Gage (1 9 92); Haedrich & Merrett ( 1992); Heath (2005);
Hiddink et al. (2006); Jenn in gs et al. (2001 a).
Primary production determine s how mu ch energy
is potentially available for secondary production . The
amount o f this energy that actually ends up in organisms
as tissu e depends on the efficiency o f the transfer of this
energy betwee n trophic levels (t he transfer efficiency),
and the number o f times this transfer is made , w hich is
defined by the food-chain length. Transfer efficiencies
fo r ectothermic marine organisms, such as zooplankton,
cephalopods, and fish, are in the range of 10- 60% (Jen-
nings et aI. 2001 a). This means that 10- 60% of the energy
that was consumed is then converted into the tissue o f the
predator. Thus, in each step in the food chain, 40- 90%
of the energy is lost to sloppy feeding, res piration, an d
incomplete digestion. Predators that are at the top of long
fo od-chains w ill therefore have less food available to them
and therefore a lower secondary production than preda-
tors halfw ay up these foo d chains . Exam ine, for example ,
the very simple food we bs in Fig. 4. 6. Phytoplankton is
eaten by krill, krill is eaten by a baleen whale, or alterna-
tively by a fish that is eaten by a baleen whale . The four-
link food-chain has a lower potential production of baleen
whales because energy is lost in each transfer in the chain
(as transfer efficie ncy is < 10 0%) and the chain is longer.
Since the energy transfer is inefficient, the produ ction of
explo ited species w ill be lower for species that are higher
up the foo d chain . Species such as mussels, anchoveta
(Peruvian anchovy, Engraulis ringens), and krill that feed
directly on phytoplankto n w ill therefore be more produc-
tive than species that are at the apex of long fo od chains
such as tuna, sharks, and cod.
Group Secondary production
(9 C m-2 y-')
Fish 0.02-0.21
Fish 5.1
Fish 2.3-5.8
Macrobenthic invertebrates 0.1
Macrobenthic invertebrates 15.4
Macrobenthic invertebrates 10.8-45.9
Meiobenthic invertebrates 17.5
Zooplankton 36.6
Zooplankton 5.4-22
 4.3 Drivers of secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

I I.0Sg Cm'y'
IS.2S gCm-' y' I
Baleen wholes Baleen wholes
I Transfer efficiency· 15%
I Transfer effldenry - 15%

Zooplankton,
induding krill
I 3SgCm ' y' Fish ) :e .( ~ I 7gCm ' y'
Transferefficiency" 20%

I• Transfer efficiency" 35%

Zooplankton,
I I 3SgCm ' y'
iY
~~
IlO0gCm ' y' I includingkrill
Phytoplonkton
I Transfer efficiency " 35%

I lO0gCm'y' I
Phyloplonkton

Figure 4 .6 Two simple food-chains that assume that all production is used by the next trophic level. Energy is lost
in every step of the food chain because transfer efficiency is less than 1000;0. Because of this, in this example the
production of baleen whales that feed on krill is higher than the production of baleen whales that feed on fish, which in
turn feed on krill.

CURRENT FOCUS: Fish production is

primary production (see figure). The highest productivity
determined by primary production
of phytoplankton and fish occurs off the coasts of Wash-
Fishing yields from cont inental-shelf ecosystems can ington and southern Bri tish Columbia. These results there-
either be controlled by the amou nt of primary production fore support the hypothesis that fish catches in these
available (bottom-up control) or by predator-prey inter- ecosystems are controlled by the primary production and
actions (top-down control; see Chapter 7).lf fish catches are therefore bottom-up controlled.
are controlled by primary production through bottom-up
contro l, a posi tive correlation between fish production
and primary production is expected. Ware and Thomson
r = 0.87;
(2005) used the mean annual chlorophyll a concentration
p<O.OOOI ;
to test the hypothesis that the fish production along the n= 11
west coast of North America is controlled by primary pro-
duction of phytoplankton. The surface concentration of
2.0
•
chlorophyll a is a proxy for the rate of primary production
and can easily be estimated using satellite images (e.g.
using SeaWiFS; htt p:/ / oceancolor. gsfc .nasa.gov/ Sea-
WiFSI). Resident species, such as herring and groundfish,
are those fish that occupy the conti nental shelf year-round
and undertake only spatially limited seasonal mig rations.
The study considered reside nt fish species only because
these are the species tha t depend exclusively on local
food production. In sustainably exploited fisheries , the
yield of fish is likely to be related to their production, and 0.0 -j--.--,--,,!- , --,-,--,--,-- ,, -, -.,--j
therefore it was considered justified to use catches as a o 2 4 6
Mean rhl-e ronrenlmlion {mg.}
proxy for fish production. The mean annual yields of resi-
dent fish species were calculated from landing statistics
from 19 60 to 1998. The results of Ware and Thomson Large-scale correlation of the annual mean chlorophyll
(2005) showed a clear alongshore variation in primary a concent rat io n and the long-term annual yield of resi-
production along the west coast of North America and dent fish for each of 11 regions on the west coast of
that the yield of resident fish was strongly correlated to North America (Ware & Thomson 2005).
 Chapter 4 Secondary Production

We can now explain the differences in the second- Relatively few marine organisms dismantle prey that
ary production in the different ecosystems and groups of are larger than their own body mass. Exceptions wou ld
organisms that we observed in Table 4 .3 . The production incl ude crabs and some pelagic shark species.
of benthic organisms in shallow seas and intertidal areas is
higher than in the deep sea because primary production is As discussed earlier. the production-to-biomass ratio of
generally higher in these areas, and because a larger frac- small organisms is higher than for large organisms. This
tion of this primary production reaches the seabed in areas means that the amount of biomass that is produced at lower
that are shallow (the deeper the water column the greater trophic levels by small organisms is higher than the produc-
the chance ofan organism intercepting the primary produc- tion of biomass at higher trophic levels generated by larger
tion on its way to the seabed) . Within ecosystems. the pro- organisms. In addition to this, energy is lost in each step in
duction of zooplankton and macrobenthos is higher than the food chain because the transfer efficiency of organisms
that of fish because they have a lower trophic level. is only around 10-60%. This means that more food is avail-
able for small, low trophic-level organisms than for large,
high trophic-level organisms. As a result of this, generally
4.4 Size structuring in marine marine ecosystems have a typical size structure with many
food-webs small organisms and fewer large organisms (Fig. 4.8) . This
regular pattern of the distribution of biomass over the body
The body-size of organisms relates to their position in food size classes oforganismscan be disrupted bydisturbance of
webs in marine ecosystems. Most marine fish and benthic ecosystems (see below under Section 4 .5.1) .
invertebrates eat their prey whole and therefore the maxi-
mum size of prey they can eat is limited by the size of their
mouth. As a result of this. larger organisms feed on larger
prey at high trophic levels, while smaller organisms prey
on smaller prey at lower trophic levels. Therefore, marine
predators generally feed on prey that is substantially
smallerthan their own body mass (Fig. 4 .7) . For example,
fish in the North Sea feed on average on prey that has a body
mass that is 424 times lower than their own body mass (Jen-
nings & WaIT 2003) . This means that a 100 g herring will
feed on average on prey weighing just 0.235 g (about the
weight of a very small sandeel) .

5.5

(
~
./
I 1 Figure 4.8 The fish catch of a 4-m beam trawl in the
5.0 i J central North Sea, sorted according to body mass. The
{ J catch consists of many small fish, and progressively less
<' fish in the large-size classes. No very small fish were
V caught because they escaped through the mesh of the
/'( )
( 1A net. Photo: Nick Dulvy with permission.
./
./
~J
4.0 4.5 Human impacts on
secondary production
3.5 , , , , Human activity has the potential to change the magnitude
4 6 B 10 12 14
of secondary production in the seas and oceans, primar-
Body moss doss (l'9,)
ily through fisheries, eutrophication, and climate change.
Figure 4.7 The relationship between body mass and In fact, a key assumption behind fisheries' management is
mean trophic level for fish in the North Sea Large fish that exploitation will increase the produetion-to-biomass
feed at higher trophic levels in marine ecosystems ratio ofexploited stocks by removing the largest body-sized
(Jennings & Warr 2003). individuals in the population.
 4.5 Human impacts on secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

4.5.1 Fisheries illustrated using the direct physical disturbance to benthic

Exploitation will decrease the standing stock biomass of a
population. and will also lead to a reduction in the average
body size when the largest individuals ofa species are pref-
erentially caught, as in the case ofmost fisheries . As smaller
organisms have a higher PIB ratio, the PIB of exploited
populations will be higher than that for pristine popula-
tions. By reducing overall population size, the fishery will
also reduce intraspecific competition for resources (food,
mates, habitat), hence this also contributes to a higher PIB .
As a result. the reduction in production due to exploitation
will usually be less severe than the reduction in biomass.
Similarly, in communities with many species that all
differ in their life-history parameters (such as growth and
natural mortality rates), the most productive species tend
to be least severely affected by exploitation. Species with
low natural mortality rates will be more strongly affected by
additional fisheries' mortality than species with high natur-
al mortality rates, because the mortality due to fishing is
larger relative to their natural mortality. Life history cor-
relates strongly with body size, such that smaller organisms
have higher growth and mortality rates. This means that
in exploited communities. a shift in dominance to smaller
species can be expected (Myers & Worm 2003) .
The effect of fisheries on secondary production can be
communities associated with bottom trawling as an example.
Asingle pass of a bottom trawl. such as a beam or otter trawl
(see Chapter 13), typically results in an approximate mortal-
ityof 50% among the macrobenthic invertebrates that live in
or on the seabed (Kaiser et al. 2006) . In areas that are trawled
regularly, this physical disturbance results in changes in the
biomass, production, species' richness. and size distribution
of benthic invertebrates (Hiddink et al. 2006) . The biomass
of large, hard-bodied organisms, such as bivalves and bur-
rowing sea urchins, decreases strongly in response to bottom
trawling because of their naturally slow life-history (i.e, they
grow slowly and reproduce infrequently or have a late age
of maturity) . Small, soft-bodied animals, such as polychaete
worms. are much less severely affected by trawling, or may
even benefit from the release from competition with the
large-bodied invertebrates. Bottom trawling therefore has
a negative effect on the biomass and production of benthic
invertebrates. butbecause ofthe shiftin emphasis from large
to small animals with high PIB ratios, the decrease is less
pronounced for production than for biomass. For example.
for the southern North Sea, bottom trawling in 2003 reduced
biomass of benthic invertebrates by 56% (relative to pristine
conditions), while production was reduced by21 % (Fig. 4.9)
(Hiddink et al. 2006) .

Bottom trawling effort Production of benthic invertebrates

3·E 3·E

56·N North Seo 56·N

55·N 55·N

54·N - 54·N

53·N 53·N

UK
52·N 52·N
<
l·W O· I·E 2·E 3·E 4·E 5·E 6·E W O· I·E 2·E 3·E 4·E 5·E 6·E

Figure 4 .9 Bottom-trawling frequency and modelled production of benthic invertebrates in the southern North Sea
Production is negatively affected by bottom trawling and therefore production is the mirror image of bottom-trawling
frequency in some areas. In the southern North Sea, production is low regardless of trawling frequency because of
frequent disturbance by waves and strong tides (Hiddink et al. 2006).
 Chapter 4 Secondary Production

Although we use bottom trawling as an example of

physical disturbance, other forms of physical disturbance
such as ice scour, organism feeding activities, anoxia,
wave erosion , and current shear stress will all affect bio-
mass and production of organisms living on the seabed
(see Hall 1994 for a review) (see also Box 4.2).

Box 4.2 Effect of bottom trawling on

the production of benthic ecosystems
There are suggestions that bottom trawling may have posi-
tive effects on the secondary production of small worms,
and th ereby increase food production for flatfish, such as
juvenile plaice Pleuronectes pfatessa that feed on small
soft-bodied prey. The idea behind this is that 'ploughing '
the seabed with heavy beam traw ls increases the produc-
tion of the small benthos that flatfish feed on by remov-
ing the large fauna that small benthos compete with over
food and space (Hiddink et al. 2008). Support for this
idea is found from observations and model predictions
fo r the 'plaice box'. The plaice box is a 38 000 km 2 gear
rest riction area (a type of Marine Protected Area) in the
south-eastern North Sea th at w as established to reduce
the by-catch of undersized plaice (Pleuronectes pfatessa)
in heavily traw led coastal nursery grou nds. Large, mature
plaice are distributed more widely and further offshore
th an juvenil es (Rij nsdorp & van Leeuwen 1996). The
plaice box was closed to trawlers with an engine power
> 30 0 hp for part of the year in 19 8 9 and for t he whole
year since 19 9 5. Th ere are no spatial rest rict ions on fish-
ing by trawlers wi th an engine power < 30 0 hp and fishing
effort by these vessels in the plaice box has increased
since 1989. Neverthel ess, total t raw ling effort in the
plaice box was reduced by more than 90%, and most of
this effort w as redistributed into adjacent areas (Pastoors
et al. 2000). At the time of closu re, it was expected that
t his closu re would result in an increase in plaice stocks
of 25-35% , but instead plaice spawning stock biomass
has declined strongly (Pastoors et al. 2000). There also
seems to have been a shift in the spatial distri bution of (a) plaice Pleuronectes platessa on a sandy seabed and
juvenile plaice to the deeper offshore w ate rs that have (b) polychaete worms such as Ophelina Jimacina form
remai ned open to all trawlers. Beam traw ling causes direct an important food source for plaice. (Photographs: Hil-
physical disturbance of the seabed leading to the mor- mar Hinz with permission.)
tality of some components of the benthos, but creates
space for colonizat ion by smalle r-bodie d opportunistic
species, such as polychaete worms and small bivalve mol- the effect of the displaced activity along the edge of the
luscs (Kaiser et al, 2006). Using an extensively validated plaice box. The overall production of benthos wi thin the
body-size-based model (Hiddi nk et al. 2006), Hiddink et plaice box increased between 1.5 and 2 times compared
al. (20 0 8 ) were able to mo del the response of the ben- with that outsi de. How ever the production of smaller soft-
thi c community to the removal of the direct distu rbance bodied fauna (the preferred food of plaice; Hinz et al.
caused by large beam t rawlers within the plaice box, and 2006) was twice as high outside the plaice box. As plaice
 4.5 Human impacts on secondary production
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
abundance is positively correlat ed w ith prey biomass, Hid-
dink et al. (2008) concl uded that plai ce aggregate most
in the areas outside the plaice box where th e pro duct ion
of their preferred prey is higher. However, fish such as
cod Gadus morhua and haddock Mefanogramm u5 aegle-
4.5.2 Eutrophication
Eutrophication (see Chapter 16) can have positive effects
on secondary production through an increase in primary
production. In some areas of the Baltic Sea, macrobe n-
thic production seems to have doubled as a response to
eu trophication (Diaz & Rosenberg 2008) . Eutroph ication
of coastal waters is viewed as an undesirable state because
it can lead to hyp oxia and blooms of toxic algae. Conse-
quently many countries h ave invested in water treatment
and management practices to reduce the inputs of nitrates
and phosphates (nu trients) from terrestrial to marine sys-
tems. Where this has been successful, the recent reduction
in the flux of nitrate and phosphates to some coastal seas
seems to have had a negative impact on the productivity
of coastal shr imp and fl atfish fisheries (Rij nsdorp & van
Leeu wen 1996 ). Howe ver, whe n large phytopl ankton
blooms di e off and sink to the bottom, dissolved oxygen
levels in bottom waters drop due to microbial breakdown
of these algae. When dissolved oxygen levels fall below 2
ml 0 2 1-1 benthic fauna start to show unusual behaviour
such as abandon ing their burrows, prob ably because oxy-
gen levels in their burrows drop faster than those in the
water column. When these animals leave their bu rrows,
they become available to epibent hic predators that can-
n ot normally extract deep -burrowing shrimp, clams, and
worms from the sed iment. Mild hypoxia can therefore
temporarily increase the e nergy flow to the mobile preda-
tors in the ecosystem by generating a pulse of energy when
the animals in lower t rophic levels become stressed due
to hypoxia (Fig. 4.10) . Th is does not always happen and
it is only w ith in a n arrow range of cond itions that hypoxia
facilitates secondary pro duction of mobile predators.
Severe hypoxia culminates in mass mortality of fish and
bent h ic invertebrates when dissolved oxygen levels fall
below 0.5 ml 0 , 1-1 (hypoxia, Diaz & Rosenberg 2008).
Areas that are exposed to long periods of hypoxia h ave
a low secondary production and no benthic macrofauna.
Benthic secondary production in Chesapeake Bay (USA)
is estimated to h ave been reduced by S%, while secondary
production in the Baltic Sea h as been reduced by 30% due
to hypoxic events.
finnus that feed on large invertebrates may be negatively
affected by bottom traw ling in two ways. Fi rst, exp loitation
reduces th e populat ion size of the fishes and, second, the
pro duction of the large invertebrate s that these fi sh feed
on is severely reduced by bottom traw ling.
100%,...--;c;-;-.,-;:--
Mild periodic
- - - - - - - ----, 0%
Energyto Energyto
mobile Severe microbes
predators seasonal
Persistent
0% L --=::::~....: 100%
Figure 4 .10 Conceptual v iew of how hypoxia alters
eco system energy flow. The green area indicates that the
majority of energy is transferred from the benthos to
higher-level predators under normal oxygen conditions.
As a system experiences mild hypoxia, there can be
a pulse of benthic energy to predators when benthi c
invertebrates that are normally not available to epibenthic
predators, leave their burrows. If oxygen co ncent rat io n
declines further, macrobenthi c and fi sh predation
decreases in importance and an increasing proportion of
benthic energy is tran sferred to microbes (orange to red).
From: Diaz & Rosenberg (2008).
4.5.3 Climate change
Climate change has an effect on the magnitude, timing, and
d istribution of primary production in the world's oceans.
This in tu rn is likely to affect secondary production. We give
one example here of the effect ofclimate on pelagic second-
ary production.
The North Atlantic Oscillation (NAO) is a climate indica-
tor that indicates the speed and direction of the westerly
winds across the North Atlantic and winter temperatures
on both sides of the Nort h Atlantic (see Chapter 7) . The
secondary production of the copepod Calanusjinmarchicus
in the North Atlantic is strongly affected by the NAO. Fluc-
tuations in abundance of C. finmarchicus can be explained
by the effect of the NAO on spring primary production and
temperature (Fromentin & Planque 1996). C.jinmarchicus
was more abundant in years with low water temperatures
and a high primary production, which were found in years
 Chapter 4 Secondary Production

w ith a low NAG index. Copepods are the main food source
for the larvae ofmany commercial fish. and climate change
is therefore likely to affect the production of planktonic food
for fish larvae. which determines the recruitment success
and consequently the fishery landings. Although there are
other copepod species (Calanus helgolandicus) upon which
the fish can feed, the species that have replaced G.finmarc-
hicus in the community are less energetically rewarding
prey d ue to their smaller body-size.
This example show that changes in the climate may alter
the spatial distribution of primary and secondary produc-
tion. This may place an additional stress on fish popula-
tions, many of which are already over-exploited. It seems
inevitable that marine top predators. such as fish. seabirds.
and marine mammals will need to adapt to a changing
level, timing, and spatial distribution of secondary produc-
tion as a result of climate change.

Chapter Summary
• Secondary production is the production of biomass by heterotrophic organisms, such as inverte-
brates an d fish. The amount of secondary production in an ecosystem therefore defi nes how much
of the primary production is converted into heterotrophic biomass and how much food is available
fo r higher trophic levels.
• The quantification of secondary production is important for understanding the energy flow in food
webs and carrying capacity of ecosystems.
• The production-to-biomass ratio (PIS) describes how much biomass is produced by the standing
stock of biomass per year. PIB of organisms is correlated to their life history and body size. PIB
of large organisms is low, while the PIB of small organ isms is high.
• Secondary production can be estimated using several methods, including cohort-based methods
and allometric relationships between body size and PIB. Cohort-based methods are more precise
but req uire more effort.
• Apart from body size, the magnitude of secondary production for a species depends on the primary
production in the ecosystem, the trophic level of the species and the transfer efficiency of energy
between trophic levels. Secondary production is high in ecosystems with a high primary production,
and higher for organisms that feed at low trophic levels.
• More food is available for small, low trophic-level organisms than for large, high trophic-level organ-
isms. As a result of this, marine ecosystems have a typical size structure with many small organisms
and fewer large organisms.
• Human impacts such as fisheries, eutrophication, and climate change generally have a negative
impact on secondary production.

Further Reading
Van der Meer (2005) and the website of Brey (200B) describe in detai l how to measure ene rgy flow in
food webs and how to estimate secondary production using several different methods. The webs ite by
Brey contains a wealth of information, and a range of computation spread-sheets that have been set up
to allow easy estimation of secondary production, and empirical models for the estimation of production,
PIB, mortal ity, and other parameters. Je nnings et al. (2001) d iscuss the linkage between primary produc-
tion and fishery landings.
• Brey, T. 2008. Population Dynomics in Benthic Invertebrates. A Virtuol Handbook, Version 0 1.2 , (http:/ /
www.thomas-brey.de/science/virtualhandbook/navlog / index. htmll ' Alfred Wegene r Institute for Polar
and Marine Research , Germany.
• Jennings, S., M, J. Kaiser, & J. D. Reyno lds, 200 1. Chapter 2, Marine eco logy and production processes.
In: Morine Fisheries Ecology, Blackwell Publishing, Oxford.
• Van der Meer, J. 2005. Measuring the flow of energy and matter in marine benth ic animal popu lations.
In: A. Eleftheriou & A. Mcintyre (eds). Methods for the Study of Morine Benthos. Blackwell Science,
Oxford.
Part Two

5
6
7

8
9
10 - - ..
11

12 •
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Estuaries
Chapter Summary
Estuaries represent th e great transit ion between freshw ater
and marine biomes, and as such they are influenced by both
aquatic realms, yet they have a di stinct, except ionally vari-
able, and fascinating environment and ecology of th eir own.
The perception of estuaries as low diversity, muddy, and
inhospitab le places is misgu ided and stems from a narrow
appreciation of th e est uari ne system. Due to th e incred ibly
varied conditions present in estuaries th ey are inhabited
5. 1 Introduction
5.1.1 What is an estuary?
An estuary is commonly thought of as the place where a river
meets the sea, but this intera ction of the two major aquatic
realms results in a wide variety of systems of which a n estu-
ary is just one type. However, while most people wo uld not
h ave trouble picturing what an estuary looks like. providing
a definition of what exactly an estuary is has proved excep-
tionally difficult. Over 40 definitions of an estuary have so
far been attempted. using a range of crite ria such as dilu-
tion ofseawater, tidal regime, and geomorphology. Salinity
levels traditionally have been used to define estuaries. but
h ave perhaps led to a focus on the role of salinity at the
expense of other environmental and biological variables.
as will be explored later. Additionally, such definitions can
produce anomalies. an extreme example being the Amazon
estuary. In the Amazon estuary. tidal influence extends 735
km from the estuary mouth. but due to the vast river flow
there is no significant seawater penetration into the estu-
ary. while mixing of river and seawater is still evident 1000
km seaward of the river mouth. Tidal influence, however. is
extreme ly important in defining the difference between, for
by a wi de range of invertebrates, often in very high num-
bers, and are vital nursery syste ms for fi sh and feedi ng
grounds for birds. They have also been referred to as the
most degraded habitat type on earth, so they are perhaps
the finest example for st udying the conflicts between ecol-
ogy, co nservati on, and human use. Such st udy, however,
requ ires a broad knowl ed ge of th e ecosystem of an estuary
and how it functions as a w hole.
example, deltas and estuaries. and consequently the ecol-
ogy of these systems. The following definition seems to be
the most suitable for the global study of estuarine ecology
and highlights how potentially limited much of the research
on estuaries has been . The vast m ajority of work has been
concentrated in the middle regions of temperate systems ,
resulting in a rather narrow percept ion of estuarine ecology
that pervades their study.
An estuary is an inlet ofthe sea reaching into a river valley
as far as the upper limit oftidal rise, usually divis ible into
three sectors: (1) lower, free connection with the open sea;
(2) middle, subject to strong salt and freshwater mixing;
(3) upper, characterized by fresh water but subject to daily
tidal action.
Defining the upper and lower limits of estuaries can be
difficult, particularly if specific levels of salin ity are used
as a guide. In unmanaged estuaries. from our defi nition,
the upper boundary of an estuary can be considered to be
the limit of daily tidal infl uence, whic h m ay be truncated
in urban estuaries by the construction of barriers suc h as
weirs. In this case, the upper limit of the estuary will always
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

be fixed spatially regardless of fiver flow or tidal incursion.

The outer limits of estuaries are much more difficult to Box 5.1: Past sea-level rise
define. Large rivers produce a plume of reduced salinity
water far out into the open sea. Hence, fixing the outer limit There is much current concern about the conse-
of the estuary as the location where the dilution of seawa- quences of global warming induced sea-level rise
ter is no longer measurable can be unhelpful. In practice, (see Chapte r 14), but there have been dramatic
the boundaries of most estuaries tend to be subjectively changes in global sea-level during the last 1.8 mil-
defined by coastal morphology or management criteria (if lion years that have moulded many of the marine
an agency only has jurisdiction to 3 nautical miles from the systems we have today, such as coral reefs and, in
coastline, this is often used as a cut-off point). What is clear particular, estuaries. Many temperate estuaries were
is that an estuary is not an isolated entity and any consid- completely covered with ice only 17000 years ago,
eration of estuarine ecology needs to place the system in a while most others did not exist as we know them
continuum from the river to the sea. Both of these major due to the lower sea-level. Consequently, estuaries
aquatic biomes have strong and controlling influences over have successively appeared and disappeared as part
the ecology of estuaries, as shall be seen in this chapter. of coastal systems. Following the retreat of the last
(Weichselian) glaciation during the Holocene, sea-
levels rose rap idly, around 20 m in 2000 years, as
5.1.2 Evolution of estuaries the ice melted and changed the face of Earth's coast
Estuaries are very different from many other marine sys- (see figure). Around 6000 years ago sea-level was
tems in that they are ephe meral over geological time, more similar to current levels, but there have been
particularly in temperate regions where they have been minor sea-level variations over this time, which can
successively influenced by the process of glaciation. They be detected, for example, in estuari ne saltmarsh sedi-
are also areas of high sediment deposition, so through time ments.
can demonstrate a degree of infilling and success ion. At
Thousands of years ago
such time-scales, they are therefore more similar to lakes
0 ,
5
-- ---- ,
10
,
15
than other marine systems . At the height of the last glacia-
tion (17000 Before Present, BP), sea-level was over 130 ----,
m lower than it is now (Fairbridge 1980) ; the retreat of
,,
,,
the ice sheet resulted in a comparatively rapid elevation of ,, Postglacial
.,,- ,,
sea-level (Box 5. 1) . This initiated flooding of the exposed ~
~
sea level
,,
continental shelf (for example, the Nort h Sea, which was -'"
0;
E
·50 c- ,, me
eit her dry or a freshwater lagoon) and eventually the inun- ~ ,,
dation of river valleys by 6000 BP when modern estuaries
were created . Consequently, the majority of the world's
-
c
~

~
>
"is
,,
,,
0; ,
,,,
~
estuaries are exceptionally new systems in geological and
evolutionary terms, which has sign ificant consequences for ,,
their colonization, diversity, and ecology. -100 c- ,,
,
, ,
--,-......
5.1.3 Classification of estuaries 5 10 15
Thousands ofyea rs ago
A problem contributing to the difficulty in defining estuar-
ies is that, globally, there is a wide range of estuary types,
demonstrating large differences in geomorphology, tidal Change in relative sea level over the last 15 000
range, and salin ity characteristics. Consequently, a range years.
of classification schemes has been devised in order to pro-
vide a comparative framework for the study of estuarine
systems .
A popular way of classifying estuaries is to use their but have a shallow sill at their mouth formed from glacial
topography (Fig. 5. 1), which has arisen in general from deposits. This limits the exchange of seawater and thus
their method of formation following post-glacial sea-level circulation wit hin the fjord. Consequently, despite their
rise. Coastal Plain estuaries (Fig. 5. 1a), which tend to be spectacular appearance, fjords can have quite anoxic basins
the most common and familiar, result from the flooding of and few organ isms living w ithin their depths. Estu aries
river valleys following eustatic sea-level rise, as do fjords can also be created by offs hore deposits, forming barriers
where flooding res ults in deep-sided estuaries formed across bays and inlets into which rivers flow. These barri-
from glacial V-shaped valleys. Fjords tend to be very deep, ers, which can be joined to the coast (longshore) or out to
 5.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 5.1 Examples of three d istinct types of estuary based on method of formation. (a) Chesapeake Bay, USA, a
coastal p lain estuary. (b) San Francisco Bay, USA, a tectonic estuary. (c) Great South Bay, Long Island, USA, a bar-built
estuary (Photos: (a, c) NASA, (b) USGS).

sea (offshore), restrict the flow of seawater, allowing the
build up of diluted water in the resulting bay and form an
estuary. These are known as bar-built estuaries (Fig. 5.1c)
and. as in the case of the south-east of the United States. can
be extensive features of the coast. Further deposition can
result in the estuary being cut off in dry seasons resulting
in what is known as a blind estuary. Finally, estuaries can
be created by a completely different mechanism: isostatic
variation. in areas of tectonic activity. The classic example
of land sinking, flooding the valley, is San Francisco Bay
(Fig. 5.1b). The San Andreas fault-line runs adjacentto San
Francisco. with a history of tectonic activity. A past large
earth movement lowered the land seawards of the fault.
enabling the Pacific Ocean to spill overthe entrance (where
the Golden Gate bridge is located) and into the basin we call
San Francisco Bay.
Change in sea-level can be either eustatic, due to varia-
tions in volume of the ocean, or isostatic, due to varia-
tions in the level of the land (see also Chapter 8).
While such a classification on topography is perhaps the
most obvious method of defining estuaries. it has little real
ecological relevance in terms ofthe conditions provided for
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

associated organ isms, except on a broad biogeographical
scale. For example, fjords tend to be boreal, whereas blind
estuaries are more prevalent in tropical regions. Estuaries
have therefore also been classified in terms of tidal range
(Box 5.2) , a factor that has huge consequences for the
dynamics and ecology of estuaries and wh ich, for example,
makes them separate from brackish water seas. Globally,
estuaries demonstrate a wider range of tidal amplitude
than other marine systems, ranging from less than a metre
in many tropical systems (e.g. Vellar estuary, India) to over
16 m in the Bay of Fundy, Nova Scotia, Canada (Fig. 5.2) .
The scale of water movement into estuarine systems can
be huge . The tid al prism (the difference in the volume of
water in an estuary between high and low tide) of the Bay
of Fundy is estimated to be 100 billion tonnes! Four catego-
ries of estuary, therefore, have been suggested depending
on tidal range: microtidal «2 m range) , mesotidal (2-4
m), macrotidal (4-6 m) , and hypertidal (> 6 m) . The tidal
range in estuaries can be artificially enhanced by urbaniza-
tion through a combin ation of encroachment and flood
defence. A classic case is the Thames estu ary in central
London, where the channel has been narrowed through
centuries of construction to a third of its width in Roman
times; the tidal range at London Brid ge is now over 10 m.
The high tidal range with in estuaries provides, however,
a major resource for the exploitation of renewable energy
(Current Focus).
Tidal mo vement is therefore a key indicative descriptor
of estuaries. However, tides have a greater importance by
varying a range of physicochemical parameters that in turn
affect organism function, survival, and distribution. While
organisms can adapt well to cons tant extre mes, such as
temperature, acute environmental variability is exception-
ally stressful. Due to this high level of variability, estu aries
are perhaps the most naturally stressful of all aquatic sys-
tems. Several key environmental parameters vary spatially
and temporally in estuaries and thus influence the organ-
isms that inhabit them.

Box 5.2: Explaining the tides (a very

simplified starting point ... imagine a
world with no land mass)
The daily movement of the tide is caused by the gravita-
tional pull of the moon. At anyone point in time, water is
pulled towards the moon forming a bulge that relates to
local high tide. Areas of the Earth perpendicular to the
line of the moon will experience low tide. As the earth
rotates, the bulge of water appears to move over the
earth surface, w here in practice the earth is moving below
the bulge. High t ide is therefore really one very large wave
movi ng over the earth's surface.
The size of high and low t ide varies over a range of
time-scales. The most familiar is the monthly cycle of
spring and neap t ides. As the moon orbi ts the Earth,
its position relative to the sun changes (resulting in the
phases of the moon) . When the moon and sun are in align-
ment, thei r g ravitational pull is complementary, resulting
in higher raising forces and therefo re greater high tides
and subsequent lower low tides (see figu re). When moon moves closer to the earth, result ing in greater gravitational
and sun are perpendicular to the earth, the pull of the sun pull. The relat ive distances and positions of moon and
coun teracts, to a small degree, the gravi tational force of sun result in long-term t idal cycles, such as the 18 .6-year
the moon resulting in low amplitude (neap) tides. In addi- lunar nodal t ide (reflected in tree rings, for example) up to
tion to the spri ng-tide cycle, there are much longer t idal an 1800-year cycle that has a strong influence on global
patterns. The moon's orbit is not consistent, so at times it climate (Keeling & Whorf 2000) .
 5.1 Introduction

Current focus: using the tide to
generate renewable energy
If CO2 levels in the atmosphere are to be reduced in order
to combat global climate change, there has to be a move
from burni ng fossil fuels to other energy-generati ng meth-
ods that are more sustai nable or release no carbon or
other greenhouse gases to the atmosphere. The marine
environment provides a maj or energy resource in terms
of wave, wind, and tidal stream power, and extensive

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Figure a - Severn Tidal Power Group ! David Kerr

Figure b - Photog raph : © La mediatheque EDF / Yannick Le Gal
Figure c - Photog raph: Open Hydro
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
research and development is underway in order to dis-
cover the most efficient w ay of harnessing this huge sup-
ply of 'free' energy. Wind and wave energy generation
relies, to some deg ree, on the prevailing weather condi-
tions, but tidal movement is predictable and consistent
(see Box 5.2), so may well be one of the key renewable
energy sources to focus on.
Tidal stream varies consi derably aroun d the world,
from practically tideless seas, such as the Baltic and
Black Seas (see 5.5. 1), to the vast tidal move me nt
present in some temperate estuaries an d inlets, in par-
ticular the Bay of Fundy in Nova Scotia, Canada, and the
Severn Estuary in SW Britain (5.1 .3 ) . Here the rate of
water movement on flow ing and ebbi ng tides is hig h
enough to potentially gen erate significant amou nts of
electrici ty; current speeds in t he Severn can be up to
4. 1 ms'" . with a t idal range of up to 14.6 m (Carling et
al. 2005), whilst the volume of water entering the Bay of
Fundy each t ide is greater than all the rivers in the world.
Plans to harness the resource from the Severn and Fundy
have been discussed for decades, but more recently their
potential has been taken more seriously as governments
look to exploiti ng thei r renewable resources.
In the Severn, plans have generally focused on building
a barrage across the estuary to generate energy (figure
a) , trapp ing w ater from higher up the estuary and pass-
ing it th rough turb ines on the ebbing tid e-a large-scale
version of 'ti dal mills' present in Europe from the twelfth
centu ry. The UK Sustain able Development Comm ission
(h ttp://www.sd-co mmissio n.org.uk/p ag es/tid al-powe r.
htm l) has undertaken maj or reviews in barrage construe-
5.1.4 Important environmental
variables
Salinity
Classically, salin ity h as been considered to be the dom i-
n ant influence on the survival and distribution of estuarine
organisms due, perhaps, to it being the most obvious vari-
able that defines an estuary. While the role of salinity m ay
have been over played in the past, it is still one of the most
important factors that affects organisms and demonstrates
a wide variation within estuaries. This variability has two
components. First , there is spatial, longitudinal va riability,
salinity ranging from 0 at the river end to around 34 at the
mouth. In tropical estuaries, evaporation can cause salinity
levels to exceed those of seawater (see 5.5) . However, the
most important aspect of salinity variation that defines tidal
estu aries is that salinity at anyone point varies consider-
ably over time. With ever y tid al cycle, an organism could
t ion , concludi ng that a Severn Barrage could produce
4 .4% of the UK's electricity needs and last 120 years,
thus providing a major and reliable renewab le contribu-
t ion. At maximum stream it could generate 15GW of
peak power, equivalent to three nuclear power stations
(Renewable Energy Centre 2007). However, there would
be major local impacts on the system above the barrage,
wi th a potential loss of 75% of intertidal habitat , large
changes in the sedi mentary and production regime as
cur rents are reduced and light penetration increases (Fal-
coner et al. 2009), and rest rictions to migrating fish. Only
one commercial-scal e tidal barrage is currently opera-
t ional, though at a much smaller scale to that proposed
for the Severn: La Rance Tidal Power Plant in Brita nny,
France (8 m tide; figu re b), which was constructed in
the 19 6 0 s, can produce 4% of Bri tanny's power, and
has long since recovered the cost of construction. In the
Severn, ou r decision is whether the wide, long-term envi-
ronmental benef its of barrage construction outweig h the
local impacts to the system: a real conservation dilemma.
In the Bay of Fundy, barrage const ruction is more dif-
ficul t and here the installation of smaller-scale underwa-
ter tu rbines has been proposed (figu re c), the first test
device being deployed in November 2009 by Nova Sco-
tia Power in the Minas Passage part of the Bay system.
This uses the Open Hyd ro Open-Ce ntre Tu rbine (http://
www.open hyd ro.com/technology.html). which is simple
and reliable for the tough conditions of Fundy and has
its b lades covered to minimize impacti ng marine ani-
mals. Potenti ally, large arrays of such devices could be
deployed in t idal streams.
potentially be exposed to near fresh water at low tide and
near marine conditions at high tide. In the mid-Ythan estu-
ary, Scotl and, salinity ranges from 3 to 29 over a tid al cycle.
Salinity is now presented as a dimensionless measure
known as Practical Salinity Units (P5U). It is unitless when
presented , i.e. just the number.
However, such dramatic variation between low- and
high-tide saliniti es is only indicative of the mid -estuary
area, salinity range decreasing cons iderably towards both
ends of the estuary (Attrill 2002 ; Fig. 5.3). The salin ity of
water trapped in the sediment of intertidal areas (intersti -
ti al water) is much less variable over a tidal cycle «2 in
the Ythan) , the sed iment filling with heavier seawater, the
lighter freshwater flowing over the surface of the sediment.
In addition , m any intertidal areas will not experience low-
salin ity water as they are exposed by the receding tide. The
 5.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 5.2 Extreme t idal range in the Bay of Fundy, Nova Scotia. The two pictures were taken 4 h apart, a student is
circled at the water's edge in the second photo (photographs: Martin Attrill).

Salinity profiles
salinity of interstitial water in subtidal sediments appears A

~'\ "
to be more similar to that of the overlying water. Salinity Fresh
levels can also vary seasonally due to changes in freshwater •
Selt
flow. This aspect of temporal salinity variation in estuar- • limited mixing zane---f
ies has been comparatively overlooked, but can have dra- A
matic implications for the ecology of estuaries (see 5.2.3) .
Surface
However, freshwater flow rates affect the current speed of
Solt wedge effect. Alargesnlume of sea water in relation
river water entering the estuary, and the way freshwater to freshwater run-off produces thewedge effect, 05 the see Depth
reacts with saltwater entering with the rising tide, together water dams bock the freshwater. Typical rertiml salinity
with the topography of the estuary, can produce estuaries profile is givenfromA-A. 8ottom
0
Salinity
as
of different vertical salinity structures. This has allowed an
alternative classification ofestuaries based on their salinity
profile. A variety of types has been defined, but basically [ - ~

A
- J
depend on how well mixed the two water sources become, Fresh
, I-I-- I ' "
and these can vary over tidal cycles and with seasonal input I
Selt
offreshwater (Fig. 5.4) . •
While salinity variation is an inherent feature of estuar- A
ies, it is not necessarily the only important stressor influ-
encing organisms. Three other factors can potentially have Surface
equally significant roles on the ecology of estuaries.
Two-layer flow. Alarge vol ume 01 freshwater in relation to see Depth
water produces a 2-layer flowwith outgoinglreshwaterflowing
18 oser incaming salt water. Typicol5alinity profile fro mA-A i5sheen, ,"". 0
Salinity
ss
16

14
0 --- - -- ~ ~

-- -- ~

~
~ 11 A

-c
c
10 • •
""- ,
c
c
c
c
S,II (
) Fresh

~
6 ,
'" A
4 »>
1 Surface

0 10 10 3D Depth
Mean mid-tide salinity Well mixed estuary. Patternsofflowand estuary topography
result in evensalinity cmss thevertical profile(A-A) ,"". 0
Salinity
as
Figure 5.3 Salinity range along the length of an estuary,
in this case the Thames. Figure 5.4 Stylized salinity profiles of estuaries.
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Sediment
Perhaps the most recognizable features of estuaries are the
expansive intertidal mudflats composed of soft, fine, grey
silt, extremely difficult to walk over (Fig. 5.5) and giving
off a distinctive sulphurous odour when the sedime nt is
disturbed. This fine, mobile sediment is a highly difficult
habitat to colonize. There are no points of attachment for
-
macroalgae or sessile organisms, while organisms intoler-
ant of mechanical disturbance wo uld not be able to deal
wit h the mobility of the substratum. Addit ionally, the fine
particles can easily clog delicate feeding and respiratory
structures, and the sedime nt makes locomotion difficult
(Fig. 5.5). It has therefore been suggested that organisms
that thrive in estuarine mudflats need to be more adapted
to the sediment than to the salinity variation (Barnes 1989) . Figure 5.5 Extensive mudflats are characteristic of most
However, despite being symbolic ofestuaries, under normal estuaries, the wide expanses of mud exposed at low tide
cond itions, large fine-grained mudflats only tend to form in being rich in organic material and difficult for organisms,
the middle reaches of the estuary and are comprised mainly and marine biologists, to move over (photographs: Martin
of marine-derived material, even though they may be many Attrill).
kilometres from the sea. The deposition of sed iment in an
estuary is mainly due to comparative tidal and river current ally rich in fine organic material that has settled out with
speeds (Box 5.3), although the highest suspended sediment silt particles in the water column. Consequently, estuaries
conce ntration tends to be further up the estuary (the turbid- have one of the highest levels of secondary production in
ity maximum) due to a dynamic interaction between fresh aquatic systems (see 5. 3 and Chapter 4). If a deposit-feed-
and saline water (see Dyer 1997) . Conseque ntly, sedime nts ing organism can tolerate the extremely stressful conditions
near the mouth and heads of estuaries tend to be much more prevalent in a mid-estuary mudflat, then growth rates and
coarse, as tidal and river flows are great here, thus prevent- production can be extre mely high due to the quantity and
ing settlement of finer particles (see also Chapter 8) . qu ality of ava ilable food.
The extens ive mudflats found in estuaries are exception-

Box 5.3: Sediment deposition in a very simplified version of sedimentation in estuaries,

estuaries which is further influenced by many factors, such as salin-
Estuaries are typically associated with extensive banks of ity structure, local topography, and tidal movement, etc.,
very fi ne mud, but these only really occur in the middle but provides the general, large-scale pri nciples. For full
of the estuary and are mainly composed of marine sedi- details see Dyer (1997).
ment. How do they for m he re, often tens of kilometres Due to the large amou nt of suspended material, estu-
from the sea? Sediment deposition is related to current aries are naturally turbid. In the 19 60 s the Kinks sang
speed-when tide or river cu rrents are fast they can hold about the Thames being a 'dirty old river'- this may have
on to much of the ir sediment. However, in the middle been the case at the t ime, but now th e comparatively
estuary, river and t idal cu rrents meet and slow down, unpolluted estuary still looks dirty due to the high natural
the reduced velocity allowing suspended solid load.
the settlement of the finest silt
particles carried in the water. Reduced velocity
As either river or t ide slows as
it moves along th e estuary, suc-
cessively smaller particles settle
out, creati ng a distinct sediment
Gravel Sa nd Silt Silt Sand Gravel/shell
profile (see figure). Gene rally,
tidal movement is much greater in
Gravel Sand Silty mud Sand Gravel/shell
terms of volume than river input,
so the mid-estuary mud is mainly •
of marine origi n. This is clearly Estuarinesediment profile

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Dissolved oxygen
Very few aquatic systems have naturally low levels of dis-
solved oxygen (DO) and appropriate oxygen levels in water
are vital to sustain life. Both estuarine waters and sedi-
ment have extremely high levels of organic material (see
5.3 .1), so consequently have very high levels of bacterial
activity. Aerobic bacteria dominate the breakdown of mar-
ter in estuarine waters. and consequently use up dissolved
oxygen in the process, resulting in reduced oxygen levels
in mid-estuary water. Oxygen levels tend to be normal at
the head and mouth of an estuary, so a longitudinal profile
of DO would show a notable dip in the mid-estuary. This is
known as a DO sag. Oxygen removal is more severe from
interstitial water in mudflats. The fine nature of the sedi-
ment prevents re-aeration by diffusion. Hence. below the
surface of the mud. bacterial action removes oxygen. with
subsequent breakdown of matter undertaken by anaerobic
bacteria. This process results in potentially toxic by-prod-
ucts, such as methane (CH.) and hydrogen sulphide (H 2S),
the latter having the effect of turning the mud black and
producing the 'rotten eggs' smell. This is a natural process in
estuarine mud (it would occur in unpolluted estuaries) and
adds a further physiological stress for organisms attempting
to live in mudflats.
Generally. the level of oxygen removal from estuarine
water will not have a dramatic effect on the associated biota;
however, many estuaries worldwide have been favoured
places of human settlement, with large cities having been
constructed on their banks. Human activity (e .g, sewage
disposal) can supplement the amount of organic matter in
the estuary and thus stimulate excessive removal of oxy-
gen by bacterial action. In extreme cases (e.g. the Thames;
Attrill 1998). estuarine waters can become exceptionally
depleted ofoxygen, with dramatic and severe consequences
for the ecology of the system (see also Chapter 15). The
naturally low level ofoxygen in mid-estuarine water makes
it exceptionally vulnerable to human impact.
Temperature
Temperature does not vary greatly over a tidal cycle and
changes in temperature longitudinally are fairly minimal.
However, in higher latitudes. seasonal patterns in tem-
perature change can be the major trigger for migration and
reproduction of estuarine organisms, particularly mobile
species, such as fish and large crustaceans (see 5.2.2) . This
influence of temperature can be more important than salin-
ity variation. so needs to be considered as a major environ-
mental factor in estuarine ecology. Temperature can also
influence the speed of microbial breakdown in estuaries.
Bacteria process organic matter much faster in the tropics
or during the summer in temperate systems. This has con-
sequences for DO levels and temperate urbanized estuar-
ies are more vulnerable to severe DO sags in summer than
in winter. Human activity can also affect the temperature
5.2 Estuarine organisms
of estuaries, with knock-on effects for oxygen levels; for
example, the discharge of warm water effluent from power
stations. It has been estimated that at the height of power
station activity, the water temperature in the Thames Estu-
ary was raised by over 3°e.
The conditions within. and surrounding. estuaries are
directly linked to human activity. Few. if any. estuaries in
the world could be regarded as totally free from human
influence, whether this is an impact on the water quality of
the system, interference from fisheries and aquaculture. or
more commonly modification of the surrounding bankside
environment. Therefore, estuaries arguably represent the
most anthropogenically degraded habitat type on earth, a
factor that must be kept in mind when investigating their
ecology (Edgar et al. 2000) .
5.1.5 Division of estuaries into zones
To enable further sub-classification of estuaries, they have
been traditionally divided up into zones reflecting the over-
all environmental conditions apparent in that particular
region. Several schemes have been devised, generally based
around salinity levels (e.g. the Venice system), but all are
subjective to a high degree and zones are hard to spatially
define in a dynamic system that is varying over tidal and
seasonal cycles.
A typical classification is as follows :
Zone 1: Head. Estuary dominated by river flow, salinity
generally < 5, strong river currents resulting in
coarse sediment of stones and gravel.
Zone 2: Upper Reaches. Main area of mixing of fresh and
saline water, salinity highly variable (e.g. 5-18),
currents can be negligible. resulting in fine.
muddy sediment in intertidal areas.
Zone 3 : Middle Reaches. Flows dominated more by tidal
currents. salinity 18-25. extensive intertidal flats
mainly muddy but with more sand present.
Zone 4 : Lower Reaches. Faster tidal currents. salinity
25-34. Sediment now mainly sand.
Zone 5 : Mouth. Where estuary meets the sea, strong tidal
currents and generally fully saline conditions.
Sediment clean sand with shell fragments, or even
rock in some cases.
5.2 Estuarine organisms
5.2.1 Origin of estuarine organisms
Estuaries are exceptionally new systems in geological
terms, particularly in temperate and boreal regions. There-
fore. they have been open to colonization by organisms only
since the retreat ofthe last ice age (5.1.2) . Tropical systems
potentially have been more stable through time, although
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

they will have been affected to some degree by sea-level
changes. The effective extinction of estuaries at higher
latitudes during the last glaciation event would have had
severe consequences for the fauna and there is much debate
as to whether brackish water conditions existed during this
period to act as refugia for estuarine organisms (Barnes
1994) . Three scenarios for the recolonization of estuaries
following glacial retreat are therefore possible.1flocal refu-
gia were present, then recolonization by similar suites of
organisms present prior to glaciation might have occurred.
Organisms mayhave remained in brackish water systems at
lower latitudes and recolonized using successively higher
latitude systems as stepping stones. Alternatively. some
species may have become extinct if no refugia existed, so
a third scenario is that organisms have evolved into estuar-
ies from suitable marine species during each post-glacial
period. Evidence is equivocal, although some estuarine spe-
cies recorded as subfossils are known to have disappeared
from the Northern European fauna after the last ice age. A
good example is the bivalve Mya arenaria (Fig. 5.6a; Box
5.4) . Barnes (1994) suggested that the diversity of very
similar Gammarus species (Fig. 5.6b) existing in brackish
water represents successive species evolving into estuaries
after each ice age.
Whatever the evolutionary pattern of estuarine coloni-
zation, estuarine organisms originate from two possible
sources:species of freshwater origin extending into estuar-
ies from rivers and marine species colonizing estuaries from
the sea. The dynamic. stressful nature of estuarine condi-
tions produces strong evolutionary selection forces. so spe-
ciation in such habitats is potentially rapid. Indeed, genetic
research on estuarine organisms, such as amphipods, has
revealed significant genetic differences between popula-
tions within the same estuary that are found in different
habitats (Stanhope et at. 1993).

Figure 5.6 Examples of estuarine species. (a) Mya arenaria, which became extinct in European estuaries during the last
ice age (photograph: Andrew Butko). (b). Gammarus roeseli, one of several very similar species of amphipod inhabiting
estuaries (photograph: Michael Manas). (c). The mysid Praunus Bexuosus, which has very advanced osmoregulation
(photograph: Kare Teines). (d). The ragworm , Nereis diversicolor, is one of the most successful organisms in northern
temperate estuaries due to its ability to colonize practically any salinity as long as mud is available (photograph: David
Samuel Johnson).

Box 5.4: Extinction and
reintroduction of Mya arenaria
Wh at happened to estuarine species duri ng glacia-
tion? Mollusc shells provide a clue. The common
estuarine bivalve Mya appeared to become extinct
in Europe during the last ice age, as its habitat dis-
appeared. It did not naturally recolonize from North
America, but most likely was reintroduced by human
movement across the Atlantic from the fou rteenth
centu ry. Subsequently, th e bivalve has spread through
brackish w ater in Europe, only reach ing the Black Sea
in the 19 60 5, and would be regarded by most as a
classic species of these habitats. Did other species
also suffer this extinctio n? We have li ttle evidence to
go on, but the fate of estuarine species during gla-
ciatio n and the subsequent method of recolonization
may be important in helping to understand diversity
patterns and speciation in estuaries.
t·
- Natural
- Anth ropogenic
The head of an estuary is dominated by organisms of
freshwater origin, with most freshwater taxa represented.
Insects generally do not penetrate far into estuaries, in par-
allel with the full marine environment, with the possible
exception of dipteran larvae such as the Chironomid ae.
The most abundant freshwater taxa in estuaries tend to be
fish (e.g. catfish in tropical estuaries) , pulmonate molluscs
(such as the Lymnaeidae) , and, in particular, oligochaetes.
These worms are extre mely successful colonizers of estu-
aries, wit h several species found only in the upper- and
mid-estuarine areas, often in vast numbers. The majority
of oligochaetes belong to two families: the Enchytraeidae
and the Tubificidae. In particular, tubificids can thrive
in estuaries wit h some organic enrichment, having been
recorded at densities of over 1 million m-2 in such mid-
estuary mudflats.
The maj ority of ot her common organisms that pen-
etrate far into estuaries are of marine origin, in particular
polychaetes, nematodes, crustaceans, fish (see 5.2.4) , and
5.2 Estuarine organisms
bivalve molluscs. Mudflats in the middle of an estuary will
tend to be inhabited by large numbers of polychaetes, oli-
gochaetes, and small crustaceans, in particular arnphipods.
In outer estuary areas, large beds of bivalve molluscs, such
as mussels and oysters, are not uncommon. In parallel wit h
the head of an estuary, examples of the majority of marine
taxa can be found in the outer estuary area. Other species
utilize estu aries during migration, either from freshwater
to the sea (catadromous species, e.g. the Chinese mitten
crab (Eriocheir sinensis), the eel (Anguilla angu illa)) or vice
versa (anadromous species, e.g. salmon species, such as the
chinook (Oncorhynchus tshawytscha )).
Plants are poorly represented below the high-tide mark
in estu aries, although huge plant-dominated areas exist
over the land-estuary transition, such as salt marshes (see
5.3.4 and Chapter 10). Few hard substrata are available for
algal attachment (apart from those of human origin), while
the turbid waters result in minimal light penetration and
restrict phytoplankton production. Benthic diatoms and
ephemeral green algae can colon ize the surface of mud-
flats (Chapters 2 and 3). The only large standing biomass of
plants in estuaries tends to be seagrass beds (Chapter 10),
which are usually restricted to the outer estuarine regions.
5.2.2 Responses of estuarine
organisms to environmental variation
A large su ite of species can be found along the full length
of an estuary, but comparatively few are able to exploit the
rich conditions present in the mid- or upper-estuarine mud-
flats due to the high degree of environmental variability
detailed in 5.1.3. Traditionally, the physiological ability to
respond to reduced salin ity has been seen as the key to the
survival of marine species in estuaries and determines the
realized distribution of any organism. A reduced salinity
in the external medium exerts an osmotic stress, resulting
in uptake of water by the organism, which has an internal
fluid concentration greater than that of the surround ing
water (hyp erosmotic). To prevent lethal dilution of body
fluid s, water uptake has to be mitigated or prevented by,
for example, active pumping of water or internal mo ve-
ment of ions. One might then expect that good powers of
osmoregulation would be a distinctive feature of all suc-
cessful estuarine organisms . In fact, they exh ibit a very
wide range of abilities to osmoregulate. Many organisms,
such as molluscs, have little, if any, osmoregulatory abili ty
and are thus termed osmoconformers. They survive and
thrive in estuaries by exhibiting exceptionally high toler-
ance to diluted blood concentrations, wh ich is sufficient
over most of their range in estuaries. At the other extreme,
crustaceans are amongst the most efficient osmoregulators .
Species such as the mysid Praunusflexuosus (Fig. 5.6c) are
able to maintain a relatively cons tant internal medium
across a very wide range of external salinities. Many other
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
animals fall between these two extremes in theirosmoregu-
latory ability. Some algae can also survive extreme salinity
variation; the green alga Ulva is perhaps the most tolerant,
changing ionic and metabolic concentrations in response
to variations in salinity. Estuarine Ulva also possess thinner
and stretchier cell walls than fully marine species, allowing
changes in tissue water content and cell volume.
An organism with blood concentrat ion t he same as the
external concen t ration is isosmotic, blood more concen-
trat ed than external is hyperosmot ic, blood less concen-
trat ed than the external medium is hyposmot ic.
Thus. while osmoregulation is clearly important to aid
survival of many species that encounter reduced salinity
conditions, considering this to be the major determinant
ofspecies distribution in estuaries is an over-simplification.
Organisms found in the most variable conditions within an
estuary are not necessarily the most sophisticated osmo-
regulators. but often simply the most tolerant. The major-
ity ofexperimental work on osmoregulation has considered
organism response to fixed salinity values, whereas organ-
isms in estuaries (particularly in subtidal areas) are sub-
ject to highly fluctuating conditions on a tidal and seasonal
basis. Therefore, an experiment determining the minimum
salinity at which a species can survive may have limited
application in the estuarine environment. Estuarine organ-
isms also demonstrate a marked physiological plasticity,
enabling them to adapt to different salinity regimes even
if they have minimal osmoregulatory abilities, such as the
mussel Mytilw; edulis (Tedengren et al. 1990). Effectively,
the majority of estuarine species are able to tolerate a wide
range of salinities. and while their absolute upstream limit
will be affected by their ability to deal with fluctuating,
reduced salinities (amongst other variables), their physi-
ological tolerance would generally be greater than that
experienced in the environment over their realized range.
Other environmental factors therefore potentially control
the survival and distribution of estuarine organisms on a
day-to-day basis, and research supports this:
• The distribution of many infaunal organisms is deter-
mined by the availability of mud habitat rather than
salinity levels (Barnes 1989) . The polychaete Nereis
diversicolor (Fig . 5.6d), for example, is found practi-
cally throughout an estuarine system wherever stable
mudbanks occur. As such a habitat is not found above
the upper estuary. Nereis is not present here. although
settling larvae (neochaetes) have been recorded from
samples in near freshwater conditions.
• The mysid Neomysis integer is an excellent osmoregula-
tor and is found across large parts of Northwestern Euro-
pean estuaries. However. avoidance of high flow areas
appears to be the key factor in determining its local dis-
tribution within estuaries. rather than salinity (Lawrie et
al. 1999).
• The shore crab (Carcinus maenas) is a classic estuarine
organism and an efficient osmoregulator. However.
modelling work suggests that salinity appears to be
unimportant in determining its movements and distri-
bution, with temperature the key factor (Attrill et al.
1999) . Below approximately 8°C the crabs become com-
paratively inactive. Dissolved oxygen concentration is
the only physicochemical parameter significantly related
to distribution patterns of the brown shrimp (Crangon
crangon) . Findings for both of these species are sup-
ported by other laboratory results.
• Temperature appears to be the dominant variable influ-
encing the movement and distribution of many estuarine
fish species (see 5.2.4) .
In summary. while an important environmental factor,
salinity should not necessarily be considered the major
influence over distribution patterns in estuaries. Overall
environmental variability is probably the limiting factor
for most organisms that penetrate estuaries. with other
environmental factors influencing their local distribution
and survival.
5.2.3 Impact of freshwater inflow on
estuarine organisms
Much focus on environmental variation in estuaries has
been on the short-term impact of tidal cycles. However.
conditions within an estuary vary over a longer, seasonal
time period, particularly in higher latitudes and in tropical
areas with seasonal monsoons. as the amount offresh water
entering the estuary varies considerably. Most organisms
respond to tidal variations in conditions by simply tolerat-
ing the variability for this short time period or by avoiding
contact with lower salinity water by burrowing. bivalves
closing their shells. or fish moving in and out of estuaries
with the tide. However. large changes in the amount of
fresh water entering the estuary due to increased. seasonal
precipitation can alter the conditions in anyone part of the
estuary quite dramatically (e.g. salinity; Fig. 5.7), changes
that are effective over much longer periods of time. This
influence of such variations in flow has generally been
neglected, despite the potentially large impact they may
have on estuarine ecology and the spatial distribution of
estuarine organisms.
Estuarine organisms can demonstrate three responses to
increases in flow. and subsequent large decreases in salin-
ity, particularly in the upper estuary where seasonal inputs
can lower the salinity to practically fresh water: either the
organisms tolerate the changes. they migrate or drift to
avoid low salinity water, or they do not survive at all. In
the first scenario. temporal samples of the community in
 5.2 Estuarine organisms
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

80 l1li0
abstraction of water; Fig. 5.8) resulted in the upstream
40 l1li0 movement of many sedentary species. Changes in the com-
•
•
16l1li0 munity at the very head of the estuary were even more
I
- 8l1li0 marked (Attrill et al. 1996). Despite very small changes
~ •
a t. in salinity (0.25) many species, particularly insects, disap-
.=. ••
~
0
u:
4l1li0
\:' . .
"", ..
peared rapidly from the community (Fig. 5.9) leaving a low-
1600
BOO \' .-.-.
..-. .... ... .
diversity assemblage of tolerant species. Traditionally, the
freshwater part of an estuary is considered to be the area
400
•
••
•• •
... .
• •.. •
•
••
< 5, but this study demonstrated that very subtle changes
• •• • •
• ••• • in the salinity regime can have dramatic consequences for
160 0 I 2 3 4 5 6 upper estuarine communities. Either species that inhabit
Salinity this area of the system are far more susceptible to salinity
variation than traditionally thought. or other factors asso-
Figure 5.7 The relationship between freshwater inflow ciated with variation in flow have large impacts on these
and salinity levels in an upper estuary. organisms.

an estuary would demonstrate few changes. whereas the Abst raction-the planned removal of water from riv-
latter two responses would result in the removal of the ers or lakes to supplement drinking supply. Generally
organism from the assemblage and possible shifts in com- water is pumped to reservoirs to maintain their level.
munityup and down the estuary. Clearly, long-term studies This action can dramat ically affect the amount of water
are needed to elucidate responses of organisms to seasona l entering estuaries.
flow changes. but unfortunately few such data sets exist.
In the Fraser River, Western Canada. flow is highly sea-
sonal but due to ice formation and melting in the Rocky
Mountains. Lowest flow rates into the estuary occur during
winter when water is locked up as snow in the mountains,
dramatically increasing over spring and summer as melt-
water flows to the coast. The responses of benthic inverte-
brates were recorded over this seasonal change (Cha pman
& Brinkhurst 1981) . There were notable patterns in organ-
ism occurrence at the more freshwater estuarine sites. with
freshwater species, such as the oligochaete Tubifex tubifex,
present in large numbers for much of the year, but absent
during winter when flow levels dropped. Similarly, the
freshwater species Paranais frici was replaced in winter by
a species more adapted to estuarine conditions, P. litoralis.
Populations of these highly sedentaryworms demonstrated
movements both up and down the estuary on a seasonal Figure 5.8 The impact of drought conditions on
basis. Similar changes to ranges within the estuary were estuaries-low tide in the Thames Estuary (at Kew) during
noted in the Thames, UK (Attrill & Rundle 2002), where low-flow conditions, with only a small freshwater channel
severe reductions in flow (due to drought conditions and evident (photograph: Martin Attrill).

1989 1990
Taxon 272829 3031 32 33 3435 3637 38 39 4045 3111620242628 3032 34 3638 40 42 4547 49
low-Row periods
leptoceridae
Caenidae
• •
• •• • • •
Unionidae
•
Erpobdellidoe -- • • - .. •- •
Corophiidae
•
:~~;~~~~~1111~;~5~
Figure 5.9 Disappearance of upper-estuarine
Hydraoorina
Ostracoda
Asellidoe •• • taxa following reductions in freshwater flow
Hydrobiidoe
Sphaeriidae • • into an estuary. The solid bars show when a
Chironomidae family of organisms was present, with the week
Oligochaeta number during each year along the top of the
Gammaridae
figure.
 Chapter 5 Estuaries
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Drought-induced changes in freshwater inflow can also primary production in the oligohaline zone. This higher
have large consequences for the water quality of the mid- production results in increased macrofaunal densities,
estuary, and subsequently impact the mobile organisms creating greater predation pressure on meiofauna and so
present there (Attrill & Power 2000a, 2000b) . Despite being reducing their numbers (see 8.3 .1 for organism size defini-
over 60 km from the river. low-flow conditions over a 4-year tions) . The impact of inflow on estuarine production was
period were shown to significantly affect a range of param- also apparent in a study of phytoplankton in the Swan River
eters in the mid-Thames estuary (including dissolved oxy- Estuary, Australia (Chan & Hamilton 2001), and led to the
gen. temperature. salinity) that are the major influences on conclusion that alterations to freshwater discharge can
mobile estuarine organisms. The long-term nature of this have a significant impact on phytoplankton biomass and
study (17 years) allowed the populations of mobile inver- species composition, with regulation of the dominant group
tebrates to be modelled and demonstrated significant shifts (e.g. green algae and diatoms) by inflow.
in their abundances and distribution patterns following the
onset of drought (Fig. 5.10) .
There is also evidence that different inflow rates can
5.2.4 Estuarine fish communities
have significant effects on the productivity of estuaries. Due perhaps to their relative ease of sampling, much work
Montagna and Kalke (1992) studied two estuaries in Texas, on the ecology of estuaries has focused on the inverte-
USA, which were very similar, apart from the size of the brates inhabiting the extensive intertidal mudflats. How-
river entering the system, providing a spatial comparison ever, estuaries also support a large fish biomass, which
of the effect of freshwater inflow. The Guadalupe estuary exploits the high levels of available food represented
had nearly 80 times the freshwater inflow than the Nueces by exceptional numbers of infaunal and mobile inverte-
estuary, and had a much higher macrofaunal density and brates. In parallel with invertebrate taxa inhabiting estu-
shellfish production, but a lower density of meiofauna. The aries, the fish fauna is represented by species originating
difference in production was explained by higher nutrient from both freshwater and marine systems. Only a few
input to the Guadalupe estuary via river flow that boosted fish species depend on estuaries for the whole of their

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200 400 ~o

Weeks from January I, 1977

Figure 5.10 Examples of models constructed for water quality and mobile invertebrates in the Thames estuary
demonstrated marked changes in seasonal patterns following the onset of drought.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Figure 5.11 Fish species living and breeding within estuarine systems: (a) the mummichog, Fundulus heteroclitus
(NOAA); (b) the smelt, Osmerus eper/anus, which strangely smells of cucumbers! (Markku Varjo/www.kuvaliiterLfi).
life cycle, however, and can be termed estuarine special-
ists. Examples include the mummichog (Fundulus het-
erod itus; Fig. 5 .11a) and the smelt (Osmerus eperlanus;
Fig. 5 .11b), the latter species laying its eggs in the upper
reaches of estuaries. In many northern temperate estuar-
ies, the three-spined stickleback (Gast rosteus aculeatus)
is common, a species more generally associated with
fresh water. However, the stickleback has only colonized
freshwater systems since the last ice age, spreading into
rivers from estuaries. Other fish species utilize the whole
length of estuaries during their life cycle. An example is
the flounder (Platichthy s flesus), the post-metamorphosis
juveniles inhabiting the very top of the estuary. extending
into rivers. As flounders grow they move down to the main
body of the estuary, where they spend most of their life,
and tend to migrate to the sea to spawn. Many marine fish
species exploit the rich environment of the mid-estuary
by undertaking migrations in and out with the tide . An
example is the grey mullet (Chelan labrosus), which fol-
lows the tide into even small creeks. Unlike most fish spe-
cies in estuaries, however, Chelon is principally a grazer.
feeding off diatom films on the mud surface and leaving
distinctive feeding traces in the mud.
Probably the most important role of estuaries for fish
species is. however, as a nursery ground for marine spe-
cies, one fourth of all fish species in the Virginia/Carolina
region of the USA being estuarine-dependent (Ray 1997).
The majority of fish found in temperate estuaries are
juveniles within the first two years of life . Vast numbers
of such fish can move into temperate estuaries at certain
times of the year (particularly winter), utilizing the high
food supply and the generally less harsh, warmer condi-
tions than present in the open sea. The high turbidity of
estuaries may also provide a certain level of refuge from
visual predators. Therefore, estuaries are exceptionally
important in providing recruits to many coastal fisheries
(see Techniques box) . Seasonal use of estuaries by fish also
occurs in tropical regions, here dominated by wet and dry
seasons. While these systems are much less studied than
5.2 Estuarine organisms
temperate areas, higher densities and species' richness
have been recorded during the rainy season. Like inverte-
brates. the overall salinity regime can influence the longi-
tudinal distribution offish species, but their comparatively
high tolerance to a range of salinities, coupled with their
motility. enables them to avoid unfavourable conditions;
salinity therefore appears unimportant in determining the
usage patterns of estuaries by fish . The majority of large-
scale studies have concluded that water temperature is
the most important parameter related to the distribution
of fish over the year. initiating migration movements. for
example. However. other parameters are also highly influ-
ential for certain species and at a more local level. Ade-
quate dissolved oxygen levels are vital for fish survival in
estuaries, and historically pollution-induced low DO levels
have reduced, or completely eliminated. the nursery roles
ofestuaries such as the Tyne, northeastern England. Some
fish species may also follow their prey. For example, whit-
ing (Merlangius merlangus) are closely associated with the
brown shrimp (Crangon crangon ), upon which they exert
strong predation pressure (Bergh ahn 1996) . On a more
local level, habitat complexity may be a highly important
influence on the size and diversity of the fish assemblage,
particularly in tropical systems where seagrass beds and
mangroves are prevalent.
Estuarine fish assemblages may also be influenced by
much larger scale phenomena. Attrill and Power (2002)
reported that diversity, abundance, and growth of fish
species in the Thames estuary over a 16-year period were
primarily influenced by variations in climate known as the
North Atlantic Oscillation (Fig. 5.12, Box 5.5) . For a large
number of fish species. this climatic influence appeared to
be greater than factors such as water temperature, salinity,
or freshwater flow. How could a variable climate pattern
have such a controlling influence? A significant relation-
ship was evident between the NAO and the difference in
water temperatures between the North Sea and estuary. At
low phases of the NAO (cold, dry winters) the estuary was
significantly warmer than the open sea, providing highly
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
TECHNIQUES: Using otolith
microchemistry to trace fish
movements
Estuaries are very important nursery grounds fo r the
early years of many coastal fish species, t he you ng fish
then migrating out of the estuary to join the coastal
stock. Other fish species undertake migrations from
freshwater to th e sea or vice versa, so experience a
range of salini ties over their life cycle. To understand the
importance of estuaries to fish stocks, and aid t heir con-
serva tion, it would be very useful to quantify this use of
estuarine systems by fish species; but how? Fortu nately,
a history of where fish have been living is stored in their
ear bones, or otoliths, solid structures laid down as the
fish grows and often demonstrating growth rings like
fish-scales or t rees. These otoli ths are produced using
the minerals from the wa ter in which the fish was liv-
ing at the t ime, so the composi tion of these bones will
be in t he same proportions as the surroundi ng water
(Leakey et al. 2009). If the fish moves between waters
of different chemical composition, then t his will result
in a different chemical signatu re of the ear bone layers
put down in each water body. By analysing the chem-
istry of otoliths we can therefore obtain information on
whether, fo r example, a fish has lived in low salinities
during its early life-stages or elucidate its migration pat-
terns (Chang et al. 2004).
Undertaking suc h analysis is, however, difficult
and involves advanced analytical equipment in
order to get enough resolution in the data to look
0.0025
at changes in habitat th roughout a fish's life: each
individual year band of the otoli th will have to
be separately analysed, for example. One of t he
main methods to do th is is to cut the otolith in
0.0015
section and use a laser to ablate a small part of
the otolith. The result ing gases are cap tured and
0.0005
analysed using a sensitive mass spectrometer, the
result ing overall equipment needed being termed
'Laser ablation inductively coupled plasma mass
spectrometry' (LA-ICP-MS; Ludsi n et al. 2006).
From th e results the concentration of elements
wi thin the sample can be determi ned. Several
elements are key to study in ter ms of assessi ng
whether a fish has been in brackish or freshwater,
as they vary consistently with changes in salin-
ity. Strontium, in par ticular, can exhibi t a strong
gradient along the freshwater-marine continuum
(Leakey et al. 2009), particularly when compared in
relat ion to t he calcium in the water- the Sr:Ca ratio
increases wi th salinity. The figu re shows the Sr:Ca results
for an otolith of a plaice (Pleuronectes platessa) caught
in the southern North Sea off the Thames Estuary. The
very centre of the otoli th was laid down when the fish
was in its larval and early juvenile stages, and it can
be seen that the samples ablated from th is point have
a lower Sr:Ca ratio than those nearer the edge, which
would be laid down in later years. It therefore appears
that this fish did indeed spend the first stage of its exis-
tence in reduced sali nity, migrating out to full sali nity
condi tions as it got older.
Using otoli th microchemistry can provide insights into
migrations of species that actually change t he way we
understand th eir ecology. A classic example involved
investigating otolith chemistry of eels (Anguilla; Tsuka-
moto et al. 1999), these species bei ng textbook exam-
ples of catadromous migration, movi ng from living most
of their lives in freshwater systems to spawn in t he sea.
Tsukamoto et al. (1999) studied the distribution of the
otolith Sr:Ca rat io in eels from the Atlantic and Pacific
to assess the proportion of time spent in freshwater and,
to their surprise, showed that many of the specimens
they collected from t he mari ne environment showed no
evidence of ever being in freshwater at all, spending
their whole life at sea. It is clear, therefore, t hat eels
need not be catadromous, but some populations are
fully mari ne.
0.003 , -- - - - - - - - - - - - - - --,
• • •
• •
0.002 •
•
• •
0.001
0
1 2 3 4 6 7 8 9
Ablotion point
Ph oto graph: Ch ris Leakey
 5.3 Productivity and food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

• 20
c.
0•-19
•
,, .
, ..-
•
~
10

9 , "
"'
Figure 5.12 Relationships
between the North Atlantic
'"•• ,, .S!
18 , ," Oscillation Index (NAOI) and
---•
'0
=, B , ,
~

--. •=0
0 17
-- ~
•=0
,
,
fish diversity, abundance,
~

• 16
, • -• 7 •
, •
and growth in the Thames
c
••
,.•
0
15
,,
• ,,
~

-
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, ,
estuary. The data are fitted to
14
0 10 20 30 ., ~

50 10 20 30
the NAO 1 that incorporates
NAOI NAOI a lag.
2.0
- 65
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es
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NAOI NAOI
1000
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NAOI NAOI

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favourable conditions for manyjuvenile fish. Consequently, beds that can form in the mouths of estuaries (Chapter 10)
more individual fish appeared to be using the estuary dur- and the systems bordering the outer estuary (saltmarshes,
ing this phase of the climatic cycle. Growth and diversity mangroves) . Production in estuaries is therefore dominated
were higher during wet, warmer phases, and increased by the utilization of detritus; amorphous organic mat-
species' number was related to the appearance of southern ter present in very high levels in estuarine sediment and
species in the estuary. The appearance of such warm water water. Typical levels of dry organic matter (measurement
southern species in northern temperate regions has been of the biomass ofall organic material) in an estuarine water
highlighted as a consequence of global warming, but some sample can be 110 mg I -" compared with 1-3 mg I - 1 for
species may just be responding to climate cycles. open seawater. Similarly. the organic carbon in an estuarine
mudflat can result in a biomass ofdetritivores ten times that
of offshore sediments. These invertebrates in turn support
5.3 Productivity and food high numbers of predators, including birds and fish. The
webs carbon from this detrital source is therefore the main foun-
dation for the estuarine food web, so where does it mainly
5.3.1 Energy sources-where does the come from? Detritus finds its way into mudflats from the full
carbon come from? range of surrounding habitats (allochthon ou s), including
fully terrestrial (e.g, leaf litter brought down by rivers),
Overall plant biomass and primary production are low in marine (material from algae, seagrass, and animal mate-
estuaries (5.2.1), with the exception of extensive seagrass rial brought in with the tide), semi-terrestrial bordering
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

systems (e.g. saltmarshes, mangroves) , and from produc- 5.3.2 The use of stable isotope
tion generated within the estuary itself (au to ch t honous) . analysis in estuarine food webs
So how important are these respective sources in estua-
rine food webs? Are particular carbon sources favoured by Carbon has two stable isotopes, 12C and 13c. Due to differ-
estuarine organisms? Until comparatively recently, such ent modes of photosynthesis, plants accumula te t he heavy
ques tions were hard, if not impossible, to answer, but the isotope of carbon at different rates (see Chapter 2) . There-
development of stable isotope techniques have enabled fore, it is possible to distinguish between, for example, a
estuarine ecologists to gain an insight into these questions. leaf fro m a tree and a green a lga by determining the stable
isotope ratios with in each plant's tissues. An alysis mea -
Organic carbon is the bioavailable carbon present in a sures the proportion of the heavy isotope and compares
sediment, so does not include mineral forms like CaC0 3 this with t he standard . The difference is expressed as 013C
found , for example, in mollusc shells. It is generally (%0), wh ich varies depending on the source carbon. There-
assessed by the loss of material after combustion in a fore, an isotopic signal can also be ob tained from detritus,
furnace . which indicates its origin. The resolution is improved con-
siderably by also determining the stable isotope ratios of
nitrogen, or preferably sulphur, within the material, giving
a second axis allowing separation of carbon sources that
Box 5.5: The North Atlantic overlap when carbon alone is used (Fig. 5.13). The isotopic
Oscillation (NAO) ratios of C and S are relatively conserved whe n plant m ate-
rial is ingested and incorporated into the bodies of animals,
The climate in the North Atlantic undergoes a rela- so analysing the tissues of estuarine animals will en able
tively unpredictable cycle in terms of its weather
patte rn, this cycle being known as the NAG, and its
UPPER
fluctuations are measured by a simple atmospheric
10 rr===j T::----r"'""~T--;----__,
pressure differential between Iceland and the Azores Oligo-phyla \~'"
~'~, Benthicmicro algae
(the NAG Index). At one extreme, high pressu re over 15 h.
, ...... ',
-----
Iceland will result in cold, dry wi nters in Nort hern
\
,, ...... ,
\
\
,, o
------
Eu rope (a low NAOI), whereas comparatively high
10
0, 0
'
~" ~ ..
• -
'" • loli
pressure over the Azores results in dominant winds 5 marsh
,,
from the SW and consequently wa rm, wet, and windy ,, Fresh
o , ma rsh ,,
wi nters. The oscillation between these two states ,
is shown in the figu re. This climatic cycle is now ---s:
0

recognized as having an extremely important influ- ~

LOWER
~

ence on the weather, the position of the Gulf Stream, 70 10

sea temperatures, and consequently the ecology of Oligo-phyla I,, M/Ephylo I'.
15 o ', a Benlhlt micro
, algae
terrestrial, freshwater, and marine syste ms in NW
~
~ ,, 0 0
,,
-a;
= , p ••
Eu rope. Cor related long-ter m cycles have been Q
~
10 •• ••
observed in a disparate range of marine organisms " ,, c ~
•
,,
from plankton, throug h to benth ic commu nities and 5 Ierr loli
,, marsh
fish catches. Fresh ,,
0 marsh ,,
NADindex (De! - Mar) 1864 - 2003 ,,
5
-30 -25 -20 -15 -10
4 Depleled Enriched
o e(%j
13

-
~o
1
,
Figure 5.13 Exampl e ran ges of st able isotop e ratio s for
carbon and sulp hur in a range of plants cont ribut ing t o th e
d etritus of upper and lower regi ons of an est uary. Symbols
o n th e figure refer t o th e co mparat ive isoto pic rati o s w it hin
the tissues of est uarine animals (o pen circles-pelagic,
clo sed sq uares- bent hic), enabling th e carbon so urce o n
.. 18L
W~I~"~O~18L~~I~~~
O ~"LOO~I~"~O~I~LO-I~"~O~"L~~I~9S~O~"L60~I~"~O~"L~-I~"~O~200LJ
O w hich th ey feed t o be assessed. M/E = mid-estuary, o ligo =
Year
o ligohaline, Terr = t errestrial material, Fresh = freshw ater,
Phyto = phytoplankton .

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
information to be obtained on the carbon source utilized
by these organisms. This has proved a very important tool in
aiding our understanding of how estuaries function.
One of the most comprehensive studies was under-
taken in the Plum Island Sound Estuary, northeastern USA
(Deegan & Garritt 1997). Samples of plant material and a
large range oforganisms were obtained from the full length
of the estuary and analysed for stable isotope ratios in order
to determine which carbon sources were most important
for the estuarine organisms and. additionally, whether the
relative importance of these sources varied over the length
of the estuary. Researchers wanted to know whether ani-
mals simply utilize local carbon sources or if they were more
selective. Organisms were found to rely heavily on local
sources of carbon (Fig. 5.13). Upper estuarine food webs
were based on fresh water, saltmarsh, and phytoplankton
carbon, in contrast to the lower estuary where marine phy-
toplankton, benthic algae, and perhaps saltmarsh material
were the most important. The results were supported by
notable shifts in the carbon sources utilized by species pres-
ent along a large length of the estuary, such as the mum-
michog (Fundulus heteroclitus, Fig. 5.11a). Interestingly,
despite the large seasonal input of terrestrial leaf matter in
New England, this carbon source seemed unimporta nt in
the food web of the Plum Island Sound Estuary.
A similar, though perhaps even more unexpected, result
was found in the tropical Embley River estuary in Australia
(Loneragan et al. 1997). Stable isotope analysis was uti-
lized to investigate whether seagrass- ormangrove-derived
carbon were important carbon sources for commercially
important prawn species in the outer estuary. Organic mat-
ter in the sediment was found to correspond to the main
local source. but this pattern was not reflected in the tis-
sues of the prawns. While prawns inhabiting seagrass beds
did seem to rely completely on seagrass-derived material.
mangrove-inhabiting prawns did not depend on carbon
from mangroves. utilizing either algae or seagrass mate-
rial. The conclusions from most work so far undertaken is
that animals in estuaries do not appear to be able to utilize
terrestrially derived material to any great degree. However,
a recent study has suggested that oligochaete worms may
provide an entry route for terrestrial carbon into estuarine
foodwebs (Attrill et al. 2009), having evolved into estuar-
ies from freshwater and terrestrial systems (earthworms).
w here they are major processors of detrital material. It is
probable, however. that most animals inhabiting estuaries
do not have the physiological capability to assimilate ter-
restrial carbon direct from detritus and most is utilized by
bacteria, the carbon being released through bacterial res-
piration (see Chapter 3) .
Analysis of nitrogen isotope ratios can provide further
evidence helping to determine the position of organisms
within food webs. The heavy isotope of nitrogen ( 15N) con-
centrates up the food chain at approximately 3%0 per step.
5.3 Productivity and food webs
Therefore, such analysis of animal tissue (together with
other components of the food web) can enable the trophic
level of an organism to be determined. This technique was
put to interesting use in the Exe estuary, south-west Eng-
land, where there is a large bed of blue m ussels (Mytilus
edulis). A copepod, Mytilicola intestinalis, occupying the
guts of Mytilus had previously been blamed for population
crashes in commercial mussel stocks in Europe. but evi-
dence that it was in fact a harmful parasitic was equivocal.
Stable isotope analysis determined that the copepod had
a nitrogen isotope ratio 2.8%0 above that of the host gut
(Gresty & Quarmby 1991), suggesting it therefore feeds
on host tissue (although not directly, perhaps sloughed off
cells) rather than sharing the gut contents.
5.3.3 The importance of birds in
estuarine food webs
The majority of books and chapters on estuaries include
diagrams of food webs, indicating the major links from
detritus up to large predators. often with attempts to quan-
tify energy flow along these links. However, such construc-
tions tend to be oversimplified in the context of estuaries,
due to the variability in species' distribution over tidal and
seasonal cycles, and can thus only ever be a generalization
of trophic interactions within estuaries. which will vary
considerably over both spatial and temporal scales. Many
large and diverse groups tend to be lumped in one box
within food webs, indicating their trophic level but mask-
ing any detail about their specific interactions. Fish in estu-
aries, for example, feed on all possible trophic levels from
primary production to other fish, and their diet potentially
varies considerably with time of year. position in the estu-
ary, and the body size of the fish . This is even more true for
birds. which have been comparatively neglected in estua-
rine food-web analyses (which concentrate on 'marine'
species). or assigned to a single compartment at the top
of the web. Both approaches oversimplify t he role of birds
in estuaries to such a degree that an erroneous impression
can be given of their importance, and thus potentially how
estuaries function.
Estuaries are exceptionally important habitats for birds,
particularly those in temperate latitudes, which provide key
feeding areas for birds undertaking migration. Principally
estuaries are vital for h uge populations of wading birds
(Charadriformes) and wildfowl (Anseriformes); 4.5 mil-
lion shorebirds migrate to just the British Isles every year,
while> 1 million western sandpiper (Calidris mauri; Fig.
5.14a) stop over on the Fraser River Estuary. west Canada.
Among the birds that use estuaries we can find examples of
species feeding at all trophic levels from geese grazing on
seagrass (e .g. Brent geese, Branta bemicla; Fig. 5.14b) to
piscivorous species such as cormorants (e.g. Phalacrocorax
carbo) and herons (e .g. Tigrisoma mexicanum) . Grazing
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 5.14 Examples of bird species reliant on estuaries for food: (a) western sandpiper, Calidris mauri, which forms
huge flocks in NW America (photograph: Alan D. Wilson); (b) Brent geese, Bronta bernie/a, major grazers of intertidal
seagrass beds in outer estuaries (photograph: Adreas Trepte).

Brent geesecan have a dramatic impact on intertidal sea-
grass beds as they eat the roots as well as the leaves. Huge
flocks can therefore be major bioturbators in outer estuar-
ies, reworking the top em of sediment 8 times in 3 months.
However, the vast majority of birds (particularly waders)
feed on the rich supply of invertebrates inhabiting the mud-
flats of estuaries. with a distinct niche separation in terms
of prey item, evidenced by different bill length s, feeding
methodology, and feeding position on the shore. Overall, the
dynamic interaction between the two groups of organisms
contributes to the size of populations of both invertebrates
and birds present in an estuary. The number of birds feed-
ing on an estuary is directly related to the size of available
mudflat, a simple area effect (Fig. S.ISa) with important con-
sequences for estuarine habitat loss. However, at a smaller
scale, the abundance of feeding birds is dependent on the
amount of available food in the mud, a higher biomass of
invertebrates sustaining a larger population of birds (Fig.
S.ISb) . The distribution of invertebrates across both estuar-
ies and individual mudflats can vary considerably, so the sup-
ply offood for foraging waders is not uniform and influences
the distribution of birds on a mudflat. Clearly, the optimum
patch for a bird to feed in is one with the highest density of
prey, but this also depends on the number ofother competing
birds foraging in the patch. Agood patch with lots ofcompeti-
tors will eventually be less suitable than a less-rich patch with
fewer competitors due to increasing interference with other
birds, so birds will move to exploit other areas in which the
rate of reward is greater. Eventually, birds should be distrib-
uted across the mudflat so that the proportion on a patch
will approximate the proportion of resources in that patch,
and all individuals receive equal rewards. This is mown as
the 'input matching rule' of the ideal free distribution (see
Sutherland 1996) and is an example ofgame theory, which

1l1li 10l1li l D,1JIJIJ 5D,DIIII D lDD 2DD JDD

Estuary size (hal Prey m-2

Figure 5.15 (a) Relationship between estuary size and t he average number of five wader species present. (b)
Relationship between prey density (Nereis, Scrobicularia) and wader density (curlew, Numenius arquata).
 5.3 Productivity and food webs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

demonstrates that the pay-offofa strategydepends on which
sttategyis adopted by others. Ifbirds conform to the IFD, the
strategy is considered to be stable as no individual can gain a
higher food intake by moving.
Ideal Free Distribution: ideal refers to birds choosing to
forage where rewards are highest, free refers to the fact
that there are no impediments to their movement.
However. other factors tend to moderate the ideal free
distribution so that it rarely applies on mudflats. One fac-
tor is territoriality: if one species is dominant and actively
defends its foraging patch, then other bird species are no
longer free to move between patches, so suitabilitywill vary
between patches. This is known as the ideal despotic dis-
tribution. On estuarine mudflats. for example. aggressive
species of gull or crow can highly influence wader distri-
bution. A further factor highly relevant to estuarine birds
is the tendency for many waders (such as dunlin, Calidris
a/pinal to forage in flocks, mainly to reduce predation risk.
Newly arriving birds tend to join existing flocks rather than
risk foraging alone; despite the potential higher rewards
in areas without flocks. predation risk reduces the suitabil-
ity of these habitats. This is known as the Allee effect and
can dramatically shift the theoretical ideal free distribu-
tion. Bird distribution can also be affected by interference
and depletion. Interference between birds can be through
direct aggressive contact (e.g. oystercatchers, Haematopus
ostralegw;) or indirectly, The movement of redshank (Tringa
totanus) over the mud influences the number of their prey.
Corophium volutatoT. which retreat into the burrow on
detecting the bird (Fig. 5 .16a) . Consequently, redshank
avoid foraging in patches recently exploited by another
redshank (yates et al. 2000), so will influence the distribu-
tion of feeding groups. Foraging redshank tend to be more
dispersed than waders such as dunlin. Finally, feeding
birds can have a dramatic impact on the invertebrates in
the mudflat (Fig. 5.16b), removing a large percentage of
the standing biomass and exporting substantial amounts
of carbon to the terrestrial environment through their fae-
ces (Post et al. 1998) . This removal of prey resource can
have a major impact on bird distribution. as previously rich
patches become depleted, altering their suitability. Simple
depletion models have been shown to accurately predict
shorebird distribution over a range of different scales (Gill
etal. 2001) .
5.3.4. Saltmarsh systems: production
where estuary meets the land
The sheltered shorelines of outer tropical estuaries and
lagoons are often bordered by extensive mangrove forests
(Chapter 10), but in temperate regions these ecosystems
are replaced with another important habitat based around
plants of terrestrial origin: saltmarshes. Adam (1990)
defines these marshes as 'areas vegetated by herbs, grasses
or low shrubs'. bordering saline water bodies. and contrast-
ing markedly from seagrass beds (Chapter 10) as they are
exposed to air for the majority of the time, becoming sub-
merged at high tide, sometimes only at high spring tides,
giving them their alternative name of tidal marsh. Due to the
main constituent plants being generally small. saltrnarshes
tend to be very flat, low-lying areas at the top end of mud-
flats (Fig.5.1?), providing a striking contrast to the dark
grey of the adjacent mud. They are therefore most impor-
tant in low-lying coastal estuarine areas. where there is not
a sharp increase in vertical gradient at the top of the shore.
and in such regions, such as parts of NE America. can form
extensive marshes thatare the dominant coastal habitat; for
example, the Great Marsh in New England, USA covers a
total ofover 8000 ha. Globally, however, saltmarshes occupy
a comparatively small area estimated at 45 000 km 2_
slightly larger than Denmark (Greenberg et al. 2006) . Most
saltmarsh is to be found in SE USA and NEAsia (Table 5.1) .

(e) '" Redshank walks (b) 80 4.0

~

.-E
~ 40 ,,
ceer mud

-
~
~
,,
,, '1' 60 3.0
=
~
.~

g
30
,, -
E
B '1'
-
~
~ ~

-E
~
~
g , g
~ =
-- 40
g
E
20 ~ 2.0 g
.-
~
~

::;
E
g

--- 10
!l-
g
c
~
~

20 1.0
'"
~
~
g

E
-
~
z
0 0 J 0
5 0 5 10 10 20 A 5 0 N D J f M A M J J
Minutes Month

Figure 5.16 (a) The response of Corophium to redshank forag ing. (b) Depletion of prey by bird foraging over the year.
A = Nereis and Nephtys in the Wash, eastern England; B = Corophium and C = MytHus in the Ythan Estuary, Scotland.
 Chapter 5 Estuaries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Table 5.1 The aproximate surface area and dominant vegetation for tidal marshes, by coast line (from Greenberg
et al. 2006).
Continent Coastline
North America North Atlantic
South Atlantic, Gulf Coast
Pacific
Eastern South America Atlantic
Europe All
Asia (Japan, Korea, Chi na) Pacific
Australia, New Zealand, Tasmania- Southern (temp erate)
South Africa Southern
" There are more extensive salt marshes in trop ical Austral ia, but th ese are high, level flats above mangroves-often hypersaline
and with large salt flats and sparse vegetation-and are not counted in the total area.
Figure 5 .17 (a) The saltmarsh of Langerbaan Lagoon ,
South Africa-the most southerly such system on the
continent. (b) Sarcocornia capensis, the South African
version of Sa/icomia common in northern hemisphere
saltmarshes (photographs: Martin Altrill).
Saltmarsh plants face similar problems to mangroves,
having to live in salty, waterlogged soils and deal with reg-
ular inund ation, so show patterns of zonatio n w ithin the
marsh reflecting the plants' tolerance to these conditions ,
particularly the high salin ity; these plants are known as
halophytes. Saltmarshes are also characterized by low plant
diversity, reflecting the harsh conditions. At the interface
between the mudflat and the marsh are pioneer species
capable of surviving in these marine intertida l cond itions
and provide stabilization of the substratum. Examples of
such plants are grasses w ithin the genus Spartina, w hich
form large stands and can be the main primary producers
Extension Dominant vegetation
(square
kilometers)
50 0 Spartina, Phragmites
15 00 0 Spartina, Juncus
440 Salicornia, Spartina
2300 Spartina, Juncus
1400 Salicornia, Spartina, grasses
25000 Chenopods, Phragmites
772 Sarcocomia, other chenopod
shrubs
70 Sarcocomia, Spartina, grasses
on the marshes of East Coast USA. Behind the pioneers
ofte n exists the main part of the marsh dominated by a
few species of fleshy herbs and grasses , such as Salicorn ia,
Sueda , and Juncus. Towards the land the flora becomes
more diverse and at this point competition between plants
becomes an important factor governing distribution (Adam
1990) , the reverse of the pattern of algae on a rocky shore.
Distribution of plants on the main marsh is, however, not
just a simple gradient o f salinity tolerance, but a mix of
responses to both salinity and flooding. In some marshes,
the soils of the mid-marsh can have higher levels of salt than
lower parts that are regularly refreshed by the tide due, for
example, to evaporation in summer, w hilst lower marshes
have more waterlogged soil. In Californian saltmarshes , it
was found that Salicorn ia was better able to tolerate flood-
ing w hereas Arthrocnemum was more able to deal w ith
higher salin it ies (Pennings & Callaway 1992).
In a sim ilar pattern to mangroves (Chapter 10) , it would
appear that few grazer species are able to feed directly on
living saltmarsh plant material, the main competitors for
this organic substrate being fungi and bacteria (Lillebo et aJ.
1999) . The majority of invertebrates living in saltmarshes
therefore consume a mix of processed detritus and micro-
organisms and incorporate saltmarsh pro duction in this
manner. Mos t foo d webs within tropical and temperate
estuarine syste ms are therefore detritus based. Within salt-
marshes the few herbivores that exist tend to be insects (e .g.
Orthoptera, Hemiptera, and Coleoptera) , plus a few mol-
luscs and crustaceans, reflecting the terrestrial nature of the
saltmarsh plants. Penn ings et aJ. (2001) stud ied herbivory
in eastern USA saltmarshes and discovered some interest-
ing large-scale patterns. Through transplant and feeding

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
experiments, they discovered that plants from northern
marshes were more palatable than equivalent plants from
southern marshes: in laboratory tests 85% of herbivores
showed a preference for the northern plant. Further investi-
gations (Pennings et al. 2009) revealed that herbivore pres-
sure was, however. much greater in the southern marshes:
herbivores were typically >10 times more abundant and
damage to plants was 2-10 times greater in southern
marshes than northern ones. On transplantation, north-
ern plants particularly suffered in southern saltmarshes. It
would therefore appear that selective pressure in southern
saltmarshes due to higher herbivore damage has resulted
in greater plant defenses at lower latitudes and thus lower
palatability, a biogeographic trait in consumer-prey inter-
action that has been noted in other systems.
Whilst comparatively few herbivores on saltmarshes
are of marine origin. saltmarshes, like adjacent estuaries.
are sites of high secondary productivity. with a range of
marine invertebrates colonizing the marshes to exploit the
detritus available. This in turn provides food supply for ver-
tebrates; saltmarshes are important foraging sites for wad-
ing birds and wildfowl, particularly at times when mudflats
are inundated. However. the marshes differ from the flats
by having a high level of structural complexity, as well as
the abundant food supply (comparable with seagrass beds;
Chapter 10), and so additionally saltmarshes are impor-
tant habitats for many juvenile fish at high tide. Rountree
and Able (2007) define five types of marsh function mak-
ing them valuable to fish and other nekton: reproduction,
foraging, refuge from predation, refuge from stressful envi-
ronmental conditions. and environmental enhancement of
physiology. However, the same authors state that little is
actually known about the structure of fish assemblages in
tidal marshes, and even less about the relative importance
of these functions. but it would seem these functions vary
across spatial gradients within the marsh and over tidal,
diel, and seasonal time-scales, resulting in organism
migration across marsh habitats over these scales to exploit
functions available. Other studies have demonstrated clear
value of marsh use by fish. For example. manipulations of
male mummichogs (Fundulu.s heteroclitu.s; Fig 5.11a) resid-
ing in marshes in NE USA revealed that fish which had full
access to the marsh surface exhibited higher growth rates
and had a greater production rate than males restricted
to pools (MacKenzie and Dionne 2008) . Australian salt-
marshes differ from those in the northern hemisphere as
they are inundated less frequently and for shorter periods
(Hollingsworth & Connolly 2006), though fish still manage
to exploit these habitats. Glassfish (Ambassisjacksoniensis)
were caught before and after feeding on marshes and two
other habitats and found to have significantly fuller stom-
achs on returning from saltmarshes, having fed extensively
on zoea larvae that were released following synchronized
spawning of the resident crabs.
5.4 Diversity patterns in estuaries
Saltmarshes represent perhaps the most terrestrial habi-
tat utilized by marine organisms, and are perhaps one of
the systems most threatened by potential sea-level rise as
a result of global climate change. as they become more
inundated. As sea-levels rise. such intertidal and supralit-
toral habitats will need to retreat landwards: it has been
estimated that with a rise of 6 mm/year, estuarine systems
in the UK will need to migrate landwards at around 10 m/
year, whilst open-coast landforms may show longshore
migration rates of 50 m/year (Pethick 2001) . Clearly this
has major implications for management. particularly in
conflict with flood defences. If large flood barriers have
been constructed at the top end of saltmarshes, as has been
the case in many low-lying areas of northern Europe. the
marsh habitat has nowhere to migrate to. As sea-levels
rise, the marsh will just become gradually inundated with
a smaller and smaller existent area-a phenomenon known
as coastal squeeze. An alternative flood-defence mechanism
is the use of managed retreats, areas of coastal land 'sacri-
ficed' to the sea so that hard flood defences are removed
and the flood tide spills over large areas of, for example, old
agricultural land. This mechanism clearly requires vacant
land by the coast-a rare commodity in developed areas
such as SE England.
5.4 Diversity patterns in
estuaries
5.4.1 Diversity trends along estuaries
Estuaries are generally considered low-diversity systems.
with few species able to survive in the harsh environment
they present. This is certainly true for mid-estuary mud-
flats, which tend to be used to represent the whole estuarine
system; this habitat contains fewer species than in border-
ing marine or freshwater systems. This image of estuaries,
however, is perhaps a little simplistic as over the full length
of the system many species from a wide taxonomic range
can be found-over 750 species of invertebrate have been
recorded from the Thames for example.
Few systems on earth will present such a wide phyletic
diversity due to the combination of marine and freshwater
taxa. Additionally. sites in outer estuaries have been noted
to have higher species' richness than adjacent marine sys-
tems. generally due to the provision of complex structural
habitats. such as seagrass meadows and mussel/oyster
beds. However. trends in benthic macro-invertebrates
have provided the paradigm for estuarine diversity trends,
exemplified by the Remane diagram (named after Adolf
Remane, a German marine scientist who worked primar-
ily in the Baltic in the early twentieth century), which is
generally used to describe how diversity varies with salinity
along an estuary (Fig. 5.18a) . This trend shows a dramatic
 Chapter 5 Estuaries
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decrease in number of species from river into the estuary, in the mid-estuary were simply marine, or freshwater taxa
with a species' minimum around 7 (known as the arten- at the extreme edges of their range, the pattern of species
minimum) then a gradual increase in diversity towards
J change into an estuary from each end representing an eco-
fully marine conditions. cline.
The diagram is subdivided into freshwater species,
marine species. and true estuarine species (green sector Ecocline and ecotone are two forms of landscape bound-
in Fig. 5.18a) . The existence of these estuarine. or brack- ary between systems. Ecoclines tend to be gradual, w ith
ish water. species has been questioned by several authors a transition of communities, whereas ecotones are more
and three completely independent studies have redrawn abrupt (see Kent et al. 1997 for more details).
the Remane diagram. removing this group of organisms
(Fig. 5.18b) . Barnes (1989) argued from a physiologi- The relevance of the Remane diagram as a model for
cal angle, suggesting these true estuarine organisms are diversity trends in estuaries has also been questioned, as
simply marine opportunists able to exploit the particular it was developed in the 1930s as a hypothetical description
conditions in the mid-estuary. but in terms of salinity toler- of trends in the Baltic (see 5.5 .1), a practically tideless sea.
ance could be found practically anywhere in the estuary. As described earlier (5 .1), the environmental variability
Sediment provision is perhaps a more important factor in estuarine systems is the major constraint to organism
determining where these organisms are found . Attrill and colonization, so an axis with fixed salinity may not be very
Rundle (2002) examined faunal patterns in estuaries at meaningful. What does a salinity of '7' actually mean in an
the evolutionary scale and concluded that species present estuary? If salinity range is used as a measure of environ-

{-I ,,
,,
, (h)
True estuarine :
•
'j.
spedes :
,,
-s
'.,-
1' 0
, !l.
Freshwater spedes

, ~
1.;::

,,, ~
,,
o 1 10 11 20 2S 30 31
o 1 10 11 20 2S 30 3S
Salinity Salinity

-ci
«) 2 1 , - - - - - - - - - - - - - - - ,
~
20
,
"
<,
{dl 2 1 , - - - - - - - - - - - - - - - - ,

• 20
-
= • ' t:,
---- ............ .~ IS
. ... ... _-- - - - __
c
-'"
10 --_

1
-- -.---_..---. - ,
. c 10
.;
=
1
"'-+ • •
2 4 6 8 8 10 1214 16 18 20 22242628 30 32
Salinity range lalinity (PIUj

{.} 12
1 - - - - ----::;;:::::= :::-1
10
•~ 8•
... ,.. 6
.; 4 ~-diversity
=
2
oL---:;-----"----;-;;;----'----;-;-;;;;--L--,--;o,-----'
<1 1-10 11-20 > 20 o 2 4 6 8 10 12 14 16
Average salinity Salinity

Figure 5.18 Examples of diversity trends in estuaries. (aHc) Patterns of macro-invertebrate diversity: (a) original
Remane diagram, (b) modified model removing estuarine species (see text), (c) linear model of diversity using salinity
range. (d) Algal diversity in the Thames estuary. (e) Zooplankton diversity in the St. Lawrence. (I) Fish diversity in
Chesapeake Bay_

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
mental variability in estuaries (Attri1l2002), a linear model
can be constructed to describe diversity trends in estuar-
ies (Fig. 5.18c) . It is often assumed that the classic model
of diversity trends for macro-invertebrates is representa-
tive of all taxa in estuaries, but this does not seem to be
true. For both algae and zooplankton (Fig. 5.18d,e) there
is a steady decrease in number of species present from sea
to river, with no species minimum in the mid- or upper-
estuary. Fish diversity is hard to determine due to their
mobility, but appears to show a decrease in the mid-estuary
area. However, a very different pattern is apparent when an
alternative measure ofdiversity is used (see Chapters 1 and
15) in this case ~-diversity, rather than the usual measures
J can be manipulated and still be comparatively representa-
of a-diversity (Fig. S.18f), demonstrating a peak in diver-
sity in the upper estuary.
5.4.2 Larger scale diversity trends
Anecdotal evidence has suggested that tropical estuaries
are more diverse than their temperate equivalents, espe-
cially in the Indo-Pacific, so potentially a latitudinal diver-
sity cline (Chapter 1) may exist in estuarine systems. If this
is the case, it raises interesting questions about organism
adaptation to fluctuating salinities. Empirical evidence for
this is rather lacking, particularly for the key mid-estuary
areas, and direct comparisons are often difficult due to
the inherently different nature of temperate and tropical
estuarine systems, particularly the overall salinity regime.
Tropical estuaries, for example, often experience hypersa-
line conditions (see 5.5.2) due to intense evaporation, so
for inner parts of these systems the salinity variability may
be very different.
Direct comparisons of numbers ofspecies found in mud-
flats across the globe are difficult due to variations in sam-
pling methodology, but initial attempts to investigate the
existence of large-scale diversity patterns have been made
in mid/outer estuary mudflats using a diversity index inde-
pendent of sample size (Attrill et at. 2001) . A significant
increase in diversity was apparent at decreasing latitudes,
supporting the idea that tropical estuaries are indeed more
diverse than those at higher latitudes. Of the manyexpla-
nations for the latitudinal diversity cline (Chapter 1), the
most likely explanation is the impact of glaciation on high-
latitude systems (Box 5.1), many of which were effectively
extinct until < 10 000 years ago. Tropical systems have
therefore remained comparatively undisturbed for a much
longer time period than temperate systems, and are thus
much older systems which have had a longer effective evo-
lutionary time to allow diversification. If tropical estuaries
are found to be comparatively diverse, it is feasible that tem-
perate estuaries are currently low diversity systems because
they are geologically new rather than solely because of the
impact of environmental variability.
5.4 Diversity patterns in estuaries
5.4.3 The role of biodiversity in
ecosystem function
Two main questions describe what is perhaps one of the
most important current ecological debates, namely whether
biodiversity matters (see also Chapters 1 and 6) . Are high-
diversity ecosystems more stable? Is the functioning of an
ecosystem affected by how many species are present (eco-
system functions include measures of primary productivity,
decomposition rates, etc.)? The comparatively low diversity
to be found in mid-estuarine mudflats makes them excel-
lent test systems for investigating the role of biodiversity in
the functioning of an ecosystem. The estuarine assemblage
tive of the natural state, unlike experiments on grassland,
rainforest, or coral reef systems, for example, where such
studies are only ever going to include a small fraction of
extant species.
Two main studies that involved estuarine invertebrates
have been undertaken to address the relationship between
diversity and ecosystem function. Emmerson et at. (2001)
investigated diversity-function relations in a series of
mesocosms measuring ammonia-nitrogen (NH 4-N) flux
as an indicator of ecosystem function (a process essen-
tial for primary production) under varying treatments of
biomass and diversity. Nitrogen flux increased with an
increase in biomass, but relationships with diversity were
idiosyncratic and varied between sites. Significant effects
of species' richness were apparent from a Swedish fjord,
but in a Scottish estuary (Ythan) only species' identity was
important. In this case, the ragworm (Nereis diversicolor;
Fig. 5.6d) had a disproportionate effect on NH 4-N produc-
tion. However, one consistent result was that ecosystem
function was much less variable and more predictable at
higher diversities, supporting the idea that diverse systems
are more stable. Bolam et at. (2002) undertook elaborate
and extensive field experiments in Forth Estuary, Scotland,
again manipulating the biomass and diversity of patches
of mudflat and relating diversity and biomass to a set of
indicators of the functioning ofa detritus-based ecosystem,
such as organic content, nutrient fluxes, and community
respiration. Neither changes in biomass nor diversity were
found to significantly affect any of the ecosystem functions,
with the exception of oxygen consumption, so provided no
real evidence that diversity is related to the functioning ofa
mudflat community. We return to this tropic in more detail
in Chapter 6.
Mesocosms are an intermediate-sized system, such as a
dug-out pond or in situ enclosure, that can be replicated
and manipulated to test both structural and functional
parameters as a representative aquatic ecosystem.
 Chapter 5 Estuaries
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5.5 Other 'brackish-water'
systems
In addition to estuaries, there are other aquatic systems that
do not fit into truly marine or truly freshwater categories.
Some of these. like estuaries, have salinity levels more dilute
than seawater, others can have salt levels much higher than
the sea. This section provides an overview of these other
'brackish-water' systems. which can be categorized into
three main groups: hyposaline seas (large bodies of water
with salinity < 34), hypersaline waters (coastal water bod-
ies with salinity mostly > 34), and lagoons (shallow coastal
systems that exhibit a range of salinities) .
Hyposaline water has salinity less than full strength sea-
water; hypersaline water has salinity greater than sea-
water.
5.5.1 Hyposaline seas
From Scandinavia through central Asia are several large,
mainly enclosed bodies of water including the Baltic, Black,
Caspian, and Aral Seas (Fig. 5.19a) . None ofthese systems
is freshwater, but they have low levels of salinity and con-
sequently many organisms of marine origin. The fauna of
these seas has many similarities to estuaries, but crucially
there are key differences between the two, exemplified by
three examples.
The Baltic
The Baltic Sea is a large (370 000 Ian') body of water sur-
rounded by the countries of Scandinavia and northern
Europe. The sea is generally very shallow (average depth 55
m), but with one basin dropping to 460 m. Crucially, there
(o)I----/=~==_=__:~
lOMO
Russio
Vistula lagoon
Germony Polond
, Ukraine
Romonio
o Bulgori
()
Figure 5.19 (a) Map of Europe and Asia indicating the position of other 'brackish'-water systems described in the text.
(b) Laguna Madre in Texas, US.
is only one narrow, shallow entrance linking the Baltic to
the North Sea between Denmark and Sweden, and restrict-
ing inflow of seawater. It takes 25-35 years to replenish the
whole Baltic from the North Sea. Over 250 rivers flow into
the Baltic. diluting the water retained within the sea. Gen-
erally salinity is < 8, with a gradient apparent in salinity
levels from Denmark to Finland. A large proportion of the
northern Baltic is frozen every winter. However. despite
the apparent salinity gradient. conditions in the Baltic are
very different from those in an estuary, as the Baltic Sea is
practically tideless. Consequently, salinity levels at anyone
point do not vary to any great degree. resulting in a stable
salinity gradient without the highly variable, and stressful,
conditions apparent in estuaries.
Some familiar marine groups. such as elasmobranchs
and cephalopods, are absent from the main Baltic due to
the consistently low salinity levels. For other organisms,
particularly benthic species. their distribution in the Baltic
tends to correspond much more closely to their theoretical
lower lethal salinity limit than is the case in the fluctuating
conditions of estuaries . Therefore. organisms are found in
much lower salinities in the Baltic than in estuaries. Two
outer-estuarinebivalves. for example. Macoma balthica and
Mytilus edulis, can be found over most of the Baltic down
to salinities of 3 and 4 respectively. Due to the stability of
the system and the extension of species' ranges, in many
parts of the Baltic there is an interesting mix of marine and
freshwater taxa that is not found so clearly in estuaries. A
fisherman on the east coast of Sweden. for example, could
catch both pike (Esoxlucius) and cod (Gadus morhua) from
the same spot on the same day! Living in highly reduced
salinities at the edge ofan organism's range does have ener-
getic costs. however. The extra energy required for survival
at low salinities means that less energy is available for
growth (the scope for growth is reduced); individuals of
(b)
Texas
Slrcsh
loguno Modre

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benthic species, such as the clamMya arenaria (Fig. 5.6a),
get smaller with a decrease in salinity up the Baltic. In sum-
mary, therefore, the Baltic presents a similar set of species
to those found in comparable estuaries, but the lack of tides
and consequent stable salinity regime allows further pen-
etration in relation to average salinity.
The Black Sea
The Black Sea represents a trio of large hyposaline seas in
central Asia (Fig. 5.19a; further east are the Caspian and
Aral Seas) and is bigger in area than the Baltic (423 000
km-) . In a similar fashion it has only one very narrow con-
nection to the Mediterranean, but is much deeper than the
Baltic, with a maximum depth of over 2200 m, and with
salinity levels ranging generally from 17 to 21. Due to the
deep basin and minimal inflow of water from the Mediter-
ranean. the vast majority of the deep water in the Black
Sea is stagnant and deoxygenated, representing probably
the world's largest body of anoxic water. Therefore, nearly
all the benthic production within the system is generated
from a shallow (30-60 m) shelfin the north-west. However,
the Black Sea is a highly disturbed system that has been
exposed to the introduction of alien species (particularly
the comb-jelly Mnemeopsis), over-fishing, and pollution
(see Chapters 13 and 15) . Furthermore, a history of inputs
into the Black Sea from surrounding countries has exac-
erbated the deoxygenation of water in the basin and has
caused the anoxic layer to rise in the water column. poten-
tially threatening the survival of the shallow and productive
north-western shelf .
The White Sea
The White Sea (Fig. 5.19a) is a large (94 000 Jan') inlet
in the Russian Arctic that presents apparently extremely
harsh conditions for organisms. Water temperature varies
dramatically over the year. the average October-May tem-
perature being -1' C, although the coldest surface tempera-
ture so far recorded was in the White Sea (-2.78'C) . During
summer. however, temperatures can reach 20°C. whilst
the sea surface and intertidal area are covered in ice from
November to May. Generally, the salinity of the White Sea
is 23-25. but following ice melt in summer it can drop to 5.
Despite these apparently hostile conditions, many typi-
cal estuarine species exist in the intertidal sediments. such
as Arenicola marina. Mya arenaria. and Macoma balthica,
and perhaps most surprisingly, beds of seagrass (Zostera
marina) develop during the summer.
5.5.2 Hypersaline waters
Hypersaline waters are those with a salinity regime higher
than that of seawater (i.e, > 34). To achieve such concen-
trated saline conditions. the water body has to have an
evaporation rate greater than the inflow of fresh water, so
5.5 Other 'brackish-water' systems
hypersaline waters are typically tropical in location. or situ-
ated in continental areas with extremely high summer tem-
peratures. They also tend to be ofa much smaller scale than
hyposaline seas. Hypersaline waters do not include inland
brines such as the Utah salt lakes, which have no connection
to the sea or a larger body of water.
An example of a hypersaline water is the Sivash (others
include the Suez canal and Curacao Lakes, West Indies) .
This is located on the Crimea peninsula on the north coast
of the Black Sea (Fig. 5.19a) and is a comparatively long,
thin body of water isolated from the Sea ofAzov (the north-
eastern section of the greater Black Sea) by a land barrier.
There is only a very small entrance to the Azov Sea, so water
exchange is exceptionally limited. Salinity in the Sivash
varies along a gradient from 11 at the connection with the
hyposaline Azov Sea up to 132 at its most inland part. Tides
in the area are minimal, so there is little daily fluctuation.
but conditions vary seasonally due to the very cold winters
and hot, dry summers experienced in the Crimea.
The conditions in the Sivash therefore present very dif-
ferent problems for organism colonization than estuar-
ies or hyposaline seas. Organisms penetrating the Sivash
originate from the hyposaline Azov Sea, and so will have
to be able to tolerate both reduced and elevated salinity
levels, their distribution up the Sivash being dependent on
their upper salinity tolerance. However. many organisms
that thrive in estuaries have also the ability to deal with
increased salinity, examples in the Sivash being the floun-
der (Platichthysflesw;) (occurs up to a salinity of 60), the
cockle (Cerastoderma edule) (65), and the mullet (Mugi!
cephalus) (110) . However, in the most hypersaline areas
(> 130) such organisms cannot survive, and here the excep-
tionally salty waters are colonized by a few specialist spe-
cies. such as the brine shrimp (Arremia salina) and larvae
of the midge Chironomus salinus (note the latin names give
a clue to their ability to deal with highly saline conditions) .
The existence of hypersaline waters provides a salinity
range from 0 to > 130 over which organisms can be distrib-
uted and therefore extends the graphs of diversity trends
Fresh water :
100
_ 75
.!!! Hypersaline
--
8.
'15 50
.8
e
~25
Bro(~sh Ultraha line
WD r
0 /
o 5 15 25 35 45 55 65 75 85 95 135 145 +300
Estuary Salinity
Figure 5.20 Hypothetical diversity trend over the fu ll
salinity range including hypersaline waters.
 Chapter 5 Estuaries
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developed for estuaries and hyposaline seas (Fig. 5.20) .
Generally, there is a decrease in diversity with an increase
in salinity from 34 until the ultrahaline conditions are
reached, which are inhabited by just a couple of species.
The Remane diagram can be extended (Hedgpeth 1967;
Fig. 5.20) to demonstrate how the diversity trend over the
full salinity range may be expressed (Fig. 5.20) .
5.5.3 Lagoons
Lagoons are comparatively small areas of sea that have
been semi-isolated by the development of a barrier. Super-
ficially, they appear similar to systems such as the Sivash,
but generally lagoons are much smaller and in particular
they are very shallow, generally only a few metres deep.
Consequently, they rarely become stratified in the summer
due mainly to wind action, but can vary in size consider-
ably. The whole SE of the USA could be viewed as a series
oflagoons and bar-built estuaries extending 4500 Ian along
the coast. Most are much smaller, the largest in the UK
being the 14 Ian Fleet lagoon in Dorset, England. Lagoons
can form through the development of two main types of
barrier. The deposition of sand can commence offshore,
which eventually builds into a bar with no connection to
the land (similar to bar-built estuaries), thus enclosing a
shallow body of water. An example is the Laguna Madre
in Texas, USA (Fig. 5.19b) . Alternatively, barrier formation
can extend out from the land (longshore barrier), eventu-
ally isolating the lagoon (e.g. the Vistula lagoon, Poland;
Fig.5.19a) .
Lagoons demonstrate a wide range of salinity regimes,
from hyposaline (e.g. Vistula, 0-6) to hypersaline (e.g.
Laguna Madre, 39-62). In rare cases a variable salinity
gradient is apparent over very small scales within lagoons.
an example being the Swanpool, Cornwall, UK. This is a
small, generally hyposaline lagoon with depths < 3 m. A low
sill at the seaward end of the lagoon enables full-strength
seawater to overflow at high tides. Due to its density. this
seawater slides to the bottom of the lagoon creating a halo-
cline with low-salinity water floating on seawater and a fast
transition in terms ofsalinityfrom 4 to 34 (see also ROFIs in
Chapter 8) . In tropical areas, lagoons are often fringed by
mangroves (see Chapter 10); reed beds, e.g. Phragmites are
the dominant fringing plant in temperate areas. However.
due to their size. shallow nature. and comparative stabil-
ity, lagoons often differ markedly from estuaries and other
larger brackish-water systems by possessing a diverse sub-
merged plant community, with macrophytes able to root
on the lagoon floor. The plants present reflect the salinity
of the lagoon, with pond species, such as water lilies (e.g.
Nymphea), present in the more freshwater systems, while
halophytes dominate saline lagoons, in particular sea-
grasses such as Halodule spp. (Chapter 10). The fauna of
lagoons tends to reflect the pool ofspecies in the neighbour-
ing main body of water. but lagoon specialists can occur.
Examples analogous to estuarine species are the lagoon
cockle (Cera.stodermaglaucum) and the snail Hydrobia ven-
trosa .
Halophytes are angiosperm plants that can tolerate
increased salt levels in the sediment. These include sea-
grasses and saltmarsh plants.

Chapter Summary
• Estuaries represent the transition system between freshwater and marine biomes, but most estuar-
ies were only formed following the end of the last ice age 6-10 000 years ago.
• Conditions within tidal estuaries are exceptionally variable, particularly salinity, sediment type,
oxygen, and temperature. This variability results in harsh conditions that are amongst the most
challenging for life in the marine environment.
• Estuarine systems include a mix of freshwater and marine organisms, few of which can tolerate the
physico-chemical conditions present in the mid-estuary. Most successful organisms are excellent
osmoregulators, which are capable of adjusting the balance between their internal body fluid salt
concentrations and those of the external water. These species can be very abundant in estuarine
mud .
• The distribution of organisms within an estuary is not just controlled by salinity. Many organisms
require the presence of mud, or depend on cues from other environmental variables, such as tem-
perature or freshwater flow, to determine where they are found .
• The amount of fresh water entering estuaries from the river has a major influence on the ecology
of the system, affecting production, diversity, and distribution of organisms.
 Further Reading

• Estuaries are exceptionally important nursery grounds for many marine fish species, young fish
exploit ing the high food source and more favourable conditions for survival and growth. In temper-
ate regions, saltmarshes associated with estuaries can also be important foraging areas for juvenile
fish.
• Estuarine food webs are powered by detritus from a range of marine, freshwater, terrestrial, and
estuarine sources, although it would appear that terrestrial carbon is relatively unimportant, despite
vast amounts entering temperate estuaries in autumn and win ter.
• Estuaries are exceptionally important habitats for birds, particularly those on migration . Four and
a half million shorebirds migrate to just the British Isles every yea r; where they exploit the high
biomass of invertebrates in mudflats.
• Many inl and seas, such as the Baltic and Black Sea, have conditions similar to estuaries, but gen-
erally do not have tides. In these systems the salinity gradient is much less variable and marine
organisms tend t o be found at lower sali nities in these seas than in tid al estuaries.

Further Reading
Books
• Adam, P. 1990 . Saltmarsh Ecology. Cambridge Un iversity Press, Cambridge.
• McLusky. D.5. & M. Ell iott. 2004 . The Estuarine Ecosystem: Ecology. Threats, and Management. Oxford
University Press, Oxford.
• Sutherland. W. J. 199 6 . From Individual Behaviour to Population Ecology. Oxford University Press, Oxford.

Key Papers and Reviews

• Attrill, M. J. & S. D. Ru ndle 2002 . Ecotone or ecocl ine: ecological bo undaries in estuaries. Estuar. Coast.
Shelf Sci 55: 929-36.
• Emmerson M. C. et al. 200 1. Consistent patterns and the idiosyncrati c effects of biodiversity in marine
ecosystems. Nature 4 11 (6833) : 73-77 .
• Lotze. H. K.• Lenihan. H. S.• Bourque. B. J., Bradbury. R. H.• Cooke, R G.• Kay. M. C. et al. 2006. Deple-
tion, degradation, and recovery pote ntial of estuaries and coastal seas. Science 3 12: 1806-1809.
• Rowntree, RA. & K.W. Able. 2007. Spatial and temporal habitat use patterns for salt marsh nekton:
implications for ecolog ical fu nctions. Aquatic Ecology 4 1: 25-45.
• Williams S. L. and Grosholz, E. D. 2008. The invasive species challenge in estuarine and coastal envi-
ronments: marrying management and science. Estuaries & Coasts 3 1: 3-20
 Rocky and Sandy
Shores
Chapter Summary
The biodiver sity of the shore is exceptionally high com-
pared to lan d, wi t h all major taxonomic groups represented .
Ecological research on shores has underpinned much of
present-day marine ecology and has strongly influenced
mainstream ecology. In addition, shores are of increasi ng
concern to governmental policy-makers becau se of their
recognized provision of goods and serv ices for humans,
6.1 Introduction
The habitat created at the point where the land meets the
sea is the most accessible part of the m arine environment for
humans. To explore deeper and further out to sea requires
rafts, canoes, or larger vessels and involves increased risks,
wh ile the shore itself, including adjacent shallow waters,
offe rs rich resources that can be collected wit hout great
effort. It is therefore no surprise that early human settle-
ments abound on coastlines, a pattern of habitation that
persists to the present day.
Shores are studied because they are accessible, taxo-
nomically relatively simple, and provide ecological goods
and services to society (see the Preface and Chapter 16
for a definition of goods and services).
Early m arine biologists found the shore attract ive for
their science for similar reasons of access ibility and the
diversity of habitats and their associated fauna. The biodi-
vers ity of the shore is exception ally high compare d to land,
with all major taxonomic groups represented (even insects,
if you look hard enough) , and the fauna and flora are eas-
ily collected for study or m anipulated experimentally. As a
such as coastal d efence, recreat ion , and fisheries p rod-
ucts. Shorelines around the world are experiencing maj or
impacts caused by human po pulat ion pressure and there is
a necessity to defend our economic and soc ial investment
in coastal development from the effects of accelerated sea-
level rise. Understanding how shores function ecologically
is therefore important not simply for intellectual reasons, but
for practical purposes if their full value is to be maintained .
result, it is not surprising that ecological research on shores
has underpinned much of m arine ecology and has been the
laboratory of prefere nce for m any m ainstream ecologists.
In addition , shores are of increasing concern to govern -
mental policymakers because of their recognized provision
of goods and services for humans, such as coastal defence,
recreation, and fisheries products (Duarte 2000), and the
curre nt threats to these services (Brown & McLachlan
2002 ; Kenn ish 2002; Thompson et al. 2002). Shore lines
around the world are experiencing m ajor impacts caused
by human population pressure and there is a necessity
to defend our economic and social investment in coastal
development from the effects of accelerated sea-level rise
by spe nd ing many millions of dollars on coastal defence
projects. Understand ing how shores function ecologically
is therefore important not simply for intellectual reasons,
but for practical purposes if their economic value, as well
as their aesthetic and cultural values are to be m aintained.
Shorelines around the world are experiencing increasing
pressure from human developments that threaten their
physical and ecological integrity despite our increasing
dependence on the services provided to human society.
 6.2 What is the shore?
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6.2 What is the shore?
Defining the shore is not as straightforward as it might
seem. The early domination of shore ecology by north-
west European and North American scientists who worked
in macro-tidal areas has resulted in a very restricted per-
spective of a shore : the area between high- and low-water
marks. As a result, shore ecology became synonymous with
intertidal ecology. This was unfortunate for several rea-
sons. First, many shores around the world do not experi-
ence significant tides and in such areas changes in air pres-
sure will cover and uncover the shore to a far greater extent
than tidal action (Fig . 6.1) . Second, the distribution and
abundance of shore biota were inevitably understood in
the context of tidal rise and fall, yet tides per se cannot be
responsible for these patterns (Figs 6.1 and 6.2) . Third, the
emphasis on tides as a controlling factor promoted the view
that physical variables limited the distribution and abun-
dance of shore organisms and thereby distracted attention
away from the importance of biological processes. Fourth,
the functional influence and extent of the shore may extend
far into the terrestrial hinterland and down beyond the surf
zone hundreds of metres offshore (Brown & McLachlan
1990). The influence ofthe shore extends even further if a
larger scale perspective is taken to include the supply oflar-
val stages from offshore water masses. the origins and end
points of migratory taxa such as turtles and shorebirds, and
the material linkages between shorelines ofdifferent types.
Thus, as for other marine systems, defining 'the shore' is
quite an arbitrary exercise and understanding patterns and
processes within an area like the intertidal zone requires
acknowledgement of a much larger scale system within
which that limited area of habitat is set.
Not all shores experience significant tides, yet they sup-
port a typical 'intert idal' fauna and flora. The functional
extent of the shore extends well above and well below
normally recognized limits.
In this chapter, the focus is very much on rocky and
sandy shores. Other kinds of shore habitats (estuary, man-
grove, tropical reef) are dealt with elsewhere in this book,
but given the broader network in which rocky and sandy
shores operate, reference to these other systems draws
attention to the important ecological linkages that exist
between them.

(0) Environmental gradient (bJ (I)

A
I A A

-~ -~ -~
~

Mean high tide

Sea
Rolk
\ Rock Rolk

Sea Sea
~

"- ~ \. Mean law tide

Figure 6.1 The wet-dry gradient (a) t hat characterizes the shore is set up by the interface between water and air. Waves
will extend this gradient up and down the shore (b), and tides (where present) further amplify the grad ient (e). The effect
of the tide is th us to greatly expand an existing gradient, tides do not create the gradient per se.

Figure 6.2 Zonat ion patterns on contrasting shores. (a) Lichens and brown algae form distinct bands on an artificial
rock wa ll at Pwllheli, North Wales, an area that experiences sign ificant tidal rise and fall of a few metres. (b) A typical
shoreline in an essentially atidal area at Tjarno, Swedish west coast. (c) The angiosperms Spartina and Sa/icomia form
characteristic zones at the edge of a salt marsh, Sylt, Germany.
 Chapter 6 Rocky and Sandy Shores
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6.3 Environmental gradients
and the shore
The shore is characterized by several environmental gradi-
ents (termed ecoelines elsewhere; e.g. Whittaker 1974) .
These gradients interact and intersect in quite complex
ways to generate specific environmental conditions for
shore organisms. All other things being equal, specific and
predictable biological assemblages will be found at the
intersections of these gradients according to their physical,
competitive, and physiological abilities to occupy particular
sections of the gradients. a phenomenon known as zona-
tion (Figs 6.2 and 6.3) .
Different species have different physiological and eco-
logical tolerances and hence occupy different sections
of environmental gradients.
Four main gradients can be recognized on shores: wet-
ness/dryness; exposure to wave action; substratum particle
size; salinity.
6.3.1 Wetness/dryness
The wetness/dryness gradient is set up at the tension
between water and air. The environment becomes progres-
sively drier with distance from the water surface and this
gradient is amplified (not created) by waves and tides (Fig.
6.1) . Almost all of the plants and invertebrates encountered
on rocky and sandy shores are marine aquatic in phylo-
Species A
- Inueasingly stressful Enviran.mental Increasingly benign-
gradient
Figure 6.3 Zonation of two species along a generalized
environmental gradient running from stressful to benign
conditions (with respect to the organisms). The two
species A and B occupy different sections of the gradient
according to their ability to tolerate physiological stress
(left-hand tail of the distribution) or biotic interactions
(right-hand tail of the distribution; see also 6.4). Note that
for terrestrial taxa, such as saltmarsh plants, the sea is a
stressful environment, while for marine taxa, it is the land
that is unfavourable.
genetic origin (Fig. 6.3), and the majority require access
to the marine environment to complete their life history.
Generally, species have different requirements (tolerances)
and are able to live further or nearer to the water surface
according to these tolerances. It does not follow that high-
shore organisms cannot withstand immersion in seawater:
many appear to be restricted to high-shore levels because
ofbiological pressures (e.g. predation or competition) from
species living at lower shore levels (6.4.1 and Chapter 1).
Most shore species are marine in origin and need regu lar
access to the sea
6.3.2 Exposure to wave action
A feature of all coastlines is that they experience wave
action to varying degrees (Box 6.1) . Waves are generated
by the frictional drag of wind on the sea surface: the longer
the distance over which the wind blows (termed fetch), the
higher the waves. Waves may also arrive on the shore in
the form of swells; these are the ghosts oflarge, wind-gen-
erated waves produced by storms far offshore. The forces
expended when waves arrive at the shore will depend on
how much energy is extracted through friction as a result of
direct contact with the immediate offshore substratum and
any associated biological structures, such as kelp forests,
reefs, or sandbanks. Thus, shallow sloping offshore areas
will tend to dissipate the energy in the waves arriving at
the shore, while steeper cliffs with deep water at their base
will experience a much greater physical impact of wave
action. Because waves are wind-generated, physically shel-
tered localities, such as fjords, narrow estuaries, and shores
facing away from prevailing wind directions, will have less
wave action on average. Wave action, of course, will vary
daily and seasonally. Many of the anatomical and behav-
ioural attributes of shore organisms reflect adaptations to
minimize the risk of dislodgement by wave action and this
allows different species to occupy different sections of the
exposure gradient.
Wave action is a major determinant of commun ity struc-
ture and composition , as well as individual shape, form ,
and behaviour.
Shore ecologists use the terms 'wave action' and 'expo-
sure' synonymously, and the latter should not be confused
with exposure to air when shores are exposed by receding
tides, more properly termed 'emersion'. In addition, the
concept ofexposure to wave action is difficult to apply sensi-
bly to sandy beaches and mudflats, because of the complex
interactions between particle size, beach slope, and wave
energy. Sediment shore ecologists thus prefer to describe
a beach as having a particular morphodynarnic state that
 6.3 Environmental gradients and the shore
Box 6. 1: Wave formation
Waves are generated by friction from wi nds at the air!
water interface. The length of fetch (the distance over
which ai r moves unimpeded by a land mass) , wind speed,
directio n, and duration, and the depth of water all affect
the period and height of waves. Waves can conti nue
to be propagated even wi thout the influence of wi nd,
this is known as swell , which decays gradually over time
in the absence of wind. Coasts that are exposed to the
ocean typically have swell with a long period. Given the
..- .
,
, Surf or breoker zone
-a
! !
.~
E Reformed WOVe!; reform
~
Uprush wovei break indeeper water
~ ....
Bockwoih
sutter
Ofkhore bar
occupies a point along a reflective-dissipative spectrum,
rather than a wave exposure grad ient (see 6.3.5) .
'Morphodynamic state' is preferred to the term 'w ave
exposure 'to describe sandy beaches and mudflats.
6.3.3 Particle size
Shores can be ordered along a particle-size gradient rang-
ing from extremely large particles, such as a cliff or boul-
der beach, to those made up of very fine particles only a
few microns in diameter (Fig. 6.4). Large particles provide
a stable surface for attachme nt, and epifauna and flora
dominate such shores. In contrast, finer particle sands are
Box 6.2: Macrofauna and meiofauna
In addition to the commonly encou ntered larger infauna
of beaches and mudflats, such as clams, shrimps, and
polych aete worms, a rich variety of tiny organisms live
on, and between, t he individual par ticles, including
nematodes, harpacticoid copepods, gastrotrichs, archaic
groups of polychaetes, kinorhynchs, and flatworms. These
are grouped together as the meiofauna. Because of thei r
small size (typically less than a milli metre) these taxa are
not familiar to most marine b iologists, let alone the non-
expert. They occur in very large numbers, hundreds per
10 0 em" of beach, and because of thei r small individual
body size (only a few fl9) , they have high res piration rates
right seabed conditions, these coasts produce some of
the best waves sought by surfers. Althoug h the surface
features of waves are clear to see, internal waves occur
beneat h the surface, which decay towards the seabed.
These internal waves rarely persist beyond a depth of
50 m. However, as waves pass into shallower areas, the
internal waves will create physical disturbance on the sea-
bed, which will increase with decreasi ng water depth. This
produces a gradient of wave distu rbance on the sea floor
that decreases with distance offshore and with depth.
•
Outer lineof Wove«est Wove«est
breckers
I
\..Wove trough !stillwater level
Oceanbonom"
often too unstable to permit surface attachme nt and the
fauna lives within the beach (the infauna and meiofauna;
Box 6.2) , unless wave action is sufficiently low. Shores of
intermediate particle size are very inhospitable for marine
life because they are too unstable for surface dwellers and
are comprised of particles that are too large for an infau-
n allifestyle (Fig. 6.4). Thus, different species are capable
of living in d ifferent sections of the particle size grad ient
and many of them are specialized to cope w it h the unique
conditions presented.
The sizes of the particles that make up the shore have a
huge effect in determining the kinds of organisms that
can survive there.
per unit mass. This means that their energetic importance
can be as high, and in many cases higher, than that of
the macrofauna in the beach. Meiofaunal taxa also occu r
on rocky s hores (Hicks 198 5; Gibbons & Griffiths 1986)
in association with the microhabitats provided by large r
species, but they have been less well studied than those
in sediments. Notwi thstanding thei r small size and thei r
taxonomic and identification challenges, meiofauna are an
extremely rewarding group to work with, since so little is
certai n about thei r ecology and functional importance in
marine intertidal systems. For an excellent website dedi-
cated to meiofauna see: www.meiofau na.org
 Chapter 6 Rocky and Sandy Shores
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The physical refuge provided for infaunal taxa by fine
particle shores brings additional challenges. Coarse (sandy)
and fine (muddy) particle beaches will present very differ-
ent physical and microbiological environments, mainly due
to their differences in surface area available for microbial
activity and their capacity to retain water at low tide (Fig.
6.5) .
6.3.4 Salinity
This gradient has been largely dealt with in Chapter 5 and
only a summary is provided here for completeness. The
salinity gradient is generated by the meeting of fresh water
and seawater and the habitat where this occurs most obvi-
ously is the estuary. Here. river water with a very low con-
centration of ionic salts meets marine water with very high
levels of such ions. The degree of physical mixing between
seawater and fresh water can range from very little. with
the less dense fresh water flowing over the top of the marine
water. to complete mixing, where turbulence by large waves
can result in similar salinities at the water surface and the
seabed. The exact nature of the mixing and hence struc-
ture of the vertical and longitudinal salinity gradient will
be variable for anyone estuary. depending on the relative
volumes of fresh and sea water, wind-driven physical tur-
bulence that results in mixing of fresh and sea water and

I'I _~"" Ihl lei

-.

Idl lei

IgI ~~ Ihl
Epifcunc/flcrc Epifo un9 cnd

Infounc
.. --
mccrophytes;

Nc mccrobictc

;11 £fEo Ai"

{Iilh Laflle boulden Small bou lden Cobble! Shingles (ool'llllOnd Fi nelll nd ",
(Tens of melT1is) (Me/res) (Centimetres) (Millime/res) (Microns)

Figure 6.4 The environmental gradient of particle size, ranging from large rocks and cliffs to mud composed of grains
only a few microns in diameter: (a) exposed cliff (Otago Peninsula, New Zealand); (b) sheltered cliff (Little Loch Broom,
Scotland); (c) boulder shore (Isle of Wight, England); (d) shingle beach (Norfolk, England); (e) sandy beach (Clacton ,
England); (I) mangrove (Manakau , New Zealand); (g) seagrass bed (Moray Firth, Scotland). (h) Shore organisms can only
live on the sides of the larger particles (epifauna and flora), and between the particles (infauna) on sandy beaches and
mudflats (except in extremely sheltered habitats where some epifauna and flora reappear). Intermediate-sized particles
that make up shingle and cobble beaches present a hostile environment for both types of organism, because they are
too large to retain water and too mobile for surface attachment.
 6.3 Environmental gradients and the shore

spring-neap tid al patterns. The distribution of t he fauna

and flora along this gradient will thus represent a response
to the average cond itions present. The majority of species
found in estuaries are marine in origin, wit h few freshwater
taxa penetrating far downstream.

• • • 6.3.5 Interactions between gradients

Mud Fine sand Coarse sand
.. • action will amplify the wetn ess-dryness grad ient, and
o -----
-§
- -- -- -
l-
20
o Reducing 0 Oxidizing
Figure 6.5 The ave rage parti cle size t hat ma kes up
sandy beac hes and mudflats has a profound effect o n
the physico-chem ical co ndit ions experienced by the
infauna. Mud s have a mu ch g reater surface area available
for micro bial activity by virt ue of th eir small individual
particle s ize. They a lso reta in water better than sands and
a re usual ly waterlogged. Th e mi crobial activity reduce s
co mpounds, suc h as iron and sulp hate, in th e sed iment
creati ng ano xic co ndit ions the extent of which is refl ected
in th e depth at which the sedi ment changes co lour from
o ra ngey-brow n (oxi dize d iron particles) to dark brown o r
black (reduced iron sulphi de) (see also Cha pte r 8).
and zonation patterns
All t he above grad ients interact to generate particular con-
d itions for life on shores. For instance, increasing wave
t hereby uplift biological zones w it h increasing wave expo-
sure. Wave action and water movement will sort particles
according to their mobility and in the process drive the
overall beach environment towards a more reflective or a
more d issipative morphodynamic state (Table 6 .1) . The
interactions between salin ity and particle size are complex
and dealt wit h in Chapter 5.
The types of fauna and flora recorded at any location on
a shore can be understood as the biological responses to the
product of these interacting gradients, allow ing for bioge-
ography (Chapter 1). The overall patterns of d istribution
and abundance are revealed as zonation patterns, which
are most obvious on exposed macro-tidal rocky shores, and
least obvious in sheltered sandy fl ats. Not surprisingly, we
understand much better the processes maintaining rocky
shore zonation t han is the case for other shore habitats.
One of the most important features of roc ky shore zon a-
tion patterns is the similarity that occurs worldwide. These
were described most elegantly by Stephe nson and Ste-
phenson (1949, 1972 ), in a period when marine ecology
was developmental and more descriptive. Similar, but not
identical, types of fauna and flora occupy similar positions

Table 6 .1 So me of the features of beaches at th e ext reme ends of th e morpho dynamic spect ru m. Intermediate
morphodynami c stat es have intermediate f eatures. After Raffaelli and Haw kin s (1996).

Dissipative beaches Reflective beaches

Sediments Fine Coarse
Waves Small Large
Slope Shallow Steep
Swash conditions Benign Harsh
Fauna Rich Impoverished

(,j Ib}r-- - - - - - - - "'I Di ssipative (a) and

refl ective (b) beach es o n
the Co ro mandal coast ,
New Zealand .
 Chapter 6 Rocky and Sandy Shores
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on shore gradients, independent of biogeographical region structuring processes that operate on all rocky shores: only
(Fig. 6.6) . The significance of these universal features of a limited range of body forms and phylogenies can cope
zonation is that they imply similar and strong underlying with life on shores. Also, these consistencies in the major

Figure 6.6 The universal zonation

scheme proposed by Step henson and
Stephenson (1972). The main zones
are where biota occur worldwide,
with slight modifications according
to biogeography. This zonation is
well-illustrated by this rocky shore on
the Otago Peninsula, New Zealand
(left), or the Nort h American example
(above). In the North American
exam ple, Pisaster starfish can be seen
Supra linoral fringe lying j ust beneath the band of black/
,:~....~ ~IQ(k lichen and litterlnld snoil.1 blue mussels on a shore in Vancouver
Island, Canada. These voracious
predators limit th e lower distribution
Mid-Iinoral zone
of the mussels and actively contri bute
(barnacles, mussels)
to th e creation of d ist inct zonation
patterns as d iscussed later in this
chapter. Photograph: lain McGaw.

,
...-...-...-...-:;:~~~fra-littOrOI fringe (large kelps]

--
oo.l';

-- -
~\..""'- --
__ - ~
""
Infro-linoral zone

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
zoning species worldwide have permitted the invention
of a spatial referencing framework for the unambiguous
location (within a shore) of where particular studies were
undertaken (Fig. 6.6) . Thus, the term midlittoral (or eulit-
toral) would conjure the same mental image of a shore
habitat for all rocky shore ecologists.
Remarkably similar general patterns of zonation recur
throughout the world which offers interest ing possibili-
ties to undertake comparative studies .
Similar schemes have been proposed for sandy shores
(Fig. 6.7), and there is some evidence of universal zonation
patterns for crustaceans (Dahl 1952). However, most general
environment of the beach, rather than its biology (Salvat
1964).
6.4 Causes of zonation
Given the striking zonation patterns seen on rocky shores.
and to a lesser extent on sandy shores and mudflats, it is not
surprising that a major preoccupation of shore ecologists
has been discovering the determinants ofzonation. Earlier
workers naturally assumed that the tides must be in some
way responsible. given the intimate association between
the so-called intertidal area and the twice-daily rise and fall
of the tides. Various schemes and theories were advanced.
exemplified by the critical tidal level arguments put forward
by Colman (1933), and later developed byDoty (1946) and
others. It was argued that as one moved down the shore,
there were certain regions where only small differences in
shore level were characterized by large changes in the period
of immersion. when averaged over a year. In other words.
the immersion-emersion gradient was particularly steep at
these points and thus critical for any species that decided to
settle in these regions. Upper and lower distributional limits
of several species seemed to coincide precisely with these
critical levels. While plausible, indeed compelling, Under-
wood's (1978) re-examination of this theory revealed the
basic science as thoroughly flawed. species' distributional
limits occurred haphazardly along the shore rather than in
groups, and re-plotting of the tidal data did not support the
idea of critical levels. Nevertheless, the concept lingers on
in several marine ecology textbooks. perhaps because of a
reluctance to take the tides out ofintertidal ecology.
Zonation patterns on shores cannot be explained by
ti dal rise and fall. The concept of a critical tidal level
that dictates e ntirely the patterns observed on shores
still persists in some marine ecology textbooks. This is
an out-dated concept and should be t reated accordingly.
6.4 Causes of zonation
Dahl's scheme
Figure 6.7 'Universal' zonation schemes for sandy
beaches provided by Dahl (1952) based on the
occurrence of crustacean groups, and Salvat (1964)
based largely on the degree to which water is retained by
the sediment.
Given that the majority of species encountered on rocky
and sandy shores are marine and aquatic in origin. we
should not be surprised that the upper zonal limits of a
large number of species have been shown to be associated
with physiological tolerance to factors such as desiccation
and thermal stress. In general, experiments have shown
that species found higher on the shore are more able to tol-
erate dryness and thermal stress than lower shore species.
Many of the experiments have been focused on adult indi-
viduals, but it is often the environmental conditions experi-
enced by the recruit (larval) stages that more importantly
determine the adult distributions, especially for sessile
taxa. such as barnacles and mussels. The juveniles of many
mobile taxa. such as marine snails, recruit onto lower shore
levels, and later migrate to higher levels as they become
larger and their physiology alters such that they can cope
with harsher environmental conditions. Juvenile stages of
most species (terrestrial oraquatic) tend to be the mostvul-
nerable to stress.
Upper dist ributional li mits of species are generally (but
not always) set by t heir to le ra nce to physical factors.
The determinants of lower zonal limits are not easy to
attribute to physical faerors. Why should aquatic organisms
require a certain period of drying? Several pioneering stud-
ies (e.g. Baker 1909) demonstrated that high intertidal spe-
cies actually grew better under a lower shore tidal regime,
while Stephenson and Stephenson (1949) suggested that
competition and/or predation might be responsible for
some zonation patterns. However. it was Joseph Connell's
 Chapter 6 Rocky and Sandy Shores
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
now classic experiments on the determinants of zonation
patterns in the barnacles Chthamalus montagui and Semi-
balanus balanoides that provided the most rigorous argu-
ment for biological factors setting lower distributional
limits ofshore species (Connell 1961a, 1961b) . The persua-
siveness ofthese experiments lies in the controlled manipu-
lation (removal in this case) of one species (Semibalanus
balanoides) occupying the zone immediately below another
potentially competitive species (Chthamalu.s montagui).
Connell was able to show that in the absence of competi-
tion for space, a limiting resource on his rocky shore, the
higher shore species could survive at lower shore levels
than those at which it was normally found . This manipu-
lative approach to understanding the determinants of
zonation patterns has been emulated repeatedly by many
workers. As a result, it is now something of a paradigm in
rocky shore ecology that lower distributional limits of spe-
cies occur as a result of biological factors, while physical
factors set upperlimits to distributions. However, there are
exceptions, especially amongst the macroalgae (Hawkins
& Hartnoll1983). Thus, grazers may prevent the upshore
extension of foliose seaweeds on some Australian shores
(Underwood & Jernakoff 1981), red and brown seaweeds
grow further upshore in the absence of limpets on the Isle
of Man (Hawkins & Hartnoll 1985), and the green seaweed
Codium may be partly limited by grazing from above (Ojeda
& Santilices 1984). Notwithstanding these exceptions, an
intriguing question posed by this paradigm is whether it is
applicable to the zonation patterns that occur along other
kinds of gradients, particularly the wetness-dryness gra-
dient on sandy shores, but also to salinity, exposure, and
particle size gradients in other habitats.
Competition and predation have been shown to be
important determinants of lower distributional limits of
species on many rocky shores.
There has been very little exploration of this question
for the last three environmental gradients, but some work
has been done on zonation patterns on sandy shores.
One of the issues for sandy shore (and mudflat) ecologists
is that the description of zonation patterns in these habi-
EHWI ~-~------;'::~:
----""
ElWI
tats requires the destruction of the medium in which the
organisms live: quantitative sampling involves digging out
volumes of sediment and separating the fauna, usually by
sieving or elutriation. Nevertheless, this approach reveals
zonation patterns that are usually not visible at the sedi-
ment surface (Fig. 6.8) .
Zonation patterns, as well as their underlying causes, are
much harder to detect on sandy beaches and mudflats.
Marine ecologists have sought to understand the role of
individual species within sediment communities by system-
aticallyremoving particular species and studying the conse-
quences. Carrying out such species removal experiments in
sandy beaches or mudflats is fraught with interpretational
problems if the habitat has to be disrupted to such a severe
extent. Just think how difficult it would be to remove 10
individuals of one species from a patch of sandy beach that
contains 100 individuals comprising 20 species. A second
problem arises in that, unlike the sessile fauna of rocky
shores, the infauna is mobile and can easily move back into
areas cleared in manipulative experiments. In other words,
it is difficult to maintain the integrity of the experimental
design ofspecies removal experiments (but see Techniques
box) . Third, the beach fauna lives in a three-dimensional
environment and displays zonation verticallyas well as hor-
izontally, and some species redistribute themselves at each
high tide. Experiments aimed at removing potential com-
petitors therefore have an additional layer of complexity.
Fourth, it is not clear whether space is a limiting resource
for which competition occurs in sandy beaches and mud-
flats, in the same way that it does on rocky shores. Certainly,
the intensive interference competition, where individuals
overgrowor crush one another, that is seen between space-
occupying species on rocky shores is virtually absent in sedi-
ment assemblages, probably because individuals tend to be
mobile (as opposed to the many attached biota found on
rocky shores) and can simplymove awayfrom one another.
Space is not such a severe constraint on sandy shores
as the fauna are mobile and can relocate to avoid com-
petition.
Figure 6.8 Zonation on
a sandy beach , Newburgh,
Scotland. Only the most
abundant species are
represented for the sake of
clarity. Data from Raffaelli
et al. (1991).
 6.5 The organization of shore communities
Despite these issues, several investigations have demon-
strated the importance of physical factors in setting upper
distributional limits, such as Petersen and Black's (1987,
1988) transplant experiments of the bivalves (Circe and
Placamen ) to higher shore levels, where they grew more
slowly and suffe red higher mo rtality due to physical fac-
to rs. The importance of biological factors in setting distri-
butionallimits is illustrated by Posey's (1986) study of a
Californian beach. Here, the burrowing activities of the
ghost shrimp Ca llianassa excluded a tube-dwelling worm
Phoronopsis from higher shore levels, while the lower distri-
butionallimits of the shrimp were probably set by predation
by a fish, the sculpin Leptocottus. Such manipulative stud-
ies are few and far between and, as in the case of Posey's
study, both upper zonal limits may be set by biological inter-
actions. Clearly, the factors responsible for zonation in a
three-dimensional habitat, such as a sandy beach, are not
as clear as for two-dimensional rocky shores.
6.5 The organization of shore
communities
In common w ith all other biological assemblages, shore com-
munities are organized by a combination of top-down (con-
sumer-driven) and bottom-up (resource-driven) processes.
Many of the classic studies on top-down processes in food
webs were first performed on rocky shores . Consequently,
there has been a tendency to generalize these results across
all shores and even across all types of ecosystem. Notwith-
standing the fact that some of these earlier studies would be
unlikely to pass the present-day peer-review process (Box
6.3), they have made a major contribution to mainstream
ecological theory. Before we discuss the relative importance
of different processes in the dynamics of shore assemblages,
it is worth rehearsing the features of shores that make them
so amenable to studying these kinds of questions.
6.5.1 The role of field experiments
Of all the arguments that can be used to convince scientists
that a particular viewpoint is correct, the experimental fal-
sification of hypotheses has proven the most persuasive (i.e.
the rejection of the null hypothesis). Field experiments
h ave to be properly designed and analysed so that there is
no ambiguity in their outcome (Underwood 1981 , 1997;
Hurlbert 1984, Huston 1997) . An important aspect of their
design is that the experimental plots (areas wit hin which
the manipulation occurs) need to be replicated many times
and dispersed appropriately over the study area (see Chap-
ter 15 ). This is often very difficult to achieve for many types
of taxa and ecosystem (Raffaelli & Moller 2000) , but not
for shores . The small body size, high dens ities, and small-
scale nature of spatial patterns of shore species means that
Box 6.3: Manipulative field
experiments
The most convincing manipulative field experime nts
are those in which the treatme nt and control plots are
highly replicated to provide the necessary statistical
power to detect an effect of a particular manipulation.
Such powerful designs will convince the most critical
reviewer or edi tor (see Chapter 15) . It is therefore
somewhat ironic that the two rocky shore experiments
that ecologists are completely persuaded by are fatally
flawed in this respect. The first is Lodge's (1948)
removal of the limpet Patella from a wide strip run-
ning down a shore on the Isle of Man, UK, and the
subsequent bloom of algae in the manipulated area.
The second is Paine's (1974) set of experime nts on
Pisaster on the Washington coast, where removal of
the starfish saw a massive increase in mussels and
a collapse in community structure (Fig. 6.9). Neither
study used a properly replicated experimental design,
and there were essen tially no controls (Raffaelli &
Moller 2000). Yet the scientific commu nity is per-
suaded by these experime nts that Patella and Pisaster
are keystone species. Why? Because (a) the effects
were so dramatic, and (b) the resultan t changes in
abundance and distribu tion of algae and mussels were
completely outside the 'norm ' for similar rocky shore
commu nities. However, Lodge and Paine were lucky
to get away wi th it: the effects of predator removals
are often much more subtle and a proper experimental
design is advised to all would-be manipulators!
For fu rther discussion, see Raffaell i and Moller
(2000).
many relative ly small plots can be located w ithin a small
spati al exte nt. The three-dimensional variation w it hin
shore sed iments is usually compressed into a layer no more
than 20 em deep. In addition, processes of interest tend to
operate over relatively short ecological time-scales (weeks
to years), allowing them to be investigated wit hin the tradi-
tional 3- to 5-year research grant period. Finally, of course,
shores are highly accessible and en able sampling to occur
with high precision; you can be sure that you collected your
samples from w ithin the experimental plot you intended
to sample. These features mean that it is much easier to
investigate certain types of processes on shores compared
to other habitats, such as forests or the deep sea.
The outcome of experimental manipulations of shore
communities are only persuasive if executed correctly
and unambiguously.
 Chapter 6 Rocky and Sandy Shores
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However, while sh ores are highly amenable to the
experimental manipulative approach, not all questions
can be satisfactorily addressed in this way, especially those
questions concerned with processes that operate over large
spatial and long temporal scales (Raffaelli & Moller 2000) .
Seductive as they are, field experiments are not the answer
to every problem, although they are a powerful investiga-
tive tool.
Despite the experimental design issues that surround
some of the earlier field experiments (Box 6.3), there is no
doubt that top-down processes are of prime importance on
some kinds of shore. Experiments involving the removal
of suspected key consumers. such as predatory starfish.
or whelks. and herbivorous sea urchins or limpets, have
often revealed strong competitive interactions between
species whose populations are regulated by the available
spatial re source (e .g, the availability of rock surface forthe
settlement of barnacles) . Often a competitive dominant
emerges in the absence of the consumer, with a resulting
loss of inferior competitors and a lower overall commu-
nity biodiversity (Fig . 6 .9) . While such experiments are
dramatically effective in demonstrating the importance of
top-down control by what have become termed keystone
predators, their outcomes need to be placed in context
(Pace et at. 1999) .
6.5.2 Keystone predator or prey?
The keystone status of starfish, such as PiseLSter (Fig. 6.9),
or limpets, such as Patella, is not due to any inherent attri-
butes of these species. Their status depends entirely on the
response of their prey resource to reduced consumption,
and in that sense the actual identity of the consumer is irrel-
evant. In other words, the factors that drive the competitive
dynamics of the prey should be the focus of investigation.
For instance, while Pisaster has been shown to be a key-
stone predator on exposed coastlines along the northwest-
ern USA, on other shores this is not the case. Similarly, the
whelk Morula has an organizing role on some shores in New
South Wales, Australia, but not on all shores (Fairweather
& Underwood 1991) .
A keystone species may simply be another 'brick in the
wall' in different circumstances. In other words, the iden-
tity of keystone species can be highly context specific.
One factor that determines whether a 'keystone effect'
will be seen in the relatively simple communities of temper-
ate systems (see below) is the recruitment dynamics of the
dominant prey. This realization has led to the development
of an extremely important, but at the same time incredibly

Keystone
predator

Superior Spedes-rlth
prey assemblage

Plscster, USA Slkhcster, New Zealand

, - - - - - - --,
: Keystone : 15 20
: predator :
~------- ~

, ,,
, ,
'- , ,
,, ,,,
, ,
L __ I
10

Superior Spedes-pcor
prey assemblage
5'- -' 0'- -'
Starfish present Starfish removed Starfish present Starfish removed

Figure 6.9 The role of keystone predators in maintaining species' richness. Left top: a strong controlling interaction
between a competitively superior prey and its predator permits the coexistence of an associated module of other
species. Left bottom: breaking the link releases the superior prey, which monopolizes the resources on which the modu le
species depend (after Paine 1980). On the right are examples of how species' richness is reduced in the absence of
keystone starfish in the US and New Zealand (after Raffaelli and Hawkins 1996).
 6.5 The organization of shore communities
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
challenging, area of shore ecology known as supply-side
ecology (Gaines & Roughgarden 1985; Gaines et al. 1985;
Lewin 1986) . The significance of this area is best demon-
strated by considering the dynamics of species with off-
shore early life-history stages, such as barnacles. mussels,
and algae. Recruitment of these taxa usually occurs every
year, but it is the strength of a particular year's cohort of
recruits that will determine the outcome ofcompetition and
hence community organization on the shore. Heavy recruit-
ment by the dominant competitor will. in the absence of
a consumer. lead to the exclusion of inferior competitors.
However. if recruitment of the dominant competitor is poor.
other species will not decline in the absence of the so-called
keystone predator. These processes are also critical deter-
minants of the likelihood of the successful colonization of
species that have been introduced into new ecosystems
through human activities.
Population recruitment processes operating far out at
sea may profoundly affect the outcome of interactions on
the shore, especially for those species that have offshore
dispersed larvae.
The central question for understanding the dynamics of
these communities is therefore 'what determines recruit-
ment strength?'. The answer rests in the ocean climate
determinants of the offshore currents that carry the larvae
or spores to the shore. If there are plenty of larvae in the
currents and if these sweep the shore at the right time. then
recruitment will be strong. In this respect it is unfortunate
that there has been an emphasis on the keystone nature of
the consumer, because the dynamics of these shores may
in fact be driven by events hundreds of kilometres offshore.
If this larger-scale perspective is taken, it could be argued
that bottom-up, not top-down processes organize the shore.
Finally. in shore communities with a more complex set
of predators. such as those found on many tropical shores
(Menge & Lubchenco 1981 ; Menge et al. 1985) and in tem-
perate estuaries and mudflats (Reise 1985; Raffaelli & Hall
1992), the removal of anyone predator does not usually
lead to the kinds of cascading effects documented for some
temperate rocky shores. since the remaining species simply
mop up any released prey resource. This effect is known as
diffuse predation (Hixon 1991) . Keystone predators are not
therefore a characteristic of such shores.
6.5.3 Primary and secondary space
Top-down effects on shores are most obvious between con-
sumers and those prey species that are primary space-
limited. That is, they compete aggressively for the rock
surface. Such taxa include truly sessile groups, such as
algae. barnacles. oysters, and sponges, as well as semi-
sessile taxa. such as mussels. Interactions between these
taxa are typically of the interference type. including over-
growth, crushing, smothering, and chemical warfare (algal
and sponge allelochemicals) . Taxa that are not sessile can
move away from such interference competition, which
explains why competitive exclusion, and hence keystone
effects. are harder to demonstrate in the mobile species
found in sandy shores and mudflats, as well as for rocky
shore gastropods and amphipods. Thus, by keeping mussel
densities low. Pisaster is partly responsible for maintaining
a high diversity of primary-space occupiers. but reduces
biodiversity overall by reducing the habitat available for
those secondary-space occupiers living in the highly com-
plex mussel matrix. a system ofextremely high biodiversity
on rocky shores (Suchanek 1992) .
The structure created by beds of primary-space occupi-
ers, such as mussels and oysters, permits a high local
biodiversity of associated fauna to develop due to
increased habitat complexity and organic enrichment
from the production of faeces and pseudofaeces.
6.5.4 Bottom-up processes
Despite a great deal of effort, much of it involving manipu-
lative field experiments. it has been hard to demonstrate
consistently an important role for top-down processes
for sandy beach and mudflat communities (Raffaelli &
Hawkins 1996) . These systems often support a much larger
range ofconsumers. including shorebirds. crustaceans. and
fish, which occur in large numbers and have high energy
demands (Table 6.2; Chapter 5) . One might therefore
expect top-down control in such systems, but this has been
difficult to demonstrate experimentally. There are a num-
ber of faerors that might be involved: low natural predator
densities, poor experimental design. prey movement in and
out of cages, inappropriately sized cages, insufficient time
duration for the experiment, and, finally. a real absence of
top-down control (see Techniques box) . There is no doubt
that many experiments that have attempted to discern the
importance of predation in these systems suffer from exper-
imental design problems (Raffaelli & Moller 2000) . Experi-
ments in these habitats are typically short-term (weeks to
months) and may be too short to reveal anything but the
initial, transient dynamics. which mayor may not be the
same as the longer term behaviour of the system. This is
important given that the effects ofcompetitive interactions,
e .g. for food resources, among prey species are likely to be
subtle and long-term.
The outcome of competitive interactions between mobile
species may be much less dramatic than for sessile taxa
because mobile taxa can move to avoid competition.
 Chapter 6 Rocky and Sandy Shores
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Table 6 .2 Exampl es of high co nsumpt ion rates by shoreb irds feedin g on (a) macro phyte stand ing cro p, and
(b) invertebrate produ cti on . Data from Thayer et al. (1984) and 8aird et al. (1985), respectively.
Prey "!o Consumed)
(a) Macrophytes
Zostera 30-75
Ruppia 20
Potamogeton 13
(a) Seagrass bed Moray Firth, Scotland; (b) wading birds that are typical invetebrate feeders.
(, j
- • .. .. '-
•
TECHNIQUES: Experimental
approaches to understand species
interactions in soft shores
The techniques and approaches for sampling and map-
ping the distribution and abundance of shore species and
relevant environmental variables are well-documented, but
there are few guides to help those who wish to explore
dynamic interactions between species, especially for soft
shores. Here, we describe a case study focused on explor-
ing the interactions between species ranging from shore-
birds to small invertebrates, on tidal flats in north-east
Scotland, and which comprise the Ythan food web.
The Ythan food web is relat ively simple, comprising only
c.100 macro-species, but an unknown number of meio-
faunal and microbial taxa. The trophic interactions between
these species are well-documented (e.g. Hall and Raffa-
elli 199 1; Gorman and Raffaelli 2003), but the dynamic
importance of those interactions, and their consequences
for system structure and function, had not been explored
using experimental manipulations of the ki nd pioneered
by rocky shore ecologists. Partly, this was because such
experiments were thought to be too difficult, and indeed
they can be. However, the Ythan team persevered and their
approaches and the lessons learned may be useful for oth-
ers embarking on such experiments, including questions of
how biodiversity is related to ecosystem functioning (see
Current Focus box).
Prey "!o Consumed)
(b) Invertebrates
Ythan estuary 36
Tees estuary 44
Langebaan lagoon 20
Ib)
The essence of any experimental approach towards
understanding the ecological significance of species' inter-
actions is that if two species perform equally well when
they are together and when they are not together, then
there can be no significant interaction between them. Con-
versely, if thei r performance is different in the two situ-
ations, then they must interact in some way. Setting up
experiments w here particular species are either present or
absent requires creative methodologies, especially in the
case of field experiments where the intervention technique
may itself produce so-called 'hidden treatment effects'
(Huston 1997). Below are some ways in which experi-
ments were carried out on Ythan species, in the field and
the laboratory, in order to identify important interactions.
Carryi ng out experimental manipulations like the ones
described above is not for the faint-hearted. A major
advantage of the Ythan is its sheltered nature (we never
lost any experiments due to scouring or to cages being
washed away by storms, unlike our experience in other
more exposed locations). This is important because such
experiments often have to run for a co nsiderable time
(many months). The naturally muddy nature of the site
meant th at increased siltation inside fine meshed cages
was rarely sig nificant. Also, the site is a nature reserve,
minimizing chances of vandalism, and the team were based
on-si te at Culterty Field Station, only a few hundred metres
from the experimental sites. Of course, experiments alone
are not sufficient to fully elucidate all the interactions: we
 6.5 The organization of shore communities

spent a great deal of time doing more empirical natural face, including the fish, so we could be sure that predators
histo ry in order to help us interpret the results and to check we re really present or absent in the different treatments) . If
the integrity of the treatments (many of these species you decide to embark on such experiments, you will need
leave recognizable tracks and signs on the sediment sur- nerves of steel, but the final product is well worth it!

Taxa Response Technique Issues Reference

manipulated taxa

Shorebirds Benthic infauna Large (me-scale] plots fenced No sedimentation effects (cage Raffaelli & Milne
(Redshank (amphipads, and roofed with thin, horizontal 'mesh' is coarse and does not 1987
(Tringa polychaetes. strings, that let fish and slow water flow ) . Strings may
totanus) , Dunlin oligochaetes, epibenthic predators in, but get fouled by drifting algae
(Calidru5 snails) excluded birds. and need to be kept clean
alpina) , regularly.
Shelduck
(Tadorna
.. ~c:~~~~~) .
Eider ducks Mussels Eiders feed by diving onto Because there are no sides Raffaelli et al
(Somateria and their intertidal beds of mussels to the cages, water flows are 1990
mollissima ) associated when they are covered by the natural, but there may be
invertebrate tide. They can be excluded significant shading effects on
community by a simple coarse-mesh roof microbial communities within
suspended on stakes within plots (needs to be explored)
large (m--scele) plots. Other
species, some birds and all fish
and epibenthic predators have
access to mussels.

Ad ult flatfish Benthic infauna Large (me-scale) plots fenced Fouling of cages by drift algae Raffaelli & Milne
(PJatichthys (amphipads, and roofed with coarse mesh can reduce flow s and lead to 1987
ffesus) polychaetes, (several em) exclude flounders. build up of sediment inside
oligochaetes, cages, so they need to be
snails) checked and cleaned reg ularly.
Exclosures like this exclude all
other large predators and have
to be used in conjunction with
the designs described above
to interpret results.
• • • • • • • • • • • • • • • • • • • • • • • ••••••••••••••••••• ••• ••••• •••••• ••• ••• ••• •••••••••••••• ••• •••• ••• •••• ••• •••• ••• •••• ••• •••• ••••••••••••• •• •• •••••••••••
Small fis h Benthic infauna Large (c. 1 m 2 ) enclosures with The relatively small mesh is Jaquet and
(gabies (amphipads, an intermediate mesh ( 1-2 likely to red uce flows and lead Raffaelli 1989
Pomatoschistus polychaetes, cm) to enclose predators. If the to higher levels of suspended
spp) and oligochaetes, substratum is prone to drying material (sediment and
j uvenile flatfish snails) out at low tide, then a short perhaps invertebrates) inside
(PJatichthys 2 -3-cm wall may be needed the enclosure. However,
ffesus) around the inside of the cages because comparisons of
to retain sufficient water. response fauna are made
Also, solid barriers should betwee n cages with fish
be inserted inside the cages at natural densities and
and pushed in flush with the cages without fis h, then
sediment surface to ensure that any difference between the
enclosed fish (and invertebrate treatments cannot be d ue to a
prey) cannot bury out of the 'hidden treatment'.
caged area.
• • • • • • • • • • • • • • • • • • • • • • • ••••••••••••••••••• ••••••••••••••••• ••• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •••••••••••••
 Chapter 6 Rocky and Sandy Shores
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Taxa Response Technique Issues Reference

manipulated taxa

Epibenthic Benthic infauna Relatively small (0.25 m 2 ) The small mesh can be Raffaelli et al.
crustaceans (amphipods, enclosures with a small mesh expected to reduce flow s 19 8 9
(brown shrimp polychaetes, (a few mm, depend ing on and lead to higher levels of
Crangon oligochaetes, the size of the predators) suspended mate rial inside the
crangon and snails) to enclose predators. If the enclosure. However, because
the shore substratum is prone to drying comparisons of response
crab Carcinus out at low ti de, then a short fauna are made between
maenas) 2-3-cm w all may be needed cages with shrimps/crabs at
around the inside of the cages natural densities and cages
to retain sufficient wate r, without shrimp/crabs, then
although crabs and shrimps are any difference between the
usually good at 'digging in' as treatments cannot be due to a
the ti de recedes. Solid barriers 'hidden treatment'.
should be inse rted inside the
cages and pushed in flush with
the sediment surface to ensu re
that enclosed shrim ps and
crabs (and invertebrate prey)
cannot bu rrow out of the caged
area.
• • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •
Invertebrate s Small infauna Solid walled. box cages c.20 As above. Raffaelli and
(ragworm and meiofauna. x 20cm, roofed with fine Hall 19 9 5;
Hediste mesh (500!J m or less) . Cage Lim ia and
diversicolor, pushed in almost flush with Raffaelli 19 9 7
amphipod sediment. Solid sides prevent
Corophium movement in and out of cages
volutator) of manipulated species and of
response species.
• • • • • • • • • • • • • • • • • • • • • • • •• • • • • ••• • • • •• •• •• • • • •• •• • •• • •• • •• • •• • • • ••• • •• • • • • • • • • • •• • • • • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • ••• • • • •• •• •• •• • • • • • •• •

Mussels Epifauna, Sheets (0.25 m 2 ) of mussels Sheets should be kept as Ragnarsson and
(Mytilus edulis) infauna, and removed from within mussel intact as possible (not alw ays Raffaelli 19 9 9
meiofauna beds, rinsed to remove any easy) . Since the effects
associated sediment and of mussels are likely to be
inverteb rates and re-Iaid on via increased deposition
bare ti dal flats. Sheets secured of fine sediment thro ugh
by pegs until firmly attached to red uced flows and mussel
sediment surface. pseudofaeces, this 'hidden
treatment' is not a problem for
interpretation.

Tube worms Infauna and Ar tificial tu be fields (0.25 m 2 The density and protru d ing Ragnarsson and
(Lanice meiofauna plots) created with drinking height of tubes is expected to Raffaell i 2000
conchilega) straws of a similar diameter and have an impact on sediment
shape to Lanice tubes. deposition / erosion rate s. Tops
of tubes act as attachment
sites for filamentous algae,
w hich may be an effect of
interest or an unwanted
'hidden treatment'. Assembling
large numbers of tubes
(typically several thousand for
an experiment) is not the most
exciting job.
 6.5 The organization of shore communities

Taxa Response Technique Issues Reference

manipulated taxa
Lugworms Infauna and Lugworms added to plots (c. All treatments start with Ragnarsson and
(Arenicola meiofauna < 1 m 2 ) of defaunted sediment, defaunated sediment, w hich Raffaelli 2000
marina) other plots left as controls. All is difficult to establish and
sediment caged below surface manouver in large quantities.
with fine mesh. Because all plots are similarly
defau nated , any difference
between treatments must
be due to the presence of
lugworms.
• •••••• ••••• ••••• ••••• ••••••••••••••••••••••••••••••••••• ••• •••••••••••••••••••••• • •••• ••••••• ••••••• ••••••• ••••••• ••••• • • • • • • • • • • • • • •• •• • • • • •
Weed Infauna and Sheets of algae secured to With large plot sizes of several Hull 198 7;
mats (Ulva meiofauna mud flat to produce plot sizes of m 2 , coverage becomes uneven Raffaelli et al.
intestinalis) 0.25 to 5 m" and patchy. 19 98

Manipulative field experiments on the Ythan estuary, Aberdeenshire. Top left: flounder-exclusion cages. Top
right: cages with different densities of gobiid fish . Centre: a cage for maintaining different densities of small
crustacean predators (note barriers that prevent escape from the caged area once the cage is sunk into the
mudflat). Bottom: tracks left by flounders (left) and shorebirds (right) provide evidence that the cages work (or
don 't) at excluding the right predator and that control (uncaged) plots are visited by predators.
 Chapter 6 Rocky and Sandy Shores
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Notwithstanding the above criticisms of manipulative field
experiments in sediment systems, it would seem that bot-
tom-up processes dominate, with predators limited by their
prey. rather than vice versa. Many prey individuals remain
inaccessible to predators, living out of reach for much of
the time within the sediment and only a proportion of the
prey standing stock (as opposed to production) may be pre-
dated. The dominance of bottom-up processes is perhaps
not surprising given that sandy shores and mudflats tend
to be net importers of organic matter from elsewhere; for
example, upstream and along the coast in the case of estu-
aries, and from kelp beds in the case of many exposed sandy
beaches.
Most prey ind ivid uals in mudflats and beaches are
unavailable (Le. buried to deep in the mud) to predators
like shorebirds and fish , and their numbers are driven by
the supply of organic matter and ot her food resources.
6.5.5 Disturbance and bioturbation
A feature of sediment systems. whether intertidal. sublit-
toral or deep sea. is physical disturbance to the structure of
the sediment and alteration of the physico-chemical envi-
ronment by the organisms themselves or external events
such as storms and ice-scour. Species living within the sedi-
ment move through it. ingest and egest particles. and draw
oxygen-rich water down from the surface to depth (Rhoads
1974) . This local-scale biological disturbance (bio turb a -
tion) can change the environment for other species. for
instance by loosening and destabilizing the sediment fabric
and making it more vulnerable to erosion by water move-
ment. Alternatively. species that pump oxygenated water
through burrows create a more favourable environment for
other species (Fig. 6.10; Box 6.4; Chapter 8) .
In addition to changing the local environment for associ-
ated species, bioturbation will also alter the flux of nutri-
ents between the sediment and the overlying water and in
this respect the biodiversity of intertidal flats may have an
overall impact on ecosystem functioning. an emerging hot
topic in ecology (Curent Focus) . Many epibenthic preda-
tors, including flatfish, crabs, and shorebirds, disturb the
sediment surface intensely during their feeding activities
(Hall et al. 1993) . While the resultant pits and surface fea-
tures created tend to fill in with fine material and perhaps
detritus. on most beaches the local effects are quickly erased
by bedload transport (Fig. 6.10) . Of course, not all interac-
tions can be classified as top-down or bottom-up: many are
mutualistic or facilitatory, as in other kinds of ecosystem
and these are reviewed in Box 6.4.
In summary, the picture that emerges from evaluations
of top-down and bottom-up processes on shores is that a
mixture of both is always present to differing degrees and
this mixture will vary with the relative strength of con-
sumer and resource recruitment. as well as the influence
of wider-scale processes, such as ocean currents and catch-
ment run-off. The latter is a particularly important concept
in the emerging field of coastal zone management in which
the interactions between land and the adjacent marine
areas are of fundamental importance.

Figure 6.10 (a) Effect of bioturbation by burrowing ghost shrimp Callianassa, (Manakau, New Zealand), which piles up
a large growing mound (seen here in section) by ejecting processed sediment through the top of its burrow entrance
(Tamaki & Flach 2000 ). Note the oxygenated burrow walls caused by the animal pumping water from the surface
(shown as light brown sediment lining burrow). (b) A depression or pit made by an eagle ray feeding at the sediment
surface on small bivalves (Manakau , New Zealand). Such pits form significant structures on intertidal flats (Thrush et al.
1991).
 6.5 The organization of shore communities

Box.6.4: Facilitation in marine
communities
Organisms that live w ithin an assemb lage are intercon-
nected through a co mplex series of interacti ons (Grimm
199 5) that can be either neutral, positive, or negat ive,
depending on the organisms involved. Organi sms exhibit
a range of interact ions wi t h different co mpo nents of their
commun ity such that a predator of one species may be
the prey of another (e.g. Travis et al. 2006).
A recently emerging area of interest is that of the 'facil-
itator', a phrase more often associated w ith corporate
business events! Interspecific facil itation is any interaction
that has a positive effect on one of the species, but that
does not have a negat ive effect on any of the other spe-
cies involved (i.e. commensalism and mutual ism) (Bron-
stein 19 9 4 ) . Facilitation includes all forms of positive
interacti on, from 'tightly coevolved, mutua lly obligate rela-
t ionships to loosely facultative relationships' (Stachowicz
20 01). Facilitation can affect marine systems at all levels
of organizat ion, from ind ividual organisms (e.g. specif ic
Symbiodiniu m spp. end osymbiont dinoflagellates in cor-
als; Lajeunesse et at. 20 03) to the formation of large
biogen ic structures by foundation species that facilitate
wh ole biotopes (e.g. horse mussel reefs or maerl beds;
see Chapter 8). Further examples of facilitation at differ-
ent levels of organization within communit ies are given in
the table below.

Table Modes of facilitation in the marine benthos. These broad mechanisms of facilitation are common to all
biomes.

Mechanism Notes Examples

Habitat creation Habitats may be created by a singl e foundation species or a guild of speci es Reef-buil ding corals 1
Increases general habitat heterogeneity Oysters and mussels-
Provides a suriace for attachment Seagrass beds"

Provision of a Transform ing a two-dimensional structure into a th ree-dimensional structure Reef-buil ding corals 1
refuge provides an environment wh ere prey is able to shelter from potential predators Oysters and mussels-
Relic structures remain ing once species are dead can facilitate long after Seagrass beds"
organisms are gone (Aronson and Precht 2001; Munksby et at. 2002) Polychaete worms"
• ••• •••• ••••••• ••••••••••• ••• •••• ••••••• ••• ••••••• •••• ••• ••••••• ••••••• ••••••• ••••••• ••••••• ••• •••• ••• •••• • •• ••• ••• ••• ••• ••• ••• ••• ••• ••• ••• •••
Hydrodynamic Decreases flow velocity and increases sedimentation (Luckenbach 198 6) Reef-buil ding corals 1
modification Facilitates by increasing sed iment stability (Bruno and Kennedy 2000) , Oysters and mussels-
improving food delivery (Worcester 199 5; Shashar et al. 1996) , and by Seagrass beds"
increasing pro pagul e retention (Eckman 198 3; Bruno 2000) Polychaete worms"

Amelioration Intertidal organisms retain mo isture at low tide, shade substrate and provide Fucoid alqae''
of desiccation moisture for associated species (Thompson et al. 199 6; Bertness et al.
stress 19 99b )
Allows species to exte nd their realized niche (Bertn ess et at. 19 99 b)
• • •• •••• ••• • • •• •••• ••• •• •• ••• •••• •• • •••• ••• • ••• • • • •••• • •• ••• • ••• ••• • • •• •• • • ••• •• • •••• •• • • ••• •• • •••• • •• ••• • • •• ••• • •• • •• • •• ••• • •• •• • ••• ••• • •• • • •
Amelioration of Through bioturbation and bioirrigat ion, organisms cause th e oxic-anox ic Luqworrns''
anoxic stress chernocllne to move dow nwards in sediment th us facilitating by reducing Ghost shrimps?
anoxic stress Stingray"
Commonly caused by bioturbating and bioirrigat ing infauna (Pearson 2001 ;
Rosenberg 2001 ; Meysman et at. 2006)
· .
Enhanced Increases the supply or retent ion of agents of reproduction Reef-buil ding corals 1
pro pagule Oysters and mussels-
retention Seagrass beds"
Polychaete worms"
Kelp"

' Luckhurst and Luckhurst 19 78 ; Jones and Syms 19 9 8; Syms and Jones 2000. 2004; 2Tolley and Volety 2005; "Dean et at. 2000; Lee and
Berejikian 2009; "Schwindt and Iribarne 2000; Dame et at. 2001; Schwindt et at. z ooa a, 2004b; sKappner et al. 2000; 6Reise 19 8 1a,
198 1b; Reise and Volkenborn 2004; Vo lkenborn and Reise 2007; Volkenborn et al. 2007, 2009; "Ber kenbusch et al. 2000. 2007;
"v alentine et al. 1994; " Estes and Palm isan 1974, Carr 1989.
 Chapter 6 Rocky and Sandy Shores
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6.6 The shore network
The previous section has stressed both the openness and
connectivity of shores. Ecologists are usually required to
delimit spatially (and temporally) their study areas in order
to m ake sense of the complexity present, but the linear con-
tinuity of the coastline and its openness to the ocean neces-
sitates a broader perspective if one is to truly understand
how shores work. While conceptualizing a particular shore
as a part of a larger network is relati vely straightforward,
quantifying those linkages will be a d aunting t ask and one
that is best suited to modelling as opposed to empirical
approaches . However, there are a number of general fea-
tures that can be described empirically.
Shores are highly open systems, receiving and exchang-
ing resources and propagules with each other and with
offshore systems.
CURRENT FOCUS: Biodiversity and
ecosystem functioning-how many
species does a shore need?
The past 10-1 5 years have seen an explosion in research
focused on the relat ionship between biodiversity and eco-
system functioning in an attempt to describe the relation-
ships between the number of different kinds of organ ism
in an ecosystem and the rates of ecosystem processes
(figure a) that underpin the serv ices that provid e benefi ts
to society (Balvanera et al. 2006 ) . The qu estion is an
important one given the signif icant species losses from
ecosystems as a result of anthropoge nic act ivities: are
there crit ical numbers and kind s of species needed to
sustain particular processes?
Biodiversity
Fig a. Possible relati onships between biodiversity and
ecosystem processes (function s). The three different
models, cu rvilinear, linear, and random , describe the
different impacts of species loss on ecosystem process
rates (after Raffaelli 2010).
Coastal water movements have an incredibly significant
impact upon the change and pattern in shore organ isms,
and are responsible for the transport of inorganic nutrients,
organic m aterial, sediment and its associated infauna, lar-
vae, and spores within the water column, as well as smalle r
fish and crustacean consumers . Often, m ajor shifts in com -
munity structure and composition on the shore can only be
satis factorily explained by cons idering near-coast hydro-
dynamics. The irony is that m any shore ecologists are not
trained in this a rea and that mainstream ecologists seek-
ing to use the shore as a convenient laboratory for testing
theory m ay not be aware of the importance of water move-
ment. Our understanding of suc h physical processes is fur-
ther hampered by the paucity of data routinely collected.
Clearly, this is an aspect of shore ecology in need of urgent
support and development.
Much of the earlier research in this area was dominated
by terre strial ecologists working on plant biodiversity and
primary producti on, but mari ne intertidal systems have
increasingly played a part in unravelling these relati on-
ships and the mechan isms behind them (Bulling et al.
20 0 6 ). This is partly because shores provide ideal experi -
mental systems (t his chapter) for exploring and test ing
mainstream ecological theory, but also because they are
rep resentat ive of a system that covers c.80% of the
planet surface: the sea bed , characterized by small inver-
tebrates that go about their business w ithin and on the
sediment and in doing so may govern the biogeochemi cal
fluxes at the sediment-water interface.
Much of the work to date in th is area has involved main-
taining different co mb inations of species, levels of spe-
cies' richness and biomasses in high ly controll ed micro- or
meso-cosm facilities, rather than in situ on the tidal flat or
beach. This is be cause for sediment habitats it is d ifficult
to manipu late infaunal species' richness in the fie ld w ith-
out disrupting the sediment habitat and inc urri ng 'hidden
treatment effects' (Huston 19 97) , although some have in
fact achieved this (e.g. Bolam et al. 2002). Meso-cosms
oft en emp loy defaunated sedi ment to w hich species are
then carefully added in order to ensure the treatments are
correct. This allow s a high degree of experimental cont rol
so that the effects of biodiversity on, for instance ammo-
nium fluxes, can be unequivocally interpreted (Bulling et
al 2006). Whilst this approach is good for experimental
design considerat ions, it lacks the realism of the fie ld sit u-
ation and is be st suited for understanding and expl oring
mechan isms and relationships, rath er than provi d ing true
estimates of fluxes under d ifferent diversity scenari os. In
 6.6 The shore network

our own experiments in this area, it is clear that the 40

Nereisdiversicofor
biot urbatory behaviou rs of different species can have
a large effect on nutrients leaving the sediment-water Corophium va/uta/or
interface. Large, mobile burrowers such as the poly-
chaete Hediste diversicofor have a much greater impact
than the surficial ploughing snail Hydrobia ufvae (figure Hydrobia ufvae
b). It is clear that the number of species is less impor-
tant than species ' identity. This is confirmed by studies 4 B
on functionally similar and dissimilar species on South biomass (g wet weight)
Australian sandflats: nutrient release rates are higher
when several different functional types are represented
40 Boston Bay,
than when all the species are of the same functional
-~ 30 South Australia
--- 3-spedesmixture
type (figure b).
Making such experiments more 'nat ural' can be
'<,
-- Salina/or (ragifis
Callianassa ceramica
achieved by adding flow to the meso-cosm systems,
Ka/e fysia scafarina
using specially designed flumes. When this was done
for Hediste, the results were quite different: under real-
istic flow condi tions, Hediste changed its behav iour
completely, switching to bei ng a filter-feeder with con- 6 12
sequent reduced bioturbatory potential (figure c). biomass (g wet weight)

This only serves to underline the pitfalls of extrapo-

40 jesen Boy, Salina/or fragifis
lati ng from simple, highly controlled experiments to the
field. Of course, the next obvious step is to assemble
-.~ 30 South Australia
--.. Sa/ina/or solidus
such experiments in the field, so that the full range of =
environmental conditions is experienced, and extending
-15 20
E
8atiflaria diemenensis
~

to larger spatial and longer temporal scales (Raffaelli ~ .,; -------- ----- -- 3-spedesmixture
2006, 20 10). Such extensions present major techni- § 10
cal and logistic challenges bu t given the success in
using intertidal sediments for informing what is a crucial 6 12
question in conservation ecology, it will be well worth biomass(g wet weight)
the effort.
Fig b Biodiversity-ecosystem functioning
experiments -> Raffaelli (2010).

o without flow
o withflow
+
+
+
+

Fig c Effect of flow (shaded bars) vs. static (clear bars)

mesocosm conditions on the release of ammonium
from sediments by three species of interdrial inverte-
o 100 200 300 400
brates. Modified from Biles et al. (2003).
ammonia ±I s.e. (1-1 mol /litre)
 Chapter 6 Rocky and Sandy Shores
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Often , major shifts in community st ructure and composi-
tion on the shore can only be satisfactorily exp lained by
considering near coast hydrodynamic processes.
In addition to the physical transport ofliving and non-liv-
ing material on- and offshore, and between different shore
types. larger organisms can make purposeful migrations.
These include larger fish, reptiles, birds, and mammals,
which undertake such journeys for breeding, feeding, otto
find a refuge from bad weather or predators. Their use of
the shore can be considerable. especially for warm-blood-
ied taxa with high energy demands, such as shorebirds and
marine mammals (Table 6.2), although, as argued in 6.5.5,
cascading effects on the community are rarely detectable.
6.7 The future of rocky and
sandy shores
The future of rocky and sandy shores depends on the tem-
paral perspective taken. A series of key analyses looking at
impacts and threats to 2025 (Brown & McLachlan 2002;
Kennish 2002; Thompson et aI. 2002, Kennish et aI. 2009)
have identified a continued increase in many of the anthro-
pogenic impacts that shores experience today. mainly
because of projected increases in coastal populations
worldwide. Looking further ahead to 2080, accelerated
sea-level rise (ASLR) will undoubtedly impinge upon low-
lying sedimentary shores and estuaries. but also on rocky
shores because of changes in currents and hence transport
patterns, as well as changes in wave climate (Chapter 15) .
Accelerated Sea-level Rise, d ue to cl imate change, will
have large-scale impacts on sandy beaches and mudflats
over the next 50-1 00 years.
Beaches are dynamic physical entities. maintained by
processes operating above and below the beach as com-
monly defined (Brown & McLachlan 1990), so that changes
in sediment supply and wave climate are likely to impact
greatly on beach dynamics. For sandy shores, ASLR may
increase erosion, create a steeper beach profile and increase
turbidity (Goss-Custard et aI. 1990). With less organic mat-
ter retained in the beach, there will be a lower biomass of
infauna. These problems will be exacerbated ifbeaches are
protected by hard engineering, as the available beach area
will be progressively sandwiched between a rising sea-level
and an immovable structure. the so-called coastal squeeze.
The net result of sea-level rise for many soft shores will
therefore be a smaller, less productive beach (Fuji & Raf-
faelli 2008), although other scenarios are possible, depend-
ing on sedimentation patterns and the relative rise of the
sea and land (Beukema 2002; Goss-Custard et aI. 1990).
Sea-level rise not only reduces intertidal area, but pro-
found ly alters sediment distribut ions.
It is likely that rocky shores, at least those below high
cliffs, will not be subject to coastal squeeze. since the biol-
ogy can migrate upwards over time without impediment.
However. both rocky and sandy shores in some regions
could experience a more severe wave climate, due to an
increase in storminess with climate change (IPCC 2001) .
Of most concern, perhaps. is the suspected relationship
between sea-level and the return time of storm surges,
catastrophic flooding events that can remove entire beaches
and mudflats. For instance, one estimate suggests that an
increase in sea-level of 0.5 m, well within the range pre-
dicted by 2080, can alter the return time of a 1.5 m storm
surge from 1 in every 100 years to 1 in 10 years or less
(IPCC 2001) . How shore communities, both soft and hard,
would respond to catastrophic disturbances at a frequency
that approximates the lifespan of much of the shore biota is
hard to predict. However. longer lived species would have
difficulty adapting to such conditions due to their lower
fecundity and infrequent recruitment.
The frequency of catastrophic wave action is likely to
increase dramat ically with rises in sea-level.

Chapter Summary
• Rocky and sandy shores are the most accessible parts of the marine environment and contain
representatives of almost all the major classes of animals and plants.
• Rocky and sandy shores occur at either end of an environmental gradient of habitat particle size
that ranges from very large (cliffs and boulders) to very small (individual sand grains). Species
occupy sections of this gradient and the wetness/dryness (shore level) and wave-action gradients,
and reveal zonation patterns that are most obvious across the shore level gradient.
 Chapter Summary

• The distribution and abundance of these species are determined by their tolerances to physical
factors, such as water movement and desiccat ion, and to biological factors , such as competition ,
biotu rbation , and predat ion.
• Rocky and sandy shores provide excellent laboratories for exp loring mainstream ecolog ical con-
cepts. Much of t he pioneering research using controlled experimental manipulations has been
carried out on the seashore.
• Different kinds of shore are net exporters or importers of energy, especially detrital material.
Understanding ecological funct ioning requires shores to be viewed as connected networks.

• Sandy and muddy shores are particularly vulnerable to climate change induced sea-level rise,
because they are often prevented from transgressing inland.

Further Reading
Little and Kitching (200 1) is an excellent concise book that deals with rocky shores, w hile Raffaelli and
Hawkins (1996) consider in depth the deve lopment of interti dal ecology. Raffaell i and Moller (2000)
critically evaluate the use and misuse of experimental approaches in ecology. Reise (1985) is a detailed
consideration of the ecology of tidal flats.
• Bertness, M. D. 2007 . Atlantic Shorelines, Natural History and Ecology. Princeton University Press,
Woodstock, UK.
• Little, C. & Kitching, J. A. 200 1. Biology of Rocky Shores. Oxford Un iversity Press, Oxford.
• Raffaelli, D. & Haw kins, S. J. 1996. Intertidal Ecology. Chapman and Hall.
• Raffaelli, D. G. & Moller, H. 2000. Manipulative experiments in animal ecology-do they prom ise more
than they can deliver? Advances in Ecolagicol Research 30: 299-330.
• Reise, K. 19 8 5. Tidal Flat Ecology. An Experimental Approach to Species Interadions. Springer-Verlag,
Berlin.
 Pelagic Ecosystems
Chapter Summary
Away from coastal boundaries and above the seabed, the
pelagic environment encompasses the entire water column
of the seas and oceans. The pelagic envi ronment extends
from the sea surface to th e abyssal depths, from the trop-
ics to the polar regions, an d is a highly heterogeneous and
dynamic three-d imensional habitat. It is th e most volumi-
nous habitat on Earth. The pelagic environment is home
to some of the most revered and reviled marine inhabit-
7.1 Introduction
The term pelagic means 'o f the open sea', and the pelagic
realm is a largely open, unbounded environme nt in which
the inhabitants have freedom, within physiological limits,
to move in three dimensions. The pelagic environment is the
largest habitat on Earth. Contrary to the common perception
that the sea is an unchanging, relentless expanse, the open
ocean is an environment where variability is very much the
norm. Patchiness in physical properties (e.g. temperature,
salinity, turbidity), biological production, and biomass exists
at a range of scales in space (centimetres to hundreds of kilo-
metres) and time (minutes to decades and beyond). One of
the key challenges to understanding open-ocean function
lies in understanding the mechanisms that cause, and conse-
quences of, this patchiness (Mackas & Tsuda 1999; Mitchell
et aJ. 2008).
The open ocean is a highly dynamic and variable environ-
ment, even though it may appear superficially uniform to
the human eye when viewed from the shore.
Despite the fact that much of the open ocean is remote from
land, beyond the horizon for land-based observers, it has not
ants, but great whales and jellyfish alike are s ubject to the
conseq uences of pelagi c ecosystem variabil ity. Physical
process es in the pelagic exert major cont rol on biologi cal
activity, and lead to substant ial geograp hic vari ability in pro-
duction. Know ledge of biophysical interactions is essent ial
for und erstandin g ecolog ical patterns and processes in the
pelagic environment, for management of fisheries ecosys-
tems, and will be key for predictin g changes in th e pelagic
induced, for examp le, by cl imate change.
escaped human impacts. For example, 90% of stocks of large
pelagic fish, such as tuna (Scombridae) and jacks (Caran -
gidae), may have been removed by fishing (Myers & Worm
2003), and whole zooplankto n com mun ities h ave shifted
their spatial distribution (Beaugrand et aJ. 2002) , possibly
in response to ocean warming, itself most likely caused by
ant hropogen ically-released greenhouse gasses OPCC 2007) .
Microscopic plastic fra gments are also widespre ad in the
oceans, and have accumulated in the pelagic zone (Thomp-
son et a1. 2004) wit h damaging consequences for a variety of
orgamsms .
Despite its apparent remoteness, the open ocean has been
influenced strongly by human activities such as fishing , pol-
lution , litter, and anthropogenic climate warming.
The pioneering studies of open-ocean ecology made from
vessels wit h evocative n ames such as Discovery , Cha llenger,
and Atlantis have been enhanced in recent years with obser-
vations from technologically advanced research platforms
that include Earth-orbiting satellites (Bricaud et aJ. 1999)
and unmanned autonomous underwater vehicles (AUVs;
see Box 7.5) (Griffi ths 2003) . The aim of this chapter is to
provide a synt hesis of open -ocean ecosys tem fun ction and the
 7.2 Definitions and environmental features
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
factors that control it, insight into difficulties associated
with sampling the heterogeneous pelagic realm, and some
examples of ecological step-changes (regim e shifts) in the
global pelagic environment.
7.2 Definitions and
environmental features
The pelagic realm spans the entirety of the water column,
beginning at the sea surface and ending just above the
seabed (the benthic realm; Chapters 8 and 9) . This mid-
water marine ecosystem is the largest on Earth and com-
prises over 99.5% of the planet's habitable space (Robison
2004) . The pelagic realm can be subdivided by total water
depth and distance from shore. The neritic zone lies adja-
cent to shore, over continental shelves, and covers about
8% of the Earth's total sea area. Out beyond the continen-
tal shelf break, which is delimited typically by the 200-m
depth contour (isobath), lies the vast, open oceanic zone
(92%of the total sea area, covering 65%of the Earth's sur-
face) . There are numerous differences between the neritic
and oceanic zones, differences that arise not least because
of differences in proximity to land and consequent differ-
ences in nutrient and sediment loading in the water column
(much of the sediment load in the seas and oceans is ter-
rigenous and is delivered by rivers and estuaries; Chapter
5) . Sailing out from a coastal port towards the open sea it
is common to notice a transition from turbid to clear, blue
waters. This transition is obvious not just from the deck of
a ship but is visible from space. Indeed, interpretations of
satellite remote-sensed observations of ocean properties
have to distinguish 'Case l' waters, where the ocean colour
is determined predominantly by algal pigments, from
'Case 2' waters, where reflections from particulate mat-
ter dominate (Fig. 7.1) (Babin et al. 2003) . Differences in
particulate loading lead to differences in underwater light
climate that, along with different nutrient availabilities,
have led to differing photosynthetic architectures in neritic
and oceanic phytoplankton. Offshore species of diatoms
have evolved lower photosystem 1 and cytochrome b(6)f
complex concentrations, enabling them to decrease their
Figure 7.1 An enhanced true-
colour view of ocean colour
from the SeaWiFS satellite (18
May 1998 13:08 GMT) showing
Case 1 and 2 waters around and
to the south-west of the British
Isles, North-West Europe. Satellite
images were received by the NERC
Dundee Satellite Receiving Station
and processed by Peter Miller and
Gavin Tilstone at the Plymouth
Marine Laboratory (PML) Remote
Sensing Group (http://www.
neodaas.ac.ukl). SeaWiFS data
courtesy of the NASA SeaWiFS
project and Orbital Sciences
Corporation.
 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
iron requirements without compromising photosynthetic
capacity (Strzepek & Harrison 2004) . However, oceanic
diatoms have probably sacrificed their ability to acclimate
to the rapid fluctuations in light intensity that characterize
dynamic and turbid coastal waters. Another adaptive bio-
logical consequence of the difference in sediment and par-
ticulate loading between the oceanic and neritic zones can
perhaps be seen in squid anatomy. Myopsin squid inhabit
the neritic zone (for example Loligo forbesi, which is com-
mon in north-west European coastal waters. or L. opalescens
from the west coast of the USA) and have a membrane
across the eye that may serve to protect the eye from par-
ticulate irritants suspended in the water: in the open ocean
myopsin squid are replaced largely by members of the sub-
order Oegopsina (for example, the European flying squid,
Todarodes sagittatus) in which the membrane is absent, pos-
sibly because it is unnecessary.
The neritic and oceanic zones are very different, due in
part to their differing distances from the coastline and
associated differences in particulate and nutrient loading.
Open ocean and coastal diatoms have different photo-
synthetic architectures that enable them to cope with
different nutrient availabilities and light climates.
The presence of a protective eye membrane in neritic
squid may be an adaptation to heavy particu late loading
in near-shore seas.
The pelagic component ofthe open ocean can be divided
further by depth. The upper surface of the ocean is known
as the neustic zone and, in the tropics especially, is a habi-
tat made harsh by exposure to high levels of ultraviolet
radiation. Floating organismsinhabiting this zone typically
have a blue colouration (Fig. 7.2) due to the presence of
protective pigments that are able to reflect this damaging
part of the light spectrum. The development of the ozone
hole in the Earth's atmosphere has resulted in increased lev-
els of UV radiation reaching the Earth's surface (the ozone
layer acts as a UV shield), particularly in the southern hemi-
sphere. In the Southern Ocean, Antarctic krill (Euphausia
superba) may be particularly vulnerable to UV-induced
DNA mutation because krill DNA is rich in thymine, which
is the base that is most susceptible to UV radiation damage
(Jarman et a1. 1999). Since krill migrate away from the sea
surface during daylight hours, however, their behaviour
will probably serve to limit DNA damage, but UV damage
to other species remains a distinct possibility, and photo-
synthesis by Antarctic phytoplankton shows inhibition by
elevated UV (Smith et al. 1992).
Light also plays an important role in pelagic ecosystem
function away from the neustic zone, both because it drives
primary production (Chapter 2) and because it enables
visual predation (predators that hunt using the sense of
sight) . In deeper, darker waters tactile predation (preda-
tion by touch) dominates (Eiane et al. 1999), but in clear
oceanic waters the threat from visual predators is increased
because these predators can detect preyovergreater ranges
(Aksnes & Giske 1993). Shark attacks on humans often
occur in turbid waters (Cliff 1991), possibly because under
these conditions prey recognition is difficult and humans
are mistaken for typical prey such as seals. The upper part
of the water column into which light penetrates is called
the photic zone. In clear tropical oceanic waters this zone
may extend as deep as 200 m (much less in more turbid,
temperate locations), although at this depth light intensity
will usually be too low to drive photosynthesis (Chapter 2) .
Figure 7.2 The Portuguese Man o'War (Physalia physalis,
a colonial Cnidarian) floats at the sea surface and has a
blue colouration (photograph: joaoquaresma.com).
Organisms that live in the neustic zone are particularly
vulnerable to increases in UV radiation.
The upper 200 m of the water column is also known as
epipelagic (Fig. 7.3) . Light at the red end of the spectrum
is absorbed rapidly by seawater and does not penetrate far
into the epipelagic zone (Chapter 2) . Red colours are effect-
ively invisible at depth, therefore, and many pelagic crust-
aceans adopt this colour as a means of camouflage against
visual predators (Fig. 7.4) . Below the epipelagic zone
are, sequentially, the mesopelagic (200 to 2000 m), the
bathypelagic (2000 to 4000 m), and the abyssopelagic
(4000 to 6000 m) zones. As depth increases, organisms in
the pelagic environment are faced with increasing physio-
logical challenges: pressure increases by 1 atmosphere for
 7.2 Definitions and environmental features
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

every 10 mincrease in depth (Box 7.1 ; 1 atmosphere = 1 kg

cm- 2, equivalent approximately to the mass ofa bag ofsugar
balanced on your finger tip) and in some locations oxygen-
J

minima layers (Rogers 2000) arise at depth because oxy-

gen is depleted by bacteria breaking down material sinking
from the sea surface. Low oxygen concentrations render
compartments of the world ocean inhospitable to multicel-
lular life. and ongoing warming together with rising atmos-
pheric CO 2 will see an expansion of oxygen minima zones,
perhaps by more than 50% by volume, by the end of the
twenty-first century (Stramma et al. 2008) .
In general terms the total mass of biota per unit vol-
ume of seawater decreases with depth (Yamaguchi et
al. 2002) . This is because, with the exception of energy
input by chema-autotrophic processes at hydrothermal
vents (Chapter 9), biological processes in the deep sea are
fuelled entirely by photosynthetically-generated organic Figure 7.4 A mesopelagic zoop lankton/nekton sample
matter from the illuminated surface region. This material showing the predominance of red-coloured crustaceans
either sinks passively, sometimes in strong pulses of'marine (photograph: Andrew Brierley).
snow' (Billett et al. 1983), or is transported downwards by
vertically-migrating organisms that excrete, or are eaten, at bon does, however, reach the deep ocean interior, where
depths deeper than which they feed. Animals migrating ver- it can be consumed by organisms on the sea bed or incor-
tically through a series ofoverlapping yet ever-deeper depth porated into sediments (Billett et al. 2006) . Trapping, or
zones form togethera 'ladder' ofmigration from the surface sequestration, of carbon in the deep sea is the end-point of
to the deep down which carbon is passed as if in a chain of the so-called 'biological pump' that transfers atmospheric
ever-smaller buckets. As material descends further from the CO 2 to the ocean (Lutz et al. 2007).
surface it becomes distributed through an ever-increasing
volume afwater. This dilution effect means that as distance The total mass of biota per unit volume of seawater
from the surface increases, food availability decreases, with decreases with depth.
the consequence that less animal biomass can be sustained
at depth. In the deep pelagic zones, energy efficiency is par-
Energy efficiency is important in the deep pelagic due to
ticularly important and animals adopt stealthy, sedentary
the dispersed nature of potential food.
lifestyles and use cunning mechanisms to ambush prey in
darkness (Seibel et al. 2000) . Photosynthetically-fixed car-

High water Pelagic

, j Neritic
Oceanic [ Phatic
. -
llfterul
•
Low water Epipelagic

-~
(antinental shelf 200m

~. ~
~ ~ - - -- ----- -------- --- --- --- --- ----------
Mesapelagic
1000 m

%~~ -
.~

0
!!>
" Bathypelagic ...
~
~- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - 4000m

Benthic _
---Abyssal ~--\-a~a~p"I~9~C___ 6000m

Hadal
• I 1 ‫סס‬oo m

Figure 7.3 Depth zones in the pelagic realm.

 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Box 7.1: Seawater as a dense and
viscous (sticky) medium
Seawater is denser and more viscous than air. The
increased density offers advantages to some mari ne
organisms, for example, providing physical support
that reduces the need fo r skeletal strength (beached
whales suffer because their skeletons are inadequate
to support their bulk in air), but also presents chal-
lenges such as rapidly increasing pressure with
depth. Seawater density varies as a function of the
concentration of dissolved salts (salinit y; salinity is
reported without units since it is defined in terms of
the ratio of the electrical conductivity of seawater
to the electrical conductivity of a po tassium chlor-
ide standard; see also Chapter 5) and tempera-
tu re (warm water is less dense than cold water).
The strength of cohesion, or stickiness, of a fluid is
quantified by its dynamic viscosity. The dynamic
viscosity of olive oil, for example, is 40 t imes tha t
of seawater. The motion of a particle of a given size
and velocity is more impeded thro ugh a medium of
greater dynamic viscosity (thin k of a marble sinki ng
through a bottle of water and a bottle of olive oil). For
a fluid of a given dynamic viscosity (e.g. seawater)
the conti nuity of motion of a particle is controlled
by its velocity and size, and can be quantified by the
Reynolds' number (Re). For a given fluid, Re is sim-
ply: (particle velocity x particle size)/ dynamic vis-
cosity. Re is dimensionless because the units used in
its calculation cancel out. Broadly speaking for small
organisms moving at slow speeds Re is less than
10 0 0 and seawater is 'sticky': ciliates, for example,
stop the moment they cease swimmi ng. For larger
organisms travelling at higher speeds Re is greater
than 1000: the inertia of a large pelagic fish, for
example, enables it to continue gliding through the
water even after it has ceased active swimming (see
also Chapter 3).
7.3 Pelagic inhabitants:
consequences of size
Pelagic organisms can be divided into two categories on the
basis of their locomotory prowess. Plankton are unable to
counteract the influence of horizontal currents and so drift
passively in the horizontal plane (ocean currents often
exceed 1 knot or e. 0.5 m s").
The word plankton is derived from the Greek word pla-
nao, which means 't o wander'.
Plankton can, however, move vertically, adjusting their
depth, and do so pronouncedly during diel vertical migra-
tions (DVM) at dawn and dusk (Fig. 7.5). Diel vertical
migrations are a ubiquitous feature of pelagic ecosystems
(Hays 2003) and are thought to be driven primarily by the
trade-off required to enable plankton to feed in the food-
rich upper water-column and yet to avoid the illuminated
upper layer in daylight because of the increased risk of
visual predation incurred there at that time (Tarling 2003).
This is probably not the whole story, however, as vertical
migration some times continues in the constant darkness of
polar winter (Berge et al. 2009) .
Daily and seasonal changes in incident light intensity
have profound effects on biological processes in the
pelagic environment, driving vertical migrations and
seasonal plankton blooms.
Some organisms, such as copepods and chae rognat hs,
complete their entire lifecycle as plankton and are called
holoplankton. Others, such as fish lar vae and barnacle
larvae, spe nd only a part of their lifecycle as pl ankton,
either growing or settling out to the seabed as they age,
and are called meropl ankton. A planktic phase provides
opportunities for dispersal and colo nization, but is also
a stage that is particularly vulnerable to predation (Pech-
enik 1999 ). Planktotrophic larvae (larvae that have an
exte nded pl anktic phase) may suffe r higher per capita
mortality than lecithotrophic larvae that have a limited
planktik phase, but planktotrophic organisms may achieve
more wides pread genetic dispersal than lecithotrophes
(Todd et al. 1998).
Animals whose larvae have a prolonged planktic phase
(i.e. that are planktotrophic) generally produce a higher
number of eggs per unit body mass than do animals
with lecithotrophic larvae. This may be because mortality
rates in the plankton are high.
Organisms that are capable of swimming to the extent
that they can overcome horizontal currents are known as
nekton. Inhabitants of the open ocean span several orders
of magnitude of size, ranging from viruses, bacteria, and
protozoa to large predators such as sharks and whales,
which may reach many metres in length and body masses
of several tonnes. Generally speaking, large organisms are
nektic and smaller organisms are planktic: micronekton
have intermediate swimming abilities and are of the order
of 4 em in length (for example, large euphausiids such as
Antarctic krill). This size-relate d difference in mobility
arises in part because of the interaction betwe en size and
 7.3 Pelagic inhabitants: consequences of size
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
I I IIII II I I I I
100
200
_ 300
.§.
"" 400
~ 500
600
700
-J8 -36 -J4 -J2
longitude degrees
Figure 7.5 An echogram showing the rapid ascent of zooplankton and nekton (as detected using a 38 kHz scientific
echo-sounder) from depth to the near surface at dusk. This migration from 400 m to 50 m takes less than 2 h. The
upper bar indicates periods of day (light blue) and night (dark blue). Temporal and spatial variability are tightly
intertwined in this echogram.
viscosity (Box 7.1) : seawater is essentially a 'sticky' medium
for small organisms (Van Duren & Videler 2003) and, for
them, a constant expenditure ofenergy is required to main-
tain motion. There are exceptions to the size-mobility gen-
eralization. however, and the Arctic lion's mane jellyfish
(Cyanea arctica) that may attain tentacle lengths of 40 m,
remains a passive, planktic drifter. The very smallest plank-
tic organisms include viruses and bacteria (Azam & Worden
2004) and protozoa (Struder-Kypke & Montagnes 2002).
The small size of these organisms belies their importance
to pelagic ecosystem function. Viruses are a major cause of
mortaliry, a driver of biogeochemical cycles, affect the form
of available nutrients and the termination of algal blooms
(Suttle 2005) . Dissolved organic carbon is taken up by bac-
teria, which are consumed byheterotrophic nanoflagellates
and in turn by ciliates in the so-called microbial loop at
the base of the food chain (Chapter 3) . This loop recycles
organic matter that is too small to be consumed by meta-
zoan plankton, and the metazoans are able to prey upon
ciliates. The microbial loop therefore fuels the pelagic food
chain, and is especially important in oligotrophic waters
(Lenz 2000) .
Very few pelagic organisms dismantle their prey before
eating, a behaviour more common in benthic biota such
as crabs.
As well as impacting mobility, organism size is also a
major architect of pelagic food-web structure. Pelagic organ-
isms will typically consume food items whole, and the size of
item thatan animal can consume is constrained by its mouth
size, such that predators are usuallysubstantially larger than
their prey (Cohen et al. 1993; Jennings & WaIT 2003) . This
concept is well captured by Brueghel's picture Big Fish Eat
Little Fish, in which small fish are tumbling out of the mouths
I I II I I
-50
-60
=
~
.~
-70 =
J!!
=
-80
-
0
~
~
'----------.J -90
-JO - 28 -26 -24
of successively bigger fish (Fig. 7.6) . A more taxonomically
extensive example from the North Sea has unicellular algae,
such as diatoms (c. 100 11m diameter), grazed by copepods
(e.g. Calanus finmarchicus, c. 3 mm length), which are in
turn predated by herring (dupea harengus, c. 20 em length),
which might be consumed by gannets (Sula ba.ssana, c. 180
cm wing span), or minke whales (Balaenoptera acutorostrata,
c. 7 m length). This strongly size-structured progression is in
marked contrast to many terrestrial food chains where small
predators (for example, hyenas, body mass c. 40 kg) may
cooperate in social groups to take herbivores that are con-
siderably larger (e.g, wildebeest, c. 250 kg).
In terrestrial systems, animals that forage in social groups
can deal with prey items much larger than themselves.
Pelagic food webs are often far more complex than the
simple four-linked-chain diatom-copepod-fish-bird exam-
ple from the North Sea. An analysis of a 29-species' food
web for the Benguela ecosystem. for example. undertaken
to determine ifculling Cape fur seals (Arctocephalus pusillus
pusillus) would increase biomass of commercially impor-
tant hake (Merluccius spp.) (Yodzis 2000) noted that there
were over 28 million pathways including hake and seals!
This complexity of food webs, and the fact that most lev-
els can be controlled either from above (top-down control,
e.g, by predation) or below (bottom-up control, e.g. by food
limitation; Verity & Smetacek 1996) renders it very difficult
to make predictions of the consequences of bioregulation.
In general. smaller mean predator:prey body size ratios are
characteristic ofmore stable environments, and food chains
are longer when mean predator:prey body size ratios are
small (Jennings & Warr 2003) . Systems that have shorter
food chains are generally much more susceptible to trophic
cascade effects (Brierley 2007; Chapter 8) .
 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
The complexity of food webs means it is difficult (if not
impossible) to predict the outcome of selective culling
of higher predators on lower tropic levels. Neverthe-
less, there is increasing evidence that populations of top
predators, such as seals, may, at current levels, have a
disproportionate predation effect on fish populations.
Figure 7.6 'Big Fish Eat Little Fish:' by Pieter Brueghel
the Elder (1557) showing smaller fish tumbling from the
mouths of bigger fish. The Metropolitan Museum of Art,
Harris Brisbane Dick Fund, 1917 (17.3.859).
7.4 Temporal and spatial
variability in pelagic
ecosystems
The open ocean is not homogenous. Interactions between
physical and biological processes result in variability over
a range of temporal and spatial scales, and patchiness is a
key feature of pelagic ecosystems. The Stommel diagram
(Fig. 7.7) illustrates the scales of variability that are inher-
ent characteristics of pelagic ecosystems, from centimetres
to thousands of kilometres horizontally and from seconds
to millennia. and shows how variations in time and space
are interlinked. It is important to appreciate the interplay
of temporal and spatial scales, and it is a theme that recurs
throughout this book. Phytoplankton are short-lived and
are influenced by small-scale mixing processes (Martin
2003) . The diel vertical migration (DVM) of zooplankton
at dawn and dusk is restricted to certain times of day but
occurs everywhere (Pearre 2003), indeed DVM is the larg-
est coordinated movement of biomass on the planet. Fish,
which are generally longer lived than zooplankton, are
impacted by environmental variability over longer time-
scales: the Peruvian anchoveta (Engraulis ringens), for
example, is influenced strongly by the E1 Nino Southern
Oscillation that exhibits decadal-scale variability (Chavez
et al. 2003; see also Chapters 1, 8, 13, and IS).
Fish, which are generally longer lived than zoop lankton,
are impacted by environmental variabil ity over longer
t ime-scales.
7.4.1 Physical processes contributing
to temporal and spatial variability
The physical properties of the open ocean are heterogeneous
by depth, position (latitude, longitude), and over time. In
addition to the depth-related changes in light intensity and
oxygen concentration already mentioned. vertical gradients
in water temperature. density, current velocity, and nutrient
concentration may also exist. Solar heating warms the upper
ocean leading to the development of a thermal gradient by
depth. In some regions, combinations of tidal and wind-
driven processes cause turbulence and mixing of heated sur-
face water. with cooler water below. However, in regions or
seasons where winds are light and wave action slight. or in
water that is too deep to be mixed completely by tidal flow
(Chapter 8). pronounced vertical stratification can become
established: warm surface waters then become effectively
isolated from cooler. deeper waters by a thermocline. Verti-
cal stratification is also promoted in situations where fresh
water is introduced. Rain, river run-off. and ice-melt all
introduce fresh water to the surface of the ocean. Low salin-
itywaters are less dense than high salinity waters (Box 7.1)
and stabilize the upper water column because more energy
is required to mix low salinitywaters downwards. The strong
density gradient between the mixed, buoyant, low-salinity
surface waters and underlying high-salinity waters is known
as the pycnocline. The depth of the mixed layer, as bounded
by the pycnocline or thermocline, will vary depending upon
prevailing conditions (Chapters 2 and 8) .
Where winds are light and wave action slight, or in water
t hat is too deep to be mixed completely by tidal flow,
vertical stratification can develop.
As well as causing downward mixing. wind can lead
to the upward transport of water from depth. Such wind-
driven upwelling occurs over a range ofscales. At the small
scale. Langmuir circulation is generated as wind blows
steadily across calm water, causing near-surface vortices
several metres in diameter to develop parallel to the wind
flow (Box 7.2) . At the interfaces between neighbouring
vortex cells, alternating lines of upward divergence and
downward convergence develop. Flotsam accumulates
on the surface above the downward zones, leading to the
development of prominent, parallel wind lanes on the
surface. Zooplankton may also accumulate in downward
 7.4 Temporal and spatial variability in pelagic ecosystems

A. 'Micro' pmrhs
R. Swarms
C. Upwelling
D. Eddies andrings
E. Island effects
__ IOOOOKm F. 'EI Nino' type events
Ice age variations JI G. Small ocean basins
H. Biogeogrcphitol provinm
__ 1000 Km I. Currents and Oleanic fronts - length

§;~~ I __ IOOKm J. Currents

K. Oleani! fronts - width
Annual cycles
-
,'/ "'-_G.--
J o Ship,
,---~ D Moorings

9
.,-lOKm
o Satellites

log l (em)
Biomass .-- 1 em
variability

Time
o log P(sec)

Figure 7.7 The Stammel diagram , overlain to show the scales that can be sampled with various platforms, and features
such as fronts. Modified from ICES Zooplankton Methodology Manual, Harris et al. (eds), (2000), page 36. Copyright
2000, with permission from Elsevier.

zones because they are able to swim upwards against the
flow (Pershing et al. 2001).
Langmuir circulation can lead to the accumulation of
zooplankton and flotsam , which forms visible wind lanes,
at the sea surface.
At the large scale, wind plays a role inducing flow in most
surface curre nts. Curre nts do not flow parallel to the direc-
tion of the w ind but, due to interactions w it h the Coriolis
force, when averaged over the whole of the water column,
curre nts move at 90° to the wind. Movement is to the right
of the wind in the northern hemisphere and to the left in
the southern hemisphere. This movement is called Ekman
transport (Box 7.2). It contributes sign ificantly to gene ral
ocean circulation and can result in pronounced upwell-
ing. In the case of the Benguela Curre nt, for example, and
other southern hemisphere eastern boundary currents, the
prevailing sout h-easterly winds blow alongshore and drive
near-shore Ekman flow away from the coas t. This in turn
draws cold, nutrient-rich waters from depth to the surface
at the coast (Carr & Kearns 2003) . Changes in global wind
patterns have the potential to affect upwelling and the eco-
systems that are dependent upon them (Grantham et a1.

Box 7.2: Wind-driven circulation
processes
As wind blows over the surface of the sea it generates
waves and induces vertical and horizontal mot ion in the
water. Langmuir cells are small-scale, parallel, helical
vortices tha t are often apparent as a series of wind lanes
on the sea surface running parallel to the direction of the
wind. Vortices are usually not large enough to bring nutri-
ents up from deep water beneath the pycnocline.
Large-scale ocean currents are also induced by wi nd,
but occur at angles to the direction of the wind rather than
parallel to it. This is because of the interaction between
 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

friction and the Coriolis force . The Coriolis fo rce is the
force experienced by a mov ing bo dy of w ater due to th e
fact that the planet is rotating. The water colu mn can be
thought of as a series of horizontal layers. The upper layer
at the sea surface is subject to wi nd friction (w ind stress)
at the top and water fr iction (edd y viscosity) at the bot-
tom. Subsequent layers are impacted by friction with lay-
ers above and beneath. Slippage between layers results in
an exponential decrease in current speed with depth until,
below the depth of frictional influence, wi nd influence
ceases. Cumulative impacts of Coriolis force result in an
increasing angle of deviation away from th e wi nd wi th
depth. Curren t vectors in all layers form a spi ral pattern
known as an Ekman spiral. The averaged effect of the
spi ral is that the mean motion of the wi nd-driven (Ekman)
layer is at right angles to th e wind direction. Reprinted
from Ocean Circulation (2nd edn), the Open University
Course Team (2001) , pp. 42 and 68. Copyright 200 1,
with permission from Elsevier.

Downwelling [ronverqentes
where seoweed, debris, foom,
ond plankton a«umulate)
Upwelling
(divergen,e)

Helical vortices -----:-;

Wind stress

Average
mation of the
'- ---J Ekman layer Average
monon of the
Ioriolis Ekman layer
force
__ - Depth,!
Ioriolis farce -- -- - - ___ ~ _~ ~ -
~~- -~ frictional
infl uence
 7.4 Temporal and spatial variability in pelagic ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Horizontal boundaries between water masses with dif-
ferent physical properties are known as fronts (Box 7.3) .
Fronts occur at a range of scales, from tidal mixing fronts
that separate mixed and stratified waters in coastal seas
(Hill et al. 1993) to major oceanographic boundaries such
as the North Wall of the GulfStream and the Antarctic Polar
Front (Taylor & Gangopadhyay2001) . High-velocitycurrent
jets associated with fronts can be important long-distance
transport routes for many marine organisms: Antarctic krill
(Euphausia superba) are transported widely throughout the
Scotia Sea from breeding centres off the Antarctic Peninsula
on frontal currents (Thorpe et al. 2004), and large oceanic
squid, such as Illex illecebrosus, take advantage of currents
for distribution and feeding (O'Dor 1992) . Meanders in
fronts can lead to columns of water (core rings) being shed
from one side of the front to the other; the retroflection of
the Agulhus current around the southern tip of Africa, for
Figure 7.8 Drift of dye behind a swimming Mastigias
spp. jellyfish showing the mixing that animal motion
can induce (image from Katija & Dabiri 2009: http://
www.nature.com/natu re/journal/v460/n 72 55/fig_tab/
nature08207J2.htm l).
example. sheds warm core rings regularly into the south
Atlantic (Garzoli et al. 1999) and this so-called Agulhas
leakage is an important mechanism for transoceanic mix-
ing. Vertical variations in current flow lead to shear stress
that has major ramifications for horizontal structuring in
the ocean (see Current Focus box) .
Whilst it is recognized commonly that organisms are
influenced by physical processes in the ocean. it is less
widely accepted that organisms can influence ocean
dynamics. However, recent work has suggested that ani-
mals can influence biogeochemical cycling (Wilson et al.
2009) and, more controversially. ocean mixing (Kunze et
at. 2006; Katija and Dabiri 2009; Fig. 7.8): rather than
just being passive occupants that are impacted by physi-
cal change. life forms in the pelagic can make active and
climate-influencing contributions to planetary function
(Brierley & Kingsford 2009).
Most fronts are highly mobile, dynamic features that can-
not be represented accurately by single, static lines on
charts.
7.4.2. Consequences of temporal
and spatial physical variability for
pelagic primary productivity and
biogeography
The depth to which water-column mixing occurs, the
mixed-layer depth, has major implications for primary
production in the open ocean because photosynthesis only
takes place in illuminated surface waters. If the mixed
layer is deep it is possible that phytoplankton will sink or
be carried down below the compensation depth (Chapter
2). reducing net production. In temperate waters. primary
production is minimal during winter when light levels and
temperatures are low and the upper water column is thor-
oughly mixed by storm action and convection (Backhaus et
at. 2003) . Phytoplankton blooms do not commence until
calmer, warmer weather in the spring leads to upper water-
column stratification. From this point on, phytoplankton
cells are retained in the upper mixed layer, benefit from the
increased illumination from the sun as it reaches higher
angles in the sky, and grow and reproduce rapidly. Phyto-
plankton require nutrients such as phosphate. silicate, and
nitrate to grow. As phytoplankton blooms develop, concen-
trations of these nutrients become depleted and the effect-
ive isolation of the mixed layer from the larger nutrient
pool beneath means that nutrients are not replenished. In
temperate waters, nutrient limitation may inhibit phyto-
plankton growth throughout the summer months. A second
bloom may though occur at the onset ofautumn when wind-
driven mixing brings nutrient-rich waters from beneath
 Chapter 7 Pelagic Ecosystems
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the pycnocline up in to the illuminated surface layer (Diehl
2002) . In the North Sea the classic two-peaked (spring and
autumn) phytoplankton bloom pattern has been disrupted
by eutrophication: riverine input of nutrients from agricul-
tural and industrial run-off have overridden natural nutri-
ent limitation and led to more-or-less continuous summer
phytoplankton production (Heath and Beare 2008) .
Although the development of stratification is a neces-
sary precursor to phytoplankton bloom formation in tem-
perate waters, the persistence of an upper layer that is
effectively cut off by density and temperature gradients
from the waters beneath can eventually inhibit phyto-
plankton growth.
A phytoplankton maximum can develop at the pycnocline
in high summer as this is the interface between nutrient-
rich deep water and illuminated but nutrient-depleted
surface stratified waters.
In regions of the world where upwelling is persistent
throughout the year (Box 7.2) nutrients tend not to be lim-
ited and annual primary production levels are high. How-
ever, in the Pacific off South America changes in prevailing
weather conditions associated with the El Nino Southern
Oscillation reduce the usually strong upwelling, and ensu-
ing nutrient limitation has dramatic negative consequences
for primary production and fisheries in coastal waters.
Tropical ocean basins tend to be permanently stratified and
primary production levels are low. As a consequence, sur-
face waters in these tropical regions lack particulate matter
and are very clear: such waters are termed oligotrophic.
Open ocean waters distant from land can be enriched with
nutrients in dust blown from land. Wind-blown (aeolian)
Saharan sand fertilizes the open Atlantic with iron. increas-
ing production (Jickells et al. 2005), but winds can also
bring pollutants and Red Sea plankton may be poisoned by
copper in desert dust (Paytan et al. 2009) . Other areas of
the world ocean have low phytoplankton biomass despite
the presence of high nutrient concentrations. These HNLC
(high nutrient, low chlorophyll) regions include the South-
ern Ocean and Equatorial Pacific, and hypotheses proposed
to explain their existence include grazing pressure and
absence of trace elements, particularly iron (Chapter 2) .
The oceans generate about half of Earth's annual global
primary production (48.5 Petagrams of 104.9 Pg C; Field
et al. 1998) but since 1999, global ocean primary produc-
tion has fallen by 0 .19 Pg C per year (Behrenfeld et al.
2006) . The majority of this reduction has occurred in the
permanently-stratified low latitude oceans (roughly 4S"N
to 45"S) because warming and strengthening stratification
have caused nutrient limitation. In polar regions, increased
wind strength (leading to increased mixing and nutrient
replenishment) and reducing ice extent (that reduces
water-column shading) could lead to increased open ocean
primary production, but these increases (e.g. 0.03 Pg C per
year since 2003 in the Arctic; Arrigo et al. 2008) will prob-
ably not counteract the mid-latitude reductions. Recently,
Smetacek (2008) has proposed that the depletion ofbaleen
whales in the southern oceans may be responsible for the
decline in primary productivity. With the removal of the
great whales from the ocean. the anticipated ecosystem
response was predation release for prey species such as
krill. However, krill have declined and have been replaced
to some extent by biota such as salps. Smetacek's (2008)
theory is that whales were keystone species in this ecosys-
tem. Krill consume phytoplankton and thereby capture ele-
ments such as iron. If krill die and sink to the ocean floor,
the iron is lost from the pelagic system. However, if the ktill
are consumed by whales, the iron is then defaecated back
into the pelagic zone and becomes available to primary pro-
ducers. Smetacek (2008) described this as 'manuring the
oceans' (see also Nicol et al. 2010) .
In the same way that fronts on weather maps mark
boundaries between different air masses. fronts in the sea
are boundaries between dissimilar bodies of water. Fronts
occur off estuaries at boundaries between fresh and salt
water, in shelf seas between tidally-mixed and stratified
waters, at continental shelf breaks adjacent to upwelling
regions and. at the global scale. between major current sys-
tems. Fronts tend to be sites with higher biological activity
than the surrounding water masses, often because nutri-
ents are transported upwards into the stratified euphotic
zone at fronts. Tidal-mixing fronts (also known as shelf sea
fronts) occur between tidally mixed and stratified waters.
They occur when the intensity of turbulent mixing caused
by tidally induced flow over the seabed is sufficient to
overcome the barrier to mixing caused by thermal strati-
fication. In simple terms, this is a function of the strength
of the tidal flow and water depth; a strong tidal flow will
generate sufficient turbulence to completely mix shallow
water. On the stratified side of the front, nutrient concen-
trations in the warm surface waters are depleted and the
strong thermal gradient prevents nutrients from beneath
being mixed upwards. Phytoplankton growth is therefore
nutrient-limited and low. On the well-mixed side of the
front, although nutrients are not limited, phytoplankton are
continually mixed down out of the illuminated surface layer
and growth is light-limited. Atthe front itself, stratification
weakens sufficiently to enable some vertical nutrient flux
but remains strong enough to hold phytoplankton in the
photic zone long enough for them to take advantage of the
nutrients. A study in the North Sea found new production
at tidal fronts to be low (Heath and Beare 2008) and it was
concluded that, in order to accord with the traditional view
that these areas are highly productive zones. they must be
loci of high recycled production. Increased phytoplankton
 7.4 Temporal and spatial variability in pelagic ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
production at fronts leads to higher zooplankton standing
stocks and increased densities of predators and underly-
ing benthos (see also Chapters 2 and 8). Plankton grazers,
including Basking sharks and Manta rays, may forage in
these food-rich zones (Priede and Miller 2009) .
Iron is thoug ht t o be one of the key limiting t race ele-
ments in HNLC regions, and experimental iron ferti liza-
ti o n in t hese locat io ns has stimulated phytoplankton
prod uction (Boyd et al. 2007).
Global variation in the pattern of annual primary pro-
duction is strikingly clear in images of averaged chloro-
phyll concentration obtained through satellite imagery
(see Fig. 2.5, Chapter 2) . Regional coherence in the pat-
tern of annual phytoplankton production has been used
as one diagnostic feature in the hierarchical separation of
the global ocean into distinct biogeographic biomes and
provinces (Longhurst 2006) . A biome is the largest coher-
ent community unit that it is convenient to recognize, and
Longhurst (2006) distinguishes four in the global ocean,
which are characterized by the principal mechanisms driv-
ing their mixed layer depth: in the Westerlies biome local
winds and irradiance force the mixed layer depth; in the
Trades biome the mixed layer depth is influenced by large-
scale ocean-circulation processes; in the Polar biome the
presence of buoyant. fresh water from ice melt in spring
constrains the mixed layer depth; and in the Coastal biome
diverse processes including upwelling force the mixed layer
depth. Within these biomes. 51 provinces are recognized
(Chapter 1). Separation of the global ocean into provinces
is very useful because it allows regional differences in physi-
cal oceanography to be used to gain understanding, and
make predictions. of regional differences in ocean ecology.
Knowledge that a particular area of ocean lies in a par-
ticular province enables predictions to be made regard-
ing ecosystem function there, even if field data for the
specific area are lacking.
7.4.3 Consequences for higher
trophic levels of variability in primary
production
Regions of the world's ocean with high primary productiv-
ity support richer pelagic communities. with higher total
biomass. than do regions with low primary production. In
fact there is a direct linear relationship between the mag-
nitude of annual primary production and nekton (fish and
squid) production (Sommer et at. 2002; Jennings et at.
2008) (Fig. 7.9) . This relationship is apparent in the dis-
tribution of global fish catches (Chapter 13) : nutrient-rich
-.,
7
s,
25
E
;; 20
1;;
•
- 15
=
s
'is
= 10
~
-
-S
~
/"
=
-5
+
~
3
u-
~ 2
: 1
0 50 100 150 200 250 300
Total phytoplankton production (g (m"2 yr 1)
Figure 7.9 The relationship between primary production
and nekton production. Fish and squid production =
(0.095 phytoplankton production) - 3.73, r' = 0 .96. 1
= Atlantic Ocean gyre centre, 2 = Atlantic Ocean gyre
boundaries, 3 = Hawaiian waters, 4 = Bothnian Sea, 5
= Gulf of Riga, 6 = Gulf of Finland, 7 = Baltic Sea, 8 =
Nova Scotian shelf, 9 = Gulf of Maine, 10= Mid-Atlantic
bight. Redrawn from Iverson 1990. Copyright 2000 by the
American Society of Limnology and Oceanography, Inc.
shelf seas and regions with strong upwelling account for
the vast majority of the world's commercial catch (Watson
& Pauly 2001), whereas oligotrophic central open-ocean
basins contribute little. Commercially important pelagic
fish species do not consume phytoplankton directly but usu-
ally predate zooplankton and micronekton that are primary
consumers. Understanding zooplankton ecology is there-
fore key to understanding fisheries production.
GLOBEC (global ocean ecosystem dynamics; http://www.
globec.org) was a global research effort to unde rstand
interactions between primary consumers, higher trophic
levels, and fishe ries.
Many zooplankton populations are bottom-up con-
trolled (that is they are limited by food availability) (Rich-
ardson & Schoeman 2004) . Zooplankton blooms are only
able to develop once phytoplankton biomass and produc-
tion has become sufficient to sustain zooplankton grazing
rates. In temperate waters, therefore. peaks in zooplankton
biomass occur in spring and autumn slightly after the phy-
toplankton blooms. In high latitudes, where seasonality is
extreme and the phytoplankton bloom is limited to a single
spring/summer peak. some zooplankton species survive
the dark. food-impoverished winter months in deep water
in a dormant state called diapause. Copepods including
Calanus finmarchicus in the sub-Arctic North Atlantic and
Calanoides acutus in the Southern Ocean build up large
stores of lipids during summer feeding, a small proportion
of which fuels their survival overwinter. At the end ofsum-
mer, growth and development are arrested and individu-
 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
als sink. over wintering in a sta te of hibernation at depths
between 500 m and 2000 m (Box 7.3) . In late w inter or
early spring, copepods emerge from diapause and migrate
to the surface to spawn. Because of the short production
season. the timing of reproduction is critical at high lati-
tudes. By using lipid reserves accumulated in the previous
year to fuel reproduction. these copepods can spawn early,
independent of the present year's phytoplankton bloom,
and ensure that their young are in place to fully exploit the
short lived phytoplankton bloom.
Co/anus finmarchicus survives food-depleted winter
months in the north Atlantic by drawing on lipid reserves.
This also enables it to produce young in advance of the
phytoplankton bloom in the following year.
The timing of the phytoplankton bloom not only influ-
ences zooplankton secondary production but also places a
significant control upon organisms that predate up on zoo-
Box 7.3: Diapause depth, water density,
and lipid composition
The overwintering depth of the copepod Co/anus finmar-
chicus varies throughout its distribution range in the north
Atlantic. In the eastern Norwegian Sea, for example, Cafo-
nus overwi nters at about 800 m, whereas in the Iceland
Basin overwi ntering is at around 150 0 m (Heath et al.
2004), despite the fact tha t both locations have similar
total water depths (c. 2000 m) . The water-colu mn vertical
temperature profile varies markedly throughout the north
Atlantic: in the eastern Norwegian Sea the temperat ure at
the overwintering depth is approximately O°C, whereas in
the Iceland Basi n it is much warmer (4°C) . This physical
variation provides much insight into the variation of the
overwi ntering depth. At the onset of diapause Co/anus
becomes physically inactive and sinks passively until it
reaches the depth where it is neutrally buoyant. This is the
depth at which the density of the copepod is the same as
the density of the surroundi ng seawater, which itself is a
function of ambient temperature and salinity. One of the
major contributors to variation in density between cope-
pods is lipid composition, such that density decreases as
the proportions of lipid increases. Using knowledge of
the temperature and salinity at the overwi nteri ng depth in
several locations, and hence the density there, it has been
possi ble to predict the propo rtion of lipid that should be
expected in individuals overwintering at particular loca-
tions. A very good linear relat ionship has been found
between predicted and actual values (Heath et al. 2004).
plankton. Developing fish larvae 'surf on the wave of zoo-
plankton production' and the match-mismatch hypothesis
(Cus hing 1990) proposes that larval fish survival w ill be
gre atest in years when the period of plankton production
overlaps most closely with the period oflarval food demand.
Satellite data that revealed between-year variations in the
timing of the spring phytoplankton bloom support this
hypothesis wit h regard to haddock (Melanogrammus aegle-
finus ) on the shelf east of Nova Scotia (Platt et al. 2003 ;
Fig. 7.10) . An index of larval haddock survival (size of age
1 year class divided by spawning stock biomass) showed
that two exceptionally strong yea r classes occurred when
the peak of the spring phytoplankton bloom was between
2 and 3 weeks earlier than the long-term average. An early
bloom may reduce larval mortality by starvation.
Survival of larval fish is greatest when the overlap
between the period of planktic food availability and food
demand by fish is greatest.
It is not yet clear what the main evolutionary drivers
of variation in copepod lipid co mposi tion are. In order
to survive the winter individuals need to descend below
the depth of wi nter mixing, and will also have increased
chances of survival overwi nter if they descend below
depths where predators can operate. In Norwegian fjords,
overwi nteri ng is shallower in fjords where visual predators
are absen t (Bagoien et al. 200 1), but the winter distri-
but ion of predators in the open ocean is not yet known.
Ironically, therefore, individuals tha t feed too successfully
over summer and lay down excessive lipid reserves may
be unable to sink to depths below predators; th is would
p rovide a strong selective pressu re agai nst over-con-
sumption and may be one reason w hy some copepods
enter diapause early in the year w hen the phytoplankton
b loom is still in full swing. Since current flow is different
at different depths, the overwintering depth will also have
a profound influence on the location at w hich individual
Co/anus surface afte r diapause. In order to complete its
lifecycle successfully, Cafonus has to surface at a location
where offspring can be spawned and hatch and eat, and
descend to overwinter to complete the lifecycle. It is likely
that few depths will enable this to be achieved, providi ng
another sou rce of selection. It is clear that the lifecycle
of Cafonus is t ied very closely to its environment; under-
standi ng the environmental space-ti me dynamics will be
vital to gaining full understanding of regional variability in
Co/anus abundance and consequences to higher t rophic
levels such as fis heries (Heath et al. 2008).
 7.4 Temporal and spatial variability in pelagic ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Spatial, as well as temporal. coherence is required
between production and consumption if high-biomass
pelagic communities are to develop. At the large scale,
it has been suggested that iron fertilization in regions of
low primary productivity could enhance production up
the food chain to zooplankton and fisheries, and that the
increased photosynthesis could also lead to an increased
drawdown of atmospheric carbon dioxide (an enhanced
biological pump) that may mitigate against climate change
(Lovelock & Rapley 2007) . Complex trophic interactions,
however. make implementation of this far from straightfor-
ward (Cullen & Boyd 2008). Indeed, recent observations
of phytoplankton blooms in the Southern Ocean, stimu-
lated by natural iron enrichment of waters flowing past
the Crozet Islands, suggest blooms stimulated artificially
are weak, perhaps because oflarge losses of the artificially
added iron. This has significant implications for proposals
to mitigate the effects ofclimate change through purposeful
addition of iron to the ocean (Pollard et al. 2009) . At the
smaller scale, patchiness is essential for maintaining eco-
system function. If phytoplankton and grazers were mixed
homogenously, then resource depletion would soon occur,
whereas patchiness and spatial segregation enable higher
overall biomass to be maintained (Brentnall et al. 2003;
Mitchell et al. 2008) . Furthermore, if zooplankton did not
aggregate in high densities, then pelagic filter-feeders, such
as basking sharks (Cetorhinus maximus) and baleenwhales,
would not be able to survive on a diet of these organisms.
Whales incur high energetic costs while foraging (Acev-
edo-Gutierrez et al. 2002) and it has been estimated, for
example, that Right whales (Eubalaena glacialis) require
copepod prey concentrations to exceed a minimum thresh-
old of 4500 individuals m~3 of seawater just to balance the
energy expended during feeding (Beardsley et al. 1996).
Furthermore, whilst some euphausiid species aggregate to
form swarms. perhaps to gain protection from predators,
paradoxically it is swarm formation that makes krill viable
prey for whales: it has been suggested that if krill off Nova
Scotia were dispersed uniformly at average densities, then
fin whales feeding there would need to swim at 900 km h'
to eat their fill in an 8-h period (Brodie et al. 1978) .
If phytoplan kton and grazers were mixed homogenously,
th en resource deplet ion would soon occur, whereas spa-
ti al segregation enables higher overall biomass to be
maintained .
Frontal regions tend to be characterized by increased
primary production and to support particularly rich pelagic
communities (Box 7.3). Fronts are therefore sites of intense
feeding activityand are targeted by mobile predators includ-
10
_ 8
~-
1981
•• 6
-g
•
c 1998
-~
.;: 4
•
1980
2000
2 2001 •
•
2 1
• •1979,1997
0 -I -2
Anomalies in the timing of spring blooms (weeks)
Figure 7.10 Larval haddock survival (size of the year
class at age 1 (R) divided by spawning stock biomass
(SSB» against deviation from the mean time of the annual
peak in phytoplankton production. Timing of the peak
of the spring phytoplankton bloom explains 89% of the
variance in larval survival , providing strong support for
the match-mismatch hypothesis. Redrawn from Platt et al.
(2003) with permission from the author.
ing fish, squid, marine mammals, and birds (Durazo et al.
1998) . The exact mechanisms by which predators locate
prey in the wide expanse of the open ocean remain largely
unknown and different cues are likely to be important at
different spatial scales (Fauchald et al. 2000) . A growing
body of evidence suggests that many marine predator spe-
cies do not forage at random across the pelagic expanse.
but follow search patterns with Levy-like distributions:
predators make occasional long-distance relocations to
'new' search areas and undertake numerous short forays in
each area (Sims et al. 2008) . This type of foraging may be
an evolutionary response to distributions of prey including
zooplankton that also exhibit Levy distributions. In some
ecosystems prey are located regularly in production 'hot
spots' (Davoren et al. 2003), attracting larger predators
in a predictable manner. Conservation measures aimed
at reducing conflict between wildlife and fishers need to
account for geographic variability such as this in ecosys-
tem management plans. Fisheries for Antarctic krill. for
example. may in future be required to operate outside the
foraging areas ofland-based central-place foragers during
their breeding season (Constable & Nicol 2002) .
Conservation measures aimed at reduci ng conflict
between wild life and fishers need to take in to account
th e fact th at predators sometimes forage at production
hotspots that occur at oceanographic features such as
fro nts.
 Chapter 7 Pelagic Ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
7.5 Sampling the open ocean
The some times extreme horizontal, vertical, and tempo-
ral patchiness that is characteristic of pelagic ecosystems,
and the huge size-range of organisms inhabiting the open
ocean, present considerable difficulties for quantitative
sampling.
Early studies of the open ocean depended almost com-
pletely on fishing nets to sample living organisms. Netting
remains an important component of biological oceano-
graphic research, but the systems in use tod ay are consid-
erably more complex than those used in the pioneering
d ays (Wiebe & Benfield 2003) . These days, nets are often
equipped with depth, temperature, salinity, and other sen-
sors. Data from these sensors can be relayed to the ship in
real time, either along conducting cables or via acoustic
links, and enable nets to be placed accurately in the sec-
CURRENT FOCUS: Microlayers and the
'paradox of the plankton'
In 19 61 Hutchinson expounded the 'Paradox of the
Pl ankton', questioning how it could be possi ble for such a
large number of plan kton species to coexist in the appar-
ently homogenous pelagic environment. The t radi tional
ecological view is that a variety of niches are needed if
species are to coexist, otherwise competitive exclusion
enables a single species to dominate. Recent experi men-
tal and theoretical work supports this view (Levine and
Hill e Ris Lambers 2009). Traditional pelagic-sampling
techniques, such as vertical netting, reversing thermo m-
eters, and early echo-sou nders, provided only quite low
vertical sampli ng resolution, and contributed to the per-
ception th at, other than the thermocline, there was little
vertical structuring in the water colum n (see Tech niques
figure, upper panel). A w ater colum n with little ver tical
heterogeneity woul d provide little opportunity for niche
differentiation, and a low number of niches should sup-
port only low diversity. Advances in the resolu tion of opti-
cal and acoustic sampling tech nology (see Techniques
box) have, however, led to the discovery of widesp read
'thin layers' of high biological activity in the ocean (McM a-
nus et al. 2003). Th e existence and persistence of plan k-
tic thin layers generates great biological heterogeneity
in the water colum n, and may go some way to expl ai n
the 'Paradox of the Plankton'. Thin layers, which range in
thickness from a few centimetres to a few metres, may be
many kilometres in horizo ntal extent and may persist for
tion of the water column of particular interest (Brierley
et al. 1998). Optical particle counters (OPCs) can be used
instead of nets to obtain estimates of zooplankton numeri-
cal density (He ath 1995), and photograph ic and video
devices en able high -qu ality im ages of ocean inhabitants
to be obt ained (Benfield et al. 1996). Light is attenuated
rapidly by seawater though, and visu al sampling is often
constra ined by water clarity (Chapter 2) . Sound, on the
other hand, propagates very efficiently through seawater,
as is testified by the long-range vocal commun ications of
some whales. Scientific echo-sounders can be used to detect
and quantify abundance of zooplankton and fish (Holliday
& Pieper 1995), and ever-increasing sampling resolution
(see Techniques box) is detect ing biologically important
features such as micro-layers (McManus et al, 2003), which
are likely to be of very m ajor importance to pelagic ecosys-
tem function (see Curre nt Focus box).
several days. Thin layers produce micro-environments of
physical, chemical, and biological parameters. They con-
tain densities of organisms several orders of magnit ude
highe r than adjacent depth zones (Benoi t-Bi rd 2009),
and may be important fo ragi ng sites for fish and other
pred ators. Layers at different depths in the same area
may contain distinct plankton assemblages. The species
or populations that comprise each distinct thin layer prob-
ably aggreg ate in response to different sets of biological
and/or physical processes.
Microlayers someti mes occu r at the pycnocline as zoo-
plankton forage on material that is suspended there, but
may be deeper or shallower. Layers can occu r in strati-
fied water where current sheer is low, but sheer has also
been proposed as one of the forming mechanisms. Some
phytoplankton cells are motile and swi m upwards against
gravity. When they swim upwards into shear zones, zones
where the direction of ho rizo ntal flow changes rapidly
over a sho rt vertical range, they are made to t umble
because of an interaction of gravitational and viscous
torques. When the shear exceeds a critical threshold, tum-
bling prevents the phytoplankton from swim ming further
upwards and they become trapped- the process is called
gyrotactic trappi ng (Du rham et al. 2009; see the figu re
below ) . This mechanism is a good example of how b io-
logical patchiness arises as a consequence of physical
heterogeneity in the ocean. Understa nding exactly how
physical and biological processes interact could lead to
more powerful ecosystem models of, for example, the
fo rmation of harmful algal blooms (Grunbaum 2009) .

lu} Ib}
~UI ZI
- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - --
x...I----:-+-~
----------------- ----------------------
T,
ulzl
I Hul az I
Gyrotacti c trapping. (a) A gyrotacti c phytoplankton 's
centre of mass (red) is displaced from its ce nt re of
buoyancy (x = z = 0). As a result, the swimming direc-
tion in a shear flow, u(z), is set by the balance of gravi-
tational (Tg ) and vi scous (T) t orques. V is swimm ing
While modern imaging and acoustic technology have
improved our ability to sample the ocean realm , we con-
tinue to be reliant upon often-rudimentary nets to obtain
biological samples.
At the larger scale, organisms that must come to the sea
surface to breath (e.g. seals, whales) , or that forage over
the sea surface (e.g. seabirds) , can be counted at sea by
observers on research vessels. Alt hough much biological
oceanograph ic data are still collected from sh ips, logistic
cons tra ints place restrictions on the amo unt of time that
ships can spend at sea. In order to make longer term obser-
TECHNIQUES: Active acoustic
sampling
Li ght is attenuated rapidly by seawater and travels only
relatively short distances, but sound propagates very
efficient ly. Thus, whereas cuttlefish can use changes in
skin colouration to communicate visually over ranges of
several metres, baleen whale s use low-frequ ency sound
(between about 10 and 30 Hertz) to communicate
7.5 Sampling the open ocean
F====:: S" ~ ~
~( )
speed and m is mass. (b) Schematic of gyrotactic trap-
ping. Cells can migrate vertically at low shear but tum-
ble and become trapped where lSI > SCR' accumulating
in a thin layer. (From Durham et al. 2009.)
vations, or observations over large extents of ocean, other
sampling platforms or techniques are required. Moored
instruments can be used to collect long time-series of data
from spot locations (Schofield et al. 2002). Auto no mous
underwater veh icles (Box 7.S), gliders , and vertically-
profiling floats, such as those in the Argo network (www.
argo .ucsd.edu) , have the potential to be able to operate in
weather conditions that curtail sampling from ships, and in
add ition can work in environments that are impenetrable
to sh ips. These autonomous and Lagrangian platforms and
sensors ('ALPS', Dickey et al. 2008) are providing a wealth
of valuable in situ data.
over ranges of kil ometres and beyond. Dolphins, sperm
whales, and other toothed whales use sound at higher
frequencies (40 Hz- 30 0 kH z) to locate prey in turbid
and deep-hence dark- locations. Sound is a very effect-
ive medium for scientific sampli ng in the ocean, and a
variety of devices are in common use for pelagic and
seabed exploration. The process of actively transmitting
sound in to the water and detecting the returned echoes
is called active acoustic sampling (as opposed to passive
 Chapter 7 Pelagic Ecosystems
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sampling w hich involves j ust listening, for example for
animal vocalizations).
In the most basic form of active acoustic sampling,
downward-facing echo-sounders transmit regular pulses
of single-frequency sound ('pings') that are reflected or
backscattered by the seabed and targets in the water col-
umn. A typical ping might be 1 millisecond long, and ping
rates of 1 ping per second can be achieved to sample the
entire water column in the c. 200 m depths of on-shelf
locations. The frequency of choice for biological sampling
is usually in the range of tens to hundreds of kHz. Bio-
logical targets can include single fish, fish schools, plank-
ton, and aggregations of organisms that in some cases
form continuous layers. Layers in mesopelagic depths
are called deep scattering layers. These are a promi nent
and ubiquitous feature of the world ocean, comprising
commu nities of crustaceans, myctophid fish and other
organisms, and have been known since the early days
of acoustic sampli ng in the 1960s. Echo-sounders oper-
ated continually along a research vessel's survey track
yield data tha t provide a two-dimensional slice through
the watercolumn (2D; x = distance, y = depth). A visual
representatio n of these data is known as an echogram
(Fig. 7.5). Echo-sounders can also be mounted on fixed
moorings, facing upwards or downwards, and when oper-
ated continuously produce a 2D dataset, where the x-axis
on the echogram is time rather than distance.
The strength, or intensity, of an echo from a water-
colum n target is a function of many factors including tar-
get size, shape, density, and acoustic frequency. In very
general terms, targets scatter sound most efficiently w hen
the sou nd waves have a similar wavelength to the target
size. Wavelength (A, m), frequency (f, Hz ) , and sound
velocity (c, m S·1) are linked according to the equation:
c =f 'A,
from which it can be seen that for a fixed sound velocity
(a nominal value for the speed of sou nd in sea water
is 1,500 m s' ") waveleng th decreases as frequency
increases. Sound at 38 kHz has a wavelength of approxi-
mately 3.9 cm, and 12 cm anchoveta (Engraulis ringens)
tha t have swim bladders about 4 cm long (air-filled swim
bladders are very strong acoustic targets) will yield an
echo almost twice as intense at 38 kHz than at 120
kHz, where the wavelength is 1.2 ern. Euphausiids j ust
15 mm long, by contrast, including Antarctic krill Euphau-
sia superba, return echoes that are about 35 t imes more
intense at 120 kHz than at 38 kHz.
The fac t that different organisms produce different
re lat ive echo intensities at different frequencies, or dif-
ferent echo spectra, can be used to discriminate different

Acoustic Frequency: 1100 kHz

_ 15 ~:------:==:::i==~===;;;;;;;;;;;j;;;;;;;;;;;;;==1
-"".'"
E 10

~ 5
oI":-::-~------------
60 min, 2m

• •
" •

o 1min, 0.125m
12:00 15:00 18:00 21 :00 00:00
Time of Doy

-80 -75 -70 -65 -60 -55 -50 -45 -40 -35 -30
Volume Smtterlna Strencth fdBl

The bottom panel shows an acoustic record co ll ected in 1998 by an upward-looking 1100 kHz echo-sounder.
The colour scale shows echo intensity, which is greatest in regions of the water column where organism packing
density or biomass is highest. The record has a sampling resolution of 1 minute x 0 .125 m, and reveals a per-
sistent thin layer between 5 and 10m from the echo-sounder. The upper panel shows the same data averaged
on to a 60 minute x 2 m vertical grid , which was the state-of-the-art as recently as 1994: no fine layer is evident
in that record. From Holliday et al. 2003.

species and/or sizes of targets. This in turn enables the
development of automated processes to identify and sum
echoes from particul ar species, and for abundance esti-
mates for species to be generated from acoustic survey
data in a robust and repeatable manner. Annual biomass
est imates of numerous pelagic species includi ng krill, her-
ring, and anchovy are determ ined fro m acoustic surveys,
and these estima tes feed in to processes that set annual
catch quotas.
The resolut ion of acoustic sampling has increased
greatly in recent years, and will likely continue to do so
given ongoing engineering and electronics advances. The
figu re on the previous page shows how high-resolution
sampling by a moored echo-sounder has revealed the
There are essentially two strategies that can be fol-
lowed when sampling the dynamic pelagic environment:
Lagrangian or Eulerian. Lagrangian or current-following
sampling obtains time-series of data from the same par-
cel of water, whereas Eulerian sampling obtains data
from the stream of water that passes by a fixed geo-
graphic location. These contrasting views of space and
time can give markedly different perspectives on biologi-
cal and physical processes.
Earth-orbiting satellites are able to provide coverage of
the entire surface of the global ocean on a weekly basis and
deliver near-synoptic information on, for example, sea sur-
face temperature, chlorophyll concentration, and frontal
position (Miller 2004) .
Satellites can also be used to track the movements of
larger an imals as they forage at sea over extended periods
of time (Thompson et al. 2003) and can relay d ata from
instruments attached to the an imals. Leatherback turtles
(Dermochelys coriacea ), for example, have been tracked
in the north Atlantic (Hays et al. 2004) and time-depth
recorders attached to their carapaces h ave revealed that
they undertake asto nishingly deep di ves (to more than
1000 m; Houghton et al. 2008) . Leatherbacks are criti-
cally endangered, and a major source of mortality for them
is capture by pelagic fisheries. Knowledge of leatherback
distribution and dive characteristics obtained via satellite
telemetry could lead to the implementation of conserva-
tion measures designed to reduce the interaction of turtles
with fisheries, and thus reduce by-catch (Hays et al. 2004) .
7.5 Sampling the open ocean
presence of persistent thin layers. The Current Focus box
provides additional details on these hith erto unknown
fine-scale features, features that could explain the main-
tenance of biological diversity in pelagic ecosystems.
Multi beam echosounders sample a fan of beams that
might make up an almost- 180° swath beneath a vessel.
When operated continually along a survey track, these
instruments deliver a th ree-dimensional (3D; depth x
along-track positio n x across-track position) view of the
water colu mn (Gerlotto et al. 199 9) . Multibeam sonars
enable entire fish schools and krill swarms to be imaged,
providi ng new insig hts into agg regative behaviour and
the way in which predators interact with prey (Cox et al.
2009).
In addition to providing fascinating data on the behaviour
of an imals, sensors attached to animals can, by 'exploit-
ing' their behaviour, provide a completely new view of
ocean processes. Elephant seals, for example, undertake
long journeys in the Southern Ocean in winter, travelling
to oceanographically important locations at times of year
when conventional research vessels seldom venture. CTD
profiles from instruments attached to these animals have
cast new light on sea ice formation and dyn amic frontal
processes in the Southern Ocean (Charrassin et a1. 2008) .
By measuring the high-latitude ocean during winter, ele-
phant seals fill a 'blind spot' in our sampling coverage, and
these 'an imal oceano graphers' have the potential to greatly
improve our understanding of ocean fun ction.
Satellites can relay information from tags attached to air-
breathing animals, such as whales and turtles, collecting
data about their behaviour and patterns of movement
in near real time.
The capacity of scientists to be able to collect d ata from
the pelagic realm seems ever to be increasing. Plans are
afoot to establish a series of permanent, automated ocean
observatories that will be able to deliver multidisciplinary
data continuously in real time, yea r on year. Although these
systems will contribute enormously to our understanding
of ocean ecosystem fun ction, they will present new ch al-
lenges in terms of extracting meaningful summaries from
potentially overwhelming quantities of d ata.
 Chapter 7 Pelagic Ecosystems
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Box 7.4: Autonomous underwater

vehicles

Autonomous Underwate r Vehicles (AUVs) are unmanned

submersibles that can be programmed to navigate in
th ree dimensions underwater. They can carry a variety
of scientific instruments and are able to make measure-
ments in parts of the ocean th at are inaccessible, either
physically or op erationally, to conventional research
platforms such as ships. The Autosub AU\/, for example,
has been equipped wi th a scientific echo-sounder and
deployed on missions beneath Antarctic sea ice. There,
it has made obse rvations on the distribution of krill
under ice, and of ice thickness, that were impossible to
make using ice-breaking research vessels (Brie rley et al.
2002). Autosub is among the largest of AUVs presently
ava ilable to the scientific community, with an instrument
payload capacity of 10 0 kg (we ight in water). Autosub
is 7 m long x 1 m in diameter, weig hs 2 400 kg, is pow-
ered by manganese alkali batteries, propeller-drive n, has
a range of about 800 km, and a maximum depth capabil-
ity of 1600 m. Web lin k: http:/ /www.noc.soton.ac.uk/
index.nf/usl_php?page=as (photog raph: Andrew Bri-
erley). Autosub has con tinued to pioneer the exploration
of hostile, under-ice envi ronments. This exploration is
not wi thout risk though and in 2005 the origi nal vehicle combines a high depth capability (6000 m) with long
became stuck in Antarctica under the Ronne Ice Shelf. range (500 km) . These characte ristics, that are usually
Since then, however, developments have con tinued, and mutually exclusive, were achieved by developing pressure
Autosub has ach ieved missio ns of over 50 km beneath balanced lithium polymer batte ry tech nology, eli minat-
the Pine Island Glacier. A new generation Autosub 6000 ing the need for expensive and bulky pressu re resistant
with deep ocean capability has been built. Autosub 6000 housings.

7.6 Pelagic fisheries
Fisheries for pelagic species have the potential to be among
the m ost sustainable and least d amaging to the enviro n-
ment. Shoaling species like the Atlantic mackerel (Scom ber
scom brus) and North Sea herring (Clupea harengus) form
single-species agg regations, and by-catch of non-target spe-
cies is minor compared to the demersal sector (Chapter 13).
Stocks of mackerel, in particular, seem to be bucking the
global trend of decline and faring well under good m anage -
ment and regulation. Myctophids, or lantern fish, are small
mesopelagic fish that form a major component of oceanic
deep-scattering layers. They have been fished historically in
the sout h-west Indian Ocean and in the South Atl antic, but
fishing ceased in 1992 because of unfavourable econom ics
and m arket-resistance, and myctophids are not presently
under threat.
Fisheries for pelagic species have the potential to be
among the most sustainable and least damaging to the
environment.
Planktivorous fora ge fish, such as sardine and anchovy,
h ave vital ecosystem functions, particularly in upwelling
zones, where they form an important mid-trophic-level link
in so-called wasp-waist ecosystems (Cury et al. 2000). In
these systems one, or just a few species, of small planktivo-
rous fish dominate their trophic level. Abundance of these
species can fluctuate wildly under variable enviro nment al
regimes and high fishing pressure and may result in m ajor
ecosystem changes. Fishing for large tropical pelagic fish,
including tuna and jacks, has also had substantial impact.
Analyses of long-lining d ata suggest that 90% of biomass
of large pelagic fish m ay have been removed (Myers &
Worm 2003) . Open-ocean fisheries have tended to develop
 7.7 Regime shifts in pelagic marine ecosystems
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
ahead of management procedures (maybe by as much as 15
years) and, in the case of pelagic long-line fisheries, it is pos-
sible that the estimated pre-exploitation biomass to which
management processes are anchored are unrealistically
low because they represent already-depleted stock levels.
This 'missing baseline' presents particular difficulty for the
long-term restoration ofstocks because the size of the stock
pre-exploitation remains unknown, and thus it is very dif-
ficult to say when, or if, restoration has been achieved. Not
only has long-lining hit pelagic fish hard, but it has been,
and is still, responsible for substantial declines in albatross
populations. Albatrosses take baited long-line hooks as they
are thrown from fishing vessels, drowning as the long-line
sinks. Some populations are showing marked and continu-
ing decline (ruck et al. 2001) but elsewhere, notably off
South Africa, efforts to educate fishermen as to practices
that can limit conflict are having major success: for every
100 albatrosses being killed in fisheries in South African
waters in 2006, 85 are now (as of 2009) being saved. Seine
netting for tuna also suffers from by-catch. particularly of
dolphins, although, following international outcry, prac-
tices are in place to reduce the impact to levels that are now
ecologically sustainable (Hall 1998).
It is possible that the estimated pre-exploitation pelag ic
fish biomass t o w hich management processes are
anchored are unrealist ically low because they represent
already-depleted stock levels, the so called 'rn issinq-
baseline' effect.
The whole issue of 'dolphin-safe' tuna remains the sub-
ject of debate and there were moves in the United States
to ease legislation relating to the defi nition of the prod-
uct. See also 'Eco labelling' in Chapter 16.
Squid are fished on the open seas, mostly using hooked,
coloured lures (jigs) at night to catch animals attracted to
bright lights. The high-intensity lights used to attract squid
to jigs are so bright that they can be seen from satellites, and
this has opened a new mechanism for potentially monitor-
ing and managing open-ocean squid fisheries (Rodhouse
et al. 2001) . Robust management is particularly important
for squid because they are short-lived. often semelparous
(spawn once and die), species and therefore vulnerable
to over-fishing. since there are few cohorts to provide a
buffer from failure of any single generation. Squid also
respond rapidly to changing oceanographic conditions
and it is becoming increasingly clear that it is essential to
understand interactions between squid and their ocean
environment in order to predict interannual variations
in recruitment. Recruitment of the squid Illex argentinus
to the Falkland Islands' fishery, for example, increases in
years when water temperatures over the squid egg-hatching
grounds are favourable (16 to 18'C) .ln years when move-
ment of the highly dynamic front between the Brazil and
Falkland currents displaces waters of favourable tempera-
ture from over the hatching area, recruitment is reduced
(Waluda et al. 2001) .
Semelparous animals, such as squid , are particularly
vulnerable to over-fishing as their populations are not
composed of multiple cohorts that provide a safety net
against over-exploitation.
7.7 Regime shifts in pelagic
marine ecosystems
Ecologists have long recognized that ecosystems may exist
in 'multiple stable states'. In the oceans, conspicuous and
rapid jumps from one state to another have become known
as regime sh ifts (Scheffer et al. 2001) . Shifts typically
take less than one year to occur and regimes may persist
for decades (Hare & Mantua 2000) . Regime shifts may
be driven by climatic changes, fishing pressure, or both,
and may be evident in physical and biological ecosystem
parameters. In the north Pacific. for example, statistically
significant regime shifts in 1977 and 1989 are apparent in a
composite index of 100 biological and physical time-series,
including the Pacific Decadal Oscillation (PDO), zooplank-
ton biomass estimates, and salmon catches (Fig. 7.11).
Regime shifts present major challenges for scientists
attempting to manage fisheries. In the North Sea a regime
shift in 1988 was evident from plankton time-series data
from the Continuous Plankton Recorder (CPR) surveys
(Reid et al. 2001) . It has been suggested that this shift was
caused by increasing flow of Atlantic waters into the North
Sea, an increase that was correlated with a change in the
North Atlantic Oscillation Index (NAOl) (Heath & Beare
2008) . Recruitment ofcod (Gadu.s morhua) in the North Sea
has declined since the mid-1980s: it is possible that changes
in the plankton following the regime shift have had a nega-
tive impact on the supply of food to young cod (bottom-up
control) and have brought the end of the 'gadaid outburst'
that previously brought good catches of cod (Beaugrand et
al. 2003) . In the face ofsuch possible environmental impacts
on fisheries, it is clear that future attempts to manage fisher-
ies will need to take environmental factors into account, as
well as data on fish population dynamics and catch levels.
This realization has led to calls for the development of an
holistic, ecosystem approach to fisheries management (Pit-
kitch et al. 2004; Chapters 13 and 16).
The 19 88 regime shift in the Nort h Sea may have been
caused by an infl ux of nut rient-rich Atlantic water.
 Chapter 7 Pelagic Ecosystems
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Although not necessarily a symptom of regime shift per
se.jellyfish appear to have increased in prominence in many
pelagic marine ecosystemsworldwide in recent years (Rich-
ardson et at. 2009). Jellyfish blooms have occurred in the
Bering Sea. the northern Benguela current. and elsewhere,
possibly in response to climate and fishing effects. Indeed,
it has been suggested that jellyfish-dominated communi-
ties are the inevitable end-point in pelagic ecosystems per-
turbed by fishing (Pauly & MacLean 2003) . In the North
Sea, correlations between the abundance ofjellyfish and an
Index describing the periodically fluctuating North Atlantic
Oscillation (NAOI) have been detected (Lynam et at. 2004) .
Furthermore it seems as though the recruitment of herring
(Clupea harengu.s) in the North Sea is adversely affected by
high jellyfish abundance. The jellyfish-herring link is prob-
ably mediated by a number of associations. Jellyfish prey
upon herring eggs and larvae. and also compete with her-
ring for zooplankton food . Juvenile haddock gain shelter
amongst the tentacles ofsome jellyfish, so haddock recruit-
ment benefits from the presence ofjellyfish: adult haddock
are predatory upon herring and jellyfish therefore mediate
increased predation by haddock (Lynam & Brierley, 2007) .
Complex interactions between climate and jellyfish may
therefore impact fish stocks. even in the absence of fish-
ing. and could have major implications for the recovery of
fish stocks. even after any cessation of fishing. Understand-
ing these linkages will be important for 'ecosystem-based'
management: indeed, it has already been shown that imple-
mentation of the jellyfish-haddock-herring interaction in
an ecosystem model of the North Sea improves predictions
of gadoid recruitment (Mackinson & Daskalov 2007) .
Jellyfish-dominated pelagic communities may be one
consequence of overexploitation of pelagic fish stocks.

1977 regimeshih There has been an almost exponential rise in the inci-
1.0
dence of the term 'regime shift' in the scientific literature
T L iTT II
~ 05 II~ ~ ll i since the early 1990s. It is possible that this is because the
incidence of regime shifts is increasing, or that accumulat-
Ia 0
ing time-series of data are enabling more changes to be
III I -r
'" ·05
~ , I IIq
detected. A note of caution is perhaps necessary regarding
this apparent increasing prevalence, however: simulation
·1.0
, ,
1965 1965 1975 1980 1985 1990 studies looking at random, independent time-series with
the same frequency content as the Pacific Decadal Oscilla-
tion have shown that techniques used to identify 'regime
1989 regimeshih shifts' may find them in noise. Detection of step-changes
1.0
does not therefore necessarily provide evidence of pro-
J!! 05
IlL .. T cesses leading to any meaningful regime shift (Rudnick &
£:
E
liI I ~ 1"
Davis 2003), since the step changes may be artifacts of the
0
~ data.
Jl ·05 I I
, 1 .1 • .1 .1
·1.0
1975 1980 1985 1990 1995 2000 7.8 The future for pelagic
marine ecosystems
Figure 7.11 Mean and standard error of a composite
index of 31 physical and 69 biological parameters from With an ever-increasing human population. and an ever-
the north Pacific between 1965 and 1997, showing growing demand for food protein, it seems likely that pres-
significant step changes or 'regime shifts' in 1977 and sure on the open ocean is likely to continue to grow. There
1989. The physical time-series represent atmospheric is a history of fisheries advancing further from shore. into
and oceanic processes, while the biological time-series deeper and more distant waters, as conventional coastal
all relate to oceanic species ranging from zooplankton resources are depleted, and this looks set to continue.
to salmon and groundfish. Each of the time-series was Fishing effort has already had major impacts on the global
normalized before plotting and statistical analysis by ocean. As traditional fish species are removed, fishing
subtracting the mean across both regimes and then effort turns from these higher trophic-level predators to
dividing the data for each regime by the standard smaller species. This phenomenon has become known as
deviation for that regime. Standard errors for each year fishing down the food web (Paulyet at. 1998) and is eco-
were computed as In,where S is the standard deviation logically unsustainable.
across all variables within a year and n is the number Humans are not just altering the open-ocean ecosys-
of time series used in the calculation «100). Redrawn tems by removing biomass but are also degrading it by
from Scheffer et al. 2001 with Nature Publishing Group's addition. The incidence ofwaste in the ocean is increasing,
copyright permission and permission from the author. with floating rubbish potentially distributing species far
 7.8 The future for pelagic marine ecosystems
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

beyond their usual ranges, leading to alien colonizations of
distant shores (Barnes 2002) . Introductions ofalien species
in ballast water from cargo ships has also had devastating
effects on pelagic ecosystems. such as the introduction of
the ctenophore Mnemiopsis leydii to the Black Sea (Kideys
2002). This ctenophore, a native of the eastern USA, was
predatory upon fish eggs and led to the collapse of the Black
Sea anchovy fishery. Dumping CO2 at sea in an attempt to
reduce further increases in atmospheric concentrations is
being investigated (Hunter 1999) . As well as the addition
ofobjects and organisms, human activityhas also increased
noise levels in the ocean. Low-frequency noise from ship-
ping, oil-exploration. and military activities may adversely
impact cetacean communication and foraging (Croll et
al. 2001) by masking the sounds these animals generate.
Killer whales (Orcinus orca) in the waters of Washington
State, USA, increase the lengths of their calls significantly
(by about 15%) in the presence of whale-watcher boat traf-
fic, and probably do so in an attempt to overcome the noise
generated by these boats that may mask their usual calls
(Foote et al. 2004) . Propagation of underwater sound in the
range of frequencies used for cetacean communications will
increase as the ocean become more acidic (Chapter 15) .
Expected changes in ocean acidity could enable sounds to
travel up to 70 per cent farther underwater, increasing the
levels of background noise in the oceans and potentially
affecting the behaviour of marine mammals (Hester et a1.
2008) .
A recent forecast of the likely state of aquatic ecosys-
tems in 2025 identified climate warming as the most sig-
nificant single threat (Chapter 15), and climate changes
have already had measurable impacts on sea-ice extent
and zooplankton distributions (Polunin 2005) . Tempera-
ture change is the most pervasive threat to marine eco-
systems globally (Halpern et al. 2008) and, if it continues
unchecked, it could result in multiple extinctions before
the end of this century (Jackson 2008; Brierley and Kings-
ford 2009) . Perhaps the biggest climate-related threat to
north Atlantic pelagic marine ecosystems arises from the
possibility that increased warming and consequent freshen-
ing of the Arctic may switch off the North Atlantic current
(NAC) and hence perturb global ocean circulation (Rahm-
storf 2002) . Because of interactions between circulation,
vertical mixing, nutrient supply, and production, reduction
of the NAC could reduce north Atlantic plankton biomass
by more than half, and reduce global export production
by more than 20% (Schmittner 2005) . It is probable that
changes like this have happened multiple times during the
Earth's history, and occurred over very short periods. If, as
some models predict, this were to happen again in the near
future, the consequences for the Earth's ecosystem and cli-
mate would be so severe that concern for the state of the
pelagic realm would probably not be at the top of human-
ity's agenda.

The incidence of waste in th e ocean is increasing, wit h

floating rubbish potentially distributing species far
beyond their usual ranges leading to alien colon izat ions
of distant shores.

Chapter Summary
• The pelagic realm is highly heterogeneous, and production is patchy in both space and time. Pro-
duction is generally higher closer to land, because of increased nutrient input (rivers, upwelling),
and close to the surface because of light availability. There is a direct link between primary produc-
tion and fisheries' production.
• Organism size has a major bearing on mobility in the pelagic environment. Plankton are generally
small «10 mm long) and are unable to swim against currents, but drift passively on them. Larger
organisms (nekton) can move actively against currents. Plankton can however move vertically and
undertake pronounced diel migrations that contribute significantly to the 'biological pump'.
• Pelagic food-webs are size-structured: small organisms are consumed by a succession of larger
grazers or predators. Most biomass occurs at the lowest trophic levels (grazers) and gradually
decreases at increasingly higher trophic levels.
• Environmental heterogeneity and the large range of pelagic organism-size (from plankton to
whales) presents a severe challenge for sampling the pelagic environment. Technological advances
 Chapter 7 Pelagic Ecosystems

provide the means to collect ever-increasing quantities of data, but net sampling remains important
for collection of biological material.
• Pelagic fish that form large single-species' shoals should be amongst the most straightforward to
manage and can be exploited with little risk of bycatch. Nevertheless, even pelagic species that
inhabit remote locations far from land have been impacted severely by fishing.
• Pelagic ecosystems can suffer step-changes, shifting rapid ly from one state to another. Such 'regime
shifts' may be due to impacts of climatic change, and have major implications for ecosystem man-
agement.

Further Reading
Longhurst (2006) provides an excellent description of the causes and consequences of geographic
variab ility throughout the world 's ocean, Mann and Lazier (2006) give a broad coverage of b iological
responses to physical processes in the ocean, and Miller (2004) provides a broad coverage of 'biological
oceanog raphy' , A useful plankton atlas of the North Atlantic was published in Volume 27 8 of Marine Ecol-
ogy Progress Series (20 0 4 ) , This provides a summary of Continuous Plankton Recorder (CPR) methods,
and describes how this invaluable long-term record has become an important implement in our under-
stand ing of how pelagic ecosystems respond to global change, Steele (2004) provides a brief review
of regime shifts and their defi nition. His article is the first article in a special issue dedicated to regime
shifts. The book Fisheries Acoustics by Simmonds and Maclennan (2005) provides excellent coverage of
the use of sound for sampling aquatic environments, as well as some information on sound production
by marine animals.
• Anonymo us, 20 0 4, Continuous plankton records: plankton atlas of the Nort h Atlantic Ocean (1958-
19 99 ) , Marine Ecology Progress Series 278. Supplement available on line at: http:/ / www.int-res.com/
abstracts/meps/CPRatlas/contenls,htm l
• longhurst, A. R. 2006, Ecological Geography of the Sea (2 nd edn) . Academ ic Press, San Diego,
• Mann, K, H, & l.azler.L R. N, 2006, Dynamics of Marine Ecosystems: Biological-Physical Interactions in
the Oceans (2nd edn) . Blackwell, Oxford,
• Miller, C. 20 0 4, Biological Oceanography, Wiley-Blackwell.
• SlrnrnondsJ. & Maclennan, D, 2005, Fisheries Acoustics, Theory and Practice (2nd edn) . Blackwell,
Oxford ,
• Steele, J. H. 20 04. Reg ime shifts in the ocean: reconciling observations and theory. Progress in Ocean-
ography 60: 13 5-4 1.
 Continental Shelf
Seabed
Chapter Summary
Continental shelves are the most heavily explo ited and uti-
lized areas of the wo rl d 's oceans and support the greatest
level of biological production. The ecology of the shallow
shelf areas is st rongly influenced by phy sical processes
such as w aves, t ides, currents, erosion, and inputs of mate-
rial from the adjacent land mass. These processes generate
a great diversity of ecosystems and habitats at regional
and local scales. The composi tion of the seabed and its
associated biota are a direct reflect ion of the physical pro-
cesses that act upon it and vary from mud sedi ments hon-
8.1 Introduction
The world's continental shelves contribute only 8% of the
global sea-surface. Nevertheless, their shallow nature means
that most of the waters of the continental shelf fall wit hin
the euphotic zone (Chapters 2 and 7) , which coupled wit h
organic and mineral inputs via riverine discharges and strong
physical mixing of the water colu mn and seabed. make
them among the most productive and economically impor-
tant regions of the world's oceans (Costanza et aJ. 1997) . In
regions where the shelf is narrow, nutrients are add itionally
supplied through upwelling of water from the deep sea. The
high productivity found on continental shelves fuels high lev-
els of secondary production (see Chapter 4) , which in turn
underpins major global fisheries (Chapters 2, 7, and 13) .
Primary production in shelf seas fuels 900;0 of the world 's
fisheries landings, consequently future environmental
changes that impact upon primary production are likely to
have major consequences for shelf sea ecosystems and the
goods and services that they provide (Pauly & Christensen
1995).
•
•
eycom bed w ith burrowing crustaceans and worms through
species-impoverished mob ile sands to bedrock encrusted
w ith luxuriant growths of particulate feed ers and algae. The
benthos is a critical link in the transfer of organic material
and nutrients from the w ater col umn above to t he seabed.
The flo w of energy th ro ugh food webs varies considerably
amo ng regi ons, w ith greater web complexi ty at mid to high
latitudes. Systems w it h strong linkages amo ng individ ual
species are prone to troph ic cascades and are mo re sensi-
t ive to the removal of key species lead ing to ecosystem
regime shifts.
The abundant plankto n and fish fauna found in these
waters are a key food resource for populations of top preda-
tors, such as seabirds and marine mammals. In add ition to
their status as hotspots of biological activity, the proximity
to the coastline and shallow n ature of shelf seas means that
they have become the focus of intensive human activities and,
in addition, receive agricultural and industrial contaminants
from terrestrial run-off (Curre nt Focus). Sh ipping, fishing,
exploration for, and extraction of, hydrocarbons, mining of
sed iments and minerals, underwater cable laying, wind farm
and tid al barrage development, offs hore aquaculture and rec-
reation are just some of the major activities that occur and
impact upon the continental shelf-sea environment. The ecol-
ogy of the continental shelf is under ever-increasing levels of
human usage, which has resulted in major changes in ecosys-
tem structure in some localities.
The intensive use of the coastal shelf inevitably increases
the risk of environmental damage from activities such as
over-fishing, eutrophication, mineral extraction, dumping of
waste, and oil spill accidents. The effects of these human
activities may be exacerbated by the additional stress
imposed by the current rapidly changing environmental
conditions, particularly if they act synergistically.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
CURRENT FOCUS: Catchment to
coast-joined up research
It is rare in ecology for marine an d terrestrial scientists
to work together, their boundaries of research are clearly
defined as either essentially dry or wet and salty ! Su ch
compart mental ization has no do ubt arisen due to t he dif-
ferent sampling techniques that are used for these envi-
ronments, an d the chemistry of the marine environment
often means that you cannot si mply apply a t errestrial
technique in an aquatic context (the chemical composi-
ti on of seawater plays havoc w ith some scientific instru-
mentation) . How ever, changi ng g lobal envi ronmental
con dit ions mean that t he impacts of physical processes,
such as rainfall and stor mi ness, are likely to have the
greatest impact in the coastal zone, such that marine sci-
enti sts need to begin to consi der ho w terrestrial catch-
ment processes are likely to affect coastal ecology and
shelf systems in the fut ure.
We kno w from cli mate forecasts that precip itatio n
events are likely to become less or more intens e in d iffer-
ent parts of the world. Rainfall erodes terrestri al sediments
and flushes nutrients and organic material from w ithin a
catchment and ultimate ly transports those components
into rivers and estuaries. This, coupled wi t h increasing
temp eratures altering th e ability of upland bog to retain its
dissolved organ ic carbon, mean that the composition of
run-off is li kely to change the quality of w ater d ischarged
into rivers. The nutrients and organic materials that pass
into rivers are altered by biogeochem ical and microb ial
processes as they pass dow n the system towards the
open sea. The intensity of rainfall w ill affect the rate of
flushing through the system and hence the residence t ime
during w hich nutrients and organic matter can be altered
8.2 Definitions and
environmental features
The contine ntal shelf extends from the extreme low-water
m ark on the shoreline down to a depth of approximately
200 m and is termed neritic (Chapter 7). Th is region
extends beyond the land from between nearly zero up
to 1500 km offs hore out to the shelf break. Beyond this
point the continental shelf slopes down to the abyssal plain
(Chapter 9) . The shelfbreak is an area where biological a nd
geological m aterial from the continental shelf is supplied
to the shelf slope , through a variety of processes suc h as
the death of organ isms or more dramatically via subma-
rine mudslides. Only on extreme low-water spring tides, or
from one form to another, and determi nes the bioavai l-
ability of the materials for phytoplankton, microbes, and
macrofauna.
Land-management pract ices are equally importa nt
determi nants of the content of run-off w it hin a catch-
ment. Plant ing of hed ges, trees, the stocking density of
livestock, and the app lication of ferti lizers and pesticid es,
all have an impact on the q uality of w ater discharged into
estuaries and coastal systems.
In add it ion to these lan dward effects, increasing sto rmi-
ness in coastal w aters w ill increase co astal erosion and
wave stress that is an important source of mortality for
coastal benth ic pop ulati ons. Indeed , it is li kely that the
biomass supported in som e coastal areas w ill decrease
significantly w ith consequences for ecosystem processes
and benthic feed ing predators.
Ultimately, the quality of material that emerges from the
mouth of this estuary into the adjacent coast is deter-
mined by the land-management practices that affect
the surrounding catchment and the regime of rainfall
and erosion pattern s that impact upon it (photograph:
Manfred Heyde).
in the strandline wreckage in the upper shore that occurs
after an onshore storm, are we able to observe unaided
some of the organisms that live at the shallowest edge of
the contine ntal shelf. Generally the continental slope h as
a shallow gradient of ap proximately 1 0 except in regions
where glacial activity has sculpted a more dramatic seabed.
The shallow depth of the continental shelf and its position
adjacent to the physical barrier of the land m ass mean that
it is strongly influenced by physical forcing processes,
suc h as glaciation events, currents, waves, the formation
of fronts and water turbidity (Fig. 8.1). The interaction of
these processes is influenced by shelf width and geographic
disposition and is strongly re lated to consistent patterns in
regional ecosystem structure .
 8.2 Definitions and environmental features
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Physical processes perform a key role in the conti-
nental shelf environment due to its proximity to land,
inputs of fresh water, seabed topography, and shallow
depth.
8.2.1 Influence of glaciation events
The physical and biological characteristics of the continen-
tal shelf habitat are strongly influenced by the geological
composition of the seabed, much of which has resulted
from past glacial events that have had a profound influence
on coastal margins and shallow near-shore seabed structure
(Fig. 8.2) . The melting and formation of ice sheets causes
the sea-level to rise and fall respectively, while the Earth's
crust is lowered underthe weight ofice, butrebounds (rises)
in its absence (Box 8.1) . Thus areas hundreds of kilometres
offshore may have been dry land at some point in recent
geological history. This is reflected in the surface topogra-
phy of the seabed where it still possible to see drowned river
deltas (e.g, off the River Congo in Africa) , while evidence of
hominid butchery of large mammal bones has been found
Sediment/land
Estuarine
sediments Sea bed
1. River
(aaslal zane 2. Estuary
[ 3. (aastal baundary layer
4.Shelf praper
S. Shelf break
Figure 8.1 Key processes that influence the continental shelf environment (adapted from Alongi 1998). POM =
Particulate organic matter, DIN:;; Dissolved inorganic nitrogen, DOM ::;: Dissolved organic matter.
to the west of Florida in the GulfofMexico at a present-day
depth of 4D m below sea-level. Glacial deposits characterize
much of the continental shelf bed in the higher latitudes
and are typified by fields of boulders and gravel beds.
The continental shelf is relatively young in geologi-
cal terms and has undergone dramatic expansion and
contraction as a result of glaciation events. Evidence
for these events can be seen vividly on the seabed as
drowned river plumes, boulder fields, and glacial scour-
ing. See Fig. 8.2 and Box 8.1.
8.2.2 Importance of waves and flow
The physical effects ofwave5 have important consequences
for the ecology of the shallower areas of the shelf (Emer-
son 1989), and their effects reach down to a depth of 80
m on open Atlantic coasts during gale-force conditions
(Chapter 6) . Clearly, the depth to which waves influence
benthic ecology will depend on the extent to which the
coastline is sheltered from prevailing winds and the extent
of fetch (Hiscock 1983). In areas where the physical force
Gases
4
Heat
, ,
II S
,
~~ ,~0,, /
,
,
Slape sedimenls
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

•
+

o 05 I
~i1 om"tr'"

Figure 8 .2 This multibeam-derived image of the seabed to the north of Anglesey, Irish Sea, shows the dramatic impact
of past glacial events o n the sea bed . Submarine drumlins are clearly visible in this image, shown as a series of rounded
mounds and pits. Such a clear image is unusual as the pits are normally filled in with deposits of fine sediment; however,
the strong tidal cur rent s in this area have prevented sediment infilling (image courtesy of Katrien Van Landeghem).

of waves causes sediment movement, wave action can be a
m ajor cause of m ortality among be nth ic animals and has
been shown to affect secondary production by limiting the
body size of organisms that can survive in a highly energetic
environment (Emerson 1989). Water movement generates
curre nts and these affect both the shallow and deeper parts
of the shelf. The phenomenon of flow is extremely impor-
tant for the ecology of the contine ntal shelf. as it affects the
passive and active transport of organ isms. their gametes.
and larvae (Techn iques box), and the rate of supply of food
from the pelagic system to the seabed , and places upper
physical constraints on the type of organ isms that live in
particular h abitats. Thus close to the shoreline. the seabed
is affected most strongly by bot h waves and currents. as
we move further offs hore the effects of waves reduce and
the effects of curre nts begin to dominate the physical and
biological processes on the seabed . This grad ient is clearly
reflected in the biomass of sessile filter and deposit feed-
ing biota. which increase wit h distance away from shallow
into deeper water where the physical stress associated with
waves and curre nts decreases and the seabed is therefore
less frequently subjected to physical disturbance.

TECHNIQUES:Where do all the larvae
go?
Tidally driven currents are essential for the dispersal of
the larvae of many organisms. Rel at ive to the speed of
surface currents, most larv ae are capable of only small
movements (a few body lengths per second compared
with flow speeds typically of >0.5 rn s'"). Larval behav-
iour in response to envi ronmental cues, such as light and
salinity, can induce vertical mig rat ion in the water column,
hence dispersal speed is altered as the larv ae move away
from, or tow ards, the surface (the speed of flow is high-
est at the surface and lowest close to the seabe d-an d
negligible at the boundary layer). In t he fig ure, we show
the output of a particle-tracking mod el t hat w as used to
understand the likely dispersal pattern of scallop larv ae
spawned within an area closed to scallop-fishing activities.
Understanding the orig in and end point of scallop larval
dispersal helps us to understand how we might design
a netwo rk of protected areas th at would increase the
sustainabil ity of the scallop popul at ion (see also Online
Resou rce Centre for a video simulation) .
 8.2 Definitions and environmental features

The output of a larval-dispersal model

for scallop released from Douglas Bay
(D), Isle of Man . The darker red the
areas, the higher the probability of lar-
vae arriving in that area of the sea after
3 weeks of drifting in the plankton (the
typical period required for develop-
ment prior to settlement to the sea-
bed). Image courtesy of Simon Neill.

Box 8.1: Rise and fall of the continental
shelf edge
The coastal margins of the State of Maine (USA) have
left clear evi dence of the rise and fall of coastal margins
in respon se to glacial events. Land -level alte red substan-
tially 14 000- 10000 years ago during the last glaciation
event. After thi s pe ri o d, global sea-level changes have
had a major influence on the coastal landscape. About
14 000 years ago global (eu st at ic) sea-level w as about
11 0m below its present level. However, the wei ght of
local ice-sheets that were over 1 km thick depressed the

lal 0
•> Maine shoreli ne Offshore
.e 40
--•
c

c Holotene shoreline \
--•
~

0
50 Helerene with lome glooomorine

-••
~

c
60
-a
--
~

E
70
~

Q
-•
~
80

Ibl Terrestriol Glociomarine

Ice sheet Retreating ftesheet
melt wafe r
,..,. Sea level
rIS ing
-
deposits deposits
Sea level

Seo level

(a) Reflect ion of sound waves from the seabed strata at a depth of cAD m offshore of Maine USA shows the suc-
cessive deposition of glaciomarine material during various glaciation events. (b) A schematic image to show the
various stages of vertical movement of the continental shelf in relation to glacial retreat and changes in sea-level.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

level of the Earth's crust, which meant that relative sea-
level was 70 m above that of the present day. Eustatic
sea-level was relatively low, but rising as the ice sheets
began to melt. Ultimately, the re lease of the weight of the
ice allowed rebound of the land to outpac e the rate of
the rising global ocean. Thus, local relative sea-level fell
(as the land rose), until it reached 55 m below the pres-
ent sea-level about 11 000 years ago. This caused the
coastline to move well offshore of the present coast. Thus
withi n the space of 4000 years the coastal margi n varied
by as much as 12 5 m, with a coastline that expanded or
contracted by te ns to hundreds of kilometres depending
on the slope of the local continental shelf and coastal
margin (the shallower the slope the greater the incu rsion
or excurs ion by the sea).

Fetch is the uninterrupted distance over which winds
exert friction at the sea surface.
The ecological importance of wave action diminishes
with reducing fetch and distance from the shore as water
depth increases.
Animals that are either attached to a substratum or that
move relatively little or infrequently are termed sessile.
The rising and falling water mass has important implica -
tions for organ isms that live on the shore (Chapter 6) . An
equally important result of this oscillation is the flow or cur-
rent that is generated as the water floods into, or ebbs from,
restricted areas of coastl ine. Current is incre ased w hen a
wate r m ass m oves through, or around , land-bounded
restrictions or across ir regularities in the seabed topogra-
phy. Typically, stra its and the narrow mouths of estuaries
have some of the strongest tidal flows, reaching speeds of
up to several metres per second . Headlands and bedro ck
protrusions from the seabed also present restrictions to the
flow of wate r and lead to stro ng cur rents around their apex
(Fig. 8.3; see also Online Resource Centre video simulation
associated with the Techniques box) .
As water m oves over the seabed, the uneven se abed
induces friction, which slows the immediate wate r column
above, so seabed currents are rarely as fast as sea-s urface
currents (except in areas of the deep sea ). Currents and the
associated bottom shear stress, influence food availabil-

West East
o 2 4 6 8

Figure 8 .3 Current velocity

generated through the tidal rise
and fait of water in a sea basin is
exacerbated dose to the coast,
where coastal morpholog y and
restrictions increase the speed of
flow. This can be seen dearly for
the example of the northwestern
European shelf above, with strong
mean surface velocities in the 1"o 54
z
English Channel , the southern
North Sea, and the George's
Channel. Current velocities are also
increased around headlands, such
as off the North of Scotland and
around the coast of Brittany and
Velocity keyemf l
Normandy on the coast of France.
- - - Over75
The darker the blue lines, the higher
- - 25· 75
the current velocity. Adapted from Under 25
Metcalfe et al. 2002 .
 8.2 Definitions and environmental features
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
ity for benthic communities (Jenness & Duineveld 1985)
and benthic secondary production (Warwick & Uncles
1980; Wildish & Peer 1983). High levels of shear stress
cause scouring of the seabed and its biota, while high cur-
rent velocities inhibit effective feeding activity. Biota that
live in such environments tend to have characteristics or
behaviours that enable them to cope with the extremes of
physical stress. Typically, attached biota are highly flexible
or encrusting, while mobile fauna will often seek shelter
from currents within the sediment or in crevice habitats. At
the other extreme. areas with reduced water movement at
the seabed will not replenish the supply of food to the sea-
bed, which then becomes a limiting factor for the growth of
benthos. At a certain current velocity threshold, food par-
ticles transported from other areas will begin to sink to the
seabed, where they become available as food to the benthos
(Creutzberg 1984; Widdows et al. 2010) . The exact figure
for the current velocity threshold will depend upon particle
size and buoyancy. The latest research highlights how flow
is strongly related to the rate of passive exchange of nutri-
ents and oxygen between the top few millimetres of the
sediment surface and the overlying water. A reduction in
flow reduces the diversity ofthe surface sediment microbial
assemblage, which in tum alters the physical properties of
the sediment. Different microbes produce different types of
extracellular products that coat sediment grains and hence
affect properties such as shear (Biles et al. 2003) .
Flow velocity influences the rate of supply and resus-
pension of particulate matter to and from the seabed,
is linked to the rate of nutrient exchange at the sed i-
ment-water interface, and places upper constraints on
the body size of biota that can live in a particular habitat.
8.2 .3 Fronts and production
The development of fronts has important ecological impli-
cations in areas where water becomes stratified (Chapter
7) . During winter periods. the water column of the con-
tinental shelf is held in a well-mixed state by high winds
and wave action. This means that dissolved oxygen, carbon
dioxide, and nutrients are relatively evenly distributed from
the sea surface to the seabed. The water column remains
well ntixed throughout the year in areas where the seabed
currents are strong and cause turbulent mixing. typically
close to the coast in shallow water. In offshore waters and
areas not strongly influenced by tidal mixing. periods of
prolonged warm temperatures and calm conditions lead to
stratification. This results in thermal depletion ofoxygen at
the seabed and nutrients in the surface layers of the water
column. Frontal systems occur at a point where a stratified
and mixed body of water meet. The resulting density gra-
dient between the two bodies ofwater means that a flux of
nutrients occurs from the mixed water mass to the nutrient-
depleted upper stratified waters of the adjacentwater mass.
This fuels primary production to a level higher than in the
surrounding waters (Chapter 7) .
As full salinity seawater approaches the coastline. it
interacts with lower salinity water discharged as an estu-
arine plume. The difference in density between the two
bodies of water sets up a frontal system due to the density
gradient between the two bodies of water (the less dense
estuarine water is more buoyant than full salinity seawater)
and may deflect the estuarine water along the coastline in
one direction due to the Coriolis force (Chapter 7) . Agood
example of such a plume is the discharge from the River
Rhine in the North Sea, which flows northwards along the
Dutch coastline . These areas have become termed regions
of freshwater influence or ROFIs .
Elevated production of phytoplankton at fronts attracts
both fish and their predators, such as seabirds and
marine mammals, and results in a greater supply of
organic matter to the benthic fauna.
The elevated primary production at fronts fuels produc-
tion in the benthos and in pelagic and demersal fisheries.
As a result. fronts are often the foci of fisheries' activities
but also attract piscivorous and planktivorous seabirds
and sea mammals, and there is evidence to suggest that
fronts may be associated with above-average by-catches of
marine mammals. such as the harbour porpoise (Phocoena
phocoenu) (McGlade & Metuzals 2000; Trites et al. 2007) .
8.2.4 Light and turbidity
Water depth and turbidity are important determinants
of the distribution of benthic algae in the shallow waters
close to the coast. Areas of the seabed affected by estua-
rine plumes are generally severely light-limited due to the
associated high load of suspended sediment and phyto-
detritus, which attenuates light in the first few metres
of the water column (Chapter 2) . Thus these areas of the
seabed tend to be dominated by animals, and any algae
are restricted to the very shallowest water adjacent to the
shore. In contrast. coastal areas that are typically open to
the ocean. and have limited riverine discharge. have much
clearer waters and here a full range of algae can be found
with clear zonation from the shallow to the deeper water
ofgreen (shallow), brown, and then red (deep) algal domi-
nance. In these situations algae can be dominant in terms of
their biomass. The width of the algal-dominated zone will
depend on water clarity and slope of the seabed (the clearer
the water and lower the slope the greater the area of seabed
that will be suitable for algal growth) .
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Algae are restricted to a narrow zone of near-shore shal-
low waters in regions where major riverine discharge and
near-bed tidal resuspension of sediments increase the
turbidity of the water column.
8.2.5 Regional ecosystem types
Basin-scale oceanographic processes va ry with shelf seabed
and coastal morphology (Warwick & Uncles 1980). These
characteristics vary on a regional basis and are the primary
determinants of regional shelf ecosystems. In the absence
of the effects of fisheries, pollution, or the flux of ant hro-
pogenic materials, a relatively small number of physical
factors regulate vegetation types or phytoplankton biomes
th at are modified by basin -scale circulat ion patterns and
coastal morphology (above). The close coupling between
physical processes and the biology of shelf seas enables
them to be partitioned into broad regional ecosystem types,
which Longhurst (1995) attributed to seven model systems.
These systems are presented in Table 8.1 and show the link
between regional physical processes, primary production ,
and then the linkages to other compartments in continental
shelf ecosystems (Chapters 1 and 7) . While each of t he eco-
systems with in each model displays diffe rences in species
composition, there is a high degree of similarity among the
ecosystems at higher levels of organization (e.g. primary
producers, secondary production processes, top predators) .
In the absence of human intervention through fishing ,
pollution, or other forms of ecological disturbance,
continental shelf ecosystems can be categorized under
seven models according to the dominant physical pro-
cesses and shared ecological features at higher levels
of organization. Human intervention can lead to entire
regime shifts within these systems in which the species'
composition is maintained but the relative dominance of
each species changes.
8.3 The seabed habitat and
biota
While it may be tempting to consider the continental shelf
seabed habitat as rather two-dimens ional compared to the
pelagic habitat above (Chapter 7) , it is very much a t hree-
dime ns ional habitat, even though the third d imension,
depth, is much more compressed than in pelagic systems.
While in pelagic systems the depth dimens ion can exceed
several thousands of metres in which biota can be found
from the water's surface to just above the seabed of the deep
sea. The seabed hab itat is bounded by the depth to which
biota can burrow and continue to live (usually no more than
2 m within the sed iment) and the extent to which they pen-
etrate into the waters above (30 to SO m for some of the
largest kelp genera such as Macrocystis) (Fig. 8.4) . In some
cases the biota are the key constituent of the habitat, as in
kelp forests, mussel and oyster reefs, m aerl beds, corals,
and sponges. We will deal with specific examples of these
habitats later in the chapter (8.7) .

Table 8 .1 Seven models of co nt inental s helf ecosystems giving th eir geographic locality, the principal primary
and seco ndary production processes and ot he r key co mpo ne nts and cha racte rist ics at higher trophic levels
(adapted from Longhurst 1995).

Model Geographic location Primary and secondary production Higher trophic levels

Model 1 Eastern Siberian and Laptev Productivity is light-limited, with seasonal cycle Benthic invertebrates are
Polar Sea coasts of Siberia. symmetrical about local irradiance max imum . abun dant and diverse
irradiance- Northeastern and Northern Latter corresponds with solar max imum or providing food fo r
mediated coasts of Greenland . min imal snow cover. abun dant but low-d iversity
production Below ice, phytoplankton productivity and populations of fish and
Northern coasts of Canadian
peak in zooplankton b iomass are low, but abundant squid. Large euphausiids
archipelago to west Beaufort
regions flora in the infiltration zone at th e ice-seawater (krill) , characteristic of
Sea.
permanently matrix . Underside of ice < 2 m thick may open-water regions, are
Almost entire coast of replaced by small Euphausia
ice -covered support de nse growth of d iatoms associated
Antarctica . crystallophorias and provide
w ith abun dant po lychaetes, copepods, and
amphipods. food for pelagic fish
(Pleurogramma spp.) and
crab-eater seals.
 8.3 The seabed habitat and biota

Model Geographic location Primary and secondary production Higher trophic levels

Model 2 Coasts of Greenland . Shallow po lar halocline induces water column Production exceeds
Polar North America from stability very early in open-water. consum ption in the water
irradiance- Newfoundland to th e Productivity is light limited , its seasonal cycle column and supports rich
mediated Aleutians. being symmetrical about th e local irradiance and d iver se macrobenthos,
production maximum. Where pack-ice remains, con ditions esp ecially in boreal regions,
Northern Asia from Finland where shelf areas uncovered
peak in to the Sea of Okhotsk. may resemble Mod el l .
regions where by ice are much more
Short sectors of Antarctic After ice -melt, in open water, phytoplankton exte nsive than around
Ice-cover accumulates during th e period wh en p roductivity
coast in midsummer in Antarctica. Low-diversity
dis perses inc reases, and then tracks its initial de cline.
partially or
eastern Ross Sea, to east of fish fauna, especially in
Ronne ice shelf and in Phytoplankton is dominated by d iatoms, a
completely in th e Antarctic, where small
Dumont d 'Urvilie Sea. subsurface chlorophyll maximum is often
summer, or Nototh enids dominate .
observed; in shoal water, significant b iomass of
only wh ere The w ider Arctic shelves
benthic macroalgae develop.
broken pac k- support a greater diversity of
Planktonic herbivores are represented by Gad idae,
ice develops.
abundant large co pepods, euphausiid s and Sebastldae, Anamlcbos sp p.
salps, of which some species form swarms that Grey whale, wal rus, and
suppo rt major stocks of baleen whales and bearded seal are boreal
seals. be nthic feed ers, having no
austral equivalents.
•• • •••• •••• • ••• ••• • •••••• •••••• •••••• •••••• •••••• ••••• • ••• • •• ••• ••••••• ••• ••• ••••••• ••• • •• ••• ••• ••••••• ••• •• • •• • • • •• • • • • • • • • • •• • • • • • • • • • • • •• • • • •• • • •
Mod el 3 On mid-latitude continental After w inter mixing, a p ulse of productivity and Most autotrophic production
Canonical shelves, under th e influence chlorophyll is induced by estab lishme nt of water passes directly or indirectly
spring-autumn of the global westerly w inds. column stability. Thereafter summer stratification th rough th e macrobenthos,
blo oms of From Finland to Iberia and is associated with relatively low productivity. which is abundant, diver se,
mid-latitude off the Mediterranean. Prog ressive mixing in autumn may induce and characteristic of each
continental From Newfoundland to renewed productivity fuell ed by nutri ents sediment type.
shelves Florida. Off Tasmania and accumulated below the summer pycnocline . Diversity of fi sh fauna
south ern Australia. This sequence is modifi ed by intermittent wind- exceeds that in polar
induced coastal convergence and d ive rge nce, ecosystems (typically 200
and persiste nt water column mixing in regions species of >50 families). In
wh ere tidal velociti es excee d critical valu e. boreal regions, major stocks
Effects of est uarine tu rbi dity p lume s may of shoaling Clupeldae and
mask th e canonical sequence, which weakens Scom bridae together with
towards th e equator. The balance between mainly de mersal Gad idae,
pico-autotrophs and larger algal cells is more Percidae, and Pleuron ecti dae.
equitab le than in very high latitud es. In shoal In much more restricted
water, esp ecially at high er latitud es (Norway, austral shelf regions,
Iceland, Newfoundlan d, Tasmania) th ere is dupelds occur as in th e
significant autotrophic p roduction in kelp north, together with a
beds. Small co pepods d ominate the inshore more-difficult-to-specify
herbivorous plan kton, larger species nearer th e demersal fauna. Energy flow
shelf ed ge, often over-wintering in deep water. from pelagic invertebrates
Their seasonal cycle of abundance follows that is mainly to dupeids and
of phytoplankton. scombrids, from be nthos
mainly to demersal fis h
fauna.
• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •
Mod el 4 Falklands shelf, the southern The seasonal productivity sch ed ule, otherwise In many respects th e
Topoqraphy- North Sea, th e shelf of appropriate to Model 3, is instead forced by heterotroph ic b iota, and
fo rced th e Gulf of Alaska wh ere oth er factors (see adjacent column), d iffering energy flows, are broadly
summer tidal mixing consistently regionally. Consequently, p hytoplankton similar to those appropriate
production d ominates the stability of productivity tends to peak in mid-summer rather to Mo del 3 eco systems.
th e water mass, temperate than in spring.
North Pacific where the In many respects the autotrophic biota, and
oceanic permanent halocline ene rgy flows, are broadly similar to those
passes inshore across the ap propriate to Model 3 ecosystems.
shelf, so constrain ing w inter
mixing to water above th e
pycnocline. New Zealand
and sim ilar locations
wh ere, topographically-
forced upwell ing sites in
shallow water dominate th e
productivity sequence.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Model Geographic location Primary and secondary production Higher trophic levels

Model 5 The Atlant ic from Iberia These are th e 'classical ' coastal upwelling Bent hic consumers are
Intermittent to Senegal and Gabon to regions of easte rn boundary current and oth er abundant, but not d iverse,
production Benguela. coasts, som e of which occur at relatively low and there is much physical
at coastal The Pacific from Oregon to latitudes. The shelf is characteristically narrow, exp or t of organic material
d ive rgences. Mexico and Peru to southern and th e influence of river effluents minor. into deep basins on th e shelf
Chile. The Indian Ocean from The equator-wa rd com ponent of the Trade or across th e shelf ed ge into
Oman to Kenya. winds induces strong and persistent offshore deep water. Along th e shelf
Ekman drift, inducing upwelling of nutrient-rich edge, deep -water rockfish
deep water. This p rocess is usually strongest (Sebastes) are abundant,
during summ er. Similarly, in th e Ind ian Ocean characteristic, and diverse.
th e South-west Monsoon forces offshore drift, Anchovies (Engraulis,
principally off Somalia. Cetengraulis) are ubiquitous
Upwelling results in a rap id increase in primary vertebrate herbivores,
production of phytoplankton, principally d iatoms, w ith in addition, sardines
and chlorophyll accumulation coincides with th e (Sardinella longiceps) in th e
durat ion of upwell ing periods. Indian Ocean. Populations
of predators, mostly
The biota have low divers ity and high coll ective
pe lagic c1upeids (Sardina ,
biomass. Special ized invertebrate herbivores
Sardinops) , mackerel
are large calanoi d copepods (typically Ca/anus
(Scomber) , hake (f'v1erluccius,
or Calanoides) , euphausiids and filter-feeding f'v1icromesistius) , sealions,
anomuran crabs, each having life history tactics and piscivorous seabirds
that take th em into deep water, or th e shallow are characteristic of th ese
sea-floor, during non-upwelling periods. Kelp regions.
forests reach th eir maximum development and
generate significant autotroph ic product ion
and accumulation of biomass. There is heavy,
intermittent settlement of large p hytoplankton
cells and faecal material to th e sediments,
frequently resulting in an oxygen deficit at
certain depths on the narrow shelves.
............. .................... ...... ...... ... ... ...................... ............. ................ ............. ........ ........ ..................
Model 6 Amazon, Niger, Congo, Indus, Trad e wind regimes force only weak seasonality Bent hic community ty pes
Small Ganges, Ir rawaddy, Mekong, in mix ed layer depth, observed minor changes conform to sediment types,
amplitude and oth ers. These are wet represent the geostrophic resp onse of the and wh ere th ese resemble
response to tropical coasts, d ominated by pycnocline to seasonality in trade wind stress those of cool er seas,
trade wind th e effluent of a few major rath er than mi xing. The basin-wide slope of the members of the global
seasonality in rivers or many smaller river th ermocline has important consequ ences in th e suite of benthic infaunal
regions with systems. Pacific and Atlantic Oceans; to th e west it lies communities occur (e.g.
sign ificant In th e Atlantic, th e Gulf deeper than th e shelfedge, but in th e east it is at clams such as Venus) .
coastal river of Guinea, the Guianas, mid-shelf level. In the east , therefo re, the benthic Inshore, orqanic-rich
d ischarge s and north ern Brazil. In regime has typical tropical character shorewards sediments may be exte nsive
which th e easte rn Pacific, from of this line, but more temperate characteristics and support stocks of
d ominate Columbia to southern in cool water seawards. On easte rn Atlant ic and crustacea dominated by
over oceanic Mexico. In the Indo-Pacific, Pacific coasts, th e nutrient cline is perennially pe naeid shrim ps. These
processes from the South China Sea shallower than th e phot ic depth, except during sediments are prone to
that would to south-western India, excep tional events, and vertically-inteqrated resuspension by wave action
otherwise including much of th e production rate is not normally liq ht-Hrnited . In monsoon seasons.
dete rmine Indonesian Archipelago Everywh ere, river d ischarges into th e low-salinity
surface layer have strong seasonality, reflecting Fish fauna is diverse at
seasonal and th e northern coast of all taxonomic levels and
changes. Aust ralia. regim es of wet and dry seasons, so that th e
seasonal sch edule of p rimary product ion rate includ es a higher p ropor ti on
is govern ed by nutrient input from th e land and of pelagic sp ecies than in
possibly reduced irradiance due to p rolonged Mod els 3 and 4 at highe r
latitudes.
heavy cloud cover during wet seasons.
Autotrop hic organisms are ty pically small cells,
excep t in coastal b looms fu elled by river-borne
nitrate, which are dominated by Coscinodiscus
and oth er diatoms. The b iomass of coastal
subtidal macroalgae is not significant due to
water turbidity. Consumers are numerically
d ominated by small copepods, but diatom
blooms support large stocks of herbivorous
c1upeids (Atlantic-Ethma/osa, Brevoortia; Ind o-
Pacific- Sardinella /ongiceps). A large p roportion
of d iatom material sinks to the seab ed.
 8.3 The seabed habitat and biota

Model Geographic location Primary and secondary production Higher trophic levels

Model 7 In th e Atlantic, only th e Ecosystem of shallow seas off th e coasts The macrobenthos
Small Caribbean. In th e Indo-Pacific of the dry tropics, wh ere river efflue nts are asso ciated with coral ree f
amplitude parts of the Arabian Sea, the minimal. Many isolated islands and archipelagos fo rmations is exceptionally
res ponse to Red Sea, north-east Australia , in tropical seas are surround ed by reduced diverse at all taxonomic
trade w ind and of the Indonesian Mod el 7 ecosy ste ms, of which th e dominant levels.
seasonality archi pelago. characteristic is th e d evelopment of coral On open sandy sediments,
in regions off reefs where topography pe rmits, elsew here unencumbered with reefs,
dry coasts unconsolidated sediments are dom inated by very high densities of filter-
with relatively carbonate sand. feeding crabs (Pinnixa,
. .
rnmor river There is w eak seasonality in mixed layer dept h, Xenophthalmus ) are
discharges. and nutrient clin e is usually shallower than th e typical, together with oth er
photic depth, except during excep t ional events. organ isms, especially filter-
Most p rimary production occurs in the benthos. feeding clams.
Macroalgae (Sargassum) , encrust ing coralline Fish fauna is also diverse,
green (Halimedia) and red algae, cyanophyte both taxonomically and
mats and sea-grass meadows dominate functionally.
community p roduct ion, in addition to th e activity Parrot-fish (Scaridae) are
of symbiotic dinoflagellate s within th e tissues of among th e most important
many invertebrates: scleractlnian corals, giant herbivores, directly
clams (Tridacna), co elenterates (alcyon ians, consum ing coralline and
anthozoans, and scyphozoans), large ascidians oth er algal mats, and these
and encr ust ing sponges. may fo rm a large-fraction of
Nutrient sources and fluxes are various: total fish b iomass.
advection, upwelling, vertical flux in fractured An intense and complex
basement rocks, some terrestrial runoff. network of trophic links
Nitrogen-fi xing bacteria occur in the tissu es betwee n fish and benthic
of some corals, and cyanobacteria fix nitrogen invertebrates is characteristic
w ithin algal mats. Internal exchange s of of this ecosyste m. This
nutrients within and between organisms is highly trophic complex supports
compl ex. Export from th e benthic ecosyste m, a w ide variety of large
exc ept in th e form of carbonate ero ded to sand predators.
and gravel factions, is a small but complex flux.
Water clarity is high, and p hytoplankton is
d ominated by th e plco- and nano-fractions, as
in oligotrophic ocean ecosyste ms. These are
consumed by protists and small zooplankters
th emselves th e p rey of many filter- and
tentacular-feedinq polyps of corals and oth er
co elenterates.

Body size affects bot h production processes and the
degree to which biota are associated with particular h abi-
tats (see also Chapter 4). The body size of animals living in
the seabed is affected by burrowing ability and constraints
on respiration due to oxygen exchange. The body size of
attached biota that inhabit the surface of the seabed are
constrained by physical processes, suc h as shear due to
curre nt velocity. The degree of mobility of the biota (i.e.
their life mode) varies from those organisms that are firml y
cemented to a substratum, to anemones that are able to
reposition themselves by a few mm per day, to highly mobile
crabs and fishes that migrate tens or hundreds of kilometres
every year. The mobility of the biota affects their ability to
respond to environmental change and places a constraint
on the extent and range of habitat that can be utilized.
8.3.1 Body size and position
The m ajor groupings of an imals based on body size are
macrofauna, meiofauna, and the microbiota. The meio-
fauna are usually de fined as those organisms that would
pass through a sieve with a mesh diameter of 0.5 mm but
that would be retained on a mesh of 0 .063 mm. The meio-
fauna are the least well-stud ied, yet probably the m ost
diverse, group of m arine organ isms that can be observed
directly using light microscopy (Lambshead et al. 200 1).
Anything larger than this is termed the m acrofauna. The
small body size of meiofauna means that their rates of pro-
duction (how much biomass is gene rated wit hin a given
time ) is much higher than for the larger m acrofauna.
Accordingly, meiofaunal population responses to environ-
mental and human disturbances can occur within days and
weeks , which make them excellent indicators of environ-
mental stress (e .g. pollution, physical disturbance). Most
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

(bJ (II

Figure 8.4 The three-dimensional extent of the seabed habitat will vary considerably depending on the hardness and
stability of the seabed. Rocky substrata provide a firm and stable anchorage for many animals and plants such as kelp,
soft corals, and sponges. The stability of this substratum means that often these animals are able to attain much larger
body sizes than similar or the same species found in less stable habitats (a). Very few organisms can penetrate bedrock.
Substrata that are composed of particles can vary considerably in stability from bedrock to fine muds and clays. Even
the largest and heaviest particles can become mobile in certain sea conditions. Boulders provide interstitial spaces
that act as refugia and provide a firm anchorage for epibiota. As particle size decreases, so the ability of animals to
penetrate into the sediment increases until in the softest sediments it is limited only by the depth to which oxygenated
water can be circulated into burrow systems. On mixed sediments (gravely shelly sands) the upper size of epibiota is
constrained by near-bed currents (animals that grow too big will be sheared off the seabed) leading to adaptations such
as a flattened body form (b). However, softer sediments like mud tend to have a less diverse array of emergent epibiota
and are usually limited to soft bodied animals like anemones and sea pens (c).

research has been devoted to the study of macrofauna due
to their amenability to experimental and observational
studies. Nevertheless, the contribution of the microbiota
(dinoflagellates, diatoms, bacteria) to biomass and pro-
duction in coastal seas is often under-represented, and in
the tropics can considerably exceed that of meiofauna and
macrofauna combined (Fig. 8.5; see also Chapter 3) . Body
size and longevity is also an important determinant of the
rate of recovery after a disturbance has occurred. Small ani-
mals recolonize areas of disturbance via larval recruitment
on a scale of days or weeks, whereas increasingly larger or
slow-growing biota can take many months or years to recol-
the substratum. In some cases calcareous algae form their
own unique biogenic habitat, these maerl beds harbour
a high diversity of biota due to their complex structure.
Infaunal organisms live buried within the substratum,
either entirely (such as free-burrowing polychaete worms
and heart urchins) or partially. Examples of partially bur-
ied infauna include burrowing shrimps, which build gal-
7
-• 6
5
-=-
~

c
e
4
3
onize and attain their former biomass. The most extreme ••
= 2
1
example of the latter would be slow-growing deep-water
0
corals found on the continental slope edge or on seamounts Bacteria Meiafou na Macrainfauna Epifouna
(Chapter 9) or maerl (calcareous algae) beds (Hall-Spencer -=~ 50
40
& Moore 2000) .
•
Despite th eir cont ribution t o benthic production and
-=
.... 30
c
'6 20
=
diversity, meiofauna and the microbiota are the least
well-stud ied size-classes of marine biota.
~

~
c
- 10
0
Bacteria Meiafou na Macrainfauna Epifouna

The biota can be categorized according to their relative

position within or on the seabed. Epibiota are those emer-
gent organisms that are anchored in or upon the substra-
tum (e .g, corals, anemones, hydroids) or those free-living
organisms that move about on the surface of the substra-
tum (e .g, gastropods, starfish, crabs, fishes) . Macroalgae
are almost exclusively epibenthic and grow attached to
Figure 8.5 Estimates of mean biomass and production
of different size classes of benthic biota in the Gulf of
Papua, northern Coral Sea (Alongi, D. M. & Robertson, A.
I. 1995. Factors regulating benthic food chains in tropical
river deltas and adjacent shelf areas. Geo-Marine Letters
15: 14~ 152. Copyright Elsevier 1995.)
 8.3 The seabed habitat and biota

leries within the substratum but emerge periodically to
forage for food or mates, or burrowing sea cucumbers that
live within the sediment and extend feeding tentacles onto
the sediment surface . In very shallow subtidal areas with
good illumination at the seabed, unicellular diatoms and
dinoflagellates contribute to the microbial community,
and along with cyanobacte ria and bacteria, inhabit the
interstitial spaces between sedime nt particles (Paterson &
Black 199 9 ) (Box 8.2).
The microbiota have an important influence on the cohe-
sive properties of the sediment through the production of
extracellular organic secretions that modify flow and other
important ecosystem functions such as nutrient exchange.

Box 8.2: Current flow over the seabed

Smooth turbulent flow Rough turbulent flo w

Freestream

logarithmic No laminar
layer sub-layer

lam inar sub-layer Mussels lmreese turbulent

flowbuyincreasingsurface
Microbial infillin g topographicrelief

Cohesive Non-cohesive Hydrodynamicallyrough

The fi gure shows the impact that microb ial organisms can
have on flow over the seabed by inf illing the gaps between
sedim ent part icles to create a 'smoother' surface. A rough
bed w ill experience greater stress for the same overall
flow than a smoot h bed. This has important consequ ences
for plants and animals living at the sed iment surface. Under
rough , t urbulent conditions, turbulent eddies are formed
th at impact the bed and increase the likelihood of erosion
of the sed iment and resid ent bi ota. Under such condi-
t ions it is not possible for t he viscous laminar sub-layer
to form. This is someti mes termed the boundary layer,
wh ich acts as a hydrodynamic and molecu lar buffer zone
between the bed and the flow above. When th is layer is
present it significantly affects the flow of part icles and
nutrients to and from the bed. The bi ological significance
of the physics becomes clearer w hen we consi der the
cons equ ence of animal growth on the seabe d. Mussels
settlin g onto a smooth substratum will increase t he sur-
face complexity of the bed making it 'rou gher'. This in tu rn
will increase turbulent flow over the seabed. The t urbulent
flow breaks down the boundary layer and encourages a
downward transport of phytoplankton from the layers of
water above, encou raging further growth and an increase
in the rough ness of the bed. Paterso n, D. A. & Black, K.
19 99 . Advances in Ecologicol Research, 29: 15 5-1 9 3 .
Copyright © Elsevier 19 9 9 .

2
The image represents the chloro-
--
E 6 3 l=
phyll a (food for mussels and
~
~
=L other filter-feeders) profile in a
0

-
~

•
0

---
0
~

~
4 0 body of water followed across a
> 0
0 ~
mussel bed over a 1.5-h period .
--•
~
0

~ 3 Phytoplankton depleted bymusselfiltration withtime 5 -

0
0
Within 1.5 h nearly a third of
--
0 0

'15 ~ the plankton was removed from

-
~
~
6 0
~
~
~
0 the entire water column. Water
Q ~

height rises from 11.00 to 12.30

0 7
11.00 12.30 with the incoming tide. (Image: J.
Time (hi Gascoigne.)
 Chapter 8 Continental Shelf Seabed
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8.3.2 Life mode and mobility of biota
The sessile components of the benthos are more closely
associated with the composition and physical character-
istics of the seabed and show seasonal growth followed
by periods of winter dormancy at higher latitudes. This is
true both of macroalgae and particularly of colonial ani-
mals, such as hydroids. In contrast, much of the epiben-
thos exhibits varying degrees of mobility from crawling
gastropod molluscs and starfishes to highly mobile fish.
Despite their apparently slow speed, starfish are known to
occur in dense feeding aggregations. which move slowly
and systematically across the seabed. consuming animals
in their path. Where these 'swarms' coincide with commer-
cial shellfish beds they can cause severe economic losses
for cultivators. Many crabs (e.g. Cancer pagurus and Maja
squinado) move inshore in the spring and summer where
mating occurs. often in dense aggregations, followed by a
movement into deeper offshore water during the winter
months to avoid wave action and severe decreases in near-
shore water temperature.
Sessile biota show seasonal patterns of growth and
dormancy at hig h latitudes, while mobile epifauna
exhibit varying degrees of inshore/offshore movement
in response to water temperature. Inshore migrations
of many decapods (crabs and lobsters) coincide with
mating aggregations.
The distribution of bottom-dwelling fish can be linked
strongly to certain habitat types within regional seas, par-
ticularly when associated with specific habitats such as
reefs or kelp beds. However, in regions where sediments
predominate at mid to high latitudes, fish species are often
associated with a range of sedimentary habitats that may
vary from fine sand to gravel as in plaice (Pleuronectes pla-
tessa) (Kaiser et al. 1999a; Shucksmith et al. 2006) (Fig.
8.6) . Such variation in habitat use can be attributed to dif-
ferent behavioural characteristics at different life-history
stages. Juvenile plaice are strongly selective of specific
sediment grain sizes, as this determines their ability to
burrow into the substratum to evade predation; however,
adult plaice are released to some extent from predation
pressure (apart from fishing) and utilize a wider range of
habitats (Gibson & Robb 1992; Shucksmith et al. 2006).
Some species make extensive spawning migrations (Box
8.3) . For example, plaice in the eastern English Channel
migrate hundreds of kilometres to reach spawning grounds
in the North Sea and show activity patterns that utilize the
prevailing tidal currents to reduce the energy expended
during the migration (Metcalfe & Arnold 1997). Other fish,
such as bass (Dicentrachus labrax), undertake seasonal
migrations that track the rise and fall of seawater tempera-
ture as they require a minimum seawater temperature of
9°C for ovary maturation to occur. Typically, stocks move
north from the coast of France and up through the English
Channel and Irish Sea in late spring, returning south in
the late autumn with falling water temperature. However,
over the past decade there is a stronger tendency for bass
to over-winter in waters where previously they were only
transient. This change in behaviour is directly linked to
increasing seawater temperatures and has also extended
the range of this species further north.

Figure 8.6 Fish show high habitat affinities when the habitat is structured, as in reefs or kelp beds. However, fish
associated with sedimentary habitats tend to be less closely associated with a specific habitat and may occur across a
wide range of sediment types at different stages of their life history. Here an adult plaice is photographed on a uniform
sandy habitat (a), while fish such as this red gurnard (b) are more closely associated with highly structured habitats. The
inset maps show the position at which each of these photographs were taken and highlight great spatial variation at
scales of 1-Skm.

Box 8.3: Migration in continental shelf seas
or;-.,-------;:------:
Sea surface
20
-
E
(urrent direction
.- --.
5 N
Plaice are normally bottom-dwelling fish that spend much
of their time buried in the sediment and, althoug h they
are widespread, they show temporally stable patterns in
distribution, which is stro ngly associated wi th the environ-
mental characteristics of the seabed habitat (Hinz et al.
2003). However, plaice also unde rtake extensive move-
ments to thei r spawning grounds. The data above were
obtained during a study in which a plaice was tagged wi th
data loggers that recorded the fish's depth throughout the
8.4 Functional roles of the
biota
As in all biological systems, the continental shelf seabed
community has representatives that can be categorized
accord ing to what they consume (predators, scavenge rs,
herbivores, filter feeders, suspens ion feeders) or what they
do to the physical structure and processes within the habi-
tat (bioturbators, eco-engineers).
8.4.1 Predators and scavengers
Most animals in continental-shelf systems are highly flex-
ible in terms of their feeding strategy. Nearly all preda-
tors will also scavenge carrion; for example, fish (d ab,
Limanda limanda ), starfis h (Asterias ru bens), decapods
(Cancer irrorat us), and gastro pod snails (e.g. whelks, Bue-
8.4 Functional roles of the biota
..
day. When the tidal stream flowed in a northerly direction
towards the spawning grounds, the fish was seen to swim
up into the water colu mn where it swam with the current
When the t ide t urns in the opposite di rection, the fish
descends to the seabed where it waits for the next turn
of the tide. By adapting its behaviour to take advantage
of the prevailing current, plaice are able to move several
hundred km in less than a week (redrawn from Metcalfe
et al. 2002).
cinu rn undaru rn). Even herbivorous sea urchins (e.g. Echi-
nus esculentus ) and suspens ion feeders such as brittlestars
(e .g. Ophiura ophiura, Ophothrixfragilis ) are known to feed
on carrion from time to time. These animals are known as
facultative scavengers. There is some controversy as to the
possible existence of obligate scavengers, i.e, animals that
consume only carrion, but it appears possible considering
the physiological energetic constraints . The most likely
candidates would seem to be sm all (< 6 mm long) lysianas-
sid amphipods of the genus Orehomene, wh ich appear to
specialize in the consumption of crustacean carrion. This
group of amphipods show m any specialist adaptat ions to a
scavenging lifestyle, such as the ability to survive extended
periods without food and to gorge on carrion such that their
body size increases by up to 500%. However, a convincing
experimental demonstration of an obligate scavenging life-
style remains elusive (Ruxton & Houston 2004) .
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Many consumers at high latitudes exhibit multiple feed-
ing modes and often resort to scavenging when carrion
is available-t hese are facultative scavengers. Carrion is
more likely to occur at high latitu des where physical pro-
cesses are a significant source of natural mortality.
The existence of a purely scavenging (obligate) lifestyle
remains speculative in cont inental-shelf systems. If they
occur, obligate scavengers are most likely to be fo und
among t he small-body-sized scavenging amp hipod
fauna.
8.4.2 Grazers
Grazing animals include herbivorous fishes, such as some
blennies (Blenniidae), sea breams (Sparidae), gastropod
molluscs, and sea urchins, all ofwhich playa key role in the
maintenance of diversity within algal-dominated commu-
nities. Herbivory in fishes is much more prevalent towards
lower latitudes, while at higher latitudes herbivores are
primarily invertebrates. In systems in which a particular
species or guild is the predominant grazer. they can have a
keystone or eco-engineering role on the habitat through
their consumption ofcertain types of algae. Grazers are not
the only eco-engineers, as we will see a little later (8.5.1).
Grazers also include carnivores such as nudibranch mol-
luscs (sea slugs) that consume encrusting bryozoa, soft
corals. and sponges by scraping at the colonies with their
radula. Some of these associations may be very specific; for
example, the sea slug Tritonia hombergii graze dead men's
fingers (Alcyonium digitatum) and may be one of the few
predators of this soft coral. Many of the external morpho-
logical features of bryozoa (spines) and the extracellular
products of sponges and soft corals act as defence mechan-
isms against the predatory activities of sea slugs, which
has developed into an 'evo lutio nary arms race' between
predator and prey.
The development of comp lex ornamentat ion in gastro-
pod shells is a stro ng evol utionary driver of cheliped
morphology (claw design) in snail-eating crabs and is a
classic example of the 'evolutionary arms race'.
8.4.3 Particle feeders
Filter feeders such as oysters. mussels, and clams extract
phytoplankton from the water column and suspended mat-
ter from just above the seabed (su spe nsion feeding) . An
individual animal of 1 g ash-free dry weight is estimated
to filter 57litres of water per day (Heip et al. 1995). Con-
sequently, filter feeders have an important role in ben-
tho-pelagic coupling as they process phytoplankton and
suspended organic matter into faeces and pseudofaeces,
which are deposited on the seabed. This material is rich in
organic matter. which is processed by the microbial com-
munity and in turn feeds suspension feeders such as clams
(e.g, Mya truncata), and bulk sediment processors such as
irregular sea urchins (Echinocardium cordatum), sipun-
culans, and polychaetes. Bryozoa, hydrozoans, sponges,
and anemones are particle feeders; although there is some
evidence that the latter two animal types can also absorb
dissolved organic matter through their body wall as a sup-
plementary food source. These groups are more prevalent
in deeper water than filter feeders that rely upon a supply
of phytoplankton. Indeed, there is a strong negative rela-
tionship between depth and filter-feeder biomass, declining
down to 50 m from 3 to 0.2 g carbon m-2 for the North Sea
(Bryant et al. 1995).
Biomass is somet imes calculated as the dry weight of
living tissues (including shell material) minus the ash
remaining after combustion , i.e. ash-free dry weight.
Pseudofaeces are the means by w hich filter-feeding biota
rid themselves of indigestible or rejected particles. These
particles are bound in mucus secreted by gill tissues.
M ucus production requires energy expenditure and is
one reason why filter feeding ceases when suspended
sediment loads become excessive.
8.4.4 Bioturbators
Animals can have both a stabilizing and a destabilizing role
within sediments. Palaeoecologists have studied in great
detail the manner in which live animals perturb sediment
structures. This has given them insights regarding the likely
agents of trace fossils that have recorded the passage of
animals through or across sediment habitats. A seminal
publication by Schafer (1972) describes in detail the dif-
ferent modes ofsediment disruption that occur as a result of
animal activities. These vary from the surface bulldozers.
such as irregular sea urchins and gastropods, to the feed-
ing pits of starfish and elasmobranch fishes such as rays,
to the burrow labyrinths and chambers created by burrow-
ing crustacea (Box 8.4 and Current Focus) . The cumulative
effects of these animal related sediment disturbances are
known as bioturbation.
Bioturbators have left their mark in fossilized sediment-
ary rocks. These are termed trace fossils.
 8.4 Functional roles of the biota

Bioturbators perform a key role in seabed systems as
they enhance the passage of oxygenated water deeper into
the sedime nt than it would ot herwise penetrate by passive
diffusion between sed ime nt particles. Increases in surface
sediment porosity have been found in association w it h the
deposit-feeding bivalve Yoldia limatula and at a depth of
9-12 cm as a result of the deposit-feeding activities of the
polychaete Heteromastus fi liform is (Mulsow et al. 2002) .
The physical movements of these animals as they feed
and reposition disrupts sedime nt structure and thereby
increases sediment porosity. The depth and complexity of
the burrow structures vary considerably among different
species and can vary in depth from a few centimetres to
metres (Jones & Jago 1993). These burrows can extend
well into the deeper layers of the sedime nt that are charac-
teristically coloured black due to the bacterial production
of hydrogen sulphide (H,S) in the absence of oxygen. The
burrows themselves increase the surface area available for
oxygen and nutrient exchange that enco urages enhanced
microbial activity on and in the burrow walls. For example,

Box 8.4: Influence of fauna on (0)

sediment structure
(a) Callianasid shrimps live in soft muddy/sand sedi-
ments and create intricate sub-sediment passageways.
Apart from the burrow entrance there are other con-
nections to the sediment surface that emerge within
sediment mounds that act as chimneys on the sea-
bed. These chimneys cause water to accelerate as it
passes over the mound , which draws water within the
chimney out. This causes the water within the burrow
system to move through the passageways and thereby
encourages new oxygenated water to be drawn into
the burrow system. The shrimp store food and 'garden'
microbial activity inside chambers.

(b)
(b) Echiuran worms use their highly extendable probos-
cis to gather surface sediment matter at great distances
(150 cm) from the entrance of their burrow. Once the
sediment has passed through their gut it is expelled in
a faecal mound. Echiuran burrows are often inhabited
by lodgers such as blennies and scale worms.

(c) Feeding pits are excavated by starfish while trying

to consume a burrowing sea urchin (photograph: James
Perrins).
 Chapter 8 Continental Shelf Seabed
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the brittlestar (Amphiurafiliform is) occurs in densities as
h igh as 70 0 m? in Galway Bay, Ireland. The burrow s con -
structed by such a high d ensity of a nimals can expose 1.4 m 2
of burrow w all m- 2 of the seabed (Solan & Kennedy 20 03 ) .
Sediment conveyors, suc h as callianassids and ech iu -
ran worms , transfer surface sed ime nts to deeper layers
wit h in the sed imen t, w hich results in a pe ak in ch lorophyll
a concentration that is greater than that at the sed ime nt
surface . Branch an d Pringle (1987) found that ch lorophyll
a concentration was greatest at a depth of 15-25 em in the
presence of Callianassa kraussi. At this depth the sub-sur-
face sediments are reworked by burrowing animals such as
urchins (Echinocardium corda t um ) an d polychaetes such as
Scoloplos armiger, w hich ingest sed imen t from w hich they
digest organic m atter an d bacteria . These processes recycle
minerals and nutrients w hen the y a re transferred to the sur-
face o f the seabed as sed imen t m ound s and faecal pellets.
Bioturbators increase the complexity of the surface of
the substratum through the creation of pits and mounds
and enhance the exchange of oxygen and nutrients
across burrow walls that occur to a depth of up to 2 m
in the sediment.
Sed imen t conveyors m ake a sign ifican t con tr ibu tion to
the resuspension of sed imen t in the overlying water colu m n
and influence seabed topogra phy. Rowden et al. (1998)
und ertook both laboratory a nd field trials u sing the mud
sh r imp (Callianassa subterranea) and found that sed imen t
reworking va ried with temp erature and h ence season. They
estimated a n a n nual sed imen t turnover budget o f 11 000
CURRENT FOCUS: Estimation of
ecosystem functioning in sediments
Mixing of marine sediments by the resid ent fauna is an
important ecosystem function (Naaem et al. 2002) that
increases the penetrat ion of oxygenated wa ter d eeper
into the sediment than w ou ld occur w ithout these fauna.
Thus sediments w ith a high biomass of fauna that mix
sediments w ill enhance biological production of micro-
bia l, mei ofaunal , and macrofaunal biota. Different spe-
cies wi thin an assemblage w ill affect the sediment to a
greater or lesser extent depending on their feedi ng mode
or lifesty le (e.g. active burrower versus sedentary deposit
feeder). It is possible to est imate the b iot urbation poten-
tial for the speci es sam pled at an individual sampling point
according to the followi ng equation (Solan et al. 2004) :
s,
BFj = L;=1
R, ' AFDMij
g (d r y weigh t) m? yr ' . Field observations a t a site in the
Nort h Sea demonstrated that the sediment expelled by the
mud sh rim p formed unconsolidated volcano-like m ounds,
w h ich sign ifican tly m odify seabed su rface topography. Ca l-
lianassa subterranea's m aximum con tr ibu tion to sediment
resuspension results in a lateral sed imen t transport r ate of
7 kg m' month:". Thus, mud sh rim ps n ot on ly re work sedi-
m ent d ee p w it h in the substratu m bu t are also important
d eterminants of the rate of sed imen t exchange between
adjacen t sed imentar y h abitats.
Ech iu ran wor ms are a bu ndant bioturbators of mud sedi-
m ents. However they are extremely d ifficu lt to stu dy in lab-
orator y stu d ies due to their fragility, an d the y a ppear to be
relatively immobile once established. Hughes et al. (1 99 9 )
studied the rate of sedimen t ejection by the ech iu ran worm
Maxmuelleria lankesteri in the field. They found that bur-
rows and sed imen ts persisted throughout the I -year stud y
period a nd that worms ejected sediments year round . The
m ean ejection rate was 2748 g burrow-' y ' . The su perfi-
cial sed imen t, on w hich M. lankesteri feeds, was ve r y r ich
in organ ic matter, w ith m onthly valu es of a pproximately
12-17% sediment dry weigh t . Ejection rate remained con -
stan t at labile fractions of organic matter below - 50% , bu t
increa sed sh ar ply a bove this threshold, so sedimen t ejec-
tion rate increased w ith increa sing food qu ality. Bu r rows
a ppeared to be static an d individual ejecta m ounds cou ld
persist for longer than a yea r. Th is is qu ite different to d eep-
sea ech iu ra for w h ich changes in burrow m orphology are
more frequent and prob ably relate to the higher quantity of
labile organ ic m atter on the con ti nen tal shelf.
BPj is the community bioturbation potent ial at sampling
pointj, estim ated as the sum of the products of the sedi-
ment reworking mod e for each species i (R) and its ash-
free dry mass (AFDM ij ) . Sj is the observed number of
species (speci es richness) at sampling point j. Sed iment
reworking mod es (R) are defined in a number of reviews
(e.g. Solan et al. 2004 ; Michaud et al. 2006) . R, values
ranged from - 1 (for sediment stabilizers) to 4 (for sedi-
ment regenerators).
We can relate the bioturbation potential of an assem-
blage of organisms by quantifying the sediment mixing
depth using a sediment p rofile imag ing camera (SPI)
(Rhoads & Cand e 197 1). The SPI consists of a ca me ra
mounted above a prism contain ing distilled water with a
side-mounted tran sparent Perspex plate. As the prism is
p ushed into the sediment it is possible to obtain a pho-
tographic image of a vert ical transect of the sediment.
The resulting image can be analysed wi th image-analysis
 8.5 Food webs in shell systems

software. The image is partitioned into layers of binary reduced sediment fracti ons, using a standardized pixel
images, from which it is possi ble to separate oxic and intensity th reshold.

1·1 (b) (<)

18 18 18
16 16
•
.• j•
• 16
_14 E 14 • • •• _ 14

- ~-! 12 fi
E E
-"-1 2 • • -"- 12
•
""- ""-
-
g-lO
.:.0 8
ca 6
•
I
•
•
.~
,. 6
10
8
golD
-,.-
.a 8
•
• ~.
,
•
•
•• • 6 ••
•
4
2
:!-: 4
2
4
2
~

•• •
0 , , , , , , , , 0 , , , 0 , , , , , , , ,
0 2 4 6 8 10 12 14 16 0.0 0.5 1.0 1.5 2.0 0 2 4 6 8 10 12 14 16
Community biotu rbation potential Community bioturbation potential Community bioturbation potential

Thi s examp le is taken from a st udy of th e effects of an
invasive species of clam (Manila clam Tapes philippina-
rum ) o n ecosystem functi on (sed iment mixin g) across
three sites in Europe. The relationsh ips betw een est i-
mated sediment mixing depth (e m) , co mmunity biotur-
bat ion potential, a nd measured habitat cha racterist ics
at the three sites a re hi ghly va riable, whic h indicates
that th e effect of Man ila cla m va ries acco rdi ng to th e
co ntext of the enviro nment it invades. (a) Ria For-
mosa , Portugal; (b) Bay of Arcachon, France, o utside
of seag rass patches: black for stat ions where a coarse
sedime nt fraction (> 5 mm) was present, and grey for
stat ions wit h finer sedi me nts; (c) Poole Harbour, UK.
Ad apted from Quei ros et a l. 2011 .

8.5 Food webs in shelf Food-web complexity confers ecosystem resilience

systems
The study of food webs provides the framework to under-
stand consequences of the interactions between species
within a system, i.e , the pathway of consumption and the
flow of energy from one trophic level to another. Several
metrics of food webs provide insight into biomass partition-
ing and production in an ecosystem. Species richness and
the number of species interactions (links between species)
are among the most important of these metrics. Even for
relatively simplified systems in wh ich many species have
been lumped together in general categories (e.g. bacteria)
the linkages among d ifferent species or groupings is h ighly
complex (Fig. 8. 7).
8.5.1 Ecosystem resilience
The flexibility of feeding modes (including cann ibalism)
gives rise to great complexity in continental-shelf systems
(Link 2002) (Box 8.5) . This complexity means that the
removal of one or two or more species from t he system is
unlikely to bring about significant cascade effects at either
h igher or lower trophic levels, and is a general feature of
marine foods we bs (Frank et al. 2005) .
unless major environmental changes (e.g. EI Nino) or
human intervention cause multiple species replacements
or extirpations.
Ecosystem resilience can we aken considerably when
environmental and human sources of stress act simultane -
ously and may lead to a phase shift in t he ecosystem. A
combination of chron ic over-harvesting across a wide range
of fish and shellfis h species combined with decadal changes
in water temperature and stratification (which affects pri-
mary production) , has caused the decoup ling of the ben-
thic- pelagic system on the eastern Scotian Shelf off Nova
Scotia. Severe declines in demersal (bottom-dwelling) fish
productivity have coincided with compensatory increases
in pelagic fish biomass (Choi et al. 2004) . What we have
seen is a switch from a system dominated by benthic biota
and bottom-feeding fishes, like cod and haddock, to one
dominated by zooplankton and planktivorous fishes. How-
ever, it is important to note that phase shifts also occur
in response to strong environmental forcing (e.g. El Nino
events) without any interference from humans (Gra nt ham
et al. 2004).
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

74 78 79

. , 68

41

3
19

2 1

Figure 8.7 Species and links of the north-west Atlantic food web. The web represents interactions at the approximate
trophic level of each species, with increasing trophic level towards the top of the web. The left side of the web generally
typifies pelagic organisms, and the right to middle represents more benthic/demersally oriented organisms. 1 = Detritus.
2 = Phytoplankton. 3 = Co/anus spp.. 4 = Other copepods. 5 = Ctenophores. 6 = Chaetognatha (i.e. arrow worms).
7 = Jellyfish. 8 = Euphausiids. 9 = Crangon spp.. 10= Mysids. 11 = Pandalids. 12 = Other Decapods. 13 = Gammarids.
14 = Hyperi ids. 15 = Caprellids. 16 = Isopods. 17 = P1eropods. 18 = Cumaceans. 19 = Mantis shrimps. 20 = Tunicates.
2 1 = Porifera. 22 = Cancer crabs. 23 = Other crabs. 24 = Lobster. 25 = Hydroids. 26 = Corals, anenomes.
27 = Polychaetes. 28 = Other worms. 29 = Starfish. 30 = Brittlestars. 31 = Sea cucumbers. 32 = Scallops. 33 = Clams,
mussels. 34 = Snails. 35 = Urchins. 36 = Sand lance. 37 = Atlant ic herring. 38 = Alewife. 39 = Atlant ic mackerel.
40 = Butterfish. 41 = Loligo. 42 = lIIex. 43 = Pollock. 44 = Silver hake. 45 = Spotted hake. 4 6 = White hake.
47 = Red hake. 48 = Atlant ic cod. 49 = Haddock. 50 = Sea raven. 51 = Longhorn sculpin. 52 = Little skate.
53 = Winter skate. 54 = Thorny skate. 55 = Ocean pout. 56 = Cusk. 57 = Wolfish. 58 = Cunner. 59 = Sea ro bins.
60 = Redfish. 61 = Yellowtail flounder. 62 = Windowpane flounder. 63 = Summer flounder. 64 = Witch flounder.
65 = Four-spot flounder. 66 = Winter flounder. 67 = American plaice. 68 = American halibut . 69 = Smooth dogfish.
70 = Spiny dogfish. 71 = Goosefish. 72 = Weakfish. 73 = Bluefish. 74 = Baleen whales. 75 = Toot hed whales,
porpoises. 76 = Seals. 77 = Migratory scombrids. 78 = Migratory sharks. 79 = Migratory billfish. 80 = Birds.
8 1 = Humans. (From Link 2002.)

Box 8.5: Complex feeding interactions
The flexibility of feedi ng modes in shelf systems makes
food-web analyses extremely complicated, but has given
rise to some fasci nati ng behaviou ral interactions between
predators and their prey. In the North Atlantic, the starfish
(Leptasterias polaris) is a voracious predator of the w helk
Buccinum undatum. When rest ing, whel ks remain buried in
the seabed to red uce the chance of detection by preda-
tors. Leptasterias are extra-oral feeders, such that once
they have begun to digest their prey they are less likely
to be able to catch and consume anything else. Extra-oral
digestion can be messy, and amino acids and adenosine
(0)
(a) A buried whelk Buccinum undatum with its sip ho n protruding above the sandy subst rat um and (b) a st arfi sh
Asterias rubens succumbs a whelk using extra-oral digestion. Hermit crabs (Pagurus bernhardus) are attracted by
the molecular stimulants released during extra-oral digestion (photograph s: James Perrin s).
Extra-oral digestion is a process whereby starfishes
extrude their stomach on to their prey, which is thereby
enveloped and covered in digestive enzymes. Not all
starfishes use this technique and many ingest their prey
whole whereupon digestion occurrs intraorally.
Organisms within food webs are assigned to a particular
trophic level according to their relationship with other
components [i.e. their role as predators and prey) in the
food web, hence bacteria and other primary producers
are found at the bottom of the food web at the lowest
trophic levels and apex predators at the top, and hence
highest trophic levels (Chapter 4).
8.5.2 Trophic cascades
Scientists have looked hard for evidence of strong species'
interactions in both terrestrial and aquatic food webs with
limited success (Table 8.2) . In situations where strong link-
8.5 Food webs in shell systems
t riphosphate (a poten t attractant of scavenging Inver-
tebrates) leak into the surrou ndi ng water. Despi te the
normal risk of being eaten, whelks will approach feeding
starfish and are able to consume some of the prey tha t is
in the process of being digested (Rochette et al. 2001).
This behaviour is known as kleptoparasitism . Rochette
et al. (2001) found that this behaviour was more preva-
lent in large r female whelks just before the time they were
due to lay their eggs. Hence the whelks were bolder w hen
thei r energy dem ands were greatest. Afte r thei r eggs had
been laid, female w helks we re far less likely to approach
or feed in the presence of predatory starfish.
(b)
ages occur among species, several rules of thumb seem to
apply. Some examples of cascades are given in Table 8.2.
In all cases, none of the cascades involve more than three
interactions between different species, i.e. they are simple
systems even though they may be embedded within highly
diverse and complex systems . These embedded mini-sys-
tems are perhaps to be expected in high-diversity ecosys-
tems that are characterized by more specialized feeding
interactions (e.g. coral reefs). The interactions that occur
wit hin the cascade are between organisms from major tro-
phic levels within a system, e.g. predator-herbivore-pri-
mary producer, few involve intermediate trophic levels.
In contrast, the food web of the Benguela upwelling system
has at least seven interactions between the bottom and the
top of the system. Key predators or herbivores in trophic
cascades are usu ally the do minant organisms at their tro-
phic level and often these can be ecosystem-engineering
biota. In the case of a significant decrease in the population
of a pred ator or herbivore, there are few others to take their
place, which means that linkage between one trophic level
and another is strong . This contrasts sharply with many of
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the more 'open' marine ecosystems where there may be
three or more predators that exert similar levels of preda-
tion on one or more species (e.g. birds, cetaceans, and seals
all eat the sam e pelagic fishes in the Benguela upwelling
system) (Yodzis 1998 ). Cannibalism is rare w ithin species
involved in systems prone to trophic cascades in sharp con-
trast to many marine ecosystems in which cannibalism is
common; for example, North Atlantic cod (Gadus morh ua)
and hake (M er/uccius spp.) are both good examples of fish
that exert considerable density-dependent predation pres-
sure on their own species.
Trophic cascades are likely to occur when the linkages
between species are strong and the linkages occur
between species assigned to major trophic levels.
Ecosystem engineering biota are those that due to their
abundance and feeding or other activities exert a strong
influence on the structure of the ecosystem, e.g. urchins
grazing kelp.
8.5.3 Hunting, fishing, and trophic
cascades
Understanding the characteristics of communities in which
trophic cascades are likely to occur is critical for effective
conservation management (Chapter 16). On the west coast
of North Ame rica, the effective conservation of sea otter
(En hy d ra /utr is ) may have helped to conserve kelp beds
that provide important habitats for many fish and inver-
tebrates. Past hunting of sea otters depleted their popu-
lations so severely that they no longer exerted significant

Table 8.2 Examples of trophic cascades from marine, freshwater, and terrestrial systems (adapted from Pace et
al. 1999).

Ecosystem Cascade Evidence Effects

Marine

Oceanic Salmon- Ten-year t ime series Increased phytopl ankton w hen salmon
zooplankton- abundant
phytoplankton
Coastal Whales-otter- Long-term data and Predation by w hales on otters leads to urchin
urchins- kelp behavioural stu dies populat ion expansion and increased grazi ng
of kelp
Intertidal Birds- urchins- Manipulation of bird Algal cover greatly increased w hen urchins
macroalgae preda tion on urchins reduced

Fresh water

St reams Fish- invertebrates- 1o and 2° product ion Annual 10 production affecte d by 6-fold
periphyton affected by predat ion of d ifference
invertebrate popul at ions
Shallow lake Fish-zoopl ankton- Ob servations of lakes Reductions in fish abundance led to shift in
phytoplankton und er cle ar and t urbid zooplan kton size-structure w ith consequent
conditions effects on phyto plankton
•••••••••••••••••••••••••••• •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •••••••••••••••••••••• •

Terrestrial

Meadow Lizards- Ob servations and Grasshopper density med iated by lizards,

grasshopper-plants expe rimental stu dies plant biomass decline wi th decreasing lizard
predation
Trop ical Beetles-ants- Ob servations and Beetles predate ants that remove herbivoro us
forest insects-p iper plants manip ulation of beetle insects that consu me plants. More fo liage
density in enclosures consu med in presence of beet les.
Boreal forest Wolves- moose- Study of moose g razin g Population cycl es of wolves, moose, and
balsam fi r over 30 years balsam fir
 8.6 Characterization of seabed communities
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
predatory control over urchin populations. Under normal
circumstances urchins consume algal material at the base
of the kelp canopy, but with an increase in their popula-
tion the urchins began to deplete kelp beds through grazing
pressure. This excessive grazing resulted in urchin barren
grounds, where the bedrock was colonized by small epi!-
ithic algal species and urchins.
Once established , urchin barren gro unds are persistent
un less predation pressure increases, the urchins are
physically removed or mortality increases due to disease.
Urchin barren grounds represent a phase-shift that has
been repeated in other systems around the globe, notably
on coral reefs. Urchins are capable of surviving on minimal
energy intake for extended periods of time. Once urchin
barrens are established, only urchin disease or an increase
in predation can possibly reverse the shift to the former
state. In the late-twentieth century, otter populations have
grown following hunting bans and improved conservation,
so they have exerted in turn more predation pressure on the
urchins. This has allowed kelp beds to establish on areas
of barren ground. Clearly, these effects can be confounded
by many other factors, such as oceanographic effects (e.g.
temperature and current patterns) on urchin recruitment.
and kelp growth and survival, which has been negatively
affected by pollution and over-harvesting in the past decade.
In general terms. the effective conservation ofotters has
helped to conserve the kelp beds (Estes & Duggins 1995) .
Or so we thought, until Estes et a1. (1998) reported annual
declines of2S%year on year for the population of sea otter
at Adak Island, Alaska. Severe declines in the population of
Steller sea lions (Eumetopias jubatus) appear to have trig-
gered a switch in the predatory behaviour of killer whales
(Orcinus oroo) in the Aleutian Islands archipelago. The otter
population living between Kiska and Seguam Islands (an
area spanning about 700 km), totalled about 53 000 sea
otters prior to the early 1990s but was reduced to 13 000
some six years later. Given that a single killer whale can
easily eat more than 1800 otters per year. it is entirely fea-
sible that whale predation may have been one cause of the
decline. The decline in sea lions is either related to cyclic
environmental changes in species of forage fishes. or due
to over-fishing of the latter, or both of these effects acting
together.
Indirect effects of human activities or environmental
changes that occur elsewhere can have indirect effects on
species linkages. This may explain the sudden increase
in sea otter predation by killer whales as a result of a
decline in the population of their normal prey, sea lions.
8.6 Characterization of
seabed communities
Lists ofspecies that comprise a communityare useful at one
level in that they provide an immediate idea of the main
characteristics of the benthos in a particular area and they
are the starting point for understanding the composition of
food webs (above) . However, an over-emphasis on single
species perhaps misses more interesting general structuring
patterns that might be observed across a range ofcommuni-
ties that have different components at the species level. As
we have seen. most communities contain a range of taxa
that can be assigned to different trophic levels or functional
groups within the communiry. Box 8.6 highlights the simi-
lar functional role performed by different species within
distinct assemblages. A broader categorization of commu-
nity constituents may be more ecologically meaningful,
particularly when one is interested in examining long-
term changes in community structure. Over long periods
of time (years) within a community, one species may be
replaced by another, but if their functional role is similar,
then the functional integrity of the community should be
maintained. This situation may occur with rising global sea
temperatures. For example. as high latitude boreal species
begin to retreat further north they will be replaced by colo-
nizing species from lower latitudes that may fulfil a similar
role. This has important implications for how we moni-
tor the composition of coastal communities through time
(Chapter 15) .
An over-obsession with single-species approaches to
monitoring may miss more relevant patterns at higher
levels of organ ization within communities. Nevertheless,
single species may be a useful indicator of ecosystem
health if they represent general community responses
to large-scale perturbations, e.g. the level of tri-butyl tin
in gastropods (Chapter 15).
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 8.6: Functional consistency
between different assemblages
Two communi ty types as descri bed by Thorson (1 9 7 1) .
Althoug h we would avoid using the specific 'labels' or
names for th ese assemblages, both contai n different
species, but in each case it is possibl e to identify dif-
ferent species that perform similar ecological functions.
This consistency in assemblage structu re is ecologically
much more impo rtant than the original aim of Thorson's
descriptions, which atte mpted to catego rize multiple
assemblages as specific ty pes. Thus, it would appear
that general rules can be applied to the composition of
soft-bottom assemblages across a variety of systems. The
distribution of these functional types wi thin assemblages
can alter in response to external forcing factors such as
organic pollution or physical st ress.

Mocomo Aim
Function
Community Community
Myo orenario Myo truncata

Surface suspension feeder

Deep bioturbator

Bivalve Bivalve

ArenicoJa marina Logis koreni

Sediment processor
Sub-surface bioturbator

Polychaete Polychaete

Spionid Abro alba

Suspension and surface deposit

feeder

Polychaete Bivalve

Macoma baJthica Ophiuro sp,

Surface deposit feeder

Bivalve Echinoderm

Cardium edule Phoxus pelJudicus

Suspension feeder
Shallow bioturbator

Bivalve Echinoderm

Pandalussp. BlKcinumundotum

Carnivore
Scavenger
Surface bioturbator

Crustacean Gastropod

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Marine benthic ecologists have typically tried to char-
acterize benthic assemblages in terms of their main (most
abundant) constituent species or those species that occur on
a regular basis in consecutive samples taken from the same
area (often the latter is more important than the former) .
In many ways it is similar to describing terrestrial systems
in terms of oak woodland, bog, or heather moorland. The
notion ofdistinct assemblages that could be assigned labels
was pioneered separately by Petersen (1914) in the North
Sea off Denmark, and later by Jones (1950) and Thorson
(1957) . Petersen gave titles or names to certain types of
benthic assemblage that were encountered, usually based
on the more conspicuous bivalves or echinoderms that were
typical of these assemblages, e.g, Abra community, Brissop-
sis community, shallow Venus community. Jones (1950)
used a slightly different labelling approach, which was based
mainly on a description of the location and sediment asso-
ciation of the community, e.g, boreal offshore muddy-sand
association. These approaches have influenced a great many
subsequent studies that have often attempted to pigeon-hole
the assemblages encountered in the terms used by Petersen.
Jones, and Thorson, hence it is not unusual to read papers
that contain phrases such as 'similarto theAbra community
as described by Petersen'. However, it is clear that benthic
communities are highly varied at different scales in space
and time. hence attempting to attach descriptions to assem-
blages that have only a partial relationship to the limited
range of assemblages of biota studied by Petersen, Jones.
and Thorson is somewhat meaningless.
There is an almost unavoidable tendency for ecologists
to attempt to give names to particular assemblages of
species. It is questionable whether this approach is useful
given the infinite number of possible variants created by
the substitution of one species for another.
The characterization of biological communities on the
basis of habitat characteristics and indicator species pro-
vides a means of describing specific biotopes that then
become a reference point against which to measure tem-
poral change or consistency in community structure. The
biotope classification scheme used by conservation agencies
in the UK is highly advanced and a useful source of ecologi-
cal and habitat information (Fig. 8.8) . This system can be
linked to the European Union Nature Information System
(EUNlS), so that it is comparable at a wider scale. The prob-
lem with such characterizations is that they are potentially
infinite. as the multivariate community statistics on which
they are based are so sensitive that it only requires a slight
deviation in community composition or habitat descrip-
tor (e.g. pebbles versus pebbles with sand) to initiate yet
another biotope description. New combinations or interme-
diate communities are conceivably limitless-and the more
we sample the same marine environment the more variants
8.7 Specific habitats
we will encounter. Global temperature changes are likely to
lead to an increase in the numberofnew variants ofbiotopes
recorded as warm water species invade colder latitudes.
What Keith Hiscock, former Programme Director of the
Marine Life Information Network, thinks of the utility of
biotope classification: 'It is more accurate to indicate
that survey data can usually be matched to a particular
biotope (enabling li ke-with-like comparisons of species
richness, extent etc.) but, inevitably, some survey data or
results of data analysis will be impossible or very difficult
or questionable to match to a particu lar biotope'.
8.7 Specific habitats
The seabed habitat is composed of the inert non-biological
and biogenic material (e .g. broken shell material) and
the biota that live in association with it. In addition to the
prevailing water-column conditions overhead, the inert
elements ofthe habitat dictate the basis ofwhat can, or can-
not, live within or upon that seabed. This normally depends
upon the interaction between seabed hardness and stabil-
ity. The physical nature of the seabed ranges from bed-
rock, boulder fields, cobble pavements, gravel lags, coarse
mixed sediment, sands, and muds. Excluding bedrock, the
physical size of the individual particles that make up these
habitats vary in diameter from micrometres up to several
metres (see also Chapter 6) . At present. sediments domi-
nate the seabed habitat of the continental shelf and vary
according to their tectonic history, the quantity and quality
of riverine inputs of sediment. and the transport by waves
and currents. On the inner continental shelf at depths of
less than 65 m, muds and sands are the most common sub-
stratum (37% and 47%, respectively), while hard substrata
are relatively rare (6%) and the remainder are made up of
reefs and shell debris (Hall 2002). For the purposes of the
next sections we will deal with the general categories of
substrata as hard (bedrock to cobble), soft (gravel to mud),
and biogenic (habitats formed by living organism) habitats.
Coral reefs. mangroves, and seagrasses are the subject of
separate consideration in later chapters.
Sediments dominate the present-day continental shelf
seabed, bedrock and biogenic reef habitats are relatively
uncommon.
8.7.1 Hard habitats
Hard substrata. though rare on the continental shelf, are
probably the most familiar habitats to the general pub-
lic (aside from coral reefs) due to their photogenic biota.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Erect sponges, Eunicella verrucosa and Pen/al1ora foliacea on slightly tide-swept moderately exposed
circalittoral rock. MCR.ErSEun

Recorded and expected MCR.ErSEun

Bedrock with the sea fan Eunicella verrucosa and the soft coral distribution for Britain and Ireland
Alcyonium glomeratum amongst a hydroid turf.
Image width ca 1.0 m.
Image: Rohan Holt
Key Informatio n researc hed by: Angus Jackson & Dr Keith Hiscock This information is not r efereed .

Distribution 01 biotope in Britain and Ireland

Recorded in southern England from Dorset westwards, in the Isles of Scilly and on the north coasts of Devon
and Cornwall, Lundy and Skomer. One record from Bardsey Island in north Wa les (without Eunicella
verrucosa) and also from several locations on the west coast of Ireland inciuding Donegal and Bantry Bays.

Description 01 b iotope

For a full description of Mainly found on exposed and moderately exposed rock, in slight tidal currents and
this biotope inciuding ofte n relatively silty, with a rich variety of species typically including branching and
characterizing species, cup sponges, the sea fan Eunicella verrucosa and the ross coral Pentagora
distri bution, survey foliacea. Typically a bryozoan turf of Cellaria spp. and Bugula spp. is present
information and amongst the larger species (see the biotope CR.Bug) . The branching sponges
references visit Axinella dissimilis, Stelligera spp. and Raspailia spp . are typically present, with
b!!p:llwww. jncc .gov.ukl cup sponges Axinella infundibuliformis and Phakeflia venfilabrum found in some
mennaidlbiotopesl643.htm cases . t,igtonium glomerafum and Parerythropodium coralloides (now Alcyonium
hibernicum) may also be present and short vertical faces sometimes have the star
anemone Pamzoaafhus axinellat!# and/or P8[azoaatlJ.us aagu;comus. There are
numerous examples of sites with lots of branching and cup spo nges where sea
fans have not been found (but are often known to be present within ti1e same
geog raphical area); some of these are included in MCR.ErSPboISH. Diazona
violacea is also often recorded in this biotope although it occurs in MCR .ErSSwi
also. There are a few instances of Swiftia pallida being found at the same sites (in
SW Ireland) as Eunicella verrucosa. W here ti1is biotope occurs on more open
coast (e.g. SW Britain and W Ireland) the cotton spinner sea cucumbe r Holothurla
forskali is ofte n present.

Figure 8.8 An example of database informat ion for a circalittoral biotope as described by the Marine Life Informat io n
Network for Britain and Ireland (MarLIN). The biotope classificat ion scheme is linked directly to the EUNIS classificati o n
system at certai n levels wi thi n its hierarchical structure. The biotope descripti on is composed of a com binat ion of
physical habitat and biological constit uents. For more informat ion on biotope classification and images of biotopes and
ecological informat ion see http:/ / www.marlin.ac.uk (photograp h: Ro han Holt).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Bedrock is inherently the most stable substratum (unless
subject to seismic activity), followed by decreasing sizes
of boulders and cobbles. All of these hard substrata can
be found in a gradient of physical conditions that range
from high to low stress depending upon their exposure
to physical processes such as near-bed flow. wave action,
and scour bywater-borne sediments and glaciers. Thus it is
possible to find bedrock rich in luxuriant epibiota in areas
with clear water and moderate current, or to have bedrock
that is species poor due to high near-bed currents or severe
wave action. Hard substrata provide a secure anchorage for
sessile biota many ofwhich are either macroalgae. encrust-
ing calcareous algae, particle or filter feeders. As for rocky
shore habitats, competition for space is intense and some
organisms such as soft corals, anemones. or sea squirts may
come to dominate a given patch of the habitat.
Hard substrata are occupied by encrusting sessile biota,
hence competition for space is a key community structur-
Ing process.
Hard substrata are particularly important for algae that
require a secure substratum on which they can settle and
then develop a holdfast. Most macro algae would soon be
washed away by currents and waves if they were anchored
in soft sediments. Some smaller algae. such as Enteromor-
pha spp., are able to attach securely to small pebbles or even
the shells of bivalve molluscs, but these occur in relatively
low-energy environments. At higher latitudes. macroalgae
are confined to a relatively narrow coastal band of shallow
water in which light is attenuated rapidly due to the load of
suspended matter in the water column. At mid to low lati-
tudes in regions of upwelling, the biomass of macroalgae
is greatest due to water clarity and the enhanced supply of
nutrients from deeper oceanic water. At lower latitudes. the
water is clear enough to support photosynthesis byepilithic
encrusting algae down to mid shelf depths (75-95 m).
Hard substrata are a fundamental requirement for the
establishment of many macroalgae and enables giant
kelp to attain a length of up to 40 m. Notable excep-
tions include Sargassum muticum, which can survive as a
free-floating form, which partly explains its invasiveness.
Kelps are the subject of fisheries in northern Europe, the
USA, and Chile, and are restricted to mid to high latitudes
(Steneck et al. 2002) . Their economic importance and sen-
sitivity to ecological regime shifts, harvesting, and other
forms of human disturbance mean that harvesting of this
resource requires careful management to ensure sustain-
able use (Box 8.7) . In Chile, management of the harvesting
of kelp resources has occurred for at least a century. The
'parcela' system occurs in two main regions where fishers
extract the kelp Durvillaea antarctica . Fishers are organized
8.7 Specific habitats
in syndicates in which each participant is allocated the har-
vesting rights to a number of boulders on which the kelp
grow. Off the coast of California, giant kelp (Macrocystis
pyrifera) are managed with the use of marine protected
areas. This species can grow at rates of up to 50 cm dol.
The stipe and fronds of these algae are buoyed by gas-filled
pneumatocysts that support the stipe and ensure that the
fronds remain close to the sea surface. where irradiance is
greatest. The high rate of primary production and retention
of kelp detritus in giant kelp forests supports highly diverse
communities with over 200 species of macrobiota ofwhich
36% may be highly associated with the kelp forest (Dayton
1985; Steneck et al. 2002).
Rock reef and boulders with high surface relief will offer a
number of different microhabitats. The sides and overhangs
of reefs and boulders tend to be dominated by particle feed-
ers such as sponges. bryozoa, and sea squirts. Many of the
sessile biota exhibit adaptation to life in changingwater cur-
rents. Flow over polyps and feeding tentacles will affect the
rate ofdelivery offood particles. At low flow rates, the deliv-
ery rate of particles may be insufficient; hence feeding may
cease because it is not energetically profitable. When flow
is too strong, feeding may not be physically possible as par-
ticles evade capture or entrapment and the increased drag
incurred may elevate the risk ofshear or bodydamage, hence
feeding structures are withdrawn. Many of these organisms
also exhibit diurnal patterns in feeding behaviour that coin-
cide with movements of zooplankton in the water column.
Sessile particle feeders modify their feed ing activity in
relation to flow velocity by cessation of feeding when
the delivery rate of particles is too low or when current
velocity might incur physical damage as a resu lt of shear.
The crevices and interstices associated with reef, boul-
der, and cobble habitat permit exchange ofwell-oxygenated
water and provide ideal refugia both from strong near-bed
flow and predators. Many commercially important fishes
utilize boulder reefs in their juvenile stages and experi-
mental and field observations demonstrate the importance
of the protection from predators provided by this habitat
(Auster & Langton 1999). The provision of suitable cryptic
habitat is a critical constraint of commercially important
taxa such as lobsters Homarus gammarus. which com-
pete aggressively for the best refuges, causing displace-
ment of individuals when there is a shortage of suitable
habitat. Small lobsters generally remain within a relatively
restricted area of the seabed moving a distance of <4 km
during a 30-month period, while larger individuals can
move as much as 45 km in the same time (Smith et a1.
2001) . Fishery enhancement programmes have sought to
increase available habitat through the use of artificial reefs
made from a varietyofmaterials includingconcrete blocks,
tyres, and even scrapped streetcars.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 8.7: Distribution and structuring

processes in kelp communities
(a) The distribution of dominant kelp genera around
the world (from Raffaelli & Hawkins 1996). The global
distribution of kelps is physiologically limited by light at
high latitudes and by nutrients, warm water, and com-
petition from macrophytes at low latitudes (Steneck et
al. 2002). (b) Urchins Strongylocentrotus droebachien-
sis are major herbivores of kelp. Over-fishing and the
subsequent extirpation of cod from the inshore waters
of Nova Scotia released sea urchins from predator con-
trol leading to a sequence of phase shifts between sea
urchin and kelp dominated communities. Only the inter-
vention of sea urchin disease increased natural mortal-
ity sufficiently to permit the periodic re-establishment
of the kelp in this system (see also 8.5.3) (adapted from
Steneck et al, 2002).

(a)

-- 0;;,,-- -------
'"'":: ."

MaCfocystis & ____ j1J~rD9'SJis,

- - leSsOniO -
Ecklonio &
Lominorio

Ecklonio
lessonio
Kelp deforestation
reported (usualiy
sea urchins)
(b) Iocsrol cod extirpated Disease cycles
•
Kelp Kelp Kelp & Codium
5 -0 o -e-e e e - 0-"

~
~
~
~ 3
~

~
~
"
0

0
~
-e; 1 Urchin Urchin

1970 1975 1980 1985 1990 1995 1000

Year

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
The availability of suitable crevices can lead to strong
density dependence for animals such as lobsters.
8.7.2 Soft habitats
Soft-sediment characteristics mirror the hydrodynamic
processes and topography of the seabed. Substrata with
particle sizes from gravels down to coarse sands are closely
determined by physical processes (water flow and wave
effects) and as a result are subject to frequent physical dis-
turbance. However as the influence of physical processes
decreases, finer sediments predominate, and biological and
chemical processes begin to have an important influence
on the physical properties of the sediment (Fig. 8.9) . Not
surprisingly, you only tend to find finer sediments in less
physically perturbed environments, i.e. in sheltered shal-
low bays, fjords, or beneath gyres or areas of deeper water
with minimal current. The stability ofsedimentary habitats
depends upon the interaction between physical, biological,
and chemical processes.
Geologists and ecologists typically describe soft sedi-
ments in terms of their particle-size composition. This
necessitates the disaggregation of particles within the
sample. As a result we turn 'living' sediment into one that
has lost most of its biological properties. i.e. the structural
effects of organic molecules and microbial films that coat
the surface of individual particles. During this process
other crucial information about the nature of the habitat
Biologiml
Physical Ihemlml
Penentoge silt ana (Or (ontent
Figure 8.9 The interaction of sediment composition
and biological recovery rate in disturbed sed iments. In
coarse sediments with a low percentage of silt and clay,
physical processes are dominant. As the percentage of
silt and clay content increases, so the contribution of
biolog ical processes, such as microbial activity, become
more important. Chemical attraction is most important in
the finest sediments. Biolog ical recovery rate is slowest
in those sediments that are infl uenced by a mixture of
physical, biological, and chem ical processes. Adapted
from Dernie et al. (2003).
8.7 Specific habitats
,is lost. such that we gain only a partial impression of the
habitat. For example, many of the fine silt and clay parti-
cles «0.063 mm diameter) are elongated or flat with high
surface-to-volume ratios and are attracted to each other
via Van der Waals forces. In contrast. larger particles are
generally spherical and exert no significant inter-particle
attraction. Particle-size analysis tells us nothing about the
packing of the components of the sediment and hence we
are unable to infer to what extent interstitial spaces exist
between particles and hence the porosity (and hence water
content) of the sediment. Sediments with high porositywill
have a greater exchange of oxygenated water, which will
increase the depth within the substratum that free-living
animals can exist. Sediment porosity also affects how eas-
ily organisms can burrow into and through the sediment.
Particle-size analysis of sediment habitats destroys the
physical properties conferred by chemical activity and
biological processes. Techniques that measure the prop-
erty of sediment in situ would give a better indication of
properties relevant to benthic communities.
Near-shore sediments less than 30 m deep are often
highly perturbed by wave action. As a result, emergent ses-
sile epifauna are often absent while highly mobile, robust,
scavengers are often dominant (e.g. swimming crabs,
hermit crabs, starfishes, whelks) . Much of the infaunal
assemblage is characterized by highly mobile short-lived
polychaetes and rapidly burrowing small bivalves (e.g,
predatory worms Glycera spp. and small bivalves such as
Mysella spp. and Donax spp.) . Some larger biomass species
are present, but these tend to be deep (20 em or more) bur-
rowers such as Ensis spp. or Mya spp. Moving into deeper
water beyond the influence of wave action. near-bed cur-
rents become the dominant physical process and can gen-
erate considerable habitat diversity over spatial scales of a
few hundred metres (Fig. 8.10) . The absence of wave dis-
turbance in deeper water coincides with an increase in the
occurrence and biomass of sessile biota such as hydroids,
bryozoans. suspension-feeding bivalves such as scallops,
and tubebuilding polychaetes such as Chaetopterus spp.
(Figs 8 .11 and 8.12) .
Soft-sediment habitats can vary considerably over dis-
tances of <100 m. The hab itat variability is driven by
physical processes such as near-bed currents.
Emergent biota increase the topographic complexity of
the seabed and are often associated with their own diverse
assemblage of biota. For example, Haines and Maurer
(1980) found that the tube complexes of serpulid worms
were closely associated with 54 species, in contrast to the
surrounding sediments that contained 107 species. The
patterns of species' association seem more strongly related
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Emergent sessile biota can support their own microcom-

munity of high diversity per unit volume of habitat. In
add ition to seabed features such as sand waves, emer-
gent fauna provide shelter or a source of prey for many
demersal fishes.

The additional structural complexity afforded by emer-

Figure 8.10 Near-bed currents can generate considerable
habitat heterogeneity in near-coast subtidal systems.
This image is derived from acoustic data of the seabed
showing a strip of seabed approximately 200 m wide.
Two distinctly different sediment habitats are apparent:
(a) mobile megaripple systems, which are subject to
daily physical stress and erosion that are dominated
small-body-sized fauna; and (b) more stable shelly gravel
sand sediments that are typified
feeding communities.
to the architecture of the structure rather than the identity
of the tube-building species. The tube complexes of both
the serpulid Hydroides dianthus and Pomatocerus triqueter
had similar associates: Nereis succinea, Lepidonotus squama-
Ius, Polydora ligni, Eumida sanguinea, Syllis gracilis (Kaiser
et at. 1999b). Thus, similar structures on the seabed would
appear to attract comparable groupings of fauna.
gent fauna and bedforms has important implications for
habitat use by more mobile species. Bottom-dwelling
fishes, such as silver hake (Merluccius bi/inearis), use small-
scale seabed features, such as sand ripples. to shelter from
currents oras coverfrom where they ambush prey (Auster
et at. 2003) . The high abundance of prey associated with
complex seabed structures is an important food source for
many bottom-dwelling fishes, as revealed by analysis of
their diets. In softer mud sediments, cerianthid anemones
and sea pens (Virgularia spp.) are among the few emergent
fauna that exist in this habitat (Fig. 8.11).
In deeper water (>50 m deep), in basins or in shallow,
sheltered areas. finer sediments. such as silts and muds.
are able to settle out due to reduced physical forcing. The
by epifauna tends to be sparse in such areas with few sessile
emergent species (mainly anemones and sea pens) and
by filter- and suspension- low abundances of mobile scavengers. such as starfishes
and hermit crabs. The fauna is typified by burrowing mega-
fauna that shape the surface of the seabed with burrow
entrances and mounds of excavated sediment and faeces
(8.4.4) . The fauna is dominated by crustaceans, typically
callianassids, with commercial fisheries for Norwaylobster
(Nephrops norvegicus) and hyperbenthic pandalid shrimps.
Echiuran worms are deposit feeders that use a highly
extensible proboscis to feed on surface organic matter at
distances up to 1 m or more from their burrow entrance.

0.9 0.07 0
0
00
0 (,j (b)
0.8 0 0.06
~
0
0.7 0.05
-...
~
~ 0.6 0
~ 0.04 0 0 0
• 05 0
--=
0.4 0
~
• 0.03
-a,

----
0
g 0.3 0
0 ~ 0.02
~

0.2 8
0
0.01
0
-
-
°0 0
o 08
0 o
0.1 0 00 0 0000000 0 0 m~

0 ~.Ol Figure 8.11 The changes in soft-

40 so 60 70 80 90 40 SO 60 70 80 90
sediment characteristics with
Water depth Water depth
1.0 increasing depth as measured from
c
0 0 (I) photographic images of the seabed.
=
0
co 00
0

'"•
E 0
0 Featureless sand habitat (a) that

-••
~

E
05
0 0 is frequently rippled (b) is typical
of relatively shallow water depths
~
=~ (40 to 60 m). Emergent fauna were
~
0 0
0
~
c increasingly evident as sandy substrata
0 ~

occurred in water deeper than 60 m

40 SO 60 70 80 90
Water depth (c). (Lindholm et al. 2004.)
 8.7 Specific habitats
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

These worms graze the surface sediment sequentially in munity has sufficient time to become replenished through
a circular fashion, such that the surface microbial com- production processes (see also section 8.4.4) . The burrow

(0) (b)
•

(e)

(e)

(g)

Figure 8.12 A selection of sedimentary habitats. (a) A fine muddy habitat wit h brittlestars and a sea pen; burrow
entrances and mounds ind icate the presence of a high number of bioturbators in th is habitat. (b) A sandy mud habitat
wit h evidence of some reworking of seabed sediments by bottom currents. A surface dwelling sea slug Scaphander
sp. leaves a distinctive surface furrow just above the starfish. (c) A mobile sandy habitat formed by near-bed tidal
currents, which is typified by small infaunal organisms and an impoverished epifaunal commu nity. (d) A typical mixed
sediment with a veneer of sand overlying a coarse gravel and shell sediment. (e) A stable, mixed sediment dominated
by cobbles and gravel. This stable substratum is typically colon ized by large, attached filter feeders, such as hydrozoans
and bryozoans and anemones. (I) A cobble and mixed sediment habitat dominated by the sli pper limpet (Crepidula
fornicata) with clumps of blue mussels (Mytilus edulis). (g) A muddy, sand habitat stabilized by a lawn of tube-build ing
polychaetes Lanice concheliga. These hab itats provide rich feed ing grounds for flatfishes. (h) A biogenic habitat
dom inated by horse mussels showing the deposition of silt and organic matter among t he shell matrix. This community
is typified by a high abundance of filter- and deposit-feeding epibiota and has a high diversity of associated species.
Photographs © E. Ivor S. Rees. See the online resource centre for additional images.
 Chapter 8 Continental Shelf Seabed
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

entrances, mounds, and pits excavated by the infauna also
provide important shelter for fish species, and often a num-
ber of species will share the same burrow complex.
Mud-sediment habitats are typified by limited emergent
sessile fauna and a low diversity of mobile epibenthos.
Many semi-enclosed seas (The Adriatic, The Baltic) and
fjordic areas are typified by mud communities due to their
sheltered nature and low current regime (Chapter 5). How-
ever, the enclosed nature of these water bod ies encourages
strong stratifica tion of the water column in the summe r.
The combined effects of eutrophication and stratification
can le ad to periodic anoxic events at the seabed w ith a
100% mortality of the benthos (Chapter 15). For example,
over the past two decades, the sublittoral benthic commu -
nities of the Northern Adriatic Sea have suffered repeated
large-scale mortalities (JustiC199 1) . These events have also
been associated with an excessive development of marine
snow, which blankets benthic biota and elevates microbial
activity suc h that oxygen at the seabed is rapidly depleted.
The benthic com mun ities in the Northern Adriatic are
composed largely of sessile, epibenthic filter- and suspen-
sion-feeding organisms. They are long-lived and typically
aggregated into so-called multi-species' clumps, whic h is an
unusual feature for muddy sediments (Box 8.8). The filter-
feeding activity of these multi-species' clumps is critical for
benthic-pelagic coupling in this system. The longevity of
the species involved means that repeated anoxic events do
not leave sufficient time for these associations to recruit and
become reestablished.
Soft-sediment communities in semi-enclosed seas areas
are subject to periodic anoxic events that can lead to
1000;0 mortality of the macrobenthos.
8.7.3 Biogenic reefs
Biogenic habitats or reefs are structures created by aggrega-
tions of organisms, which may or m ay not rise from the sea-
bed, that form a discrete community from the surround ing
habitat. Biogenic reefs can be composed ent irely of the reef-
building organisms or accumulations of biota, organic, and
inorganic m aterial. Suc h habitats are formed by bivalves
(e.g. oysters, mussels), polychaetes (e .g. Sabel/aria spp.),
corals, and sponges. Locally, biogenic reefs can contribute
to significant proportions of the seabed habitat (Lenihan &

Box 8.8: Multi-species' clumps in the

10)
Northern Adriatic
(a) Characteristic high-biomass co mmunity co ns ist ing
of s po nges, ascidians, and brittlestars at 25 m depth in
the Gulf of Trieste. The organisms are typically aggre-
gated into so-ca ll ed multi-species' clumps. Marine
snow events are often associated with hypoxia-related
mortalities. In an advan ced stage, enormous cloud-like
mucus aggregates eventually sink to the sea floor, fur-
Ib)
ther accelerating the colla pse of benthic co mmunit ies.
(b) Dead multi-species' clump covered with marine snow
during an oxyge n crisis. Death of the s po nge or ascid-
ian co re of s uch aggregations also kills the assoc iat ed
fauna, for example cru staceans and polychaetes. (c)
The first recolonization phase is characterized by more
rapid-growing , o pport unistic form s, here by tubeworm s
and the ascidian Ciono. They bear little resemblance to
I')
the typical multi-species' aggregations formerl y found
here. Knowledge about s uch successions provides valu-
able information on past collapses and on the resilience
of these co mmunit ies. Photograph a: Kurt Fedra; pho-
tographs b- e: Michael Stachowitsch .
 8.7 Specific habitats
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Peterson 1998; Cranfield et al. 1999). For example, exten-
sive oyster beds occurred in Chesapeake Bay on the eastern
US coast and in the Foveaux Strait, southern New Zealand
(Crassostrea virginica and Tiostrea chilensis respectively) .
However, in both localities, long-term harvesting has
severely reduced the seabed coverage of oyster reefs.
Reef-building fauna can exert strong grazing pressure
on primary production in the water column through filter
feeding . The removal or degradation of such structures
through harvesting or pollution has led to large-scale
ecosystem changes particu larly in the zooplankton com-
munity.
In the case of Chesapeake Bay it was estimated that the
oysters filtered the entire volume of the water body every
day. With such a large turnover ofwater volume it is not dif-
ficult to understand why the ecology of water bodies such
as Chesapeake Bay might be changed by reducing oyster
reef biomass. These reefs act as a sink for phytoplankton
production and transfer this biomass from the pelagic to
the benthic system. In addition to their role in transferring
energy to the seabed, biogenic structures greatly contrib-
ute to marine habitat complexity by increasing the three-
dimensional relief of seabed topography and often have a
nursery function for juvenile fishes and crustacea. In the
case of fauna that provide a hard surface, such as bivalves
and tubeworms, the reef structure may provide a settle-
mentsurface forepibiota such as algae. soft corals. sponges.
tunicates, hydroids, and bryozoa, which further contribute
to the processing of water borne particulate matter. Reef
structures represent irregular features on the seabed and
consequently affect flow around and over them. Erosion
due to currents will be greatly reduced in the interstices of
the reef matrix, which creates the right conditions for depo-
sition of faeces and other organic matter that fuels produc-
tion of the associated benthos and microbial communities
(Lenihan & Peterson 1998).
As biogenic reefs are constructed primarily of living
organisms, they are particularly vulnerable to physical
disturbance, fishing, or pollution effects associated with
eutrophication. The initial establishment of reefs depends
upon the chance settlement of a cohort of recruits coupled
with favourable environmental conditions. Hence restor-
ing degraded reefs is fraught with problems and prone to
failure. Restoration is further complicated when the reef-
building organisms are slow growing, as in the case of the
calcareous algae known as maerl. Maerl grows at a rate of
about 1 mm ;r1into twiglets and branches that interlock
to form a living sediment matrix. This open matrix has
large interstitial spaces that permit deep penetration of
oxygenated water into the maerl substratum. Maerl is also
associated with the reef-building bivalve Umaria hians,
which constructs 'nests' of shell debris and other material
attached to its byssus threads and can form beds at den-
sities of more than 700 individuals m~2 within the maerl
matrix (Hall-Spencer & Moore 2000) . This bivalve is scarce
in any other type of habitat and hence is highly vulnerable
to environmental impacts that might adversely affect the
maerl habitat. Maerl habitats may also be threatened by the
consequences ofocean acidification due to their calcareous
structure.
Some reef-bui lding biota can be many hundreds of years
old and hence they are particularly vu lnerable to any
form of disturbance.

Chapter Summary
• Continental-shelf systems account for approximately SOfo of marine habitats yet they are t he site
of much of the ocean's global primary production that ultimately fuels major world fisheries.
• Shelf systems are relatively young on a geological scale, with large changes in the extent and posi-
tion of the coastal margin occurring during the last glaciation event. Drowned river deltas, glacial
lag deposits, and glacial scour are features of the current continental shelf seabed.
• Tidal currents generate turbu lent flow as they move across the shallow seabed areas of the shelf
close to the coastline. This turbulence generates mixing throughout t he water column and prevents
thermal stratification, and enhances the flow of material to the seabed and hence benthic produc-
tion. Further offshore in deeper water, stratification occurs and leads to t he development of fronts
at the interface with mixed water masses.
• The world's continental-shelf systems can be categorized into regional ecosystem types according
to the prevalent environmental conditions that impinge upon t hem and characterize t he timing of
the spring/summer phytoplankton bloom that fuels shelf food webs.
Chapter 8 Continental Shelf Seabed

• The flora and fauna of the continental shelf seabed system can be subdivided accord ing to their
fu nctional role (e.g. predators, herbivores) and ecosystem function (e.g. ecosystem engineers, sedi-
ment processors, habitat formers). Large-scale population changes in key species can lead t o effects
on other trophic levels in some relatively simple systems.
• Early marine ecologists attempted to categorize particular assemblages of species that occur on
continental shelves. However, it is questionable w hether t his approach is useful given the infinite
number of possible variants created by the substit ution of one species for another and the likely
large-scale changes we will see w it h current trends in global ocean warming.
• Seabed habitats can be categorized according to the characteristics of the substratum (hard or
soft-sediment). The physical characterist ics of soft-sediment habitats are indicative of t he physi-
cal energy that affects the seabed, with mud occurring in low energy environments, while coarse
sands occur in tidally swept areas exposed to wave action. Some habitats are com posed of living
biota such as kelp fo rests, maerl beds, and oyster reefs t hat are critical links with their associated
communities of organisms.

Further Reading
Dayton (1994) discussed the issues of scale and stability in hard bottom marine communities, whi le
Snelgrove and Butman ( 1994) review the debate on the relationship between animal assemblages and
soft sediment habitats. Hall (2002) assesses the major impacts t hat affect present day shelf systems.
• Dayton, P. 19 9 4. Community landscape: scale and stability in hard bottom marine communities. In P.
Giller, A. Hildrew, & D. Raffaelli (eds) Aquatic Ecology: Scole, Pattern and Process. Blackwell Scientific
Publications, Oxford, pp. 289-332.
• Gray, J. S. & Elliott M. (2009) Ecology of marine sediments: from science to management. Oxford
University Press, 225 pp.
• Hall, S. J. 2002. The continental shelf benthic ecosystem: current status, agents for change and future
prospects. Environmental Conservation 29: 350-74.
• Snelgrove, P. & C. Butman. 19 9 4 . Animal-sediment relationships revisited: cause versus effect. Ocean-
ogrophy and Marine Biology: An Annual Review 32: 1 11 - 77 .
 The Deep Sea
Chapter Summary
The deep-sea floor represents the largest, yet least-known,
habitat on eart h and ranges from the edge of the cont i-
nental shelf at 200 m depth, down to the abyssal plai n 5
km below the surface, w ith tren che s pl unging to 10 km
in places. The environment is remarkab ly constant across
the ocean floor: col d, dark water overlying soft, deep mud.
While the high hydrostati c pressure is th e most obvious
physical feature of the deep, it is food supply from the sur-
face that is the limit ing factor for life on the abyssal p lain. In
temperate areas, the food inp ut can be seasonal, providin g
cues for reproduct ive cycles. Due to the lack of food , the
community of animals in the d eep sea is of much lower
abu ndance than in shallow wate rs, but some organisms can
grow considerably larger than the ir shallow-water relatives,
s uch as 2 5 cm s ingle-celled organisms! Pote ntia lly the re
9.1 Introduction
The deep ocean represents the largest habitat on the planet.
yet remains the least known; humans have landed on the
m oon, but due to conditions inhospitable to humans. no
one has yet set foot on the deep-ocean floor. The kilometres
of wate r separating us from the abyssal floor prevent much
remote sensing of the bottom features. As a result, even the
topography of the world's seabed is not fully documente d ,
and the life that is found there is even less well-documented.
Therefore , unlike other h abitats in the m arine re alm, the
stud y of deep-sea organisms has been exceptionally difficult
and our knowledge of how the deep sea functions has, until
recently, had to be pieced together from samples representing
a tiny fraction of the ocean floor. The total area of quantitative
mud samples taken so far from the deep sea is only abo ut sao
are mi ll ions of s pecies inhabiti ng the deep-sea benthos;
the main grou ps of large, mob ile organi sms are echino-
derm s, decapod crustaceans, and fi sh, many of which show
remarkable adaptations to deep-sea life. Recent exploration
using s ubmers ibles has revealed exciti ng 'island' habitats
in the deep sea with a leve l of producti on and diversity
higher than the surro undi ng e nv ironments. These incl ude
hyd rothermalvent communities, which are powered by pro-
duction from chemosynthetic bacte ria and are practically
independent of s unli ght. Vents have a unique, re markable,
and productive assoc iated fauna, incl udi ng huge vestimen-
tife ran wo rms that have no mouth or gut, but rely on vast
populations of bacteria within the ir bodies, and the Pompe ii
worm that lives in water temperatures above 60°C- the
most thermotolerant animal so far discovered.
square metres- perhaps a millionth of the total seabed area
(see www.sams.ac.uk) . Only the development of submers ibles
in recent decades has led to a more vibrant view of deep-sea
ecology and enabled the discovery of some of the most excit-
ing and fascinating habitats on ear th . However, the dark, cold
depths of the abyss still generate a sense of the unknown that
has resulted in varied descriptions of deep-sea environment
from a complete ly lifeless re alm to one occupied by strange
monsters, epitomized by books such as John Wyndham's The
Kraken Wakes . The truth lies somewhere in between, and the
aim of this chapte r is to detail the enviro nment that exists on
the ocean floor. the problems facing organisms living there,
what these organisms are , and how they are distributed; and
to explore some of the astonishing 'island' habitats that have
more recently been discovered within the deep sea.
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
9.2 Definitions and
environmental features
9.2.1 What is the deep sea?
The definition of 'the deep sea' is relatively vague, but
generally represents all the water and seabed beneath the
edge of the continental shelf (Fig. 9 .1; this shallow area
being termed neritic, see Fig. 7.3) . Generally, this bound-
ary tends to be at a depth of about 200 m, so the deep sea
can be regarded as any water or benthic habitat situated
below 200 m . The deep-sea benthos can be divided into
separate depth regions that refer to the general topogra-
phy of the ocean floor that is generated as a consequence
of plate tectonics. At the edge of the continental shelf is the
shelfbreak, where the gradient of the floor increases down
the continental slope. This can be exceptionally steep at
many continental margins (e.g . off the south-west coast of
the British Isles) and, if visible, would be among the most
impressive natural features on earth . In such areas. the
slope can extend downwards from 200 to 4000 m, but more
often the gradient is less dramatic, and the steep slope gives
way to a gentler continental rise between 2000 to 5000 m .
At around 4000 to 5000 m, the ocean floor is reached and
extends over the ocean basins at depths generally around
5000 m (the abyssal plain) . The benthic area associated
with the gradient from continental shelf to abyss is known
as the bathyal region (though some definitions end this
region at a depth of about 2 Ian), the area on the sea floor
is termed the abyssal region.
Early attempts to map the ocean floor relied on extensive
extrapolation from the few sonar transects that were avail-
able. For example. the famous three-dimensional maps of
the ocean floor produced in the late 1960s (published in
National Geographic magazine) relied on relatively few
transects across the ocean (Kunzig 2000). the topogra-
phy between them was inferred by an artist's impression .
Consequently, these early diagrams illustrated the abyssal
plain as generally a huge, flat expanse-an image that has
persisted in the minds of both professionals and amateurs.
However, more recent detailed work in certain parts of the
Sea level
/ I
(ontinentol.helf :i
Continental slope ~
9-
(ontlnenfa
. I'me /
-;1
Sea mount Abyssal plain
Figure 9.1 A hypothetical cross-section of an ocean basin indicating the main topographical features of the deep sea
and terms used for areas of the deep-sea floor. Vertical scale is much exaggerated.
world has revealed the abyss to be far less uniform, with
many small topographical features resulting in 'rolling hills'
rather than plains. Additionally, such smaller-scale studies
have revealed the existence of many sea mounts. which
rise from the ocean floor but do not break the surface (Fig.
9 .1) . In original maps that extrapolated from known points,
it is clear that such features would be missed. but these
have recently been found to host fascinating and diverse
communities (de Forges et al. 2000) . Other features of the
ocean floor are much larger and well known and coincide
with areas of generation or subduction (one crust mov-
ing under another) of the oceanic crust. The abyssal plain
does not extend across the whole Atlantic ocean basin. but
is interrupted by a long chain of mountains known as the
mid-ocean ridge (Fig. 9.1, Chapter 1) . The ridge is the site
of the formation of ocean crust. which spreads out evenly
on each side (meaning the Atlantic is getting wider), and
therefore can also be the site of intense volcanic activity
that results in hydrothermal vents (9.5) . Trenches in
the ocean floor (Fig. 9 .1) occur where plates meet and the
ocean crust buckles and deepens as it moves beneath an
adjacent plate. These trenches represent the deepest parts
of the sea and can extend down to 10 000 m . The deep-
est point of all is the Mariana Trench off the Philippines
(10912 m) . The bentltic area within a trench (a depth of
between 6 000 to 10 000 m) is known as the hadal region.
9.2.2 Problems with sampling the
deepsea
Despite being the world's largest habitat, the ecologyofthe
deep-sea floor is the least understood due to inherent prob-
lems of sampling (Chapters 7 and 15). Traditionally, our
knowledge of the organisms of the deep has been pieced
together from the contents of comparatively few remote
trawls, grabs, and dredges that have been hauled up from
the depths. Piecing together the ecosystem on the abyssal
floor, or even how animals live their lives. from such sam-
ples is extremely difficult (if not impossible) and involves
considerable guesswork. To comprehend how difficult such
an exercise is. sampling the deep sea has been likened to
c
-es
~
AbJ'Sll1 5
I
Mid-ocean ridge
I- Trench
6
7
 9.2 Definitions and environmental features
sampling the rainforest by flying a plane above the clouds,
pulling a net through the trees and constructing the system
from the contents of the net. This would clearly be ridicu-
lous, but it is how deep-sea biologists have had to work. In
recent years our means of investigating the deep sea has
improved dramatically, first by the use of photography and
particularly by the development of manned submersibles.
For the first time scientis ts can actually see what the organ-
isms are like in their natural surroundings .
However, even taking a trawl from the sea floor is excep-
tionally difficult and requires a scale of sampling unnec-
essary fo r the rest of the marine realm. To pull a trawl or
dredge along the abyssal seabed at a depth of 5000 m would
require nearly 11 000 m of wire ; considering the oceanic
conditions involved a large ship is required. Additionally,
knowledge of the location of the trawl is vital to know it is
actually on the seabed, so sophisticated acoustic devices are
required . Deep-sea sampling is therefore very expensive and
prone to failure, even for the collection of the most basic of
samples; simply placing and retrieving a sampling device on
the deep sea floor takes hours rather than minutes.
As well as traditional gea r, much of our knowledge of
life on the ocean se abed, particularly detail of m egafaunal
anim als, is from photography. Two main types of cam era
TECHNIQUES: Stills image and video
sampling in the deep sea
Dr Kerry Howell (Mari ne Institute, University of Plymouth)
discusses some of the latest advances and applications
of imaging techniques in the deep sea. In the past our
knowledge of life on the deep-sea bed was li mited to
w hat could be broug ht up in a t rawl or box core. While
th is provid ed us wi th a basic understanding of species
composit ion, distri bution, and abundance in the deep, it
told us very little about t heir relationship w ith their envi-
ronment. Advances in technology now allow us to use
cameras to observe deep-sea organisms in situ (see fig-
ure a) , provid ing us wi th new insights into the ecology
and behaviour of the deep-sea benth os.
The use of photography and video as sampli ng tools
is growing rapidly, and t he range of systems used is
immense. Some of the more well-known and established
systems include rem ote ly ope rate d veh icles (ROVs) ,
auto nom ous unde rwate r vehicles (AUVs), landers,
manned submersibles, and towed photography and vid-
eog raphy frames (sledges, drop frames) (for review see:
Solan et al. 2003; Coggan et al. 2007). Essentially all
use mounted video and/ or st ills cameras to sample the
deep-sea benthos.
have been employed since the 1980s. Originally, cameras
with open shutters were mounted on sampling gear such as
benthic sleds; the film-winding mechanism was connected
to the flash unit. The camera therefore recorded the seabed
before the sampling gear moves over it (Fig. 9 .2a) . Alter-
natively, stat ionary photographic gear has been dropped to
the seabed-basically a frame with a camera mounted on
it known as a bathysnap (Techn iques box). Photographs
were taken at certain intervals (e. g. 1 hour, 1 d ay) and the
gear is left on the seabed often for months. The camera was
retrieved by transmitting an acoustic signal to the seabed ,
which released weight s attached to the camera mount,
and the bathysnap floated to the surface to be retrieved.
Such series of images gave us important information on the
dynamics of the deep-sea bed . Cameras (still or video) ca n
also be deployed with bait attached to the frame (e .g. a fish
carcass) in order to attra ct and photograph scavenging ani-
m als (Fig. 9.2b) . Suc h pieces of sampling ge ar were fondly
known as bathysnacks ! More recently, suc h underwater
observation has moved on with the use of digital and high
definition vide o and st ills camera technology, allowing
quantitative analysis of the sea floor and some beaut iful
pictures that bring the deep to life (Fig. 9.2c, Techn iques
box).
(a) Sea-spiders mating at 900 m depth on the Wyville-
Thomson Ridge. Photograph: Crown Copyright BERR/Defra.
Lande r systems are stat ic and deployed on the sea-
bed . They te nd to be use d to study temporal changes
in communities or physiological / behavi ou ral ecology. The
Bathysnap system (Lam pitt & Burnham 19 8 3), consisting
of a downw ard-facing stills camera mounted on a frame,
can be deployed for one year or more on the seabed, tak-
ing images at set t ime-intervals, provi ding information on
 Chapter 9 The Deep Sea
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changes occurring at a site over time. This system was
pivotal in providing evidence of a seasonal pulse in the
food supply to the deep sea in the form of marine snow
(see 9.3.5; Billett et al. 1983). Baited landers, equipped
with video cameras trained on the bait, have been used to
study swimming speeds, tail beat frequencies, and escape
respo nses of deep-water fish (Bagley et al. 19 9 4 ; Bailey
et al. 2003).
Beyond Lander systems, all other systems tend to be
used to study distribution, abundance, and organism-
environment relationships. Towed camera systems are
relatively inexpensive and include drop-frame systems
that are suspended in the water colum n up to 10 m off
the bottom, bed-hop systems that are hopped up and
down over the seabed, and sledge systems that are towed
along the seabed (figure b). These systems tend to be
towed along straight transects of predetermined length
providing strips of video of the seabed and/or 'quadrat'.
like stills images along those transect lines. ROY, AU\/,
and manned submersi ble systems may be driven along
more complex tracks, although still providing (albeit not
straight) strips of video of the seabed and associated
stills images. Images may be quantitatively analysed to
provide estimates of species' abundances. Video data
tend to be used to provide semi-quantitative, or qualita-
tive, information on species' abundance, habitat charac-
teristics, and organism behaviour, although increasingly
researchers are looking to obtai n quantitative data from
video, as digital and high definition techno logy improves.
Such systems have been used to map the distribution of
species and assemblages in various deep-sea ecosys-
tems, such as hydrothermal vents (Sarrazi n and Juniper
(b) A typi cal drop-frame system used for video and
image survey. Photo: Kerry Howell.
•
•
- •
. -
•
(c) A North Atlantic codling , sheltering behind a ro ck
at 500 m depth o n Hatton Bank. Image Crown Copy-
right BERR/Defra.
1999), cold seeps (Olu et al. 1996), canyons (Hecker
et al. 1988), and sea mounts (Lundsten et al. 2009), as
well as to study fish-habitat associations and behaviour
(Uiblein et al. 2003; Lorance and Trenkel, 2006; figure c) .
While video and image sampling provides us with a new
dimension to deep-sea research, its use is not wi thout
pitfalls. The key downside to this type of sampling is the
lack of physical samples. Where some species are easily
identified from video and image data, many require physi-
cal samples to firmly establish identifications. Frequently
the use of 'morphospecies ' must be employed in order to
interpret the image and video data. The various platforms
available can rarely be towed at a constant speed or at a
constant height above the seabed, making interpretation
of data and comparisons between tow s and areas chal-
lengi ng-two lasers are regularly used with such gear to
provide consistent scale in the resulting images. Video
data are often of low quality compared to the stills came ra
data, and integration of these different data is difficult In
recent years the use of high-definitio n video in benthic
sampling has improved both our ability to identify species
from video data and obtain quantitative data from video
through allowing high-quality frame grabs of a given size
field of view. As technology has moved on, there is no
doubt that video and image sampli ng is becomi ng an
effective, accepted, established method of sampling the
deep-sea, with equal po tential in shallow water.
 9.2 Definitions and environmental features
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 9.2 Photographs of organisms on the deep-sea floor: (a) and (b) taken during the 19805, (c) a more recent
dig ital image. (a) A red crab Geryon trispinosus reacting to the approach of a photosled. (b) A 'bathysnack' photo of the
spider crab Neolithodes attracted to bait. (Copyright National Oceanographic Centre, Southampton). (c). The deep-sea
coral reef Lophelia with an associated squat lobster (photo: NOAA).

The most expensive, but enlightening, method of sam-
pling the deep sea is the use of manned submersibles, such
asAlvin, Shinkai 6500, and Nautile (Fig. 9.3) . Certainly our
understanding of how the deep-sea system functions has
progressed in leaps since the extensive use of submersibles
for observation, sampling, and even experimentation, with
scientists now able to set out experiments on the ocean floor
and record the response of organisms in real time. Deter-
mining the ecology of deep-sea vents, for example, would
never have been possible by using remote sampling tech-
mques.

Figure 9.3 Examples of submersibles used to explore the deep sea.

(a) Alvin, (b) Johnson Sealink (both photos: NOAA), (c) Nautile (photo:
IFREMER).
 Chapter 9 The Deep Sea
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9.2.3 What is the environment like on
the abyssal plain?
The deep abyss is clearly very different from all ot her
marine habitats, but how is that reflected in the physical
and che mical environme ntal parameters that influence
organisms? Other chapters have demonstrated that single
variables can have a large influence on the distribution of
organisms within a system (exposure to air on intertidal
shores, salinity in estuaries). Therefore, it is important to
review the cond itions in the deep-sea floor (at 5000 m)
CURRENT FOCUS: Carbon capture and
storage in the deep sea
Perhaps the most pressing issue facing the world today is
creating global sustai nable energy generation that does
not produce further greenhouse gases, the aim being to
reduce CO 2 emissions and th us the concentration of such
gases in the atmosphere in an effort to combat global
climate change. Burning fossil fuels such as coal, gas, and
oil, has been the pri me method of energy generation, cre-
ating the at mospheric build up of CO2 ; for example, 96%
of carbon emissions from 199 1 to 2000 resulted from
usi ng fossil fuels for ene rgy (US EPA 2002). Therefore,
a focus of more recent energy development, particularly
in developed cou ntries, has been on renew able energy
sources (such as wind, solar, hyd roelectric, and tidal) and
new-generation nuclear power. There is an impending
problem, however, of how we generate enough electric-
ity in the near futu re, as old fossil-fuel powe r stations and
nuclear installations are decommissioned, yet renewable
technology and the construction of new nuclear stations
is not ready to fill the energy generation gap. In the UK,
for example, there is concern of potential energy short-
ages by 20 15-20 due to th is gap in provision. One w ay
to cou nter such a problem, and to help com bat cli mate
change, is if we can remove the CO2 from power stations
burni ng fossil fuels and lock this away somehow, prevent-
ing it reaching the atmosphere. This approach is known as
Carbon Captu re and Sto rage (CCS) and with developing
technology could provide a major contribution to reducing
emissions, particularly in countries such as China cu r-
rently reliant on burning fossil fuels. One problem is what
to do with the CO2 once it is captu red; one solution is to
store it in the deep ocean.
A number of technologies are cur rently available for
capturing CO, (see http://www.be llo na.no) and this can
be done either post-co mbustion ('end of pipe' separation
using chemical cleaning through an absorbent removing
80-90% of CO, ). pre-combustion (90% of CO, removed
from fuel before burning) , or by using oxy-fuel com bus-
to determine which parameters potentially influence the
organisms found there (Gage & Tyler 1991) . Some param-
eters vary little below 2 000 m ; for example , salin ity is rela-
tively consta nt at 34.8 + 0 .3, whilst pH is fairly constant
below 2000 m around 7.7-7.8 (Dore et aI2009 ), raising
concerns about potential deep-sea impacts of ocean acidifi-
cation, particularly plans to capture CO2 and store it in the
deep sea (Current Focus), as cur rently no change in pH has
been apparent at such depths (Dore et aI 2009).
tion (oxygen is used du ring burni ng instead of ai r so
the exact amount can be regulated, which aids removal
of 100% of CO, in the flue). If suitable storage can be
found. CCS. if fully implemented, can potentially captu re
236 b illion tons of CO2 , correspondi ng to a 33% reduc-
tion in global emissions by 2050 compared with today
(Soloman 2007). So where can such large volu mes of
captured CO 2 be stored?
Storage (or seq uestration) of CO 2 is much mo re
efficient if it can be converted into liquid: th is can be
achieved by either cooling or using pressu re. Options
t herefore are to store CO2 either in terrestrial, subter-
ranean aquifers, trapped below rock, or the deep sea;
be low about 800- 1000m CO, has a liquid-li ke density.
Terrestrial sto rage is problematic as the buoyant CO 2 can
migrate upwards through any available conduit (House et
al. 2006), so all such reservoirs must have impermeable
layers and be continu ally monitored for leakage. Disposal
in the deep sea could therefore be preferable and has
three main alternatives: inject the CO 2 into the deep water
itself ('di rect ocean storage'); store it in deep-sea sedi-
ments; or sequestrate the CO 2 in deep-sea basalt aquifers
beneath the ocean floor.
Injection of CO2 into the deep ocean is seen as just
accelerati ng the natural process of CO2 uptake tha t has
resulted in much of the emitted CO2 ending up in the
ocean as b icarbonate rather t han in the atmosphere
(Sabine et al. 2004). How ever, the re are two maj or
concerns that have made this option undesi rable. This
process will cause co mparatively rap id acidification of
the deep-sea with profou nd effects on deep-sea organ-
isms. Experiments suggest that the impact of such dis-
solved CO 2 under the pressures of the deep-sea are more
severe than at atmospheric pressu re, wi th orga nisms
dying quicker and at lower CO 2 concentrations tha n the
surface (Ishimatsu & Ku ri hara 2008). Additionally, this is
not a permanent solution: current circulation will mean a
large fraction of the injected CO2 would be released to
the atmosphere afte r a few hundred years (House et al.
2006).
 9.2 Definitions and environmental features

Permanent storage of CO 2 in deep-sea sedi ments

does seem feasible, as long as the local conditions and
the depth of injection are suitable, as liquid CO 2 can be
denser than the overlying pore water or CO2 hydrates can
be formed to stop CO2 flow and cap the system. House
•
et al. (2006) suggest that injection into water depths of
>3000 m and 300 m below the sedi ment surface results
in permanent storage of th e COz' They also conclud e that
all the CO 2 emmisions of the US can be stored in an 80
km z area, with the US economic zone capable of storing
thousands of years of current US CO 2 emissions.
A further permanent solution is to store CO2 in suitable
deep-sea geological formations, as the deep-sea basalt
provides a vast reservoir of cap acity able to accommo- Schematic of a carbon-capture and storage scheme
date centuries of emissions and, in the US, wi thin pipeline using seabed geological formation s. Adapted with
distances to populated areas on the west coast (Gold- permission from the Bellona Foundation (http:/ / www.
berg et al. 2008; see figu re). In such deep aquifers, the bellona.no).
injected CO 2 would react wi th calcium and magnesium
ions from the basalt, form ing stable carbo nate minerals. field off Norway has been injecting 1 million tons of CO2
For certai n areas of the world, storage of captu red CO 2 a year since 19 9 6 and storing the gas in deep saline
in deep-sea sedi ment and basalt could therefore provid e a aquifers (Solomon 2007).
major method of reducing carbon emissions, whilst fossil
fuel power stations are still being used. Such technology
is al ready in act ion in shallower water: the Sieipner gas

9.2.4 Light
The deep-sea water column can be divided up in terms of
light penetration (see Fig. 7.3). The top layers (euphotic)
h ave enough light for photosynthesis. Down to about 1000
m there is still enough light for some vision (dysphoric
zone) , but below this there is no light at all (aphotic) . The
abyssal plain is therefore very different from practically all
other marine habitats in that no light pene trates the deep
ocean to these depths; the abyss is in permanent dark-
ness. Consequently, photosynthesis is not possible, so no
living plants exist in the deep sea, resulting in a food web
dependent entire ly on energy from detritus and carrion
originating from the systems above (with the exceptio n of
bacterial chemosynt hesis in hydrothermal vents, see 9 .5. 2).
However, many deep-sea organ isms have evolved methods
of generating light using light-emitting bacteria contained
in special cells (biolu m in escen ce ; Box 9. 1) . Th is light
generation in the darkness has many uses, such as finding
m ates of the same species, finding food, and predator avoid-
ance . Scientists in the first submersibles entering these dark
depths were amazed at the extent of the bioluminescence
as organ isms emitted light on contact with the submersible.
9.2.5 Temperature
The temperature of deep-sea water is low and constant.
Below abo ut 2000 m, temperature gene rally ranges
between only - 1' C to 4' C, with the majority of the abyssal
water at around 2°e. As organisms only ever encounter cold
water, m any are killed by the temperature shock as they are
brought to the surface in samples. The minimum recorded
temperature is - 1.9°C beneath Antarctica, where cold water
sinks. However, there are two particular deep-sea areas that
h ave unusually high temperatures. The Mediterranean Sea
h as a very deep basin and water at 4000 m here has been
recorded at temperatures of 14°C, while water at 2000 m in
the Red Sea can be as high as 21.S' C.
 Chapter 9 The Deep Sea
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Box 9.1: Bioluminescence
Bi oluminescence is the light produced by a chemical
react ion w it hin an organi sm. Perhap s the most fam iliar
bio luminescent organisms are fireflies (actually beet les) ,
but li ght product ion is comparatively rare on land and is
much more a feature of the marine environment, w here it
is a relatively common feature. Practicall y all marine taxo-
nomic groups from dinoflagellates to fish have members
that can biolumin esce (producing the light themselves or
using bacteria housed in light organs or photophores) ,
part icularly be low the euphot ic zone in the ocean-for
example, approximately 90% of animals are biolumines-
cent in t he mesope lagic zone. Tw o main chemicals are
requi red to produce bioluminescence: luciferin creates the
light, but require s luciferase, which catalyses t he oxidat ion
of luciferi n resulting in light. Most of t he light is b lue-
9.2.6 Dissolved oxygen
The oxygen content of the water is relatively constant across
the abyssal plain, with a concentratio n of c.S mg 1-1 below
2000 m. Under normal oceanic conditions, the oxygen min-
im u m t ends t o bej ust below the euphotic layer (400 to 500
m ). Some areas of the deep sea have notably low oxygen
levels, due to specific local cond itions, suc h as the Santa
Catalina Basin off California, which consequently ap pears
to have a lower faunal divers ity than comparable nearby
regions suc h as the San Diego Trough.
9.2.7 Bottom currents
Levels of oxygen, and other variables, are kept compara-
tively constant because the deep-sea floor is continually
green in colo ur (generall y in the range 440-479 nm)
as blue light travels furthest in water and most marine
organis ms are sensitive to blue light. Notab le exceptions
are deep-sea malacosteid fish (I oosejaws) , whi ch have
an unusual ability to produce red light (Haddock et al.
2004) . This is achieved through the use of filters and a
fluorescent pi gment insid e the photophore, wh ich takes
the energ y and re-emits it as red light. Generally, fish
cannot see red light, but loosejaw s (e.g. Aristostomias)
have extra photoreceptive p igments, all owing light to be
detected in this range. This predatory fish can therefore
emit light that only it can detect and allows red-coloured
prey to be illuminated (Fig. 7.4) .
Images from http:/ / w ww.l ife sci.ucsb.edu /b io lum / .
Copyright Steven Haddock. See website for more info r-
mation of biolumi nescence.
refreshed by a range of bottom curre nts, which can provide
environmental cues for organ isms (e.g. to direct the action
of feeding appendages, m igration, etc.) . As well as directly
measuring flow, we can see that currents exist from photo-
graphs of, for example, sea anemones whose tentacles are
trailing in a uniform direction. Three main types of curre nt
exist in the deep sea. First, in some parts of the ocean , tidal
currents can reach down as far as the base of the continen-
t al slope (e .g. Bay of Biscay, Eu rope) an d can even f orm
familiar ripple patterns on the deep-sea floor. Tidal curre nts
will change direction, but generally the bottom curre nts
are unidirectional and come from two sources. Second , the
oceanic conveyor (Chapters 7 and 12) is vitally important
for the movement of water and provides constant, unidir-
ectional curre nts in the deep sea. For example, cold, de nse
water sinks at the Antarctic and moves northwards across
 9.2 Definitions and environmental features
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the Pacific above the seabed (Box 12.1) . Third, the Corio-
lis current arises from the rotation of the earth and the
relative movement of water in respect to the seabed. As the
earth spins. the majority ofthe water in the oceans remains
stationary, resulting in oceanic currents (Chapters 7 and
8). However, at the ocean floor, a small layer of water (the
viscous sublayer) moves with the earth. whereas the water
further up the column moves at a relatively slower speed.
The sea floor is therefore moving beneath the water col-
umn, resulting in a current. Due to the scale of the earth's
movement. however, the impression is of the water moving
over the seabed.
9.2.8 Hydrostatic pressure
The most notable, and predictable, feature of the deep sea
is the immense hydrostatic pressure due to the weight of
overlying water. the single most limiting factor for humans.
Pressure increases by 1 atmosphere every 10 m, so on the
abyssal plain it is over 500 atmospheres (d. 4 atmospheres
on a very deep scuba-dive) . At the bases of trenches it is
even greater. An average-sized person standing on the
bottom of the Mariana trench would experience pressure
equivalent to holding up 48 jumbo jets! One consequence of
pressure. as every diver knows. is that it compresses gases,
including the swim bladders of fish. The impact on gas is
illustrated by attaching a polystyrene cup to the outside of
submersibles (Fig. 9.4), the cup shrinking to a much smaller
Figure 9.4 Before and after. The impact of hydrostatic
pressure at 3000 m on a polystyrene cup. All the air in
bubbles within the po lystyrene has been squeezed out,
shrinking the cup size. Photo: Matt Johnson.
size by the impact of pressure squeezing air from the mate-
rial matrix. High pressure can also slow down the rate of
enzyme catalysis.
However, it has to be remembered that, although the
pressure seems severe to us, organisms that have evolved
to live in the abyss do not experience any fluctuations in
pressure, or the other variables discussed above. and so are
not necessarily subject to environmental stress from such
factors. Organisms adapt well to living at extremes; it is
variability in the environment that is particularly hard to
deal with (Chapters 5 and 6) . There is one physical factor
that potentially does pose problems for organisms living on
the abyssal sea floor: sediment.
9.2.9 Sediment
In parallel with the mid-estuary (see 5.1.4), the sediment
across the vast majority of the ocean floor is soft, fine mud,
though at a much greater scale. This soft sediment rep-
resents the world's largest single habitat due to the con-
sistency of the physico-chemical conditions. The mud on
the abyssal plain has been deposited over millennia, and
consequently in some areas can be up to 1000 m thick. so
benthic organisms have to develop strategies in order to
remain above the sediment, such as possessing long stilts,
long stalks of sessile animals, climbing on other organisms,
and flotation methods. As this parameter is probably the
single physical variable affecting organism distribution. it
is worth looking at the sediment in more detail.
Sessile organisms settle as larvae and then can not move
after settlement, e.g. barnacles, sponges, most bryozo-
ans.
Deep-sea sediments can be divided into two clear classes:
clay particles. inorganic sediments found mainly under
oligotrophic surface waters such as mid-ocean gyres; and
biogenic oozes, sediments found below productive sur-
face waters and containing >30% biogenic skeletal mate-
rial. The composition of this biogenic material can vary.
depending on the dominant taxa in the surface plankton,
and two subclasses of biogenic ooze can be identified. Sili-
ceous oozes are silicon based. and are therefore made up
from the skeletons of two main groups: diatoms (whose
skeletons are known as frusrules, Fig. 2.15) and radiolar-
ians (Fig. 1.5f) . Due to the dominance of diatoms in many
ocean regions, siliceous oozes are found beneath diatom-
productive surface waters such as the sub-Antarctic and
central-west Pacific. Calcareous (or Foraminiferan) oozes
are sediments based on calcium carbonate (CaC0 3) and are
composed of the skeletons of two groups of plankton with
calcareous skeletons, namely the Foraminifera (Fig. 1.5g)
and coccolithophores (Fig. 2.20) . As foraminiferans are the
more widespread of these two groups. the sediments are
 Chapter 9 The Deep Sea
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commonly named after them. Coccolithophores can, how-
ever. form massive blooms in surface waters (Chapters 2 and
7; Fig 7.1 Case 1), turning the water a chalky bright blue
colour similarto an alpine river. Calcareous oozes tend to be
found in shallower water than siliceous oozes as the hydro-
static pressure at great depth forces CaC0 3 into solution.
The composition ofdeep-sea sediments is therefore rela-
tively predictable and depends on the productivity and spe-
cies' composition ofthe surface waters. This fall of material
from the euphotic region of the ocean to the deep-sea floor
has major implications for deep-sea life. as we will see later
(9.3), and is unlike the situation on the continental shelf
(Chapter 8) . Hard substrata are very uncommon in the deep
sea, which has consequences for many sessile groups that in
shallow waters tend only to be found on reefs. Examples of
exposed rock, or other hard material, include hydrothermal
vents (9.5), sea mounts, steep slopes where sediment can-
not settle (such as trench walls or mid-ocean ridges), beds
of manganese nodules, and whale skeletons. On death, the
bodies of whales fall to the ocean floor, where scavengers
quickly remove the tissues and leave the skeleton. The
bones appear to remain for a long period of time, forming
an important 'island' habitat for a high diversity of organ-
isms (Fig. 9.5; Baco & Smith 2003), including those gener-
ally found only on hydrothermal vents. It is possible that
whale skeletons provide an importantstepping stone for the
dispersal of vent organisms (and others) as the bones con-
tain sulphurous compounds necessary for chemosynthesis
(9 .5.5) . It has been estimated that whale skeletons may
be on average only 9 km apart across the deep-sea floor.
This distribution may have been modified by the whaling
industry, both by removing whales and in dumping flensed
skeletons regularly in certain areas .
In conclusion, the environmental variables discussed
here do not vary greatly and therefore do not have as dra-
matic a controlling influence in the deep sea as in other
marine systems such as estuaries and rocky shores. To
discover what may be the major limiting factor for abyssal
organisms we have to look at biological variables.
9.3 Food supply to the deep
sea
9.3.1 Production in the deep sea
As light is absent on the abyssal plain, no photosynthesis
occurs. The ocean floor is therefore one of the few major
habitats in the world where living plants are absent and
thus the deep sea does not have a direct input from the pri-
mary production underlying the majority ofthe world's eco-
systems. A different form of primaryproduction does occur
in some isolated parts of the deep sea : bacteria associated
with hydrothermal vents (9 .5) using sulphur compounds
to fuel chemosynthesis (Box 9 .2) . However, the organ-
isms occupying the vast majorityof the ocean floor have no
direct input from primary production, but instead have to
relyon the input oforganic material from the euphotic layer
of the ocean, mainly in the form of particulate organic
matter (POM) . The deep-sea bed is therefore an entirely
allochthonous system. Only about 1 to 3% of the surface
net primary production reaches the abyssal seabed (Gage
& Tyler 1991) and is the food supply for the whole deep-sea
system away from hydrothermal areas. Therefore, food sup-
ply is the major limiting factor for deep-sea organisms and
is the main reason there is a comparatively low abundance
and biomass of animals on the ocean floor.
Allochthonous systems rely on the input of organic mate-
rial from outside the system, compared with autochthon-
ous systems that mainly generate their own production.
Figure 9.5 Deep-sea hagfish
on a whale skeleton. Copyright
NOAA.

Box 9.2: Chemosynthesis at
hydrothermal vents
Microb iolog ists first uncovered chemosynthesis In
the late-nineteenth centu ry, but until t he discovery
of hydrothermal vents it was cons idered to play no
significant role in the photosynthesis-dom inated car-
bon cycle of the Earth (van Dove r 2000). Chemo-
synthesis is a significant microb ial process involved
in seawater sulphur cycling. Organic matter is con-
sumed by sulphate-reduc ing bacteria (generally in
the absence of oxygen, such as in anoxic sediments),
converti ng sulphates to sulph ides. This product can
then be subject to microbial oxygenation, resulting in
the generation of organic compounds:
5'-(sul phide) + CO, + a, + H,O -> 50~- +
[CH,OI (org anic materia l)
However, when this process occurs away from vents
there is no additional organic material form ed, si nce
organic carbon is bei ng oxi dized to generate the sul-
phid e in the first place. At vents, new suppl ies of
sulphide are being generated from the geochemical
interaction of seawater and heat, allowing a net gain
of organic compounds an d accumulation of new bio-
mass. The process was termed 'chemosynthesis' to
give a direct comparison with 'photosynthesis', but
should be more thoroughly described as 'ch emo-
autolithotrophy' (van Dover 2000). If this seems a
mouthfu l, animals (such as those at vents) utilizing
chemosynthesis are ter med 'ch emo het eroo rgano-
trophs '.
9.3.2 Dissolved organic matter (DOM)
While the most important food input is from paM , DaM
m ay have an important role in providing carbon to sed i-
m ent-dwelling organisms. Measu re ments of interstitial
water have shown that DOM in deep-sea sediment can
be 10 times that of the overlying water and it is suspected
that some large an im als (such as vesti mentiferan worms
and some polychaetes) derive a significant proportion of
their carbon from DOM sources. However, DOM is created
mainly from the metabolic processes of metazoans, bacte-
rial action, and decay, so it is primarily a reworking of car-
bon that has been de rived from external sources .
9.3 Food supply to the deep sea
9.3.3 Large food falls
The whole bodies of dead an imals and large fractions of
plants can sink intact to the oce an floor and provide a foo d
source for a suite of scavenging organisms, suc h as amphi-
pods, brittlestars, and fish (in particular hagfish; Fig. 9.5
and rat-tails Fig. 9.lOb) , which may be attracted to feed on
the amph ipods. Fish, whale, and squ id carc asses rapidly
attract a range of large scavenging animals, as witnessed
by baited cameras (Jones et al. 1998) , and it is clear that
such animal food falls are the prime resources for a range
of deep-sea an imals. However, the appearance of a carcass
on the ocean floor is an unpredictable and sporadic event,
so scavengers have to be able to respond to, and m ake the
most of, any food fall that occurs. In particular, these organ-
isms may h ave to endure long periods between meals and
so some scavengers have become particularly adept at gorg-
ing. The giant amphipod Eurythenes (9 .4.11; Fig. 9 .6) may
be able to eat up to 75% of its body weight (Hargrave et al.
1994), enough to sustain a mature female for over a year.
While suc h amph ipod species appear to have adapted to
feed on carrion, animal carcasses do not form the sole food
source for the majority of fish species that appear when bait
is provided, but provide important ene rgy subsidies that are
rapidly exploited . Initially it was proposed that some fish
that quickly appear on bait, such as rat-tails, would demon-
strate a 'sit and wa it' strategy, as this would be more energy
efficient than constant foraging. However, when ra d io
transmitters were placed in bait (Priede et a1. 1991 ; see also
Techniques box in Chapter 10) it was found that these fish
are active foragers and the food fall is dispersed over great
distances as faecal deposits.
Large food falls of plant material also provide an impor-
tant carbon supply to the deep-sea floor. This can be from
the shallow water m arine environment, in the form of
Figure 9.6 The giant deep-sea amphipod Eurythenes
gryllus which can grow up to 140 mm long
(photograph: Bruno Danis).
 Chapter 9 The Deep Sea
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algae and seagrass, or plants that have been washed from
terrestrial regions. in particular woody debris. Fruit such
as mangos have even been recovered from the deep-sea
floor. Terrestrially derived material is often comparatively
unimportant in coastal marine systems (e.g. estuaries; see
Chapter 5), despite its large biomass, due primarily to the
lack of marine organisms able to process the cellulose and
lignin present in terrestrial matter. In some deep-sea areas
wood can be commonly encountered. such as in trenches
and basins in the Caribbean, and seems to be a key source
of carbon for some species.
In particular. wood is processed by boring bivalves
(Xylophagainae; Fig. 9.7), which convert it to faecal pel-
lets. making it available to other organisms. It appears that
such species have symbiotic bacteria in their gills that can
digest cellulose (Distel & Roberts 1997), although they lack
the dense populations of gut bacteria found in termites. for
example. It is an indication of the importance of woody
debris in the deep sea that this feeding strategy is apparent.
Experiments set up by submersibles using wood structures
for settlement. etc., have been ruined by deep-sea animals
eating the wood, while wood has also been suggested as an
important stepping stone for the dispersal of vent organ-
isms (Distel et al. 2000) .
Both terrestrial plant material, and floating seaweed such
as Sargassum floating within the Sargasso Sea in the west-
ern Atlantic. can provide a seasonal input to the deep sea
associated with storm seasons such as the monsoons. In the
case of Sargassum, storms during the hurricane season burst
flotation bladders, resulting in plants sinking to the abys-
sal floor below. The discovery of such seasonal inputs has
major consequences for deep-sea animals and has altered
our perception of the deep sea as a never-changing. season-
less system (9.3.5) . This is much more apparent when the
main input of food material to the deep sea is considered.
Figure 9.7 A block of wood retrieved from the deep-
sea containing the wood-eating boring bivalves from the
family Xylophagainae (photo: Meg Daly).
9.3.4 Particulate organic matter (POM)
from the euphotic zone
The importance, and temporal patterns. of comparatively
amorphous POM falling to the seabed from the ocean sur-
face layers was quantified in the 1970s and 1980s using a
combination ofsediment traps and long-term photographic
records (Billett et al. 1983; Lampitt 1985). The results of
these studies provided one of the most important discover-
ies in marine biology that has changed the way we view the
deep sea. Some dead, or dying, material from the plank-
ton falls through the euphotic zone without being recycled
(most organic matter is degraded in the water column) and
sinks to the deep sea. This material can be categorized into
three main groups: faecal pellets (primarily from copepods
and includes partly digested matter and bacteria), moults
(the hard parts of the plankton, including dead intact small
organisms). and. in particular. amorphous aggregates. This
latter category has been termed 'marine snow' (or phytode-
tritus) as it is flocculent organic material that falls through
the water column to the seabed and is from a range of
sources. in particular gelatinous animals (such as salps),
bacteria, and the remains of diatoms. The aggregates are
also comparatively rich in protein, trace metals, carbohy-
drates, and lipids. An important feature of marine snow is
that as it falls it 'scavenges' other particles. and so the size
of each aggregate increases with depth. This has the effect
of speeding up the sinking rate, so that the organic matter
reaches the sea floor much more quickly than individual
particles and can avoid decomposition in the water column.
This input ofPOM is the prime supply ofcarbon to the deep-
sea benthic ecosystem.
9.3.5 Timing of food inputs to the
deep-sea benthos
Primary production in the euphotic zone of temperate and
polar areas is highly seasonal (Chapter 2), with the major
temperate bloom occurring in spring. Therefore, the major-
ity of phytodetritus sinking out of the upper layers of the
ocean occurs during these blooms. Due to the aggregation
of particles, sinking rates for most material are around 100
m d- l (rather than perhaps 2 m d- l for a large individual
phytoplankton), so organic material would take between
1 to 2 months to reach the abyssal sea floor. Using primar-
ily long-term photographic records of one portion of the
deep-sea floor, the pattern of phytodetritus arrival has been
determined. In the temperate Porcupine Sea Bight, mini-
mal amounts of organic matter can be seen on the sea floor
during May and June. However, during late June the floor
starts to become covered in dark phytodetrital 'fluff, which
builds up rapidly during July until it is covering practically
the whole seabed (Lampitt 1985; Fig. 9 .8) . The input of
material begins to decrease and the organisms on the sea-

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
~
Ol
1 ../
-i
~
o
~ Work on organisms in the Porcupine Abyssal Plain. and
~
~
~
."
€~
o
a (Fig. 9 .9). Five species of echinoderm were found to show
, , , remarkable reproductive synchrony, all producing small
May June July
Figure 9 .8 Seasonal deposition of phytodetritus onto the
ocean floor (4 km depth) of the Porcupine Sea Bight.
bed rapidly respond to the food supply, the detritus being
quickly removed into the deep-sea food web. By mid-August
much of the seabed is again clear. Practically all material is
taken up by either microbes or metazoans, and so does not
become incorporated into the sediment. Animals feeding on
the sediment (e.g. holothurians) therefore have to process
vast quantities in order to extract sufficient organic material.
The input of food therefore provides a strong, regular,
and predictable seasonal signal for deep-sea organisms in
what is otherwise a seasonless. unchanging environment.
This has allowed the biology of deep-sea organisms to be
viewed under a different light, with the potential for life
strategies and breeding cycles to have developed in order
to correspond to, and maximize the use of, this seasonal
input of food . Several species appear to have r-selected
characteristics (thought unlikely in the deep sea) and have
populations that directly respond to the input of detritus.
Figure 9 .9 A female deep-sea spider crab, Neolithodes,
carrying an egg mass. Crabs hold their abdomen under
their body, compared with lobsters, which have a straight
'tail', the female abdomen being much larger and hairier
than the male's enabling it to carry the eggs (photograph:
Craig Cary, University of Delaware College of Marine and
Earth Studies and Delaware Sea Grant).
9.4 The organisms of the deep sea
These tend to be small. opportunistic organisms such as
foraminiferans, nematodes. and copepods; foraminiferans
such as Alabaminella becoming the dominant species after
the arrival of the phytodetritus (Smart & Gooday 1997) .
other areas, in recent years has demonstrated that many
species. such as isopods, bivalves, and echinoderms. dem-
onstrate seasonal maturation ofovaries and egg production
planktonfeeding larvae in January or February, the larvae
reaching surface waters in time for the spring phytoplank-
ton bloom. Such reproductive strategies do still remain
unusual in the context of the whole deep-sea and reflect
evolutionary developments in areas where such strong sea-
sonal signals exist. For much of the rest of the ocean floor,
megafaunal organisms reproduce throughout most of the
year and tend to produce large eggs with a lot of yolk, indi-
cating more direct or abbreviated development.
r-selected species have generally fast generation times,
short lifespans, and mature early. They are commonly
found in disturbed or rapidly chang ing areas and survive
in these cond itions as successive generations. The alterna-
tive (k-selected) are long-lived, but competitive, organisms
that rely on stable conditions to survive and reproduce.
Such stability is clearly a feature of the deep sea.
A further consequence of the increase in sinking rates
of material is that comparatively large amounts of food
arrive on the ocean floor at specific times during the year,
rather than a continual low input of food. This also means
that there is a vast difference in the amount and timing of
food supply across the ocean floor. Deep-sea areas in tropi-
cal regions with minimal seasonality within the plankton
will not experience large, seasonal falls oforganic material,
whereas benthic regions beneath oligotrophic mid-oceanic
gyres will have a continually low amount of available food .
The deep-sea benthos is therefore far from being the same
habitat across the globe. While this may be true for other
physicochemical factors, the great variability in food supply
appears to be the prime forcing factor underlying spatial
patterns in biomass. abundance. diversity, and life histories.
9.4 The organisms of the deep
sea
9.4.1 General patterns of organism
change from shallow water to the deep
sea
One of the great gradients in the marine realm is the depth
gradient from coastal waters. across the shelf. and down
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the continental slope to the abyssal plain. Providing infor- ing food concentration. However, some larger organisms
mation on how assemblages of organism change along do not demonstrate such a body size decrease, even quite
this dine dearly requires samples at all depths. This can the opposite, as exemplified by Figure 9.lOc, which plots
be problematical, as in many areas the continental slope is individual fish body size against depth: fish on average get
very steep and hard, if not impossible, to sample. The scale bigger as you move into the deep sea. Large deep-sea fish
and steepness of the continental slope can be dramatic in
places. South of the British Isles, for example, the slope (eJ 16
drops 2000 m over a few kilometres-a sloping diffhigher .. . "'. .• ••
than those of the Grand Canyon. Therefore, our knowledge
of species' patterns as we move from the shallows to the
14
12 •
• -• .' • •
~ Bacteria
deep sea has been built mainly from a few geographical 'k 10 ~ Meiofauna
• Mauofauna
areas where the slope is shallow enough to allow detailed
-g 8
sampling over the whole depth range. One such area is the - • Megafauna
Porcupine Sea Bight to the south-west of Ireland (indi-
cated in contour lines on Fig.?l) . Samples from trawls,
and other devices, can be pooled to enable general patterns
to be explored and some very clear trends have become
apparent. These were supported by samples taken from the o
other side of the Atlantic and more recently we have been
-2
able to piece together samples from around the world to • ••
generate an overall global picture of how patterns of organ- -4
o 1000 2000 3000 41100 5000 601
isms change. llepth 1m)
(bJ 16 - , - - - - - - - - - - - - - - - - - - ,
9 .4.2 Abundance and biomass of • Bacteria
14 •• • Meiofauna
assemblages • Mauofauna
12 •
The number of individual organisms in any given area, • • Megafauna
and their total biomass, shows a sharp decline as you move 10
'k , "'. '" '"'" "' . .'" .
from shallow to deepwater (Fig. 9 .lOa, b; Rexet at. 2006),
although the rate of decline varies depending on the size of -
~
= 8 '" It... ~ t . '" ••
• • • ••
- • .. • •
•
organisms. The large animals (megafauna) show the dear- '"
g
E
g
6
:c 4 ' 1
est decrease in abundance with depth, whilst there appears
to be very little change in the number of bacteria. Overall, .s 2
however, there are many more organisms per unit area in
shallow water (Chapter 8) than there are in the deep sea; o
• . .. •
• • •
the abyssal plain is characterized by having a very sparse
11100,---------------,
fauna. These trends have been related to overall food supply
and its quality. Lowest levels of biomass are found in abyssal
•
regions under waters of low productivity, whereas coastal •
BOO
biomass is boosted by terrestrial run-off and high coastal
productivity, which will diminish with increasing distance g • •
~
from land. An exception to this pattern can be deep trenches .S' 600
relatively close to land, which act as traps for coastal sedi- ~
.
- • •
ment and detritus and consequently can often have a stand- .'
ing biomass much higher than would be predicted from the •
•
•
•
•
•'. .
trend in Fig. 9 .lOb. •
•
200 • • • •
• • •
9 .4.3 Size of individual organisms •
•• • .' • •
The trend in individual organism size shows a less consis-
tent pattern and varies between different sized organisms. o 1 ? , , ,
Generally, for the macrobenthos there is a decrease in mean Figure 9.10 Depth-related trends in (a) global abundance
size with depth, supported by trends in the meiofauna of organisms, (b) total organism biomass, and (c) size of
(Gage & Tyler 1991). This also has been related to decreas- individual fish off New England.
 9.4 The organisms of the deep sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

are thought to be very old, as their growth rates are slow
in the cold water. The orange roughy, for example, found
on sea mounts can live 120-130 years and does not reach
maturity until the age of 23-29 . This species is therefore
exceptionally vulnerable to over-fishing (Koslow 1997) .
Depth-related increase in size becomes extreme in some
deep-sea groups, which demonstrate gigantism: giant
organisms are one of the major features of the deep sea
(9.4.11), a trend also apparent in polar seas (Chapter 12.9),
suggesting this phenomenon may be a function ofcold tem-
peratures rather than depth.
9.4.4 Diversity trends
OUf impression of diversity in the deep sea has changed
dramatically over the period of its study. In the nineteenth
century, Edward Forbes suggested that an 'a zo ic zone' ( =
'no animals', so lifeless) existed below 600 m, following a
series of dredges in the Aegean Sea. It just happened that
this is a particularly sparse region of the deep sea. which
was rather bad luck for Forbes, and with further sampling
it was clear that life existed in the depths; however, the
arguments as to how many species are present in the deep
sea still continue. We tend to think of coastal regions as
teeming with species, whereas the dark depths of the abyss
have comparatively little life. This image perhaps arises
from the trend in abundance (Fig. 9 .10a), and having
fewer individual organisms clearly will affect the number
of species present in any given area (Chapters 1 and 15).
However, perhaps a more suitable measure of diversity is
how many species are encountered when studying a cer-
tain number of individuals, which will control for changes
in density. Work from the late 1960s and into the 1980s
suggested that such patterns ofdiversity do not necessarily
demonstrate a linear relationship with depth (Fig. 9.11a),
as perhaps would be expected, but a peak in diversity at
around 2000 m depth (Rex 1981) . Potentially this rela-
tionship may be still affected by the declining density with
depth, and clearly there is a need to increase sampling in
the deepest areas to clarify this pattern. When quantitative

(-J 25 PolydlOetes
• • 6 ,,
,,'
-- 15 •
20 •
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15 Invertebrate megafauna
• •
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0 50 100 150 200 250 300 350 400 450 500 = , I
• • • ,, •• • •
lndiriducls 900 an"2 5
,, • • ••
'- ..
•
,
0
Figure 9.11 Diversity patterns in the deep sea. (a) An 60 40 20 0 2 0 4060 DO
example of the number of species expected for each 50 N latitude S
individuals encountered, indicating a peak in diversity
around 2000 m. (b) The relationship between number Figure 9.12 Latitudinal diversity trends in three groups
of individuals in a 900 cm 2 sample and the number of of invertebrate for deep-sea sites suggesting tropical
species in the sample, demonstrating a remarkably similar deep-sea areas are more diverse than those at higher
ratio regardless of depth. latitudes, particularly in the northern hemisphere.
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
samples from a range of deep-sea sites are collated there
appeared to be a consistent ratio of number of species to
number of individuals in a specified area, regardless of
depth (Fig. 9 .11b; Grassle 1989) . Additionally, abyssal
sites can vary considerably in their diversity. even those
comparatively close geographically (see 9.2.6) . A distinct
latitudinal diversity trend (see Chapter 1) is also appar-
entin the deep sea for several groups (Fig. 9.12), although
there is evidence that the southern hemisphere is more
diverse than deep-sea areas in the northern hemisphere
(Rex et a1. 1993) . The trend in diversity with depth there-
fore remains to be confirmed, perhaps due to the compara-
tively small number ofsamples we have managed to obtain
from the deep sea. However. what is clear is that overall
the deep sea is far more diverse than early workers could
possibly have imagined (see section 9.4.6) .
9.4.5 Trends in species composition
Most large environmental gradients in the marine envi-
ronment demonstrate a distinct sequential distribution
of organisms, such as for rocky shores (Chapter 6) and
estuaries (Chapter 5) . Closely related organisms have
specific environmental requirements and so fill a realized
niche that has minimal overlap with similar potentially
competing species. Perhaps surprisingly. given the huge
spatial scale, a sequential distribution of similar species
is also apparent along the depth gradient from coast to
abyss. An example is for squat lobsters (galatheid crust-
aceans) in the Porcupine Sea Bight (Fig. 9 .13), where
species from two closely related genera each exist across
comparatively narrow depth ranges. Where overlap does
occur (e.g. Munidopsis rostrata and M. bermudezi), the
species appear to be functionally separated; for example,
each member of the pair has one of two different chela
morphologies (Fig. 9.13) . In the case of the example pair
of species, M. bermudezi has spade-shaped chelae, while
those of M. rostrata are spear-shaped. How this morpho-
logical difference relates to feeding, and thus niche sep-
aration. is however unclear.
Depth (m)
Species o 1000 2000
Munida rugosa
Munida sarsi
Munida tenuimana
•-
Munidopsis curvirastro
Munidopsis rostrato - distribution of squat lobster
Munidopsis bennudezi
Munidopsis aries
Munidopsis antonii
Munidopsis porfoiti
Munidopsis crossa
An organism 's realized niche represents the range of
cond itions over which the species exists in its habitat.
This contrasts with the fundamental niche, which is the
range of conditions over w hich the species could survive
if other factors, such as competition, were not involved .
9.4.6 How many species are there in
the deep sea?
One of the great debates in ecology is how many species
actually exist on the earth. Much of the debate has centred
on diverse terrestrial systems such as tropical rainforests
(with their huge insect diversity), with inputs to the debate
from coastal marine areas such as coral reefs. As the deep
sea was generally regarded as species poor, the world's lar-
gest habitat had not been considered as being important in
terms of global diversity until comparatively recently. The
vast majority of work on the deep sea has concentrated on
the larger animals. but as more and more samples are pro-
cessed from the sediment it is becoming clear that the diver-
sity of small organisms in the deep sea is very high indeed;
most new mud samples that are thoroughly studied reveal
species new to science. However, the problem arises with
estimating the number of species in the whole ocean basin
from the tiny fraction of the seabed that we have sampled.
Attempts to undertake this extrapolation have launched the
deep sea into the midst of the 'How many species?' debate.
The diversity of microbes has only recently been
approached using new techn iques that amplify ribo-
somal RNA in samples. rRNA is a constitutive molecule
in bacteria, and sequences can be determined in order
to assess the number of species present, even if the
bacteria cannot be cultured.
The World Resources Institute (http:/ /www.wri.org)
states that approximately 1.4 million species are known to
exist on the planet. most of these are insects, especially bee-
tles (Chapter 1). Estimates in the early 1990s suggested a
3000 4000 5000
Figure 9 .1 3 Bathymetric
- species in the Porcupine
Sea Bight, illustrating a
clear sequential distribution.
Species illustrated are M.
bermudezi (left) and f\1.
rostrata (right).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
total of 3 to 4 million species were present on earth, mainly
in the terrestrial environment, but attention was drawn to
deep-sea diversity following a study by Fred Grassle and
Nancy Maciolek of Woods Hole Oceanographic Institute
(Grassle & Maciolek 1992). They had taken a large number
of replicate samples from along a deep-sea depth contour
off New England, USA, and had found a remarkably high
number ofspecies new to science. in particular polychaetes.
Additionally, new species continued to be encountered with
additional samples. The pattern of species' capture with
increasing sample area was assessed and used to estimate
further species' capture rates across the deep-sea basin,
with a conservative conclusion that there were probably at
least 10 million species in the deep sea. This caused much
controversy, particularly among terrestrial ecologists and
some coastal marine ecologists who criticized the tech-
niques used. but initiated a more detailed consideration of
the globe's total biodiversity, particularlywhen the smallest
organisms are considered.
Research on nematode worms has shown that this group
is exceptionally species rich in the deep sea. but, as in most
habitats. had been comparatively ignored, and estimates
of their diversity in the deep sea have been as excessive
as 100 million species, although recent detailed analyses
have considerably reduced such predictions (Lambshead &
Boucher 2003) . Recently, it has also become evident that
there is a vast diversity of bacteria and viruses in the world's
oceans (e.g, Beja et al. 2002), a large undefined number
of parasite species, plus perhaps a much-underestimated
insect diversity in the terrestrial biome. Biodiversity esti-
mates are therefore constantly under revision. The only real
certainty is that we do not know how many species there
are, and estimates now range from 10 million to over 111
million species in total. It is unlikely we will ever be much
more accurate. particularlywhen the majority of the Earth's
surface remains unsampled.
9.4.7 The main groups of organism on
the deep-sea bed
We are very familiar with the main groups of larger marine
organism dominant in shallow waters, but comparatively
few taxonomic groups of animal have proliferated on the
deep-ocean floor and are most regularly caught in samples.
Some taxa that are comparatively innocuous or species
poor in coastal regions are dominant in the deep sea. The
assemblage composition of the abyssal plain, even at the
level of phylum, will therefore show marked differences
from shallow water.
From the comparatively few samples fully analysed, the
taxonomic composition of smaller organisms in the mud
(termed macrofauna (>0.5 mm) and meiofauna «0.5
mm), see 8.3 .1) are similar to equivalent sediments in shal-
low waters. The macrofauna are dominated by polychaetes,
9.4 The organisms of the deep sea
bivalve molluscs. and pericarid crustaceans (e .g . amphi-
pods. cumaceans), while the main meiofauna constituents
are nematodes. copepods, and Foraminifera. It is the larger
megafauna that show the differences. organisms that are
big enough to show up in photographs and to be caught in
trawls. These can be divided into three groups.
9.4.8 Sessile megafauna
Sessile organisms are generally uncommon in soft-sediment
environments due to the lack of suitable hard substratum
for attachment. However. two comparatively unfamiliar
groups of cnidarian that are found in coastal areas are
much more successful in the deep sea. Both are members
of the Anthozoa (a group containing corals and anemones) :
the sea fans (gorgonians), and the sea pens (pennatulids) .
These organisms are anchored to the sediment by means
of a stalk, with the feeding and reproductive zooids held
well above the fine mud. Both groups are often found in
comparatively large beds and seem to be characteristic of
relatively high-energy deep-sea regions. A further group
of deep-sea anthozoans are the extensive hard coral reefs,
whose size and importance has only recently been appreci-
ated with the use of video technology.
Deep-water corals occur worldwide, often on sea mounts;
extensive reefs are present between 800 and 1300 m off
west Ireland, for example. One Lophelia pertusa reef (Fig.
9.2c) on the SulaRidge off Norway, was found to be over 14
km in length and rose 30 m above the bed in some places.
The reefs are also extremely old-recent pieces of skeleton
dated using 14C were found to be at least 4550 years old!
Due to their complexity compared with the muddy bottom,
deep-sea coral reefs also have a diverse associated commu-
nity, including fish, and thus have been popular areas for
fishing. Only recently has it become apparent that trawl-
ing has done extensive damage to many of these ancient
deep-sea reefs (Hall-Spencer et al. 2002) . The only other
group ofsessile organisms that are commonly encountered
in the deep sea are the sponges (Porifera) . For example,
beds of soccer-ball-sized glass sponges (Pheronema) can be
found below 1000 m in the Porcupine Sea Bight and their
main opening (o scu lu m) is regularly used as ready-made,
sediment-free burrows by animals such as Munida squat
lobsters (Fig. 9.2c) .
9.4.9 Sedentary megafauna
The group of deep-sea organisms that we probably know
least about are the large animals living below the mud sur-
face . While our grabs and dredges can sample the smaller
and shallow-living fauna. the only real information we have
on anything larger or deeper is from photographs, either of
part of the organism or, more tantalizingly. marks left on
the mud surface (termed Lebensspuren-German for 'life-
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Figure 9.14 Example of traces left by deep-sea organisms
on the mud surface taken at the Hawaii-2 observatory at
-5000 m depth. (a) Track trace, 'the lugworm' presumably
an animal moving along or under the surface (photograph:
Stace E. Beaulieu WHOI). (b) Spoke trace, a feed ing
impression made from the central hole, perhaps by an
echiuran worm (photograph: ECOMAR project, Oceanlab,
University of Aberdeen).
traces'; Fig.9.14) . Another group of organisms that is not
commonly encountered in shallow water, but appears to be
a major constituent of the deep-sea infauna, is the Echiura
(spoon worms) . These live permanently in burrows, but
extend a feeding proboscis across the mud surface to collect
depositing detritus. Occasionally the proboscis has been
caught in photos and the extended part has been measured
at over 50 cm long. suggesting an animal size of at least
a metre. Echiuran worms also leave a distinctive. rosette-
like feeding trace (Fig. 9.14b) and examples of these that
have been photographed were clearly made by organisms
biggerthan 1 m. It is likely that many unusual and fascinat-
ing large animals live below the deep-sea sediment surface,
but unless our technology develops dramatically they will
remain unknown.
Sedentary-organisms that tend to stay in one place, but
could move, if required. Examples include sea anemones,
large burrowing worms such as Arenicolo, and students.
9.4.10 Mobile megafauna
The group of deep-sea organisms we know most about
are the large animals that move about on. or just above,
the mud surface and are caught in both photographs and
trawls. Many taxonomic groups are represented in the
mobile megafauna. but three are particularly dominant and
characteristic ofthe deep-sea fauna: echinoderms. decapod
crustaceans. and fish.
Echinoderms
The deep sea could reasonably be termed the kingdom of
the echinoderm, as this phylum is far more prevalent than
in most shallow regions. All classes of echinoderm are well
represented in the deep-sea benthic fauna, but two groups
are particularly widespread and diverse: the brittlestars
(Ophiuroidea) and sea cucumbers (Holothuroidea). The
holothuroids in particular are remarkably diverse and com-
mon in the deep sea, and show a fantastic range of mor-
phological developments to life in the deep ocean, from
swimming ability due to the development of 'fins' (e.g.
Enypniaste; Fig. 9 .15) to highly modified oral tentacles (e .g.
Peniagone) that are used as hand-like structures to collect
sediment particles. In some food-rich parts ofthe deep sea.
sea cucumbers can also be abundant, forming 'herds' that
move together across the seabed. Examples include Kolga
hyalina and Scotoplanesglobosa, whose suction-like feeding
method has been termed 'vacuum cleaning', as they suck up
sediment and its inhabitants. Deposit-feeding sea cucum-
bers have to process vast amounts ofsediment to obtain suf-
Figure 9.15 The swimming holothurian Enypniastes,
illustrating the amazing diversification of sea cucumber
form in the deep sea (photo: NOAA).
 9.4 The organisms of the deep sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

ficient food : a single individual can pass 100 g of sediment
through the gut every day. Such organisms, together with
burrowers, can have a large bioturbating effect and are
highly important in structuring and altering the sediment.
and in potentially influencing small-scale diversity patterns
(Widdicombe et al. 2000) .
Decapod crustaceans
Crabs, prawns, and lobsters are a familiar component of
practically all coastal habitats, but like echinoderms the
most common large crustaceans on the deep-sea floor
belong to a less familiar group. Below the edge of the con-
tinental shelf, the dominant group of walking (re pt a n t)
crustaceans are the squat lobsters-anomuran crustaceans
related to hermit crabs (Fig. 9 .13) . Crabs are comparatively
rare in the deep sea and seem to be mainly a shallow-water
group, with a couple of exceptions. The red crabs (Geryon
and Chaceon) can extend down to below 1000 m in many
parts of the world and are often the object of commercial
fisheries . In the Porcupine Sea Bight, the red crab spe-
cies is Geryon trispinosus (Fig. 9 .2a) , which appears to
undertake an ontogenetic depth-related migration as it
passes through its life stages. Young crabs are present only
in deeper water, while the largest breeding adults are in
depths at the top limit of the deep sea (2-300 m) .ltwould
appear that the larvae settle out at depth and through their
life the crabs migrate up the continental slope to shallow-
water breeding grounds (Attrill et al. 1990). It is possible
that the absence of small crabs in the shallow areas is due
to competition from the comparatively high densities of
Munida sarsi squat lobsters present at these depths (Fig.
9 .13) . Below 1000 to 2000 m there are very few crab spe-
cies to be found, with the amazing exception of a couple
of species (e .g. Cyanograea) that exist on the ocean floor
around hydrothermal vents (9 .5.3) .
Ontogenetie-a factor that changes as an organism pro-
gresses thro ugh different developmental stages. Exam-
ples are o ntogenetic shifts in diet, and changes in the
shape or size of certain body parts, such as crab chelae.
The noun is ontogeny.
The other main group of deep-sea decapod crustaceans
are the prawns, which tend to swim above the seabed
(n a tant) . Many of these are large compared with shallow-
water species, and are often a bright red colour (Fig. 9 .16a).
This would be an unusual anti-predator mechanism in
coastal regions, but is a common strategy in the deep sea
and is related to the relative attenuation of light. Red light
does not penetrate far into the water column, and so in the
gloomy (dysph otic) regions of the deep sea, where some
light still penetrates, the red wavelength is absent. There-

Figure 9.16 (a) Examples of deep-sea prawns, highlighting their use of red colouration for 'camouflage' (photo:
NOAA). (b) Head of the rattail Nematomurus. (c) The 'jellyfish' Conocavara (both photos: Martin Attrill). (d) The deep-sea
anglerfish Phrynichthys, collected at 800 metres depth in 1991 (phote: WHOI).
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
fore, red organisms will be 'invisible' as there is no red light
to reflect off them. A fascinating predator-prey arms race
has evolved in the deep sea. with some species of deep-sea
fish possessing light organs that produce red light-a torch
to reveal red prey in the dark! (Box 9 .1)
Natant organisms mainly swim , whereas reptant organ-
isms mainly crawl on the seabed.
Fish
Perhaps the most evocative images of the deep sea are the
weird, alien-like fish with huge teeth, bulging eyes, or enor-
mous mouths, which have been trawled up from the deep
and feature in many a documentary series. However, most
of these species inhabit the featureless open-water habi-
tat and few groups of deep-sea fish are actually adapted
to a true benthic lifestyle. These are mainly rays, hagfish,
some flatfish, and angler-fish, a group that has diversified
in the deep sea and generally employs some form of bio-
luminescence as a lure (Fig . 9 .16d) . Most fish found on
the abyssal floor are known as benthopelagic, swimming
just above the seabed but not resting on it. A diverse group
of fish comprise this assemblage, but there appears to be
a common. elongated body form regardless of taxa that is
the ideal shape for deep-sea life. This is exemplified by the
rat-tails (Macrouridae; Fig. 9 .16b), with long dorsal and
anal fins supported by many fin rays and practically no tail
fin. In cold water, with comparatively low energy inputs,
fast movement may not be practical, so it is likely that most
benthopelagic fish move slowly and continually across the
bottom.
Rat-tails, such as the roundnose grenadier (Coryphaenoi-
des rupestris), are members of the same major group as cod
and haddock (Gadiformes). They are a successful, diverse,
and comparatively abundant taxonomic group within
the benthopelagic fishes and have supported commercial
fisheries, particularly by Russian fleets (Randall & Farrell
1997). A major problem for benthopelagic fish is the ability
to remain above the sediment. Hydrodynamic lift, as used
by many coastal fishes, requires relatively fast movement
and thus a large amount of energy, so is nota suitable strat-
egy in the deep sea. To achieve neutral buoyancy, deep-sea
fish either use buoyancy devices or reduce tissue density. As
with shallow fish species, many still utilize swim bladders
to achieve buoyancy, despite the problems of gas compres-
sion under the immense hydrostatic pressure-fish with
gas-filled swim bladders have been found to a maximum
depth of 5000 to 7000 m where the energetic costs of main-
tenance probably become too great.
An alternative buoyancy option comparatively unaf-
fected by pressure is to use lipids instead of air in a swim
bladder. Lipid accumulation in organs such as the liver is
used for buoyancy by shark species, but some fish, such as
the orange roughy (Hoplostethus atlanticlLS) and the coel-
acanth (Latimeria chalumnae), have wax esters making
up more than 90% of the swim bladder fat to boost buoy-
ancy (Randall & Farrell 1997), while others (e.g .Antimora
rostrata) have fat-filled swim bladders, mainly cholesterol
and phospholipids. An alternative buoyancy method is
to reduce body density (particularly skeletal and muscle
density) by converting tissues to lighter substances such
as water, gelatinous material, or cartilage. Such fish with
watery or gelatinous tissues (e.g. Acanthonus, Conocovara;
Fig. 9 .16c) are only slightly denserthan water and true jel-
lyfish!
9.4.11 Gigantism in the deep sea
A feature of the deep sea is that some groups that are
classified as macrofauna in coastal waters have deep-sea
species that are so large they can be caught in trawls and
considered megafauna (Gage & Tyler 1991) . Giant amphi-
pod and isopod crustaceans are features of the deep-sea
benthos (and also Polar regions; Chapter 12) and among
the major scavenging organisms. Examples include the
massive amphipod Eurythenes gryllus, which can grow to
140 mm (Fig. 9 .6), and the giant swimming isopod Bathy-
nornus gigantelLS (Fig. 9 .17), which can grow to 0 .5 min
length and is commercially fished! Sea spiders (pycno-
gonids) also have giant representatives in the deep sea:
Colossendeis colossea has a leg-span up to 0.5 m, its long
legs acting as stilts that help to keep the body above the
sediment. However, perhaps the most remarkable exam-
ple of gigantism occurs in a group known as the xenophy-
ophores (Levin 1994), originally thought to be related
to sponges but now known to be giant single-celled pro-
tozoans (their own phylum within the Protoctista), that
are so large they appear in photographs of the seabed and
are bigger than most macrofaunal metazoans. Their form
Figure 9.17 The giant deep-sea isopod Bathynomus
giganteus.
 9.5 Hydrothermal vents
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
is varied, from spherical to disc-shaped and can have a
branching n etwork below the mud surface . The largest,
the leaf-shaped Stannophyllum, is 0 .25 m in diameter and
1 mm thick! In some areas of the deep sea. such as the
south Pacific. xenophyophores are the dominant taxon
and can comprise 97% of the biomass.
The best-known example of a deep-sea giant is the
legendary giant squid Architeuthis. The maximum size of
this species remains unclear. the largest caught specimen
(1878) measuring nearly 17 m long. Sailors' observations,
and sucker scars on sperm whales. suggest squid lengths
> SO m, but it has also been pointed out that such scars may
increase in size as the whale grows. However. there appears
to be an even bigger species, the 'colossal' squid Mesony-
choteuthis hamiltoni, a specimen of which was caught in
2003 from 2000 m off New Zealand (http:/ /www.tonmo.
com/science/publicigiantsquidfacts.php) .
Why do giant taxa exist in the deep sea? Several theories
have been produced, including links to the metabolic effects
of great hydrostatic pressure and cold. the differences in
dissolved oxygen levels (see 12.9), delayed onset of sexual
maturity. and indeterminate growth-organisms live a very
long time and continue growing. Other ideas relate to the
method of food capture. and perhaps have a clearer evo-
lutiona ry route. For example, giant scavenging amphipods
could be an adaptation to a foraging strategy where high
motility is needed to locate sparsely dispersed food. How-
ever, we are still not clear how, or why, animals often living
in extremely oligotrophic areas become so large.
Figure 9 .18 (a) A black smoker. (b) A dense aggregation of ventimentiferan tubeworms (Riftia) near a hydrothermal
vent. (Copyright: NOAA.)
islands in the deep sea
9.5 Hydrothermal vents->
islands in the deep sea
Thirty years ago, practically all deep-sea ecology was
focused on the comparatively featureless deep-sea bed and
our impressions ofdeep-sea life were therefore determined
by this image. However, discoveries over the last couple of
decades, through the use of submersibles and more inten-
sive acoustic mapping, have demonstrated that the ocean
basin is not a continuous. featureless floor but within these
plains are a series of other features that have exciting,
unique, and often diverse communities: islands in a sea of
mud. Most are based on unusual outcrops of hard substrate
that have been formed by different means, and include sea
mounts (De Forges et al. 2000) and deep-sea coral reefs
(Hall-Spencer et al. 2002; Fig.9.2c) . However, the most
dramatic and unusual island communities are associated
with hydrothermal vents.
9.5.1 What and where are
hydrothermal vents?
Hydrothermal vents are associated with parts of the ocean
floor that exhibit high levels of tectonic activity, such as
the spreading axes of plate formation (mid-ocean ridges),
and vent clusters have been given evocative names such as
'Rose Garden' and 'Snake Pit'. The first vent was observed in
1977 on the Galapagos Rift (Pacific) from the submersible
Alvin (Fig. 9 .3a) by a team including Bob Ballard-the man
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

behind the rediscovery of the Titanic. The system was found

by 'chance' when investigating temperature anomalies in
surface waters. Within such regions, hot magma chambers
occurnear the seabed and heat up water that has permeated
into the ocean floor; water temperatures above lOQOC are
possible due to the high hydrostatic pressure that prevents
waterboiling. This superheated water erupts back out ofthe
seabed carrying with it a rich cloud ofminerals, such as sul-
phides, methane, manganese, and many other trace metals.
The vent therefore often appears as smoke emerging from a
chimney formed by mineral deposits (Fig. 9 .1Sa) . The hot-
test, and most dramatic, type of vent is therefore termed
'black smoker' due to the colour of the plume, and water
temperatures within the plume can be up to 350°C. 'White
smokers' also exist, which tend to be a little cooler. and in
some areas hot water escapes through cracks and crevices
in the seabed to form diffuse vents with water temperatures
much lower than the smokers. Hot emissions from smokers
are rapidly mixed in the cold deep-sea. so most vent animals
generally live in water temperatures close to the ambient
of 2°C (the plume water also contains no oxygen), though
there are astonishing exceptions, such as the polychaete
worm Alvinella pompejana (or Pompeii worm; Fig. 9 .19),
which forms burrows on the vent chimneys (Cary et a1.
1998) . Water temperatures within the worm burrows mea-
sured by Alvin were found to average 6SoC, with frequent
spikes up to 81 °C. Pompeii worms emerge from burrows Figure 9.19 The Pompeii worm (Atv/nella popejana}-the
to feed on filamentous bacteria and have been known to most thermotolerant multicellular organism on Earth?
survive short exposure to 105°C! Alvinella is the most ther- (Copyright: Nature.)
motolerant eukaryotic organism known.
vents is not primarily explained by production offree-living
bacteria, but through chemosynthetic, symbiotic bacteria
9.5.2 Production at hydrothermal
that live within the vent invertebrates. A group of animals
vents unique to vent environments has therefore evolved that
Hydrothermal vents are exceptional among deep-sea relies upon a symbiotic relationship with bacteria.
islands, and vastly different from the rest of the deep sea,
in having a huge biomass of associated organisms (Fig.
9.5.3 Classic vent animals
9.1Sb) . Clearly, alternative methods offood supply are sus-
taining these communities. and this production is autoch- Probably the most striking examples of this dependence on
thonous and related to the supply of reduced compounds symbiotic organisms are the large vestimentiferan tube-
(particularly sulphur compounds) emerging from the vent. worms characteristic of vent communities in the Pacific
Vent assemblages are sustained by primary production gen- (Fig. 9. I Sb). Previously these worms were classified within
erated by bacteria through chemosynthesis (Box 9.2) and another unusual worm group, the Pogonophora, then
considered of little importance until recently, when vents given a phylum of their own (Vestimentifera), but through
were investigated. molecular analysis are now known to be highly developed
Chemo-autotrophic bacteria are present in hydrothermal members of the Polychaeta. The 1 to 2 m long worms, such
fluid and tend to be members of the most ancient Archaea. as Riftia pachyptila, live in white tubes attached to the vent
These can tolerate exceptionally high temperatures and are surrounds (15 to 20°C) with a red tentacular plume extend-
therefore either known as hyperthermophiles (SQ-115°C) ing from the tube, which can be retracted quickly when
orthe most extreme superthermophiles (> 115°C) . Bacte- disturbed. While superficially the worms look like normal,
ria are also free-living in the vent environment, such as the if large, tube-dwelling polychaetes feeding on particulate
filamentous bacteria fed upon by Alvinella, and thus pro- material, they have two strange anatomical features: they
vide a continually replaced food supply for vent animals. completely lack a mouth and digestive system and they
However, the comparatively large biomass associated with have a specialized organ (tro ph o som e) that houses che-
 9.5 Hydrothermal vents
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
mosynthetic bacteria deep within the animal's body; bac-
teria compose up to 50% of the weight of the worm. Riftia
relies on bacteria for its organic carbon supply, the plume
of tentacles is used to uptake other nutrients from the sur-
rounding environment.
Other key components of the vent fauna are large, white
bivalve molluscs, which form extensive clusters in cracks
and crevices around smokers and other vents. These are typ-
ified byrwo genera: the giant clam (Calyptogena; Fig.9.20),
which can grow up to 26 ern, and the vent mussel (Bathy -
modiolus). These molluscs also house symbiotic bacteria (in
cell vacuoles rather than a specific organ), which supply
the majority of the bivalve's organic carbon needs. Calypto-
gena takes in ambient CO2-rich water over the gills through
siphons, while its foot extends into the crevice where it lives
in order to exploit warm sulphide-rich vent fluids.
The other major group present on vents are decapod
crustaceans. which scavenge off other vent animals rather
than having endosymbiotic bacteria. Squat lobsters are
common. but Pacific vents also have associated crab spe-
cies (e.g, Bythograea thermydron ; Fig.9.20) that are key
members of the vent food-web but comparatively uncom-
mon anywhere else in the deep sea due, perhaps. to the
planktonic larval strategy generally adopted by the group.
How this species has colonized and adapted to life on vents
is therefore an interesting question, but it would appear
that larval stages of the crab remain in the vicinity of the
vent. Like shallow-water crabs, large numbers of eggs are
produced, but first-stage zoea of Bythograea have been cap-
tured in plankton tows of bottom water over vents rather
than at the surface thousands of metres above. However,
the most remarkable feature is the megalopa (settling larval
stage), which is enormous compared with shallow-water
crabs (5-10 cm carapace length) and common in both
water overlying vents and within clumps of Riftia where
they appear to take refuge.
Figure 9 .20 Examples of organisms associated with hydrothermal vents. (a) The giant vent clam Calyptogena (Photo
taken by Richard A. Lutz). (b) Swarms of shrimps (Rimicaris) around vents in the North Atlantic (© Missao Seahma,
2002 (FCT, Portugal PDCTM 1999MAR15281) w/IFREMER).
islands in the deep sea
Vestimentiferans are classic features ofPacific vents. but
in the mid-Atlantic (whose vent systems have a very differ-
ent fauna to the Pacific), the dominant animal is often a spe-
cies of shrimp (e.g, Rimicaris exoculata; Fig.9 .20), which
can form huge swarms around hydrothermal vents. These
shrimps are characterized by large, paired dorsal eyes that
can extend halfway down the midline of the shrimp; the
shrimps do not possess normal eyes and eyestalks. It has
been proposed that Rimicaris can detect thermal radiation
emitted from hot vent fluids, thus enabling the shrimp to
navigate around the vent without being cooked.
While the tubeworms, bivalves, and decapod crusta-
ceans are the most prominent groups associated with vents.
most other taxa are also represented, particularly sessile
and sedentary animals. such as sponges and anemones.
Few fish species are found only in vent habitats. an excep-
tion being the well-named Thermarces, which has aspects
of its biochemistry adapted for high temperatures as well
as high pressure. The fish appears to feed on the abundant
swarms of amphipod crustaceans (Halice) that can reach
densities of > 1000 1-1above lower temperature vents!
The exact composition of vent assemblages and the rela-
tive position of species at a vent seem closely related to the
chemical speciation within the vent water (Luther et a1.
2001) . Significant differences in oxygen, iron, and sulphur
speciation are correlated with the distribution of taxa in dif-
ferent microhabitats.
9.5.4 other types of vent and seep
Not all chemosynthesis-based communities in the deep
sea rely on hot-water vents and distinct assemblages have
been discovered associated with other conditions, where
a suitable concentrated source of nutrients is available.
Most of these are termed cold seeps; for example. where
oil leaks onto the sea floor from underground reservoirs.
 Chapter 9 The Deep Sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

2.5
These communities are often dominated by the bivalves (oj Riffio pochypnlo
0
that have symbiotic relationships with chemosynthetic bac-
teria. The deepest chemosynthesis-based community so far -"
~

~
2.0
0
discovered is at 7326 m in the Japan trench (Pacific) and is 0 1.5
-.'"
~
0

dominated by the bivalve Maorithyas hadalis (Fujikura et al. :E 1.0 8 o

1999) . At this site, as in other trenches, the assemblage is o
sustained by chemosynthesis using the high sulphide con- 0.5
tent of the sediment associated with the geologic fault . A
large deep-sea oil 'lake' exists on the sea floor in the north- 0 1 2 3 4
ern Gulf of Mexico. The lake is ringed by deep-sea bivalves, 2.0
(bJ Bothymodiolus thermophilus
which can cluster so closely that individuals get pushed into
"
the lake-with fatal consequences.
--
0
~

~
1.5
0
'2>
0
0 . ____ 0 - -

9.5.5 Dispersal and gene flow in vent
• :E
orgamsms
Most vent organisms are uniquely associated with vents or
seeps, and a feature of vent fauna is the number of endem-
ics, many with ancient lineages. The persistence of ancient
taxa has led to suggestions that vents have been compara-
tively immune to major planetary extinction events. as
they are only indirectly dependent on the sun. However.
hydrothermal vents are comparatively temporary in nature
as the Earth's crust will move over the magma chamber and
the vent will 'die'. Observation of the Rose Garden vents
near the Galapagos Islands since discovery in 1979 has
suggested some degree of succession as the vent matures
and its chemical nature changes (Hessler et al. 1988; Van
Dover 2000) . Rifria seems associated with comparatively
new vents, but declines in relation to decreases in sulphide
concentration . The bivalves, however. persist and even
expand their populations as vestimentiferans disappear.
suggesting possible competitionbetween mussels and tube-
worms. New vents will clearly emerge through the same
geological process, but one of the most interesting aspects
of vent ecology is how organisms disperse between vents
and how new vents become colonized . The majority ofvent
organisms appear to have larvae with abbreviated develop-
ment (lecit hotroph ic), so will be colonizing nearby vents.
Surveys in the Pacific have suggested vents are generally
< 10 km apart but there is up to 100 km between vent
fields, presenting dispersal problems between these strings
of islands for short-lived larvae of endemic vent species
(Van Dover 2000) . If dispersal, and thus gene flow, is lim-
ited then there would be extensive genetic differentiation
between vent fields. Two different models of gene flow are
apparent in vent taxa (Vrijenhoek et al. 1998; Van Dover
2000) . Rifria fits a 'stepping-stone' model with most gene
exchange occurring between neighbouring populations
and gene flow declining with distance (Fig. 9.21a), whereas
patterns of gene flow are different for Bathymodiolus (Fig.
9.21b) where migration rate appears unrelated to distance.
This is termed the 'island' model suggesting long-distance
dispersal and mixing of larvae within a 'migrant pool'. The
.'"-
~
1.0 __ A - - - - - - - -
~
0
",03.
0.5
o 1 2 3 4
log (distonce)
Figure 9.21 Gene flow models in vent organisms. (a)
Rlitia, the isolation-by-distance model, with migration rate
decreasing with distance. (b) Bathymodiolus, the island
model, where migration rate is constant, regardless of
distance.
vent mussel appears to be unusual in this respect. though
its apparent wide dispersion may be also influenced by its
ability to colonize a range of seep and vent types.
Despite the general lack of dispersal ability, vent organ-
isms appear to successfully colonize the majority of vents.
The puzzle of how poorly dispersing larvae can travel large
distances has focused on the supply of potential stepping-
stones between vents that provide the suitable nutrient sup-
ply for chemosynthesis to occur. Whale skeletons provide
such a resource (HzS is produced by bacterial decomposi-
tion of lipids). so larvae could disperse over several gen-
erations (Smith & Baco 2003) . Conversely, it has also been
suggested that some groups of organisms may have origi-
nally invaded vents from biological material, such as whale
bone and wood; analysis of such material from the deep
sea revealing small mussel species (e.g . Idas washingtonia)
in the same subfamily as Bathymodiolus, which appear to
have preceded vent specialization within this lineage (Dis-
tel et al. 2000) . These small bivalves possess chemosyn-
thetic endosymbionts, utilizing sulphide produced by wood
decomposition, so it is feasible that wood (and bone) were
vectors that originally transported mussels to vents.
While vent taxa appear to disperse effectively, through
a variety of strategies. it would appear that some deep-sea
islands remain uncolonized . Recently. a new vent field was
discovered in the mid-Atlantic (named 'Lost City'), which
had steep-sided black smokers and dense microbial com-
munities, yet none of the large invertebrates associated
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

with other Atlantic vent systems (Kelley et al. 2001) . This currents have not, as yet, brought settling larvae of vent
new field lies 15 km off the main axis of the mid-Atlantic organisms.
ridge and clearly is in a position where the main dispersive

Chapter Summary
• The deep ocean floor (below 200 m) represents the largest habitat on the planet, but the least
known. The abyssal plain extends across the bottom of much of the ocean at depths of 4000-
5000 m.
• Sampling the deep-sea floor is except ionally difficult and is an expensive undertaking. As a result,
much of our knowledge of larger organisms comes from photography and comparatively few
samples. More recent ly, submersibles have revolutionized how we can sample and observe this
distant environment.
• Conditions on the abyssal plain are remarkably constant, generally being dark and cold (2°C), w ith
the seabed made up of fine , deep mud. Hydrostatic pressure is over 500 times that at the surface.
• Food supply is the main limiting factor for deep-sea animals, as the food web relies on the fall of
organic material from the surface layers, mainly as 'marine snow'. This fall is seasonal in temperate
regions, giving regu lar annual cues to benthic organisms.
• Only 1-3"0 of surface production reaches the ocean floor, so animals on the abyssal plain are in low
abundance and total biomass. However; individual animals can grow very large, with giant members
of groups such as sea spiders, amphipods, and xenophyophores (giant single-celled protozoans)
a feature of the deep sea.
• There is much controversy over how many species live in the deep-sea, with estimates as excessive
as 100 million! We will never know the actual number, but it is possible that the majority of species
on earth live in the deep sea.
• Many deep-sea organisms produce light, known as bioluminescence. This can be for a range of
functions, such as attracting prey, deterring predators, spotting prey in the dark, and advert ising
for mates.
• In the late 19705 and early 1980s the use of submersibles assisted the discovery of an entirely
new ecosystem in the deep-sea-hydrot hermal vents. The sulphur in these vent systems is used by
bacteria to generate production throug h chemosynthesis-primary production without t he need
for sunlight. Many vent animals, such as giant tube worms known as vestimentiferans, have vast
numbers of these bacteria living symbiotically in t heir bodies and providing them with a food sup-
ply.
• How vent animals disperse continues to puzzle marine ecologists. Some species may use stepping-
stones on t he ocean floor to reach new vents. Whale carcasses could be very impo rtant for vent
animal dispersal as their bones contain sulphur.

Further Reading
Books
• Gage, J. D. & Tyle r, P. A. 199 1. Deep-Sea Biology: a Natural History of Organisms at the Deep-Sea Floor.
Cambrid ge University Press, Cambridge.
• Herring, P. 2002 . The Biology of the Deep Ocean. Oxfo rd Un ive rsity Press, Oxford.
• Van Dover, C. L. 2000. The Ecology of Deep-Sea Hydrathermal Vents. Pri nceton Un ivers ity Press, Prince-
ton , NJ.
Chapter 9 The Deep Sea

Key papers and reviews

• Levin, LA., Etter, RJ. , Rex, M.A., Gooday, AJ., Smith, CR, Pineda et al. 200 1. Environmental infl uences
on reg ional deep-sea species diversity. Annual Review of Ecology and Systematics 32, 51 -93 .
• Martin , W" Baross, J., Kelley, D" & Russell, MJ, 2008, Hydrothermal vents and the origin of life, Nature
Reviews Microbiology 6, 805-814.
• Rex, M.A. et al. 2006, Global bathymetric patterns of stand ing stock and body size in the deep-sea
benthos. Marine Ecology Progress Series 317: 1-8.
• Roberts J.M ., Wheeler AJ., & Freiwald A. 2006. Reefs of the deep: the biology and geology of cold-
water coral ecosystems. Science, 213 : 543-547.
 Mangrove Forests and
Seagrass Meadows
Chapter Summary
Mangrove forests and seagrass meadows represent two of
the most valuable marine habitats in the world, rivalled only
by co ral reefs for their importance in providing a high level
of productivity and physical structure that supports a con-
siderable biodiversity of associ ated animals. However, both
systems are remarkable in that they are based on higher
pl ants more generally associated w ith terrestrial systems,
so mangrove trees and seag rasses demonstrate fascinating
physical, biological, and life-cycle adaptati ons that enable
survival in the marine realm. Mangrove forests host a unique
mix of marine and terrestria l animals, including insects, birds,
fish, and particularly crabs, w hose activities heavily influence
10.1 Introduction
A fund amental, and obvious, difference between the ecology
of terrestrial and marine systems is the taxonomy of the main
primary producers that power the respective food webs. Pro-
duction within the ocean environment (Chapter 2) is mostly
generated by small, often microscopic algae, suppleme nted
in coastal waters by larger brow n, red, and green macroalgae
attached to the seabed and intertidal zone. Generally, stand-
ing biomass is low (on a global scale) , although production
itself can be very high. With comparatively few exceptions (as
we will see), marine animals do not generally rely on plants
for shelter, giving the impression that the sea is an animal-
dominated, rather than plant-dominated, system (thin k of
coral reefs, for example). The terrestrial environme nt, in con-
trast, is dominated by large primary producers such as trees,
grasses, and herbaceous flowering plants (a ngio sp er m s),
which are comparatively recent in evolution ary terms; terres-
trial angiosperms , for example, only appe aring extens ively in
the fossil record approximately 100 million years ago. Wher-
the product ivity of mangrove fore sts. Spec ies such as mud-
skippers demonstrate incred ible levels of adaptation to life
in this intertidal habitat. Seag rass beds provide a st ructural
hab itat on generally feat ureless soft-sediment bottoms, and
so are uti lized by a w ide and diverse range of fish and inver-
tebrates, providing a physical ho me, food supply, and shelter
from predation. Seag rass meadow s are also vital grazing
areas for large vertebrates, such as turtles and sea cows.
Both mang roves and seag rasses provide a range of fu nctions
that influence the w ider coastal ecosystem and have value for
humans, so their fragmentation and loss has conseq uences
far beyond the orga nisms that live associated wi th these
plants.
ever conditions allow, the land is covered by plants and so the
m ajority ofland an imals utilize plants as a structural habitat.
In a sim ilar manner to insects, which dominate the terres-
trial animal fauna, few terrestrial vascular plants have been
able to exploit marine cond itions . In fact, only one group
is able to live full y beneath the sea: the seagrasses. These
angiosperms can grow, flower, and reproduce all within the
subtidal e nviron ment, and in parts of the world form vast
mea dows in coastal habitats. This results in a very unusual
habitat, much more similar to those on land than those gener-
ally found in the sea, and therefore providing an important
prod uction source and home for m any associa ted marine
organisms .
Two other important coastal systems are created by higher
plants: mangrove forests and saltm arshes.
For more details on saltmarsh ecology see Adam (1993).
Wh ile these assemblages of plants cannot tolerate con-
tinual immersion in seawater, they are highly adapted to
 Chapter 10 Mangrove Forests and Seagrass Meadows
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dealing with the problems faced by plants on the fringes of

the marine environment. Consequently they too can cover
huge areas of the land/sea interface and provide a key role
both in terms of the functioning of coastal ecosystems and
the provision of a structural habitat for a diverse range of
species. Saltmarshes tend to be associated with estuarine or
lagoonal systems at higher latitudes; their ecology is there-
fore outlined in Chapter 5. Mangroves, on the other hand,
are closely connected with both marine and estuarine
conditions, and have a diverse and important associated
fauna. Together with coral reefs and seagrass meadows.
mangroves are recognized by UNEP as the most important
marine habitats. This chapter will therefore discuss how
two contrasting plant groups (seagrasses and mangroves)
are able to survive in the marine environment. and, in par-
ticular, investigate their relationship with a diverse and
often unusual range of animals, which associate them-
selves with these plant-based habitats.

10.2 Mangrove forests

10.2.1 What is a mangrove?
Mangroves are woody trees or shrubs that flourish at the
sea/land interface in sheltered tropical coastal and estua-
rine regions where fine sediment collects. They can be
subdivided into two categories : true mangroves, which
only occur here. and mangrove associates. which can
also be found elsewhere. e.g. rainforest. An individual tree
is termed a mangrove. while the whole forest habitat is
a mangal (or simply 'mangrove forest') . There are three
basic forms of mangrove. depending on shore morphology
and sediment. salinity regime of the surrounding water.
and the relative tidal and freshwater influence (Fig. 10.1) .
Riverine mangroves form where there is a low tidal range
and a dominance of freshwater flow, such as the deltas of
major rivers. Most of the large areas of mangrove forest in
Asia are riverine mangroves. Tide-dominated mangroves
are fully intertidal, often in full-strength seawater and are
subject to high-wave action. These are also termed 'fring-
ing' mangroves and are often the pioneer species that first
colonize the intertidal mudflats. Basin mangroves occur to
the landward-side of fringing mangroves, where there are
lower tidal currents and wave action, but where salinity can
be highly variable due to evaporation and rainfall. Figure 10.1 Examples of types of mangroves: (a)
riverine mangrove, (b) tide-dominated (or fringing)
For an excellent, more detai led text on mangrove ecol- mangrove, (c) fring ing mangrove roots w ith associated
ogy, see Hogarth (1999). community of animals. Copyright: (a) US Fish & Wildlife
Service, (b) NOAA, (c) Martin Attri ll.
Mangroves are taxonomically diverse (Tomlinson
1986), with representatives in mangals of 16 very differ- families dominate the world's mangrove flora, however,
ent plant families . This suggests that the mangrove habi- in terms of both diversity and ecological role. The first
tat has evolved separately at least 16 times . Two main is the Avicenniaceae, represented by eight species of

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
the genus Avicennia (the black mangrove); the second,
the Rhizophoraceae, which includes the red mangrove
(Rhizophora, 8 species) together with three other gen-
era (Bruguiera, Ceriops, and Kandelia) . Other important
families include the Combretaceae (which includes the
white mangrove. Laguncularia). the Sonneratiaceae
(important in Australia and Southeast Asia; 5 species),
and also one species of palm (Palmae), Nypa, demon-
strating the width of mangrove taxonomic range. Nypa
pollen and fruits have fossilized well, due to the condi-
tions in mangrove forests, providing information on the
evolution of palms and climate change. Nypa fruits from
the Eocene (60 mya) have been found in the UK!
10.2.2 Where are mangroves found?
Mangroves are strictly tropical, and their distribution
across the globe coincides very closely with that of
coral reefs, but they are also found in tropical regions
where local conditions do not favour reef development,
such as the Amazon region of South America. Distribu-
tion is generally confined to the 20°C isotherm either
side of the equator. modified by either warm currents
extending their distribution (e .g. east Australia). or
cold currents extending into the tropics (e .g. west South
America) . Diversity is highest in the Indo-West Pacific
(IWP) and declines dramatically away from this region
to a minimum in the Caribbean/West Atlantic (Ellison
et al. 1999). This is thought to be due to increased local
diversification following continental drift (vica r ia n ce
hypothesis), ratherthan the IWP being the centre of ori-
gin of mangrove taxa and from where they subsequently
dispersed to other parts of the world. Mangroves develop
wherever shallow-sloping, generally muddy shores are
available within this region, especially lagoons, estuar-
ies. and river deltas. Diversity is then due to separate
evolution of species. rather than dispersal from a centre
of origin.
A vicariance event is t he formation of a barrier to
genetic exchange that causes separation of related taxa
(e.g. continental drift, glaciation).
Within a mangrove forest. there is a clear pattern of
distribution of species with distance away from the sea.
The fringing mangrove species are found at the sea edge,
and across most of the world these pioneer trees tend to
be species of Rhizophora. Other true mangrove families
inhabit conditions behind these fringing species; in Flor-
ida, for example. Avicennia and Laguncularia are located
in the mid-swamp, Laguncularia preferring natural topo-
graphic highpoints where sediment is less waterlogged.
Behind these true mangroves are distributed a range of
10.2 Mangrove forests
mangrove associates, generally forest plants that are
able to tolerate the conditions found in the high swamp,
but cannot deal with the excessively harsh environment
inhabited by the true mangroves. So why do mangroves
show such a distribution pattern in relation to distance
from the sea and why is it so difficult for terrestrial trees
to inhabit the coastal fringe? Two main factors limit plant
distribution: increased salt levels and waterlogged sedi-
ment, although other more minor factors (such as soil
nutrient levels) can also have an influence.
10.2.3 How mangroves deal with
living in a marine environment
When considering how terrestrial organisms penetrate
the intertidal zone. we have to invert our usual percep-
tion about the stresses affecting marine organisms living
in this habitat. On a soft-sediment shore, high salinity
levels and water being maintained within the sediment
are crucial to the survival of a marine organism. but both
cause extreme problems for terrestrial plants used to liv-
ing in dry soil with minimum salt content.
Waterlogged sediment
The thick, waterlogged mud present in mangrove forests
presents a key problem for trees, the sediment is excep-
tionally low in oxygen and tree roots need oxygen to
respire and function. Mangroves have developed three
main morphological adaptations to enable their roots to
obtain oxygen despite growing in anoxic conditions (Box
10.1) . All involve root structures that exit the sediment
enabling air to be taken in though special pores (called
lenticles) and keep the section of root within the sedi-
ment supplied with oxygen.
Dealing with increased salt levels
The presence of salt results in two main problems for trees
living in marine conditions. First. the uptake of salt dis-
rupts cellular mechanisms and is fatal for most plants. This
can be dealt with through either exclusion of salt by roots,
tolerance ofsalt in tissue (this is much higher in mangroves
than other plants), or secretion of excess salt through the
bark or by shedding leaves (they often taste salty iflicked).
Second. and perhaps most importantly, salt water in sedi-
ment reduces the osmotic difference between the root and
the sediment making it difficult to take up water (Hogarth
1999) . Rhizophora only takes water from the top 50 em
of soil (fresh water is less dense than seawater and hence
occurs in the upper layers of soil in these systems) and it is
thought that Avicennia excludes 90-95% salt at root sur-
face (salt can be excreted, though we are not sure exactly
how it is excluded) . Due to this osmotic difference, man-
groves take up water much less easily than other plants
 Chapter 10 Mangrove Forests and Seagrass Meadows
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and so n eed a much greater proportional root biomass to

Box 10. 1: Mangrove root structures
Different mangrove families have varyi ng st rategies
enab ling them to get oxygen to roots w ithin anoxic
sed iment. Rhizophora produces aerial roots (a), w hich
leave the tree up to 2 m from the ground and then
penetrate the so il, giving the tree support. The aerial
section is rich in lenticles to take in air. Rhizophora can
al so produce aerial branches to aid oxygen uptake. Bru-
guiera roots periodically break the soil surface during
growth, producing 'knees' above the sediment surface
(b) through wh ich air is taken up. Avicennia roots have
a feature symbolic of mangrove forests, w ith vertical
tubes (pneumatophores) emerg ing every 15- 30 em
from horizontal roots (c) . The tip of each tube has
abundant lenticles for air uptake. A 2 to 3 m high
Avicennia can have up to 10 0 0 0 pneumatophores.
(0)
ach ieve this (the add itional growth needed for roots there-
fore restricting energy being put into vertical growth and
reproduction) . Wit h in a mangrove forest. trees inhabit-
ing higher salinity soils have a larger below:above ground
biomass ratio than those in more freshwater conditions ,
highlighting the efforts required to survive in marine sedi -
ments (Saintilan 199 7; Fig. 10.2a). Mangroves also have
much greater root biomass than ot her trees. In Australia,
mangrove root biomass was estimated as 125 tonnes per
hectare (r ha-' ), compared with 9 0 t har! for large eucalyp-
tus and 32 t ha-! for Acacia (Snowden et aJ. 2000).
The difficulty in taking up water has additional impor-
tant consequences. Plants tend to regulate temperature by
transpiration. allowing water to be evaporated from leaves
to cool the plant. Mangroves cannot afford to cool leaves
primarily by this route as water is a limiting resource. but
to achieve maximum photosynthesis leaves also need to be
held perpendicular to the sun-which consequently maxi-
mizes temperature increase ! Rhizophora holds leaves at
angles to the sun depending on how exposed the leaf is.
Those at the edge of the tree, in full sun, are held at 75' ,
thus preventing overheating, while shaded leaves furt her
back into the tree are fully exposed to the sun d irection (0°) .

(01
o
10 o Avicennia
E
~
• Aegiceras
o
o
e=
i5 1 • •o
~
o

s
••
~

= o• 0
(b)
10 20 30 40 50
Salinity
500
(bl
<> S./anceo/ato
-E
400
o S. alba
--=
E
~
300
~

'" 200
\
"-
100
, , ""0 , ,
(e) 0 20 40 60 80 100
Salinity (% seawater)

Figure 10.2 Dealing with salt levels. (a) The cost

of living in high salinity s e d ime nt s- ma ng roves
require proportionally larger root biomass to enable
water uptake when salinity is high . (b) Comparative
distribution along a s a linity gradient of two closely
related Sonneratia s pe cies, their natural distribution
relating to a combination of salt tolerance and
competitive ability.
 10.2 Mangrove forests
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Salt tolerance also varies between species within the

same genus, which relates to their natural distribution
within a mangrove forest. For example. in Australia, Son-
neratia alba has a higher salinity tolerance than S. lanceo-
lata and is therefore found closer to the sea. However. S.
lanceolata outcompetes S. alba at lower salinities as it can
grow taller (Ball & Pidsley 1995; Fig. 10.2b) .

10.2.4 How do mangroves reproduce?

Mangroves all produce flowers. which require pollinat-
ing. A large range of flower size and method of pollination
exists, reflecting mangrove taxonomic diversity. from the
small wind-pollinated flowers of Rhizophora to the large,
beautiful blooms of Sonneratia and Bruguieru. which are
pollinated by bats, moths, birds, and butterflies.
The key problem facing mangroves living in marine sedi-
ments is dispersal of resulting seeds, which would need to
tolerate inundation and high salt-levels, or be dispersed by
the sea. Most mangroves demonstrate a degree ofvivipary;
following pollination the growing embryo remains on the
parent plant (up to several months) . The young plant
therefore does not leave the adult as a seed or fruit, but as a
fully developed seedling known as a propagule. The most
advanced vivipary is shown by Rhizophora (Fig. 10.3)-
seedlings in South-East Asia have been recorded up to 1 m
long. Mangroves put a huge amount of energy into propa-
gule production; Avicennia in Costa Rica can produce more
than 2 000 000 propagules ha- 1 yr" representing 10 to
40% of net primary production (Smith 1992) . Figure 10.3 The propagules of Rhizophora. Photograph:
Martin Attril!.
Vivipary is the process of giving birt h to live young and
is generally associated wit h animals. In plants, it refers the root system. The assemblage of organisms associated
to the seeds germinating on the plant instead of falling. with mangroves is therefore a unique mixture of animals
that colonize the mangrove forest from both the land and
Rhizophora seedlings drop from the parent plant the sea, resulting in a dynamic and diverse associated
directly into the water. Initially they float horizontally, community.
turning vertically after about a month when roots develop
(by 40 days) . The roots drag on the bottom and the seed-
10.2.5 Terrestrial organisms
ling can get stranded horizontally, or sink, where they
erect themselves vertically after rooting. If not rooted after
associated with mangroves
30 days, propagules retain buoyancy and are viable for > 1 Non-woody plants are not common in the marine section
year. although survivorship is species-specific and depen- of mangrove forests, due to the same pressures of salinity
dent on propagule weight. and waterlogged soil that affect the mangroves themselves.
So, why are mangroves only found in the tropics? The Epiphytic species that can avoid the sediment are the most
combination of three key components has a high energy successful, particularly those belonging to two groups-the
cost: being a tree, tolerating salt. and coping with water- bromeliads and the mistletoes. Insects. however. are suc-
logged soil. The environmental conditions (light limita- cessful, as anyone who has visited a mangrove swamp will
tion) in temperate regions would not allow photosynthesis know to their cost! Ants. termites, and mosquitoes are par-
all year round and so the tree would not gain enough ticularlyabundant (Hogarth 1999), with some mosquitoes
energy to survive. moving on to unusual hosts; Aedes pembaensis, for example.
Mangroves provide an incredibly complex structural has been recorded feeding off mudskippers at low tide. This
habitat, both above the water line and below it through species also has an unusual life cycle, laying eggs on the
 Chapter 10 Mangrove Forests and Seagrass Meadows
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pincers ofcrabs, after which the larvae develop in the crabs'
burrows. The major ecological impact ofinsects. however. is
their grazing activity on the leaves of the mangroves. dam-
aging the leaf and thus reducing the potential of the tree
for photosynthesis. growth. and reproduction. The seasonal
emergence of caterpillars (e.g, the moth Nophopterix) can
have particularly dramatic impacts. Grazing can also have
a controlling effect on the successful settlement and growth
of new propagules. Sousa et al. (2003) noted that settling
Rhizophora propagules were only successful in clear gaps
within the existing forest (e.g. those caused by lightning
strike) . While offering better growth conditions, refuge
from predation by the beetle Coccotrypes rhizophorae (Fig.
10Aa, b) was just as important, with seedling mortality
increasing with distance from the gap into the forest.
A range of terrestrial vertebrates has also become spe-
cialized for life in mangroves, including species of reptile
and amphibian that have developed exceptionally high
tolerance to high salinity water. One example is the crab-
eating frog (Fejervarya cancrivora, Fig. lOAc) . Amphibia
are not generally associated with marine systems, but F.
cancrivora can survive as both tadpole and adult due to
exceptional osmoregulatory abilities. The most diverse and
obvious group ofvertebrates in mangroves, however, is the
birds. which use the mangrove forest for nesting, feeding,
and as a roost at high tide. Many mangrove systems around
the world are protected specifically due to the high num-
bers of these high-profile organisms they support. The bird
fauna is a mix between waterfowl and terrestrial species
that feed off insects, etc.• within the mangrove canopy.

.- •

•
,
.
•
•
• - •

•
• •

•
1
-.'
• ••
'.
•

• •
., ~

• •
-
•
•
,.' • •.
. .,
, -•
• •

•
•• ••

• •

Figure 10.4 (a). The beetle Coccotrypes rhizophoroe, a key predator of new settling mangrove progagules (b) (with
kind permission from Springer Science & Business Media from Sousa et al. 2003). (c) The crab-eating frog Fejervarya
cancrivora, one of the few amphibians able to survive in marine conditions (copyright Nick Baker, www.ecologyasia
com). (d) The gastropod Terebrolia pa/ustris, adults of which are able to graze mangrove leaves (photograph: Christoph
Kuhne).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Crocodiles are frequenctly associated with mangroves.
Croeady/us acutus, for example, has special salt glands
that remove salt from its body which is acquired during
feeding activities.
The complex nature of the mangrove ecosystem allows
extensive niche differentiation within the canopy bird
fauna. Noske (1995) studied the feeding guilds of these
birds in Malaysia, recording 17 species from four contrast-
ing feeding guilds (neetarivores, aerial hawkers, bark for-
agers, foliage insectivores) . Within these guilds, species
avoided direct competition through small-scale spatial
variation in their distributions. For example, two species
of woodpecker were each restricted to a different tree
species (Avicennia and Sonneratia). and thus separated
within the forest due to differential distribution of the
mangroves. Within the same tree, two species of foliage
insectivores (flyeater, Gerygone sulphurea, and ashy tai-
lorbird, Orthotomus ruficeps) were spatially separated by
height, the flyeater only foraging below 4 m in the canopy
and the tailorbird at the canopy top.
Hutchinson (1957) defined a niche as an In-d imensional
hypervolume' representing a space of all environmental
factors that affect the welfare of a species. Niche overlap
can therefore potentially result in competition, niche d if-
ferentiation allowing species to coexist.
Mangrove birds can be key species for the conservation
of mangrove habitats, but full details of their ecology is nec-
essary in order to plan suitable management strategies. A
good case study is that of the scarlet ibis (Eudocimw; ruber,
Fig. 10.5) within the Caroni Swamp in Trinidad. The ibis
forages within the channels of the swamp and returns to
roost in the tops of trees at dusk-a spectacular sight when
thousands ofbirds return at once. Caroni Swamp comprises
10.2 Mangrove forests
over 5600 ha of mainly state-owned habitat, principally
mangrove. and is fed by four rivers. The ibis population
peaks in autumn/winter (up to 10000 birds); most birds
then migrate to South America leaving behind a small
breeding population (Bildstein 1990). Despite protection
of their mangrove habitat. this is a reversal of the situation
in the 1950s and 1960s, when the majority of birds stayed
to breed. so the decline in breeding numbers was somewhat
of a worrying puzzle. Non-breeding birds feed off marine
prey, such as fiddler crabs (Uca) and polychaetes (Nereis),
but it was noted that nestlings raised on such salty prey did
not develop properly, breeding adults switching to foraging
in freshwater areas inland.
Despite official protection of the mangrove forest. much
of the freshwater wetland in Trinidad had been drained for
rice production. removing the ibis's feeding grounds. As a
result the birds began to migrate to the Orinoco delta to
breed, where freshwater habitat was still available. A fur-
ther twist to the story was uncovered when high levels of
mutation (chlorophyll deficiency) were recorded in Rhi-
zophora in parts of Caroni Swamp (Klekowski et al. 1999),
traced to high levels of mercury within the sediment under
the trees. particularly those where scarlet ibis were nest-
ing. Samples of feathers from ibises and other birds in the
roost revealed that the ibis had exceptionally high levels of
mercury in their feathers (41 ppm compared with 6 ppm
for other species) . The high level of mercury in feathers was
traced to the ibis's new foraging grounds in the Orinoco.
which are key gold-mining areas . The mining operations
release high levels of toxic metals into the watershed . Mer-
cury is accumulated in feathers (Chapter 14), so when the
ibis returned to Trinidad for winter to moult, the feathers
contaminated the soil and impacted the mangroves. Many
birds demonstrate a remarkable tolerance to metal contam-
ination, being able to 'dump' metals in feathers and then
shed them, removing the toxin.
Figure 10.5 The scarlet ibis,
Eudocimus tuber, an inhabitant of
mangroves in the Caroni swamp,
Trinidad (photograph: Mike
Lane, rspb-images.com).
 Chapter 10 Mangrove Forests and Seagrass Meadows
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TECHNIQUES: Animal-attached
remote sensing

Many large vertebrates associated wi th marine and

coastal environments, like the scarlet ibis discussed
in this chapte r, move consid erabl e dist ances dur-
ing migration to breeding grounds or whilst foraging.
Traditionally, such movements have been stu died and
inferred by visual observations (e.g. the ibis flying to
Orinoco), or by tagging organisms (e.g. bi rd rings, fish
tags) and recording when these marked individuals are
seen, or caught, elsewhere. Such methodology is lim-
ited, wi th respect to its power of inference, particularly
if the organisms of interest are not easy to observe,
move long distances across oceans, or (as is the case
wi th most marine organisms) th ey are primarily under

Ireland

Wales

England

" ..-Jaw'tsJt. . ...

(a) A gentoo penguin , PygosceJis papua, with a multi-channel data recorder on its back (from Ropert-Coudert &.
Wilson 2005). (b) Recorded flight paths of Gannets (Morus bassanus) foraging from Skomer Island , superimposed
on water depth, fishing intensity, and chlo rop hyll a production (courtesy Stephen Votier and Matthew Witt).
 10.2 Mangrove forests

wate r. Conseq uent ly, met hods have been developed using
increasi ngly sophisticated miniturized technologies that
allow us to attach devices to organisms (see figu re a)
and follow them more closely. Such devices can record
exactly where organisms have been and, most recently,
simultaneously record more complex information on their
environment, physiology, and behaviour. This branch of
science is known as telemetry (Greek: tele far, met-
ros- measurement ) and the technology is termed ani-
mal-attached remote sensing or bio-Iogging fo r s hort
(Ropert-Coude rt & Wilson 2005). Bio-Ioggers can be
attached to organisms, record their movements, and then
be retrieved later (e.g. fro m seabi rds at breeding colonies;
e.q. Wilson 2003), can auto mat ically release from the
organism and be recovered (e.g. 'pop-up ' tags on large
fis h; Gore et al. 2008), or provide streamed data via satel-
lite o r mob ile receiver (Block et al, 2005) .
Bio-Ioggi ng has revo lut ion ized our knowledge about
the movements and foraging patterns of seabi rds- pre-
viously very little was known beyo nd at-sea observa tions
abo ut what b irds do away from th eir colony and w here (c) Basking shark Cetorhinus maximus (photo: NOAA).
they go. Figure (b) provides an illust ration of t he move-
ment t races obtained by suc h devices, which include GPS either side of the Atlantic. Additionally, basking sharks are
capability to record location, in this case forag ing t rips not protected outside of Europe, so east Atlantic sharks
of the gannet Morus bass anus from Skom er Island off could be exposed to hunting in w aters ou tside European
Wales. Birds flyaway from the co lony in co mparat ively protection meaning th is endangered species may be more
straight lines and change their movem ent pattern as they vulnerable than we thought
circle to forage at a range of locations. Geo- referenced Bio-Iogging can also provide information on the physi-
data can then be co mpared wi th other data sets, such as ology and behaviou r of a marine organism whilst it is div-
primary produ ction hotspots or key fishing areas, to pro- ing and foraging. For example, beak ang le senso rs have
vi de insights on the cues used by gannets to find suitable been attach ed to penguins (Spheniscus magellanicus)
feeding grounds (see also plaice vertical movements in carrying bio-Ioggi ng devices, which record every t ime
Chapter 8). the beak is open w hilst the animal is at sea, in addition
Bio-Iogg ers have also provided information on the to the range of environmental parameters (Wilson et al.
movement of large fish, such as t una (Block et al. 2005) 2003). These devices are retrieved after one fora ging
and basking sharks (Gore et al. 2008). The basking shark run, and reveal when penguins take breat hs at the surface
Cetorhinus maximus (figure c) is the world's seco nd larg- and can also determine w hen they cap ture prey under-
est shark (grow ing up to 10m) , feeding on coastal plan k- water (Wilson et al. 2002). Penguins seem to be able to
ton during the summer around productive coasts, such as predict and prepare for deep dives, as they take an extra
the w est coast of the British Isles. A series of satelli te tags breath at the surface for every 2.5 m increase in maximum
that monitor position and depth w ere attached to sharks depth (Wilson 2003, Ropert-Coudert & Wilson 2005) ;
off the Isle of Man (in the Irish Sea; Gore et al. 2008) the descen t rate is also quicker for deep dives. Penguins
to fin d ou t where the British sharks w ent in wi nter w hen have to assess the best strategy for air intake and divi ng in
they are rarely seen ; it was assum ed they headed sou th relat ion to opti mally exploit ing available prey; for example,
down the coast of Europe. However, one fem ale shark taking in more breaths allows deeper divi ng, but requires
travelled over 9500 km across the Atla ntic to t he coast more time spent at the surface. The beak sensors indicate
of Newfo und land and on route dived to a depth of 1264 that b irds inhale an ext ra breath for every fo ur fis h caug ht
m , using th e deep m id-ocean! This finding has major in t he dive beforehand, providi ng enough oxygen for prey
impli cations for ou r understanding of the species and its pursuit, but minimizing the time spent at the surface away
conservation, as it is clear fish around the globe can prob- from the prey (Ro pert-Co udert & Wilso n 2005).
ably intermingl e rather than being in discrete populations
 Chapter 10 Mangrove Forests and Seagrass Meadows
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10.2.6 Marine organisms associated the adults graze directly on mangrove leaves once their
with mangroves radula has metamorphosed to be able to penetrate the
Examples from the vast majority of marine taxa can be leaf surface.
found associated with mangroves or in the surround-
ing sediment; the sessile fauna attached to submerged Ontogenetic means relating to t he development of an
roots is particularly diverse. the roots providing a hard organism. Thus ontogenetic changes are those that occur
substratum for attachment that otherwise is restricted over the developmental life cycle (e.g. a larva will have
in a soft-sediment environment (Farnsworth & Ellison different characteristics to an adult, such as an ontoge-
1996; Figure 10.lc) . Despite domination by long-lived netic change in feeding).
groups. such as sponges and ascidians, the mangrove
root community in Florida was found to be incredibly The classic marine organisms generally associated
variable, and the assemblage composition on individual with mangroves tend to inhabit burrows within the sur-
roots changed dramatically over short time periods (l to rounding mud and. unlike those in temperate mudflats,
2 months; Bingham & Young 1995). This was thought to for example, are much more active at low tide. Two key
be related to the intensity of stochastic perturbations.
such as physical disturbance from strong tidal flow and
predation causing large fluctuations in the abundance of
certain species. This disturbance prevented competitive
processes from producing a stable. equilibrium commu-
nity. There is some evidence that this 'fouling' community
on mangroves can impact the fitness of mangrove trees
due to their smothering effect, perhaps impeding gaseous
exchange. In Hong Kong, Aegiceras corniculatum fouled
with large numbers of barnacles were found to produce
fewer flowers, the energy needed to cope with respiratory
stress perhaps affecting resources available for reproduc-
tion (Li & Chan 2008) .

Sessile organisms are those that are fixed in place so

they cannot move, such as barnacles and sea squ irts.
Stochastic means involving a random or chance variable.
For example, a severe storm is a stochastic perturbation.

Fewer marine species are associated with mangrove

trees above the water line; except for gastropod mol-
luscs. the majority are detritivores or graze off epiphytic
algae. The most abundant mangrove snails are mem-
bers of the genus Littoraria and, in a similar process to
mangrove birds. different species show distinct niche
separation within the mangrove. For example, in Papua
New Guinea, L. pallescens lives on the mangrove leaves
(where it grazes on algae rather than the leaf itself), L.
intermedia inhabits tree bark in freshwater creeks. while
L. scabra is also associated with bark. but on seaward trees
(Hogarth 1999). This species undertakes a daily vertical
migration up and down the tree in order to avoid becom-
ing totally submerged (Alfaro 2008), varying its diet as it
encounters different sub-habitats during its migration-
it is even able to ingest and assimilate zooplankton. Few
marine snails are actually able to feed on the mangrove Figure 10.6 Mudskippers: mangrove fish remarkably
leaves themselves, an exception being Terebralia palustris adapted to life out of water. Here Periopthalmadon
(Fig. lOAd) . This species demonstrates an ontogenetic is gu lping air to take it down into its burrow
change in diet, the young feeding off detritus, whereas (photographs: Toru Takita and Atsushi Ishimatsu).

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groups will be considered further here: mudskippers
and crabs. Mudskippers (Fig. 10.6) are unusual fish
related to gobies, represented by several long-named
genera (e.g. Periophthalmus, Boleophthalmus, Scartel-
aas) and are exceptional among fishes in their amphibi-
ous behaviour. They live in water-filled burrows,
emerging as the tide drops, often following the tide in
and out (Ikebe & Oishi 1996) to forage, 'walking' across
the mud surface using modified pelvic and pectoral fins.
Most are omnivores. but some species specialize (e.g.
Periophthalmodon feeds on crabs) . Mudskippers are
highly physiologically adapted to this amphibious life-
cycle, but do have to return periodically to their burrows
(Box 10.2) . However, they are remarkably tolerant to
desiccation; Periophthalmus cantonensis, for example,
can survive 2 .5 days out of water, while P. sobrinus
spends 90% of time out of water and can lose 20% of its
Figure10.7 The two main families of crabs dominant in
mangrove forests. (a) Ocypodidae: Uca lactea annulipes
feeding on a dead crab. (b) Grapsidae: Perisesarma
samawati dragging a leaf down into its burrow (photos:
Verheyden & Gillikin www.mangrovecrabs.com).
10.2 Mangrove forests
body mass yet survive (Gordon et al. 1978) .
Crabs are perhaps the most important group of man-
grove fauna. They are particularly abundant and diverse
in this habitat, have a major impact on sediment dynam-
ics through their burrowing activity, and are the main
processors of mangrove detritus. The action of crabs has
a major influence on the whole functioning of the man-
grove system (as we shall see) and so they are an example
of an ecosystem engineer. Two main families of crab are
dominant in mangroves : the Grapsidae (e .g. Sesarma,
Fig. 10.7b) and the Ocypodidae (e .g. fiddler crabs such
as Uca, Fig. 10.7a) . The grapsids have the most important
role in terms of the functioning of the mangrove ecosys-
tem, so we will look further at how they influence forest
productivity.
An ecosystem engineer is an organism that directly or
ind irectly modulates the availability of resources to
other species. It is able to modify, maintain, and create
hab itats (see Lawton & Jones 1995; and Chapter 8).
Mangrove leaves are exceptionally unpalatable for
invertebrates due to high proportions of carbon exacer-
bated by high tannin levels. Generally it is assumed that
a C:N ratio of < 17 is required to be profitable to inver-
tebrates (i.e. there is enough nitrogen in the substance
to be worth the effort), but ratios in mangrove litter can
be 70 to 100 for Rhizophora (Lee 1998). Consequently,
the majority of carbon produced by the mangrove forest
is liable to be exported away from the syste m as leaves,
or the nutrients become locked up due to slow microbial
decomposition. Grapsid crabs, however, have the rare
ability to utilize mangrove leaf litter as a prime food
source, despite its apparent unpalatability, but the diges-
tive mechanisms for this important feeding habit have
yet to be elucidated. A few species, such as S. messa, are
able to feed directly off fre sh leaf material; S. leptosoma
has even been observed making daily vertical migra-
tions up mangrove trees to graze on live leaves (Van-
nini et al. 1995). Grapsid crabs also store leaves within
burrows (Fig. 1O.7b), so fulfil an important function in
retaining carbon material within the mangrove syste m .
Robertson (1986) concluded that S. messa populations
could remove or store up to 28% of all Rhizophora lit-
ter, with major implications for the reduction oforganic
matter export from mangrove forests and thus the flow
of energy into coastal systems (Lee 1998) .
Grapsid crabs also have a major ecological impact
through their burrowing activity (bio turba tion; see also
Chapter 8), which can influence the chemical make-up of
 Chapter 10 Mangrove Forests and Seagrass Meadows
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Box 10.2: How mudskippers aerate
their burrows
Mudski ppers' burrows are constructed in highly anoxic
sediment and measurements wi thin burrows have
shown that the wa ter in deeper chambers contains
practically no oxygen at all. It has therefore been some-
wh at of a puzzle as to how mudskippers cope with
these inhospitable conditions, part icularly as eggs are
laid and reared in ap parently hyp oxic w ate r. Ishimatsu
et al. (1998) noted that wal king near Periophthal-
modon burrows caused bubbles of gas to be released
up the main shaft. Further observations revealed how
mudskippers oxygenate d their living quarter s- before
ente ring the burrow the fi sh fi lls t heir mouth cav-
ity with ai r (Fig. 10 .6 ) and trans ports this down
t he burrow, often making ret urn trips. Air released in
the breeding chamber becomes trapped, providing an
oxygen reservoir for the fish and develop ing embryos
that are often laid on the roof of chambers, w here air
w ill accumulate.
0, 80% surtece ---' l --
Breeding chamber -
eggs on roof
02 < 3% surfoce
30cm
the sedimen t and subsequent forest productivity. This is
exemplified by a study in Queensland, Australia (Smith et
al. 1991 ), which investigated the impact ofremoving crabs
from mangrove areas. The st ud y includ ed three treat-
ments: a removal area (R) , where all crabs were trapped
and removed; a disturbance area (D), where activity was
undertaken but crabs not removed (to see if the physical
disturbance of the experi ment had an effect, termed pro-
cedural control) ; and control areas (e ) , which were left
alone . Levels of so il chemicals were measured and forest
production assessed by the fall of stipules (for growt h,
stipules are outgrowths of the leaf base, whic h are shed as
the leaf grows) and the number of m ature propagules on
trees (for reproductive outpu t) . Bu rrowing was found to
have significant effects on the sed iment chemistry, w ith
increases in sulphide and ammo nia in exclusion plots due
to lack of aeration by burrowing, which would normally
allow oxidatio n to nutrients more useful to plants. There
were also significant impacts o n forest productivity, w ith
higher growt h (stipule fall ) and propagule production in
areas that included crabs, particularly during the m ain
su mmer growing season (e. g. Fig. 10 .8) .
The conclusions from work u nd ertaken in Australia
and SE Asia are unequivocal: crab ac tivity is key to the
healthy functioning of mangrove forests through recyc-
ling of organic m aterial and bioturbation. However,
Mcivor and Sm ith (1 995) assessed the ecological roles of
crabs in Florida mangrove forests, where the family Xan-
thid ae is more common than grapsid crabs . Xanthid crabs
do not have leaf-processing abilities, so it was concluded
that in the Americas, crabs do not have a significant role
in leaf breakdown, the latter is presumably achieved pri-
marily by microbial action .
~
~
- 4
c=
~
c
- 3
--
~
~ Crob removal
~
--
~
E
c
~ 2
E
~
z
0'--( DR ( 0R ( 0R ( 0R ( 0R ( 0R ( 0R
Nov Dec Jon Feb Mar Apr Mav
Figure 10.8 The results of crab-removal experiments
on mangrove forest productivity. The production of new
propagules was greater in areas that included crabs
due to their bioturbating activities (Smith et al. 1991).

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10.2.7 The wider role of mangrove
ecosystems
Mangrove forests as a whole provide a range of valuable
functions that influence surrounding coastal systems, and
impact on human activities such as fisheries (Chapter 12).
Two of the most important are their potential role in nutri-
ent input and energy flux between mangrove and marine
systems, and the provision of a nursery for fish species
that recruit to local fisheries and coral reefs.
Despite the efforts of crabs, much detrital material
from mangroves is exported out of the swamp to sur-
rounding systems, particularly from fringing mangroves
(Robertson et al. 1992), providing a large potential source
of food. Jennerjahn & lttekkot (2002) estimated that 46
x 10 12 g C/yr (i.e. 46 000 000 tonnes!) of mangrove car-
bon reaches the ocean each year, representing 11 % of all
terrestrial carbon entering the marine environment. The
relative value of this material to marine organisms within
adjacent systems is inconsistent. due to the general unpal-
atibility of the tree leaves to marine animals. The use of
stable isotopes (Chapter 4 .3 .2) has proved valuable in
assessing how important mangrove detritus is compared
with other carbon sources. Schwamborn et al. (2002)
investigated the uptake of different carbon sources by
crustacean larvae in a tropical estuary to which a large
amount of mangrove detritus was exported. They found
the contribution of mangrove carbon to larval nutrition to
be negligible, with only the zoeae of porcelain crabs hav-
ing a significant proportion of mangrove carbon in their
tissues. A similar. though perhaps even more unexpected.
result was found in the tropical Embley River estuary in
Australia (Loneragan et al. 1997). Stable isotope analy-
sis was utilized to investigate whether seagrass- or man-
grove-derived carbon were important carbon sources for
commercial prawn species in the outer estuary. Organic
matter in the sediment was found to correspond to the
main local source. but this pattern was not reflected in
the tissues of the prawns. While prawns that inhabited
seagrass beds did seem to rely completely on seagrass-
derived material, mangrove-dwelling prawns did not
depend on carbon from mangroves, but utilized either
algae or seagrass material.
Mangrove leaf litter does not even seem to be valuable
in nutrient-poor habitats, and Lee (1999) demonstrated
that additions of mangrove detritus to sandy substrata did
not enhance the marine benthic community. perhaps due
to the high associated tannin levels. It therefore appears
that carbon from mangroves is rarely directly utilized by
marine organisms, the carbon probably entering the food
web following bacterial decomposition and recycling.
10.2 Mangrove forests
However, mangroves do have a clear physical role influ-
encing the flux of material to coastal systems by provid-
ing a buffer for land run-off, e.g. from storms. During the
terrible Indian Ocean tsunami of December 2004, areas
in SE India where mangroves had been cleared suffered
more damage than adjacent coasts where mangroves
remained (Danielsen et al. 2005) . This was a tragic illus-
tration of the important role of mangroves that act as
'green' barriers to coastal erosion processes. In particu-
lar. mangroves reduce the amount of sediment washed
into the coastal region, which would otherwise negatively
impact adjacent reef systems through increased turbid-
ity that reduces light penetration (Hogarth 1999); where
mangroves have been removed (e .g. for shrimp farming)
there are potential consequences for the health and sur-
vival of local reef systems.
Tannins, among many other chemicals, have been pro-
duced by plants in an 'arms race' with insect grazers.
Such chemicals are unpalatable, so help protect the
plant. Tannins are responsible for the astringent taste of
unripe fru it and red wine.
Mangroves have a clear positive role in the provision
of recruits to local fisheries and, in particular, coral reef
systems. This conclusion had been somewhat anecdotal
(Baran & Hambrey 1998) due to the presence ofjuvenile
coral reef fish in mangrove systems, but Mumby et a1.
(2004) have now unequivocally demonstrated the value
of mangroves to coral reef fish populations. Working in
Belize, they assessed the assemblage of fish present on
replicate reefs with or without a rich mangrove stand
nearby (Fig.10.9a) . There were marked differences in the
reef-fish communities between the two sets of sites (Fig.
10.9b), and mangrove extent was the dominant factor
that affected the fish assemblages. In particular, the bio-
mass of fish species known to use lagoons or mangroves
as juveniles was enhanced in reefs near to mangrove-rich
areas. Mumby et al. (2004) concluded that the main rea-
son for these results was that, once fry are large enough
to leave seagrass habitats, mangroves provide a refuge for
juveniles from predators and a plentiful food supply that
increases juvenile survivorship and recruitment to coral
reefs. They noted that the largest herbivorous fish in the
Atlantic. the parrotfish Scarus guacamaia. whose life his-
tory critically depends on mangroves, has become locally
extinct since mangrove removal. It is clear that conserva-
tion policies targeted at protecting coral reef habitats also
need to consider nearby mangrove systems.
 Chapter 10 Mangrove Forests and Seagrass Meadows
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(a) Mangrove ,xlenl (rirh" seart') N -------. I

Reef ,ysl,m T
8 TU L G (
101_102 km
33 36-11 79-84 25 46-57 25
lit,
10°_10 1 km
Transect
10-2_10 -1 km - .
•••
-
.. --
---- • ••
---
-- -.-
•••

Mangrove-rich profil' Mangrove-scorce profile

(h)
Stress: 0.19

a GE
L
aa GW
a GW aL

Figure 10.9 Experiment by Mumby et al. (2004) in Belize to assess how impo r tant mangroves are as a
nursery ground for coral reef fish. Coral sites, w ith and without associated mangroves, were studied (a) and
it was clear that coral reefs with nearby mangroves had a d ifferent fish community w ith a higher b iomass. (b).
Mu ltidimensional scaling ord ination showing the similarities between fish communities at each site--the closer
the sites on th is 'map', the more similar their fish assemblages. Blue squares are all the mangrove-rich sites.

10.3 Seagrass meadows
10.3.1 What are seagrasses?
Seagrasses are the only truly marine angiosperms. gener-
ally growing in soft sediments in shallow coastal waters.
Below ground there is a network of rhizomes and roots
(Fig. 10.10), the rhizomes spread horizontally joining
individual plants, while the roots extend vertically into
the sediment. The root-rhizome network of the Mediter-
ranean Posidonia oceanica can build up over hundreds of
years. forming a peat-like 'm a tte' several metres thick
(Borg et a1. 2006), which has even been used as a tool for
dating ancient wrecks due to its known growth rate. Above
ground the seagrass is made up of discrete shoots that
emerge from the rhizome and comprise several strap-like,
lam ina te leaves that grow from the base of the shoot (the
leaf sheath), although the genus Halophila has rounded
leaves Fig. 1O.l1b. The number and height of leaves var-
ies considerably between species. the longest leaves (over
6 m) belonging to the Japanese species Zostera caulescens
(Aioi et a1. 1998; Fig. 10.11c, d) . In suitable conditions
(see 10.3.2), seagrasses can form extensive meadows
covering la rge areas of seabed (e.g. the seagrass bed
within the Spencer gulf near Adelaide. Australia. covers

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- - leaves
- - leaf sheath
- - leafsear
(= node)
- - Internode(vertical rhizome)
Apical meristem
(horizontal rhizome)
Internode
. __ (horizonlol rhizome)
- root
over 4000 km-; Keuskamp 2004) with densities of shoots
> 1200 m-2 (e.g, Posidonia oceanica; Borg et al. 2006),
creating one of the most important and extensive subtidal
marine habitats in the world.
The taxonomy and origin ofseagrasses has been subject
to much debate, but seagrasses are clearly polyphyletic
and generally assigned to two families, Potamogetona-
ceae and Hydrocharitaceae, neither of which is related
to the grasses familiar on land. Fossil evidence suggests
that seagrasses first appeared in the marine environment
around 100 million years ago. the oldest Cretaceous fos-
sils include the genus Posidonia. but their ancestors are
uncertain. Two candidates have been put forward : coastal
plants (e.g. saltmarshes, mangroves) and freshwater
hydrophytes. Some seagrasses have lignified stems and
two genera are viviparous. linking them to mangroves,
while freshwater plants show many of the adaptations
required to survive in the marine environment, such
as basal meristems and lacunar gas transport systems
(Hemminga & Duarte 2000) . Certainly it seems likely
that the seagrass habitat has evolved several times over
the last 100 million years (perhaps from both ancestral
routes), with the genera Phyllospadix (Fig. 1O.lla) and
Enhalus appearing significantly later than other sea-
grass groups (Larkum & den Hartog 1989). However
they have evolved, seagrasses possess three key attri-
butes that enable them, uniquely. to colonize the marine
environment (Hemminga & Duarte 2000) : (a) leaves
10.3 Seagrass meadows
Figure 10.10 Schematic d iagram
representing the main structural features
of a seagrass.
with sheaves adapted to high-energy environments; (b)
hydrophilous, and thus submarine, pollination; and (c)
extensive lacunar systems that enable transport of oxy-
gen to the below-ground structures in anoxic sediments.
Polyphyletic-a useful grouping of organisms that has
more than one evolutionary root form. For example,
'winged vertebrates ' would include birds and bats, but
each has very different origins. Hydrophyte a true
plant that has fully adapted to live in water. Hence also
hydrophilous.
The diversity of seagrasses is surprisingly low. with
only c.50 species represented worldwide (Hemminga &
Duarte 2000), although this figure has generated much
discussion. The majority of the species are contained
within three of the oldest genera: Zostera, Posidonia, and
Halophila . There is little evidence that seagrasses have
ever been more diverse. a major reason perhaps being
due to the very low rate of sexual reproduction (10.3.3)
and dispersal restricting gene flow. However, seagrasses
are exceptionally plastic in nature, and also show much
genetic diversity even within meadows (Reusch et a1.
1999a), which means it remains unclear how many spe-
cies of seagrass exist (Box 10.3) . Most seagrass meadows
are monospecific, particularly in temperate regions. but
tropical meadows have been reported with up to 12 sea-
grass species present (Duarte 2001).
 Chapter 10 Mangrove Forests and Seagrass Meadows
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10.3.2 Where are seagrasses found?
Unlike mangroves and saltmarshes, seagrasses are found
in all the world's coastal seas except for Antarctica (prob-
ably d ue to ice scour) and cove r approximately 0. 1 to
0.2% of the global ocean (Duarte 2002) . Some species
have extensive d istributions , such as Zostera marina (eel-
grass) , which occurs in Europe from the White Sea to the
Mediterranean, on both coasts of Nort h America and the
Nort hwest Pacific (Gree n & Short 2003). Ot her species
are more restricted . Posidonia ocean ica is the dominant
seagrass across the Mediterranean, bu t is not found else-
where, whereas some seagrasses have a very narrow range
indeed ; P kirkmanii occurs only in a sm all area off SW Aus-
trali a. The peak of d iversity occurs in Malaysia, and sea-
grass species richness declines with distance along m ajor
cur rents from this point (Muka i 199 3) , resulting in su g-
gestions that this may be the centre of origin for seagrasses
(Hemminga & Du arte 2000) .
With in their biogeographical range, much of the coast
is devoid of se agrass due to unsuitable habitat cond itions;
so individual se agrass beds can potentially be separated
by large d istances of inhospitable coast. The vast m ajor-
ity of se agrasses re quire a soft substratum that will en able
Figure 10.11 Examples of different seagrass forms.
(a) Pbyttospadts iwatensis, part of a genus that can
grow on rocky s ho res and are known as s urf grasses
(photograph: Daniel Mosquin). (b) The broad-leaved
Halaphilia ovalis (photograph: Keith D. P. Wilson).
(c) The world 's largest s ea g rass, Zostera caulescens
from Japan. The person in (d) is 1 .83 m tall (photos:
Akihiro Dazai, Shizugawa Nature Center).
Box 10.3: Diversity of seagrass: 1
how many species are there?
Seag rasses are morp ho log ically plastic, a te rm that
describes speci es that ap pear very different depend-
ing on the envi ronment to w hich they are exposed.
As classification is generally based on morphological
features (e.g. shape of leaf margins), there is around
a 20% uncerta inty w ithin the seag rass world as to
how many species of seag rass actually exist, wit h
most arguments focused within the three main gen-
era (Hafop hila, Zostera, Posidonia ). Molecul ar tax-
onomy (e.g. the use of DNA markers) has he lped
the confusion to some degree and ten ded to reduce
the number of existing speci es defined using mor-
pho logical featu res. For example, intertidal Zostera
marina looks d ifferent from subtidal plants and in the
UK has been considered a separate species (Z angus-
tifolia) , although genetic evi dence from mainland Europe
suggests it is just a plastic form of Z. marina. Outside
the UK the speci es is not recognized . However, the
use of genetics has raised further problems, and has
drawn into do ubt the identity of some genera. For
example, the genetic distance between Heterozostera
and Zostera is similar to that between species of Zos-
tera, suggesting th at one genus shoul d include both
these taxa (Hemminga & Duarte 2(00) . Whatever the
final total of species, it is clear that seagrasses are a
very low-diversity group.

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the penetration of roots; although some species can grow
on rocks (e.g. Phyllospadix, Posidonia) this is unusual and
most only develop on sand or mud.
However, some features of soft sediments make plant
growth impossible, particularly highly mobile or exposed
sediments that can result in burial of colonizing sea-
grasses, or those with very high inputs of organic mat-
ter resulting in reduced, anoxic sediment conditions.
Paradoxically, the presence of a seagrass meadow on
soft sediment can increase the sediment organic content,
from both the seagrass production itself and the capture
of other detrital material. Seagrass beds can also change
the particle size distribution of the sediment. the baf-
fling effect of seagrass blades slowing water currents and
enhancing the deposition of fine sediment particles. Sea-
grasses therefore have a very complex relationship with
the sediment, which we are only starting to untangle.
Seagrass is also limited by the light levels, which must be
above the threshold where photosynthesis is still possible.
As a result, the maximum depth where seagrass mead-
ows are found is related to their compensation point.
This depth is controlled by the clarity of the water, so in
comparatively turbid. temperate regions. seagrass beds
are found at depths shallower than in clear. tropical or
Mediterranean water. Zostera marina in Europe is gener-
ally found above 6 m depth, whereas Posidonia oceanica in
Figure 10.12 (a) An intertidal seagrass meadow of Zostera marina at Salcombe, SW England. (b) Close up of Z.
Marina plants. (Photos: Martin Attril!.)
10.3 Seagrass meadows
the clear waters off the island of Malta has been recorded
as far down as 40 m (Borg et al. 2005) . High-turbidity
water can therefore be a limiting factor for seagrass colo-
nization and growth.
While the lower level of a seagrass bed is set by light
levels (unless limited by habitat availability, e.g. the pres-
ence of coral reefs in the tropics). factors controlling the
upper limits are less well studied (Hemminga & Duarte
2000) . Several seagrass species, such as Zostera marina
and noltii, Phyllospadix, and Halophila spp., can form
extensive intertidal meadows (Fig . 10.12) . Desiccation
can be minimized by the structure of the bed. dense con-
tinuous seagrass trapping water beneath the flat-lying
leaves. Ultraviolet damage is also thought to be a major
factor preventing intertidal survival, particularly of sub-
tidal species, while in some regions upward extension
may be prevented by physical factors such as wave expo-
sure. ice scour, or the lack of suitable substratum.
The depletion of the ozone layer primarily through our
use of CFCs has allowed increased fluxes of UV radi-
ation , in particular the damaging UVb. There is much
speculation abou t its effects on plants, but concerns
include inhibition of photosynthesis and the cost of tis-
sue repair and production of blocking compounds (see
also Chapter 12).
 Chapter 10 Mangrove Forests and Seagrass Meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Many seagrasses show a tolerance to a wide salinity
range (for example, Z. marin a occurs in full -strength
seawate r and also down to a salinity of 5 in the Baltic),
and seagrasses often are a major feature of estuaries and
hypersaline lagoons (Chapter 5), although the majority of
species perform optimally und er fully marine conditions.
However, success in estuaries and similar coastal systems
m ay be limited by high levels of plant nutrients in the
water, whic h is becoming an increas ing p roblem through
agr icultural run-off (Chapter 14). Such high levels of, for
example, nitrate and ammonium, can d irectly affect the
growth of seagrass (Short et al. 1995), but it also influ-
ences the competitive balance between the seagrass pro-
d uctivity and that of algae associated with the seagrass
meadow. represented by an epiphytic assemblage grow-
ing on the leaves or by macroalgae that grow alongside,
or amongst, the seagrass meadow.
ing the exte nsive natural Posidonia ocean ica bed s with
consequen t loss of large areas of seagrass coverage (see
Cu rrent Focus box). While not so dramatic, the Japanese
seaweed Sargassum m uticum poses a threat to native Zos-
tera beds in Nort h-west Europe. While direct competition
under natural cond itions does not appear to occur, physi-
cal damage to seagrass bed s (e.g. from boat anchors) can
allow the colonizatio n of Sargassum, and once established
it appears that seagrass cannot reclaim the space. Large
beds of Zostera in NW France have been lost to Sargassum
by this mechanism (Givernaud et al. 1991 ) and it wo uld
also appear that seagrass beds may, unfortunately. aid the
settleme nt of Sargass um, the seagrass cano py can trap
floating fragments of the seaweed that can then become
attached and grow wit hin the root-sedimen t matrix
(1\veedley et al. 2008) .

20 0 r - - - - - - - - - - - - - - , BO
Epiphytes are organisms growing on the surface of
plants, but not deriving nutrition from them. Generally
the term is used for other plants (including algae), but
sessile animals such as bryozoans can also be termed
MmroQ Igee
epiphytes. 150 60
-
0

Williams and Ruckelshaus (1993) d emonstrated that o0- --=

E

Zoste ra marina showed a saturation-type response to

--~ ~

-
~
~
increasing nitrogen levels; above sedimen t ammo nium
conce ntrations of 100 umol l-' the seagrass was unable -- 100 40
0
~

-
~
o 0
E
to increase growt h rates. Once ove r such a threshold. o E
= ~

E
algal growth may con tinue. resulting in a shift in domi- . ~

nance w it hin the seagrass bed (Short et al. 199 5). This 20 ""
can have detrimental results for the seagrass, in particular
due to light limitation imposed by the algae reducing sea-
grass productivity and. ultimately. survival. Hauxwell et
al. (200 1,2003) demonstrate d that eelgrass (2. marin a ) Eelgrass
o o
was now absen t or d isappeari ng in all Waquo it Bay estu-
aries (Massachusetts) d ue to excessive algal growt h (Fig. o 100 200 300 400

10.1 3), exceptthose that received the lowest land -derived
nitrogen loads.
Introduced algae are also posing a severe threat to
seagrass coverage in Europe. The alga Caulerpa taxifolia
has been acciden tally introduced to the Med iterranean
from sout hern France and is spread ing rapidly. smot her-
Nilrogen loading role (kg N·h,l.y" )
Figure 10.13 The relationship between the growth of
seagrass and macroalgae at increasing levels of nitrogen
loading, indicating algal biomass increases relative to
seagrass under increasing nutrient co nd it io ns.

CURRENT FOCUS: Invasive species
Ever since humans have been moving round the world
we have been transporti ng species with us, either
intentionally for cultivation and recreational hunting,
or as stowaways in, for example, the ballast water of
ships. A vast range of species have therefore been
introduced into terrestrial, freshwa ter, and marine
regions across the globe where they are not native, with
over 500 such species established in the coastal waters
of the USA, for example. Where conditions are similar to
native areas, the species can be incorporated into the
 10.3 Seagrass meadows

flora an d fauna of the new region: a significant number

of familiar terrestrial species in northern and southern
latitu des have been introduced (e.g. rabbits and green
shore crabs). A large proportio n of introduced species
do not cause significant problems, but this is not the
case wh en an introduced (or 'alien') species becomes
invasive. These organisms can outcompete, or outgrow,
native fauna and flora causing large changes in native
biodiversity and often fo rm very large populatio ns
indeed. Consequ ently our introduction of invasive
species is now seen as one of the main global th reats
to biodiversity, even leading to the ter m 'invasional
meltdown' (Grosholz 2004). In response to this
increasing threat to biodiversity, governm ent agencies
have been set up to deal with this crisis, such as the
US Departm ent of Agricul tu re National Invasive Species
Informat ion Center (http://www.i nvasivespeciesinfo.
gov). This body has clearly defined invasive species
as: (1) non-native (or alien) to the ecosystem under
consideration and (2) whose introduction causes or is
likely to cause economic or environmental harm or harm
to human healt h.
What makes an introduced species become invasive?
Certai n traits seem key to invasion success (Kolar &
Lodge 2001), including: the ability to reproduce rapidly
and both asexually and sexually; fast growth; high disper-
sal abili ty; the ability to deal with a wide range of envi-
ronmental conditions and food types, and release from
nat ural predators and parasites that con trolled popula-
tions in nat ive areas. In particul ar, an important factor in
the persistence of invasive species is termed propagule
pressure: the rate at which a species is introduced to
the ecosystem. Successful establishment has been corre-
lated with th e number of introduction events and number
of organisms introduced (or inoculum size; Drake et al.
2005). Therefo re, it is more likely a species beco mes
invasive if humans are continually introduci ng it to new
areas.
The Invasive Species Speci alist Group (http:/ /www. Three of the world 's top 100 worst invasive species:
issg.org) has produced a Top 100 of the world 's worst (a) Caulerpa taxifolia (photo: NOAA), (b) The South
invasive species, which includes a range of organisms African native ribbed mussel ; Au/acomya ater (centre),
causing major problems in marine habitats, such as the surrounded by the invasive blue mussel Myti/us galfo·
seaweed Cau/erpa taxifofia (a), the mussel fv1yti/us galfo- provincia/is (photo: Martin Attrill), (c) Carcinus maenas
provincia/is (b) and the crab Carcinus maenas (c) . (photo: Ar Rouz).
Cauferpa taxifofia is a popular decorative alga used in
fish tanks and seems to have been introduced acciden- exceptionally fast and is able to cover 100% of the sea-
tally into the Medi terranean in 1984 from the Oceano- bed, smo thering all native sessile invertebrates, algae,
grap hic Museum in Monaco. By 2000 it had colonized and, in particular, the seagrass Posidonia oceanica. Inva-
13 1 km' of seabed at 103 locations along 191 km of sion of seagrass beds seems particularly successful when
coast (Occhipi nti-Ambrogi & Savini 2003). The aquarium seagrass has already experienced some decline due to
strain of th e alga (cap tive bred to be resistent) grows other human pressures; dense meadows seem to rest rict
 Chapter 10 Mangrove Forests and Seagrass Meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
C. taxifofia to the bed margins, but impacted beds seemed
too fragile to resist the progagule pressure (Occhipint i-
Ambrogi & Savi ni 2003) and competitive ability (Pergent
et al. 2008) of the invader. C. taxifolia has been rep lacing
Posidonia across the Mediterranean where it can invade
damaged beds, vastly reducing native speci es' diver-
sity and fish hab itat; the seawee d also prod uces toxic
substances (caulerp enynes) aiding its invasion. More
recent ly, the same Caulerpa strain has been documented
in Californi a (Jousson et al. 2000), where $US6 mill ion
w as spent up to 2004 trying to eradicate it, and in 2002
it appeared in Sydney Harbour. A second Caulerp a spe-
cies (C racemosa) has more recently been introduced to
the Mediterranean from Australia, the first record being
off Lybia in 19 9 0 (Klein & Verlaque 2008) and in the fol-
lowing 17 years it has spread quickly to 12 countries and
all maj or islands in the Mediterraean. This invasion event
could be one of the most serious in the Mediterranean
(Klein & Verlaque 2008), but has not received as much
attention as C taxifolia.
f\1ytilus galfoprovinicialis is native to the Mediterranean
and surrounding areas, but in 19 7 4 was introduced to
the west coast of South Africa, most li kely through bal-
last w ater. It spread dramatically (about 11 5 krn -year" ")
and now occupi es available rocky shore along the whole
of the west coast of South Africa and at least the south-
ern half of Namib ia (Branch & Steffani 2004). Its rapid
spread w as due to a series of key features of the invader
itself and also the nat ive communi ty, such as t he high
productivity and strong wave action of the South Afri-
can West Coast, a lack of predators and parasites, and
the mussel's fast growth and high rep roductive output.
Indigenous mussels have been competi tively displaced
in the interti dal, particularly the endemic species Aula-
comya ater, and the new mussel matrix has also affected
the grazing ability, and thus population, of som e native
limpet speci es such as Scuteflastra argenvilfei (Branch &
Changes to the global cover of seagrass have raised
much recent concern, Green and Short (2003) stating that
15% of seagrass worldwide had been lost over the 10-year
period up to 2003, due mainly to a combination of human
activities. However, seagrass within the northern hemi-
sphere, particularly Z. marina, was devastated du ring the
1930s by a mysterious wasting d isease that killed massive
areas of seagrass and resulted in the loss of many beds in
Europe and Nor th America. The culprit was identified as
a slime mould Laby rinthula zosterae, causing brown spots
to appear on the leaves, whic h spread to the shoot wit hin
weeks. Many of the surviving beds were located wit hin
Steffani 2004). However, this invasive species has had
some unexpected positive effects. The African black oys-
tercatcher, Haematopus moquini, is one of Afric a's rarest
wadi ng b irds, wi th a population that was as low as 3000
pai rs (Coleman & Hockey 2008). The rapid colonization
of rocky sho res by large f\1. galfoprovincialis has provided
a new, more accessible, and widesp read food source for
t he oystercatcher, result ing in an increase in t he popul a-
t ion size and a much more successful breeding rate: in
19 7 8 only 10 % of pai rs raised two chicks, which had
increased to 30% by 1988.
Carcinus maenas is the most common intertidal and
estuarine crab in northern Europe, yet its introduction to
other parts of the world through ballast and aquaculture
has caused large problems, particularly in estuaries along
t he east coast of the USA where it w as first recorded in
181 7 . This crab is now found on the west coast of the
USA , whe re it grows larger than in other areas; it also
occu rs in Aust ralia. In general, Carcinus is a maj or pest
of the shellfish industry. In the USA, Carcinus potentially
interacts wi th th e native estu arine blue crab Calfinectes
sapidus, th e two crabs' abundance being neg atively cor-
related, although Calfinectes may in this case show resis-
tence to the Carcinus invasion as the European crab is not
found in Ch esape ake Bay w here Caflinectes is com mon
(DeRivera et al. 2005). However, in California, Carcinus
predation has affected the spread of another introduced
species. The clam Gemma gemma has been present in
Bodega Harbor for nearly 50 years wi thout showi ng signs
of be ing invasive, but t he situa tion changed upon t he
arrival of Carcinus in 1989 (Grosholz 2004) as the crab
beg an preferentially predati ng th e nat ive Nutricola clams
freeing up space on the shore for Gemma to spread. It is
clear that invasive species can also have indi rect effects
and positive interactions wi th other alien species that may
be difficult to predict.
estuaries, from where d ispersal and recolonization could
occur. It has been suggested that the salinity tolerance of
the seagrass was greater than th at of the slime mould,
allowing some beds to survive in reduced salinity refug ia
(Durako et a1. 2003) .
10.3.3 Reproduction and growth of
seagrasses
Seagrasses can reproduce both sexu ally and, rarely,
asexually (e.g. through f r agments of drifting r h izom e) ,
the prominence of sexual reproduction within beds vary-
 10.3 Seagrass meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

ing widely across species and geographical location. The coatings of Zostera) . However. evidence suggests they do
majority of seagrass genera are dioecious, which is rela- not disperse far from source. 80% of Zostera seeds from a
tively rare in terrestrial angiosperms and has been sug- Chesapeake Bay population remaining within 5 m of their
gested as a way of avoiding self-fertilization (Hemminga bed of origin (Orth et al. 1994). The seedlings themselves
& Duarte 2000) . may also be a dispersive stage, while in the two vivipa-
rous genera (Amphibolis and ThalcLssodendron), the seed-
Dioecious-having separate male and female plants. lings develop attached to the mother plant. However, it
would appear that the survival of both seeds and seed-
Flowers tend to be produced seasonally, even in tropi- lings is very low indeed, the probability that any given
cal species where it often coincides with very high spring shoot will successfully establish a new seagrass genet is
tides, and is generally controlled by temperature (Ramage <0.00001 (Hemminga & Duarte 2000) . Sexual reproduc-
& Schiel 1998), which facilitates simultaneous flowering tion is therefore exceptionally inefficient within seagrass,
ofseagrasses across wide areas. However. only a small pro- resulting in clonal propagation as the major method of
portion of a bed will flower at once « 10%), and there is seagrass meadow survival. The consequence is ancient
great variability between years, making flowering a com- beds (as outlined earlier) and highlights how potentially
paratively rare event in seagrass beds. with minimal allo- vulnerable existing seagrass beds are; recolonization is not
cation of carbon to this process by the seagrass (in direct straightforward.
comparison to mangroves), resulting in the existence of Established seagrass patches grow through the lateral
very old clones in some areas . One extensive single Zostera extension of the below-ground rhizomes into uninhabited
marina clone in the Baltic is thoughtto be > 1000 years old surrounding soft sediment (as long as the conditions of
(Reusch et al. 1999b) and represents the largest known that sediment favour seagrass growth), eventually pro-
marine plant, covering a total area of 6400 m 2 and weigh- ducing a new shoot unit, or ramet. Growth rates vary
ing approximately 7000 kg! In contrast. flowering occurs considerably between species but tend to be related to the
relatively commonly within intertidal Zostera beds, such size of the seagrass, with a negative relationship between
as those in Northern Ireland. It appears that disturbance rhizome diameter and horizontal extension rate (Duarte
and stress enhance seagrass flowering, and thus sexual 1991; Fig. 10.l4a) . AI; a result, the smallest species, such
reproduction, compared with more stable subtidal beds, as Halophila ovalis (Fig. 10.lIb), can spread up to 5 m y '
which favour vegetative growth. and are often regarded as pioneer species in multi-species
Practically all seagrass species have hydrophilous meadows. Rhizomes can also branch. allowing a two-
pollination, a development within seagrasses that allows dimensional colonization of new sediment.
survival in marine systems, pollen being released into the
water column to fertilize female flowers (Hemminga & The time between the development of two seagrass
Duarte 2000) . The resulting seeds vary in their disper- units is known as the plastochrone interval and is a use-
sal ability; some species have negatively buoyant seeds ful measure to compare growth rates between species
(e .g. Halodule spp.) that will not travel far, while others and under different environmental conditions.
possess structures that enhance buoyancy (e.g. the seed

(oj 1000 10
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611/90 911/90 12/1/90 313191 611/91 911/91 12/1/91 3/2/92 6/1/92 9/1/92
Rhizome die meIer (em) Dete

Figure 10.14 (a) The growth of seag rass rhizomes of different sized seagrass species smaller species w ith thi nner
rhizomes grow faster. (b) Seasonality in seagrass prod uctivity-Zostera marina off Washington State, USA.
 Chapter 10 Mangrove Forests and Seagrass Meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Leaf growth can be highly seasonal in temperate spe-
cies, relating to temperature and especially light levels.
A study on Zostera marina on the west coast of the USA
exemplifies such seasonal patterns of production (Nel-
son & Waaland 1996; Fig. 10.14b), peak summer values
being 6.5 times those in winter. Unlike the beds them-
selves, leaves do not live particularly long, with a lifes-
pan generally shorter than land plants (Hemminga et al.
1999) . Leaf age also varies considerably between species
(up to a year for Posidonia oceanica), but most will shed
leaves throughout the growing season (e.g, Zostera mean
leaf lifespan is < 100 days), resulting in large amounts of
plant organic matter entering the coastal ecosystem; in
dense seagrass areas (e.g. parts of the Mediterranean)
much of this litter can wash up on beaches, where in
some locations it has been harvested by local people for
use as an agricultural fertilizer.
10.3.4 Factors structuring the
assemblages associated with
seagrass
Seagrass meadows make available a high level of physical
structure within what is usually a comparatively homog-
enous, featureless subtidal habitat. Additionally they are
highly productive systems (from both the seagrass and
the associated algae) and so provide potential food and
shelter for a wide range of organisms. Many studies have
demonstrated that seagrass beds have a richer associated
community than surrounding soft sediments. includ-
ing invertebrates living in the sediment and on seagrass
blades (Connolly 1997; Lee et al. 2001), larger mobile
invertebrates (e.g. crabs, cephalopods), and certain fish
that shelter within the meadow (Jackson et al. 2001) .
This is perhaps not surprising as seagrass clearly provides
a complex structure within which animals can hide from
predators, and also provides completely new habitats (e.g.
the leaves) that will host species not found in soft sedi-
ment. Lee et al. (2001) highlighted this, by demonstrat-
ing that all invertebrates recorded living in soft sediments
off Hong Kong were also present in adjacent seagrass
beds, but 48 additional species were only found associ-
ated with seagrass. However. the structural complexity
of the habitat may not be the only factor influencing this
boost in species diversity. Edgar (1999) undertook some
elegant experiments with artificial seagrass and found
that a much richer community developed in treatments
that also included seagrass detritus than those with sim-
ply artificial leaves. He concluded that small invertebrates
required the provision of food and showed little depen-
dence on solely the seagrass structural characteristics.
Some fish are only found in a certain habitat, such as
seag rass beds. These are termed obligate inhabitants,
and wo uld disappear with loss of habitat. Other fish use
the bed o ut of 'cho ice ' at certain times of the day. These
are known as facultative inhabitants.
Seagrass beds have an important role as a nursery
ground for the juveniles of commercially important fish
species (Jackson et al. 2001) . For some species, the physi-
cal habitat is key as a shelter from predation, but other fish
are attracted to seagrass beds due to their supply of food
in the form of invertebrates; Jenkins and Hamer (2001)
demonstrated that King George whiting (Sillaginodes
punctata, Fig.1O.15b) juveniles tended to be associated
with density of their prey (small crustaceans) as much as
seagrass habitat. Clearly, seagrass beds are important due
to a combination of shelter and food supply.
Similarly, seagrass beds may attract larger predators
too, preying on the small fish and larger invertebrates shel-
tering in the bed. Predation pressure has been suggested to
be a major force structuring the assemblages found within
seagrass beds. For example, denser parts of seagrass beds
(i.e. those with more shoots per metre) have been shown
to provide more shelter for prey items (Edgar & Robertson
1992). Predators maybe expected to forage less efficiently
in dense. thick seagrass, thus providing a refuge for smaller
animals . A further factor that may influence the success
of predators is distance from the edge of a bed, the pre-
sumption being that the further in the bed a prey organism
is. the harder it is for predators to reach it. This has been
demonstrated in a range of experiments where survival
of prey in the field has been measured; Bologna and Heck
(1999), for example, reporting that bay scallops (Argopec-
ten irradians, Fig. 1O.15a) living along edges of beds, suf-
fered a higher predation than those within the meadows.
However. these scallops on the edge also seemed to grow
quicker. so there may be a trade-off between survival and
growth. A method used to assess relative predation levels
in seagrass beds is tethering. Prey items (e.g. prawns) are
attached to lines and placed within different parts of the
seagrass bed. Comparative losses to predation can then
be recorded (e.g. Hovel & Lipcius, 2001) . Gorman et al.
(2009) tethered juvenile cod (Gadu.s spp.) over a range
of seagrass patch sizes and found highest predation levels
occurred on the edges of intermediate size patches (25
m 2 ) , suggesting predators may be attracted to larger patch
areas because of increased prey numbers. but patches of
this size do not provide enough safety for prey. Seagrass
beds also host their own predator species, which utilize
cryptic camouflage to hide within the canopy and feed

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
off small invertebrates and, occasionally, fish. The best-
known group are the Sygnathidae-the pipefish and sea-
horses (e.g. Hippocampusjayakari, Fig. 10. 15c) which can
Figure10.15 Organisms using seagrass beds as cover.
(a) The bay scallop Argopecten irradians within a seagrass
bed (photo: Dave Clausen). (b) King George whiting
Sillaginodes punctata (photo: Peter Macreadie). (c) The
cryptic predatory fish Hippocampus jayakari (photo: Ole
Johan Brett).
10.3 Seagrass meadows
be found associated with seagrass beds across most of the
world. Seahorses, in particular, have a very high conserva-
tion status. resulting in protection ofseagrass beds in some
regions (see also Chapter 14).
Additional to theories on predation refuge, there is
a direct relationship between the structural complexity
of a meadow and the associated organisms. which also
can explain their distribution within a bed. A5 a habitat
becomes more architecturally complex. it is expected that
more niches will become available. allowing higher num-
bers of species to be supported. Such a relationship has
been observed with coral reef fish and cactus-dwelling
insects, for example. Similarly. there have been clear
examples within seagrass beds of measures of complex-
ity being related to diversity. Webster et al. (1998) dem-
onstrated a positive relationship between shoot density
and associated invertebrates. while several classic studies
have positively related seagrass biomass to the number of
species recorded (e.g. Heck & Orth 1980). Increasing sea-
grass biomass has been seen as an analogue for seagrass
complexity, but Attrill et al. (2000) raised an alternative
explanation that high seagrass biomass simply provides
a greater leaf area (due to the two-dimensional nature
of the leaves) and so the relationship is a species-area
effect; more species are recorded because a greater area
has been sampled. Attrill et al. (2000) highlighted this by
demonstrating a close relationship between diversity and
seagrass biomass. but not with alternative measures of
structural complexity (Fig. 10.16) . Whatever the reason,
thicker, healthier beds do seem to provide a more favour-
able habitat for increased diversity.
At a larger spatial scale, the structure of a seagrass
meadow itself can also affect the assemblage oforganisms
associated with it. A key concern in seagrass (and terres-
trial) ecology is the fragmentation of beds (habitat) into
smaller patches. Patchy beds can be naturally generated
by specific environmental conditions, but much fragmen-
tation of continuous beds is due to human activities, such
as damage caused by boat anchors. propellers. or moor-
ings (Fig. 10.17) . Habitat fragmentation has a range of
consequences that impact organisms living within that
habitat. The overall area of the seagrass can be reduced,
which may impact big species requiring a comparatively
large territory. so the relative importance of fragmenta-
tion for conservation is a major issue : is one large area
better than several small areas? This has become known
as the SLOSS debate: Single Large Or Several Small
reserves.
A further consequence offragmentation is that discrete
patches of seagrass can form islands that are separated
from the next patch by bare sediment, potentially isolat-
ing organisms from the main population. Crossing this
sediment therefore presents a risk, and corridors of veg-
etation are very important for the movement of species
 Chapter 10 Mangrove Forests and Seagrass Meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

30

2l l- •
- ••
30
~
g

-
Ci.20 l-
• • • • -
~
2l •
-- 15f- • • • •
g g
~

• • •• •••
-- 20
~

g
• •• • • •
.::- 15
g
• •
..•
~
'0
•• • • •
--
g
~

•• • • • •• •• • •
--
g 10 l- g

g
~

10 •• •
z • g
d •
5f- z 5

0 100 200 300 400 0 100 200 300 400 500 600 700 800 900
Complexily index Seog ro~ biomass (g. OWl)

Figure 10.16 The relationship between invertebrate d iversity and seagrass arch itecture. Attrill et al. (2000)
demonstrated that structural complexity was not related to associated diversity, but there was a relationship with
seagrass biomass. They suggested this was due to increasing biomass providing a larger area to sample, and so
more species were encountered .

such as crabs (Micheli & Peterson 1999). Fragmentation
also increases the edge effect within seagrass habitat.
a patchy bed having a much larger edge:area ratio than
continuous beds. Previously we saw how predators are
potentially much more successful at the edges of beds, so
increasing the amount of edge can increase overall pre-
dation pressure. Fragmentation can also change water
flow and sediment deposition, and ultimately physical
conditions within a bed. While the detrimental impact
of fragmentation on land is comparatively well-accepted,
evidence from seagrass beds is more equivocal. Bowden
et al. (2001) demonstrated higher diversity of sediment-
dwelling invertebrates in large Zostera marina patches
than small ones, but McNeill and Fairweather (1993)
found that several small patches had a higher over-
all diversity than continuous patches of the same area.
Studies into the impact of patch size on predation pres-
sure have also produced contrasting results. Irlandi et al.
(1999), for example, worked on the role of fragmentation
on the survival ofthe same scallop species as Bologna and
Heck (1999), but found no consistent patch size effect.
The sea is a relatively open system , as there are rarely
any barriers at a localized scale to organ ism disper-
sal through the water between habitat 'islands" unlike
between two forest areas, for example. Factors such as
the longevity of the larval dispersal phase and meso-
scale oceanic physical barriers determine connectivity
between different areas of the sea.
The consequences of fragmentation within the marine
environment (beyond the detrimental loss of overall area)
require further investigation, but processes involved may
be quite different in this open system to those on land.

Figure 10.17 Zostera marina

bed in Jersey, English Channel.
The clear patches are gaps in
the seagrass meadow caused
by the physical impact of
mooring chains used by the
yachts. (Photograph: Emma
Jackso n/ Paul Tucker.)
 10.3 Seagrass meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

However. there is one further scale of organism size reliant

on seagrass where seagrass loss may have more notable
consequences.

10.3.5 Seagrass as a food supply for

large grazers
The majority of small grazers, such as gastropod molluscs
and amphipods, which inhabit seagrass beds generally
feed on the epiphytic algae, rather than directly grazing
the seagrass leaves. Such grazers therefore potentially
have a role in limiting the growth of such algae within
seagrass beds, and thus could influence the productivity
of the seagrass itself by preventing algal overgrowth and
shading (Williams & Ruckelshaus 1993). Additionally,
invertebrate grazers may be key in reducing the impact
of increasing nutrients within coastal systems, which may
favour growth by algae over seagrass (10.3.2), although
experiments are so far inconclusive (e .g. Keuskamp
2004) . The only invertebrates that demonstrate a major
grazing impact on the seagrasses themselves are sea
urchins, with examples of overgrazing apparent across
the globe in tropical and temperate waters (Eklofa et al
2008) . An example is Lytechinu.s variegatu.s, which can
occur in huge numbers (up to 360 m-2 ) within seagrass
beds off the east coast of North America. The urchin has Figure 10.18 (a) Tha/assio testudinum is known as turtle
been demonstrated to seriously overgraze beds in Florida, grass (photo: NOAA). (b) The green turtle, Chelonia mydos,
removing (for example) nearly 0.8 km- of meadow in 8 which grazes primarily on seagrass, giving the seagrass its
months (Rose et al. 1999). name (photo: www.adakris.com).
The major direct grazers of seagrass are. however,
marine vertebrates, in particular two groups: the turtles young leaves or leaf tips, which are more nutritious and
and the sea cows (Sirenia) . Both groups have representa- have lower lignin content. Turtles are seen to return to the
tive species that feed primarily on seagrass and can have same feeding area in order to graze newly grown vegeta-
major impacts on the growth. productivity. and structure tion. This continued grazing stresses the plant, resulting in
of seagrass meadows. The green turtle (Chelonia mydas, reduced leaf production, so eventually these feeding areas
Fig. 10.18b) grazes primarily on Tholassia testudinum are abandoned. In beds oflow density, turtles are less select-
(hence its common name, turtle grass, Fig. 10.18a), par- ive and forage more widely.
ticularly in the Caribbean and adjacent tropical regions. Four extant species of Sirenia exist: three species of
manatee (Fig. 10.19), and the dugong (Dugong dugan) .
The green turtle is actually brown , so its name may Manatees are not seagrass specialists; while they feed off
appear somewhat inappropriate. However, it was named seagrass when in salt water, manatees spend much time
after the colour of its fatty flesh. The turtles were hunted in freshwater where they forage on submerged vegeta-
primarily to make turtle soup. tion. For example, water hyacinths are a staple food for
the West Indian manatee (Trichechus manatus) in many
Young turtles are pelagic omnivores, but once they Florida rivers. The dugong occurs in the Indo-West Pacific
reach 20 to 35 em in size they begin benthic foraging, pref- region and is more strictly marine, with seagrass forming
erably on seagrass, though they will graze on algae where the main diet. Unlike manatees. dugongs can feed in large
seagrass is not available (BjomdaI1980) . Adults demon- herds of 100 to 200 individuals, particularly in the exten-
strate a die! feeding pattern, resting during the night (e.g. sive seagrass beds off northern Australia. Unlike turtles,
on coral reefs) and foraging during the daytime. Their dugongs often take the whole seagrass plant, roots and
specific foraging strategy depends on the seagrass density. all, leaving distinctive feeding trails through the seagrass
In high-density areas turtles are selective, avoiding older bed (Preen 1995) . In dugong foraging areas off Austra-
leaves or those covered in epiphytes. and consuming the lia. the seagrass beds are composed of two main species :
 Chapter 10 Mangrove Forests and Seagrass Meadows
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Zostera capricorni is the dominant large species inter-
spersed with patches of the fast-growing pioneer Haloph-
ila spp.. Dugongs prefer to feed on Halophila as it has a
high nitrogen content and low proportion of fibre. and as
a pioneer species Halophila is the first to recolonize the
disturbed areas left by dugong feeding. In this way, graz-
ing by herds of dugongs alters the species composition of
the seagrass meadow, stimulating the growth of Haloph-
ita, and herds have been observed grazing the same loca-
tion for up to a month as they crop the new growth of
Halophila within their grazing trails. This activity has
been termed cultivation grazing, as the dugongs' feed-
ing results in a greater proportion of their favoured food
supply.
As well as four existing species of sea cow, a further
species (the 10-m long Stellers sea cow, Hydrodama-
lis gigas) was hunted to extinction by 1768-within 30
years of its discovery in the Arctic waters of the Bering
Strait.
10.3.6 The wider role of seagrass
meadows
As well as providing a habitat maintaining high levels of
biodiversity. a nursery ground for fishery species, and pro-
viding food for large endangered grazers, seagrass beds
perform other critical functions that make them valuable
to both coastal ecosystems and humans (Green & Short
2003) .
For a marine ecosystem, seagrass beds have exception-
ally high biomass and productivity: Duarte and Chiscano
(1999) estimated an average production of 1012 g dry
weight m-2 y-l. This is higher than other marine primary
producers, such as macroalgae (365 g dry weight m-2 y-l)
and phytoplankton (128 g dry weight m-2 y-l), and com-
parable to key terrestrial systems such as savannah (900 g
Fig 10.19 Manatees, and particularly
dugongs, feed on seagrass and generate
d isturbance to the seabed. Manatee use
of habitat close to the shore in shallow
water, e.g. Florida, makes them vulnerable
to injury by boat propellers. (Photograph:
Oxford Scientific/photolibrary.)
m-2 y-l) and borealforests (800 gm-2 y-'; Whittaker 1975).
Seagrass beds therefore provide large amounts of carbon
for input into coastal systems. supporting food webs and
commercially important species such as prawns (see Lon-
eragan et al. (1997) in 10.2.7, for example) . The high leaf
biomass produced by seagrass beds is also harvested by
humans for a range of uses, such as packing material. fibre
for use in mat weaving, and even seagrass furniture and
storage boxes (Green & Short 2003).
It is useful to compare seagrass productivity with that of
other systems: savannah> 900 9 m- 2 v:'. boreal forests
= 800 g m- 2 y-' , lakes and streams = 250 g m- 2 r' .
Rainforests, however, produce 2200 9 m~2 y-' (Whittaker
19 75).
Seagrass beds also provide key ecological services.
The root-rhizome system enhances sediment stabiliza-
tion and thus prevents erosion, while the foliage slows
water currents through their baffling effect. encourag-
ing sediment to settle and preventing resuspension.
Extensive seagrass beds therefore are stabilizing fea-
tures within the coastal landscape, and provide a nat-
ural form of coastal protection. In the low-lying Wadden
Sea (Netherlands), seagrass debris was traditionally used
to make dykes. and restoration of Zostera marina beds
through transplantation is being investigated as a natural
barrier to protect the coast (van Katwijk 2003) . Perhaps
the greatest value of seagrass beds is. however, indirect
roles in water purification and nutrient cycling (Green &
Short 2003) . Through sedimentation processes and the
active uptake of nutrients into the seagrass meadow eco-
system. large seagrass beds can be effective in removing
nutrients from the water column and trapping them for a
comparatively long time in leaflitter; most algal-dominated
or planktonic systems have a much quicker turnover of
nutrients. Seagrasses can therefore help mitigate problems
 10.3 Seagrass meadows
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

of eutrophication (10.3.2) and even bind organic pollut-
ants. Similarly. seagrasses can help drawdown and remove
carbon dioxide and play some role in the amelioration of
climate change, particularly species such as Posidonia oce-
anica whose root-rhizome matte can persist for hundreds
of years. While their overall impact compared with phyto-
plankton in the world's oceans will be low, their high pro-
ductivity gives them a disproportionate influence in coastal
systems (Green & Short 2003).
The matte of Posidonia can be roug hly aged due to
known growth rates. It has therefore been used to date
old wrecks in the Mediterranean!
Seagrass beds therefore provide a range of goods and
services of benefit to coastal ecosystems and humans (see
Chapter 16). Costanza et al. (1997) attempted to put an
economic value on the world's ecosystems relating to these
services, suggesting seagrass/algae beds are worth $19 004
ha- 1y-1, mainly due to their nutrient cycling role. Green and
Short (2003) therefore estimated the global value of sea-
grasses to be $3.8 trillion (i.e. $3.8 x 1012 ) , but pointed out
that this does not represent the total worth of the ecosystem
and is not a purchase value!

Chapter Summary
• Mangroves and seagrasses are both 'true plants' and their aggregations represent two of t he most
valuable marine hab it ats in the world, being highly productive and with a very high associated bio-
diversity.
• Mangroves are found mainly in the tropics and are woody trees that can flourish at the land/sea
interface. Through morphological and physiological adaptations, mangroves can deal with their
roots being in waterlogged, anoxic sediment, and can tolerate the high levels of salt, surviving in
conditions that would be fatal for most plants.
• A dynamic mix of terrestrial and marine organisms share mangrove forests. They are important sites
for many bird species, including species of hi gh conservation status such as scarlet ibis.
• Crabs are t he most important marine group of organisms associated w ith mangroves, their burrowing
activity and consumption of leaf litter being important for carbon cycling and in turn ing over the
sed iment (which affects the production of mangroves).
• Mangroves have an important wider role, exporting carbon to surrounding areas, protecting the
coast from erosion and providing a nursery area for many fish species, including those from coral reefs.
• Seagrasses are the only angiosperms that can survive fully submerged in the marine environment. They
are found across the world's coastal seas and can form huge meadows covering 1000s of km 2 •
• Meadows mainly form in shallow subtidal soft sediments in clear water, but can extend int o the
intertidal zone or even grow on rocks. In the clear waters of the Mediterranean, Posidonia beds
can grow down to 40 m.
• Seagrass leaves form a substratum for the settlement of a d iverse epiphyte community. The rela-
tionship between seagrass and algae is complex, and can be altered by increased nutrient levels that
favour the algae, outcompeting the seagrass.
• The physically complex nature of seagrass beds, compared to surrounding bare sand, results in
meadows having a high associated biodiversity of marine animals (invertebrates and fish). The diver-
sity and abundance of animals is associated directly with the amount and complexity of seagrass
that is present, from the density of shoots to the overall areal cover of seagrass.
• The global cover of seagrasses has been reduced dramatically (15% from 1993 to 2003) as they
are sensitive to changes in light levels, nutrients, and human mechanical disturbance.
Chapter 10 Mangrove Forests and Seagrass Meadows

Further Reading
Books
• Green, E, P. & Short, F. 1. 2003, World Atlos of Seaqrasses. University of Cal iforn ia Press,
• Hemminga, M, A. & Duarte, C M, 2000, Seogross Ecology Cambridge University Press,
• Hogarth, P. J. 19 9 9, The Biology of Mongroves, Oxford University Press, Oxford ,

Key papers and reviews

• Alongi, D,M, 2002 , Present state and future of the world's mangrove forests, Environmental Conserva-
tion 29: 331 -349,
• Duarte, C. M. 2002. The future of seagrass meadows. Environmental Conservation 29: 192-206.
• Jackson, E" Rowden, A.A., Attrill, MJ" Bossey, SJ" & Jones, M,B, 200 1, The importance of seag rass beds
as a habitat for fis hery species, Oceonogrophy ond Morine Biology: on Annuol Review 39, 269-303 ,
• Molnar, J.L" Gamboa, R.L" Revenga, C , & Spaldi ng, MD, 2008, Assessi ng the g lobal threat of invasive
species to marine biodiversity. Frontiers in Ecology and the Environment 6: 4 8 5-4 9 2.
• Ropert-Coudert, Y. & Wilson, R.P. 2005. Trends and perspectives in animal-attached remote sensing.
Frontiers in Ecology and the Environment 3 , 4 3 7-444.
Coral Reefs
Chapter Summary
The first sight of a coral reef has inspired many to seek a
career in marine b io logy. The bands of bright colou r fringi ng
the coasts of tropical islands and highlighting small coral
atolls in an otherwise deep-blue ocean are a marvel to most
of us and attract a globally significant tou rism business.
These reefs can be hund reds of metres thick, and yet they
have been built by a thin veneer of living coral tissue. Spe-
cies' diversity on reefs can equal that in rainforests, but
reefs are probably more accessi ble because you can float
11. 1 Introduction
Coral reefs support some of the most diverse and produc-
tive communities in the marine environment. Living corals
create limestone formations that may be thousands of kilo -
metres long and hundreds of metres deep. While the sm all
polyps that form living coral are best viewed under a micro-
scope, limestone coral reefs are clearly visible from space.
Coral reefs const itute a shallow, productive, and brightly
illuminated ecosystem, supporting an am azing diversity of
plant and animal species . In many areas, by providing pro-
tection from wave ene rgy, they also help foster ecological
oases such as of mangroves and seagrass beds (Chapter 10) ,
in otherwise deep and oligotrophic oceans. Coral reefs are
an iconic ecosystem; they figure prominently in advertising,
attract major tourism and exemplify the complexities of the
marine environment.
This chapter describes the global distribution and typol-
ogy of coral reefs, the biology of reef building corals, and
the factors that influence their growth and reproduction.
We will look at the productivity of re efs, and the biology
and diversity of animals supported by this production and
silently above them observing the inhabitants. Indeed, reef
research has burgeoned with the advent of widely available
scuba-diving gear in the 1950s. However, for millions of
people in the tropics, reefs are not only a source of fascina-
tio n, but thei r mai n source of food, buildi ng materials, and
income. The activities of bu rgeoning human populations
are th reateni ng co ral reefs around th e world, and although
reefs can be highly productive, growth of the reef itself can
be a transient process, easily upset by changes in climate,
sedimentation, fis hing, and pollution.
habitat. Despite their vas t size, reefs are among the most
sensitive of marine habitats to human disturbance; they are
in fact the marine ecosystem most threatened with anthro-
pogenic degradation. We consider the roles of climate
change, fishing, and pollution in driving this degradation.
11.2 Reef development and
distribution
From the seafarer's perspective, reefs are rocks close to the
sea surface that can damage a ship's hull. However, coral
reefs are distinct because they are biogenic, or deposited
by living organisms (Veron 2000). Growing corals and
calcare ous algae deposit carbonate and this can form vas t
limestone structures that raise the living reef high above
the surround ing seabed. Thus, the Great Barrier Reef in
Australia extends for 2000 km and has an are a of 48 000
km-, and Enewet ak Atoll in the tropical Pacific is over 1300
m thick. While the reef at Enewetak Atoll is probably 50 mil-
lion years old, most of the limestone that forms the struc-
ture of the Great Barrier Reef was deposited in the last 500
 Chapter 11 Coral Reefs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

000 years and most modern reef grow th d ates only from
the last 10 000 years, during the present interglacial period Table 11.1 The global distribution of warm water
(Holocene) (Chapter 1). coral reefs. After Spalding et al. (2001).
Most reefs are found within a band 30° north or south of
the equator (Fig. 11.1 ) . The extent of shallow-water coral Region Area (km 2 ) "!o of world
reefs worldwide is 284 300 km- (Table 11.1 ) ; this is only total
around 3% of the total tropical continental shelf area but is
Atlantic and Caribbean 21600 7.6
inordinately rich in terms of biodiversity.
Caribbean 20000 7.0
Atlantic 16 0 0 0.6
Coral reefs cover <0 .10;0 of the global ocean surface
area, yet, for example, they host over a quarter of all
Indo-Pacific 261 200 91.9
known fish species on Earth and the vertebrate species'
Red Sea and Gulf of Aden 17400 6.1
density (number of species per unit area) is far greater
Arabian Gulf and
than that of rain forest.
Arabian Sea 4200 1.5
Indian Ocean 32000 11.3
See http: //www.unep-wcmc.org / for global maps of coral Southeast Asia 91 700 32.3
reef distributions. Pacific 1 15 900 40.8

The re are two broad groups of corals: reef- build ing or Eastern Pacific 1600 0.6
hermatypic corals, and the non reef-building aherma-
typic corals. Hermatypic corals are largely confined to the
Total
.-1- ,- 284400

tropics, wh ile ahermatyp ic corals are found worldwide.

The growt h of hermatypic corals and ot he r reef-builders,
and hence the distribution of coral reefs, is strongly influ-
enced by the physical environment.
Reef-building corals are known as hermatypic.
The latitudin al span of coral reefs corresponds w it h
a temperature range of 18 to 36°C, wit h opt imu m ree f
development occurring at 26 to 28°C. Tempe rature helps
explain the absence of reefs fr om much of the tropical
coas ts of the Americas (Fig. 11.1 ) and West Africa, where
cool upwelling water (Chapter 7) does not support coral
growth. Reefs in areas where temperatures vary cons ider-
ably in space and time will often show highly intermittent
patterns of growt h . Suc h an area is the Gala pagos Islands,
where several ocean curre nts, carrying water of different
temperatures, m eet. During warm periods there may be
rapid acc re tion of reefs, bu t during cooler periods, reefs
stop growing a nd are eroded by a va riety of an imals, a
process known as bioeros ion, However, in regions such
as West Africa other forces are at work, and land-derived
siltat ion also inhibits reef formation. In 11. 3 we look more
closely at factors affect ing growt h of corals.
Reef growth is influenced by sea temperature.
Corals and other carbonate-form ing organ isms form
several types of reef, depending on the availability of
underlying substratum (existing carbonate reef or igneous
rock), long-term changes in sea level, light levels, and wave
action . Fringing reefs develop on the shelving shores of
most rocky tropical islands (Fig. 11.2). These reefs develop
because corals settle and grow on well-illuminated and
shallow areas of the rocky substratum. As the corals grow
towards the sea surface, they create a shallow platform

Figure 11.1 Global distribution of coral reefs. After Spalding et al. (2001).
 11.2 Reef development and distribution
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Patm reel Barrier reef
and. over several thousand years. the platform reaches a
height where it isjust exposed by low tides. Further upward
growth of the reef then stops because the corals cannot tol-
erate drying and intense wave action. However, the fringing
reef may continue to grow horizontally. as the edge of the
platform provides shallow and well-lit areas for more corals
to settle and grow. Horizontal development will continue
until the base of the platform is too deep and poorly illumi-
nated to support coral growth .
Fringing reefs grow on shelving coastlines.
Patch reefs or bommies are small reefs that grow in
shallow lagoonal areas and are often surrounded by sand.
Patch reefs may grow upward until they are just below the
surface at low tide, but they are often deeper (Fig. 11.3).
Barrier reefs surround many tropical islands and are usu-
ally separated from the land by lagoons with patch and
fringing reefs. The lagoons are typically 1-10 Ian wide.
Barrier reefs on one side of an island will be exposed to
the prevailing oceanic swells, and are visible from the
land as a line of breaking surf (Fig. HAl . Barrier reefs
may develop from fringing reefs following periods of
Figure 11.3 A lagoonal patch reef in Fiji. (Photograph:
Simon Jennings.)
Figure 11.2 Different types of coral
reef.
Awn
sea level rise relative to the land. in which land subsid-
ence may also be important. Barrier reefs grow quickly
because the exposure of the corals to prevailing wind and
currents can enhance growth (Fig. 11.5) . Atolls are per-
haps the classic example of a coral reef, a ring of reef with
low-lying islands surrounding a central lagoon. Atolls can
be 10 km or more across, and many are famed for their
biological diversity, seabird colonies, and military signifi-
cance (Box 11.1) . Charles Darwin was the first scientist
to speculate on the formation of atolls, and his theory is
widely accepted today (Fig. 11.6). When a volcanic island
is formed, it is quickly colonized by corals and a fringing
reef forms. Then, as the island subsides or sea level rises,
corals grow most rapidly on the outer edges of the former
fringing reef and a barrier reef is formed . Eventually, the
island may be lost altogether, but the ring-shaped atoll
remains.
Other types of reef are patch, atoll , and barrier reefs.
The theory of atoll formation was first put forward by
Charles Darwin.
Figure 11.4 A lagoon and barrier reef in Vanuatu . Note
the line of surf breaking on the barrier reef in the
distance. (Photograph: Simon Jennings.)
 Chapter 11 Coral Reefs
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Figure 11.5 An o ute r reef slo pe o n the Great Astrolabe Reef in Fiji. (Photograph: Simon Jennings.)
Box 11.1: Aldabra Atoll
Aldabra Atoll , 34 km by 14 km in size and one of the
world's largest co ral atolls, is situated in the Indian Ocean,
approximately 200 miles north of Madagascar (9°25'5
46°25'E). The scientific importance of Aldabra Atoll was
recognized by 18 50 , since, unlike most other atolls and
despite regular visits from fishermen in preceding years,
there was no permanen t settlement on the island and it
had been left relatively undisturbed. By 1850, giant tor-
toises had virtually disappeared from other Indian Ocean
atolls, due to direct exploitation and habitat modificatio n
following guano digging and logging. The guano deposits
on Aldabra were insufficient to make digging commercially
viable and it was a hostile atoll with difficult boat access.
When a company proposed to lease the atoll for woodcut-
t ing in the late 1800s, Charles Darwin and other eminent
scientists argued for protection of the tortoise popula-
t ion. No protective legislation was passed, but private
arrangements we re reached with the lessor in retu rn for
assistance with rent.
The famous expedition diver, Jacques Cousteau, vis-
ited Aldabra Atoll in 1954, and the popular media cov-
erage that followed publicized its biological importance.
However, with the 'Cold War' at its height followi ng the
Cuban Missile Crisis, and Aldabra formi ng part of the Brit-
ish Indian Ocean Territory, the British and US Governments
Signed a 1965 treaty to make the islands of the territory
available for defence purposes. While the isolation and
hostility of Aldabra may have discouraged visits from fish-
ermen, they would have been no deterrent for the military,
who had already developed another atoll , Diego Garcia
in the Chagos Arc hipelago south of India, as a military
base. The British Government was clearly unappreciative
of the ecological importance of Aldabra. Denis Healey,
a senior British poli tician , had responded to a question
in the House of Commons by stating that 'the island of
Aldabra is inhabited-like Her Majesty's Opposition Front
Bench-by giant turtles [sic] , frigate birds and boobies;
nevertheless, it may well provide useful facilities for aircraft'.
The Royal Society, Smithsonian Institution, National Acad-
emy of Scien ces, and other bodies, vigorously opposed
development. The protest culminated with the British Royal
Society mounting an expedition to Aldabra in 1967. They
aimed to ob tain all possible information on the islands
before any development started. Devaluation of the Brit-
ish currency, rather th an the views of environmentalists,
eventually rendered the military scheme too expensive and
subsequent changes in international relations and defence
strategy meant that development never occurred. Partly as a
result of the military threat, however, Aldabra is one of the
most thoroughly studied oceanic atolls and its ecological
significance led to its designation as a World Heritage Site
by the IUCN in 1982. It is now managed by the Seychelles
Island Foundation (http:/ /www.sif.sc/) .
Source: Stoddart (1984).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Figure 11.6 The formation of an atoll. A volcanic island
is colonized by corals and a fringing reef develops
(upper). As the land subsides (m iddle), so a barrier reef
is formed, which, as the land subsides further or sea
level rises (lower) becomes an atoll.
Historical patterns of reef growth are typically revealed
by examining cores cut into reefs. Reef growth is rarely con-
tinuous, and periods of fast growth are often interspersed
with periods of bioerosion. The fastest recorded rates of
net reef growth are around 20 m in 1000 years, but3 m per
1000 years is more typical today. On the Great Barrier Reef
and at Enewetak Atoll coral growth involves an average
deposition of 4200 tannes of limestone krrr?r i . The linear
extension of individual corals can reach 20 em y-I, and for
short periods reef accumulation can be rapid. but such rates
of annual growth are not sustained over geological time. In
geological time, reef growth has been primarily affected by
sea level fluctuations of up to 140 m, caused by repeated
accumulation and melting ofglaciers in the northern hemi-
sphere and the associated expansion and contraction of the
area of warm tropical seas (Veron 2000) . Falls in sea level
expose reefs. while increases in sea level promoted reef
11.3 Corals and coral communities
growth. as corals grew quickly to remain well-illuminated.
However, sea levels have also risen by 10 m or more in 1000
years. which is faster than maximum coral growth rates;
in such cases, corals have been left behind in deep water,
unable to keep pace. Maximum rates of reef expansion and
growth usually occur in the warmer interglacial period.
Fluctuations in sea level have a key effect on reef growth.
Bioerosion involves removal of carbonate by grazers
(e.g parrotfish and sea urchins) and borers (e.g. sponges,
bivalves); see 11 .7.
Reef growth is also rapid when shallow shelf areas sub-
side. provided that the rate of subsidence does not carry
corals out of the brightly illuminated zone.
11.3 Corals and coral
communities
Corals build vast limestone structures but, in evolutionary
terms. th e corals are quite simple organisms. During reef
formation, their most important features are the capacity to
live colonially and to deposit calcium carbonate skeletons.
Corals. and hence reef growth, are very sensitive to the
physical environment.
Hermatypic corals are largely confined to the tropics,
while ahermatypic corals are found worldwide. The pol-
yps of hermatypic corals usually contain symbiotic algae or
zooxanthellae, which photosynthesize and provide energy
for the coral polyp (Fig. 11.7). The relationship is symbi-
----,'iL----- ?<-- - li>ntode
- - --tt------+I-- Phorynx
: - - - - - - - - - Meson" ,1
~lome nt
:::0-- - Connecting sheet
-----1t-- Them
- -Sderoseplum
----=---------'---- 8' ,,1plate
Figure 11.7 A coral polyp. The zooxanthellae are found
in the gastroderm is. After Muller-Parker & D'Elia. (1997)
and others.
 Chapter 11 Coral Reefs
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otic because the polyps provide protection and nutrients
for the zooxanthellae, while the zooxanthellae fix carbon
and produce ene rgy for the polyp (Table 11.2). A number
of stress ors, such as elevated temperature, ultraviolet light,
and nutrient levels, can cause the symbiosis to break down
and ultimately kill the corals.
Hermatypic corals contain symbiotic algae that fix carbon
dioxide and produce energy.
Zooxan thellae are dinoflagellate symbiotic algae,
mostly belonging to the genus Symbiodinium . They con-
tain characteristic dinoflagellate pigments, as well as chlo-
rophyll. Zooxanthellae can live independently of the host
coral in a free-living motile stage, but in the coral polyps
they lose their flagellae and motility. The symbiotic algae
can be transmitted during coral reproduction, but corals can
also obtain them directly from seawater (Muller-Parker &
D'Elia 1997). Successful coral growth requires that the cor-
als can gather nutrients from oligotrophic tropical waters .
The tentacles of the coral polyps can capture nutrient-rich
zooplankton directly while the zooxanthellae provide pho-
tosynthetic by-products.
The zooxanthellae are autotrophic and require nutri-
ents, light, and carbon dioxide to fix carbon. These symbiotic
algae can obtain the nutrients by recycling waste products
from their animal host, from the zooplankton caught by
their animal host, and through direct uptake from seawater.
During photosynthes is, carbon dioxide is removed from the
water to produce organic matter. When the rate of photosyn-
thesis is high, the rapid uptake of CO, will promote calcium
carbonate precipitation at the base of the polyps.
Table 11.2 Benefits of the symbiosis between
zooxanthellae and corals. Modified from Muller-
Parker and D'Elia (1997).
For the anima!
Supply of reduced carbon providi ng low respiration
costs and conservation of metabolic resources
Increased growth and reproduction
Increased calcification rate
Conservation of nutrients
Sequestration of toxic compounds by algae
•• ••• ••• ••••• ••• ••• ••• ••• ••• ••••• ••• ••• ••• ••• •••••••• ••• ••• ••• ••••••••
For the zooxanthellae
Supply of CO2 and nutrients from host maintenance in
photic zone
Protection from UV damage by animal tissues
Maintenance of a high population density of a single
genotype by host under uniform environmental
conditions
- gbundersea).
The successful reproduction and recruitment of corals
is fundamental to reef development. Reproduction ensures
new individuals will form and recruitment is the process by
which young corals join the coral community. Most herma-
typic corals consist of polyps, and these colonies grow by
asexual budding. Polyps can also detach from some colo-
nies and establish new colon ies elsewhere or, particularly
with branching corals, pieces of skeleton with attached pol-
yps will break off and subsequently grow.
Corals can reproduce sexually and asexually.
While detached polyps m ay be ciliated and able to drift
or swim, the long-distance dispersal of corals is mostly
achie ved throu gh sexual re product ion (Carlon 1999).
Here, corals release eggs and sperm, and fertilized eggs
develop into a ciliated larva, which can drift over long dis-
tances before settling. Corals may be gonochoric, simul-
taneous, or sequential hermaphrodites. Most species are
simultaneous hermaphrodites.
Some coral species reproduce by brood ing; the eggs are
fertilized internally and the ciliated larva (p la nu la) devel-
ops inside the coral polyp (Richmond 1997). However,
most species are broadcasters, releasing eggs and sperm
into the water column for fertilization (Fig. 11.8). Spawn-
ing corals exhibit m ass releases of gametes during particu-
lar periods of the year, usually related to lunar cycles. On
the Great Barrier Reef, gamete release by over 100 species is
synchron ized, presumably because the corals are respond-
ing to common cues. Synchronization no doubt incre ases
the probability of fertilization within species and also has
the effect of swamping egg and larvae predators (Oliver &
Babcock 1992).
Once eggs are fertilized they develop into planulae that
are capable of settlement in 1- 3 days. These larvae gene r-
Figure 11.8 Coral spawning showing the eggs
emerging from the polyps (photograph: Greg Bunch/
 11.4 Coral reef productivity and food chains
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
ally only acquire their zooxanthellae after settlement and
metamorphosis, whereas the larvae of brooders already
contain zooxanthellae from the parent colony. During
metamorphosis the larva secretes a calcified basal plate and
the form of the polyp develops. Factors such as suspended
sediment load. temperature. and salinity will affect rates
of coral egg fertilization and larval survival. Interestingly,
even distantly related corals seem to require the presence of
crustose-coralline algae for successful metamorphosis and
settlement. These algae in tum need the grazing of fishes
and invertebrates to keep them clear of other organisms,
thus within the ecosystem there is an indirect connection
between the amount of grazing and coral establishment.
The reproduction and growth of hermatypic corals is
strongly influenced by the physical environment. Corals are
principally affected by temperature, light, depth, salinity,
wave energy, sediment, and pollution.
The physical environment determines coral distribution.
Light is vital to corals, as it allows the zooxanthellae to
photosynthesize. Most reef accretion occurs at depths of 0
to 10 m, and even in clear oceanic water, hermatypic cor-
als are rare below 30 m. We saw in Chapters 2 and 7 how
quickly light attenuates as it enters the water, although light
penetration is good in shallow water when the sun is almost
vertically overhead and the water is clear. Indeed, working
underwater on coral reefs at a depth of3 to 4 m there is still
sufficient ultraviolet light to cause sunburn.
Corals need light to grow and are rarely found at depths
>30 m.
Diving down an outer reef slope it is always surprising
how quickly the bright colours of the reef and a superabun-
dance of small colourful fish are replaced by more sombre
oceanic blues. As the light intensity fades, so corals become
increasingly scarce, and are found only in small patches
(Fig. 11.5). The availability of light determines the maxi-
mum depth at which corals are found. Coral linear exten-
sion rates may drop from a centimetre per year at 2-5 m
depth to a few millimetres or less at 10 m. In the presence
of bioeroders, such as parrotfish and sea urchins, it is not
surprising that almost all reef accretion takes place in the
shallow well-lit zone.
We have already seen that temperature governs the
global distribution of reefs, with optimum reef develop-
ment occurring at 26 to 28°C. Corals have quite low toler-
ance to temperature variation, although tolerance is species
and site specific. Corals that have evolved in very stable
temperature regimes are typically less tolerant to change
than those that have evolved in more variable environ-
ments. Sheppard et al. (1992), for example, describe reef
corals in the western Arabian Gulf that survive maximum
temperatures of 38°C and minimum temperatures of 12°C.
Such temperature changes in the central Indian Ocean
would cause extensive coral death and, in many cases, sus-
tained increases in temperature of 2 to 3°C for a few weeks,
as occur during E1 Nino events (Chapters 7 and 8), may be
enough to lead to mass mortality.
Most corals are sensitive to temperature change.
Reefs grow fastest when salinity is 33 to 35, typical
of offshore oceans. At lower salinities, in the vicinity of
river estuaries, for example, extensive coral reefs do not
develop, even if sediment loads are low and light penetra-
tion through the water is good.
Wave action generates currents around reefs and
enhances the transfer of nutrients and dissolved gases such
as oxygen. However, some corals cannot withstand the
turbulence induced by waves. For this reason, wave action
has an important structuring force on coral communities,
especially on outer reef slopes. Many tropical regions are
also affected by powerful waves during hurricanes. The his-
tory of hurricane damage has affected the distribution of
modern reefs, since corals in areas impacted by hurricanes
will usually be tolerant to intense disturbance or be short-
lived species that can recolonize an area between hurricane
events. In the Caribbean, for example, the distribution of
reef types reflectshistorical patterns ofstorm and hurricane
disturbance (Hubbard 1997).
The zonation of corals is partly explained by the effects
of wave action.
Some corals can remove sediment from their surface, but
in general sediments cause smothering, abrasion, shading,
and recruitment inhibition in reef corals. Pulse sediment
loads are often storm-related and reef organisms may be
only acutely affected by them, but suspended sediments
that result from agricultural practices on land, dredging,
and coastal development have had a significant impact on
reefs in recent times. One of the main effects ofincreases in
suspended sediment load is to shade corals, and they can no
longer grow in the reduced light levels.
( Suspended sediment can kill corals. )
11.4 Coral reef productivity
and food chains
Swimming up to coral reefs from the surrounding waters,
it soon becomes clear that reefs are highly productive. The
productivity is usually expressed per unit of projected sur-
face area of the reef. This is very different from the true
 Chapter 11 Coral Reefs
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surface area, which accounts for the complexity of the reef
habitat. and can be 15 times greater than projected area
(Hatcher 1988, 1997).
Coral reefs are very productive, but most of the produc-
tion is recycled withi n the reef.
Corals are responsible for significant carbon fixation on
coral reefs, but less than half the carbon they fix is available
to consumers, because most is respired, recycled. or accu-
mulated within the coral colony. In fact, only a few reef spe-
cies, such as the gastropod Drupella. the crown-of-thorns
starfish Acantha.ster, and some parrotfishes (Scaridae) or
butterflyfishes (Chaetodontidae), feed on coral polyps
directly. Reef algae are extremely productive, and the car-
bon that they fix plays a much greater role in supporting
reef food chains because they are directly grazed by many
reef species and because across whole reefs coral typically
cover only a small proportion of the total substratum.
Not much coral production is eaten directly.
Shallow and well-lit coral reefs provide an ideal substra-
tum for algal growth. Most reef areas not covered with cor-
als are colonized by turfs of filamentous and small fleshy
algae that are directly grazed by fishes and invertebrates.
The algae and photosynthetic bacteria that account for
most reef production across whole reefs ultimately rely on
the surrounding seawater to supply organic nutrients and
Current
°l----- ----:;;::~
10 Iepepods
30 2
40
5
10
lorvoc:eons
Figure 11.9 Zoop lankton densities at sites on the
reef front. Zooplankton abundance falls to almost
zero as water crosses the reef because fishes and other
planktivores are grazing the zooplankton. After Hamner
et a l. (1988).
disperse the organic compounds they leak or excrete. Most
turf algae are constantly grazed by herbivores, keeping
them in the most productive phase of growth through the
intense feeding and probably local recycling of nutrients via
defecation and excretion. Rates of gross primary produc-
tion by reef algae range from 1 to 40 g C m-2 d-" 20 to 90%
of what is left after respiration and export being grazed by
herbivores, even though some algal species have evolved
anti-grazing mechanisms.
Reef algae can be very productive and support many fish
and invertebrate food chains.
Phytoplankton production in the water surrounding
reefs also makes an important contribution to the produc-
tion of reef animals. The phytoplankton support zooplank-
ton that are grazed by reef animals as currents carry them
across the reef. The extent of plankton use byreef fishes was
dramatically illustrated by Hamner et al. (1988) . As water
flowed over the reef slope, virtually all copepods and other
zooplankters were picked off by planktivorous fishes (Fig.
11.9). Although production in the waters surrounding reefs
is low on a per unit area basis. the continuous flow ofwater
overthe reefs means that reef planktivores can eat plankton
from a very large area of ocean (Polunin 1996).
Reef animals also eat plankton that drift over the reef.
The 24-h cycle has often been used to measure net com-
munityproduction on reefs because photosynthetic produc-
tion takes place in daylight hours and respiration occurs at
night. Net production over the 24-h period is known as the
excess production (E), such that an excess production of
zero equates to a photosynthesis/respiration ratio (P/ R)
of one . On most reefs. E is very low in relation to measured
rates of production. This indicates strong competition
among animals for the food produced in the ecosystem. The
low E and prevailing oligotrophy ofsurrounding waters also
imply nutrient recycling within the system, but it is unclear
how this might occur. For entire reefs. gross community
production is typically2.3 to 6.0 gC m-2 d-" while Eis-Q.01
to 0.29, and P/R is 1.0 to -1.11 (Hatcher 1988).
In spite of their primary productivity approaching that
of upwelling systems (Chapter 6), the capacity of reefs to
produce fish is probably no greater than that ofother conti-
nental shelf areas. Thus in the South Pacific, fishery yields
of 14 to 35 t krrr- y-! have been reported from many loca-
tions and this compares favourably with 20 to 50 t krrr- y-!
from temperate shelves.

11.5 Reef fauna
While 100 000 or so species are now known from coral reefs,
when these communities have been fully studied they may
ultimately prove home to over a million species. However
we already know that on an area-specific basis, the species'
richness of animals on coral reefs is exceptionally high. At
least 4000 species of marine fish, almost one-third of the
global total, are found on coral reefs.
Coral reefs are among the world 's most diverse ecosys-
tems.
We also know that the diversity of reef animals is far
from uniform, with higher species' richness of most groups
in the Indo-Pacific rather than the Atlantic, and a centre
of di versity in Sout h-East As ia. In the case of some 794
species of Scleractinian reef-building corals, for example,
the number of recorded species peaks in South-East As ia
(particularly central Indonesia, southern Philippines and
western Melanesia), and fall s at higher and lower latitudes
and longitudes. Remote reefs in higher latitudes often have
the fewest species. The same general patterns of species'
richness apply to almost all other groups of reef animals;
for example, between the Indo-West Pacific, wh ich conta ins
South-East Asia, and the East Pacific (Table 11. 3).
Diversity is determined by reef history and the local
physical environment.
Local va riations in the diversity of reef organisms are
attributable to the regional pool of species, the variety of
h abitats, and spatial differences in enviro nmental factors
that determine which species are represented in a particu-
lar patch of habitat. When a specific site on a reef is followed
over time, it will be evident that the mix of species changes.
This dynamism is determined by the interaction between
processes introducing species new to the site (e.g. larval
drift, survival, and settlement) and those leading to local
demise (mortality of all kinds). Area is important in this;
Table 11.3 The diversity of reef animals expressed as the number of known species. Modified from the
compilations of Spalding et al. (2001) and Paulay (1997).
Group Indo-West Pacific
Scleractinian corals 719
Alcyonarian corals 690
Cypraeid gastropods (cowries) 178
Bivalves 2000
Echinoderms 1200
Reef fish 3000
11.5 Reef fauna
large areas have more species than small areas, and there
are remarkable sim ilarities in their make-up (Bellwood &
Hughes 2001 ).
On geological timescales there have been mass extinc-
tions of reef animals.
Reef-building corals evolved over 200 million years ago,
and their distribution was effectively circumglobal in shal-
low seas for at least 100 million years . Given the position
of the cont inents at this time (Chapter 1) the only m ajor
barrier to coral distribution was the proto-Pacific ocean,
extend ing from As ia to the Americas. Subsequently, the
con tinents moved apart, and create d oceans that were
largely unconnected, and the coral reefs and associated
comm unities in the Indo-West Pacific, East Pacific, West
Atlantic, and East Atlantic evolved in different ways (Vero n
2000). Then, around 3 to 4 million years ago, the Isthmus
of Panama emerged and severed the connection between
the East Pacific and West Atlantic, and these communities
also evolved independently. Based on the fossil record, it is
clear that the coral reefs we see today are not the result of
a long history of evolution in a stable environment. Rather,
the diversity we observe is a result of large -scale extinction
events and rapid periods of evoluti on . Some reefs were
effectively elim inated by mass extincti on every 20 to 30
million years, with a delay of 3 to 10 million years before
they appeared again. Other reefs were less affected by these
extinctions and evolution continued.
Modern patterns of large-scale diversity are influenced
by the isolation of reef provinces following continental
drift.
Events during the last 2 million ye ars appear to have led
to the major differences in the diversity of reef animals in
the East Pacific, West Atlantic, East Atlantic, and Indo-West
Pacific (Paulay 1997). The East Pacific reef fauna proved
vulnerable to the variable environmental conditions in this
region and there were several large-scale extinctions after
Eastern Pacific Western Atlantic
34 62
0 6
24 6
564 378
208 148
300 750
 Chapter 11 Coral Reefs
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the East Pacific and West Atlantic faunas became isolated .
This isolation prevented recolonization from the West
Atlantic although, despite the distances involved, there was
some recolonization from the central Pacific. Today. there-
fore. more of the East Pacific fauna is shared with the Indo-
West Pacific than the Atlantic. In the West Atlantic there
were several mass extinctions, including those associated
with oceanographic changes that followed the closure of
the Isthmus of Panama. Despite subsequent speciation.
diversity in the West Atlantic remains relatively low. Rates
of extinction in the Indo-Pacific region were lower than
elsewhere, at least in the last 5 million years. and almost
all extant coral genera are found in the fossil record. Rates
of speciation were also low, but coupled with the low rates
ofextinction they contributed to the high levels of diversity
observed today. The complex pattern of islands and ocean
currents through them, combined with changes of sea level
and limited dispersal, provided multiple opportunities for
local populations to become geographically separated
(Mora et al. 2003) .
When scientists first began large-scale studies of coral
reefs in the 1950s and 1960s, they sent back pictures of
colourful flourishing reefs supporting abundant and diverse
communities of animals. Early research focused primarily
on the systematics and ecology of the corals and other ani-
mals. and the first collections of time-series' data on coral
abundance and diversity were initiated. It became clearthat
reefs were not the stable communities, which were struc-
tured by competition, that many scientists thought they
were looking at. Rather. reefs were dynamic ecosystems.
In contrast. the geology ofreefs has tended to emphasize
continual change because of the huge time spans involved,
but there is geological evidence also of consistency in com-
munity structure over considerable periods of time. Thus,
reefs formed successively at the same location by repeated
land uplift in northern Papua New Guinea exhibit remark-
able within-habitat similarity in the coral species present
over a 95 000 year time-span. This is in spite of there being
more than seven times as many coral species available in
the regional pool of species (Pandolfi 1999).
Thus reefs do change over time. but at the same time
demonstrate some characteristics of stability. Many ques-
tions surround the nature of these processes structuring
this intricate ecosystem, and the extent and nature of its
resilience to natural and anthropogenic environmental
change.
11.6 Threats to coral reefs
In the 1970s, many scientists had begun to ask whether
contemporary changes in reefs were faster and larger
than those seen previously. and whether these changes
were the result of human impacts. Decline in coral cover
on Caribbean reefs and on the Great Barrier Reef since
the 1970s and 1980s, respectively, is cause for great con-
cern and indicates that reef ecosystems are not sufficiently
robust to withstand the major human disturbances (Bell-
wood et al. 2004) .
Most reef research is still relatively young and most
'long-term' time-series of ecological data began in the
last 35 years. Since many of the first scientists to work on
reefs considered that they were rather stable ecosystems.
the first observations of disease and damage recorded by
reef scientists were considered to be unprecedented and
catastrophic. In the longer term. a more pluralistic view
of reefs has arisen. It is clear that reef development is a
cyclical rather than a continuous process, with episodes of
rapid coral growth interspersed by episodes ofcoral death
and erosion.
Despite the natural variability and evidence of resil-
ience over large time spans. it is also clear that human
impacts are a threat to coral reef ecosystems. Today. the
relative roles of natural and human activities on reefs are
a focus of much research. which seeks to understand what
drives the balance between coral reef growth and bioero-
sion, the causes of coral bleaching. and what has been rec-
ognized as the worldwide degradation of reefecosystems.
The threats are both direct. from increased sedimentation,
destructive fishing practices. ship groundings. or pollu-
tion. and indirect. due to climate change and over-fishing
(Chapters 12 and 14) .
11.6.1 Disease
Corals and other reef organisms are susceptible to diseases
caused by pathogens or parasites (Richardson 1998) . The
likelihood and effects of disease may be aggravated by the
direct and indirect impacts of human activities. One of
the first recorded coral diseases was the so-called 'black
band disease' that affected brain corals in the Caribbean.
This is caused by the cyanobacterium Phormidium coral-
lyticum. which invades the coral tissue and produces a fine
black band that spreads across the surface of the coral.
The cyanobacterium and associated micro-organisms cre-
ate anoxia. which kills the living coral tissue . The bacte-
ria utilize the organic compounds released by the dying
coral cells. The black band will move a few millimetres
every day, leaving a bare coral skeleton, which is usually
colonized by filamentous algae. It appears that physically
damaged corals are more susceptible to black band dis-
ease . Several other diseases have since been recognized in
corals. although accurate diagnosis is often difficult.
Corals can suffer from a number of diseases leading to
large regime shifts in community structure.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
11.6.2 Storms, cyclones, and
hurricanes
In shallow water, storm-induced waves can lea d to destruc-
tion of branching corals and even to destruction of corals
on the reef slope due to debris falling from the reef crest.
Storms can also cause the death of reef fish when they try
to seek shelter in corals. which are then smashed by wave
action. Coasts exposed to frequent storms will have entirely
different coral communities from those found in sheltered
areas and close to the equator. where cyclones and hur-
ricanes are relatively rare. In the cyclone belt, typically
10° to 25° north and south of the equator, many shallow
reefs are dominated by fast-growing Acropora corals that
quickly recolonize reefs following hurricane damage. With
hurricanes occurring at intervals of years to decades. slow-
growing corals rarely have time to develop. The recovery of
reefs following storms may be further delayed by effects of
human activities.
Fast-growing corals dominate reefs exposed to cyclone
and hurricane activity.
11.6.3 Climate change
It is widely predicted that climate change will lead to ris-
ing sea levels over the next century. Future sea level rise
is expected to be 3-10 mm y-l and evidence suggests that
healthy corals could accrete at this rate in the past. How-
ever, there is concern that other impacts will weaken cor-
als, degrade coral communities. and impair their capacity
to accrete during periods of sea level rise. These other
factors include climate-linked increased frequencies and
intensities of storms or ENSO events (Chapters 7 and 15;
Box 11.2) and also direct human impacts. such as nutrient
inputs from poor land-management. In deeper water corals
11.6 Threats to coral reefs
will not photosynthesize or deposit carbonate as fast, and
their ability to keep up with sea level rise and resist bioero-
sion will be reduced.
11.6.4 Coral bleaching
Coral bleaching is a generalized response of corals to stress
(Coles & Brown 2003) . Bleaching is so called because the
zooxanthellae are ejected from the corals and the skeleton,
which is typically white, becomes visible (Fig. 11.10) .
Bleaching is also associated with decreases in growth and
reproductive output, and prolonged bleaching leads to
coral death. Following bleaching, the coral framework is
often taken over by bioeroding animals and reef growth
is replaced by bioerosion. Moreover. bleached corals will
be colonized by filamentous green algae, which, although
more productive. tend to take over the reef from corals and
thus reduce reef accretion. Since fish and invertebrates are
also commonly dependent on the refuge that coral pro-
vides, it is likely that many species will be lost and herbivo-
rous species will become more abundant.
Coral bleaching has major implications for the future of
coral reefs, leading to possible lo ng-term changes in spe-
cies composition of t he coral and its associated fauna.
Many of the most severe bleaching events have been
attributed to high water temperatures, which occur sea-
sonally and may be further enhanced in certain years by
regional climatic events. Bleaching can be induced by short-
term exposure to temperatures that are elevated by 3 to 4°C
and longer term exposure to elevations of 1 to 2°C, although
vulnerability to bleaching depends on the thermal regime
to which corals have already adapted.
The 1997-98 ENSO event caused increases in sea tem-
perature and bleaching on most of the world's coral reefs
Figure 11.10 Bleaching of
massive corals in the Galapagos
Islands. (Photograph: Simon
Jennings.)
 Chapter 11 Coral Reefs
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Box 11.2: Natural archives of were distinct biologically fo r more than 2000 years (Aron-
environmental change in corals and son et al. 2004).
reef ecosystems
Coral reefs have been profoundly impacted by humans but
it is not always easy to discern the relative roles of natu ral
and human processes in long-term changes. We expect
that the changes wrought by humans cannot decline in
the foreseeable future (e.g. McClanahan 2002) and in
some respects records of past change can inform us about
for ms of future change. We are lucky that through cor-
ing into reef structu res and individual corals (figure) much
information has been derived abo ut rates of change in the
surrounding environment and responses to this of the
co rals themselves and the wider commu nity. Four exam-
ples illustrate this remarkable historical data.
Massive corals from the Huon Peninsula of northern Papua
New Guinea retain an annual growth pattern and fluores-
cence of the growth bands that varies wi th rainfall, while
the relat ive natural abundances of the stable isotopes of
oxygen in the skeleton are indicative of EI Nino-related
changes in water temperat ure since 1880. This in turn has
made it possible to infer that EI Nino is not just a modern
phenomenon, but the magnitude of recent EI Nino events
tends to be larger than ove r the last 130 000 years (Tudhope
et al. 200 1). In western Sumatra, cores from massive corals Example of a co re of the co ral Acropora palmata
show that a mass mortality of corals and fishes on reefs coin- from Galeta Reef, Panama. The excellent preservation,
cided with upwelling and a bloom of algae, the latte r prob- upward-curving growth pattern of the individual coral-
ably driven by inputs to the sea of iron derived from burni ng lites, and light-coloured layer of crustose-co ralline algae
fo rest during a dry year (Abram et al. 2003) . at the top all indicate that this co ral has not been over-
Coral coring into whole reef structu res has shown that turned and probably w as part of a framework formed
at Discovery Bay in Jamaica, the modern changes in the in place. Submarine m icrocrystalline calc it e coats the
com munity are unprecedented over the last 1260 years coralline crust , a red encru sting foraminifer Homotrema
(Wapnick et al. 2004). In Panama, the community of reef tops this and penetrates the unprotected base of th e
corals has in the most recent decades converged wi th that coral. Scale bar 0.5 em (Macintyre & Glynn 1976). Photo-
of corals reefs some 1 50 0 km distant in Belize, which graph: Ian Maci ntyre.

outside the central and western Pacific. Ultimate ly this

led to large-scale coral m ortality and losses of 70- 80% of The f req uency of coral bleaching events is expected t o

coral cover on many reefs. The effects were particularly in crease in the future.

pronounced in the Indian Ocean, where more than 90%

of coral died. The biological and economic consequences
have been profound on many islands that rely on reefs to
act as coastal sea defences, to attract tourist di vers, and
to provide fishing grounds (Jon es et al. 2004) . Wh ile the
ENSO is a natural event, the frequency and intensity of
ENSOs may be affected by human -induced climate change .
The frequency of coral bleaching is expected to increase in
the future (Sheppard 2003) .
11.6.5 Crown-of-thorns starfish and
other coral predators
Crow n-of-thorns starfis h (Aca nth aster planci) feed on liv-
ing coral (Fig. 11.11 ), and at h igh abundance they can
kill large areas of reef. Crown-of-thorns starfis h are free-
spawning sexually reproducing species, and a single female

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
may produce 12 to 60 million eggs in a spawning season.
The eggs and larvae are planktonic for 9 to 23 days before
settlement. Following settlement. the juvenile starfish grow
to 1 em diameter in 4 to 5 months and shortly afterwards,
they start to feed on live coral. The juveniles grow fast and
reach maturity in 2 years or so. feeding on coral by everting
their stomachs over the live coral and secreting an enzyme
that breaks down the coral tissue, allowing them to absorb
the products. Crown-of-thorns starfish often move across
reefs in fronts, large groups of animals that kill most of the
corals in their path.
Crown-of-thorns starfish (COTS) are a major agent of
change on Pacific reefs.
Typically, the abundance of adult crown-of-thorns star-
fish is 1 to 20 km-2 , but during outbreaks they can reach
densities of SOD krrr-'. The first major crown-of-thorns out-
break that was witnessed on the Australian Great Barrier
Reef led to massive media interest and a race by scientists
to understand and control the population explosion. Out-
breaks have been reported from many other regions. There
are many possible causes of starfish outbreaks and no single
theory seems to apply in all circumstances. One popular
theory suggests that fishing has reduced the abundance
of fish predators on juvenile starfish, and this has allowed
the juvenile starfish to proliferate, leading to outbreaks of
adults in subsequent years (Moran 1986) . Other theories
suggest that outbreaks are due to natural phenomena, such
as exceptional larval recruitment. In reality, outbreaks
probably have different causes on different reefs, and both
natural and anthropogenic factors no doubt contribute.
11.6 Threats to coral reefs
There is evidence that outbreaks occurred prior to human
impacts. but equally, there is evidence for an increased
incidence of outbreaks in some heavily disturbed or fished
regions. Recovery of reefs may take 20 to 50 years.
Starfish outbreaks are often linked with disturbance asso-
ciated with fishing.
11.6.6 Pollution, sediments, and
nutrients
The main causes of increased sediment loadings on coral
reefs are run-off following deforestation. port develop-
ment. and dredging. Erosion rates from deforested farm-
land can be 100 times greater than from natural forests.
often reaching 1000 tonnes or more krrr- y-l. Coastal devel-
opment also increases sediment loading. as road run-off is
often discharged directly to the coast. It is hard to separate
the effects of nutrient inputs from those of sedimentation
on coral reefs, because they often go hand in hand. How-
ever, nutrients derived from industrial discharge. vegeta-
tion removal, and lack of sewage treatment are thought
widely to have accelerated algal growth on many reefs at
the expense of corals. Corals are also directly sensitive to
nutrients such as phosphate. Locally, oil pollution from
tanker or ship groundings has killed areas ofreef and there
are major concerns about increased nutrient levels from
farmland and sewage inputs.
Nutrients from agricultural runoff and sewage discharge
have accelerated algal growth at the expense of corals.
Figure 11.11 A crown-
of-thorns starfish
(photograph: Jeffrey
Jeffords/Divegallery.com).
 Chapter 11 Coral Reefs
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11.6.7 Fishing
Burgeoning human populations with inherent needs for
food and income have driven the development and expan-
sion of fisheries on coral reefs. Fishing leads to direct
damage to reef habitat and a reduction in the abundance,
biomass, and mean size of species targeted by the fishery,
and local extinction of the most vulnerable species. Fish-
ing can also have more profound and complex impacts on
the structure and function of reef ecosystems.
Habitat-destructive fishing methods may be used on
reefs, such as reef drive netting and trapping, blast and
chemical fishing. The latter methods are highly unselec-
tive and often adopted by fishers desperate to meet imme-
diate requirements for food or income. Blast fishing is
practised on many reefs, even though it is often illegal.
Commercially produced explosives from mines or arma-
ments are frequently used, but mixes of charcoal and
oxidizing agents are a common alternative. Completed
bombs are dropped into the water after igniting a short
delay fuse . Given that charges are deployed in different
locations, detonate at different depths, and contain differ-
ent types and amounts of explosives, it is hard to quantify
their impact. However, repeated explosive fishing reduces
actively growing reef to dead coral rubble. Much of the
kill is wasted, since fish and invertebrates will be eaten
by other fish, invertebrates, and birds before collection
begins, and fishers only collect a small proportion of the
remaining fish. Explosive fishing thus impacts the reef
ecosystem at all levels and recovery from damage takes
many years.
The ecological relationships between sea urchins and
fishes, which we discuss in 11.7, are readily affected by
fishing (McClanahan et at. 2002) . The persistence of her-
bivorous fishes appears to depend on the presence of sea
urchin predators, which maintain sea urchin populations
at a level where their low gross production makes them
inefficient competitors. A fishing-induced shift towards a
herbivore community dominated by one species of urchin,
rather than many species of fishes and urchins, has been
a major factor in the degradation of reef ecosystems in
the Caribbean. These impacts are further discussed in
Chapter 13.
Fishing has driven sea urchin population explosions in
some parts of the world.
Our examination of separate human impacts on coral
reefs is, of course, rather misleading. Even though scien-
tists tend to study single impacts, rather than synergistic
or cumulative impacts, impacts are rarely separable. Most
over-fished reefs, for example, will be found close to highly
populated areas, where agricultural development leads to
high sediment loadings, discharge of human and animal
waste leads to high nutrient loadings, and where land is
reclaimed for port developments and possibly housing. One
of the main criticisms of many human-impact studies on
reefs is that there is too much emphasis on finding a single
cause of change in the reef ecosystem, and not enough
emphasis on looking for synergistic and cumulative causes
(McClanahan 2002) .
11.7 Reef growth and
bioerosion
While corals are laying down limestone and building
reefs, many other reef processes are eroding the lime-
stone and producing coral rubble and coral sand even on
undisturbed reefs (Fig. 11.12) . Reefs are presumed to be
'healthy' and showing net growth when corals have the
upper hand. However, in many cases erosion is the domi-
nant process and the reef fails to grow. Even on growing
reefs, erosion rates are usually high and net accretion only
just exceeds net loss. Relatively small shifts in the struc-
ture of reef communities can thus shift the balance from
net accretion to erosion (Glynn 1997) .
Reef growth is a balance between accretion and bioero-
sron.
Most of the erosion of the reef substratum is by organ-
isms. Many of these bioeroders are not visible on the reef
surface, since they bore into coral skeletons. Internal bor-
ers include species of sponge, polychaetes, crustaceans,
and molluscs. While rates ofbioerosion are very variable,
and will depend on the solidity of the carbonate matrix,
borer abundance, and body size, bioerosion rates of over
2 kg CaCO, rrr- y-l have been recorded for individual spe-
cies. The principal external grazers are the larger species
of mollusc, echinoderm, and fish . Depending on abun-
dance, individual species can bioerode 3 kg CaC0 3 m-2 y-l
and more (Glynn 1997).
( Many bioeroders are hidden in the reef. )
Very few bioeroders invade coral through living tissue.
Rather, they tend to attack dead skeletons. Thus natural
and human impacts that lead to the death of coral tissue
(11.6) allow bioeroders to colonize . There are positive
feedbacks here, of course, since the death of corals allows
bioeroders to proliferate and the proliferation ofbioerod-
ers further weakens a reef and makes it more vulnerable to
storm damage. Storm damage will result in further coral
death, allowing more bio-eroders to colonize.
Some reefs have entered long-term cycles of net bio-
 11.7 Reef growth and bioerosion
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Internal bioeroders [bcrers]

Microborers
A. Algae, fungi, bacteria

Macroborers
B. Spanges (CHon/doe)
I C. Bivalves (Whophogo)
D. Barnacles (l, hot')'o)
E. Sipunculans (Aspidosiphon)
F. Palychaetes (E,,/ddoe)

External blcecders (gro" n)

G. Purrariish (Sror;doe)
H. PuHeriish (k o/hron)
I. Hermit crab (Anicu'",)
J. Limpet (Aemoeo)
K. llnhin (D/odemo)
L. Chitan (Aeon/hop'eoro)

Figure 11.12 Internal and external b ioeroders on a coral reef. After Glynn (1997).

erosion. In the Galapagos Islands. for example. where
conditions are not ideal for coral growth and where many
corals died afterthe 1982-83 ENSO, most reefs are slowly
crumbling to rubble with little sign of recovery. Even when
some recovery was observed, this was further stalled by
more coral bleaching and death. In Galapagos, the main
bioeroder is a sea urchin Eucidaris. which erodes carbon-
ate as it grazes and reached very high densities (up to 30
m~2) following the 1982-83 ENSO.
Sea urchins are important bioeroders of coral reefs and
are key 'ecosystem engineering' biota
The relative dominance of herbivorous fishes and inver-
tebrates has profound influences on rates of reef accre-
tion and bioerosion. The grazing activities of herbivorous
fishes clear space for coral settlement and enhance the
survival and growth of young coral colonies. Conversely,
urchin grazing leads to bioerosion, which may exceed the
rate of carbonate accretion. The significance of urchin
grazing was illustrated following a major die-off of urchins
in the Caribbean, when carbonate began to accrete in
some (less intensively fished) areas previously subject to
bioerosion. If urchin populations are established, they can
reduce algal biomass so markedly that they out-compete
herbivorous fishes . While grazing. the area-specific rates
ofbioerosion due to urchins are higher than those of car-
bonate eroding fishes such as parrotfishes, and urchins
have been implicated in limiting reef growth in many loca-
tions .
The loss of hermatypic corals through bleaching,
crown-of-thorns starfish outbreaks. and other causes
has potentially profound consequences for coral reef
ecosystems because the corals and underlying carbonate
constitute habitat for a vast range of species (Current
Focus) .
 Chapter 11 Coral Reefs
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CURRENT FOCUS: Impacts of coral
loss on coral ecosystems
Hermatypic corals may be the weakest link in coral reef
ecosystem resilience because they are susceptible to a
variety of large-scale threats including bleaching, dis-
eases, algal overgrowth driven by nutrient inputs and
loss of grazers, cyclone damage, and coral-predator out-
breaks. The link between sea surface warming and coral
bleaching means that corals may be the Achilles heel of
this iconic ecosystem and indeed coral cover is tending
to decline all over the world. But what is the connec-
tion between coral reefs as integral ecosystems and coral
cover? The widespread bleaching death of corals that
occurred in the Western Indian Ocean in 19 9 8 showed
that fish communities were affected in various ways. Those
species that were reliant on branchin g corals for food
or shelter declined quickly. These species include many
coral-feedi ng butterfly fish and damselfish, and co lo urful
gobies that live amongst the branches of corals. Such
species would be lost completely from areas where hard
corals were co mp letely elimi nated. Fortunately th ro ugh
11.8 Dynamics of reef animals
Coral reefs provide superb natural laboratories for the
study of ecology, behaviour, and population dynamics
because the inhabitants are usually so much more visible
than in many other marine ecosystems (Fig. 11.1 3). Coral
reefs have indeed provided many examples of important
ecological processes and responses of these to environ-
TECHNIQUES:Visual and other
assessments of coral reef health
Over the years, abundant data have accumulated on vis-
ible aspects of community structure, such as densities
of particular species or groups of fishes and the bottom
cover of hard corals. However there are many potential
pi tfalls in such data and it is frustrati ng that the absence
of clear protocols used in the collection of past data con-
strai ns our ability to identify and interpret past trends.
Mobile animals like fish are a case in point. Here, visual
techniques have been prevalent but these include circular
and rectangular areas (transects), areas varying greatly in
size, and gathering of visual data accordi ng to different
the potential dispersal of larvae, areas can locally recover
from such loss. However where larval supply is limited
(as at remote oceanic sites) the recovery may be slow.
This has been the case in the Seychelle Islands, where
9 years after the 1998 bleachi ng event, coral cover was
still low, although thankfully sufficient to allow some return
of coral-dependent fish to shallow-water reefs. In other
locations, such as the Chagos Archipelago (British Indian
Ocean Territory), coral recovery was faster because cor-
als in deeper water were not affected by the bleachi ng,
and long-term impacts on fish species have been small.
The Seychelle Islands, however, also illustrate that where
coral recovery is poor, the recruitment to some reef-asso-
cia ted fishery species may be adversely affected because
of the nursery function played by live branching corals.
Mari ne protected areas (Chapter 16), because they had
been put in locations where there was a lot of branching
coral that was especially susceptible to bleachi ng , suf-
fered particularly bad ly. The structural complexity of the
habitat declined more and declines of fish species were
greater in most cases than in unprotected areas.
Reference: Pratchett et al. (2008).
mental changes. Clear water however does not guarantee
ease of understanding! Even accurately recording densities
of animals may be surprisingly difficult (Techniques box) .
This is regrettable; interpreting past changes in populations
through existing data requires us to be able to combine data
that may prove surprisingly different in the way they were
collected and thus in the light they may throw on particular
aspects of the ecosystem.
protocols. Major issues arise with the counti ng of small
cryptic and large mobile species. Most surveys do not
include crypt ic species, while the variability of data for
large species is so great that the statistical power to detect
differences in time or space is small. What th is means is
that the best data are derived from studies focusing on
particular species or groups of species. The small species
are more accurately recorded in small areas that are inten-
sively searched, and in some cases these counts have
been checked against other techniques. The large mobile
species are more likely to be encountered in large sample
areas with plenty of replicat ion but avoidance of divers
and other factors like mobility can mean they are under-
estimated. In Fiji for example, emperors (Lethrinidae) are
 11.8 Dynamics of reef animals

important in fishery catches around reefs but these are
rarely recorded in underwater census work! Likely local
extinctions of large species, such as the bumpheaded
parrotfish (Bolbometopon muricatum), were in fact identi-
fied by surveys of fishe rme n's knowledge. Techniques
such as baited video have been used elsewhere but these
cannot give estimates of actual densities. The visual data
can be used to give rough estimates of biomass where
the length of individual fish is also recorded; however,
accuracy of length estimation under water comes only
wi th training and ongoing verification. For competent
data collection, underwater visual census work requires
substantial preparation also fo r species' identification,
underwater record ing, and so on. For bottom cove r, visual
data are also widely used, but for the information to be
consistent and for observer errors to be reduced, careful
preparation and training are requi red. More reliable data
on the benthos come from use of video transects, though
these requi re a definite protocol (e.g. distance of camera,
angle, categorization of bottom cover) and often involve
painstaking work back in the laboratory.
For further information see McClanahan et al. (2007).

However, it is perhaps not surprising that scientists have

used reefs to test many hypotheses about the processes that
structure an imal communities.

Reefs provide ideal natural laboratories for the study of

behaviour and ecology.

One nice example of the ways in which coral reefs have

been used as laboratories is for the study of the factors
structuring reef fish communities. In the early years of reef
science, when many scientists were still coming to terms
with the species richness and range ofadaptations observed
in reef fishes, they were quick to suggest that the high
di versity of reef fishes must be a consequence of commu-
nities that were structured by very strong competition for
resources. This was assumed to res ult in population sizes
close to carrying capacity and limited by the availability of
shelter or food. Moreover, the supply of larvae was assumed
to be almost limitless in comparison with the capacity of
established populations to accept new individuals. Care-
ful experimentation and study of the dynamics of reef fish
populations soon falsified this hypothesis, and it was clear
that population sizes were often determined and limited
by the rates at which larval fish recruited from the plank-
ton to the adult populations: the 'recru itm en t limitation'
hypothesis. This also implied that one species would not in
time out-compete another, because the local abundance of
juveniles was unlikely to be related to the number ofspawn- Figure 11.13 The clear, warm water overlying coral
ing adults at the same location. In these terms, population reefs means that they are ideal places for the study of
sizes and thus whole commun ities would be less orderly, marine ecology. Many fish and corals are highly visible (a)
being determined by chance events in the plankton. and thus divers can easily conduct underwater studies
However, no one facto r can adequately account for the of marine life (b). (Photographs: Simon Jennings.)
complex structure of reef fish communities. For one thing,
there may be significant recruitment to local populations
derived from local adult spawn ing (Jones et al. 1999). likely to be observed when the potential of the community
There is also evidence that communities are not necessar- to absorb settling individuals is high. In this case, the subse-
ily chaotically structured; in some respects patterns are quent abundance of a cohort w ill be a function of the abun-
repeated in space and in time. Recruitment limitation is dance at settlement and density independent mortality.
 Chapter 11 Coral Reefs
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Figure 11.14 Striped cleaner wrasse (Labraides
dimidiatus) attending a monocle bream (Sec/apsis sp.),
These wrasse use their thick lips and front canines found
at the front of both jaws to remove ectoparasites.
(Photograph: E. Schloql.)
Conversely, when the capacity of the community to absorb
settling individuals is lower, density dependent mortality
may be detected and result in modified relative abundance
(Doherty 2002} .ln overall terms, the structure and dynam-
ics of reef fish communities are determined by many of the
same factors that determine the abundance of much less
visible communities in deeper, muddier, and superficially
less attractive ecosystems.
No single factor can adequately account for the complex
structure of reef fish communities.
Of note amidst the great wealth of coral reef species is
the large number of very close associations. such as sym-
bioses. between species . We have already considered the
coral-zooxanthellae relationship that is a basis for reef
construction, but there are many more. These include fish
that live with burrowing shrimps and in sea anemones. and
delicately coloured crabs that live within coral heads. There
are shrimps that live deep inside the shells of hermit crabs,
and small fish, such as the 'cleaner wrasse'. that remove
ectoparasites from fish that could easily eat the cleaner.
Such close associationshelp to explainhow so many species
can coexist; they also highlight how in many cases the loss
of one species may have knock-on effects on others (Fig.
11.14) .
11.9 Reefs and human society
There is no doubt that coral reefs are threatened by climate
change and direct human impacts, and that globally reefs
will be very different a few years hence from what they are
now (Knowlton 2001) . Yet reefs are more than a source of
fascination and a scientist's and tourist's playground. For
millions of people, often in the poorest countries of the
world. reefs provide their food and income.
Reefs are a source of food and income for millions of
people.
On many tropical coasts. subsistence fishing is the main
source of dietary protein and fish protein accounts for a
greater proportion of total dietary protein in countries
where per capita gross domestic product (GDP) is low
(Kent 1998). In the fishing villages of the Pacific Islands,
fish consumption of200 to 300 g per person d~l is common
and is far greater than the consumption of other protein.
For the South Pacific Islands as a whole, with a population
of around 6.5 million, per capita annual fish production
is approximately 17 kg. In the heavily populated coastal
regions ofSoutheast Asia and Central America, people treat
fishing as a fallback source of food and income when no
alternatives are available.
Subsistence fishing is the main source of dietary protein
in countries where GDP is low.
Many reef fish caught for subsistence are not traded and
are not recorded in conventional fishery statistics. Thus
their value to society may be overlooked by policy-makers.
For the Pacific Islands, Dalzell et al. (1996) calculated the
replacement value of subsistence fisheries production as
$US180 million, substantially more than the $US82 mil-
lion of commercial fisheries production.
Coral reefs are alsovaluablebecause they attract tourists.
especially divers and snorkellers. Over ten million people
visit the Great Barrier Reef in Australia each year. provid-
ing annual tourist revenue of around $US700 million and
making it one of the most commercially significant ecologi-
cal sites on the planet. Over 25%of all tourists visiting the
Seychelles Islands pay to enter one of the Marine National
Parks, and the income from this has exceeded the budget of
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the government's Division of Environment. Whole towns,
such as Sharm El Sheikh in Egypt are supported by revenue
from tourist divers in the Red Sea, to the extent that a ship
grounding in the nearby Strait ofTiran resulted in compen-
sation payments for reef damage of $US1765 m-' . Valua-
tion ofcoral reefs as a source of tourist revenue is a complex
process. depending on expected rates of recovery and 10s5
of value to tourist divers (Spurgeon 1992) .
Reef tourism has brought significant economic benefits
to many countries but also contributes to the anthropo-
genic pressures that act upon coral reefs.
a result of coral mining, coral bleaching, or sedimentation
may leave coasts vulnerable to wave erosion and storms. In
the Indian Ocean's Maldive Islands, the mining of corals as
building materials has removed sections of reef and left the
coast exposed to wave action. The cost of replacing these
reefs with concrete blocks that dissipate wave energywould
be $US2 million krrr' . The government recognized that it
would be ecologically and economically efficient to use the
concrete for building and to leave the coral reef where it
was! Rates of coral mining have been cut from a peak of 1
million tonnes year ! in the early 1990s to a few thousand
tonnes at designated sites today.

Reefs also provide important ecosystem services in Reefs act as coastal defences and hence provide an
terms of coastal defence. Shallow reefs cause waves to import ant 'service' for human society.
break and dissipate wave energy. Loss of these defences as

Chapter Summary
• Coral reefs are some of t he most diverse and productive commun ities in the marine environment.
They are created from tiny coral polyps but are easily visible from space. With the exception of
deep water corals, most corals grow at temperatures of 18-36°C and most are found 30° north
or south of t he Equator:
• Coral reefs are rarely stable communities living in benign environments. Rather, they are continuously
evolving and subject to physical disturbance on time scales from seconds to centuries.
• Contemporary distributions of reef corals and associated animals reflect 200 million years of
evolution and the separation of oceans due to continental drift.
• Rates of reef growth only just exceed rates of bioerosion, while fixation of carbon only j ust meets
the community respiratory demand for fixed carbon. Small shifts in reef community structure due to
human and environmental impacts can lead to net bioerosion and loss of net productivity.
• Coral reefs constitute natural laboratories for the study of ecology. Thus reef science has made impor-
tant contributions to the w ider understanding of marine ecology.
• Reefs provide millions of people, often in the world's poorest countries, with a vital source of food ,
income, and other environmental services.
• Coral reefs are threatened by human impacts, including fishing , pollution, sedimentation, and
climate change.

Further Reading
The edited boo k by Birkeland (1997) Life and Death on Coral Reefs is an excellent summary of the his-
tory of reefs, reef growth, and the impacts of natural and human activltles, Spalding et al. (200 1) provides
detailed maps of global reef distribution, protected areas, and human threats to reefs. This is an essential
reference text for anyone w ith an interest in coral reefs. Sale's (2 00 2) edited book on reef fishes gives
a good description of the ecology of fishes on coral reefs and shows how reefs provide a perfect natural
laboratory for the study of fis h ecology,
Chapter 11 Coral Reefs

• Birkeland , C. 1997, Life and Death an Coral Reefs, Chapman and Hall, New York,
• Sale, P. F. (ed.) 2002, Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem, Academic Press,
San Diego,
• Spalding, M, D" Raviliaus, C, & Green, E, P. 2001 . World Atlas of Coral Reefs. University of California Press,
Berkeley.
Polar Regions

Chapter Summary
The polar oceans and seas have been a lure for the explorer
and scientist ever since the first whalers and sealers identi-
fied them as rich hunting grounds. They are now receiving
much attention due to a rapidly changi ng landscape and sea-
sonal dynamics attri butable to global climate change (IPCC
2007a, 2007b, 2007c). Organisms living in Arctic and Ant-
arctic waters are ad apted to low temperat ures, long periods
in the year of poor, or no light, and an ecosystem dominated
by the seasonal formation, consolidation, and subsequent
melt of a layer of frozen seawater that can be more than 10
m thick. The effects of global climate change are likely to
have profound influences on these regions, especially in the
Arctic. However, ou r understanding of their ecology, and
therefore th e potential threats of cl imate change, is still
rud imentary due largely to the hostile working condi tions.
Like other extreme envi ron ments, th e metabolic and physi-
ological adaptations th at enable life to go on are a pote n-
t ial source for novel biotechnological applications, and polar
organisms, in particular microorganisms, are also poten tial
proxies for life on extrate rrestrial syste ms.

12.1 Introduction
Cold, hostile, barren , wh ite wastelands would be a fairly
typical impression of the frozen pack ice that covers polar
oceans and seas. This image is reinforced during the long
polar winter when, if t he sun does rise above the horizon,
the fleeting light is no more than dull d rear y half-light. Even
in summe r, snow blizzards can descend with no warning,
forming cond itions of such poor visibility that it is impos-
sible to see just a few centimetres in front of you. It is of
course not all gloom and despondency, and even in the
bleak winter, ethereal displays of aurora borealis (in the
North) or aurora australis (in the South) , light up the sky in
electromagnetic pyrotechnic displays that enhance the feel-
in g of being in a part of a world governed by physical forces
quite disco nnected fro m the rest of the Ear th (Fig 12.1 ).
At its maximum extent area pack ice (Fig. 12.2) can
cover an area comprising 13% of the Eart h's surface,
making it a biome that compares with those of the tundra Figure 12.1 Aurora borealis lighting up the sky over a
and deserts. Outside of the polar circles, sea-ice is also frozen sea-ice land scape in west Greenland (photograph:
an ephemeral feature of the Baltic, Caspian, and Okhotsk David Thomas).
 Chapter 12 Polar Regions
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Seas. Despite this, the study of these regions still lags
behind what is known from temperate and tropical seas.
Relatively few oceanographic research expeditions ven-
ture into polar waters each year, and there are limited
numbers of coastal research stations. so that despite over
200 years of scientific endeavour in the Arctic and Antarc-
tic, polar marine research is still a rather young research
area. Vast expanses of the polar oceans and coastlines
remain unvisited, and we know very little indeed about
the polar systems in winter, simply because even now we
cannot conduct large-scale research programmes during
winter months.
Pack ice can cover areas as large as the t undra and des-
erts , although because of host ile working condit ions we
know relatively little abo ut these frozen realms.
Seagoing research is always expensive, but specially
strengthened ice-breaking ships that can sail into pack ice
(Fig. 12.3), and whose powerful engines consume vast
quantities of extra fuel to break through even modest ice
fields, are even more expensive than the norm. There are
permanently manned coastal stations dotted around the
Antarctic continent, as well as stations that are just manned
for the summer. Likewise. on Arctic coasts there are several
research centres that conduct scientific research through-
out the year. although for logistical reasons most of the
activity takes place during summer months. However, these
stations are few. and the hostile conditions and immense
effort in simply keeping the stations running mean that
research opportunities are limited during winter months.
There have been attempts to study pack ice processes by
establishing floating ice camps. These are either set up by
freezing a ship into the ice and building a camp around the
ship, or deploying the equipment and camp personnel by
Figure 12.2 The seasonal
dynamics of polar seas and
oceans are dominated by
the annual formation and
consolidation of millions of
square kilometres of frozen
seawater that drive ocean
circulation, climate, and
the ecology of the regions
(photograph: David Thomas).
air. In 1992 a floating base on the sea-ice was established
for the joint Russian-American expedition. Ice Station
Weddell, in the Weddell Sea. The ice camp started in the
February drifting northwards with the pack ice until finally
breaking up in the June . A similar concept was used for the
year-long Arctic SHEBA project, October 1997 to October
1998. where 35 scientists. technicians, and a ship's crew
collected valuable time-series' data on the physics, chem-
istry, and biology in and under the pack ice. Studies such
as these have highlighted the need for multidisciplinary
research teams combining forces to maximize the under-
standing of the key processes taking place.
Ice camps and drift stations are good opportunities for
collecting temporal data sets in pack ice regions.
There is a longer history of drift stations in the Arctic
than in the Antarctic, and probably the most famous ice
drift in ships were the pioneering drifts by Nansen on
the Fram from 1900 to 1906, and Amundsen from 1918
to 1925 in the Maud. Since these early ship drift experi-
ments. there has been a large number of ice camps in vari-
ous parts of the Arctic. The longest series of camps were
those by the Russian scientists who started annual pack ice
camps in 1937 that continued until 1991. The stations were
generally constructed on multi-year ice floes about 2 km in
diameter and 3 to 5 m thick. The series was started again in
2003 with station NP-32, which ended in March 2004 when
the researchers had to be rescued as their ice floe began to
break up. These drift stations have collected some of the
most comprehensive data sets about weather patterns,
ocean processes, and of course the sea-ice on which they
were floating.
Polar regions are places of stark contrast. It is not with-
out reason that the polar oceans are considered to be some
 12.1 Introduction
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Weekly mean seawater temperatures

--
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Daily freshwater pool temperalures

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<-,q."'i. ~<::J <::::J'I>

Daily mean soil temperatures

Figure 12.3 Modern ice-breaking research ships, such 10
as the German RV Polarstern, enable scientists to study 5
deep into pack ice, throughout the year. They become
0
floating laboratories and are key to the rapid progress
~ /0 :.
made in our understanding of these hostile regions of --
~
0
-5
the past 50 years (photograph: David Thomas). --
.e
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~

- 10
• " •.. f .-
• "'C•
~

• ~ , ~\J.
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of the most hostile places on Earth for life to survive, but
surprisingly they support considerable life. Contrary to the '" - 20
" · .,S·'
l'
I. •
picture described above, in the summer the polar experi-
- 25-
ence is dominated by long days, where at the height ofsum-
mer the sun does not sink beneath the horizon. Although
seldom hot, temperatures rise to such an extent that it is
possible to work in lightweight clothing, and one of the
greatest problems is ensuring that the correct precautions Figure 12.4 Seasonal variability in mean temperature
are taken to avoid severe sunburn. Peck et al. (2006) illus- in Antarctic marine, freshwater, and terrestrial sites.
trate this point in their comprehensive review of the envi- Data presented for sea temperatures are from Signy
ronmental contraints on life in Antarctic ecosystems. Not Island (northern maritime Antarctic) and McMurdo
only are there large ranges in seasonal light and tempera- Sound (continental Antarctic). Data for freshwater and
ture, the latitudinal differences in climate are huge when terrestrial temperatures are from Adelaide Island
looking at Antarctica as a whole (Figs 12.4 & 12.5) . They (southern maritime Antarctic). From Peck et al. (2006).
stress how environmental pressures. in particular tem-
perature. are key in determining resource and colonizable damental ecological consequences. As further illustrated
space availability, resulting in many biological differences by Brierley and Kingsford (2009), it is the vulnerability to
between organisms living as little as 10 m apart with fun- changes in seasonal dynamics. in particular those linked
 Chapter 12 Polar Regions
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Air Soil Freshwater pool Sea at 20 m

20 -,-::------,---------, 20 -,-::------,- - - - -----, 2-,-::------,- - - - ---,
December December December December

10 10 10 I

0 0 0 0
--
~

---,•
0

c -10 - 10 -10 -I
~
•
... E
- 20 - 20 - 20 -2

- 30 - 30 - 30 -3

July July July July

1--.----.-,,--.--'-1
10 14 18 22 26 30 10 14 18 22 26 30 10 14 18 22 26 30 20 22 24 26 28 30
Time (dale)

Figure 12.5 Maritime Antarctic variability in temperature in summer (blue lines December) and winter (red lines July). Data
show comparisons of short-term (sub-hourly) temperature variability in summer (thick upper line) and winter (thin lower
line) over several days in air, soil , freshwater, and marine environments (all data for Signy Island). From Peck et al. (2006).

to se a-ice dynamics, that make the polar regions so acutely

fine tuned to even slight climate perturbations. Conditions at the poles are not uniformly harsh . In winter

The distinctive seasons at the poles are of course the rea- it is difficult to imagine any life existing at the poles. In

son for the obvious migrations and behaviour of the larger summer, life flourishes during the long days, and tem-

biota: polar bears, arctic foxes, walrus, seals, whales, pen- peratures can be above freezing .

guins, and a plethora of other seabird species (Sale 2006).

Intriguing as the behaviours and ecologies of these larger
animals a re, the seasonal free zing over of polar oceans, the
consolidation of an ice layer on the surface of the water. and
its subsequent melt have far-reaching consequences on the
whole of the ecosystem. in particular the seasonal dynam-
ics of the plankton and the season ality of coastal benthic
communities. In this chapter various aspects of polar eco-
systems will be discussed w it hin the framework of seasonal
changes in the extent of sea-ice.
Pack ice not only influences the polar regions themselves.
but also helps drive global ocean thermohaline circulation
patterns through the formation of deep water masses (Box
12.1 ), as well as influencing global weather patterns. Over
the past decade there has been increasing interest in the
effects of global climate warm ing on sea-ice dynamics. and
the consequences for global ocean circulation and the ecol-
ogy of polar regions.

Box 12.1: Sea-ice and ocean
circulation
Despite their very different characteristics, they are all
interconnected by a large-scale movement of water that
is re ferred to as The Globol Conveyor Belt (Broecker 199 7;
Broecker et al. 199 9; Clark et al. 2002).
The basis of themohaline circulation is that when a kilo-
gram of water sinks from the surface into a deeper part
of the ocean, it displaces a kilogram of water from the
deeper waters. As seawater freezes in the Arctic and Ant-
arctic and sea-ice fields form, cold, highly saline brines are
expelled from the g rowing ice sheet (see 12.2), increas-
ing the density of the water and making it sink.
In the conveyor bel t circulation, warm surface and inter-
mediate waters (0- 1000 m) are transported towards the
northern North Atlantic, where they are cooled and sink to
form North Atlantic Deep Water that then flows southwards.
In southern latitudes, rapid freezing of seawater during
ice formation also produces cold, high-density water that
sinks down the continental slope of Antarctica to form
Antarctic Bottom Water. These deep-water masses move
into the Sou th Indian and Pacific Oceans where they rise
towards the surface. The retu rn leg of the transport begins
with surface waters from the northeastern Pacific Ocean
flowing into the Indian Ocean and then into the Atlantic.
It is not just the temperatu re and salinity of the deep-
water formation in the polar regions that is crucial to the

-- . _.-
ocean circulation. These water masses are oxygen-rich, and
so are fundamental for transport ing oxygen to the ocean
depths whe re respiration by deep-sea organisms con-
sumes oxygen. The transport of dissolved organic matter
and inorganic nut rients are also fundamentally governed
by this t ransport, increasingly nutrients being remineralized
The freezing of seawater to form the pack ice of the
Arctic and Antarctic is fundamental for the deep water
circulation of water masses.
12.2 What is pack ice?
Because ice is the dominant feature governing the ecology
of polar regions, it is prudent to understand exactly what
pack ice is.
Icebergs are not derived from seawater, but are broken-
off pieces of freshwater glaciers and ice shelves.
Although icebergs are a conspicuous feature of polar
marine landscapes, they are not actually formed in the
sea itself, but derive from the large glacie rs and ice sheets
that cover the Antarctic continent or Ellesmere Island and
Greenland in the Arctic (Fig. 12.6). The ice sheets grow
from snow accumulation and spre ad out, eventually reach-
ing the coasts . The ice sheets, less dense than seawater,
can spre ad to cover thousands of square kilometres of the
ocean. Tides, currents, wind, and wave action cause stresses
in these huge masses of ice that result in them breaking up,
or calving, into icebergs that vary in size from a few square
metres to m any hundreds of square kilometres. Icebergs in
12.2 What is pack ice?
The si nking of co ld saline
water in the Arctic and Ant-
arctic Weddell and Ross Seas
drives large-scale ocean circu-
lation in t he so -called Global
Conveyor Belt.
(see Chapters 2 & 3) duri ng the transfer of the deep-water
masses. Therefore, water rising at the end of the co nveyor
bel t in the northeastern Pacific has higher nutrient load-
ing, and lower oxyge n conce ntrations than North Atlantic
waters at the begi nning of the conveyor belt (Sarmiento
et al. 2004).
shallow coastal regions can ground, caus ing severe disrup-
tion to benthic communities (see also Chapter 1), whereas
others are carried on ocean curre nts where they are slowly
broken into smaller components and of course melted. Due
to the physical pressures and strains that form in these hu ge
blocks of ice, they can somet imes explode in spectacular
fashion.
Pack ice is instead formed from the freezing of seawater
in autumn when the surface of the water is cooled to below
- 1.8°C, the freezing point of seawater (Eicken 1992). The
resulting ice crystals rise to the surface whe re they aggre-
gate into dense slicks of grease ice. It is at this early stage
that the ice is 'in ocu lated' with organisms because plank-
ton stick to, or are 'sca ve n ged' by, the ice crystals as they
rise through the water. After a few hours of further freez-
ing, the ice crystals accumulate to form loosely aggregated
discs, ice pancakes, 5 to 10 em in diameter (Fig. 12.7).
These grow larger becoming 20 to 50 ern thick 'sup er pan-
cakes', several metres across. Wind and wave action raft
the pancakes together, and often several end up lying on
top of one another. They freeze together and after one or
two d ays a closed ice cover h as formed, strong enough to
support working on the ice with heavy sledges, generators,
and ice-coring equipment. Further free zing and the subse-
quent thickening of the ice take place by congelation ice
growth, where water molecules free ze on to the bottom of
the ice sheet. However the pack ice zone is still dominated
 Chapter 12 Polar Regions
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 12.6 Sea-ice (foreground)

is frozen seawater, and not the
same as icebergs, which are
formed when the freshwater ice
sheets flowing off the Antarctic

- continent (cliffs in background)

break up (photograph: David
Thomas).

by water currents, wind, and wave action, and ice floes are
continually being moved apart. so that areas of open water
appear between the floes, or rafted under great pressure
so that huge ridges over ten metres thick comprised of ice
boulders span large distances.
The pack ice undergoes a characteristic formation pro-
cess includ ing grease and pancakes.
Unlike freshwater ice, frozen seawaterforms a semi-solid
matrix, permeated by a network ofchannels and pores (Fig.
12.10) . Salt does not enter the ice-crystal structure and so,
as the ice forms. salts and other dissolved constituents of
seawater are expelled and collect as a highly concentrated
brine solution within the labyrinth of brine channels and
pores in the ice matrix (Weissenberger et al. 1992; Krembs
et al. 2000) . The morphology of these channels and pores,
the total volume of the ice occupied by them, and the salin-
ity of the brines contained within them, are governed by
temperature and the age ofthe ice. In colder ice the volume
occupied by the channel system is less, and the salinity of
the remaining brine is higher than in warmer ice. As the ice
grows and ages there is a continuous loss of brine due to
brine expulsion and gravity drainage, resulting in a gradual
reduction of bulk ice salinity (Box 12.1) .
When seawater freezes it is not solid but rather forms
a structure more akin to a sponge fi lled with a highly
concentrated brine.

Figure 12.7 Pancake ice

forms when sea-ice crystals
coagu late and grow together
in turbulent water conditions
(photograph: David Thomas).
 12.3 Arctic vs Antarctic pack ice
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

12.3 Arctic vsAntarctic pack
•
Ice
There are profound differences between the Arctic and
Southern Oceans with major implications for the organisms
living in the two regions (Spindler 1994; Comiso 2003b) .
The total area covered by the Southern Ocean (between
50 to 60 and 70"S) is about 36 million km-, much larger
than the 15 million krrr' of the Arctic Ocean (between 70
to SOON) . At its maximum extent. sea-ice in austral winter
forms a girdle covering 20 million km 2 around the Antarc-
tic continent. This is an area greater than that covered by
North America. By summer this has melted to a mere 4 mil-
lion km- . In contrast, the Arctic Ocean is almost totally cov-
ered by about 14 million km 2 of frozen seawater in winter,
although by summer only about 7 million krn- melts (Fig.
12.8) .
The la rgely land-locked Arctic Ocean has considerably
more ice, which lasts several years compared to the
larger Southern Ocean , which has predominantly ice that
lasts just one year.
The main reason for these differences is that the Arctic
basin is a Mediterranean-type sea almost enclosed entirely
by land. There are only two broad openings, at the Bering
and Fram Straits. where exchange with other oceans is
possible . In contrast. the Southern Ocean is a circumpolar
girdle that is open to, and exchange is possible with, the
Atlantic. Indian, and Pacific Oceans. Therefore a much
higher percentage ofArctic sea-ice lasts for longer than one
year (multi-year ice) even surviving up to 10 years or more,
whereas most of the ice in the Antarctic lasts less than a
year. Consequently the Arctic ice has the greater mean ice
thickness of around 3 .5 m, compared to 1.5 m for Antarc-
tic sea-ice. Rafting and deformation processes can result in
significantly thicker floes being formed in localized areas
(Haas 2004) .
An important feature of the Arctic Ocean is that about
one-third of the ocean is taken up by shelf seas with depths
of 100 m or less. In fact the Arctic Ocean only has a mean
depth of 1800 m, the smallest ofany ocean. In the Antarctic,
the continental shelves are very narrow. and so the Antarc-
tic pack ice zone is largely overdeep oceanic basins between
4000 and 6500 m deep.

lal March. 5, 2000 Ibl Sept. 11,2000 I

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...."""
2'"
' 8%
" ..
"'"
.8%

Figure 12.8 The maximum

a nd m inimum extent of sea-ice
600s cover in the Arctic Ocean (top)
a nd Southe rn Ocean (bottom)
(images: Josefino Com iso, NASAl
GSFC).
 Chapter 12 Polar Regions
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There are no river inputs into the Southern Ocean, in
stark contrast to the Arctic basin into which flows consid-
erable freshwater run-off from large river systems.
The Southern Ocean is largely cut off from terrestrial
influence, except for limited aerial deposition. whereas the
Arctic basin is characterized by a high input of fresh water
from many large river systems. such as the Mackenzie, Db,
Lena. and Yenisey. These river systems naturally input high
amounts of suspended solids, dissolved organic matter,
and inorganic nutrients (Dittmar & Kattner 2003). Natu-
rally these rivers also discharge pollutants such as PCBs,
heavy metals, and biological contaminants, which will be
absent from the Antarctic. As a result of such large amounts
offreshwater input, much of the surface waters of the Kara,
Laptev, East Siberian, and Beaufort Seas have low salini-
ties. Arctic ice formed in coastal areas can be heavily laden
with sediments, which are then transported large distances
in the moving ice fields carried by the transpolar current.
Even allochthonous material, such as tree trunks and soil
turfs, become encased in Arctic ice floes and are eventually
released many thousands of kilometres from the place they
were initially caught up in the ice.
Even during the melt seasons there are significant differ-
ences in the ways in which melting takes place. As summer
approaches, more solar radiation is absorbed by the ocean,
and the surface layer of the ocean warms up, increasing the
rate of melting of the ice. However, in the Arctic the sea-
ice begins to melt at the surface and extensive melt pools
form decreasing the albedo (reflectance of light) from the
ice surface, allowing more solar radiation to be absorbed,
thereby increasing the melting process. In the Antarctic,
melt occurs mainly from the bottom and sides of the ice
floes, which are in contact with the ocean, and melt pools
are less often encountered on the surfaces of Antarctic sea-
•
Ice.
Surface melt ponds are a conspicuous feature of the
surface of Arctic ice in summer. These are only rarely
found in Antarctic ice.
12.4 Life in a block of ice
Underneath a pristine white snow cover, the ice is often
a light-brown through to rich-coffee colour, caused by
a thriving sea-ice biota composed of a multitude of tiny
(mostly microscopic) organisms comprising viruses, bacte-
ria, algae, protists, flatworms, and small crustaceans (Fig.
12.9). They include many of the plants and animals of the
phyto- and zooplankton ofthe open ocean, which is in fact
where they originate (Chapter 6) . Unlike their counterparts
in warmer seas and oceans, these polar planktonic organ-
isms have a unique phase in their seasonal cycle when they
are caught up into the semi-solid matrix of the ice (Garrison
1991; Palmisano and Garrison 1993; Thomas & Dieclanann
2002).
Often sea-ice is turned brown due to a rich microbial flora
and fauna that grows within the semi-solid ice matrix.
As grease ice forms, planktonic organisms stick to, or
are caught between, ice crystals as they rise through the
water when surface waters freeze (Box 12.2; Garrison et
Figure 12.9 The growth of
photosynthetic diatoms can
reach such proportions that the
ice floes are frequently co loured
brown (photograph: David
Thomas).

al. 1989). Subsequently, as the ice grows and consolidates,
the organisms become trapped with in the brine ch annels.
Bacteria are conspicuou s in sea-ice assemblages, enter-
ing the ice mostly on the surfaces of larger organisms. As
temperatures drop there is a gradu al transition in bacte-
rial populations from the diverse mixed-species' inoculums
originating in seawater to psychrophilic species (mini-
mum growth temperature < DOC, optimal growth tempera-
ture < 15°C, and m aximum growth temperature < 20°C).
The growth of psychrophilic heterotrophs (Dem ing 2002)
is fuelled by large pools of dissolved organic m atter (DOM)
cons isting largely of carbohydrates produced by the death
and lysis (breaking apart) of sea-ice organisms, as well as
by the exudation of organic polymers by algae and bacteria
(Fig. 12.10). Muc h of this organic m atter is produced as
extracellular polymeric substances (EPS; Krembs et al.
2002) , in suc h quantities that in dense sea-ice microbial
Box 12.2: Where do ice organisms
come from?
For several of the sea-ice fauna, the mechanisms by which
they are incorporated into sea-ice is unclear, since many
do not have an obvious planktonic life. The most obvious
vector is that residual multi-year ice contains populations
of organisms that act as innocula for new ly formed ice.
Whereas t his is fine in t he Arct ic, in t he Antarctic only a
very small percentage of the sea-ice lasts for more than
one season, so this seems unli kely.
Nematod es are apparently not present in Antarctic
sea-ice (only one record by Blome & Ri emann 19 9 9 ) , a
stark contrast to Arctic sea-ice, where free-living species,
especially belonging to the superfamily Monhysteroida, are
found in abundance (Riemann & Sime-Ngando 199 7). No
rotifers have been found in Antarctic sea-ice either, even
though these too are also common in Arctic sea-ice sam-
ples. The reasons for these Arctic/Antarctic differences are
unclear, and it is possib le that they are simply sampl ing
artefacts: in t ime, more comp rehens ive sampling may
produce more com plete faunal records for Antarctic sea-
ice. Foram iniferans, w hich are very abundant in Antarctic
sea-ice, had for many years remained unknown from Arctic
sea-ice but since the late 19 9 0 s have now been found
t here, albe it only in a few samples. Alternatively, it may
be that suitable vectors for colonization of sea-ice are not
present in the Antarct ic.
In coastal reg ions wi th shallow water depths it is not
d ifficult to imagine colonizati on of the sea-ice fro m the
12.4 Life in a block of ice
assemblages , there is evidence that the organisms are liv-
ing in a situation more akin to biofil ms .
The most con spicuous organ isms in the ice are pen-
n ate diatoms (un icellular photosynthetic microalgae; Fig.
12.10), which reach such concentrations that their photo-
synthetic pigments discolour the ice brown. Diatom stand-
ing stocks up to 1000 ug chioro phylll-l have been measured
in sea-ice, which compare with typical values of 0 to 5 pg
chlorophyll 1-1 for surface waters in the Southern Ocean
(l.egendre et al. 1992 ; l.izotte 20 01 ). Primary production
in Antarctic sea -ice (63 to 70 Tg C y-l) is estimated to con-
tribute S% to the total annual primary production (1300 Tg
C y-l) in the sea-ice influenced zone of the Southern Ocean.
This apparently minor contribution is in fact highly signifi-
cant, in that the sea-ice organisms provide a concentrated
food source that extends the short period of primary pro-
duction in the water column (Box 12.3).
benthos by larv al stages, even in species w ith poor swim-
mi ng capabil ities. Another commonly cited vector in shal-
low w ater is lifting of organisms from the benthos attached
to anchor ice, platelets of ice formed in shallow coastal
waters. However, most of the pack ice, espec ially in the
Antarct ic, overlies water several th o usand metres deep
and here mechanisms of colonization by non-plankton ic
organisms remain enigmat ic.
Antarcti c t urbellarians spawn in sea-ice in aust ral sum-
mer. Eggs, j uveniles, and adults w ill be released into the
water col umn upo n ice melt. Altho ugh sea-ice t urbellarian
species can swim, none have been reported in the plankton
and it is presumed that they sink to the sea floor. It has
been sug gested t hat sea-ice t urbellarians may have an
adhesive d isk by w hich they attach to crustaceans before
being released from the ice. Swi mming crustaceans,
including amphi pods that migrate from the sea floor to
the ice peripheries, or the common ice copepods may act
as vectors to transfer the flat worms to different ice floes
(Janssen & Gradinger 19 99 ).
Many ciliate spec ies have been described fro m sea-ice,
wi t h no eq uivalent p lanktonic form being descri bed (Petz
et al. 199 5). It is specul ated that for many of these spe-
cies, colonizat ion takes place v ia rest ing spo res, although
there is no d irect evidence for th is. There is a simil ar
conundrum for the Arctic nematodes, and even w hale
baleen plates that conta in th rivin g po pulations of nema-
todes have been cited as poss ible vectors for bring ing
nematodes into close contact w ith sea-ic e floes.
 Chapter 12 Polar Regions
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I salinities found in the smaller channels. Rotifers can pen-
Figure 12.10 A sea-ice diatom in a sea-ice brine
channel (photograph: Christopher Krembs).
Up to 5% of the total Southern Ocean primary produc-
tion takes place wit hin the sea-ice. However; this forms a
highly concentrated food source for grazing zooplankto n
in winter when the water column is devoid of food.
Heterotrophic protists and metazoans. such as rotifers,
nematodes. turbellarians, foraminferans, and small cope-
pods can accumulate in sea-ice at concentrations ranging
from hundreds to thousands of individuals per litre; sev-
eral orders of magnitude higher than those in the water
(Fig. 12.11 ; Schnack-Schiel et al. 2001; Michel et al.
2002) . The smaller protozoans and metazoans graze the
dense growths of bacteria, flagellates, and diatoms, while
the narrow brine channels exclude larger species from
exploiting these food sources (Krembs et al. 2000) . Small
~f
"0
channels with diameters < 200 urn have been shown to be
effective refuge from grazing organisms. Only rotifers and
turbellarians can traverse 'channe ls' significantly smaller
than their body diameter. Turbellarians change their
body dimensions in response to salinity changes, shrink-
ing (because of osmotic water loss) with the increasing
etrate channels just 57% the width of their body diameter,
w hereas most other organisms simply congregate in the
narrowest of the tubes into which they can physically fit,
according to body size. Even despite the physiological and
biochemical prerequisites for survival and growth within
the ice matrix, there have been surprisingly few obligate/
endemic microalgal or protozoan species associated with
•
sea-Ice.
The smallest brine channels within the ice provide micro-
scopic refuges from grazers for diatoms.
Within the ice there is therefore a complex microbial
food-web based on a concentrated source of primary pro-
duction within the ice . Although ice is an effective barrier to
light, the light conditions within the ice are certainly more
favourable to algal growth in the top 2 m of the ocean's
surface th an when the algae are mixed through the upper
mixed-water layers in open waters . Sea-ice algae also have
well-developed photo-acclimation and adaptation (see
Chapter 2), resulting in them h aving efficient light-harvest-
ing mechanisms for growing in low light (Kirst & Wieneke
1995) . As long as re-s upply of inorganic nutrients is pos-
sible, either by exchange or remineralization processes
(Cha pters 2 & 3) within the ice itself, dense algal biomass
is ensured.
Figure 1 2.11 Food-web based
around the Antarctic pack ice. (a)
pennate diatoms; (b) autotophic
flagellates; (c) foramin ifers; (d)
ci liates; (e) turbellarians; (f)
copepod nau plii; (g) harpactico id
cope pods; (h) calanoid copepods;
(i) euphausiid larvae ; (k) Antarctic
krill, Euphausia superba; (I)
young notot henoid fish, such as
Pagothenia borchgrevinki. Note
not to scale (i mage: Sigrid Schiel).

Sea-ice organisms are adapted to low light, low tempera-
tures, and high salinities, all prerequisites for life within
a block of ice.
Surprisingly not many endemic organisms have been iso-
lated from Antarctic or Arctic sea-ice.
Naturally this growth has implications for pelagic organ-
isms that remain free of the ice matrix. Amphipods, cope-
pods, krill, and ice fish are examples of types of organism
that graze on the rich food source associated with the ice
(Schnack-Schiel 2003). This food source is collecte d on the
peripheries of ice floes or in cracks and crevices of rafted
ice, or ice that has recently been broken up or begun to melt.
For many of these organisms their seasonal dynamics and
life histories are tightly coupled to a source of food in the
ice, and even the interannual distributions of krill, the piv-
otal organism in the Southern Ocean food-web, is strongly
correlated with pack ice cover because of food contained
w ithin it (Box 12.3).
The complex interaction of low temperatures and high
salinities in sea-ice brines of course bring about changes
in the biochemical nature of the organisms themselves
(see Chapter 2), and in turn implications for their qual-
ity as a food source for protozoan and metazoan graz-
e rs. For example, polyunsaturated fatty acids (PUFAs)
Box 12.3: Southern Ocean krill
Euphausia superba stocks in the Southern Ocean are esti-
mated to exceed 1.5 billion tonnes (cf. the total mass of
people on the Earth approximates to 0.5 billion ton nes) and
are the primary food for squid, penguins, seals, and baleen
whales. In fact they are often referred to as being central to
the Southern Ocean food-web (see reviews in: Nicol & de
la Mare 19 9 3 ; Brierley & Thomas 2002). Krill feed vora-
ciously on phytoplankton and also feed carnivorously on
copepods. Krill populations can form dense swarms, which,
if they come to the surface, can tu rn the water a spec-
tacular blood red.
Adult krill can survive extended periods of starvation,
even shrinking over winter periods. However, j uvenile krill
require a constant supply of food. The dense growth of
sea-ice organisms, often on th e periphery of ice floes,
provides such a source of food throughout t he w inter
w hen food in th e water column is not present. When th e
ice melts, the organisms released from the ice can initiate
ice-edge algal blooms that are rich grazing grounds. Even
12.4 Life in a block of ice
are produced by both bacteria and microalgae; however,
many ot her marine organisms cannot produce PUFAs, and
require them to be supplied in their diet (Nichols 2006).
Enhanced PUFA production wit hin sea-ice algae and bac-
teria has been measured, induced by low irradiance, low
temperature, and high salinities, and therefore se a-ice
assemblages will be a richer source of essential PUFA for
grazing organisms . Since the conditions that stimulate
PUFA production in sea-ice microbes are most extre me
in winter, it is probable that PUFA production in the ice
organ isms w ill be maximal at that time. Organisms graz ing
within winter sea-ice will therefore have a diet enriched in
PUFAs, which may be a significant factor in maintaining
viable stocks (especially for zooplankton larvae ), and for
maintaining the fitness, enabling the exploitation of more
favourable feeding conditions upon ice melt in spring. An
example of such seasonal dynamics is shown by Arctic
copepods. Female Ca lanus glacialis have been shown by
Soreide et aJ. (2010) to feed on the PUFA-rich ice algae in
the spring to fuel an early maturation and reproduction,
w here as the subsequent offs pring feed on the high-quality
food during the phytoplankton bloom in the ice -free wate rs
2 months later. Naturally with diminishing Arctic ice cover
(Current Focus) such timings and feeding dynamics w ill
be change d, and since copepods are a rich food source, it
is likely that the transfer of energy-rich lipids through the
food chain w ill be greatly affected.
if blooms are not initiated, the large amounts of particulate
material released from the ice upon melting are valuable
food sources.
It is now clear that the distribution patterns of krill are
closely linked to sea-ice condit ions. In years when sea-ice
cover is prolonged there is significantly higher krill recruit-
men t, and in some reg ions of the Antarctic, krill abundance
can be predicted on the basis of cycl ical variations in sea-
ice exte nt (Atkinson et al. 2004). However, it cannot be
underestimated how difficult it is to catch and study the
population dynamics and behaviour of krill. Nat urally, until
this can be done reliably over wide geographic regions,
ou r understanding of krill biology is limited. Nicol and Bri-
erley (20 10) outline the pros and cons of a variety of
techniques that have been employed, including net sur-
veys, photographic/video, and acoustic methods.
The salp (So/po thompsonii) is thought to reach high den-
sities in years following red uced ice extent. Salps live for
less than one year, and feed by filter-feeding phytoplank-
ton. They do not feed on ice organisms. In the absence of
krill, the salps are able to exploit the spring phytoplankton
 Chapter 12 Polar Regions
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Other seabirds

.~
• '(
(, ) I
Penguins

Algae
Zooplankton
(induding kri' ~II)~~-J~}- -:)
---
("-._ - - _ ..
• • Seal
Boeterio Protozoa

Simplifi ed drawing of Antarctic pelag ic food-we b s how ing th e cent ral role of krill as a 'keysto ne s pecies' (after
Med lin & Priddle 19 9 0 ).

bloom and undergo explosive population growth. In good
sea-ice years, the krill have the upper hand over the salps
because the sea-ice has provided good feeding grou nds
over the winter, resulting in good gonad development and
possibly allowing multiple spawning to take place. In these
years the krill exploit the phytoplankton bloom, resulting in
poor food stocks for the salp populations.
One of the problems with the studies abou t the distri bu-
tion of krill under sea-ice is the difficulty in actually mea-
suring the distribu tion of the krill. Recent developments in
autonomous underwater vehicles (AUVs) mean that it is
now possible to deploy them reliably under pack ice to con-

o - 45

-so
25
· 55

50
E
- GOO- m lon g tran sect
und er ice floes by Autosub
-65
75 equipped w it h an upw ard-
and d ownw ard-l o okin g
-70
echo-so u nder. Th e hu g e
100
·75 swar ms of krill are swi m-
min g mainly at a wate r
L -_ _~_ _~_ _~_ _~ ~_ _~_--'L.......j· 80 d epth of 50 m (image:
100 200 300 400 500 Andrew Brierley, from Brier-
Distance (m) ley et al. 2002).

duct extensive echo-sounder surveys covering areas of many
hundreds of square kilometres. In a study in the Weddell
Sea in January 200 1, the density of krill w as th ree times
higher under the ice compared to open water, wi th the
vast majority of the krill wi thin a band 1 to 13 km south
of the ice edge (Brierley et al. 2002).
In another study using innovative technology for observ-
ing marine organisms, Clarke and Tyler (2008) used the
deep-water, remotely operated vehicle, ISIS, and rat her
Krill population dynamics are reviewed by Brierley and
Thomas (2002).
12.5 Sea-ice edges
When large volumes of sea-ice melt. the freshwater
released lowers the salinity in the waters at the ocean su r-
face and can stabilize the upper water column, effectively
setting up a frontal system, which is associated wit h algal
blooms (e .g. Strass & N6t hig 1996 ; also see Ch apter 2)
and subsequent higher rates of grazing . In the Southern
Ocean, the spring phytoplankton bloom tracks polewards,
beginn ing in October, in the wake of the melting ice-edge.
Rates of sea-ice decay are equ ivalent to movements of the
sea-ice edge of up to 1.6 km h-' . With the exception of tides
over mudflats, the passage from day to night, or the spread
of forest fires, it is difficult to conceive of a faster changing
biological environment (Squ ire et aJ. 1995). The marginal
ice zone (MIZ) exten ds u p to 100 to 200 km in width,
the extent of which is determined by the pe netration
of waves and swell that break the pack into numerous
12.5 Sea-ice edges
surprisi ngly showed adult krill grazing at depths down to
3000 m. Not only was it surprising that krill are found at
such depths (it was previously thought that they lived in
the upper 500 m) , additionally many mature females were
viewed at the greatest of depths. The authors point out
that because krill are such strong swim mers it would only
take the individuals about 4 h to migrate fro m the deepest
sites to the surface.
smaller floes. Floe size increases rapidl y w it h distance
from the sea- ice edge (Fig. 12.1 2). Although more pro -
nounced in the Antarctic, MIZs are also important features
in the relatively limited zones where Arctic sea-ice meets
warmer waters .
Melting sea-ice releases vast volumes into the surround-
ing sea, often forming a stabilized , low-salinity surface
water layer in which algal blooms take place.
Alt hough the stabilized water column has often been
observed at melting ice-edges, it is not always the case.
When there are strong pre vailing winds and pronounced
wave activity in the MIZ, the released fresh water will be
effectively mixed wit h surface waters (Bathmann et a1.
199 7; Murphy et aJ. 1998).
The blooms of algae take place because there is a
reduced likelihood of algae being mixed downwards into
light-limited depths. The inoculum is often species being
released from the ice matrix. It is not just an inoculum of
algae of course, and inorganic d issolved nutrients, DOM,
bacteria, metazoans, and protozoans released from the ice
all contribute to a highly dynamic biological system. In turn
Figure 12.12 The concentrati on
of ice floes in the marginal ice
zone (MIZ) decreases further
toward s the open ocean. The
surface waters of MIZs ca n be
highly productive, if stabilized by
melt water from melting sea-ice.
(Photograph: David Thom as.)
 Chapter 12 Polar Regions
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the blooms are a rich feeding ground fo r zooplankton , and

in turn larger predators. Swarms of krill feeding in 'fren-
zies' have been recorded at ice edges, and in turn the MIZ
is often a very intense feeding ground for seabirds , whales,
and seals. Birds and mammals also utilize the ice edges in
their migrations, exploiting the rich food sources as they
migrate.

Ice-edge algal blooms in turn attract zooplankton graz-

ers, often in a 'frenzy' of feeding activity. In turn , birds
and mammals are attracted to ice edges for the rich
sources of food .

Not all of the material released from the ice is incorpo-

rated into ice-edge blooms (Riebesell et aJ. 1991 ). There
have been studies to show that much of the biology ac tually
aggregates into large accumulations and sinks quickly to
depth as m arine snow (Chapte r 3). The feeding of zooplank-
ton on the ice organisms can also effectively package a high
percentage of the ice biota into rapidly sinking faecal pellets Figure 12.13 Faecal pellets produced by zooplankton
(see Fig. 12.13). Mean settling velocities for faecal pellets of and protozooplankton are important in transporting
between 60 and 200 m day-' are common, although values organic matter from surface waters to the benthos.
up to 1500 m day-' are reported (Levente r 1998). There The faecal pellet shown was collected at 400 m, and
are numerous reports of faecal pellets from copepods and is full of sea-ice diatoms consumed at the surface.
protozoans containing unbroken ice di atom frustules, often Interestingly, many of the diatoms seem to be intact.
of monospecific origin, reaching the sediments. Krill faecal (Image: David Thomas.)
pellets contain mostly broken/digested diatom frustules
and are easily broken. Therefore their efficiency as a major
flux-mediator to great depths is questionable, despite them Aggregating ice organisms and faecal-pellet production
having potentially high settling velocities . However, a sed i- results in a large downward flux of biogenic material to
ment trap under a krill swarm recorded a flux of 660 mg C the underlying sediments.
m-2 d- 1, which is the greatest flux recorded fo r faecal matter
of herbivo rous plankton (Ca dee et aI 1992).

Box 12.4: Biology and products for
elucidating past sea-ice extent
Contrary to the satellite record account of sea-ice in the
Antarctic presented in the Current Focus box, Curran et
al. (2003 ) provided indirect evidence that, at least in
some regions of the Southern Ocean, there have been
decreases in sea-ice since 19 50 . They measured con-
centrations of methanesulphonic acid (MSA) in ice cores.
This is a breakdown product of OM S, which in turn is a
brea kdown product of DMSP (Chapter 2) produced in
large quantiti es by algae in the high-salinity, low-temper-
ature bri nes of sea-ice. By measuring concentrations of
MSA in the glacial ice core, they have estimated sea-ice
extent in a particul ar sector (80 0E to 140 0 E) off the east
Antarctic coast. They estimate that sea-ice extent in th is
region was rather constant between 184 1 an d 19 50 and
th ereafter there was a sharp decrease of about 20%.
Dixon et al. (20 0 5) also measured MSA concentrations
in several ice-sheet ice cores and estim ated that the sea-
ice extent in the Amundsen an d Ross Seas was generally
hi gher, from 180 0 to 19 9 2 compared to the period 14 8 7
to 18 0 0 . Most recently Becag li et al. (2009) have shown
MSA concentrations in the glacial ice of Talos Dome to
be a good proxy fo r sea-ice extent in the Ross Sea over
the past 14 0 years.
Interestingly the results of Curran et al. (200 3) were
not to o dissimilar from conclusions drawn from analyses
of early whalin g records. De la Mare (1 9 9 7 ) estimated

th e extent of the Antarcti c summer ice-edge from posi-
ti ons where w hales were caught, or record ed by scien t ific
expeditions, from the early 19 205 up to 19 60 . This is
because the w haling for blue, fin, and mi nke w hales was
focused on product ive ice-ed ge reg ions and there was an
internati onal requirement to record the pos it ion of w hale
catches. Therefore it w as possib le to make estim at ions
of previo us ice-ed ge extents before satellites w ere used,
and compare these to the satell ite data collected since the
19 70 s. De la Mare concluded that there had been a 2 5%
drop in the extent of t he summer sea-ice in the Southern
Ocean in j ust twenty years. However, ot her analyses of the
data had ind icated t hat t he w hale catch data may not be
as re liable as first thought (Ackley et al. 2003; Vaughan
2000). The debate has conti nued and most recently
The major characteristic of this flux from the ice is the
highly seasonal nature of short pulses of organic mate-
rial that result in adaptive feeding strategies for benthic
organisms , which may receive only occas ional pulses of
material. This effect is compounded by the short, intense
periods of primary production that are characteristic of
open w aters in polar re gions (Ch apte r 2) , quite differ-
ent from the fluxes of material in tropical or temperate
regrons,
In both the Arctic and Antarctic su mme r, light is not
the limiting factor to phytoplankton growt h in the open
ice-free waters when day lengths reach up to 24 h. In win-
ter, light is severely limiting. Low temperatures are not
considered to be limiting to phytoplankton production in
either of the polar regions. Despite such similarities, the
productivity of the open Arctic and Antarctic waters are
quite different. Over much of the open Arctic Ocean, the
water is strongly stratified wit h a d istinct pycno cline at
between 20 and 50 m (Chapters 2 & 7). Inorganic nutri-
ents in the su rface waters are quickly exhausted follow-
ing phytoplankton growt h . Nut rien ts are only replaced
by regeneration processes in the surface waters, or when
the pycnocline is disrupted and nutrient-rich water from
below introduced into the surface wate rs . In coastal
waters or regions of nutrient upwelling, such as along the
western Bering Strait, primary production yields are simi-
lar to temperate regions.
It is important to note that the Arctic Ocean and seas
cover consid erable latitudinal gradients , ranging from
sub-polar, wit h seasonal conditions quite similar to those
d escribed for temperate regions in Chapters 2 and 3 to
the waters close to the north pole which have a very short
window of the year in which primary production can take
place (Fig. 12.14; Leu et aJ. 2011). There is a great ten-
d ency to cons ider the Arctic as a whole , but Fig. 12.14
12.5 Sea-ice edges
Corte and Guinet (2007 ), accounting for the b ias in the
w haling data, also high light a signif icant reduct io n in the
sea-ice exten t happeni ng in the 19 60 s, espec ially in the
Wed dell Sea region.
Another example of sea-ice algal-prod ucing b iomark-
ers for elucida ti ng past sea-ice extent is t he recently
described C25 mono unsat urated hydrocarbo n (IP25)'
wh ich has been found to be prod uced by sea-ice diatoms
and to be very stable in sed iments over geo log ical t ime
(Belt et al. 2007, 2008). The marker has proven to be a
robust proxy for sea-ice and the position of ice edges as
far back as the past 300 000 years have been est imated
from its presence in sedim ent cores taken from different
regi ons of the Arcti c (Masse et al 2008; Muller et al.
2009; Vare et al. 20 10).
clearly indicates that more precise consideration of large-
scale processes needs to be made. Although the same holds
true for the Southern Ocean, the latitudinal range covered
is not as great as in the Arctic, since much of sout hern
polar region between 70 0 S and the south pole is actually
covered by the land mass of the Antarctic continent.
Natu rally, sea-ice cover has profound implications
for the amount of light penetrating deep into the water
column. This potentially has consid erable effects on the
diel vert ical migration of zoopla nkton (DVM), which is
often thought to be triggered by light. Likewise summer-
time periods wit h no , or very short, night periods could
8S'N I- _ n
80'N 1__
7S' N 1_
~
Mar Apr May June July Aug Se pt
Figure 12.14 Conceptual overview of the primary
production regimes in the European Arctic along a
latitudinal gradient. Image courtesy of Eva Leu and first
published by Leu et al. (2011).
 Chapter 12 Polar Regions
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severely impede the environmen tal triggers for DVM
behaviour. Wallace et al. (20 10) h ave looked at the influ-
ence of sea-ice cover on the DVM of Arctic zooplankton,
and found that in ice-free sites there was a synchronous
migration, whereas in ice-covered sites there was asyn-
chronous behaviour. Interestingly these authors do not
think the e ffect of ice on the DVM was particularly du e
to light effec ts, but rather due to effec ts of the ice cover,
in conju nction wit h the hydrography, on food availa bility,
turbidity, and species compos ition . Cottier et al. (2006)
h ave also identified an unsynchronized DVM during Arctic
summe r, whic h returned to a more synchronous behav-
iour once there was a significant period of night.
The Southern Ocean has high concentrations of inor-
ganic nutrients at all times of the year. In contrast, the
Arctic surface waters become nutrient-limited.

Box 12.5: Washing powder to 'life in space'

The brown colouration of the ice on the surface of the moon of Jupiter, Europa, has raised the tantalizing link with
ice systems on Earth. It is unlikely that the colouration is due to diatoms, although organisms that live in sea-ice
are useful proxies in the growing field of astrobiology (image: courtesy of NASAfJPL-Caltech).

In recent years, the stu dy of sea-ice org anisms has inten-
sified, fu elled in part by the realization th at the physio-
logical and biochemical acclimations that micro-organisms
thriving in the ice have to undergo may have consi derable
pote ntial for biotechno logical app lications. These incl ude
the prod uction of po lyunsaturated fatty acids, w hich in ice
organisms keep membranes fluid at low temperatures, for
aquacultu re, livestock, and human food. Research is also
concentrating on the use of cold-adapted enzymes for a host
of industries, ranging from cleaning agents to food process-
ing (Cavicchioli et al. 2002).
Some of the keenest interest in sea-ice organism biol-
ogy co mes from the new breed of astrob iologists w ho are
enthusiastically scrutinizing the ice-covered seas of Jupiter's
moons, Europa and Ganymede, and the surface of Mars, as
well as speculat ing about life in the ice-covered neoprotero-
zo ic 'snowball earth' . Despite the tantalizing lure to co m-
pare the brown colouratio n observed on Europa's surface
to diatom-coloured sea-ice, the extraterrestrial ice syste ms,
tens to hundreds of kilometres thi ck, are substantially differ-
ent to the 1 to 10m thick ice we know from Earth's polar
oceans. If life form s do exist, or have existed on these bod-
ies, it seems that they will be quite unlike those that domi-
nate the sea-ice found on Earth today (Cavicchio li 2002;
Chyba & Philli ps 2002; Marion et al. 2003).
 12.6 Polar benthos
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In contrast, the Southern Ocean is an example of a
high-nutrient, low-chlorophyll region. Inorganic nutrients
are seldom limited in open waters, but at the same time
phytoplankton growth is moderate. Open waters rarely
become stratified, except for the stratification at ice edges
discussed above. Recent large-scale iron-fertilization
experiments indicate that, for many regions of the South-
ern Ocean, a paucity of iron is the major factor limiting
the potential for phytoplankton growth (discussed in more
detail in Chapter 2) .
Nicol et al. (2010) have raised an intriguing hypothesis
that krill actually store about 24% of the available iron in
the Southern Ocean, and that the eating of krill by baleen
whales (the major consumers of krill) is an efficient way
of releasing iron back into the system. They analysed the
iron content of faecal matter from whales and found it
to be particularly iron-rich. They went on to hypothesize
that 'allowing the great whales to recover might actually
increase Southern Ocean productivity through enhancing
iron levels in the surface layer.'
12.6 Polar benthos
form solid blocks of ice. In some sites, it is not uncommon
for macroalgae and seagrasses to become encased in the
sea-ice. together with fauna that was not able to migrate
to deeper waters (Fig. 12 .15) . When ice melts in the late
spring, melt ponds consisting of freshwater form, and big
sheets of melting ice can result in lowering of the salini-
ties of the surface waters of coastal waters for significant
periods of time . Fast-growing, short-lived opportunistic
macroalgae such as Enteromorpha dominate the resulting
floras of the ice-scoured parts of shores.
Tide or wind-driven blocks of sea-ice are particularly
effective in clearing intertidal areas of all sessile organ-
Isms.
The effect of ice scour and the clearing of benthic habi-
tats by seasonal drifting ice can reach down to depths of 10
m or more in extreme cases, and ice disturbance is possibly
the major structuring element of polar nearshore biologi-
cal communities (Gutt 2001; and Chapter 1). Therefore
sublittoral communities can be highly disturbed, at times
showing characteristics of a highly ephemeral flora and
fauna (Box 12.5).

Blocks of ice, especially on a shore with a large tidal range,
can be very effective at removing attached intertidal
organisms (Fig. 12.15) . It is therefore a general feature
of polar intertidal shores that very little life is supported
from autumn through to late spring when ice thaws again.
Tide pools, even large ones. are no refuge. since these just
The keels of icebergs can cause dramatic destruction
of benthic assemblages growing at depths between 10
and 500 m.
In particular, in shallow coastal regions in both the Arctic
and Antarctic, the grounding of icebergs causes consider-

Figure 12.15 (a) Blocks of loose sea-ice are effective at scouring rocky shores clean of attached organisms,
especially in reg ions with a high tidal range. (b) In some shallow sites macroalgae, seagrasses, and inve rte brates can
become encased into the sea-ice matrix. (Photographs: David Thomas.)
 Chapter 12 Polar Regions
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able d amage to benthic com m u nities (Gu tt 2000; Gerdes
et al. 2003; Gu tt & Piepenburg 2003) . However, the keels
of large icebergs can be ve ry d eep and damage from large
icebergs scraping across the benthos has been recorded
by remotely operated vehicles carrying camera and video
equipme nt. Sessile organisms are erad icated and pioneer
species begin to grow in high abundances on the disturbed
substratum. In some areas, major iceberg scour events have
been estimated to take place over periods of every SO to 200
years. The consequence of this periodicity in disturbance,
combined with t he slow growth of many species (particu-
Box 12.6: Macroalgae in polar regions
Some macroalgal species, including the red Iridaea cor-
data, occu r at latitudes of 77 °5, w here th ey experience
up to 10 mon ths of ice cove r. Polar macroalgae are gener-
ally highly adapted to low lig ht conditions often growing
under sea-ice fo r much of the year, and only experiencing
short windows of light in the summer (reviewed by: Kirst
& Wieneke 1995; Wieneke et al. 2009; Wulff et al. 2009).
Many species are severely photo-inhi bited (see Chapter
2), even at low incident irradiances and/or susceptible to
ultraviolet radiation damage, although in some species this
damage is slight if measurable at all (Karsten et al. 2009).
Several species, including the brown Laminaria solidun-
gu/a from the Arctic and the red Po/maria decipiens from the
•
•
Several species of macroalgae grow in seaso nally ice-covered wat ers, are very efficient primary producers at low
light, and have seaso nal growth st rateg ies t o best utilize the sho rt w indows of light in summer months (photo graph:
David Thomas).
larly in Antarctica) . rneans that areas disturbed in this man-
ner are likely to be characterized by a continuous natural
fluctuation between extreme d isturbance and recovery.
Com munities ca n be held at early successional stages, or
even completely destroyed by scouring, and these effects
occur from t he intertidal to depths down to sao m in Ant-
arctica. The wide scales of d isturbance intensity are thought
to contribute to the overall high levels of Antarctic benthic
biological diversity. Iceberg scour effects are less prevalent
in the Arctic where there are far fewer icebergs compared
to the Antarctic.
Antarctic, actually begin to grow during periods of darkness
at the end of th e wi nter, w hen still covered by the ice.
These species have not found a way of growi ng without
light. Instead they begin to grow by using the starches and
other metabo lites that they sto red in the previous year's
growth period. The new tissues produced are ready to begi n
photosynthesis as soon as light becomes available when the
ice breaks up. This kick-start maximizes the growth period
during the short su mmer months. The development of
new blades in the dark is probably controlled by circannual
rhythms governing seasonal growth patterns. This hypothesis
is supported by indications of free-running growth rhythms
when these seaweeds are grown under constan t conditions
(Wieneke et al. 2009).
•
./ .
"

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Kirst and Wieneke (1995) review many of the responses
of polar macroalgae to low light and low temperatures.
12.7 Polar bentho-pelagic
coupling
The largest proportion of the Antarctic shelf benthos fauna
is made up of sessile suspension-feeders, such as sponges,
cnidarians, bryozoans, ascidians, and echinoderms (Fig.
12 .16). Suspension feeders can feed on a whole range of
particulate organic matter, extending from bacteria, pica-
and nanoplankton, through to zooplankton several centi-
metres in length, a particular species having adaptations
for a particular size class of food (reviewed by Arntz et
al. 1994). Any extensive assemblage comprised of differ-
ent types of suspension feeder will be a three-dimensional
community with a range of feeding strategies and types
that have the ability to exploit this huge spectrum of food
classes.
Suspension feeders make up the vast majority of shelf
and deep sea benthos of polar regions.
Such suspension feeders survive in an environment of
high primary production in spring and summer. but almost
nothing in winter, and so the scarcity of primary production
and diverse abundant benthic assemblages of high biomass
are somewhat anomalous. It was long thought that these
organisms simply fed on the short pulses of phytodetrirus,
and then survived long periods of feeding inactivity. How-
12.8 Endemism in polar benthos
ever. it now seems that this is not as straightforward. In par-
ticular. resuspension of sediments and lateral advection
of organic rich material. are important for the transport
of biogenic material from shallow sites to deeper basins.
Resuspended and advected material is thought to be the
main food source during winter months when the influx of
phytodetrirus and faecal pellets from waters above is negli-
gible (Klages et al. 2001) .
There is evidently no uniform pattern in the degree of
coupling ofAntarctic invertebrate benthic animal reproduc-
tion and the extreme seasonality ofprimary production and
concentrated food source. However, there are many exam-
ples where reproduction takes place uncoupled from the
summer supply of food. One explanation is that the organ-
isms utilize the high influx of food to best build up gonadal
tissues to the maximum.
12.8 Endemism in polar
benthos
The benthic floras and faunas of the Arctic and Antarctic
are quite different. In general. the numbers ofspecies in the
major groupings of macrobenthic organisms are between
1.5 and 6 times greater in the Antarctic than the Arctic. In
fact the Antarctic species diversity is akin to the same levels
of diversity recorded for tropical regions (Brey & Gerdes
1997; Chapter 1). The differences are also compounded by
the fact that there is a much higher degree of endemism
among the Antarctic flora and fauna compared to that of
the Arctic (Briggs 2003) . The degree of endemism varies
greatly between different groupings of organism: up to
Figure 12.16 In many regions
:-..- surrounding the Antarctic, the
benthos is covered by diverse
assemblages of suspension
feeders. The bentho-pelagic
coupling between seasonal
primary production in the water
column and transport of this
food source to the benthos
is key to the survival of such
assemblages. (Photograph: Julian
Gutt, Alfred Wegener Institute.)
 Chapter 12 Polar Regions
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70% of the fish genera and 95% of fish species found in the
Antarctic are endemic; whereas only 5% of polychaete gen-
era and 57% of the polychaete species in Antarctic waters
are endemic. Only about 5% of the macroalgae found in
Arctic waters are endemic, and in the Antarctic 30% of the
macroalgal species found are endemic. Interestingly crabs,
flatfishes, and balanomorph barnacles, common in the Arc-
tic, are missing from the Antarctic fauna (Eastman 2000) .
Of course these numbers are only approximate and change
considerably as more taxonomic research takes place, and
by the introduction of powerful molecular techniques to
unravel phylogenetic conundrums.
The whole question of endemism and species' diversity
and abundance in the Southern Ocean flora and fauna is
of course greatly limited by the relatively small areas that
have been properly surveyed. For example, the Antarctic
deep-sea (abyssal) benthos has received little attention,
and has often been viewed as a region of low biodiversity.
However, three coordinated expeditions in the deep Wed-
dell Sea (748 to 6348 m) between 2002 and 2005 showed
that this is not true (Brandt et at. 2007) . Among the 13000
specimens examined, the team found : 200 polychaete spe-
cies (81 previously unknown to science), 160 species of
gastropods and bivalves, 76 species of sponges (17 previ-
ously undescribed), 674 isopods (585 new to science), 57
nematode species, and 158 foraminifera species. Likewise,
studies on metazoans (size fraction 32 to 1000 mm) from
the South Sandwich Trench (Brant et at. 2004) revealed
unexpectedly high standing stocks, well above the pre-
dicted estimates from worldwide relationships of meiob-
enthos abundance and water depth.
Alt ho ugh there are only short pulses of food descending
from upper water layers, resuspension and lateral advec-
tion of sediments are important processes for feeding
sessile organisms for the rest of the year.
There are a much higher number of endem ic genera and
species in th e Antarctic compared wit h the Arctic fauna
and flora.
The explanations for the differences in degrees of
endemism between the Arctic and Antarctic are mainly
due to the greater age and longer isolation of the Antarc-
tic (Crame 1999) : Arctic benthic floras and faunas arise
from the last 2 million years. The Arctic benthos is more
akin to cold-temperate Atlantic or Pacific forms, it being
more accessible to invasion from these regions . There are
the first reports of planktonic species from outside the
Arctic Basin moving into, or even through, the Arctic;
most notably the diatom Neodenticula seminae is thought
to have migrated from the Pacific across the Arctic basin
and into the North Atlantic as a result of reduced ice cover
(Reid et at. 2007) . It is proposed that this is the first time in
800 000 years that such a migration has taken place, and
naturally the speculation is that such events may happen
with benthic as well as other plankton.
The Antarctic was effectively cut off from the world
ocean 25 million years ago by the formation of the Ant-
arctic Circumpolar Current (ACC), and lack of shallow-sea
linkages is traditionally thought to effectively isolate the
waters surrounding the Antarctic continent from recruit-
ment from elsewhere. However, there are studies, such as
Clarke et at. (2005), that bring into question this long-held
view, and increasingly it does seem that as climate regimes
change, especially in regions such as the western Antarctic
Peninsula, invasion of Antarctic waters by non-polar spe-
cies will be be measured (Barnes and Peck 2008) .
Clearly there are many vectors that can facilitate the
migration of species into the Polar regions, and ballast
water in ships is often cited as a probable mechanism.
However, even the transport of organisms simply on
anthropogenic derived debris, including plastic, has been
found to be a probable source of the introduction of inva-
sive species (Barnes 2002a; Convey et at. 2002 ; Barnes
& Fraser 2003) . Large-scale transport of plastic material
across the Arctic is superbly illustrated by a consignment
of 29 000 plastic, floating bath-toys, including ducks,
frogs, and turtles, lost from a container ship in the North
Pacific in 1992. It was hypothesized that the floating toys
would be transported across the Arctic Ocean into the
North Atlantic, and toys showed up on North Atlantic
coastlines in 2003 and findings are still being reported in
July 2007.
The Antarctic was cut off from ot her waters about 25
million years ago, whereas the Arctic is far younger, hav-
ing been established about 2 million years ago.
12.9 Gigantism in polar waters
One of the characteristics ofmany benthic organism groups
(particularly molluscs and crustaceans) in polar regions is
the fact that they reach much greater sizes than their coun-
terparts in warmer waters. Of course small species are still
present, and not all polar invertebrates are large.
Antarctic sea spiders up to 400 mm across are a hundred
times the size of the common European sea spider. Isopods,
such as Glyptonotus antarcticus, found throughout Antarc-
tica, the Antarctic Peninsula, and sub-Antarctic Islands
from the intertidal to 790 m depth, are up to 20 em in length
and weigh 70 g. In comparison, isopods in other parts of the
world may reach a maximum size of just several centime-

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tres. Other 'giants' include 2 to 4 m tall sponges and ribbon
worms over 3 m long. It is thought that this 'gigan tism' is
brought about by a combination of factors (Fig. 12.17; see
also Chapter 8) .
Low water temperatures certainly slow metabolic rates
to the extent that growth rates are slow enough to enable
them to live longer. Respiration rates are barely measurable
in many of the benthic organisms by standard laboratory
techniques. These result in some polar organisms having
lifespans that are considerably longer than allied species
from warmer waters (Brey 1998) .
It appears that the primary cause leading to variations
between polar organisms and those from warmer climes is
due to differences in the dissolved oxygen content of the
water (Chapelle & Peck 1999, 2004) . The physiological
limit on the size of a particular organism is the amount of
oxygen it can get into its blood, and in oxygen-rich waters
this is largely dependent on the efficiency and length of the
circulation systems supplying oxygen to the tissues. It is also
true that in colderwaters the oxygen demands of tissues are
less, contributing to the possibiliry of large size.
IGigantic' invertebrate species are thought to result
from slow growth rates in low-temperat ure waters and
t he increased dissolved oxygen concentrations in polar
water.
Gigantism in polar waters is not restricted to organisms
with highly developed circulation systems for transfer of
oxygen. Ctenophores, anemones, sponges, copepods, and
pteropods all have representative species that are much
12.10 Birds and mammals
larger than allied species from temperate and tropical
waters . These larger organisms have more tissue volume
to which they must supply oxygen, but relatively less sur-
face area with which to sequester the oxygen. Therefore,
the higher oxygen contents of the low-temperature polar
waters are ideally suited to support these larger species.
12.10 Birds and mammals
The birds and mammals that inhabit polar regions are of
course the most conspicuous organisms ofthe pack ice. and
attract an inordinate amount of attention from the public
and policy-makers interested in the tourism. conservation,
and exploitation of the regions. Historically it was these
organisms that stimulated much of the early enthusiasm
for the exploration of the Arctic and Antarctic.
Evocative as these animals are, an interesting compari-
son is that the total biomass of bacteria (each weighing less
than 1 picogram) in the Southern Ocean is around 3 x 10 7
tonnes, whereas that of whales (each approximately 100
tonnes) is only around Bx 10 6 tonnes. Even a single krill
super-swarm extending over 450 krn- is estimated to have
a biomass of2.1 x 106 tonnes (Fogg 1998).
Sea-ice is a vital requirement as a platform for repro-
duction for many mammal and bird species (reviewed by
Ainley et aI. 2003) . Antarctic seals, such as the leopard
(Hydruga leptonyx), crabeater (Lobodon carcinophagus),
Ross (Ommatophoca rossi), and Weddell (Leptonychotes
weddellii) seals, and emperor penguins (Aptenodytes for-
steri) in the Antarctic give birth to their young on the ice
Figure 12.17 Giant sponges are
a consp icuous component of
Antarctic benthic commun ities.
These grow at extremely slow
rates, and are thought to be
the longest li ving organ isms on
Earth, although their colonial
nature means that not all cells are
ancient. (Photograph: Ju lian Gutt,
Alfred Wegener Institute.)
 Chapter 12 Polar Regions
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in late winter/early spring. Other seal species, such as the
Antarctic fur seal (Arctocephalus gazella) and southern ele-
phant seals (Mirounga leonina), also spend some time in
ice-covered waters. This ensures that young become inde-
pendent by late summer when food is most available. Sea-
ice is also an important platform for birds to renew their
plumage. Penguins and flighted birds, such as snow and
Antarctic petrels, all use icebergs and/or ice floes as plat-
forms to avoid predators while replacing their insulating
feathers, which are vital for surviving the cold, as well as
flight feathers (Fig. 12.18) .
Sea-ice is an important platform for raisi ng young and
hauling o ut for many seal species.
In the Antarctic many of the penguin species (Fig. 12.18)
and seals (Fig. 12.19), such as the crabeater, rely on the vast
stocks of krill as a food source (Smetacek & Nicol 2005) .
Crabeaters feed almost exclusively on krill, and therefore
the links between sea-ice distribution and krill discussed
previously have important implications on the foraging
ecology of the seals. Leopard seals feed on krill, but also
feed on penguins and seal pups. The Ross seal preys on
squid, whereas the Weddell and elephant seals feed on
fish, which in turn feed on the krill, such as the Antarctic
toothfish (Dissosthichus mawsoni) and Antarctic silverfish
(Pleuragramma antarcticum) .
The rich sources of food associated with ice edges and
under ice floes provided major feed ing grounds for birds
and mammals alike.
In the Arctic, the main food-item for many of the birds
and mammals is the Arctic cod (Boreogadus saida), a fish
that feeds on crustaceans, often associated with sea-ice
floes. However, pelagic amphipods, especially of the genus
Parathemisto, also form an important part of the diets of
seals, such as the ringed (Phoca hispida), harp (P. groen-

· - --""-_r-
--
~-
~ ~
-' ~~

....- =-.
--== -
- -.
-- -- -
- -
_

~- -
- - -.- -
~

Figure 12.18 (a) Penguins are a conspicuous feature of Antarctic pack ice, such as these Adelle penguins
(Pygoscelis odeliae), the most numerous of the Antarctic penguins. (b) Emperor penguins (Aptenodytes forsten)
are associated with sea-ice all year round (c) King penguins (Aptenodytes patagonicus) are found on sub-antarctic
isla nds, such as South Georgia (d) The snow petrel (Pagodroma nivea) is an obligate ice species and well camouflaged
against t he ice. (Photographs: David Thomas.)
 12.10 Birds and mammals
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Figure 12.19 (a) Adult Weddell seals (Leptonychotes weddelil) breed further south than any mammal on Earth.
They spend much of the winter in the water; keeping breathing holes open in the overlying ice by grinding the ice
with their teeth . (b) Crabeater seals (Lobodon carcinophagus) are thought to be the most numerous seal species on
Earth (estimates up to 30 million). They feed on krill using interlocking teeth to 'st rain' krill from the water. (c) Adult
leopard seals (Hydruga leptonyx), which , although notorious for eating penguins and seals, actually has krill as a large
part of its diet. (d) Antarctic fur seals (Arctoceptho/us gozel/o) on South Georgia spend time in the marginal ice zones.
(e) Southern elephant seals (/VIiroungo leonino) are known to feed under sea-ice (photographs: David Thomas.)

landica), hooded (Cystophora cristata) , and bearded
(Erignathus barbatus) seals. These amphipods feed on phy-
toplankton, including the dense accumulations of ice algae
on the peripheries of ice floes.
Walruses (Odobenus rosmarus) do not feed on ice-asso-
ciated organisms; however, they also use sea-ice for haul-
ing out. often using their distinctive tusks as ice axes. Their
prey is mainly made up from molluscs. such as bivalves
(Mya truncota) and whelks (Buccinum spp.), and so they
are restricted to hauling out on ice covering shallow ( < 70
m) coastal regions.
Probably the most evocative of all the mammals associ-
ated with sea-ice is the polar bear (Fig. 12.20, Ursus mariti-
mus) . It is difficult to estimate how many polar bears there
are, but estimates place the number at between 20 000 and
40 000 in the whole of the Arctic basin. Within a year many
polar bears may travel many hundreds. if not thousands
of kilometres. These large roaming distances are of course
extended (easily over 100 000 km-) because the bears are
travelling on a moving platform of ice that is blown by wind
and carried on ocean currents. Although much of these
distances are completed on top of the ice, because polar
bears are such strong swimmers, they can swim distances
in excess of 100 km at a time . This results in polar bears
sometimes being observed several hundreds of kilometres
offshore, probably because the ice floes they were traveling
on had melted from underneath them (Born et aI. 1997;
Wiig et aI. 2003) .
The ice is a vital platform for them to forage on their
prey, which comprises seals, walruses, and whales (Stirling
1998). Although polar bears do spend time on land, it is a
true marine mammal, depending on the sea- and pack ice
 Chapter 12 Polar Regions
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
for its existence, and it is the largest of the non-aquatic car-
nivores. Many polar bears preferto remain within the pack
ice all year long (if possible), since the ice floes provide a
platform from which the bears can catch seals, which are
their main prey.
The southern limits of polar bears are basically governed
by the southernmost extent of sea-ice.
Polar bears are found throughout the ice-covered waters
of the Arctic Ocean. The greatest majority of bears roam
near pack ice that is thinner or breaks open on a regular
basis. Generally, bears avoid heavily ridged, rough sea-ice
and thick multi-year ice, mostly because the densities of
seals are low in these ice types. The southern limits of polar
bears are basically governed by the southernmost extent of
sea-ice, and a few have been reported as far north as close
to the north pole, although generally it is thought that very
few stray further than 800 N, since the ice is generally thick
multi-year ice-floes.
Polar bears are a good example of the profound and
complicated effects of decreasing Arctic sea-ice (Current
Focus) . The predicted decreases in summer sea-ice will
result in polar bears migrating further north to forage for
food than at present. These effects have been highlighted
by many researchers (Derocher et al. 2004; Stirling and
Parkinson 2006), and the combined effects of decreases in
sea-ice thickness and the progressively early sea-ice break-
up are linked to decreasing size in polar bear populations
in the Western Hudson Bay and Baffin Bay. A consequence
of this is that the surviving bears have to search for alter-
native food sources close to towns and communities. This
is because earlier break-up of sea-ice is forcing bears on
to land earlier in the year, thereby preventing them from
feeding on seals and building up sufficient fat stores with
which to survive before the autumn/winter formation
of sea-ice when they can return to the sea-ice to hunt for
Figure 12.20 Polar bear (Ursus
maritimus) walking on sea-ice
(photograph: courtesy of Finlo
Cottier).
seals. As the bear populations decline, problem interac-
tions between bears and humans will continue to increase,
as the bears seek alternative food sources. Polar bears
usually return to the same area for overwintering and can
utilize the same maternity den several times. However,
warming of some permafrost regions has already resulted
in such dens collapsing, and making the suitabiliry of dens
more precarious than has been the case up to now (cf.
Lunn et al. 2004) .
In both the Arctic and Antarctic, baleen whales are
able to forage under ice only as long as they can hold their
breath. These are open-water species and generally fol-
low the seasonal retreat of ice edges, subsequently leaving
the polar regions before the seas freeze over in autumn.
Therefore, although blue (Balaenoptera musculus), fin (B.
physalus), and right (B. glacialis) whales all migrate to
the Southern Ocean to feed on zooplankton such as krill,
minke whales (B. acutorostrata) are the only cetaceans to
occur deep in the Antarctic pack ice. Some populations
of minke whales even live in the pack ice all year round.
These 'small' whales that feed on krill use a hardened ros-
trum on top of their heads to break the ice to enable them
to breathe.
Few whales are capable of living deep within the pack
ice, and most species that frequent polar waters feed in
open waters or in the relatively diffuse ice-edge regions.
In the Arctic, beluga (Delphinapterw; leucas), bowheads
(Balaena mysticelUS), and narwhals (Monodon rnonocerus)
also break sea-ice with their backs to form breathing holes,
and their lack of dorsal fin is considered an adaptation to
having to break ice with their backs. However, in general,
cetaceans in the pack ice of both hemispheres tend to be
mostly found in leads and open-water areas towards the
periphery of pack ice . Bowheads and minke whales are the
only whales to be found truly within the Arctic pack ice.

Open water is vital for breathing mammals, and seal spe-
cies living deep within the pack ice expend much energy
in keeping breathing holes open.
The toothed sper m (Physeter macroceph alus) and killer
whales (Orcinus orca) are found in sea-ice regions. The
former largely feed on squid, consuming up to 3% of their
body we ight per day. Killer whales predate on seal, birds,
or cetaceans in the pack ice, but they also feed on fish,
including the large Antarctic toothfish. Certainly it seems
that some whales, including bowheads, narwhals, minke,
and belugas, may shelter in the pack ice in an effort to
avoid groups of killer whales.
For all the mammals living in pack ice, breathing
holes or areas of open water are vital for survival. This
is the reason why most whales are restricted to the dif-
fu se marginal ice-zones, or areas of open wate r wit hin
Box 12.7: Ozone holes and the poles
Seasonal depletion of ozone in the troposphere over both
the Arctic and Antarctica and increased ultraviolet radiation
reaching the ocean's surface are well-reported phenomena
(Uchino et at. 19 9 9 ) . The consequences of this have been
the source of much speculation and include the possibility
of harmful effects on organisms living in surface waters of
the polar oceans (reviewed by Brierley & Thomas 2002).
In te rms of the ecology of sea-ice and ice-associated
waters, the ecosystem components that may suffer the
largest influence of an increase in UV radiation are th e
blooms that occu r in the stabilized waters of the marginal
ice-zones during spring and summer. The melt-water-sta-
bilized shallow mixed depths may be 20 m or less, and
UVb can penetrate to dep ths in excess of 50 m. Sea-ice
itself, especially if covered by snow, is a particularly good
barrier to UV light, and so sea-ice organisms and those
living under ice cover are unlikely to be severely damaged
by UV effects.
In Antarctic waters, links between UV rad iation increases
and reduced viability of natural bacterial assemblages have
been shown, although bacterioplankton is often not very
sensitive to increased UV radiat ion, due in part to rap id
repai r of UV damage (Wi nte r et al. 200 1). Relatively swift
population changes in bacterial species' co mposition and
acclimation to hig h UV radiation may also have con trib-
uted to low UV induced inhi bition of bacte rioplankto n.
After strong UV exposu re there can actually be increased
bacterial production resulting fro m increased phytoplankton
mortality and inactivation of viruses that reduce marine
bacteria. There are reports of increased concentrations of
bacterial grazers, ciliates, hete rotrophic nanoflagellates,
12.10 Birds and mammals
the pack. Antarctic Weddell seals maintain their breath-
ing holes by gnawing away the ice at the periphery of
the hole w it h their teeth. Older Weddell seals h ave worn
teeth as a result of blowhole excavation, and starvation
following broken teeth is eviden tly a common cause of
mortality. Arctic ringed seals use heavy claws on their
fore-flippers to maintain breathing holes in ice up to
2 m thick.
There are several flighted birds that are highly adapted
to an almost exclusive life in the pack ice: Ross's and ivory
gulls (Pagophila eburnean and Rhodostethia rosea, respec-
tively) in the Arctic and the snow petrel (Pagodroma nivea)
in the Antarctic. These are all white in colour, an ad apta-
tion allowing them to approach their prey more closely as
we ll as avoiding predators, as long as their background
is white.
and choanoflagellates followi ng high UV radiation (David-
son & van der Heijden 2000).
It has been proposed that one of the environmental fac-
tors influencing krill abundance in the Antarctic is increased
UV damage due to ozone depletion, followi ng evidence that
Euphausia superba may be more susceptible to damage
than other Antarctic zoo plankton (Jarman et al. 1999). In
the pelagic zone, krill swarms are most often found well
below the sea surface during daylight and are unlikely to be
exposed to high UV levels. Interestingly, it has recently been
shown that vertical migration by zooplankton is influenced
by UV: deeper migrations occur in the presence of high
levels of UVb. Therefore, the depth and duration of ver tical
migrations may be influenced by ozone-related increases in
UV, in tu rn impacting predato rs that feed on these species.
Image of a stained concentrated sample of sea-Ice
bacteria viewed under the microscope. The fluorescent
stain makes it easy to count the numerous bacteria. The
large structures are sea-ice diatoms (photograph: S6nnke
Grossmann).
 Chapter 12 Polar Regions
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Seasonal ozone holes result in increased harmful doses UV radiation may ind uce chances in the vertical migra-
of UV radiation reaching the surface of polar oceans. tion patterns of zooplankton .

CURRENT FOCUS: Decreasing sea-ice

Some of the most dramatic large-scale changes (and
most widely repo rted) to be recorded in any marine sys-
tem in the past 30 years are the changes in perennial
ice-cover in the Arctic (i.e. the yearly mini mum ice cover) ,
which has been reported as decreasing at a rate of about
9.2% per decade (Comiso 2002; Stroeve et al. 2007).
There is also a red uct ion in the yearly maximum ice extent,
which is decreasi ng at a rate of 2.8% per decade. The
consequence is an annual mean decrease of around 4.3%
per decade.
However, it is not only the extent that is reducing, but
20 ,----------"F"~~~..,
- Yearly mQlimum
18 - Yearly mean
- Yearly minimum
16
Per rent (hange I Decade:- 2.826%
E
14 - -
- -- - - --
~1 2
- ~ ....-..~__~
• • .,:1 - ....
=
!e;:.':;
": "t.;:(h;:;,;::
__ c
"g;:,
~c
e I Decade:-4.307%
__ .::'--., .. ~
~ 10
8 Per rent (hange I Decade:- 9.048%
6 - - ~
4
, , , , , , Mean sp ring sea-ice thickness in the Arctic for (a) 1982-
1980 1985 1990 1995 2000 2005 2010
87, (b) 1988-95, (c) 1996-2000, and (d) 2001-D7.
Per cent change per decade in yearly concent rat ions of From Maslanik et al. (2007).
Arctic sea-ice area. Data collected by satell it e o bserva-
tions. These data are routinely updated on http:/ /arctic- These sorts of major findings have led several research-
roos.org / . (Source: Nansen Environmental and Remote ers to conclude that there will be no perennial sea-ice
Sensing Centre, Norway, h!1p:llarctic-roos.org) in the Arctic summers after the 2050s (Serreze et al.
2007). This would mean that, although sea-ice would
form in wi nter, it would all melt in the followi ng spring /
also the thickness of the ice: Haas (2004) and Haas et summer and there would be little thick ice, which is char-
al. (2008) reported on a series of surveys made between acteristic of the Arctic (Maslanik et al. 2007). In fact, the
19 91 and 2007, between Svalbard and the North Pole, seasonal dynamics of ice fo rmation, consolidat ion, and
where sea-ice thickness was routinely measured. Dur- melt would be similar to that we know of fo r the Southern
ing the whole period there was a 22.5 % reduct ion in Ocean pack ice today.
the average sea-ice thickness fro m 3.1 1 m to 2.41 m. Schiermeier (2007) gives a very thought-provoking
Rothrock and Zhang (20 0 5) also reported a greater than social-economic synopsis of how the Arctic region may
2 m decrease in sea-ice thickness in the central Arctic change over the next 20 years as a result of warming
between the 19605 and 19 9 0 5. Maslanik et al. (2007) climate. Among the examples of possible developments
have summarized these thickness changes showi ng the following standout:
how the oldest ice types have essentially disappeared,
• By 20 12, the polar bear may be li sted as a th reatened
and 58% of the multi-year ice now consists of relat ively
species.
young 2- and 3-year-old ice, compared to 35% in the
mid-1980s. • By 20 17, vecto r-borne diseases become more wide-
spread among the Inuit and mosquitoes migrate to

the Arctic, and the Arctic cod could be replaced by
temperat e fish.
• By 2027, the Arctic Ocean may remain ice-free in Sep-
tember and oil tankers and freight ships may be able
to sail the Northeast passage.
The tren ds in the Antarctic are not so clear-cut, an d
there are some years that have significantly more ic e,
and others w ith signi ficantly less ice. In fact there is
evidence of a slight decadal increase in ic e cover in
the Antarctic (Parkinson 2004). There is an apparent
paradox in the effects o f global climate change on
both polar regio ns, which naturally is the subject o f
muc h d iscussion to scientists trying to mo del future
climat e dynamics (Walsh 2009).
The Antarctic Peninsula region is one of the regions of
the world that is warming the fastest, where average air
temperatures have risen by 2°C per decade (Vaughan
et al. 200 1, 2003). This warmi ng has been linked to
increased glacial melt and retreat on the Peninsula (Cook
et al. 2005), which has received considerable attention
by a general non-scientist audience. Correspondi ng with
this rapid warming of the western peninsula, there are
significant decreases of 8% per decade of sea-ice extent
in the Belli ngshausen and Amundsen Seas. However,
this is balanced by a correspo ndi ng increase of 7% per
decade in the Ross Sea (Comiso 20 10). These two sec-
tors are adjacent to each other and it would appear that
there is a movement of ice from the Amundsen Sea into
the Ross Sea, as well as increased ice production in the
latter.
It is very di ffi c ult to guess the effects that such
changes in ice cover may make to polar seas. It is
cl ear that ocean-wide pred ictions w ill mask cons ider-
able, smaller, regi o nal-scale differences (d. Leu et al.
20 1 1). Arrigo et al. (2008a) have calculated thatthe
reduction in sea- ice cover has res ulted in an increase
in the annual primary production of between 27 and
35 Tg carbon year" between 2003 and 2007. They
hypothesize that, should the trends on Arctic sea-
ic e loss continue, there may be a 3-fold inc rease
in prod uctivity in the Arctic above those measured
between 19 9 8 and 2002. To put these fig ures into
context, estimates of annual primary production by
pelagic phytoplankton in the Arctic range from 300 Tg
12.10 Birds and mammals
carbo n year ' to 500 Tg carbon year" (Pabi et al. 2008).
In Antarctic waters (south of 60°5), phytoplankton pri-
mary production is estimated to have averaged 19 49
+70. 1 Tg C year" between 1997 and 2006 (Arrigo et
al. 2008b).
In the western side of the Antarctic Peninsula, several
long-term monitoring stations have been established
(Clarke et al. 2008; Montes- Hugo et al. 2009) and, as
described in Chapter 2, they are proving invaluable for
recording major ecological changes. Montes-Hugo et al.
(2009) report how the region is undergoing transition
from a cold-d ry polar regime to a warm-humid sub-Ant-
arctic climate. They notice that the changes have resulted
in a shift in coastal primary production over the past 30
years, with decreases occurring in the north of the region
and increases in southerly stations of thei r study area.
These are clearly linked to the changing sea-ice extent
in the region and the altered seasonality of key environ-
mental signals th is brings about (Clarke et al. 2007).
Naturally, there are some organ isms, such as the
krill in the Southern Ocean and polar cod in the Arct ic,
whose recrui tment is directly linked to sea-ice extent.
It is likely t hat kri ll spawning an d rec ruitm ent wi ll be
significantly red uced if sea-ice extent and/or season is
furth er re duced (Atkinson et al. 2004), and the sub-
sequent effects on birds, seals, and whales is subject
to much speculation (Nicol et al. 2008). Thi nner sea-
ice floes may result in increased primary production
w ithin the ice an d g reate r inocula of seeding o rgan-
is ms into th e water on ice m elt. Naturally, increased
food sources in the ic e w ill possibly enhance zoo-
plankton stocks in under- ic e waters. It is also p os-
sible that extended periods o f primary production
may result in the summer open-waters, especially
in the Southern Ocean where inorganic nutrients are
available in excess. Decreases in ice extent have even
been proposed to be beneficial fo r increasing emperor
penguin hatching success, since the breeding colon ies
w ill be closer to feed ing g rounds.
In the Arctic, increased river run-off and altered organic
matter and inorganic nutrient loading into the coastal
wa ters where ice forms will have numerous effects on
the biology of these waters. Naturally there will also be
an increase in pollutants bei ng carried into the coastal
wa ters with increased riverine flow.
Chapter 12 Polar Regions

Chapter Summary
• Polar regions are characterized by highly seasonal changes in day-length and temperatures. Althoug h
extreme low temperatures prevail, this is not the main limiting factor to life in polar regions.
• Although the effects of climate change are maybe more pronounced in the Arctic at present, changing
climate will have profound implications for ecosystems in both polar regions.
• The annual formation , consolidation, and subsequent melt of sea-ice is the fundamental process
that determines the unique ecology of the Arctic and Antarctic oceans.
• A significant primary production takes place in the ice itself, providing a vital source of food at times
of the year when food in the water column is sparse.
• The stabilization of the water column by melting ice can induce ice-edge algal blooms that induce high
g razing activity.
• Benthic assemblages in polar regions are dominated by suspension feeders, which not only utilize
the highly seasonal pulses of food from waters above, but also from resuspended and advected
sed iments.
• Sea-ice scraping the intertidal and the scraping of the seafloor by icebergs have considerable destructive
effects, down to below 300 m, on polar benthic assemblages.
• High dissolved oxygen concentrations, low temperatures, and longevity in polar waters enhances the
phenomenon of 'gigantism'.
• Many bird and mammal migrants frequent polar waters in summer months. However, only a few obli-
gate species live throughout the year deep in the pack ice.
• Seasonally high doses of UV rad iation have m ixed effects on polar ecosystems, although damaging
effects may be far less than often perceived.

Further Reading
For general texts on t he b iology of polar regions cons ult Thomas (2004) , McGonigal and Woodworth
(200 1) , Thomas et al. (200B) , Sale (200B) , Shirihai (2002) , St irling ( 199B), and Wood in and Marquiss
( 1997) . For more informat ion on the bio logy and physics of sea ice, consult Brierley and Thomas (2002) ,
Knox (1994) , Hempel and Hempel (2009) , Thomas and Dieckmann (20 10) , and Eicken et al. (2010) . Arntz
et al. (1994) review the zoobenthic processes. Mastro and Wu (2004) present an inspiring view of Antarctic
benthos, ice, and mammals. Smetacek and Nicol (2005) describe vividly t he potential effects of g lobal
cl imate change on plankton through to whales living in polar oceans.
• Arntz, W. E., Brey, T., & Gallardo, V. A. 19 9 4 . Antarctic zoobenthos. Oceanography and Marine Biology.
an Annual Review: 32: 241 -304.
• Brierley, A. S. & Thomas, D. N. 2002. Ecology of Southern Ocean pack-ice. Advances in Marine Biology:
43: 171 - 2 76 .
• Eicken, H. R. , Grad inger, M., Salganek, K. , Shirasawa, D. K. , Perovich, M., & Lepparanta, M. (eds) . 20 10.
Field Techniques for Sea Ice Research. University of Alaska Press.
• Hempel, G. & Hempel, I. 2009. Biological Studies in Polar Oceans- Exploration of Ule in Icy waters. ","rtschaft-
verlag NW, Bremerhaven, Germany.
• Knox, G. A. 19 9 4 . The Biology of the Southern Ocean. Cambridge University Press, Cambridge.
• Mastro, J. & Wu, N. 2004. Under Antarctic Ice. University of Californ ia Press.
• McGonigal, D. & Woodworth, L 200 1. The Complete Story Antarctica. Frances Lincoln, London.
• Sale, R. (200B) . The Arctic-The Complete Story. Francis Lincoln Ltd., London.
• Shirihai, H. (2002) . A Complete Guide to Antarctic Wildlile , Princeton University Press, New Jersey, USA.
• Stirl ing, I. (199B) . Polar Bears. The University of Michigan Press, An n Arbor, Michigan , USA.
 Further Reading

• Smetacek, V. & Nicol S, 2005, Polar ocean ecosystems in a changing world, Nature: 437: 362-368,
• Thomas, D. N, 2004, Frozen Oceans-The ffoating World of Pack-ice, Natural History Museum, London,
• Thomas, D, N, & Dieckmann, G, 5, (eds) , 20 10, Sea Ice (2nd edn) . Wiley-Blackwell Publishing, Oxford,
• Thomas, D, N" Fogg, G, E" Convey. P., Fritsen, C , Gilli, J-M " Gradinger, Ro , Laybourn-Parry, J., Reid K" &
Walton, D, H, 2008, Biology of Polar Regions, Oxford University Press,
• Wood in,S, J. & Marquiss, M, 199 7, Ecology of Arctic Environments, Blackwell Science, Oxford,
This page intentionally left blank
This page intentionally left blank
Fisheries
Chapter Summary
Fishi ng ought to be the perfect example of an industry
based on a renewable resource, since fishers take har-
vests they need not sow. Fisheries are a key contri butor to
global food security and econo mic activity, but fisheries are
often subsidized, w asteful, cause excessive environmental
damage, and ignite confli cts between otherwise friend ly
nations. Scientific understanding of fish populations and
their management is good, but much of this understanding
is not translated into effective management, and relatively
13.1 Introduction
Fishing provides food, income, and employment for mil-
lions of people, but fishing is also one of the most wide-
spread human activities in the marine environment and can
have unsustainable env ironmental costs that threaten rare
species and m arine ecosystems. Fisheries, of course , do not
o nly target fish. The term is loosely used to refer to humans
capturing many w ild m arine species, ranging from algae to
invertebrates, fish, and w hales.
Fisheries are a vital source of food , income, and jobs for
millions of people especially in the developing world .
In thi s chapter we describe the scale and impact of fisher-
ies, the biological processes that support fish production,
how sustainable le vels of catch can be predicted, and how
fisheries and marine ecosystems can be managed to meet
a range of objectives. Our emphasis is on fisheries that tar-
get fish and invertebrates, as these groups account for the
majority of global landings.
few fisheries realize their potential benefits to fish ers and
society. In past decades, the main objective of fishery man-
agement was to maxi mize catches without compromising
future catches. For biological, soci al, and econom ic reasons,
th is obj ective was rare ly met. Some fi sheries collapsed and
others th reatened species and habitats of conservati on
concern that were not their intended targets. Today, fish ery
managers still face great challenges as they start to take
account of the impacts of fishing on the ecosystem and to
integ rate conservation concerns into management plans.
13.2 Global fisheries
Global fish landings rose steadily from 1950 to the early
1990s, but have slightly decreased since then and now
hover around 80 million tonnes (Fig. 13.1), and their first
sale value is approximately $U550 billion. The cessation of
the long-term increase in global fishery landings reflects
the overfis hing of many species, and landings are likely to
remain stable or decline in future . Fisheries contribute sig-
nificantly to the global supply of protein, particularly in the
world's poorer countries , and sustainable management of
fisheries brings benefits to society and environment alike .
Global fish-catches are dominated by remarkably few
species. Five species of fish, out of more than 15 000 found
in the sea, usually account for more than 15% o f annual
landings, although thi s does fluctuate as a consequence of
the variable dynamics of these species and the effects of
fishing and climate . These species are the Peruvian anchovy
(Engraulis r ingens) , the Alaskan pollock (Th eragra chalco-
gramma ) , the Chilean jack mackerel (Tra chur us murhyi) ,
the Atlantic herring (Clupea harengus) , and the chub
mackerel (Sco mber j aponicus ) . All these fishes are found
 Chapter 13 Fisheries
• • • • • • • • •• • • •• • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • •• • •• • • • • • •• • • • • • • • • • • • • • ••••••• • • •• • • • • • • •• • •

140 , -- - - - - - - - - - - - - - -----,
in upwellings or on continental shelves. areas where levels
120
of primary production are very high (Chapters 2, 7, and
~ 1110
8) . Indeed, the majority of global landings come from pro- c
.2 BO v
ductive shelf ecosystems and upwellings, and not from the S
=60
;;;
open ocean, where production is generally low (Fig. 13.2) . World excluding Chino
40
Not all fisheries' catches are represented in the statis-
2O -L-- /'
tics available, owing to catches that are taken illegally or
o +-~-~~-~~~-~~-~~___\
not reported (Box 13.1) . A recent estimate of the scale of 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005
illegal and unreported fishing suggests annual catches of Year
between 11 and 26 million tonnes valued at US$10 bn and
US$23.5 bn (Agnew et aI. 2009) . Illegal and unreported Figure 13.1 International landings of marine fishes and
catches were higher in developing countries with weak gov- invertebrates by all countries excluding China. Data from
ernance systems. FAD (www.fao.org).

Global landings' statistics are updated annually at www. people migrated across the Pacific thanks to the ubiquity
fao.org. For further information on all the fished species of fishes and coconuts. As seafaring and navigational skills
listed in this chapter see www.fishbase.org. improved, so vast offshore fish resources were discovered.
By the early 1500s, fishers from France and Portugal were
regularly crossing the Atlantic Ocean to fish for cod (Gadw;
morhua) off the coast of Canada (Box 13.2) . Many wars
13.2.1 A brief history of fisheries'
were fought over fish, and Kurlansky's fascinating book
exploitation Cod: a Biography ofthe Fish that Changed the World (1997)
The sea has been fished since ancient times, and there tells the story of the burgeoning cod fishery and the inter-
are many references to fisheries in Greek, Egyptian. and national struggle to control it.
Roman texts . In many small, island nations, fish have been
a vital source of protein, and Polynesian and Melanesian People have caught fish since prehistoric times, and
many wars have been fought over fish.

o
• .
Ln(Catch) • •
~ >8 ,
0 >6
= >4
==
>1
>2
•
=
=
=
<0
< -1
< -3
lSI < -4
< -5
- < -6

Figure 13.2 Spatial distribution of marine fish landings from 1950 to 2004, expressed as natural logarithm of the
average reported catch (in metric ton km- 2 year- '). From Worm et al. (2009).

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Box 13.1: Catches and landings
Fish and other animals that fishers bring ashore are
often called catches or landings. Although these
terms are often used interchangeably, this is not cor-
rect. Catches describe the fish caught by the fish-
ers but, as well as the fish they are tryi ng to catch,
catches contain a range of other species, some valu-
able and some not; these are known as by-catches.
By-catches have caused social and political contro-
versy because they can include species such as dol-
phins, seabirds, or turtles.
Valuable by-catch species will be kept, but the
remainder of the by-catch is usually discarded at sea
because it contains animals smaller than legal size-
limits or not suitable for selling and eating. The dis-
carded animals are known as discards. Since many
discards will have died or been wounded during cap-
t ure, they do not survive when returned to the sea.
Landings describe fish that are brought ashore, and
are thus a measure of catches minus discards. Since
discards account for around 27% of the catches in
global fisheries, landings data, such as those pub-
lished by the FAG, greatly underestimate the num-
bers of fish and other animals killed by fishing.
Source: Alverson et al. (1994).
While fishes, especially in estuarine and coastal areas,
were depleted by pre -industrial fisheries, fishing re ally
began to affect fish stocks and the marine ecosystem on
a global scale following the Industrial Revolution. With
industrialization, the power a nd range of fishing vessels
increased rapidly, as did the ca pacity to catch and store
fish. Methods for the large-scale canning and freezing of
fish products were developed, and the new intensive farm-
ing industry needed large volumes of cheap fish-meal as
anim al feed. Countries suc h as the former USSR, J apan,
Spain, Korea, and Poland h ad m assive government sub-
sidized fleets that ranged the world's oceans in search of
fish. Until the 1970s, there was little control of these fleets,
since most of the wo rld's oceans were not under national
control. However, in the early and mid-1970s, increasing
competition for fish led m any countries to claim n ational
jurisdiction up to 200 miles from their coast. Since 90%
of world catches were taken within 200 miles of the coast,
these claims brought 90% of fisheries under n ational con-
trol. The demise of the subsidized high seas fleets followed,
but most of the fisheries under national control were st ill
poorly m anaged and collapsed in the subsequent decades
(Cushing 1988; Burke 1994).
13.2 Global fisheries
Box 13.2: Collapse of a fishery: the
Canadian cod
Cod have been fished off the coast of Newfoundland
for 500 years, but in 19 9 2 , after years of intensive
fishi ng, cod were fished to commercial extinction and
the Canadian Government was forced to close the
fishery. The collapse of the cod is a classic example
of too many fishers chasi ng too few fish, and as the
fishery became increasingly mechanized and tech ni-
cally efficient, so the fishing capacity of the fleets
far exceeded the biological productivity of the cod
stock.
From the fifteenth to the nineteenth centuries, cod
were mainly caught with hook and line, and were so
abundant that fishers thought their numbers would
not be affected by fishi ng. However, technological
developments, such as the introduction of large trawl
nets, powered winches to haul the nets back to the
fishi ng vessels, freezer traw lers that could store large
catches, and sonar devices to locate shoals of cod,
vastly increased fishi ng capacity and the cod became
threatened. Annual cod landings peaked at around
810 000 to nnes in 19 6 8 , when many large Euro-
pean freezer trawlers regula rly travelled across the
Atlantic to fish. By 1977, when Canada took control
of the fishing grounds wi thin 200 miles of her coast,
and effectively closed the European fishery, landings
had already fallen to 20% of their maximum.
Even with the cod stock under national control,
social and political pressures still made it very difficult
to reduce fishing effort, and the demise of the cod
continued. The abundance of adult Canadian cod fell
from an estimated 1.6 million tonnes in 1962 to 22
000 tonnes in 1992, when the fishery was finally
closed. The closure was a disaster for the Canadian
fishi ng industry and many fishers were left strug-
gling to survive on welfare payments, while service
and processi ng industries, that once thrived in many
coastal tow ns, had to shut or relocate. Ten years
later, the cod stock has shown little sign of recovery
and many boats now fish for other species, such as
shrimp.
Source: Hutchings & Myers (1994).
13.2.2 Overfishing and the need for
management
There are m any detailed reasons why individual fisheries
are overfis hed but, in basic terms, overfis hing is a conse-
quence of too many fishers and vessels chas ing too few fish.
 Chapter 13 Fisheries

Why does this happen? Studies of many fisheries around
the world have shown that when a potential fishery is dis-
covered, new fishers start to fish as fast as they can . Indeed,
on an individual basis, the faster fishers fish, the more
money they will make. Other fishers who find out about
the new fishery will also join the race to fish. Soon, there
will be too many fishers chasing too few fish, the stock will
be depleted and catch rates and profits will fall because the
rates of fishing exceed the biological capacity for replen-
ishment.
Good fishery management seeks to ensure that catch
rates never exceed the rates of biological replenishment
of fish stocks.
The range of phases that a fishery can go through can be
described as fishery development, full exploitation, over-
exploitation, collapse, and recovery. During each of these
phases, there are clear trends in fish abundance, fleet size,
catch, and profit (Fig. 13.3) . Fishery managers usually
work to support the objective that catch rates do not exceed
potential rates of replenishment, and that the sustainabil-
ity of the ecosystem is not compromised. 'TYPically, this is
consistent with keeping catch rates at levels below those
associated with full exploitation.
The objectives of preventing over-exploitation and
ensuring that catches and profits are sustainable in the
long term have proved hard to achieve in practice. Thus in
2007, 14% of the worlds's assessed stocks were collapsed,
where collapse was defined as stock biomass less than 10%
of unexploited biomass. This compares with reductions in
unexploited biomass of 40-60% that are expected in sus-
tainable fisheries. The global figure of 14% collapsed hides
significant regional variation in the state of stocks and per-
a
~
formance of fisheries management. For example, in east-
ern Canada. 60% of assessed stocks were collapsed in 2007
(Worm et al. 2009) .
Ensuring that catches and profits are sustainable are not
the only goals offishery management. Today, managers are
increasingly seeking to implement ecosystem-based man-
agement, where management decisions take account of
conservation and ecosystem concerns, such as the wider
effects of fishing on biodiversity, rare species. birds. and
mammals. Later in this chapter we will look in detail at
the effects of fishing on the environment and what can be
done to mitigate these effects while maintaining fishery
production.
Despite the potential benefits of fisheries to society, the
effects of fishing on ecosystems and rare species are a
growmg concern.
13.2.3 Fishery science
Fishery science was first treated as a scientific discipline in
the late-1850s, when the Norwegian Government hired sci-
entists to find out why catches of cod fluctuated from year
to year. Cod had been caught in northern Norway, and then
preserved by salting and drying for many centuries. The
money made from exporting dried cod was used to import
other foods and to pay traders and bank loans in southern
Norway. However. cod were not always a reliable source
of income and, when the cod fishery failed, the people
of northern Norway would start to default on their bank
loans. For the Norwegian government. fluctuations in the
cod fishery caused economic and political hardship, and so
the government hired scientists to explain why the catches
fluctuated and what might be done about it.

.-
-~
~c
~
. •c
c
<,
r-, Fishery science began in Norway during the nineteenth
century, because the Government wanted to know why

.-.
"S_

--
::c....!:!:!
~~
e :;:;
/
cod catches fluctuated .
c->
z-
----- By 1900, most of the developed economies were employ-
...--•
c V <, ing fishery scientists. These scientists described the biology
and migrations of fishes and had shown that abundance
~

-, fluctuated from year to year because the numbers of young

fish entering the fishery were very variable . Moreover,
:§ 0 - -- - - - -- - - - -- ------
"\-- -- - ..-"
it was clear that the abundance of a year-class of young
'" Fully Over- fish was established in the first few months of life, and
Developing Fishery Fi~hery
Unexploited exploited exploited rol1opse retovery depended on conditions in the ocean environment. By the
~~hery
~shery fishery
1960s, fisheries science was an advanced field and scien-
tists had developed models that predicted fishery landings
Figure 13.3 Patterns of exp loitation in an unregulated and profits when fish were killed at different rates. These
fishery. Ideally, fisheries are regulated to hold them in models allowed sustainable rates of fishing to be estimated,
the developing or fully exploited phase. After Hilborn & but the advice that scientists gave was rarely translated into
Walters (1992). effective management (Smith 1994).
 13.4 Fished species and their fisheries
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
By the 19605, fishery scientists could predict potential
fish catches and profits when fis h were killed at different
rates .
13.3 Fish production
While fished species are some of the most conspicuous and
intensively studied inhabitants of marine ecosystems, they
account for a fraction of total production. Fish, at least by
the time they are sufficiently large to be caught, usually feed
relatively close to the top of long food chains. As we saw in
Chapters 4 and 7, these food chains are quite inefficient,
and only a fraction ofpreyproduetion is converted to preda-
tor production at each step in the chain . This means that
the production offished species per unit of primaryproduc-
tion falls as the length of food chains increases, and that
higher fisheries' yields can be taken from species lower in
the food chains, like plankton-feeding sardine or anchovy,
rather than from their predators, such as hake. The effects
ofinefficiency in the food chains are such that, while global
marine primary production is thought to range from 30 to
60 X 109 tonnes y-l, fish production is unlikely to exceed 2
x 10 8 tonnes.
Fish account for a fraction of total prod uction in the sea
because the food chains leading from primary produc-
tion to fish productio n are quite inefficient.
Globally, phytoplankton account for almost 90% of pri-
mary production and thus support most fish production.
Ecosystems with higher primary production invariably
support higher fish production, and so fish production is
highest on the continental shelves and in upwellings (Fig.
13.2). More than 20% of primary production is probably
required to sustain fisheries on the continental shelves and
in upwellings, and thus fishing must have a major impact
on patterns of energy flow in marine ecosystems (Pauly &
Christensen 1995) .
Ecosystems where primary production is higher will sup-
port higher fish prod uction.
13.4 Fished species and their
fisheries
Knowledge of the life histories and distribution of fished
species is key to understanding how they are affected by
fishing and the environment. Thus large species with slow
growth and late maturity tolerate much lower rates offish-
ing than smaller and faster growing species, and the abun-
dance of species with short life cycles and a small number
of age-classes in the population will fluctuate more from
year to year.
Large and slow-growing species are the most vulnerable
to fishing.
Most fish and shellfish species form a number of stocks
across their geographical range. These stocks have char-
acteristic life-stories and migrations, and will therefore
respond differently to fishing. Stocks of the same species
can interbreed, but mixing between them is low, and so
they respond more or less independently to fishing. This
means that stocks are treated as management units in most
fisheries.
Fish stocks are populations of fish that have character-
istic life histories and can be treated as a management
unit because they respond more or less independently to
fishing. Fish stocks are treated as the primary manage-
ment units in most fisheries.
Fish stocks do not respect national or administrative
boundaries, and they migrate on many scales, from local to
oceanic (Chapter 8) . Migrations allow stocks to remain in
the best possible conditions for feeding, growth, or repro-
duction. Since migrating fish often cross the boundaries
of nations, international management areas, and marine
reserves, catches of fish in one area can affect catches of
fish in another. This can lead to international competition
for 'shared stocks' and, for this reason, many fisheries are
assessed and managed by groups of nations. For example,
the Inter-American Tropical Tuna Commission (lATIC) was
founded in 1949 to manage tuna fisheries in the tropical
Pacific Ocean and includes member countries from North,
Central, and South America, France, Japan, and Vanuatu.
Because stocks may migrate between the national waters
of many countries, many fisheries are jointly managed by
several countries.
Most fished species have pelagic larvae and will grow in
mass by 5 to 6 orders of magnitude in the course of their
2 to 20-year life-cycles (Fig. 13.4). Most fished species are
also very fecund, but the majority of eggs and larvae will
perish, from starvation or predation, in the first few weeks
oflife. Thus, although many fished species have fecundities
of103to 106 , the mean number ofadults produced per adult
per year usually falls in the range 1 to 7. The extentoflarval
mortality is shown, for example, by the West African rock
lobster Uasus islandii) . For every 1 million eggs laid, only
one, on average, survives to adulthood.
 Chapter 13 Fisheries

Figure 13.4 The life

cycle of the sea bass
(D/centrorchus lobrox).

2adult bass
Weight = 3000 g
Length = 65 em
Age = 12 years

1million bass eggs

Weight = 0.0005 g
180 Juvenile bess
Diameter = 1.0 mm
Weight = 5g
Age = 7days
Length = 60 mm
Age = 180 days

1400 bass larvae

Weight = 0.008 g
Length = 10 mm
Age = 49 days

13.5 Fish population biology
Fish abundance. like that of other species, fluctuates in
space and time.Abundance fluctuations are driven by phys-
ical and biological processes that affect the production and
survival of eggs and larvae, and by growth and mortaliry
during the juvenile and adult phases. When scientists dis-
covered that they could age fish by counting growth rings
on ear bones (otoliths) or scales, it became clear that only
a few age-classes accounted for most of the biomass in fish
stocks, even when many year-classes were present. The fish
in these abundant age-classes often dominate catches for
several years.
Recruitment is the term used to describe the number of
fish that reach a specified stage in the life cycle, usually the
age ofjoining the fishery. Large variations in egg and larval
survival mean that recruitment is very variable from year to
year, and often varies by a factor of20 or more.
Recruitment in fish stocks is highly variable. This is the
main reason why the abundance of fish stocks fluctuates
from year to year.
On average, more adult fishes would be expected to pro-
duce more recruits. If there were no limit to this relationship.
populations would grow indefinitely. In fact, compensation
occurs. and the number of recruits produced per spawner
is higher at intermediate rather than large population size
(Fig. 13.5). At large population size, densiry dependent
effects, such as spawners consuming their own larvae (com-
mon in plankton-feeding fishes like anchovy) or reduced
reproductive output due to competition for food or space.
lead to reduced average recruitment. Relationships between
spawner and recruit abundance (often known as stock-
recruitment relationships) determine how fish stocks
respond to fishing, because they describe the capaciry of the
stock to maintain abundance in the face of fishing pressure.
 13.6 Fishing methods
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

15,------------------,
Various mathematical models are used to describe
I • Red kingcrob I spawner-recruit relationships. These all feature high
recruitment at low population size and lower recruitment at

-'"- 1.0
large population size. Variance around the average model
is as important as the model itself. Such variance is driven
~
~

- • by physical and biological processes that are largely unpre-

c
c
~ - dictable, such as the stability of the water column and the
~
c
-'" •
••
timing of phytoplankton or zooplankton production peaks
·2
di! - 05
in relation to the timing of spawning and larval develop-
ment (Chapter 7) . The impossibility of predicting annual
•
levels of recruitment creates uncertainty for the fisher,
•
the fisheries' scientist, and anyone else who depends on a
• fishery. Owing to the challenge of predicting recruitment,
o 2 4 6 8 10
fisheries' surveys are often used to measure directly the
StOlk (tonnes XIQ'J abundance of young fishes a year or two before they enter
the fishery.
Figure 13.5 The spawner-recruit relationship for Alaskan
red king crab. Note that more recruits per spawner are View stock-recruitment relationships for many of the
produced at low abundance and the considerable variance world 's major fish stocks at http:/ /www.dal.ca/myers.
around the relationship that is largely due to the effects of
the environment on egg and larval survival.

Stock-recruitment or spawner-recruitment relationships

13.6 Fishing methods
describe the average numbers of recruits produced by a Humans use a staggering variety of innovative and not so
given number of spawners, and are used to help assess innovative methods to catch fish. These range from simple
the capacity of a fish stock to tolerate fishing . baited hooks on a handline, to dynamite bombs that are

(oj (bJ

/
(J (dJ

Figure 13.6 Examples of fisheries: (a) tuna line fishery, (b) tuna purse seine fishery, (c) squid jig fishery, and (d) dynamite
fishing on a coral reef. Copyrights: M. Marzot (FAO Photograph) (a), Fishing News International (b, c), and Thomas Heeger
(d).
 Chapter 13 Fisheries
thrown into the sea to stun fish (Fig. 13.6) . When fish are
very valuable. complex and expensive methods are worth
using. Thus, off Cape Cod in the USA, large bluefin tuna
(Thunnus maccoyii), which can sell for up to $US400 000
each, are tracked by spotter planes and shot from fast boats
with electrified harpoons (see also Chapter 14) .
Fishing gears are conveniently categorized into two
groups: active and passive. Active gears are usually towed
(,j
(b)
Figure 13.7 Examples of active fishing gears: (a) purse seine and (b) bottom trawl net.
across the seabed or used to encircle fish. These include the
familiar trawl and beam trawl nets that are towed behind
fishing vessels on most of the world's continental shelves.
and the giant encircling seine nets that are used to catch
oceanic fishes, such as anchovies and tunas (Fig. 13.7) .
Active gears also include dredges that are towed across the
seabed to catch shellfish, and gears such as spears, har-
poons, and explosives.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Passive fishi ng gears are put in the water and fish are
caught when they move into the gear: Active fishing gears
are towed or moved in other ways to pursue the fish.
Passive gears are put in the water and fish are caught
when they move into the gear. Examples of passive gears
are nets that are set on the seabed or left to float in the open
ocean, and entangle fish by the gills (Fig. 13.8). Other pas-
sive gears in widespread use are the baited pots used to
catch crabs, lobsters, or prawns, and various types of fish
traps (Sainsbury 1996).
Fishers would like their gears to catch target species with
great efficiency, and to catch little or no by-catch. However,
gear design relies on many compromises and factors such
(b)
13.6 Fishing methods
as price and efficiency are taken into account. As a result,
many gears catch target species but also impact the environ-
ment and non-target species. Thus trawl nets crush rare ani-
mals on the seafloor, and may catch non-target sea turtles
or skates, and gill nets can catch seabirds and marine mam-
mals. Only a few gears efficiently catch target species and
few others. These include the large purse seine nets used to
surround shoals of anchovy, herring, or sardine.
Not surprisingly, fishers are highly innovative people and
will always strive to increase the efficiency of their gears.
As legislation is introduced, either to reduce catching effi-
ciency or to reduce the environmental impacts of fisheries,
so fishers usually alter their behaviour and gear to maintain
their income.
Figure 1 3.8 Examples of
passive fishing gears: (a) gill
net and (b) long-line.
 Chapter 13 Fisheries
13.7 Fish stock assessment
A good understanding of the population biology of fished
species is needed to predict the levels of catch that can be
taken from fisheries, but without compromising catches in
future years. For fishing to be sustainable, the fishing mor-
tality that reduces population biomass must be balanced
by the levels of recruitment and growt h that maintain it
TECHNIQUES: Data inputs to fish stock
assessments
Fish stock biomass can be measured directly or it can be
predicted from knowledge of the contributions of recruit-
ment and growth and the losses from nat ural mortality
and fishi ng mortality (Fig 13.9). This box describes some
of the tech niques used to measure fish stock abundance,
recruit ment, growth, and nat ural and fishing mo rtality.
Direct estimates of biomass tha t do not rely on com-
mercial fishe ries data (fishery independent) are made
using a range of survey techniques. When these surveys
focus on younger age-classes of fish they will also pro-
vide estima tes of the numbers of young fishes that will
subsequently enter the fish ery. For bottom-dwelling spe-
cies in shelf seas, trawl surveys are widely used to esti-
mate abundance. These are usually conducted annually
and cover the same area wi th a standard fishing gear, in
an attempt to control those factors that lead to variations
in catch rates th at are not driven by true abundance. For
pelagic species, th at ofte n fo rm mono-specific schools,
acoustic surveys can be used to esti mate abundance.
Sound pulses are produced by the survey vessel and
when they meet objects of different density in the water
column, including fishes, the echoes they produce can
be recorded and proc essed to provide est imates of
fish abundance. The gas-filled swi m-bladders of fishes
account fo r much of the echo. Processing requires that
th e acoustic reflect ivity or target strength of the fishes
is known and th at the echoes from individual fish can
be integrated over depth and the distance travelled by
the ship.
Other methods of estimating fish abundance directly
include mark and recapt ure, underwater visual census,
depletion methods, and egg production methods. When
using mark- recaptu re, tagged fish are allowed to mix
wi th their popul ation, which is then re-sampled, with
the proportions of marked and unmarked fishes being
used to esti mate abundance. Successful application of
th e method relies on an identifiable population and the
random mixing of marked and unmarked fishes. It tends
to have been used most effectively for crustaceans that
live in fairly well-defi ned habitats. Underwater visual cen-
(Fig. 13. 9). Methods of fisheries' stock assessment seek to
estim ate the levels of fishing mortality that will safely be
balanced by recruitment and growth (Techniques box) . If
these levels of mortality are exceeded, then the size of the
stock and the capacity of the stock to maintain fishing mor-
tality will fall. Excessive fishing mortality is the main cause
of stock collapse.
sus involves counting and, in some cases, sizing fishes
directly. It is ofte n used over shallow-water habitats, such
as co ral reefs, but has also been in the deep sea from a
submersible vehicle. Depletion methods use relat ionships
between catch per unit effort and cumulative catch, over
a short period, to estimate abundance. They are easily
b iased if catch ability changes through time or there is
short-term immig ration or emigration from th e popula-
tion. Corrections have been proposed to deal wi th these
issues but require additional data collection. Egg produc-
tion methods use the abundance of fish eggs in the sea
to est imate the biomass of spawners that produce these
eggs. Eggs are caught in fine-meshed nets on surveys
tha t cover the spawning area and spawning season. Esti-
mates of the fecundity of spawners and the sex rat io
can then be used to estimate the numbers of fish that
would need to have reproduced to produce the observed
abundance of eggs.
Fishes sampled on surveys and in commercial fisheries
can be used to esti mate size at age and hence growth.
The ear bones (otoli ths) of fishes are usually used for
ageing, although scales are prefer red for some species
and do not require that the fish is killed when ageing.
Banding on the otoliths reflects seasonal growth patterns
and the ban ds can be counted to estimate age. Relation-
ships between size and age can be used to model growth.
When species cannot be aged, there are also a range of
methods that use the size distribution of a population to
estimate growth.
Total mortality rates in a fish population can be esti-
mated from the relationship between catch rates and age,
since the decreases in catch at age reflect reduct ions
in numbers owi ng to mortality, if other baises, such as
changi ng catchabili ty, can be controlled for. However, it is
very hard to sep arate the total mortality into natural mor-
tality and fishing mortality, owi ng to the effects of fishing
and inte ractions between fish populations on popula-
tion dynamics. For this reason , natural mortality is ofte n
app roximated, most recently by using life-history theory
that links rates of natural mortali ty to maximum body size,
actual body size, growth, and temperat ure.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Fish stock assessments are used to predict the catches
that can be taken from fisheries without compromising
catches in future years.
Many methods are used to assess sustainable levels of
fishing. Potential yields of fisheries are initially calculated
on a per-recruit basis because, as we saw in 13.5, recruit-
ment is unpredictable from year to year. However, once the
abundance of recruits in a year-class has been measured,
the yields per recruit can be converted to a total yield that
can be taken from the fishery.
Yield-per-recruit models are used to determine the
rates of fishing that give the best trade-off between the size
of fish caught and the numbers in the stock. Because fish
will die from both natural and fishing mortality, the num-
bersoffish in a year-class declines over time. However, indi-
viduals will also be growing over time. As a result, there
will be an optimal age for catching fish, the age when their
biomass is highest (Fig. 13.10) .
Yield-per-recruit models are models that are used to
predict when the potential yields per recruit are high-
est, but they ignore the potential effects of fishing on
recruitment.
Since yield-per-recruit models only predict the age when
population biomass is highest, they ignore the potential
effects of fishing on recruitment. The age at maximum pop-
ulation biomass could well be less than the age at maturity.
Thus intensive fishing could impair recruitment. Indeed.
we have already seen how recruitment falls when spawn-
Recruitment Growth
Population biomass
Fishing marta lily Natural Mortolily
Figure 13.9 The population biomass of fish is increased
by the processes of recruitment and growth and is
decreased by natural and fishing mortality.
13.7 Fish stock assessment
Mortolily
1
."
--
=
~
0
0
E
z
0
Grawth
1
Population Biomass
1
Aae •
Figure 13.10 As fish get older their numbers decl ine
due to mortality. However, their individual body size will
increase due to growth. As a result, population biomass
(size x numbers) is greatest at an intermediate age.
ing stockbiomass is low in our analysis ofstock-recruitment
relationships.
Replacement lines can be used to test whether fish-
ing will lead to recruitment failure and stock collapse. A
replacement line shows the replacement level where aver-
age recruitment rates are high enough to balance spawning
stock size. Using the replacement line, and a stock-recruit-
ment relationship, such as introduced in 13.5, Fig. 13.11
shows two replacement lines. corresponding to low (a)
and high (b) rates of fishing. We predict the fate of the
population from the starting stock size by using the stock-
recruitment relationship to predict recruitment in the next
generation and taking this as the new stock size'S'. In our
first example. the replacement line crosses the spawner-
recruit curve and the population will reach a theoretical
equilibrium. In the latter example. the replacement line is
steeper because fishing mortality is higher, so the stock can-
not replace itself and tends towards collapse.
Replacement lines are a method for the analysis of
spawner-recruit data that can be used to assess the risk
of recru itment overfishing.
 Chapter 13 Fisheries
(a)
Law fishing mortality
I-
J
b
~
~
Spawners - _•
Figure 13.11 Replacement lines on a spawner-recruit curve: (a) low fishing mortality and (b) high fishing mortality.
The diagram in Fig. 13.11 represents average and ide-
alized conditions. In reality. there are uncertainties in the
data used to conduct population analyses and a best single
estimate of the potential yield from a fishery is not neces-
sarily a good or reliable estimate. In recent years, there has
been much more emphasis on confronting risk and uncer-
tainty in fisheries' science. and the single best estimates that
were once used to advise fishery managers are increasingly
expressed as a series of estimates and associated probabili-
ties. For example, rather than stating that the total allow-
able catch should be one million tonnes, the scientists would
provide advice as a decision table, where the probabilities
of different stock sizes occurring in the future are given for
a range of capture options (Hilborn 1996) . This advice is
often more useful than advice based on single best estimates
as it allows managers to assess the potential consequences
of their decisions.
Reference points are usually used to guide manage-
ment (Caddy 1998). Reference points may provide targets
for stock biomass or fishing mortality that are sustainable
or avoid serious and irreversible harm to a fish stock. An
example of a reference point is B MSY' the biomass at which
the maximum sustainable yield is taken from the fishery.
Another example would be Bpa' the minimum stock bio-
mass that is consistent with the precautionary approach.
This means that if the biomass is above Bpa. then there is
a specified probability that biomass is above BUm' the limit
reference point identifying the biomass that is needed to
ensure stock persistence. Biomass reference points are usu-
ally presented with corresponding fishing mortality (F)
reference points. These indicate the rates of fishing mortal-
ity that need to be achieved to meet the biomass reference
points. Examples would be FMSY' Fpa' and FUmwith the values
determined using models that link biomass and fishing mor-
tality. Since the models are only representations of the real
world, it is never certain that a given value of F will lead to
the predicted value of B.
(bl
High fishing mortality
I.'"
-
J
~
.11
Spawners - _•
13.8 The management process
There are many possible goals of fishery management, from
maximizing catches. employment, income supply. or profit,
to ensuring that conflicts are avoided and rare species are
not threatened. Methods of analysis, such as those already
described for optimizing yields from single-species stocks,
have been used to assess how other management objectives
can be met (Hilborn & Walters 1992). Many fisheries are still
managed to meet social and economic objectives, although
there is increasing emphasis on fishery conservation and
protection of marine ecosystems. Once management objec-
tives are identified. science provides the basis for setting a
management strategy and advising on a management action.
Figure 13.12 gives examples of management objectives,
strategies, and actions. We have already seen how science
can be used to advise on management strategy and action.
Fishery management actions usually consist of catch
controls, effort controls. or technical measures. Catch
controls are implemented as total allowable catches or indi-
vidual catch quotas and effort controls are usually imple-
mented by limited licensing schemes for fishers or vessels,
effort quotas. or vessel and gear restrictions. Technical mea-
sures include controls on the size of mesh in nets in order to
let young fish escape, and closed seasons or area closures in
fisheries. All these management actions have advantages and
disadvantages, and may be difficult or expensive to enforce.
Most fisheries are managed using a combination of all three
approaches.
In modern fishery management, there is increasing
emphasis on a so-called precautionary approach, as man-
agers try to learn from lessons of the past and to apply this
wisdom in the future. The precautionary approach is based
on the idea that management actions taken today should
not compromise the needs offuture generations. and should
avoid changes that are not reversible. and identify unwanted
outcomes of management actions in advance, and the mea-
sures needed to correct them. The precautionary approach
applies both to the management of the target stock, and

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
to managing the impacts of fishing on the ecosystem (FAO
1995).
From ecological. economic, and social perspectives, fish-
eries' management has often been unsuccessful. An FAO
analysis suggested that the main factors leading to unsus-
t ainable fishing included inappro priate incentives, high
demand for limited resources, poverty and lack of alterna-
CURRENT FOCUS: Faith-based
fisheries
In a challenge to the growing percep tion that fi sheries
were in crisis as a result of g rowi ng demands for food
and income and ineffective management, Hilborn (2006)
questioned the quality of the science th at was used to
support these claims. He suggested that the view that
'fisheries management has failed, we need to abandon
the old app roaches and use marine protected areas and
ecosystem-based management' had become an ingrained
belief among many worki ng on fisheries ' issues and th at
they were looking for evidence to support this view, rather
than observi ng fis heries to ask how much evidence th ere
was to support this and othe r competi ng hypot heses.
Con t rove rsially, he contrasted advocacy in fi sheries
with scientists' unanimous condemnat ion of faith-based
teachings in evo lution. Hilborn em phasized that scien-
tists working on fisheries' issues sho uld reject agenda-
driven, faith -based publication, and revive a peer-review
process that was failing, because he felt th at almost any
paper showing a sig nificant decline in fish abundance or
t he benefits of marine-protected areas had a high prob-
ability of getti ng favourable review s in some high-profile
j o urnals. He pressed th e parts of th e marine science
commu nity that had adopted a faith-based approach to
remem ber t hat they were scientists and to go back to
searching for testable hypotheses and ev idence.
As we ll as high lighting weaknesses in the scientific
and peer-review process, Hilborn 's challenge reflected
the different w orld views assoc iated wi th conse rvat ion
and sustainable-use agendas. Scie ntists wil l have different
opi nions abo ut de sirab le states of the environment and
the role of fisheries. The se op inions are influenced by
their backgrou nds, interests, professional responsibilities,
and political and environmental views. They also influence
how sc ient ists perceive the current state of th e env iron-
ment and the perfor mance of fisheries' management, and
influence their behaviour and work as profess ional scien-
tists. As such, it is unavoidable that some scientists see
sustainable use w hen others see a pressing conserv at ion
issue (Jennings 2007) . This is especia ll y th e case in rela-
tion to changes in abu ndance, w here ach ieving maximum
13.8 The management process
tives, to fishing and lack of governance. These factors are
often paraphrased as 'too many fishers chasing too few fish'.
The FAO analysis also showed that scientific advice on the
status of fish stocks and the effects of fishing made only a
small contribution to a complex management and decision-
making process, and often carried little weight in relation to
immediate social and economic considerations .
sustainable yie ld for a fish po pulat ion is often associated
wi th declines in biomass of 4 0 -60% from the unex-
plo ited state. Thu s, in relation to a management objective
for sustainable use, such a decline may be acceptable,
while those w ith objectives that tend towards preserva-
t ion might consider the same decli ne to be unacceptab le.
More recent ly, Hilborn and Boris Worm, th e author of
a paper that Hilborn had previously cri t icized, decided
to coll aborate. Their intenti on was to avoid faith-based
approaches, by enco uraging a hypothesis and data-driven
exercise where scient ists w ith both conserv at ion and fish-
eries' backgrounds worked together w ith the same data in
an attempt to draw scientific concl usions about the state
of w orld fisheries. The analysis explicit ly exami ned th e
trade-offs between co nservation and sustainable use, and
showed that fi shing rate s below those that gave maxi-
mum multi-species sustainable y ield wo uld provid e a sig-
nif icant proportion of th e potent ial food and income from
a fishery, whi le minimizing speci es'col lapses and imp acts
on fish size and abundance (Worm et al. 2009) . Further,
th ey showed th at fishing rates were decreasing in half of
th e ten systems that they examined in detail , and in so me
cases reaching or falling below th e rate s th at wo uld y ield
maximum multi-sp ecies sustainable y ield . The auth ors
did cauti on that their analysis w as largely co nfined to
intensively managed fi sheries in deve loped co unt ries,
w here scienti fic data on fish abundance are coll ected,
and pointed out that so me excess fi shing effo rt is simply
disp laced to co unt ries w ith weaker laws and enforcement
capac ity. However, this data-focused analysis did serve
to dem onstrate that management was working in so me
fisherie s and that not all fisheries' managem ent had failed.
Interestingly, the manag ement methods used to co ntrol
exploitation rate s were, and sti ll are, diverse and a com-
bination of approaches, such as catc h quotas and co m-
munity management co upled w ith st rateg ically pl aced
fi shing clos ures, ocean zon ing, selective fishi ng gear,
and economi c incent ives, cou ld all help to meet manage-
ment objectives for fi sheri es and ecosystems. The most
important thing was that these manageme nt efforts were
customized to the place and th e fishers to be managed.
 Chapter 13 Fisheries

Maintain sustainability 13.9.1 Fish communities

Management offishery
objectives Species vary in th eir vulnerability to fishing. Apart from
Minimize environmental
impacts the simple fact that a la rge hook or net with a large mesh

I will only catch large individuals, vulnerability depends on

behaviour and life history. Life history determines the levels
Maintain abundance of fishing mortality that a population can tolerate, and spe-
Management of bycotch species cies with slow growth, late maturity, and large body size are
strategies Maintainabundance very vulnerable to fishing . In many cases. species with la rge
oltorgetstock body size are also the favoured targets of fishers.
Fishing has consistently reduced the abundance oflarge
fishes in the world's oceans. Thus communities once domi-
Area closures to protect
nated by large fishes are now dominated by small fishes
Management bytotchspecies
and invertebrates. To some extent these changes can be
actions (otch limits (size and reflected in the composition of la ndings. For example, Fig-
nu mbers) for torgetstock ure 13.13 shows that smaller species now dominate land-
ings from parts of the Atlantic. Pacific. and Indian Oceans.
Figure 13.12 From a management objective to a However, changes in the composition of landings are not
management strategy and action. always indicative of changes in the sea because fishers'
gears are selective and small species may be differentially
13.9 Environmental impacts of targeted when they are more valuable.
fishing Manyfisheries are 'mixe d' fisheries and catch many spe-
cies of target and non-target fishes. This applies particularly
While fishing provides food, income, and employment, the to trawl-net fisheries that catch bottom-dwelling fishes and
ever-increasing intensity and diversity of fishing operations many trap and line fisheries on coral reefs. The differential
has environmental costs that impact the productivity and vulnerability of species to fishing means that some will be
biodiversity in ecosystems. Here, we see how non-target dramatically depleted by levels of fishing that others can
fishes, birds, mammals, and turtles are affected by fishing withstand. The North Sea, for example, has been heavily
and the impacts of fishing on habitats such as sea mounts, trawled for over 100 years, and species with large body sizes
kelp forests, and coral reefs. These impacts are a growing and slow growth, such as the largest skates and rays, have
concern for fishery managers and conservationists. been virtually extirpated in that period. One estimate sug-
:---~

- -

Change in ~on do rd length(em)

_ <·100
_ > ·100··50
Figure 13.13 Differences between the mean maximum lengt h 0 > ·50 · ·5
of fish and invertebrate species landed in global fisheries in the 0 > · 5. < 0
19505 and 19 905. From Pauly et al. (2005). o no chongefinaeose
 13.9 Environmental impacts of fishing
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
gests that the current biomass oflarge fishes weighing 4-16
kg and 16-66 kg, respectively, is now 97'4% and 99·2%
lower than in the absence of fisheries exploitation, while
the community biomass (fishes 64g to 66kg) is 38% lower
than predicted in the absence of exploitation. Community
biomass is less affected because small and intermediate-
sized fishes can still be productive at high rates of fishing
(Jennings & Blanchard 2004) . Throughout the world's seas,
there are examples oflarge, slow-growing species becom-
ing locally and regionally extinct. These include groupers
and large parrotfishes on tropical reefs and sharks and
skates in the Atlantic (Dulvyet al. 2003).
13.9.2 Birds and marine mammals
Fishing is often most vehemently criticized when birds,
marine mammals, and turtles are taken as by-catch. These
impacts have consistently attracted more public attention
than the impacts offisheries on fish, and have forced fishery
closures and significant changes in fishing methods. Mass
dolphin mortality in the eastern tropical Pacific tuna purse-
seine fishery during the 1960s and early 1970s attracted
considerable public attention and provoked widespread
criticism ofthe environmental impacts offishing. Hundreds
of thousands ofdolphins were killed annually because purse
seiners set their nets around pods of dolphin to catch the
tuna that swam with them. When the nets were hauled. the
dolphins were trapped and usually died. By 1980, the popu-
lation ofeastern spinner dolphins (Stenella longirostris) was
reduced to one-fifth ofits original abundance. Intense pub-
lic pressure and consumer boycotts of tuna products led to
new fishing practices to release trapped dolphins alive and
the use of observers to monitor dolphin mortalities on all
•
purse seiners.
Today, annual dolphin mortality is less than 5% of that
in the 1970s. and consumers increasingly purchase pole
and line caught 'dolphin friendly' tuna. Levels of marine
mammal by-catch in most fisheries are now set so that the
(0) ~ :AI;
Figure 1 3.14 (a) A drowned black-browed albatross caught up in the meshes of a trawler fishing in the Southern Seas.
(b) These shags became entangled in a ghost-fishing bottom-set gill net while trying to extract the gadoid fish (middle).
(Photographs: (a) Richard Woodcock (b) Blaise Bullimore.)
mortality rates do not threaten the long-term viability of the
population (Allen 1985; Hall 1996) . However, while many
consumers were concerned about dolphins. far fewer were
concerned about sharks, and it has become clearthat shark
by-catches in tuna long-line fisheries have led to worldwide
collapses in some shark populations (Baum et al. 2003).
Seabirds are caught by accident in long-line and gill
net fisheries . There is particular concern for the viability
of wandering albatross (Diomedea exulans) populations
because these albatrosses are frequently caught on long-
lines used to catch southern bluefin tuna (Thunnus mac-
coyii) and Patagonian toothfish (Dissostichus eleginoides)
in the Southern Ocean (Fig. 13.14) . The bluefin runa fleet
deploys 107 million baited hooks annually and killed 44
000 albatrosses prior to 1989. Despite the introduction of
some conservation measures, this albatross could decline
to extinction ifhook numbers are not dramatically reduced.
Seabird catches on long-lines are an inconvenience for
the fishers as well. They lose bait and have to reset the lines.
Conservation measures introduced include bird scarers
and devices that set the lines below the diving depth of the
birds. However. some bird populations have already been so
depleted by fishing that any further by-catches are likely to
threaten their viability (Weimerskirch et al. 1997).
13.9.3 Trawling impacts on the seabed
When trawls are dragged over the seabed, they are bound to
kill animals and damage habitats. The significance of trawl-
ing impacts depends on the habitats where they are fished
and levels of narural disrurbance on the fishing grounds. On
sandy seabeds in shallow, tide-swept, and wave-impacted
areas, most of the animals living on and in the seabed are
very well adapted to high rates of mortality and disrurbance,
and the effects of trawling are relatively minor (Chapters 8
and 15) . Conversely, in deep areas where wave and tidal
action are low and the seabed habitat is dominated by habi-
tat-forming (biogenic) species. trawling can have major and
(b)
 Chapter 13 Fisheries
long-term impacts that reduce both biomass and diversity
(Jennings & Kaiser 1998; Kaiser & De Groot 2000). Typi-
cal examples of vulnerable habitats are maerl beds, coral
reefs, and the biogenic habitats on sea mounts. The impacts
of trawling on sea mounts are perhaps the most dramatic
described to date (Box 13.3 ).
Simple empirical and modelling stud ies have shown that
many seabed species w ill be extirpated if trawling frequen-
cies exceed 2 to 3 times per year. However, large-scale stud ies
of the distribution of fauna on many major fishing grounds
show that many vulnerable species persist. The reason for
this is that trawling d isturbance is actually very patchy (Fig.
13.15). While m any shelf seas are swept, on average, at
least twice each year, fishers tend to return to favoured fish-
ing grounds and trawl tows that they know to be free from
obstructions. As a result, some areas may be trawled 10 to 15
times each year, while adjacent areas are vir tually unfished.
Provided that spatial patterns of effort are consistent from
year to year, animals can recolonize fished areas from those
that remain unfished. Management measures that increase
the long-term homogeneity of effort, such as rotating closed
areas, m ay increase the cum ulative effects of trawling.
In add ition to the changes to ecosystem processes caused
by bottom fishing d isturbance, alteration of the seabed may
also change its functional importance for associated target
species. In other words, not only does fishing deplete fish
stoc ks, but it may also adversely affect their habitat. This
Box 13.3: Trawling impacts on sea
mounts
Technological development of fishi ng gears and fish-
ing boats is making more and more habitat accessible
to trawling. Sea mou nts, once difficult to locate and too
rocky to trawl, have been heavily fished in recent decades,
A multi beam image of Ely Sea mount. A caldera is visible at the top. (Image: Jason Chaytor/NOAA).
re alization has sparked a flurr y of activity to identify wh at
has become termed 'essential fish h abitat'. Amendments to
the US Magnuso n-Stevens Act require fisheries m anagers
to co ns ider the wider ecological impacts of fishing ge ars
upon fish h abitat in addition to issues such as fishing effort
control and total allow able catches (Auster & Langton
1999 ). Essential fish habitat (EFH) is a description open
to interpretation, but it is clearly defined w ithin legislation
to mean 't hose waters and substratum necessary to fish for
spawning, breeding, feeding or growth to maturity'. This
legislation is an important step towards an ecosystem based
fisheries management (13 .10) as it recognizes the potential
negative effects of the direct and indirect effects of fishing
on fish populations. The introduction of this legislation
caused a hiatus among m anagers, w ho we re faced w ith
the t ask of identifying EFH for a multitude of species. This
revealed large voids in our knowledge about the basic biol-
ogy of many of the species currently under management.
Some elements of EFH, such as spawning and nursery
areas, are relatively well-known for the majority of com mer-
cially explo ited species, and in many cases these are already
afforded some protection by permanent or seasonal area clo-
sures. Nevertheless, for some particularly vulnerable species,
such as rays, we know w here breeding aggregations occur,
but the habitat into which the eggs are laid remains open
to speculation . However, of equal relevance are the habi-
tat quality issues that affect the acquisition of food and the
as fishing vessels can now 'mine ' them for stocks of long-
lived and slow-growi ng species, such as orange roughy
(Hofpfostethus atfanticus). Electronic positioning systems
on the vessels and nets can be used to posi tion the net
precisely and to traw l on the relat ively ti ny sea mounts
tha t rise from depths of several kilometres to within 500
 13.9 Environmental impacts of fishing
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
to 2000 m of the surface.
Sea mounts are unique deep-sea environments, and,
because they rise from great depths, their topog raphy
enhances local wate r cur rents. These currents carry
nutrients and prey over the sea mounts, and rich com-
plex com munities of suspension feeders, such as corals,
develop, in contrast to the low biomass communities of
deposit feeders on the surroun ding seafloor. Many ben-
thic species living in association with sea mounts are new
to science, long-lived, and vulnerable to traw ling.
When sea mounts are fished for the first time the nets
can take by-catches of several tonnes of coral! In fact,
as the first orange ro ughy fisheries developed off New
Zealand, there was interest in starting a precio us coral
industry based on black coral by-catch! The damage to
coral is the first and most dramatic effect of traw ling on
avoidance of predators. The identification of those habitats
that may have an important or 'essential' functional role for
individual species is likely to be complex for those species
that utilize different habitats at partic ular stages of their
life history. For example, many fish species start life close
inshore , moving further offshore as they increase in bod y
size (Rijnsdorp & van Leeuwen 1996) . It might be relatively
straightfor ward to identify EFH for fish strongly associated
w ith seabed str uctures, such as reefs or bioge nic habitats
(seagrasses, m angroves, oyster beds), however many fish in
temperate systems exhibit highly flexible lifestyles and utilize
a wide range of different habitat types. Never theless, for such
species, it is possible to identify areas that consistently attract
the greatest proportion of the population, and presumably
these areas fulfil some functional role.
Previous studies of the relationship between fish assem -
blages and their environment have focused on the relation-
ship between fish distribut ion and enviro nmental variables
such as salin ity, depth , and substratum type (e .g. Smale
et al. 1993). In some cases these variables are good co r-
relates of some fish assemblages. They do not necessarily
defi ne the essential fe atures of a specific h abitat; rather
they constitute a co mponent of that habitat that m ay act as
a sur rogate for some other more important habitat feature .
Habitat complexity and str ucture appear to be important
physical features for some fish species (Auster et aI. 199 7).
Many stud ies have demonstrated the relationship between
flatfish species and the sediment particle composition of the
seabed (Gibson & Robb 1992). For example , small plaice
are better able to bury themselves in sediments that have
a particular grain-size composition and choose particular
sedimentary habitats accordingly. Hence, a specific particle
size-compos ition m ay be an essential habitat requirement
for flatfish, w hereas the presence oflarge sess ile epifauna or
sea mounts and has immedi ate knock-on consequences
for fish and invertebrates th at use coral habitat.
When t rawled and untrawled sea mounts are compared,
it is obvious th at the untrawled mounts have a diverse
inverteb rate fauna of high b io mass, dominated by sus-
pension feeders including hard and soft corals, hydroids,
sponges, and brittlestars. Of the inverteb rate species
studied on untrawled sea mounts south of Tasmania,
2 4-43% were new to science and 16--33% we re prob-
ably rest ricted to the sea mo unt environ ment. The benthic
biomass on untrawled sea mo unts w as 10 6 % g reater,
and the number of species per sample 46% g reater, tha n
on traw led sea mounts. The unwanted effects of traw ling
on these habitats provided justification for establishing a
'Mari ne Protected Area' around twelve sea mounts.
Source: Koslow et al. (2001) .
•
-.. .... ~
Figure 13.15 The patchy spat ial distribution of bottom
trawling activity around the UK in 2007. Each point is
the record of a vessel location from a sat ellit e vessel
monitoring syst em. (Lee et al. 2010.)
rocky substrata might be considered non-essential. In con-
trast, str uctural complexity g reatly increa ses the survival
ofjuvenile roundfishes as it provides refuge from predation
(Tupper & Boutillier 1995) (Box 13.4).
Just because we find fish associated with a particular
habitat does not necessarily ind icate that the habitat h as an
essential functional role. For example , there is great inter-
est in the relatively recent discovery of deep-water co ral
reefs on the continenta l shelf edge of the Nort h Atlant ic
and elsewhere. These reefs provide prominent habitat fea-
tures in a relatively uniform seabed landscape and act as
foci for fish such as redfish (Sebastes spp.) for w hich there
is a commercial fishery. Conser vation gro ups a rgued for the
 Chapter 13 Fisheries
Box 13.4: Essential fish habitat
Biogenic (living) and physical features of seabed habi-
tats can have a critical function for certain commercially
important species. Mud habitats appear to have few large-
scale topographic features, but large cerianthid anemone s
provide shelter for animals such as spider crab (Lithodes
sp.) (a). Depressions in the seabed formed by other
(01
protection of the reefs on the basis that they provided EFH
for the redfish (Malakoff 2004) . However, redfish are found
in a wide variety of h abitats across a large geog raph ic area,
and despite a concerted research effort evidence of a critical
link between redfish ecology and deep-water corals remains
uncertain (Fossa et al. 2002; Kaiser 2004) .
13.9.4 Effects of fishing on coral reefs
In Chapter 11, we saw that coral reefs are among the most
delicate and highly structured m arine habitats. The topo-
gra phic comple xity of reefs provides refuge and feeding
opportunities for m any fish and invertebrate species. Areas
of act ively growing reefs that h ave not been damaged by
human activities can sustain fishery yields of up to 5 tonnes
km- year! (Fig. 13.1 6). These fisheries are usually prose-
cuted by line and spear fishers, who cause minimal d amage
to coral and catch a range of species from many trophic lev-
els. However, growing human populations have driven the
organisms, such as sea scallops, o r the t roug hs of sand
waves provide cove r for silver hake (Merluccius biliniaris)
from where they ambush prey (b). Attached fau na, such
as sponges, provide complex th ree-dimensional structure
in which fish, such as sculpin (Myoxocephalus sp.), can
shelter from predators and ambush their prey (c).
(Photographs: © Peter Auster.)
(bl
development and expansion of fisheries on tro pical coasts,
and fishers are inc reasingly turning to habitat destructive
fishing methods to maintain yields. For m any fishers, who
have few, if any, alternative so urces of food and income,
there is no choice but to do this.
Muro-ami drive netting, bottom set gill nets, and heavy
traps have all caused habitat destruction on reefs. Muro-ami
fishing is widely practised in South-East As ia and involves
fishers driving fish towards a net w it h weighted scare-lines
that are dro pped repeatedly on to the coral. However, fish-
ing with explosives has even greater effects on reefs. Explo-
sive, blast, or dynam ite fishing is pract ised in m any regions,
and although it is often illegal, this is unlikely to deter fish-
ers desperate for food and income. Repeated blast fishing,
whe re explosive charges are detonated over and on the reef,
soon reduces large areas of actively growing reef to rubble.
Needless to say, fisheries of this type are not sustain able,
killing manyjuvenile and non -target species and destroying
their habitat.
 13.10 Ecosystem-based fishery management
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Fisheries also have indirect effects on coral reefs. Sea
urchins and fishes, such as the colourful parrot and sur-
geonfishes, are the dominant herbivores on reefs. The
persistence of herbivorous fish on reefs depends on the
presence offish that eat sea urchins. These urchin predators
maintain sea urchin populations at a size where their low
gross production makes them poor competitors with herbiv-
orous fish. If populations of urchin-eating fish are reduced
by fishing, then urchin populations expand and the urchins
graze reef algae to such low levels that herbivorous fish can
no longer compete. The dominance of urchin grazers on
heavily fished reefs has knock-on consequences for corals.
Thus, herbivorous fish clear space for coral settlement, and
enhance the growth and survival of young coral colonies,
while urchins erode the substrate as they graze and pre-
vent coral recruitment and growth. On heavily fished reefs
where urchins dominate the grazer community. bioerosion
leads to loss of structural complexity, reduced fish biomass
and disruption of the ecological processes responsible for
fish production (McClanahan 1992) (see also Chapter 8) .
13.9.5 Effects of fishing on kelp forests
As in our last example of the indirect effects of fishing, we
look at another situation where urchins playa keystone role.
Kelp forests are found in many cool. shallow. and nutrient-
rich coastal waters (Chapter 8), and support diverse fish
and invertebrate fisheries. Sea urchins graze on kelp, and
when sea urchins become abundant, either as a result of
high levels of recruitment or the indirect effects of fishing,
they can graze kelp until the kelp forest ecosystem shifts
to an alternative state, known as 'u rch in barren ground'!
The extent ofMacrocystis kelp forests offsouthern Califor-
nia has shrunk dramatically since the mid-twentieth century.
This is partly the result of changing oceanographic condi-
tions and pollution. but is also due to the depletion of urchin
Figure 13.16 Selling fish caught
in a coral reef fishery in Fiji.
Photograph: S. Jennings.
predators. Both the spiny lobster (Panulirus interruptus)
and the sheepshead (Semicossyphus pulcher) were once suf-
ficiently abundant to help limit urchin populations, but this
is no longer the case. Ironically, a large fishery that targets
the red sea urchin (Strongylocentrotusfranciscanus) has now
developed, depleting urchin populations and allowing the re-
establishment ofkelp in some areas (Tegner & Dayton 2000) .
Compare this example of a fishing effect wit h that of
hunti ng of sea otters in Chapter 8.
13.10 Ecosystem-based
fishery management
Fisheries can provide society with huge benefits in terms of
income. food, and employment, but instead. fisheries are
often unsustainable and an environmental threat.
The ecosystem approach to fisheries management
(EAFM) is widely adopted by the current management agen-
cies. The EAFM is part of the ecosystem approach and is con-
sistent with the concept of sustainable development, which
requires that the needs offuture generations are not compro-
mised by the actions of people today. The broad purpose of
the EAFM is to plan, develop, and manage fisheries to meet
the multiple needs and desires ofsocieties. butwithoutjeop-
ardizing the options for future generations to benefit from
the full range of goods and services (including, of course,
non-fisheries benefits) provided by marine ecosystems (FAD
2003) . The approach is usually geographically specific, adap-
tive. considers multiple drivers. takes account ofuncertainty,
seeks to balance multiple objectives, and involves stakehold-
ers (FAD 2003; Browman & Stergiou 2005; Murwaski 2007) .
The success of the EAFM depends on whether high-level
governmental commitments to an EAFM can be turned into
 Chapter 13 Fisheries

specific. tractable, and effective management actions that
will lead to better fish-stock management and remedy the
unwanted impacts of fishing on non-target species. habitats,
and ecological interactions. With some notable exceptions,
such progress with implementation has been slow to date
(Pitcher et al. 2009) . Moreover, implementation of EAFM
will not remove the high, short-term costs of moving towards
sustainability (principally the costs ofcapacity reduction and
providing alternative employment) and ways ofmeeting and
mitigating these costs still need to be explored.
Many of the existing moves towards the implementation
of the EAFM have often been characterized by management
action to mitigate the environmental impacts of fishing on a
case-by-case basis. Thus turtle excluder devices (lEDs) have
been fitted to trawls to stop turtles being killed as by-catches,
or fisheries for small pelagic 'forage' fishes have been closed
in the vicinity of seabird breeding colonies. These manage-
ment actions are likely to be the first steps in a long process
of integrating environmental concerns into fisheries' man-
agement, and many commentators now see the EAFM as an
evolutionaryratherthanrevolutionaryprocess. In the longer
term it is likely that indicators of the impacts of fishing on
habitat and non-target species will be used to set targets for
ecosystem-based fishery management and to assess the suc-
cess of management action. The choice of indicators is likely
to reflect the growing priorities of species' and habitat con-
servation as justifiable goals of management, and it is likely
that increasingly large areas of the sea will be closed to fish-
ing in order to meet conservation objectives (Chapter 16) .
13.11 The future of fisheries
Many fisheries are currently fished beyond sustainable limits
and expected reductions in fishing effort will provide long-
term benefits, by creating more productive and more profit-
able fisheries and reducing environmental impacts. Capacity
for improved fisheries' management will be greater in the
developed world where there will be some commitment to
meeting the short-term costs of effort reduction. The pros-
pects for sustainability in poorer nations are not so good.
unless the international community makes the financial
commitment to provide alternative livelihoods for fishers.

Chapter Summary
• Fisheries are a vital source of food , income, and employment, especially in the developing world .
Around 80 million tonnes of fish are landed each year and 20 species of fish account for over 40Cfo
of these landings.
• Fishing gears can be described as active or passive. Active gears are towed towards the fish , while pas-
sive gears are not. Fishing gears catch a range of species, including bycatches, that will be discarded
by the fishers if they are not worth eating or selling.
• Stocks fluctuate in abundance as a result of natural and fishing effects. Variations in egg and larval
survival have a major impact on the size of year classes recruiting to the fishery.
• Fish stocks are usually assessed to predict the size of catches that can be taken without compromising
future catches. Fishery management actions consist of catch controls, effort controls, and technical
measures.
• Fisheries have environmental costs that can threaten rare species and the sustainability of the fished
resource. There have been increasing attempts to mitigate these costs by adopting the precautionary
approach and ecosystem-based fishery management.
• Large reductions in global fishing capacity are needed to get the greatest social and economic benefits
from fisheries and to ensure that biodiversity conservation and sustainability goals are met.

Further Reading

A wide-ranging introduct ion to marine fisheries ecology is provided by Jennings, Kaiser, and Reyno lds (2 0 01 ).
Th is book describes f isheries exploitation, conservation, and management in tropical, temperate, and polar
environments, and focuses on issues of contemporary concern such as marine reserves, the effects of fish ing
on coral reefs, and the incorporation of the precautionary princ iple into management advice.
• Jenn ings S., Kaiser M. J. & Reyno lds J. D. 2 0 01. Marine Fisheries Ecology . Blackwell Science, Oxford.
Aquaculture
Chapter Summary
Aqu acu lture in marine systems can be traced back to well
before Roman t imes. Even then it was clear that the culture
of marine speci es w as feasib le only at great expense. While
freshw ater products conti nue to contribute most in terms of
lan dings and val ue, marine produ cts are becoming increas-
ingly important, and technological advances make it more
viable to produce fi sh and other biota at reasonable cost
and w ith a reduced environmenta l impact. Aquaculture ere-
14.1 Introduction
Marine aquaculture continues to be a rapidly expand ing
global industry and is probably one of the best examples
of our ability to take biological knowledge and apply it
to improve the biological and economic yield from the
marine environme nt. Given current rates of global human
population growt h, it will be necessary to produce an
additional 40% of protein from the sea by 2030. As cur-
rent yields from capture fisheries taken around the world
have either reached a plateau or are diminishing, there is
a growing need to consider aquaculture as an alternative
source of obtaining protein from the sea. As many wild
capture fisheries have collapsed and local economies have
suffered the consequences of the ensuing economic hard-
ship, many have pointed to aquaculture as the solution to
the impending shortfall in food production from the sea.
Some even speculate that aquaculture could remove the
need to fish wild stoc ks altogether. As our understanding
of the life-history requireme nts of an increasing range of
species increases, so previously 'd ifficult' species have
become more feasible subjects for cultivation. In addition
to these advances, increasing automation, improved feed
ates its own environmental prob lems and has led to disease
outbreaks, over-harvest ing of forage fi shes to generate fish-
meal, genet ic dilution of w ild stoc ks from farm escapees,
and has caused eco log ical problems in areas where local
carry ing cap acity has been exceeded. A better understand-
ing of these issues w ill help to ensure that aquacultu re is
undertaken in an environmentally sustai nable manner.
technology, and high technology waste -treatme nt systems
have contributed to a decline in the costs of production of
many species. As a result, fish-farmed cod (Gadus morhua)
landed on the shelves of major retail outlets for the first
time in 200 1 (although this remains financially unviable
at present given the subsequent demise of the comme rcial
companies involved ).
Although aquaculture can be traced back several millen-
nia, it is still an industry very much in its infancy in some
parts of the world and consequently is associated with its
own social and environme ntal problems that vary accord-
ing to geographic context. Indeed some sectors, such as
shrimp cultivation, have witnessed their own 'gold rush'
as a result of high market values of shrimp . As with any new
industry, the primary concern of participants has been to
invest in technology and research des igned to overcome
the problems of production and stock control, such that
the enterprise becomes economically viable. In contrast,
less attention has been given to the environmental conse -
quences of cultivation practices. Yet it is ironic that in many
parts of the world the environme ntal impact of aquaculture
practices has become one of the impediments to the fur-
ther expansion of the industry. Thus it appears that short-
 Chapter 14 Aquaculture
• • • • • • • • • • • • •• • • •• • • •• • • • •• • • • • • • • • • • • • • • • • • ••• • • • • • • • • • • • • • • • •• • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • •

term economic return continues to dominate the business In past and present times aquaculture of omnivores or
of aquaculture in developing countries . This chapter aims shellfish has provided an easily harvested and reliable
to introduce the historical developme nt of aquaculture, source of food .
the variety of techniques used to rear a range of different
organisms, the technology employed to increase productiv- In the past, aquaculture has provided a reliable and easily
ity, and the environmental and biological consequences of harvested source of protein that is independent of natural
aquaculture in m arine ecosystems. As aquaculture involves fluctuations in capture fisheries. However, the present-day
the rearing of organisms in an artificial environment, there production of fish-oil, which is key for the cultivation of car-
are potential welfare issues that are of concern to wider nivorous fish species, has declined over the last two decades;
society, hence the chapter also considers this issue. this means that the further expansion of this sector of aqua-
culture may be impeded (Current Focus : The catch-22 of
The environmental impacts of aquaculture have become aquaculture) . The term 'a qu a cu ltu re' has only been in
one of the impediments to its further expansion. use for about 40 years, which coincides with its incre asing
industrialization, most notably in the salmonid sector of the
industry. The term 'culture' implies human intervention that
14.2 Aquaculture past and enhances production of the cultivated species. This m ay be
very simplistic at one level (e.g. the introduction of nutrients
present and organic material from animal wastes, as in Chinese poly-
Fishes, molluscs, crustaceans, and plants have been culti- culture systems), ranging through to highly sophisticated
vated by humans for several thousand years. Archaeological computer-controlled culture in intensive water-recirculation
evidence is strongly suggestive of the culture of carp (Cyprin- systems. In the early 1970s the production offreshwater and
idae) by early civilizations as widely distributed as China, marine fish and shellfish was the equivalent of only 12% of
Japan, and Italy. Indeed, carp are recurrent motifs in art the annual world fish landings for human consumption (c.
from these regions. Car p were no doubt cultivated for their 6 million tonnes). At that time, this source of protein pro-
food value but also for their aesthetic appeal. whic h gave vided 4% of the world's supply of animal protein, excluding
rise to varieties such as koi carp, much valued by aquarists in the contribution of milk. In As ian countries, aquaculture
present-day cultures. Carp are an ideal species for cultivation makes a far greater contribution to the overall supply of ani-
due to their tolerance of high-stocking densities and low dis- mal protein due to the prevalence of freshwater aquaculture
solved oxygen levels, their omnivorous diet and high growth in this area, and almost 75% of fish cultivation arises from
rates. However, marine species present a much greater tech- Asia (Allsopp 1997; Subasinghe et aJ. 2009). Since the early
nological challe nge because of their requirement for high 1970s, the production of finfish has increased ten-fold while
water quality and, in many cases, their carnivorous diets, a the contribution of capture fisheries to world protein supply
fact recognized long ago by the Romans (Box 14.1). has only doubled (Fig. 14.1). As a result, in 2007, aquacul-
ture contributed c. 45% to the global production of fisheries,
Fish have been cultured for many thousands of years. worth US$94.s billion at first sale value, of which marine
However, the culture of marine species is far more systems contributed US$37.S billion (FAO 2007).
demanding than that of freshwater species.
While production of protein from wild-capture fisheries
reached a plateau in the early 1990s and latterly has
begun to decline, aquaculture now provides nearly 45%
Box 14.1: Aquaculture in Roman (65.1 million tonnes) of all aquatic products (both fresh-
times water and marine).
'There are two kinds of fish-ponds, the fresh and
the salt. The one is open to common folk, and not While m arine-capture fisheries are governed by enviro n-
unprofitable, where the Nym phs furnish the w ater for mental factors that affect recruitment and hence are unpre -
our domestic fish; th e ponds of the nobility, however, dictable and vulnerable to over-exploitation, aquaculture
fi lled w it h sea-water, for whi ch only Neptune can is largely dependent upon inputs of feed and upon good
furni sh the fish as w ell as the water, appeal to t he m anagement of the cultivation system to avoid disease
eye more than the purse, and exhaust the po uch of and enviro nmental degradation. These criteria for success-
the owner rather than fill it.' ful aquaculture in some way appear to be more att ain able
From Rerum Rusticarum by Marcus Terentius Varro than a more rational use of wild fisheries. Despite this,
(12 7- 126 BC), translated by Hooper & Ash (1934). m any aquacu ltu re practices are themselves d ependent
upon wild-capture fisheries to provide protein from lower
down the food chain (e .g. smaller fishes, such as sandeels,

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Ammodytes spp., or anchoveta) to make fishmeal. However,
this irony h as been brought sh ar ply into focus by some that
have made a case that aqu aculture is partly the cause for
the demise of certain world-capture fisheries (Naylor et a1.
2000). For this and other reasons, plant-based fish-feeds
are seen as the most attractive solution to disengage aqua-
CURRENT FOCUS: The catch-22 of
aquaculture
At present, the cultivation of predatory finfish species is
highly dependent upon the availability of fish oils th at
are included in the formulated diets that are fed to these
species. As a result, aquacultu re is a net 'consumer' of
wild captu re fisheries, in particular, of oil rich species
such as anchoveta and othe r small pelagic species. While
it is possible to replace the protein in fish feed wi th plant-
derived alternatives, the rep lacement of fish oil with plant-
based oils is not so simple. Fish oil has a particularly high
content of n- 3 highly unsatu rated fatty acids (HUFAs)
that are essential for the optim al growth and healt h of
farmed fish (Tu rchini et al. 2009). Thus, the availability
and efficacy of the use of fish oil presents a challenging
bottleneck to the further development of the aquacultu re
industry focused on carnivorous fish, especially given the
continued decline in the annual production of fish oil from
1985 (1481 t) to 2006 (988 t) . The same issues do
not apply to the cultivation of herbivorous or om nivorous
freshwater species, such as carp and tilapia.
What are the alternatives?
Current research indicates th at fish can cata bolize oils
produced by plant species such as soya, linseed, palm,
canola, and sunflower. This means that some of the fish oil
currently used in fish meal is simply used to maintain the
metabolism of the fish by providing a sou rce of energy
and hence this can be replaced by a plant substitute. A
vegetable oil that would provid e a good substitute for fish
oil would have a high satu rated fatty acid and monoun-
saturated fatty acid content (Tu rchini et al. 2009). Many
forms of vegetable oil are rich in n-6 and n-9 fatty acids
and they can be blended to produce an optim al feed that
achieves good growth rates, although this will still lack
sufficient HUFA to produce the same results as a feed
blended wi th fish oil.
One method to reduce the reliance on industrial fish-
eries to generate fish feed is to improve the manner in
w hich we utilize waste from the fish-processing industry.
Fish viscera contain livers, w hich are storage organs that
contain high levels of fish oil. Viscera retained from pro-
cessed catfish contained up to 2 1 mg s' dry weight of
14.2 Aquaculture past and present
culture from its dependence upon wild fisheries, which
provide an unpredictable product of var iable quality. With
the increasing move towards genetically engineered crops,
it should be possible to manufacture feeds that contain the
particular protein and lipid requirements of marine piscivo-
rous species (Current Focus).
n- 3 fatty acids (Sathivel 2002), and it is now com mon
practice to integrate fish offal products from the process-
ing industry into the feed admi nistered to Pongosius cat-
fish. However, in certain parts of the developed world,
such as Europe, there is an illogical squeamishness about
feeding recycled body tissues to the same species, w hich
no doubt stems from the feed-related disease outbreaks
tha t occu rred in terrestrial livestock. Unlike terrestrial live-
stock, many carnivorous fish species are nat urally can-
nibalistic.
In addition to fish, other marine biota may produce suf-
ficient n-3 HUFA to provide a viable alternative to fish oil.
Recent studies have examined the potential of unicellular
algae, copepods, and benth ic invertebrates. In particular,
the cultu re of Co/anus finmorchicus generated sufficient
n- 3 HUFA to adequately replace fish oil in the diet of cul-
tu red Atlantic salmon (Olsen et al. 2004). However, the
cultivation of copepods in sufficient quantities to replace
fish oil remains uneconomically feasible at present, but
could be a promisi ng possibility at some poi nt in the
future. The use of unicellular o rganisms also offers the
possi bility of using gene manipulation to produce strains
tha t will generate commercially viable quantities of n-3
HUFA. The use of unicellular algae would be energetically
more efficient that cultivating copepods because there is
one less energy transfer step in the process (sunlig ht-
algae vs sunlight-algae-copepods).
Even once the above issues have been reso lved, there
are other considerations that may affect the future desi r-
ability of farmed fish fed alternative diets wi th lower lev-
els of fish oil. One of the strongest marketing messages
attached to fish-related products are the health advan-
tages conferred by eati ng fish, many of w hich are related
to its high n-3 HUFA content. A reduction of the latter
in the final product could detract from its marketability.
Conversely, a red uct ion in the use of fish oils would likely
decrease the likelihood of bioaccumulation of polychlori-
nated biphenyls and related co mpounds in the tissues of
farmed fish. It is clear that the issue of findi ng an accept-
able replacement for fish oil in the diet of cultivated fish
is a key issue if we are to make the necessary prog ress
to max imize the future potential of marine fish cultivation
as a signi fican t sou rce of dietary protei n.
 Chapter 14 Aquaculture
Aquaculture is often dependent upon feeds produced
from fish at low trophic levels, such as sandeels and
anchovies, which have high fish-oi l content. These 'fish-
eries to feed fish' are themselves a major environmental
concern.
In terrestrial systems, the domestication and farm-
ing of animals has centred on cattle, pigs, sheep, goats,
chickens, turkeys, geese, and duck. The restricted range
of farmed species means that technology is easily transfer-
able between species in terrestrial systems. This restricted
range ofspecies contrasts sharply with the hundreds offish,
mollusc, crustacean, and, latterly, echinoderm species that
have become the subject of widespread cultivation. The
diversity of farmed marine species makes their cultivation
an exciting though onerous area of research, as the indi-
vidual requirements of such a wide range of taxa require
specific research effort.
A much greater range of animal species is cultivated in
marine systems compared with land-based systems. The
diversity of cultivated species in marine systems greatly
increases the research burden necessary to bring these
species to commercial levels of production.
Algae and bivalve molluscs are among the most attrac-
tive candidates for cultivation, as these are the most effi-
cient in converting energy into biomass that is available for
consumption, and they are ranked second and third behind
finfish in terms of tonnes of production (Fig. 14.2) . Algae
produce sugar and starch through the process of photo-
synthesis. hence, provided water clarity is sufficient and
there are adequate nutrient supplies in the water column,
little input is required by the cultivator (Chapter 2) . Bivalve
120
90
~
•00
.e0 60
••
-••
0
0
30
.,
~
0
0 of world aquaculture production. both in terms of tonnage
s
~
iE-30
-60
1950 1960 1970 19BO 1990
Year
r-... Food fishsupplies fromoquowlture
Food fishsupplies fromrupturefisheries
Non-food uses
Figure 14.1 Ut ilization of fish supplied from wi ld capture
and aquaculture sources in terms of fish used for human
consumption or fish used for no n-food uses, e.g. fert ilizer,
fuel. Source: FAD (2007).
molluscs are filter feeders and feed on naturally occurring
phytoplankton in the water column and convert this to
body tissue. Again. little or no input is required to provide
sufficient food for the cultivated species, although care is
needed to ensure that bivalves are not overstocked to the
extent that the carrying capacity of the local environment
is exceeded. In contrast, most fish and crustaceans feed on
animals higher up the food chain; hence overall energy con-
version efficiency is reduced (Box 14.2) .
Carrying capacity is the amount of biomass that can be
supported in terms of oxygen and food requirements by
a particular volume of water. Once the carrying capac-
ity of a system is exceeded, the effects of competition
will increase density-dependent mortality and possibly
water quality.
To date approximately 300 species are cultivated across
all aquatic systems. Of these. 20% are carnivorous. but
these yield only 10% by weight of all production. How-
ever. carnivorous species tend to be those most prized by
gourmets and consequently they command high prices per
unit weight and contribute 40% ofall aquaculture revenue.
Although herbivorous and omnivorous fishes (e.g. tilapias
and carps) continue to account for the majority of global
fish production, they still command a relatively low price
per unit weight. Nevertheless, they are the best subjects to
fulfil basic world food-requirements as they do not require
sophisticated cultivation systems and are inexpensive to
rear. They also tend to be species that are highly tolerant
of high stocking densities and low dissolved oxygen levels.
Thus. in a world with an ever increasing human population,
these are the fish that are likely to meet the future demands
as a basic source of high quality dietary protein.
While herbivorous and omnivorous freshwater fish con-
tinue to dominate world fish aquaculture production in
terms of biomass, carnivorous fishes continue to com-
mand the highest per unit we ight financial value.
To this day, freshwater fish form the largest component
and financial value (Fig. 14.2) . For fish production, it is
apparent that freshwater and diadromous (e.g. salmonids)
fish products remain the dominant sector of the market.
2000 2007 while in the marine and brackish water sectors, molluscs.
algae. and crustaceans dominate (Fig. 14.2) . However.
freshwater fish products are. in general, relatively low value
per unit of production compared with marine fish products,
which are worth at least three times as much as freshwa-
ter equivalents (Fig. 14.2) . However. marine products are
more risk prone and hence costly to produce. as the marine
sector of aquaculture remains an emergent industry (FAO
2002) .
 14.3 How do we produce food from the sea?
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

1·1
30000
Box 14.2: Conversion efficiency . 1998
2\ 000 2007
Conversion efficiency refers to the passage of • 20000
energy through food-chains and webs and is dis- ,
-e
~ 15000
~
cussed in Chapters 4 and 7. As one organism
consumes another, energy is used to create body 10000

tissue, for metabol ism and reproduction, wh ich \000

results in net energy loss. Some organ isms are more 0
efficient at converting one form of organic mate- MiS(eliollE!oUl Morine DiodromoUl (rUlta(e<lns Molium Algae freshwater
aQuatic fi,hes fishes fish
rial into another, but the net result always results animals
in energy loss. As more and more links are added Ibl
3\ 000
to a food chain, so the process of the conversion . 1998
30000 2007
of energy (J) into body mass becomes less and
less efficient. Hence the conversi on of light into 2\ 000
•
the tissue of plants is the most efficient process, ~ 20000
while the food chain that links microalgae to large 1\ 000
carnivorous fishes , such as sharks, is one of the 10000
most ineffici ent. In contrast, the produ ction of edible \000
protein from bivalves is highly efficient as there are 0
only two steps in the process (sunlight-microal- MiS(eliollE!oo1 Morine Diodromau1 (rUlta(e<lns Molium Algae freshwater
aQuatic fi,hes fishes fish
gae--bivalves) . animals

Figure 14.2 (a) Global annual production (10005 tonnes)

14.3 How do we produce food
from the sea?
The production of marine species spans the spectrum from
the relatively unsophisticated release of species into natu-
rally enclosed systems, where they derive their nutrition
from n atural sources (extens ive cultivation) , to the highly
soph isticated and controlled cultivation and high density
stocking of species in totally enclosed intensive-recircula-
tion systems. Extens ive systems are typically based upon
brackish water coastal lagoons that have high levels of pri-
mary production in the form of phytoplankton or algae,
which stimulate the production of high numbers of food
organ isms required by fish or prawns that are released
into these systems . Another example of extens ive cultiva-
tion would be the deposition (known as relaying) of the
seed of bivalve molluscs harvested from the wild in areas
with enhanced productivity and easier access for harvest-
ing. The productivity of extens ive systems can be further
enhanced by the additional input of nutrients or fertiliz-
ers (e.g. the input of animal faeces). Production may also
be enhanced with some hum an manipulation of feeding
regimes or stocking density and species' composition. As
soon as human intervention is involved in the cultivation
process it is deemed to be semi-intens ive. Intensive systems
are typified by high stocking densities and usually require
the use of artificial feeds that are dosed with vitamins and
of different groups of marine taxa for 1998 and 2007
showing the dramatic rise in production over a 10-year
period. (b) Global annual first sale value (US$1 0000005)
of different groups of marine taxa for 1998 and 2007
showing the dramatic rise in value over a 1O-year period.
Source FAO 2007.
antibiotics to ameliorate the effects of disease and stress,
which are symptomatic of high stocking density. These sys-
tems are also subject to close environmental control (often
using computerized systems) and require constant moni-
toring (Allsopp 1997).
Extensive cultivation systems rely on primary production
to fuel the growth of cultivated species, whereas inten-
sive cultivation systems require sophisticated monitoring
and environmental control.
As in terrestrial agriculture systems , monoculture is
typically undertaken in developed countries and generates
the greatest income within the marine aquaculture sector.
Monoculture is attractive to farmers because it requires
investment in a limited range of equipment and food, and
simplifies marketing of the product. Monocultured species
tend to be those that are tolerant of high stocking densi-
ties; however, outbreaks of disease are the greatest threat
to monoculture systems, as the organisms are often much
more vulnerable to infection due to their suppressed immu-
nity resulting from elevated stress levels. Alt hough the con-
 Chapter 14 Aquaculture
CURRENT FOCUS: Fish welfare and
aquaculture
The environ ment in which fish are cultivated is artificial,
and, by necessity, the fish are held at high stocking den-
sities to provide the greatest yield pe r unit of energy
expended and to maximize financial profitability. Exam-
ples of extensive cultivation in which fish are allowed to
grow in semi-natural conditions are unusual. High stock-
ing densi ties can lead to increased aggressive behaviou r
among fish (leading to fin-nipping), a g reater prop ensity
to transfe r parasites among individuals, and intense inputs
of organic pollutants (faeces and uneaten feed) in the
vicini ty of the farm, which reduces wa ter quality. All of
the latter elevate stress levels in fish, which make them
more suscepti ble to pathogens. Fi nally, the fish need to
be slaughtered efficiently, w hich will involve further physi-
ological stress as the fish is removed f rom its environ ment
prior to slaughter. Each of these facto rs can ulti mately
red uce the quality of the product and hence the price it
attracts at market. As a result , there has been a strong
financial incentive for the aquaculture industry to invest in
research that has sought to mini mize t he negat ive physi-
ological responses that are associated with husbandry or
the envi ronment in w hich the fish live.
Definitions of welfare
Since the earl y 1990s, the scientific interest in issues that
relate to fish welfare has been reflect ed in the steady rise
of publications focused on aspects of this topic. Fish wel-
fare is complex and controversial and is well-reflected in a
recent spate of pape rs wi th divergent views on the sub-
ject (e.g. Hunt ingfo rd et al. 2006, 2007; Arlinghaus et
al. 2007). A function-based definition of welfare woul d
suggest tha t an animal's w elfare is good if it has adapted
to its environment, and is in good healt h and biological
function. An alternative nat ure-based defini tion of good
welfare would relate to the ability to lead a natural life with
the exp ression of behav io ur as observed in the wild. A
feeling s- based approach would define good welfare as
the conditions in which an animal is free of negative expe-
riences such as pain, fear, and hunger, and has access
to posi tive experiences, such as soci al companionship
(Hunt ingford & Kadri 2009). The above definitions are
developed from an anthropocentric point of view, and the
reader should be aware that it is difficult for humans to
develop a perspective on what a fish (or any othe r animal)
experiences, and hence wh at is or is not acceptable (fo r
a philosophical perspective on these issues see: Evans
2009; Sandee et al. 2009). The issue of welfare is inevi-
tably vulnerable to 'belief-based ' assertions, w hereas the
scientific approach demands a dispassionate examination
of the evidence surrou nding welfare issues.
The definition of welfare is important because it deter-
m ines how we measure perfor mance agai nst specific
objectives. For example, assessing the behavioural rep-
ertoi re of far med fish compared to thei r wild cou nter-
parts would be appropriate if a nature-based definition
of w elfare is adopted. In contrast, measu rement of physi-
ological status or growth rate would be appropriate if
using a function-based definition of welfare. Once per-
formance metrics have been identified, it is possible to
target research to improve particular aspects of a defined
attribute of welfare. However, if good welfare requires
fish to lead a completely nat ural life, aquaculture (or any
other kind of farmi ng) can never meet such a defini tion
of welfare.
What has the industry done about fish
welfare?
There exist already guidelines and legislation wi thin which
the aquacultu re industry must operate in certain parts
of the world. These guidelines address a proportion of
issues that fall under a 'welfare ' heading. Outside these
commitments, there are other initiatives th at are closely
tied to improving profitability. Fish th at are in poor con-
dition, diseased, and heavily parasitized do not attract
buyers!
It is important to select the app rop riate species for
cultivation as some species, st rains, and individuals react
better th an others to intensive husbandry syste ms. For
example, fish that nat urally school at high densities are
more li kely to adapt to high density stocki ng conditions
t han speci es that are primarily soli tary and territorial.
Research on welfa re-friendly husbandry syste ms has
focused on specific aspects of the cul tivation process
th at include issues surrounding humane transport (e.g.
Iverson et al. 2009) and slaughter (e.g. Knowles et al.
2008), various systems for feedi ng fish according to their
current appetite (e.g. Noble et al. 2008), and passive
size-g rading (e.g. Pfeiffer & Freeman 2004) . The devel-
op ment of welfare indicators that are easily measured can
be used to reflect general fish welfare and these would
include food intake, fin condi tion, and water quality. How-
ever, as product quality is related to the price paid in the
supermarket, there is probably a strong link between fish
welfare indicators and the average income of the target
market.
 14.4 What is cultivated and where?
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
ditions in which fish are cultivated lead to highly efficient
production. this artificial environment raises issues relating
to the ethics of animal welfare (Current Focus: Fish welfare
and aquaculture) (Fig. 14.3) .
Monocu lture yields the highest financial income but is
prone to outbreaks of disease, environmental , and ethi-
cal issues.
Polyculture tends to be practised in countries with less
well-developed economies and is often associated with
subsistence farming or fishing. However, more developed
countries are beginning to realize that the cultivation of
'companion' species can increase both production and
income. and often alleviates the need for the use of expen-
sive chemicals or maintenance. For example, sea urchins
Psammechinus miliaris are used to graze fouling algae off
the nets ofsalmonid cages while yielding their own produer
(sea urchin gonads) (Ross et al. 2004) . Some of the best
examples of polyculture come from freshwater systems in
which carp. tilapia, or crustaceans are cultivated. In this
case the aquatic organisms are cultivated in combination
with plant or animal husbandry. For example, tilapias are
farmed from rice-paddies. or domestic animals housed in
enclosures suspended over cultivated ponds enrich the
water with their faeces. Those species best suited to this
form of culture tend to be either herbivorous or consume
prey low down the food-chain (i.e. zooplankton or arthro-
pod grazers) .
Polyculture is usually practiced with species that feed
lower down the food-chain, although there is increasing
interest in the use of companion species that provide
cleaning services that would normally require the use of
chemicals or human husbandry.
14.4 What is cultivated and
where?
Historically, the majority of aquaculture has developed in
freshwater environments, which probably refleers the lim-
ited nature of the natural resource and also the perception
that the cultivated species are unable to escape an enclosed
body of water (Figs 14.1 and 14.2). This contrasts with the
reluctance of mariculturists to explore the possibility of
ranching due to the inability to contain released individu-
als. Freshwater aquaculture continues to dominate world
production of aquatic animals with 30 million tonnes pro-
duced in 2006 (FAD 2008) . In addition to this a further 1.9
and 10.8 million tonnes were produced in brackish and
marine waters. respectively. In addition to animal produc-
tion, a further 15.1 million tonnes of aquatic plants were
produced in 2006, of which 99.8% were cultivated in
marine waters (FAD 2008).
Go to http:/ /www.fao.org for the latest facts and figures
for world aquaculture production.
Production is dominated by countries in Asia. China is
by far the world's leader in terms of overall production,
with 35 million tonnes of food fish produced in 2005 . The
relatively low value per unit production is due to the domi-
nance of low-value cyprinids (carp and their relatives) in
the Chinese aquaculture sector. This contrasts sharply with
Japan's production of O.77 million tonnes, which was val-
ued at US$3.06 billion, comprising of high-value species,
such as scallops, oysters, and amberjacks. Within the last
decade, the low-income food deficit countries have main-
tained an upward trend in production due to their active
promotion of aquaculture as a means of subsistence. How-
ever, in contrast to areas such as Asia and South America.
Africa has been slow to develop its potential for aquacul-
ture, despite considerable investment. Production in Africa
has risen at a rate of 12% per annum since 1970 to the
present day, but this is approximately half the rate of most
other areas.
While Asia and Central America have expanded marine
aquaculture rapid ly, Africa is yet to realize its fu ll poten-
tial, despite extensive water resources in the sub-Saharan
region. The main bottleneck remains economic infra-
structure in many states that continue to be bli ghted by
political governance challenges. Sadly, the situation has
changed little in the five years since the publication of
the first edition of th is book.
Although nearly half of all aquaculture production is
composed of finfish, more than 90% of this fish produc-
tion is derived from freshwater systems. The remainder of
the production is divided mainly between plants and mol-
luscs. Crustaceans contribute approximately 5% to world
production in terms of weight but their economic value is
considerably more than this (Fig. 14.2) . The cultivation of
salmonids is so successful that production has overtaken
the amount offish generated by salmonid wild-capture fish-
eries. The 'farmed salmon' is lovingly known as the 'chicken'
of the sea because ofits dominance offish counters in West-
ern supermarkets.
However. as we will see later. the proliferation in sal-
monid production has led to a plethora of environmental
problems. Cultivated marine fish species are exclusively car-
nivorous species that command a high market value . Bass
(Dicentrachus labrax), sea bream (Sparidae), and turbot
(Psetta maximus) are now commonly cultivated throughout
 Chapter 14 Aquaculture

Box 14.3: Cultivation of southern

bluefin tuna

Harvesting southern bluefin tuna from holding pens is

a delicate operation to ensure that the fish are main-
tained in pristine condition . Any damage to the fish
will ultimately lower their value at market. As soon as
the fish are harvested , they are returned for imme-
diate processing and shipping to markets in Japan.
Photograph reproduced with the permission of the
Tuna Boat Owners of South Australia/Australian Fish-
Figure 14.3 Fish that make ideal subjects for ing Management Authority.
aquaculture are tolerant of high-density stocking
levels, but high-stocking densities inevitably lead to
physiological and behavioural problems. These sole So/eo
so/eo are prone to caudal fin damage, as they instinctively
try to bury themselves into the base of the rearing tank.
Technological advances in feed and rearing systems mean
that many fish species are now much less expensive to
produce than wild-caught fish.

southern Europe, where warm waters promote high growth

rates. Humans will go to real extremes to cultivate some of
the most prized fish species (Box 14.3).

Carnivorous species are favoured for marine aquacul-

ture and they command higher prices than herbivorous
species. However, herbivorous species of fish represent
the means to produce high-quality protein in the most
efficient manner with least reliance (none in some cases)
on wild-capture fisheries for feed .

Red and brown algae are cultivated in substantial quan-
tities with 14. 8 million tonnes cultivated in 2005 worth
US$7. 1 billion. Red algae are somewhat more valuable
than brown algae as they are produced for food consump-
tion, where as brown algae (mostly kelp species) supply
the alginate industry. Nearly all cultivated mollusc species
Undertaking research on methods to improve the
growth of southern bluefin tuna is an expensive
undertaking, when each fish is valued in US$1000s.
Here, scientists measure the dimensions of a fish.
(Photograph: Brett Glencross.)
 14.5 Food requirements and constraints
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
are bivalve molluscs of which mussels contribute most in
terms of production, followed by oysters, clams, and scal-
lops (Table 14.1). Although in many cases bivalves com-
mand a relatively low price per unit product, they require
no investment in feeds or antibiotics, and hence produce
a much lower environme ntal footprint compared to pro-
duction of marine finfish. The cultivation of crustaceans is
largely based on penaeid shrimp (89% by weight of fresh-
water and marine global production) , which are currently
valued at approximately U5$5 billion per year at first sale.
Although a high-value species, shr imp are costly to pro-
duce and their cultivation has been associated with envi-
ronmental degradation of coastal margins and widespread
disease outbreaks.
Alginates are derivatives of marine algae that are used
in everyday products ranging from shaving foam to food-
thickening agents.
Southern bluefin tuna are captured hundreds of kilo-
metres out to sea and then transferred to holding pens
close to the coast where they are conditioned prior to
processing. Bluefin tuna are among the world 's most
endangered fish species, and trade in Atlantic bluefin
tuna was banned by the European Union in 2010.
14.5 Food requirements and
constraints
In marine plants, good growt h will be achieved with suf-
ficient light, oxygen, carbon dioxide, and nutrients. Over-
stocking marine plants will lead to competition for all of
these resources and will yield lower production per kilo -
gram of plant mass. In terrestrial systems, domesticated
herbivores convert vegetable matter into highly desirable
protein products. This contrasts sharply w ith aquatic sys-
Table 14.1 World aquaculture production in 1999 of the six most important marine species in terms of
production (tonnes). The value (US$1000s) of each of these species is also shown. The relative value per unit
product is shown as the ratio of the value to total production. Statistics reproduced from the FAO (2002).
Species Common name
Crassostrea gigas Pacific oyster
Ruditapes phifippinarum Manila clam
Patinopecten yessoensis Scallop
Penaeus monodon Prawn
Mytifus edulis Mussel
Chonos chonos Milkfish
-
terns in which only bivalves and gastropods convert phy-
toplankton, particulate organic matter, and alga e into
high-quality protein. In contrast, herbivorous fish are low-
value (but high production) species. Cultivation of high-
value carnivorous fish, crustacean, and mollusc species
dep ends upon a dependable and consistent high-qu ality
protein diet. Artificial feeds are the staple diet of most cul-
tivated carnivorous species, but these still depend on fish-
meal derived from low-value by-catch species for their
protein component. Half of the production costs for salmo-
nids and Asian shr imp production is spe nt on artificial
feed (New et al, 1993). The idea of catching fish to feed to
fish (or terrestrial animals) is increasingly controvers ial
(Naylor et al. 2000), as well as energetically inefficient
(Pitcher & Hart 1982; Box 14.2). As a result, there is great
interest in the development of artificial feeds based on
plant-derived protein (Curre nt Focus: The catch-22 of
aqu aculture).
Finding a viable replacement for the 'fish ' component
in artificial feeds for carnivorous fish species is a key
bottleneck in expanding aquaculture further. Once the
link between wild-capture fisheries and aquaculture can
be severed , it is likely that aquaculture will dominate
world fish production.
Artificial diets based on the protein derived from soy-
bean, lupin, and canola (a type of rapeseed) appear to
yield acceptable growt h rates and are half as cos tly to
produce. Plant-based feeds offe r benefits in add ition to
cost savings. Plant crops are more reliable than the wildly
fluctuating stocks of small pelagic fishes used for fish-
meal, the nutrient composition is more easily controlled,
and the shelf-life of plant-based feeds is su pe rio r. With
the current trend for ret ailers to offer sustainable prod-
ucts wit h ingredients that can be traced to source, plant-
based feeds offer a much simpler solu tion in terms of
product tracking. Another consideration is the potential
to introduce pathogens through imports of feed. Frozen
Production Value Ratio
3600459 3 3 127 13 0.92
18204 13 2194522 1.21
9 28724 12 524 48 1.35
575842 36 5 1783 6.34
498461 2 72419 0.55
38 1930 599957 1.57
 Chapter 14 Aquaculture
pilchards imported from South America and then fed to
farmed southern bluefin tuna kept in suspended fish cages
(Box 14.3) introduced a virus which then infected South
Australian stocks of pilchard and caused high mortalities
(Thorpe et al. 1997) .
Plant-based feeds are seen as the future for more sus-
tainable farming of marine carnivores (see Current Focus:
The catch-22 of aquaculture).
14.6 The role of biotechnology
The production per unitvolume ofwater ofmarine aquacul-
ture systems has increased with biotechnological advances.
Often the species that have the highest unit value are the
most demanding in terms of husbandry or dietary require-
ments. For example, halibut (Hippoglossus spp.) require
very cold water at elevated pressure for their eggs to hatch,
after which the newly emerged fish larvae are particu-
larly problematic to wean on to artificial feeds. In another
example, the formulation of an appropriate pellet feed is
currently a major problem for the cultivation of southern
bluefin tuna in South Australian fish farms, partly due to
the expense of having a laboratory subject with a price tag
ofUS$1000s per individual (Box 14.3).
Cryopreservation enables gametes to be stored until
they are required and li berates hatcheries from the need
to condition male fish synchronously with female brood-
stock.
Biotechnological advances have enabled the cryo-
preservation of viable gametes. which has eliminated the
breeding constraints associated with species that have sea-
sonal reproductive cycles and ensures a reliable supply of
larvae year round or when conditions (biological or eco-
nomic) are most favourable. This is particularly important
for markets in developed countries where retailers expect
a predictable source of products throughout the year. Con-
trolled sex differentiation has enabled the production of
sexually sterile fish. This can be achieved by a number of
techniques, including the induction of triploidy in female
fish, that yield monosex stocks of fish. Sexually sterile fish
put more energy into tissue growth (soma) and yield a
greater proportion of consumable tissues at market size.
Fish with suppressed gonad maturation will not develop
manyofthe behavioural traits (i.e, elevated levels ofaggres-
sion) that occur with the onset of maturity and spawning
condition. Genetic selection has been used to reduce head
and fin size. This helps to further reduce waste in the final
product. Artificial diets now include growth stimulants that
improve feed-conversion rations. They are often dosed with
antibiotics to reduce the risk of infection in intensive finfish
and crustacean aquaculture systems. Finally. in common
with terrestrial farmed systems, marine organisms are now
the subject of trials using recombinant DNA methodologies
to produce fish with altered body shape and size charac-
teristics.
For more information on genetically modified fish go
to http://www.ems.org/salmon/genetically_engineered.
htrnl.
14.7 Negative effects of
biotechnology
Biotechnology has certainly helped to improve our abiliry
to cultivate marine organisms more efficiently and to pro-
vide better quality products. However. there is consider-
able concern regarding the deleterious effects of escapees
of normally farmed fish and, latterly, genetically modified
organisms. The genetic diversity of wild stocks is threat-
ened byescapes and accidental releases of hatchery-reared
individuals that can competitively exclude wild fish. A
reduction in genetic diversity has the potential to lower
resistance of wild stocks to environmental change and
pathogens. This issue has been particularly prominent in
the salmon industry of North America. Large-scale hatch-
ery release programmes have been undertaken to coun-
ter the effects of habitat loss and overfishing. However.
hatchery-reared fish compete with the existing wild fish
for habitat and food, prompting Hilborn (1992) to argue
that large-scale hatchery programmes for salmonids in
the Pacific North-west posed the greatest single threat to
the long-term maintenance of salmonid stocks (but for a
recently revised opinion see: Hilborn 1999) . The issue of
escapees is largely a problem for cage-based cultivation
systems that are located within the marine or freshwater
environment. However. this problem could be eliminated
entirely if cultivation systems were moved into land-based
cultivation systems in which discharges ofwater are strictly
controlled (see Section 14.11) .
Large-scale releases of hatchery-reared fish int o the
w ild are perceived by some to pose one of the great-
est threats to the long-term maintenance of salmonid
stocks.
Artificial feeds are a convenient means for administer-
ing medication to captive organisms. Although the use of
antibiotics reduces infection rates in intensive cultivation
systems, their excessive use can lead to a build-up of drug
resistance in the pathogen. As uneaten feed accumulates
on the seabed beneath fish cages, the encapsulated anti-

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
biotics can affect microbial communities in the immediate
vicinity, leading to a reduction in their diversity. Additional
concerns associated with the use of antimicrobials in fish
feeds include: the spread of drug-resistant plasmids to
human pathogens; transfer of resistant pathogens from
fish farming to humans; and presence of antimicrobials in
wild fish.
Encapsulated feeds can lead to the release of large
amounts of antibiotics into the marine environment with
the potential to alter microbial communities in the envi-
ronment immediately surrounding the cultivation site.
14.8 Cultivation systems
Terrestrial farmers need to contain and protect their live-
stock and crops using enclosures and barriers. Equally.
mariculturists need to ensure that their livestock is secure.
Mobile biota (e.g. fishes, snails, shrimp) have different
containment requirements to those that are sessile (e.g.
bivalves. algae) . Semi-enclosed coastal water bodies. such
as lagoons and saline ponds. provide naturally enclosed
or semi-enclosed culture systems. However. these coastal
resources are limited, and often they are associated with
a unique fauna that may be of conservation interest.
such that they clash with the needs of the aquaculturist.
Shrimp cultivation in Central America and Asia has led
to the creation of artificial coastal ponds in areas where
there formerly existed mangrove forests. These ponds
need to be in close proximity to seawater so that the pond
water can be exchanged on a frequent basis. However.
the coastal margin is a finite resource and the demand for
space has resulted in such a high density of shrimp ponds
that the effluents from one pond have contaminated the
intake water of the adjacent pond . Not surprisingly, this
has resulted in a severe reduction in coastal water quality
and serious outbreaks of disease that have caused entire
shrimp harvest failures. We will return to this subject later
in the chapter.
The use of natural ponds and lagoons is usually asso-
ciated with extensive culture or semi-intensive culture.
Often, wild juveniles may be captured and released into
the ponds to on-grow by feeding on the natural food within
the pond. Alternatively, hatchery-reared juveniles are
released into the ponds in conjunction with supplemental
feeding or enhancement of pond productivity using natural
or artificial fertilizers . The stocking density of natural and
semi-natural pond systems has to be monitored carefully
to avoid exceeding the carrying capacity and oxygen sup-
ply within the system. In some cases. additional aeration
of the pond water is undertaken using paddle aerators or
14.9 Cultivation of fish in cages
by pumping air directly through air-blocks located in the
base of the pond.
The coastline is a fi nite resource and the excessive devel-
opment of coastal aq uaculture has led to a reduction
in coastal water quality in some regions, particularly in
central America and Indonesia
14.9 Cultivation of fish in
cages
Ponds and lagoons do not permit farmers to maintain close
control of their stock; they are less easily maintained and
disease problems are not so easy to treat. Suspended cages
provide an excellent means of retaining the cultivated spe-
cies in open well-aerated seawater. while liberating farm-
ers from the constraint of limited coastal pond resources.
Suspended fish cages are used in all aquatic systems. Essen-
tially, they consist of a large net bag with buoys at the top,
which is anchored to the seabed using anchors and chains
(Fig. 14.4). Nevertheless, suspended cages are themselves
limited to coastal areas that are sheltered from adverse
weather conditions and are within a short distance of the
shore for ease of maintenance. For this reason. the great-
est concentration of caged fish farming tends to occur in
coastal fjordic systems (sea lochs, rias, inlets) that provide
natural shelter from wind and wave action. Such areas are
only found in a limited number of locations in a particular
country, and many countries lack such an environment.
The most prolific producers of suspended-cage farmed fish
include Norway, Scotland, Canada, New Zealand, Chile,
and Greece . All of these countries have complex coastlines
that are either riddled with inlets or fjords or have a high
number of offshore islands that provide natural shelter.
Once again the limited nature of the coastal resource has led
(in the past) to over-expansion of this sector of the industry.
with high densities of fish farms developing within these
semi-enclosed water-bodies.
Suspended-cage culture is usually confined to coastal
areas that are sheltered from adverse weather conditions
by the morphology of the coastline.
This has led to problems with carrying capacity in sys-
tems in which the exchange of water is reduced in com-
parison with open coastal systems (Gowen & Bradbury
1987; Black & Truscott 1994) . Single, isolated fish farms
will increase the demand on oxygen supplies in the sur-
rounding water; they will reduce current flow beneath the
fish cages and increase the supply of organic matter to the
seabed. Typically this increases the physiological stress
 Chapter 14 Aquaculture

TIdal current

• •
• •
• • • •
• • •
• •
• •
• •
• •
• •
• •
Faeces and food pellets • • •
• •• •

Anoxic area of seabed beneatth cage

Figure 14.4 A typical suspended fish cage showing t he buoys on the surface of the sea, the anchor ropes, and the
zone beneath the cage that will be affected by falling uneaten food pellets and fish faeces. A build-up of organic matter
beneath t he cage can lead to anoxia and an impoverished benthic fauna. In extreme cases of organic pollution, only
bacterial mats persist beneath fish cages. The presence of the cage and the ropes that anchor it to the seabed will
increase friction and hence the turbulence of the flow of water around the cage. This will tend to cause a zone of lower
velocity water beneath the cage that will further concentrate faeces and uneaten pellets as they fall through the water
column. A proportion of the solid particles will be carried downstream by the prevailing tidal currents, leading to zones
of decreasing organic enrichment around the cage.

on the benthic community beneath the cage and leads to water column have been linked with outbreaks of toxic algal
a reduction in species' diversity or. in extreme cases. the blooms and mass fish mortalities (Smayda 1990).
elimination of all macrobenthos, which are then replaced
by bacterial mats of Beggiatoa spp. (Pearson & Rosenberg Depending on their size, when fish farms occur in isola-
1987; Chapter 15) . tion they have relatively little effect on the wider envi-
ronment.
In cases of severe organic enrichment, benthic communi-
ties that are found beneath fish cages can be replaced by
mats of bacteria. However, management practices have
improved such that organic waste from excess feed has
been reduced greatly and cages are moved regu larly to
enable systems to undergo a period of recovery.

When farms occur in isolation it is relatively simple to

alleviate the environmental problems by moving the loca-
tion of the farm to allow the affected seabed to recover over
a number of years (Fig. 14.5) . However, some enclosed
water bodies have been overpopulated with fish farms,
which have magnified the adverse effects of cage farming
and eliminated the possibility for simple management solu-
tions to the associated problems. Typically. these systems
have been associated with greatly reduced dissolved oxygen Figure 14.5 Isolated fish farms are less likely to cause
concentrations in the water column, which has increased severe environmental effects than large concentrations
stress levels for the fish and increased their vulnerability of fish farms in enclosed water bodies. (Copyright: US
to disease outbreaks. The environmental changes in the National Oceanic and Atmospheric Administration.)
 14.10 Cage cultivation: a lousy system?
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
14.10 Cage cultivation: a
lousy system?
Intensive cultivation of any species is likely to encourage
the rapid spread of d isease or parasites . It is not surprising
then that sea lice infestations are common in most coastal
areas in which marine salmonid aquaculture occurs. Sea
lice (Lepeophtheirus salmonis) are isopod parasites that feed
on the blood of marine fishes. In salmonids, a parasite load
of only 10 sea lice can lead to mortality of the fish as they
migrate to sea. As cage-farmed fish are held in high den-
sity, the de nsity of sea lice within the vicin ity of the cages
is also high. Concern has been raised that wild mi grating
salmon ids (salmon and sea trout) are more suscepti ble
to infestation as they pass close by salmon farms that are
found on their mi gration route. Th is potential for elevated
infestation rates has been linked by some to the decline in
w ild salmon id populations and h as the potential to affect
other salmonid species (Bjorn et al. 2007)
TECHNIQUES: Using cleaner-wrasse to
remove salmon lice
Sal mon farming is par ti cularly important in Northern
Europe which supplies 5 3% of the w orld market at pres-
ent (FAO 2007). The majority of these fi sh are culti-
vated in cages located in coastal areas t hat are sheltered
from adverse weather con ditions. Salmon are vulnerable
to att ack by sea lice, wh ich reduces t he qual ity or even
kill s the fish if the infestati on is heavy enough. Chemi cal
treat ments to remove the sea lice are associated w it h
concerns regarding bi o-accumu latio n of th e chemicals
in the final sal mon produ ct whi ch are then passed onto
humans although this is strictly monitored in some loca-
t ions. In add ition, th e excessive use of chemicals in some
local ities has led to the development of resistance that
necessi tates the developm ent of new chemicals or the
use of increased doses of chemical treatment. This con-
stant battle to eradicate sea lice in sal mon farmin g is
costly and potentially damaging to the immediate environ-
ment around th e fish farm due to bio-accumu lation and
persiste nce of some chem icals such as dichlorvos.
Intensive research effo rts have been made to exam-
ine th e uti lity of so-called 'cleaner-wrasse' and attent ion
t urned first to try and utilize t he gol dsinny (Ctenofabrus
rup estris). However, the small body-size of these w rasse
means that they could escape from conventional salmon
nets and possi bly act as a vector for any fish pathogens
ingested by the sea lice cons umed during the 'cleaning '
process. As a result , co mmercial farm ers initially were
As in all intensive systems, cage-based aq uacultu re prac-
tices elevate the risk of t he ra pi d sp read of d isease and
paras ites.
The loss of fish stock to sea lice infestation led to the
development of che mical treatments that would kill the sea
lice. However, these were limited to two m ain treatments:
dichlorvos (an organophosphorus derivative now banned
for use in the fish aquaculture industry) and hydrogen
peroxide. The frequent and widespread use of these com-
pounds led to reduced efficacy caused by resistance that
developed in the sea lice. In more recent times, there has
been a tendency to look to biological control methods. How-
ever, the latter require intense research and initial a ttempts
to use golds inny wrasse (Ctenolabrus rupestris) led to con-
cern about their escapability and potential to act as vectors
of disease. However, recent technological advances mean
that the cultivation of the larger ballan wrasse, which is less
likely to escape from salmon nets, is now commercially fea-
sible (see Techn iques box) .
concerned that the w rasse could spread di sease and
parasites from one farm to another (Costello et al. 1994;
Gibson & Sommervi lle 19 9 6 ) . A simple sol ution to the
wrasse esca pee problem is to use smaller meshes on
the sal mon cage but t hese might impede w ater flow and
could also incur a greater biomass of fou ling biota on the
net meshes.
The solution might be to t urn attention to the use of
a larger body-sized wrasse species, such as the ballan
wrasse (Labrus bergyfta ) . However, the development of
a w il d-capture fishery for ballan w rasse would hardly be
a sustainable solution to provi ding the cleaner-wrasse
need ed for the sal mon industry, hence a new programme
of research to develop the scientif ic knowledge to rear
these fish on a commercially viable scale was required.
Below, aquacult ure specialist Anne Berit Skiftesvik, leads
us through the technological and scient ific challenges that
had to be overcom e to understand how to rear this fish
on a commercial scale.
What was the driver to focus on ballan
wrasse and not some other species?
It was known from anecdotal accounts that the w rasses
would pick lice off the sides of salmon. Therefore, early on
in the quest for the 'best' w rasse species to use, several
species were tested and the ballan w rasse (a) proved
its elf an effect ive lice-pic ker. Further, ballan wrasse
are large enough to be co-cult ured w ith large r salmon
(small er wrasse would be eaten by the salmon) and are
 Chapter 14 Aquaculture
large enough so that a reasonable mesh size can be used
in sea cages (the mesh size must be matched to the size
of wrasse used to prevent their escape; however, small
mesh sizes are not practical). Balian wrasse continue
to pick lice at lower temperatures than other species
(which greatly extends the geographic range over which
they can be used effectively, particularly northward).
Balian wrasse are also more robust than other species.
When considering a new species for
culture, what are the first things you need
to understand?
You need to know as much about thei r natural ecology
(and behaviour) as possible, particularly the ecology of
the reproductive adults and the early life-stages and the
physical environmen t that they live in. To accomplish
this for ballan w rasse, we undertook a series of projects
that aimed to characterize their spawni ng habitat and
their spawning behaviour in the wild (using underwater
video came ras). The information gained in these projects
formed the basis for our first attempts to cul ture the
species.
For ballan wrasse, what turned out to be
the major challenges to cultivating them
successfully and how did you solve them?
The amount of space that ballan requi red for their
spawning behaviour displays was difficult to assess
and was at fi rst underestimated (i.e. size of th e tank
and; water depth). The number of males in the brood-
stock holding tank must be matc hed to the space
available so that males can establish territories. The
fish must be provided wi th structure in which they can
hide (e.g. macrophytes simulated using shredded black
plastic garbage bags) . Wild brood-stock had to be given
enough t ime to acclimate so that they were not stressed
in captivity or by the frequent appearance of humans.
Artificial spawning substrata must be provided (e.g.
pieces of carpet) over which the adults can play out their
spawning dance and onto which the eggs can settle and
adhere. These artificial substrata must then be removed
from the brood-stock tank and placed in egg incubators.
The eggs must be removed from the tank because: ( 1)
larvae (b) would be flushed out of the brood-stock
tank and cannot be cul tured in that environment and
(2) if the eggs are not removed from the brood-stock
tank, the males will invest energy to protect them and
will not continue spawning (c). There proved to be a
minimum temperature below which egg development
was poor. Larvae of the ballan wrasse were qui te fussy
and required live feed for a relatively long time compared
to other marine species and a specially-formulated diet
was required at weaning to obtai n good survival results.
Larvae did not perform well in terms of growth and
 14.11 Breaking away from the coastal margin
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
survival under the fluorescent lighting typically used in
hatcheries. Better results were obtained when the larvae
were cultu red under natural light (i n a facility with a
transparent roof) an d later using lamps with a spectral
output that is closer to natural sunlight (note that ballan
wrasse eggs (d) are deposited in shallow illumina ted
w ater in the early summer).
Are there any other technical issues that
need to be overcome to make ballan
wrasse a viable proposition?
Reducing the duratio n of the period during which the
larvae require live feed woul d help to reduce the cost of
cultivation. Improving weaning success in the transit ion
fro m live feed to formulated diet. Improving the nut ritional
quality, taste, and palatabili ty of the formulated diet
(specif ic to th is species), as this would increase g rowth,
14.11 Breaking away from the
coastal margin
With the ever-increasing demands on the coastal margin,
the prospects for the expansion of suspended-cage culti-
vation is finite. This has led to research into alternative
technologies for intensive marine fish cultivation. Two
developments are most noteworthy: the development of
offshore automated fish cages and the development of
recirculation systems. Automated fish-cage systems are
a recent development in the last decade (Fig. 14. 6). The
essential features of these systems are that the fish are
fed automatically, they can be lowered to the seabed such
that they are beyond the effects of wave action and cause
less of a navigation hazard to shipping, and they can be
resurfaced for repair, maintenance, and har vesting (Dahle
1995) (Fig. 14. 6).
survival, and reduce waste. Improving the culture tank
environment so that it is better-suited to the specific
req uirements of ballan w rasse larv ae and early juveniles
(e.g. flow, depth, structure, shelter). If ballan w rasse are
to be used with salmon, the nets on salmon farms must
be kept much cleaner of fouli ng organisms th an would
norm ally be required. This is because the ballan w rasse
will, nat urally, eat the food that is easiest to get. Cleaner
nets encourage them to eat more sea lice.
Do ballan wrasse provide an effective
solution to the salmon lice problem?
Balian w rasse can be very effective in keep ing sea lice
infestation under control (particularly egg-bearing female
lice) th roughout the on-growing period-at a stocking
density of only 1 % that of the salmon. It is important to
emphasize here that w rasse are continuously eliminating
lice, w hereas other t reat ments are short-lived and
must be repeate d at regular interv als (which is much
more invasive and damaging to the salmon, and the
environment). The lice can never develop resistance
to this form of control (as they do to chemicals). Also,
w rasse can be used even if the salmon are ill or in poor
condi tion (a situation that makes the use of chemicals
impossible- that would result in mass mortality).
Nonetheless, w rasse must be viewed as one part of a
multi-pronged approach to controlli ng salmon lice (e.g.
some topical chemical treat ments; lice t raps; vaccination)
since t hey will never completely eradicate the parasite.
To find out more about offshore fish farm cultivation visit
http: / /www.oar.noaa.gov/ spot l itel archive/spot_hawai i.
html.
Recirculation systems present the most sophisticated
level of current aquaculture rearing techniques. Enclosed
tank and raceway systems have been used to cultivate
marine fish for a number of decades, but in the past they
have been restricted to coastal locations by the neces-
sity to pump a sufficient through-put of se awater. This
incurred costs, both from the pumping of water and, in
some cases, the need to heat it when warm-water species
were cultivated in temperate areas. With the developme nt
of recirculation systems, the cultivation of marine species
is no longer tied to locations adjacen t to the coast (Fig.
14.7). In addition, non-indigenous species can be culti-
vated as there is no risk of accidental introductions into
 Chapter 14 Aquaculture

(a) unit area by reducing stress induced by disease and water

contamination. Recirculation systems are divorced from
, [~~:!::I-Automoted feed unit__, the environmental problems associated with cage and
Buoy
pond cultivation, as the waste products can be collected
and disposed of in an appropriate manner and even used
as fertilizer. There is even the potential for diversification
An(hor ropes into areas such as hydroponics in which high-value plant
crops could be grown in conjunction with semi-recircula-
tion systems, such that they remove excess nitrogen and
Weight phosphorus products and yield a vegetable crop as a bonus
(Fig. 14.8) .
Seabed
(al . - - (bl

Figure 14.7 Recirculation systems (a) can be constructed

on land far from the sea, as they require minimal inputs
of fresh seawater and can be maintai ned using artificially
made seawater, if necessary. Land-based systems have the
advantage that they can be enclosed, which gives greater
potential for e nvironmental control (b). (Photog rap hs: M. J.
Kaiser.)

Figure 14.6 (a) A schematic of an offshore fish cage

as currently in use in the North Atlantic and the Gulf of
Mexico. These 1 5 m deep nets are entirely automated and
sunk to the seabed to avoid the effects of extreme weather:
Apart from occasional servicing and reloading of t he feed
hopper, they are relatively low in terms of maintenance
needs. (b) Moi swim near t he surface inside an offshore
aq uac ulture cage, (photo: NOAA). (c) SeaStation 3000
with feeding tube approximately 13m below the s urface
offshore of Honolulu, Hawaii (photo: NOAA).
Figure 14.8 A fine crop of salad greens growing on
the local environment. Such systems also have greater the waste products of aquaculture. Hydroponics has the
biosecurity in circumstances when genetically modified advantage of using natural plant growth t o remove excess
organisms are cultivated. The highly controlled environ- nit ro gen and phosphorous from cultivation systems.
ment of recirculation systems increases productivity per (Photograph: Kevin Fitzsimmons, University of Arizona.)
 14.12 Shrimp cultivation: the gold rush
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Recircu lation systems mean that marine species can be
cultivated almost anywhere. Any waste generated by
these systems can be remediated in biological fi ltration
systems and can also incorporate hydroponic cultivation.
14.12 Shrimp cultivation: the
gold rush
Shrimp are a high-value crop that is prized throughout the
world. The high by-catches (16 kg of by-catch for every 1 kg
oflanded shrimp) associated with wild-capture shrimp fish-
eries (Chapter 13) mean that their cultivation is an attractive
way of overcoming this adverse side-effect of the wild-
capture fishery. Once the technological difficulties in rear-
ing shrimp had been overcome, shrimp culture increased
rapidly in Asia and Central America. Consequently, shrimp
farming has become a multibillion US$ business world-
wide. However, uncontrolled and unplanned expansion in
the early days of the industry resulted in widespread crop
failures due to disease and poor water quality (Fig. 14.9) .
These chronic problems have arrested the further expan-
sion of shrimp aquaculture . Disease is mostly responsible
for recent production declines. Nowadays. shrimp produc-
tion is seriously affected by rapidly spreading viral epidem-
ics across the Asian region . Of the 20 known types of virus
that affect shrimp. the white-spot virus in Asia and Taura
Syndrome virus in the Americas are the most threatening.
Wild-capture shrimp fisheries yield high-value catches
but generate large by-catches of non-commercial value
and species of conservation importance (e.g. turtles, sea
snakes). Shrimp cu lture elim inates the environmental
effects of by-catch, but has led to its own environmental
problems.
In 1987, Taiwan was among the world's leading shrimp
producers with 115 000 tonnes of Penaeus monodon pro-
duced by small family-run intensive farms . However. a
combination of environmental and disease factors crippled
the industry with a two-thirds decrease in production by
1988. Despite attempts to revive the industry by cultivat-
ing alternative Penaeus species, production was down to
25 000 tonnes by 1994 and many farmers turned their
attention to farming marine fish (Rosenberry 1994). The
main culprit was the excessive number of shrimp farms
that developed in the coastal margin. Farms were packed
together so tightly that the effluent from one farm polluted
the intake water of the adjacent farm. As this process was
repeated many times along the coastline. so the quality of
the coastal water deteriorated and elevated the physiologi-
cal stress for the cultivated shrimp. This in turn probably
made the shrimp more vulnerable to disease. which then
spread uncontrolled from one farm to the next. This col-
lapse in the Taiwanese shrimp industry left a gap in the
world market that was quickly filled by production from
China. which rose at a rate of 80% per year and reached
199 000 tonnes in 1988. Again, a similar story unfolded
and resulted in the spread of white-spot virus from China
to other Asian countries causing mass mortality in a wide
range of shrimp species (Nakano et at. 1994) .
The rapid and uncontrolled expansion of shrimp farm ing
has resulted in severe disease problems. White-spot virus
spread from China to the other Asian countries causing
mass mortalities of shrimp.
Similar problems have occurred in the shrimp-culti-
vation industry in the Western hemisphere. In Ecuador.
extended drought elevated the salinity and nutrient lev-
els in the Guayas River estuary, which supported a large
number of shrimp farms. Vibrio spp. thrive in this type of
Figure 14.9 Deforestation along the
coastline of Java has occurred to give the
land over to the development of shrimp
cultivation ponds. This story is repeated
around the world and has often led to severe
environmental, water quality, and disease
problems. (Photograph: L. LeVay.)
 Chapter 14 Aquaculture
environment and infected the shrimp held in the farms bor-
dering the estuary. This infection causes shrimp to swim at
the surface of the ponds where they fall prey to seagulls.
The name of this syndrome is Gaviota, which is the Spanish
word for seagull. These outbreaks of disease were treated
with antibiotics or by encouraging the growth of harmless
bacteria that out-competed the harmful Vibrio spp . but had
mixed results. Fortunately. EI Nino rains lowered the salin-
ity in the affected estuaries and thereby diluted nutrient
concentrations and eliminated the disease in 1993 (Cham-
berlain 1997) . In the future. marine organisms mayexperi-
ence a higher incidence of disease outbreak and pathogen
attack with increasing physiological stress induced by the
current rapidly changing global climate (Harvell et at.
2002) .
14. 13 Shrimp farming and
mangroves
As we have seen in Chapter 10. mangroves act as nursery
areas for estuarine fishes and invertebrates, and provide
a feeding and breeding ground for birds and mammals.
They also prevent coastal erosion by storm and wave
action, and prevent soil erosion. In the early years of the
shrimp-farming industry. areas occupied by mangroves
were considered ideal for development for shrimp farm-
ing as they were considered to have little economic value .
As they were the natural habitat for many of the cultivated
shrimp species, they seemed to be the best location for
shrimp farms (Fegan 1996) . However, it turns out that
mangroves have acid sulphate soils with an acidity of pH
3 to 4 when dried out, which creates unfavourable con-
ditions for shrimp cultivation. In a global context, the
(0)
Figure 14.10 (a) Shrimp pond constructed in a deforested mangrove swamp. (b) The new approach to shrimp cultivation
that incorporates the development of mangrove forest in conjunction with shrimp ponds. (Photograph: L. LeVay.)
development of shrimp farms has accounted for only 5%
of mangrove destruction to date, but on a localized scale
the impact of shrimp farming may be far more severe. For
example. the construction of ponds used for aquaculture
has destroyed 20% of the mangrove forests in areas of
Ecuador (Phillips et at. 1993) .
Although mangrove areas are natural habitats for many
shrimp species, areas cleared of mangrove forest are far
from ideal for their cultivation. The removal of mangroves
for shrimp cultivation also leads to coastal erosion and
the loss of critical ecosystem goods and services.
While most shrimp-producing countries now recog-
nize the ecological importance of mangroves. the high
revenues earned from shrimp cultivation are likely to
maintain the pressure for development of some areas of
mangroves . Recent attempts to model the social and bio-
logical benefits of mangrove conservation indicated that
only 12% of the mangrove outside Thailand's mangrove
conservation areas should be given over to shrimp farming
and that 61 % of these mangroves should be maintained in
their natural state (Pongthanapanich 1996). Nowadays,
the importance of mangrove forest for the sustainable
use of coastal areas is widely acknowledged . Hence new
shrimp-farm developments incorporate mangrove planta-
tions that naturally remove some of the excess nutrients
and organic matter produced by the cultivation process
(Fig. 14.10).
Socio-economic and biological modelling indicates that
only a small proportion of mangrove forests should be
given over to shrimp cultivation.
(bl
 14.14 Cultivation of molluscs
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

14.14 Cultivation of molluscs d ement each year, but the mass mortalities occur just prior
to the cockles attaining the size at which they would recru it
Bivalve aquaculture is confined to intertidal and shallow to the fishery. Increasing seawater temperatures, sewage
subtidal areas. One of the biggest attractions of bivalve spe- discharge, agricult ural run-off, and weakened genetic
cies is that they require no inputs of food by the farmer, as stocks all have been blamed for the failures in this fishery.
they feed on phytoplankto n. In add ition, bivalves generally
require relatively little husbandry and hence are suitable Bivalves require relatively little husbandry and convert
for cultivation in areas of the world where the use of high primary production (phytoplankton) into protein. As a
technology is unfeasible at present. Despite the obvious result, the cultivation of bivalve molluscs is often highly
attractions of bivalves as a potential crop, as in other sec- sustainable.
tors of the aquaculture industry, environme ntal problems
have occurred due to over-exploitation of limited coastal The cult ivation of bivalves can help to redress the
resources (e.g. space) . Various environmental effects may adverse effects of other aquaculture activities . For example,
result from differe nt stages of the bivalve cultivation pro- the effl uents from fish farms are nutrient enriched, and can
cess: seed collection, seed nursery and on -growing, and lead to the development of toxic algal blooms . The filter-
harvesting (Table 14. 2). Bivalve fisheries are themselves feeding activities of bivalves re move algae and particulate
at threat from changing environmental conditions. Recent matter from the water column and hence reduce the like-
mass mortalities of important bivalve fisheries (such as lihood of bloom formation (Shpigel et al. 1993). Mussels
oysters in France) h ave occurred due to outbreaks of dis- are particularl y effective organ isms that remove excess par-
ease. In the UK, one of the econo mically most important ticulate-bound nutrients from eutrophic systems (Haamer
cockle fisheries, worth US$ millions per annum, h as expe- 1996), and have been used for the restoration of enclosed
rienced chronic mass mortalities for reasons that are as yet water masses that are heavily polluted (Russell et al. 1983).
unknown. This particular fishery undergoes good spat set- While these mussels are unfit for human consumption, they

Table 14.2 A summary of the environmental effects associated with different st ages of bi valve cu lt ivat ion,
adapted from Kaiser et al. (1 9 98). I

Seed collection

Ecol og ical effect s of harvesting wi ld seed (e.g. reduction of food for bird s, physical impacts on the seabed by fishing
gear, trampling across shores).
Alteration of habitats by use of spat settlement materials, such as crushed shells, gravel, or man-made products (known
as cultch).
Effluents from seed hatcheri es may conta in antibiotics and chemical poll utants.
Introductions of alien species with imported brood-stocks.
• • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • • • • • •• • •• • •• • • • •• • •• • •• • • •• • • • • • •• • •• • • •• • • •• • •• • • • • • •• • • •• • •• • • •• • •• • •

The on-growing phase

Over-stocking leading to problems wi th carry ing capacity of enclosed systems, such as bays.
High density of int erti dal st ructures leadin g to poor w ater circulat ion and build-up of organic matter and reduced spec ies'
diversity in local benth ic community.
Spraying of chemicals on interti dal areas to remove 'pest species', such as burrowing shri mps.
Alteration of habitat by addition of gravel and other material to provide firm substratum on which to grow bivalves.
Exclusion of birds, fi sh, and crustaceans from feedi ng areas due to use of protect ive netting.
• • •• • •• • • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • • •• • •• • •• • • •• • • •• • •• • • •• • •• • •
Harvesting
Disturbance to w ading bird s.
Physical disturbance of subst rat um by mechanical harvesting devices.
By-catch morta lity of invertebrate species associated wi th bivalve cult ure sites.
 Chapter 14 Aquaculture
represent a cost-effective and self-perpetuating means of
maintaining water quality. Although these mussels may be
unfit for human consumption in their primary condition,
it may be possible to consider harvesting them as fish feed
provided that they contain no pathogens or compounds
that might be bio-accumulated up the food chain.
Suspended rope cultivation of bivalves generates some
similarenvironmental problems to suspended fish cage cul-
tivation. The location ofmussel farms is critical if these envi-
ronmental effects are to be minimized. Mussels require a
good exchange ofwaterto replenish phytoplankton biomass
to achieve adequate growth rates for commercial purposes.
Flow is severely reduced toward the centre of a set of mus-
sel ropes. The reduced flow enhances sedimentation rates,
hence faeces and pseudofaeces tend to accumulate beneath
the mussel ropes leading to organic enrichment of the sedi-
ment. The degree to which this occurs is strongly related
to the flow regime at the site of cultivation. Hartstein and
Rowden (2004) studied three contrasting sites ofsuspended
mussel cultivation in New Zealand. They found that the site
with the highest mean flow regime had the lowest percent-
age organic content and that organic content was always
higher directly within the mussel farm area compared to
the surrounding sediments (Box 14.4).
Figure 14.11 A reef of the invasive Pacific oyster Crassostrea gigas in the German Wadden Sea. Extensive beds of
these oysters are now forming in areas occupied by valuable mussel fisheries (Photo: Susanne Diederich/Alfred-Wegener
Institute).
While there is now wide concern regarding the intro-
duction ofalien or exotic species into different geographi-
cal areas of the world through ships' ballast water, humans
have been deliberately moving bivalve species around the
world for many years . For example. Asian Manila clams
(Tapes philippinarum) and Pacific oysters (Crassostrea
gigas) have been grown in Europe for at least the last thirty
years. The importation of adult and bivalve seed has been
responsible for the introduction of a wide range of marine
organisms that are alien to countries where formally they
did not occur (Reise et al. 1999) . These organisms can
have severe ecological consequences and financial impli-
cations for the aquaculture industry when they include
competitors of bivalves, such as the slipper limpet (Crep-
idulafornicata). bivalve predators. such as the American
whelk tingle (Urosalpinx cinerea), and diseases, such
as Bonamia, which infects the blood cells of flat oysters
Ostrea spp. Furthermore. in the case of both Manila clams
and Pacific oysters. these species have become naturalized
in many of the locations where they were introduced. In
particular, Pacific oysters have developed large reefs in
France and The Netherlands where they have over-grown
beds of native mussels that were formerly of high com-
mercial value (Fig . 14.11) .
 14.15 Ranching at sea
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Bivalve cultivation has been linked to the introduction of a stock-enhanceme nt programmes wo rldwide. Reseeding
large number of alien species in certain countries, many of and stoc k-enhanceme nt programmes are more likely to
which have established self-sustaining populations. be financially viable if the species in ques tion have a high
fin ancial or resource value. Examples include red sea bream
(Pagrus major) and Japanese flounder (Paralichthys oliva-
ceus) in Japan, and Atlantic cod in Norway (Svanstad &
14.15 Ranching at sea Kris tiansen 1990 ; Watanabe & Nomura 1990). The rearing
environme nt does not expose hatchery fish to the natural
Technological advances in rearing techniques have con- variability of temperature and food availability that they
siderably incre ased the range, quality, and quantity of fish encounter in the wild. They are also protected from preda-
that can be cultivated, and has provided a new impetus for tors. As a result, hatchery-reared fish of an equivalent age to

Box 14.4: Environmental problems pared w ith surro und ing areas (outside) . At this site, the
associated with suspended rope opport unist ic dorvallid po lychaete Schistomeringos loveni
cultivation of mussels is numerically dom inant beneath the mussel ropes, co m-
Suspended rope cultivation of mussels is practised exten- pared to the species-rich surro und ing areas, whi ch are
sively in New Z ealand. As in other locali ties, the environ- dom inated by more bioturbating fauna such as Amp hiura
mental effects of cultivat ion are closely linked to physical s pp.. At the higher energy Blowh ole Point, the organic
parameters. In low-energy environments, such as Cath- content of th e sedi ment is far lower than at Cath eri ne
erine Cove, organic material accumu lates beneath the Cove, neverth eless signif icant subtle differences are sti ll
cultivation site, partly due to the reduct ion in w ater flow apparent in benthic co mmunity st ructure (adapted from
among the mussel ropes. Clear changes in the benthi c data in Hartste in & Rowde n 2004) .
co mmunity occur beneath the mussel ro pes (inside) com-

Catherine (ave - lowenergy

145

• lnside Blowhole Point - high energy

~
•
•
c
40
• Outside . I n ~i d e
] 30
c • Out~ide
•
~ 20
~
10

• ---.e
~
0

E
<>
0

c "';::
... • ~ -"c
. - •••-- -
•
•
0 c
•
J;
•
'0
c
•
.~
0
'0
0 •a •••
•e
--
0

• -" -
'5 0
_
~ -e ~ '0

- - -•• ...-
0
~
~
c
~
0 ~
~
c c c
~
0
e E • ••
c 0 a ~
0
c
E
-e
< ~ ••
~
~ E
0

~
~
0
~•

Table The environmental co nd it io ns at Catherine Cove and Blowhole Point upstream and
d ownstream of the cu lt ivat ion sit es.

Current (cm 5-') Percentage organic

content
Catherine Cove (low energy) 3 .4 1 Upstream 10.6 Insi de
3 .16 Dow nstream 5.4 Outside
• • • •• • • •• • •• • • •• • • •• • •• • • •• • • •• • •• • • •• • • •• •• • ••• •• •• •• • •• • • • • • •• • • • • • •• • • • • • •• • •• •• • •• •• •• •• • •• •• • •• •• • •• • •• •• • •• • •• • •• •• • •• • •• •
Blowhole Point (high e nergy) 10.2 Upstream 3.2 Insi de
9. 7 Dow nstream 2.9 Outside
 Chapter 14 Aquaculture

wild fish are inferior in terms of their behaviour and physi-
ology. Recent research indicates that their chances of sur-
vival are greatly increased if they are conditioned to natural
temperature regimes and food in advance of release. For
example, the technique required to eat an artificial food
pellet will differ greatly from a natural prey item that will
exhibit cryptic behaviour and escape responses (Brown &
Laland 2001) . Hatchery-reared fish that have never expe-
rienced a predator threat can be trained to avoid preda-
tors more effectively. Brown and Laland (2001) describe
approaches for using wild 'trainer' fish that demonstrate
the appropriate behavioural responses to predator stimuli
in view of hatchery individuals.
Fish reared for mass release into the wild need to be
'taught' how to behave in response to predators and
prey.
Releasing many millions of small fish or shellfish into the
sea is, to an extent, an act of faith. How do we know that
the released individuals make any contribution to overall
catches? For sedentary taxa such as bivalves this is not so
much of a problem, but for mobile taxa such as fish it is
necessary to tag them in some way so that future returns
can be ascertained. This is usually achieved by chemically
tagging the fish such that a chemical signature is incor-
porated in the bony body parts, such as the otoliths. In
Hawaii, hatchery-reared striped mullet (Mugil cephalus)
eventually accounted for 75% of the sampled fish popula-
tion in nursery areas. Thorough pilot studies that identified
the optimum release-size of fish, the best sites and season
for release, contributed to the success of this programme.
Bivalves, such as scallops, need to be seeded at a density
that is sufficient to permit effective fertilization at spawn-
ing. Not only must the density at which the animals are
released be considered, but also local hydrography, which
affects larval dispersal.
Successful mass-release programmes require detailed
knowledge about what constitutes a favourable environ-
ment for a particular species.
14.16 A conservation role for
aquaculture?
Sturgeon (Acipenseridae) were originally harvested for
their eggs or caviar. Today they are also appreciated for the
quality of their flesh. However, the demand for caviar led
to overfishing of the wild populations and, in combination
with the effects of pollution. many species are at low levels
of spawning stock biomass. Recent advances in the aqua-
culture industry mean that sturgeons are now cultivated
around the Caspian Sea and in North America. These fishes
can achieve phenomenal growth rates and some species
will achieve 3.8 kg in their first two years with a conversion
ratio of 1.5 :1 or better. As improvements in aquaculture
techniques continue to develop there is great potential to
alleviate pressures ofover-fishing on the wild stocks ofstur-
geon, although these continue to be threatened by changes
in climate and environmental qualiry (Elahimanesh 2001) .

(oj (b) .....---~"""l"'"-

Figure 14.12 Sea horses are harvested and then sold dry for the traditional medicine trade in China (a). Conservation
of sea horses requires a combination of education regarding their vulnerability to exploitation, and the use of
aquaculture to replace a wi ld-capture industry (Photograph: Patrice Ceisel/Shedd Aquarium and Project Seahorse). Such
approaches have been used successfully to supply the aquarium trade with reef fishes such as clownfish (b).
 14.16 A conservation role for aquaculture?
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Aq uaculture could alleviate fish ing pressure on wild
stocks of species of conservation importance, such as
sturgeons and sea horses.
Syngnathids (sea horses and pipefishes) are threatened
by over-exploitation due to the demands of the Chinese
medicine trade (Fig. 14.12) . These fishes have unique life-
history strategies that involve male incubation of the eggs
in a brood pouch. They have a low reproductive output and
in some species they pair-bond for life. Hence these fishes
are highly vulnerable to sources of additional mortality.
As a result, syngnathid aquaculture is seen as a potentially
lucrative commercial venture. which may aid the conser-
vation of wild populations. Cultured syngnathids could
help to meet any future increases in global demand and
possibly alleviate the effects of overfishing. The extent to
which syngnathid culturing reduces the exploitation of
wild syngnathid populations will depend, in part, upon its
effects on subsistence fishing communities that currently
depend upon syngnathids for their livelihood. Syngnathid
fishers are commonly so poor that they cannot stop catch-
ing syngnathids unless they earn money in other ways.
One outcome of syngnathid culture in countries that do
not traditionally exploit them might be reduced prices for
syngnathids in source countries. This could force fishers to
catch more syngnathids in order to meet their basic needs
or deflect them from one diminished resource to another,
creating new conservation problems. Aquaculture is likely
to have the greatest conservation value when syngnathid
fishers become syngnathid farmers, thereby direetly reduc-
ing pressure on wild syngnathid populations. Once such a
shift in perspective is achieved, the value oflive syngnathids
in the wild as a supply of brood-stock will exceed their value
as a dead product.
To find out more about the biology and cultivation of
syngnathids go to http:/ /www.projectseahorse.org.

Chapter Summary
• Global aquaculture activities continue to increase in terms of their overall contribution to fish-
based sources of protein. Nevertheless, marine species are primarily carnivorous and are unlikely
to achieve levels of production seen in species that feed at lower trophic levels (e.g. carps and
tilapia).
• The cultivation of carnivorous species requires the manufacture of feeds from other sources of
protein. While much effort has been centred on replacing fish-based protein with plant-based pro-
tein , the former remain the primary component of fish feeds and create their own environmental
problems associated with industrial fisheries.
• The cultivation of marine algae and bivalve molluscs are among the most environmentally sustain-
able sectors of the cultivation industry as neither requ ire inputs of feeds. However; bivalve cultiva-
tion can exceed the carrying capacity of relatively enclosed marine systems (e.g. lagoons).
• Most cultivation sites are located in coastal areas where aquaculturists compete for space with
other stakeholders. Constraints on carrying capacity and space have necessitated the development
of automated offshore fish cages that remain on the seabed with minimal maintenance.
• Developments in modern recirculation systems mean that land-based cultivation of marine species
may become economically viable on a large scale within the next decade.
• Aquacu lture of genetically modified species has the potential to dilute the genetic integrity of wild
populations when cultivated fish escape holding nets. Sea lice infestations associated with salmonid
cultivation sites have been blamed for declines in wild fish that are infested as they pass cultivation
sites.
• The movement of cultivated species around the globe has led to introductions of 'exotic' pest
species, diseases, and parasites into new environments.
Chapter 14 Aquaculture

Further Reading
For a comprehensive overview of the environmental effects of aquaculture see Black (200 1) . Naylor et al .
(2000) highlight the add itional impacts of harvest ing fish to grow fish. Hilborn (1992, 19 9 9) provid es
an insight into the debate surrounding the use of hatcheries to supplement declining stocks of salmonids.
• Black, K. D. 200 1. Environmental Impacts of Aquaculture. Sheffield Academ ic Press, Sheffield.
• Hilborn, R. 1992. Hatcheries and the future of salmon in the Northwest. Fisheries 17 : 5-8.
• Hilborn, R. 1999. Confession of a reformed hatchery basher. Fisheries 24: 30-31 .
• Naylor, R. L, Goldbu rg, R. , Primavera, J., Kautsky, N., Beveridge, M. cn, Clay, J., Folke, C , Lubchenco,
J. , Mooney, H. A. , & Troell, M. 2000. Effect of aquaculture on world fish supply. Nature 405: 1017-24.
Disturbance, Pollution,
and Climate Change
Chapter Summary
Human activiti es around the globe have been linked to a
diverse range of ecological changes in marine ecosystems.
Many of these activities involve exploitation of biological
and mineral resources, while other forms of interference
are linked to indust rial and agricultu ral disch arges into river
basins. Often, the changes in marine systems that result
from th ese activit ies are catastroph ic, w hile others are sub-
t ler and only becom e apparent after many years. In order to
assess the relative ecol ogical importance of human interfer-
15.1 Introduction
Human activities are having an ever-increas ing influence
on global marine ecosystems . While the debate continues
a bout the causes and significance of present global warm-
ing, few would now deny that the world's climate is chang-
ing more dramatically than at any time in the last century,
a nd scientis ts have even debated the proxim ity of the next
ice age (King 2004 ; Weaver & Hillaire-MarceI2004). More
recently, attention h as turned to the effects of changing
the acidity of the oceans through the increase in the par-
tial pressure of CO 2 in the atmosphere (Caldeira & Wickett
2005) . The prospect of life without calcium carbonate is dif-
ficult to contemplate (b ivalves with no shells, mass failure
oflarval stages, spineless sea urchins). Although the subtle
effects of ch anges in weather patterns mi ght not cause
immediate alarm, sign ificant events suc h as the break-up
of a large area of the Antarctic ice shelf in 1995 made global
media headlines (Vaughan & Doake 1996). More recently,
the reopening of the Arctic route from the Atlantic to the
Pacific further highlighted the decline in ice sheet cover.
With the exceptio n of desert and polar regions , coast al
areas are de nsely populated, particularly at the mouths of
ence, it is necessary to understan d how marine co mmuni-
t ies respond to ecological d isturbance and env ironmental
change. It is also imperat ive to app rec iate t he tem poral
and sp at ial scale at w hich these processes are relevant
Asce rtaining w heth er ecological changes have occurred in
response to d istu rbance or environ mental changes req uires
a rigorous approach to experimental design and monitoring
and a careful co nsideration of t he issue of sta tist ical power
to detect change.
estuaries and sheltered bays that provide safe a nchorages
and convenient access inland . In contrast to the vast tracts
of open oceanic waters, the coastal margins of the world's
land masses are the focus of intensive human activities.
Global climate is currently changing faster than at any
time in the last 100 years and has already caused dra-
matic changes in polar ice cover.
Human activities modify the marine environment, both
through the removal of biomass and habitats and via the
additio n of contaminants and physical structures. Marine
biological resources are heavily exploited for consumption
and economic gain (Chapter 13), and habitats often altered
incidentally. Rivers convey terrestrially derived m aterial
load ed with sewage, agricultural, and industrial pollutants
onto the continental shelf (Chapter 8) . Understanding the
ecological responses to these human activities requires an
appreciation of both watershed and marine environmental
processes. Marine traffic, oil and gas extraction, and dredg-
ing are all concentrated in shelf areas, although the price
and demand for oil has pushed exploration further down the
continental shelf slope. Further offs hore in the mid-ocean,
 Chapter 15 Disturbance, Pollution, and Climate Change
direct human influences are limited to oceanic crossing by
marine vessels and fishing activities. The decreasing influ-
ence ofhuman activity with distance from the coast is related
to the physical limitations imposed by the environment
(wave height and depth) and the logistics of getting there.
Nevertheless, these activities are expanding further offshore
as coastal resources are depleted and technological develop-
ments enable exploitation of more extreme environments.
Understanding the ecological consequences of human
activities in the coastal zone requires knowledge of land-
ocean interactions that include watershed and marine
environmental processes.
Extreme environments offshore in deeper water are made
more accessible with technological advances that reduce
costs, increase profitability, and increase safety. Despite
the latter; the more extreme the environment, the more
risk of adverse incidents with much larger ecological
repercussions.
In this chapter, the role ofhuman activities in causing eco-
logical disturbance is considered. and their significance is
gauged against the scale and frequency of natural sources
of disturbance. To understand the ecological importance of
human activities in the marine environment, we need to be
able to detect changes in measured ecological characteristics
using appropriate observational or experimental techniques.
An understanding of the scale at which ecological processes
operate should underpin the ultimate selection of metrics
chosen for study (e .g, diversity, abundance, biomass) . We
discuss the relevance of a selection of measures and the
importance of appropriate experimental design. The wide
range of human impacts on the marine environment dictates
that we are selective in our coverage. Issues surrounding
aquaculture and fisheries were addressed in previous chap-
ters (Chapters 13 and 14) .
15.2 Ecological role of
disturbance
Earlier chapters have discussed the spatial and tempo-
ral scale at which various small- and large-scale processes
operate in the marine ecosystem (Chapters 1, 6, 7, and 8) .
These dynamic processes affect ecological processes and the
structure of communities and habitats. such that they are
in a continuous process of change. These natural fluctua-
tions form the backdrop against which the relative impor-
tance of human activities should be assessed. Almost any
human intervention in the marine environment, whether
positive (e.g. habitat restoration) or negative (e.g. dumping
of waste), leads to some measure of ecological disturbance.
Pickett and White (1985) defined disturbance as 'any dis-
crete event in time that disrupts ecosystem, community. or
population structure and changes resources. substratum
availability, or the physical environment'.
Most human activities in the marine environment cause
some form of ecological disturbance. These occur against
a background of natural disturbances that occur at a vari-
ety of spatial and temporal scales.
15.2.1 Sources of disturbance
Disturbances act at different scales and frequencies. Changes
in sea level. ocean temperature. and water circulation, mod-
ify habitats and their associated fauna over large areas and
usually overlong timescales ( >20 years) . Natural phenom-
ena such as cyclones and hurricanes have regional impacts
on a seasonal basis and affect a wide range of marine habi-
tats to different extents (Hall 1994) . Periodic outbreaks of
ecosystem-engineering organisms. such as starfishes and sea
urchins, can lead to periods of prolonged habitat modifica-
tion (Chapter 8). Rising ocean temperatures may facilitate
the proliferation of non-indigenous species, which can alter
the existing community assemblage through the process of
competition for space and other resources. Human agents
of change vary from the direct effects of an oil spill, habitat
damage by bottom fishing on the seabed, eutrophication of
sea basins. discharge of toxic substances. to trampling across
the seashore. Whatever the source ofdisturbance. it is a fun-
damental process that contributes to the maintenance of
diversity in all ecosystems.
Disturbance is one of the most important ecological
processes in the maintenance of diversity by opening
up resources for colonization by opportunistic species.
However, excessive levels of disturbance lead to species
poor communities.
15.2.2 Scale of disturbance
There is an intimate link between the spatial and temporal
scale at which environmental change occurs. At the smallest
scales (J.1m). chemical reactions between sediment particles,
flocculation oforganic matter in the water column, viral. and
bacterial processes occur on a very short timescale. At the
next scale up. minute-by-minute disturbances occur as the
result of the feeding activities of macrofauna in sedimentary
habitats and as a result of their movements upon or through
the sediment, creating burrows or furrows in their wake. At
slightly larger scales, up to one metre, larger-scale bioturbat-
ing processes become important (e.g. faecal mound forma-
tion. burrow chamber excavation), and the feeding activities
 15.2 Ecological role of disturbance
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
of megafauna such as birds, fishes. and crabs become impor-
tant agents of disturbance that occur every tidal cycle. Thus
the seabed is a mosaic of patches in different stages ofalter-
ation and recolortization (Grassle & Saunders 1973) . Each
modification on its own is relatively small compared to the
total habitat resource; however. the summed total of these
effects is such that they have a significant role in determining
the characteristics of that habitat (Fig. 15.1) .
Small-scale physical disturbances may seem relat ively
insignificant when considered on their own, but their
additive effects may influence w ider-scale community
structure.
The additive effects of small-scale natural disturbances
are well illustrated by the effects of the burrowing and
feeding activities of the soldier crab (Mictyris plarycheles)
in southeastern Tasmania. As soldier crabs forage across
intertidal mudflats they create intensely disturbed areas of
sediment in discrete patches interspersed with undisturbed
areas. These small-scale disturbances have the most pro-
found effect on the meiofaunal assemblage, such that nema-
todes, species' richness, species' diversity. and evenness were
significantly reduced in disturbed as opposed to undisturbed
areas. although total abundance was unaffected. Changes in
community structure were subtle and resulted from an over-
all change in the balance of relative abundances of many
species. rather than from changes in a few dominant species
(Warwick et al. 1990). Hall et al. (1993) undertook a simi-
Figure 1 5.1 The physical disturbance created by individual
fauna, such as estuarine fiddler crabs, may be small in scale
(em), but the additive effects of the disturbance created
by the entire popu lation within an estuary can lead to the
complete reworking of the surface of these sediments in
just one low tide (photograph: M.J. Kaiser).
lar study in a Scottish sea loch. They hypothesized that the
pit-digging activities ofa large predatory crab (Cancer pugu-
rus) would generate significant community changes in the
soft-sediment assemblage. Yet, despite a carefully designed
experiment. no ecological effects were apparent. They con-
cluded that larger-scale natural disturbance processes. such
as wave disturbance, masked any subtle effects that pit dig-
ging by crabs might generate.
Even t he additive effects of multip le small-scale dis-
turbances may be masked by much larger-scale envi-
ro nmental disturbances, such as storm-induced wave
perturbat ion. Thus the relative effects of biota on the
environment are context-dependent, such that a species
may have an important effect on the ecology of a com-
munity on one location, but less of an effect in another
locat ion.
15.2.3 Recovery rate
The scale of physical disturbances created by micro-, meio-,
and macrofauna are relativelysmall and the recovery time of
the habitat in response to those disturbances is rapid, occur-
ring within seconds to weeks (Table 15.1) . Recovery times
in response to disturbance increase with scale. At smaller
scales ( < 1 rn), recolonization occurs through active move-
ment and passive transport ofadults into the disturbed area.
At larger scales of disturbance, typical patterns of recoloni-
zation occur. For example. physical disturbance of the sea-
bed by towed bottom fishing gear disrupts the surface of the
seabed and kills, damages, or digs out many of the infauna
and epifauna in the path of the trawl. The immediate post-
trawling effects are typified by a reduction in resident species
number and abundance (Kaiser et al. 2002) . However, this is
always accompanied by a short-term (2 to 3 days) influx of
scavenging species. which are attracted to the carrion gener-
ated in the disturbed area (Ramsay et al. 1997). Thereafter,
the recolonization rate is linked to the supply oflarvae to the
disturbed area and habitat stability. If disturbance involves
disruption of the habitat, a process of habitat restoration is
required before recolonization of the associated biota occurs
in full (Fig. 15.2) . For those habitats formed by living biota
with slow growth rates and irregular recruitment of larvae.
recovery times are measured in years or even decades (Collie
et al. 2000) .
Recolonizat ion after disturbance events follows a typ ical
pattern, with short-term immigration of active and scav-
enging fauna, followed by longer-term (months t o years)
recolonization thro ugh larval recruitment. The scaveng-
ing fauna disperse within a few days after the biota killed
by the disturbance have been consumed.
 Chapter 15 Disturbance, Pollution, and Climate Change

Table 15.1 The relationship between the s pat ia l s ca le of a disturbance and the time taken for recovery to
occur. Recovery is defined as the point at which the biological co mmunity wit hin the disturbed area is no longer
significantl y different from that in other s imila r and proximate areas that were not the subject of the disturbance
(control areas).

Spatial scale Temporal scale Processes

(frequency)

~m milliseconds- seconds Chemical reactions, virus and bacterial driven processes

mm-crn secon ds-minutes Meiofaunal processes, macrofauna l sediment reworking, predation,
herbivory, faecal production
0 .1- 1 m rn inutes-days Bioturbation , diatom mat formati on, megafaunal disturbances (e.q.
feed ing pit excarvation) , precipitation of minerals (calcium carbon ate
mounds)
1-1 0 0 m days-months Recolonization and redi stribution of small microbiota, biomass and
pop ulat ion fluctuations, sediment resuspension and settlement,
bedload transport, t idal scour, and currents
100-10 000 m months-years Hurricane and strong events, iceberg scouring, sub marine landslid e
events, seismic activity, recolonizat ion of large macrobiota
> 10 0 0 0 m years-decades Volcanic and seis mic activity, anoxic events, submarine landslides,
global warming, EI Nino events, coral bleaching, global warm ing,
reco lonizati on of large slow-growing macrobiota

0.7
Figure 15.2 The relationship between the rate at which
• Silty sand
0.6 sedimentary habitats recover (quantified as how quickly
\ • Mud
• Muddysand 0 standard pits dug into the sediment filled in (decrease in
• 0
depth of pit cm d- 1) ) and the rate of biological commun ity
• • 0
recovery (measured in terms of the rate at whi ch the

• •
difference between control and dug plots decreased
• 0 in terms of the total number of individual organ isms
•
- 0.1 inhabiting the sediment). Muddy sand treatments filled in
more slowly than any other treatment and consequently
0
-0.02 -0.015 -0.01 -0.005 o recolonization was much slow er.
Habitat recovery rate mm/day

15.2.4 Intermediate disturbance in low-energy environments, such as fjords. The fallout of

hypothesis
The responses of species' diversity and assemblage char-
acteris tics to disturbance can be described by an impor-
tant ecological paradigm: the intermediate disturbance
hypothesis (Box 15.1 ). Rhoads (1974) and Pearson and
Rosenberg's (1978) models of the changes that occur in
macrofaunal commun ity structure along a gradient of dis-
turbance follow the principles of the intermediate distur-
bance hypothesis (Fig. 15 .3). Their models of macrofaunal
community responses to physical disturbance and organic
enrichment are amplysupported by direct observations. The
Pearson and Rosenberg (1978) model is well-illus trated by
the situation that occurs beneath suspended fish farm cages
uneaten food pellets and faeces that descend to the seabed
results in an organ ically enriched environment, which in
extre me cases is suitable only for the growth of bacteria
or a few species of small opportunistic taxa (oligochaetes
and Capitella spp.) that are highly tolerant of low-oxygen
cond itions (Chapter 14). Such a commun ity has very low
diversity. At increasing distances from the area beneath
the cage, the loading of organic enrichment decreases, dis-
solved oxygen levels increase, and environmental stress is
reduced , such that the opportun istic species are gradually
replaced by larger body-sized biota, such as echinoderms
(sea urchins and brittlestars) and bivalves, many of which
perform important ecological functions , such as mixing
 15.2 Ecological role of disturbance
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 15.1: Intermediate High i - - -r== = = : : : : ; - - - - - - - - i

2
disturbance hypothesis
Although not the first, Connell's ( 1978) appli- 3
cat ion of the intermediate disturbance hypoth-
esis (IDH) is perhaps the most quoted. He used
the IDH to explai n changes in species' diversity
under different scenarios of disturbance in two
I
habitats of high diversity: tropical rainforests
and coral reefs (figure). At low levels of dis-
t urbance, succession processes eventually lead Climax community
Grosslystressed community e.g. deepwater roral reef
to a climax com munity dominated by relatively
e.g. beneath site of cage cultivation of fish
few species of large biomass (3). When this Low
state is disturbed, e.g. by a tree fall in a rain- Frequent distu rbance - - - - - - - - - - - - Infrequent disturbance
forest or the damage of coral reef structures by Immediatelypail-distu rbance - - - - - - - - - Long cher 0 disturbance
a passing hurricane, space becomes available Intense distu rbance - - - - - - - - - - - - Minimal disnr rbcme
that permi ts colonization by opportunistic spe-
cies (2). The modified assemblage now has a
co mbinat ion of climax and opportunistic species, thereby bance increases, only a few opportunistic species persist
increasing diversity. As the severity or frequency of distur- resulti ng in an assem blage of low diversity (1).

(oj
100cm

Figure 15.3 The Pearson and Rosenberg

(1978) model of the response of seabed
50 rm communities to physical disturbance (a) and
BiOQ.enicsediments a gradient of gross pollution (b). Towards
(shells &
calcareous the left of the diagrams the benthic
frogments)
communities experience the greatest
o
intensity of stress and the community is
Minerolsediment
(pebble, groyel) characterized by low diversity, and typically
is dominated by only oligochaete and
STAGE1 STAGE 2 STAGE 3 STAGE 4 STAGE5
Small encrusting Shell encrusting Iuniene s Sponges Reefforming polychaete worms and mats of bacteria.
Bryozoa Bryozoa Gostropods Brittle stars Bryozoo In Figure (b) only the top few mm of the
Small biyolyes Mussels Erecl Bryozoa Iuniretes Echinoderms
Oysters Mussels Gostropods Crobs sediment are oxygenated at the left of the
Oysters Erecl Bryozoa Bisolses
Mussels Gastropods diagram. As stress decreases to the right of
Anemone Mussels
Oysters Anemone the diagram, so the body size and longevity
Oysters of the fauna increases (typified by large
Timesince disturbance burrowing bivalves and echinoderms). The

(bj
depth of oxygenated sediments gradually
increases with decreasing stress levels and
increasing bioturbatory activity. The same
gradient occurs in response to organic
enrichment usually along a gradient
of distance from the source of input.
Figure (a) is the response of epifaunal
communities to dredging, showing the
macrofaunal succession on the seafloor of
the Foveaux Strait, New Zealand (Cranfield
et al. 2004). (Figure (a) reproduced from
Journal of Sea Research, 2004, vol. 52,
Gross pollution Distonce Normol 109-126 with permission from Elsevier.)
 Chapter 15 Disturbance, Pollution, and Climate Change

sediments that enhance oxygenation and microbial produc-
tion (Fig. 15.3) . Exactly the same type of response would be
observed in response to sewage discharge or in areas with
high inputs of nutrients.
The intermediate disturbance hypothesis describes the
response of community diversity across gradients of dis-
turbance. Highest diversity occurs at intermediate lev-
els of disturbance that result in assemblages with both
opportunistic and climax species.
15.3 Measuring the effects of
human activities
In order to study the effects of human interference on the
ecology of marine communities and their components, we
need to be able to quantifyappropriate measures ormetrics
that respond in some way to the human activity of interest.
These metrics must be amenable to quantification in a reli-
able and consistent manner. Processes that respond over
decadal timescales require long-termstrategies ofsampling
if these are to be quantified. The metrics to be measured
may be univariate responses of single factors. such as
change in abundance or species' richness; distributional
techniques that measure the distribution of individuals or
biomass among an assemblage oforganisms; or community
responses that measure the responses ofmore than one spe-
cies, known as multivariate responses.
15.3.1 Univariate measures
Measures of changes in body-size class describe the
relative abundance of small and large individuals in a
population. This is particularly important w hen trophic
status changes with increasing body size, e.g. th e tran-
sit ion from juveniles considered as prey, to adults that
become predators.
In most cases. the effects of human activities are not spe-
cies-specific and have variable effects on different compo-
nents ofan assemblageoforganisms. For example, release of
a contaminant from a point source of discharge (e.g. chemi-
cal discharges from an outfall pipe) is likely to have greater
cumulative effects on a range of sedentary fauna and less
severe effects on mobile fauna that are transient within the
area affected by the discharge. In the case of direct physical
disturbance (e.g, by bottom trawling or aggregate dredging),
certain fauna may be more vulnerable than other constitu-
ents of the biological assemblage. The resultant community
changes are often subtle and might not be revealed by the
examination of the response of individual species. In these
cases it is more usual to take multi-species samples that are
3
Phytoplankton
2 f-
1 I- ~
~''"
o
·1 I- "'\ -I'
·2
3
Herring
2 l-

1 I-
When investigating the response of a single species to an
,-Y; w
environmental gradient or disturbance treatment in an
experiment, it is typical to measure changes in abundance.
o
·1 I- ~ --;/'
biomass, or some other physiological. morphological, or , , ,
behavioural response. However, measuring the response of ·2
3
a single species takes no account of the effect that changes Kiniwoke clutch
in the abundance orbody-size class distribution of that spe- 2 l-
cies mighthave on communitystructure. This is particularly , f),."
1 l-
important when the trophic status of taxa changes through
their life history. This is typified by the relationship between o ~ t-;
17
cod (Godu.s morhua) and whiting (Merlangiu.s merlangus) . ·1 f-
:'-. -0.
.~
Small cod are consumed by adult whiting, which in turn , ,
·2
are eaten by adult cod. Single species that are the focus of 1950 1960 1970 1980 1990
long-term studies tend to be those that are easily identified
and counted in situ (e.g, seabirds, pinnipeds, limpets, bar- Figure 15.4 Parallel long-term trends in phytoplankton
nacles). or show strong morphometric changes in response biomass, herring abundance, and kittiwake clutch-size
to a stress agent (e.g. development of male characteristics driven by patterns in weather in the North Sea. The y axis
in female whelks) . Often, such taxa are considered to be is a relative scale showing the degree of change around a
indicators of environmental change that may (or may not) mean value (0 :;:: no change from mean). (From Aebischer
be reflected in other parts ofthe ecosystem (Fig. 15.4) . et al. 1990.)
 15.3 Measuring the effects of human activities
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

representative of the biological assemblage. Within each Diversity indices summarize counts of multiple species
sample, counts of multiple species can be collapsed into a within a sample in a single coefficient. Different indices
single coefficie nt, such as a diversity index. For example, are sensitive to either changes in rare or dominant spe-
some diversity indices give a measure of the extent to which a cies within the assemblage.
relatively small number of species account for a large propor-
tion of the total number or biomass of individual organisms
w ithin a sample (Box 15.2; see also Chapter 1).

Box 15.2: Univariate and distributional

community characteristics
Sample A B C
Abra olba 150 2 1
Acanthocardia echinata 5 1 3
Acteon tornatilis 1 1 1
Chamelea gallina 1 3 6
Corbulo gibba 1 1 4
Donax vittatus 55 5 2
Dosinia sp. 2 1 1
Ensis ensis 1 15 2
Fabulina fabula 2 350 1
Total number of species S 9 9 9
Total number of individuals N 218 379 21
Species' richness (Margale!) d = (5 - l ) f ln N 1.49 1.35 2.63
Pielou's evenness J r = H' f l og 5 0.4 0.18 0.9

This example shows th ree samples of a benthic assem-
blage with only the abundance of the bivalve taxa recorded.
The distribution of individuals within each of samples
A, B, and C is very different. In samples A and B, Abra
alba and Fabulina fabula are numerically dominant, w hile
in sample C the individuals are more evenly distributed
among the species. Below the community data are shown
two univariate metrics of these samples, the total num-
ber of species and the total number of individuals. These
metrics are then used to calculate a diversity index (Mar-
galef) or an index of evenness (Pielou) derived from the
Shannon Wiene r diversity index (H') and the total number
of species (S). Sample C has the highest species' richness
as the same numb er of species are distributed among a
smaller number of individuals. Accordingly, sample C also
has the highest index of evenness (measured on a scale
between 0 and 1). The same community data can be dis-
played graphically in a k-dominance plot, which shows the
cumulative percentage dominance of each species in the
assemblage ranked according to dominance.

100

.. A
80
0~
•
~
0
c
0
E
60
0
Q
• y8
-"
.<
. a 40
E
"
~

20
.c
0
1 10
Species rank
 Chapter 15 Disturbance, Pollution, and Climate Change

While diversity indices are a useful tool for detecting
major community changes that occur as a result of gross
disturbance or along steep environmental gradients. they
can be insensitive if the changes are manifested as spe-
cies' replacements with similar levels of abundance. In
addition. if diversity indices are to be used effectively, it is
essential that the scale at which community diversity met-
rics are measured is appropriate for the scale at which an
agent of change may operate. A good example of this scale
effect is the response of diversity metrics to bottom fishing
disturbance. Fishing gears disturb large areas of the sea-
bed. Even so, highly abundant small-body-sized animals
(e.g, polychaete worms) are relatively resilient to physi-
cal disturbance, while less common larger fauna. such as
burrowing sea urchins and bivalves, are highly vuloerable
to disturbance. Typically, marine ecologists collect many
small samples of the seabed to try and improve the chance
of detecting responses to environmental change (15.3.5) .
However, Kaiser (2003) found that it was not possible to
detect the effects of fishing on community diversity when
small-scale (0.1 m-) samples were collected. Only when
larger-scale samples were considered. which sampled more
effectively the less common and more vulnerable species,
did the effects of fishing on diversity emerge (Fig. 15.5) .
This example underlines how sampling at the wrong scale
can lead to erroneous conclusions about changes in com-
munity diversity!
While collecting many small samples may increase statis-
tical power, fewer larger samples reveal changes in rare
species more effectively.
(oj
The use ofdiversity indices can fail to detect large changes
or differences in the composition of biological communities.
For example, two communities mayhave the same diversity
index even though their species' compositions are entirely
different. Alternatively. the abundance ofone species might
decrease while another increases by an equivalent amount
in response to environmental stress. These limitations have
been overcome to an extent by the introduction ofnew mea-
sures, such as taxonomic diversity and taxonomic distinct-
ness (Somerfield et at. 1997) (Chapter 1). These indices
are more sensitive to environmental and other disturbance
gradients than traditional measures (Fig. 15.6). However, in
order to calculate taxonomic distinctness it is necessary to
have a detailed knowledge of the taxonomy of most of the
components of the assemblage. a feature that is lacking or
variable for many areas of the world.
Policy makers and environmental managers are par-
ticularly interested in 'indicators' of change. Typically they
dislike the complexity of natural systems and would pre-
fer a single metric or group of metrics that convey simply
whether the state of the environment is 'good'. 'bad', or 'the
same'. However, in reality. there is such complexity behind
any of these metrics that they are prone to misinterpreta-
tion. As with diversity indices. indicators such as the mean
trophic index (MTl) that indicates the mean trophic status
of the fish community in the sea, does not tell you why a
particular change might have occurred or whether it is
driven by natural environmental fluctuations or induced by
human activities (see Chapter 4 for more on trophic level) .
See Borja et at. (2000) and Borja & Dauer (2008) for a fur-
ther discussion of the application of a range of different
indicators used to assess system status.

Figure 15.5 The size of sample units collected (note: do not confuse with the number of samples collected) is critically
important if rare species are those most vulnerable to a particular form of disturbance, such as bottom fishing (a). If
the size of samples collected is too small (A), then species' richness will not be sampled with sufficient power to detect
the effects of the disturbance. This is illustrated in an example of a study of the effects of sample size on the ability
to detect the effects of fishing on benthic diversity (b). As the size of the samples collected increases (A, B, and C),
the effects of fishing on species' richness (means + 2 SE) suddenly become apparent as indicated by the significant
differences (denoted by 0) between fished and unfished areas.
 15.3 Measuring the effects of human activities
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

New diversity indi ces, such as taxonomic distinctness, are

sensitive to changes in abundance or biomass of particu-
lar species and have overcome some of the insensit ivity
of other ind ices.

15.3.2 Distributional measures

These techniques summarize a set of species counts from a
single sample as a curve or histogram. For example. k-dom-
inance curves rank species in decreasing order of abun-
dance, the steeper the initial part of the curve the greater
the contribution of one or a few species to the overall
abundance (Box 15.2) . Counts of each taxon are converted
to percentage abundance relative to the total number of
individuals in the sample. The cumulative percentages are
then plotted against species rank (Lambshead et al. 1983).
A similar plot can be generated for biomass and superim-
posed on the abundance plot to give ABC (abundance-bio-
mass-comparison) curves as defined by Warwick (1986) .
In a relatively pristine or low-energy environment, a
community typically will be dominated by large-bodied
individuals (e.g. sponges, soft corals, large fishes) and
the biomass curve would lie above the abundance curve
(relatively few individuals contribute to a relatively high
proportion of the biomass, giving a steep biomass curve) .
At increasing levels ofenvironmental or physical stress, the
large body-sized biota are replaced by high abundances of
very small biota (many individuals contribute a relatively
small proportion of the total biomass but a relatively high
proportion of total abundance, giving a steep abundance
curve) and the biomass and abundance curves eventually
cross over such that the abundance curve lies above the
biomass curve.
Another distributional technique that is useful in the con-
text of exploited systems is to examine the distribution of
different body-size classes of organisms in the community.
Typically large body-sized organisms are those that are long-
lived or slow growing and therefore the most vulnerable to
over-exploitation or disturbance from anthropogenic activi-
ties. Thus under a regime of over-exploitation or excess dis-
turbance, the proportion oflarge body-sized individuals will
be expected to diminish, while smaller body-sized classes
will become more prevalent. If the number oforganisms are
allocated to Log base 2 size-classes, it is possible to estimate
the slope of this relationship. The steeper and more nega-
tive the slope, the lower the proportion of big 'things' in the
community, which indicates potential over-exploitation or
a condition of elevated disturbance (Rice & Gislason 1998).
While this rule holds quite well for highly structured marine
systems, it requires a greater input of taxonomic identity to
interpret the results for terrestrial systems (Petchey & Bel-
grana 2010) .
••
4.0
. ..,..-
•:. ......
•• • ••
H' 3.0
2.0
100 1000 10000
Distance [m)
Figure 15.6 The example shown is calculated from
species ' abundance data for an oilfield in the North Sea.
Various diversity indices were calculated and plotted
against distance from the centre of the oilfield to a
distance of 10 km. Taxonomic distinctness (~*) was
found to be the most sensitive univariate measure of
community structure, increasing linearly as samples were
collected further away from the centre of hydrocarbon
contamination while the Shannon-Wiener diversity index
(H') was insensitive beyond 100m from the centre of the
oilfield (Somerfield et al. 1997).
Dist ributional techniques, such as ABC curves, provide a
useful insight int o changes in biomass distribution rela-
tive to the abundance of biota in response to distur-
bance.
15.3.3 Multivariate techniques
These techniques compare two or more samples based on
the extent to which these samples contain the same or dif-
ferent species at varying levels of abundance. Multivariate
analytical techniques incorporate both species' identity
and abundance or biomass. A comparison between pairs
of samples will yield a similarity coefficient that indicates
the degree (percentage) of similarity between each pair of
samples. When there are more than two pairs of samples,
pairwise comparisons are made between each possible
 Chapter 15 Disturbance, Pollution, and Climate Change

combination of samples. The resulting similarity coeffi- 15.3.4 Detecting change

cients are used as the basis to classify or cluster mutually
similar groups of samples. This can be taken on a further
stage to yield an ordination plot (Fig . 15.7), which maps
the samples in either two or three dimensions, such that the
distances between pairs ofsamples reflect their relative dis-
shnilarity ofspecies composition (Clarke & Warwick 1994).
In a similar manner, the same samples can be analysed in
terms of their environmental characteristics (depth, salin-
ity, bottom current speed, etc.) and another ordination plot
generated. The similarity matrices on which the species and
environmental data plots are generated can then be com-
pared to investigate the extent to which environmental
similarities among samples reflect patterns in community
data (Fig. 15.7) . These analyses are complex but have been
made accessible to non-specialists through the develop-
ment of sofrware packages such as PRIMER (Plymouth
Routines in Multivariate Ecological Research) .
Mult ivariate techniques, such as multi-dimensional scal-
ing ordinat ion (MDS), can be used to visualize the lit-
eral similarity between multiple samples in relation to
experimental manipulations or environmental gradients.
The closer together two sample points appear in the
ordination plot, the more similar their assemblage com-
posit ion; the further apart they appear in the plot, the
more dissimilar their const ituents.
Stress, 0.13
TO
wN
aT o
T wN o
a T o wN RWB
o activities and the rate at which restoration of community
a DRO
RWB o 0 RWB
As marine ecologists, we are interested in detecting eco-
logical changes in response to human activities in the
marine environment. This might be the change in biomass
of plankton or fish abundance over several decades, or
might be the change in community characteristics in areas
where aggregate extraction occurs. To stand any chance of
success we need to ask the correct question at the outset.
This is a problem that besets many of the long-term data
sets that continue to be maintained today. While they are
an invaluable source of data, many were never designed
to answer some of today's ecological challenges. Long-
term data sets often track environmental factors, such as
seawater temperature, which is reflected in the response
of ecological metrics such as phytoplankton biomass (Fig.
15.4) . However, many other variables are also correlated
to these fluctuations and may be either synchronous or out
of phase. Long-term ecological changes are strongly driven
by environmental fluctuations and it is difficult to disen-
tangle the relative importance of the influence of multi-
ple environmental factors . For example, to ascertain the
non-lethal effects of chemical contaminants on fish larval
survival, it would be desirable to conduct a series of con-
trolled laboratory experhnents that manipulated only this
variable while environmental conditions were held con-
stant. Adding additional variables into the experimental
design is possible but much more demanding on resources.
Similarly, the ecological consequences of activities such as
dumping of waste, channel dredging, aggregate extrac-
tion, and bottom fishing require an experimental approach
to determine the degree of change attributed to these
attributes occurs (if at all) .

~; Long-term data sets are an invaluable tool to elucidate

long-term trends and responses in biol ogical metrics.
iIY
However, many of these data sets are unable to answer
iIY conclusively some of today's pressing environmental
questions due to t hei r original design and sampling
limitations (see Green 198 9).

Figure 15.7 An MDS ordination plot of fish and benthic communities sampled from sandbanks in the Irish Sea using
a bottom fishing trawl. Each point represents one standardized trawl samp le and t he codes relate to locations around
the coast of Wales. Interpretation of the plot is quite simple. The closer together the samples appear in the plot, the
greater the degree of similarity between them in terms of species' compos ition and abundance. Not surprisingly, the
samples collected from the same location tend to be more similar to each other than samples collected from elsewhere.
In addition, a key environmental parameter (carbonate content of the sediment) can be overlaid on the plot. This shows
that locat ions shown above the solid line of the plot have a relatively low carbonate content (small bubbles), whi le those
below the line have a relatively high carbonate content (large bubbles) (from Kaiser et al. 2004).
 15.3 Measuring the effects of human activities
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Long-term data sets of fish abundance were set up spe-
cifically to measure fluctuations in spawning stock biomass
(Ch apter 13) and provide key guidance when setting con-
servation priorities for fish populations. However, as fish
become less abundant with over-exploitation, it becomes
more difficult to sample the population with accuracy (i.e,
there simply are not enough fish to sample, or they are too
elusive). Knowledge of the statistical power of surveys to
detect trends is essential, since the consequences of not
detecting a real trend can be profound (see Peterman 1990)
(Techniques box). In ot her words, a population m ay be
heading for extinction but we might not detect this critical
decline because the survey design does not have sufficient
statis tical power. This situation is particularly acute for spe-
cies that are highly vulnerable to fishing effects or that are
uncommon w ithin an assemblage under normal circum-
stances . Maxwell and J ennings (2005), examined these
effects for Nort h Sea fish survey data and found that the
power of the survey to detect abundance decreases on tim-
escales of < 10 years was low. Hence, there is a real danger
that some species could become extinct many years before
we become aware of their demise.
Techniques: The importance of
statistical power
Statistical power is not about flexi ng your analytical prow-
ess. Every experimental study has some level of error,
whether from deficien cies in sampling or due to natural
variability. Statistical tests are associated with a probabil-
ity value, which is often set at 0.05. What this means is
that there is a 1 in 20 chance that the result obtai ned
occurred by chance alone. Hence, there is always a dan-
ger tha t our apparently significant effect is in fact false
and occurred by pure chance. This is known as a Type I
error. This is particularly likely to occur when undertaking
multiple pairwise tests, the more tests that we perform the
greater the chance of getting an erroneous result by pure
chance (e.g. testing for differences in each environmental
parameter measured at each of two sites). The chance of
making a Type I error is reduced by correcti ng or loweri ng
the level at which significance is deemed to have been
achieved (e.g. from 0.05 to 0.0 1).
When significant differences occur between two treat-
ments, but we fail to find this difference, a Type II error
has occurred. Non-significant outcomes are equally as
important and just as informative as significant effects.
Consider the example of the study of the effects of a
shellfish fishery on benthic communities, the outcome of
Vulnerable species could become extinct many years
before we realize their demise if survey design is inad-
equate to detect declines in their populations.
15.3.5 The experimental approach
The ab ility to design and interpret appropriately designed
expe riments is one of the fundamental tools of the ecolo-
gist. The re are a number of crucial steps that must be con-
sidered to avoid comm on pitfalls made by both students
and professionals alike. First, what is the question you are
trying to answer? Let us say we are interested in knowing
the effects of bivalve shellfis h harvesting on the associated
benthic fauna in a sandflat habitat. So the question is 'What
changes does shellfis h h arvesting cause in the associated
benthic community?', or to put it as a null hypothesis 'Shell-
fish harvesting causes no ch ange in associated benthic com-
munity structure '. Thus we h ave identified that we need to
manipulate a benthic assemblage containing an appropri-
ate target species (e .g. clams, cockles, mussels) by subject-
ing it to a typical harvesting methodology (e.g. hand raking,
which may decide whether fisheries managers decide to
close, or permi t harvesting, and possibly whether the fish-
ermen cont inue to make a living or not. When no effect of
the fishery is reported, it is important to exami ne whether
the statistical power of the experimen t was sufficient to
detect the effects of interest (see Hall et al. 1993 for an
elegant example). This underlines the value of prelim.
inary sampling that can be used to calculate the amount
of replication required to detect a certain level of effect
(e.g. a 10% change in abundance of a particular spe-
cies or community metric) before the main experimental
manipulation is performed. Such an approach was used
by Stewart et al. (2010) to hig hlig ht the level of repli-
cation required to detect the outcome of implementing
marine reserves in temperate systems. They found that
to detect large effects with statistical rigour would neces-
sitate over 30 repli cate reserves. Such an experiment
is now possible given the increasing number of marine
reserves implemented across t he world. When read-
ing scientific papers that report non-significant results,
always exami ne the error bars surrou nding the mean or
median values that are reported. If these are large com-
pared to the mean or median (i.e. they have a high error
: mean ratio) then treat their declared 'non-signif icance'
with caution.
 Chapter 15 Disturbance, Pollution, and Climate Change

(0) IbJ
Treatment plot 0 0
o o 0 0
0
o 00 0
o o
o o 0 0 0
8
o o 0
a (ontrol plot 0
0
o 0 0
o 0 0 0
000
o
o 0
0
o 0 0 0
0 0 0 0
0
0 0 0
0 0
0 000
0

X
0

Pseudo-replication Replitation

Figure 15.8 (a) The wrong way to do it! One treatment plot and one control plot each sampled eight t imes. The eight
samples are not replicates of the treatment, they are simple multiple samples of a plot. Multiple samples are taken to
ensure that a representative selection of the biological assemblage is sampled at the correct spatial scale. (b) The right
way to do it! Multiple rep licated treatment and control plots. Each plot is a replicate in an investigation to determine, for
example, the effects of shellfish harvesting on benthic biota (c). Photograph © Gen Broad.

suction dredging) . This is the experimental treatment. The
manipulated treatment will need to be compared with a
control that is not subjected to the treatment.
Good experimental design is dependent upon asking the
correct question at the outset.
An appropriate site needs to be selected, ideally this
should be relatively uniform in nature, with no obvious
additional sources of variation (e.g. riverine discharge at
one end) or these will need to be taken into account in the
eventual experimental design. The chosen site will also
have a representative fauna, as clearly there is no point
investigating the effects ofshellfish harvesting at a site with
no shellfish. The treatment (the act of harvesting) needs
to replicate as closely as possible the intensity and scale of
activity that is normally conducted (Fig. IS.B), otherwise
there is a danger that the results will be open to the accusa-
tion that they are not truly representative of the real activi-
ties they purport to represent. Other factors to consider
might be the seasonality, intensity, and frequency of the
normal harvesting activities.
If an experiment is designed to answer questions about
the effects of a particular human activity, it is important
that the scale and techn iques used to create the treat-
ment effect are representative of the activity of interest.
Having identified a likely site for the experiment it is
important to ensure that there are no strong biological
gradients by taking preliminary samples in a random grid
pattern across the proposed study site. A strong biologi-
cal gradient (i.e. much higher densities of shellfish at one
end of the site) will complicate the process of ascertaining
the effects of the shellfish harvesting treatment but can be
accounted for by using a Latin squares approach that rep-
licates the control and treatment plots across the environ-
mental gradient. However, time and budget constraints
do not always permit the luxury of preliminary sampling,
hence it is important to build additional treatment and
control replicates into the design to ensure that any anom-
alous replicates do notjeopardize the validity of the experi-
ment. It is much better to sample an excessive number of
replicates, as it may not be possible to return and collect
additional samples at a later stage once the experimental
manipulation has been completed.
Preliminary sampling often identifies environmental or
biological gradients or anomalies that may compl icate
later analysis, and enables the calculation of the sam-
pling effort necessary to detect a given level of change
in a variable. Often, the luxury of prel iminary sampling
is not possible, hence the potential pitfall of collecting
too few samp les needs to be acknowledged in the sam-
pling design. It is better to collect too many samples
than too few.
15.3.6 Pitfalls to avoid
This brings us on to a classic pitfall: the difference between
a sample and a replicate. In Fig. 15.8a, a treatment and con-
trol plot are shown. Eight samples have been collected from
each plot, from which it is possible to calculate means and
errors and to generate statistical tests for significant differ-
ences between the two plots in measured variables (abun-
dance, biomass) . But this tells us nothing about the effects
of shellfishing on the benthos. It can only tell us whether

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
one plot is different (or not) compared with the other. The
samples within the treatment and control plots are not rep-
licates. The common pitfall is to treat the samples within
the plots as if they were replicates of the treatment and
control. This is known as pseudo-replication. A properly
replicated design is shown in Fig. 15.8b. Clearly more sam-
pling effort is used, but the treatment and control plots are
replicated (2 treatments x 3 replicate plots x 8 samples) . 50
what can one do if time and budget dictate that this is too
many samples? It is important to preserve or increase rep-
lication at the level that addresses best the initial question.
In this example, if we had to reduce our sampling effort by
half, it would be better to take only 4 samples from each of
3 control and 3 treatment plots rather than taking 6 samples
from each of 2 control and 2 treatment plots. The greater
the level of replication. the greater the statistical power
to detect differences among treatments (Techniques box) .
What can we do if it is not feasible to replicate the treat-
ment? Abandon the experiment is one alternative. but not
very helpful if a scientific study is required for policy advice.
Typically, such an example might occur if the cost of creat-
ing the treatment is prohibitive. as in the study of the eco-
logical effects ofaggregate extraction undertaken by Kenny
and Rees (1996) . Using ships to generate experiments can
be very expensive, typically U5$30 000 per day (or more),
and clearly places a constraint on what can be achieved on
a fixed budget. Kenny and Rees (1996) overcame this prob-
lem by using a Before After Control Impact (BACI) design,
in which both a designated control and treatment plot are
studied priorto any experimental disturbance (Underwood
1991). Once the similarity of these plots was confirmed,
the experiment proceeded. The design is still pseudorep-
licated (there is only one treatment and one control plot)
but we have more confidence that the difference detected
immediately after aggregate extraction is indeed attrib-
uted to the effects associated with dredging (as opposed
to some other random factor) . However, an examination
of this study reveals the weakness of such designs as the
authors were unable to account for changes recorded some
24 months later and were only able to speculate that these
were site-specific changes caused by local physical forcing
due to wave action (Kenny & Rees 1996).
In some cases, a Before, After, Control, Impact experimen-
tal design is the only viable option, but such a design
has far weaker powers of inference than a fully replicated
experiment w ith equal numbers of control and treatment
replicates.
BACI designs are appropriate for the examination of
short-term responses to human interference. but are highly
unsatisfactory for detection of long-term effects. This basic
design could be improved by introducing multiple replicate
control plots th at can be studied for the effects of random
15.4 Agents of change
factors that might also lead to changes in community struc-
ture. For example. if four control plots were studied, three
might exhibit similar changes over time while one of these
might experience a chance settlement oflarvae ofa particu-
lar species that did not occur at the other sites. This design
tells us that we can be more confident that the difference
between the treatment and control sites that we studied are
real effects and not attributed to a chance occurrence.
15.4 Agents of change
15.4.1 Riverine input and land use
The composition and quantity ofriverine discharge into the
shelf seas will affect h abitat composition and biology in the
immediate area of discharge. Globally, this is an important
process given that 70%of the sediment input to the sea is
from riverine sources. although this varies from region to
region (Milliman 1991) (see also Chapter 8) . Dam con-
struction, fluvial management regimes, and the effects of
changing patterns in precipitation linked to global climate
change will all affect the rate and quantity of riverine inputs
in the marine environment. The amount of sediment dis-
charged is related to drainage basin size; the surface area of
a small drainage basin provides lower storage capacity for
sediment than a larger basin. Thus smaller rivers discharge
a proportionately greater load ofsediment per unit ofwater
discharged than much larger systems.
Some 70tyo of sediment input into the sea is derived
from rivers, hence changes in land-use and rainfall are
li kely to have a significant impact on marine communities
in coastal regions.
Some of the world's largest rivers are located in South
America where they are known to play an important role
in structuring the topography and sedimentary conditions
of the adjacent seabed (Amazon and Papuan continental
shelves) . Close to the river mouth the water column is
heavily laden with sediment and results in a distinct layer-
ing of sediment reflecting discrete periods of deposition of
riverine sediment and erosion of the seabed. Consequently
the fauna is highly impoverished in this environment and
tends to be dominated by bacteria (Rhoads et al. 1985).
Field studies demonstrate that the body size, abundance,
and depth distribution of benthic fauna are at their lowest
across the continental shelf coincident with peaks of riv-
erine discharge and maximum trade-wind stress. During
periods of low riverine discharge and minimal wind stress.
macrofauna abundance was highest and bacterial biomass
increased bya factor of two (Aller & 5tupakoff 1996).
The quality a nd quantity of sediment transported by
river systems is affected by the land-use practices that occur
in the river catchment. Deforestation and other agricultural
 Chapter 15 Disturbance, Pollution, and Climate Change

practices have led to substantial soil erosion, such that it

is estimated to be 3.7 times greater than 2500 years ago,
prior to the period when forests were cleared for agricul-
tural purposes. Widespread cultivation ofland in northern
China is considered to have caused the tenfold increase in
sediment discharge from the Yellow River. The increasing
demand for greater areas of agricultural land to support
subsistence farming in developing countries seems likely to
increase the sediment discharge from regionally important
rivers (Hall 2002) .

Deforestation for agricultural purposes has been associ-

ated w ith a 3.7 times increase in soil erosion.

15.4.2 Eutrophication
High nutrient loads in river discharge are associated with
phytoplankton blooms that generate mainly diatomaceous
phytodetritus. This material descends to the seabed where
it fuels high rates of microbial respiration and depletion
of oxygen (a n oxia) at the sediment-water interface (Fig.
15.9) . Such events tend to coincide with periods of calm
weather when inshore waters undergo stratification. The
Baltic Sea, the Adriatic, and the Gulf of Mexico are well-
documented examples oflocations where such events occur
on a regular basis (Turner & Rabalais 1994; Chapter 8) .
Systems that are particularly susceptible to eutrophication
would include those with restricted tidal inundation. poor
water exchange or tho se susceptible to stratification. Typi-
cally such systems include fjordic areas, enclosed bays. and
areas with relatively deep water.
High nutrient inputs into enclosed bays and other areas
prone to water-column stratification have been associ-
ated with eutrophication of coastal waters.
While periodic anoxic events occur naturally. their
extent and severity appears to be related to human influ-
ences. Nitrogen loading doubled in the River Mississippi
berween the WOOs and 1980s, and it is thought that the
increasing scale of anoxic events in the Gulf of Mexico is
linked to eutrophication (Turne r & Rabalais 1994; Box
15.3) . Evidence for this hypothesis arises from srudies of
stable isotope signatures and organic tracers in sediment
cores, which indicate that nutrient levels started to increase
in the 1950s and finally levelled offin the 1980s, coinciding
with a threefold increase in the use of chemical fertilizers
by the agriculrure industry in the latter half of the rwentieth
century (Eadie et al, 1994) . The sources of nitrogen that
Figure 15.9 Although this looks like the aftermath of
an oil pollution incident washing ashore, it is in fact the
product of a phytoplankton bloom die-off off the coast of
Cape Cod (NE United States), lovingly known as'munge'
by local people (the word 'rn unge' or 'rn unq' means to
mash into a mess). The genus responsible for the bloom is
probably Phaeocystis. (Photograph: D. A. Kaiser.)
flow into the Mississippi would appear to be diffuse and can
originate as much as 1000 Ian upstream. thus it is almost
impossible to pinpoint a single major source of contamina-
tion. Arresting the activities of an entire industry will take
considerable scientific proof that requires the elimination
ofother possible causative agents (e .g. climate change) . For
example, hydrocarbon fuel consumption appears to be the
primary source of atmospheric inputs of nitrogen. which
have increased by 50 to 200% over the last 50 years (Paerl
1995).
Sources of nitrogen input into river systems are diffuse
and may occur many hundreds of kilometres from the
sea, but evidence suggests that agricultural run-off is
the primary culprit.
 15.4 Agents of change
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 15.3: Anoxic events in the Gulf of

Mexico
Weather condi tio ns, large-scale physical oceanographic
processes, biological productivity, the amount of nutri-
ent discharge, and other factors affect oxygen depletio n
in coastal waters. The largest zone of oxygen-depleted
waters in the entire western Atlantic Ocean, occurs in
the northern Gulf of Mexico on the Louisiana continental
shelf adjacent to the outflows of the Mississippi and Atch-
afalaya Rivers. In the last decade, the extent of bottom
water hypoxia ( 16 000 to 18 000 km') has been greater
than twice the surface area of the Chesapeake Bay, rival-
ling extensive hypoxic/anoxic regions of the Baltic and
Black Seas. Depending upon environmental condi tio ns,
hypoxia occurs from late February to early Octobe r, but
is most widespread, persistent, and severe in June, July,
and August. See also Justic et al. (2005).

RoDom Dissolved Oxygen Contours

SEAMAP Summer Groundfish Survey
June 14-July 16, 2006 NOAA Ihip Oregon II

Dissolved Oxygen
mgJL
• 0.00-0.10
. 0.11-1.00
• 1.01 -1.10
• 1.11 -2.00
2.01 -2.10
2.11 -3.00
o 3.01 -3.10
o 3.11 -4.00
o 4.01 -4.10
4.11 -1.00
Gulf of Mexi(o • 1.01 -1.10
• 1.11 -6.00
• 6.01 -6.10
• 6.11 -7.00
• 7.01 -7.10
• 7.11 -8.00

Bottom dissolved oxygen concentration as measured by NOAA in mid July 2006. To put this into
context, the extent of the dead zone is greater than that shown in satellite derived images of the
area covered by the Deepwater Horizon oil spill that was finally capped in July 2010 (see Box 15.5).

Mass fish kills, like the one shown here, typically

occur in the vicinity of the Mississippi dead zone.
 Chapter 15 Disturbance, Pollution, and Climate Change

15.4.3 Water use
Clearly the inputs derived from riverine discharge have
an important influence on shelf-sea ecosystem processes.
Consequently, any activity that alters riverine discharge
is likely to have ecological consequences for near-shore
ecosystems . Major dam schemes are responsible for some
striking changes in marine ecosystems. For example, in the
Adriatic Sea, the output of the River Po and adjacent river
systems has been lowered by 12% in the recent years. The
reduction in nutrient inputs has been associated with a
decrease in primary production in the local shelfwater mass
(Alongi 1998). The structure of many river delta regions is
maintained by the supply of suspended riverine sedime nt.
Accretion of the Nile delta was reversed after the construc-
tion of the barrage on the River Nile in 1868, and further
exacerbated with the construction of the Aswan dam. The
reduction in supply of riverine sediment to the coastline led
to coastal eros ion rates of between 5 and 240 m per year.
The associated reduction in nutrients transported out to sea
was linked with a decline in landings from fisheries for both
pelagic and demersal fisheries (Box 15.4). In later years,
fishery production increased as the reductions in nutrients
supplied through the Nile discharge were replaced through
coastal urbanization and the concomitant increase in dis-
charge of sewage into the River Nile (Nixon 2004).

Box 15.4: Effects of damming the River

Nile
Catches of commercially important fish species (a) fell
dramatically after closure of the Aswan High Dam in
1964. Both demersal (jacks, mullets. bass, and redfis h)
and pelagic (herring, sardine, and anchovy) fish landings
remai ned low until 1980 when they rose steadily. Shrimp
landings (b) showed similar trends but have never recov-
ered to levels experienced prior to closure of the Aswan
(0) 8D DDD
70DDD
High Dam. The declines in fisheries are in part thought to
relate to the fall in phosphorus and nitrogen released into
the Mediterranean Sea from the River Nile. (c) However,
as populations along the river expanded it seems highly
probable that inputs from sewage have offset the loss of
nutrient input as a result of closure of the Aswan High
Dam. Reproduced with permission from American Scien-
tist 92: 156-16 5.
Ib) 80Doo ,
70Doo - Damdoses

-
:=- 60 DDD
•§ 50000
• Jocks, mullets
• Red/ish, boss
• Herrings, sardines, ollChovies
-
:=- 60 Doo
•cc
0 50000
=
0

-
=

-...
ac 40000
-g> 40000

--
c
c 0
0 30000 30000
,/ Domdoses E
~
20000 20000
, ~
~

10000 10000
0 0
1960 19m 1980 mo 2000 1960 1970 1980 1990 2000
Year Year

('I Nile Mediterranean

6700 tonnes
4000-8000 tonnes phosphorus
dissolved attached to sedimen
nitrogen "-- '

...
•• Water treatment pla nt

Sediment
--- 108000 tonnes
16000 tcnnes nitrogen
~ Dam phosphorus

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Reductions in riverine discharge, as a result of water
abstraction and dam construction, affect coastal erosion ,
primary production , and commercial fisheries. River sys-
tems that are subject to damming may be more adversely
affected by climate change related changes in precipita-
t ion .
15.4.4 Hydrocarbon exploitation
The extraction of oil and gas from the sea inevitably
releases hydrocarbons into the marine environment as a
result of drilling activities, and in the past, due to the use
of contaminated drilling mud (Olsgard & Gray 1995) . The
ecological effects of the addition of fine sediment to the
seabed beneath drilling platforms and the contaminants
within drilling mud are associated with a localized reduc-
tion in species' diversity. These effects are ameliorated with
increasing distance from the drilling platform. In the case
of gas platforms in the Gulf of Mexico, community changes
are confined to within 100 m of the drilling platform (Mon-
tagna & Harper 1996) . However, in the North Sea, the
cumulative effects of using drilling mud over periods of up
to nine years, led to ecological changes at distances of up to
6 km from the drilling platform. However, the more recent
use of water-based drilling mud has considerably reduced
adverse ecological effects on seabed communities (Olsgard
& Gray 1995). The pollutant effects ofdrilling activities are
far less dramatic than the impacts of accidents that occur
while carrying oil in bulk across the oceans.
Understanding the negative ecological effects of the
contaminants in drilling mud has prompted the oil and
gas industry to seek more environmentally friendly alter-
natives.
High-profile examples of oil-spillage incidents include
the grounding of the MV Exxon Valdez off Canada and the
MV Braer off the Shetland Islands or the destruction of oil
pipelines and refineries during the Gulf War. The ground-
ing of the MV Braer differed from most oil spill incidents in
that it coincided with extremely severe storm-force winds
that were maintained for a number of weeks. The result-
ing sea conditions meant that the oil was highly dispersed
by natural wave action (Box 15.5). However, when a ship
runs aground, the good news is that the potential amount
of oil that can be spilt into the ocean is understood from
the cargo capacity of the vessel. These spills were miniscule
compared to the recent Deepwater Horizon oil well blowout
in the Gulf ofMexico. As oil resources become more scarce,
oil companies are attempting to drill for oil in waters below
15.4 Agents of change
1000 m deep. Exploration of the deeper parts of the ocean
incurs greater risk as it becomes logistically more difficult
to control drilling operations. Experts have estimated that
BP's Deepwater Horizon well leaked 4 .9 million barrels of
oil into the Gulf ofMexico before itwas capped inJuly2010.
This was not the first time a leak of this scale had occurred
in the Gulf of Mexico, where the Ixtoc Ileakissued 3.3 mil-
lion barrels of oil in 1979. While the Deepwater Horizon
grabbed a lot of headlines, it is a one-off incident and per-
haps not much bigger (in terms of its ecological impact)
than the annual 'dead zone' that occurs off the Mississippi
delta (see Box 15.3).
Technology for dealing with these incidents, and our
understanding of the ecology of the biological recovery pro-
cesses that occur after such incidents, are much improved.
Indeed, it is often ecologically better to leave natural eco-
logical processes to degrade oil spills rather than to inter-
vene with the use of chemical dispersants. The use of
dispersants is often driven more by aesthetic demands to
preserve the appeal of tourist beaches, rather than on any
scientific grounds. In the early 1970s, the oil dispersants
used to clean beaches after the MV Torrey Canyon oil spill
were more harmful to organisms than the oil itself (South-
ward & Southward 1978). Nowadays, dispersants are much
less toxic and bioremediation of oil-contaminated habitats
is enhanced by the use of bacterial digestion to speed the
breakdown ofthe oil.
The use of dispersants on oil spills can have more severe
ecological consequences than if the oil were permitted
to biodegrade. However, social and economic issues
often dictate that unsightly oi l needs to be removed from
tourist hotspots, and thereby override ecological consid-
erations. The process of degradation can be accelerated
by the addition of 'oil-eat ing' bacteria.
15.4.5 Mining geological resources
Advances in marine technology have made the mineral
resources of the seabed accessible in a wide range of dif-
ferent marine environments. These range from relatively
shallow coastal waters, where sand and aggregate (gravel)
are extracted, to deep-sea mining of manganese nodules
on the abyssal plain, to diamond dredging off the coast of
Namibia. In each of these examples, sediments are removed
directly from the seabed (usually via a dredge head) and the
desired products extracted on board the vessel at the sur-
face . Not surprisingly, these activities represent an intense
localized disturbance to the seabed and completely alter the
biological and geological composition of the habitat.
 Chapter 15 Disturbance, Pollution, and Climate Change
Box 15.5: Impact of oil on the marine
environment
Crud e oils and petroleum products are complex sub-
stances, typically most of the volatile fractions evaporate
into the atmosphere shortly aft er they have been released
into the environment The heavier fractions are then
exposed to a variety of physical, chemical, and b iological
processes according to the prevailing weather conditions.
For example, aerosols and emulsions are for med as a
result of wave action, while exposu re to ultraviolet light
leads to photo-oxid ation at the surface of the sea. Persis-
(. J Largesl accidental oil spills
Million ba rrels
0 1 2 3
Deepwater Horizon, well
USA,201 0
htec1, well
Mexico, 1979
Nowruz Field, well
Persian Gulf, 1983
Amoro Cadiz, lanker
Fro me, 1978
TorreyCanyon, lanker
UK, 1967
ExxonValdez, lanker
USA, 1989
Most aggregate extraction is permitted under licenses
granted for defined areas of the seabed. Improvements
in satellite navigation systems have enabled more accu-
rate compliance with these licenses by aggregate com-
panies, but also enable stricter enforcement through the
use of 'black box' recorders that log vessel movements.
ten t rough seas contribu ted to emulsification of the oil in
the MV Broer incident and helped the rapid dispersal of
the oil. Oil tankers may run aground frequently, but they
are small incidents co mpared to the recent BP Deepwater
Horizon well blowout (a). Of the 4.9 mill ion barrels of
oil leaked into the Gulf of Mexico from the Deepwater
Horizon well , 800 000 barrels were collected using spe-
cialized booms to gather the oil for removal by specialized
'clean-up ' vessels. The hot cli mate in the Gulf of Mexico
would have hastened the evaporation of the more toxic
lighter fractions of oil.
(b) Thefoolprinl ofthe Deepwater Horizon oilspill asof26 July2010 Ibl.Thegrey
areasonthemap depid theextent ofthespill os esrerfuiaed fromthesheenfromthe
4 S ail allOlysedfro msatelliteimagery(source NOAA).
.:."II..,.-'" .
....
Extent of sli(kvisible in
; ~Ofell it e imogery, July267010
Deep'/iCfer horizon MC742
imidenllc(cticn
I~ , I I
"'
I
M'lts
I ! , 1~ I
(() Satellite derived imageIe) of thesameoilspill. Photo: NASA.
The demand for raw materials to supply housing and
construction projects is unlikely to decline in the foresee-
able futu re, and Charlier and Charlier (1992) predicted that
production would reach 200 million tonnes for the United
Kingdom alone in the next century. Extrac tion of marine
aggregate in the United Kingdom has increased from 7 mil-

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
lion tannes per annum in 1969 to a relatively constant fig-
ure ofapproximately22 million tannes per annum between
1989 and 2003. Dredging ofaggregates and the disturbance
of the seabed generated by towed bottom fishing gears has
some similarities in terms of their ecological effects on ben-
thic biota and habitats. However, while fishing activities are
widespread, aggregate dredging is confined to restricted
areas thatare strictly controlled through licensing schemes.
However, dredging is a much more intensive activity, and
removes the habitat to depths of up to 1 m , Hence, recovery
of the habitat is a key process in determining the rate of
recovery of the biota associated with that habitat (Dernie
et al. 2003; Fig. 15.2).
Aggregate extraction causes intense, but localized , dis-
turbance of the seabed that can lead to long-term habi-
tat alteration lasting in excess of several years.
Kenny and Rees (1996) used a commercial gravel
dredger to remove 50 000 tonnes of aggregate off the
east coast of England. 'IWo years later. the sediment com-
position in the area from which the aggregate had been
removed was still dominated by particles finer than in a
comparable control area. and was much more prone to
resuspension as a result of wave action. This is perhaps
not surprising given that habitat recovery is likely to
occur as a result of the active transport of gravel material
into the site, a process that requires highly energetic pro-
cesses (violent storm activity and strong seabed currents) .
Although species' diversity was restored after two years.
the biomass of many of the longer-lived species remained
greatly reduced (e .g . the horse mussel, Modiolus modio-
lus) . The natural disturbance regime at individual sites
will determine the rate of habitat and biological recovery
that is likely to occur as a result of dredge disturbance
(Hall 1994) .
Fears of shortages of metal resources in the early 1970s
sparked interest in the idea of mining manganese nodules
in the deep sea. Manganese nodules contain metals such
as iron. manganese, copper. nickel, cobalt. zinc. and silver.
Dredging for manganese nodules involves the use ofremotely
operated seabed vehicles that crawl along the seabed scoop-
ing up surface deposits. and thereby create a furrow in the
seabed surface. Experimental studies have demonstrated
(not surprisingly) that the dredging process reduces both
habitat and species' diversity within the dredge track, and
produces a sediment plume. Sedimentation at these depths
occurs at the rate of a few millimetres every 1000 years. As
a result. dredge tracks will persist for many years creating
long-term changes in deep seabed topography, while filter-
feeding organisms may be adversely affected by the unnatur-
ally large pulse of sediment that settles out of the plume
(Theil & Schriever 1990).
15.4 Agents of change
Early excitement regarding the feasibility of deep-sea
mineral extraction subsided with a reduction in the
stock market value of commodities such as copper and
cobalt.
Mining minerals at extreme depths is an expensive busi-
ness and only likely to become economically viable when
the combined nickel, copper, and cobalt content of the
manganese nodule exceeds 2.5% at an abundance of > 10
kg rrr-. Only a few regions in the Pacific Ocean and from the
Central Indian Basin in the Indian Ocean meet these criteria.
Economic-grade manganese nodules are generally found in
the middle of the ocean in water depths exceeding 4500 m .
Manganese nodules would have to be lifted at the rate of 3
million tonnes per year for 20 years at an individual mine
site covering an area> 6000 km 2 to make such a proposition
economically feasible. The lower costs associated with the
terrestrial mining of these metals mean that mining in the
deep sea is likely to remain on hold for the foreseeable future
although there are indications that the demand for minerals
in China will make this financially feasible (Glasby 2000; see
also http:/ /www.whoi.edu/workshops/deepseamining for
further insights into deep-sea mining).
15.4.6 Contaminants
In addition to concern regarding the effects of elevated
nutrient inputs into coastal waters. there is considerable
concern over the long-term and often subtle effects of per-
sistent contaminants in the marine environment. Many of
these contaminants, such as radionuclides and organic
substances, are derived from industrial and heat-gener-
ation sources. Polychlorinated biphenyls (PCBs) are
particularly persistent and accumulate through the food
chain with negative effects expressed in top predators. For
example, PCB contamination of prey has been linked to
hatching failure for a number of avian predators, while
contaminants such as mercury occur in higher concentra-
tion in the feathers of seabirds sampled in the latter half of
the twentieth century. compared with those sampled from
museum collections (Arcos et al. 2002) . While the effects
of such contaminants on apex predators have been well-
documented, the effects on organisms at lower trophic
levels is less well-studied. Although invertebrates such as
amphipods are used in lethal toxicity tests, the incidence
of contaminant mortality associated with bioengineer-
ing organisms (Chapter 8) that affect habitat structure
remains unknown. The effects of contaminants may be
subtle in that they do not necessarily cause direct mor-
tality but may have negative population effects via their
influence on recruitment processes and larval viability.
For example, Atlantic croaker (MicropogoniC15 undulatus)
 Chapter 15 Disturbance, Pollution, and Climate Change

larvae exposed to the chemical Aroclor 1254 have signifi-
cantly reduced growth rates and are less capable of evad -
ing predator stimuli (McCarthy et a1. 2003) .
Contaminants can have subtle sub-lethal effects that
affect the performance and subsequent survival rate of
organisms. Larval stages are particularly vulnerable to
these effects that are easily overlooked .
Abnormalities in the growth and reproduction of a
number of different molluscs became apparent in the
mid-1980s. Symptoms included reduced growt h, shell
deformation, and declining population abund ance in spe -
cific localities. In particul ar, dogwhelk (Nucella lapillus)
populations had become locally extinct in the United King-
dom and elsewhe re, usually in localities close to harbours
and ports . The most striking symptom associated wit h
these declines was the occurrence of imposex. Imposex
is manifested in female gastropods by the development of
a vas deferens and in some cases a penis, which lowers
reproductive success. Not all molluscs exhibited the same
symptoms; po pulations of Littorina li ttorea had lower
egg production, while oysters developed thickened and
deformed shells (Matthiessen et a1. 1995). The causative
agent was identified as tributyl tin (TBT) based anti-foul-
ing paint that was used on the hulls of boats. Legislation
has since banned the use of this paint on certain categories
of vessels and has been associated wit h a recovery in mol-
lusc populations in countries where its use is restricted.
A much more rece nt issue of concern is the possible
effect of different types of man-made nanomaterials and
nanoparticles on natural systems and organisms. This
area is well reviewed by Handy et a1. (2008) . Nanopar-
tides have occurred naturall y since the formation of the
Earth, but latterly humans have begu n to manufacture
specific nanoparticles (NPs) w ith particular properties
(Table 15.2) . Manufactured NPs could be carbon-based
(carbon spheres or nanotubes), metal-based, compos ite,
or multi-layer NPs (e.g. platinum core- silica shell) . Conse-
quently, commercially available nanoproducts are di verse

Table 15.2 Location of nanoparticles in the natural environment, the types of particles and their
ecotoxicological potential. Reproduced from Handy et al. (2008).

Particle types and ecotoxicological potential

••••••••••••••••••••••••••••••••••••••••••••••••••• ••• ••• ••• •••••••••••••••••••••• ••• ••• ••• ••• ••• ••• •••••••••• ••• ••• ••• ••• ••• ••• ••• ••••••••••••• ••••
Volcanic dust
Bismuth oxide nanoparticles were found in the stratosphere in 19 8 5, and the presence of these materi als was linked
to volc anic eruptions in the 19 8 0 s.

Ocean surface microlayer (SML)

Contains colloi ds, sub-micron components of phytoplankton, and carbon particles. Functions in t ransport of mat erial at
the ai r-water interphase. There are concerns that organic pollu tants present in t he SML may be adsorbed to colloi ds
and other nano-scale material in the SML.

Freshwater
Nat ural freshwater contains very com plex colloid material, which includes inorganic minerals and organic matter such
as humic substances. Concerns exist over the accumulat ion and t ransportation of NPs in the colloid fraction.

Other natural waters

Nanopart icles were found in many types of natural w ater including the oceans, surface waters, groundwater, atmospheric
w ater, and even treated drinking w ater. These include a wid e variety of nanoscale mineral particles, and demonstrates
the ubi quitous nat ure of nanoparticles in the natural envi ronment.
• •••••••••••••••• ••• ••• ••• ••• ••• •••••••••••••••••••••• •••••• •••••••••••••••••••••••••••• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
Ice cores
Carbon nanotubes, carbon full erenes, and silicon dioxide nanocrystals have been found in 10 OOO-year-old ice cores.
The carbo n nanopart icles are assumed to be derived from natural combustion processes and deposi ted into the ice
core via at mospheric deposition.

Historic sediments
Examination of th e Cretaceous- Tertiary (K-T) bou ndary layer at Gubbio, Italy showed iron particles (hematite) and
silicates. The average particle siz e of the hemat ite was 16- 2 7 nm. There is specul ation tha t meteorite impacts coul d
alter NP format ion in sediments at the K-T boundary.

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
and offer many potential applications that include elec-
tronics, optics, textiles, medical devices, cosmetics, food
packaging, water treatment technology, fuel cells, cata-
lysts, biosensors, and agents for environmental remedia-
tion. The small size of nanoparticles means that they affect
sub-cellular level processes and are consequently complex
to understand. Furthermore, how they become integrated
into the marine environment and then integrated into
organisms is equally complex. For example, in marine
surface waters the small size of NPs means that they will
be dominated by Reynolds' number (Chapter 3) and this
will affect the diffusion ofNPs and lead to trapping of high
concentrations of NPs in the ocean surface microlayer.
Organisms that are in intimate contact with this ocean sur-
face microlayer (e.g. eggs, fish larvae, zooplankton) may
therefore be particularly vulnerable to any effects associ-
ated with NPs. Organisms associated with biofilms or the
sediment surfaces may be affected similarly.
See Evans et al. (2000) for the controversy surrounding
potential replacements for TBT.
15.5 Climate change
So farwe have examined the effects of human activities that
have relatively restricted spatial effects on communities or
particular groups of animals. However the potentially sig-
nificant consequences of global climate change for marine
systems and activities affect all regions of the planet at both
small and large scales (Hall 2002) . Those changes likely to
occur in response to global warming include : sea-level rise,
water-column warming, precipitation, wind speed and
patterns, water-column circulation, and the frequency and
intensity of storms. We give only a few examples ofenviron-
mental changes that might affect marine ecosystems.
15.5.1 Temperature effects
Global warming is likely to affect biological processes and
biodiversity in the oceans. Rising temperatures may result
in a reduction in the equator-to-pole temperature gradi-
ent. The frequency of El Nifio-like conditions in the tropi-
cal Pacific will probably increase, with the eastern tropical
Pacific warming to a greater extent than the western tropi-
cal Pacific (lPCC 2000) . In conjunction with hydrographic
conditions, temperature plays a significant role in deter-
mining the biogeographic distribution of species and we
can undoubtedly expect to see changes in species' distri-
butions with climate change (Chapter 1) . For example, a
northward extension of warmer conditions may enable the
merger of the currently geographically disjunct distribu-
tions of warm temperate species, such as the commercially
15.5 Climate change
important clam Mercenaria mercenaria and the eastern
oyster (Crassostrea virginica) . The present northern limit
of these species is Cape Cod on the eastern seaboard of the
United States, although isolated populations are found fur-
ther north in the warmer waters of the Gulf of St. Lawrence.
These temperature changes are also likely to extend the
spread of some non-native species that have been intro-
duced through ship's ballast water or other practices, such
as aquaculture . Many introduced species are considered
to be pests, as they predate commercially valuable shell-
fish ; for example, the green crab (Carcinus rncencs) that
has become established on the western coast of the United
States and in Australia.
Increasing sea temperatures will extend the poleward
distribution of low-latitude species and may enhance the
geographic spread of non-native invasive species.
We have already seen in Chapters 5, 7, and 8 that
semi-enclosed water bodies are prone to anoxic events as
a result of stratification of the water column and oxygen
depletion at the seabed. The frequency of such events may
increase as warmer temperatures lower the oxygen carry-
ing capacity ofwater, while the biological oxygen demand
of the biota will increase. Lower oxygen carrying capacity,
coupled with eutrophication, will increase the likelihood of
such events, which may have more frequent adverse effects
on coastal fisheries. Temperature effects on fisheries are
of particular concern since water temperature is a strong
predictor of fish distributions, the timing of spawning,
growth rate, and survival oflarvae (Heath 1992; Lehody
et at. 1997). In the coastal waters of the USA, for exam-
ple, a reduction in the spatial extent of oxygen-rich, cool
water may cause concomitant changes in the distribution
of striped bass (Morone saxatilis) (Coutant 1990). Further
increases in global sea temperature are likely to cause new
combinations of species mixes both in fish and benthic
assemblages .
Coral bleaching is an increasing global phenomenon
(Harvell et at. 1999) that occurs when the symbiotic zoo-
xanthellae are expelled, algal pigmentation is lost, or
both scenarios occur, giving the coral tissues a 'bleached'
appearance (Chapter 11) . These events have been linked
with exceptionally high seawater temperatures, elevated
doses of ultraviolet radiation, infection by pathogens, and
the alteration of local salinity regimes. The degradation
of coral reefs has important economic consequences for
local communities that often depend on reef-related eco-
tourism and associated fisheries as an important source of
Income .
Coral bleaching has severe implications for artisanal fish-
eries and eco-tourism.
 Chapter 15 Disturbance, Pollution, and Climate Change
15.5.2 Change in rainfall
The effects of climate change on rainfall may be impor-
tant given the influence of river and land run-off in estua-
rine and coastal systems (Chapters 5 and 8) . The effects
of increasing rainfall can also combine with tidal surges
resulting in a greater intensity of coastal and flood plain
inundation (Fig. 15.10) . Rainfall is a prominent seasonal
feature in areas of the tropics especially where monsoon
rains occur. Global predictions ofchanges in rainfall suggest
little change in southeast Asia and South America. where
riverine influences are especially important, but potential
small increases (5 to 20%) for the Indian subcontinent, East
Asia, Canada, and Northern Europe and potentially large
increases ( >20%) for Northern Asia and the Sahara (lPCC
2000) . Even if these predictions are accurate. it is difficult
to ascertain their consequences given the changing use of
water abstraction with industrial growth in many of the
countries affected . Changes in the quantity of freshwater
discharged from estuaries into coastal waters will affect the
intensity of stratification that occurs along the density gra-
dient formed in the Region of Freshwater Influence (ROFl,
Chapter 8) . Thus the changes reported in Table 15.3 are
likely to lead to an increase or decrease in the strength of
alongshore density driven currents which may have impor-
tant ecological consequences for the dispersal oflarvae and
propagules and other organisms associated with fronts.
30
• Tidal
2l • Fluvial and 'incombination'
--
~
~
~
20
-
0
~ deira & Wickett 2005) . Such large-scale changes in ocean
0 15
~
~
~
E
~ 10
z
5
Figure 15.10 The increasing frequency of closures of
the River Thames barrier in recent years is one indication
of the increasing effect of elevated rainfall and greater
incidence of tidal surges and sea level change (King
2004).
15.5.3 Water circulation
Intensification of alongshore wind stress on the ocean sur-
face may already have increased coastal upwelling inten-
sity (Bakun 1990) . As many of the most productive marine
regions in the world occur in regions of intense upwelling,
the potential for climate change to affect fisheries seems
highly likely (Bakun 1990) . Recent anomalous changes in
the upwelling of cool, nutrient-rich water off the coast of
the western United States led to an extensive anoxic event
resulting from unusually high productivity. Extensive areas
of the seabed from the continental shelf edge to within 700
m of the surf zone were severely oxygen depleted. resulting
in mass kills of commercially important fish and shellfish
species (Grantham et at. 2004) . Changes in wind patterns
may alter wind-induced currents that are important for
larval transport, which means that larvae may no longer
be conveyed to habitats suitable for further development
(Heath 1992) .
15.5.4 Ocean acidification
Levels of atmospheric carbon dioxide (CO,) are rising and
are reducing oceanic pll, causing shifts in seawater carbon-
ate chemistry (Doney et at. 2009) . This process, termed
ocean acidification (OA), has seen our oceans absorb up
to a third of atmospheric CO 2 since the onset of the Indus-
trial Revolution (Sabine et at. 2004) . Increasing the con-
centration of CO2 disrupts the natural buffering capacity of
seawater towards higher concentrations of carbonic acid,
dissociating into hydrogen (H+), bicarbonate (HCO,), and
carbonate ions (CO~~; eqn 15 .1) . Increased H+ production
already has caused the pH of seawater to decrease from a
pre-industrial pH of 8 .16 to present levels of pH 8.05 (Gui-
notte & Fabry 2008) and is forecast to decrease further
by 0.3-0.5 pH units at the end of this century, equivalent
to a 100-150 % H+ increase (Houghten et at. 2001; Cal-
pH are the greatest experienced over the last 300 million
years (Caldeira & Wickett 2003) but continue to rise at an
accelerating rate outstripping even the most pessimistic of
projections.
CO 2 (arm) iii CO 2 (aq) + H,D iii H2C03 1i1 H+
+ HCO,IiI 2W + CO;- (15.1)
The organisms most at risk are marine calcifying organ-
isms (i.e. molluscs, echinoderms. crustaceans) that biomin-
eralize carbonate (CO~~) and calcium (Ca 2 +) ions to form
calcium carbonate (CaCO,) skeletal or shell structures
(eqn 15.2) (Current Focus) . As more CO 2 enters oceanic
surface waters. the seawater's natural buffering capac-
ity steals away these vital carbonate building blocks that
are required for calcification by converting the reactive
H+ and CO;- ions towards more stable HCO, (eqn 15 .1) .
Thus the availability of these carbonate ions (referred to
as the saturation state) will determine whether organisms
can successfully deposit their vital CaC0 3 scaffold. Seawa-
 15.5 Climate change
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 15.3 Mod elled river discharge und er present day and future rainfall scenarios, showing th e difference in
discharge for wate rsheds w ith or w it hout dams.
I

Discharge 1960s Discharge 2050s Relative change

(km ' yr-') (km' yr-') ("!o)
Africa
Dam unirnpacted Kouilou 28.4 20.0 - 2 9 .6
Cross 59.9 61.8 3. 1
Chari 29.1 34.3 17 .9
Dam impacted Seneg al 5.7 2.5 - 5 6 .0
Congo (Z aire) 1349.0 1267.5 - 6 .0
Volta 32.8 4 8 .1 46.7
•• •••••••••••••••••••••••••••••••• •••••••••••••• ••••••••••• ••••••• ••••••• ••••••• ••••••• ••••••• •••• ••• •••• ••• •••• ••••••• ••••••• ••••••• •••• ••• •••••••
Asia
Dam unirnpacted cs 22.3 20.8 - 6 .7
Chu Salween (Thanlwin) 98.5 13 5 .2 37.2
Nad ym 16 .0 26.5 65.9
Dam impacte d Ku ra 22.0 13.7 - 3 7.8
Ganges-Brahmaputra 1 186.9 13 8 8.4 17.0
Indus 121. 2 174 .6 4 4 .1

Australasia
Dam unirnpacted Merauke 1.5 0.9 - 4 0 .6
Fly 13 5.4 147 .5 9.0
Sepik 10 0 .7 13 3 .6 32.7
Dam impacted Murray 1 1.1 9.5 - 14 .3
Ramu 32.7 4 0 .1 22.8

Europe
Dam unimpacted Adour 6.5 6.2 - 4 .9
Pechora 142.0 174. 1 22.6
Mezen 26.5 32.8 23.8
Dam impacted Kuban 13 .0 9.7 - 2 5 .1
Volga 23 4.0 2 46.3 5.2
Severn, Dvina 101.2 12 3 .4 2 1.9

North and Central America

Dam unimpacted Patuca 12 .3 3.4 - 7 2 .0
Yu kon 187.2 246.0 3 1.4
Kobu k 0.2 0.8 212.2
Dam impacted Grande de Matagalpa 30. 1 7.7 - 74 .3
Mississippi 530.6 540.0 1.8
Colorado 1.3 2.4 8 1.6
•• ••••••• ••••••• •••• ••••••• •••••••••••••• ••••••••••••••••••••••••• ••••••• ••••••• ••••••• ••••••• ••••••• •••• ••• •••• ••••••• ••••••• ••••••• •••• ••• •••••••
South America
Dam unimpacted Coppename 10 .7 0.7 - 9 3 .4
Essequibo 155. 1 78.8 - 4 9 .2
Santa Cruz 0.9 1.0 17 .3
Dam impacted Parnai ba 26.6 5.0 - 8 1.2
Am azonas-Orinoco 6802 .4 5536.5 - 18 .6
Doce 2 4 .4 33.4 37. 1

The authors used a HadCM 3 cli mate-change mode l under the A2 scenario to generate their outputs. What is clear is that the
changes in rainfall and hence d ischarge vary considerably from one region to another. In some cases, rivers with dams show much
greater changes relative to more 'natura l' free-flow ing river systems. The conclusion is that habitat restoration and naturalization
of river systems may be important to develop resilience to climate driven changes in precipitation (Palmer et al. 2008).
 Chapter 15 Disturbance, Pollution, and Climate Change

CURRENT FOCUS: Ocean acidification

Labo rato ry-based expe riments have confi rmed that
high CO 2 conditions impact marine calcifyi ng organisms
through changes in calcification rates (increased and
decreased) , and via distu rbance to physiological and
metabolic processes (Ries et al. 2009). Such expe riments
are extremely important in aiding our understanding of
how organisms might react to GA. However, most of these
tri als are short-term relat ive to the organism's average life-
span and do not rep licate the chronic effects of OA that
will span decades. Chronic exposure to increased CO2 may
have complex effects on the growth and reproduct ive suc-
cess of calcareous marine organisms (Doney et al. 2009)
and could induce physiological acclimat ion or flexibili ties
that are not observed in short-term experiments. Long-
te rm experiments currently in prog ress will be essential to
det erm ine whether calcifying org anisms can demonstrate
acclim ation to this rapid ly changing envi ronment.
Marine volcanic vent sites (Chapter 9) reduce seawa-
te r pH and provi de insights into the poten tial implications
of OA. Com mun ities abund ant with calcareous organisms
loc ate d beyond the vents shift towards com munities that
lack corals and have significant reductions in sea urchi ns
and coralline algae (Hall -Spencer et al. 2008). Fu rthe r-
more gastropod shells dissolve increasi ng their risk of
predation due to the reduced carbonate satu ration state.
Further work on these natural underwater OA laboratories
is required to better understand the implications of OA and
how communities coul d be affecte d as preli minary obser-
vations do not bode well fo r the futu re of calcifying organ-
isms. Comparat ive stu dies using natural systems can be
complicated by the effects of confounding variables that
make it diffi cult to arrive at unambiguous conclusions. Hall-
Spencer et al. (2 0 0 8 ) chose thei r sites carefully such that coralline algae) at a mean of pH 8.2 but few epiphytic
all vents were at ambient temperatu re and there were no calcifiers (only bryozoan s such as Electra po sidoniae)
differences that relate d to chemicals such as arsenic and occurred on seag rass fronds at mean pH 7 .6. (d , e).
sulphu r that are often associated with other vent systems. Photos: Riccardo Rodolfo-Metalpa.

Observational evidence of the effects of

acidification
Figure (a) shows a Posidonia oceanica seagrass
meadow located at a shallow CO2 vent at a depth of 2
m off the Italian coast (Ischia). This location provided
an opportunity to undertake a comparative study of
calcifying organisms that occurred in close proximity
to a source of elevated CO 2 (Hall-Spencer et at. 2008).
Photo: Riccardo Rodolfo-Metalpa.
Martin et al . (2008) examined calcifying epiphytes on
the fronds of the Posidonia oceanica that occurred in They also examined rocky shore communities at the
seawater with different pH values (b, c). Fronds of sea- CO 2 vents. In locations where the seawater had a mean
grass were heavily fouled by epiphytic calcifiers (mainly pH 8.13 , they found abundant calcify ing species, such

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
as coralline algae, Paracentrotus Iividus, Mytilus 90110-
provincia/is, and barnacles (f), but where seawater had a
mean pH 7.79, coralline algae were absent and limpets
such as the Patella caerulea (9) showed signs of severe
shell dissolution . Photos: Riccardo Rodolfo-Metalpa.
Colonies of the symbiotic coral Cladocora caespitosa
(h) were transferred into the vent area and showed live
polyps but skeletal dissolution after 3 months at pH
7.43 (i). Photos: Riccardo Rodolfo-Metalpa.
Experimental evidence of the effects of
ocean acidification
In order to survive, marine calcifiers must be able to con-
tinue to populate through reproduction to display possible
adaptations tow ards OA Early life-stages are the most
sensitive part of an organism's life cycle, and therefore
15.5 Climate change
most likely susceptible to OA. Furthermore, some larval
species, such as echinoderms, form skeletal structures in
a yet more readily soluble form of CaC0 3 : magnesium cal-
cite. Labo ratory studies of larval responses to OA are lim-
ited and have so far demonstrated inhibitory effects that
increase the risk of recruit ment failure under conditions
of OA Notable effects include reduced sperm swimming
speed, red uced egg size and fertilization success, as well
as increased occurrences of abnormalities and mortal-
ity. However, these larvae have been derived from adults
not previously exposed to high COz conditions. Although
these trials do indicate the underlying stress responses of
larvae, they do not offer enough information on an organ-
ism 's ability to acclimate and adapt towards OA. Experi-
ments currently in progress have observed abnormal
development of larvae obtained from adults previously
exposed to high COz' as well as reduced survival 0).
OA is a recent phenomenon wi th key research emerg-
ing only wi thin recent years. It is evidently clear that many
organisms can display detrimental reactions towards OA,
while others appear to be able to compensate for it, but at
what cost? We still have much to learn about OA's impacts
on our oceanic flora and fauna from the individual level to
food-web impacts.
•• •
- ...- .... -
.~
Psammechinus miliaris sea urchin larvae derived from
adults exposed to normal concentrations of CO2 (right)
and high concentrations of CO2 (left). The larva on the
right shows abnormal development. The scale bars =
100 ~m (photographs Coleen Suckling).
 Chapter 15 Disturbance, Pollution, and Climate Change
ter saturated with CO~- allows organisms to biomineralize
their CaC0 3 structures, but in undersaturated conditions
they cannot. Marine CaC03 is typically secreted in two main
forms: calcite and aragonite (aragonite is 50% more soluble
than calcite) . The stability of each form is governed by the
amount of available CO~-, temperature, salinity, pressure,
and a stoichiometric solubility product for each form (Feely
et al. 2004) . These factors determine the depth at which
calcite and aragonite become undersaturated, known as the
saturation horizon. Below this depth boundary, organisms
that utilize CaC0 3 for biogenic structures will be vulner-
able to dissolution. The elevated partial pressure of CO,
has increased its depth of influence in the ocean and has
contributed towards the upward shoaling of the carbon-
ate saturation horizon by 50-200 m over the last 200 years
(Sabine et al. 2004) . This has narrowed the depth range
over which organisms can calcify normally. Models forecast
further upward shoaling of this saturation horizon, caus-
ing surface waters to become undersaturated with respect
to aragonite in many parts of the oceans by the end of this
century, although parts of the Southern Ocean already are
undersaturated (Orr et al. 2005) .
CO'3- + Ca' + ~ CaCO3 (15.2)
Geographic location will playa key role to the extent
of OA's effects on marine calcifying organisms. Colder
waters naturally retain more CO 2 and are more acidic than
warmer waters (Guinotte & Fabry 2008) . As a result, satur-
ation states are highest in shallow, warm tropical waters
and lowest in cold, high latitude regions (Feelyetal. 2004) .
There is particular concern over the future of polar marine
organisms that are uniquely adapted towards their cold sur-
roundings. In an environment where larval and adult devel-
opment is ten times slower than in warmer regions of the
world, the ability for organisms to adapt to these changing
conditions is highly questionable.
Changes in wind stress may intensify coastal upwelling
and have been linked already to anomalously high produc-
tion and mass kills of commercially important fisheries.
15.6 Interaction of multiple
factors
We have provided a sample of the influence of human
activities on the marine environment. We have dealt with
each of these factors separately for simplicity, but multiple
factors may operate at the same time or in sequence. While
one factor on its own may not have serious consequences
for an organism or community, the synergistic action
of several factors may prove catastrophic. For example,
organisms under one form of environmental stress (e.g.
rising mean sea temperatures) may be less able to cope
with the physiological demands of adapting to increas-
ing frequencies of freshwater discharge that might occur
with changing rainfall patterns, and their resilience may
be further weakened by exposure to industrial contami-
nants. The effects of multiple and sequential human inter-
ference are well illustrated by a testimony given to the
United States Congress to encourage it to consider the con-
sequences of introducing a non-native oyster into Chesa-
peake Bay. Declines in native oyster stocks in Chesapeake
Bay are well documented and have been linked to reduced
water quality and overfishing, but attempts to reinvigo-
rate the oyster stocks have repeatedly failed. One solution
appears to be to introduce a non-native species that may
be more tolerant of present day environmental conditions
and parasitic fauna that were accidentally introduced into
Chesapeake Bay as a result of past aquaculture introduc-
tions or discharge of ship's ballast water. The testimony
given in Box 15.6 highlights the complex considerations
that face managers of natural resources that have to weigh
the ecological risks and potential benefits of such intro-
ductions.
 15.6 Interaction of multiple factors
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 15.6: Non-native oysters in the
Chesapeake Bay
This text is paraphrased from a testimony given to the
108th US Congress (Fi rst Session), Subcommittee on
Fisheries Conservation, Wildlife and Oceans, Commi ttee
on resources, United States House of Representative in
2003 by Professors J. L. Anderson and R. Whitlatch, both
experts in oyster ecology and the ecology of Chesapeake
Bay.

Good morning Mr Chairman and members of the Subcommittee. Thank you for this oppor-
tunity to speak to you about the proposed introduction of the non-native oyster Crassostrea
ariakensis .
The [native] oyster stock in the Chesapeake Bay has declined dramatically. Harvest is now
about one per cent of what it was at the end of the nineteenth century. Fishing pressure and
habitat degradation resulting from agricultural, industrial, and residential pollution, defores-
tation, and oyster reefdestruction have contributed to the decline. In recent decades, however,
the diseases MSX and Dermo have been identified as the core reasons for further decline. It
should be noted that MSX is caused by a parasite that was introduced to the East Coast from
Asia. Fisheries' management efforts and various restoration programs have not been successful
in restoring the oyster stock to date. The loss of the oyster has been devastating to the oyster
industry and its dependent communities. Those that remain in the Chesapeake oyster process-
ing sector now rely on oysters that are brought in from the Gulf of Mexico region and other
areas for their economic survival. Furthermore, the loss of oysters has contributed to declines
in water quality and clarity.
The introduction of the non-native Suminoe oyster, or Crassos trea ariakensis, from Asia has
been proposed as a solution to these difficult problems. Indications are that it may grow well
in the Chesapeake Bay and it is known to be resistant to MSX and Dermo. Despite the positive
results of introductions of some oyster species, some extre mely negative consequences have
been observed as well. A major risk of introducing a non-native oyster comes from pathogens,
such as MSX, or the introduction of other animals or plants that may be attached to oysters.
While in Australia and New Zealand, introduced non-native oysters have displaced native
oysters.
Aquaculture of ste rile non-native oysters, represents an appropriate interim step that pos-
sesses least risk (in terms of the available options) to the Chesapeake Bay and its dependent
communities. However, limits and controls on aquaculture practices must be implemented
to minimize the risk of introducing pathogens or reproductive non-native oysters during this
transitional phase. This approach may provide limited benefit to parts of the oyster industry
and it provides decision-makers with the added information required to make future decisions.
Moreover, this option allows more time for innovative, science-based efforts to restore native
oyster populations. On the other hand, the option of not allowing any introduction fail s to
address fishing industry concerns and will not result in improved understanding of the rami-
fications of non-native introductions. It may also increase the risk of rogue or uncontrolled
introductions. The option of the direct introduction of reproductive non-native oysters, is not
advised given the limited knowledge base on C. ariakensis and the potential for irreversible
consequences of introducing a reproductive non-native oyster into the Chesapeake Bay. It is
unlikely that there exists any 'quick fix' to the Chesapeake oyster situation .
Chapter 15 Disturbance, Pollution, and Climate Change

Chapter Summary
• Natural agents of disturbance to marine commu nities and systems occur across a full range of
spatial and tem poral scales.
• The response of commu nity metrics (diversity) to d ist urbance can be predicted from ecological
paradigms, such as the intermediate disturbance hypothesis.
• The relative impact of human activit ies on marine ecosystems needs t o be assessed against a
background of natural environmental fluctuations that occur at a variety of tem poral scales. Our
ability to detect the effects of human intervention critically depends on an appropriate analytical
or experimental ap proach.
• Coastal shelf environments are subjected t o the most intensive human activities that include fish-
ing, aq uacu lture, mi neral and hydrocarbon extraction, shipping activit ies, tourism , and discharges
of effluents and pollutants.
• Eutrophicat ion, which has result ed from elevated inputs of organic matter and nutrients from agri-
cultural run-off, has caused widespread blooms of toxic microalgae and anoxic events that have
resulted in mass mortalities of marine biota.
• Persistent contaminants, such as PCBs, have subtle effects at t he population level by affecting sur-
vivorship of larvae and juveniles. The full impact of these contam inants is a subject of specu lat ion.
• The congested inhabitation of coastal margins means that much of the world's population is vu l-
nerable to changes in sea level linked to global climat e warmi ng.
• Increases in global rainfall will elevate freshwater and sediment d ischarge into coastal waters
thereby affecting density-d riven currents in ROFls and w ill change the dist ribut ion of biological
commu nities.

Further Reading
Clarke et al. (1994) provi de a readable and sympathetic (to the non-mathematical) guide to the detection
of ecological changes in marine (and other) communities. Evans et al. (200 0) provide a synthesis of the
debate surrou nding replacement of tributyl tin w ith suitable, less environmentally damag ing alternatives.
Hall (2002) provides a review of agents of change in coastal systems in the present and also examines
possible future impacts. For an up to date review of ocean acid ification see Fabry et al (2008) .
• Clarke. K. & Warwick, R. 199 4 . Change in Marine Communities: an Approach to Statistical Analysis and
Interpretation. Natural Environmental Research Council , Plymouth Marine Laboratory, Plymouth.
• Evans, S, M., Birchenough, A. e., & Brancato, M. S. 2000, The TBT ban: out of the frying pan into the
fire? Marine Pollution Bulletin 40: 204-2 1 1.
• Fabry, VJ" Seibel, BA, Feely, RA & Orr, J,e. 2008, Impacts of ocean acidification on marine fauna and
ecosystem processes. ICES Journal of Marine Sciences 65: 4 14-432.
• Hall, S. J. 2002. The continental shelf benthic ecosystem : current status, agents for change and future
prospects. Environmental Conservation 29: 350-374.
Conservation
Chapter Summary
In 1768 , only 27 years after they had bee n discovered, the
giant Steller sea cows (Hydrodamafis gig as), w hich grazed
on algae around Bering Island , were driven to exti nction by
hunters. North Atlantic right whales (Eubalaena glacia/is)
were reduced to near extinction by commercial whaling
in the eighteenth and nineteenth centuries, and only 300
remain today. Large fishes of all spec ies are increasingly
rare following decades of over-exploitation, and marine
habitats are lost as a result of land reclamation, polluti on,
and commercial development. Shou ld w e, and do we, care?
16.1 Introduction
In preceding chapters, we have seen how pollution, fisher-
ies, and aquaculture, together with clim ate change, have
impacted, and are continuing to impact, the m arine envi-
ronment. Given that humans are the most sign ificant con-
sumer of natural resources on the planet, these are just a
subset of the possible activities (Table 16.1) that impact the
m arine environment.
In many cases, human impacts are unsustainable, threat-
e ning species, habitats, and ecosystems, and the envi-
ronmental goods and services they provide. One recent
analysis attempted to estimate the distribution of combined
human impacts on the world's oceans. The distribution of
impacts was very patchy, and the highest impacts occurred
in some coastal regions close to human population centres
(Fig 16.1 ). However, the analysis also suggested that no
areas remain unaffected by human influence and that 41 %
of the area cons idere d was affected by multiple drivers. In
the broadest sense, the coastal areas with high impacts are
often those that are stud ied most intensively by scientists,
while areas where impact is expected to be lower are often
As a reader of this book you probab ly do, but many others
in the world w ill be more concerned wit h the source of their
next meal. In dealing w ith issues of conservation and sus-
tainable developm ent , the marine ecologist enters a wid e
arena, w here practice and po li cy are also sw ayed by moral,
cultu ral, polit ical, soci al, and econo mic values. However, this
is also a challenging and rewardi ng arena, w here science
plays a key role in assessing the sustainability of human
impacts, prioritizi ng conserv at ion projects, and underp in-
ning the development of effective conservation pol icy.
less well-known . For example, an analysis of records in the
Ocean Biogeographic Information System, which is cons id-
ere d to be the most compre hensive datab ase with records
of the distribution and identity of marine taxa, showed
that the gre at majority of m arine diversity was described
for shallow coastal waters, wh ile the records of diversity for
deep, pelagic are as were relatively scarce (Fig 16.2) . On the
one hand this is a good sign, that we are focusing research
efforts in areas most likely to be impacted by human activi-
ties, but, on the ot he r, it is a concern that we know so little
about areas that are starting to be impacted by direct and
indirect human impacts.
Applied m arine ecology is the source of scientific evi-
dence to identify when and where conservation actio n is
needed, both by assessing the sustainabihty of impacts and
developing methods to mitigate unsustainable impacts.
Good scientific knowledge of a system can be needed to
support effective conservation, but it is not necessarily suf-
ficient to achieve it; since progress towards conservation
objectives will be strongly influenced by social and eco-
nomic factors.
 Chapter 16 Conservation

(01

•
•

• Very 10. impact «1.4) o Medi um impact (4.96-11.47) • High impact (12-15521
o law impact (1.4-4.95) o Medium High impact (8.47- 121 • Very High impact [> 1552)

(bJ
r;::::::;-:--=- -,
•

Figure 16.1 Global map (a) of cumulative human impact

Relative volume
on marine ecosystems as predicted by Halpern et al. 0
(2008). Inset boxes show highly impacted regions in the
1000
Eastern Caribbean (b), the North Sea (c), and the Japanese
waters (d), and one of the least impacted regions, in
2000
northern Australia and the Torres Strait (e). From Halpern
et al. 2008. 3000

4000
c.35 xlO6km3
- -
--
E
5000
~
....
m
C
6000

Figure 16.2 Global d ist ribution of marine taxa recorded 7000 Continental shelfand slope Number of rercrds
in the BOIS database. Area is scaled on the graph to 0 Ill"
be proportio nal to volume of ocean. The number of 8000 200 10'
taxonomic records for each combination of sample and 400 10'
9000
bottom dept h is standardized to the volume of water. 600 10'
The inset shows in greater detail the continental shelf 10000 800 10'
and slope, where the majority of records are found . From 1000 Ig;
Webb et al. 20 10. II 000
 16.2 Why conserve?
• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • ••

a whole range of actions. It m ay include outright protection

Table 16.1 Principal human impacts on the of populations or areas from human disturbance; but it may
marine environment. also involve zoning and other types of regulation that help
to keep human use within sustainable limits.
Aggregate extraction and mining
Aquaculture Sustainable management requires human intervention to
Dredgi ng maintain or create an environment that does not compro-
Engineering and co nst ruction mise the wellbeing of future generations.
Fisheries
Land-based impacts In this chapter, we cons ider the ethical a nd economic
Military activities foundations of marine conservation, together with how con-
Oil and gas servation issues can be identified and prioritized. We discuss
Reclamation i the role of poverty in driving the use of the m arine enviro n-
Recreation ment and highlight how marine conservation has to find a
Renewable energy way to accommodate the short-term needs, aspirations, and
Shipping expectations of humans. We therefore look in some detail
at the economics of m arine conservation , the strengths and
weaknesses of the policies that promote it and the legisla-
tion introduced to back it up. We also describe how conser-
Applied marine ecology underpins conservation advice vation policy is implemented and give some examples of the
and action through the provision of a robust evidence- successes and failures of conservation initiatives.
base of science.

At least in political terms, conservation contr ibu tes 16.2 Why conserve?
to sustainable development. Sustainable development
requires that the needs of future generations are not Ecology is at the scientific heart of conservation, since pop-
compromised by the actions of people today. Sustainable ulation growth is limited by the ava ilability of resources,
development h as m any facets, and includes social objec- and species interact wit h each other and their abiotic envi-
ti ves, suc h as human equ ity. Conse rvationists highlight ronment. Thus the n atural enviro nment limits the scope for
that recognition of the natural limits on hum an popula- development and exploitation, and sets an ever-changing
tion and economic growt h must go hand in hand w it h baseline (e .g. the effects of climate change) . Apart from
attempts to meet social objectives. Increasingly, n ational the fa ct that some conservation objectives, suc h as protec-
and international a greements express a move towards tion of particular species and maintenance of water quality,
sustainable development, and these underpin much of the are now incorporated into law, conservation is justifiable
conservation and environmental pro tection legislation we on ethical and econom ic grounds. However, perceptions
see tod ay. The contemporary tre atment of conservation of conservati on differ and justification is never a strictly
contrasts with the preservationist approach, which focuses quant itative exercise; one person's sustainable harvesting
on the protection of species and habitats wit hout reference of renewable fish populat ions will be another's devastation
to n atural change and human requirements (Agardy et a1. of a fragile marine environment.
2003). It is important to m aintain a sense of pers pective Conservation of biological diversity has been a m ajor
in conservation and remember that, even wit hout human focus of recent conservat ion efforts. As mentioned in Chap-
intervention, some species would become extinc t through ter 1, biodiversity has been define d as 't he variability among
n atural processes. living organisms from all so urces including, inter alia, ter-
In this chapter, marine conservat ion is considered as a restrial, m arine, and ot her aquatic ecosystems and the
contribution to sustainable management of the seas. Con- ecological complexes of which they are part; this includes
sistent with sustainable development, sustainable manage- diversity within species, among species and of ecosystems'
ment requires human intervention to m aintain or create an (Convention on Biod ivers ity; Box 16.1 ). Some of the key
environment that does not compromise the wellbeing of justifica tions for biod ivers ity conservation are: ( 1) that
future generations. The extent to which individuals, towns, humans have moral a nd ethical responsibilities to care for
regions, nations, and the international commun ity regard life on Eart h, (2) that living organisms enrich our lives, (3 )
long-term human wellbeing as dependent on the presence that 'e cosyste m services' are provided by many species,
of a clean, produc tive, and biodiverse marine enviro nment, and (4) that living organisms allow ecosystems to adapt to
will determine the strength of ethical and economic support change and are a source of materials that benefit humans
for m arine conservation. Conservation potent ially involves (Kunin & Lawton 1996) . At the personal level, belief in the
 Chapter 16 Conservation
relevance of various justifications will depend on social cir-
cumstances. Thus moral and ethical responsibilities to care
for life on Earth may not hold much sway if you are starving.
A common justification for the sustainable use of the
m arine environment is that m arine species provide impor-
t ant benefi ts for humans (Norse 1993). Thus, fisheries and
aquaculture are a vital source of food, income, and employ-
ment, particularly in the world's poorer countries (Chapters
13 and 14); and marine species are the source of m any use-
ful compounds, such as the algal polysaccharides, carra-
geenans, and agars that are used in food m anufacture. The
sea is also an important so urce of non-biological resources,
suc h as hydrocarbons for fuel and sand and gravel used in
bu ilding. Such direct economic benefits from the sea are
probably the easiest to quantify, as they have real economic
value (i.e. they are tradable commod ities on the wo rld's
stock m arkets), but are not necessarily the most important
benefits derived from marine systems.
Benefit may also derive from goods and services that
have no 'tru e ' market value, suc h as the storm protection
affo rded by coral reefs, control of carbon dioxide in the
atmosphere, and waste and nutrient removal or recycling
(Table 16.2). In some attempts to value the marine environ-
ment, these services are the most valuable properties of the
seas and oceans . However, their value is rarely accounted
for when assess ing the sustainability of human impacts. We
look at issues associated with cost ing suc h services later in
this chapter in sect ion 16.4. The m arine enviro nment is
widely used for recreation, and coral reef-related tourism
can be one of the most valuable industries in ot herwise
poor countries with little other means of wealth generation
(Chapter 11 ). People using the sea for recre ation generally
choose a clean, healthy, and productive environment in
preference to one that is polluted and animal poor.
16.3 What to conserve
At a societal level, the general greening of governme nt pol-
icy is intended to encourage nations, companies, and indi-
viduals to conduct their activities in a sustainable way. Many
of these actions, and the ways in which society addresses
and fails to address issues of sustainability, are covered in
16.5. However, when human impacts are not m anaged in a
sustainable way at source, conservation efforts often focus
on h alting unsustainable rates of habitat or species loss.
Unfortunately, the magnitude of existing human impacts on
the m arine environment is such that a great deal of effo rt
is focused on fighting rearguard actions rather than plan-
ning for sustainabiHty before the impact occurs (cure the
cause n ot the sympto ms) . It is hoped that the greening of
government policy will help to encourage proactive, rather
than re active, conservat ion . Proactive conservation, for
example, might require that measures to mitigate unsustain-
Box 16. 1: International agreements
that support marine conservation
At the World Summit on Sustai nable Development
(WSSD) in Johannes burg (2002), the follow-on meet-
ing to the United Nations Conference on Environment
and Development (UNCED) held in Rio de Janeiro,
Brazil in 1992, signatories agreed on a plan of imple-
mentation for sustainable development. The plan gives
high priority to integ ration of the th ree components of
sustainable development, namely: economic develop-
ment, social development, and environmental protec-
tion. It also recognizes the particular circumstances of
the major regions of the world, including the plight of
small island states, for which coastal zone management
and sea level rise are important issues.
Recognizing that marine ecosystems are critical for
global food security and sustaini ng economic prosper-
ity (fisheries and shipping), the WSSD plan of imple-
mentation included strong commitments to improved
conservation of the marine environment, including
application of an Ecosystem Approach by 2010 (Box
16.3), implementation of the FAO code of conduct for
responsible fisheries (fisheries that do not overexploit
fish populations or harm marine wildlife and habitats),
maintenance of the productivity and biodiversity of
important and vul nerable marine and coastal areas,
establishment of marine protected areas, development
of nat ional and international programmes for halting
the loss of marine biodiversity, and control of pollution
and the spread of alien species. These can be seen as
a wish list rather than a series of actions that will be
universally implemented on the timescale suggested.
However, raising these issues at international summits
highlights thei r importance and underpins improve-
men ts in environmental protection at inte rnational,
national, regional, and local levels.
There can be rapid uptake of high-level commit-
ments in other fora. For example, following WSSD, the
2002 Ministerial Declaration of the Fifth International
Conference on the Protection of the North Sea recog-
nized the need to manage all human activities using
an Ecosystem Approach that co nserves biological
diversity and ensures sustainable development. Subse-
quently, at the national level, the United Kingdom Gov-
ernment published 'Safeguarding our Seas', a strategy
for the conservation and sustainable development of
the marine environment. This included specific commit-
ments to marine conservation, such as the adoption of
an ecosystem approach, that were consistent with the
requirements of WSSD.
Source: http://www.johannesburgsummit.org/
 16.3 What to conserve
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 16.2 Examples of ecosystem services from natural marine ecosystem s (Costanza et at. 1997).

Ecosystem service Examples

Gas regulation
Water regulation
Nutrient cycl ing
Waste treatment
Provision of nat ural refugia
Food production
Provision of raw materials
Sourcing of genetic materials
Provision of recreat ion
Provision of cultural assets
Oceans balancing CO 2 content of atmosphere, thus regulating atmospheric
temperature
Oceans as ultimate source of water as a basis for agriculture, industry, and
transport
Gaseous fixation and organic matter decom position as sources of nitrogen for
primary production in all ecosystems
Breakdown of sewage by micro-organisms in conti nental shelf waters
Habitats such as seagrass and saltmarsh as nursery grounds for fisheries
Coastal waters as generators of fishery products
Marine sediments and rocks as sources of aggregate for build ing
Provide natural compounds useful in medicine
Offer sport fishing habitat, opport uniti es for ecotourism
Offer resources for aesthetic, educational, and scientif ic purposes

able impacts are incorporated into plans for development
or exploitation before those plans are sanctioned (16.6.1) .
Conservation actions must be prioritized to ensure
appropriate use of limited funds, but decisions can be
difficult and emotive.
Prioritization is needed to identify the conse rvation
actions that make the biggest contribution to sustainabil-
ity. At the global level, prioritization involves international
decisions about the investment in combating threats such
as climate change. At regional and local scales, prioritiza-
tion is needed to decide how scarce resources should be
allocated to proactive and reactive conservation, and the
specific issues to address. Prioritization involves many diffi-
cult and emotive decis ions . Thus the last few surviving indi-
vidu als of a species usu ally attract great public and media
interest, and provide impetus for conservation action, but
may stre tch, disp roportionately, resources that could be
used for large-scale habitat conservation or maintaining the
abundance of common species that play important roles in
the ecosys tem and provide direct benefits to humans.
In public perception, marine conservation is often epito-
mized by conce rn for marine mammals, seabirds , and sea
turtles, even though less conspicuous species and marine
h abitats are threatened by human activities .
The tendency to 'value' some species more than others
is a consistent trait in humans when surveyed for their
willingness to contribute financially (willingness to pay)
to the conservation of biodiversity. Large charismatic
taxa (marine mammals) attract higher bids than organ-
isms at lower trophic levels such as invertebrates and
algae [Ressurreicac et al. 2010).
Conservation will never be an entirely logical process
when so many value judgements are involved , and since
attempts to conserve whales a nd dolphins often gain strong
public support, efforts to conserve them may be more suc-
cessful. Protecting such charismatic species may also have
positive and negative implications for h abitats and other
ecosystem components on which they depend. An example
of the former might be the removal of fishing from a par-
ticular locality to avoid cetacean by-catch, which may have
concomitant beneficial effects for associated species (e.g.
seabirds or fish). Negative effects can result when the pro-
tected species becomes a 'pest', as exemplified by the con-
flict between sport fishermen and fish-eating cormorants
or seals.
Methods for conservation prioritization of individual
species are often relatively quantitative. Thus the World
Conservation Union OUCN) produces a 'Red List' of threat-
ened species, which is intended to be an easily and widely
understood system for classifying species at high risk of
extinction (Box 16.2) . This system is used to class ify all the
world's animal species for which d ata are available, and
many fishes and marine mammals h ave been listed .
Species are prioritized for conservation by the IUCN:
httpv/wwwlucnredlfst.crq.
Habitat conservation is now playing a greater role in the
marine environment, with widespread calls for greater use
of marine reserves. Thus far it has not been poss ible to cre-
ate very large marine reserves, so animals such as whales
are still managed on a population-by-population basis.
Habitats and regions can be ranked for conservation prior-
ity according to factors including their biological diversity
within particular biogeographical regions (Chapters 1, 7,
 Chapter 16 Conservation
and 8) and roles in sustaining particular species or groups
of species. The process of selecting sites for conservation
will typically involve the measurement or description of
attributes of a site or series of sites, an evaluation of these
measures against a set of criteria and a method of com-
bining the results to enable ranking of sites (Bibby 1998) .
Measures typically include species' diversity and rarity, size
of area, representativeness, naturalness (naturally a very
h ard thing to define ), cultura l criteria, and vulnerability.
Combining all scores is a problem, as some are strictly quan-
titative (area, diversity), while others are qualitative (natur-
alness). One approach is to rank sites based on quantitative
criteria and then to deal with practical considerations at
the final stage.
Prioritization of habitats and regions for conservation
can be a quantitative and qualitative process that can
complicate the integration of these data into a single
reference point.
Box 16.2: The nrcx Red List
The IUCN Red List recog nizes seven categories of spe-
cies extinction, threat, and endangerment where there are
sufficient data (see figu re). The categorization is based
on factors such as reduction in population size over a
specified time period, geograp hic range size, and abso-
lute population size. A species may be listed as critically
endangered, for example, because it has decreased in
abundance by >90% over the last 10 years or 3 gen-
erations. Marine mammals and turtles have been listed
for some time, and other marine species are increasingly
appearing on the list. Certain sharks, rays, and chimaeras
are likely to be added. There has been some debate about
whether managed commercial fish stocks should be
(Adequate dataJ
(EvaluatedJ
Data deficient (DO)
Not evaluated (NE)
Networks of marine protected areas may be proposed to
help conserve species and habitats. The idea here is that a set
of reserves is selecte d to meet specific conservation objec-
tives, such as the representation of each of the community
types known in a region at least once, or the conservation of
a fixed proportion (e.g. 30%) of biodiversity fe atures. Algo-
rithms can search a species or attribute by site database to
find a minimum set of areas that meet a given objective. If
sites are selecte d sequentially to define a minimum set to
meet a stated objective, then the select ion of any new site
depends on the properties of those already selected. Thus
the new set complements the series. A w idespread tool used
to develop such networks is the MarXan software devel-
oped by Hugh Possingham and colleagues at the Univers ity
of Queensland. The tool has adv anced considerably since
its early inception, when it was possible only to integrate
biological and habitat data for consideration . More recently
the tool has been expanded to integrate social and economic
data , such that it is possible to set a fixed conservation objec-
tive that is achieved by minimizing economic and social costs
included in the list. Some fish-stock managers argue that
the reference poi nts used for management are conserva-
tive, and if population biomass were kept at, or above,
those targets then there would be little risk of extinction.
Others argue that the observed rates of decline in many
exploited fish populations meet listing criteria and that the
population biology of fish makes them no less prone to
extinction than many bird and mammal species (Hutch-
ings 2001). Regardless of the pros and cons of these
arguments, the Red List has a role in highlighting species
that are severely depleted or threatened wi th extinction,
and should help to promote the conservation action that
is sought by fishery managers and conservationists alike.
Source: http: / /www.iucnredlist.org
Extinct (EXJ
Extinct in thewild (EW)
Critically endangered (CR)
(Threatened)
Endangered (EN)
Vulnerable (VUJ
Near threatened (NT)
least concern(lCJ

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
(a) Using only bialagi,,1 dete (el Fine resolution economic dala
Fishing
revenue
per PU
- annum per planning unit (PU) area and clearly shows the
Ibl Using biologicol and economic Idl Ircnemlr impact
dolo
I.l
. ,
,
e --
o
o '~
ie ,§
.-
.
_E
.~
'g g O.S
-~
,g-
o
ArelHTlinimizing
to marine stakeholders (see Richardson et al. 2006) . The
value ofsuch tools is their ability to investigate the outcome
of different management scenarios. In a case study in Wales
(UK), Richardson et a1. (2006) were able to demonstrate
that the inclusion of the spatial data on the distribution of
economic activities related to fisheries significantly reduced
the financial impact on the key stakeholders (fishers) while
maintaining the conservation objectives (Fig. 16.3).
MarXan freeware is now widely used in the planning
of networks of marine conservation zones or marine
protected areas and was used to inform the design of
the Great Barrier Reef conservation areas (http://www.
uq .edu.au/marxan).
Rigorous quantitative procedures for prioritization are
often seen to be essential, and yet the approaches to pri-
oritization we have described can be seen as an intellec-
tual rather than a real-world exercise. Indeed, many sites
are protected simply because they were in areas where
enforcement was possible, where they brought immediate
economic benefits to a local community, or where there
was regional or national support for protection, or perhaps
more importantly minimal opposition to their creation.
It is also important to recognize what site-based con-
servation can and cannot achieve. The openness of marine
systems means that pollution impacts. for example, have
to be tackled by reducing polluting inputs, not by setting
up reserves. A terrestrial analogy was the acid rain that fell
on Sweden in the 1970s and 1980s. Conservation actions
(e.g. liming lakes) in Sweden had minimal effect until the
UK Government was persuaded to take action to reduce
sulphur emissions from its coal-fired power stations. which
were the cause of the acid rain. Similar arguments can be
proposed for stopping fishing and habitat damage too,
16.4 Economics of conservation
Figure 16.3 MarXan software generated different marine
reserve designs according to the type of data used. The
outcome of using only conservation data (a), conservation
and economic data (b). Panel (c) shows the distribution
of economic activity expressed as gross revenue per
spatial heterogeneity in the commercial value of different
areas around the coastline, with darker areas having
the highest value. Panel (d) shows the economic impact
on stakeholders of the scenarios shown in panel (a =
minimising) and panel (b = fine resolution). Integrating
economic considerations reduced considerably the
economic costs in the short-term. Note however, this
figure does not account for any economic benefits that
might be accrued from the implementation of marine
reserves.
Fine resolution
because reserves displace activities while outright control
of the activities is needed to stop them. It would be inex-
cusable to lose sight of the activiry and thus fail to address
the problem at source. This is why conservation of the
marine environment involves other actions, such as regu-
lation of fisheries and pollution (see Chapters 13 and 15)
and integrating the management of multiple uses (16.5) .
Such linkage between multiple issues, together with the
fact that each issue may be addressed by different govern-
ment departments and nations, has highlighted the need
for more joined up conservation objectives and methods of
planning. One framework for achieving this is dubbed the
'e co syste m approach' (Box 16.3).
16.4 Economics of
conservation
Economic development has environmental costs, which are
rarely paid for by the businesses, governments. and indi-
viduals that profit from the development. The assimilation
of sewage by ecosystems and side effects of species' declines
wrought by fishing are cases in point; the polluter and fisher,
respectively. are rarely asked to bear the costs of their actions.
Failure to take account of the environmental cost of
human activities has meant that development is driven by
false economic incentives and disincentives, and is unlikely
to be sustainable. Moreover. because many human activities
in the marine environment, especially fisheries. are subsi-
dized or unprofitable, there are very high short-term eco-
nomic costs associated with moving towards sustainability.
The high short-term costs of changing human behaviour are
one of the greatest impediments to effective conservation.
Fisheries provide an excellent example of the way in
which short-term economic forces promote unsustain-
 Chapter 16 Conservation
Box 16.3: The ecosystem approach
The recognitio n that sectoral issues that affect the
mari ne environment were often managed in different
ways, by enti rely different bodies and without sufficient
regard for thei r cumulative or synergisti c impacts, has
led to the recognit ion that a more 'joi ned-up' app roach
was needed to ensure environmental protection. The
ecosystem approach is intended to provide this. It has
variously been defined as 'the integrated management
of human activities, based on know ledge of ecosystem
dynamics, to achieve sustainable use of ecosystem
goods and services, and maintenance of ecosystem
integrity' or in less scientific terms, as an approach th at
'puts emphasis on a management regime that main-
tains the health of the ecosystem alongside app ro-
pri ate human use of the marine environment, fo r the
benefit of current and future generations'.
As with the aspi rations of inte rn ational meet ings,
th ese defini tions are 'high level ' and do not he lp to
set operational management obj ectives. The science
sup port and adv isory process must th erefo re seek
to guide the choice of objectives and met hods of
achieving them. This work is cu rrently in the early
stages, but is likely to revo lve arou nd the develop-
ment of a suite of indi cators of human activity and
ecosystem impacts that can be used to measure the
success of management and th e respo nse of the
ecosystem. With any such approach , the main chal-
lenges are separating the ecological impacts of the
human activ ity fro m the impact of environmenta l and
clim atic effects, and deve lo ping an approach that
is sufficiently powe rful to detect imp acts on the
ti mescales that matter to managers (the lifetime of
Governments and often sho rter).
The Co mm ission set up by the 1982 Convent ion on
the Conservat ion of Antarctic Marine Living Resources
(CCAMLR) has ta ken an ecosystem approach to tack-
li ng anthropogenic (mainly fishery-rel ated) mortality
of marine animals. The problems include loss of alba-
t rosses and petrels to fishery long-lines, entanglement
of marine mammals in marine debris, and impacts of
fishing on the seabed. In the first case, the Commission
acted by controlling the timing of fishing and manner of
fish offal disposal, as well as requiring scientific observ-
ers on all vess els fishing outside nat ion al w aters in
CCAMLR areas. The management of the Great Barrier
Reef Marine Park (Box 16 .4 ) also provides an example
of an ecosystem approach.
For fu rther details see the CCAMLR (www.ccamlr.
org) and GBRMPA (www.gb rmpa.gov.au) websites.
ability, even when the long-term econom ic benefits of sus-
t ainable fisheries are known to be high. For the fisher, the
decision w hether to catch fishes now or leave them in the
sea w ill depend on their future va lue. If the value of a fish
stock 5 years in the future is perceived to be less than the
money that could be made after 5 ye ars by catch ing the fish
now, selling them, and investing the money in a bank, then
there is an economic incentive to fish as hard as possible in
the short-term . This is known as 'disco un tin g the future'.
Discount rates are used to measure the rate at w hich the
perceived value of a resource, such as a fished stock, falls
over time. Discount rates reflect the cost of return on alter-
n ative investments. Thus if you 'invest ' so me money in fish
by leaving them in the sea, you require that its value should
grow at least as fast as the value of money in the bank. If the
value of fish in the sea grows more slowly, or if the future
value of the fish might be jeopardized by activities of com-
peting fishers, then it is a good economic strategy to catch
the fish sooner rather than later.
The present value (PV) of income V, t years into the
future is:
v,
PV(V,) = (l + 8)'
where 0 is the discount rate. The decline in perceived
value of a unit of income at different discount rates is shown
in Fig. 16.4. High discount rates (typically 0.1 to 0.2) tend to
be used by fishers because fishers are uncertain about reap-
ing the benefits from fishes left in the sea, especially when
their competitors might catch them, and processes such as
stock recruitment are highly unpredictable. Fishers' rates are
typically higher than bank interest rates and thus it generally
pays to catch fish and invest the profits. This explains why
1.0. - - - - - - - - - - - - - - - - - - ,
0.8
m
~ 0.6
0
>
m
.=
>
0
~ 0.4
0.2
o 10 20 30 40 50
Time Iyearsl
Figure 16.4 The decline in the perceived value of a unit
of income at different discount rates. Thus the economic
benefits of intact and the modified ecosystem must be
directly co mpared .

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
species such as whales, wit h very low growth rates, were
'mined' rather than fished sustainably. Market instruments
that capture at a private level the social and global values
of sustainable fishing through, for example, premium pric-
ing for sustainably harvested fish, may be an important step
towards sustainability (Kaiser & Edwards-Jones 2006).
OUf arguments about the effects of discounting on fish-
eries also apply to other forward projections of value; for
example, in the context of climate change. Thus if global
warming has costs in 25 years, the willingness to invest in
mitigating them now wo uld be very low, even if the dis-
count rate were small (Hanley 1998 ).
Where areas of the marine environme nt are being con-
verted for human uses, such as aqu aculture, there are sev-
eral key questions to ask about the costs of such conversion.
For example, what is being lost and what gained, who are
the beneficiaries and losers, and what is the economic ratio-
nale for conservation? In recent years, a growing range of
approaches have been applied to value the services pro-
vided by marine ecosystems (Techn iques box) . Valu ing
TECHNIQUES: Valuing marine
ecosystems
There is growing pressure to emphasize the economic
costs and benefits of different conservation options, and a
range of tools have been developed to value marine eco-
system services. Broadly, economic valuation methods can
be divided into revealed preference or stated preference
methods that value use and non-use values, respectively.
Revealed preference methods estimate the ' use value' of
ecosystems, while stated preference methods provide an
alternate approach when services are not marketed. This
is a particularly useful approach for rather nebulous con-
cepts such as 'beq uest value' and 'cultural value'.
Revealed preference methods can include market
analysis where, for example, coral reefs or fisheries are
valued in terms of their contribution to tourism or catches.
In other cases, avertive behaviour and replacement-cost
methods may be used. These assume that the cost of
aver ting environmental damage is a proxy for the benefits
that a service provides or that the replacement cost of a
service provided by marine ecosystems, such as nutrient
cycli ng, is a proxy for its value. Another example mig ht be
the loss of a mangrove forest that fulfils many functions
including prevention of storm damage to the coastli ne. A
'value' can be attributed to this service in terms of the
cost incurred to build a concrete breakwater to replace
this service if the mangrove were to be removed.
Stated preference methods include choice modelling
and contingent valuation. Here, people are questioned
16.4 Economics of conservation
the functions of intact ecosystems alone is inadequate for
supporting decision-making because human-converted
ecosystems also have value to society. Thus the economic
benefits of intact and the modified ecosystem must be
directly compared. Two marine case studies are instruc-
tive in this regard. Full economic valuation of Philippine
mangrove, as against the aquaculture to which it may be
converted (assuming a 6% discount rate over 30 years),
shows that conversion makes sense in terms of short-term
private benefits . However, when external costs such as loss
oflong-term timber and charcoal supply, offshore fisheries,
and storm protection, are incorporated, the total economic
value (TEV) of mangrove is around 70% greater than that
of shrimp farms. Sim ilarly, on Philippine reefs (assuming
10% discount over 10 years), destructive fishing practices
had high initial benefits to the users, but the benefi ts of sus-
tainable reef fisheries and tourism were then lost. The TEV
of intact reef was 75% higher than that of a destructively
fished reef (Balmford et aJ. 2002).
about their (hypothetical) responses to changes in the
availability of ecosystem services. For example, in the
contingent valuation approach, people may be asked how
much they are willing to pay (WTP) , or, alternatively, how
much they are willing to accept (WTA) in compensation,
for a given change in an ecosystem service. While conti n-
gent valuation methods focus on payments, choice mod-
elling is an alternate stated preference method in which
people are asked to rank the acceptability of the status
quo against other scenarios for ecosystem services. A
criticism of WTP methods is that they can generate unre-
alistic values that have yet to be tested by attempting to
extract the stated value from human society.
All the methods for valuing ecosystem services are
subject to biases and concerns, and the development
of these methods is an active area of research. Another
issue that has recently been raised is the need to avoid
double counting when valuing services. For example,
when services are classified in groups such as 'support-
ing services ', 'provisioning services', 'regulating services',
and 'cult ural services'. To avoid the risk of double coun t-
ing, Fisher and Turner (2008) recent ly proposed an
alternate classification of servi ces as 'intermed iate' (e.g.
prima ry production, nutrient cycl ing) , 'fi nal services' (e.g.
habitat provision, fisheries production), and 'benefits'
(e.g. food and recreat ion) , all supported by abiotic inputs
like sunlight and nutrients. In this approach, servi ces and
benefits are distinguished and double-counting is avoided
because only the final benefits are valued.
 Chapter 16 Conservation

Table Expressed willingness to pay (Euros) to prevent a given (10 %) decline in marine biodiversity
of different taxa or marine biodiversity in its entirety showing the median and mean values stated by
residents and vi sitors to the Azores (Ressurreicao et al, 2010).

Valuation Scenario Level of Loss Sample Group Median Mean

Algae 10 % Visitors 23 € 66 €
Birds 10 % Visitors 25 € 71 €

Fish 10 % Visitors 30 € 86 €

Invertebrates 10 % Visitors 24 € 68 €

Mammals 10 % Visito rs 30 € 85 €

All marine species 10 % Visito rs 138 € 58 1 €

• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • ••

Algae 10 % Residents 16 € 45 €
Birds 10 % Residents 17 € 48 €

Fish 10 % Residents 20 € 58 €

Invertebrates 10 % Residents 16 € 46 €

Mammals 10 % Residents 20 € 58 €

All marine speci es 10 % Residents 96 € 405 €

This image shows a researcher questioning tourists about their willingness to

pay to prevent a given loss in species diversity in the Azores Archipelago. The
study investigated preferences for marine mammals, seabird s, fi sh , marine inver-
tebrates, and algae (see table). As in other studies, there were stronger pref-
erences for the charismatic fauna (fish and mammals), but, more importantly,
respondents were willing to pay much more to co nserve ' b io d iversity' in its
entirety co mpared with the summed values they gave for each of the taxa inde-
pendentl y. An extension of this study also revealed that WTP for biodiversity
was relatively consistent over a 3-year period that straddled the global financial
crisis between 2007 and 2009, which demonstrated an unexpected resilience
to the background economic climate.
 16.5 Conservation policy and legislation
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Ecosystemsand the production of services Other copitol

inputs People

D ~ ~
Primary and intermediate Final ecosystem
Goodsjhenelits Volueo! ....01 which
processes services goods.... II value

Nutrient '--'\ Food

BioturbotiO"r---V cycling production ,--,/

Biodiversity
Mangrove '--'\
trees
Primary
production r-r-v Biomass r--V
Ieaste!
defence

A schemat ic to show the provision of primary and intermediate processes by biodiversity through t o final eco-
system services and how these underpin the provision of good s o r benefits to human society. Goods have direct
monetary va lue that ca n be traded as commodities, whereas ecosystem services (ES) have monetary value that
is assessed through the techniques described in this box such as 'will ing ness to pay' (adapted from Fisher et
al. 2008).

16.5 Conservation policy and
legislation
Human impacts on the marine environment are determined
by the actions of individuals, villages, towns, cities , nations,
and businesses steered by government regulations or ince n-
tives, social pressure, conscience, or market forces. These
impacts can be mitigated, even eliminated , by a variety of
means, but in this the actions of individuals are of para-
mount importance. Human behaviour can be infl uenced
by many means includ ing education, persuasion, economic
incentives, legal pressure , and militar y force. Broadly
speaking, conservation faces a choice between top-down
and bottom-up approaches, or more usu ally some mixture
of the two, to achieve its goals.
The greater the proportion of society that is influenced
by its own desire to conserve, the more effective conser-
vation is likely to be. In practical terms, this means that
humans impacting the environment should see and share in
the benefits of conservation and sustainable development.
This requires effective education. Two countries that exem-
plify this are Australia and New Zealand. These countries
h ave adopted extremely 'green' policies towards use of the
marine environment.
Education and experience in the early years of life have
a major influence on attitudes and actions . Childre n who
regard conservation as an important issue are likely to
retain this opinio n when they diverge into a ra nge of careers
or lifestyles. Education, at least for most children and young
adults, is based on a syllabus that is mandated by regional
or national government. The content of this syllabus can
influence how people subsequently respond to, and deal
with, sustainable development issues. In many countries,
the general 'greening' of government policy is now reflected
in the school syllabus and this has encouraged childre n to
think about the role of conservation and sus tainable devel-
opment, and has also increased aware ness of issues such
as climate change that may not be locally visible. However,
childre n attend ing a small school on a Pacific island where
90% of animal protein comes from fish will have a very dif-
ferent perception of the marine environment from childre n
at a landlocked inner city school where their exposure to
marine species is through aquaria, supermarket counters,
and restaurants. Education level also strongly influences
the responses given in contingent valuation studies of eco-
system services. People educated to degree level or higher
cons istently give more pos itive res ponses or are willing to
pay higher values to conserve abstract concepts such as
 Chapter 16 Conservation
biodiversity. Care needs to be taken to tease out people's
willingness to pay from their ability to pay-richer people
are able to pay more than those with low incomes (Ressur-
reicao et al. 2010) .
Nature reserves and public aquaria also play an increas-
ing role in teaching parties of visiting schoolchildren and
adults about the marine environment. For example, the
Monterey Bay aquarium in California, USA opened in 1984
and is visited by 1.8 million people a year. This aquarium
runs education programmes to raise awareness of overfish-
ing of ocean species, such as the bluefin tuna (Fig. 16.5) .
Thus by displaying related rona species in aquaria, visitors
are able to see animals that would rarely be seen except in
cans and photographs. This must have a major effect on per-
ceptions ofthese animals, which will increasinglybe seen as
beautiful and endangered sea creatures, rather than over-
priced food in short supply.
For those parts of society that do not see the benefit of
sustainable development. or are unable to support it. eco-
nomic incentives and legal measures are needed. Rigorous
policing and heavy fines do change the behaviour of some
groups of people but they are unlikely to be effective with-
out the support of wider society, and this support is most
likely to be gained through persuasion and bottom-up pro-
cesses, such as those fostered by education.
Policies on sustainable development are influenced by
the electorate. non-governmental organizations (NGOs),
the media, science, industry, and economic and military
concerns. Governments are lobbied on many issues by peo-
ple with many perspectives (st akeh old ers), and for every
argument in favour of conservation and sustainable devel-
opment, there are likely to be opposing arguments from
those sectors of society that fear losses of food. income. or
access rights.
Nevertheless. there is a general 'greening' ofgovernment
Figure 16.5 Monterey Bay
Aquarium in California, USA, is one
of many large aquariums that runs
education programmes with a strong
conservation message. Copyright
Monterey Bay Aquarium.
policy, driven in part by international gatherings and dec-
larations such as the Rio Convention on Biological Diver-
sity and the Johannesburg World Summit on Sustainable
Development (WSSD) (Box 16.1) . Several governments
have expressed aspirations to move towards embedding
the principles of sustainable development in all a spects of
policy, rather than having an environment ministry that has
to compete with, rather than work with. other ministries.
such as industry, transport, and fisheries, for funding and
influence. Indeed. the treaty of the European Community
states 'that environmental protection requirements are to
be integrated into the definition ofCommunity policies and
activities. in particular with a view to promoting sustain-
able development'. Of course, it often takes a long time for
such high-level aspirations to be converted into action.
Many current systems for marine environmental man-
agement are confused by conflicting interests and shared
responsibility. For example, in UK estuaries, human activi-
ties are regulated by at least 80 parliamentary acts and a
series ofEU regulations. Even though several estuarine sites
of important conservation status have been designated for
protection as SSSls (Sites ofSpecial Scientific Interest), port
and harbour authorities still regulate shipping activity in
these areas, and gravel or sand extraction can be licensed.
Thus many perceive sites that have legislated conservation
status to be 'paper parks' that have only weak enforcement
to prevent degradation of conservation features.
Even in cases where the need for rapid conservation
action is recognized. many groups often have to liaise and
reach agreementbefore action canbe taken. Thus the North
Atlantic right whale (Eubalaena glacialis ) was brought near
to extinction by commercial whaling, and by the 1900s the
population numbered around 300 individuals. Despite
complete cessation ofcommercial whaling. the right whale
was still at risk from entanglement in fishing gear and col-
 16.5 Conservation policy and legislation
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
lision with ships. A population analysis in 1998 suggested
that the rates of mortality affecting the whale population
could drive the whale to extinction within 200 years (Cas-
well et al. 1999). The only way to save the whale was to
reduce mortality, and this could best be achieved by reduc-
ing the probability of ship collisions, which accounted for
80% ofall deaths. Such collisions often occurred in the Bay
of Fundy, where a shipping route crosses one of the main
feeding areas used by the whales. In late 2002, after sev-
eral years of pressure from the WWF and other bodies, the
International Maritime Organization gave the Canadian
Government permission to reroute shipping in the Bay of
Fundy. The new shipping lanes came into effect on 1 July
2003 and are expected to reduce the risk of ship collisions
by 80% and should help to prevent the extinction of the
population (Fig. 16.6). Clearly in such cases, good scientific
advice, and both national and international understanding
and agreement, are needed.
International agencies can playa key role in coordinat-
ing conservation actions across many areas ofjurisdiction.
Thus whales, turtles, fishes, and water currents do not
respect national boundaries, and local or national conser-
vation will often be ineffective. The International Whaling
Commission, for example, tries to regulate whaling on a
global scale, though agreement is hard to reach in such an
international agency when countries perceive conservation
issues in different ways and some seek to continue exploita-
tion while others strive to ban it.
• issues in coastal areas. Management should therefore be
., r -
Grond ' •~
Monon %.-"
Island
Atlantic Ocean
New .hipping lanes
- - Old .hipping lanes
- - _. Right whale
feeding grounds
Figure 16.6 Shipping lanes in the north-west Atlantic
were moved to reduce the probability that endangered
right whales wou ld be struck by ships.
The recognition that management of many human
activities in the marine environment has become overly
complex and heavily influenced by sectoral concerns has
prompted the development of an ecosystem approach
(Box 16.3) . This approach builds on other attempts to
improve cooperation among sectors. through approaches
such as 'int eg rated coastal zone management' (lCZM),
which have already been widely used with various levels
of success in some coastal regions. Integrated coastal zone
management (lCZM) is a dynamic, multidisciplinary, and
iterative process that promotes sustainable management
of coastal waters and lands (coastal zone). ICZM brings
together all those involved in the development. manage-
ment. and use of the coast in a framework that facilitates
integration of their interests and responsibilities. Over the
long term. ICZM seeks to balance cultural, economic, envi-
ronmental. recreational. and social objectives in order to
achieve common goals. In Europe the environmental con-
cerns that have led to the development of ICZM thinking
include the impacts of fishing (Ch apter 13), aquaculture
(Chapter 14), pollution (Chapter 15), rapid human pop-
ulation growth, and poor employment opportunities in
coastal communities.
Integrated coastal-zone management provides a frame-
work for management of multiple human impacts and
activities. The integrated approach of ICZM is consis-
tent with the ecosystem approach to management in t he
marine environment.
A European Union (EU) ICZM Demonstration Pro-
gramme consisting of 35 projects in a range of socio-eco-
nomic. cultural. administrative, and physical conditions
across Europe in 1996 to 1999 concluded that a sectoral
approach (e.g, dealing with issues impact by impact) to
management did not meet the needs of managing complex
inherently inter- and multidisciplinary; promote integration
of the terrestrial (e.g. human settlements. watershed con-
siderations) and marine (e.g. fisheries) components; high-
light the need for integration of all relevant policy areas,
sectors, and levels of administration; and use informed
participation and cooperation ofall interested and affected
parties to assess the societal objectives. In short. ICZM
implies a new style ofgovernance that involves partnership
with all ofthe segments of civil society, and solicits the col-
laboration ofall coastal zone stakeholders in the conception
and implementation of a development model that is in their
mutual interest (European Commission 2000) .
Eight principles have been drawn from successful coastal
management initiatives and helped to form the basis for a
call on ED member states to set up national strategies for
ICZM by 2006 (European Commission 2002) . These prin-
ciples include: (1) a broad overall perspective; (2) a long-
 Chapter 16 Conservation
term perspective taking into account the precautionary
principle; (3) adaptive management; (4 ) local specificity
and diversity; (5) working with natural processes and car-
rying capacity of ecosystems; (6) involving all parties in
the management process; (7) support and involvement of
relevant administration bodies at national, regional, and
local levels; (8) a combination of instruments to facili-
tate coherence between sectoral policy objectives. Thus in
Europe, the move towards ICZM recognized the important
role of coastal lands and waters for nature and ICZM is an
ambitious strategy, or at least a wish list, for addressing
some of the overarching environmental concerns for the
coastal zone. ICZM is considered a prerequisite for success-
ful management of coastal and marine resources around
the world, and many international bodies, such as the Food
and Agriculture Organization of the United Nations. Inter-
governmental Oceanographic Commission, United Nations
Environment Programme, and the World Bank. support
and promote ICZM.
When it comes to environmental decision-making at a
global level, the dichotomy in the sustainability, profitabil-
ity, and capacity for species' and habitat conservation in the
developing and developed world needs to be recognized.
Developing countries still have some of the greatest assets
in wilderness areas and biological diversity. but they have
the greatest human population growth rates and fewer
resources for conservation. It is also worth remembering
that opportunities for conservation in developed Western
nations are often subsidized bypoor people. The removal of
capacity in developed countries can have harsh social and
economic consequences in the short term but, in the longer
term, these are often softened by government subsidies and
job opportunities in other sectors of the economy. In the
poorer countries of the world, fishing is often the occupa-
tion of last resort for families with no other opportunities
for subsistence. The scale of poverty and reliance on fish-
eries in the developing world has been widely described
elsewhere (Kent 1998) . It is possible that 1 billion people
in 40 developing countries may lose access to their primary
source of protein as a result of overfishing (UNDP 2003) .
The international community will have to intervene to
provide funding for conservation in the poorer countries.
This would, for example, include providing the means to
generate alternatives sources of livelihood to alleviate the
poverty that lies at the root, for example, ofdestructive fish-
ing practices and unsustainable coastal development that
threaten biological diversity.
16.6 Conservation in action
Action to meet the objectives of marine conservation is
being taken on many fronts, and this has involved many
levels of ecological (species, habitats, ecosystems) and
administrative (local and international, NGO and govern-
mental) organization. To show how all of these levels are
being incorporated is beyond the scope of this book; instead
we give three examples that help to illustrate the range of
actions involved. The first of these is the assessment of envi-
ronmental risk in any project, in the process referred to as
'enviro nmen t al impact assessment' (EIA) . The second is
ecolabelling, which provides consumers with a basis for
environmental choice and seeks voluntary participation of
an industry in practices that meet sustainable development
objectives. The third is the use of marine reserves (marine
protected areas), from which fishing and other forms of
extractive use are excluded.
As we consider these various forms of conservation
action, it is worth considering the overall context in which
conservation policy is implemented. Most conservation
action is ultimately driven by high-level objectives. As we
have seen, these objectives are often chosen internationally
at fora such as the World Summit on Sustainable Develop-
ment (Box 16.1). Then, sustainable development strategies
have to be developed to help meet the objectives. Conserva-
tion actions consistent with the strategies are then taken to
meet the objectives. Progress towards objectives is moni-
tored, and strategies and actions (hopefully not objectives!)
amended to ensure objectives are met.
16.6.1 Environmental impact
assessment (EIA)
The aim ofElA is to prevent. reduce, or offset any adverse
impacts of each and every major development affecting
the environment, including the sea (Barrow 1997) . EIA
is a formal process to identify and predict the environ-
mental impacts of a project, with a view to mitigating
adverse impacts or addressing them in revised plans. Such
assessments are required for activities such as oil-rig and
wind-farm construction, and aggregate extraction. Inter-
estingly, however. fisheries' development is usually exempt
from EIA. The omission of fishing has led to some internal
argument among the industries concerned in Europe,
since fishing has been identified as the greatest threat to
the marine environment by the Oslo and Paris Commis-
sion, which upholds the Convention for the Protection of
the Marine Environment of the North-East Atlantic from
dumping and land-derived and offshore sources of pollu-
tion. The purpose of EIA is to support the objectives of
conservation and sustainable development by integrating
environmental protection requirements into the planning
process at the earliest possible stage. The EIA process
serves to predict the environmental. social. economic. and
cultural consequences of a proposed activity and to assess
plans to mitigate any adverse impacts resulting from that
activity. Although there is much variation in practice,
particularly among countries, EIA often provides a focus

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
for the involvement of society in reviewing the potential
impact of the activity, through submissions from the pub-
lic and government bodies.
Environmental impact assessment aims to predict the
impacts of development and to mitigate or avoid those
impacts that are unsustainable.
Once it is decided that an EIA should go ahead, a six-
stage process begins. This involves seoping, quantifica-
tion, report production, decision on project, and, if the
development is allowed to go ahead, development and
monitoring. During seoping, all the potential impacts of
the projects are listed, and during the quantification stage,
the magnitude of each impact is assessed in relation to the
existing habitats, species, and activities at the proposed
development site . Based on scoping and quantification, an
Environmental Statement is produced and this is reviewed
by government and associated agencies to determine
whether development should go ahead.
A developing and more comprehensive form of impact
assessment is Strategic Environmental Assessment (SEA) .
SEA assesses the wider impacts of any development. tak-
ing account of interactions with other forms of develop-
ment and the wider environment.
16.6.2 Ecolabelling
Consumer choice can have a powerful influence on the
use of the marine environment as demonstrated by the
boom in sales of 'do lp h in friendly' or 'd olp h in safe' tuna
when the public saw the first pictures of dolphin kills
in tuna purse seine net fisheries . Today, increasingly
detailed information is available on the provenance of
wild caught fish.
What we ultimately buy in the supermarket may influ-
ence the behaviour of fishers and other users of the
marine environment.
In Great Britain, the Marine Conservation Society pub-
lishes a 'Good Fish Guide' to help consumers who like to
eat seafood but are concerned about the impacts of fishing
on fish stocks, marine wildlife, and habitats, to choose fish
that come from sustainably managed fisheries that mini-
mize damage to the marine environment and do not harm
other wildlife. Organizations such as the Seafood Choices
Alliance are important non-governmental bodies that
attempt to generate consensus among users of seafood
(retailers. processors, importers. and catching sector)
about how to move towards sustainable and safe seafood
(see website http :/ /www.seafoodchoices.com) .
Internationally, the Marine Stewardship Council (MSC)
runs a market-based certification programme and seafood
16.6 Conservation in action
ecolabel to recognize and reward sustainable fisheries .
The MSC was founded in 1996 as ajoint venture between
WWF and Unilever, became an independent charitable
organization in 1999. and is funded by grant income and
royalty fees paid for use of the MSC ecolabel on products.
Products bearing the MSC ecolabel have won the patron-
age of royalty and celebrity chefs alike, and retail giants
put MSC ecolabelled products on their shelves, with an
ever increasing range of different products currently on
offer. Fisheries certified under the MSC scheme include
the Western Australian rock lobster, New Zealand hoki,
Bering SealAleutian Islands pollack, and Alaska salmon.
The certification process is conducted by a panel of inde-
pendent scientists who assess the fishery against criteria
for the status of the stock, ecosystem impacts due to fish-
ing, and the management systems in place (Philipps et al.
2003) .
Several groups now certify or recommend fishery prod-
ucts from sustainable fisheries (see http://www.mcsuk.
org and www.msc.org).
With the commitment to improving fishing practices by
the industry, qualification for the MSC ecolabel should be
relatively straightforward for fisheries where the choices
of how much fish to catch and how to catch it are under the
control of a single group of fishers. It will be in their inter-
est to invest in long-term sustainability and in ecolabelling
that will attract premium prices and access to consistent
markets. However. as we saw in Chapter 13. the majority
of the world's fisheries are not like this, and most fishers
have little control over the setting of fishing quotas. and
they share the fish resource with other fishers and nations
who may not choose to fish responsibly and are caught up
in the race to fish . Fishers who participate in these fisher-
ies may be impeded from realizing their ambition to move
towards MSC certification due to the actions of others that
are beyond their control. Thus the MSC scheme focuses
very much on consumer choice as the driver for change
in fisheries (Kaiser & Edwards-Jones 2006) . Interestingly,
although consumer choice is held up as the main driver
for change by the MSC, it is the major retailers that have
had the most significant impact in terms of changing fish-
ers' behaviour to date. Many of the world's largest retailers
have stated a desire to source all fish-related products from
MSC certified fisheries by 2012 . Thus retailers have set a
new standard. irrespective of consumer choice. The rea-
soning behind this may seem to be a wholehearted accep-
tance of sustainable use of natural resources, but another
explanation may be simply that unreliable sources of fish
from collapsed or teetering fisheries is simply bad for busi-
ness and over-complicates supply-chain logistics. Irrespec-
tive of the above, the MSC benchmark set by retailers has
initiated significant changes in the attitude and behaviour
 Chapter 16 Conservation
of fishers' organizations in d eveloped countries (previ-
ously many were skeptical of the benefits of accreditation)
and this is perhaps reflected in the tenfold increase in the
number of certified fisheries in just the last 5 years. The
MSC has its detractors and supporters, leading to contem-
porary debate on the role of the organization in promoting
sustainable fishing (see Hilborn & Cowan 2010; Jacquet et
al. 2010; Kaiser & Hill 2010).
16.6.3 Marine reserves
Reserves, where human activity is spatially controlled
or banned, have useful roles to play in marine conserva-
tion and there has been an upsurge of interest in them,
often stimulated by growing appreciation of the effects of
fishing on habitats and species. It is notable that < 1% of
the marine environme nt has reserve status as opposed to
6% of land, and this alone suggests that marine reserves
need to be more extensive than they are. No reserve can
be fully effective at protecting m arine life if ships can spill
oil and ot her toxic su bstances in the vicinity, if curre nts
feed contaminan ts to the animals living there, if animals
migrate from the reserve and can be affected by fishing
or pollution elsewhere, and if climate change drives the
protected species to ot her locations. The proper solution
to these problems lies in the effe ctive regulation of the
human activities involved. Thus far, the greates t progress
in tackling large-scale issues in marine conservation has
involved t ackling the impacts directly. For exa mple, by
stopping whalers killing whales, preventing yachts using
TBT on their hulls, and controlling d ischarges of heavy
metals and radio activity into the marine environmen t
(Chapter 15). Wit h some of these activities controlled, and
moves towards greater limitation of fishing effo rt, now is
a good time to start using reserves more widely to support
marine conservation.
Box 16.4: The Great Barrier Reef
Marine Park
The Great Barrier Reef (GBR) Marine Park is an example
of one of the first attempts to conserve and manage at
the ecosystem scale. The GBR Marine Park Act (1975)
underpins the conservation of the GBR, providing for
conservation of the GBR and sustainable use of the sur-
rounding region. The main tool for protecting and preserv-
ing the GBR, as requi red by the Act, is zoning. Zoning
separates conflicting human activities and protects the
most vulnerable areas. The Park is managed by the Great
Marine reserves protect a very small proportion of the
marine environment. In the open marine environment,
the use of reserves for conservation must go hand in
hand with control of human activity outside the reserve.
One of the success stories in marine reserve conserva-
tion is that of the large Great Barrier Reef Marine Park in
northeastern Australia (Box 16.4). However, many marine
reserves are small and vulnerable to climatic events, land-
derived pollution and run-off, and poaching.
Small reserves on and around coral reefs have provided
most of the evidence for the potential conservation ben-
efits of reserves. Most important has been the demonstra-
tion that when protection is effective, many site-attached
reef fish species and invertebrates attain greater densities
and sizes than in areas where they are fished. This may
be important to fisheries because these species may pro-
duce larvae that w ill support recruitment to fished areas,
may themselves migrate out into the fished areas, and, in
the case of rot ational closure, ma y ultimately be caught
directly. Alt hough there is some evidence for rapid build-
up of abundance of fished species soon after protection,
this is very soon dissipated when areas are reopened; thus
rotational closure seems not to be a useful strategy, unless
fishing effort is otherwise curbed. With respect to other
potential benefits of marine reserves to fisheries, late
juve niles and adults do mi grate to fished areas, but the
movement is often over small distances, and unless fishing
effort is otherwise reduced, this is unlikely to compensate
for the loss of yield due to protection. The protection of
adult fishes to ensu re larval recruitment to fished areas
is perhaps the most useful potential benefit of marine
rese rves to sustainable fisheries, but regrettably, it is the
least well understood.
Once establishe d, marine reserves can undoubtedly
Barrier Reef Marine Park Authority (GBRMPA), and the
GBR was recognized as a World Heritage Site in 198 1.
The GBR Marine Park is divided into four sections for
management purposes (figure a), and the challenge for
managers is deciding who can do what and where in each
of the sections. Zoni ng plans for each section (e.g. figure
b) provide for activities that are as-of-right, wi th permis-
sion, or prohibited, and widely available maps ensure that
all potential users are aware of restrictions on their move-
ments and activities.
 16.6 Conservation in action
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

The least rest rict ive zones are 'general use' in which (b)
activi ties such as shippi ng and traw ling may be permit-
•• •s
ted, but mining, oil drill ing, commercial spear-fishing,
,• •s
- - - •• a •
••
•~ --• , • •• -• i
0
and spear-fishi ng with breathing apparat us are not •• •
e ~ 0
•0
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0
Other zones provid e for habitat protection, estuarine
conserva tion, or general conservation, w hile pe rmit-
•e
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ting restricted commercial or recreat ional use. The most uowlture Permit
restrict ive zones are 'marine national park zones', w hich Bait nellin
Booti ,di¥i , hoto ro h
are no-take 'areas'; 'scientific research zones', which (rabbin tro in
Horm t filhing lor aQuarium fish,
only all ow access fo r agreed scientific research; and rl n eIIhwr
Permit

'preservat ion zones' w here all entry is prohi bited except Hormt fi lhing lor lell IU[umber,lrolhul, Permit
tro ilol rOlk lob~er
in emergencies and to con duct scientific research that Limited lolleltin
Limited I ear filhin lnorkelonl
woul d be impossible elsewhere. In 2004, a new zon- Line filhin
ing plan w as introduced to incorporate 28 new coastal Nelli n other than boit neni
Reseonh other than limited im II resecnh Permit
protected areas and a Representative Areas Prog ram, Shipping (other than in a delignated
Ihipping oreo)
w hich ensu res that examples of th e ent ire range of Tourilm Pro rom Permit
habitats and biodiversity are represented wi thin highly Trocnionol use of marine reseures
Trowli
Marine National Park zones. Trolling

14"\ rT----,----------,---,-------,----,
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The four management areas of the Great Barrier Reef

Marine Park.

Zoning of the Cairn s/Cooktown Management Area of the

Great Barrier Reef Marine Park with a key t o permitted
activities.

For further details see the Great Barrier Reef Marine Park Authority website (http:/ /www.gbrrnpa.gov.au).
 Chapter 16 Conservation
Box 16.5: Paying for marine
conservation
Polici ng Mari ne Protected Areas (MPAs) is an
expensive busi ness and governments rarely provide
adequate fundi ng. Given that the polici ng and man-
agement of a small MPA requi res several staff and
around € 100 000 per year, income from recreational
divers tha t use MPAs could make an important finan-
cial contribution to effective marine conservation.
Over 200 MPAs in the Caribbean and Central
America contain coral reefs that are likely to attract
recreat ional scuba-divers. Indeed, a survey of MPA
use by dive operators showed that 46% conduct at
least 80% of their diving in a MPA
At present, only 25% of MPAs wi th coral reefs
charge divers an entry or user fee, and this is typically
€2-3 per dive or diver. However, divers have already
shown willi ngness to pay up to €25 per day to access
some MPAs, and this is only a fraction of their total
expendi ture on equipment, training, accommodation,
and entertainment.
The wider Caribbean and Central America is a
prime location for diving and attracts 57% of all
international scuba-diving tourists. Provided the rec-
reational use of MPAs can remain consistent with the
goals of conservation and sustainable development,
higher charges for diving access to all MPAs would
help secure much needed funding for MPA protection
and management. Indeed, if user fees were raised to
around €25 per diver this would raise approximately
€93 million per year, sufficient to cover some 78% of
the predicted shortfall in funds for MPA management
in this region.
Source: Green & Donnelly (2003).
h ave an important educational role in d rawing public
atten tion to areas of special ecological significance, pro-
viding opportun ities to see rel atively undisturbed marine
h abitats, and encouraging people to observe the benefits
of conservation.
The Great Barrier Reef Marine Park, and some othe r
reserves around the world, also show that marine reserves
can be very successful econo mically (16.6) . Th is is impor-
tant, as econo mic success is likely to foster comm un ity
support and good enforceme nt, both of which are para-
mount to success ful management. On many coral reefs,
diving tourism is a key source of income to support reserve
man agement. However, not all areas benefit from tourist
ex pend iture and, as wit h other conservation tools, there
are socio-economic cons traints to the effective man age-
ment of marine reserves. Some of the best studied marine
reserves a re at Su milon and Apo Islands in the ce ntral
Philippines, and Russ and Alcala (1996) have described
20 years of hopes and fru strations on Sumilon Island. A
marine reserve was established there in 1974, but there
h ave been several major breakd owns of management.
Remarkably, this was at a site where the aggregate fish-
eries' yield from the island was higher when the marine
reserve was ope rating (Russ & Alcala 199 6). One of the
key problems with management on the island seemed
to be that fishers were not convinced of the real benefits
of the marine reserve and were not full y involved in its
management. There are other examples of re peated break-
down of reserves on tropical reefs. Together they indicate
that management imposed from outside the commun ity,
and wit hout the support of the commun ity, is unlikely to
work.
Given the small areas that are designated as reserves
in the marine environment and the key role that they can
play in protecting species an d h abitats of conse rvation
concern, they should be used more wide ly to support con-
servation objectives. However, the designation and effec-
tive protection of marine reserves must go h and-in-hand
with direct control of overall human impacts (Fig. 16.7).
In this section on conservation in action, our examples
h ave shown that, because of the multiple concerns, the
complexity of the issues and interdisciplinary demands of
decision-makers, conservation action is as much art as sci-
ence. The uncertainty of environmental decision-making
was well illustrated by the concerns for deep-sea pollution
raised by the disposal of the Brent Spar oil platform (Gage
& Gordon 1995 ; Angel & Rice 1996) . Shell aba ndoned
plans to dispose of this redundant oil-sto rage platform
by sin king it in water 2200 m deep in the northeastern
Atlantic. Shell had been given scientific advice that deep-
sea disposal was the best environmental option, but envi-
ronmental groups protested that toxic residues wou ld
leak from the platform and contaminate the food-chain.
Greenpeace boarded the platform in a bid to pre vent its
sinking and eventually the Brent Spar was to wed to a
fjord in Norway to be dismantled. It may well be that the
environmental costs of disposing of the platform inshore
have been greater than those of deep-sea disposal, and the
arrival of the platform inshore also caused controversy in
Norway. Scientists have continued to d ebate the pros and
cons of the various disposal options, and yet the des ire
of Greenpeace to make an issue of the disposal and the
ens uing campaigns at fuel stations in Germany effectively
forced the final disposal option.
 16.7 Evidence-based conservation
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

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DESTRUCTIVE FISHING PROHIBITED

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Agr lcultun... Ftshcrtes and Ce nserva tlnn Department

Figure 16.7 This sign at Tai 0 fishing village in Hong Kong informs people that they can still fish, but only if they do
it in an environmentally sustainable manner. The use of indiscriminate and destructive fishing practices is illegal and
fishers are subject to heavy fines and a prison sentence if they ignore the warn ings. (Photo copyright: Johanna Junback.)

16.7 Evidence-based Evidence-Based Management (http:/ /www.cebc.bangor.

conservation
As scientists, we are primarily driven by the desire to
understand better the natural systems that operate in the
marine environment. Understanding causal relationships
requires a deductive hypothesis driven approach that
aims to eliminate external influences that might gener-
ate errors in our reasoning. However, conservation is an
emotive area of science and is prone to 'belief-based sci-
ence', where scientists decide upon a position and then
look for evidence to support it (Hilborn 2006; see Chapter
13). Similar problems can occur in the field of medicine,
where scientific errors can endanger human life . Thus it
is not surprising then that some of the most robust sci-
entific evaluation methodologies have arisen in the field
of medicine, where systematic review methodology has
been developed to provide a framework for the evaluation
of multiple independent studies. This approach has been
advocated for conservation biology through the Centre for
ac.uk) . Systematic review defines the protocols used to
search the available published literature using specific cri-
teria for selecting or rejecting the inclusion of the studies
located. The evidence-based approach is important as it
generates conclusions that avoid issues of publication bias
(the tendency ofjournals to publish only positive outcomes
or certain types of study) or at very least to highlight the
issue. An example of the application of the approach is the
study of the response of fish and other taxa to the imple-
mentation of no-take marine reserves in temperate systems
(Stewart et at. 2010) . The study validated the conclusions
of some previous studies, but highlighted potential pub-
lication bias in data that reported biomass metrics as the
response variable (for fish) . The study also highlighted the
potential for habitat-confounding effects in the response
metrics in the reported studies, which often did not pro-
vide adequate habitat data for a robust validation of their
conclusions. Anybody undertaking a systematic review
soon realizes how poorly scientists report data that are
 Chapter 16 Conservation
vital for understanding or interpreting the reported results
(journals do not like long tables of results, although the
internet should make access to original data easier) . The
most important characteristic of systematic review is its
rigour, which provides policy makers with a high level of
confidence in the reported findings and recommendations.
16.8 Life-cycle analysis
In Chapters 13 and 14 we looked in detail at the ecologi-
cal issues that are associated with food production in the
marine environment. Both wild-capture fisheries and
aquaculture contribute significantly to the world supply of
protein, and this will need to increase into the future. Aqua-
culture is becoming increasingly important and is likely to
overtake wild -capture fisheries as the main source ofaquatic
protein production inthe next 5 years. In additionto the eco-
logical problems associated with wild-capture fisheries and
aquaculture, the post-harvest processes also have associated
impacts on the environment that are generated from the
transport and processing of the product. It is important to
consider all stages of the production process to have a truly
objective view of whether one form of production might be
better than another. Such an approach is adopted by Life
Cycle Analysis (LCA), which was developed primarily for
land-based industries. Although still in its infancy for food-
based products, it provides a valuable basis for influencing
the sourcing policy of retailers. An interesting example of
the application of this technique was a comparison of the
environmental impacts of wild-caught cod and farmed
salmon compared to farmed chicken (Ellingsen & Aanon-
dsen 2006) . What the LCA revealed was that the capture
phase (fishing) for cod and the feeding phase for salmon
and chicken dominated all the other environmental impacts
considered in the study. The production of chicken was the
most energy efficient. but cod and salmon production were
similar in this respect. However, to produce a 200 g fillet
of cod, the environmental impact (footprint) of fishing gear
affected an area of seabed 100 times larger than the area of
land needed to grow the food necessary to produce a stan-
dard 200 g fillet of chicken. The analysis also demonstrated
that, if salmon aquaculture could become more dependent
on plant-derived sources of protein. it would become much
more environmentally friendly than current practices used
to produce salmon (Fig. 16.8) . (See also http:/ /www.eco-
trust.org/lca for information about LCA ofsalmon farming.)
16.9 The future
Every contemporary conservation action takes place in a
marine environment that has already been dramatically
altered by human activities. Some of the biggest impedi-
Remaining energy
• sources
D Natural gas
14 .-- - - - - - - - - - - - - ---1 1 Hydropower
12 1 Mineral oils
10
4
2
o
Formed solmon fillet Farmed vege-salmanfillet
Figure 16.8 Life-cycle analysis showing the energy score
for the production of a farmed chicken fillet, a farmed
salmon fillet, or a farmed 'vegetarian' salmon fillet , given
the possibility of new advances in feed production.
The energy consumed (MJ) per fillet unit (FU) is lowered
considerably if salmon farming could move further away
from feeds dependent on wild-capture fisheries. From:
Ellingsen, H. & Aanondsen, SA (2006) Environmental
impacts of wild caught cod and farmed salmon-a
comparison with chicken. International Journal of Life
Cycle Analysis, 1: 60-65.
ments to successful conservation are the massive changes
to marine habitats and species that have already occurred
and the emphasis on reactive rather than proactive man-
agement. However, awareness of marine conservation
issues is growing and many governments have made inter-
national commitments to sustainable development and the
ecosystem approach. Few of these international commit-
ments have yet to be translated into successful conservation
action, but there are some encouraging examples that sug-
gest combined controls on human impacts and large-scale
marine zoning schemes, which include marine reserves.
could lead to long-term improvements in sustainability.
The wealthy developed world currently has more capacity
to implement conservation measures, and yet many poorer
nations are responsible for species-rich and productive
marine environments. In many poorer nations, prospects
for improved sustainabilityare not good, unless the interna-
tional community commits to supporting and financing the
ecosystem approach and subsidizing the very high short-
term social and economic costs associated with moving
towards sustainability.
Current conservation actions take place in a marine envi-
ronment that has a lready been dramatically altered by
human activities.
 Further Reading
• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Chapter Summary
• Conservat ion is the sustainable management of the marine environment. Sustainable management
requires human intervent ion to maintain or create an environment t hat ensures that the well-bei ng
of future generat ions is not compromised.
• National and internat ional agreements express an aspiration to move towards sustainable develop-
ment, and these underpin much of the conservation and environmental protection legislation that
we see today.
• There are ethical, ecological, and economic reasons to conserve, but short-term economic forces
often d rive unsustainable development, despite the long-term economic benefits of conservat ion.
• Recent conservation policy reflects a high-level aspiration to achieve sustainable development.
However, converting high-level aspirations into practical , funded, and effective conservation actions
remains a challenge.
• Sustainable development includes not only biological and ecological considerations, but also
involves a considerat ion of the conseq uences of actions (e.g. conservation) for local economies,
and social and cultural structures.
• Conservat ion actions invo lve many levels of ecological (species, habitats, ecosystems) and adminis-
trative (local to inter national) organization. Their success depends on the w ealt h and cul t ural values
of society.

Further Reading
Kunin and Lawton ( 1996) provide a holistic analysis of the importance of b iod iversity and the necessity
for conservat ion. Norse (1993) provides a conservat ionist's po int of view of t he int eg rat ion of conserva-
t io n in decision making, wh ile Sutherland ( 199B) provides an objective v iew of the role of conservation
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Weblinks
Below we have provided a selection of weblinks that will
help you gain a more in-depth understanding of some of
the issues we have covered in Marine Ecology: Processes,
Systems, and Impacts. More importantly these websites open
the door to specific regional examples of marine ecology at
work, current issues, and data that you can download and
use. Weblinks evolve all the time, 50 while we have tried
our best to ensure all of these links are current some will
inevitably change. If they have changed, typing some of
the keywords in the description text will probably take you
relatively quickly to the new location. Alternatively. visit the
book's online resource centre at www.oxfordtextbooks.
co.uk/orc/kaiserze/ to access up-to-date URLs for all links
given here.
Antarctic & Arctic: There are many websites dealing with
Arctic and Antarctic issues. However. by going to the fol-
lowing websites it is possible to follow links to this wealth of
information and direct links to the organizations at which
Polar research is conducted:
http:/ /www.antarctica.ac.uk.
http:/ /www.arcus.org/index.html http:/ /nsidc.org/
index.html http:/ /www.scar.org.
Antarctic living resources: This is the website of the Com-
mission for the Conservation of Antarctic Marine Living
Resources. http:/ /www.ccamlr.org/pU/e/gen-intro.
htm. It contains information on Southern Ocean eco-
systems and efforts to take an ecosystem approach to
management of fishery resources there.
Antarctic spring phytoplankton bloom: Part of the NASA
Goddard Space Centre's web site, this provides images of
the seasonal development of the spring phytoplankton
bloom in the North Atlantic. It also provides information
on patchiness and some of the problems this presents
for sampling. http:/ /daac.gsfc.nasa.gov/CAMPAIGN_
DOCS/OCDST/nab.html.
Aquaculture: The Food and Agriculture Organisation of
the United Nations compiles and publishes download-
able data and figures on the cultivation ofaquatic organ-
isms around the world http:/ /www.fao.org. To find out
more about aquaculture research visit the University of
Stirling, Institute of Aquaculture website http:/ /www.
aquaculture.stir.ac.uk.
Benthos: The virtual handbook written by Tom Brey of
the Alfred Wegener Institute is a mine of information
regarding benthic ecology and production processes:
this can be cited as: T. Brey 2001. Population Dynamics in
Benthic Invertebrates. A Virtual Handbook . Version 01.2.
http :/ /www.thomas-brey.de/science/virtualhand-
booklnavlog/index.html Alfred Wegener Institute for
Polar and Marine Research, Germany.
Biodiversity research: DIVERSITAS is a major inter-
national program dealing with biodiversity and eco
system processes. as well as the links between eco-sys-
tern services and society. Many marine and intertidal
aspects are included in this program http :/ /www.
diversitas-international.org/.
Biodiversity and ecosystem function: A major website
holding up-to-date literature on marine biodiversity and
ecosystem functioning can be found at http:/ /www.
abdn.ac.uklecosystemibioecofunc/.
Bioluminescence webpage: http :/ /www.Iifesci.ucsb.
edu/biolum/, A site full of excellent information on
the biology of bioluminescence with pictures and video
clips.
Carbon cycle: For a general introduction to the marine
carbon cycle and the links between chemistry and biol-
ogy and global climate change see: http:/ /earthguide.
ucsd.edu/virtualmuseum/climatechangel/06_3.
shtml.
Climate change: A wealth of information about global cli-
mate change can be found at the website of the Intergov-
ernmental Panel on Climate Change: http:/ /www.ipcc.
chi. The North Atlantic Oscillation website, http:/ /
www.Ideo.columbia.edU/NAO/, provides everything
you wanted to mow about this climate pattern. describ-
ing the underlying mechanism, plotting data and linking
to other useful NAG web resources.
Coccolithophorids: For a detailed introduction into the
biology, biogeochemistry, and geology of this important
group of phytoplankton go to: http:/ /www.soes.soton.
ac.uk/staff/rt/.
Consequences of climate change: A global analysis of the
current and predicted effects of climate warming can be
found at http:/ /www.ipcc.ch.This site contains lots of
informative reports and illustrations of the predicted
effects of global warming.
Conservation: The website of the Society for Conservation
Biology http z/ z'conbio.net/scb/ provides up-to-date
access to key issues affecting the conservation of all
natural resources. The Marine Conservation Society of
the United Kingdom http:/ /www.mcsuk.org and Marine
Conservation Biology Institute USA http:/ /www.mcbi.
org provide lots of useful links to other organizations,
conservation work opportunities and projects, and sci-
entific information on current topical issues.
Coral reefs: For a global perspective on coral reefs see
http:/ /www.reefbase.org and for the International
 Weblinks
Society for Reef Studies webpage go to: http:/ /www.
fit.edu/isrs.
Deep-Sea: NOM Vents programme. http:/ /www.pme!.
noaa.gov/vents/. A site dedicated to information and
research on the geology and biology of hydrothermal
vents, with lots of pictures and video clips.
Detecting change in biological communities: For infor-
mation on detecting change in communities and key
considerations in experimental design, see the manual
on offer at http:/ /www.primer-e.com.
Diatoms: A key resource for anyone wanting to learn more
about diatoms is the International Society for Diatom
Research, which includes links to many other diatom
websites: http:/ /www.isdr.org/.
Estuaries: The website of the Estuarine Research Federa-
tion http:/ /www.erf.org/ provides information from
the world's largest estuarine science organization,
including publications, education, and links.
European Network of Excellence: MarBEF is a major net-
work of European marine ecologists that involves over
80 different institutes . This is an excellent starting point
for finding out what is going on in Europe and an ideal
starting point for finding placement work opportunities
or employment http:/ /www.marbef.org/outreachl.
Evolution & Diversity: The Tree of Life Web Project (ToL)
is a collaborative effort of biologists from around the
world. On more than 3000 worldwide web pages, the
project provides information about the diversity of
organisms on Earth, their evolutionary history (phylog-
eny), and characteristics. http:/ /tolweb.org/tree/ .
Exploitation ofnon-biological resources and renewable
energy: For exploitation of non-renewable offshore
resources and alternative forms of energy generation
such as windfarms see http:/ /www.thecrownestate.
co.uk. This website has links to reports and information
regarding the amount ofmaterial removed from the sea-
bed and the potential of wind and wave energy to meet
future energy requirements.
Flagellates: A website dealing with flagellates that are
important in microbial processes in marine systems, and
well introduced at http:/ /tolweb.org/notesl?note_
id=50.
Fisheries: Up-to-date global fisheries statistics includ-
ing biological and economic information is available
through http:/ /www.fao.org. Regional information
for Europe is available at http:/ /www.ices.dk where it
is possible to download a database of European fisher-
ies statistics. Current research in the US can be accessed
through http:/ /www.noaa.gov/fisheries.html which
is a highly informative website with respect to current
issues in fisheries and gives access to free to use photo-
graphic images . A particularly informative industry-run
website can be found at http :/ /www.fishingnj.org,
which gives the fishers' angle on current issues. A more
commercial perspective is given at http:/ /www.seafish.
co.uk where you will also find excellent seafood recipes.
Other informative research websites include those of
the Centre for Environment. Fisheries. and Aquaculture
Science http:/ /www.cefas.co.uk, Fisheries Research
Services Aberdeen http:/ /www.scotland.gov.ukltop-
ics/marine, the Australian Institute of Marine Science
http:/ /www.aims.gov.au. Visit the Worldfish Center
website for more information about Asian and African
fisheries and projects http:/ /www.worldfishcenter.
org.
Habitat listing: The MarUN database held at the Marine
Biological Association of the United Kingdom gives
access to a wealth of information about intertidal and
subtidal coastal habitats with links to primary and 'grey'
literature that is invaluable for learning and research
http:/ /www.marlin.ac.uk.
Harmful algal blooms: Information about algal blooms
and harmful algal blooms, red tides, and algal toxic-
ity can be found at: http:/ /www.whoi.edU/science/
redtide/ as well as http:/ /www.bigelow.org/hab/ .
Longterm data sets: There are a number of long-term
oceanographic data sets for which biological, chemical.
and physical data are collected to examine seasonal,
inter-annual. and even decadal variations:
Hawaii Ocean Time-series (HOTS) http:/ /hahana.soest.
hawaii.edu/hot/hotjgofs.html
Bermuda Atlantic Time-series (BATS) http://bats.bios.
edU/
Monterey Bay time-series study http:/ /www.mbari.org/
bog/Projects/centraicaVsummary/ts_summary.htm.
VOS UnderwaypC02 Program http: www.pme!.noaa.gov/
co2/uwpco2/
Continuous Plankton Recorder Survey: http:/ /www.sah-
fos.ac.uk/.
Mangroves: For mangroves, see http:/ /www.ncl.ac.ukl
tcmweb/tcm/mglinks.htm, A site listing most of the
major websites dealing with mangroves and wetlands .
Maps of major marine environments:
http:/ /www.oceansatlas.org/
http :/ /www.teachers.ash.org.au/jmresources/
marine/environments.html
Marine Institutes: There are a number of websites that
give extensive listings of places around the world where
marine research takes place:
http :/ / oceanlink.island.neVcareer/ careerlinks.
html
http:/ /www.skio.peachnet.edU/resources/
marinelinks.php
http:/ /www.sams.ac.uklabout-us/
linksl?searchterm=links
http:/ /www.marbef.org
Marine systems: GLOBEC http :/ /www.pm!.ac.ukl
globec/ is the International Geosphere-Biosphere

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •
Programme (IGBP) core project responsible for under-
standing how global change will affect the abundance,
diversity, and productivity of marine populations. This
web site gives summaries of recent GLOBEC-related
work and access to data.
Meiofauna: The website of the International Association
of Meiobenthologists and all you wanted to know about
meiofauna http:/ /www.meiofauna.org/.
Microbial loop: Background information about the micro-
bialloop and why it is important can be found at: http:/ /
www.bigelow.org/bacterial.
Satellite imagery: The Sea-viewing Wide Field-of-view
Sensor (SeaWiFS) Project http:/ /seawifs.gsfc.nasa.
gov/SEAWIFS.html uses satellite observations to pro-
vide quantitative data on global ocean bio-optical prop-
erties. This website provides an overview of the project,
has some excellent summary maps and even enables you
to produce mapped globes from a perspective of your
choice.
Weblinks
Seagrasses: WCMC Global Seagrass Database. http :/ /
www.unep-wcmc.org/marine/seagrassatlas/. Based
around the world atlas of seagrasses, the website gives
some introductory information, but most interestingly
has a series of online maps showing the distribution of
seagrass species around the world .
Seaweeds or macroalgae: Probably the best starting point
for any seaweed-related enquiries. http:/ /www.sea-
weed.ie. Algaebase http:/ /algaebase.org has details
on 57 000 algal species, 1500 images, 33 000 biblio-
graphic items, 104 000 distributional algal records, and
a 27 ODD-word online glossary.
Viruses: This website gives a good general overview of
aquatic viruses and current research topics in the field,
as well as further weblinks: http:/ /library.thinkquest.
org/CR0212089/halo.htm.
This page intentionally left blank
Index
Locators for headings which also have subheadings refer to gene ral aspects of that topic
Species appear un der their common and family names where possible
c -proteobacte ria 100-1 ,1 0 7
ABC curves 409
a bunda nce
annual variations 23
bacteria 105
and body size 23, 27-8
and compe tition 24-6
deep sea 264
seasonal trends, m icrobial 11 7
a byssal plain 252-3, 256-60
a byssopelagic zone 74 , 196
ACe (Anta rctic Unipolar Curre nt) 344
acclimation 47-9
accretion , Nile delta 4 16
acid ification 57, 422-6
acoustic sa mpling 209-11
active fishing gears 364-5
activity conce pt 115
adaptations, polar regions 334
add itive effects, disturbance 403
adsorption 115
aggregate extract ion 417-9
agriculture, impact 41 4
Agu lhas leakage 203
a he rmatypic corals 30 6
Alaskan pollo ck 357
albatross, im pact of fishing 37 1
Aldabra Atoll 308
algae . see also phytoplankton; seaweed
blooms 7 1, 120- 1,337- 8, 4 14
ca rbon storage 34
coralline 3 12 , 424-5
dinflagellate symbiotic 3 10
elemental composition 53 , 54-5
farming/biofuel 67,68
inorgani c nutrients 50
microbial ecology 111- 5
primary production 34-6, 64-8, 73
salinity cha nges , tolera nce 154
zonation 3, 224
alginate s 385
alien species 397, 42 1
Allee effect 163
Allen plots 130-1
allo chthonous species 99 ,260
allometric relationships, secondary
production measurement 131- 3
alternative stable states 122
Alvin 255,271
Amazon es tuary 143
ammonite s, complexity 27
a m moniu m 101 , 122
amphipod, gia nt 261 a rten -mi nim um 166
Amundsen Sea 1 Arthrocnemum spp. 164
a nchovy, Peruvian 357 asse mbly, genome 102
a ngios pe rms, seagrasses. see seagrass assessm ent . see measurement
a nimal attached remote sensing 284-5 Aswan High Da m 4 16
a nimal motion, te mporal/spatial patterns Atlantic Ocean, food webs 236
203 Atlantis 194
a nnotation , genomic 102 ato lls 30 7, 308- 9
a nnual variations. see seasonal cycles a tten uation , light in water 45
a noxia 4 14-5 . see also eutrophication aurora borealis 325
anoxygenic heterotrophs 43 Australia
anoxygenic phototrophs 44 conservation 444-5
Anta rctic/Arctic comparisons 331- 2, Embley River estuary 161
343-4, 350-1 endemism 15
Anta rctic krill 196 Swan River estuary 156
Anta rctic shallow waters, fauna 24 a utochthon ous species 100, 160
Antarctic Unipolar Curre nt (ACC) 344 a utomated aquacult ure cages 39 1- 3
a nti-fouling paint 420-1 a utomatic measurement devices 82-6
a ntibiotics 386, 394 a utonomous un derwater veh icles (AUVs)
a nticyclon ic gyres 7 1 83, 194, 209 , 2 12,25 3,254, 336
a photic zone 45 a utotrophs
a ppe nd icular ians 94 net ocean productivity 74-6
aquaculture 377-8, 399 season al cycles 122
biotechnology 386-7 zooanthellae 3 10
cages 387-9 1 a utumn season 118,11 9 ,1 22,1 23
conservation role 398-9 AUVs . see autonomous underwater
cultivation systems 387, 387- 9 1 veh icles
d isease 383, 386-7,393-4, 399 azoic zone 265
environmental impacts 395-7 Azores, conservation 438
feed re qu irements/ constraints 378- Azov Sea 169
80, 385-6
further reading 400 BACI (Before After Control Im pact)
global d istribution 383- 5 experimental design 4 13
global sta tistics 38 1,385 bacte ria 89. see also m icrobial ecology
historical account 378-8 1 communities 106- 7
methods 38 1-3 fingerprinting methods 10 7
mollusc 39 5-7 growth dynamics 115-8
offshore 39 1-3 key organism groups 97- 109
population biology 390 marine snow communities 108-9
sea ranching 397-8 oligotrophic 98
shrim p 393-4 osmotrophs 93
welfare 382, 384 polar regions 333
aquaria, public 440 species numbers 90
aquatic systems, primary production 73 Bacteroidetes 100
archaea 89,97-109 balla n wrasse 389- 9 1
Arctic/Antarctic comparisons 331- 2, Baltic Sea 168-9
343-4,35 0-1 bar-built estuaries 145
Arctic Ocean 331 barnacles 2 , 3, 4 , 180
sea-ice cha nges 339,35 1 barrie r coral reefs 307. see also coral
nutrients limiting growth 340--1 reefs; Great Barrie r Reef
a rms races, evolutionary 38, 232 , 289 barrie r, River Thames 422
Arrhenius re lationship 11 basin mangroves 278
 Index

basking shark 285 biotechnology 386--7 isotopes 4 0

bathymetric distribution, lobster 266 biotopes, continental shelf 241,242 pools 95
Bathymodiolus 274 bioturbation . see a150 disturbance radiocarbon la belling 78-9
bathypelagic zone 74,75,196 continental shelf biota 232-4 sources, estuaries 159- 61
bathysnacks 253-4,255 grapsid crabs 287 storage, deep sea 256--7
bathysnap system 253 shores 188, 191 carbon dioxide 38-41,78,422--6
Bay of Fundy 148, 149 birds carnivores 232. see also predator-prey
beaches. see shores estuaries 161- 3 systems
bears, polar 347-8,350 impact of fishing 371 carrying capacity
bedrock substrata, continental shelf polar regions 345-51 aquaculture 380
241-4 shore experiments 185 ecosystems 12 6
Before After Control Impact (BACI) bivalve molluscs oxygen 421
experimental design 413 aquaculture 395-7 catches, fisheries 359,368
Beggiatoa 43 competition 25 Caulerpa taxifolia 295-6
belief-based science 447-8 experiments 181,411-2 CCAMLR (Convention on the
benthic ecosystems. see seabed habitat! suspended rope cultivation 397 Conservation of Antarctic Marine Living
biota black band disease 314 Resources) 436
bentho-pelagic coupling 232, 343 Black Sea 169 CDOM (coloured dissolved organic
benthos, polar regions 341-4 black smokers 271-2 matter) 45--6,46, 81, 82
Big Fish Eat Little Fish picture 199-200 bleaching, coral 315--6,421 cell-counting, bacterial 116
biodiversity blind estuaries 145, 146 Challenger 194
and abundance 24 blooms, piankton 71, 120-1,337-8, 414 change. see also regime shifts
conservation 439, 440 body mass . see size detecting 408,410-1
coral reefs 306,313-4 BOIS database 430 natural 402
deep sea 265-7 bommies 307 sea-level 144-5,151-2
and ecosystem function ix, 21, 22 bottom-trawling 137-9,364 charismatic species 433
estuaries 143, 165-8 bottom-up processes chemical dispersants 4 17
hypersaline waters 169 food web dynamics 117-8 chemolithotrophs 97-8,98
index 15, 16,407,408,409 secondary production 134 chemo-organotrophs 43
mining 419 shore commun ities 181, 183, 188 chemosynthesis 261,272
patterns 9, 10,11,15-22 boundary layer 229 chemotrophs 43-4
polar regions 335 Bouvet Island 11 Chesapeake Bay 145, 249, 4 26, 4 27
seagrass meadows 292,299-300 brachiopods, competition 25 Chilean jack mackere l 357
shore communities 182, 190-1 brackish water systems 168-9 choice, consumer 443-4
willingness to pay for 438 Braer, oil spillage 417 chlorophyll 41,51-2,204
biodynamics. see population dynamics breathing holes, pack ice 348-9 chronic life cycles, viruses 111
bioerosion, coral reefs 309,318-20 Brent goose 161-2 chub mackerel 357
biofuel 67 Brent Spar oil platform 446 clam species (various)
biogenic reefs, continental shelf 248-9 brine channels, sea-ice 334 climate change 421
biogeography 9-15,203-5 broadcast-spawning 23 secondary production 127,128-3 1
bioinfonnatics 102 bryozoa, secondary production 127 classification of estuaries 144-8, 15 1
bio-iogging 285 bubbles in w ater 45--6 cleaner wrasse 322,389-91
biological capacity, fishe ries 360 buffer zone, current velocity 229 climate change 6, 139--40,401,421. see
biological pump 57,124 bulldozers 232 a150 temperature
bioluminescence 257,258 Burgess Shale 18 acidification 422--6
biomass carbon sinks 57
continental shelf 248 cages, aquaculture 387-91,391-3 coral reefs 315
deep sea 264 calcium 54 eutrophication 421
definitions 232 Cambrian fauna 19 rainfali 422
estuaries 159- 60 CAMERA (Community sea-ice 350-1
fisher ies 366-8 Cyberinfrastructure for Advanced water circulation 422
kriil 345 Marine Microbial Ecology Research and climate patterns, marine 6--7
microbial 90, 115--6 Analysis) 102 coastal biomes 11-2,205
and ocean depth 19 7 Canada, Fraser River 155 coastal p lain, estuaries 14 5
to production ratio (P/ B) 128 Canadian cod 359 coastal waters, primary production 71
and size 91 carbon 55-9 Coastal Zone Colour Scanner (CZCS) 10,
temporaVspa tial patterns 204-5 aigal growth 64-8 II
biomes 11-2,205 bacterial growth 116 coccolithophorids 56
biota. see flora/fauna cycles, globai 123-4 cod 238
 Index
•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

aquaculture 377 glaciation 2 19,220-2 red coloured 197

Canadian 359 hard substrata 241-4 shore 186
continental shelf 244 light/turbidity 223-4 cryopreservation 386
deep-sea 254 primary prod uction 71 cultivation systems, aquaculture 387
historical account of fishing 358 seabed habitat/biota 224-31 culture-independent genetic analysis 99
polar regions 351 size, organism 227-9 curlew 162
salinity tolerance 168 specific habitats 241-9 currents, ocean 5--6, 422
whiting impact 406 trophic cascades 237-8 Antarctic Unipolar 344
cohort-based methods 129- 31 wave action/currents 219-23,229 continental shelf 2 19-23,229,246
cold seeps 273-4 continental slope 252 deep sea 258-9
colonies, and organism size 28 Continuous Plankton Recorder (CPR) Gulf Stream 7
colour sensors 36, 195 surveys 84-5,213 polar regions 328-9
coloured dissolved organic matter Convention on Biological Biodiversity 15 cyanobacteria 59
(CDOM) 45-6,81,82 Convention on the Conservation of Cycliophora phylum 2
Community Cyberinfrastrueture for Antarctic Marine Living Resources cyclones 315,402
Advanced Marine Microbial Ecology (CCAMLR) 436 cyclonic gyres 71
Research and Analysis (CAMERA) 102 conversion efficiency 381 CZCS (Coastal Zone Colour Scanner) 10,
compensation conveyor belt, global 258,328-9 II
depth 48 copepod species
irradiance 46 human impacts 139-40 damming rivers 416--7
point, seagrass meadows 293 parasites 161 Darwin, Charles 307,308
competition spatial patterns 206 data sets, long-ter m 84-6,410
and abundance/biodiversity 24-6 Cope's rule 28 DBL (diffusive boundary layer) 50, 52-3
and ammonium 122 coral bleaching 315--6,421 decapod crustaceans, deep sea 269-70
and latitude 26 coral reefs 56, 58, 305, 323 decomposition 55, 89, 93-7
shore zonation 180 acidification 424-5 deep sea 251,275. see also hydrothermal
complexity 27 further reading 323-4 vents
conservation 429-3 1,449 hu man impacts 314-8,320,322-3 abundance/biomass 264
in action 442-7 Impact of fishing 317, 318, 322, 363, abyssal plain 256--60
ecolabelling 442, 443-4 374-5 biodiversity 265-7
economics 43 5-9, 446 organisms/communities 309-11, carbon storage 256--7
ecosystem approach 432,435,436 3 13-4,320 currents 258-9
environmental impact assessment population dynamics 320-2 definitions 252
442- 3 prod uctivity/food webs 311-3 dissolved organic material 261
evidence-based 447-8 reef development/distribution 305-9 dissolved oxygen 258
fish communities 207 reef growthlbioerosion 318-20 further reading 275-6
fund ing 446 reproduction 3 10-11 gigantism 270-1
further reading 449 types 307 hydrostatic p ressure 259
future scenarios 448 Coriolis current 259 large food falls 261-2
habitat 433-5 Coriolis force 202,223 light 257
legislation/policy 439-42 Corophium volutator 163 major organism groups 267-70
life cycle analysis 448 CPR (Continuous Plankton Recorder) organisms 253, 254, 255, 258, 260,
marine reserves 444-7 surveys 84-5,213 261,263-71
reasons for 431-2 crab species particulate organic material 262
role of aquaculture 398-9 climate change 421 produ ctivity 260-3
valuing certain species over others d isturbance 403 sampling 252-5
432-5 food webs 237 sediment 259--60
consumer choice 443-4 mangrove 287-8 size, organism 264-5
contaminants 4 19- 21. see also pollution spawner-recruitment relationships species composition trends 266
continental shelf 1,195,217-8,249-50 363 temperature 257-8
biogenic reefs 248-9 temperature effects 154 timing of food inputs 262-3
biota, functional ro les 231-5,240 critical depth 48-9 zonation 263-4
communities 239-41 critical tidal level 179-81 Deepwater Horizon oil spillage 415, 4 17,
definitions 2 18 crocodiles 283 418
ecosystem type 224-7 cross-section, ocean basin 252 definitions
fisheries 358 crown-of-thorns starfish 1, 316--7 biodiversity 15
food webs 235-9 crustaceans. see also crabs; krill; lobsters; biomass 232
fronts/production 223 shrimps continental shelf 2 18
further reading 250 deep-sea 269-70 deep sea 252
 Index
••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
estua ries 143-4
fisheries catches/landings 359
mangroves 278-9
ontogenetic 286
pack ice 329-30
pelagic 194
pelagic ecosystems 195-7
productivity 67
seagrass meadows 290-1
secondary production 126-8
sessile organisms 286
shores 173
success 26-7
welfare 382
deforestation 414
deltas 143
density of seawater 4,198
deposition, sediment 150
depth distribution, lobster 266
determinants of zonation 179-81
detritus, marine 93~. see also marine
snow
nature/production 94-6
u tilization/recycling 96-7
diamond dredging 417
diapause depth 206
diatoms
adaptations 195-6
frustules 37-8
lipid constituents 54
polar regions 332,333-4,340
diel vertical migration (DVM) 19, 339-40
diffusive bou ndary layer (DBl) 50, 52-3
dimethylsulphide (DMS) 6 1
dimethylsulphonioproprionate (DMSP)
60-1
dinflagellate symbiotic algae 3 10
dioecious species 297
direct economic benefits 432
disaggregation 245
discards, fisheries 359
Discovery 194
disease
aquaculture 383,386-7,393-4,399
co ral reefs 3 14
dispersal, hydrothermal vent organisms
274-5
dispersants, oil spillage 417
dissipative beaches 177
dissolved organic carbon (DOC) 55, 95
dissolved organic matter (DOM) 45-6,
94-5
deep-sea 261
food webs, microbial 114
marine snow commu nities 108-9
polar regions 337
dissolved oxygen (DO). see
eutrophication; oxygen
distinctness, taxonomic 409
distribution, species 430 genomics 104
aquaculture 383-5 mangroves 289- 90
climate change 421 role of microbial ecology 9 1-3
coral reefs 305-9 seagrass meadows 302-3
human impacts 407,409,430 secondary p roduction 126
kelp beds 244 sediment 234-5
mangroves 279 shores 190-1
seagrass meadows 292-6 ecosystem goods/services viii-ix
disturbance 402 and conservation 431,433,439
ecological role 402-6 coral reefs 322-3
impact of fishing 371-4 impact of fishing 375-6
intermediate disturbance hypothesis ecosystems
404--{i carrying capacity 126
recovery rate 403-4 continental shelf 224-7
scale 402-3 secondary production 134-6
shores, rocky/sandy 188,191 ecotones 166
sources 402 ectoparasites 322
diversity index IS, 16, 407,408,409. see edge effects
also biod iversity sea-ice 337-41
DMS (d imethylsulphide) 61 seagrass meadows 300
DMSP (d imethylsulphonioproprionate) education, and conservation 439, 440
60-1 efficiency
DO (d issolved oxygen) . see
growth 91-2
eu trophication; oxygen
trophic yield/food chain 92-3
DOC (dissolved organic carbon) 55,95
effort controls 368
dolphins 213, 371,433
EFH (essential fish habitat) 372-4
DOM. see dissolved organic matter
EIA (environmental impact assessme nt)
dred ge netting 364
442- 3
dredging 417- 9
Ekman transport 201-2
drilling mud contamination 417
El Nino Southern Oscillat ion (ENSO) 6-7
drop-frame syste ms 253-4
annual variations in abundance 23
drought, impact on estuaries 155--6
climate change 421
drug resistance 386
coral reefs 3 15,316
d ugongs 301-2
primary production 204
dunlin 163
remote sensing 81
DVM (diel vertical migration ) 199,
temporal/spatial patterns 200
339-40
dynamic viscosity of seawater 196-9 electrode measurement devices 79-80
dynamite fis hing 363,374 eleme ntal composition, algae 53, 54-5.
see also nutrients
echinoderms. see sea urchins elephant seals 211
echo-sounding 211,220,336-7 Ely sea mount 372
ecoclines 166, 173-9 Embley River estuary, Australia 161
ecolabelling 442,443-4 emersion, shores 174
ecology, terrestriaVmarine comparison endemism 12-5,343-4
277 energy, renewable 147-8, 159-60
econo mic viability, mining 419 engineers, ecosystem 237-8, 287, 319
econo mics of conservation 435-9,446 ENSO. see EI Niflo
ecosystem approach enviro nmental grad ients, shores 173-9.
to conservation 432, 435,436 see also patterns, environmental
to fisheries management 375--6 environmental impacts. see human
ecosystem-based management 360, impacts
375-6 environmental variables, estuaries
ecosystem engineers 237-8, 287, 319 148-54
ecosystem fun ction 15 epifauna 175
and biodiversity Ix, 21, 22, 167-8, epifluorescence 37, 8 1, 116
190-1 epipelagic zone 74, 75, 196
and d isturbance 404 epiphytes 77-8,294
estuaries 167-8 EPS (exoploymeric substances) 94

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
erosIOn
coral reefs 309,318-20
current velocity 229
human impacts 414
sea-ice 341
error-to-mean ratio 411
essential fish habitat (EFH) 372-4
estuaries 143, 170-1
biodiversity 165-8
birds 161-3
carbo n sources 159-60
classification 144-8
definitions 143-4
dissolved oxygen 151
environmental variables 148- 54
evolution 144
fish communities 156--9
further reading 171
hypersaline waters 169-70
hyposaline seas 168-9
impact of freshwate r inflow 154-6
lagoons 170
origins of organisms 151- 3
productivity/food webs 159--65
salinity 148-9
saltmarsh systems 163-5
sediment 150, 154
stable isotope analysis 160-1
temperature changes 151, 154
zones 151
ethical responsibilities 431-2
EU. see European Union
eukaryotes, species numbers 90
Eulerian sampling 211
euphotic zone 4,45
Europa 340
European Union
Nature Information System (EUNIS)
241
regulations 440-2
Eurythenes (giant amphipod) 261
eutrophication 49-50,139,402,414-5,
421. see also hypoxia; oxygen
evidence-based conservation 447-8
evolution, estuarine species 144, 151- 3
evolutionary arms races 38,232,289
excess production, coral reefs 312
excretion 94
Exe estuary, Devon 161
exoploymeric substances (EPS) 94
experiments
acidification 425
human impacts 411-2
shore communities 180-2, 184-7,
190-1
explosive fishing 363,374
exposure, shores 174-5. see also wave
action
extinction 11
and abundance 23
coral reefs 3 13-4
detecting change 4 11
KT 18
and organism size 28
sea cows 429
whales 440-1
extra-o ral digestion 237
extreme environments 402
exudates 94
Exxon Valdez oil spillage 417
eye membranes, squid 196
facilitation 189
faecal pellets 338
faith-based fisheries management 369
Falkiand Isiands 11
farming, fish. see aquaculture
fauna/flora. see flora/fauna
fecundity, fish species 361
feeding, sioppy 94
feelings-based definitions, welfare 382
fetch 222
field experiments. see experiments
finge rprinting methods, bacteria 107
fish/fish communities
deep sea 270
estuaries 156--9
eutrophication 414
farming. see aquaculture
mangroves 290
and primary production 135, 136,
205-7
and sea urchins 318
seagrass meadows 298-9
shores 185
size structuring 136
vertical migration 199
welfare 382, 384
fishmeal feeding, aquaculture
378-80,385-6
fisheries 357,376
ecosystem-based management 375--6
environmental impacts 370-5
fish stocks assessment 366-8
further reading 376
future scenarios 376
global 357-61
historical account 358-9
human impacts 137-8
impact on birds/mammals 371
impact on coral reefs 3 17,318,322,
363,374-5
impact on kelp beds 375
management 359-60,368-70
methods 363-5
overfishing 359--60
pelagic ecosystems 212-3
population biology 362-3,366
Index
production 361
science 360-1
seabed impacts 371-4
stocks 361
water use impacts 416
fjords 144,1 46
Fleet Lagoon, Dorset, UK 170
flexible genomes 103
flora/fauna
conservation 433
continental shelf 224-31
coral reefs 309-1 1, 313-4
deep sea 260,266,268-70
hydrothermal vents 272-3
impact of fishing 371
mangroves 286-8
microbial 97-115
polar regions 11-2, 205, 332-7,
341-51
seagrass meadows 298-301
sea ice 332
Florida, mangroves 286
flound ers 157
flow cytometry 116
fluorescence 37,81,116
foam 62
food labeliing 442,443-4
food webs/chains 91
continental shelf 235-9
coral reefs 311-3
estuaries 159--65
marine detritus recycling 97
microbial 89,114,116-8,124
pelagic ecosystems 199- 200
polar regions 334,336
secondary production 135
fossils, trace 232
fragmentation, habitat 299-300
Fraser River, Canada 155
fringing
coral reefs 307
mangroves 278
fronts, bioiogical 72,204,207,223
frustules, diatoms 37-8
function-based definitions, welfare 382
functional roles, continental shelf biota
240
fund amental niches 266
funding, conservation 435-9, 446
further reading
aquaculture 400
conservation 449
continental shelf 250
coral reefs 323-4
deep sea 275--6
estuaries 171
fisheries 376
human impacts 428
microbial ecology 125
 Index
patterns, marine environmenta l 29
pelagic ecosystems 216
polar regions 352-3
primary production 87-8
seagrass meadows/mangroves 304
secondary production 140
shores, rocky/sandy 193
future scenarios
conservation 448
fisheries 376
pelagic ecosystems 214-5
shores, rocky/sandy 192
Galapagos Islands 306, 315
gastropod molluscs, biodiversity 10,
18-9, 20
gears, fishing 364-5
gene flow, hydrothermal vent organisms
274-5
genetic analysis, culture-independent 99
genetic modification, aquacultu re 386
genomics, microbial 101-4
ghost shrimp 181
gigantism
deep sea 270-1
polar regions 28, 344-5
glaciation
continental shelf 219, 220-2
origins of estuary organisms 152,
153, 157
global
aquaculture statistics 381,385
carbon/nutrient cycles 123-4
conveyor belt 258, 328-9
d istributions. see distribution
fishe ries statistics 357-8
primary production 69-76
secondary production 132-3
gold rush, shrimp 377,393-4
gonad secondary pro duction 128
Good Fish Guide (Ma rine Conservation
Society) 443
goose, Brent 161-2
Gould, Stephen J. 18
government policy, greening 432,
439-42
grand cycle, p rimary production!
decomposition 34,55
grazmg
continental shelf biota 232
food web dynamics 116--7
mangroves 282
seagrass meadows 301-2
grease ice 329,330,332
Great Astrolabe Reef 308
Great Barrier Reef 305--6,309
h uman impacts 314
Marine Park 43 6, 444-5, 446
Great South Bay, Long Island 145
greenhouse effect 6. see also climate detecting change 4 10-1
change estuaries 143, 146, 155--6
greening of government policy 432, eutrophication 4 14-5
439-42 experiments 411-2
grey mullet 157 fisheries 370-5
gross photosynthesis 46 further reading 428
gross production, definitions 67 hydrocarbon exploitation 417, 418
growth dynamics/measurement. see also indicators 408
nutrients interaction of multiple fact ors 426
microbial ecology 9 1-2, 115-8 measuring/assessment 406--3,442-3
secondary production 129-30 mining 4 17- 9
Guadalupe estuary 156 and natural fluctuations 402
Guidelines for Systematic Review of ozone holes 349-50
Effectiveness of Interventions in pelagic ecosystems 194,214-5
Conservation and Environmental renewable energy generation 148
Management website 132 riverine input/land use 413-4
Gulf of Mexico 219,415,417, 418 seagrass meadows 299, 300
Gulf Stream 7 and secondary production 136-40
Gulfwar 417 shores 172,192
gyrotactic trapping 209 water use 4 16--7
humus, marine 95
habitat/s osee also specific habitat types hurricanes 315,402
conservation 433-5 hydrocarbon exploitation 4 17,418
fragmentation 299-300 hydrodynamic processes 192
hadal zone 74 hydrophilous species 291,297
haddock 207 hydrophytes 291
haloclines 4 hydroponics 392
halophytes 164,170 hydrostatic pressure, deep sea 259
hard substrata, continental shelf 241-4 hydrothermal vents 197, 252, 271- 5
Hawaii Ocean Time series (HOT) 85 chemosynthesis 261
herbivory, fish 232 organism dispersal/gene flow 274-5
hermatypic corals 306,309-1 0,320. see organisms 272-3
also coral reefs productivity 272
hermit crab 237 hypersaline waters 169- 70
herring 23,214 hyposaline seas 168-9
heterotrophs 43-4. see also secondary hypoxia. see eutrophication; oxygen
production
marine snow 108-9 IATIC (Inter-American Tropical Thna
microbial 98, 122 Commission) 361
net ocean productivity 74-6 ibis, scarlet 283
high-nutrient-lew-chlorophyll (HNLC) ice-breaking research ships 326--7
regions 51-2,204 ice pancakes 329,330. see also pack ice
highly unsaturated fatty acids (HUFAs) icebergs 329, 330, 341
379 ICZM (integrated coastal zone
historical accounts management) 441-2
aquaculture 378-81 ideal despotis distribution 163
fisheries 358-9 IDH (intermediate disturbance
Hong Kong, sustainable fishing 447 hypothesis) 404-6
HOT (Hawaii Ocean Time series) 85 immigration rates 11
HUFAs (highly unsaturated fatty acids) increment summation method 130-1
379 indicators, environmental impacts 408
human impacts 401-2,428,431. see indices, biodiversity 15, 16, 407, 408, 409
also climate change; conservation; Indo-West Pacific hotspot 19
disturbance; pollution induction,lytic cycles 110
aquaculture 395-7 industrial revolution 57
contaminants 4 19-2 1 industrialization, aquaculture 378
continental shelf 2 17 infauna 175
coral reefs 314-8,320,322-3 inoculu m size 295
current changes in sea-ice 350-1 inorganic nutrients 49-53, 54

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••
integrated coasta l zone management
(ICZM) 441-2
Inter-American Tropical Tuner
Commission (IATIC) 361
intermediate disturbance hypothesis
(IDH) 404--jj
internal waves 175
International Union for Conservation of
Nature (IUCN) 433,434
intertidal ecology 173. see also shores
invasive species 294-6, 396
invertebrates, human impacts 137-8
Irish Sea
glaciation 220
larvae dispersal 221
succession 69
iron 51-2,54
krill 341
and primary production 204-5
irradiance 46--7. see also light in water
island biogeography 10--1
IUCN (International Union for
Conservation of Nature) 433, 434
jack mackerel, Chilean 357
J amaica 11,316Japan 11,71
jellyfish blooms 214
Juncus spp. 164
J upiter 340
karyostrophy 48
k-ecotypes 106
kelp beds 239
continental shelf 242
global distribution/structuring 244
impact of fishing 375
primary production 76-8
keystone species 182- 3, 204, 336
kill-the-winner hypothesis 110
kinematic viscocity 112-3
kleptoparasitism 237
knees, mangroves 280
krill 19 6, 204, 341, 335-7, 345
K-seleetion 263
KT mass extinction 18
labelling food 442,443-4
lacunar systems 291
lagoons 170
Lagrangian sampling open ocean 21 1
Laguna Madre, Texas 170
land use, human impacts 413-4
Lander systems 253-4
landings, fisheries 359
Langmuir circulation 200-1
large food falls, deep sea 261-2
large oceanic gyres 71
larvae dispersal, scallop 220-1
larval viability, contaminants 419- 20
latent cycles, viruses 110
lateral advection 343
latitude, and competition 26
LCA (life cycle analysis) 448
leatherback turtles 211
lecithototrophic organisms 4,274
legislation, conservation 439-42
leucine growth dynamics, bacterial 115-6
life cycle analysis (LCA) 448
life mode, continental shelf biota 230-1
life-stage, and secondary production 128
Light Detection and Ranging (UDAR) 81
light in water 44-6
acclimation 47-9
continental shelf 223-4
coral reefs 311
deep-sea 257
and photosynthesis 46--9
and primary production 70
zonation 4,45
limiting resources 117-8, 180. see also
nutrients
lipids 53, 54; see also HUFAs; PUFAs
littoral zone 3
lobsters 266
Long Island, Great South Bay 145
long-term data sets 84-6,41 0
low latitude p lankton communities 122
low molecular weight (LMW) products 93
lugworms, experiments 187
lysogenic/lytic cycles, viruses 110
mackerel 2 12,357
Macoma balthica 168
macroalgae. see seaweeds
macro-ecology 9
macrofauna, continental shelf 227-9
mammals 345-51,371,433. see also
dolphins; polar bears; whales
management
conservation 440
ecosystem-based 360
fisheries 359-60,368-70
manatees 301-2
mangroves 164, 170, 277-8, 303
adaptations 279-81
associates 278,281-8
carbon storage 34
conservation 436--7
definitions 278-9
d istribution 279
ecosystem function 289-90
further reading 304
primary prod uction 35
reproduction 281
shrimp aquaculture 394
manipulative field experiments. see
experiments
Index
mapping, deep-sea 252
Marella 18, 19
Margalefs diversity index 15
marginal ice zone (MIZ) 337,338
Marine Conservation Society
Good Fish Guide 443
marine detritus . see detritus
marine humus 95
Marine Life Information Network 241,
242
Marine Protected Areas (MPAs) 446
marine reserves 440,442, 444-7
marine snow 95,96,105,107,108-9,
197
Marine Stewardship Council (MSC) 443,
444
market va lue, and conservation 432
MarXan software 435
mass balance calculation 75
mass extinction. see extinction
MDS (multi-dimensional scaling) 410
mean troph ic ind ex (MTI) 408
measurement. see also below
fisheries stocks 366-8
growth, bacterial 115-8
human impacts 406--13,442
secondary production 129-33
un ivariate measures 40 6--9
measurement, primary production 78-86
automatic devices 82-6
electrodes 79-80
fluorescence 8 1
oxygen 78, 79-80
radiocarbon labelling 78-9
remote sensing 8 1-3
Mediterranean Sea 120,169,257,292,
296
meiofauna 175, 227- 9
melt pools, pack ice 332
membranes, eye 196
Membranipora membranacea
12 7
mesocosms 167,190-1
mesopelagic zone 74,75,196
meta-analyses, secondary prod uction
132-3
metabolism
heterotrophic 43-4
microbial ecology 89-91
metazoan zooplankton 111
methane clathrate 7
methanesulphonic acid (MSA) 338
m icrobial ecology 89, 124-5. see also
bacteria
algae 111-5
archaea 89,97-109
biomass 113
decomposition process 93-7
deep-sea 266
 Index

food web dynamics 116-8 MTI (mean trophic index) 408 Northeast passage 35 1
further reading 125 mudflats, estuaries 150 Norway, fisheries science 360-1
genomics 101-4 mudskippers 286-8 nucleotides, labelled 115-6
global carbon/nutrient cycles 123-4 mullet 157 number of species, deep sea 266--7. see
growth dynamics/measurement multibeam echosounders 21 1,220 also biodiversity
115-8 multidimensional scaling (MDS) 4 10 nutriclines 119
growth yield 91-2 multivariate measures, human impacts nutrients/ nutrient dynamics 49--63
Identifying 98-9 409-10 algal growth 64-8
key organism groups 97-115 mummichog 157,161 Antarctic/Arctic comparisons 340-1
metazoan zooplankton 111 Muro-ami fishing 374 aquaculture 385--6
organic-matter degrading species mussels 3,161,186,295-6 carbon 55-9, 64
99-104 Mya arenaria 152, 153 coral reefs 317
as powerhouse of ocean 89-91 myopsin, squid 196 cycles, global 123-4
prokaryotes 97-109 Mytilicola intestinalis 161 inorganic 49-53,54
protozoa 111 iron 51-2,54
seasonal cycles 118-23 nanomaterials 420-1 nitrogen 54,59-60
size 90-1 nanoparticles 420-1 phytoplankton 66
trophic structure 114 natant organisms 270 seagrass meadows 294
trophic yield/food chain efficiency natural fluctuations 402 sulphur 54, 60-3
92-3 nature-based definitions, welfare 382 trends, global 70
viruses 109- 11 nature reserves 440,442,444-7
wider ecological context 91-3 Nautile 255 obligate inhabitants, seagrass meadows
microbial loop 199 nekton. see fish; squid 298
rnicrobiota, continental shelf 227-9 nematode worms 27 ocean basin cross-section 252
microchemistry, fish 158 Neomysisinreger 154 ocean currents. see currents
microlayers 208 neritic zone 195, 196, 252 oceanic carbon pools 95
mid-ocean ridge 252 net community/ecosystem/primary oceanic conveyor 258, 328-9
migration, continental shelf biota 230-1. production, defi nitions 67 oceanic zone 195,196
see also vertical migration netting, fish 208,252-3,364 oceanography 4-5
Milankovitch cycles 6 networks, shore 190-2. see also food offsho re aquaculture 391-3
mineralization 89 webs/chains oil platforms, disposal 446
mining, human impacts 417-9 neustic zone 196 011 spillage 415,417,418
missing baseline effects 213 NGOs (non-governmental organizations) oligotrophic species/environments 49-
Mississipi dead zone 415 440 50,98, 122,204
mixed layer depth 48-9,203 niche differen tiation 283 ontogenetic, definitions 286
mixing 70 Nile River 4 16 ontogenic factors 269
mixotrophs 44 Nimbus satellite 10 OpenHydro Open-Centre Turbine
MIZ (marginal ice zone) 337,338 nitrate, seasonal cycles 122 148
mobility nitrifying prokaryotes, microbial 43, opticle particle counters (OPCs) 208
continental shelf biota 230-1 97-8,101 organic recycling 96--7
• • •
deep-sea megagfau na 268-70 nitrogen 54,59-60 orgamsm size. see size
models, disturbance 40 5 flux, estuaries 167 organisms of specific ecosystems. see
molluscs. see also bivalves; mussels; isotope ratios 161 flora/fa una
oysters pollution 414-5 organotrophs 97-8
aquaculture 395-7 no n-governmental organizations (NGOs) osmoconforme rs 153
biodiversity 10,18-9,20 440 osmoregulation 153-4
contaminants 420 no n-native species 397,42 1 osmotrophs 93, 98
monosex stocks, aquaculture 386 North America 10, I S, 155 otoliths, fish 158,362
Monteray Bay aquarium 440 North Atlantic right whale 440-1 over fishing 359--60
morphodynamic states, shores 174-7 North Atlantic cod 238 oxygen/oxygen levels 28. see also
morpho-species 15 North Atlantic Oscillation eutrophication
mortality estuarine fish communities 15 7, 159, abyssopelagic zone 197
fishing 367-8 160 carrying capacity 421
measurement 129-30 human impacts 139-40 deep-sea 258
mosaics, patch 403 regime shifts 213 estuaries 151
MPAs (Marine Protected Areas) 446 remote sensing 81 hypoxia 139
MSA (methanesulphonic acid) 338 North Sea mangroves 288
MSC (Marine Stewardship Council) 443, foam 62 measurement of primary production
444 regime shifts 213-4 78,79,79-80
 Index
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polar regions 345 regime shifts 19 5, 213-4 bentho-pelagic coupling 343

respiration 42-3
oxygenic heterotrophs 43
oysters 249,349-50,396,421, 426, 427
oystercatche rs 163
ozone holes 349-50
Pacific Ocea n 204,2 13-4
pack ice 326,328,329-32,346. see a150
sea-Ice
palaeoecology 232
pancakes, ice 329. 330
parad ox, plankton 208
Paranais spp. 155
parasites 237
particle feeders 232, 243
particle size gradients 175- 7. see also
sediment
particulate organic carbon (POC) 55
particulate organic material (POM) 94-5,
96
deep-sea 260,262
food webs, microbial 114
marine snow communities 108-9
passive fishing gears 364-5
patches
coral reefs 307
mosaics 4 03
patterns, marine 1-2,29. seeal.so
seasonal cycles; spatial patterns;
temperature; temporal patterns;
zonation
abundance/size 23-8
biodiversity 9,15-22,165-8
biogeography 9-15
biomes 11-2
climate 6-7
endemism 12-5
estimating past changes in sea-ice
338-9
estuaries 165-8
further reading 29
local versus regional 11
oceanography 4-5
pelagic ecosystems 200-7
polar regions 339
predator-prey systems 163
productivity 8-9
secondary production 132- 3
shore zonation causes 179- 81
PCBs (polychlorinated biphenyls) 4 19
pelagic ecosystems 194-5, 215--6
definitions 19 5-7
fisheries 212-3
further reading 2 16
future scenarios 214-5
physical processes 200-3
primary production/biogeography
203-5
sampling open ocean 208-12 benthos 34 1-4
size, consequences 198-200 birds/mammals 345-51
temporaVspatial patterns 200-7 current changes in sea-ice 350-1
penguins 284-5,346 endemism 343-4
Peruvian anchovy 134,357 estimating past changes in sea-ice
pH 38-9,57,79 338-9
Phaeocystis spp. 62 further reading 352-3
phase shifts 122. see also regime shifts gigantism 28,344-5
Philippines 436-7 organisms 11-2,205,332-7
phosphorus 54, 60 pack ice 329-32
photic zone 45, 196 primary production 71
photo-acclimation, polar regions 334 sea ice edges 337-41
photo-respiration 94 policy, conservation 439-42
photography, wildlife 157, 253- 5, 258 pollock, Alaskan 357
photophores 258 pollu tion
photosynthesis 36-42. see also primary and biodiversity 16
production coral reefs 317
algal growth 66 eutrophication 4 14-5
carbon dioxide 38-41 human impacts 419-21
and light 46-9 oil spillage 4 17-8
pigments 4 1-2 polychlorinated biphenyls (PCBs) 419
seasonal cycles, microbial 119, 121 polyculture 378,383
photosynthetic quotient (PQ) 55 polyphyletic taxa, seagrasses 291
phylogeography 13 polyps, coral reef 309-10
physical processes polyunsaturated fatty acids (PUFAs) 335,
continental shelf 219 340
coral reefs 3 11 POM. see particulate organic material
d eep-sea 256--60 Pompeii worm 272
pelagic ecosystems 200-3 population biology
physics of seawater 198 aquaculture 390
physiological tolerance, and zonation 179 fisheries 362-3,366
phytodetritus, continental shelf 223 population dynamics
phytoplankton. see also algae coral reefs 320-2
blooms 71, 120-1, 4 14 krill 337
fronts, biological 223 Porcupine Sea Bight 262-3,264,266
n utrient dynamics 66 Portuguese Man '0 War 7, 196
prod uctivity 8,9,35 PQ (photosynthetic quotient) 55
remote sensing 8 1,82 pravons 152, 153,269
shape 52-3 precautionary approach to fisheries
succession 69 management 368
pigments, photosynthetic 41-2 predator-prey systems. see also food webs
plaice continental shelf 23 1-2,237
continental shelf biota 230-1 estuaries 163
hu man impacts 138-9, 373 shores 181- 7
plankton. see also phytoplankton; seagrass meadows 300
zooplankton preliminary sampling 411
larvae dispersal 220-1 primary production 33-4,87
paradox 208 algal growth 64-8
pelagic ecosystems 198- 9 consequences for higher trophic leve ls
planktotrophic organisms 4 205-7
plasticity, seagrasses 292 continental shelf 2 17
plastochrone intervals 297 by ecosystem type 34
Plum Island Sound Estuary 161 and fronts, biological 223
pneumatocysts 77 further reading 87-8
poe (particulate organic carbon) 55 global trends 69-76
polar bear 347-8,350 heterotrophic metabolism 43, 43-4
polar regions 325-9, 352 inorganic nutrients 49-53
Arctic!Antarctic comparisons 331-2 light in water 44-6, 45,46-9
 Index

marine plants/algae 34-6 realized nich es 266 river disch arge, human impacts 4 13-4,
measurement 78-86 recirculation systems 391-3 417, 423. see also individual rivers by
nutrients limiting growth 53-63 recolonization/recovery rates, afte r name
pelagic ecosystems 203-5 disturbance 4 03-4 riverine mangroves 278
photosynthesis 36--42,46-9 recruitment strength 183 rivet hypothesis of biodiversity 22
phytoplankton 35,36 recyciing 96-7,120,121-3 rocky/sandy shores. see shores
polar regions 339 red coloured crustaceans 197 rock substrata, continental shelf 241-4
respiration 42,42-3 Red List (lUCN) 434 ROFIs (regions of freshwater in fluen ce)
seasonal trends 69 Redfield ratio 54-5 223
seaweeds 76-8 redshank 163 Roman times 378
and secondary production 134-5 redundancy hypothesis, biod ivers ity 15, root structures, mangroves 280
terrestrial comparison with aquatic 73 22 Rose Garden hydrothermal vent 2 71,274
primary space, shores 183 reefs, continental shelf 248-9. see also ROVs (remotely operated veh icles)
procedural control 288 coral reefs 253,254
production-to-biomass ratio (P/B) 129. reference points, fisher ies 368 R-selection 263
see also secondary production reflective beach es 177 rubbish pollution 215
and body mass 131- 3 regime shifts RUBISCO (ribulose biphosphate
human impacts 137-8 coral reefs 314 carboxylase/oxygenase) 37,39-40
productivity/ production. see also primary; impact of fishing 375
secondary production pelagic ecosystems 195, 2 13-4 SAHFOS (Sir Alistair Hardy Foundation
aquaculture 381,385 regions of freshwate r in fluen ce (ROFIs) for Ocean Science) 84
autochthonous 160 223 Salicornia spp. 164
bacterial 116 regulations, conservation 440-2 salinity
coral reefs 3 11-3 Remane diagrams 165--6 estuaries 148- 9
deep sea 260-3 remineralization 89,334 hyposaline seas 168
definitions 67 remote sensing 195 impact of freshwater inflow 154-6
estuaries 159- 65 animal attached 284-5 lagoons 170
fisher ies 361 primary production 8 1-3 mangrove adaptations 279-81
and fronts, biological 223 polar regions 336--7 pack ice 330
hydrothermal vents 272 remotely operated vehicles (ROVs) response of organisms 153-4
patterns, marine 8-9 253 ,254 seagrass tolerance 294
seagrass meadows 302 renewable energy 147-8, 159-60 shores, rocky/ sandy 176--7
seasonal cycles, microbial 118-23 replacement lines, fish eries 367-8 zonation 4,5, 176--7
prokaryotes 97-109. see also microbial replicates 412-3 salmon aquaculture 389-91
ecology reproduction salt-wedge effect 149
propagule pressure 295 coral reefs 310-1 saltmarsh systems 163- 5, 277-8
propagules, mangroves 281 mangroves 281 sampling
proteobacteria 100-1, 107 seagrass meadows 296-8 deep sea 252-5
proteomics 102 reptant organisms 270 measuring hu man impacts 408
proton acceptors 42, 43 research, river catchment to coast 218. see open ocean 208-12
protozoa I II also experiments pitfalls 412-3
protozoop lankton 338 reserves, marine 440,442,444-7 San Andreas fau lt 145
provinces 12, 205 resilience, ecosystem 235-7,320 San Francisco Bay 145
pseudofaeces 232 resource limitation 11 7-8, 180. see also sandpiper 161-2
PUPAs (polyunsaturated fatty acids) 335, nutrients sandy shores. see shores
340 respiration 42,42-3 Sargasso Sea 262
purple sulphur bacteria 43 and decomposition process 93-4 satellite sampling 211
purse seine netting 364 microbial 89, 119, 121 saturation irradiance 46
pycnoclines 4, 339 patterns, marine 75 scale, microbial ecology 89. see also size
pyrosequencing 102 seasonal cycles 119, 121 scallops 220-1,299
vertical distribution 74 scarlet ibis 283
quorum sensing 10 7 resuspension, sediment 343 scavengers
Reynolds' number 112- 3, 198 continental shelf 23 1
radiations, evolutionary 17 ribulose biphosph ate carboxylase/ deep-sea 261-2
radiocarbon labelling 78-9 oxygenase (RUBISCO) 37,39-40 scrence
ragworm 152, 154, 167, 186 Riftia 272-4 conservation 447-8
rainfali 422 right whale 440-1 fisheries 360-1
ramets 297 Rio Convention on Biological Diversity 440 scouring, by sea-ice 341
ranching, aquaculture 397-8 rippies 45-6 sea cows 301-2,429

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sea horses 398
sea-ice 328. see also pack ice
biota 332
birds/ mammals 346
current changes 350-1
edges 337-41
past changes 338-9
sea level changes 7,144-5,151-2
climate change 422
coral reefs 309
glaciation 219-22
sea lice 389-91
sea mounts 252,372-3
sea ranching 397-8
sea temperature. see temperature
sea urchins
and acidification 425
barren grounds 239, 375
coral reefs 319
deep-sea 268-9
and fish communities 318
seabed habitats 1, 4
continental shelf 224-31
fisheries 371-4
human impacts 138- 9, 371-4
Seafood Choices Alliance 443
seagrass meadows 277,303,277-8
associated organisms 298-301
carbon storage 34
definitions 278-9,290-1
distribution 292--6
ecosystem function 302-3
further reading 304-
grazing 301-2
primary production 35,78
reproduction 296-8
seals 211 ,346,347,349
seasonal cycles/dynamics. see also
temperature; temporal patterns
abundance 23
autumn 118,119,122, 123
microbial ecology 117-23
po lar regions 326,327-8
primary production 69
secondary production 128-9
spring 118, 12G-1 , 206
summer 118,121-3
winter 118, 123
seawater, physics of 198. see also
temperature
seaweeds. see also kelp beds
carbon storage 34
po lar regions 342-3
primary production 35,76--8
and seagrass meadows 294
SeaWiFS project 36,195
secondary production 126-8, 140
allometric re lationships 131-3
to biomass ratio 128
Index
d rivers 134-6 Sir Alistair Hardy Foundation for Ocean
further reading 140 Science (SAHFOS) 84
human impacts 136-40 sites of special scientific interest (SSSIs)
measurement 129-33 440
meta-analyses 132-3 Sivash 169- 70
size structuring 136 size, organism 27-8
secondary space, shores 183 and abundance 23
sedentary megafauna, deep sea 267-8 and biomass 91
sediment continental shelf 227-9
continental shelf 241,245-8 deep sea 264-5, 27G-1
coral reefs 311,317 food webs 136
deep sea 259-60, 268 measuring effects of human activities
ecosystem function 234-5 406
estuaries 150, 154 microbial 90-1
human impacts 413-4 and P/B ratios 131-3
influence of fauna on structure 233 pelagic ecosystems 198-200
manipulative experiments 190-1 polar regions 28, 344-5
and mining 4 19 sloppy feeding 94
resuspension 343 smelt 157
shores, rocky/sandy 174, 180 snow, marine 95,96, 105,107,108-9,
size gradients 175- 7 197
suspended 223 snowball earth 340
terrigenous 195 social circumstances, human 432,442
wave action 220 soft sediment, continental shelf 245-8
seine netting 364 solubility pump 57
self-sustaining seasonal cycles 122 somatic secondary production 128
sessile organisms Sorcerer II 102, 103
deep-sea 267 Southern Ocean
definitions 286 Arctic!Antarctic comparisons 332
Severn estuary, energy generation 14 7-8 biodiversity 20
shags, impact of fishing 371 Bouvet Island 11
Shannon-Weiner diversity index 15, 40 7, diatoms 333-4
409 high-nutrient-low-chlorophyll regions
shape, phytoplankton 52-3 204
shark, basking 285 krill 335-7
shelf break 218,252 nutrients limiting growth 340-1
Shinkai 6500 255 organisms 334
shipp ing lanes 441,445 sea-ice changes 339
shore crab 154 sea temperature changes 6
shores, rocky/sandy 172,192-3 southern right whale 86
biodiversity 190-1 Spartina spp. 164
bottom-up processes 181, 183, 188 spatial patterns
definitions 173 biodiversity 18- 21
disturbance/bioturbation 188, 191 pelagic ecosystems 200-7
environmental gradients 173-9 spawner-recruitment relationships 363
experiments 181-2, 184-7, 190-1 speciation rates 11
further reading 193 species richness. see biodiversity
future scenarios 192 species-area relationships 11. see also
organization of communities 18 1- 9 biodiversity
particle size gradients 175-7 sponges 242,345
primary/ secondary space 183 spring blooms/cycles 118, 120-1, 206
salinity gradients 176--7 squat lobster 266
shore networks 190-2 squid 196, 199,205-7,213,363
wave action exposure 174-5 SSSIs (sites of special scientific interest)
wetness/dryness gradients 173 440
zonation 177-81 stable carbon isotopes 40,160-1
shotgun sequencing 102 stakeholders 440
shrimps 157,377,387,393-4 starfish 1,182,237,316-7
siphon cropping clam 127, 128 statistics
 Index

aquaculture 381,385 coral reefs 306,311,316 trophic structure, microbial 114. see also
detecting change 411 deep-sea 257-8 food webs
fisheries 357-8 estuaries 151 trophic yield/food chain efficiency 92-3
stepping stone models 274 polar regions 328 tropical waters, primary production 70
stickleback, three-spined 157 response of organisms to 154 true mangroves 278
stipules 288 temporal patterns 5, 6. see also seas onal tube worms 186
stochastic peturbations 286 cycles/dynamics Tubifex tubifex 155
stock-recruitment relationships 362-3 abundancelbiodiversity 16-8, 23, 25 tuna 194
stocks, fisheries 361 ,366-8 food inputs, deep sea 262-3 aquaculture 384-5
Stommel diagram 200-1 pelagic ecosystems 200-7 dolphin-safe 213
storms, coral reefs 315 primary production 69 fisheries 363,364,371
stratification, continental shelf 223. see TEPs (transparent exopolymer particles) turbidity
also zonation 95 continental shelf 223-4
stressed environments 426. see also terrestrial habitats and seagrass meadows 293
human impacts carbon pools 95 turbulent eddies 229
biodiversity 15 and mangroves 281-5 turtles 211,301,371
coral reefs 310 primary production 73, 76 type 1/11 errors 411
current velocity 229 terrigenous sediment 195
estuaries 146,168 tethering, and seagrass meadows 298 UK Sustainable Development Commission
microbial ecology 94 TEV (total economic value) 436 148
response of organisms 153-4 Thames, River 146,156,157,159,422 ultraviolet (UV) light 7
submersibles, deep sea 255 thermoclines 4,5, 118, 122 adaptations to 196
subsidized fleets, fisheries 359 three-spined stickleback 157 algal growth 64
substrates, chemical 39 thymidine, labelled 115-6 damage 63
success, definitions 26--7 tidal energy generation 147-8 ozone holes 349-50
succession, phytoplankton 69 tidal-mixing 204 and seagrass meadows 293
Sueda spp. 164 tidal range ultrahaline conditions 170
sulphur 54,6G-3 Bay of Fundy 149 Ulva spp. 154
sulphur-oxidizing/reducing bacteria 43 continental shelf 222-3 univariate measures 406-9
summer seasonal cycles 118,121-3 estuaries 146 universal features, zonation 178, 179-81
supply-side ecology 183 tidal surges 422 uplift zones 177
surface area tide-dominated mangroves 278 upwelling 71,422,426
and biomass 113 timescales. see temporal patterns urchin barren grounds 239,375. see also
to volume ratios 28,90 Titanic 272 sea urchins
surface currents 6 top-down control US Magnuson-StevensAct 372
suspended rope cultivation, bivalve food web dynamics 116-7 UV. see ultra violetlight
molluscs 396,397 secondary production 134
suspended sediment 223 shore communities 181 valuation, marine ecosystems 437
suspension feeding 232 topographical classification of estuaries Van der Waals forces 245
sustainable development 431 ,435 144, 145, 149 variance, spawner-recruitment
sustainable fishing 447 total economic value (TEV) 436 relationships 363
Swan River estuary, Australia 156 tourism vertical migration 199, 339-40
swell 175 and climate change 421 vicariance hypothesis 279
Symbion pandora 2 coral reefs 322-3 viruses 109-11,116-7
symbiosis 310, 425 willingness to pay 438 vivipary 281,291
synergistic effects, human impacts 426 trace fossils 232 volume to surface area ratios 28, 90
syngnathids 399,400 Trades biome 11-2,205 vulnerability to fishing 370
transcriptomics 102
tannin 289 transparent exopolymer particles (TEPs) walruses 347
taxonomic 95 waste/rubbish pollution 215
distinctness 15,409 trawling 137-9,252-3,364,371-4 water circulation 422. see also currents,
diversity 15 trenches, deep sea 252 ocean
TBT (tributyl tin ) 42G-I tributyl tin (TBT) 42G-I water use, human impacts 416-7
technical measures, fisheries management triploidy 386 waterlogged soils, adaptations 279
368 trophic cascades 237-8 wave action
tectonic estuaries 145 trophic function 16 coral reefs 311
telemetry 285 trophic levels 12,91 patterns, marine environmental 5
temperature, land/ sea. see also climate secondary production 126 shores , rocky/sandy 174-5
change; seasonal cycles/dynamics size str ucturing 136 temporal/spatial patterns 200

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wave formation 175
websites
aquaculture 383,386,391
autonomous underwater vehicles 2 12
conservation 433, 443
Convention on the Conservation of
Antarctic Marine Living Resources
436
coral reefs 306, 308
fish production 135
Great Barrier Reef Marine Park 445
Guidelines for Systematic Review of
Effectiveness of Interventions in
Conservation and Environmental
Management 132
invasive species 295
MarXan software 435
OpenHydro Open-Centre Turbine 148
photography 157,258
sea horses 399
Seafood Choices Alliance 443
Sorcerer II 103
stock-recruitment relationships 363
UK Sustainable Development
Commission 148
world register of marine species 90
Index
World Resources Institute 266 wrasse 322,389-91
World Summit on Sustainable WTP (wiliingness to pay) 437,438
Development 432
welfare, fish 382, 384 xenophyophores, deep-sea 270-1
Westerlies biome 11-2,205
wetness/dryness gradients, shores 173 Yellow River 4 14
whales 86 yield-per-recruit models 367
biogeography 204
conservation 433, 440-1 zonation 2-4
extinction 429 causes 179- 8 1
impact of fishing 371 continental shelf 223-4
polar regions 338-9, 348-9 coral reefs 31 1
whe lks 237 estuaries 15 1
White Sea 169-70 pelagic ecosystems 196--7
whiting 157, 406 shores 173-9
wildiife photography 157, 253- 5, 258 universal features 178
wiliingness to pay (WTP) 437,438 zooanthellae 309,311
wind action zooplankton
and climate change 426 coral reefs 312
pelagic ecosystems 200,201-2 metazoan III
wind speed patterns 5 polar regions 338
winter seasonal cycles 118, 123 productivity 8, 74, 75
wood, deep-sea 262 vertical migration 199
World Resources Institute 266 Zostera spp. 294, 297-8, 300, 302
World Summit on Sustainable
Development (WSSD) 432,440
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