Eutrophication in Coastal Marine Ecosystems

Coastal and Estuarine Studies
Series Editors'
Malcolm J. Bowman ChristopherN.K.
Coastal
and Estuarine Studies
52
Bo Barker Jorgensen and

Katherine Richardson (Eds.)
Eutrophicationin
Coastal Marine Ecosystems
American Geophysical Union

Washington,
Ser!es Editors
Malcolm J. Bowman
MadneSdencesResearchCenter,State University
of New York
StonyBrook,N.Y. 11794, USA
ChristopherN.K. Mooers
Divisionof AppliedMarinePhysics
RSMAS/University of Miami
4600 RickenbackerCswy.
Miami, FL 33149-1098, USA
Editors
Bo BarkerJergensen
Max PlanckInstitutefor Madne Microbiology
D-28359 Bremen
Germany
Katherine Richardson
Danish Institutefor Fisheries Research
DK-2920 Charlottenlund
Denmark
Eutrophication
in CoastalMarineEcosystems
/ BoBarkerJorgensen
and KatherineRichardson(eds.).
p. cm. -- (Coastalandestuarine
studies;52)
Includesbibliographical
references
andindex.
ISBN 0-87590-266-9
1. Marineeutrophication. 2. Coastalecology.I. Jorgensen,
Bo Barker.
II. Richardson,Katherine. III. AmericanGeophysical
Union. 1V Series.
QH91.8.E87E871996 96-29236
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ISSN 0733-9569
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CONTENTS
PREFACE
Katherine Richardsonand Bo Barker J•rgensen .......................... vii
I Eutrophication:Definition, History and Effects
Katherine Richardson and Bo Barker J(•rgensen............................ 1
2 Atmospheric Processes
Willera A. H. Asman and S•ren E. Larsen ..................................
3 Water Masses, Stratification and Circulation

Jacob Steen M(•ller .................................................................. 51
4 Material Flux in the Water Column
Thomas Ki•rboe ..................................................................... 67
5 Carbon Flow in the Water Column Case Study:

The Southern Kattegat
Katherine Richardson ..............................................................
6 Material Flux in the Sediment

Bo Barker Jprgensen .............................................................. 1
7 Case Study--Aarhus Bay

Bo Barker Jprgensen .............................................................. 137
8 Benthic Macrofauna and Demersal Fish
Lars Hagerman, AIf B. Josefsonand J(•rgen N. Jensen ............... 155
9 Shallow Waters and Land/Sea Boundaries
Jens Borum .......................................................................... 179
10 Case Study: Kertinge Nor

Hans Ulrik Riisgt•rd, Carston J•irgensenand
Frede OstergaardAndersen................. :................................... 205
11 The Use of Models in Eutrophication Studies
Andr• W. Visser and Lars Kamp-Nielsen ................................... 221
12 Conclusion,Researchand Eutrophication Control

Katherine Richardson ............................................................. 243
INDEX ............................................................................................. 269
LIST OF CONTRIBUTORS ..................................................................

PREFACE
Overthe last 10-20years,eutrophication

hasbecomegenerallyacknowledged
as
an environmentalthreatfor manycoastalmarineareas.Nevertheless,mostof our
knowledgeof the effectsof eutrophication on aquaticecosystems is derivedfrom
limnologicalstudies.There are fundamentaldifferencesbetweenmarine,brack-
ish, and freshwatersystemsthat lead to differentresponses to eutrophication.
Therefore,the aim of this book is to providethe readerwith a synthesisof our
currentunderstanding of eutrophicationin coastalmarineareasandthebiological/
ecological responsesto it.
This book evolved out of the interaction between scientists from a number of
differentdisciplinesinvolved in the Marine ResearchProgramsponsoredby the
Danish Ministry of Environment and Energy duringthe period 1988-1994.This
researchprogram was establishedin the wake of considerablepublic attention
given to oxygendepletioneventswhich repeatedlyoccurredduringlate summer
in Kattegat bottom waters during the 1980s. In 1987, the Danish Parliament
adoptedmeasuresto reduce the nitrogenand phosphorusinput from Denmark to
the surroundingmarinewatersby 50% and 80%, respectively.Acknowledgingthe
needfor more researchinto the ecologicaleffectsof eutrophic•ttion,
the Parlia-
ment elected at the same time to fund the Marine ResearchProgram.
While conceivedwithin and partially supportedby a Danish researchprogram,

this book is designedas a generaltext dealingwith coastaleutrophicationin
temperate waters. A unique feature of the book is the integration of a general
descriptionof the chemicaland biologicalprocessesin coastalmarineecosystems
with a discussionof the effectsof eutrophication,drawingexamplesmainlyfrom
Danish waters. The reader will find a generic presentation of the processes
(hydrographicand atmospheric)that are responsiblefor the delivery of nutrients
to coastalmarinewaters, as well asfor the effectsof eutrophicationon pelagicand
benthic processes.Two papers deal specificallywith eutrophicationof the very
shallowwaters found at the land-seainterface.The final paperstreat the problem
of collatingand presentingrelevant scientificresultsin a form which is usefulfor
the administratorwho is dealingwith eutrophicationissues.Several of the papers
are followed by 'case studies' in which specificprojects carded out within the
Marine Research Program are described. We intend these case studies to be
illustrativeof someof the generalprinciplespresentedin the main papersand to
serveas modelsfor other workersphnning similarstudiesin otherareas.So that
otherscan profit most from the experiencesgainedin connectionwith the Marine
ResearchProgram,we have attemptedto be ascandidas possiblewith respectto
the successesand failures which resultedfrom the researchprojectsdescribedin
the case studies.
We thank all of our friends and colleagueswho have helped to produce this
book----especially
our colleaguesaroundthe world who served as anonymous
reviewers for the chapters presented here. Finally, we acknowledge that the
dream which led to this book could not have been realised without the financial
support of the Danish Environmental Protection Agency or the administrative
support of many of the Agency's personnelrainparticular J0rn Kirkegaard and
Jesper Andersen, who supplied wise guidance and support throughout the
production of the book.
Bo BarkerJorgensen
Eutrophication:
Definition,History and Effects
KatherineRichardsonand Bo BarkerJ•rgensen
Introduction
"Eutrophication" of coastalmarinewatersis a muchdiscussed topic- bothin the

scientificandpopularliterature.Unfortunately, however,few of thosewho usethe
termtake the timeto reflectupontheprocess that is actuallybeingdiscussedanda
numberof differentuses(definitions)ofthe term havecomeinto commonpractice.
In fact, the term eutrophicationhas its rootsin two Greekwords- eu meaning
"well" and tropewhichmeans"nourishment". Eutrophication can be definedas
theprocess of changing the nutritionalstatusof a givenwaterbodyby increasing
the nutrient resources.
The mostfrequentuseof the term and that whichis employed throughout this
bookis to describeincreases in the input of mineralnutrients(primarilynitrogen
andphosphorus) to a particularwaterbody.However,aspointedout by Nixon
[1995],it is not onlynitrogenandphosphorus thatdeterminethenutritionallevel
(= trophicstate)of a waterbody.He suggests thateutrophicationbedefined as"an
increasein therateof supplyof organiccarbonto an ecosystem". Thisproposed
definitionhastheadvantage thatit allowsus,at leastto somedegree, to quantify
thetrophicstateof thewaterbodies withwhichweareworkingonthebasisof a
singleproperty.
Organiccarboninputto a systemcomes eitherviaprimaryproduction withinthe
system(autochthonouscarbon)or via externalinputto thesystem(allochthonous
carbon).
Therearefewgoodmeasurements of allochthonouscarbon
inputto marine
systems.However,theprimaryproduction in manymarinesystems is wellmea-
sured.Thus,Nixon [1995]hasproposed a classification
schemewhichdescribes
fourtrophicstates(oligotrophic,
mesotrophic, eutrophicandhypertrophic)for
Eutrophicationin CoastalMarine Ecosystems

Coastal and Estuarine Studies, Volume 52, Pages 1-19
Copyright1996by the AmericanGeophysical
2 1. Eutrophication:
Definition,HistoryandEffects
TABLE 1.1.
Organiccarbonsupply(primaryproduction)
g C m-2y-•
Nixon's (1995)classificationscheme
for marine waters.
Oligotrophic < 100

Mesotrophic 100-300
Eutrophic 301-500
Hypertrophic > 500
Rodhe's(1969) classificationscheme
for lakes
Oligotrohic 7-25
Eutrophic(natural) 75-250
Eutrophic(polluted) 350-700
marinecoastaland estuarineecosystems basedon the primary productionoccur-

ring there.A similarschemewas developed for freshwatersby Rodhe[1969]. These
two classification
schemesare presentedin Table 1.1.
Most marinesystems can be classifiedas beingfrom oligotrophicto eutrophicin
their naturalstates.The SargassoSea,wherethe water columnis thermallystrati-
fied throughoutthe year and mineral nutrientsbecomeconcentratedin subsur-
facewaterswherelight doesnot penetrate,is a goodexampleof an oligotrophic
marinesystem.This book, however,is concernedwith coastalregionsof tempe-
rate shelfseasand theseare typicallyclassifiedas beingmeso-or eutrophic.In
suchseas,seasonalchangesin solar heatingand wind activity acting together
periodicallydestroythe stratificationof the water columnand ensuretransport
of nutrient-richdeepwater into the upperlayer of the water columnwherepho-
tosynthesiscan take place.Meso- and eutrophicseashave a higherfish produc-
tion than oligotrophicseas- a fact that has led to the quite serioussuggestion
that fisheriesin somewatersmay be improvedby kheadditionof nutrients(see
section 1.6).
Eutrophication canoccuras a resultof naturalprocesses. It occurs,for example,

via "upwelling"-in regionswhere the local hydrographicconditionslead to
transportof nutrient-richdeepwater (from the light limitedaphoticzone)to nu-
trient-poorbut light-richsurfacewatersof the "euphotic"(or "photic")region
of thewatercolumn.Forthe mostpart,however,whenwe speakof eutrophica-
tion, it is "cultural"eutrophication or that which is associated with anthropo-
genicactivitieswhichis of interest.It shouldbe notedthat both in popularand
scientific literatureit hasnow becomecommonto (incorrectly)extendthe appli-
cationof thetermeutrophication to includenot onlytheprocess of increasingthe
nutritionalstatusof a regionbut alsoto encompass the effectsof this
RichardsonandJorgensen 3
Whetheror not eutrophicationis occurringnaturallyor as a resultof anthro-

pogenic activities,
it affectstheecosystem in whichit isoccurringin thesameman-
ner.The mostimmediateeffectof eutrophication in mostsystems is an increasein
the plant(phytoplankton and/ormacrophyte) biomass.The plantbiomass present
at any givenpoint in time is a functionof plantproduction(growth)and loss(via
grazing,sedimentation, mortalityanddilution)processes. The production process,
growth,is, in turn,a fun/:tionof lightandnutrientavailabilityand(to a lesser de-
gree)temperature. Thus,any of thesethreefactorsaloneor in combination canbe
limitingfor the productionof plant biomassin the marineenvironment at any
pointin time.Whena nutrientis limitingor colimiting,a changein nutrientavail-
abilitythrougheutrophication canaffectthe plantbiomassin an ecosystem.
Nutrient Limitation
Most of our understandingof nutrient limitation of phytoplanktoncomesfrom

laboratorystudiescarriedout on unialgalcultures(see,for example,reviewby
Heckyand Kilham [1988]). As a result,thereis now a reasonable understandingof
the mechanismsof nutrient limitation at the cellular level. However, when consid-
eringentireecosystems
andth• potential
effects.of
eutrophication
uponthem,it is
necessary
to considerthe effectsof nutrientlimitationat levelshigherthan that of
the individual cell.
For somepurposes, for example,it canberelevantto consider nutrientlimitationat

the levelof populations[e.g.,Goldmanet al., 1979; and discussion by Howarth,
1988]. For otherpurposes, it may be relevantto considernutrientlimitationof
communitynet primaryproductionor net productionof the entireecosystem [see
Howarth, 1988 for examples]. The effectsof nutrientenrichment
at theselevelsof
the ecosystem are muchlessunderstood than thoseoccurringat the cellularlevel
andmuchof the research beingcarriedout on eutrophication andits effectstoday
focuseson the effect of nutrient enrichmentor reductionat the communityor
ecosystem
level.It isinteresting
to notethatmuchof [heapparent
disagreement
foundin the literatureconcerning
nutrientlimitationand the causes/effects
of eu-
trophicationcan be explainedby the fact that comparisons are, in somecases,
beingattempted between studies
carriedout at differenthierarchical
levelswithin
the ecosystem.
Theeutrophication effectswe recognizearethoseresulting
froma netincreasein
plant biomasswithin the system.Suchan increase in biomasscan only occur
throughan increase in "new" production as described
by Dugdaleand Goering
[1967].In the casestheydescribed, theexternalinputof nitrogenin theformof
nitrateis predictedto yieldan increase
.inphytoplanktonbiomass.Theseauthors
alsoidentifieda formof productionwhichtheycalled"regenerated"
based uponthe
recyclingof nitrogenwithintheeuphotic zone(seechapters
4 and5, thisvolume}.
Regenerated
production
doesnot leadto a netincrease
in biomasswithinthe
system.
Standard
primaryproductionmeasurements arenotableto
Definition,Historyand Effects
between newandregenerated production.Thus,an increase in themeasuredprimary

production ratedoesnotnecessarily implyan increasein biomassbut cansimplybe
the resultof an increase
in nutrientrecycling
rateswithin the euphoticzone.
The stimulation of plantbiomass whichcanresultfromeutrophication haspoten-
tial ramificationsfor energyflow andcangiveriseto a shiftin the balanceof natu-
rally occurring processeswithin the ecosystem. It is thesechangesin the balance
betweenthe differentprocesses occurringwithin the systemthat give rise to the
effectsthat are popularlyassociated with eutrophication (hypoxia,algal blooms,
changes in species diversityand abundance,etc.- seesections1.6-1.9).
1.3.CulturalEutrophication:
History
It is believedthat man hasbeenawareof the effectsof eutrophicationsincebefore
the beginning of writtenhistory.The factthat the Aztecsof Tenochtitlanchosenot
to dispose of their excretoryproductsin the nearbylake but, instead,spreadthem
on landsuggests that theywereawareof andconcerned aboutculturaleutrophica-
tion [Vollenweider,1992]. In addition,many believethat it was an algal bloom
causedby culturaleutrophication that is beingreferredto in the Bible:
... and all the waters that were in the river were turned to blood.
And thefish that wasin the riverdied;and the riverstank,and the Egyptians
couldnot drink of the water of the river... (Exodus7: 20-21}.
The culturaleutrophication of Europeanlakes(leadingto algalbloomsand oxygen
deficiency)
hascertainlybeenacknowledged asa problemsincethe early1800s[see
Vollenweider,1992].Asa result,thestudyof eutrophication's.impact on ecosystems
hasdeveloped almostexclusively withinthedomainof limnology. Understanding of
eutrophicationandits effectsis nowwell developed withinfresh-water
systems and
considerablesuccess hasbeenachievedherewith eutrophication controlbasedon
models designedto identify"acceptable" levelsof eutrophication
(seechapter! 1}.
However,it is onlyrelativelyrecentlythatculturaleutrophication of marinewaters
hasbeenperceived as a potentialenvironmental threat [e.g.,Rosenberg, 1985;
Gray,1992;Nixon, 1995].The lack of earlierconcernovereutrophication of ma-
rineareasis largelyexplained by thefactthat marineareasare characterized by a
greaterwaterexchange with surrounding waterbodiesthan landlockedlakes.As a
resultof thiswaterexchange,
thereisa greater
capacity
fornutrients
entering
a ma-
rinesystem
to bedilutedandtransported
awayfromthe inputsitethanthereis in
most lakes.
Eutrophication
in MarineversusFresh-water
Systems
In spiteof thisgenerally
greaterabilityfor dilutionof nutrientsin marinesystems,
the fundamental ecosystemresponse to eutrophication is similarin freshand ma-
rinewaters.Thus,muchcanbe learnedaboutmarineeutrophication by
the limnologicalliterature.However,there are essentialdifferences

betweenthese
two typesof systems
that preventus from simplyapplyingknowledge
gained
throughlimnological
studiesto themarineenvironment.
Themodels developed
to identify"acceptable"or "tolerable"
levelsof eutrophica-
tionin fresh-water
systems,for example,arefor themostpartnotimmediately ap-
plicableto marineareas.Many of thesemodelsarebasedon Vollenweider's [1976]
empirical(regression)
modelfor lake eutrophication whichincludes the flushing
rate(annualrateof waterexchange) andsedimentation ratesfor bothnitrogen and
phosphorus. The morevariablehydrodynamic propertiesandwaterexchange rates
in mostmarineasopposed to lakesystemsandthefactthat ratesof andprocesses
leadingto N and P sedimentationare generallynot well documented
for marine
systems makesthe immediateapplicationof Vollenweider-type modelsdifficult
[Gray,1992; seealsochapter11].
Anotherdifferencebetweenfreshand marinesystems is that phytoplankton are
generally believedto be phosphorus limitedin the formerandnitrogenlimitedin
thelatter.Thereis a livelydebatewithinthescientific community asto whetherthis
is,in fact,the caseand,if so,why thisshouldbe [see,for example,$metacek et al.,
1991; Codispoti,1989; Hecky and Kilham, 1988; Howarth, 1988; Smithand
Hollibaugh, 1989] and it is not the intentionto activelyenterthis debateor to
reviewthe problemhere.
Hecky and Kilham [1988] have, however,pointedout that the relativeelemental
requirements of marineand freshwaterphytoplankton appearto besimilar.On the
basisof a comparisonof the relativeelementalcompositionof phytoplankton and
that of averageoceanand river waters(Table 1.2), they arguethereare morepo-
tentialelementalcandidatesfor limitingphytoplanktongrowthin marinethan in
freshwater.In freshwater,theyidentifyonlythe relativepresence of phosphorusas
beinglower than or similarto phytoplanktonelementalcomposition. In marine
waters,however,nitrogen,siliconand phosphorus are all identifiedas beingpre-
sentin relativeamountssimilarto or lessthanthosefoundin phytoplankton. Thus,
theiranalysissuggests that P limitationof fresh-water
phytoplankton is the most
likelywhilethesituationwith respect to marinephytoplankton ismoreuncertain.
TABLE 1.2. Relativeelementalcompositionof algae (nor-
malizedto total dissolvedP (molarbasis))comparedto rela-
tivemeancomposition in riverandoceanwaters.FromHecky
and Kilham [1988].
Element River Algal Ocean
C 738 102 1,000

N 28(21) 11.1 13
Si 146 96 43
K 26 1.3 4,434
P 1.0 1.0 1.0
S 146 0.54
It shouldbenotedthattheHeckyandKilhamanalysis alsoincludeda comparison

of the relativeelemental
composition
of phytoplankton
and marineand freshwa-
terswith respectto metals.For freshwaters,onlyiron and cobaltwereidentifiedas
beingpresentin relativequantities similarto thosefoundin phytoplankton. Iron,
zinc,copper,manganese andcobaltwereall foundto bepresentin relativequanti-
tiesin marinewatersthat weresimilarto or lessthan thosereportedfor phyto-
plankton.
Whilethiscomparisonof therelativeelemental
compositionof phytoplankton rela-
tiveto marineandfreshwaterdoesnotestablish whichelement(s)
is (are)limiting
for phytoplanktongrowth,it doessuggestthattheapparent differences
reported
withrespect
to phytoplankton nutrientlimitation
in marineandfreshwatersmay
havetheirbasis
in thefundamental differences
in chemistry
between thetwotypes
of aquaticenvironments.
Thegeochemical
cyclingof N andP is alsoaffectedby the basicchemical differ-
ences
between
marineandfreshwater.Whiletheseprocesses arestillnot well un-
derstood,
it isclear,forexample,
thatmarine
sediments
havea lowerP-binding
ca-
pacitythanfresh-water
sediments.
Thisis at leastpartlydueto differences
in iron
chemistry
inthetwosediment
types
thatcanberelated
to thegreater
availability
of
sulfate/sulfidein marine than in fresh water.
Thus,although bothmarine
andfresh-water
systems
canrespond toeutrophication
byincreasingplantbiomass,
thedifferences
in marineandfresh-water chemistry
alonesuggestthattheprocesses
surrounding
eutrophication
inmarine systems
may
bequitedifferent
fromthoseoccurring
infreshwater.
Asa result,
it isarguedhere
thatthestudy ofeutrophication
inmarineenvironmentsisa uniquescientific
disci-
plinewhichisrelated
tobutdistinct
fromthestudyofeutrophicationinfresh-water
systems.
CulturalEutrophication
in MarineWaters-
Extent of the Problem
Examples
ofmarine
areas
where
cultural
eutrophication
isnowperceived
to bea
threat
canbefound alongtheedges of all continents
withtheexception
of
Antarctica.
Nixon[1990]
identifies
theregions ofthecoastlines
ofEurope,
North
andSouth
America,
Africa,
India,south-east
Asia, Australia,
China andJapan
as
allsuffering
fromundesirable
effects
ofcultural
eutrophication.
It isareas
ofreduced
waterexchange,
forexample,
-semienclosed
seas
suchastheBalticandAdriatic,
- fjords
withsillsthatrestrict
waterexchange,
-lagoons,baysandharbors,
which
typically
exhibit
evidence
ofadverse
effects
ofcultural
eutrophication.
Inad-
dition,
however,
somecoastal
areas,
particularly
those
underriverinfluence
mixingwithopenseawatersislimitedarealsoareas
of concern.
A goodexample
of suchan areaisthesouth-east
"corner"of theNorthSea(TheGerman Bight)
wheretheElbe,RhineandWeserRivers entertheNorthSea.Here,signs
of hyp-
oxia and anoxiaalongthe seabottomhavebeenobserved.
Mostof thepublicandpoliticalinterest in eutrophication
istriggered
bytheactual
manifestation
of visibleeffectsof culturaleutrophication in coastalwatersand,
fromthe discussionabove,it is clearthat sucheffectsare foundalongnearlyall
marinecoastlines.
Whilethisconcernwith visiblechangesin thelocalenvironment
isunderstandable,
it maywellturnoutthattherealimportance of marineeutrophi-
cationona globalscaleisitspotentialinfluence
ongeochemical
cycling.
Many authors[e.g.,Smayda,1990; Richardsonand ./Ertebjerg,1993; Billenet
al., ! 99!; Conleyet al. 1993] havepointedoutthatculturaleutrophication alters
therelativeavailabilityof nutrientelements in coastalwaters.In particular,it has
beenemphasized that while culturaleutrophication increasesthe deliveryof N
and P to coastalwaters,it has very little influenceon Si delivery.Not all algal
groupshavea requirement for $i. Therefore, it hasbeensuggested thatchanging
the relativeavailabilityof Si in relationto N andP will discriminateagainstphy-
toplanktonwith a silicbnrequirement(.diatoms)[e.g.,Billenet al., 1991 and ref-
erencestherein].
Indeed, in their 1993 review, Conley et al., concludethat there is evidencefor
changes in the relativeavailabilityof Si and/orchanges in the relativeoccurrence of
differentfunctionalalgalgroupswhichare consistent with thosepredictedunder
conditionsof reduced$i availabilityfrom marinecoastalregionsaroundtheworld.
It should be noted here that, while most eutrophication-related discussionhas
focusedon the total phytoplanktoncommunityor biomass,the relativeoccurrence
of differentfunctionalgroupsin thephytoplankton communityis notpurelyof aca-
demicinterest.Changes in the phytoplankton community's speciescomposition can
haveprofoundeffectson the structureof the restof the foodweb (seesection1.7
andchapters4 and5, thisvolume).In addition,conditions favoringflagellaterather
than diatomdevelopment may increase the probabilityof occurrence of toxic/nox-
iousphytoplanktonblooms[e.g.,Smayda,1990].
The stimulationof phytoplankton growth/biomass by eutrophicationalsohasa po-
tentiallyimportantrole to play in the carboncyclingtakingplacein the world's
oceans.Considerable scientificeffortis presentlybeingdirectedtowardelucidation
of thecarboncyclein the sea.A betterunderstanding of thesecarboncyclingpro-
cessesis clearlyimportantin termsof the discussion concerning globalwarming
(greenhouse effect)predictedon the basisof theanthropogenically inducedglobal
increasein productionof CO2. However,the quantitativerole of the oceansin
globalcarboncyclingis stillnot clear[seefor example,Mantouraet al., 1991].
Nevertheless,
on the basisof the oceans'sizealone,it is intuitivelyobviousthatcar-
boncyclingheremustbe a dominating factorin termsof globalcarboncycling.
The quantitative
globalimpactof a eutrophication inducedincrease
in algalbio-
mass(productivity}
on carbonfixation,sedimentation andburialhasnot yetbeen
established.
However,it isclearthat,by itsverynature,marineeutrophication
at leastpotentially,affectcarboncyclingprocesses occurringin the sea.Thus,while

it is the visibleeffectsof eutrophicationoccurringlocally that attract attentionto
marineeutrophication, it is possiblethat the real importanceof the phenomenon
may befoundat the globallevel.
Eutrophication:
EnrichmentPhase
As indicatedearlier,mostsystemswill respondto eutrophicationby generatinga
greaterbiomassof plant material.Sedimentation of this organicmaterialwill in-
creasefood availabilityfor benthicorganisms and resultin changesin benthosbio-
mass.The increasein organicmaterialin the pelagicand benthicsystemsincreases
the food availabilityfor fish and can result in an increasein fish biomass.Gray
[1992] callsthis the "enrichmentphase"in his generalschemeof eutrophication
effects(Figure1.1) and it is the existence
of thisinitialenrichmentphasethat gives
riseto proposalsaimedat increasingfish biomassthrough eutrophication.Indeed,
someauthors[e.g., Tatara, 1991; Larssonet al., 1985] have arguedthat the in-
creasein fisheriesyield which has beenrecordedin coastalseasin recentcenturies
may be a directresultof anthropogenic eutrophication.Changesrecordedin the
growthrate of herringin the Baltichave also beenattributedto eutrophication
[Hanssonand Rudstam,1990].
When consideringproposalsto increasefisheriesyield through eutrophication,
however,it is importantto rememberthat eutrophicationwill only lead to an in-
creasein fishbiomassif all levelsof thefoodchainleadingup to fishare limitedby
Enrichment
phase
Initial effect
Extreme
effect :."Ma,.•..•o•l• .T'a,•e-...•. :'"'""•'•
Ultimate
effect "::
.'_.•:'t.
':':.•'• "•:.
Figure1.1. Generalscheme
of eutrophication
effects.
ModifiedfromGray
Richardson
andJergensen 9
nutrientor foodavailability.
Thisconcept
is,perhaps,bestillustratedbyusinga
terrestrial
analogyin whichthefisharerepresented
by a fieldof cattle.Thegrass
whichtheyeatwouldthenrepresent plankton.
If growthof thecattleislimitedby
foodavailabilitythenfertilizingthe grass(eutrophication) will relievetheirstarva-
tion and lead to an increasein biomass.However,therewill comea levelof fertili-
zationwheresomeotherfactorthanfoodavailability limitsthebiomass production
of thecattle(water,physiological reproduction rate,etc.).Abovethislevelof fertili-
zation,no benefitin the yield of cattlewill be achieved.
Justasthereis a levelabovewhichincreased fertilizationwill not increase
thebio-
massof cattlein a field of grass,thereis a levelof nutrientavailabilityoverwhich
no "benefit"will resultin the yieldof fisheries.
Thus,it is only ecosystemsin which
the biomassof fish(or the animalstheyeat if theydo not feeddirectlyon phyto-
plankton)is limitedby foodavailabilitythatcanbeenriched to producea greater
fishbiomassvia eutrophication.
1.7.Eutrophication:
Initial and Secondary
Effects
In additionto increasingthe biomassat oneor moretrophiclevels,eutrophication
can lead to a changein speciescomposition.Eutrophicationinducedchangesin
species compositionof benthicorganisms are,perhaps,the bestwell-described (see
chapter8). However,therehasbeenincreasing awareness in recentyearsconcern-
ing the importanceof the sizestructureof the phytoplankton community in con-
trollingenergytransferin the foodweb (see,for example,Cushing[1989];Ki•rboe
[1993];and chapter4 in thisvolume).
Any eutrophication inducedchangein thespecies composition of thephytoplank-
toncommunity whichleadsto a changein sizestructure
of thephytoplankton com-
munitywill potentially
affectenergyflowin theentireecosystem. Thus,eutrophica-
tioncan,at leastin theory,playan importantrolein dictatingwhetherthehigher
trophiclevelsin a givensystemare dominated by marketable fishor by jellyfish
[e.g.,Fisher,1976;GreveandParsons, 1977].Littleisactuallyknownabouttheef-
fectsof eutrophication
on thesizestructureof thephytoplankton community under
various conditions but this is an area that warrants further research.
The increasedplantbiomassresultingfrom eutrophicationwill giveriseto sec-

ondaryeffectson the ecosystem.Sucheffectsincludea reductionin thedepthto
whichlightcanpenetrate in thewatercolumnanda subsequent reductionin the
depthdistribution
of benthicplants(seechapter9).
Eutrophication
andAlgalBlooms
Anothersecondary
effectof eutrophicationcanbe exceptional
"blooms"(rapid
growthandhighbiomassaccumulation of a single
phytoplankton
species)
of toxic
or nuisance
phytoplankton.
Blooms of theprymnesiophyte,Phaeocystis
sp.in
Cells ml -• Days
a b ß
10000
200 ßß
8000 160
6000 120
4000
2OO0 80
•
40 _
ß
'73'7•4
'7•5
'7•6 '7•4'•5'7•6 '7•8
'7:9
'•0 '•2'•3'•4'•5
Days Days
100 c ß 100 d
80 / 80 ßß
60 ß e.•'"'e 60 e/ ß
40 ß 40
20/'""•'// 20
0 , , , • "'• , , , • 0 • • I..... ,"'
'73'74'75'76'77'78'79'80'81'•2 '•3'•4'•5 '74'75'7•6 '7•8
'•9'•0 '82 '83 '•4'•5
Year Year
Figure1.2. Development in the annualoccurrences

of Phaeocystis in the southernNorth Sea
duringthe period1973-198.5.a) Annualaverages of numbersof Phaeocystis cellsml-•,
basedon equallyweightedmonthlyaverages to accountfor irregularsamplingoverthe year
(r=0.61, p<0.0$); b) Numbersof daysperyearwith morethan 100 Phaeocystis cellsml-•
(r =0.73, p <0.01); c) Durationof the Phaeocystis springpeak(periodwith morethan 1000
cellsml-•) (r = 0.89, p <0.01); d) Numbersof daysper yearwith morethan 1000 Phaeocystis
cellsml-• (r = 0.77, p < 0.01). From Cadreand Hegeman[1986.]
southernNorth Seahave,for example,oftenbeenattributedto culturaleutrophica-

tion and there seemslittle doubt that bloom occurrencesof this organismhave
increasedin recentyearsconcomitantly with increasing
culturaleutrophication
of
thisarea(Figure1.2).
It shouldbe noted,however,that the relationshipbetweenculturaleutrophication
and bloomsof toxic/nuisance phytoplanktonis far from completelyunderstood
and culturaleutrophicationis not alwaysimplicatedin bloom formation.On the
basisof the variationobservedin the occurrence
of dinoflagellate
cystsin sedimen-
tologicalsectionstakenfrom a regionon Bornholm,Denmark (Figurel.3), it has
beenarguedthat phytoplanktonbloomswereoccurring140 millionyearsago.The
workersstudyingthesesediments [Noe-Nygaardand Surlyk,1988;
Richardson
andJorgensen 11
12 dinoflagellates
S. pelionense
other dinocysts
10
0 20 40 60 80 100 ø/o
Total organic matter
Figure!.3. Sedimentologicalsectionmadefroma regionon Bornholm, Denmark,showing the

monospecific occurrencesof the dinoflagellate
Sentusidium pelionense
in bedswith census
populations of the bivalve,Neomiodonangulata.The relativeproportionof dinoflage!late
cystsin relationto thetotalorganicmatteris indicated.
It isnotpossible
fromsucha section
to establishcauseand effectbetweenthe dinoflagellate bloomsand massmortalitiesof
Neomiodon. However,therepeated coincidenceof theseeventssuggests
thatthebivalvemor-
talities
mayhavebeencaused
bythedinoflagellate
blooms.
FromNoe-Nygaard
etal.
et al., 1987;Piasecki,
1984,1986]havealsoarguedthat thereis evidence
in this
fossilrecordfor massmortalities
of bivalves
occurring
contemporaneously
with the
largeoccurrences
of dinoflagellates.
In addition,recordsof the earlyEuropean
explorers
of North Americadescribe
veryclearly
theeffectsof eatingshellfish
fromanareawheretoxicphytoplankton
werepresent [e.g.,Hallegraeff,
1993].Shellfishcollectionhasbeenbannedfor
muchof recenthistoryoff thecoastof Alaskabecause of thethreatof toxicalgal
blooms.Thus,toxicphytoplankton blooms havebeendemonstrated to occurin re-
gionsnotsuffering
fromculturaleutrophication.
Scientists
[e.g.,Maestrini
andGranili,1991]andmediaalikewerequickto blame
a 1988bloomof theprymnesiophyte, Cbrysocbromulina
polylepis, in theSkager-
rak/Kattegaton culturaleutrophication.
However,evidence is accumulatingthat
suggests
thattheoccurrence of thebloomcannotbedirectlyrelatedto an increase
in thetotalnutrientavailabilityin 1988 relativeto otherrecentyears.Gray [1992]
refersto evidencethatthebiomass of Cbrysochromulina recordedcouldhavebeen
supported by "normal"stocksof nitrogenin thisarea.
In addition,Heilmannet al. [1994] haveexaminedwater columncharacteristics
relatingto phytoplankton distributionand productivityduringthe bloomwith
thosefoundduringthe sametime periodin the yearsprecedingand following
1988.Theydemonstrated that thereweresignificant differences in the amountof
chlorophyllrecordedin surfacewatersaswell asin therelativeproportionof total
watercolumnchlorophyll foundin a subsurface chlorophyllpeakasopposedto at
thesurfaceduringthedifferentyears.However,thesituationobserved duringthe
Cbrysocbromulina bloomdid not represent an extremewith respectto the amount
of chlorophyllpresentor its relativepositionin the watercolumn.Theseauthors
wereunableto demonstrate a significant
differencein the total water columnpri-
maryproduction occurring in thetimeperiodexaminedin the differentstudyyears
(1987-1993).
Thus,whatwasinteresting aboutthisbloomwasthe fact that a singletoxic species

cameto dominatethe phytoplankton community.Culturaleutrophication may be
implicatedas a causativeagentherethrough,for example,a changein the relative
availabilityof nitrogenand phosphorus [Gran(•liet al., 1993; Edvardsenet al.,
1990]. However,the mechanism(s) of this potentialinteractionbetweenthe Cbry-
sochromulina bloomandculturaleutrophication has(have)not yet beenidentified.
It hasbeenargued[i.e., Smayda,1990] that culturaleutrophication hasincreased
the frequencyof toxic and nuisancebloomsand thisis probablythe case,at least
in someareas.Certainly,in the $etoInland Sea(Japan)there hasbeena demon-
strabledecreasein the frequencyof "red tides"(waterdiscolorationdueto exces-
sivephytoplankton growth)aftercontrolmeasures weretakento reducethe chem-
ical oxygendemand(COD) of the waters discharginginto this sea [Prakash,
1987]. However,it is not yet clearwhetheror not culturaleutrophication
in some
manner"selects"for toxic organisms(througha changein the relativeabundance
of toxic species)or whetherthe apparentincreasein frequencyof nuisance
Richardson
andJergensen 13
toxicphytoplanktonbloomsisa resultof thefactthattheseorganisms

represent
a
subsetof all phytoplankton
andthattherehasbeenan increase in totalphyto-
planktonbiomass. Thus,considerable
work still remainsto be donein orderto
quantifythe relationship
betweennuisance
andtoxicphytoplankton bloomsand
culturaleutrophication.
Eutrophicationand Hypoxia
Perhapsthe mostseriousand certainlymostwidelydiscussedlocaleffectof excess
eutrophication
is the "hypoxia"(oxygenconcentration
lowerthanat air saturation
("normoxia"))thatit cancausein thewatercolumn.Hypoxiaisanothersecondary
effectof the increase in phytoplankton
biomass that resultsfromeutrophication.
The increased plant productionincreases
the deliveryof organicmaterialto the
bottomvia sedimentation andthemicrobialprocesses associatedwiththedecayof
thisorganicmaterialconsume oxygencausinga drawdownin theoxygenconcen-
tration in surroundingwaters. In extremecases,this hypoxia is so severethat
"anoxia" (zerooxygenconcentration) occursin the bottomwaters,hydrogensul-
fideproductionin the sedimentis stronglyenhanced and matsof sulfur-reducing
bacteriamay form uponthe seabottom(seechapters6 and 7).
Differentunitsof oxygenconcentration in seawaterareusedin thechapters of this
book.The concentration unitsof gmo!I-•, ml 1-1,and mg 1-• havethe following
conversionfactors:0.0320 mg [xmo1-1, 0.0224 ml !xmol-•, and 1.428 mg m1-1.
Where oxygenconcentrationis givenas % saturation,this is the % of air satu-
rationat the ambienttemperature andsalinityat atmosphericpressure.
In chapter8,
the physiologically more relevantterm, oxygentension(i.e., oxygenpartial pres-
sure),is usedwith the unit of tort (mm mercury),which is •/760of a standard
atmosphere. At air saturation(21% oxygen),the oxygentensionin seawater is 160
torr. The conversionfactor betweenoxygentensionand concentration varieswith
salinityand temperature.
As the most importantsourcesof oxygento marinewatersoperatein the surface
waters(the air/waterinterfaceand phytoplanktot•photosynthesis),
it followsthat
theregionsin whichhypoxiais mostlikelyto develop arethosewheresurface and
bottomwatersare separatedfrom oneanotherby a steepdensitygradientor "pyc-
nocline".The densityof wateris determinedfromitstemperature andsalinitychar-
acteristics
(seechapter$). In somecases,it is temperatureand,in others,salinity
that dominatesin determining the watercolumn'sdensityprofile.Thus,the pres-
enceof a pycnocline can be identifiedby the presence
of eithera "thermocline"
(steeptemperaturegradient)or a "halocline"(steepsalinitygradient)in thewater
column.
Themostimportantsourcesof oxygento bottomwatersaredown-mixing (usually

wind-driven)
fromthesurfacethroughthe pycnocline
andtheadvection of bottom
watercontaining
oxygenfrom surrounding seas.Thus,naturalvariations
in water
exchangeprocesses
andweatherconditions (whichcontrolwind-mixing of
andbottomwater)playan importantrolein determining

the development
andin-
tensityof hypoxiceventsin a givenregion.
Whenoxygenconsumption exceeds oxygendeliveryto the bottomwater,hypoxia
will result.Againhere,however,it isimportantto emphasize thathypoxiacanresult
fromnaturaleutrophication processes aswellasculturaleutrophication.
Gray[1992]
citesan exampleof hydrogen sulfide(H2S)production(whichonlytakesplaceunder
anoxicconditions) occurring naturallyunderthethermocline in upwellingareasoff
Peru.What is interesting aboutculturaleutrophication in this respectis that it is
causing an increase
in theintensityandthedistribution
of hypoxiain coastalwaters.
Biological systems are, of course,dependent
on oxygen.Thus,evensmallchanges
in oxygenavailabilitycangiveriseto physiological
changes in the organismsfound
in thesystem(seechapter8). The firstresponseto hypoxiathat canbe observed at
the populationlevelis a behavioralone.Many fish,for example,will respondby
fleeingan area of reducedoxygenconcentration. This often leadsto increased
catches especiallyfor fishermenusinggearsplacedat a fixed geographic position
(the fact that greaternumbersof fish are movinggreaterdistances increases
the
probabilityof themmeetinga net).Thus,slightlyreducedoxygenavailabilitycan
givea boomin the localfishery.
Hypoxiacan alsoincreasecatchesof lessmobileorganisms. The Norway lobster
(Nephrops norvegicus),for example,livesin burrowsin the seabedandis fishedin
the Kattegatand Skagerrakby bottomtrawling.This trawling,however,only
catchesindividuals
that are out or on their way out of their burrows.Thoseindi-
vidualssafelytuckedawayin theirunderground homeswill not be caught.The
oxygenavailabilityin theseburrows,however,is considerably lowerthat in the
free-moving
watersabovetheseabottom.Duringperiodsof low oxygenavailabi-
lity in thebottomwaters,the oxygenconditions
in theburrowscanbecomeintoler-
ableandthe lobstersareforcedup to the waterscoveringthe seabottomin order
to survive
(seechapter
8). Thismakesthemmorevulnerable
to trawlingandcatches
of Norwaylobstershowa clearincrease
in response
to hypoxia(Figure1.4).
Asoxygen becomeslessavailable
in bottomwaters,thelesstolerantspecies begin
to die- thuschanging
thestructure of thebottomfaunalcommunity (andincreas-
ingtheorganicmaterialavailablefor microbialdegradation).
In severecases,bot-
tomwatersmaybecome anoxiccausing die-offof mostorganismsandthe forma-
tionofmatsofsulfurbacteriaasmentioned above.Suchconditionsare,clearly,
not
conducive
to a productive
fishery.
In manytemperateregions,
stratification
of the watercolumnis a seasonalphe-
nomenon.Whenwintercomes andstratification
isweakened or brokendown,oxy-
genis mixedintobottomwatersandhypoxia/anoxia relieved.
Recolonizationby
oxygen-requiring
organismsof thebottomcannowproceedbut,if hypoxia/anoxia
reoccurs
duringthefollowingsummer(s), therecolonizationprocess
will beinter-
rupted.
Aslongasthispatternof annual(ornearlyannual)hypoxia eventspersists,
thebenthic
faunacommunity willnotbeableto reestablish itsprehypoxiaspecies
andage
Catches, kg h -1
32
30
28
26
24
22
20
18
14
10
0 i
20 30 40 50 60 70 80 90 100 110
Oxygen saturation, %
Figure1.4. Catches(kg trawl h-1) of the Norwegianlobster(Nephropsnorvegicus)

as a
functionof oxygenconcentrationin bottomwaters.From Bagge[1977].
Eutrophication
of a Marine CoastalEcosystem:
A DanishCaseStudy
This book dealswith the differentmodesof deliveryof nutrientsto a marine
ecosystem (chapters2 and 3) andtheeffectsof eutrophication on thevarioustro-
phiclevelsoccurring withintheecosystem (chapters4-12). Theprinciples discussed
areapplicable to mosttemperate coastalmarinesystems. However,wehavechosen
to illustratemanyof theconcepts addressed with examples fromtheKattegatand
surrounding baysandfjords(Figure1.5).Thispresentation formhasbeenchosen
in orderto facilitatecomparison of the relativeimportance of variousprocessesin
nutrientturnoverin the systemandto emphasize the importance of obtaining
an
overalldescription of nutrientturnover in anecosystem in orderto assess
theimpli-
cationsof
16
1. Eutrophication:
Definition,Histoo andEffects
Osk•
•j• 0 50100
150
20 KlJomelers
5In,,
anger t •t 30m
• • S•eden
!
• Denmark)
• . • •'
•--•:'• Germany
•
"• H•a,• • r•7 ' Pola
Figure 1.5. Barhxmerr
5 of the transition area betweenthe Noah Sea and the Baltic Sea.
(Map designand research:
JonathanWvss,TopazDesignandThorkildAarup.}
The Kattegatrepresents the transitionareaseparatingthe Balticfrom the $kagerrak

and North Sea.From Figure1.5, it can be seenthat thisis a relativelyshallowwater
body. In addition, there are a number of bays and inlets along the Danish and
Swedish coasts. Water volume and circulation in these inlets is reduced in relation
to that occurringin the moreopenregionsof the Kattegat.Thus, nutrientsentering
these inlets wfil potenuallvinfluencethe local ecosystemdifferentlythan those
enteringthe moreopenregionsof the Kattegat(seechapters9 and 10}.
The netcirculationpatternin theKattegatis onein whichbottomwaterof relative-
ly highsalinitw{enteringfrom the Skagerrak in the north}flowstowardthe Baltic
and surfacewater flowsfrom the Baltictoward the North Sea{seechapter3).
Skagerrak
North
Sea
56øN
Figure1.6. Distributionof hypoxia(< 3 mg 02 !-1) in theKattegatin 1988[HELCOM,

1990.]
surfaceoutflow is driven by fresh-waterinput to the Baltic.Thus,the surface

watersin theKattegatareconsiderablylesssalinethanthebottomwaters.
Hypoxiain theKattegat'sbottomwatersbeganto occurregularly overlargeareas
duringthe 1980sandis nowan annually occurringphenomenon isthisregion-
althoughtheintensityandgeographic distribution
of thishypoxia
variesfromyear
toyeardepending onwaterexchange conditions.
Themostextensive hypoxiaevent
recordedto dateoccurredin 1988 (Figure1.6).Thisrecurring
hypoxiahasaffected
thelocalfisheryandhascaused publicoutcry.In theaftermathof therealization
thatculturaleutrophication
isthemostlikelycause of theobserved
changesin the
marineecosystem of theKattegat,manyquestions arebeingasked concerningthe
nutrient
sources whicharemostresponsible fortheobservedeutrophication
effects
andtherelativevalueof differentproposed
remedialactions.
It istheresponsibility
of thescientific
communitytodevelop
thenecessaryexpertise
to answer suchquestions.Thisbookrepresents
ourattemptto collate
andsynthe-
sizetheexisting
expertisewithrespect
to howcoastal
marine
ecosystems respond
to
eutrophication.
It isourhopethatthissynthesis
willhelpintheanswering
ofsome
ofthese
questionsbutalsoin generally
drawing
theworks ofthescientific
andthe
administrative
communities
closerto one anotherby providingboth a reviewof
"thestateof theart"withrespect
tomarinecoastal
eutrophication
andbystimulat-
ingideasforfurtherdirections
for
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Cad&, G. C., andJ. Hegeman,Seasonal andannualvariationin ?haeocystis
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Howarth,R.W., Nutrientlimitationof netprimaryproduction in marineecosystems,
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Vollenweider,
R. A., Advances in definingcriticalloadinglevelsfor phosphorus
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Elsevier,Amsterdam,
2
AtmosphericProcesses
Wi!lem A.H. Asman and S•ren E. Larsen
Introduction
Nitrogenand phosphorus can be limitingfactorsfor algalgrowthin the marine

environment[Dugdale,1967; Rytherand Dunstan,1971]. The atmospheric phos-
phorus inputto estuarine
andcoastalwatersisnegligible compared to thecontribu-
tion from other sources.'Atmospheric
nitr.ogeninputis, however,potentiallysigni-
ficant and contributesup to 20-50% of the externalnitrogenloadingof these
waters[Paerland Fogel,1994]. For thesereasons,onlyatmospheric nitrogeninput
is discussed
in thischapter.
The mostimportantgroupsof atmospheric
nitrogencompounds
that act as nutri-
ents are:
- The NHx group:gaseous

ammonia(NH3), andammoniumin particles
(NH4*
aerosol).
- TheNOygroup:thegaseous
compounds
dinitrogen
pentoxide
(N2Os),HNO4
and nitric oxide (NO), nitrogendioxide (NO2), nitric acid (HNO3), nitrous
acid(HNO2), peroxyacetylnitrate(PAN) nitratein particles(NO3- aerosol)
and nitrate radicals (NO3).
- Organicnitrogencompounds.The atmosphericconcentrations
of thesecom-
poundsareverylow andtheirsourcesarenotwellknown.Forthesereasons
organicnitrogen
compoundsarenottreatedin thischapter,
apartfromPAN
that is a relativelywell-knownreactionproduct.
The combinationof NH3 and NH4* is calledNHx; that of NO andNO2 is called
NOx.The dominant NOy compounds ar seaareNO2, HNO3, PAN,andNO3-
aerosol.
Individual
aerosol particlesconsistof numerous
compounds.
Theparticles
candiffermarkedlyin size(0.1-5 txm)andtheirchemical
compositions
area func-
tion of their size.

Coastal and Estuarine Studies, Volume 52, Pages21-50
Union
22 2. AtmosphericProcesses
The atmospheric nitrogeninputis causedby two processes:wet deposition,which

is the removalfromthe atmosphere by precipitationand by dry deposition,which
is the removalby atmosphericturbulence at the seaor landsurface.Thereare two
importantdifferences betweenwet and dry deposition.Removalby wet deposi-
tion takesplaceoverthewholeatmospheric layer,wheresnowandraindropsare
found.Removalby dry deposition occursonly verynearthe seaor landsurface.
Wet deposition occursonlywhenprecipitation occurs,whichin WesternEurope
is approximately 5-10% of the time.Dry depositionis constantlyoccurring,even
when it rains.
Atmospheric depositionto theseais noteasilymeasured. Althoughconcentrations

in precipitation
can be measuredat sea,it is not easyto determinethe amountof
precipitationtakingplaceover the sea.This is not easybecausethe collectioneffi-
ciencyisheavilyinfluenced bythedisturbed windfieldaroundtheshipor theplat-
form.Dry deposition is evenmoredifficultto measure andit is notpossibleto do
soroutinely. Forthesereasons, it is difficultto estimate
the atmospheric nitrogen
inputto theseafrommeasurements and,therefore, atmospheric transportmodels
areoftenusedto calculate theinput[vanJaarsveld, 1992].In atmospherictrans-
portmodels, it is necessary
to describeall processesinfluencingthe concentration
of all involvedcomponents in anairparcelonitswayto wheredeposition occurs.
Theses processes include:
emissions,transport by thewind,mixing,reactionand
deposition. Deposition processesshouldnot onlybeknownfor seaareasbut also
for landareasbecause thedepositionto landareasdetermines howmuchis left for
deposition to thesea.Thechange in mass of a compound in anair parcelduring
transport canbedescribed bythefollowing simplifieddifferential
equation:
ratein changeof mass= emission
rate+ formationratebyreaction
- removalratebyreaction- wetdepositionrate- drydeposition
rate
+ rateofchange
dueto otherexchange
mechanisms (1)
Theformatiofiandremoval rateof onecompound dependsontheconcentration of
othercompounds and,in thisway,thedifferential
equationsof allcompounds are
intertwined.
Thiscomplicates theintegration
of thedifferential
equationsin time/
space,whichis neededto findtheconcentration/deposition
at sea.Theannualde-
position
in a seaareaiscomputed byfollowingtheair parcelson theirwayto the
areaduringoneyearandcalculating theconcentration
anddeposition with(1).The
mainsources
of thenitrogeninputto the estuaries
andthe coastalareasare land-
basedanda largefraction
of thisinputdoesnotoriginate
fromsources
in coastal
areasbutratherfromsources morethana fewhundred kilometers
away.Forthis
reason,it isnecessary
to consider
a ratherlargeareain modelcalculations.
Thischapter discusses
thevariousatmospheric
processes thatarepartof atmo-
spherictransport modelswiththeemphasisonthedeposition processes.
Thede-
tailedsetup of such
models isnotdiscussed.
However, at theendof thispaperan
example of theresults
of anatmospheric
transport
model,'ACDEP',[Asman et al.
1994a]ispresented for theKattegat.
Estimates
for othermarineregions arealso
Asman
andLarsen 23
2.2. Emissions
Ammonia
Thepredominant
atmospheric
NH3 sources
arelivestock
wastes,
withsomewhat
smallercontributions
fromfertilizer
application
andproduction
[Buijsman
et al.,
1987].In Figure
2.1,thegeographicaldistribution
of theNH3emission
densityin
Europeis presented.The totalemission in Europe(excluding
theformerUSSR)in
1989was4534 ktonneN yr-•. Cattle,pigsandtheapplication of fertilizers
arethe
mostimportant sourcesandcontribute,53, 18 and17% of theNH3emission, re-
spectively.
Theemission density
isrelatively
highinDenmark, though lowerthanin
TheNetherlands andBelgium.Since1950,European NH3 emissionshavedoubled
[Asman et al., 1988].Theseasonal variation in theNH3 emissionrateis poorly
known.It is guessed thattherateishighest in spring
andsummer [Asman, 1992].
6O
55
5O
45
35
.• ........
ß
30
ß . .............
...... . .... * ......

..........
25 .'-"".".•"-.'".'..'*- ".: .'"--'2 2-' •"--'*- ßß.
'2--: :•---- ....
2O
15
.ii;'::•!::•'i:::. '":: /•0•, oboveS.O0
10. i' ::::::::::::::::::::: ';i:i' 2.00 4.00
:.':::"'iii!ii!:
:::::
i ::i: :::•1.O0
2.00 O.õ0 1.00
.•.::•0.2S0.S0
,•..-•.,
20 25
.... • ............
30 35 40 45 50 55 60 65 70
0.o 75 80
IE-coordinotem
Figure2.1. Emission
densityof NH3 in Europe(tonneN km-2yr-•) without
24 2 AtmosphericProcesses
II• above 6.00

-.•
ß 5.00- 6.00
6375 •1 4.00- 5.00
•J •.oo - 4.00
•.:• 2.00- 3.00
6345 ::• 1.00 - 2.00
ß .
.:• 0.00 - 1.00
6315-'
...
6285
6255 :{{•::'•:...:{•:••)•L::: .......... ": ........

::::::::::::::::::::::::::
....
•'6225
:::::::::::::::::::::::::::::
6195-
6165
6135
6105
6075-
Figure2.2. Emission
density
of NH3 in Denmark(tonneN km-2yr-]).
The NH3 emissionrate is generallyhigherduringdaytimethan duringnighttime,

whichis the resultof a highertemperatureandwind speedduringdaytimeand the
fact that manureis mainlyspreadduringdaytime.NI-I4+ aerosolis not emittedto
the air. Thismeansthat all atmospheric
NI-I4+originatesfromgaseous
NH3.
The NH3 emissionin Denmarkis 109 ktonneN yr-• [Asmanet al., 1993]. Cattle
and pigsarethe mostimportantsources andcontribute46 and 37%, respectively,
to the total NH3 emissions.
Figure2.2 showsthe geographical distributionof the
NH3 emissiondensityin Denmark.The NH3 emissiondensityvarieson a regional
bas•s,both on Europeanas well as Danishscales.The seamay also act as a minor
sourceof NH3 emission[Quinnet al., 1988a,b,and 1990; Asmanet al.,
Asman and Larsen 25
NitrogenOxides
Anthropogenic emissionof NOx is dominatedby the contributionof NO. Most of
theNOx emissionis generatedduringthe combustion of fossilfuelsand originates
mainly from N2 and 02 presentin the air neededfor the combustion. The total
emission of NOx in Europe,excludingthe formerUSSR,is 5094 ktonneN yr-], of
which 2427 is from stationarysourcesand 2667 from mobilesources[Pacynaet
al., 1991]. In WesternEuropeancountries,the contributionof mobilesources(road
traffic,internalnavigation)is about60% of the total. For EasternEuropeancoun-
triesthis was in 1991 about 40%, but it is certainlyincreasing. The geographical
distributionof the NOx emissiondensityin Europeis shownin Figure2.3. The
NOx emissiondensityis highestin the mostdenselypopulatedareasof Europeand
is, for that reason,somewhatlower in Denmark.The EuropeanNOx emissionhas
increasedby a factor 3 since1950 [Pacynaet al., 1991]. The NOx emissionrate is
6O
55
:::::::::::::::::::::::::::::::::::::
5O
45 =================================
40-
35
30
..
25
20-
15- :::i . :"/•J), above 6.00

.... ,.oo- .0o
10
:::::::::::::::::::::::::::::::::
.//' • :_• 1.00- 2.00
::::::::::::::::::::::::: 0.25-0.50
:. :::::: c:" ::• 000 - 025
20 25 30 35 40
,7i.'
.'•..
i 1....1..1
45
,,1ß•ßßi....i.,,...i
50
....,i,,.
ß, 55 60 65 70 75 80
IE-coordinotes
Figure
2.3.Emission
density
of NOxin Europe
(tonne
N km-2
26 2. Atmospheric
Processes
6405 -
6375
6345
6315
6285
6255
""
E 6225 -
6195
6165
6135
6105-
6075
Figure
2.4.Emissions
ofNOxfromlargepointsources
inDenmark.
Theradius
of thecircle
indicates
therelativesourcestrength.
highest
during
daytime
during
rushhoursandduring thewinterheating
season.
All
otherNOycompoundsarenotemitted
totheair,butarereaction
products
ofNOx.
The NOx emission
in Denmarkis 89 ktonneN yr•. The mostimportantsources
arelargepointsources(powerplantsetc.:44%) androadtraffic(34%) [Asmanet
al., 1993].Thegeographical
distribution
of theemissions
isdividedintolargepoint
sources (mainlypowerplants;Figure2.4) andareasources(Figure2.5).
NOx emissions
in EuropeareaboutaslargeasNH3 emissions. The uncertainty
in
bothnitrogen
emissions
isat least30-40%. Theemission
of othercompounds
Asman
andLarsen 2:7
64-05 -
.....
!"...'..'"f:: • o•ov•
•.oo
6575- -::..
:'-•i :-"
:..•' :• s.oo- •.oo
i•:!•ii!!!::.ii:3.• :E'• 4.00- 5.00
.!/..iii::::iiiii
..... .[.:. .. ß .'_• •.oo- •.oo
6545 :/::i::ii!!!ii..
:ii :i:•.i '..'•
/:::':::•:i!:•i:.-"7::Z: :'
" i• 2.00
•.oo -
- 3.00
2.oo
6515
\ '
6285 .:' :'!
6255
, : ..
'•' 6225
i'•:
'"i::.::i:::;iii•-'.'iiiiz•:
!:-.!•::iiiiii
....
-: '....
•;' .:.. :' :':':::•
::.
::
6195
6165
6135
6105
:':i!i!!!',',',':!ii':!',11....::::,:,,. ':.:,:.:::i
6075
•o• ,D..M.U-774 .........
ß - , .....
435 465
UTl•-c•rdin•t• (kin)
Figure2.5. Emission
densityof NOx fromareasources
in Denmark(tonneN km-2yr-•).
playa role in the atmospheric chemistryof nitrogencompounds like S02 andhydro-

carbons,is not discussedhere becausetheir influenceis indirect.In atmospheric
transportmodels,griddedemissiondata are used.In suchmodels,it is assumed
that theemissionis homogeneously distributedwithineachgridelement.In Europe
andNorth America,gridsizesof theorderof 100-150 km areused.The useof such
sizescancauseproblemsin coastalareas,wheretheemission oftenonlyoccurson
the land area within the grid element.The dry depositionat seawill in suchcases
be overestimated in the model becausethe air concentration
is too highdue to the
toohighemission
densityat sea.To avoidthisprobleman emission
gridsizeof 15
km was usedin the ACDEP modelto calculatethe depositionto the
2.3. Reactions
Compounds are chemically convertedthroughatmospheric reactions.Each com-

poundhasits ownspecific physical andchemical characteristics,
andit is therefore
removedfrom the atmosphere at a differentrate than that of othercompounds.
With respectto deposition,
reactionsareveryimportant.For example,NH3 is re-
movedrelativelyquicklyfrom theatmosphere by dry deposition,ascomparedto its
reactionproduct,NH4* aerosol.This, combinedwith the relativelyfast reaction
fromNH3 to NH4* aerosol, resultsin a transportof NHx overlongerdistances than
would be the case if the reaction were slow.
UnderWesternEuropean conditions, mostNH3 will reactwith acid aerosol,e.g.

aerosolcontaining
sulphuric acid(H2SO4). Althoughthisis a fastreactionin the lab-
oratory[Robbinsand Cadle, 1958; Baldwinand Golden,1979; Huntzickeret al.,
1980; McMurry et al., 1983], it is foundthat the overallconversion
rate of NH3 in
the atmosphere
is muchlower,namelyabout30% h-1 [Erismanet al., 1988; Asman
andvanJaarsveld,1992].Thiscannotyetbeexplained. However,it maybethatall
acidaerosol
neartheearth'ssurface hasreactedwith NH3 gndthatNH3, therefore,
hasto betransported
higher
upin theatmosphere
beforeit canreact.Thistransport
takestimeandthiscouldbeoneof thereasons
whytheconversion ratefromNH3 to
NI-I4*aerosol
in theatmosphere
is notashighasin the laboratory.Onceboundto
SO42- in particles
asNH4*,NH3 isnotreleased
again.A minorpartof NH3 reacts
withHNO3andHC1to formNH4NO3andNH4Cl-containing particles.
Reactions:
NH3 + HNO3 •--- NH4NO3 (2)
NH3 + HCI •- NH4C1 (3)
Thesereactions
canproceedin bothways,whichmeans thatNH3 (andHNO3 and
HC1)notonlycanbeconsumed, butcanbeproduced [Stelsonet al., 1979;$telson
andSeinfeld,
1982a-c;PioandHarrison,1987;Allenet al., 1989;Ottleyet al.,
1992;HarrisonandKitto,1992;Mozurkewich,1993].In theUSA,thesereactions
aremoreimportantthanin WesternEurope,because
theratioof NOxto SO2emis-
sionislarger.Over thesea,the NH3 concentration
is ratherlow and for that reason
thereisoftennotenough
NH3toformNH4NO3 andNH4Cl-containing
particles.
Theequilibriumconstants
ofthese
reactions
aretemperature
andrelative
humidity-
dependent.
Thereactions ofNOyaremuchmorecomplex becausemanyothercompounds are
involved(Figure2.6).Someofthereactions
areinfluencedbysunlight
andveryre-
activecompounds, radicals,
areformed.Because theyaresoreactive,
theyoccur
onlyin verylowconcentrations,buttheirrolein atmosphericchemistry
during
daylighthoursisveryimportant.Examplesof theseradicals
areRO2,RCHOand
RO(O)2,allorganic forms,andtheinorganic
onesOH andNO3(these radicalsare
notinion-form; R denotes
a saturated
hydrocarbon chain;NO3denotesNO3radi-
cals).
In addition,
otherreactions
arealsodirectly
influenced
bysunlight,
whichis
indicatedin Figure2.6by'hv'.NOxis emitted mainlyto theatmospherein the
formofNO. NO israpidly oxidizedtoNO2byreaction withozone(03)and
Asmanand Larsen 29
Ground
Figure2.6. Atmospheric
reactions
of NOy.
At the sametime, HNO2 is also formed. NO2 can reactto PAN, HNO3, NO3 radi-
cals,and N2Os. N2Os is a gaseouscompoundthat is stableonly at night,as it is
photolyzed
by sunlight.
HNO3 or N2Oscanreactfurtherto nitrate(NO3-)-contain-
ingaerosols
or be takenup by cloud-and raindrops,whichalsoleadsto NO3- for-
mation.The atmosphericchemistryusedin the ACDEPmodelis described by Gery
et al. [1989] and Hertel et al. [1993].
The factthat a compoundhasa highconcentration doesnot implythat the com-
poundis an importantcontributorto deposition,for thiswill not onlydependon
theconcentration,but alsoon the efficiencyof the removalmechanism.In fact,the
oppositecan occur:namelythat theconcentrations of somecompounds arehigh
becausetheyarenot removedat a highrate.
2.4.MeteorologicalAspects
Amountof Precipitation
Theatmospheric removalmechanismthatcontributes mostto thenitrogen deposi-
tion in marineareasis wet deposition.
The amountof wet deposition generally
increaseswith theamountof precipitation.
It is therefore important to knowthe
amount of precipitation
at sea.Theamountof precipitation isverydifficulttomea-
sureonshipsandplatforms because
thecollection efficiencyoftheraingauge isnot
verywellknownastheair flow aroundtheshipdisturbs thecollection.It isgener-
allyassumed thattheamountof precipitation at seais lowerthanin coastal re-
gions.Meteorological weatherprediction
models givea meanannualamount of
precipitationfor theNorthSeaof 550 mm[KrellandRoeckner, 1988;Petersen
al., 1988].Precipitation
measurements
onoil andgasplatforms
in theNorthSea
areof theorderof 400mmyr-• [Rendell
etal., 1993].Theseasonal
variationin the
rainfallat seacan be differentfrom that measuredon land. This is causedby the
factthatthetemperatureoftheseawaterisdifferent
fromthetemperature onland.
Duringthesummer, thetemperature onlandnearthesurface canbecome rather
highcompared to theairaloft,whichcanleadto convective
precipitationonland.
Duringautumn, thetemperature of seawaterisoftenhigherthantheair tempera-
ture,leading
to moreconvective
precipitation
at seain autumn.
The amountof precipitation
overtheKattegat
wasdetermined
fromdataat 21
coastalsitesin DenmarkandSwedenandon severalislands[Allerupet al., 1992].
Thisamountwascompared with datafrom20 stations on theJutlandpeninsula.
Overthe four-yearperiod1988-1991 precipitation on the Kattegatwas 84% of
that foundonJutland.Theratio betweenthemonthlyamountsof precipitation on
JutlandandtheKattegatvariesfrom0.6 to 1.0. Thehighestratio seems
to occurin
the late autumnand earlywinter.Thisconfirmsthe trenddiscussed above.Model
calculations[Asmanet al., 1994a] showedthat it wasimpossibleto reproducethe
wet deposition of nitrogencompounds measuredon the islandof Anholt in the
Kattegatwith the amountof precipitationmeasuredon Jutland.This illustrates,
thatit isimportantto usethecorrectamountof precipitation
for seaareasin atmo-
spherictransportmodelsandnot, asis oftendone,valuesfrom land areas.
Turbulence
andTransportin theAtmosphere
The lowersurfaceroughness heightfor momentum at seacausesa higherwind
speed, butlessturbulence at seathanonland[Garratt,1990;Gryning,1993].The
reduced turbulence will for manycompounds leadto lowerdry deposition veloci-
tiesat seathanonland(seesection on drydeposition).
Theatmosphere at seatends
oftento bestablein winterandspringandunstable in summerandautumn.Thisis
caused by differences
in temperature betweenair andsea.Understableconditions
thewindspeed isreduced, whichleadsto reduced drydeposition
velocities,where-
astheyareincreased
underunstableconditions.
Transport
intheatmosphere
isusuallydescribed
bywindfields,whicharebasedon
meteorological
observations.In Eulerianmodels thisinformation is useddirectly.
In Lagrangian
modelsthisinformation isusedtocalculate trajectories,
i.e.thepath
anairparcel
travels
asa functionoftimeunder influenceofthevarying windfields.
Usually,
back-trajectories
areusedin calculations, i.e.thetrajectto a point,a so-
called
receptor
point,isfollowed.Winddirection andwindspeed arefunctions of
height.
Thismeansthatairatground levelhasanorigindifferent fromairaloft.
Atmospheric
turbulence
causes
airto beexchangedbetween
different
heights.
In
atmospheric
transport
models
thisexchange
is oftenmodeled
byusing K-theory
[Stull,1988]:
8c •(Kz•C)
a• = a-• •zz
Asmanand Larsen 31
Here,the changein concentration

is dependent
on changing
concentrations
be-
tweenverticallayersin the model.
Solubilityof Gasesin Water

Solubility
in wateris a veryimportantpropertyof gases.
It determines to a largeex-
tenttherateat whichgases areremovedby dryandwetdeposition. Thesolubility
isexpressedin theHenry'slaw coefficient
(Ha expressedin mol 1-• atto-•) whichfor
species
A is definedhereas
[A.H20]
= (5)
PA
where[A.H20] is theconcentration of the dissolved
gasin water(tool1q) andPais
thepressure of the gasin air (atm).The largera Henry'slaw coefficient,the more
solublethe gasis. It shouldbe mentionedhere that thereexist differentdefinitions
of Henry'slaw coefficient,whichcan beconfusing.
For compounds
that dissociate,
like acidsand bases,evenmoreof thecompound
can dissolve in water. This means that the amount dissolved at a certain concentra-
tion in air is alsoa functionof the pH of the water.The pH of cloudandprecipita-
tion water is usuallybetween4 and 5, whereasthe pH of seawateris around8.
The Henry'slaw coefficients for nitrogencompounds are shownin Tables2.1 and
2.2. Theyshowthat NO, NO2 and PAN are poorlysolublein water.NO andNO2
TABLE 2.1. Henry'slaw coefficients
H at 25øC (tool1-1atm-•) andtheirtemperature
coef-
ficients,-AH/R (øK).
Compound H -AH/R Reference

NH3 5.60x10 *• 4092 DasguptaandDong[1986]
NO 1.93x10 -3 1479 Schwartzand White [1981]
NO,_ 1.20x10 -2 1965 Schwartzand White [1981]
HNO2 4.90x 10*1 4781 Schwartzand White [1981]
HNO3 2.10x10 *s 8706 Schwartzand White [1981]
NO3 radical verylarge
N,.Os* verylarge
PAN 2.80 6513 Kameset al. [1991]
* Reactswith water to HNO3 (seeHNO3).
TABLE 2.2. Dissociation:

constantsK at 25øC and theirtemperature
coefficients,
-AH/R
(øK).Concentrationsare in tool 1-•.
Compound K -A H/R Reference

NH3 * 1.78x10 -s - 429 Batesand Pinching[1950]
HNO2 5.01x10 -4 -1258 Schwartzand White [1981]
HNO3 ** 1.55x10 *• 0 Schwartzand White [1981]
* NH3.H20 5-* NH4* + OH-
* * temperature
dependence
included
in Henry'slawcoefficient
(Table
32 2. Atmospheric
Processes
reactin water,butnotveryfastcompared
to thedissociation
reaction
mentioned
before,toformNO2-(nitrite)
andNO3-(nitrate)
[Schwartz
andWhite,1981].PAN
ishydrolyzed
inwater,
whichproceeds
ata reasonable
speed [Kames
etal.,1991].
Thereaction
products
areNO2-andNO3-.Theother
gasesaresoluble
inwater.
Thetemperature
dependence
ofHenry's
lawcoefficient
isdescribed
by
H(T)
=H(298.25)exp
• T 298.i'5
...... (6)
whereT isthetemperature
in K. Thisequation
is alsovalidfor thedissociation
constants,
butthenoneshouldreadK instead of H. Forseawater,it isnecessaryto
takeintoaccountthattheionicstrength
is solarge,thatit influencesHenry'slaw
coefficients
andthedissociation
constants
[Millero and Schreiber,1982].
Wet Deposition
Wet depositionrefersbothto theprocessof wet deposition
andto theamountde-
positedby thisprocess.Compounds canbe removedby'differentwet deposition
processes.
Thereexistremovalprocesses within clouds(in-cloudscavenging)
and
removalprocesses below-cloud base(below-cloud scavenging),
wherecompounds
areremoved
by fallingraindropsandsnowflakes.
The atmospherecontains aerosolparticles
whichconsistpartlyof hygroscopicsub-
stances.When the relativehumidityis more than 40%, aerosolscontain at least
30% water by weight.When the relativehumidityincreases, more water vapor
condensesontothe aerosols and clouddropletsare formed.Most of the NH4* and
NO3- is foundin thoseaerosols,which can act as condensationnuclei.Most cloud
dropletswill evaporateagainand it is estimatedthat the cycle,aerosol-• cloud
droplet-• aerosol,is repeatedat leastten timesbeforethe aerosolis removedby
precipitationformedfromclouddroplets.The process of removalof aerosolsdue
to theirroleas condensationnucleiis the mostimportantprocessfor in-cloudre-
movalof particles.Removalof aerosolsby below-cloudscavenging is not very
efficient.
The flux of gasesintodropletscanbe described

by the followingequation[Peters,
1983]:
------(%- Cw*) (7)

where
Fg = fluxintothedrop(molm-2s-•)
fg = ventilation
coefficient
(dimensionless),
whichistheratioof uptakeof a drop
movingrelativeto theair anda non-moving drop.The ventilationcoefficient
isneeded to describe
theeffectof enhanced
uptakedueto internalcirculation
in thedrop,whichincreases withfallspeedandthereforealsowith dropsize
(thefall speedincreases
with drop
AsmanandLarsen 33
Dg= diffusivity
of thegas(m2s-1)
r = radiusof the drop (m)
Cg= gasphase
concentration
of thegas(molm-3)
Cw•'=
thetheoretical
gasphaseconcentration,
whichwouldbein equilibrium
with
theconcentration
of dissolved
gasat thegasdropletinterface
(molm-3).
Thevalueof Cw*isfoundfromtheconcentration
intheliquidphase:
Cw
cw* = (8)
HRT
c•,= concentration
of thedissolved
gasin theliquidphase(toolm-3)
H = Henry'slaw coefficient(mol 1-• arm-•)
R = gasconstant(atto1-• mol-• K-•)
T = temperature(K).
The flux rate will thusdependon theconcentration differencebetweengases and

liquidphases. Sometimef611owing exposure
of a dropto gasconcentrations,
equi-
libriumwill bereachedbetweenthephases. Forthesamegas,it will takemoretime
to reachequilibriumfor largedrops(rain drops,radius100-2500 •m) than for
smalldrops (cloud droplets,radiusabout 10 Ixm). The size and the lifetimeof
clouddropsis suchthat theywill reachequilibrium with thesurrounding(intersti-
tial) air within a few seconds.For moderatelysolublegases,the concentration
in
the interstitial air will be almost the same as the concentration in the air before the
cloud was formed becauseonly a small fractionof the gas dissolves into the
droplets.The concentrationbelow the cloud will usuallynot be much different
fromthat in thecloud,i.e. thereexistsnearequilibriumbetweenraindropsformed
out of cloud dropletsand the surroundingair belowthe cloud.For that reason,
theywill not absorbmuchgasbelowthe cloud.
In the caseof highlysolublegases,the largestfractionof the gaswill dissolveinto
the dropletsand the concentrationin the interstitialair will becomevery low com-
paredto the situationbeforecloudformation.This meansthat thesedropswill be
far fromequilibriumwith the air belowthecloud.The maximumuptakerateof the
raindrops is muchlowerthanof theclouddropletsandtheirlifetimeismuchshorter.
Forthesereasons, thedropswill notgetsaturated with thegasbelowcloudbaseand
theyare,therefore,not saturatedwhentheyarecollected at theground.Thiswill be
the situationfor NH3, HNO3, N2Os [Asman,1994]. This situationcan causearti-
facts,because gascanbetakenup in therainin thesampleraftercollection.
Thecloudbaseis oftena few hundredmetershigh,whereascloudsusuallyaremuch
thicker.Therefore,the volumeexposed to below-cloudscavenging
isnormallysmall
compared to the volumeexposed to in-cloudscavengingand,asa result,sois the
relativecontributionof below-cloud
scavenging to theconcentration
in precipitation.
WhenNH3 isabsorbed bycloudandraindrops,whichareusuallyacidic,it willreact
with H* to formNH4*. ThisNH4* cannotbedistinguished
fromtheNH4* originating
fromNH4*-containing aerosol.The sameholdsfor NO3- in precipitation, which
originatesfromthe scavenging
of HNO3, N2OsandNO3--containing aerosol.It
alsonearlyimpossible
to findthecontribution
of below-cloud andin-cloudscaveng-
ingfrommeasurements.Onlymodelscanproduce thiskindof information.
Wet deposition isinfluenced
bytheair flowin andaroundtheclouds,cloudphysics
andcloudchemistry. A simpleway to expressthe removalrate of airbornecom-
pounds(bothgases andaerosols)is thescavenging
coefficient A, whichis thefrac-
tion of the airborneconcentrationremovedper unit of time. The airborneconcen-
trationCgcanthenbedescribed by
Cg= %,0exp(-ht) (9}
where
Cg,0 = concentration
at t = 0
X = scavenging
coefficient (s-•)
! = time (s).
Scavenging coefficients dependon rainfallrate, which is the resultof a seriesof

processes. Scavenging coefficients
can be usedto describeremoval by in-cloud
processes and below-cloud processesseparately
or the removalby both processes.
For gases,in- andbelow-cloud scavengingcoefficientsare functionsof Henry'slaw
coefficientif equilibriumis established
betweenthe air andthe drop.If no equilibri-
um isreached, whichis thecasefor highlysolublegasesbelowthe cloud,the coeffi-
cientwill dependon the diffusivityof the gasand on the ventilationcoefficient,
which is a functionof the radius[Levineand Schwartz,1982; Asman, 1994].
Scavenging
coefficients
cannotbe usedif compoundsare involvedin complicated
reactionsin theclouds.Thisis, however,not the casefor NHx and NOy. In- and
belowcloudscavenging coefficients
for a rainfall rate of 1 mm h-• are shownin
Table 2.3. They are upperestimates.Usually,the coefficientswill be smallerbe-
causeprecipitationoccursonlyin part of theareaof interestand mixingheightcan
bemuchhigher.A morerealisticnumberwouldbe aboutV•0-V3 of the resultsmen-
tioned in Table 2.3. Most of the NH3, NH4+ aerosol,HNO3, NO• radical, N2Os,
andNO•- aerosolwill beremovedafter onehour of continuousprecipitation.NO,
NO2 and PAN are removedat a very low rate by precipitation.When it occurs,wet
depositionis a muchmoreefficientremovalprocessthan dry deposition(seenext
section}.However,it rainsonly5-10% of the time in north-western Europe.This
meansthatwet depositionaveragedovera longerperiod,e.g.a year,is lessefficient
than suggested by Table2.3. It can, therefore,be of the sameorderas the lesseffi-
cientdry depositionprocess, becausethislastprocessoccursall the time.
2.7.Dry Deposition
Dry depositionrefersboth to the dry depositionprocessas well as to the amount
depositedbythisprocess.Dry deposition isthetransportof airbornecompounds to
thelandandseasurfaceby atmospheric turbulence.Atmospheric turbulence canbe
produced eitherby mechanical processes,i.e. windwhichstrikesovera roughsur-
face,or by a highertemperatureof the surfacethan of the air, i.e. wind
Asman and Larsen 35
TABLE 2.3. Scavenging coefficients (upperestimates)

of nitrogencompoundsat a rainfall rate of 1 mm h-•.
For in-cloud scavenging,a mixing heightof 1 km is
assumed[Asman et al., 1994a].
Scavenging
coefficientX (s-1)
Compound in-cloud below-cloud
NH3 1.4x 10-3 9.5 x 10-s

NH4 +aerosol 1.3x10 -3 5.0x10 -6
NO 1.9x10 -• = 0 *
NO2 1.4x 10 -20 =0 *
HNOz 1.5 x 10 -s =0 *
HNO3 1.4x 10-3 6.2 x 10-s
NO3 radical 1.4x 10-3 6.0x 10-s
N2Os 1.4x10 -3 4.0x10 -s
PAN 1.3x10 -7 =0 *
NO3- aerosol 1.3x10 -3 5.0x10 -6
* Almostno uptakewill take place.
strikesover the surface.Atmosphericturbulenceis producedby two typesof

processes: a mechanical process, in whichthe windis alteredby a roughsurface;
anda convective process, whentheseasurfaceiswarmerthantheair. Eventhough
dry deposition is calculatedwith an atmospheric transportmodelfor seaareas
only,it isnecessaryto takedry deposition on landintoaccount.Thereasonfor this
isthat dry depositionis a sinkandpartlydetermines the amountleft in the air par-
celthatcanbe deposited at sea.For thisreason,roughness heightanddry deposi-
tion on land are discussed here as well. First, surfaceroughness
will be discussed
because it isimplicatedin atmosphericturbulence processes.
SurfaceRoughness
Table2.4 showthesurface roughness fordifferent
surfaces
[Arya,1988].It appears
that
seasurfaces
areveryflat,i.e.thattheydonotcause asmuchturbulence
aslandsurfaces.
TAB L E 2.4. Surfaceroughness
for momentum
for differentsurfaces.
Surface Surfaceroughness
(m)
Ice,mudflats 10-s
Sea,largeexpansesof water 10-4-10-3
Snow(onfarmland) 2x10 -3
Grass(cut,uncut) 8x 10-3-2x 10-2
Farmland(summer) 2x10-2-1x10 -•
Forest 1
Towns (outskirts) 0.4
Centresof towns(small,large) 0.6,
36 2. Atmospheric
Processes
Thesurface roughness
for momentum for theseais,contraryto almostall landsur-
faces,notconstant,
butis a functionof thewindspeed.The reasonfor thisis thai
thesurfacechangesbecause wavesareformed. Themechanically produced rough.
hesslengthfor momentum, Z0m,isgivenbythefollowingequation[Lindforset al.
1991]:
g0m =
0.13v+ 0.0144u,
2 (10
u, g
where
Z0m -' surface

roughness lengthfor momentum (m)
v = kinematicviscosityof theair (mz s-1)
u, = frictionvelocity(m s-•)
g = gravitation(m s-2).
Thefirsttermin equation10 describes
a smoothsurface.Thesecondtermdescribe•,
roughconditions.Up to a windspeedof about3 m s-• thefirsttermdominates
an½
thesurface
roughness
decreases
withwindspeed.
At largerwindspeeds,
wavesare
formedandthesurface
roughness
increases
withwindspeed. Thesurface
rough-
nessfor momentum
cannotbemeasured
directly,butiscalculated
frommeasured
verticalwindprofiles.
AerodynamicResistance
Theresistance
totransport
intheairfroma reference
height
(Zr)tOtheheight
Z0m is
theso-called
aerodynamic
resistance.
Thisresistance
describes
thetransport
of all
gases
andparticles
to a thinlaminar
boundary
layer(0.1-1mm)justabovethesur-
face.Onlyforparticles
withradiuslarger
than5 Izmisthetransport
in theatmo-
spherenoticeably
influenced
bygravitation.
Theaerodynamicresistancera(sm-1)
atreference
height
zr(m}forallgasesandparticles
isgiven
by[Arya,1988]:
where
Von Karman's constant = 0.4

Monin-Obukhov
length
(m);Thisisa function
oftheratioofmechanically
to
thermallyproduced
turbulence.
Thefunction
•I/hisa correction
foratmospheric
stability.
For stableandconditions(L > 0): '•/ith= -5 z•./L
For unstableconditions
(L < 0): •h = 2 In ((1 + x2)/2),withx = (1 - 15zr/L)v4
For neutral conditions: XI/'
h -'
Asman and Larsen 37
LaminarBoundaryLayer Resistance
Gases
The laminarboundarylayerresistance
rb for gases(s m-1) is definedby
(12)
rb= /cU.In -•T0c
wherez0cis the surfaceroughnessfor concentration
of gasesat sea(m) and is given
is for smoothconditions(ReynoldsnumberRe = ZOmU./V < 0.15) by
z0c= 30 (v/u.)exp(-13.6/cSc2•3) (13)
andfor roughconditions(Re > 0.15):
z0c= 20 Z0mexp(-7.3 /cReTMSc•2) (14)
where
Sc= Schmidt
number
= v/Dg,whereDg= diffusivity
of thegas(m2s-S).
Thevalueof rbfor gasesat seacanthenbe foundfrom (12), (11), (13) and (14).
For land surfacesthe ratio ZOm/ZOc of gaseswith $c around0.6 to 0.$ is approxi-
matelyindependent of wind speedandhasthe valueof 7 to 12 for grassyor tree-
coveredsurfaces,but a value of 2 to 3 for tall trees[Brutsaert,1991].
Thislaminarboundaryresistance is a somewhat artificialresistance.
It is a kindof
correctionfactor,whichis neededto find the atmospheric resistance
for transport
of compounds fromtheatmospheric resistance
for transport of momentum, which
canbe determinedrelativelyeasily.
Particles
Particlescontaina substantialfractionof the atmospheric nitrogencompounds.

Thereare severalmechanisms by whichparticlescancrossthe laminarboundary
layerbut noneof thesemechanisms is veryefficient.Particles
havesomeproperties
whichcausetheir laminarboundarylayerresistance to be muchhigherthan for
gasesforbothseaandlandsurfaces. Thediffusivityof particlesismuchlowerthan
forgases.Thismeansthatparticles arenotableto cross thelaminarboundary layer
efficiently
bydiffusion.
Onlyverysmallparticles
withradius
< 0.1I•m,which
do
not contributemuch to the total aerosolmass,have reasonablediffusivities.For
particleswith a radiuslargerthanabout1 I•m,transportismoreefficient
because
theninterception andimpaction arealsoimportant.
Buta largefraction
of thepar-
ticles,includingmostnitrogen-containing
particles,
hasa radiusbetween0.1 and1
!-tinand is not easily
.•--.ref.
height
ra•...•rVgd
--.Zom
Figure2.7. Resistance
modelfor drydeposition
of particles
to thesea.
Wind tunnelmeasurements haveshownthat the dry deposition velocitiesof these

particles
arelow andthattheyarelimitedbythetransportacrossthethin laminar
boundarylayer[M611er andSchumann, 1970;$ehmelandSutter,1974]. Fieldmea-
surements,whichare veryuncertain,sometimes showmuchhigherdry deposition
velocities
[Sievering,
1981, 1984;Smithet al., 1991]. Thesedifferences wereattri-
butedto processeswhichwerenot takenintoaccountin thewind tunnelstudies,but
theycouldalsoresultfrom uncertaintiesin the measurements. $1inn[1983] givesan
overviewof all processesinvolvedin the air-to-seatransferof particles.Williams
[1982] postulatedthat seaspraycan enhancethe transportthroughthe laminar
sublayerup to threeordersof magnitudeby disruptingthe layer. Recentexperi-
mentsin an air-seaexchange tunnelindicate,however,that this effectis negligible
[Larsenet al., 1994, 1995]. For this reason,the model of [Slinn and Slinn, 1980;
Figure2.7] wasusedto calculatethe laminarboundarylayerresistance rb for (sea)
water:
K/JlO
rb= (15)
u.2(5½
-1/2+ 10-3/$t)
where
u•o= windspeedat 10 m height(m s-•)

Sc = Schmidt
number particle= v/Dp
Dp= Diffusivity
particle(m2s-1)
St = Stokes
number = u.2Vgw/(gu),withVgw
= gravitational
settling
velocity
of the
humidifiedparticle(m s-1)and
g = gravitation(m s-2).
Dp andVgwcanbe foundin Hinds [1982].Parallelto the aerodynamic and the
laminarboundarylayerresistance,
thereisa resistancedueto gravitational
settling,
whichisimportantonlyforlargerparticles.
Dueto thehighrelativehumidity in the
laminarboundarylayer,the particleswill get humidifiedwhich causesthem to
grow[Fitzgerald,
1975].Thisincreases theirsettlingvelocityand, therefore,
their
dry deposition
velocity.Figure2.8 showstheresultsof the modelof Slinnand $1inn
[1980]forthedrydeposition
velocity
asa function
of windspeed
andparticle
size.
A minimumin the dry depositionvelocityis observedfor radii between0.1 and 1
grn.A substantial
fractionof thenitrogen-containing
particlesis of this
Asman and Larsen 39
2 ..... 5 10 20
._. lOO
E lO
E
ß6 1
6.. 0.1
0.01
0.001 0.01 0.1 1 10
radius (l•m)
Figure2.8. Dry deposition
velocityof particlesat seaas a functionof theirradiusandthe
windspeed.
For land surfacesrb for particlesis not well known [Davidsonand Wu, 1990], but
is thoughtto be ratherhigh,of the orderof 500 s m-•. It dependson the particle
sizeandthe surfacestructure,e.g. on the presence of hairson leavesetc.In general,
dry depositionvelocityof particleson land showsalsoa minimumfor radii be-
tween0.1 and 1 txm.The valueof rbfor landsurfaces will belargerthanfor thesea
becausevegetationis rougher,which enhancesthe possibilityof capture.
SurfaceResistance
Gases
Liss[1983]givesan overviewof processes involvedin air-to-seatransferof gases.

At the sea,the surfaceresistance re is negligiblefor highlysolublegaseslike NH3,
HNO3 andN2Os [Asmanet al., 1994c].For thesegases,the resistance to transport
to the wateris thereforeentirelydeterminedby the resistance to transportin the air
(ra + rb).
In thecaseof poorlysolublegasesthereactivityin thewaterphaseis important.if

a gasreactsfast,thenthe concentration of the dissolved
gasin the upper,laminar
layerof the water decreases.This enablesmoreof the gasto get dissolved. In this
case,theresistance to uptakealsobecomes lower,but usuallynot aslow asfor the
highlysolublegases.It mainly dependson the reactionrate. The dry deposition
velocityis to a largeextentdeterminedby the surfaceresistance for this typeof
gases. Forthatreason,refor thesegasesdoesnotvarymuchwith windspeed. This
is partlythe casefor PAN.
If no reactionor onlya slowreactiontakesplace,thanthe resistance
r• becomes
verylargeand dominates. This is the casefor NO andNO2.
Thesurface resistance
for theuptakeof gases
bylandsurfacesdepends ontheprop-
ertiesof thegasandthesurface.HighlysolubleandreactivegaseslikeNH3,
and N2Oswill reactwith all surfacesor will dissolvein water layerson vegetation
and their surfaceresistance
will be low. For lesssolublegases,transportthrough
the stomataandsubsequent
absorptionin theleavesis important.Stomata,how-
ever,areonlyopenduringdaytime.
Consequently a diurnalvariationin thesurface
resistance
anddrydeposition
velocity
will occur.Thisisthecasefor e.g.NO2.Such
mechanisms
do not existat seaand thisis onereasonwhy the dry depositionvelo-
city of NO2 on landwill be higherthanat sea.Duringwinter,deciduous forests
haveno leavesandconsequently thesurface
resistance
will behigherduringwinter.
This is also true for coniferousforestsbecausethe transfervelocity through the
stomatais a functionof temperature. Duringrelativelylow temperature and light
intensityconditionsin winter,the biologicalactivitywill be reducedand the sur-
faceresistancewill thereforebe relativelyhigh for thesegases.Sucheffectswill
not exist at sea.
Particles
The surfaceresistance for particlesis assumed

to benegligiblebothfor seaand land
surfaces,
i.e.thatall particles
thatreachthesurface will betakenup bytheseawater.
Fluxes
The flux of gasesto a surfaceis calculatedfrom

F =--Ve(Ca--Cw*) (16)
whereF is the flux for reference
heightz ref(toolm-2 s-S}.The flux is by definition
negativeif thecompound isremovedfromtheatmosphere. In thisequationcais the
air concentration abovethe seasurface(mol m-3) and Cw*is the theoreticalgas
phaseconcentration, whichwould be in equilibriumwith the concentration of dis-
solvedgasat thesea-airinterface(molm-3 air}.If cais largerthanCw*,dry deposi-
tion takesplace.In theoppositecaseemission takesplace.
The dry deposition
velocityis definedby
F
•d -- (17)
Ca
It canbe seenfrom thisequationthat Vdis onlyequalto veif Cw*is zero.This is the

casefor mostgases,exceptfor NH3. Thisholdsfor seawater and for agricultural
crops.
c,•* of NH3 in seawater canbe found from [Asmanet al. 1994b]-

[NHx]
c•* = (•8)
RTHNH3(.•._.._I+
TNH
3 10-pH
4KNH )
TNH
Asman and Larsen 41
where
c,* = NH3 concentration

in air, whichwouldbein equilibriumwith [NHx] (mol
m-3)
[NHx]= NHx concentration
in thesurface
(molm-3)
3',N•3= activity
coefficient
NH3.H20
3'N•4= activitycoefficient
NH4+
R = gasconstant(8.2075 x 10-z atm1tool-• K-•)
HN•3= Henry's
lawconstant
forNH3(mol1-• atm-•)
pH = pH waterin surface,
whichisa measure
of theactivityof H+in thesurface
solution
KNH4= dissociation
constant
forNH4
The valueof cs*increases
stronglywith temperature
dueto the temperature
depen-
denceof/-/NH3and KNH4.
The activitycoefficientof NH3.H20 in seawateris approximated
by the following
equation,whichis validfor an NaCI solutionof 25øC[RandallandFailey,1927]:
•/s•3= 1 + 0.085I (19)
The ionic strengthI for sea water as a functionof salinitycan be found from
[Lymanand Fleming,1940]
I = 0.00147 + 0.01988 S + 2.08357 x 10-s S2 (20)
Moreover,the relationshipis not valid if seawater is dilutedconsiderably with
waterfor whichthe relativecontributionof the differentionsdiffersmarkedlyfrom
that in seawater (e.g.in estuaries).
Theactivitycoefficient
for NH4+ in seawaterat 25øCcanbefoundbyusingan ion
pairingmodel[MilleroandSchreiber, 1982;Asmanet al., 1994b]
Y•4* = 0.883- 0.0768lrt(sal) (21)
Asmanet al. [1994b]foundsuchhighNH3.H20 concentrations in theNorth Sea,
thatdry deposition is reduced substantially.
In a fewcases an upwardfluxwas
noted.Quinnet al. [1988] describe suchNH3 emissions in the PacificOcean.In
general,
marine(endogenous) NH3 emission at seais necessary to explainNH4+
concentrationsin precipitation
overtheoceans [DentenerandCrutzen, 1994].
Table2.5 showsexchangevelocities
for gases
andparticles.
Table2.5 showsalso
therateat whichtheconcentration
of thecompoundswill beremoved (% h-•) by
drydepositionif nosubstantial
concentration
wereavailable in seawater.Thedry
depositionvelocityisalsoshownforan average landsurface (Z0m= 0.3 m).Table
2.5 showsthat dry depositionvelocities
aremuchlowerovertheseathanover
land.Thisiscaused bythedifference
in surface
roughness aswellasbythediffer-
entpropertiesof thesurface(onlandbiological
processesin vegetationcanbeim-
portant).Forthisreason, specific
drydepositionvelocities
should beusedfor sea
areasto calculatethe dry depositionto the
TABLE 2.5. Computed exchange velocitiesandremovalratesof nitrogencompounds to

seaand landsurfaceat a wind velocityof 5 m s-l at 10 m heightand a mixingheightof
1000 m [Asmanet al., 1994c].
Sea Land
Ve Removalrate ve Removalrate
Compound (rams-l) (% h-1) (mms-1) (% h-•)
NH3 7.6 2.7 22 7.9

NH4 + aerosol 0.2 0.07 1.23 0.44
NO 3.5x 10 -4 1 x10 -4 0.98 0.35
NO2 2.2x 10-3 8)<10-4 6.05 (day); 2.2
2.74(night) 1.0
HNO2 6.9 2.5 8.67 3.1
HNO3 6.4 2.3 65.1 23
NO3 radical 6.6 2.4 65.1 23
N2Os 6.1 2.2 65.1 23
PAN 1.0 0.36 1.94 0.70
NO3- aerosol 0.2 0.07 1.23 0.44
The dry deposition

velocities
in Table2.5 are presented
moreaccurately
thanactuallyknown.The uncertaintyis at
least 50 %.
2.8. Model Results and Discussion
Processesthat play a role in atmospheric transportmodelshavebeenpresentedand

discussed.In principle,an atmospheric transportmodelcannow be constructed by
puttingthe processes for eachcomponentin a differentialequationof type (1}. In
thisway, a setof equations is obtained,whichhasto be integratedto find the con-
centration/deposition at a receptorpoint at sea.Thereexistmanydifferenttypesof
atmospheric transportmodels.They are differentin the sensethat they are either
Eulerianor Lagrangian,that contrastingnumericalmethodsare usedto solvethe
equations,differentsetsof chemicalreactionsare used,different horizontal and
verticalresolution is usedetc.The choiceof the modeltypedepends on manyfac-
tors:the compounds and areasof interest,the locationof importantsourceareas
comparedto the locationof the areasfor which the depositionshouldbe calcu-
lated,thelengthof the periodof interestetc.A factorthat can be veryimportant
is the availabilityof computerresources, because the necessarycalculationstake
muchtime.A way to avoidexcessive cputime is to calculatethe depositionfor a
limited setof differentsituations(classes).
All situationsare then attributed to one
of theseclasses and the averagedepositionis then foundfrom the valuesfor each
classweighted with thefrequency of occurrence of thatclass.Thistypeof modelis
calleda statistical
model[seee.g.AsmanandRunge,1991].
Beforeapplyinga model,its resultsmustbe verifiedwith measurements.
An exam-
ple for suchverificationfor the ACDEP modelfor the wet depositionof NH4*,
whichis shownin Figure
Asmanand Larsen 43
Artholt !990
2OO
160
100
• 50
0.•,•,•/,
'•' -. ""'-
'-- -•
•.....
J F M A M J J A 8 O N D
Figure2.9. Comparison
of modeledandmeasured
wet deposition
of NHx for Anholtin 1990.
Table2.6 showsresultsof the calculationswith the ACDEP modelfor the Kattegat

for the year 1990. The modelresultswere in reasonable
agreement with measured
concentrations and wet depositiondata [Asmanet al. 1994a].The largestpart of
the atmosphericnitrogeninput is attributedto wet deposition.Wet depositionof
NHx contributes
42% to thetotalnitrogeninput,whileNOycontributes
30%. The
NHx contribution
to thedry deposition
is 17% whiletheNOycontribution
is 11%.
NH3 and HNO3 contributemost to the dry deposition,becauseof their high depo-
sition velocitiesdespitetheir lower concentrations
relative to NO2, PAN or the
nitrogen-containing
aerosols.
The contributionof NH3 andHNO3 to thewet depo-
TABLE 2.6. Deposition of nitrogen compoundsto the

Kattegat(kgN km-2 yr-•)•1[Asmanet al., 1994a].
Compound dry wet total
NH3 167.2 64.2 231.4

NH4* aerosol 16.8 340.3 357.1
NO 1.6 0.0 1.6
NO,, 18.1 0.(5 18.1
HNO, -
0.5 0.0 0.5
HNO3 46.8 90.1 136.9
HNO4 0.5 1.0 1.5
NO3 radical 0.4 1.2 1.6
N2Os 7.4 15.8 23.2
PAN 3.6 0.0 3.6
OrganicNO3- 1.4 0.0 1.4
NO3- aerosol 6.9 174.9 181.8
Total N 271.2 687.5 958.7
Thenumbers
aregivenmuchmoreaccurately
thanactually
44 2. Atmospheric
Processes
> 1885
1717-1885
1549-1717
1381-1549
1213-1381
876-1045
1046-1213
708- 876
540- 708
< 540
Figure2.10.TotalNHx deposition
in Kattegat(kgN km-2 yr-•).
sitionis alsoimportant,but the contributionof the aerosolsdominates.Table 2.6

illustratesagainthat wet depositionis a more importantremovalprocessfor
aerosols thandry deposition. The geographical distributionsof the total deposition
(thesumof wetanddrydeposition) of NHx andNOy aregivenin Figures 2.10 and
2.11 showinglowerdepositions at seathan on land. This differencebetweenland
and searesultsis to a largepart causedby the loweramountof precipitationat sea,
and also by lower dry depositionvelocitiesat sea,and also becausemost sources
are land-based,which leadsto higherconcentrations on land. Model resultsshow
that Denmarkcontributes35% of the total NHx depositionto the Kattegat,but
only7% to thetotalNOydeposition. In fact,Germanyisthelargestcontributorto
the totalNOy deposition to the Kattegatwith about35%. Detailedresultsof the
calculationsare presentedin Asmanet al.
Asmanand Larsen 45
Figure2.11.TotalNOydeposition
inKattegat
(kgN km-2yr-•}.
The contributionof the atmosphericinput of nitrogento the Kattegatis about

20-30% of thetotalinputincludingthe transportfromotherseaareas,runoffetc.
(seechapter 11).
In general,wet depositionis moreimportantthandry deposition
at sea,whereas
nearsourceareason land dry depositioncanbe moreimportantfor compounds
with high dry depositionvelocities.
Lindforset al. [1991]estimated thenitrogendepositionto theBalticSeafrommea-
suredconcentrations and measuredmeteorological data. They founda nitrogen
depositionto the SouthBaltic,CentralBalticand North Balticof 1140-&_350,
910+270 and 650+280 kg N km-2 yr-•, respectively. Van Jaarsveld [1992] gives
an overviewof estimates of the nitrogendeposition
to the North Sea.He gives
bestestimates
a total deposition
of NHx (sumof dry and wet deposition)of 270
kgN km-2yr-1anda totaldeposition
of NOyof 380kgN km-2yr-1.Thisgivesa
total N deposition
of 650 kg N km-2 yr-1. The wet depositionof NHx to remote
oceanic
areasis 40-50 kg N km-2 yr-• andthewet deposition
of NOy in these
areasis 30-40 kg N km-2 yr-• [Galloway,1985; Buijsmanet al., 1991; Duceet
al, 1991].
Acknowledgments.Thisworkwaspartlyfundedby the DanishEnvironmental Protection

Agency, Copenhagen,
Denmark,withintheprojectDanishMarineResearchProgramme 90.
Thisworkispartlybasedonresearchcarried
outbythefollowingpersons:
PeterAllerup,
Jes
J•rgensen, HenningMadsen,$•ren Overgaard,Flemming Vejen(DanishMeteorological
Institute,Copenhagen,
Denmark),$ven-ErikGryning,AnnaMaria Sempreviva,
PoulHum-
melsh•j,NielsOttoJensen(Ris• NationalLaboratory,
Roskilde,Denmark),Ole Hertel,
Ruwim Berkowicz,Erik H. Runge,JesperChristensen,
Mads Hovmand (National Envi-
ronmental
Research
Institute).
Trajectories
used
inthemodelcalculations
wereprovided
by
the Meteorological
Synthesizing
Centre-West,EuropeanMonitoringand Evaluation
Pro-
gramme at theNorwegian
Meteorological
Institute,
Oslo,Norway.
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3
Water Masses,
Stratification and Circulation
JacobSteenM•ller
Introduction
Theaimof thischapteris to describe the physical

oceanographic processesthat
mayplaya rolein eutrophication.
Themanifestation of adverseeffectsof eutrophi-
cationin coastalmarineenvironments isclosely
relatedto hydrographicprocesses.
Thetermhydrographic processesis usedhereto meanphysical processes suchas
advection,thedevelopmentof stratification,
establishment
of frontsandthemixing
of watermasses. The salinityandtemperature stratification,
whichis present in
manycoastalwaters,resultsin a spatialseparation
of photosynthetic
andminerali-
zationprocesses
whichcan lead to oxygendepletionof the lowerlayersof the
watercolumn[Fenchel,1992].
It is importantto notethat the oxygendepletionis not causedby theeutrophica-
tionitself,but thatoxygendepletion requires
hydrographic conditionsto develop
thatfavorstagnant or isolatedwatermasses.
Sucha spatialseparation of primary
productionand mineralizationis not uniquebut is foundin manymarineareas
aroundtheworld.Amongthemoreextremeexamples of areasexhibitingthisphe-
nomenon are the Black Sea and the North Sea.
In the BlackSea,the hydrographic conditionshavecausedoxygendepletioninde-

pendentlyof the recentincreasein nutrientloads.The BlackSeareceivesa large
riverineinflow, where the surplusof water leavesthe Black Sea throughthe
Bosporus Strait(Figure3.1). In the Bosporus, a pronouncedtwo-layerflow system
is maintainedby the surplusof water from the BlackSeaandthe inflowof saline
Mediterranean waterenteringthroughfirstthe Dardanelles andthenthe Marmara
Sea.The flow throughthe Bosporus is dueto a balancebetweenthe surfacewater
slope(thebarotropicgradient)whichforcesthesurfacewaterout of the BlackSea
Eutrophication
in CoastalMarineEcosystems
Coastaland EstuarineStudies,Volume52, Pages51-66
Copyright1996by the AmericanGeophysical Union
52 3. Water Masses,Stratificationand Circulation
BLACKSEA
;PHORU
MARMARA SE
ßQ•
MARMARASEA BOSPHORUS BLACKSEA NET FRESH-WATER

I I INPUT
L
20.?'10•m5/s I.....
19.1ß103m'¾s •____m
20.2
ps• 17.9
p• 9.5.105m
57.5psu!• • NET-ENTRAINMENT
/////////////////••',o•
/ /
• • "'u/ /
,, ............
Figure3.1. The BlackSea.Waterexchange of the BlackSea.Salinitystratificationisrespons-

ible for naturaloxygendepletionof the stratabelowthe halocline.Data elaboratedfrom
Onliiata[1990].
and the pressuregradientat the lower layercausedby the densitydifference(the

baroclinicgradient)betweenthe brackishBlackSeawater and the salineMediter-
raneanwater in the Marmara. The stratificationof the BlackSea is thereby
Moller 53
6JE 7!E 8[E 9JE

Skagerrak
57'N
Kattegat
986-1988
North Sea
1981
The Sound
ittle Belt
Drogden
Baltic Sea
55'N
1982
! O0 krn
54'N
I I I . I I
Figure3.2. Oxygendepletionareasof theNorth SeaandKattegat[Richardson,

1989].
tainedby the balanceof the salinewaterinflow throughthe Bosporus andtheverti-

cal mixingof the salinebottomwaterinto the brackishsurfacewater.The vertical
mixingis primarilycausedby wind stirring.Phytoplankton and detritusfrom the
upperwaterlayerof theBlackSeasettleto thebottomlayerwheretheyaredegraded
andconsumeoxygen;in additionthe sedimentwill alsosustaina potentialoxygen
demanddueto degradation of settledmaterial.The supplyof oxygento the lower
layerislimitedto theadvective transportthroughtheBosporus becausethestratifi-
cationhampersdownwardmixing(entrainment) of oxygen-richsurfacewaterinto
the lowerlayer.The consumption of oxygenthusexceeds theoxygensupplyand
oxygendepletion becomes a permanent situationbelowthepycnocline.
TheNorthSeahasexperienced considerableeutrophication
duringthelastdecades
and,in recentyears,oxygendepletionhasbeenreported[e.g.,Richardson, 1989].
Theoxygendepletion hasbeenobservedin thepartsof theNorthSeawheretem-
peraturestratification
develops
duringthe summer(Figure3.2). Thesolarheating
of the surface water stabilizes the water column and createsa stratification which
hampers the downward transportof oxygenandthusenhancesan oxygendeple-
tion.Theextension
of thedepletedareais,amongotherfactors,
determined
bythe
extension
of the stratification,
maintained
througha balancebetweenthe stabiliz-
ingforces(heatinput)andthe destabilizing
forces(tidalandwind-mixing)
[e.g.,
Pedersen,
1994].
The North Seaand the Black Seaillustratethe importanceof the hydrographic
conditions
for thedevelopment
of eutrophication
effects.
Alsothe
processes
of theDanishStraitsandcoastal
watersarestronglyinfluencedby thehy-
drography.In thefollowing,
thebasicphysical
phenomena of theDanishStraitsare
described,
andit is seenthatmanyof thehydrographic processesidentifiedin the
BlackSeaandNorth Seaalsoprevailin thesecoastalareas.
3.2.Advectionand Mixing
Transportandmixingof waterand matterin the seaare described by the general
equations of continuityand motion.In their exactform, theseequationscontain
termsthatexpress thetransportof momentum, heatandmass.Generally,however,
it is not possibleto solvethe equationsand expressthe transportand mixing of
matterin the oceanwithoutintroducingsimplifyingassumptions. One of the rea-
sonsfor thisis the presenceof nonlineartermsin the equations.The equationscan
only be solvedby directcalculationor by integrationusinga computercodewhen
the nonlinearterms.can be eitherneglectedor determinedby introducingsuitable
approximations[Rodi 1980 and 1994].
It is theart of physicaloceanographic scienceto assess
andchoosesuitablesimplifi-
cationsthatallowa rationalanalysisof hydrographic processes
without"spoiling"
the result.The choiceof approximations isdependent uponthe problemto be ana-
lyzed.In particular,it is importantto analyzethe temporaland spatialscalesof the
(biological) system.Asan illustration, we canfirstlookat theresuspensionof par-
ticulate matter in a coastal environment and then at the renewal of bottom water of
the deepbasinsof the BlackSea.It is apparentthat the spatialand temporalscales
of the two processes
aresignificantly different.In the firstcase(resuspension)
the
detailed turbulence structure close to the sea bottom must be described at a time
scaletakingthewaveperiodinto consideration, whilein the secondcase(renewal}
sucha detailedturbulence description
isof minorimportance. The problemdictates
the propersimplifications.A carefulconsideration of theseaspects should,there-
fore,precede anybiologicaL/oceanographicalinvestigation.
The followingreviewof
the hydrography of the DanishStraitsin relationto eutrophication will in more
detailillustrate
thislink betweentheassessment of thebiologicalproblemandthe
hydrographic analysis.
The ContinuityEquation
Thechange of a property
in thesea,(e.g.,theconcentration
of oxygenor theamount
of plankton
withinthephoticlayer)canbedescribed asthesumof thechanges due
to advective
transport,
turbulenttransport (dispersion
or mixing)andtheexchange
withothercompartments of matterthroughbiologicalor chemicalreactions:
'½'
at - Ui3:Xi 3Xi+T(c,...) (1)

wheret is time,x is theCartesian
coordinate, u is the mean(nonturbulent) flow
velocity,
c istheconcentrationof matter,u' andc' aretheturbulentpartof u and
Moller 55
andT is a termexpressing
theinteraction
between
compartments.
In Eq.1, theleft
termexpresses
therateof thechange
of concentration,
thefirsttermontheright
the advection(transportby nonturbulent motion)of matterwith thecurrent,the
secondterm on the rightthe turbulenttransport(dispersionor mixing)of matter
andthe lastterm the chemical/biological
exchangeof the matter.
Depending on the problem,someof the abovetermsmay be neglected in orderto
simplifythesolution. Typically,thebiologistwill focuson thelastterm(T), e.g.by
investigating thechange in growthrateof somealgaeasa function of thelightpenetra-
tion (thetransporttermsareneglected). Thisis perfectlysatisfactory whentheinvesti-
gationiscarriedoutin a closedenvironment (i.e.,anaquarium or a testtube)without
spatialgradients in concentrations.
However,whentheinvestigation iscarriedoutin
the field, the transporttermsmay be dominantfor the observedchanges.On the
otherside,the physicists maytendto neglectthelastterm(T) andfocuson thetrans-
portprocesses which,asdescribed above,arewelldescribed bythegeneral equations
of motionandcontinuity.The argumentshowsthat it is importantto analyze,which
of thetermsdominatetheproblemto be addressed, beforetheinvestigationis started.
The Densityof SeaWater

The densityof the seawater is of greatimportancefor the transportprocessesin the
sea.The verticalmixingis reducedwhena verticaldensitygradient(oftenreferredto
asinterface)is presentandthe horizontalmovement of wateris influenced
by hori-
zontaldensitygradients (oftenreferredto asfronts}.Thedensity of seawaterdepends
on thesalinityandtemperature. For depthsgreaterthanseveralhundredmeters, the
pressurealsoinfluencesthedensity. Therelationship between thesalinityandtempe-
ratureon the onesideandthe densityon theotherhasbeendetermined by measure-
mentsandisgivenin theformof analgorithm
(Figure
3.3;UNESCO1981a,b}.
Temperature, øC 30 '
25
2O
15 oo
10 • ,, •
5
0 5 10 15 20 25 30
Salinity, psu
Figure
3.3.Thedensityof seawater,p (kgm-3),isa function
of temperature
andsalinity.
TheSalinity
unitpsuisdefined
in UNESCO [1981b], forpractical
calculations
psuisequal
to ppt or
1• WIND,
w(m/s)
Ve
• (2.5.10-2w)
3+(0.3
lOOO Ag h
v)3
h1 Vl /31
UPPER LAYER: Ve=VeO, V=Vl, h=hl, w=w
•t-I / ^%0
I / j/-f-/-•/--•/ LOWERLAYER: Ve=Vel, V=VO, h=hO, w=O
•O J'•VoPo A=
Po-Pl
PO
Figure3.4. A simplified
two-layer
system
andan evaluation
of theentrainment
velocities
basedon Pedersen's
theory[1986].
Stratification
Whenthedensity of theseawatervarieswithdepth,thewatercolumnis saidto be
stratified.The stratification
may be causedby heatingof the surfacewater or re-
ducedbysalinitydueto riverineinfluence.Othermechanisms suchaswindstirring
and the actionof shearstresses due to bottomfriction resultin irregularmotions
(turbulence)of the water.The turbulentmotionwill resultin mixingof water thus
workingagainstthe forcesthat causestratification. Stratification
of watermasses
reduces themixingbetween differentlayersof thewatercolumndueto dampingof
turbulentmotionsin a densitygradient.The turbulentmotionvarieswith current
and wind conditions,which may both showgreat variability. For homogeneous
flow, the turbulentkineticenergyeventually is dissipated
into heat.In a stratified
flow,partof theturbulentkineticenergyisusedto mix thelayersof differentdensity.
If we considera situationwherethe watercolumnis stronglystratifiedand may be
considered asa two-layersystemdividedby a sharpinterface(Figure3.4), any de-
formationof the interfacewill producea restoringforcedue to the buoyancy:if
bottomwateris liftedinto the surfacelayer,gravitywill seekto tow it backinto the
bottomwater,and if surfacewater is 15ushed into the bottomwater, buoyancywill
seekto lift the water back into the surfacelayer. To overcomethis mechanism,
energyhasto be supplied.This energyis transferredfrom the turbulentkinetic
energyof the flow.
FollowingPedersen [1986], the verticalmixingprocesscan be describedas a two-
way entrainment process.Whena layerof no movementis overlaidby a turbulent
layer,the quietlayeris entrainedinto the turbulentlayer.This processincreases
the
potentialenergyof the watercolumnby lifting densewater into the surfacelayer.
Similarly,a turbulentbottomlayerentrainswater from a quietsurfacelayer.When
both layersare turbulent,the processis two-way.The efficiencyof the mixingcan
beassessed by relatingthegainin potentialenergy,dueto the mixing,with the pro-
ductionof turbulentkineticenergyof the flow. To illustratethe magnitudeof the
entrainmentwe considera simpletwo-layersystem(Figure3.4). The mixing
Moller 57
tweenthe layersis determined by theturbulence production

dueto thewind,the
velocityshearandthe bottomfriction.W is the windspeed,h thewaterlayer
depth,v the averagevelocityof thecurrent,p themeandensityand•'etheentrain-
mentvelocity.
The entrainmentassessment givenin Figure3.4 is only a roughapproximation to
the problembut it illustratesthe very strong(cubic)dependence of the entrain-
mentto thewindspeedandthecurrentspeed. Thisstrongnonlinearrelationshipil-
lustrates
how shortstormeventshavea largeimpacton the mixing.
Flow Condition
The advectivetransportof matterin theseais governed by the flow conditions. The

velocityfield entersthe continuityequationas shownin Eq.1. The velocityfieldis
determined by the balanceof forcesactingon thewater.This balanceis quantified
throughthe momentumequation.The momentumequationexpresses the balance
betweenthe inertia forces,the pressureand gravityforces,the rotationalforces
(Coriolisforce)andthe frictionalforces.As it wasthecasefor thecontinuityequa-
tion alsothe momentumequationcannotbe solvedin the generalcase,simplifying
assumptions mustbe introduceddepending on theproblemto be investigated. Some
of the termsmay be neglectedin orderto simplifythe solution.In oceanographic
problemsthe frictionterm may often be neglected,whereasin mostcoastalprob-
lemsthisterm is dominatingthe problem.It is thereforecrucialto addressand ana-
lyzethe dominanttermsof the problembeforetheinvestigation is started.
In manyshallow-watercasesthe flow is governedby a balancebetweenthe bottom
frictionand the pressuregradient.When the pressure gradientis due to a water
levelgradient,the flow is saidto be barotropic;whenthe pressuregradientis due
to a densitygradient,the flow is saidto be baroclinic.
An exampleof a barotropi-
callydominatedflow is thetidal currentin theNorth Sea.An exampleof baroclini-
callydominatedflow is the exchangeflow betweenthe MarmaraSeaandthe Black
Sea.In the generalcase,both modesof flow forcingmustbeconsidered whenthe
water is stratified.
In manyoceanographic casestherotationof theEarthinfluences theflow pattern.

An exampleof the influence of therotationof theEarthis givenbelowin thesec-
tionon the Skagerrak front.Whentherotationof theEarthis entering theprob-
lem,thetermgeostrophic flow isoftenusedexpressingthattheCoriolisforcingbe-
comesimportant.
3.3.Hydrographyof the DanishStraits

TheDanishStraitsshowexamplesof themajorityof thephysical
featuresof rele-
vancewhenconsideringeutrophication.
The DanishStraitsarepart of theBaltic
Seaand,hydrographically,
theyformthetransition
areabetween thebrackish
ProperandthesalineNorthSea.In thefollowing thesewatersareexamined and

localexamples usedto illustrate
theinteraction
betweenhydrography andeutroph-
ication.Thisdiscussionalsogivesthehydrographicbasisforthefollowingchapters
whichdealwithbiological aspectsof theeutrophication
processes.An overviewof
theareais shownin Figure3.2 wheregeographical namesusedin the text canbe
found.
The conditionsinsidethestraitsystemaredetermined by the boundaryconditions

and the lawsof nature[e.g.,Moller and Hansen,1994]. The imposedboundary
conditionssuchas bathymetry, the meteorological
forcing,river inflow, tide and
surgesactthroughthelawsof natureandtheresulting hydrographic conditions are
consideredtheoutputof theDanishStraitsystem.The hydrographic conditions are
describedin termsof the salinityand temperaturestratificationas well as the
advectionandturbulentmixingof matter.
Bathymetry
The bathymetryof the systemis depictedin Figure5 in chapter 1. Three domi-
natingfeaturesshouldbe noted.The hydrographic boundarytoward the BalticSea
is givenby the Darssand Drogdensills.The sill depthat Drogdenis approx. 8 m
and at Darssapprox. 17 m. The connectionbetweenthe North Seaand the Baltic
Seais formedby three channels:the Great Belt, the Soundand the Little Belt. The
water depthof the DanishStraitsis shallowwith typicaldepthsbetween10 and 20
m. The boundarybetweenthe Kattegatand the Skagerrakin the North Seais char-
acterizedby a slopingbottom toward the deep Norwegian Trench. In the Ska-
gerrak,the depthincreases
to severalhundredmeters.
Figure3.5. Idealized
depiction
of a) highpressure
situation
creating
a Balticoutflow,b) low
pressure
situationcreatingan inflow [Weidemann,
M•ller
Tideand Meteorology
The Danish Straits form the transition between the tidal North Sea and the non-
tidalBalticSea.The tidalinfluencethusdecreasesfromthe Skagerrak towardthe
Baltic.The flow throughthe DanishStraitsis causedby the waterleveldifference
betweenKattegatandthe westernBalticSea.Dueto the shiftingwinds,thewater
leveldifferenceis highlyvariablecausingan oscillatory
flow throughthe straits.
Eventhoughthe net currentis northbound(dueto the fresh-water surplusof
15,000 m3 s-• from the Baltic, the instantaneous
currentfluctuatesfrom north-
boundto southbound with peak discharges throughthe channels being10-15
timesthemeandischarge. Predictive
modelsfor currentandwaterlevels,therefore,
mustincludethe combined effectof tidal forcingandthe meteorological forcing
[e.g.,Vestedet al., 1991].The meteorological forcingof thesystemisgivenby the
solarheatingandthewindforcing.Thewind andatmospheric forcingarethedom-
inatingcurrent-generating
mechanisms(Figure3.5) and the wind-induced
currents
arealsothemain contributors
to themixingenergyin the lowerwaterlayer.
Stratification
The waters in the Danish Straits are stratified due to the outflow of brackish water
fromtheBalticSea.Whenthe flow is northbound, brackishwateris forcedthrough
the Straitsas a surfacecurrent(Figure3.6). Sincethe brackishwateris of lessden-
PRINCIPLE
SKAGIrRRAK
FRONT
BELTFRONT
•5
KATTEGAT (;$•EAT BELT BALTIC SEA
DEPTH
OBSERVED INFLOW 21 JULY 1971

SOUTHBOUND CURRENT
•AGERRAK
FRONT
BEL'rFR•T
••.-z•----•'•_• _,./,••,/. s=8

.•
• •/•'•2•
45
T•GAT •EAT •LT B•C •A

•P•
(=)
OBSERVED OUTFLOW 25 MAY 1971
NORTHBOUND CURRENT
Figure3.6. Schematic
diagramof the currentandstratification
conditions
of theDanish
Straits.Modifiedfrom TheBeltProject,Ministryof theEnvironment
Great Belt
;•resund
150.000
75.000
rna•= o
' i i i i i i i i i t i i 1 i i i "1 i i i i i' i i i i i i i i '"'i'"' i i i
29/06/90 o6/o7• 13/o7/9o 20/07/90 27/07/90 03/08/90 1(//o8/9o
Figure3.7.Measureddischarge
throughtheGreatBelt,thickline(attheGreatBeltBridge)
andtheSound,thinline(atDrogden}
duringa six-weekperiodin summer1990.Modified
fromMel!erandPealersen
[1993].
sitythanthewaterfromtheSkagerrak,it formsa surface

layer.Thesurface layer
depth isbasically
determined
bythesilldepth atDrogden andDarss. Duringsouth-
wardcurrent thesurface
waterisforcedbackwhileundergoing continued mixing
withthebottom water.Whenthemoresaline waterpassesthesillsit plunges
down
the slopes.
TheBalticSeaBoundary
Theinflowof saline
waterto theBalticSeaisa highlyintermittent
phenomenon
(Figure
3.7).Thetypical
duration
of aninflowsituation
istwoto fourdays.How-
ever,withirregular
intervals,
theduration
ismuchlonger.
In theareawheretheKat-
tegatandBeltsurfacewatersmeetthe13altic
surface
waterandplunge downthe
slope,
a front(theBeltfront}
isformed.
Atthisfront,thesurface
salinity
rapidly
de-
creases
fromtheBeltsurface
watersalinity
(15-25psu)to theBalticsurface
water
salinity
(8psu}.
Thedischarge
under"normal"
conditions
is,according
toJacobsen
[1980],divided
between
thethreechannels:
theGreatBelt,theSoundandtheLittle
Beltintheratio7:3:1.If aninflowevent
continues
fora longtime,theentire
BeltSea
andtheKattegat areflushedwithsaline
NorthSeaandSkagerrakwaterandwaterof
highsalinityplunges
intotheBalticSea.Undertheseconditions
the total inflowis
divided betweentheGreatBeltandtheSound as8:3,whileforthehigh-salinity
waterit is6:5[Jakobsen,
1995].Such
rarelarge
inflows
ofsaline
waterplaya crucial
rolefortherenewalofthebottom waterofthedeepbasins
intheBaltic
Sea,whereas
thetypicalandfrequentinflow
eventsofa fewdays'duration
renewonlytheinter-
mediatewaterlayersof theBalticSea.A reviewof thewaterbalancefor the Baltic
SeaisgivenbyMellerandHansen[1994],wherefurtherreferences canbe
Moller 61
TheNorth SeaBoundary
The boundaryprocesses towardthe North Sea(Skagerrak) are morecomplicated

thanthoseat thesouthern boundary. Thisis dueto themoreopenbathymetry that
allowsfor an internallycontrolledflow as opposed to the flow overtheDrogden
andDarsssillswherethebathymetry andbottomfrictiontogethergoverntheflow.
In theSkagerrak, theBalticoutflowformsa surfacelayerof brackishwaterwhich,
in general,followstheeasternandnortherncoastline dueto theCoriolisforce.The
interface at the surfacebetweenthe Balticoutflowandthe Skagerrak surfacewater
is calledthe Skagerrak front. The locationof thisdensityfront is dependenton the
combined influenceof tidal and wind forcing.The hydrography of thefront shows
an annualvariation correspondingto the variation in the Baltic outflow and the
localwindforcing,[Jakobsen et al. 1994 and Andersson
andRydberg,1993].
The residualtidal currentat the Skagerrakcoastof Jutlandis eastboundand this,
combinedwith the predominantwesterlywinds,createsa counter-clockwise (cy-
clonic}currentin the Skagerrak.The salineNorth Seawater divesunderthe Baltic
outflowwhen it meetsthe Skagerrakfront. In the centralSkagerrak, a domingof
Atlantic water and water from the northern and central North Sea is observed. In
the dome, water of salinity 35 is raisedto levels-20 'm or less,[e.g.,Poulsen,
1991]. The North Seawater and the Atlantic water mix and enterthe Kattegat
below the Baltic outflow water. Due to rivefine water inflow to the southern
North Seathe water with origin heretendsto interleavebetweenthe Kattegatsur-
face water and the deep inflow from the Skagerrak.Water from the southern
North Seaholdshigherconcentrations of nutrientsdueto the riverrunoff;thishas
beenidentifiedas interleavingwater in the Kattegatwith highernutrientcontents
than the bottom water. The water from the southern North Sea can be distin-
guished
from the SkagerrakandotherNorth Seawaterby its contentof Gelbstoff
[Jakobsen
et al. 1994].
Mixingand Effectsof Stratification

Dueto mixingbetween thelayers,thesurfacesalinityincreases
fromthesouthto-
wardthe north.An observerfollowinga northbound surfacecurrentthroughthe
DanishStraitswill thusexperience increasing
salinityovertimedueto thismixing.
Because the salinityincreasestowardthe north,measurements takenat a fixed
pointin the Beltswill showincreasing salinityovertime duringsouthward flow
anddecreasing salinityovertimewhentheflowisnorthward. In generaltheenergy
transferfrom the wind to the seais proportionalto the cubeof the wind speed,
whereby themixingbetween thelayersisdependent onthethirdpowerof thewind
speed,Figure3.4.Thewindspeed cubedshows a moreextreme variationthanthe
wind speed
62 3. WaterMasses,
Stratification
andCirculation
Figure
3.8.Distribution
ofnitrogen
loadingtotheDanish
Straits.
a: 1950s,
b:1980s.Unitis
1000tonnesofnitrogen
peryear.Atm.istheatmospheric
source.
FromHansen etal.[1994].
General Circulation
Thegeneralwatercirculation
in a two-layermodelof theDanishStraits
andthe
nutrient
transports
andsourcesto thesystemaredescribedbyHansenet al. [1990
and1994].Basedon a reviewof available
salinity
andcurrentobservations,they
determined
themeandischarges
andverticalexchanges
between
thedifferentparts
of the DanishStraits.The findingsarepresented
in chapter11.
Thesedatawereusedasinputto a modelforthenitrogen andoxygen balanceof
thebottomwater.In Figure3.8, the increase in theestimated nitrogenloadingto
thesystemfromthe1950sto the1980sisillustrated. It isnotedthatthecontribu-
tionsfromtheSkagerrak andBalticSeaarenotstatedin Figure3.8. Thisis dueto
thecomplicatedstratification
andcurrentpatterns whichmakethe interpretation
of theloading
figuredifficult.Hansenet al. [1994]conclude thatthenitrogencon-
centration
at theboundary towardtheSkagerrakandhencethecontributionto the
nutrientbalanceof Kattegat
havenotchanged significantly
between the1950sand
the 1980s.The contributionfromthe Skagerrak
is approximately
160,000tonsof
inorganic
nitrogen
peryear.Hansen
et al. [1994]arguethatthecontribution
from
theBalticSeahasincreased
by a factor1.7 betweenthe 1950sandthe 1980s.The
contribution
fromtheBalticSeaduringthe1980sis approximately20,000tonsof
inorganic nitrogenperyear.Dataon phosphorus loadingareinsufficient
to esti-
matechanges overtime.In general,it is advised
to investigate
boththe nitrogen
andthephosphorus loadingaspartof eutrophicationstudies.
Modelresultssuggest
that the significant
increasein nitrogenloadingrelatesdirectlyto the observed
eutrophicationeffectin theDanish
Moller 63
Be •th, m
I
2 -
Sep. 17, 1993 Sep. 11, 1993
17:06
I 07:10
4 -
Oct. 10, 1993

6 -
II :: X12:00
'l i Sep.11,1993
X
o
8
I •, 07:05
10
Oct.
10,1993
. • t % ,,*"=
%. ø%ø % ool
12
%. %øø
%.
14
%% '*'.
% I
16
Sep. 17, 1993
/J
18-
17:05',. -'",
,
20 , Bottom
10 14 1'8 2'2 2'6 3•0 -' -O.4O' o.oo 0.40'
Salinity, psu Current velocity north, mls
Figure3.9. Exampleof salinityandcurrentprofilesat the GreatBeltBridgeon threedays

duringfall 1993. Note the influenceof stratification
on the velocityprofile.Unpublished
data from A/S Storebafitsforbindelsen.
Currentand the Effectsof Stratification

Because of the variablebalancebetweenthe barotropicand the barocliniccompo-
nent,the currentcan be differentin speedand directionfor variousdepths.The
meancurrentin the upperlayeris directedout of the Baltic,whereasthe meancur-
rent in the bottom layer is directedtoward the Baltic.This is due to the general
estuarinecirculation.It should, however,be noted that the instantaneous current
profilemay be entirelydifferentdueto the combined actionof wind,densitygradi-
entsandtidal forcing(seeFigure3.9).
On October10, 1993, the currentprofileis barotropically dominated. The flow is
towardthe Baltic(southward) at all depths.On September 17, 1993,the currentis
toward the Baltic (southward}for the surfacelayer and toward Kattegat(north-
ward)for the bottomlayer.The barotropicpressure gradient,causedby the water
levelbeinghigherin Kattegatthanin theBaltic,forcesthesurface watertowardthe
south,whereasthe baroclinicpressure gradient,whichis causedby a tiltinginter-
facebetweenthetwo layers,balances thebarotropicgradientin thelowerlayerand
forcesthe bottomwaterto flow towardnorth.On September 11, 1993, the situa-
tion is the opposite.
The waterlevelis higherin the Balticthanin the Kattegat,
forcingthesurfacewaterto flow towardnorth,whilethebaroclinic gradientdueto
the salinitybeinglargerin the Kattegatthan furthersouth,togetherwith a tilting
interface,forcesa southwardbottom
Scalingconsiderations
The largevariabilityin currentconditions,stratificationand mixing conditions
bothin timeandin space,hasgreatinfluence on theinterpretationof the eutrophi-
cationmechanisms. The Kattegatmaybeconsidered a two-layersystemon an aver-
age,but whenlookeduponat a time scaleof daysand hours,the systemis more
complicated. It is, therefore,importantto adjustthe timescaleof the hydrographic
investigation to the timescaleof the biologicalproblemin question.If, for exam-
ple, the long-termtrendsin primaryproductionin the southernKattegatare inves-
tigated,it maybe appropriateto pool all data from the southernKattegatfor each
year and analyzeit in combinationwith the averagedhydrographicconditions.If,
on the otherhand,the springphytoplanktonbloom,which developsover a few
days,is examined, the hydrographicprocessesmustbe resolvedat the sameshort-
term scale.The scaleproblemsare associated with intrusionof mixed water, sub-
surface maximaof planktongrowthandthetimescaleof verticalmixing,seee.g.,
Pealersen [1993] and H•jerslev[1985]. In chapter5, examplesof suchshort-term
andlocal-scale problems aredescribed.
Monitoring
The monitoringof marinesystemsmusttakethe hydrographicvariabilityof the

system intoaccount.
Thetimevariationin biological
parametersasillustrated by
thespringbloom,andthetimevariationin the hydrographic
parametersas illus-
tratedbytheintermittence
oftheflowthrough theBelts,showhowthemonitoring
planningmusttake the timevariationinto account.
Monitoringof coastalsystems
is expensive.
It is thereforecrucialto definethe ob-
jectiveof themonitoring programmes beforecommencing the monitoring.Poor
planningcanresult inoversampling (wasteofmoney)or,evenworse, inincomplete
evaluation of questions[NationalResearchCouncil,1990].Modelsof thesystem
variabilityandstructure canassistin planningthe monitoring. As an example,
WulffandRahm[1989]haveusedmodeling to demonstratethatonlya fewwell
chosen stations with a highsamplingrateare necessary
to monitorthe nutrient
conditions in theBalticSea,asopposedto manybutseldomly visitedstations.
Modeling
Whenthephysical
description
of thehydrography
anditsrelation
to thebiological
processes
are considered
quantitatively,mathematicalmodelshave to be used.
Modelsof thehydrographic
processes
andthegeneral
circulation
havelongbeen
usedfor special
purposes,
examples
fromtheDanishStraitsarethe forecastmodel
forcurrents
andwaterlevelbyVested
et al. [1991]andthecirculation
modelby
Stigebrandt
Moller 65
Whenaddressing
the applicability
of modelsin the contextof eutrophication
it
should
bebornin mindthat a numericalmodelis nothingmorethana simplified
theoreticalabstractionof a natural system.Elementsthat are considered
to be im-
portantforthetaskat handareexpressed
in standard
mathematical
terms,andcal-
culations
areperformed by computer.
Numericalmodelsareusedto synthesizein-
formation,answerquestions,
solveproblemsor makedecisions.
Examples of mod-
elsthatcombinethehydrographicandbiological
systems
aregivenin chapter11.
Conclusions
TheDanishStraitsareprobablysomeof the beststudiedregionsof theworld.The

hydrography of the DanishStraitshasbeenstudiedandmonitoredfor morethana
century.The knowledge of the hydrographic
processes andits interaction with bio-
logyhavereacheda stagewherelackof measurements is hardlythereasonfor lack
of progressin science.The futuredevelopment in knowledge of thisinteresting sys-
tem will be achievedthroughthe combineduseof numericalmodeling,remote
sensing and detailedmeasurement programs.As it hasbeenpointedout in thepre-
vioussections, the variabilityandpatchiness
of the biologicalparameters areclose-
ly linkedto the variablehydrographic conditions.Furtherprogress in the fieldof
biologyis thereforecloselylinkedto the understanding of the relationbetweenthe
hydrographic and biologicalprocesses.
Of particularinterestfor future studyis the verticalmixing processes and their
importancefor the planktondynamics.Much hasto be learnedbeforethe combi-
nationof verticaland horizontaltransportprocesses is sufficientlyunderstoodand
reduced to a level that can be modeled.
The monitoringstrategies
haveuntil now beenbasedmainlyon traditionalvessel-
basedcruises.
Thismonitoring methodwill betransformedin thefuturewhenremote
sensing,
automated(on-line)monitoring
andmodelingtoolsbecome morewidespread.
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of theTurkish
straits,in The PhysicalOceanography
of Sea Straits,editedby L. Pratt, pp. 25-60.
Kluwer, Dordrecht,The Netherlands,1990.
Vested,H. J., H. R. Jensen,
H. M. Pedersen,
A.~M.JorgensenandB. Machenhauer,An oper-
ationalhydrographic warningsystemfor theNorth Seaandthe DanishBelts,Continental
ShelfRes.,/2, 65-81, 1992.
Wulff, F., andL. Rahm,Optimisingthe Balticsamplingprogramme: the effectsof usingdif-
ferentstationsin calculationsof total amountof nutrients,Beitr. Meereskunde,Berlin, 60,
61-66, 1989.
Weidemann, H., Untersuchungen
•iberunperiodische
undperiodische
hydrographische
Vor-
g//ngein derBeltsee,
KielerMeeresforsch.,
7, 70-86,
4
Material Flux in the Water Column
Thomas Kiorboe
Introduction
Thereis a continuous exchange of substances

between thepoolsof soluteandpar-
ticulatematerialin the pelagiczone.For example,inorganicsolutenutrientsand
carbondioxideare incorporated intoparticulateorganicmatterby photosynthesis
and are subsequently remineralizedby metabolicprocesses.Otherquantitatively
importantprocesses are summarizedin Figure4.1. Mechanismsof transportof
soluteand particulatesubstances differradically.While both particlesand solutes
may be transportedwith the surroundingwater and undertakeBrownianmove-
ments(thelatteronly importantfor solutemolecules andverysmallparticles,how-
ever)particlesare in additionsubjectto gravityand,in the caseof organisms,may
ß Photosynthesis
ß Assimilation of DOM by heterotrophs
ß Precipitation and coagulation of DOM into colloidal particles
Dinsolved Parttc•ate
matter matter
* Cell lysis
* Exudation and leakage of DOM from cells
*
IExcretion
of
inorganic
solutes
Sloppy feeding
Leakage of solutesfrom fecal pellets
Figure4.1. Exchange
of substance
betweenthe poolsof dissolved
and particulate
matter.
Summaryof quantitativelyimportantprocesses.

Union
68 4. Material Flux in the Water Column
T A BL E 4.1. Mechanisms
of transportof particlesandsolutes
Transportmechanism Solutes Particles
Brownianmotion(diffusion) + Importantfor particles< 1

Advection + +
Gravity - Important
forparticles
> 1 !xmandw. density
> medium
Motility - Importantonlyfor swimmingorganisms
moveactively(Table4.1). This hasseveralimplications for the exchange of sub-

stancebetweenthe variouspoolsin the pelagiczoneand for the distributionof
matter.Oneconsequence is thatsoluteandparticulatematerial,aswell asthe dif-
ferentprocesses associated
with particlesandsolutes,aredifferentlydistributedin
thevertical.Forexample,photosynthesis occursonlyin theeuphoticzonedueto its
dependency on light,whilesedimenting phytoplanktersand organicparticlesto a
largeextentare remineralized belowthe euphoticzone.Stratificationof the water
columnand the verticaldisplacement of theseoxygen-generating and -consuming
processesmaycauseanoxiato developbelowthe pycnocline.
The purposes of thischapterareto
1. describethe differentmechanisms and propertiesof the exchangeof substance
betweenthesoluteandparticulatepoolsin thewatercolumn;
2. describe the differentmechanisms of transportof soluteand particulatematerial
in the pelagiczoneand
3. to discuss the implicationsof the exchangeand transportprocesses for pelagic
food web structureand for the supplyof oxygen-consuming materialto the sea
floor in coastalmarinewaters.ThroughoutthischapterI will useconceptualex-
amples,preferentiallyfrom Danishwaters,to illustratethe discussion. A sub-
sequentchapter(Richardson,chapter5) will provideflux budgetsfor the Kat-
tegatspecifically.
4.2.Exchangeof Substances
between the Dissolved and Particulate Pools
Table4.2 givesan overviewof thetypes,sizesandtypicalconcentrations of parti-

culateorganicmaterialin coastalwaters.The term "particle"is hereusedin its
widestsenseandincludes alsolivingorganisms. Solutes maybetransformed to par-
ticulatematerialby at leastthreedifferentprocesses(Figure4.1): i) uptakeof inor-
ganicnutrientsby phytoplankton and bacterioplankton, ii) uptakeof dissolved or-
ganicmatter,primarilyby heterotrophic microorganisms; andiii) precipitation
and
coagulationof soluteorganics to colloidalparticles.Theseprocesses are discussed
separatelyin the following.The other typesof particleslistedin Table 4.2 are the
resultof trophicinteractions(zooplankton)or physicalprocesses (aggregates).
Organicparticles may be remineralized
to soluteinorganics
by heterotrophs
and
soluteorganics maybeexudedor leakfromlivingcellsor organicparticles.
These
processeswill be dealtwith
Kiorboe 69
TABLE 4.2. Typesandtypicalsizesandconcentrations

of organicparticles
occurring
in
coastal waters
Type Size,cm Typicalconc., Reference

# ml q
Colloids 5 -120 x 10 -7 109 Wells &

Goldberg1991
Vira 5 X 10-6 107 Borsheim1992
Submicron
particles 0.4-0.9 x10 -4 107-108 Longhurst
et al. 1992;
Koike et al. 1990
Bacteria 0.3-1.0 x10 -4 10s-106 Fogg1986

Transparent
exopolymeric
particles
(TEP) 5-50 X 10-4 102-104 Alldredge
et al. 1993
Marinesnow 10-•-10• 10-3-10-2 Alldredge
& Silver1988
Picoalgae 0.2-2 x10 -4 104 Fogg1986
Nanoalgae 2-20 x 10-4 103 "
Microalgae 2-20 X 10-3 102--103 "
Microzooplankton 2-100 • 10-4 10-2-100 "
Mesozooplankton 2-20 x 10-1 10-3-10-4. "
4.3.Conversionof DissolvedInorganicMaterial to Organic:

PrimaryProduction
Primaryproduction of thephytoplankton liesat thebasisof pelagicfoodwebsand
providesthe mostimportantenergyinputfor heterotrophic processesin thewater
columnand on the seafloor. The accumulation of phytoplankton biomassin the
euphoticzoneis limitedby lightduringwinterandin deeplymixedwatercolumns,
butisnormallyassumed to belimitedbytheavailabilityof inorganicnutrients
dur-
ingtheproductive summer season.
Whenthenutrient concentration
islowtheuptake
rateof nutrients(U) by a spherical
phytoplankton celldepends on theconcentra-
tion of nutrientsin the ambientwater (C), the sizeof the cell (characterized
by its
radius,r), themolecular
diffusivity(quantifiedby thediffusion
coefficient,
D) and
ontheadvective transport
of nutrientsto thecellsurface
(characterized
bythedimen-
sionlessSherwood number,Sh)(seee.g.BergandPurcell[1977]for a formalproof):
U = 4•'rDShC (1)
The Sherwood
numberis the ratio of totalnutrienttransportto thecellsurface(by
advection
anddiffusion)
to thetransport by diffusion.
If theadvectivetransportis
zero,Sh= 1, andtheuptakerateisgoverned onlybytherateof moleculardiffusion.
FromEq.1 it followsthatin thediffusion-limited
case(i.e.,Sh= 1)themass(orvol-
ume)specific
uptake
rate(U/cellvolume
= (4•'rDShC)/(4/3•'r
3)= 3DShC/r
2)
Depth, m 0
10
15
20
/ 24
25
30
Chlorophyllfraction>11 IJrn,%
100
80
60
4O
20
0 i i i i [ [ i i i
'""•j
.....'....F "' M A M J J A S O N D
Figure4.2. Seasonalvariationin verticalwatercolumnstructure(a) and sizecomposition of

the phytoplankton (b) in southernKattegat.In the Kattegatverticalwater columnstructure
is determinedmainlyby salinity.Bloomsof phytoplankton occurin association
with the ver-
nal stratification
of the water column(March-April),beginningdeepeningof the upper
mixedlayerin latesummer(August-September), and in late autumn(November-December)
wherethe watercolumnbecomes deeplymixed.Thesebloomsare all dominatedby phyto-
planktonretainedon an 11-1xmscreen,whilecells< 11 !xmcharacterize the phytoplankton
duringsummerstratification.Data from Ki•rboe andNielsen
Kiorboe 71
clineswith the squareof the cellradius.Thus,smallcellsareverymuchmoreeffi-

cientthan largecellsin collectinginorganicnutrientsfrom the environment.For ex-
ample,a 1-1xmcellextractsnutrients100 timesmoreefficientthana 10-1xmcell.
Or moregenerally,picophytoplankton (0.2-2.0 Ixm)are muchmoreefficientthan
nanophytoplankton (2.0-20 Ixm)that,in turn,aremuchmoreefficientthanmicro-
phytoplankton (> 20 Ixm)cellsin thecompetition for inorganicnutrients.
In spiteof this,not all phytoplanktoncellsin theoceanbelongto thesmallest size
class.Empiricalevidence suggests
that microphytoplanktonbloomsanddominates
the phytoplankton biomassin localizedor episodic,nutrient-rich,turbulentenvi-
ronments whileverysmallor motileformsdominatein oligotrophic, stagnantwa-
ters(seeKiorboe[1993] for a review).Turbulentmixingbringsinorganicnutrients
towardthe surfacewhile stratificationretainsthe phytoplankton in the euphotic
zone.Transitionsin time or spacein the verticalwater columnstructureare, there-
fore, indicativeof ephemeralor localizedenhancements of phytoplanktongrowth
conditions,and this is wherethe microphytoplankton bloomsand dominates the
planktonflora. Someexamplesfrom Danishwatersare shownin Figures4.2 and
4.9. Apparently,the competitivedisadvantage of largecell sizeis offsetby other
factorsin someenvironments. One suchfactoris the advectivetransportof nutri-
entsto the cell surface(i.e., Sh > 1). In the diffusion-limited case(i.e.,when the up-
takeof nutrientsacrossthe cell surfaceexceedsthe deliveryby diffusion)a nutrient-
depleted regionaroundthe cellwill be established. If the deliveryof molecules to
thisregionis enhanced by advection, eitherbecause thecellswimsor sinksthrough
the water or because of local fluid velocitygradients(shear,turbulence), thenthe
uptakeratewill increase. Themagnitude of increase isgivenbytheSherwood num-
ber- the Sherwoodnumberis the factorwith whichdiffusiontransportis increased
dueto fluid motion.It is not straightforward to calculatethe Sherwoodnumber
(forexamplesseee.g.LoganandAlldredge[1989],Kiorboe
[1993],MurrayandJack-
son[1993]);it dependson whetherthecellsinks/swims
or is suspended
in a turbu-
lent shearfield and it is a functionof the cell size,the shearrate and the swimming
/sinkingrate.Table4.3 givessomeestimates
of Sherwood
numbers
for differently
TABLE 4.3. Sherwoodnumberscalculated
for settling(Shsett)
and swimming(Shswim)
cells
andforcellssuspended in a turbulentfluidshearfield($htu•)-TheSherwood number isthe
factorbywhichnutrientuptakein cellsisincreased dueto advectivetransport.Calculations
of Sherwood numbers fromequations presented in Kiorboe[1993].Settling
rates(v,cms-1)
calculatedfromcellradius(r, Ixm)asv = 2.48r•'•7[Jackson,1990].Swimming velocity(v,cm
s-•) calculatedfor flagellatesfrom theirequivalent sphericaldiameter(ESD,Ixm)as v =
9.3X10-2ESD 0'26[Sommer 1988].Forcalculation of Sherwood number in a turbulent flow
fielda shearrateof 1 s-• hasbeenassumed; thisisequivalentto theaverageturbulent shear
generatedin a 10-mupper mixedlayerbya windofca.6 ms-• [MacKenzie andLeggett, 1991].
Celldiameter,
Ixm Shsett $hswim $hturb
1 1.007 1.84 1.004
10 1.034 5.41 1.041
100 1.116 23.1 1.4!
1000 11.24 -
sizedcellsthatareswimming, sinkingor subject to fluidmotion.Smallcellsgain

verylittlefrommoving through thewater(swimming, sinking)
or fromfluidmotion
(turbulence),whilethenutrient uptakein largecellsissignificantly
increased.
Thus,
thecompetitive pressureforsmallsizeisrelaxed in a turbulent
environment andfor
swimming cells(flagellates),
andthisisconsistent withtheobserved distributions
of
thevariousforms.However,theeffectof theadvective transportin largecellsis in-
sufficient
to entirelycompensatefor the declining
size-specific
nutrientuptakeby
moleculardiffusionwith increasing
cellsize.
Anotherfactorthat may helpoffsetthe competitive disadvantage of beinglarge
and,thus,explaintheoccurrence of largephytoplankters in episodic,nutrient-rich
environments is predation[Munk and Riley,1952, Geideret al., !986, Kiorboe,
1991]. The growthof phytoplankton cellsis, unlikethe growthof their zooplank-
ton predators,only weaklyrelatedto cell size[e.g., Banse,1982b; Blascoet al.,
1982,NielsenandSand-Jensen, 1990]. Smallphytoplankton cellsare preyedupon
by smallpredators, e.g.heterotrophicnanoflagellates,andthe phytoplankton prey
and theirpredatorshavesimilarpopulationgrowthrates(on the order of hours).
Thus,thepredators of smallphytoplankton cellshavethe capacityto controltheir
phytoplankton prey populations.Largephytoplankton cellsare eaten by larger
metazoans, e.g.copepods, andthesehavegenerationtimesoneto severalordersof
magnitude longerthanthoseof theprey.Thus,thenumerical response in predator
populationsto variationsin phytoplanktonpreypopulation sizeswill beincreasing-
ly delayed
with increasing phytoplanktoncellsize.
Whennutrients areepisodically
injected intotheeuphotic zone,population
sizesof
bothsmallandlargephytoplankton cellswill startto increase.
However,popula-
tionsof smallphytoplankton
cellswill soonbecaughtupbytheirpredators, while
thelargecellsmaycontinue
theirgrowthlargelyunutilized by grazers
untilthein-
organicnutrients
havebeenexhausted. Thismayexplainwhymicrophytoplankton
dominatesandbloomsin episodically
nutrient-enriched environments.
Theinterplay
between
nutrients
andpredators
in controlling
thephytoplankton
bio-
massmayhelpexplainan apparent
paradox.Asnotedabovebiomassaccumulation
inthewatercolumn isnormallyultimatelylimited
bynutrient
availability.
At thesame
timeit appears
thatthegrowth rateof thephytoplankton
israrelylimitedbynutrient
availability;
rather,
thephytoplankton growat rfiaximumrateslimitedonlybythe
availability
oflight[e.g.,Goldman,1987].Thus,phytoplankton biomass isnutrient-
limited
whileitsspecific
growth rateislight-limited.
Anexample of thisapparent
paradoxisprovidedbytheseasonalvariation
innutrient
concentration,
phytoplank-
tonbiomass,specific
growthrateof thephytoplankton,
anddailyirradiancein the
Kattegat
(Figure4.3).Phytoplanktonbiomass
accumulatesprimarily
duringthever-
nalwatercolumn stratification
when theconcentration
ofinorganic
nutrientsishigh,
anddeclines
tolowvalues when thenutrients
havebeen exhausted.
Phytoplankton
growthrate,ontheotherhand,ishighest
during
summer
stratification
whenthenu-
trientconcentration
is belowthedetection
limit,andratherfollowstheseasonal
vari-
ation
inirradiance
and,hence,
availability
oflight.
Nutrient
limitation
ofphytoplank-
tongrowthislikely
tooccur
onlysubsequent
toepisodic
fertilization
ofthe
Kiorboe 73
NO2+ NO3,lag-atI-• 10
8
Phytoplankton
biomass,g C m-2 25
2O
15
10
Phytoplanktongrowth rate, d-• 1.2

1
0.8
0.6
0.4
0.2
Daily irradiance,megajoulem-2 d-• 25
20
15
10
J FMAMJ J ASOND
Figure4.3. Seasonalvariationin the concentrationof inorganicnutrients(NO2 + NO3) in

the uppermixedlayer(a), phytoplankton biomass(b), phytoplankton growthrate (c), and
dailyirradiance(d) in southernKattegat.Phytoplankton biomass depends on the concentra-
tion of inorganicnutrients(notethat the nutrientscaleis logarithmic),whilephytoplankton
growthrate appearsto be independent on nutrientconcentration but to varyin proportion
to irradiance.Phytoplankton biomasswasestimatedfrom depth-integrated chlorophyllby
assuming a chlorophyll:carbon ratio of 50. The phytoplankton growthratewascalculated
asthe estimateddailyprimaryproduction(•4Cincubations) dividedby phytoplankton bio-
mass.Daily irradianceis a standardcurvefor the location.Data from Kiorboeand Olsen
(unpublished) andfrom Richardson andChristoffersen
zone,wherethephytoplankton may"escape" predatorcontrolandexhaustthenutri-

ent source.In oligotrophic waters,largecellsare replacedby smallerformsdueto
competition for nutrientsandtheseare controlledby predation.Hence,nutrientsare
regeneratedat thesamerateastheyarebeingutilizedby thephytoplankton, andthe
turnoverrate is determined by the light-limitedgrowthrate of the phytoplankton.
Becausethe phytoplankton productionrate (primaryproduction)is the productof
biomassandgrowthrateit islimitedby eitherlightand/orinorganicnutrients.
4.4.HeterotrophicUptakeof DissolvedOrganicMatter:
Bacterial Production
Dissolvedorganicmattermay be assimilated by cellsand therebytransformedto

particulateorganicmatter.Uptakeof dissolved organicmatteris, of course,limited
by the samephysical constraints astheuptakeof dissolved inorganics,andthe up-
take rate can,thus,be described by Eq. 1. The concentration of dissolved
organic
matter(DOM) in c9astalregionsis relativelyhigh(typically1-3 mg C l-S),but the
majority(80-90%) is normallyconsidered to be veryrefractoryand to havelong
turnovertimes[Sondergaard and Middelboe,1995]. It shouldalso be notedthat the
dissolved fractionis operationally definedasmaterialpassingan 0.2-1xmfilter and
someof the "solute"DOM mayin factbeparticulateandoccurascolloidalor sub-
micronparticles(seebelow);recentestimatessuggestthat > 10% [Koike et al.,
1990], > 30% [Benneret al., 1992] or about16% [Kepkayet al., 1993] of the ma-
terial passingan 0.2~lxmfilter is particulate.Thus, the concentrationof small or-
ganicmolecules thatcanbeassimilated by cellsis low, evenin coastalregions,and
approximately equivalentto thecarbonbiomass of pelagicbacteria.Becauseof that
anddueto theconstraints impliedby Eq.1, onlyverysmallcellscanefficiently uti-
lize the sourceof dissolved
organics.
Heterotrophic
bacteriadominatethe pico-
planktonandare,consequently,
the mainconsumers
of DOM.
The quantitative importance of bacterialproductionasa sourceof particulatema-
terialin coastalregionsis significant.
Particleproductiondueto bacterialassimila-
tion andutilizationof DOM equalson the averagesome30% of the particulate
primaryproduction [Coleet al., 1988].In somecases bacterial
production
mayap-
proachor evenexceedtheprimaryproduction [e.g.,Borsheim,
1992].
Takingintoconsideration thefactthatall dissolved organics ultimatelystemfrom
phytoplankton productionin a pelagicfoodwebwithoutexternalinputandgiven
thegrowthyieldof pelagic bacteria(0.1-0.6[B•rsheim, 1992]),it mayat firstap-
pearparadoxical thatbacterialassimilationis sohighrelativeto primarsrproduc-
tion. It is a frequentmisunderstanding, however,that heterotrophic assimilation
andsecondary production(i.e.,thesumof production of all heterotrophicorgan-
isms)in a closedsystem cannotexceedthe primaryproduction[Strayer,1988].
Thiscaneasilyoccurif the organicmatterpasses severalconsumers beforeeventu-
allybeingrespired. Notethattheenergetic constraint
is thattotalrespiration can-
notexceed primaryproduction. Thus,a highratioof bacterial to primaryproduc-
tionimplies thatdissolved
organics aretakenup andexcreted by bacteria-or
Ki•rboe 75
terialpredators- severaltimes;i.e., that DOM is recycledseveraltimes.This is

likelyto bethecasealsoin neriticwaters,eventhough allochtonous
organic matter
fromriverrunoffmaycontribute to bacterial
production.In coastal
waters,theflux
of labileterrigenous
organic mattercorresponds to onlya fewpercentof theprima-
ry production;
evenin estuarine
watersterrigenous
organicmatterfluxis < 20% of
theprimaryproduction[SmithandHo!libaugh,1993].
4.5.Precipitationand Coagulation
of DissolvedOrganicMaterial
Anotherpotentiallyimportant but as yet incompletely understoodmechanism
of particleformationfrom solutesubstances is by physico-chemical processes.
Recently,Wells and Goldberg[1991] described the occurrence of small(5-120 nm)
colloidalparticlesin highconcentrations (--! 09ml-•) in watersoff California(Table
4.2}. The organicnatureand the verticalstratificationof theseparticlessuggest
themto be of bioticorigin,althoughtheirmodeof formationis uncertain.Koikeet
al. [1990] and Longhurstet al. [1992] found concentrations on the order of
107-108ml-• of organicsubmicrometer particles(0.4-1.0 Ixm)in surface watersof
the north Pacificand off Nova Scotia,respectively. This sizerangewouldinclude
bacteriaandpicophytoplankton, but theseorganisms contributed < 5% of thepar-
ticlesand the majority were, thus, nonliving[Koikeet al., 1990]. One potential
modeof formationof submicrometer particlesis by nanoflagellate-bacterial inter-
action [Koike et al., 1990]. Finally, Alldredgeet al. [1993] discovered significant
concentrations (up to 5000 ml-•) of larger(2-100 •m) transparent exopolymeric
particles(TEP) in surfacewatersoff California.Evenlargermucusparticles,or ag-
gregates consisting of mucusand solidparticles,severaltensof cm in diameter,
havebeendescribedfrom the Adriatic [Stachowitsch et al., 1990]. Boththe parti-
clesof TEP and the giantmucusparticlesin the Adriaticcanbe formedfrompoly~
mericmaterialexudedby diatoms[Stachowitsch et al., 1990;Ki•rboeandHansen,
1993, Passowet al., 1994], bacteria,and from macrophyteleachates[Alber and
Valiela, 1994]. Alldredgeet al. [1993] hypothesized that colloidalparticlesform
fromexopolymeric solutesby cationbridgingof 3-10 nm microfibrils, that these
furthercoagulate or otherwise coalesce to colloidalparticles, ashasbeendescribed
in freshwater[Jensen andS•ndergaard, 1982],andsubsequently to thelargerpar-
ticlesof TEP.Thus,particulate materialmayformdirectlyfromDOM by physico-
chemical processes,andtheconcentrations recorded for thesevarious
typesof or-
ganicparticles(Table4.2) suggest thatthismaybea majorpathwayfromsolutes
to particles.
Thesedifferenttypesof recently discovered organicparticlesmayhave
importantimplications for transportprocesses in the plankton;theymay act as
sorptionsitesfor solutes[Moral andGschwend, 1987;WellsandGoldberg, 1991]
andattachment sitesfor bacteria[Alldredge et al., 1993;AlberandValiela,1994],
serveasfoodfor particlegrazers[Shimeta, 1993],andcoagulate withotherparti-
cles,includingphytoplankton [Passow et al., 1994;Ki•rboeandHansen,1993],
intomarinesnowaggregates andthusenhance theverticaltransportof substances
by sedimentation
(see
4.6.The Transformation of Particulate to Dissolved Matter
Matter boundin suspended particlesmaybetransformed to the solutestate,either

in theformof inorganicions,or in theformof dissolved organicmatter.The gener-
ation of inorganicnutrientsis the inescapable resultof metabolicprocesses, by
which organicsubstances are oxidizedto their low-energyinorganiccomponents.
Thesewill be excretedto the environment by the heterotrophicorganisms. Scaling
arguments suggest
that,on average,themajorityof the remineralization will be due
to verysmallorganisms: because the biomass of planktonicorganisms is on average
approximately constantin equal,logarithmicsizeclasses [Sheldonet al., 1972], and
because theweight-specific
metabolicrateof organisms declines
with the bodymass
raisedto an exponentof ca. -0.25 [e.g.,Banse1982a], organismssmallerthan 100
Ixmaccountfor > 90% of total pelagicremineralization.
Due to the significanceof smallorganisms and becausesmall particlessink very
slowly(seebelow),the majorityof the organicmatterproducedin the euphotic
zonewill be remineralized within the zoneif the particlesizedistributionfits the
equilibriumSheldon-distribution.
However,if the sizedistributionis pertubatedto-
wardlargerparticlesizesdue,for example,to nutrientenrichment and/oraggrega-
tion of particles(seebelow)sedimentation of particulatematerialmay displacea
significant
fractionof theremineralizationprocess to belowthe pycnocline.
Dissolvedorganiccompounds areexcreted or lostdirectlyor indirectlyfromorgan-
ismsand ultimatelystemprimarily from the phytoplankton;river runoff con-
tributesonlylittle additionalorganicmatter,evenin coastalwaters(cf. above).The
"demand"for dissolved organicmatterin the watercolumnis high.The require-
mentsfor bacterialuptakeof DOM andfor the formationof colloidaland larger
nonlivingorganic particles
directlyfromDOM together mayexceedthepelagicpri-
mary production.Bacterialproductionaverages30% of primary productionin
aquaticenvironments [Coleet al., 1988]. With an assumed growthefficiencyof
40% [Bj•rnsen andKuparinen, 1991],bacteriawouldaloneon average requirethe
equivalenceof 75% of theprimaryproduction asDOM. We haveno quantitative
estimatesof the turnoverrate of colloidalorganicmaterial.However,carboncon-
centrationsof suchparticles are similarto carbonconcentrations of the phyto-
plankton
(ontheorderof 100IxgC 1-•, Well•andGoldberg,
1991)andtheoretical
[Shimeta,1993] aswell as experimental studies[e.g.,Gonzfilezand Suttle,1993;
Tranviket al., 1993;MarchantandScott,1993]suggest thattheseparticlesarein-
gestedby nanoflagellates
at highrates.It followsthat the turnoverof colloidalor-
ganicparticles and,hence,the demandfor DOM is relativelyhigh.Sincemost
DOM in thewatercolumnultimatelystemsfrom photosynthetic carbonfixation,
theseconsiderationssuggestthatrecycling of organicmatteris quantitativelyvery
important.
Thisconclusion
is furthersubstantiated
by the factthat directexudationof DOM
from phytoplanktoncellsis presumably
small.While the olderestimates of DOM
leakagesuggested
that up to > 70% the primaryproductioncan be lostin
Ki•rboe 77
form [e.g.,Fogg,1983], morerecentestimates

suggest
that realisticexudationrates
areratheron theorderof 10% of primaryproduction
[Baines
andPace,1990],or
lower (seeJumarset al. [1989]). The lower estimatesare also consistentwith the
theoretical
considerations
of Bjornsen[1988].Bjornsensuggested
thatexudation
of
DOM fromhealthyphytoplankton is dueprimarilyto passive
diffusion
across
the
permeablecellmembrane.
Accordingly, theexudationratedependsonthecellsur-
facearea.Bjornsen's
modelcombined withrealistic
assumptionsof phytoplankton
cellmembranepermeabilities
leadsto phytoplankton
exudationratesthat are com-
parablewith thosemeasured experimentally, i.e., 1-10% of theprimaryproduc-
tion (seealsoKiorboe[1993]).However,because theexudationratedepends on
thecellsurfacearea,andbecause bacterialcellsurface areaperunitvolumeof sea
water exceedsthe cell surfacearea of all otherorganisms combined[Williams,
1981],theseconsiderationswouldalsosuggest thatleakage of DOM frombacteria
wouldbean importantsourceof dissolved organicmatter.Thus,a significant
frac-
tion of organicmatterrecyclingin the water columnmayoccurwithinthe micro-
bial community.
Jumarset al. [1989] likewisemaintainedthat recycled DOM is a moreimportant
sourcethandirectleakagefrom phytoplankton cells.Theseauthorsemphasized the
importance of inefficientgrazingand digestion: DOM may resultfrom "sloppy
feeding",i.e., spillageof dissolved
compounds from break-upof phytoplankton
cellsduringthe digestionprocess,or from leakageof sol.•tesfromfecalpellets.By
simplediffusion-advection models,theyshowedthat solutescontainedin fecalpel-
letswouldbe rapidlyleakedto the environmentand,thus,remainin thewater col-
umnratherthan fallingout with the pelletitself.Jumarset al. [1989] estimated
that
thesepathwayscouldaccountfor a DOM flux equivalentto 20-70% of the prima-
ry production,severalfold higherthanthe leakagerate of DOM directlyfrom phy-
toplanktoncells(seealsoBainesandPace[1990]).
4.7.Mechanisms
of Transportof SoluteInorganicNutrients
The foregoingdiscussion of exchange processes betweenthe soluteandparticulate
poolsof materialin the watercolumnhasalsoconsidered small-scale diffusion-ad-
vectiontransportof solutes; i.e., transportin and out of particles.I will now con-
siderthe larger-scale
processes and focuson the transportof inorganicnutrients:
What are the sources of inorganicnutrients,and how are theytransported to the
euphoticzonewheretheycan beutilizedby thephytoplankton?
Therearetwo primarysources of inorganic
nutrientsfor primaryproductionin the
euphoticzone, viz. "new" and "regenerated" nutrients[Dugdaleand Goering,
1967].Regenerated nutrientsaredueto remineralizationof organicmaterialin the
euphoticzonewhilenewnutrientsaretransported to the euphoticzonefromelse-
where.New nutrients maybe transported to theeuphotic zoneby variousmech-
anisms;
viz.by atmospheric transportandsubsequent dryor wetdeposition onthe
seasurface (e.g.LarsenandAssam,chapter2, thisvolume),landrunoff(Moller,
chapter3, thisvolume),upwelling,verticalmixing,entrainment acrossthe
Spring tide
Warm
a Tidal front
Wind parallel to coast
Warm
b Upwelling
Cold
Warm
c Wind-generated
mixing
Cold
Figure4.4. Schematic of varioushydrodynamic processesthat may enrichthe euphoticzone

•vith inorganicnutrients.Intensityof hatchingfrom white to grey indicatevariation from
cold nutrient-richto warm nutrient-poorwater. a: The positionof a tidal front varies•vith
the neap-springtidal cycle.Thus,in a fortnightlycyclecold nutrient-richwater stratifies,and
phytoplanktonis •ithheld in the euphoticzone,•vherethey bloom. b: Alongshorewinds
causedeep,nutrient-richwater to ascendnearthe coast.When the up,veiledwater stratifies,
the phytoplankton will bloom.c: Episodicwind eventsmaycausea temporarydeepening of
the uppermixedlayerand, thus,m•xingof nutrient-richcold •vaterinto the nutrient-poor
surfacelayer;thiswill causethe phytoplanktonto bloom.
cline, cross-frontaladvectionof barocliniceddies,etc. Several hydrodynamic

processes of nutrientenrichment
of the euphoticzonehavebeenschematically de-
pictedin Figure4.4. While atmosphericdepositionof inorganicions, diffusionof
nutrientsacrossthe pycnocline
aswell aslocalremineralization
of nutrientsmay be
more or lesscontinuousprocesses, most hydromechanical processes give rise
Kiorboe 79
episodicinjections
of nutrients
intotheeuphotic zone.For example, windevents
maytemporarily deepentheuppermixedlayerof thewatercolumn,andthusmake
nutrientsimmediatelybelowthepycnocline available
to surface
populationsof the
phytoplankton.Likewise,theintensity
of coastal
upwelling dependsonthestrength
of alongshore
windsandis,therefore,episodic.
Also,entrainmentof deep,nutrient-
richwaterinto the uppermixedlayeris drivenby velocitydifferences betweenthe
two layers,andthiswill dependon the intensityof thetidalor wind-generated cur-
rents.Horizontalexcursion of tidal frontswill followthe neap-spring
tidal cycle
and depends alsoon the wind intensity.Thus,winds,and currentsgenerated by
winds,maycauseepisodic injectionsof nutrientsintotheeuphoticzone.
As notedabovethe levelof phytoplankton
biomass
is typicallydirectlydependent
on the availabilityof inorganicnutrients.However,the time scaleof the nutrient-
enrichment processes hasimplicationsfor the sizecomposition of the developing
phytoplankton community. If the nutrientsupply(whethernewor regenerated} is
continuous,a phytoplanktoncommunitydominatedby smallformsis expectedto
develop,while episodicavailabilitywill lead to dominanceof largerforms.The
largerformswill typicallybloomat suchspario-temporal oceanographic "singulari-
ties" [Legendreand Le F•vre, 1989] wherenutrientsare episodically available.As
discussed above,this is mainlydue to the differentcapabilityof the predatorsof
largeandsmallphytoplankton cellsto controlthepopulation
sizesof theirprey.
4.8.Mechanismsof Transport
of SuspendedParticulateMatter
Suspended particlesmaymovewith thesurrounding waterandsettlebygravity.In
thissectionwe shallin particularconsider
theverticalflux of particulate
material.
Sedimentation of organicparticulatematerialmay relocatethe oxygen-consuming
degradation of particulateorganicmaterial(POM) from the euphoticzoneto
belowthepycnocline. If thesedimentationof POM, measured in reductionequiva-
lents,exceedsthe downwardmixingandentrainment of oxygen,anoxiawill even-
tuallydevelop.The amountof sedimenting POM depends, of course,on thebio-
massof suspended
POM which,in turn,depends
on theavailability
of inorganic
nutrients.
However,if theresidence
timeof suspended
POM in theeuphotic
zoneis
long,theorganic particles
maybeeatenor otherwise degraded in theuppermixed
layer.Theverticalfluxof particulate
material,therefore,alsodepends onthesink-
ingvelocityof suspended POM and,thus,on theprocesses thataffects
sinking
velocity.
I shallconsider
theseprocessesin somedetailin thefollowing.
Thefallvelocity(v) of a suspended
particle
depends
onitsexcess
density(p- p')
andonthegravitational acceleration
(g)on onehandandonthefrictional
resis-
tanceof thewaterontheother;thelatteris a function
of thesizeof theparticleand
oftheviscosity
(rt) ofthewater.Thefallvelocity
of a spherical
particle
of radius,
r,
is described
by Stokes'law:
v = % gr2(p- p')rl-•
TABLE 4.4.Settling velocitiesforspherical

phytoplankton cellsof differentsizes
calculated
fromStokes' law.In (1) a constantdifferential
celldensity
of 0.05g cm-3 hasbeenassumed;
i.ev = 1091r2cms-•. In (2) thedeclining
celldensity
withincreasing cellsizehasbeentaken
intoaccount;
i.e.,v = 2.48r•'•7cms-• [Jackson,
1990].FromKi•rboe[1990].
Settling
velocity,m d-•
Cell diameter,•m (1) (2)
1 2.36 x10 -3 1.99 x10 -2

10 2.36 x10 -• 2.94 x10 -•
100 2.36 x10 • 4.35 x10 ø
1000 2.36 x103 6.44 x10 •
In Table4.4 Stokes'settlingvelocities
for four sizecategories
of sphericalphyto-
planktonhavebeencalculated; cellssmallerthanca. 100 •m in diametersinkin-
significantly,
whilelargercellssediment rapidlyout of theuppermixedlayer.
Observed densityandsizedistributions of suspended particlesare frequentlyinsuf-
ficientto accountfor the observedverticalflux of particulatematter. For example,
sinkingof phytoplankton subsequentto bloomsmay exceedthe predictedStokes'
settling
velocityby ordersof magnitude
[e.g.,$metacek, 1985].Two examples from
Danishwatersmay serveto illustratethis (I shallsubsequently
returnto theseex-
amples):
1. During an early springbloom of the diatom Skeletonemacostatumin the
Kattegat,Olesen[1993] observedthe cellsto sinkwith velocitiesof up to near4
m d-•. S.costatumcellsmeasureapproximately 5 Ixmin diameter;thus,accord-
ing to Table 4.4, they are expectedto sink 1-2 ordersof magnitudeslower.
However, S. costatumis chain-formingand possesses spines,and this may
changeits fall velocity.It is thereforemore relevantto comparethe observed
sinkingvelocityto experimentaldeterminations of S. costatumfall velocities;
theserangebetween0.1-1.4 m d-• [Smayda andBoleyn,1966; Riebesell,1989].
The sinkingvelocityof $. costatumobservedin the Kattegatand elsewhere(e.g.
40-50 m d-• duringa springbloomin the Baltic,[yonBodungenet al., 1981]),
thus,significantlyexceeds thosedetermined experimentally.
2. Throughout summerin theKattegat,OlesertandLundsgaard [1994] founda rela-
tivelyhighand nearlyconstantsedimentation of particulateorganicmaterialto
theseafloor,ca.300 mgC m-2 d-•. Sincetheconcentration of organicparticles,
excluding zooplankton, is alsorelativelyconstantandon the orderof 150 mg C
m-3 duringthe sameperiod,an average sinkingvelocityof suspended organic
particlesof ca. (300 mgC m-2 d-•)/(150mgC m-3)= 2 m d-• canbecalculated.
Duringsummerthe phytoplankton communityis dominatedby nanoflagellates
[Thomsen,1992] and the sizedistributionof suspended particlesobtainedby
electronic particlecountershowsthat themajorityof theparticle-biomass in the
sizerange2-200 Ixmis in particles< 10 Ixm(ownobservation). Suchsmallpar-
ticleswill sink< 0.25 m d-•. Thus,hereagainwe finda significant differencebe-
tweenexpected fall velocityandbulkPOM settling
Kiorboe 81
Thereason for thesediscrepancies between observedandexpected settling

veloci-
tiesisthatsuspended particles mayaggregateintolarge(mm-to cm-size), rapidly
sinking"marinesnow"particles. Whensmallparticles combine intolargeraggre-
gates,theirfall velocity
will increase
accordingto Stokes'
law.Marinesnowaggre-
gatestypicallyconsist of inorganic particles,
detritalorganicparticles,biological
particles
(e.g.mucus-feeding webs,molts,fecalpellets)
aswellasmicroorganisms
JAildredgeandSilver,1988].Marinesnowaggregates arefragileanddisintegrateto
primaryparticles whensampled bytraditional
means (nets,pumps, watersamplers).
The existenceof occasionallysignificantconcentrations
of marinesnowhasbeen
acknowledged for sometime [SuzukiandKato, 1953,Alldredge andSilver,1988]
andit is now generallybelievedthat the downwardflux of particulate
materialin
theoceanoccursmainlyin the formof suchaggregates [FowlerandKnauer,1986].
Aggregate
formationof suspended
particlesmay occurby physical
coagulation.
Thisis a processby whichsuspended particlescollidedueto fluidshearor differen-
tial settlingvelocitiesand stick togetherupon collision[e.g., McCave, 1984;
Jacksonand Lochmann,1993]. The coagulationrate dependon the collisionrate
betweensuspended particlesand on their "stickiness"(= probabilityof adhesion
uponcollision).The collisionrate of sphericalparticles,in turn, is proportional
to
the particlesizecubed,to the particleconcentration squaredandto the turbulent
shearrate (thusignoringBrownianmotionand differentialsettlingasmechanisms
of particlesencounter;theseare insignificantfor particles.>! ixmand in shallow
water, respectively[McCave, 1984; Kizrboe et al., 1994]).
Stickyparticlessuspended in a fluid shearfieldwill coagulate;
asparticlescombine
the concentrationof particleswill decline,and the averageparticlesizewill in-
crease.Classicalcoagulationtheorypredictsthat thedecrease in particleconcentra-
tion and the increasein averageparticlesizeovertime will both be approximately
exponential[Kiorboeet al., 1990a]. Figure4.5 providesa laboratorydemonstra-
tion, that phytoplanktersmay be stickyand that aggregate formationproceeds as
Particle concentration,ml-• Averageparticle
volume,•Jm
3
10 6 -
300
100
10 5 50
0 2'0 4'0 6'0 8'0160120140160 0 2'04'0'"•'08'0'i6o•'b•o •o
Time, min. Time, min.
Figure4.5. Cellsof the diatomSkeletonerna costatum will form aggregatesby physical

coagulationwhensuspended in a shearfield.Dueto coagulation theconcentrationof sus-
pended particles
will decline
approximately exponential(a)andtheaverage volume of par-
ticleaggregates
will increase
exponentially(b).In thepresent
example cellsweresuspendedin
a laminarfluid shearfieldof 3 s-• at a concentration
of 50
82 4. MaterialFluxin theWaterColumn
Cells m!-•
Sinkingvelocity,
m d-4 (chlorophyll) Critical concentration
3.5 105-
a a
Skeletonema costatum
3.0
104-
2.5
2.0 103
Lepocylindrus •
danicus
1.5
1.0
10 2
Thalassiosira
spp.•,, v
0.5 10 4
0 ! • , •'"'i [ • [ [ ! , ] ! •' t""'-•! [ , • • i",",
10 o
Sedimentation
rateofaggregates,
cm3m-2d-1
103
10 -1
102
10 -2 I '1 I I I I I I I I I I j "'1 '1 I I '1 I I I I I I I I I I
24 1 5 10 15 20
February March
101
..:...:...:
10 o
10-• .....................
Flocculationpotential, arbitrary scale

10 -2
Maximum concentration, cells ml -•
105
104
103
b
Skeletonetna
/' ^ Lepocy#'ndrus
102 / • danicus
10-3-
10 4 // D Rh'.
•zos,
ole,
ala sis
niahebetata
, spp.
10-•*
10 0 v Coscinodiscus concinnus
f.semispina
10-s
10 -•
10-2
10-6
2'4
.....i'''•....1'0'
'"'"i"5'""'""
February March
10 -2 10 -• 10 ø 10 •i 102 i 103
Critical concentration, cells ml-•
i 1 '••)......
i.....
105
Figure4.6. Comparisonof observed Figure4.7. Developmentof populationsizesof

sinkingvelocityof suspended particles fivediatomspeciesduringa three-weekperiod
(a) and sedimentationrate of aggre- in a shallowDanishFjord (Isefjord).(a).Popu-
gates(b)with particleflocculationpre- lationsof all speciesinitially increaseexponen-
dicted from coagulationtheory and tiallywith similarpopulationgrowthratesand,
measured particlestickiness
andin situ subsequently, stabilizeat species-specificcon-
turbulentdissipation rates(c}duringa centrations.Theseequilibriumconcentrations
three-weekperiodin a shallowDanish are well predictedby coagulationtheory (b).
fjord (Isefjord).From Kiorboe et al. The line in (b) is x = 3'. From Kiorboeet al.
[1994].
Kiorboe 83
predictedby classical coagulation

theory.Many marinesuspendedparticlesare
sticky,includingmineralparticles[Edzwaldet al., 1974;Leussen,
1988],TEP
[Passow et al., 1994;Ki•rboeandHansen,1993]andmostdiatoms[Ki•rboeet al.,
1990a;KiorboeandHansen;1993, Loganet al., 1994;Drapeauet al., 1994].
Thus,coagulationis potentiallyimportantfor thesedimentation
of POM.
Figure 4.6 providesa fielddemonstration,thataggregateformation bycoagulation
canin factaccountfor observed patternsin sinkingof particulate
matter[Ki•rboe
et al., 1994].In a shallowDanishfjord(Isefjord)a predictorof coagulation
(based
onmeasured concentrations andstickinessof suspendedparticles
andon turbulent
fluidshearratescalculated from windvelocities)mimicked verywelltheobserved
temporalpatternin particlesinkingduringa three-week period.Thiswasfurther
verifiedby the observedtemporalpatternin occurrence
and sedimentation
rate of
aggregated particles(Figure4.6c). Thus,coagulation
appears
to beresponsible
for
aggregation of suspended particlesandan importantdeterminant
of sedimentation
of particulate
materialin coastalwaters.
Jackson[1990] combinedclassical coagulationtheorywith phytoplankton growth
dynamics and showedthat at a certaincriticalphytoplankton concentration,
Ccr,
cellgrowthandcoagulation(andsedimentation) will balance,providedcellgrowth
doesnot becomenutrient-limited.An estimateof Ccris givenby:
Ccr-- 0.384/a(ce9'd3)
-1 (3)
where/a is the phytoplanktonnet growthrate in the absenceof coagulation, c•is

the stickiness,d the cell diameterand 3'the fluid shearrate. Thus,coagulationmay
alsoinfluencethe populationdynamicsof the phytoplankton by puttingan upper
limit to cell concentrations. The development of the populationsof five diatom
species in the shallowDanishfjord (wherenutrientsdid not become limitingfor
biomassaccumulation)during a springphytoplanktonbloom is consistent with
Jackson's criticalconcentration model:initiallythepopulations growexponentially
and subsequently they stabilizeat species-specific concentrations(Figure4.7a).
Also,theobserved maximumcellconcentrations of thesefivespecieswereaccurate-
ly predicted by thecriticalconcentration model(Figure4.7 b}.
In thelightof coagulation
theoryletusnowreconsider
thetwoaboveKattegatex-
amples wherewefounda discrepancy between
observed
andexpected
settling
rates
of particulatematerial:
TheSkeletonetna
costaturn
bloomdescribed
by Olesen[1993]culminated
withcell
concentration
of ca.104cellsm1-1,
whereupon
thecellsaggregated
andrapidlyset-
tledout;a significant fractionof thecellscollectedin sediment
trapsoccurred as
aggregates. How doesthiscompare to the "criticalconcentration" modelof
Jackson? Fromthedevelopment of thephytoplankton population
[Olesen, 1993]
(Figure4.3)wecanestimate aninitialnetpopulation growthrate(/z) of 0.06d-a
(= 6.9.10-7 s-l). The wind velocityduringthe peakand declineof the bloom
(February 20-28)averaged 6.5m s-• (observationsfromtheDanish Meteorological
Institute),
andsucha windvelocity givesriseto anaverage turbulent
shearrate(9')
intheupper10m mixedlayerofca.I s-• (calculated fromthemodel presented
MacKenzie
andLeggett,
1993).
Withalength
(d)ofS.costaturn
cells
of7 x10-4cm
anda cellstickiness
(c•)of 0.1 [Kiorboeet al., 1990a]we cancalculate
a critical
concentration
(Ccr)of 7.7)<103cellsml-• byinsertingthesevalues
in Eq.3. Thisis
closeto the observedmaximumcell concentration,
104 ml-•, and coagulationthe-
ory,thus,appears
capable
of explaining
theobserved
aggregation
andsedimenta-
tion of the bloom.
in thesecondexample consideredabovethehigher thanexpectedsinking

velocity
of suspendedorganic
particles
duringsummer in theKattegat
isalsodueto aggre-
gation.OlesenandLundsgaard [1994]foundthemajorityoftheparticulate
material
collected
in sediment
trapsto occuraslarge,amorphous aggregates.
However,be-
cause aggregation
bycoagulation dependsontheparticle concentration
squared,
coagulationisnotimmediately consistent
withtherelativelyloworganic particle
concentration
encountered
in the surfacewatersof the Kattegatduring summer:
100-150mgC m-3(excl.zooplankton)
or 1-1.5ppm.Thevolume fractionof sus-
pendedparticles
maybemuchgreater thanmeasured microscopically
or withan
electronic
particle
counter
becausetheparticles
of TEP(transparent
exopolymeric
particles)
cannotbevisualized
in themicroscope unless
stained
[Alldredgeet al.,
1993]andcannotbesensed byanelectronicparticlecounter[KiorboeandHansen,
1993].Fromtheconcentrations andaveragediameters of TEPin surface watersof
theSantaBarbaraChannelandMontereyBay(California)reportedby Alldredge et
al. [1993]onecancalculate
thatthevolumefractionof suspended TEPhereranges
between 0.1-400 ppm.Although we do not knowto whatextenttheseobserva-
tionscanbeextrapolatedto othercoastalareas,includingtheKattegat,theysug-
gestthatparticlevolumeconcentrations
maybeverymuchhigherthanmeasured
bytraditionaltechniques.
Andparticlecoagulation maybemuchmoreimportant
thananticipatedfromtheconcentrationandsizedistributionof "traditional"
par-
ticles.This remainsto be closerexaminedin the Kattegatand elsewhere,but may
reconcile
the observed
aggregation and sedimentation
of POM throughoutthe
oligotrophic
summer periodin theKattegat
withclassical
coagulation
theory.
4.9.MaterialFlux andPelagicFoodWeb Structure

in Coastal Waters
Because smallorganicparticles do not sinksignificantly,

and because POM does
not accumulate in the watercolumn,smallorganicparticlesare boundto be min-
eralizedmainlyin thepelagiczone.Smallcellsandparticlesare eatenby smallhe-
terotrophs, e.g.bacteriaandpicoalgae by heterotrophicnanoflagellates.These,in
turn, areeatenby, for example,ciliates,that are eatenby copepods that areeventu-
ally eatenbyconsumers at highertrophiclevels.Becausethereis a considerableres-
piratoryenergylossat eachtrophiclevel,the majorityof the primaryproduction
due to smallcellsis remineralizedby microorganisms in this so-calledmicrobial
loop,andonlylittleenergyreaches highertrophiclevels.Normally,smallcellsdo
not bloom,i.e., occurin very high biomassconcentrations, becausepredatorcon-
trol is efficient.Exceptions are bloomsof smalltoxicphytoplankters that may
Kiorboe 85
capepredationcontrolby chemical defense,

e.g.the bloomof thetoxichapto-
phycean
flagellate
Chrysochromulina polylepis
thatoccurredin theKattegat during
June1988[Nielsenet al., 1990].However,
smallphytoplankton cellsrarelyoccur
in concentrations
sufficientfor coagulationand, hence,sedimentation
to become
important. Thereforethemicrobialloopis characteristicof regeneratingsystems
whereinorganicnutrientsare efficientlyrecycledin the euphoticzone.Thereis a
highdegree of predatorcontrolin microbial
communities; for example,population
sizesof picoalgae and bacteriaare controlled
by theirnanoflagellate grazers(cf.
aboveandAndersen andFenchel[1985]),andtheciliatecommunity in theKattegat
is rarelyif everfood-limitedbut ratherlimitedefficientlyby copepod predation
[Nielsenand Kiorboe,1991, 1994]. In the longrun, however,the turnoverrate in
the regenerative microbialloop food websappearsto be governed by the light-
limitedgrowthrate of thephytoplankton.
Microbiallydominated
planktoncommunities arenotalwaysandexclusively based
on regenerated
production.In the Kattegatand the nearbySkagerrak,as well as
elsewhere,the pycnoclineis characterizedby significantconcentrations of auto-
trophicnanoflagellates duringsummerstratification[Nielsenet al., 1990;Bjornsen
et al., 1993]. A significantfractionof the watercolumnprimaryproductionis due
to thesesubsurface populations, e.g.ca. 30% of the annualprimaryproductionin
theKattegat[Richardson and Christoffersen,1991],andtheyapparently dependto
a large extent on new, entrained nutrients [Bjornsen'et al., 1993; Olesenand
Lundsgaard,1994]. As neitherPOM nor remineralized nutrientsaccumulate here,
theremustbe a downwardflux of matterthat equalsthe entrainmentof new nutri-
ent. Both in the Kattegatand Skagerraksucha downwardflux has accordingly
beenobserved[Bjornsenet al., 1993; Olesenand Lundsgaard,1994], and in the
Kattegatthe flux rate fitswell with independent estimatesof the rateat whichnew
nutrientsare entrainedacrossthe pycnocline[Olesenand Lundsgaard,1994]. This
sedimentation may be facilitatedby packagingof smallparticlesinto largerfecal
pellets.Sedimentation of smallcellsmay alsooccurif the concentration of other
stickyhydrosols,e.g.the particlesof TEP, are sufficiently
highfor coagulation
to
occurat significantrates.In the Kattegatthisis a likelymechanismby whichnew
inorganicnutrientscontinuously entrainedfrom belowthe euphoticzoneor de-
positedfrom the atmosphere againleavethe euphoticzone,because sedimented
materialis characterized
by aggregated particles(cf.above).
4.0. The ClassicalFoodChain:GrazingversusSedimentation

Largephytoplankton cellsbloomin springandsubsequent
to episodic
nutrienten-
richmentsof the euphoticzonebecausetheirpredators
areinsufficient
in control-
lingtheirpopulationsizes.The primaryproductiondueto largephytoplankton
cellsfuel the so-calledclassicalfood chain:somefractionof the phytoplanktonis
consumed directlyby mesozooplanktersandthusmadeavailable to consumers
at
highertrophiclevels.In theKattegatandin theSkagerrak
theproductionof cope-
podsdepends directlyontheconcentration andproduction
of microalgae
Integrated
chlorophyll,
mgm-2
35O
a
30O
25O
20O
150
100
5O
Benthicbiomass,g 0.1 m-2

b
75
5O
25 e ß
;
• ee
ß
0 ß ,,
, i
56ø00 57'ø00 58ø00 59ø00

Latitude, øN
Figure4.8. Depth-integrated
chlorophyllbiomassacrossthe Kattegat/Skagerrak front as
measured duringsevencruises
(a) and benthicinvertebratebiomass (excluding
largespecies)
acrossthefront(b).Thepositionof the frontisdynamicandvariesbetweenapproximately
57ø15and57ø45N. Onaverage bothphytoplankton andbenthic biomassesaresignificantly
elevatedin the regioncoveredby the excursions of the front. Phytoplanktondata from
Heilmannet al. [1994]andbenthicinvertebrate
datafromJosefson andJensen(pers.comm.).
et al., 1990b;KierboeandNielsen,1994].However,because largephytoplankton

cellsbloomexactlybecause predationpressureis low, and becausethe biomass
concentration ishighduringblooms,
themajorityof thecellsarelikelyto coagulate
andsubsequently
settleout of the watercolumn.
Thespringphytoplankton
bloomin temperate watersis dominated by largedia-
toms,andisanexample of suchan episodic
bloom.In theKattegat,for example,
themesozooplankton
onlyconsume < 1-5% [Nicolajsen
et al., 1983]or ca. 12%
[Kierboe
andNielsen,1994]of thespringbloomprimaryproduction. Grazingby
heterotrophic
dinoflagellates,
theonlyothersignificant
groupof grazers thatcon-
sumelargephytoplankters
[Hansen,1991],mayaddto this.However,at leastin
someyears,the majorityof the springbloomsediments
to the seafloorin the
Kattegat
[e.g.,Christensen
andKanneworff, 1985;Olesen1993]aselsewhere
(e.g.
KielBight[Smetacek,
1980;Peinert
et al., 1982]).
Storm-induced
entrainment
of newnutrients
to thesurface
layerandsubsequent
bloomingoflargephytoplankters
isanother
exampleofepisodic
microalgal
blooms.
KiorboeandNielsen[1990]andNielsenandKierboe[1991]describedsucha
wind-generated
bloomintheKattegat.
Althoughcopepodproductivity
increased
Kiorboe 87
response
totheelevated
foodavailability,
themajority
oftheepisodic,
newproduc-
tionsedimented
outofthewatercolumn. Otherexamples
of short-lived
wind-gen-
eratedmicroalgalbloomsand their effecton sedimentation
and foodwebstructure
havebeenprovided
bye.g.Mullinet al. [1985],Cowles
et al. [1987],Hitchcock
et
al. [1987],andNair et al. [1989].
Frontsconstitutethefinalexample
of localized
andepisodic
availability
of newnu-
trients[e.g.,LoderandPlatt,1985]to beconsideredhere.Fronts
arefrequently
characterizedby elevatedconcentrations of microalgae [Le Fivre, 1986]andof
highzooplankton productivity[Ki•rboeet al., 1988],andthesefeatures alsochar-
acterizethefrontsbetween differentwatermasses in theKattegat/Skagerrak area
[Richardson,1985;Ki•rboeet al., 1990] (seealsoFigure4.8a). Elevated sedimen-
tationof POM isalsoexpected at fronts,butisdifficult
to document dueto thedy-
namicpositionof mostfronts.TheKattegat/Skagerrak front,for example, makes
significant
short-termexcursions (ontheorderof 50-75 km [Pedersen andM•ller,
1981]), and there are no sedimenttrap data availablefrom the frontal areasin
Danishwaters.However,the biomass andproductivityof benthicfaunais signifi-
cantlyelevatedin the areacoveredby the excursions of the Kattegat/Skagerrak
frontrelativeto theregions
northandsouthhereof(Figure 4.8b),suggestingelevat-
edsedimentation of POM in thefrontalregion[Josefson
andJensen, unpublished].
4.11.HydrodynamicControlof PelagicFoodWebStructure
Theflux of materialandthe structureof pelagicfoodwebsareultimatelygoverned
by hydrodynamic processes.
It hasbeenshownabovethat
1. thespario-temporal variationin theavailabilityof "new"nutrientsisunderhydro-
dynamiccontrol;
2. the sizedistributionof the phytoplanktonis determinedby the spatio-temporal
variationin the availabilityof inorganicnutrients(continuous
or pulsed);and
3. the fate of the pelagicprimary production,flux of materialand, hence,the
structureof the pelagicfoodweb dependon the sizecomposition of the phyto-
plankton.
Thus,microbialfood websare characteristic of stratifiedwaters,wherethe supply
of nutrientsis relativelycontinuous,
and classicalgrazingfoodchainsdevelopin
shallowturbulentenvironments and at oceanographic discontinuities
in watercol-
umnstructure, wherenutrientavailability
is pulsedor episodic.Themicrobial
food
webandtheclassical grazingfoodchainrepresent extremes in a continuum,
andin
theseaall intermediate
typesof pelagicfoodwebstructure exist.
Theexportof organicmaterialfromtheeuphotic zoneisprimarilyin theformof
sedimenting particulate
materialandiseventually limitedbytheimportof newin-
organic nutrients.
In microbial
pelagiccommunities, wheresuspended particlemass
isrelatively
low andthesuspended particles
small,coagulation
andsubsequent sedi-
mentation of particulate
materialispresumablyfacilitatedbytheparticlesof TEP.
It is otherwisedifficult to reconcileobservedsedimentation
ratesof
organicaggregates in suchcommunitieswithclassical coagulationtheory.In epi-

sodic,nutrient-rich
environmentstheverticalflux of particulate
materialis substan-
tial. Largeparticles(diatoms)
occurin highconcentrations, and aggregated live
phytoplankton cellsaccountforthemajorportionof thesedimented material.
Theserelationshipsareparticularlyevident
onoceanwideandseasonalscales.
For
example, in thepermanently stratified
oceangyresandduringsummer stratifica-
tionin temperatewaters,pelagic foodwebsappearto beof themicrobial
type.In
thepartiallystratified
zonesof themajorupwellingregionsandduringbeginning
vernalstratification
in temperate
waters,on the otherhand,classical-type
grazing
food chainsdominateand substantialsedimentationof phytoplanktonoccurs
[Legendre
andLe F•vre,1989;Kiorboe,1991,1993].Thelattertypeof environ-
mentalsosupports
productionat highertrophiclevelsandsignificant
fisheries
[e.g.,
Ryther,1969;Cushing,1989].
The variationin pelagicfoodweb structurein relationto hydrodynamicfeatures
appears,however, to recuronmuchsmallerspario-temporal scales.
Microbialfood
websin stratifiedwatercolumnsmay be rapidlyreplacedby grazingfood chains
andheavysedimentation whereand whenepisodicor localizedinjections
of inor-
ganicnutrientsto theeuphoticzoneoccur.Likewise,a microbialcommunityagain
takesoveroncethe short-lived microalgalbloomhasexhaustedthe inorganicnutri-
ents.Episodicstormsand localizedtidal frontsconstituteexamples,which were
considered above.A transectstudyin the Skagerrakprovidesanotherexampleof
howspatialvariationin pelagicfoodwebstructuredepends in a predictableway on
km-scalevariationin the hydrodynamics [Ki•rboe et al., 1990b]. In the partially
mixedperipheralregionsof the Skagerrakmicrophytoplankton occursin highcon-
centration,copepodproductivity(indicativeof classical grazingfood chain)is high
and microbialactivity(bacterialgrowth rate) is low; in the central,stronglystrati-
fied part, on the contrary,phytoplanktonbiomassis low and dominatedby small
flagellates,copepodproductivityis low and microbialactivityis high (Figure4.9).
Thus, in this examplepelagicfood web structurechangesfrom a classicalto a
microbialandbackto a classical typealonga transectlessthan 80 km long.
4.12. Conclusion
Coastalecosystems are in generalphysicallymorevariable,energeticand turbulent

than the openocean.This is becausetidesare important,currentsimpingeon
coastsand deposited wind energywill dissipatein a relativelyshallowwater col-
umn.The spatio-temporal variabilityin the hydrodynamicsgivesriseto a highly
variablestructureof the pelagicfoodweb. Furthermore, the hydrodynamic pro-
cessescauseinjectionsof inorganicnutrientsintothe euphoticzoneon an intermit-
tent basisandto leadsignificant organicproductionthat is boundto be eventually
exportedfromtheeuphotic zone.Exportof organicmatteris mainlyin theform of
sedimentation to the seafloor and aggregate formationby physicalcoagulation
appearsto beimportantin facilitatingthe POM
Kiorboe 89
DENMARK NORWAY
1 2 3 4 5 6 7 8 9 10 11 12 Station No.
Deptmh'
0I' '2
a
I '•'4'
'L<2•
J 24--
20
I ;5 27
30 Sigma-t 27
40
lO
2o
30
Volumeratio, • 5
40 >8 !•m/<8 !•m
o[ /'___-"••'
10 0.5
\\\/o'."-'"-
0.3
20. /•;';I
•' • o•
• Fluorescence,'
• - o.•
30
40
/ • arbitra•
units
10
20 •s 2
3
30 Bacteria 5
40 generation
time,d
Eggs/Did
50
Fecundity
I Ternora
40 [] Acarha
3O
e
20
10
• 2 345 6 7 8 9 10 11 12 Station No.
Figure
4.9.Horizontal
variation
inthevertical
water
column
structure
across
theSkagerrak
andassociated
variation
in properties
ofthepelagic
community
in May.Waterdensity
as
sigma-t
units
(a);volume
ratiooflarge(> 8 •m) tosmall(< 8 Ixm)phytoplankters
(b);
chlorophyll
biomass
asfluorescence
(c);bacteria
generation
time(=growthrate
-•)(d);and
fecundities
ofthecopepods
Acartia
claus•
andTemora longloomis.
From Kiorboe
Theinputof physical
energy
to coastal
ecosystems
will,ontheonehand,acttoho~
mogenize
thewatercolumnvertically.
Thisis counteracted,
however,by fresh-
waterrunofffrom land,that will tendto verticallystabilizethe water column.
Coastal
watersin general
andestuaries- astheKattegat-in particularare,there-
fore,typicallystronglystratified
duetosalinity
differences.
Theoccurrence of a pyc-
noclineandthedifferent transportcharacteristics
of soluteandparticulatematerial
will verticallydisplaceoxygen-consuming and -producingprocesses. Anthropo-
geniceutrophication mayenhance theverticalflux of organicparticles
and,thus,
potentiallyincrease the oxygendeficitbelowthe pycnocline with anoxiaas one
detrimental effect.However,the magnitude of the oxygendeficitis not relatedto
the amountof introduced nutrientsin a simple,linear way. As discussed in this
chapteronereason forthisis,thatnutrients delivered
intermittentlyaremorelikely
to giveriseto enhanced organicparticlesedimentation than nutrientsdelivered
continuously.In the latter case,remineralizationof organicparticlesmay occur
withinthe euphoticzone,and otherprocesses (e.g.denitrification)may remove
"excess"inorganicnutrientsfrom thewatercolumn.
Acknowledgments. Thanksaredueto PaulWassmann, JensHeilmann,and Morten Sonder-
gaardfor criticallyreadingan earlierversionof the manuscript,and to Alf Josefsen
for per-
missionto useunpublished data.The manuscript wasfinalizedin the summerof 1993.
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5
Carbon Flow in the Water Column

CaseStudy:The Southern
Kattegat
Introduction
TheKattegatis amongthe beststudiedmarineregions in theworldandcertainly

onefor which someof the longest. time seriesfor biologicaldata are available.
Nevertheless,the increasein intensityand geographic distributionof anoxiaand
hypoxiaobserved in thisseaduringthe 1980scameasa surprise to scientists
aswell
asto thepublicat large.Recordsfromtheearlypartof thiscenturysuggest thatcer-
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in the BeltSeas)havelongbeenplaguedby per-
iodicoccurrences of hypoxia.However,previously theseincidents wereapparently
limitedto deeper"holes"in the seabottomwherebottomwater exchange canbe
restricted
- especiallyduringperiodsof calmweather(typicallyin latesummer).
Sincethe early 1980s,widespreadhypoxia(definedhereas oxygenconcentrations
of < 3 mg O2 1-1)hasbecomean annualfeaturein bottomwatersof the Kattegat.
The magnitudeof the problemvaries,however,fromyearto year,presumably asa
functionof weather(mixing)conditionsand nutrientinput.The mostseverecondi-
tionsobservedto datewererecordedin 1988 wherethe hypoxiaextendedessential-
ly overthe entireKattegatsouthof about57øN latitude(seechapter1; Figure1.6).
It hasgenerallybeenassumed[•rtebjerg, 1987;Rosenberg et al., 1990;Kronvang
et al., 1993] that the causeof the observedincreasein oxygendepletion of bottom
watersis an increase in sedimentationof organicmaterialfromthewatercolumnto
thebottomwhichgivesriseto an increase in biological
oxygendemand(BOD) in
near-bottom waters.This presumedincreasein sedimentation of organicmaterial
shouldbe a consequence of an increasein phytoplankton primaryproduction
resulting froma documented increasein eutrophicationof thisarea(seechapters 3
and 12).

Union
96 5. CarbonFlowin theWaterColumn
Primaryproduction
inthisandmost other
estuarine
marine areashasbeen shown
to respond
directly
to or becorrelatedwithincreases
in nitrogeninput[Gran•li,
1987;Nixon,1992].Thus,it is increases
in nitrogen
loadingthatarefrequently
citedasbeingresponsible
for hypoxiain theKattegat.Verylittlewasactually
known,however, aboutcarbonflowwithinthewatercolumnhereor aboutany
changesthatmayhaveoccurred
inthepatternofthisflowasa result
ofeutrophica-
tionpriortotheexecution
oftheDanishMarine ResearchProgram during
theper-
iod 1988-1993.
A majorgoalofthisprogram
wastoincrease
understanding
of theinteraction
be-
tweennutrient
inputandoxygen
depletion
in Kattegat
bottomwatersin orderto
determinewhethera reductionin nutrientloadingcan be expectedto reducethe
intensity
and/orfrequency
of hypoxicevents.
In orderto achieve
thisgoal,it was
necessary
to improve
theexisting
understanding
of energyflowwithinthepelagic
community.Therefore,
a number ofstudies
wereinitiated
whichcontributedtothe
overallgoalsof
1. Describing
theannualcycling
of carbon,
nitrogen
andoxygen
withinthewater
column
2. Identifying
the potentialinfluenceof hydrographic featuresand in particular,
wind-drivennutrientupwellingon patternsof energyflow and
3. Identifying
anylong-term changesthatmayhaveoccurred in theproductionof
organicmaterialin theKattegat.
s.2.Description
of theStudiesCarriedOut
One centralstudywas carriedout at a fixed positionin the southernKattegat
(56ø11' N; 12004' E) between1988 and 1990. The samplingstrategywas designed
to providea description of carbonflow within this systemfor the calendaryear
1989.A buoyequipped with automatedtemperature, salinityand currentsensors
anda fluorometer for determining
chlorophyll-a fluorescencewas deployedat the
station.Sedimentation was estimatedusingsedimenttraps throughoutthe water
column.These,however,were unfortunatelyonly in position during the period
March to October 1989 [Olesen,1993; Olesenand Lundsgaard,1994; Olesen,
1994].
In additionto the automaticregistrationof data carriedout at this position,the
stationwasvisitedat approximately fortnightlyintervals.On thesevisits,standard
hydrochemical determinationswere carriedout. Sampleswere alsotaken for the
determination of biomassand/orspeciation of bacteria[Bjornsenet al., 1992], phy-
toplankton,heterotrophic nanoflagellates [Thomsenet al., 1992] microzooplank-
ton [Hansen,1991; Nielsenand Ki•rboe, 1994] and mesozooplankton [Ki•rboe
and Nielsen,1994]. Primary[Richardson and Christoffersen,1991] and secondary
[Bj•rnsenet al, 1992:bacteria;KiorboeandNielsen,1994:mesozooplankton] pro-
duction measurements were also carried out on most
Richardson 97
Short-term
fluctuations
in carbonflow wereexamined
duringthree"intensive"
study
periodsinwhichthebuoyposition wasvisited
everyday(weather
permitting)
duringa periodof approximatelythreeweeks.Thesetookplacein May-June,
1988,August-September, 1989andOctober-November, 1989.Duringa 10-day
periodin April 1989andtheAugust-September 1989intensive
sampling period,
measurementsof nitrateuptakeusingstandard
•SNtechniques[Kaaset al, 1992]
were carried out.
5.3.Carbon/NitrogenFlow:AnnualCycle
Anestimate for phytoplankton primaryproductionof 290 g C m-2yr-• wasmade
usingthe •4Cincorporation methodat thefixedpositionin theKattegatin 1989
[Richardsonand Christoffersen, 1991].The exactrelationship between •4Cincor-
porationand net andgrossphotosynthesis is unclear[Peterson, 1980]butin an-
otherstudycarriedout in thisresearch
program,Jespersen et al. [1994]foundusing
severallaboratoryculturesof phytoplankton
that the resultsfrom the •4Cmethod
approximated netphotosynthesisundermostof theconditions tested.
Furtherstudiesare necessaryin orderto determine therelationship between•4Cin-
corporationand neffgross photosynthesis undernaturalcohditions. However,even
if the•4Cmethodof estimating primaryproduction approximates netphotosynthe-
sisassuggestedbyJespersen et al., thevalueof 290 g C m-2 yr-• for annualprimary
productionat the fixed station in the Kattegatpresentedby Richardsonand
Christoffersen
[1991] must be correctedfor phytoplankton's dark respirationbe-
forean estimateof the carbonavailablefor thepelagicfoodchaincanbemade.
Net dielphotosynthesis(i.e.that occurring
overa 24-hourperiod)cannotbedirect-
ly measured.From culturestudies,however,it is known that dark respirationis
oftenon the orderof 5 % of the maximumrateof photosynthesis. The lightcondi-
tionsovermuchof the water columndo not, of course,supportmaximumphoto-
synthesis.
Giventheseconsiderations, a respiration
lossdueto darkrespirationon
theorderof 15% of thetotal primaryproduction wouldappearreasonable. Using
thiscorrection,
phytoplankton respiration
wouldaccountfor a consumption of
about45 g C m-2 yr-s at the buoystation.A reasonable
estimateof netprimary
production
wouldseem, then,to beontheorderof 245g C m-2yr-•.
Sedimentationof organicmaterialat thebuoystationwasestimated to be63 g C
m-2duringtheperiodMarchto October, 1989[Olesen andLundsgaard, 1994].It
wasnotpossible to maintainthesediment trapsin position
duringthewinterper-
iod.However,sedimentation duringthewintermonthsis expected to besmall.In
addition,
the sedimentation
valuesduringtheperiodMarchto Octoberagreewell
with an earlierestimateof sedimentation
in the Kattegat(66 g m-2 yr-•) madeon
the basisof benthicmetabolismat a numberof differentstations[Jorgensen and
Revsbech, 1989].Thus,thevalueof 63 g C m-2istreatedhereasanestimate of an-
nualsedimentation
occurring
at thebuoystation.
Some of thissedimented
material
derives
directly
fromprimaryproduction
whilesome will,of course,
originate
from
heterotrophic
98 5. CarbonFlow in theWater Column
Microzooplankton
Bacteria
114.3
g Mesozoopla
,!•
63
g
Sedimentation
Figure5.1. Flow of carbonin the pelagicfood web at a fixed positionin the Kattegat
(56ø11'N;12ø04'E).All,unitsare in g yr-•. Note that the sumof the valuesoutsideof the
ringisgreaterthan thevaluefor net primaryproduction.This is becausesomeof the carbon
beingconsumed by thevariouscompartments or sedimenting is the productof heterotrophic
processes.Thus,carbonfixedvia primaryproductioncan appearmore than oncein the de-
scriptionof carbonflow.Seetext for thesources
of the valuescited.
Kiorboe(seechapter4, thisvolume)hasemphasized that a quantitativedescription

of the flow of carbon(energy)within the pelagiccommunitywould requireesti-
matesof respiratory lossof carbonat eachtrophiclevelbecauseof the potential
confusionresultingfrom lossand reuseof carbonat all trophic levels.Unfor-
tunately,suchestimates do not exist.Nevertheless,
a semiquantitative description
of the flowof carbonfromprimaryproducers and into the pelagicfood chainin
the Kattegatcan be obtainedby examiningth• ingestionby the variouspelagic
compartments(Figure5.1).
Bjornsen et al. [1992]estimated
bacterialcarbonconsumption in the watercolumn
to beontheorderof 30% of primaryproduction (ca.87 g C m-2 yr-•) at thebuoy
positionin 1989. Kiorboeand Nielsen[1994] and Nielsenand Kiorboe [1994]
haveestimated grazingbymesozooplankton andmicrozooplankton (ciliates)at this
stationto be37 and 143g C m-2 yr-•, respectively.
Otherworkers [Hansen andNielsen,1992]estimated thatmicrozooplankton graz-
ing consumed 10-20% of the phytoplankton biomass on a daily basis.Phyto-
planktonbiomass at thisstationin 1989converted fromchlorophyll to carbon
unitshasbeenpresented byKiorboe(chapter 4, thisvolume). With theexception of
thespring bloomperiodwhenit reaches a valueof nearly25 g C m-2,phytoplank-
tonbiomass isontheorderof 2 g m-2duringtheproductive periodof theyearand
slightlylessduringthewinter.Applying a valueof 2 g C m-2 to Hansenand
Nielsen'sestimateof microzooplanktonconsumption, yieldsa valuefor microzoo-
planktongrazingof 73-146 g C m-2yr
Richardson 99
mgC m-2 d-•

1000
800
600
400
2OO
March April une July • Aug • Sep • Oct •

Month
Figure5.2. Sedimentation
of total particulate
organiccarbon(POC)andphytoplankton car-
bonfromthe surfacelayerthroughthe pycnoclineinto the bottomwaterat the buoystation
in theKattegat:March-October, 1989. After OlesenandLundsgaard[1992].
As pointedout earlier,carboningestionby thesevariouscompartments of the

ecosystem neednot bemutuallyexclusive.Bacteria
donot,for example, drawall of
theircarbondirectlyfrom primaryproducers andit is not onlyphytoplankton par-
ticlesthat are ingested
by micro-andmesozooplankton. Nevertheless,thisanalysis
suggests that most of the phytoplankton primaryproductionoccurringat the
Kattegat stationis processed
in thewatercolumn.$edimenting material, then,will
largely betheproducts of heterotrophic
processes.
Thisargument issupported bya
comparison of phytoplankton
carbonandtotalPOCsedimenting through thepyc-
noclinefrom the surfaceto bottomlayer (Figure5.2) whichindicates that POC
sinkingout is only dominated by phytoplanktonC duringthe springbloom.
Duringtherestof theproductive period,phytoplankton C (asdetermined fromthe
chlorophyll
content
in thesedimenting
material)
represents
< 30%ofPOC[Olesen
andLundsgaard,1994].
5.4.NitrogenInputandPrimaryProduction
Phytoplankton
production in marine
watershasoftenbeenshownto belimitedby
nitrogen
availability.
In addition,
totalprimary
production
iscomprisedofa "new"
anda "regenerated" component dependingupontheionicnitrogensourceused
tosupporttheproduction [DugdaleandGoering,1967].Only"new"production
(based
on nitrate-N}canleadto a netincrease
in organic
materialin thesystem.
Thus,
it isnewproduction
thatismostrelevant
toconsider
interms
of
lOO 5. Carbon Flow in the Water Column
tion analyses.A quantitativedistinction

betweennew and regenerated production
in thesecoastalwatersis not possible.Nevertheless, an estimateof the magnitude
of the net increasein the productionof organicmaterialin the Kattegatcanbe
madeby considering thetotalnitrogenavailabilityin theKattegat.
Theannualnetloadingof nitrogento theKattegatvialandrunoff,atmospheric depo-
sitionand advectionfrom surroundingseashasbeenestimatedto be on the order
of 1.5x10s t [Planla•gningsr•det,
1987;Hansenet al., 1994;andchapters 3 and12,
thisvolume].In additionto the nitrogenenteringtheKattegatfromexternalsources,
thereis a poolof nitrogenalreadypresentin Kattegatwaters.Frominorganicnitro-
genconcentrations in winter(whenwe assume that the majorityof the nitrogen
presentin the pelagicsystemis in the inorganicform), this pool sizecan be esti-
matedto be on the order of l x!0 s t N [Richardsonand Christoffersen,1991].
Dividingby the area(31,000km2}applyingthe Redfield[19581ratio (C:N molar
ratio = $.7) to the combinedallochthonousand autochthonousnitrogensourcesand
assumingthat all of thesenitrogenatomsare usedjustonceduringthe annualpro-
ductioncycleyieldsthetheoreticalnewproductionin this area(48 g C m-2 yr-•).
Comparison of thisvaluefor new productionand total annualproduction(290 g C
m-2 yr-1beforecorrection for phytoplankton'sdark respiration)leadsto theconclu-
sionthat mostof the nitrogenwithin the systemis beingremineralizedand reused
duringan annualproductioncycle.The measuredsedimentation rate (63 g C m-2)
suggests that this reuseleadsnot only to regeneratedproduction[sensuDugdale
and Goering,1967] but alsoto somenew production(i.e. leadsto a net increase in
organicmaterial).That the theoreticallyderivedestimateof new productionmay
be an underestimate of actualnew productionmay be at leastpartly explainedby
the fact that, in the aboveanalysis,the Kattegat is treated as a singlesystemand
nitrogeninput to the systemas a whole is considered. In reality, however,phyto-
planktonactivityin the Kattegatis controlledby nutrientexchanges occurringat a
muchmorelocal scalethan that of the entire Kattegat(Figure5.3).
This regionis stronglystratifiedduringthe most productivepart of the year. The
surfacelayercorresponds more or lessto the euphoticzoneand the phytoplankton
activityin the surfacelayerreducesthe availabilityof nutrientsin this layersothat
nutrientsbecomelimiting for primary production.In their sedimentationstudy,
Olesenand Lundsgaard[1994] noted that nitrogen is apparentlyremineralized
fasterin the water columnthan carbonat the buoystationas evidencedby the fact
that sedimentingorganicmaterial exhibiteda higherC :N ratio (8.4 molar ratio}
than that observedfor suspended material in the photic zone (6.6). They suggest
that at leastsomeof thiswater columnremineralizationis occurringabovethe pyc-
noclineand thisalecoupling of N and C would, in theory,meanthat an individual
nitrogenmoleculemay support"extra" phytoplanktonproductionwhich can be
considered as new productionwith respectto carbonbut as regeneratedwith re-
spectto nitrogen.
In additionto remineralizationof nitrogenin the upperpart of the water column,
the transferof nitratefrom bottomto surfacewaters(and the atmospheric deposi-
tion of nitrogento surfacewaters)willalsoleadto newproduction.
Richardson 101
SEA SURFACE
Primary
production
Import Biomass
Export
• Nutrients
' Regeneration
PYCNOCLINE
Sedimentation
Export
Regeneration
Import
• Nutrients
Import
inorganic nitrogen
SEA SURFACE
Total
•. primaryproduction
Import
inorganic 290
gC;
56
gN '"•
nitrogen
48
CO;,g•",,,,•
inorganic
nitrogen
Particulate
and
• • dissolved
organic
material .
PYCNOCLINE
CO2
+168 g 02
Sedimentation
[ Tempora ......--"•accumulation
,, 63gC
I • I nitrogen
7.6gN+34'g
O2 I ]---""•Export
Figure 5.3. a: Schematic

diagram identifying
sourcesof nutrients
(including
locationof nu-
trientregenerationin thewatercolumn} whichcontrolphytoplanktonactivity
in theKat-
tegat.b: Biologically
mediatedcarbon andnitrogenflowin thewatercolumn at thefixed
position in theKattegatduring1989.Theamount of oxygen required
to remineralizethe
sedimented material
isalsogivenin thefigure.Sources
forthevaluespresentedaregivenin
the
102 5. Carbon Flow in the Water Column
mixingof regenerated
nitratefromthebottomto thesurface
layerislikelyto con-
tributeto newproduction
throughoutthesummer season.Hansenet al. [1990]
haveestimatedthat on the orderof 1.1x10s t N were transportedannuallyfrom
bottomwatersthroughthepycnocline andintosurface watersduringthesummer
periodduringthe1980s.Thisvaluewouldcorrespond to a netorganic production
of 29 g C m-2 yr-•. In addition,it mustbeexpected thattheprimaryproduction
occurringduringthewinter,at the timeof thespringbloomandin the bottom
waters(whenthephoticzoneextends to belowthepycnocline} will largelybesup-
portedby nitrateand,thus,be characterized by a relativelylargeproportionof
"new" production.
OxygenBudget:BottomWaters
Data are availablefor the period of most active phytoplanktonproduction
(March-October) in 1989that allowexamination of theoxygenbudgetin bottom
watersat the buoystation.Olesenand Lundsgaard [1994]estimated
that the or-
ganiccarbonsedimentation of 63 g m-2 hereduringthisperiodwasaccompanied
by the sedimentation of 7.4 g of nitrogen.This sedimentedcarbonwouldrequire
168g 02 duringitsrespiration to CO2andthenitrogenwouldrequire34 g 02 to
be oxidizedto nitrate.Thus,a total'of 202 g 02 m-2 would be requiredfor the
remineralization
of thesedimented material(Figure5.3b).
A reductionin oxygenconcentrationof only 61 g 02 m-2 in bottomwater (i.e.
belowthe pycnocline)
wasrecordedduringthe sameperiod[Olesenand Lunds-
gaard,1994].However,thereis an inputof oxygento bottomwatersduringthe
summermonthsvia lateral advectionfrom more oxygen-richareas (e.g. Skager-
rak) and by mixingthroughthe pycnoclinewhich will, to someextent, mitigate
the oxygenlossdueto remineralization processes.Models[Hansenet al., 1990;
Hansenet al., 1994; andchapter11, thisvolume]describing water flow and mix-
ing processes
in thisregionsuggest that an oxygenusagebelowthe pycnoclineof
approximately 190 g m-2 in remineralizatior•
combinedwith the oxygeninput via
hydrographic processeswould yield a drop in oxygenconcentrationin bottom
watersthat agreeswell with the observed.This good agreementbetweenmea-
suredchanges in oxygenconcentration in the bottomwatersand thosepredicted
from carbonsedimentation ratesand oxygenadvectionsupportsthe assumedlink
betweenoxygendepletioneventsand primaryproduction(sedimentation of or-
ganiccarbon).
3.6.SeasonalCyclein Sedimentation
It has previouslybeenassumedthat the major sedimentationof carbon from the
watercolumnto the bottomoccursin connection with thespringbloom.However,
oneof the resultsthat emergedfrom thisstudywasthat the sedimentationof par-
ticulateorganiccarbonout of the water columnwas variablebut remained
Richardson 103
fromthetimeof the springbloomuntillatesummer(Figure5.2). Duringthesum-

merperiodwhenphytoplankton carbonwasa minorcontributor to thetotalPOC,
microscopicexaminationof sedimented
materialindicated
that it waslargelycom-
prisedof "aggregates"
or marinesnowof unidentifiedorigin[Olesen andLunds-
gaard,1994].
5.7.Subsurface
PhytoplanktonPeak
Anotherresultarisingfrom the studywasthe factthata subsurface
phytoplankton
peakdominates primaryproduction in the Kattegatfromtheperiodimmediately
followingthe springbloom until the autumnalbreakdownof stratificationin
September-October [Richardson andChristoffersen,
1991;Heilmannet al., 1994].
De )th, m
0
o
lO
2o
29 , •
March April May June July AugustSeptember
October
Month
Figure
5.4.Distribution
of a) salinity
andb) fluorescence
throughthewatercolumn
at the
buoystation
in theKattegat
fromMarchto October, 1989.AfterOlesen
andLundsgaard
mgC
4000
Daily production 1989

3000
2000
1000 -
0-- -
...........
.....
' Jan' •eb 'March'

April
l"May' June
' july' Aug' Sep' 0Ci
.......
i Nov' Dec'
Month
Figure
5.5.Dailyprimary
production
at thebuoystationin theKattegat
during1989.Stars
represent
weeksin whichmorethanonesample wastaken.FromRichardson andChri-
stoffersen[1991].
De :)th,rn
-
16
•,7 22 2.4
2,8
2'1
2•,,.•22 22 15 12
1.4151411
11111417
18
22•
2.9
2.2
2,12.1
1(3 1310 1113 15
10 _
17
16 2,32.12,1
2.0
2.0
(• 21
10 1,215 1.5 1
12 12 •1 •0
19
20- 11
1816 09 lJ 1112.10 12 1517

• •18
14
30-
Jan Feb March April May June July Aug Sep Oct Nov Dec
Month
Figure5.6. Distributionof the 480/665 absorptionratio throughthe water columnat the

buoystationin 1989.Valuesof over2.0 (shaded) indicatea phytoplanktonpopulationthat
is nutrient-depleted
[seeHeathet al., 1990]. FromRichardsonand Christoffersen[1991].
Theoccurrence
of subsurface
chlorophyll
peaksin thisareahasbeenacknowledged
foroverfiftyyears[Pettersson,
!934].How.
ever,thestudies
described
hererepre-
sentthefirstattemptto quantifytheimportance
of thesepeaksfor the total prima-
ry productiontakingplacein theKattegat.
Figure5.4 showstheverticaldistribution
of chlorophyllthroughoutthewatercol-
umnat thebuoystationfromMarchto October,1989.Thespringbloomis clearly
themostsignificant
featurein thesurfacewatersat thisstation.However,a strong
subsurfacechlorophyll
peakwaspresent fromtheendof Marchuntilthemiddleof
July.Althoughchlorophyll
concentrations werelow throughout thewatercolumn
duringthe periodbetween the middleof July and the middleend of August,
Richardson andChristoffersen[1991]havereported thata subsurface
chlorophyll
peakwasalsopresent duringthis
Richardson 105
Theeffectof thesubsurfacephytoplankton
peakfromtheperiodfollowing the
springbloomuntilthemiddleofJulycanbeseen in theannualdistribution
of pri-
maryproduction throughouttheyearin 1989(Figure 5.5).Althoughthehighest
dailyratesrecorded
duringtheyearwereduringtheveryshortspring bloom,sub-
stantial
rateswerealsorecorded in theperiodfollowing thespringbloomuntilthe
middleof Julyas a resultof the activityof the subsurface
phytoplanktonpeak.
RichardsonandChristoffersen [1991]haveestimated that 19% of theannualpri-
maryproductionat thebuoystationoccurred duringthespringbloomwhileonthe
orderof 33% occurredin thesubsurface peakin themonthsfollowing thespring
bloom.
Theratioof carotenoid to chlorophyll

pigments (asindicatedby theabsorption in
acetone extractsat 480 and 665 nm) can be usedasa qualitativeindicatorof the
nutrientstatusof a phytoplankton population[Heathet al., 1990].The distribu-
tionof thisratio throughout the watercolumn(Figure5.6) showsthepresence of
highvalues(indicating nutrientdepletion)
in surfacewatersandlowvaluesin bot-
tomwatersfrom theperiodfollowingthe springbloomuntilaboutmid-July.After
thistime and until the autumnalbreakdownof stratification,highratiosare re-
cordedthroughoutthe water column,suggesting the presence
of nutrientdepleted
phytoplankton throughout thewatercolumn.
The light attenuationcharacteristics
of the water columnshowthat the lower
boundaryof the euphoticzone (1% light penetrationlevel)in thisregionduring
JulyandAugustliesbetween15 and 18 m [Richardson a0_dChristoffersen,
1991].
Theannualdistributionof nitratethroughoutthe watercolumnat a nearbystation
in the Kattegat(Figure5.7) indicatesthat the nutriclinedeepensthroughoutthe
summer. Measurements of nitrate concentrations carried out in 1989 at a station
Depth, rn
10
20
30
40
Ja b •March
• April ' May • une• July• Aug• Sep• )ct N)v Dec
1991 Month
Figure
5.7.Annual
distribution
of nitrate
through
thewatercolumn
during
1991ata fixed
station(56ø40'N; 12ø07'E)in theKattegat.
From/Ertebjerg
TABLE 5.1. Nitrate concentrations(•mol 1-:)

at 15 and 20 m from May to Sept. 1989 near
the buoystation(seetext). Data suppliedby the
DanishNational EnvironmentalResearchAgency.
29 May 11 July 14 Aug 18 Sep
15 m 0.2 0.5 0 0.3

20 m 12.4 11.5 0.7 1.3
TABLE 5.2. Nitrate concentrations (•mol 1-•) at

15 and20 m duringJulyandAugustat a stationin
the southernKattegatduringthe 1980s (seetext
for details).Data suppliedby the DanishNational
EnvironmentalResearchAgency.
Year Depth July August
15 m 0.5 0
1981 20 m 0.2 0.4
15m 0 0
1982 20m 0.7 0
15 m 0 0.1
1983 20 m 10.6 2.1
15 m 0.2 0
1984 20 m 0.1 0
15 m 0.1 0
1985 20 m 0.1 0.1
15 m 0.7 0
1986 20 m 1.9 0.5
15 m 0.1 0.5
1987 20 m 1.9 0.5
15 m No data 0
1988 20 m No data 0
15 m 0.5 0
1989
20 m 8.0 0
nearthe buoystation(56010' N, 11048' E) showa very substantialdrop in the con-

centrationof nitrate at 20 m betweenmid-Julyand mid-August(Table 5.1). A lon-
gertimeseries
of nitrateconcentrations
at 15 and20 m duringthemonthsof Jul.y
and Augustat anotherstationin the southernKattegat(56ø40'N; 12ø07'E:Table
5.2) suggestthat thisseasonal
patternin the distributionof nitratethroughoutthe
water columnmay be typical.Thus, onepossibleexplanationfor the lessdominant
subsurface chlorophyllpeakand the dropin water columnprimaryproductionob-
servedat the buoystationin mid-Julymay be that therewas at this time no longer
an overlapbetweenthe euphoticzoneand the nutrient-richbottomwater.
It should,however,benotedthat thisexplanationassumes
that the subsurface
peak
is beingmaintainedwith bottomnutrientsand, thus,comprisesa large
Richardson 107
of "newproduction" (high"f-ratio",i.e. % of totalproduction

comprisedbynew
productionasdefined byEpplyandPeterson [1979]).Assumingthatthese peaks
aremaintainedbyalgalgrowthin situ(i.e.in thesubsurface peak)andnotbyad-
vection,
therelatively
largestandingstocks observed wouldalsosupportthisargu-
ment.Nevertheless,
theworkof Kaaset al. [1992],in whichnitrateuptakewasex-
amined using•SNtracertechniques, indicates thatthesubsurface
phytoplankton
peakmayon someoccasions
exhibita relativelylowf-ratio.
Kaaset al.'s argumentis, in part, basedon a hydrographicanalysis of thecondi-
tionsat thebuoystation[Pedersen, 1991]whichsuggests thatthesubsurface phy-
toplankton peakmayoftenbe associated with an "intrusion"layer(i.e.waterwith
temperature andsalinitycharacteristics
whichdifferfromboththesurface andbot-
tomwaters).Phytoplankton confinedto thisintrusionlayerwouldnot, undernor-
mal conditions, have immediate accessto nutrients in the bottom waters. Further
work is clearlynecessary to describethe fate of the carbonfixed by subsurface
chlorophyllpeaksin thisregion.
5.8.MesozooplanktonResponse to
PhytoplanktonDistribution/Activity
Theproduction(eggsproducedper femaleper day)of two commoncopepods and
thebiomassdistributionof the combinedcopepodpopulations throughouttheyear
at the buoystationare illustratedin Figure5.8. In addition,the surfacewatertem-
peratureand the integratedwatercolumnbiomass of phytoplankton >11 Ixm(i.e.
thoseabovethe minimumgrazablesizefor mostcopepods) are alsoshown.
Copepodeggproductionresponded clearlyto theperiodsof the springbloomand
the autumnalbreakdownof stratification.The markedreactionof copepodpro-
ductionto what arepresumed to bepeaksin newproduction(asevidenced by the
relativelylarge numbersof net (i.e. large)phytoplankton observed duringthe
springbloomand at the time of the autumnalbreakdownof stratification (see
Kiorboe[1993]) makesthe measurement of copepod eggproduction uniquelysuit-
edasan indicatorof changesin nutrientavailabilityin thepelagicfoodweb.
In contrast,totalcopepod biomass at thisstationin theKattegatshowed a strong
correlationwith watertemperature and exhibiteda singlepeakduringmid-sum-
mer.The factthat biomass showedlittleresponse to peaksin primaryproductionis
a functionof the relativelylonggeneration timeof copepods andthetemperature
sensitivity
of thegeneration time [e.g.,McLaren,1978].
5.9.Short-term Fluctuations in Carbon Flow
Theeffectof wind-generated
mixingof nitrate-rich
bottomwaterontotalprimary
productionandonthestructureof thepelagic
foodwebwasstudied duringoneof
theintensive
studyperiods
at thebuoystation(October 24 to November
9,
mg m-2 200 a Chlorophyll>1 l•m
150
100
5O
e
ße ß
oC 2O
15
10
5 •
Eggs•-1 d-1 25
,• C Acartia
20 •.'
15 '"
e
e
ee ß ß
ß ß ß
0 ..... ß i , i i ! , ! , i
Eggs (:2
-• d-• 7O e
6O
e
d Centropages
50
4O ße e
30 e
e
ee ße
2O ß
e
e
ß e
ee
10 e
ß ß
ee
0 , i
ß ! , e e ee, i , ,
mgC m-2 1000 oß e ,Copepod

o ß oiomass
e
.
ß ß
.
e e
-
e
500 . ß
ee e ß
ee
• ß ß e
. ß ß e
e
.
e
ß eß
0 •-'F'M'A'M'j ,j ,A, S, O, N,
Figure5.8.Distribution
ofa)chlorophyll-a
integrated
overthewatercolumn,
b)tempera-
ture,c)eggproduction
perAcartia
female,
andd) eggproduction
perCentropagus
female
ande)copepod biomass
atthebuoystation.
FromKierboeandNielsen
[1994].
Richardson 109
Ciliates Copepods
P:8.2 P:18.2!
Phytoplankton
B<11:622
I B<11:679
1
P:783 J
Other grazers. Accumulation.Sedimentation
Ciliates b Copepods
Ip: 22 !
Phytoplankton
9<11:652
1B<11•791
P:575 '
Other grazers. Accumulation. Sedimentation
Ciliates c Copepods
2l_•.•_J-3
P:
Phytoplankton
Other grazers. Accumulation. Sedimentation
Figure5.9. Carbonbudgetsat the buoystationreferredto in the text a) before,b) during,

andc) aftera stormin October-November, 1988. Unitsfor biomass (B)andproduction (P)
aremgC m-2 andmgC m-2 d-], respectively.FromNielsenandKierboe[1991].Reprinted
by permissionof OxfordUniversityPress.
That studyis describedin detail by Kierboeand Nielsen[1990], and Nielsenand

Kierboe[1991]. StrongwindsduringOctoberhadgraduallyerodedthe pycnocline
anda stormwith windsof up to 25 m s-• at thebeginning
of Novemberresultedin a
watercolumnwhichwas mixed almostto the bottom.The mixingof the watercol-
umnledto an inputof >35 mmolnitratem-2to thephoticzoneat thebuoyposition
duringthestorm.Thisnutrientinputgaveriseto an increase duringthedaysfollow-
ing the stormin phytoplanktonbiomassand primaryproduction(Figures5.8 and
5.9) whichwasmostpronouncedfor the larger()11 •m) phytoplankton
Depth,
m Wind
• Wind
•
0 20
IJ•I Salinity,
24
10
15
26
20
, I I , , , I II• I , , I I I I ,
Arbitraryunits
30 Fluorescence
>11pm
20
10
Eggs (::2
-• d-•
4
Eggs (::2
-• d-•
20
15
10
0 , s "'1"' , ,
24 ,40' ; ' ' ' ,• .... 1'0
october November
Figure5.10.Temporal variation
in thevertical distribution
of a) salinity(simplified),
b) flu-
orescencein the>11-•m fractionat 2.5 m, c) fecundityof Acartiaclausii,andd) fecundity
of Temora 1ongicornis.
FromKiorboeandNielsen
Richardson 111
Thisincreasein largephytoplankton
species
resulted
in a statistically
significant
in-
crease(doubling)of copepodproductionmeasured as eggproduction per female
(Figure5.10). The increased
eggproductiongaveriseto nearlya doublingin the
concentration
of copepodnauplii.However,as in the annualcasedescribed
above,
thecopepodbiomass remainedessentiallyunchanged in the periodfollowingthe
storm(datanot shown).Again,thisis because
naupliido not contributegreatlyto
thetotal copepodbiomass.
Thisexampleillustrates the potentialfor substantialchangesin thepatternof car-
bonflow in the pelagiccommunityoververyshorttimesscalesin thisregionin re-
sponse to changingweather(wind}conditions. Appreciationof theimportance of
localweatherconditionsfor the flow of energyin thepelagicecosystemhasonlyre-
centlyemerged (seeKiorboe,[1993]andchapter4, thisvolume)andthereisa need
for furtherstudyin orderto quantifythe relationship betweenwindconditions and
energyflow aswell asthe interannual variabilityin productionprocesses
thatcan
beascribedto differingweatherconditions.
5.0. Long-termChangesin OrganicProduction

A prerequisite
in orderto quantifychangesin organicproduction
overtimeis the
existence
of a goodhistoricaldata set describing
primaryproduction.The most
sensitiveand commonmethod usedtoday to determineprimary productivityin
aquaticenvironmentswas first described in 1952 by $teemann Nielsen.The
methodwasrathera noveltyin thatit requirestheadditionof radioactively
labeled
CO,.and quitea numberof yearspassed beforeit wasroutinelyused.Thus,for
mostmarineregions,thereareno historical primaryproduction datafrombefore
aboutthemid-1960swhichiscomparable to thosecollected
today.
Fortunately
for thisstudy,SteemannNielsen,himself,
carriedouta comprehensive
studywiththeaimof describing annualprimaryproduction in theKattegatduring
theperiod1954-1960.In hisstudy[Steemann Nielsen,
1964],samples weretaken
at approximatelyfortnightly
intervals
at a fixedstationin thenorthern Kattegat
(56ø51'2N; 11ø48'3E) andparticulate
primaryproduction wasdetermined follow-
inginsituincubations.SteemannNielsen's
conclusion
wasthattheannual primary
productionduring thisperiod
wasbetween 51and82gC m-2yr-• (mean = 67).
No attempthasbeenmadeto exactly
duplicate
SteemannNielsen's
methods and
sampling
strategy.
However, Richardson
andHeilmann [1995]havecollated
all
available
particulate
primaryproduction
datacollected
during
theperiod1984-
1993fromstations
nearthefixedposition
of $teemannNielsen.
In sofaraspossi-
ble,theyattempted
to applythesamemethods of datatreatmentas $teemann
Nielsen.
Usingthese
procedures,
theyconcludethatannual primaryproduction
in
theKattegat
intheirstudyperiod wasontheorder of240g Cm-2yr-•.
Theiranalysis
indicatedthat primaryproduction estimates
duringthe winter
months(whenlightispredictedto belimiting
forprimary
production)aresimilar
during
the1950s andtheyears between 1984and1993.However,fromabout
Primaryproduction,
g C m-2month-1
50-
40 .
30
20
10
0
J F M A M J J A S O N D
Month
Figure5.11.Dailyprimaryproduction
at fourdifferentdepthsin the watercolumnthrough-
out the yearas estimated
by Steemann
Nielsen[1964] (closedcircles)and Richardsonand
Heilmann[1995] opencircles.
timeof thespringbloomandfor mostof the monthsduringthe summer(whennu-

trientavailabilityis predictedto controlprimaryproduction)estimates of primary
productionare verymuchhigherin the 1984-1993 studyperiodthan in the 1950s
(Figure5.11}. This observation led theseauthorsto concludethat the apparentdif-
ferenceobserved in annualprimaryproductionbetweenthe 1950sand the 1980sis
a consequence of eutrophication(seechapter3 for a discussionof the extentof the
eutrophication occurringin thisperiod).
5.11. Conclusions
The comprehensiee studiesof energyflow in the pelagiccommunityin the Kattegat

carriedout as a part of the DanishMarine ResearchProgrammehave indicated
thattherehas,indeed,beena substantial increasein the magnitudeof the primary
production occurringannuallyin thissemienclosed seasincethe 1950s- a period
in whichland-based sources of nitrogento this semienclosed seahaveapproxi-
matelydoubled[Hansenet al., 1995]. Recordedsedimentation ratescombinedwith
analysesof advection ratesof oxygenintothe bottomwatersof the Kattegatand
throughthepycnocline supportthehypothesis thattheincreased frequency andin-
tensityof hypoxiaandanoxiaobserved in thisregioncanbe directlyrelatedto the
primaryproductionoccurringlocally.
Sedimentation of particulate
organiccarbonwasnot, asexpected,largelyconfined
to theperiodduringandimmediately followingthe springbloombut continuedat
a relativelyconstantlevelthroughoutthe summermonths.Carbon flow within the
pelagicfoodwebis highlydynamicandseemingly smallchanges in winddirection
and/orintensitycangiveriseto nutrienttransferfrom bottom to surfacewatersin
thisstratifiedseawhichcan,in turn,dramaticallyalterenergy
Richardson 113
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in Eutrofiering
av hays-ochkustomrc•den,
22, NordiskaSyruposier
omVatten-
forskning,Laugarvatn1986. Nordforski,Milj/Svfirsserien,
1987.
œrtebjerg,
G.,Marineareas,fjords,coasts,
andtheopensea(inDanish),
TheWaterQuality
Act'sMonitoring Programme1991, SpecialReport61, DanishEnvironmental
Protection
Agency,1992.
Bjornsen,
P.,L. Hansen, B.Lokkegaard,
andL. Berg,Bacteria
plankton
andbacteriagrazing
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T. Fenchel,Havforskningfra Miljostyrelsen,
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Dugdale,
R. C., andJ. J. Goering,Uptakeof newandregenerated
formsof nitrogen
in pri-
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Epply,R. W., andB.J. Peterson,
Particulate
organicmatterflux andplanktonic
newproduc-
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Gran•li,E., Nutrientlimitationof phytoplankton
biomass
in a brackish
waterbayhighlyin-
fluencedby river discharge,Estuar.Coast.ShelfiSci.,25, 563-569, 1987.
Hansen,I. S., G. AErtebjerg,L. A. J•rgensen,Analysisof oxygensedimentation in the Katte-
gat,the Belt Seasand the westernBaltic(in Danish),Havforskning fra Miljostyrelsen, 1,
133 pp., DanishEnvironmental ProtectionAgency,Copenhagen, 1990.
Hansen,I. S., G. •rtebjerg, K. Richardson,J.P. Heilmann,O. V. Olsen,and F. B. Pedersen,
Effectsof reducednitrogeninput on oxygenconditionsin the innerDanishwaters(in
Danish),Havforskningfra Milj•styrelsen,29, DanishEnvironmental ProtectionAgency,
Copenhagen, 103 pp., 1994.
Hansen,I. S., G. AErtebjerg,
andK. Richardson, A scenarioanalysisof effectsof reduced nitro-
geninputon oxygenconditions in theKattegatandtheBeltSea,Ophelia,42, 75-93, 1995.
Hansen,P. J., andT. G. Nielsen,Microzooplankton (in Danish),in PlanktonDynamicsand
Carbonand Nutrient Flow in Kattegat,editedby T. Fenchel,Havforskningfra Miljo-
styrelsen,10, 61-76, DanishEnvironmental Protection Agency,Copenhagen, 1992.
Hansen,P. J., Quantitativeimportance andtrophicroleof heterotrophic dinoflagellates in a
coastalpelagicalfoodweb,Mar. Ecol.Prog.Ser.,73,253-261, 1991.
Heath,M., K. Richardson,and T. Ki•rboe, Opticalassessment of phytoplankton nutrient
depletion,J. Plank.Res.,12,381-396, 1990.
Heilmann,J.P., K. Richardson,
andG. AErtebjerg,
Annualdistribution
andactivityof phyto-
planktonin theSkagerrak-Kattegat
frontalregion,
Mar.Ecol.Prog.Ser.,112,213-223,1994.
Jespersen,
A.M., M. S•ndergaard, K. Richardson,
andB.Riemann, Estimate of theaccuracy
andprecisionof the•4C-methodfordetermination
oftheprimary
production ofplankton-
ic algaeby useof routinemethodology
(in Danish),
Havforskning
fra Miljostyrelsen,
55,
DanishEnvironmental
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53 pp., 1995.
J•rgensen,
B. B., andN. P. Revsbech,
Oxygenuptake,bacterial
distribution,
andcarbon-ni-
trogen-sulfur
cyclingin sediments
fromthe BalticSea-NorthSeatransition,
Ophelia,
31(1), 29-49, 1989.
Kaas,H., H. H. Kaas,andF. M•hlenberg,
Upwarddirected
transport
of nutrients
saltsto
thephoticzone(in Danish),in PlanktonDynamicsandCarbonandNutrientFlowin
Kattegat,
editedby T. Fenchel,
Havforskning
fra Milj•styrelsen,
10, 121-136,Danish
Environmental
Protection
Agency,Copenhagen,
1992.
Ki•rboe,T., andT. G. Nielsen,Effects
of windstress
on verticalwatercolumnstructure,
phytoplankton
growth,andproductivity
of planktonic
copepods,
in TrophicRelation-
shipsin theMarineEnvironment,
editedby M. Barnes,
andR. N. Gibson,
pp.28-40,
AberdeenUniversityPress,
114 5. CarbonFlow in theWaterColumn
Kiorboe,
T., andT. G. Nielsen,
Mesozooplankton,production
andgrazing(in Danish),
HavlCorskning
•Cra
Mil/ostyrelsen,
10,77-101,Danish
Environmental
ProtectionAgency,
Copenhagen,1992.
Kiorboe,
T., Turbulence,
phytoplankton
of pelagicfoodwebs,
Adv. Mar. Biol., 29, 1-72, 1993.
Kiorboe,
T., andT. G. Nielsen,
Regulationof zooplankton
biomass andproduction in a
temperate,
coastal
ecosystem.
1. Copepods.Limnol.Oceanogr.,
39, 493-507,1994.
Kronvang,B., G. œrtebjerg,
R. Grant,?. Kristensen,
M. Hovmand,andJ. Kirkegaard,
Nationwide monitoring
of nutrients
and theirecological
effects:Stateof the Danish
AquaticEnvironment, Ambio,22(4), 1993.
McLaren,I. A., Generation lengthsof sometemperate copepods: Estimation,
prediction,
and
implications,]. Fish.Res.BdCan.,3S, 1330-1342,1978.
Nielsen,T. G., andT. Kiorboe,Effectsof a stormeventon thestructureof the pelagicfood
webwithspecial emphasis onplanktonic ciliates,
]. Plank.Res.,13, 35-51, 1991.
Nielsen,T. G., and T. Kiorboe,Regulationof zooplanktonbiomassand productionin a
temperate,coastalecosystem. 2. Ciliates,Limnol.Oceanogr., 39, 508-519, 1994.
Nixon, S. W., Quantifyingthe relationship betweennitrogeninput and the productivityof
marineecosystems, NixonPro.Adv.Mar. Tech.Con/C., S, 57-83, 1992.
C)lesen,
M., Thefateof anearlyspringbloomin theKattegat,Ophelia,37(1), 51-66, 1993.
Olesen,M., Comparison of thesedimentation of a diatomspringbloomandof a subsurface
chlorophyllmaximum,MarineBiology,/21, 541-547, 1995.
Olesen,M., and C. Lundsgaard, Sedimentation of organicmaterialfrom the photiczonein
thesouthern Kattegat(in Danish),HavlCorskning •Cra
Mil/ostyrelsen,
10, 167-183, Danish
Environmental ProtectionAgency,Copenhagen,1992.
C)lesen,
M., andC. Lunds•ard, Seasonal sedimentation of autochthonous
materialfromthe
euphotic zoneof a coastalsystem, œstuar. Coast.SheffSci.,1995,in press.
Pedersen,F. Bo, Hydrographicconditionsin the southernKattegat(in Danish),HavlCorsk -
ninglCraMiliostyrelsen,
3, DanishEnvironmental ProtectionAgency,Copenhagen, 1991.
Peterson,B.J., Aquaticprimaryproductivity andthe •4C-CO2method:a historyof the pro-
ductivityproblem,Ann.Rev.Ecol.Syst.,I •, 369-385, 1980.
Pettersson,H., Scatteringand extinctionof light in sea-water,MeddelandenG/3teborgs
H/3gskolas Oceanografiska Institution.,4b(4), 1934.
Planl•egningsrfidet
for Forskningen, Nitrogenand phosphorusin the water environment:
consensus report(in Danish),Planlmgningsrfidet for Forskningen,
Forskningssekretariatet,
Copenhagen, Denmark,1987.
Redfield,A. C., The biologicalcontrolof chemicalfactorsin the environment,Am. Sci.,46,
205-222, 1958.
Richardson,K., andA. Christoffersen,Seasonal distributionandproductionof phytoplank-
tonin thesouthern Kattegat,Mar. Ecol.Prog.$er., 78, 217-227, 1991.
Richardson,K., andJ.P. Heilmann,Primaryproductionin the Kattegat:Pastand present,
Ophelia,41,317-328, 1995.
Rosenberg,R., R. Elmgren,$. Fleischer,P. Jonsson, G. Persson,and H. Dahlin, Marine eu-
trophication casestudiesin Sweden,Ambio,19(3), 102-108, 1990.
$teemann Nielsen, E.,Theuseof radio-activecarbon(CTM) for measuring
organicproduction
in thesea,]. Cons.Intl Explor.Mer., 18(2), 117-140, 1952.
Steemann Nielsen,E., Investigations
of therateof primaryproduction at two Danishlight
shipsin the transitionareabetweenthe North Seaand the Baltic,MeddrDanre.Fisk.-
Havunders.,4(3), 31-77, 1964.
Thomsen, H. (Ed.),Planktonin the InnerDanishWaters(in Danish),Havforskning
fra
Miljostyrelsen,
11, 331 pp., DanishEnvironmentalProtectionAgency,Copefihagen,
6
Material Flux in the Sediment
BoBarkerJorgensen
Introduction
Marinesediments accumulate in the coastalzoneduringinterglacial periods,i.e.

overthelastca.6000yearssincetheseareached itspresentlevel,anderodeduring
glaciations.About90% of theglobalflux of riverineparticulates andorganiccar-
bonis currentlytrappedin deltaicand shelfregions[Gibbs,1981].Due to the fer-
tilizationby rivers,by coastalupwelling,or by intrusionof deepslopewateronto
theshelf,about30% of theoceanic primaryproduction takesplacewithinthe10%
of the oceanareawhichencompasses shelfand coastalsystems.Some25-50% of
theorganiccarbon,nitrogen,andphosphorus producedby the localplanktoncom-
munitiessinks out of the water columnto the sediment[Wollast,1991]. Most of
thedeposited organicmatteris, however,againmineralized andonlyabout10% of
it becomesmorepermanentlyburiedand contributes to the meanorganiccontent
of 1-3 % dry weightin shelfsediments[Berner,1982].
Dueto their largestoragecapacityfor organicmatterand nutrients, the sediments
havean importantregulatoryandbufferingfunctionin thecoastalecosystem. They
affectthe seasonal
oxygenbalanceof the bottomwatersand,throughtherelease of
nutrientsto the water column,alsoaffectthe seasonalphytoplanktonproduction.
Dueto the highrateof microbialmetabolism in coastalsediments,theyconstitute
an anoxicworld whereonly a thin layerbeneaththe surfaceand aroundanimal
burrows containsoxygen.The depthof theoxic-anoxic interfacechanges overthe
year,depending on the deposition
rateof organiccarbonandtheoxygenconcen-
trationin the overlyingwater.The sediments andthe benthiccommunities are,
therefore,the mostsensitivepartsof the coastalecosystem to eutrophicationand
hypoxia.
Whentheoxygensupplyfallsor thedemand
increases,
dramatic
changes
occurin the benthos,in the dominantmetabolicpathwaysof microbialprocesses,
Eutrophicationin Coastal Marine Ecosystems

Coastaland EstuarineStudies,Volume 52, Pages115-135
Union
116 6. Material Flux in theSediment
in thesediment
chemistry,
andin thenutrientfluxto theoverlying
water.These
phenomena andtheirdependence
oneutrophication arediscussed
in thischapter,
usingmostlydata fromDanishwaters.
6.2. SedimentTypes
The seafloorof thecomplexestuarine
system
extending
from the BalticSeainto
theNorthSea(Figure6.1) developed
asa submerged
glaciallandscape,
shapedby
theextensive
icecoversmorethan20,000 yearsago.Meltwaterdepositsare stillex-
posedinsome areas.Extensive
fine-sandsediments occurin theNorthSeaandinthe
western Kattegatwheremudaccumulation is preventedby currentsandespecially
bywaveactionreaching downto therathershallowbottomat depthsof ca.30 and
20 m, respectively.
Mud accumulation, at a meanrateof ca.500 g m-2 yr-•, occurs
mostlyin deeperareasor in protectedbasinsalongthe coasts,suchas in the Belts
and the westernBaltic[Madsenand Larsen,1986]. On the southernand western
slopesof thedeep,glaciallyerodedtroughin the Skagerrakand northeastKattegat,
thesediment buildsup at highratesof 2-4 mm yr-• [vanWeeringet al., 1987].
Hard bottom
':""•
'"":::""
(sand,
gravel)
[vS-q Wadden Sea
Sandymud
Greymud
Blackmud
25 (! 25 5(} 75 Jill) km
AARHUS
BAY
...
..
.....
.... •::-:-z.x.;-•.:-x.z-•-:.:-k.
•4'
....
...
i:===========================================
'"
Figure
6.1.Sediment
typedistribution
fromtheBaltic
SeatotheNorthSea.[FromLarsen,
Jorgensen 117
In a depositional
fanin thenorthern
Kattegat
upto 10 mmyr-1of mudaccumula-
tionhasbeenmeasured. Theorganicsedimentation
rate,230g org.C m-2yr-•, is
hereof thesamemagnitude asthelocalphytoplankton
productivity
(cf.chapter5).
The areacoversonly 10% of the area of innerDanishwatersbut accumulates
40%
of thetotalmudsedimentsand35% of theorganic
matter[Madsen andLarsen,
1986].Themainsources
of thefine-grained
sediment
arethelargeNorthEuropean
riversdischarging
intothe southeast
North Sea.Fromthere,muchof thematerialis
carriedintothe Skagerrak
andKattegatby theJutlandCurrent,aftermanysedi-
mentation-resuspension
cyclesin theNorth Sea[e.g.,EismaandKalf,1987].Some
40-50% of the organiccarbon,whichis deposited
on the seafloorin the northern
Kattegatarea,alsoaccumulates there.Thishighfractionis explained
by thepoor
degradabilityof the organicmaterialafterthe longtransportfromthe North Sea
[Jorgensenet al., 1990].In otherareasof Danishwaters,only10-15% of thede-
posited
org.C resists mineralizationbeforeburialbelow1-2 m of sediment.
Theseburial fractionscorrespond well to the averagevaluesfor coastalsediments
andalsoreflectthe generaltrendof higherburialefficiency of organicmatterat
highersedimentation rates[HenrichsandReeburgh, 1987].The burialefficiency
of
organiccarbonand nutrientsis generallyhigherin the absence of oxygenand of
bottomfauna. This has beendemonstrated mostclearlyfor permanently anoxic
(euxinic)basins[Canfield,1989], whereasthe effectof only intermittenthypoxia,
which occursin Danish coastal waters, still remainsto be demonstrated.Benthic
animalsare importantfor the mechanicaldegradationof detritusandfor the main-
tenanceof a mixedsedimentzone,mostly3-6 cm deep[MadsenandLarsen,1986;
van Weeringet al., 1987; chapter7, this vol.], in whichthe organicmatteris ex-
posedto oxygenat intervals.
The degradationof organicmattercontinues at decreasing
ratesdeepdownin the
sediment,even into the sulfate-depleted
zone belowseveralmetersdepth,where
the microbial metabolismleads to methane formation. As a result, the methane
pressurebuildsup in the sedimentof manyof the Danishcoastalbasinsto above
theambienthydrostatic pressure.Thus,themethane formsgasbubbles trappedin
the sediment,which can be seenas acousticscatteringlayersat 2-5 m depthin
seismicprofiles.Methanefrom deepersources in thenorthernKattegatandSka-
gerraksediments alsoescapes asbubblesintothewatercolumnandcreates "pock
marks"at the sedimentsurfaceor causesthe formationof carbonatechimneysasa
resultof methaneoxidationto CO2 within the sediment[Jensenet al., 1992; Dan-
doet al., 1994].Thesesediment
localities
harbora special
andinteresting
faunaof
pogonophores andbivalveswithsymbioticmethane- or sulfide-oxidizing
bacteria
in their tissue.
6.3.Depositionof OrganicMatter
Themainsource
of organic
matterto estuarine
andshelfsediments
isthedeposi-
tionof detritalmaterialfromthelocalplanktoncommunity
in theoverlying
water.
Consequently,
thereisa roughcorrelation
between
thephytoplankton
primary
118 6. Material Flux in the Sediment
ductivity,the waterdepththroughwhichthe detritussinksunderprogressing de-

composition, and the primarysedimentation on the seafloor [e.g.,Suess,1980;
Hargrave,1984].Thereare,however,manyfactorswhichcomplicate anddelaythe
couplingof theseprocessesto the benthicmetabolism,includingthe seasonaltem-
perature,the degradability
and decaytimeof the organicmatter,the burialof or-
ganicmatterinto anoxicsedimentlayers,or the resuspensionand lateraltransport
of organicmatterto deeperor lessexposedareas.
As an example,organic-rich ephemeralmudblanketsin LaholmBayon the Swed-
ishKattegatcoastwereobserved to form on the moresandysedimentsurfaceafter
the sedimentation of the springphytoplanktonbloom [Floderusand Hfikanson,
1989]. Duringsuccessive resuspensioncycles,thesemud blanketsweretransported
out of thebayandintothedeeperpartsof the Kattegat.Lateraladvectionwassim-
ilarlyfoundto redistribute thedepositedorganicmattertowardthe deeperpartsof
the Kiel Bightin the westernBalticSea("sedimentfocusing"[Balzeret al., 1986;
Graf, 1992]). The distributionof sandyand muddysediments in Figure6.1 shows
areasof relativeexportandimport,respectively, of organicmaterialthroughlater-
al advectionof organic-richsediment.Althoughthe organicmaterialmay be rela-
tively refractoryafter manyresuspension cycles,it potentiallyenhancesthe local
oxygendemandand nutrientreleasewithin the sedimentationbasins.Thesebasins
tendto haveorganic-rich
sedimentsand develophypoxiain the poorlyventilated
bottom water.
The flux of organicmatterto the sedimenthasbeenmeasuredby sedimenttraps

suspended at differentdepthsin the watercolumn.It is difficultin shallowcoastal
systems to determinethe net flux of primarysedimenting materialon the back-
groundof a muchlargergrossflux of resuspended sediment.A discrimination be-
tweenprimaryand secondary sedimentationhasbeenmadein somestudiesby the
useof freshchlorophyll or otherchemicalconstituents for correction[e.g.,Kemp
andBoynton,1992]. Dueto the salinityandtemperature stratificationof the Baltic
SeaandKattegatwaters(chapter3), theupwardtransportof resuspended sediment
ismostof theyearblockedby thepycnocline, andsediment trappedabovethispyc-
noclineis,therefore,representative
of thenetdeposition.
In a fieldstudyin theAarhus
Bay(chapter
7) thi•;blocking
effectwasusedto dis-
criminateseasonal grossand net depositionrates(Pejrupet al., submitted).The
datain Figure6.2 showa halo-andthermocline at 8-13 m depth,belowwhichthe
amountof particulatematerialcollected
bythetrapsincreased exponentially
down
towardthesediment surfaceat 16 m depth.Byextrapolation of sediment
trapdata
from0-11 m downto 16 m, a netdeposition of 2.9 g m-2 d-1wasdetermined. Due
to frequent
resuspension,thegrossdeposition was30-foldhigher,eventhoughthe
dataperiodwasa relativelycalmsummer witha well-developed pycnocline.
Thefractionof theprimaryproduction in coastalwaters,whichis deposited
to the
sediment,is mostlyin the rangeof 25-50% of the primaryproductivity[Nixon,
1981;Wollast,1991].With a productivityof eutrophiccoastalwaterssuchas the
Kattegatof 250-300 g C m-2 yr-•, the meanorganiccarbonflux to the sediment
shouldbe in the rangeof 75-150 g C m-2 yr-•. The annuallydeposited
Jorgensen 119
5
I
10
I
15 f øC 2O
I I
15
I
20
I
25 S%o,,30
, I I__
0
10-
15-
, ,,
5•) 100 150

g m-2d
-1
Figure6.2. Sediment trapdata:Totaldryweightof sediment (o), trapped
at different
water
depthsduringJuly2-26, 1990,in centralAarhusBay.Fp= flux of primarysediment; F, =
totaldownward fluxof sediment; D, = netdeposition
rate;Dg= gross depositionrate.(Data
fromValeuret al. [1992]).Salinityandtemperature
stratification
measured onJune21, 1990,
demonstratesa pycnocline at 8-13 m depth.(AarhusAmtskommune, unpublishedreport).
in the 10-30 rn deepBalticand Kattegatwaterswas:26% in southernKattegat

(chapter5), 32-45% in AarhusBay(chapter7}, andabout30% in the Kiel Bight
[Smetacek,1980].
Thefractionof the phytoplankton productionwhichsinksout of theeuphoticzone
mayvary stronglyoverthe year.Thereare manyexamples of therapiddeposition
of the springbloomof diatomswhich,uponnutrientdepletionor dueto wind-dri-
venturbulence,suddenlyaggregate and overa few daysor weekssinkto the bot-
tom (chapters 4 and5). The largerthe bloomandthefasterit develops, the smaller
a fractionappearsto begrazedor mineralized in thewatercolumn,andthemoreis
deposited[e.g., Smetacek,1985]. This was alsothe casein the Kattegatwhere,
however,the springbloomaccounted for only8% of theyearlynetcarbonflux to
the sedimentand sedimentation wasfoundto proceedat a steadyrate throughout
the phytoplanktongrowthseason[OlesenandLundsgaard, 1995].Due to the sud-
dendeposition of thespringbloomandof blooms,whichmaydeveloplaterduring
thesummerjustbelowthe pycnocline, burstsof bacterialgrowthandmetabolic ac-
tivity occur at the sedimentsurface[Graf et al., 1983; Meyer-Reil, 1983]. These
burstsappearto fadeout againwithin2-4 weeksasthemostlabileorganicmateri-
al is depletedandthe restof it becomes buriedinto the sediment[e.g.,Hansenand
Blackburn,1992;chapter7, this
120 6. MaterialFluxintheSediment
10
mm SEA WATER
-5
OXYGEN
-10
-15
SEDIMENT
I
-2o
50 100 150 200 250

•M
mm SEA WATER
1.5
OXYGEN
0.5
SEDIMENT
I I I
-0.5
190 195 200 205 210 215

•tM
Figure6.3. Oxygendistributionacrossthe sediment-waterinterfacemeasuredin situ at 600

m water depth in central$kagerrakby a microelectrode mountedon a benthiclander,
"Profilur".The data are presentedat two differentresolutionsto demonstrate(top) the
sharpoxic-anoxicinterfaceona macroscopic scaleand(bottom)theoccurrence of a $00
thickdiffusive
boundary layerin whichthe100-•m depthintervals
of oxygenmeasurements
arejustsufficient
to allowaccuratediffusionfluxcalculations.
[Gundersen
et al.,
Jorgensen 121
Thecontribution
ofterrestrially
derivedorganic
material tocoastal
waters
isgener-
allypoorlyknownbutis estimatedto besmallrelative
to theplankton
material.
Thus,althoughbothligninandpolysaccharide
components ofvascular
plants
were
identified
in sediment
trapmaterialfroma semienclosed
bayonthePacific
Coastof
Washington,USA,theytogether comprised <10-35%of thetotalsedimenting or-
ganic
carbon[Hedges etal., 1988].Thecontribution
of particulate
organicmaterial
fromlandto theKattegat
wasestimated to bein average8 g C m-2yr-• equivalent
to 3% of theprimaryproduction
[Olesen
andLundsgaard,
1995].
6.4.The Sediment-Water Interface
Thesedimenting organicmaterialisprimarilymineralized by aerobicmicroorgan-

ismsandanimals ontheseafloor.Theoxic(i.e.oxygen-containing) zoneof coastal
sedimentsis, however,generallyrestricted
to a few millimetersthinlayerat the
sedimentsurfaceand surrounding the burrowsof macrofauna [Revsbech et al.,
1980;Jorgensen andRevsbech, 1985].Thisoxiclayercomprises onlytheupper-
mostpart,oftenonly10-20%, of thebrown(oxidized) sediment layer[Jorgensen
andRevsbech, 1989].Althoughtheoxygenuptakeis regulated overallby thenet
deposition
anddegradabilityof organicmatter,themechanism anddynamics of the
oxygenuptakearecomplex.Oxygenpenetrates intononpermeable sedimentsmost-
ly by moleculardiffusionthroughthediffusiveboundarylayer,whichconstitutes
an 0.2-1 mm thick, unstirredwater film overlyingthe sediment.This boundary
layeris apparentfrom highresolutionmeasurements with oxygenmicroelectrodes
applieddirectlyon the sea floor [Gundersen and J•rgensen,1990]. Figure6.3
showsan examplefrom the deeppart of the Skagerrak,at 600 m waterdepth,
whereoxygenpenetrated13 mm into the sediment.
By diffusionflux calculations from boundarylayeroxygengradients or by diffu-
sion-reaction modelingof the wholeoxygenprofilein the sediment, the respiration
rate in the oxic surfacelayer can be calculated(Figure6.4). Duringsummer,there
is often a maximumin respirationrate at the lower boundaryof the oxic zone
wherereducedcompounds suchas ammoniumdiffuseup from belowand areoxi-
dized,e.g.by nitrifyingbacteria.In sediments of thesouthernKattegatandAarhus
Bay,it was foundthat the diffusiveuptakeaccounted for 45-65% and 70%, re-
spectively, of the total oxygenconsumption measured in sediment cores[Rasmus-
senandJorgensen, 1992]. The unaccounted uptakeis mostlydueto biopumping
and respirationof burrowingfaunaand the relativedifference betweendiffusive
andtotal uptakeis, accordingly, closelyrelatedto the densityof benthicanimals
[Gludet al., 1994; cf. chapter8, this vol.]. Furthermore, the interactionbetween
theoverflowing seawaterand sediment surfacetopography creates
lateralpressure
gradients which,in poroussediments, maydrivean advective porewatertransport
through thesediment and,thereby,enhance theoxygen consumption andexchange
of nutrients[Hiittel andGust,
02 [ •JH) 02
0 50 100 150 200 ._250 0 100 200 •00 0 100 200 30o
'", i i i i --
I
05,'-......... '_'__
..c:: '
oo o'• oi'•' o'.6 o.• 0.0 0i2 I

0/, I
0.6 08
02 consumpfion
(]JmO[
cn•3h
-1) 02consumption
JHmol.
crn-3h-1)
Figure6.4. Oxygendistributions measured in situin a coastalsediment(AarhusBay, 16 m
waterdepth).Left:Oxygengradientsin thediffusiveboundarylayerare usedto calculatethe
diffusiveflux into the sedimentas the simpleproductof gradientand diffusioncoefficient.
Centerandright:Oxygengradients before(a) andafter (b) the depositionof a springphyto-
planktonbloomin lateMarch.The thickness of theoxiczonevariedfrom4.8 mm (a) to 1.2
mm (b) overthe year.The rate of respirationin the oxic zonewas calculatedper unit sedi-
mentvolumeby a zero-orderdiffusionreactionmodel.Beforethe sedimentation event,the
rate of respirationwas uniformthroughoutthe oxic zone.After the event,the respirationin
the much thinner oxic zone had increasedseveral-fold,with a maximum at the oxic-anoxic
interfaceat 1.2 mm depth.The calculatedareaoxygenuptakerate increasedfrom 265 (a) to
550 (b) •mol 02 m-2 h-• followingthesedimentation
event.FromRasmussen
andJorgensen
[!992].
6.5. Anaerobic Mineralization Processes
The degrationand oxiditionof the organicmatterbelowthe thin oxic zoneis most-

ly carriedout by microorganisms. Someof theseorganismshydrolyzeand ferment
the macromolecules to smallorganiccompounds,while othersuseoxidantsother
than 02 to respirethecompounds to CO2.Althoughthe net resultof carbonoxida-
tion may be similar, there are major differencesbetweenthe anaerobicand the
aerobicfoodchains,in whichthe organisms basicallyhavea very uniformenergy
metabolism, theaerobicrespiration.The anaerobic, microbialfoodchaincomprises
a depthsequence of metabolictypes,eachof whichis onlyableto exploita fraction
of theenergy availablein theorganicmatterandeachof whichexcretesenergy-rich
inorganicor organicproducts,which can again be oxidizedwhen they reachup
into the overlyingchemical zones.Table6.1 showsa rangeof suchredoxreactions
whichmay be catalyzedby bacteria.Someof thesemay alsoproceedchemically,
e.g.theoxidationof Mn2', Fe2*or H2Sby 02.
Thereis a moreor lessdistinctverticalzonationof the dominantenergymetabo-
lismsin coastal
sediments,witha) aerobicrespiration in theuppermost
fewmm,b)
nitraterespiration(denitrification)
in the followingfew mm-cm, c)
Jergensen 123
TABLE 6.1. Mineralizationprocesses in marinesediments

by whichorganicmatterbe-
comesoxidizedwith differentelectronacceptors.
The reoxidation
of thereduced
products
withoxygenisalsoshown.AfterCanfieldeta!. [19931.
02 respiration:
CH20 + 02 --> CO2 + H20
Denitrification'
CH20 + 4/5NO3-+ 4/5H*-4 C02 + 2/3N2+ 7/5H20
Mn reduction:
CH20 + 2MnO2 + 4H* • 2Mn2++ 3H20 + CO2
2Mn 2++ 02 + 2H20 • 2MnO2 + 4H +
CH20 + 02 --->CO2 + H20

Fe reduction:
CH20 + 4FeOOH + 8H + ---)4Fe2++ CO2 + 7H20
4Fe2++ 02 + 6H20 • 4FeOOH + 8H +
CH20 + 02 -• CO2 + H20

Sulfate reduction:
CH20 + 1/2SO42-
+ H + -'• CO2 + ¾2H2S+ H20
•/2H2S+ 02 --) ¾2SO42- + H+
CH20 + 02 -'> CO2 + H20
Methanogenesis:
CH20 ---)1/2CH4+ 1/2CO2
•/2CH4+ 02 •/2CO2 + H20
CH20 + 02 --> CO2 + H20

NH4 + oxidation:
NH4 + + 202 --->NO3-+ H20 + 2H +
(Mn(!V))andd) iron (Fe(III))reduction

in themainpart of thebrownoxidized
sediment,
whichmaybea fewto tencentimeters deep,e) sulfate
reduction,
which
mostly
extendsasthedominant process
downtooneorseveral metersdepth,
andf)
methanogenesis,
whichistheterminal
metabolism
fororganic
matter
afterdepletion
of the mentionedoxidants.Denitrificationis in thiscontextexceptional
in that the
reducedproduct,N2,hasa stabletriple-bond,
whichrenders it useless
asanenergy
substrate,
evenin thepresence of oxygen.Ammonium released bytheanaerobic
degradation
ofnitrogen-containing
organiccompounds is,however, anexcellent
en-
ergysubstrate
usedbythenitrifying bacteria.
Although nitratemaybereduced di-
rectly
to ammonium byseveraltypes of anaerobic
bacteria,theprocessisofmuch
less
significance
thandenitrification
inmarinesediments[e.g.,Binnerupetal.,1992].
Denitrification
isofmajorimportance forthenitrogen
cycle andnutrient balancein
estuaries
andmayreachhighratesundercertain conditions, suchashigh
124 6. MaterialFluxin theSediment
FMday-• HMday-• pM day-•

20 40 60 80 0 20 40 60 80 0 20 40 60 80
I ,, , i I I •
Depth, cm I
31 3
Manganesereduction Iron reduction Sulfate reduction
Figure6.5. Distributions
of manganese,
iron,andsulfatereductionratesin sediment from
northernKattegat.The Mn(IV) and Fe(III) reductionratesweremeasuredfrom the accu-
mulationof Mn2+and Fe2+in the presence of molybdateto inhibit sulfatereduction.
Sulfatereductionwasmeasuredin a separateincubationby radiotracertechnique.From
Canfield[1993].Reprintedby permissionof Springer-Verlag.
load or intensivebiopumping (1-3 mmolNO3- m-2 d-1, Sorensen et al., 1979;

Seitzinger,
1988]. Nevertheless,the processwas found to accountfor only a few
percentof the organicmatter oxidationin most Danishcoastalsediments,with
valuesincreasingto 3-6% in the Skagerrakat 400-700 rn depth [Canfieldet al.,
1993b; Nielsenet al., 1994]. Oxidized mineralsof manganeseand iron in the
brownsediment layercan,however,beusedasrespiratory electronacceptors for
the oxidationof organiccarbonby certainbacteria[e.g.,Lovley,1987; Burdige,
1993]. Alternatively,
theycan serveas oxidantsof sulfideproducedin the sedi-
mentby bacteriarespiring sulfateand,thus,contributeonly indirectlyto the oxi-
dationof organicmatter[Aller, 1994].It is experimentallydifficultto determine
theratesof metalreductions or to discriminatetheirrolesin organiccarbonoxi-
dation.Much informationon processes and rates,therefore,derivesfrom model-
ing of geochemicalgradients in deepersediments. By combinations of chemical
andradiotracer methods it has,however,beenpossible to demonstrate themutu-
al zonation
of thethreeprocessesin coastal
se;diments [Canfieldet al., 1993a].
Althoughthereis significant
overlap(Figure6.5), the depthdistribution of the
oxidationprocesses
clearlyfollowsa depthsequence of decreasingredoxpoten-
tialandenergyyield.Thesequenceisprobably determined bycompetition among
theanaerobically
respiringbacteria
for common organic substrates[e.g.,Lovley
and Phillips,1987].
Theironcycling isof particular
interest,
becauseFe(III)mineralsbindphosphate
andthusregulate itsrelease
fromthesediment. In addition,ironbindsthelarge
amountsof sulfideproduced.Althoughmanganese generally
occurs in muchlower
concentrations
thaniron,Mn(IV)mineral phaseshavea fasterturnover(chapter
7).
Dueto themuchslower 02 oxidationkinetics
of reducedmanganese thanof re-
ducediron,Mn2+mayescape throughthethin,oxicsedimentzoneandupinto
Jorgensen 125
•t
18 20
15
E10
øt 02 E
E 20
o
• 5
3O
0 40 ...........
0.0 O.2 O.4 0.6
Mn2•',,•M
lob 260 •00

02, uM
Figure6.6. Distributionsof dissolvedmanganesein the watercolumn(left)and in the sedi-

mentpore water (right)in AarhusBay on threedifferentdaysin August,1992. The water
density,crt,showedthat a pycnocline createdstablewaterstratification
in the lowest5 m,
downthroughwhich the oxygenconcentration droppedsteeplytowardthe bottom(left).
One third of the Mn 2+ flux from the sediment was reoxidized near the sediment surface
while two thirds diffused out of the sediment into the lower water column where it was oxi-
dizedto MnO2 andsubsequently redeposited.
FromThamdrupet al. [1994],andGundersen
et al. [1994]. Reprintedwith permission
fromElsevierScience
Ltd.
watercolumn(Figure6.6). There,it is subsequentlyoxidizedto MnO2 andis again

depositedbut at a differentlocationdue to lateraltransportby bottomcurrents.
Throughhundredsof suchemission-deposition cycles,manganese may gradually
moveaway from the organic-rich,reducedcoastalsediments to finally become
trappedin more oxidizedsediments on the continentalslope.In the 700 m deep
troughin central$kagerrak(seemapin chapter1), migratingmanganese oxidesare
focusedtowardthe deepest sediments in whichmanganese aloneconstitutes
up to
5% of the dry weightin the upper5 cm.Mn(IV) is herethemainoxidantfor the
mineralization
of organicmatter[Canfieldet al., 1993b].At intermediate
depthsof
around400 m in theSkagerrak, Fe(III)wasthemostimportantoxidant.
In organic-richcoastalsediments,mostanaerobicmineralization
is by sulfatere-
duction, whichmayherebeof similarimportance andefficiency
asaerobic respira-
tion for the oxidationof organiccarbon[Jergensen,
1982; chapter7, thisvol.].
Sulfate
respiration
proceeds
at steadily
decreasing
rateswith depthdownto
126 6. MaterialFluxin the Sediment
depletion
of sulfate
at several
meters
belowthesediment
surface,
wheretheme-
thanogenic
bacteria
thentakeover.
Thelarge
amounts
ofH25formed
bythesulfate
reducers
dominate
thechemistry
of thesediments
in whichblackironsulfides
(FeS}
and,especially,
pyrite(Fe$2)
accumulate.
Calculated
aspotential
oxygen
demand,
theburialof Fe$2in thesecoastalsediments is equivalent
to 10-25% of theburial
of organic
carbon[J•rgensen et al., 1990].
Depending
ontheavailability
ofoxidants,
theH25iscontinuously
reoxidized
inthe
sediment.
The removalof sulfideis importantfor the benthicfaunadueto thein-
terference
of H25with theaerobicrespiratorysystem(chapter8). The H2Soxida-
tionappearsto takeplacemostlyin theanoxicsedimentthroughthepartialoxida-
tionandbinding of sulfidebymanganeseandironandthesubsequent transportof
ironsulfides
upto thesurface layerswhere02 istheterminaloxidant(chapter7).
Onlyat veryhighorganic loading
of thesedimentor duringhypoxiaarethereac-
tiveMn(IV) andFe(III)poolsdepleted andH25mayreachdirectlyup to the oxic
layer.There,sulfurbacteria
carryouttheoxidationin a narrowzone(ca.0.1 mm}
of overlapping, counter-diffusing
02 andH2S[Jorgensen andRevsbech, 1983].In
particular the filamentous
Beggiatoaspp.proliferate
and grow as sub-mmthin,
white filmson the FeS-blackenedsedimentsurface.Due to eutrophication,these
sulfurbacteria havespread
duringthelastdecadeconcurrentlywith theprogressing
hypoxia in NorthEuropeancoastalwatersandtheyhaveevenbecomea periodical-
ly dominantbottomcommunityin someareas.
6.6.NitrogenCycling
Nitrogenandphosphorus are depositedto the seafloor boundin sedimenting
algal
cellsandorganicdetritus,whichin the water columnundergopartialdecomposi-
tionwitha faster
loss
ofthenutrients,
N andP,•hanofcarbon.
Whenreaching
the
sediment, the organicmaterialis, thus,partly depletedin N and P relativeto the
Redfieldmolarratioof C:N = 6.5 andC:P = 106 in theplankton.Furthermineral-
izationin thesediment depletes theorganicnitrogento a C :N of >10. In the north-
ern Kattegat,whereextensivedegradationof the organicmatter has taken place
duringitstransportfromthe North Sea,the C:N is even15 at the sedimentsurface
and increases to >20 with depth[J•rgensenet al., 1990]. In contrast,the C:P ratio
is lowestat the sediment surfacebecause releasedphosphateaccumulates here,
boundto iron minerals. The C:P ratiosdeeperin the sedimentreach300-600 and
aregenerally maximalat sedimentation ratestypicalof shelfsediments, 0.1-.1 mm
yr-• [IngallandvanCappellen,1990].
A low C:N ratio is indicativeof relativelyfresh,undegradedorganicmatter.
Accordingly,
theseasonal isopleths of C:N in a sediment
fromAarhusBay(Figure
6.7) showthedeposition of the springdiatombloomin two consecutiveyearsand
itsrapidmixingdownto 4-6 cmdepthby bioturbation. A bloomof dinoflagellates
wasdeposited in August(cf.chapter7), whileduringtherestof theyeartheinflux
of nitrogen-rich
materialwas lower and the sedimentC:N remainedrather con-
Jorgensen 12 7
C:N, mot mot-'
Sediment depth. cm ß <,0.00

ß ,0.00-,025
ß,025-,050 1050-1075
ß1075-11
00ß >11
00
0
8
m A m j j A S O N D J F M A M
NO3. nmel cm•

Sediment depth. cm ß <250 ß 250-5O0 5.00-7
50 50--1000
ß>1000
0
'
2
t
3
8
M A M J J A S ¸ N D J F M A M
1991
1990
Figure
6.-.Isepleths
of(top)
C:Nmolar
ratios
oforganic
matter
and(bottom}
nitrate
inthe
pore
waterinamarine
sediment
from
Aarhus
Ba.•
during
1990-1991.
From
Lomsteinand
Blackburn[ 1992].
Duringthedegradation
el• theN-containing
compounds(mostly
proteins
andnu-
cleic
acids),
urea
(CO(NHz}z},
amine
acids
andother,
still
poorly
defined
dissolve
organic
nitrogen
(DON}
compounds
areproduced.
Inaddition
toammonium,
arepartlyreleasedto theoverlying water.Theureafluxappears to beof similar

magnitude asthe ammonium flux in several
coastalsediments
[Lornstein et al.,
1989;chapter7, thisvol.l.Ureaisexcretedasa nitrogen
wasteproductbytheben-
thicfaunaandisalsoproduced byseveralanaerobicbacteria
[Pealersen
etal., 1993].
Some50-75% of theammonium
produced
wasfoundto be nitrifledto NO3- in
differentshelfsediments of theNorth Sea,the Kattegat,and the BeringSea[Billen,
1978;Lornstein andBlackburn, 1992;Henriksen et al., 1993].Thereis a complex
balancebetweenthea) flux of ammoniumandDON into the water, b) nitrification
of ammoniumto nitrate,c) flux of nitrateinto the water,and d) alenitrificationof
nitrateto N2.Thus,biopumping by theinfaunaenhances theadvective ammonium
flux,whichmaybypass thenitrification
zone,butat thesametimethebiopumping
bringsoxygendownintotheanimalburrowsand,thereby,expandsthe nitrifica-
tion zone.Nitrificationis alsosensitiveto eutrophication which may changethe
balanceof oxygenandammonium fluxesawayfromtheoptimum[Blackburn and
Blackburn,1992].Nitrificationmay,thus,be stronglyimpededby hypoxiaand by
highorganic depositionwiththeresultthatammonium is directlyreleased
into the
water[Klumpand Martens,1987; Caffreyet al., 1993]. Sincea largepart of the
alenitrification
is dependent on NO3- producedby nitrification,alenitrification is
alsoimpeded, therebyremovinglessN nutrientsfromthe ecosystem. Thispositive
feedbackmechanism thus tendsto enhancethe adverseeffectsof eutrophication
[Kempet al., 1990].
Denitrification takesplacejustbelowthe O2 zoneand is limitedby the availability
of nitrateenteringby diffusionor biopumpinginto the anoxicsediment.The zone
of alenitrification
maybeonly 1-2 mm thick,similarto the O2 zone,asshownfor a,
Danishestuaryby microelectrode technique[Binnerupet al., 1992]. Denitrification
mayalsoextendto oneor severalcentimeters, deepestwhenthe nitrateconcentra-
tion in the overlyingwater is high and the microbialactivity is relativelylow
(Figure6.7}. Due to the shortdiffusionpathbetweenthe O•_and NO3-zones,cou-
pled nitrification-denitrification
seemsto dominateover nitrate comingfrom the
watercolumnin manycoastalsediments. If, however,the bottomwater concentra-
tion exceeds 30-50 IzM NO•- or if nitrificationis suppressed,e.g. by hypoxia,ex-
ternalnitratebecomes themoreimportantsource[Nielsenet al., 1994]. In spiteof
large seasonaland spatialvariationsin alenitrification,it has been observedin
Danishcoastalsediments that severalcounteractingfactorsaffectingthis process
leadto a ratherconstantdenitrificationrate over the year of around400 Izmol N
m-•-d-• [Nielsenet al., 1994].
The removalof combinednitrogenby alenitrification
in estuariesand costalenvi-
ronmentsis importantfor the nitrogencycleand crucialfor the understanding
of
theeffectsof eutrophication
(seechapter9). Thefractionof thetotalnitrogeninput
to differentcoastalecosystemswhichis removedagainthroughthis process has
beenestimated to rangefrom10% to >60% [e.g.,Mantouraet al., 1991].Although
for a numberof estuariestheestimated valuesfall mostlyin the rangeof 30-50%
[Seitzinger,
1988],theefficiencyis oftenmuchlowerandis stronglydependent on
the retentiontime of the estuarinewater mass[Nielsenet al., 1994]. The burial
Jergensen 129
organicnitrogenconstitutes a smallercomponentin theN budget,beingequivalent

to about1% of the annualN requirement for primaryproductionin innerDanish
waters[Jergensenet al., 1990].
6.7.Phosphorus
Cycling
Althoughphosphorus doesnot undergoreduction-oxidation processesin marine
sediments, its chemistryis complicatedby the diverseformsof bindingin organic
and inorganicphases,and much researcheffort hasbeendevotedto methodsfor
the identificationof thesepools.Much of the phosphorus depositedon the sedi-
mentis boundin freshplanktonmaterialandisgradually released
to theporewater
duringmineralization. The freephosphate is rapidlyboundto oxidizedphases of
ferricoxyhydroxides and,to a lesserextent,to oxidizedmanganese,bothof which
arepresentin the oxidizedsurfacelayerof the sediment. In deepersedimentlayers,
wherethesemetaloxideshavelargelybeenreduced,the released phosphate accu-
mulatesin the pore water and diffusesup towardthe surfacewhereit may again
bind to excess FeOOH.
The distributionof the differentphosphatepoolsin relationto Fe(III) and Mn(IV)

is shownfor a Danishcoastalsedimentin Figure6.8 [Jensen andThamdrup,1993].
The dynamicpoolsof looselysorbedphosphate, iron-boundphosphate, and fresh
(i.e. leachable)organicphosphorus constituted
nearly50% of the total P in the up-
permost0-1 cm but werelargelydepletedbelow3 cm depth.Only the phosphate
poolsboundto clay minerals("adsorbedRP"), to calciumin apatiteor calcium
carbonateminerals("apatite P"), or to refractoryorganicmaterialwere present
belowthisdepth.Theseare the mainformsthat becomepermanently buriedinto
.1 .1
ParticulateP-pools,pmolg DW FeandMnoxides,
prnolg DW Pore-water
DRP,pM
0 10 20 30 40 50 100 0 10 20 30 40 50 60
0
•Retmctory
org.
P t•lApal•te-P I•• RP ..- BD-Mn. _ .. _ Fa(HCl)-Fell(oxaJate)
[;•bleorg.P IIIIron-boundRP
{'--]LooselysorbedRP
.e- BD-Fe
Figure
6.8.Depthdistributions of phosphorus,
ironandmanganese in Aarhus
Bay,February
1991.a: Phosphate poolsanalyzed bysequential
extractiontechniques;RP= ReactivePhos-
phorus.b: Iron andmanganese; BD-FeandBD-Mn= ironandmanganese extractedwith
Bicarbonate bufferedDithionite;for comparison,
Fe(III)calculatedfromthe difference
in
totalironextractedwith HC1andFe(II)extracted
withoxalate.c: solublereactive
phospho-
rusintheporewater.FromJensen
andThamdrup
[1993].Reprinted
bypermission
of Klu-
wer Academic
marinesediments [Berneret al., 1993].Throughthisburial,a fractionof thetotalP

influxto estuaries
istrapped,usuallyonlya few percent[Billenet al., 1991].
Duringmineralization,
thereis a net release
of phosphate into the overlyingwater
whichisstrongly
regulated
by the adsorption kineticsto amorphous FeOOH in the
surfacesediment.The FeOOH:PO4-3 ratio in Danish surfacesedimentswas 6.5-
16, neartheequilibrium of phosphatesaturation for thisironmineralphase[Jensen
andThamdrup,1993].Intermittent,partialreductionof the FeOOH pool dueto
hypoxiaor suddensedimentation of a phytoplanktonbloom causespeaksin the
phosphate flux into thewater.The restof the yearthe net flux is low andperiodi-
cally may changedirectiontoward sedimentuptake[Kempand Boynton,1992;
chapter7]. In contrastto fresh-watersediments, in whichalsoreducediron miner-
alsretaina certaincapacityto bindphosphate, the Fe(!I) in marinesedimentsmost-
ly reactswith sulfide.As a consequence,theP retentionin marinesediments is rela-
tivelylessefficientthanin fresh-watersediments. However,in both systems, a close
couplingexistsbetweenphosphorus andirongeochemistry.
6.8.Effectsof Eutrophication
andHypoxia
Amongthe manyeffectson sediments of increased
organicdepositionand of hy-
poxiain the lowerwatercolumnare:
- a shift in the balance of oxidants toward anaerobic mineralization and sulfate re-
duction,
- reducedbottomfaunaactivityand a shifttowardstrongerdiffusionlimitationof
solutefluxes,
- accumulation of metalsulfidesandof H2Sin the porewater,
- inhibitionof nitrificationandpreferential
releaseof ammonium,
- releaseof Fe(III)-boundphosphateto thewater column,
- releaseof H2Sin caseof severeoxygendepletion,
-enhancedburialof organiccarbonandnitrogenin thesediment.
Theoxidants
of thesuboxic
zonebetween
theoxygenandsulfaterespiration
zones,
i.e. NO3-, Mn(IV) andFe(III}, are moreimportantin offshoresediments
with lower
organicdeposition
thanin coastalsediments
[Canfieldet al., 1993].Byan increased
organicfluxdueto eutrophication,
theconsumptionrateof theseoxidantsincreases
more than their transportrate down into the sediment.The nitrate zone thus be-
comesverynarrowand limitingto alenitrification, manganese oxidesbecomere-
duced,and Mn 2' is lostto the water column.Also iron oxidesare reducedand the
Fe(II)is boundby sulfide.Eutrophication
preferentially
stimulates
sulfatereduction,
whichmayevenbecome
moreimportant
thanoxygenfor thedirectrespiration
of
organicmatter.Most of theoxygenuptakemaythen- directlyor with Mn andFe
asintermediateelectroncarriers
- beusedfor thereoxidation of thelargeamounts
of H2Sto sulfate.The developmentof whitefilmsof the filamentous sulfurbacte-
ria, Beggiatoa
spp.,on the sedimentshowthat the H2Sis now reachingthe very
surfaceandthatthebuffercapacity of theintermediate
oxidants hasbeen
Jorgensen 131
4OO
$00
200-,-
•00 TM
'0
Ooys
._.15
.e_10
.o_
0 Iøn
• Apr Jut Ocr Jan
1989 1990
Figure
6.9. Oxic-anoxic
transition
of sediment
fromAarhus
Bay.Sediment
cores
weresealed
gas-tight
withoutheadspace
butwitha 4 cmwatercolumn andincubatedatinsitutempera-
tureatdifferent
times
oftheyear.a:Chemical
changesin'theoverlying
waterduring 40days
incubation
in fall 1989.b: timelagafterdepletion
of oxygenbeforeH2Sbecame
detectable
(>1IxM)in theoverlying waterat different
timesof theyear.(TinaSolbek
Schmidt,
unpub-
lisheddata).
Thetransitionfromthewell-oxidized
to thereduced
sediment,
asa resultof eutro-
phication
andhypoxia,hasbeenreproduced experimentally
in belljarson thesea
floor[e.g.,Balzer,1984]or in sediment coresin thelaboratory.Thelattermethod
hasbeenused asanassay forthecapacityofa sediment towithstandoxygen deple-
tionbeforedramaticchanges in chemistry
andnutrientflux [T.S.Schmidt,1990]
(Figure6.9). In late fall, the oxygenwasdepleted after 3-4 days,and Fe2* Was
rapidlyreleased fromthesediment. After9 days,theoxidation capacities
of reac-
tiveMn(IV) andFe(III) wereapparently
exhausted.
In addition,H2Swasreleased
in
smallamounts.
Twoweeksafterthestartof theexperiment,
thefreeFe2*wasgrad-
ually taken up againas it becameboundby sulfidein the sediment.Concurrent
withtherapidconversion of Fe¸OH to Fe2*,phosphatewasno longerboundeffi-
cientlyand was releasedto the anoxicwater.The retentiontime betweentotal
depletionandthe first releaseof H2S,whichis indicativeof the buffercapacityof

the most reactiveMn- and Fe-oxides,was found to vary from 0 to 16 days
throughoutthe yearwith the longestretentiontime in winter and the shortestin
summer,especiallyduringperiodsof hypoxiain situ(cf. Rasmussen andJorgensen
[1992]).
In conclusion, the mineralizationprocesses in coastalsedimentsand the nutrient
fluxesacrossthe sediment-water interfaceare very sensitiveto eutrophicationand
especially to hypoxia.Thesediments functionasan intermediate storagesitefor ni-
trogenandphosphorus. Thesenutrientsarereleased throughoutthe yearbut most-
ly duringthegrowthseason of the phytoplankton.Althoughthe burialefficiencyof
organicmatterincreases with its depositionrate [Henrichsand Reeburgh,1987],
the retentioncapacityof coastalsedimentsfor N and P is limited. An important
question,for which the databaseis still insufficientor partly contradictory,is
whetherthe increased fluxesof N and P mainlyleadto depositionin estuariesand
shelfsediments, or whetherN and P are exportedto and buriedin sediments be-
yondtheshelfarea,andwhetherthe excess N is mostlydenitrified[e.g.,Walshet
al., 1985; Christensenet al., 1987].
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7
CaseStudy- AarhusBay
BoBarkerJorgensen
7.1. Introduction
AarhusBayis a hydrographically opencoastalecosystem situatedat theBalticSea-

Kattegattransition.An intensive
fieldstudyof thebiological,
chemical andphysical
processesin the watercolumnandin the sediments wascarriedout in 1990-1991
with the main goalof understanding the seasonal
elementcyclingand the nutrient
couplingbetweenwater and sediment. Specificquestions
were:
- howmuchof theprimaryproduction sinksoutandis mineralized
in thesediment?
- how doesnutrientreleasefromthesedimentaffectprimaryproduction?
- how do eutrophication andhypoxiaaffectthechemicalenvironment andbiologi-
cal processes
in the sediment?
Theemphasis of thisstudywason directmeasurementsof fluxesandprocess rates.
A singlesamplingstation,"Station6", at 16 m waterdepthin thecentralbaywas
studiedfor 1.5 yearswith participation
fromtheDanishUniversities
of Aarhus,Co-
penhagen andOdense, theCountyof Aarhus,aswellastheHydraulicInstitute,the
WaterQualityInstitute,andtheNationalEnvironmental Research Institute.
Through
thechosen approachof thestudy,a detailed
coherentdatasetwasobtainedforone
location,basedon whichan annualbudgetof themainelement cycles
couldbecal-
culated.The transports
overtheboundaries of theopenbaysystem were,however,
poorlydefinedandthebudget couldtherefore notbefullybalanced.
7.2.AarhusBay
AarhusBaycoversan areaof 320km2 andhasa meanwaterdepthof 15 m. It
deepens
in theeastern
partandconnectsto thesouthern
Kattegat
andtheBeltSea
overshallowsand throughnarrowtroughs(Figure7.1). Geologically,it was
formedduringthe lastglaciaton
by icemarginoscillations
whichleft terminal

Coastaland EstuaxineStudies,Volume52, Pages137-154
Copyright
1996by theAmerican
Geophysical
Union
138 7. CaseStudy- AarhusBay
'. 5 km
I ' ' 0
"K"A'L '
/ ß
EBEL-
TOFT•
" •'-"" VIG
St. 6
• AARH • '
BAY "•-'
I
'X-....•/•'•
..... - .... .=_
k•) "'"'•i
½/ • • r'/
'--7),'-?
Figure7.1. AarhusBayandthe positionof the samplingstation,Station6 (56ø09"10

' N,
!0ø19"20' E).Depthcurves: 10 m, ---- 20 m;waterdepths>20 m areshaded. Inset:
Mapof theBalticSea-NorthSeatransitionshowinglocationof AarhusBay.
moraines anddead-ice formations. On top of quaternary till andglaciafluvial

de-
posits,the sedimentationbasinof AarhusBayis todaygraduallyfillingup at a
meanrateof ca. 2 mm yr-• (Pejrupet al., submitted}.
A determination of the total
thicknessof depositedpostglacial
mudis, however,difficultdueto seismicscatter-
ingbymethane bubbles whicharepresent belowthesulfatezone,from3-4 m sedi-
mentdepth.Thesediment consists
of21% sand,23% siltand56% clayandhasan
organiccontentof 2.1-3.7% org.C [Valeuret al., 1992].
7.3.Hydrographyand Plankton
Duringthefieldstudy, thewatercolumn wasstratified
during70-80% of theyear
withBalticsurfacewaterof 15-25psuoverlyingsalineKattegatwaterof 29-33psu
[SorensenandNielsen,1992](Figure7.2). Duringspringandearlysummer, this
stratification
isfurtherstabilized
bysurfacewaterheating,
andthesalinityandtem-
peraturedifference
between topandbottom mayreach13psuand11øC,respective-
ly.Theexchange of watermasses follows
closely
hydrographic events
in the
Jorõcnscn 139
Depth. m
0
Temperature,
c
18-21
15-18
12-15
9-12
10 6- 9
3-6
0-3
o
Salinity.
psu
> 32
29-32
26 - 29
23-26
lO 20-23
17 - 20
14-17
<11
o
Oxygen.
mg I-•
>12
10-12
8-10
6-8
•o 4- 6
2-4
<2
ol ' I
Fluorescence.
4 •10
•0
1-2
14
J F M A M J J A S O N DIJ1991 F M A M
1990
Fiõurc7.2. Watcœ
columndistribution
of, a) tcmpc[atu[c,
b) salini•',c) o•gcn, andd) in-
duccdfluorescence
du•ingthep•.od, Janua• •99•a) •99•. Data•[omSe[enscn and
ernKattegat,whichtilt the pycnocline

and forcedeepKattegatwater into or out of
thebayaccording to theregionalwindfield.Thecalculated meanresidence timeof
waterin thebayisonly12 daysandthetransportdistance duringonecurrentevent
is usuallyshort,2-5 km, after which the current reverses[Christiansenet al.,
1994].Tidal currentsarelessimportant,asthetidal amplitudeisonly 20-40 cm.
The lowerwatercolumnbecame graduallydepletedin oxygenas stratification be-
camestronger duringspring,dueto thedegradation of planktonanddetritussink-
ing down fromthe euphoticzone(Figure7.2c). The oxygenconcentration at air
saturationof thebottomwatercorresponded to about270 •M in summerand350
•M in winter.Hypoxiastartedin April andMarch,respectively, of thetwo years
studied,shortlyafterthecollapseof a springphytoplankton bloom.More extensive
oxygendepletion, downto <2 mgO•_1-• (i.e.<50 p•MO•_or 15-20% of air satura-
tion), occurredduringlate summerand fall, with lowestoxygenconcentrations
duringperiodswhenthe zooplanktongrazingpressurewas relativelylow and a
largerfractionof thephytoplankton wastherefore degraded at thesedimentsurface
[Sorensen and Nielsen,1992]. Deeperwater from southernKattegatflowedinto
thebayon severaloccasions and,asoxygenwasgraduallydepletedfrom thispartly
isolatedwatermass,resultedin the suddendeathof manydemersalfishand benthic
invertebrates.This strong,intermittenthypoxiais apparentin Figure 7.2, which
showsthe temporalcoincidence of low oxygenand high salinityof the bottom
water. Measurements carried out with a benthic micrbsensor instrument or with a
specialbottomwatersamplerrevealedverticaloxygengradients
alsoin the lowest
few metersor decimeters overthe sedimenton occasionswhen a stablepycnocline
justovertheseabedprevented mixingof the bottomwater[Gundersen et al., 1994;
cf.Jorgensen,1980].On oneoccasion oxygendroppedfrom280 to 65 IzM through
thebottom2 m of water(chapter6, Figure6.6, left). This small-scale
hypoxiawas
lesssignificant
for thegeneraloxygenbalance,but wascriticalto the benthicinver-
tebrates,whichweretherebyexposed to evenloweroxygenlevelsthan indicated at
thedepthresolution of conventionalhydrographicinstruments
(Figure7.2).
The springbloomof diatoms,mostlyThalassiosira spp.,whichovera few weeks
assimilated
thenutrientsaccumulated duringwinter,occurredin the periodof late
Februaryto early April. As is also the casein the Kattegat [Richardsonand
Christoffersen,
1991], the springbloomconstitutedonly a small fractionof the
annualproduction,14% in 1990, but with highphotosynthesis rates,up to 180
mmolC m-2 d-• (= 2.2 g C m-z d-i), overa shortperiod(Kruse,submitted)Figure
7.3). The diatomssankout of the water columnwithin a few daysafter the nutri-
ent depletion,and apparentlyintactdiatomcellswith a highchlorophyllcontent
and a C :N ratioof 6-7, similarto the Redfieldratio for livingplankton,appeared
as a flocculent,orangedetritusfilm on the sediment.As is typical of manyeu-
trophiccoastalsystems [Billenet al., 1991], silicawas depletedbeforenitrogen
andphosphorus andthe phytoplankton community changed to flagellated
forms,
which were mainly P-limitedduring springand N-limited later in the summer
[S•rensen andNielsen,1992].The algaewerestronglygrazedduringsummer and
detritussettledasfecalpellets.A bloomof dinoflagellates, Ceratiumspp.,devel-
opedin thefall justbelowthepycnocline
(Figure7.2d},wherethe algae
Jorgensen 141
175
'150
12.5
100
ryproducfion
•
?5
150
50
B.
125
25 100 •
0 A.
SO ca.,
25
0
ß
C-0
J•n Apr Jut 0of Jo,
n Apr
Figure7.3. Biological
activityin the watercolumnduring1990-1991calculated
persquare
meter,basedon measurementsin incubatedwatersamplesfromten depths.Primaryproduc-
tion wasmeasuredby the •4CABM-method.Planktonrespirationwas measured from the
decreasein oxygenoverseveralhoursin watersamplesincubatedin gas-tightplasticbags.
Bacterial
production
wasmeasured
by the 14C-thymidine
incorporation
method.Data from
B. Kruse(submitted).
nutrientscontinuouslyreleasedfrom the sediment.Suchpycnoclinebloomsalso

developin the Kattegatoutsidethe bay [Nielsenet al., 1990; Bj•rnsenet al.,
1993].Thelarge,spinyCeratium
cellsweren6t extensively
grazed
andreached
the bottom as whole cells.
Respiration in thewatercolumnmostlyfollowedvariations in theseasonal plank-

tonproductivity, thoughoftenwith a timelag (Figure7.3). A comparison between
photosynthesis and total respirationshowswhichfractionof the phytoplankton
production wasmineralized throughthegrazingfoodchainandmicrobialloop,and
how muchsettledout of the water column.During the whole year, 68% of the
fixedcarbonwasrespiredin the water,and32% maythushavereached thesedi-
ment,withtherelativelyhighestcontributions comingfromtherapidlysettlingdia-
tomandCeratiumblooms. Thispercentage of sedimentationandbenthicreminerali-
zationfallsin the centralrangeof valuespublished for shallowcoastalecosystems
[e.g.,$uess,1980;Nixon, 1981]. The bacterialproduction reflectedthe respiration
through theyearwithsmallmaximafollowingblooms of phytoplankton. Assuming
that the bacteriaallocatehalf the assimilated organiccarbonto the measured cell
growthand usehalf for respiration, the total carbonflow throughthe microbial
loopwouldbe48% of themeasured primaryproduction(B. Kruse,in
]•2 7. CaseStudy- AarhusBay
7.4.Sedimentation
and Resuspension
Verticalsediment
fluxesweremeasured
by biweeklyharvesting
of sedimenttraps
permanently situatedat ninedepthsin the watercolumn[Valeuret al., 1995]
(Pejrupet al.,submitted).Dueto thepresenceof a pycnocline,
whichpreventedver-
ticalmixingduring70-80% of theyear,it waspossible to distinguish
betweenthe
netfluxof primarysediment fromabovethepycnocline andthemuchlargerfluxof
resuspended materialfrombelow(cf.chapter6, Figure6.2).Onlythesettling
of the
Ceratiumbloom,whichdeveloped
just belowthe pycnocline,
couldnot be distin-
guishedby thisapproach.
Currentsandwavescaused resuspension of sediment in the relativelyshallowAar-
husBay,but theerodibilityvariedstronglythroughout the year[Lund-Hansen et
al., 1993;Valeuret al., 1995]. A fine detrituslayer,deposited by the springbloom
waseasilybroughtinto suspension. Duringfall and winter,repeatedresuspension
events removed the flocculent material and left a more consolidated sediment sur-
facewhichlargelyresisted resuspension,
evenat measured currentvelocities
of up
to 28 cm s-•. Therewasa positivecorrelationbetweenbottomshearstress,i.e. cur-
rentvelocity,andresuspension measured at a 1-daytime resolution(Floderusand
Lund-Hansen, submitted).Theresuspensionwas,however,apparentlyalsoaffected
bywavepumping whichmaycausea swellingandloosening, "liquefaction",
of the
surfacesedimentand bringit into suspension; cf. Maa and Metha [1987]. During
the strongest storms,the amountof materialin suspension >0.5 m abovethe bot-
tom corresponded to a meansedimentlayerof 2. mm cyclingin the water at one
time.The depthof erosionis,however,likelyto bevariable,dependent on sediment
topography etc.,andmaylocallybemuchdeeperthana fewmm.
Thesephenomena weredemonstrated by an extremeresuspension eventshownin
Figure7.4. Brackish Balticwaterinitiallyoverlayedthe seafloor, but afterstorms
on December26 and27, salinebottomwater fromthe Kattegatflowedinto Aarhus
Bay.Due to the closebottomcontactof thisheavywater, sedimentmaterialwas
entrained, andit thuscarrieda highersuspension load(ca.10 mgd.wt. 1-1)thandid
the brackishwater(1-2 mg l-l). This is alsoseenfrom the higherturbidity(Figure
7.4). Sedimentation ratesmeasured at dailyintervals! m abovethe bottomshowed
resuspension peakswhich did not coincidewith maximumcurrentvelocitiesbut
ratherwith maximumwaveheightsand orbitalvelocitiesof the bottom water (al-
thoughthehighest orbitalvelocityreached on26 December (6 cms-•) wasonlyone
third of the highestcurrentvelocity).On that occasion,the sedimenttrap at 1.5 m
abovethe bottomcollected500 g m-2 of sediment materialwithin 24 h (Floderus
and Lund-Hansen, submitted).Only five timesduringthe yearwere orbital veloci-
tiesof >5 cms-• reached, withthemaximumbeing12 cms-• [Floderus, 1993].
The cycleof resuspension-resedimentationis importantfor the couplingof process-
es at the sediment-water interface.High respirationrates,rapid oxygenationof
sedimentiron sulfides,rapid releaseof nutrients,etc. may occurduringa storm
suchas that illustratedin Figure7.4. However,field samplingand flux
Jorgensen 143
35
3
3O
%o
25
2O
2O
cms-1 Current I
15
-I velocity
500
/•00 Wcwe Orbifcz[ _1

cms
,.,:,]oo heighf• vetocity

• 200
100
0 ' " i' ' ! i ! 0

22. 24.. 26. 21t. 30. 1. 3. 5.
Dec. Jon.
Figure7.4. Physicalmechanismscausingresuspension duringa windy periodin winter

1990-1991.Upperframes:salinity,turbidity,andcurrentvelocityat 0.5 m abovethe bot-
tom.Bottomframe:waveheightsand inducedorbitalvelocitiesoverthe bottomcomputed
fromlocalwind data. The velocityof the oscillatingwater movement,ratherthanthe total
currentvelocity,correlatedcloselyto the total sedimentflux (netdeposition
plusresuspen-
sion)perdaymeasured at 1 m abovebottom(shownashorizontallines).Thehighest value,
measured on December 26-27, corresponded to'500 g d.wtperm2.Data fromValeuret al.
[1992] and Floderusand Lund-Hansen(submitted).
mentsaredifficult(andthereforenot available)for suchoccasions, whichtherefore

causes
an underestimationof certainfluxes.It wascalculated
that a sediment
particle
wastypicallyresuspended at least60 timesto >1 rnabovebottombeforeit wastrap-
pedbelowthe2.5-cmdeepsediment layerof highestmixingrate(Pejrupetal., sub-
mitted).Themeansettling velocityof resuspended particles
was0.5-2 rnh4 during
theyear.Consequently, theresuspended materialhada shortresidence timein the
water,andthe resuspension followedchanges in currentandwaveenergywithin
hours.As a result,the lateraltransportdistance of sedimentmaterialduringeach
resuspensioneventwasonlya smallfractionof thetypicalwatertransport distance
of 2-5 km [Christiansen et al., 1994].Furthermore, themeasured resuspension
144 7. CaseStudy-Aarhus
Bay
creasedexponentially with heightabovethesediment, andoverthe yearthemateri-

al trappedat 4 m abovebottomwaslessthan10% of thattrapped0.5 rn above(cf.
chapter6; Figure6.2). The closebalancebetweenthe net depositionand the accu-
mulation of sedimentsuggested that most of the primary sedimentremained
trappedwithinthesedimentation basinof AarhusBay.Thus,the total net deposi-
tionmeasured by thesediment trapmethodwas990 g d.wt. m-2 yr-•, whilethenet
accumulation of sedimentcalculatedfrom2•øpbprofileswas890 g d.wt. m-2yr-•.
7.5.SedimentOxygenUptake
The aerobicmineralization of organicmaterialin the sedimentwas measuredboth
in thefieldandin laboratory-incubated coresasthe total andthe diffusiveuptakeof
oxygen(Figure7.5}.Seasonal in situdataon diffusiveoxygenuptake,obtainedbya
benthicmicroelectrode instrument,"Profilur" [Gundersenand Jorgensen,1990],
showedhowuptakeratesdepended on a combination of freshdetritusinflux andof
the oxygenconcentration in the overlyingwater (Gundersen et al., in prep.).Over
the year, oxygenconsumption showedonly little dependence on the temperature
whichvariedbetween0 and 17øC.A springpeakin oxygenuptakewasfollowedby
a periodof lowerrespiration rateduringsummerwhile oxygenin the bottomwater
waslow. An intermittent inflowof moreoxicwateriri lateSeptember immediately
enhanced theoxygenuptake,whichindicatedthatthemicrobialrespiration waslim-
itedby oxygenavailabilityduringsummer.Lowerratespersisted throughoutwinter
1990-1991 untila phytoplankton bloomsedimented the nextspring.The thickness
of the oxic zone,which varied betweena minimum of 0.6 mm in summerand a
maximumof 4 mm in winter,alsocloselyreflectedthe combinedeffectof oxygen
concentration
in thewaterandthepotentialsedimentOz consumptionrate.
The total oxygenuptakemeasured in incubatedcoreswas only 20% higherthan
the calculatedone-dimensional diffusiveuptake.This apparentlyindicatingthat
biopumping, current-induced advectiveflow or surfacetopographyplayedlittle
role [Gundersenet al., 1994]. The coreincubation,however,underestimates the ef-
fectof largeinfauna,whichis not well represented or is lessactivein the cores.
Concurrent studies on the sea floor with a microsensor and a flux chamber instru-
mentshowedthat the total oxygenuptakeunderthe leastdisturbedin situcondi-
tionswas60-70% higherthanthediffusiveuptake.
The coreincubation alsodoesnot includetheeffectof resuspension of the surface
layerwhichoccurs frequently
in situ(seechapter6). Experimental resuspension in
the laboratoryof sedimentfromjust belowthe oxygenzoneshowedan extremely
highinitialoxygenconsumption rate, ca. 100-foldhigherthan the specificrates
measured in situ [Hansenet al., 1994]. Especially the rapid oxidationof pyrite,
FeS2,andotherreducedironmineralswasimportantfor theenhanced oxygencon-
sumption, therateof whichdecreased two ordersof magnitude withina fewhours.
By combining theseexperimental resultswith field data on actualresuspension
events,thepotentialoxygendepletionin the lowermetersof the water columndur-
ingresuspension couldbecalculated. Theresults indicated thattheinitial,rapid
Jorgensen 145
400 ,,
300
2OO
ce •/•
lOO
]o
• lO
3o
Specific
02 upfc•ke
•, 2o
• lO
1 d
o. L
-1
[E -2
-3
-4
02:Sedimenf
-.5'
Jani I iAprI I ijujlI Iocfl
I •Jen I Apr
, •
Figure7.5. Oxygendistribution andconsumption ratesduring1990-1991.a) 02 concentra-
tionsin surfacewater and 10 cm over the bottom.a) DiffusiveO2 uptakeratesof the sedi-
mentcalculated from the in situ02 gradientin the diffusiveboundarylayermultipliedwith
thediffusioncoefficientof 02 at the prevailingtemperature andsalinity.c) Meanvolume-
specific
02 consumptionratescalculated
fromthediffusive02 uptakeof thesediment
divid-
edbythedepthof theoxiczone.d) Isopleths
of O2distribution
in thesediment;
numberson
curves
indicate02 concentrations
in •M. DatafromGundersen
et al. [1994].
fectwassmall,only about3% of the oxygenpoolat air saturationin a 1 m water

columnwould be consumed within an hour by resuspensionof the top 5 mm of
sediment.
Localeffects
onoxygenat thesediment-water
interface
may,however,
be
moresignificant,
andtheresuspensionconverts
ironandmanganeseminerals
to an
oxidized state which is more reactive to
Bay
7.6. Anaerobic Mineralization
Belowthe oxic zone,mostoxidationof organicmatter was due to sulfatereduc-

tion.Sulfatebecame depleted at 2.5 m depth,belowwhichmethaneaccumulated
andformedgasbubbles belowca. 3.5 m. The rateof sulfatereductionlargelyfol-
lowedtheseasonal temperature variation,andthezoneof maximumreduction rate
movedupwardduringsummer, from5-6 cmto 2-3 cm,asthesediment became
morereducedand sulfidic[Thamdrupet al., 1994; Figure7.6]. A distinctzoneof
highsulfatereduction ratewithinthetop 5 mmsuddenly appearedwith a delayof
a few weeksafterprecipitation of the springdiatombloom(datanot shown).In
someyears,thiszonewasvisiblefor several weeksasa thin,blacksurfacebandof
iron sulfideoverlyingthe brownishoxidizedsedimentzonewhich, duringearly
spring,extended to severalcmdepth[Moeslund et al., 1994].The microbialdegra-
dationof the freshlysettledphytodetrituswasthussointensivethat an anoxic,sul-
fidicmicrozone developed on top of the sediment. Deeperin the sediment,sulfate
reduction proceeded at rapidlydecreasing rates,downto thedepthof complete sul-
fatedepletionat 2.5 m.
Mass balancecalculationsshowedthat 85 % of the H2S formed from sulfatereduc-
tion was againreoxidizedthroughthe redoxcascade of oxidizediron and man-
ganese, nitrateandoxygen(chapter6). Especially the top few cm of sediment were
richin reactiveironand manganese oxides,with ca. 10-foldmoreiron thanman-
ganese [Thamdrup et al., 1994;Figure7.7). Below2-3 cmdepth,theconcentration
of extractedoxidizediron droppedto a background levelof non-reactive Fe(III) of
ca. 20 Ixmolcm-3. The calculatedturnovertime of the total manganese poolwas
1-3 weeksandof the reactiveiron pool2-6 months.The mainzonesof metalre-
ductionwere evidentfrom maximaof dissolvedFe2* and Mn 2', which occurredat
2-3 cmandat I cmdepth,respectively. A highMn2' peakwasobserved in Aprilas
the resultof intensivemanganese reductionjust belowthe freshlysettledphyto-
planktondetritus.Recyclingof thereducedmetalstookplacethroughupwarddif-
fusionalongsteepsurface gradientsandsubsequent oxidationwith oxygen.
FreeH2Swasdetected
onlybelowthezoneof reactive
iron (Figure7.7). With a cal-
culated
turnover
tit:he
of <10min,thelargeamounts
of H2Sformedin themainsul-
fatereductionzonemustthushavebeenrapidlyreoxidizedor precipitated by the
metaloxides,whichweretransported downwardinto the sediment by bioturba-
tion.Quantitative
evidencefor anaerobicsulfidereoxidation
throughdown-mixing
of metaloxideshasbeenlacking,but in the AarhusBaysediment thismechanism
wasindeedconfirmed by calculations
of massbalanceandtransportcoefficients.
Themaintenance of a zoneof oxidized metalsthroughcontinuous Mn2' andFe2'
oxidationby 02 is importantto preventthe emissionof H2Sinto the overlying
water.Laboratoryexperimentsshowed thatthetotalMnO2poolcouldbedepleted
withinonemonthin the absence of oxygen.Accordingly, the extensivehypoxia
duringsummer 1990created totalMnO2depletion andlow ironoxidelevelsfor
3-4 weeksin October (Figure
7.7).A largeMn2' poolwasreleased to the
Jorgensen 147
Su[fc•fe reducfion
'= 10
• 5
, I , I I ! ' ! i , , I I I ! I
6 50
]0
Jcm Apr Jul 0of Jcm Apr
Figure7.6. Sulfatereductionin thetop 0-10 cm of sedimentduring1990-1991. Top: Inte-
gratedratesperm2 of sediment. Bottom:Isopleths
of reductionrates(nmol$042-cm-3 d-I).
Data from Thamdrupet al. [1994]. Reprintedwith permissionfrom ElsevierScienceLtd.
Hn
• ,F•..............
0
,
cm H2S2 ••
5
1
•5 ••50 0
I i I I I J i , , i J • i
10
JQn Apr •u[ •cf J•n Apr
Figure7.7. Isopleths
of total,solid-phase
manganese
andironin thesedimentandof HIS in
theporewaterduring1990-1991.Concentrations oncurvesarein •mol cm-3[orthemetals
andin •M for H2S.Data [rom Fossing
et al.
water,butsoonreturnedastheMn•-+wasoxidizedto MnO,_higherup in thewater

columnand settledagain, trappedtogetherwith other sedimenting particles
[Thamdrupet al., 1994].
7.7.Nutrient Cycling
Theexchangeable phosphatein thesediment occurred mostlyadsorbed to ironhy-
droxidesandwaspartlyreleased duringlatesummerasthe irongraduallybecame
reducedandreactedwith sulfide[Jensen andThamdrup,1993;Jensenet al., 1995].
Duringthe initialdegradationof the springplanktonbloomon the sedimentsur-
face,a shortpulseof dissolved phosphorus releasefrom the organicallybound
phosphatealsooccurred(Figure7.8). As the manganese and iron oxidepoolsbe-
camedepletedin fall 1990, a muchlargerpulseof phosphorus was emittedfrom
thesedimentbecause the FeOOH-adsorbed phosphate couldno longerbe retained.
Thiscauseda transientaccumulationof phosphatein the bottomwaterof up to 2.0
and3.4 izM HPO42- in 1990 and 1991, respectively
[S•rensenand Nielsen,1992].
Someof the phosphate wastrappedagainby adsorptionto the metaloxidesin the
watercolumnandsubsequently sedimented.The shortperiodof this open "iron-
manganese window"was thusimportantfor the nutrientcyclingin the sediment,
Ammonia 2
1
Ni,ro,e
Phospho,e
0.5
Urec• 0.•
0.3
0.2
0.•
0.0
i i t ! I i ! I i i I , ! i I
Apr Jul Oct ion Apr Jori Apr Jut 0•, Jon Apr
Figure7.8. Nutrientfluxesacross
thesediment-waterinterface
measured in laboratoryincu-
batedcoresduring1990-1991.Coreswerekeptat in situtemperature underin situwater
untilincubationon thedayof sampling. The P-fluxincludes
the total dissolvedP. Positive
valuesindicate
fluxfromsediment to water.DatafromLomstein andBlackburn [1992]and
Jensen
et al. [
Jorgensen 149
but rapidrecyclingvia the watercolumnlargelyretainedthe elements withinthe

bay.The largephosphorus pulseoccurred in thefall whenlow nitrogenavailability
andfadingdaylightlimitedtheprimaryproduction.Accordingly, it hadno immedi-
ateeffecton the planktonproductivity.Experimental studiesshowedthat addition-
al releaseof phosphatemayhavetakenplaceduringresuspension eventsandmay
thus accountfor a discrepancybetweenmeasuredand calculatedrelease(H.S.
Jensen,pers.comm.).
Therewas a preferentiallossof phosphatefrom the freshplanktondetritusas it
settledout of the water column, and the C:P ratio increasedfrom a Redfieldratio
of 106 in thealgaeto 155 in thosesediment trapswith theleastresuspendedmaterial.
Phosphate, however,became trappedin thesedimentandburiedmoreefficiently than
organiccarbon.Belowthe mixingzonein thesediment the C:P ratiowasca. 133.
An oppositetrendwas foundfor organicnitrogen,whichwasdepletedin thesedi-
mentrelativelyfasterthan organiccarbon.Althoughthe nitrogenwasalsoprefer-
entiallylost from the sedimenting detritus,wherebythe C:N ratio increasedfrom
theRedfieldratio of 6.5 up to 8.1 in the sedimenttraps,the C:N ratio belowthe
mixingzoneof the sediment wasca. 11 '(LomsteinandBlackburn,submitted; chap-
ter6, Figure6.7). The nitrogenwas mainly buriedasorganicN and only 5% asad-
sorbedor freeNH4+. Comparedto the 21% of the deposited organiccarbon,which
wasburiedinto deepersedimentlayers,the burialof deposited nitrogenwasonly
15%, whereasof phosphorus it was 32% (Figure7.9). Nitrogenis thuspreferen-
tially releasedduringmineralization,while the sedimenttendsto trap phosphate.
Furthermore,a reactivepool of phosphateis accumulatedin the oxidizedsurface
sediment, boundto reactiveFe(III) minerals,and may sendpulsesof phosphate up
intothe water columnduringhypoxia.This phosphatepoolremainsat the surface
andis not buriedbecausethe phosphate-binding Fe(III) mineralsbecomereduced
deeperin the sedimentand thusreleasethe phosphate againto diffuseupward.
While 15% of the depositedparticulateorganicnitrogenwas buriedin the sedi-
ment,the restwasdegradedand convertedinto dissolvedorganicnitrogen(DON),
urea,and inorganicnitrogen[Lomsteinand Blackburn,1992]. Radiotracerstudies
of •4C-ureaturnovershowedits major importanceasa productin organicdegrada-
tion and as an intermediate in the formation of NH4+; cf. Lund and Blackburn
[!989]. Nitrogenwasthusreleasedfrom the sedimentto the waterat relativelycon-
stantrates,mostlyin the form of ureaand NH4+ (Figure7.8). The formerdominated
in the springwhenthe sedimentwas ratheroxidizedand the ureaconcentration in
theoverlyingwater was low. During periodsof oxygendepletionin late summer,
theureawasfurtherdegradedin the sedimentto NH4+,whichwasthenrele. ased.
Theseasonal variationof nitrateflux from the sedimentis regulatedby severalfac-
torsincludingnitrification,denitrification,nitrate concentrationin the overlying
water,andtemperature
[e.g.,Kempetal., 1990].Nitrification
waslowdurin]g
win-
ter and in periodswhenthe oxiczonewasthin, < 1 mm, i.e. after sedimentation
of
thespringphytoplankton bloomandduringsummer[Jensen et al., 1990].Themean
diffusiontime througha 1 mm deepO_,zoneis onlyca. 10 min, and sucha thin
oxiczonecombinedwith the shortretentiontime may hinderthe efficient
150 '• CaseStudy- -Xarhus
Bay
um uptakeb,, the mtrif.•ingbacteria.The nitrificationof an estimated

40% of the
NH4' consumed 0.5 mol O2 sr-t or 5-8% of theannualsediment ox.•genuptake.
During winter, the nitrate concentranonof the bottom hater increasedto near 20
•N! and, in periods,the sedimentbas taking up rotrate{Figure7.81.Oser a whole
.,,ear,the total budgetof depositedparticulateorganicnitrogentPON} bas: 15øo
buried as PON, 12øo released as DON, •0øo released as urea, 26ø0 releasedas
'•H4', and 18øonitrifledto NOc of bhich half {9ø0}bas releasedas NO•- and the
other9ø0demtrihedto N: [Valeuret al., 1992;Lomstein
andBlackburn,
1992].
'.8. Budgetand Conclusions

In thecalculanon of an annualbudgetfor pro•esstsof the mainelementc}cles,as
,sdonein the tollobing{Figure7.9), muchimportantinformationis loston thedy-
namicsand regulanonot the proctsses bhich can be readonl.,,out of the seasonal
data.The annualbalanceis, hobever,usefulm the understanding ot thecoupling
ot processes
in the hater column and sedimentand to checkthe internalconsisten-
cs of the seasonal
data.A stmphhed schemeis presentedhere,in bhichdatabase
beencalculated for a l-m: areaot theseafloorosera .•ear.Theproductionor con-
sumpt{on of oxsgenand otheroxidantsis gisenin molarunitsto facilitatecom-
Annualbudgel(toolrn-2 yr •)
DIN DON
o 34 1o •8)
98
12
H•O 0 15 Felll.
(? 71 B SO•a•
Na
N: 0 18
PO0•O
MINERALIZATION
FeI•
or9, C FeSt
Figure7.q. •ummar•of fluxesandproces• ratesmeasured

duringthefieldstud•m Aarhus
Ba•, Nla• 19t}0-Nla• Iqt}l. Numbersm parentheses
x•eredemedb• aliiterence
•hile the
reslare basedon independent
rate mea•uremcnt•
and calculationsLlnitsare givenin tool
m: • r i lot each ricHlent.
Jorgensen 151
parisonto thecarbontransformations andelement cycling

by takingthereaction
stoichiometryof theelements,
C, O, N, Mn, Fe,andS intoaccount(cf.chapter
6,
Table6.1).It shouldbenotedthatalmostall dataarebasedondirectprocess
mea-
surementsandthata balanced budgetis,therefore,
notto beexpected,mainlybe-
causethe systemis openandwith a poorlydefinedlateralexchange,
but alsobe-
causeof possibleinaccuracies
in the measuredrates.
Theannualnetphotosynthesis of phytoplankton
was21.8molC m-2 yr-• (260g C
m-2yr-•),whichplacesAarhusBayin theuppermesotrophicrangeof coastaleco-
systems.Givena Redfieldratioof elemental
composition,
theconcurrent assimila-
tionof nitrogenand phosphorus nutrientswas 3.35 mol N and 0.21 mol P. The
measured planktonicoxygenrespirationwasequivalentto 14.8 mol C or 68% of
theprimaryproduction, andtheremaining7.0 mol C or 32% maythushavebeen
deposited on the seafloor (B. Kruse,submitted). Sediment
trap studiesconcluded
that a somewhatlargeramountof detritus,9.9 mol C equivalentto 45%, had
settledfrom the photiczone[Valeuret al., 1992].
Dueto frequentresuspensionof thesurfacesediment,combined withefficient
mixing
oftheupper2-3 cmasshownby2•øpbdata[Valeuret al., 1992],deposited detritus
wasrecycled throughthelowerwatercolumnmanytimesbeforeburialintodeeper
layers.The measuredgrossverticalflux of organiccarbonat 1.5 rn abovethe sea
floorwas600 mol C, i.e. 60-foldhigherthanthe netdeposition.The resuspension
cycle
wasevenmoreintensive closerto thesediment
surface(cf.chapter6, Figure6.2).
Of the deposited organiccarbon,2.1 mol wasburiedbelowthe bioturbated layer
whilethe remaining7.8 mol was mineralizedto CO2. Another1.2 mol CO2 was
formedby dissolutionof 93% of depositedcarbonateshells[Valeuret al., 1992].
Themeasured CO2releasewas9.8 mol, corresponding wellto thenetcarbondepo-
sition.The total oxygenuptakemeasuredin sedimentcores,6.5 mol 02, was too
lowto accountfor the oxidizedorganiccarbon,but it is alsolikelyto be an under-
estimate,as discussedabove.The calculatedtotal uptakebasedon a comparison
within situflux chambermeasurements was 9.2 mol 02 [Gundersen et al., 1994].
Of the oxidantsin the suboxiczone (cf. chapter6), NO3- couldaccountfor only
0.15x 5/4 =0.18 mol C oxidized,and denitrificationwasthusinsignificant for the
carbonoxidationin thesediment(LomsteinandBlackburn,submitted}. Manganese
andiron reductions wereapparentlyinvolvedin the oxidationandprecipitation of
sulfideratherthan directlyin the oxidationof organiccarbon.With a redoxstoi-
chiometryof 2 mol Mn(IV) or 4 mol Fe(III) to oxidize1 mol org. C, theywerealso
of minorsignificance as indirectcarbonoxidants,eachequivalentto ca. 0.4 mol
org.C [Thamdrupet al., 1994].
$ulfatereductionwas 1.72 molandcouldaccountfor 3.4 mol org.C or 44% of the
organiccarbonoxidizedin the sediment[Fossinget al., 1992]. Of the H2Sformed,
0.25 mol or 15% was buriedmostlyas pyrite,while the restwas reoxidizedand
couldpotentiallyconsume3.0 mol 02, i.e. onethird of the calculated02 uptake.
Theseredoxbalances are in generalaccordance
with earlierresultsfromDanish
coastalsedimentswhich, however,were basedon oxygenuptakemeasurements in
cores[J•rgensen,
Bay
The measuredannualreleaseof urea pluscombinedinorganicnitrogenfrom the

sedimentwas0.96 tool N, whichcouldcover29% of the nitrogenrequiredfor the
measured primaryproduction[Lomsteinand Blackburn,1992]. Sources from the
landimmediately surroundingAarhusBayandfromtheatmosphere contributedan
additional0.55-0.70 mol or 16-21%, the atmosphericsourcebeingone third of
theterrestrial
source[SorensenandNielsen,1992].The nitratepoolaccumulating
in the watercolumnduringwinterand usedby the springphytoplanktonbloom
corresponded to 12-15% of theannualconsumption. Overthe year,an estimated
68% of the nitrogenassimilatedby the phytoplankton
wasrecycledin the water
column.The total nitrogeninputfrom sediments,land and atmosphere, ca. 1.75
tool, exceededthe lossthroughsedimentation,1.06 mol, the excesspresumably
beingexported.Dissolved organicnitrogencompounds-otherthan urea- were
also released from the sediment at an annual rate of 0.18 mol N. The role of this
DON as an N sourcefor phytoplanktonis poorlyunderstood. The total nitrogen
fluxfromthesedimentappearsto exceedthedepositionminusburialrateby25%,
whichmayreflectaccumulatedinaccuracies
in the manydirectlymeasuredrates.
Phosphate released
fromthesediment wasequivalent to only16-19% of theannu-
al planktonuptake.Landsources correspondedto only4-9%, after a 70-80% re-
ductionin recentyears,especially due to a 90% reductionsince1990 from the
largestsinglesource,the city of Aarhus,througha new sewagetreatmentplant
[SorensenandNielsen,1992].Therehas,consequently, beena notablereductionin
the phosphate concentration of the water columnin AarhusBay over the last
decade,and the systemnow appearsto be moredependent on phosphate inflow
fromthe BalticSeaandKattegat.In spiteof the strongreductionof the terrestrial
phosphate source,
phytoplankton growthstillbecame nitrogen-limited
in latesum-
mer, althoughthe periodswith potentialnutrient limitation were alltogether
longer.Primaryproductionin 1990-1991 was ca. 20% lower than in 1987-89,
and this decreasecontinuedin 1992-1993. A longer time seriesis, however,re-
quiredto discriminate thistrendstatistically
frominterannual fluctuationsdueto,
e.g.variationsin precipitation
causingvariations in thewashoutof agriculturalni-
trogenfertilizer.Furthermore,the problemof oxygendepletionis alsocoupled to
conditionsoutsidethe bay, as hypoxiamay originatein the heavybottomwater
fromKattegat.The bottomwaterthenbecomes furtheroxygendepletedin thebay
dueto the highbenthicrespiration.Occasionally, e.g. in September1990, heavy
watermasses fromKattegatpressed thebottomwaterdeepintothe bayandagainst
thecoastwith theconsequence that demersalfishwerefoundsuffocating alongthe
shore.A bottomhypoxiacan,however,alsobeexportedfromthebaywhenlighter
Balticwaterflowsin and expelsthe bottomwaterto leavea uniformlyoxicwater
column [Nielsenet al., 1993].
In conclusion,the centralAarhusBay showeda nearlybalancedcarboncyclein
whichmorethanonethirdof the mineralization of the primaryproduction
took
placein the sediment.Nutrientregeneration
andreleasefromthe sediment
wasa
moreimportant source
for phytoplankton
growththanthecontributions fromthe
atmosphere
andthesurrounding land.The baysystemis, however,opento water
andnutrientexchange
withthesouthernKattegat,
andtherehasconsequently
Jorgensen 153
onlylittleeffecton primaryproductivity of the recentreductionsin nutrientdis-

charge intothe bay.Especially the phosphate discharge hasbeenstrongly reduced,
whereasthe agriculturalcontributionof nitrogenhas not been significantly
changed. Althoughphosphate appeared to be thelimitingnutrientfor thebuildup
ofphytoplankton biomass in latespring,inorganic nitrogenwasdepleted in theeu-
photiczoneduringmostof thegrowthseason.
Thenitrogenand phosphorus nutrientsshowedimportantdifferences in the mech-
anisms of releasefrom the sediment,especiallyin theirseasonality
andresponse to
hypoxia. Nitrogendidnotaccumulate in thesurface sediment butwasgradually re-
leasedthroughoutthe year, mostlyas NH4+ and urea.Phosphateaccumulated in
thetop 2-3 cm of surfacesediment,boundto oxidizediron minerals,andwasre-
leasedin pulseswhenhypoxiaor a settlingphytoplankton bloomcauseda partial
iron reductionin this sedimentlayer. It is notable, that in contrastto the open
exchange of nutrientswith the surrounding waters,sedimentparticlesare largely
retainedwithin the system,andthroughrecyclingbetweensedimentandwaterthey
arealsoimportantin regulatingthe nutrientbalancewithinthe bay.
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Phosphorus cycling
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Jensen,
M. H., E. Lornstein,
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BenthicNH4+ and NO3- flux followingsedi-
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effecton the benthiccommunity,Oikos, 34, 68-76, 1980.
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Kemp,W. M., P. $ampou,J. Caffrey,M. Mayer,K. Henriksen,andW. R. Boynton,Ammo-
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Danish),Havforskning fra Miljostyrelsen,16, 74 pp., DanishEnvironmentalProtection
Agency,Copenhagen, 1992•
Lornstein,B. Aa., and T. H. Blackburn,Seasonalvariationin sedimentcarboncyclingin
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a •4C-ureashorttermincubation. J. Microbiol.Meth., 9, 297-308, 1989.
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H. P. Hansen,andC. Simonsen, Dynamicsandcomplexityin
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New York, 1981.
Pejrup,M., J. Valeur,and A. Jensen,Vertical sedimentfluxesin the AarhusBay, Denmark,
measuredby useof sedimenttraps,Cont. ShelfRes.,submitted.
Rasmussen, H., and B. B.J•rgensen,Microelectrode studiesof seasonaloxygenuptakein a
coastalsediment: role of moleculardiffusion,Mar. Ecol. ?rog.Ser.,81,289-303, 1992.
Richardson,K, and A. Christoffersen, Seasonaldistributionand productionof phytoplank-
ton in the southernKattegat.Mar. Ecol. Prog.Ser., 78, 217-227, 1991.
Sorensen, H. M., and K. Nielsen,AarhusBugt 1990-1991: Hydrography,Nutrientsand
Plankton(in Danish),67 pp., Countyof Aarhus,Envir. Dept, 1992.
Suess,E., Particulateorganiccarbonflux in the oceans:Surfaceproductivityand oxygenuti-
lization, Nature, 288, 260-263, 1980.
Thamdrup,B., H. Fossing,and B. B. J•rgensen,Manganese,iron, and sulfur cyclingin a
coastalmarinesediment(AarhusBay, Denmark), Geochim.Cosmochim.Acta 58, 5115-
5129, 1994.
Valeur,J. R., A. Jensen,and M. Pejrup,Turbidity,particlefluxesand mineralisation
of C
and N in a shallowcoastalarea,Austr.J. Mar. Freshw.Res.,46, 1995.
Valeur,J. R., M. Pejrup,andA. Jensen,
Particulatenutrientfluxesin VejleFjordandAarhus
Bay(in Danish),Havforskningfra Miljostyrelsen,14, 127 pp., DanishEnvironmentalPro-
tectionAgency,Copenhagen,
8
Benthic Macrofauna and Demersal Fish
LarsHagerman,Alf B.Josefson
andJ•rgenN. Jensen
Introduction
Eutrophication stronglyaffectsthebenthicecosystem, becauseof increased primary

production of planktonicmicroalgae or of benthicmicro-andmacrophytes, which
areto a largeextentdegradedin the sediment.Sincemanyof the macrobenthic or-
ganisms havelife spansof severalyears,eutrophication effectswill last,andsome-
timesbe integrated,overlongertimeperiods.The natureof the effectsdepends on
severalfactorssuchasthe amountand qualityof sedimenting organicmaterial,the
degreeof oxygendepletionin the bottomwater,and the differentialresponse by
thebenthicpopulations to thesefactors.The effectsmaybeevidentat verydifferent
levels,rangingfrom the physiologyof individualsto the ecologyof the entireben-
thicecosystem. Effectsof a progressing degreeof eutrophication followa sequence,
startingwith enhancedgrowth of the individuals,followedby growthin popula-
tion sizewith associated changesin species composition,then followedby physio-
logicaland behavioraleffects,and possiblywith massmortalitydueto anoxiaas
the ultimatestage[Gray 1992]. In this chapterwe summarizesomerecentphysio-
logicaland ecologicalstudieson the effectsof eutrophication on benthicmacro-
fauna(invertebrates > 1 ram}and demersalfish,with examples takenprimarilyfrom
Scandinavian waters.The subjectstreatedare: eutrophication effectson demersal
fishpopulations, effectsof increased food levelson macrobenthos, and effectsof
hypoxiaon macrobenthos, in particularthe Norway lobster.The rationalefor
treatingthe Norway lobsterin more detailis, that this economically important
species hasplayedan importantrole in the politicaldebatein Denmarkon eutro-
phication,and that it is a goodrepresentative for thoseinfaunalbenthicinverte-
brateswhichare sensitive
to eutrophication.

Coastal and Estuarine Studies, Volume 52, Pages 155-178
Copyright1996by the AmericanGeophysicalUnion
156 8. BenthicMacrofauna and DemersalFish
Landings,tonnesx103
20
15
10
0
1972 1975 1978 1981 1984 1987 1990
Figure8.1. Annuallandings
of thedemersal
fishspecies,
cod(blackbars)andplaice(greybars)
fromtheKattegat.Data fromICES(International
Councilfor theExplorationof theSea).
8.2. Effects on Fisheries
TheKattegatandSkagerrak arenaturallyproductivemarineareaswhichhavepro-
videdthe basisfor an extensive fisheryduringat leastthe past100 years.Fromthe
beginning of the 1980s,catchesof the demersalfish cod and plaice,however,de-
creaseddramaticallyin theKattegat(Figure8.1; ICES, 1992, 1993), whereascatch-
esof dab increased in southernKattegat[Baggeet al., 1993]. Thesechanges were
partly attributedto hypoxia,whichhasincreased in frequencyand spatialexten-
sionduringthe 1980s [e.g.,Badenet al., 1990a;chapter1, this vol.]. Catchesof
plaiceand dab havebeenlow in south-eastern Kattegatwhenoxygenconcentra-
tions were low in autumn [Pihl, 1989; Petersenand Pihl, 1995]. This was inter-
pretedasthe resultof an avoidance reactionby the fishand/orof directmortality.
A factorcontributing to the decreasein plaiceand cod stocksin southernKattegat
maybe the adverse effectson youngstagesdueto eutrophication-induced massoc-
currence of filamentous algaein nurseryareas[Baggeet al., 1990]. Concurrent
with
the decreasein stocksize,the individualmean size of plaiceand dab has
Hagerman,
Josefson
andJensen 157
decreased duringthe 1980s[Baggeet al., 1993;Petersen andPihl,1995].A number

of explanations relatedto eutrophication havebeenproposed to accountfor these
changes, e.g.physiological stress,
causingstarvationduringhypoxicperiods [Peter-
senandPihl,1995]andfoodlimitationof plaice.Theabundance of foodpreferred
byplaice,benthicbivalves andcrustaceans [Blegvad,1930],hasdecreased [Bagge
et al., 1993],whilefooditemsusedby dab,mostlybrittlestars,haveincreased in
abundance [Pearson et al., 1985;Josefson andJensen, 1992a,b;Baggeet al. 1993].
In contrastto plaice,dabshowan increasing standingstockin southern Kattegat
[Bagge et al., 1993]. However,noneof thesehypotheses haveyet beenverified,and
Bagge et al. [1993]suggested that foodlimitationisnota likelyexplanationfor de-
creased growthin plaiceand dab.
Theimportantfisheryfor Norwaylobsteris alsoaffectedby eutrophication. It is
knownthat low oxygenlevels,in additionto causingstarvation[Hagermanand
Baden,1988],mayforcethelobsters to emergefromtheirburrowsup on thesedi-
mentsurfacewherethey are more easilycaughtby trawls [Baggeand Munch-
Petersen,1979]. This increasedcatchability
is evidentfrom dataon the catchper
uniteffortfromsouth-eastern Kattegat[Badenet al. 1990b],whichshowpeakval-
uesduringhypoxicconditionsin autumn.The samestudyindicatesa localdrastic
decreasein the lobsterstock,with zerocatchin 1989, whereasfisherystatisticsdo
notindicatesimilarchanges overa largerareain the easternKattegat[Badenet al.,
1990b].Fishingfor lobsterin southernKattegatbecameunprofitableand nearly
stoppedat the endof the decade[Badenet al., 1990a]andthe fisherymovednorth-
ward,whichin itselfmayindicatea generaldecrease of thestock.
The mostnegativeeffectsof progressing eutrophication on fisheriesof demersal
fishare apparentin the Kattegat,whereasfew effectshavebeenreportedfrom the
$kagerrak,andthey are at leastnot apparentfrom the dataon fishlandingsduring
theperiod1972-1987 whencombinedfor Skagerrakand Kattegat(ICESdata in
Josefson
[1990].
To conclude,althoughdirectfield evidence for effectsof eutrophication
on thefish-
eryexistsfrom local areasand althoughseverallikely mechanisms havebeenpro-
posedfor this, the fisherystatisticssuggest
differenttrendsin the Kattegatand in
theSkagerrak whichat presentare difficultto explainonlywith overfishing.
8.3.Effects of Increased Food Levels on Macrobenthos
Asa consequence of eutrophication,an enhancedsedimentation of phytoplankton

to the seafloor will increasethe food supplyto the benthicfauna.Unlessfactors
suchashypoxiaandavailablephysicalspacearelimiting,thebenthicfaunais likely
to respondto an increased foodlevelby increased abundance and biomass (stand-
ing stock).Amongthe underlyingassumptions for sucha response are, that the
macrobenthos is normallyfood-limited,andthat mortalityratesremainunchanged.
Examples givenin thefollowingfromthe$kagerrak-Kattegat aremostlyfromben-
thosof offshoresoftsediments, wherephysicalspaceisunlikelyto bea limitingfac-
tor [Peterson,
Severalstudiesin adjacentsea areas have demonstratedincreasedabundance

and/orbiomass in recentyears,someof themattributingthechanges to eutrophica-
tion:the BalticSea[Cederwalland Elmgren,1980; Brey,1986], the DutchWadden
Sea[BeukemaandCadee,1986], and the centralNorth Sea[Kr6ncke,1992].
Althoughit is well knownthat macrobenthos may respondto increasedorganic
load by increasingthe standingstock [Pearsonand Rosenberg,1978], little is
known about the mechanisms
involved. Questionsto be further addressedare:
Whichcomponents of theorganicmaterialaremostimportantasfood,howisphy-
toplanktontransportedto the benthos,what are the most important response
mechanisms of the benthos,what is the expectedresponse
time, which faunalcom-
ponentsarefavored/disfavored?
Benthicspeciesmay respondto increasedfood levelsby increasedindividual
growthrate and/orincreased numberof individuals[Dauerand Conner,1980].
The latterresponse
mayinvolveincreased survivalof juveniles
or increased
repro-
ductivefitness[Levin, 1986], thus leadingto an increasednumberof recruits.
Whilegrowthof the residentanimalswill startsoonafter a phytoplankton sedi-
mentationpulsehas reachedthe bottom [Graf et al., 1982; Christensenand Kan-
neworff,1985], effectson recruitmentwill.be evidentonly sometime after the
food input, typicallyafter a year or more [Johnsonand Wiederholm,1992].
Whichof thetwo mechanisms of biomass increase
will dominatewill dependon
factorssuchasthetimeof foodinputto thebottomrelativeto the growthpoten-
tial andstagein thereproductive cycleof thebenthicpopulations,
the magnitude
of the input,etc.
8.4.Effectson Benthos
in the Kattegat-Skagerrak
Area.
Thegreateconomic importance of fisheryafterdemersal fishandthe factthat this
fishcategoryutilizesmacrobenthic species asfood[Blegvad, 1930]weretheback-
groundfor an extensive mapping of benthos in Danishwatersin thebeginning of
thiscentury[Petersen, 1913,1915].The resultwasa uniquematerial,a database,
froma relatively
pristinetimeperiod,against whichtherecentstatusof thebenthos
canbecompared. Comparisons of the faunalbiomass andspecies composition in
the1980swiththesituation in thebeginning of thecenturyin theKattegat-Skager-
rak [Pearson
et al., 1985;Rosenberg et al., 1987;Josefson andJensen, 1992a]have
shownmarkeddifferences (Figure8.2). Lowerbiomasses of the total macrofauna
in the1980swereobserved at shallowdepths of <50 m, whileincreases weredomi-
nantat greaterdepths.At intermediat•e depthsbothdecreases and increaseswere
observed.Seaurchins(Echinocardium cordatum)andsomemolluscs haddecreased
whereasbrittle starsand polychaetes had increasedtheir biomass.The most
markedincrease, >10-fold,of an individual specieswasfoundfor thefilterfeeding
brittlestar,Amphiura
filiformis,
in thesouthern Kattegat.
Generally,
therewasa
shiftfromlargeto smallspecies
anda decreasein individual
sizewasalsoapparent
withinthedominatingspecies,Amphiurafiliformis[Josefson
andJensen, 1992a].
Rosenberg andM/311er
[1979]compared thefaunain Swedish fjordsduring
Hagerman,
Josefson
andJensen 159
Biomassdifference,g w.wtm-2
+400
+200
-200
-400
-600 , , , • , , .- Depth, m
10 20 50 100 200 500
Figure8.2. Comparisonof total benthicmacrofaunal

biomass(raw weight)in the
Kattegat-Skagerrak
betweenthe1980sand1910splottedagainst
waterdepthona logscale.
Data from Pearsonet al. [19851,squares;Rosenberg et al. [1987], circles;Josefson
and
Jensen[1992a],triangles.
+ indicates
increaseand- indicatesdecreasesincethe1910s.
1970, beforehypoxia-induced
problemsbecameapparentin the Kattegat,and
showedincreasedbiomassof the total macrobenthos
in the 1970s irrespective
of
depth.
Timeseriesof benthosmeasurements
with at leastannualsamplingfromtheperiod
1973-88in theeasternSkagerrak
andnorthernKartegat [Josefson,
1990]suggesta
doublingof thetotalmacrobenthic biomass duringthisperiod,withthefastest in-
crease
in thelate1970sandearly1980s[Austen et al., 1991;Josefson et al., 1993].
In mostplacesthe biomass increase wasaccompanied by an increasein thetotal
density
of individuals [Josefsonet al., 1993].With a ca.one-year timelagat 100m,
andtwo yearsat 300 m, biomass, andin mostinstances alsodensity,measured in
spring,weresignificantly correlatedwith runofffrom surrounding land areas,
whichdetermines the inorganicN-nutrientpool for the springphytoplankton
bloomand the annualmeanchlorophyll-a concentrations in the euphoticzone
[Josefsonet al., 1993;chapter9, thisvol.].Examples of therelationbetween
Biomass,g w.wt 0.1 m-2

25- -
b
100 m 300 m
r• 0.76 r • = 0.58
20- = -
!5-
!0-
• ee
5-- -
I 1 1 I I I I 1
0 1 2 3 4 0 1 2 3 4
Chlorophyll-a,
pgI-• Chlorophyll-a,
Ijg I-•
Figure8.3. Benthicbiomass in springat 100 m (a) and300 m (b) depthplottedagainstmean

annualchlorophyll-a in theeuphoticwatercolumn,one(a) andtwo (b) yearsearlier,during
theperiod1973-1988.Basedon datain Josefson et. al [1993].
columnchlorophylland biomassfrom 100 and 300 m water depthare shownin

Figure8.3. The changesof the benthosduring 1973-1988 involvedchangesin
speciescompositionandin dominance patterns[Austenet al., 1991;Josefsonet al.,
1993]. The greatestincreases in dominancewere shown by ophiuroids,notably
Amphiurafiliformis,and polychaetes [Josefson, 1990], specieswhich werealready
presentamongdominants at the beginningof the period.
A studyof somaticgrowthin the one species contributingmostto the increasein
total macrobenthicbiomass,Amphiurafiliformis,showedthat growthrateswereat
leastequallyhighin the beginningof the 1980sat highdensities
and largeindivid-
ual sizecompared to the 1970s,suggestinghighenergyinputto the bottomduring
thisperiod[JosefsonandJensen,1992b].
The generaldoublingof biomassin Kattegatwas of the samemagnitudeas for
chlorophyll-a concentrations in the euphoticzone [Josefson et al., 1993] and for
primaryproduction(e.g.,Richardsonand Heilmann, 1995). Studiesof sedimenta-
tion in the Kattegatsuggestsedimentationtimesof one to severalweeksfor the
phytoplankton biomass to reachthe depthsof the presentarea(chapter4). A two-
yeartime lag betweenthe changes in the pelagicand the benthicresponse (when
sampling benthos in spring)isreasonable, providedthat thedominatingmechanism
of increaseis an increasedrecruitment dueto increased reproductive fitnessof resi-
dents.A similarlag betweenchanges in benthicbiomassor abundance andpelagic
chlorophylllevelshasbeenreportedfrom thewesternNorth Sea[Buchanan,1993]
and is evidentin time seriesfrom the southernNorth Sea [Beukema,1991; Beu-
kema and Cadee,1991]. The describedbiomassincreasehas occurredin an
Hagerman,
Josefson
andJensen 161
which,in contrastto southernKattegat,seldomexperiences

hypoxicconditions
in
thebottomwater.The biomassincreasemay thusbe explainedby increasedfood
inputto thebenthos
in the1980s.Thealternative
explanation
involving
decreased
mortalityis lesslikely because
the greatestmacrobenthic
biomassincrease
occurred
in areasfrom which landingsof potentialpredators,the demersalfish, have re-
mainedat the samelevel.it shouldbe pointedout, however,that otherexplana-
tionsin additionto eutrophication havebeenproposedfor benthicchanges in the
Skagerrakandthe North Sea.For instance, EvansandEdwards[1993] presented
evidence
of climate-relatedeffectsin the pelagicsystemin the westernNorth Sea,
whichin turn could haveresultedin increasedinput of organicmatterto the sea
floor in the 1980s.
8.5.AdaptationalandPhysiological
Effectsof Hypoxia
Benthicinvertebrates exposedto low oxygentensions showdifferentresponses due
to theirdifferentbehavioralstrategiesandphysiological tolerances.
Epibenthicspe-
cieshavemostlya low toleranceto decreased oxygentensions.Crustaceans suchas
Crangoncrangon,Palaemonadspersus, and Carcinusmaenasare examplesof this.
Mostspecies showinitial reactionsto hypoxiawhenthe oxyger•tensiondecreases
belowhalf air saturationand, just like mostfish, try to escapefrom the hypoxic
areaby walkingaway or swimminghorizontallyor vertically.They may alsomove
up from the sedimenton to stonesor algaewherethe oxygenavailabilityis often
higher.Animalsthat cannotescapereactto hypoxiawith otherbehavioror, if the
severeness of hypoxiaincreases, with physiological and biochemicalmechanisms.
The most stationaryspecies,which frequentlyhave to copewith hypoxiccondi-
tionsin theirhabitat,showmostlybettertolerances and havedeveloped moreeffi-
cientmechanisms to conserveenergyaslongaspossible.
It shouldbe pointedout, that it is the partialpressureand the availabilityof oxy-
gen,ratherthan the concentration of oxygenin the immediateenvironment, that
determines whetheran organismcan survivehypoxia.Thus,flowingwatercan in-
creasethe oxygenavailabilityconsiderably for a stationarybenthicanimalrelative
to stagnantwater.Thisis especially truefor smalleranimalslackingventilatory or-
gans.As longas the supplyof oxygencanmatchthe consumption, the animalwill
notsufferfromhypoxia,eventhoughtheoxygencontentin the watermaybe very
low.Experiments with smalleranimals,suchasjuvenileAmphiura,in whichwater
ispumpedthrougha respiratory chamber,will thustendto overestimate thein situ
toleranceto hypoxiasincethe experimental animalis continuously providedwith
moreoxygenthanundernaturalconditions. The criticaloxygencontentundersuch
experimental conditions
mayevenbesolow that it is difficultto determine.
Themostcommonhypoxiaresponse usedby species
with ventilatoryorgansis to
somehow increasethe oxygenavailability.Burrowingpolychaetes andmostcrus-
taceansincrease theirventilatoryratewhenoxygentensionsfall belowhalfair satu-
ration.They can in this way irrigateand oxygenatetheir burrowsand maintain
theirlevelof aerobicrespiration.Theybehaveasoxyregulators [Mangum,
Tem )erature, øC
20-
15-
10-
Te
5-
0- Abra
alba
• Macoma
balthica
• Astarte
borealis
%
' I ...... I' I" I I I '1 I I ' " I' " 1...... I .... I I.....I' I'"1 1 i i i
2 3 5 7 10 20 30 50 70 100 200
Exposure,days
Figure8.4. Effectof temperatureon the resistance

(LTs0)to anoxicconditionsin someben-
thicinvertebrates:
a polychaete,
T. stroemi,andthreebivalves.AfterDriesandTheede[1974].
The toleranceto completelyanoxicconditionsshowswide variationamongdiffer-

ent species.An activecrustacean,suchas Crangoncrangon,has an LTs0 (= the
time until 50% of the animalshavedied) in anoxia at 10øCof only two hours.At
the other extreme,the bivalve, Astarte borealis, from the western Baltic has an
LTs0of 2000 hours[DriesandTheede,1974]. Bivalvesgenerallyhavethe highest
tolerances, followedby polychaetes,e.g. Nereisdiversicolor:LTs0 100 hours,and
Terebellidesstroemi:LTs0 90 hours. Crustaceanshave the shortestsurvivaltimes.
One exceptionis the Balticisopod,Saduriaentomon,whichcan surviveup to 200
hoursof anoxia[Hagermanand $zaniawska,1990]. The presence of H2Sreduces
the survivalof severalspeciesunderhypoxicor anoxicconditions.On the other
hand, a high toleranceto anoxia is often combinedwith a toleranceto H2S
[Theedeet al., 1969; Vismann,1991]. This is importantin the habitat,asanoxiais
mostly,if not always,followedby an increased upwarddiffusionof H2Sfrom re-
ducedsediment layers(chapter6). The hightoleranceis mainlydueto mechanisms
at the cellularlevel.A sufficientcontentof metabolicstoragesubstrate/e.g.glyco-
gen)andthe abilityto reducethe overallmetabolicrequirements by reducingdif-
ferenttypesof activityarenecessary to achievethishightolerance.Low mobilityis
oftencorrelated with a low metabolicrate and thusa hightolerance,e.g.in sedi-
ment-dwelling bivalves,suchas Arcticaislandica.Amongrelatedspecies,those
with a highermetabolicrate and smallerenergeticreserves will generallyhavea
shortersurvivaltime. Anoxiaand H2S are toleratedbetterat low temperatures,
andthetolerance decreases
steeplywith increasing
temperature (Figure8.4) [Theede,
1984; Hagermanand $zaniawska,1992]. This suggests that specieswith a
Hagerman,
Josefson
andJensen 163
metabolicrate and smallenergystoreswill havea low anoxictoleranceandthusa

short survival time.
Echinoderms havealwaysbeenconsidered to be sensitive

to low oxygentensions
[Gaston, 1985],probablydueto theirrelativelylargesizecombined with a lackof
realventilatory appendages. As alreadymentioned, theyarequantitatively impor-
tant, especiallythe brittlestars,on or in soft bottomsof the Kattegatregion.
Rosenberg et al. [1991]observed thatat around10% of air saturation, Amphiura
emerged fromthe sediment, a behaviorthat increases theoxygenavailability con-
siderablyfor theanimal.It is,however,difficultundertheexperimental conditions
used,to conclude aboutthetolerance of Ampbiurato low oxygentensions in situ.
Otherechinoderms, suchas Echinocardium cordatum,whichare normallybur-
roweddeepwithin the sediment,seemto be the first species to escapefrom the
sediment uponanoxia,andmassmortalityhasbeenreportedevenat 30% air satu-
rationof oxygen[Detlefsen andWesterhagen, 1984].E. cordatomharborssulfide-
oxidizingbacteriain the intestine[Temaraet al., 1993],whichindicates the pres-
enceof sulfidein theintestine.E. cordatum thusprobablyrequires a sufficient
oxy-
gentensionfor a bacterialdetoxification of sulfideandfleesfromanoxicsediments
to avoid excessive sulfide concentrations.
The ability to withstandextensiveperiodsof low oxygenconcentration has been

demonstrated in severallaboratoryexperiments.It may thereforeappearaston-
ishingthat apparenteffectsof oxygendepletioncan be detectedin the field at
comparatively higherlevelsof oxygenconcentration.This discrepancy
might be
explainedas an artifact in the monitoringof oxygen.Measurements of bottom
waterconcentrations of oxygenare mostlydoneat a heightof 0.5-1 m abovethe
bottom,and may not be representativefor the oxygenconcentrationjust above
thesediment.Behavioralresponses of benthicanimalsexperiencinghypoxiaindi-
catethat a sharp oxygengradientmay existjust abovethe sediment.Thus, Jor-
gensen[1980] observedthat bivalvesextendedtheir siphonsup into the water
duringhypoxia.
Alsopredator-prey relationships
are affectedby oxygendepletion.Laboratoryex-
periments[Sandberg,1994] indicatethat the predatoryisopod,Saduriaentomon,
predatedlessefficienton a mobilespeciesof amphipodduringhypoxiathanon an-
otherlessmobileamphipodspecies. Changes in predationratemayalterthepopu-
lationsizeand dynamicsof the prey species and may especiallyin species-poor
communities causegreatchanges at thecommunitylevel.
Facultativeanaerobiosis is a generalphenomenon amongbenthicsoft-bottom
speciesbutthemetabolicpathwaysusedin anaerobiosis canvary.Anaerobiosis oc-
cursonlywhenthe oxygentensionhasdecreased to a levelwherebasicmetabolic
needscanno longerbe maintainedaerobically. It canbe eitheran exerciseanaero-
biosisor an environmental anaerobiosis[deZwaan andPutzer,1985]. The classical
glycolysiswith lactate(lacticacid) as an anaerobicendproductis foundin active
species,suchas crustaceans and someerrant polychaetes. Other groups,mainly
polychaetes and bivalves,accumulate fattyacidssuchassuccinate and,if the period
of anaerobic metabolism is prolonged,sometimes alsopropionate. The increase
iJmol
glucosyl
unitsg drywt-• IJmol g dry wt-1
...... Decrease of glycogen stores

800 - Accumulation
ofsuccinate -20O
Arctica islandica
600 - -!50
orearis
400 - -lOO
200 - - 50
o- i _ 0
0 10 20 30 40 50 6o
Days
Figure8.5. Decreaseof glycogenstoresand accumulation of succinateduringlong-term

anaerobiosisin somebenthicinvertebrates:
a priapulid,H. spinulosus,and two bivalves.
After Oeschger
[1990].
succinateis accompanied by a decreasein glycogen,for examplein the bivalves,

Arcticaislandica,Astarteborealis,and the priapulid,Halicryptusspinulosus,
which
are commonin soft bottomsin the westernBalticand Kattegat(Figure8.5)
[Oeschger, 1990]. Duringan initial phaseof short-termanaerobiosis,aspartateis
usedas a substrate givingopinesand acetateor alanineas endproducts. Someof
the moreactivepolychaetes,suchas Nereisdiversicolor,alsoproducelactatedur-
ing short-termanaerobiosis,for instanceduringlow tide [Sch6ttleret al., 1984].
Low salinitywill underseverehypoxiaor anoxiaresultin an increasedstressanda
reductionin survivaltime. An osmoticadjustmentto lower salinityrequiresenergy
andthe drainon energystoreswill be faster,thusresultingin a fasteraccumulation
of anaerobicendproducts as shownfor somepolychaetes(e.g. Arenicolamarina)
by Sch6ttleret al. [1990] (Figure8.6). The burrowingpolychaete,Nephtysho•n-
bergii,is rathertolerantto anoxia.It survives
at leastfivedaysat 12øC,and the an-
imal alsoremainsactivewith an aerobicmetabolism(but possiblywith functional
anaerobiosis)
downto 15-20 torr 02 and partly aerobicevenat 7 torr [Sch&tler,
1982]. No lactateis, however,producedin N. hombergii,but insteadopines
Hagerman,
Josefson
andJensen 165
IJmoles
g drywt-•
100
: : Acetate ,p 20%0
o. - - - ..o Propionate /'
,/, .,,o
32%0
50
•- .. 20%o
.• .- 32%0
1'2 2'4 3'6

Hours in anoxia
Figure8.6. Excretionof volatilefattyacidsbythelugworm,Arenicolamarina,afterdifferent

timesof anaerobicexposureand at differentsalinities.After Sch&tleret al. [1990].
to bethe anaerobicendproducts at the beginning andsuccinate laterduringanaero-

biosis(SchSttler,op. cit.). The highcapacityof active,burrowinganimalsfor main-
tainingan aerobicmetabolismduring severehypoxiais probablya characteristic
phenomenon. Tube-dwellinganimalshavea lower capacity,as theycancompen-
satefor low oxygenby increasing the ventilationrate and thusbringwaterfrom
abovedirectlyinto their tubes.
8.6.The Norway Lobster- a CaseAnimal

The Norway lobster,Nephropsnorvegicus, is economically
very importantin the
Kattegat-Skagerrakarea.The progressing hypoxiaduringthelastdecades hashad
a detrimentalimpact on the stock of this speciesand has motivateda Danish-
Swedish-British
collaborativeresearchon the ecophysiology
of N. norvegicus.
Nor-
way lobsters,whichweredeador dyingdueto hypoxia,werefoundfor the first
timein autumn1985. Oxygendeficiency was seriousin 1988 (< 15% air satura-
tion),lastedlonger,andreachedan extension of 4000 km2. No Nephrops were
caughtafterthat period.N. •orvegicus liveson andin mud-claybottomsof a con-
sistencywhichmakesit possiblefor the animalsto excavatehorizontalburrows.
Theyusetheirfirstthreepairsof pereiopods andthirdmaxillipeds
to excavateand
transportheapsof sediment to the openings [AtkinsonandTaylor,1988].Thebur-
rowscanbeof severaltypesrangingfroma singleopeningwith onlyoneinhabitant
in the shaftto burrowsconstitutinga networkwith manyopenings andmorethan
oneinhabitant.Most commonis a singleburrow ("U-tube") with two openings
[RiceandChapman,1971].Typically,oneopening isbroadandcraterlike (theen-
trance)with a heapof excavated
materialin front,whilethe otheropeningis sim-
ple[DybernandHoismter,1965].Theanimalsusethefrontopening for both
andentrance [FigureidoandThomas,1967].The burrowsoftenoccurin small

groups.Themostimportant functionof theburrowsis mostcertainlyprotection
frompredators.Otherfunctions
mightbeasmoulting siteandasthecenterof terri-
tory.N. norvegicus
leavesthe burrowfor foragingand for mating.Somefood
mightbebroughtbackto theburrowfor feeding. The burrowthusserves asthe
"home"for an individual.
Juveniles
ofteninhabitsmalltunnelsconnected to the
burrowsof the adults[Chapman,1980]. It is mostlymalesthat leavetheir bur-
rows for excursionsand under normoxic conditionsfemalesstay in the burrows
duringtheegg-carryingperiod(May-September) [Figureido andThomas,1967].It
isonlywhenhypoxicautumnconditions forcethefemales to emergethattheyare
caughtin greaternumbers.Nephropsis activelyventilating its burrow.By inter-
mittentbeating
of thepleopods, a currentof wateris circulated throughthebur-
row,thuspreventingit frombecoming too hypoxic(provided thewateroutsideis
moreor lessnormoxic).Observations
by Atkinsonand Taylor [1988] indicatethat
gillventilation
of thescaphognathites
canbesufficient
to preventhypoxicburrows
undernormoxicconditionsin the overlyingwater. It is also a possibilitythat a
bottomcurrentcanhelpa passive
exchange
of waterin the burrow(cf. Huettel
and Gust [1992]).
Experimental
investigations
haveshownthatwhentheoxygenconcentration
de-
creasesto ca.50% of air saturation,Nephropsrisehigheron their legs,showsigns
of restlessness,
and markedlyincreasetheir cleaningbehavior.At evenloweroxy-
gentensions,
theyemerge
fromtheirburrows[Hagerman
andUglow,1985]andat
10-20% of air saturationfeedingactivity stopsand they remain inactiveon
stretchedlegswith loweredclaws,if possible
on top of a smallmound,thustrying
to reachmoreoxygen-rich surroundings [Hallb•ickand Ulmestrand,1990]. It is
clearthat Nephropswill bemorevulnerable to trawl catchundertheseconditions,
obviouslyan explanationfor the increased autumncatchesin the early 1980s,
whichoccurredat the sametime as severehypoxia.
A usefulreactionto hypoxiais,asmentionedabove,to try to increasethe availabil-
ity of oxygen
byincreasingthewaterflowto thegills.The scaphognathite beatfre-
quencyof quiescent Nephrops increases
froma normoxic rateof ca.60 min-• to ca.
120 min-• at an oxygentensionof 40 tort. The heartrateremainsstableoverthe
samerangeof oxygentensions (Figure8.7) [Hagermanand Uglow, 1985]. This
mustberegarded asan acuteresponseto short-termhypoxia.Scaphognathite rates
will decrease
belownormoxicratesif hypoxiaprevailsfor weeks[Kwee, 1993]. In
commonwith otherdecapods,Nephropsshowsno ventilatorypausesor cardiac
arrests,whichare commonduringnormoxia,when subjectedto moderateshort-
term hypoxia.
Increasedventilationincreases
the extractionefficiencyfor oxygen(from 20-30%
to 30-40%) andthisis importantfor theabilityto maintainstable02 uptakelev-
elsduringhypoxicevents.HagermanandUglow[1985]calculated that,at halfair
saturation,
0.25ml waterwaspumpedperscaphognathite beatpergill, or 75 txl02
waspumpedpastthe gillseachminute.The extractionefficiency compares well
withan oxygen uptakerateof 15 txlg-• h-• for a N. norvegicus
of 1O0g wet
Hagerman,
Josefson
andJensen 167
Beats min -•
150 -
lOO
oø8ee ee ßß
eo ß ß ß
o
ß oo oo•
o 0
0 0 ooo
50 øo ß
O(
• 0 00 0
0
o 5'0
Pw02, torr
Figure8.7. Heart(0) andscaphognathite

(©) beatingfrequencies
in Nephrops
norvegicus
as
a functionof wateroxygentensions
(10øC,30-32 psu).AfterHagermanandUglow[1985].
The mostsensitive periodsof decapodlife, from an ecologicalas well as from a

physiological
viewpoint,arethe moultandimmediate postmoultstages,
whenthe
newcarapaceis stillsoft.The individualisduringthisstagean easyprey,somoult-
ingmusttakeplacein a protected place,i.e. in theburrow.Cuticlepermeability
is
increasedand so is the metabolic demand,which is shown as a considerablein-
creasein oxygenconsumption rate duringthe moultand immediatepostmoult
[Alcarazand Sard•, 1981]. It is thus obviousthat exposureto hypoxiaduring
moultingcanbedisastrousto theindividual. Juvenile
lobsters
moultseveraltimesa
year,whileadultsmoultoncea year[Figureido andThomas,1967].
Most decapods, and especially
the burrowingspecies,keeptheir respiratory
rate
stableovera widerangeof oxygentensions. The tensionwherestableoxygenup-
takeisno longerpossible
iscalledthePcor criticaloxygentension.ForN. norvegi-
custhis tensionhas beenfound to be ca. 40 tort [Hagermanand Uglow, 1985].
Downto thistensionit is possible
for thespecies
to maintainan activelife,feeding
etc.,whereas
belowthePctheactivityis decreased, feedingstops,andananaerobic
metabolismmay start.
Survival
at oxygen
tensionsbelowthePcis dependent ondurationand,themore
severe
thehypoxia,on energyproduction
via an anaerobic
metabolism.
In N. nor-
vegicus,
like in mostotherdecapods, glycolysis
is the majoranaerobic metabolic
pathway[Giide,1983].Glycogen is usedasa substrateandvia glucose- andfruc-
tosephosphate,phosphoenolpyruvate andpyruvate,lactate(lacticacid)isproduced
intracellularly
andleakedto thebloodwhereit accumulates andcanbemeasured. If
theanimalissuddenly exposed to hypoxia,lactateaccumulates at oxygen
168 8. Benthic Macrofauna and Demersal Fish
below15 torr (10% of air saturation).

If theanimalisgraduallyadaptedto hypoxia
overa 30-dayperiod,accumulation startsonly at 9-12 torr [Schliitter,1993]. The
animalssurvivefor onlytwo daysat 15 torr [Hagermanet al., 1990]. Obviously,an
anaerobicmetabolism startsat oxygentensions far belowthe Pcand, by beingtotal-
ly inactive,
N. norvegicuscanreduceitsmetabolic rateandutilizetheavailable oxy-
genin theinterval40-15 torr, whichis energeticallymoreefficientthanturningto
an anaerobicmetabolism. The accumulationof lactateis reversibleand uponreturn
of oxygenated conditionslactatecanbemetabolized in thehepatopancreas, whichis
accompanied by an increased oxygenuptake(oxygendebt) [Bridgesand Brand,
1980]. Evenif the animalis slowlyadaptedto severehypoxia,the survivaltime is
verylimitedandoncesevere hypoxia(< 10% of air saturation)hasdeveloped it isa
question of onlya few daysbeforethe populationof N. norvegicus dies.
A consequence of the initial hyperventilation duringmoderatehypoxiais an in-
creasein blood(haemolymph) pH, i.e. a respiratoryalkalosis.The increaseis from
a normoxicpH of 7.75-7.90 to a hypoxicpH of 7.90-8.10 at Po260 torr [Hager-
manandUglow,1985].The increased ventilationchanges the bloodacid-base bal-
ance by a wash-outof CO2, which decreases the haemolymphPco2(Truchot,
1983).Uponprolongedexposureto hypoxiaandespecially to severehypoxiaa res-
piratoryacidosis
occurs.Thisis mainlydueto theaccumulation of lactate.
Like mostothercrustaceans, Nephropsnorvegicushas the copper-containing hae-
mocyaninasrespiratorybloodpigment.The haemocyanin is not boundin erythro-
cytesbut is dissolved
in the blood.Haemocyaninshowsa considerable variation
amongindividuals depending on their feedingleveland moultstage.Starvationis
known to decrease decapodhaemocyanin concentration[Uglow, 1969; Hagerman,
1986] and the qualityof food influencesthe final level [Hagerman,1983]. It has
experimentally beenshownthat moderatehypoxia(half-saturation) inducesa syn-
thesisof haemocyanin in N. norvegicus. Despitea largeindividualvariation,bio-
synthesisaveraged 8% of theoriginalvalueperday,i.e. it took abouttwo weeksto
doubleor replacethe wholehaemocyanin pool. In N. norvegicus exposedto 60
torr (approx.half-saturation)for 12 days,haemocyanin concentration increased
fromthenormoxicvalueof 0.28 mmol1-• to hypoxic0.59 mmoll-j, whereascon-
trolsshowedno changes [HagermanandUglow,1985].This synthesis is supposed
to servea compensatory functionfor the loweredoxygentensionof the ambient
water, but the responserequiresan appropriatefeedinglevel.Starvedcrustaceans
showno suchsynthesis of haemocyanin but can insteadusethe haemocyanin asa
proteinresource
with a verylowhaemocyanin levelastheresult[Hagerman,1986].
At oxygentensionsbelow30 torr, thehaemocyanin concentration
decreases
rapid-
ly. N. norvegicus
usesitshaemocyanin for metabolic needswhenits stopsfeeding
(hypoxia-induced
starvation}[Schli•tter,1993].
Verylow haemocyanin
levels(0.03mmol1-• bloodascompared
to 0.5-0.8 mmol
1-• for well-fednormoxicindividuals)were found in N. norvegicuscollectedin
areassubjected to severehypoxia(13-22 torr} in southernKattegatin the autumn
1986 [Hagermanand Baden,1988]. Suchlow haemocyanin levelsmakeN. nor-
vegicus
evenmorevulnerable
to hypoxia.Haemocyanin
isespecially
under
Hagerman,
Josefson
andJensen 169
conditions
the importantcarrierof oxygento the tissues
and a lowerconcentration
of haemocyanin
transports
lessoxygen,evenif it functions
in a normalway.
Autumnstormsnormallyreoxygenatebottom waters.This was alsothe casein
southernKattegatin 1986 and one monthafter reoxygenationthe meanhaemo-
cyaninconcentrationin N. norvegicus
hadincreasedto 0.76 mmol1-•, a dailysyn-
thesis
rateof 0.024mmol1-• bloodasalsoshownin theearlierexperimental studies
[Hagerman and Uglow, 1985; Hagermanand Baden,1988]. The recoverywas,
however,veryslowor evenabsentin someareas.Feeding experiments haveshown
thatonlydecapods whichhaveothercrustaceans asimportantfooditemscansyn-
thesizehaemocyanin to optimal levels[Hagerman,1983; Depledgeand Bjerre-
gaard,1989;Badenet al., 1990b].Thecontentof crustaceans
in thestomachsof N.
norvegicusfrom southernKattegatafterreoxygenation of the bottomwaterwas
onlyVslowerthanin thosefrom northernKattegat.Severe hypoxiameansstarva-
tionnot only to N. norvegicusbut alsoto other benthiccrustaceans
aswell as other
invertebrate
groups.As foodis themostimportantsourceof essential proteins,vita-
minsandminerals(incl.copper),it is possible that a mineraldeficiency mighthave
preventedtheposthypoxic biosynthesis of haemocyanin in someareas[Badenet al.,
1990b].It hasalsobeennotedthat manganese isleakingfromthesediment during
severehypoxia[Garringaet al., 1991;Thamdrupet al., 1994].Thismanganese can
bedeposited asmanganese dioxideon thegillsandcarapace of N. norvegicus,and
it wasobservedthat, ascopperconcentrations fell in sometissues, manganesecon-
centrationsmarkedlyincreased [Badenet al., 1994]. It is thusa possibility
needing
furtherstudythat manganese might interactwith copperduringrecoveryfrom
hypoxiaandinfluencebiosynthesis of haemocyanin.
The concentration of haemocyanin indicatesindirectlythe amountof oxygenthat
canbe boundto the pigment,but saysnothingaboutat what oxygentensionthe
bindingcan and will take place.This oxygenaffinityis expressed by the ps0,the
oxygentensionwhere50% of the haemocyanin is saturated with oxygen.The affini-
ty for oxygencan vary with the environmental conditions[Mangum,1983] and
oftensothat species subjectedto hypoxiacan take up oxygenmoreeasilyfrom the
water,i.e. they have a higheraffinity for oxygen.Burrowingspeciesalsotend to
havea higheraffinityfor oxygen[Bridges, 1986]. N. norvegicus adaptedto normox-
ic conditions were foundto havea Ps0of 11.5 torr at pH 7.9 [Bridges,1986] and a
slightly,butnot significantly,higheraffinityin hypoxia-adapted individuals[Schltit-
ter,1993].The oxygenaffinitycanbemodifiedby severalextrinsicandintrinsicfac-
tors. One suchintrinsicfactor is the lactateconcentration in the haemolymph.
Lactatecanimprovethe oxygenaffinityand this improvement can counteractthe
decrease in affinitycausedby the lactate-induced loweringof pH [Truchot,1980].
In N. norvegicus, haemolymph lactateimprovedPs0ca. 3 torr, i.e. from 11.5 to 8.5,
andthisis similarto what hasbeenfoundfor otherdecapods [Zeiset al., 1992].
Alsourate(uricacid),whichaccumulateduringhypoxialowerthan ca. 25 torr, can
modifytheoxygenaffinityof haemocyanin [Lallieret al., 1987].Theecological con-
sequence of the modifiedaffinityis a betteroxygenuptakeat severehypoxia,which
will enableN. norvegicus to utilizean aerobicmetabolism longerbeforean anaero-
bicmetabolism is totallytakingover,i.e. anincreasing hypoxic
Anoxicsediments richin decomposingorganicmaterialoftencontaintoxichydro-

gensulfide.Whenreachingthe oxic zone,hydrogensulfideis oxidizedto thiosul-
fateandsulfate(chapter6). Whenseverehypoxiaoccurs,hydrogen sulfidecandif-
fuse out into the burrow water or the near-bottom water. Some macrobenthic
species,
generally
thosethatmaybetemporarilyexposed to hydrogensulfidein the
environment,havedeveloped tolerancesanddetoxification mechanisms [Vismann,
1990; Vismann,1991]. It is possiblethat N. norvegicusin certainareasis exposed
to hydrogensulfidefrom the sedimentduringsevereautumnhypoxia,but it is not
knownwhethertheyhavedeveloped suchmechanisms.
The physiological ecologyand adaptations to hypoxiaof the Norway lobsterare
typicalfor the largerbenthiccrustaceans.
A speciesshowingextremelygoodadap-
tationto hypoxiaand evenanoxiais the Balticdiggingisopod,Saduriaentornon,
whichhasan anaerobicmetabolismwith alanineor lactateasendproducts, depen-
dingon inactivityor activity,respectively,
duringthe anoxicexposure.It hasalso
theabilityto extractoxygenveryefficientlyfrom the waterdueto a veryhighoxy-
genaffinityof the haemocyanin. S. entomonshowsan excellentability to detoxify
hydrogensulfide(Vismann1991, Hagermanand Vismann1993). The ecological
physiology of S.entomonwasreviewedby HagermanandSzaniawska (1992).
8.7.Effectof Hypoxiaon MacrobenthicCommunities

Severeseasonal hypoxiaandanoxiamay leadto areasof the seafloor totallyde-
voidof macrofauna, yet thissituationis rare.Such"deadbottoms"withoutmacro-
scopiclife havebeenobserved occasionally in North Europeanwaters[Josefson
and
Widbom, 1988; Fallesen,1992] and, in particular,in partsof the BalticSea[Wei-
geltand Rumohr,1986; Andersinet al., 1990].
Reductions in species
diversity,abundance an.dbiomassdueto hypoxiaandanoxia
have beenobservedin parts of the North Sea,the Kattegat,and the Baltic Sea
[WeigeltandRumohr,1986;Westernhagen et al., 1986; Rosenbergand Loo, 1988;
Andersinet al., 1990; Niermannet al., 1990; Josefsonand Jensen1992a; Rosen-
berget al., 1992].Partsof the GermanBightwereaffectedby oxygendepletionin
theperiod1981-1983andverylow oxygenconcentrations in 1983 (< 1 mg021-1)
causeda reductionin species diversity,abundanceand biomass[Niermannet al.,
1990]. Recoverytook placeduringthe followingyearsand in 1986 the "prehypox-
ic" benthic fauna had been reestablished.
A severeand wide rangingoxygendepletionin Kiel Bay, westernBaltic Sea,in

1981 resultedin a decrease
in biomass,abundanceand speciesdiversitybelowthe
halocline[Weigeltand Rumohr,1986]. Only a few speciessurvived,notablythe
bivalvesArcticaisIandica,Astartespp., and Corbulagibba, and the sipunculid,
Halicryptusspinulosus.Theseare amongthe specieswhich in laboratoryexperi-
mentshavebeenparticularlyresistantto hypoxiaand anoxia.A reviewof the
macrofauna
datafromKielBayindicates a shiftfromlargerto smallermeansizeof
individuals[Weigelt
Hagerman,
Josefson
andJensen 171
Hypoxiaand anoxiamay resultin a shift in species distributions.

Fallesenand
Jorgensen[1991] observeda shift in the distribution
of the polychaete species,
Nephtyshombergii andNephtysciliata,followinga severeoxygendepletion in
]trhusBay,Denmark, in 1981.Before theoxygen depletion,
thedistributions
ofthe
two specieswere complementary due to differencesin their sedimentpreference,
whileafterthe oxygendepletion,N. hombergiidominated the wholeareaas a re-
suit of their successfulrecolonization in 1982.
Lowconcentrations of oxygen(< 1 ml 1-h)wereobserved in partsof the southern

Kattegatin autumn1988 [/Ertebjerget al., 1990; Rosenberg et al., 1992]. Mass
mortalityof Abraalbaandreportsof largenumbers of deadinvertebrates captured
in demersal fishtrawlsin south-eastern Kattegatwerecoupledto thisevent[Baden
et al., 1990]. Stationssampledin 1911/1912 by Petersen[1913] and in 1984 by
Pearson et al. [1985] wererevisitedin orderto detectpotentialeffectsof the 1988
hypoxiaeventon the benthicmacrofauna [JosefsonandJensen,1992a].The results
indicated reductions of biomassin 1989 comparedto 1984,whereastheabundance
wasunchanged. The greatestbiomassreductionsof 70-80% were foundin areas
wherethe oxygenconcentration was below 1 ml 1-• in autumn1988 (Figure1.6).
The decreases in biomassweremostpronounced at depthsjustbelowthe halocline
at 15 m waterdepth.An explanationfor thismaybethatthe initialpoolof oxygen
availablefor the oxidationof phytoplanktonsinkingbelowthe halocline,which
actsas a barrierto the exchangeof oxygen,is proportionalto the heightof the
watercolumnbelowthe halocline.Rosenberg and Loo [1988] andRosenberg et al.
[1992] alsofund the largestdecreasein biomassat stationsjust belowthe halocline
followingthe hypoxiceventin autumn1988 in south-eastern Kattegat,wheresen-
sitivespecies were eliminated,thusleavinghypoxia-resistant species suchasthe bi-
valve,oceanquahog(Arcticaislandica).
The resultsof a 1989 revisit[Josefsonand Jensen,1992a] confirmedthe general
differences
at the species
levelfoundin 1984 as comparedto the situationin 1911-
1912. The biomassand abundanceof the brittle star, Amphiura filiformis,were
stillmuchhigherandthe biomass of theechinoid,Echinocardium cordatum, was
stilllowerthan in the beginningof the century.A previously observed decreasein
themeanindividualweightof the total fauna[Pearson et al., 1985] hascontinued,
andthemeanweightwason the average 50% lowerin 1989compared with 1984.
Severalphyla of invertebrates contributedto this decrease, althoughespecially
ophiuroids (primarilyAmphiurafiliformis)andpolychaetes decreased in size.The
change towardsmaller-sizedanimalsmayresultfromhypoxia-induced elimination
of olderindividualsandensuing recruitment of juveniles.
A comparison of benthosdata from the beginningof thiscenturywith present
monitoringdatain southern
Lillebruit,
Denmark,suggests that thearealextension
of azoicbottomshasincreasedand that species
whichare sensitive
to low oxygen
concentrations
havedecreasedthroughoutthe area[Leonhard& Varming,1992]
(Figure
8.8. Conclusions
Boththe synopticcomparisons over 80 yearsand time seriesfrom the last two

decadessuggest an increasein benthicmacrofaunal biomass at waterdepthsgreater
thanca. 50 m in the northernpart of the Kattegatand easternSkagerrak.At depths
shallowerthan 50 m, mainlyin the Kattegat,reductions of biomasshaveoccurred
in severalplaces.Thisis alsothe areafrom whichadverseeffectson fisheries have
beenreported.
How do the observed changes of macrobenthos populationsfit with predictions
fromprevious modelsof eutrophication-induced responses in the benthos?Existing
modelsby Pearsonand Rosenberg [1978] and Rhoadsand Boyer [1982] allow
qualitativepredictions of successional
patternsin relationto changedorganicload.
For instance,theypredictdominance of small-sizedspeciesor individualsanddom-
inanceof species feedingat the sediment-water interfacein contrastto deep-bur-
rowingforms,in areasaffectedby eutrophication. Indeed,suchchangesseemto
haveoccurredin the Kattegat.It is not known,however,to what extentintensive
trawlingfor fishandlobsterhavecontributedto thischange,sincetrawlingmaybe
expected to affectsizein a similarmanneraseutrophication [e.g.,Graham,1955].
The Pearsonand Rosenberg [1978] modeldescribes an increasedbiomassearlyin
the eutrophication process, whereaslater, whenoxygenconditionsdeteriorate,the
biomass will decrease andeventuallythe originalspecies will be replacedby oppor-
tunists.Whenlookingat theKattegat-Skagerrak areaasa whole,the changes in the
benthosappearto conformto this model.Generally,the energyinput to the ben-
thosis inversely relatedto the water depthand directlyrelatedto the phytoplank-
ton productivity in the overlyingwater [Suess, 1980]. Thus,whenthe levelof nutri-
entenrichment increases, whichhasoccurredduringthe lastdecades,we wouldex-
pecta response in the benthiccommunitywhichdependson the water depthand
the distanceto the mainnutrientsources.In deepareas,distantfrom the productive
zone,the biomass generallyshowedan increase, whereasin shallowareas,someof
themsituatedin the euphoticzone,spatiallyandtemporallyhighlyvariablehypox-
ia hasoccurred,whichhascausedreductionsof biomassand individualsize(Figure
1.6). It maybe morethan a coincidence that someof the directevidencefor hypox-
ia-inducedfaunal reductions[Rosenbergand Loo, !988; Josefsonand Jensen,
1992a;Fallesen,1992; Rosenberg et al., 1992] derivesfrom the pycnoclinedepthin
theKattegat,wherea largepart of the primaryproductionoccurs[Richardson and
Christoffersen, 1991] and whereoxygenationimmediatelybelow this water layer
maybe restricted. However,onlylimitedpartsof the areaseemto havereachedthe
stage,whereopportunistic polychaetes (e.g. CapitelIaspp.)dominate,or eventhe
azoic
Hagerman,
Josefson
andJensen 173
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Experimentswith the isopodSaduriaentomon,Mar. Ecol. Prog.Ser., 103,
73-80, 1994.
Schli•tter,H., Haemocyaninsiltbindingsevne og affinitetsmodulerende
faktorer hos jom-
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Sch6ttler,U., An investigation on the anaerobicmetabolism of Nephtyshombergii(Anne-
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Sch6ttler,U., B. Surholt,and E. Zebe, Anaerobicmetabolismin Arenicolamarinaand Nereis
diversicolor duringlow tide,Mar. Biol., 81, 69-73, 1984.
Sch6ttler,U., D. Daniels,andK. Zapf, Influenceof anoxiaon adaptationof euryhalinepoly-
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Temara,A., C. De Ridder,J. G. Kuenen,and L. A. Robertson,Sulfide-oxidizing
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the burrowing
echinoid
Echinocardium
cordatum
(Echinodermata),
Mqr. Biol.,115,
179-185, 1993.
Thamdrup,
B.,R.N.Glud,
andJ.W.Hansen,
Manganese
oxid.
ation
and
/xnsitu manganese
fluxesfrom a coastalsediment,Geochim.Cosmochim.Acta, 58, 2563-2570, 1994.
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approaches
to environmental
problemsof the Baltic,Limnologica
(Berl.), 15, 443-458, 1984.
Theede,H., A. Ponat,K. Hiroki, and C. Schlieper,
Studieson theresistance of marinebottom
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9
Shallow Waters and Land/Sea Boundaries
JensBorum
9.1. Introduction
Two importantissuesrelatedto eutrophication and shallow-water

ecologywill be
discussedin thischapter.The first concerns the roleof shallowwatersasrecipients,
transportersand sinksof nutrientloadingfrom land.Attentionis primarilydirected
towardnitrogen,asit is thisnutrientthatis believed to bethemainlimitingnutrient
forplantgrowthandprimaryproduction in temperate coastal
waters[RytherandDun-
stan,1971; Gran•li et al., 1986]. The secondissueaddressedis how nutrientenrich-
mentinfluencestheautotrophic communities andtheprimaryproduction on whichall
otherbioticcomponents andprocesses withinthecoastalzoneultimatelydepend.
Forpracticalpurposes, "shallow"coastalwatersin thepresentcontextaredefinedas
marineandbrackishareaswith waterdepthsof lessthan20 meterswhichrepresents
theapproximate depthlimit to whichbenthicplantsmaycontributesubstantially to
primaryproduction. Thiszoneincludes a largepartof themarineDanishareas,ex-
tendingfroma fewto morethan50 kilometers fromthecoast,andcovers anareaap-
proximately of the samesizeas the land area.The topography of Denmarkis of
glacialoriginandestuariesandembayments aretypicallyshallowwithsandyor silty
sediments.AlthoughtheDanishterm"fjord"is a common namefor estuarine areas,
it shouldnot be confused with the classicalNorwegianfjord. Only a few Danish
fjordshavea sill anddeepinnerbasins. The tidalamplitude
variesfrom2 metersin
theWaddenSeato a few centimeters in someestuariesandin partsof theBeltSea.
9.9..Nutrient runoff
Reliableestimatesof total nutrientrunofffrom land onlyexistfrom the mid-1970s

(Figure9.1) and, therefore,do not includethe periodof exponential
increase
in
agricultural
andurbannutrientrunoffduringthe 1950sand 1960s.Pointsource
Eutrophication
in CoastalMarine Ecosystems
Coastaland Estuarine Studies,Volume 52, Pages179-203
Copyright
1996by theAmerican
Geophysical
Union
180 9. ShallowWatersand Land/SeaBoundaries
.,
300 a Nitrogen
• ? 200
'- E
o-•
Z v 100
i , , • • , ' i' ', ':",'- •: •' 'i' "•" , , ß i ", ',
8
b Phosphorus
oT
o fl_ 4
o .
0 ; ;-..... ... ... • .... ,. .
975 1980 1985 1990
Year
Figure9.1. Area specificnitrogen(a) and phosphorus(b) runoff from the countyof Fyn
(3505 km2),Denmark.Contributions from urbansewage,industrialwastewaterand other
point sources(shadedbars) and from diffusesources(open bars). Data from FynsAmt
[1993].
nitrogencontributionswere relativelyconstantfrom 1976 to 1988 and thereafter

declineddue to the implementation of advancedsewagetreatment(Figure9.1a).
The largestcontributionto nitrogenrunoff,hoxvever,is from diffusesources,which
remain highlyvariablefrom year to year dependingon climate and rainfall. Con-
sistentwith a constantapplicationof fertilizerssince1980, no systematicreduction
of nitrogenrunoffhasbeenobserved from 1976 to 1992 (Figure9.1a).
The phosphorusrunoff was slowly reducedfrom 1976 to 1988 but after 1988
declinedrapidlyand is now only 20-25% of the levelbefore1988 (Figure9.lb).
Consequently, Danish coastalareas have experienceda substantialreductionin
phosphorus loading,while nitrogenloadinghas beenmoreor lessconstantduring
the last 15-20 years.Typically,nitrogenloadingper squaremeterof Danishcoastal
watersis of the samemagnitudeas, or evenlarger than, nutrient applicationto
heavilyfertilized
Borum 181
9.3.Nutrient Retentionin CoastalEcosystems

The coastalzone plays an important role as a filter insertedbetweenland and
oceanby retainingsuspended materialsand nutrientsfrom land [Sharpet al., 1984;
Nixon andPilson,1984].Basicunderstanding and quantitativeknowledge of nutri-
entretentionand lossesin coastalwatersare essential
to evaluateand predictopen-
watereutrophication.One needsto know how muchof land runoffactuallyreaches
theopenwatersto be ableto evaluatethe presentroleof runoff versusnutrientde-
position
fromtheatmosphere
(Figure9.2).
Nitrogenand phosphorus from land enterthe biogeochemical cyclesof the coastal
areasand are lost by sedimentburial and, in the caseof nitrogen,by bacterialdeni-
trificationunderanoxicconditions(Figure9.2). Nutrientscontainedin importedor
autochtonouslyproducedorganic particlessettle on the sedimentsurfaceor are
subjectto biodepositionby benthicsuspension feeders.Ratesof grosssedimenta-
tion in shallowmarineareasare veryhighdueto frequentresuspension of the sedi-
mentsurfacelayers(cf. chapters6 and 7), and the traditionaluseof sedimenttraps
givespoor informationon net sedimentation rates.Net ratescan be measured by
analysisof sedimentdepthprofilesof nutrientscombinedwith 2•øpbdating,but
time resolutionis poor, in the order of decades,dueto resuspension and bioturba-
tion of the estuarinesediments[Floderus, 1992]. Therefore, we have no simple
LAND COASTAL ZONE OPEN SEA
N2 N2 N2
NO x NO x NO x
NH 3 NH 3 NH 3
N:
run..
o• •N-ex
N-import
Sediment burial
Figure9.2. Schematicpresentationof nitrogenloading,retentionandtransport withinthe

coastalzone.Nutrientsfrom land are graduallyretainedby sediment
burialor lostthrough
denitrification
duringtransportfrom landto opensea,whilethe relativeimportance of
atmospheric andoceanicinputincreases withdistancefrom
182 9. Shallow Waters and Land/Sea Boundaries
T A BL E 1. Temperate
coastalecosystemsfor whichnutrientmassbalances
havebeenestab-
lished.Localities,
meannutrientinputs,and references.
mmol m-2 d-•

Locality N input P input Sources
Narragansett
Bay 6.6 - Seitzingeret al., 1984
LoughHyne 5.4 0.31 M. Johnson, pers.comm.
BothnianBay 0.54 0.006 Wulff et al., 1990
Baltic Sea 0.65 0.016 Wulff et al., 1990
RoskildeFjordarea1 6.7 0.41 Kamp-Nielsen,1992
,, area2 6.2 0.34 Kamp-Nielsen,1992
Limfjorden 4.8 - Countyof Viborg
RingkobingFjord(1987-1991) 4.6 0.10 Countyof Ringkobing
MariagerFjord (1986-1992) 6.4 - Countyof Nordjylland
NorsmindeFjord 23.9 - Countyof Aarhus
meansof resolving seasonal

or annualchar•ges
in sediment
nutrientburialfollow-
ingalterationin anthropogenic
nutrientloading.
While benthicburial is the main phosphorus sink duringtransportfrom landto
opensea,sediment accumulation of nitrogenaccountsfor lessthan20% of total
nitrogenremovalin estuaries. The restis lostby reductionof nitrateto gaseous
nitrogen[Seitzinger,
1988;1990;Billenet al., 1991;chapter6, thisvol.].Thedeni-
trificationprocess
is drivenby nitratediffusinginto the sedimentfrom the water
columnand by couplednitrification-denitrificationwithin the sediment[Jenkins
andKemp,1984].Denitrification ratesin coastalmarineareasrangefrom0 to 500
ixmolN m-z h-• [Seitzinger,
1988],exhibiting substantial
localvariabilitybutalso
showing thepotentialimportanceof denitrification.as
a nitrogensink.Despite the
largespatial
andtemporal
variability
of measured
denitrification
rates,estimates
of
annualdenitrification in verydiverseDanishcoastalareasexhibitedsurprisingly
moderatevariationarounda meanvalueof 400 !xmolN m-z d-1, corresponding to
20 kg N ha-• yr-• [Nielsenet al., 1994].
Nutrient massbalancesestablished
for wholemarineecosystems,
as thoseknown
fromfreshwaters[e.g.,Ahlgren,
1967;Andersen, 1971],aresubjectto considerable
errorbecause
of the dynamic waterexchange with adjacent
seasandfew figures
havebeenpublished[e.g.,Wulffet al., 1990;Kamp-Nielsen,
1992].Reportedmass
balancesanda numberof unpublishedDanishmassbalanceestimatesfor nutrients
in estuaries
(Table1) suggest
that steady-state
phosphorus
retention(Figure9.3a)
rangesfroma fewto almost
80%of totalphosphorus
input(input= loading
from
land+ importfromadjacent
seas,
whereimportisestimatedbased ontheannual
salt balanceof the coastal area and annual means of total nutrient concentrations
inthewaterimportedfromadjacent seas).Phosphorus retention
isusuallyless
than
20% of theinput(Figure
9.3a)[Billenet al., 1991],butin coastal
areaswithlong
residencetimes,suchas the BalticSea,phosphorus removalmayexceed
Borum 183
025
O2_0
0.0 252
o_ 0.05
o.oo
......... •..... i . i , i ,' ' [ , '

0.0 0.1 02 0.3 0.4 0.5
Phosphorusinput
(mmolm-2 d-1)
6
• E
' i . i 'r ...... I ........... ' ....
2 4 6 8
Nitrogen input
(mmolN m-2 d-1)
Figure9.3. Phosphorus(a) andnitrogen(b) retention

versus totalphosphorus andnitrogen
inputto thecoastalareaslistedin Table1. Onlycoastalareaspresumablyin steadystateare
included.¸- RingkebingFjord,differentyears;&: MariagerFjord,differentyears;O' other
areas.
[Wulffet al., 1990].Nitrogenretention(permanent burial+ denitrification)

ranges
from2 to 65% of nitrogeninput(input= loadingfromland+ nitrogenfixation+
atmospheric deposition+ importfromadjacent seas;Figure9.3b).Absolute nitro-
genretentionratesincrease with increasing
nitrogenloadingandvarybetween 0.25
and5 mmolN m-2 d-•, a rangecomparable to publishedratesof directlymeasured
denitrification
from estuarineareas[Hattori, 1983; Seitzinger,
184 9. ShallowWaters and Land/SeaBoundaries
ß 0o
0 50 100 150
Nitrogen concentration
(mmolN m-a)
Figure9.4. Nitrogenretention(sedimentburialplusdenitrification) versusaverageannual
nitrogenconcentrationin coastalareaslistedin Table 1. Mean valuesfor RingkobingFjord
(O) andMariagerFjord(&) areincludedin thedescribed relationship
(r2 = 0.54, n = 11).
Seitzinger[1988, 1990]reportedthat approximately 50% of the inorganicnitrogen

loadingfromlandis lostthroughdenitrification independent of loadingratesand
of hydraulicand bathymetricdifferencesamongestuaries.This observationhas
tendedto translateinto a general"50% of total nitrogenloading"-rulein the litera-
ture.Apartfrombeinghighlyunlikelydueto the markeddifferences in bathymetry
and flushing,the 50%-rulepredictsthat changes in nitrogenloadingdo not influ-
encepercentage losses despitemajorconcurrent changes in the biologicalstructure
of the shallowcoastalareas.The presentcompilationof datafalsitiesthe 50%-rule
(Figure9.3b).Nitrogenretentionrangesfrom 2 to 75% of total nitrogenimport
amongdifferentcoastalareas.In addition,tidalcoastalareaswith shortwaterresi-
dencetimeshavenegligible percentage
losses[Pejrupet al., 1993].
It isto beexpected
thatareas
subject
to veryhighfatesof nitrogen
loading
and/or
with shortwater residencetimesmust havelow percentagenitrogen retention.In
orderto bedenitrifiedor permanently
buried,importednitrogenneedsto beassimi-
latedandtransported downto thesediment. In areasof shortresidence times,only
a smallfractionof the importednitrogenmayreachthe sedimentand, therefore,
lossesrelativeto importsarelow. In slowlyflushedcoastalareas,importednitro-
genmay,however, passthesediment compartment severaltimes,andrelativelosses
exceedthe 50% [Wulff et al., 1990]. To accountfor differencesin flushing,nitro-
genlosses
mightbebetterestimated
fromaverage
watercolumn
concentrations
of
totalnitrogen(Figure9.4), However,substantial
residualvariationstillremainsun-
explainedand likelyreflectsdifferences
in bathymetry,physicalmixingpatterns
and biological
Borum 185
9.4.Response
to ReducedNutrientLoading
We haveno broadempiricalbasisto predicthownutrientlosses of coastalecosys-
temsrespond to reducedloading.As emphasized later,benthicplantpopulations,
andprobablyalsothe benthicinfauna,will benefitfromreduced nutrientloading
andtheirinfluenceon coastalnitrogencyclingmayaffectthe proportions of nitro-
genretentiondueto changes in denitrification
[CaffreyandKemp1990;Kristen-
sen,1988;Pelegriet al., 1994]. Benthicinfaunabioturbatesandmanyinvertebrate
species
constructandirrigateburrows.Duringventilation, oxygenandnitratefrom
the water column are transportedto the burrow lumenand stimulatemineraliza-
tion,nitrificationanddenitrificationwithinthesediment (chapter 6). Stimulatednitri-
ficationand alenitrification are primarilydue to the areal increasein the anoxic-
oxictransitionzoneand burrowdimensions and densityare, therefore,key factors
determining the effectsof infaunaon nitrogencycling[Aller, 1988; Pelegr•et al.,
1994].If, indeed,the densityof burrowinginvertebrates increases with reducednu-
trientloading,nitrogenlosses throughalenitrification
shouldbe enhanced dueto di-
rectreduction of nitratefromthewatercolumnor to anincrease of couplednitrifica-
tion-denitrification.Conversely, faunalstimulationof sedimentmineralization and
subsequent releaseof NH4+ and ureato thewatercolumnmayreducesediment bur-
ialof nitrogen and,hence, mayjustshiftthebalance between. thetwonitrogen sinks.
Stimulation of benthicmicroalgaeand macrophytes dueto improvedlight condi-
tionsfollowinglowernutrientloadingalsoaffectsthe dynamicsof the anoxic-oxic
transitionzonein marinesediments [Revsbech et al., 1981]. Duringbiomassbuild-
up,benthicmicroalgaeprovidea net oxygeninputto thesediment,andinducediel
changes in oxygenconcentrations leadingto rhythmicchangesin the depthposition
of the anoxic-oxicinterfaceand in alenitrificationrates[Revsbech et al., 1981; Ris-
gaard-Petersenet al., 1994]. The net effectof stimulated growthof benthicmicroal-
gae,however,seems to be a markedinhibitionof denitrification [Nielsenet al., 1994].
Oxygenreleasefromrootsof submerged macrophytes duringphotosynthesis stimu-
latesboth nitrificationand denitrification[Caffreyand Kemp, 1990], and, there-
fore,increased abundance of rootedmacrophytes shouldenhancenitrogenlosses.
With the possibleexceptionof benthicmicroalgae,the integratedeffectof biotic
components on alenitrificationsuggeststhat relativenitrogenlossesshouldincrease
with reducedloading.This predictionis, however,contradictory to the moregen-
eralviewpointthat nutrientutilizationandconservation aremoreefficientin mature,
nutrient-poor
ecosystems than in perturbed,nutrient-richecosystems[Odum,1971].
Thoughthe detailedstudieson regulationof denitrificationsuggestan increased
lossof available
nitrogen
withhigherabundance
of benthic
faunaandrootedmacro-
phytes,the net resultmay well turn out to be the oppositeat the ecosystem
level,
becauseinorganic nitrogenavailabilityisreducedasa responseto reduced
loading.
Forexample,extendeddepthpenetration of rootedmacrophytesmayimprovesedi-
mentoxygenconditionsbut a largerproportionof the total nitrogenpool within
theecosystem may alsobe boundwithinplantbiomass and consequentlybe less
availableto denitrifying
100 '
80
õ 50•
o 4o
z
20
23.9
.... ! .... i '............ i ' '' ' i ! i '

0 2 4 6 8
Nitrogeninput
(mmolN m-2 d-•)
Figure9.5. Percentage
nitrogenretentionversusnitrogeninput to the coastalareaslistedin
Table1. Relationships
for differentyearsin Ringkobing Fjord(dashed,
r2 = 0.389, p = 0.26)
andMarlagerFjord(solid,r2 - 0.579, p = 0.047) areshown.
There doesnot appearto be a clear relationshipbetweenthe proportionallossof

nitrogenand the nitrogeninput among differentcoastalecosystem[Billenet al.,
1991]. Year-to-yearvariationwithin two Danishestuariessuggests that the propor-
tion of nitrogenretentiondeclineswith reducednitrogen loading (Figure 9.5}.
However,sincea systematic changein loadingha• not occurredover severalyears
in theseestuariesand sincemajor changesin benthicflora and fauna often havere-
sponsetimeslongerthan oneyear,the observed changesin relativenitrogenlosses
may well reflecttransientresponsesand not tell us what happenson a longertime
scale.Reducednitrogenloadingto a shallowDanish embayment,KertingeNor,
causedthissystemto becomenet nitrogenexportingduringthe first two yearsafter
loadingwasreduced(chapter10), but a new steadystatehasnot yet beenreached.
The generaldeclinein phosphorus loadingto Danishestuarinesystems since1988
hasprovidedmoreinformationon systemsresponses to reducedP loading.How-
ever,as in the caseof nitrogendynamicsin KertingeNor, new steady-state mass
balanceshavenot yet beenestablished. In the largeand very shallow(meandepth:
!.9 m) RingkobingFjord, P loadingwas reducedby 50-60% from 1988 to 1991
[RingkobingAmtskommune,1992]. Export of phosphorusfrom the fjord to the
North Searemainedhigh,andthe ecosystem changedfrom beinga P-retainingto a
net P-exportingsystem[RingkobingAmtskommune,1992]. Though water resi-
dencetime in Ringk•bingFjord is short (0.3 yr) it is expectedto take more years
beforea new steady-stateP retentionhasbeenreached.
The shallowcoastalzonedoesindeedfunctionas an importantnutrientfilter and
we have gainedsubstantialknowledgeon the mechanisms of process
Borum 187
andcanalsoprovideroughestimates of nutrientretention.Our abilityto offer

moreaccurateestimates
of nutrientretentionandpredictchanges in retentionat
thesystems
level,however,stillneedsto be improved.We havefair ideason how,
for example,rootedmacrophytes influenceratesof denitrificationin the root zone
andcanalsodescribe thebasicinfluence of increased plantabundance on distribu-
tion and availabilityof nitrogenpoolson a localscale.The overalleffectof these
complexrelationships in termsof ecosystem nutrientretentioncan,however,hard-
ly be determined usinga mechanistic approach.Therefore,we needto put more
emphasis on massbalancestudiesin coastalecosystems of differentloading,hy-
draulicsandmorphometry and,moreover,followsystems responses to changes in
loading.Anotherattractivepossibility isto assessnutrientdynamics in manipulated
mesocosms. However,mesocosm experiments shouldbe designed andoperatedso
thattheysimulaterealisticchanges in the biologicalstructureof bothwatercolumn
andbenthiccommunities, i.e. they mustbe spatiallyandtemporallyscaledaccord-
ingto the sizesandgeneration timesof the importantbenthiccomponents andnot
onlyto thoseof theplankton.
9.s.CoastalPlantCommunities
andEutrophication
Increasednutrientrunoffhassevereconsequences for the ecologyof coastalwaters,
eventhoughthe coastalzoneis alreadyeutrophiccompared to manyotheraquatic
environments beforeanthropogenicloadingwasinitiated.Nutrient-enriched coastal
watersexhibitperiodsof hypoxiaor anoxiaand massmortalityamongbenthicin-
vertebratesand fish may occur.In the literature,theseeventsare frequentlyex-
plainedasa resultof increasedproduction of organicmatterwithintheecosystem
due to stimulationof the planktonicmicroalgaeas observedin eutrophied,deep
lakesandopenmarinewaters.Aquaticecologists oftenforget,however,that benth-
ic plantcommunities are importantcontributors to the autotrophicproductionin
pristinecoastalareasand,therefore,neglectbenthicplantresponses to nutrienten-
richment.
Benthicmacrophytes attaindensepopulations whichareasproductive assomeof

the mostproductive terrestrialplantcommunities [Westlake,1963;Mann, 1972;
McRoyand McMillan, 1977]. Sinceeutrophication seemsto inhibitratherthan
stimulatebenthicplant populations[Cambridgeet al., 1986; Sand-Jensen and
Borum,1991], nutrientenrichmentof shallowcoastalareasmaynot stimulatethe
totalprimaryproduction perunit areabutrathershiftthemainproductivity from
thebenthic to theplanktoniccommunity. Thefundamentalsof eutrophicationphe-
nomenain coastalwaterscanonlybeunderstood by including
theeffectson all au-
totrophiccomponents. Accordingly, thebasicquestions
are,howandwhydifferent
plantcomponents respond to nutrientenrichment andhow is the integrated re-
sponseof totalprimaryproduction to eutrophication?
The highproductivityin coastalwatersoriginatesfroma widevarietyof plants
rangingin sizefrom picoplanktonof lessthan I Izmin diameterto 30 m long
perennialmacroalgae.Pristineshallowwatersof temperateregionsare
byrootedseagrasses andbenthicmicroalgae on sediments

andby perennial
macro-
algaeon rocksandhardbottomsediments. If phytoplankton
biomasses
aremoder-
ate,lightpenetration
throughthewatercolumnishighandtheprimaryproduction
of benthicplantsmay exceedphytoplanktonproductionsubstantially in these
coastalecosystems[Mann, 1972;Walker et al., 1988].
A characteristicchangein the qualitativecomposition of plant communities is ob-
servedfollowingincreasednutrientinputsto embayments and estuaries[Sand-
JensenandBorum,1991].Phytoplankton biomasses
increase [Boynton et al., 1982;
Nixon andPilson,1983;Monbet,1992],theabundance of epiphyticmicroalgae on
seagrassesand on macroalgaeincreases[Borum,1985; Twilley et al., 1985; Cam-
bridgeet al., 1986], andephemeral macroalgaesuchas Ulva lactucabecomemore
abundantandmay accumulate in greatmasses [Harlin andThorne-Miller,1981;
Valielaet al., 1992;Sfrisoet al., 1992]. Concurrentwith thesechanges, the depth
penetration andabundance of seagrasses andperennialmacroalgae decline[Borum,
1983;Kautskyet al., 1986;Cambridgeet al., 1986]. Elementsof thissequential de-
velopment havebeenobserved frommanycoastalareasandhavealsobeenexperi-
mentallydocumented usingmesocosm manipulation[Twilleyet al., 1985;Fonget al.,
1993]. Accordingly, nutrientenrichmentof shallowcoastalwaterschanges the bal-
anceamongautotrophiccomponents from dominanceof perennialmacroalgae and
seagrassestowarddominance of ephemeralmacroalgae andpelagicmicroalgae.
9.6.Nutrient Requirements
and Supplies
It is not very clearhow the total nutrientconcentrationin the water columncon-
trols plant communitycomposition.Microalgaeand ephemeralmacroalgaehave
largesurfaceareato volume(SA:V) ratios,and are known to have higherratesof
nutrientuptakeper unit of biomassthan largeplantswith low SA:V ratios (cf.
chapter4). With high ratesof uptakeper biomass,yet at limiting nutrientcon-
centrations,
smallmicroalgae areusuallyassumed to bebetterableto meettheirnu-
trientrequirementsfor growththanplantswith low SA:Vratiosand,therefore, small
microalgaeshouldbecompetitively superiorto largerin oligotrophic
waters.Thisex-
planationseems intuitivelyplausibleandis supported by observationsof changesin
thesizecomposition of phytoplankton comrhunities in openwaters(cf.chapter4). It
doesnot explain,however,why large,slow-growing benthicplantswith low SA:V
ratiosdominatein shallowcoastalecosystems with low nutrientconcentrations.
Dominance of anygivenphototrophic organismimpliesthat it is ableto sustaina
constantand sufficiently high biomassby compensating lossesof nutrientsand
otherresources throughexploitationof theseresources
in theenvironment. If rela-
tive lossesare low, as theyare for largerplantswheregrazinglossesare much
lowerthanfor microalgae [Duarte,1995],gainscanbelow.Therefore, successful
resource acquisitioncannotbe evaluatedfrom absoluteratesof gain alone(e.g.
ratesof nutrientuptakeperbiomass) butmustbecompared to the demand of the
organism
anditsabilityto satisfy
thisdemand
throughvariousmechanisms
[Sand-
Jensenand Borum,
Borum 189
Specificgrowth rate, d-1

0.75 -
a
Growth rate
0.50
t -
0.25 -
Nitrogen content, % of dw.

100 -
b
Nmax
Nitrogen content
75-
N critical
50-
25-
Nitrogendemand,mg N (g dw.)-• d-•

40
c
30
Nitrogen demand
20
10
Phyto- Ulva C/ado- Cera- Chaeto- Fucus

plankton phora •ium morpha
Figure9.6. Maximum specificgrowthrates(a), nitrogencontentsof tissue(b), and nitrogen

demandsneededto sustainmaximumgrowth (c) of phytoplankton,Ulva lactuca,Clado-
phorasericea,Ceramiumrubrum, Chaetomorpha linurnand Fucusvesiculosus in Roskilde
Fjord,Denmark.Nitrogencontentis shownascriticalcontent(shadedbars)and maximum
observed
content(shaded
plusopenbars).DatafromPedersen
1Os ....
!:1 ./
• 10'•
•'• 10
3
:•.'0 iJM
NHa
+ • :,,,,
zlZ 10
2
I i' i
10 102 103 104 10s
N-requirements
(/JgN (g dw)-1 h-•)
Figure9.7. Relationships
betweenammoniumuptakeratesat differentexternalammonium
concentrations(numbers)and nitrogenrequirements duringmaximumgrowthof different
marinealgaerangingin sizefrom planktonicmicroalgae to largekelps(M. Hein andM.F.
Pedersen,unpublisheddata).Dashedline indicates
balancebetweenuptakeandrequirement.
The internalconcentration
of nutrients(e.g.total nitrogencontentper plant bio-
massunit)requiredto saturateplantgrowthvarieswith thegeneticallyfixedmaxi-
mumgrowthrate of the plant.Smallorganisms typicallyhavehigh growthrates
andrequirehighinternalnutrientconcentrations [Duarte,1995; SmithandKalff,
1982].According to Redfield,the average C:N:P molarratiofor planktonicalgae
is 106:16:1IRedfieldet al., 1965]. The slow-growing
macroalgae havemuchhigher
C:N:P ratios (ca. 800:49:1 [Duarte, 1992]) but somefast-growingmacroalgal
specieswith simplemorphology haveratioscloserto that of phytoplankton(e.g.
?orphyrasp.:137:23:1[Atkinson and Smith,1984]). Seagrasses
are slow-growing
andhaveanaverage C:N:Pratioof 474:24:10[Duarte,1990].
Pealersen
[1993]examined andcompared nitrogenacquisition
andgrowthof differ-
enttypesof marinealgaein a shallowcoastalarea.Themaximum,specific
growth
raterangedfrom0.065 d-• in theperennialbrownalga,Pucusvesiculosus, to 0.66
d-• for a naturalphytoplanktoncommunity, whilegrowthratesof fourephemeral
macroalgae werebetween theseextremes (Figure9.6). Thecriticalnitrogencontent
(sensu Hanisak[1979]),belowwhichalgalgrowthis nutrient-limited,variedfive-
foldand,together withthedifferences
in growthrates,resulted in a 50-foldhigher
nitrogendemand perunitbiomass andtimefor phytoplankton thanfor Fucusvesi-
culosus (Figure
9.6).Thus,smallplantsrequirea muchhighernutrientsupplyrate
thanlarge,slow-growing plantsto sustainmaximumgrowth.
Thebiomass-specific
nutrientuptakeof microalgaeismuchfasterthanthatof, for
example,seagrasses
andkelps[e.g.,Duarte,1995],although
ananalysis of therela-
tionship
betweenmaximum inorganic
nitrogenuptakeandSA:Vratiosshowed that
perennial
macroalgaewithlowSA:Vactually havethesameor evenlargeruptake
capacity
perunitof surface
areacompared to microalgae[Heinet al., 1995].
Borum 191
Nitrogenreserves,mg N (g dw.)-•
6
Nitrogen reserves
4
0 • •
Storage capacity, d
20-
b
Storage capacity
15-
10-
Phyto- Ulva Clado- Cera- Chaeto- Fucus

plankton phora mium morpha
Figure9.8. Nitrogenreserves (N .... minusNcritical;

a) andnitrogenstoragecapacity(thetime
nitrogenreserves can sustainmaximumgrowth;b) of phytoplankton, Ulva lactuca,Clado-
phorasericea,Ceramiumrubrum, Chaetomorpha linum and Fucusvesiculosusin Roskilde
Fjord,Denmark. Data from Pedersen[1993].
entuptakemay well befastin smallalgae,but thehighnutrientrequirements may

actuallymean,that smallalgaeneedhigherexternalnutrientconcentrations to sat-
isfyrequirements for growththanslow-growing macroalgae.
Thisisobservedwhen
ammonium uptake,estimated for differentexternalammonium concentrations
and
differentalgalspecies,isrelatedto algalnitrogenrequirementsat maximumgrowth
(Figure9.7). The low nitrogenrequirements of slow-growing,
perennialmacroalgae
can be satisfiedat external ammonia concentrationsof about 0.5 IxM, while the
fast-growing
Ulva lactucarequiresan externalconcentration
of 2 IxM to achieve
maximumgrowth.Thoughmicroalgae andephemeralmacroalgae havehigherbio-
mass-specific
nutrientuptake,largerplantsareindeedmorecapableof supporting
maximum growththroughnutrientuptakeunderlowexternalconcentrations.
Plantnutrientrequirements can,alternatively,
be at leasttemporarily
met by ex-
ploitinginternalstoresof nutrients[Chapman andCraigie,1977]andit hasbeen
reportedthat fast-growing algaeare ableto buildup largernutrientstores
slow-growing
perennial
algae[e.g.,Lobbanetal., 1985].ThoughPedersen
[1993])
foundthat maximumnitrogencontenttendedto be directlyrelatedto the maxi-
mumgrowthrate (Figure9.6), the criticalnitrogencontentexhibiteda similarrela-
tionship
and,therefore,
thecapacity
to accumulate
nitrogen
reserves
wasnotvery
differentamongthe six plant speciesof widelydifferentform and sizeexamined
(Figure9.8). Because
nitrogenrequirements per unit timevaried50-fold,storage
capacity,expressedas the time nutrientreservescan sustainmaximumgrowth,
wasmuchlongerfor slow-growing
thanfor fast-growing
plants.Slow-growing
plantsare, therefore,ableto bufferlong-term(e.g. seasonal)fluctuationsin exter-
nal nitrogenavailability,whilenitrogenstoresin planktonicmicroalgae canonly
sustainmaximumgrowthfor aboutone day withoutexternalnitrogensupplies
(Figure9.8).
Someperennialplants,suchaslaminarians andseagrasses, growby continuouslyre-
newingtheirphotosynthetic tissues.
Thisgrowthformallowsan efficientrecyclingof
nutrientswithin the plant. Remobilizationof nutrientsin old tissuesand subse-
quentreallocation to youngtissuesfurtherreducethe demandfor nutrientuptake
from the environment[Patriquin,1972; Borumet al., 1989]. For a shallow-water
Danisheelgrass population,Pealersenand Borum[1993] estimatedthat internalre-
cyclingcouldaccountfor 27% of annualnitrogenrequirementsand for 50%, or
more,of the requirementsat thetime of maximumeelgrass growthin May-June.
Consequently, slow-growingmarine macrophytes seemwell adaptedto coastal
areasof low inorganicnutrientavailability.Despitetheir low SA:V ratios,theyare
bettercapableof meetingnutrientrequirements becauseof adequateuptakemech-
anisms,exploitationof internalstores,and,for someplant species,internalnutrient
recycling.Hence,largemacrophytes experience shorterperiodsof nutrient-limited
growththansmall,fast-growing plants.Smallplants,suchasplanktonicalgae,depend
more on the immediatenutrientconcentrations in the water columnand requirea
constantandrich nutrientsupplyto sustaina highbiomassand production.
9.7.Regulationof PlantBiomassand PrimaryProduction

Phytoplanktoncommunitiesare regulatedby light, nutrientsand by grazingand
otherlossprocesses
(cf.chapter
4). Accordingto theanalysis above,phytoplankton
biomass
andgrowthshould
beclosely
coupled
•othetotalnutrient
concentration
in
the water column.Empiricaland experimental documentation from fresh-water
lakesshowsthat phytoplanktonbiomassincreases with increasingphosphorus
loading[Vollenweider, 1968;Schindler,1978].In marineareas,empiricalrelation-
shipshavebeenestablished betweenphytoplanktonbiomassand total nitrogen
concentration[Nixon and Pilson,1983; Monbet, 1992] and phytoplanktonbio-
masshasalsobeenexperimentally stimulatedby nitrogenenrichmentof meso-
cosms[Twilleyet al., 1985;Nixon et al., 1986].In Danishcoastalwaters,phyto-
planktonbiomasscorrelates
wellwith concentrations
of totalnitrogen(corrected
for nitrogen
boundin phytoplankton
to eliminate
autocorrelation)
in thewatercol-
umnthroughout thegrowthseason,andin particularduringsummerwhen
Borum 193
1000
0.641 July
,,• 100
0
,., ,•' 10
0 ""
n I
100 10;0 10000

Total N
I,ugN I't)
Figure9.9. Phytoplanktonbiomassversusconcentrations of total nitrogen(not including
nitrogen boundin phytoplankton,
whichwassubtracted byassuming a C:chlorophyll
weight
ratioof 40 anda molarC:N ratio of 6.6 IRedfieldet al., 1963])duringsummer(July).Data
fromdifferentDanishcoastalareas[Sand-Jensen et al., 1994a].
genis most depleted[Sand-Jensen et al., 1994a] (Figure9.9). Only duringearly

springdoesphytoplanktonbiomasscorrelatebetterwith total phosphorus than
with total nitrogen.Concurrentwith the stimulationof phytoplanktonbiomassby
eutrophication the total amountof suspended particlesincreasesand both factors
contributesignificantlyto increaselight attenuationin the water columnand re-
ducelightpenetrationto the benthicplantcommunities [Sand-Jensenet al., 1994a].
The relationshipsbetweennitrogenloadingor nitrogenconcentrationand phyto-
planktonbiomassare, however,subjectto largevariabilityamongsystems [Nixon
andPilson,1983; Monbet, 1992]. Thisvariabilitymayoriginatefrom differencesin
rnorphometry and physicalenergyinput.In estuarieswith a largetidal amplitude,
phytoplankton biomassis significantly
lowerthan in low-tidalestuaries whensys-
temsof equalnitrogenloadingor concentrations are compared[Monbet,1992].
Tidalinfluenceon the amountof suspended materialand,thereby,on lightclimate
in the water columnmay be one explanationfor this difference[Cloern,1987;
Nienhuis,1992; Monbet, 1992], but wind-drivenor tidal breakdownof stratifica-
tionis anotherimportantfeature[Cloern,1984]. Phytoplankton biomass develop-
ment,for example,reactspromptlyto short-term changes in stratification
of the
shallowestuary,RoskildeFjord[Sand-Jensen et al., 1994b].Phytoplankton abun-
danceincreases duringperiodsof stratification
but declines duringmixing,prob-
ablybecausethesuspension-feedingmussels comeintocontactwiththeentirephy-
toplanktonpopulationin the mixedwater column[Sand-Jensen et al., 1994b].
Duringstratification,
the benthoscanonlyfeedon phytoplankton populations in
the enclosedbottom waters.Benthicmusselsor ascidiansmay have a sufficiently
highfiltrationcapacityto controlphytoplankton
biomass
in shallowcoastal
194 9. Shallow Waters and Land/Sea Boundaries
[Officeret al., 1982;chapter10, thisvol.],butwatercolumnmixingandstratifica-

tion eventsdetermine when,andif, thiscapacitycanbe expressed.
Nutrient enrichmentof shallow embaymentsstimulatesgrowth of ephemeral
macroalgae with simplemorphology andhighgrowthrates(e.g.Ulva [Sfrisoet al.,
1992],Cladophora [Birchet al., 1981], Chaetomorpha [Nienhuis,1983]),resulting
in massaccumulations of floatingmacroalgae in enclosed,
nutrient-enriched
waters
[Valielaet al., 1992;Geertz-Hansen et al., 1993].A rathercomplexseriesof inter-
actingenvironmental factorssuchaslight,temperature, nutrientconcentrationand
herbivore grazingcontrolthesuccess of individualmacroalgal species
and,hence,
species
dominance
andsuccession
[Geertz-Hansen
et al., 1993;Fonget al., 1993;
Borumet al., 1994].In addition,macroalgalbiomassaccumulationis greatlyinflu-
encedby estuarinemorphometry andhydrodynamics,andour abilityto predictthe
dynamics
of ephemeral
macroalgal
communities
asa function
of nutrientloading
in
shallowareasremainslimited.However,thegeneralpatternis that the biomass
of
ephemeralmacroalgaeincreases
in shallowareas,but decreases
in deeper
waters
dueto increased
light attenuation
from suspendedmaterialand phytoplankton
[Sand-Jensen
andBorum,1991;McComb'and Humphties,1992].
Sinceslow-growing, perennialmacrophytes seemcapableof meeting theirnutrient
requirements evenat lownutrientconcentrations in thewatercolumn,nutrienten-
richment maynot significantlystimulate macrophyte growth.Lightis a moreim-
portantregulatingfactor,andlightattenuation seems to controlthedepthpenetra-
tion andarealcoverof perennialmacroalgae and seagrasses[Borum,1983;Kaut-
skyet al., 1986;Duarte,1991].Because totalnutrientconcentration, phytoplank-
tonbiomass, andlightattenuation in thewatercolumncorrelate, thelowerdepth
limitof perennialmacrophytes is an indirectfunctionof thetotalnutrientconcen-
tration(Figure9.10).In coastalDanishareaswithconcentrations of totalnitrogen
exceeding 1 mgN 1-• duringthe growthseason, eelgrass,Zosteramarina,is con-
finedto theupper5 m of thelittoralzonewhilein areas withconcentrations below
0.5 mgN 1-aeelgrass maypenetrate to 10m depth(Figure 9.10).Thelatterdepth
rangecorresponds
to theprevailing
conditions
foundin theouterpartof Danish
estuaries
andopenwaters[Ostenfeld,
1908]beforethe onsetof majoranthropo-
genicnutrient
inputto thesea.In upperestuarineareas,
suchasthecentral basins
of Limfjorden,
thedepthlimitof eelgrasswasca.5 rn [Ostenfeld,
1908]andthe
mediandepthlimitis nowreduced to 2.5 m [Olesen,
1993].According to Figure
9.10,thischangein depthlimitsuggests
thatthemeanconcentration
of totalnitro-
genbetween springandfallhasincreasedfrom0.4mgN 1-• atthebeginning ofthis
centuryto 0.8 mgN 1-• in the1980s.
Deepgrowthandextensive arealcoverof eelgrass
andperennial
macroalgae
are
important features
for coastal
ecosystems
because benthic
plantcommunities
sta-
bilizethesediment,contribute
substantially
to ecosystem
production,
andprovide
surfaces
andshelterto a richfauna[Mann, 1972;Thayeret al., 1975;Sand-Jensen
andBorum,1991].Assuming
that the reduction
in depthpenetration
of macro-
phytes
isfullyreversible,
should
nutrient
loading
bereduced,
theestablished
empiri-
calrelationship
between
totalnutrientconcentration
andeelgrass
depthlimits
Borum 195
lOO
Eelgrass depth limit
r• - o.547
a - 0.755
• n-
oo o
oo o oo o -
o
o
o.1
100 1000 10000
Total N
{jJgN 1-1)
Figure9.10. Relationship
betweenmeanconcentration of totalnitrogenanddepthlimit of
eelgrass(Zosteramarina) colonization.Data from differentDanishcoastalareas[Sand-
Jensenet al., 1994a].
750
ß----. o
o o
::3 ,..... 31.4
'o o
o T
L •"
500 0
, .--,.
õ 'E
oo
• • 250
• Lp•
/ •'-: © ß16.8
•
o
o 2 4 6 8 !o
N-loading
(molN rn-2
Figure9.11. Annualphytoplankton productionversusnitrogenloadingof differentcoastal
areas.
Data from(O) Boyntonet al. [1982],(A)the MERL mesocosms [Nixonet al., 1986],
and(e) fromareaslistedin Figure9.12 andfromvariousDanishcounties. Thecurverepre-
sents
thefunction:
y = 244 + 175 log(x)fittedbyleastsquaresregression,
r = 0.599,n = 51.
resents
a powerfulpredictive tool for administrators
managing coastaleutrophica-
tionproblems. However,therelationship doesnot tell usanythingaboutthetime
patternof the re-establishment
of formerrich eelgrass beds.Suchpredictionsrely
ondetailed knowledge of colonizationcapacity
of theplants.Basedonee!grass seed
production, patch formationand mortality,and subsequent vegetativepatch
growth,OlesenandSand-Jensen [1994]estimated thetimecourseof eelgrass
recol-
onizationin Limfjordento beseveraldecades followingreductionof nutrientload-
ing.Thisestimate may,however, beconservative because muchfaster
196 9. ShallowWatersandLand/Sea
Boundaries
Primary production
(g C m-• y-•)
0 200 400 600 800

I I I I
Bothnian Bay {1)
San Fransisco Bay NB (2)
San Fransisco Bay SB (2)
Bothnian Sea {1)
Ems-Dollard (3)
Baltic Proper (1)
Oostershelde {3)
Westershelde (3) •:'>.'....
'-.-.•:!i:.•
:...
Hempstead Bay (4)
Niantic River {4) ':•'.,
:"--"..
.....
-' ß-3'!;]
Kattegat {5) i, I
Wadden Sea (3)
Grays Harbor (6) .............
•.:...••••:...:.:•j
Chariestown River ,•......•..•
.:.v...........
Grevelingen(3)
Jordan Cove
Alewife Cove (4)
Narraganset Bay (4)
Barataria Bay (7)
RoskildeBredning ":'::"-
:-"..-..
' f.'-•i J
Chesapeake Bay MD (9) ':,
.'-:.•',
"::'.
ß' '.:.':•L!•I J
Frederiksv. Br. {10)
Flax Pond {4)
Veerse Meer (3) i•!:."":'"---""-•.."•.,.•)'.-'.•!
-- 1
Puget Sound (11) !
Roskilde Vig {10) I
Rottnest Island {12)
Great South Bay {13)
Chesapeake Bay VG (14) •"••••'
.........................
"•=•:.1 I
St. Margaret's Bay (15)
Bissel Cove {4)
Figure 9.12. Total primary productionin 31 differentcoastalmarine areas(references in

parentheses).Shadedbars:benthicproduction;open bars:pelagicproduction.References:
(1) Elmgren[1984], (2) Jassbyet al. [1993], (3) Nienhuis[1992], (4) Welshet al. [1982],
Richardsonand Christoffersen[1991], Gran•li & Sundbiick[1986], (6) Thom [1984], (7}
Dayetal.[1973],
(8)Borum
eral.[1990],(9)Kemp'et
al.[1983],(10)Winter
etal.[1975],
(11) Jensenet al. [1990], (12) Walker et al. [1988], (13) Livelyet al. [1983], (14) Murray
Wetzel [1987], (15) Mann [1972].
of deep-watereelgrasspopulationswasobservedin LakeGrevelingen,whereplant
areal coverwas more than doubledwithin a 10-yearperiod after an improvement
of lightpenetration[Verhagenand Nienhuis,1983].
Justlike phytoplanktonbiomassincreases with increasingnutrientloadingsodoes
phytoplanktonproduction[Boyntonet al., 1982]. Estimatesof annualpelagicpro-
ductionfrom differentcoastalareasand from the MERL mesocosmexperiments
[Nixon et al., 1986] showthat nitrogenloadingstimulates phytoplankton produc-
tion (Figure9.11). However,the increasein productionlevelsoff at high loading
ratesandmaximumratesof productionrarelyexceed500 g C m-2 yr-1. Thispat-
tern,firstly,reflects
a gradualdecrease
in community
turnover(growthrate)
Borum 197
800
600
31.4
400
16.8
200
I ..... i........ I ......

2
N-loading
(toolN m-2 y-l)
Figure9.13. Total annualprimaryproductionversusnitrogenloadingof differentcoastal

areas.Data fromthoseareaslistedin Figure9.12 wheretheN-loadingis known[Borumand
Sand-Jensen,
in press].
increasingnutrient concentration,and, secondly,a declinein the efficiencyby

whichnutrientsare utilizedby phytoplanktoncommunities. Apparently,the con-
trollingroleof nutrientsfor annualphytoplankton productiongraduallydiminishes
with total nutrientconcentrationand is replacedby otherconstraining
factorssuch
aslightclimateand lossprocesses.
Thoughphytoplankton productionof coastalareasis stimulatedby nutrientenrich-
ment,total primaryproduction(includingcontributions from benthicplant com-
munities}may not be enhanced,becausethe increasein phytoplanktonbiomass
reduces depthpenetrationand arealcoverof benthicplantpopulations, i.e. the eco-
systemis light-limited.Perennialkelpsand seagrass meadowsmay attain annual
production ratesof 1,000 g C m--•or more[M,•nn, 1972;McRoy andMcMillan,
1977;Pedersen and Borum,1993]. Commonly,the integratedorganiccarbonpro-
ductionof entireestuarineor coastalecosystems rangesbetween250 and 500 g C
m-2 yr-• (Figure9.12) [Nixonet al., 1986]and,apparently, total nutrientconcen-
trationhaslittle impacton systems production[BorumandSand-Jensen, in press]
(Figure9.13). Pristinecoastalareasmay exhibithighratesof annualproduction
originating primarilyfromdensemacrophyte bedsandwith low contributions by
phytoplankton. In regionssubjectto highanthropogenic loading,phytoplankton
production mayreachthe 500 g C m-2 yr-• but contributions from benthicplants
arethennegligible.
Hence,themostimportant effectof nutrientenrichmenton pri-
maryproducers in shallowcoastalareasis to inducequalitativechanges in plant
communitycomposition andprimaryproduction [BorumandSand-Jensen, in press].
Integrated
primaryproduction doesnot seemto be affectedto a greatextent,
thoughan enhancement of primaryproduction mayoccurin deepercoastalareas
thatarephytoplanktondominated underunperturbed conditions (cf.chapter
9.8.Influence
on OxygenDynamics
andHigherTrophicLevels
If totalorganic
carbonproduction
of coastal
systems
remains
ratherunaffected
by
nutrientenrichment, whatis thenthe influence of eutrophication on oxygendyna-
micsandhighertrophiclevelswithin the coastalzone?Thereseemto be no obvious
reasonsfor expectingmajorchanges in net systemproductionwith increased nutri-
ent loadingof coastalareas.Nixon and Pilson[1984] reportedthat Narragansett
Bayexhibited netexportof organicmatter,butcoastal areasaremostoftenslightly
heterotrophicat thesystemslevel[e.g.,Smithet al., 1991] indicatingthat autochto-
nouslyproducedorganicmatter is primarily mineralizedwithin the coastalzone
itselfirrespective
of nutrientloading.Therefore,annualoxygenconsumption and
releaseshouldbe independent of anthropogenicloading,and we can hypothesize
that observedchangesin oxygendynamicsmustoriginatefrom increasedspatial
and temporalseparationof oxygenreleaseand consumption ratherthan increased
rates.The changesin plant compositiondescribedabovecould, theoretically,in-
duce increasedseparation.However, the complexrelationshipsbetweenplant
dominanceand oxygendynamicsin shallowcoastalwatersneedto be examined
more thoroughly.
Likewise,the influenceof coastalzonenutrientenrichmenton faunalcomposition
andsecondary productionseemsto be rathercomplex(seechapter8). Thereareex-
amples,especially from deeperphytoplankton dominatedareas,suggesting thatthe
biomassof benthicanimalsincreases with increasingnutrientloading(cf. chapter
8), but, in general,shallowcoastalwaterscannotbe shownto respondto eutrophi-
cationby producinga largerbiomassof animals[Nixon et al., 1986]. Nixon et al.
[1986]suggestedthatthelackof observed responsescanbepartlyexplainedbyin-
adequateharvestingandmeasuring techniques.
Alternatively,however,the lackof
responsecouldreflectthat total organiccarbonproductionmaynot be enhanced.
Hence,eutrophicationeffectson highertrophiclevelsmaypredominantly influence
species
composition of animalpopulations(cf. chapter10) ratherthan total sec-
ondaryproduction.
Acknowledgments. A largenumberof peoplehavecontributed or helpedin variouswaysto
obtainthe dataand form the discussion of thischapter.I am in particulargratefulto the
othermembers of our research groupat the Freshwater-Biological
Laboratory,K. Sand-
Jensen,O. Geertz-Hansen, M. F. Pedersen,
O. Pedersen,M. Hein,andB.Kjoller,for provid-
ingtheories,data,discussions,
constructivecriticismandtechnicalsupport.I alsothankM.
Johnson,andrepresentatives from the counties of Aarhus,Nordjylland,ViborgandRing-
kzbingfor lettingmeutilizeunpublisheddatain thisreview.
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Andersen,
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10
CaseStudy:KertingeNor
HansUlrikRiisgfird,
Carsten
Jiirgensen
andFrede•stergaardAndersen
Introduction
Thiscasestudydescribes
investigations
conducted in 1991-1992in KertingeNor, a
shallowcoveon the northernpart of Fyn, Denmark(Figure10.1). By the end of
1989, annualdischargesof nitrogen(N) and phosphorus (P) to the fjord system
KertingeNor/KertemindeFjord werereducedby 45% and 78%, respectively, as
domesticsewagewasno longerled into the system.
The significantreductionin the externalnutrientloadmadethe fjord systemsuit-
ablefor studyinghow nutrientreductionaffectedits recovbry from eutrophication.
KertingeNor combinesexceptionally clearwater,dominance of macrophytes (eel-
grass,Zosteramarina,andthick matsof filamentous algae,Chaetomorpha linum),
highdensitiesof smalljellyfish(Aureliaaurita)and a densepopulationof benthic
ascidians(Ciona intestinalis).This madethe covean interestingareato studythe
dynamicsof the biologicalstructurein an eutrophicecosystem in whichnutrient
fluxesandsuspension-feeding organisms play a decisive
role.
Thischapterpresentsthe main resultsof concurrentprojectson hydrography,nu-
trients,macrophytes,
plankton,jellyfish,and ascidians
and synthesizes
the interac-
tionsbetweennutrientdynamicsandthe biologicalstructure.
0.2. Water Exchange

The fjord systemconsistingof KertemindeFjord andKertingeNor (Figure10.1)
coversan area of 8.5 km2 and has a meanwater depthof 2 m and a maximum
depthof 8 m. Thefjordhasa sillat itsmouthto theopensea(GreatBelt).Thedis-
chargeoverthesillisforcedby a diurnaltidewithanaverage
amplitude
of ca.20 cm.
Thetidegivesriseto maximum
discharges
at thefjordentrance
of 100-200m3s-1.

Union
206 10.CaseStudy:
Kertinge
Nor
6.8 >,2
ngeNor
240 PE
lkm
,o ,
Figure10.1. Investigation
area,KertingeNor/KertemindeFjord, Denmark.Water depths(m)
are shown.Samplingstationsand amountsof discharged sewage(PE = personequivalents)
to the fjord-system
in 1989 (beforesewagereduction)are indicated.
The fresh-waterinputof 0-0.05 m3 s-• is negligible

with respectto the waterex-
changeof thefjordsystem.The salinityin thecentralpart of the systemvariestypi-
callybetween14 and22 psuoverthe year.The temperature rangesbetween0 and
22øC [Larsenet al., 1994].
The waterexchange of the fjord systemis governedby density-driven
circulation.
The salinityin the GreatBeltoutsidethe fjordvariesasa resultof changing
Riisg•rd,JQrgensen
andAndersen 207
Kertinge Nor Great Belt
Lower salinity in the Great Belt than in Kertinge Nor

, Higher salinity in the Great Belt than in Kertinge Nor
m3/s•
decreasingsalinity
increasingsalinity
L II , I, , I,,
ß
..
....
. . . .•: -. •: . •-.•
ß .'
. .
1 i I i i I i 1 1 I 1
J F M A M J J A S O N D J F M A M J J A S O N D
1991 1992
Figure10.2.Upperpartof figure:Illustration
of waterexchange inKertingeNor(KN).Low
salinity
in theGreatBelt(GB}compared to KN gives riseto a density-driven
circulation
that
flowsintothefjordsystem at thesurfaceandoutat thebottom(counter-clockwise). High
salinity
in GBcompared to KN gives riseto a density-drivencirculation
thatflowsintothe
fjordsystem at thebottomandoutat thesurface (clockwise).Lowerpartof figure: Calcu-
latedflowratesof thedensity-drivenexchange of waterbetween theKertinge Nor andthe
GreatBelt.Thelightbarsindicate flowsituations withdecreasing salinity
in theGreatBelt,
i.e.counter-clockwise
circulation,
andthedarkbarsindicateincreasing
salinity,i.e. clock-
wisecirculation.FromJiJrgensen
[1995].
situations
(cf.chapter3).OutflowofwaterfromtheBalticSeagivessalinities
down
to10psu,whereas inflowtotheBalticSeagives
salinities
upto 27 psuintheupper
layeroftheGreatBelt.Because saline
waterismoredensethanfreshwater,thesali-
nityvariationscauselongitudinal
density
variations
fromtheinnerpartofthefjord
systemto themouth.Asa consequence of longitudinal
density
gradient,density-
drivenverticalcirculationoccurs.Whentidal forcingflushesdensewater overthe
sillit will flowdownbelowthefjordwaterandgiveriseto a density-driven
208 10. CaseStudy:KertingeNor
tion systemwithinthe entirefjord system.When,on the otherhand,lighterwater

is forcedinto the fjord the circulationis in the oppositedirection.On an annual
time scalethe two circulationdirectionshaveequal probability.An approximate
residencetime of water in the centralareasof the systemis betweenoneweek anda
fewmonths,with an average of approximately 1.5 month[Jiirgensen, 1995].How-
ever,because of the dynamics of the exchangeprocesses,
the "residence time" is not
a veryusefulconcept in thisfjordsystem.A qualitativeillustrationof theflow rate
and the directionof the exchangeof water is givenin Figure10.2.
10.3.
NitrogenandPhosphorus
Balance
A generaltransportpatternof nutrientsthroughthe fjord systemwasobtained
fromstudieson totalnitrogen(tot-N) andtotalphosphorus(tot-P).The transport
of thenutrients
wasdescribedby meansof thenumerical,hydrodynamic modelsys-
tem "MIKE11". The modelsolvesthe equations for conservationof massandmo-
mentumand describes the advectiveand the dispersivetransportof matter[DHI,
1990]. The modelwas calibratedand verifiedby salinity[Jiirgensen,
1995]. The
transportof totalphosphorusthroughthe fjord entrancewasmeasured directly
andwasin closeagreement with the simulations.
The dailynutrientinputsfrompointsources,
diffusesources
and the atmosphere
were calculated based on direct measurements.The nutrient fluxes from the sedi-
mentto thepelagicwerein the modeldetermined as the difference
betweenthe
computed andthemeasured nutrientconcentrations.
Thenutrientfluxesfromthe
sedimentestimatedby the model were confirmedby laboratoryincubations
(Christensen
eta!., 1994]. The incubations
showedthe sametemporalvariations
andthesameorderof magnitude asthenumerical
simulations.
Afterthesewage
discharge
to the fjordsystem
hadbeenstopped
by the endof
1989,theannualnutrientloadwasreduced
by 45% N and78% P. Consequently,
the releaseof nutrientsfrom the sediment(internalload) becamemuch more im-
portantfor thetotalnutrientbalance
of thefjordsystem.
Duringthesummer
per-
iodsin 1991 and1992 thesediment
wasthedominatingsourcefor bothtot-N and
tot-P. The nutrientfluxescalculatedfrom the model,however,alsoshowedperiods
with low nutrientuptakeby the sediment(Figure10.3).
In 1991,theannualrelease of P fromthesediment was3.3 timeshigherthanthe
totalexternalinputfromlandandair,whiletheannualnetrelease of N wasonly
0.4 timesthe externalload (Table10.1). In 1992, whenthe nutrient-assimilating
matof filamentousalgaedisappeared(seelater),thesediment release
was3.4 times
and1.9 timeshigherfor P andN, respectively, thantheexternalinput.Theex-
tremelyhighreleaseof N andP observed duringlateJune1992(Figure10.3)coin-
cidedwith thedecayof thethickfilamentous
algalmat.
Themodelalsoshowed
a netexportof bothN andP fromthefjordto theopensea
(Figure
10.3).Apartfromshortperiods
withminorimports
inthespring
andinthe
autumn,tot-N wasexported
overthe entiretwo-yearperiod.For tot-P,a
Riisgfird,
Jtirgensen
andAndersen 209
TABLE 10.1. Balance of nitrogen(N) andphosphorus (P) in Kertinge

Nor/Kerteminde
Fjordin 199I and1992.All figuresarein metrictonnes.
FromChristensen et al. [1994].
1991 1992
N P N P
Inputfromlandandprecipitation 35 1.6 40 1.6

Net releasefrom sediment 13 5.4 75 5.5
Net exportto the GreatBelt 48 7 115 7.1
KgJday
5O0
Kg/d•y
lOO
d F M A M d d A $ O N D d F M A M d d A $ O N D
1991 1992
Fig10.3.Threemaintransports
of nitrogen(N, upperpart)andphosphorus
(P, lowerpart)
in KertingeNor.
Externalsource:Nutrientloadsfrom pointsources (wastewater),diffusesources (agricul-
ture),andatmosphericdeposition(rain).
internalsource:
Nutrientexchanges between waterandsediment, positivevaluesfor release
fromsediment andnegative valuesfor uptake.
Boundary transport:
Nutrienttransports overthe boundarybetween Kertinge Nor andthe
GreatBelt.Positivevaluesareimportsintothe KertingeNor, negativevaluesare exports
to the Great Belt.
The two linesfor internalsourcesand boundarytransportsgivethe upperand lower esti-
matesof the simulations.
FromJi•rgensen
importwasobserved
in thewinter,whereas
therewasa pronounced
exportduring
the restof the period.The net exportof P from the fjord systemto the GreatBelt
was approximately7 tonnesin both 1991 and 1992, whereasthe export of N was
48 tonnesin 1991 (a "normalyear" with extensivegrowthof benthicplants)and
115 tonnesin 1992. The lossof N throughdenitrificationin the fjord systemwas
estimated to 26 tonnesN in 1992.The totallossof P andN fromthe system may
be comparedto the mobilepoolsof thesenutrientsin the sediment,whichwerees-
timated to be 30-52 tonnes of P and 150-225 tonnes of N.
10.4. Nutrient Concentrations
The concentration of tot-N variedthroughoutthe seasonfrom 25 to 150 •mol 1-1,

with characteristicpeaksin concentration duringwinter and late summer(Figure
10.4a). The winter peaksreflectfresh-waterrunoff from the surroundingarea,
which is the major externalinput of inorganicnitrogen(inorg-N) to the system.
The late summerpeaksweredueto sedimentreleaseof inorg-N whichwasrapidly
assimilatedby fife phytoplankton..The fastassimilationresultedin verylow inorg-
N concentrations duringthe summermonths(Figure10.4a). The tot-N concentra-
tion wassignificantly higherduring1992compared to thepreceding years.
The concentration
of tot-Pvariedbetween0.5 and 12 •mol 1-1,with the lowestval-
uesin December-March andthe highestin May-October(Figure10.4b).The same
patternwasobserved for inorg-Pwith concentrations
of upto 6 i.tmol1-• duringthe
summerdueto internalloading.
The spatialandtemporalvariationin inorg-Pandtot-Pin 1991 wasfollowedat 13
stationsin the fjord systemand comparedwith a stationin the Great Belt [M•h-
lenbergandJiirgensen, 1994]. Longitudinalgradientsof inorg-Pwith the lowest
concentrations in the innerpart of the fjord systemindicatedthat KertingeNor
actedasa sinkfor inorg-Pduringlate Februaryto mid April, probablydueto assi-
milationby the macrophytes. From late May throughOctoberthe oppositegrad-
ientwasfound,indicatingthat KertingeNor actedasa sourcefor inorg-Pandtot-
P. In Novemberand Decemberthe concentration of inorg-Pagaindecreased from
the GreatBelttowardKertingeNor implicating an inwardflux of inorg-P,prob-
ably drivenby adsorption and precipitation processesin the sediment.
The mea-
suredgradients arein closeagreement withconcentrations computedfromthetot-
P release simulations.
0.5. Macrophytes
In thesouthern
partof Kertinge
Nor (St.1 onFigure10.1),a densematof filamen-
tousgreenalgae(primarilyChaetomorpha linum)covered the sedimentsurface
with maximumbiomasses of 65 g d.wt m-2in August1991 [Larsenet al., 1994].In
1992, the biomass
of thesefilamentous algaepeakedalreadyin earlyJune(80
Riisgfird,
JQrgensen
andAndersen 211
Totalnitrogen
150 o St .1
= St.2
100
pmoVI
Inorganicnitrogen
75 o St.!
= St.2
25
0 ,
1984 1985 1986 1987 1988 1989 1990 1991 1992
I•møl/I
iTotal
phosphorus
15
10
o St.1
St.2
•mo!/I , , , ,
Inorganic
phosphorus
10- o St.!
8- = St.2
6-
4-
2-
0
!984 !985 1986 1987 1988 1989 1990 1991 1992
pg/!Chlorophyll
-a
100 o St.1 c
= St.2
75
1984 1985 1986 1987 1988 1989 1990 1991 1992
rng
C/rn2/d
tPdmary
production
4000
o St.!
.2
2000
1984 1985 1986 1987 !988 1989 1990 1991 1992
Figure10.4.Nitrogen(a),phosphorus (b),chlorophyll-a
(c)andphytoplanktonprimarypro-
duction(d) in Kertinge
Nor in 1984, 1987and1989-1992.FromRiisgfirdet al.
d.wt m-2),afterwhichtimetheystarteddying.No plantswerefoundin Augustand

throughouttherestof 1992.
Profilemeasurements throughthe mat in May 1992 (while the algaewere still
growingwell) showedhigh 02 concentrations in the upperhalf of the mat but
anoxicconditionsin the lowerpart [Christensen et al., 1994]. Due to the anoxic
conditionshighNH4• andPO43-concentrations werefoundat the sediment surface
underneath themat. The concentration of thesenutrientsdecreased up throughthe
mat because of assimilation
by the algae.The steepnutrientgradientthusindicated
that the mat wasveryefficientas a filter for the nutrientsreleasedfrom the sedi-
ment. However,the nutrientsbound in the algal biomasswere releasedrather
quicklyasthealgaediedanddecayedin 1992.
The bottomflora of the northernpart of KertingeNor (St. 2 on Figure 10.1) was
dominatedby rootedmacrophytes, mainlyeelgrass,
but filamentousalgaewerealso
foundbetweenthe shootsof eelgrass. It wasexpectedthat the eelgrassbedswould
increase andthatthe coverage of filamentousalgaecoulddecrease asa consequence
of reducednutrientloadingandlowerconcentrations in the water becauseeelgrass
is ableto satisfyits nutrientdemandfrom the sedimentthroughroot uptake.
A studyon the influenceof eelgrass and filamentousalgaeon the cyclingof P re-
vealedthat the P releasefrom sedimentsunder filamentousalgae was 2.5 times
higherthanfromthe sediment coveredwith eelgrass[Christensen et al., 1994]. The
releaseof P from Chaetomorpha detrituswas also significantlyhigherthan from
eelgrassdetritus(decayconstants:0.090 and 0.029 d-1, respectively).Theseresults
indicatethat increases
in the eelgrass
bedsat the expenseof filamentousalgaewill
havea positiveeffecton the recoveryof the fjord systembecausenutrientswill be
lessavailablefor thephytoplankton duringthegrowthseason.
0.6. PlanktonDynamics
The biomassof phytoplankton,expressed as the water columnconcentrationof
chlorophyll-a,
wasnormallylow duringmostyears(Figure10.4c).Intensivesam-
plingduringFebruaryandMarchsuggested thattherewasa shortspringmaximum
of chlorophyll-a
(Figure10.4c).Apartfr.om thispeakin earlyspring,chlorophyll-a
neverexceeded 10 •g 1-1during1991, whichwassimilarto the preceding years
(Figure10.4c).The chlorophyll-aconcentration
was alsolow duringthe first five
monthsof 1992, but in Julychlorophyll-a
increased
markedlywith concentrations
reaching120 •g 1-• in October.The phytoplanktonprimaryproductionalsoin-
creasedmarkedlyduringthesummerof 1992andtheratesweresignificantly high-
er thanin thepreceding"normal"years(Figure10.4D}.
Thepelagicbiomass levelsandthesuccessions
of planktonspecies
weresimilardur-
ingthe springperiodsof 1991and 1992, butthe developments wereverydifferent
duringthetwo summerandautumnperiods(Figure10.5).In 1991 the auto-and
heterotrophic biomasses werelow anddominated by diatomsanddinophyceans as
well asciliates,rotifersandepibenthic
harpacticoids
(Table10.2). In 1992 the
Riisgfird,Ji•rgensen
andAndersen 213
Autotrophicplankton
[•] Diatoms
• Other
autotrophs
Heterotrophicplankton
25o • Mesozooplankton
• Cilliates
2oo • Dinofiaoeaates
150
10o
0 ,
J F M A M J J A S O N D J F M A M J J A S 0 N D
1991 1992
Figure10.5. Biomassesof autotrophicand heterotrophicplanktonin KertingeNor in 1991

and 1992. Basedon data from Riisgfirdet al. [1995].
TABLE 10.2. Mean heterotrophicbiomasses (!xg C 1-]) on

stations1 and 2 in KertingeNor (seeFigure10.1) duringthe
summerperiod(May-September)1991 and 1992. From Riis-
grimet al. [1995].
1991 1992
St. 1 St. 2 St. 1 St. 2
Dinoflagellates <0.1 10.3 54.6 87.5

Ciliates 6.3 1.4 12.4 11.8
Copepods* 2.5 i).4 1.8 2.7
Rotifers <0.1 <0.1 1.0 4.2
Spionidlarvae 0.6 0.1 1.1 0.7
Bivalve larvae <0.1 0.1 0.2 0.1
Total 9.4 12.3 81 107
mainly
massof phytoplanktonwasexceptionallyhigh.In the beginning of the periodthe

autotrophicbiomasswas dominatedby the diatom,Skeletonetna costatum,fol-
lowedlaterby anotherdiatom,Stephanodiscushantzschii.The diatombloomwas
succeededby a bloomof smallcyanobacteria
whichlasteduntiltheendof Novem-
ber.The heterotrophic
biomass wasdominated by ciliatesin the beginning of the
period,butwaslatersucceeded by heterotrophic
dinoflagellatesappearing in very
highbiomasses.
0.7. Jellyfish(Aureliaaurita)
The predationimpactby the jellyfish,Aureliaaurita,on zooplankton in Kertinge
Nor wasstudiedduring1991and 1992.The waterprocessing capacity(clearance)
asa functionof medusasizeandwatertemperature wasmeasured in thelaboratory
usingrotifers(Brachionus
plicatilis)or copepods (Acartiatonsa)aspreyorganisms.
From thesedata and from measurements of medusadensityand sizedistribution
in the KertingeNor theclearance capacities of the jellyfishpopulationwereesti-
mated[Olesenet a1.,,1994;Olesen,1995].
ß
In 1992thefirstyoungmedusae (ephyrae)of thenewgenerationof Aureliaaurita

appearedin February.Duringthe followingmonths,numbersincreased dramati-
callyanda maximumdensity of about300 individuals
m-3wasmeasured in April.
FromAprilandthroughout therestof theseason,thedensity
of medusaedecreased
(Figure10.6}.
Thegrowthpatternof Aureliaauritawasdifferentin 1991compared
with 1992.
During1991thegrowthwaspooruntilearlyAugust, whena pronounced
increase
in bothumbrelladiameterand specificgrowthratewasobserved(Figure10.6).A
maximumin the umbrelladiameterwasobservedin earlySeptember1991, wherea
meanof 54 mmwasmeasured. The instantaneousspecific
growthrate (/z) reached
a maximum
of 0.07d-• inlateAugust
1991.in 1992a maximum
meanumbrella
diameter
of only37 mmwasmeasured
in lateJune,wherealsoa maximum
of/z =
0.09 d-1 was found.
Smallmedusae
(umbrella
diameter
= 4 mm)collected
in KertingeNor showed
rapid
growth
in thelaboratory
whenrotifers
wereoffered
in theconcentration
range
of
130-13,000rotifers1-•. Duringa 10-dayincubation
period,theumbrelladiameter
increasedfromapproximately 4 to 9 mmat preyconcentrations
higherthan700
rotifers
1-1.Thiscorresponded to a dry-weight
increase
from0.1 to 0.9mg.At the
lowestconcentrationof rotifers (130 ind. 1-1)the diameterincreasedto 6.5 mm,
corresponding
to an increase
of 0.36 mg.A maximum instantaneous'
specific
growthrateof 0.22d-1wasobtainedat a preydensity
of approximately
400ro-
tifers1-1,corresponding
to a growthof 60 •g C 1-•.
Themaximalspecific
growthrateof 0.22d-• foundin thelaboratory
experiments
maybecompared to themaximalgrowthrateof 0.09 d-• observed in Kertinge
Nor wherethemeancarbonconcentration of thezooplankton wasonly6.5 and
4.7IzgC 1-• in 1991and1992,respectively.
It canthusbeconcluded
that
Riisgfird,
JQrgensen
and Andersen 21.5
Density,ind. m
35O
300
a
250
200
• 1991
150
100
50
0 ,
Diameter, mm
70-
60- b
50-
40-
30-
20-
10-
0 i i i' ' i i i I I I
Specificgrowthrate, d-•
0.10 -
0.08- c
0.06 -
0.04 -
0.02 -
0-
-0.02
-0.04 ..... . , ,
Figure10.6. Aureliaaurita.a: Population densityof jellyfishin KertingeNor in 1991 and

1992.b: Mean diameterof jellyfish;representatives.d.is shownfor two dates.c: Instanta-
neousspecificgrowthrateof jellyfish.[FromOlesenet al., 1994.]
auritain KertingeNor wasseverely

food-limited
andneverexploitedits potential
for growth.
Theestimated populationclearance
capacities
showed thatAureliaauritawasable
to filtera watervolumecorresponding
to several
timesthe wholewatervolumeof
Kertinge Nor dailyduringAugustandSeptember 1991,aswell asin June1992.
Furthermore,
the meanresidencetime (t 1/2)for a zooplanktonorganismwas < 5
daysfrom springto autumn.Thispredation impactexplainsthelow biomass of
zooplankton
duringpartof thezooplankton
growth
216 10.CaseStudy:
Kertinge
Nor
TABLE10.3. Cionaintestinalis.
Population
density(95% confidence
limitsare givenin
parentheses),
individualtotal dry weightand populationfiltrationrate at differenttimesof
theyearin Kertinge
Nor. Thetheoretical
meanresidence time(t•/2)of an algalcellisshown
aswellasthequotient(Q) of totalpopulation
filtrationpotential
of ascidians
covering 2.81
km2to thewholewatervolume
in Kertinge
Nor (5.48km2withanaverage
depthof 2 m).
BasedonPetersen
andRiisgfird
[1992];revised
according
to Riisg•trd
et al. [1995].
Time Tempe- Density, Weight, Population
filtration t •/2 Q
rature, rate
øC ind.m-2 mgind.-• I h-1 m-2 x104m3h-1 h d-•
March 1991 6.4 76 (45-129) 57 30 8.4 46 0.2

May 1991 !3.5 20 (13-31) 169 38 11 37 0.2
Sep.1991 12.4 237 (195-287) 56 191 54 7 1.2
Dec. 1991 3.5 277 (207-372) 49 47 13 30 0.3
April 1992 8.6 139 (113-170) 90 104 29 13 0.6
June1992 20.2 33 (25-44) 295 139 39 10 0.9
0.8. Ascidians(Ciona intestinalis)

In orderto establish
thepotentialgrazingimpactof Cionaintestinalis
in Kertinge
Nor the populationdensitiesand the individualfiltrationratesas a functionof size
of the ascidians,
watertemperatureand algalcell concentration
were determined
[Petersenand Riisg•rd,1992].
The maximumfiltrationrate of Cionaintestinalis (Fmax,ml min-•) expressed asa
functionof the total bodydry weight(W, g) at a giventemperature (T, øC)wasde-
scribedas Fmax = (8.3T- 6.9)Wø'68.Thus,from populationestimates and water
temperature in KertingeNor, populationfiltrationcouldbe computed(Table10.3).
It is seenthat populationfiltrationvariedconsiderably duringthe year.In Septem-
ber 1991 the populationcouldcleara volumeof watercorresponding to the total
volumeof KertingeNor per day, while in May 1991 it could only clear0.2 times
the total volumeper day. To illustratethe potentialgrazingimpactof the total C.
intestinalispopulationon phytoplanktonit was calculatedthat the theoretical
meanresidence time (t•/2)for algalcellsin a fully mixedwater column(2 m3)var-
ied between7 and46 h, dependingon timeof year (Table10.3).
The filtrationcapacityof the Cionapopulationin KertingeNor variedbothduring
the yearand betweenyearsas a resultof variationin populationdensityand indi-
vidual temperature-and size-dependent filtration rates.In general,the filtration
capacitywas low in winter, due to low temperatures, and in mid-summer,dueto
low populationbiomass, while it was high in late summerand earlyfall, where
temperatures andbiomass werebothhigh.
No dataon Cionapopulationdensitywereobtainedfrom July to December!992
dueto highwaterturbidity,but the filtrationrate wasdecreased
8-10 fold dueto
overloadingof the feedingsystemby high in situ concentrationsof the
Riisgfird,
Jiirgensen
andAndersen 217
Stephanodiscushantzschii,
whichdominated thephytoplankton inJuly1992.Thus,
reduced
filtrationratesdiminished
thegrazingimpactby C. intestinalis
in thesum-
mer and fall of 1992.
0.9.Biological
Structure
andNutrientDynamics
Thebiologicalstructure
of the KertingeNor ecosystemin 1991is summarized in
Figure10.7.Thewatercolumnwasextremely clearwhichallowedsufficient
light
penetration
to thebottomwherea significant benthic
primaryproductionof fila-
mentousalgaeandeelgrass tookplace.Thedense algalmatwasimportantforthe
control of the nutrient flux from the sediment into the water column. Below the
algalmatthe sedimentwasblackandsulfidicdueto anoxicconditions andwithout
livinganimals.On thealgalmat,however,
a largenumber(3000-4000ind.m-2)of
small(<3 mm)cockles, Cardiumsp.,wereobserved clingingto thealgalfilaments
justabovetheanoxicbottom.Furthermore, smallsnails,Littorinasp.(4000-5000
ind.m-2)andHydrobiasp.(2000-3000ind.m-2),wereseentogetherwithmussels,
Mytilusedulis(60-80 ind.m-2;<20 mmshelllength).Thus,undertheprevailing
conditions
all thebenthicanimalshadmovedupabove'theanoxiczone.
Duringsummer1991,the waterprocessing capacity of the jellyfishpopulationwas
veryhigh,with a maximumrate obtainedin earlySeptember wherethe jellyfish
populationcoulddaily process
a watervolumecorresponding to ca.13 timesthe
wholewater volumeof KertingeNor. This suggests that Aureliaauritacouldwell
controlzooplanktonin KertingeNor duringsummerandfall. Laboratory experi-
mentsprovedthat themedusae werefood-limitedat in situzooplankton concentra-
tions.Moreover, A. aurita was apparentlygrowingin excessof its food source,as
zooplankton densities in the water columnof KertingeNor duringthe day (Table
10.2)couldnot explainthe observed growthof A. aurita.It hasmorerecentlybeen
observed,however,that the densityof harpacticoids in the water columnduring
nightcan exceedthe densityduringthe day by a factorof 20 (unpublished results)
and night-swimming harpacticoidsmay thereforehave beenan importantfood
sourcefor the jellyfishin KertingeNor in 1991.
In 1991 the filter-feedingCionaintestinalis exerteda highgrazingpressure on phy-
toplankton,which partly explainedthe low observedphytoplanktonbiomass.In
particular,duringlate summerand fall, the Cionapopulationreacheddensitiesof
ca.250 ind. m-2. Duringfall, the densepopulation of C. intestinalis
hadthepoten-
tial capacityto filter the total watervolumeof KertingeNor 0.2-1.2 timesdaily,
andthe meanresidence time of an algalcellin thewatercolumn(t 1/2)wasonly7 h
in September 1991 (Table10.3). Frompreviousdataand observations this situa-
tionseemed to havebeenthe prevailingfor the structureand dynamics of Kertinge
Nor for the decadepreceding1992.
During1991 andthe previous"normal"yearsthewatercolumnof KertingeNor
wasvery clear and the chlorophyll-aconcentrations
were low throughoutthe
growthseason(Figure10.4c).At thesametime,a highbiomassof the
218 10:CaseStudy:
Kertinge
Nor
•phytoplankton
ß .
ß ,
Aurelia aurita"
ß .
ß .
4• epibenthic
harpacticoids .,, ß .
sticklebacks
% Ciona intestinalis
Zostera
harpacticoids ,
.
'Chaetomorpha
microbenthic harpacticoids
diatoms
Figure 10.7. Biologicalstructurein 1991 ("normal year") in KertingeNor. Three food-

chainswereidentified:1) phytoplankton--> ascidians(Ciona intestinalis);2) epiphyticdia-
toms-->epibenthic harpacticoids-->jellyfish(Aureliaaurita)+ sticklebacks;
3) macrophytes
-->detritus-->decomposing microorganisms. From Riisgirdet al. [1995].
macroalga,Chaetomorpha tinurn,was recordedon the bottomthroughoutthe year

(matsup to 40 cm thick duringthe summer).The productionof filamentousalgae
was limitedby the availabilityof N, and the algalmat thereforecontrolledthe re-
leaseof inorganicN fromthe sediment[Christensen et al., 1994]. This "normal"
situationexistedfor KertingeNor until June 1992. A long periodof calm
Riisgfird,
Jiirgensen
andAndersen 219
weatherwith highinsolationbeganin the middleof May andpersisted for 8-9

weeks.Thiscausedhighprimaryproduction in thefilamentous algalmatwhichled
to theformationof largeoxygenbubbles that caused partsof thewholealgalmat
to float up from the sedimentto the water surface[Christensen et al., 1994].
Floatingin thewater,thefilamentous algalmatcouldnolongeractasan absorbing
filterfor the nutrientflux fromthe underlyinganoxicsediment andlargeamounts
of nutrients were releasedto the water column.
Thephytoplankton populationimmediatelyresponded to theelevated nutrientcon-

centrations. Within a week, the phytoplanktonbiomassincreased80-fold in areas
wherethe algalmat wasmore or lessseparated from the sedimentsurface[Christ-
ensenet al., 1994]. DuringJune1992,thephytoplankton biomass increased almost
exponentially whichreducedthe lightpenetration depthintothewaterto only30
cm.The massiveshadingby phytoplankton causeda total collapseof the remaining
benthicalgal mats and from AugustChaetomorpha linum had disappeared from
KertingeNor. The growthof eelgrass alsodecreased. This enableda highflux of
nutrientsfrom the sediment(Figure10.3) andextremelyhighchlorophyll-a concen-
trationswere measuredin October(Figure10.4c).
DuringJune1992theparentgeneration of Cionaintestinalisdiedoff dueto itsnat-
urallife cycle.The filtrationcapacityof the ascidian populationwas,thus,low by
the end of Juneand beginningof July becauseonly newly settledspecimenwere
present. The declinein filtrationcapacityby the endof June1992 wascoincident
with the increasein phytoplankton biomass. In July algalcell concentrationsex-
ceeded optimumconcentrations for filtrationand C. intestinalis becamesaturated
andsubsequently reduced its filtrationrateto a minimumof its potentialcapacity
[Petersen and Riisgfird,1992]. (2.intestinalis thereforedid not controlphytoplank-
ton duringthe summerand fall of 1992 in KertingeNor.
Themarkedchange in primaryproducers
hadnosignificant
influenceonthejellyfish
populationwhichoccurred in comparably
highdensities
duringboth1991and1992.
Also,thewaterprocessing rateswereapproximately
equalduringbothyearsandthe
highpredation rateprevented themesozooplankton
fromincreasing in numbersasa
responseto theincreasedphytoplankton
biomass
(Table10.2).Thus,evenduringex-
tremesituationswithchlorophyll-aconcentrations
of upto 120 t•g14,theAure!ia
auritapopulation
hadanimportant regulating
impact
onthezooplanktondensity.
It maybeconcluded thatKertinge
Nor until1992wasan inherently
unstable
eu-
trophicecosystemin whichinteractions
betweensuspension-feeding
organisms
and
mobilizationof nutrientsfrom the sedimentdeterminedthe dynamicsof the bio-
logical
structure.
In thepresent
casestudytheinstability
of thesystem blurredall
possible
short-term
effects
causedbythesignificant
reductionin nutrient
discharge
by the end of 1989.
Theestimated
exportratesof nutrients
(Table10.1)maybeexpected
to leadto a
markedreductionof the internalnutrientload within the next 5-10 years,though
the exhaustionratesfor nutrientsfrom the sedimentpools (enhanced by former
sewage
disposal)
willdecrease
exponentially
overtheyears.
Theexhaustion
ofnutri-
entsmayalsobedependent
onthefrequency
of "abnormalyears".
Possible
220 10.CaseStudy:
Kertinge
Nor
ationof thebiological
structurein Kertinge
Nor duringthisreestablishing
periodre-
mainsunknown at thepresent,
andnoreliableinformation existsabouttheformer,
unpollutedfjordsystem.Thefirstenvironmental
examination of thesystem
wasmade
in 1974bythecountyof Fyn,butat thattimethesystem wasalreadyeutrophic.
Followingthepresent casestudy,thecountyof Fynhasbeenresponsible for moni-
toringthedevelopment in KertingeNor. Sofar, it canbestatedthatthephytoplank-
tonbiomass waslowduringboth1993and1994("normalyears"withclearwater;
seeFigure10.4).Thefilamentous algalmatwasveryweaklydeveloped, whereas the
eelgrass
hadfavorable growthconditions. AlsotheCionaintestinalis population
was
dense.Furthermore, a normalbrackish-water infaunahaddeveloped extensively.
At
thepresenttimeit is unknownwhethertheKertingeNor ecosystem, possibly
dueto
the radicalinterruptionsof the "normal"biological structure
andmassive nutrient
lossin 1992,hasstarteda development
towarda new,morestablecondition.
References
Christensen,
P. B., F. Mohlenberg, D. Krause-Jensen,
H. $. Jensen,
S. Rysgaard,P. Clausen,
O. Sortkjaer,
L. Schliiter,S. B.Josefsen,
C. Jiirgensen,
F. O. Andersen, J. Thomassen,M. S.
Thomsen, and L. P. Nielsen,Nutrienttransportand biologicalinteractions in Kertinge
Nor/Kerteminde Fjord (in Danish),128 pp., Havforskningfra Miljostyrelsen,
43, Danish
Environmental ProtectionAgency,Copenhagen, 1994.
DHI, MIKE11, A microcomputer basedmodellingsystemfor riversand channels,Technical
Reference, DanishHydraulicInstitute,Horsholm,Denmark,1990.
Jiirgensen, C. Modellingof nutrientreleasefrom the sedimentin a tidal inlet,KertingeNor,
Funen,Denmark, Ophelia, 42, 163-178, 1995.
Larsen,G. R., C. Jiirgensen, P. B. Christensen, N.J. Olesen,J. K. Petersen, J. N. Jensen,E.
Mortensen,O. Sortkjaer, P. Andersen,KertingeNor/KertemindeFjord- statusand devel-
opment(in Danish),Havforskning fra Mil/oityrelsen,44, 132 pp., DanishEnvironmental
Protection Agency,Copenhagen, 1994.
Mohlenberg,F., and C. Jiirgensen, Spatialand temporalvariationin phosphorus in a small
marineinlet after cut-offof sewerdischarges, in Changesin Fluxesin Estuaries:Impli-
cationsfrom Scienceto Management,editedby K. Dyer, and B. Orth, pp. 215-218, Olsen
& Olsen,Fredensborg, Denmark.1994.
Olesen,N.J., K. Frandsen,and H. U. Riisgfird,Populationdynamics,growthand energetics
of jellyfish(Aureliaaurita) in a shallowfjord, Mar. Ecol. Prog.Ser., 105, 9-18, 1994.
Olesen,N.J., Clearancepotentialof the jellyfishAureliaaurita, and predationimpacton
zooplankton in a shallowcove,Mar. Ecol.Prog.Ser.,/24, 63-72, 1995.
Petersen,J. K., andH. U. Riisgfird,Filtrationcapacityof the ascidianCionaintestinalis
and
its grazingimpactin a shallowfjord,Mar. Ecol. Prog.Ser.,88, 9-17, 1992. (seealso
Erratum:Mar. Ecol.Prog.Ser.,108, 204).
Riisgfird,
H. U., I. Clausen,
F. Mohlenberg, J. K. Petersen,
N.J. Olesen,P. B. Christensen,
M.
M. Moller, and P. Andersen, Filter-feeding animals,planktondynamics and biological
structure in KertingeNor (in Danish),Havforskning fra Mil/ostyrelsen,
45, 75 pp.,Danish
Environmental ProtectionAgency,Copenhagen, 1994.
Riisgfird,H. U., P. B. Christensen, N.J. Olesen,J. K. Petersen, M. M. Moller, andP.
Andersen, Biologicalstructurein a shallowcove(Kertinge Nor, Denmark)- Controlby
benthicnutrient fluxes and suspension-feeding ascidiansand jellyfish, Ophelia, 41,
329-344,
11
The Use of Models

in EutrophicationStudies
Andr•W. VisserandLarsKamp-Nielsen
Introduction
Modelsare differentthingsto differentpeople.Theyareessential to themannerin

whichwe ashumans viewtheworld;a concept recognized
by Greekphilosophers
3000yearsago.Theyare alsofundamental to scientific
understanding.
The essen-
tialcharacter of a modelisto simplifyrealityin somewaywiththeexpress purpose
of highlighting or accentuatingcertainrelationshipsandprocesses.Modelscanbe
conceptual and expressed verbally(dialogues and discourses
of renaissancesci-
ence).They can be physicalor a diagram;scaledup or downto bringthemto a
humandimension (coloredballsconnected by strawsto represent
molecules,
points
of lightprojectedontothe ceilingof a darkenedauditoriumto represent the celes-
tial sphere).In modernscientificusage,the termmodelhasgenerallycometo refer
to a mathematicaldescription.
Mathematicalmodelshavefor a longtime beenan integralpart of scientificprac-
ticein the hard sciences
suchas physicsand chemistryand in their applicationin
engineering.Their unquestionablesuccessliesprimarilyin the limitednumberof
universallaws and constantswhich appearto governmost of the interactionsof
matterand energy.In contrast,ecosystems are extremelycomplexand the princi-
plesbehindtheir behaviorremainlargelyunknown.Nevertheless, the descriptive
andpredictivepowersof mathematical modelshaveattractedbiologists and eco-
logicalresearchersoverthe pastdecades.
The rangeof thesemodelshascovereda broadspectrum of reality[Plattet al.,
1981]from reductionist:
examiningspecific
processes isolatedfromexternalinflu-
ences,a 'mathematical
lab experiment'
if youwill to holistic:
attemptingto coveras
manyinterconnectedprocesses
asisfeasiblein simulating a naturalsystem.Models

Coastaland Estuarine Studies, Volume 52, Pages221-242
Union
222 11. The Useof Modelsin EutrophicationStudies
canalsobecategorized bythetypeof question theyseekto address [Franks,1995].

They can be theoreticalin that they qualitativelyexplorethe interactionof well-
foundedformulations in an innovativemannerleadingto new testablehypotheses.
They canbeheuristic,formulatedandparameterized with regardto a well-defined
setof observations
to gaininsightintothedynamics of a particularsystem. Finally,
theycanbepredictive,extrapolatinga heuristicmodelbeyondits samplerange.In
practice,modelshavecharacteristics of all threecategories.They havea theoretical
basiswhich,togetherwith observations, is usedto parameterize a heuristicmodel,
the predictivepowerof which is usedto gaugethe success of the underlyingcon-
ceptsand formulation.
Lastly,modelscan be typified by their scope.Theseincludeempiricalmodels,
sometimescalled black box models,which seekto describean observeddata setas
a mathematical functionusuallythrougha statisticalfittingproceduredisregarding
any possiblecausalprocesses. Suchmodelsare usefulfor identifyingtrends,astest
beds againstwhich conceptualmodelscan be formulated (i.e. causalprocesses
mightbeinferredfromthe mathematical functionderived},and canbe usedaspre-
dictivemodelsfor 'well-behaved'systems. In the caseof fresh-watersystems,an
empiricalapproach[Vollenweider,1968, 1976] hasprovidedthe successful basis
for predictingand managingeutrophication. Unfortunatelyvery few marinesys-
temsare'well-behaved' andempiricalhodelscanfail dramaticallywhenappliedby
the unwary.Dynamicmodelson the otherhandseekto build up the behaviorof a
systemfromwell-defined subprocesses
and their supposed interrelation.If empiri-
cal modelstry to describehow thingschange,dynamicmodelsinvestigate whythey
change.While dynamicmodelsare difficultto implement,they do havea clear
advantage that in principletheycanrespondto changinginput and forcingcondi-
tions.Theirpredictivecapabilityis moresoundlybasedon naturalprocesses than
that of empiricalmodels.In oceanography, the unqualifiedterm 'model'is most
oftenusedto referto a dynamicratherthanan empiricaldescription.
In whichever mannermodelsareclassified, theyareartifices,designedbypeoplefor
a specificpurpose.Theinherentconflictbetween mathematical tractabilityandreal-
ismleadsto compromises betweensimplicity andcomplexity depending on thepur-
posefor whichthemodelis used.Scientists shouldusethemodelin thehypotheti-
co-deductive processcharacterizingthe'stronginterference'scientific
method[Platt,
1964].Thisis neededin ecosystem research sinceobserved phenomena canoftenbe
explained bydifferent
theoriesandbecaused bydifferentmechanisms [Schefferand
Beets,1994],a consequence of the usualnon-linearity
of thesesystems. In thiscon-
text, modelscan be usedto get an overviewof complexstructures and for testing
and/orfalsifying functional
relationships.Consequently, the modelis equallyvalu-
ableif it actsunexpectedly
anda hypothesis canbe rejectedaswhenit behaves as
expected.
Forsuchstrategicpurposes,
models
shouldbeassimpleaspossibleto be
penetrable
by analytictechniques;
modelresultsshouldnot be asconfounding
as
direct observation.
Oncemodelshavebeenverifiedandvalidatedtheycanserveaspredictive
toolsfor
decision
makersandmanagers, providedthatthepredictions
madearewithin
Visserand Kamp-Nielsen 223
rangeof validation.
Themodel,forthesetacticalpurposes,
ismostcredible
whenit
actsasexpected.
It isgenerallyaccepted thatstudyof eutrophication in limnicsystemsiswellin ad-
vance of thatin marinesystems. Thisispartlybecause eutrophication
in lakeswas
recognized earlier,butalsobecause it wassimpler to quantify.Lakesaremorpho-
logically
well-defined systemswithmeasurable in-andoutflows. Moreimportantly,
theflushing ratesof lakesaregenerally muchslower thantheirmixingratessothat
it canbe readilyassumed that similarconditions applythroughout. Whilemuch
canbe learnedby marinemanagers andscientistsfromthe expertise accrued by
limnologistsovertheyears,it should bestressedthata directtransfer
isinappropri-
ate;themarineenvironment presents a newsetof challenges.Marinesystems have
muchfasterflushingrates,oftensimilarto theirmixingratesaswell asthe time
scaleoverwhichpertinent biologicalprocessesoperate. Whileflushingratescanbe
made'artificially'slowerby considering a largerarea,thismakesthe system less
welldefined.It is a characteristic
of marinesystems thatfluctuations
dominateand
meanconditions areseldomencountered. Interpretationof observations
is compli-
cated:doesa changein someparameterindicatea changein the system,or is it a
transientpulsefromoutside.In marinesystems, thedetection
of a trendrequires
yearsof data,thedetection
of a change
in trendrequires
decades.
Giventhe poor quantificationof eutrophication (as definedby Nixon [1995]; a
changein trophicstate)and its effectsin marinesystems,few eutrophication model-
ing studiesas suchhavebeencarriedout. However,thereis a growingbodyof
work investigatingecosystem modelsin marineenvironments. Thesemodelscon-
tain, asan integralpart, descriptionsof couplednutrientand biologicalprocesses.
Further,it is becomingapparentthat physicalprocesses are particularlyimportant
in determiningkey characteristics of variousmarinesystems.This realizationhas
led to the development of dynamicphysical-biological-chemical ecosystem models
[Legendreand Demers,1984]. Sinceit is likely that the potentialof suchmodels
will becomeincreasingly exploitedin the near futurein investigatingeutrophica-
tion, we will devotesometime in what followsto discuss their formulation.
Thepurposeof thischapteris to presentsomekeyconcepts andmethods for eutro-
phicationstudiesin marinesystems whichare usefulor mightproveso in the near
future.In this we choosea few examplesfrom lakes,estuaries,fjordsand coastal
seasasillustrations.We do not intendthis asan exhaustivereviewof the subject.
Model Construction
Oncea problemor hypothesis has beenidentifiedthroughmanagement/policy

needsor scientificinterests,
the construction
of a mathematical
modelcanproceed.
Generallythisis alongwell-proven lines[Nihoul,1976]asillustrated
Figure11.1.
Thefirststepis a demarcation
of thesystem
intophysical
space;
whereandwhen
and statevariables;what. For instance,physicalspacemay representa lake, estu-
ary,fjordor coastalseaovera seasonal
cycle.In eutrophication
studies,
at
Scientific
paradigm
fJ availible
•
[problem
definition
data"
]
]•-• demarcation
]J
i L resøurce•
•//• requirement
J Lsøphisticatiøn
J.,J
I
I /r ( flow
diagram,
equations,
computer
algorithm
]
/
[ verification
]-•revision
,1
nsitivi•
analysis
valid•ation
Figure11.1. Outline of modelconstruction.
someof the statevariableswould be nutrients(N, P, and others).However, there

areothervariableswhichmaybe modeledand potentiallyplay an importantrolein
nutrientconcentrationsin a particularsystem,e.g. phytoplankton,zooplankton,
detritusetc.Demarcationof the systemis in recognitionthat a modelcannotbe all-
encompassing and encapsulates
the compromise
that mustbe struckbetweensim-
plicityandreality.
The secondstepis giventhis demarcation,.
how are externalinfluenceson the sys-
temtreated.Theseincludeboundaryconditions, initialconditionsandforcingfunc-
tions.In mathematicaltermsthis ensuresthat the modelis well posed.Boundary
conditions describe how state variables are influenced from outside the model do-
main, for instancethe flux of nutrientssuppliedto an estuaryby river inflow.
Likewise,initial conditionsdeterminethe pre-existingstateof the systemand the
importanceof its historydependence. Thoseinfluencesdeemedimportantto the
systembut which cannotbe dynamicallymodeledmust be imposedas external
forcingfunctions. An examplehereis theannualvariationof light intensitygovern-
ing photosynthesis in mid-latitudecoastal
Finally,mathematical
equations
areusedto express
thedynamic
interactions
of the
statevariables.In this context,it is oftenusefulto sketchthe interactionbetween
dynamic statevariables
in a flowdiagram, e.g.Figure11.6illustrates
theflowof ni-
trogenbetweenstatevariables in an idealizedfjordmodel.A fundamental law ex-
ploitedin eutrophication,
indeedin ecological modelingstudiesisthatof massbal-
ance.If C is the concentrationof somenutrientin a systemthenthe timerateof
changeof C is givenby:
dC/dt = Fin- Font+ R (1)
whereFinandFontarethe fluxesin andout of thesystem, andR isthe netincrease
dueto internalproduction andremoval(if removalisgreaterthenproduction then
R isnegative). Fluxesin andoutof thesystem aregenerallygoverned bytwo physi-
calmechanisms, diffusion(or mixing)andadvection (seechapter3). R is generally
a biologicalterm expressing the transferto andfrom otherstatevariables.
In all but the mostreductionist models,thesedynamicinteractions are non-linear
whichmustbe solvedby numericalratherthananalyticmeans.Numericalsolution
techniques requirea discretization of thegoverning dynamicequations.That is,so-
lutionscan only be specified at particularpointsin spaceandtime.An important
consequence of thisis the treatmentof sub-gridprocesses. For examplea sub-grid
process commonto nearlyall environmental modelsis turbulence,
or morespecifi-
callyhow turbulenceaffectsthe mixingof materialandmomentum.Discretization
alsohasimplicationsto technicalconsiderations suchas numericalstability.
Onceimplemented
asa computersimulation,
a modelgoestrougha seriesof stages:
Verification:the modeldoeswhat is expected.
Sensitivity
analysis:
howdetaileddo thegoverningparameters andforcingfunctions
needto be.Sincefor operationalandtacticalapplications,
forcingfunctions have
to be suppliedby a real-timemonitoringprogram,thisis a criticalstepfor man-
agersto considerin determiningthecosteffectiveness
of implementing a model.
Calibration:thoseparameters which are poorlyknownfrom naturecan be
'tuned'to givethebestfit of themodelto observations.Whilecommonly prac-
ticedin thepast,tuningis becoming unfashionablein the scientific
community.
In complex models theremaybescores of parameters,
anycombination ofwhich
canbetinkeredwithto geta 'goodfit'. Generalist
modelsshouldbetunedaslittle
aspossible:it isbetterto havea discrepancy
between modelresultsandobserva-
tionsthanbetween theparameters usedandthosemeasured experimentally.
Validation:testingthe modeloutputagainst independent observations.
Inherent
in thisstepis defininga criterion.If themodelis to be usedasa management
tool,thoseinvolved asendusersshouldcontribute to theestablishment
of this
validation criterion.
Modeldevelopment is an iterativeprocess
involving
refinement
asnewresources,
data,andunderstanding become available.
Valuablemodelseventually
leadto inter-
pretations usefulfor policyandmanagement implementation
andin exceptional
casesto a reviewof thescientificparadigmuponwhichtheyare
11.3.Lakes
Early this century,much effort in limnologywas devotedto classificationand

grouping of lakesaccording to theirproductivityasdefinedfrom theirspeciescom-
position.However,manylimnologists felt lake typologywasa blindalleyandthus
turnedto statisticalanalysisand experimentalecology.The eutrophicationof lakes
by phosphorus madelimnologyfocuson quantifyingnutrientloading,its relation-
shipto concentrations andprimaryproduction,andmodelingtheserelationships.
One classis the simpleempiricalsteady-state models,built on multi-lake,cross-sec-
tionalanalysiswhichconsiders lakesascontinuously stirredtank reactors,muchlike
a chemostatin chemicalengineering.Behindall eutrophication modelsliesthe law of
conservation of masswhichfor a nutrientin a confinedbodyof water canbe written
d (CV) / dt = M - QC - S (2)
where C is the nutrientconcentration,V the volumeof the water body,M the in-
comingmassof nutrient,Q the discharge from the water body, and S the massof
nutrientlostto sedimentationor the atmosphere. If the incomingnutrientis biolo-
gicallyavailableandtakenup by phytoplankton, thenthe amountsedimented out
depends on the amountof detritusproducedeitherdirectlyfrom phytoplankton or
throughhighertrophiclevels.In thiscaseit can be assumed that S is proportional
to massof nutrientin the lake, CV, with a proportionalityfactorc•,termedthe loss
coefficient.
At steadystate,Eq. 2 canbe rewrittenas
C = Lc/(Hr) (r/(r + or))= Lc(1 - Rc) / (Hr) (3)
wherer = QIV is the flushingrate,Lc = HM/V is the arealoadingof nutrient,H is

the meandepthof the waterbody,and Rc='oe/(r+ oz)is termedthe retentioncoeffi-
cient.The netlossof nutrientexpressed eitheras cror Rcand its relationship
to site-
specific
constants like morphology andhydraulicregimehaschallenged limnologist
for morethan 25 years.In a review,Kristensenet al. [1990] tested20 of theseem-
piricalmodelsfor inlakephosphorus concentrationsP in relationto the loadingon
131 annualdata setsfrom Danish lakes.Among the best was the well-known
OECD-modelapplication[Vollenweider and Kerekes,1982] which parameterizes
the phosphorus retentioncoefficientas:
Rp= 1 - 1.55 P exp(-0.18)/(1 + r exp0.5) exp(0.82) (4)
In a similarvein,Jensenet al. [1995] developed
and testedan empiric•al
modelfor
nitrogenconcentrationandloadingfor 98 Danishlakes.
Parallelto the development of thesenutrientloading-concentration models,have
beenmodelsrelatingnutrientconcentrations to phytoplanktonbiomassin lakes
[e.g.NichollsandDillon, 1978;Ahlgrenet al., 1988].The principalbehindtheseis
Lieberg'slaw of limitingfactors,that thelimitingnutrientis takenup asa constant
fractionof thecellmassor pigmentcontent.While attractiveas a simplifying prin-
cipal,manylaboratoryand field experiments havedemonstrated that thesecondi-
tionsarenot alwaysmet.For instancedifferentnutrientscan be limitingfor
entcomponents of thephytoplanktoncommunity at thesametime,cellvolumeand

pigmentcontentvarywith nutrientstatusandlightclimate,luxuryuptakeof P and
N canoccurat highconcentrations, otherautotrophic andheterotrophic compo-
nentsof the ecosystemcan competefor nutrients,and chemicalreactions are also
possible.Nevertheless,
for concentration
rangesof totalphosphorus up to 3 gM,
correlations
with summerchlorophyllarefair with linearslopeof 0.5 - 1 [Ahlgren
et al., 1988].
Thesesuccessesnotwithstanding, the complexity,difficultiesin parameterization
and the possibilityof multiplecausalityhaveled to the role of empiricalmodels
beingquestioned. In response, limnicmodelersareturningto theoretical, dynamic
modelswith high-resolution temporalandspatialscales, to explorethe relationship
betweenenvironmental factorsandeutrophication.
1.3. Estuaries
Estuariesare the most immediatemarine systemsto feel the impact of anthro-

pogenicloadingof nutrientsand organicmaterial.An estuaryis by definitionan
areawhere seawater and freshwater and their associated propertiesmix. How-
ever, unlike riversflowing into lakes,the freshwater enteringan estuaryhas a
dynamicinfluenceon circulationandmixingbyvirtueof its lowersalinityandden-
sity(seechapter3).
The mixingof freshandsaltwaterin the estuarymeansthat theinflowis not only
from the river, but alsofrom the adjacentsea(Figure11.2). Conservation
of vol-
ume and salt within an estuarygive:
QR+QB=Qs and SRQR+SBQB=SsQs
whichcanbe rearranged
to give
Qs = QR(s•- sR)/(s•- ss) and Q• = QR(Ss- S•)/(S•- Ss)
River Sea
••7 [e•trainment•/
•?
0 Xl
Figure
11.2.Circulation
andmixing
ina well-mixed
228 11. TheUseof Modelsin Eutrophication
Studies
[e.g.Bowden,
1984].Forinstance,
theriverRhinehasa meandischarge rateof QR
= 1200m3/sandcarries
essentially
no salt,SR= 0 psu.At themouthof theRhine,
theentrance
to theRotterdamwaterway,meansurfaceandbottomsalinities
are27
psuand30 psu,respectively.
Thisgivesa meansurfaceoutflow,andbottominflow
of Qs= 12,000m3/sandQB= 10,800m3/s.Thatis,anoverwhelming
percentage
of
the waterfoundin the RhineEstuaryoriginates
from the North Searatherthan
from the river itself.
Thisisreflectedin theflushingrate r of theestuary;

r = (Q• + Q•) / v' = (S• - S•)/(S• - Ss)Q• / v (5)
whichfor the Rhineis 10 timesfasterthanthe flushingratefor a lakeof the same
volumewith the sameriver inflow:r' = Q•/v. The energyrequiredto movethis
enormousamount of water comesnot from the hydraulichead of the river, but
ratherfromthepotentialenergyinherentin thefresh-saltwaterpartition.
Oneusefulpropertyexploitedin estuarinestudiesis that saltis a conservative
tracer.
This conceptwasusedby Officer [1979] to examinethe behaviorof non-conserva-
tive dissolved
constituents
(e.g.nutrients)empirically.Briefly,the one-dimensional
(alongestuary)steady-state
advectiondiffusionequations for saltS and a nutrient
C at some location can be written
Q•t S - g,, A dS/dx = 0 (6)

Qi•C - g• A dC/dx = F (7)
whereA isthecross-sectional areaof theestuary,K• is the longitudinal dispersion
coefficient,
andx is directedpositivedown-estuary. x = 0 is the riverend,andx = l
is the seaendof the estuary.F is the flux of the nutrientat thisparticularlocation
andcan,throughmanipulationof Eqs6 and7, bewrittenas:
F = Q•t (c- s dC/dS) (8)
The netlossof nutrientC from the estuaryis thengivenby L = F($o)- F(Si) which,
if the salinityat the riverendof the estuaryis So= 0 givesa fractionallossG writ-
ten as
G=(Co-Co*)/Co, wh•reC0*=C•-St(dC/dS)[l (9)

Thus,plottingthe meansalinityversusmeannutrientconcentration alongan estu-
ary givesan empiricalrelationshipof the utilizationor releaseof the nutrient(Fig-
ure 11.3)withinthe estuarywithoutspecificdependence on river dischargeor mix-
ing characteristics.
While thismethodhasfound somerefinement[e.g.Officerand
Lynch,1981], it remainsthe basisfor a powerfulempiricaltool in eutrophication
studies[e.g.OfficerandRyther,1980] in examiningthe role of silicatedepletionin
limitingprimaryproduction[vanRaaphorstet al., 1988] in examiningthe regener-
ationof benthicphosphorus in eutrophication of a shallowwater estuary).
Dynamicmassbalancemodelsof estuaries and othermarinesystems involvingthe
mixingof two distinctivewater massesare wide spread[e.g. Granthamand Tett,
1981;SmithandVeeh,1989;Pejrupet al., 1993;Hansenet al., 1995].Thisis
C
I il)"
'"
Co
"•
ii,
c !
(iv) .. - -
... -. -" C=O
(ii)
..
o
S0 = 0 SL !
So =0
Figure11.3. The fractionallossG of a nutrientconcentratiori

C in an estuaryasdeduced
fromC versussalinityS relationship.
a: concentration
in riverCo> concentrationin seaC •;
(i) conservative
(G = 0), (ii) non-conservative
andestuaryactsassink(G < 1), (iii)non-conser-
vativeandestuaryactsassource(G >1), (iv)no netflux outof estuary(G = 1). b: concentra-
tionin river C 0 < concentration
in seaC 2;(i) conservative,
(ii) non-conservative
andestuary
actsassink,(iii) non-conservativeandestuaryactsassource,(iv) no netflux intoestuary.
because the physicalcirculationof estuaries

havebeenlong studied.Indeed,phys-
ical modelsof estuarinedynamicsare now found widely in engineering appli-
cations,from the construction of leviesand dikesto the dredgingof navigation
channels. With thisproliferation,ecosystemmodelerscan makeuseof well-tested,
versatilephysicaldescriptions to quantifytransportand mixing rates, and turn
theirattentionto trophicdynamics,nutrientcycling,primaryproductionand hyp~
oxia [e.g.Soetaertet al., 1994; Hansenet al., 1995]. As thesemodelsgain credibi~
lity, their developersare comingto the stagewherethey can givemanagement
advice[e.g.SmithandHollibaugh,1989].
Fjords
Fjordsaregenerally distinctivesystems
in bothphysical andbiologicalterms.They
aredeep,enclosed basins,usuallywith a restrictive
sillat theirseawardapproaches.
Thisrelativelysimpleformis attractivefor modeling asthedemarcation is wellde-
fined.One of the few successful empiricalmodelingstudiesof eutrophication in
coastalseaswasprovidedby Gowenet al. [1992]in examiningScottishsealochs
(fjords).They essentially
followthe classicalempiricalapproachof Vollenweider
[1968,1976] for fresh-water lakes.However,takingnitrogenasthelimiting
::::••rradiance
' •x--
•
-• ouOgow •
Surface
layer
• •_• mixing
• River
exc•nge
• en•fainment
• •
Figure11.4. A schematic
diagramof the physicalfeaturesof a 0ord.
ent, theirmethodstresses the dynamic(ratio of relativechange)rather than the sta-

tic (ratio of concentration)relationshipusedin limnic systems.This is in recogni-
tion of the rapid flushingrate of marinesystems comparedto lakes.In thisway, by
analyzing60 observationdata sets,Gowen et al. [1992] estimatedthe yield of
chlorophyllfrom nitratefor 21 sealochs. Furtherthey suggested that an appropri-
ate yield valuecan be usedto predictthe potentialmaximum increasein phyto-
planktonresultingfromanthropogenic nitrogendischarge.
Giventhe long time scaleneededto identifytrends,marinescientistsare not con-
tent to leavesuchimportantenvironmentalquestionsto empiricalformulations,
and haveturnedtheirattentionto dynamicmodelingof fjords.Physicallyspeaking,
most fjordsare estuariesbeingthe site of the mixing of fresh and salt waters.
However,because of theirdepth,theyhavean accentuated verticalstructurerather
thenthe longitudinalstructureexhibitedby well-mixedestuaries.Most fjordsare
stratifiedwith a near-surfacepycnoclinedueto fresh-waterrunoff andoccasionally
a deeperpycnocline dueto tidal mixing(Figure11.4). This long-livedverticalstruc-
ture partitionsthe water columninto threelayerswithin which verticalmixingis
muchfasterthanmixingbetweenlayers.Thereis a slow,but measurable mixingof
freshsurfacewaterwith intermediate wateroriginatingfrom the opensea.The bot-
tom layerisgenerallyquitestable.However,slowbut finitemixingwith intermedi-
ate-layerwatersslowlyreduceits density,occasionally allowingthe intrusionof
densersalinewatersfrom the opensea.This causesa rapid turnover;a breakdown
of the lower pycnoclineand a completemixing of the bottom and intermediate
waters.Suchturnovereventsoccurperhapsonceor twicea
VisserandKamp-Nielsen 231
irradiance
Flush
out
] Surface
layer
fixation
•--•
uptake
J--•
,
C phytoplankton
N
Z
!c
a' '
c
a
r Pc
n
i
v
o
r
t 1-• e 1-.%
C phytoplankton
phytoplankton
s o s
N
[uptake
,•• , n
I Flush
in• layer '
Figure11.5.Schematic
trophicinteractions
in a fjordasmodeled
byRossetal. [1993].
Several
ecosystem
models
of fjordsxvithinthisphysical
contexthaveappeared
over
theyears[e.g.Tett,1986;Aksnes andLie,1990;Rippeth
et al.,1996].Asanillu-
strative
example,wediscuss herethemodeldevelopedbyRosset al. [1993].This
modelxvasdesigned for strategic
purposesandconcentrated
ononlya smallnum-
ber of dynamicinteractions.In particular,
biotaweredividedintothreemajor
trophiclevels;
phytoplankton, herbivores
andcarnivores
(Figure 11.5).Whilethisis
far from a state-of-the-art
description
of biological
interactions,
ignoringe.g.spe-
ciescomposition,
competition
andsuccession,foraging
behavior,
andthemicrobial
loop,it doesunderline
thespiritofsimplicity
thatvaluable
models
should
embrace.
These
modelbiotaweregivenappropriate
motilebehavior.
Herbivorous
zooplank-
ton and carnivores
couldmovefreelybemeensurfaceand intermediate
layers;
however, phytoplanktoncouldonlybe transported vertically
by watermotion
(mixing or entrainment)
or bysinking.
Nitrogen,
assumed to bethelimiting
nutri-
ent,cycled rapidly
in thesurfaceandintermediatelayers
between dissolved
inor-
ganic nitrogen
andphytoplankton throughuptakeandexcretion,andzooplankton
andcarnivores throughexcretion
(Figure
11.6).Thephysicalexchangeofwaterbe-
tween layerswasderivedfromconservationofsaltandvolume,observedstructure,
riverflowandtidalexchange, and•vasexpressed
asentrainment andmixingrates
with each
232 11. The Useof Modelsin Eutrophication
Studies
phyto Flush out
// .....
Surface
] e • Surface
•----/--'--•
phytoplankton
• [ DON DON
/I
J,/•,•• --
•[ Surface
•*'-/ \
• ..............
Zooplankton
m
g
g
ex
ex
m Carnivores
Intermediate
phytoplankton
[--••[
Intermediat
Sea) DON DON
ujIntermediate
•// (Sea)
Bottom
DIN
(Sea'
phyt Sediment/
DIN
Figure11.6. Idealizednitrogencyclingin a fjord ecosystem asincorporatedin the modelof
Rosset al. [1993]. Cyclingbetweenthe 10 nitrogenstatevariables(roundedboxes)are by
ex: excretion,r: demineralization,
u: uptake,g: grazing,s:sinking,en: entrainment,m: mix-
ing, t: turnover,d: diffusion.Further,six externalnitrogensources(hexagonalboxes)are
identifiedaswell asa flushingout sink.Inputandoutputof nitrogento andfromthe system
areby specified flow
Visser
andKamp-Nielsen 233
Even
thissimple
rendering
ofthenatural
system
results
inarather
complex
mathe-
maticalmodelinvolving:
ß 14 coupled
differential
equations
describing
the14 statevariables;
10 fornitro-
gencyclingandfourforcarbon.Eachofthese
equationsisofthegeneralform
dCn/dt=aoC,
+ Zm•nbnm
C,n+CnZm•ncnmCm+
ZjFi(t) (10)
a slightvariationof theVolterraequation,
whereCnis theconcentration
of the
nthstatevariable,
a0is itsgrowth/decay
rate(e.g.excretion
rateof nitrogen
by
phytoplankton),
bnm represents
linearcoupling
to otherpools,largelyphysical
exchangeprocesses
suchas the entrainmentrate of intermediatedissolvedinor-
ganicnitrogen(DIN) into the surfacelayer,Cnm non-linear coupling, primarily
trophicinteraction (e.g.nitrogen
lostfromsurface phytoplankton poolby zoo-
planktongrazing),andFi(t) is externalforcingfunctions suchastheconcentra-
tion of DIN in inflowingriverwater.
ß A totalof 38 parameters governing
thesystem dynamics; 15 forphytoplankton,
10 eachfor zooplankton andcarnivores,
and3 for nutrients.Theseincludeup-
takerates,excretionrates,mortality,grazingratesetc.
ß 14 externaldrivingfunctions,includingthe seasonal variationof lightintensity,
nutrientconcentration
in river and seawater,the immigrationof zooplankton
andcarnivores,
andspecification of the intensityandtimingof turnoverevents.
Themodelwasappliedto KillaryHarbour,a fjordor•thewestcoastof Ireland,
and a notionalScottishsealochapproximating
the innerbasinof LochLinnhe.One
surprisingresultwas that nutrientloadingwas primarilydrivenby nutrientcon-
centrationsin the opensearatherthan in the river. internalcyclingof nutrients
appearedto havelittleinfluence.Thiswasevidenced in the responseof thesystem
to turnover events. While such events increased the nutrient concentration in the
euphoticzone,theywereflushedoutof thesystem fasterthantheycouldbetaken
up.Inorganicnitrogen
supplyexceededbiologicaldemandfor all buta shortperiod
at peakspringbloom.The strongestcontrolon the sizeof the springbloomwas
physical
factors,temperature
andirradiation,
aswellasthedynamics of thesubse-
quentzooplanktonbloom.This latterindicates a top-downcontrol,depending
ultimately
onthesuccessof zooplanktonoverwinteringin thedeeplayerand/orthe
importof zooplankton
fromtheadjacent sea.
In a laterstudy[Rossetal., 1994],themodelwasfurtherrefinedespecially
withre-
spect to thegrazingdescriptionandwastested foritsgenerality
onfourIrishand
Scottish sealochs,
eachwith rapidflushing rates.Thesesimulations
confirmed the
importance of top-downcontrolanda furthersimplification wasmadeto only
threestatevariables:
phytoplankton, zooplanktonandcarnivorecarbonin a single
layer.Thefit ofthisminimal model wasindistinguishable
fromthatachievedbythe
moresophisticated dynamic description
of Figure11.5.Thishighlights
aninterest-
ingpoint;that'improving'
a model
does
notnecessarily
mean increasing
itslevelof
s.6.Coastal Seas
Of theaquaticsystems mentioned here,quantifying

andqualifyingeutrophication
in coastalseasposesthegreatestchallenge.Caughtastheyare, betweenthe land
andthe deepblueseatheyfeelboththe impactof anthropogenic fluxesand the
rhythmiccyclesof climaticvariationplayedout overthe deepoceanbasins.That
there are natural,interannualvariationsin ocean- atmospherecouplingis well
known,E1Nifio and theNorth Atlanticoscillationfor instance.Althoughnot rigor-
ouslydemonstrated, it is likely that thesevariationsimpactshelfseasalso;the
'greatsalinityanomaly'of the 1970sin the North Seafor instance[e.g.Turrell,
1992; Lindeboomet al., 1994]. While the term eutrophicationis neutralsaying
nothingaboutthesourceof thecauseor thequalityof theeffect,for policymakers
thereis a cleardistinction:thereare thoseundesirableeffectsthat can be regulated
for, andthosethat cannot.Clearly,a properunderstanding of environmental dyna-
micsis crucialfor soundpolicyimplementation.
Giventhe complexdynamicsplayedout in coastalseas,empiricalmodelingof
coastaleutrophicationis rare. One notableexceptionis Nixon [1992] who reports
the relationshipbetweendissolx/ed inorganicnitrogen(DIN) for primaryproduc-
tion andphytoplankton biomassin a wide rangeof marineenvironments. It was
foundthatat loadinglessthan5 mmolm-2yr-1 thenetprimaryproduction wasless
thanthatwhichwouldbeexpectedby the Redfieldratioindicatingthe significance
of nitrogenrecyclingat low input rates.The rigor of this relationshipis yet to be
fully explored.
Eutrophication by nutrientloadingis a two-prongedproblem.Firstly,there is the
questionof how thesenutrientsare dispersed from a source,and secondly,their
subsequent stimulationof primaryproduction.In this, the distributionand avail-
ability of nutrientsin coastalseasare intimatelyconnectedwith buoyancyeffects
(seechapter3). 7 hisis exhibitedin two phenomena; nutrientsderivedfrom riverine
sources carriedin buoyantlow salinitycoastalplumesandthe stratificationandde-
stratificationof the seasonalthermoclineand its role in governingthe vertical
cyclingof nutrients.
An increased understanding of the couplingbetweenphysicaland biologicalpro-
cesseshasresultedin the hypothesis that the seasonalcyclesof phytoplanktonin
shelfseascanbeexplainedin termsof the relationship betweenverticalmixingand
the requirementof planktonicmicroalgaefor light and nutrients[Pingteeet al.,
1977]. The key to this systemis the development of the seasonalthermocline;the
periodwhenlightconditions are suitablefor photosynthesiscoincidewith develop-
ing watercolumnstabilityso that nutrientslostform the euphoticzonetendto re-
mainlostfor the duration.Conditionssuitablefor planktonbloomsonly occurfor
a shortperiodin the springand occasionally in the autumn;for the mostpart con-
ditionsfor phytoplankton growtharerelativelypoorbecause of inadequatelightin
the winterandlimitingnutrientsin the
Visser
andKamp-Nielsen 235
Whilethisistheseasonal
scenario,
a similar
mechanism
isthought
to operatefor
episodic
nuisance
bloomsoftenoccurring
insummer.
Hereacombination ofstrong
windsand/ora spring
tidetemporallyreduces
watercolumnstability,
injecting
nutrients
intotheeuphotic
zone,andtriggering
thebloom.
Overtheyears
a number
ofmathematical
models
formulated
toinvestigate
thissys-
temhasappeared [e.g.RadachandMaier-Reimer, 1975;Jamartetal.,1977;Steele
andHenderson, 1981;FashamandPlatt,1983;Tayloret al., 1986;Tett et al.,
1986;Stigebrandt
andWulff,1987],eachwithvarying levels
of sophistication
and
success.
Onedistinctivedifferencebetweenthese
washowvertical mixing processes
weretreated.Theserangedfroma uniformdiffusivity,
to entrainmentintothesur-
facewind-mixedlayer,to a state-of-the-art
dynamicdescription.
An exampleof a vertical'point' modelthat serves to illustratethisis that formu-
latedby SharplesandTett [1994].In thisandothersuchmodels,the advection of
nutrientsand lateralbuoyancy effectsareconsidered unimportant andnot model-
ed, thusrestricting
their suitabilityto, for instance,
the centralgyreof the North
Sea.None the less,it accentuatesomeimportantprocesses with potentialapplica-
tion to eutrophication.
The modelformulationcanbe dividedinto two aspects as
follows:
Physical:
ß Momentumis impartedto the watercolumnby a tidallyvaryingpressure gradi-
ent and surfacewind stressandlostthroughfrictionat the bottom.The vertical
stressis givenby r(z) = Nz au/az whereu is thehorizontalvelocityvectorand
Nz is the verticalturbulentviscosity.Thus
u/•t+fzxu-•(Nz•u/•z)/•z= -A sin(wt) (11)
withsurface
andbottom
boundary
conditions
respectively
%= ks]wlw and•'b=
ß Densitychanges
withinthewatercolumn arebrought aboutbysurface
heating
andcoolingandturbulent
vertical
diffusion.
Verticalmixingoftemperature
T is
regulatedby
T/•t-•(K• •T/•z)/•z =0 (12)
whereK=istheverticalturbulentdiffusivity.
ßTurbulent
properties
NzandKzarecalculated
dynamically
through
a level-2
tur-
bulentclosure
scheme [MeliorandYamada,1982].Essentially
thisscheme
recog-
nizesthatthevertical
mixingof momentumandmaterialbecomes suppressed
as
thewatercolumn stratifies.
Competing
withthisistheturbulent
cascade
of ener-
gyfromthemacro-
to themicro-scale;
energy
whichis usedin partto erode
stratification.
Formulations
of thisscheme
aremanyandvariedandwill not be
reproduced
here.Interested
readers
canrefertoLuyten
etal.[1996],oneofthe
more readabletreatmentsof the
Biological:
Fourdepth-and time-dependent
statevariableswereconsidered
in describing
bio-
logicalinteractions:
ß Phytoplankton
biomass
X: aX/Oz = a(KzaX/Oz)/az + I•X-gX (13)
/x isthereproduction
rateandg thegrazingrateby zooplankton
ß Dissolved
inorganicnitrogenS: aS/Ot=a(KzaS/az)/az-uX + egX (!4)
u is the uptakerate by phytoplanktonand e is the fractionexcretedby zoo-
plankton.
ß InternalalgalnutrientN: •N/•t = •3(K•N/•z)/•z + uX-gN (15)
ß PAR(photosynthetically
activeradiation)I: •3I/az = - I (X0+ eX) (16)
wheree simulates
theselfshadingby phytoplankton,
and A0is theattenuation
coefficient.
Onenovelfeatureof themodelis that it includesa biologicalinfluenceon the phys-

ics,namelytheheatingandstratificationof thewatercolumnby absorptionof solar
radiationQ• by phytoplanktonX. Specifically
•Qs/•Z = - Q• (,•o+ •X)
The modelwas usedto exploremechanisms involvedin sustainingthe subsurface
chlorophyllmaximumobserved in the centralNorth Sea.The potentialimportance
to eutrophication
is discussed
in chapter5. With respectto this, threehypotheses
that havebeenpresented weretested:
1. Pingreeet al. [1977] suggestedthat a slowleakageof nutrientsinto the thermo-
clinecoupledto the relativelylong residence time of phytoplanktonin that re-
gioncanleadto enhancedproductivity.
2. Steeleand Yentsch[1960] suggested that phytoplanktonsinkingratesdecrease
asnutrientsuppliesincrease allowingthemto take advantageof higherambient
nutrient levels near the thermocline.
3. Margalef[1978]andTett [1987] proposed that dinoflagellates
anddiatomscan
migrateverticallyto takeup nutrientsat depthand photosynthesis nearthe sur-
face.
Of themodelsimulations incorporating
thesemechanisms, only (1) produced a sub-
surfacechlorophyllmaximum(Figure11.7):that is it is dueto purelyphysicalef-
fects,theslowdiffusive(background)entrainment
of nutrientsinto a stabilized
layer
of thewatercolumnratherthana behavioral adaptationof thephytoplankton.
A second effectexploredby thismodelwashow it responded to varyingdetailin
the wind forcingwhichis the major sourceof verticalmixingin the centralNorth
Sea.In particular,a comparisonwasmadebetweenmodelresultsdrivenby season-
ally averaged winds,and moredetailedwind forcingfrom daily observations. It
wasfoundthat the morerealisticmeteorological inputsreproduced the
Visser
andKamp-Nielsen 23-
Hek.Iht, m
75
50
25
o ' 5'0
mg chl m-3 Time, days
I Above
8.015.0-8.0 3.0-5.0
2.0-3.0
F---•1.0-2.0
[---•0.5-1.0
I-----]Below0.5
Figure11.7.Subsurface chlorophyll
maximum simulated bySharples andTett [1994],fora
notionalcentralNorthSeasituation. Forcingissimulated by monthly meanmeteorological
conditions (wind,temperature,light),anda gentleentrainmentof nutrientsintothethermo-
clineis included,testingthehypothesispostulated
byPingreeet al. [1977].
maximumwithoutrecourse to theartificiallyinduced
background diffusionusedin
testinghypothesis (1) above,thusidentifying thesourceof theslowleakageof nu-
trientsinto the euphoticzone,and highlightingthe needfor soundphysicalframe-
works uponwhichto developecologicalmodels.
While this classof modelhasfoundits widestapplicationto dateasa researchtool,
someinvestigators are turningtheir attentionto eutrophicationand its associated
influence.An indicationof this was presentedby Stigebrandtand Wulff [1987]
who developed a time-dependent physical-bio-geochemicalmodelwith highvertical
resolutionto investigate
nutrientand oxygenconditions in the BalticSea.While
this modelhad poor horizontalresolution,it showedreasonable correlationwith
20 yearsof observations
in theEastGotlandBasin.
Closerto thecoast,ecologicaldynamicsareinfluenced asmuchbyhorizontalasby
verticaltransportandmixing.Thesecomplex systems areonlynowdrawingtheat-
tentionrequiredto modeltheirphysical aspects[e.g.Simpson et al., 1993].Given
this,fully interactive
physical
andbiological
models of suchsystems areasyetnot
forthcoming. Nonetheless,
somesimplifieddynamic descriptions haveshownsome
success in investigating
eutrophication.
Forinstance, it is estimated thatthenitro-
genandphosphorus loadcarried
bytheRhineintothesouthern Bightof theNorth
Seahasincreased
6-fold sincethe 1930s.Especially
in the coastalareas,silicateis
nowthefirstnutrientdepleted
byspringbloomsasopposed to nitrogen
andphos-
phorus60 yearsago.To whatextentthistrendhasgivenriseto enhanced
phyto-
plankton
growthandchanges in species
composition
wasexplored byFransz
238 11. The Useof Modelsin Eutrophication
Studies
mg
rn-3
1000
750
SO0
250
0 , , , , , , , , , ,
1250
1000
750-
500 /,,"•, /' i
25O
0-, , , , , , , , , , ,
J'F H A H J J A S 0 N O
53o Vii
52
ø 7 ,/
,/ 3ø z+o 5ø
Figure11.8.Seasonal
variationof diatom(a) andotherphytoplankton
(b) carbonwithina 6
kmwidestripof theNetherlands
coast(stripI of c) assimulated
byFransz
andVerhagen
[1985].Simulations
arefor (a) 1980 conditions,
(b) 1930 conditions
and(c) 1930 riverdis-
charge with1980ambient seaconcentrations.
Similarvariations,
although
smaller
in inten-
sityareexhibited
in othermodelstripsextending
beyond100km fromthe
Verhagen[1985] usinga dynamicmodel.Whiletheywerecautious in ascribing

too
muchsignificance to their results(therebeinga paucityof observational
evidence
for validation)theyshowed,asillustratedin Figure11.8:
Diatombiomass hasnot alteredappreciably overthelast60 years.Whilethereis
someindicationof changein thenearshorezone(Figure11.8),2-foldincrease in
the springbloomanda 2-folddecrease in theautumnbloom,duringthesummer
months,and indeedintegrated overthe wholeyear,the diatombiomass hasre-
mainedrelativelyunchanged.
In contrast,the biomass of otherphytoplankton species,
mainlydinoflagellates,
hasincreased by a factorof 2 to 4 between 1930and1980.Half of thisincrease
appears
to bedueto theincreased
loading
ofN andP intheRhine,
andtheother
half from increasedconcentrationsin the coastalsea, also from anthropogenic
sources
discharged
throughotherrivers,e.g.MeuseandScheld.
60 yearsago,diatoms
dominated
thephytoplankton
of theDutchcoastal
zone.
Now, thishasswitched
to other,nonsilicate
dependent
species.
Thesetypesof calculation,despitetheirhighdegree of uncertainty,
directre-
searchers
in theirplanning
of futurestudies,
bothin identifying
possible
processes
andin thedesign of observational
programsneeded to corroborate
theirimpor-
tance.
Withtheadventof cheap,readily
available
andmassive
computing
power,a signi-
ficantsectionof theoceanographic
communityhasembarked onthenumerical
modelingof large-scale
ocean
systems.
Thistrend,
firstevident
inphysical
oceano-
graphy,
isbecoming
morepopular
inthestudy
oflarge-scale,
shelf-sea
ecosystems.
Anextensive
review
of these
types
of models
astheypertain
to theNorthSeawas
provided
byFransz
etal.[1991].
Morerecently,
fullydeveloped,
3-dimensional
cou-
pled
physical-biological
modelsarebecoming
available,
e.g.Aksnes
etal.[1995]
for
theNorthSea,TamsaluandMyrberg[1995]forthephysical
componentand
Tamsalu
andEnnet
[1995]
forthebiological
component
ofaBaltic
ecosystem
model.
Conclusions
Eutrophication
studies
oflakes
areatthestagewhere
predictive
models
arewide-
spread
and successful.
Thisisnotsoformarine
systems.
Thesingle-most
complicat-
ingfactor
inmarine
ecosystems
isthatthey
areunbounded.
Length
scales
inmarine
systems
arerarely
geographical,
butdepend
ongoverning
processes
often
incombi-
nation;
e.g.anadvective
velocity
times amechanism's
timescale.
Aproperdescrip-
tionofnutrients,
theirsources
andcycling
together
withwater motion
andmixing
isa fundamental
criterion
inunderstanding
andregulating
forsuch
potentially
cat-
astrophic
events
asmassive
ortoxic
plankton
blooms
and
anoxia.
Ecological
and
marine
scientists
aremeeting
thechallenges
posed
bythese
questions
inthemany
andvariedenvironments
in whichtheyarefound.
Empirical
modeling
hasitsplace
inilluminating
relationships
andaccentuating
processes.
However,
it isbecoming
clear
that
coupled
physical-biological
represent thebestavenuetowardthe future.This is in recognitionthat eutrophica-

tion is not simplya questionof nutrientloading,but that the pathwaysthrough
which nutrientsimpacton marineproductivityare many and varied, beinggov-
ernedasmuchby physicalasbiologicalprocesses. Here muchcan be learnedfrom
the largebodyof expertise existingin the physicaland ecologicaloceanographic
modelingcommunity. Whilethe conceptof slippingbiologicalmodulesinto exist-
ingphysical modelsis appealing,
it mayin practiceprovefar from straightforward.
In the comingyears,managersand policymakersmay expectmarinemodelsto
comecloserto realizingtheir potentialas predictivetools.In this, it is anticipated
that decision
makerswill work closelywith modeldevelopers, in particular
in definingthe questionto be addressed
helpingto establishadequatemonitoringprograms,the cost effectivenessof
whichcanbe gaugedby sensitivityanalysis
applyingriskassessment to establish
reasonable
modelvalidationcriteria.
Finally,it shouldbe notedthat an ecologicalmodel,no matterhow well testedand
validated,can neverbe a substitutefor monitoringand scientificinterpretation.
Their implementation and interpretationdemanda 'headsup' approach.Models
cannotbetreatedasoff-the-shelf productswhichcanbe blindlyappliedto provide
answers; the scientificcommunityaswell asdecisionmakersare ill servedby those
who suggest theycan.Nonetheless, the quantitativeandpredictivepowerof models
is hardto ignore,especially in thesedaysof unprecedented and rapid environmen-
tal change.
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Tett, P., A. Edwards,and K. Jones,A modelfor the growthof shelfseaphytoplankton
in
summer,Estuar.Coast.ShelfSci.,23, 641-672, 1986.
Turrell,W. R., New hypothesis concerningthe circulationof the northernNorth Seaand its
relationto North Seafishstockrecruitment, ICESJ. Mar. Sci.,49, 107-123, 1992.
van Raaphorst, W., P. Ruarij,and A. G. Brinkman,The assessment of benthicphosphorus
regeneration in an estuarineecosystemmodel,Neth. J. SeaRes.,22, 23-36, 1988.
Vollenweider, R. A., WaterManagement Research, OECD, ParisDAS/CSI,68.27, 1968.
Vollenweider,
R. A., Advances in definingcriticalloadinglevelsfor phosphorus
in lakeeu-
trophication,
Mem. Ist. It. ldrobiol.,33, 53-83, 1976.
Vollenweider,
R. A., andJ. Kerekes, Eutrophication of Waters,Monitoring,Assessmentand
Control, OECD, Paris,
12
Conclusion,Researchand
EutrophicationControl
Introduction
Fromthepreceding
chapters,
it is clearthateutrophication
canhaveprofound
effectson coastalmarineecosystems.
However,theeffectof nutrientenrichment
on
nutrientmetabolism in marineenvironmentsis a complicated
phenomenon that
will dependuponthequantitiesandspecies
of nutrientsbeingdeliveredto thesys-
temaswellasthemechanism(s) andtimingof thedelivery.
In addition,thehydro-
graphic,geological
(i.e.bottomtype)andbiological characteristics
of therecipient
are importantin determining theeffectthat eutrophication
will haveon an ecosys-
tem.Thus,it is difficultto generalize
abouttheeffects of eutrophication
in marine
coastalenvironments and predictionof the potentialeffectsin anygivenenviron-
mentwill requirethoroughanalysis of the physical,chemicalandbiologicalpro-
cessesoccurringthere.
2.2. Nutrient Limitation,Sourcesand Fluxes

From availableinformation,thereis no reasonto believethat the initial biological
responseto eutrophication in temperate
regionsdiffersgreatlybetweenfreshand
marinewatersor from onemarineregionto another.Plantbiomass in all of these
environmentsis, at leastduringsomeperiods,limitedby nutrientavailability andin-
creasing
nutrientinputvia eutrophication will,whennutrientlimitation is in effect,
increase
plantgrowthand/orchange thespecies composition
of theplantcommunity.
In mostfreshwaters,phosphorus(P)availability
isacceptedto belimitingforplant
growth.Thus,mostremedial actions
withrespect to eutrophication
in freshwater
havefocused onP controlandattemptsto describetheregulationof productivity
in

Union
244 12. Conclusion,Researchand EutrophicationControl
thesesystemshavegenerally beenbasedon massbalances with P (seechapter11).

In marinesystems,however,thesituationis morecomplicated. Here,it is generally
arguedthat nitrogen(N) ratherthan P is usuallythe potentiallylimitingnutrient
for primaryproduction[e.g.,Smetaceket al., 1991].
Thisargumentis not universally accepted (seechapter1, section1.4). However,it
doesseemclear,on thebasisof a comparison of the elementalcompositionof phy-
toplankton andtypicalfreshandmarinewaters,thatnitrogen,phosphorus andsili-
ca areall potentialcandidatesfor limitingplantgrowthin marinewaters.In fresh
waters,phosphorus is the macronutrientmostlikelyto limit phytoplankton pro-
duction(seechapter1, thisvolume,andHeckyandKilham[1988]).The possibility
that N and/orothernutrientsmay be limitingfor plant biomassin marinesystems
makesit muchmoredifficultto establish massbalancedescriptions of suchregions.
Thisis becausethereappears to bethepossibility for differentnutrientsto be limit-
ing for phytoplanktongrowthat differenttimesin marinewaters.Thus,it is not
immediatelyobviouswhich nutrientshouldbe chosenfor the establishment of a
massbalanceto describe productionin marinesystems. However,evenif, asmany
suggest,nitrogenavailabilitycontrolsproductionin mostmarinesystems, establish-
ing an N massbalanceis not as straightforwardasestablishing a P massbalance.
Thisis because biochemical processes (denitrificationand nitrogenfixation)in ad-
ditionto geochemicalprocesses (input/removaL/burial) controlnitrogenavailability
in aquaticecosystems. Similarbiochemical processes with respectto phosphorus
input/removalare not found.Reliabledata on the ratesfor the input/removalof
nitrogenvia biochemicalprocesses arestillscarce.
In addition,atmospheric deliveryof nitrogento the coastaloceanscanbe a quanti-
tativelyimportantinputprocess.This is not the casefor P input. Atmospheric N
contributionsto total N deliveryin mostmarinesystems are, however,not yet well
quantified.The greaternumberof processes affectingN input/outputto coastal
marinesystems makethe establishment of a quantitativemassbalancefor N more
difficultthanfor P. Thus,manyof the advances madein the field of limnologywith
respectto modelingeutrophicationeffectsand the potentialenvironmentalim-
provementthat mightbe expectedfollowingremedialactionsare not directlyap-
plicableto coastalmarineenvironments.
12.3.Establishing
CauseandEffectRelationships
It is verydifficultto quantifyand, thus,predictcausalrelationships whena change
in ecosystem structuredueto eutrophication is observedin the marineenvironment.
Unequivocal identification
of causeand effectusuallyrequiresthat the "effect"in
questioncanbe reproduced in a testsystemwhenthe systemis subjected to the sus-
pectedcausaltreatment.Manipulationof entiremarinesystems is usuallynot poss-
ible."Mesocosm" (small-scaleexperimental modelof the studysystem)studieshave
beenvaluablein clarifying manyof theecosystem responses observed in the wakeof
marineeutrophication [e.g.,Isaksson et al., 1994; Hinga, 1990; Oviatt et al.,
Richardson 245
Oxygenconcentration,
mg 1-1
6
0 I
1960 19'65 19'70 19'75 19'80 19'85 19'90 1995
Figure12.1. Averageannualoxygenconcentrations (mg1-1)duringthe pooledmonthsof

August,September andOctoberin bottomwater(deepest availablemeasurementbelow19
m) in the regionenclosedby the followingcoordinates: 55ø55'-56ø40'N;10ø40'-12ø30'E.
Data fromthe InternationalExplorationof the Seas(ICES)Oceanographic Database.
However,thereare somefundamentaldifferences
betweenmesocosms andthe sys-
temsthey are designed
to mimic.The differences
usuallyidentifiedas beingthe
mostimportantarethoseassociated with theartificialboundaries imposed on the
system by themesocosm (i.e. lackof or onlylimitedcontactto naturalsediment,
growthof microorganisms on thewallsof themesocosm, etc.).It is oftenargued
thatthesedifferences
in boundaryconditions mayalterprocesses relatedto nutrient
turnoverwithrespectto thoseoccurring in nature.Thus,it isnotallquestions rela-
tingto causeandeffectin ecosystem responsesto eutrophication thatcanbean-
sweredwith the helpof a mesocosm.
In naturalmarinesystems,it ismostcommon thatcauseandeffectwithrespect to
eutrophication
responsesareargued onthebasis of correlations
between different
changes/responses
occurring withinthesystem.Thisstatistical
approach,however,
merelyindicatesthattwo variables changein a consistent
manner in relationto
eachother.Suchanapproach doesnotidentify
cause andeffectrelationshipswith
certainty.
Asa result,thereis oftenconsiderable
publicandscientificdebate con-
cerningwhethercauseandeffectrelationships in responseto eutrophicationare
established
witha degreeof certaintythatwarrantsspecific
remedialactions.
In theKattegat,
forexample,
it iswellestablished
thatoxygen concentrations
dur-
ingthelatesummer months
havebeendecreasing duringtheperiod1965-1992
(Figure12.1).Thecommonlyused•4Cmethod of measuringaquatic
primary
246 12. Conclusion,
Research
andEutrophication
Control
ductionwasdeveloped by SteemannNielsen[1952] who carriedout muchof his

earlyworkusingthemethodin theKattegat.As a result,thereexistsan unusually
longtimeseriesof dataon primaryproductionusingsensitive radioactivemethod-
ologyfor this marineregion.This time seriessuggests
that there has beenan in-
creasein the phytoplanktonprimaryproductionoccurringhere in the periodbe-
t-weenthe 1950sand the late 1980s-early 1990s (seechapter5, this volume,and
Richardson and Heilmann[1995]). This increaseis difficultto quantifyowingto
differencesin the methodsusedduringthe two studyperiods.However,Heilmann
and Richardson arguethat pelagicprimaryproductionhasincreasedby at leasta
factorof two betweenthe two studyperiods.
Thus,the reductionin oxygenconcentrations
observedin the bottomwatersof the
Kattegatduringthe lastthirtyyearscorrelates
with an increasein pelagicprimary
productionoccurringin the sameperiod.While this correlationdoesnot necessari-
ly indicatecauseand effect,thereis strongevidencefrom mesocosms
and somenat-
ural (especially
fresh-water)systems that an increasein the magnitudeof primary
productionresultsin an increasein hypoxiain bottomwaters (seechapter1 and
referencestherein).
Accepting thereis a likelycausallink betweenincreased pelagicprimaryproduction
and increased hypoxia,we thenwould like to determinethe causeof the increased
primaryproduction.As identifiedearlier(chapter1), primary productionis gen-
erallylimitedby light or nutrient'availability.There is no evidenceof a consistent
changein the light climatein the Kattegatthat would stimulateprimaryproduc-
tion duringthe periodof interest(S.E.Jensen,The Royal Veterinaryand Agri-
culturalUniversity,Copenhagen: unpublisheddata). Thus, it would appearthat
the mostlikelycauseof the increasedprimaryproductionis an increasein nutri-
ent availability.
Nutrient availabilityis, however,affectedby both natural and anthropogenic
processes.The hydrographic deliveryof nutrientsinto and out of the photiczone
determines the magnitudeof primaryproduction(seechapters4 and 5). Until re-
cently,mostinterestin termsof eutrophication's influenceon phytoplankton pro-
ductivityhasbeendirectedtowardadvectiveprocesses (the horizontaldeliveryand
removalof material)affectingnutrientavailability.However,the verticaldelivery,
via atmospheric depositionand upwellingof nutrientsfrom bottomwatersto the
surfacelayer is also critical to the productionprocesses occurringin stratified
coastalwaters.Examplesof the importanceof verticalnutrientfluxesfor pelagic
processesin theKattegatcanbe foundin chapters2, 4, and 5.
Upwellingis associated with a weakeningor breakdownof stratification.Such
changesare ultimatelydependentupon weatherconditions:wind (directionand
strength)andprecipitation (in the caseof the Kattegat,for example,fresh-water
inputto theBalticis importantin determining surfacesalinity).The exactrelation-
ship betweenchangesin nutrientavailabilityaffectingprimary productionand
weatherconditionsis still not quantified.However,it may be predictedthat a
greaterproduction of turbulentkineticenergyduringthesummermonths(i.e.prior
to the development of hypoxiain bottomwaters and when stratificationof
Richardson 247
watercolumnisgreatest)
willenhance
upwelling
ofnutrients
frombottom intosur-
facewaters
andstimulate
phytoplankton
growth.
At thesametime,turbulence
in
thesurface
layermaypromote aggregate
formation
(see
chapter4).Aslargeaggre-
gates
sinkmorequickly thansmaller
particles,
such
turbulence
eventsmayresultin
anincreasein thedelivery
of organic
material
tothebottom.
It may,then,bear-
guedthatanincreaseinturbulence
duringsummermonthsmaystimulatehypoxia
byincreasingthephytoplanktonproduction
andbyinducingdelivery
of organic
material to the bottom.
Ontheotherhand,turbulence willalsostimulatethedelivery
ofoxygen to bottom
w•aters
whichwillreduce thelikelihood of a serious
hypoxiaeventoccurringlater
duringtheseason. Thus,it isnotclearhowa long-termchange intheproductionof
turbulentkineticenergy
duringsummer months whenthewatercolumnis perma-
nentlystratified
mightbeexpected to affecttheprobability
andintensity
of hypoxia
events.Turbulence
generatedduringthelate-summer/autumn
monthswhenhypox-
ia isoccurring,
however,
will havea mitigating
effectonhypoxia
events
byincreas-
ing oxygendeliveryto bottomwaters.
Jacobsen [1994] examinedlong-term(1890-1988)variations in the productionof
turbulent kinetic energyfrom wind and currentsin the Great Belt area of the
Kattegat.For mostof the Kattegat,upwellingof nutrientsis a functionof wind
generated turbulence.
Here,thewindspeedcubed(W3)canbeusedasa proxyfor
wind generated turbulence.
Jacobsen hascalculated W 3 for the differentseasons
of
the year (winter= December,January,February,spring= March,April, May and
soon) for threedifferentstationsin the GreatBelt(Figure12.2).
W3, m3s-3 W3, m3s-•
1500 I i 1500
------- Yesborg Spring
.... Resna•s
.......... Romse
1 ooo 1000
..
500 500
o o ,,
15oo
Winter
'.
lOOO 1000
500 500
0 ,
1900 1920 1940 1960 1980 1900 1920 1940 1960 1980
Figure
12.2.Cubic
velocity
ofwindspeed
(W3)atthree
different
stations
intheKattegat.
The
coordinates
of the stationsare (Vesborg:55ø46'N10ø33'E;Resn•es: 55ø45'N 10ø$2'E;
Romse:55ø31N10ø48'E) asa function
of year).W3isusedhereasa proxyforturbulent
ki-
neticenergy
added
tothewatercolumn
fromwindactivity.
FromJacobsen
248 12. Conclusion,
Research
and EutrophicationControl
Fromthisfigure,it canbe seenthat thereappearsto havebeenan increasein W3

duringautumnandwintersinceabout1960.The patternis lessconvincing for the
springandsummermonths.The lackof a clearpatternin the wind conditions dur-
ing summermonthsmakesit unlikelythat a long-termchangein wind condi-
tionsduringthe periodcanexplainthe observed increasein primaryproduction
and hypoxiaeventsin thisarea.On thecontrary,it maybe arguedthat the appar-
ent increasein wind generatedturbulencethat has occurredduring the autumn
monthsshouldhavereducedthe intensityof hypoxiaeventsowingto its havingin-
creasedthedeliveryof oxygento bottomwatersduringthe periodwhenhypoxiais
mostlikelyto occur.
Fromtheavailableinformation,it is not possible to totallyeliminatethe possibility
that somenaturalchangeor combinationof naturalchangesin the forcingcondi-
tions for nutrientsin the photic zone may be relatedto the changesobservedin
pelagic primaryproduction. However,with ourcurrentunderstanding of thedyna-
micsof marineecosystems, it seemsmostlikely that the increases
in the frequency
and intensityof hypoxiaeventsin the Kattegatare a resultof an increasein the
availabilityof nutrientswhich has stimulatedthe productionof organicmaterial
originatingthroughphytoplankton primaryproduction.
12.4.Long-termChanges
in Anthropogenic
Nutrient Deliveryto the Kattegat
Thereare data showingan increasein anthropogenicinput of nutrientsto the Kat-
tegatsincethe 1950s.Hansenet al. [1995] havearguedthat anthropogenic nitro-
geninputto thesewatersdoubledbetweenthe 1950sandthe 1980s(seechapter3).
Data do not appearto be availablein orderto conductsimilaranalyses for phos-
phorus[Hansenet al., 1995].
Whiletheincrease in anthropogenic inputof nitrogento the Kattegatmay havein-
creasedby a factorof two, the absolutemagnitudeof the nutrientsourcesmostaf-
fectedby anthropogenic activities(i.e. runoff and atmospheric input) is still rela-
tivelysmall(214 thousandtonnesper annum)in termsof the grossnitrogendeliv-
eryto theKattegat(794 tonnesper annumfrom Table 12.1). This discrepancy be-
tweenthe sizeof the localanthropogenic input of nutrientsto the regionand the
total nutrientdeliveryhasled to considerable discussionasto whetheror not reme-
dial programs designed to reduceeutrophication fromlocalsources canbe expect-
edto resultin a measurable improvement in oxygenconditions in theKattegat.
Thereare, however,severalimportantfactorsthat needto be taken into account
whenconsidering eutrophicationeffectsand their relationshipto the localanthro-
pogenicnutrientinputversusmoredistantnutrientsources.The first is that it is net
ratherthangrossdeliveryof nutrientsthat is mostrelevantin termsof the long-
termresponse of the ecosystem.Largeamountsof nutrientsexit the Kattegatover
boththe Balticand (especially)
the Skagerrakborders.Thus,the net nutrientdeliv-
ery overthesebordersis considerably lessthan the grossdelivery.As runoff
Richardson 249
atmospheric
delivery
ofnitrogen
isalmost
entirely
netdelivery,
therelative
impor-
tance
ofthese
sources
inthenetbudget
ismuchgreater
thaninthegross
N budget
for the Kattegat(Table12.1).
Relatingsuchnitrogen
budgets
tophytoplankton
activity
isfurther
complicated
by
thefactthatthesebudgets
aremost often
created
fortotalnitrogen
orphosphorus
input.Considerable
amountsof nitrogen
areboundupin complex organic
com-
pounds (forexample,
humicsubstances).
Mostphytoplankton
arenotabletoeffi-
cientlyutilizesuchorganic nitrogencompounds asa nutrientsource.In addition,
theturnover time(i.e.timerequiredto breakthecompound downto itsinorganic
constituents) for manyorganic nitrogen compounds is largerelativeto theresi-
dencetimeforwatermasses inmanyareas(including theKattegatwheretheaver-
agewaterexchange is on the orderof fourmonths[Hansenet al., 1995]).Thus,
the nitrogenboundup in theseorganiccompounds is oftennot immediately
availablefor phytoplankton growthandit istheoretically
possiblefor suchcom-
poundsto betransported throughtheKattegatwithouteverbeingincorporated
into phytoplankton.
The percentage of organicnitrogenvariesfromeachof thesources shownin Table
12.1. The highestpercentage (>90%) is foundin BalticSeawaterenteringtheKat-
tegat.Thus,of thenet deliveryof 122,000tonnesof nitrogenentering theKattegat
yearlyfrom the Balticonly an estimated8 tonnesis estimatedto bein an inorganic
form immediatelyavailablefor phytoplankton growth[Richardson and.,ZErtebjerg,
1991] (Table 12.1). Giventhat mostof thenitrogenenteringtheKattegatvia local
anthropogenic inputis in an inorganicformthat is immediately
availableto phyto-
plankton,the potentialof localnitrogeninputto influencephytoplankton growth
in theKattegatmayactuallybegreaterthanthatof BalticSeanitrogen eventhough
it initiallyappearsthat morenitrogenis comingfromthelattersource.
Similarly,the timingof nutrientdeliveryis importantin determining
the relative
importance of a particularnutrientsourceto phytoplankton growth.In surface
TABLE 12.1. AnnualNitrogen(N) and Phosphorus

(P) input to the Kattegatin 1000
tonnes.From Richardson
and ]Ertebjerg[1991].
Baltic Skager- Atmo- Den- Sweden Get- Total

rak sphere mark many
"Gross"inputtotalN 180 400 60 90 45 19 794

"Net" inputtotalN 122 -173 49 90 45 19 152
"Net" inputinorganic
N 8 54 49 75 34 16 236
Baltic ' Skager- Atmo- Den- Sweden Ger- Total

rak sphere mark many
"Gross"inputtotalP 18 62 0•5 5.8 1.6 2.6 90.5

"Net" inputtotalP 10.7 6.6 0.5 5.8 1.6 2.6 14.6
"Net" inputinorganic
P 2.2 4.7 0.5 5.0 0.6 2.0
waters,phytoplankton are apparentlylimitedby nutrientavailabilityfrom the

periodfollowingthespringbloomuntiltheautumnalbreakdown of stratification
(seechapter5). Thus,nutrientsenteringthe surfacewater duringthis time will
potentially
stimulatephytoplankton growth.On the otherhand,nutrientsadded
to the watercolumnduringthe winterwhenlight is limitingfor phytoplankton
growthwill not necessarily
resultin an increasein phytoplankton growth.This
meansthat there is the possibilityfor nutrientsto be transportedthroughthe
Kattegatduringthe wintermonthswithouthavingany effecton phytoplankton
growth.
Thus, the useof an annualbudgetfor total nitrogendeliveryto/removalfrom a
givenwaterbodyas a tool for identifyingthe causes of eutrophicationeffectsin
coastalmarinewatersis limitedbothby the fact that mostphytoplanktonpreferen-
tiallyutilizeinorganic
nitrogenformsandthelackof seasonal resolution.
Suchbud-
getsare,however,usefulfor describing
theoverallnutritionalstatusof an areaand
for identifying
long-term
changes
in therelative
importance
of various
nutrient
sourcesto a given area.
Anotherapproach that maybe appliedwhenlookingfor a potentialcausefor an
observed change,isto consider anychanges that mayhaveoccurredconcurrently in
the ecosystem. In section12.3, it hasbeenarguedthat the mostlikelycauseof the
observed increase in frequency andintensityof hypoxiaeventsin the Kattegatis a
change in nutrientavailability
for phytoplankton.Thus,identification
of anychanges
in the inputof nutrientsto thisregionis of importancein explainingthe observed
eutrophication effects.
From Table 12.1, it is clearthat the major sourceof nitrogenand phosphorus to
the Kattegatis transportfrom neighboring water bodies.Thus, it is importantto
determinewhetheror not there hasbeena major changein nutrientinput via this
sourceduringrecentdecades whichmightexplainthe appearance of the eutrophi-
cationeffectsobservedin the Kattegat.There is no comprehensive data seriesfor
total nitrogenand phosphorus concentrations in the watersenteringand leaving
the Kattegat.However,Smithand Richardson(unpublished data) haveexamined
the availabledata for nitrateand phosphate concentrationsin surfaceand bottom
watersat the bordersof the Kattegatduringthe period1970-1992 (Figure12.3).
Note that theseworkersexaminedthe bordersof the Kattegatproper.This means
that the southernborderis placedbetweenthe Kattegatand the Belt Seasand not
at the entranceto the Baltic.Thus,the surfacewater enteringat this borderrepre-
sents the combined outflow from the Baltic and Belt Seas.
The dataarelesscomplete for the beginningof the periodthan in recentyearsand

rigorousstatisticalidentificationof trendsin the data is difficult. Nevertheless,
theseworkersconcludethat there is no evidencefor a consistentchangein phos-
phate or nitrate concentrations in bottom waters in the northern Kattegat (i.e.
water enteringfrom the Skagerrak).Likewise,there appearsto be no consistent
trendin phosphate concentrations enteringthe southernKattegat(surfacewateren-
teringthe Kattegatfromthe BeltSeas)duringthe studyperiod.Theremay, on the
otherhand,havebeenan increasein nitrateconcentrations in surfacewaters
Richardson 251
ingthesouthernKattegat.However, thistrendisdifficult
to identify
owingto the
paucity
of thedatain theearlyyearsof thestudyperiod.
Assumingsimpletwo-layer"estuarine
circulation"andconservation
of volumeand
massof salt, Smithand Richardson (unpublished data)alsoexamined waterex-
change(bothhorizontalandvertical)in theKattegaton thebasisof knowledge of
salinityand fresh-waterinput.In thisanalysis, theywereunableto demonstrate a
consistentchangein the amountof waterentering(waterexchange through}the
Kattegatwhichmayhaveincreased the nutrientdeliveryfromsurrounding waters
duringthe period1970-1992. Thus,thisstudysuggests that therehasnot beena
majorchangein inorganic nutrientdeliveryto theKattegatvia advection fromthe
Skagerrak(i.e. the largest"gross"inorganic nutrientcontributor to the Kattegat,
Table 12.1) in thisperiod.While theremayhavebeenan increase
in nitrateconcen-
trationsenteringtheKattegatfromthesouth,thisstudydoesnotindicatewhether
thesechanges haveoccurredwithintheBalticor BeltSeas.
Concentrations
of nitratein surfacewatersexitingthe Kattegatto the Skagerrak
mayalsohaveincreasedduring
thestudy
period.Thus,thereappears to havebeen
anincrease
in inorganic
N concentrations
in waterexitingtheKattegat/Baltic
com-
plexbutnotinthewaters
entering
thissystem
fromtheSkagerrak/North
Sea.
This
studydoesnotaddress
thepotential
change
intransport
oforganic
nutrient
sources
acrossthe bordersto the Kattegat.
Anincrease
in inputof organic
nitrogen
to theKattegat
fromtheBaltic
mightbe
expected
given
thefactthattotalnutrientinputto theBaltic
hasalsoincreased
since
the1950s[Larsson
etal.,1985].Forvariousreasons
(including
therelatively
long
residence
timeforwaterintheBalticandthepermanent water
column stratifi-
cationwhichleadsto nutrient-poor
surfacewaters),
it isarguedthatinorganic
nu-
trientsin thesurface
watersoftheBalticwillbequicklyutilized
bythelocalphyto-
planktonpopulation
andnotbetransportedto theKattegat
[Richardson
and
./Ertebjerg,
1991].Therelative
proportions
of organic
andinorganic
nitrogen
in
watersentering
theKattegatfromtheBaltic(Table12.1)support
thisargument.
Thus,thereissomereason
tosuspect
thatthepossible
increase
innitrate
concentra-
tions
inthewater entering
theKattegat
over itssouthern
bordermaybetheresult
ofprocesses
occurring
intheBeltSeas.
There
isamuch
greater
percentage
ofinorganic
relative
toorganic
nitrogen
entering
theKattegat
through
theSkagerrak
border
than
fromtheBaltic
(Table
12.1).
Inad-
dition,
considerably
morenutrients
aretransported
overthisborder
thanoverthe
Baltic
border
(Table
12.1).
Thus,
input
over
thisborder
maybeexpected
tohave
the
greatest
influence
onphytoplankton
growth
ofanyofthenutrient
sources
tothe
Kattegat.
Again,
however,
Smith
and
Richardson
(unpublished}
were
unable
toiden-
tif-y
along-term
change
ininorganic
nutrient
delivery
overthis
border
(Figure
12.3).
Nevertheless,
itshould
benoted
thatanumber
ofauthors
have
argued
thattheJut-
landCoastal
Current
(JCC)
may,under
someconditions,
transport
large
amounts
ofnutrients
fromtheGermanBight
(which
isundertheinfluence
ofElbe,
Rhine
andWeserRiver
outflows)
totheSkagerrak
[e.g.,
Aureetal.,1990;
Maestrini
• 12
'6 10
E 8
• 4
• 2
0
70 75 80 85 90
14-
0 ß
70 75 80 85 90
ß: 2
fl.. 0 • - • • • • •
70 75 80 85 90 95
• 2 d
o
70 75 80 85 90 95
Figure12.3A. Monthlyaverages in surface(0-6 m) and bottom(definedas the deepest

recordin all dataprofilesthat are> 19 rn in depth)nitrateandphosphate
concentrations
at
stationssampledwithinthe geographic
coordinatesof 57ø20'-57ø45'Nand 10ø20'-1lø40'E
duringthe period1970-1993.Data from the International
Explorationof the Seas(ICES)
Oceanographic
Richardson 253
• 10
4 7O 75
I
80 85 90
16
• 14• b
0
E ,t' '
• 2 ß
Z 0
70 75 80 85 90
• 2
70 75 80 85 90 95
70 75 80 85 90 9õ
Figure
12.3
B.AsforFigure
12.3
Abutstations
taken
from
acoordinate
boxatthesouthern
borderoftheKattegat
(56ø05'-56ø45'N
and
254 12. Conclusion,
Researchand EutrophicationControl
N concentration,FM
40
30
20
•o::i•,•,
:'•,,• . ,.,i',.
,,,.,'.
,iti...
,:,
::!•.,•, •! i "' ! ',• i':'.j•'' .. :i i •! ': '••, ,4
..:•
/,": '
:
0 , ,
1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993
Figure12.4.Distributionof nitrateconcentrationsduringtheperiod1980-1992. -.... : open

NorthSeawaterin theNorwegian trench(meannitrateconcentration in thedepth100-400
m) and ß: surfacewaters(mean0.30 m) in a coastalregionoff the port of Hirtshalson
the Danishwestcoast.The coastaldata.wereselected to only includewatersaffectedby
coastalfresh-waterinflow (i.e.JutlandCoastalCurrent)by excludingvaluesfrom waters
withsalinity>34 psu.A seasonal patternin nitrateconcentrationsis clearlyevidentin the
coastalsurfacedatabut not in the deepNorwegianTrenchWaters.FromHeilmannet al.
[1991].
Gran•li,1991].It hasalsobeensuggested
thatthesenutrientsmaybe furthertrans-
portedinto the Kattegatandthat this nutrientsourcemay be importantin the
provocationof eutrophication
effectsin theKattegat.Indeed,thereis at leastone
well-documented recordin which nutrient-richJCC water has beentrackedwell
intothe Kattegat[A•rtebjerg,1990].
Whilesuchtransporteventscan be dramatic,they appearto be highlyepisodic
(Figure12.4).The importance of suchepisodic eventsin termsof the nutrientdy-
namics of theKattegatasa wholehasyetto bequantified. It shouldbenoted,how-
ever,that mostof the waterenteringthe Skagerrakand subsequently reachingthe
borderof the Kattegatis not of JCC originbut ratheroriginatesfrom the open
NorthSea.It hasbeensuggested that on the orderof 10% [Jakobsen et al., 1994]
of the water enteringthe Kattegatfrom the $kagerrakoriginatesfrom German
BightWatertransported by theJCC.If we assume that 10% of thewaterinflowto
theKattegatalsocontains 10% of the nutrientinputthen,in orderto effectuate a
10% increase in thetotalannualinputof nutrients to theKattegatovertheSkager-
rak border,the concentrations
in the JCC waterwould havehad to haveapproxi-
matelydoubled.Nitrate concentrations in the regionoff the north-westDanish
coastwhichis affectedby the JCC when it is presentare mostoften at the same
levelasor lowerthan(Figure12.4)thoseobserved in thewatersof the
Richardson 255
1000 tonnes N
4OO
/*"':*'"'...'
Commercial
fertilizers
300
2OO ,
Animal fertilizers
lOO
L.... ,,,,?'"• ..... I I I .... I

900 1920 1940 1960 1980 90
Figure12.5. The useof commercial

and animalfertilizersin Denmarkduringthe period
1900-1989 [DanishEnvironmental
Protection
Agency,1991].
trench(i.e. watersaffectedby the openNorth Seaand North Atlantic)whichalso

feedthe Skagerrak.Data are not availableto assess
whetheror not changes may
haveoccurredovertimein theorganicnutrientinputacross
theSkagerrak/Kattegat
border.
Thus,it seemsunlikelythatchanges in inorganic

nutrientinputcapableof support-
ingthe observed increase in primaryproductionhaveoccurred duringrecentde-
cadesat the bordersof theKattegatanditssurroundingseas.It isunclearfor both
the Skagerrak andBalticborders whetheror not changes haveoccurred in the
transport
of organic nutrientmaterial.
However,evenif theyhaveoccurred,
it
seemsunlikelythattheirmagnitude
wouldhavebeensufficient
to havecaused
the
recordedchanges
in primaryproduction.
On theotherhand,increases
in nitrogen
inputviarunoffandatmosphericdeposi-
tion havebeendocumentedto haveincreasedduringthis period[Hansenet al.,
1995].It hasbeensuggested
thatchanges
in agricultural
practice,
in particular
a
dramaticincrease
in the useof commercial
fertilizers(Figure12.5) maybe largely
responsible
forthisincrease
[Danish
Environmental
Protection
Agency,
1991].
2.5.Monitoringfor Eutrophication
Effects
Evidence
foreutrophication
ismostoftensought
inchanges
in nutrient
concentra-
tionsintheareabeing
studied.
Thus,
monitoring
programs
aredesigned
toidentify
changesinnutrient
concentrations
resulting
fromeutrophication.
Often,monitor-
ingislimited
tomeasurement
ofinorganic
nutrients.
Aspointed
outinthe
256 12. Conclusion,
Researchand EutrophicationControl
section,however,it is importantthat consideration

alsobe givento organicnutri-
ent concentrations.
Thereis a problemin tryingto identifythe extentof eutrophicationby examining

nutrientconcentrations in the water column.Basically,this problemarisesbecause
of the fact that oneis tryingto relatea statevariable(nutrientconcentration)to a
changein the rateof flux (of nutrients)to the environment.
An analogyherewouldbe tryingto comparethe sizeof bankaccountswith the ac-
countholders'salaries.It is often but not alwaysthe casethat the holdersof the
largestbank accountsare alsothosewith the largestsalaries.The rate at which
moneyis beingremovedfrom the accountis, however,alsoimportantin determin-
ing its sizeat any giventime. The sameis true with regardto nutrientconcentra-
tionsin the marineenvironment. In fact, eutrophicationeffectsare only observed
whenthe incomingnutrientsare incorporatedinto organicmaterial.Thus, if nutri-
entsare usedquicklyuponenteringthe marineenvironment,thereis the possibility
that a changein therate of deliveryto the systemwill neverbe reflectedin the con-
centrations observed in the water column.
Monitoringprogramsoftenattemptto overcomethis problemby focusingprima-

rily on thewintermonthswhenphytoplankton activityis minimaland not likelyto
belimitedby nutrients.Thus,it is arguedthat nutrientconcentrations duringwin-
ter monthswill be thosewhichare mostlikelyto exhibitchanges resultingfrom
changes in input. For a regionsuchas the Kattegat,however,measuringnutrient
concentrations duringthe winter and assumingthat thesenutrientsare directlyre-
latedto the phytoplankton activityand eutrophicationeffectsrecordedin the sum-
merand autumnis problematic.This is because water exchangein the regionis so
variable.Duringsomeyears,it occurssoquicklythat the nutrientsmeasuredduring
thewinterdo not remainin the systemlongenoughto affectproductionprocesses
later in the year. During other years,the nutrientsmeasuredduring the winter
monthsprovidea good indicationof the nutrientsavailablefor phytoplankton
growthlater in the year.
Eutrophication
can,then, theoreticallyoccurwithout necessarily
resultingin mea-
surablechanges
in inorganicnutrientconcentrations
in the watercolumn.
Mostmonitoringprogramsacknowledge the problemsassociatedwith usingnutri-
entconcentrations
asan indicatorof eutrophication and attemptto take accountof
nutrient"use"by includingmeasurement of phytoplanktonbiomass(chlorophyll)
and/orphytoplankton primaryproduction.Chlorophyllconcentration represents
anotherstatevariableof the system.Thus, the problemsassociated with using
chlorophylldeterminations
in assessing thecondition of theecosystem with respect
to eutrophication
are similarto thoseconfrontedwhen usingnutrientconcentra-
tions.Chlorophyll
measurements canbeusedasa proxyfor biomass presentat any
giventime.However,theytell little aboutthe productionand lossratesof biomass
withinthe system.
In theory,primaryproductionmeasurementswhichdescribethe conversionratesof
CO2to organicmaterialin the systemoughtto be a bettertool than biomass
Richardson 257
surements in identifying
eutrophicationeffects.Unfortunately,
however,mostof
themethods employed todayfor determiningratesof primaryproduction measure
total productionandareunableto differentiate
between"new"and"regenerated"
(sensu DugdaleandGoering[1967])production (seechapters1, 4 and5).
The ratioof newproduction (thatleadingto a netincreasein organicmatterin the
system)andregenerated production(basedon recycling of nutrientswithinthesys-
tem and not leadingto a net increase in organicmaterial)is not constant.Thus,
two identicalmeasuredvaluesof primaryproductionmay be associated with two
very differentnet productions of organicmaterial.Eutrophication effectssuchas
hypoxiaarethe resultof a net increasein theproductionof organicmaterialwithin
the system.Thus,oneshouldideallymeasurechanges in new productionovertime
in orderto monitorchangesin the ecosystem
resultingfrom eutrophication.
In openmarinesystems, new and regenerated production are traditionallydeter-
minedby measuring therelativeassimilation
by theplanktoncommunity of nitrate
andammonium[DugdaleandGoering,1967]using•SN.In suchsystems, thepres-
enceof nitraterepresentsan input from outsideof the system(usuallyvia up-
welling).Thus,nitrateassimilation
isassumed to giveriseto newproduction while
ammonium uptakerepresents regenerated
production. Aspointedoutby Dugdale
andGoering in theirseminalpaper,however,
thisapproach doesnotreadilylend
itselfto coastalmarinesystems because
of the difficulties
herein definingthe
boundaries of thesystem.
In coastal
ecosystems,
it isnotalwayspossible
to identify
nitrateand ammoniumashavingoriginated
respectively
fromoutsideandwithin
the system.Thus,application of the•SNmethodfor determining therelativepro-
portionsof nitrateandammonium uptake[Dugdale andGoering, 1967]doesnot
necessarily
identifynewandregenerated production in coastalsystems.
Although
thereare techniques that at leastpartiallycompensate for thisweakness in the
method,noneof themlendthemselves easilyto monitoring
studies.
New production
(netproduction
of organicmaterial)in aquaticecosystems
can
oftenbeapproximated by determining
sedimentation
rates(mostof theorganic
materialproduced in the systemis, ultimately,
deposited
uponthe bottom).
Initially,
onemightwonderwhysofewmonitoring programsrelated
totheidentifi-
cationof eutrophication
effects
actually
includemeasurementsof sedimentation.
Measurement
of sedimentation
ratesin shallowcoastalsystems
is, however,fraught
with technical
difficulties
(i.e.separation
of truesedimentation
fromresuspension,
cf.chapter
6) andreliable
methods
suitable
forroutine
usein monitoring
programs
arenot readilyavailable.
Oneapproach
thathasbeen
applied
withsome
success
in thestudy
of stratified
areasis the measurement
of sedimentation
•atesabovethe pycnocline
wheremea-
surements
will notbeinfluencedbyresuspension.
At present,
however,
thedeploy-
mentof sediment trapsis seldomincluded
asa partof routinemonitoring
pro-
grams.
Anobviousconclusion
hereisthatthere
isanurgent
needforthedevelop•
mentof goodmethods
whichcanbeused to determine
thenetproduction
occur-
ringinthephotic
zone
inorder
tobeabletomore
directly
monitor
ecosystem
ef-
fectsof
258 12. Conclusion,
Research
andEutrophication
Control
12.6.
The Reductionof Eutrophication'
PoliticalInitiatives
Althoughconcern overculturaleutrophication of marinewatersis a relativelynew
phenomenon, it has quicklygainedpoliticalinterest.A group representing the
Environmental Ministersfrom all countriesborderingthe North Seahas,for exam-
ple, identifiedculturaleutrophication as one of the major environmentalthreats
facingthis sea[North SeaTask Force, 1994]. In a seriesof Ministerial Declara-
tions,mostcountriessurrounding the North and Baltic Seashave, in principle,
agreedto reducing the culturaleutrophicationof thesewaterbodieswith nitrogen
andphosphorus by on the orderof 50% by the early2000s.
Denmarkhasbeenoneof themostprogressive nationswith respectto the introduc-
tion of legislation
designedto reduceculturaleutrophication and, in 1987, mea-
sureswereadoptedto reducenitrogenandphosphorus inputto surrounding waters
by 50 and 80%, respectively.This plan calledfor the reductionto be carriedout
withinfiveyears(i.e.by 1993}.Thegoalswith respect to phosphorus reductionand
nitrogenreductionfrom wastewater treatmentwere essentially met within this
timeframe.However,theplanwasnot successful in achieving
the desiredreduction
in runoffof nitrogen
fromagricultural
landandnewmeasures arecurrentlybeing
consideredfor thepurpose
of reducing
nitrogenrunofffromagriculture
to marine
areas.
Thesemeasures havebeenintroduced on thebasisof a generalpoliticalandpublic

awareness concerning thenegativeeffectsof excess culturaleutrophicationandthe
beliefthata reduction in nutrientinputswill benefittheenvironment. Our quanti-
tativeunderstanding of how culturaleutrophication affectsmarineecosystems is
stilllimited.In addition,the fieldof "recoverybiology"(i.e. how and underwhat
conditions doesa system"return"to its pre-eutrophied state?)is not well devel-
opedfor marineecosystems. Thus,it is difficultat thistimeto predictprecisely the
effectsof a 50% nutrient reduction on the environment.
Thefactthatthesegoalsfor nutrientreduction havebeenpoliticallyratherthansci-

entifically
definedhasevokedcriticism froma numberof circles.It is,however,im-
portantto notethatscience is onlyoneof the disciplinescontributing to political
decisions.Indeed,it hasbeenarguedthat sciencealoneoften "fails the environ-
ment"in that thetimerequiredto obtainthe "proof"requiredto establish cause
andeffectin a strictscientific
sense will preventthe opportunityfor intervention
whichmayaverttheoccurrence of anadverse effect[WynneandMayer•1993].
International
politicaldecisions
to reduceterrestrial
nitrogenandphosphorus in-
putsby 50% acrossthe boardalsoignorethefactthat not all countries
contribute
equallyto eutrophication
of internationalwaters.For somecountrieswhich con-
tributeonlyslightly
to cultural
eutrophication
onaninternational
scale,
thegoalofre-
ducing nutrientinputto themarineenvironment
by50% mayappearunreasonable.
Gray[1992],forexample,hasargued thecasefor a morestrategic
planfor reduc-
ingculturaleutrophication
to international
watersby usingthe exampleof
Richardson 259
way.Byhiscalculation,
Norwaycurrentlycontributes
0.5% of theculturaleutro-
phication
of nitrogen
to theNorthSea.Proposedplansforreducing
nitrogenand
phosphorusinputsfromNorwayareexpected to achievereductions
of 45-55%
and 20-30%, respectively,
and are estimatedto coston the orderof $2 billion.
Grayraises thequestionof whethersucha reduction on an inputthatrepresents
0.5% of thetotalanthropogenic
inputof nitrogento theNorthSeawill havea de-
tectable
effectontheecosystem.
Theimplication in Gray'sargument isthatthecost
implications
of sucha smallreductionare not justifiedin termsof theNorth Sea
ecosystem
as a whole.
It is importantto note,however,thatGray'spurpose in choosing thisexampleisto
illustrateproblemsrelatedto internationallegislation. He doesnot addressthe
questionof whetheror not the costimplications mightbe justifiedfor otherpur-
posesthanimprovement of the North Seaecosystem (i.e.improvement of localen-
vironmentalconditions in fjordsand near-coast
regions). While Graymaybe cor-
rect in his analysisof the limited potentialbenefitsof eutrophication controlin
Norway for the North Seaecosystem asa whole,a truecost-benefit analysisrelat-
ing to Norwegian (or any other) eutrophication controlprogramswould haveto
take all potentialbenefitsof the adoptedmeasuresinto consideration.
12.7. What Effect Will Remedial Actions Have?
Althoughthe nutrientreductiongoalsdescribed abovewerenot identifiedaloneon

the basisof scientificadvice,scientists
are the obviousadvisorswhenpoliticianstry
to anticipatethe effectsof remedialactions.As hasbeenpointedoutearlierin this
chapter,thescience of recovery biology(i.e.howa system respondsto a reduction
in eutrophication) is not yet well established.However,the few studiesthat have
beencarriedout in whichtheresponses of naturalmarinesystemsto a reductionin
eutrophication
havebeenrecorded
emphasize
thefactthat biological
structure
in
marinesystems
is stochastic.
Theexample of KertingeNor, Denmark(chapter10)demonstrates thestochasticity
of biological
systems verywell.Externalnutrientloadingto thissystemhasbeen
significantly
reduced in recentyearsandnutrient
releasefromthesediment hasbe-
comeimportant in determiningthebiological
structure
ofthesystem. In 1991,sedi-
ment releaseof P and N amountedrespectivelyto 3.3 and 0.4 timesthat coming
from externalsources.In 1992,P release
againamounted to justover3 timesthat
coming
fromexternal
sources
butN release
fromthesediment
wasovertwicethat
from externalsources.
This increased
N releasein 1992 wasthe resultof the decay
of a filamentous
algalmat.Thedifferencein N availability
duringthetwoyearsre-
sultedin the developmentof dramaticallydifferentpatterns
of primaryandsec-
ondaryproduction duringthetwo years.
Biological
systemsareinherently
unstableandextremeevents(weatherconditions,
algalblooms,
etc.)cananddoregularly change
thedirection
in whichthesystem
is
developing.
Thisinherentinstability
in biological
systemsmakes the
prediction
of theeffectof specific
actionson biological
structure
a formidable
task
indeed.Predictionof futureeventsor conditionscan only take placewith the help
of theoreticalor numericalmodels(seechapter11). Suchmodelscannot,however,
recreatethe stochastic
natureof the marineecosystem. While many includeterms
representing themajorprocesses occurringin the system, theseare mostoftenin-
troducedasconstants or asvalueschangingin a constantmanner.In reality,these
processes oftenvaryin theirmagnitude overshorttimescales andthe factorscon-
trollingtheirmagnitude arestillonlypoorlyunderstood (see,for example,thedis-
cussion in chapters
4 and5 of theinfluenceof windeventson sedimentation rates).
Thus,quantitative predictionof the effectsof a 50% reductionin the anthropo-
genicnutrientloadingto themarineenvironment is difficultat thepresenttime.
At a moregeneral level,however,it is possible
to predictthat a reductionin nutri-
entwill decreaseprimaryproductionand,thus,sedimentation of organicmaterial
whichwill reducethe probabilityof severehypoxiaevents.Hansenet al., [1995]
haveestimated thepotentialeffectof thevariouspoliticalinitiatives
to reduceeutro-
phicationin the Balticand North Season the oxygenconditionsin the Kattegat.
Theseworkerscreateda dynamicnumericalmodelwhich includeshydrographic
processes(bothadvective andvertical)aswell asdominatingprocesses in the nitro-
gencycle(N incorporation intonewproduction, bacterialregeneration of inorganic
N fromorganicanddenitrification). Inputof N to the modeloccursat the borders
to surrounding seas,via atmospheric input and from land runoff (distributed
aroundthe area).The modelis linked to the oxygenconditionsof the area and is
usedto simulateoxygenconditionsunder variableN-loadingconditions.Model
verificationwas conductedby comparingsimulatednitrogenand oxygencondi-
tionsduringthe 1980swith thoseactuallyobserved. Althoughmeasurements for
verificationof the modelusinginput conditionsfor the 1950s are limited, those
that do existsuggestthat themodelcan alsosimulateconditions at that time with
reasonableaccuracy.
The modelwasrun assuming
five differentscenariafor nitrogenreductionto the
system:
1. "1980s"'assuming averageloadingandh.ydrographic conditions

for the 1980s.
2. "1993": assuming the predictedloadingconditionsif the Danishlegislationof
1987 hadachieved itsgoalof a 50% reductionin land-based
loadingof N to the
KattegardBeltSea(seesection12.6).
3. "1996" where"1993" N loadingis furtherreducedby assuming a 50% reduc-
tion in land-based
N loadingfromNorth SeaandBalticcountries.This scenario
alsoassumes a 10% reductionin atmospheric NH4 depositionoriginatingout-
side of Denmark.
4. "2000" improves"1996" conditionsby assuming a further7% reductionin the
Danishcontributionto the atmospheric NH4 deposition(resultingfrom recent
Danishlegislation
relatingto theagriculturalsector).In addition,a general30%
reductionin NOx depositionis assumed.
5."20??"whereNOx deposition is reducedby 64% (i.e. to theminimumlevelcon-
sideredto betechnically
Richardson 261
N, mg 1-1 ,
200 6e•
5 .e5-
.
1O0 ' The
1980S 1993 1996 2000 20?? Scenario
Figure12.6. Maximumannualinorganicnitrogenconcentrationsat variousstationsin the

Kattegat/Belt
Seasassimulated
by themodeldescribed by Hansenet al. [1995]assuming
variousloadingconditions.
Seetext for description
of theloadingconditions.Positionsof
stations are shown in the inset.
02,
5
mg
'-1 - 4
•kage••.•
',• "'
//""'•;•'•'/Kattegat
•L.
7 6•
4
3
-• .
2 ' •e
1980s 1993 1996 2000 20?? Scenario
Figure12.7. Minimumannualoxygenconcentrations at variousstationsin theKattegat/Belt

Seasassimulated by themodeldescribed by Hansenet al. [1995]assuming variousloading
conditions.
Seetext for description
of loadingconditions.
Positionsof stationsareshownin
the inset.
All modelrunsassume that the biologicalprocesses

withinthe systemhaveadapted
to the new reducedN-loadingconditions.
The maximumconcentrations
of inorganicN in surfacewatersat severalstations
as predicted
by themodelassuming thevariousloadingconditions
areshownin
Figure12.6.All of thereduction scenaria
wouldleadto a reduction
in surfaceN
concentrations
according to the model.However,the mostpronounced effect&-
curs after a reductionin the local DanishN sources(i.e. "1993" scenario).Mini-
mumannualoxygenconcentrations in thebottomlayerat thesedifferentstations
werealsosimulated(Figure12.7) by the
2.8. Time Perspective'

When Will Remedial Actions Have an Effect?
An importantquestion in termsof eutrophication

controlis whenremedialactions
maybeexpected to havean effectuponthe ecosystem in whichtheseactionshave
beenapplied.Interannualvariabilityin the factorsregulatingnutrientinput and
turnoverin coastalmarinesystemmakesthis questiondifficultto answer.Nutrient
loadingvia runoffis, for example,a functionof the amountandtimingof precipi-
tation occurringover the catchmentarea (Figure 12.8). In areas with restricted
waterexchange, the influenceof localrunoff (meteorological
conditions)will gen-
erallybe morepronouncedthan in more openwaterswhere advectiveprocesses
dominatenutrientdelivery.Thus, year to year variabilityin oxygenconditionsin
coastalareaswith limited water exchangemay be greaterthan that observedin
moreopenwaters.This canbe demonstrated by examiningdata on the distribution
of hypoxiain theDanishLimfjord.Here,duringtheperiodfrom 1988 to 1994 where
remedialactionshavebeenin effectto reducenutrientinputto coastalwaters,the
areaof the fjordaffectedby hypoxiahasvariedfrom lessthan5 to over30% with
theextentof hypoxiabeinggreatest in 1988 and1994 (Figure12.9). Thus,positive
effectsthat may be expectedto result from remedialactionsdirectedtoward a
reductionof nutrientrunoffmaybemaskedby variabilityin thelocalmeteorologi-
calconditions
- especially
those
affecting
winterrainfall.
Interannualvariabilityin hydrographic patternscanalsoaffectthe extentto which
eutrophication effects(i.e. hypoxia)occursin a givenyear.Unusuallyhigh water
exchange ratesmayremovenutrientsfrom a givenareabeforephytoplanktonpro-
ductionandorganicsedimentation takeplace.Therefore,the highnutrientconcen-
trationsresultingfrom largeamountsof precipitationduringwinter months(cf.
Figure12.8) neednot necessarily resultin severehypoxiaconditions.Evenwhen
highlevelsof primaryproductionand organicsedimentation take place,strong
windactivityduringthelatesummerandautumnmonthscanreducetheprobabili-
ty of a severehypoxiaeventby mixingoxygeninto bottomwaters.
Similarly,unusuallycalm conditionsduringthe summerand autumnmonthscan
contributeto the developmentof extremehypoxiaconditionsevenwhen nutrient
input/primary production/organic
sedimentation havenot beenexceptionally high.
Giventhe numberof factorsaffectingthe development of eutrophication
effects
andtheinherentvariabilityassociated
with all of thesefactors,precise
predictionof
whenremedial
actions
canbeexpected
to elicita positive
response
in theecosystem
is difficult.
Anotherfactorwhichcomplicates the predictionof when the effectsof remedial

actions to reduceeutrophicationeffectsmightbeexpected to appearisthepotential
for internalpoolsof nutrientsto be storedwithinthe systemin sediments. Via this
mechanism, nutrients
can,in theory,be releasedfromsediment poolsandcontinue
to stimulate
highlevelsof primaryproduction
andorganicfalloutlongafterother
anthropogenic
sources
of nutrientsto the systemhavebeenreduced.Time series
Richardson 263
N concentration,IJmolI-•
12
ß93 86•81
11
/,•/0 88
10
9 085 • ø82
•84
8
ß 76
6
5
400 6(30 860 10'001'2'0014'00''16'00
Runoff, millionm3 month-•
Figure12.8.Winterconcentration (meanJanuary-February)of inorganicN in thesurface

layer(0-! 0 m) in thesouthern
KattegatandGreatBeltasa functionof winterrunoff(mean
December-February) fromDenmarkin the period1975-89.FromRichardson and•rte-
bjerg [1991].
%
35
3o
25
20
, <4mg
I-• .•
15
10
0 " '
1988 19•9 19•0 19•1 19•2 19•3 19'94
Figure12.9.Percentage
areain theDanishLimfjordannually
affected
byhypoxia
in theper-
iod 1988-1994. Data from The Countyof Viborg,Denmark,Environment
andTechnical
Department.
scribing
burialof N andP in sediments
arelackingfor mostcoastal
marineareas.
Thus,thedegreeto whichculturaleutrophication
mayhavealterednutrientburial
rates is unclear.
However,considerable
nutrientreserves
may be buriedin the sediment.It is esti-
mated(Christian
Christiansen,
pers.comm.)that 21,000tonnesof nitrogenand
6500tonnesof phosphorus
areburiedannually
in theKattegat proper(i.e.exclud-
ingtheBeltSeas).BoBarker
Jorgensen(pets.comm.)hasindependentlyestimated
nitrogen
burialintheKattegat
andBeltSeasto be25,000t yr-•. Muchofthisbur-
ial is recordedin the northernregionsof the Kattegat[Jorgensen
et al., 1990]
264 12. Conclusion,
Research
andEutrophication
Control
maybeassociated with sedimentation out of North Sea/Skagerrakwatersafteren-

teringthe Kattegat.Jorgensen
et al. [1990] estimatedthat nitrogenburialat a sta-
tion in theopenregionof theBeltSea(i.e.with strongcurrentconditions) repre-
sentson the orderof 1% of theannualphytoplanktonrequirementin thisarea.On
theorderof 30-40% of theannualphytoplankton requirement for nitrogenmay,
on the otherhand,be buriedeachyear in the northernKattegat.
Processes
relatingto nutrientreleasefrom sedimentsare still not well understood
(seechapters6 and 7). Thus,it is difficultto predicthow this nutrientreservoir
maycounteract eutrophicationcontrolmeasures. It doesseemclear,however,that
nutrientreleasefromsediments will alsovaryinterannually
dependingon oxygen
(redox)conditions,magnitudeof resuspension, mechanicaldisturbance of the bot-
tom (through,for example,fishingandgravelextractionactivities)etc.
Duringthe mostrecentyears,measurements of oxygenconcentrations in bottom
watersat somestationsin the Kattegathave beensomewhathigher than those
recordedduringthe 1950s.Proponents of the Danisheutrophication controlmea-
suresinitiatedfor thesewatersin 1987 argue,of course,that the apparentimprove-
mentis a directresultof theseactions.However,giventhe inherentvariabilityin
the system,it is not possibleon the basisof only a few yearsof data to establish
with statistical
certaintythattherehasbeena persistent changein the oxygencon-
ditionof the Kattegat.Thereis the very real possibility,evenif remedialactions
havehada positiveeffect,that yearswith low oxygenconcentrations duringsum-
mer months will still occur.
If oneassumes thatthevariances observed aroundtheregression line describing the

decrease in oxygenconcentrations observedin the southernKattegat over time
(Figure12.1) are an expression of the naturalvariabilityoccurringin the factors
regulatingnutrientturnoverhereand that thisvariabilitywill continuein the fu-
ture,thenit is possible
to calculatehow longa data time serieswould be required
in orderto demonstrate withan acceptable levelof confidence that a changein the
ecosystem hasoccurred. Let us,for the sakeof argument,hypothesize that the oxy-
genconcentrations duringthe late summerin the southernKattegatwill now be
constant(i.e. slope= 0) ratherthan decreasing as a resultof the remedialactions
takento combateutrophication. In otherwords,let us testa constantdecrease rate
of oxygendepletionagainsta constantoxygenconcentration (i.e. no furtherde-
creaseover time).
Statistical
analysis
of thishypothesis(assuhaingthat the levelof variationaboutthe
newlinewill beexactlythesameasthataroundtheoldline(Figure12.1))indicates
that21 yearsof data(Table12.2)wouldberequiredin orderto discriminate a con-
tinuednegativegradientof 0.050 mg 02 1-• yr-• (i.e.the slopeobserved in the line
describingoxygen concentrationsoverthelast30 years)asopposed to a zerogradi-
ent(slope)with 95% confidence. The usuallyaccepted significance
for thistypeof
erroris 80% [e.g.,Cohen,1988]whichwouldrequire18 yearsof data.Beingable
to detecta muchmorerapidratioof improvement (i.e.a gradientof _+0.100)with
80% confidence will require14 yearsof data.Evendetecting a gradientof_+0.100
withonly50% confidence will require11 yearsof
Richardson 265
TABLE 12.2.
Thenumber
ofyears
ofdata
required
toattain
thepower
shown
against
vari-
ousgradients
(inoxygen)
concentration
overtime
ina test
ofzero
gradient.
Forexample,
thetable
indicates
that21years
ofdatawould
berequired
inorder
tobe95%certain
that
wecoulddetectthatthegradient
(slope)
ofthelinedescribing
theoxygen
concentrations
in
thebottomwaterofthesouthernKattegat
during themonths
ofAugust-October
was0.05
mg021-•yr-•rather
than zero.
Analysis
conductedbyE.McKenzie,
Strathclyde
Univ.,
UK.
Power
Gradient 0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95
0.005 63 66 69 72 75 79 82 87 92 99
0.010 39 41 43 45 47 50 52 55 58 63
0.050 14 14 15 16 16 17 18 19 20 21
0.100 9 9 9 10 10 11 11 12 12 14
Proponents
andopponents oftheremedial
actionsthathavebeentakenagainst
eu-
trophication
effects
intheKattegat
areforced
to arguetheircases
atthemoment on
thebasis
ofdatatakenduringoneor,atmost,onlya fewyears.Fromthestatistical
analysispresented
above,however,it is clearthat thereare no immediate
answers
to the questionof whetheror not remedialactionsdirectedtoward a reductionof
hypoxiainthiscoastal
marine ecosystemhavehadthedesired
effect.
Realistically,
a
datasetof ontheorderof 20 yearswillprobably
berequired
beforescientists
will
withreasonableconfidencebeableto ascertain
whether
or notDanishlegislation
enactedin 1987 has reducedthe intensityof hypoxiaeventsin the southern
Kattegat.
The numberof yearsrequiredto obtainstatistical evidence for a changein the
ecosystem will varyfromsystem to systemdepending uponthe individualcharac-
teristics
of thesystem. However,asa general ruleforall coastal
marineecosystems,
immediatequantifiableeffectsof measures designed to reduceeutrophication
shouldnot beexpected. In mostcases, manyyearsof datawill berequiredin order
to identifywith statistical
certainlychanges
in theecosystem.
12.9.Science
and "Safe"Limitsof Eutrophication
In the Introductionto thisbook (chapter1), it wasarguedthat it is the responsibi-
lity of the scientificcommunityto developthe necessary expertiseto answerthe
questionsof politicians,administratorsand the publicat largeconcerning the ef-
fectsof culturaleutrophicationon the marineecosystem and to adviseconcerning
the relativevalueof variousproposedremedialactions.It shouldbeemphazised here,
however,that scientists cannotbe expectedto identifyand recommend coursesof
actionto combatculturaleutrophication in the absence of cleargoalsfor environ-
mental conditionsdesiredin a givenarea.
In flesh-watersystems,Vollenweider-type
empiricalmodelshavebeenemployed to
identify"acceptable"levelsof eutrophication
in specific
waterbodies(seechapters
1 and 11). This hasoftenbeeninterpretedas scientific
adviceconcerning
able"levelsof culturaleutrophication. It is importantto note,however,that while

theconceptof "acceptable"/"tolerable"/"safe" levelsof eutrophication
maybeuse-
ful in an administrativesense,it hasno real meaningin a scientificcontext.In order
to evaluatewhetheror not levelsof eutrophication can be consideredas "accept-
able",it is necessary to havedefinedqualitycriteriafor the conditionsdesiredin
theenvironment for whichacceptable limitsarebeingdiscussed. Suchqualityobjec-
tivesmustbe established politically.However,scientificinput is requiredin order
to identifyrealisticobjectives
andthe methodsthat may beusedto achievethem.
References
]Ertebjerg,G., Nitrate inflow from the North Seain 1989 (in Danish),ScientificReport
from the DanishEnvironmentalProtectionResearchInstitute,4, 109-111, Copenhagen,
1990.
Aure,J., E. $vendsen,F. Rey,andH. R. $kj61dal,The JutlandCurrent.Nutrientsand physi-
cal oceanographic conditionsin lateautumn1989, ICES CM90 C:35, 1990.
Cohen,J., Statistical
PowerAnalysisfor the BehaviouralSciences, 567 pp., ErlbaumAsso-
ciates,Hillsdale,New Jersey,1988.
DanishEnvironmental ProtectionAgency,Environmental impactsof nutrientemissions in
Denmark(in Danish),Reportfrom the DanishEnvironmentalProtectionAgency,1,203
pp., Copenhagen, 1991.
Dugdale,R. C., andJ. J. Goering,Uptakeof new and regenerated formsof nitrogenin pri-
maryproductivity,Limnol. Oceanogr.,12, 196-206, 1967.
Gray,J. S., Eutrophicationin the sea,in Marine Eutrophicationand PopulationDynamics,
editedby G. Colombo,I. Ferrari,V.U. Ceccherelli,and R. Rossi,pp. 3-15, Olsen &
Olsen,Fredensborg, Denmark,1992.
Hansen,I. S., G./Ertebjerg,and K. Richardson,A scenarioanalysisof effectsof reducedni-
trogeninput on oxygenconditionsin the Kattegatand the Belt Sea,Ophelia, 42, 75-93,
1995.
Hecky,R. E., andP. Kilham,Nutrientlimitationof phytoplanktonin freshwaterand marine
environments:a review of recent evidenceon the effects of enrichment, Limnol. Oce-
anogr.,33(4(2)), 796-822, 1988.
Heilmann,J.P., D. $. Danielssen,and O.V. Olsen,The potentialof the Jutland Coastal
Currentasa transporterof nutrientsto the Kattegat,ICES C.M. 1991/C:34, 1991.
Hinga,K. R., Alterationof phosphorus dynamicsduringexperimentaleutrophication of en-
closedmarineecosystems, Mar. Pollut. Bull., 21(6), 275-280, 1990.
Isaksson,I., L. Pihl,andJ. Van-Montfrans,Eutrophication-related changesin macrovegeta-
tion and foragingof youngcod (GadusmorhuaL.): A mesocosm experiment,]. Exp.
Mar. Biol. Ecol., 177(2), 203-217, 1994.
Jacobsen,T. $., Energyproductionby current and wind in the Great Belt (in Danish),
Havforskning fra Mil/ostyrelsen,
31,49 pp., Copenhagen, 1994.
Jakobsen,F., G../Ertebjerg,C. T. Agger,N. K. Hojerslev,N. Holt, J. Heilmann, and K.
Richardson, Hydrographic and biologicaldescriptionof the Skagerrakfront (in Danish),
Havforskning fra Miljostyrelsen,
49, 106 pp., 1994.
Jergensen,B. B., M. Bang,and T. H. Blackburn,Anaerobicmineralizationin marinesedi-
mentsfromtheBalticSea-NorthSeatransition,Mar. Ecol. Prog.Ser.,59, 39-54, 1990.
Larsson,
U., R. Elmgren,andF. Wulff, Eutrophication and the BalticSea:Causesandconse-
quences,Ambio,/4(1), 9-14,
Richardson 267
Maestrini,S.Y., andE. Gran•li,Environmental

conditions
andecophysiological
mechanisms
whichledto the 1988Chrysochromulina polylepis
bloom:an hypothesis,
Oceanol.
Acta
•4(4), 397-413, 1991.
North SeaTaskForce,NorthSeaQualityStatusReport!993, 132pp.OsloandParisCom-
missions,InternationalCouncilfor the Explorationof the Sea,Olsen& Olsen,Fredens-
borg,Denmark,1994.
Oviatt, C., P. Lane,F. French,and P. Donaghay,Phytoplankton species
and abundance in
responseto eutrophicationin coastalmarinemesocosms, J. PlanktonRes.,••(6), 1223-
1244, 1989.
Richardson, K., and G. œrtebjerg,Nitrogen,phosphorus,
andorganicmaterialin the ter-
restrialand marineenvironment,in Reportfrom a ConsensusConference
(in Danish},
DanishMinistry of Educationand Research,1991.
Richardson,K., and J.P. Heilmann,Primaryproductionin the Kattegat:pastand present,
Ophelia,41,317-328, 1995.
Smetacek,
V., U. Bathmann,E.-M. N•Sthig,andR. Scharek,Coastaleutrophication: causes
and consequences,
in OceanMargin Processes in GlobalChange,editedby R. F. C.
Mantoura,J.-M. Martin, andR. Wollast,pp. 251-179,JohnWiley& Sons,Chichester,
1991.
Steemann Nielsen,E., Theuseof radio-active carbon(CTM)for measuring
organicproduction
in the sea,J. Cons.Intl Explor.Mer., 18, 117-140, 1952
Wynne,B., andS. Mayer,How science
failstheenvironment,
New Scientist,
I38, 33-35,
Index
Abra alba 171 hypoxia 161-171
Acartia 108 organicdeposition 158, 172
ACDEP model 42-46 time series 159, 171
Acid aerosol 28 Biologicalmodel 236
Activitycoefficients
in seawater 41 Biological
oxygendemand(BOD) 95
Aerodynamicresistance 36 BlackSeahydrography 51-53
Aerosolparticles 21, 32-34, BosporusStrait 51-53
37-39 Bottomfauna(seealsobenthos) 14, 155, 158
Air-seagastransfer 39-42 Boundarylayer,atmospheric 37
Algal blooms 9-13 Brittle stars 158
Amino acids 127-128
Ammonia (NH3) 21 C-14method 97,111,245
atmospheric
chemistry 28 Carotenoid 105
atmospheric
deposition 42-44 Centropagus 108
atmospheric
emission 23-24 Ceratium 140
Ammonium (NH4*) 21, 42-44 Chaetomorpha
linum 194,
in sediment 128, 149 210-212
uptakein macroalgae 191 Chemicaloxygendemand(COD) 12
Amphiurafiliformis 163, 171 Chrysochromulina
polylepis 12, 85
Anaerobiosis in benthos 163-165, Chlorophyll 103-105,
167-168 108, 212
Anoxia, definition 13 Ciliates 98
Aphoticzone 2 Ciona intestinalis 216
Arctica islandica 162, 164, Circulation model 62
170, 171 Cladophora 194
Ascidians(seeCiona} Clouddroplets 32-34
Astarte borealis 162, 164, C:N ratio 100, 149
170 Coastaleutrophication 234
Atmosphericchemistry 28-29 Coastalzoneas nutrient filter 181,186
Atmosphericdeposition 22, 42-46 Cod 156-157
Atmosphericemissions 23-27 Continuityequation 54
Atmospherictransportmodel 22, 42-46 Copepods 85, 86,
Atmosphericturbulence 30, 34-35 107-111
Aurelia aurita 214 Copepodeggproduction 107-111
Coriolis force 57, 61
Bacterial
consumption 98 C:P ratio 149
Bacterialproduction 74-76, 141 Crangoncrangon 162
Baltic Sea Crustaceansand hypoxia 161-170
atmospheric
deposition 45 Current,cyclonic 61
benthos 170
map 16 Dab 156
model 237 Danish Straits 57-65
oxygendepletion 170 Dark respiration 97
water exchange 59-60, 250 Denitrification 123-124,
Baroclinicand barotropicflow 57, 63 128, 150,
Barotropicgradient 51 182, 184-185
Beggiatoa 126, 130 Denmark
Benthicmacrophytes(seemacrophytes) atmospheric emissions 24-27
Benthicmicroalgae 185 atmosphericdepositions 43-46
Benthos Densityof seawater 55
biomass 171-172 Deposition,net vs.gross 118
diversity 170-172 Diatoms 86, 140
effect on denitrification 185 siliconlimitation 7, 237-239
growth 160 Diffusion
H2Stolerance 162, 170 limitation 69-71
270
Diffusion H aemocyanin
andhypoxia 168-169
transport 121,144 Halocline 13
Diffusiveboundarylayer 121 Henry'slaw 31,41
Dinitrogenpentoxide(N2Os) 21 Heterotrophicbacteria 74
Dinofiagellates 140 Heterotrophicdinofiagellates 86
Dinoflagellate
cysts 10-11 Hydrogensulfide(H2S) 130-132, 146
Dissolvedorganicmatter(DOM) 74-77 H2Stoxicity 162, 170
Dissolvedorganicnitrogen(DON) 127-128, Hydrographicbuoy 96
149,249 Hydrographicmodels 64
Dry deposition 22, 34-42 Hydrography
bay 138-140
Echinocardium
cordatum 163, 171 fjord 205-208
Eelgrass 194, 212 Hypertrophic,definition 2
Electronacceptors 123 Hyperventillation 168
Elementalcomposition
of algae 5 Hypoxia 14
Elementcycling 151 bottom fauna 14, 161-165
Entrainment 53, 56-57, definition 13, 95
79, 85, 109 distribution 17, 95, 140,152,
Estuary,circulationandmixing 227 170-171,263
Euphoticzone 2, 100, 105 time series 245-246,
Europe,atmospheric emission 23, 25 262-265
Eutrophic,definition 2
Eutrophication Intrusion 107
benthos 158-161,172 Ionicstrengthof seawater 41
cause 95-96, 246 Iron in sediments 123-125, 146
definition 1 Iron sulfide 146
geographicdistribution 6-7, 95 Isefjord 82
historyanddevelopment 4, 95,
111-112,180, Jellyfish
(see
Aurelia)
246-255 JutlandCoastalCurrent 251
lakes 5
marine vs. fresh-water 4-6, 243-244 Kattegat 95-112
model 5, 8 atmosphericdeposition 43-46
sediments 130-132 eutrophication 248-255
Exudation of DOM 76-77 hypoxia 17, 95, 171,
245-246
Fertilizers 23, 255 map 16
Filamentous
algalmats 210-212 model 260
Fishproduction 8-9 phytoplankton
bloom 86
Fisheries
andeutrophication 8, 14, sedimentation 80, 84
156-157, 171 Kattegat/Skagerrak
front 87
Fjordmodels 231
Fjords 229-233 Lake models 226
Floatingmacroalgae 194 Liebig'slaw 226
Fluorescence 110, 139 Lightlimitation
Food chain 85 benthicmacrophytes 194
Food web 87 phytoplankton 72-74
Forcingfunctionsof models 224 Little Belt 58
Fossil fuel 25 Luxuryuptakeof nutrients 227
Fossil record 12
Fronts 87 Macrophytes
Fucus vesiculosus 190 competition
with phytoplankton187-188, 219
depthpenetration 194-195
Gassolubility 31-32 growthrates 189-192
Gelbstoff 61 internal nutrient concentration 190 ,
Glycolysis
duringanaerobiosis 167 Manganesein sediments !23-125, 146
Grazing 85-87, 98 Map of BalticSeato North Sea 16
Great Belt 58 Marine snow 75,
Author Address List Bo BarkerJorgensen
Max Planck Institute
for MarineMicrobiology,
FredeOstergaard Andersen Dept.of Biogeochemistry
OdenseUniversity Fahrenheitstr. 1
Instituteof Biology D-28359 Bremen
Campusvej55 Germany
DK-5230 Odense M
Denmark
LarsKamp-Nielsen
FreshwaterBiological
Laboratory
WilIem A. H. Asman University
of Copenhagen
National EnvironmentalResearchInstitute Helsing•rgade51
Frederiksborgvej
399, DK-3400 Hillemd
P.O. Box 358 Denmark
DK-4000 Roskilde
Denmark Thomas Kiorboe
Danish Institute for Fisheries Research
JensBorum Charlottenlund Castle
Freshwater BiologicalLaboratory DK-2920 Charlottenlund
Universityof Copenhagen Denmark
Helsingorgade51
DK-3400 Hillerod Soren E. Larsen
Denmark Dept.of Meteorology
andWindEnergy
RisoNationalLaboratory
Lars Hagerman P.O. Box 45}
Marine BiologicalLaboratoratory DK-4000 Roskilde
Universityof Copenhagen Denmark
Strandpromenaden 5
DK-3000 Helsingor JacobSteenMoller
Denmark DanishHydraulicInstitute
AgernAlI• 5
Jorn NorrevangJensen DK-2970 H•rsholm
National Environmental Research Denmark
Institute
Frederiksborgvej
399 Katherine Richardson
P.O. Box 358 Danish Institute for Fisheries Research
DK-4000 Roskilde Charlottenlund Castle
Denmark DK-2920 Charlottenlund
Denmark
Alf B. Josefson
National Environmental Research Hans Ulrik Rii•gaard
Institute Instituteof Biology
Frederiksborgvej
399 OdenseUniversity
P.O. Box 358 Campusvej55
DK-4000 Roskilde DK-5230 Odense M
Denmark Denmark
CarstenJiirgensen Andr• W. Visser

Countyof Fyen Danish Institute for Fisheries Research
Orba=kvej100 Charlottenlund Castle
DK-5220 Odense SO DK-2920 Charlottenlund
Denmark

Eutrophication in Coastal Marine Ecosystems

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Eutrophication in Coastal Marine Ecosystems

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Coastal and Estuarine Studies

Bo Barker Jorgensen and

American Geophysical Union

Pdnted in the United States of

3 Water Masses, Stratification and Circulation

5 Carbon Flow in the Water Column Case Study:

6 Material Flux in the Sediment

7 Case Study--Aarhus Bay

10 Case Study: Kertinge Nor

12 Conclusion,Researchand Eutrophication Control

INDEX ............................................................................................. 269

LIST OF CONTRIBUTORS ..................................................................

Overthe last 10-20years,eutrophication

While conceivedwithin and partially supportedby a Danish researchprogram,

"Eutrophication" of coastalmarinewatersis a muchdiscussed topic- bothin the

Eutrophicationin CoastalMarine Ecosystems

Oligotrophic < 100

marinecoastaland estuarineecosystems basedon the primary productionoccur-

Eutrophication canoccuras a resultof naturalprocesses. It occurs,for example,

Whetheror not eutrophicationis occurringnaturallyor as a resultof anthro-

Most of our understandingof nutrient limitation of phytoplanktoncomesfrom

For somepurposes, for example,it canberelevantto consider nutrientlimitationat

between newandregenerated production.Thus,an increase in themeasuredprimary

the limnologicalliterature.However,there are essentialdifferences

Element River Algal Ocean

C 738 102 1,000

It shouldbenotedthattheHeckyandKilhamanalysis alsoincludeda comparison

at leastpotentially,affectcarboncyclingprocesses occurringin the sea.Thus,while

The increasedplantbiomassresultingfrom eutrophicationwill giveriseto sec-

Figure1.2. Development in the annualoccurrences

southernNorth Seahave,for example,oftenbeenattributedto culturaleutrophica-

Figure!.3. Sedimentologicalsectionmadefroma regionon Bornholm, Denmark,showing the

Thus,whatwasinteresting aboutthisbloomwasthe fact that a singletoxic species

toxicphytoplanktonbloomsisa resultof thefactthattheseorganisms

Themostimportantsourcesof oxygento bottomwatersaredown-mixing (usually

andbottomwater)playan importantrolein determining

Figure1.4. Catches(kg trawl h-1) of the Norwegianlobster(Nephropsnorvegicus)

The Kattegatrepresents the transitionareaseparatingthe Balticfrom the $kagerrak

Figure1.6. Distributionof hypoxia(< 3 mg 02 !-1) in theKattegatin 1988[HELCOM,

surfaceoutflow is driven by fresh-waterinput to the Baltic.Thus,the surface

Nitrogenand phosphorus can be limitingfactorsfor algalgrowthin the marine

- The NHx group:gaseous

Eutrophicationin CoastalMarine Ecosystems

The atmospheric nitrogeninputis causedby two processes:wet deposition,which

Atmospheric depositionto theseais noteasilymeasured. Althoughconcentrations

...... . .... * ......

25 .'-"".".•"-.'".'..'*- ".: .'"--'2 2-' •"--'*- ßß.

'2--: :•---- ....

II• above 6.00

.:• 0.00 - 1.00

6255 :{{•::'•:...:{•:••)•L::: .......... ": ........

The NH3 emissionrate is generallyhigherduringdaytimethan duringnighttime,

15- :::i . :"/•J), above 6.00

•o• ,D..M.U-774 .........

playa role in the atmospheric chemistryof nitrogencompounds like S02 andhydro-

Compounds are chemically convertedthroughatmospheric reactions.Each com-

UnderWesternEuropean conditions, mostNH3 will reactwith acid aerosol,e.g.

Here,the changein concentration

Solubilityof Gasesin Water

Compound H -AH/R Reference

TABLE 2.2. Dissociation:

Compound K -A H/R Reference

The flux of gasesintodropletscanbe described

------(%- Cw*) (7)

25 .'-"".".•"-.'".'..'- ".: .'"--'2 2-' •"--'- ßß.