Barnes - Review Oceanography and Marine Biology

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OCEANOGRAPHY
and
MARINE BIOLOGY
AN ANNUAL REVIEW
Volume 46
Editors
R.N. Gibson
Scottish Association for Marine Science
The Dunstaffnage Marine Laboratory
Oban, Argyll, Scotland
robin.gibson@sams.ac.uk
R.J.A. Atkinson
University Marine Biological Station Millport
University of London
Isle of Cumbrae, Scotland
r.j.a.atkinson@ millport.gla. ac. uk
J.D.M. Gordon
Scottish Association for Marine Science
The Dunstaffnage Marine Laboratory
Oban, Argyll, Scotland
john. gordon@ sams.ac. uk
Founded by Harold Barnes
ｾ＠ CRC Press
V Taylor & Francis Group
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Contents
Preface v
Use, abuse, misconceptions and insights from quota models - the Droop cell quota
model 40 years on
Kevin J. Flynn
Effects of benthic algae on the replenishment of corals and the implications for the
resilience of coral reefs 25
Chico L. Birrell , Laurence J. McCook, Bette L. Willis & Guillermo A. Diaz-Pulido
Autecology ofCrangon crangon (L.) with an emphasis on latitudinal trends 65

Joana Campos & Henk W. van der Veer
Biology of the planktonic stages of benthic octopuses 105

Roger Villanueva & Mark D. Norman
The ecological and evolutionary importance of maternal effects in th_e sea 203
Dustin J. Marshall, Richard M. Allen & Angela J. Crean
Effects of climate-induced coral bleaching on coral-reeffishes- ecological and

economic consequences 251
MorganS. Pratchett, Philip L. Munday, Shaun K. Wilson, Nicholas A.J. Graham, Joshua E.
Cinner, David R. Bellwood, Geoffrey P. Jones, Nicholas V.C. Polunin & Tim R. McClanahan
Otolith chemistry to describe movements and life-history parameters offishes:

hypotheses, assumptions, limitations and inferences 297
Travis S. Elsdon, Brian K. Wells, Steven E. Campana, Bronwyn M. Gil landers, Cynthia M.
Jones, Karin E. Limburg, David H. Secor, Simon R. Thorrold & Benjamin D. Walther
Paradigms in fisheries oceanography 33 L

William C. Leggett & Kenneth T. Frank
Author Index 365
Systematic Index 399
Subject Index 407

Preface
The 46th volume of this series contains eight reviews written by an international array of authors
that, as usual , range widely in subject and taxonomic and geographic coverage. The editors wel-
come suggestions from potential authors for topics they consider could form the basis of appropri-
ate future contributions. Because an annual publication schedule necessarily places constraints on
the timetable for submission, evaluation and acceptance of manuscripts, potential contributors are
advised to make contact with the editors at an early stage of preparation. Contact details are listed
on the title page of this volume.
The editors gratefully acknowledge the willingness and speed with which authors complied
with the editors' suggestions, requests and questions and the efficiency of CRC Press in ensuring
the timely appearance of this volume.
Oceanog raphy and Marin e Biology: An Annual Review. 2008, 46, 1-23
© R.N. Gibson, R. J. A. Atkinson, and J.D. M. Gordon, Editors
Taylor & Francis
USE, ABUSE, MISCONCEPTIONS AND INSIGHTS

FROM QUOTA MODELS- THE DROOP
CELL QUOTA MODEL 40 YEARS ON
KEVIN l FLYNN
Institute of Environmental Sustainability, Wallace Building, Swansea
University, Singleton Park, Swansea SA2 8PP, Wales, UK
E-mail: K.lFiynn@swansea_ac.uk
Abstract The Droop cell quota model is the most cited model of phytoplankton growth, even
though many pay scant regard to the original description and to its limitations for the description
of the interactions that define phenotypic plasticity. While the mechanistic basis of the concept and
most ecosystem applications of quota models are C based, much experimental work is cell based,
and most theoretical studies ignore the important differences between cell and C nutrient quotas.
The future application of the quota approach would be enhanced by the adoption of a normalised
quota ("Quota) description, employing a dimensionless constant (KQ) to define the response curve,
rather than using the original fixed-curve form. Establishment of the range of these KQ values for
different phytoplankton species would limit the number of free parameters in ecosystem variants of
quota models while recognising the importance of curve shape for phenotypic variation. KQ for N
is typically >3, while for Pit is typically <0-2. In addition, appropriate control linkages are required
to regulate nutrient transport to the quotas of limiting and non-limiting nutrients _ Together, these
would enable the establishment of a more coherent quota-based description of algal growth more fit
for the development of plankton functional-type models.
Introduction
The Droop quota model was first publi shed in 1968 (Droop 1968), spawning not only applied
applications but extensive theoretical analyses over the following 40 yr. The driving concept of the
model, that organism (specifically phytoplankton) growth is first and foremost a function of inter-
nal nutrient availability, contrasts with the Monod (1942, 1949) description of microbial growth ,
which relates growth simply to external resource availability. Perhaps ironically, given that both the
works by Monod (1942, 1949) and Droop (1968) were based upon steady-state chemostat studies,
the interface between these contrasting approaches is of most potential value in dynamic situations
(Droop 1975), where organism growth can continue (as allowed by the remaining internal resource)
in the absence of sufficient external resource. More recently, with the increasing appreciation of the
importance of stoichiometric differences between consumer and food (Sterner & Elser 2002), the
quota model has found an additional role for the description of how phytoplankton prey stoichio-
metry varies with nutrient status (e.g., Mitra & Flynn 2006).
Without doubt the work of Droop (the original paper cited now in excess of 330 times) has made
a profound impact on our science. Indeed, sometimes the cell quota model is referred to simply
as the Droop equation (e.g., Borchardt 1994, Oyarzun & Lange 1994, Pascual 1994), just as the
Monod equation carries the name of its originator. The history of the quota model, and of the initial
KEVIN J. FLYNN
experiments of Droop, is described by Leadbeater (2006). However, the quota model represents but
a small part of the prodigious research output of Droop and his coworkers. Indeed, the quota model
itself almost seems like an aside in the complex (and well worth reading) story of the vitamin 8 12
nutrition of the microalga Monochrysis (Droop 1968). Alas, most of the works by Droop still remain
to be digitised and are thus not as readily available to a global audience as they should be.
The aim of this review is not to consider technical aspects or detailed results but to consider the
uses of the quota approach subsequent to Droop's work, to draw attention to some of the abuses and
misconceptions, and to consider insights from the mathematical analyses of quota-type constructs
as they pertain to the current development of phytoplankton models.
The quota description

The Droop quota model originated as a purely empirical description of the relationship between the
cell quota (an amount of a resource within a cell, hence 'cell quota') and the organism 's steady-state
growth rate. The original work was conducted with reference to vitamin 8 12 , later extended toP, and
then even to light (Droop et al. 1982). To differentiate the Droop description type from any others,
it will be accorded the term 0 Quota from hereon. The original parameter names are not used here
because kQ (etc.), used to signify the subsistence quota by Droop, is confusable with the Michaelis-
Menten/Monod half-saturation constant k. The 0 Quota description is thus
(I)
where l1max' is the theoretical growth rate at infinite quota, Q, ;, is the minimum (subsistence) quota,
Q is the current quota, and 11 is the resultant growth rate. The curve varies in shape over realistic
values of Q and 11 with the values of Q,;, and ＱｾｷｸＧﾷ＠
Quotas were originally reported of nutrient per cell , although in later works nutrient:joule quo-
tas were used (Droop et al. 1982), which could be considered as akin to nutrient:C quotas. There
are some important differences between cell- and C-based nutrient quotas, which are considered
further below. However, the concept that growth rate varies with the value of the internal nutrient
quota remains the same.
To normalise the 0 Quota curve, making the value of 11"wx' meaningful , such that when Q attains
the maximum value Q""'.r then 11 = l1ma.r' the Droop description can be rewritten as
(2)
The relative growth rate 11rcl is thus given by
(3)
From the form of the 0 Quota description in Equation 2 it can be seen that the curve becomes increas-
ingly hyperbolic as the ratio Q,a... :Q,;" increases. From a physiological point of view then , the
2
USE, ABUSE, MISCONCEPTIONS AND INSIGHTS FROM QUOTA MODELS
expectation is that a nutrient that can be accumulated to high relative concentration (such as vitamin
8 12 and P) can be essentially amassed in a form that does not affect growth. Excess P, for example,
may be accumulated as polyphosphate in certain microbes (e.g., Rhee 1973, Watanabe et al. 1987) so
that Q,11.. :Q, ;, may easily exceed 10. In contrast, N, which cannot be accumulated in an inert state,
does not display such a wide quota range (for N, Q,uu:Q,;, =ca. 4) and accordingly one may expect a
flatter relationship between the quota and growth rate, as the Droop model indeed describes.
There are various other quota-type descriptions in the literature. The curve attributed to
Caperon & Meyer (1972) contains an additional parameter, Kq, which allows the form of the curve
(Equation 4) to be altered independently of the ratio of Q,w.. :Q,;,· Another constant ().!, 11.." ) , akin to
!lmax' in the Droop formulation, is used as a scaling constant to describe).!.
(Q-Qmin)
(4)
The similarity between Equation 4 and that describing Michaelis-Menten enzyme kinetics is
apparent; the quantity Q- Q,;, equates to the concentration of the growth-limiting substrate, with
Kq analogous to the half-saturation constant for the process. However, the shape of this hyperbolic
curve when Q::; ｑＬＢＧｾＢＧ＠ can be varied from being effectively linear (Kq and !lmax" very large), to a true
rectangular hyperbola (Kq small, and !lmax" tending to !lmax).
Equation 4 can be normalised (Flynn 2002) to remove !lmax", allowing the direct use of !lmax• so
yielding the description given in Equation 5. This normalised quota description is termed "Quota
from hereon.
_ (1 + KQ) · (Q-Qmin) (5)

).! - J..Lmax · (
Q- Qmin ) + KQ · ( Qmax - Qmin )
Constant KQ is dimensionless, unlike the value of Kq in Equation 4, which has the same dimensions
as the quota. KQ must not be confused with Kif (cf. Baklouti et al. 2006). The value of KQ sets the
curve form irrespective of the unit basis (cell or biomass) or of the numeric range of Q,;, and Q,"..
(Figure 1). Values of KQ exceeding 10 give linear relationships (Figure I A).
Figure I B shows the relationship between Q,"'x:Q,;, and the value of KQ (KQeq"i") that allows
the original Droop model ( 0 Quota) and "Quota descriptions to yield the same values of ll· The value
of KQ required to obtain equivalence is
QillaX
[ Qmm
-Il-l (6)
While the 0 Quota description (Equation 2) has a curve form set by the ratio of Q,11 x:Q,;, (and which
becomes linear as Q,wx: Q,,;, approaches unity), "Quota (Equation 5) can describe any curve from
linear to rectangular hyperbolic irrespective of the value of Q,,11.. :Q,;,· The simplicity of the 0 Quota
equation (three constants) versus "Quota (four constants) is thus bought at the cost of a lack of flex-
ibility. However, as considered below, it may be possible to constrain KQ for a given nutrient type
and so remove a free variable.
Cell versus biomass quota descriptions

Original emphasis on quota experimentation centred on the cell quota. It can be argued that the
cell (organism) is the central unit of life and thus warrants its position as the quota base. Although
3
KEVIN J. FLYNN
1.0 10
0.8
0.6
0.4
0.1
0.2
Qmin'Qmax = 0. 2 0.01
0.0
10 100
0.0 0.2 0.4 0.6 0.8 1.0
Q:Qmax
(B)
(A)
Figure 1 The shape of the normalised quota ("Quota) curve (Equation 5) with different values of KQ (A).
At the value of Qmax:Q,.,;, used (5; Q,.,;,:Q"'"' =0.2), the shape of the Droop quota ( 0 Quota) curve is given when
KQ =0.25 (bold line). Panel B shows the value of KQ required (KQ•qai••; Equation 6) for the "Quota equation to
give the same shape as a 0 Quota curve (Equation 2) at different values of Q,., 0 _..:Q,.,;,·
there is a long history of studies of size-related phytoplankton physiology (Banse 1976, Blasco et al.
1982), and there may be various general trends relating cell size to activity and growth rates, intra-
cellular biochemistry will be most closely related to the concentration of material available within
the cell, and hence to biovolume, which equates to carbon (C). Cell-size-scaled functions are most
closely related to the passage of material and energy into the cell. As the whole basis of the quota
concept is that internal rather than external nutrient concentrations regulate growth, it appears to be
more logical to describe quotas in terms of C.
Cell-based quota relationships are also inevitably skewed by the fact that cell size varies with the
cell cycle and with various environmental and physiological factors. P-deprived cells may be larger
or alternatively of similar size to P-sufficient cells (Lehman 1976, Gotham & Rhee 1981 , Elrifi &
Turpin 1985, John & Flynn 2002), while N-deprived cells are typically smaller (e.g. , Davidson et al.
1992, Wood & Flynn 1995). This complicates the interpretation of other issues, such as changes in
the quota of non-/lesser limiting nutrients as a function of limiting nutrients (e.g., Elrifi & Turpin
1985). Droop et al. (1982), using calorimetry to derive Joules cell- 1 (and assuming here thatjoules:C
is constant), noted no variation in cell size with light- or indeed with vitamin 8 12-limited growth,
although they did warn about problems of comparing cell and biomass quotas. Others have noted
changes in cell quota with light (Zevenboom et al. 1980, Falkowski et al. 1985, Healey 1985) as well
as with temperature (Goldman 1979). Zonneveld et al. (1997) modelled changes in cell size in light-
limited algae. Different combinations of factors affecting cell size will then affect the packaging
effect of the photosynthetic apparatus (e.g., for diatoms; Taguchi 1976) while nutrient stress will
further affect C fixation, all of which generates additional problems (Liu et al. 2001).
The term 'cell quota model' is ambiguous, which is unfortunate given that quota models based
on different units are not necessarily comparable. Some, like Spijkerman & Coesel (1998), specifi-
cally use the term 'cellular quota' to indicate that the quota used is on a cell basis. Armstrong (2006)
refers to a 'nitrogen cell quota' and then assigns units of N:C. The 'carbon quota model' could also
4
be considered ambiguous because it could (and usefully) be referring to the amount of C within a
cell. The simplest solution is perhaps to refer to the units in the title of the model ('nutrient-C quota
model' ; 'nutrient-cell quota model').
There are rather few occasions where a model refers to both C- and cell-based quotas. Usually
this is done to accommodate specific requirements, notably simulating changes in cell size (Flynn
& Martin-Jezequel 2000, Flynn 2001) and changes in cellular concentrations such as toxins (John &
Flynn 2002, Davidson & Fehling 2006). Through the use of X-ray microanalysis it is now possible
to determine C:N:P for individual cells (Heldal et al. 2003). However, while biochemically based
models need quotas in terms of a biochemical base (typically C), in the simu lation of lag phases,
where cell-cycle events may be important, operating with a cell quota model may help (Cunningham
& Maas 1978, Davidson et al. 1993, Davidson & Cunningham 1996).
If one accepts that, mechanistically, the quota description is best considered ·on a C rather than
cell basis, then individual-based models describing the activity of plankton in Lagrangian scenarios
(Woods & Barkmann 1994) should couple cell and C quota descriptions. Relying on a cell quota
description of growth for what may well be synchronised populations of cells could lead to signifi-
cant errors because cell sizes (and hence for example N:cell) vary 2-fold during their cell cycle; this
2-fold variation over the cell cycle is a large fraction of the 3- to 4-fold variation expected in N:C in
N-starved compared with N-replete cell suspensions.
Ideally, then, a coupled C-cell structure is desirable, the C:cell relationship affecting resource
acquisition, whereas the nutrient:C quota affects internal biochemical dynamics. Ultimately,
however, and perhaps most importantly for the selection of C-based over cell-based formulations,
the vast bulk of ecosystem models use biomass as the main unit, and not organism numbers.
Unfortunately, most traditional quota experimentation was cell based and conversion between
cell and biomass bases is not easy. The result is a large literature of data (little of which involves
marine species of ecological importance) reporting various combinations of Q111 ; 11 , Q,"'·" K" (these
three terms usually in terms of cell s), Q"'"-':Q,;,, llmax• and so on, but which are not readily usable for
transforming into other units or quota formats. The form of the quota curve may thus be expected to
vary (and will be shown to do so below) depending on growth conditions and on whether the basis of
the quota is cell or C (or any other unit, such as dry weight). In the following, to differentiate between
different specific values of KQ (as used in "Quota, Equation 5) these will be identified by subscript;
such as KQ,.,11 , KQc or KQJryueixht for cell, Cor dry weight quota-specific values, respectively.
There are few datasets available for making simultaneous comparisons of cell quota and C
quota models , and even fewer for multinutrient applications (e.g., Elrifi & Turpin 1985, Liu et al.
2001 , John & Flynn 2002). Figure 2 shows data reconstructed and transformed from figures shown
in Elrifi & Turpin (1985) for the freshwater chlorophyte Selenastrium. Note the variation in cell
size with nutrient status (Figure 2E; a feature that Elrifi & Turpin (1985) played down), that NKQ
> PKQ, and KQ," 11 < KQc- One of the most interesting features is that with P limitation N:C falls
(Fig ure 2C), while with N limitation P:C increases (Figure 2D); the pattern in cell-specific quotas
(Figure 2A,B) is different because of the variation in cell size (Figure 2E). An explanation for the
variation inC-specific quotas (Figure 2C,D) is sought in the section on nutrient transport regulation.
The similarity between the relationships of growth rate vers us Chl:C for N-and P-limited growth
(Figure 2F; see also Liu et al. 2001) is consistent with the demand for C controlling the synthesis of
the photosystems, and hence chlorophyll (Flynn 2001).
Figure 3 shows the fit of cell- and C-based "Quota models of Nand P limitation to the batch
culture data for a dinoflagellate. Both models fit the data but, because of the changes in cell size
during P stress (Figure 3E), the shape of the quota curves is different (note the different values of
PKQ"" and PKQc). That P-limited cells became larger compensates for changes in growth rate in
P-limited growth (Figure 3E); the C quota relationship covers a greater range of Qm,u:Q 111 ; 11 and the
5
KEVIN J. FLYNN
2.0 2.0
PKQcell = 0.155
1.6 • 1.6 ｾ＠ .... -.:: 0 N-limited
• I
Ｎｾ＠
0 • P-limited
-
r'
1.2 1.2
I I
:3. :3.
::1_ ::1_ 0
0.8 0.8
••
0.4
0.0
\
••
• I
0.4
0.0
f oo
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 0.0 0.2 0.4 0.6 0.8 l.O
pgN cell - 1 pgP cell- 1
(A) (B)
2.0 0 N-limited 2.0
• P-limited
•
1.6 1.6
Ｎｾｾ＠ 0
I
:3.
::1_
1.2
0.8
-
I
:3.
::1_
1.2
0.8
e/ 0
ｧｾ＠
0
o0 o
0.4
0
0 .
••
\! 0.4
0
oo 0
0.0 0.0
0.05 0.10 0.15 0.20 0.25 0.00 O.Q2 0.04 0.08 0.10 0.12 0.14
N:C P:C
(C) (D)
20 0.05
•• 0
...•• o e
0 N-limited
15 e P-limited 0.04 Ｐｾ＠
ce
ｾ＠ •
c..
Qj
u 10
l!
:2
0.03
ｾ＠ﾷ
•
c
uoJ)
a. o• ｾ＠ｯｾ＠
u
0.02 -·fi)YJ •
ｯ･ｾ＠ｾＰ＠ｾｯｾｯ＠
o.
• ••
5 0 0.01 0 N- limited
e P-limited
0 0.00
0.0 0.5 1.0 1.5 2.0 0.0 0.5 1.0 1.5 2.0
ｾ＠ (d-1) ｾ＠ (d-1)
(E) (F)
Figure 2 Transformed data digitalised and recompiled from Elrifi & Turpin (1985) for Selenastrum minu-
tum, showing "Quota (Equation 5) fits to cel l-specific data (A, B) and C-specific data (C,D), and changes in cell
size (E) and Ch i:C (F) with growth rate. Data are for steady state under either nitrate-Nor P-limited growt h.
Ratios are by mass; Redfield mass N:C = 0. 176 and P:C = 0.024.
6
USE , ABUSE , MISCONCEPTIONS AND INSIGHTS FROM QUOTA MODELS
4000 10
3000
I_,
I _, u 6
E 2000
_§_ ""
ｾ＠
ｾ＠
;s 20 4
:0
1000 u
0 10 20 30 40 10 20 30 40
Ti me(d) Time (d)
(A) (B)
C-q uo ta (gN gC- 1) C-quota (mgP gC- 1)
0.00 0.05 0.10 0.15 0.20 10 15 20
1.0 1.0
PKQc = 0.7
0.8 0.8
0.6 0.6
-;;
:l: 1!
=>..
0.4 0. 4
0.2 0.2
PKQcell = 1.8
0.0 0.0
0.0 0.1 0.2 0.3 0.4 0.5 10 20 30 40 50 60
Cell-q uota (pgN cell - 1) Cell-q uota (fgP cell- 1)
(C) (D)•
•
• • •
'1i- 4
.0 • •
u
""
.=;, 3 • o•• oo 0 0 0
0
v;""
N 0 0
;s •• 0 P-replete
• P-deplete
10 20 30 40
Ti me(d)
(E)
Figure 3 Fits of cell quota a nd C qu ota models to the data of John & Flynn (2002) for P-replete (N-Iimiting)
and P-limiting batch growth of th e din o flagellate Alexandriumfundyense. The forms of the "Quota curves are
shown in (C) and (D) for Nand P, respectively. Also shown is the cell size (E); P-limited cell s approach double
the size of non-P-Iimited cells.
7
KEVIN 1. FLYNN
curve is greater ＨｾＧｋｑ｣＠ < ｾＧｋｑＬ･ＯＱ＠ in Figure 3D; CF ｾＧｋｑ｣＠ > ｾＧｋｑＬ･ＯＱ＠ in Figure 2). The 0 Quota curve
descriptions with reference to the same Q111 ; 11 and Qmax values shown in Figure 3C,D yield NｋｑＺＡＱｾＧ［Ｂ＠ =
t"
0.38, NKQ'(!l";.. = 0.38, P KQ::1 = 1.38, P KQ'(!l";.. = 0.46, which are very different from the KQ values
shown in Figure 3 for 11 Quota, not least because NKQ equiv < pKQequiv while NKQ > ｾＧｋｑＮ＠
In order to readily compare quota-based phenotypic descriptions between different organisms
and construct functional group models, a common base is needed. From the above, one can argue
that quota descriptions for comparative purposes are best C-based (avoiding the many orders of
magnitude variation in cell size between organisms and hence in values of Q and Kif as used in
Equation 2 or Equation 4) and are most readily compared between organisms when using the 11 Quota
formula; the dimensionless curve descriptor KQ allows a comparison between the implications of
quota-f..L responses for different nutrients.
Although Qmax: Q,;"' and indeed the absolute cell-based value of Q111 ; 11 , have been used to define
competitive advantage, the shape of the quota curve (which is fixed in °Quota as a functi on of
Qmax: Q,;"; Equation 6) is important in conferring competitive advantage (Flynn 2002). A low value
of KQ (Figure I A) is advantageous, especially if nutrient stress is not long-lived or too extreme. As
such a condition (i.e., non-extreme limitation) is most likely to occur in nature, the form of the upper
range of the quota-growth curve is the most important for ecosystem models.
Empirical to mechanistic relationships

While the original 0 Quota model was never intended to offer anything other than an empirical
description, a mechanistic basis may be sought for the quota concept. That growth would be related
positively to the amount of substrate within an organism, and that there must be a finite lower
limit below which growth cannot occur (the subsistence quota Q,;11) , is not an unexpected result.
Consistent with the form of the Michaelis-Menten equation for enzyme kinetics (and even though
growth is a function of myriad enzymic reactions) one may also expect this quota-f..L relationship to
be hyperbolic, or perhaps sigmoidal. The availability of internal substrate (i.e., Q,ax - Q,;,) does
not refer simply to unassimilated material (e.g., nitrate within a vacuole) but also to material that
has been assimilated and that can be recycled and redistributed internally. Clearly the latter requires
more processing effort, and growth (in C and/or cell terms) reliant on internal recycling may be
expected to be slower than using unassimilated material made available in ideal form. The nature
of the nutrient, and the manner in which an organism accumulates, distributes and uses it, will thus
have an impact on the shape of the quota-growth curve, as reflected in the value of KQ.
The shape of the quota-growth curve (KQ) describes an important phenotypic characteristic
(Flynn 2002). Some workers specifically make the relationship between the quota and J.l a linear
function. For example, Geider et al. (1998) make f.1 a linear function of the N:C quota; the form of
this relationship is given by Equation 7, having the same constants as Equation 2.
f..L=f..l . Q-Qmin (7)

rnax Qmax -Qmin
This linear relationship for N appears reasonably robust (N KQc > 5 for over a dozen contrasting algal
species; Flynn unpublished). However, Flynn et al. (2002), using NKQc = 3, commented that even a
shallow curve could have important implications for the behaviour of phytoplankton consuming N
within a light-dark cycle.
As noted, the initial shape of the curve, leading back from Qmax to Q,;11 as nutrient stress devel-
ops, is likely to be all important in nature, where extreme nutrient limitation is not likely due to in
situ nutrient recycling and because loss processes are likely to exceed f.1 at lower growth rates. By
8
default, the Droop equation assigns a more curved form for theN quota. Thus values ofNKQ ｡ｳｵｭｾ＠
ing Droop kinetics describe curves (N KQ,":,;·iv= 0.2, Elrifi & Turpin 1985; NKQ""";" > 0.3 in various
data collated and presented in Morel 1987) that are more hyperbolic than "Quota fits (N KQ typically
>3). For P, against which classic Droop ( 0 Quota) kinetics appear much better suited than they do for
N (Caperon & Meyer 1972), the value of KQ is typically less than 0.2 (P KQ:,:,;•i•· < 0.25, Gotham &
Rhee 1981; PKQ:,:;r·· < 0.15, Elrifi & Turpin 1985; Pｋｑ［ｾＬＢ＠ = 0.052-0.175, Morel 1987; PKQ2,;';''< 0.1,
Grover 1991; PｋｑＬｾ［ＺｾＺｩｧｨｴ＠ < 0.075, Ducobu et al. 1998). Whether the much higher values for the dino-
flagellate PKQ shown in Figure 3 are typical of these organisms is not known. Certainly it would be
useful to know if different phytoplankton groups expressed different NKQc and PKQc values. From
Figure 5 in Droop (1968) the curve for vitamin 8 12 is tight, with 812 ｋｑＬｾＺＯｴＧＧ＠ of about 0.05.
Why should the quota-11 relationship for N typically have a quasi-linear form (i .e., NKQc > 3)?
Nitrogen cannot be accumulated to any significant amount to support another generation in an
inorganic, biochemically inert, form (in total contrast to P; Watanabe et al. 1987). The amount of
inorganic N (as nitrate, for example) that may be accumulated cannot equate to more than a few
per cent of that required for construction of a daughter cell. Nitrogen can only be accumulated at
high densities (gN per cell volume) in organic form, and indeed all the vital components of the cell,
other than the membranes and cell walls, are dominated by proteinaceous and nucleic acid-based
compounds. Accordingly, the concentration of enzymes, photosystems, and so on for a given set of
conditions may be expected to relate more or less directly to the rate of growth. In contrast, nutrients
that can be accumulated to great excess (P, Fe, vitamins, etc.) would be expected to have a very dif-
ferent functional relationship between the quota and growth rate.
Although the linearisation of the quota description for N appears justified, there is no evidence
to support the universal adoption of such simple linear relationships for non-N (P, Si, Fe) quota con-
trols of growth (e.g., Moore et al. 2002), and plenty of evidence to the contrary. While the original
0 Quota model by default included a non-linear response curve, the removal of that non-linearity
could be viewed as unjustified. Doing so could be considered as similar to replacing a hyperbolic

description of external resource acquisition (e.g., nutrient uptake) with a linear function (Holling
Type f). An inappropriate choice of quota description has important ramifications beyond the mod-
elling of algal growth dynamics because a proper simulation of changes in the nutrient quota and of
associated changes in behaviour by zooplankton is important in predator-prey simulations (Marra
& Ho 1993, Mitra & Flynn 2005).
Although the quota-growth curve describes growth rate as a function of internal nutrient resource
availability, one may also expect that beyond a certain upper value for Q, no further change in the
growth rate will occur. Thus, in consideration of the P quota, in those groups in which P can be
laid down as polyphosphate (which excludes diatoms and dinoflagellates) this accumulation product
is effectively biochemically inert and further accumulation , while raising Q, cannot increase the
growth rate. Indeed, at the extreme (most likely in consequence of growth limitation by some other
factor) an overabundance of such an inert material occupying the cell volume could conceivably be
counterproductive. Flynn (2003) suggests the inclusion of an absolute maximum value of Q, Q"""
and a redefinition of Q,wx so that this is now the value of Q sufficient (if all else is in excess) to
support llmax· Thus , for example, ammonium-grown phytoplankton may not grow any faster than
nitrate-grown cells but the N:C quota of the former can be higher; both cell lines can attain Q"'"-'
(and hence 11 attains IJ.,"J but ammonium-grown cells can attain a value of N:C of Q""·' while such a
high value of N:C represses the consumption of nitrate so that these cells cannot attain a N:C much
above Q,ax (Flynn et al. 1999). This may explain why Liu et al. (2001) report a curvilinear quota
curve for ammonium-supported growth, while others (e.g., Geider et al. 1998) use a linear function
(note, however, that the original Geider et al. (1998) model was fitted to data (Davidson et al. 1992)
for ammonium-grown cells).
9
KEVIN J. FLYNN
Thus, there would appear to be grounds to assign a mechanistic meaning to the quota concept,
although not to the original 0 Quota equation itself. A mechanistic basis is easier to consider from
biochemical arg uments on a C basis, rather than using the original cell quota description (Droop
1968). That mechanistic basis, and our understanding of it, is important and it should not be treated
lightly by unjustifiably altering the form of the quota-growth curve.
Applicability of the quota approach for different nutrients

Since the original description, other nutrients have been subjected to the quota treatment. These
include, in addition to vitamin B12 and P, N, Fe, Si, and even light (Droop eta!. 1982, Baird &
Emsley 1999). The nature of these nutrients, their functional role within phytoplankton, differs
greatly and has a profound impact on the applicability of a quota approach.
From an empirical point of view, a quota application for Si may be justified; a diatom grown in
a Si-limited chemostat (i.e., at steady state) shows a relationship between Si quota and 11 (Paasche
1973). However, at a mechanistic level a quota relationship for Si is not acceptable because previ-
ously assimilated Si is not available for redistribution within the cell (though it may be redistributed
via dissolution of Si frustules from cells that have lysed; Nelson et a!. 1976, Fehling et a!. 2004).
There is a quota relationship for Si in a Si-limited chemostat because at steady state, Monod and
quota descriptions fit the same data (Droop 1973). However, while the growth rate can explain the
quota, the Si quota shou ld not be used to deduce the growth rate. The link between Si and 11 should
be made directly to external nutrient availability, operating in a Monod-like manner (Flynn &
Martin-Jezequel 2000).
A rather different issue affects the usefulness of a Fe quota-11 relationship. The need for Fe
varies greatly with light avai lability because the critical role of Fe in photosynthesis (Raven 1990)
places a variable demand for this element as cells regulate photosystem synthesis during light accli-
mation. The need for Fe also increases with growth rate in general (via the role of Fe in respiration)
and with the consumption and hence reduction of nitrate as the N source (Raven 1990, Sunda &
Huntsman 1997, Armstrong 1999, Flynn & Hipkin 1999, Kustka eta!. 2003). In consequence, a
single quota relationship (on a cellular or C base) is not expected for Fe. Figure 4 shows the output
of the mechanistic model of Flynn & Hipkin (1999) as used by Fasham et a!. (2006). Although
there are no data against which to fully tune such models, the model structure costs Fe-mediated
-::s
I
ｾ＠
::::
..c: 0.1
3
2
l?
0.01
0 50 100 150 200 250

Fe:C (J.ig:g)
Figure 4 Simulated relationship between the Fe:C quota and growth rate for a diatom growing on nitrate
(thin lines) or ammonium (thick lines) at different photon flux densities (PFDs). At any given PFD the ammo-
nium curve is higher than that for nitrate. Output is for the diatom model used by Fasham et al. (2006).
10
growth processes between the three major Fe demands according to biochemical knowledge. Values
of FeKQc for the curves shown in Figure 4 range from 0.05 (ammonium grown, highest light) to I
(nitrate grown, lowest light). Most likely there is not a single value of KQ for other nutrients either,
the relation ship varying depending on other external factors (this being especially likely for KQ,e11 in
cell quota descriptions because of the variation in C cell- 1). The quota curves are thus not fixed but
vary with C limitation , consistent with the variation in critical N:P with light (Leonardos & Geider
2004). However, the situation for Fe can be expected to be so extreme it renders a single simple Fe
quota description (fixed FeKQ) for all likely nutrient and light conditions effectively useless.
Whi le vitamins, specifically B12 , have enjoyed a recent revival in interest (Croft et al. 2005,
Bertrand et al. 2007, Droop 2007), N and Pare the most important nutrients for quota descriptions
in ecosystem models. Of these two, the quota-11 interaction for N is also poorly described using the
0 Quota structure. The values of N:C and P:C lend themselves to use not only in quota controls of
growth rate but also in control of nutrient acquisition. Thus N:C can be used to control ammonium
versus nitrate versus amino acids versus N 2 fixation (Flynn et al. 1999, Flynn 2003, Stephens et al.
2003). Likewise, P:C could be used to control the use of inorganic versus organic P sources; growth
using dissolved organic P need not be limiting and expression of phosphatase activity indicates suf-
ficient internal stress to derepress enzyme synthesis and not necessarily P-limited growth. In both
instances the stress that biologically derepresses the use of alternative nutrients can be linked to
declining nutrient:C (N:C and P:C) quotas between Q ahs and Qmax· The linkage between quotas and
the control of nutrient transport is considered further but first it is necessary to consider the meaning
of high quota values.
Misconceptions and misunderstandings over high quota values

Two misconceptions have commonly been associated with the use of the quota model; one is that a
high quota indicates a high growth rate, and the other is that the maximum growth rate is attainable
only at the highest quota. In part these are functions of a misunderstanding that has arisen over the
physiological explanation of the nutrient quota. They also relate to interpretations of nutrient:C quo-
tas and to the Redfield ratio. The original quota equation (Droop 1968) contained no reference to a
maximum quota; the maximum rate of growth was tied to the rate of nutrient transport and the quota
(as a nutrient:cell quota) had no obvious biochemical boundary as does a nutrient element:C ratio.
The Redfield ratio (Redfield 1958) is an average elemental (stoichiometric) ratio for oceanic
particulate material. It is widely and colloquially used as an assumed value, if not the optimal
value, of C:N:P for phytoplankton. However, algal N:C and P:C can exceed Redfield values (Geider
& La Roche 2002), the highest growth rates often be ing assoc iated with values exceeding Redfield,
and there is no biological (physiological) basis for such a set ratio (Kiausmeier et al. 2004a). The
optimal C:N:P is also expected to vary with cell size (higher N:C in smaller cells) and in eukaryotes
versus prokaryotes (higher P:C versus lower P:C respectively in smaller cells) (Raven 1994). The
qualitative ranges of N:C and P:C that may be expected under N, P or light limitations are shown
in Figure 5.
It has long been known that a high quota for a given nutrient, or indeed for several nutrients
simultaneously, cannot be interpreted to indicate a high growth rate (Donaghay et al. 1978, Tett
et al. 1985). Light and temperature limitations of growth prevent such extrapolations. The quota can
only indicate whether a particular nutrient is non-limiting and not whether growth is occurring at
any particular rate. The more complicated issue involves relating high quotas to high growth rates.
The quota is a ratio, and ratios can be high because the denominator is small, or because the
numerator is large. Thus a high N:C could reflect a relatively high cellular N content (optimal) or a
low C content (suboptimal). From a biochemical standpoint, one expects physiological regulations
to ba lance the cellular response to these events, to not only increase (up-regulate) acquisition of a
II
KEVIN J. FLYNN
,---------
'' -N
''
''
''
'
N:C
Figure 5 Schematic representation of the C quota range of N and Pin relation toN, P or light (i.e., carbon)
limitations assuming that the other factor(s) are non-limiting. Zones indicate N-limitation (-N), P-limitation
(-P), co-NP-limitation (-NP), and light limitation (-Light). Minimum quotas marked NC'";.' and PC'";,; quota
required to support maximum growth rates marked NCmax and PCmax; absolute maximum quotas marked NC.,_,
and ?Cabs- Scales are only representative, but note the difference between PC.,_,: PC'""-' and NC.,,:NCmax-
limiting nutrient but, critically, also to decrease (down-regulate) acquisition of non-limiting nutri-
ents. One of the reasons that Flynn (2003) introduced Q""' (absolute maximum possible quota) in
addition to Qlllax (quota required to support the maximum growth rate) was in reflection of the fact
that under non-nutrient limiting conditions the quota could exceed Qlllax· Values of Q between Q lllin
and Q111 11 x wou ld be expected to be associated with up-regulation of nutrient acquisition, and between
Qlllax and Q""' with down-regulation. The latter zone would be expected to be especially apparent
for P:C when Nor light, or indeed when the intrinsic maximum rate of growth (i.e., cell cycle), is
limiting (e.g., Elrifi & Turpin 1985). It is also noted for N:C with light limitation (Laws & Bannister
1980), with ammonium-grown cells showing higher N:C than nitrate-grown cells (Wood & Flynn
1995, Flynn et al. 1999). Indeed, the variation of N:C over the light-dark die! cycle can be linked
to the control of dark-N assimilation , which is especially important for nitrate assimilation (Clark
et al. 2002 , Flynn et al. 2002).
The constant Qa,, (Flynn 2003) represents the absolute maximum possible value of Q at which
nutrient tran sport must be terminated. However, it is apparent that depending on other factors ,
transport may be terminated at a lower value of Q, at a value here termed QTco,. Thus in P-limited
cells, NCh"" for N assimilation may be less than NCIII"-'' and hence N:C in P-limited cells declines
(Figure 2). For different N sources different va lues of NCTcon are expected such that ｎｃｾ［ＬﾷＢＧ＠ >
ｎｃｾ［ＧＢ＠ > ｎｃｾＬＺＮ＠ Similarly, different values of QTcon are also expected for the use of dissolved
organic P (requiring the synthesis of the phosphatase enzy me) versus the direct use of dissolved
inorganic P (i.e., ｐｃｾＮ［Ｌ＾＠ｐ･ｧｾＺ｜＠
Armstrong (2006), commenting that the implementation of the linear form of the N:C quota
model by Geider et al. (1998) is inappropriate at low light, offered an optimisation model alterna-
tive to describe why the maximum N:C quota is not an optimal quota under such conditions of light
(=C) limitation. The mechanistic basis for this lies in the (de)repression control of cell physiology
that is linked to the cellular concentration of metabolites (Flynn 1991 , 2003, Flynn et al. 1997,
2002). The typical algal model does not refer to metabolites and to product-inhibition links (see
Flynn et al. (1997) for ammonium nitrate controls via such links and John & Flynn (2000) for P con-
trols) because of the resultant increase in complexity and decrease in integration step size required
12
USE, ABUSE , MISCONCEPTIONS AND INSIGHTS FROM QUOTA MODELS
to run such models. However, a more empirical association can be made to cellular C:N:P to drive
an active control between quota nutrient acquisition. For N:C and the interactions between light,
ammonium and nitrate acquisition this association is shown in Flynn et al. (2002), with elevated
values of N:C downregulating N-source acquisition. Thus, at very high N:C ratios N-source uptake,
and thus growth rate, is restricted. At the same time, the demand for C (and hence the link to Chl:C)
is heightened , which can be used to modulate the synthesis of Chl:C (Flynn 2001).
The control of nutrient acquisition in models is more of a challenge than the use of quotas to
control growth and the mechanisms by which it is achieved has important implications (Morel 1987,
Flynn 2002). This control is at least as important for the non-limiting nutrient as for the nutrient
that limits growth.
Nutrient acquisition - the quota-transport interface

The great novelty of the Droop approach, in contrast to that of Monod, was to relate growth to
the internal rather than external nutrient pool concentrations. In reality, growth is a function of
both these pools and the methods by which nutrient acquisition (via Monod-like kinetics) into the
quota is described, and the subsequent control of nutrient transport and growth by the quota, are
all important for the final model behaviour. The simplest way to link these functions is by defining
the maximum nutrient transport rate T,,.ax as equal to [.lmax· Qmax (Goldman & McCarthy 1978). This
makes the tacit assumption that the maximum growth rate is actually simultaneously co-limited by
both nutrient transport and internal processing. However, this simple link between transport- and
quota-type models fails to describe the development of surge transport capabilities that offer com-
petitive advantage (Turpin & Harrison 1979) and change nutrient uptake ratios. This link also does
not down-regulate nutrient acquisition when another factor limits growth.
Empirically these types of interactions were considered over three decades ago (Droop 1974,
1975) and two quota descriptions were identified that could be viewed as functioning in opposite
directions. For the limiting nutrient, substrate availability controls (limits) nutrient uptake, which
controls the limiting quota QL and subsequently [..l via the quota equation. For the non-limiting
nutrient, [..l (as set by QJ controls the non-limiting quota QN via a control on the uptake of the non-
limit ing nutrient, which in turn affects the remaining non-limiting substrate concentration. Droop
(1975) also considered the special instance of a limiting yet inexhaustible nutrient (namely light).
For the limiting nutrient the quota relationship in Droop's arguments used the real Q"';,., while
control of the acquisition of non-limiting nutrients was by reference to an apparent Q,..;,; this latter
value equates in some ways to Qr,, in the discussion above. Davidson & Gurney (1999) make aver-
sion of this regulation using a hyperbolic regulation term rather than using a quota description . The
advance that we make now is to recognise the mechanism behind these interactions and how they
can be manipulated to control transport of different nutrients .
The kinetics of nutrient acquisition are a consequence of changing transport capabilities and
are not fixed; they vary with the type of nutrient and the nutrient status as reflected by the quota
(Smith & Kalff 1982, lkeya et al. 1997, Flynn et al. 1999). Knowledge of the existence of interac-
tions between external and internal nutrient availability and surge acquisition dates from the 1970s
(Conway et al. 1976). Droop (1973) postulated a linear relationship between cell-specific nutrient
transport and the nutrient:cell quota and ended by questioning whether in non-steady state the trans-
port capacity of the lesser limiting nutrients become controlled (as we now know it to be) by down-
regulation. Elrifi & Turpin ( 1985) later concluded that the original 0 Quota model could not handle
the consumption of non-limiting nutrients correctly over the entire range of nutrient supply ratios
(here N: P) and growth rates because of the lack of fidelity in such controls and the basis of their con-
struction (making reference to external nutrient concentrations). Zonneveld ( 1996) declares there is
13
KEVIN J. FLYNN
no meaningful basis for the Droop handling of non-limiting nutrients. The point remains, however,
that Droop apprec iated that the handling of non-limiting nutrients is important; most experimental
and modelling studies place their emphasis on the assimilation of single nutrients (i.e. , that which is
limiting) or upon single nutrient-light interactions.
The abi lity to perform surge uptake and to modulate uptake of non-limiting nutrients (e.g.,
Conway et al. 1976, Conway & Harrison 1977), especially as they may feature to different extents in
different organisms, has important imp! ications also for the theoretical analyses of 0 Quota dynam-
ics (e.g., Lange & Oyarzun 1992, Pascual 1994, Bernard & Gouze 1995, Smith 1997). Analyses of
the competitive advantage based solely on transport kinetics (Healey 1980, Button 1991) are also
inadequate. It is a balance of both transport and subsequent internal factors (in part summarised by
the form of the quota curve) that govern the outcome of competition (Flynn 2002) and indeed makes
experimental determinations of transport kinetics such a challenge (Flynn 1998).
There are various examples where the combined kinetics of Monod and quota equations have
been studied, together with empirical data, to drive discussions on nutrient transport kinetics, espe-
cially in chemostats at low dilution rates where external nutrient concentrations fall below detection
(e.g., Gotham & Rhee 1981). Nutrient stress, as driven by low chemostat dilution rates relative to
J.lmax• can have different levels of physiological severity depending on the identity of the limiting
nutrient (thus Si stress may be more severe than N stress at low dilution rates (Harrison et al. 1976)).
In reality, Tmax (rather than being fixed as equal to J.lmax·Q 11111_,) is itself a variable with Q, typically
initially increasing as Q declines (Gotham & Rhee 1981). Because of this variability, and indeed
because a high T.nax may compensate for a high half-saturation for transport (K, nu'trient affin-
ity being set by T,"jK,), a single set of equations describing Monod-style growth kinetics cannot
describe phytoplankton growth completely. Various approaches have been developed to enhance the
nutrient transport control of the quota model (notably Morel 1987) providing a Droop-based model
for use under dynamic situations (Grover 1991).
There are two issues here. One is the potential surge transport of the limiting nutrient into an
organ ism previously deprived of that nutrient and the other is of 'luxury transport' of non-limiting
nutrients. Even if the transport capacity remains constant (T,""' set by J.lmax QmaJ, then there is de
facto an increasing capacity for acquisition over that required to satisfy demand as Q declines to
Q111 ; 11 • Surge transport has been studied for N, P and Si (Conway et al. 1976, Parslow et al. 1984) and
shows different responses for different organisms and different nutrient types. The surge transport
of P (e .g., Smith & Kalff 1982) displays capacities of an order of magnitude above that required to
support the current growth rate (i.e., as Q ｾ＠ Q111 ; 11 then T,""x ｾ＠ >> J.lmax ·Q""'x). Ammonium di splays
similar surge kinetics but nitrate does not (Parslow et al. 1984, Syrett et al. 1986, Flynn et al. 1999).
Hence, T,/1/IXfor p can be similar to that for nitrate-N (g element g c- 1) despite the 40-fold difference
in minimum quota values. The relationship between the N:C quota and nitrate T,,ax ＨｔＬ［ＺＮｾＢＧＢＩ＠ appears
bell shaped (Flynn et al. 1999). Thus ｲＬ［ＺＮｾＢＧＢ＠ falls below the demand rate (i .e. , J.l·(N:C)) at high N:C ,
when theN status is so high due to ammonium assimilation or with light limitation that the ability
to use nitrate is repressed. This mechanism prevents nitrate-growing cells from having such a high
N:C as ammonium-growing cells have. T,;;;:.:'"' also falls close to the demand rate at extremely low
N:C, when the cel l is so starved that it is increasingly physiologically incompetent.
There are various ways in which these changes in dynamics have been explored. Morel (1987)
gives a detailed treatment of simple descriptions of changes in uptake kinetics and how the resultant
value of the apparent half-saturation constant for growth (Kg) also changes. In keeping with experi-
mental data for N-source uptake, Flynn et al. (1997) used linear or curvilinear descriptions, whereas
later Flynn (2003) used sigmoidal functions, which can be readily altered to describe a range of
patterns relating T.nax to the nutrient quota. Although curves are more appropriate as empirical
descriptors (conforming to the way that biochemical feedback processes occur), linear equations
are more tractable for mathematical analysis. Indeed, the simple form of the Droop equations has
14
undoubtedly been instrumental in making them such a popular target for mathematical and theoreti-
cal biological studies.
The patterns that are observed between Q and T,""' now provide us with a mechanistic basis for
a description of the nutrient transport component of quota-based models, to enhance the phenotypic
capabilities of the original Droop model. Transport capabilities are under (de)repression regulation,
with synthesis minimised (repressed) when the cell contains a sufficient amount of the incoming
nutrient element and maximised otherwise. The value of Q controlling transport (Qm,) varies with
various factors with interactions that lay behind the form of Figure 5. In reality, rather than being
the whole organism Q that biochemically controls T,""'' control is via metabolites that could be the
nutrients themselves within the cells (transinhibition) or more commonly a downstream product of
nutrient assimilation. Thus for the control of nitrate and ammonium transport, glutamine (Gin) is
considered a likely regulatory metabolite (Flynn 1991) and has been so employed in complex mod-
els (Flynn et al. I997). However, to involve an explicit description of such metabolite pools creates
an overly complicated model for routine use, requiring additional state variables for metabolite
quotas. Even the most demanding of modellers is unlikely to want to consider simulating all of the
phenotypic variation that molecular biology now indicates may be present (with several transport-
ers for each substrate; e.g., Hildebrand 2005). John & Flynn (2000), considering the interactions
between different intracellular P pools, P transport and P:C quota-linked growth, suggest that the
removal of P into inert polyphosphate would enable better decoupling of transport from assimila-
tion. However, they also indicate that it was not necessary to specifically model the presence of
these pools provided that an appropriate variant of the quota model is used. An empirical link back
to the whole organism nutrient quota is thus more appropriate and more desirable (Flynn & Fasham
1997, Flynn 2003, Stephens et al. 2003).
While N stress does not appear to greatly affect P accumulation (although transport is affected
(Conway et al. 1976)), such that the P quota rises to a maximum value and may exceed that attained
during nutrient-replete conditions (Elrifi & Turpin I985, Liu et al. 2001), P stress appears to have a
greater affect on N assimilation (Healey & Hendzel 1975, Terry 1982, Elrifi & Turpin 1985, Figures 2
and 5). The former event is especially important when one considers marine biogeochemistry because
N limitation will inevitably result in a strong shift away from the Redfield N:P. This is all the more
likely because of the high value of PC",,:PC"'"' (>l); in comparison NC",,:NC,""' is much narrower
(< 1). The behaviour of a quota model in which T,,w, for the non-limiting nutrient is ultimately brought
to zero as Q ｾ＠ Q""' (Flynn 2003) describes the control of P transport in this situation.
The more interesting event is where P stress is associated with a decline in theN quota (Figures 2
and 5). The significance of this event assumes that N is not exhausted during P-limited growth
(noting, for example, that Elrifi & Turpin 1985 make no mention of measuring residual nitrate
concentrations). This is a potential problem in batch-style experiments; given the great range of
P:C in phytoplankton (Geider & La Roche 2002), and that P can be accumulated to excess during
N limitation, it is not always trivial in a culture system at quasi-natural biomass levels to ensure that
P limitation is not associated with concurrent exhaustion of theN source.
In P-replete cells, the intracellular concentration of glutamine, and the value of the
glutamine:glutamate ratio (Gin:Giu) varies with theN status, being highest in previously N-starved
ammonium-refed cells, lower in nitrate-growing cells, and lowest inN-starved cells (Flynn 1990).
The concentration of Gin is implicated with the regulation of N-source transport (Flynn 1991), but
the impact of P stress upon the intracellular accumulation of Gin is not known. If P stress resulted
in the accumulation of Gin, then this could explain the repression of N transport that must accom-
pany the noted decline in N:C (Figure 2C). From the relationship between N:C and P:C in P-limited
Selenastrum, then ｑｾ［ｾ［ｲ･＠ declines as P:C declines (from data shown in Figure 2; ｑｾ［ｾ［ＧＢ＠ = 4.8·P:C
+0.1125; R 2 =0.91). What is not known is the shape of this relationship in cells grown on ammonium
(Figure 2C shows nitrate-grown P-limited cells). One may expect this relationship to be steeper
15
KEVLN J. FLYNN
than for growth on nitrate (closer to vertical) because ammonium assimilation is repressed at higher
internal concentrations of Gin (and hence of higher N:C; Flynn et al. 1999).
To conclude, the control of nutrient transport is ideally made a function of both the respective
nutrient:C quota and of the quota of other nutrients. There are two components to this: ( l) the value
of the quota at which transport halts CQr, 011 ) and (2) the magnitude of T,""x at values of Q < QTco/1" In
the simplest form, the combined description is given by T,""" = !lmax· Qmax·(Q < QTco11 ); the Boolean
logic term simply halts transport if Q attains QTco"' with Qrc"" being a function of other nutrient:C
quotas as required. What can be seen readily is that deviation from Redfield C:N:P may be rapid as
stress is applied and can be strongly divergent between P- versus N-limited cells. Droop recognised,
and modelled, the multinutrient interactions at a simpler level, but appeared (Droop 1975) unsure
regarding whether the resultant model complexity was justified. Today we can be reasonably sure
that the effort is indeed worth it.
Competition, nutrient supply ratios and stoichiometric

predator-prey models
Despite the steady-state origins of the Droop cell quota model, it is still useful in following com-
petition in dynamic systems (Droop 1975, Grover 1991, Ahnet al. 2002). This is so, even though
delays in cell responses are not handled adequately (Davidson & Cunningham 1996), which can
have important implications in competition scenarios (Li et al. 2000). Although links between
nutrient:cell and nutrient:C quotas can be interpreted to explain population growth and resource
availability (Savage et al. 2004), the interplay between nutrient uptake capabilities and the shape
of the quota curve has great capacity for affecting competition between algae (lkeya et al. 1997,
Yadstein 1998, Flynn 2002, John & Flynn 2002). That diatoms do not accumulate polyphosphate
could be a factor affecting their competitive advantage when under P stress (Egge 1998), especially
if the inability to remove newly assimilated P to an inert form that does not affect further transport
(John & Flynn 2000) prevents diatoms from making best use of P pulses.
The most advantageous quota configuration is a high Qmax:Q"';"' low Q"';"' high Q""·'·' coupled
with a low KQ value (Figure 1). This would endow an organism with a capacity to accumulate much
surplus nutrient (Q""·' >> Qma) in times of plenty and to continue growing on that nutrient reserve at
a high relative growth rate for as long as possible in the absence of any new input. The interface with
transport kinetics is important (Kiausmeier et al. 2004b), as is the control of non-limiting nutrient
transports (Flynn 2002, 2003) because these processes top-up the quotas and drain the environment
of nutrients required by future generations of potential competitors (Flynn 2005b). Thus the magn i-
tude and control of T,""x is important.
The value of the critical N:P ratio, at which Nand P quotas exert equal control of growth (Rhee
& Gotham 1980), varies with growth rate and with light over the die! cycle and with day-integrated
irradiance (Leonardos & Geider 2004). Different algae display different critical N:P ratios at low
growth rates (Ahlgren 1985), as a function of differences in Q111 ; 11 and in KQ, but these become less
obvious at high !l because of the similarity in values of Q,wx· Although competition has been the
subject of many studies since those of Rhee (l974) and others, these studies have been primarily
associated with freshwater phytoplankton (and especially with chlorophytes and cyanophytes, which
accumulate polyphosphate), and considered with nutrient:cell quota formulations. Multinutrient
C-specific studies, especially of marine species, are sorely lacking. The importance of these studies
arises because growth and nutrient consumption must not be made a function only of the most lim-
iting nutrient; otherwise the consumption of the lesser-limiting nutrients is not described correctly
(Sciandra & Ramani 1994, Davidson & Gurney 1999), and competition simulations described using
such models have the potential to give seriously erroneous results (Flynn 2005b).
16
The implications of the quota control of growth are also important for those conducting experi-
ments and ecosystem investigations on the impacts of N:P nutrient supply levels. It is readily
apparent from the manipulation of even the simplest quota models that great care must be taken in
conducting a nd interpreting batch-style experiments in which the impact of variable nutrient N:P is
studied. The larger Qmllx:Q,"i"' and the smaller the value of KQ, the longer it takes for nutrient stress
to affect growth. Thus it takes very much longer for cultures to become growth limited to the same
extent by P than by N availability. Furthermore, the duration of the period before effective limita-
tion is affected by the extent to which the organisms managed to engage in surge assimilation (i.e.,
the value of Q",,:Qnwx and the value ofT,""-' relative to !l·Qm") prior to nutrient exhaustion. This is
again far more of a problem for P because the ready accumulation of P (especially in those that
can accumulate polyphosphate) enables Q""' to far exceed Qnwx· The nutrient status (quota status)
of the phytoplankton at the start of a given batch study thus becomes an important factor affecting
whether the organisms display characteristics of one or other nutrient limitation during the duration
of the investigation. In steady-state chemostat studies, the importance of the ways in which prior
nutrient history affects the cell's response to perturbation may be missed, while they can have great
consequences for batch studies and for natural events.
There is increasing interest in modelling the stoichiometric link between planktonic preda-
tor and prey and indeed an appreciation of the general importance of stoichiometric differences
between consumers and their food in ecology (Sterner & Elser 2002). It is thus important to get
the quota description of growth rate correct because the description affects the growth not only of
the phytoplankton prey, but also of their predators. The adequacy of the description is especially
important where the interaction is enhanced by the development of antigrazer strategies in nutrient-
stressed phytoplankton (Mitra & Flynn 2005, 2006). For this purpose, nutrient:C quota relation-
ships are required, although certainly one could argue also for a description of cell size (C cell- ')
because predators capture cells not biomass. In this context, assuming the quota curve is always
linear (Moore et al. 2002) if it is not, or conversely using a 0 Quota formula to describe the wrong
type of hyperbolic curve, is all the more worrying.
Simulating genetic and phenotypic diversity

Another issue that Droop raised during development of the quota model that is of high relevance to
our current modelling activities is the subject of genetic and phenotypic genetic variation. Droop
( 1974) encountered this in the form of ' fast-adapted ' and 'slow-adapted ' P- and 8 12 -limited chemostat
cultures of Monochrysis. Harrison et al. (1976) encountered a similar event for Si-limited diatoms.
To what extent such observations reflect evolution within a clone or selection within non-clonal
cultures is not known but for applications of models to field situations the whole topic of diversity is
one that is invariably avoided.
While molecular biology has demonstrated the great diversity of plankton , in total contrast,
modelling typically amalgamates groups, glossing over phenotypic differences that define diversity
and succession (Irigoien 2006). Models assume uniformity within groups, and indeed typically this
is extended to functional groups in the widest possible sense of the term (phytoplankton, zooplank-
ton). We know so little in quantitative terms about integrated algal physiology, including factors such
as how non-limiting nutrients are handled, that we cannot make a fully parameterised model for
even one clone (Flynn 2005a, 2006) and this lack of knowledge makes the whole issue of diversity
even more problematic. Droop (1974) ends by asking whether "the phytoplankton of a region might
be regarded [for modelling purposes] as an envelope, the sum of its component parts, and it would be
interesting to know whether the kinetic properties of this envelope show any coherence". In fact, it is
now more than a matter of interest because consideration of this matter is becoming a necessity.
17
KEVIN J. FLYNN
Conclusions
In one way or another, the development and use of the cell quota model by Droop (1968) has stim-
ulated the research of generations of phytoplankton scientists. 1t also affects those interested in
predator-prey interactions and those who appreciate the importance of variable stoichiometry in
global-scale ecosystem models. Today the original quota model (Droop 1968) is rarely used, but the
legacy of the work remains powerful. Not infrequently the work of Droop is referenced even though
the methods employed barely follow the original description.
While early researchers appreciated the limitations of the empirical quota descriptions, later
developments have not always maintained a connection with reality as supported by either empiri-
cal data fits and/or through a mechanistic basis. The 'cell quota model' became the 'quota model',
ignoring the differences between C and cell bases that affect the validity of the original empirical
construct. Manipulations of the quota description to describe the competitive advantage of one spe-
cies over another ignored the vital importance of the nutrient transport process. Furthermore, sim-
plifications of quota descriptions, which have serious implications for simulations of phytoplankton
growth, nutrient transport and trophic dynamics, have been made with little or no justification and/or
no biological validation. There have also been many variations on the theme without a full apprecia-
tion of what Droop had achieved by the mid-l970s. In part this is perhaps because the original mod-
els, with their cell-based units, did not lend themselves so readily to the C-based models required
in ecosystems. The simplistic elegance of the 0 Quota equation, while lending itself to ready math-
ematical investigation, was also inappropriate for one of the main applications, nitrogen.
Assignment of typical values for the normalised, dimensionless curve descriptor KQ in "Quota
(Equation 5) for different nutrient (element) types in different plankton groups would decrease the
number of free variables in models, while better describing the quota-j..l relationship than is achiev-
able using 0 Quota with its fixed curve form. As an approximation, it may be tempting to set the
upper quota values for N:C and P:C to the Redfield ratio (Redfield 1958). However, the maximum
quotas (especially for P:C) readily exceed the Redfield values, and indeed maximum growth rates
may not be attainable at Redfield values (e.g. , Figure 2).
One of the greatest challenges still is the correct description of the quota of non- or lesser-limit-
ing nutrients. The call by Elrifi & Turpin (1985) for "much further work ... to determine the kinetics
of non-limiting nutrient utilization and their significance to algal competition" has not been met
two decades on (Flynn 2005b). Whether such work is best conducted under steady state (the arena
in which the original quota studies were conducted) or in some form of non-steady-state system
is debatable. That is especially so given the selective pressure that can develop within chemos tats
(Dykhuizen & Hartl 1983) affecting the appearance of 'fast' and 'slow ' acclimated populations
(Droop 1974, Harrison et al. 1976, Maske 1982). Furthermore, while a good dynamic model may be
expected to satisfactorily describe steady-state conditions, the opposite need not be so.
The gulf between genetic, phenotypic and modelled diversity needs to be closed. Although we
have a reasonable qualitative understanding of algal physiology, our quantitative understanding is
at best described as incomplete. Likewise, how genetic diversity translates to phenotypic diversity
is unclear. Without an understanding of the breadth of phenotypic diversity we cannot fully explore
the implications for model diversity. However, what we can be sure of is that features such as the
form of the quota-j..l curve and of the interactions between quota and nutrient transport will be
important variables in such descriptions.
There is a time and place for all ideas; quite a number of the topics that were explored by Droop
in his early work on the quota concept have recently come back to the forefront of our science.
Whatever the future holds, we can be sure that quota-type models are here to stay.
18
USE, ABUSE , MISCONC EPTIONS AND INSIGHTS FROM QUOTA MOD ELS
Acknowledgements
I am indebted to Michael Droop, to whom this work is dedicated in hi s 90'h year, because our dis-
cussions have added much to the content of this work and to Paul Harri son and to John Raven for
the ir most useful comments in the later stages of manuscript preparation . Help from John Leftley
and Ian Davies is also much appreciated.
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23
Oceanography and Marin e Biology: An Annual Review, 2008, 46, 25-63
© R. N. Gibson , R. J. A. Atkin son, and J.D. M . Gordon, Editors
Taylor & Franci s
EFFECTS OF BENTHIC ALGAE ON THE

REPLENISHMENT OF CORALS AND THE IMPLICATIONS
FOR THE RESILIENCE OF CORAL REEFS
CHICO L. BIRRELU, LAURENCE J. MCCOOKI.2,
BETTE L. WILLIS 1 & GUILLERMO A. DIAZ-PULID03
1
ARC Centre of Excellence for Coral Reef Studies and School of Marine and
Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
E-mail: CLBirrell@gmail.com , Bette.Willis@jcu.edu .au
2GreatBarrier Reef Marine Park Authority, Townsville 4810, QLD,
Australia, and Pew Fellowships Program in Marine Conservation
Corresponding Author E-mail: L.McCook@gbrmpa.gov.au
3ARC Centre of Excellence for Coral Reef Studies and Centre for Marine Studies,
The University of Queensland, Brisbane, St. Lucia 4072, QLD, Australia
E-mail: g.diazpulido@uq.edu.au
Abstract The ecological resilience of coral reefs depends critically on the capacity of coral popu-
lations to re-establish in habitats dominated by macroalgae. Coral reefs globally are under rapidly
increasing pressure from human activities, especially from climate change, with serious environ-
mental, social and economic consequences. Coral mortality is usually followed by colonisation
by benthic algae of various forms , so that algae dominate most degraded and disturbed reefs. The
capacity of coral populations to re-establish in this algal-dominated environment will depend on
direct and indirect impacts of the algae on the supply of coral larvae from remnant adults, on settle-
ment of coral larvae and on the post-settlement surviva l and growth of juvenile corals. The effects
of benthic algae on coral replenishment vary considerably but the thick mats or large seaweeds
typical of degraded reefs have predominantly negative impacts. Some algae, mostly calcareous red
algae, may enhance coral settlement on healthy reefs . Algal effects on coral replenishment include
reduced fecundity and larval survival, pre-emption of space for settlement, abrasion or overgrowth
of recruits , sloughing or dislodgement of recruits settled on crustose algae, and changes to habitat
conditions. There is a serious lack of information about these effects, which are likely to cause
bottlenecks in coral recovery a nd significantly reduce the resilience of coral reefs.
Introduction
Globally, degradation of coral reefs due to the impacts of human activity is increasing, raising con-
cerns for the future persistence of reefs and the social and economic goods and services they provide
(Bryant et al. 1998 , Wilkinson 2004, Pandolfi et al. 2005). Reefs face an increasing number, inten-
sity a nd frequency of stresses and disturbances (Hughes & Connell 1999, Karlson 1999, Hughes
et al. 2003), including climatic change in particular (Hoegh-Guldberg 1999, Hoegh-Guldberg et al.
2007). Coral reefs are subject to frequent disturbances, natural or anthropogenic, such as hurri-
canes/cyclones, crown-of-thorns starfish outbreaks, diseases and mass bleaching of corals. Their
resilience, or capacity to resist or recover from these disturbances, is critical to their long-term
25
CHICO L. BIRRELL ET AL.
persistence and contributions to economies (McCook et al. 200Ib, Hughes et al. 2007). Recent
research has shown that the capacity of reefs to recover from disturbances is especially vulnerable
to human impacts (McCook 1999, Hughes et al. 2003 , 2007, McCook et al. 2007).
The recovery of reefs after disturbance requires the re-establishment or replenishment of coral
populations, either by regrowth of surviving coral fragments or the arrival and settlement of coral lar-
vae and their post-settlement growth and survival (Hughes 1994, Hughes & Tanner 2000). However,
it is important to realise that this replenishment takes place against a background of benthic algal
dominance (McCook 1999, Hughes et al. 2005, 2007, McCook et al. 2007) because disturbed coral
reefs are almost universally colonised by some form of benthic algae (Diaz-Pulido & McCook
2002, 2004) and degraded coral reefs are generally dominated by benthic algae (Table I; Hughes
et al. 1987, Done 1992, Hughes 1994, Connell et al. 1997, McCook 1999, Hughes et al. 2007).
Indeed, the state of a reef as resilient or degraded is largely determined by whether algal dominance
after disturbance is temporary, because coral populations recover, or becomes long term, precluding
coral recruitment and regrowth. Impending climate change, with increasing sea temperatures and
consequent increases in severity and frequency of mass coral bleaching (Hoegh-Guldberg 1999)
and coral disease (Bruno et al. 2007), inevitably followed by coral mortality and subsequent algal
overgrowth, will seriously reduce the capacity of coral populations to re-establish before subsequent
disturbances (Hughes et al. 2003, 2007, Diaz-Pulido et al. 2007b).
Algal inhibition of coral replenishment has the potential to cause a serious bottleneck for reef
recovery, depending on the nature of the algal assemblage. Diaz-Pulido & McCook (2002) found
algal colonisation, after the 1998 mass bleaching on the Great Barrier Reef, to be distinctly different
on two reefs within 15 km of each other, with one reef dominated by fine, filamentous algal turfs,
the other by larger, fleshy upright algae. Subsequent work at the first reef (Orpheus Island; Hughes
et al. 2007) showed that the nature of the algal assemblage (turfs vs. larger seaweeds) had major
effects on coral recruitment and on the resilience of the reef. Thus the effects of benthic algae on the
processes of coral population recovery are critical to the resilience of coral reefs, and increasingly
so with impending climate change.
Algal effects on coral recovery can be separated into competitive effects of algae on surviv-
ing coral colony fragments and effects on coral population replenishment, including reproduction
(fecundity) and recruitment (including larval dispersal/supply, settlement and post-settlement sur-
vival and growth). Previous work has considered competitive effects in some detail and specifically
identified algal effects on coral recruitment as a critical aspect and one for which there is little direct
evidence (e.g., McCook et al. 200la).
The present review focuses on effects of benthic alga on larval supply and recruitment, par-
ticularly on (I) habitat for coral replenishment, (2) production of coral larvae and their dispersal ,
(3) coral settlement and (4) post-settlement survival of corals. It is important to note that effects
on different coral life-history stages are cumulative because corals must pass through every stage
successfully to re-establish populations (Hughes & Tanner 2000, Hughes et al. 2000). Given the
considerable diversity of forms of algal assemblage (Table I; Figure 1), the review emphasises the
need to consider the effects of different forms of algae separately. Despite the importance of this
topic, there are surprisingly few published studies (McCook et al. 200Ia and see the section 'State
of knowledge', p. 31). This review therefore has two aims: to review existing research and to provide
a framework and context for future research.
The diversity of algae and their effects on coral replenishment

The benthic algae of coral reefs are extraordinarily diverse, ranging from small filaments a few mil-
limetres high, through thick mats of tough algae, to large forests of leathery macrophytes (Figure I;
Steneck & Dethier 1994, Walters et al. 2003). The nature of algal assemblages dominating degraded
26
ALGAL EFFECTS ON CORAL R EPLENISHMENT AND REEF RESILIENC E
Table 1 Comparison of algal communities resulting on degraded reefs

Dominant Dominant macroalgal
Case study Disturbance(s) macroalgal taxa functional group
Kaneohe Bay, Siltation (dredg in g & land Dicryosphaeria Pulvinate or c ushi o n-like
Hawaii clearing) and e utrophicatio n cavernosa (also
(sewage)' suspension- and
filter-feeding biota) 2
Discovery Bay, Hurricane Allen ( 1981) and Turf algae (controlled Filamento us/EAC
Jamaica reduced herbi vory by grazing o f
( overfi shingjJ Diadema antillarum)4
Further reduction of herbivory: Dicryota, Padina, Corticated foliose, articulated
mass mortality of Diadema Halimeda and calcareo us
antillarum)' Lobophora4
La Saline Reef, C hronic nutrient pollution from Padina, Gracilaria Corticated foliose, corticated
Reunion g roundwater and overfishi ng crassa' macrophyte
-mortality to cora ls from
algal overgrowth 6
Moorea, French Dredging for building materi al Boodlea siamensis, Filamentous (cushion-like), leathery
Polynesia (si ltati on)", coastal develop- Sargassum sp. and macrophyte
ment (sedimentatio n and Turbinaria ornata''
sewage) 8 , agriculture (terres-
tri al run-off), overfi shin g,
Acanthaster planci ( 1982) 9 · 10
Silt-laden wet season run-off2
Malidi, Watamu, Mass bleaching 12 Not reported Filamentous and diminutive algae,
Mombasa & fl eshy algae; mass bleac hing led to
Kisite Marine an increase of turf algae by 88%
National Parks, (3 1% ± 3.7% to 58.5% ± 3.6% mean
Kenya (protected) ± SEM), increase of fleshy algae by
I I 5% (4.5% ± 1.6% mean ± SEM to
9.8% ± 2.3% mean± SEM) 12
Vipingi , Kanamai , Mass bleaching and overfish ing 12 Not repo rted Filamentous and diminuti ve algae,
Ras lwat ine & fleshy algae; mass bleac hing led to
Diani reefs an increase of flesh y algae by 222 %
(non-park, (4.0% ± 3 1.2% to 12 .9 % ±4.3 %
unprotected) mean± SEM) and no signifi cant
change of turf algae after bleaching
disturbance 12
G love rs Reef, Disease & reduction in herbivory Lobophora variegata, Corti cated fo li ose, leathery
Beli ze, Caribbean (by diseases and overfi sh in g) Dicryota. Turbinaria, macrophyte"
Sargassum
San Salvador, Bleaching & hurri canes Not reported Algal turfs, macroalgae and
Bahamas encrusting algae 14
Experimental Mass bleaching of corals, Sargassu m spp . (also Leathery macrophyte, corti cated
si mul at io n of experimental exclusion of large Padina, Lobophora) foliose"
overfi shin g fishes
Note: Macroalgal fun ctional groups are based o n those in Steneck & Dethier's ( 1994) categori sation with pulvinate or cush-
io n-like alga as an additional gro up ( R.S. Steneck personal communication). Superscript numbe rs indicate references
as foll ows: 'S mith et al. 198 1, 2 Done 1992, ' Hu ghes 1994, 4 Hu ghes et al. 1987, ' Less ios 1988, 6C uet et al. 1988,
7Gabrie et al. 1985 , "Salvat 1987, 9 Bouchon 1985, 1°Faure 1989, 11 Payri & Nairn 1982, 12 McCl anahan et al. 200 1,
14
" McC lanahan & Muthi ga 1998, 0strander et al. 2000, " Hughes et al. 2007 and L. McCook (personal observation).
EAC, ep ilithi c algal co mmunit y, diminutive (less than a few em hi gh) algal forms grow ing on the reef substratum .
27
Figure 1 (See a lso Colour Figure I in the insert following p. 250.) Different algal assemblages dominating
reef habitats, creating large differences in the suit ability of the habitat for coral replenishment. A. Crustose
calcareous algae, especially from the Order Coral lina les, form a calcified crust over the substratum and are
genera ll y assoc iated with habitats that promote coral recruitment. (continued on facing page)
28
ALGAL EFFECTS ON CORAL REPLENISHMENT AND REEF RESILIENCE
reefs can differ enormously, depending on factors such as the extent and cause of degradation or
propagule supply (Table 1 and references therein ; Done 1992, McCook 1999). Clearly, such different
forms and assemblages have very different characteristics (Littler et al. 1983, Olson & Lubchenco
1990, Steneck & Dethier 1994) and consequently vastly different effects on coral replenishment
processes (Figures 1 and 2).
Addressing this diversity is a key challenge for understanding algal effects on reefs. With an
estimated 600 species of algae on the Great Barrier Reef (Diaz-Pulido & McCook in press), spe-
cies-level treatment is not practical and higher taxonomic distinctions are not well correlated with
ecological traits (e.g., a small area of filamentous turfs may include 30-50 species from a wide
range of families and phyla). Algal characteristics most relevant to ecological processes are not the
traits linked to taxonomic categories but include physical (e.g., height, structure, growth form) and
chemical traits (e.g. , production of allelopathic chemicals). Most of the relevant physical attributes
are effectively captured in the commonly used 'functional groups' (Littler 1980, Littler & Littler
1980, Littler et al. 1983, Carpenter 1990, Olson & Lubchenco 1990, Steneck & Dethier 1994),
which have been previously used to summarise and simplify algal-coral interactions (McCook et al.
200la). Chemical traits are more difficult to simplify because secondary metabolites are often spe-
cies specific (e.g., Walters et al. 2003, Kuffner et al. 2006). The algal functional groups of Steneck
& Dethier (1994), listed in Table 2, are used primarily in this review, with reference to individual
taxa where necessary.
Coral replenishment processes, resilience and terminology

Terminology in this review closely follows that defined by Harrison & Wallace (1990). Coral replen-
ishment makes combined reference to larval supply, settlement, and post-settlement processes. In
the context of this review, effects of algae on larval supply include impacts on reproduction, fecun-
dity and dispersal. Two reproductive modes are distinguished for corals: spawning refers to gamete
release from parent coral polyps followed by external fertilisation and development; brooding refers
to development of planulae larvae within the parent coral polyp, which are generally competent to
settle soon after their release. Settlement involves the attachment of coral larvae to the substratum.
?resettlement behaviour refers to intensive testing and searching behaviour and exploration of the
substratum by larvae that generally precedes settlement. Often used synonymously with settle-
ment, metamorphosis involves morphological changes such as differentiation of aboral epidermis
in preparation for skeleton deposition, and consolidates settlement to form a spat. Settlement can
reverse, with larvae detaching and returning to presettlement behaviour under unfavourable con-
ditions (Sammarco 1982, Richmond 1985, Yermeij & Bak 2002). In this review, settlement and
Figure I (conTinued) B. Filamentous algal turfs , closely cropped by herbivorous fishes and sea urchins, cre-
ate a low turf (1-5 mm in height), which is compatible with coral recruitment. C. Aggregations of cyanobac-
teria (microalgae) may form longer filaments (30-100 mm in height) and often generate hostile chemical
conditions. D. Thick mats of larger, more robust corticated algae may create a dense layer over much of the
reef substratum (50-150 mm in height), trapping sediments and generating chemical and nutrient conditions
that may be inimical to coral seltlement and early recruits. E. A dense mat of the ephemeral, corticated brown
alga, Chnoospora implexa, covering large areas of reef and live corals (up to 500 mm high). Because this mat
was highly seasonal, and short-lived, it subsequently disappeared, with lillie apparent impact on the underly-
ing corals. The impact of such a mat on coral replenishment would depend strongly on the timing of the bloom
relative to coral spawning and settlement. F. Dense mat of the corticated, foliose brown alga, Lobophora
variegara, covering corals killed during a mass bleaching event and rendering the substratum apparently inac-
cessible to coral recruits. G. Canopy of the leathery macrophyte, Sargassum (brown alga), which may reach
heights of up to 3-4m and densities of 100 plants m- 2, pre-empting space for coral recruitment and signifi-
cantly altering light and hydrodynamic regimes.
29
Table 2 Summary of literature on coral recruitment, classified by phase of recruitment, and

type of study, against algal functional groups, env ironmenta l and other ecological factors
Recruitment phase Type of study
Early
post-settlement Juvenile Rec ruitment In situ
Larval (<0. 5 cm0) ( 1-5 cm0) on artificial recruitme nt
Factors settlement survival co ral survival surface (on benthos)
Macroalgal functional groups

C rustose
A1ticul ated calcareous
I , ,..... '"· 53. SM. 59.63
3·· 60 .• , ,.,
2 "··'
Mi croalgae 2"·''
Filamentous 354.6U3 314.51. ., 2 '"· 56
Fo li ose 161 ,.o
2" · 53 j 9. 2':1. 55.62 I "T j 9.1 1T.29 . .'\Y
Corticated foli ose
Cort icated macrophytes 3·· 52. 61 49.29.62 I "T j 9. l1 T.29. ;\9
Leathery macrophytes 261. 63 16' 3'· 29 211T. 2H j 9. 11T,29. :w
Environmental factors
)1 7, 24, ｾＵ＠
Sediment 1'6
Light 2"-,.
Pollutant s
Depth ,.,
) 21. 25. 41
2 "· 42 ,,. 7"- 44-49

Disturbance ) 9. 26. 4l
Other/spatial variation 11 7· 1.s. n. 21. 30.12 .

:n. 41. 44, 48. so
(G reat Barrie r Ree f on ly)
Other ecological factors

Grazer damage I" I" I'
Da msel fi sh territo ries I 'o 21 1. 2M
Allelopathy ) 20. '!.7. :'18

2"
Note : Table e ntries give the number of studies found fo r each combinati o n of topics; superscript numbers indicate the rel-
evant references as foll ows: 1Mo rse et al. 1988 , ' Mo rse & Morse 199 1, ' Morse et al. 1994, 4Morse et al. 1996.
' Ra imondi & Morse 2000, 6Heyward & Negri 1999, ' Hughes et al. 1999, ' Sammarco 1980, ' Hughes 1985 , 1989.
1996 (based on related data), 10 Potts 1977 , 11 Mille r & Hay 1996, 12 Rylaarsdam 1983, 1' Sammarco & Carleton 198 1,
14
Birke land 1977, '' Brock 1979, 16Bak & Enge l 1979 , " Babcock & Davies 1991 , " Babcock 1988, 19 Mundy &
Babcock 2000, '°Fearon & Ca meron 1996, 21 Re iche lt-Brushett & Harriso n 2000, 22 Ku ffne r 200 I, ''Sammarco 199 1.
24Hodgson 1990, "Epstein et al. 2000. '"Mumby 1999, 27 Hu ghes et al. 2000, 2' G leason 1996, " Connell et al. 1997,
2004, ·" 'Harriott & Fi sk 1988 , " Maida et a l. 1995a, b, '' Fi sk & Harri ott 1990, " Sammarco & Andrews 1989, 34 Mun dy
& Babcock 1998, " Gilmour 1999, '"Negri et al. 200 I, "Fearon & Cameron 1997, " Koh & Sweatman 2000, " Tanner
1995, '"'Fairfull & Harri ott 1999, 41 Negri & Heyward 2001, 42 Babcock & Mundy 1996, " Dunstan & Joh nson 1998.
44
Harriott 198 5, 45 Wallace & Bull 198 1, 46 Wallace 1985a, 47 Wallace 1985b, 4' Banks & Harriott 1996, 49 Harriott 1992,
50 Baird & Hughes 1997, 51 KutTner & Paul 2004, 51 Kuffner et a l. 2006, " Ba ird & Morse 2004, ;., Birrell et al. 2005,
55 Edmunds & Carpenter 200 1, 56 Yan Moorse l 1985, " Miller & Barimo 200 1, ''Kitamura et al. 2007 , " Harrin gton
et al. 2004, 60 Nugues & Szmant 2006, 61 Yermeij et a l. in review, 62 Box & Mumby 2007 , 63Maypa & Ray mundo 2004.
Superscript T indi cates tempe rate latitude zone study. Note that studies of recruitment on artifi cial substrata (e.g. ,
cerami c settle ment plates) may be co nfo unded by the material of the substrata, and in situ studies may mi ss many
small and cryptic recruits. Both approaches may confound differences in sett le ment wi th post-settlement m01tality.
Lite rature survey post- 1978 ; for e nvironme ntal and other ecological factors su rvey is not co mprehe nsive because
recent publications numbe r in the hundreds: survey illustrates propmtional researc h effort; some studies are repo1ted
in more than one reference.
30
metamorphosis are treated together. Post-settlement survival refers to the levels of survival and
mortality after settlement (e.g., due to environmental disturbance, competition with other organ-
isms) and may vary strongly with size or age of the coral. Post-settlement survival is generally
used more specifically to refer to the dynamics of corals not visible in situ with the naked eye
(i.e., <0.5 em in diameter or approximately 6 months after settlement; e.g., Wilson & Harrison
2005), whereas recruit survival generally refers to the dynamics of corals visible in situ (generally
with diameters >0.5 em and more than 6 months after settlement; e.g., Hughes et at. 2007). In the
literature, data on coral recruitment often refer to identification of corals when visible in the field ,
photographs or on retrieved surfaces (i.e., diameter greater than -0.5 em; Wallace l985b), with
limited capacity to distinguish the dynamics of settlement and those of post-settlement growth and
survival. Thus effects reported on recruitment may arise from the effects on either the settlement
or post-settlement stage.
State of knowledge
The effects of benthic algae on coral replenishment are inadequately studied given their importance
to reef ecology and persistence. There are relatively few published stud ies that directly address these
effects and those few address only a fraction of benthic algal species and provide very uneven cov-
erage of different algal types, environmental influences or coral life stages (Table 2). This makes it
very difficult to detect and describe even preliminary patterns (Table 3).
Although it is widely accepted that benthic algae have predominantly negative effects on coral
recruitment during reef disturbance and degradation (e.g., McCook et at. 200la, Mumby et at.
2007), research to date has focused strongly on the induction of coral settlement by crustose calcar-
eous algae (CCA*) in the Order Corallinales (Tables 2, 3 and 4), with relatively few detailed studies
of coral settlement using the algae commonly present during reef degradation. In contrast, most
research into algal effects on post-settlement survival and growth has focused on large, fleshy algae,
with turfing and crustose forms under-represented. Importantly, much of the evidence for algal inhi-
bition of coral recruitment stems largely from field surveys of Caribbean reefs using visua l or photo-
graphic methods that only detect recruits at approximately 6 months post-settlement (>-0.5 em; e.g.,
Hughes 1989, 1996, Edmunds & Carpenter 2001, Edmunds 2002), preventing distinctions between
effects on settlement and post-settlement survival (see Harrison & Wallace 1990; similar limita-
tions apply even to studies using microscopic examination of artificial substrata if post-settlement
morta lity is not monitored). There is even less direct information available on the effects of algal
assemblages on 'supply-side' processes of fecundity and larval dispersal and survival.
Another knowledge gap involves interactions and synergies between algal effects and other
stressors on coral replenishment (but see Birrell et at. 2005). Finally, the tendency for under-report-
ing of 'negative' results, showing no effect for a particular factor (Underwood 1999), means that
reviews such as this may under-represent aspects where good resea rch methods have shown the lack
of effects. Overall, there is a need for significant further research into algal effects on coral replen-
ishment, using a broader range of algal types, distinguishing between effects on different coral
stages and exploring the different mechanisms for those effects.
Given the paucity of direct evidence for algal effects on coral replenishment, the review begins
with a summary of evidence for effects of algae on physical and chemical aspects of habitat condi-
tion and considers how that evidence may be relevant to coral replenishment. The effects of envi-
ronmental conditions and pressures on coral replenishment have been reviewed elsewhere (e.g.,
Harrison & Wallace 1990, see also Table 2).
' Note that throughout this review, CCA is used to include all crustose. calcareous algae, including those in the Order
Corallinales, but also taxa such as Peyssonnelia, from other taxonomic groups ; 'coralline· is used to specify taxa from
the Order Corallinales.
31
Figure 2 (See also Colour Figure 2 in the insert.) Disturbance, algal colonisation and effects of algae on
coral recruitment. A. Colonisation of severely bleached coral tissue by fine filamentous algae. Disturbances
that lead to coral tissue death usually result in colonisation of exposed coral skeleton by some form of ben-
thic algae. Subsequent succession may result in very different algal assemblages, with very different conse-
quences for coral replenishment. B. Overgrowth of damaged corals by the corticated, foliose brown alga,
Lobophora variegata , has dramatically reduced substratum available for coral settlement. C. Healthy coral
recruit attached to a crustose calcareous alga; such algae may enhance settlement of coral larvae. D. Coral
recruit emerging from filamentous algal turf. During settlement and early growth, the smaller coral would
have been more strongly affected by physical and chemical conditions in the turf. (continued on facing page)
32
Effects of macroalgae on habitat conditions

for coral replenishment
Just as trees are critical to the nature of a forest habitat, macroalgae may have major effects on
the physical and chemical conditions of the reef environment, which may in turn affect the larval
dispersa l, settlement and survival of corals (Harrison & Wallace 1990). Although there is a signifi-
cant amount of information on such habitat effects (e.g., Amsler et al. 1992, Martin-Smith 1993),
especially from temperate algal beds (e.g., Reed & Foster 1984, Wing et al. 1993, Valiela et al.
1997, Eckman et al. 2003) the focus here is on key aspects relevant to coral replenishment, that is,
benthic space, light availability, water flow and turbulence, benthic sediment regimes and chemical
environments, including nutrient regimes and microbial environments.
Effects of macroalgae on benthic space

The availability of benthic space, for coral settlement and growth, is strongly limited by algal
assemblages, which occupy much of the substratum on coral reefs. Benthic algae are rapid colonists
of newly available bare space on coral reefs, commencing with diatoms, microbes and cyanobacte-
ria, then simple filamentous algae and CCA, followed by more complex filamentous turfs and per-
haps by larger, more robust algal types (McClanahan 2000, McClanahan et al. 2001, Diaz-Pulido
& McCook 2002, Diaz-Pulido et al. 2007a). Most of the apparent 'bare space' on reefs is in fact
occupied by variable mixtures of CCA and very short, closely grazed filamentous algal turfs, barely
apparent to the naked eye.
The extent to which this space is unavailable to corals will depend strongly on the nature and
density of the algal assemblage; a sparse, close-cropped turf-CCA assemblage will have very dif-
ferent impacts than a dense algal mat, or a bed of large, canopy-forming Sargassum seaweeds.
Most algal assemblages probably do not completely preclude access to substratum for coral larvae,
given their small size (500-2000 11m in diameter; Harrison & Wallace 1990) relative to the spacing
between algal filaments or the hold fast attachments of larger algae (authors' personal observation).
However, dense algal assemblages will certainly hinder access to the substratum. It has been sug-
gested that dense stands of filamentous algae prevent spores of other macroalgae reaching the sub-
strat um (Hruby & Norton 1979, Olson & Lubchenco 1990). In considering space occupied by algae,
it is important to recognise that many algal assemblages form a distinct canopy, whether at the sca le
of tens of millimetres for algal turfs or metres for a Sargassum bed. Space under the canopy may
be rel at ively bare or occupied by understorey species; on the inshore Great Barrier Reef, beds of the
leathery macrophyte Sargassum often have substantial understorey cover of corals, smaller foliose
macroalgae (e.g., Pad ina sp.) and filamentous turfs (authors' personal observation; see also McCook
1999, Hughes et al. 1987, 2007).
Furthermore, not all algal types will preclude coral settlement. Corals can settle and even grow
on several types of macroalgae, primarily calcareous red macroalgae (Morse et al. 1994, Morse
et al. 1996, Heyward & Negri 1999, Raimo ndi & Morse 2000, Harrington et al. 2004), but also fila-
mentous (C. Birrell personal observation) and articulated calcareous green algae (Halimeda spp.;
Nugues & Szmant 2006). However, most filamentous and fleshy algae will not provide suitable
attachment sites for coral colony formation and many taxa have antifouling mechanisms such as
shedding of surface cell layers (Olson & Lubchenco 1990, de Nys & Steinberg 1999).
Figure 2 (continued) E. Acropora corals e mergent from a dense mat of Lobophora variegata (as in Band
Figure I F). F. Leathery macrophytes (e.g., Sargassum) may form a n extensive canopy, but still retain signifi-
cant und erstorey substratum suitable for coral sett lement and recruitment, such as the filamentous turfs s hown
here. G. Trapping of sediments by filamentous algal turfs may enhance stress experienced by coral recruits
a nd sig nificantly reduce the suitability of habit at for their survival and growth.
33
n
Table 3 Summary of evidence for algal effects on coral replenishment: available evidence for interactions between different algal functional ::r:
groups (rows) and different mechanisms of interaction (columns) n0
Mechani sm of macroalgal interaction r
w
-1>- Algal functional group
Overgrowth/
smothering
ｾｨ･ｭｩ｣｡ｬ＠
(alle lopathy) Abrasion
Epithallial
sloughing
Space
pre-emption Shading/ovenopping
Sediment
accumu lat ion
Morphology/
hydrodynamics
-
o:l
;;o
;;o
Microalgae L-M
m
r
S- MS+Jl. 36 r
m
....,
Crustose L-J L- 10
)>
S+'· s. o. 21-.1o. 12. "· 36. 38 S-' · 9 S+'o r
S-5. 2M. 30.33 S-39
PS-I)· J I. 16. 24. 35 . _,7 PS-•· 24 PS+'o
PS+-2,.27 . .11
Anicul ated calcareo us L-7 L-3 L-' o

S- 7 S-.l S+'o
PS -2o.-2.1 PS-20-2.1 PS- 'o
R-'o.-"
Filamentous & diminutive forms L- I. IO.J l.-12
(<2 em) including EAC and turf S- 1. H S+ 10 S- 31 S- 17 · 33 S- 17 S-40 S- 17 · 33 S- 17 S-'o

PS- IｉＮｾｾＭ 16. J5. _,7 PS- '0 PS - 2. " ·"
R+- " ··"
Foliose and conicated foliose L-'-M.-'2 L-8..' 1
(creeping and upright) S-5. 30.42 S+li. 10.:\ I
S-U0..\1
)>
PS- 6· lO-B PS-" PS-' PS-'·•' PS-6. 13. JO-n" PS+'' r
R-6. "·'6 R-6." R-19. zo.-z3. zc> R-6. " ·'6 0
)>
L-42 r
Conicated macrophytes L-'o m
s-•' S- '" 'Tl
'Tl
PS-6.Jo. n PS-6. 10." PS+l' PS-' 0 m
R_ 6. R-6. rs. zs. 26
n
HS. 25. 26 R-6. ''· 1s R-6. IK.25.26 >-l
C/l
R-I IJ. 20.22
0
Leathery macrophytes L- '"·•' L-' o
z
S- 'o .• , S+ '"
n
S-' o 0
;;o
PS-6. 10. n PS- ' 0 PS- 14· 15 PS-6. 20.22 PS - 10 )>
PS+1' PS- 15 r
R-6. HI . 2:'i. 26 R-l 1J.2o.22.26 R-6. 18.25.26
;;o
m
'-o
Note: Effects are indicated by the stage studied : L, e ffects on larval survival or di spersal; S, effects on coral settlement; (PS) effects on post-settlement survival of corals; and R, effects r
w m
Vl on coral recruitment (i.e., cannot di stingui sh between settlement and post-settlement effects). Effects also indicated by the nature of the effect:-, negative impact or inhibition; z
+, positive effect or enhancement; - , ambigu o us interacti o ns. Greyed areas indicate combinations of algae and interactions that are not relevant or possible. Superscript numbers Vi
indicate re ferences as follow s: ' KutTner & Paul 2004 , 1Nug ues & Robens 2003, 3 Littler & Littler 1999, ' Heyward & Negri 1999, 5Baird & Morse 2004, 6Hughes et a!. 2007 ,
::r:
7Nugues & Szmant 2006, ' Kuffner eta!. 2006, "Harrington eta!. 2004, 10Maypa & Raymundo 2004, 11 Bak & Engel 1979, 12 Potts 1977, 11Fairfull & Harriott 1999, 14Gleason 1996, 3:
m
15 River & Edmunds 2001 , 16Sammarco 1991 , 17 Birrell eta!. 2005, "Carpenter & Edmunds 2006, '"Connell eta!. 1997,2004, 20 Hughes 1985, ' 'Hughes 1989, 21 Hughes 1994, z
>-l
23 Hughes 1996, 24Harrington 2004, Steneck eta!. (unpubli shed data), 25 McCJanahan et a!. 2005, 26 M iller & Hay 1996, 27 Morse et a!. 1988, 28 Morse & Morse 1991 , 19 Morse eta!. )>
1994, 30 Morse eta!. 1996, 3' Birre ll 2003, 32 Negri eta!. 200 I, 33 Petersen eta!. 2005, 34 Raimondi & Morse 2000, 35 Van Moorsel 1985, 36 Webster eta!. 2004, 37 Sammarco & Carleton z
0
1981 , 18 Kitamura et a!. 2007, 19 Kitamura eta!. 2005 , 40 Birkeland 1977, "Box & Mumby 2007, 42 Vermeij eta!. in review. ;;o
m
m
'Tl
;;o
m
-
C/l
r
m
z
n
m
Table 4 Summary of evidence for induction o f coral settlement by algal taxon (or microorgani sms associated with algae)
Reprod uctive
Alga l taxo n Group Form Regio n/ocean Study Coral taxon mode
Amphiroa anceps Artie. CoA Dead Indian Lab Acropora millepora 1

s
Hydrolitlwn boergensii CCoA Extract Carib bea n Lab & Aga ricia humilis 2· 4 6, A. ｴ･ｮｴｾｦｯｬｩ｡Ｑ＠
B
field 6
Live intact Caribbean Agaricia humilis 3 B
Dead Caribbean Lab Aga ricia humilis 5 B
Hydrolithon onkodes CCoA Dead Pac ifi c Lab Acropora millepora 1 s
( Poro/itlwn onkodes) Li ve, dead Pacific Lab & field Ac ropora millepora 1 s
1-Iydm /it/wn reinboldii CCoA Dead Pacific Lab & field Acropora tenuis 7, A. millepora 7 s
Extract , dead Pac ific Lab Agaricia humilis 5 B
n
Extract Pac ific Lab Favia favus\ Gonioastrea retifonnis 5, Cyplwstrea sp. 5 s ::c
Live fragment Pac ifi c Lab Acropora digit({era\ A. nasuta'. A. tenuis 5· 7, A. milleporo7, A. florida 5, s n
0
A. gemnufera\ A.fomw.w '. A. hyacinthus5, A. sp. J5, A. sp. 45, A. sp.
8\ A. sp. 95, A. sp . 10\ A. sp. 11 5
r-
cc
w 1-! ydm/itlwn sp. CCoA Li ve Pacific Lab Acropora pa/ifera 8, Stylophora pistillata 8 B ;;>;:!
0\
Litlwphyllum CCoA Dead Pac ifi c Lab Acropora millepora 1 s ;;>;:!
m
insispidum r
r
Litlwphyllum CCA Dead Ind ian Lab Acropora millepora 1 s m
kotSc/i)'all!/111
,...,
)>
Lobophora variegora" Corticated Live fragment Pacific , Lab Acropora digitifera 5, A. 1Wsuta 5, A. tenuis5, A. florida 5, A. gemmifero\ s r
foliose Caribbean A. fo mwsa5, A. hyacinthus 5, A. sp . I'. A. sp. 4 5 & A. sp . 6 5
Lytlwpore/la CCoA Li ve Pacific Lab & fie ld Acropora milleporo7 s
melobesioides
CCoA Live, dead Pacific Lab & field Acropora tenuis 7, A. millepora 7 s
Mesophyllwn sp. CCoA Live, dead Indi an Lab Acropora mi/lepora 1 s
Neogoniolithon CCoA Dead Indi an Lab Acropora millepora 1 s
brassica-florida
Neogoniolitlum.fosliei CCoA Live Pacific Lab & fie ld A cropora mil/epora 7 s
CCoA Live, dead Pacific Lab & fie ld Acropora tenuis 7, A. millepora 7 s
Peyssonn elia sp. CCA Live fragment Pacific , Lab Acropora digitifera 5 s
Caribbean
CCA Dead, li ve, Indi an Lab Acropora millepora 1 s
extrac t
Live fragment Pac ific , Lab Acropora nasuta 5, A. ten uis 5 , A. florida '. A. gemmifera 5, A. formosa 5, s
Caribbean A. hyacinthus 5, A. sp. 15, A. sp. 4 5 & A. sp. 7 5
Dead Pacific, Lab Agaricia humilis 5 B
)>
Caribbean
r
Extract Pacific, Lab Faviafavus 5, Gonioastrea retiformis5 , Cypllllstrea sp. 5 s C)
)>
Caribbean r
Dead Indian Lab Two mixed species spawning slicks' s m
'T]
Live Pacific Lab Acropora palifera 8, Stylophora pistillata 8 B 'T]
m
Porolithon sp. CCoA Live Pacific Lab Acropora palifera 8, Stylophora pistillata 8 B n
-3
CCoA Li ve Caribbean Lab & field Agaricia hwnilis9 B Cll
Tirwwdenna pmtotypwn CCoA Live, dead Pacific Lab & field Acropora tenuis1, A. millepora1 s 0
Mixed CCoAb CCoA Live Caribbean Lab& field Agaricia danai9 , A. humilis9, A. tenuifolia9 B
z
n
CCoA Dead Caribbean Lab & field Agaricia tenuifolia 9 B 0
:;tl
Mixed CCoN CCoA Live Pacific Field Acroporidae 10 , Poritidae 10 , Pocilloporidae 10 SB )>
Live Caribbean Field Agaricidae 10 , Poritidae 10 , Favidae 10 , Acroporidae 10 SB r
:;tl
Mixed CCoA CCoA Extract Pacific Lab Pseudosiderastrea tayamai 11 s m
'"0
Bacteria from H. Bacteria Live Pacific Lab Acropora mil/epora 12, A. willisae' 2 s r
w
__, onkodes m
z
Bacteria from Bacteria Live Pacific Lab Acropora microphtlwlma" s U3
Litlwphyllwn sp. ;:r:
Biofilm on Millepora Bacterial Live Agaricia danai9 , A. hwnilis9, A. tenuifo/ia 9
3:
Caribbean Lab & field B m
complanata skele10n microalgae z
-3
Dead Caribbean Lab & field Agaricia danai9 , A. tenuifolia 9 B )>
CCoA sp.l CCoA Live, extract Caribbean Lab & field Agaricia humilis 9 B z
0
CCoA sp.4, sp. 5 CCoA Live Caribbean Lab & field Agaricia humilis 9 B :;tl
m
Note: All algae are calcified except Loboplwra va riegata and bacteria or microalgal communities. Coral reproduction modes areS (spawning taxa) and B (brooding taxa). Superscript m
'T]
numbers indicate references as follows : ' Heyward & Negri 1999, 2 D.E. Morse & Morse 1991 , 3Steneck & Morse (unpublished, cited in D.E. Morse & Morse 1991 ), ' D.E. Morse :;tl
et al. 1994, 5 A.N.C. Morse et al. 1996, 6 Raimondi & Morse 2000, 7 Harrington et al. 2004, 8 Baird & Morse 2004, 9 D.E. Morse et al. 1988, '0 R.S . Steneck et al. (unpublished data), m
Harrington 2004, "Kitamura et al. 2007, "Negri et al. 2001, "Webster et al. 2004. ｾ＠
CCA , crustose calcareous algae; CCoA, crustose coralline algae.

-z
r
m
n
m
a Lobophora va riegata was observed to induce initial stages of larval metamorphosis by Morse et al. ( 1996); see text p. 43 for funher discussion .
h Algae on Millepora complanata skeleton .
' Algae on settlement tiles.

Impacts of macroalgae on light conditions

Most macroalgae create shade on spatial scales relevant to coral larvae and recruits and so may
affect photosynthesis, as well as factors such as ultraviolet radiation stress, calcification, localised
temperatures and visibility of corals to predators. Although there is little direct evidence relevant to
coral reefs, recent results (Box & Mumby 2007) have shown strongly detrimental effects of shad-
ing by the brown foliose algae Lobophora variegata and Dictyota pulchella. The extent and nature
of shading will vary considerably between algal functional groups and will depend more on the
nature and density of the entire algal assemblage than individual algae (Reed & Foster 1984, Wing
et al. 1993, River & Edmunds 2001, Quan-Young & Espinoza-Avalos 2006). Upright algae such as
leathery macrophytes (e.g., Sargassum) and algae with foliose morphologies (e.g., Padina, Ulva)
can individually shade substratum at scales of square centimetres to square metres, yet assemblage
canopies may shade entire reef zones, especially in the case of algal phase shifts (Hughes et al. 1987,
authors' personal observation). Filamentous algae, articulated calcareous algae (e.g., Amphiroa) and
corticated macrophytes (e.g., Hypnea, Dictyota) are likely to create smaller and less-continuous
areas of shade (10-2 to 101 cm 2). Smaller algal assemblages will generally have less tissue to absorb
light, and hence create less shade, although this will depend on the density of the algal assemblages.
For example, articulated calcareous algae (Halimeda) can form dense enough stands to strongly
block out light (Hay 1981).
Importantly, shading by algal canopies will affect the spectral quality of light transmitted and
reflected, absorbing most strongly in the photosynthetic wavelengths, with consequences for coral
photosynthesis. Both light intensity and spectral quality are cues for habitat selection during settle-
ment of corals (Mundy & Babcock 1998), so that these impacts may also affect larval presettlement
behaviour and settlement preferences.
Furthermore, shading by algae may not be exclusively detrimental. Although light is important
for coral photosynthesis and calcification (Barnes & Chalker 1990), strong light levels can have
energetic costs, due to photoinhibition (Hoogenboom et al. 2006), and in extreme circumstances
may overload the photosynthetic system, causing coral bleaching (Lesser 1997). Thus high light
environments may favour development of coral colonies with self-shading morphologies (Oliver
et al. 1983, Titlyanov 1991, Muko et al. 2000, Anthony et al. 2005), and, in some circumstances,
shading by algae during mass bleaching has been shown to increase survival in mature (Jompa &
McCook 1998) and juvenile corals (up to 130 days old; Birrell 2003). However, it should be noted
that these benefits are probably outweighed by other, negative impacts in the long term.
Impacts of macroalgae on water flow and turbulence

Different algal assemblages may have major effects on water fiow speeds, gradients and turbu-
lence, with potentially important consequences for coral replenishment. Water fiow, gradients and
turbulence affect the physical dispersal and settlement ability of larvae (reviewed by Abel son &
Denny 1997), and the development and survival of settled individuals, through effects on exchange
of nutrients and other chemicals, important to rates of photosynthesis and respiration (Barnes &
Chalker 1990, Kuhl et al. 1995), and to the intensity of algal chemical interactions (e.g., allelopathy).
Nutrient and carbon exchange may have significant impacts on rates of photosynthesis and respira-
tion, in turn affecting coral energy budgets, potentially critical to the survival of juvenile corals.
Water fiow patterns are also critical to sediment deposition or abrasion (see next section) and other
physical interactions (e.g., whiplash by algal fronds; Anthony & Svane 1994, Vogel 1994, River &
Edmunds 200 1).
The scale of algal impacts on fiow dynamics is largely determined by the height and struc-
ture of the algal assemblage and so can be expected to differ markedly between algal functional
38
groups. Kelp forests can influence coastal water circulation patterns (Jackson & Winnant 1983)
and leathery macrophytes such as Sargassum spp. can influence water flow within metres to deci-
metres of the substratum (Duggins et al. 1990; Sargassum beds, which may reach 3 m tall, are com-
mon on coastal coral reefs and may develop during algal phase shifts; e.g., McCook 1996, Hughes
et al. 2007). Filamentous algae affect water flow within microns to millimetres of the substratum
(Carpenter & Williams 1993, Larkum et al. 2003). Indeed Carpenter & Williams (1993) demon-
strated filamentous turfs 4.0-6.0 mm in height can have major effects on boundary layer formation,
reducing flow speeds up to 15-fold within 3.0 mm of the surface of settlement tiles relative to above
free-stream flow speeds.
Algal impacts on water flow are also strongly influenced by algal morphology and texture (e.g.,
Abelson & Denny 1997), so that even crustose algae can significantly affect boundary layer water
flow and turbulence. By enhancing the small-scale complexity of the surface, crustose algae gener-
ate variable-flow regimes in pressure points, eddies and sheltered pockets (Carpenter & Williams
1993, Vogel 1994, Abelson & Denny 1997). Vogel (1994) discusses algal adaptations to flow regimes
and how roughness of surface features affects drag created in water. Put simply, morphologies with
greater drag (i.e., less streamlined) have larger effects on flow regimes. It is also worth noting that
epiphyte loading in algal canopies increases drag, generating greater downstream turbulence (Vogel
1994) although greater flow speeds can dislodge epiphyte communities (e.g., Bergey et al. 1995).
These effects on water flow occur at scales relevant to coral settlement and recruitment. The
height of coral recruits ranges from microns at settlement, to centimetres after the first few years
growth, so that they will be influenced by the effects on boundary layer dynamics and water flow
gradients of even very short algae (e.g., filamentous turfs; Larkum et al. 2003).
Impacts of macroalgae on benthic sediment regimes

The effects of benthic algae on water flow may also affect sediment transport, and hence scour-
ing and abrasion, and sediment deposition and resuspension (discussed above; see also Abelson
& Denny 1997). Benthic algae may also trap sediments, enhancing sediment deposition, and may
influence sediment composition and chemistry, with potential impacts on coral life stages ranging
from gamete fertilisation (Gilmour 1999) and larval settlement (Babcock & Davies 1991, Birrell
et al. 2005) to coral growth and survival (Rogers 1990, Riegl & Branch 1995, Fabricius et al. 2003,
Nugues & Roberts 2003, Fabricius 2005).
Generally, increased turbulence and flow speed promote transport and resuspension of sedi-
ments (Abelson & Denny 1997). This reduced turbulence and flow may reduce resuspension
between algal holdfasts (Steneck 1997). This from algal surfaces (Stamski & Field 2006), trap-
ping sediments and enhancing deposition , with consequent impacts on coral replenishment. Purcell
(2000) observed that sediment load in filamentous turf and diminutive algal assemblages increased
with assemblage height across reef zones. Indeed, the relationship was approximately linear for all
zones (reef base, fore-reef flat and mid reef flat) except the reef crest, where Purcell (2000) suggested
that higher wave energy disproportionately limited sediment accumulation (algal heights <0.2 em
as opposed to 0.7-0.8 em in other zones). Note, however, that potential feedback interactions are
possible. In more turbulent areas such as reef crests, wave action may limit the height and density
of algal assemblages, further limiting sediment trapping and accumulation (Cheroske et al. 2000,
Becerro et al. 2006).
In contrast, in less-turbulent areas, sediment trapping by filamentous turfs may serve to anchor
the assemblage, facilitating its growth and promoting algal overgrowth of corals or other organ-
isms. This may even overwhelm defensive processes such as sloughing of coral mucus (McCook
2001, Nugues & Roberts 2003) or epithallial cell layers of crustose coralline algae (Steneck 1997).
39
Nonetheless, Purcell (2000) observed sediment loads to be least on substrata with relatively high
coverage of crustose algae, apparently as a result of their Iimited potential to trap sediments com-
pared with filamentous turfs.
Potential indirect effects of algae on the composition of trapped sediments may arise from
ecological interactions between algae and other organisms such as herbivores. Different grazers
favour different algal assemblages (e.g., Chittaro 2004 for parrotfishes), and grazing patterns can
affect sediment composition through accumulation of faecal material. For example, Petersen et al.
(2005) report the accumulation of faeces from grazing hermit crabs in sediments amidst algal turfs,
and grazing and defaecation by parrotfishes can produce large amounts of carbonate sediments
(Bellwood & Choat 1990, Bellwood 1996).
Finally, algal impacts on sediment regimes may have more complex effects if the trapped sedi-
ments bind with chemicals such as nutrients, pesticides or other toxicants, increasing their retention.
These pollutants generally have detrimental impacts on coral survival and replenishment (Epstein
et al. 2000, Reichelt-Brushett & Harrison 2000, Negri & Heyward 2001, Furnas 2003, Negri et al.
2005, Markey et al. 2007) and sediment derived from terrestrial run-off from agriculture often con-
tains high levels of such pollutants (Haynes & Michalek-Wagner 2000, Ramade & Roche 2006).
Impacts of macroalgae on chemical environments,

including nutrient regimes
Macroalgal assemblages can have major effects on habitat chemistry and nutrient regimes, including
effects on waterborne chemicals and nutrients; effects on particulate sediments, either suspended
or as deposits; and effects on the surface area for settlement (e.g., due to surface chemistry of crus-
tose algae; Amsler et al. 1992, Larkum et al. 2003, Walters et al. 2003). Many of these effects will
influence fitness or fecundity of adult corals, or dispersal, survival or settlement and post-settlement
survival and growth of coral larvae. Algal effects on chemical environments may derive directly
from the biological properties of the algae, or from their effects on water flow, mixing and diffusion
gradients, and sediment accumulation. During photosynthesis and respiration, macroalgae use or
produce carbon dioxide and oxygen alternately, simultaneously fixing nitrogen (for cyanobacteria
only), phosphorous and carbon, thereby generating localised gradients in oxygenation and nutrient
concentrations that radiate from individual algae and assemblages (reviewed in Carpenter et al.
1991, Amsler et al. 1992, Larkum et al. 2003). Furthermore, algal alterations of environmental
chemistry (alkalinity-acidity ratios) may affect coral calcification, and non-calcareous algae can
even stimulate calcification in nearby corals enhancing their growth (McConnaughey et al. 2000).
The nature and importance of these effects may be significantly altered by ocean acidification due
to climate change (Diaz-Pullido, McCook et al. 2007).
Impacts ofmacroalgae on microbial environments

An emerging area of research involves interactions between macroalgae and microbial environ-
ments for corals. A series of studies have shown detrimental microbial colonisation of live corals
to be enhanced by macroalgae (Nugues et al. 2004), apparently due to release of organic carbon by
benthic algae (Kline et al. 2006, Smith et al. 2006). Recent work has found complex interactions
between macroalgal and microbial effects on coral larval survival and settlement (Yermeij et al. in
review). A number of studies have suggested coral settlement to be induced by microbial biofilms
associated with coralline algae (Heyward & Negri 1999, Negri et al. 2001 , Webster et al. 2004). The
emerging evidence for links between macroalgae and microbial assemblages suggests these effects
are of considerable ecological significance, but current results are extremely limited, precluding
identification of general patterns.
40
Effects of macroalgae on coral fecundity,

larval dispersal and survival
Reproduction and successful dispersal of coral propagules are crucial aspects of coral replenish-
ment and hence reef resilience (e.g., Karlson 1999, Hughes et al. 2000, 2005, Hughes & Tanner
2000, Knowlton & Jackson 2001). A wide range of environmental stresses (e.g., turbidity, sedi-
ment, reduced light at depth, lesions, bleaching) has been shown to reduce coral reproductive out-
put (e.g., Michalek-Wagner & Willis 2001; review by Harrison & Wallace 1990). Thus, stress or
compromised energy budgets resulting from algal interactions (reviewed in McCook et al. 200lb)
or algal alterations of the habitat (see 'Effects of macroalgae on habitat conditions', p. 33) are likely
to reduce coral reproductive output but there is even less published evidence on these aspects than
for effects on settlement or recruitment. Two studies have demonstrated effects of shading and
abrasion (and potentially chemical effects) on coral reproductive output. Experimental clearance of
algal assemblages (dominated by Halimeda spp., Chlorodesmis fastigiata, Peyssonnelia spp. and
Turbinaria ornata) demonstrated that the algae caused a 50% reduction in release of planulae from
the brooding coral Acropora palifera (Tanner 1995). Hughes et al. (2007) observed algal reduction
of coral fitness (measured as tissue thickness) and reproductive output (egg size, number of eggs per
polyp, number of reproductive polyps per square centimetre) in fragments of the spawning coral
Montipora digitata experimentally transplanted close to the large algae Sargassum spp. and Padina
spp. (in contrast to transplants more distant from the large algae, but still close to filamentous turf
algae).
Also relevant is recent work highlighting the potential for proximity to algae to increase coral
disease. Release of organic carbon from benthic algae has been shown to alter microbial colonisa-
tion of live coral tissue (Kline et al. 2006, Smith et al. 2006), in some cases causing coral mortality.
In another study, contact with the calcified, upright green alga Halimeda opuntia caused infection
of the coral Montastraea faveolata by ' whiteplague type II' disease (Nugues et al. 2004).
Algal effects on fecundity can be expected to vary considerably among coral and algal taxa. For
example, coral taxa vary in capacity to compensate for effects of stress on reproductive output (e.g.,
Cox 2007), algal impacts on mature corals vary considerably (McCook et al. 200la) and reproduc-
tive output varies amongst corals (Hall & Hughes 1996).
The fertilisation and survival of reproductive propagules may be affected directly by algal
release of waterborne chemicals or by indirect environmental effects. Many reef macroalgae have
been shown to release waterborne chemicals (including allelopathic secondary metabolites; Walters
et al. 2003, Gross 2003) and such chemicals have been shown to be deleterious, even lethal , to a
range of invertebrate larvae (Walters et al. 1996, reviewed by de Nys & Steinberg 1999, Gross 2003)
but there are only a few reports specific to corals. Waterborne chemicals from Sargassum polycys-
tum and Laurencia papillosa killed unsettled larvae of Pocillopora damicornis over 24 h (Maypa &
Raymundo 2004). Chemicals released by the cyanobacterium Lyngbya majuscula also killed larvae
of Acropora surculosa and Pocillopora damicornis (Kuffner & Paul 2004). Extracts from some
CCA showed toxic activity against coral larvae (Kitamura et al. 2005). Significantly, recent results
have found macroalgae to have serious, indirect detrimental effects on coral larval survival, appar-
ently due to enhancement of microbial densities in the water (Yermeij et al. in review).
Indirect effects on fertilisation by effects of algae on habitat conditions have not been specifi-
cally demonstrated but many of the effects discussed in the previous section have been shown to
reduce fertilisation success of coral gametes. Examples include the effects of sediment regimes
(Gilmour 1999), light and ultraviolet radiation levels (Edmunds et al. 2001), nitrogen and phos-
phorus levels (Harrison & Ward 2001) and exposure to toxicants such as insecticides, fungicides
(Markey et al. 2007), antifoulants (Negri et al. 2001) and herbicides (Negri et al. 2005).
41
Larval dispersal is dependent on water movement and circulation patterns (Oliver & Willis
1987, Willis & Oliver 1990, Abelson & Denny 1997, Storlazzi et al. 2006). Water movements may
affect gamete dilution and fertilisation success (e.g., Oliver & Babcock 1992), delivery or retention
of larvae on a reef and larval vulnerability to benthic (Lindquist 1996, Fabricius & Metzner 2004)
and near-reef predators (Baird et al. 2001, Pratchett et al. 2001). Although there is currently no
evidence to suggest the specific nature or importance of these indirect effects, it may be that effects
of algal canopies on larval delivery at small scales explain the pattern of reduced coral settlement
under Sargassum canopies (Jompa 2001).
Effects of macroalgae on the settlement of coral larvae

There is more published research available on algal effects on coral settlement than on the supply-side
or post-settlement stages. Recent work has expanded the geographic scope of such studies, includ-
ing work from the Caribbean (Kuffner et al. 2006, Nugues & Szmant 2006), Hawaii (Vermeij et al.
in review), Guam (Kuffner & Paul 2004), the Great Barrier Reef (Birrell 2003, Birrell et al. 2005,
in review) and Ningaloo reef in Western Australia (eastern Indian Ocean; Heyward & Negri 1999).
However, this work is disproportionately dominated by studies of enhancement by coralline algae
(Tables 2 and 4). Only relatively recently has there been significant attention paid to the effects of
algae involved in reef degradation, and this work remains insufficient to demonstrate clear patterns
or relationships, such as between algal functional groups and different mechanisms for algal effects
(Table 3; Appendix). Even at the level of functional groups, several mechanisms have not been stud-
ied at all. Relatively few algal taxa have been studied, although effects on settlement may be relatively
specific (e.g., Harrington et al. 2004, Maypa & Raymundo 2004, Kuffner et al. 2006, Nugues &
Szmant 2006). For example, crustose coralline algae are often lumped in assemblages, yet one or two
species may play a fundamental role in coral settlement whereas others can be deleterious to coral
settlement or post-settlement survival (e.g., Suzuki et al. 1998, Harrington 2004, Harrington et al.
2004, Kim et al. 2004, Kitamura et al. 2005).
In the few cases that have received repeated attention, effects appear variable, even contrasting
or inconsistent, even for the same alga. For example, the foliose brown alga Lobophora variegata ,
widespread on damaged reefs, has been variously shown to have both positive (Morse et al. 1996,
Birrell et al. in review) and negative (Baird & Morse 2004, Kuffner et al. 2006) effects on coral
settlement. Certainly, effects can vary considerably amongst algal taxa (Birrell et al. in review).
There is also discussion about the extent to which enhancement of settlement by crustose coral-
line algae is due to properties of the algae or of microbial biofilms present on the algae (see next
section). The extent to which these apparent inconsistencies represent different processes, vari-
ability among individuals, or differences in methods remains unclear. For example, many studies
use artificial substrata to facilitate microscopic examination, yet recruitment on to such substrata
is often very different from that on natural substrata (often predominantly CCA; e.g., Morse et al.
1988, Mundy 2000, Raimondi & Morse 2000, Birrell et al. in review).
Positive effects of macroalgae on coral settlement

As many as 25 algae, primarily calcareous red algae (CRA) and in particular crustose coral! ine algae
have been observed to induce settlement of coral larvae (Table 4), although some controversy sur-
rounds the identification of specific mechanisms for this induction. Morse et al. (1988, 1994), Morse
et al. (1996) and Morse & Morse ( 1991) suggested that coral settlement is induced by polysaccha-
ride morphogens found in cell walls ofCRA from both the Caribbean and the Pacific. In contrast,
Heyward & Negri (1999), Negri et al. (2001) and Webster et al. (2004) suggest the morphogens that
42
induce coral settlement may be less specific and originate from bacterial communities associated
with CCA and possibly coral skeletons. Furthermore, Baird & Morse (2004) noted greater settle-
ment (up to 80% ± 20% mean± standard error of the mean [SEM]) in unfiltered versus filtered (0.2
11m) seawater, suggesting a role for waterborne molecules. Negri et al. (2001) observed relatively
specific settlement induction by I out of20 bacterial strains (Pseudoalteromonas Strain A3 isolated
from the coralline CCA Hydrolithon onkodes). Indeed, both algal and bacterially derived induction
may operate simultaneously, or perhaps at different timings or spatial scales, and understanding of
this aspect will clearly develop further as new studies emerge. The chemical recognition of settle-
ment cues or morphogens may be common to all scleractinian corals regardless of mode of repro-
duction (brooder or gamete spawner) or geographic origin (Morse et al. 1996). Table 4lists records
of observed response to induction by 26 species of corals, and up to 55% of coral larvae collected in
wild slicks were induced to settle in response to crustose coralline algae (Heyward & Negri 1999).
Corals can demonstrate varying degrees of specificity in responses to inductive cues from crus-
tose coralline algae, but some corals do appear to prefer a few specific algae. Baird & Morse (2004)
observed metamorphosis of Acropora palifera in response to 3 out of lO algal taxa, but metamor-
phosis of Stylophora pistillata in response to 9 out of lO algal taxa suggesting a more opportu-
nistic life-history strategy. Heyward & Negri (1999) observed settlement and metamorphosis of
Acropora millepora larvae on seven different CRA, including upright, geniculate, branching coral-
lines (Amphiroa) and non-corallines (Peyssonnelia), as well as on coral skeleton and CRA skeleton.
In contrast, Morse et al. (1988) and Morse et al. (1996) observed algal induction of coral settlement
to be relatively specific to algal species. Settlement and recruitment in the field also appears very
species specific (Raimondi & Morse 2000, Harrington 2004, Harrington et al. 2004, on natural
substratum and settlement plates). Heyward & Negri ( 1999) also observed approximately half of the
larvae collected from two different mass spawning slicks of coral larvae to settle on a Peyssonnelia
sp. (a non-coralline crustose red alga; Ningaloo Reef, Western Australia).
Examples of positive impacts on coral settlement from macroalgae other than CRA are relatively
scarce (Table 4) but do exist and are supported by evidence of algal effects on other invertebrate
larvae. In a study of waterborne influences of macroalgae on settlement of the coral Acropora mille-
para on to the crustose coralline alga Hydrolithon reinboldii, water treated with Lobophora varie-
gata, a corticated foliose brown macroalgae, enhanced settlement and substratum testing behaviour
prior to settlement (relative to controls and other algal treatments; Birrell 2003 , Birrell et al. 2008),
although other algae had inhibitory effects (see next section). In another study of waterborne effects,
L. variegata apparently induced initial metamorphosis features (elongation) of Cyphastrea sp. coral
larvae (Morse et al. 1996); such transformations precede settlement of a coral larva (Harrison &
Wallace 1990). However, Baird & Morse (2004) report apparent avoidance behaviour of coral larvae
in response to fragmented portions of Lobophora variegata. This apparent discrepancy may reflect
differences amongst coral species or stages, or the effects of compounds released in response to tis-
sue damage from fragmentation of the alga.
Nugues & Szmant (2006) report settlement of as many as half of the larvae of the coral Favia
fragum on surfaces of the articulated calcareous green alga Halimeda opuntia, despite availability
of suitable rubble substrata. Coral larvae have also been recorded to settle on the frondose green
alga Ulvafasciata (Yermeij et al. in press); settlement on algal fronds is likely to lead to dislodge-
ment and mortality of the coral recruit. Maypa & Raymundo (2004) found waterborne influences
from the leathery macrophyte Sargassum polycystum (brown alga) and corticated foliose alga
Laurencia papillosa (red alga) to enhance settlement of Pocillopora damicornis (up to 71% ± 4%
mean± SEM, approximately 3-fold relative to controls). Walters et al. (1996) found the macroalgae
Padina australis (corticated foliose brown alga), Hypnea musciformis (corticated macrophyte, red
alga) and Ulva fasciata (foliose green alga) from Hawai'ian reefs provided waterborne chemical
43
cues that enhanced settlement of a polychaete (Hydro ides elegans). Thus algae other than CCA can
provide positive cues for larval settlement. This is a challenging point because many of the above
fleshy algae are characteristic of more degraded reefs, so positive responses may seem counter-
adaptive. However, it may be that such responses are adaptive if they enhance the chances of larvae
finding reef substratum from open water (off reef). Inducers characterised from CRA are generally
insoluble in seawater (e.g., Morse et al. 1988, 1994, Morse et al. 1996) so it may be that signals from
other algae serve to guide larvae in open water towards a reef substratum, before insoluble cues
from CRA are detectable.
Work with algal-associated microbial biofilms and settlement of invertebrate larvae generally
has suggested that these provide cues for invertebrate settlement, as well as the algae with which
they are associated (Hoffman & Brand 1987, Johnson et al. L99La,b). As indicated above, recent
work focused on coral settlement has found this to be partly true for at least three species of cor-
als (Acropora millepora, A. willissae, A. microphthalma; Negri et al. 2001, Webster et al. 2004).
Specific bacteria isolated from CCA (Hydrolithon onkodes) have been identified as inducers of coral
settlement (Negri et al. 2001) and diverse bacterial communities alone (i.e., without calcareous or
crustose algal substratum) have induced coral settlement (Webster et al. 2004). Thus, it is possible
that the presence of microbial biofilms may contribute to the occasional surprising settlement of
coral larvae on the surface of upright algae, such as observed for Halimeda opuntia (an upright,
calcareous green alga unlikely to enhance coral survival; Nugues & Szmant 2006 in Cura<;:ao,
Caribbean; this result probably also reflected the high abundance of planulae in this study, as sug-
gested by the authors, or the presence of epiphytic CCA on the Halimeda). This suggestion is con-
sistent with evidence that waterborne influences from H. opuntia were not found to affect settlement
of the coral Pocillopora damicornis (Maypa & Raymundo 2004, central Philippines).
In summary, although interesting patterns for induction of coral by algae are beginn ing to
emerge, these patterns are based on relatively few examples with many exceptions, the interactions
appear complex and variable, and reliable generalisations are not yet in reach. Fortunately, this is
an area of active research, with well-established methods and techniques, that promises continued
rapid development.
Negative effects of macroalgae on coral settlement

Chemical effects (allelopathy)
Macroalgae may be a source of both waterborne and insoluble (tissue-attached) chemical cues that
may either kill or damage larvae before they arrive and settle or may deter larvae from exploring
a habitat and settling. Such chemical effects have been found in cyanobacteria, microalgae and
macroalgae and have long been accepted to affect settlement of a range of invertebrate larvae (e.g.,
Pawlik 1992 , Walters et al. 1996, 2003, de Nys & Steinberg 1999, Gross 2003), although there
are relatively few studies relevant to algal impacts on coral settlement (Table 3). Kuffner & Paul
(2004) observed that the presence of a cyanobacterium, Lyngbya majuscula, reduced larval sur-
vival of Acropora surculosa and settlement of Pocillopora damicornis on surfaces with high cover
of a crustose coralline alga (unidentified). Kuffner et al. (2006) reported negative influences of
the cyanobacteria Lyngbya polychroa and L. confervoides and several algae (Dictyota pulchella,
Lobophora variegata, and Chondrophycus poiteaui) on presettlement behaviour of larvae of Porites
astreoides, also in the Caribbean. Maypa & Raymundo (2004), also working with Pocillopora dam-
icornis, observed that, although waterborne influences from Sargassum polycystum and Laurencia
papillosa promoted coral settlement, in both cases unsettled larvae died within 24 h and all spat
died after LO days in the Sargassum polycystum treatment. Baird & Morse (2004) observed no
settlement of planulae from either Stylophora pistillata or Acropora palifera in treatments with
fragments of Lobophora sp. and planulae stopped sw imming, sank and remained motionless for
44
ALGAL EFFECTS ON CORAL REPLENISHMENT AND REEF RESfUENCE
the duration of their observations. Birrell (2003) and Birrell et al. (2008) observed that Acropora
millepora larvae avoided substratum testing behaviour in response to waterborne influences from
the alga Chlorodesmis fastigiata, despite the presence of a crustose coralline alga known to induce
settlement (Hydrolithon reinboldii; e.g., Morse et al. 1996, Harrington 2004).
Studies of filamentous algal effects on mature corals have shown some species can cause tissue
necrosis, apparently due to allelopathic chemicals (Corallophila huysmansii and Anotrichium tenue
on massive Porites spp.; Jompa & McCook 2003a,b). It is likely that such effects may inhibit coral
settlement or kill coral larvae upon contact. ft is relevant here that species of crustose coralline algae
have been reported to show allelopathic inhibition of settlement of macroalgae (Suzuki et al. 1998,
Kim et al. 2004). Recent work has shown complex interactions between apparent chemical effects
of algae and effects of microbes on coral settlement (Vermeij et al. in press). This area merits further
research effort because chemically mediated inhibition of coral settlement by macroalgae has the
potential to significantly increase the extent of impacts well beyond their occupation of space, with
serious consequences for coral population replenishment and resilience.
Epithallial sloughing
Algae that periodically shed surface epithallial tissue layers, known as epithallial sloughing, can
effectively reduce fouling organisms (including corals) by providing an unstable and short-lived
surface for attachment (Johnson & Mann 1986, Keats et al. 1997, Littler & Littler 1999, Harrington
et al. 2004). Epithallial sloughing is particularly common amongst crustose coralline algae and
effectively prevents fouling by filamentous and other diminutive forms of algae. Algal overgrowth
of such coralline algae can cause tissue death within 2 wk (Keats et al. 1997). This prevention of
algal fouling may explain why live coralline algae are more appealing to coral larvae than dead
corallines (Morse et al. 1996, Harrington et al. 2004). The mechanism of epithallial sloughing is
predominantly reported for the red algal (Rhodophyta) families Corallinaceae, Sporolithaceae and
Delesseriaceae (Johnson & Mann 1986, Littler & Littler 1999). Although sloughing is occasionally
reported for other taxa, including some brown algae (Phaeophyceae; e.g., Moss 1982), these seem
unlikely to play a major role in coral settlement. Epithallial sloughing may explain strong differ-
ences in suitability of crustose coralline algae as settlement substratum for corals (Harrington 2004,
R.S. Steneck personal communication). Surveys of larval settlement of the corals Acropora mille-
para and A. tenuis on a range of crustose coralline algae demonstrated that those which provide
unstable and renewed surfaces (e.g., Neogoniolithon fosliei, see Littler & Littler 1999) tend to have
reduced settlement, whereas greatest settlement is observed on species that do not slough epithal-
lial layers (Harrington 2004, Harrington et al. 2004, R.S. Steneck personal communication). It is
worth noting, however, that these differences may well reflect post-settlement mortality of spat, due
to epithallial sloughing, and that coral settlement may actually be fairly indiscriminate (Harrington
et al. 2004).
Other habitat effects: shading, pre-emption of space and sediment trapping

Many of the effects of algae on habitats previously identified (see pp. 33-40) can be assumed to
have significant effects on coral settlement but pub! ished demonstrations of such impacts are scarce
(Table 3). Certainly, the presence of algae has been shown to reduce coral settlement but the effects
are variable and precise mechanisms or causes unclear. Birrell et al. (2005) tested the effect of two
different filamentous algal turfs on settlement of the coral Acropora millepora; in one case the turf
inhibited settlement relative to controls with turfs removed, and in the other there was no differ-
ence. Similar results were obtained by Petersen et al. (2005). Experimental removal of Sargassum
canopy enhanced coral recruitment (Jompa 2001) and the development of Sargassum canopy, due
to experimental exclusion of herbivores, caused reduced coral settlement compared with plots dom i-
nated by filamentous turf algae (Hughes et al. 2007), although it is possible that these results reflect
45
post-settlement mortality rather than differential settlement. It would be very valuable to explore the
relationship between inhibition of settlement and the height and density of algal assemblages, both
within and between different algal assemblage types (e.g., comparisons of coral settlement in differ-
ent turfs and between turfs and other algal assemblages such as Sargassum canopies). Birrell et al.
(2005) suggested that the differences in turf height and/or thickness may have caused the different
results for two turfs mentioned above.
Algal pre-emption of space and 'recruitment barriers' have been widely inferred (e.g., McCook
et al. 200la and references therein) but it is not entirely clear to what extent the effect is caused by
physical pre-emption of space or by other factors. Dense turfs of the filamentous alga Enteromorpha
intestinalis in culture apparently inhibited colonisation by spores of the alga Ulothrix pseudojiacca
by space pre-emption (Hruby & Norton 1979, Olson & Lubchenco 1990). McCook et al. (200la)
suggest a continuous macroalgae canopy (e.g., foliose or corticated foliose algae) may reduce lar-
val access to substratum below, and hence inhibit settlement. In the case of crustose algae, closely
adherent foliose forms and thick, dense algal mats, this reduction of access may be effectively
true. However, coral larvae are motile and relatively small (approximately 0.5- to 2-mm diam-
eter; Harrison & Wallace 1990) and so it is questionable whether either a filamentous turf or a
Sargassum canopy could be effectively continuous to coral larvae; theoretically both have sufficient
space between algal thalli for corals to gain access to substratum. Thus space pre-emption may to
some extent be a scale-dependent concept. However, although algal assemblages may not strictly
prevent access of coral larvae to substratum, it is clear that access will be substantially inhibited due
to (I) entanglement, predation or allelopathy within the algal canopy, (2) metabolic costs of actively
navigating through the canopy and (3) habitat effects on chemical and nutrient regimes, oxygen-
ation, hydrodynamics or sediment trapping. The concept of a recruitment barrier may therefore be
more relevant than strict space pre-emption.
Sediment trapping and accumulation by algae are likely to be a major limitation on access to
substratum, potentially acting as a complete barrier, especially on degraded reefs exposed to high
terrestrial run-off. In one of the few studies to consider interactions between human impacts and
algal effects, Birrell et al. (2005) found that sediment trapping by filamentous turfs can reduce
settlement of the coral Acropora millepora.
There is no direct evidence for algal shading affecting coral settlement and many coral larvae
are not photosynthetic (Harrison & Wallace 1990). However, both intensity and spectral quality
can affect coral settlement (Mundy & Babcock 1998) and Baird & Hughes (2000) report that shade
reduced overall coral recruitment by 96% (based on data from underneath plate corals at 2m depth
on a reef crest approximately 8 wk after settlement, so that differences are probably at least partly
due to post-settlement mortality). In contrast, Kuffner (2001) observed that reduced ultraviolet radi-
ation favoured settlement of the coral Po cillopora damicornis. Thus algal impacts on coral settle-
ment through shading are plausible but they are likely to differ between coral species and to depend
on the extent and spectral quality of algal shading. Shading effects on settlement are probably less
significant than shading effects on post-settlement survival and growth as photosynthesis becomes
more important in later stages.
Effects of macroalgae on the post-settlement

survival and growth of corals
The effects of benthic macroalgae on the post-settlement survival and growth of juvenile corals will
be of major importance to the replenishment of coral populations after disturbances, in part because
coral recruits are more vulnerable to a broader range of impacts than established corals. However,
once again, these conclusions are based as much on conceptual considerations as empirical evi-
dence due to the scarcity of published research (McCook et al. 200la, Table 3, Figures l and 2,
46
but see Box & Mumby 2007). In contrast to studies of settlement, studies of recruitment and post-
settlement have favoured larger-bodied upright fleshy algae (foliose and corticated foliose, leathery
macrophytes), typical of 'phase shifts', mostly as a result of dramatic and long-term degradation of
Caribbean reefs (Table 3). Significantly, coral post-settlement dynamics are of much longer dura-
tion, up to years, in contrast to the days to weeks between larval release and settlement (Harrison &
Wallace 1990), so that effects have longer to accumulate.
Algal effects on post-settlement survival of corals seem to be generally negative. The majority
of studies in Table 3 reported impacts varying from mortality to reduced growth. It is important
to consider sublethal effects as well as effects on survival/mortality because reduced growth rates
or fitness may have important long-term consequences for population-level recovery (e.g., Box &
Mumby 2007). Examples of neutral or positive effects include survival of recruits on crustose and
thin filamentous turfs (Birrell 2003, Harrington et al. 2004); algae sheltering or obscuring recruits,
thus protecting them from damage by grazing herbivores or corallivores (e.g., Bak & Vaneys 1975,
Bak 1994, Miller & Hay 1998); and shading of coral recruits from bleaching damage (Birrell2003,
and by analogy to Jompa 2001 for established corals).
Direct effects of algae on coral recruits (e.g., abrasion, overgrowth, epithallial sloughing) have
received more attention than potential indirect effects, such as changes to physical and chemical
habitat conditions or grazing regimes. However, as shown (pp. 33-40), changes to light levels, flow
rates, chemical and nutrient regimes and sediment accumulation will all have potentially power-
ful impacts on fitness and growth of juvenile corals, and these warrant direct investigation. Other
examples of possible indirect effects include incidental ('collateral') damage to recruits from grazers
feeding on adjacent algae (e.g., Bak & Vaneys 1975, Bak 1994) or obscuring of recruits (preceding
paragraph). Potts (1977) suggested that damsel fish behaviour may facilitate algal impacts on corals
by favouring accumulation of algal biomass, although territorial defence may also reduce damage to
coral recruits from larger herbivores (Sammarco & Carleton 1981 ; see also Ceccarelli et al. 2001).
Note that most of the preceding examples provide circumstantial evidence only and such indirect
effects warrant direct investigation in the specific context of coral replenishment.
Mechanisms for algal effects on post-settlement corals

The mechanisms for direct impacts of algae on coral recruits are essentially those identified for
mature coral-algal interactions (McCook et al. 2001b), namely overgrowth/smothering, shading,
abrasion and chemical effects (but omitting recruitment barriers and epithallial sloughing, both of
which affect settlement and were addressed on pp. 45-46). Table 3 summarises available evidence
for each of these mechanisms , classified against the algal functional groups involved; some of the
combinations are not possible (e.g., crustose algae cannot generally shade or abrade). As indicated
in McCook et al. (200lb; their Table 6), coral recruits are more vulnerable to many of these mecha-
nisms than established corals because they are easier to overgrow or shade and generally more
vulnerable to physiological effects. As suggested in that paper, the properties of the algae are likely
to be more relevant than the properties of the coral recruits, which are still small and have limited
development and differentiation (but see next section).
However, many areas have not received any research attention, and chemical effects, abrasion
and sediment accumulation have been overlooked for a range of functional groups . For example,
chemical or allelopathic effects seem likely for species from all functional groups (e.g., Walters
et al. 2003), including crustose coralline algae (Suzuki et al. 1998, Kim et al. 2004, Kitamura et al.
2005), and the scarcity of reports presumably reflects lack of research (perhaps due to the technical
requirements of such research) rather than indicating that such effects do not occur. McCook et al.
(2001a; their Table 6) list the mechanisms they consider likely to be common for each algal func-
tional group, emphasising overgrowth and shading for most groups, abrasion for the larger groups,
47
sloughing for crustose algae and chemical effects for microalgae (such as cyanobacteria). A recent
study by Box & Mumby (2007) specifically tested the mechanisms involved, showing that effects of
the widespread foliose, brown algae Lobophora variegata and Dictyota pulchella can in large part
be attributed to shading and abrasion.
The strength of each mechanism (overgrowth/smothering, shading, abrasion, chemical effects)
will vary with a range of factors including, in particular, the type, height and density of the algal
assemblage. For example, abrasion by leathery and corticated macrophytes (e.g., Turbinaria spp. or
Sargassum spp., both brown algal genera) is likely to be more severe than by foliose (e.g., Padina
spp., brown alga) or filamentous algae (e.g., Chlorodesmis spp. green alga). Indeed Gleason (1996)
observed Turbinaria spp. to completely remove coral recruits from settlement tiles (Turbinaria is a
particularly tough and spiky, upright brown alga). However, a dense canopy of large leathery algae is
likely to shelter coral recruits rather than abrade them. Abrasion from foliose algae (Ulva spp. green
alga, Lobophora variegata, Dictyota menstrualis brown algae) does not appear to be as extreme,
even when combined with shading and potentially chemical effects (e.g., Fairfull & Harriott 1999,
Kuffner et al. 2006). It is not practical to compare the relative strength of the different mechanisms
because their effect will depend on the above factors in each circumstance.
All four mechanisms can be expected to increase in intensity with density, although abrasion
may moderate if the assemblage is dense enough to limit frond movement. Height of the algal
canopy will affect the morphologies that can be overgrown; generally, an algal turf or crust will
not overgrow any but the smallest recruits, whereas a thick algal mat will overgrow most recruits,
except upright, branching corals (Figures 1 and 2). Height will have a major effect on shading, with
larger algae shading larger recruits, and well grazed algal turfs providing little effective shade.
Other factors that will affect the strength of effects include water flow and wave action, which
will increase the impact of abrasion on adjacent corals and recruits (e.g., River & Edmunds 2001,
Eckman et al. 2003).
Size and morphological development of coral recruits

Although coral recruits are initially relatively small and undifferentiated, as they grow, their size
relative to adjacent algal assemblages and their morphology will both change, with consequences
for their interactions with the algae. Coral survival has been shown generally to increase with
growth, especially in the very early post-settlement period (Rylaarsdam 1983, Hughes & Jackson
1985, Babcock & Mundy 1996, Hughes & Tanner 2000, Wilson & Harrison 2005). Babcock &
Mundy (1996) showed that survival and development of older coral recruits (>5 months) was great-
est on upward facing surfaces with more Iight but that survival of younger corals was lower on these
surfaces, possibly as a result of deleterious impacts of sediments. Thus corals are likely to be most
vulnerable to algal impacts immediately after settlement, and vulnerability to different mechanisms
is likely to change. For example, newly settled spat seem likely to be much more vulnerable to
allelopathic impacts than established juvenile corals.
In particular, as the relative size of coral recruits changes relative to different algal types, the
mechanisms of algal effects will change. Coral recruits greater than a few millimetres in height may
emerge from a close-cropped filamentous turf (Figures I and 2), reducing the potential for shading
and abrasion, and reducing the relative effects of flow regimes and chemical environments within
the turf (e.g., Carpenter & Wi II iams 1993, Larkum et al. 2003). In contrast, very small recrui ts may
be protected from abrasion caused by larger seaweeds by small-scale surface features. An example
is provided by two simultaneous studies of a phase shift caused by experimental exclusion of herbi-
vores. Experimental plots became overgrown by algae, predominantly Sargassum spp. (large, leath-
ery brown macrophyte, up to 3 m tall) and Padina spp. (corticated foliose, brown alga), whereas
control plots were dominated by closely cropped filamentous turfs. Hughes et al. (2007) found the
48
larger algae inhibited survival of coral recruits (0.5- to 5.0-cm diameter), naturally recruiting on
to the reef substratum. In contrast, in the same experimental plots, Birrell (2003) observed higher
survival of smaller (diameters <0.5 em) Acropora millepora spat transplanted within days after
settlement and followed from individual polyps for 130 days. It appears the smaller size of the latter
recruits meant they were less frequently in contact with the larger algae, were less frequently subject
to abrasion and were less affected by shade (as suggested by Babcock & Mundy's 1996 observations
discussed in the first paragraph of this section). Indeed, algal canopies may have provided some pro-
tection to these very small recruits during a mild bleaching (Great Barrier Reef, summer of2002, as
suggested for adult corals, Jompa & McCook 1998). Increasing size (perimeter, height and surface
area, polyp number) of coral recruits may also increase intensity of competition for space, the range
of other benthic organisms encountered and the range of different chemical and physical features of
the habitat encountered (Jackson 1979).
As coral recruits grow, they increasingly express interspecific differences in morphological
traits and life-history characteristics so that morphology will become increasingly relevant to the
outcomes of interactions with algae. Although algal properties are particularly important (McCook
et al. 200la), it is also true that different corals interact differently, even with the same alga (e.g.,
Nugues & Bak 2006 using Lobophora variegata). Furthermore, changes in size and morphology
will interact. For example, growth of simple, rounded morphologies (e.g., favids) will be less sig-
nificant to their interactions with algae than growth of upright branching morphologies (e.g., tabular
or staghorn Acropora spp., which stand clear of the substratum and shade competitors; Baird &
Hughes 2000).
Effects of spatial and temporal scale of algal dominance

Moving from the level of individual coral recruits to the level of populations, the spatial scale
and duration of interactions will have major consequences for the effects of algal assemblages on
coral replenishment and reef resilience. The spatial extent of disturbances is critical to the nature
of the consequent recovery and succession (McCook 1994, Connell et al. 1997, 2004, Folke et al.
2004). Localised disturbances such as storm damage, ship groundings or dynamite fishing can
facilitate algal dominance and invasion on limited scales (10 2 -10 4 m 2 ; e.g., Schaffelke et al. 2006,
Raymundo et al. 2007). Recovery from such degradation will involve external supply of coral lar-
vae, encroachment from surrounding populations, and control of algal biomass by herbivores. In
contrast, mass bleaching, large-scale run-off or widespread overfishing may lead to macroalgal
dominance throughout entire regions (Hughes 1994, Jackson et al. 2001, McClanahan et al. 2001,
Berkelmans et al. 2004). In such circumstances, larval supply may be seriously reduced at regional
scales (e.g., Hughes & Tanner 2000) and herbivory may be unable to control such large-scale algal
increases, resulting in much more intense and more general algal inhibition of coral replenishment.
Small-scale (25-m 2) , experimentally induced phase shifts (Hughes et al. 2007) were reversed rela-
tively rapidly (Bellwood et al. 2006) because diverse herbivore populations were present in adjacent
undisturbed habitat, which would not be the case for reef-wide phase shifts. Even where disturbance
is patchy, fragmentation of reef habitats may lead to reduction in overall larval supply, and overall
survival and fitness of recruits, becoming a long-term threat to resilience (Hughes et al. 2005).
Similar considerations are relevant to the duration of algal dominance, with more severe deg-
radation generally involving longer-term reductions in coral replenishment and greater loss of reef
resilience. Decadal-scale algal 'phase shifts' on reefs in the Caribbean have led to widespread
reductions in coral recruit survival, as well as death of mature colonies (Hughes 1994, Hughes &
Tanner 2000, Edmunds 2002, Rogers & Miller 2006, Edmunds & Elahi 2007). Indeed macroalgal
impacts in the Caribbean have played a key role in changing reefs, apparently irreversibly, relative to
their geological past (Pandolfi & Jackson 2006). In contrast, experimental herbivore exclusion over
49
2 yr reduced but did not completely inhibit recruit survival (Hughes et al. 2007). Seasonal blooms
in algal biomass and overgrowth (on the scale of months; e.g., Diaz-Pulido & Garz6n-Ferreira 2002,
Rogers 1997) may have minimal effects on coral replenishment, either because overgrowth is short-
lived or because it is asynchronous with key life-cycle stages (e.g., spawning or settlement).
Overall, short-term and more localised dominance by macroalgae is likely to have less severe
impacts on reef resilience, not simply because effects are less extensive, but also because effects
are less intense within the patch. In such circumstances, if macroalgal dominance is localised and
alleviated within years, long-term reef decline may be avoided. However, long-term and large-scale
dominance by macroalgae will generally result in more sustained and more intense impacts on coral
replenishment and consequent serious loss of reef resilience.
Conclusions and overall implications for reef resilience

Overall , it is clear that benthic macroalgae have a wide range of potentially major impacts on the
different stages or processes of coral replenishment and that these effects are critical to the ecologi-
cal resilience of coral reefs. Macroalgal 'phase shifts', especially those dominated by larger, fleshy
algae or thick mats of algae, can hinder coral replenishment by reducing adult fecundity, larval dis-
persal, settlement and post-settlement growth and survival. In contrast, reef substratum dominated
by crustose coralline algae and fine , closely grazed filamentous algal turfs is relatively well suited
for coral replenishment. Importantly, effects on the processes of fecundity, larval dispersal , settle-
ment and post-settlement growth and survival are cumulative and interdependent because to recruit
successfully, a coral requires each stage to be successful.
Algal effects on coral larval supply, settlement and post-settlement survival are diverse, com-
plex and highly variable, ranging from positive effects, such as induction of settlement on coralline
crusts, to strongly negative effects, such as exclusion of settlement and recruitment by thick algal
mats. In general, negative effects appear more common, especially for larger, fleshy algae or thick
mats typical of phase shifts and degraded reefs. Algal effects on coral replenishment appear to be
often specific to taxa or assemblages and functional groups and may include direct effects, such as
direct overgrowth of coral recruits, and indirect effects, especially changes in the physical , chemical
or microbial nature of habitats due to algal overgrowth.
Although numerous factors and circumstances will influence the outcomes, several key points
are worth emphasising. The different processes or stages of coral replenishment respond very dif-
ferently to different algal influences. Within each stage, variabi Iity in algal effects is strongly related
to key properties of the algal assemblage, especially algal size, growth form or functional group,
density and chemical properties, including nutrient processing, production of allelopathic second-
ary metabolites or effects on microbial communities. With the exception of chemical effects, most
of these traits are well captured by the functional groups, such as crustose, filamentous and various
upright fleshy groups. However, there is still considerable specificity among both algal and coral
taxa, and the life-history traits of corals, especially their size and morphology, will become increas-
ingly important as the corals grow.
It is clear that existing information on algal effects on coral replenishment is insufficient to
adequately understand this critical aspect of reef resilience. All topics need further research, but
algal effects on larval supply, effects of fleshy algae on coral settlement, effects of a lgae mediated
by changes in microbial assemblages and several specific combinations of algal type and competi-
tive mechanisms warrant particular attention. Effects of crustose coralline algae on coral settlement
have been better studied than most aspects. There is a real need for careful attention to the nature
and properties of the algae in these interactions and research should aim to resolve the algae studied
to functional groups as a minimum, in addition to the best feasible taxonomic descriptions, and
description of canopy heights, density and growth form.
so
Overall, g iven algal dominance of degraded reefs, the review demonstrates the importance
of more careful consideration of algal effects on coral replenishment to coral-reef resilience, in
both scientific and management contexts. The nature of the algal assemblage arising from dis-
turbances can vary from filamentous algal turfs to beds of large, canopy-forming algae (Table I;
Diaz-Pulido & McCook 2002), and the differences in algal assemblages will have major impacts on
the future of the reef (e.g., Table 3) and on the effectiveness of management strategies. Clearly, there
is not yet sufficient evidence to draw strong conclusions about these differences but the urgency of
impending degradation warrants some preliminary comments. Where algal communities are domi-
nated by CCA and closely cropped filamentous turfs, coral replenishment is likely to be strongest.
Blooms of seasonal algae may have a relatively low impact unless the bloom period overlaps with
coral spawning and/or settlement periods. Canopies of large, leathery algae, such as Sargassum, are
likely to seriously inhibit coral replenishment and recovery but the most severe impacts seem likely
to arise with thick and dense mats of fleshy algae, which render most of the substratum inaccessible,
especially in conjunction with heavy sediment deposition. The density of any algal assemblages will
strongly influence the extent of such barriers and the extent of chemical and nutrient gradients.
Options for direct management responses to algal dominance are largely limited to proac-
tive steps to prevent establishment of undesirable algal assemblages. Once established, there is
little that can be done to remove algal blooms at any significant scale. Proactive strategies should
aim to maximise the relative success of filamentous turfs and CCA , minimise the growth and
accumulation of larger, fleshy algae and minimise the extent to which algae interact with anthro-
pogenic sediments and nutrients. Perhaps most important is the protection of herbivore guilds, espe-
cially herbivorous fishes , which maintain low algal biomass, in turn enhancing coral recruitment
(McCook 1999, Hughes et al. 2007, Mumby et al. 2007). Measures to reduce pollution , especially
increased sediments, may reduce competitive dominance by larger, fleshy algae and will minimise
sediment trapping and formation of detrimental chemical or microbial microhabitats within the
algal assemblage.
More generally, measures that enhance the overall resilience of the reef ecosystem, such as
maintaining coral health , ecosystem biodiversity and trophic structure and integrity (Hughes et al.
2003, McCook et al. 2007), will serve to maintain the capacity of the system to resist and recover
from disturbances and indirectly slow or prevent increases in algal dominance. Particularly impor-
tant is to reduce the frequency and severity of disturbances, such as coral bleaching and cyclones.
Both disturbances and loss of resilience depend critically on climate change, and the most critical
overall need is for urgent and dramatic actions to reduce the rate and extent of climate change, by
reducing emissions of greenhouse gases.
Globally, increasing reef degradation , espec ially due to the impending impacts of changing
climates (Hoegh-Guldberg et al. 2007), means that the extent and duration of algal dominance
will increase and the effects of this dominance on coral replenishment are likely to cause a severe
bottleneck for reef recovery. Although much attention has focused on the global -scale effects of
climate change on corals as the primary reef builders, there has been less detailed consideration of
climate effects on key processes and interactions, such as the interactions between algae and coral
replenishment. Increasingly frequent and severe mass bleaching of corals will result in increasingly
extensive algal colonisation of dead corals. But recent work (Diaz-Pulido et al. 2007b) has also
shown that climate change, particularly ocean acidification, will have major effects on reef algae,
probably enhancing dominance by turfing and fleshy algae and decreasing the abundance of CCA.
Such changes will alter the context for coral replenishment, interacting synergistically with stresses
on corals, and leading to increasing dominance by thicker algal mats and larger fleshy algae, in turn
causing increased inhibition of coral replenishment. As climate change and other human impacts on
coral reefs increase, understanding and addressing the changing dynamics of coral replenishment
on algal-dominated reefs become increasingly important.
51
Acknowledgements
We thank T.P. Hughes and R.S. Steneck for invaluable discu ssion and L. Ha rrington, C. Damiano
and especially 1. E. Smith for comments on the manuscript. We gratefully acknowledge the support
of F. Birrell, L. Birrell, M. Birrell, 1. Barendrecht, R. Bonaldo, Y. Tibiri<ra and C. Rodenas-Lopez to
C. B. during the preparation of this review, and L.McC., C. B. and G.D.- P. acknowledge support from
the Pew Fellowship Program in Marine Conservation.
Appendix
List of coral taxa and algae used in published studies of algal impacts on coral settlement or post-
settlement survival. Approximately 800 species of corals have been taxonomically identified world-
wide (Veron 2001).
Re productive
Coral mode Macroal gae
Acropora digitifera s Hydro /ith on reinboldii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Acropora florida s Hydrolithon reinboldii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Acropora formosa s Hydrolithon reinboldii 1, Lobophora va riegata 1, Peyssonnelia sp. 1
Acropora gemmifera s Hydrolithon reinboldii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Acropora hyacinthus s Hydrolithon reinboldii 1, Lobophora variegata 1, Peyssonne lia sp. 1
Acropora microphthalma s Bacteria/microa lgae2
Acropora millepora s Sargassum spp.\ Pad ina spp.\ Lobophora sp.\ mixed CCoA\ Chlorodesmis
fastigiata '. Lobophora va riegata' . filamentous turf'.4 Hydrolithon
rein boldii 5, Lithoporella melobesioides 5, Neogon iolithonfosliei 5,
Porolithon onkodes 5, Titanoderma prototypum 5 Amphiroa anceps 6,
A. folia cea 6, Hydrolith on onkodes6 , Lithophyllum insispidum 6 ,
L. kotschyanum 6 , Mesophyl!um sp. 6, Neogoniolithon brassica-florida 6 ,
Peyssonnelia sp 6 , Hydrolithon onkodes' & bacteri a'
Acropora nasuta s Hydrolithon reinbo!dii 1, Lobophora variega ta 1, Peyssonnelia sp. 1
Acropora palifera B Hydrolithon sp-", Lobophora sp.', Peyssonnelia sp. ' . Porolithon sp .',
filamento us turf(< IS mm he ight in combination with 10 mm sed ime nts)'
Acropora sp. I s Hydrolithon reinboldii Loboplwra variegata Peysson nelia sp. 1
1
,
1
,
Acropora sp. 4 s Hydrolithon sp. 1, Lobophora sp. 1, Peyssonnelia sp. 1, Porolithon sp. 1
Acropora sp. 6 s Loboplwra variegata 1
Acropora sp. 7 s Peyssonnelia sp. 1

Acropora spp. 8, 9, I0, I I s Hydrolithon reinboldii 1
Acropora surculosa s Lyngbva majuscula 10

Acropora tenuis s Hydrolitlw n reinboldii l.-', Lithoporella melobesioides'. Neogoniolitlwn
fosli ei-'. Porolithon onkodes' . Titan oderma prototypum\ Lohophora
variegata 1, Peyssonnelia sp. 1
Acropora willisae s Lithophyllum sp 7
Agaricia agaricites B CCoA 11 • endolithic algae", filame ntous turfs"
Agaricia danai B Microa lgae/bacteria 12 , mixed CCoA both o n dead Millepora complanata
Agaricia lwmilis B CCoA sp. 112 , sp. 2 12, sp. 3 12 , sp.4 12 , sp. 5 12 , Hi/denhrandia sp. 12, microalgae
o r bacteria" , mixed CCoA' 2, Porolithon sp. 12
Agaricia humilis B Hydrolithon hoergensii 1• 13 · 14 · 17 ·", H. reinholdii 1, Neogon iolithon
megacarpum "· ". Porolithon pachydermum 13 , Peyssonnelia sp. 1, Halimeda
opuntia 15 , filamentous turfs (thick & ung razed; thin & grazed; primarily
Cladophora spp. & C/adophoropsis spp.) 16; mixed CCoA (Hydrolithon.
Mesophyl/wn, Pneophyllum, Porolithon & Titanoderma) 16, unidentified
CCoA 11, endo lithi c algae 11 , fil amento us turfs 11
52
Reproductive
Coral mode Macroalgae
Agaricia tenuifolia B Hydrolithon boergensii 1', mi croalgae/bacteria 12 , mixed CCoA' 2
Agaricia spp. B Lobophora variegata 14, Dictyota pulchella 24
Cyphastrea sp. s Hydrolirhon reinboldii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Favia favus s Hydrolithon reinboldii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Faviafragum B Halimeda opumia 1\ filamentous turfs (thick & ungrazed; thin & grazed;
primarily Cladophora spp. & C/adophoropsis spp.) 16, mixed CCoA
(Hydrolithon, Mesophyl/wn , Pneophyllwn, Porolithon & Titanoderma) 16
Gonioastrea retiform is s Hydrolith on reinbo/dii 1, Lobophora variegata 1, Peyssonnelia sp. 1
Montipora capitara s Ulvafasciara''· Acanthophora spicifera 25 , Pterocladiel/a caeru/escens 2',
Sargasswn polyphyllum 2'
Oculina arbuscula Sargassum spp. 19, Dictyora spp. 19, Dictyopteris spp. 19, Zonaria spp. 19,
Lobophora spp. 19
Poci/lopora damicornis B Lyngbya majuscula 10, L. confervoides 20, Halimeda opuntia 20, Lourencia
papillosa 20 , Peysonnelia rubra 20 , Sargassum po/ycystum 20,
Porites astreoides B Chondrophycus poiteaui!Lourencia poiteauP 1, Dictyota confervoides 21 ,
D. menstrualis 21 , D. pinnatifida 21 , D. pulchella 21 , Lobophora variegata 21 ,
L. po/ychroa 2 1, induced algal phase shift by herbivore exclusion 22
Porites porites B Sargassum hystrixn
Stylophora pistillata B Hydrolithon sp. 8, Lobophora sp. 8, Peyssonnelia sp. 8, Porolithon sp"
Tubastrea au rea B Hydrolithon boergensii"
Note: Coral reproductive mode is li sted as brooders (B) and spawners($ ; mode unknown for Oculina arbuscula). Superscript
numbers indicate references as follows: 'Morse et al. 1996, ' Webster et al. 2004, ' Birrell 2003, 4 Birrell et al. 2005,
' Harrin gton et al. 2004, 6 Heyward & Negri 1999, 7 Negri et al. 200 I, ' Baird & Morse 2004, 9 Potts 1977, 1°Kuffner &
Paul 2004, 11 Van Moorsel 1985, 12 Morse et al. 1988, ''Morse & Morse 1991, 14 Morse et al. 1994, 15 Nugues & Szmant
2006, 16 Petersen et al. 2005, 17 Raimondi & Morse 2000, "Steneck & Morse (cited in Morse & Morse 1991 ), 19M iller
& Hay 1996, 20 Maypa & Raymundo 2004, 21 Kut'fner et al. 2006, 22 Lewis 1986, 23 River & Edmunds 200 I, 24 Box &
Mumby 2007, " Vermeij et al. in press.
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Oceanography and Marin e Biology: An Annual Review, 2008, 46, 65-104
© R.N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon , Editors
Taylor & Francis
AUTECOLOGY OF CRANGON CRANGON (L.) WITH

AN EMPHASIS ON LATITUDINAL TRENDS
JOANA CAMPOS 1•2 & HENK W. VANDER VEER 2
'Centro lnterdisciplinar de lnvestigar;ii.o Marinha e Ambiental,
Rua dos Bragas, 289, 4050-123 Porto, Portugal
E-mail: jcampos@fc.up.pt
2
Royal Netherlands Institute for Sea Research, PO Box 59,
1790 AB Den Burg Texel, The Netherlands
E-mail: veer@nioz.nl
Abstract This review aims to update and extend the synopsis by Tiews (1970) on the biology
and fisheries of Crangon crangon (L.). Its wide distributional range along the European coast from
the White Sea to Morocco within the Atlantic and throughout the Mediterranean and Black Seas
reflects the capability of C. crangon to cope with a wide range of temperature and salinity condi-
tions and is further explained by its migratory capacity. Present knowledge suggests that the limit-
ing factor at the northern cold water edge of its distribution is formed by egg and larval development
and at the southern warm water edge by maintenance costs. No information is available about the
genetic population structure, but patterns in isoenzymes and in morphometric characters indicate
the existence of various subpopulations. Over its distributional range, especially along the north
Atlantic coast, clear trends in life-history parameters are observed, most likely reflecting tempera-
ture conditions. Due to its generally high abundance, the common shrimp forms a key component
in the functioning of coastal shallow ecosystems; however, it is unclear whether the population
dynamics of the species is subject to top-down or bottom-up control. On the one hand, C. crangon
is an opportunistic feeder with a wide prey spectrum though it remains to be solved whether growth
conditions are optimal and only determined by prevailing water temperatures, or whether food
limitation is a reg ulating mechanism. On the other hand , top-down control by predation cannot be
excluded since C. crangon is also an important food item for a variety of predators, especially fish
spec ies. There are strong indication s that predation by C. crangon might regulate some of their prey
species. Topics for further research include (I) the analysis of the genetic population structure by
means of molecular tools; (2) the study of growth and reproduction in relation to latitude; (3) the
application of dynamic energy budgets for the analysis in terms of energy of the various trade-offs,
including growth versus reproduction; and (4) the analysis of the mechanisms determining recruit-
ment, especially whether top-down or bottom-up control is occurring.
Introduction
The brown shrimp Crangon crangon (L.) is a marine coastal decapod species with a wide distribu-
tion range along the European coast from the White Sea in the north of Russia to the Mediterranean
and Black Seas (Muus 1967, Tiews 1970, Gelin et al. 2000). It is present in Malta (Micaleff &
Evans 1968) and Morocco (J. Campos personal observation), within the latitude parallels of 34°N
and 67°N (Mediterranean, temperate and cold climatic zones). Within the Mediterranean, the dis-
tributi on of C. crangon is not clear. Only in the Adriatic Sea, it is subjected to a small-scale fishery
65
JOANA CAMPOS & HENK W. VANDER VEER
(D. Tagliapietra persona l communication). Expa nsion and contracti on of the population range
still seems to continue since recently the brown shrimp has been reobserved in Icelandic waters
(B. Gunn arsson personal com munication) after a first inc idental observation in 1895 (Doflein 1900),
though not li sted among the Icel a ndic Decapoda spec ies in 1939 (Holthui s 1980).
Crangon crangon inhabits mainly soft botto m (sandy, sandy-mud a nd muddy substrata) estua-
rine and marine shallow areas, including coastal lagoons, with preference for grain sizes between
125 and 7LO flm (Pinn & Ansell 1993), a lthough it may occur at depths of 20-90 m (A l-Ad hub &
Naylor 1975), espec ially during winter ( Hin z et al. 2004), and anecdotic in for mat ion suggests even
to 120m depth as in the Brev ik Fjord, Sweden (Wollebaek 1908).
Crangon crangon is a very abundant species in European estuaries and hence an important
component of those ecosystems. Due to its high abundance, it forms an extensive food source for a
large range of predators, including fish like gadoids and pleuronectiforms, crustaceans, and wading
birds ( Pihl 1985, Henderso n et al. 1992, Del Norte-Campos & Temming 1994, Walter & Becker
1997). In turn it preys heav ily upon several benthic spec ies such as bivalve spat and juvenile plaice
(Pihl & Rosenberg 1984, Vander Veer et a l. 1991 , 1998, Ansell & Gibson 1993, Oh et a l. 2001,
Amara & Paul 2003).
In the 1970s, Tiews (1970) compiled all ex isting knowledge with respect to brown shrimp biol-
ogy and fi sheries at that time. Since then there have been numerous publications about the species.
The main aim of this review is an update of the compilation by Tiews (1970) with a broadened and
partly changed scope. In thi s respect, the intention is to give more emphasis on the ecology of the
species, especially on its role and function in the ecosystem in relation to its di stribu tiona l range.
The bac kbone of this review is the analysis of life-history strategy of C. crangon over its latit udina l
di stribution range. The various life-hi story traits are described from an ecophysiolog ical point of
v iew whereby energy will be used as a token for fitness with the aim to detect gaps in the knowledge
of the species. Thi s review is ma inly based on publi shed in for mation. In add itio n, valu able informa-
tion from grey literature references has been incorporated.
Taxonomic status and genetic population structure

Taxonomic status
Crangon crangon (Linnaeus, 1758) belongs with other shrimps, prawns , lobsters, crayfish and crabs
to the crustacean order Decapoda, which derives its nam e fro m five pairs of ambul ato ry thoraco-
pods called pereiopods, posterior to three pairs ofthoracopods termed maxill ipeds since they func-
tion as mouth parts. However, above a nd under order level there is st ill some hierarchical debate.
The Crustacea have been variously considered to be a phylum , subphylum , supercl ass or class of
Arthropoda (phylum or superphylum) (see Martin & Dav is 2001 , Brusca & Brusca 2003) and most
now treat Crustacea as a subphylum of Arthropoda, considering Arthropoda as a monophyletic
group, which is not full y establi shed . Within C rustacea the suborder or supersection Natantia, gro up-
ing together a ll known shrimp spec ies, persists for some authors due to its simplic ity. Nowadays,
C. crangon is placed in the class Malacostraca, subclass Eum a lacostraca a nd superorder Eucarida
since Natantia is no longer considered to be a valid taxon (Martin & Davis 200 1). As Malacostraca
C. crangon conforms to the commonest pattern of eight thoracic segments and six abdom inal seg-
ments, each bearing a pair of limbs; as Eumalacostraca it possesses a carapace enclosing the thorax,
stalked , movable eyes, bira mous antennules, sca le-like a ntenna! exopods, telson and uropods form-
ing a tailfan and biramous pleopods 1-5; as Eucarida C. crangon has a well-developed carapace
that is fused to all the tho racic somites, a telso n without a cauda l furca, and typically metamorphic
larva l development. Crangon crangon belongs to the infraorder Caridea, which occ urs within the
suborder Pleocyemata - since their fertilised eggs are incubated by the female and remain stuck to
the pleopods (sw imming legs) until they are ready to hatch- a nd consists of species for which the
66
AUTECOLOGY OF C. CRANGON (L.) WITH AN EMPHASIS ON LATITUDINAL TRENDS
third pereiopods do not terminate in chelae and the lateral edges of the second abdominal segment
overlap those of the first and third segment. Within the infraorder Caridea C. crangon belongs to
the superfamily Crangonoidea, due to its short rostrum, and to the family Crangonidae (Haworth,
1825), which is characterized by the fact that the first pereiopods are subchelate.
Crangon crangon is the type species of the genus Crangon. Several synonyms occur in earlier
literature, the commonest being C. vulgaris. In the past, Tiews (1970) listed the position of the spe-
cies with regard to the closely related north-east American C. septemspinosa Say, and north-west
American C. alaskensis Lookington, as not certain: they might be subspecies of a single species
or even full synonyms of each other, but Tiews did not provide detailed taxonomic information.
Also the south European form of the species inhabiting the Mediterranean and the Black Sea has in
the past sometimes been considered to be a subspecies, though generally no subspecies are distin-
guished. In European waters C. crangon and C. allmanni are closely related (Smaldon et al. 1993),
whereby in North American waters C. dalli Rathbun , 1902 strongly resembles C. allmanni (own
morphological observations). For more detailed information see Zariquiey-Alvarez (1968), Tiews
(1970), Zarenkov (1970), Butler (1980), Christoffersen (1988), Smaldon et al. (1993) and Hayashi &
Kim (1999).
Though still under debate the present status of the genus Crangon includes 18 species and
subspecies (Christoffersen 1988). Due to misidentifications in the past, present distribution patterns
of the various species are difficult to determine. While in the north-east Atlantic only two species
seem to occur, C. crangon (Linnaeus, 1758) and C. allmanni Kinahan, 1860; and in the north-west
Atlantic only one species has been found, C. septemspinosa Say, 1818, in the south-west Atlantic
no Crangon species is registered. On the other hand, in the north-east Pacific more (sub)species
are found: C. alaskensis Lockington, 1877; C. alba Holmes, 1900; C.franciscorumfranciscorum
Stimpson, 1856; C. fran ciscorum angustimana Rathbun , 1902; C. handi Kuris & Carlton, 1977;
C. holmesi Rathbun , 1902; C. nigricauda Stimpson, 1856; and C. nigromaculata Lockington, 1877.
Finally, a recent revision of the north-east Asian species has resulted in the following seven species
being listed: C. affinis DeHaan, 1849; C. amurensis Brashnikov, 1907; C. cassiope De Man, 1906;
C. dalli Rathbun, 1902; C. hakodatei Rathbun , 1902; C. propinquus Stimpson, 1860; and C. uritai
Hayashi & LN. Kim, 1999 this last one being the most closely related to C. crangon (Hayashi &
Kim 1999).
With respect to C. crangon, there is still serious doubt whether C. septemspinosa from the north-
east Atlantic is the same species or a different one and the same applies for C. affinis from north-east
Asia. A detailed genetic analysis of the various Crangon species is required to resolve the present
uncertainties.
Population structure
For Crangon crangon, a study analysing various isoenzymes on a large scale (1000 km) (Bulnheim
& Schwenzer 1993) identified four regional groups: the North Sea and Baltic Sea; the north Atlantic
Ocean ; Portugal and the Adriatic Sea. On a smaller scale (100 km) two analyses using the variabil-
ity in morphometric characters even suggested the existence of a much more detailed population
structure: Maucher (1961) suggested differences between North Sea and the Baltic Sea populations
and Henderson et al. (1990) distinguished six subpopulations in British waters alone. However, in
both studies the results on spatial variability were based on a single sampling programme only. A
recent analysis of the stock structure in U.K. populations by means of variability in morphology
and genetics could not find support for a subpopulation structure on a small scale (Beaumont &
Croucher 2006).
So far C. crangon genetic population structure has not been studied over its distributional range
by molecular tools of DNA sequencing.
67
Autecology of Crangon crangon

Morphology
Characteristics of the species
This description of the distinctive morphology of Crangon crangon is based on Holthuis (1955),
Zariquiey-Alvarez (1968) and Smaldon et al. (1993). The rostrum is unarmed with a triangular
shape and a rounded apex , measuring half the length of the eye or slightly more. The carapace
presents an anteriorly directed spine in the anterior quarter of the median line and three pairs of
lateral spines: antenna!, below the orbit; pterygostomian, on the antero-ventral corner; and hepatic
spines, on the lateral border of the carapace. The stlylocerite, which is a lateral expansion of the
first segment of the antenullar peduncule, is acutely pointed and half the length of this peduncule.
In the scaphocerite, which is the laterally expanded and flattened exopod of the antennae, the apical
spine exceeds the lamellar portion. The third maxilliped is equal in length to the scaphocerite and
possesses an exopod and an arthrobranch (arthrobranchs are small gills also associated with the
pereiopods). The mandible has only a molar process and no incisor process or mandibular palp, and
the teeth are sharply pointed. Pereiopod l is subchelate and stout and pereiopod 2 extends to three
quarters the length of propodus (segment 6) of pereiopod 1, while the dactyl (segment 7) of pereio-
pod 2 is about a quarter of the length of the propodus of pereiopod l. The sixth abdominal segment,
pleonite 6, is smooth dorsally without a groove or carinae, this feature enabling C. crangon to be
easily distinguished from C. allmanni. The endopods of pleopods 2-5 are two-segmented and each
lacks an appendix interna. Finally the telson has two pairs of small lateral spines.
Differences in form and dimension of various quantitative morphological traits can be used to
study patterns of geographic variation and differences among populations (Henderson et al. 1990),
whereby especially the following characters are used after standardizing for total length: carapace
length, telson length, inner uropod length, inner uropod width, maximum length of subchela , maxi-
mum width of subchela, length of segment 4 (merus) of first pereiopod, and maximum length of
segments 4 (merus) and 5 (carpus) of pereiopod 5 (Figure 1).
Flagellum
Uropod
Figure l Morphology of Crangon crangon.
68
Figure 2 The endopod of the first (I) and second (3) pairs of pleopods and the olfactory branch of the first
antenn a (2) in Crangon crangon in males (right panel) and females (left panel). (After Meyer-Waarden &
Tiews 1957.)
Differences between sexes

Morphologically, differences between sexes are not immediately obvious, especially under 20 mm
length (Meredith 1952). Three main morphological characteristics are described to distinguish
sexes: the endopod of the first and second pairs of pleopods and the outer branch (olfactory) of the
first antenna (antennule) (Figure 2).
The endopod of the first pair of pleopods is shorter in males than in females (Gel in et al. 2000)
of all ages (Schockaert 1968). In females it is always clearly visible and each looks look like a narrow
spoon (Meredith 1952), while in males it is spine-like and hardly visible (Tiews 1970) (Figure 2). It
is a useful character to distinguish sexes of smaller shrimps (Lloyd & Yonge 1947), although dif-
ficult to use in animals under 22 mm (Dalley 1980), or even under 25-30 mm (Gel in et al. 2000). In
females above 27 mm this endopod is visible by eye and may attain 6 mm length (Meredith 1952).
In males, the endopod of the second pair of pleopods bears an appendix masculina used in
copulation and sperm transfer (Figure 2). It is spined on one side (Tiews 1970) and clearly visible
in shrimps from 15-16 mm total length (TL) onwards (Muus 1967), although some authors found it
only apparent over 20-30 mm length (Lloyd & Yonge 1947, Meredith 1952, Tiews 1970). Since the
appendix masculina is absent in females , it can be useful to separate sexes when the first endopod
is of doubtful size (Meredith 1952).
Finally, the outer or olfactory branch of the first antenna (antennule) is longer and has more
segments and olfactory hairs in males than in females (Lloyd & Yonge 1947, Tiews 1954, 1970).
The second antenna also presents some differences between sexes, which have been described by
Ehrenbaum (1890), Kemp (1908), Havinga (1930), Meredith (1952) and Tiews (1954, 1970). Namely,
it is longer than body length in males while in females it is shorter. Nevertheless it is often not prac-
tical to separate sexes based on this feature because in preserved material the antennae often break
(Tiews 1970).
69
Table 1 Linear relationships between total length (mm) and, respectively, carapace length
(CAR), telson length (TEL), maximum length of subchela (SUBLE), maximum width of
subchela (SUBWI), length of segment 4 of first pereiopod (PERI), inner uropod length (INNLE),
inner uropod width (INNWI), and maximum length of segments 4 (MAX4) and 5 (MAX5) of
pereiopod 5 for Crangon crangon in the western Dutch Wadden Sea in September 2003
CAR TEL SUBLE SUBWI PERl INNLE INN WI MAX4 MAX5
Number of cases 30 30 74 74 74 30 73 73 73
Squared multiple R 0.99 0.99 0.99 0.98 0.99 0.99 0.98 0.99 0.99
Coefficient 0.206 0.148 0.101 0.032 0.092 0.135 0.033 0.080 0.057
95% Cllower 0.201 0.144 0.099 0.032 0.090 0.133 0.032 0.078 0.056
95% Cl upper 0.210 0.153 0.103 0.033 0.094 0.137 0.034 0.081 0.058
Note: Cl, confidence interval.
Source: Data after J. Campos (unpublished observations).
Differences in relation to growth

Growth of C. crangon seems to be isometric since various morphometric characters show linear
relationships with total shrimp size (Table 1). With size and hence during growth, the number of
segments of the olfactory branch of the first antenna increase after each moult by a definitive number
that varies regularly between one and three according to the age and size of the shrimp and depends
on prevailing temperature (Tiews 1954). However, the relationship between shrimp size and number
of segments varies between males and females (Figure 3). The increase in segment numbers is faster
in males than in females and with increasing shrimp size the differences between males and females
become large enough to distinguish between sexes, though the morphologies of endopods of the first
and second pleopods are much more rel iable characters for use in sex determination.
! - J u veniles -o-- Males ｾｆ･ｭ｡ｬｳ＠
50
:s 40
c:"'
<!)
E 30
bD
ｾ＠
'"-<
0
....<!) 20
.D
E
::J
z 10
0
0 20 40 60 80 100
Total length (mm)
Figure 3 Number of segments of the olfactory branch of the first antenna (n) in males and females of
Crangon crangon in relati on to shrimp size (mm). (Data after Tiews 1954.)
70
Life cycle
In general, the life cycle of C. crangon is similar to that of many other species. Reproduction of
brown shrimp occurs in deeper (10-20 m) and more saline waters off shore, usually in sandy or
muddy areas (Tiews 1954, Henderson & Holmes 1987). During the egg stage, the eggs are not
free floating in the plankton but are carried by females. After hatching of the eggs, free-floating
planktonic larval stages are followed by settlement and demersal juvenile and adult stages. Due
to the rigid exoskeleton, growth of C. crangon is irregular and takes place by various moultings,
whereby the exoskeleton is released, an increase in body volume occurs and a new soft skeleton is
formed that hardens in a few days (Smaldon 1979). After the first planktonic stages, shrimp larvae
migrate to shallow nursery areas, such as estuaries, where they mature (Tiews 1970, Heerebout
1974, Boddeke et al. 1976, Beukema 1992). With increasing size, adults move towards deeper water,
where they reproduce.
The onset of sexual maturity appears to be at a size between 35 and 40 mm total length (Meredith
1952). There is some debate about whether C. crangon is a dioecious species with male and female
reproductive organs in different individuals or a protandrous hermaphrodite, beginning its life as
a male and later changing into a female. For a long time only anecdotal information was present
(Boddeke et al. 1988). Recently, Schatte and Saborowski (2006) observed in an 8-month labora-
tory experiment that I out of 70 males performed morphological sex reversal. They concluded that
C. crangon may be capable of changing sex; however, the low frequency of occurrence suggests that
the species is more a facultative than an obligate protandric hermaphrodite and hence consequences
at population level are most likely not relevant.
Brown shrimp is an euryhaline species (Broekema 1942, Lloyd & Yonge 1947, Muus 1967,
Tiews 1970, Criales & Anger 1986) occurring at salinities between 0 and 35 (Mees 1994, Mouny
et al. 2000) (salinity expressed in accordance with Practical Salinity Scale 1978) and commonly is
found in waters of relatively low salinity (1-5) (Havinga 1930, Boddeke 1976). Crangon crangon
can survive at temperatures between 6°C and 30°C (Lloyd & Yonge 1947, Abbott & Perkins 1977,
Jeffery & Revill 2002). At lower temperatures, as during severe winters, brown shrimp prefer high
salinity and hence show a tendency to migrate to offshore waters (Broekema 1942).
Ecophysiological characteristics
Combining information from various locations in a description of the ecophysiological charac-
teristics of brown shrimp without knowing the possible existence of genetic subpopulations may
result in a misinterpretation of latitudinal variation. Therefore, and since most available information
refers to Atlantic locations, in this review the description of Mediterranean shrimp ecophysiology
is mentioned separately, whenever this information exists. Furthermore, the combination of knowl-
edge from various shrimp stocks may introduce some bias because of adaptations of local stocks to
environmental conditions, either occurring as phenotypic plasticity or as genetic selection.
Egg stage
Fertilisation in brown shrimp is external (Tiews 1970). Brown shrimp has no copulatory organs, the
spermatophores being applied to the ventral side of the female usually close to the genital opening
(Lloyd & Yonge 1947). Sperm may then be stored in the oviducts (Boddeke 1982). Copulation and
spawning occur within 48 h of mating (Abbott & Perkins 1977), and egg extrusion takes between
4 and 8 minutes. Crangon crangon has post-spawning parental care by carrying the eggs, which
are attached to the pleopods with secretions from a cement gland after copulation, taking a further
30 minutes (Lloyd & Yonge 1947). The newly attached egg is spherical but gradually it enlarges
almost exclusively in one dimension and becomes elliptical (Lloyd & Yonge 1947).
71
Table 2 Egg development stages in the common shrimp Crangon crangon

Broekhuysen Meredith Ohet al.
Stage Colour Description ( 1936) (1952) ( 1999)
I Greeni sh, transparent Early spawned, small eggs, early blastoderm I, II, III , IV A, A+ A
2 White Bigger eggs, large blastoderm, gastrulation V, VI B- B
3 White to light brown Eyes of larvae become visible VII B+ c
4 Brownish Large eyes visible, outline of carapace and VIII C-,C,C+ D
abdomen
5 Brown Whole prelarvae visible, abdomen se parated IX D E
from head, first e mpty egg capsules
6 Larvae hatched, leav ing only degenerated X, XI E F
eggs and empty egg capsules
Source: Adapted after Oh et el. ( 1999), based on Havinga ( 1930), Broekhuysen ( 1936), Mered ith ( 1952), Tiews ( 1970) and
own observations.
In early stages of development the size distribution of the eggs probably is not homogeneous,
but as the ovary approaches spawni ng most ova attain a certain maximum size. Egg size depends on
female size, whereby larger females tend to produce larger eggs (Marques & Costa 1983). The maxi-
mum egg diameter reported is in the range of 0.58 mm (Meredith 1952, Pandian 1967) to 0.61 mm,
shortly before spaw ning (Lloyd & Yonge 1947). Eggs produced in winter are usually larger than
summer ones (Havi nga 1930), respectively with minimum diameter of 0.43 and 0.37 mm on the
Dutch coast (Boddeke 1982) and maximum diameter of 0.86 and 0.76 mm at Port Erin Bay, Isle of
Man (Oh & Hartnoll 2004).
During incubation different developmental stages can be distinguished (Table 2). The incu-
bation period of the eggs is dependent on prevailing water temperature (Meredith 1952, Tiews
1954, Boddeke & Becker 1979), but on ly those eggs that develop between 6°C and 21°C are viable
(Wear 1974). Different relationships for the incubation of the eggs (Din days) until hatch have been
described by various authors (for summary see Temming & Damm (2002)):
D = 1031.341'- 1354 (Belgian waters; Redant 1978) (I)
D = 20437(T + 3.6)-23 (U.K. waters; Wear 1974) (2)
D = 1230.271'- 1 43 (Dutch coastal waters, summer eggs; Boddeke 1982) (3)
D = 1548.821'- 149 (Dutch coastal waters, winter eggs; Boddeke 1982) (4)
However, the differences between these relationships are small and in general egg development
might last from 2-3 wk at 20°C to up to more than 3 months at 6°C (Figure 4). With increasing
temperature, egg development can occur at lower salinity, though at salinities below 15 eggs fail to
develop and are lost by the females (Broekema 1942).
Larval stage
The larvae have been described by Ehrenbaum (1890), Havinga (1930), Lebour (1947), Dalley
(1980), Gurney (1982), Du Cane (1839), Williamson (1960) and Criales & Anger (1986), including
five (Ehrenbaum 1890, Williamson 1960, Dalley 1980, Criales & Anger 1986) to six pelagic stages
and an extra post-larval stage (G urney 1982). These first planktonic stages occur in higher-sa linity
locations (Marques 1982). The length at hatching is 2 mm , increasing to 4.6-4.7 mm at the end of
72
120
-B-- Redant (1978)
\I --a-- Wear (1974)
ｾ＠
100 ｾＭ Summer eggs, Boddeke (1982)
ｾ＠ --)(--Winter eggs, Boddeke (1982)
<!)
80
.§ - · +- -Meixner (1967)
c +- \+" '
<!) 60
E
0.
0
-;:; 40
>
<l)
a
20
0
0 5 10 15 20 25
Water temperature (•C)
Figure 4 Egg development time (d, days) of Crangon crangon in relation to water temperature ( 0 C).
the last larval stage, when the animals settle (Lloyd & Yonge 1947). Larvae hatching from summer
eggs are smaller than those from winter eggs: respectively 2.14 and 2.44 mm (Boddeke 1982).
Larval development is only successful at a narrow temperature range of 9°C to l8°C and at a
narrow salinity range mainly in the polyhaline zone (salinity around 32) with mortality at salinities
below 16 and slower development at a salinity of 25 (Criales & Anger 1986). Within this salinity
range the length of the pelagic larval period (D in days) depends on temperature (Lloyd & Yonge
1947), and various relationships have been published:
D = 941.781'" 1347 (Wadden Sea area; Temming & Damm 2002) (5)
D = 952.091'" 1258 (Dutch coastal waters, summer larvae; Boddeke 1982) (6)
D = 1148.421'" 1405 (Dutch coastal waters, winter larvae; Boddeke 1982) (7)
In addition, measurements in the laboratory at l2°C, l5°C and l8°C are available from Criales &
Anger (1986). Overall, the length of the larval stage corresponds with that of the egg stage at the
sa me temperature and, within the relatively small temperature range (9-I8°C), larval development
varies from about 3 wk at l8°C to about 7 wk at 9°C (Figure 5).
The number of larval moults at metamorphosis is mainly a reflection of development time as is
indicated by the relationship between the number of moults (M), larval development time (D; days)
and water temperature (T; 0 C), after Criales and Anger ( 1986):
M = 0.00584*D*T 1347 (8)
This means that the number of moults increases from on average 5.9 at I2°C to 7 at l8 °C (Criales &
Anger 1986).
Settlement
Settlement occurs in the first or second post-larval stage at 4-6 mm body length. Kuipers & Dapper
(1984) reported an average length at settlement of 4.7 mm total length, occurring after 2-5 months
of development. The processes inducing settlement in C. crango n are unknown. In flatfish spe-
cies, favourable food conditions are considered to be the clue triggering settlement on the sediment
73
120
---e-- T emming & Damm, 2002
100 --a-- Summer eggs; Boddeke, 1982

ｾ＠ --o- Winter eggs; Boddeke, 1982
.§"'
80 - -•-- Criales & Anger, 1986
c 60
"'E
0.
0
v> 40
a"'
20
0
0 5 10 15 20 25
Water temperature (•C)
Figure 5 Larval development time (d, days) of Crangon crangon in relation to water temperature (0 C) sum-
marized by Temming & Damm (2002).
surface (Creutzberg et al. 1978). It is unclear whether settlement in larval shrimps is induced by a
similar mechanism.
It is also unclear whether the larvae are only being transported passively, by being swirled up
in the water column by increasing tidal or wind-induced currents and sinking down at low current
velocities (Rijnsdorp et al. 1985, Bergman et al. 1989) or whether, in addition, larvae are able to
affect this transport selectively by swimming up from the seabed during flood tides and remaining
on the seabed during ebb tides, so-called se lective tidal transport as observed in flatfish species
(Rijnsdorp et al. 1985, Jager 1999).
Nevertheless, settlement is only possible when larvae reach the sediment surface. Once there
larvae have to maintain position without being displaced . In this respect active partial burying by
the settling larvae, as in some fish larvae, might be effective because it might reduce drag forces
induced by currents close to the seabed (Arnold & Weihs 1978). Such a mechanism in com bina-
tion with the size of the larvae would imply that sediment conditions might be important. In gen-
eral, shallow and silty estuarine areas are mentioned as suitable for settlement (Berghahn 1983,
Kuipers & Dapper 1984, Boddeke et al. 1986, Henderson & Holmes 1987).
Ju venile stage
Field in formation indicates that the habitat requirements of juvenile shrimp a re rather broad, i nclud-
ing very fine to coarse sand (Kuipers & Dapper 1981, 1984).
Brown shrimp use an ambush strategy and rarely actively search or pursue their prey (Gibson
et al. 1995). Juvenile shrimps eat mainly meiofauna a nd shift towards a diet on macrofauna-s ized
items when they reach a total length over 20 mm (Pihl & Rosenberg 1984, Gee 1987). Food items
are taken approximately in relation to their relative occurrence (Pihl & Rosenberg 1984), and there-
fore the brown shrimp has been defined as a trophic generalist (Evans 1983, Pihl & Rosenberg
1984), omnivorous (Lloyd & Yonge 1947, Muus 1967, Tiews 1970, Kuhl 1972) or a carnivorous
opportunistic (Pihl & Rosenberg 1984) and even cannibalism is very common (Marcha nd 198 1).
Feeding and growth of the brown shrimp occur at least within a temperature range between
soc and 25°C (M. Fonds unpublished, cited in Van Lissa 1977 and in Kuipers & Dapper 1981). In
the laboratory maximal growth showed a positive relationship with increasing temperature and an
inverse relationship with shrimp size (Figure 6). From these growth experiments in aquaria the fol-
lowing growth equation could be determined between daily length growth (dL/dt; mm d- 1), water
temperature (T; oq and shrimp body size (L; mm):
74
--10mm -- 30mm · · · · ·50mm

- - 20mm -----40 mm - - 60mm
0.3
--o
I
E 0.2
5
..c
0
ｾ＠ -...-.......... _.... .......-
0.1
l5
_....
_....
_....
0
0 5 10 15 20 25
Water temperature (•q
Figure 6 Body size growth (mm d- 1) of juvenile and adult shrimp Crangon crangon in relation to water
temperature (0 C) and shrimp size (mm) in the laboratory under optimal food conditions. (Data after M . Fonds
(unpublished observations cited in Van Lissa 1977 and Kuipers & Dapper 1981).)
dL/dt = 0.1625 + 0.01025*T- 0.00403*L (9)
Juvenile shrimps show maximum growth at about 25°C (Van Lissa 1977, Freitas et al. 2007). In rela-
tion to adults, juveniles show faster growth and are more tolerant of high temperatures (Van Donk &
De Wilde 1981). Young shrimps also seem to prefer lower salinities than adults (Marques 1982).
Adult stage
The maturity of females is easy to evaluate by the presence of eggs, while in males it can only be
estimated since they have no external feature revealing this status (Muus 1967, Schockaert 1968).
Therefore there is more information about female maturation and it has been assumed that maturity
of males occurs at the same time as for females (Muus 1967), which might be incorrect.
The described variability in size and age at maturity in C. crangon suggests that they mature
in a similar way to various fish species, such as plaice Pleuronectes platessa, according to a trajec-
tory in the length and hence age (Rijnsdorp 1993). In fish this maturation envelope is a reflection
of the result of becoming sexually mature when the animal has passed some fixed size threshold
(Roff 1991) in combination with a distinct spawning period of once a year. In Crangon crangon
size at maturity seems to be more related to temperature than to age (Meredith 1952). The size-
at-maturation threshold differs for males and females, whereby males become mature at a smaller
size (22-43 mm total length) than females (30-55 mm total length) (Lloyd & Yonge 1947, Boddeke
1966, Muus 1967, Schockaert 1968, Meixner 1970, Marques & Costa 1983, Gelin et al. 2000, Oh
& Hartnoll 2004).
No detailed information is available about maturation in males. In females, bigger individu-
als seem to start to have eggs earlier than smaller ones (Meredith 1952, Marques & Costa 1983).
During the first stages of egg development there is a considerable increase in number of eggs but in
subsequent stages this increase tends gradually to cease (Spaargaren & Haefner 1998). The aver-
age number of eggs per female is positively correlated with body size but variability exists between
areas and between summer and winter eggs (Figure 7). There is a suggestion of a lower fecundity
during winter as a result of the limited volume of eggs that a female can hold because winter eggs
are larger (Henderson & Holmes 1987).
75
Havinga, 1930
Winter eggs; Boddeke, 1982
Overall; Boddeke, 1982
Winter eggs, Henderson & Holmes, 1987
Overall; Henderson & Holmes, 1987
Winter eggs; Oh et al., 1999
Summer eggs; Oh et al., 1999
Overall; Oh et al., 1999
15000
::s"' 10000
i5ll
"'
....
"'
.D
§ 5000
z
ＰＱＭＮＬｾ＠
30 40 50 60 70 80
Total length (mm)
Figure 7 Fecundity (number of eggs) in relation to total length (mm) of female C. crangon.
Feeding and growth of adult shrimps also occurs at least within a temperature range between
5°C and 20°C (M. Fonds unpublished in Kuipers & Dapper 1981). In the laboratory maximal growth
showed a positive relationship with increasing temperature, an inverse relationship with shrimp size
(Figure 6) and the same relationship as found for juveniles seemed to apply for adults, whereby no
differences were described between males and females (Van Lissa 1977, M. Fonds unpubli shed in
Kuipers & Dapper 1981):
dL/dt = 0.1625 + 0.01025*T- 0.00403*L (10)
where dL/dt is daily length growth (mm d- 1), Tis water temperature (0 C) and L is shrimp body
size (mm).
Adult shrimps can endure extremely low temperatures (Havinga 1930, Tiews 1970), but they
seem to be less tolerant of high temperatures (Van Donk & De Wilde 1981), although they live
in areas up to 30°C temperature (Havinga 1930, Tiews 1970). Actually, shrimps from all stages
of development can tolerate a combination of temperature of -l.8°C and salinity between 18 and
26 ( Boddeke 1975). The salinity optimum at 20-22°C is around 28-29 for 2-yr-old shrimps and
15-20 for 1-yr-old shrimps, while at 3-5°C the salinity optimum is 33. Therefore with increasing
temperature the salinity optimum shifts towards less-saline water, which means that brown shrimp
can stand lower salinities better when the temperature is high. In contrast, with increasing age the
salinity optimum shifts towards a higher salinity (Broekema 1942). Therefore young shrimps can
endure lower salinities than older ones (Tiews 1970). Optimum salinity also differs between sexes,
being higher for males than for females at least at I5°C (Lloyd & Yonge 1947). Although brown
shrimp can be found within a salinity range of 5-35 (Hagerman 1971), males cannot withstand such
low salinities as females and die at salinities below 10 (Lloyd & Yonge 1947). Females usually avoid
salinities under 12.6. Finally, low salinity increases the duration of the ovarian cycle since it delays
brown shrimp maturation (Broekema 1942, Spaargaren & Haefner 1998, Gelin et at. 2001).
76
Food and role as predator

Food
Crangon crangon is characterized as either a trophic generalist (Evans 1983, Pihl & Rosenberg
1984) or an omnivorous (Lloyd & Yonge 1947, Muus 1967, Tiews 1970, Kuhl 1972) or carnivorous
opportunistic (Pihl & Rosenberg 1984).
The diet of brown shrimp includes both meiofauna and endobenthic macrofauna as evidenced
by field studies (Pihl & Rosenberg 1984, Pihl 1985, Nilsson et al. 1993) and experiments (Hedqvist-
Johnson & Andre 1991, Nilsson et al. 1993) and consists of three predominantly bottom-dwelling
categories: infaunal organisms (bivalves, cumaceans, foraminiferans, harpacticoids, nematodes,
oligochaetes) (Jensen & Jensen 1985, Oh et al. 2001), epifaunal organisms (amphipods, isopods,
gastropods) and demersal organisms (mysids, shrimps and fishes). As a consequence, cannibalism
is also very common (Marchand 1981). Potential prey items change with increasing shrimp size
and shift from juvenile shrimps eating mainly meiofauna towards a diet on macrofauna-sized items
when they reach a total length over 20 mm (Pihl & Rosenberg 1984, Gee 1987). Part of the food
consists of regenerating body parts acquired by sublethal browsing of the siphon tips of bivalve spe-
cies (Bonsdorff et al. 1995).
Shrimps use an ambush strategy to catch their prey and rarely actively search or pursue their
prey (Gibson et al. 1995). Although Gibson et al. (1998) found that brown shrimp has higher activ-
ity during the light period, most authors state that it is more active (Nouvel-van Rysselberge 1936,
Hagerman 1970, Al-Adhub & Naylor 1975, Dyer & Uglow 1978, Van Donk & De Wilde 1981 , Gelin
et al. 2001) and predation rates are higher during darkness (Lloyd & Yonge 1947, Dyer & Uglow
1978, Ansell & Gibson 1993, Norkko 1998), with feeding peaks at dawn and dusk coinciding with
the period between low and high tide (Del Norte-Campos & Temming 1994). During daytime the
brown shrimp buries itself in the sand (Dyer & Uglow 1978, Gelin et al. 2001) and may attack prey
when they approach (Pinn & Ansell 1993).
Apart from selecting prey according to its size (larger shrimp eat larger prey) (Gibson et al. 1995),
food items are taken approximately in relation to their relative occurrence (Pihl & Rosenberg 1984),
so seasonal changes in the diet are mainly caused by fluctuations in food availability (Plagmann
1939, Pihl & Rosenberg 1984).
Role as a predator
Due to its high abundance, predation by C. crangon can have a significant effect on its prey popula-
tions (Evans 1984, Pihl & Rosenberg 1984, Pihl 1985, Norkko 1998) and hence it is considered an
ecologically important benthic predator (Reise 1977, Kuipers & Dapper 1981, Kuipers et al. 1981,
Jensen & Jensen 1985, Gee 1987, Matilla et al. 1990, Nilsson et al. 1993, Bonsdorff et al. 1995,
Cattrijsse et al. 1997, Oh et al. 2001, Hiddink et al. 2002)
Predation processes are in general based on size-based predation relationships. For instance,
based on stomach content analysis, it seems that fish predators should be in general four times
larger than their prey (Daan et al. 1990, Vander Veer et al. 1997). In the case of C. crangon, such
relationships will also determine to a large extent its potential prey spectrum. Its relatively small
maximum size of less than 9 em total length in combination with its demersal way of life implies
that predation is concentrated on demersal small prey items, small species or on the early and small
life stages of larger species.
Predation on siphon tips of bivalves is an example of consumption of parts of prey species,
the whole animal either being inaccessible or too large to tackle. Siphons are used by bivalves for
feedin g, defecation, reproduction and respiration and when they are extended near to or above the
sediment surface, these unprotected parts become vulnerable to predation. Predation on siphon
77
tips not onl y by shrimps but a lso by crabs a nd fi shes is a genera l phenomenon in coastal areas (e.g.,
Mace r 1967, Edwards & Steele 1968, De VIas 1979). Despite the fac t that siphon tips are regener-
ated , thi s type of predation has several important consequences for bivalves because regeneration
of lost siphon tissue takes up energy at the cost of growth and reproduction and induces behavioural
changes in bivalves (burying depth). Inhibited feeding and reduced growth have been observed
as a consequence of sublethal browsing of siphon tips by shrimps (Ka merma ns & Huitema 1994,
Bonsdorff et al. 1995).
Predation on small species includes meiofauna (Hedqvist-Johnson & Andre 1991 ) and oli-
gochaetes (Reise 1977). Although shrimp predation can be substa ntia l, there are no studies analysing
whether thi s type of predation is responsible for a top-down control of these small spec ies.
Predation on infaunal macrofaun a (Moller & Rosenberg 1983, Matilla et al. 1990, Beukema
et a l. 1998, Strasser 2002, Flach 2003) and on just-settled flatfish larvae (Vander Veer 1986, Van der
Veer & Bergman 1987, Pihl 1990, Vander Veer et al. 1990, Wennhage 2002, Amara & Paul 2003)
before they become too large for shrimps to prey upon (Pihl & Rosenberg 1984, Nilsson et a l.
1993) are examples of predation on early and small life stages of la rger species. Shrimp ca n prey
in the field on bivalve spat up to a size of a few millimetres (Figure 8A) and interannu al variation
I OMacoma • Cerastoderma 6. Mya

4
A
•
E'
3
•0
5
"'
N
·;;; 2
6.o
6.
"'> 6. t:,O
'iii"
> 6.
0
o6.
6.
0
0 20 4{) 60 80
Shrimp size (mm)
25
B
20
E'
5
"'
N
·;;;
15
>.
<lJ
c:
10
5
31-35 36-40 41-45 46-50 51-55 >=56
Shrimp size (mm)
Figure 8 Predator-prey size relationships for Crangon crangon as predator and (A) bivalve spat as prey
based on field data (sto mach content analysis) (mean spat size of various bivalve species from Vander Veer
et al. 1998) and ( B) flatfish la rvae as prey based on laboratory observations (mean flatfi sh larvae size (0),
together range (grey) and minimum and max imum observed size after Vander Veer & Bergman 1987).
78
in this predation has been suggested to be controlling bivalve recruitment (Van der Veer et al.
1997, Philippart et al. 2003). A similar size-based relationship is found for flatfish larvae as prey
(Figure 8B). In this case, predation by shrimps did not determine the recruitment of the flatfish ,
but acted as a fine control damping interannual variability (Vander Veer 1986). Cannibalism is the
most extreme form of predation and it is suggested to be very common in shrimps (Marchand I98 1).
Stomach content analysis in the Dutch Wadden Sea shows that cannibalism on just-settled shrimps
of about 6 mm total length occurs in shrimps over 30 mm in size (Derks 1980), which means a
predator-prey size ratio of about 5: l. There is no information available about the importance of can-
nibalism in controlling and regulating recruitment.
So far it is obvious that the role of predation by shrimps must be substantial due to their high
abundance. Top-down control has been suggested in some cases; however, this aspect has not been
studied in detail up to now.
Recruitment
Recruitment is defined as the process whereby juveniles survive to attain sexual maturity and join
the reproductive population. Shrimps become mature at a size between 22 and 43 mm total length in
males and 30 and 55 mm total length in females (Lloyd & Yonge 1947, Boddeke 1966, Muus l967,
Schockaert 1968, Meixner 1970, Marques & Costa 1983, Gel in et al. 2000, Oh & Hartnoll 2004) and
this normally occurs within the first year of life. Studies on the level and variability in recruitment in
C. crangon must therefore focus on the early life stage of C. crangon, where densities of more than
100 individuals per square metre are not uncommon (Berghahn 1983). So far such process-oriented
studies are lacking partly due to the shrimp's distribution patterns and extremely high abundance.
Recruitment seems to be successful in most areas and years since over a wide latitudinal range,
C. crangon is continuously abundant in shallow coastal systems (see for instance Tiews 1970,
Pihl & Rosenberg 1982, Kuipers & Dapper 1984, Oh et al. 1999). At this stage at least, water
temperature can be listed as an important abiotic factor: timing of immigration and settlement of
shrimp larvae is strongly related to prevailing water temperature (Beukema 1992) and recruitment
is positively related to water temperature (Henderson et al. 2006). Besides temperature, the North
Atlantic Oscillation (NAO) and river flow influence recruitment, probably due to their effects on the
productivity and growth of estuarine organisms (Henderson et al. 2006).
Whether just-settled juveniles suffer from growth limitation is unknown but there is no infor-
mation suggesting that starvation-induced mortality occurs. Hence, predation and cannibalism
might be an important source of mortality (Henderson & Holmes 1989). Nevertheless according
to Henderson et al. (2006) predator abundance in a 25-yr data series varied considerably through
time with no correspondence between the peaks and troughs in predator and C. crangon abundance.
Therefore top-down control alone seems to be insufficient to explain the regulation of the brown
shrimp population. The importance and impact of cannibalism should be studied in more detail
since Pihl & Rosenberg (1982) estimated that up to more than 20% of the annual food consumption
of C. crangon in Swedish shallow waters might consist of young shrimp. Whether cannibalism was
acting as a density-dependent source of mortality was not studied and it is unknown if cannibalism
acts as a controlling factor (generating interannual variability in recruitment) or as a regulating fac-
tor (damping interannual variability in recruitment).
Latitudinal gradients
Seawater temperature
Seasonal patterns in seawater temperature are the result of complex interactions whereby, especially
air-sea interaction, hydrodynamic processes and local bathymetry play an important role. On a large
79
sca le, trends in sea-surface temperature are to a large extent a reflection (with some time delay) of
trends in air temperature. Over the distributional range of C. crangon, a general latitudinal trend
in sea-surface water temperature is observed along the European coast, with average temperatures
decreasing with increasing latitude. In the Mediterranean a weaker trend is present, with increasi ng
temperatures from east to west due to a combination of factors (i.e., increasing air temperatures,
reduced influence of mixing by Atlantic oceanic water through the Strait of Gibraltar, etc.). Finally,
from Turkey into the Black Sea temperatures again decrease with increasing latitude. Along the
European coast, mean seawater temperatures vary between around 25°C in summer and I4°C in
winter in southern Europe and about l5°C in summer and 2°C in winter in northern Denmark and
in England (see, for instance, http://www.nodc.noaa.gov/OC5/indprod .html).
Most long-term datasets are collected in subtidal areas and there is less detailed information
available for surface waters and for intertidal regions (Figure 9). Along the European Atlantic coast,
the seasonal pattern in temperature shows maximum values in July-August and a minimum in win-
ter. Maximum summer temperatures vary from about 10°C at a latitude of70°N in Norway to about
21 °C at 4l 0 N in. Portugal. The seasonal fluctuation is lowest at highest latitude (about 8°C), high-
est at intermediate latitude (about l5°C) and intermediate at low latitude in Portugal (about l0°C).
In addition to seasonal fluctuations, daily fluctuations of several degrees occur (Figure 10). In the
Mediterranean, a similar seasonal pattern is observed, although summer temperatures appear to be
higher than along the European Atlantic coast with values above 20°C (Figure 9).
Seasonal migration
Changes in environmental factors, especially temperature (Boddeke 1976, Boddeke et al. 1976,
Beukema 1979, Spaargaren 1980, Henderson & Holmes 1987) and to a lesser extent salinity
(Broekema 1942, Lloyd & Yonge 1947, Tiews 1970, Labat l977a,b, Marques 1982, Henderso n &
Holmes 1987, Gelin et al. 2001), light intensity/day length (Spaargaren 2000) and food conditions
(Broekema 1942, Lloyd & Yonge 1947, Tiews 1970, Boddeke 1976, Spaargaren 2000), affecting
the physiological performance of shrimps are responsible for observed migration patterns , tidally
(Janssen & Kuipers 1980), daily (Hartsuyker 1966) and seasonally.
The most pronounced patterns are seasonal migrations, especially near lagoons and estuarine
areas. The temperature tolerance of the various life stages of C. crangon (Figure ll) suggests that
suboptimal or even lethal temperature conditions are the main forcing reason for the observed sea-
sonal migration patterns. Along the northern Atlantic coast the migration during autumn/winter to
deeper and often more saline waters can be considered as a refuge from the low winter temperatures.
The return to shallow brackish areas during spring/summer (Broekema 1942 , Lloyd & Yonge 1947,
Tiews 1954, Muus 1967, Boddeke 1976, Boddeke et al. 1976, Marques 1982, Baden and Pihl 1984,
Henderson & Holmes 1987, Beukema 1992, Attrill & Thomas 1996, Spaargaren 2000, Drake et al.
2002, Gibson et al. 2002) can be explained by a search for warmer temperatures (Spaargaren 1980).
More southwards, in the Mediterranean , and in some years also a long the Atlantic coast, migration
movements in summer to deeper waters seem to be an escape from excessively high temperatures
in search for colder waters (Labat 1977a). Above 27°C an exodus of C. crangon from the intertidal
towards deeper water occurs (Berghahn 1983, 1984).
Various other abiotic and biotic factors can complicate the seasonal migration patterns. Firstly,
salinity directly affects the temperature tolerance of shrimps: at low temperatures shrimps prefer
Figure 9 (see facing page) Seasonal pattern in water temperature (°C) a long the European Atlantic coast.
Data source: Valosen, Norway (J. Campos & V. Freitas unpublished observations); Sandvik, Sweden (Pi hi &
Rosenberg 1982); Balgzand , The Netherlands (H.W. Vander Veer & J.IJ. Witte unpublished observations);
Gironde, France (Bachelet 1986); Minho, Portugal (J. Campos & Y. Freitas unpublished observations) and
Vacca res , France (Gel in et al. 2000). Mean values are presented together with observed range (if availab le).
80
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Figure 10 Daily fluctuations in water temperature (0 C) in the surface water of the Marsdiep near the south-
ern part of the Isle of Texel, western Wadden Sea, The Netherlands. (Data after H. M. Van A ken, unpublished
observations.)
30
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Egg Larvae Juvenile Adult
Figure 11 Optimal temperature range (°C) of Crangon crangon in relation to life stage. For references see
text.
high salinities, while at high temperatures, low salinities are preferred (Broekema 1942). Especially,
the combination of low temperature and low salinity is avoided (Broekema 1942, Van der Baan
1975, Marques 1982). On the other hand, despite low temperatures in winter, when salinity is over
25 apparently it is unnecessary to migrate from the estuary (Meredith 1952). Also many shrimps
remain in the open sea in Atlantic waters during summer, suggesting that there is no physiological
necessity to live in lower salinities at higher temperatures (Spaargaren 1980).
Another factor is life stage. The young (and smaller) shrimps (Temming & Damm 2002)
and ovigerous (berried) females (Lloyd & Yonge 1947, Van der Baan 1975) are the first invad-
ing shallow areas in spring/summer, while the bigger ones are the first to leave these areas in
winter (Muus 1967, Boddeke et al. 1976). Emigration to deeper waters is size dependent since
shrimps tend to inhabit deeper zones as they grow (Spaargaren 2000), resulting in increasing aver-
age size with depth (Del Norte-Campos & Temming 1998). Furthermore, migration differs with
age and sex groups (Boddeke 1976), which partly reflects differences in the reproductive cycle
(Van der Baan 1975, Boddeke 1976, Kuipers & Dapper 1981, Henderson & Holmes 1987, Gelin
et al. 2001) whereby berried females and fertile males are more sensitive to temperature (Boddeke
1976, Boddeke et al. 1976) and prefer higher salinities, while young shrimps seem to prefer lower
salinities (Marques 1982). As a consequence, a second migration seawards may occur in summer
to reproduce (Henderson & Holmes 1987). In contrast, in the Mediterranean Sea brown shrimp
82
migrate seawards in spring/summer and return to shallow waters in autumn (Labat 1977a, Gelin
et al. 2000), although juveniles enter Mediterranean lagoons in spring to grow and females leave
these lagoons in winter to reproduce (Labat 1977b).
Reproduction
When referring to the reproduction period some authors mean the months/seasons of higher abun-
dance of ovigerous females , others refer to the timing of egg hatching and others to the period of
higher abundance of larvae. Taking this into account, the breeding seasons of brown shrimp seem
to vary with location (Figure 12). However, besides excluding mature males that are not clearly
identifiable, these studies usually exclude non-ovigerous females that are clearly mature on the basis
of ovarian condition or the form of their appendages (Oh & Hartnoll 2004).
At latitudes around 51-54°N, females with eggs are present all year (Meredith 1952, Kurc et al.
1965, Heerebout 1974, Boddeke 1982, Marques 1982, Moreira et al. 1992, Del Norte-Campos &
Temming 1994), although, in some cases, less abundantly .in autumn, which may be considered to
be a resting period (Lloyd & Yonge 1947, Meredith 1952, Tiews 1954, Boddeke et al. 1976, Boddeke
& Becker 1979, Duran 1997, Oh & Hartnoll 2004).
Bergen (Norway)
60
Oresund
55 Baltic Sea
Bus urn 1--
adebusum
Dutch Wadden Sea
Bristol Channel
50
45
Languedoc coast
40 1
S 0 N D J F M A M I J A S 0 N D J
Month
Figure 12 Reproductive period of Crangon crangon in relation to latitude. (Data after Kuipers & Dapper
1984, based on Tiews 1970.) Shaded areas represent fixed winter spawning season and the shifting summer
spawning.
83
In the Mediterranean and Baltic Seas, only one spawning season is reported corresponding,
respectively, to the coldest months (Labat 1977a, Crivelli 1982, Gelin et al. 2000) and to summer
(Henking 1927, Muus 1967). Along the Atlantic coast the number of spawning periods increases
with latitude up to three per year and/or these periods are more protracted , sometimes overl apping
each other (subsequent spawning periods start before the previous one has finished) (Lloyd & Yonge
1947), although to the south, in the Tagus estuary, brown shrimp reproduce throughout the year, but
mainly during spring (Marques 1982).
Fecundity of brown shrimp seems to be significantly higher at southern latitudes in the
Mediterranean when compared with the fecundity along northern Atlantic coasts (Gel in et al. 2000,
2001), although this may reflect different genetic subpopulations and not latitudinal variation.
Overall , the reproductive period seems to shift from a restrictive period from summer/autumn
in the northern part of the distribution via all-year-round reproduction to a winter period near
the southern edge in the Mediterranean (Figure 12). In areas where reproduction seems to occur
throughout the year spawning peaks seem to shift from north to south, from summer in German and
Danish coasts (Tiews 1970) to winter in the Dutch Wadden Sea.
According to Oh & Hartnoll (2004), differences between winter and summer broods are not in
egg numbers but the mean egg volume and dry weight of the eggs. Consequently, the reproductive
investment of C. crangon is higher in a winter brood than in a summer brood.
The migration of ovigerous females and fertile males to deeper and more saline areas may dis-
tort the conclusions of previous studies. Therefore, probably in some of the latitudes represented in
Figure 12, the reproduction period may be greater in extent. Furthermore, the percentage of oviger-
ous females may not reflect quantitatively the reproduction cycle because of the great fluctuations in
the size of the stock of mature females (Boddeke & Becker 1979).
Life-history traits
Size at hatching
The length at hatching is 2 mm, increasing to 4.6-4.7 mm at the end of the last larval stage, when
the animal settles (Lloyd & Yonge 1947). Larvae hatching from summer eggs are smaller than the
ones from winter eggs: respectively, 2.14 and 2.44 mm (Boddeke 1982). There is no information of
a latitudinal trend in size at hatch.
Settlement
In estuarine shallow areas settlement starts earlier than in marine sandy coastal places, coinciding
with the annual bloom of pelagic cope pods (Boddeke et al. 1985). In most places within the Atlantic
settlement takes place during the warmer period. After cold winters the moment of settlement and
peak densities of settlers are delayed (Beukema 1992). There is no in formation about settlement
period for the Mediterranean Sea.
Settlement occurs at 4-6 mm body length, in the first or second post-larval stage (Pihl &
Rosenberg 1982), at an average length of 4.7 mm (Kuipers & Dapper 1984). Due to lower winter
temperatures and consequently longer larval development time, in more northern areas the settle-
ment of post-larval shrimp is expected to take place later than in southern areas (Beukema 1992).
Growth
The analyses of growth and age are complicated by the fact that there are no visible morphometric
or other characters that are related to the age of C. crangon. In the past Tiews (1954) suggested a
method to determine growth and age based on the fact that the number of segments of the outer
antennae is directly related to the number of moults (Figure 13). In combination with information on
the relationship between the frequency of moulting and water temperature (Figure 14), the trends in
84
AUTECOLOGY OF C. CRANGON (L.) WITH AN EMPHASIS ON LATITUDlNAL TRENDS
I -+-Juvenile --e- Male ---•--- Female I

50
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Figure 13 Relationship between the number of segments (n) of the olfactory branch of the first antenna and
the number of moults (n). (After Tiews 1953.)
I --e-- 5.1"C - 9 . 8"C ｾ＠ 15.4"C

100
75
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Figure 14 Relationship between the frequency of moulting (n) and water temperature (°C). (After Tiews
1953.)
the number of segments of the antenna together with that in the prevailing water temperature would,
in principle, allow a reconstruction of growth patterns and hence age. This method has been applied
in the past by Tiews (1970) and was reintroduced by Schockaert (1968) in Belgian waters and by
Gelin et al. (2000) in the Mediterranean. Preferably, this method should be validated before it is
applied to other areas. However, this was not done by Schockaert (1968) or by Gel in et al. (2000); in
both cases basic information from Tiews (1954) for the German Wadden Sea was taken . The rela-
tionship between shrimp size and the number of segments seems to be rather robust. For the western
Dutch Wadden Sea a similar relationship was found (Figure 13); however, the observed variability
was greater than described by Tiews (1954).
With respect to the relationship between the frequency of moulting and water temperature, the
data ofTiews (l954) are puzzling. Tiews provides information for three temperatures: 5.1 °C, 9.8°C
and 15.4°C. In combination with the relationship between shrimp size and the number of segments,
85
100
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Total length (mm)
Figure 15 Relationship between total length of Crangon crangon (mm) and the catch efficiency (%) of a
2-m beam trawl with 5-mm mesh size, based on a series of comparisons of beam trawl and seine catches. Dots
represent measurements; line is polynomial function. (Data after Van Lissa 1977.)
growth rates can be calculated for the trajectory 18-45 mm (4-16 moults) and for the above tem-
peratures they are 0.5, 1.0 and 1.5 mm d- 1, respectively, which is far above maximum growth rates
found by M. Fonds (unpublished cited in Van Lissa 1977 and in Kuipers & Dapper 1981) and by
Meixner (1969) in the laboratory. This means that the relationship between water temperature and
frequency of moulting needs to be revalidated before the method of Tiews (1954) can be applied .
Furthermore, since moulting is related to growth, food conditions also play a role. Neither Tiews
(1954) nor Schockaert (1968) and Gelin et al. (2000) provide information on this aspect. Therefore,
their results should be considered as preliminary and not yet validated.
With the introduction of more quantitative sampling designs, the analysis of growth based on
shifts in size-frequency distributions over time became popular. However, the applicability of thi s
method is limited. First, most sampling gears, especially trawls, have a very low efficiency for the
smallest size classes (Redant 1978). For a 2-m beam trawl with 5-mm mesh size the brown shrimp
catch efficiency increases from about 28% for shrimp of 15- 20 mm total length to 100% for a size
of 50 mm onwards (Figure 15). Furthermore, migration movements and size-selective predation
processes bias the growth patterns over time.
Shifts in length-frequency distributions over time have been used for two different approaches.
With the aid of software programs such as ELEFAN, modal size class progressions over time have
. been used to determine the Yon Bertalanffy growth function (VBGF) parameters for each sex (Oh
et al. 1999). By this method , no differences in growth between the German Bight and the Irish Sea
could be found (Oh et al. 1999). As an alternative, Kuipers & Dapper (1984) assumed max imum
growth rates of shrimps in the field. By combining experimentally established maximum growth
rates in relation to temperature and shrimp size with the modal progressions in size-frequency
distributions, they calculated immigration and emigration patterns. However, Kuipers & Dapper
(1984) did not provide evidence in support of their assumption of maximum growth rates of shrimps
in the field.
This means that at present no reliable estimates of the growth rates of shrimps in the field
are available. Therefore the controversy about the origin of the exploitable stock in the German
and Dutch Wadden Sea in autumn, whether it is based on summer (Boddeke 1982) or winter eggs
(Kuipers & Dapper 1984), still exists, despite a recent study by Temming & Damm (2002), whose
analysis was also based on the assumption of maximum growth in the field .
86
Size at maturity
The onset of sexual maturity seems to be variable between 35 and 50 mm total length (Meredith
1952 summarized in Gelin et al. 2000 and in Oh & Hartnoll 2004). There is a weak suggestion of
an increase in size with decreasing latitude; however, it is unclear whether this really reflects geo-
graphical variation or whether it is caused by differences in criteria used between studies or is a
consequence of different genetic subpopulations instead of latitudinal variation.
Age
Most published information about age should be considered with some caution since so far reliable
estimates of growth rates of males and females in the field are lacking. Therefore, aspects such as
number of spawnings in the life cycle, age-specific reproductive investments and mortality sched-
ules and maximum lifespan cannot be analysed at present.
Published information shows that females attain a larger size than males (Meredith 1952).
Maximum size reported for females is 95 mm (Tiews 1954, 1970, Heerebout 1974), while males may
reach a maximum size of75 mm (Tiews 1970) but both are rarely attained (Kuipers & Dapper 1981).
Females live longer than males (Meredith 1952), up to 5 yr for females and 4 yr for males (Lloyd &
Yonge 1947, Henderson & Holmes 1987), and older shrimps are extremely rare (Tiews 1954).
There seems to be a difference in both maximum length and longevity with latitude, with a
tendency for greater longevity in intermediate latitudes (about 3 yr) decreasing towards edges of
distribution (1-2 yr), although Gelin et al. (2000) stated that lifespan decreased with latitude. The
reason for this difference may be related to reduced growth rate or to a shorter lifespan or a combi-
nation of both (Muus 1967). Nevertheless, information from the edges of the distributional area is
insufficient to substantiate this tendency.
Crangon crangon fisheries

Since the synopsis ofTiews (1970), several studies on brown shrimp fisheries have been published,
most being on the efficiency and selectivity of fishing gears (Polet 2000, Munro & Somerton 2002,
Polet 2002 , Polet et al. 2004, Revill and Holst 2004a, Polet et al. 2005), impacts (Safran 1987, Robin
1992, Boddeke 1996, Walter & Becker 1997, Berghahn & Purps 1998, Yorberg 2000, Cabral et al.
2002, Lancaster & Frid 2002, Gam ito & Cabral 2003), and measures to reduce by-catch (Berghahn
et al. 1995, Graham 2003) and discards (Revill & Holst 2004b). The influence of several factors on
C. crangon catchability includes population structure and sampling Strategy (Polet & Redant 1999)
and environmental variables such as temperature (Jeffery & Revill 2002), light level, sediment type
and turbidity (Addison et al. 2003) have also been studied. Additional information can be obtained
from the working group dedicated to the investigation of the brown shrimp fishery (Working Group
on Crangon Fisheries and Life History, WGCRAN) in the International Council for the Exploration
of the Sea (ICES), which meets and reports annually.
Fisheries characteristics
Because of its bottom-dwelling mode of life, C. crangon is caught with demersal fishing gear: for
a long time the most common gear used has been a pair of beam trawls (Tiews 1970). Nowadays,
the North Sea brown shrimp fishery is performed by about 620 vessels, with a maximum engine
power of 221 kW (300 hp) (Polet 2000, 2002), using twin beam trawls with a minimum mesh size of
20 mm 2 (inside mesh) due to small size of the target species (ca. 35-80 mm TL) (Revill et al. 1999).
Trawl design and sorting equipment vary considerably between countries and vessels (Lancaster
1999). The length of each beam varies from 6 min the Solway Firth fishery in the United Kingdom
(Lancaster 1999) to 7-9 min Belgium (Polet & Redant 1999). The parts of the fishing gear that make
87
contact with the sea bottom are mainly the shoes and the rollers of the ground rope; tickler chains
are not used (Vorberg 2000). Despite a considerable decrease in the number of vessels, the fishing
effort (fished area per unit time) increased considerably in the 1980s (Berghahn & Vorberg 1997).
After hauling, the catch is sorted on deck by means of a riddle (Lancaster 1999, Polet & Redant
1999, Graham 2003). This separates consumable size or 'consumption' shrimps (usually >45 mm
total length) from non-commercial by-catch (a wide variety of benthic species mostly crustaceans,
echinoderms and molluscs, fish and undersized C. crangon), which is discarded into the sea. The
catch is generally cooked on board the vessel. The consumption fraction is usually passed through
the riddle once more after cooking to separate fish or any small shrimps that were not separated
by the first riddling prior to cooking (Lancaster 1999).
At present there is no minimum landing size for C. crangon in the European Union (EU).
Traditionally it was determined by the limitations of hand picking as the 'pickers' could not unshell
very small individuals. Since the 1990s most of the shrimps are being landed rough (unpicked , i.e. ,
with shell) and exported and hence the selection of larger shrimps for consumption has become
less relevant, prompting fears that juvenile shrimps may be landed if the market conditions allow
(Lancaster 1999).
Fishing areas
The traditional fishing grounds (Tiews 1970) are still the most exploited areas: the brown shrimp
fishery is performed commercially mainly in the coastal zone and estuaries surrounding the North
Sea (Berghahn & Purps 1998, Polet 2000, 2002), along the German, Dutch, Belgian and Danish
coasts and on the east and west coasts of the United Kingdom. On a much smaller scale it is also
performed in several areas of the French coast (Robin 1992), in the Tagus estuary, Portugal (Cabral
et al. 2002), in the Adriatic Sea (D. Taglapietra personal communication) and in Romanian waters in
the Black Sea (D. Micu personal communication). In Algeria and Tunis there was a shrimp fishery
at least in the past (Holthuis 1980).
Landings
Seasonal patterns
Several environmental factors have been reported to affect the success of the Crangon fishery.
Light levels and endogenous rhythms affect its emergence behaviour (Hagerman 1970, A l-Ad hub &
Naylor 1975) and influence brown shrimp catchability. Light intensity in turn covaries with turbid-
ity and depth and hence these variables may also affect catchability (Berghahn et al. 1995, Addison
et al. 2003). Also sediment type is reported to affect the success of the fisheries (Addison et al.
2003) due to the preference of C. crangon for muddy or sandy substrata (Pinn & Ansell 1993).
Therefore muddy and sandy deeper areas are the ones that provide higher catch rates, especially
when the water is turbid and the light levels are low (Addison et al. 2003). In some studies especially
in shallow waters, brown shrimp catch rates are dependent on the tidal phase (AI-Adhub & Naylor
1975, Henderson & Holmes 1987, Berghahn et al. 1995, Lancaster 1999), but in deeper waters, it was
not considered to be the most relevant factor (Addison et al. 2003).
Seawater temperature clearly affects brown shrimp catchability since it influences the verti-
cal escape response of the shrimp to towed ground gear. However, small non-marketable shrimp
(<50 mm TL) are captured irrespective of seawater temperature (Jeffery & Revill 2002). A descrip-
tion of vertical escape behaviour of the species is given in Jeffery & Revill (2002). Another factor
affecting the success of brown shr.imp fisheries might be predation. Predation pressure is dependent
on both the abundance of the predators and the prevailing water temperature. Normally predation
pressure will covary with temperature and hence show a seasonal pattern . Gadoids are a main
88
predator of C. crangon. Berghahn (1996) reports a mass invasion of juvenile whiting Merlangius
merlangus causing a considerable decrease in brown shrimp abundance that was reflected in a steep
decline of North Frisian shrimp catches from June 1990 to July 1991 (Berghahn & Purps 1998).
As a consequence, indices of Crangon crangon abundance based on catch rates are biased by
systematic effects of environmental factors on its catchability (Del Norte-Campos & Temming
1994, Lancaster 1999). To overcome this, Addison et al. (2003) proposed an adjusted index of catch
rates incorporating information on light level, sediment type, turbidity and temperature that more
accurately describes trends in abundance.
Overall, fisheries for C. crangon show a quite stable seasonal pattern that is related to the local
environmental conditions and the recruitment patterns of juvenile shrimps. The normal pattern con-
sists of very low catches during winter, increasing catches in spring, a slight depression in catches
in June/July and a strong autumn fishery. However, peak autumn landings in recent years extended
to November/December and to September/November in German and Dutch fisheries, respectively
(Anon . 1996), instead of September/October in previous years (Boddeke 1982). In some areas such
as the Loire estuary and the Tagus estuary, brown shrimp fishing is only a summer activity (Robin
1992, Cabral et al. 2002).
Annual catches
The North Sea C. crangon fisheries are a valuable marine resource, with a market value between
€50-70 million (Polet 2002, Anon. 2006). Total North Sea brown shrimp landings increased with
oscillations from around LO,OOO t in 1970 to almost 30,000 t in the mid-1980s, then dropped to
about 10,000 t again in late 1980s. Since 1990, landings have increased and Danish, German, Dutch
and U.K. fleets attained a record catch of over 37,000 t in 2006 (Figure 16). Of these shrimp 87%
were landed by Germany and the Netherlands alone, with around 16,000 t each, while Denmark
accounted for ll%, with the remainder landed by the United Kingdom (Anon. 2006). In 1999, the
EU total allowable catch (TAC) was 26,000 t, valued at €53 million, and the German and Dutch
fleets account for 84% of the total landings (Revill et al. 1999). In the Tagus estuary 35 vessels
operate with an estimated annual catch of about 1750 t, of which approximately 90% is discarded.
However, although this fishery is targeting on brown shrimps (50% of the catches), due to a decrease
in its commercial value, flatfish such as Solea solea and S. senegalensis have become the main target
species in recent years (Cabral et al. 2002). For 2006 no EU TAC has been defined for brown shrimp
landings. Although targeting brown shrimp, the landings of fishery also include valuable round- and
----- DK - Ge --o-- -0-- NL

---B --------· France ---a- UK
16000
ｾ＠ 12000
"'c
""
'B
c 8000
..::!
::J
WJ
4000
0
1970 1974 1978 1982 1986 1990 1994 1998 2002
Figure 16 Landings (t) of Crangon crangon by various countries. (Data after Anon. 2006.) OK , Denmark;
Ge, Germany; NL, Netherlands; B, Belgium; UK, United Kingdom.
89
flatfish species like cod Gadus morhua, whiting Merlangius merlangus, dab Limanda limanda ,
plaice Pleuronectes platessa, flounder Platichthysfiesus and sole Solea solea (Polet 2000).
Annual fluctuations are not only determined by market conditions but also affected by envi-
ronmental variability. Relevant climatic factors are the winter NAO index plus the sea-surface tem-
perature in winter, which enhance recruitment of Crangon crangon and hence influence shrimp
landings in the subsequent autumn and spring fishing seasons (Anon. 1996). Still under debate
is the potential impact of eutrophication. Eutrophication due to river run-off in coastal waters is
assumed to improve densities of a major food resource for juvenile shrimps, the calanoid copepods
(Boddeke et al. 1986), and as a consequence result in enhanced shrimp catches (Boddeke 1978,
1996). However, it is unclear whether it would act on stock size (enhanced recruitment) or biomass
of individual shrimps (enhanced growth) and the underlying mechanisms of such a hypothesis are
not presented. Any suggestions so far are anecdotal or based on correlations.
In recent years a decline in U.K. landings has occurred that is consistent with the general trend
of the North Sea Crangon fishery to 'slide' in a north-easterly direction, possibly caused by climatic
factors (Anon. 1996).
Impact of C. crangon fisheries

Impact on shrimp stocks
Shrimp trawling has been claimed to be responsible for depleting shrimp stocks (Dahl et al. 1994).
Between 30% and 60% of the weight of C. crangon caught is currently discarded (Graham 1997,
Van Marlen et al. 1998). There is no legal minimum landing size for brown shrimp in the European
Union, but a minimum market size of 45 mm of total length (minimum carapace width of 6.5 mm),
though shrimp as small as 20 mm (TL) are regularly caught in these fisheries (Van Marlen et al.
1998). The discarding of non-marketable C. crangon in the North Sea is substantial in magnitude,
representing around 27,000 tor 75 billion individuals annually (Revill & Holst 2004b) and corre-
sponding to around 50% (Lancaster & Frid 2002) to over two thirds of the shrimp catch by number
(Van Marlen et al. 1998). In the Lower Saxony fishery in Germany marketable sized shrimps (over
50 mm total length- equivalent to 8 mm carapace length) made up only II% (by weight) of the
catch (Walter 1997). However, most undersized shrimps are separated from the catches by the
riddling process and return to the sea alive (Lancaster & Frid 2002). Their survival rate seems to
be high in the entire capture, hauling, riddling, discarding and bird predation processes: 75-80%
survival is estimated for the Solway Firth (Lancaster & Frid 2002) and for the Belgian fi shery
(Mistakidis 1958). The majority of mortalities seem to occur in the trawl and not in the riddling
process (Lancaster & Frid 2002). Moreover, it seems that natural mortality is much higher than
mortality caused by fisheries (Anon. 1979), which can be on average three times higher than fishing
mortality for shrimps over 30 mm total length (Tiews & Schumacher 1982).
Impact on the benthic community

Shrimp trawls are considered to be relatively light fishing gears with low impact on the sea bottom
(Rumohr et al. 1994, Vorberg 1997) and basically non-destructive (Stock et al. 1996). However,
besides disturbing the sediment surface during hauls, the beam trawl fishery in general has a con-
siderable impact on benthic communities, reducing the diversity of benthic species (e.g., Bergman &
Hup 1992).
Due to the small mesh size used and since fishing grounds are also densely inhabited by other
species, including juvenile fish, brown shrimp catches also include large amounts of by-catch,
which consists of a wide variety of non-commercial fish, especially gobies Pomatoschistus spp., and
benthic species (mostly crustaceans, echinoderms and molluscs) together with undersized brown
shrimp and commercial fish species (Anon . 1973, Mohr & Rauck 1979, Symonds et al. 1985, Sankey
90
1987, Boddeke 1989, Rauck & Wienbeck 1990, VanBeek et al. 1990, Kaiser & Spencer 1995, Walter
1997, Berghahn & Purps 1998, Polet 1998, 2002, Cabral et al. 2002), namely, some flatfish species,
such as dab Limanda limanda, plaice Pleuronectes platessa, flounder Platichthys flesus and sole
Solea solea (Garthe et al. 1996) and round fish species like cod Gadus morhua, whiting Merlangius
merlangus (Berghahn & Purps 1998, Polet 2000) a nd bib Trisopterus luscus (Safran 1987, Robin
1992). Other flatfish species are netted occasionally and in much lower quantity: Psetta maxima,
Scophthalmus rhombus, Buglossidium luteum, Microstomus kitt and Glyptocephalus cynoglossus
(Berghahn & Purps 1998).
This by-catch is discarded immediately after sorting onboard the vessels (Berghahn & Purps
1998, Po let 2000, Cabral eta!. 2002). Part of the by-catch may survive, but several factors contribute
to mortality of discarded animals, namely haul duration, tow depth, total volume of the catch, con-
ditions on deck, sorting process, temperature and species and size of individuals (Kelle 1976, Van
Beek et al. 1990, Berghahn & R0sner 1992, Berghahn et al. 1995, Kaiser & Spencer 1995, Cabral
et al. 2002, Gamito & Cabral 2003). Despite the fact that total fish by-catch attains only around
10% by weight (annual average) (Tiews 1990), the brown shrimp fishing fleet has a significant nega-
tive effect on the stocks of several North Sea commercially important species (Revill et al. 1999),
such as 0 and I age group plaice (Van Marlen et al. 1998), if the discard mortality due to the entire
brown shrimp, sole and plaice fisheries is considered (Berghahn & Purps 1998). In contrast, the
brown shrimp fishery has a relatively small impact on cod, whiting and sole. Annual landings lost
due to current levels in the European Crangon crangon fisheries have been estimated to be around
7000-19,000 t for plaice (Revill et al. 1999), valued at approximately €20 million (Van Marlen et al.
1998). This is equivalent to 10-25% of the 1998 TAC for plaice in the North Sea. Estimates for cod,
whiting and sole are 2000 t, 1500 t and 600 t, respectively (Polet 2002). In the Irish Sea the yield
of sole and plaice was estimated to reduce 1.4% and 8.9%, respectively, as a consequence of the
English west coast brown shrimp fleet activities (Sankey 1987).
Fishery waste may be eaten by fish, marine mammals and scavenging seabirds of (e.g., Hudson
& Furness 1988, Garthe et al. 1996, Walter & Becker 1997). Walter & Becker (1997) estimated that
6-14% (average 9.8%) of discarded shrimps by in the German C. crangon fishery is eaten by gulls,
mainly smaller ones like black-headed gulls Larus ridibundus and herring gulls Larus argentatus,
which had an average swallowing rate of 1.3 and 0.4 shrimps per minute, respectively. Discards may
also increase levels of particulate and dissolved organic matter, which in turn may attract scaven-
gers and decomposers (e.g., Berghahn 1990, Kaiser & Spencer 1995).
Synthesis
Distributional range
Along the European coast the brown shrimp Crangon crangon is one of the most widely distributed
spec ies showing, in general, continuously high abundances of juveniles and adults (Havinga 1930,
Boddeke & Becker 1979, Fabbiani 1979, Pihl and Rosenberg 1982, Berghahn 1983, Henderson &
Holmes 1987, Beukema 1992, Del Norte-Campos & Temming 1998, Beyst et al. 2001, Temming
& Damm 2002, Amara & Paul 2003), reflecting that annual recruitment must be successful under
most conditions. Detailed information on the factors determining the species' distributional limits
are lacking, although it will include the prevailing temperature conditions.
Despite the fact that the temperature to.lerance range varies between life stages, a minimum
temperature for C. crangon seems to be about soc. At such temperature egg and larval develop-
ment is slow and lasts a number of months. Low temperatures may even cause mortality to early
larval stages (Criales & Anger 1986). A longer larval stage also means a longer period of exposure
to predation. Hence, the limiting factor at the northern cold water edge of the distribution might be
91
formed by the temperature-induced length of the egg and larval development. Since temperature
conditions will show annual fluctuations, the distributional edge will also show spatial variability,
that is, expansion and contraction of the population range. This might explain the occurrence of
the species in Icelandic waters in 1895 (Doflein 1900) and the subsequent absence until the recent
reobservation by B. Gunnarson (personal communication).
Each species can only tolerate increasing temperatures within a specific range. At first , various
physiological rates increase exponentially with increasing temperature. Subsequently, metabolism
shows a further increase while food intake rate slows down (see, for instance, Willmer et al. 2000)
and hence the remaining scope for growth and reproduction decreases. At a certain temperature,
energy uptake can no longer compensate the metabolic demands . Under these conditions, an indi-
vidual cannot survive for long. Juvenile and adult stages are able to exhibit migration movements to
escape from these unfavourable conditions. However, this is not the case for the more passive larval
stages, which show a lower temperature tolerance compared with other life stages. With a decreas-
ing scope for growth the energy available for reproductive investment will decrease. Warm water
conditions may cause recruitment failure in spring due to starvation (Kattner et al. 1994). The warm
water distributional limit is therefore most likely to be a reflection of a mixture of limiting fac tors
(i.e., reproduction and survival of the larval stages).
Suboptimal temperature conditions occur more often at the edges of the distribution, both low
temperatures towards the northern edge and high temperatures at the southern edge. Therefore,
migration movements, tidally, daily and/or seasonally, will be more pronounced and often towards
both distributional edges, explaining the disappearance of shrimps in shallow waters in winter in
the northern part and in summer in the southern part of the distribution. There are also indications
that especially at high temperatures in the Mediterranean , salinity conditions might also act as a
trigger (Gelin et al. 2000, 2001).
Latitudinal trends
Previous studies of latitudinal trends in other marine species' life histories indicate some trends. In
exotherms, the physiological rates usually are higher with temperature. Thermal gradients would be
expected to have similar effects but various metabolic processes show ' latitudinal compensation':
individuals from colder high-latitude environments may maintain physiological rates nearly as high
as those from low-latitude localities. This is observed in some fish species like Menidia men idia,
Marone saxatilis, Fundulus heteroclitus, Sebastes diploproa, in which individuals from northern
populations have a higher inherited capacity for growth (Boehlert & Kappenman 1980, Isely et al.
1987, Conover & Present 1990, Nicieza et al. 1994, Schultz et al. 1996). The northern-derived cope-
pod Sco ttolana canadensis also grow faster at high latitudes (Lonsdale & Levinton 1985, 1989);
in contrast, the growth rates of the bivalve Macoma balthica become lower at increasing latitude
(Drent 2002, 2004). Faster growth seems to be related not only to temperature but also to the length
of the growing season. Later beginning (water warming up) and earlier ending (water cooling down)
of seasons causes shorter growing periods at higher latitudes. The trend of later spawning and
recruitment with latitude, such as the shift from winter to summer larval release in more northern
regions reported for the crab Carcinus maenas by Sprung (2001) also contributes to shorten the
growing season. However, other factors like food availability may be as important as temperature in
the structuring of latitudinal tendencies in life-history events (Drent 2002, 2004). Overwinter mor-
tality in northern fish populations is high and size selective (Schultz et al. 1998), despite the larger
energy storage in the north that prepares individuals for the colder season. The reserve accumula-
tion rate of somatic storage has a genetic basis (Schultz & Conover 1997).
An analysis of trends in life-history parameters requires insight into the subpopulation structure
of Crangon crangon. In this respect only limited information is available. In other species with a
92
similar distributional pattern, molecular techniques have revealed some patterns of subpopulation
structure at least between the Mediterranean and the Atlantic coast, but in some cases have also
demonstrated further grouping within these two areas (Gysels et al. 2004a,b, Roman & Palumbi
2004). Preliminary analysis in C. crangon based on morphometric variability and isoenzyme pat-
terns suggests that some form of subpopulation structure might be expected at least between the
Mediterranean and the Atlantic coast (Maucher 1961, Bulnheim & Schwenzer 1993, Henderson
et al. 1990). Therefore, the analysis of latitudinal trends in life-history parameters is restricted to
patterns along the coastline, thereby excluding the Mediterranean.
Despite the wealth of information available about various aspects of the biology, ecology and
life history of the species, it is amazing that there is still a lack of knowledge about essential aspects
of its role and functioning in the ecosystem. Most striking is the lack of knowledge about the growth
conditions for C. crangon in natural conditions. Recent studies on growth (Schockaert 1968, Gel in
et al. 2000) either refer to the work of Tiews (1954), ignoring the fact that differences in growth
conditions might be present, or assume maximum growth and apply model predictions to analyse
the life history in the field (Kuipers & Dapper 1984, Temming & Damm 2002). Conclusions about
age at maturity and maximum age that are based on these assumptions about growth should be
considered as preliminary as long as the assumptions about growth conditions in the field have not
yet been validated.
A starting point for the analysis of growth conditions in the field are laboratory observations
on maximum possible growth in relation to food conditions and temperature. For C. crangon basic
information is available from the work by M. Fonds and coworkers as referred to by Kuipers &
Dapper (1984). However, the underlying experiments have never been documented except for an
internal student's report (Van Lissa 1977), which means that at present the quality of the data cannot
be evaluated. Therefore, for C. crangon, more experiments on growth in relation to abiotic (tem-
perature, salinity) and biotic (food conditions, shrimp size) conditions need to be performed. Such
experiments should include so-called common garden experiments with individuals from different
populations over the range of the species to analyse whether counter-gradient growth compensation
does occur (cf. Conover & Present 1990). Once such information is available, growth conditions in
the field and in relation to the distribution of the species can be analysed. It is doubtful whether the
standard methods applied so far (i .e., estimates based on shifts in length-frequency distributions over
time) are applicable. Due to the continuous immigration of just-settled juveniles in combination with
size-selective predation and emigration movements, size-frequency distributions often do not pro-
vide insight into or reflect population growth. An alternative might be the introduction of dynamic
energy budgets (DEBs) (Kooijman 2000) for C. crangon. After estimation of only seven species-
specific parameters according to standard procedures (Kooijman 2000, Van der Veer et al. 2006),
the DEB model can be applied for the estimation of growth under prevailing temperature and food
conditions. Recently, this approach has been applied successfully for the analysis of food and growth
conditions in various bivalve species in the intertidal in the Dutch Wadden Sea (Cardoso et al. 2006).
It seems therefore worth trying to implement this model for the analysis of growth in C. crangon.
Present preliminary information suggests that there seems to be some patterns in life-history
parameters with latitude, which most likely reflect trends in temperature conditions. Reproductive
period shifts from a restrictive period in summer-autumn in the northern part via all-year reproduc-
tion to a winter period near the southern edge. This further suggests that reproductive investment
is highest in the centre of the distribution. An analysis of latitudinal trends of various life-history
parameters such as size at hatching, maximum age, size and age at first maturation can only be per-
formed after information about latitudinal trends in growth in the field becomes available.
More information on recruitment is also required. Crangon crangon is one of the most abun-
dant epibenthic predators and more information becomes available that it might regulate some of
its prey species, especially various bivalve species in temperate estuaries (Van der Veer et al. 1998,
93
Philippart et al. 2003). On the other hand, due to its high abundance over a wide latitudinal range
C. crangon is also an important food item for a variety of predators, especially fish species (Pihl
1985). Nevertheless, there are no indications of top-down control by predators. Any insight in pro-
cesses determining recruitment level and variability are lacking at the moment. In general in marine
species, recruitment is assumed to be determined in the early life stages when numbers are at a
maximum (Leggett & DeBlois 1994). The fact that predators exploit more the juvenile shrimp while
the fishery exploits more the adult shrimp after the predators have taken their toll might explain
why there are so far no suggestions of an impact of the shrimp fisheries on recruitment (Welleman
& Daan 2001).
The above account indicates that there is an urgent need for various types of process-oriented
studies on aspects of the life history in C. crangon over its latitudinal range.
Future research
Future studies should include a detailed genetic analysis of the various Crangon species to resolve
the present uncertainties in this genus, followed by the analysis of the genetic population structure
of C. crangon by means of molecular tools. A basic gap in knowledge is the lack of information
regarding growth conditions in the field in relation to abiotic and biotic conditions, including the
possibility of counter-gradient growth compensation. Such information would provide insight in
the population structure and dynamics of C. crangon over its distributional range and form a start-
ing point for recruitment studies. This would also finally result in an analysis of latitudinal gradients
in life-history parameters. It is questionable whether this can be based on existing knowledge since
additional information from the northern part of distributional range seems to be required .
Acknowledgements
This study was funded by FCT, Portugal, through the grant SFRH/BD/11321/2002, the project
POCI/CLI/61605/2004 and in part by the EU project Resolving Climatic Impacts on Fish Stocks
(RECLA IM); EU Contract Number 044133.
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Oceanogra{Jhy and Marin e Biology: An Annual Review, 2008, 46, I 05-202
© R.N. Gibson, R. J. A. Atkin son , and J.D. M. Gordon , Editors
Taylor & Francis
BIOLOGY OF THE PLANKTONIC STAGES

OF BENTHIC OCTOPUSES
ROGER YILLANUEVA 1 & MARK D. NORMAN 2
1/nstitut
de Ciencies del Mar (CSIC), Passeig Maritim de Ia
Barceloneta 37-49, E-08003 Barcelona, Spain
E-mail: roger@icm.csic.es
2 Sciences, Museum Victoria, GPO Box 666, Melbourne, Vic 3001, Australia
E-mail: mnorman@museum.vic.gov.au
Abstract Octopuses of the family Octopodidae adopt two major life-history strategies. The first
is the production of relatively few, large eggs resulting in well-developed hatchlings that resemble
the adults and rapidly adopt the benthic habit of their parents. The second strategy is production of
numerous small eggs that hatch into planktonic, free-swimming hatchlings with few suckers, simple
chromatophores and transparent musculature. These distinctive planktonic stages are termed para-
larvae and differ from conspecific adults in their morphology, physiology, ecology and behaviour.
This study aims to review available knowledge on this subject. In benthic octopuses with plank-
tonic stages, spawning characteristics and duration of planktonic life seem to play an important
role in their dispersal capacities. Duration of the hatching period of a single egg mass can range
from 2 days to II wk, while duration of the planktonic stage can range from 3 wk to half a year,
depending on the species and temperature. Thus these paralarvae possess considerable potential
for dispersal. In some species, individuals reach relatively large sizes while living as part of the
micronekton of oceanic, epipelagic waters. Such forms appear to delay settlement for an unknown
period that is suspected to be longer than for paralarvae in more coastal, neritic waters. During the
planktonic period, paralarval octopuses feed on crustaceans as their primary prey. In addition to
the protein, critical to the protein-based metabolism of octopuses (and all cephalopods), the lipid
and copper contents of the prey also appear important in maintaining normal growth. Littoral and
oceanic fishes are their main predators and defence behaviours may involve fast swimming speeds,
use of ink decoys, dive responses and camouflage. Sensory systems of planktonic stages include
photo-, mechano- and chemoreceptors controlled by a highly evolved nervous system that follows
the general pattern described for adult cephalopods. On settlement, a major metamorphosis occurs
in morphology, physiology and behaviour. Morphological changes associated with the settlement
process include positive allometric arm growth ; chromatophore, iridophore and leucophore genesi s;
development of skin sculptural components and a horizontal pupillary response. At the same time,
anima ls lose the Ki:illiker organs that cover the body surface, the 'lateral line system' and the oral
denticles of the beaks. Strong positive phototaxis is a common response for hatchlings and some later
paralarval stages but this response reduces, disappears or reverses after settlement. There are many
gaps in our knowledge of the planktonic phases of benthic octopuses. Most of our understanding
of octopus paralarvae comes from studies of just two species (Octopus vulgaris and Enteroctopus
dojieini) and knowledge of the vast majority of benthic octopus species with planktonic stages is
considered rudimentary or non-existent. Research is needed in a variety of fields, from taxonomy
to ecology. Studies of feeding and nutrition are critical in order to develop the nascent aquaculture
of key species and ageing studies are necessary to understand planktonic population dynamics,
105
ROGER VILLANUEVA & MARK D. NORMAN
particularly in commercially valuable spec ies targeted by fisheries . Current and potential anthro-
pogenic impacts on these early life stages of octopuses, such as pollution , overfishing and global
warming, are a lso identified.
Introduction
Amongst the cephalopods, one of the most familiar groups is the bottom-dwelling or benthic octo-
puses of the family Octopodidae. This large family contains over 200 species (Norman & Hochberg
2005a), which range in size from pygmy taxa mature at <I g (e.g., Octopus wolfi) to giant forms
exceeding 100 kg (e.g., Enteroctopus dofieini) (Norman 2000). Member species occupy all marine
habitats from tropical intertidal reefs to polar latitudes and into the deep sea to nearly 4000 m (Voss
1988). Benthic octopuses adopt two major life-history strategies (Boletzky 1977a, 1992). The first
is production of relatively few, large eggs resulting in well-developed hatchlings that resemble the
adults and rapidly adopt the benthic habit of their parents (Figure LC,D). The second strategy is
production of numerous small eggs that hatch into distinctive free-swimming, planktonic and semi-
transparent hatchlings occupying ecological niches distinct from those of the adults (Figure I A,B).
This latter category of hatchling typically has poorly developed limbs, few suckers, simple chro-
matophores and transparent musculature.
This marked contrast between the morphology and ecology of the planktonic stages of cephalo-
pods and their adult form led to the coining of the term 'cephalopod paralarva'. Young & Harman
(1988, p. 202) defined paralarva as "a cephalopod of the first post-hatching growth stage that is
pelagic in near-surface waters during the day and that has a distinctly different mode-of-life from
Figure 1 (See a lso Colour Figure I in the insert following p. 250.) Planktonic and benthic hatchlings in
Octopodidae. Adult female Wunderpus photogenicus 26 mm ML in laboratory carrying egg strin gs with
developing embryos within the arms (A) and hatchling (total length -3.5 mm) from same egg mass (B).
Note the well-developed dorsal mantle cavity of the paralarvae. (Reproduced with permi ssion from Mi ske &
Kirchhauser 2006.) Female Octopus berrima at the time of hatching in the laboratory with a benthic j uvenile
hatchling (total leng th -20 mm) in foreground (C) and within 10 min o f hatching (D) showing well-developed
arms and chromat ic a nd sculptural components of the skin. (Photos: David Paul.)
106
BIOLOGY OF THE PLANKTONIC STAGES OF BENTHIC OCTOPUSES
that of older con specific individuals". This term alludes to the metamorphic transformations seen in
arthropods and fishes from a larval juvenile form to a morphologically distinct adult form . As the
transformation in cephalopod species with planktonic young is less dramatic, the term 'paralarva'
was considered appropriate. Octopus paralarvae can be considered members of the meroplankton
because these young octopuses live as plankton for only a part of their life cycle. According to their
size (in total length), most planktonic octopuses can be considered mesoplankton (0.2-20 mm)
(Harris et al. 2000).
Egg size and adult body size show significant variation within the family Octopodidae (Hochberg
et al. 1992). Pygmy species with benthic young can produce eggs smaller in size than those of giant
taxa with planktonic young. As a consequence, egg size alone is not an effective indicator of which
Iife-hi story strategy is adopted. Boletzky ( l977a, 1978-1979) proposes that egg size relative to body
size is a more effective predictor. He proposes that the boundary between these two strategies
occurs when egg length represents 10-12% of mantle length (ML). Eggs >12% of ML produce ben-
thic hatchlings while eggs <LO% of ML produce planktonic hatchlings. Table l lists those octopus
species known or likely to have planktonic paralarvae. It comprises three classes of information-
species for which planktonic paralarvae have been described; species that produce small-type eggs
(<10% of ML; sensu Boletzky, l977a); and species for which only submature material is available
and eggs in the submature ovary are numerous and appear to be of the small-type category.
After residence in the plankton of varying duration, octopus paralarvae undergo a dramatic
morphological and ecological transition from a free-swimming pelagic animal to the predomi-
nantly benthic life of the juvenile stage. The end of the paralarval period varies, dependent on the
spec ies and/or the environmental context. Some species such as Octopus vulgaris have a relatively
short presettlement period during which they rapidly become benthic in habit. Other paralarvae
have an expanded, transitional presettlement phase split between periods of swimming in the water
column and benthic crawling. There is a third category of a prolonged/suspended paralarval state
in which some paralarvae reach considerable sizes in epipelagic waters. At the start of this pelagic
period , these relatively large, actively swimming young octopuses (<2 em total length) can be con -
sidered planktonic (sensu Omori & Ikeda 1984) because their power of locomotion is insufficient to
prevent them from being passively transported by currents. At the end of this phase, however, they
are clearly micronektonic (sensu Pearcy 1983, animals 2-LO em in total length), attaining the ability
to swim freely without being overly affected by currents.
Most of our knowledge of octopus paralarvae comes from studies of just two species, 0 . vul-
garis a nd Enteroctopus dofleini, potentially due to both their fisheries value and their proximity to
major centres of scientific research in the Northern Hemisphere. At this stage, knowledge of the
vast majority of benthic octopus species with planktonic stages is considered rudimentary or non-
ex istent. This is despite references to octopus paralarvae dating back more than 2300 yr. Probably
referring to Octopus vulgaris paralarvae of the Mediterranean Sea, Aristotle noted that "the crea-
ture is extraordinarily prolific, for the number of individuals that come from the spawn is something
incalculable" and " they are so small and helpless that the greater number perish". Hochberg et al.
(1992) drew together published and unpublished data on identification of octopus paralarvae and
proposed both a suite of taxonomic characters and a standardized format for morphological descrip-
tion. This work remains the seminal study on identification of octopus paralarva over a wide range
of taxa. Boletzky (2003) reviewed recent literature on the early stages of cephalopods, particularly
issues of yolk absorption and biological adaptations throughout these early growth stages.
A note of caution must be made on spec ies identifications for octopus paralarvae treated in the
literature. Considerable historical confusion surrounds the taxonomy of adult benthic octopuses (see
Norman & Hochberg 2005a). Similarly, the absence of detailed morphological descriptions for all
paralarval species and the lack of appropriate taxonomic tools mean that taxonomic identifications
for many studies (particularly those based on wild-caught paralarvae) must be taken as tentative.
107
Table 1 Species of Octopodidae known (or likely) to possess planktonic para larvae: maximum
values of egg length (ELmax• in mm) and egg length index (ELirnax• egg length as percentage
of mantle length)
Species ELm:u ELI '""' Reference Paralarvae hatched in laboratory
Abdopus abaculus 2.4 7.9 . Norman & Finn 2001

Abdopus aculeatus 3 7.2 Norman & Finn 2001
Abdopus 10nganus 2.8 Norman & Finn 2001
Amphioctopus aegina 2.4 4 Norman unpubl. data Eibl-Eibesfeldt & Scheer 1962,
Ignat iu s & Srinivasan 2006
Amphiocropus arenicola 2.7 -4 Huffard & Hochberg
2005
Amphiocropus burryi 2.5 Hochberg et al. 1992 Forsythe & Hanlon 1985
Amphiocropus exannularus 3.9 7.3 Norman 1992a
AmphiocLOpus kagoshimensis 1.8 Norman unpubl. data
Amphioctopus cf kagoshimensis 3.8 8.3 Norman & Kubodera
2006
Amphioctopus marginatus 3 4.3 Norman 1992b
Amphioctopus morori 6 7.8 Norman 1992a
Amphioctopus neglectus 7 Nateewathana &
Norman 1999
Amphiocropus ovulum 3 Sasaki 1929
Amphiocropus rex 3 6.5 Nateewathana &
Norman 1999
Amphiocropus robsoni 5.2 8.8 Norman 1992a
Amphiocropus siam ens is 1.7 Nateewathana &
Norman 1999
Amphioctopus varunae 2 3.3 Norman 1992a
Aphrodocropus schulrzei 7.5 7 Smith 1999
Callistocropus aspilosomatis Small type Norman 1992c
Callistocropus lechenaulrii Small type Norman unpubl. data
Cal/istoctopus lureus 0.8 Norman & Sweeney
1997
Callisroctopus macropus 2.5 Mangold 1998 Boletzky et al. 200 I
Calliswcropus nocrurnus Small type Norman & Sweeney
1997
Callisroctopus ornarus 3.5 2.7 Norman 1993
Cistopus indicus 4.5 3.8 Norman & Sweeney
1997
Eledone cirrhosa 7.5 Small type Boyle 1983 Man gold et al. 197 1
Enteroctopus dojleini 8 Small type Hochberg 1998 Gabe 1975,0kubo 1979,1980,
Marliave 1981, Snyder 1986a,b,
and others
Enrerocropus magnificus 7 1.9 Villanueva et a l. 1991
Enteroctopus megalocyathus 12 0.2 Ortiz et al. 2006 Ortiz et al. 2006
Euaxoctopus panamensis 1.4 Voss 1971
Hapalochlaena lunulara 3.5 Hochberg et al. 1992 Overath & Boletzky 1974
Macroctopus maorum 7 2.7 Stranks 1996 Batham 1957
Macrorriropus defilippi 2.1 Mangold 1998 Hanlon et al. 1985
Octopus alecto 2.5 Hochberg et al. 1992
Octopus berenice 1.5 Hochberg et al. 1992
108
Table 1 (continued) Species of Octopodidae known (or Iikely) to possess planktonic para larvae:
maximum values of egg length (ELmax• in mm) and egg length index (ELl max• egg length as
percentage of mantle length)
Species ELrll!IX ELl max Reference Paral arvae hatched in laboratory
Octopus bimacu/atus 4 Hochberg et al. 1992 Ambrose 1981
Octopus bocki 2 9.5 Norman & Sweeney
1997
Octopus campbelli 1.7 Small type O'Shea 1999
Octopus cyanea 2.5 1.7 Norman 1991 Van Heukelem 1973
Octopus fa von ius Small type Norman unpubl. data
Octopus filosus 1.8 Voss & Toll 1998
Octopus ha wiiensis 3 Hochberg et al. 1992
Octopus hummelincki 3 Hochberg et al. 1992
Octopus huttoni 3.1 O'Shea 1999 Brough 1965 (as Robsonel/a
australis)
Octopus joubini 4.8 Small type Voss & Toll 1998 Forsythe & Toll 1991
Octopus laqueus 2.8 Small type Kaneko et al. 2006 Kaneko et al. 2006
Octopus mimus 3 Small type Cortez et al. 1995a Zuniga et al. 1997, Warnke 1999,
Baltazar et al. 2000, Montoya 2002
Octopus parvus 1.8 Small type Sasaki 1929
Octopus rubescens 4 Hochberg et al. 1992
Octopus salutii 6 5 Hochberg et a!. 1992 Mangold-Wirz et al. 1976
Octopus se/ene 1.6 3.2 Voss 1971
Octopus tetricus 2.5 Hochberg et a!. 1992
Octopus 'tetricus' West 2.4 Norman unpubl. data Joll 1976, 1978
Australia
Octopus veligero Small type Hochberg unpubl. data
Octopus vitiensis 2 Norman unpubl. data
Octopus vulgaris 2.7 Hochberg et al. 1992 Naef 1928, Vevers 1961 , llami et al.
1963 and others
Octopus warringa 3 Small type Norman 2000 Norman 2000
Octopus wo(fi Small type Norman unpubl. data
Pteroctopus tetracirrhus 8.3 9 Boletzky 1981
Robsonella fontanianus 5 Small type Hochberg et al. 1992 Gonzalez et a!. 2006
Scaeurgus jumeau 2.6 II Norman et al. 2005
Scaeurgus nesisi 1.7 3.6 Norman et al. 2005
Scae urgus patiagatus 2.5 Hochberg et al. 1992
Scaeurgus tuber 2.7 6.2 Norman et al. 2005
Scaeurgus unicirrhus 2.5 Hochberg et al. 1992 Boletzky 1984
Thawno ctopus mimicus Small type Norman & Hochberg
2005b
Wunderpus photogenicus 3.6 10.1 Hochberg et a!. 2006 Miske & Kirchhauser 2006
Note: The list includes (I) species that produce small-type eggs (ELI< 10, sensu Boletzky 1977a), (2) species for which
only submature material is available and eggs in the submature ovary are numerous and appear to be of the small-type
category and (3) species for which planktonic paralarvae have been described from laboratory hatched individual s.
For such samples that are not directly linked to spawning adult females, there is potential for mis-
identification or oversimplification of the diversity of taxa represented in a region. As Hochberg
et al. (1992, p. 245) state, their work: "is a preliminary study whose sole purpose is to summarize
!09
the current status of our knowledge .... It should not be used as an identification manual without
considerable reservation and without further critical study".
A number of other octopod families have a completely pelagic life cycle that jncludes plank-
tonic hatchlings. These include the families Amphitretidae, Vitreledonellidae, Bolitaenidae and the
superfamily Argonautoida (AIIoposidae, Tremoctopodidae, Ocythoidae and Argonautidae). These
octopods are represented by approximately 21 species (Sweeney & Roper 1998) and have not been
included in the present review. Their origins and links to paralarval strategies are discussed in the
section 'Permanent paralarvae: neoteny and holopelagic octopuses', p. 182. The aim of the current
work is to review available knowledge on all aspects of octopus para larvae of the benthic octopuses
(family Octopodidae) and encompasses their diversity, spawning characteristics, morphology, sen-
sory systems, diet, biochemical composition, growth, behaviour, predators, distribution, settlement,
biogeography and evolution. This review is also presented as a vehicle for identifying gaps in our
knowledge and candidates for future research.
Spawning and hatching characteristics of benthic octopuses

with planktonic paralarvae and implications for dispersal
Egg care and duration of embryonic development
In all species of incirrate octopuses (including the benthic octopuses, family Octopodidae), the
eggs are highly vulnerable to predation (see ' Predators on egg masses and paralarvae', p. 170). The
eggs of these octopus groups only have the chorionic membrane protecting the ovum. They lack
the additional protective membranes, capsules or jelly masses found in other cephalopod groups
(Budelmann et al. 1997, Boletzky 1998). These additional outer layers appear to convey physical
and/or chemical protections that enable nautilus, cuttlefish, squid and cirrate octopuses to deposit
eggs that require no parental care. All female incirrate octopuses must guard their eggs throughout
the developmental period, after which the females die. The female must continuously clean the
egg surfaces with her suckers, vent il ate the eggs with water flushes from the funnel and protect
the eggs from potential predators. The eggs of these octopuses possess a stalk of varying length
(the 'chorion stalk') that is used to attach the egg directly to a hard substratum or can be joined
together to form egg strings or festoons (i.e. , Cosgrove 1993, Huffard & Hochberg 2005). The
eggs are typically attached to hard surfaces in protected shelters such as caves, crevices or mollusc
shells but in some groups can be carried directly within the webs of the female (i.e., as in some
pygmy species, Forsythe & Hanlon 1985; genus Wunderpus, Miske & Kirchhauser 2006; genus
Hapalo chlaena, Norman 2000; and genus Amphioctopus, Huffard & Hochberg 2005). Females of
wholly pelagic octopus families also carry the eggs in a variety of manners: within the arm crown
(families Bolitaenidae, Vitreledonellidae, Amphitretidae, Alloposidae), within greatly elongated
distal oviducts (family Ocythoidae), attached to small mineralized rods (family Tremoctopod idae)
or within an encased shell-like capsule (family Argonautidae) (Young 1972, Nesis 1987).
Eggs laid by octopuses with planktonic hatchlings typically number in the thousands but can
reach as high as 500,000 in Octopus vulgaris (Mangold 1983) and 700,000 eggs in 0. cyanea
(Van Heukelem 1983). However, lower numbers of eggs can also be produced by certain spec ies
with planktonic hatchlings (i.e., 450 for Wunderpus photogenicus; Miske & Kirchhauser 2006).
Body size constraints for pygmy octopus species that produce planktonic young also make it likely
that egg production for such species would be in the hundreds not thousands of eggs. Within each
species-specific range, temperature is the main factor regulating the development of the octopod
embryos, which is faster at higher temperatures. For small-egg species of the family Octopodidae,
the fastest embryo development is found in tropical species. Examples of rapid development are
18-20 days for Amphioctopus aegina incubated at 28-30°C (Ignatius & Srinivasan 2006), 21 days
110
in Octopus cyanea at mean temperature of 27. 1oc (Van Heukelem 1973), 22-25 days in 0. vulgaris
at 25°C (Mangold 1983), 22-30 days in 0. laqueus at 26°C (Kaneko et al. 2006) and 23 days at
26°C in Wunderpus photogenicus (Miske & Kirchhauser 2006). In contrast, cold-adapted species
have much longer embryo development, as found in the giant octopus Enteroctopus dofleini from
the north Pacific, which shows the longest known egg incubation period for an octopus species with
planktonic hatc hlings, lasting 161 days at 9.2-1 3.9°C when the female tends the eggs (Gabe 1975)
and up to 5-6 months at 9.4-l3°C when the eggs are incubated experimentally without the female in
breeder nets (Snyder 1986a, S. Snyder unpublished manuscript). For Eledone cirrhosa, 3-4 months
at 14-l8°C are necessary for hatching (Mangold et al. 1971).
The hatching process and dispersal

Stimulus for hatching
When an octopus embryo is fully developed inside the egg and apparently ready to hatch, the phys-
iological mechanism(s) that promote the hatching process are unknown. A natural tranquillizer
described in the perivitelline fluid of loliginid squid prevents premature hatching (Marthy et al.
1976); however, its presence in octopus eggs has not been assessed. Mechanical stimulation pro-
vided by the brooding female may aid or regulate the timing of hatching but no quantitative studies
have been done on this subject. During hatching, brooding females sometimes forcibly expel water
through the funnel over the eggs (Sarvesan 1969, Kaneko et al. 2006). This turbulence may act as a
stimulus to instigate hatching. During laboratory incubation of eggs without female care, hatching
predominantly occurred after agitation as has been observed for Octopus cf tetricus (Joll 1978 as
0. tetricus) and Enteroctopus dofleini (Snyder l986a).
Mechanics of hatching
Laboratory observations on Octopus bimaculatus showed prehatching individuals pumping ener-
getically in their egg cases prior to hatching (Ambrose 1981). To escape the chorion membrane, rapid
mantle contractions by the embryo may mechanically put pressure on the chorion membrane or it
may ensure that the hatching gland is pressed firmly against the inner wall of the chorion to ensure
direct application of the enzymatic solution released from this gland (see description p. ll8). Active
use of the anns and suckers has also been observed in some species such as Scaeurgus unicirrhus
(Boletzky 1984). After the enzymatic secretions of the hatching gland dissolve and hence perforate
the chorion membrane, the Kolliker organs also probably help to prevent the retraction of the emerg-
ing octopus back into the egg capsule during hatch ing (Naef 1923, Boletzky 1966) (see 'Surface epi-
thelia and integumentary structures', p. I 16). The hatching period can take up to 44 min to complete
under laboratory conditions in Octopus tetricus (Le Souef & Allan 1937 as 0. cyanea). A schematic
drawing of the hatching process is given in Figure 2.
Timing of hatching
In situ observations found that hatching occurred at night or in darkened conditions in egg masses of
Enteroctopus dofleini at 17-24 m depth (Cosgrove 1993), whereas daytime hatching was observed
for paralarvae of Octopus bimaculatus, swimming upwards and reaching depths of 1-5m below the
surface (A mbrose 1981). Under laboratory conditions, paralarvae of 0. cyanea hatch only at night
(Van Heukelem 1973) and both day and night hatching has been observed in 0 . cf tetricus (Joll
1978). In addition to embryonic rhythms, species-specific differences in the timing of hatching may
be influenced by adult rhythms. Mechanical stimulation provided by the brooding female on the egg
mass may differ between nocturnal and diurnal species, making maternal activity an unquantified
factor in the hatching process. Under laboratory conditions, non-brooding adult 0. vulgaris prefer
Ill
Figure 2 Line drawing showing the hatching process in Octopus vulgaris. The hatching gland (or Hoyle's
organ) is present on the distal tip of the mantle and the glandular cells are limited to a narrow transverse band.
The hatching gland and the Ktilliker organs covering the body surface have been emphasized to show position
and orientation. See text for details. (Original drawing from Jordi Corbera with permission.)
nocturnal activity patterns (Brown et al. 2006) and for this species most hatching events occur at
night (R. Villanueva personal observation).
Para larval hatching in cephalopod species without maternal care, as in the squid Loligo vulgaris,
is influenced by the transition from light to dark, which seems to function as a 'ze itgeber' or synchro-
nizer, stimulatinghatching (Paulij et al. 1990). The attraction of visual fish predators to the brooding
octopus site may prevent major hatching during daytime, selecting for night hatching to avoid preda-
tion (Van Heukelem 1973), as has been observed in other invertebrate larvae such as the hatching of
decapod crustacean zoeae (Forward 1987, Ziegler & Forward 2005, 2006). The tendency for sunset
and nocturnal hatching in octopus paralarvae needs to be confirmed and quantified, with the influ-
ence of tidal and lunar rhythms taken into account. Similarly, the roles of external synchronizers and
circadian rhythms in adult octopuses are poorly known (Houck 1982, Wells et al. l983a, Cobb et al.
1995a,b, Brown et al. 2006, Meisel et al. 2006) but future research on this field may shed light on the
potential links between female brooding behaviour and the timing of hatching.
Hatching duration within an egg mass

The hatching period from a single egg mass can be rapid (i.e., hours), continue over a few days or
for weeks, influenced by factors such as the duration over which the eggs were laid, the incubation
112
temperature and the species. Egg laying under aquarium conditions in temperate and tropical spe-
cies takes 10 days at 18.2-20°C in Octopus luteus (Arakawa 1962), 4-7 days at 21-2]DC (Caveriviere
et al. 1999) and 9 days at 17-I9°C in 0. vulgaris (Iglesias et al. 2004). In cold water species, it
takes 14 days at 9.2-l0.3°C (Gabe 1975) and 20 days at 15.2°C (Yamashita 1974) for Enteroctopus
dojleini, and for Eledone cirrhosa, it can take from 8 days (Joubin 1888), to 10-15 days at 14°C
(Mangold et al. 1971) or nearly 1 month (Gravely 1908). As a consequence of these diverse egg-
laying periods a single octopus egg mass can contain eggs in different developmental stages.
The duration of the hatching period of a single egg mass observed under laboratory conditions
ranges from 2 days at 26°C in Octopus laqueus (Kaneko et al. 2006) to 78 days at I0-12.8°C for
Enteroctopus dojleini (Gabe 1975). Examples of duration of hatching period from a single egg mass
in Octopodidae species with planktonic hatchlings are listed in Table 2. The times listed are likely
to be underestimates for all species as there have been no laboratory or field studies undertaken
that collected and quantified the daily hatching rate for these species. They probably underestimate
minor hatchings at the beginning and end of the hatching period. Advantages and disadvantages
of a single major hatching event in comparison with minor events spread over days to weeks have
not been quantified for cephalopods and, again, further research is required. Experimental designs
under laboratory conditions to quantify hatching should minimize observer influence as much as
possible. Variations in light regimes, degree of exposure of study animals (i.e., removal of protective
cover to allow observation can unnaturally expose the brooding octopus), observer behaviour, use
of flash photography, mechanical vibrations and temperature fluctuations may all act as hatching
stimuli for the embryos, causing or altering hatching processes. Wild brooding females disturbed by
human observers may also cause premature hatching through increased light levels, increased water
turbulence around the egg mass and behavioural responses by the female. Use of remote low-light-
level videography may be a promising avenue for investigating natural hatching processes.
Morphological characteristics of planktonic octopus paralarvae

At hatching, the external attributes of octopus paralarvae are distinctive and often markedly dif-
ferent from that of post-settlement juveniles and the first growth stages of species with benthic
hatchlings. All inner organs of planktonic octopus paralarvae are well differentiated at hatching
except for the reproductive system. However, there are few data on the development of the diges-
tive, circulatory, respiratory, excretory and muscular systems after hatching and prior to settlement.
Most information comes from embryological studies on prehatching and hatchling individuals and
has been reviewed by Boletzky ( 1989). The surface epithelia, integumentary structures, nervous and
sensory systems of the para larvae also have been the object of research and the present knowledge is
reviewed. The order of morphological and anatomical characters in this section follows Budelmann
et al. (1997).
Body form and musculature

One of the most evident attributes of octopus paralarvae is their largely transparent form. All mus-
culature is transparent including those of the mantle, head , arms, webs and suckers. This trans-
parency is not visible in preserved material as the musculature becomes opaque on fixation . This
transparency matches the planktonic lifestyle of the paralarvae, minimizing their silhouette, and
hence visibility, to predators (and prey) below. No studies have examined the microscopic structure
of the transparent musculature of octopus para larvae. The mantle musculature of some holopelagic
octopods contains thin outer layers of longitudinal and circular muscle enclosing a thick layer of
transparent gelatinous matrix supported by narrow strands of radial muscle (e.g., Amphitretus,
113
Table 2 Duration of hatching period from a single egg mass in Octopodidae species with
planktonic hatchlings
Hatching Temperature Laboratory
0
duration ( C) during or field
Species (days) hatching observation Comments Reference
Amphioctopus aegina 3 Np Laboratory Sarvesan 1969 (as

Octopus dollfusi)
3 28-30 Laboratory Ignatius & Srinivasan
2006
Amphioctopus burryi 10 23-24 Laboratory Forsythe & Hanlon 1985
Enteroctopus dojleini 39 12.5- 15.3, Laboratory Eggs incubated Okubo 1973
mean 13.9 without female
49 4-7 Laboratory Ruggieri & Rosenberg
1974
78 10-12.8 Laboratory Eggs incubated Gabe 1975
without female
30 14 Laboratory Okubo 1979
27 Np Laboratory Okubo 1980
45 9-13 Laboratory Eggs incubated Snyder 1986a,
without female unpubli shed
<7 Np Field Cosgrove 1993
Macroctopus maorum 10 Np Laboratory Batham 1957
Octopus laqueus 2-9 26 Laboratory 75% hatched in I h Kaneko et al. 2006
of the same day
Octopus mimus 14 16,20 and Laboratory No differences Warnke 1999
24 between
temperatures
Octopus cf tetricus 28 19 Laboratory Joll 1976
6 21
10 22 .6
8-15 20 Laboratory Eggs incubated with Joll 1978
and without female
Octopus vulgaris 6-12 22-23 Laboratory Vevers 1961
3-8 21-27 Laboratory Caveriviere et al. 1999
5 17-19 Field Caveriviere et al. 1999
Octopus huuoni 21 Np Laboratory Brough 1965 (as
Robsonel/a ausTralis)
Wunderpus phorogenicus 3 26 Laborato ry Miske & Kirchhauser
2006
Note: Np, not provided.
Haliphron, Mangold et at. 1989). A similar arrangement is likely to be present in octopus paralarvae
but as yet the histological structure of the musculature of these animals has not been examined.
General body proportions of octopus paralarvae vary throughout paralarval growth (Figure 3)
and between species. At hatching, planktonic octopuses are squat with arms shorter than ML. See
hatchlings in Figures 1B, 3A, 17A,D, 26, 27 and 41. A smaller proportion of species have paralarvae
with arms longer than ML, particularly micronektonic paralarval stages (Figure 4). The relative
length of different arm pairs also varies between some species and can be diagnostic at a generic level
(Hochberg et at. 1992). For example, some para larvae have arms of equivalent length (Figure 3, 6A),
114
Figure 3 (See a lso Colour Figure 3 in the insert.) Individua ls of Octopus vulgaris from hatchin g to settle-
ment obtained from rearing experiments described in Villanueva (1995). Im ages not to scale. Age (days) a nd
mantle length (ML) of the individuals measured fresh are (A) 0 days, 2 .0 mm ML; ( B) 20 days, 3.0 mm ML;
(C) 30 days, 4.3 mm ML; (D) 42 days, 5.9 ML; (E) 50 days, 6.6 mm ML; (F) 60 days , 8.5 mm ML. Octopuses
from this expe rim ent sett led between 47 and 54 days. Indi viduals were photographed under anaesthesia (2%
ethanol) potentially causin g chromatophore contraction in some cases. (Photos by Jean Lecomte, Observatoire
Oceanologique de Banyuls, CNRS. Reproduced with permission from Villanueva et a l. 1995, modified.)
those of the gen us Callistoctopus possess longer dorsal arm pairs (Figure 4A,B), the seco nd pair is
the longest in Euaxoctopus (Figure 5), whereas Macrotritopus defilippi paralarvae possess a longer
third arm pair (Fig ure 6, right), as do certain unidentified paralarvae (Figure 4B,C).
Sucker number, arrangement and relative size can also be used to separate species (Hochberg
et al. 1992). At hatching there are typically few suckers (three or four) present in a single straight
row. During growth suckers are added, with the double row gradually becoming apparent for gen-
era such as Octopus, Enteroctopus and Callistoctopus. Genera such as Eledone retain the single
row of suckers into adulthood. The body form and transparency of octopus para larvae show strong
parallels with a number of holopelagic octopuses (families Bolitaenidae, Vitreledonellidae and
Amphitretidae) and squids (fami ly Cranchiidae) (see ' Permanent paralarvae: neoteny and holope-
lagic octopuses', p. 182).
115
Figure 4 (See also Colour Figure 4 in the insert.) Micronektonic octopus paralarvae. Top, unidentified
paralarva of the genus Callistoctopus from the Coral Sea, Australia, showing longer dorsal arm pair. (Photos:
David Paul.) Centre, unidentified paralarva (Macrotritopus sp.?) from Hawaii showing long arms relative to
body length, particularly the third pair. (Photos: Chris Newbert.) Bottom, unidentified paralarva from Hawaii.
(Photos: Jeffrey Rotman.)
Surface epithelia and integumentary structures

Chromatic elements
As with many other cephalopods, octopuses possess three major chromatic elements within the
skin- chromatophores, iridophores and leucophores- that produce the different chromatic pat-
terns that play such important roles in octopus behaviour (Packard & Hochberg 1977, Hanlon &
Messenger 1996, Messenger 2001). Chromatophores are the primary chromatic element present in
the skin of octopus paralarvae. These organs are flexible pigment pouches surrounded by radiating
musculature. In the relaxed state, the elastic pigment sacs are tiny and effectively invisible within
the transparent musculature (Figure 7, left). Contraction of the radial muscles surrounding the pig-
ment sac causes it to expand significantly, resulting in display of a relatively large visible disc of
colour (Figure 7, right). In adult cephalopods, chromatophores of up to five colours are present in
the skin at densities of up to 200 mm- 2 (Packard & Sanders 1969), enabling presentation of complex
116
chromatic displays (Hanlon & Messenger 1996).

In octopus paralarvae, chromatophore numbers
are typically low and they are relatively large in
proportion to body size. Chromatophores of just
one or two colours (red and black) are typically
present, enabling expression of relatively simple
colour patterns, that is, uniform colour versus
transparency (contracted chromatophores).
At hatching, octopus paralarvae possess
a low number of large chromatophores, pres-
ent in fixed arrangements. They are known as
'founder chromatophores' and their mode of
growth and development is described in Packard
(1985). Patterns and positions of these founder
chromatophores can have taxonomic value and
Figure 5 Euaxoctopus panamensis, 11-mm mantle enable species identification (Hochberg et al.
length (ML). Note the large second arm pair, measur- 1992). The number and distribution of chro-
ing 32 mm long. Collected using lsaacs-Kidd mid water matophores on the skin over the arms, funnel,
trawls (IKMT) between 0 and 500 m depth , 09°N 90°W, eyes, head, mantle and perivisceral epithelium
off Costa Ri ca, eastern Pacific. (Reproduced with per-
(i.e., chromatophore fields) of octopus para-
mission from Nesis & Nikitina 1991 , modified.)
larvae can be used to separate species (Young
et al. 1989, Hochberg et al. 1992) (Figure 8).
Founder chromatophores remain relatively unchanged throughout ontogenetic growth and are still
visible subdermally in post-settlement animals in the same patterns of dark and dense chromato-
phores. These chromatophores are particularly evident in adults of pygmy octopus species and can be
diagnostic to species level (i.e., Octopus bocki and 0. wolfi) (Norman & Sweeney 1997). Reflective
tissues (iridophores) are not typically evident in the skin of octopus paralarvae, particularly in the
earliest stages. They are present, however, in the membranes enclosing the eyes and viscera, provid-
ing a reflective surface to these opaque body organs as an additional ambient light reflector appro-
priate for a pelagic environment (Figure 4 bottom). Small spots of dermal iridescence are evident
in some paralarvae, potentially produced from the bristles of the Kolliker organs (described in the
section 'Kolliker organs', p. 120) (e.g., unknown species; Figure 9). In some late-stage paralarvae,
potentially close to settlement, iridesce nce is visible in the position of the ocellus that is found in
oce llate spec ies (e.g., unidentified Amphioctopus sp.; Figure 9). Leucophores are white-reflecting
components of cephalopod skin. They are not typically evident in the skin of octopus paralarvae.
Figure 6 (See also Colour Figure 6 in the insert.) Unidentified paralarva from the Coral Sea, Australia ,
showing arms of equivalent length (left). (P hoto: David Paul.) Pa ralarva of Macrotritopus defilippi from
Caribbean Sea showing longer third arm pair (right). (Photo: Raymond Hixo n.)
117
Figure 7 (See also Colour Figure 7 in the insert.) Chromatophores contracted (left) or expanded (rig ht) on
the head of paralarvae. The left image corresponds to an unidentified paralarva of unknown genus and the
right image is from an unidentified paralarva of the genus Callistoctopus. Both individuals from Coral Sea,
Australia. (Photos: David Paul.)
A 8 c
Figure 8 Distribution of chromatophore fields in Octopodidae. (A) Left lateral view, optical section ; (B) dor-
sal view; (C) ventral view. Superficial or tegumental chromatophores are represented by stippled spots. A, arm;
AB*, arm base; ADM , anterior margin of dorsal mantle; AYM , anterior margin of ventral mantle; DE*, dorsal
eye; DH*, dorsal head; DM , dorsal mantle; F, funnel; PC , posterior cap; Y*, visceral; YH*, ventral head; YM,
ventral mantle. Extrategumental chromatophores are indicated by (*). (Reproduced with permission from
Hochberg et al. 1992.)
As with iridophores , these structures may be evident in paralarvae close to settlement. The simple
chromatic capacities of planktonic octopus paralarvae show a stark contrast with the complex skin
and capacities of the benthic hatchlings of octopus species with large eggs (e.g., Hapalo chlaena
maculosa, Figure 10).
Hatching gland
The hatching gland or Hoyle's organ is located at the posterior tip of the mantle (Figure 2). The
enzymatic action of this gland helps the octopus during the hatching process by dissolving the apical
pole of the chorion membrane. It is assumed that there is a protease hatching enzyme similar to that
described in squids (Paulij et al. 1992) although its presence in octopods has not been investigated.
118
Figure 9 (See also Colour Figure 9 in the insert.) Iridescence in octopus paralarvae. Left, unidentified par-
alarva showing scattered points of iridescence, potentially from Kolliker organs in skin. Right, Amphioctopus
sp. paralarva showing iridescent tissue in location of ocelli of ocellate octopuses. Both individuals collected
while night diving on a moonless night at-10m deep over a seafloor depth of 450 mat Osprey Reef, Coral Sea,
Australia. Photographs taken in shi pboard aquaria immediately after capture. (Photos: M.D. Norman.)
Figure 10 (See also Colour Figure 10 in the insert.) Hapa/ochlaena maculosa hatchling, a direct benthic
species, showing well-developed skin colour and scu lpture. ( Photo: David Paul.)
In embryos that do not execute the second reversion (Boletzky & Fioroni 1990), the hatching gland
also helps the animal to hatch via the opposite pole, adjacent to the egg stalk (Boletzky 1966). In
incirrate octopods, the glandular cells of the hatching gland are limited to a narrow transverse band
(Orelli 1959, Fioroni 1978, Boletzky 1978-1979, Boletzky 1982). The two different cell types and
structure described for the hatching gland of loliginid squids (Arnold & Singley 1989, Paulij &
Denuce 1990) have not been observed.
In addition to the chemical effects of the hatching gland enzymes, the hatching process is aided
by mechanical effort through powerful stroke movements of the mantle that enables the animal
to free itself from the chorion membrane (Figure 2). Active movements of the arms and suckers
have also been observed for Scaeurgus unicirrhus (Boletzky 1977b, 1984). There are no quantified
119
studies on the duration of the hatching process. In Octopus tetricus individuals can take up to
44 min to hatch under laboratory conditions (Le Souef & Allan 1937, as 0 . cyanea). The hatching
gland is a transitory organ. Soon after hatching the gland is shed along with the rest of the embry-
onic epidermis and its many ciliated cells (Budelmann eta!. 1997).
Kolliker organs
Kolliker organs are bristle-like structures present on the surface of the head, arms, funnel and
mantle of embryos, paralarvae and recently settled octopus individuals, giving the animals a punc-
tate appearance (Figures ll and 12). These organs are only found in incirrate octopods, including
individuals of some octopus species with direct benthic hatchlings such as Eledone moschata (Naef
1923, Boletzky 1973). First described by Kolliker (1844) from Argonauta embryos, they have also
been described by other authors (Querner 1927, Naef 1928, Adam 1939, Fioroni 1962, Boletzky
1978-1979, Joll 1978). Detailed description of the histology and ultrastructure of the Kolliker organs
can be found in Boletzky (1973) and Brocco eta!. (1974). These organs consist of three structural
components (Figure 13): (1) an ectodermal follicle of specialized cells, (2) an extracellular fascicle
of cannular rodlets secreted by the basal chaetoblast and (3) mesodermal muscles. These muscles
presumably help to evaginate the fascicle and spread the rodlets (Figure 13A). The length of the
Kolliker organs is relatively constant in preserved specimens (30-40 f.Jm) for species with very dif-
ferent hatchling size, representing 4% of the ML in Argonauta argo and 0.4% in Eledone moschata.
Their density in planktonic paralarvae is, however, higher than in benthic juveniles (Boletzky 1973).
In paralarvae of some species, high densities of Kolliker organs have been found on the ventral
surface of the head (Young eta!. 1989). During hatching, the combined effect of mantle movements
and the presence of Kolliker organs help the animal to move in one direction and exit the chorion
membrane (Naef 1923, Boletzky 1966, 1978-1979). This does not seem to be the sole function of
these organs. For captive-reared Octopus vulgaris, Kolliker organs have been recorded from hatch-
ling through to settlement, and on the distal portion of the arms in pre- and post-settlement para-
larvae, indicating the addition of new organs after hatching and during the entire planktonic phase
(Villanueva 1995) (Figure llF-H).
After hatching, the primary function of the Kolliker organs during the planktonic phase remains
unknown and many hypotheses have been proposed for these amazing structures. As Kolliker
organs in the expanded form can increase the body surface of the animal, it has ·been hypothesi zed
that they may help in some passive mode of planktonic transport (Naef 1923, Boletzky 1973); how-
ever this use seems doubtful in large planktonic animals due to the small size of the organs relative
to body size. Alternatively, due to the shining appearance of the everted fascicles in live individual s
ｯ｢ｳ･ｲｶｾ､＠ under a binocular microscope (R. Villanueva personal observation), it is possible that light
reflection could produce defensive counter-shading or crypsis in the water column. Kolliker organs
are transitory structures because there are no reports of their presence in subadult and adult benthic
octopuses and it is unknown how they are transformed and/or degenerate in the octopus skin after
settlement. Naef (1923) suggests that Kolliker organs form the basis for the formation of the juve-
nile and adult skin warts or skin papillae. Kolliker organs have been reported in subadult pelagic
octopods Bolitaena and Eledonella (Chun 1902 in Adam 1939), suggesting that these organs may
have a function related to a planktonic/pelagic lifestyle (see 'Permanent paralarvae: neoteny and
holopelagic octopuses', p. 182).
Integumental pores and glandular cells

Pores of different diameter have been observed on the epidermis of the arms, head, funnel and
mantle of hatchling paralarvae and these appear related to glandular cells (Young eta!. 1989, Lenz
et al. 1995). In laboratory-hatched individuals of Octopus cyanea, densities of these pores (5 flm
120
'"'t/!"",.:/" '""'iti'
ｾﾷ＠ﾷｾ＠Ｚｾﾷ＠ th ｾ＠ＧｾＡ＠
Figure 11 Ki:illiker organs in Octopus vulgaris throughout planktonic stage. Scanning electron microscope
images of individuals collected during rearing experiments described in Villanueva (1995). (A) Oral view of
19-day-old individual 3 mm mantle length (M L) measured fresh . Note the ' porcupine' aspect of the body due
to the emerged fascicles of the Ki:illiker organs on the skin. (B) Left ventrolateral view of 30-day-old indi-
vidual, 4.8 mm ML (fresh). Note the density of Ki:illiker organs on the mantle. The hole near the mantle margin
is due to handling using forceps. (C) Left lateral and (D) ventral views of 50-day-old individual, 7.3 mm ML
(fresh). Note the density of emerged Ki:illiker organs radiated on the ventral mantle, mantle margin, funnel
and near the eye" (E) Right lateral view of 50-day-old individual, 6.5 mm ML (fresh), showing Ki:illiker organs
near the tip of the fourth right arm (F), on the middle of third right arm (G) and a radiated fascicle near the
tip of the left third arm (H). Both individuals aged 50 days were in presettlement stage. All individuals were
killed following anaesthesia in 2% ethanol and lowered water temperature (3-4°C), then fixed in 5% buffered
formalin. Original"
121
Figure 12 Kolliker organs in Enteroctopus megalocyathus hatc hling paralarvae. Individuals collected dur-
ing rearing experiments described in Ortiz et al. (2006). Scanning electron microscope images from ventral
(A) and lateral (B) views. Note the density of Kolliker organs on the mantle, head and arms and the ventral
mantle. (C) Skin surface of the ventral mantle showing Kolliker organs and cilia (D) observed inside the rect-
angle. (E) Kolliker organs from ventral mantle in different degrees of expansion. (Specimens kindly provided
by N. Ortiz, Centro Nacional Patag6nico, CONICET.) Original.
in diameter) represented 10% of the skin surface for some areas but these high densities were not
observed in field-collected specimens (Young et al. 1989). The pores have small spheres in the aper-
tures that may be the secretory products of these potential mucus-secreting cells (Figure 14).
Sucker surfaces
In hatchling octopus paralarvae the main features of the outer surface of the suckers resemble
that of the adults (Nixon & Dilly 1977, Kier & Smith 1990). The infundibulum of the suckers has
numerous flattened pegs that are already endowed with minute pores (Figure 15) (Schmidtberg
1997, 1999). Pegs may provide friction to aid the suckers in attaining suction adhesion . However, as
observed in hatchlings of Octopus vulgaris (Schmidtberg 1999) and 0. cyanea (Young et al. 1989),
the infundibulum is encircled by a plain rim and lacks the circumferential marginal folds that sur-
round the infundibulum in suckers of adult individuals or hatchlings of direct benthic species such
as Eledone moschata (Schmidtberg 1997, 1999). These circumferential marginal folds may aid
formation of a tight seal (Nixon & Dilly 1977, Kier & Smith 2002), suggesting that the suction pro-
cess in hatchling octopus paralarvae is not as effective as in adults or hatchlings of directly benthic
species (Schmidtberg 1997, 1999).
Sculptural components
Adult benthic octopuses are renowned for their camouflage and background-matching abilities.
Beyond chromatic components, this disguise is aided by sculptural components: papillae (branched
122
Figure 13 Kolliker organ from the skin of Octopus sp. hatchling paralarvae. (A) Scanning electron micro-
scope image of a radiated fascicle showing the rodlets and three new fascicles (white arrows) beginning to
emerge. Scale 30 Jlm. (B) Longitudinal section of an emerged fascicle, transmission electron microscope
image. Scale 5 Jlm. Inset, section through a microvillus of the chaetoblast that inserts into the basal end of a
rod let. Inset scale 0.5 Jlm. (C) Diagram of an everted fascicle. C, chaetoblast; E, epidermal cell; L, lateral fol-
licular cell; M, obliquely striated muscle; R, rod let. (Reproduced with permission from Brocco et al. 1974.)
Figure 14 lntegumetal pores and glandular cells . Scanning electron microscope images of Octopus cyanea
hatchlings showing (left) the pores on the arm tips (scale 0.1 mm) and (right) the oral surface of the arm show-
ing the pores and the secretory spherules (scale 0.01 mm). (Reproduced with permission from Young et al.
1989.)
or unbranched), skin flaps and raised ridges (i.e., lateral mantle ridge) (Figure 16). In stark contrast
to benthonic hatchlings (Figures lD and 10) and adults, octopus paralarvae lack any evidence of
these components, even in the largest forms (Figure 4).
Loose skin film

In some species, an unpigmented, transparent, loose skin layer has been observed to cover the body
of the whole animal (Figure 17). Hatchlings of Enteroctopus megalocyathus observed under a bin-
ocular microsco·pe show a transparent skin film densely surrounded by Kolliker organs and cover-
ing the mantle, funnel, head, arms and eyes (Ortiz et al. 2006) (Figure 170). Observations using
scanning electron microscopy (SEM) do not reveal this layer, instead showing the direct surface of
the skin (Figures 12 and 23). This may be an artefact of the fixative process required for electron
123
Figure 15 Sucker structure of Octopus vulgaris hatchling paralarvae. (A) Sagittal section of the sucker,
stained with haematoxylin and eosin. Scanning electron microscope images showing the whole suckers (B)
and infundibulum (C). C, cuticle; i, infundibulum; P, peg or projection of cuticular process of infundibulum; R,
rim. (Reproduced with permission: (A) from Nixon & Mangold 1996, (B) and (C) from Schmidtberg 1997.)
Figure 16 (See also Colour Figure 16 in the insert.) Adult Octopus cyanea in camouflage display amongst
soft corals, Puerto Galera, Philippine lslands. (Photo: Gunther Deichmann.)
microscopy. The presence of a similar loose skin structure has also been reported for laboratory-
hatched E. dofieini by Green (1973, p. 39), noting that "The lateral sides of each arm were outlined
with a transparent web". Kubodera & Okutani (1981, p. 149) noted that wild paralarvae of the same
species had a "body all covered with gelatinous tissue which is more prominent in smaller speci-
mens". Kubodera (1991) also showed that this loose skin layer is not only related to the hatchling
stage but also present during paralarval growth (Figure 17B). In addition to the genus Enteroctopus,
124
Figure 17 Skin film in En.teroctopus. (A) Dorsal views of E. dojlein.i hatchling (scale I mm) and (B) a 14 mm
mantle length individual (scale 5 mm). (C) Lateral view, scale I mm. (D) Ventral view of newly hatched E.
megalocyathus after preservation in formaldehyde showing the skin film covering the whole animal (scale
2 mm). (Reproduced with permission: (A) from Green 1973, (B) from Kubodera & Okutani 1981, (C) from
Kubodera 1991, (D) from Ortiz et al. 2006.)
the loose skin film also seems to be present in Octopus bimaculatus from the eastern north Pacific
(from drawings of Hochberg et al. 1992; their Figure 257) and in the Macrotritopus defilippi species
complex from Hawaiian waters (Hochberg et al. 1992; their Figures 260 and 261). Diekmann et al.
(2002) drew this structure for Argonauta argo and for an undetermined species of Octopus sp. col-
lected in the subtropical eastern north Atlantic.
A parallel supradermal skin layer is also found in three families of oceanic squids: Octo-
poteuthidae, Cycloteuthidae and Bathyteuthidae (Voight et al. 1994). A number of other soft-bodied
pelagic cephalopods possess a gelatinous subdermal layer within the skin . These taxa include pelagic
octopods such as Amphitretus, Haliphron and the deep-sea cirrate octopods, and squids including
Mesonychoteuthis and Chiroteuthis (Mangold et al. 1989). The function of such a gelatinous layer
(supra- or subdermal) is unknown but it is possible that its gelatinous matrix is more buoyant than
seawater (as in scyphozoans) or contains buoyant ammonia solution. It is possible that such layers
are used to attain neutral buoyancy, potentially aiding passive paralarval dispersion. The bristles of
the Kolliker organs in octopus paralarvae may also play a role in anchoring the loose skin film to
the body surfaces. The microscopic structure of this loose skin fi lm in octopus paralarvae and its
relationship to the integument needs to be examined in detail and its characteristics described in
live animals. Live animals should be observed and killed under controlled conditions to avoid pos-
sible premortem stress and/or fixative artefacts that may influence the general skin attributes in the
preserved animal.
125
Sensory systems
Central nervous system
The nervous system of para larvae matches the general pattern described for adults (Young 1971 ,
Wells 1978) but it is comparatively larger by volume. The brain, penetrated by the oesophagus,
consists of two large components, the supra- and the suboesophageal masses, each subdivided into
brain lobes (Figure 18). The brain of Octopus vulgaris hatchlings has been estimated to weigh
0.2 mg (20% of the total body weight of the animal); addition of the eight brachial ganglia and
eyes results in the nervous system representing approximately one quarter of the paralarval fresh
weight (Packard & Albergoni 1970). The relative proportions of the lobes of the paralarval brain
are markedly different from those of juveniles or adults. In 0. vulgaris and Eledone cirrhosa these
differences have been related to morphological development and changes in mode of life (Frosch
1971, Marquis 1989, Nixon & Mangold 1996, 1998, Nixon & Young 2003). For example, at hatching
the buccal and basal lobes are larger than in juveniles, while the brachial lobes are smaller. Brachial
lobes, which represent 8% of the total volume of the brain , increase to 13% at settlement, coincid-
ing with the rapid growth of the arms and suckers and the development of the tactile sense that is
characteristic of the octopus's benthic life, reaching 18% in the adult (Nixon & Mangold 1996). The
reduced brachial lobe seems to be an attribute of octopod planktonic life because Amphioctopus
ocellatus, a species with direct benthic hatchlings, has a brachial lobe that represents 15% of the
brain volume at hatching (Yamazaki et al. 2002). In general terms, the sensory systems of octopus
paralarvae show adult-like characteristics, with the exception of the ' lateral line system', the pres-
ence of which has not been reported for adult octopods. The main sensory system components are
treated individually below.
Photo receptors
Eye photoreceptors The eyes of octopodid paralarvae are located laterally and directed slightly
forward. During the planktonic stage there is a relatively slight increase in eye diameter relative to
the head and mantle in reared Octopus vulgaris (Villanueva 1995). Adult octopuses are blind to
colour (Messenger 1977) and sensitive to polarized light (Moody & Parriss 1961, Shashar & Cronin
1996). These attributes can probably be extended to paralarvae but no experimentation has been
done in this respect. Eye receptors of young octopus have been described for spec ies with benthic
hatchlings, including 0 . australis and 0. pallidus (Wentworth & Muntz 1992), showing that by the
time of hatching all relevant components of the visual system are recognizable in their essentially
adult form (see reviews by Budelmann et al. 1997, Nixon & Young 2003). However, further dif-
ferentiation and growth takes place. There is little information on the vision of planktonic octo-
puses. Unpublished observations (A. Bozzano, Institut de Ciencies del Mar) showed that the eyes of
Figure 18 Sagittal section of hatc hling Octopus vulgaris. DG, digestive gland; F, funnel; S, sucker; SM,
supraoesophageal mass; ST, statocyst. (Reproduced with permission from Nixon & Mangold 1996, modified.)
126
BIOLOGY OF THE PLANKTONIC STAGES OF BENTHfC OCTOPUSES
Figure 19 Transversal section of the eye of Octopus vulgaris hatchling, stained with toluidine blue. BM,
basal membrane; I, iris; L, lens; LB, lentigenetic body; P, photoreceptors; PL, plexiform layer; PN, photo-
receptor nuclei; SN, supporting cell nuclei . Photo courtesy of Anna Bozzano.
Octopus vulgaris are also completely formed at hatching and the retina already shows all the adult
differentiated retinal layers (Figure 19). In the hatchling eye, it is possible to distinguish the iris and
the lentigenic body as well as the fully developed lens. The photosensitive retina consists only of
rod-like photoreceptors and supporting cells. A basement membrane separates the supporting cell
nuclei from the photoreceptor nuclei. The plexiform layer, posterior to the photoreceptor nuclei, con-
tains the synaptic processes of the photoreceptors and the efferent fibres from the brain lobes. These
structures contribute to the formation of the optic nerve collecting fibres at the back of the eye.
Photosensitive vesicles In addition to the normal retinal photoreceptors of the eyes, most cephalo-
pods have small groups of photoreceptors located external to the eyes; these have been termed
the extraocular photoreceptors or photosensitive vesicles (Mauro 1977). In adult stages of benthic
and pelagic octopods the photosensitive vesicles consist of a single pair of organs located inside
the mantle cavity (Nishioka et al. 1962, Young 1978). Each organ is a spherical vesicle attached to
the posterior margin of each stellate ganglion , recognizable as an orange spot in Eledone cirrhosa
(Cobb et al. 1995a,b) and colourless in Octopus vulgaris (Mauro 1977). The presence of photosensi-
tive vesicles has been recorded in developed embryos of 0 . vulgaris (Marquis 1989) but their devel-
opment throughout planktonic life is unknown. The function of these vesicles remains enigmatic
in benthic octopods although it seems to be related to regulation of circadian activity (Cobb et al.
1995a,b, Cobb & Williamson 1998, 1999).
Mechanoreceptors
Stato cysts and statoliths The two sphere-like, membranous statocysts are situated in cavities of
the cranial cartilage. They consist of fluid-filled spaces each containing a mineralized statolith
borne on receptor hairs. Their mechanoreceptors respond to mechanical stress caused by a relative
movement between receptor hair cells, the statoliths and the surrounding medium (Budelmann et al.
1997). The octopod statocyst has been the subject of detailed research in adult individuals (Young
1960, Budelmann et al. 1973, Budelmann 1977, Budelmann & Young 1984, Budelmann et al. 1987).
Statocysts in 0. vulgaris hatchlings are relatively large and their anterior-posterior length represents
32% of ML in fixed specimens, then decreasing to ll% of ML after settlement (Nixon & Mangold
1996) (Figure 18). Octopus vulgaris hatchling statocysts were analysed histologically by Biillow &
127
Figure 20 Statoliths of Octopus vulgaris paralarvae. Scanning electron microscopic images from antero-
lateral (A) and posterior (C) views of hatchling statoliths with their respective crystalline surface structure
presented inside the rectangles (B, D). In paralarvae aged 30 days, statolith growth is observed on the pos-
terior side of the statol ith (E, F). The crystalline structure of the surface observed inside the lower (G) and
upper (H ) rectangle of the image F is also indicated. Individuals obtained from rearing experiments described
in Villanueva et al. (2004). Original.
Fioroni (1989) indicating that, in comparison with the adult statocysts, the cartilaginous capsules
lack the detached epithelium that probably lies within the cartilaginous layer. The crista statica is
divided into three parts and the anticristae are absent. Colmers et al. ( 1984) describe neuroepithelial
structures of the statocyst and statoliths of species with benthic hatchlings in 0. maya and 0. sp.
(reported as 0. joubini). The statol iths of 0. vulgaris hatch Ii ngs (Figure 20A-D) have a hem ispheri-
cal shape that corresponds to the knob present on the peak of the limpet-shaped statoliths of adult
individuals of Octopodidae, as observed in 0. vulgaris (Young 1960, Sakaguchi 2006), Eledone
cirrhosa (Clarke 1978), Enteroctopus magnificus (V ill anueva et al. 1991) and E. dojleini (Ikeda
et al. 1999). The hatchling or natal statolith can be recognized externally on the adult statolith as
its size is nearly constant and is independent of the sizes of the adult body or statolith (Sakaguchi
2006). After hatching, statolith growth takes place on the posterior side of the statolith, as observed
in laboratory-reared 0. vulgaris paralarvae aged 1 month (Figure 20E-H).
'Lateral line system' Ciliated primary sensory hair cells, sensitive to local water movements, are
arranged in epidermal lines located on the arms, head, anterior part of the dorsal mantle and fun-
nel in 0. vulgaris hatchlings (Lenz et al. 1995, Lenz 1997). The epidermal line runs in an anterio-
posterior direction. The dorsal, dorsolateral , ventrolateral and ventral lines are paired, occurring on
128
Figure 21 Epidermal lines in Octopus vulgaris hatchling paralarvae. (A) schematic drawings showing the
course of the epide rmal lines (ind icated by dotted lines) from dorsal (left), ventrolateral (central) and ventral
(r ight) views. DL, dorsal line; DLL, dorsolateral line; FL, funnel line; VL, ventral line; YLL, ventrolateral
line. (B) Scanning electron microscope (SEM) image from the lateral view of the head showing the dorsal,
dorsolateral and ventral lines. DA, dorsal arm; DLA, dorsolateral arm; VLA, ventrolateral arm. (C) SEM
image of the funnel line showing the ciliated cells of the funnel line (black arrow) and the ciliated cells
in the immediate neighbourhood of the line (w hite arrow). (Reproduced with permission from Lenz 1997,
modified.)
both sides of the head and on the left and right arms but there is only one line along the midline of
the funnel (Figure 2LA,B). The ciliated cells of these lines have an elongated apical surface bear-
ing up to six long (l0-11m) cilia and short microvilli. The dorsal lines are the longest. The funnel
line has the most complex structure, composed of two parallel rows of ciliated cells and several
smaller, accessory non-ciliated cells with long microvilli in the centre of the line (Figure 2LC). The
epidermal lines found in octopus paralarvae have not been reported in adult octopuses but they
129
are homologous to those described in adults of sepioid and teuthoid cephalopods. The cells of the
epidermal lines are able to perceive hydrodynamic pressure and neurophysiological experiments in
adult decapod cephalopods showed that epidermal lines can be considered as an organ analogous
to the lateral line system found in fishes (Budelmann & Bleckmann 1988, Bleckmann et a l. 1991 ,
Budelmann et al. 1997).
Single ciliated cells and group-arranged ciliated cells In addition to the ciliated cells of the epi-
dermal lines, hatchling 0. vulgaris have ciliated cells on the epidermis that are randomly scattered
over the body surface of arms, suckers, head, funnel and mantle or are in special arrangements
on the funnel, external yolk sac and the olfactory organ (Lenz et al. 1995, Lenz 1997, Wildenburg
1997, see 'Chemoreceptors' below). During the embryonic stage, the cilia help during rotation of
the embryo (Boletzky & Fioroni 1990), presumably keeping the chorionic fluid in motion and pre-
venting the embryo from sticking to the chorion after rotation has occurred. After hatching their
function is unknown. Body surfaces that lack cilia are the growing tips of the arms, cornea, margin
of the eyes, funnel aperture and the inner side of the mantle.
Sucker mechanoreceptors A variety of presumed mechanoreceptors has been described on the

suckers of adult octopuses (Graziadei 1964, Graziadei & Gagne 1976a,b) and their presence in the
para1arval suckers can be expected. However, Schmidtberg (1999), after studying the hatchling suck-
ers of 0. vulgaris, concluded that the ciliated cells present on the suckers are chemosensory recep-
tors rather than mechanoreceptors. The development of sucker mechanoreceptors during paralarval
and juvenile growth and its relation to a planktonic or benthic mode of life need to be examined.
Chemoreceptors
Olfactory organ In 0 . vulgaris hatchlings, paired oval-shaped olfactory organs are situated on
either side of the head, ventrally behind the eye and near the mantle edge (Figure 22). They measure
around 35-45 J.lm in length (Lenz 1997, Wildenburg 1997). In this species the surface of the organ
is covered by a brushborder of microvilli and cilia. It is composed of one epithelial cell type, four
sensory morphological cell types with a chemosensory function and a fifth , mechanosensitive mor-
phological cell type, suggesting the olfactory organ has both chemical and mechanosensitive func-
tions in planktonic 0. vulgaris (Woodhams & Messenger 1974, Wildenburg 1997). In Enteroctopus
megalocyathus the organ is larger (Figure 23). In hatchlings of directly benthic octopuses such as
Octopus joubini, the olfactory organ resembles that of the adults except in size, and the receptors are
smaller (Emery 1976). Electrophysiological and behavioural analyses of the receptor cells from the
olfactory organ in adult loliginid squid have proved their chemoreceptor function (Gilly & Lucero
1992, Lucero et al. 1992, Lucero et al. 2000). The same function can be expected in octopuses.
Lip chemoreceptors Ciliated receptors and sensory cells have been described on the finger-like
papillae that distally fold the muscular lip around the beaks in 0 . joubini (Emery 1975). These
receptor cells seem more developed in octopuses than in cuttlefish or squid; their presence in octo-
pus paralarvae has not been assessed.
Sucker chemoreceptors In hatchlings of 0. vulgaris, primary ciliated, flask-shaped receptor cells

of presumed chemoreception function are common on the rim but rare at the lateral regions of
the suckers and absent on the epithelium of the infundibulum (Schmidtberg 1997, 1999). These
chemoreceptor cells seem to correspond with those previously described on the epithelium of the
rim sucker of adult octopuses (Graziadei 1962, 1964, 1965, 1971 , Graziade i & Gagne 1976b).
130
Figure 22 Olfactory organ in Octopus vulgaris hatchling paralarvae. Scanning electron microscopic
images showing (A) the position (arrow) of the olfactory organ and (B) the cilia (arrow) on the organ surface.
Transmission electron microscope images showing (C) sensory cells of morphological type I with an apical
cilia pocket and cell morphological type 2 with a spacious ciliated cavity, and (D) sensory cell of morphologi-
cal type 5, cell apex with one kinocilium and microvilli (di, dictyosome). Scale bar 2 Jlm. (Reproduced with
permission from Wildenburg 1997, modified .)
Digestive system
Buccal mass
The buccal mass consists of the two jaws of the beak, a radula, salivary papillae and associated
musculature. At hatching, the buccal mass is fully formed and functional (Nixon & Mangold 1996).
The upper and lower beaks are transparent and have oral denticles (Figures 24 and 25). These den-
tides are absent in adult octopuses, which have smooth and darkly pigmented beaks. Oral denticles
have been described in hatchlings of Octopus vulgaris (Boletzky 1971, Nixon & Mangold 1996,
Nixon & Young 2003), 0. mimus (Castro-Fuentes et al. 2002), Eledone cirrhosa (Boletzky 1974),
as well as in the juvenile stages of the pelagic octopods Argonauta argo and Tremo ctopus violaceus
(Boletzky 1971) and ctenoglossans (Strugne ll et al. 2005). See p. 148 for functioning of the buccal
mass components.
Digestive tract
The digestive tract of octopus paralarvae is functional at birth and feeding commences rapidly
after hatching (Villanueva et al. 2002, Morote et al. 2005, Iglesias et al. 2006). The external yolk
sac that is evident within the egg capsule is sometimes visible externally in the earliest hatchling
stages, indicating premature hatching (Figure 26). The white of the yolk sac is also visible within
131
Figure 23 Olfactory organ in Enteroctopus megalocyathus hatchling pa ralarvae. Specimen collected during
rea ring experiments described in Ortiz et al. (2006). Scanning electron microscope images showing the posi-
ti o n (left) and the organ (right). Note the la rge size of the orga n in comparison with Octopus vulgaris hatc hling
(Fig ure 22). (Specimen kindly provided by N. Ortiz, Centro Nacional Patag6nico, CONICET.) Origina l.
·. ..
Figure 24 Bucca l mass and denti culati o n o n the bea ks of Octopus vulgaris. Left, whole mount of a hatch-
ling individual. Ri ght, oral surface of the ros trum of the upper (top) and lower (bo tt om) beaks showing den-
ticulation in 1-day-old specimen. D, denticles; LB, lower beak; UB , upper beak. (Left, modified from Nixon
& Mangold 1996; right , from Bolet zky 1971 a nd reproduced with permission.)
the visceral mass in these early hatchling stages (Figure 26). The yolk sac is rapidly devoured or
discarded after hatching (see p. 135) and its presence internally does not hamper direct feeding
because the digestive tract is immediately capable of ingesting prey (Boletzky 1975).
132
Figure 25 Denticulation of beaks in Octopus vulgaris paralarvae. Scanning electron microscope images
of (A) oral view of hatchling; (B) 50-day-old specimen in presettlement stage, 7.3 mm mantle length (ML)
(fresh) a nd (C) 60-day-old recently settled individual of 9.3 mm ML (fresh). Note the broken denticles on the
lower beaks of posthatching individu als and the rostral tip of the beak in the settled individual, in transition
to the typical adult beak form. Individuals obtained from rearing experiments described in Villanueva (1995 ).
Original.
Ink sac
For those species that possess an ink sac in the adult form, the ink sac of their paralarvae is func-
tional from birth (Yamashita 1974, Gabe 1975, loll 1978, Okubo 1979, Kaneko et al. 2006). The
positions of this and other organs of the digestive tract are shown in Figure 27. The organ is visible
through the body wall in those taxa that lack a reflective iridophore membrane surrounding the
viscera (Figure 26).
133
Figure 26 (See also Colour Figure 26 in the insert.) Planktonic paralarva of Octopus warringa within
10 min of hatching in the laboratory showing short arms, transparent musculature, simple chromatophores
and external yolk sac (within arm crown). (Photo: David Paul.)
A B c
Figure 27 Scaeurgus unicirrhus hatchling after fixation. (A) Lateral view. (B) Dorsal view. (C) Ventral view
after removal of the ventral mantle musculature. bh, branchial heart; cv, cephalic vein lying beside the intes-
tine; fr, funnel retractor; g, gill; is, ink sac; oo, olfactory organ; r, rectum; sg, stellate ganglion. (Reproduced
with permission from Boletzky 1984, modified .)
Food, feeding and nutritional requirements

Yolk reserves
After hatching, octopus paralarvae possess available yolk reserves that help the animal during
the first hours or days, combining endogenous (yolk) with exogenous (prey) feeding until the yolk
is completely absorbed (Boletzky 1975, 1989). In octopods, part of the yolk is enclosed within
the hatchling proper and the rest forms an external sac enclosed within a membranous envelope
134
(Figure 26). The yolk can be considered as a unit independent from the digestive system: the para-
larvae absorb the yolk directly into the blood as the yolk nutrients flow to the circulatory system,
not via the alimentary canal (Boletzky 1975). The amount of yolk in hatchling individuals varies
greatly. The reduced volume or absence of the external yolk sac at hatching can be considered
a sign of health or competence of the animal, indicating that these reserves have been correctly
absorbed. In contrast, a large external sac indicates premature hatching (Boletzky & Hanlon 1983,
Boletzky 1987) and a quick loss/discarding of this external sac reduces the survival rate of the
hatchlings (Okubo 1979). Observations under experimental conditions show that well-developed,
non-premature hatched Octopus vulgaris paralarvae start to feed during the first 24 h after hatching
(Villanueva et al. 2002, Morote et al. 2005, Iglesias et al. 2006) and that the presence of an inner
yolk sac does not apparently interfere with any organ functioning (Boletzky 1975).
The amount of yolk is proportional to body weight and the yolk absorption is related to tem-
perature in squid paralarvae (O'Dor et al. 1986, Vidal et al. 2002, 2005). The same relationship can
also be expected for octopus paralarvae. Large octopus hatchlings from species adapted to low tem-
peratures, such as Enteroctopus megalocyathus, can survive under starved conditions up to 15 days
at II.SOC (Ortiz et al. 2006), while species with small hatchlings, such as Octopus cf tetricus, can
survive up to 10 days at 20°C (loll 1978 as 0. tetricus). Under the same temperature conditions,
starved 0. vulgaris hatchlings lose 16% and 28% of their dry weight after 2 and 4 days, respectively
(Villanueva et al. 2004). In 0. vulgaris, the maternal diet before spawning (crab or sardine diet)
influences the lipid composition of the eggs and hatchlings and has been related to paralarval sur-
vival under starvation conditions. Starved paralarvae fed a maternal sardine diet had low survival
rates and low lipid content, particularly for phosphatidylcholine and phosphatidylethanolamine as
well as low content in n-3 and n-6 polyunsaturated fatty acids (PUFAs) (Quintana et al. 2005,
2006). Table 3 shows survival of different paralarval species after hatching in the laboratory; some
of these results are the product of unsuccessful feeding experiments for which the short survival
period suggests that metabolic fuel was provided mostly by the yolk and whole animal reserves. The
physiological conditions that enable the first digestion of external prey have not been determined for
octopus paralarvae and need further research .
Natural prey
At the moment of prey capture, octopus paralarvae bite and administer salivary products using their
beaks and radula. The saliva contains enzymes that predigest the prey, enabling easy removal of the
flesh from exo- or endoskeletons. The beak and radula are then used to macerate the predigested
flesh, sucking up the edible content of prey such as crustaceans and rejecting their exoskeletons
(Hernandez-Garcia et al. 2000). They sometimes also ingest small pieces of prey carapace (fglesias
et al. 2006) (see p. 148). This mode of ingestion makes the study of stomach contents difficult. As
a result, there are few reports on the diet of octopus paralarvae in the wild. Passarella & Hopkins
(1991) examined stomach contents of 57 paralarvae (<20 mm ML) of Octopodidae (Macrotritopus
defilippi, Octopus sp. and Scaeurgus unicirrhus) collected from eastern Gulf of Mexico at depths
between 0 and 900 m and found that the major prey types were euphausiids (53% of the stomachs)
and non-cephalopod molluscs (23%), as well as ostracods, hyperiid amphipods, decapod crusta-
ceans and fishes. Octopus paralarvae share a preference for crustacean prey with squid paralarvae
(Passarella & Hopkins 1991, Vecchione 1991, Vidal & Haimovici 1998), in common with most
juvenile cephalopods (Nixon 1987).
A wide variety of live and inert prey has been consumed by octopus paralarvae in laboratory
experiments (Table 3). Most of the successful or long-term laboratory rearings used decapod crus-
tacean zoeae (Figure 28) as the primary prey for small-sized octopus paralarvae (Octopus vulgaris
type) (ltami et al. 1963, Forsythe & Toll 1991 , Villanueva 1994, 1995, Shiraki 1997, Carrasco et al.
135
Table 3 Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from hatching to
settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
Temp. Reared to Geographic
Species and prey offered (oC) Survival rate(%) settlement Comments area Reference
Amphioctopus burryi
Live wild zooplankton (copepods , larval 23- 24 To 16% at 26 d No No growth in ML NW Atlantic Forsythe &
crustaceans and fishes) and Anemia Hanl o n 1985 ;;o
nauplii 0
0
Calliswcropus macropus m
;;o
Hatchling zoeae of Pagurus prideaux 16 To 6 d No Without food survived 3-4 d Mediterranean Boletzky et al.
Enteroctopus dojleini
2001
-< r
r
)>
Anemia , frozen Calanus, frozen and li ve Np To 7 d No Eating not observed NE Pacific Green 1973 z
zooplankton c
m
Pieces (2-5 mm) of prawns (Pa/aemon
ｾ＠
I0.6-- 1 1.8, To 26d No Food pieces submerged NW Pacific Okubo 1973
w pacijicus), c lam (Ruditapes mean previously in freshwater to
0\
?:=>
philippinarum ) and crab 11.0 increase floatabilit y
ｾ＠
Live mysidaceans, amphipods and pieces Np 4% at 135d Presettlement Individuals reached 33 mm TL NW Pacific Okubo 1974 )>
of shrimp after 70 d at liS d ;;o
;:;-:::
Artemia and hatchlings of green ling fish 8.5- 15.6, To 19d No Feeding and development not NW Pacific Yamashita 1974
ｾ＠
mean observed
11.8
z
0
;;o
Crushed egg yolk, grou nd shrimp and 10-12.8 Np No Only adu lt Arremia and fry NE Pacific Gabe 1975
ｾ＠
mussel , live gammarids, Anemia biomass fish accepted as prey; )>
and fry of fi sh Hemi/epidotus occasionally dead siblings z
hemilepidotus captured by the paralarvae
Mysidaceans (5-I 5 mm) during first 7.8- 14.7, To 169 d Settlement Individuals reached 35 mm TL NW Pacific Okubo 1979
feeding and pieces of shrimp (Palaemon mean from at 169 d
pacijicus) after 70 d 10.8 100-117d
From hatching to 50 d: dead Np 8% at 6 month s Settlement Tank with upwelling water NW Pacific Okubo 1980
mysidaceans + amphipods ; 50- 80 d : from 88 d system
dead mysidaceans + arnph ipod s + pieces
of shrimp ; from 80 d: pieces of shrimp
Anemia biomass , frozen krill (Euphausia 10 With Anemia: 50% SR at No The preferred prey was krill; NE Pacific Marliave 1981
pacifica), larval cottid fish (Hemilepidorus 5 d and maximum to 22 d; neustonic feeding behaviour
hemi/epidorus), trout micropellet s with krill: 50% SR at 16 d described
and maximum to 87 d
Frozen or fresh chopped body and muscle 11 - 11.5 4% after 6- 7 months Settlement Hatchling food size equivalent NE Pacific Snyder 1986a,b, co
of crabs Cancer producrus, Pugerria from 5 to to octopus head width; unpublished
0
r
producrus, tails of Panda/us danae 6 months developed paralarvae feed on manuscript 0
0
shrimps, Euphausia pacifica, beef heart chunks of food 3- 6 x 25 mm .-<
and lamb kidney suspended in the tank 0
'T1
Enrerocropus megalocyarhus ....,
Starved 11.5 To 15 d No SW Atlantic Ortiz et al. 2006 :c
rn
Hapalochlaena lwwlara '"0
Anemia and small crustaceans 26 To 7 d No Slight paralarval growth CentralE Overath & r
)>
Pacific Boletzky 1974 z
;;-::
Ma crocropus maorwn ....,
Starved Np To 8 d No SW Pacific Batham 1957 0
z
w
Ocropus bimacularus
Arremia and wild plankton Np To6d No NE Pacific Ambrose 1981
n
CIJ
ｾ＠
-.J
Ocropus cyanea
Crab and mysis zoeae, copepods Promysis Np To21 d No Growth increase in 0.5 mm Hawaii Van Heukelem 0
rn
CIJ
orienwlis and Lucifer sp. TL; unfed controls died in 5 d Islands 1973
Ocr opus joubini
0
'T1
Wild live zooplankton, zoea of penaeid 24 To 10% at 7 d and 0.2% at Settlement Addition of vitamin NW Atlantic Forsythe & Toll co
rn
shrimp, mysidacean shrimp 23 d from 21 d supplement mixture to the 1991 z
....,
rearing tanks
:c
Ocropus laqueus n
Arremia nauplii , copepods and pieces of 26 To 7 d No Only feeding on pieces of NW Pacific Kaneko et al. 0
(")
shrimp shrimp was observed 2006 ....,
Ocropus mimus 0
'"0
Arremia metanauplii , zoeae of <22 To 31 d No Best results with zoeae as food SE Pacific Zuniga et al. c::
CIJ
Leprograpsus variegarus and Cancer and octopus density of 25 ind 1997 rn
CIJ
serosus, and rotifers J-1
Hatchling zoeae of Pagurus sp. and Cancer Np To 12 d No SE Pacific Warnke 1999
serosus
(conrinued onnexr page)
Table 3 (contin ued) Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from
hatching to settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
Species and prey offered (OC) Survival rate(%) settl ement Comments area Reference
ArTemia nauplii 21 -22 10% at 5 d, maximum No SE Pacific Baltazar et al.
survival to 17 d 2000
Arremia, Brach ion us, zoeae of Cancer 17- 23 To 23 d No SE Pacific Montoya 2002
seTosus, 1-IepaTus chiliensis, EmeriTa
ano/oga and Pleuroncodes monodon and ;:o
micropellets 0
0
OcTopus TeTricus rn
;:o
Copepods, Arremia , small pieces of fi sh
and mollusca
OcTopus cf TeTricus
To 32 To6d No All food refused SW Pacific Dew 1959 (as
0 . cyaneo) -rr<
;I>
Anemia and rice powder Np To 21 d No No growth, no evidence of E Indi an l oll 1976 z
eatin g c
rn
w
OcTopus vulgaris
ｾ＠
00 ArgmwuTa argo hatchlings Np To 12 d No Mediterranean Naef 1928 Ro
Harpacticoid copepods. ArTemio. ci li ates , 23 To 9 d No No feeding observed NEAtlantic Vevers 196 1 ｾ＠
yeast cells ;I>
;:o
Palaemon serrifer decapod palaemonid Mean 9% at settlement Settlement P serrifer zoeae feed with NW Pacific ltami et al.
zoeae 24.7 from 33 d ArTemia nauplii 1963 ""
p
Zoeae of crabs and prawn s, Arremio Np To 35 d No Growth ceased from 25 d Mediterranean Mangold & z
biomass Boletzky 1973 0
;:o
Anemia biomass 25.1 To 67 % at 22 d Transition to Microalgae Nannocloropsis NW Pacific Imamura 1990 ｾ＠
benthic added to the culture tank ;I>
stage
z
Anemia biomass 25- 28 30% at 25 d Transiti on to Tank volume of 20 m3 and NW Pacific Hamazaki et al.
benthic microalgae Nannoc/oropsis 199 1
stage added to the tank
Liocarcinus depuraTor and Pagurus 21.2 9% to settlement at 4 7 d Settlement Food added 5 times per day Mediterranean Villanueva
prideoux decapod crab zoeae from 47 d 1994, 1995
Anemia and Porrunus TriTuberculmus crab Np 30% at 29d Presettlement Indi viduals with 19 suckers at NW Pacific Shiraki 1997
zoeae 29 d
Artemia biomass ( 1- 2.7 mm) feed with or 21. 24 and To 88 % at 24 d No Hi gher growth and surviva l NW Pacific Hamasaki &
wi thout Nwuwchloropsis algae o n the 27 with 100-400 x lo-' algal Takeuchi 2000
rearing tank cells/ml
Rotifers, fi sh eggs, micropellet s, wi ld 18- 20 To 32 d No Best survi val with Artemia NEAtlantic Iglesias et al.
copepods, Artemia nauplii and OJ
metanauplii 2000
metanauplii , zoeae of shrimp Pa/aemon
0
r
serratus , zoeae of crab Carcinus nwenas 0
0
and Necora puber --<
Artemia bi omass ( 1- 3 mm) and pe ll ets 20-22.5 To 6.7% at 30 d No Fatty ac id of cultured oc topus Mediterranean Navarro & 0
'Tl
(250-500 f!m ) with 6% moisture reflected that of the food Villanueva ,...,
2000 ::r:
tTl
Na nn och/oropsis algae on the rearing tank 25 To 45 % and 24% at 16 and No Enriched Artemia increased NW Pacific Hamasak i & '"0
at 100 x lo-' cells/m l; Artemia biomass 20 d , respectively survival and growth Take uchi 2001 r
)>
(2 mm) not enriched or enriched with z
yeast or shark egg powder r;
,...,
A rtemia biomass ( 1.5- 2 mm) feed with 17-29 To 62 .5% at 40 d No Hi ghest survival at 2 1°C NW Pacific Hamasak i & 0
z
w
Nwmoch/oropsis algae
Ocwpus vulgaris
Mori oka 2002
n
(/)
\0
Artemia biomass and zoeae of Maja Np To 56 d No Tank volume of 9m 3 and NEAtlantic Moxica et al. ｾ＠
squinado microalgae /socluysis, 2002 0
tTl
Tetraselmis and Clwetoceros (/)
Anemia nauplii and millicapsules of 19.4-22.5 To 4.6 % at 30 d No Total proteolytic activity Medi terranean Vill anueva et al. 0
'Tl
1.3- 2 mm in 0, 0.3 mg fre sh weight correlated with paralarval 2002 OJ
weight tTl
z
,...,
Live and frozen Maja brachydacryla zoeae 2 1.1 -22.2 3.4% at 60 d Settlement Parabolic tanks with upwelling NEAtlantic Carrasco et al.
::r:
1-3 d old and Artemia bi omass
Maja brachydacryla zoeae and Artemia 22.5 3 1.5% at 40 d
from 52 d
Settlement
water system
Microalgae (Chlorel/a sp., NEAtlantic
2003 , 2006
Iglesias et al.
n
0
biomass (1-4 mm) from 40 d /sochrysis ga/bana and 2004 n,...,
Chaetoceros sp.) added daily 0
'"0
to the culture tank c:
(/)
(continued on next page) tTl
(/)
Table 3 (continued) Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from
hatching to settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
Species and prey offered ("C) Survival rate (%) sett lement Comments area Reference
Artemia nauplii and essential amino acids 19.2-2 1.1 To 12.5% at 30 d No Best survival in trials receiving Mediterranean Villanueva et al.
added to the rearing tank amino acids 2004,
Villanueva &
Bustamante
2006 ;;o
0
Anemia metanauplii and zoeae of Maja 20± I To 26 d No Better growth and survival CentralE Fernandez- 0
squinado with light intensity of Atlantic Lopez et al. tTl
;;o
6000 lux 2005 <
Artemia metanauplii , cladocera ns Moina 21 - 22 To IOd No Protease activity indicates NEAtlantic Morote et al. r
salina, zoeae of Maja brachydactyla and hatchling condition 2005
r
;I>
Palaemon serratus, eggs and larvae of fish z
Solea senegalensis, artificial pellets c:::
tTl
Artemia nauplii and thawed frozen fish 21.2-24.8 To 45.9% at 32 d Transition to Fish flakes effective for NW Pacific Okumura et al. <
;I>
"""
0 (Ammodytes persona/us) flakes benthic improving the DHA content 2005a p,o
stage of the paralarvae
3:
Artemia biomass of 0.8 and 1.4 mm 18-20 3d No Preference for Artemia 1.4 111111 NEAtlantic Iglesias et al. ;I>
;;o
at densities of 0.1 Artemia 2006 ;;>::
mi -I
ｾ＠
Artemia nauplii and defrozen fish 24-26.9 To 10% at 42 d Tran sition to Fish flakes improved DHA NW Pacific Kurihara et al. z
(A mmodytes personatus) flakes benthic content of the para larvae 2006 0
;;o
stage 3:
Octopus vulgaris ;I>
Artemia metanauplii , Grapsus grapsus and Np To 27 % at 28 d No Best survival and growth with NEAtlantic Iglesias et al.
z
Plagusia depressa zoeae G. grapsus zoeae 2007
Artemia nauplii supplemented with 20± I To 39% at 40 d No Best survival with A. wnsa up SE Atlantic Iglesias et al.
copepods (Acartia tonsa). juvenile mys ids to 15 d supplemented with 2007
(Metamysidopsis elongata atlantica) and Artemia
crab zoeae (Ca llinectes sapidus)
Artemia 0.8 mm 20 2d No Prey capture higher during NEAtlantic Marquez et al.
light periods, decreasing in 2007
the dark
Robsonella jimtanianus
Artemia, small crustaceans and 10-16 To34 d Np SE Pacific Gon za lez et a l.
micropellets 2006
Scaeurgus unicirrhus
to
Artemia biomass 19 To6 d No Mediterranean Bolet zky 1984
Wunderpus plwtogenicus
0
r
Artemia naupli , rotifers Brachionus and 26 To4 d No SW Pacific Mi ske &
0
0
copepods Kirchhauser .-<
2006 0
'Tl
Note: DHA , docosahexanoic acid; ML, mantle length; Np , not provided; SR, survival rate; TL, total length. -l
::r::
tn
'"0
r
)>
z
;;>'::
-l
0
z
n
C/J
"'"
ｾ＠
tn
C/J
0
'Tl
to
tn
z
-l
::r::
n
0
(")
-l
0
'"0
C/J
c:::
tn
C/J
Figure 28 Decapod crab zoeae hatchlings used as live prey in successful rearing experiments of Octopus
vulgaris paralarvae. Left to right: Liocarcinus depurator, 0.5 mm carapace length (CL); Pagurus prideaux,
1.2 mm CL (photos: R. Villanueva); Maja brachydactyla, 1.1 mm CL (photo courtesy of Guiomar Rotllant).
2003, 2006, Iglesias et al. 2004) or mysidaceans, amphipods and euphausiids for larger-size para-
larvae (Enteroctopus type) (Okubo 1979, 1980, Marliave 1981). Preference for these prey types
correlates with the few available field observations. Itami (1975) found that during the hatching
season of Octopus vulgaris in the Akashi Straits, Japan, the presence of paralarvae collected in
plankton nets 1-2m above the seafloor in coastal waters was associated with areas rich in shrimp
and crab zoeae and megalopa. After copepods, decapod crustacean zoeae are the most abundant
crustacean group in the meso- and macroplankton (size >1 mm) on the continental shelf of the
north-west Mediterranean Sea over summer (Razouls & Thiriot 1968), coinciding with the peak
hatching season for 0. vulgaris in that area (Mangold 1983, Villanueva 1995). Decapod crustacean
larvae are probably one of the main natural prey of planktonic 0 . vulgaris and other species of lit-
toral octopuses although stomach analyses from wild paralarvae need to be examined. In contrast,
the ability of planktonic octopuses to feed on inert food , as observed under laboratory conditions
(seep. 146), suggests that scavenging activity in the wild is also possible. Immunoassay techniques
used to analyse stomach contents of squid para larvae (Venter eta!. 1999, Hoving et al. 2005) may be
useful tools for gaining better insights into the earliest feeding stages of octopus para larvae.
Prey size and prey density

In comparison with most carnivorous larval fishes, for which mouth opening diameter limits the size
of the prey that are generally ingested whole, planktonic octopuses can capture prey of their own
size using their well-developed arms and suckers. Prey size and prey density preferences of plank-
tonic octopus have been determined only under experimental conditions. Artemia of 1.1-1.7 mm
(Imamura 1990) or 1.5-2 mm length (Hamazaki et al. 1991) have been recommended for reari ng
Octopus vulgaris hatchlings (3 mm total length). Iglesias et al. (2006) also fed hatchlings of the
same species with both small (0.8 mm) and large ( 1.4 mm) Artemia, recording preference (77%)
for large Artemia that represented nearly 50% of the total length of the octopus. Octopus vulgaris
hatchlings capture a range of live decapod crustacean zoeae, including Liocarcinus depurator,
Palaemon serrifer, Pagurus prideaux and Maja brachydactyla (1.3, 2.5, 3.1 and 3.4 mm in total
length, respectively), representing 45-118% of octopus total length and 2-32% of octopus fresh
weight at hatching (Figure 29). Laboratory experiments using these prey obtained high growth and
survival rates during the first half of planktonic life, suggesting the suitability of this range of prey
sizes (Itami et al. 1963, Villanueva 1995, Carrasco et al. 2003, 2006, Iglesias et al. 2004).
142
14{) 35
....l 120 ｾ＠ 30
I-< I-<
"'::lD. 100 "'::lD. 25
B
u
B
u
.....00 80 0 20
'0
*"'"' 60 *"'"' 15
ｾ＠
....l
I-< 4{) 10
>- I-<
01 >-
0:: 20 01
0:: 5
0
0 5 10 15 20 10 100 1000
Octopus TL (mm) Octopus TW (mg)
Figure 29 Predator-prey size relationships in Octopus vulgaris during the paralarval stage expressed as
length (left) and fresh weight (right). Octopus data points correspond to reared 0. vulgaris aged 0, 10, 20, 30,
42,50 and 60 days (data from Villanueva 1995). Selected prey are hatchling zoeae of Maja brachydactyla (dark
circles) used as prey in Iglesias et al. (2004) and Carrasco et al. (2006); Pagurus prideaux (wh ite circles) and
Liocarcinus depurator (white squares) used as prey in Villanueva (1995); adult stages of the copepod Acartia
tonsa (diamonds) and Artemia nauplii , AF strain (triangles). TL, total length; TW, total weight. Original.
Prey densities in successful cultures using decapod crustacean zoeae ranged from 0.1-0.3
Pagu rus prideaux ml- 1 (Villanueva 1995) to 0.01-1 Maja brachydactyla ml- 1 supplemented with
0.05-0.8 Artemia ml- 1 (Carrasco eta!. 2003, 2006, Iglesias et al. 2004). The effect of different prey
densities needs to be studied in detail. Using Artemia as prey, Iglesias et al. (2006) found no sig-
nificant differences in the number of attacks by Octopus vulgaris hatchlings on Artemia of 1.4 mm
length at densities of 0.1, 0.5 and 1 Artemia ml- 1; however, Marquez et al. (2007), using Artemia
nauplii (0.8 mm length), observed higher consumption rates at 9.4 Artemia ml- 1 in comparison with
2.3 and 4.7 Artemia ml- 1• As Octopus vulgaris paralarvae grow in the second half of their plank-
tonic phase, larger prey are required . Hatchling decapod zoeae decrease in size relative to presettle-
ment paralarvae (>10 mm total length), representing only 9-26% of their length and 0.04-0.7%
of their weight (Figure 29). Presettlement 0. vulgaris-type paralarvae, large Enteroctopus-type
paralarval forms and micronektonic paralarvae forms (see p. 182) probably require larger prey. In
fact,£. dojleini hatchings (10 mm total length) eat mysidaceans 5-15 mm in length during the first
feeding phases in successful laboratory experiments (Okubo 1979). The limited data collected from
the field (Passarella & Hopkins 1991) suggests that euphausiids can be a main prey source for rela-
tively large octopus paralarvae in the wild.
Food searching and prey capture

Experiments with Octopus vulgaris hatchlings showed that light enhanced consumption rates
3-fold in comparison with dark conditions. A higher percentage of non-feeding individuals was
also recorded in the dark, suggesting the importance of light (and vision) in predatory behaviour
(Marquez et al. 2007). However, these authors showed that light may not be essential for prey cap-
ture as a positive correlation was found between prey density and consumption rates in dark condi-
tions. Observations of the swimming paths of 0. vulgaris paralarvae in laboratory conditions over
2 months of planktonic life found that paralarval behaviour is affected by the presence of prey-
individual paralarvae tend to increase their turning rate and reduce swimming speed in the presence
of prey (Villanueva et al. 1996). In the sea, both responses may combine to improve the exploitation
143
of patchy food environments as curvilinear paths and slow swimming speeds increase the probabil-
ity of residence time in a zooplankton patch, increasing the probability of prey encounters.
Capture of live prey

In 0. vulgaris, prey capture can be predicted by a human observer as the paralarva modifies its rou-
tine swimming behaviour in a recognizable behavioural sequence (Boletzky 1987, Villanueva et al.
1996, Hernandez-Garcia et al. 2000). After a zoea prey is selected, three phases can be identified
(Figure 30). The first phase is the 'attention phase'; paralarvae reduce speed and approach the prey,
using a range of different manoeuvring movements including forward, backward and lateral swim-
ming. The second phase is the 'positioning phase'; the anterior end of the body is directed towards
the prey and an aiming posture is adopted with arms drawn together and pointed anteriorly. The
body axis is aligned directly towards the prey. At this time the paralarva is almost immobile, some-
times rotating its position around the prey using jets of water through the flexible funnel, attaining
the best position for attack. The third phase is the 'attack phase'; the paralarvae swims forward fast,
usually through one (sometimes two) powerful jets from the funnel and the prey is seized with all
arms. During the prey capture sequence, a change in chromatophore pattern usually takes place
between the second and third phase (Hernandez-Garcia et al. 2000). During the attention phase,
the paralarvae maintain contracted chromatophores, so that the octopus is nearly transparent to
a human observer; then, during the positioning phase and/or during the contact with the prey, the
chromatophores from the dorsal mantle, head and arms are expanded dramatically. After seizure of
the prey the chromatophores are contracted again. This visual signal is suspected to be defensive
A B c
.
.
.
'
Figure 30 Behavioral sequences during prey capture in 20-day-old individual of Octopus vulgaris (4.4 mm
total length) preying on hatchling zoeae of Pagurus prideaux (3 .1 mm total length). After the prey is selected ,
three phases can be identified: (A) attention, (B) positioning and (C) attack (see text for explanation). Note that
during the attention phase, the octopus maintains contracted chromatophores, then , during positioning and
contact with the prey, the chromatophores from the dorsal mantle, head and arms are expanded. After seizure
of the prey (D), chromatophores are contracted again. The dark oval spot inside the mantle cavity represents
the digestive gland. (Original drawing from Jordi Corbera based on video recordings from Villanueva et al.
1996.)
144
behaviour (see ' Defences', p. 168). Selection of the attack angle probably depends on the type of
prey, its size and defences (i.e., many crustacean zoeae possess dorsal spines) (Figure 28). Further
research is required on the predatory behaviour of octopus paralarvae, as have been made on lolig-
inid squid paralarvae (Chen et al. 1996). Such studies may detect ontogenetic changes in predatory
behaviour along with behavioural responses specific to different prey types.
After prey have been selected, attack distances are usually two to four times the total length of
the octopus, or sometimes more. In Amphioctopus burryi paralarvae preying on wild zooplankton,
these d istances are 10-30 mm (Forsythe & Hanlon 1985). For Octopus vulgaris aged 30 days (mean
octopus total length of 7.4 mm), the reaction distance (R, the maximum predator-prey distance at
which the paralarvae notice the prey during the attention phase) was 15.5 mm (Villanueva et al.
1996). Using an estimated mean cruising speed of25.6 mm s- 1, the estimated water volume searched
(VS) by 30-day-old 0 . vulgaris paralarvae (VS = 2/3·rrR 2 ·cruising speed; Blaxter & Staines 1971)
is 5.5 I min- 1 (Villanueva et al. 1996). This volume cannot be extrapolated to hour units until daily
activity periods are recorded as paralarvae have static periods during which they remain hovering
using weaker ventilatory pulses to provide dynamic lift (Boletzky 1977a). Forward swimming is
always used to capture prey, while backward jetting is used while subduing and ingesting prey.
Mean time taken from striking prey to backwards swimming after subduing the prey is 0.3 s in
0. vulgaris (Villanueva et al. 1996) (Figures 31 and 32). As indicated (see 'Sucker surfaces', p. 122),
the sucker structure of octopus paralarvae suggests that hydrostatic suction is not as effective in
200
A B
160
l
120
N,;! , ｾ｜Ｂ＠
80
ｾＭﾷＧ＠ ..,. l·. /

40
ｾ＠ ' :,f ••:..i;
0
I <J>
E 160
c D
s
l.,
"vv 120
:;;- 80
OJ.)
c:
"§ 40
ｾ＠ ;!
E ............
,,,. _,J!
Ｍｾ＠ 0
Vl
E F
160
r
120
80
40
0
•.,..... ; ,;...,..)"
......
J
. '
ｦＺ｟ＭＬｾＱ •.,J\ _.,kj':
·::·
!
ｾＮ［ｴ＠ .-.•. Ｎ｛Ｑｾ［＠
-4 -2 -0 2 -2 0 2 4
Time (in seconds)
Figure 31 Swimming performance during six successful prey captures by 30-day-old Octopus vulgaris
paralarvae (4.5 mm mean mantle length), using live Pagurus prideaux hatchling zoeae as prey. Time elapsed
before and after capture and swimming speed are indicated at time intervals of 0.04 s. Time 0 indicates the
instant when the octopus strikes the prey. Before prey capture, the paralarva can swim forward (---),
backwards (-----) or laterally C···, only observed in example A), and the arms are pointed towards the prey
(---at bottom of each graph). The same paths in the same order are used in Figure 32. (Reproduced with
permission from Villanueva et al. 1996.)
145
6.------=,.---------,
....-"\, ＶＰｾ］ＭＬ＠
5
:
00
0
%
(A)
ｳｯｬｾ＠ (B)
4 40 e
"/c 0
·.
: /
ｾＮＯ＠
0 • .1'
;'
0 0
ＰＫＭｾＮＺｬ＠
ｾ＠ / i
0 5 10 15 20 0 10 20 30 40 50 60
40,.----------------------, 20,----------------------,
s (C) (D)
30 / 15 s..,
q,ooo
e
· ...._>
e c
5
><
20 e. 10 0
···•.. /..
10 5
ＰＫＭＮｾＺｬ＠ＰＫＭｾＮＺｬ＠
0 5 10 15 20 0 10 20 30 40
70.----------------------, 30 . - - - - - - - - - - - - - - - . ,
(E) (F)
: Ｍｾ
30
ＧＵＨＧ＠
20
10
ＰＫＭｾ＠
0 20 40 60 80 0 10 20 30
X(mm)
Figure 32 Swimming paths of six successful prey capture sequences of 30-day-old Octopus vulgaris para-
larvae, 4.5-mm mean mantle length (open circles) and Pagurus prideaux hatchling zoeae as prey 0. Each
point represents the respective position of the animal at 0.04-s time intervals. c, capture; e, end position ; s,
startin g position. Inset of B, path of octopus before attack, represented by(-----). The same paths are used
in the sam e order in Figure 31. (Reproduced with permission from Villanueva et al. 1996.)
early paralarvae as it is in adults or octopus hatchlings of directly benthic species (Schmidtberg

1997, 1999). This may represent an impediment to holding and subduing prey although the gland
cells on the epithelium of the sucker rims that secrete mucopolysaccharides probably assist in adher-
ence of paralarval suckers (Kier & Smith 1990, Schmidtberg 1999).
Capture of inert prey

Live prey is not a prerequisite stimulus in provoking attacks by octopus paralarvae. Laboratory
studies using inert food showed that attacks usually take place when the dead prey or food particle
descends in the water column (Boletzky & Hanlon 1983). Pellets, millicapsules and fish flakes have
been used as supplementary food for 0. vulgaris paralarvae and are captured when sinking through
the water column (Navarro & Villanueva 2000, 2003, Okumura et al. 2005a, Kurihara et al. 2006).
As the escape response of many water column residents of open ocean is to passively and rapidly
146
sink (i.e., pteropod molluscs and gastropod veliger larvae; Lalli & Gilmer 1989), capture of sinking
food items may not simply be an attempt to capture inert or dead food sources.
Capture of dead prey from the bottom of rearing tanks has also been reported by Itami
et al. (1963) for 0. vulgaris when live prey were scarce in the water column. Okubo (l980) reared
Enteroctopus dojleini from hatching to settlement on floating frozen prey (mysidaceans, amphi-
pods, pieces of shrimp), using a tank with an upwelling water system that maintained movement
of the food particles. Snyder (1986a,b, unpublished manuscript) fed paralarvae of the same species
over 5- 6 months exclusively on inert food and pieces of crab and shrimp meal (3-6 mm wide,
25 mm length) suspended in the tank (Table 3). Marliave (1981) described in detail the neustonic
feeding behaviour of paralarval E. dojleini on pieces of floating thawed krill in laboratory condi-
tions. When the mantles of E. dojleini individuals aged 6 days came into contact with floating
pieces of krill, the octopuses would turn over and adhere to the surface tension film in an inverted
posture with the oral surface of the arms extended towards the surface. On contacting the food with
their arm tips, individuals would seize the krill and leave the surface to feed on it within the water
column, suggesting chemotactile discrimination of these food sources (Figure 33). The neustonic
feeding described by Marliave ceased once the paralarvae reached 1 month old and was replaced
by the capture sequences more typical of the smaller Octopus vulgaris. Neustonic feeding was also
reported by Snyder (unpublished manuscript) for Enteroctopus dojleini and Boletzky (1987) for
Octopus vulgaris hatchlings.
Overall, octopus paralarvae seem to be visual predators but chemical and tactile senses also
seem to play important roles during prey searching and require further research. Octopuses are blind
to colour (Messenger 1977). Certain cephalopods have been shown to be polarization sensitive (see
among others Shashar & Cronin 1996, Shashar et al. 1996). Hatchlings of the squid Loligo pealei
attacked planktonic prey under polarized illumination at a 70% greater distance than under depolar-
ized light (Shashar et al. 1998). The role of polarization vision in octopus paralarvae is unknown
although it is likely to play an important role. As visual predators, octopus paralarvae may target lumi-
nescing prey, particularly when feeding in deeper waters and at night. Dinoflagellate bioluminescence
has also been proposed to help in locating and capturing non-luminous prey during nocturnal feeding
for juvenile cuttlefishes (Fleisher & Case 1995). The same may apply for octopus paralarvae.
Figure 33 Neustonic feeding in Enteroctopus dojleini. Individuals adhering to the surface film in inverted
posture (upper right individual) and normal swimming posture (lower left). Note that reflected glare indi-
cates attachment of the suckers to the water surface and depression of the surface tension film. Scale 4 mm.
(Reproduced with permission from Marliave 1981, modified.)
147
ROGER VlLLANUEVA & MARK D. NORMAN
Buccal mass, denticulate beaks and external digestion

In comparison with adults, octopus paralarvae have relatively short arms with few suckers and a
large buccal apparatus (containing the beaks and radula) and this apparatus is particularly important
at this life-history stage in subduing and chopping the prey prior to ingestion. At hatching, the diam-
eter of the nearly spherical buccal mass represents 30% of the ML and is innervated by the buccal
lobe of the brain that is also proportionally much larger than in recently settled individuals (Nixon
& Young 2003). After settlement, octopuses have a large arm crown and numerous suckers, repre-
senting the main means of prey capture and manipulation. rn adult octopuses, buccal mass length
decreases to around 13% of ML (Nixon 1985, Nixon & Mangold 1996, Nixon & Young 2003).
As stated, the posterior salivary gland papilla and radula are well developed and fully functional
at hatching (Nixon & Mangold 1996). Octopus paralarvae beaks possess oral denticles . These den-
tides have also been observed for para larvae of loliginid (Boletzky 1971) and ommastrephid squids
(Shigeno et al. 2001) and in hatchlings of octopod species with direct benthic young, although
showing less-developed denticulation in these octopod species with direct benthics (Boletzky 1971 ,
1977a). They have also been reported in adult pygmy squid, ldiosepius (Adam 1986, Kasugai et al.
2004). The function of these denticles, typically associated with early stages or pygmy species such
as /diosepius, remains unclear. However, detailed observations on the external digestion and initial
ingestion process (see this section) suggest that denticles may be useful to detach the semidigested
flesh from the exoskeleton of the crustacean prey (Kasugai et al. 2004). Two factors may account
for this dentition. The first is that the radula may be too poorly developed to grip and remove flesh
from the prey. The second is that the dentition may aid gripping the prey in paralarvae with few,
proportionally large (and hence clumsy) suckers. The beaks of presettlement and recently settled
captive-reared Octopus vulgaris individuals show loss of some denticle tips, presumably worn by
their use during feeding on crustacean zoeae larvae (Figure 25B,C). The erosion of the denticles
seems to be a stage in the transition to the thick , darkly pigmented and chitinized beaks of juve-
nile 0 . vulgaris that lack denticles and have rostral tips more characteristic of the adult octopus
(Nixon & Mangold 1996).
[n octopuses, two categories of glands discharge their secretion into the buccal cavity: (1) diffuse
glands of single or small groups of gland cells on the lips, salivary papilla and buccal epithelium
and (2) five major glands (the single submandibular salivary gland below the radular complex, the
paired anterior salivary glands that lie on the posterior surface of the buccal mass, and the paired
posterior salivary glands that lie adjacent to the swollen crop diverticulum anterior to the digestive
gland) (Boucaud-Camou & Boucher-Rodoni 1983, Budelmann et al. 1997, Nixon & Young 2003).
The posterior salivary glands secrete a mixture of substances, including biologically active ami nes,
enzymes (particularly proteolytic enzymes) and toxins with venomous, pharmacological, digestive
and haemolytic properties (Grisley & Boyle 1987, Grisley 1993, Key et al. 2002). The adult octopus
cephalotoxin is responsible for the paralysis and ki II ing of crabs (Ghiretti 1959, 1960) and the ability
of octopus saliva to release crab muscle from the carapace prior to ingestion is principally caused by
proteases in the saliva (Grisley & Boyle 1987), injected into the crab by a narrow hole produced in
the carapace or the cornea of the crab (Grisley et al. 1996, 1999). Prey is then disarticulated and the
flesh removed and ingested, leaving the clean exoskeleton, which is discarded by the octopus.
This process is generally known as external digestion (Nixon 1984) and in octopus paralarvae
has been described for 0. vulgaris hatchlings feeding in laboratory on recently hatched decapod
crab zoeae Pachygrapsus marmoratus, P. transversus and Eriphia verrucosa (Hernandez-Garcia
et al. 2000). The extraction of the edible content of the zoeae by the octopus paralarva means
that the prey remains consist only of a transparent, moult-like exoskeleton with attached append-
ages. Similar observations have also been reported for 11-day-old loliginid squid paralarvae (Loligo
vulgaris) feeding on mysidacean shrimp in the laboratory (Boletzky 1974) and for adults of the
148
pygmy squid ldiosepius (Kasugai 2001, Kasugai eta!. 2004). During external digestion and inges-
tion, the prey is actively handled with arms, suckers and buccal mass. Boucaud-Camou & Roper
(1995) found chymiotrypsin activity on the sucker surface of Octopus sp. paralarvae and suggested
that this enzymatic activity was probably related to secretions of the posterior salivary glands and
involved in diffusion of the octopus enzymes and venom when handling the prey during the external
digestive processes. In addition to an external digestion that rejects the entire crustacean carapace,
analysis of stomach contents of 0. vulgaris hatchlings eating Artemia showed the presence of tho-
racic appendices (thoracopods) of this prey in the stomach contents (Iglesias et al. 2006). Similarly,
exoskeleton crustacean remains were found in stomach contents of wild paralarvae and juvenile
squids (Vecchione 1991 , Vidal & Haimovici 1998), showing that external digestion is not the only
digestive choice for para larvae. The selection of different modes of ingestion and/or digestion by the
paralarvae is probably related to prey characteristics. The mode of digestion as well as the percent-
age of prey ingested or rejected require further research.
Daily food ration by octopus paralarvae is also poorly known. ltami et al. (1963) found that
0. vulgaris of 3-5 or 6-8 mm total length ingested respectively 3-5 or 7-10 Palaemon serrifer
zoeae (2-3 mm in total length) day- 1 when reared at a mean temperature of 25°C. Hatchlings of
the same sp(!cies maintained at 20°C ingested up to lO Artemia nauplii (0.8 mm length) per day
(Marquez et al. 2007). After prey capture, the duration of the ingestion process in Octopus vul-
garis hatchlings preying on 0.8- to 1.4-mm Artemia ranged from 4 to 10 min (Iglesias et al. 2006).
For 15-day-old paralarvae, the duration was up to 15 min when ingesting 250- to 500-j.lm pellets
(Navarro & Villanueva 2000).
Digestive enzymes
In octopods, the anterior and posterior salivary glands and the digestive gland are considered the
most important sites for digestive enzyme synthesis, with final digestion and absorption taking
place in the caecum and digestive gland (Boucaud-Camou & Boucher-Rodoni 1983). Using histo-
chemical methods Boucaud-Camou & Roper (1995) studied enzymes in wild Octopus sp. para-
larvae of 1.7-2.6 mm ML and found non-specific esterase activity, particularly on the epithelia of
the digestive tract (crop, stomach and caecum) and high alkaline phosphatasic activity in the cae-
cum, digestive gland and skin. High levels of acid phosphatase activity were found in the digestive
gland and digestive duct appendages and acetyl-glicosaminidase activity on the posterior salivary
glands, digestive gland and stomach. Protease and chymiotrypsin activity were recorded in all parts
of the digestive tract with virtually zero glucoronidase, amylase and cathepsin B activity. The high
proteol itic activity of the digestive gland seems to be related to the carnivorous diet of the para-
larvae .
Using ftuorometric methods to analyse enzymatic activity in 0. vulgaris hatchlings, Morote
et al. (2005) obtained variation in hatchling protease activity between different egg masses, record-
ing trypsin activity for only 20% of the individuals analysed. This result suggests that trypsin activ-
ity is developed only after active exogenous feeding. In fact, total proteolytic activity, and trypsin
and chymiotrypsin levels in advanced embryos and unfed hatchlings at day 0 show no differences.
However, 5-day-old fasting paralarvae have been shown to decrease their proteolytic activity
(Villanueva et al. 2002). Once external feeding commences, 0. vulgaris paralarvae can adjust their
digestive enzymes to different diets and food rations during the first month of life. This adaptation
seems to be positively correlated with paralarval growth by weight. Differences in enzyme activ-
ity can be detected after 5 days of rearing at a mean temperature of 20°C under high or low feed-
ing regimes, with higher proteolytic, trypsin and chymiotrypsin activities correlating with higher
growth and feeding ratios. In comparison with carnivorous larval fishes, levels of trypsin activity in
0. vulgaris paralarvae seem to be higher. Zambonino-Infante et al. (1996) reported trypsin activity
149
for Dicentrarchus labrax larvae at days 15, 20, 30 and 40 as 40, 120, 78 and 67 mU/mg- 1 of protein
respectively, with a sharp increase in activity after day 20. In Octopus vulgaris paralarvae the cor-
responding trypsin activity under a high feeding regime at days 10, 15 and 20 was 370, 460 and
340 mU/mg- 1 of protein, respectively, with the sharp increase in activity occurring after day 15
(Villanueva et al. 2002).
Nutrient absorption and the importance of the skin

After external digestion and ingestion, food travels through the buccal mass and down the oesopha-
gus and crop to the stomach for internal digestion, aided by salivary and digestive gland enzymes.
Smaller food particles move into the digestive gland or caecum for further digestion . The caecum
processes fine particles and fluids and is considered the main absorptive organ in adult octopods
(Boucaud-Camou & Boucher-Rodoni 1983, O ' Dor et al. 1984). The same role can be expected
for octopus paralarvae although its characteristics have not been studied in detail. R. Villanueva
(unpublished) encapsulated glass ball beads (10-30 Jlm in diameter) within Artemia nauplii and
offered them as food to 12-day-old Octopus vulgaris paralarvae reared at 20°C. The para larvae
started to defaecate glass balls after I h, suggesting that the duration of digestion in this growth
phase is relatively short.
Skin absorption
A secondary and intriguing absorptive tissue of octopus para1arvae is the integument. Castille &
Lawrence (1978) found that planktonic hatchlings identified as Octopus sp. (probably 0. joubini)
uptake radio-labelled amino acids (valine) and hexoses (glucose, mannitol) directly from seawater.
They suggest that this uptake mechanism is more active than diffusion, it is saturable and specific,
and that little of the uptake is due to the bacterial flora associated with the octopod hatchlings.
Radio-labelled amino acid (phenylalanine) uptake from seawater was also recorded in 0. vulgaris
aged 0, 7, 14 and 21 days (Villanueva et al. 2004) and has been recorded for adult cuttlefishes, Sepia
officina/is (de Eguileor et al. 2000). In these laboratory experiments, the contribution to absorption
of radio-labelled marker molecules made by microorganisms in both the cephalopod skin and the
seawater could not be ruled out. Further support for this skin absorptive mechanism came from
Boucaud-Camou & Roper (1995), who used histochemical methods to demonstrate high alkaline
phosphatase activity in the skin of wild Octopus sp. paralarvae. They suggest that the presence
of this digestive enzyme indicates active absorption through the skin from seawater during the
paralarval period . A high microbial presence in the skin mucus covering of rhynchoteuthion squid
paralarvae has also been suggested to be a source of food to these paralarvae (Vidal & Haimovic i
1998).
On the basis of the absorptive and mechanical characteristics of the skin, the addition of small
molecules to seawater in the laboratory has been used experimentally to explore the contribution
of the skin to paralarval growth and survival. Vitamin supplement mixture was added to aquaria
(I mg [- 1 every 3 days) containing 0. joubini paralarvae in rearing experiments that resulted in
successful settlement (Forsythe & Toll 1991). Rearing trials on 0 . vulgaris paralarvae assessed the
contribution of the daily addition of amino acid solution (16 mg 1- 1 of crystalline essential amino
acids) to the rearing tanks. Survival rates for paralarvae aged 20 days were three times higher for
the treated group compared with the control group although the dry weight of the treated para-
larvae was equal to or lower than the controls (Villanueva eta!. 2004). The findings of these studies
combine to suggest that small organic molecules dissolved in seawater are potentially important
nutritional sources (directly or indirectly) for metabolic needs during the first feeding period of
octopus paralarvae.
150
Respiration
In addition to the gills, a high amount of oxygen is obtained by transcutaneous means in cephalo-
pods (Portner 1994). Skin respiration provides between 8% and 41% of total oxygen uptake for
subadult 0. vulgaris (Madan & Wells 1996) and its importance is probably higher in planktonic
octopuses due to their high surface/volume ratio. In fact, skin respiration predominates in early
ontogenetic stages of fishes, but progressively loses importance as gill gas exchange becomes more
efficient and surface-volume ratio declines (Rombough & Moroz 1997). A similar sequence can
also be expected in planktonic octopuses, but no data have been published on this subject. One day
before hatching, oxygen consumption rates in 0. vulgaris ranged from 14 to l7 nmol 0 2 ind- 1 h- 1,
increasing three times in unfed hatchlings (53 nmol 0 2 ind- 1 h- 1) (Parra et al. 2000). Oxygen uptake
as measured in the egg l day before hatching can be considered a good estimation of the resting
metabolism of the hatchling para larvae, with the difference in oxygen uptake after hatching primar-
ily corresponding to the cost of swimming. By comparing the oxygen uptake of advanced embryos
with that of the adults (Wells eta!. 1983a,b), the consumption of a medium-size egg mass of 0 . vul-
ga ris (i.e., 300,000 eggs) can be estimated as being approximately twice that of the brooding female
(of 2 kg total weight). Methods for the transport of 0. vulgaris hatchlings over a 24-h period were
determined by Fuentes et al. (2005), who obtained nearly 100% survival when using transparent
30-1 plastic bags filled one third with oxygen-saturated seawater and two thirds with pure oxygen
gas. Paralarval densities were <3000 ind 1- 1 and temperature was maintained at l4°C.
Biochemical profiles of paralarvae and nutritional requirements

Proteins and amino acids
Proteins are the major organic component of octopus tissue. In contrast to the lipid-based metabo-
lism found in many animal groups (i.e., mammals), cephalopods have a vigorous protein and amino
acid metabolism (Lee 1994). Due to the rapid growth of octopus paralarvae, there is a large amino
acid requirement for maintaining optimal growth and to supply the fuel for energy. Mobilization of
muscle protein provides metabolic energy during periods of starvation and the direct use of protein
as an energy reserve may account for the lack of major glycogen or lipid reserves in cephalopod
tissues (Storey & Storey 1983, O ' Dor et al. 1984). The total protein content measured as N x 6.25
in 0. vulgaris hatchlings represents 73% of the dry weight. However, it should be noted that total
amino acid and the non-protein nitrogen content represent 44% and 37% of the dry weight, respec-
tively (Villanueva et al. 2004). This high non-protein nitrogen content is of a similar range to that
reported for adult cephalopods (Robertson 1965, Sikorski & Kolodziejska 1986, Iida et al. 1992,
Ruiz-Capillas et al. 2002). Major components of this nitrogen fraction are volatile bases such as
ammonia and trimethylamine oxide, creatine, free amino acids, nucleotides, purine bases and urea.
Lysine, leucine and arginine represented 49% of the total essential amino acids and glutamate and
aspartate represented 47% of the non-essential amino acids for 0. vulgaris hatchlings (Villanueva
et al. 2004) (Figure 34).
Fasting experiments in 0 . vulgaris hatchlings demonstrated mobilization of amino acids as
a fuel resource (Villanueva et al. 2004). After 2 days, proline was the first free amino acid to be
deleted . This amino acid is involved in oxidative metabolism in cephalopods, showing notable drop
in man tle muscle concentrations during exercise in adult squid (Storey & Storey 1978) and probably
is also actively metabolized during the continuous, energetically expensive jet-propelled swimming
that is characteristic of octopus paralarvae. After 4 days of fasting, the levels of free non-essential
amino acids decreased to nearly half of hatching levels (with the exception of cysteine), the level
of essential amino acids decreased in both the total content and free forms, free tyrosine was not
detected and animals lost 28% of their dry weight. Reared individuals at 25 days of age showed an
151
12 12
10 Arg lO His
8 8
6 6
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0 0
12 12
lO lO
lie
8 8
6 6
4 4
2 2
.<:
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ｾ＠
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0;,
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-o
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c
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0!) 0!)
w :r:"' ｾ＠ "' ｾ＠
0!) 0!)
ｾ＠ "'
w :r:"' ｾ＠
0!) 0!)
i i i i
Figure 34 Total amino acid content (mean and standard deviation in mg 100 mg- 1 of dry weight) of Octopus
vulgaris from mature ovary, spawned eggs at stages I- ll and X-XII, hatchlings, and hatchlings fasted fo r 2 and
4 days. EAA, essential amino acids. (Reproduced with permissio n from Villanueva et al. 2004.)
152
BIOLOGY OF THE PLANKTONlC STAGES OF BENTHIC OCTOPUSES
60 15
14
-·-- ----·
Q
ｾ＠ 13
a 55 12 ｾ＠
' ''
ｾ＠
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o-q.:•
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11
ｾ＠
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45
ｾＭ
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8
7
6
,3
40 5
0 2 3 4
Dry weight (g)
Figure 35 Mean value of total amino acid content (solid circles) and total lipid content (open circles) in
Octopus vulgaris hatchlings (0.3 mg dry weight, OW) and five wild, recently settled 0. vulgaris juveniles
of 814, 1128, 1380, 2189 and 3671 mg OW. (Data obtained from Navarro & Villanueva 2000, 2003 and
Villanueva et al. 2004.)
increase in free essential amino acids in comparison with hatchlings, and glutamate was the most
abundant free amino acid, followed by arginine and aspartate. These amino acids, with leucine and
lysine, were also the most abundant in the total content, although glutamate had the highest levels.
For free essential amino acids, arginine reaches the highest levels and represents nearly half of the
free essential amino acid pool for hatchlings, 55% after 4 days of fasting, 38-59% at 10 days and
32-45% at 25 days of rearing (Villanueva et al. 2004).
The total amount of amino acids in 0 . vulgaris paralarvae is lower than in recently settled juve-
niles. These biochemical changes associated with paralarval and juvenile growth are related to mor-
phometric changes in body proportions, mainly due to the notable growth of the arms (Naef 1923,
1928, Boletzky 1977a, Nixon & Mangold 1996, Villanueva et al. 2004), which continues throughout
development because juveniles have arm lengths four to five times shorter than subadult and adult
individuals (i.e., 0 . vulgaris; Villanueva 1995). The development of the protein-rich muscular arm
crown is accompanied by a relative decrease in total lipid content (Navarro & Villanueva 2003),
this being due to the relative decrease of the visceral mass in which lipids are abundant (O'Dor et al.
1984) (Figure 35).
Lipid and fatty acids

Octopus paralarvae have relatively low lipid content. Lipid represents 11-14% of dry weight in
0. vulgaris hatchlings and variation in this content throughout paralarval growth (11-25%) in rear-
ing experiments seems to be related to diet (Navarro & Villanueva 2000, 2003, Moxica et al. 2002,
Okumura et al. 2005a). The lipid-rich nervous system of hatchling 0. vulgaris paralarvae represents
approximately one quarter of the animal's fresh weight (Packard & Albergoni 1970), suggesting the
importance of lipids in the diet to maintain suitable growth during planktonic life. After settlement,
the total lipid content of wild juveniles decreases, ranging from 7% to 13% of total dry weight in
animals of 45-3671 mg in dry weight. The lipid content in recently settled octopuses was found to
be significantly and negatively correlated with the weight of juveniles due to morphometric changes
associated with arm growth (Figure 35) and could be fitted to the following regression equation
(Navarro & Villanueva 2003):
Lipid(%) = 11.436- 0.0016 x dry weight (mg)
153
35
30
25
"0
;g.
-;;;
20 ,
:S
.....
11 ｾ＠
0
15
ｾ＠
10
0
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a.
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"0
0
..c ｾ＠ "'
Vl
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t;o
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E
Lipid class
Figure 36 Lipid class composition as percentage of total lipid in Octopus vulgaris hatchlings (solid bars),
Pagurus prideaux hatchling zoeae (g rey bars), Artemia biomass enriched with SuperSelco (open bars) and
30-day-old reared 0. vulgaris fed with Artemia (bars with transverse lines). Data as mean of four replicates.
Error bars are standard deviation . chol, cholesterol; dag; diacylglycerides; ffa, free fatty acids; lpc, lysophos-
phatidylcholine; mag/pigm, monoacylglycerides/pigments; palcl , phosphatidic acid/cardiolipin; pc, phosphati-
dylcholine; pe, phosphatidylethanolamine; pi , phosphatidylinositol; ps, phosphatidyl serine; se, sterol esters;
sm, sphingomyelin; tag, triacylglycerides. (Reproduced with permission from Navarro & Villanueva 2000,
modified.)
In general, the lipids of hatch Iing 0. vulgaris are rich in cholesterol (24%), phosphatidylchol ine
(2 1%), phosphatidylethanolamine (16%), and sterol esters ( 14%) and are relatively low in triacylglyc-
erides (6%) (Navarro & Villanueva 2000) (Figure 36). Endogenous synthesis of cholesterol is absent
in adult cuttlefi shes (Zandee 1967), suggesting that cholesterol is an essential dietary nutrient in
cepha lopods; the cholesterol requirements of octopus paralarvae, however, have been not examined
in detail. The use of reserve lipids has been recorded during fasting of hatchling 0. vulgaris para-
larvae because the animals reduce their content in triacylglycerides and monoene fatty acids after
3 days (Qu intana et at. 2006). In hatchlings, fatty acids represent 4.6% of lipids- of which 27%
were saturated, 14% were monoenes and 49% were PUFAs and the majority of the PUFAs were n-3
(36%) and longer than 20 C atoms (Navarro & Villanueva 2000).
The dietary requirements for n-3 PUFA, particularly docosahexaenoic ac id (DHA), is c ritical
in ea rly developmental stages of fishes a nd crustaceans due to their high demand in membrane
synthesis, where the n-3 PUFAs are incorporated (Henderson & Sargent 1985). The same role is
expected for early stages of cephalopods (Navarro & Villanueva 2000). Levels of DHA and e icosa-
pentaenoic acid (EPA) fatty acids in 0. vulgaris hatchlings represent 21-27% and 13- 18% of the
total fatty acids, respectively (Navarro & Villanueva 2000, Okumura et at. 2005a, Kurihara et at.
2006). The effect of the fatty acid composition of food is evident in paralarvae within a few days of
hatching. It has been suggested that their presence in the diet is critical for the early development of
paralarvae because their level s are associated with healthy and normal paralarval growth in rearing
experiments (Navarro & Villanueva 2000, 2003, Hamasaki & Takeuchi 2001, Moxica et at. 2002,
Okumura et at. 2005a, Kurihara et at. 2006). A ratio of DHA/EPA of approximately 1.5 seems a
necessary condition for normal growth and development of 0 . vulgaris paralarvae. High mortality
and poor grow th associated with nutritional imbalance in fatty acid profiles has been observed when
154
DHA/EPA is <1.5 (Navarro & Villanueva 2000,2003, Okumura et al. 2005a). DHA pl ays a n impor-
tant role in maintaining the structura l a nd functional integrity of cell membranes in fishes (Sargent
1995) a nd this fatty acid may be even more important for hea lthy development and survival of the
fas t-grow ing, phospho! ipid-rich octopus para larvae.
Elemental composition
The elemental compositi on of hatchlings, reared paralarvae and recently settled wild juveniles of
0. vulgaris was reported by Villanueva & Bustamante (2006) (Figure 37), showing that S, Na, K,
P and Mg were the main elements present, and levels of Ag, Cu , Mn , Ni and Zn higher compared
with other cephalopod hatc hlings such as Loligo vulgaris and Sepia officina/is. Concentrations
of non-essential elements (Ag, AI, Ba, Cd, Hg, Pb) found in hatchlings and reared para larvae of
Octopus vulgaris are lower compared with those found in subad ult and adult octopuses (Seixas et al.
30000 ｾｯＮＭ＠
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0 ""<: 0
u0 :::1
0.. ｾ＠ u0 :::1
0.. ｾ＠ｾ＠
0
u0
t!
""<:
3u ...
""<:
0
Figure 37 Compariso n of mea n and standard deviation in e lemental content ()lg g- r dry weight, OW) for
some major (S, Mg, P) and minor (As, Cu , Zn) essenti al elements in Octopus vulgaris hatchlings (mea n OW
0.34 mg), Arremia-fed 20-day-old 0. vulgaris (mea n OW 0.68 mg), 0. vulgaris wild juveniles (mean OW
1836 mg) and prey (Maja brachydactyla hatchling zoeae and Artemia nauplii). (Reprod uced with permission
from Villanueva & Bustamante 2006, modified.)
155
2005), showing their incorporation during growth. The richness of Cu in 0. vulgaris hatchlings is
remarkable (217 1-1g g- 1 dry weight) and may indicate a particular nutritional requirement for this
element during paralarval growth. Copper is of particular interest due to its critical role in haemo-
cyanin, the respiratory pigment that represe nts 98% of cephalopod blood proteins (Ghiretti 1966,
D'Aniello et al. 1986). Reared 20-day-old 0. vulgaris paralarvae that were fed on Artemia nauplii
(a prey with relatively low Cu content [9.5 1-1g g- 1] in comparison with natural prey such as Maja
brachydactyla zoeae [72.5 1-1g g- 1]), showed nearly half the Cu content of the ' natural' profile for
octopus hatchlings or wild juveniles, suggesting a dietary effect (Figure 37). These findings concur
with nutritional experiments carried out on recently settled (3-4 g fresh weight), subadult and adult
Octopus vulgaris fed with sardine (low Cu content) versus control animals fed with crab (high Cu
content). In the sardine-fed animals, the Cu content in the digestive gland (the main reserve for Cu)
dropped to 1/10 compared with controls after 3 months of this diet. Haemocyanin disappeared from
the circulating blood and the octopuses died after 5 months of rearing (G hiretti & Violante 1964).
Zinc content of octopus paralarvae seems to be inversely related to Cu content as individuals with
low levels of Cu (fasted or reared paralarvae) showed significant increases in Zn content compared
with hatchlings or juvenile wild octopuses with their higher levels of Cu (Villanueva & Bustamante
2006). Zinc can act as a metabolic antagonist of Cu because they compete for binding sites on the
proteins responsible for mineral absorption and/or synthesis of metalloenzymes (Watanabe et al.
1997, Lall 2002, Craig & Overnell 2003).
Octopuses are carnivores and the majority of their elemental composition can be assumed to be
derived from their diet. However, absorption also takes place directly from seawater, as observed
under experimental conditions for strontium and cobalt (Hanlon et al. 1989, Miyazaki et al. 2001).
Strontium is of critical importance for statolith development and thus normal swimming behaviour
and survival of hatchling cephalopods, including octopuses. Egg incubation in artificial seawater
without strontium produced 0. vulgaris hatchlings that showed behavioural defects characterized by
swimming in a spinning motion ('spinners'). Statoliths from 0. vulgaris spinners were irregular in
shape and considerably reduced in size compared with control animals. Some strontium-deficient ani-
mals lacked one or both statoliths. Normal development of the aragonite statoliths and normal swi m-
ming behaviour were obtained when strontium levels reached 8 mg 1- 1 (Hanlon et al. 1989). Cobalt
also seems to be important in the development of adenochrome, the red-violet pigment that confers a
characteristic purple colour to the branchial hearts of octopuses, the organs involved in excretion pro-
cesses. Miyazaki et al. (2001) showed that 0. vulgaris hatchlings incorporate radio-labelled cobalt
in the digestive gland and the inner side of the branchial hearts within I min of immersion in radio-
labelled seawater. Other organs and tissues were not radiographed. Miyazaki et al. (2001) suggested
that adenochrome might be a cobalt-binding substance, in addition to iron, and that the radio-l abelled
cobalt may indicate the incipient development of adenochrome in the hatchlings.
Growth and duration of the planktonic stage

Size at hatching
A comparison of morphometries of planktonic hatchlings in Octopodidae is shown in Table 4. There
is a wide range of sizes, from 2.5 to 18.3 mm in total length in fresh individuals, with the larger
hatchlings belonging to the largest of the benthic octopuses, genus Enteroctopus. Shrinking due to
fixation in preserved hatchlings shows that ML and total length can be 12-25% and 13- 17% shorter
(respectively) in preserved specimens compared with fresh (unpreserved) material (Boletzky et al.
2001, Ortiz et al. 2006). These differences should be considered when comparing species and data
from the literature. The number of suckers per arm also shows a considerable interspecific variation
ranging from 3 to 21 (Table 4, Figure 38). The number of suckers is not affected by preservation
156
Table 4 Size and sucker number per arm in hatc hlings of Octopodidae species
wi th pla nktonic stages
Meas ured Number
fresh or of suckers Geographi c
Species preserved ML TL per arm area Referen ce
Amphioctopus Np 3.1 ±0.1 6 Indi an Ocean Ignatius & Srinivasan

aegina 2006
Amphioctopus burryi F 1.5 ± 0.05 2.5 ± 0.08 4 NW Atlantic Forsythe & Hanlon
1985
Callistoctopus F 4 5.5 7 Mediterranean Boletzky et a l. 200 I
macropus
p 3 4.8
Enteroctopus Np 9 .3 NW Pacific Yamashita 1974
dofe/ini Np 5.3-5.5 10 (9.5- 10. 1) NW Pacific Okubo 1979
p 3.5 ll -14 NE Pacific Gabe 1975
Np 6-8 10--1 2 NE Pacifi c Snyder l986a,Snyder
unpubli shed
Np 3.4 6.9 NE Pacific Hartwick 1983
Enteroctopus F 8.4 ± 0.7 18.3 ± 1.7 21.2 ± 2.7 SW Atl ant ic Ortiz et al. 2006
mega/ocyathus
Eledone cirrhosa Np 4.5 8 Mediterranean Mangold et al. 1971
Hapalochlaena Np 2.3 10 Centra l E Overath & Bolet zky
lww lata Pacific 1974
Macroctopus F 7.1 (6 .7-7.6) 7-8 SW Pacific Batham 1957
mao rum
Octopus bimaculatus Np 2.6 4 4 NE Pac ific Ambrose 198 1
Octopus cyanea p 1.1 -2.0 3 Hawaii Islands Youn g et al. 1989
Octopus huuoni F 3.8 ± 0.1 4 SW Pacific Brough 1965 (as
Robsonel/a australis)
Octopus joubini F 2.4-2.6 6-8 NW Atl antic Forsythe & Toll 199 1
Octopus laqueus Np 1.7 ± 0.2 3.3 ± 0.3 3 NW Pacific Kaneko et al. 2006
Octopus mimus Np 1.9 2.0--.2.4 3 SE Pacific Warnke 1999
Np 0.98 1.9 3 SE Pac ifi c Baltazar et a l. 2000
Np 1.5 ±0.1 3.1 ±0. 1 3 SE Pacific Castro- Fuentes et al.
2002
Octopus salwii F 3.5-4 5.5 4 Mediterranean Mangold- Wirz et al.
1976
Octopus tetricus F 2.5 3 SW Pacific Dew 1959
(as 0. cyanea)
Octopus cf tetricus Np .2.5 E Indian Jo ll 1976
Octopus vulgaris F 2.1 (2-2.3) 3.2 (3-3.5) 3 NW Pacific ltami et al. 1963
Np 4 NW Pacific Hamazaki et al. 1991
F 2 2.9 3 Mediterranean Villanueva 1995
F 3.7-4 NW Pacific Okumura et al.
2005a,b
Scaeurgus Np 4 Mediterranean Boletzky 1984
unicirrhus
Note: Onl y spec ies in whi ch individual s hatc hed in the laboratory from egg masses laid from a prev io usly identified femal e
have been incl uded. F, fresh; ML, mantle length ; Np, not provided; P, preserved; TL, total len gth. Measurements in
millimetres.
157
24
§
21
•
"'....
QJ
18
ｾ＠
QJ
""'u
15
12
•
::l
0
.....0
'J>
9
• .o
E
::l
6 0
z 3 ｾＰ＠ •
0
0 2 4 6 8 10
ML(mm)
Figure 38 Relationship between mean number of suckers per a rm and mantle length (ML) for hatch lings of
14 Octopodidae species with planktonic stages. The figure only includes species for which individuals hatched
in the laboratory from egg masses laid by identified females (see T<').ble 4). Black circles indicate species mea-
sured fresh; white circles indicate species measured after fixation (with presumed shrinkage), as well as spe-
cies for which measurement conditions (fresh or preserved individuals) were not indicated. Original.
methods and provides a useful parameter of paralarval size and growth. Distal suckers are usu-
ally smaller than the other suckers at hatching, with some exceptions, such as Amphioctopus bur-
ryi, which hatch with four suckers per arm with the proximal sucker being considerably smaller
(Forsythe & Hanlon 1985).
Intraspecific variation in size and number of suckers at hatching has been reported for species
such as Octopus vulgaris from the north-west Pacific. Females collected from the same region pro-
duced hatchling individuals ranging from 1.1 to 3.2 mg mean fresh weight and three to four suckers
per arm (Okumura et al. 2005a,b, Kurihara et al. 2006). Maternal body size and egg incubation tem-
perature also influence hatchling size in 0. vulgaris because female weight is positively correlated
with hatchling size (in ML and mantle width) (r = 0.681) and hatchling size is negatively correlated
with the egg incubation temperature (r = -0.381) (Sakaguchi et al. 2002, Sakaguchi 2006). There
is a similar tendency in other cephalopod groups because egg incubation at warmer temperature
produces comparatively smaller hatchling sizes in cuttlefish (Bouchaud 1991) and loliginid squids
(Villanueva 2000, Gowland et al. 2002, Vidal et al. 2002, Peel et al. 2004).
Ageing and factors influencing growth

The analysis of statolith growth increments, a technique routinely used to estimate age and growth
in squids, is not possible in octopods due to the crystallization characteristics of their statoliths-
loose composites without evident growth increments. As a consequence, other hard structures have
been investigated to find periodic depositions of growth. The number of concentric rings in the
lateral wall of upper beaks from reared 0. vulgaris para larvae proved to be highly correlated with
their age in days during the first month of life (Hernandez-Lopez et al. 2001). The internal shell
remnants ('stylets') in the family Octopodidae also have growth increments in the form of concen-
tric layers (Sousa-Reis & Fernandes 2002, Bizikov 2004) and their deposition proved to be daily
under aquarium conditions for a species with direct benthic hatchlings , 0. pallidus (Doubleday
et al. 2006). The internal shell analysis promises to be a helpful technique to be used in the future
in ageing of octopus paralarvae. Fluorochrome alizarin complexone is an effective chemical marker
because it is incorporated into the statoliths of 0. vulgaris hatchlings (Fuentes et al. 2000) and adults
(Sakaguchi et al. 2000, Sakaguchi 2006), suggesting that this marking technique could potentially
be used to identify alizarin-stained octopod paralarvae.
158
60 - , - - - - - - - - - - - - - - - - - - - - - - - ,
"'
OJ
00
.0:: 30
y = 168566x - 2·6676
r = -0.9476
20 ＱＭＬｾ＠
16 18 20 22 24 26 28 30
Temperature (oC)
Figure 39 Relationship between the mean rearing temperature and age at settlement from successful rearing
experiments of Octopus vulgaris. Error lines indicate temperature ranges. (Data obtained from ltami et al.
1963, Villanueva 1995, Iglesias et al. 2004 and Carrasco et al. 2006.) Exponential regression line, equation
and correlation coefficient indicated. Original.
After hatching the main abiotic factor influencing planktonic octopus growth seems to be
temperature, as has been observed in other cephalopod paralarvae (Forsythe 1993). Hamasaki &
Morioka (2002) reared 0. vulgaris hatchlings at temperatures of l7°C, 19°C, 21°C, 23°C, 25°C,
27°C and 29°C and fed with Artemia prey (1.5-2 mm in length) over the first 40 days of life. They
concluded that growth rate increased with increasing rearing temperature up to 2l°C, and that
temperatures higher than 27°C were not suitable for this species. Under suitable temperature, food
and settlement conditions, it would be expected that age at settlement would be inversely correlated
with temperature. In fact, a comparison of successful rearings to settlement using crustacean zoeae
as food for 0. vulgaris (Itami et al. 1963, Villanueva 1995, Iglesias et al. 2004, Carrasco et al.
2006) shows that warmer rearings produced faster growth and that settlement was observed earlier
(Figure 39). Modelling of 0 . vulgaris settlement patterns according to temperature in temperate
latitudes suggests shorter planktonic periods when temperature is increasing (early spring to mid-
summer) or longer planktonic periods when temperature is decreasing (during autumn and winter)
(Katsanevakis & Verriopoulos 2006).
The duration of the planktonic period in Octopodidae seems to be species specific, temperature
dependent and, under laboratory conditions, ranges from 3 wk in the pygmy octopus 0 . joubini to
6 months in the giant octopus Enteroctopus dofleini (Table 3). This is a considerable proportion of
the life cycle, taking into account that, under laboratory conditions, life cycle of the same species
(including embryonic period) ranges from 6 months to 3.5 yr (Forsythe & Toll 1991, Snyder unpub-
lished manuscript). In addition to prey availability, it is reasonable to suspect that behaviour and asso-
ciated spatial distributions can influence planktonic growth. Vertical migration rhythms and related
residence periods in the water column at different temperatures need to be investigated to obtain a
more precise view of the expected growth and related duration of planktonic life in octopuses.
Behaviour
Swimming behaviour
The locomotion of octopus para larvae is based primarily on jet propulsion, the characteristic mode
used by most octopods for swimming (Wells 1990). The main exception is fin swimming in the
159
Figure 40 Schemat ic line drawing showing differences between the mantle cavities of Octopod idae and
Loliginidae para larvae. Left, Octopus vulgaris (3-mm mantle length [ML) , aged 20 days) with two cavities
(ventral and dorsal), compared with Loligo opalescens (7.8-mm ML, aged 50 days) with only one dorsal
mantle cavity (right). Individuals not at the same scale. (Original drawing from J. Corbera.)
semigelatinous deep-sea cirrate octopods (Collins & Villanueva 2006). The funnel, pallial aper-
ture and interbrachial webs of octopus paralarvae are proportionally more developed than those of
squids. Their arms are also larger, increasing in relative length as the animal grows. During a jetting
cycle, the contraction of the mantle and collar muscles produces high hydrostatic pressure inside
the mantle cavity, which generates a propulsive jet of water through the funnel, resulting in the dis-
placement of the animal. During the first days after hatching, the volume occupied by the internal
yolk reserve in cephalopods probably reduces the effective water volume available for ventilation
and jet propulsion. Using ultrasonography and optical methods to estimate ventilation volume of
Octopus vulgaris paralarvae, Tateno (1993) showed that fraction ejected during the first 2 wk of life
increased with growth.
Swimming in octopus paralarvae differs from other planktonic and pelagic cephalopods due
to the particulars of their morphology. Octopus paralarvae lack fins and the vanes or keel s found
on the lateral arms of many decapodiform cephalopods (i.e., ommastrephid squids). The body of
planktonic octopus paralarvae tends to be globular and less elongate than in planktonic squids,
which typically have a shell ('gladius') that guides mantle contraction during jet propulsion. In
addition to the ventral mantle cavity, octopuses also have a dorsal cavity, absent in most squids
(Figures 40 and 41). The relative percentages of water that occupy the dorsal and ventral cavities
during the jetting cycle in octopus paralarvae are still unknown and need to be quantified in order
to understand their swimming capacities. Cranchiid squids (Clarke 1962) and pelagic octopods
(Packard & Wurtz 1994) have dorsal and ventral mantle cavities that facilitate sophisticated swim-
ming and manoeuvrability through independent control of both cavities. Swimming behaviour in
octopus paralarvae that hatch at a small size (as in 0. vulgaris) modifies as the animal grows from
hatching to settlement. These changes are directly related to morphometric changes, primarily the
strong development of the muscular arm crown (Villanueva et al. 1996). Similarly, differences in
swimming behaviour can be expected for different octopus species according to the specifics of
their hatchling size and body form.
Swimming behaviour of planktonic para larvae

Hydrodynamic forces probably dictate the swimming capacities and related behaviour of different
species of octopus paralarvae. However, other unknown neurological and/or physiological charac-
teristics may also play roles. The para larvae of two species groups provide examples of extremes in
form and swimming behaviour: (l) small planktonic hatchlings (ML -2 mm) with short arms and
-3 suckers per arm (0. vulgaris-type) and (2) large planktonic hatchlings (ML -6 mm) with long
160
Figure 41 The use of the dorsal and ventral mantle cavities for jet swimming in Enteroctopus dojleini hatch-
lings. The left individual is shown during the inhalatory phase; note the anterior part of the dorsal mantle and
the ventral mantle cavities expanded by the internal water pressure and the relatively flaccid funnel. The right
individual is in the expulsive phase; note the contracted dorsal and ventral mantle cavities and the rectilinear
funnel due to the expulsion of water from the mantle. (Reproduced with permission from Okubo 1973.)
arms and >10 suckers per arm (Enteroctopus-type). There seems to be a continuum between these
two extremes. Large planktonic hatchlings with short arms have not been described to date.
Using video-recording techniques, the swimming behaviour in Octopus vulgaris was studied
by Villanueva et al. (1996) in groups of individuals aged I, 15, 30, 42 and 60 days (by which time
they had become benthic). Backwards, squid-like swimming is the predominant type of locomotion
during routine swimming throughout planktonic life, with forward displacement representing only
1% of swimming (excluding prey capture sequences; see 'Capture of live prey', p. 144). Cruising
swimming speed increased as animals grew and relative swimming speed in units of octopus length
decreased with size (Figure 42). The mean speed and distance covered during a burst jet cycle
ranged from 41 to 95 mm s- 1 and 6 to 23 mm at respective ages of I and 60 days. The mean maxi-
mum speed reached was 211 mm s- 1 for individuals aged 30 days and 4.5 mm in ML. These maxi-
mum speed values are similar in range to those observed for hatchling squid paralarvae: 160 mm s- 1
in Loligo vulgaris (Packard 1969), 150-250 mm s- 1 in L.forbesi (Zuev 1964 in Mileikovsky 1973)
and 52 mm s- 1 in lllex illecebrosus (O'Dor et al. 1986).
In captive large octopus paralarvae, such as those of the genus Enteroctopus, constant swim-
ming by jet propulsion is intermittently interspersed by descent to the bottom of the rearing tank for
short periods of time, as has been reported for£. dojleini (Gabe 1975, Snyder unpublished manu-
script). During the first month of life£. dojleini actively use their arms and tactile discrimination
to collect floating inert food from the water surface film , described by Marliave (1981) as neustonic
feeding (see 'Capture of inert prey', p. 146). One of the most extreme examples in a hatchling con-
sidered to be planktonic is that of E. megalocyathus, for which hatchlings have a mean of21 suck-
ers per arm and can swim slowly with loose arms for several hours at a time in the water column,
as well as crawling for short distances on the substratum of the aquaria (Ortiz et al. 2006). When
disturbed, animals responded in two ways: swimming (sometimes ejecting ink) or crawling on the
aquarium substratum with a coordinated action of the arms and displaying expanded chromato-
phores. Ortiz et al. (2006) suggest that E. megalocyathus hatchlings may reside in the water layer
close to the seafloor, the hyperbenthos (sensu Mees & Jones 1997), for a short period until they
attain a benthic mode of life.
Swimming behaviour of micronektonic paralarvae

Wild observations of paralarvae on moonless nights over deep water (-1 km) in the Coral Sea
found significant differences in swimmmg behaviour between different species of paralarvae
161
Age (days)
2 10 20 30 40 50 60
ｾ＠ t
C> ｾ＠ Q§
100
I 90 240
"' X
E: 80 -o
Q)
5-o 70 ｾＬＧＱ＾＠
220 ·=
.s::
Q)
Q) S'"\{{' " 00
c:
60 /
ｾ＠ >/ ｾ＠
200 -;;;
""c:
·v;
50 /
l '
ｾ＠
·:;
u 40
30
//1/ \ 180
/
/
20 Ｏｾ＠ 160
/
/
ﾷｾ＠
10
0
r-- --]'
/ Crawling
2 2.9 4.5 6.4 8.6

ML(mm)
Figure 42 Mean and standard deviation of cruising swimming speed (in mm s- 1) (black squares) and total
length index (white squares) versus mantle length (ML, in mm) and age (in days) of Octopus vulgaris para-
larvae. Crawling speed of recently settled individuals aged 60 days is also indicated. Data collected from
digitized video recordings of groups of five individuals. Top, schematic drawings of 0. vulgaris individuals
aged I, 30 and 60 days. (Reproduced with permission from Villanueva eta!. 1996.)
(M.D. Norman unpublished data). Those paralarvae with short arms and near-spherical bodies (i.e.,
Figure 9) showed relatively slow swimming speeds. Longer-armed, more elongate species (such as
Callistoctopus sp.; Figure 4 top) swam faster and took on an elongate form superficially similar to
small ommastrephid squid also occurring in the same environment (Callistoctopus sp.; Figure 43).
This body form may partially explain why certain micronektonic paralarvae are able to delay
settlement (see 'Prolonged paralarval stages', p. 182). From hydrodynamic and energetic perspec-
tives, these paralarvae may be adopting a squid-like strategy: an elongate mantle that enables more
energy-efficient jet swimming. This form of locomotion is not possible as a prolonged mode of
swimming for settled, benthic octopuses because their small mantle volume cannot power the dis-
placement of relatively long and heavy muscular arms (Wells et al. I983b, 1987) (see also 'The
settlement process', p. 176).
ln addition to jet propulsion, long-armed large paralarvae such as Macrotritopus defilippi have
been observed in the wild drifting with all arms spread out radially. The animal seems almost
neutrally buoyant, remaining almost stationary with little or no jetting (Hanlon et al. 1985). These
animals also combined these modes of locomotion with slow backwards jet swimming with the
arms trailing in a V and the tips usually curled, but also with fast backwards jets when disturbed
by a diver. It is remarkable that these animals were also observed to crawl over a coral substratum
and as described by Hanlon et al. (1985, p. 238): " ... they spread the arms radially and landed oral
surface first. Both animals quickly slid into holes and disappeared from view. It was clear that the
substrate was not alien to them."
More research is necessary to understand swimming behaviour in octopus paralarvae. Some
similarities can be expected with the complex slow-swimming behaviour of small squids that employ
various fine-scale adjustments, such as manipulating funnel diameter during jetting, altering arm
162
Figure 43 (See also Colour Figure 43 in the insert.) Unidentified paralarva of the genus Callistoctopus from
the Coral Sea, Australia, showing elongate form when swimming. Photograph taken in situ while night div-
ing on a moonless night at-10m deep over a seafloor depth of 450 mat Osprey Reef, Coral Sea, Australia.
(Photo: M.D. Norman .)
position and swimming in different orientations to increase swimming performance (Bartol et al.
2001). In addition, the proportion of water volume ejected from the mantle is expected to change
throughout paralarval stage, as occurs in hatchling squid, for which this volume is proportionally
higher compared with later growth stages (Thompson & Kier 200la,b, 2006).
Crawling
Crawling behaviour is readily observed in hatchling paralarvae contained in captivity. The physical
constraint of aquaria may account for some or all crawling behaviour over aquaria surfaces (i.e., Joll
1978, Ambrose 1981). However, in hatchlings of some species such as Enteroctopus megalocyathus
(seep. 161), a combination of swimming and crawling has been reported (Ortiz et al. 2006). An
adhesion reflex, in which the suckers are pressed against a surface and coordinated crawling takes
place, can be experimentally induced in planktonic hatchlings of Scaeurgus unicirrhus by reducing
the space available down to a droplet of water (Boletzky l977b). Crawling of octopus paralarvae
on hard substrata has also been observed in the wild. Paralarvae of at least three species attracted
using lights at night over deep water in the Coral Sea readily adhered to any hard surfaces, particu-
larly ropes, buoys, light traps, divers and camera housings (M.D. Norman personal observation). On
several occasions paralarval numbers of one unidentified species were so numerous that thousands
of animals completely covered the mooring lines between the ship and a boat tender, while all div-
ers returning from night dives were covered in crawling paralarvae. Rafting behaviour has been
reported for both paralarval (Smale & Buchan 1981) and adult octopuses by which they attach on
floating surface objects. Thiel & Gutow (2005) listed II species of cephalopods rafting on wood or
macroalgae, including adult Octopus bimaculatus, 0. bimaculoides, 0. micropyrsus, 0. variabilis
and 0. vulgaris. This may have advantages both as a means of passive transport/energy conserva-
tion and as potential food-aggregating structures.
163
Responses to light and gravity

Positive phototaxis seems to be a common response to light in octopus hatchlings as well as in
some later paralarval stages. Under laboratory conditions, positive phototaxis has been reported
for hatchlings of several species, including Amphioctopus burryi (Forsythe & Hanlon 1985),
Enteroctopus dojleini (Ruggieri & Rosenberg 1974, Yamashita 1974, Okubo 1979), Macro ctopus
maorum (Batham 1957), Octopus bimaculatus (Ambrose 1981), 0. cyanea (Dew 1959), 0. mimus
(Montoya 2002), 0. vulgaris (Vevers 1961, Villanueva 1995, Nixon & Mangold 1998), 0 . hut toni (as
Robsonella australis) (Brough 1965) and Wunderpus photogenicus (Miske & Kirchhauser 2006).
In contrast, negative phototaxis and an avoidance of strong light intensity has only been observed
for hatchlings of one species, Octopus cf tetricus (loll 1976)- interesting behaviour that requires
further research.
In interpreting some hatchling behaviours, discrimination between positive phototaxis and neg-
ative geotaxis can be difficult. Laboratory-hatched Enteroctopus dojleini that were transported to a
hatching site in the field immediately began swimming up towards the surface (High 1976). Octopus
bimaculatus hatched in the field during the daytime also swam upwards to depths of 1-5 m below
the surface (Ambrose 1981). Rising hatchlings can be interpreted as either positive phototaxis (head-
ing towards surface light) or negative geotaxis (resisting gravity and rising towards surface waters).
Newly hatched squid Loligo pealei also rise to surface waters. Sidie & Holloway (1999) found use
of lights at the bottom of experimental tanks could not prevent the vertical movement of the squid
paralarvae towards the surface in the first 6-12 h after hatching. This suggests that negative geotaxis
is the stronger factor in this behaviour. Similar processes may occur in octopus paralarvae.
Migration to surface waters could aid hatchling dispersal because surface currents may carry
the paralarvae beyond the natal environments. Movement to surface waters may also enable access
to neustonic prey such as crustacean zoeae. For tropical octopus species on isolated coral reefs, sur-
face currents may transport hatchlings away from high-predator reef environments to the compara-
tive safety of open ocean, potentially aiding in gene flow between coral reefs and atolls.
Positive phototactic behaviour has been used to collect octopus paralarvae at night in the field .
Using light traps, Moltschaniwskyj & Doherty (1995) collected 2066 individual octopus paralarvae
on the Great Barrier Reef, estimating this number to be around half the total number of plank-
tonic cephalopods attracted to their lights. The strong response of octopus paralarvae towards light
may be higher than for other planktonic cephalopods. Light attracts not only hatchlings, such as
Enteroctopus dofleini collected on surface waters (Packard 1985), but also relatively large para-
larvae such as those of the Macrotritopus defilippi species complex (Hanlon et al. 1980b, Brower
1981, Hanlon et al. 1985) and Amphioctopus burryi (Hanlon et al. 1980b, Forsythe & Hanlon 1985).
Some octopus taxa are only known from material attracted to Iights in surface waters at night - the
unresolved paralarval form 'Octopus teuthoides' is only known from a handful of micronektonic
specimens (Robson 1929, Voss 1963, Norman & Sweeney 1997). Tables 5 and 61ist planktonic and
micronektonic octopus paralarvae collected using lights at night.
Under laboratory conditions, positive phototaxis appears to be strongest at the time of hatching
and can be used to concentrate paralarvae within rearing tanks (i .e. , feeding or transferring them
to other reservoirs). Positive phototaxis appears to decrease as the paralarval octopus approaches
settlement (Villanueva 1995). However, there are no quantified studies on this subject. Fernandez-
L6pez et al. (2005) tested the influence of light intensity (1000, 3000 and 6000 lux) on the survival
and growth of captive-reared 0 . vulgaris paralarvae, obtaining the best results with the highest light
intensity treatments during daylight periods . Okumura et al. (2005a) suggest that the survival rate
of 0 . vulgaris paralarvae was negatively affected by an unstable photoenvironment in captive-bred
paralarvae exposed to variable intensities of natural light (due to cloud drift and intermittent full
sun). Changes in light tolerance throughout the planktonic stage were also observed by S. Snyder
164
Table 5 Sampling methods, number of individual s collected and abundances of Octopodidae paralarvae from the literature
Horizontal Number of
or vertical Depth Day/ individuals Geographic
Species Gear towns range (m) night collected Abundances Observations area Reference
o;l
E/edone cirrhosa Pl ankton net Np 0- 200 Np 118 Mid water or near the Higher from NEAtlantic Stephen 1944 0r
bottom, rarely at surface May to August 0
Variety of Horizontal 0--200 Np 62 Largest individuals near to Higher from NEAtlantic Collin s eta!. 0
.-<
plankton and the seafl oor May to June 2002
0
nets oblique 'TJ
towns
>-l
::r:
Emeroctopus Net 0 IOOcm Horizontal 20--760 Np 790 Higher at< 100m; to 0 .9 Found at bottom NE Pacific Green 1973 tTl
'1:1
dofteini ind h- 1 of tow depths less than r
400 ｾ＠
Ill
z
;;:;
Enterocwpus Net 0 130c m Horizon tal 0--20 over Day and l7 Absent on the surface, Collected in NW Pacifi c Yamash ita &
dofteini depths of night captured between 9 and temperatures of Tori sawa 1983 >-l
0
20--200 21 m subsurface 2.6--6.7 °C z
Conical net 0 Hori zon tal Surface Night 594 Mean of 6--8 ind by Collected from North Kubodera 1991 n
C/J
0\
lJl 130cm positive tows early June to Pacific
;p!
mid-August 0
Macrotritopus Light Undersea 15--40 Night 16 Large NEAtlantic Hanlon et al. tTl
C/J
defilippi laboratory individuals, 1980b, 1985 0
7- 15 mm ML 'TJ
Macrotritopus sp. 8 m 2 RMT Vertical 0-2000 Day and 161 96% ind collected between Represented NEAtlantic Lu & Clarke
co
tTl
and a 1-m 2 night 0 and 100m during 12% of the total 1975 (as z
>-l
ring net daylight cephalopods Scaeurgus ::r:
collected unicirrhus) n
Ocwpus cyanea 2- and 4-m' Oblique From 100 Day 388 82% collected <50 km Hawaiian Bower et al. 0
n
ring nets to surface offshore Islands 1999 >-l
0
Octopus Net 0 IOOcm Hori zolllal 20--760 Np 197 Higher at <100m; to 0.9 Found at bottom NE Pacific Green 1973 '1:1
rubescens ind h- 1 of tow depths less than cC/J
300m tTl
C/J
ROY Indi vidual s 0--400 Day 40 Higher between 300 and Individuals NE Pacific Hunt 1996
observed 400 m; to 0 .2 ind h- 1 forming shoals
observed
(continued on next page)
Table 5 (continued) Sampling methods, number of indi viduals collected and abunda nces of Octopodidae paralarvae from the literature
Horizontal Number of
or vertical Depth Day/ individuals Geographic
Species Gear town s range (m) night collected Abundances Observations area Reference
Octopus vulgaris Plankton net Np 0- 100 Np 69 Abnormal high sea Found at bottom NEAtlantic Rees 1950
temperatures assoc iated depths less than
with abundance on the 155m
northern species range
100 x 100 em Horizontal Surface Mostly 159 No specimens coll ec ted in No differences in NW Pacific Takeda 1990a ;;o
square net and diurnals surface during the day; size between
0
0
0.2--4 higher abundances inshore individuals m
;;o
from the at night and offshore collected in
bottom during day; from 0 .03 to
0.2 1 g 1000 m-3
surface or
bottom layers
-rr<
)>
Bongo net 0 Horizontal Surface Day and 641 Higher at night ; 5- 87 ind Two hatching NW Pacific Sakaguchi et al. z
60cm night 1000 m-3 peaks: spring 1999 c
m
01
and fall, higher
in fall
ｾ＠
01
Ro
Bongo net 0 Horizontal Near the Np 96 Abundance depending on NEAtlantic Gon zalez et al.
ｾ＠
75 em bottom at the strength of the upwelled 2005 )>
35- 105 water; to 8 ind 1000 m-3 ;;o
;;>':::
Bongo net 0 Horizontal Surface Day and 584 In surface during night, near Upwelling pulses NEAtlantic Otero 2007
ｾ＠
75 em and near night the bottom at day; from positively
z
the 0.0 I to I ind I000 m-3 related with 0
;;o
bottom at para larval
ｾ＠
36- 85 abundance )>
Octopodidae 8-m' RMT Oblique 0-300 Np 1439 Abundant in coastal bays Octopodidae SW Atlantic Rodhouse et al. z
and Bongo represen ted 1992
60-cm0 60% of total
cephalopods
Octopodidae Li ght trap Drifting 0-20, few Night. 2066 Higher in subsurface of Octopodidae Great Molt sc hani wskyj
and at 100 around Great Barrier Reef represented Barrier & Doherty
anc ho red new Lagoon , low on the shelf; 53 % of total Reef 1995
li ght traps moon 0.07-5.57 ind h- 1 cephalopods
Note: ML, mantle length; Np, not provided; RMT. rectangular mid water trawl ; ROY, remotely operated vehicle.
Table 6 Examples of large Octopodidae individuals collected or observed on the water column
or surface
Measured
fresh or Geographic
Species Size preserved Gear Depth (m) area Reference
Amphiocropus 13-15 mm ML F Light 21, under NW Atlantic Hanlon et al.

burryi surface 1980b
16mm ML F Light Surface NW Atlantic Forsythe &
Hanlon 1985
Cal/isroctopus 27 mm TL p Trawl Np NEAtlantic Rees 1955
macropus
Eledone 29 mmTL p Plankton net Np NEAtlantic Rees 1956
cirrhosa
Enteroctopus To 14mmML p Net 0 100 em 20-760 NE Pacific Green 1973
dojfeini 33-73 mm TL p Larval net Surface NW Pacific Yamashita 1974
To 14mmML p Conical net 0 Surface N Pacific Kubodera 1991
130cm
Eua.xoctopus II mmML, p IKMT 0-500 CentralE Nesis & Nikitina
panamensis -43 mmTL Pacific 1991
Macrotritopus 12-15 mmML F Light 15-40, under NW Atlantic Hanlon et al.
defilippi surface 1980b, 1985
1.3-11 mmML p Bongo net 0-200 Atlantic and Nesis & Nikitina
Indian 1981
Oceans
Macrotritopus 9-13.5 mm ML F Plankton net 100-300 Mediterranean Joubin &
sp. and Atlantic Robson 1929
(as M. danae)
2.5-10 mm ML F RMT & ring 0-100 NEAtlantic Lu & Clarke
net 1975(as
Scaeurgus
unicirrhus)
127 mm TL F Li ght 0-38, under Hawaiian Brower 1981
surface Islands
Octopus 15-25 mm ML p IKMT 0-770 NE Pacific Young 1972
mbescens (as Octopus sp.)
Not measured Observed 60 min an NE Pacific Present study,
from ROV area of see Figure 44
728 m depth
·octopus To 16mmML p Light Surface Central E Norman &
teuthoides · Pacific Sweeney 1997
Octopus 50 mmTL F? Light Surface Medite rranean Sparta 1933
ｶｵｬｧ｡ｲｩＮｾ＠
Octopodidae 14 mm ML p Surface Hawaiian Berry 1914

56 mmTL Islands
Note: F, measured fresh; IKMT, Isaacs-Kidd midwater trawl; ML, mantle length; Np, not provided; P, measured preserved;
RMT, rectangular midwater trawl; ROV, remotely operated vehicle; TL, total length.
167
(unpublished manuscript) in captive-reared Enteroctopus dofleini. Light intensity was reduced dur-
ing the second half of the planktonic phase because high light levels resulted in premature settlement
for a large number of individuals. Light seems to play an important role in the predatory behaviour of
octopus paralarvae although light may not be essential for capturing prey in 0 . vulgaris hatchlings
(Marquez et al. 2007). The behaviour and activity patterns of octopus paralarvae in the absence of
light (or in low light levels) are practically unknown and require detailed research. Tateno (1993)
suggested that ultrasonography can be used in the laboratory as a non-invasive technique to record
octopus paralarval activity in total darkness. This technique may offer new insights .
It must be noted that all behavioural observations of captive octopus paralarvae are severely
limited by the removal of a critical attribute of the natural environment of these animals- a realis-
tic water column . Rearing tanks severely lim it the capacity of the octopus para larvae to adju st their
depth in response to experimental factors such as changing light levels, prey, predators and tidal or
lunar cycles. For example, natural variability in light levels may be at significantly lower levels than
in experimental situations such as full sunlight on shallow rearing tanks.
Immediately following settlement, octopuses show strong negative phototaxis and reclu-
sive behaviour, as observed under laboratory conditions in Octopus vulgaris (ltami et al. 1963,
Villanueva 1995) and 0. cyanea (Wells & Wells 1970), a behaviour that is more typical of adult
benthic octopuses. There are exceptions, however, because some octopuses possess ambiguous pho-
totactic behaviour. During the early post-settlement period , Sparta (1933) collected relatively large
juveniles of 0 . vulgaris (50 mm in total length) at night using surface lights in the Strait of Messina,
Mediterranean Sea. Adult benthic octopuses will also swim towards surface lights at night, as has
been observed for Callistoctopus aspilosomatis on the Great Barrier Reef (R. Fitzpatrick personal
communication 2005, A. Harcourt personal communication 2007) and sometimes in large num-
bers, as for an undescribed species of Callistoctopus in New Caledonia (G . Boucher persona l com-
munication 1997).
Defences
Relatively high swimming speed may prevent paralarval capture by some predators. Bursts of jet
swimming in 0. vulgaris paralarvae can reach a mean swimming speed of 41-95 mm s- 1 at age of
0 and 60 days , respectively, covering a mean distance of 6-23 mm , respectively. Swimming paths
in hatchling 0. vulgaris are highly rectilinear in comparison with older paralarvae and may maxi-
mize dispersion of the individuals from the egg mass and minimize attraction of predators to the
hatching site (Villanueva et al. 1996). In large paralarvae of Macrotritopus defilippi, inking and fast
backward jetting have been observed as a response to the approach of divers, with 0.5-m traverses
per jet outswimming a diver over 3 m of distance, followed by slow backward swimming to the
seafloor (Hanlon et al. 1985).
In the open ocean, the most common form of defence by octopus paralarvae is likely to be a
dive response, into the relative safety of deeper darker waters. Such behaviour has been observed
in Macrotritopus defilippi (Hanlon et al. 1985), en masse for large Octopus rubescens paralarvae
in Monterey Bay, California, in response to the approach of a deep-water remotely operated vehicle
(ROY) (Hunt 1996) and for unidentified octopus paralarvae in the Coral Sea (M.D. Norman personal
observation). This escape response is common to many pelagic, shelled molluscs (both veliger larvae
and holopelagic pteropods) (Lalli & Gilmer 1989). In these molluscs, retraction of locomotory wings
or ciliated podia combines with shell weight to enable rapid sinking. Because they have a lower spe-
cific gravity, octopus para larvae use funnel jetting as additional propulsion to aid rapid descent.
When the proportionally large and simple chromatophores of octopus para larvae are contracted,
the animals become nearly transparent, all except for the eyes, ink sac and visceral mass. These
opaque organs are typically bound within a silvery membranous layer containing reflective irido-
phores. This combination of transparency and reflective body organs is a camouflage adaptation for
168
life in the water column of open ocean where animals are vulnerable to visual predators that detect
prey by looking for silhouettes or outlines. Transparency is a remarkable characteristic of many
oceanic zooplankton, an attribute uncommon in other aquatic habitats. It is generally accepted that
transparency is a successful form of camouflage from visual predators and/or prey in the optically
featureless pelagic environment (Johnsen 2001).
Behavioural responses of planktonic Octopodidae to predators have not been recorded in the
field or laboratory. Chromatophores and ink sac are fully functional in octopus paralarvae from
hatching. Chromatophore patterns may be used in concert with ink release to distract potential
predators, as occurs in adult octopuses (Hanlon & Messenger 1996). Octopus paralarvae are likely
to be particularly vulnerable to predation during prey capture because their motion is slowed and
their attention is focused on prey. At this time, detection of potential predators may be lessened
or suspended. During prey capture sequences, octopus paralarvae expand their chromatophores,
changing to a dark coloration (Hermindez-Garcfa et al. 2000), and perform a range of different
swimming motions when focusing on the prey (Villanueva et al. 1996). These behaviours may
increase the visibility of the para larvae to predators (see Figure 30).
Dark colouration may be used in concert with ink injection. As a series of ink decoys is released
by a fleeing dark paralarva, rapid transformation to a transparent form with a rapid shift in trajec-
tory may deceive or confuse a visual predator (Boletzky 1987). This behaviour is called a blanch-
ink-jet manoeuvre and is found in many cephalopods (Hanlon & Messenger 1996). A pursuing
predator continues the chase trajectory and finds itself in empty water. Functional ink ejection has
been observed in captive hatchlings, such as Enteroctopus dojleini (Yamashita 1974, Gabe 1975,
Okubo 1979), Octopus cf tetricus (loll 1978) and 0. laqueus (Kaneko et al. 2006) and in the wild for
Macrotritopus defilippi (Hanlon et al. 1985) and in unidentified paralarvae (M.D. Norman personal
observation) in response to the approach of divers.
Potential schooling behaviour has been reported for the micronektonic paralarvae of one spe-
cies, Octopus rubescens, off Monterey Bay, California (Hanlon & Messenger 1996). Figure 44
shows such an aggregation, photographed from a deep-water ROY in this region. Hunt (1996)
reports high densities of paralarvae of this species at depths of 200-400 m. It is unclear whether
this is a potential defensive behaviour, an artefact of water column aggregations within the layer
of vertically migrating zooplankton known as the 'scattering layer' (see p. 175) or offers some
enhanced feeding success.
Figure 44 (See also Colour Figure 44 in the insert.) A dense swarm of Octopus rubescens with the jellyfish
(Phacellophora camtschatica) photographed 26 June 2003 at 1115h local time from the ROY YENTANA at a
depth of about 60 min 728 m of water in the Monterey Submarine Canyon, north-east Pacific. Temperature
9°C and oxygen concentration 2.66 ml 1- 1• No euphausiids were observed on the dive tape. (Image and data
reproduced with permission from Monterey Bay Aquarium Research Institute, ©2003, MBARI.)
169
Predators on egg masses and paralarvae

As brooding females of most octopus species continually guard their eggs at a fixed permanent site,
Ambrose (1988) proposed that they are more susceptible to predation. As the duration of brooding
and embryonic development increases with decreasing temperatures, winter-brooding females thus
have an even higher vulnerability to predation. Ambrose recorded 70- 100% mortality of brooding
0. bimaculatus females monitored in the wild during winter off Southern California. Moray eels
(Gymnothorax mordax) were presumed to be the primary predators. The fate of the egg masses was
unknown . The egg masses of Enteroctopus dojf.eini females that died prior to paralarval hatching
on the British Columbia coast, north-east Pacific, were eaten by the crab species Chorilia longipes,
Scyra acutifrons and Oregonia gracilis (Cosgrove 1993). Two egg strings of the same species were
also consumed by the seastar Evasterias troschelii in the presence of the live brooding female at
19 m depth in the same area (J.A. Cosgrove personal communication 2006). Nesis & Nigmatullin
( l 98 l) reported egg masses of Eledone caparti from stomach contents of three blue sharks Prionace
glauca (169-182 em length), collected off Dakar and Cabo Verde. Under aquarium conditions,
eggs of Macroctopus maorum have been preyed on by the fissurellid gastropod, Scutus breviculus
(Batham 1957).
Brooding females of octopus species that carry their egg masses, such as Hapalo chlaena (Dew
1959, Tranter & Augustine 1973, Norman 2000), Wunderpus photogenicus (Miske & Kirchhauser
2006), Amphioctopus burryi (Forsythe & Hanlon 1985) and Macrotritopus dejilippi (Hanlon et al.
1985) may be able to escape or hide from predators, suggesting a possible advantage over species
that attach egg strings at a permanent site. However, in order to protect egg masses and themselves
from predators , brooding females can partially or completely barricade the permanent spawning
shelter with rocks or shells (Wodinsky 1972, Ambrose 1988, Anderson 1997) or close bivalve shells
from within (Eibl-Eibesfeldt & Scheer 1962).
In open oceanic waters, pelagic fishes are the main predators of octopus paralarvae. Longnose
lancetfish (Alepisaurus ferox) actively prey on pelagic cephalopods, including octopus para larvae.
Stomach contents for this species examined from around the Pacific Ocean (Rancurel 1970) included
seven individuals of Macrotritopus forms (6.5-18 mm ML) from the south Pacific (16°-23 ° S); three
'Octopus teuthoides' forms (18-25 mm ML) from East Tonga Islands, south-west Pacific a nd one
individual of the same species (28 mm ML) from West Midway Islands, north-west Pacific; and
six unidentified and unmeasured planktonic Octopodidae. Stomach analysis of Alepisaurus ferox
from Suruga Bay, north-west Pacific, found 68 individuals of Octopus sp, ranging in size from 7
to 23 mm ML, of which 69% were 8-16 mm ML and collected mainly during March (Okutani &
Kubota 1976). In total, octopus paralarvae (Octopodidae) were present in l l% (Rancurel 1970)
or 12.5% (Okutani & Kubota 1976) of the A. ferox stomachs containing cephalopods. Octopod
paralarvae not sorted by families occurred in 3% of the stomachs of this fish in western equato-
rial Indian Ocean (Potier et al. 2007). The albacore (Thunnus alalunga) is an active predator of
pelagic and planktonic cephalopods. Stomach contents of this species collected in the north-east
Atlantic during July and October included seven young Eledone cirrhosa (21-33 mm total length)
in localities near Cape Finisterre and five Octopus vulgaris (6.5-18 mm total length) collected in
the Gascogne Gulf during August and October (Bouxin & Legendre 1936). Parker et al. (2005)
reported unidentified cephalopod paralarvae in the diet of oceanic loggerhead sea turtles (Caretta
caretta) in the central north Pacific. All proved to be octopodid paralarvae (D.M. Parker personal
communication 2006). Ephyra larval stage of jellyfish scyphomedusae has been observed feeding
on unidentified octopod paralarvae (Figure 45) from plankton samples collected off Lizard Island,
Great Barrier Reef (P. Parks personal communication 2007).
In littoral waters, fishes are also expected to be the main predators of octopus paralarvae but, as
far as we know, no references on this subject have been published and information only comes from
170
Figure 45 (See also Colour Figure 45 in the insert.) Ephyra larval stage of jellyfish scyphomedusa feeding
· on unidentified octopod paralarva. Specimens collected using a plankton net at about 180m depth, off Lizard
Island, Great Barrier Reef. (Data and image reproduced with permission from Peter Parks/imagequestmarine.
com.)
opportunistic personal observations. Fishes are attracted to octopus egg masses during hatching
and have been observed during daytime at a short distance from the egg mass, preying on Octopus
vulgaris individuals that have hatched seconds or minutes before, as has been observed for the
Mediterranean dusky grouper (Epinephelus marginatus) at 10-15 m deep in the Medes Islands,
north-west Mediterranean (R. Coma personal communication 2006); serranid fish (Serranus sp.) at
15m depth on the Rfa de Vigo, north-east Atlantic (A. Guerra personal communication 2007); and
the sand smelt (Atherina presbyter) that preyed on hatchlings from egg masses placed in floating
cages for Octopus vulgaris ongrowing aquaculture in the Ria de Yigo, north-east Atlantic (J. Iglesias
personal communication 2007).
Cannibalism has not been observed in captive rearing of octopus paralarvae. Under laboratory
conditions, attacks on conspecifics have been reported for 0. vulgaris paralarvae (Boletzky 1987,
Villanueva 1995). However, these attacks do not result in cannibalism, as has been observed for
juvenile and subadult benthic stages of some octopus species (i.e., Itami et al. 1963, DeRusha et al.
1987, Aronson 1989, Cortez et al. 1995b).
Species identification and diversity

Prior to the review paper of Hochberg et al. (1992), morphological descriptions and identification
tools for octopus paralarvae were few and widely scattered in the literature. A number of research-
ers such as Berry (1914), Chun (l915), Naef (1923), Degner (l925), Robson (1929) and Rees (1954)
171
along with subsequent researchers in the 1970s and 1980s descr ibed individual paralarvae a mongst
regional or broader treatments of the family. Hochberg et al. ( 1992) were the first to compile a suite
of diagnostic characters such as founder chromatophore patterns, sucker attributes, arm formulae
and body shape.
Table l lists those species of the family Octopodidae that are known (or presumed) to produce
planktonic paralarvae. Three categories of species are listed: (1) those for which planktonic para-
larvae have been described from laboratory-hatched individuals, (2) those with small-type eggs
(i.e., egg length typically less than 10% of ML), and (3) species for which the eggs in the submature
ovary can be estimated as being of the small-egg type produced in large numbers (versus large-type
eggs produced in low numbers). The first category typically results from captive studies in which
eggs hatch and young paralarvae are described. The second category typically comes from studies
of preserved material for which laid eggs or mature ovarian eggs form the basis of the egg-type
discrimination (sensu Boletzky 1977a, 1978-1979). The third category comes from dissection of
preserved submature females as the only material available to provide any indication of early life-
history strategy.
In only a few studies have paralarval forms been successfully raised through to settlement,
enabling identification of the post-settlement form. A good example is the 'Macrotritopus' prob-
lem. In 1922, a distinctive paralarval form with greatly elongated third arms formed the basis of
the generic name Macrotritopus Grimpe, 1922. On the basis of apparent left-handed male sex ual
modification (hectocotylization) in one specimen, Rees (1954) attributed all reports of thi s paralar-
val form to the seamount and continental slope genus, Scaeurgus. In parallel studies in the United
States (Hanlon et al. l980a, 1985) and Soviet Union (Nesis & Nikitina 1981 ), Macrotritopus-type
paralarvae were raised to adulthood and identified as the long-armed species Octopus defilippi
(now treated as Macrotritopus defilippi; see Norman & Hochberg 2005a). As representatives of this
distinctive paralarval form have been found in the Pacific and Indian Oceans, where M. defiliippi is
not reported, it is possible that this distinctive paralarval form may represent more than one species
(Hochberg et al. 1992).
Other historical conundrums also await resolution . Octopus teuthoides Robson, 1929 was coined
for a distinctive elongate paralarval form that received considerable attention in subsequent litera-
ture (see Norman & Sweeney 1997, Toll & Voss 1998). The adult form, however, still awaits iden-
tification . At least 10 other octopodid taxa have been form a lly described on the basis of paralarval
or juvenile material (Norman & Hochberg 2005a). For many species of benthic octopuses , nothing
is known of egg size or juvenile stages. In combination with the many species yet to be described
by science, particularly in the tropical Indo-Pacific region (Norman & Hochberg 2005a), we can
be confident that the number of known paralarval species is far outweighed by the forms yet to be
defined/described. In regions with well-known faunas or lower diversity in octopodid species, para-
larvae are slightly better known (i.e., Mediterranean Sea and eastern Pacific off North America).
In some cases, paralarval diversity can be a clue to total species diversity of benthic octopuses
in a geographic region . F.G. Hochberg & R.E. Young (unpublished data) recog nized 16 species of
paralarvae in material collected around the Hawaiian Islands. At that stage, only eight spec ies of
benthic octopus were recorded from these islands, with some of these species being large-egg type
(see Norman & Hochberg 2005a). Hence the estimates of species number in the region appeared
to be a significant underestimate. Subsequent studies have found new small-egg species in the
region, such as Amphioctopus arenicola (Huffard & Hochberg 2005), and more await description
(F.G. Hochberg unpublished data).
A revolution is brewing, however, for the identification, description and discrimination of par-
a larval forms . With the advent of cheap, reliable and accurate DNA sequencing technolog ies and
sequence databases such as GenBank, it will be possible to definitively identify paralarvae. In
172
combination with high-resolution and accurate photography, it will enable development of compre-
hensive species identification keys for octopus paralarvae. The capacity to identify paralarval stages
will also enable a much more thorough understanding of development and morphometric changes
associated with growth and life in the plankton . Until this process is under way, some caution must
be taken with taxonomic identifications of wild-caught paralarvae because there is potential for
misidentification or oversimplification of the diversity of taxa represented in such samples.
Distribution patterns
Sampling methods
Most benthic octopus species with planktonic stages spawn in shallow, rocky or coral substra-
tum areas and consequently hatchlings can be abundant near the coast. Surveys targeting octopus
paralarvae such as Octopus vulgaris have been done in shallow bays and littoral waters (Takeda
1990a, Sakaguchi et al. 1999, Gonzalez et al. 2005, Otero 2007). Oceanic plankton sampling is usu-
ally rich in oegopsid squid paralarvae and poor in octopuses, with some exceptions. For example,
oceanic surveys in the north Pacific sampled large volumes of water and captured large numbers
of Enteroctopus dofleini paralarvae (Green 1973, Kubodera 1991). Table 5 shows literature records
of the depth ranges and different sampling methods, primarily nets and light traps, used to collect
octopus paralarvae.
Classic bongo nets, conical nets of different sizes, Isaacs-Kidd midwater trawls (IKMTs) and
rectangular midwater trawls (RMTs) have been used to collect octopus paralarvae (see Table 5).
Piatkowski ( 1998) reviewed the ad vantages of targeted sam piing using modern opening/closing nets
and discussed problems such as net speed and net avoidance by cephalopod paralarvae. The strong
positive phototaxis of octopus paralarvae (see 'Responses to light and gravity', p. 163) has been used
during night surveys to attract and collect large para larvae inhabiting surface or near-surface waters
(see Table 6). Light traps proved to be a powerful method for collecting large numbers of octopus
paralarvae (Moltschaniwskyj & Doherty 1995) but little is known of their sampling efficiency, sam-
pling bias due to water clarity and species-specific capture selectivity. An advantage of this method
is the collection of live animals in excellent conditions for experimental work. For example, Hanlon
et al. (1980a, 1985) resolved the 'Macrotritopus' taxonomic problem (see also Nesis & Nikitina
1981) by collecting live 'Macrotritopus' paralarvae individuals using light and rearing them to the
adult stage in the laboratory, where they were identified as Macrotritopus defilippi.
Geographic range
Total geographic range of paralarvae of benthic octopuses is poorly known for most species. As
for many attributes of octopus paralarvae, it is probably best known for Octopus vulgaris and
Enteroctopus dofleini (see Table 5). Taxonomic problems for the family Octopodidae are suffi-
cient that accurate distributions for adult octopuses are not available for most species (Norman &
Hochberg 2005a), let alone for paralarvae. Greater resolution may become possible when molecular
tools enable accurate species identifications and hence collation of accurate geographic distribu-
tional data.
The greatest geographic range for octopus paralarvae is likely to occur for widely distributed
Indo-West Pacific coral-reef species such as Octopus cyanea and Callistoctopus ornatus. These
small-egg species have distributions spanning two thirds of the globe's circumference (Norman
1991, 1993). Van Heukelem (1973) reported captive Octopus cyanea paralarvae that lasted in the
water column for 21 days before dying. Norman (1991) suggested that the paralarval stage would
173
have to be significantly longer for this species (up to months , as has been recorded for the similar
0. vulgaris paralarvae; see Table 3) to explain the gene flow necessary between the widely spaced
coral-reef habitats in the tropical Indian and Pacific Oceans.
At this stage, there are no reports of octopus paralarvae from polar regions. Benthic octopuses
at these high latitudes exclusively produce large-egg hatchlings as in Benthoctopus (Nesis 2001),
Bathypolypus (Muus 2002, Barratt et al. 2007) and Pareledone (Allcock 2005), as do many other
polar marine invertebrates that show high parental investment in a few, large and well-developed
young (i.e., Poulin & Feral 1996). The largest planktonic hatchlings in the family Octopodidae
belong to the genus Enteroctopus (see Table 4), cold-adapted species distributed in high latitudes.
E. dojleini is distributed from littoral depths to more than 1500 m (Hartwick 1983, Hochberg 1998)
and Kubodera (1991) collected E. dojleini paralarvae in the north Pacific at almost 57°N in the
Bering Sea. Enteroctopus megalocyathus of South America has the largest planktonic hatchlings
described and their morphometries and behaviours are ambiguous between pelagic and benthic
modes of life (Ortiz et al. 2006) (see 'Swimming behaviour of planktonic paralarvae', p. 161). In
common with the Octopodidae of high latitudes, deep-sea benthic octopuses produce large eggs and
have benthic hatchlings (Voss 1988). The notable exceptions appear to be members of the middepth
genera Scaeurgus and Pteroctopus (Table 1), which have small-type egg sizes and for which little is
known of their paralarvae (Bello 2004).
Horizontal dispersal
Horizontal movement dictated by oceanographic conditions in upwelling areas has been suggested
to be of great importance in the distributions of Octopus vulgaris paralarvae (Demarcq & Faure
2000, Faure et al. 2000, Gonzalez et al. 2005, Otero 2007). Upwelling intensity may act as a limiting
factor, generating periods of coastal water retention, potentially beneficial for nutrient enrichment
processes. These periods generate low, horizontal larval dispersion off shore in some zoological
groups (Cury & Roy 1989). Using oceanographic models, Demarcq & Faure (2000) and Faure et al.
(2000) hypothesised that in the Arguin Bank, influenced by the West African coastal upwelling
system, the periods of high retention indices generated during spring benefits planktonic 0 . vulgaris
paralarvae by limiting offshore paralarval dispersion . Faure et al. (2000) suggested that offshore
paralarval dispersion can be a negative factor in paralarval survival due to the wind-induced break-
down of the retention areas during autumn.
These hypotheses were partially corroborated by Gonzalez et al. (2005) and Otero (2007), who
found that high abundances of 0. vulgaris paralarvae were correlated with high upwelling retention
indices in the north-west Iberian coast, the northern limit of the Canary current. However, nearly
all paralarvae collected by these authors were individuals with three suckers per arm, suggesting
that they were hatchlings incorporated into the relatively low-turbulence water mass . The effect
of upwelling intensity on fish and invertebrate larval distributions varies with the behaviours and
vertical distributions of the larvae, and careful sampling is necessary to determine the contribution
of upwelling to the offshore transport of larvae as a cause of variations in larval settlement levels
(Shanks & Eckert 2005, Shanks & Brink 2005).
The paralarvae of species with large hatchlings such as Enteroctopus dojleini seem to be dis-
tributed in both shallow and oceanic waters, having been found off shore in the north-east Pacific
Ocean in higher abundances between the surface and 100m over bottom depths of <200m (Green
1973), as well as over the continental shelf in the north-west Pacific Ocean (Yamashita & Torisawa
1983). However, significant numbers of E. dofieini paralarvae have also been encountered in more
distant offshore waters (200-300 miles from the coast) and collected I h after sunset in surface
waters along the Aleutian Islands and southern Bering Sea (Kubodera 1991). Selective tidal transport
174
can also influence the distributions and densities of prey such as crustacean zoeae (Forward &
Tankersley 2001) and is expected to influence the distributions of octopus paralarvae, as has been
observed in other shallow-water and bottom-spawning cephalopods such as loliginid paralarvae
(Zeidberg & Hamner 2002).
Vertical distribution and abundances

Few studies have recorded vertical daily cycles of octopus paralarvae, most being focused on
Octopus vulgaris. In shallow coastal waters, paralarvae of this species are nearly absent from the
sea surface during daytime and present from the seafloor to the surface at night, with higher abun-
dances of hatchlings (easily recognized by their three suckers per arm) found near the surface
at night (Takeda 1990a, Sakaguchi et al. 1999, Otero 2007) (Table 5). The hatchling individuals
probably come directly from egg masses in the rocky substrata of the shallow waters sampled. Die!
changes in the open ocean and for older paralarvae are practically unknown and need to be investi-
gated through use of high-resolution discrete-depth sampling.
Sampling between 0 and 2000 m depth in the north-east Atlantic, Clarke & Lu (1975) col-
lected the highest number known to date of Macrotritopus paralarvae (n = 161). Most (73%) of
Macrotritopus sp. collected were concentrated between 0 and 50 m depth and no die! migration was
detected. However, some vertical movements to deep waters may exist because Rees (1954) reported
a Macrotritopus individual collected between 800 and 1500 m, Clarke (1969) noted an individual
collected between 460 and 510 m and Clarke & Lu (1975) recorded one specimen between 1000
and 1250 m depth.
Qualitative observations of paralarval numbers at night in the open ocean of the Coral Sea
found much higher numbers of octopus paralarvae on moonless nights compared with moonlit
nights (M.D. Norman personal observation). Hunt (1996) found that Octopus rubescens paralarvae
were most abundant at depths of 200-400 min Monterey Bay, California. This may correspond to
the daytime depth ranges of the vertically migrating gelatinous zooplankton layer, visible on ship
depth sounders and defined as the 'scattering layer' by Eyring et al. (1948).
Vertical movements are suspected to be important for retention of para larvae over settled areas
like seamounts for deeper-water species such as Scaeurgus unicirrhus. Paralarvae presumably
belonging to this species have been collected from the Great Meteor Seamount, north-east Atlantic,
the only cephalopod para larvae related to bottom-dwelling adults collected over this seamount
(Diekmann et al. 2006). Endemism and seamount associations of members of this genus have been
discussed elsewh.e re (Norman et al. 2005).
Factors influencing differences in abundances between hatchlings and older paralarvae are
poorly known. Only 7% of 643 Octopus vulgaris paralarvae collected by Sakaguchi et al. (1999)
had more than three suckers per arm(= sucker number at hatching; see Table 4), and only 4% of 780
Enteroctopus dojleini individuals collected by Green (1973) in oceanic waters were >6 mm ML. In
the first instance, the abundance of small animals suggests that mortality rates are higher during
the early paralarval stages. However, other factors cannot be discounted . Diversity in sizes may be a
product of cohorts with differing growth rates, as has been observed in same-age cohorts of several
octopus species (Van Heukelem 1976, Forsythe 1984). Horizontal displacement of older paralarvae
and/or net avoidance by these larger paralarvae with faster swimming speeds and higher sensory
development may also be a factor.
The potential influence of sensory systems on paralarval distributions is unknown. For exam-
ple, the use of sound by cephalopod paralarvae as an orientation cue in relation to reefs cannot be
excluded, as has been observed for reef fishes and crustacean larvae (Montgomery et al. 2006), poten-
tially influencing their settlement distribution. Octopuses have well-developed mechanoreceptors
175
analogous to the receptors of fishes (see 'Sensory systems' section, p. 126), capable of detecting low
frequencies; however several studies suggest that cephalopods cannot detect underwater sound or
vibrational stimuli much above 100Hz (Packard et al. 1990, Budelmann et al. 1997).
Relationships between paralarval and adult populations

Seasonal reproduction patterns of each species will dictate the presence of the different paralarvae
in the plankton throughout the year. Maximum abundances of Octopus vulgaris paralarvae are
recorded during summer and autumn (Rees 1950, Rees & Lumby 1954, Takeda 1990a, Sakaguchi
et al. 1999, Gonzalez et al. 2005, Otero 2007), corresponding to spawning peaks of 0 . vulgaris in
temperate regions that are in spring and early autumn (Mangold 1983). The warm coastal waters in
autumn accelerate embryonic development (see 'Egg care and duration of embryonic development',
p. I LO) for the last of the spawnings, after which young paralarvae of this species will practically
disappear from the plankton during winter and spring.
Variability in life span and growth in benthic octopuses with or without planktonic stages is
influenced by many factors, of which temperature is probably the most important (Semmens et al.
2004). In benthic octopuses with planktonic stages, under laboratory conditions, the duration of the
life cycle including embryonic development ranges from 6 to 12 months in pygmy octopuses such
as 0. joubini (Forsythe & Toll 1991), nearly I yr in 0. vulgaris (Iglesias et al. 2004) and 3.5 yr in
the large cold-adapted species Enteroctopus dojleini (S. Snyder unpublished manuscript). In the
short-lived species, pulses of recruitment can be related directly between young stages and adults
of the following year. For a few species, there is some support for a relationship between the suc-
cess of the paralarval population and adult abundances. After a 6-yr field study, Ambrose (1988)
concluded that the primary regulatory processes of a subtidal population of Octopus bimaculatus
in the north-east Pacific Ocean appeared to take place in the paralarval and juvenile stages. The
importance of early stages was supported in Ambrose's study by heavy recruitment of settled indi-
viduals in I yr leading to unusually high adult octopus densities in the subsequent year. Relatively
large 0. vulgaris paralarvae (to 6 mm ML) were collected by Rees (1950) and Rees & Lumby (1954)
in the English Channel. These authors concluded that periodic 'plagues' of 0. vulgaris during warm
years along the south coast of England (the northern limit of distribution of the species in the north-
east Atlantic) resulted from the transport of the paralarvae during the summer months across the
English Channel from southern hatching areas. In coastal upwelling areas of West Africa, catches
of adult 0. vulgaris during summer are significantly correlated with the upwelling intensity during
the previous winter, indicating the influence of oceanographic conditions on octopus para larvae and
juveniles and the subsequent effects on the fished adult populations (Caveriviere & Demarcq 2002).
In the same region, exceptional oceanographic conditions favouring paralarval and juvenile sur-
vival also seem to be the origin of demographic explosions of 0. vulgaris (Caveriviere 1990, Diallo
et al. 2002). A similar relationship between upwelling intensity and adult catches has been found
in the north-west Iberian coast (Otero 2007). These data suggest that populations of planktonic
octopuses may benefit from particular oceanographic conditions, as has been observed for loliginid
paralarvae (Vecchione 1999, Zeidberg & Hamner 2002).
The settlement process

After a period of constant swimming that ranges from 3 wk to 6 months (depending on the species; see
Table 3), planktonic octopuses undergo a transitional period from a pelagic lifestyle to the predomi-
nantly benthic life of the juvenile stage. The end of the planktonic para larval period in octopuses is not
always abrupt as it is in many other benthic invertebrates with planktonic larval forms. There seem to
be three presettlement strategies, dependent on the species and/or the environmental context:
176
I. Species with a short presettlement period. After a short period in contact with hard surfaces
and benthos, paralarvae of these species definitively settle to the seafloor at relatively small
sizes. These young octopuses, considered as juveniles from this point onwards (sensu Young
& Hannan 1988), live on the benthos and have similar habits to that of the adults. From an
ecological point of view, at this stage the young animals are equivalent to the hatchlings
of large-egg octopus species that immediately adopt a benthic habit on hatching. A typical
example of such species is 0. vulgaris (Villanueva 1995, Nixon & Mangold 1996).
2. Species with an expanded, transitional presettlement period. In these species, a strict
benthic life is gradually adopted, split between swimming and benthic crawling. These
paralarvae can reach a relatively large size in the water column and the animals seem
to live in contact with both the benthos and the water column, as has been suggested for
Macrotritopus defilippi in the western Atlantic (Hanlon et at. 1985) and for Amphioctopus
burryi (Forsythe & Hanlon 1985).
3. Species with a prolonged/suspended paralarval state. Certain paralarvae reach consider-
able sizes, particularly those occurring in oceanic epipelagic waters. Due to their size
and swimming capacities they can be considered micronektonic paralarvae. These para-
larvae have been described as 'extended pelagic stages' (Rees 1954) or 'super-paralarvae'
(Strugnell et at. 2004) and have been suggested to be individuals that delay settlement
due to the absence of suitable habitat, i.e., shallow reefs (see 'Prolonged para larval stages:
micronektonic paralarvae', p. 182). It is also possible that the swimming capacities, behav-
iour, and the well-developed sensory systems of these micronektonic paralarvae may be
used to actively remain in the epipelagic realm , effectively delaying settlement in order to
exploit resources in this habitat.
The physiological processes and environmental cues that govern the settlement metamorpho-
sis have not yet been described . Only external morphology and behavioural characters have been
reported for this period of dramatic ecological change.
Morphological characteristics at settlement

Major ex ternal morphological changes associated with the settlement process are positive allomet-
ric arm growth, the addition of new suckers, chromatophore, iridophore and leucophore genesis , the
development of skin sculptural components and a horizontal pupillary response. At the same time,
animals appear to lose the Kolliker organs that cover the body surface and the 'lateral line system'
formed by the epidermal lines located on the arms, head, anterior part of dorsal mantle and funnel.
These structures have not been reported for adult benthic octopuses (Budelmann et at. 1997). A
more minor morphological change is the loss of the oral denticles of the beaks. This transformation
is also reflected in changes in the relative sizes of the various lobes of the paralarval and juvenile
brain (see 'Central nervous system', p. 126).
Positive allometric arm growth

From a hydrodynamic point of view, hatchling octopus paralarvae have a squid-like form that
gradually changes to the typical octopus form after settlement, due primarily to the notable arm
growth . Benthic juveniles and adult octopods have a relatively small mantle cavity volume and have
to produce high ventilation pressures to generate the necessary thrust for locomotion when they
swim. These morphological constraints appear gradually throughout the planktonic phase and it
is expected that they would progressively dictate the locomotion capacities of the paralarvae and
juveniles. As proposed by Wells (1990), cephalopods will try to escape using jet locomotion when-
ever possible, particularly adult octopus. During jet propulsion, Wells et at. (l983b, 1987) found
177
that the hearts of benthic octopuses cease beating, resulting in oxygen debt, as the venous system
is incapable of retuning blood aga in st the gradients produced by the rise in internal mantle pres-
sure. This makes jet swimming impossible as a regular mode of locomotion for benthic octopuses.
At the end of the planktonic phase, the growth of the arm crown and the expected increase in the
internal mantle pressure necessary for jet swimming have been suggested as factors that may in sti-
gate settlement in Octopus vulgaris (Villanueva et al. 1995, 1996). For micronektonic forms such
as Callistoctopus sp., this energetic problem may be solved by adopting the hydrodynamic form of
squids with an elongate, large mantle that enables locomotion by jet swimming in the epipelagic
realm , potentially delaying settlement (see Figure 43).
Under laboratory conditions, presettlement reflexes of Octopus vulgaris paralarvae commence
when ML reaches 50% or less of the total length (Villanueva 1995). This relationship is similar in
Enteroctopus dofieini as settlement takes place when ML and arm length represent approximately 45%
and 55% of total length, respectively (Okubo 1979) (Figures 46 and 47). It is interesting to note that total
length of Octopus vulgaris at settlement (1 1-13 mm) is not dissimilar to that of the length of Enteroctopus
dojieini paralarvae at hatching (10 mm), a species that under laboratory conditions will settle at total
lengths of approximately 30 mm (Okubo 1979, 1980) (see Figure 48 for species comparisons).
Morphological transformations at settlement are less well known for long-armed paralarvae,
such as members of the genus Callistoctopus (e.g., Figures 4 and 43), Euaxoctopus (Nesis &
Nikitina, 1991) (Figure 5) and Macrotritopus (Rees 1954) (Figure 6). These paralarvae can develop
markedly long arms, particularly one arm pair that can reach up to three times the length of the
others (i.e., for Euaxoctopus, Nesis & Nikitina 1991). This longest arm pair corresponds to the first
pair in Callistoctopus, the second in Euaxoctopus and the third in Macrotritopus (see Figures 4-6).
Hanlon et al. (1985) postulated that the long, slender arms may be aids to flotation because they
represent a large proportion of the surface area of the animal. Chemical and morphological com-
position of these expanded arms and body musculature may be an interesting subject for further
research because the arms may be buoyant in a comparable fashion to the elongate ammonia-buoy-
ant arm pairs of squids in the family Chiroteuthidae (Voight et al. 1994). An alternative explanation
may be that this longer arm pair act as analogues of the elongate feeding tentacle pair of sq uids
and cuttlefishes. Further research on how octopus paralarvae use their two mantle cav ities (dorsal
and ventral) (see examples in Figures I B, 26, 40, 41, and 43) during the jet propulsion cycle may
80.------------------------------.
70
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0 W 40 W W 1001Wl401WlWWO
Age (days)
Figure 46 Relative decrease of mantle length (ML) as percentage of total length (TL) from hatching to
settlement during experimental rearings of Enterocropus dojfeini and Octopus vulgaris. (Data for£. dojfeini
obta ined from Okubo 1979 (dark circles) and data for 0. vulgaris obtained from Villanueva 1995 (wh ite
circles).) Initial settlement periods are indicated for both species: £. dojfeini, black arrow; 0. vulgaris. white
arrow. Original.
178
80
70
.-l
f-<
......
0
60
•• • •
if!.
..c"'
"'
50
40
t ... •• \0
0
'on
c: 30
oo
ｾ＠
0 \
E 20 0
< 10
0
0 20 40 60 80 100 120 140 160 180 200
Age (days)
Figure 47 Relative increase of arm length as percentage of total length (TL) from hatching to settlement
during experimental rearings of Enteroctopus dojieini and Octopus vulgaris. (Data for£. dojieini obtained
from Okubo 1979 (dark circles) and data for 0. vulgaris obtained from Villanueva 1995 (w hite circles).)
Initial settlement periods are indicated for both species: £. dofleini (black arrow); 0. vulgaris (white arrow).
Original.
80
E'
5
..c
50
70
60
D
'
-·
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c:
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-;;; 30
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0 W 40 W W 1001W1401W1WWO
Age (days)
Figure 48 Growth in total length from hatching to settlement during experimental rearings of Enteroctopus
dojieini and Octopus vulgaris paralarvae. (Data for£. dofleini obtained from Okubo 1979 (black circles) and
Okubo 1980 (black squares). Data for Octopus vulgaris obtained from Itami et al. 1963 (white squares) and
Villanueva 1995 (white circles).) Initial settlement periods are indicated for both species: £. dojieini, black
arrows; 0. vulgaris, white arrows. Original.
also shed light on the poorly known hydrodynamic and energetic adaptations of sw imming in these
long-armed paralarvae.
Chromatophore genesis and new skin sculptural components

After a nearly transparent life in the plankton, recently settled octopuses develop a dense net of
chromatophores, particularly on the dorsal surfaces, which help the animal in camouflage on the
seafloor and that develop into body patterns resembling those of the adults. As noted by Packard
(1985, p. 293): "The dorsal spurt in chromatophore genesis at the end of the planktonic phase is so
dramatic as to hint at something like metamorphosis. It is as if the skin were waiting for its owner
to settle on the seafloor before bringing out the fine-grain dress that is going to serve for the rest of
its life, and replace the coarse-grain set of extra-tegument spots (on the surface of the viscera) that
179
served during the transparent planktonic phase." All the founder chromatophores of para la rvae can
be identified in recently settled individuals and are assumed to remain functional. However, they
were never expanded during the extensive photographic surveys of Packard, who suggested that they
may belong to planktonic, rather than benthic, camouflage patterns. Kolliker organs are prese nt on
the skin of recently settled individuals (Villanueva 1995) and probably disappear relatively quickly.
It is unknown at which stage these animals completely lose the Kolliker organs. The presence of
these organs has not been reported in the literature for later-stage juveniles or adult octopuses. At
settlement, other chromatic components also develop, including epidermal iridophores and leu-
cophores. This transformation has not been described in detail and requires further research.
For many species, the sculptural components of the skin also undertake a dramatic transforma-
tion from the relatively smooth paralarva to highly sculptured, benthic animals (Figure 16). Papillae,
flaps, ridges, patch and groove skin texture, and the lateral mantle ridge are all sculptural features of
post-settlement juveniles and adults. In some species, papillae in the skin can be dramatically raised
(complete with side branches) to form a rugose or even hairy appearance, as occurs in members of
the genus Abdopus (Norman & Finn 2001).
Horizontal pupillary response

In line with many pelagic cephalopods, octopus paralarvae possess a circular pupil (see examples
in Figures IB, 3, 4 centre, 26, 41). In contrast, adult benthic octopuses have a horizontal pupillary
response to light intensities: when exposed to bright light the pupil form s a horizontal slit, while
the dark-adapted pupil is close to circular, as observed in Octopus vulgaris and Eledone cirrhosa
(Muntz 1977, Douglas et al. 2005) (see also Figure !C). A horizontal pupil is present in octopus
hatchlings of directly benthic species (see Figure IC ,D). The horizontal shape of the pupil correlates
with the longest rhabdomes found in the central retina, where they form an equatorial strip (Young
1963). This adaptation may be related to a benthic mode of life so that objects in the seafloor/water
interface can be better discriminated (Muntz 1977). In other cephalopods that live in the water
column, such as Loligo pealei, the central retinal strip is absent (Young 1963). In Enteroctopus
dojleini reared from planktonic hatchlings, the horizontal slit of the pupil was observed only in ben-
thic individuals older than 8-9 months (S. Snyder unpublished manuscript). Quantification of these
observations is necessary, however, because the constant circular pupil s of planktonic octopuses
contrast with the alternative choices of circular or horizontal shapes depending on light intensities,
observed when individuals move to the substratum after settlement.
The prese nce of a horizontal pupil in paralarvae that are still present in the micronekton has
only been observed in several live photographs of larger animals (e.g., Figure 4 bottom). The pres-
ence of this feature may represent animals close to settlement, animals in a transitional phase during
which they are spending time split between swimming and benthic crawling, or be an attribute of
delayed settlement (see 'Prolonged paralarval stages: micronektonic paralarvae', p. 182).
Behavioural and ecological characteristics at settlement

The shift from a planktonic to a benthic life implies that the adaptations necessa ry for thi s change
are attained by the octopuses over a relatively short time. It is also assumed that octopuses settle to
the seafloor. However, they have also been found to use other hard surfaces, including the underside
of buoys set over 64 m of water (Wells & Wells 1970), surface flotsam (Smale & Buchan 1981) and
have taken on a role as epifauna covering floating cages for fish culture at more than 25 m deep
in the Mediterranean Sea (R. Villanueva personal observation). Most descriptions of settlement
behaviour come from laboratory experiments. These are typically characterized by high peaks of
mortality during these periods , at least for Octopus vulgaris (V illanueva 1995, Iglesias et al. 2004,
Carrasco et al. 2006), for which cannibalism has also been observed immediately after settlement
180
(Itami et al. 1963). These findings indicate that laboratory settlement requirements are poorly
understood and need to be improved. The natural settlement process is probably modified under
laboratory conditions, potentially accelerating settlement through factors such as (I) the physical
limits imposed by the size of normal rearing tanks, preventing possible movement within the water
column , (2) light intensity and (3) the prior feeding history of the reared paralarvae, which are
usually indirectly trained to receive food during laboratory daylight periods. Octopuses collected
from floating structures in the wild (Wells & Wells 1970) or from ROVs in the water column (Hunt
1996) become exclusively benthic when transferred to rearing tanks. However, in some species
such as Amphioctopus burryi, relatively large individuals of 0.8-1.2 g wet weight collected from
the sea surface at night showed both pelagic and benthic behaviour in the laboratory, swimming in
the water column at night and living on the substratum by day (Forsythe & Hanlon 1985). Large
Macrotritopus-type paralarvae have also been found to be benthic during the day and pelagic at
night (Hanlon et al. 1985). This behaviour is suspected to be common in many species. Kanamaru
(1964) reported a mix of planktonic and benthic organisms (shrimp and crab larvae and flatfish
remains) in the gut contents of a juvenile Enteroctopus dofleini, 51 mm in total length, suggesting
this migratory capacity. Relatively large Octopus vulgaris paralarvae (II mm ML) have been col-
lected from the plankton (Degner 1925, Rees 1953).
In laboratory experiments, presettlement individuals tend to remain attached to the surfaces of
the tanks for the majority of the time, only swimming to capture food in the water column (Itami
et al. 1963, Forsythe & Toll 1991, Villanueva 1995). Recently settled individuals show a prefer-
ence for dark or shady areas of tanks and have reclusive behaviour, using holes, provided shelters
or gastropod shells as refuges. At this stage, individuals search for food on the floor of the aquaria
rather than in the water column. To identify individuals as presettlement or post-settlement can be
difficult. To discern between planktonic or benthic individuals, a behavioural criterion was used
by Villanueva (1995): when settled individuals are disturbed (i.e., gently touched with the tip of
a pipette) and respond by crawling, rather than swimming away, they are considered to be post-
settlement, benthic juveniles. Settled individuals also begin to direct fluxes of water from their fun-
nel to the origin of the disturbance.
Ambrose (1988) developed a means of assessing the population dynamics of recently settled
octopus individuals. The densities of recently settled and juvenile 0. bimaculatus were estimated
by sampling the hold fasts of the giant kelp, Macrocystis pyrifera, 15 times over 2 yr consecutively
at 4-LO m depth at Catalina Island, California. Up to three individuals were collected from a single
holdfast, ranging in size from recently settled animals of 5 mm ML to juveniles of 50 mm ML.
Individuals <10 mm ML were collected in all months, indicating that paralarvae settled throughout
the year, with the highest octopus densities recorded in early summer, indicating the peak period of
settlement. In the Bay of Naples, Mediterranean Sea, Naef (1928, p. 292) found that recently settled
individuals of Octopus vulgaris are "dredged up with sand, gravel and all sorts of detritus and are
easy raised on a corresponding substratum in the aquarium. They always bury deeply in such sedi-
ments or hide in narrow cavities, coming to the sediment surface only at night to forage."
On reaching the benthos, recently settled octopuses still possess symbionts remaining from
their planktonic stage. Chromidinid ciliates of the genus Chromidia typically infect renal organs
of oceanic cephalopods with a pelagic distribution . However they are also found in benthic octo-
pus species, but only those with a planktonic paralarval stage, such as Eledone cirrhosa, Octopus
salutii, 0. vulgaris and Scaeurgus unicirrhus (Hochberg 1982, 1983). It has been suggested that
these symbionts are acquired through association with crustaceans living in the water column and
are transported to the seafloor when octopuses settle (Hochberg 1982, 1983). It is not known how the
ciliates reach the renal organs and they appear to do no harm to the tissues of their host cephalopods
(Furuya et al. 2004).
181
Prolonged paralarval stages: micronektonic paralarvae

There may be a third octopus paralarval strategy that appears peculiar to animals present in the
water column over deep waters. In these habitats, large octopus paralarvae (some more than 100
mm in total length) have been encountered in plankton nets, attracted by lights or observed from
ROVs (see Table 6). Due to the large size and swimming capacities of these individuals that live
in epipelagic waters, they can be considered as part of the micronekton. Strugnell et at. (2004)
coined the term 'super-paralarvae' to refer to these peculiar, often long-armed, paralarvae. For
Macrotritopus-type paralarvae, Rees (1954) discussed the impact of ocean currents sweeping indi-
viduals off shore over very deep water. For these paralarvae, Rees (1954, p. 69), proposed that settle-
ment was delayed a nd that they could attain "nearly twice the normal size for metamorphosis". He
coined the term 'extended pelagic stages' for such para larvae. In relation to Macrotritopus defilippi,
Nesis & Nikitina (1981, p. 847) pointed out that: "The macrotritopuses are able to delay their set-
tling to the bottom and may have a chance to cross the Atlantic".
The prevalence of micronektonic para larvae, their identities and the circumstances under which
they exist are poorly known . They reach large sizes and still exhibit the characteristic paralarval
features of nearly transparent musculature, large and simple chromatophores and round pupils. The
nature of the settlement process for these forms is unknown, as is discriminating between whether
this is an accidental process or whether such species have actively delayed sett lement to exploit
resources of the epipelagic realm. As discussed (see 'Defences' section, p. 168), schools or shoals of
young Octopus rubescens have been reported in midwater in Monterey Bay, California (Figure 44).
Young (1972) captured large individuals of this species (15-25 mm ML) using IKMT plankton
trawls off California. These individuals possessed developed skin sculpture, including papillae on
the head and mantle, supraocular papillae and a granulated skin texture. Young's largest specimen
had a hectocotylized arm with a short, broad and incompletely formed ligula and lacked a ca lamus .
It is unknown whether these larger individuals constitute micronektonic juveniles, late-stage para-
larvae close to settlement, or a transitional stage with both micronektonic and benthic behaviours.
Permanent paralarvae: neoteny and holopelagic octopuses

Extended pelagic phases in oceanic paralarvae may have played a role in the evo lution of cer-
tain holopelagic octopuses. Octopus families that have completely pelagic life cycles fall into
two major groups. The ctenoglossans (tribe Ctenoglossa) contain three families (Amphitretidae,
Vitreledonellidae and Bolitaenidae), which are typically relatively small (typically <20 em in total
length, largest <50 em), sem igelatinous and transparent residents of oceanic m idwater depths between
aro und 200 and 800 m. The second group, the argonautoids (superfamily Argonautida), includes
the argonauts, blanket octopuses and their relatives (families Argonautidae, Tremoctopodidiae,
Alloposidae and Ocythoidae). These octopuses tend to be larger (up to 2m or more in total length),
more muscular, non-transparent pelagic octopuses, typically residing in shallower, neritic waters
(0-200 m) (Norman 2000).
Strugnell et a t. (2004) used molecular sequencing data to demonstrate that the closest relatives
of the ctenoglossans are two genera of benthic octopuses from the family Octopodidae, Pareledone
and Graneledone. In this study, molecu lar data and parallels in morphology between octopus para-
larvae and ctenoglossans supported the hypothesi s that the latter group evolved from paralarvae
that never 'returned to earth'. Prolonged residence in the pelagic realm and acquisition of sexual
maturity (and activity) in the water column are suggested as the mechanisms by which this group
became wholly pelagic. The micronektonic or 'super-paralarvae' concept (discussed in 'Prolonged
paralarval stages: micronektonic paralarvae', p. 182) may have been the critical stage that enabled
182
the evolution of the ctenoglossans. The origin of the other major group of holopelagic octopuses, the
argonautoids, remains unknown .
Anthropogenic impacts on early stages of octopuses

Pollution
Most octopodid species with planktonic paralarval stages live in shallow waters and can be affected
by the many pollutants introduced to the sea by human activities. These pollutants can affect octo-
puses from the early stages of development. Eggs of incirrate octopods lack an egg capsule so
that the chorion is in direct contact with the seawater. It is expected that contaminants can have
a deleterious effect on octopuses compared with those cephalopod species that have a protecting
egg capsule. For example, cuttlefishes predominantly absorb metals into the outer egg capsule, act-
ing as an effective shield that limits exposure of the embryos to soluble metals (Bustamante et al.
2002, 2004). Compared with recently spawned eggs, developing Octopus vulgaris eggs have higher
concentrations of most essential elements and also of some non-essential elements (i.e., Ag and Pb)
due to the absorption of these elements from seawater during embryonic development (Villanueva
& Bustamante 2006). Due to chronic exposure to organophosphorus pesticides such as parathion,
abnormal embryo gastrulation and arrested development has been observed in 0. mimus·embryos
at pesticide concentrations of over 0.4 mM (Gutierrez-Pajares et al. 2003). Subadult and adult octo-
puses can be used as bioindicator species in polluted areas (Butty & Holdway 1997) and are sensi-
tive to marine pollutants such as ethylene dibromide and mercuric chloride (Adams et al. 1989).
Hatchlings of 0. pallidus (a directly benthic species) are more sensitive to exposure to petroleum
hydrocarbon toxicants such as 4-chlorophenol compared with other aquatic invertebrates tested ,
such as Daphnia magna or Hydra species, and do not appear to be adversely affected by the applica-
tion of chemical dispersants to oil spills (Long & Holdway 2002). Scheel (2002) noted that densities
of Enteroctopus dojleini recorded during 1995-1998, after the 1989 Exxon Valdez oil spill, were
only 1-50% of densities recorded in British Columbia in the late 1970s and early 1980s. Scheel
suggested that the presence of the highest octopus densities in the intertidal and shallowest subtidal
areas made populations in these habitats highly vulnerable to human impacts.
Overfishing
Coastal species of benthic octopuses represent an important fishery resource in different areas
of the world (see, among others, Takeda 1990b, Lang & Hochberg 1997, Balguerfas et al. 2000,
Caveriviere et al. 2002, Rocha & Vega 2003). Since 1950, octopus captures have been constantly
increasing (Jereb & Roper 2005) and in recent years (1997-2003) world captures of Octopodidae
have ranged from 290,000 to 409,000 tonnes, with the single species Octopus vulgaris representing
11-18% of these captures (FAO 2005). Protection of spawning activity by closing fishing during
peak spawning periods has been proposed to protect Octopus vulgaris populations (Itami 1975,
Jouffre & Caveriviere 2005). Itami reviewed 0. vulgaris restocking strategies used by Japanese
fishing associations in Hyogo prefecture since 1929. He proposes the provision of thousands of
specially designed clay pots in which females could spawn. He suggests that these be located on
sandy and muddy substrata on fishing grounds rich in zooplankton (particularly crustacean zoeae)
to ensure sufficient prey densities are available for the planktonic octopus hatchlings.
Global warming
A picture of how climate change will affect marine plankton dynamics is slowly emerging (Hays
et al. 2005, Sommer et al. 2007) but how this will affect planktonic octopuses is uncertain. Due to
183
their high metabolic rate and extremely pH-sensitive blood oxygen transport, oceanic cephalopods
are amongst the most sensitive of marine groups exposed to the ocean acidification that is predicted
to result from elevated seawater C0 2 levels (Portner et al. 2004). At this stage, the direct physiologi-
cal effects of seawater acidification on planktonic stages of cephalopods are unknown and further
research is required. It is suspected that indirect effects of climate change may severely affect adult
octopus populations. An example was provided by a prolonged harmful algal bloom (HAB) lasting
nearly 2 months, which appears to have nearly eliminated the once-ubiquitous population of 0. cf.
mercatoris (a direct benthic species) in St. Joseph Bay, Florida (Tiffany et al. 2006). HABs seem to
be increasing in frequency, duration and severity worldwide, influenced by anthropogenic impact
and coinciding with trends in global warming (Van Dolah 2000). Such episodes may affect littoral
octopus populations in the future .
As with all marine life, climate change will also affect biogeographic boundaries that are
dictated by seawater temperature. This effect may manifest itself in two ways. Firstly, octopus
taxa geographically associated with land masses that do not extend into higher latitudes will run
out of available habitat and be unable to shift to higher latitudes. Secondly, octopus paralarvae
from warmer latitudes may be amongst the vanguards of invasions into previously cooler habitats.
Qualitative evidence comes from reports of an Australian warm-temperate octopus species, 0. tet-
ricus, which has been found outside its typical warmer geographic range in the cool temperate
waters of Victoria, Australia (L. Altoff personal observation 2007). As this species preys on other
octopuses (M.D. Norman unpublished data), it may act as an invasive species, effectively (and rap-
idly) displacing resident octopus taxa, some of which are endemic/restricted in distribution. Further
research is required into the potential scale of such impacts.
Concluding remarks
The distinctive form of octopus paralarvae and their differences in lifestyle from that of their par-
ents make them enigmatic and fascinating creatures. Their numbers, diversity and wide geographic
range make them important predatory members of planktonic assemblages. The duration of their
planktonic phase varies significantly between species - laboratory studies recording ranges of
3 wk to 6 months. This period is a significant proportion of the total life cycle of these animals, with
various studies reporting lifespans of between 6 months and 3.5 yr. For some species, the duration
of the pelagic period seems to be considerably extended and young octopuses can reach relatively
large sizes as part of the micronekton of epipelagic, oceanic waters. For these individuals, settle-
ment appears to be delayed for an unknown period, potentially in order to enhance dispersal and/or
exploit food resources in this pelagic realm.
Preliminary information is available for many attributes of octopus paralarvae, particularly for
two species, Octopus vulgaris and Enteroctopus dojleini. However, many opportunities exist for
new and exciting research. The most pressing research areas fall into five categories:
I. Accurate taxonomy and development of identification tools. Use of molecular sequenc-

ing techniques will enable concrete species identification , linked with databases such as
GenBank and potentially programs such as Barcode (see Strugnell & Lindgren 2007).
This will greatly expand the capacity to describe paralarvae of diverse species in detail
through all growth stages. Use of high-resolution photography and standardised morpho-
logical descriptions will be critical to this process.
2. Faunal surveys and biogeography. Equipped with better knowledge of paralarval species
discrimination, surveys of regional faunas can be undertaken to gain a better understand-
ing of the ranges, timing and abundances of the various paralarval taxa. These data can
then be analysed in relation to biogeography and oceanography.
184
3. Rearing techniques. Rearing of paralarvae requires innovative approaches to better simu-

late natural conditions for paralarvae, particularly in relation to the water column, water
quality and turbulence, prey and light regimes. Specialized treatment of brooding adult
females will also enable provision of healthy paralarvae for taxonomic and experimental
studies.
4. Growth, development and nutrition. With access to healthy para larvae of all growth stages,
research can be undertaken into morphology, physiology and behaviour during growth and
development. A greater understanding of all aspects of nutrition is critical to the develop-
ment of aquaculture for key species and needs further study, including aspects of feeding
requirements and nutrient absorption through the skin. Morphological transformations
throughout the paralarval period, particularly in skin components, are also worthy of fur-
ther investigation .
5. Hatching and settlement processes. All aspects of the cues, timing, duration and mechan-
ics of the hatching and settlement processes require more detailed research. Assessment
of the total duration of paralarval period is also required in order to assess the dispersal
capacities of different species. Development of accurate ageing techniques would be a
valuable tool in these studies.
With most of our knowledge of octopus paralarvae applying to just two species, Octopus vul-
garis and Enteroctopus dofieini, there is considerable scope for further research. The total number
of benthic octopus species with planktonic stages is likely to be high (there are at least 68 named
species and many more are yet to be described). It is clear that many new and exciting morphologi-
cal, physiological and behavioural adaptations await discovery.
Acknowledgements
We wish to gratefully acknowledge Eric Hochberg (Santa Barbara Museum of Natural History) for his
support and advice on all aspects of octopus natural history; Mitsuo Sakai and Toshie Wakabayashi
(National Research Institute of Far Seas Fisheries) for their considerable efforts in translating many
Japanese articles on planktonic octopuses into English; Jose Manuel Fortufio (Institut de Ciencies
del Mar, ICM) for assistance and advice in obtaining SEM images; Anna Bazzano (ICM) for advice
on cephalopod vision and unpublished observations on the eye morphology of planktonic Octopus
vulgaris; James A. Cosgrove (Royal British Columbia Museum), Yuzuru Ikeda (University of
the Ryukyus), Tsunemi Kubodera (National Science Museum), Richard E. Young (University of
Hawaii) and the librarians of the ICM Dolors Fernandez and Marta Ezpeleta, provided valuable
literature related to planktonic octopuses; Nicolas Ortiz (Centro Nacional Patag6nico) provided
hatchlings of Enteroctopus megalocyathus for SEM analysis and Erica Vidal (Universidade Federal
do Parana) provided images of Loligo opalescens paralarvae as the basis for Figure 40. Sincere
thanks to the many photographers who contributed live animal photographs, particularly David
Paul. M.D. Norman would like to thank Julian Finn , John Ahern, David Paul and the staff of
the Undersea Explorer for invaluable field and laboratory assistance with planktonic and broader
cephalopod research. R. Villanueva's recent research into planktonic octopus was funded by the fol-
lowing research projects: Xarxa de Referencia de Recerca i Desenvolupament en Aqiiicultura de Ia
General itat de Catalunya; Programa para Movilidad de Investigadores, Secretarfa de Estado de
Universidades e Investigaci6n del Ministerio de Educaci6n y Ciencia; Planes Nacionales de Cultivos
Marinos, JACUMAR, Secretarfa General de Pesca Maritima, Ministerio de Pesca, Agricultura y
Alimentaci6n, Spain; and by the Concerted Action CEPHSTOCK from the Commission of the
European Communities. M.D. Norman's research was funded by Australian Biological Resources
Study, the Australian Research Council and the Hermon Slade Foundation.
185
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Taylor & Francis
THE ECOLOGICAL AND EVOLUTIONARY IMPORTANCE

OF MATERNAL EFFECTS IN THE SEA
DUSTIN J. MARSHALL, RICHARD M. ALLEN & ANGELA J. CREAN
School of Integrative Biology, The University of Queensland, St. Lucia, Qld, 4072, Australia
E-mail: d.marshalll@uq.edu.au , richard.allen@uq.edu.au, a.crean@uq.edu.au
Abstract Maternal effects are non-genetic effects of the maternal phenotype or environment on
the phenotype of offspring. Whilst maternal effects are now recognised as fundamentally impor-
tant in terrestrial systems, they have received less recognition in the marine environment despite
being remarkably common. The authors review the maternal effects literature and provide a simple
framework for understanding maternal effects that increase offspring fitness (termed anticipatory
maternal effects) and maternal effects that increase maternal fitness at the expense of offspring
fitness (termed selfish maternal effects). The review then addresses various well-studied (offspring
size effects, maternal care, oviposition effects) and poorly studied (manipulating offspring disper-
sal potential, toxicant resistance, sibling competition, mate choice) examples of maternal effects
in the marine environment with a focus on marine invertebrates and fish. Offspring size effects
are strong and pervasive in the marine environment but the sources and underlying causes of off-
spring size variation remain poorly understood. More generally, the authors suspect that changes
in offspring phenotype are often adaptive maternal effects in response to environmental change.
Maternal effects are of particular importance to marine systems because they not only form a link
between the phenotypes of different generations, but the biphasic life cycle of most marine organ-
isms suggests that maternal effects also link the phenotypes of populations.
Introduction
An organism's phenotype is the product of its genotype, the environment that the organism itself
experiences and the environment or phenotype of its mother. This effect of the maternal environ-
ment or phenotype is termed a maternal effect and is one of the most important influences on
offspring phenotype and performance (Wade 1998). For over 20 yr, maternal effects have been
subject to intense interest in plants, insects and terrestrial vertebrates (Mousseau & Fox 1998a)
but these pervasive and ubiquitous effects have received less attention in the marine environment.
This review seeks to identify and explore maternal effects in the marine environment, calling on
terrestrial examples where appropriate and highlighting the potential for maternal effects in a range
of marine organisms.
For most organisms, maternal investment in each offspring exceeds paternal investment. Most
multicellular organisms are anisogamous (produce gametes of different sizes): ova are large and
sperm/pollen are small. The differential investment in gametes has led to mothers and fathers play-
ing very different roles regarding their influence over the phenotype of their offspring. Whilst the
contribution of fathers in most species is usually only genetic, mothers typically determine many
aspects of the offspring phenotype. At the very least, mothers provide offspring with their nutritional
requirements until they can feed for themselves but, in most organisms, mothers also determine the
environment in which offspring develop and the environment in which they are released or become
203
independent. This close association between offspring and mother has led to the recognition that
maternal effects are the most important determinant of an offspring's initial phenotype (Wade 1998).
Whilst maternal effects were originally considered troublesome sources of variation in quantita-
tive genetic studies (Fa lconer 1981), evolutionary biologists now recognise that maternal effects can
influence evolutionary trajectories, speciation rates (Wade 1998) and oscillations in mean phenotype
(Mousseau & Fox l998a). Simultaneously, it has become clear that the role of maternal effects in
ecology cannot be ignored. Maternal effects can generate population cycles (Ginzburg 1998), buffer
phenotypic variation in relation to environmental change and link the phenotypes of different popu-
lations/generations (Plaistow eta!. 2006). Accordingly, the number of studies examining maternal
effects has increased dramatically (Figure 1). Classic examples of maternal effects in terrestrial
systems include offspring provisioning (e.g., offspring size), brood protection and oviposition site,
but also include less-obvious effects such as the manipulation of gene expression in offspring, off-
spring dispersal profiles, immune responses, resistance to toxicants, offspring competition and sex
determination. Thus maternal effects encompass a range of different influences on the phenotype of
offspring and these effects have become a major field of study in evolutionary ecology across a range
of taxa. In marine systems, however, maternal effects have received far less attention.
The most striking maternal effect is the effect of offspring size (or provisioning) on offspring
performance. Juveniles with identical genetic backgrounds can differ dramatically in their chances
of survival and reproduction due to differences in the amount of resources they receive from their
mothers. Accordingly, there have been a number of reviews of offspring size effects in marine inver-
tebrates and fish (see Emlet eta!. 1987, Chambers & Leggett 1996, Chambers 1997, Ramirez-Liodra
2002, Marshall & Keough in 2008a). However, maternal effects as a whole have received very little
consideration in marine systems and many types of maternal effects have not been considered at all.
This seems remarkable given that the supply of new individuals into marine populations is recog-
nised as an important driver of marine population dynamics (Underwood & Keough 2001). Given
that maternal effects can strongly affect the performance of offspring, one can easily imagine that
maternal effects play an important role in marine systems but these effects are largely unexplored,
or more importantly, unrecognised.
When the marine literature is examined, it quickly becomes apparent that maternal effects
are important and prevalent; however, they are sometimes not recognised for what they are.
1500
1000
500
1980 1990 2000

Year
Figure 1 Number of citations of studies examining maternal effects since 1980. Data produced from enter-
ing "maternal effects" as a search topic into lSI Web of Science.
204
ECOLOGICAL & EVOLUTIONARY IMPORTANCE OF MATERNAL EFFECTS IN THE SEA
Consequently, in many studies where authors find that the maternal phenotype affects the phe-
notype of the offspring, they have been forced to 'reinvent the wheel' with regard to providing
ecological and evolutionary implications of the observed effects. Furthermore, in the absence of a
broader maternal effects framework , it can be difficult to reconcile seemingly conflicting findings.
For example, why does maternal nutritional stress result in a decrease in offspri ng size in some spe-
cies whilst it induces an increase in offspring size in others? The present authors believe that many of
these seemingly disparate phenomena can be unified under the single theme of maternal effects and
that an understanding of these effects will be facilitated by viewing them in such a framework . It is
also hoped that this will guide future research such that previously unconsidered forms of maternal
effects may well be common in the marine environment. The goals for this review, therefore, are to
I. Provide an overview of current maternal effects theory and develop a general framework
for viewing maternal effects in the marine environment.
2. Briefly review the incidence and types of maternal effects in terrestrial systems to provide
a guide to likely maternal effects in the marine environment.
3. Review the types and sources of maternal effects in marine organisms.
4. Highlight the potential importance of maternal effects for the ecology and evolution of
marine populations.
5. Provide some suggestions for new approaches and directions for the study of maternal
effects in the marine environment.
The first goal is to familiarise workers in marine systems with a field of study that is becoming
increasingly sophisticated in terrestrial systems. It is also hoped that this section provides a new
framework for interpreting maternal effects in an ecological and evolutionary context. The second
goal is to illustrate the range of maternal effects in well-studied, terrestrial organisms as a means
of indicating which organisms/stages in marine systems are also likely to exhibit maternal effects.
The third goal is to review the available literature on maternal effects in marine systems and the
authors have striven to also find those studies that may not have been interpreted as maternal effects
by the original authors but may be viewed as such. The fourth goal is to highlight the particular
importance of maternal effects for marine systems. The imp Iications of maternal effects for marine
populations specifically have been overlooked by most general considerations but in this review an
attempt is made to illustrate why maternal effects are likely to be important in the dynamics and
evolutionary trajectories of marine populations. The final goal is to identify the significant gaps in
our understanding of maternal effects in marine systems and it is the authors' desire to encourage
more research into what is believed will be fruitfu l lines of further research.
An introduction to maternal effects

In thi s section, the authors aim to provide the fundamentals of maternal effects for those who have
not previously considered maternal effects in an ecological and evolutionary framework. First, a
framework is provided for viewing and discussing maternal effects and to provide some means of
classifying different types of maternal effects. Then an overview of maternal effects in terrestrial
system s is given as a means of both familiarising the reader with common maternal effects and
illustrating the breadth and sophistication of the field outside of the marine environment.
Maternal effects: definitions and usage

Numerous excellent reviews have provided a general history of maternal effects and the reader is
directed to these for a historical overview of the study of maternal effects (see Roach & Wulff 1987,
205
DUSTIN 1. MARSHALL, RICHARD M. ALLEN & ANGELA J. CREAN
Mousseau & Dingle 1991, Mousseau & Fox 1998b,c). Similarly, there are many different definitions
of maternal effects and it seems that each new review of the topic provides a different definition. This
reflects the nebulous nature of maternal effects more than any imprecision or redundancy by previ-
ous authors: whilst some phenomena (such as varying energetic investment in offspring) are clearly
maternal effects, others seem harder to classify. For the purposes of this review, Elizabeth Lacey's
definition of maternal effects is the most useful; she defines a parental effect as 'any [maternal]
influence on offspring phenotype that cannot be attributed solely to offspring genotype, to the direct
action of the [non-maternal] components of the offspring's environment, or to their combination'
(1998, p. 56; note that the present authors have slightly modified this definition [material in square
brackets] to exclude paternal effects as there are too few data to speculate regarding paternal effects
in marine systems). The most difficult part of this definition is determining what the 'non-parental
components' of the offspring's environment actually are. If the mother determines the site of off-
spring release, then many aspects of the offspring's external environment will still be influenced by
mothers. This matter is discussed further in this review. Nevertheless, this definition is probably the
most comprehensive whilst still excluding some ambiguous issues such as extranuclear inheritance
(for a comprehensive discussion of the nomenclature of maternal effects, see Lacey 1998).
Maternal effects can take a variety of forms and can dramatically increase or decrease the fit-
ness of their offspring. Maternal effects can act as a buffer against environmental variation, enhanc-
ing offspring fitness. However, maternal effects can also act as a conduit by which environmental
variation in the maternal generation can influence the phenotype of offspring. Thus, before mater-
nal effects in the marine environment are explored , it is necessary to consider ways in which to
classify and group maternal effects. Wade ( 1998) divided maternal effects into stages (prezygotic,
postzygotic-prenatal and postzygotic-postnatal) according to when they manifest themselves. Lacey
(1998) considered the three general genetic mechanisms by which maternal effects can act to affect
offspring phenotype. Whilst these classifications are useful for different aspects of the study of
maternal effects, for the purposes of this review an outcome-based approach is proposed . By focus-
ing on the consequences of different maternal effects, it is hoped that their evolutionary and demo-
graphic implications will be made clearer.
Maternal effects can sometimes act to increase offspring fitness in the subsequent generation
and are therefore sometimes considered 'adaptive maternal effects' (Bernardo !996a,b, Mousseau &
Fox 1998b, Agrawal 2001). However, several authors have suggested caution with regard to viewing
maternal effects as adaptive and indeed there are numerous examples of maternal effects decreasing
offspring fitness (Bayne et al. 1975, Bernardo l996b, Rossiter 1996). Thus there has been an inter-
esting debate on the adaptive significance of maternal effects (Heath & Blouw 1998). Why do mater-
nal effects sometimes act to increase offspring fitness but other times decrease maternal fitnes s?
Importantly, maternal effects are typically classed as 'adaptive' only when they increase the
fitness of their offspring (Mousseau & Fox l998a,b). However, maternal effects that decrease off-
spring fitness may still increase the fitness of the mother. For example, bryozoan colonies that suffer
a predation event redirect their resources away from their offspring, temporarily producing off-
spring that have lower chances of survival (Marshall & Keough 2004a). Whilst a reduction in off-
spring size reduces the fitness of offspring, this maternal effect may still increase maternal fitness
because it provides mothers with more resources for recovering from the predation event (Marshall
& Keough 2004a). It may thus be misleading to regard maternal effects as adaptive on the basi s of
their effects on offspring alone.
It is important to note that whilst it may seem counterintuitive, the fitness of mothers and off-
spring are not necessarily correlated. To explain, maternal effects such as offspring size can be
regarded as a phenotype that both the mother and offspring 'share' in that variation in the phenotype
will affect the fitness of both mothers and offspring (Bernardo l996b). However, whilst the fitnes s
of both mother and offspring are affected , selection will act on the maternal effect to maximise
206
maternal fitness only (Smith & Fretwell 1974, Bernardo 1996a). The simplest way to understand
why selection maximises maternal, rather than offspring, fitness is to consider the alternative. If
selection acted to maximise offspring fitness, then mothers would produce one large, 'perfectly'
resourced offspring that consumed all of her resources such that she died following reproduction.
In reality, mothers typically produce many offspring that"each have lower fitness but the fecundity
benefits are such that maternal fitness is higher overall (Einum & Fleming 2000a). Thus mothers
and offspring are in conflict with regard to the level of maternal investment that benefits each party
and their respective interests will only sometimes be aligned (whether that be provisioning, brood
protection, oviposition site, etc.; Trivers 1974). Thus maternal effects may still be adaptive (for
mothers) even if they result in a decrease in average offspring fitness. Accordingly, it is suggested
that maternal effects be classed according to their consequences for offspring and suggest the terms
anticipatory maternal effects (AMEs) and selfish maternal effects (SMEs) to describe the two broad
classes of maternal effects (Marshall & Uller 2007).
Anticipatory maternal effects are defined here as manipulations of offspring phenotype that act
to increase maternal fitness by increasing fitness of individual offspring. Such examples are com-
mon in the terrestrial literature and are examined in more detail below. Importantly, mothers must
be able to 'anticipate' (or at least influence; Einum & Fleming 2002) the natal environment in order
for mothers to produce offspring with the appropriate phenotype. Note that the present authors rec-
ognise that this 'anticipation' does not involve a conscious prediction regarding the offspring envi-
ronment by which mothers 'choose' the appropriate phenotype of their offspring; rather the word
'anticipate' is here used as a convenient shorthand to denote that selection should favour mothers
that produce offspring of a certain phenotype when the maternal environment is a good predictor of
the environment the offspring will encounter.
Selfish maternal effects are defined here as manipulations of the offspring phenotype that act
to increase maternal fitness by decreasing offspring fitness. When mothers are under nutritional ,
competition or pollution stress, they sometimes reduce the mean quality of their offspring (George
et al. 1991, Cox & Ward 2002, Marshall & Keough 2004a, McCormick 2006). These effects may
be regarded as 'selfish' in that mothers are effectively sacrificing current offspring performance
for their own survival or for increased fecundity. Importantly, redirecting resources away from
offspring will only benefit mothers if they have a good chance of using those resources to increase
their overall reproductive success.
Whilst decreasing the mean quality/phenotype of offspring in response to environmental change
is likely to be common, it is not the only way in which mothers may increase their overall fitness at
the expense of offspring in the current round of reproduction. When the environment varies unpre-
dictably or there is uncertainty regarding the habitat to which offspring will disperse, selection
may favour mothers to produce a range of offspring phenotypes (phenotypic bet hedging; Seger &
Brockman 1987). For example, if mothers cannot 'predict' the habitat or competitive environment
of their offspring, mothers that produce a range of offspring sizes should be favoured (Capinera
1979, Crump 1981, McGinley et al. 1987, Geritz 1995, Dziminski & Alford 2005). Mothers can
also manipulate the dispersal profiles of their offspring and in a range of taxa, mothers produce
offspring with a range of dispersal phenotypes so as to 'spread their risk' regarding the colonisation
of new habitats (Strathmann 1974, Zera & Denno 1997, Krug & Zimmer 2000, Krug 2001, Toonen
& Pawlik 2001). Thus it is suggested here that there are two broad classes of maternal effects:
AMEs, which act to increase offspring fitness, and SMEs, which act to decrease offspring fitness.
Throughout this review, different maternal effects are described using this terminology where pos-
sible. It is hoped that the use of this terminology emphasises that maternal effects generally are
unlikely to be simple environmental ' by-products' that are impervious to selection and, at the very
least, should be scrutinised in a selection framework.
207
DUSTIN J. MARSHALL , RICHARD M. ALLEN & ANGELA J. CREAN
Examples of maternal effects in terrestrial systems

Maternal effects have been the object of study in terrestrial systems for almost 100 yr (reviewed
in Roach & Wulff 1987). The goal in this section is to use this literature to highlight the diversity
of potential maternal effects and indicate how similar analogues may occur in the marine environ-
ment. Simultaneously, the reader is made aware from discussion of some well-studied and classic
examples of maternal effects, and of the general types of maternal effects that have been the object
of study in other systems, in the hope that clear parallels can be seen in marine systems.
Plants and insects are among the best-studied groups and there is a rich and sophisticated litera-
ture on maternal effects in these two groups (Wulff 1986a,b, Mousseau & Dingle 1991 , Bernardo
1996a,b, Mousseau & Fox 1998b). Maternal effects in these groups range from simple effects such
as propagule size effects (for a recent review, see Bernardo 1996a) through to more dramatic manip-
ulations of offspring phenotype, such as predation resistance. It is noted that there are a number of
maternal effects (such as post-hatching parental care in birds; Stenning 1996) that are common in
terrestrial systems but herein the focus is on maternal effects that are Likely to have clear analogues
in the marine environment.
Offspring provisioning
Some of the best examples of AMEs involve the manipulation of offspring size by mothers. In
an elegant series of experiments on the seed beetle Stator limbatus, Fox et a!. (1997) showed that
mothers produce larger eggs when they lay their offspring on thick-coated (well-defended) seeds.
These extra resources better enable offspring to bore through the thick seed coats. A similar effect is
observed in the heteropteran Adomerus triguttulus; when mothers are presented with poor-quality
seeds, they increase the ratio of trophic eggs to viable eggs that they lay (Kudo & Nakahira 2005).
Trophic eggs are non-viable eggs upon which offspring can feed (analogous to nurse eggs in marine
gastropods) and represent an alternative food source for the offspring under poor food conditions.
In plants, there is a rich literature on seed size effects and the reader is directed to these specific
reviews (e.g., Coomes & Grubb 2003, Moles & Westoby 2003, Moles et a!. 2005). Interestingly,
most seed size considerations focus on among-species effects (reviews above) but nevertheless, there
is also an extensive literature on within-species effects and some of the best known and most inter-
esting examples of offspring size as a maternal effect come from plant studies (Stanton 1984, 1985,
Galloway 1995, 200la, Bernardo 1996a). Overall , plant mothers can be remarkably sophisticated
regarding offspring provisioning, increasing the size of seeds in response to decreases in environ-
mental quality such that offspring have a greater chance of subsequent survival (Agrawal 2001).
Importantly, there can be conflicting selection on offspring size in plants. For example, increases in
offspring size can positively influence competitive ability but can also increase the risk of predation
(Gomez 2004). It is suggested that the general experimental approaches in these studies could serve
as excellent models for studies of offspring size effects in sessile marine organisms.
Studies of offspring provisioning in freshwater fish are relatively more common than marine
studies and one of the first examples of offspring size effects comes from a study on the brown trout,
Salmo trutta (Bagenal 1969). More recently, Einum and Fleming, in a number of excellent papers,
show that offspring size effects can be strong, pervasive and highly context dependent in freshwater
fish (Einum & Fleming 1999, 2000b, Einum eta!. 2002, Einum 2003).
Terrestrial studies of offspring size as a maternal effect suggest that some generalisations can
be made. Generally, benign environments will select for a decrease in offspring size (Einum &
Fleming 1999, Fox 2000). Accordingly, offspring size effects should be examined under field con-
ditions whenever possible. However, whilst initial increases in environmental 'harshness' prob-
ably result in selection for increasing offspring size, very harsh environments may not select for
increased offspring size (Brockel man 1975). The present authors suggest that, rather than classifying
208
environments as 'harsh' or 'benign', future research should focus directly on the relationship between
offspring size and performance as, ultimately, this will be the most important determinant of the
benefits of increasing or decreasing offspring size (Smith & Fretwell 1974, Parker & Begon 1986,
McGinley et al. 1987, Bernardo 1996a).
Dispersal
The manipulation of offspring dispersal potential is one of the most interesting and dramatic types
of a maternal effect in terrestrial systems (Mousseau & Dingle 1991, Zera & Denno 1997, Mandak
& Pysek 1999, Parciak 2002). In a classic example, when pea aphid (Acyrthosiphon pisum) mothers
experience 'crowding' (high intraspecific competition), they produce more dispersive (winged) off-
spring that can escape the poor-quality environment (Sutherland 1969). Similarly in reptiles, moth-
ers can manipulate offspring hormone levels to affect their tendency to disperse (Shine & Downes
1999, De Fraipont et al. 2000, Olsson et al. 2002).
Offspring dormancy
Another well-studied aspect of maternal effects relates to offspring diapause in insects. Photoperiod
is the most widely studied environmental effect on diapause, but others include temperature (and
interaction with photoperiod), maternal age, host availability, maternal starvation, and geographic
location (Mousseau & Dingle 1991). In an analogous example in plants, maternal nutritional history
can also affect the timing of germination (Galloway 200lb).
Offspring defences
Some maternal effects can be remarkably sophisticated and these effects can act to buffer off-
spring from negative changes in their environment. In terrestrial plants and freshwater inverte-
brates, mothers that experience predation (or cues for predation) can produce predation-resistant
offspring, inducing permanent phenotypic changes in their offspring (Agrawal et al. 1999). For some
terrestrial invertebrates and freshwater fish, mothers that experience heavy metal stress increase the
pollution resistance of their offspring (Munkittrick & Dixon 1988, Vidal & Horne 2003), possibly
by increasing the level of metallothionen-producing RNA in their eggs (Lin et al. 2000) or increas-
ing offspring size (Hendrickx et al. 2003). Similarly, maternal effects can act to increase offspring
resistance to toxins contained in their food (Gustafsson et al. 2005). Interestingly, in the cladoceran
Daphnia magna, mothers kept in poor food environments produce offspring that are more resistant
to bacterial infection (Mitchell & Read 2005).
Oviposition site
The location that mothers choose to lay their eggs will dramatically influence the subsequent
survival/performance of their offspring and the most common examples of these effects are in
phytophageous insects (Mousseau & Dingle 1991, Sadeghi & Gilbert 2000, Monks & Kelly 2003).
Importantly, maternal age and the number of eggs that she is carrying (her 'egg load') can strongly
affect the strength of preference in mothers whereby older, or high-egg-load mothers will accept
lower-ranked (and thus lower-quality) plants (Singer et al. 1992, Fletcher et al. 1994, Sadeghi &
Gilbert 2000, West & Cunningham 2002, Javois & Tammaru 2004). Thus the maternal environment/
experience can strongly influence offspring performance by determining the local environment of
the offspring in species for which eggs are bound to one site for some period. Whether similar
effects occur in marine organisms is an unexplored but intriguing possibility with initial studies
suggesting such effects are likely (von Dassow & Strathmann 2005). Oviposition as a maternal
effect is, of course, not restricted to phytophageous insects: beetle mothers also avoid ponds that
contain predators (Brodin et al. 2006) and later in this review, the various effects of oviposition in
amphibians are highlighted.
209
AMEs versus SMEs

Most of the examples cited above represent AMEs and whilst such examples are common , there are
equally numerous examples of SMEs in terrestrial organisms and the authors do not wish to mislead
that maternal effects are commonly AMEs in terrestrial systems. For example, as phytophageou s
mothers age or accumulate eggs, they tend to accept lower-quality plant hosts on which to lay their
offspring (Singer et al. 1992, Fletcher et al. 1994, Sadeghi & Gilbert 2000, Javois & Tammaru
2004). Similarly, in five species of acanthosomatid stink bugs mothers tend to lay smaller (poorer-
quality) eggs on the periphery of their clutches because these eggs are more likely to experience
mortality due to predation (Kudo 2001). Numerous abiotic factors negatively affect seed size in
plants and offspring size in animals and the reader is directed to a number of excellent reviews on
this topic (Williams 1994, Bernardo 1996b, Rossiter 1996). Maternal exposure to toxicants can have
strong, negative effects on offspring fitness with numerous human examples (Gallagher et al. 1998,
Sram et al. 2005). Finally, another maternal effect that has received less attention is the influence of
maternal fecundity on offspring performance as mediated through sibling competition (Beckerman
et al. 2006). If offspring dispersal is poor, offspring from highly fecund mothers will experience
higher levels of intraspecific competition (and lower performance) than offspring from less-fecund
mothers (Klug et al. 2006).
Overall, maternal effects can dramatically change the performance of offspring and there are
a number of clear analogues between the effects observed in terrestrial systems and those that may
occur in marine systems. Mothers have the potential to affect the size, dispersal potential , point of
release and general phenotype of their offspring in a range of marine organisms, but many of these
effects have received scant attention in the marine literature.
Types and sources of marine maternal effects

This section deals with the types of maternal effects present (or likely to be present) in the marine
environment and how they have an impact on offspring fitness and population dynamics. For some
effects there is excellent evidence for their importance and prevalence (e.g., offspring size effects)
but for others, evidence is limited (e.g., oviposition effects). Nevertheless, terrestrial studies suggest
that these less-studied effects are likely to be of similar importance in the marine environment; they
have simply been overlooked thus far. For maternal effects for which evidence is limited , attention
is drawn to their potential importance and to avenues of investigation that may be va luable. The
scope of this review is limited to marine invertebrates and fish despite the fact that maternal effects
are likely to occur to some degree in all marine organisms. Literature on maternal effects in marine
reptiles such as turtles is therefore excluded, but it is noted that offspring phenotype (including sex)
can be affected by maternal nest site choice in this group (Godley et a l. 2002, Burgess et al. 2006).
Similarly, discussion of maternal effects in marine birds is excluded as there is too little space to
cover this rich Iiterature. Discussion of maternal effects in marine algae is also excluded, in thi s case
because of the scarcity of appropriate studies.
Maternal investment
Maternal investment may be defined as an association between a mother and her offspring, before
or after fertilisation, that carries an energetic or fitness cost for the mother and a fitness benefit for
the offspring (Clutton-Brock 1991). Benefits of parental investment for offspring include reducing
the risk of predation/starvation, lowering the negative effects of adverse environmental conditions,
or increasing the rate of development. However, providing care may incur costs to parents such
as decreased parental survival, decreased mating opportunities, or reduced number of offspring
(Sa rgent 1997). Hence, parents may increase their reproductive output through either continued
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ECOLOGICAL & EVOLUTrONARY IMPORTANCE OF MATERNAL EFFECTS IN THE SEA
investment into present progeny (thereby increasing offspring survivorship and fertility; i.e., AMEs)
or investment into expected future progeny (through increased adult survivorship and fertility; i.e.,
SMEs). Therefore, any parent that continues to invest in its offspring does so at the expense of its
potential future reproduction and hence should invest according to the value of its current brood
relative to that of its own expected future reproduction (Williams 1966).
Offspring provisioning
Offspring provisioning (which, for the purposes of this review, encompasses propagule size and
subsequent nutritional input from the mother) is one of the most obvious types of maternal effects
and can have far-reaching consequences for the performance and phenotypes of offspring. In every
taxon that has been studied, offspring size affects many important components of offspring fitness
(Bernardo 1996a) and the marine environment is no exception. Several reviews have examined the
role of offspring size on subsequent performance in marine fish (Kamler 1992, Chambers & Leggett
1996, Chambers 1997) and invertebrates (Marshall & Keough 2008a) and the reader is invited to
explore these for an in-depth review of causes and the consequences of offspring size variation
in these groups. The present goal, therefore, is not to retrace old ground but to briefly summarise
the state of knowledge of these effects and highlight their importance. The factors that affect the
degree to which mothers provision their offspring (i.e., the sources of this maternal effect) are then
addressed. Note that because of the differences in life-history stages among marine invertebrates
and fish, these two groups are considered separately.
Effects of offspring provisioning on offspring performance: marine invertebrates The study of

offspring size effects in marine invertebrates has a long history. Thorson (1950) was one of the first
to seek to understand the broad interspecific and geographical patterns in offspring size in marine
invertebrates. Whilst the interspecific variation in offspring size is impressive in marine inverte-
brates, here the focus is on intraspecific variation and effects of offspring size. Offspring size has
pervasive effects on subsequent performance in marine invertebrates, affecting every life-history
stage with potentially dramatic consequences for fitness .
In broadcast spawners (i.e., those that shed eggs and sperm into the surrounding medium), larger
eggs are larger targets for sperm and are therefore more likely to be fertilised at low concentrations
of sperm (Levitan 1996a). However, at higher sperm concentrations, larger eggs are more likely to
suffer polyspermy (Marshall et al. 2002), a fatal condition in marine invertebrates. These effects
of egg size on fertilisation kinetics suggest that the fitness return of producing offspring of any one
size will strongly depend on the local sperm environment in broadcast spawners. Levitan (2002)
even suggests that differences in the size of eggs produced by three sea-urchin species are due to
differences in the average sperm environment: species with an increased risk of sperm limitation
produce larger eggs than species for which sperm limitation is less likely. On ecological timescales ,
whether mothers adaptively adjust the size of their eggs according to local sperm conditions remains
unclear. Certainly the threat of fertilisation failure (either through sperm limitation or polyspermy)
due to producing eggs that are the ' wrong' size for the local sperm environment must represent a
strong, proximal selection pressure and previous studies suggest that broadcast spawners can 'detect'
the presence of other individuals during gametogenesis (Hamel & Mercier 1996). Nevertheless,
given the pervasive effects of offspring size in later life-history stages, the present authors wonder
whether mothers can adjust egg sizes for one stage irrespective of downstream effects and still gain
a fitness benefit. An intriguing experiment would be to manipulate the density of a species with
external fertilisation and determine if the species adjusts the size of its eggs accordingly.
In species with non-feeding larvae, offspring size affects a number of elements of the pelagic
period. Egg size affects development time in broadcast spawners, with larvae from larger eggs
generally taking longer to become competent to settle than larvae from smaller eggs (Marshall
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& Bolton 2007; but see Marshall et al. 2000). Larval size can determine the maximum longevity
of coral larvae (Isomura & Nishimura 2001), with larger larvae surviving for longer periods than
smaller larvae. Similarly, larval settlement behaviour depends on larval size, with larger larvae
remaining 'choosy' regarding settlement cues for longer than smaller larvae (Marshall & Keough
2003a). In both the laboratory and the field, smaller larvae accept poor-quality settlement cues
sooner than larger larvae in three species of colonial invertebrate (Marshall & Keough 2003a).
Presumably, the effects of offspring size on larval longevity and settlement behaviour are mediated
via energetics: larger larvae have more resources and can better 'afford' to engage in costly swim-
ming (Hoegh-Guldberg & Emlet 1997, Bennett & Marshall 2005) than smaller larvae. The effects
of offspring size on the timing of the onset of competence to metamorphose, longevity and the onset
of indiscriminate settlement all suggest that there is potential for marine invertebrate mothers with
non-feeding larvae to manipulate the dispersal (both the minimum and maximum) of their off-
spring. In terrestrial systems, mothers manipulate the dispersal potential of their offspring accord-
ing to local conditions in order to maximise their own fitness (aphids: Sutherland 1969, plants:
Donohue 1998, lizards: De Fraipont et al. 2000). Whilst this idea has not been explored specifically
in marine invertebrates, Krug (1998) showed that mothers in poor-quality environments produced
more dispersive offspring than mothers in higher-quality environments for the sacoglossan Alderia
modesta. Whether or not mothers change the size (and thus dispersal properties) of their offspring
according to local conditions remains an intriguing, but largely untested, possibility. Nevertheless,
any environmental factors that change the size of offspring within a population will consequently
alter the dispersal profile of larvae in that population and this has interesting implications for the
dynamics of that population (Fowler 2005). For example, a stress that reduces mean offspring size
will result in fewer larvae being likely to 'escape' that population.
In species with feeding larvae, offspring size effects (and maternal effects generally) have been
viewed as weaker because maternal provisioning provides only a small proportion of total resources
upon settlement (Marshall & Keough 2008a). Nevertheless, egg/larval size affects larval feeding
ability, the length of the feeding period and post-metamorphic size in echinoids with feeding larvae
(Hart 1995, McEdward 1996, Allen et al. 2006) and it seems likely that larger eggs will be favoured
when planktonic food is scarce (Allen et al. 2006). Again, one might expect mothers to adaptively
react to local planktonic food concentrations by producing larger or smaller eggs, especially in spe-
cies that are filter-feeders as adults (and can therefore better assess the conditions their offspring
will encounter) but this has not been tested.
The effects of offspring size cross the metamorphic boundary, affecting post-metamorphic per-
formance in a range of marine invertebrates with non-feeding larvae or direct development (no
larval stage). In colonial marine invertebrates, larval size affects survival , growth (Marshall et al.
2003 , Marshall & Keough 2004b, 2005, Marshall et al. 2006) and even reproduction and second-
generation offspring quality (Marshall et al. 2003) in the field. [n unitary (non-colonial) organisms ,
Ito (1997) found that offspring from larger eggs in the opisthobranch Haloajaponica were more
resistant to starvation than offspring from smaller eggs and Marshall & Keough (2003b) found that
larger Ciona intestinalis settlers had higher survival in the field. Offspring size also determines
the outcome of competitive interactions: adults derived from larger offspring are better competi-
tors in the presence of conspecifics (Marshall & Keough 2003b, Marshall et al. 2006). Again,
given the benefits of producing larger offspring when intraspecific competition is likely to be high
(Marshall et al. 2006), one might expect mothers at higher densities to produce larger offspring.
Initial evidence supports this expectation (Allen et al. 2008) but it appears that few published tests
are available. Offspring size affects post-metamorphic survival and growth in snails with direct
development (Moran & Em let 2001) and increasing offspring size may also offer a size refuge from
predation (Rivest 1983). Whilst it is expected that offspring size effects are likely to be strong in
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direct developers, the fact that this group has a mobile juvenile stage (cf. sessile marine inverte-
brates) makes field tests of more difficult and published studies rare.
Overall, offspring size has pervasive effects throughout marine invertebrate life histories regard-
less of development mode and for the most part, larger offspring have been shown to have higher
fitness (or at least performance) than smaller offspring. Numerous factors such as competition, pre-
dation and food abundance can affect the relative benefits of producing large versus small offspring
but there are surprisingly few examinations of whether mothers react to changes in the environment
in order to optimally provision their offspring. It is suggested that adaptive plasticity regarding off-
spring size is likely in marine invertebrates but there have been few tests. Nevertheless, whilst adap-
tive plasticity in offspring size is probably ubiquitous , the magnitude of plasticity is likely to differ
across groups. Marshall et a!. (in press) compared among- and within-brood variation in offspring
size across five phyla of invertebrates. They found that among-brood variation was much higher in
direct developers than in species with a larval phase and interpreted thi s variation as indirect evi-
dence for adaptive plasticity in offspring size in this group (Marshall et al. in press). Because moth-
ers with direct-developing offspring are more able to 'assess' the habitat in which their offspring
will be released, it seems likely that this group should exhibit higher levels of adaptive plasticity
with regard to offspring size. Furthermore, because direct developers, by definition, do not have a
larval stage, the relationship between offspring size and performance is likely to be more direct than
in species with a larval stage, enabling mothers to produce offspring of the appropriate size for a
particular habitat. In contrast, a species with external fertilisation and a larval stage faces a signifi-
cant challenge with regard to optimally provisioning its offspring for any single environment. To
illustrate, consider the ascidian Ciona intestinalis. At high conspecific densities, smaller eggs will
be favoured at fertilisation because they are less susceptible to polyspermy (Marshall & Keough
2003c) but producing smaller eggs results in less-dispersive larvae (Marshall & Bolton 2007) that
will perform poorly in the presence of conspecifics (Marshall & Keough 2003b). Thus, there are
potentially conflicting (and unpredictable) selection pressures acting on offspring size across the
life history in species with complex life cycles (Marshall & Keough 2006). Whilst adaptive plastic-
ity is expected in offspring size across a range of development modes in marine invertebrates, it is
predicted that this plasticity will be more constrained in species with complex life cycles.
Effects of offspring provisioning on offspring performance: fish Offspring size effects in marine
fishes have received considerable attention from empiricists and theoreticians and a number of
excellent reviews have summarised the available literature (Kamler 1992, Chambers & Leggett
1996, Chambers 1997, Heath & Blouw 1998). Therefore, only a brief overview is provided here.
The meas urement of offspring size effects in fish represents a significant challenge: both the larval
and adult stages are usually highly mobile, making it difficult to determine performance measures.
As a consequence, fish offspring size effect studies are largely restricted to laboratory conditions
and performance measures are typically restricted to early life-history stages. Larval survival and
resistance to starvation are the most common measures of performance and, in many species, lar-
vae from larger eggs perform better with regard to both. In a more recent study Grorud-Colvert
& Sponaugle (2006) showed that well-provisioned recruits also showed a higher level of predator
avoidance behaviour as they did not need to feed as much as poorly provisioned larvae. Despite the
initial effects of offspring size being strong, the effects on performance in later life-history stages
are less clear.
Some studies have shown that the effects of offspring size diminish over time but confidence in
these laboratory-based findings is limited (Heath eta!. 1999). The relationship between offspring
size and performance is extremely sensitive to local environmental conditions (Kaplan 1992, Einum
& Fleming 1999, Fox 2000) and benign laboratory environments can dramatically underestimate
213
the importance of offspring size effects. Thus, it may be premature to conclude that the effects of
offspring size diminish over time in marine fish, particularly given that some excellent studies in
freshwater fish have shown reasonably persistent, strong effects on offspring performance (Einum
& Fleming I999, Einum 2003). However, it is worth noting that larger offspring are not always
'better'; in some instances larger offspring suffer higher predation (Kamler I992, Chambers &
Leggett I996, Chambers I997, Heath & Blouw I998, Dibattista et al. 2007). At the very least, it
appears that offspring size can affect the early life-history stages of a number of marine fish spe-
cies and given the importance of recruitment for population dynamics, these effects may be crucial.
Given that egg size can affect initial larval growth rate and that larval growth rate can be a good
predictor of subsequent post-metamorphic performance in the field (Shima & Findlay 2002), it is
suggested that offspring size effects in fish may be stronger than previously thought and generally,
larger offspring will have higher fitness than smaller offspring.
Sources of variation in offspring size Offspring size is an important determinant of subsequent

performance in both marine invertebrates and fish, but what are the sources of variation in offspring
size? Offspring size is a remarkably plastic trait and can vary according to a range of different fac-
tors. This section reviews some common sources of variation in offspring size, examines any com-
mon patterns in offspring size variation and attempts to explore if there are any underlying adaptive
foundations for these patterns. Offspring size can also vary among populations with factors such
as latitude and depth (Sainte-Marie I99I, Bertram & Strathmann 1998, Lardies & Castilla 2001,
Kokita 2003). However, studies of these factors are excluded here because it is not possible to rule
out genetic differences among these populations rather than non-genetic maternal effects as the
source for offspring size variation.
Seasonal variation
Across both marine invertebrates and fish, in species that reproduce throughout the year, moth-
ers produce larger eggs during the cooler winter months and smaller eggs during warmer summer
months (Table I and Figure 3.3 in Chambers 1997). These changes in offspring size are often
associated with a concomitant change in fecundity (see references in Table I), suggesting that this is
an important maternal effect that could change the dynamics of populations across the seasons. In
marine invertebrates, the species for which data could be found are largely restricted to copepods
and amphipods. This may be due to the fact that these species typically brood their offspring and
breed for long periods, making collecting such data relatively straightforward, or these effects may
be stronger and more apparent in these groups.
Why do mothers tend to produce larger offspring in the winter months? Table 2 lists the range
of factors that can change over the season and all of these factors could affect the size of offspring
that are produced, some of which represent direct effects on mothers (i.e., non-adaptive) whilst oth-
ers could represent anticipatory adjustments of offspring size in order to increase offspring fitness .
Whilst each of these factors has the potential to affect offspring size, some have been examined
more than others and one of the most popular explanations is that seasonal changes in temperature
drive the observed changes in offspring size.
In Chambers's (1997) review of seasonal variation in fish egg sizes, he suggests that temperature
regime during oogenesis is the most dominant factor in fish. To support this suggestion, Chambers
showed that offspring sizes change irrespective of any factor other than temperature in captive spe-
cies in controlled conditions. Chambers concluded that the inverse relationship between offspring
size and temperature may have no adaptive basis and is more likely to be a simple by-product of a
mismatch between the effects of temperature on development and growth (Chambers I997). Indeed,
there is some theoretical support for such an effect and it has been suggested that a decrease in
offspring size associated with increased temperature be regarded as a physiological inevitability
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Table l Summary of studies reporting seasonal changes in offspring size in marine

invertebrates
Season o r factor associated Study
Study Group Species with si ze increase type
Sheader ( 1996) Amphipoda Gammarus insensibilis Winter Field

Soto et al. (2006) Ampelisca araucana Winter Field
Jeong et al. (2007) Jassa slalleryi Autumn (cf. spring) Field
Yu & Suh (2006) Synchelidium trioostegitum Autumn (cf. spring) Field
Pardal et al. (2000) Ampithoe va/ida Winter (cf. spring) Field
Sheader ( 1983) Gammarus duebeni Winter Field
Bell & Fish (1996) Pectenogammarus planicrurus Winter Field
Skadsheim (1984) Gammarus oceanic us Winter Field
Chaetogammarus marin us Winter Field
Chaetogammarus stoerensis Winter Field
Gammarus salinus No change Field
Skadsheim (1989) Gammarus sa linus Decreased temperature and Lab.
salinity
Pond et al. ( 1996) Copepoda Cal anus helgolandicus Winter Field
Halsband-Lenk et al. (200 I) Centropages typicus Winter Field
Diaz et al. (2003) Euterpina acutifrons Winter Field
Guisande et al. ( 1996) Euterpina acutifrons Food Lab.
Leme (2006) Decapod a Sesarma rectum Winter Field
Sampedro et al. ( 1997) Pisidia longicomis Winter (cf. spring) Field
Oh & Hartnell (2004) Crangon crangon Winter Field
Timofeev & Sklyar (2001) Euphausiacea Thysanoessa raschii Increased temperature and Field
salinity
Peel (2001) Cephalopoda Sepioteuthis australis Summer Field
Marshall & Keough (2008b) Bryozoa Watersipora subtorquata Summer Field
Table 2 Summary of the factors associated with seasonal changes that could affect
the size of offspring that are produced
Parameter Mechanism Supporting studies
Maternal environment
Temperature Kinetics of growth and provisioning Sheader (1996), van der Have & de Jong
( 1996), Chambers ( 1997)
Maternal size Maternal size-offspring size correlation Sakai & Harada (200 I)
Maternal age Maternal age-offspring size correlation Ito (1997)
Offspring environment
Temperature Slower development/decreased performance Fischer et al. (2003)
Oxygen demands in brood environment Hendry et al. (200 I)
Nutrition Decreased food availability Guisande et al. ( 1996)
Salinity Decreased offspring performance Gimenez & Anger (200 I)
(van der Have & de Jong 1996). Alternatively, a change in offspring size in response to tempera-
ture could be an adaptive response: for species that feed in the plankton, increases in offspring
size decrease the length of the planktonic period, potentially countering the effect of temperature
215
on developmental rate (Vance 1973, Clarke 1992). One aspect of temperature that has received
less attention than the above is its effect on oxygen demands of the brood. Given that temperature
will increase the oxygen demand of broods (Baynes & Howell 1996) and larger eggs require more
oxygen (Strathmann & Chaffee 1984, Moran & Allen 2007), then mothers may have to reduce the
size of their eggs when temperatures are higher such that they receive sufficient oxygen. However,
it should be noted that larger eggs do not necessarily suffer more than smaller eggs when oxygen
levels are low (Einum et al. 2002). Whilst temperature represents a good candidate for the underly-
ing factor for seasonal changes in egg size, whether the change be an adaptive response or not, there
are other factors that may play an important role.
In addition to temperature, environmental factors such as food and salinity, and maternal fac-
tors such as age and size, and the likely competitive environment of offspring will also change
across the season. For example, Guisande et al. (1996) showed that Euterpina acutifrons mothers
that experience lower food levels (which occur during winter) produce larger offspring. This change
in offspring size was viewed as an AME: mothers increase the size of their offspring so that they
can better cope with low food conditions. Food levels are typically lower during the winter months
and development is slower. So if increased offspring size allows offspring to develop faster or cope
with lower food levels, then mothers may gain a fitness benefit from producing larger offspring.
Thus, the seasonal pattern in offspring size has been interpreted as an adaptive strategy by which
mothers maximise fecundity (by producing smaller eggs) when selection on increased egg size is
relaxed during the warmer months (Skadsheim 1984, Bell & Fish 1996). It is particularly interest-
ing that this explanation has been invoked repeatedly in copepods and amphipods, two groups for
which mothers brood their offspring and can detect the likely food conditions that their offspring
will experience. Whilst this explanation has intuitive appeal, there are too few studies outside of
these groups to determine the generality of this effect.
Gimenez & Anger (2001) found that salinity strongly affects egg size, with mothers producing
larger eggs at lower salinities in the estuarine crab Chasmagnathus granulata. Embryos utilise
more resources during development at lower salinities due to the costs of osmoregulation and so
mothers may produce larger offspring in order to cope with this change (Gimenez & Anger 2001).
In a number of other studies, it is difficult to disentangle the effects of salinity and temperature as
both change over the season (Skadsheim 1989, Timofeev & Sklyar 2001).
External environmental factors are not the only changes that occur across seasons that could
affect the size of offspring produced: the mothers producing the offspring also change. The size and
age of reproductive mothers can both change across the seasons and both can affect offspring size
(see below). Whilst some studies have separated maternal size differences from seasonal effects
(Soto et al. 2006), it is worth noting that any systematic differences in maternal size/age across
seasons may also affect offspring size and should be noted in future studies.
In order to disentangle the competing explanations for seasonal variation in offspring size, two
approaches are suggested. First, multifactorial, manipulative studies that vary salinity, tempera-
ture and food independently would be useful for determining which factors/cues elicit a change in
the size of offspring produced by mothers. Second, measuring the relationship between offspring
size and subsequent performance across seasons would be a valuable step for determining whether
changes in offspring size across seasons represent an AME by which mothers are maximising their
fitness by producing offspring of 'optimal size'. For example, Marshall & Keough (2008b) esti-
mated the relationship between offspring size and performance in the field in summer and winter for
the bryozoan Watersipora subtorquata. They found that there was a steeper relationship between
offspring size and post-metamorphic performance in summer and that this relationship resulted in
larger offspring sizes being favoured. These findings matched the observed variation in offspring
size across the seasons; the size of W. subtorquata larvae was greater in summer than in winter.
216
Thus, in some instances at least, seasonal changes represent an adaptive response by mothers to
maximise their fitness but more studies are needed.
Small-scale temporal variation: maternal age and spawning sequence

As well as showing seasonal variation, offspring size can also vary at smaller temporal scales. The
age of mothers can affect the size/quality of offspring they produce. Berkeley et al. (2004) showed
that maternal age was an excellent predictor of offspring provisioning and subsequent performance
in the rock fish Sebastes melanops. Similar effects were suggested for Pacific herring Clupea pallasii
(Hershberger eta!. 2005). For invertebrates, problems associated with accurately aging field-caught
individuals make such studies rarer, although Gardner (1997) showed a decrease in offspring size
across moults in the crab Pseudocarcinus gigas. The size of offspring can also change over a single
spawning season but it is unclear whether this is a maternal age effect or not. Jones et a!. ( 1996)
found that mothers decreased the size of their eggs over subsequent spawns in the dorid nudibranch
Ada/aria proxima. A similar decrease in offspring size was observed in the annual gastropod Haloa
japonica (Ito 1997) but interestingly, offspring size increased with maternal body size.
Maternal size
A positive relationship between maternal body size and offspring size is well known in both marine
fish and invertebrates. A number of reviews of fish (Chambers & Leggett 1996, Heath & Blouw
1998) provide a comprehensive list of offspring-maternal body size correlations and these lists
are not repeated here. In marine invertebrates the relationship appears to be more variable, with
many species showing a positive relationship but others show no relationship or even a negative
one (Table 3). The underlying causes for this correlation are largely unknown. Sakai & Harada
(2001) suggest an intriguing explanation by which larger mothers can provision their offspring more
efficiently and quickly than smaller mothers; thus producing larger offspring carries less of a cost
for larger mothers relative to smaller mothers. Alternatively, larger mothers may produce larger
offspring because they are more fecund and are adaptively provisioning their offspring to deal with
higher levels of competition (McGinley et al. 1987). If the relationship between maternal body
size and offspring size is an adaptive response to increased sibling competition, the relationship
would be expected to be more common in species with philopatric or poorly dispersing offspring.
Whereas the compilation of studies considered in the present review is by no means exhaustive
(and probably underestimates the number of species for which no relationship occurs), no such size
relationship pattern can be found, but further studies that specifically address this intriguing ques-
tion are awaited. Alternatively, offspring-maternal body size relationships may simply be a product
of physiological constraints and have no adaptive basis (Congdon & Gibbons 1987, Fox & Czesak
2000), but this explanation seems to be unlikely for most species.
Maternal nutrition
Maternal nutrition can have mixed effects on offspring size. While some studies show that a decrease
in maternal food availability decreases offspring size (Bayne et al. 1978, Qian & Chia 1991, Qian
1994, George 1995, Chester 1996, Krug 1998, Meidel et al. 1999, McCormick 2003, Steeret al. 2004,
Gagliano & McCormick 2007), others show an increase in offspring size in response to decreased
food availability (Guisande et al. 1996, Allen et al. 2008). This variation in the effects of maternal
nutrition is a good example of why such effects need to be viewed in a maternal effects framework.
It is suggested that decreases in offspring size represent a SME while increases in offspring size rep-
resent an AME (although whether a change in offspring size is viewed as a decrease or an increase
depends on the point of reference). Ultimately, whether a decrease in maternal food results in an
AME or a SME will depend on ( 1) whether mothers have an opportunity to reproduce at some later
stage and/or (2) whether maternal nutrition is a good predictor of offspring nutrition.
217
Table 3 Summary of studies investigating the effect of maternal body size on offspring size
Study Species Development Relationship
Invertebrates
Green ( 1998) Keratella cochlearis D +ve
Miloslavich & Dufresne (1994) Buccinum cyaneum D +ve
llano et al. (2004) Buccinum isaotakii D +ve
Valentinsson (2002) Buccinum undatum D
Kohn & Perron (1994) Conus spp. ( 13 spp.) p No relationship in 11/12 species
but -ve in C. marmoreus
Chaparro et al. ( 1999) Crepidula dilatata D +ve
Ito (1997) Haloa japonica L +ve
Steer et al. (2004) Euprymna tasmanica D
Bridges ( 1996) Capitella sp. I (cf. Capitella p +ve
capita/a Fabricius)
McCarthy et al. (2003) Phragmatopoma /apidosa p
Bridges & Heppell ( 1996) Streblospio benedicti L +ve
McLaren ( 1965) Pseudocalanus ? +ve
Soto et al. (2006) Ampelisca araucana B
Sheader ( 1983) Gammarus duebeni D
Dunn & McCabe (1995) Gammarus duebeni D +ve
Jeong et al. (2007) Jassa slalleryi B +ve
Bell & Fish ( 1996) Pectenogammarus planicrurus B +vein 1/9 samples
Yu & Suh (2006) Synchelidium trioostegitum B +ve
Clarke (1992) Ceratoserolis trilobitoides B +ve
Sera/is polita B
Willows (1987) Ligia oceanica D +ve
Sam pedro et al. ( 1997) Pisidia /ongicornis p
Clarke ( 1993) Chorismzis antarcticus p +ve
Eualus gaimardii p +ve
Nematocarcinus lanceopes p +ve
Notocrangon antarcticus p
Kim & Hong (2004) Pa/aemon gravieri p
Gimenez & Anger (200 1) Chasmagnathus granulata p +ve
Dugan et al. ( 199 1) Emerita analoga p +Ve in 8/22 sites
Damiani (2003) Pagurus /ongicarpus p
Ouellet & Plante (2004) Homarus ｡ｭ･ｲｩ｣ｮｵＮｾﾷ＠ p +ve
DeMartini & Williams (2001) Scylla rides squommosus p
Barnes & Barnes ( 1965) Semibalanus balanoides p +ve
Marshall et al. (2003 ), Bugula neritina L +vein 2/3 sites, -vein 1/3
Marshall (2005)
Bingham et al. (2004) Leptasterias aequalis D +ve
Marshall & Keough (2003c) Uniophora granifera L +ve
Marshall et al. (2000) Pyura sto/onifera L +ve
Marshall & Keough (2003b) Ciona intestinalis L +ve
Fishes
Bradford & Stephenson ( 1992) Clupea harengus p +ve spring spawners but not
autumn spawners
Ware (1985) Clupea pa/lasii p +ve
Ciechomski ( 1966) Engraulis anchoita p +ve
218
ECOLOGiCAL & EVOLUTIONARY IMPORTANCE OF MATERNAL EFFECTS IN THE SEA
Table 3 (continued) Summary of studies investigating the effect of maternal body size on
offspring size
Study Species Development Relationship
Hinckley ( 1990) Theragra chalcogramma p

Hi slop ( 1988) Melanogrammus aeglefinus P +ve
Marteinsdottir & Able ( 1988) Fundulus heteroclitus B +ve for I12 populations
Bengtson et al. ( 1987) Menidia menidia p
Pankhurst & Conroy ( 1987) Hoplostethus at/anticus p
Koslow et al. ( 1995) Hoplostethus at/anticus p
Conroy & Pankhurst ( 1989) Allocyttus niger p
Pseudocyttus macu/atus p
McEvoy & McEvoy ( 1991) Psetta maxima p +ve
Buckley et al. ( 1991) Pseudopleuronectes p +ve
america nus
Nore: Relationship is indicated as positive (+Ve), negative (-ve), no relationship, or not rep01ted (-).lnvettebrate modes
of development: B, brooder; D, direct development; L, Jecithotrophic larvae; P, planktotrophic larvae. Fish modes
of development: B, benthic eggs; P, pelagic eggs.
There appears to be a temptation in the marine literature to view mothers as simple conduits by
which environmental variation affects offspring size. However, terrestrial studies illustrate that it is
not as simple as 'poor provisioning in, poor provisioning out' and in many instances, mothers can
buffer offspring from poor nutritional conditions by increasing the size of their offspring. Similar
effects are likely in marine organisms but, in order to observe these effects, there must be a focus
on natural variation in maternal nutrition. If maternal nutrition is reduced to unnaturally low levels,
then mothers may reduce the size of their offspring but this gives little information about the role of
maternal nutrition in determining offspring size because the mother is being presented with a novel
nutritional stress. Further studies would be welcome that examine the role of maternal nutrition in
determining offspring size, using natural variation in maternal nutrition, but that do not confound
population effects with differences in nutrition.
Summary of the sources of offspring size variation

Identifying the underlying causes of offspring size variation is problematic because important life-
history traits are often correlated. For example, offspring size could increase in summer months
because mothers are responding to changes in the environment their offspring will encounter,
because the average size or age of mothers has changed or because mothers have access to more or
less food. Disentangling these competing hypotheses will be difficult but ultimately rewarding given
that offspring size can have profound effects on the recruitment success and subsequent population
dynamics of marine populations. What is clear is that offspring size is a highly dynamic trait under
a range of maternal influences and many factors can modify the size of offspring mothers produce.
Brood care
Offspring size/provisioning does not represent the only reproductive investment that mothers can
make in their offspring, they can also protect the offspring from predation and maintain local envi-
ronmental conditions such that they benefit offspring. These behaviours tend to increase offspring
fitness at the expense of current or future maternal fecundity and as such, the balance between
maternal care and fecundity (from a life-history theory perspective) is determined by the same
considerations as those for the balance between offspring size and fecundity. The various aspects
219
DUSTIN 1. MARSHALL, RICHARD M. ALLEN & ANGELA 1. CREAN
of brood care and how they act as a maternal effect are discussed next. Note that the authors do
not consider the simple act of 'brooding' of offspring on/in the body as being a maternal effect, but
focus on maternal behaviours that (I) have the potential to affect offspring performance/phenotype
and (2) show signs of, or the potential to, vary among individuals of the same species according to
the maternal phenotype or environment. Although brood care by fathers is relatively common in
marine fish, this type of care is excluded from this review as it is not a maternal effect.
Many species of both invertebrates and fish brood their offspring on their bodies. One of the
main constraints to brooding in the marine environment is the low diffusion coefficient and solu-
bility of oxygen, which affects oxygen acquisition and therefore the capacity to aggregate embryos
(Fernandez et al. 2003, Green & McCormick 2005, Fernandez et al. 2006b). Accordingly, many
brooding mothers show specific behaviours that provide oxygen to embryos to enhance develop-
ment, survival and growth of the brooded embryos (Wheatly 1981 , Chaffee & Strathmann 1984,
Strathmann & Strathmann 1995, Naylor et al. l999). Brooding female crabs adopt very clear behav-
iours (e.g., abdominal flapping), not present in non-brooding females, which are implicated in both
the detection of oxygen conditions and oxygen provision to the embryos (Fernandez et al. 2000,
Baeza & Fernandez 2002, Fernandez & Brante 2003). The frequency of abdominal flapping has been
found to increase with embryonic development, coinciding with an increase in oxygen demands of
the embryos (Baeza & Fernandez 2002). This suggests that brooding females are capable of modi-
fying their behaviour depending on the oxygen demands of their embryos. However, there is a sub-
stantial cost associated with active brooding behaviours (Fernandez et al. 2000), which increases
with the frequency at which oxygen is provided to the embryos (Baeza & Fernandez 2002), and may
increase with body size (Fernandez et al. 2006a).
Brood care can extend beyond the maintenance of oxygen levels for offspring and in some spe-
cies, mothers appear to carry their offspring for extended periods in order to decrease mortality,
which can be high in early juvenile stages. While brood care is not necessarily an obligate reproduc-
tive strategy (Thiel 1998a), juveniles receive significant benefits in the form of growth and survival
(Aoki l997, Kobayashi et al. 2002). However, brood care may also lead to conflicts both among
offspring and between the mother and offspring, particularly during later life-history stages when
resources such as food and space become limiting (Thiel 2003). Furthermore, parasites and other
epibionts may be transferred from parents to offspring (Thiel 1998b). The benefits of brood care
may be dependent on ecological variables (e.g., presence of predators, Kobayashi et al. 2002), and
the duration of brood care is likely to be influenced by the availability of resources such as food
and shelter (Thiel l999, 2003). Maternal care can be particularly costly for species with benthic egg
masses that require continual protection as it often results in adults being unable to feed during thi s
period (Bosch & Slattery 1999).
Overall, brood care is likely to represent a significant maternal effect in marine invertebrates
and fish with non-dispersive offspring but apart from studies on amphipods (Thiel l998a , 1999),
there are few other examples of how much of an effect brood care has on subsequent offspring per-
formance. This may be because, in many species, brood care is obligate (and therefore, removal of
maternal care results in complete reproductive failure) but the suspicion is that even slight variation
in the degree of brood care may have profound effects on subsequent offspring performance.
Offspring release
Many life-history studies focus on easily quantifiable maternal effects such as offspring provision-
ing and offspring phenotype. While these factors can profoundly influence both maternal and off-
spring fitness , where and when offspring become independent are clearly also important (Resetarits
1996). When environments vary in quality, natural selection should favour mothers that release their
offspring in places and at times that increase offspring (or at least, maternal) fitness . This section
220
first highlights the importance of oviposition 'choices' in the terrestri a l literature and then attempts
to identify the consequences and prevalence of maternal effects on offspring release ·in marine
organisms. Consideration is then given to the two major ways in which offspring release can affect
offspring performance: spatial variation in offspring release and temporal variation in offspring
release. Here the terms 'release site' or 'release time' are used to mean the spatial or temporal posi-
tion where mothers give offspring independence and no longer provide any maternal care. Release
site is a general term that can be used when describing all reproductive modes but in this review the
term 'oviposition' is used to specifically mean the location where oviparous mothers release their
eggs.
Oviposition effects in terrestrial systems

Across many taxa, there is good evidence that mothers select locations to release their offspring
based on environmental qualities that increase offspring fitness and this choice can be the "single
greatest determinant of offspring success" (Mousseau & Fox 1998b, p. 403). Accordingly, the study
of oviposition (the site of egg laying) effects (in insects and amphibians particularly) is a major
and sophisticated field (reviewed in Thompson 1988, Thompson & Pellmyr 1991). However, the
effect of the location where offspring are released has received less attention in marine systems. To
adequately describe the fitness consequences of oviposition across the terrestrial literature is beyond
the scope of the present review. A brief list is provided of the different effects that oviposition site
can have on offspring phenotype/performance (Table 4), as is a list of the cues mothers use to
choose among different potential sites for depositing their offspring (Table 5).
Offspring release site effects in marine systems

In the marine environment, there are some clear potential analogues to the ovipositing phyto-
phageous insects but these marine groups have received relatively little attention. Herbivorous
amphipods that are closely associated with marine macroalgae and sacoglossan sea slugs are both
groups in which the site of maternal release from brooding (in the case of amphipods) or oviposition
(i n the case of sea slugs) will strongly affect offspring performance. However, in one of the few stud-
ies to consider such effects, Poore & Hill (2006) found no difference in preferences of brooding and
non-brooding females , despite performance differing greatly among different host plants (Poore
2004). Nevertheless, it may be expected that in a range of organisms that are closely associated with
particular hosts and have poorly dispersing young, the location that offspring are released will have
profound consequences for offspring performance.
Species that associate with hosts are not the only marine organisms in which to expect strong
effects of oviposition on offspring performance. Von Dassow & Strathmann (2005) found that
there was clear ranking of preferences with regard to oviposition sites in the bubble shell snail
Haminaea vesicular. Mothers preferred to deposit egg masses on red algae and eel grass over other
substrata and when more substratum was artificially added, the abundance of snails and egg masses
increased, which the authors interpreted as evidence that mothers were limited in their access to
suitable sites (von Dassow & Strathmann 2005). It is possible that gastropod mothers that are car-
rying a high 'egg load' may also show decreases in the stringency of preferences over time as in
ovipositing insect mothers but this remains to be tested (Singer et al. 1992). Many other gastropods
with benthic egg masses appear to show clear preferences for different substrata and use a variety
of cues to identify these substrata and some of these oviposition preferences appear to be related
to enhancing offspring survival (Biermann et al. 1992, Benkendorff & Davis 2004). For example,
Neptunea pribiloffensis lays its eggs next to the sea anemone Tealia crassicornis, a behaviour that
probably reduces mortality due to grazing by the urchin Strongylocentrotus droebachiensis and this
laying behaviour has been interpreted as a form of 'babysitting' (Shimek 1981). Importantly, a range
of environmental stresses can have profound effects on offspring phenotype, suggesting that any
221
Table 4 Summary of insect a nd amphibi an studies that report effects of oviposition site on
o ffspring attributes
Effec t o n o ffsprin g Mechani sm St udy
Insects
Differential survival Predati on/paras iti sm Ohsaki & Sato ( 1994), Loader &
and growth Damman ( 199 1)
Seasonal shift in host avail abilit y, seasona l sh ifts in Rausher ( 1980), Rausher ( 198 1)
host nutrient quality that increases age of host
leaves that increases sc lerop hylly in mature leaves
Differential survival Larval size Rausher & Papaj ( 1983)
Egg load Rausher ( 1979a)
Li ght intensity Rausher ( 1979b)
Intraspecifi c variation in host quality Ng ( 1988)
Differe ntial growth Food availability Loader & Damman ( 1991)
Differe ntial growth Light inten sity (elevated larvae body temperature) Gross mueller & Lederhouse ( 1985)
Progeny size Competin g siblings Rosenheim & Rosen (1991)
Sex rati o Host body size Jones ( 1982), King ( 1988)
Temperature Lysyk (2000)
Host plant preference Imprinting Anderson et al. ( 1995)
Amphibians
Differential survival Temperature Howard ( 1978)
Predation Resetarits & Wilbur ( 1989)
Conspecific canniba li sm Spieler & Lin senmair ( 1997)
Desiccatio n Sp ie ler & Lin senmair (1997)
Pathogen Kiesecker & Blaustein ( 1997)
Parasite Kiesecker & Skelly (2000)
UV-B Palen et al. (2005)
Po nd size (linked to desiccati on probability) Seale ( 1982)
Differential growth Competition Lawler & Morin ( 1993)
Canopy cover/te mpe rature Skell y et al. (2002)
Paras ite Ki esecker & Skelly (2000)
differences in oviposition location may be important (Przeslawski 2004). Howeve r, what is largely
lacking is information on the degree of variation in ovi positio n preferences among mothers and,
most importantly, the consequences of thi s variation for the subseq uent performance of offspring
(but see Biermann et al. 1992 for a ra re exception).
Variation in oviposition location among broods of eggs is not the only source of materna l effects
on offspring survival; location within a brood or clutch may a lso be important. In acanthosomatid
stinkbugs, eggs deposited on the outside of the egg mass suffer higher predation than those on the
inside of the egg mass ( Kudo 2001). The authors are unaware of a ny similar studies on predation
in marine organisms but there are other effects of the position in the egg mass in marine spec ies.
Booth ( 1995) showed that in the gastropod Polinices sordid us, eggs in the middle of the large
(37-mm diameter) egg mass had access to less oxygen and developed more slowly than eggs in the
outer region of the egg mass. Other gastropod egg masses are constrained by the availability of
oxygen (Strathmann & Chaffee 1984) and it is likely that this particular maternal effect (position
within the mass) will have important consequences for the timing of offspring emergence and the
size/qua lity of offspring emerging from the egg mass.
The location in which offspring are released for organisms with sedentary offspring or those
that produce egg masses is an obvious candidate for a matern al effect but what about spec ies that
222
Table 5 Summary of insect and amphibian studies that report factors influencing maternal
choice on ov iposition site
Cue Ovipositin g spec ies Host Study
Famil y of plant Various le pidopterans Vari o us species Ehrlich & Raven ( 1964)
Plant species Papilio mac/1aon Vari o us species Wiklund ( 1975)
Various Heliconius spp . Vario us Passijlora spp. Smiley ( 1978)
Light intensity Bartus philenor, Aristolochia orbicularis, A. micrantha Rausher ( 1979b)
B. po/ydamus,
Parides montezuma
Papilio glaucus Prunus serotina Gross mue lle r &
Lederho use ( 1985)
Pl ant morphology Bartus philenor Aristolochia reticula/a, A. serpen taria Rausher ( 1978)
Plant density Battus philenor Aristo/ochia reticula/a Ra usher & Papaj ( 1983)
Plant chemistry Pieris rapae Cruciferae Renwick & Radke ( 1983)
Egg load on pl ant Battus philenor Aristolochia reticula/a , A. serpentaria Rausher ( 1979a)
Egg load in mother Bartus philenor Aristolochia reticula/a, A. serpentaria Odendaal & Rausher
( 1990)
Plant nutriti onal quality Bartus philenor Aristolochia reticu/ata, A. serpentaria Rausher ( 1981 )
Plant sclerophylly Bartus philenor Aristo/ochia reticu/ata, A. serpentaria Rausher ( 198 1)
Maternal experience Bat/us philenor Aristolochia reticulata, A. serpen taria Rausher ( 1978)
Euphydryas editha Castilleja indiviso, Plantaga erecta , Singer ( 1982)
Collinsia tinctoria, C. parviflora,
C. bicolor
Particular plants in a Euphydryas editl1a Pedicularis semibarbata Ng (1988)
populati on
Expe rience as larvae Spodoptera lirtoralis N/A Anderson et al. ( 1995)
Note: NIA =not appli cable.
release dispersive, planktonic larvae? Evidence for an effect of offspring release location on off-
spring performa nce is limited but given that many organisms with planktonic larvae migrate to
specific spawning location s or show distinct offspring release behaviours (MacFarlane & Moore
1986, McEuen 1988, Fleming 1996, Kotake et al. 2005 , Corgos et al. 2006), this is likely to affect
subsequent offspring performa nce and be an important source of maternal effects. Even if moth-
ers do not migrate to a location to release their offspring, offspring are essentially ' inheriting' the
environment in which their mothers occurred. Thus the chances of an offspring performing well or
poorly may be strongly affected by the quality of the environment in which the mother occurs and
releases her young, a non-ge netic materna l effect that has received little attention in either marine
or terrestrial systems.
Timing of offspring release

Just as the location in which offspring are released can affect subsequent performance, so can the
time at which offspring are released. For example, Searcy & Sponaugle (2000) found seasonal
differences in the performance of Thalassoma bifasciatum larvae, with spring cohorts spending
shorter times in the plankton than autumn cohorts . Similar effects appear to occur in other marine
fish (Amara et al. 1994, Marteinsdottir et a l. 2000) but specific investigation s are rare. In his excel-
lent review of the factors affecting, and consequences of, the timing of larval release, Morgan
(1995) suggests that there is a hierarchy of cues that regulate the release of crab larvae. Morgan
(1995) suggests that release times are plastic and that there are important fitness consequences for
offspring depending on when they are released over both short (die! , tidal) and long (seasonal) tem-
poral scales. The present authors agree and suggest that thi s is a fruitful line of research because
223
offspring performance is likely to be as strongly affected by when offspring are released as it is by

where they are released.
Mate choice as a maternal effect

The classic view of the sexes is that males compete for fertilisation s but females choose males
(Bateman 1948). For marine organisms that copulate, transfer spermatophores or pair spawn,
females often choose amongst males regarding which individual will fertilise the majority of her
eggs (but see Berglund 1991 , Berglund et al. 1993 for an interesting exception). Because the mater-
nal environment and phenotype can affect which male is mated with and because offspring per-
formance may in turn depend on male identity, mate choice can be viewed as a maternal effect. To
date, the majority of positive associations in marine species between mate preference and offspring
survival have been found in reef fish. However, whether this is a true reflection of the prevalence of
adaptive mate choice across marine taxa or purely an artefact of the ease of observing and detecting
mate choice and its consequences in these species is unclear. Although several studies have found
relationships between indicator traits used to select mates and offspring fitness, evidence for 'adap-
tive' mate choice is highly variable in quality and appears to be quite different between species with
demersal and pelagic eggs (Petersen & Warner 2002).
One of the commonest forms of female choice in benthic-spawning fish is to lay eggs in nests
already containing eggs (Magnhagen & Kvarnemo 1989, Petersen 1995, Forsgren et al. 1996, Kraak
1996a, Petersen & Warner 2002). This behaviour may be explained by a reduced risk of predation
or cannibalism ('the dilution effect'; Petersen & Marchetti 1989, Forsgren et al. 1996), increased
parental care (Sargent et al. 1986), or mate-choice copying. Much debate has centred on whether
female preference for males with eggs in their nest is an adaptive response to increased egg su r-
vival or purely a form of 'copying' (Pruett-lones 1992, Jamieson 1995, Kraak 1996b). Although
these two hypotheses are not mutually exclusive, female preference for nests with an intermediate
number of eggs and eggs in earlier stages of development suggests female choice for egg survival
rather than mate-choice copying (Cote & Hunte 1989, Hoelzer 1990, Jamieson 1995). Furthermore,
in choice trials, females do not always copy the observed mate choice of other females (Forsgren
et al. 1996). Regardless, copying may be equally adaptive to independent mate choice if direct male
assessment is costly and/or some females are less able to discriminate and choose higher-qu ality
males. Therefore, females' preference for males with eggs in their nest is most likely to be an adap-
tive maternal effect, resulting in direct benefits via increased offspring survival (Petersen 1995,
Forsgren et al. 1996, Kraak 1996a).
Female choice for males already guarding eggs may not always be adaptive as male clutch size
does not always influence egg survival. For example, in Stegastes partitus, egg survival remained
unchanged over the normal range of brood sizes defended by males, most likely because the major-
ity of egg losses occur at night when males are not defending their eggs (Knapp & Kovach 1991 ).
Moreover, significant variation exists among males in the number of eggs cannibalised, probably
depending on male condition (Kraak 1996a). Therefore, for mate choice to be adaptive, females
must be able to detect such quality differences. Females may base their mate choice on egg presence
only when other characters are approximately equal. Alternatively, choice could be based on several
cues, taking each into account according to some priority or weighting system.
Before any males have obtained eggs, females may spawn with the largest males defending
the best-quality nest sites, or they may spawn randomly among a group of males (Jamieson 1995).
Numerous studies have found a female preference for large males (e.g., Thompson 1986, Hastings
1988, Gronell 1989) and a positive correlation between male size and egg survival (Cote & Hunte
1989, Knapp & Warner 1991). In addition, females may be able to vary the number of eggs released
during a spawning act, releasing more eggs when spawning with larger males; alternatively females
224
may choose to spawn with larger males when they have more eggs to lay (Cote & Hunte 1989).
Conversely, some studies have failed to find a relationship between male size and egg-hatching
success (Knapp & Kovach 1991, Petersen 1995) and consequently no fema le preference for male
size alone (Magnhagen & Kvarnemo 1989, Petersen 1989, Knapp & Kovach 1991, Pampoulie et al.
2001). This lends support to the hypothesis that female choice in benthic-spawning fish is an AME
as females are apparently only using male traits that correlate with offspring survival. However, in
some cases, although females preferentially spawned with larger males, the proportional survival of
egg batches was uncorrelated with male size (Cole & Sadovy 1995).
Overall, mate choice is likely to have strong effects on subsequent offspring performance, par-
ticularly in species such as benthic-spawning marine fish. Similar mate choice effects may exist in
some other organisms but information is scarce.
Adaptive manipulation of offspring phenotype

There are a number of maternal effects that do not clearly fit into the other categories that have
been discussed in this section but nevertheless have the strong potential to affect the performance
of offspring. Table 6 summarises non-marine studies that have shown an adaptive manipulation of
offspring phenotype in response to environmental stimuli; marine organisms have received less
attention. These effects are included in this review, despite the fact that marine examples are rare,
because they are equally likely to occur in marine organisms and it is hoped that highlighting them
may stimulate research in these areas. Adaptive offspring size variation has been explicitly excluded
from this list as this maternal effect is covered elsewhere in this review. For simplicity and brevity,
environmental sex determination in marine turtles is excluded from the review; this maternal effect
is, however, common in this group. From Table 6, it is clear that there is a range of factors that could
affect the phenotype of offspring in the marine environment that have not been explored. However,
there are some initial indications that a number of these maternal effects are likely to be common
among marine organisms.
The effect of maternal environment on the dispersive properties of offspring observed in lizards
and aphids has some clear analogues in marine systems. Krug (1998) showed that when Alderia
modesta mothers (that previously ｰｲｯ､ｵ｣ｾ＠ only lecithotrophic larvae) were starved, they produced
a higher proportion of dispersive, planktotrophic larvae. Krug (1998) suggested that this change
Table 6 Summary of studies reporting environmental stimuli that can induce

the manipulation offspring phenotype by mothers
Maternal effect Environmental stimulus Study Species
Predati o n resistance Predator kairomones Agrawal et al. ( 1999) Daphnia culcul/ata

Herbivory Agrawal et al. ( 1999) Raphanus raphanistrum
Pollution resi stance Cadmium Lin et al. (2000) Oreochromis mossambicus
Mercury Vidal & Horne (2003) Tubifex tubifex
Di spersal phenotype Maternal parasitism Sorci et al. ( 1994) Lacerta vivipara
Massot & Clobert ( 1995) Lacerta vivipara
Maternal nutrition/competition Mousseau & Dingle ( 1991) Aphidae
Diapause Temperature, photoperiod Reviewed in Mousseau & Many insects
Dingle (1991)
Sex determination Maternal nutrition Warner et al. (2007) Amphibolurus muricatus
Rev iewed in Cameron (2004) Mammalia
Di sease resistance Pathogen exposure Grindstaff et al. (2006) Ficedula hypoleuca
Environmental quality Mitchell & Read (2005) Daphnia magna
225
in offspring phenotype was an adaptive strategy by which mothers produced offspring that were
more likely to escape a poor nutritional environment. Similarly, Marshall (in press) found that when
Bugula neritina mothers were exposed to a brief pollution stress (copper), they produced larvae
that swam for longer than larvae produced by unexposed mothers. Marshall (in press) also found
that offspring from pollution-stressed mothers were more resistant to that pollutant themselves. If
maternal experience is a good predictor of the likelihood of pollution stress, then mothers may be
manipulating the phenotype of their offspring such that they are more likely to escape that stress
and be more resistant to exposure themselves.
Maternal experiences of competition may also affect offspring phenotype. Allen et at. (2008)
found that Bugula neritina colonies that had experienced high levels of competition produced more
dispersive offspring than colonies that had not experienced competition. In a rare example in fish,
Kerrigan (1997) found that if Pomacentrus amboinensis mothers experienced competition, they
produced larvae that were longer with larger heads, possibly to increase their ability to resist com-
petition themselves. Overall, it is likely that mothers manipulate the phenotype of their offspring
according to local conditions in a range of ways in the marine environment but most of the potential
effects on offspring phenotype remain largely unexplored.
Maternal environmental effects

Most of the maternal effects that have been discussed thus far have focused on changes in the off-
spring phenotype that are largely due to the maternal phenotype. However, there is another type of
maternal effect by which the maternally determined environment directly affects the performance
of the offspring either before release from the mother or after release. For example, the exposure of
amphipod mothers to hypoxic conditions can kill brooded offspring before they are even released
from the brood chamber (Wiklund & Sundelin 2001). Thus, regardless of offspring genotype, their
performance is affected by the maternal environment. Post-release maternal environment effects
are likely to occur in offspring that show low dispersal initially after release from the mother and
can take two forms. The first maternal environment effect occurs because offspring essentially
'inherit' the environment of their mothers and so offspring performance will be determined by
where they are released. In species with mobile mothers this effect can be mitigated by maternal
choice of release location and time as discussed above but for sedentary or sessile organisms, off-
spring will (at least at first) inherit the environment in which their mothers occurred. The ultimate
effect of inheriting the maternal environment will also depend on the degree to which offspring can
disperse and the scale of environmental variation. Nevertheless, for some species for which off-
spring dispersal does not exceed the scale of environmental variation, offspring performance may
be strongly influenced by the maternal environment and there may be a (non-genetic) correlation
between offspring maternal performance due to this maternal environment effect.
The second maternal environment effect that may occur is through differential female fecundity.
Offspring from highly fecund mothers will experience (at least initially) higher sibling competition
than offspring from less-fecund mothers. Again, if offspring are highly dispersive, then this effect
is probably uncommon but if offspring are likely to encounter/compete with siblings then this will
affect their overall performance. Interestingly, McGinley et at. (1987) predict that larger (and thus
more fecund) mothers should produce larger offspring than smaller mothers because these offspring
are more likely to experience competition and may require more resources. The predictions of
McGinley et at. (1987) appear to be supported by Einum & Fleming (2002), who suggest that mater-
nal body size-offspring size correlations are more common in fish with benthic-developing eggs
than in fish with pelagic eggs. Competition for resources may not be the only maternally induced
environmental effect that offspring may experience. The number of siblings that an offspring is
released with (i.e., maternal fecundity) may also affect its chances of being preyed upon (Leslie
226
2005) and, in benthic egg masses, its oxygen environment (Strathmann & Chaffee 1984, Booth
1995). These ideas have not been explored in marine organisms in depth but it is worth noting that
the maternal environment itself is capable of affecting offspring phenotype and maternal fecundity
can also be an important determinant of offspring environmental conditions.
Constraints on anticipatory maternal effects

Throughout this review the pervasive nature of maternal effects has been highlighted and the preva-
lence of maternal effects in other systems emphasised. However, it is not the authors' wish to pro-
vide an unbalanced view of maternal effects: maternal effects will not always occur, will certainly
not always be adaptive for either offspring or mother and will not always persist. In this section
some of the constraints on maternal effects are reviewed, specifically why AMEs may not always
occur despite the clear benefits of such effects. First, AMEs will be considered as a form of adaptive
(transgenerational) phenotypic plasticity.
There must be constraints on adaptive transgenerational phenotypic plasticity; if there were not,
mothers would be able to consistently match the phenotype of their offspring to the environment.
The constraints on maternal effects as adaptive phenotypic plasticity across generations are similar
to the constraints on adaptive phenotypic plasticity within a generation. The difference between
the two is that for AMEs the environmental cue is experienced by the mother and the effect is on
the offspring phenotype, whereas for adaptive plasticity the environment of one individual induces
a phenotype change in that same individual. DeWitt et al. (1998) classed adaptive plasticity con-
straints into costs and limitations and, in terms of maternal effects, the costs and limitations may
act on the mother, offspring or both. DeWitt et al. (1998) lists nine costs and limitations that may
constrain the evolution of adaptive phenotypic plasticity (Table 7) and whilst there has been some
debate over this list (van Kleunen & Fischer 2005), it is here regarded as a useful base for consider-
ing this issue. Each of these costs and limitations is likely to apply to AMEs and whilst exploring
each of these in detail is beyond the scope of this review, what are believed to be the most prevalent
and likely in the marine environment are highlighted. These are (I) information acquisition costs,
(2) production costs, and (3) information reliability limits.
Information acquisition costs

There are a number of costs associated with mothers acquiring information about the offspring
environment so that they can adjust the phenotype of their offspring appropriately. DeWitt et al.
(1998) highlight the costs of producing and maintaining sensory structures as a cost based on mor-
phology but the act of gaining in formation about the habitat of the offspring may also have an asso-
ciated cost. For example, ovipositing mothers may need to search multiple habitats before releasing
their offspring, which is at least energetically expensive and at worst carries some predation risk
(S tamps et al. 2005).
Production costs
Some phenotypes are simply too expensive to produce. For example, if competition is extremely
high and offspring require massive amounts of resources to survive, mothers may still not increase
their per-offspring investment because it would dramatically reduce their fecundity. Overall if the
costs of 'rescuing' the phenotype of offspring outweigh the benefits, then AMEs in this situation
are unlikely (Bernardo l996a,b). There is another form of production cost that is particularly rel-
evant to marine organisms with complex life cycles: trade-offs among life-history stages. In this
review we noted the example of Ciona intestinalis, for which larger offspring were favoured in one
life-history stage but smaller offspring were favoured in another (Marshall & Keough 2003b,c,
Marshall & Bolton 2007). In frogs, for example, a predator-resistant larval phenotype results in a
227
Table 7 Modified table from DeWitt et al. (1998) summarising the potential costs
and limitations of transgenerational phenotypic plasticity
Costs
Maintenance Costs of producing and maintainin g structures used to sense and predict offs prin g environment,
costs incurred by mothers
Production costs Costs of producing the desired phenotype, incurred by mothers (e.g., provisioning offspring to
increase offspring size) or by offsprin g (mother induces a response for the offspring to change
phenotype, e.g., grow spines in response to predation)
Information Costs of acquiring information about the environment the offspri ng will experience (e.g., risk of
acquisition costs predation to mothers, energetic cost of search behaviour in oviposition)
Developmental Increased plasticity may result in increased developmental problems (e .g., functional asymmetry)
instability
Genetic costs Pleiotropic effects of havin g a plastic phenotype whereby more plastic genotypes perform poorly in
stable conditions
Limitations
Information Mothers limited in their ability to predict the environment when an environmental cue (information)
reliability limit is not present or is unreliable
Lag-time limit Offspring phenotype must be expressed within a certain time from when the mother experiences the
cue; transgenerational plasticity can be limited if the environment changes before the offspring's
phenotype can be expressed or the phenotype is not expressed fast e nough
Developmental Plasticity may not be able to produce extreme offspring phenotypes in extreme environments;
range limit non-plasti c offspring phenotypes may be better suited to those extreme environments and have
higher fitness over plastic phenotypes , in such environments non -plastic offspring are favoured and
plasticity is limited
Epiphenotype When offspring phenotypes are 'added' onto existing phenotypes, they are termed epiphenotypes; if
limit these epiphenotypes are weaker than phenotypes induced during early development, then plasticity
is limited
lower-quality adult phenotype (Relyea 2000, 2001). Thus selection on the entire life hi story will
determine whether transgenerational plasticity carries a survival advantage or not.
Information reliability limits

If there is no cue to the likely environment of the offspring, then it is impossible for mothers to
adaptively adjust the phenotype of their offspring. A lack of a reliable cue could be due to the
maternal environment and offspring environment being displaced in space or time. If offspring
initially disperse at a scale that exceeds the scale of environmental variation, then mothers will be
unable to adjust the phenotype of their offspring accordingly. Similarly, if the environment varies
unpredictably over short timesca les, then mothers wi II be unable to produce offspring of the appro-
priate phenotype. Such limitations are likely to occur in marine organisms with highly dispersive
larval stages and initial evidence supports this finding. Marshall et al. (in press) found that marine
invertebrate species with non-dispersing offspring show greater variation in offspring phenotype
(size) among mothers than species with dispersing offspring. They also found that there was more
variation within individual broods in species with dispersing offspring, suggesting that in these
species, mothers are using diversified bet hedging to cope with uncertainty regarding the likely
habitat of their offspring (Marshall et al. in press). More generally, it is predicted that AMEs will
be found to be more common in marine organisms with less-dispersive offspring relative to species
that produce larvae that disperse to other habitats. Note that this does not necessarily preclude spe-
cies with larval stages from expressing AMEs. For example, species of copepod release larvae in
the water column but these larvae are likely to exist in the same habitat as the mother as the scale
228
of environmental variation in this environment probably does not exceed the scale of dispersal and
AMEs have been shown in this group (Guisande et al. 1996).
Other constraints on maternal effects

There has been long-standing and vigorous debate regarding who has 'control' over offspring
phenotypes and particularly maternal care (Trivers 1974, Godfray 1995, Livnat et al. 2005). Whilst
parent-offspring conflict probably occurs in marine organisms, the authors can find few examples
of offspring having 'control' over their own phenotype and many of the studies discussed in this
review strongly suggest that mothers determine offspring phenotype. One potential example is that
of the diminutive seastar Parvulustra parvivipara. This species broods its offspring in brood cham-
bers where sibling cannibalism occurs and fully formed juveniles that are a quarter of her size can
emerge from the mother (Byrne et al. 2003, Byrne 2006). In this instance, mothers may be unable
to control the size of her offspring such that offspring may emerge that are larger than what would
maximise her fitness. Nevertheless, it is suspected that parent-offspring conflict will be rare with
regard to the types of maternal effects discussed in this review but it is noted that such conflict can
act as a constraint on maternal effects generally.
Physiological constraints will also constrain maternal effects, particularly regarding offspring
size. In some species, the optimum offspring size may simply be too large for mothers to produce
(due to morphological constraints; e.g., Congdon & Gibbons 1987) or too large for oxygen diffusion
to work effectively. Thus the optimum phenotype for mothers to produce may be inaccessible and
mothers may produce offspring with a suboptimal phenotype.
The importance of maternal effects in marine systems

Whilst maternal effects are important in any system, there are a number of specific elements of
maternal effects that make them of particular interest in marine systems. In this section, the theoret-
ical considerations of maternal effects are first reviewed and then the importance of maternal effects
in the marine environment is considered from both an ecological and an evolutionary perspective.
Theoretical considerations
Maternal effects can affect a number of crucial traits in offspring, the effects of which have been
considered in theoretical studies. Whilst few theoretical studies have examined marine organisms
specifically, there is a range of general maternal effects models that are worth considering. Elkin
& Marshall (2007), Fowler (2005), and Stamps (2006) explore the role of maternal effects in the
dispersal and habitat selection of offspring. Fowler (2005) demonstrated that maternal effects could
have a stabilising effect on (otherwise chaotic) population dynamics. Furthermore, it appears that
the presence of maternal effects on populations can result in population cycles or oscillations over
the scale of four populations or longer. A similar cyclic effect of maternal effects of population
dynamics has been suggested by Ginzburg (1998) but this model did not examine maternal effects
on dispersal specifically. Stamps (2006) presented an interesting modification of an earlier model
(Stamps et al. 2005) showing that dispersers that receive more energetic reserves from their moth-
ers are more likely to settle in higher-quality habitat. Elkin & Marshall (2007) specifically examine
the effect of offspring provisioning on dispersal in marine invertebrates and show that when there
are large differences in habitat quality, offspring that have more reserves are more likely to settle in
higher-quality habitats than offspring with fewer reserves.
Whilst some models have suggested that maternal effects will have a stabilising effect on popu-
lation dynamics, there is no clear consensus with many other models suggesting that maternal effects
will actually have a destabilising effect (reviewed in Plaistow et al. 2006). This is because maternal
229
DUSTIN 1. MARSHALL, RICHARD M. ALLEN & ANGELA 1. CREAN
effects can introduce a 'delayed density-dependence' by which there is a time lag between an envi-
ronmental change (e.g., a decrease in carrying capacity) and a population response (e.g., Rossiter
1994, Lindstrom & Kokko 2002). Whilst the role of maternal effects in decreasing or increasing
population stability remains unclear, what is certain is that maternal effects can act as a powerful
force linking events in one generation to the population dynamics of the next. Overall, maternal
effects are likely to phenotypically link generations in the marine environment but this idea has
received little attention in the marine environment. This is remarkable given that links among gen-
erations may also constitute links among populations and this idea is discussed further below.
Ecological perspective
Maternal effects, sublethal effects and the production of recruits
In marine systems, the production of recruits in any single population is largely viewed as a prod-
uct of the number of reproductive adults and their average reproductive success. The existence of
maternal effects, particularly the effect of offspring size/quality, suggests that other factors such as
environmental quality should also be considered. Obviously, environmental factors will affect the
number and fecundity of adults but there is also the potential for more subtle effects on offspring
quality. For example, any decrease in the availability of food may not only reduce fecundity, it may
also reduce the size of offspring that are produced. Because smaller offspring are likely to have a
lower chance of surviving, a decrease in food availability may dramatically reduce future recruit-
ment through the combined effects of decreased offspring quantity and quality.
The impact of sublethal effects on population dyna mics is only just being recognised . Sublethal
effects such as competition and injury from predation can have subtle effects on the production of
offspring and, more importantly, the size/quality of offspring (Bernardo & Agosta 2005). Whilst
these effects have received little attention in marine systems, it is likely that there are a range of bio-
logical interactions that result in a reduction in the quality of offspring produced by mothers in that
population. Overall , it is emphasised that reductions in fecundity are not the si ng le factor related to
the production of recruits in marine systems. Rather, maternal effects constitute a link between the
maternal environment, the maternal generation and the offspring generation, which creates the pos-
sibility for a range of environmental factors to have cascading and potentially dramatic effects.
Marine populations: demographically open but phenotypically closed?

Most marine organ isms have a dispersive larval stage that can travel among popul ations. Traditionally,
marine populations have been viewed as demographically 'open ,' by which larvae di sperse among
populations and the population dynamics of any single population is not determined solely by the
local production of recruits (Underwood & Fairweather 1989, Caley et al. 1996, Underwood &
Keough 2001). More recently, this view has been challenged: studies of reef fish and mussels sug-
gest that marine populations may not be as open as previously thought, with up to 60% of recruits
locally derived from the same population (Jones et al. 1999, Swearer et al. 1999, Becker et al. 2007).
It is likely that for any single population, some recruits will be locally derived and others will be
from other populations but generally speaking, species with longer larval planktonic periods will
probably have lower rates of self-recruitment than species with shorter planktonic periods (Shanks
et al. 2003). Regardless of the relative levels of self-recruitment, the dynamics of any single marine
population will rarely be completely independent from the input of recruits from other popula-
tions and overall, most marine populations are viewed as being somewhat demographically linked.
However, little attention has been paid to whether marine populations are linked phenotypically.
In demographically open marine systems, events in one population can affect the population
dynamics through changes in the production and transport of larvae (Caley eta I. 1996). At its most
extreme, some populations can act as sources for larvae whilst others can act as sinks by which
230
there is no net production of recruits in that population and these dynamics have interesting implica-
tions for the management of marine populations (Crowder et al. 2000, Armsworth 2002, Figueira
& Crowder 2006). While it is now recognised that populations are not demographically indepen-
dent, populations are typically viewed as phenotypically independent. An implicit assumption of
most marine meta-population theories is that the mean phenotype within any single population is
independent of the average phenotype of other populations. However, the existence of maternal
effects suggests that this assumption may not be appropriate. Consider an environmental stress that
affects Population A and changes the mean phenotype of reproductive mothers in this population.
This change in maternal phenotype then translates (via a maternal effect) into a change in the mean
phenotype of the offspring produced in Population A. If these offspring then disperse and success-
fully recruit into Population B, then the mean phenotype of Population B will change despite no
environmental change occurring in this population. Of course, this assumes that the scale of larval
dispersal exceeds the scale of the environment stress. Nevertheless, the existence of maternal effects
suggests that marine populations may be 'phenotypically open', by which changes in phenotype
in one population lead to changes in phenotype in another population independent of the initial
stimulus (Figure 2). This maternal effect-mediated link between the phenotype of settling larvae
and their source population environment has some interesting imp I ications for connectivity in the
marine environment.
In the marine environment, different populations of the same species can show remarkable dif-
ferences in their average phenotypes (Keough & Chernoff 1987, Yamada 1989, Bertness & Gaines
1993, Warner 1997, Wright et al. 2000). Warner (1997) speculates that population-level differentia-
tion is due in part to phenotypic plasticity and in part to local genetic differentiation. The present
authors agree but suggest that there is another element that is not being considered: maternal effects.
Throughout this review instances for which mothers adaptively manipulate the phenotype (e.g.,
offspring size, pollution resistance) of their offspring have been highlighted. Obviously different
phenotypes will be better suited to different conditions and so one could imagine an instance when
mothers in one population produce offspring that have the 'best' phenotype for that local population
but that phenotype performs poorly in other locations. If so, then externally derived settling larvae
may have a lower chance of surviving and recruiting into another population because their moth-
ers have given them the 'wrong' phenotype. Thus maternal effects may act to reduce connectivity
(A)b 0 0
(B)
---£4
0 0 0
____,.
(C)
Q Q
0
--4
0 @
Figure 2 Schematic showing potential role of maternal effects in linking phenotypes between populations .
In panel (A), two populations with the same average phenotype (indicated by the open ellipses) and propagules
(with the same phenotype) dispersing from the population on the left. An environmental stress occurs in the
popul ation on the left and in panel (B), the mean phenotype of the left population changes in response to the
stress (indicated by shading). In panel (C), the mean phenotype of offspring dispersing to the population on
the right has changed (via maternal effects) and the mean phenotype of the population on the right has been
modified (as indicated by shading).
231
{A)b
•
(B)
•
(C)
Figure 3 Schematic showing potential role of maternal effects in decreasing connectivity between popula-
tions. In panel (A) the populations share the same phenotype and are well linked demographically (ind icated
by arrows) but an environmental stress occurs in the population on the left. In panel (B) the mean phenotype
of the population on the left has changed in response to the stress and thus so has phenotype of the propagules
(due to maternal effects). In panel (C) the demographic links among the populations have disappeared because
the phenotypes of the exogenous propagules are poorly matched to the local environment.
among marine populations because they result in a 'mismatch' in phenotypes among environments,
biasing recruitment success in favour of local recruits (Figure 3).
There are two scenarios by which maternal effects (and thus phenotypic links among popula-
tions) can alter marine populations: changes in mean phenotype in one population due to recruit-
ment from another population and decreased connectivity due to a phenotypic mismatch among
populations. The relative likelihood of each of these effects will ultimately depend on the propor-
tion of propagules exchanged between populations and the costs and benefits of maternally induced
phenotypes across different environments. If the maternally induced phenotype does reasonably
well in both populations (e.g., increased offspring size), then maternal effects are unlikely to reduce
connectivity. However if, for example, mothers produce offspring that are pollution resistant but are
poor competitors in the absence of pollution (Marshall in press), then these offspring are unlikely to
successfully recruit into pollution-free populations.
Implications for fisheries management

Many marine fisheries are under intense fishing pressure and most major exploited fish popula-
tions have dramatically declined (Hutchings & Reynolds 2004). Furthermore, many fisheries are
remarkably slow to recover once exploitation has ceased (Hutchings 2000). Maternal effects may be
implicated in the collapse and failure to recover of marine fisheries. As noted in this review, larger,
older mothers produce higher-quality offspring that have a great chance of surviving. Many fisher-
ies selectively remove larger fish and decreases in the mean size of exploited stocks are common
(Swain et al. 2007). Furthermore, changes in the mean size of reproductive females can be associ-
ated with (and possibly precipitate) fisheries collapses (Olsen et al. 2004). These lines of evidence
strongly suggest that the effective contribution of older, larger fish to the next generation of recruits
is far greater than previously recognised and this maternal effect could play a significant role in
the recruitment of exploited stocks (Berkeley et al. 2004). Ignoring this maternal effect and the
impact of size-biased fishing could be responsible for a number of fisheries collapses and some have
recommended that larger fish be protected on this basis (Birkeland & Dayton 2005). In contrast to
this recommendation, some models suggest that maternal age effects on offspring quality will not
have major effects on the effects of size-based exploitation (O'Farrell & Botsford 2006). The pres-
ent authors believe it is likely that larger mothers produce offspring that have far greater chances of
survival (either due to producing higher-quality offspring or spawning in higher-quality sites, and
232
the like) and future fisheries management strategies should incorporate age-/size-based maternal
effects.
Implications for aquaculture

The importance of maternal effects for terrestrial agriculture has long been recognised and a similar
realisation has begun in aquaculture (Cruz & Ibarra 1997, Deng et al. 2005, Eriksen et al. 2006). As
described throughout this review maternal phenotype (often referred to as 'condition' in aquacul-
ture studies) can dramatically affect the survival and performance of offspring and has the poten-
tial to dramatically affect yields in aquaculture breeding programmes. However, the relationship
between maternal condition and progeny quality is again unlikely to be a simple 'high-quality food
in -t high-quality offspring out' situation. When conditions are benign, mothers can benefit from
producing smaller (lower-quality) offspring and gaining a fecundity benefit (Brockelman 1975).
Thus aquaculturists may inadvertently be creating conditions that result in a decrease in the quality
of offspring that are produced. Initial evidence in freshwater systems suggest that this can happen
(Heath et al. 2003). Clearly, the maternal environment will determine the quality of offspring that
are produced and it is predicted that the study of maternal effects will become increasingly impor-
tant in aquaculture.
Evolutionary perspective
Do maternal effects retard or facilitate species' range expansions?
In the preceding section there was discussion of the potential for maternal effects to reduce popu-
lation connectivity when different environments stimulate mismatched phenotypes among popula-
tions. Such an effect would tend to reduce the probability of a species expanding its range as it is
possible that a mother at the edge of the species range will produce an offspring with the 'wrong'
phenotype for beyond that range. There is another mechanism by which maternal effects may retard
species' range expansions. If the quality of habitat decreases as one moves from the centre of a pop-
ulation to the edge, then mothers may have fewer resources with which to provision their offspring
at the edge of the range. If offspring provisioning affects recruitment success (which is likely) then
this may result in fewer successful recruits being produced at the edge of the species range and thus
reducing the rate of expansion.
Whilst it is argued above that maternal effects can retard species' range expansions, maternal
effects could alternatively play a role in expanding species' ranges, particularly regarding invasion
by exotic species. Buckley et al. (2003) found invasive populations of Scotch broom, Cytisus sco-
parius, produced larger seeds than native populations and speculated that this could have facilitated
the invasion of this species. Einum & Fleming (2004) argue that when environmental conditions
are uncertain , mothers should produce larger offspring than usual to ensure survival regardless
of local conditions. It may be that the maternal effect of increased offspring size allows invasive
marine species to colonise new habitats successfully but this has not been tested as far as the pres-
ent authors are aware. An intriguing study would be to examine the size of offspring in native and
invasive populations of a marine organism and determine whether the patterns shown by Buckley
et al. (2003) also occur in the marine environment. Overall, the role of maternal effects in species'
range expansions depends on whether the maternal effect is an AME or a SME; the former will
facilitate the expansion, the latter will retard the expansion.
Evolution of pollution resistance

Many marine organisms associated with anthropogenic habitats show increased resistance to anthro-
pogenic pollution (e.g., Hoare et al. 1995, Martinez & Levinton 1996, Wallace et al. 1998, Levinton
et al. 2003, Mouneyrac et al. 2003, Daka & Hawkins 2004, Rainbow et al. 2004, Piola & Johnston
233
2006). A strong maternal effect for pollution resistance has been demonstrated for a number of
aquatic species for which exposure to a pollutant in the maternal generation increases pollution
resistance in the subsequent generation (Munkittrick & Dixon 1988, 1989, Lin et al. 2000, Vidal &
Horne 2003, Marshall in press). The role of transgenerational phenotypic plasticity in the genetic
evolution of traits remains unclear (Price et al. 2003) but it is possible that the maternal effect of
pollution resistance facilitates the genetic evolution of pollution resistance in the sea. Studies that
examine the relative role of genetic evolution and maternal effects in determining the resistance of
marine populations to pollution would be welcomed.
New approaches and directions

The need for more studies on maternal effects in the marine environment generally has been identi-
fied but in this section the emphasis is on some species approaches and directions that may be valu-
able for investigating maternal effects.
Quantitative genetics approaches

Quantitative genetics approaches have long been used to partition variation associated with mater-
nal effects and describe variation in traits due to additive genetic variance (Falconer 198 1). Thus,
these approaches can be invaluable for estimating the importance of maternal effects relative to
other influences (Heath & Blouw 1998, Heath et al. 1999) but they have been underutili sed in
marine studies. This is despite the fact that many marine organisms are broadcast spawners, which
allows the use of quantitative genetics desig ns typically only available to those studying plants.
Because sperm and eggs from multiple individuals can be crossed in many combinations in broad-
cast spawners, diallel and 'North Carolina II' designs can be used to examine maternal effects
(Lynch & Walsh 1998). Such designs have been used successfully to examine a range of traits in
marine broadcast spawners, particularly in aquaculture studies (Boudry et al. 2002, Deng et al.
2005, Evans & Marshall 2005, Marshall & Evans 2005, Ivy 2007) and these powerful tools could
be used more frequently for examining maternal effects in the sea.
Marine algae
Throughout this review the focus has been on marine fish and invertebrates and marine algae have
largely been ignored. This was not a deliberate strategy; examples of maternal effects in this major
and important group were not found . The authors suspect that maternal effects are as prevalent and
important in marine algae as other groups and believe that thi s would be a fruitful line of research,
particularly given that there are indications that release time and recruit size can affect a number of
key performance traits in this group (Sante! ices et al. 2003)
Paternal effects
Throughout this review the focus has been on maternal effects, but associated literature searches
have yielded some very interesting (non-genetic) paternal effects on offspring performance. In fish
particularly, fathers can have strong effects on a number of key offspring traits and paternal brood
care, cannibalism and selection/defence of the nesting site are all very important determinants of
offspring success (Knapp & Kovach 1991 , Payne et al. 2002, Karino & Arai 2006). Obviously, there
are also strong paternal effects on offspring performance in sex role-reversed pipefish (Berglund
et al. 1986, 1997, Berglund & Rosenqvi st 2001). Whilst such effects are less likely in species
234
without brood care there are a number of other paternal effects that have gone largely untested in
marine organisms despite some remarkable effects being documented in other groups. For example,
Galloway (2001a) found that the paternal environment affected the properties of offspring in the
plant Campanula americana. Whether similar effects exist in marine organ isms remains largely
untested: there may be some surprising paternal effects in the sea.
In most organisms, mothers determine the size of offspring that are produced and in the sea
this also holds to a certain extent. However, in marine broadcast spawners, the chances of an egg
being fertilised depends on its size because larger eggs are larger targets for sperm (Levitan 1996b,
Marshall et al. 2000, 2002). Thus at low sperm concentrations larger eggs are more likely to be
fertilised than smaller eggs and at high sperm concentrations, smaller eggs are less likely to suffer
lethal polyspermy (Marshall et al. 2002, 2004). This suggests that although mothers may determine
the range of zygote sizes that can be produced, males (or more specifically, the amount of sperm
that they release) will determine the final size of zygotes that are successfully fertilised. This sug-
gests that in marine broadcast spawners, the paternal (sperm) environment can change the size dis-
tribution of offspring produced in the field , a paternal effect that is probably unique to this group.
Conclusion
The present review has shown that maternal effects can act in a variety of ways to strongly influ-
ence the subsequent performance of offspring in the marine environment. However, it is recognised
that research on maternal effects in marine organisms has only just begun and their importance is
only beginning to be appreciated. This review forms only a first glance and summary of the field of
maternal effects in the marine environment. The authors anticipate that as interest in these effects
grows and matches that for maternal effects research in terrestrial systems, each of the broad types
of maternal effects addressed here will become its own subdiscipline and that a broad review such
as this will not be possible. The authors look forward to further research in this field and hope that
this review proves to be valuable for those interested in maternal effects in the sea.
Acknowledgements
During the preparation of this manuscript, D.J.M . was supported by grants and an Australian post-
doctoral fellowship from the Australian Research Council and R.M.A . and A.J .C. were supported
by Australian post-graduate awards. Tobias Uller, David Semmens, Jim Atkinson and Patrick Krug
provided valuable comments on the manuscript, which we greatly appreciate. We thank Patrick
Krug, Tobias Uller, Hugh Dingle, Mick Keough and Richard Emlet for stimulating discussions on
this topic . Part of this work stemmed from the "Maternal effects in the marine environment sympo-
sium" at the 2006 Larval Biology Conference at the Oregon Institute of Marine Biology.
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Colour Figure 1 (Birrell et al.) Different a lga l assemblages dominating reef habitats, creating large differ-
ences in the suitability of the habitat for coral replenishment. A. Crustose calcareous algae, especially from
the Order Corallinales, form a calcified cru st over the substratum and are genera lly associated with habitats
that promote cora l recruitment. B. Filamentous a lga l turfs, closely cropped by herbi vorous fishes and sea
urchins, create a low turf (1-5 mm in height), which is compatible with co ral recruitment. C. Aggregations
of Cyanobacteria (mi c roalgae) may form longer filaments (30- 100 mm in heig ht) and often generate hostile
chemica l conditions. D. Thick mats of larger, more robust corticated a lgae may create a dense layer over much
of the reef substratum (50- 150 mm in height), trappi ng sed iments a nd generating chemica l and nutrient co ndi-
tions that may be inimical to co ra l settlement and ea rl y recruits. E. A dense mat of the ep hemeral , corticated
brown alga, Chnoospora implexa , covering large a reas of reef and live cora ls (up to 500 mm hig h). Because
this mat was hi g hl y seaso nal , and short- li ved, it subseque ntly disappea red, with little apparent impact on the
underlying corals. The impac t of such a mat o n cora l reple ni shment would depend strongly on the timing
of the bloom relative to co ral spaw ning a nd settleme nt. F. Dense mat of the corticated, foliose brown a lga,
Lobophora variegata, covering cora ls killed during a mass bleaching event and rendering th e substratum
appare ntl y inaccessible to coral recruits. G. Ca nopy of the leath ery macrop hyte, Sargassum (brown a lga),
which may reach heights of up to 3-4m a nd densities of 100 plants m- 2 , pre-empting space for co ral recr uit-
ment a nd sign ifica ntl y a ltering light and hydrodynamic regimes.
Colour Figure 2 (Birrell et al.) Disturbance, algal colon i sation and effects of algae on coral recruitment.
A. Coloni sation of severely bleached cora l tissue by fine filamentous algae. Disturbances that lead to coral tis-
sue death usually result in colonisation of exposed coral skeleton by some form of benthic algae. Subsequent
succession may result in very different algal assemblages, with very different consequences for coral replen-
ishment. B. Overgrowth of damaged corals by the corticated, foliose brown alga, Lobophora variegata , has
dramatically reduced substratum avai lable for cora l sett lement. C. Healthy cora l recruit attached to a crustose
ca lcareous alga; such algae may enhance settlement of coral larvae. D. Coral recruit emerging from filamen-
tous algal turf. The recruit wou ld have been more strongly affected by physical and chemical conditions in
the turf during settlement and early growth. E. Acropora cora ls emergent from a dense mat of Lobophora
variegata (as in Band Figure I F). F. Leathery macrophytes (e.g., Sargasswn) may form an extensive canopy.
but st ill retain significant understorey substratum suitable for coral sett lement and recruitment, such as the
filamentous turfs shown here. G. Trapping of sediments by filamentous alga l turfs may enhance stress experi-
enced by coral recruits and significant ly reduce the su itabi li ty of habitat for their survival and growth.
Colour Figure 1 (Villanueva & Norman) Pl anktonic and benthic hatchlings in Octopodidae. Adult female
Wunderpus photogenicus 26 mm ML in laboratory carry ing egg strings with developing embryos within the
arm s (A) and hatchling (total length -3. 5 mm) from sa me egg mass (8). Note the well-developed dorsal mantle
cavity of the paralarvae. (Reproduced with permi ssion from Mi ske & K i rchhauser 2006.) Female Octopus
berrim a at the time of hatching in the laboratory with a benthic juvenile hatchling (total length - 20 mm) in
foreground (C) and within 10 min of hatching (D) showing well-developed arm s and chromatic and sculptural
components of the skin . (Photos: David Paul.)
Colour Figure 3 (Villanueva & Norman) Individua ls of Octopus vulgaris fro m hatching to settl ement
obta ined from rea ring ex periments described in Vill a nu eva (1995). Images not to sca le. Age (days) a nd
ma ntle length (ML) of th e indi viduals measured fresh are (A) 0 days, 2.0 mm ML; (B) 20 days, 3.0 mm
ML; (C) 30 days, 4.3 mm ML; ( D) 42 days, 5.9 ML; (E) 50 days, 6.6 mm ML; (F) 60 days. 8.5 mm ML.
Octopuses fro m thi s ex periment settl ed between 47 and 54 d ays. Indi vi du als were photog raphed un der anaes-
thesia (2% eth anol) potenti all y causing chromatophore co ntraction in so me cases. (Photos by Jea n Leco mte.
Obse rvatoire Ocea nologique de Banyul s, C NR S. Reprodu ced with permission fro m Vill anu eva et al. 1995 .
modifi ed.)
Colour Figure 4 (Villanueva & Norman) Micronektonic octopus paralarvae. Top, unidentified para larva
of the genus Callistoctopus from the Coral Sea, Australia, show ing longer dorsal arm pair. (Photos: David
Paul.) Centre, unidentified paralarva (Macrotritopus sp.?) from Hawai i showi ng long arms relative to body
length. particu larl y the third pair. (Photos: Chris Newbert.) Bottom , unidentified paralarva from Hawaii .
(Photos: Jeffrey Rotman.)
Colour Figure 6 (Villanueva & Norman) Unidentified paralarva from the Coral Sea, Australia, showing
arms of equivalent length (left). (Photo: David Paul.) Para larva of Macrotritopus defilippi from Caribbean Sea
showing longer third arm pair (right). (Photo: Raymond Hixon.)
Colour Figure 7 (Villanueva & Norman) Chromatophores contracted (left) or expanded (right) on the head
of para larvae. The left image corresponds to an unidentified para larva of unknown genus and the right image
is from an unidentified paralarva of the genus Callistoctopus. Both individuals from Coral Sea, Australia.
(Photos: David Paul.)
Colour Figure 9 (V illanueva & Norman) Iridescence in octopus paralarvae. Left, unidentified paralarva
showing scattered points of iridescence, potentially from Kolliker organs in skin. Right. Amphioctopus sp.
para larva showing iridescent tissue in location of ocelli of ocellate octopuses. Both individuals collected while
night diving on a moonless night at-10m deep over a seafloor depth of 450 m at Osprey Reef, Coral Sea.
Australia. Photographs taken in shipboard aquaria immediately after capture. (Photos: M.D. Norman .)
Colour Figure 10 (Villanueva & Norman) Hapalochlaena maculosa hatchling, a direct benthic species,
showing well-developed skin colour and sculpture. (Photo: David Paul.)
Colour Figure 16 (Villanueva & Norman) Adult Octopus cyanea in camouflage display amongst soft cor-
als, Puerto Galera , Philippine Islands. (Photo: Gunther Deichmann.)
Colour Figure 26 (Villanueva & Norman) Planktonic paralarva of Octopus warringa within 10 min of
hatching in the laboratory showing short arms, transparent muscul ature. simple chromatophores and ex ternal
yolk sac (wi thin arm crown). (Photo: David Paul.)
Colour Figure 43 (Villanueva & Norman) Unidentified paralarva of th e genus Ca llisroctopus from th e
Coral Sea. Australia , showing elongate form when swi mming. Photograph taken in situ while night diving on
a moonless night at-10m deep over a seafloor depth of 450 m at Osprey Reef, Cora l Sea. Australia . (Photo:
M .D. Norman.)
Colour Figure 44 (Villanueva & Norman) A dense swarm of Octopus rubescens wi"th the j elly fi sh
(Phacellophora carntschatica) photographed 26 June 2003 at II ISh loca l time from th e ROY YENTANA at a
depth of about 60 m in 728 m of water in th e M onterey Submarine Canyon, north-east Pacific. Temperature
9°C and oxygen concentrati on 2.66 ml 1- 1• No euphausiids were observed on the di ve tape. (Image and data
reproduced with permi ssion from M onterey Bay Aqu arium Research Institute, ©2003, MBARI.)
Colour Figure 45 (Villanueva & Norman) Ephyra larval stage of j elly fi sh scyphomedusa feeding on
un identi fied octopod paralarva. Speci mens coll ected using a plankton net at about 180m depth, off Li za rd
Island. Great Barri er Reef. ( Data and image reproduced with permi ssion from Peter Park s/im agequestm arine.
com.)
Strontium Barium
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s
:l
:;
s 48°
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460 460
75 50 (fall) 50 (win ter)
B
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48° 48°
46° 46°
64° 60° 56" 64° 62° 60° 56°
Colour Figure 3 (Elsdon et al.) Vari atio n in di ssolved stro ntium and barium concentratio ns in the Gul f of
St. Lawrence, Ca nad a, showing spatia l va ri ati o n (within each plot) and tempora l va ri ati on between seasons
fo r stro ntium , comparing fa ll (A) with winter (8 ); barium , compa ring fa ll (C) with w inter ( D). Va lues in parts
pe r mi lli on. (S.E. Ca mpan a unpub lished data.)
8
Sr:Ca
9.4
8.2
Colour Figure 4 (Elsdon et at.) (A) Sea surface temperatures (SSTs) collected during the upwelling season
along centra l Ca lifornia (5-19 June 2006; National Oceanic and Atmospheric Administration Coast Watc h
program) and representing (B) the Ba:Ca ratios (J..Lmol mol - 1) and (C) Sr:Ca rati os (mmol mol- 1) coll ected dur-
ing the same upwelling season ( B. Wells & K . Stierhoff unpubli shed data, figure prepared by K . Stierhoff).
White arrows represent region s of active upwelling and the black arrow represents in fusion of sa line, warmer
waters from farther off shore into the region . Note: Variability in Ba:Ca is derived largely from th e distribution
of upwelling in the region and wi ll vary with the degree and timing of upwelling.
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Years
Colour Figure 1 (Leggett & Frank) Ordination of the time of series of spawning stock biomass
of various species from scientific surveys conducted throughout the north-west Atlantic, illustrating
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of colours is proportional to the magnitude of the standardized anomaly in standard deviation units.
Alphanumeric labelling refers to the Northwest Atlantic Fisheries Organization management unit.
Oceanography and Marine Biology: An Annual RevieiV, 2008, 46, 251-296
© R. N. Gibson , R. J. A. Atkinson , and J. D. M. Gordon , Editors
Taylor & Francis
EFFECTS OF CLIMATE-INDUCED CORAL

BLEACHING ON CORAL-REEF FISHES-
ECOLOGICAL AND ECONOMIC CONSEQUENCES
MORGANS. PRATCHETT 1, PHIUP L. MUNDAYu, SHAUN K. WILSON3 ,
NICHOLAS A.J. GRAHAM 3 , JOSHUA E. CINNER 1, DAVID R. BELLWOODu,
GEOFFREY P. JONESt. 2 , NICHOLAS Y.C. POLUNIN 3 & TIM R. MCCLANAHAN4
'ARC Centre of Excellence for Coral Reef Studies, and 2School of Marine and
Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
E-mail: morgan.pratchett@jcu.edu.au
3 School of Marine Science & Technology, University of
Newcastle, Newcastle-upon-Tyne N£1 7RU, UK

4
Wildlife Conservation Society, Marine Programs, Bronx, NY, 10460-1099
Abstract Global climate change is having devastating effects on habitat structure in coral-
reef ecosystems owing to extreme environmental sensitivities and consequent bleaching of reef-
building scleractinian corals. Coral bleaching frequently causes immediate loss of live coral
and may lead to longer-term declines in topographic complexity. This review identifies coral
cover and topographic complexity as critical and distinct components of coral-reef habitats that
shape communities of coral-reef fishes. Coral loss has the greatest and most immediate effect on
fishes that depend on live corals for food or shelter, and many such fishes may face considerable
risk of extinction with increasing frequency and severity of bleaching. Coral loss may also have
longer-term consequences for fishes that require live corals at settlement, which are compounded
by devastating effects of declining topographic complexity. Topographic complexity moderates
major biotic factors , such as predation and competition, contributing to the high diversity of
fishes on coral reefs. Many coral-reef fishes that do not depend on live coral are nonetheless
dependent on the topographic complexity provided by healthy coral growth . Ecological and eco-
nomic consequences of declining topographic complexity are likely to be substantial compared
with selective effects of coral loss but both coral cover and topographic complexity must be
recogni sed as a critical component of habitat structure and managed accordingly. Urgent action
on the fundamental causes of climate change and appropriate management of critical elements
of habitat structure (coral cover and topographic complexity) are key to ensuring long-term per-
sistence of coral-reef fishes.
Introduction
The world's climate is constantly changing and has a major influence on all biological processes,
species and ecosystems. Most notably, extreme and rapid shifts in climatic conditions have a per-
vasive influence on temporal patterns of biodiversity; major episodes of species extinctions (e.g. ,
the end-Permian extinction event) and diversification are strongly associated with periods of rapid
climate change (e.g., Sepkoski 1998 , Benton & Twitchett 2003). Currently, mean atmospheric tem-
peratures are increasing at a largely unprecedented rate, with concomitant changes in many other
climatic variables (e.g., rainfall , incidences of extreme climate events). The current ongoing rate of
251
MORGANS. PRATCHETT ET AL.
Table 1 Exponential increase in research on ecological

effects of global climate change within marine and
freshwater environments
Topic of research
Decade Climate change +Ecology +Marine & freshwater
1972- 1979 54 0 0
1980-1989 136 2 0
1990-1999 11,190 1054 17
2000-2007 19,259 2854 123
Total 30, 160 3910 140
Note: Data represent numbe rs of Institute for Scientific Information
(lSI) publi shed papers included under each topic (climate
change, ecology, and marine and freshwater research) co nsid -
ered hierarchically (records start in 1972).
warming (-0.02°C yr- 1) is greater than at any time in the last 1000 yr, largely due to anthropogenic
activities (Houghton et al. 2001, Jones & Moberg 2003, Houghton 2005). Atmospheric temperatures
have been much higher (up to l0°C warmer) in the geological past, but recent temperature increases
follow a long period of relative stability and current climatic conditions have not been experienced
for more than 120,000 yr (Houghton 2005). Global warming is also expected to continue for the
next century due to continued increases in greenhouse gas emissions and the inertia in the climate
system (Houghton et al. 2001).
The effects of climate change on the biology and ecology of organisms are receiving consid-
erable and increasing attention in the scientific literature (Table 1). The most apparent effects of
recent climate change are changes in phenology (e.g., altered timing of breeding activities; Walther
et al. 2002, 2005, Parmesan & Yohe 2003, Hpye et al. 2007) and shifts in the distribution of spe-
cies (e.g., Thomas et al. 2004, Perry et al. 2005, Poloczanska et al. 2007). Climate change has also
been implicated in dramatic shifts in species composition and community structure across anum-
ber of important and highly sensitive ecosystems (e.g., arctic, arid, tropical rainforests and coral-
reef ecosystems), as well as contributing to species extinctions within these systems (Brown et al.
1997, Walther et al. 2002, Williams et al. 2003, Thomas et al. 2004). Thomas et al. (2004) predict
that 15-37% of species in terrestrial ecosystems will be "committed to extinction" given a 2.0°C
increase in mean global atmospheric temperatures. Impending species losses will not only alter
biolog ical diversity but potentially reduce productivity and ecosystem stability, increasing se nsitiv-
ity to future disturbances and increasing the likelihood of ecosystem collapse (Tilman 2000, Myers
& Knoll 2001) . .
The devastating effects of recent climate change were first recognised and are most pronounced
on coral reefs, where there are clear links between increasing ocean temperatures and regional-
scale bleaching of scleractinian corals (Williams & Bunkley-Williams 1990, Glynn 1991, Walther
et al. 2002, Parmesan 2006). Climate-induced coral bleaching has caused massive devas tation to
coral-reef habitats (Hoegh-Guldberg 1999, Wilkinson 2000a) and is predicted to become more fre-
quent and more severe in coming decades (Sheppard 2003, Donner et al. 2005). Scleractinian corals
function exceedingly close to their upper thermal limit, at which bleaching may occur when sea
temperatures exceed normal local limits by as little as l.0°C (Jokiel & Coles 1990). The increasing
occurrence and importance of climate-induced coral bleaching reflects gradual increases in global
sea-surface temperatures, which have increased by 0.6°C in the last century (Lough 2000, Hoegh-
Guldberg 2004), bringing baseline ocean temperatures much closer to the maximum thermal tol-
erances for reef corals. Consequently, naturally occurring thermal anomalies (e.g., El Nino) will
252
EFFECTS OF CLIMATE-INDUCED CORAL BLEACHING ON CORAL-REEF FISHES
increasingly exceed thermal tolerances of corals, resulting in more frequent and severe episodes of
coral bleaching (Hoegh-Guldberg 1999, Stone et al. 1999).
Wh ile linkages between global climate change, thermal stress and coral bleaching have been
well studied and are becoming better understood (reviewed by Brown 1997, Douglas 2003, Hughes
et al. 2003, Hoegh-Guldberg 2004), the ecological ramifications of climate-induced coral bleach-
ing for fishes and other coral-reef organisms are only just beginning to become apparent (e.g.,
Jones et al. 2004, Aronson & Precht 2006, Graham et al. 2006). Corals (especially, reef-building
scleractinian corals) are fundamental to the functioning of coral-reef ecosystems, contributing to
primary production, nutrient recycling, and reef growth (Hoegh-Guldberg 2004, Wild et al. 2004).
Scleractinian corals are also the primary habitat-forming species (foundation species; Dayton 1972)
in coral-reef habitats (e.g., Connell et al. 1997). Removal or destruction of corals will therefore pro-
foundly alter the structure and dynamics of coral-reef habitats, with potentially significant effects
on highly diverse assemblages of species that associate with coral reefs (e.g., Wilson et al. 2006,
Munday et al. 2007, Pratchett et al. 2008). This review considers the effects of climate-induced coral
bleaching on coral-reef fishes, which are an important component of coral-reef ecosystems, in terms
of both their economic value (Westmacott et al. 2000a) and ecological function (Bellwood et al.
2004, Hughes et al. 2007). More than one quarter of known fish species are strongly associated with
coral reefs (Spalding et al. 2001) and will be increasingly affected by ongoing degradation of coral-
reef habitats caused or exacerbated by climate-induced coral bleaching (Jones et al. 2004, Munday
2004a, Pratchett et al. 2006).
This review provides the first comprehensive assessment of effects of climate-induced coral
bleaching on coral-reef fishes. Climate-induced coral bleaching has had major effects on the biolog-
ical and physical structure of coral-reef habitats in recent years (mostly since 1998; e.g., Wilkinson
2000a,b) and numerous studies have documented concomitant changes in the abundance, diversity
or composition of fishes (Shibuno et al. 1999, Booth & Beretta 2002, McClanahan et al. 2002a,
Spalding & Jarvis 2002, Munday 2004a, Sano 2004, Bellwood et al. 2006a, Garpe et al. 2006,
Graham et al. 2006, Pratchett et al. 2006). These studies concur that communities of coral-reef fishes
are strongly influenced by changes in habitat structure caused by climate-induced coral bleaching,
but there is little consensus on the processes involved or the key aspects of habitat structure that
shape communities of coral-reef fishes. This review examines associations between coral-reef fishes
and benthic reef habitats and identifies two critical components of habitat structure, namely coral
cover and topographic complexity. Changes in the abundance of coral-reef fishes following mass
bleaching are contrasted with loss of coral versus declining topographic complexity, emphasising
differences in the timing of these effects. These data are also used to forecast future effects of
climate-induced coral bleaching on diversity and composition of reef fish assemblages. Notably,
many studies have warned of impending waves of species extinctions due to climate-induced
degradation of marine and terrestrial habitats (Walther et al. 2002, Thomas et al. 2004). Herein,
threatened species of coral-reef fishes are identified based on their susceptibility to coral loss, com-
bined with biological attributes (e.g., restricted geographic range and rarity ; McKinney 1997) that
exacerbate extinction risk. Finally, economic consequences of expected changes in the abundance,
diversity and composition of coral-reef fishes are considered, with a view to adopting management
strategies that will minimise economic costs of climate-induced coral bleaching.
Mass bleaching: geographic extent and differential effects

Bleaching is a stress response common among scleractinian and alcyonarian corals, clams and
anemones that causes the pigmented symbiotic microalgae (zooxanthallae; Odum & Odum 1955) to
be expelled, leaving the animal tissue pale or white (Hoegh-Guldberg 1999). Persistent low levels
of natural or ' background' bleaching occur on all coral reefs (Will iams & Bunkley-Williams 1990)
253
MORGAN S. PRATCHETT ET AL.
contributing to natural attrition and turnover among corals. However, 'mass bleaching' in which
multiple species exhibit unusually high incidences of bleaching tends to reflect extreme environ-
mental stresses (Glynn 1991). Mass bleaching may result from high or low water temperatures,
excessive ultraviolet radiation, aerial exposure, reduced salinity, high sed imentation, pollutants, or
toxins (Williams & Bunkley-Williams 1990, Glynn 1991 , Smith & Buddemeier 1992, Brown 1997,
Hoegh-Guldberg 1999). Recent and severe mass bleaching events have primarily resulted from
positive thermal anomalies, linked to global climate change (Glynn 1991, Hoegh-Guldberg 1999).
In the most extreme example, global mass bleaching in 1998 resulted from severe El Nino condi-
tions (Wilkinson 1998, Stone et al. 1999), combined with the Indian Ocean dipole (Saji et al. 1999),
which dramatically increased sea-surface temperatures throughout the tropical Pacific, Indian a nd
Atlantic Oceans (Goreau et al. 2000). Throughout 1998, mass bleaching occurred on an unprec-
edented geographic scale (Goreau et al. 2000) and effectively 'destroyed' 16% of the coral reefs
around the world (Wilkinson 2000a).
The 1998 global mass bleaching was the most devastating and widespread bleaching event
ever recorded and contributed greatly to increased acceptance of global climate change as both a
real phenomenon and a significant threat to entire ecosystems (Walther et al. 2002). The sig nifi-
cance of this event was highlighted by the death of coral colonies that had survived 100-1000 yr
of environmental fluctuations and climate change (Hodgson 1999, Goreau et al. 2000). Effects
of the 1998 bleaching were nonetheless spatially variable, both at very large (geographic scales;
McClanahan et al. 2007a) and very small scales (e.g., between adjacent coral colonies; Marshall &
Baird 2000). Coral bleaching was particularly severe on coral reefs in the Indian Ocean, where
coral cover declined by an average of 46% following the 1998 bleaching (Hoegh-Guldberg 2004).
In contrast, coral bleaching killed only 3% of corals in the south-west Pacific (Papua New Guinea
and Australia's Great Barrier Reef [GBR]), although there were isolated incidences of very high
(up to 90%) coral mortality (Berkelmans & Oliver 1999). Since 1998, there have been only isolated
instances of mass bleaching (e.g., Berkelmans et al. 2004, McClanahan et al. 2007b, Pen in et al.
2007) but further mass bleaching on the scale of the I998 event is inevitable given sustained and
ongoing climate change (Sheppard 2003, Hoegh-Guldberg 2004, Donner et al. 2005).
A notable and recurring pattern in the effects of bleaching on coral communities is strong dif-
ferences in bleaching susceptibilities among coral taxa. Following bleaching, some coral species
may become locally extinct while others appear largely unaffected (e.g., Marshall & Baird 2000,
Loya et al. 2001, Floros et al. 2004, McClanahan et al. 2004, 2007a). In general, there is a clearly
defined hierarchy of bleaching susceptibilities, at least among coral genera (Brown & Suharsono
1990, Marshall & Baird 2000, McClanahan et al. 2004, 2007a, Figure 1). However, coral bleaching
is possibly less selective than some other major disturbances, such as outbreaks of the corallivorous
seastar Acanthaster planci and storm damage (e.g., Hughes & Connell 1999, Figure l). Taxonomic
differences in susceptibility to bleaching are generally ascribed to physiological and morphologi-
cal attributes, such as colony integration (Soong & Lang 1992, Baird & Ma rshall 2002) and tissue
thickness (Loya et al. 2001). However, there is also marked intraspecific variation in susceptibil-
ity to bleaching, especially during moderate bleaching (Baird & Marshall 2002). Susceptibility to
bleaching and subsequent survival of corals may vary according to differences in their depth and
habitats (Hoegh-Guldberg & Sal vat 1995), history of thermal stresses (Jokiel & Coles 1990, Brown
et al. 2002, McClanahan & Maina 2003), differences in thermal sensitivities of symbionts (Baker
2001) and fine-scale hydrodynamics (Nakamura & van Woesik 2001, McClanahan et al. 2005).
Variable responses of coral species to thermal stress both within reefs and ac ross the tropical oceans
suggest there is some potential for corals and their endosymbionts to adapt to changing climatic
conditions (Douglas 2003, Hughes et al. 2003). It is clear that some corals are extremely resistant
to increasing temperatures, rarely showing any visible sign s of coral bleaching (Marshall & Baird
254
EFFECTS OF C LIM AT E- IN DUCED CORA L BLEAC HING ON CORAL-REEF F ISH ES
100 r-
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Figure I Selecti vity of coral di sturbances. (A) Variation in bleachin g susce ptibilit y a mong di ffe re nt cora l
types (genera pl us grow th fo rm s: Tab, tab ul ar; Cor, cory mbose; A rb, arborescent) on the Great Barri e r Reef
(Marshall & Baird 2000). (B) Selectivi ty of cora l bleaching versus o ut breaks of Acanthaster planci (Pratc hett
200 1), show ing taxo nom ic contributions to overall coral loss by each of the worst-affected coral spec ies,
whe re bot h d isturba nces caused -50% decl ine in overall coral cover. Note: Coral ran k ings a lso di ffe r between
dist urba nces, so num bers do not refer to a part icul a r co ral spec ies.
2000). Give n predicted increases in the severity a nd freque ncy of cora l bleaching, taxonomic differ-
ences in susceptibility to bleaching a re likely to become a major driver of community structure a nd
spec ies diversity for sclerac tini an cora ls (Marsha ll & Baird 2000, Hughes et al. 2003, McCl ana ha n
et a l. 2007a), with concomita nt influences on the structure and diversity o f communities of coral-
reef fi shes.
255
Associations between fishes and coral-reef habitats

Coral-reef fishes strongly associate with conspicuous features of habitat structure (e.g., Jones &
Syms 1998, Munday & Jones 1998) but there are opposing schools of thought on the critical aspects
of coral-reef habitats. Certain authors (e.g., Jones 1988, Holbrook et at. 2000, 2002 , 2006, Munday
2000, Jones et at. 2004) consider that live coral cover has a major influence on the distribution and
abundance of coral-reef fishes. Accordingly, major changes in the abundance, diversity or composi-
tion of fishes have been related to extensive coral loss (Williams 1986, Sano et at. 1987, Jones et at.
2004, Munday 2004a, Pratchett et at. 2006). Alternatively, there is considerable correlative evi-
dence linking the abundances and diversity of coral-reef fishes with spatial and temporal variation
in topographic complexity (e.g., Luckhurst & Luckhurst 1978, McClanahan 1994, Jennings et at.
1996, Ohman & Rajasuriya 1998, Lawson et at. 1999, Gratwicke & Speight 2005, Garpe et at. 2006,
Wilson et at. 2007) and some authors perceive that live coral is largely irrelevant, except in provid-
ing habitat diversity and topographic complexity (Sale 1991, Lindahl et al. 2001, Garpe et at. 2006).
Ultimately, both coral cover and topographic complexity may be critical elements of coral-reef habi-
tats, although they may influence different components of reef fish assemblages. For example, coral
cover is important for specialist fishes that depend on corals for food or shelter (Williams 1986,
Lewis 1997, 1998, Syms 1998, Munday 2000, Pratchett et at. 2006), whereas topographic complex-
ity plays a key role in enhancing diversity of coral-reef fishes (Lindahl et at. 2001, Gratwicke &
Speight 2005, Graham et al. 2006).
The relative importance of coral cover versus topographic complexity is critical to understand-
ing the effects of habitat perturbations in coral-reef ecosystems (Wilson et al. 2006). Comparative
studies on the effects of habitat perturbations on coral-reef fishes have differentiated between dis-
turbances that affect live coral cover versus topographic complexity (e.g., Sano et at. 1987, Wilson
et at. 2006). Disturbances are separated into (l) biological disturbances (e.g., climate-induced coral
bleaching, outbreaks of A. planci, and coral disease), which kill corals without immediately com-
promising the integrity of coral skeletons (e.g., Sano et at. 1987, Garpe et at. 2006) and (2) physical
disturbances (e.g., severe tropical storms and tsunamis), which break down, displace and/or overturn
entire coral colonies, simultaneously reducing both live coral cover and structural complexity (e.g.,
Cheal et at. 2002, Halford et at. 2004, Baird et at. 2005). Biological disturbances can have severe
effects but these effects appear to be limited to fishes that are highly dependent on corals for food
or shelter (e.g., Williams 1986). In contrast, physical disturbances that cause a loss of topographic
complexity can have much more wide-ranging effects (e.g., Sano et at. 1987) because many coral-
reef fishes that do not depend on live corals are nonetheless dependent on topographic complexity
provided by healthy coral growth (e.g., Carpenter et at. 1981, Lawson et at. 1999, Gratwicke &
Speight 2005 , Glynn 2006). At Iriomote Island, Japan, healthy, diverse and topographically com-
plex coral assemblages were converted to a homogeneous flat plain of unstructured coral rubble
(Sano et at. 1987). As a consequence, 47 of 62 species (76%) of fishes completely disappeared and
9 of 15 remaining species exhibited significant declines in abundance. Extirpated species were
partly replaced by more generalist species but overall species richness on resulting rubble banks
was a fraction (35%) of the species richness recorded in former coral-dominated habitats (Sano et at.
1987). Notably, declines in coral cover and topographic complexity recorded at Iriomote Island
were caused by a biological disturbance (outbreaks of A. planci). While biological disturbances
do not directly affect the structural integrity of coral skeletons, exposed coral skeletons are highly
susceptible to physical and biological erosion (Hutchings 1986, Glynn 1997) leading to their even-
tual (after 4-LO yr) collapse and gradual declines in structural complexity (e.g., Sano et at. 1987,
Sheppard et at. 2002). Consequently, longer-term consequences of biological disturbances (includ-
ing climate-induced coral bleaching) may be analogous to physical disturbances, affecting both live
256
EFFECTS OF CLIMATE-INDUCED CORAL BLEACHING ON CORAL -REEF FISHES
coral cover and the physical structure of coral-reef habitats (e.g., Sheppard et al. 2002, Garpe et al.
2006, Graham et al. 2006).
Effects of climate-induced coral bleaching on coral-reef fishes

Climate change is rapidly emerging as the single greatest threat to coral-reef fishes (Wilson et al.
2006, Munday et al. 2007, Pratchett et al. 2008). Munday et al. (2008) reviewed direct effects of
climate changes (e.g., ocean warming, acidification, sea-level rise) on the reproductive potential
and dispersion of coral-reef fishes. Such effects are likely to become increasingly important in the
future (Poloczanska et al. 2007). Currently however, the most devastating effects of climate change
in coral-reef ecosystems relate to locally severe and geographically extens ive ep isodes of coral
bleaching (Smith & Buddemeier 1992, Goreau et al. 2000, Munday et al. 2007), which significantly
alter the biological and physical structure of coral-reef habitats and thereby affect coral-reef fishes
(Jones et al. 2004, Munday 2004a, Pratchett et al. 2006). Until 1998 very few studies had explored
the broader ramifications of coral bleaching and associated habitat modification for reef-associated
motile organisms (but see Glynn 1985, Tsuchiya et al. 1992). However, major effects of coral bleach-
ing on coral-reef fishes would be anticipated given prior research showing responses of fishes to
coral loss and habitat modification caused by outbreaks of A. planci (Williams 1986), severe tropi-
cal storms (e.g., Walsh 1983, Letourneur et al. I993) and experimental disturbances (Lewis 1997,
1998, Syms I998).
To assess effects of coral bleaching on coral-reef fishes, this review compiled data from six
independent studies (Shibuno et al. 1999, Booth & Beretta 2002, Spalding & Ja<vis 2002, Munday
2004a, Sano 2004, Pratchett et al. 2006), which together documented changes in abundance of 116
species of coral-reef fishes in the aftermath of mass bleaching. Densities of fishes were recorded
1-3 yr post-bleaching and compared with densities recorded before the bleaching. Only 45 of I 16
fishes exhibited significant changes in abundance, and responses ranged from local extinction to
several-fold increases in abundance (Figure 2). Fishes that increased in abundance were mostly
dietary and habitat generalist species (e.g., roving herbivores) that appear to move into areas vacated
by competitively dominant specialist species (see also Hart et al. 1996). Fishes that exhibited
declines in abundance were mostly species that depend on corals for food or shelter and probably
died as a direct result of coral depletion (e.g., Kokita & Nakazono 2001, Jones et al. 2004, Munday
2004a, Pratchett et al. 2006). It is possible that declines in abundance of fishes may result from
movement of fishes to unaffected habitats (e.g., Walsh 1983, Letourneur et al. 1993). However, the
potential for coral-reef fishes to find more suitable habitats following extensive coral bleaching may
be very Ii m ited due to the large scale of bleaching (e.g., Berkel mans et al. 2004) relative to potential
movement of post-settlement reef fishes (e.g., Chapman & Kramer 2000). Furthermore, competi-
tion among coral-reef fishes and priority effects in the occupation of habitats are likely to prevent
successful colonisation of displaced individuals (AI many 2003). Fishes in highly degraded habitats
are also likely to have experienced a protracted decline in resource availability, leading to reduced
physiological condition (Pratchett et al. 2004), which would further limit their ability to outcompete
conspecifics and invade new habitats.
The effects of coral bleaching and coral loss on coral-reef fishes may not always be immediately
apparent or become manifest through short-term declines in adult abundance. For example, reduced
availability of preferred coral prey can have significant but sublethal effects on coral feeding fishes
(Kokita & Nakazono 2001, Pratchett et al. 2004, Berumen et al. 2005). Pratchett et al. (2004)
showed that there was no short-term decline in the abundance of an obligate coral-feeding butterfly-
fish (Chaetodon lunulatus) despite a 55% decline in coral cover caused by mass bleaching. However,
C. lunulatus did exhibit significant declines in physiological condition (Pratchett et al. 2004), which
257
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Figure 2 Changes in the abundance of coral reef fishes following climate-induced coral bleaching. Data
presented for 45 (of 116) spec ies that exhibited significant changes in abundance following mass bleaching
that caused >50% coral loss. Data sources: Shibuno et al. (1999), Booth & Beretta (2002), Spalding & Jarvis
(2002), Munday (2004a), Sano (2004), Pratchett et al. (2006).
contributed to reduced survival and eventual population declines (Pratchett et al. 2006). Similarly,
reductions in live coral may limit settlement and recruitment for fishes that are otherwise unaffec ted
by coral depletion (Booth & Beretta 2002, Jones et al. 2004, Osenberg et al. 2006, Feary et al.
2007a,b). Limitations to population replenishment will undoubtedly reduce species abundance but
these effects may not be immediately apparent (Feary et al. 2007b).
Several studies have documented extensive declines in the abundance and diversity of coral-reef
fishes several years (>3 yr) after climate-induced coral bleaching (e.g., Garpe et al. 2006, Graham
et al. 2006). These studies attribute changes in reef fish assemblages to the delayed effect of struc-
tura l collapse of dead corals, which reduces overall topographic complexity of coral-reef habitats
(see also Sano et al. 1987). Many different fishes declined in abundance, including herbivorous
fishes (Graham et al. 2006) that might be expected to benefit from the increased abundance of algae
following extensive coral loss (Table 2, Figure 3). However, delayed effects of coral bleaching on
reef fishes may also be due to either (1) a lack of recruitment by fishes that need coral at settlement
(e.g., Jones et a!. 2004), (2) reductions in survivorship and/or reproductive output of fishes that
lead to gradual declines in population size (Pratchett et al. 2004) or (3) secondary declines in the
abundance of piscivorous fishes due to declines in coral-dependent prey fishes . Consequently, loss
of live coral may be as important as declining topographic complexity in protracted effects of coral
bleaching on coral-reef fishes (e.g., Jones et al. 2004, Table 2). Existing studies have never attempted
to separate these effects, although there is substantial correlative and indirect evidence that both live
coral and topographic complexity are important attributes of coral-reef habitats and strongly affect
communities of coral-reef fishes (Carpenter et al. 1981, Lawson et al. 1999, Holbrook et a l. 2000,
Munday 2000, Garpe & Ohman 2003, Graham eta!. 2006). Longer-term effects of coral bleaching
on coral-reef fishes are poorly understood, mostly because there are few studies that have measured
258
Table 2 Temporal basis of contrasting effects of coral loss

versus declines in topographic complexity on coral reef fishes:
examples of major families of coral reef fishes affected by
coral loss versus declines in topographic complexity during
the periods <3 yr and 3-10 yr post-bleaching
Period
<3 yr 3-10 yr
Live coral cover Chaetodontidae Labridae

Gobiidae Pomacentridae
Topographic complexity None Acanthuridae
Scaridae
changes in the reef fish assemblages >3 yr after bleaching (Jones et al. 2004, Bellwood et al. 2006a,
Graham et al. 2006), and no studies have sampled >10 yr after bleaching.
Loss of live coral

The most immediate and predictable effect of climate-induced coral bleaching is a decline in live
coral cover caused by mortality of entire coral colonies as well as partial loss of live tissue for many
surviving corals (e.g., Baird & Marshall 2002). Coral loss reduces resources available to coral-
dependent fishes, with expected consequences for individual condition (e.g., Kokita & Nakazono
2001, Pratchett et al. 2004) and population size (e.g., Munday 2004a, Pratchett et al. 2006). The
important question is what proportion of fishes actually depend on live corals for their long-term
persistence. A wide range of associations exist between reef fishes and live corals, from species that
depend on live coral for food and habitat (Munday 2002, Pratchett 2005), to species that are rarely
associated with live coral and are characteristic of sites with low coral cover (Sano et al. 1984).
Current estimates of the proportion of coral-reef fishes with apparent and direct reliance on live
corals are 9-11 % (Jones et al. 2004, Munday et al. 2007). Of 1221 coral-reef fishes recorded on
the GBR, Munday et al. (2007) estimated that 104 species (9%) have direct and explicit reliance on
corals (Figure 4; see also Jones et al. 2004). These species include (I) corallivorous fishes that feed
on live coral tissue (e.g., many Chaetodon butterflyfishes; Pratchett et al. 2006), (2) coral-dwelling
fishes, including species living entirely within the branches of live coral colonies (e.g., Gobiodon
coral gobies; Tsuchiya et al. 1992, Munday et al. 1997, Munday 2004a,), as well as species that
shelter within live corals when threatened but otherwise feed above their host coral (e.g., Dascyllus
damsel fishes ; Holbrook et al. 2002) and (3) fishes that settle on or near live corals but do not neces-
sarily associate with coral throughout their lives (e.g., many damselfishes; Booth & Beretta 2002,
Feary et al. 2007a). Based on these findings, coral loss is expected to affect <12% of coral-reef
fishes. However, Jones et al. (2004) showed that 75% of coral-reef fishes declined in abundance fol-
lowing extensive (90%) coral mortality and habitat modification caused by climate-induced coral
bleaching and sedimentation, which might suggest that importance of corals for coral-reef fishes
has been underestimated .
It is intuitive that coral-dependent fishes will be significantly and adversely affected by coral
bleaching and coral loss. Effects of coral depletion on strongly coral-dependent fishes are nonethe-
less highly variable. For example, Munday (2004a) examined effects of coral bleaching and coral
loss on coral-dwelling gobies. Although all species were obligate coral dwellers and highly depen-
dent on live corals, declines in the proportional abundance of the six species ranged from 50% to
100% (Munday 2004a). Specific responses of coral-dependent fishes may vary according to (I) the
extent to which populations are limited by the availability of live coral, (2) their versatility in use
259
0.5
..······························ ...... Macroalgal cover
.·· ····································································································
...........
"""c:
"'
0 .··
---
..c:
u '
'\
'Ｍｾ＠ "
c: I
I
I
\
0 \
0.
0 -0.5 ' ' Topographic complexity
0::
--- --- --- ---
Coral cover --- ---
-1
0 2 3 4 5 6 7 8 9 10
(A)
0.5
"
u
c:
"'c:
-o
::l
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.5
"'
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'.g"c: -0.5
....
0
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Habitat-
2
""' associated fishes
-1
0 2 3 4 5 6 7 8 9 10
Time after mass bleaching (years)
(B)
Figure 3 Conceptual diagram of changes in coral reef habitats and fish communities following climate-
induced coral bleaching. (A) Timing and magnitude of proportional changes in macroalgal cover, topographic
comp lexity and coral cover. (B) Response envelops for strongly coral-dependent fishes (e.g., obligate coral-
li vores), habitat-associated fishes and herbivores.
of alternate resources and (3) the degree to which sublethal responses mitigate or delay declines in
abundance (Wilson et al. 2006). Importantly, highly specialised coral-dependent fishes will respond
to changes in the abundance of their predominant food or habitat type rather than changes in live
coral cover per se.
Corallivorous fishes
Corallivorous fishes have the most apparent and direct reliance on live corals (Randall 1974) and are
consistently among the worst-affected fishes following extensive coral loss (e.g., Bouchon-Navaro
et al. 1985, Williams 1986, Kokita & Nakazono 2001, Pratchett et al. 2006, Wilson et al. 2006,
Figure 2). Worldwide, there are 117 species of coral-reef fishes from LO families that have been
reported to feed, at least in part, on scleractinian corals (A. Cole unpublished data). The most diverse
260
25 55%
0 Settlement
0 Habitat
• Food
20
15
·c"'v
v
0..
"'
......
0
0 10
z
0 v v v v v v v v v v v v v v v v
"' :-,:"' -o"' "' -o"' :-,:"' "' -o"' -o"' -o"' "' -o"' -o"' -o"' -o"'
:-,:"'
c0 c :00 "20 :g.D ..c·;:::::l c2 ] "'2 :.2c :.2c :gu"' "2"' :.2c "§ "2v
-o
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-o v (.!) "' c v ｾ＠ Ui u u
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t: Vl 2
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e
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u "'
c "'
E 0
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..c <(
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Vl
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ｾ＠
0..
Figure 4 Coral-dependent fishes on the Great Barrier Reef. Numbers indicate percentage of species in each
family considered to be coral dependent out of total number of species listed for each family in Randall et al.
(1997). Where species used corals for more than one purpose, precedence was given to food, then habitat, and
then recruitment.
and best-studied group of corallivorous fishes are the butterflyfishes, family Chaetodontidae (e.g.,
Tricas 1985, Harmelin-Vivien & Bouchon-Navaro 1983, Harmelin-Vivien 1989, Irons 1989, Sano
1989, Zekeria et al. 2002, Pratchett 2005, 2007a). Other fam i Iies with significant numbers of coral-
feeding species are the Pomacentridae (14 species), Monacanthidae (9 species), Labridae (8 species),
Balistidae (7 species), and Tetraodontidae (7 species) (A. Cole unpublished data). Despite this diver-
sity, corallivorous fishes still only account for a small proportion (<5% of species) of the overall
diversity of fishes on coral reefs (Spalding et al. 2001). However, Iive coral may also contribute to the
nutritional intake of many fishes that do not feed directly from the surface of corals. For example,
many coral-reef fishes opportunistically exploit and derive considerable benefit from feeding on
coral gametes (Pratchett et al. 2001, McCormick 2003). Corals also produce large quantities of
mucus (e.g., 1.7 1 m- 2 day- 1), which is enriched by trapping organic matter from the water column
(Wild et al. 2004) and probably represents a significant input to the trophodynamics of coral-reef
ecosystems (Wilson et al. 2003). Many fishes may supplement diets with coral mucus and tissue,
which may go undetected because coral tissue is often indistinguishable from exogenous material
and partially digested matter in the gut (Zekeria et al. 2002). This situation may be particularly true
of many cryptic coral-dwelling species, for which there is limited knowledge of feeding behaviour.
Reduced availability of coral clearly limits the abundance of corallivorous fishes (Carpenter
et al. 1981, Bell & Galzin 1984, Bouchon-Navaro et al. 1985, Findley & Findley 1985, Roberts et al.
1988, Ohman et al. 1998, Cadoret et al. 1999, Bozec et al. 2005), although relationships between
261
MORGANS . PRATCHETT ET AL.
0
•
•
...
-0.5 • •• • •
"'>0 •
u
-;;;
0
u
:2
-1
• • ....... ,.......
•
"'c:
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_g-1.5 ••
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•
..0
< •
<l
-2
•
-2.5 ＭＱｾＫＮＬｊ＠
0 20 40 60 80 100
Percentage of live coral in diet
Figure 5 Declines in the abundance of 22 corallivorous fishes following coral depletion versus percentage
consumption of scleractinian corals. Data extracted from 17 st udies that explored fish responses following cli-
mate-i nduced coral bleaching, outbreaks of Acanthaster planci, sedimentation, and experimentally imposed
disturbances. Responses (declines in abundance) are standardised for variation in proportional declines of
live coral cover, following Wilson et al. (2006). Dotted line indicates line of best fit for the linear relationship
between declines in the abundance of butterfly fishes versus proportional consumption of scleractinian corals.
Grey shading indicates obligate corallivores.
coral cover and abundance of corallivores are not always apparent (e.g., Bell et al. 1985, Fowler
1990, Kulbicki et al. 2005). Responses of corallivorous fishes to changes in availability of corals
are likely to depend on (I) their dependence on corals for food, (2) the severity and extent of coral
loss and (3) the extent to which live coral (versus other factors such as recruitment) may be limiting
their abundance. The extent to which corallivorous fishes feed on corals (vs. other non-coral prey)
is highly variable (e.g., Hobson 1974, Pratchett 2005) and obligate coral feeders are much more
affected by coral loss than facultative coral feeders (Bouchon-Navaro et al. 1985, William s 1986,
Wilson et al. 2006, Pratchett et al. 2006, Figure 5). Facultative corallivores are relatively unaffected
by moderate decline in abundance of corals, presumably because they can compensate by increas-
ing intake of non-coral prey. However, corals may represent an important and necessary component
of their diet, such that even facultative corallivores are adversely affected by extensive coral loss
( Pratchett et al. .2006).
Among obligate coral-feeding butterftyfishes there are marked differences in the range of
different corals eaten as well as the proportional consumption of different corals. For example,
Chaetodon trifascialis is an extreme specialist, which feeds almost exclusively on Acropora hya-
cinthus (Pratchett 2005), whereas Chaetodon lunulatus feeds on a wide diversity (up to 52 spe-
cies) of corals (Berumen et al. 2005, Pratchett 2005). This variability in the dietary habitats of
coral-feeding butterftyfishes is likely to influence their reliance on particular corals as well as their
responses to different types of disturbances (Figure 6). Like facultative corallivores, highly versatile
obligate corallivores can access a greater diversity of prey and may partially compensate for initial
depletion of preferred prey resources by increasing intake of alternate prey types (i.e., prey switch-
ing; Pratchett et al. 2004) and increasing the area over which they forage (Tricas 1989, Kokita &
Nakazono 2001, Samways 2005). Consequently, generalist species may be more resilient to changes
in cover and composition of hard corals (e.g., Pratchett et al. 2004), whereas effects of disturbances
262
-10 Coral-feeding butterflyfishes (Chaetodon)
-20 •
-30 •
-40
... .· ···•
-50 •... .
..
-60 • R2 = 0.7575
Q)
u
-70 .·
r::
"'
-o
r::
:::l
-80 •
.L:l
-90
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.5
"'on -100
r:: 0 10 20 30 40 50 60
"'u
.c
cQ)
l:::: -40 Coral-dwelling gobies (Gobiodon)

Q)
0..
-50
• •
-60
-70
• •
-80 • R2 = 0.7477
-90
-100
0 2 4 6 8 10 12 14
< Specialists
No. of co ral taxa used
Generalists >
Figure 6 Declines in abundance foll ow ing severe cora l depletion in relation to number of different coral
taxa used for strongly co ral-dependent reef fishes. Data for cora l-feeding butter fl yfis hes come from Li zard
Island, northern GBR, following coral depletion caused by Acanthaster planci ( Pratchett 2001). Data for
cora l-dwelling gobies are from Kimbe Bay, where globa l warming and coastal development caused extensive
cora l loss (Mu nday 2004a). Dotted lines indicate line of best fit for logarithmic relati onship between dec! ines
in the abundance of fish species versus number of cora l spec ies th at th ey use.
on spec iali st species will vary according to changes in abund ance of the particular coral species
on which they specialise. In Moorea, for example, recurrent disturbances (bleaching, outbreaks of
Acanthaster planci, and severe storms) throughout the last 25 yr have substantially altered coral
composition, causing a tra nsition from Acropora- to Pocillopora- and Po rites-dominated coral
assemblages (Berumen & Pratchett 2006). Accordingly, local abundance of butterfly fishes that feed
predominantly on Acropora spp. has declined, whilst Pocillopora specialists and more generalist
corallivores have proliferated (Berumen & Pratchett 2006).
While dietary composition and specialisation are fundamental in determining responses of
corallivorous fi shes to coral losses (Pratchett et al. 2006), the range of corals consumed by coral-
feeding fishes is known for <25 species (Pratchett 2005). Until recently, very few studies di stin-
gui shed among coral taxa when documenting diets of coral-feeding fi shes. Rather, most studies
263
(e.g., Harmelin-Yivien & Bouchon-Navaro 1983, Bouchon-Navaro 1986, Sano 1989, Pitts 1991 ,
Zekeria et al. 2002) treated all scleractinian corals as a single prey category and simply distin-
g uished between obligate versus facultative corallivores. The few studies that have explored specific
prey preferences (Irons 1989, Tricas 1989, Pratchett et al. 2004, Berumen et al. 2005, Pratchett 2005,
2007a) have shown that corallivorous fishes may be very specialised, consuming only a very small
suite of available coral prey. Moreover, dietary preferences of corallivorous butterftyfishes appear
to be highly convergent. For example, at Lizard Island (northern GBR) most coral-feeding butter-
ftyfishes feed predominantly on either Acropora hyacinthus or Pocillopora damicornis (Pratchett
2005), demonstrating significant selectivity for either or both these corals (Pratchett 2007a). These
coral species are among the first corals affected during mass bleaching (Marshall & Baird 2000) and
are highly susceptible to predation by Acanthaster planci (De'ath & Moran 1998, Pratchett 2007b)
and displacement during storms (Mad in & Connolly 2006), probably explaining why highly specia-
lised butterftyfishes are disproportionately affected during these types of disturbance. Chaetodon
trifascialis, for example, is often extirpated (100% decline in local abundance) even during fairly
moderate (<21%) declines in live coral cover (e.g., Syms 1998). As habitat perturbations become
more frequent and more severe, it appears likely that highly specialised obligate coral feeders will
be increasingly replaced by much more generalist and facultative corallivores, as has already been
demonstrated following recurrent disturbances in Moorea (Berumen & Pratchett 2006).
Coral-dwelling fishes
The majority of coral-dwelling fishes are relatively small in body size and depend on the complex
structure provided by live coral colonies for shelter (Munday & Jones 1998). Coral-dwelling fishes
comprise two fairly distinct groups. ｔｨｾ＠ first group, exemplified by coral gobies (Gobiodon spp.,
Paragobiodon spp.), generally remain hidden among the branches of their host coral colonies. This
group (also including the crouchers Caracanthus spp., the scorpionfish Sebastapistes cyanostigma
and some hawkfishes, e.g., Neocirrhitus annatus) live, feed and reproduce within live corals and
often remain within a single coral host for the duration of their lives. The second group of coral-
dwelling fishes are the species that retreat into live corals at night or when threatened but otherwise
remain in close proximity and feed above their specific coral host (e.g., Eviora spp., Pomacentrus
spp., Chromis spp., Dascyllus spp.). Most coral-dwelling species have small home ranges and indi-
viduals often exhibit strong fidelity to a single coral head (Sale 1971, Feary et al. 2007a). Even
species that leave their coral habitat to forage across the reef tend to exhibit strong fidelity to their
shelter site (Marnane 2000).
Variation in the abundance and composition of scleractinian corals has a major influence on
the structure and dynamics of coral-dwelling fishes, although the apparent strength of assoc ia-
tions between fishes and corals are taxonomy and scale dependent (Jones 1991, Sale 1991, Jennings
et al. 1996, Munday et al. 1997, Holbrook et al. 2000). While the community structure of fishes
on individual coral heads can vary unpredictably from one coral head to another (Sale & Dybdahl
1975, Sale et al. 1994), distinct assemblages of fishes can be consistently found on different spec ies
and growth forms of coral (Gladfelter et al. 1980, Ebersole 1985, Tolimieri 1995, Munday et al.
1997, Holbrook et al. 2000, 2002). Suitable coral habitat also appears to be a limiting resource for
many coral-dwelling fishes (Holbrook et al. 2000, Schmitt & Holbrook 2000, Munday et al. 2001,
Munday 2004b) and the population dynamics of these species often match the population dynam-
ics of their preferred coral habitats (Kuwamura et al. 1994, Munday et al. 1997). For example, even
though there are peaks of recruitment among juvenile coral-dwelling gobies, the size of the adult
population remains stable and is closely correlated with the number of coral colonies large enough
to support a breeding pair (Kuwamura et al. 1994, Hobbs & Munday 2004). When coral colonies
decline in abundance there is a corresponding decline in the abundance of coral-dwelling gobies
264
(Kuwamura et al. 1994, Munday 2004a). Adult population size is less rigidly controlled by habitat
availability in many other coral-dwelling species (Sale 1972, Gardiner & Jones 2005). However,
these species still usually decline in abundance following significant declines in coral cover (Lewis
1998, Spalding & Jarvis 2002, Jones et al. 2004, Wilson et al. 2006), demonstrating that their habi-
tat is in limited supply.
Many coral-dwelling fishes favour coral species from the families Acroporidae (mainly
Acropora spp.) and Pocilloporidae (Pocillopora, Stylophora and Seriatopora), probably because
their complex branching structure provides refuge from predation (Beukers & Jones 1997). On
Indo-Pacific reefs, species of Gobiodon (Gobiidae), Paragobiodon (Gobiidae) and Caracanthus
(Scorpaenidae) are almost exclusively associated with corals from these two families (Tyler 1971,
Patton 1994, Munday et al. 1997). Similarly coral-dwelling damselfishes (Pomacentridae) from the
genera Amblyglyphidodon, Chromis, Dascyllus , Plectroglyphidodon, and Pomacentrus are most
commonly associated with acroporid and pocilloporid corals. Numerous Eviota and Bryaninops
species (Gobiidae) occur where there are dense stands of acroporid corals (Larson 1985, 1987,
Randall et al. 1997) and Sebastapistes cyanostigma (Scorpaenidae) is commonly found among
the branches of pocilloporid corals (P. Munday personal observation). Coral-dwelling fishes asso-
ciate with a variety of other coral taxa, but these too are usually species with a high degree of
structural complexity. For example, Gardiner & Jones (2005) found that nine common cardinal-
fishes (Apogonidae) exhibited strong association with the branching coral Porites cylindrica . Also,
Gobiodon acicularis, one of the few Gobiodon species to inhabit non-acroporid corals, lives among
dense thickets of Echinopora and Hydnophora (Munday et al. 1999). Those coral-dwelling fishes
that are not associated with complex branching corals are typically well camouflaged and cryptic,
such as the elongate gobies of the genus Bryaninops that can be found on the stems of black corals
and sea whips (Larson 1985, Randall et al. 1997).
Ironically, coral species most frequently used by coral-dwelling fishes are often those that are
most susceptible to bleaching (Munday et al. 1997, Munday 2004a, Feary et al. 2007b). Overall,
there is high concordance in primary coral preferences of coral-dwelling fishes (particularly for
gobies and damselfishes), which means that coral bleaching tends to have a negative effect on a
broad suite of coral-dwelling fishes. Despite this broad overlap in habitat preferences, coral dwellers
still vary greatly in their ecological versatility, from species that inhabit just one species of coral,
to species that use a wide range of available coral types (Munday 2002, Munday et al. 2007). The
most specialised species (i.e., those fishes that occupy fewer coral species) appear to suffer greater
declines in abundance following coral loss (Munday 2004a, Figure 6). Effects of coral mortality are
greatest for highly specialised species because they are not able to adjust their patterns of habitat
use as preferred coral habitats become scarcer. In contrast, the more generalist species increase their
use of alternative coral species if their primary preferences decline in abundance, which results in
less-serious declines in their population abundance (Munday 2004a).
Coral bleaching could further influence local abundance and population structure of coral-
dwelling fishes through its effect on habitat patch size. Social group size of some coral-dwelling
fishes is correlated with habitat patch size (e.g., Wong et al. 2005, Thompson et al. 2007) and the
total number of all coral-dwelling fishes on a coral head often increases in proportion to the coral
colony size (Munday et al. 1998). Therefore, communities of older and larger corals can support
larger populations of coral-dwelling fishes . Bleaching reduces the average size of coral colon ies
through mortality of mature corals and this will probably reduce the overall abundance of coral-
dwelling fishes (Feary et al. 2007a). Because of the close association between body size and fecun-
dity in most coral-reef fishes, reduction in average coral colony size could also affect reproductive
output for species for which the size of dominant breeding individuals is correlated with coral
colony size (Kuwamura et al. 1994, Hobbs & Munday 2004).
265
Coral as settlement habitat

Species that closely associate with Iive coral as juveniles and adu lts commonly exhibit strong selec-
tion for live coral habitat at settlement (Gutierrez 1998, Ohman et al. 1998 , Srinivasan 2007). For
these species, larvae often settle directly into adult habitat and may even be cued by resident conspe-
cifics already present in suitable habitat patches (Sweatman 1985, 1988, Booth 1992, Ohman et al.
1998, Lecchini et al. 2005). Many coral-reef fishes also associate with live coral when they first
settle to the reef, even if they do not exhibit strong associations with live corals in later life (Booth &
Beretta 1994, Jones et al. 2004, Feary et al. 2007b). These juvenile fishes use live colonies as a set-
tlement cue (Ohman et al. 1998), food source (Harmelin-Vivien 1989) or to provide refuges against
predation (Webster 2002). Widespread reliance on live corals around the time of settlement may
explain why the effects of coral loss sometimes extend beyond species known to be coral dependent
( Booth & Beretta 2002, Bellwood et al. 2006a). Jones et al. (2004) estimate that 65% of fishes on
coral reefs in Papua New Guinea were preferentially associated with live coral at settlement and
observed declines in population abundance of different species closely corresponded with the pro-
portion of juveniles that settled on live coral. Furthermore, Graham et al. (2007b) documented a
substantial decline in smaller size classes (<35 em) of important fisheries species following coral
bleaching and ongoing habitat degradation in the Seychelles. These declines in smaller size classes
are attributed not only to increased predation and competition following loss of the physica l reef
structure but also to repeated recruitment failure (Graham et al. 2007b).
For fishes that are only loosely associated with coral habitats, adult survival might be largely
unaffected by coral loss but settlement may be reduced (Bouchon-Navaro et al. 1985, Booth & Beretta
2002, Jones et al. 2004, Feary et al. 2007b, Graham et al. 2007b, Srinivasan 2007). Therefore, even-
tual declines in adult abundance result from a natural attrition combined with a lack of repleni sh-
ment. The extent to which settlement failure is reflected in adult abundance depends on the severity
and duration of recruitment failure, population turnover and adult longevity (Halpern et al. 2005,
Feary et al. 2007b). Declines in the juvenile population will have a strong effect on adult population
size if the juvenile population is relatively small compared with the adult population and popula-
tion size is essentially limited by recruitment. Declines in the juvenile population will have smaller
effects on the adult population if they are relatively large compared with the adult populations and
there is an oversupply of juveniles available to recruit to the adult population ( Halpern et al. 2005).
Longevity will also influence how settlement failures affect adult populations because, for long-
lived species, occasional good recruitment provides a buffer against intervening periods of little or
no recruitment (storage effect; Warner & Hughes 1988), whereas adult populations of short-lived
species decline rapidly following sett lement failure (Bellwood et al. 2006a, Fearyet al. 2007b). For
longer-lived species (such as many commercially exploited fisheries spec ies), the time lag between
recruitment failure and apparent declines in adult abundance may be decades rather than years
(Bellwood et al. 2006a, Graham et al. 2007b). rn these cases, effects of recent mass bleachings may
not have even begun to become apparent in adult populations of long-lived species.
Loss of topographic complexity

The importance of the physical structure of coral-reef habitats for fishes has been extensively stud-
ied and there is strong support for links between topographic complexity and abundance of fishes,
biomass and diversity (Risk 1972, Luckhurst & Luckhurst 1978, Sano et al. 1987, Grigg 1994,
Friedlander & Parrish 1998). Experiments using non-coral materials to construct artificial reefs of
differing complexities (e.g., Caley & St John 1996, Gratwicke & Speight 2005), manipulation of
complexity within coral colonies or assemblages (Sano et al. 1984, Lewis 1997, Syms & Jones 2000,
Glynn 2006), and comparison of biological versus physical disturbances (Wi lson et al. 2006) all
indicate that topographic complexity has a majo r influence on cora l-reef fish communities. Habitat
266
complexity has an important influence on biotic interactions, such as predation and competition,
and has a major influence on the local abundance of coral-reef fishes, especially during the early life
stages (Almany 2004, Hixon & Jones 2005). Increased structural complexity moderates predation
intensity and competitive interactions, thereby increasing local diversity and abundance of fishes
(Hixon & Jones 2005, Lee 2006). Reef habitats with reduced topographic complexity typically sup-
port lower fish abundance, fewer species and increased evenness (Syms & Jones 2000, Gratwicke
& Speight 2005, Graham et al. 2006). Loss of structural complexity is especially detrimental for
small-bodied fishes (including both small species and juvenile phases of larger-bodied species)
because these fishes are highly susceptible to predation and often depend on specific microhabitats
to evade predators (Hixon & Beets 1993, Beukers & Jones 1997).
Climate-induced coral bleaching kills corals, but leaves the underlying skeleton completely intact
(Hoegh-G uldberg 1999). Exposed coral skeletons are then subject to a whole suite of bio-eroding
organisms that undermine the structural integrity of these carbonate structures (Hutchings 1986).
Over time, coral skeletons of erect branching corals (e.g., Acropora and Pocillopora) break down
into coral rubble (Sheppard et al. 2002, Graham et al. 2006), whereas more robust skeletons of mas-
sive corals (e.g., Porites) may become dislodged or gradually eroded in situ (Sheppard et al. 2002).
These processes contribute to long-term declines in structural complexity and can ultimately result
in structurally depauperate reef landscapes (e.g., Sano et al. 1987, Sheppard et al. 2002). Successive
degradation of reef habitats compounds initial coral losses and significantly extends effects of coral
bleaching on coral-reef fishes (e.g., Wilson et al. 2006). On reefs in the Indian Ocean, severe mass
bleaching in 1998 and subsequent collapse of 3-dimensional corals have converted complex coral-
dominated habitats to areas of flattened carbonate pavement or rubble fields where macroalgae now
predominate (Sheppard et al. 2002, Garpe et al. 2006, Graham et al. 2006). Associated with these
shi fts in benthic habitats, species richness of fishes declined by as much as 50% and while coral-
dependent species were disproportionately affected, many other functional groups of fishes, includ-
ing herbivorous fishes, also disappeared, probably due to declines in topographic complexity (Garpe
et al. 2006, Graham et al. 2006, Figure 3). Even where there is no apparent change in the abundance
or species richness of fishes, coral loss and reef collapse have caused marked shifts in the commu-
nity structure of fish assemblages (Bellwood et al. 2006a). In general, fish communities in degraded
post-bleaching habitats are characterised by dietary and habitat generalists (e.g., omnivores and
detritivores), which replace coral-dependent specialists ( Bellwood et al. 2006a, Graham et al. 2006).
These post-bleaching fish assemblages may be fairly resilient to future disturbances but are nonethe-
less undesirable because the loss of entire functional groups (e.g., corallivores and herbivores) may
have ramifications for recovery, productivity and ecosystem function (Bellwood etal. 2006a).
Declines in topographic complexity are not a certain consequence of climate-induced coral
bleaching. In reef habitats o nce dominated by erect branching corals (e.g., lagoonal habitats domi-
nated by monospecific stands of staghorn Acropora) degradation of structural complexity can be
fairly rapid and particularly severe, reducing complex coral habitats to flat rubble banks (e.g., Glynn
2006, Graham et a l. 2006). Elsewhere, however, dead corals may remain intact for many years and
may become the foundation for new coral growth (e.g., Bellwood et al. 2004, DeVantier & Done
2007). Also, on some reefs (mostly, highly exposed reef slopes) live corals contribute little to overall
topographic complexity; rather the inherent complexities within the vertical reef matrix contribute
most topographic relief and habitat structure (e.g., Halford et al. 2004). The extent to which reef
habitats exhibit declining topographic complexity following widespread coral mortality depends
on (I) the fragility of the original coral assemblage, branching corals being more susceptible to
collapse than massive corals, (2) the underlying complexity of the reef framework, (3) abundances
of bioeroding organisms such as excavating parrotfishes (Bellwood et al. 2003) and sea urchins
(McC lanahan &Shafir 1990) and (4) the extent of physical erosion caused by persistent wave action
or acute storms (Mad in & Connolly 2006, Smith et al. 2007).
267
Persistence and recovery of fish assemblages

The strong linkage between coral-reef fishes and underlying habitat clearly makes them susceptible
to climate-induced coral bleaching. However, provided bleaching is sporadic and does not cause
100% mortality of critical coral species, even highly susceptible fish populations may have the
potential to persist and recover. For example, Holbrook et al. (2006) show that dramatic declines in
fish abundance and diversity may not occur until coral cover is reduced to <lO% (see also Wil son
et al. 2006). Recovery of fish communities will be expected, provided there are refuge adult popu-
lations and recovery of critical aspects of the biological and/or physical structure of these habitats
(e.g., Halford et al. 2004). Recovery of fish populations is reliant upon many factors, such as the con-
tinual supply of fish recruits (Doherty & Williams 1988) and the ability of fishes to reclaim space
occupied prior to temporary disruptions in habitat structure. Pre-emption of space by new species
may retard the recolonisation by some previous residents (A lmany 2003), although competitive
hierarchies can eventually reinstate species as they gradually recruit back to the reef, a process that
appears to be particularly important for habitat and feeding specialists (Munday et al. 2001). Clearly
however, coral-reef fishes affected by disturbance-mediated changes in coral-reef habitats must be
limited by some biological or physical aspect of habitat structure (e.g., live coral cover, topographic
complexity, habitat diversity or coral composition) and recovery can only occur after the habitat
itself has reverted to a state suitable for settlement and survival of these fishes (Halford et al. 2004).
The recovery of specialist species, for example, will be dependent upon renewed abundance of their
preferred coral species.
Following major habitat perturbations, and in the absence of any further disturbances, it may
take as little as 5 yr for coral cover to return to predisturbance levels (e.g., Halford et al. 2004,
Gardner et al. 2005). The time taken for coral cover to increase depends on the severity and extent
of coral loss, which dictates the ability of surviving corals to recover, reproduce and reseed affected
areas (Hughes & Connell 1999, Riegl & Piller 2003, Golbuu et al. 2007). Importantly, isolated reefs
are likely to be more sensitive to declines in viability of local populations, whereas well-connected
reefs, such as those along continental margins or large archipelagos, are more likely to be reseeded
by larvae from nearby and relatively unaffected populations (Ayre & Hughes 2004). Recovery
will be much faster if at least some coral colonies survive the bleaching, as often occurs during
mass bleaching (e.g., Baird & Marshall 2002), because growth of surviving corals leads to more
rapid increases in coral cover compared with settlement and subseq uent growth of new individu als
(Connell et al. 1997), whereas local populations of mature corals are the most reliable source of new
recruits (Hughes et al. 2000). Where viable source populations a re avai lable to initiate recovery,
settlement and survival of juvenile corals will also be conditional upon the availability of suitable
settlement substrata (Hughes et al. 2007). It is frequently hypothesised that local populations of
herbivores play a key role in keeping reef substrata relatively free of both turf-forming and macro-
algae, which facilitates the settlement and subsequent survival of coral recruits (Bellwood et al.
2004, Mumby et al. 2006, Hughes et al. 2007, Ledlie et al. 2007). Some herbivores can have nega-
tive effects on coral recruitment, either through incidental predation on cora l recruits (McClanahan
et al. 2005) or by promoting coralline algae that inhibit coral recruitment (Harrington et al. 2004).
However, large-scale caging experiments demonstrate that exclusion of large-bodied fishes (analo-
gous to overfishing of herbivorous fishes) leads to extensive growth of fleshy macroalgae, which
suppresses fecundity, recruitment and survival of corals (Hughes et al. 2007).
Coral mortality following bleaching provides space on the reef that is rapidly colonised by
turf-forming algae (Diaz-Pulido & McCook 2002). On reefs where herbivorous fishes and/or sea
urchins are abundant, algal assemblages may remain as cropped turf forms following coral bleach-
ing and coral loss (Aronson et al. 2002, Arthur et al. 2005). However, where grazing pressure is
low, or if coral mortality is extensive, local stocks of turf-feeding spec ies may be unable to counter
268
increased algal abundance and macroalgal blooms can develop (Ostrander et al. 2000, McClanahan
et al. 2001b, Williams et al. 2001, Diaz-Pulido & McCook 2002, Aronson & Precht 2006), bringing
about a phase shift from coral- to macroalgal-dominated reefs. Once established, macroalgae may
persist because many of the fish species traditionally expected to target macroalgae feed almost
exclusively on epilithic turf-forming algae and avoid larger fleshy thalli (Bellwood et al. 2006b,
Ledlie et al. 2007). Furthermore, some species traditionally regarded as herbivorous are actually
detritivores (Wilson et al. 2003). Indeed there are relatively few fish species that ingest substan-
tial quantities of macroalgae (Choat 1991, Choat et al. 2002, 2004, Crossman et al. 2005, but see
Mantyka & Bellwood 2007) and the presence of macroalgae tends to discourage the presence of
many 'herbivorous' fish species (McClanahan et al. 1999, 2000, 2002b). While many herbivorous
fishes are important in preventing increasing biomass of macroalgae in coral-reef habitats by inten-
sive grazing of reef substrata, thereby preventing phase shifts (Bellwood et al. 2004, Mumby et al.
2006, Hughes et al. 2007, Led lie et al. 2007), an entirely different suite of fishes is needed to remove
macroalgae once they become established (Bellwood et al. 2006b).
If corals do recover and remain the dominant habitat-forming species on coral reefs, it is still
likely that climate-induced coral bleaching will cause significant changes in community structure
(Hughes et al. 2003, 2005, McClanahan et al. 2007a). Foremost, increased frequency of mass bleach-
ing is likely to prevent community reassembly of scleractinian corals (West & Salm 2003, Donner
et al. 2005). Initial increases in coral cover within highly perturbed habitats are affected by fast-
growing, early successional corals (Hughes 1985, Golbuu et al. 2007), whereas recovery of long-
lived and slow-growing coral may take 50-100 yr (Done 1988, Fong & Glynn 2000). Fortunately,
faster-growing corals (e.g., Acropora and Pocillopora spp.) contribute most topographic complexity
(Sheppard et al. 2002) and are the major corals used by corallivorous and coral-dwelling fishes (e.g.,
Munday et al. 1997, Pratchett 2005). However, dominance by monospecific stands of coral can lead
to competitive dominance and thus reduced diversity within fish assemblages (Graham et al. 2007a).
As climate-induced coral bleaching occurs more frequently, recurrent disturbances are likely to
cause directional shifts in coral composition (Hughes et al. 2003, McClanahan et al. 2007a). There
are two possible outcomes of climate forcing on coral communities. While climate-induced coral
bleaching remains an infrequent but catastrophic occurrence, coral communities are likely to be
dominated by fast-growing early successional 'weedy' species (Acropora spp.), which persist in
habitat patches in various states of recovery (e.g., Golbuu et al. 2007). Many faster-growing corals,
such as branching Acropora and Pocillopora, are however highly susceptible to coral bleaching
(Marshall & Baird 2000, Loya et al. 2001) and may be unable to persist as bleaching becomes
more frequent and more severe. Consequently, coral communities are likely to become dominated
by bleaching-resistant species (Hughes et al. 2003, McClanahan et al. 2004, Arthur et al. 2005,
McClanahan et al. 2007a), most of which are less structurally complex and rarely used by coral-
dwelling or coral-feeding species (Bellwood et al. 2006a, Golbuu et al. 2007, Munday et al. 2007).
Future threats to biodiversity

Perhaps the most significant, and irreversible, consequence of climate-induced coral bleaching on
coral-reef fishes will be the extinction of species with associated declines in biodiversity (sensu
Thomas et al. 2004). Until recently, the occurrence and importance of species losses on coral reefs
has been largely overlooked because (I) marine species are generally predicted to be much less
prone to extinctions because marine environments are more 'buffered' against environmental
change (Carlton 1993), (2) marine species are expected to be less vulnerable to extreme population
fluctuations owing to their large geographic ranges (Gaston 1994) and (3) high diversity may confer
a degree of functional redundancy by which some species are expendable (Steele 1991). On the
269
contrary, climate change is already implicated in species extinctions across a wide range of ecosys-
tems (e.g., Fahrig 2001, Walther et al. 2002, Julliard et al. 2003, Thomas et al. 2004), including coral
reefs (Hawkins et al. 2000, Dulvy et al. 2003, Munday 2004a). Climate change is greatly altering
marine environments and compounding direct anthropogenic effects (Roberts et al. 2002, Hughes
et al. 2003), causing geographically extensive habitat degradation that simultaneously affects dis-
parate populations of increasingly large-range species. Increasing fragmentation of habitat patches
may further limit the potential for remnant populations to repopulate locations where species are
extirpated (Hughes et al. 2003, Hughes et al. 2005). It is very likely therefore, that climate-induced
coral bleaching will ultimately cause global extinctions of many more coral-reef fishes. Moreover,
functional redundancy on coral reefs may have been significantly overstated (e.g., Bellwood et al.
2003). It is also important to separate functional redundancy from response diversity (Elmqvist
et al. 2003). If entire groups of fishes all respond to a disturbance in the same way (e.g., if all spe-
cies are extirpated following climate-induced coral bleaching), then ecological functions will stop
irrespective of how many species are fulfilling that role. Thus, functional redundancy in the absence
of response diversity will give a false sense of security (Bellwood et al. 2004). Even for groups with
high functional redundancy and response diversity, Naeem et al. (1994) suggest that all species are
important because the higher the number of species in a community the greater the efficiency of
biogeochemical and trophic functions (see also Tilman & Downing 1994).
Despite the potential effects of climate change and widespread habitat degradation , there are
few reported incidences of global extinctions of marine species (Dulvy et al. 2003). This is largely
attributable to the fact that detecting species extinctions in marine environments is very difficult
(Dulvy et al. 2003) and there are no large-scale, phylogenetically controlled datasets on population
decline (Munday 2004a), such as those available for terrestrial species. However, extinction risk for
individual species may be predicted based on an individual's susceptibility to disturbance and inher-
ent biological properties such as longevity, population dynamics, population size and geographic
range (McKinney 1997, Purvis et al. 2000, Dulvy et al. 2003). In terrestrial environments, it is spe-
cies with small populations, restricted geographic ranges, and limited ecological versatility that are
most at risk of extinction from climate change and associated habitat degradation (Owens & Bennett
2000, Julliard et al. 2003). Similarly, in marine systems it is rare, endemic and highly specialised
coral-reef fishes that have recently disappeared or are committed to extinction (Hawkins et a l. 2000,
Munday 2004a). Importantly, species with multiple traits that predispose them to extinction (e.g.,
restricted geographic ranges and small population size) face a disproportionate risk of extinction
(e.g., Williams et al. 2006). To assess extinction risk of coral-reef fishes caused or exacerbated by
climate-induced coral bleaching, this review attempts to identify species that have restricted ranges,
are locally rare and are highly specialised with specific reliance on corals.
Restricted-range coral-reeffishes
Geographic ranges of coral-reef fishes are mostly very large, but vary greatly (Hughes et al. 2002,
Bellwood et al. 2005). Forcipiger flavissimus, for example, is the most widespread butterftyfish
(geographic range of 1.06 x 108 km 2) with a circumtropical distribution as well as a very large
latitudinal range (from 34°N to 32°S). At the other extreme, there are some coral-reef fishes with
extremely small geographic ranges (<l km 2), and these species may be much more susceptible to
extinction due to an increased probability that any given disturbance may make the species unvi-
able (Gaston 1998). Several recently discovered coral-dwelling gobies (Gobiodon spp.) are currently
known from only one site each in Papua New Guinea (Munday et al. 1999). The abundance of
one of these species declined precipitously following extensive mortality of its preferred host coral
on nearshore reefs, and it may be threatened with extinction due to ongoing habitat deg radation
throughout its known range (Munday 2004a). There are a relatively large proportion of fi shes (up
270
25 A can th un'd ae 25 Ch ae t o d on fd
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n = 74 species n = 127 species
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Geographic range of occurrence (log 10 km 2 )
Figure 7 The distribution of geographic ranges (log 10 km 2) for 559 species of nominal coral reef fishes (i.e.,
does not include deep-water and temperate species) within four major families. Geographic ranges were esti-
mated based on maximum area encompassed within irregular polygons around locations of occurrence, based
on data published in Hughes et al. (2002). Grey bars indicate species with geographic ranges <8 x 106 km 2
to 24% of species) with geographic extents restricted to a single reef or region (Figure 7). Hawkins
et al. (2000) define restricted-range spec ies as those with ranges <80,000 km 2 and estimate that 24%
of coral-reef fishes (n =1677 species) fit within this category. However, there are some striking taxo-
nomic differences in patterns of range size (Hughes et al. 2003, Figure 7). Across four of the major
families of coral-reef fishes (Acanthuridae, Chaetodontidae, Pomacanthidae and Pomacentridae),
25.6% of species (158/612 species) had geographic ranges <80,000 km 2 , although the proportion
of restricted-range species ranged from <7% for the Acanthuridae, 21 % for Chaetodontidae and
Pomacanthidae and up to 34% for Pomacentridae (Figure 7).
Small range size per se does not increase a species susceptibility to climate-induced coral
bleaching but means that geographically restricted disturbances can have potentially dire conse-
quences. However, the extraordinary spatial extent of habitat destruction caused by the 1998 global
mass bleaching event (Wilkinson 1998) suggests that even large-range species may be threatened
by habitat perturbations. Susceptibi Iity of fishes to extinction is probably more dependent upon their
geographical location rather than range size (Hawkins et al. 2000, Roberts et al. 2002). Species
with restricted geographic ranges that are centred within areas subject to disproportionate effects
271
of climate change and/or direct anthropogenic disturbances are at much greater risk than similarly
restricted-range species located in relatively unaffected locations and/or areas devoid of additional
anthropogenic stresses (Downing et al. 2005, Graham et al. 2007a). The severe 1982 El Nino is
blamed for the extinction of Azurina eupalama, a plankton-feeding damselfish that was endemic
to the Galapagos Islands (Jennings et al. 1994). Meanwhile, A. hirundo, an ecologically equivalent
species persists in the Guadalupe and Revillagigedo islands (Allen 1991).
Rarity in coral-reef.fishes
Risk of extinction is intuitively much greater for populations comprising few individuals compared
with larger populations. For example, smaller populations are much more likely to become non-
viable following stochastic reductions in population size (Gaston 1994). There are many examples
of 'rare' coral-reef fishes that are rare not only because they are geographically restricted, but
also because they have consistently low local abundance throughout their geographic ranges (Jones
eta!. 2002). Chaetodon bennetti, for example, is relatively widespread but never common (Allen
et a!. 1998); mean densities of C. bennetti across three geographically separated locations in the
southern Pacific (<1 individual ha- 1) are an order of magnitude lower than those of the next-rarest
species (M. Pratchett & M. Berumen unpublished data). For terrestrial species there is a consis-
tent and often-striking positive relationship between geographic ranges and population abundance
(Gaston 1998, Lawton 1999). For coral-reef fishes, however, previous studies have failed to detect
any relationship between geographic range size and local abundance (Jones et al. 2002). For both
Chaetodontidae and Acanthuridae, which are the only families of fishes for which there are good
data on local abundance of multiple species across geographically widespread locations, there is no
apparent relationship between geographic ranges of occurrence and mean abundance (Figure 8).
It is possible that restricted-range species are much more common than expected due to historical
effects of extinction filtering (Williams et al. 2006), by which extant species with restricted ranges
have only persisted by virtue of their high abundance. However, despite a generally poor relation-
ship between range size and abundance among reef fishes (Jones et al. 2002), there are coral-reef
fish species that are geographically restricted and locally rare (Figure 8; Acanthurus polyzona and
Prionurus punctatus). Perhaps these species are destined for extinction .
Extreme rarity can predispose a species to extinction but common species are also likely to dis-
appear if they are highly susceptible to particular disturbances. Recurrent disturbances, predicted
to result from sustained and ongoing climate change, are likely to have successive and cumula-
tive effects on all susceptible species (Smith & Buddemeier 1992), irrespective of their geographic
range. For example, species of fishes and corals that experienced significant declines in abundance
during the 1998 global mass bleaching may become extinct if locally severe and geographically
extensive mass bleaching reoccurs within the time required for affected populations to recover.
Coral-reef fishes at greatest risk are those that exhibited disproportionate declines in abundance
during previous mass bleachings. Thus coral-dependent and highly specialised coral-reef fishes are
increasingly likely to be threatened with extinction.
Ecological specialisation
Ecological specialisation increases extinction risk for several reasons. Foremost, specialist species
are usually expected to be geographically restricted and locally rare (Brown 1984), which increases
extinction risk. These relationships notwithstanding, specialist species are expected to be dispro-
portionately affected by changes in resource availability, compared with generalist counterparts
(Munday 2004a, Pratchett et al. 2006, Figure 6). Both Munday (2004a) and Pratchett et al. (2006)
showed that highly specialised coral-dependent species became locally extinct following coral loss
272
16
14
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Geographic range of occurrence (Log 10 km 2 )
Figure 8 Average rank abundance versus geographic range of occurrence (log 10 km 2) for coral reef fishes
from two distinct families. Rank abundance was calculated across 12- 15 geographically separated locations .
For Chaetodontidae data were derived from Jones et al. (2002), Khalaf & Abdallah (2005), and Shokri et al.
(2005). For Acanthuridae data are from Letourneur et al. (1993) and Hughes et al. (2002).
caused by mass bleaching. In contrast, more generalist (i.e., ecologically versatile) species were
relatively unaffected, presumably because they were able to exploit alternate prey resources as pre-
ferred corals were depleted (Pratchett et al. 2004). Notably, however, these patterns arise because
corals used by specialist species are a subset of corals used by more generalist species, and the coral
species most frequently used by coral-dependent fishes are also those most susceptible to bleaching
and other disturbances (Munday et al. 1997, Feary et al. 2007b, Srinivasan 2007).
Ecologically equivalent groups of coral-dependent fishes (e.g., corallivorous butterftyfishes and
coral-dwelling gobies) might be expected to exhibit some resilience to coral loss because niche-
based competition theory would predict that sympatric species each specialise on different coral
species (Schoener 1974). Therefore , selective depletion of corals (e.g., during moderate bleaching)
would affect some fishes but have limited negative or even positive indirect effects on their com-
petitors. A common pattern, however, is that many species tend to specialise on the same coral
resources, possibly because these corals confer higher individual fitness . For example, all nine
species of apogonids studied by Gardiner & Jones (2005) preferred to inhabit Porites cylindrica.
Similarly, Acropora nasuta appears to be a preferred coral habitat for a variety of Gobiodon species
273
(Munday et al. 1997, 2001), probably because growth and survival are higher for a range of goby
species in this coral (Munday 2001). Specialisation and reliance on a relatively small suite of coral
species increased the vulnerability of coral-dwelling species to declines in the availability of those
coral resources. To what degree coral-dependent species will shift their resource use if preferred
coral habitats decline is unknown (e.g., Pratchett et al. 2004) but it is clear that at least some spe-
cies are strict specialists that use only a narrow range of coral types (e.g., Munday 2004a, Berumen
& Pratchett 2008) and loss of these habitats will have serious implications for their persistence
(Munday 2002).
Ecological theory predicts that specialists should have smaller ranges than generalist species
because the distributions of specialist species are more likely to be constrained by the distribution
of a few key resources than are the distributions of generalist spec ies that can use a wide range of
resources (Brown 1984). If this relationship holds, highly specialised species may face a 'double
jeopardy' of extinction or even a 'triple jeopardy' where specialist species are also rare (Hawki ns
et al. 2000, Munday 2004a). A ll the evidence to date suggests that coral-dependent fishes do not,
on average, have smaller geographic ranges than other coral-reef fishes, possibly because the coral
species used have widespread distributions themselves or because the fishes change their patterns
of resource use in accordance with the relative abundance of different coral species in different
geographic regions. Both of these alternatives appear likely. Gobiodon species A, an extreme spe-
cialist that inhabits just one species of coral (Acropora tenuis) has a geographic distribution extend-
ing from Japan to the southern GBR (Munday et al. 1999). The widespread distribution of its host
coral probably contributes to the relatively large geographic range of this coral goby. Gobiodon
histrio, which has an even larger geographic range, prefers the same suite of coral species at loca-
tions separated by thousands of kilometres (Munday 2002). In contrast, G. quinquestrigatus, which
uses a range of coral species within sites, also changes its pattern of habitat use among geographic
locations (Munday 2002). Moreover, Jones et al. (2002) found no clear relationship between geo-
graphic range size and specialisation for either butterftyfishes or anemonefishes. A similar conclu-
sion regarding the relationship between range size and specialisation in anemonefishes was also
reached by Ollerton et al. (2007).
Specialist species are also expected to be less common compared with generalist counterparts
because their populations are more likely to be constrained by the abundance of specific resources
(Brown 1984). There is some evidence among coral-dependent fishes that specialists have smaller
populations than generalists but the pattern is far from consistent. Coral-dwelling gobies that inhabit
just one or two coral species tend to have smaller population sizes than generalists and their popula-
tions decline more rapidly following loss of preferred habitat (Munday 2004a). In contrast, butter-
fly fishes that are specialist coral feeders are often locally abundant and can have higher densities
than many generalist species (Jones et al. 2002). For example, Chaetodon trifascialis is the most
specialised of coral-feeding fishes , feeding almost exclusively on Acropora hyacinthus (Pratchett
2005), and yet it is also the most widely distributed of butterfly fish species (Allen et al. 1998) and
frequently ranks in the top three most abundant butterftyfishes throughout its geographic range
(Jones et al. 2002). For butterftyfishes generally, there are many species that might be considered to
have an increased risk of extinction owing to (l) relatively small geographic ranges, (2) consistently
low abundance or (3) extreme dietary specialisation (Figure 9). There are, however, surprisingly few
butterftyfishes that face multiple jeopardy of extinction. For example, the only dietary specialist that
has a restricted geographic range (<80,000 km 2) is Chaetodon larvatus, which is the most abundant
butterftyfish throughout its range.
Other factors that increase susceptibility to extinction include short lifespan and low intrinsic
rates of population growth (Pimm et al. 1988). In many cases, these aspects of population demo-
graphics would balance each other, such that short-lived species would be expected to have higher
turnover and greater potential for population growth. Consequently, both short-lived and long-lived
274
(A) Dietary specialisation
(B) Restricted range (C) Low abundance
Figure 9 Venn diagram showing the number of Chaetodontidae (of 127 species) facing increased risk of
extinction due to (A) dietary specialisation, in that they selectively consume only one or two different coal
genera (the numbers in parentheses refer to all obligate coral-feeding species), (B) restricted geographic ranges
(<80,000 km 2) and/or (C) consistently low abundance.
species may be equally susceptible to extinction for very different reasons, and identifying outliers
in the expected relationship between longevity and population growth might be critical in estab-
lishing species-specific extinction risk. Overall, it appears the highly specialised coral-dependent
fishes face the greatest risk of extinction from future mass bleaching and associated coral loss,
although unexpected extinctions may also arise due to added effects of exploitation and other distur-
bances (Hawkins et al. 2000, Dulvy et al. 2003). Many highly specialised coral-dwelling fishes are
extremely small and cryptic (Munday & Jones 1998, Bellwood et al. 2006a), suggesting that recent
mass bleaching and degradation of coral-reef habitats may have already caused numerous, but as yet
unappreciated, extinctions (Dulvy et al. 2003).
Socioeconomic consequences
Worldwide, the goods and services that coral reefs provide are estimated to be worth almost U.S.$30
billion yr- 1 (Cesar et al. 2003). Sustained and ongoing climate-induced coral bleaching will signifi-
cantly diminish the value of these goods and services , resulting in serious consequences for peo-
ple and even countries dependent on coral reefs (Hoegh-Guldberg 1999, Wilkinson 1999, 2000b,
Hughes et al. 2003, Lesser 2004). Coral bleaching has the potential to affect fisheries, the liveli-
hoods and health of fisheries-dependent communities, reef-related and coastal tourism and impor-
tant ecosystem services provided by reefs (Wilkinson 1999, Westmacott et al. 2000a, McClanahan
et al. 2002a, Cesar et al. 2003, Grandcourt & Cesar 2003, Sheppard et al. 2005, Graham et al.
2007b). To date, empirical studies have focused largely on the effects of bleaching on fisheries and
tourism, which are the most obvious immediate effects (but see Sheppard et al. 2005).
Fisheries
Coral bleaching has the potential to affect reef and reef-related fisheries through a number of mech-
anisms: (I) coral mortality or structural loss may cause a decline in the abundance of reef-related
275
fishes (i.e., those that depend on coral for settlement, feeding, dwelling or are associated with the
reef structure), leading to reduced catches of these fishes (Westmacott et al. 2000a, Graham et al.
2007b), (2) highly mobile predatory species, although not directly dependent on reef structures, may
decline in abundance following declines in abundance of prey species (Westmacott et al. 2000a),
(3) declines in reef fish biodiversity may lead to a reduction in energy transfer to higher trophic lev-
els, which may mean that reefs will support a reduced biomass of higher-order predators (Munday
et al. 2007), (4) many fishes can be negatively affected by a high abundance of late-successiona l
algae (McClanahan et al. 2002b) that may dominate after coral mortality; (5) coral mortality may
cause a reduction in abundance of some small-bodied ornamental coral-feeding and coral-dwelling
fishes, which are valued by the aquarium trade (Wilson et al. 2006) and (6) macroalgae habitats
attract some invertebrates (McClanahan et al. 200la), such that the abundance of some invertebrate
feeders may increase (Pratchett et al. 2008). These changes in the relative abundance of targeted
species are likely to significantly affect fisheries yields, species composition of catches and the
economic value of coral-reef fisheries (Westmacott et al. 2000a). Most likely, catch composition
will change even if there is no decline in catch rates, which may reduce the total value of landings
(Westmacott et al. 2000a).
Despite potential effects of climate-induced coral bleaching on coral-reef fisheries, no studies
have actually shown that total catch, catch composition, or value of fisheries have been affected by
severe mass bleaching (McClanahan et al. 2002a, Grandcourt & Cesar 2003). However, detect-
ing definitive effects of coral bleaching on fisheries yields may be very difficult because the con-
founding effects of overfishing in many locations outweigh any effects that loss of live coral may
have on temporal trends in fisheries yields. For example, in Mombasa, Kenya, Westmacott et al.
(2000a) found a decline in catch while effort remained the same but concluded that bleaching had
no detectable effect because the rate of decline in the fishery was consistent for several years prior
to the bleaching. In a longer-term study of Kenyan fisheries (1994-2001), McClanahan et al. (2002a)
found that catches of Siganidae overall were reduced by 8% after the bleaching and that catch per
fisherman per day decreased 20-30% for Siganidae and Scaridae but they attribute most of this
change to a 17% rise in fishing effort over the study period. Likewise, in the Seychelles fishery, low
abundance and yield of herbivorous Siganidae post-bleaching was attributed to a prebleaching trend
associated with fishing effort (Grandcourt & Cesar 2003). These results reinforce the importance of
examining long-term trends , fishing effort and catch composition rather than simply documenting
changes in focus parameters immediately before and immediately after punctuated disturbances
(Hughes & Connell 1999).
Failure to detect significant effects of climate-induced coral bleaching on coral reef fis her ies
may also be due to the fact that many fisheries mainly target fishes that are not dependent on coral
(e.g., Acanthuridae, Siganidae, Scaridae and various planktonic spec ies) (Bellwood 1988, Goreau
et al. 2000, Figure 10). In artisanal fisheries in both Kenya and Papua New Guinea, coral-dependent
fishes made up only a very small proportion of the species and individuals caught (Fig ure 10).
Despite major differences in fishing intensity (Cinner & McClanahan 2006), the overwhelming
majority of fishes caught in both these fisheries were associated with the reef structure but not
explicitly reliant on live corals. There were also significant landings of fishes that are not really
dependent on coral reefs but may be caught in the proximity of coral reefs (e.g., Carangidae and
Scombridae) (Figure 10). These data suggest that artisanal fisheries may be relatively unaffected by
coral loss caused by climate-induced coral bleaching but there could be major consequences associ-
ated with the longer-term declines in topographic complexity (Graham et al. 2007b). However, the
significant lag between the coral loss and its potential effect on most target fish populations might
mask the effects of bleaching on fisheries' catches. Changes in fishing locations or habitats, coinci-
dental with bleaching (Westmacott et al. 2000a), or simultaneous/subsequent disturbances such as
cyclones, increased sedimentation, or freshwater run-off (Jones et al. 2004, Munday 2004a), may
276
Papua New Guinea

(n = 244 s pec ies/2,396 individuals)
80
o Species caught
70 c Individuals caught
60
50
40
..c 30
u
13 20
40
30
20
10
ｏＫｌＭｾｲ＠
Coral-dependent Habitat-dependent Reef-associated
Figure 10 Relative contribution (by species and individuals) of coral-dependent, habitat-dependent, and
reef-associated fishes in artisanal fisheries in Papua New Guinea and Kenya. Categories of associations were
inte nd ed to represent decreasing susceptibility to climate-induced habitat modification ion coral reefs. Data
were reana lysed from Cinner & McClanahan (2006) and McClanahan & Mangi (2004).
also make it difficult to establish the relative importance of different disturbances. Consequently,
effects of climate-induced coral bleaching on coral-reef fisheries are likely to be difficult to detect
becau se they are highly protracted and potentially masked by a wide range of other factors .
Economic costs of coral bleaching on coral-reef fisheries may be most apparent in niche fish-
eries targeting mainly coral-dependent fishes (e.g., aquarium fisheries). The international marine
ornamental fish trade is currently worth U.S.$90-300 million yr- 1 (Sadovy & Vincent 2002) and
mostly targets small coral-reef fishes such as the Pomacentridae, Chaetodontidae, Monacanthidae
and Apogonidae (Kolm & Berglund 2003, Tissot & Hallacher 2003, Lunn & Moreau 2004).
Many of these fishes (especially butterfly fishes) are coral dependent and thus highly susceptible to
climate-induced coral bleaching. However, it is unclear if or how this fishery might be affected by
significant declines in wild populations of coral-dependent fishes . Importantly, aquarium fisheries
may opportunistically exploit individuals from a range of targeted species, such that overall catch
rates are insensitive to fluctuations in relative abundance of different species. However, the most
specialised of coral-reef fishes are often difficult to maintain in aquaria (Allen et al. 1998, Michael
2004) and generally not targeted for the ornamental trade (Allen et al. 1998).
Analyses of the predominant fish species caught for the ornamental trade confirm that relatively
few are coral dependent. Of the 124 most expensive ornamental fish species caught around the world,
80% were associated with the habitat structure but only 15% were coral dependent (Figure 11).
277
80.0 200
70.0
..c 160
8 ;;:;
"'
u 60.0 VJ
"§ 2
ｾ＠
"'0> 50.0 120 <J:
...
E "'0.
c: 40.0
.2
:; Ｍｾ＠ "'
0.
:g 30.0
80
c0
"""'ｾ＠
u "'>
c 20.0
40 !3
-<
"'ｾ＠
"' 10.0
c..
D
0.0 0
Coral-dependent Habitat-dependent Reef-associated
Figure 11 The proportion of fish caught and average price paid per fish for the 124 most expensive species
in the ornamental fishery for coral reef fishes categorised as coral-dependent, habitat-dependent and reef-
associated. Categories of associations were intended to represent decreasing susceptibility to climate-induced
habitat modification on coral reefs. Prices were obtained from the Aquatic Connections aquarium supply retail
shop (Sunrise, Florida, USA) website (see Sadovy & Vincent 2002).
Interestingly, there was significant variation in the average price of fishes within these three groups;
the price was highest for coral-dependent species and lowest for non-reef species (Figure 11). This
may suggest that the species most susceptible to bleaching are also in high demand, or at least attract
greater value. Therefore, climate-induced coral bleaching might be expected to affect total value if
not the overall catches of aquarium fishes. Notably, there was a marked decline in the total value of
marine aquarium fishes imported into Hong Kong in 1997-1998, driven mainly by decline in the
value of imports from Indonesia and the Philippines (Chan & Sadovy 1998). These economic trends
are not currently attributed to overriding effects of mass bleaching but to coincidental changes
in the national metrics used to record imports of marine aquarium fishes (Chan & Sadovy 1998).
However, the recent disappearance of several coral-dependent fishes from aquarium catches (e.g.,
Oxymonocanthus longirostris) has been directly attributed to declines in local stocks following the
1998 mass bleaching (Dulvy et al. 2003).
Tourism
In contrast to the rather inconclusive studies concerning effects of bleaching on cora l-reef fisher-
ies, several studies have been able to detect and project the effects of coral bleaching on reef-based
tourism (e.g., Westmacott et al. 2000b, Uyarra et al. 2005, Andersson 2007). Bleaching has been
found to negatively affect tourism and tourism-related industries by reducing the attractiveness of
particular locations or activities for tourists, resulting in a change of either destination or activity
and subsequent loss of reef-related revenue (Westmacott et al. 2000b, Uyarra et al. 2005). Tourists'
perceptions of changes in coral-reef habitats after bleaching are often limited (except where there
has been extensive degradation and extensive loss of fishes) but knowledge of recent bleaching
may influence where tourists choose to dive (including snorkelling) on both small spatial scales
(i.e., a particular dive site) and large spatial scales (i.e., a particular country or region). In Kenya
and Tanzania, >75% of divers avoided dive sites known to be recently bleached (Westmacott et al.
2000a, Andersson 2007). Where user fees exist for access to marine protected areas and areas under
278
customary ownership, changes in specific dive site selection may affect revenue generation used for
reef management and community development. On a larger scale, bleaching may reduce national
and regional economies by influencing the choices of destinations. For example, 19% of Zanzibar,
Tanzania, and 30% of Mombasa, Kenya, tourists would change their holiday destination as a result
of bleaching (Westmacott et al. 2000a), 80% of tourists visiting Bonaire would be unwilling to
return at equivalent cost in the event of coral bleaching (Uyarra et al. 2005) and there was 5-10%
decline in the number of tourists visiting Palau subsequent to the 1998 coral bleaching (Graham
et al. 2000).
The recreational value of diving in Kenya and Tanzania was no different in 1999 (after wide-
spread bleaching) from 1996 (before the bleaching), suggesting that visitors were still eager to visit
and view coral-reef habitats (Westmacott et al. 2000a). However, the divers in 1999 were less expe-
rienced than divers in 1996, suggesting that more experienced divers may have chosen to dive in
alternative regions that experienced less bleaching. In 1999, estimates of economic losses from diver
satisfaction ranged from U.S.$1.6-4.8 million in Zanzibar (Ngazy et al. 2002). A 'willingness to
pay' survey of tourists in the Philippines found that individual divers were prepared to pay an aver-
age of U.S.$202 more to dive a 'pristine' reef compared with a bleached or degraded reef, whereas
snorkellers were willing to pay an additional U.S.$25 (Cesar 2000).
Overall economic losses attributable to recent climate-induced coral bleaching are staggering,
ranging from tens of millions of dollars for a single country to billions of dollars for the Indian
Ocean (Wilkinson 1999, Cesar 2000, Westmacott et al. 2000a). For example, changes in destination
choice and decreases in consumer surplus (i.e., the value of the dive experience to the diver less the
costs of the vacation) resulted in total losses to the Palau tourism industry as high as U.S.$750,000
over the 2 yr following bleaching (Graham et al. 2000). In the Philippines, recent bleaching is
predicted to result in economic losses ranging from U.S.$6 million to as high as U.S.$27 million,
depending on the time required for reefs to recover (Cesar 2000). The overall economic damages
from the 1998 coral bleaching event in the Indian Ocean (over a 20 -yr time frame with a 10% dis-
count rate) could be over U.S.$8 billion; U.S.$1.4 billion loss of food production/fisheries, U.S.%3.5
billion loss of touri sm revenue, U.S.$2.2 billion loss of coastal protection and U.S.$1.2 billion in
other services (Wilkinson 1999, Westmacott et al. 2000a).
Managing effects of climate-induced coral bleaching

Managing effects of climate change on coral reefs represents a considerable challenge, especially
given that reef managers themselves cannot prevent the predicted increases in sea temperat ures
and storms that are associated with climate change. However, by reducing other stressors on the
reef environment (e.g., overfishing, pollution and sedimentation) reef managers could potentially
increase resilience to climate-induced coral bleaching and reduce the likelihood of catastrophic and
irreversible changes in habitat structure, as has been suggested by Hughes et al. (2003) and West &
Salm (2003). Considerable research is still needed to establish links between management and reef
resilience (McClanahan & Maina 2003, Jones et al. 2004, McClanahan et al. 2005). It seems logical ,
however, that minimising direct anthropogenic stresses will serve to maximise the capacity of reefs
to withstand climate-induced coral bleaching. At the very least, coral communities on reefs with
intact fish assemblages and minimal additional stresses will have a greater chance of recovering
after bleaching (Brown 1997, Mumby et al. 2006, Hughes et al. 2007). Accordingly, the objectives
of coral-reef management should be 3-fold: (I) eliminate or minimise extrinsic disturbances (pol-
lution and sedimentation, e.g., Orpin et al. 2004), (2) protect threatened and functionally important
species (Bellwood et al. 2004) and (3) abolish destructive activities (e.g., blast fishing) that degrade
benthic reef habitats (Kaiser et al. 2000, Baird et al. 2005). There are a variety of management tools
that may be adaptively employed to achieve these objectives, including ban s on catching particular
279
spec ies, gea r restrictions, or prohibiting a ll extractive activities (McClanahan & Cinner 2007), but
their relevance and effectiveness are very context specific, depending on a range of social, eco-
nomic and cultural factors (McClanahan et al. 2006, Cinner 2007, Cinner et al. 2007). For example,
prohibiting all extractive activities within specified areas (no-take areas) may be the best way to
ensure minimal levels of protection for heavily exploited species (Russ 2002) but resource users
may be more amenable to gear-based bans (McClanahan et al. 2006). Restricting the use of certain
gear types (e.g., gill and seine nets that tangle in corals) may also have added benefits of preventing
declines in topographic complexity (Kaiser et al. 2000, McClanahan & Cinner 2007).
Marine protected areas that limit or prevent (e.g., no-take areas) extractive activities are con-
sidered by many as currently the most effective way to minimise long-term consequences of cli-
mate-induced coral bleaching on coral-reef ecosystems (e.g., Westmacott et al. 2000b, Marshall &
Schuttenberg 2006a,b). Protecting large areas of reef from fishing helps to preserve the abundance
and diversity of exploited fish species (Halpern & Warner 2002, Russ 2002). Where exploited spe-
cies include important herbivorous fishes, this protection may be fundamental to rapid recovery
of coral communities following climate-induced coral bleaching (Bellwood et al. 2003 , Hughes
et al. 2007). However, marine protected areas must be recognised as a small part of the solution
to problems faced by coral reefs because, ultimately, they cannot protect coral-reef ecosystems
from extrinsic disturbances (Gray 1997, Boersma & Parrish 1999, Jones et al. 2004, Hughes et al.
2005). Importantly, marine protected areas encompass only a minor proportion of coral-reef area
(Wilkinson 2004) and may detract from effective management of broader-scale issues (Bellwood
et al. 2004, Hughes et al. 2005, Jones et al. 2007). Moreover, marine protected areas benefit exploited
species when habitat is degraded (e.g., Hawkins et al. 2006) but the majority of small and potenti ally
threatened coral-reef fishes are not exploited (e.g., Munday 2004a). The greatest threats to marine
biodiversity throughout the world occur in coastal zones near to high population densities, where
pollution , marine litter, eutrophication, species introductions/invasions, water-shed alteration and
physical alterations of sea margins have contributed to habitat loss and habitat conversion, with the
associated loss of species (Gray 1997). A substantial proportion of the g lobal human popul ation
(-8%) now lives within 100 km of coral reefs, and burgeoning populations continue to put pressure
on these sensitive ecosystem s (Hawkins et al. 2000). This is a particular problem in Indonesia where
areas with greatest biodiversity are situ ated closest to centres of highest human population growth
(Gray 1997). If marine biodiversity is to be conserved, better protection and management of coastal
zones and catchments, which are rarely included with marine protected areas, are needed.
Beyond simply conserving biodiversity, strategic placement of marine protected areas may be
used to protect habitats that support high abundance of particularly threatened and ecologically
important coral-reef fishes (Beger et al. 2003, Roberts et al. 2003). Herbivorous fishes , for exa mple,
are considered to be important in facilitating recovery of coral communities following ex tensive
morta lity (Mumby et al. 2006, Hughes et al. 2007) and preventing phase shifts to highly undesir-
able algal-dominated habitats (Hughes et al. 2003, Bellwood et al. 2004). Other importa nt spe-
cies are keystone predators that regulate the deleterious effects of prey species (e.g., McClanaha n
2000, Dulvy et al. 2004) or fulfil unique but critical ecological functions (Bellwood et al. 2003).
Balistapus undulatus, for example, is a major predator on bioeroding sea urchins and is hypo-
thesised, therefore, to have indirect positive effects on coral recruitment and cover (McClanahan
1995, 2000). In some cases, these key species may be deserving of special protection at a global
scale (e.g., worldwide bans on exploitation) (Wood 2004). There are already worldwide ban s on the
exploitation of heavily exploited food fishes , such as Cheilinus undulatus, enacted under the 1973
Washington Convention on International Trade in Endangered Species of Wild Fauna and Flora
(CITES) (Sadovy 2005). Similar levels of protection or ex situ conservation may be fund amental
280
to preventing the extinction of rare or threatened species (Wood 2004) and functionally important
spec ies and groups (Bellwood et al. 2003, 2004).
This review emphasises the importance of both live coral cover and topographic complexity
in maintaining diverse communities of coral-reef fishes. As such, live coral cover and topographic
complexity need to be recognised as critical components of coral-reef ecosystems and managed
accordingly. Branching corals are especially important in providing surface topography, food
and habitat for coral-reef fishes (Jones et al. 2004) but are also highly susceptible to bleaching
(Marshall & Baird 2000) and other direct anthropogenic stresses (e.g., destructive fishing practices,
McManus et al. 2004). To minimise reductions in structural complexity caused by climate-induced
coral bleaching (e.g., Graham et al. 2006), there need to be unequivocal reductions in destructive
activities (e.g., blast fishing, seine netting, coral mining and anchor damage) that compromise topo-
graphic complexity (McManus et al. 2004). Some reefs have a high level of landscape complexity,
such that even after the framework provided by branching corals collapses, caves, crevices and over-
hangs remain intact (e.g., Ha lford et al. 2004). The call for the establishment of marine protected
areas in habitats that are somewhat resistant to coral bleaching and subsequent physical degradation
(e.g., West & Salm 2003, Marshall & Schuttenberg 2006a, Salm et al. 2006) may provide a source
of population replenishment for nearby reefs that are damaged by bleaching (Graham et al. 2007a,
McClanahan et al. 2007a). However, it is imperative that structural complexity is protected both
inside and outside marine protected areas.
The importance of structural complexity also raises the question of engineering increased topo-
graphic complexity to retain fish diversity in the likely event of reef collapse. Human intervention
in coral-reef recovery is, however, rarely effective on large spatial scales and the exorbitant costs
associated with engineering recovery in already degraded reef systems may be better spent on
increasing protection of nearby healthy coral systems that will enhance natural recovery processes
and ensure the continuity of ecosystem function (Spurgeon & Lindahl 2000, Adger et al. 2005).
Habitat management is also important in adjoining habitats, such as mangroves, seagrass meadows,
estuaries and coastal wetlands. These habitats are important nursery and juvenile habitats for many
coral-reef fishes (Nagelkerken et al. 2000, 2002), some of which, like the rainbow parrotfish, Scarus
gaucamai, are important grazers (Mumby et a l. 2004). Furthermore, these habitats stabilise coast-
lines, preventing erosion and filtering sediments, nutrients and pollution from terrigenous sources
that may exacerbate existing stresses to corals. All coastal habitats are increasingly threatened by
terrestria l development, as well as climate change (Roessig et al. 2004, Poloczanska et al. 2007),
and require additional protection to prevent their continued loss or degradation .
Conclusions and future directions

This review reveals that habitat structure, particularly coral cover and topographic complexity, plays
a critical and probably underappreciated role in structuring reef fish assemblages. Sustained and
ongoing climate-induced coral bleaching, which can cause coral loss and reduced topographic com-
plexity, may therefore have profound effects on the abundance, diversity and community structure
of coral-reef fishes (e.g., McClanahan et al. 2002a, Jones et al. 2004, Munday 2004a, Pratchett
et al. 2004, 2006, Sano 2004, Bellwood et al. 2006a, Garpe et al. 2006, Graham et al. 2006). Coral
loss has unequivocal effects on highly specialised fishes that feed or shelter on live corals but the
effects of extensive and lasting coral loss extend well beyond those fishes that are traditionally
thought to need live coral (e.g., butterflyfishes, damsel fishes and gobies; Jones et al. 2004). There is
also strong evidence that topographic complexity is an important attribute in maintaining species
diversity of coral-reef fishes, which is likely to be fundamental in limiting ecological and economic
consequences of climate-induced coral bleaching. In general, communities of coral-reef fishes can
281
recover quickly following temporary reductions in coral cover (e.g., Halford et al. 2004), and may
exhibit considerable resilience to climate-induced coral bleaching, as long as the physical structure
is not compromised. Here, adaptive management may be critical in preventing declines in topo-
graphic complexity and protecting against long-term shifts ｩｾ＠ the structure of coral communities
toward less structurally complex bleaching-resistant corals (e.g., Hughes et al. 2003, McClanahan
et al. 2007a). The longer-term consequences of climate change and coral bleaching for coral-reef
fishes are far from certain, but reducing direct anthropogenic pressures and improving management
of coral-reef habitats are important elements in preventing ecological and economic consequences
of declines in the abundance and diversity of coral-reef fishes.
Effects of climate-induced coral bleaching are compounding pre-existing pressures from natural
and direct anthropogenic stresses (e.g., overfishing, pollution, excess nutrients and disease epidem-
ics) to accelerate and exacerbate widespread degradation of coral-reef ecosystems (Nystrom et al.
2000, Jackson et al. 2001, Kleypas et al. 2001, Nystrom & Folke 2001, Hughes et al. 2003, Pandolfi
et al. 2003). To prevent further declines in the condition of coral-reef habitats, and thereby con-
serve communities of coral-reef fishes, it is imperative to move beyond traditional reduction ist man-
agement strategies (e.g., marine protected areas) to implement adaptive and targeted management
strategies that recognise individual and critical components of habitat structure (e.g., topographic
complexity). This requires an entirely different approach to management, requiring bold decisions
to prioritise conservation of critical functional attributes rather than focusing on individual stocks
or species. Protection of critical habitat attributes is much more achievable and probably far more
effective at providing ecosystem resilience than current efforts aimed at preserving biodiversity.
This review has focused on climate-induced coral bleaching, which until now has been the most
apparent and devastating effect of climate change in coral-reef ecosystems. However, the potential
effects of climate change on coral-reef habitats and reef fishes are extensive (reviewed by Roessig
et al. 2004, Munday et al. 2007, Poloczanska et al. 2007). Global climate change will not only raise
the temperature of the oceans but also cause major changes in sea level, hydrodynamic conditions
and ocean chemistry (Roessig et al. 2004, Poloczanska et al. 2007). Increasing concentrations of
atmospheric carbon dioxide are reducing pH and altering the carbonate-bicarbonate ion balance in
the world's oceans (Pelejero et al. 2005). Consequences of these changes for scleractinian corals
are weaker skeletons, reduced extension rates and increased susceptibility to erosion (Kieypas et al.
1999, Orr et al. 2005). As ocean acidification undermines the structural integrity of coral skeletons,
predicted increases in the frequency and severity of severe tropical storms (Henderson-Sellers et al.
1998, Walsh 2004, Webster et al. 2005) are likely to lead to increased breakage and dislodgement
of corals (Madin & Connolly 2006), further affecting topographic complexity and 3-dimensional-
ity of coral-reef habitats. Furthermore, sea-level rise combined with erosion of shallow-water habi-
tats may threaten shallow-water specialists. Increased sea temperatures, reduced ocean acidity and
modified circul.ation patterns could also have significant direct effects on individual performance
and population dynamics of coral-reef fishes (Munday et al. 2007). It is hoped appreciation of the
likely impacts of climate change on coral-reef fishes will fuel international efforts to take action on
climate change, while bold management initiatives are needed to maximise capabilities of coral-
reef ecosystems to withstand future and unexpected effects.
Acknowledgements
This contribution was supported by the ARC Centre of Excellence for Coral Reef Studies and
Leverhulme Trust. We are grateful to colleagues and collaborators, especially A. Cole and M.
Berumen, who have contributed unpublished data, as well as D. and L. Pratchett, who helped ready
the review for publication. A. Hoey and T. Schenk assisted in compiling data. Comments by T. Hughes
and A. Baird greatly improved the review.
282
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Taylor & Francis
OTOLITH CHEMISTRY TO DESCRIBE MOVEMENTS AND

LIFE-HISTORY PARAMETERS OF FISHES: HYPOTHESES,
ASSUMPTIONS, LIMITATIONS AND INFERENCES
TRAVIS S. ELSDON 1, BRIAN K. WELLS 2 ·3 , STEVEN E. CAMPANN,
BRONWYN M. GILLANDERS 1, CYNTHIA M. JONES 5, KARIN E. LIMBURG 6 ,
DAVID H. SECOR7, SIMON R. THORROLD8 & BENJAMIN D. WALTHER 8
1
Southern Seas Ecology Laboratories, School of Earth and Environmental Science,
University of Adelaide, SA 5005, Australia
E-mail: travis.elsdon@adelaide.edu.au, bronwyn.gillanders@adelaide.edu.au
2Southwest Fisheries Science Center, Fisheries Ecology Division, Santa Cruz, CA 95060, USA
E-mail : Brian.Wells@noaa.gov
3 University of California Santa Cruz, Long Marine Laboratory, Santa Cruz, CA 95060, USA
4
Population Ecology Division, Bedford Institute of Oceanography,
Dartmouth, Nova Scotia B2Y 4A2, Canada
E-mail: campanas@mar.dfo-mpo.gc.ca
5Center for Quantitative Fisheries Ecology, Old Dominion University, Norfolk, VA 23529, USA
E-mail: cjones@odu.edu
6 State University of New York College of Environmental Science and Forestry,
Syracuse, NY 13210, USA
E-mail: KLimburg@esf.edu
7Chesapeake Biological Laboratory, University of Maryland Center
for Environmental Science, Solomons, MD 20688, USA
E-mail: secor@cbl.umces.edu
xwoods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
E-mail: sthorrold@whoi.edu, benjwalther@gmail.com
Abstract In ever-increasing numbers, researchers wish to extract information based on chemi-

cal analyses from otoliths to determine movements and life-history patterns of fish. Such analyses
make assumptions about chemical incorporation and interpretation that are beyond those that are
important for stock discrimination studies, another common application. The authors aim to clarify
the methods of determining fish movement based on natural and artificial otolith chemical tags and
review current trends in determining movement using otolith chemistry, otolith sampling methods,
and what influences otolith chemistry. Both spatial and temporal variability in water and otolith
chemistries, which underpin the assumptions of several methods, are discussed. Five methods for
determining movement and migration of fish are outlined: (1) estimates of movement and life-history
traits of a single fish group, (2) assessing connectivity among groups using natural chemical tags in
otoliths, (3) transgenerational marks to determine parentage and natal origins, (4) profile analysis
to define life-history variation within a population and (5) profile analysis to describe movements
through different environments. Within each of these methods, background information, specific
hypotheses being tested and assumptions and limitations of each technique are provided. Finally,
297
TRAVIS S. ELSDON ET AL.
research directions required to fill current knowledge gaps a nd enhance the usefulness of otolith
chemistry to determine fish movement are identified.
Introduction
Otoliths are proving extremely valuable tools for studying movement and life-history characteristics
·of teleost fishes. The term 'movement' can be used to describe both small-scale random changes in
position or place and large-scale non-random changes from one region to another (migration ; Dingle
1996). Irrespective of the scale at which we view movements, identifying and describing movements
remains a challenge. Many techniques can be used to identify fish movements (Gillanders et al.
2003), and these can be classified into broad categories of natural tags (e.g., chemical, genetic, and
parasitic) and applied tags (passive integrated transponder tags, acoustic tags, artificial chemistry,
and archival tags). Natural chemical tags recorded in otoliths have some obvious advantages over
applied tags because all fish are marked from early life (many as embryos), the tags are usually
permanent, and tags can be related to fish age. The challenge of using natural tags is to tran slate tag
variability into an interpretable pattern of movement. Our aim is to focus on otolith chemical tags,
both those that occur naturally and those that are applied artificially. Specifically, these tags have
shown great promise for determining fish movements based on the variation in chemical composi-
tion , but technical and statistical challenges remain.
Otoliths are paired structures composed of biogenic calcium carbonate, typically in the form
of aragonite, deposited on a protein matrix . Forming part of the inner ear of teleost fishes, these
structures sit within a membrane filled with endolymph fluid (Campana 1999, Popper & Lu 2000).
Otoliths accrete new crystalline and protein material on to their exterior surface daily, and incor-
porated within these accreted layers are minor and trace elements along with the major constituents
of aragonite (C, 0, and Ca, Campana 1999) (collectively referred to as 'chemicals'; see 'Glossary').
Hence otoliths provide a chemical chronology over the entire life of a fish. Quantifying and inter-
preting the chemical composition of fish otoliths is a growing field within fish ecology. T he first
otolith chemistry papers were published up to 30 yr ago (Gauldie & Nathan 1977, Papadopoulou
et al. 1978, Gauldie et al. 1980, Kalish 1989, Radtke 1989). However, investigations of elements in
calcified structures of fish pre-date this by several decades (Dannevig 1956, Odum 1957, Sr uptake
in bone, Rosenthal 1957). Recently there has been a surge in publications that have used otolith
chemistry to determine fish movements (206 papers, 1996-2005, Campana 2005a), three interna-
tional otolith symposia with dedicated chemistry sessions (Secor et al. 1995a, Fossum et a l. 2000,
Begg et al. 2005), and several reviews (Campana 1999, Thresher 1999, Elsdon & Gillanders 2003a).
There is no doubt that variation in otolith chemistrycan be used to explore life-history informa-
tion. But what does this information tell us? How can we interpret differences in otolith chemistry
and infer possible fish movement and life-history traits? Can we develop protocols and procedures,
based on the quality and amount of information collected and associated ass umption s, to estimate
realistic movement and life-history patterns of fish from otolith chemistry? Can we use nat ural or
applied otolith tags to study population dynamics in the sa me way that we would use other tags?
Campana (2005b) highlighted the applications and assumptions when using otolith chemistry to
discriminate among fish groups. An obvious assumption of the approach is that there are character-
istic and reproducible markers for each group. All possible groups contributing to the group mixture
should be characterized, although statistical techniques that identify uncharacterized groups can be
used. The marker also must remain stable over the interval between characterization and mixing.
Many researchers wish to go further and extract more information beyond short-term population
associations and use otolith chemistry to determine lifetime movements and life-history patterns. In
doing so, it is necessary to make a number of assumptions about chemical incorporation and inter-
pretation in addition to those already presented for mixed stock analysis. Determining movements
298
OTOUTH CHEMISTRY OF FISHES
of fish from otolith chemistry relies on combinations of different chemical signatures (hereafter
referred to as a ' tag') being incorporated in different environments. Using this information, we can
link groups of fish with similar tags through space (different locations and habitats) and time (differ-
ent seasons or years) to determine where and when fish moved. If desired, chemical signatures can
be examined across an otolith to provide natural tags for several different life-history stages. These
chemical profiles can then be related to different environments the fish has lived in; thus, move-
ment patterns of individuals and groups can be deduced. An important assumption is that changes
in environments experienced by fish are temporally matched by changes in associated chemical
incorporation in the otolith (Secor et al. 1995b, Elsdon & Gillanders 2006a).
Within the current literature, researchers have drawn conclusions about fish movement and
life-history behaviours from natural otolith chemical tags, but often using data of varying qual-
ity and quantity, and without stating the assumptions that are made when determining fish move-
ments using otolith chemistry. Given this confusion, we have highlighted five methods to determine
fish movement from otolith chemistry and their underlying assumptions. All of these methods can
describe fish movement and life history. However, the amount of data required and the number of
assumptions made differs among methods. Two of these methods make no assumptions about which
environmental parameters influence otolith composition, while three do.
The authors aim to clarify the methods of determining movement, and to a lesser degree vital
rates, based on otolith chemistry. First, current trends in determining movement using otolith chem-
istry, otolith sampling methods, and what influences otolith chemistry are reviewed and second,
both spatial and temporal variability in water and otolith chemistry that underpin the assumptions of
several methods. Third, five methods for determining movement and migration of fish are outlined:
(I) estimates of movement and life-history traits of a single fish group, (2) assessing connectivity
among groups using natural chemical tags in otoliths, (3) transgenerational marks to determine par-
entage and natal origins, (4) profile analysis to define life-history variation within a population, and
(5) profile analysis to describe movements through different environments, where group(s) refers to
all fish with a similar chemical tag. Within each of these methods, the authors provide background
information and state the specific hypotheses being tested and clarify which assumptions are made
and what limits the interpretability of each method . This should help researchers improve experi-
mental designs and methods of measurement, use proper statistical analyses, and develop more rig-
orous sets of inferences about fish movement and life histories. Last, research directions required to
fill current knowledge gaps and enhance the usefulness of otolith chemistry to determine fish move-
ment are outlined. The examples and discussions given have largely been based on a handful of
elements (e.g., strontium and barium) and isotopes (e.g., oxygen and strontium) for which adequate
data exist. Assumptions, inferences, and interpretations of the different methods are, however, the
same regardless of the chemicals being examined.
Otolith sampling methods

General methods of otolith preparation and analysis on a wide range of instruments (e.g., Laser
Ablation Inductively Coupled Plasma-Mass Spectrometry (LA ICP-MS), electron and nuclear
microprobes, synchrotron-based methods, micromilling for stable isotopes) can be found in the
existing literature (Campana et al. 1995, 1997, Sinclair et al. 1998, Radtke et al. 1999, Markwitz
et al. 2000, Limburg et al. 2007). Briefly, otoliths are dissected from fish and chemical signatures
are quantified after either dissolving whole otoliths or sectioning the otolith (Figure 1). Differences
in how instruments quantify these chemicals are not the focus of this review. What is of concern,
however, is the choice of instrumentation and type of analysis done as this will determine the spatial
resolution of chemical tags within the otolith matrix analysed and the resultant information on fish
movement. Otolith analyses can be divided into two broad types: those based on whole otoliths or
299
(A) Method of (B) Otolith (C) Data obtained

otolith analysis sampling
Whole otolith
.... Whole otolith

dissolved in acid and
analysed as a solution
.... One value per
element/ isotope, which
is an integrated tag
over the fish's life
Otolith sections Otolith sectioned

(e.g., through core)
and portions of otolith One value per
material sampled
.... .... element/isotope, per

otolith portion sampled,
which is a tag that
refl ects a specific life
period
Figure 1 Two methods of otolith sampling: whole and otolith sections (A, B) and the data obtained from
such methods (C).
those based on otolith sections (Figure 1). These two approaches can provide very different types of
information and each can be used successfully to answer different questions (as discussed in depth
in Campana 2005b).
The analysis of whole otoliths provides a tag that integrates chemical signatures across the
entire life of the fish, from embryonic stages to capture (Figure 1). Hence, sampling whole otoliths
provides a chemical tag of environments integrated over the fish's entire life, and can serve as a
mark of a particular group. Solution based analyses of whole otoliths are often more precise than
those obtained using probe based techniques (Campana 1999) and can, therefore, be the preferred
option in some applications (Campana et al. 1997, Secor et al. 2001). Whole otolith analyses are
particularly good for characterizing chemical tags of groups of fish, then subsequently tracking the
movement or mixture of those groups over short periods (Campana et al. 1995, 2000, Gillanders &
Kingsford 1996). Unique chemical tags in otoliths of groups of fish will remain distinct and iden-
tifiable for a period of time even if the groups move or mix , thereby accreting new otolith material
with new chemistry, provided this additional material is minimal. Statistical techniques then allow
the proportions of each group in a mixture of fish with unknown origins to be accurately estimated
(Campana 1999). Separation of the groups in the mixture ceases to be possible when the composition
of new material incorporated after the initial characterization of group signatures alters the chemi-
cal tag (Campana 2005b). Thus, whole-otolith chemical tags are unlikely to remain constant over
long periods of time, but are stable over shorter intervals of months, seasons, or occasionally years
(Kennedy et al. 1997, Campana et al. 2000, Elsdon & Gillanders 2003a, Campana 2005b). In some
instances, little otolith growth occurs during periods of mixing and therefore otolith chemical tags
can be used to determine life time migration behaviours (e.g., contingent structure, Secor 1999).
In contrast, chemical tags can be established for different life-history stages, such as larvae,
juveniles, and adults, when otoliths are sectioned and sampled on spatial scales that correspond to
300
OTOLITH CHEMISTRY OF FISHES
Method of analysis Data obtained
Otolith sections -one 12

analysis per otolith
One portion of otolith analysed, 8
so tag reflects a specific
life-history period.
c 4
.g
c
E
Q) focus /
•
outside
u
Otolith sections -profile c core edge
0
analyses across otoliths u
-;;;
u
Continuous "6
Q)
12
sampling ..c:
(i.e., laser)
u
8
Two or more portions of the same
otolith analysed, so tags represent 4
different life-history periods of
same fish.
focus/ outside
Discrete sampling core edge
(i.e., probe/ milling)
Position on otolith
Figure 2 Methods of sampling otolith sections for chemistry: one analysis per otolith, profile analysis across
otolith, and the data obtained from such methods.
the time periods of interest (Figure 2). Sampling along sections of the otolith can be accomplished
using a range of instruments that can determine chemical tags in otolith material at spatial scales
<I J..lm that can correspond to temporal scales of <l day (Markwitz et al. 2000). Analyzing sec-
tions of otoliths allows for the detection of small-scale chemical differences in otoliths that would
otherwise be averaged out using whole-otolith solution techniques (Fowler et al. 1995a,b, Elsdon &
Gillanders 2003a). Thus, for different life-history stages, we can determine unique chemical tags
that can be related to different fish groups or environments.
Chemical analyses of otolith sections can be divided into two categories: examination of a
single location within an otolith and examination of the chemical profile at two or more locations
across a sectioned otolith (Figure 2). In the former, chemistry is determined for a discrete portion
of otolith that can then be related to a specific life-history period. We have used the term profiles to
describe the analysis of two or more different locations along the otolith growth axis; this includes
the continuous quantification of chemicals across the otolith surface. X-ray fluorescence, Micro-
Proton Induced X-ray Emission (PIXE), electron microprobe, micromilling and mass spectrometry,
and LA ICP-MS methods can a ll produce profiles of chemical tags, which also have been referred to
a nd displayed as transects, trajectories, profiles, scans, chronologies, 2-dimensional maps, and line
sca ns in the literature. The aim of profile analyses is to relate changes in chemistry across otoliths
to fish movement.
What influences otolith tags

Information on otolith crystallization is beyond the scope of this review and was comprehensively
detailed by Campana (1999). Nevertheless, it is important to discriminate between chemicals that
are likely to be good indicators of environmental parameters of specific areas, such as water chem-
istry, temperature, and salinity, and those chemicals that are controlled by physiology. Chemicals
that are incorporated into the otolith via substitution for calcium (i.e., SrC03 ) (Bragg 1924) and
301
included in interstitial spaces (Wyckoff 1964, Faure & Powell 1972 , de Vries et al. 2005) are likely
to reflect environment parameters. Several element and isotope ratios (i.e., Sr:Ca, Ba:Ca, and Sr
and 0 isotopes) appear to reflect environmental parameters either linearly or non-linearly, and as
such they are ideal tracers for determining fish movement (Kennedy et al. 1997, Bath et al. 2000,
Limburg et al. 2003, Elsdon & Gillanders 2004, Dorval et al. 2007, Kerr et al. 2007). Elements that
are under physiological regulation or those that may leach out of otoliths, including N, K, Cl , Zn ,
and Cu, are less likely to reflect environmental parameters (Limburg unpublished data, Kalish 1989,
Proctor & Thresher 1998, Rooker et al. 2001 , Miller et al. 2006).
Several experiments have attempted to identify the sources of elements that are ultimately
deposited in otoliths (e.g., Hoff & Fuiman 1995, Farrell & Campana 1996). For example, 83% and
98% of Sr and Ba, respectively, in otoliths were derived from the surrounding water in marine
species (Walther & Thorrold 2006) and 88% of Sr was from the surrounding water in freshwater
species (Farrell & Campana 1996), with the remaining percentage assumed to be from dietary
intake. Similarly, dissolved inorganic carbon (DIC) typically contributes 70-80% to the carbon
deposited in otoliths, with the remaining 20-30% coming from metabolic sources (Kalish 1991 ,
Thorrold et al. l997a, Solomon et al. 2006). It should be noted that not all chemicals will act in simi-
lar manners, with chemicals such as strontium representing water chemistry, but sulphur isotopes
representing dietary sources.
Environmental processes affecting otolith composition have been reviewed by Campana (1999),
Secor & Rooker (2000), and more recently Elsdon and Gillanders (2003a). Relationships between
elements and environmental processes are often examined using element-to-ea ratios, as elements
can substitute for Cain CaC03 , and therefore elemental incorporation will be dependent on Ca con-
centration. For at least some element-to-ea and isotope ratios, otolith composition reflects ambient
water concentrations, albeit with varying degrees of mass discrimination (Brown & Harri s 1995,
Farrell & Campana 1996, Bath et al. 2000, Elsdon & Gillanders 2003b, Kraus & Secor 2004, Hobbs
et al. 2005, Dorval et al. 2007, Munro et al. 2008). For many elements, however, there is not a
clear or consistent relationship between water and otolith chemistry (e.g., Mg, Elsdon & Gillanders
2003b, Wells et al. 2003a, Dorval et al. 2007).
The effect of salinity on otolith chemistry requires careful consideration. Ions will follow a
mixing curve between two end-members defined by the element-to-Ca ratio (i.e., ambient Sr:Ca).
For instance, Sr:Ca ratios in fully marine environments (salinity= 35) are relatively constant, while
freshwater end-members show considerable geographic and temporal variability. In most systems,
freshwater Sr:Ca end-members are considerably lower than the global ocean end-member, and thi s
pattern explains why most studies have found a positive correlation between otolith Sr:Ca and salin-
ity (Secor & Rooker 2000). In some systems, however, the freshwater Sr:Ca end-members exceed
the marine end-member, leading to a negative correlation between otolith Sr:Ca and salinity (Kraus
& Secor 2004, Limburg & Siegel 2006). Underlying differences in water chemistry may therefore
explain the various positive, negative, and no effects of salinity on otolith Sr reported in the litera-
ture (Fowler et al. 1995b, Hoff & Fuiman !995, Chesney et al. 1998, Elsdon & Gill a nde rs 2002,
2004, Martinet al. 2004, Martin & Thorrold 2005, Dorval et al. 2007) and points to the importance
of critically evaluating water chemistry when studying systems. Salinity effects that are indepen-
dent of Sr:Ca water concentrations (e.g., due to osmoregulation) have rarely been studied (K raus &
Secor 2004, Zimmerman 2005), but do show some effects (partition coefficients calculated from
Elsdon & Gillanders 2004 and published in Martinet al. 2004).
Temperature, independent of its relationship to growth rate, can affect the assimilation of some
elements into otoliths. Temperature generally has a positive influence on otolith Sr:Ca (Bath et al.
2000, Elsdon & Gillanders 2002, Martin et al. 2004). The effects temperature has on Ba, Mn ,
and Mg are varied, with studies detecting positive, negative, and no effects. These differences are,
however, based on only a few experiments (Fowler et al. 1995a,b, Hoff & Fuiman 1995, Elsdon &
302
Gillanders 2002, Martin & Thorrold 2005). The influence of temperature on otolith chemistry is
Iikely to be due to both physiology (Townsend et al. 1992) and kinetic processes (i.e., temperature
affecting crystallography, Niel son & Christoffersen 1982).
Interactions between environmental variables can occur when changes in one variable (e.g.,
salinity) affect the way another variable (e.g., temperature) influences otolith chemistry. Several
experiments have documented interactions among environmental variables (Secor et al. 1995b,
Elsdon & Gillanders 2002 , 2004, Martin & Thorrold 2005). Additional care is therefore required
when linking changes in otolith chemistry to water chemistry variations in environments, such as
estuaries, where more than one variable can differ.
Variation in water and otolith chemistry

Determining movements of fish based on otolith chemistry is often reliant on knowing the spatial
and temporal extent of chemical variation in ambient water and otolith chemistry. Where groups of
fish have distinctly different tags in space and time, then connectivity of individuals among those
groups can be distinguished without information about water chemistry. Some knowledge of the
variation in water chemistry can, nonetheless, aid in evaluating the reliability of natural tags over
years and generations. Moreover, using otolith profile analyses to determine movements of fish
through different environments relies on knowledge of spatial and temporal differences of water
chemistry of those environments. For methods of determining variation in water and otolith chem-
istry, see 'Detecting variability at different spatial and temporal scales' (p. 321).
Water chemistry
It is important to recognize that water chemistry is likely to vary in space and/or time as chemical
concentrations are affected by mixing of water masses, ion exchange between sediments and water,
complexation, precipitation, and adsorption (Wilson 1975, Aston 1978, Figures 3 and 4). In inland
waters, hydrologic processes, including groundwater transport and retention , play important roles in
chemical availability. Together with hydrology and microbial processes, the extent and heterogene-
ity of parent material (bedrock, soils) determine the availability of elements and isotopes. Although
isotopic signatures, such as Sr and 0 isotopes, are commonly viewed as being reliably stable, these
a lso may differ, especially if water masses of different composition mix , or there are changes in
water vapour sources of precipitation or groundwater flow (Fairbanks 1982, Rohling & Bigg 1998).
Importa ntly, correlations between water chemistry and other environmental factors, such as salin-
ity, should not be assumed to be constant.
Spatial differences in water chemistry have often been derived via predictive relationships
between chemicals and salinity, where actual chemical concentrations are not measured. For exam-
ple, a common viewpoint is that water Sr is positively and Ba negatively correlated to salinity.
However, many freshwater locations have water Sr:Ca ratios greater than that of seawater (Limburg
1995, Wells et al. 2003a, Kraus & Secor 2004), and ambient Ba levels can be linked to particulate
sediments (Li & Chan 1979). It is therefore important to assess spatial patterns in water chemistry
both within and among locations (e.g., rivers, estuaries, and reefs). Although published studies on
spatial scales of water chemistry (e.g., Ca, Sr, Ba) variability are limited (see Table I for a review;
Figures 3 and 4), significant variation in water chemistry has been detected at spatial scales ranging
from tens of metres to hundreds of kilometres (Figures 3 and 4). Variation in ambient water chemis-
try is likely to be system dependent, based on tides, water movements, hydrogeology, precipitation,
and upwelling (Figure 4), but geographic separation does not guarantee useful differences in water
chemistry among locations. There is clearly a need to understand variation in water chemistry in
specific systems to aid interpretations of fish movement through environments.
303
Strontium Barium
so·
c: so·
E
::l
:;
s 48°
-;; 48°
u.
Sr concentration (fall and winter) .,,_ __,_

75 50 (fall) 50 (winter)
so·
so·
...
c"'
ｾ＠
48°
48°
460 460
64° 60° 56° 64° 62° 60° w
Figure 3 (See also Colour Figure 3 in the insert following p. 250.) Variation in dissolved strontium and
barium concentrations in the Gulf of St. Lawrence, Canada, showing spatial variation (within each plot) and
temporal variation between seasons for strontium , comparing fall (A) with winter (B); barium, comparin g fall
(C) with winter (D). Values in parts per million . (S.E. Campana unpublished data.)
Water chemistry at any site typically varies over time (Figure 3). Some knowledge of temporal
variation in water chemistry is particularly important if fish movements are to be related to habitats
over time. Sampling of temporal variability is generally done by taking replicate samples at fixed
time intervals (Surge & Lohmann 2002), and those samples are assumed to represent areas and
times beyond the point of sample collection. Two studies have shown little variation in Mg, Mn , Ca,
Sr, and Ba from estuarine waters over monthly and seasonal scales (Dorval & Jones 2005, Elsdon
& Gillanders 2006b) (Table 1). However, water chemistry in dynamic environments with large
tidal ranges may vary over seasonal (Figure 3) and shorter timescales (days, tidal cycles, Elsdon &
Gillanders 2006b). For example, large differences between samples collected on different days have
been detected for Ca, Mn, Sr and Ba within three small (<10 km) tidal estuaries, where variation on
scales of days accounted for up to 64% of the total variation of scales of days, weeks, months, and
seasons (e.g., Ca, Ba, Elsdon & Gillanders 2006b). Similarly, water samples collected 1-2 h apart
from a single site can have differences in Mn concentration as large as 3.3x (average 1.73x from
85 paired samples), with an average difference of 29.48 Jlg 1- 1 (average sample 46.42 Jlg J- 1) (United
States Geological Survey data, Hackensack River, New Jersey). Oxygen isotopes in freshwater sys-
tems are responsive to floods and droughts and may change over seasons and years (Fairbanks
304
Figure 4 (See also Colour Figure 4 in the insert.) (A) Sea surface temperatures (SSTs) collected during the
upwelling season along central California (5- 19 June 2006; National Oceanic and Atmospheric Administration
Coast Watch program) and representing (B) the Ba:Ca ratios (J..lmol mol - 1) and (C) Sr:Ca ratios (mmol moJ - 1)
collected during the same upwelling season (B. Wells & K. Stierhoff unpublished data, figure prepared by
K. Stierhoff). White arrows represent regions of active upwelling and the black arrow represents infusion of
saline, warmer waters from farther off shore into the region. Note: Variability in Ba:Ca is derived largely from
the distribution of upwelling in the region and will vary with the degree and timing of upwelling.
1982, Kerr et al. 2007). Thus, to detect and interpret temporal variation within estuaries it is useful
to examine a range of temporal scales and ideally these should be nested (see 'Detecting variability
at different spatial and temporal scales'). An appropriate experimental design is not necessarily an
expensive process and can lead to a greater understanding of the systems in which we work.
Otolith chemistry
Otolith chemistry of individuals or groups of fish living in different environments may differ if they
reside in environments long enough to incorporate a detectable chemical tag. Detailed reviews of
spatial and temporal variation in otolith chemistry exist elsewhere (Gi Ilanders et al. 200 l, Gillanders
2002a), and therefore we present only a brief synopsis of these and more current literature.
305
Table 1 Summary of publi shed and unpubli shed data that examined spatial and temporal scales of variation in ambient chemistry that are
potenti ally useful to investigate movements of fish (organized from smallest to largest scales)
Location of Chemicals
Sampling design Scale of investigation study analysed Differences Source
Spatial scale investigations

I estuary, 8 locati ons 1- 20 km East coast, Mn (also Cd, Significant difference among stati ons Hatje et al. (2003)
Au stralia Ni , Cu, Zn)
5 estuarine habit at ' locati ons', 5-90 km East coast, USA Sr, Ba, Mn , Analysed by ' habitats '; significant differences for Dorval & Jones
6 sites per locati on Mg Sr, Ba, Mn , Mn among habitats (2005)
I bay (San Francisco Bay), 5- 140 km West coast, Mn Significant differences on scale of sites, with sites Roitz et al. (2002)
24 si tes dispersed thro ugh USA grouping out spati ally, observed from spatial
bay mapping -3
;:o
ｾ＠
2 estuaries, 2 locati ons in each I 0---480 km East coast, Sr, Ba, Mn, No significant differences for Sr, Mg, Li : Gillanders
Australia Mg, Li significant differences for Ba, Mg among sites (unpubli shed data) (/j
4 locat ions (3 bays and open 10-760 km Sout h-east Ca, Sr, Ba, Analysed by locations; significant differences for Ha mer et al. (2006) sn
w
coastal), 4- 10 sites per coast, Austra li a Mn , Mg all among locations, I bay different from other m
0 locat ion locat ions
r
C/l
0\
I river, 2 tributaries 20 km East coast, USA Ca, Sr, Ba, Significant differences for Ca, Sr, Mg ; no Walther & Thorrold 0
0
Mn , Mg signi ficant differences for Ba, Mn (unpubli shed data) z
12 rivers, I location per river 20- 900 km East coast of Ca, Sr, Ba, Significant differences for locations for all Walther & Thorrold m
-3
USA and Mn , Mg chemicals (unpubli shed data) ;J>
Canada r-'
36 rivers 60 km Idaho, USA Ca, Sr, Ba, Mg Significant differences between location s Wells et al. (2003a)
Temporal Scale Investigations

Within years
I river, I location 85 co ll ections, paired East coast, USA Mn Significant differences among samp les collected 'USGS NW IS data
samples collected 1-2 hours apart, average difference x 1.73; (http://waterdata.
h apart observations of means usgs.gov/nwi s)
2 estuaries , I location per 2 coll ections over 2 tides South coast, Ca, Sr, Ba, Mn Sign ificant differences among tides for Ca, Sr, Ba, Elsdon & Gil landers
estuary Australia Mn at one location (2006b)
I estuarine location 3 nested scales of tidal East coast, Mn (also AI, Significant differences among hours for Mn ; no Hatje (2003)
cycles, 3 tidal stage Australia Fe, Cu, Cr, significant differences for tidal cycle or tidal stage
(flood, slack, ebb) , 4 h Pb, Zn)
I bay location Roughly weekly Antarctica Mn Significant differences among times- Grotti et al. (200 I)
sam piing over I00 days observations from table in paper
3 estuaries. I location per 16 collections on nested South coast , Ca, Sr, Ba, Mn Significant differences among seasons for Sr Elsdon & Gillanders
estuary scale of 2 seasons, 2 Australia (3 estuaries) and Mn (I estuary); no significant (2006b)
months, 2 wk, 2 days differences for months; significant differences
among weeks for Ca, Sr, Mn (2 estuaries);
significant differences among days for Ca, Sr, Ba
(3 estuaries}, Mn (2 estuaries)
5 estuarine habitat 'locations', 6 collections, 2 per East coast, USA Sr, Ba, Mn, Significant differences for Sr among months; no Dorval & Jones
6 sites per location month for 3 months Mg significant differences for Ba, Mn, Mg among (2005)
months
3 seasons (summer, East coast, Mn (also Cd, Significant differences among seasons for Mn Hatje et al. (2003)
0
....,
I estuary, 8 locations
winter, summer) Australia Ni , Cu, Zn) 0
r
I bay (San Francisco Bay}, 3 seasons (winter, West coast, USA Mn Significant differences among times at individual Roitz et al. (2002) =i
24 sites dispersed through summer, spring) sites, observed from table :r:
bay n
:r:
16 rivers Single collections from Idaho. USA Ca, Sr, Mg No significant differences detected Wells et al. (2003a) m
'-' each river compared 3::
0
-.1
between two seasons
Vi
....,
6 rivers One collection during Idaho, USA Ca, Sr, Mg Variation between seasons was not significant Wells et al. (2003a)
;:o
-<
summer flow compared 0
'T]
to fall flow collections
'T]
Vi
Among years :r:
2 locations (bay and coastal) 4 collections on nested South-east Ca, Sr, Ba, Analysed as 'time' differences ; significant Hamer et al. (2006) m
C/J
scales of 2 seasons coast, Australia Mn,Mg differences inCa, Sr, Mn , Mg; no significant
within 2 yr difference in Ba
9 estuaries 4 collections on nested East coast, Sr, Ba, Mn, No sign ificant differences for Sr (time or estuary); Gillanders
scale of 2 yr, 2 months Australia Mg,Li significant differences in Ba, Mn with estuary and (unpubli shed data)
within years month (year); significant differences for Mg
bet ween years
>25 locations from Lake Single collections in New York, USA Ca, Sr, Na, Ba, Element:Ca ratios geographically consistent Limburg & Siegel
Ontario to the Hudson River synoptic surveys. 2 yr Mn bet ween a very wet and very dry year (2006)
mesohaline estuary running
" United States Geological Survey National Water Information System (USGS NWIS)
Spatial variation in otolith tags has been investigated in at least 30 papers (Gillanders et al. 2001).
Studies have typically assessed differences in otolith chemistry in several locations along extensive
coastlines (>1000 km) (Campana et al. 1994, Edmonds et al. 1999). Several studies have, however,
examined more than one spatial scale using a nested design by sampling fish at replicate sites (scales
of hundreds of metres to kilometres) within several locations separated by at least lO km (Thorrold
et al. l997b, Campana 1999, Gillanders et al. 2001, Patterson et al. 2004). Spatial discreteness of oto-
lith tags has been detected for sites separated by as little as several metres (Gillanders & Kingsford
2000, Kingsford & Gillanders 2000, Wells et al. 2003a) and for locations over broader spatia l scales
(up to 1200 km; Secor & Zdanowicz 1998, Thorrold et al. 1998, Campana 1999). Other studies have
found no differences in chemical tags among locations separated by as much as 3000 km (Proctor
et al. 1995, Kalish et al. 1996). The distinctiveness of otolith chemical tags among groups is likely
to depend on (l) individuals occupying environments with sufficiently different physico-chemical
properties, (2) the amount of time fish spend in an environment before being captured , and (3) the
selection of elements and isotopes to be assayed. Distance among locations is not a good predictor of
the magnitude of difference in otolith chemistry as otolith chemistry will reflect differences in envi-
ronmental properties and the scales at which these vary (see previous section, 'Water chemistry').
Temporal differences in otolith chemistry have been investigated in at least 15 publications (see
Gillanders 2002a). The majority of papers have investigated otolith tag differences on either annual
(Campana et al. 2000, Rooker et al. 2001, Dorval & Jones 2005, Kerr et al. 2007, Walther et al.
2008) or monthly scales (Hamer et al. 2003) to assess the stability of tags from locations among
different annual cohorts. If tags are stable among years, then matching unknown chemical tags to
known tags from specific cohorts to determine connectivity is not necessary. Unfortunately, this is
rarely the case (Milton et al. 1997, Rooker et al. 2001, Gillanders 2002a, Hamer et al. 2003 , Dorval
& Jones 2005). A general finding among published papers was that otolith tags showed signifi-
cant interannual variation. Temporal variability of otolith tags therefore likely reflects differences
in temperature, salinity, and water chemistry (Figures 3 and 4). Sampling fish using appropriate
designs (i.e., a nested design that incorporates temporal and spatial aspects of the system) that also
accommodates for variation in fish growth rates by sampling the population in a representative
fashion can go a long way to identifying sources of variation.
Methods for determining movements

and life-history measurements
In the following section we refer to a ' population' of fish as all fish of the same species within
an area of interest that have the potential to mix (as opposed to a reproductive population), and a
'group' refers to fish with similar otolith tags within a population . We refer to 'location' as an area
that groups of fish inhabit and 'region' as the area inhabited by a population and containing more
than one location (see 'Glossary ' ).
Method 1: Estimates of movement and life-history traits

of a single fish group
Background
In this method, we aim to determine movement and life-history traits , including survival , mixing
rates, and recruitment, within a single group of fish. For estimates of movement and life-history traits
of more than one group of fish see Method 2. The method is based on establishing baseline chemi-
cal tags (natural or applied) for fish groups of interest. This method only requires that the group of
308
interest possesses a tag that is unique from a ll other groups . Fish of unknown group membership are
then assigned to the group using chemical tags in otoliths. Otolith chemistry can be quantified using
solution techniques or by sampling sectioned otoliths (Figure 1). The analysis of whole otoliths is
particul arly relevant to this method if a group of fish has been segregated long enough to possess a
unique tag, and these fish subsequently mix with other groups (Campana 1999, 2005b).
For natural tags, it is important to identify all group tags to evaluate the uniqueness of the
group being examined. Deliberately applied otolith chemical tags can be generated by spiking rear-
ing water with unnaturally high level s of a common element (e.g., Sr, Brown & Harris 1995), an
element typically in low concentrations (e.g., lanthanides, Ennevor & Beames 1993), a fluorescent
bone-seeking chemical (e.g., tetracycline, Jones et al. 1999), or an unnatural isotopic ratio of a com-
mon element (e.g., Ba, Thorrold et al. 2006). The key to artificially applied tags is that the tag is
substantially different from that which would occur naturally.
To use otolith tags to address questions of mortality, movement, mixing rates, and recruitment
the basic assumptions of mark-recovery studies should be met. Specifically, Brownie et al. (1978)
and Schwarz & Amason (1990) identified up to eight assumptions that must be met, or compensated
for, to use tags to their full potential. These assumptions are relevant to all methods. We discuss
each of these assumptions relative to natural and applied tags (see Table 2).
Table 2 The five methods of determining fish movements based on otolith chemistry
and the assumptions that are made for each method
Method
Ass umpti on I' 2 3 4 5

I . Marked sample is representative of the target group, and o nly the target group X X X X X
2. Age of indi vidual s is correctly identified X X X X X
3. There is no tag loss X X X X X
4. Survival rates are not affected by the ha ndlin g or tagg in g itself X X X X X
5. The period of recovery is correctly identified X X X X X
6. Taggin g does no t a lter fish behaviour X X X X X
7. The fate of a give n tag is random X X X X X
8. All tagged individuals of an identifiable class in the sampl e have the same recovery rates X X X X X
9. Segregation of indi vid ual s to incorporate unique tags X X X X
10. Growth differences among gro ups of fish are quantified X X X X
II . Similar met hods are used to detect tags X X X X
12. The mate rnal tag source is identified X
13. Estimatin g tag rete ntion in the mother and period o f tag transmi ss io n X
14. Otolith chemi stry of individuals within groups ca n be differentiated into identifiabl e X
contin gents
15. Samp lin g of fish and the ir profil es is representative of all profiles that exist X
16. Independence of sampling alo ng a profile X X
17. Oto li th che mistry changes predictably wit h envi ronme ntal parameters X X
18. Interact ive effect of environmental parameters on oto lith che micals are known X
19. Ontogenetic e ffects o n otolith chemistry are known ( if reco nstructions bridge different X
life-hi sto ry periods)
20. Spatial and te mporal variation in environmental parameters are quantified X
21. Correlations between otolith crystallization and chemistry are known X
' The summary does not di stin gui sh between natural tags and applied tags ; see Method I in text for further detail s.
309
Hypotheses and assumptions

If one group possesses a tag that is distinctly different from all other tags, then that tag can be used
to trace fish that move among groups.
Assumption 1: Marked sample is representative of the target group, and only the target group
In any study it is critical that the sample fish are representative of the group for which inferences
are to be made.
Natural tag There are two concerns related to natural tags. First, it is possible that the natura l mark
occurs on only a subset of fish from a group if, for instance, individual s used to determine baseline
signatures are from a small, but environmentally distinct habitat within a location. Therefore, fish
should be sampled from multiple areas to ensure the signature is characteristic of the whole group
and not only a subset. Second, it is possible that the sampled natural tag represents multiple groups
that are not of interest. It is critical that the natural tag from an identified group be compared to
all possible other groups to ensure it only characterizes the group of interest. This second concern
cannot be addressed with statistical techniques used to identify uncharacterized groups as unchar-
acterized groups may have different tags. Determining the direction of fish movement among these
groups becomes impossible if two geographically isolated groups have the same tag. Thus, if during
the course of sampling, it is determined that two or more groups of fish possess the same tag, then
the spatial or temporal resolution of the hypothesis requires alteration . Ultimately, the hope is that
among-group variation exceeds within-group variation, thus providing discrete spatial and temporal
resolution of group tags.
In addition to sampling the spatial extent of group tags it is important to quantify the degree of
temporal variation in tags to match the scale of the question being addressed. One typical method
is to collect otolith tags from each group throughout their residency in a particular location . If
individuals leave a habitat or location over time (e.g., salmon emigration from a natal watershed),
then sampling must occur before fish start to leave. On a longer time frame, studies have shown
that location-specific tags often vary interannually. Therefore, baseline tags must be quantified for
each cohort of interest unless chemical tags remain the same over time (see 'Variation in water and
otolith chemistry' ).
Applied tag Typically, in applied marking studies an appropriately chosen subsample of fish is
marked (e.g., tagging on spawning grounds, in the hatchery), and the tag cannot be confused with
natural groups.
Assumption 2: Age of individuals is correctly identified

If the age of a fish is incorrectly identified and the elemental tag of that group varies over time, then
the tag in the recovered fish may be classified incorrectly.
Natural tag It is critical to know the age of unknown fish so that we can correctly identify indi-
viduals to specific groups using the appropriate baseline data (see, for example, Gillanders 2002b).
Age is also critical for the estimation of cohort- and age-specific rate estimation and can commonly
be obtained from otoliths.
Applied tag To estimate cohort- and sex-specific rates of a group with an applied tag it is impor-
. tant to know the age of the tagged fish and use a tag specific to that age group, so that we can cor-
rectly identify fish to specific groups using their otolith tags.
Assumption 3: There is no tag loss

Otoliths are considered chemically inert such that, once material is accreted, it is not reworked .
Although this may be true for ions substituting for Cain the aragonite structure, elements that are
310
weakly bound in interstitial spaces of the otolith may leach out during storage (e.g., Zn, Limburg
unpublished observations). Tag loss or alteration may also occur from the method of preservation
(Milton & Chenery 1998, Proctor & Thresher 1998, but see Campana et al. 2000). Some elements
are more affected than others, depending on where they are incorporated in otoliths, and caution
should be taken to determine if there are preservation effects on elements or isotopes of interest, or
alternatively the same methods can be used for all fish. Delayed removal of otoliths may also affect
their integrity. For example, freezing of brown trout (Salmo trutta trutta, Linnaeus, 1783) heads
resulted in partial erosion of otoliths, possibly due to contact with acids in the braincase (Limburg
unpublished observations). The eroded otoliths showed differential accumulations of Sr and Zn that
were likely due to post-mortem transport of the elements. Tag loss due to the methods of preserva-
tion may be reduced or eliminated by using consistent methods of otolith extraction and storage for
all fish or by using elements or isotopes not subject to preservation effects. Extraction methods have
included ultraclean procedures for otolith removal and storage or rigorous decontamination proce-
dures following extraction and storage (e.g., Thresher 1999, Secor et al. 2001).
Tag loss can occur due to the method of chemical sampling. If the original chemical tag is iden-
tified on a sectioned otolith at a defined spot (e.g., the core) using a probe-based assay, then otoliths
from fish sampled subsequently must be analysed using the same analytical approach and the same
region (Gillanders 2002b) (also see Method 2, Assumption 11). Different principles apply to the
analysis of whole otoliths, for which the tag represents the entire lifetime of the fish up until the time
of capture. Any otolith growth subsequent to that point has the potential to change the tag because
new material will be added, which may have different chemistry. Therefore, it is important that the
use of whole-otolith tags be restricted to relatively short periods of time after otoliths are taken for
tag characterization, during which the whole-otolith composition does not change appreciably due
to subsequent growth (e.g., otolith weight does not increase by more than 5%, Campana et al. 1995).
Thus, a spatially restricted otolith sampling procedure, such as laser ablation, microprobe or milling
small portions of otoliths, offers a reliable methodology for reducing tag alteration if subsequent
otolith growth is an issue.
Assumption 4: Survival rates are not affected by the handling or tagging itself
Natural tag The otoliths of all members of the population are tagged naturally in situ; therefore,
this assumption is typically not violated.
Applied tag Handling and tagging of fish may cause immediate or delayed mortality. Violation of
this assumption, wherein tagged fish have higher mortality than non-tagged fish, would lead to an
underestimation of mortality rates and incorrect interpretation of fish movement. Unfortunately, the
effects of long-term survival rates due to chemical tagging are largely unknown, although studies of
fluorescent tags do exist (e.g., Tsukamoto et al. 1989).
Assumption 5: The period of recovery is correctly identified

The time between tagging and recovery (fish collection) should be correctly identified, so that life-
history measurements, which are intrinsically time related, can be estimated correctly. Hence,
estimates of recovery periods are necessary to determine movement rates or survival based on
appropriate cohort tags.
Assumption 6: Tagging does not alter fish behaviour

If tagged fish associate with themselves more than with untagged fish of the same population there
will be overdispersion of the data (observed variance is greater that the theoretical variance of the
model) and migration and life-history measurements will be biased.
311
Natural tag Natural tags are not affected by the action of the study, so this assumption does not
apply.
Applied tag Applying a tag may result in changes in behaviour and associations among fish, such
as schooling and migration (McKinnell et al. 1997, Hay & McKinnell 2002), and tagged fish may
not mix with untagged fish , for example if fish are tagged in a school of similar size or age. Thus, it
is important to consider and, if possible, correct for behavioural effects of tagging.
Assumption 7: The fate of a given tag is random
Natural tags This assumption simply implies that the likelihood of collecting a tag, and therefore
an individual fish, is random between collection periods. We see no reason why natural chemi-
cal tags in fish would violate this assumption , unless there is a delayed or cumulative reaction to
elemental exposure or for some reason fish from different tag groups associate differently compared
to others.
Applied tags For applied tags, any alteration in behaviour, such as clustering of tagged fish, and
associations among fish (previous assumption) are likely to affect the collection of a tag.
Assumption 8: All tagged individuals of an identifiable class in the sample have the same recov-
ery rates
Natural tags In terms of sampling, all individuals must be collected by the same sampling gear
with the same catchability and effort (C.M. Jones personal communication). Sample sizes should
not be fixed, but rather reflect differences in population densities in most cases.
Applied tags For applied tags, the recovery rates are usually taken as a nuisance parameter and
not investigated further. There may, however, be concern if the distribution and mixing rate of the
fish are size dependent as opposed to age specific, which may occur when applied tags affect fish
growth. This is important for mortality and production estimation and for inferring movements of
a whole group.
Limita(ions and inferences

Using natural chemical tags as a mark-recovery tool provides a means to reliably 'mark' many more
fish than conventional applied tags at zero cost. However, the development of appropriate statisti-
cal models to interpret recoveries quantitatively is in its preliminary stages (C.M. Jones personal
communication). This method, however, holds much promise if all of the relevant assumptions are
addressed since inferences about movement and life-history measurements can be quite powerful.
In the meantime, the advantage of applied tags, such as altering otolith chemistry, is that normal
mark-recapture procedures can be followed and quantitative estimates developed for movement
and survival using well-known statistical techniques. By addressing assumptions, otolith tags can
answer the same range of questions as traditional tag-recovery studies (e.g., mortality, relative con-
tribution of tagged groups, and distribution).
The most important difference between measuring movement and survival by use of natural
and applied otolith tags is that for natural tags it is necessary to determine the number of tagged
fish within a group through an independent survey (C.M. Jones personal communication). To infer
population-level movements of fish among groups it is important to recognize that estimates of the
number of fish marked, the survivorship of fish in different groups, and the recovery rates of groups
are needed. With estimates of these values, mark-recovery calculations from natural tags can be
used to estimate true population movements (e.g., estuary X contributes 80% of the recruits to the
312
population) (C.M. Jones personal communication). Without group-specific estimates of survivor-

ship, descriptions of movement can be reported as relative rates given the representative sampling
done, as have been previously published (Thorrold et al. 1998, Gillanders 2002b).
Example: Applied elemental tagging fish in early life

Ennevor and Beames (1993) demonstrated that lanthanide elements could be used to mark the oto-
liths of coho salmon fry (Oncorhynchus kisutch, Walbaum 1792). Likewise, Schroder et al. (1995)
used artificially elevated strontium concentrations to mark chum and sockeye salmon fry with suc-
cess. Swearer et al. ( 1999) and Jones et al. ( 1999) present two examples of applying these techniques
in which the degree of self-recruitment of reef fish was determined by natural (Swearer et al. 1999)
and applied (Jones et al. 1999, 2005) tags. Jones et al. (1999) applied otolith tags to a known portion
of damselfish (Pomacentrus amboinensis, Bleeker 1868) embryos at Lizard Island (Great Barrier
Reef) that were later identified in recruited juveniles. With knowledge of the proportion of embryos
marked and the proportion of juveniles with the applied tag, Jones et al. (1999) determined that as
many as 60% of the damsel fish that recruited to the region were from local sources as opposed to
the products of long-distance dispersal.
Method 2: Assessing connectivity among groups

using natural chemical tags in otoliths
Background
Method 2 extends the previous section in that more than one group of fish is marked and, in sub-
sequent sampling, each group is recovered (Table 2). From this information, the contribution of
different groups to a mixed population is determined. Here we examine a specific case in which
the researcher uses natural chemical signatures in otoliths to describe connectivity of individuals
and groups in an effort to evaluate group mixing, movements among groups, and natal homing. We
discuss only natural tags in otoliths, as they are the more complicated extension of traditional mark
recovery, but the method could be easily extended to using different applied chemical tags (e.g.,
Munro et al. in press). We do not discuss issues related to describing mortality and productivity as
they follow the same assumptions as the previous methodology and are applied to multiple popula-
tions simultaneously.
Hypoth eses and assumptions

Otolith chemical tags can be used to estimate connectivity among groups if groups possess dis-
tinctly different chemical tags and those groups subsequently mix.
Assumptions for Method I should be addressed (Table 2), in addition to:
Assumption 9: Segregation of individual groups to incorporate unique tags

All groups of fish must be chemically distinguishable from one another, or estimates of movement
among groups are not possible. Logically, this implies that groups have been segregated in different
locations (or habitats) during the same life-history stages, or at least at some life-history stage in the
case of whole-otolith tags. Furthermore, it is assumed that enough otolith material is incorporated
during the time period when the groups were segregated so that these differences can be detected
(see also Assumption 3 for statistical tag loss, if fish have only a small portion of their otolith tagged
from one location). If groups cannot be distinguished, then all fish with similar tags should be
treated as a single group in any analyses.
313
Assumption IO: Growth differences among groups offish are quantified

Differences in growth rates are not important for establishing tag differences; however, they do
become important if recaptured fish from different groups have had different growth rates and
whole otoliths are analysed. Therefore, it is important that fish size and age within each group are
known , and where possible, fish of similar size and age are collected between regions (Thorrold
et al. 1998, Wells et al. 2003b). If there is a substantial difference in growth between groups of
fish it may be necessary to account for such differences. Growth differences among groups can be
used as a covariate in order to determine if correlations between otolith tags and growth occurred
(Gil landers et al. 2001).
Assumption II: Similar methods are used to detect tags

Similar methods of chemical analyses should be used to estimate tags in all groups; otherwise
variation in analytical methods can lead to false identification of group-specific tags (Campana
et al. 1997). Thus, the same region of the otolith must be sampled for all groups of fish. We also
recommend that the same analytical protocol (instruments, standards, etc.) is used for all groups,
as different methods may result in different estimates of chemical concentrations (Gunn et al. 1992,
Campana et al. 1997, Secor et al. 2002, Elsdon & Gil landers 2003a, Ludsin et al. 2006). It is, how-
ever, possible to use different analytical techniques between the assessment of the baseline and
unclassified dataset, so long as they can be standardized and compared. For instance, Thorrold et al.
(1998) examined baseline variation in juvenile weakfish (Cynoscion rega lis, Bloch and Schneider
1801) using solution-based ICP-MS of otoliths from major groups of weakfish along the Atlantic
coast. Adults collected from the mixed population were, however, examined using laser-ablation
ICP-MS to analyse the otolith region formed during the juvenile period (that period examined using
solution-based techniques earlier) (Thorrold et al. 2001). The data were normalized so that relative
differences in location-specific tags were not affected by sampling method.
Limitations and inferences

If all groups are not included in the baseline dataset, errors may be made when estimating the
mixed-stock composition (Campana et al. 2000, Gillanders 2005). Specifically, if a group is not
included in the baseline dataset, but recovered subsequently, it may be misclassified to another
known group, depending on how distinctive its tag is and on the statistical test used (Gillanders
2005). Methods to deal with undescribed groups as a contributor to the mixed population do exist
(Smouse et al. 1990, Pritchard et al. 2000). Excluding or consolidating groups that make up a small
proportion of the mixed population (e.g., a given river mouth from a larger estuary, Thorrold et al.
1998) may improve the estimates of group proportions in the mixed population (Fabrizio 2005).
The identification of multiple group tags to assess connectivity is a powerful technique. The
analysis of connectivity can also be used to describe the proportion of a population that results from
self-recruitment. In addition to addressing assumptions of Method I and those outlined in this sec-
tion , it is important to recognize the limitation of inferring connectivity and self-recruitment if only
a subset of groups from the entire population is identified . If only subsets of groups are examined
then it is important that there are no substantial overlaps in tags among groups, which could bias
estimates. It is difficult to assess if this has occurred unless all groups are sampled, which requires
adequate fish sampling (see ' Variation in water and otolith chemistry'). Conversely, if a number of
groups have unique tags that are not represented by other groups, then connectivity of a subset of the
population can be assessed. Again, to infer connectivity as a proportion of the actual population it is
necessary to determine the relative number of tagged fish within groups (Jones et al. 1999), and the
survivorship of fish within particular groups or locations, so that mark-recapture calculations using
natural tags can be done (C.M. Jones personal communication).
314
Water chemistry information is not needed to evaluate connectivity. Nevertheless, an initial

examination of water chemistry across the land or seascape may provide useful information on
potential variability in otolith signatures (Wells et al. 2003a, Limburg & Siegel 2006). Dorval &
Jones (2005), Dorval et al. (2007) and Elsdon & Gil landers (2006b) demonstrate examples of using
nested designs to determine variability in water chemistry. See also 'Detecting variability at differ-
ent spatial and temporal scales'.
Example: Mixed composition and natal homing of weakfish along the Atlantic coast
Thorrold et al. (2001) described connectivity among groups of weakfish spawning in estuaries along
the Atlantic coast of the United States using natural otolith tags. Baseline elemental signatures of
young-of-the-year juveniles were quantified from five major groups along the Atlantic coast using
a nested design within each of the five estuarine systems. Fish were collected from the same five
areas during the spawning season 2 yr later, and the degree of connectivity between source regions
on spawning grounds as well as natal homing was described on a cohort-specific basis. A further
step of determining the actual connectivity in a population, as opposed to describing the propor-
tion of self-recruitment from the sampled fish , would require estimates of the number of fish pos-
sessing each of the different tags (C.M. Jones personal communication). See also Campana (1999)
and Campana et al. (2000) for estimating connectivity between spawning groups and Gillanders
(2002b) for estimating connectivity between juvenile and adult fish.
Method 3: Transgenerational marks to determine

parentage and natal origins
Background
Otolith transgenerational marking refers to the incorporation of a tag from the mother to the egg
that is subsequently incorporated into the otolith primordia of the progeny. Several research ques-
tions can be addressed using transgenerational marks, such as estimating self-recruitment, indi-
vidual and group fitness, and natal origin if, for example, one evaluates stock mixing when both
diadromous and non-diadromous forms contribute to a group. These techniques are an extension of
Method 2 (Table 2).
The approach is based on the observation that oocyte chemistry reflects that of the mother at
least up to the point after fertilization when the chorion (the membrane surrounding the embryo)
hardens and becomes impermeable to dissolved ions. Maternal chemistry will therefore be recorded
in the composition of the embryonic otoliths. Tags for transgenerational marks can be both natural
(i.e., reflecting the mother and the environment she has lived in) and artificial (i.e., female exposed
to enriched stable isotopes or elements). It is unclear at thi s point whether the incorporation of ele-
ments is linearly or non-linearly related to the ambient and ovarian concentrations. However, otolith
cores appear to be chemically di st inct from material deposited after hatching (Brophy et al. 2004),
and oocyte chemistry can reflect artificial tags of the mother for Ba (Thorrold et al. 2006) and natu-
ral tags of the environment in which the mother has lived for Sr (Kalish 1990, Rieman et al. 1994).

Chemical tags within females pass to the egg during oocyte development and are subsequently
incorporated into embryonic otoliths.
Assumptions for Methods 1 and 2 (Table 2), in addition to:
Assumption 12: The maternal tag source is identified
315
TRAVIS S. ELSDON ET AL .
Natural tag Ambient water chemistry influences the com position of body fluids within a female
and developing egg, albeit with some degree of physiologica l discrimination likely for most ele-
ments. Therefore, analysis of water samples can be used to establish that maturing females are
likely to pass on a unique signature from their environment. In the study of anadromy and life his-
tory, for example, the chemistry of fresh and marine waters needs to differ significantly; this often
occurs, but not always. However, without a complete record of waters to which females have been
exposed or a representative sample of an otolith from those env ironments, little can be said about
natal origins or habitat. Rieman et al. (1994) presents an example of how to ground truth and use
natural maternal tags.
Artificial tag This concern is alleviated if unnatural levels of elements or isotopic ratios are used
since they cannot be found in nature.
Assumption 13: Estimating tag retention in the mother and period of tag transmission
Natural tag If the fish undergoes long migrations or residence in different waters (Rieman et al.
1994) the oocyte chemistry and the tag deposited in the embryonic otolith may be unreli able as an
indicator of natal origin. However, once the egg is fertilized and the chorion hardens, the otolith's
internal environment and therefore the tag are likely to be stable.
Artificial tag If females are artificially tagged only once, yet they spawn multiple times, then the
tag in the egg is likely to degrade with each spawning event (Thorrold et al. 2006). If females are
artificially tagged in advance of spawning, then loss of the tag becomes an important consider-
ation when estimating the proportion of eggs produced by a female that will carry the unique tag.
Whether tag degradation is related to the number of spawning events (egg production) or simply the
duration of spawning season is unclear (but see Thorrold et al. 2006).

The use of otolith chemistry to determine natal origin, and therefore life history, is a powerful
technique, but comes with easily violated assumptions. To determine if a given system is appropri-
ate a few steps must be taken . First, it is necessary to demonstrate that potential water chemistries
experienced by the female are indeed distinct. Second, it is important to examine the signatures of
known-origin fish to confirm that there are tag differences in transgenerational signatures. Third ,
experiments should be done to determine the effect of time exposed to varying environments on the
oocyte tag (Thorrold et al. 2006).
Examples: Determining resident and anadromous origins of salmon and maternal transmission
Natural tag One use of tran sgenerational marks is to determine whether sa lmon (Oncorhy nchus
spp., Walbaum, 1792) in coastal rivers are from anadromous sources or resident sources or have
themselves switched life hi stories from their maternal parent (Rieman et al. 1994, Limburg et al.
2001). For example, Rieman et al. (1994) proposed that if the prehatch region of an otolith had high
Sr then the egg most likely developed when the female lived in marine waters, indicating that the
parent was anadromous. Furthermore, if Sr in the otolith core was similar to that in later-formed
otolith material (i.e., both high Sr, indicating a marine tag), then it was likely the fish was a lso ana-
dromous. Rieman et al. (1994) demonstrated that sockeye salmon otoliths could be used to deter-
mine if the maternal parent of an individual fish was anadromous or resident (low Sr in otolith core,
similar values to material deposited later). Limburg et al. (200 1) also demonstrated that anadro-
mous mothers could give ri se to resident offspring and vice versa in Baltic Sea trout (Salmo trutta,
316
Linnaeus, 1758). These studies assume that high Sr:Ca corresponds to marine waters, which may
not always be the case (e.g., Kraus & Secor 2004) and therefore requires testing.
Artificial tag Newer methods include injecting developing females with enriched isotopes (e.g.,
Ba, Thorrold et a!. 2006) or unique elemental tags, such that the developing eggs incorporate the
tag, which is then deposited in embryonic otoliths. Thorrold et al. (2006) demonstrated that an
individual female fish could be injected with an enriched barium isotope, and that the signature
was transferred to the egg and progeny. Similar results have been found for freshwater species (e.g.,
Gillanders et al. unpublished data).
Method 4: Profile analysis to define life-history variation

within a population
Background
Profile analysis of natural otolith tags can define differences in movement patterns of individuals
within a population, for example, different contingents (sensu Hjort 1914, Clark 1968, Secor 1999),
where 'contingents' refers to groups of fish with similar patterns of life-history behaviours. The use
of profile analysis to identify contingents relies on establishing relationships between otolith tags
and environmental parameters. However, interpretations can be limited to quantifying variability
in patterns without necessarily reconstructing the exact movements of fish (this is dealt with in
Method 5). In such cases, the descriptions of fish movements are limited to outlining that differ-
ent contingents occupied different environments across seasons and years of their life (e.g., Fowler
et al. 2005), but does not necessarily identify the location of the environments (this is dealt with in
Method 5) (Table 2).
Contingents are typically characterized by similarities of ontogenetic and lifetime patterns of oto-
lith chemical concentrations (for example, of Sr:Ca or Ba:Ca) in individuals within a group. Typically,
coarse generalizations can be made, such as identifying cohorts of precocious emigrating anadromous
fishes or cohorts of anadromous fishes that forage and overwinter within freshwater or in an estuary,
instead of migrating to sea. The relative proportions of different cohorts that appear in an unbiased
sample of adults (for example, in a spawning run) may reflect the importance of different habitats, or
combinations of habitats, for survival and ultimately contribution to the spawning population .

Profiles of otolith chemistry can infer contingents if groups of fish have different chemical profiles
that reflect life-history strategies and possible movements among habitats or areas.
Assumptions for Methods I and 2 (Table 2), in addition to:
Assumption I4: Otolith chemistry of individuals within groups can be differentiated into identifi-
able contingents
Classification of contingents is reliant on determining similar patterns in chemical tags across oto-
liths. Environments must, therefore, be sufficiently homogeneous that they influence the tags of all
members of a given contingent in a similar manner. Furthermore, for the contingent to be uniquely
distinguishable from other contingents, these patterns must covary among individuals within the
contingent in a way that is interpretable from an ecological or life-history perspective.
Assumption I5: Sampling offish and their profiles is representative of all profiles that exist
As with most tag studies, it is assumed that individuals caught and the contingents identified from
those fish are representative of all contingents that exist. The relative proportions of fish belonging
317
to different contingents within a sample can then be identified . If sa mpling has been limited, then
conclusions should be limited to within-group descriptions of contingents. Descriptions of con-
tributions of contingents to a population require representative sampling of that population (e.g.,
sampling mixed contingents of an anadromous species on a spawning ground).
Assumption 16: Independence of sampling along a profile

The repeated sampling of several locations within a single otolith raises concerns over the indepen-
dence of measurements in subsequent statistical analyses. Methods to address non-independent data
through time are discussed separately (see 'Further data and statistical considerations', p. 321) and
efforts should be made to address hypotheses in light of non-independent sampling.
Assumption 17: Otolith chemistry changes predictably with environmental parameters

When describing movements of fish using profiles of otolith tags, it is assumed that otolith chemi-
cals change with environmental parameters, such as water chemistry, temperature, or salinity. Thus ,
it is important to quantify how otolith tags change with environmental parameters using experi-
mental manipulations or carefully designed field tests. Chemicals under physiological or genetic
control (Geffen et al. 1998, Halden et al. 2000) are not suited for reconstructing environments.
Nevertheless, if a link can be established between water chemistry, temperature, or salinity, then it
should be possible to describe the environments where fish have lived. This still does not give an
indication of the geographic location of the different environments unless specific locations have
unique characteristics that are reflected in the otolith tag (see, for example, Dorval et al. 2007).
Importantly, links between otolith tags and environmental parameters are often species specific and
therefore should be determined for each species of interest (Gillanders & Kingsford 2003).

Identification of contingents based on otolith chemistry profiles does not require fine-scale link-
age between otolith chemistry and environmental parameters. Rather, the current method relies on
environmental gradients to define large-scale movements (e.g., freshwater to marine water habitats).
Contingents are sometimes defined based upon profile patterns alone without verification of the
underlying otolith chemistry environmental relationships , but as indicated below (Assumption 19)
seasonal or ontogenetic changes in physiological state could result in incorrect interpretations of
changes in a particular natural tag. Because contingent definition emphasizes movements between
habitats or areas, other approaches such as telemetry can serve as strong corroborative evidence
of contingent behaviours (Brenkman et al. 2007, Wingate & Secor 2007). Still, the ability to assign
contingents to particular habitats at particular times in their lives will be curtailed because water
chemistry shows important temporal-spatial variability, which is unknown. To deduce pattern s of
specific habitat use requires that chemical profiles be related to spatial and temporal data on envi-
ronmental paran1eters (this is described in Method 5).
Example: Contingents of Hudson River striped bass from otolith Sr:Ca

Secor et al. (1995b, 2001) and Zlokovitz et al. (2003) aimed to determine contingents of striped
bass (Marone saxatilis, Walbaum, 1792) using otolith Sr and Sr:Ca profiles across sectioned oto-
liths. Striped bass were collected in the Hudson River and their otoliths dissected and sectioned.
Otoliths were analysed for Sr and Ca with a series of 5-IJm point samples across the otoliths using
an electron microprobe. Data were adjusted for otolith growth using marginal increment analyses
to account for differences in annual increment widths among years. Based on known relationships
between otolith Sr:Ca and salinity in their system, Secor et al. (1995b) classified striped bass to dif-
ferent life-history behaviours: resident, mesohaline, and ocean contingents (Figure 3, Secor 1999).
Contingents were related to habitats characterized by different salinities. In particular, the striped
318
bass of the resident contingent showed evidence of high exposure rates to freshwater sources of
polychlorinated biphenyls (PCBs). Contingent membership also has consequences for growth, age
at maturation, and population persistence (Kraus & Secor 2005). Still, contingent designations only
define a coarse set of movements; more precise spatial and temporal movements can be inferred
from chemical profile analysis (see Method 5).
Method 5: Profile analysis to describe movements

through different environments
Background
Describing fish movement through environments using natural otolith tags relies on an established
link between environmental parameters (salinity, temperature, water chemistry) and otolith chem-
istry (see 'What influences otolith tags', p. 301). Satisfying the many assumptions concerning the
effects of environmental variability on otolith chemistry is no easy task (Table 2). Many studies
have not addressed these assumptions adequately. For instance, Campana (2005a) notes that several
palaeo-reconstructions of past environments using otolith chemistry did not verify the relationship
between water and otolith chemistry and therefore may have produced erroneous results. Once
correlations between otolith chemistry and environmental variables are established there remain
several further assumptions that need to be evaluated before we are able to describe fish move-
ments. Perhaps the most important overlooked scenario is that a change in otolith chemistry may
represent a change in the environment surrounding a stationary fish. Hence, knowing the variability
of environmental parameters in space and time is integral to describing movement. It is this last
assumption that can cause misinterpretations of fish movements.

Chemical profiles can be used to infer environmental and habitat occupancy of fish if relationships
between otolith chemistry and environmental parameters are known.
Assumptions for Methods/, 2, and Assumptions 16 and 17 (Method 4) (Table 2), in addition to:
Assumption /8: interactive effects of environmental parameters on otolith chemicals are known
In addition to establishing a link between otolith chemistry and environmental parameters, it is
important to recognize that several parameters may simultaneously affect chemical tags. For exam-
ple, if temperature and water chemistry both influence otolith composition (Fowler et al. 1995a,b,
Elsdon & Gillanders 2004), then simultaneous changes of these may have interactive effects on
otolith chemistry (when one environmental parameter influences the effect of another). Investigations
have shown that interactions can occur and they should be considered (Secor et al. 1995b, Elsdon
& Gillanders 2002, 2004). For example, environmental reconstructions based on otolith 8 18 0 (and
corals, foraminiferans, sclerosponges) are influenced by both temperature and the oxygen isotope
composition of ambient waters. When environmental parameters do interact to affect otolith tags,
then reco nstructions need to tease apart these effects or they may misinterpret movements using
only one variable. lt may, therefore, be necessary to examine the spatial and temporal changes of
the interacting parameters (see also otolith crystallization in Assumption 21) within the water bod-
ies being examined.
Assumption 19: Ontogenetic effects on otolith chemistry are known (if reconstructions bridge dif-
ferent life-history periods)
Otolith tags can differ with life-history stages (larval, juvenile, subadult, and adult otolith growth)
and metamorphosis (Toole et al. 1993). If profiles of chemical tags bridge life-history stages, then
319
tag differences may represent ontogenetic effects and not changes in environmental parameters.
Fish with obvious metamorphic stages, such as eels (Arai et at. 2000, 2002, Correia et at. 2003), are
particularly prone to ontogenetic changes in otolith chemistry that could be misinterpreted as large-
scale movements. Rearing fish in constant, or at least known, environments during ontogenetic
(Fowler et at. 1995b, Elsdon & Gillanders 2005a) and physiological changes (e.g., osmoregulation,
Zimmerman 2005) can elucidate such effects.
Assumption 20: Spatial and temporal variations in environmental parameters are quantified
To determine fish movement from otolith tags , it is often assumed that differences in otolith chemis-
try profiles represent fish movement, when in fact they could represent a change in the environment
around a stationary fish. Thus, to infer fish movement, it is necessary to demonstrate that changes
in otolith profiles must have resulted from a movement between habitats . Few descriptions of fi sh
movement using otolith chemistry have acknowledged this issue (Kraus & Secor 2004, Elsdon
& Gillanders 2006a). Long-term stability of environmental parameters should not be assumed,
especially in dynamic environments (Table 2, Figures 3 and 4). Examining spatial and temporal
variation in environmental parameters can provide a solution to this problem (see 'Further data
and statistical considerations'), as otolith tags can be compared to environmental parameters in
space and time to determine where fish were during periods of tag incorporation (e.g., Elsdon &
Gillanders 2006a). The best descriptions of fish movement would be expected in environments with
stable water chemistry, temperature, and salinity (e.g., Elsdon & Gillanders 2005b). Barring such
constancy, researchers may also be able to infer movement on fairly coarse spatial scales, such as
among estuarine salinity zones (e.g., Kimura et at. 2000), if underlying chemical gradients are suf-
ficiently different.
Assumption 21: Correlations between otolith crystallization and chemistry are known
Links between environmental properties or physiology and otolith chemistry are undoubtedly cor-
related to otolith crystallization rate. Examples where otolith crystallization has been correlated
to otolith chemistry include Sr:Ca changes with ontogeny (Tzeng 1996), different effects of tem-
perature at low versus high salinity (Elsdon & Gillanders 2002), and annual variations in Sr:Ca
(Sadovy & Severin 1992). Correlations between crystallization rate and otolith chemistry have been
discussed in Campana (1999), although there are limited data on the chemical processes that are
responsible. It is important, however, to realize that differences in chemical tags along profiles can
be caused by variation in crystallization rate and might not necessarily represent differences in
environmental properties (see also Assumptions 17- 19). This may, in turn, result in similar misin-
terpretations as those described for Assumption 20. Since otolith crystallization rate is often highly
correlated with the somatic growth rate of the fish, comparisons of somatic growth rate among the
groups or stages of interest can usually point to potenti a l misinterpretations.

Done correctly, the determination of fish movement by relating otolith chemical profiles to envi-
ronmental parameters provides valuable information. Determining precise fish movements using
profile analysis is perhaps the ultimate goal of many studies, but it is difficult to achieve in practice.
Few in ferences about precise fish movements can be made if assumptions on how environmental
parameters affect otolith tags and the spatial and temporal variation in environmental parameters
are not met. Studies that do not meet assumptions, particularly about the spatial and temporal extent
of variation in environmental parameters, may misinterpret fish movements . For instance , a migra-
tion inferred as an estuarine-to-marine movement could in fact represent an estuarine-to-freshwater
movement if Sr:Ca in the freshwater end-member is higher than the marine Sr:Ca values (Kraus
320
& Secor 2004). To what extent misinterpretation of fish movements has occurred in the existing
literature is unknown.
Example: Estuarine residency determined using otolith Sr:Ca and temporal collection of water
Sr:Ca
Elsdon & Gillanders (2006a) linked otolith Sr:Ca of the estuarine fish black bream (Acanthopagrus
butcheri, Munro 1949) to temporal collections of water Sr:Ca to determine if fish were resident or
migrants to particular sites. Water Sr:Ca was collected on nested spatial scales of months, weeks, and
days in summer and winter at two estuarine locations. The sampling design allowed for the detec-
tion of coarse (month and week) and fine (day) temporal scales of variation (Elsdon & Gillanders
2006b). Water Sr:Ca variation was used, along with known correlations, to predict otolith Sr:Ca of
a stationary 'resident' fish at each location. Fish were collected at each location corresponding to
the last water sample, so otolith Sr:Ca of wild fish could be compared to the predicted stationary
'resident' fish. Otoliths of fish were analysed using LA ICP-MS to generate profiles of Sr:Ca across
the otolith. Fish were classified as residents if their otolith Sr:Ca matched that of the predicted con-
centrations of a stationary 'resident' fish or as migrants if their otolith Sr:Ca did not match predicted
values (Figures 3 and 4, Elsdon & Gillanders 2006a).
Further data and statistical considerations

Statistical techniques for examining natural and applied otolith tags include univariate and multivar-
iate approaches. Simple guidelines already exist both for general statistics of otolith data (Campana
2005b) and for more specific statistics used to determine connectivity among groups (Method 2,
Gillanders 2005). We do not cover what has already been published, but instead highlight three
areas that require clarification: detecting variability at different spatial and temporal scales, non-
independence of repeated measurements within sectioned otoliths, and limitations in using natural
tags to assess philopatry and movement rates, as well as some further data considerations.
Detecting variability at different spatial and temporal scales

Detecting and interpreting variation in otolith tags and environmental parameters in space and time
is required to advance interpretations of movement via Methods l, 2, and 5. It is critical that otolith
and water chemistries vary at scales appropriate to the hypotheses and questions being addressed.
Many papers investigating patterns in space and time do so by collecting data using either fixed
or haphazard sampling designs (i.e., sampling water chemistry once a month for several years to
determine 'monthly' or 'seasonal' patterns). Although fixed sampling designs provide useful infor-
mation, the data acquired may only have relevance for a particular point in space or time. This is
especially true if variation occurs at scales smaller than those being investigated. It is therefore
useful to examine variation in space and time using a nested or hierarchical sampling design . Such
designs are commonly described in the ecological literature (Underwood 1997, Quinn & Keough
2002 , Gotelli & Ellison 2004), but they are less commonly used to describe variation in environ-
mental parameters. Nested designs entail collecting data on several scales of space or time, such as
taking replicate sampling of water chemistry (1-2 m apart), within sites (kilometres apart), within
locations (tens of kilometres apart) (Dorval & Jones 2005), or sampling water chemistry on differ-
ent tidal cycles within replicate days, weeks, months, and seasons (Elsdon & Gillanders 2006b).
Data obtained using nested designs can be analysed using nested analysis of variance (A NOVA;
either ANOVAs for univariate or multivariate ANOVAs [MANOVAs] for multivariate analyses) to
determine scales of significant differences. In addition, data can be examined using variance compo-
nents (Vaughan & Corballis 1969, Graham & Edwards 2001) to determine the proportion of the total
321
variation attributed to different scales. Variance components have not been widely used in ecological
research, perhaps due to differing views about their applicability to mixed-model and orthogonal
ANOVA designs. Nested designs are, however, ideally suited to variance component calculations.
Repeated measurements on an otolith

Quantifying chemical tags within two or more specific portions of a single otolith raises questions
of independence of sampling and repeated measurement on a subject. Primarily, investigations of
movement, such as Method 2, are best done using independent otoliths. For example, otoliths of
juvenile fish caught at specific locations are used to establish chemical tags for those locations
(Campana 2005b), and then otoliths of adult fish are analysed in the juvenile portion of otolith
growth to establish the locations of juvenile occupation. In this respect, the otoliths used to establish
tags and those for which movements are determined are independent.
If otolith data consist of chemical profiles, individual measurements within that profile (of
the same fish's otolith) are not independent. Therefore, repeated measures of analysis of variance
(RM-ANOVA) can be used to investigate differences among groups of fish over time, where otoliths
of individual fish have been repeatedly sampled. It is important to recognize that a group of fish
may contain individuals that have different otolith tags if fish movements do not completely overlap.
The method requires that individual fish within a group have similar chemical tags across their
otoliths (i.e., tag (across the otolith) x individual term is non-significant, Underwood 1997). Thus in
applications of RM-ANOVA, chemical profiles have been classified into age or size bins (Secor &
Piccoli 1996, Kimura et al. 2000). Mixed model RM-ANOVA can provide a more efficient means
to extract information from profile data by estimating degrees of freedom from fitted covariance
structures, rather than assumed covariance (Jones 2000, Kimura et al. 2000). RM-ANOVA is a use-
ful way to group together individuals with similar life-history patterns (Method 4) or movements
(Method 5). If individuals have similar tag patterns through time (tag (across the otolith) x individu-
als (group); not significant), then this could be used as grounds for grouping fish with similar pro-
files. Regardless of how data are treated, questions of data independence when examining otoliths
using profile analyses should be acknowledged and statistically addressed.
Limitations in using natural tags to assess philopatry

and movement rates
Otolith chemistry is increasingly used as a tag to quantify movement and philopatry without careful
attention to underlying assumptions and limitations. There is a rich and well-established statistical
literature that deals with the use and misuse of tags (Brownie et al. 1978, Seber 1982, Williams
et al. 2002) that can guide investigators in using tagging data properly. Unfortunately, these statisti-
cal approaches have only been developed for applied tags and the theory and methods of use for
natural tags is in its infancy (C.M. Jones personal communication). Until these methods are better
developed, we caution investigators to be circumspect in their attempts to develop rate estimates
with natural otolith tags.
Conclusion and future research needs

We have highlighted five methods that use otolith chemical tags to determine movement and life-
history measurements of fish. Each of these methods addresses a discrete and different hypothesis
about fish movements. The first three methods are primarily based on reconstructing movements
by linking groups of fish in space and time. The last two methods are based on analyzing chemi-
cals across otoliths and relating these patterns to possible movements. Method 4 allows inferences
related to ontogenetic and lifetime movement modalities (i.e., contingents). Method 5 permits more
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OTOLITH CHEMlSTRY OF FlSHES
spatially and temporally precise estimates of residency and movement. By using one of these five
methods , and addressing the corresponding assumptions, inferences and interpretations of fish
movement using otolith chemistry can be maximized .
Three major knowledge gaps require further investigation. First, knowledge of factors influenc-
ing otolith chemistry is still limited , making it difficult to generalize environmental effects among
species. Advancing our knowledge base in this area will help us understand why otolith tags differ,
and if they are likely to differ in predictable ways. Second, it is important to know the spatial and
temporal scale of variation in both otolith tags and environmental properties. Some excellent data
on spatial and temporal variability in otolith chemistry exist. Less emphasis has been placed on
examining variability in environmental properties, specifically for dissolved elements that are use-
ful in otolith studies (i.e., Sr and Ba). Obtaining these basic patterns is imperative to determining
movements of fish based on all methods. Third, natural otolith chemistry holds great promise to
address issues of philopatry and movement, but the ability to fulfil this promise will depend on the
clarification of proper statistical models and techniques.
Technological advances have made chemical analyses of otoliths more routine . Technology will
continue to improve, and it is foreseeable that we will be able to quantify chemicals with greater
accuracy and precision. These advances have the potential to increase our understanding of fish
movement; however, the interpretation of data will still rely on a thorough understanding of the
assumptions presented here.
Acknowledgements
Travis Elsdon received support by an ARC postdoctoral fellowship at University of Adelaide and
from the Postdoctoral Scholar programme at the Woods Hole Oceanographic Institution, with fund-
ing provided by the Ocean Life Institute. Brian Wells received support from a NOAA Fisheries
postdoctoral fellowship and the National Academy of Sciences. Karin Limburg received support
from National Science Foundation grant DEB-0238121. Cynthia Jones received support from the
National Science Foundation grant OCE-0525964. David Secor received support from National
Science Foundation grant OCE-0324850. Benjamin Walther received support from the MIT/WHO I
Joint Program , the Woods Hole Oceanographic Institution Ocean Life Institute, and the United
States Coast Guard Academy. We thank those who provided unpublished data.
Glossary
Chemical: Collective term used to represent elements (i.e., Ca, Sr), isotopes (i .e., 8 13 C, 8 180), and
other trace compounds (elements in trace levels of abundance, such as rare earth elements).
Contingent: A term first used by Hjort (1914) and later by Clark (1968) to describe groups of fish
with similar migration pathways.
End-member(s): Water masses with distinct chemical properties between which gradual changes
occur, for example, mixing of two chemical end-members (freshwater and saltwater) along
an estuary, where a gradual chemical change is detected from one end-member to the other.
Group(s): Fish within a population that have similar otolith chemical tags. These fish can be con-
sidered to have occupied similar areas or had similar movement patterns.
Location: The area inhabited by a group(s) of fish. A region is made up of more than one location.
Migration: One type of movement, commonly associated with a response to changing resources
(Dingle 1996).
Movement: Change in location from one place to another. There are several subcategories of move-
ment, such as foraging, commuting, territorial, and ranging, as outlined in Dingle (1996).
Philopatry: Tendency of a fish to stay in or return to its home area.
323
Popu lations (of fish): A unit of fish of the same species within a given area that has the potential to
mix. Two units of fish of the same species that occupy non-overlapping areas (i.e., Atlantic
and Indian Oceans) and do not mix would be considered separate populations.
Profile: The quantification of chemicals in two or more different portions of one otolith. These
have also been referred to in the literature as transects, trajectories, profiles, scans, chro-
nologies, and line scans, but for the purpose of this review have been unified in name. The
main use of profile analyses in otoliths is to determine differences in chemical tags that
relate to different life-history periods, be that days, weeks, months, or years.
Region : The area inhabited by units of fish at a population level. This gives no scale to the area, but
suggests that it is large enough to incorporate groups of fish with different otolith tags, and
therefore would contain more than one location.
Tag: The chemical concentrations (univariate or multivariate) in otoliths that can be used as an
identifiable measurement of fish movement. Tags can be of natural origin (chemicals in
natural abundances) or deliberately applied (chemicals in altered abundance or unnatural
isotopic ratio, or an e lement typically in low concentration (e.g., lanthanides)). For whole-
otolith solution analyses, one tag is estimated, which is the integrated signature of the
otolith. For sectioned otoliths, one or more tag(s) can be estimated that relate to different
life-history periods of the fish.
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Oceanography and Marine Biology: An Annual Review, 2008, 46, 331-363
© R.N. Gibson. R. J. A. Atkinson, and J. D. M. Gordon , Editors
Taylor & Francis
PARADIGMS IN FISHERIES OCEANOGRAPHY

WILLIAM C. LEGGETT 1 & KENNETH T. FRANK 2
1
Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada
E-mai I: wleggett@queensu.ca
2Department of Fisheries and Oceans, Bedford Institute
of Oceanography, Dartmouth NS B2Y 4A2, Canada
E-mail: FrankK@mar.dfo-mpo.gc.ca
Abstract The development of the field of fisheries oceanography over the past century has
been heavily influenced by a relatively small number of paradigms that have shaped thinking,
influenced lines of enquiry and occasionally stalled progress in the field. This review provides
an overview of what are considered to be the most influential paradigms in the discipline. Each
begins with a brief discussion of its origins. Next their respective (and often overlapping) impact
on the development of the discipline is discussed and then the evolution of these paradigms
as shaped by new advances in approaches and technologies and by direct challenges to their
underly ing assumptions is reviewed. For each, the endpoint is an overview of the current state
of knowledge and thinking and the probable future direction of research in the area. The review
concludes with an overview of the probable future directions of research in the discipline as a
whole.
Introduction
The discipline of modern fisheries oceanography has its origins in the work of Johan Hjort (1914,
1928), who was the first to formally hypothesize a link between the dynamics of fish populations
and the dynamics of their environment. In his 'critical period' paradigm Hjort argued that variabil-
ity in food availability during the tran si tion from endogenous to exogenous feeding in larval fishes,
typically a very narrow time window, was central to the survival of individual larval cohorts. Hjort
hypothesized that when food was abundant, survival (and recruitment) would be high, and when
food was scarce survival and recruitment would be low. This hypothesis was subsequently general-
ized by Cushing (1975) who reasoned, in his ' match mismatch' hypothesis, that food availability
was linked to the interaction between interannual differences in the timing of spawning/hatching
and the timing and magnitude of the primary a nd secondary production cycles in the ocean. These
hypotheses dramatically influenced the direction of research in the field by (I) focusing research into
the causes of interannual variability in recruitment on the egg and larval stages of fishes , (2) provid-
ing a simplifying construct within which to explore the causes of temporal changes in the abun-
dance of commercially important marine fishes and (3) by linking fluctuations in the abundance of
fishes directly to the dynamics of other components of the ocean ecosystem. In hindsight, Hjort's
major contribution appears to have been to awaken thinking and research into the nature of thi s
dynamic interaction between fish and their environment. Prolonged adherence to Hjort's ideas, and
the lure of Cushing's hypothesis, combined to dominate thinking and research in the field for most
of the twentieth century, some would say negatively (Leggett & DeBlois 1994). As the discipline has
advanced several new paradigms have evolved. While originally offered as simplifying constructs,
33 1
WILLIAM C. LEGGETT & KENN ETH T. FRANK
Table 1 Paradigms in fisheries oceanography

I. Spawning stock biomass (SSB) is a su itable proxy for the reproductive potential of a stock .
2. Marine fish eggs and larvae are generall y designed for dispersion and potential co lonizati on (panmixia).
3. In marine temperate systems, fish spaw n in springtime so that peak larval abundance coincides with maximum prey
availability (Cushing's match/mi smatch hypothesis).
4 . Environmentally based recruitment models, when updated with new data, invariably fail; recruitment predictio n is an
intractable problem, particularly when it is based o n processes associated wi th the growt h and mo11ality of the early
life-history stages.
5. Populations cannot irreversibly collapse/collapsed populations will recover in the absence of fishing.
6. Fish stocks can be managed in iso lati on from their total environment/habitat.
7. Population recovery is synonymous with rebuilding.
and as the foundation for new studies of important processes governing the dynamics of fi sh stocks,
some of these new paradigms now approach the status of dogma once accorded Hjort's hypothesis
and have the potential, if pursued uncritically, to once again delay progress in the field. This review
examines the major paradigms that have shaped thinking and research in fisheries oceanography
over the past century and explore how recent research has affected understanding of their validity
and usefulness now, and going forward. Table l provides an overview of these paradigms ordered
hierarchically from individuals to ecosystems.
The need for a more holistic and effective approach to the science of fisheries oceanography,
and of the management strategies applied to marine fishes, is evident from the breadth of species
now undergoing serious decline, not only worldwide, but also within more restricted ecosystems
(Dower et al. 2000, Figure 1).
The advent of new methods (ageing techniques for larval fishes, the application of biochemical
and molecular techniques, the development of instrumentation and computing capacity that has
allowed physical oceanographers to measure and model the highly dynamic and variable environ-
ment of continental shelf ecosystems, satellite imagery, etc.) have created new opportunities to
explore the dynamics of marine fishes in relation to the dynamics of their physical environment and
the ecosystems they inhabit.
Paradigm 1: Spawning stock biomass is a suitable

proxy for the reproductive potential of a stock
The Hjort and Cushing models focused primarily on the factors determining interannual variability
in mortality rates experienced by larvae (the life stage widely believed to be the most vulnerable to
environmental variability (reviewed in Leggett & DeBlois 1994). Another highly influenti a l para-
digm holds that .it is the product of the number of offspring generated by a spaw ning stock a nd the
rate of ｭｾｲｴ｡ｬｩｹ＠ experienced by those offspring until they recruit to the reproducing population
that govern the dynamics of fish populations. This thinking is inherent in stock recruitment model s
(Ricker 1954, Beverton & Holt 1957) that have formed the cornerstone of studies of the recruitment
dynamics of fishes , and of management based on these studies, for most of the latter hal f of the
twentieth century. These models assume strong density dependence (Figure 2).
Fundamental to the practical application of these models has been the assumption that the total
spawning stock biomass (SSB) is an acceptable proxy for the reproductive potential of the stock of
interest. This assumption is employed because SSB can be readily derived from fisheries survey
data, whereas total egg production (TEP), a more reliable and realistic indicator of reproductive
output is more labour intensive to obtain and, for this reason , does not exist for most stocks.
The use of SSB as a proxy for TEP implies that (l) spawner biomass is proportional to the TEP
and (2) in lay terms, "an egg is an egg is an egg," that is, all eggs are equa l in their potential to
332
herring 4VWX-SSB
yellowtail flounder 5Z-SSB
turbot 4RST-SSB
little skate 4VWX-SSB
winter skate 4X-SSB
smooth skate 4VWX-SSB
smooth skate 4T-SSB
cod 4T-SSB
cod 4X-SSB
silver hake 4VWX-SSB
cod 5Z-SSB
winter skate 4VsW-SSB
haddock 4VW-SSB
cod 4Vn-SSB
mackerel-SSB
winter skate 4T-SSB
haddock 4X-SSB
plaice 3Ps-SSB
haddock 5Z-SSB
thorny skate 4T-SSB
thorny skate 4VWX-SSB
cod 4VsW-SSB
pollack 4VWX-SSB
white hake 4T-SSB
cod 2j3KL-Otfhore Survey-SSB
cod 3NO spring-SSB
plaice 2J3K-SSB
plaice 4VT-SSB
1970 1975 1980 1985 1990 1995 2000
Years
Figure 1 (See also Colour Figure I in the insert following p. 250.) Ordination of the time of series of spawn-
ing stock biomass of various species from scienti fie surveys conducted throughout the north-west Atlantic,
illu strating that the majority of the stocks are at biomass levels well below (red) the long-term average.
Intensity of colours is proportional to the magnitude of the standardized anomaly in standard deviation units.
Alphanumeric labelling refers to the Northwest Atlantic Fisheries Organization management unit.
produce a recruit to the population. However, the variation in SSB is generally insufficient to account
for the related variation observed in recruitment in marine fish populations (Shepherd et al. 1984,
Wooster & Bailey 1989, Rijnsdorp et al. 1991, Marshall et al. 1998). Notwithstanding this reality,
the paradigm that SSB is a suitable proxy for total reproductive effort has persisted and has, in turn,
been an important contributor to the persistence of the Hjort and Cushing hypotheses and the focus
of research into the causes of recruitment variation in marine fishes. This includes the search for
ecological and/or environmental factors affecting egg and larval mortality- an approach that has
proved challenging and, in only limited cases, successful (see Paradigm 4). This has impeded the
development of a coherent understanding of the recruitment dynamics of marine fishes in particular
and the science of fisheries management in general (Rothschild 1986, Hilborn & Walters 1992).
333
WILLIAM C. LEGGETT & KENNETH T. FRANK
North Sea herring

•
c<lJ
40
•
§
.2 •
..,
u
"'
0:: 20 •• • •
•
•
• ' •••• ••• •
•
0
2 3
SSB
Figure 2 Ricker stock recruitment model fit to data for North Sea herring. SSB, spawning stock biomass.
In the 1990s these assumptions began to come under increasing scrutiny (Lowerre-Barbieri
et al. 1998, Marshall et al. 1998, Marteinsdottir & Steinarsson 1998, Marshall & Frank 1999,
Marshall et al. 1999). Marshall et al. (1998) were the first to demonstrate in situ the potential fallacy
of the assumption inherent in the use of SSB as a surrogate for TEP. Their work with Barents Sea
cod (Gadus morhua) showed that recruitment was positively correlated with the quantity of lipid
energy stored in the liver of mature females or, in other words, with female condition . Boyd et al.
(1998) observed a similar relationship between parental fat levels and recruitment in Cape anchovy
(Engraulis capensis). In cod, total liver energy was proportional to TEP and, like TEP, varied with
capelin (Mallotus villosus) abundance (Yaragina & Marshall 2000) such that by either measure the
reproductive potential of a fixed number of mature females was significantly higher when the quan-
tity of food available to maturing fish was abundant and correspondingly lower when it was scarce.
In contrast, cod SSB was found to be not statistically different at high and low prey levels. In short,
their study confirmed prior suspicions regarding the paradigm that SSB is an inadequate surrogate
for TEP and demonstrated that replacing SSB with more accurate measures of reproductive poten-
tial is fundamental to a fuller understanding of the dynamics of recruitment in marine fishes.
The work of Marshall et al. (1998, 1999) has been an important factor in redirecting the focus
of studies into the causes of interannual variation of recruitment in marine fish populations. Their
findings demonstrated that a more successful pursuit of process-oriented models of the recruitment
dynamics of marine fish will require integration of the processes affecting reproductive output
(growth, production and condition of spawners) with mortality processes affecting egg, larval and
juvenile survival (UIItang 1996, Marshall et al. 2000).
Research by Yaragina & Marshall (2000) has demonstrated that the search for a comprehensive
understanding of the factors regulating variability in reproductive potential, independent of SSB ,
may be as complex, and as inextricably tied to environmental and ecological factors, as are the
causes of variation in egg and larval survival. For example, their study of temporal variation in the
liver condition index (LCI) -an important determinant of reproductive potential (Marshall et al.
1999)- of five length classes of north-east Arctic cod (Gadus morhua) showed that while varia-
tions in the abundance of capelin, a major food source, was the proximate determinant of variation
in LCI, an indirect, but perhaps not ultimate, determinant of variation in the index appears to have
been the abundance of herring (Clupea harengus), which influence cod LCI indirectly via their
predation on capelin, which in turn are the main prey of cod.
Interest in the role and importance of maternal effects as regulators of the recruitment dynamics
of marine fishes has increased since the publication of these findings. Scott et al. (2006) modelled
the daily reproductive output of a range of simulated age/size-structured populations of Atlantic
334
cod , created under contrasting stock recruitment scenarios, over an entire spawning season. The
objective was to determine the effects of individual female condition and egg quality on stock repro-
ductive potential (SRP). Their findings suggest that, in two populations having equal SSB, the effect
of low levels of individual condition in one can lead to almost total reproductive failure for that
population . Moreover, the positive effect of increased individual condition was found to depend on
the particular population structure designated in the model, a variable that, in situ, can be strongly
influenced by both fishing intensity and environment. Indeed, they reported that differences in
population size and age structure produced by differences in fishing mortalities ranging from 0 to
1.0 could reduce the SRP by 48-74% depending on the related assumptions regarding female con-
dition and quality. Any factor, anthropogenic or environmental, inducing changes in mortality of
equivalent magnitude would be expected to produce a similarly scaled result.
Vall in & Nissling (2000) studied the effect of female age on the survival of cod eggs and lar-
vae in the Baltic, where successful spawning is restricted to the deep basins at salinities varying
between II and 20 ppm. Due to the oxygen depletion commonly prevailing in these areas, neutral
egg buoyancies above oxygen-critical depths are important to egg survival. They found that large
females produce larger eggs that exhibit neutral egg buoyancy at lower salinities, thereby ensuring
egg development in more favourable oxygen conditions. The number of recruited cod (age 2), in
the Baltic Sea over two eras characterized by different conditions (1967-1980 and 1981-1994), was
found to be positively related to the fraction of eggs produced by older females (5+ yr), implying a
strong maternal effect on recruitment. Berkeley et al. (2004) report a similar positive relationship
between female age and probability of egg survival in longnose grenadier (Coelorhynchus carmina-
tus). Marteinsdottir & Steinarsson (1998) report similar findings for the egg and early larval stages
of cod.
The findings of Yallin & Nissling (2000) also illustrate the potential for negative effects of
fishery-induced changes in population age structure on population size and persistence. Scott et al.
(1999) modelled this fishing effect and found that the effects of the loss of more fecund older/larger
individuals in the population could lead to overestimation of the number of potential recruits to
populations experiencing higher levels of fishing mortality by as much as 60%.
Environmental variables can also influence the condition of females and the demographics of
populations in ways that can dramatically alter reproductive output independent of SSB. Scott et al.
(1999) note that when size- (growth-) related maternal effects on egg viability were incorporated
into their fishing effect model, the number of potential recruits to heavily exploited populations
could be reduced by a further LO%.
The work of Choi et al. (2004) illustrates just how profound these environmental influences
can be. In their paper on the devolution of the Scotian Shelf ecosystem off Nova Scotia, Canada,
they document declines in growth rates, size at age and age at maturation of the entire benthic fish
community that mirror the changes modelled and documented above. These changes occurred pro-
gressively over a 45-yr time period (1960-2005), the most dramatic changes occurring in the early
1990s. They resulted in average sizes of mature (age 5) cod, haddock (Melanogrammus aeglefinus),
pollock (Pollachius virens) and silver hake (Merluccius bilinearis) that were 70-80% of the 1970s
levels and remain depressed in spite of a moratorium on fishing that began in 1993 (Figure 3).
Drinkwater (2002) estimates that approximately 30-50% of the decline in SSB of cod that occurred
in the 1980s and early 1990s was linked to these reductions in deep-water temperatures and their
depressing effect on growth rates and corresponding sizes at age. Given the strong positive relation-
ship between body size and fecundity in these species (Pinhorn 1984, Waiwood & Buzeta 1989), a
corresponding decline in per individual reproductive potential, independent of losses due to coinci-
dent reductions in the total number of spawners, clearly occurred.
335
70.-----------------------------------------,
-Cod
- Haddock
-Poll ock
60 • - Silver hake
•
30
•
Figure 3 (See also Colour Figure 3 in the insert.) Changes with time in lengths at age 5 for four groundfi sh
species from the eastern Scotian Shelf.
Their analysis also revealed that these dramatic changes in reproductive output were not simply
the consequence of reductions in the size of reproducing adults (a product of the negative effects
that quotas based on biomass and the behaviour of fishermen focusing their efforts on the largest
fish available; e.g., see Drinkwater 2002). For example, during the 1960s and 1970s the physiologi-
cal condition of these fishes exceeded the 45-yr norm. However, throughout the 1980s and 1990s
physiological condition declined sharply and by 2000 the majority of the fish were in below-average
condition. Given the documented impact of female condition on egg quality and recruitment in
cod (Marshall et al. 1999), and the evidence of maternal effects on survival linked to female size
and condition, it is likely that in this species, and perhaps others, a further reduction in effective
reproductive output, independent of SSB, was experienced as a consequence of combined effects of
declining size and condition, both of which had an environmental component.
There is also evidence that the total metabolic rate of the e ntire demersal ecosystem was
depressed as a consequence of changes in ocean climate. These ocean climate changes included
a progressive decline in bottom temperatures, an increase in the volume of the cold intermedi ate
layer, and movement of the Gulf Stream Front to a more offshore position. These changes are judged
to have been caused by an increased along-shelf advection from the Gulf of St. Lawrence and south-
ern Newfoundland augmented by local, atmospherically induced cooling (Drinkwater et al. 2003).
One of the outcomes of thi s change was a dramatic reduction in the biomass of the once-dominant
euphausiid (Euphausia superba) and a corresponding decline in their contribution to the overall diet
of the demersal fish assemblage. For example, the contribution of this euphausid species to the diet
of pollock and cod declined from >65% by weight in the 1980s to <10% in the 1990s (Hanson &
Chouinard 2002, Carruthers et al. 2005).
The resulting hysteresis in the structure of the Scotian She! f ecosystem in the late 1980s pro-
duced an ecosystem dominated by smaller pelagic fishes and benthic invertebrates (mainly shrimp
and crab) in which the once-dominant large-bodied demersal fishes now play a relatively minor role.
The fact that these once-dominant species have not recovered even in the absence of exploitation,
336
as traditional stock recruitment models would predict, suggests that a fundamental change in their
fitness has occurred. The disjunction between SSB and effective reproductive output appears to be a
significant factor in this change in fitness and may have contributed in a major way to the dramatic
collapse of these once-dominant demersal species in the early 1990s.
Paradigm 2: Marine fish eggs and larvae are generally

designed for dispersion and potential colonization (panmixia)
Reproduction in commercially exploited marine species generally involves the spawning of billions
of tiny eggs that float in the near-surface waters during the spring of each year. The generality and
magnitude of these events were widely considered to be an adaptation to the very high mortality of
early life stages caused by the vagaries of the environment (Rothschild 1986, Rothschild & DiNardo
1987). One variable identified as important in this context was ocean currents, often driven by wind,
which caused larvae to be transported to regions where food and other factors were less favourable.
Several correlation studies reported significant relationships between larval survival, measured by
the abundance of the recruiting year-class, and dispersive events
For example, it has been hypothesized that warm core rings (eddies representing instabilities in
the Gulf Stream that can entrain large volumes of water from the continental shelf) can transport
sufficient numbers of eggs and larvae off the shelf to have a significant negative impact on recruit-
ment. Myers & Drinkwater (1989), who examined this hypothesis using estimates of entrainment
from 14 yr of satellite imagery and recruitment estimates for 25 fish and shellfish stocks ranging
from the Mid-Atlantic Bight to the southern Grand Banks, found that increased warm core ring
activity was associated with low recruitment levels in 17 of 18 groundfish stocks examined. The sole
exception was cod on Georges Bank. While the level of significance related to each stock was low,
the collective result was consistent with the original hypothesis. For other examples of the possible
link between dispersive effects and recruitment see Carruthers et al. (1951) and Bailey (1981). The
findings of these and other studies led to the view that either excessive dispersion of larvae or dis-
placement to areas distant from the nursery ground was a primary cause of the reduced recruitment
that resulted when wind strengths and direction were unfavourable. However, in most cases updated
analyses of these models have failed to support the relationships originally observed (Myers 1998,
see Paradigm 4).
The seminal work of Sinclair (1988) showed that many continental shelf spawning locations of
marine fishes were located in areas characterized by retention features or semipermanent gyres, the
current characteristics of which act to minimize the advection of the egg and larval stages and con-
sequently their vulnerability to dispersive processes. Many subsequent studies have expanded the
suite of species that utilize relatively non-dispersive oceanographic settings for spawning and early
larval development (Hinrichsen et al. 2001 , North & Houde 2001, Lett et al. 2007). In addition,
the advent of technologies allowing high-resolution, discrete-depth sampling of the water column
revealed that ontogenetic shifts in depth distributions and vertical migratory behaviour of larvae
also serve to minimize dispersion from the spawning areas. These findings have moderated the
belief that the early life stages of marine species were simply passive drifters and that survival was
largely dependent on the "mercy" of the currents.
One of the most striking examples of this non-dispersive reality involves haddock that spawn
on the offshore banks of the Scotian She! f. Because of the recirculation that occurs around each
of these discrete spawning banks there is a strong tendency for the egg and larval distributions of
haddock that spawn there to be discrete. And, when larvae metamorphose to the juvenile stage, a
development process that takes about 90 days, settlement to the bottom occurs in the same zones in
which they were spawned, which now become prime feeding areas for the juvenile and adult stages
(Frank et al. 2000).
337
WILLIAM C. LEGG ETT & KENN ETH T. FRANK
These findings are consistent with the results of modelling st udies of the scales of connectivity
in Caribbean reef fishes (Cowen et al. 2006). They found that larva l dispersal scales for most spec ies
were of the order of 50-100 km , much smaller than has generally been assumed. Their analyses also
indicate that passive dispersal/retention is insufficient for population replenishment, recruitment
levels generated from the use of passive dispersal assumptions in the model being one to two orders
of magnitude lower than that required for successful population replenishment.
These studies call for a general rethinking of the adaptive character of the spawning behaviour
of many marine species from spawning as a vehicle for colonization or bet hedging to one in which
the entire early life-history period is viewed as an elegant suite of adaptations to an environment that
is highly variable at interannual and smaller timescales but is more predictable in the longer term.
However, while this longer-term predictability is reflected in adaptations involving both the
timing and location of spawning, interannual variability in the ocean environment can resu lt in
importa nt disruptions to their efficacy that lead to recruitment variability and even recruitment fail-
ure. Well-known examples include the relationship between capelin recruitment and onshore wind
discovered by Leggett et al. (1984), the destabilizing effects of warm core rings on the retention
dynamics of Scotian Shelf banks (Myers & Drinkwater 1989) and the influence of upwelling events
on recruitment processes along the North African coast (Cury & Roy 1989). Such disruptive events
can also lead to the establishment of new subpopulations through colonization of new habitats when
environmental conditions permit. Detection of such colonization episodes is most evident when they
occur outside the normal range of distribution. The larval drift associated with anomalous ocea no-
graphic conditions involving the displacement of cod larvae from Iceland to West Greenland - a
colonization event covering a distance of almost 1000 km (Frank 1992) - is a striking case in point.
A similar displacement, on a much smaller geographic scale, was shown for haddock larvae originat-
ing from the eastern Scotian Shelf. Larvae of this species episodically drift downstream to Browns
Bank on the western Scotian Shelf. In the case of both cod and haddock, the dispersed larval stages
appear to persist and to contribute to the recruiting year-class in the colonized area from which they
then make a subsequent return to their spawning area during the maturation phase (Frank 1992,
Brickman 2003). Similar events appear to be a characteristic of many Caribbean fishes (Cowen et al.
2006). Discovery of this phenomenon has resulted in the need for sig nificant upward revisions in the
estimates of year-class strength at the natal site and a corresponding bonus to the local fishery. Its
implication for the assessment and ma nagement of adjacent stocks is a lso profound.
Paradigm 3: In marine temperate systems, fish

spawn in springtime so that peak larval abundance
coincides with maximum prey availability
(Cushing's match/mismatch hypothesis)
The Hjort and Cushing hypotheses, which were so instrumental in directing the early research into
the population dynamics of marine fi shes, were founded on the dynamic interaction between the
temporal and spatial distributions of larval fishes and their prey. Leggett & DeBlois (1994) system-
atically reviewed the scientific evidence for and against these hypotheses and found Hjort's hypoth-
esis to be wanting. Support for Cushing's hypothesis was judged equivocal, mainly because of the
difficulty of adequately operationalising the hypothesis and the technical challenges of assembling
data on appropriate time and space scales, realities acknowledged by Cushing himself in his update
of the hypothesis (Cushing 1990).
An important feature of the Cushing hypothesis was its removal of the restriction inherent
in Hjort's thesis that food-mediated mortality would be restricted to a brief 'critical' stage in lar-
val development (the transition from endogenous to exogenous feeding). Under the Cushing model
338
recruitment success became associated (at least in theory) with the abundance of food during the
entire period of larval development. One of the explicit corollaries of this thinking was the expecta-
tion that spawning in north temperate marine fishes would be adaptively linked, temporally, to the
annual spring (and in some cases fall) production cycle(s) in the sea. This corollary also determined
and directed much of the research into the link between ocean physics, primary and secondary
production, and the recruitment dynamics of fish populations.
Solid evidence of the importance of this link to recruitment has been elusive (Cushing 1990,
Leggett & DeBlois 1994). Two papers highlight the contribution of advances in the understanding
of physical/biological linkages in the ocean and the availability of more sophisticated sampling
technologies, in particular satellite remote sensing, to an understanding of the potential importance
of Cushing's ideas.
Mueter et at. (2006) utilized established relationships between the dynamics of the mixed layer
and the onset of primary production to develop a 35+-yr time series for the timing of the spring
bloom in the Bering Sea in an attempt to explain recruitment variation in walleye pollock (Theragra
chalcogramma). This indirect measure of the onset of spring primary production conformed closely
to the onset as determined from 6 yr of fluorescence data. The production series so developed was
then related to indices of walleye pollock survival over the same time interval. The indices were
expressed as the residuals from a Ricker stock recruitment model. Walleye pollock survival rates
were strongly and inversely related to the timing of the spring bloom dates, a relationship inter-
preted by the authors as evidence of the important role of the timing of the spring bloom in relation
to the timing of spawning as a determinant of larval survival and recruitment in this species. While
possibly a case of overinterpretation due to the use of indirect approximations of the independent
and dependent variables, the findings are nonetheless supportive of the Cushing hypothesis.
In a more direct and convincing study, Platt et at. (2003) employed satellite remote sensing to
determine the timing of the spring phytoplankton peak on the eastern Scotian Shelf. This they related
to peaks in the production of larval haddock. While their data series was short (8 yr) and was divided
into two distinct periods (1979-1981 and 1997-2001) their analyses revealed a strong relationship
(r2 = 0.89) between variation in recruitment and variation in the timing of the spring bloom.
Unresolved by both studies is the extent to which other components of the ecosystem, perhaps
themselves linked to and affected by physical attributes of the ecosystem that are co-related to the
timing of the spring bloom (predator abundance and diversity, temperature effects, etc.), might
influence the environment occupied by eggs and larvae (either positively or negatively) and the
extent to which this result can be generalized to other areas and other species.
In contrast to these findings , Mousseau et at. (1998), who examined the annual cycles of abun-
dance of fish larvae and their zooplankton prey in relation to the biomass and production of phyto-
plankton on the Scotian Shelf, discovered that the production of copepod nauplii and copepodites
was sustained throughout the year and that fish larvae specializing on copepod prey also occurred
year-round. This occurred notwithstanding the fact that the spring bloom of large phytoplankton,
normally assumed to form the basis of the food web for larval fishes, was restricted to February-
April. This year-round food availability was produced by a non-peak food web structured on the
large-microphage shunt of the microbial food web (small phytoplankton ｾ＠ appendicularians/
ｰｴ･ｲｯ､ｳｾ＠ fish larvae). Mousseau et at. (1998) concluded that the year·round presence of fish lar-
vae and the fact that several of their major prey items exploit the microbial food web challenges the
long-standing belief that the feeding of marine fish larvae depends primarily on the reproduction of
herbivorous calanoid copepods grazing the spring and autumn blooms of large phytoplankton.
De Figueiredo et at. (2005) provide further support for this link between larval feeding and the
large microphage shunt of the microbial food web. They found that Protozoa and appropriately sized
metazoan prey, previously largely ignored as potential food items, can contribute significantly to
the dietary and energy requirements of larval fish. They conclude that the inclusion of these dietary
339
Body size Stage duration Growth rate
Figure 4 Graphical representation of the 'bigger is better' (A), 'stage duration' (B) and 'growth-selective' (C)
hypotheses.
components into measures of the food resource available to larval fishes diminishes the validity
of the key assumption underlying the Cushing hypotheses- that is, when, at times other than the
spring bloom, food levels in the sea are limiting to larval growth and survival.
There is mounting evidence, as well, that at larger scales, water temperature may play a greater
role in mediating larval growth and survival than food availability (see Meekan et al. 2003, Takasuka
& Aoki 2006). This, too, raises the questions, what other components of the ecosystem (predator densi-
ties, types, sizes, feeding rates, etc.) are influenced by physical factors linked to the timing of the spring
bloom, and how do these ecosystem level interactions influence larval survival and recruitment?
A second corollary of the Cushing hypothesis is that larvae that experience superior feeding
conditions, by virtue of their association with areas/times of enhanced food abundance, should
exhibit faster growth and higher survival, leading ultimately to improved recruitment. This corol-
lary, the so-called 'growth-mortality ' hypothesis (Anderson 1988, Hare & Cowen 1997) is, in fact ,
comprised of three non-exclusive functional hypotheses: the 'bigger is better' hypothesis, the 'stage
duration' hypothesis and the 'growth-selective' hypothesis (Figure 4).
Underlying all three hypotheses is the general assumption that following the transition to exog-
enous feeding the risk of death to an individual will be inversely related to the quantity and quality
of food avai !able and, by extension, to rates of growth and development. The positive effect of high
growth and development rates on survival is generally believed to result from the rapid increase in
length and/or changes in behaviour related to development during this period that, in turn , differen-
tially influences the susceptibility of individual larvae to predation (reviewed in Litvak & Leggett
1992, Leggett & DeBlois 1994).
'Bigger is better' hypothesis

The 'bigger is better' hypothesis evolved , in large part, from the results of general models that
aggregate data at the species level (an approach criticized by Pepin & Miller (1993) for its distorting
effects when generalized to intraspecific studies) and , in part, from the results of laboratory studies
that showed larger larvae were less vulnerable to predation. However, as demonstrated by Litvak &
Leggett (1992) the experimental designs typically used in these studies to assess the relation ship
between size and vulnerability commonly compounded the effects of age and size by using larvae
of different ages to obtain the desired range of sizes investigated. Furthermore, most studies of the
effects of size and/or age failed to provide the predator with a choice of prey sizes/ages and there-
fore examined only the capture component of the predation act, whereas predation involves three
multiplicative probabilities: encounter, attack and capture (reviewed in Litvak & Leggett 1992).
Laboratory and in situ mesocosm experiments in which larvae of identical ages but different sizes
and of identical sizes but different ages were subjected to predation by both visual and non-visual
predators clearly illustrated this bias (Litvak & Leggett 1992). Contrary to the predictions of the big-
ger is better model, in predation trials involving experimental cohorts of larvae of identical age, but
340
possessed of a distribution of sizes, both non-visual Uellyfish) and visual (fish) predators consumed
disproportionately more larger larvae. And, when these predators were offered cohorts of larvae of
identical sizes but possessing a distribution of ages, older larvae were selectively consumed. This
also is contrary to expectation. Pepin et al. (1992) report similar findings . Bertram & Leggett (1994)
found no difference in predation risk when metamorphosing winter flounder (Pseudopleuronectes
americanus) of like age but different sizes and of like size but different ages were subjected to
predation by Crangon sp. The principal difference in all these experiments, relative to those from
which the bigger is better model was developed, is that the predators were offered a choice of larvae
of different sizes or ages upon which to prey, as would occur in nature.
As noted by Leggett & DeBlois (1994), the findings reported by Litvak & Leggett (1992) and
supported by Pepin et al. (1992) and Bertram & Leggett (1994) suggest that, contrary to predictions
of the bigger is better model, for individual members of a larval cohort being smaller at a given age
could, under some conditions, and at certain stages of development, confer a survival advantage.
This difference in perspective derives from an explicit recognition of the reality that, in nature,
individual larvae exist, and are preyed upon, as members of a population characterized by evolving
distributions of ages, sizes and sizes at age. Supporting field evidence is provided by the work of
Fortier & Quinonez-Velazquez (1998), who studied the hatch date frequency distributions and daily
growth rates of pollock and haddock larvae on the Scotian Shelf in 1992 and 1993. They found
that, in haddock, growth varied little over the hatching season and that there was no significant
relationship between growth and survival. In pollock, slow growth invariably resulted in low sur-
vival, but fast growth resulted in both low and high survival of individual daily cohorts. Fortier &
Quinonez-Velazquez (1998) concluded that fast growth was a contributing but insufficient condition
for enhanced survival and that for both species investigated, increased predation late in the hatch-
ing season could decouple growth and survival. It appears, therefore, that differences in individual
vulnerability to predation, and the population effects of this variability on recruitment, will be a
function of the evolving structure of the distributions of larval size, age, and size at age throughout
the larval period and of the predators' response to them . Clearly, many of the inferences initially
drawn from the bigger is better model require rethinking.
'Stage duration' hypothesis

The 'stage duration' hypothesis was advanced simultaneously by Houde (1987) and Chambers &
Leggett (1987). This model is founded on the observations that (I) variance in sizes at metamorpho-
sis in larval fishe s is lower than variance in sizes at intermediate ages between hatching and meta-
morphosis, thereby implying a 'target size' for metamorphosis and (2) the timing of metamorphosis
is more strongly related to the achievement of a target size rather than a target age (Chambers et al.
1988). Therefore, larvae that experience more favourable feeding conditions and grow more quickly
should develop more rapidly and achieve metamorphosis at earlier ages. The stage duration hypoth-
esis predicts that, as a consequence, faster-growing larvae should experience lower cumulative mor-
tality during the larval stage, during which mortality rates are known to be very high . Simulation
studies of the potential impact of the reduced time to metamorphosis resulting from accelerated
growth indicate that resulting survival could be increased up to 100-fold by rapid growth (Chambers
& Leggett 1987, Houde 1989).
However, when Bertram (1993) incorporated the size-/age-specific mortality relationships iden-
tified by Litvak & Leggett (1992) and Pepin et al. (1992) into the stage-specific survival model in a
manner that recognized the combined probabilities of detection, attack and capture that character-
ize vulnerability to predation, he observed that the hypothesized positive effect of fast growth on
cumulative survival inherent in the stage-specific model was negated. Indeed the revised model
demonstrated that, in some cases, survival advantage went to slower-developing individuals. This
341
outcome is consistent with the experimental results reported by Litvak & Leggett ( 1992) and Pepin
et al. (1992), with the finding by Pepin et al. (2003) that wild, fast-growing larvae studied via high-
resolution in situ sampling experienced higher rates of mortality than did slower-growing larvae and
with the conclusion by Fortier & Quinonez-Velazquez (1998) that rapid growth and development is
a necessa ry, but not sufficient, condition for improved survival.
'Growth-selective ' hypothesis

The 'growth-selective' hypothesis derives principally from the work of Takasuka eta!. (2003), who
found that slower-growing larvae experienced higher rates of predatory losses independent of their
individual size at capture (hence the name 'growth-selective' hypothesis). Inherent in this hypoth-
esis is the assumption that the nutritional/physiological state of individual larvae may influence
their probability of capture (perhaps because of a reduced capacity to detect and/or avoid preda-
tory attacks) independent of size ('bigger is better') or developmental state ('stage duration'). Their
in situ analysis was conducted by comparing the size and growth rates of individual larvae recov-
ered from the guts of a suite of predators (as assessed through otolith analysis) with the distribution
of sizes in the larval prey field exploited by these predators. Significantly, they found evidence
of both negative and positive size-selective predation depending on the particular predator spe-
cies investigated. However, the combined effect of all predators was neutral. This finding helps to
explain the conflicting results of individual studies in which one or a small number of predators was
employed or studied.
A follow-up study (Takasuka eta!. 2004) provided further evidence of predator-specific growth-
selective mortality. Larval anchovy (Engraulis japonicus) having slower recent growth rates than
those in the population from which they were consumed (independent of size at capture), exhibited
higher predation losses when preyed on by juvenile conspecifics. However, predation by skipjack
tuna (Katsuwonus pelamis) on the same population of anchovy larvae produced no such growth-
selective mortality.
Fu im an et al. (2006) exam ined the presumed basis for growth-selective predation in a suite of
experiments involving larval red drum (Sciaenops ocellatus). These experiments were conducted
both in the laboratory and in in situ enclosures. They found that populations of larval red drum
consisting of 15 fast- and 15 slow-growing larvae of comparable size, when exposed to predation
and maintained in in situ enclosures, showed no evidence of growth-selective predation . This result
could, however, be a product of the particular predator used and is consistent with the findings of
Takasuka et al. (2004). Laboratory experiments involving larval red drum designed specifically to
evaluate the behavioural dynamics presumed to underlie growth-selective predation revealed no
evidence of a growth rate effect on performance in II survival skills. This outcome raises important
questions about the fundamental assumption of the growth-selective hypothesis.
The strong focus of research on the importa nce of size, growth rate and development rate as
determinants of survival reflected in these three hypotheses, and in the creative field and laboratory
experiments designed to assess them , has meaningfully advanced knowledge of the behaviour, ecol-
ogy and dynamics of the larval stage of fishes. To date, however, it has contributed only modestly
to the ultimate objective of a fuller understanding of recruitment processes in fishes. Like the Hjort
and Cushing hypotheses that preceded them, there may be a danger that this focus, if sustained at
the expense of other research directions could stall advances in the field by precluding a more holi s-
tic view of the factors regulating larval survival and recruitment. The hypothesis that larger larvae
should experience a survival advantage when subjected to predation is, for example, counter to the
predator-based hypothesis of optimal foraging that predicts predators will actively select larger prey
items from a prey field consisting of individuals of different sizes (Werner & Hall 1974, Charnov
1976, Litvak & Leggett 1992). Moreover, the underlying premi se that the processes inherent in
342
these growth-rel ated hypotheses are vital to recruitment continues to be built, in the main , on a
shaky foundation of correlation studies in which cause and effect are often conflated and/or con-
fused. For example Jenkins & King (2006) conclude, on the basis of correlation studies, that larval
growth in seagrass-associated fishes was important to post-larval abundance and interannual varia-
tion in recruitment. However, larval growth was also strong ly correlated to water temperature, and
water temperature was, in turn, strongly correlated with recruitment. An equally credible conclu-
sion might be that temperature had an influence, either directly or indirectly (see Frank & Leggett
1982, 1983), on survival independent of growth rates. In fairness to Jenkins & King (2006) some
consideration was given to other processes, including variable physical transport processes that
affected larvae differentially from year to year (of which variable sea-surface temperature could be
an indicator). However in this example, as in others (see, for example, Meekan et ai. 2003 , Takasuka
& Aoki 2006), the link between increased growth rates and enhanced survival and recruitment has
become almost axiomatic.
Paradigm 4: Environmentally based recruitment

models, when updated with new data, invariably fail
There is a long history of attempts to explain variation in recruitment based on the relationship
between some direct or indirect measure of year-class strength and environmental variables
(Cushing 1982). The most commonly used environmental variables have been temperature, salin-
ity and wind. These have been incorporated into exploratory correlation analyses that typically
use indices of year-class strength based on landings, catch per unit of effort, fishery-independent
scientific surveys, or model outputs based on reconstructed population sizes such as virtual popula-
tion analysis (VPA), as measures of recruitment. Unfortunately, estimation of year-class strengths
using these approaches is not a trivial problem and the resulting estimates can be misleading. Often
researchers have been forced to use commercial landings data or landings per unit of effort (e.g.,
Sutcliffe et ai. 1977), data sources that typically fail to conform to the key ass umption of time-
invariant fishing effort. Such data series have been distorted by technological developments that
change the relationship between a unit of effort and the resultant catch. More reliable data, derived
from fishery-independent surveys, are, unfortunately, scarce.
Temperature, because it regulates many physiological processes, has long been considered an
important explanatory variable of recruitment and has recently received growing attention in the
context of global warming (Cardinale & Hjelm 2006). One general pattern that has emerged is
that above-average temperatures are associated with better survival among stocks occupying the
northern limit of their distribution (Ottersen & Stenseth 2001). Salinity has frequently been used
as an indirect measure of nutrient flux, with higher-than-average salinity corresponding to elevated
nutrients. Sutcliffe et ai. (1983) found a positive correlation between cod recruitment and salinity
on the Newfoundland/Labrador shelves, which they assumed represented increased vertical mixing
that supported increased plankton production. The physical process by which wind may influence
recruitment is thought to be primarily through distributional effects on the egg and larval stages
(but wind-induced upwelling could also increase vertical mixing and plankton production). For
example, the larval stages of Pacific hake (Merluccius productus) appear to be negatively affected
by along-shelf winds that induce offshore Ekman transport to areas where survival is poor (Bailey
1981). Conversely, Atlantic menhaden (Brevoortia tyrannus) appear to benefit from both alongshore
and longshore wind-induced transport to coastal nursery grounds (Stegmann et ai. 1999). While
there is sufficient biological justification to consider these physical variables as important contribu-
tors to recruitment variability it should be noted that they are often selected due to their ease of
measurement and the long record of measurement- decades to centuries in some cases.
343
Unfortunately, this rationale makes it unlikely that such relationships will withstand the test
of time . Indeed, when updated with new data such relationships are prone to failure. In a compre-
hensive reexamination of over 60 published environment-recruitment correlation studies of marine
fish and invertebrates, Myers (1998) tested the performance of each using data accumulated sub-
sequent to the publication of the original relationship. In many cases the analysis applied to these
new data duplicated exactly the original. The overall result was disappointing. Most previously
published relationships failed when updated with new data. Interestingly, those correlations that
remained significant when retested generally occurred in populations close to the limits of the spe-
cies range. In northern waters this included Barents Sea cod, Baltic Sea cod, and Pacific herring
(Clupea pallasii). Recruitment in these species exhibited a consistently positive relationship with
temperature. At the southern limit of the range limits recruitment was typically negatively corre-
lated with temperature.
Insights into the possible causes of such latitudinally linked effects are provided by the work
of Fogarty et al. (2001), who examined the relative variability in recruitment of cod and haddock
stocks distributed throughout the north Atlantic. Recruitment variability was measured as the stan-
dard deviation of the residuals from a Ricker stock and recruitment relationship. Despite their close
taxonomic relationships, overlapping spawning times, and similar egg sizes, haddock stocks gen-
erally exhibited higher recruitment variability than cod in each of nine geographic .areas where
they co-occurred. Both stocks also exhibited higher variability at the extremes of their geographic
ranges (Barents Sea in the north and Georges Bank to the south; Figure 5).
The authors explain these species-specific differences on the basis of contrasting life-history
traits, physiological tolerances and population dynamic processes. For example, cod, which spawn
over a more extended time period than haddock, may thereby dampen the risk of extreme survival
outcomes (boom-bust) due to environmental variability. Laboratory studies (Laurence 1977) show
that cod larvae can withstand a much broader range of temperature and salinities than haddock,
implying that equivalent environmental forcing can be expected to have a lesser impact on growth
and survival of larvae of cod relative to haddock. The reduced temporal variability in recruitment
of cod relative to haddock also led Fogarty et al. (2001) to speculate that density-dependent mecha-
nisms, possibly cannibali sm, may be a more important process in cod. These species differences
r- o Cod
1.2 r-
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Figure 5 Variability in the long time series of recruitment data for cod and haddock showing that in every
region where the two species co-occur, haddock exhibit hi gher interannu al variability in recruitment, sugges-
tive of stronger environmental effects on hadd ock than on cod.
344
80 80
60 60
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9
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Figure 6 Spawning stock biomass (dark line), fishable biomass (dashed line) and exploitation rates (grey line)
for eastern Scotian She! f haddock.
have important implications for the management and potential recovery timescales of the two spe-
cies. For example, the formation of large year-classes at low levels of spawning stock may be more
common in haddock, thus serving to initiate the process of stock recovery. Evidence in support of
this possibility may be drawn from the study by Platt et al. (2003) of haddock larval survival in rela-
tion to spring bloom timing and the apparent recovery of the eastern Scotian Shelf haddock stock
following its collapse in the early 1990s (Figure 6).
Myers (1998) offers several statistical and analytical suggestions for improving the success of
future attempts to link environmental factors to recruitment variability. These include testing of
general hypotheses through the examination of several populations at once to detect general pat-
terns; employing data-splitting procedures- one portion for the exploratory analysis and the other
for testing; correcting for variation in spawner abundance (trends in recruitment may result from
changes in SSB).
Notwithstanding these inherent difficulties, such correlative approaches remain important
tools for identifying relationships worthy of more in-depth investigation through a combination
of laboratory and in situ studies and simulation modelling. Ultimately, however, the development
of recruitment models with 'staying power' will likely depend upon the acquisition of a greater
understanding of the biology of the species and of the behaviour of key elements of the physical
and biological environment occupied in support of the development and rigorous testing of a priori
hypotheses. This hypothesis-testing approach has been more common in freshwater than marine
systems (Magnuson 1988, Frank & Leggett 1994), in part because of the many logistic advantages
of working at smaller scales and in what are often less complex systems.
One of the few examples from the marine environment of a long-lasting environment/recruit-
ment model involves the demonstrated link between the frequency of onshore winds during the
period of residence of the larvae of capelin in the beach gravel where they are spawned and their
survival and recruitment (Leggett eta!. 1984). This model rests on the results of an extensive series
of field and laboratory investigations focused on the early life history of the species in eastern
Newfoundland waters. In the case of capelin, onshore winds produce a shoreward movement of
warmer, prey-rich waters that displace the cold, upwelled, predator-laden waters that typically dom-
inate the near shore during the capelin spawning season (Frank & Leggett 1982). A combination of
passive (wave-induced) and active (apparently temperature-induced) emergence from the spawning
gravel follows hatching. These cause the larvae to become entrained in a water mass rich in prey and
relatively poor in predators (Frank & Leggett 1982, 1985, Figure 7), thereby increasing the survival
probabilities of individual larvae (Frank & Leggett 1983). The frequency of these onshore wind
events and of the resulting emergence events is also key because survival time of larvae in the gravel
is limited to 3-4 days post-hatch - a time limit set by the rate of consumption of yolk reserves
345
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Quiescent Capelin Emerging Capelin
-Offshore Wind__. ...-Onshore Wind-
Figure 7 Dynamics of the nearshore environment influencing the larval stages of capelin and the resulting
impact on recruitment. The histogram shows onshore wind interval.
following hatching. In years when the frequency of onshore winds is high, survival is favoured.
When onshore winds are infrequent, survival is depressed.
During the period of larval hatching, the combined effects of water mass replacement creat-
ing favourable conditions for feeding, growth and survival coupled with short post-hatching beach
resident times result in increased larval survival and recruitment. The original model documenting
this relationship was based on capelin year-class data from 1966 to 1987 and from wind field data
that reflect variability in the atmospheric pressure systems that generate onshore winds over large
areas of Newfoundland's east coast. It explained nearly 60% of the interannual variation in year-
class strength in the eastern Newfoundland capelin stock (Leggett et al. 1984). Higher-than-average
water temperatures during the 6-month period of post-emergent pelagic drift also had a positive
effect on year-class strength. There is no documented biological basis for this added contribution
to explained variance. When retested with an additional 16 yr of data the model was found to be
robust (Carscadden et al. 2000). However, the added contribution to explained variance contrib-
uted by the incorporation of temperature during the post-emergent drift interval into the model no
longer prevailed- another example of a failed correlation based on purely exploratory correlative
assessments. This body of research provides an important counter-example to the paradigm that
346
environmentally based recruitment models invariably fail when updated with new data. It also illus-
trates the importance of a detailed understanding of the causative factors shaping the relationships
to the success of the approach .
Clearly variation in recruitment in marine fishes has an important environmental component.
However, understanding the nature of this component and the development of models that reliably
predict recruitment based on this knowledge remains in its infancy. Adjusting for the spawning
stock component in such models and accounting for other factors such as the size or age compo-
sition of the stock, physiological condition of the spawners, distributional changes, and adverse
effects associated with low population levels, so-called Allee effects (Liermann & Hilborn 2001)
are important next steps, as is the gaining of a deeper understanding of the underlying biological
and ecological drivers of the relationships that allow them to be fine-tuned in time and space.
The work of Ottersen et at. (2006) illustrates how the changing composition of the Barents Sea
cod spawning stock has actually strengthened the effect of the environment on recruitment. They
found that the magnitude of the correlation between cod year-class strength and depth-averaged water
temperatures during the period 1946-1999 increased from being relatively weak to strongly posi-
tive over time. The apparent mechanism behind this evolving relationship was the reduction in the
age and size composition of the stock, a change associated with an intensive, size-selective fishery.
It was speculated that this, in turn, may have resulted in differences in the timing, duration or loca-
tion of spawning, all of which have been demonstrated to be age or size dependent in other species.
This suggests that while a diverse age structure may effectively dampen the impact of environmental
variability on recruitment at both annual and interannual timescales, erosion of this age structure
may cause environmental effects to predominate. Such changes may help to explain, in part, the low
success rate of environmentally based models to reliably predict recruitment through time.
Paradigm 5: Populations cannot irreversibly collapse/

collapsed populations will recover in the absence of fishing
Until recently, thinking in the discipline and resulting management strategies were focused on the
idea that the compensatory dynamics inherent in stock recruitment models that form much of the
foundation for research into the population dynamics of marine fishes (Ricker, 1954, Beverton &
Holt 1957, Myers et at. 1995) would preclude irreversible population collapse, even under extreme
exploitation or highly variable recruitment. Both the Ricker and Beverton & Holt models incorpo-
rate a compensatory response that assumes increasing per capita reproductive success (recruits per
ad ult) as SSB declines to low levels. This leads naturally to the assumption that when fishing mor-
tality is reduced or eliminated, overfished stocks should recover to a stable equilibrium at relatively
high levels of SSB (Frank & Brickman 2000). This expectation was reinforced by the dramatic
resurgence of heavily exploited stocks during the virtual cessation of fishing in the north Atlantic,
North Sea and Baltic during WWII (Pope & Macer 1996). More recently, support for this paradigm
was provided by the rapid positive response of north-west Atlantic groundfish stocks following the
implementation of extended jurisdiction to 200 miles in Canadian Atlantic waters in 1978 and the
resulting reduction of fishing effort (Figure 8).
However, the lack of generality of this paradigm was brought into sharp focus in the early 1990s
when one of the largest cod stocks in the world collapsed (SSB declined by +99% relative to the
1960s) (Hutchings & Reynolds 2004) and then failed to respond to a moratorium on exploitation
that continues to this day (Figure 8). This phenomenon was repeated over the same time interval for
several other fish stocks within the north-west Atlantic (Choi et at. 2004, 2005).
While controversy regarding the primary cause of the collapse continues (Hutchings 1996, Rose
et at. 2000, Lilly et at. 2001) it is becoming clear that it was not the simple product of overfishing.
The popular analogy of the straw that broke the camel's back appears to apply in this case- the
347
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1950 1960 1970 1980 1990 2000 1950 1960 1970 1980 1990 2000 1950 1960 1970 1980 1990 2000
Figure 8 Spawning stock biomass (solid line) and landings (dashed line) of cod in nine areas in the north-west Atlantic. I, northern (Northwest
Atlantic Fisheries Organization Division 2J3KL); 2, northern Gulf of St. Lawrence; 3, southern Gulf of St. Lawrence; 4 , St. Pierre Bank; 5,
southern Grand Banks; 6, eastern Scotian Shelf; 7, Gulf of Maine; 8, western Scotian Shelf; 9, Georges Bank.
ﾷｾ＠ OD
., V>
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Cumulative depletion
(% of biomass removed)
Straw load
Figure 9 The last straw: time course of change in the biomass of northern cod (Northwest Atlantic Fisheries
Organization Division 2J3KL) in relation to cumulative exploitation.
argument is, in reality, about which of the many interacting factors constituted the proverbial straw
(Figure 9).
Clearly, overfishing was an issue. These populations were subjected to many decades of sus-
tained heavy exploitation, commonly two to four times the level of natural mortality, that resulted
in reductions in spawning biomass from 77% to 99% of the historical maximum (Myers et al. 1997).
However this reduction occurred without the collapse of the populations affected even though all
stocks exhibited growth overfishing (exploitation of individuals prior to age of maturity) and sub-
sequent recruitment overfishing (recruitment inadequate to replenish the SSB). Notwithstanding
repeated scientific advice to reduce fishing mortality, exploitation remained high until the collapse
occurred (Lilly et al. 2001). The collapse was immediately followed by an initial 2-yr moratorium
on fishing with the expectation , con sistent with the prevailing paradigm, that recovery would occur.
To date no such recovery has occurred notwithstanding repeated extensions of the fishing morato-
rium (Shelton & Healey 1999).
Changes in ocean climate clearly played a role in the collapse. The ocean climate on the
Labrador and Newfoundland shelves is determined by local winter atmospheric conditions that
form part of a larger-scale atmospheric pressure system known as the NAO or North Atlantic
Oscillation (Drinkwater 2002, 2006). The NAO is defined as the winter-time sea-surface pressure
difference between Iceland and the Azores. The relative strength of this difference varies annually.
Positive NAO values (associated with years when the Icelandic low deepens and the Azores high
349
increases) produce both an intensified latitudinal pressure gradient and westerly winds. Negative
NAO values (reflecting a weakening of these pressure systems) produce decreased westerly winds.
The 40+-yr time series of the NAO index exhibits strong decadal variability. Positive NAO years
are characterized by southward penetration of cold Arctic air masses, which produce greater ice
formation along the Newfoundland coast, within the Gulf of St. Lawrence, and along the eastern
Scotian Shelf (Figure 10). These cold, windy conditions also increase convective heat loss , produc-
ing below-normal water temperatures and increases in the volume of the cold intermediate layer
(Figure 10). Positive NAO years dominated the early 1970s and early 1980s and were particularly
pronounced during the late 1980s to mid-1990s, when cod stocks were collapsing throughout the
northern waters of the Canadian Atlantic region (Drinkwater 2002).
These intensified cold periods are believed to have contributed in fundamental ways to changes
in the growth rates, age and size at maturity and even the distribution of many species inhabiting
the cold intermediate layer. Recent examples of the effect on distribution include the southward
extension of Arctic cod from the Labrador Shelf to the southern Grand Banks off Newfoundland
and of capelin from the southern Grand Banks to the Scotian Shelf and beyond (Figure 11).
In general, growth rates, size at maturity and age at maturity in the areas affected by the NAO
declined (Choi et al. 2004, Olsen et al. 2005, Figure 3). A corresponding decrease in individual and
population fecundity (reproductive potential) presumably resulted. This coupled with a significant
reduction in age structure would render the populations more vulnerable to collapse.
In the case of cod the reasons for their failure to recover in the absence of fishing are now com-
ing to light (Frank et al. 2005). This failure is now known to be linked to the dominant position
that cod once occupied as top predator in the benthic food chain of the historical ecosystem and to
fundamental changes in the structure and energy flux in this ecosystem subsequent to their collapse
(Frank et al. 2005). The collapse of cod and the resulting reduction in the predation pressure they
exercised resulted in a massive increase in the biomass of small pelagic fish species and of benthic
macroinvertebrates, species that historically constituted their principal prey (Figure 12). These spe-
cies then became, in turn, important predatory regulators of the early life stages of their former gad-
oid predators (Frank et al. 2005, 2006). This negative feedback is believed to have exacerbated the
recruitment failure being experienced by cod (Swain & Sinclair 2000) and, together with the loss
of reproductive potential related to low water temperatures, reduced growth and reduced individual
fecundity at maturity (Choi et al. 2004), may have constituted the final straw in the demise of cod.
Several studies conducted since the collapse have now demonstrated that extensive delays in,
and/or failure of, the recovery of collapsed stocks are common. Hutchings & Reynolds (2004)
examined the evidence of the ability of 90 marine fish populations, representing 38 species and
11 families, to recover after collapse. They found recovery to be negatively associated with collapse
(r = -0.46, p < .000 1). Moreover, 41% of the 90 populations continued to decline 5 yr after collapse.
The magnitude of these population collapses was also negatively associated with recovery 10 and
15 yr after the declines. Only 12% of marine stocks (all of them clupeids) had exhibited full recov-
ery, while 40% (primarily gadoids, but some clupeids) had experienced no or very limited recovery
15 yr after collapse. Moreover, among 36 stocks in which exploitation rate declined after collapse,
and for which estimates of fishing mortality were available, population recovery was still highly
and negatively associated with the magnitude of the population decline (all populations, r = -0.63,
p < .0001; clupeids excluded, r = -0.79, p < .0001) over periods of 5 or 15 yr. Beverton (1990), in
his review of the collapse of 10 major fisheries for small pelagic marine species, notes that only
one stock (Icelandic summer spawning herring (Clupea harengus harengus)) had fully regained its
original size and that the Icelandic spring-spawning herring stock had failed to recover 20 yr since
it collapsed.
A major assumption, inherent in the formulation of the compensatory stock/recruitment mod-
els discussed, is that the curve representing the relationship between stock and recruitment passes
350
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Figure 10 Physical environmental changes from the Newfoundland Shelf and areas to the south illustrating
the backdrop against which many of the stocks were subjected during the past four decades. Note that all axes
except air temperature have been reversed to highlight the coherence of changes in the physical variables in
response to NAO forcing. (GSL =Gulf of St. Lawrence; SS =Scotian Shelf; CIL =Cold Intermediate Layers;
Stn. 27 = 30k east of St. John 's, Newfoundland.)
351
Post- 1985
55
50
45
ＴＰＧＭＭｾＭＬＭｾＭ｟ｊ＠ｾ＠
-75 - 70 -65 - 60 - 55 - 50 - 45 - 65 - 60 - 55 -50 - 45
Figure 11 Arctic cod range expansion based on scienti fie surveys conducted between 1970 and 1994. The
period post-1985 was a time of intense cooling and a resultant southward increase in the distribution of Arctic
cod. Dots show locations of positive catches (i.e., presence).
@0,------------------------------------------.
- Cod
----· Shrimp 1
-Shrimp2
--Shrimp 3
300 -Shrimp4
- Snow crab
'E
0
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1970 1975 1980 1985 1990 1995 2000
Figure 12 Changes in cod biom ass in the no rthern Gulf of St. Lawrence and associated changes in their
prey, namely, shrimp from four different areas and snow crab.
through the origin. This assumption underlies the expectation that populations should recover
from the relaxation of fishing, even when SSB has been driven to very low levels . The logical
necess ity that the relationship between parent stock size and recruitment pass through the origin
(i.e., without parents there can be no offspring) has probably done more harm than good in terms
of the management of commercial fisheries. This implies that the parent stock size can be driven
to very low levels without any permanent consequences, yet it is well known from other animal
populations that thresholds exist below which population recovery is imposs ible. These thresholds,
352
Non-zero intercept S-R model
20
ＰＫＭｾＬＮ＠
0 20 60 100 140
SSB
Figure 13 Schematic representation of the non-zero intercept stock recruitment model illustrating the basis
for the Allee effect. (SSB =spawning stock biomass.)
termed 'Allee effects' (Liermann & Hilborn 2001, Figure 13), result from a variety of behavioural
and physiological changes that occur as population densities decline.
Several recent examples demonstrate the existence of Allee effects in commercially exploited
marine species for which recruitment is inhibited below a parent population size well before the
zero intercept is reached (Shepherd & Partington 1995). In the case of southern Australian abalone
(Haliotis australis) which exhibits this effect, the underlying mechanism for this relatively seden-
tary species is believed to be density-dependent mating success, the probability of finding a mate
being the limiting factor when population size is low. Coho salmon (Oncorhynchus kisutch) also
exhibit an Allee effect (Chen et at. 2002). Another line of evidence in support of the existence of
Allee effects is given by a non-zero intercept model fitted to southern Grand Banks yellowtail floun-
der (Limandaferruginea) stock and recruitment data for the years 1968-1982. This model provided
a superior fit to the data compared to that obtained with a standard Ricker model (Figure 14A,B).
For yellowtail flounder a threshold SSB of 18 kilotonnes was indicated. Recruitment failure
would be expected to occur if biomass levels fall below this threshold. In this analysis the residual
pattern diverged between the two model fits, the magnitude of the residual variation being different
in nearly every year and in some years of opposite sign . Such differences have a profound impact on
any conclusions drawn from attempts to explain the residual variation based on the availability of
environmental data, a common practice as detailed above.
Increased awareness of the vulnerability of marine fish populations to irreversible collapses,
triggered by the collapse of north-west Atlantic cod, sparked an awareness of, and interest in, the
implications of the operation of Allee effects in the stock/recruitment dynamics of marine fishes
in general. A 2006 Institute for Scientific Information (lSI) search of all records linking the Allee
effect to fish revealed only 38 records, of which only 6 were published prior to 2000, the earliest
publication date being 1993, 3 yr after the collapse of cod. Because of the difficulty in detecting
these effects with the data currently available (Myers et al. 1995, Shelton & Healey 1999) most
attempts to understand its potential consequences have involved modelling (but see Hutchings 1996,
Marshall et at. 1999).
Frank & Brickman (2000) showed that biological reference points relative to stock recruitment
relationships for marine fishes that are developed using aggregated data from multiple stocks, a
common practice in conventional fisheries management and stock assessments, are likely to be inac-
curate and to obscure Allee effects. This finding and their observation that the extent and timescale
of recovery of collapsed stocks may depend on recolonization from adjacent substocks have, in turn,
fostered interest in the importance of stock structure and metapopulations in population stability,
collapse and recovery.
353
WILLIAM C. LEGGETT & KENN ETH T. FRANK
ＲＰＮＭｾ＠
A
•
160
ｾ＠
c
0
§ 120
5 •
c
§"' 80 •
5....
u
"'
c.:;
40
40 60
SSB ('000 ml)
120 B CJ 0, 0 • non-zero
Figure 14 Fitting of a non-zero intercept model versus the standard Ricker model (A) for yellowtail floun -
der on the southern Grand Banks (Northwest Atlantic Fisheries Organization Division 3NO). The result is a
better fit, estimation of a minimum spawning stock biomass (SSB) level, and a very different residual pattern
compared to the standard model (B).
Gruntfest et al. (1997) defined a metapopulation as a set of local populations connected by

migration in which the crucial feature is a low, often-random and density-dependent rate of move-
ment between patches. Thus the dynamics of local populations are largely, but importantly, not
completely independent. Dispersal between local populations has been shown to reduce the likeli-
hood of an Allee effect (Gascoigne & Lipcius 2004) and even a small a mount of interconnectivity
may be sufficient to reduce the risk of extinction/failure to recover for each of the subpopulations
involved (Hill et al. 2002). An important corollary is that habitat fragmentation that isolates local
subpopulations, such as those previously discussed on the various banks of the Scotian Shelf, or dra-
matic reductions in abundance, and thus the interconnectivity of local populations, can create Allee
effects (Cantrell et al. 2001). In metapopulations or in spatial populations consisting of demes, the
high costs of dispersal can induce the Allee effect, particularly when suitable habitats are separated
by uninhabitable areas (Hui & Li 2004).
Zhou & Wang (2004) developed a model that incorporated both a local population and a meta-
population. Their work indicates that a threshold exists below which the metapopulation goes extinct
as a direct consequence of the existence of Allee effects in the corresponding local populations.
They also observed that the threshold fraction of occupied patches needed by the metapopulation
354
to persist increases as the population size on occupied patches declines, and that as demographic
stochasticity in local populations increases in the presence of an Allee effect the risk of extinction
of the metapopulation increases, no matter how many patches are occupied initially.
Brassil (2001) reported that the magnitude of the Allee effect required to reduce the mean time
to extinction of a metapopulation by one half was on the order of 50 times lower than that required
to effect a similar reduction in the mean time to extinction of a single population. Moreover, ·as
rates of migration between subunits decreased, as might occur as local population density declines
(Frank 1992), the metapopulation became increasingly more sensitive to small changes in the mag-
nitude of the Allee effect.
The overall reduction in the size of local stocks and the progressive loss of spawning compo-
nents from north-west Atlantic cod demonstrates the unplanned, negative consequences of such an
aggregated management scale (Smedbol & Stephenson 2001). The rapid and unexpected collapse
of what might be termed the 'cod megapopulation' of the north-west Atlantic is a lso consistent with
the results and predictions of inquiries into the dynamics of Allee effects at the local and meta-
population levels.
Paradigm 6: Fish stocks can be managed in isolation

from their total environment
Typically fish stock assessments have ignored the complexities detailed above and have focused
principally on the intrinsic aspects of fish population dynamics and fishing as if the stock existed in
a simple vacuum . Such simplifications, once deemed necessary to tackle a very complex problem,
are no longer required given the evolving understanding of the broader ecosystem dynamics within
which individual populations operate.
For example, the consequences of the collapse of gadoid species in the north-west Atlantic have
now been shown to reach far beyond the interplay between the historically dominant predators and
their prey. Frank et al. (2005) documented a trophic cascade resulting from the collapse of cod that
encompassed all trophic levels and nutrients (Figure 15).
The correlation between the groundfish community time series and that of each subsequent
trophic level was negative for small pelagics (-0.61, n = 33), changed to positive for zooplankton
(0.63, n = 23), and then to negative for phytoplankton (-0.73, n = 23). The ecosystem restructuring
associated with this cascade has totally, and perhaps permanently, a ltered the dynamics of the area
thereby fulfilling the prophecy of Knowlton (2004) that "humans are well on their way to impact-
ing oceans as if they were merely a very large lake, with implications for a lternate stable states".
Traditionally only simple, small-scale, low-diversity ecosystems were considered susceptible to
such profound ecosystem restructuring. The dynamic ecosystem response to the collapse of cod is
the first demonstration of a trophic cascade in a large marine ecosystem.
This ecosystem restructuring to an alternate state may account for the failure of cod populations
to comply with the historical paradigm that predicts the recovery of depressed populations in the
absence of exploitation. The alternate state that now exists resulted from a complex suite of interact-
ing variables and led, in addition to increased predatory mortality on the early life stages of cod and
other demersa l species, to a suite of phenotypic changes that included smaller average body sizes,
reduced condition and reduced reproductive output in the gadoid species, all of which reduced the
potential for recovery along lines predicted by stock recruitment theory.
Capel in, too, have recently shown evidence of significant phenotypic changes, related to changes
in the ecosystem they occupy, that have altered the historical relationship between numerical abun-
dance and biomass. Beginning in the early 1990s, coincident with the collapse of cod, size at age
in capelin began to decline. In addition, acoustic surveys designed to assess the abundance of the
species became ineffective, in many cases failing to detect these typically pelagic species. Cod were
355
500 20 80 400
A =landings B =small fish
ｾ＠
=biomass c:Jsnow crab
400 c:::Jseals oshrimp
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I 95% C I
I 95% C I
ｾ＠
ｾ＠ 300
ｾ＠ｉｾ＠
"'""c:
ｾ＠
10
-;;; ., ""-;;; 40 Ｌｾ＠
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r+ r+ 5
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VJ
20 r+
ｉＡＧｾ＠
100
0
[I] rt 0 0 ｴｦｬｲｾ＠ lrf-1
0
200 400 2 800

c =large D ocolour Clnutrients I 95%C I
=small
r-r-
-t- 300 c:
150
r-r- I 95%C I 1.5 -- 600
ｾ＠
c:
0
ｾ＠
0
c: ｾ＠
c:
0 rh
g."' c:
"'
0.
c:
0
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N
100
50
rl- ｾ＠
200
100VJ
-;;;
0
N
E
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0.
ｾ＠
..c:
0..
0.5
r+-
200
0 0 0
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Pre -collapse Post-collapse
0
Figure 15 Trophic cascade on the eastern Scotian Shelf. Data the same as in Frank et al. (2005) but expressed
as means during the pre- and post-collapse periods of groundfish on the eastern Scotian Shelf. Cl, confidence
interval.
major predators of capelin. Following the collapse of cod, seals and seabirds became the dominant
predator of capelin. This shift in dominance from demersal to surface predators may have caused
capelin to move deeper in the water column (where they are more difficult to detect acoustically),
thereby displacing them from their zooplankton prey and resulting in reduced feeding and growth
rates. There is a growing interest in such non-lethal trophic effects (termed ' trait-mediated indirect
interactions') in which the presence of a predator in the environment influences the interaction
between two other species (prey and their resource) by altering a behavioural trait of the prey spe-
cies (Trussell et al. 2003). The slower seasonal growth rates experienced by capelin also led to later
and later spawning times (peaks in August as opposed to historical peaks in June; Carscadden et al.
1997). This shift in the timing of spawning may have negatively affected egg and larval survival
and, in turn , led to reduced recruitment success.
Paradigm 7: Recovery is synonymous with rebuilding

In those cases where recovery from depressed population numbers does occur, it is commonly
believed that the structure of the population, including substock structure, production attributes,
behavioural adaptations, and phenotypic makeup, will resemble the historical condition. Recent
evidence suggests that this may also be incorrect. For example, haddock populations in the north-
west Atlantic collapsed synchronously with cod but, unlike cod, have shown modest signs of recov-
ery during the fishing moratorium. This partial recovery was fuelled by the survivorship of strong
year-classes produced in 1998 and 1999, leading to strong numerical abundances of this species.
However, biomass levels remain well below the historical at these levels of numerical abundance
(Figure 16).
356
1.2
q 0.8
ｾ＠ 0
E
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i:i5
0
1970 1975 1980 1985 1990 1995 2000 2005
Figure 16 Total mortality, weight at age, length and 50% maturity and index of condition from two surveys
for eastern Scotian Shelf haddock. (Bottom panel is the same as Figure 6.)
This reduced biomass results from major changes in the phenotypic characteristics of the recov-
ered stocks, some of which may have a genetic basis. Haddock now mature at smaller sizes and
younger ages, exhibit lower weights at age (implying reduced growth) and experience increased
natural mortality that is now approximately double (M = 0.2-0.4) the precollapse levels Thus, in the
traditional sense of the word, while these stocks have recovered numerically they have not rebuilt.
Conclusion
This review has attempted to provide the reader with a critical but objective insight into the evolu-
tion and current status of seven paradigms that have had a major influence on the development of
the science of fisheries oceanography over the past century. Many remain central to the field but are,
as should be the case, continuing to evolve as new information becomes available and new insights
are drawn from this information.
357
One of the central themes of the review is that nothing is ever as simple as it seems, and that too
rigid an adherence to a hypothesis that is intuitively appealing can, if not continuously challenged,
dampen the creativity of thought and action that is necessary to advance the discipline. The main-
tenance of an open, critical and creative dialogue, unpopular and uncomfortable as this can be both
for proponents of a theory and for those who challenge, is vital to the advancement of the field.
A second theme is that the dynamics of the systems and phenomena we seek to understand
are invariably more complex than initially meets the eye. It is becoming more and more evident
that even what appear to be simple systems and system responses are shaped in complex ways by
the ecosystem of which they are a part. This requires that we be more holistic in our thinking and
more comprehensive in our studies. Ecosystems rather than individual s or populations are rapidly
becoming the object of study as the search for solutions to traditional problems such as recruitment
dynamics are pursued.
Fortuitously, advances in the technologies and methodologies necessary to approach the disci-
pline from this perspective are occurring at a rapid pace, as is the ability of the current and upcom-
ing generation of physical, chemical and biological oceanographers and marine ecologists to speak
one another's language with sufficient fluency to create the synergy that is clearly required to be
effective at this level of inquiry. This is, perhaps, one of the greatest advances in the discipline in
recent decades. No aspirant to the profession should ignore this reality.
Finally, this need to think in ecosystem-level terms and to conduct effective research at this
scale bring into focus, once again , the value of large-scale monitoring programmes that provide the
high-quality decadal and longer timescale databases essential to advances in the discipline. Satellite
imagery and in situ remote sensing are now contributing remarkable new insights at the ecosystem
level and will become increasingly important in the future. And the assembly and ease of acces-
sibility of large-scale databases deriving from monitoring and process-oriented studies around the
world are proving to be powerful in advancing the discipline. However, the requirement for ships
at sea in support of skillfully designed sampling programmes executed to provide both decadal
and longer-scale insights into the dynamics of key aspects of large-scale ecosystems and to support
process-based investigations of the operational basis of these dynamics has never been greater. One
need only look to the contributions of initiatives such as the Continuous Plankton Recorder pro-
gramme administered by the Sir Alister Hardy Foundation for the Ocean Sciences, the California
Cooperative Oceanic Fisheries Investigation , annual bottom trawl surveys such those administered
by the Department of Fisheries and Oceans in Canada, the National Marine Fisheries Service in the
United States, and by International Council for the Exploration of the Sea (ICES) member natio ns in
Europe to recent advances in the discipline to understand this reality. This may not be the glamor-
ous science that garners competitive grant monies, but without it the contribution of those monies to
the understanding and solution of problems that have taken on enormous worldwide importance in
this time of global climate change will be increasingly at risk.
Acknowledgements
This work was supported by Discovery grants from the Natural Sciences and Engineering Research
Council of Canada to W.C. Leggett and to K.T. Frank and by Fisheries and Oceans Canada, Ocean
Sciences Division. We thank Liam Petrie for his assistance in producing the figures.
References
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363
AUTHOR INDEX
References to complete articles are given in bold type, references to bibliographi c lists are in regular type.
Almeida, P.R. See More ira , F. , 101

A
Amara , R., 94, 236
Abbott, O.J., 94 Ambrose, R.F. , 186
Abdallah, M. See Khalaf, M.A., 288 Amiard, J.C. See Mouney rac, C., 245
Abe, 0 . See Shibuno, T., 294 See Ra inbow, P.S., 247
Abele, D. See Fab ricius, K.E ., 56 Amiard-Triquet, C. See Mouneyrac, C., 245
Abelmoschi , M. See Grotti, M., 326 See Ra inbow, P.S ., 247
Abelson, A., 53 Amsler, C.D., 53
Aberle, N. See Sommer, U., 200 Andel ma n, S. See Roberts, C.M., 293
Able, KW. See Gillanders, B.M. , 326 Anderson, D.R. See Brow nie, C. , 324
See Martei nsdotti r, G., 244 Anderson, J.T. , 358
Ackerly, D.D. See Moles, A.T., 245 Anderson, P., 236
Ackerman, J.L. See Bellwood, D.R., 283 Anderso n, T.J. , 186
Ackerson, MV. See Colmers, W.F., 189 Anderson, T.R. See Fasham, M.J.R. , 20
Adam, W. , 186 Andersson , J.E.C. , 283
Adams, P.M ., 186 Andre, C. See Hedqvist-Johnson , K., 98
Addison, J.T., 94 Andrews, J.C. See Sammarco, P.W. , 62
Aderjoud, M. See Cadoret, L., 284 Anger, K. See Cria les, M.M ., 96
Adey, W.H . See Carpenter, R.C ., 55 See Gimenez, L., 240
See McConnaug hey, T.A ., 59 Anggoro, A.W. See Baird, A.H., 283
Adge r, W.N., 283 Anonymous, 94
Adjeroud , M. See Pen in, L., 292 Ansell , A.D., 95
Adlandsvik , B. See Ma rsha ll C.T., 361 See Pinn , E.H ., 101
Aedo, D. See Santelic ies, B., 248 Anteweberhan, M. See McClanahan, T.R., 290
Agosta , S.J. See Bern ardo, J., 237 Anthony, K.R.N ., 53
Ag rawa l, A.A ., 235 See Hooge nboo m, M.O., 57
Ahlgren , G. , 19 See Orpin , A.R ., 292
Ahn , C.Y., 19 Antunes, C. See Correia, A.T. , 325
AI-Adhub, A.H.Y., 94 Aoki, I. See Takasuka , A. , 363
Albal adejo, V.D. See Carpenter, K.E., 284 Aoki, K. See Miyazaki , T., 195
Albergo ni , V. See Packard , A., 197 Aoki, M ., 236
Alder, S. See De Fra ipont , M., 238 Apte, S.C. See Hatj e, V. , 327
Alford, R.A. See Dzimin sk i, M.A ., 239 Arai, N. See Ikeda, Y., 193
See Willi ams, Y.M., 296 Arai, R. See Karin o, K., 242
Allan , J. See Le Souef. A.S., 194 Arai , T. , 324
Allcock, A.L. , 186 See Kotake, A., 243
See Barratt, l.M ., 186 Arakawa, K .Y., 186
Alle n, B.J. See Lev into n, J.S ., 243 Araki , A. See Sakaguchi, H., 199
Allen, G.R., 283 Archer, D. See Kleypas, J.A. , 288
See Ollerton, J., 292 Arditi , N. See Gruntfest Y., 360
See Randall , J.E., 293 Arias, A.M. See Drake, P., 97
See Roberts, C.M ., 293 Arias-Gonzalez, J.E . See Mumby, P.J., 291
Allen, J.D., 235 Aristotle, 186
See Mo ra n, A.L. , 245 Arm stro ng, B. See Floros. C. D., 285
Allen, M. See Allen , G.R., 283 Armstrong, K.M . See Ostrander, G.K., 61
Allen, R.M., 235 See Ostrander, G.K ., 292
See Marshall, D.J ., 203-250 Armstrong, R.A ., 19
Almansa, E. See Marquez, L., 194 Armswo rth , P.R., 236
See Quintana, D., 198 Amason, A.N. See Schwarz, C.J. , 329
AI ma ny, G.R., 283 Arnold, G.P., 95
See Feary, D. A., 285 Arnold , J.M. , 186
See Jo nes , G . P. , 288 Arntz, W. See Fernandez, M., 240
365
AUTHOR INDEX
Aro, E. See Hinrick sen, H.-H ., 360 Barbieri, L.R. See Lowerre-Barbieri, S.K., 361
Aronson, R.B., 186, 283 Barimo, J. See Miller, M.W., 60
Arraigada, S. See Gonza lez, M.L., 191 Barkman, R.C. See Bengtson, D.A., 236
Arronte, J.C. See Carrasco, J.F., 188 Bark mann , W. See Woods, J., 23
Arthur, R., 283 Barnes, D.J ., 54
Assis, C.A. See Moreira, F., 101 Barnes, H., 236
Aston, S.R., 324 Barnes, M. See Barnes, H., 236
Ateweberhan, M. See McClanahan , T.R., 290 Baron, N. See Pandolfi, J.M., 61
Attrill, M.J., 95 Barratt, I.M., 186
Auby, I. See Pampoulie, C., 246 Barrowman, N.J. See Myers, R.A., 362
Augustine, 0. See Tranter, D.J., 200 Barshis, D. See Smith, L.W., 294
Au mont, 0. See Orr, J.C., 292 Bartol, I.K., 186
Ay6n, P. See Lett, C., 361 Bateman, A.J., 236
Ay re, D.J., 283 Bates, S.S. See Fehling, J., 20
Bath, G.E., 324
Batham, E.J., 186
B Batson, J.N. See Miller, M.B., 328
Bayle-Sempere, J. See Gillanders, B.M., 326
Baba, M. See Morse, A.N.C., 60 Bayne, B.L., 236
Babaluk, J.A. See Halden, N.M., 326 Baynes, S.M., 236
Babcock, R., 53 Beach, K.S. See Kuffner, I.B., 59
See Mundy, C., 60 Beames, R.M ., See Ennevor, B.C., 325
See Oliver, J., 61 Beaumont, A.R., 95
Babcock, R.C. See Mundy, C.N., 60 See Hoare, K., 241
See Poloczanska, E.S., 292 Beaumont, L.J. See Thomas, C. D., 294
Bachelet, G., 95 Beaunier, P. See Mouneyrac , C., 245
Baden, S.P., 95 Becerro, M.A ., 54
Baeta, M. See Villanueva, R. , 201 See Kuffner, I. B., 58
Baeza, J.A., 236 Becker, B.J., 236
Bagenal, T.B., 236 Becker, H.B. See Boddeke, R., 96
Bailey, K.M., 358 Becker, P.H. See Walter, U., 104
See Werner, E., 363 Beckerman, A.P., 236
Baird, A.H., 54, 283 Beebee, T.J.C. See Walther, G.R., 295
See Hughes, T.P. , 57, 88 Beets, J.P. See Hixon, M.A., 287
See Markey, K.L. , 59 Beger, M., 283
See Marshall, P.A., 290 Begg, G.A ., 324
See McClanahan , T.R., 290 See Scott, B.E., 363
See Pratchett, M.S., 293 Begon, M. See Parker, G.A., 246
Baird, M.E., 19 Behr, P.J. See Valiela, I. , 62
Bairlein, F. See Walthe r, G.R., 295 Bell , J. See Koslow, J.A. , 243
Bak, R.P.M. , 54 Bell , J.D. , 283
See Epstein , N., 56 Be ll , M.C., 236
See Nugues, M.M., 60, 61 Be llo, G ., 186
See Yermeij, M.J.A. , 63 Bellwood, D.R., 54, 283
Baker, A.C., 283 See Hughes, T.P., 57, 58, 288
See McClanahan , T.R. , 290 See Mantyka, C.S ., 289
Bakken, M. See Erik sen, M.S., 239 See Pratchett, M.S ., 251-296
Bakkenes, M. See Thomas, C.D., 294 See Wil so n, S.K., 296
Baklouti, M., 19 Bengtson, D.A., 236
Balazs, G.H. See Parker, D.M., 197 Bengtssson, J. See Elmqvist, T., 285
Balch, N. See O'Dor, R.K ., 196 Ben kendorff, K., 236
Baldo, F. See Drake, P., 97 Bennett, A.A. See Hobbs, J.A., 327
Balguerfas, E., 186 Bennett, C. E., 236
Baltazar, P., 186 Bennett, D.B. See Naylor, J.K., 246
Banaigs, B. See Lecchini, D., 289 Bennett, P.M. See Owens, I.P.F., 292
Banks, S.A., 54 Bennett, W.A . See Tiffany, B.N., 200
Bannister, T.T. See Laws, E. A., 22 Benton, M.J., 283
Banse, K., 19 Benton, T.G. See Beckerman, A.P., 236
Barber, Y.C. See Budelmann, B.U., 188 See Plaistow, S.J., 247
366
AUTHOR INDEX
Beretta, G.A . See Booth , D.J ., 284 Bl ax te r, J.H.S., 186

Berger, S. See Wa lther, G. R., 295 Bleckma nn , H., 186
Berger, W.H. See Jackson, J.B.C., 58, 288 See Budelma nn , B. U., 188
Bergey, E.A ., 54 Bl ouw, D.M. See Heath , D.O., 241
Be rgha hn, R., 95 Blum, J.D. See Kennedy, B.P., 327
Berglund , A., 236 Bobak , M . See Sra m, R.J ., 249
See Kolm , N., 289 Bock, C . See Ferna ndez, M ., 239
Berg ma n, K. See McC la na han, T.R., 290 Boddeke, R.,95,96
Bergma n, M.J .N., 95 Boehler!, G.W., 96
See Va n der Vee r, H.W., 103 Boersma, P.O., 284
Bergsten, J. See Brod in, T. , 237 Boetti ger, C. A. See Bergey, E.A., 54
Berke ley, S.A., 236, 359 Bolanos, A. See Quinta na, D., 198
Berke l ma ns, R., 54, 283 Bolch, C .J. See Fehling, J., 20
Bern , H.A. See Nishioka, R.S., 196 Bolet zky, S.v., 186, 187
Bern ard, 0., 19 See Bu delm a nn , B.U., 188
Bern ardo, J. , 237 See Ha nlon, R.T. , 192
Bernet, P. See Berglund, A., 236 See Ma ngold , K., 194
Berrien, P. See Steg mann , P.M, 363 See Ma ngold-Wirz, K., 194
Berry, S.S., 186 See Ove rath , H. , 197
Berry, W.J. See Bengtson, D.A., 236 See Villa nueva, R., 201
Bersa no, J.G.F. See Igles ias, J., 193 Bolitho, E.E., See Willi a ms, S.E., 296
Bert ness, M.D., 237 Bolton, T.F. See Marsha ll, D.J., 244
See Trussell , G.C., 363 Bond, T. See C i n ne r, J. , 285
Bertra m, D.F., 237, 359 Bonduri a nsky, R. See Ma rsha ll , D.J., 244
Bertra nd, E. M., 19 Bon hom me, F. See Boudry, P., 237
Berumen, M.L., 283, 284 Bonito, V. See Becerro, M .A., 54
See Pratchell, M.S., 293 Bonsdorff, E., 96
Berz, G. See Hende rson-Se lle rs, A., 287 Booth , D.J. , 284
Beukema, J.J., 95 Booth , D.T., 237
See Philippart, C .J.M., 101 See Burgess, E.A., 237
Beukers, J. S., 284 Bopp, L. See Orr, J.C., 292
Beverton, R.J H. , 359 Borchardt , M.A., 19
Beyst, B., 95 Borcha rdt, T. See Da hl , K., 97
Bhasin , H. See Stone, L., 294 Bos, O.G . See Philippa rt , C. J.M ., 101
Bidder, A. M. See Ma ngold , K., 194 Bosch, 1., 237
Bi dwell , J. P. See Ha n ion, R.T., 192 Bossc hiete r, J.R. See Boddeke, R., 96
Bierman n, C. H., 237 Botsford, L.W. See Hill , M.F., 360
Bi gelow, K.A. See Bower, J.R ., 187 See Jackso n, J. B.C., 58, 288
Bi gg, G. R. See Rohling, E.J ., 329 See O'Fa rre ll, M.R., 246
Bijo ux, J.P. See Graha m, N. A.J ., 286 Bo ucaud -Ca mo u, E., 187
Bil derback, D. See Limbu rg, K.E., 327 See Vill a nueva, R., 20 1
Bin gha m, B.L., 237 Bo uchaud, 0., 187
Binkova, B.B. See Sram, R.J ., 249 Boucherea u, J.L . See Pa mpoulie, C. , 246
Birch, G.F. See Hatj e, V. , 327 Boucher-Rodoni , R. See Boucaud -Ca mou , E., 187
Birke la nd, C.. 54, 237 See No rma n, M.D., 196
See Smith , L.W., 294 See O' Dor, R.K., 196
Birrell , C. L. , 25-63, 54 Bouchon, C., 54
Bisazza, A. See Berglund, A., 236 See Bo uchon-Nava ro, Y. , 284
Bizikov, V. A., 186 Bouchon-Navaro, Y. , 284
Bjornda l, K.A. See Jac kso n, J.B .C., 58 See Har melin-Vi vie n, M.L., 287
See Pandolfi , J.M ., 292 Boud ry, P., 237
Bl aber, S.J.M. See Milton, D.A. , 328 Boull e, D.P. See Jen nings, S., 288
Bl acka ll , L.L. See We bster, N.S., 63 Bo urque, B.J. See Jackso n, J.B .C., 58
Bl ackwell , P.G. See Mumby, P.J. , 60 See Jackso n, J.B .C., 288
See Mumby, P.J ., 29 1 Bou xin, J., 187
Bl anc ha rd, T. See C hesney, E.J., 325 Bowen, K.G. See Fogarty, M.J. , 360
Bl a nton, B.O . See Stegma nn, P.M. 363 Bowe r, J.R., 187
Blasco, D., 19 Box, S. See Mumby, P.J ., 29 1
Blauste in , A.R. See Kiesec ke r, J.M., 242 Box, S.J., 54
367
AUTHOR INDEX
Boyd, A.J., 359 Brown, P. , 324

Boyd, P.W. See Fasham, M.J.R., 20 Brownie, C., 324
Boyle, M.J. See Hughes, T.P. , 57 Bruggemann, J.H. See McClanahan, T.R., 290
Boyle, P.R., 187 Bruland, K.W. See Roitz, J.S ., 329
See Co ll ins, M.A., 189 Brumbaugh, D.R. See Mumby, P.J., 60, 291
See Gowland, F.C., 191 Bruno, J.F., 54
See Grisley, M.S., 191 Brusca, G.J. See Brusca, R.C., 96
See Key, L.N., 193 Brusca, R.C. , 96
Bozec, Y.M ., 284 Bryant, D., 55
See Kulbicki, M., 289 Bryden, C.A. See Heath, D.D., 241
Braastad, B.O. See Eriksen, M.S ., 239 Buch, K. See Mumby, P.J., 291
Brabant, J.C. See Van Marlen, B., 104 Buchan, P.R . See Smale, M.J., 199
Bradbury, R.H. See Hoegh-Guldberg, 0., 57 Buckley, L.J., 237
See Jackson, J.B.C., 58, 288 Buckley, R. See Downing, N., 285
See Pandolfi, J.M., 61, 292 Buckley, Y.M. , 237
Bradford, R.G., 237 See Allen, R.M., 235
Bradshaw, C. See Sheppard, C .R.C., 294 Buddemeier, R.W. See Kleypas, J.A., 288, 289
Bragg, W.L., 324 See Smith, S.V., 294
Brakefield, P.M . See Fischer, K., 240 Budelmann, B.U., 187, 188
Brana, F. See Nicieza, A.G., 101 See Bleckmann , H., 186
Branch, G . See Roberts, C.M., 293 Bull , G.D. See Wallace, C.C., 63
Branch, G.M. See Riegl, B., 61 Bullock, T.H. See Bleckmann, H., 186
Brand, U. See Hoffman, D.K., 57 BUIIow, B.v., 188
Brander K.M. See Symonds, D.J., 103 Bulnheim, H.P., 96
Brante, A. See Fernandez, M., 239 Bunkley-Williams, L. See Williams, E.H . Jr, 296
Brassil, C.E., 359 Burgess, E.A., 237
Bralley, J. See Campana, S.E., 324 Burke, L. See Bryant, D., 55
See Lilly, G.R., 361 See Cesar, H., 284
See Olsen, E.M., 246 Burnham, K.P. See Brownie, C., 324
See Olsen, E.M., 362 Burns, B.R. See Buckley, L.J ., 237
Breitbart, M. See Kline, D. I., 58 Burrows, M.T. See Gibson, R.N., 98
Brenkman, S.J., 324 Burton, J. See Hobbs, J.A., 327
Brickman, D., 359 Buskey, E.J. See Liu, H., 22
See Frank, K.T., 360 Bussiere, L.F. See Marshall, D.J., 244
Bridges, T.S ., 237 Bustamante, P., 188
Brierley, A.S. See Jennings, S., 288 See Seixas, S., 199
Brink, L. See Shanks, A.L., 199 See Villanueva, R., 201
Broad, K . See Mumby, P.J., 291 Bustamante, R.H. See Roberts, C.M., 293
Brocco, S.L., 187 Bustos-Obregon, E. See Gutierrez-Pajares, J.L., 191
Brock, R.E., 54 Butler, A. See Poloczanska, E.S., 292
See Smith, S.V., 62 Butler, T.H., 96
Brockelman, W.Y., 237 Buuon , D.K., 19
Brockman, H.J. See Seger, J. , 248 Buuy, J.S., 188
Broderick, A.C. See Godley, B.J., 240 Buzeta, M.-1. See Waiwood, K.G., 363
Brodin, T., 237 Byrne, M. , 237
Broekema, M.M.M., 96 Byrne, R.A. See Meisel, D.V., 195
Broekhuysen, G.J., 96 Bythell , J.C. See Ledlie, M.H., 289
Bromley, P.J. See Daan, N., 97
Brooks, A.J. See Holbrook, S.J., 287
Brophy, D., 324
Brough, E.J., 187
c
Brower, K., 187 Cabral, H. See Gam ito, R. , 97
Brown, B.E., 284 Cabral, H.N., 96
Brown, E.K. See Storlazzi, C. D., 62 Cadee, G.C. See Philippart, C.J.M., 101
Brown, E.R ., 187 Cadigan, N.G. See Lilly, G.R., 361
Brown, J.A. See Chambers, R.C., 359 Cadiz, P. See Raymundo, L.J ., 61
See Gillanders, B.M., 326 Cadoret, L., 284
Brown, J.H., 284 Cahu, C.L. See Zambonino-lnfante, J.L. , 202
See Savage, V.M., 23 Caldarone, E.M. See Buckley, L.J. , 237
368
AUTHOR INDEX
Caldeira, K, See Hoeg h-Guldberg, 0., 57 Castille, F.L., 188

Calderon , R. See Fernandez, M. , 239 Castro, B.G. See Cortez T. , 189
Caley, M.J. , 237, 284 Castro, J.J. See Hernandez-Ga rcia , V., 192
See Jones, G.P. , 288 Castro-Fuentes, H., 188
See Munday, P.L. , 291 Castro-Hernandez, J.J. See Hernandez-Lopez, J.L., 192
See Ohman, M.C. , 291 Cattrij sse, A., 96
Calvo, A. See Pelejero, C., 292 Caveriviere, A., 188
Cameron, A. See Thomas, C. D., 294 See Diallo, M. , 189
Cameron, A.M. See Fearon, R.J ., 56 See Jouffre, D., 193
Cameron, E.Z., 237 Ceccarelli , D. See Hughes, T.P., 58, 288
Campana, S.E. 324, 325 Ceccarelli , D.M., 55
See Bath, G.E., 324 Cech, J.J. See Roessig, J.M., 293
See Begg, G.A., 324 Cech , J.J. Jr. See Solomon, C.T., 329
See Elsdon, T.S. , 297-330 Cerra, A. See Byrne, M. , 237
See Farrell, J., 326 Cesar, H., 284
See Fowler, A.J., 326 See Ngazy, Z. 291
See Secor, D. H., 329 See Westmacott , S., 295
Thorrold, S.R., 330 Cesar, H.S.J. See Grandcourt, E.M., 286
Campbell, A.C. See Payne, A.G., 246 Chaffee, C., 238
Campbell , J. 1.. See Halden, N.M. , 326 See Strathmann, R.R. , 249
See Campana, S.E., 325 Chalke r, B. E. See Barnes, D.J., 54
Campbell, S. See Baird, A.H., 283 See Oliver, J.K., 61
Camphuysen, K. See Garthe, S., 98 Chamberlain, C.P. See Kennedy, B.P., 327
Campos, J., 65-104 Chambers, R.C., 238, 359
See Freitas, V., 97 Chan, L.H. See Chesney, E.J., 325
Cantrell, R.S ., 359 See Li, Y.H ., 327
Caperon, J. , 19 Chan , T.T.C., 284
Capinera, J.L., 238 Chang, H. See Webster, P.J., 295
Capone, D.G. See Ku stka, A. , 22 Chaparro, O.R., 238
Caputi, N. See Edmonds , J.S., 325 Chapman, C., See Berkeley, S.A., 236, 359
Card, M. See Hu ghes, T.P., 57, 288 Chapman, M.R ., 284
Cardina le, M., 359 Charnov, E.L., 359
Cardoso, J.F.M .F., 96 See Savage, V.M., 23
See Va n der Veer, H.W., 103 Cheal, A.J., 284
See Meekan, M.G., 362 See Halford, A., 287
See Sammarco, P.W., 62 Chen, D.G., 359
Carloni , F. See Hal sband-Lenk, C., 241 Chen , D.S., 188
Carlton , J.T., 284 Chenery, S.R. See Milton, D.A., 328
Carpenter, E.J . See Kustka, A. , 22 Cherel , Y. See Potier, M. , 198
Ca rpenter, K.E., 284 Chernoff, H. See Keough, M.J., 242
Carpenter, R.C., 55 Cheroske, A.G., 55
See Cheroske, A.G ., 55 Chesney, E.J., 325
See Edmunds , P.J. , 56 Chester, C.M., 238
Ca rpenter, S. See Fo lke, C. , 56 Chia, F.S. See Qian, P.Y., 247
Carpenter, S.R. See Adger, W.N., 283 Chin , A. See Diaz- Pulido, G., 55
Carr, M.H. See Caley, M.J ., 237 Chittaro, P.M., 55
See Shanks, A.L., 248 Cho, J .Y. See Kim, J. , 58
Carrasco, J.F., 188 Choat, J.H ., 284, 285
See Igle sias, J ., 193 See Bellwood, D.R., 54, 283
Carruthers, E. H., 359 See Crossman, D.J., 285
Carruthers, J.N., 359 See Wilson , S.K., 296
Carscadden , J.E., 359 Choi, J.S., 359
See Leggett, W.C., 361 See Frank, K.T. , 360
Case, J.F. See Fleisher, K.J., 190 See Kim, J., 58
Caselle, J.E. See Swearer, S.E., 249, 329 Chouinard, G.A. See Campana, S.E., 324
Casey, K.S. See Bruno, J.F. , 54 See Hanson , J.M. , 360
Cass, A.J. See Chen D.G., 359 Christensen, R.J. See Eyring, C. F. , 190
Castilla, J.C. See Lardies, M.A ., 243 Christoffersen, J. See Niel son, A. E. , 328
See Roberts, C.M ., 293 Christoffersen, M.L. , 96
369
AUTHOR INDEX
Chun, B.S. See Kim, J., 58 Conway, H.L., 19

Chun, C., 188 See Harri son, P.J., 2 1
Chung, A.S. See Ahn , C.Y., 19 Cook, C.N. See Marshall, D.J., 244
Ciechomski, J.D., 238 Cooke, R. See Jackso n, J.B.C. , 58
Cifuentes, M. See Fernandez, M., 239 See Jackson , J.B.C., 288
Cifuentes, S. See Fernandez, M., 240 Cooke, R.G. See Pandolfi, J.M ., 292
Cinner, J., 285 Cooke, W.J. See Parker, D.M., 197
See McClanahan, T., 290 Coomes, D.A., 238
Cinner, J.E . See Pratchett, M.S., 251-296 Cooper, A. See Strugnell, J., 200
Cisternas, P. See Byrne, M. , 237 Cooper, A.B. See Hendry, A.P., 241
Clark, D.R., 19 Coote, A.R. See Sutcliffe, W.H., 363
See Flynn, K.J ., 21 Corballis, M.C. See Vaughan, G.M., 330
Clark, J., 325 Corbett, S.C. See Brenk man , S.J., 324
Clark, V. See Hawkins, J.P. , 287 Corgos, A., 238
Clarke, A., 238 Cornette, F. See Boudry, P. , 237
Clarke, M.R ., 188, 189 Corpuz, V.T. See Carpenter, K.E., 284
See Lu , C.C., 194 Correia, A.T., 325
Clauser, A.A. See Palen , W.J., 246 Cortez T., 189
Clayton, J.L. See Wells, B.K., 330 Corwin, S. See Townsend , D.W., 330
Clements, K.D. See Choat, J.H., 285 Cosgrove, J.A. , 189
See Crossman, D.J., 285 Cosner, C. See Cantrell, R.S., 359
Clobert, J. See De Fraipont, M., 238 Costa, J.L. See Moreira, F., 101
See Massot, M., 244 Costa, M.J. See Cabral, H.N., 96
See Sorci , G., 248 See Marques, J.C. , I00
Cloney, R.A. See Brocco, S.L., 187 See Moreira, F. , 101
Clough, A.M. See Miller, M.B., 328 Cotano, U. See Diaz, E., 239
Clutton-Brock, T.H., 238 Cote, J.M ., 238
Cobb, C.S., 189 See Gardner, T.A., 286
Cocheret de Ia Moriniere, E. See Nagelkerken, 1., 291 See Uyarra, M.C ., 295
Coenjaerts, J. See Polet, H., 102 Cotret, 0. See Bustamante, P., 188
Coesel, P.F.M. See Spijkerman , E., 23 Cousens , R.D. See Shepherd, J.G. , 363
Cohen, Y. See Kuhl, M., 59 Coutin, P. See Hamer, P.A., 327
Coimbra, J. See Correia, A.T., 325 Couvet, D. See Julliard, R. , 288
Cole, K.S. , 238 Cowan, J.H. Jr. See Fuiman, L.A ., 360
Coleman , G. See Cheal, A.J., 284 Cowen, R.K. , 359
Coles, S.L. See Jokiel , P.L. , 288 See Hare, J.A. , 360
Coli, J.C. See Maida, M., 59 Cowlishaw, G. See Purvis, A. , 293
Collet, B. See Boudry, P., 237 Cox, E., 55
Collingham, Y.C. See Thomas, C.D., 294 Cox, E.F., 238
Collins, M.A., 189 Craig, S., 189
Colmers, W.F. , 189 Crean, A.J., See Marsha ll , D.J., 203-250
Colmes, K.E. See Mumby, P.J. , 60 Cresswell, R.C. See Syrett, P.J., 23
Conan , J.Y. See Cuet, P., 55 Creutzberg, F., 96
Congdon, J.D., 238 See Kuipe rs , B.R., 99
Connell, J.H., 55, 285 Criales, M .M. , 96
See Hu ghes, T.P. , 57, 288 Crivelli, A.J., 97
Connolly, S.R. See Anthony, K.R.N ., 53 See Gellin, A., 98
See Be llwood , D.R., 283 See Pampo ulie, C., 246
See Hoogenboom, M.O., 57 Croft , M.T., 19
See Hughes, T.P. , 57,288 Cronin , T. See Shashar, N ., 199
See Madin , J.S. , 289 Cronin , T.W. See Shashar, N., 199
Conover, D.A ., 96 Crook , D. See Munro, A.R., 328
Conover, D.O. See Schultz, E.T., 102 Crosby, M.P. See Shokri, M .R. , 294
Conrad, M.E. See Solomon, C.T., 329 Crossman, D.J., 285
Conroy, A.M., 238 Croucher, T. See Beaumont, A.R., 95
See Pankhurst, N.W., 246 Crowder, L.B. , 238
Conroy, M.J. See Williams , B.K., 330 See Figueira, W.F., 240
Convey, P. See Walther, G.R., 295 Crump, M.L., 238
370
AUTHOR INDEX
Cruz, P., 238 De'ath , G., 285

Cuesta, J.A. See Drake, P., 97 See Berkel mans, R., 54, 283
Cuel, P., 55 See Ha rrington , L., 56, 287
Cunningham, A., 19 DeBlois , E. See Leggett, W.C. , 361
See Davidson, K., 19,20 DeBlois, E.M. See Leggett , W.C. , 100
Cunningham, J.P. See West, S.A., 250 de Eguileor, M., 189
Curry, J.A. See Webster, P.J., 295 de Figueiredo, G.H., 360
Curtin, C.G. See Brown , J.H ., 284 De Fraipont, M., 238
Cury, P. , 189, 359 Degner, E., 189
See Faure, V. , 190 deGroot, G.J. See Zevenboom, W., 23
Cushing, D.H. , 359 Dejmek, J. See Sram, R.J., 249
Czesak, M.E. See Fox, C.W., 240 de Jong, G. See van der Have, T.M., 250
Dekker, R. See Beukema, J.J., 95
See Philippart, C.J.M., 101
D Del Norte-Campos, A.G .C., 97
de Nys , R., 55
Daan , N., 97
See Wright , J.T. , 250
See Rijnsdorp, A.D., 362
Delafontaine, Y. See Pepin, P., 362
See Welleman, H.C., 104
Delanghe F. See Polet, H., 102
Dahl , K. , 97
Delean, S. See Cheal, A.J., 284
Dahlbe rg, M.L. See McKinnell, S., 328
Demanche, J.M. See Donaghay, P.L., 20
Dahlgren, C.P. See Mumby, P.J., 60, 291
Demarcq, H. , 189
Dai, X. See Houghton, J.T., 287
See Caveriviere, A., 188
Daka, E.R ., 238
See Faure, V., 190
Dale, A.W. See Gonzalez, A.F., 191
DeMartini, E.E., 239
Dalley, R., 97
den Hartog, C. See Nagelkerken, 1., 291
Dal sgaa rd, T. See Kuhl, M., 59
Deng, Y.W., 239
Damiani , C.C., 238
Denno, R.F. See Zera, A.J., 250
Damm, U. See Revill , A., 102
Denny, M. See Abelson, A. , 53
See Temming, A., 103
Denny, M.W. See Wing, S.R., 63
Damman, H. See Loader, C., 243
Denuce, J.M . See Paulij , W.P., 197
Dang, T. See Lucero, M.T., 194
D'A niello, A., 189 Depczy nski, M. See Bellwood, D.R ., 283
Danilow icz, B.S . See Brophy, D., 324 Depontual, H. See Campana, S.E., 325
Dani s, B. See Bustamante, P., 188 Derks, P., 97
Dankers, N. See Dahl, K., 97 DeRusha, R.H ., 189
Dankwa , H.R. See Callrijsse, A., 96 Desaunay, Y. See Amara, R. , 236
Dannev ig, E. H., 325 de Siqueira, M.F. See Thomas, C.D., 294
Dappe r, R. See Kuipers, B.R., 99 De Stefano, R. See Brown, E.R., 187
See Vander Veer, H.W., 103 Dethier, M.N. See Steneck. R.S. , 62
Daufresne, T. See Klausmeier, C.A., 22 DeVantier, L.M ., 285
Dauvin , J.-C. See Mou ny, P. , 101 De Vias, J., 97
Dave nport , J. See Hoare, K., 241 de Vries, M.C. , 325
David son, F.J.M. See Pepin , P., 362 Dew, B., 189
David son. J. See Diaz-Pulido, G., 55 De Wilde, P.A.W.J. See Kuipers, B.R., 99
David son, K. , 19, 20 See Van Donk , E. 104
See Fehling, J., 20 DeWitt, T.J., 239
Davies. P. See Babcock, R., 53 deYoung, B. See Rose, G .A., 362
Davies l.L. See Symonds, D.J., 103 Dhonl, J. See Iglesias, J. , 193
Davi s, A.R. See Benkendorff. K .. 236 Diallo, A. See Caveriviere, A., 188
Davis, C.O. See Conway, H.L., 19 Diallo, M., 189
Davi s, G.E. See Martin , W. , 100 Diamond , J. See Pimm , S.L., 292
Daw, T.M . See Graham, N.A.J., 286 Diaz, E., 239
Dawit, Y. See Zekeria, Z.A., 296 Diaz, F. See Baklouti, M., 19
Day, T. See Hendry, A.P., 241 Diaz-Pulido, G., 55. 285
Dayton , P.K., 285 See McCook , L.J. , 60
See Birkeland, C., 237 Diaz- Pulido, G.A . See Birrell , C.L. 25-63
Dean, J.M. See Secor, D.H ., 329 Dibattista, J.D., 239
371
AUTHOR INDEX
Dickie, J.B. See Moles, A.T. , 245 Dubinsky, Z. See Falkowski, P.G., 20
See Olsen, E.M., 246, 362 Ducobu, H., 20
Diekmann, R., 189 Dufresne, L..See Miloslavich , P., 245
Dijkema, R. See Boddeke, R., 96 Dugan, J. See Roberts, C.M ., 293
Dilly, P.N. See Nixon, M., 196 Dugan, J.E. , 239
DiMarco, F.P. See Vidal , E.A.G., 201 Dugdale, R.C. See Harrison , P.J., 21
DiNardo, G.T. See Rothschild, B.J., 362 Duggins, D.O., 55
Ding, Y. See Houghton, J.T., 287 See Eckman , J.E. , 56
Dingle, H., 325 Dulvy, N.K., 285
See Mousseau , T.A., 245 Dunlap, W.C. See Oliver, J.K ., 61
Dinsdale, E.A. See Hughes, T.P. , 57, 288 Dunn, A .M., 239
Dioses, T. See Markwitz, A., 328 Dunne, R. See Brown, B. E., 284
DiTullio, G.R. See Bertrand, E.M., 19 Dunstan, P.K. , 55
Dixon, D. See Sheppard, C., G 294 Duran, M., 97
Dixon, D.G. See Munkittrick , K.R. 245, 246 Dusek, E. See McCl a nahan, T.R., 59
Dixon , G.K . See Syrett, P.J., 23 Duthie, G.G. See Wells, M.J., 202
Doesburg, W. See Boddeke, R., 96 Dybdahl, R. See Sale, P.F., 293
Doflein , F. , 97 Dyer, M .F., 97
Doherty, P.J., 285 Dykhuizen, D. E., 20
See Moltschaniwskyj, N.A., 195 Dytham, C. See Hawkins, J.P., 287
Doledec, S. See Bozec, Y.M., 284 Dziminski, M.A., 239
Domain, F. See Caveriviere, A., 188
Dombronsky, Y. See Gruntfest Y., 360
Donaghay, P.L., 20 E
Done, T. See Salm, R.V., 293
Done, T.J., 55, 285 Eagle, J.V. See Jones, G.P., 288
See Arthur, R., 283 Eaglesham, G. See Negri, A.P., 60
See DeVantier, L.M ., 285 Eakin, C.M. See Hoegh-Guldberg, 0., 57
Doney, S.C. See Moore, J.K., 22 Ebersole, J.P., 285
See Orr, J.C., 292 Eckert, G.L. See Shanks, A.L., 199
Donnelly, P. See Pritchard, J.K., 328 Eckman, J.E., 56
Donner, S.D., 285 See Duggins, D.O., 55
D'Onofrio, G. See D'Aniello, A., 189 Eclair, L. See Downing, N., 285
Donohue, K., 239 Edmonds, J.S., 325
Dorenbosch, M. See Nagelkerken, 1., 291 Edmunds, P.J., 56
Dorval, E., 325 See Carpenter, R.C., 55
Doubleday, Z ., 190 See River, G .F., 61
Douglas , A. See Brown, B. E., 284 Edwards, A.J. See Hoegh-Guldberg, 0., 57
Douglas , A.E., 285 See Mumby, P.J., 291
Douglas, R.H., 190 Edwards, M.S. See Graham , M.H., 326
Dower, J.F., 360 Edwards, R., 97
See Pepin , P., 362 Edwards, R.A . See Smith, J.E., 62
Downes, S.J. See Shine, R., 248 Egge, J.K. , 20
Downey, P. See Buckley, Y.M ., 237 Eggleston, D. B. See Gillanders, B.M., 326
Downing, J.A. See Tilman, D., 295 Ehrenbaum, E., 97
Downing, N., 285 Ehrich, S. See Hinz , H. , 99
Drake, P., 97 Ehrlich, P.R., 239
Drent, J., 97 Ehtisham, A. See Schultz, E.T., 102
Driessen , G. See Boddeke, R., 96 Eibl-Eibesfeldt, l.v., 190
Drinkwater, K. See Choi, J.S., 359 Einum, S., 239
Drinkwater, K.F., 360 Elahi, R. See Edmunds, P.J., 56
See Myers, R.A ., 362 Elder, N.E. See Hershberger, P.K., 241
See Sutcliffe, W.H ., 363 Elfman, M. See Limburg, K.E. , 328
Droop, M.R., 20 Elfwing, M. See McClanahan, T.R., 290
See Tett, P., 23 Elkin, C.M., 239
Drummond, A. See Strugnell, J. , 200 Ellis, J.R. See Perry, A.L., 292
Du Cane, C ., 97 Ellis, T. See Vander Veer, H.W., 103
Dubi, A. See Hoegh-Guldberg, 0., 57 Ellison, A.M. See Gote lli, N.J., 326
372
AUTHOR INDEX
Elmqvist, T., 285 Fam;l l, J. , 326

See Fol ke, C., 56 Fasham, M.J.R ., 20
Elri fi, l.R., 20 See Flynn, K.J., 21
Elsdon, T.S., 297, 325 Fatemi, S.M.R. See Shokri , M.R. , 294
See de Vries, M.C., 325 Faure, G., 56, 326
See Munro, A.R., 328 See Cuet, P., 55
Elser, J.J. See Sterner, R.W., 23 Faure, L. See Kurc, G., 100
Eltink, A.T.G.W. See Creutzberg, F., 96 Faure, V., 190
Emanuel, K. See Henderson-Sellers, A., 287 See Baklouti, M. , 19
Emaurois, C. See Golbuu, C., 286 See Demarq, H., 189
Emery, D.G., 190 Fautin , D.G. See Ollerton , J., 292
Emlet, R., 239 Fearon, R.J., 56
Emlet, R.B. See Hoegh-Guldberg, 0., 241 Feary, D.A., 285
See Marshall , D.J., 244 Feely, R.A. See Orr, J.C., 292
See Moran, A.L., 245 Fehling, J., 20
Emsley, S.M. See Baird, M.E. , 19 See Davidson, K., 20
Emslie, M.J. See Jones, G.P. , 242, 327 Feige, M. See Stock, M., 103
Emson, R.H. See McCarthy, D.A., 245 Feldheim, K.A. See Dibattista, J.D., 239
Engel, A. See Sommer, U., 200 Feller, R.J . See Van der Veer, H.W., 103
Engel, M.S. See Bak, R.P.M., 54 Fenaux, L. See George, S.B., 240
Ennevor, B.C., 325 Feral , J. See Poulin, E., 198
Epstein, N., 56 Fernandes, R. See Sousa-Reis, C., 200
Erasmus, B.F.N. See Thomas, C. D., 294 Fernandez, L. See Sampedro, M.P., 248
Eriksen, M.S., 239 Fernandez, M., 239, 240
Erlandson, J. See Jackson, J.B.C., 58, 288 See Baeza, J.A., 236
Ernande, B. See Olsen, E.M., 246 Fernandez-Delgado, C. See Drake, P., 97
Eskildsen, K. See Stock, M., 103 Fernandez-L6pez, A., 190
Espinoza-Avalos J. Quan-Young, L.l., 61 Fernandez-Palacios, H. See Fernandez-L6pez, A., 190
Espmark, A. See Eriksen, M.S. , 239 Fey, D. See Radtke, R.L., 329
Estes, J.A. See Jackson , J.B.C., 58, 288 Fiandra, L. See de Egu ileor, M., 189
Evans, F. See Micaleff, H., 100 Field, M.E. See Stamski, R.E., 62
Evans, J.P., 239 See Storlazzi, C. D., 62
See Marshall , D.J., 244 Fig ueira, W.F., 240
Evans, S., 97 See Crowder, L.B ., 238
Ewanchuk, P.J. See Tru sse ll, G.C., 363 Findlay A.M . See Shima, J.S. , 248
Find ley, J.S., 285
Findley, M.T. See Find ley, J.S., 285
F Finn, 1. See Hochberg, F.G., 192
See Norman, M.D., 196
Eyring, C.F., 190 Fioroni , P., 190
Fabbiani , F., 97 See Boletzky, S.v., 187
Fabricius, K. See Harrington, L., 56, 287 See Bullow, B.v., 188
Fabr icius, K.E., 56 See Lenz. S., 194
See Negri , A.P., 60 Fischer, G. See Stock, M., 103
Fabrizio, M.C., 325 Fischer, K., 240
Fabry, V.J. See Orr, J.C. , 292 Fischer, M. See van Kleunen, M., 250
Fadli, N. See Baird, A. H., 283 Fish, J.D. See Bell, M.C. , 236
Fagan, W.F., Cantrell, R.S., 359 Fisk, D. A .• 56
Fahrig, L., 285 See Harriott, Y.J., 57
Fairbanks, R.G. , 326 Flach, E.C., 97
Fairfull, S.J.L. , 56 Flament, P. See Bower, J.R., 187
Fairweather, P.G. See Underwood, A.J., 249 Flegal, A.R. See Roitz, J.S., 329
Falconer, D.S., 239 Fleisher, K.J., 190
Falkowski, P.G., 20 Fleming, I.A., 240
Fangue, N.A. See Tiffany, B.N., 200 See Ei num, S., 239
FAO, 190 Fletcher, G.L. See Rose, G.A., 362
Farke, H. See Dahl , K. , 97 Fletcher, J.P., 240
Farmer, M.J. See Milton, D.A., 328 Flindt, M.R. See Pardal, M.A., 246
373
AUTHOR INDEX
Flores, Y. See Sante! icies, B., 248 Fransen, C. See Smaldon, G., 103
Floros, C. D., 285 Frechet, A. See Campana, S.E., 324
Flynn, K. See Meeka n, M.G., 362 Freckleton, R.P. See Dulvy, N.K. , 285
Flynn, K.J., 1-23, 20,21 Freidenburg, L.K. See Skelly, O.K., 248
See Clark, D.R., 19 Freire, J. See Cargos, A., 238
See Davidson, K., 20 See Sampedro, M.P., 248
See Fasham, M.J.R., 20 Freitas, V., 97
See John, E.H., 21 Freon, P. See Lett, C., 361
See Mitra, A., 22 Fretwell, S.D. See Smith, C.C., 248
See Stephens, N., 23 Frid, C.L.J. See Lancaster, J., 101
See Syrett, P.J., 23 Friedlander, A.M., 286
See Wood, G., 23 Friese, D. See ｾｯｬｩｮｳＬ＠ M.A., 189
Fodrie, F.J. See Becker, B.J., 236 Fromentin, J.M . See Walther, G.R., 295
Fogarty, M.J., 360 Frosch, D., 190
Folke, C., 56 See Mangold , K., 194
See Adger, W.N ., 283 Fryer, B.J. See Ludsin, S.A., 328
See Bellwood, D.R., 283 Fuentes, L., 190
See Elmqvist, T., 285 See Iglesias, J., 192, 193
See Hughes, T.P., 57, 288 Fuentes, M. See Boletzky, S.v., 187
See McCook, L.J., 60 Fuentes-Yaco, C. See Platt, T., 362
See Nystrom, M., 291 Fuiman, L.A., 360
Folt, C.L. See Kennedy, B.P., 327 See Hoff, G.R., 327
Fonds, M. See Freitas, Y., 97 Fujimoto, H. See Tsukamoto, K., 330
Fong, P., 286 Fujinaga, K. See llano, A.S., 242
Forchhammer, M.C. See H0ye, T.T., 287 Fujita, Y. See lkeya, T., 21
Foreman, K. See Valiela, 1., 62 Fukunaga, K. Hamasaki, H. , 192
Forrester, G.E. See Holbrook, S.J., 287 Fung, I.Y. See Moore, J.K., 22
Forsgren, E., 240 Furnas, M., 56
Forsythe, J.W., 190 See Meekan, M.G., 362
See Adams , P.M., 186 See Wilson, S.K., 296
See Colmers, W.F., 189 Furness, R.W. See Garthe, S., 98
See DeRusha, R.H., 189 See Hudson, A.V., 99
See Hanlon, R.T., 192 Furuya, H., 190
Fortier, L. , 360
See Mousseau, L., 362
Forward, R.B., 190 G
See Ziegler, T.A., 202
Fossum, P., 326 Gabbott, P.A. See Bayne, B.L., 236
Foster, M.S. See Reed, D.C., 61 Gabe, S.H., 190
Fowler, A.J., 286, 326 Gabrie, C., 56
See Begg, G.A., 324 Gagam, M.K. See Pelejero, C., 292
See Campana, S.E., 325 Gagliano, M., 240
Fowler, M.S., 240 Gagne, H.T. See Graziadei, P.P.C., 191
Fowler, S.V. See Buckley, Y.M., 237 Gagne, J.A . See Campana, S.E., 325
Fowler, S.W. See Bustamante, P. , 188 Gagnon, J.E. See Ludsin , S.A., 328
Fox, C.W., 240 Gaines, S.D. See Bertness, M.D., 237
See Heath, D. D., 241 See Halpern , B.S., 287
See Mousseau, T.A., 245 Gall, A. See Mumby, P.J., 291
Fox, S. See Williams, S.E., 296 Gallagher, M.D., 240
Foy, E.A. See O'Dor, R.K., 196 Gallon, J.R . See Stephens, N., 23
Frache, R. See Grotti , M., 326 Galloway, L.F., 240
Frank, K.T., 311, 360 Galzin, R. See Bell , J.D., 283
See Carscadden, J.E ., 359 See Graham, N.A.J., 286
See Choi, J.S., 359 See Lecchini, D., 289
See Dower, J.F., 360 See Letourneur, Y., 289
See Leggett, W.C., 331-363, 361 Gam ito, R. , 97
See Marshall C.T., 361 See Cabral, H.N., 96
See Platt, T., 362 Garcia-Gonzalez, D. See Drake, P., 97
Franklin, R.L. See Solomon, C.T., 329 Gardiner, N.M ., 286
374
AUTHOR INDEX
Gardner, C., 240 Glynn, P.W., 286

Gardner, T.A., 286 See Fong, P., 286
Garfield, P.C. See Blasco, D. , 19 Gnanadesikan, A. See Orr, J.C., 292
Garpe, K.C., 286 Goby, G. See Munday, P.L., 291
Garthe, S., 98 See Pratchett, M.S ., 6 1,293
Garzon-Perreira, J. See Diaz-Pulido, G., 55 Goddard, S.V. See Rose, G.A. , 362
Gasco igne, J., 360 God fray, H.C.J., 240
Gaston , K.J. , 286 Godley, B.J., 240
Gates, R.D. See Edmunds, P.J., 56 Goering, J.J . See Nelson , D.M., 22
Gatje, C. See Stock, M. , 103 Golbuu , Y., 286
Gattuso, J. See Kleypas, J.A., 288, 289 Goldman , J.C. , 21
Gauldie, R.W., 326 Gomez, E. See Hoegh-Guldberg, 0., 57
See Markwitz, A., 328 Gomez, E. D. See Raymundo, L.J., 61
Geber, M.A. See McGinley, M.A., 245 Gomez , J.M. , 240
Gee, J.M. , 98 Gon za lez, A.F., 191
Geffard, A. See Rainbow, P.S., 247 Gonzalez, A.V. See Villanueva, R., 20 1
Geffen, A.J., 326 Gonzalez, M.L., 191
Geider, R.J., 21 Gonzalez-Gurriaran, E. See Sampedro, M.P., 248
See Leonardos, N., 22 Goodon , M. See Brown, B.E., 284
Gellin, A., 98 Gorczynska, M.l. See Mumby, P.J., 291
George, S.B., 240 Goreau, T.F., 286
Gerace, D. See Ostrander, G.K. , 61, 292 Gorissen , M.W. See Nagelkerken, 1., 29 1
Geritz, S.A.H., 240 Goswami, B.N. See Saji. N.H. , 293
Ghebremedhin, S. See Zekeria, Z .A., 296 Gotelli, N.J., 326
Ghiretti, F., 190, 191 Gotham, I.J., 2 1
Gibbons, J.W. See Congdon, J.D. , 238 See Rhee, G.-Y., 23
Gibson , D.J. See Baird, A.H., 54 Goudswaard, P.C. See Boddeke, R., 96
Gibson , R.N., 98 Gourlay, M. See Sheppard, C., 294
See Ansell, A.D., 95 Gouze, J.L. See Bernard, 0., 19
Giddins, R. See Johnson, C.R., 58 Gowland, F.C., 19 1
Gilbert, F. See Sadeghi, H., 248 Graham , M.H., 326
Giles, K. See Bingham, B.L., 237 Graham , N .. 98
Gill, A.B. See Mumby, P.J., 291 Graham, N.A.J., 286
Gill, J.A. See Gardner, T.A. , 286 See Ledlie, M.H. , 289
See Uyarra, M.C., 295 See McClanahan, T.R., 290
Gillanders, B.M., 326 See Pratchett, M.S., 251-296, 293
See de Vries, M.C., 325 See Wilson, S.K., 296
See Elsdon, T.S. , 297-330 Graham, T., 286
See Fowler, A.J., 326 Grainger, A. See Thomas, C. D. , 294
See Hamer, P.A., 327 Grambole, D. See Markwitz, A. , 328
See Kin gs fo rd , M.J. , 327 Grandcourt, E.M., 286
See Munro, A.R., 328 Grant, A. See Gardner, T.A., 286
Gillooly, J.F. See Savage, V.M., 23 Grantham. B.A. See Shanks, A.L., 248
Gilly, W.F. , 191 Gratwicke, B., 286
See Chen. D.S., 188 Gravely, F.H., 191
See Lucero, M .T., 194 Gray, J.S., 286
Gilmer, R.W. See Lalli, C.M., 194 Gray, W. See Henderson-Sellers, A., 287
Gilmour, J., 56 Graynoth, E.J. See Gauldie, R.W., 326
Gimenez, L., 240 Graziadei, P., 191
Ginzburg, L.R., 240 Graziadei, P.P.C., 19 1
Giordana, B. See de Egui leor, M., 189 Green, A. See Kulbicki, M., 289
Gittleman, J.L. See Purvis, A., 293 Green, B.S ., 240
Giuditta, A. See Brown, E.R., 187 Green, E.P. See Spalding, M.D., 294
Gladfelter, E. H. See Gladfelter, W.B., 286 Green , J., 24 1
Gladfelter, W.B. , 286 Green , M.G., 19 1
Gleason, D.F. See Edmunds, P.J. , 56 Green , R.E. See Thomas, C. D., 294
Gleason, M.G ., 56 Greenfie ld , P. See Hoegh-Guldberg, 0., 57
Glen, F. See Godley, B.J., 240 Grigg, R.W. , 286
Glover, D.M . See Moore, J.K. , 22 Griggs, D.J. See Houghton, J.T., 287
375
AUTHOR INDEX
Gr ima ldi , A. See de Egu il eor, M., 189 Halsband-Lenk, C., 241
Gr impe, G., 191 Hamano, T. See Sakaguchi, H., 199
Grindstaff, J.L., 241 Hamasaki, H., 192
Grisley, M.S., 191 Hamasaki, K., 191
Gronell, A.M., 241 Hamel , J.F., 241
Gronkjaer, P. See Hinricksen, H.-H., 360 Hamer, P.A., 327
Grorud-Colvert, K., 24 1 Hamner, W.M. See Zeidberg, L.D. , 202
Grosberg, R. See Hughes, T.P., 57, 288 Hanlon, R.T., 192
Gross, E.M., 56 See Adams, P.M., 186
Gross, M.R. See Sargent, R.C ., 248 See Boletzky, S.v., 187
Grossmue ller, D.W., 241 See Colmers, W.F., 189
Grotti, M., 326 See DeRusha, R.H. , 189
Grover, J.P., 21 See Forsythe, J.W. , 190
Grubb, P.J . See Coomes, D.A., 238 See Shashar, N ., 199
Gruber, N. See Orr, J.C., 292 Hannah , L. See Thomas, C. D., 294
Gruber, S.H . See Dibattista, J.D., 239 Hannigan , R. See Dorval, E., 325
Gruntfest Y., 360 Hansen , K.E. See Van Marlen, B., 104
Guerra, A. See Cortez T., 189 Hansen , L.J. See Roessig, J.M., 293
See Gonza lez, A. F., 191 Han se n, T. See Sommer, U., 200
Gu ill a rd, R.R.L. See Nelson, D.M., 22 Hanson, J.M. , 360
Gu ill aume, M.M.M. See McClanahan, T.R., 290 See Campana, S.E., 324
Gu isande, C., 241 See Swain, D.P., 249
Gunderson, L. See Folke, C., 56 Hansson , L.A. See Gustafsson, S., 241
Gunn, J.S., 326 Harada, Y. See Sakai, S., 248
See Proctor, C. H. , 328 Harborne, A.R. See Mumby, P.J., 60, 291
Gunna rsson, B. See Marteinsdottir, G., 244 Harbour, D. See Pond , D., 247
Gunther, D. See Campana, S.E., 325 Hardcastle, J. See Ledlie, M.H., 289
Guo, X.M. See Deng, Y.W., 239 Hare, J.A., 360
Gurney, A.R., 98 Hare, J.A. See Thorrold, S.R., 330
Gurney, W.S.C. See Davidson , K. , 20 Harman, R.F. See Young, R.E., 202
Gust, N. See Pratchett, M.S ., 61,293 Harmel in-Vivien, M. See Letourneur, Y., 289
Gustafsson, S., 241 Harmelin-Vivien, M.L., 287
Gutierrez, L., 286 See Bell , J.D., 283
Gu tierrez-Paja res, J.L., 191 See Bouchon-Navaro, Y., 284
Gutow, L. See Thiel, M. , 200 Harms, K.E. See Connell, J.H., 55
Guy, J.A. See Sa le, P.F., 293 Harold, A.S. See Munday, P.L., 291
Guzman, H.M. See Pa ndolfi , J.M., 61 Harrin gton, L., 56, 287
Gysels, E.S., 98 See Birrell, C.L., 54
Harriott, V.J., 56, 57
See Banks, S.A., 54
H See Fairfull , S.J.L., 56
See Fisk, D.A., 56
Hackney, J.M. See Carpenter, R.C., 55 Harri s, J.H. See Brown , P., 324
Hadfield , M.G. See Walters, L.J. , 63 Harris , P.M. See Toole, C.L., 330
Haefner, P.A. See Spaargare n, D. H., 103 Harri s, R. See Pond, D., 247
Hagadorn, I.R. See Nishioka, R.S., 196 Harris, R.P., 192
Hagerman , L., 98 Harrison, P. See Wilson , J., 63
Haimovici, M. See Vidal, E.A.G., 20 1 Harrison , P.J., 21
Halavik, T.A. See Buckley, L.J., 237 See Conway, H.L. , 19
Halden, N.M ., 326 See Parslow, J.S., 22
See Campana, S.E., 325 See Turpin, D.H., 23
Hales, L.T. See Hatje, V., 327 Harrison, P.L., 57
Halford , A. , 287 See Reichelt-Brushett, A.J., 61
Hall , D.J. See Werner, E., 363 Harrowfield , I.R. See Gunn, J.S ., 326
Hall , K.C. See Fowler, A.J., 326 See Proctor, C. H. , 328
Hall, V.R., 56 Hart, A.M., 287
Hal Iacher, L.E. See Tissot, B.N., 295 Hart , M.W., 241
Halpern , B.S., 287 See Byrne, M. , 237
See Roberts, C.M., 293 Hart, P.J.B. See Kaiser, M.J. , 288
376
AUTHOR INDEX
Hartl, D.L. See Dykhuizen, D.E., 20 Heppell , S. See Bridges, T.S. , 237
Hartmann, F. See Stock, M. , 103 Herdiana, Y. See Baird, A.H., 283
Hartnoll, R.G. See Oh, C.-W., 101,246 Herman, P.M.J. See Paulij, W.P., 197
Hartsuyker, L., 98 Hernandez-Cruz, M.C. See Fernandez-Lopez, A. , 190
Hartwick, B., 192 Hernandez-Garcia, V., 192
Harvell, C. D. See Bruno, J.F. , 54 See Hernandez-Lopez, J.L., 192
See Hoegh-Guldberg, 0., 57 ｈ･ｲｮ｡､ｺＭｇｯｬｾＮ＠ C.L. See Balguerfas, E., 186
Harvey, I.F. See Fischer, K., 240 Hernandez-Lopez, J.L., 192
Hashimoto, K. See Shibuno, T., 294 Herrmann, F. See Markwitz, A., 328
Hasselquist, D. See Grindstaff, J.L., 241 Herron-Perez, P. See McClanahan, T.R., 59
Hastings, A. See Hill, M.F., 360 Hersh, D. See Val iela , 1., 62
Hastings, P.A., 241 Hershberger, P.K., 241
Hatay, M. See Smith, J.E., 62 Hervouet, Y. See Boudry, P., 237
Hatfield , E.M.C. See Rodhouse, P.G., 198 Hewitt, C.L. See Schaffelke, B., 62
Hatje, Y., 327 Heyward, A.J., 57
Hatziolos, MA. See Hoegh-Guldberg, 0., 57 See Negri, A.P., 60
Hauser, R. See Marthy, H.J., 195 See Webster, N.S., 63
Hauxwell , J. See Valiela, 1., 62 Hiddink J.G., 99
Havinga, B., 98 High, W.L. , 192
Hawkins, J.P., 287 Hilborn, R., 360
See Roberts, C.M., 293 See Liermann, M., 361
Hawkins, S.J. See Daka, E.R ., 238 Hildebrand , M. , 21
Hay, D.E., 327 Hilker, M. See Anderson, P., 236
Hay, M.E., 57
Hill, M.F., 360
See Miller, M.W., 60 Hill , N.A. See Poore, A.G.B., 247
Hayashi , K.-1., 98
Hill, R. See Buckley, Y.M ., 237
Hayashibara, T. See Morse, A.N.C., 60
Hill, R.T. See Negri , A.P. , 60
Hayes, R.L. See Goreau, T.F., 286
Hinckley, S., 241
Haynes, D., 57
Hinricksen, H.- H., 360
Hays, G.C., 192
Hinz, H., 99
See Godley, B.J., 240
Hipkin, C.R . See Flynn, K.J., 21
Head, R. See Pond, D. , 247
Hirche, H.J. See Halsband-Lenk, C., 241
Healey, B.P. See Lilly, G.R .
Hirakawa, J. See Tsukamoto, K., 330
See Shelton, P.A., 361,363
Hirota , J. See Bower, J.R., 187
Healey, F.P., 21
Hislop, J.R.G. , 241
Heaney, S.I. See Tett, P., 23
See Daan, N., 97
Heath, D.O., 241
Hixon , M.A. , 287
Heath, J.W. See Heath , D.O., 241
See Ca ley, M.J., 237
Hedqvist-Johnson , K., 98
Hixon, R.F. See Colmers, W.F. , 189
Heerebout, G.R., 98
See Hanlon , R.T., 192
Heesen. H.J.L. See Rijnsdorp, A.D. , 362
Heino, K. See Ol se n, E.M. , 362 Hjelm , J. See Cardinale, M. , 359
Heino, M. See Olsen, E.M. , 246 Hjermann, D.O. See Ottersen, G., 362
Heldal , M., 21 Hjort, J., 327, 361
Hellemans, B. See Gysels, E.S., 98 Ho, C. See Marra, J ., 22
Helm , P.L. See O' Dor, R.K. , 196 Hoare, K. , 241
Henderson, P.A., 98, 99 Hobbs, J.A., 327
Henderson, R.J., 192 Hobbs, J.P., 287
Henderson-Arzapalo, A. See Secor, D. H., 329 Hobday, A.J. See Poloczanska, E.S., 292
Henderson-Sellers, A., 287 Hobson, E.S., 287
Hendri ck, V. See McClanahan, T.R., 290 Hochberg, F.G., 192
Hendri ck, V.J. See Williams, 1.0., 296 See Huffard, C.L., 192
Hendrickx, F., 241 See Lang, M.A., 194
Hendrix , J.P. See Hanlon, R.T., 192 See Norman, M.D., 196
Hendry, A.P., 241 See Packard, A., 197
See Dibattista, J.D., 239 See Young, R.E., 202
See Einum, S., 239 Hodge, J. See Chen, D.S., 188
Hendzel, L.L. See Healey, F.P., 21 Hodgson, G., 57, 287
Hen king, H., 98 Hodgson , K.E. See Peel, G.T., 197
377
AUTHOR INDEX
Hoegh-Guldberg, 0., 57, 241, 287 Hughes , T.P., 57, 58, 287, 288
See Donner, S.D., 285 See Adger, W.N ., 283
See Hughes, T.P. , 57, 58, 288 See Ayre, D.J. , 283
See Poloczanska, E.S., 292 See Baird, A.H ., 54
See Walther, G .R., 295 See Bellwood, D.R., 54
Hoelzer, G.A., 241 See Bellwood, D.R. , 283
Hoey, A.S. See Bellwood, D.R., 54, 283 See Caley, M.J ., 237
Hoff, G.R., 327 See Connell, J.H., 55, 285
Hoffman, O.K., 57 See Hall , V.R., 56
Holbrook, S.J., 287 See Jackson , J.B.C., 58, 288
See Schmitt, R.J ., 294 See McCook, L.J., 60
Holdway, D.A. See Butty, J.S., 188 See Pandolfi, J.M. , 6 1, 292
See Long, S.M., 194 See Warner, R.R., 295
Hol land, D.L. See Bayne, B.L., 236 Hui ,C., 36 1
Holland , G. See Henderson -Sellers, A. , 287 Hui sman , J. See Ducobu , H. , 20
Holland, G.J. See Webster, P.J., 295 Huitema , H.J . See Ka merman s, P., 99
Hol li ng, C.S . See Folke, C., 56 Huitric, M. See McC lana han, T.R., 290
Holloway, B. See Sidie, J., 199 Hulet, W. See Colmers , W.F., 189
Holmes, K.E. See Mumby, P.J ., 291 Humphrey, C. See Markey, K.L. , 59
Holmes, R.H.A. See Henderson, P.A ., 98 See Negri , A.P. , 60
Hol st, R. See Revill, A., 102 Hunt, J.C., 192
Holt , S.J. See Beverton, R.J.H ., 359 Hunte, W. See Cote, l.M., 238
Holthuis, L.B. 99 See Lawson, G.L. , 289
See Smaldon, G., 103 Huntin gfo rd, F. See Berglund , A., 236
Hong, S.Y. See Kim, S.H ., 242 Huntl ey, B. See Thomas, C. D., 294
Hong, Y.K. See Kim, J., 58 Huntl ey, M. See Harris, R.P., 192
Honkoop, P.J.C. See Beukema, J.J., 95 Huntsman, S.A. See Sunda, W.G., 23
Hoogenboom, M.O., 57 Hup, M. See Bergm an, M.J.N. , 95
See Anthony, K.R.N. , 53 Huppert , A. See Stone, L., 294
Hooidonk , R.J. See Nugues, M.M., 61 Hutchings, J.A., 242, 361
Hooker, N. See Morse, D.E., 60 See Myers, R.A., 362
Hooten , A.J. See Hoegh-Guldberg, 0., 57 Hutchings, P.A., 288
Hopkins, T.L. See Passarella, K.C., 197 Hwan g, P.P. See Lin , H.C., 243
Horan, D.L. See Wells, B.K., 330
Hormazabal, M . See Santelicies, B., 248
Horne, A.J. See Vidal , D.E., 250 I
Horr igan, FT. See Lucero, M.T., 194
Hosten s, K. See Beyst, B., 95 Ibarra, A.M. See Cruz, P., 238
Ho uck , B.A., 192 ldechon g, N. See Graham , T., 286
Ho ude, E.D., 361 ldip, D. Jr. See Golbuu, Y., 286
See Kimura, R., 327 Iglesi as , J. , 192, 193
See North , E.W., 362 See Fuentes, L., 190
Hou ghton, J., 287 See Mox ica, C. , 195
Hou ghton, J.T. , 287 Iglesias- Prieto, R. See Hoegh-G uldbe rg, 0., 57
Ho ulihan , D.F. See Well s, M.J., 202 Ignatius, B., 193
Hoving, H.J.T., 192 !ida, H., 193
Howard , R.D., 241 Ikeda, T. See Omori, M. , 197
Howel l, B.R. See Baynes, S.M., 236 Ikeda, Y., 193
H0ye, T.T., 287 See Kaneko, N., 193
Hruby, T., 57 See Kasuga i, T. , !93
Hsu, S.C. See Lin , H.C., 243 lke moto, T. See Arai, T., 324
Huang, R. See Limburg, K.E ., 327 lkeya, T., 21
Huang, W. See Lucero, M.T., 194 llano, A.S ., 242
Hubbard, D.M. See Dugan, J.E., 239 Illingworth, J. See Gauldie, R.W. , 326
Hudson, A.Y., 99 lmaizuml , K. See Tsukamoto, K., 330
Huette! , M. See Wild, C., 295 Imamura, S., 193
Huffard , C.L., 192 lnejih , A.C. See Faure, V., 190
Hughes, J.P. See Fische r, K., 240 In gram , B.L. See Solomon, C.T., 329
Hughes, L. See Thomas, C. D. , 294 lri goien, X., 21
378
AUTHOR INDEX
Iron s, O.K., 288 Johansso n, F. See Brodin, T. , 237

Irvine, J.R. See Chen D.G., 359 John , E.H., 21
Irwin , D.E. See Price, T.D., 247 John , H. See De Fraipont, M., 238
lsely, J.J ., 99 Johnsen , S., 193
Ishida , A. See Orr, J.C. , 292 John son, C. A. See Houghton , J.T. , 287
Ishii , T. See Miyazaki , T., 195 Johnson, C.N. See William s, Y.M., 296
Isidro, E.J. See Correia, A.T., 325 John son, C.R., 58
lsomura, N. , 242 See Dunstan, P.K. , 55
lta mi , K., 193 Johnson, M.P. See Barratt, I.M ., 186
Ito, K., 242 Johnson, R.M. See Heath, D.D., 241
Itoh, T. See Rooke r, J. R., 329 Johnston, E.L. See Piola, R.F., 246
Ivy, T.M., 242 Johnston, I. See Willmer, P. , 104
Iwa moto, A. See Kurihara, A., 194 Jokiel , P.L., 288
See Okumura, S., 197 Joll , L.M. , 193
lwao, K. See Morse, A.N.C., 60 Jompa, J., 58
lwase, A. See Golbuu , Y., 286 See McCook, L.J., 60
Izawa, Y. See ltami , K., 193 Jones, C.M., 327
Izquierdo, M.S. See Fernandez-L6pez, A., 190 See Bath, G .E., 324
See Campana, S.E., 324, 325
See Dorval, E., 325
J See Elsdon, T.S ., 297-330
See Fowler, A.J ., 326
Jackson, G. See Doubled ay, Z., 190 See Martin , G.B. , 328
Jackson, G.R., 58 See Thorrold , S.R., 330
Jackson, J. See Strugnell , J. , 200 See Wells , B.K., 330
Jackson, J.B.C., 58, 288 Jones, G.P., 242, 288, 327
See Hughes, T.P., 57, 288 See Beger, M., 283
See Knowlton, N. , 58 See Beukers, J.S., 284
See Pandolfi , J.M. , 61,292 See Caley, M.J. , 237
Jackson, S. See Campana, S.E., 325 See Ceccarelli, D.M., 55
Jaeckle, W.B . See Bingham , B.L., 237 See Feary, D.A. , 285
Jager, Z., 99 See Gard iner, N.M., 286
James, D. See He nderson, P.A., 98 See Hixon , M .A., 287
Jami eson, 1., 242 See Munday, P.L., 29 1
Janssen G.M., 99 See Ohm an, M.C., 291
Jarvis, G. E. See Spalding, M.D., 294 See Pratchett, M.S. , 2SI-296, 293
Jaspars, M. See Key, L.N. , 193 See Syms, C., 294
Javois, J., 242 See Thompson, Y.J., 295
Jeantet, A.Y. See Mouneyrac, C., 245 See Thorrold, S.R., 330
See Rainbow, P.S., 247 See Wilson , S.K ., 296
Jeffe ry, S., 99 See Wong, M., 296
Jeffries , T. E. See Brophy, D. , 324 Jones, H.L. , 242
Jeffs, A. See Montgo mery, J.C., I95 See Pimm, S.L., 292
Jenkin s, G.P., 36 1 Jones, M. B. See Mees, J., I95
See Hame r, P.A ., 327 Jones, P.O. , 288
Jennin gs , S., 288 Jones, R. See Negri, A.P., 60
See Graham , N.A.J. , 286 Jones, W.T. , 242
See Led li e, M.H., 289 Jonker, R.R. See Ducobu, H., 20
Jen o, K. See Fernandez, M., 240 Jo nsso n, B. See Nilsson, P., 101
Jen sen, D. See Revill , A. , 102 Joos, F. See Orr, J.C., 292
Jensen, J.N. See Jen sen, K.T., 99 Jorgen sen, B.B. See Kuhl , M., 59
Jensen, K.T., 99 See Wild , C., 295
Jensen , R.A . See Morse, D.E., 60 Joubin , L., 193
Jeong, S.J., 242 Jouffre, D. , 193
Jereb, P., I93 See Caveriviere, A. , 188
Jiddawi , N., See Ngazy, Z. 291 See Diallo, M ., 189
Jiguet, F. See Jullia rd, R., 288 See Semmens, J.M., 199
Jin , H.J . See Kim , J. , 58 Julliard, R., 288
Johann sson A. See Matilla, J. , 100 See Levinton, J.S ., 243
379
AUTHOR INDEX
K Kimura , R., 327

See Furuya, H., 190
Kaiser, M.J., 99, 288 See Takasuka, A., 363
Kalff, J. See Smith, R.E.H., 23 King, B. H., 242
Kalish, J. See Fossum, P., 326 King, D. See Jenkins G.P., 361
Kalish, J.M ., 327 Kingsford, M.J., 327
See Campana, S.E., 325 See Gillanders, B.M., 326
Kamermans, P., 99 See Patterson, H.M. , 328
Kamler, E., 242 Kinin month, S. See Berkel mans, R., 54, 283
Kana, T.M . See Geider, R.J., 21 Kinsley, L.P.J . See Sinclair, D.J., 329
Kanamaru, S., 193 Kinzie, R.A . See Radtke, R.L., 329
Kaneko, N., 193 Kirby, M.X. See Jackson, J.B.C., 58, 288
Kang, S.E. See Kim , J., 58 Kirchhauser, J. See Miske, Y., 195
Kanias, G. D. See Papadopoulou, C., 328 Kiron , Y. See Watanabe, T., 201
Kaplan , R.H., 242 Kitamura, M., 58
Kappel, C.Y. See Mumby, P.J., 60, 291 Kjesbu, O.S. See Marshall C.T., 361
See Pandolfi, J.M., 6 1 Klanten, S.O. See Pratchett, M.S., 61
Kappenman, R.F. See Boehlert, G.W., 96 See Pratchett, M .S., 293
Karina, K., 242 Klausmeier, C.A., 22
Karlsen, H.E . See Packard, A. , 197 Kleypas , J. See Hughes, T.P., 57, 288
Karlson, R.H., 58 Kleypas, J.A., 288, 289
Karlsson, A. See Forsgren, E., 240 See Moore, J.K., 22
Kasugai, T., 193 Kline, D. I., 58
Katawijaya, T. See Baird, A.H., 283 Klueter, A. See Wild , C., 295
Katsanevakis, S., 193 Klug, H. , 242
Klumpp, D.W., 287
Kattner, G., 99
Knapp, R.A ., 242
Kawaguchi, T. See Suzuki , Y., 62
Knight, M.A. See Keats, D.W., 58
Kawasaki, K. See Muko, S., 60
Knobbe, E.T. See Ostrander, G.K ., 61,292
Keats, D.W., 58
Knoke, Y. See Stock, M., 103
Kelaher, B. See Levinton, J.S ., 243
Knoll, A. H. See Myers, N., 291
Kelle, W., 99
Knowlton, N., 58, 361
Kellermann, A. See Stock, M., 103
Hoegh-Guldberg, 0., 57
Kelly, D. See Monks, A., 245
See Kline, 0.1 ., 58
Kemp, S.W., 99
Knudsen, C. See Sadovy, Y., 329
Kennedy, B.P., 327
Kobayashi , T., 242
Keough, M.J., 242
Kocan, R.M. See Hershberger, P.K., 241
See Marshall, D.J., 244
Koch, E.M.W. See Larkum, A.W.D., 59
See Quinn, G .P., 328 Koesters, N. See Beckerman, A.P., 236
See Underwood, A.J., 250 Koh , E.G.L., 58
Kerambrun, P. See Gel lin, A., 98 Kohata, K. See Watanabe, M., 23
Kerr, A.M. See Connell, J.H. , 55 Kohn. A.J., 242
Kerr, L.A., 327 Kokita, T., 243, 289
Kerrigan, B.A. , 242 Kokko, H. See Lindstrom, J., 243
Key, L.N., 193 Kolliker, A., 194
See Grisley, M.S., 191 Kolm , N., 289
Key, R.M. See Orr, J.C., 292 Kolod ziej ska, I. See Sikorski, Z.E., 199
Khalaf, M.A., 288 Koltes, K.H. See Aron so n, R. B., 283
Kidokoro, H. See Shigeno, S ., 199 Konig, B. See Berglund , A., 236
Kidwell, S. See Jackson, J.B.C ., 58, 288 Kooijman , S.A.L.M., 99
Kier, W.M., 194 See Zonneveld, C., 23
See Thompson, J.T., 200 Koppelman, J.B. See lse ly, J.J., 99
Kiesecker, J.M ., 242 Koslow, J.A., 243
See Skelly, O.K. , 248 Kotake, A., 243
Kilham, S.S. See Nelson , D.M., 22 Koueta, N. See Villanueva, R., 201
Kim, J., 58 Kovach, J.T. See Knapp, R.A. , 242
Kim, J.N. See Hayashi , K.-I., 98 Koyama, T. See Kitamura, M., 58
Kim, S.H., 242 Koziumi , N. See Baird, A.H., 54
Kimmener, W.J. See Smith, S.Y., 62 Kraak, S.B.M., 243
380
AUTHOR INDEX
Kramer, D.L. See C hapma n, M.R., 284 Lambert, Y. See Marsha ll C.T., 36 1
See Lawson, G .L., 289 Lancaster, J. , 99, 100
Kraus, R.T., 327 Landergren, P. See Limburg, K.E., 328
See Kerr, L.A., 327 Landsea, C. See He nderson-Sellers, A., 287
Kremb, S.G . See Wild, C., 295 Lang, J.C. See Soong, K., 294
Kris hn an, V.V. See Stamps, J.A ., 249 Lang, M.A., 194
Kri stense n, P. See Revill , A., 102 Lan gdon, C. See Kley pas, J.A., 288
Kristensen , P.S. See Van Marlen , B., 104 Lange, C. B. See Jackson, J.B.C. , 58, 288
Kristi ansson, P. See Limburg, K. E., 328 Lange, K. 22
Kri stofferson, A.H. See Halde n, N.M., 326 See Oya rzun , F.J., 22
Kroncke, I. See Hin z, H. , 99 Lan genbuch, M. See Portner, H.O., 198
Krug, P.J., 243 Lanyon, J.M . See Burgess, E.A., 237
Kuang, Y. See Li, B.T., 22 Lan zavecchia, G. See de Eguileor, M., 189
Kuba, M. See Meisel, D.V., 195 Lapsley, C.T. See Beckerma n, A.P., 236
Kubodera, T., 194 See Plaistow, S.J., 247
See Norman, M.D. , 196 Lardies, M.A ., 243
Kubota, H. See Takasuka, A., 363 Larkum, AW.D., 59
Kubota, T. See Okutan i, T., 197 See Diaz-Pulido, G., 55
Kudo, S., 243 La Roche, J. See Geider, R.J ., 21
Kuffner, I.B. , 58, 59 Larrain, A. See Soto, E., 248
Kuhl , H., 99 Larso n, H.K., 289
Kuhl , M., 59 Laterveer, M. See Petersen, D. , 61
See Larkum, A.W.D. , 59 Latkoczy, C. See Thorrold , S.R., 330
Kuhlm ann , H.J . See Van Ma rlen , B., 104 Laurence, G.C., 361
Kuipers, B.R., 99 See Buckley, L.J., 237
See Janssen G.M., 99 Laurent, T. See Kurc, G., 100
Kujawksi, T. See Rumohr, H., 102 Lawford , A.L. See Carruthers, J.N ., 359
Kulbicki, M., 289 Lawler, A .R. See Addi son, J.T., 94
See Bozec, Y.M., 284 Lawler, S.P., 243
Kulk a, OW. See Rose, G.A., 362 See Naee m, S., 291
Kunito, T. See Arai, T., 324 Lawren ce, A .D. See C roft, M.T. , 19
Kuntz, N.M. See Kline, D. I. , 58 Lawre nce, A.L. See Castille, F.L., 188
Kunugi, M. See Watanabe, M ., 23 Lawrence, J.M . See George, S.B., 240
Kunz, T.J. See Poloczanska, E.S. , 292 Laws, E.A., 22
Kurc, G., 100 See Liu , H., 22
Kurihara, A., 194 See Smith, S.V., 62
See Okum ura, S., 197 Lawson, G.L., 289
Kustk a, A., 22 Law ton, J.H ., 289
Kuwada, H. See Tsukamoto, K., 330 See Naeem , S., 29 1
Kuwamura, T., 289 Lea, OW. See Swearer, S.E., 249, 329
Kvarn emo, C. See Forsgren, E., 240 Leadbeater, B.S.C., 22
Kvarnemo, L. See Mag nhagen, C., 244 Lebour, M.V. , 100
Lecchini , D., 289
Lede rhouse, R.C. See Gross muell e r, D.W., 241
L Ledli e, M .H., 289
Lee, P.A. See Bertrand, E.M ., 19
Labat, J.-P. , 100 Lee, P.G., 194
Lacey, E.P., 243 See Vidal, E.A.G., 20 1
Ladd , C. See Mueter, F.J., 362 Lee, S.C., 289
La fferty, K.D. See Roberts, C.M., 293 Le Gall, M.M. See Za mbonino- lnfante, J.L. , 202
Laforsch, C. See Agrawal, A.A., 235 Legawa, R. See Baird, A.H., 283
Lagardere, F. See Amara, R. , 236 Lege ndre, L., Moussea u, L. , 362
Lago, M.J. See Fuentes, L., 190 Legendre, R. Se Bouxin , J., 187
See Igles ias, J., 192 Leggett , W.C. , 100, 331-363, 36 1
Lall, S.P., 194 See Bertra m D.F. , 359
Lalli, C. M., 194 See Carscadden, J.E., 359
Lam, JW.H. See Bath, G.E. , 324 See Chambers, R.C., 238, 359
See Secor, D.H., 329 See Choi, J.S ., 359
Lambert, W.J. See Jones, H.L. , 242 See Dower, J.F. , 360
381
AUTHOR INDEX
See Frank, K.T., 360 Lipinski, M.R. See Hovin g, H.J.T. , 192
See Litvak M.K ., 361 See Venter, J.D., 201
Lehman, J.T., 22 Litchman, E. See Klausmeier, C.A., 22
Leichter, J.J. See Wing, S.R., 63 Little, C.M. See Donner, S.D., 285
Le me, M.H.D., 243 Littler, D.S. See Littler, M.M., 59
Lengfellner, K. See Sommer, U., 200 Littler, M.M., 59, 361
Leniham, H.S. See Jackson, J.B.C., 58, 288 Liu, H., 22
See Penin , L., 292 Liu, X. See Deng, Y.W. , 239
Lenz, 1. See Harris, R.P., 192 Livingston, M.E. See Kalish, J.M ., 327
Lenz, S., 194 Livnat, A., 243
Leonardi, M.G. See de Eguileor, M., 189 Llewellyn , G. See Mumby, P.J., 291
Leonardos, N., 22 Lloyd, A.J., 100
Leslie, H. See Roberts, C.M., 293 Loader, C., 243
Leslie, H.M. , 243 Lofqvist, J. See Anderson, P., 236
Le Souef, A.S., 194 Lohan, M.C. See Bertrand, E.M., 19
Lesser, M.P. , 59, 289 Lohmann, K.C. See Surge, D.M., 329
Lessios, H.A., 59 Long, S.M., 194
Letourneur, Y., 289 Longerich, H. See Campana, S.E., 325
See Graham, N.A.J., 286 Lonsdale, D.J ., I 00
Lett, C., 361 Lopez, D. See Gonzalez, M.L. , 191
Levin , L.A . See Becker, B.J., 236 Lopez, G.R. See Wallace, W.G ., 250
Levin, S.A. See Klausmeier, C .A., 22 Lorenzo, A. See Quintana, D., 198
See Livnat, A., 243 Lotze, H.K. See Diaz-Pulido, G., 55
Levinton, J. See Martinez, D.E., 244 Loucks, R.H. See Sutcliffe, W.H., 363
Levinton, J.S., 243 Lough, J.M., 289
See Lonsdale, D.J. , 100 See Hughes, T.P., 57, 288
See Wallace, W.G. , 250 See Pelejero, C., 292
Levitan, D.R., 243 Lovern, M.B. See Warner, D.A., 250
Low, P.J. See Perry, A.L., 292
Lewis, A.R., 289
Lowe, D.M. See Bayne, B.L., 236
Lewis, S.M., 59
Lowerre, J.M. See Lowerre-Barbieri, S.K., 361
Li, B.T., 22
Lowerre-Barbieri, S.K., 361
Li, Y.H., 327
Loya, Y. , 289
Li, Z. See Hui, C., 361
See Stone, L., 294
Libby, D. A. See Townsend, OW., 330
Lu, C.C., 194
Liermann , M., 361
See Clarke, M.R ., 189
Lighthill , 1. See Henderson-Sellers, A., 287
Lu, Z. See Popper, A.N. , 328
Lillebo, A. I. See Pardal, M.A., 246
Lubchenco, 1. See Olson, A.M., 61
Lilly, G.R., 361
See Roberts, C.M., 293
See Olsen, E.M., 246, 362
Lucas, V. See Potier, M., 198
Limburg, K.E. , 327, 328
Lucero, M.T., 194
See Elsdon, T.S., 297-330
See Gilly, W.F., 191
Lin, H.C., 243
Luckhurst, B.E., 289
Linares, F. See Iglesias, 1., 193
Luck hurst, K. See Luckhurst, B.E., 289
See Moxica, C., l95
LUdemann, K. See Berghahn, R., 95
Lindahl, U., 289
Ludsin, S.A., 328
See Garpe, K.C., 286 Lumby, J.R. See Rees, W.J., 198
See Spurgeon, J.P.G., 294 Lunn, K.E ., 289
Lindeman, K.C . See Mumby, P.J., 291 Lunow, C. See Jones, G.P., 242, 327
Linden, 0. See Westmacott , S., 295 Lyman, S.J . See Crowder, L.B., 238
Lindgren , A.R. See Strugnell, J.M., 200 Lynch, M., 243
Lindsay, K. See Orr, J.C., 292 Lysyk, T.J., 243
Lindstrom, J., 243
Lindstrom, K. See Klug, H., 242
See Pampoulie, C., 246
M
Linquist , N., 59
Linsenmair, K.E. See Spieler, M. , 248 Maas , P. See Cunningham, A., 19
Lipcius, R.N. See Gascoigne, J., 360 Mace, G.M. See Purvis, A., 293
382
AUTHOR INDEX
Macer, CT., I00 Marshall , J.F. See Pelejero, C., 292

See Pope, J.G . Marshall, P., 289
MacFarlane, J.W., 243 See Hu ghes, T.P., 57, 288
Machano, H. See McClanahan , T.R. , 290 See Orpin, A.R ., 292
Machavaram, M.Y. See Solomon, C.T., 329 Marshall , P.A ., 290
Mac intyre, H.L. See Geider, R.J ., 21 See Baird, A.H., 283
Mad a n, J.J., 194 See McCl a na han , T.R ., 290
Madin , J.S ., 289 Ma rteinsdottir, G., 244, 36 1
Maeda, S. See Itam i, K. , 193 See Scott B.E., 363
Maelfait, J.P. See Hendri ckx, F., 24 1 Marthy, H.J ., 195
Magi, E. See G rott i, M., 326 Martin , G.B., 328
Magnhagen, C., 244 Martin , W. , 100
See Berglund, A., 236 Martin , A.Y. See Hern andez-G arcia, V., 192
Magnuson, J.J., 36 1 Martinez, D.E. , 244
Mahyiddin , D. See Baird , A.H ., 283 Martin -Jezeq ue l, V. See Flynn , K.J. , 21
Ma ida, M. , 59 Martin s, R.S. See Vida l, E.A.G., 20 1
Maier-Rei mer, E. See Orr, J.C., 292 Martin -Smith, K.M., 59
Maina, J. See McC la na han, T.R., 59, 290 Maruyama, K. Hamasa ki, K., 192
Mancera, J.M . See Morote, E., 195 Mary, C.M .S. See Klu g, H., 242
Mandak, B., 244 Maske, H., 22
Maneiro, I. See Guisande, C., 241 Maskell , K. See Hought o n, J.T. , 287
Mangi , S. See McC lan a ha n, T.R., 59, 290 Masson , M. See Gabrie, C., 56
Massot, M ., 244
Mangold, K., 194
See Sorci, G., 248
See Nixon, M., 196
Mastain, 0 . See Mo uney rac, C., 245
See O' Dor, R.K., 196
Matear, R. See Orr, J.C., 292
See Wells, M.J., 202
See Polocza nska, E.S ., 292
Mangold-Wirz, K., 194
Mather, J. See Meisel, D.V. , 195
Mann , K.H. See John son, C.R. , 58
Matilla, J., 100
Mann, N.H. See Helda l, M., 2 1
Matsunaga , K. See Suzuki, Y., 62
Mann , R. See Bartol, I.K., 186
Mauche r, W.O., 100
Mantyka, C.S., 289
Mauro, A., 195
Ma rcha nd , J., 100
Maury, 0. See Poti er, M., 198
Marchetti , K. See Petersen , C.W., 246
May pa, A.P. , 59
Marijni ssen S.A .E. See Hiddink J.G., 99
See Raymundo, L.J ., 6 1
Markey, K.L., 59
McA lli ster, D.E. See Roberts, C.M., 293
Markle, D.F. See Toole, C.L. , 330
McArdle, D. See Pandolfi, J.M., 292
Markwitz, A., 328 See Robert s, C. M., 293
Marliave, J.B ., 194 McCabe, J. See Dunn, A.M ., 239
Marnane, M.J. , 289 McCa rthy, D.A., 245
Marques, J.C., 100 McCa rthy, J.J . See Goldman, J.C . 21
See Parda l, M.A., 246 McC lan a han, T., 290
Marq uez, F. See Ortiz, N., 197 See C inne r, J., 285
Marquez, L. , 194 See Goreau, T.F.. 286
See Quintana, D., 198 McClanahan , T.R. , 59, 290
Marqui s, C.P. See Baird, A.H., 54 See Graham, N.A.J., 286
Marqui s, F., 195 See Pratchett, M.S., 251-296
Marra, J. , 22 McClean, C .J. See Robe rt s, C.M., 293
Marsac, F. See Pot ier, M. , 198 McC le lland , J. See Va liel a, 1., 62
Marsh, H. See Arthur, R., 283 McClenachan , L. See Pandolfi , J.M ., 292
Marsh, S. J. See He nderson, P.A., 99 McColl in , D. See Ollerton, J. , 292
Marshall , C.T., 36 1 McConnau ghey, T.A ., 59
See Yaragina, N.A., 363 McCook, L. See Hu ghes. T.P., 58, 288
Marshall, D.J., 203-250, 244 McCook , L.J ., 59, 60
See Allen, R.M ., 235 See Birre ll , C.L., 25-63, 54
See Bennett, C. E., 236 See Ceccarelli, D.M ., 55
See Elkin, C. M., 239 See Diaz-Pulido, G. , 55, 285
See Evans, J.P., 239 See Jompa , J .. 58
383
AUTHOR INDEX
McCormick, M.l., 245, 290 Meyer, J. See Caperon, J., 19

See Berumen, M.L., 284 Meyer-Waarden, P.F., 100
See Feary, D. A., 285 Micaleff, H. , 100
See Gagliano, M., 240 Michael, S.W., 290
See Green, B.S., 240 Michalek-Wagner, K. , 60
See Jones, G.P., 288 See Haynes, D., 57
See Pratchett, M.S., 293 Micheli, F. See Mumby, P.J., 60, 291
McCulloch, M.T. See Patterson, H.M., 328 See Pandolfi , J.M., 61
See Sinclair, D.J., 329 Mickleson , J.M. See Droop, M.R., 20
See Pelejero, C., 292 Miclat, R.I. See Carpenter, K.E., 284
McEdward, L. See Em let, R., 239 Midgley, G.F. See Thomas, C. D., 294
McEdward, L.R., 245 Mileikovsky, S.A., 195
McEuen, F.S., 245 Miles, L. See Thomas, C.D., 294
McEvoy, J. See McEvoy, L.A., 245 Milicich, M.J. See Jones, G.P., 242, 327
McEvoy, L.A., 245 Miller, I. See Cheal, A.J., 284
McField, M. See McClanahan, T.R., 290 See Rogers, C.S., 62
McField, T. See McClanahan, T.R., 290 Miller, J.M. See Vander Veer, H.W., 103
McGinley, M.A., 245 Miller, M. See Steer, M.A., 249
McGuffie, K. See Henderson-Sellers, A., 287 Miller, M.B., 328
McKee, B.M. See Chesney, E.J., 325 Miller, M.J. See Kotake, A., 243
McKinnell, S., 328 Miller, M.W., 60
McKinnell, S.M. See Hay, D. E., 327 Miller, T.J. See Pepin, P., 362
McKinney, M.L. 290 Mills, D.J. See Proctor, C.H., 328
McKinnon, A.D. See Meekan, M.G., 362 Miloslavich, P., 245
McLaren, I.A ., 245 Milton, D. See Poloczanska, E.S., 292
McLaren, J.W. See Bath, G.E., 324 Milton , D.A., 328
See Campana, S.E., 325 Miramand, P. See Bustamante, P., 188
McLeod, E. See Salm, R.V., 293 Miranda , A. See Guisande, C., 241
McManus, J. See Bryant, D., 55 Miske, Y., 195
McManus, J.W., 290 Mistakidis, M.N., 100
McMillan, P.A. See Becker, B.J., 236 Mitani, I. See Takasuka, A., 363
Meekan, M. See Montgomery, J.C., 195 Mitchell, S.E., 245
Meekan, M.G., 362 Mitra , A. , 22
Mees, J., 100, 195 Mitsuhashi, M. See Ikeda, Y., 193
See Beyst, B., 95 Mittermeier, C.G. See Roberts, C.M., 293
See Cattrijsse, A., 96 Miyazaki, N. See Arai, T., 324
Meidel, K., 245 Miyazaki, T. , 195
Meijer, G.J. See Nagelkerken , 1., 29 1 Moberg, A. See Jones, P.D., 288
Meisel, D.V., 195 Moberg, F. See Nystrom , M. , 291
Meixner, R., 100 Mod in, J. See Gibson, R.N. , 98
Mejia, S.R. See Halden, N.M ., 326 Mohr, H., 101
Melendy, A.M. See Bruno, J.F. , 54 Moksness, E. See Fossum, P., 326
Me ltofte, H. See H\'lye, T.T. , 287 Moles, A.T., 245
Memmot, J. See Buckley, Y.M., 237 Moller, P., 101
Menard , F. See Potier, M., 198 Moller, A. See Stock, M., 103
Mendes, J.M. See Mumby, P.J., 29 1 Molloy, C.J . See Syrett, P.J., 23
Menge, B.A. See Ca ley, M.J., 237 Moltschaniwskyj, M.A. See Steer, M.A.,
Menze, A. See Walther, G.R., 295 Moltschaniwskyj, N. See Hughes, T.P., 58, 288
Mercier, A. See Hame l, J.F., 241 Moltschaniwskyj, N.A., 195
Merck , T. See Kattner, G., 99 See Hughes, T.P., 57, 288
Meredith, S.S., 100 Monfray, P. See Orr, J.C ., 292
Mesnil, B. See Mangold-Wirz, K., 194 Monks, A., 245
Messenger, J.B ., 195 Monod, J. , 22
See Han lon , R.T., 192 Montagnes , D.J.S. See de Figueiredo, G.H., 360
See Woodhams, P.L., 202 Montero, P. See Ruiz-Capillas, C., 198
Metaxas, A. See Meidel, K. , 245 Montgomery, J.C., 195
Metelo, I. See Pardal, M.A., 246 Montoya, J.E., 195
Metzner, J. See Fabric iu s, K.E. , 56 Moody, M.F., 195
384
AUTHOR INDEX
Moore, J.K., 22 Munoz, J.L. See Iglesias, J., 193

Moore, M.N. See Bayne, B.L., 236 See Mo rote, E., 195
Moore. R. See MacFarlane , J.W. , 243 Munoz, L. See Zuni ga, 0., 202
Moothien -Pillay, R. See McClanahan, T.R., 290 Munro, A.R., 328
Mora ito poulou-Kass imat i, E. See Papadopoulou , C., 327 Munro, P.T. , 10 1
Mo ra l, A. See Rui z-Capillas, C., 198 Muntz, W.R .A., 195
Mo ra les, J. See Rui z-Capillas, C., 198 See We ntworth , S.L., 202
Mora n, A.L., 245 Mur, L.R . See Ducobu , H., 20
Moran, M.J. See Edmonds, J.S. , 325 See Zevenboom, W., 23
Moran , P.J . See De'ath , G., 285 Murphy, E. F. See Lilly, G.R ., 36 1
Moreau , M.A. See Lunn , K.E. , 289 Muthiga, M. See Hoegh-Guldbe rg, 0. , 57
Moreira, F., 10 1 Muthiga, N.A. See McC la naha n, T.R ., 59, 290
Morel , F.M.M., 22 Muus, B., 195
Moret zsohn , F. See Tsuchiya, M. , 295 Muus, B.J., 101
Morgan, M.J. See Ol se n, E.M., 246, 362 Myers, D.L. See Rieman, B.E., 329
Morgan, S.G., 245 Myers, N., 29 1
Morin, P.J. See Lawler, S.P., 243 Myers, R.A. , 362
Morioka, T. See Hamasa ki , K., 19 1 See Fogarty, M.J ., 360
Morita, M. See Edmonds, J.S., 325
Mo rote, E., 195
Moroz, B.M. See Rombough, P.J., 198 N
Morse, A.N.C., 60
See Ba ird , A.H., 54 Naeem, S., 291
See Morse, D.E., 60 Naef, A., 195
See Raimondi , P.T., 6 1 Nagelkerken , 1., 291
Morse, D.E., 60 Naim, G. See Cuet , P., 55
Moss, B.L., 60 Naim, 0. See Pay ri , P.E., 61
Mosseau, T.A. See Fox, C.W., 240 Najjar, R.G. See Orr, J.C. , 292
Mouchet, A. See Orr, J.C., 292 Nakahara, M. See Miyaza ki , T., 195
Mouneyrac, C., 245 Nakahira, T. See Kud o, S., 243
Mo un y, P., 101 Nakai, K. See ltami , K. , 193
Moussea u, L., 362 Nakamura, K. See !ida, H., 193
Mousseau, T.A., 245 Nakamura, T., 291
Moxica, C., 195 Nakano, Y. See Kitamura, M ., 58
See Fuentes, L. , 190 See Loya, Y. , 289
See Iglesias, J ., 192, 193 Nakao, S. See ll ano, A.S., 242
Moya no, F. J. See Morote, E., 195 Nakashima, B. See Carscadden, J.E. , 359
Mueter, F.J., 362 Nakashima Y. See Kuwam ura, T., 289
Muir, B.S. See Sutcliffe, W.H ., 363 Nakazono, A. See Kok ita, T., 289
Muir, D.G. See Jo hn son, C.R., 58 See Sakaguchi, H., 199
Mukai , H. See Kobayashi, T., 242 Nanola, C.L. Jr. See McManu s, J.W. , 290
Mukminin. A. See Baird , A.H. , 283 Naser, M. See Zeke ria, Z.A., 296
Muko, S. , 60 Nash , R.D. M . See de Figueiredo, G.H., 360
Mumby, P.J., 60, 29 1 See Oh, C.-W., 10 1
See Box, S.J., 54 Nateewathana, A., 195
See Hoegh-G uldberg, 0., 57 Nathan, A. See Gauldie, R.W., 326
Munday, P.L. , 29 1 Navarro, J.C., 195
See Beger, M., 283 Navas , J. I. See Marq uez, L., 194
See Hobbs , J.P. , 287 Naylor, E. See AI-Adhub, A.H.Y., 94
See Pratchett, M.S., 251-296,293 Naylor, J.K ., 246
See Jones, G.P., 288 Negri, A . See Ha rrin gton, L., 56, 287
See Ohman, M.C., 29 1 Negri , A.P., 60
See Thompson, Y.J. , 295 See Heyward, A.J. , 57
See Wo ng, M., 296 See Markey, K.L., 59
Mundy, C., 60 See Webster, N.S., 63
See Babcock, R., 53 Neil son, J.D. See Carruthe rs, E. H., 359
Mun dy, C.N., 60 Nellen , W. See Diek ma nn , R., 189
Munkittrick, K.R ., 245,246 Nelson, D.M., 22
385
AUTHOR INDEX
Nesis, KN , 195, 196 0

Neudecker, T, See Revill, A., 102
See Van Marlen, B., 104 Obura, D. See McCook, L.J., 60
Neu shul, M. Amsler, C.D., 53 See Sm ith, J. E., 62
New man, M.J.H. See Pandolfi, J.M., 292 O'Cla ir, R. See Brocco, S.L., 187
Ng, D., 246 Odendaal , F.J., 246
See Singer, M.C., 248 O ' Dor, R.K., 196
Ngazy, Z ., 291 See Voight, J.R. , 201
Nichols, D.S. See Steer, M.A. , 249 See Well s, M.J., 202
Nichols, J.D. See Williams, B.K., 330 Odum , E.P. See Odum, H.T., 291
Nicholson, M.D. See Addison, J.T., 94 Odum , H.T., 291, 328
Nicieza, A.G. , 101 O'Farrell , M.R., 246
Nickell , L.A. See Gibso n, R.N., 98 Offner, N. See Boletzky, S.v., 187
Nielsen, N.A. See Daan, N., 97 O gde n, J.C. See Gladfelter, W.B., 286
Niel sen, R.L., Rieman, B. E., 329 See Pandolfi , J.M. , 6 1
Oh, C.W., 101 , 246
Nielson, A.E., 328
Oh, H.M. See Ahn, C.Y., 19
Nienhuis, P.H. See Nagelkerken , 1., 291
Ohk i, K. See Ikeya, T., 21
Nigmatullin , C.M. See Nesis , K.N. , 195
Ohman, M .C., 29 1,292
Nikitina, IV. See Nesis, K.N., 196
See Garpe, K.C. , 286
Nil sson , J.A . See Grindstaff, J.L., 241
See Lindahl, U., 289
Nil sson, P., 10 I
Ohsaki , N., 246
Nishimura, M. See lsomura, N., 242
Oka, H.P. See Kotake, A. , 243
Ni shioka, R.S., 196
Okaji , K. See Golbuu, Y. , 286
Nissling, A. See Vall in, L. , 363
Okamura, A. See Kotake, A., 243
Nival , S. See Halsband-Lenk, C., 241
Okey, T.A. See Polocza nska, E.S., 292
Nixon, M., 196
Okubo, S., 196, 197
Nixon, M. See Hochberg, F.G. , 192
Okumura, S., 197
Noble, A.E. See Bertrand, E.M., 19
See Igles ias, J., 193
Noble, L.R. See Gowland, F.C., 191
See Kurihara, A., 194
Noble, R.L. See lsely, J.J., 99
Okutani , T., 197
Nog uer, M. See Houghton, J.T. , 287
See Kubodera, T,, 194
Norambuena, H. See Buckley, Y.M., 237 O lafsson E.B . See Marilla , J. , 100
Norberg, J. See E lmq vist, T., 285 Olivares, A. See G utierrez- Pajares J.L., 19 1
Norcross, B.L. See Mueter, F.J. , 362 See Zuniga, 0., 202
Nordemer, I. See McClanahan, T.R. , 290 O livares-Paz, A. See Castro-Fuentes, H., 188
Norkko, A. , 101 Oliver, J., 61
See Bonsdorff, E., 96 See Orpin , A.R., 292
Norland , S. See Heldal , M., 21 Oliver, J.K. , 61
Norman , M.D. , 196 See Berkel ma ns, R., 283
See Hochberg, F.G., 192 See Willi s, B.L., 63
See Nateewatha na, A., 195 Ollerton, J. , 292
See Strugne ll , J. , 200 Olney, J. E. See Walthe r, B.D., 330
See Villanueva, R. , 105-202 Olofsso n, C . See Ol sson, M. , 246
No rth , E.W., 362 Ol se n, E. M ., 246 , 362
No rton, T.A. See Hruby, T. , 57 Olson, A.M., 61
Nose, Y. See Sa no, M. , 294 Olson , R.R. See Jo hn son, C.R., 58
Nouvel -van Rysselberge, L., 101 Ol sson, M., 246
Nozais , C. See Villanueva, R. , 20 1 Omori , M. , 197
Nuckols, J.R. See Gallagher, M .D., 240 See Morse, A.N.C., 60
Nugues, M.M., 60,6 1 O'Nea l. J. P. See Fuiman L.A., 360
See Hawkins, J.P., 287 Ooze ki , Y. See Takasuka, A., 363
Nystrom, M., 291 Opdyke, B.N. See Kleypas, J.A ., 288
See Bellwood, D.R. , 283 See Pelejero, C., 292
See E lmq vist, T. , 285 Oppenheimer, M. See Donner, S.D., 285
See Hughes, T, P., 57, 288 Orell i, M.v., 197
See McClanahan, T.R., 290 Ormond, R.F.G. See Robe rt s, C. M ., 293
See McCook , L.J ., 60 Orpin , A.R., 292
386
AUTHOR INDEX
Orr, J.C., 292 Parker, G.A., 246

Ortega-Huerta, M.A. See Thomas, C.D., 294 Parmesan, C., 292
Ortiz, N., 197 See Singer, M.C. , 248
Osborne, K. See Cheal, A.J., 284 See Walther, G.R., 295
Osenberg, C.W., 292 Parra, G., 197
O'Shea, S., 197 Parrish, B. B. See Carruthers, J.N., 359
Oshima, Y. See Kaneko, N., 193 Parrish, J.D. See Friedlander, A.M ., 286
Ostrander, G.K., 61, 292 Parrish, J.K . See Boersma, P.D., 284
Ota, M. See Furuya, H. , 190 Parriss, J.R. See Moody, M.F., 195
Otake, T. See Arai, T., 324 Parslow, J.S., 22
Otero, J., 197 Partington, D. See Shepherd, S.A., 363
See Gonzalez, A.F., 191 Pascoe, S. See Revill , A., 102
Otero, J.J . See Fuentes, L., 190 Pascual, M., 22
See Iglesias, J., 192, 193 Passarella, K.C., 197
See Moxica, C., 195 Patarnello, T. See Gysels, E.S., 98
Ottersen, G., 362 Patterson , H.M., 328
Ouellet, P. 246 Patterson , M.R. See Bartol, I.K ., 186
Overath, H., 197 Patton, WK ., 292
Overnell, J. See Craig, S., 189 Paul , C. See Amara, R. , 94
Owens, I.P.F.. 292 Paul , V.J. See Becerra, M.A., 54
Owens, N.J.P. See Clark, D.R., 19 See Kuffner, I. B., 58, 59
See Flynn, K.J., 21 Paulij , W.P., 197
Oyarzun, F.J., 22 Pawlik, J.R., 61
See Lange, K. 22 See Toonen, R.J., 249
Oyarzun, R.F. See Chaparro, O.R., 238 Payet, R. See Sheppard, C., 294
Payne, A.G., 246
Payri, P.E., 61
p Pearce, N.J.G. See Geffen , A.J., 326
Pearcy, W.G., 197
Paasche, E., 22
Peel, G., 246
Pacala, S.W. See Livnat, A., 243
Packard, A., 197 See Doubleday, Z., 190
Packard, T.T. See Blasco, D., 19 Peel, G.T., 197
Page, C.A. See Bruno, J.F., 54 See Semmens, J.M. , 199
Page, S. See Flynn, K.J., 21 Pelejero, C., 292
Palen, W.J., 246 Pella, J.J. See McKinnell , S., 328
Palmer, M.C. See Mueter, F.J., 362 Pellmyr, 0. See Thompson, J.N ., 249
Palumbi, R. See Roman , J., 102 Pen in, L., 292
Palumbi, S.R. See Hughes, T.P., 57, 288 Pen land , L. See Golbuu, Y., 286
Pampoulie, C., 246 Penven, P. See Lett, C., 361
See Gysels, E.S., 98 Pepin P., 362
Pandian, T.J., 101 Peplinska, A.M. See Syrett, P.J., 23
Pandolfi, J.M., 61,292 Peres, A. See Zambonino-lnfante, J.L., 202
See Hu ghes, T.P., 57, 288 Perez, M. See Gonzalez, M.L. , 191
See Jackso n, J.B .C., 58, 288 Perkins , E.J. See Abbott, O.J ., 94
Panfili, J. See Campana, S.E., 325 Perkins, W.T. See Geffen, A.J., 326
Pankhurst, N.W., 246 Perley, P. See Carruthers, E. H. , 359
See Conroy, A.M., 238 Perron, F. E. See Kohn , A.J., 242
Pantos, 0. See Smith, J.E., 62 Perry, A.L., 292
Papadopoulou, C., 328 Pescod, C.L. See Mumby, P.J., 291
Papaj, D.R. See Rausher, M.D., 247 Petersen, C.W., 246
Pappalardo, P. See Fernandez, M., 239, 240 Petersen, D., 61
Parciak, W. , 246 Peterson, C. H. See Jackson, J.B .C., 58
Pardal, ·M.A., 246 See Jackson, J.B.C., 288
Paredes, G. See Pandolfi, J.M., 292 Peterson, G . See Elmqvist, T., 285
Paris, C. B. See Cowen, R.K., 359 Petrie, B. See Choi , J.S. , 359
See Mumby, P.J., 60 See Drinkwater, K.F., 360
Parker, D.M. , 197 See Frank, K.T., 360
387
AUTHOR INDEX
Pet-Soede, L. See Cesar, H., 284 Porcher, M. See Gabrie, C., 56

See McClanahan, T.R., 290 Portmann, A. See Mangold, K., 194
See Westmacott, S., 295 Portner, H.O. , 198
Petz, A.M. See Shashar, N., 199 See Fernandez, M., 239, 240
Philipp, D.P. See lsely, J.J., 99 See Voight, J.R., 201
Philippart, C.J.M., 101 Possingham, H.P. See Pandolfi, J.M., 61
Phillips, O.L. See Thomas, C. D., 294 See Roberts, C.M., 293
Piatkowski, U., 198 Post, E. See H13ye, T.T. , 287
See Collins, M .A., 189 See Walther, G.R., 295
See Diekmann, R., 189 Potier, M., 198
Piccoli, P. See Campana, S.E., 325 Potts, D.C., 61
See Zlokovitz, E.R., 330 Poulin, E., 198
Piccoli, P.M. See Kimura, R. , 327 Powell, J.L. See Faure, G., 326
See Secor, D.H. , 329 Pratchett, M.S., 61, 251-296, 292, 293
Pierce, G.J. See Grisley, M.S., 191
See Baird, A.H., 54, 283
See Seixas, S., 199
See Berumen, M.L., 283, 284
Pihl, L., 101
See Hughes, T.P., 57, 58, 288
See Baden, S.P., 95
See Munday, P.L., 291
See Gibson, R.N., 98
See Wilson, S.K., 296
See Vander Veer, H.W., 103
Precht, W.F. See Aronson, R. B., 283
Piller, WE. See Riegl, B., 293
Prego, R. See Gonzalez, A.F., 191
Pimm, S.L., 292
Present, T.M .C. See Conover, D.A., 96
Pinazo, C. See Baklouti, M ., 19
Pin horn , A.T., 362 Price, T.D., 247
Pinn, E.H., 101 Priddy, J. See Crowder, L.B., 238
Piola, R.F., 246 Pritchard, J.K. , 328
Pischetola, M. See D'Aniello, A., 189 Proctor, C. H., 328
Piscopo, S. See Brown, E.R., 187 See Gunn, J.S., 326
Pitcairn, M. See Buckley, Y.M., 237 Pruett-Jones, S., 247
Pitts, P.A., 292 Przeslawski, R., 247
Plagmann, J., 101 Pueschel, C.M. See Keats, DW., 58
Plaistow, S.J., 247 Purcell, SW., 61
Planes, S. See Jones, G.P. , 327 Purps, M. See Berghahn, R., 95
See Thorrold, S.R., 330 Purvis, A., 293
Plante, F. See Ouellet, P. 246 Pysek, P. See Mandak , B. , 244
Platt, T. , 362
Plattner, G. See Orr, J.C., 292
Ploberger, W. See Meisel , D.V., 195 Q
Podolsky, R.D. See Allen, J.D. , 235
Pogodina, A.R. See Solomon, C.T., 329 Qian, P.Y., 247
Polet, H., 101, 102 Quan-Young, L.I., 61
See Revill, A., 102 Quazuguel , P. See Zambon ino-lnfante, J.L. , 202
See Van Marlen, B., 104 Queguiner, B. See Baklouti, M. , 19
Poloczanska, E.S., 292 Querner, F.v. , 198
Po lunin, N.V.C. See Dulvy, N.K., 285 Quinlan, J.A. See Stegmann, P.M, 363
See Graham, N.A.J., 286 Quinn, G.P. , 328
See Jennings, S., 288 Quinonez-Velazquez, C. See Fortier, L., 360
See Ledlie, M.H., 289 Quintana, D., 198
See McClanahan, T.R., 290 See Marquez, L. , 194
See Pratchett, M.S., 251-296, 293 Quintana-Fellay, A. See Castro- Fuentes, H., 188
See William s, I.D., 296 Quintero, M.E. See Balguerfas, E. , 186
See Wilson, S.K., 296 Qvarnstrom, A. See Price, T.D., 247
Pond , D., 247
Pondaven, P. See Fasham, M.J.R., 20
Poore, A.G.B., 247
R
Pope, J.G., 362
See Shepherd, J.G. , 363 Radcliffe, C. See Revill , A. , 102
Pope, S.K. See Cobb, C.S., 189 See Van Marlen, B., 104
Popper, A.N., 328 Radke, C. D. See Renwick, J.A.A., 247
388
AUTHOR INDEX
Radtke, R.L ., 329 Reyes, R.B. Jr. See McManu s, J.W., 290
See Tow nsend , D.W., 330 Reyesgav il a n, F.G . See Nicieza, A.G., 101
Raimondi, P.T., 6 1 Reynolds, J.D. See Dulvy, N.K. , 285
See Morse, D. E., 60 See Hutchings, J.A., 242, 36 1
Ra in bow, P.S., 247 See Perry, A.L. , 292
See Mouney rac, C., 245 Reynolds, K.E. See Schultz, E.T., 102
Ra itt, R.W. See Eyring, C.F. , 190 Reysenbach, A.L. See John son, C.R., 58
Rajagopa lan, B. See Stone, L., 294 Rhee, G.-Y., 23
Rajasuriya, A. See Ohman, M.C., 292 See Gotham, l.J., 21
Ra made, F., 6 1 Riba , J. See Villanueva, R., 20 1
Ra maekers, G. See Boddeke, R., 96 Richardson, A.J. See Hays, G.C., 192
Raman i, P. See Sc iandra, A., 23 See Poloczanska, E.S., 292
Ramirez- Liodra, E.R., 247 Richmond , R.H., 6 1
Ramos-Es pl a, A. See Gil landers, B.M., 326 Ricker, W. E., 362
Rancure l, P. , 198 Ridd , P.V. See Orpin, A.R., 292
Ra nd al l, J.E., 293 Riebese ll, U. See Sommer, U., 200
Rasheed, M.Y.M . See Wild , C., 295 Riegl, B., 6 1, 293
Rauck, G., 102 Rieman, B.E., 329
See Mohr, H. , 101 See Wells , B.K., 330
Rau sher, M.D., 247 Riemann , S. See Rev ill , A. , 102
See Odendaal , F.J., 246 See Van Marlen, B., 104
Raux-Dee ry, E. See Croft, M.T., 19 Riesselman, C.R. See Bertra nd , E.M., 19
Raven , J.A., 22 , 23 Ri gby, P.R. See Semmens, J.M ., 199
See Diaz- Pulido, G., 55 Rijnsdorp, A.D., 102, 362
See Kustka, A. , 22 See VanBeek, F.A ., 103
Raven , P.H. See Ehrli ch, P.R ., 239 See Van der Vee r, H.W., 103
Raviliou s, C. See Spalding, M.D., 294 Rinkevich, J. See Epstein , N., 56
Raymundo, L.J ., 6 1 Risk, M.J ., 293
See Maypa, A.P., 59 Ritson-Williams, R. See Kuffner, I.B., 59
Razo uls, S., 198 Rivaro, P. See Grotti, M., 326
Re, M .A. See Ortiz, N., 197 River, G.F., 61
Read. A.F. See Mit chell , S.E., 245 Rivera, W. See Baltazar, P., 186
Red ant, F., I02 Rivest, B.R., 247
See Polet, H., 102 Roac h, D.A ., 247
See Rev ill, A., 102 Robb, L. See Gibson , R.N., 98
See Va n Marle n, B., 104 Robbin s, W.D. See Choat, J.H., 285
Redfi eld, A.C., 23 Roberts, C.M ., 293
Reed, D.C., 6 1 See Hawkins, J.P., 287
See Ams le r, C. D.. 53 See Nagelkerken, 1., 291
See Hughes, T.P. , 57 See Nugues , M.M., 60
Rees, M. See Buckley, Y.M ., 237 Roberts, M.J. See Vid a l, E.A.G ., 20 1
Rees, W.J ., 198 Robertson, J.D .. 198
Reichelt-Brushett, A.J. , 61 Robin . J.-P.. 102
Reid, M.L. See Stamps, J.A. , 249 Robinson, C. See Hays, G.C., 192
Reipschlager, A. See Portner, H.O., 198 Rob in son, J. See Graham, N.A.J., 286
Rei se, K., 102 Robson, D.S. See Brownie, C., 324
Reist, J.D. See Halden, N. M., 326 Robson , G.C. , 198
Relyea , R.A., 247 See Jo ubin , L. , 193
Rengefors, K. See Gustafsson, S., 241 Rocha, F. , 198
Renken, H. See Mumby, P.J., 29 1 Rocha, F.J. See Gonzalez, A.F., 191
Re nwick, J.A.A., 247 Roche, H. See Ramade, F., 6 1
Reschenhofe r, E. See Mei sel, D.V., 195 Rockstrom, J. See Adger, W.N., 283
Resetarit s, W.J ., 247 Rod gers, K.B . See Orr, J.C. , 292
Resh, V.H. See Bergey, E.A., 54 Rodhouse, P.G. , 198
Rev ill , A., 102 Rodri gues, M.J . See Hughes, T.P., 58, 288
See Jeffer y, S., 99 See McClanahan , T.R., 290
See Van Marlen, B., 104 Rodri guez, A. See Dra ke, P., 97
Revill, A.S., 102 Rodrig uez, C. See Carrasco, J.F. , 188
Revsbech, N.P. See Kuhl , M., 59 Rodrig uez, E. See Quintana, D., 198
389
AUTHOR INDEX
Rodriguez, M. See Carrasco, J.F., 188 Saborowski , R. See Schatte, J., 102
See Morote, E., 195 Sachse, M. See Budelmann, B.U., 188
Rodriguez, P. See Baltazar, P. , 186 Sadeghi , H., 248
Roeleveld , M .A.C. See Villanueva, R. , 201 Sadovy, Y., 329
Roess ig, J.M., 293 See Chan, T.T.C ., 284
Roff, D.A., 102 See Cole, K.S., 238
Rogers, C.S., 62 See Dulvy, N.K., 285
Rogers, R.W., 62 Sadovy, Y.J. , 293
Rohlin g, E.J., 329 Safran , P., 102
Rohwer, F. See Kline, D.!., 58 Sainte-Marie, B., 248
Rohwer, F.L. See Smith, J.E., 62 Saito, M.A. See Bertrand, E.M., 19
Roit z, J.S., 329 Saji . N.H. , 293
Roman, J., 102 Sakaguchi, H., 199
Rombough, P.J., 198 Sakai , K. See Loya, Y., 289
Roo, J. See Fernandez-L6pez, A., 190 See Muko, S., 60
See Iglesias, J., 193 Sakai , S., 248
Rooker, J.R. , 329 Sakamoto, W. See Ikeda, Y., 193
See Secor, D.H., 329 Sala, E. See McClana han , T.R., 290
Roper, C.F E. See Jereb, P., 193 See Pandolfi, J.M ., 61, 292
See Boucaud-Camou , E., 187 See Smith, J.E., 62
See Sweeney, M.J. , 200 Sale, P.F., 293
Rose, G.A., 362 See Hoegh-Guldberg, 0., 57
Rose, J.M. See Bertrand, E.M., 19 Salih, A. See Baird, A.H.
Rosecchi , E. See Gellin, A., 98 Salm, R. See McCook, L.J., 60
See Pampoulie, C., 246 Salm, R.V., 293
Rosen, B. See Hughes, T.P., 57, 288 See West, J.M., 295
Rosen , D. See Rosenheim, J.A. , 247 Salle, R. See Eriksen, M.S., 239
Rosenbe rg, N.D. See Ruggieri, G.D., 198 Sal vat, B., 62
Rosenberg, R. See Moller, P., 101 See Hoegh-Guldberg, 0., 287
See Pihl , L. , 101 Sambali, H. See Loya, Y. , 289
Rosenheim, J.A., 247 Sammarco, P.W., 62
Rosenqvi st, G. See Berglund, A., 236 See Maida, M. , 59
Rosenthal , H.L., 329 Sampedro, M.P. , 248
R!'lsner, H.U. See Berghahn, R., 95 Samways, M.J. , 293
Rossiter, M., 247, 248 See Floros, C. D. , 285
Rossiter, M.C., 247 Sanchez, J. See Guisande, C., 241
Roth schild , B.J., 362 Sanchez, F.J. See Fuentes, L. , 190
Roughgarden , J. See Hughes, T.P. , 57, 288 See Igl es ias, J. , 192
Roy, C. See Cury, P., 189, 359 See Moxica, C., 195
Ruckel shau s, M. See Robert s, C.M ., 293 Sanchez, J. See Igles ias, J. , 193
Rudi , E. See Baird, A. H., 283 Sanchez, P. See Villanueva, R., 20 1
Ruggieri , G. D. , 198 Sanchez-Jerez, P. See Gillanders, B.M., 326
Ruiz Sebastian, C . See McClanahan, T.R. , 290 Sanchirico, J.N. See Mumby, P.J. , 291
Ruiz-Capillas, C. , 198 Sand, 0. See Packard , A., 197
See Villanueva, R., 201 Sandberg, E. See Bonsdo rff, E., 96
Ruiz-Tag le, N. See Fernandez, M. , 240 Sandell, M. See Grindstaff, J.L., 241
Rumohr, H., 102 Sanders, G.D. See Packard, A., 197
Russ, G.R., 293 Sandin, S.A. See Smith, J.E., 62
See Klumpp, D.W., 287 See Vermeij, M.J.A. , 63
Ruth, M. See Stock, M., 103 Sandow, M. See Sommer, U., 200
Rutledge, P.S . See Shashar, N., 199 Sankey, S.A., 102
Ryan, D. See Halford, A., 287 Sano, M .. 294
Rylaarsdam , K.W. , 62 San tel ices, B., 248
Sanudo-Wilhelmy, S. See Kustka, A., 22
Sargent, J.R. , 199
s See Henderson, R.J., 192
Sargent, R.C., 248
Sabatie, R. See Potier, M. , 198 Sarmiento, J.L. See Orr, J.C. , 292
Sabine, C.L. See Orr, J.C., 292 Sarvesan, R .. 199
390
•
AUTHOR INDEX
Sasaki, M., 199 See Rooker, J.R., 329

Sasal , P. See Pampoulie, C., 246 See Wingate, R.L. , 330
Sato, Y. See Oh sa ki , N., 246 See Zlokovitz, E. R. , 330
Satoh, S. See Watanabe, T., 20 I Segawa, S. See Shigeno, S ., 199
Savage, Y.M., 23 Seger, J. , 248
Savitz, D. A. See Gallagher, M.D., 240 Seixas, S., 199
Scanlan, D.J. See Heldal , M ., 2 1 Seki , M.P. See Bower, J.R., 187
Schaffel ke, B., 62 Sekiya, S. See Tsukamoto, K., 330
See Di az- Pulido, G., 55 Selig, E.R. , See Bruno, J.F. , 54
Schatte, J., I02 Semme ns, J.M., 199
Scheel, D., 199 See Doubleday, Z., 190
Scheer, G. See Eibl-Eibesfeldt, 1., 190 Sepkoski , J.J . Jr, 294
Scheffer, M . See Folke, C., 56 Severin , K.P. See Campana, S.E., 325
Scheibling, R.E . See Meidel , K., 245 See Sadovy, Y. , 329
Schelten, C. See Hawk in s, J.P., 287 Sewell , A.T. See Dugg ins, D.O. , 55
Schelten, C.K. See Lindahl, U., 289 Shackell , N.L. See Frank, K.T., 360
Schindler, D.E. Pal en, W.J., 246 Shafir, S.H. See McC lanahan , T.R. , 290
Schinner, G.O. See Bierma nn , C.H ., 237 Shanks, A.L., 199, 248
Schipp, R. See Budelmann , B.U., 188 Shannon, L.J. See Boyd, A.J ., 359
Schlit zer, R. See Orr, J.C ., 292 Shashar, N ., 199
Schmidt, N.M. See H0ye, T.T. , 287 Shaw, M. See Smith, J.E .. 62
Schmidtberg, H., 199 Shaw, R. See Buckley, Y.M ., 237
Schmith, E. B. See Soto, E., 248 Sheader, M. , 248
Schmitt, R.J., 294 Shears, T.H. See Pepin, P., 362
See Holbrook, S.J., 287 Sheaves, M. See Munday, P.L. , 291
Schneider, M. See Diekmann, R., 189 She lton, P.A., 363
Schockaert, E., 102 See Lilly, G.R., 361
Schoener, T.W., 294 Shepherd, A.R.D. See Robert s, C.M., 293
Schofield, K.A. See Kali sh, J.M., 327 Shepherd, J.G ., 363
Schomann , H. See Rumohr, H., 102 Shepherd, S.A., 363
School, A. See Marthy, H.J ., 195 Sheppard, A. See Sheppard, C., 294
Schrey, E. See Stock. M. , 103 Sheppard, A.W. See Buckley, Y.M ., 237
Schrimm, M. See Pen in , L. , 292 Sheppard, C., 294
Schroder, S., 329 Sheppard, C.R .C., 294
Schueler. F.W. See Roberts, C. M. , 293 Sheridan , P.F. See Gillanders, B.M., 326
Schuhmacher, H. See Peterse n, D.. 6 1 Sherwood. K. See Graham , T., 286
Schulien, F.N. See Boyd, A.J. , 359 Shibuno, T. , 294
Schult z, E.T., I02 Shieh, S. See He nde rso n-Sellers, A. , 287
Schumacher. A. See Tiews, K., 103 Shi geno, S., 199
Schuttenberg, H. See Marshall . P. , 289 See Kasugai , T. , 193
Schwa rz, C.J., 329 Shi gesada , N. See Muko, S., 60
Schwenzer, D.E. See Bulnheim, H.P., 96 Shima, J. See Lecc hini , D.. 289
Sciandra, A., 23 Shima. J.S., 248
Scott, B., 363 See Osenberg, C.W., 292
Scott. B.E., 363 Shi rnek. R.L., 248
Scott. J.M. See Droop, M.R ., 20 Shimi zu, M. See Sano, M., 294
Scully, E.P. See Ostra nder, G.K. , 6 1, 292 Shimoike, K. See Morse, A.N.C. , 60
Seabra, M.l. See Nug ues, M.M., 6 1 Shine, R., 248
Seaby, R.M. See Henderson, P.A., 99 See Wa rner, D.A., 250
Seale, D. B., 248 Shiraki. M. , 199
Searcy, S.P., 248 Shok ri, M .. R., 294
Sebast ian, C.R. See McC lana han , T.R ., 290 Siddo n, C. E. See Eckman , J.E., 56
Seber, G.A .F. , 329 Sidie, J., 199
Secor, D. H., 329 Sie, S.H. See Campana, S.E., 325
See Campana, S.E. , 325 See Proctor, C.H., 328
See Elsdon, T.S ., 297-330 Siegel, D.l. See Limburg, K.E., 328
See Kerr, L. A., 327 Siemelink, M .E. See Boddeke, R., 96
See Kimura, R., 327 Sih, A. See DeWitt, T.J., 239
See Kraus, R.T. , 327 Sikorski, Z.E. , 199
39 1
AUTHOR INDEX
Silva-Garcia, A. See Drake, P., 97 Somerton, D.A. See Munro, P.T., 101
Simon, 1. E. See Frank , K.T. , 360 Somes, J.R. See Henderson, P.A ., 99
Simpson, S.D. See Montgomery, J.C. , 195 Sommer, U., 200
Sinclair, A.F. See Swain, D.P., 249 Soong, K., 294
See Swain, D.P., 363 Sorci, G., 248
Sinclair, D.J. , 329 Soto, E., 248
Sinclair, M ., 363 Sousa-Reis, C., 200
Singer, M.C., 248 Spaargaren, D.H., 103
Singley, C.T. See Arnold , J.M., 186 Spagnol, S. See McCook, L.J. , 60
Siregar, A.M. See Baird, A.H., 283 Spa ld ing, M. See Bryant, D., 55
Skadsheim, A., 248 See Roberts, C .M. , 293
Skelly, O.K ., 248 Spalding, M.D. , 294
See Kiesecker, J.M ., 242 Spalding, S. See Sheppard , C.R .C., 294
Skirving, W.J. See Berkel mans, R., 54, 283 Sparta, A., 200
See Donne r, S.D., 285 Speelmans, M. See Hendrickx, F., 241
Skjoldal, H.R. See Harris, R.P., 192 . Speight, M.R . See Gratwicke, B., 286
Sklyar, V.Y. See Timofeev, S.F., 249 Spencer, B. E. See Kaiser, M.J., 99, 288
Slater, R.D. See Orr, J.C., 292 Spieler, M., 248
Slattery, M. See Bosch, 1., 237 Spijkerman, E., 23
Smaldon , G., 102, 103 Sponaugle, S. See Grorud-Colvert, K., 241
Smale, M.J., 199 See Searcy, S.P., 248
Small, A .M . See McConnaughey, T.A ., 59 Sprung, M., 103
Small, L.F. See Donaghay, P.L., 20 Spurgeon, J.P.G. , 294
Smedbol, R.K., 363 Sram, R.J. , 249
Smigielski, A.S. See Buckley, L.J. , 237 Srinivasan, A. See Cowen, R.K., 359
Sm.iley, J., 248 Srinivasan, M ., 294
Smith, A.G . See Croft, M.T., 19 See Ignatius, B., 193
Smith, A.M. See Kier, W.M ., 194 See Jones, G.P., 288
Smith, B.D. See Mouneyrac, C., 245 St. John, J. See Ca ley, M.J ., 284
See Rainbow, P.S., 247 St. John, M. See Hinricksen , H.- H. , 360
Smith, C. See Payne, A.G., 246 St. Mary, C.M. See Osenberg, C.W., 292
Sm ith , C.C., 248 Staines, M.E. See Blaxter, J.H.S. , 186
Smith, C. D., 199 Stallones, L. See Ga ll agher, M.D., 240
Smith, C.M. See Yermeij, M.J.A., 63 Starn, A. See Berg man , M.J.N. , 95
See Walters, L.J., 63 Stamps, J.A., 249
Smith, D.C. See Koslow, J.A. , 243 Stamski , R.E. , 62
Smith, G.W. See Nugues, M.M ., 61 Stansbury, D.E. See Lilly, G.R., 361
Smith, H.G. See Gr indstaff, J.L., 24 1 Stanton, M.L. , 249
Smith , H.L. , 23 Starger, C.J. See McC lanahan, T.R., 59
Smith, J.E., 62 Staudigl, M. See Budelmann, B.U., 188
See Diaz-Pulido, G., 55 Steck is, R.A. See Edmonds, J.S., 325
See Sc haffelke, B., 62 Steel , W.J., See Sale, P.F., 293
See Yermeij , M.J.A., 63 Steele, 1. H. , 294
Smith, L.D. See Webster, N.S., 63 See Edwards, R., 97
Smith, L.W. , 294 Steene, R. See A llen, G.R., 283
Smith, ME. See Fuiman L.A. , 360 Steene, R.C. See Randall , J.E., 293
Sm ith , P.C. See Drinkwater, K.F., 360 Steer, M.A., 249
Smith, P.J.S. See Wells, M.J. , 202 See Peel , G .T., 197
Smith, R.E.H ., 23 Stegmann, P.M, 363
Smith, S.Y., 62, 294 Steinarsso n, A. See Marteinsdotlir, G., 361
Smouse, P.E., 329 Steinberg, P.O. See de Nys , R., 55
Smriga, S. See Smi th, J.E., 62 See Marshall , D.J., 244
Snyder, S., 200 See Wright , J .T., 250
Sobri no, I. See Drake, P. , 97 Steneck, R.S., 62
See Semmens, J.M ., 199 See Diaz-Pulido, G., 55
Socorro, J. See Ferna ndez- Lopez, A., 190 See Hoegh-Guldberg, 0., 57
Sogard, S.M. See Berkeley, S.A., 236, 359 See Hughes, T.P., 57, 58, 288
Soggia, F. See Grotli, M. , 326 See Jack son, J.B.C., 58, 288
Solomon, C.T., 329 Stenning, M.J., 249
392
AUTHOR INDEX
Stenseth, N.C . See Ottersen, G., 362 Sykes, M.T. See Wal ther, G.R., 295
Stephen, A.C. , 200 Symon, C. See Rod house, P.G. , 198
Stephens, M. See Pritchard, J.K. , 328 Symonds, D.J., 103
Stephens, N ., 23 Syms, C., 294
Stephenson, R. See Smedbol, R.K., 363 See Jones, G.P., 288
Stephenson, R.L. See Bradford , R.G ., 237 Syrett, P.J. , 23
Sterner, R.W., 23 Szmant, A.M. See Nu gues, M .M., 61
St ick, K. See Hershberger, P.K., 24 1
Stjernman, M. See Grindstaff, J.L., 241
Stobart, B. See Downing, N., 285 T
Stock, M., 103
Stoffle, R.W. See Mumby, P.J. , 291 Taguchi , S., 23
Stone, G. See Will mer, P., 104 Tait, R. See Ha nl on, R.T., 192
Stone, L. 294 Takabayashi , T. See Suzuki, Y. , 62
Storey, J.M . See Storey, K.B. , 200 Takada , Y. See Shibuno, T. , 294
Storey, K.B. , 200 Takahashi , M. See lkeya, T., 21
Storlazzi, C.D., 62 Takasu , F. See Muko, S., 60
Stranks, T.N., 200 Takasuka, A., 363
Strasser, M., 103 Takeda, R. , 200
Strathmann, M.F. See Strathmann, R.R. , 249 Takeuchi, T. See Ha masa ki, K., 191
Strathmann, R. See Em let, R. , 239 See Kurihara , A., 194
Strathmann, R.R. , 249 See Okumura, S., 197
See Bertram, D.F., 237 See Javoi s, J., 242
See Biermann , C. H., 237 Tanabe, S. See Arai, T., 324
See Chaffee, C., 238 Ta nkersley, R.A. See Forward, R.B., 190
See von Dassow, Y.J. , 250 Tanner, J. See Bellwood, D.R., 283
Strazzullo, L. See D'A niell o, A., 189 Tanner, J.E ., 62
Strong, A. See Goreau, T.F., 286 See Connell , J.H., 55
Strugnell, J., 200 See Hughes, T.P., 57, 58, 288
Strugnell, J.M .. 200 Targett , T.E. See Thorrold , S.R., 330
Styan, C. A. See Marshall, D.J., 244 Tateno, S., 200
Suatoni, E. See Levinton, J.S., 243 Taunton-C lark, J. See Boyd, A.J., 359
Suh, H.L. See Jeong, S.J., 242 Taylor, E.W. See Nay lor, J.K., 246
See Yu , O.H. , 250 Taylor, P.R . See Little r. M.M ., 59
Suh arsono, See Brown, B.E., 284 Teesda le, W.J. See Ca mpana , S.E., 325
Sunda, W.G. , 23 See Halden, N.M., 326
Sundbac k, K. See Nil sson, P., 101 Teg ne r, M.J . See Jackson, J.B.C., 58, 288
Sunde! in , B. See Wiklund , A.K.E ., 250 Tei xei ra, C.M. See Cabra l, H.N., 96
Sundermann, G. See Lenz, S., 194 Teleki, K. See Down in g, N .• 285
Surge, D.M., 329 See West macott , S., 295
Sutcliffe, W.H ., 363 Temme, D. H. See McGinley, M.A., 245
Sutherl a nd , O.R.W., 249 Temmin g, A., 103
Suthe rs, I.M . See Begg, G.A., 324 See Del Norte-Ca mpos, A.G.C., 97
See Ma n e in sdottir, G., 244 Terry, K.L., 23
Sutton , D.C. See John so n, C.R. , 58 Tett, P., 23
Sutton, S. See Ci nn er, J., 285 Tett a manti , G. See de Eguileor, M ., 189
Su zuk i, Y., 62 Teyssie, J.L. See Bustama nte, P. , 188
. Sva ne, I. See Anthony, K.R.N., 53 Thakar, M.S. See Fox, C.W., 240
Svedang, H. See Limburg, K.E., 328 Thiam , M . See Caverivie re, A., 188
Svensson, I. See Berglund , A. , 236 See Dia ll o, M., 189
Swain, D.P. , 249, 363 Thiel , M. , 200, 249
Swart, P.K. See Thorrold , S.R., 330 Thiessen, A. See Stock, M. , 103
Swearer, S.E., 249, 330 Thingstad , F. See Heldal , M., 21
Sweatman, H. See Brun o, J.F., 54 Thiriot, A. See Razo ul s, S., 198
See C hea l, A.J., 284 Thomas, C. D., 294
See Koh, E.G.L., 58 See Sin ger, M .C., 248
Sweatman, H.P.A., 294 Thomas, R.M . See Attrill , M.J. , 95
Sweeney, M.J., 200 Thomas, S. See Orpin, A.R. , 292
See Norman , M.D., 196 Thompson, J.N ., 249
393
AUTHOR INDEX
Thompson, J.T., 200 Tsukamoto, K. , 330

Thompson , L.J. See Naeem , S., 291 See Arai, T. , 324
Thompson , P.A. See Parslow, J.S., 22 See Kota ke, A., 243
Thompson, R.J. See Chaparro, O.R., 238 Tsukiji , M. See Tsuchiya, M. , 295
Thompson, S., 249 Tsuneki, K. See Furuya, H., 190
Thompson , V.J. , 295 Tubrett, M. See Campana, S.E., 325
Thorrold, S.R., 330 Turner, M.F. See Droop, M.R., 20
See Bath, G.E., 324 Turpin , D.H ., 23
See Campana, S.E., 325 See Elrifi, l.R., 20
See Elsdon, T.S. , 297-330 Tweddle, J.C. See Moles, A.T., 245
See Fowler, A.J., 326 Twitchell, R.J. See Benton, M.J., 283
See Jones, G.P., 327 Tworek, J.A . See Smouse, P.E., 329
See Martin , G.B. , 328 Tyler, J.C. , 295
See Walther, B.D., 330 Tze ng, W.N. , 330
See Wells, B.K., 330
Thorson , G., 249
Thresher, R. See Campana, S.E., 325 u
Thresher, R.E., 330
Uematsu, K. See Yamazaki, A., 202
See Gunn , J.S ., 326
Uemura, D. See Kitamura, M., 58
See Proctor, C. H., 328
Uglow, R.F. See Dyer, M.F., 97
Tiews, K., 103
Uku , J.N. See McClana han , T.R., 290
See Meyer-Waarden, P.F., 100
Uller, T. See Marshall, D.J., 244
Tiffany, B.N., 200
Ulltang, 0., 363
Tilman, D., 295
Underwood, A.J., 62, 249, 250, 330
Timofeev, S.F., 249
Utoh, T. See Kotake, A., 243
Tinch, R.R.T. See Uyarra, M.C., 295
Uyarra, M.C., 295
Tindle, C. See Montgomery, J.C., 195
Ti ssot, B.N., 295
Titlyanov, E. A., 62
Todd , C. D. See Jones, H.L. , 242
v
Tokunaga, T. See !ida, H. , 193 Vadstein, 0., 23
Tolimi eri , N., 295 Valdivieso, V. See Baltaza r, P., 186
Toll, R.B., 200 Vale ntin sson, D., 250
See Forsythe, J.W. , 190 Val iela, 1., 62
See Hochberg, F.G., 192 Vall in , L., 363
See Voss, G.L., 201 Valone, T.J. See Brown, J.H., 284
Tollrian , R. See Agrawal, A.A., 235 Valvassori , R. See de Eguileor, M. , 189
Toole, C.L., 330 Van A ken , H.M . See Philippart, C.J.M., 101
Toonen, R.J ., 249 VanBeek , F.A., 103
Torisawa, M. See Yamashita, Y., 202 See Rijn sdorp, A.D., 362
Tosca no, M.A . See Aron so n, R. B., 283 Vance, R.R. , 250
See McCl a nahan, T.R., 290 van den Berg, H.A . See Zonneveld, C., 23
Totterdell, l.J. See Orr, J.C., 292 Va ndenberghe, E.P. See Sargent, R.C., 248
Town send , D.W., 330 Vander Baa n, S.M., 103
See Radtke, R.L. , 329 van der Have, T.M. , 250
Townsend Peterson, T. See Thomas, C. D., 294 van der Linden , P.J. See Houghton, J.T. , 287
Tranter, D.J., 200 VanderMeer, J. See Va nder Veer, H.W., 103
Tricas, T.C., 295 van der Meere n, T. See Iglesias, J. , 193
Trilestari , S. See Baird , A.H. , 283 Vander Veer, H.W. , 103
Trivers, R.L, 249 See Berg man, M.J.N ., 95
Troadec, H. See Campana, S.E., 325 See Campos, J., 65-104
Trompetter, W.J. See Markwitz, A., 328 See Cardoso, J.F.M.F. , 96
Troost, K. See Hiddink J.G ., 99 See Freitas, V., 97
Trussell, G.C., 363 See Rijn sdorp, A.D., 102
Tsuchiya, K. See Shi geno, S., 199 van de r Velde, G. See Nagelkerken, 1., 291
Tsuchiya, M., 295 Van Dolah, F.M., 200
See Cadoret, L., 284 Van Donk, E. 104
394
AUTHOR INDEX
van Dykhuizen, G. See Chen, D.S., 188 Voight , J.R ., 201

Vaneys, G. See Bak, R.P.M., 54 Volckaert , F.A.M. See Gysels, E.S. , 98
Van Hannen , E.J. See Paulij, W.P., 197 Vol k, E. See Schroder, S., 329
Van Heukelem , W.F., 201 Yolk , E.C. See Brenkman, S.J., 324
van Jaarsveld , A.S. See Thomas , C. D., 294 Vollhardt, C . See Negri, A.P., 60
van Kleunen , M. , 250 von Dassow, Y.J. , 250
Van Leeuwen , P.l. See VanBeek, F.A., 103 Vorberg, R., 104
Van Lissa, J.H.L., 104 See Berghahn, R., 95
Van Marlen , B., 104 See Stock, M., 103
Van Montfrans, J. See Dorval, E., 325 Voss, G.L. , 201
Van Moorsel, G.W.N.M ., 63 See Toll , R.B. 200
Van Noort, G.J. See Creutzberg, F., 96 Voss , R. See Hinricksen, H.-H ., 360
van Riel , M.C. See Nagelkerken, 1., 291 Vynne, C. See Roberts, C.M., 293
Van Straalen, N.M. See Hendrickx , F., 241
Van Stra len, M. See Rijnsdorp, A.D., 102
Van't Hoft, T. See Nagelkerken, 1., 291 w
van Woes ik, R. See Golbuu, Y., 286
See Loya, Y., 289 Wabnitz, C.C.C. See Mumby, P.J. , 291
See Nakamura, T., 291 Wachet, R.W. See Miller, M.B. , 328
van Wyngaardt, S. See Venter, J.D., 201 Wada, S. See Kobayashi, T., 242
Vasco, D. See Singer, M.C ., 248 Wade, M.J., 250
Vaughan , G.M., 330 Wagner, H.G. See Douglas, R.H., 190
Vecchione, M., 201 Waiwood, K.G., 363
Vega, M.A. See Rocha, F., 198 Walker, B. See Elmqvist, T. , 285
Veley, V.C.F. See Carruthers, J.N., 359 See Folke, C., 56
Venter, J.D. , 201 Walker, J.W. See Jennings, S., 288
See Hoving, H.J.T., 192 Wallace, C.C., 63
Vergara, A.M. See Chaparro, O.R., 238 See Connell, J.H ., 55, 285
Verheij , E. See McClanahan, T.R., 290 See Harrison , P. L., 57
Verheye, H.M. See Venter, J.D., 201 Wallace, W. See Levinton, J.S., 243
Verhoof, H.C.C.M. See Paulij , W.P. , 197 Wallace, W.G ., 250
Veri simo, P. See Corgos, A. , 238 Wa lsh , B. See Lynch, M., 243
Verme ij , M.J.A. , 63 Wa lsh, K., 295
Veron , J.E.N., 63 Walsh , T.W. See Smith, S.V., 62
See Robe rts, C.M ., 293 Walsh, W.J., 295
Verriopoul os, G. See Katsanevakis, S., 193 Wa lter, U., 104
Verschoor, J.A. See Venter, J.D. , 201 Walters, C.J. See Hilborn, R., 360
Verschoore R. See Pol et, H., 102 Wa lters, L.J., 63
Vevers. H.G ., 201 See Kuffner, l.B., 59
Vi ctor, S. See Golbuu, Y., 286 Wa lther, B.D., 330
Vida l, D. E., 250 See Elsdon, T.S., 297-330
Vida l, E.A.G., 201 Wa lther. G.R., 295
See Igles ias, J ., I93 Wa ng, G. See Zhou, S.R. , 363
Videler, J.J. See Zekeria, Z.A., 296 Waples, R.S . See Smouse, P.E., 329
Villanueva, R., 105-202. 201 Wapstra, E. See Olsson, M ., 246
See Collins, M.A., 189 Ward , S. See Cox, E. F., 238
See Iglesias, J ., I93 Ward , S. See Harrison , P.L., 57
See Navarro, J.C. , I95 Ware, D.M., 250
See Parra, G., I97 Warnau , M. See Bustamante, P., 188
See Se mmen s, J.M., 199 Warner, D.A., 250
Villareal, T.A. See Liu, H., 22 Warner, R.R., 250, 295
Villate, F. See Dia z, E., 239 See Halpern , B.S., 287
Vinayac handran, P. N. See Saji. N.H. , 293 See Jackson , J.B.C., 58, 288
Vincent , A.C.J. See Sadov y, Y.J., 293 See Knapp, R.A., 242
Viner, D. See Uyarra, M.C., 295 See Pandolfi, J.M ., 292
Violante, V. See Ghiretti, F., 191 See Petersen, C.W. , 246
Virtue, P. See Koslow, J.A., 243 See Roberts, C.M., 293
Vogel, S., 63 See Swearer, S.E., 249, 329
395
AUTHOR LNDEX
Warnke, K., 201 Wild , C. , 295

Warren, M.J. See Croft, M.T., 19 See Fabri ciu s, K.E., 56
Watabe, T. See Miyazaki , T. , 195 Wildenburg, G. , 202
Wata nabe, M., 23 Wilkinson , C., 63, 295
Watanabe, T., 201 Wilkin son, C.R., 295
Waters, C. See Carruthers, E. H., 359 Williams, A.J. See Munday, P.L., 291
Watkinson, A. See Uyarra, M.C., 295 Willi a ms, B.K., 330
Watkin son, A.R. See Gardner, T.A. , 286 William s, D.M. , 295
Watts, J.E.M. See Webster, N.S., 63 See Doherty, P.J., 28 5
Waycott, M . See Williams, Y.M ., 296 Willi a ms, D.Mc.B. See Ha lford , A., 287
Wear, R.G. , 104 Williams, E.H. Jr, 296
Webb, C.O. See Moles, A.T., 245 Williams, G.C., 250
Webb, R.I. See Webster, N.S. , 63 William s, H.A. See DeMartini, E.E., 239
Weber, A. See Vander Veer, H.W., 103 Williams, J.D., 296
Weber, P.K. See Solomon , C.T., 329 Williams , J. See Mumby, P.J., 60
Webster, M.S., 295 Williams, M.D., 250
We bster, N.S., 63 Willia ms, S.E., 296
See Negri, A .P., 60 See Thomas, C. D., 294
Webster, P. See Henderson-Sellers, A., 287 See Williams, Y.M. , 296
Webster, P.J., 295 Willia ms, S.L. See Carpenter, R.C., 55
Wehrtma nn, l.S . See Kattner, G., 99 See Cheroske, A.G ., 55
Weihs, D. See Arnold , G.P., 95 Willi a ms, Y.M., 296
Wei rig, M. See Orr, J.C., 292 Willi a mson, C.E. See Pal en, W.J., 246
We lleman, H.C., 104 Willi a mson, D.I., 104
We ll s, B.K. 330 Willi a mson, R. See Cobb, C.S., 189
See Elsdon , T.S ., 297-330 See Douglas, R.H., 190
Well s, F. See Roberts , C.M., 293 Willi s, B. See Hughes, T.P., 57, 288
Well s, J. See O' Dor, R.K., 196 Willis, B.L., 63
See Wells, M.J., 202 See Birrell, C.L., 25-63, 54
Well s, M.J., 202 See Bruno, J.F. , 54
See Madan , J.J ., 194 See Hughes, T.P., 58, 288
See O ' Dor, R.K., 196 See Michal ek-Wagne r, K., 60
Well s, S.M. See Westmacott, S., 295 See Oliver, J.K., 61
We nner, A.M. See Dugan , J.E., 239 Willmer, P., 104
We nnhage, H., 104 Willows, R.I. , 250
See Gibson, R.N., 98 Wil son, D.S. See DeWitt , T.J. , 239
Wentworth ; S.L., 202 Wilson, J., 63
Werner, E. , 363 See Hughes, T.P., 57, 288
Werner, F.E. See Stegmann , P.M , 363 Wil son, S. See Sheppard, C .R.C. , 294
Werner, T.B. See Roberts, C.M., 293 Wil son, S.K., 296
West, G.B. See Savage, V.M ., 23 See Graham, N.A.J., 286
West, J. See Westmacott, S., 295 See Ledlie, M.H ., 289
West, J.M ., 295 See McClanahan, T.R., 290
West, S. See Budelmann, B.U., 188 See Pratc hett , M.S., 251-296, 293
West, S.A., 250 Wil son, T.R.S., 330
Westin , L. See Limburg, K.E. , 328 Wing, S.R., 63
Westmacott, S., 295 Wingate, R.L. , 330
Westoby, M. See Moles, A.T., 245 Wink s, C. See Buckley, Y.M., 237
Wheatly, M.G. , 250 Winn a nt , C. D. See Jackson, G .R., 58
Wickstrom, H. See Limburg, K.E. , 328 Winte rbotto m, R. See Munday, P.L., 291
Widdows, J. See Bayne, B.L., 236 Witte, J.IJ. See Cardoso, J.F.M .F., 96
Wiebe, P.H. See Harris , R.P., 192 See Vander Veer, H.W., 103
Wiederhold , M.L. See Colmers, W.F. , 189 Witte nberg, R. See Buckley, Y.M., 237
Wienbeck, H. See Rauck, G., 102 Wittouck, J. See He rshberge r, P.K. , 241
Wiese, K. See Berghahn, R., 95 Wodin sky, J., 202
Wiklund , A.K.E., 250 Wohlers, J. See Sommer, U., 200
Wiklund , C., 250 Wolan ski , E. See Fabricius, K.E., 56
Wilbur, H.M. See Resetarits, W.J., 247 See McCook, L.J. , 60
396
AUTHOR INDEX
Wolff, W.J. See Hiddin k J.G., 99 Yool, A. See Orr, J.C. , 292
Wolkowicz , G.S.K. See Li , B.T., 22 Yos hida, K. See Ikeda, Y., 193
Wollebaek , A., 104 Yoshida, M. See Yamazaki, A., 202
Wo ng, M., 296 Yoshida, Y. Hamasaki, H.
Wood, E., 296 Yo ung, C.M. See McCarthy, D.A., 245
Wood , G. , 23 Yo ung, J.Z ., 202
See Flynn, K.J. , 21 See Budelmann, B.U., 188
Wood, J.B . See Semmens, J.M. , 199 See Ni xon, M ., 196
Woodfin, R.M. See Naeem, S., 291 Young, R.E., 202
Woodhams, P.L. , 202 See Bower, J.R., 187
Woodley, C.M. See Roessig, J.M. , 293 Yu , O.H. , 250
Woods, J. , 23 See Jeong, S.J., 242
Wooster, W.S ., 363 YUfera, M. See Parra , G., 197
Wormuth, J.H. See Vidal, E.A.G., 201 Yukihira .H. See Golbuu, Y., 286
Worst , D.E. See Hoving, H.J.T., 192
Wright , J.T., 250
Wright, P. See Scott, B., 363 z
Wulff, R.D. , 250
See Roach, D.A., 247 Zakas, C. See Allen , J.D., 235
Wurt z, M. See Packard, A., 197 Zambonino-lnfante, J.L., 202
Wyckoff, R.W.G. , 330 Zandee, D.I., 202
Wyman, K. See Falkowski, P.G., 20 Zarenkov, N.A., 104
Zariquiey-Aivarez, R., 104
Zdanowicz, V.S . See Rooker, J.R. , 329
y See Secor, D.H., 329
Zeidberg, L.D., 202
Yahya, S.A.S. See Garpe, K.C., 286 Zekeria, Z.A., 296
Yamada, S.B., 250 Zera, A.J., 250
Yamada, Y. See Kotake, A., 243 Zevenboom, W., 23
Yamagata, T. See Saji . N.H., 293 Zhang, G .F. See Deng, Y.W., 239
Yamamoto, M. See Shigeno, S., 199 Zhang, H. See He nderson -Sellers, A. , 287
Yamanaka, Y. See Orr, J.C ., 292 Zhou, S.R., 363
Ya mash ita, Y., 202 Ziegler, T.A. , 202
Yamau chi , Y. See Tsuchiya, M., 295 Zimmer, R.K. See Krug, P.J ., 243
Yama za ki, A., 202 Z immer man , C.E. 330
Yarnazato, K. See Loya , Y., 289 Zlokovitz, E. See Secor, D. H., 329
Yang, M.-H. See Secor, D.H. , 329 Zlokovitz, E.R., 330
Yaragina, N.A. , 363 Zollner, E. See Sommer, U., 200
See Marshall CT., 36 1 Zonneveld, C., 23
Yau, C. See Co llin s, M .A., 189 Zouhiri , S. See Mo un y, P., 101
Yin , M.C. See Gibson, R.N ., 98 Zuev, G.V., 202
Yin, Q.Z. See Hobbs , J.A ., 327 Zuidema, D. See Bergman, M.J .N., 95
Yogo, Y. See Ku wam ura, T., 289 Zuniga, 0., 202
Yohe, G. See Parmesan, C., 292 Zuniga-Romero, 0. See Castro-Fuentes, H., 188
Yonge, C.M. See Ll oyd, A.J., 100 Zwaan, B.J. See Fischer, K., 240
397
SYSTEMATIC INDEX
References to articles are given in bold type, references to text pages are in regular type.
A Amphioctopus, 110, 117, 119

aegina, 108, 110, 114, 157
Abdopus, 180 arenicola, 108, 172
abaculus, 108 burryi, 108, 114, 136, 145, 157, 158, 164, 167, 170, 177,
aculeatus, 108 181
tonganus, 108 exannulatus, 108
Acanthaster planci, 27, 254, 255, 256, 257, 262, 263, 264 kagoshimensis, 108
Acanthastrea , 255 cf kagoshimensis , 108
Acanthopagrus butcheri, 321 marginatus, 108
Acanthophora spicifera, 53 mototi, 108
Acanthuridae, 259,261, 271, 272, 273,276 neglectus, 108
Acanthurus lin ear us, 258 ocel/atus, 126
nigrofuscus, 258 ovulum, 108
polyzona , 272 rex, 108
Acartia tonsa , 140, 143 robsoni, 108
Acropora,49,255 , 263, 265, 267, 269 siamensis, I 08
digitifera, 36, 52 varunae, 108
florida, 36, 37, 52 Amphiroa, 38, 43
formosa, 36, 37, 52 an.ceps, 36, 52
gemmifera, 36, 37, 52 foliacea, 52
hyacinthus, 36, 37, 52, 262, 264, 274 Amphitretidae, 110, 115, 182
microphthalma , 37, 44, 52 Amphitretus, 113, 125
millepora, 36, 37, 43,44,45,46,49,52 Ampithoe valida, 215
nasuta , 36, 37, 52, 274 An.otrichium ten.ue, 45
palifera, 36, 37, 41 , 43, 44, 52 Aphidae, 225
sp. I, 36, 52 Aphrodoctopus schultzei, 108
sp. 4, 36, 52 Apogonidae, 261, 265, 277
sp. 6,36,52 Argonauta, 120
sp. 7, 36, 52 argo, 120, 125, 131, 138
sp. 8,36, 52 Argonautida, 182
sp. 9,36, 52 Argonautidae, 110, 182
sp. I0, 36, 52 Argonautoida, II 0
sp. II, 36, 52 Aristolochia micrantha, 223
surculosa, 41 , 44, 52 orbicularis, 223
tenuis, 36, 37, 45 , 52, 274 reticulata, 223
willisae, 37, 44, 52 serpentaria, 223
Acroporidae, 37, 265 Artemia , 136, 137, 138, 139, 140, 141 , 142 , 143, 149, 150,
Acyrthosiphon pisum, 209 154, 155, 156, 159
Ada/aria proxima, 217 Arthropoda , 66
Adomems triguttulus, 208 Astreopora, 255
Agaricia, 53 Atherina presbyter, 171
agaricites, 52 Azurina eupalama, 272
danai, 37, 52 hirundo, 272
humilis, 36, 37, 52
tenuifolia, 36, 37, 53
Agaricidae, 37
Alderia modesta, 212,225
B
Alepisaurusferox, 170 Balistapus undulatus, 280
Allocyttus niger, 219 Balistidae, 26 1
Alloposidae, 110, 182 Bathypolypus, 174
Amblyglyphidodon , 265 Bathyteuthidae, 125
Ammodytes person.atus, 140 Battus philenor, 223
Ampelisca araucana, 215, 218 po/ydamus, 223
Amphibolurus muricatus, 225 Benthoctopus, 174
399
SYSTEMATIC INDEX
Blenniidae, 261 Chaetogammarus marin us, 215

Bolitaena, 120 scoerensis, 215
Bol itaen id ae, II 0, 115, 182 Chasmagnathus granulata, 216,218
Boodlea siamensis, 27 Cheilinus undulatus, 280
Brachionus, 138, 141 Cheilodipterus, 258
Brevoortia tyrannus, 343 Cheiloprion labiatus , 258
Bryaninops, 265 Chiroteuthidae, 178
Buccinum cyaneum, 218 Chiroteuthis, 125
isaotakii, 218 Cit/orella, 139
undatum, 218 Chlorodesmis, 48
Buglossidium luteum , 91 fastigiata, 41, 45, 52
Bugula neritina , 218, 226 Chnoospora implexa, 29
Chondrophycus poitea ui, 44, 53
Chorilia longipes, 170
c Chorism zis antarcticus, 2 18
Chromidia , 181
Ca/anus, 136 Chromis, 264, 265
helgolandicus, 215 dimidiata , 258
Callinectes sapidus, 140 Chrysiptera rollandi, 258
Callistoctopus, 115, 116, 118, 162, 163, 168, 178 Ciona intestinalis, 212,2 13, 218, 227
aspilosomatis, 108, 168 Cirrhitichthys oxycephalus, 258
/echenaultii, 108 Cirrhitidae, 261
luteus, 108 Cistopus indicus, 108
macropus, 108, 136, 157, 167 Cladophora, 52,53
nocturnus, 108 Cladophoropsis, 52, 53
ornatus, 108, 173 Clupea harengus, 218, 334
Ca mpanula americana, 235 harengus harengus, 350
Cancer productus,137 pallasii, 217, 218, 344
setosus, 137, 138 Coelorhynchus carm inat us, 335
Capitella, 218 Coeloseris, 255
capitata, 218 Collinsia bicolor, 223
parvijfora, 223
Caracanthidae, 261
tinctoria, 223
Caracan thu s, 264, 265
Conus, 218
Carangidae, 276
Corallinaceae, 45
Carcinus maenas, 92, 139
Corallinales, 28, 31
Caretta caretta , 170
Corallophila huysmansii, 45
Caridea, 66, 67
Cranch i id ae, 115
Castilleja indivisa, 223
Crangon , 67, 87, 88, 90, 94, 341
Centropages typicus, 215
af.finis, 67
Centropyge acanthops, 258
alaskensis, 67
multispinis, 258 alba, 67
vroliki, 258 allmanni, 67, 68
Cerasroderma, 78 amurensis, 67
Ceratoserolis trilobiroides, 218 cassiope, 67
Chaetoceros, 139 cran gon , 65-104,2 15
Chaerodon, 259, 263 dalli, 67
aureofasciatus, 258 franciscorum, 67
baronessa, 258 angustimana , 67
bennetti, 272 hakodatei, 67
citrinellus, 258 handi, 67
larvatus, 274 holmesi, 67
lunulatus, 257, 258, 262 nigricauda , 67
melannotus, 258 nigroma culata , 67
meyeri, 258 propinquus, 67
plebius, 258 septemspinosa, 67
rainfordii, 258 uritai, 67
trifascialis, 258, 262, 264, 274 vulgaris, 67
Chaetodontidae, 259,261 , 271,272 , 273, 275, 277 Crangonidae, 67
400
SYSTEMATIC INDEX
Crango noidea, 6 Euphausia pacifica, 137

Crepidula dilatata, 218 superba , 336
Crustacea, 66 Euphydryas editha, 223
Ctenochaetus striaflls, 258 Euprymna tasmanica , 218
Ctenoglossa, 182 Euterpina acurifrons, 215,216
Cycloteuthidae, 125 Evasterias rroschelii, 170
Cynoscion regalis, 314 Eviora, 264, 265
Cyphastrea, 26, 37, 53, 255
Cytisus scoparius, 233
F
D Favia, 255
favus, 36, 37, 53
Daphnia culcullata, 225 Jragrum, 43, 53
magna, 183, 209, 225 Favidae, 37
Dascyl/us, 259, 264, 265 Favites, 255
Decapod a, 66 Ficedu/a hypoleuca, 225
Delesseriaceae, 45 Forcipiger jfavissimus, 270
Diadema antillarum, 27 Fundulus hereroclitus, 92
Dicentrarchus labrax, 150
Dictyopteris, 53
Dictyosphaeria cavernosa, 27 G
Dictyota, 27, 38, 53
confervoides, 53 Gadus morhua , 90, 91, 334
menstrua/is, 48, 53 Galaxea, 255
pinnatifida, 53 Gammarus duebeni, 215,2 18
pulchella, 38, 44, 48, 53 insensibilis, 215
oceanicus, 215
salinus, 215
E Glyplocephalus cynoglossus, 91
Gobiidae, 259,261,265
Echinophyllia, 255 Gobiodon, 259, 264, 265, 270, 274
Echinopora, 255, 265 acicularis, 265
Eledone, 115 axillaris, 258
caparti, 170 hisrrio, 258, 274
cirrhosa , 108, Ill, 113, 126, 127, 128, 131, 157, 165, quinquesrrigatus, 274
167, 170, 180, 181 rivularus, 258
moschata, 120, 122 sp. A, 258
Eledone/la, 120 sp. C, 258
Emerita ana/oga, 138,2 18 unico/or, 258
Engraulis an choita, 2 18 Goniasrrea, 255
capensis, 334 retiformis, 36, 37, 53
japonicus, 342 Goniopora, 255
Enteroctopus, 115, 124, 125, 142, 143, 156, 16 1, 162, 174 Gracilaria crassa, 27
dofleini, 105, 106, 107, 108, Ill, 113, 114, 124, 125, Graneledone, 182
128, 136, 143, 147, 157, 159, 161 , 162, 164, 165, Grapsus grapsus, 140
167, 169, 170, 173, 174, 175, 176, 178, 179, 180, Gymnothorax mordax, 170
181, 183, 184, 185
magnificus, 108, 128
megalocyathus, 108, 122, 123, 125, 130, 132, 135, 137, H
157, 161, 163, 174, 185
Enteromorpha intestinalis, 46 Halichoeres cosmeticus, 258
Epinephelus marginatus, 171 melanurus, 258
Eriph ia verrucosa, 148 Halim eda, 41 , 43, 44, 52, 53
Eualus gaimardii, 218 opun tia , 41 , 43, 44, 52, 53
Euaxoctopus , 115, 178 Haliotis australis, 353
panamensis, 108, 117, 167 Haliphron , 114, 125
Eucarida, 66 Haloajaponica, 212,217,218
Eumalacostraca, 66 Haminaea vesicula, 221
40l
SYSTEMATIC INDEX
Hapalochlaena , 110, 170 Lobopll_vllia , 255

maculosa, 118, 119 Loliginidae, 160
lunu/ara , 108, 137, 157 Loligo forbesi, 161
He/iconius, 223 opa/escens, 160, 185
Hemi/epidot us hemi/epidotus, 136, 137 pealei, 147, 164, 180
Hepatus chi/iensis, 138 vulgaris, 112, 148, ISS, 162
Hildenbrandia, 52 Lucifer, 137
Homarus am ericanus, 2 18 Lyngbya confervoides, 44, 53
Hop/ostethus at/anticus, 219 majuscula, 44, 52, 53
Hydnoph ora , 255, 265 po/ychroa, 44, 53
Hydra, 183 Lyth oporella melobesioides, 36, 52
Hydroides elegans, 44
Hydrolithon, 36, 52, 53
boergensii, 36, 52, 53 M
onkodes,36,37,43, 44, 52
reinboldii, 36, 43, 45, 52, 53 Macoma , 78
Hypnea, 38 balthica , 92
musciformis, 43 Ma croctopus maorum, 108, 114, 137, 157, 164, 170
Macrocystis pyrifera, 181
Ma cro tritopus, 116, 165, 167, 170, 172, 173, 175, 178, 181 ,
I 182
ldiosepius, 148, 149 danae, 167
//lex illecebrosus, 162 defilippi, 108, liS, 117, 125, 135, 162, 164, 165, 167,
lsochrysis, 139 168, 169, 170, 172, 173, 177, 182
ga lbana, 139 Maja brachydactyla, 139, 140, 142 , 143, ISS, 156
lsopora, 255 squinado, 139, 140
Malacostraca, 66
Mal/alliS vil/osus, 334
J Mammalia, 225
Melanogrammus aeglefinus, 219, 335
Ja ssa sla lleryi, 215, 218
Menidia menidia , 92, 219
Merlangius mer/angus, 89, 90,91
K Mer/uccius bilinearis, 335
produ ctus, 343
Katsuwonus pelamis, 342 Merulina, 255
Kerate/la cochlearis, 218 Mesonychoteuthis, 125
Mesophyllum , 36, 52, 53
Metamvsidopsis e/ongata atlantica, 140
L
Microstomus kilt , 91
Labrichthvs unilineatus, 258 Millepora complanata, 37, 52
Labridae , 259, 261 Moina salina, 140
Lacerta 1 ivipara, 225 Mon aca nthidae, 26 1,277
Lams argenta/us, 91 Mono chrysis, 2, 17
ridibundus, 9 1 Mon tastrea, 255
Lauren cia papillosa , 41, 43, 44, 53 faveo/ata, 41
poiteaui, 53 Montipora. 255
Leptasterias aequalis, 218 capita/a, 53
Leptograpsus variegatus, 137 digitata , 41
Leptoria , 255 Maron e saxatilis, 92,318
Ligia oceanica, 218 Mya, 78
Limandaferruginea, 353 Mycedium, 255
limanda , 90,91
Liocarcinus depurator, 138, 142, 143
Lithophyllum, 37, 52 N
insispidum , 36, 52
kotschyanum, 36, 52 Nannochloropsis, 138, 139, 140
Lobophora , 27. 44, 52, 53 Nasa lituratus, 258
variegata, 27, 29, 32, 33, 36, 37, 38, 42, 43, 44, 48, 49, Natantia, 66
52, 53 Necora puber, 139
402
SYSTEMATIC INDEX
Nematocarcinus lanceopes, 218 warringa, 109, 134

Neocirrhitus annat us, 264 wolfii, 106, 109, 134
Neoglyph ididon me/as, 258 Oculina arbuscu/a , 53
Neogoniolithon brassica-jlorida , 36, 52 Ocythoidae, 11 0, 182
fosliei, 36, 45, 52 Oncorhynchus, 3 16
megacarpum, 52 kisutch, 313, 353
Neptunea pribiloffensis, 22 1 Oregonia gracilis, 170
Notocrango n antarcticus, 218 Oreochromis mossambicus, 225
Oxymonacanthus longirostris, 258, 278
0
p
Octopodidae, 105, 106, 107, 108, 109, 11 0, 11 3, 11 8, 135,
136, 138, 140, 156, 157, 158, 160, 165, 166, 167, 169, Pachygrapsus marmoratus, 148
170, 172, 173, 174, 182, 183 transversus, 148
Octopoteuthidae, 125 Padina, 27, 33, 38, 41, 48, 52
Octopus, liS, 123, 125, 128, 135, 149, ISO, 167, 170 australis, 43
alecto, 108 Pagurus, 137
australis, 126 longica rpu s, 218
berenice, 108 prideaux, 136, 138, 142, 143, 144, 145, 146, 154
berrima, 106 Palaemon gravieri, 218
bimacu/atus, 109, Ill , 125, 137, 157, 163, 164, 170, pacificus, 136
176, 18 1 serratus, 139, 140
bimaculoides, 163 serrifer, 138, 142, 149
bocki, 109, 117 Panda/us danae , 137
campbelli , 109 Papilio glaucus, 223
cyanea, 109, 110, Ill , 120, 122, 123, 124, 137, 138, mac/w on, 223
157, 164, 165, 168, 173 Paracirrhites forsteri , 258
defilippi, 172 Paragobiodon, 264, 265
favoni us, 109 Pareledone, 174, 182
jilosus, 109 Parides montezuma, 223
hawiiensis, 109 Parvulustra parvivipara, 229
hummelincki, 109 Passijlora, 223
hu//oni, 109, 114, 157, 164 Pa vona , 255
joubini, 109, 128, 130, 137, ISO, 157, 159, 176 Pectenogammarus planicrurus, 2 15, 218
/aqueus, 109, 11 0 , 113, 11 4, 137, 157, 169 Pectinia, 255
ltl/eus, 113 Pedicularis semibarbata , 223
maya, 128 Peyssonn elia , 3 1, 36, 41, 43, 52, 53
cf mercatoris. 184 rubra, 53
micropyrsus, 163 Phacel/ophora cam tscharica, 169
miiiHIS, 109, 11 4, 13 1, 137, 157, 164, 183 Phaeophyceae, 45
pallidus, 126, 158, 183 Phragmatopoma lapidosa , 218
parvus. 109 Pieris rapae . 223
rubescens. 109. 165, 167, 168, 169. 175 Pisidia longicomis, 2 15 ,2 18
salutii, 109, 157, 181 Plagusia depressa , 140
selene, 109 Plantago erecta, 223
tetricus, 109, Ill , 120, 135, 138, 157, 184 Polin ices sordidus, 222
cf tetricus, Ill , 114, 135, 138, 157, 164, 169 Platichthysjlesus, 90,9 1
teuthoides, 164, 167, 170, 172 Plectroglyphidodon, 265
variabilis, 163 johnston ianus, 258
velige ro, 109 lacrymatus, 258
vitiensis, 109 Pleocyemata, 66
vulgaris, 105, 107, 109, 110, Ill , 11 2, 11 3, 114, liS, Pleuron codes monodon, 138
120, 121, 122, 124, 126, 127, 128, 129, 130, 131 , Pleuronectes platessa, 75 , 90, 91
132, 133, 135, 138, 139, 140, 142, 143, 144, 145, Pneophyllum , 52, 53
146, 147, 148, 149, ISO, 151 , 152, 153, 154, ISS, Pocil/opora, 255, 263, 265. 267, 269
156, 157, 158, 159, 160, 16 1, 163, 164, 166, 167, damicom is, 41 , 43, 44, 46, 53, 264
168. 170, 171 , 173 , 174, 175, 176, 177, 178 , 179, Poc i ll oporidae, 37, 265
180. 18 1, 183, 184, 185 Pollachius virens, 335
403
SYSTEMATIC INDEX
Pomacanthidae, 261 , 271 Scaeurgus, 172, 174

Pomacentridae, 259, 261, 265, 271, 277 jumeau, 109
Poma centrus, 264, 265 nesisi, 109
amboinensis, 226, 313 patiagatus, 109
bankanensis, 258 tuber, 109
lepidogenys, 258 unicirrhus, 109, 119, 134, 135, 141, 157, 163, 167, 175,
mo/uccensis, 258 181
sulfureus, 258 Scaridae, 259, 261, 276
vaiuli, 258 Scarus gaucamai, 281
wardi, 258 sordidus, 258
Pomatoschistus, 90 Sciaenops ace/latus, 342
Porites, 45, 255, 263, 267 Scombridae, 276
astreoides, 44, 53 Scophtha/mus rhombus, 91
cylindrica, 265, 273 Scorpaenidae, 261, 265
porites, 53 Scottolana can adensis, 92
Poritidae, 37 Scutus breviculus, 170
Porolithon, 37, 52, 53 Scy/larides squammosus, 218
Scyra acutifrons, 170
onkodes, 36, 52
Sebastapistes cyanostigma, 264, 265
pachydermum, 52
Sebastes diploproa , 92
Portunus trituberculatus 138
melanops, 217
Prionace glauca, 170
Selenastrum, 15
Prionurus puncta/us, 272
minutum, 6
Promysis orienta/is, 137
Semihalanus balanoides, 218
Protozoa, 339
Sepia officina/is, 150, 155
Prunus serafina, 223
Sepioteuthis australis, 215
Psetta maxima, 91,219
Seriatopora, 255, 265
Pseudoalteromonas, 43 Sera/is polita, 218
Pseudocalanus, 218 Serranidae, 261
Pseudocarcinus gigas, 217 Serranus, 171
Pseudochromidae, 261 Sesarma rectum, 215
Pseudocyttus maculatus, 219 Siganidae, 261, 276
Pseudopleuronectes americanus, 219, 341 Siganus spin us, 258
Pseudosiderastrea tayamai, 37 Solea senega/en sis, 89, 140
Pterocladiella caerulescens, 53 so/ea, 89, 90, 91
Pteroctopus, 174 Spodoptera liuoralis, 223
tetracirrhus, 109 Sporolithaceae, 45
Pugettia productus, 137 Stator limbatus, 208
Pyura stolonifera, 218 Stegastes fasciolarus, 258
partitus, 224
Streblospio benedicti, 218
R Strongylocentrotus droebachiensis, 221
Stylophora, 255, 265
Raphanus raphanistrum, 225 pistillata , 36, 37, 43, 44, 53
Rhodophyta, 45 Synchelidium trioostegitum, 215,218
Robson ella australis, 109, 157, 164
fontanianus, 109, 141
Ruditapes philippinarum, 136 T
Tea/ia crassicomis, 221
s Tetraodontidae, 261
Tetraselmis, 139
Salmo trutta, 208, 316 Thalassoma bifasciatum, 223
trutta tnttta, 3 11 quinquevittatum , 258
Sargassum, 27, 29, 33, 38, 39, 41, 45, 46, 48 , 52, 53 Thaumo ctopus mimicus, 109
hystrix, 53 Theragra chalcogramma, 2 19, 339
po/ycystum, 41 , 43,44,53 Thunnus alalunga, 170
po/yphyllum, 53 Thysanoessa raschii, 215
404
SYSTEMATIC INDEX
Tirannderma, 52 , 53
prororypum, 37, 52
v
Tremoctopodidae, 110, 182 Vitreledonellidae, 110, 115, 182
Tremocropus vio/aceus, 131
Trisopterus luscus, 91
Tubasrrea a urea, 53
Tubifex rubifex, 225
w
Turbinaria, 27, 48, 255 Warersipora subrorquara, 215,216
ornata, 27, 41 Wunderpus , 110
phorogenicus, 106, 109, 110, Ill , 114, 141, 142, 164,
u 170
U/orhrix pseudojlacca, 46
U/va, 38,48
fasciara, 43, 53
z
Uniophora granifera , 218 Zonaria, 53
405
SUBJECT INDEX
References to complete articles are given in bold type, references to sections of articles are given in italics,
references to pages are given in regular type.
A B
Ac idi ficat ion , of ocea ns, 40, 5 1, 187,257, 282 Baltic Sea, 67, 84,316, 335, 344,347
Adriatic Sea, 65, 67, 88 Barents Sea, 334, 344, 347
Ageing, octopus larvae, 105, 158- 159 Behaviour, of octopus la rvae, 105, 110, 112, 11 3, 11 6,
Ageing techniques , fishes, 332 143, 144, 145, 147, 156, 159- 169, 174, 177,
Allee effect, 347, 352, 353, 354, 355 180- 181, 185
A lle lopathy, 30, 34, 38, 44- 45 Benthic a lgae, effe cts on replenishment of cora ls, 25-63
Aquac ulture , 233, 234 co nclusions and implications, 50- 5/
Aquarium trade, 276, 277, 278 cora l fecundity, larval dispersal a nd surviva l, 41-42
Autecology of Crangon, 65-104 co ral reple ni shme nt processes, 29-31
autecology, 68-79 diversity of algae and e ffect s on cora ls, 26 - 29
differences between sexes, 69-70 effects on the settlement of coral larvae, 42-46
differences in relation to growth, 70 negative effects, 44-46
ecophysiolog ica l characterist ics, 71-76 chem ica l, 44-45
adult stage, 75- 76 epitha lli a l sloughing, 45
egg stage, 7/ - 72
other effects, 45-46
juvenile stage, 74-75
positive effects, 42-44
larva l stage, 72 - 73
habi tat co nditi ons, 33-40
sett lement, 73- 74
benthic sed iment regimes, 39-40
food and role as predator, 77- 79
benthic space, 33-37
life cycle, 7/
chem ical env ironments, 40
morphology, 68- 70
lig ht conditions, 38
recruitment, 79
microbial environment s, 40
species characteristics, 68
water flow and turbulence, 38- 39
fi sheries, 87- 91
post-settlement surviva l and grow th , 46- 49
fisheries charac teristics, 87- 88
fishing areas, 88 mechanisms, 47-48
impact of Crangon fisheries , 90-91 size and development of recruits, 48- 49
landings, 88- 89 spatial and tempora l sca le, 49- 50
annual catches , 89- 90 state of knowledge, 31-32
seaso na l patterns, 88- 89 Bering Sea, 339
impact on benthic community, 90- 91 Biodiversity, effects of coral bleaching, 269-275
impact on shrimp stock s, 90 Biofilms, 40, 42, 44
Iat it ud inal grad ients, 79- 84 Black Sea, 65, 67, 80, 88
life history traits, 84-87 Bleaching, 25, 26, 27, 29, 38, 41, 47, 49, 51
age,87 effects on cora l-reef fishes, 251-296
growth, 84- 86 Bottom-up cont rol, 65
settlement, 84 Boundary layer, 39
size at hatching, 84 Bouyancy, 125, 162 , 178
s ize at maturit y, 87 Brood care, 219-220, 234
reproduction , 83 -84 By-catch, 87, 88, 90, 9 1
seasonal mi gratio n, 80- 82
seawater temperature, 79- 80
sy nthesis, 91- 94
distributional range, 91 - 92
c
future research, 94 Ca lorimetry, 10
latitudin a l trends, 92- 94 Camou fl age, 105, 122, 124, 168, 169, 179, 180
taxonomic status a nd genetic population structure, Cannibali sm, 74, 77, 79, 344
66-67 Car ibbean Sea, 27, 31, 36, 37, 42 , 44, 47, 48, 117
407
SUBJ ECT INDEX
Ce ll q uota models, 1-23 Disease, of corals, 25, 26, 27, 4 1

a ppli cab ility of approach for diffe rent nutrie nt s, /0- // Dispe rsa l, 203,204, 207,209, 2 10, 2 12,225,226,229,23 1
ce ll q uota description, 1-3 coral, 26, 29, 3 1, 33, 35, 38, 40,4 1- 42 , 50
cell vs bi omass quota descripti ons, 3-8 octopus la rvae, 105, 1/ 0- 112, 164, 174 - 175, 184, 185
competiti on, nutrie nt suppl y ratios a nd stoichometri c Distributi on patterns, octo pus larvae, 173 - 176
predator-prey models, 16- 17 Disturbance, 252, 254, 255, 256, 257, 262, 263, 264, 266,
e mpiri ca l and mechani stic relationships, 8- 10 267,268,269,270,27 1,272,273,275,276,
mi sconceptions and mi sundersta ndings, 1/- 13 277,270,280
nutrient acqui sition, 13-16 Di versit y, algae, 26-29
si mul atin g genetic and phenoty pic di versity, / 7 octopus larvae, 109, 11 0, 171- 173, 184
concl usions, 18 phytopla nkton, 17, 18
Che morece ption, 105, /30-13 1 DNA seque ncing, 67, 172
Chro matophores, 105, 106, 115, 11 6, 11 7, 111 8, 134, 144, Dormancy, 209
162, 168, 169, 172, 177, 179- 180, 182 Dredg in g, 27
Climate cha nge, 25, 26, 51, 251 ,252, 253, 254, 257, 270, Droop cell q uota mode l, 1-23
272, 279, 281 , 282 ,336,358
Clim ate- induced coral bleachin g, effects on coral-ree f
fi shes, 251-296 E
assoc iations between fi shes a nd coral reef habit ats,
Ecosystem models, I, 5, 8, II , 18
256- 257
EINin o,252,254, 272
conclu sions and future directi ons, 281-282
Energy budgets, 65, 93
effects of climate-induced coral bleaching on coral
Eutroph ication, 27
reef fi shes, 257-267
Ex tin ction, 25 1,252, 253,257, 269,270, 27 1,272,274,
coral as settlement habitat, 266
275,28 1
coral-dwellin g fi shes, 264-265
corallivorous fi shes, 260-264
loss of live coral, 259-266 F
loss of topographi c compl ex it y, 266-267
future threats to bi odiversity, 269-275 Fish po pul ations, 92, 232,268,276, 33 1, 332, 333, 334,
ecolog ical spec ialisati on. 272-275 339, 350, 353
ra rity in coral reef fi shes, 272 Fisheri es, coral-reef, 275-278, 279
restricted- range coral reef fi shes, 270-272 Crangon, 65, 66, 87-91, 94
ma nagin g effects of climate- induced coral bleachin g, impacts, 87, 90- 9/ ,94
279-281 ma nagement, 232
mass bleac hing: geographi c ex te nt a nd d iffe re nt ia l oceanog raphy, 331-364
effect s, 253-255 octopus, 106, 107
pe rsiste nce and recovery of fis h assembl ages, 268-269 Fishing mort alit y, 335, 347, 349, 350
soc io-eco no mic conseque nces, 275-279 Functi onal gro ups, algae, 27, 29, 30, 38. 42, 47, 50
fi she ries, 275- 278
to uri sm, 278-279
Coastal ecosyste ms, 65, 66 G
Co nn ecti vit y, 23 1,232, 233,297, 299, 303,308. 313-315, Ga lapagos Islands, 272
32 1, 338, 354 Genetic popul ation structure, 65,66- 67,7 1,84,87
Cont inuo us pl a nkton recorde r, 358 Georges ba nk , 337, 344, 348
Cora l bleac hin g, effects on cora l-reef fi shes, 251-296 Geotax is, 164
Cora l reefs, effects of be nthic a lgae, 25-63 Globa l wa rming, 252, 263, 343
Cora l-reef fi shes, e ffe cts of coral bleac hin g on, 251-296 e ffect on octo pu s larvae, 106, 183- 184
Cora l Sea, 11 7, 11 8, 11 9, 162, 163. 168, 175 G razin g, 27, 40,47
Core rin gs, 337, 338 G reat Ba rrie r Reef (GB R), 26, 29, 30, 33, 42, 49, 254, 259,
Criti cal pe ri od/stage, 33 1, 338 263,264,274
C ushin g's hy pothes is, 33 1, 332, 333, 338-343 G ulf Strea m, 336, 337
D H
Defences, 105, 145, 168- 169, 209, 234 Habitat ava il abilit y, 265
Di gestive e nzy mes, octopu s la rvae, 149-150 degradati on, 266,270
systems, octopu s larvae, 13/ -133 loss, 280
408
SUBJECT INDEX
management, 281 ecological perspective, 230-233

modification, 257, 259, 277, 278 aquaculture implications, 233
perturbation , 264, 268, 27 I fi sheries management implications, 232
struct ure, 25 I, 253, 256, 267, 268, 279, 28 I, 282 maternal and sublethal effects, recruit
Hatching, octopu s larvae, 105, 106, II 1-113, I 14, I 15, I 17, production, 230
I 18, I 19, 120, 126, 127, 128, 130, 131, 132, populations, 230-232
134, 135, 136-141, 142, 147, 148, 151, 156, evolutionary perspective, 233-234
158, 161, 164, 166, 168, 170, 171 175, 176, pollution resistance, 233-234
177, 185 maternal effects and range expansions, 233
Hjort, J., 33 I, 332, 333, 338, 342 theoretical considerations, 229-230
Hurri canes, 25, 27 maternal effects: definitions and usage, 205-207
new approaches and directions, 234-235
ma rine algae, 234
I paternal effects, 234-235
quantitative genetics approaches, 234
ｉｃＭｐｾｓＬＲＹＳＰＱＬＳｉＴＬＳＲＱ＠
types and sources of marine maternal effects,
Isoen zy mes, 65, 67, 93 2/0-229
Isotope ratios, 302, 303, 305, 307, 309, 316, 324 adaptive manipulation of offspring phenotype,
Isotopes, 299, 300,302, 303, 304,308,311,315, 316, 317, 225-226
319, 323, 324 brood care, 2/9-220
constraints on anticipatory maternal effects,
227-229
K information acquisition costs, 227
information reliability limits, 228-229
Kelp fo rests, 39
other constraints, 229
production costs, 227-228
mate choice as a maternal effect, 224-225
L maternal environmental effects, 226-227
Kiilliker organ, 105, I I I, I 12, I 17, 119, 120, 121 , 122, 123, maternal investment, 210-219
I25, 177, I80 maternal nutrition, 217-219
Lateral line, octopus larvae, 105, 126, 128- 130, 177 maternal size, 2/7
Life-history patterns, 297, 298, 322 offspring provisioning, 2/1-214
strategies, I05, I06, I07 seasonal variation, 214-217
traits, Crangon, 84-87 small-scale temporal variation, 2/7
Lipids, 105, 135, 151, 153- 154 offspring release, 220-224
Longevity, 266, 270, 275 marine release site effects, 221-223
offspring release timing, 223-224
terrestrial oviposition effects, 22/
ｾ･､ｩｴｲ｡ｮ＠ Sea, 65, 67, 71, 80, 84, 85, 92, 93, 107, 136,
M
138, 139, 140, 141, 142, 157, 167, 168, 171,
ｾ｡ｮｧ･ｭ･ｮｴＬ＠ coral reefs, 51,251 , 253, 279,280, 282 172, 180, 181
fisheries, 232- 233, 332, 333, 338, 345, 347, 352, 353, ｾ･ｩｯｦ｡ｵｮＬ＠ 74, 77, 78
355 ｾ･ｴ｡ｭｯｲｰｨｳｩｳＬ＠ 29, 31, 37, 43, 73, 105, 177, 182, 319, 341
ｾ｡ｲｩｮ･＠ Protected Areas ＨｾｐａＩＬ＠ 278,280, 281,282 ｾ･ｴ｡ｰｯｵ＠ lation s, 353, 354, 355
ｾ｡ｲ｣ｨＭｭｩｳｴ＠ hypothesis, 331, 332,338-343 ｾｩ｣ｨ｡･ｬｳＭｾ･ｮｴ＠ kinetics, 2, 3, 8
ｾ｡ｴ･＠ choice, 203, 224-225 ｾｩｧｲ｡ｴｯｮＬ＠ 80-82, 84, 86, 92, 316, 320, 323
ｾ｡ｴ･ｲｮｬ＠ care, I I2, 203, 219, 220, 221, 229 ｾｯ､･ｬｳＬ＠ cell quota, 1-23
ｾ｡ｴ･ｲｮｬ＠ effects in the sea, 203-250, 334, 335, 336 ｾｯｮ､＠ equation, I, 2, 10, 13, 14
examples of maternal effects in terrestrial systems, ｾｯｲｰｨｧ･ｮｳＬ＠ 42, 43
208-210 ｾｯｵｬｴｩｮｧＬ＠ 70, 71, 73, 75, 84, 85, 86
ａｾｅｳ＠ vs ｓｾｅｳＬ＠ 210
dispe rsa l, 209
offspring defences, 209
N
offspring dormancy, 209
offspring provisioning, 208-209 Neoteny, I 10, I 15, 120, 182- 183
oviposition site, 209 North Atlantic Oscillation (NAO), 79, 89, 349
importance of maternal effects in marine systems, North Sea, 67, 87, 88, 89, 90, 91, 334, 347
229-233 Nutritional requirements, octopus larvae, 134- 143
409
SUBJECT INDEX
0 Kolliker orga ns, 119- 120

loose sk in film, 123- 125
Octo pu ses, benthic, biology of planktonic stages , sc ulptural compo nen ts, 122- 123
105-202 s ucker su rfaces, 122
a nthropogeni c impacts, 183- 184 perma ne nt para la rve, neoteny a nd holope lag ic
glo ba l warming, 183-184 octopuses, 182- 183
overfis hing, 183 predato rs on eggs and larvae, 169- 171
pollution, 183 prolonged parala rva l stages, micronektonic paralarvae,
behaviour, 159-169 182
crawling, 163 se!!lement process, 176- 18 1
defen ces, 168-169 behavioural and ecologica l cha racter istics,
responses to li ght, g ravity, 163- 168 180- 18 1
sw imming, 159- 163 morpholog ical characte ri sti cs, 177- 180
concluding re marks, 184- 185 chromatopho re genes is, sk in co mpone nts,
distribution patterns, 173- 176 179- 180
geog raphic range, 173-174
horizontal pupillary response, 180
hori zontal dispersa l, 174- 175
positive allometric arm grow th , 177- 179
re lation ships between larva l a nd adult populations,
spawning characteristi cs, 110- 113
176
egg care a nd emb ryon ic development, 110- 111
sampling methods, 173
hatch ing and dispersal, 111-1 13
vertical di stributio n, abundance, 175- 176
duration, 112-113
food, fee ding, nutritional require ment s, 134- 143
mechanics, Ill
biochemical profiles, nutritio na l req uirement s,
stimulus, Ill
151- 156
timing, 111- 112
protein s and amino ac ids, 151- 153
species identifi cati o n, diversity, 171- 173
lipids and fatty ac ids, 153- 154
Offspring fitness, 203,206,207,210,211,214,219, 220,
elemental composition, 155- 156
22 1,224
buccal mass, beaks, external di gestio n, 148- 149
Offspring provisioning, 204,208-209,211- 214, 217, 220,
digestive enzymes, 149- 150
229,233
food searching, prey capture, 143- 148
Ornamental fish trade, 277, 278
ine rt prey, 146- 148
live prey, 143- 146 Otolith che mi stry, 297-330
grow th, duration of pla nkt onic stage, 156- 159 conclusio n and future research needs, 322-323
agein g, factors influe nc ing grow th , 158- 159 further data and stati sti ca l co nsiderati ons , 321-322
size at hatching, 156- 158 detecting variab ilit y at different sca les, 32 1
natural prey, 135- 142 limit ati ons in usi ng natura l tags to assess
nutrient absorption , impo rtan ce o f skin , 150- 151 philopatry and movement rates, 322
res piration , 151 repeated measurements o n an oto lith , 32 1-322
skin absorption, 150- 151 influe nces o n otolith tags, 301- 303
prey size and den sity, 142- 143 methods for determining movements and life-hi story
yo I k re se rves , 134- 135 meas ureme nts, 308-32 1
mo rpltolog ica l characteri sti cs of para la rvae, 113- 134 assessing co nnectivit y among gro ups using natural
body form, mu sc ul ature, 113- 116 chemica l tags in otolit hs, 3/3- 315
digestive system, 131- 133 estimates of movement and life- hi story trait s of a
bucca I mass, 131 single fish group, 308- 313
digestive tract, 131- 133 profi le analysis to define li fe-history variati on
ink sac, 133-134 within a population , 317- 318
se nsory systems, 125- 131 profile analysis to describe movements through
central ne rvou s syste m, 125-126 different e nvironments, 319- 321
chemoreceptors, 130- 131 tran sgenerational marks to determine parentage
mechanoreceptors, 127- 130 and natal origi ns, 315- 317
photoreceptors, 126- 127 oto lith sa mplin g methods, 299- 303
surface epithelia, integumentary structure, variation in water a nd otolith chemi stry, 303- 308
116- 125 otolith chem ist ry, 305-308
chromatic elements, 116- 118 water chemistry, 303- 305
hatc hing gland , 118- 119 Overfishing, 27, 49, 106, 183, 347, 349
integumental po res, glandul a r ce ll s, 120- 122 Oviposition, 203,204,207, 209, 2 10, 221,222 , 223,228
410
SUBJECT INDEX
p Respiration, octopus larvae, /51

Rhythms, Ill, 112, 159
Papua New Guinea, 254, 266, 270, 276, 277 Ricker model, 334, 339, 344, 347, 353, 354
Paradigms in fi sheries oceanography, 331-363
conclusion , 357-358
Cushing's Match/mismatch hypothesis, 338-343
'Bigger is better' hypothesis, 340- 341
s
'Growth selective' hypothesis, 342-343 Scale effects, 38, 39, 42, 43, 46, 49-50, 51
'Stage duration' hypothesis, 341-342 Scotian Shelf, 335,336, 337, 338,339,341, 345, 348, 350,
eggs and larvae designed for dispersion/colonization 354, 356, 357
(panmixia), 337-338 Sedimentation, 27, 29, 30, 33, 34, 38, 39, 40, 45-46,
populations cannot irreversibly collapse /collapsed 47,51
populations recover in absence of fishing, Selective tidal transport, 74
347- 355 Sensory systems, octopus larvae, 125-131
recovery synonymous with rebuilding, 356- 357 Settlement, coral, 25, 26, 29, 30, 31, 32, 33, 35, 36, 37, 38,
SSB proxy for reproductive potential of stock, 332-337 39,40,41,42- 46,47,48,49,50,51,52
stocks can be managed in isolation, 355-356 coral-reef fishes, 251, 258, 261, 266, 268, 276
updated recruitment models invariably fail, 343-347 Crangon, 71, 73-74 , 79,84
Parasites, 220, 222 octopus larvae, I05, II 0, 117, 118, 120, 126, 136, 137,
Parental care, II 0 138, 139, 140, 147, 150, 159, 161, 162, 164,
Paternal effects, 206, 234- 235 168, 172, 174, 175, 176-181, 182, 184, 185
Persistence, 251, 259, 268- 269, 274 Sex determination, 204, 225
Pesticides, 40
Shading,34,38,41,45,46,47,48
Phenology, 252
Spawning, behaviour, fishes, 338
Philopatry, 321, 322, 323
characteristics, of benthic octopuses, 105, 110-113
Photon flux densities, (PFD), 10
coral-reef fishes, 315,316, 317
Photosynthesis, 38, 40, 46
stock biomass, (SSB), 332-337, 345, 347, 349, 352, 353,
Phototaxis, 105, 164, 168, 173
354
Phytoplankton, I, 2, 4, 8, 9, 10, II, 14, 15, 16, 17, 18,339,
Specialisation, 272- 275
355, 356
Specialist species, 256, 257, 262, 263, 264, 265, 267, 268,
Pollution, 27, 30, 40, 51
270,272,277,281,282
effect on octopus larvae, 106, 183
Speciation, 204
resi stance, 209, 225, 231, 232, 233-234
Spring bloom, 339, 340, 345
Polychlorinated biphenyls (PCBs), 319
Statocysts, 126, 127- 128
Population cycles, 204, 229
dynamics, Crangon , 65 Stock recruitment models, 332, 334, 337, 339, 347, 350,
octopus larvae, I05, 181 353
reef fishes , 264, 270, 282 reproductive potential (SRP), 335
structure, Crangon, 65, 66- 67, 87, 92, 93, 94 Storms, 256, 257, 263, 264, 267, 279, 282
Predation, 65, 77, 78, 86, 88, 90, 91, 93,206, 208, 209, Swimming behaviour, octopus larvae, 144, 145, 146, 156,
210, 212, 213, 214, 219, 222 , 224, 225, 227, 159-163, 174
228, 230, 251 , 264,265,266,267,268,341
Predator-prey model s, 16- 17
PUFAs, 135, 154 T
Tags, artificial , 298, 315, 316,317
chemical , 297, 298,299, 300,301, 305, 308, 309, 310,
R 311, 312, 313, 315, 317, 319, 320, 321 , 322,
Rarity, coral-reef fishes, 272 323,324
Recruitment, 308, 309, 313, 314, 315 natural , 298,299,303,309,310,311,312,313,314,
coral, 26, 28, 29, 30, 31, 32, 33, 25, 39, 41, 42, 43, 45, 315,3/6,318,321,322
46,47,50,51 Top-down control, 65, 78, 79, 94
Crangon, 65, 79, 89, 90, 91 , 992, 93, 94 Topographic complexity, coral reefs, 251,253, 256, 258,
fishes,331, 332, 333, 334,335, 336, 337, 338, 339,340, 259,260,266- 267, 268,269,276, 280, 281,
341, 342, 343- 347, 339, 350 351, 353, 354, 282
355,356,358 Total egg production (TEP), 332, 334
Redfieldratio,6, II, 15, 16,18 Tourism, 275, 278-279
411
SUBJECT INDEX
Ts un amis, 256
Turbulence, 33, 38, 39
w
Wadde n Sea, 70, 73 , 79, 82, 83, 84, 85, 86, 93
White Sea, 65
u
Ultraviolet radiation , 38, 4 1, 46
X
Upwell ing, 338, 343
X-ray microana lys is, 5
v
Virtual po pulation ana lysis ( VPA}, 343
z
Vitamin 8 12 , 2 , 3, 4, 9, 10 Zoopla nkto n, 9, 17, 136, 137, 144, 145, 169, 175, 183,339,
Von Be rta la nffy fun ction , 86 355, 356
412

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.

Founded by Harold Barnes

CRC Press is an imprint of the

© 2008 by R.N. Gibson, R.).A. Atkinson and ).D.M. Gordon

No claim to origina l U.S. Government works

International Standard Book Number-13: 978-1-4200-6574-9 (Hardcover)

and the CRC Press Web site at

Autecology ofCrangon crangon (L.) with an emphasis on latitudinal trends 65

Biology of the planktonic stages of benthic octopuses 105

Effects of climate-induced coral bleaching on coral-reeffishes- ecological and

Otolith chemistry to describe movements and life-history parameters offishes:

Paradigms in fisheries oceanography 33 L

Author Index 365

Systematic Index 399

Subject Index 407

USE, ABUSE, MISCONCEPTIONS AND INSIGHTS

The quota description

The relative growth rate 11rcl is thus given by

_ (1 + KQ) · (Q-Qmin) (5)

Cell versus biomass quota descriptions

1.6 • 1.6 ｾ＠ .... -.:: 0 N-limited

2.0 0 N-limited 2.0

Ti me(d) Time (d)

C-q uo ta (gN gC- 1) C-quota (mgP gC- 1)

0.00 0.05 0.10 0.15 0.20 10 15 20

0.0 0.1 0.2 0.3 0.4 0.5 10 20 30 40 50 60

Cell-q uota (pgN cell - 1) Cell-q uota (fgP cell- 1)

Empirical to mechanistic relationships

f..L=f..l . Q-Qmin (7)

could be viewed as unjustified. Doing so could be considered as similar to replacing a hyperbolic

Applicability of the quota approach for different nutrients

0 50 100 150 200 250

Misconceptions and misunderstandings over high quota values

Nutrient acquisition - the quota-transport interface

Competition, nutrient supply ratios and stoichiometric

Simulating genetic and phenotypic diversity

EFFECTS OF BENTHIC ALGAE ON THE

The diversity of algae and their effects on coral replenishment

Table 1 Comparison of algal communities resulting on degraded reefs

Coral replenishment processes, resilience and terminology

Table 2 Summary of literature on coral recruitment, classified by phase of recruitment, and

Macroalgal functional groups

Leathery macrophytes 261. 63 16' 3'· 29 211T. 2H j 9. 11T,29. :w

2 "· 42 ,,. 7"- 44-49

Other/spatial variation 11 7· 1.s. n. 21. 30.12 .

Other ecological factors

Allelopathy ) 20. '!.7. :'18

Effects of macroalgae on habitat conditions

Effects of macroalgae on benthic space

Anicul ated calcareo us L-7 L-3 L-' o

Filamentous & diminutive forms L- I. IO.J l.-12

(<2 em) including EAC and turf S- 1. H S+ 10 S- 31 S- 17 · 33 S- 17 S-40 S- 17 · 33 S- 17 S-'o

Amphiroa anceps Artie. CoA Dead Indian Lab Acropora millepora 1

CCA , crustose calcareous algae; CCoA, crustose coralline algae.

' Algae on settlement tiles.

Impacts of macroalgae on light conditions

Impacts of macroalgae on water flow and turbulence

Impacts of macroalgae on benthic sediment regimes

Impacts of macroalgae on chemical environments,

Impacts ofmacroalgae on microbial environments

Effects of macroalgae on coral fecundity,

Effects of macroalgae on the settlement of coral larvae

Positive effects of macroalgae on coral settlement

Negative effects of macroalgae on coral settlement

M = 0.00584DT 1347 (8)

dL/dt = 0.1625 + 0.01025T- 0.00403L (9)

dL/dt = 0.1625 + 0.01025T- 0.00403L (10)