ArticlePDF Available

Abstract and Figures

As the world’s oceans continue to undergo drastic changes, understanding the role of key species therein will become increasingly important. To explore the role of Atlantic cod (Gadus morhua Gadidae) in the ecosystem, we reviewed biological interactions between cod and its prey, predators and competitors within six ecosystems taken from a broad geographic range: three are cod-capelin (Mallotus villosus Osmeridae) systems towards cod’s northern Atlantic limit (Barents Sea, Iceland and Newfoundland–Labrador), two are more diverse systems towards the southern end of the range (North Sea and Georges Bank–Gulf of Maine), and one is a species-poor system with an unusual physical and biotic environment (Baltic Sea). We attempt a synthesis of the role of cod in these six ecosystems and speculate on how it might change in response to a variety of influences, particularly climate change, in a fashion that may apply to a wide range of species. We find cod prey, predators and competitors functionally similar in all six ecosystems. Conversely, we estimate different magnitudes for the role of cod in an ecosystem, with consequently different effects on cod, their prey and predator populations. Fishing has generally diminished the ecological role of cod. What remains unclear is how additional climate variability will alter cod stocks, and thus its role in the ecosystem.
Content may be subject to copyright.
Trophic role of Atlantic cod in the ecosystem
Jason S. Link
1
, Bjarte Bogstad
2
, Henrik Sparholt
3
& George R. Lilly
4
1
National Marine Fisheries Service, Northeast Fisheries Science Center, Woods Hole, MA 02543, USA;
2
Institute of Marine
Research, PO Box 1870 Nordnes, N-5817 Bergen, Norway;
3
International Council for the Exploitation of the Sea, H. C.
Andersens Boulevard 44-46, 1553 Copenhagen V, Denmark;
4
Fisheries and Oceans Canada, Northwest Atlantic Fisheries
Centre, PO Box 5667, St John’s, NL, Canada A1C 5X1
Introduction 2
Comparison of case studies from major cod ecosystems 2
Baltic Sea 4
North Sea 6
Barents Sea 7
Iceland 12
Eastern Newfoundland–Labrador 13
Gulf of Maine–Georges Bank 15
Generalities, comparisons and synthesis 17
Basic cod feeding ecology 17
Cannibalism 18
Abstract
As the world’s oceans continue to undergo drastic changes, understanding the role of
key species therein will become increasingly important. To explore the role of Atlantic
cod (Gadus morhua Gadidae) in the ecosystem, we reviewed biological interactions
between cod and its prey, predators and competitors within six ecosystems taken from
a broad geographic range: three are cod-capelin (Mallotus villosus Osmeridae) systems
towards cod’s northern Atlantic limit (Barents Sea, Iceland and Newfoundland–
Labrador), two are more diverse systems towards the southern end of the range
(North Sea and Georges Bank–Gulf of Maine), and one is a species-poor system with
an unusual physical and biotic environment (Baltic Sea). We attempt a synthesis of
the role of cod in these six ecosystems and speculate on how it might change in
response to a variety of influences, particularly climate change, in a fashion that may
apply to a wide range of species. We find cod prey, predators and competitors
functionally similar in all six ecosystems. Conversely, we estimate different magni-
tudes for the role of cod in an ecosystem, with consequently different effects on cod,
their prey and predator populations. Fishing has generally diminished the ecological
role of cod. What remains unclear is how additional climate variability will alter cod
stocks, and thus its role in the ecosystem.
Keywords Competitor, ecological function, Gadus morhua, North Atlantic,predator,
prey
Correspondence:
Jason S. Link,
National Marine
Fisheries Service,
Northeast Fisheries
Science Center,
Woods Hole, MA
02543, USA
Tel.: +1-508-495-
2340
Fax: +1-508-495-
2258
E-mail: jlink@
mercury.wh.whoi.edu
Received 8 Jun 2007
Accepted 23 Jun 2008
Journal compilation Ó2008 Blackwell Publishing Ltd
No claim to original US government works 1
F I S H and F I S H E RI E S , 2008, 9, 1–30
Cod prey and other fisheries 19
Cultivator effects 20
Cod and marine mammals 20
Climate change 21
Summary 22
Acknowledgements 23
References 23
Introduction
The Atlantic cod (Gadus morhua Gadidae) is an
important species in many of the world’s ocean
systems from an economic, ecological and cultural
perspective (Jensen 1972; Garcia and Newton
1997; Kurlansky 1997; FAO 1998). It is a species
facing notable changes within the ecosystems in
which it lives, and documenting the role of cod in
the ecosystem will be important as these systems
continue to change. As overfishing of the world’s
fish stocks (Garcia and Newton 1997; FAO 1998)
and climate change scenarios continue to be
expressed (ACIA 2005; IPCC 2007), examining
how marine fishes will respond remains a critical
issue. In many respects, cod is one of the few fish
species for which we should be able to do this
and, as such, serves as an example species.
Comparable species from other ecosystems (be
they ecological or economic or cultural equiva-
lents) may not have had the level of study that
cod has had. Thus scientists and managers in
those systems may be informed by the insight
obtained from an examination of cod.
Our focus here is twofold: to review the extent to
which cod dynamics and distribution can be influ-
enced by interactions with predators, prey and/or
competitors, and to explore the extent to which
changes in cod stock size can affect other species in
the ecosystem. We highlight the extent to which
population change, particularly due to fishing and
climate variability, may affect the interactions
between cod and other members of its ecosystem.
To help us explore the role of cod in the
ecosystem, we review biological interactions
between cod and its prey, predators and competitors
within six ecosystems (Table 1; Fig. 1). These six
examples are from a broad geographic range: three
are cod-capelin (Mallotus villosus Osmeridae) sys-
tems towards cod’s northern limit across the top of
the Atlantic (Barents Sea, Iceland and Newfound-
land–Labrador), two are more diverse systems
towards the southern end of the species’ range on
either side of the Atlantic (North Sea and Georges
Bank–Gulf of Maine), and one is a species-poor
system with an unusual physical and biotic envi-
ronment (Baltic Sea). We then attempt a synthesis
of the role of cod in these and other ecosystems and
speculate on how the role of cod might change in
response to a variety of influences, particularly
climate change.
Comparison of case studies from major cod
ecosystems
For each of six ecosystems (Fig. 1), we describe the
diet of cod and the way that changes in the
abundance or availability of prey have affected
the cod’s diet and recruitment, growth and mortal-
ity. Of considerable interest is the extent to which
changes in the size of cod populations have affected
the dynamics of prey populations. We also overview
some changes in predator populations, and discuss
ways in which these predators may have affected
cod dynamics, especially recruitment but also the
mortality of adults. The possibility of competition is
also discussed. In some instances, we highlight
phenomena that are particularly well studied within
a specific cod population or ecosystem, but less so in
others.
It is not our intent to compile an extensive review
of the prey and predators of cod or of cod catch and
population dynamics. The diversity of the food of
cod has been described in delightful detail by some
early investigators (Zatsepin and Petrova 1939;
Brown and Cheng 1946; Hansen 1949; Popova
1962; Rae 1967). More recent studies tend to report
cod prey in a more quantitative and aggregated
manner. The predators of cod are less thoroughly
documented. Pa
´lsson (1994) and Methven (1999)
have compiled informative lists and reviews of this
information for several ecosystems.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
2 No claim to original US government works
Table 1 Key parameters for cod in the six example ecosystems.
Baltic Sea North Sea
Barents
Sea Iceland
Newfoundland/
Labrador
Gulf of Maine/
Georges Bank
Years of peak abundance Early 1980s 1970 Mid-1930s and
mid-1940s
Around 1930 and
mid-1950s
Early 1960s Late 1960s
Current cod B/L as % of peak cod B/L 12 (B) 20 (B) 35 (B)
40 (L)
30 (B)
35 (L)
2 (B) 10–15% (B)
Peak cod B/L as % of total fish B/L during cod peak 32 (B) 4 (B) 25 (B) 50 (L) NK 25–30% (B)
Current cod B/L as % of current total fish B/L 4 (B) 1 (B) 25 (B) 25 (L) NK 5–10% (B)
Thermal type of ecosystem Temperate enclosed Temperate Boreal Boreal Boreal Temperate
General interaction strengths in ecosystem Moderate–strong Moderate–weak Strong Strong Moderate–strong Weak
Cod growth dependant on forage fish Moderate No Strongly suspected Strongly suspected Possible Not Likely
Cod recruitment dependant on zooplankton Maybe Maybe Maybe Maybe NK Not likely
Forage fish predation on cod eggs/juveniles Strong Maybe Moderate Maybe NK Minimal
Marine mammal predation on cod Minimal Minimal Moderate Strongly Suspected Moderate-minimal
Predatory release of cod prey as cod decline Yes Possible Suspected Yes Yes Some
Increase in invertebrate fisheries after cod decline? No – salinity too low
for crustaceans
Yes Possible Yes Yes Possible
B, biomass; L, landings; NK, not known.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 3
Baltic Sea
The Baltic is a unique marine system as it is the
world’s largest brackish water sea. Salinity is
generally <20&, with a declining gradient from
south to north, where it is close to zero. Further-
more, salinity varies interannually mainly as a
result of sporadic inflows of saline water from the
North Sea. Cod concentrates in the southern areas
and can spawn successfully only where the salinity
is above 11&(Westin and Nissling 1991). A
further physical feature of the Baltic Sea is that
the bottom water in the deepest parts is often
oxygen depleted. As these are generally the areas
preferred by cod for spawning and feeding, the level
of dissolved oxygen is an important factor for the
stock dynamics of cod in this area.
The fish community in the Baltic Sea is very
simple as it is dominated by three main species: cod,
herring (Clupea harengus Clupeidae) and sprat
(Sprattus sprattus Clupeidae) (Sparholt 1994). Cod,
herring and sprat are very important for the
commercial fishery with annual landings of around
0.5–1.0 million tonnes. Cod catches peaked in 1984
and the stock is currently depleted (ICES 2003b,
2005b). The sprat stock now dominates (landings of
340 000 tonnes in 2002) the Baltic whereas
herring is depleted, with the management system
attempting to rebuild herring and cod. The propor-
tion of cod relative to all fish biomass in the
ecosystem is 4% at present, but has been as much
as 30% in the 1980s when the cod stock peaked and
sprat were concurrently sparse (Table 1).
Species interactions in the Baltic have been
investigated during the last two decades by several
entities, including International Council for the
Exploration of the Sea (ICES) Groups, European
Commission projects and individual scientists (see
Ko¨ster et al. 2003 for a detailed review). Cod eat
herring and sprat, while herring and especially sprat
eat cod eggs. These interactions seem to result in at
least two semi-stable states of the ecosystem: one
dominated by sprat that keeps cod down via cod egg
predation and another dominated by cod via
predation on sprat. This is shown by direct mea-
surement of the diet composition, calculations of
total amounts consumed and by historical stock
assessments. Other interactions that might indi-
rectly influence cod are less well studied. For
example, a large sprat stock seems to depress the
herring stock by food competition (Mo¨ llmann and
Ko¨ster 2002; Mo¨llmann et al. 2003, 2005). Salmon
(Salmo salar Salmonidae) are also present in the
system and can eat a notable amount of sprat
(Karlsson et al. 1999; Hansson et al. 2001). The
growth of salmon is related to the biomass of sprat,
implying that this species benefits from the sprat
dominated state. However, there are also indications
Figure 1 Location of the six ecosystems examined in this study.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
4 No claim to original US government works
that a large sprat stock increases the incidence of
the so-called M74 disease in salmon, perhaps via a
B-vitamin esterase in sprat, negatively affecting the
salmon stock. Thus, cod directly or indirectly
influences sprat and herring stocks, herring growth,
and salmon growth and health.
Climate variability has meant increased precipi-
tation and river run off and less frequent inflows
from the North Sea, resulting in a lower salinity in
the Baltic Sea. This negatively influences not only
the cod recruitment but also the amount of the
marine copepod Pseudocalanus elongates (Clausoca-
lanidae), which is an important prey for herring and
sprat. Thus these phenomena influence the produc-
tion of these two forage fish species and indirectly
the production of cod. Due to a very long turnover
time for the water (around 30 years), the Baltic Sea
is highly vulnerable to eutrophication, and this has
been very pronounced in the 20th century. Thurow
(1997) showed that herring and sprat biomass
increased in the 1900s at a time corresponding
approximately to the intensification of eutrophica-
tion, also ultimately influencing cod stocks. Thus,
although the Baltic Sea fish community is simple in
terms of number of fish species, it is quite compli-
cated in terms of stability and interactions.
As in other ecosystems, cod in the Baltic is a
generalist, eating whatever is available (Sparholt
1994). Herring and sprat constitute about half the
diet, with the isopod Saduria entomon (Chaetiliidae)
accounting for another third. Other invertebrates
such as the polychaete Harmothoe¨ sarsi (Polynoidae)
and the macroplanktonic crustacean Mysis mixta
(Mysidae) make up a small percentage of the diet for
large cod, but can constitute up to two-thirds of the
diet for small cod. Juvenile cod constitute a small
percentage of the diet of large cod, with other fish
constituting 10% (Fig. 2). Annual variation in the
diet reflects variation in abundance of the prey field.
In the 1980s, cod consumed about 1.5 million
tonnes per year (Sparholt 1994), and ate signifi-
cantly more herring and sprat than was taken by
the commercial fishery. Recently, consumption has
dropped to around 300 000 tonnes due to the
reduced size of the cod stock.
Growth of cod in this ecosystem has been related
to available biomass of cod prey items (Gislason
1999) and there is evidence of density-dependent
effects (ICES 2003d, 2005b), with consequences for
maturity and fecundity. The variation in weight at
age in the period 1977–1997 was a factor of about
1.5.
A model of harvest strategies for all the commer-
cial fisheries in the Baltic shows, somewhat surpris-
ingly, that revenue is maximized by fishing down
the cod stock and thus increasing the catch of
herring and sprat (Gislason 1999). The price of cod
was assumed in the model to be 10 times the price
of herring and sprat. However, the effects of
predation on cod eggs by herring and sprat were
not included, because they have only been investi-
gated recently. The conclusion would probably be
very different if this interaction was included.
Cannibalism seems to be a significant regulatory
mechanism for the cod stock in periods when the
cod stock is large. A Ricker type stock–recruitment
curve results from the assumption that production
of 0-group cod is proportional to cod spawning stock
biomass (SSB) (Sparholt 1995, 1996a,b) with
recruitment (at age 3) peaking at a spawning stock
size of 550 000 tonnes. This observation would
indicate some form of compensation, notably via
consumption of juveniles.
Total consumption of juvenile and adult cod by
harbour porpoises (Phocoena phocoena Phocoenidae)
and grey (Halichoerus grypus Phocidae), harbour
(Phoca vitulina Phocidae), and ringed (Phoca hispida
Phocidae) seals is estimated to be only about 2000
tonnes per year (ICES 1990). However, the biomass
of seals may have been an order of magnitude or
more greater a century ago, and total fish (mostly
herring and sprat) consumption by these marine
mammals has been estimated for that time to be
320 000 tonnes per year (Thurow 1997). The
proportion of cod in the diet at that time was not
Figure 2 Diet of cod (average diet composition by
weight per length group) in the Baltic Sea (adapted from
Sparholt 1996b). Based on 43 544 cod stomachs sampled
in 1977–1990.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 5
known, but it is suspected that the mortality on cod
must have been significant. Seabirds are not major
predators on cod in the Baltic. Some cormorants
(Phalacrocorax spp. Phalacrocoracidae) take juvenile
cod periodically, but only in very small amounts
(ICES 1990).
Cod is the dominant medium-sized (30–100 cm
in length) predator in the Baltic. Salmon is the only
predator that might be of some significance as
competitor. However, such competition is likely
minor as the biomass of salmon is about 10 000
tonnes (ICES 2004c) compared to a biomass of cod
of over 1 million tonnes in the early 1980s and over
0.5 million tonnes until its decline after 1986.
North Sea
Cod has been one of the most important fish stocks
in the North Sea, socioeconomically speaking, for at
least the last two decades. The fluctuations in stock
size and in catches of cod have been described in
detail elsewhere, but we would be remiss without
noting the gadoid outburst from the mid-1960s to
the mid-1980s, where cod and other gadoids, such
as haddock (Melanogrammus aeglefinus Gadidae),
whiting (Merlangius merlangus Gadidae), saithe
(Pollachius virens Gadidae) and Norway pout (Tris-
opterus esmarki Gadidae), exhibited peak abun-
dances (Cushing 1980). The reason for the
outburst was good recruitment in some of those
years (Hislop 1996). Now the cod stock is both
growth and recruitment overfished, with the
spawning stock size below pre-1960s levels (ICES
2004a). The total biomass of fish in the North Sea is
about 10 million tonnes (Andersen and Ursin 1977;
Sparholt 1990, ICES 2003a, 2005a,c), so cod only
constitutes a small proportion of the North Sea fish
community (Table 1) and is therefore not expected
to have a large impact on the rest of the system.
This may have been different historically, before
heavy fishing on the stock began and the stock was
at a higher level of abundance.
A significant amount of research effort has been
devoted to studies of multispecies interactions in the
North Sea for the past two to three decades. ICES
has coordinated major stomach sampling projects,
in 1981 and 1991. In both years about 100 000
stomachs from cod, haddock, whiting, saithe,
mackerel (Scomber scombrus Scombridae), rays (Raja
spp. Rajidae), gurnards (Eutrigla gurnardus Trigli-
dae) and horse mackerel (Trachurus trachurus
Carangidae) were collected and analysed (in
addition to a lesser amount for other species; ICES
1997, 1989). The primary objective was to obtain
input data for the MultiSpecies Virtual Population
Analysis (MSVPA) model for the North Sea (Sparre
1991).
As in other ecosystems, cod in the North Sea eat
what is available within the size range of what they
are capable of ingesting (ICES 1997, 1989). Small
cod eat mainly crustaceans, gradually increasing
the proportion of fish in the diet with ontogeny. All
age groups eat some Annelida as well. The most
important crustaceans are Caridae, Astacidea,
Anomura and Brachyrhyncha (ICES 1997, 1989).
The most important fish species are herring,
Norway pout, haddock, whiting, sandeel (Ammo-
dytes spp. Ammodytidae) and dab (Limanda limanda
Pleuronectidae) (Fig. 3). The available evidence
indicates that cod and other species studied in the
North Sea do not alter their preferences for partic-
ular prey, and that the consumption of a given prey
species by an individual cod is generally propor-
tional to the abundance of the prey. Indications of
this can be seen in Fig. 3 where herring increases in
importance by a factor of about 5 from 1981 to
1991, coinciding with a recovery of the North Sea
herring stock from a spawning stock size of
195 000 tonnes in 1981 to 980 000 tonnes in
1991 (ICES 2004c).
Norway lobster (Nephrops norvegicus Nephropi-
dae) is an important food item of cod and constitutes
about 5% of its food by weight in the North Sea.
This means that cod probably eat more Nephrops
Figure 3 Food composition (by weight) of North Sea cod
in 1981 and 1991 based on ICES Stomach Sampling
Projects (1981: 11 471 cod sampled; 1991: 9719 cod
sampled) (ICES 1989, 1997). The values are calculated
based on data averaged by cod age; weighting is by
stock numbers by age (ICES 2005a) and stomach content
weight by age.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
6 No claim to original US government works
than are caught commercially. There is an increas-
ing trend in the commercial landings of Nephrops in
the last couple of decades, which may be due to
release from predation as the cod stock has
decreased (ICES 2003e). Thus the dynamics of the
Nephrops stocks in the North Sea seem to depend
strongly on the dynamics of cod, as is the case in the
Irish Sea (Brander 1988; Brander and Bennett
1989) and probably other areas where they
co-occur. Norway lobster is the only commercially
important prey species for which cod is the main
predator.
Cod is a cannibal in the North Sea; as such, it is
one of the main predators of its own juveniles. As
elsewhere, at the youngest ages, predation generally
dominates cod mortality, while the fishery takes
over at the older ages. According to the MSVPA
model (ICES 2003a, 2005a,c), predation mortality
is about 1–1.5 per year on 0-group, about 0.5 on
1 group 0.1–0.2 on 2–6 group and 0 on older cod.
The main predators are cod, whiting, gurnards, grey
seals and sea birds (ICES 2002, 2003a, 2005a,c),
with a potentially high predation mortality of
0-group cod given the caveats of MSVPAs (ICES
2003a). Fig. 4 shows natural mortality of 0-group
cod with and without grey gurnards included. The
role of grey gurnard as a predator on 0-group was
analysed in more detail by Floeter et al. (2005),
highlighting the importance of this more recently
prominent piscivore.
It has been claimed that herring and sprat eat cod
eggs and larvae in the North Sea (Cushing 1980;
Daan et al. 1985), but the phenomenon is not as
well investigated in this area as it is in the Baltic,
where it is clearly shown to be important for cod
recruitment (see Baltic Sea). The other main pelagic
species, mackerel, is well investigated via the two
large ICES stomach sampling projects and has been
analysed in the MSVPA model; the results indicate
that it does not seem to interact much with the cod
stock. Cushing (1980) discusses the release of food
with the declining pelagic stocks as a possible factor,
but the data and knowledge are not conclusive.
The role of marine mammals as predators of cod
is not well understood. Among all cetaceans and
pinnipeds, only grey seals have been included in the
North Sea MSVPA but they are responsible for a
relatively small amount of the mortality experienced
by cod. There is little information about food items
of other seals and of whales. This topic merits
further investigation.
Although entirely unclear, there is little evidence
for competition between North Sea cod and other
fish species. Assuming production in the North Sea
is limited, that the growth of cod did not display a
density-dependent decline during the ‘gadoid out-
burst’ when the cod and other gadoid stocks
(potential food competitors) were very large is
indicative of limited competition. This interpretation
is further confounded by changes in North Sea
plankton associated with leading climate indicators
(Beaugrand et al. 2003). The potential for compe-
tition should be further explored by the analysis of
dietary overlap between cod and the other main
predators (whiting, haddock, saithe and mackerel).
Barents Sea
Cod is the main piscivore in the Barents Sea
(Bogstad et al. 2000), with the fluctuations in stock
size and in catches of Northeast Arctic cod
1
further
described elsewhere (Nakken 1994; Hylen 2002).
The stock abundance is about one-third of the peak
level and somewhat below the long-term (1946–
2005) mean (Table 1; ICES 2007); however, the
stock is at present in a healthy state, with current
SSB above B
pa
.
The interactions between cod and the two most
abundant planktivorous species, herring and cape-
lin, combined with variability in climate (tempera-
ture, inflow) to a large extent govern the dynamics
Figure 4 Natural mortality (M = M1 + M2) of 0-group
cod in the North Sea as estimated from MSVPA, with and
without gurnards included as a predator (adapted from
ICES 2003a).
1
The Northeast Arctic cod stock is the same species, Gadus
morhua, being compared to other cod stocks in the other
ecosystems; it is not to be confused with Arctic or polar cod
Boreogadus saida referred to here and in other ecosystems
as cod prey/competitors.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 7
of the Barents Sea ecosystem (Hamre 1994; Hjer-
mann et al. 2007). Cod is a predator on capelin,
herring and young cod (Bogstad et al. 1994; Bogs-
tad and Gjøsæter 2001; Johansen 2003), while
herring prey on capelin larvae. Fig. 5 shows a
simplified Barents Sea food web. Abundant year
classes of herring have a strong adverse effect on
capelin recruitment while they are present in the
Barents Sea at ages 0–3 (Gjøsæter and Bogstad
1998), indirectly influencing the cod stock. In
periods with low capelin abundance, cod switch to
krill and amphipods as prey (Bogstad and Mehl
1997). Low capelin abundance has also been shown
to influence individual growth of Northeast Arctic
cod (Mehl and Sunnana
˚1991).
Russian qualitative cod stomach content data
(frequency of occurrence for the main prey species,
degree of fullness) show that the abundance of
herring in cod stomachs in the 1980s and 1990s
was much lower than in the 1950s and 1960s
(Ponomarenko and Yaragina 1979; Gjøsæter and
Bogstad 1998), a difference which cannot be
explained only by the difference in abundance of
young herring between those two periods (ICES
2006a). Additionally, the occurrence of cod canni-
balism declined strongly from the early 1960s to the
Cod
Capelin
Krill Amphipods
Herring
Harp seal
Minke whale
Figure 5 A simplified Barents Sea food web.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
8 No claim to original US government works
1970s (Ponomarenko et al. 1978; Yaragina et al.
2008), and the limited amount of Russian quanti-
tative stomach content data for the 1950s (Bogstad
et al. 1994) indicate that the level of cod cannibal-
ism was much higher in the 1950s than in the
1980s. These differences in the importance of
juvenile cod and herring as cod prey are partly
due to different size composition in the cod stock
(more larger, piscivorous cod in the 1950s and
1960s), but could also be due to changes in
geographical distribution of either predator or prey.
Quantitative stomach content data have been
collected by Norway and Russia since 1984, and a
joint Norwegian–Russian stomach content database
(Mehl and Yaragina 1992) has been established.
The annual consumption of various prey species by
cod was calculated based on diet composition,
amount of food eaten and a model for stomach
evacuation rate (Bogstad and Mehl 1997). An
updated time series for the period 1984–2006 is
given in ICES (2007). Figs 6–8 show the variation
in diet composition for cod aged 1–2, 3–6 and 7+
respectively. More details on the consumption by
the various age groups are given below.
The diet of cod aged 1 and 2 is dominated by krill
and amphipods (Themisto spp. Hyperiidae), northern
shrimp (Pandalus borealis Pandalidae) and capelin.
A more detailed study of the diet of cod aged 0–2
was carried out by Dalpadado and Bogstad (2004).
They found that the 0- and 1-group cod feed mainly
on crustaceans, with krill (Euphausiidae) and am-
phipods composing up to 70% of their diet. A shift in
the diet from crustaceans to fish was observed from
ages 1 to 2. The diet of a 2-year-old cod mainly
comprised capelin and other fish, and to a lesser
degree, krill and amphipods. Shrimp was also an
important prey in cod aged both 1 and 2.
Cod aged 3–6 prey mainly on capelin, but in
years of low capelin abundance, amphipods, krill,
shrimp and fish species other than capelin [cod,
Figure 6 Diet composition (proportion, by weight) for cod aged 1–2 in the Barents Sea 1984–2006 (adapted from ICES
2007).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 9
herring, Arctic or polar cod (Boreogadus saida
Gadidae), haddock, redfish (Sebastes spp. Scorpaeni-
dae) and in some years blue whiting (Micromesistius
poutassou Gadidae)] are also important. Cod aged 7+
generally prey on a variety of fish species, with
capelin as the main prey. The proportion of krill and
amphipods in the diet of 7+ cod in years with low
capelin abundance is much lower than in younger
cod. The percentage of fish prey in the diet is
generally proportional to the abundance of those
fish in the sea. This clear ontogenetic shift towards
piscivory is typical of cod (Pa
´lsson 1994). During its
spawning migration, mature Northeast Arctic cod
mainly feeds on adult herring and on Norway pout
(Michalsen et al. 2008).
Other abundant piscivorous fish species in the
Barents Sea are haddock, deep-sea redfish (Sebastes
mentella Scorpaenidae), Greenland halibut (Rein-
hardtius hippoglossoides Pleuronectidae), long rough
dab (Hippoglossoides platessoides Pleuronectidae) and
thorny skate (Raja radiate Rajidae). Bogstad et al.
(2000) found that while cod on average consumed
4.7 million tonnes of prey in the period 1990–1996,
the five other species mentioned consumed about
2.0 million tonnes of prey, assuming the same
consumption/biomass ratio for these species as for
cod. Of these 2.0 million tonnes, less than half is fish
prey. However, it should be kept in mind that the
biomass of deep-sea redfish and Greenland halibut
was much larger in the 1960–1970s than it is at
present (ICES 2007).
Individual growth and size at the age of Northeast
Arctic cod show strong variations (ICES 2007), and
growth has been shown to be positively related to
capelin abundance (Mehl and Sunnana
˚1991).
Variations in growth have a strong effect on
fecundity and atresia; skipped spawning has even
been observed in years with low condition factor
(Marshall et al. 1998). Both growth in length and
weight at length showed much less decline during
Figure 7 Diet composition (proportion, by weight) for cod aged 3–6 in the Barents Sea 1984–2006 (adapted from ICES
2007).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
10 No claim to original US government works
the second and third capelin collapses (mid-1990s
and early 2000s) than during the first collapse in
the late 1980s (Gjøsæter et al. 2008). The reason
for this difference may be that more, other fish prey
was available for cod in the mid-1990s, while in the
1980s, cod had to switch to less nutritious food
such as krill and amphipods. A tentative conclusion
is that cod may compensate for the absence of
capelin by feeding on other fish species if this is
possible.
Cod is also an important prey item for the two
most abundant marine mammal stocks: minke
whale (Balaenoptera acutorostrata Balaenopteridae)
and harp seal (Phoca groenlandica Phocidae) (Fig. 9).
Nilssen et al. (2000) calculated that harp seals in
the Barents Sea eat approximately 100 000 tonnes
of cod annually in years with high capelin abun-
dance, and 300 000 tonnes annually in years with
low capelin abundance. Folkow et al. (2000) found
that minke whales eat about 250 000 tonnes
annually. These calculations were based on abun-
dance estimates, stomach content data from the first
half of the 1990s and bioenergetics models. Except
for cod cannibalism, these two marine mammal
stocks are the most important predators of cod aged
1+, and the estimates of consumption of cod by
harp seal and minke whale are fairly close to the
estimates of biomass removed by a natural mortality
of 0.2 y
)1
(Bogstad et al. 2000).
Predictions of interspecies interactions from the
various multispecies models created for the Barents
Sea ecosystem sometimes produce contradictory
results. Schweder et al. (2000) found that capelin
catches decreased with increasing whale abun-
dance, while Bogstad et al. (1997) found that
capelin catches increased with increasing minke
whale abundance, due to strong indirect effects.
Hamre (2003) argues that a large cod stock may
reduce the average obtainable catch of all three fish
stocks, including cod, significantly. The models by
Bogstad et al. 1997 and Schweder et al. 2000 did
not test different levels of fishing mortality for cod,
but Hamre’s results differ from those obtained using
single species models for Northeast Arctic cod (e.g.
Nakken et al. 1996). There should be enough
contrast in the data to investigate to what extent
Figure 8 Diet composition (propor-
tion, by weight) for cod age 7 and
over in the Barents Sea 1984–2006
(adapted from ICES 2007).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 11
prey switching actually occurs. This is a key factor
in explaining differences of the modelled outcomes
and how the ecosystem may respond as cod
abundance changes.
Iceland
The fluctuations in stock size and catches of
Icelandic cod are described elsewhere (Schopka
1994), with cod the most abundant piscivore in
Icelandic waters. As with cod in many other areas,
cod in Icelandic waters is currently close to histor-
ical low levels (Table 1, ICES 2006b).
The main prey species for Icelandic cod is capelin
(Pa
´lsson 1983, 1994; Magnu´sson and Pa
´lsson
1989, 1991a), but shrimp is also an important
prey for cod (Pa
´lsson 1983, 1994; Magnu´sson and
Pa
´lsson 1989, 1991b). From the perspective of the
prey, cod is the main fish predator on capelin
(Pa
´lsson 1997), and Stefa
´nsson et al. (1998) found
a highly significant negative correlation (P< 0.01)
between juvenile cod abundance and each of three
different abundance indices for shrimp. This is quite
likely due to predation mortality on shrimp by cod.
Management of Icelandic cod and shrimp in a
multispecies context has been addressed (Stefa
´nsson
et al. 1994; Danı´elsson et al. 1997).
Cod growth is dependent on capelin abundance
in Icelandic waters (Steinarsson and Stefa
´nsson
1996). The ICES North Western Working Group
(NWWG) used capelin biomass and mean weight of
the year class in the previous year to predict weight
at age of cod during the period 1991–2003 (ICES
2004b). However, the relationship between capelin
biomass and mean weight increase of cohorts seems
to be much weaker in recent years, most likely due
to changes in the spatial distribution of capelin or
uncertainties in the estimation of capelin stock size.
(a)
(b)
Figure 9 Predation mortality (M2) on (a) age 1 and (b) 2 cod in the North Sea, the Baltic Sea and the Barents Sea (adapted
from ICES 2005b,c, 2007).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
12 No claim to original US government works
Also, predictions of capelin biomass were not
available to NWWG in 2004–2006. Thus, in recent
years, NWWG set the weight at age in the predic-
tions equal to the status quo (last year of observa-
tion; ICES 2006b). The share of capelin in the diet in
recent years has been reduced as has total con-
sumption and mean weight at age (H. Bjo¨rnsson,
MRI, Iceland, pers. comm.).
The approach used in 1991–2003 implies that
the process relating capelin biomass to cod weight
at age is more or less instantaneous. An alternative
analysis using growth rates shows that growth is
high during the years preceding the high capelin
biomass. This suggests that the factors and pro-
cesses causing high growth rates of cod and
eventually high weight at age are also causing the
biomass of capelin to increase. The two may thus be
indirectly rather than causally linked. The variabil-
ity in capelin stock size has been lower in Icelandic
waters than in the Barents Sea (Gjøsæter et al.
2002; Vilhja
´lmsson 2002). Cod is the main predator
on capelin in Icelandic waters, followed by minke,
humpback and fin whales (Vilhja
´lmsson 2002). The
annual consumption of capelin by cod may amount
to about 1.5 times the cod biomass.
Stomach content data for marine mammals in
Icelandic waters are scarce. Out of 68 minke whale
stomachs sampled, one was almost full of cod and
another contained cod or cod-like species together
with euphausiids (Sigurjo
´nsson et al. 2000). Codf-
ishes (Gadidae) were also an important prey item for
harp seals in coastal areas off Northern Iceland in
the period February to May (Hauksson and Bogason
1995). Thus, it is suspected that marine mammals
may be important predators of cod in this ecosys-
tem. Some multispecies models show that not only
may cetaceans have a considerable impact on future
yields from Icelandic cod (Stefa
´nsson et al. 1997a),
but seals may also have an even greater impact
(Stefa
´nsson et al. 1997b). The consensus is that
marine mammals likely influence the cod stock, but
to what degree remains to be validated.
Eastern Newfoundland–Labrador
The ‘northern’ cod stock off southern Labrador and
eastern Newfoundland crashed during the late
1980s and early 1990s and since the mid-1990s
has remained at about 2% of the level seen in the
early 1960s (Lilly et al. 2005; Table 1). Other
changes in the Newfoundland–Labrador ecosystem
included concurrent declines in most other demersal
fish, including species that were not targeted by
commercial fishing (Atkinson 1994; Gomes et al.
1995); a surge in snow crab (Chionoecetes opilio
Oregoniidae) and especially in northern shrimp
(Lilly et al. 2000); an increase in the abundance of
harp seals from fewer than 2 million individuals in
the early 1970s to more than 5 million in the late
1990s (Healey and Stenson 2000); and numerous
changes in the biology of capelin, the dominant
forage fish in the area (Carscadden et al. 2001). It
has been asserted that the collapses of cod
(Hutchings and Myers 1994; Myers et al. 1996)
and other demersal fish (Haedrich and Fischer
1996) were due entirely to fishing, but there is also
recognition that the cooler water temperatures of
the last three decades of the 20th century, and
especially of the early 1990s, may have contributed
substantially to the various changes observed in cod
(Parsons and Lear 2001; Drinkwater 2002) and
other components of the ecosystem (Narayanan
et al. 1995; Colbourne and Anderson 2003). It has
been difficult to isolate and quantify the relative
impacts of fishing, climate variability and species
interactions.
The upper trophic levels of this Arcto-boreal
ecosystem were historically dominated by three
species (capelin, cod and harp seals) that were
linked trophically (Lilly 1987; Hammill and Stenson
2000) and exploited commercially (Templeman
1966). The importance of capelin to cod was always
evident from the vast shoals of cod that migrated
into the traditional inshore fishing grounds in
pursuit of capelin that had approached the coast
to spawn (Akenhead et al. 1982). Food habits
studies supported the role of capelin as a major
prey, but also revealed a wide variety of additional
prey that changed gradually as cod grew and also
differed spatially, seasonally and annually (Lilly
1987, 1991). The major prey for small cod is
crustaceans, notably hyperiid amphipods in the
north and euphausiids on Grand Bank. For med-
ium-sized cod (30–70 cm), the major prey are
schooling planktivorous fish, the most important
of which is capelin, but Arctic (polar) cod are eaten
in the north, herring are consumed in inshore
waters, and sand lance (Ammodytes dubius Ammo-
dytidae) are important on Grand Bank. Larger cod
tend to feed on medium-sized fish and crabs,
especially toad crabs (Hyas spp. Oregoniidae) and
small snow crabs. Other notable prey species, such
as northern shrimp, bank clam (Cyrtodaria siliqua
Hiatellidae) or short-finned squid (Illex illecebrosus
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 13
Ommastrephidae), are moderately important only in
certain seasons or years depending upon their
relative abundance.
As in the Barents Sea and Icelandic waters,
capelin seems to be an important food item for cod.
A compilation of diet data for a study of biomass
flows (Bundy et al. 2000) concluded that capelin
comprised about 60% of the diet of large (>35 cm)
cod on an annual basis during the period 1985–
1987. The importance of capelin was further
emphasized by the observation that, over a series
of years, the quantity of capelin in the stomachs of
cod caught during the autumn off eastern New-
foundland increased with the abundance of capelin.
Additionally, during years of low capelin abun-
dance, the cod were not able to compensate fully by
feeding more intensively on other prey (Lilly 1991).
Earlier management-driven hypotheses explored
whether exploitation of capelin would result in a
reduction in the growth rate of cod or a decline in
the proportion of the cod migrating inshore (where
they would be accessible to the traditional inshore
fishery). The approach was not to construct explor-
atory, heuristic models but rather to conduct
empirical analyses to reveal relationships that could
then be built into predictive models (Shelton 1992).
Despite the expectation that linkages among species
would be strong in a system with few abundant
members, it proved difficult to find evidence of such
links. Only weak evidence could be found of a
positive relationship between capelin biomass and
success of the inshore cod fishery (Akenhead et al.
1982; Lear et al. 1986). Similarly, neither Aken-
head et al. (1982) nor Millar et al. (1990) found a
significant relationship between cod growth and
capelin biomass. It was felt by several authors
(Akenhead et al. 1982; Shelton et al. 1991) that
measurement error may be high, given the com-
plexities and limitations of quantifying fish abun-
dances and vital rates, and that the potential for
Type II error was high. Krohn et al. (1997) found,
however, that with the inclusion of data from the
early 1990s, capelin biomass explained some of the
variability in cod growth and condition.
The role of capelin in the collapse of cod during
the early 1990s remains unclear. Estimates of
capelin biomass from offshore hydroacoustic sur-
veys declined dramatically from 1991 onward, and
the capelin changed their autumn distribution
towards the southeast (Carscadden and Nakashima
1997). It has been suggested that these changes,
together with changes in the timing of capelin
migrations, made the capelin less accessible to cod,
thereby contributing to low condition and possibly
an increase in the mortality of the cod (Atkinson
and Bennett 1994; Lilly 2001). However, cod
distribution also changed during the early 1990s,
such that most of the cod remaining during the
latter stages of the collapse seemed to have undi-
minished access to capelin, at least in the offshore
during the autumn (Lilly 1994; Taggart et al. 1994;
O’Driscoll et al. 2000). It has been hypothesized that
the change in cod distribution came about from a
southward redistribution of fish (Atkinson et al.
1997; Rose et al. 2000), not spatial differences in
mortality (Hutchings 1996). Rose et al. (2000)
further hypothesized that the redistribution of the
cod was a response to the redistribution of capelin,
and Atkinson et al. (1997) and Rose et al. (2000)
hypothesized that the change in distribution of the
cod resulted in the cod becoming more accessible to
trawlers, thereby contributing to the cod collapse.
However, dramatic changes in distribution of cap-
elin and cod did not occur during a cold period in
the mid-1980s (Lilly 1994; Atkinson et al. 1997).
There remains uncertainty regarding the extent to
which the low water temperatures and extensive ice
cover of the early 1990s contributed to changes in
the abundance and distribution of capelin, the
distribution of cod, the feeding success of the cod,
and the mortality of cod from natural causes and
fishing (Lilly et al. 2005 and references therein).
The predators of cod tend to change as the cod
grow (Lilly 1987; Pa
´lsson 1994; Bundy et al. 2000).
Very small cod are eaten by squid, various demersal
fish (such as sculpins) and some seabirds. Larger
juveniles have many predators: demersal fish, most
notably larger conspecifics and Greenland halibut;
harp seals and hooded seals (Cystophora cristata
Phocidae); certain toothed whales, such as harbour
porpoise and pilot whales (Globicephala melaena
Delphinidae); and probably minke whales. Large
cod seem to have few natural predators, but seals can
prey upon them by belly-feeding, a mode of predation
whereby the seal takes a bite from the cod’s abdomen,
consuming the liver and some of the other abdominal
organs, but generally leaving the rest of the carcass
and the head (Lilly et al. 1999).
The predator that has attracted most attention is
the harp seal (Bundy et al. 2000; Hammill and
Stenson 2000). There was speculation that seals
contributed to the collapse of the cod stock (Atkin-
son and Bennett 1994), but it is generally thought
that their contribution was small. However, the
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
14 No claim to original US government works
total mortality of cod in the offshore has remained
very high since the moratorium on directed fishing
in 1992, and analyses of tagging data have revealed
that adult cod in the inshore experienced high
mortality in addition to that caused by the reopened
fishery in 1998–2002 (Lilly et al. 2005). It is
possible that the seals could be maintaining cod in
a ‘predator pit’ (Shelton and Healey 1999). It has
been concluded by some authors (DFO 2003; Rice
et al. 2003), based on the large size of the harp seal
population, the known predation by harp seals on
cod and the paucity of information pointing to other
factors, that predation by harp seals is a contribut-
ing factor to the high mortality of cod. It must be
emphasized, however, that there is very little
information on harp seal diet in the offshore, where
most of the seal foraging is thought to occur. The
little information available for hooded seals indi-
cates that they too could be important predators on
cod (McLaren et al. 2001).
The role of cod within an ecosystem may become
more apparent when cod biomass declines, as
happened off Labrador and eastern Newfoundland.
The surge in snow crab and particularly northern
shrimp is consistent with a release from predation
pressure from cod (Lilly et al. 2000; Bundy 2001;
Worm and Myers 2003) and other demersal fish,
but it is difficult to separate the influence of predator
release from the effects of environmental change. It
has been postulated that the increase in both snow
crab and northern shrimp was related to improved
recruitment associated with the cold water during
the 1980s and 1990s (Parsons and Colbourne
2000). It may also be noted that there is no
evidence that capelin or any other finfish increased
following the cod collapse.
The degree to which competition with other
species has influenced the dynamics of cod is
difficult to determine. It has been suggested
(Anderson and Rose 2001) that Arctic cod might
be a competitor of pelagic juvenile cod, and may
have had a larger impact during the cold years of
the early 1990s when Arctic cod expanded its
distribution southward (Lilly et al. 1994). Most
concerns regarding competition are focused on the
harp seal, which is estimated to have consumed
about 3 million tonnes of food per year in the
northern cod stock area during the late 1990s
(Hammill and Stenson 2000; Stenson and Perry
2001). Most of this food was pelagic planktivores,
notably capelin, so the potential for competition
with cod exists. However, cod and seals share
capelin and other planktivores (Arctic cod, sand
lance, herring) with numerous additional preda-
tors, including other demersal fish, several species
of baleen whales and birds (Bundy et al. 2000;
Carscadden et al. 2001).
Gulf of Maine–Georges Bank
As at many other places around the globe, cod in
the Gulf of Maine–Georges Bank ecosystem are no
longer one of the biomass dominants of the fish
community, only comprising around 5–10% of the
total fish biomass in the ecosystem (Table 1;
Serchuk et al. 1994). Despite this, the species
remains a key component of regional fishery land-
ings and is still an ecologically important organism.
The history of the US northwest Atlantic cod fishery
and subsequent changes in the fish community are
well documented (Serchuk and Wigley 1992; Ser-
chuk et al. 1994; Murawski et al. 1997; Fogarty
and Murawski 1998), with cod currently around
25–30% of historical levels.Fish biomass is now
dominated by elasmobranch and pelagic species in
the ecosystem. Although there has been some sign
of recovery in other groundfish stocks, cod stocks
have remained at low levels.
The diet of cod has also been well documented for
this part of the Atlantic, namely describing the
generalist feeding nature of this species (Langton
and Bowman 1980; Langton 1982; Bowman and
Michaels 1984; Vinogradov 1984; Link and
Almeida 2000; Link and Garrison 2002a). These
studies have shown that cod typically eat the same
main types of food across the Gulf of Maine and
Georges Bank, despite local changes in habitat.
Usually, the diet represents local, ambient benthos
augmented by seasonal migrations of small pelagic
forage fish (i.e. Atlantic herring, Atlantic mackerel).
Link and Garrison (2002a) showed a notable
change in the diet composition across the past three
decades, principally reflecting changes in the rela-
tive abundance of the prey field (Fig. 10). As herring
and mackerel declined in this ecosystem during the
1970s, sand lance (Ammodytes spp. Ammodytidae)
replaced those small pelagics as the dominant
component in the diet (Fogarty et al. 1991). As
herring and mackerel began to recover in the late
1980s, those two species again comprised a signif-
icant portion of the diet. The ontogenetic shift in the
diet observed in this ecosystem confirms the com-
mon change from benthivory to piscivory as cod
grow (Link and Garrison 2002a).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 15
Several studies have examined the relationship
among cod consumption, diet and feeding to cod
growth, recruitment and reproduction (Mayo et al.
1998; O’Brien 1999; O’Brien and Munroe 2000;
NEFSC (Northeast Fisheries Science Center), unpub-
lished data). No detectable changes attributable to
diet-related considerations have been observed in
growth rates, density dependence or stock–recruit-
ment relationships. Most of the effects on the cod
stocks have been attributed to overfishing (Serchuk
and Wigley 1992; Serchuk et al. 1994; Murawski
et al. 1997).
The prominence of cod in this ecosystem has
diminished. Link and Garrison (2002b) show that
the amount of energy flowing through the cod
population has declined notably, with cod consum-
ing about one-third of what the population once did
on Georges Bank (Fig. 11). Cod used to be the
dominant piscivore in the ecosystem, but that is no
longer true. Other gadoids (i.e. hakes) and a suite of
elasmobranchs consume a much higher amount of
fish than cod. Essentially, there are less cod and the
cod that are present are smaller than historically
speaking. The sum result of this stock (in abundance
and size) is that cod eat less than before. However,
cod are still one of the top 10 fish predators in the
ecosystem.
Some populations of cod predators have increased
over the past four to six decades, whereas most have
steadily declined. Species such as sharks, Atlantic
halibut (Hippoglossus hippoglossus Pleuronectidae),
large hakes and larger cod are much less abundant
generally and in this ecosystem than they were 40+
years ago (NEFSC 1998). Whether the observed
decline in cod stocks caused declines in the popula-
tions of cod predators is unknown, but not strongly
suspected. Other cod predators, such as goosefish
(Lophius americanus Lophiidae) or sea raven (Hemi-
tripterus americanus Cottidae), have increased, but
generally do not consume large amount of biomass
and cod do not comprise a large portion of their diet.
Conversely, whether the increases in some other cod
predators have resulted in cod populations being
stuck in a ‘predator pit’, ultimately hindering stock
recovery, is unknown. There was some suspicion that
highly abundant elasmobranchs such as spiny dog-
fish (Squalus acanthias Squalidae) or winter skate
(Raja ocellata Rajidae) significantly prey upon cod, but
this has been disproven (Tsou and Collie 2001a,b;
Link et al. 2002). However, the role of small pelagic
(a)
(b)
Figure 10 Percentage diet composition (by weight) of cod at Georges Bank, Gulf of Maine ecosystem, 1973–1998: (a) for
1973–1985 and (b) for 1986–1998 (adapted from Link and Garrison 2002a).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
16 No claim to original US government works
fish feeding upon larval stage cod remains a key issue,
with the magnitude of this process potentially signif-
icant but currently unresolved (Garrison et al. 2000,
2002).
Multispecies models (Tsou and Collie 2001a,b;
Link and Garrison 2002b; Link 2003) suggest that,
like elsewhere, the earliest life-history stages expe-
rience the most predation mortality. How predation
mortality of these early life stages has impacted on
cod recruitment is unclear, but is suspected to be
secondary to recruitment overfishing. Link (1999,
2002) had shown how complex the food web of this
ecosystem can be, and ultimately questioned how
feasible it might be to predict specific effects of
species interactions beyond a general, aggregate
biomass level (Link 2003).
There is a suite of potential cod competitors
(Garrison and Link 2000a,b; Link et al. 2002).
However, competition is generally difficult to quan-
tify in the field. There are four requirements that
must be fulfilled to demonstrate competition: spa-
tiotemporal overlap, similarity of resource utiliza-
tion (i.e. diet), limiting resources and notable
population impacts of the interaction. Given these
difficulties and assumptions for demonstrating com-
petition, the first two items can be shown, but
Georges Bank is a highly productive ecosystem
(Cohen et al. 1982; Sissenwine et al. 1984), sug-
gesting that resources may not be limiting. It is also
unclear whether opposite directions of population
trajectories among cod and potential competitors
are causal or just inversely correlated in this system.
Arguably, some of the bigger competitors of cod in
this ecosystem are the fisheries for small pelagics,
shrimp and decapods (Worm and Myers 2003). Yet,
there is limited evidence that cod could not switch
to alternate prey and are in fact resource limited.
Thus although the concept merits further investi-
gation, the evidence to date suggests that it is
unlikely that competition is currently limiting cod
stocks in this ecosystem.
Generalities, comparisons and synthesis
Basic cod feeding ecology
The cod ecosystem overviews above and various
reviews of cod feeding habits (ICES 1992; Pa
´lsson
(a) (b)
(c) (d)
Figure 11 Cod abundance and diet at Georges Bank, Gulf of Maine ecosystem. (a) Minimum swept area abundance of
different size classes of cod across the time series; (b) mean proportion of fish (% weight) in the diet of cod; (c) total amount
of food consumed by cod and (d) total amount of fish consumed by cod (adapted from Link and Garrison 2002b).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 17
1994; Methven 1999) reveal that cod have a broad
diet consisting mainly of crustaceans and teleost
fish. It has been demonstrated repeatedly that the
diet of cod shifts ontogenetically. Small cod tend to
feed on small crustaceans, such as mysids, eup-
hausiids, amphipods and small shrimp. Medium-
sized cod feed on larger crustaceans and small fish,
especially planktivorous fish that are sometimes
referred to as ‘forage fish’ (capelin, sand lance,
herring, Arctic cod and other juvenile gadoids such
as hakes). Large cod feed on crabs and medium-sized
demersal and forage fish. Forage fish may be
replaced or supplemented by squid or the juveniles
of larger fish. Other taxa found in the diet include
ctenophores, cnidarians, polychaetes, gastropods,
bivalves and echinoderms, but these are seldom
found in large quantities and perhaps, particularly
in the case of ctenophores and brittle stars, indicate
poor feeding conditions. Differences in biotic com-
munities across ecosystems and the subgeographies
within ecosystems, and across seasons within those
ecosystems, alter the realized local prey field, but the
general pattern described here is consistent for cod
wherever cod feeding habits have been described.
The gradual change in diet with increasing
predator size is considered to be a consequence of
energetic advantage associated with the obtaining
of large prey items, constrained by the cost of
acquiring the prey and a morphological limitation
on maximum prey size (Kerr 1971; Scharf et al.
2000). This increasing prey size involves not only a
change in taxa but also an increase in individual
size within a taxon (Pa
´lsson 1983; Lilly 1984;
Scharf et al. 2000). Despite this tendency for
increasing prey size, even the largest cod eat a wide
size range of prey, and never entirely stop eating
large zooplankton, shrimp and benthic inverte-
brates. Indeed, individual large cod may be found
with several thousands of euphausiids in their
stomachs (Lilly 1987; Scharf et al. 2000).
Do differences in diet translate into broad impacts
on cod populations? One area where diet quality can
be critical is seen in the interaction between cod and
forage fish. Forage fish are clearly very important to
the northern stocks (c.f. Newfoundland, Barents
Sea, Iceland examples). Climate effects on forage fish
are suspected or known in these locales; e.g.
concern about changed migration patterns for
capelin north of Iceland and in the Barents Sea
due to environmental variability (Gjøsæter 1998;
Vilhja
´lmsson 2002). In the more southerly stocks,
this may not be as strong a consideration, but is an
obvious climate-related change to the prey field that
could have significant effects on cod populations.
Further evidence of diet impacts on cod popula-
tions is unclear. Some studies indicate that a more
‘balanced’ diet, specific diet components or simply a
greater availability of food increase cod growth
(Brown et al. 1989; Mehl and Sunnana
˚1991;
Jobling et al. 1994; Clark et al. 1995; Krohn et al.
1997; Lambert and Dutil 1997; Dutil and Lambert
2000; Rose and O’Driscoll 2002; Mello and Rose
2005). Other investigators indicate that spawning
ceases or is curtailed if inadequate food is present
(Kjesbu 1994; Burton et al. 1997; Lambert and
Dutil 2000). Lambert and Dutil (1997) and Swain
(1999) suggested that, combined with overfishing,
changes in cod diet are responsible for declines in
cod stocks and distribution shifts. However, the
growth and mean size of cod in the Georges Bank–
Gulf of Maine ecosystem have remained relatively
constant across time despite large changes to the
abundance of those stocks (Mayo et al. 1998;
O’Brien 1999; O’Brien and Munroe 2000).
Conversely, many studies have related how
much, but not what, cod eat relative to the
reproductive state, recruitment and growth of cod.
Yaragina and Marshall (2000) found the liver
condition index of Northeast Arctic cod to be
positively correlated with the frequency of occur-
rence of capelin in cod stomachs. The total lipid
energy for mature females in the stock is propor-
tional to the total egg production (Marshall et al.
1999). Link and Burnett (2001) show that the
amount of food eaten by cod is related to the
maturity state, with food consumption greater post-
spawning to recover depleted energy reserves. Cod
growth has been shown to be dependent on capelin
abundance in both Icelandic waters (Steinarsson
and Stefa
´nsson 1996) and the Barents Sea (Mehl
and Sunnana
˚1991) and on the total amount of
prey in the Baltic Sea (Gislason 1999). Additionally,
basic bioenergetic considerations can affect cod
growth, recruitment, reproductive success and
physiology (Jobling et al. 1994; Krohn et al. 1997;
Lambert and Dutil 1997, 2000; Brander 2000;
Dutil and Lambert 2000; Dutil et al. 2003).
Cannibalism
Bogstad et al. (1994) compared cod cannibalism in
the Barents Sea, Icelandic waters and the New-
foundland area. They found that the proportion of
cod in cod diet increases with cod size. On average,
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
18 No claim to original US government works
the proportion was <1% for cod <50 cm, and
increased to 5–9% in cod >100 cm. The maximum
prey size was about 50% of the predator length, and
the range of prey size increased with predator size.
For all these areas, cod stomachs have been sampled
annually, and the year-to-year variability in the
frequency of occurrence of cod in cod stomachs was
found to be large. Uzars and Plikshs (2000) and
Neuenfeldt and Ko¨ster (2000) found similar results
for Baltic cod, but predation on cod aged 2 and older
(>15 cm) seem to be less frequent than in the other
areas.
For the North Sea and the Baltic, predation
mortality (M2) has been calculated using MSVPA
(ICES 2003a,d, 2005a–c). Estimates of cannibalism
mortality are also provided for Northeast Arctic cod
by the Arctic Fisheries Working Group (ICES 2007).
Fig. 9 shows the predation mortality (M2) for cod
aged 1 and 2 for these areas. The M2 values were
highest for Northeast Arctic cod and lowest for
Baltic cod. For the Barents Sea and the Baltic Sea,
M2 is only due to cannibalism. For the North Sea,
cannibalism accounts for 50–70% of the predation
on cod aged 1 and about 90% of the predation on
cod aged 2. Link and Garrison (2002a,b) noted that
cannibalism is a less important factor currently
than it may have been historically for Georges Bank,
but with cod still comprising a small but notable
2–5% of the diet of cod. Similar values have been
observed for other ecosystems (ICES 1992; Pa
´lsson
1994; Methven 1999). It is likely that the conver-
gence of spatiotemporal overlap among juveniles
and adults, coupled with the extent of alternate
prey, influence the degree of cannibalism by cod.
Cod prey and other fisheries
What are the impacts of cod feeding on the rest of
the food web? To answer these questions, one must
understand at a basal level the amount of food eaten
by cod. By scaling individual consumption of cod to
population levels, total removals of prey can be
estimated (Sparre 1991; Sparholt 1994; Bogstad
and Mehl 1997; Link and Garrison 2002b). Rem-
ovals relative to prey population sizes can then
provide an assessment of the mortality induced by
cod. Thus, what are the implications of changing
cod stock size for prey populations of cod? In some
instances, cod appear to regulate prey populations.
The more simple ecosystems (Iceland, Barents,
Newfoundland–Labrador, Baltic) tend to have fewer
species but stronger species interactions and, in
those cases, alterations to cod stocks are cascaded to
their prey. This is seen as a prey population expands
(if cod abundance declines) or declines (if cod
abundance increases, but only to a point; e.g. Baltic
sprat versus cod). Conversely, in some ecosystems
this is not seen at all. Fewer instances in the more
complex North Sea and Georges Bank-Gulf of Maine
ecosystems show a change in cod prey populations
related to a change in cod abundance (e.g. Nephrops
in the North Sea).
Because of the broad and omnivorous nature of
cod feeding, it is likely more feasible to list those
benthivorous and piscivorous fish species or marine
mammals from the same ecosystem that are not
potential competitors of cod. Some researchers have
shown that the dietary overlap (a unitless propor-
tion ranging from 0 to 1) among cod and other
species generally ranges from 0.2 to 0.7 for the
entire fish community (Garrison and Link 2000a,b).
Yet in most instances, competition is indeterminate
and suspected to be a minor element affecting cod
competitors and cod.
As the predatory role of cod changes in the
ecosystem, there are major implications for fisheries
management. For instance, the abundance and
fisheries landings for some forage fish have had an
inverse relationship to cod stocks (e.g. Baltic sprat).
But arguably the major observation is that of the
interaction between cod and major crustacean prey
(Bogstad et al. 2000; Lilly et al. 2000; Bundy 2001;
Worm and Myers 2003; Parsons 2005). Cod
predation is a larger source of shrimp mortality
than fishing in the Barents Sea and Icelandic waters
(Magnu´ sson and Pa
´lsson 1991b; Bogstad et al.
2000). In the Newfoundland–Labrador area, where
there was a collapse in cod and a surge in shrimp,
cod took far more shrimp than the fishery during
most of the 1980s, but by the late 1990s, the fishery
for shrimp far exceeded removals by cod (Lilly et al.
2000). An inverse relationship between cod bio-
mass and shrimp (particularly Pandalidae) abun-
dance has been found (Stefa
´nsson et al. 1998; Lilly
et al. 2000; Worm and Myers 2003). The Nephrops
fishery in the North Sea and the Irish Sea (Brander
1988; Brander and Bennett 1989) has also shown
an inverse relationship to cod stock size. In many
instances, the decline in cod has had a markedly
positive impact on shrimp, crab and lobster fisheries.
However, Hanson and Lanteigne (2000) indicate
that cod was not an important source of natural
mortality for American lobster, and there is simi-
larly limited evidence in the Georges Bank–Gulf of
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 19
Maine ecosystem (Link and Garrison 2002a; Worm
and Myers 2003).
It is highly conceivable that several fisheries
could be competing with cod, particularly for small
pelagic fishes and economically valuable inverte-
brates (Jakobsson and Stefa
´nsson 1998), as in the
case of the Nephrops fishery in the North Sea and the
Irish Sea (Brander 1988; Brander and Bennett
1989). In the latter case, a mixed fishery model was
used to estimate the joint yield for cod and Nephrops,
and European Union fisheries management policy
was altered to allow cod biomass to be reduced in
order to benefit the Nephrops stock. In instances
where the relationship is strongly suspected, a
precautionary approach should be adopted to
include this possibility.
Cultivator effects
A wide range of organisms preys on eggs and larvae
of cod (Pa
´lsson 1994). Here we focus on trophic
loops, wherein cod prey on forage species but these
forage species may, in turn, depress the recruitment
of cod by preying on the cod’s early life stages (eggs,
larvae or early juveniles) or by competing with
those early life stages for food. In the Baltic Sea, for
example, herring and especially sprat prey on cod
eggs (Ko¨ster and Mo¨ llmann 2000), and it is thought
that the system alternates between two semi-stable
states, one dominated by sprat and the other by cod
(Ko¨ster et al. 2003). Similarly, there is evidence
from the North Sea (Daan et al. 1994) and the
southern Gulf of St Lawrence (Swain and Sinclair
2000) that recruitment of cod is more successful
when the biomass of planktivorous pelagic fishes is
low. The evidence is unknown or unclear for the
other ecosystems we examined (Table 1).
The existence of such ‘cultivation’ effects (Walters
and Kitchell 2001) is also less clear in the case of
juveniles. The presence of trophic loops (Rice 1995),
with cod preying on the adults or juveniles of
another species and the larger individuals of that
other species preying on juvenile cod, has often been
reported. For example, cod off eastern Newfound-
land and in the Gulf of St Lawrence prey on short-
finned squid (Lilly and Osborne 1984), and squid
feed on juvenile cod (Dawe et al. 1997). Cod prey on
juvenile Greenland halibut (Lilly 1991) and Green-
land halibut feed on juvenile cod (Bowering and
Lilly 1992; Hovde et al. 2002). Despite the existence
of such trophic loops, we are not aware of examples
where a cod decline has been followed by an
increase in another piscivore, which has then
depressed the recruitment of cod.
Cod and marine mammals
The abundance of fish that might prey on cod
juveniles has declined throughout most of the north
Atlantic during the past few decades (Pauly et al.
1998; Christensen et al. 2003). This does not
necessarily mean that the whole predator field has
declined. The populations of some marine mam-
mals, such as Northwest Atlantic harp seals (Healey
and Stenson 2000) and Scotian Shelf grey seals
(Bowen et al. 2003), have increased dramatically
during recent decades as they have rebounded
under less-intensive harvesting or culling. These
and other mammals, such as minke whales, have
not been adversely affected by the declines in cod
populations, because cod is generally a small
portion of their diet and they are sustained by other
prey, most notably forage fish (Folkow et al. 2000;
Hammill and Stenson 2000; Nilssen et al. 2000).
The mortality rate of juvenile cod in some of these
areas is very high (Fu et al. 2001; Lilly et al. 2005).
Depensation in the form of a ‘predator pit’ is possible
(Shelton and Healey 1999), but seal diet data are
generally insufficient to address the question ade-
quately. Cod is, however, a more important prey for
Barents Sea minke whales than for other marine
mammal stocks (Folkow et al. 2000), although it
seems to be less preferred as a prey species than
herring and capelin (Haug et al. 1996; Skaug et al.
1997). Mammal predation on cod is also suspected
to be high in Icelandic waters and other parts of the
Barents Sea. However, this appears to be less of a
factor in the other ecosystems we examined
(Table 1). Nevertheless, there is evidence from
various sources that the natural mortality of adult
cod is unusually high in the northern Gulf of
St Lawrence (Benoıˆt and Chouinard 2004), the
southern Gulf of St Lawrence (Chouinard et al.
2003), the eastern Scotian shelf (Fu et al. 2001) and
inshore waters of eastern Newfoundland (Lilly et al.
2005). It has been concluded by some (Rice et al.
2003) that predation by seals has contributed to the
high cod mortality and to the lack of recovery in
these cod stocks.
When a cod stock is healthy, predation by marine
mammals is but one of many sources of mortality to
which the stock has become adapted. However,
when a cod stock has been depleted by fishing,
perhaps exacerbated by adverse environmental
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
20 No claim to original US government works
conditions as hypothesized off eastern Canada (Dutil
and Lambert 2000; Drinkwater 2002), rejuvenated
populations of marine mammals have the potential
to impede attempts to promote cod recovery. Such
circumstances have led to calls for the deliberate
reduction of mammal numbers. This inevitably
raises questions about the ability of science to
provide reliable information regarding the efficacy of
such reductions (Yodzis 2001), the ability of
humans to steer ecosystems into specific configura-
tions, and the legal and ethical implications of
attempting to do so (Molenaar 2002, 2003). Clearly
this is an area that merits continued attention.
Most predators of cod do not exhibit a large
dependence upon cod as prey. Rarely does the
frequency of occurrence and per cent diet compo-
sition exceed 10–15% for cod as prey. Yet there are
some exceptions. Scaling the amount of cod
removed by predators demonstrates that, in some
ecosystems, predation on cod can be a significant
source of mortality, whereas in other locales, it is
minor relative to other influences on cod stocks.
Again, in simpler ecosystems with stronger species
interactions, the potential for there to be significant
‘predator pits’ is likely higher than in more complex,
more diffuse species interacting ecosystems.
Climate change
As noted above, the abundance of cod and its prey
and predators have been affected not only by
fisheries but by environmental variation. Of great
interest is the potential impact of the global atmo-
spheric warming that is currently occurring and is
projected to continue (IPCC 2001, 2007). In the
area of the North Atlantic, the intensity of warming
is projected to vary geographically, with the greatest
warming in the Arctic and Subarctic and possibly
little or no warming in certain areas, such as the
Labrador Sea.
Predictions regarding the extent to which this
atmospheric warming will affect cod and interacting
species require a downscaling from Global Circula-
tion Models to regional physical oceanography, a
process that is not yet well advanced for many areas
where cod is found (Vilhja
´lmsson et al. 2005).
Nevertheless, Drinkwater (2005) predicted future
changes in the abundance and distribution of
various cod stocks by coupling projections of tem-
perature increase in shelf waters occupied by those
stocks (IPCC 2001, 2007) with observed responses
of cod to past temperature variability. He found that
cod will likely spread northwards along the coasts of
Greenland and Labrador and occupy larger areas of
the Barents Sea, whereas stocks in the southern
range will decline (southern North Sea and Georges
Bank) or even disappear (Celtic and Irish Seas). As
noted by Vilhja
´lmsson et al. (2005), such predic-
tions must be tempered by knowledge that the
abundances of some cod stocks and the species with
which they interact are now so altered from historic
levels that cod populations may not respond to
climate variability as they did in the past. Additional
uncertainty arises from fisheries-induced evolution-
ary changes in life-history traits (Jørgensen et al.
2007), which might alter the manner in which
species respond to environmental change.
The role of cod in the ecosystems of the future will
depend not only on the abundance and distribution
of cod, but also on the abundance and distribution
of their prey and predators. It is possible that some
ecosystems will migrate northward but remain
similar to their present state. However, it is more
likely that the various species within each ecosys-
tem will respond differently to climate change (Rose
2005). Thus, predicting the role of cod under
scenarios of climate change requires that one
should consider the impact of climate change on
abundance and distribution of each of the major
interacting species and the extent of overlaps among
them. We discuss just a few examples to illustrate
the types of changes that investigators might be
obliged to consider.
If climate change favours some prey species over
others, then the prey field available to cod may
become less favourable for cod condition. For
example, in the East Newfoundland–Labrador area,
the decline in capelin and the rise in northern
shrimp may have been related, at least in part, to
climate variability during the early 1990s. This
change in prey availability has been hypothesized to
have caused a reduction in cod condition, which, in
turn, has contributed to the observed increase in the
mortality of the cod (Rose and O’Driscoll 2002).
The impact of cod as a predator may change as a
consequence of climate change. If cod becomes
prominent in northern areas in which it is currently
absent or in low abundance, then the potential prey
species that are currently there may experience
increased mortality. If an increase in temperature
promotes population growth in those cold-water cod
stocks that are now at low abundance, such as
those on the Eastern Scotian Shelf and off Eastern
Newfoundland–Labrador and West Greenland, then
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 21
those species that are thought to have increased as
a result of predator release, such as sand lance on
the Eastern Scotian Shelf and northern shrimp off
Eastern Newfoundland–Labrador, might experience
a decline. Conversely, if warming promotes a decline
in cod stocks towards the southern end of the
present cod distribution, then some prey stocks in
those areas might increase. However, the relative
importance of cod in the southern areas is already
less than in the northern areas.
The consequences to cod as a prey taxa may also
change as climate change affects the abundance
and distribution of its predators. Of particular
interest is the impact that reductions in sea ice
might have on populations of seals that pup on ice
(e.g. harp and hooded seals, and grey seals in some
areas). Reductions in the extent or duration of sea
ice might cause declines in seal populations, which,
in turn, might promote increases in cod popula-
tions, particularly those highly depressed cod stocks
that some hypothesize may be held in a predator pit
by marine mammals and other predators.
Summary
The dominant factor in the dynamics of most cod
stocks, at least during the most recent two to three
decades, has been fishing (Table 2; Lilly et al. 2008).
One way to compare the relative importance of
several extrinsic factors on population dynamics is
to investigate how much of the variation of a given
population abundance or biomass can be explained
by each of the factors. The results in Table 2, based
on analyses of data from the Baltic, North and
Barents Seas, show that the main impact on both
SSB and recruitment was from fishing (ICES 2003c).
Fishing accounted for 21–52% of the variance (ICES
2003c). For the period included within the study,
climate and predation accounted for a smaller part
of the variation. Several studies have shown that
most cod stocks have a history of overfishing and
are currently depressed or in the recovery stage
(Schopka 1994; Fogarty and Murawski 1998;
O’Brien and Munroe 2000; Hylen 2002; ICES
2003c; Lilly et al. 2008). This means that the
abundance of cod is generally lower now and will
likely continue to be for the near future. With excess
fishing, the average size of cod will continue to be
small. Additionally, as abundance is generally low,
the distribution and range of these stocks are
reduced. Thus, due to the direct effects of fishing
on cod, it appears that the ecological role of cod is
diminished relative to historical roles in many cod
ecosystems. What remains unclear is how addi-
tional climate variability will alter cod stocks, and
thus the role of cod in the ecosystem.
Additionally, cod recruitment by temperature for
a set of cod stocks (Fig. 12) shows that, below 1 °C
and above 10 °C, recruitment is very low and dome-
shaped in between. The implication is that as the
climate changes, particularly if global warming
occurs as predicted (Turrell et al. 2003; Drinkwater
2005; IPCC 2007), then recruitment for cod is likely
to diminish for stocks living at the upper tempera-
ture range and may increase for the stocks living at
Table 2 Ratio of spawning stock biomass and growth and
recruitment variance explained by the extrinsic factors:
fishing, predation and climate.
Population Factor SSB Recruitment
North Sea cod Fishing ()) 0.52 ()) 0.26
Predation ()) 0.12 ()) 0.16
Climate ()) 0.18
Baltic Sea cod Fishing ()) 0.21 ()) 0.43
Barents Sea cod Fishing ()) 0.25 ()) 0.33
Predation 0 0
Climate (+) 0.18
()) means a negative effect of the factor on the population and
(+) means a positive effect. Adapted from ICES (2003c).
SSB, spawning stock biomass.
Figure 12 The relationship between recruitment and
surface water temperature for different cod stocks (adapted
from Brander (2000).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
22 No claim to original US government works
the lower temperature range. Additionally, if the
North Atlantic continues to warm, the range of cod
will likely move northward, making cod a rarer
organism in those ecosystems where it is already at
the southern extreme of its range. Thus, it appears
that the ecological role of cod will likely change in
ecosystems in the southern and northern ranges of
the present cod distribution due to climate changes.
Clearly, the magnitude or effects of the ecological
role played by cod in these ecosystems is tightly
coupled to their abundance. It is probable that based
on densities alone, the declined cod stocks in all of
these ecosystems have a much smaller role than
they did in historical times. Conversely, any recov-
eries of cod imply an increased role of cod in an
ecosystem. Beyond that, the specific impacts of any
changes due to climate variability might remain
difficult to predict.
Acknowledgements
Thanks to two anonymous referees and to the editor
for their valuable comments. We would also like to
thank Jaime Alvarez, Institute of Marine Research,
Bergen, for preparing Fig. 5, and Brian Smith of the
NEFSC for assistance in checking the references.
References
ACIA (Arctic Climate Impact Assessment). (2005) Arctic
Climate Impact Assessment. Cambridge University Press,
Cambridge, UK, 1042 pp.
Akenhead, S.A., Carscadden, J., Lear, H., Lilly, G.R. and
Wells, R. (1982) Cod–capelin interactions off northeast
Newfoundland and Labrador. In: Multispecies Approaches
to Fisheries Management Advice (ed. M.C. Mercer), Cana-
dian Special Publication in Fisheries and Aquatic Science 59,
141–148.
Andersen, K.P. and Ursin, E. (1977) A multispecies
extension to the Beverton and Holt theory of fishing,
with accounts of phosphorous circulation and primary
production. Meddelelser fra Danmarks Fiskeri - og
Havundersøgelser Ny Serie 7, 319–435.
Anderson, J.T. and Rose, G.A. (2001) Offshore spawning
and year-class strength of northern cod (2J3KL) during
the fishing moratorium, 1994–1996. Canadian Journal of
Fisheries and Aquatic Sciences 58, 1386–1394.
Atkinson, D.B. (1994) Some observations on the biomass
and abundance of fish captured during stratified-random
bottom trawl surveys in NAFO Divisions 2J and 3KL,
autumn 1981–1991. NAFO Science Council Studies 21,
43–66.
Atkinson, D.B. and Bennett, B. (1994) Proceedings of a
northern cod workshop held in St. John’s, Newfound-
land, Canada, January 27–29, 1993. Canadian Technical
Report of Fisheries and Aquatic Sciences No. 1999, 64 pp.
Atkinson, D.B., Rose, G.A., Murphy, E.F. and Bishop, C.A.
(1997) Distribution changes and abundance of northern
cod (Gadus morhua), 1981–1993. Canadian Journal of
Fisheries and Aquatic Sciences 54(Suppl. 1), 132–138.
Beaugrand, G., Brander, K., Lindley, J.A., Souissi, S. and
Reid, P.C. (2003) Plankton effect on cod recruitment in
the North Sea. Nature 426, 661–664.
Benoıˆt, H.P. and Chouinard, G.A. (2004) Mortality of
northern Gulf of St. Lawrence cod during the period from
1990 to 2003. DFO Can Sci Adv Sec Res Doc 2004/042.
Bogstad, B. and Gjøsæter, H. (2001) Predation by cod
(Gadus morhua) on capelin (Mallotus villosus) in the
Barents Sea: implications for capelin stock assessment.
Fisheries Research 53, 197–209.
Bogstad, B. and Mehl, S. (1997) Interactions between
Atlantic cod (Gadus morhua) and its prey species in the
Barents Sea. In: Forage Fishes in Marine Ecosystems
(Proceedings of the International Symposium on the
Role of Forage Fishes in Marine Ecosystems). University
of Alaska Sea Grant College Program, University of
Alaska Fairbanks, Fairbanks, Alaska, Report No 97-01,
pp. 591–615.
Bogstad, B., Lilly, G.R., Mehl, S., Pa
´lsson, O
´.K. and
Stefa
´nsson, G. (1994) Cannibalism and year-class
strength in Atlantic cod (Gadus morhua L.) in Arcto-
boreal ecosystems (Barents Sea, Iceland and eastern
Newfoundland). ICES Marine Science Symposium 198,
576–599.
Bogstad, B., Hiis Hauge, K. and Ulltang, Ø. (1997)
MULTSPEC – a multi-species model for fish and marine
mammals in the Barents Sea. J Northw Atl Fish Sci 22,
317–341.
Bogstad, B., Haug, T. and Mehl, S. (2000) Who eats whom
in the Barents Sea? NAMMCO Scientific Publications 2,
98–119.
Bowen, W.D., McMillan, J. and Mohn, R. (2003) Sustained
exponential population growth of grey seals at Sable
Island, Nova Scotia. ICES Journal of Marine Science 60,
1265–1274.
Bowering, W.R. and Lilly, G.R. (1992) Greenland halibut
(Reinhardtius hippoglossoides) off southern Labrador and
northeastern Newfoundland (Northwest Atlantic) feed
primarily on capelin (Mallotus villosus). Netherlands
Journal of Sea Research 29, 211–222.
Bowman, R.E. and Michaels, W.L. (1984) Food of seventeen
species of northwest Atlantic fish. NOAA Tech Memo
NMFS-F/NEC-28.
Brander, K. (1988) Multispecies fisheries in the Irish Sea.
In: Fish Population Dynamics – The implications for
management (Pd Edition) (ed. J.A. Gulland). John Wiley
and Sons Ltd, Great Britain, pp. 303–328.
Brander, K. (2000) Effects of environmental variability on
growth and recruitment in cod (Gadus morhua) using a
comparative approach. Oceanologica Acta 23, 485–496.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 23
Brander, K.M. and Bennett, D.B. (1989) Norway lobsters
in the Irish Sea: modelling one component of a multi-
species resource. In: Marine Invertebrate Fisheries (ed. J.F.
Caddy). John Wiley & Sons, London, UK, pp. 183–204.
Brown, W.W. and Cheng, C. (1946) Investigations into the
food of the cod (Gadus callarias L.) off Bear Island, and of
the cod and haddock (G. aeglefinus L.) off Iceland and the
Murman Coast. Hull Bulletins of Marine Ecology Volume
III,18, 35–71.
Brown, J.A., Pepin, P., Methven, D.A. and Somerton, D.C.
(1989) The feeding, growth and behaviour of juvenile
cod, Gadus morhua L., in cold environments. Journal of
Fish Biology 35, 373–380.
Bundy, A. (2001) Fishing on ecosystems: the interplay of
fishing and predation in Newfoundland-Labrador. Cana-
dian Journal of Fisheries and Aquatic Sciences 58, 1153–
1167.
Bundy, A., Lilly, G.R. and Shelton, P.A. (2000) A mass
balance model of the Newfoundland-Labrador Shelf.
Canadian Technical Report of Fisheries and Aquatic Sciences
2310, xiv + 157.
Burton, M.P.M., Penney, R.M. and Biddiscombe, S. (1997)
Time course of gametogenesis in northwest Atlantic cod
(Gadus morhua). Canadian Journal of Fisheries and Aquatic
Sciences 54(Suppl. 1), 122–131.
Carscadden, J. and Nakashima, B.S. (1997) Abundance
and changes in distribution, biology, and behavior of
capelin in response to cooler waters of the 1990s. In
Forage Fishes in Marine Ecosystems (Proceedings of the
International Symposium on the Role of Forage Fishes in
Marine Ecosystems). University of Alaska Sea Grant
College Program, University of Alaska Fairbanks, Fair-
banks, Alaska, Report No 97-01, pp. 457–468.
Carscadden, J.E., Frank, K.T. and Leggett, W.C. (2001)
Ecosystem changes and the effects on capelin (Mallotus
villosus), a major forage species. Canadian Journal of
Fisheries and Aquatic Sciences 58, 73–85.
Chouinard, G.A., Sinclair, A.F. and Swain, D.P. (2003)
Factors implicated in the lack of recovery of southern Gulf of
St. Lawrence cod since the early 1990s. ICES CM 2003/
U:04.
Christensen, V., Gue
´nette, S., Heymans, J.J., Walters, C.J.,
Watson, R., Zeller, D. and Pauly, D. (2003) Hundred-
year decline of North Atlantic predatory fishes. Fish and
Fisheries 4, 1–24.
Clark, D.S., Brown, J.A., Goddard, S.J. and Moir, J. (1995)
Activity and feeding behavior of Atlantic cod (Gadus
morhua) in sea pens. Aquaculture 131, 49–57.
Cohen, E.B., Grosslein, M.D., Sissenwine, M.P., Steimle, F.
and Wright, W.R. (1982) Energy budget of Georges
Bank. Canadian Special Publication in Fisheries and Aquatic
Science 59, 95–107.
Colbourne, E.B. and Anderson, J.T. (2003) Biological
response in a changing ocean environment in New-
foundland waters during the latter decades of the 1900s.
ICES Marine Science Symposium 219, 169–181.
Cushing, D.H. (1980) The decline of the herring stocks and
the gadoid outburst. Journal du Conseil International pour
l’Exploration de la Mer 39, 70–81.
Daan, N., Rjinsdorp, A.D. and van Overbeeke, G.R. (1985)
Predation by North Sea herring Clupea harengus on eggs
of plaice Pleuronectes platessa and cod Gadus morhua.
Transactions of the American Fisheries Society 114, 499–
506.
Daan, N., Heessen, H.J.K. and Pope, J.G. (1994) Changes in
the North Sea cod stock during the twentieth century.
ICES Marine Science Symposium 198, 229–243.
Dalpadado, P. and Bogstad, B. (2004) Diet of juvenile cod
(age 0–2) in the Barents Sea in relation to food
availability and cod growth. Polar Biology 27, 140–154.
Danı´elsson, A
´., Stefa
´nsson, G., Baldursson, F.M. and
Tho
´rarinsson, K. (1997) Utilization of the Icelandic
cod stock in a Multispecies Context. Marine Resources
Economics 12, 329–344.
Dawe, E.G., Dalley, E.L. and Lidster, W.W. (1997) Fish
prey spectrum of short-finned squid (Illex illecebrosus)at
Newfoundland. Canadian Journal of Fisheries and Aquatic
Sciences 54(Suppl. 1), 200–208.
DFO (Department of Fisheries and Oceans). (2003) North-
ern (2J + 3KL) cod. DFO Can Sci Advis Sec Status Report
2003/018.
Drinkwater, K.F. (2002) A review of the role of climate
variability in the decline of northern cod. American
Fisheries Society Symposium 32, 113–130.
Drinkwater, K.F. (2005) The response of Atlantic cod
(Gadus morhua) to future climate change. ICES Journal of
Marine Science 62, 1327–1337.
Dutil, J.D. and Lambert, Y. (2000) Natural mortality from
poor condition in Atlantic cod (Gadus morhua). Canadian
Journal of Fisheries and Aquatic Sciences 57, 826–836.
Dutil, J.D., Lambert, Y. and Chabot, D. (2003) Winter and
spring changes in condition factor and energy reserves
of wild cod compared with changes observed during
food-deprivation in the laboratory. ICES Journal of
Marine Science 60, 780–786.
FAO (Food and Agriculture Organization). (1998) The State
of World Fisheries and Aquaculture 1998. FAO, Rome,
Italy.
Floeter, J., Kempf, A., Vinther, M., Schrum, C. and
Temming, A. (2005) Grey gurnard (Eutrigla gurnadus)
in the North Sea: An emerging key predator? Canadian
Journal of Fisheries and Aquatic Sciences 62, 1853–1864.
Fogarty, M.J. and Murawski, S.A. (1998) Large-scale
disturbance and the structure of marine ecosystems:
fishery impacts on Georges Bank. Ecological Applications
8, S6–S22.
Fogarty, M.J., Cohen, E.B., Michaels, W.L. and Morse,
W.W. (1991) Predation and the regulation of sand lance
populations: An exploratory analysis. ICES Marine
Science Symposium 193, 120–124.
Folkow, L.P., Haug, T., Nilssen, K.T. and Nordøy, E.S.
(2000) Estimated food consumption of minke whales
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
24 No claim to original US government works
Balaenoptera acutorostrata in Northeast Atlantic waters
in 1992–1995. NAMMCO Scientific Publications 2, 65–
81.
Fu, C., Mohn, R. and Fanning, L.P. (2001) Why the
Atlantic cod (Gadus morhua) stock off eastern Nova
Scotia has not recovered. Canadian Journal of Fisheries
and Aquatic Sciences 58, 1613–1623.
Garcia, S. and Newton, C.. (1997) Current situation,
trends, and prospects in world capture fisheries. In:
Global Trends: Fisheries Management (eds D. Pikitch, D.
Huppert and M.P. Sissenwine). American Fisheries
Society Symposium 20, Bethesda, MD, USA, pp. 3–27.
Garrison, L.P. and Link, J.S. (2000a) Dietary guild struc-
ture of the fish community in the northeast United
States continental shelf ecosystem. Marine Ecology Pro-
gress Series 202, 231–240.
Garrison, L.P. and Link, J.S. (2000b) Fishing effects on
spatial distribution and trophic guild structure of the fish
community in the Georges Bank region. ICES Journal of
Marine Science 57, 723–730.
Garrison, L.P., Michaels, W., Link, J.S. and Fogarty, M.J.
(2000) Predation risk on larval gadids by pelagic fish in
the Georges Bank ecosystem: I. Spatial overlap associ-
ated with hydrographic features. Canadian Journal of
Fisheries and Aquatic Sciences 57, 2455–2469.
Garrison, L.P., Michaels, W., Link, J.S. and Fogarty, M.J.
(2002) Spatial distribution and overlap between ichthy-
oplankton and pelagic fish and squids on the southern
flank of Georges Bank. Fisheries Oceanography 11, 267–
285.
Gislason, H. (1999) Single and multispecies reference
points for Baltic fish stocks. ICES Journal of Marine Science
56, 571–583.
Gjøsæter, H. (1998) The population biology of capelin in
the Barents Sea. Sarsia 83, 453–496.
Gjøsæter, H. and Bogstad, B. (1998) Effects of the presence
of herring on the stock-recruitment relationship of
Barents Sea capelin (Mallotus villosus). Fisheries Research
38, 57–71.
Gjøsæter, H., Bogstad, B. and Tjelmeland, S. (2002)
Assessment methodology for Barents Sea capelin (Mal-
lotus villosus Mu
¨ller). ICES Journal of Marine Science 59,
1086–1095.
Gjøsæter, H., Bogstad, B. and Tjelmeland, S. (2008). Why
did three capelin stock collapses in the Barents Sea affect
the ecosystem differently? Marine Biology Research (in
press).
Gomes, M.C., Haedrich, R.L. and Villagarcia, M.G. (1995)
Spatial and temporal changes in the groundfish assem-
blages on the north-east Newfoundland/Labrador Shelf,
north-west Atlantic, 1978–1991. Fisheries Oceanography
4, 85–101.
Haedrich, R.L. and Fischer, J. (1996) Stability and
change of exploited fish communities in a cold ocean
continental shelf ecosystem. Senckenbergiana Maritima
27, 237–243.
Hammill, M.O. and Stenson, G.B. (2000) Estimated prey
consumption by harp seals (Phoca groenlandica), hooded
seals (Cystophora cristata), grey seals (Halichoerus grypus)
and harbour seals (Phoca vitulina) in Atlantic Canada.
Journal of Northwest Atlantic Fisheries Science 26, 1–23.
Hamre, J. (1994) Biodiversity and exploitation of the main
fish stocks in the Norwegian – Barents Sea ecosystem.
Biodiversity and Conservation 3, 473–492.
Hamre, J. (2003) Capelin and herring as key species for the
yield of north-east Arctic cod. Results from multispecies
model runs. Scientia Marina 67(Suppl. 1), 315–323.
Hansen, P.M. (1949) Studies on the biology of the cod
in Greenland waters. ICES Rapports et Proce
´s-Verbaux des
Re
´unions du Conseil International pour l’Exploration de la
Mer 123, 1–77.
Hanson, J.M. and Lanteigne, M. (2000) Evaluation of
Atlantic cod predation on American lobster in the
southern Gulf of St. Lawrence, with comments on other
potential fish predators. Transactions of the American
Fisheries Society 129, 13–29.
Hansson, S., Karlsson, L., Ikonen, E. et al. (2001) Stomach
analyses of Baltic salmon from 1959–1962 and 1994–
1997: possible relations between diet and yolk-sac-fry
mortality (M74). Journal of Fish Biology 58, 1730–1745.
Haug, T., Lindstrøm, U., Nilssen, K.T., Røttingen, I. and
Skaug, H.J. (1996) Diet and food availability for North-
east Atlantic minke whales, Balaenoptera acutorostrata.
Reports of the International Whaling Commission 46, 371–
382.
Hauksson, E. and Bogason, V. (1995) Food of harp seals
(Phoca groenlandica Erxleben, 1777) in Icelandic waters in
the period 1990–1994. ICES CM 1995/N:14, 7 pp.
Healey, B.P. and Stenson, G.B. (2000) Estimating pup
production and population size of the northwest Atlantic harp
seal (Phoca groenlandica). DFO Can Stock Assess Sec Res
Doc 2000/081.
Hislop, J.R.G. (1996) Changes in North Sea gadoid stocks.
ICES Journal of Marine Science 53, 1146–1156.
Hjermann, D.Ø., Bogstad, B., Eikeset, A.M., Ottersen, G.,
Gjøsæter, H. and Stenseth, N.C. (2007) Food web
dynamics affect Northeast Arctic cod recruitment. Pro-
ceedings of the Royal Society of London, Series B 274, 661–
669.
Hovde, S.C., Albert, O.T. and Nilssen, E.M. (2002) Spatial,
seasonal and ontogenetic variation in diet of Northeast
Arctic Greenland halibut (Reinhardtius hippoglossoides).
ICES Journal of Marine Science 59, 421–437.
Hutchings, J.A. (1996) Spatial and temporal variation in
the density of northern cod and a review of hypotheses
for the stock’s collapse. Canadian Journal of Fisheries and
Aquatic Sciences 53, 943–962.
Hutchings, J.A. and Myers, R.A. (1994) What can be
learned from the collapse of a renewable resource?
Atlantic cod, Gadus morhua, of Newfoundland and
Labrador. Canadian Journal of Fisheries and Aquatic
Sciences 51, 2126–2146.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 25
Hylen, A. (2002) Fluctuations in abundance of Northeast
Arctic cod during the 20th century. ICES Marine Science
Symposium 215, 543–550.
ICES (International Council for the Exploration of the Sea).
(1989) Database report of the stomach sampling project
1981. ICES Cooperative Research Report, No 164. Editor
Niels Daan.
ICES. (1990) Report of the Working Group on Multispecies
Assessment of Baltic fish. ICES CM 1990/Assess:1.
ICES. (1992) Report of the Working Group on Multispecies
Assessment of Baltic Fish. ICES CM 1992/Assess:7.
ICES. (1997) Database report of the stomach sampling
project 1991. ICES Cooperative Research Report, No.
219.
ICES. (2002) Report of the Study Group on Multispecies
Assessments in the North Sea. ICES CM 2002/D:04.
ICES. (2003a) Report of the Study Group on Multispecies
Assessments in the North Sea. ICES CM 2003/D:09.
ICES. (2003b) Report of the Baltic Fisheries Assessment
Working Group, Copenhagen 7–16 April 2003. ICES CM
2003/ACFM:21, 522 pp.
ICES. (2003c) Report of the ICES Advisory Committee on
Ecosystems, 2003. ICES Cooperative Research Report, No.
262.
ICES. (2003d) Report of the Study Group on Multispecies
Assessment in the Baltic. ICES CM 2003/H:03, 78 pp.
ICES. (2003e) Report of the ICES Advisory Committee on
Fisheries Management 2003. ICES Cooperative Research
Report, No. 261.
ICES. (2004a) Report of the Working Group on the Assess-
ment of Demersal Stocks in the North Sea and Skagerrak.
ICES CM 2004/ACFM:07.
ICES. (2004b) Report of the North-Western Working Group,
Copenhagen 27 April–6 May 2004. ICES CM 2004/
ACFM:25, 469 pp.
ICES. (2004c) Report of the ICES Advisory Committee on
Fisheries Management and Advisory Committee on Ecosys-
tem. ICES ADVICE 2004.
ICES. (2005a) Report of the Working Group on the Assess-
ment of Demersal Stocks in the North Sea and Skagerrak.
ICES CM 2005/ACFM:07.
ICES. (2005b) Report of the Study Group on Multispecies
Assessment in the Baltic. ICES CM 2005/H:06, 96 pp.
ICES. (2005c) Report of the Study Group on Multispecies
Assessments in the North Sea. ICES CM 2005/D:06, 159
pp.
ICES. (2006a) Report of the Northern Pelagic and Blue
Whiting Fisheries Working Group, Copenhagen, Denmark,
25 August–1 September 2005. ICES CM 2006/ACFM:05,
241 pp.
ICES. (2006b) Report of the North-Western Working Group,
Copenhagen 25 April–4 May 2006. ICES C.M. 2006/
ACFM:26, 604 pp.
ICES. (2007) Report of the Arctic Fisheries Working Group,
Vigo, Spain 18–27 April 2007. ICES C.M. 2007/
ACFM:16, 651 pp.
IPCC (International Panel on Climate Change). (2007)
Climate Change 2007: The Physical Science Basis. Contri-
bution of Working Group I to the Fourth Assessment Report
of the Intergovernmental Panel on Climate Change (eds
S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis,
K.B. Averyt, M. Tignor and H.L. Miller). Cambridge
University Press, Cambridge, UK, 996 pp.
IPCC (International Panel on Climate Change). (2001)
Climate Change 2001: The Scientific Basis. Contribution of
Working Group I to the Third Assessment Report of the
Intergovernmental Panel on Climate Change (eds J.T.
Houghton, Y. Ding, D.H.J. Griggs, M. Noguer, P.J. van
der Linden, X. Dai, K. Maskell and C.A. Johnson).
Cambridge University Press, Cambridge, UK, 881 pp.
Jakobsson, J. and Stefa
´nsson, G. (1998) Rational harvest-
ing of the cod-capelin-shrimp complex in the Icelandic
marine ecosystem. Fisheries Research 37, 7–21.
Jensen, A.C. (1972) The Cod. Thomas Y Crowell Co., New
York.
Jobling, M., Meløy, O.H., dos Santos, J. and Christiansen, B.
(1994) The compensatory growth response of the
Atlantic cod: Effects of nutritional history. Aquaculture
International 2, 75–90.
Johansen, G.O. (2003) Size-dependent predation on juve-
nile herring (Clupea harengus L.) by North-east Arctic cod
(Gadus morhua L.) in the Barents Sea. Sarsia 88, 136–
153.
Jørgensen, C., Enberg, K., Dunlop, E.S. et al. (2007)
Managing evolving fish stocks. Science 318, 1247–1248.
Karlsson, L., Ikonen, E., Mitans, A. and Hansson, S. (1999)
The diet of salmon (Salmo salar) in the Baltic Sea and
connections with the M74 syndrome. Ambio 28, 37–42.
Kerr, S.R. (1971) Prediction of fish growth efficiency in
nature. Journal of the Fisheries Research Board of Canada
28, 809–814.
Kjesbu, O.S. (1994) Time of start of spawning in Atlantic
cod (Gadus morhua) females in relation to vitellogenic
oocyte diameter, temperature, fish length and condition.
Journal of Fish Biology 45, 719–735.
Ko¨ ster, F.W. and Mo¨llmann, C. (2000) Trophodynamic
control by clupeid predators on recruitment success in
Baltic cod? ICES Journal of Marine Science 57, 310–
323.
Ko¨ ster, F.W., Mo¨llmann, C., Neuenfeldt, S. et al. (2003)
Fish stock development in the Central Baltic Sea (1976–
2000) in relation to variability in the environment. ICES
Marine Science Symposium 219, 294–306.
Krohn, M., Reidy, S. and Kerr, S. (1997) Bioenergetic
analysis of the effects of temperature and prey availabil-
ity on growth and condition of northern cod (Gadus
morhua). Canadian Journal of Fisheries and Aquatic Sciences
54(Suppl. 1), 113–121.
Kurlansky, M. (1997) Cod: A Biography of the Fish that
Changed the World. Walker and Co., New York, USA.
Lambert, Y. and Dutil, J.D. (1997) Condition and energy
reserves of Atlantic cod (Gadus morhua) during the
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
26 No claim to original US government works
collapse of the northern Gulf of St Lawrence stock.
Canadian Journal of Fisheries and Aquatic Sciences 54,
2388–2400.
Lambert, Y. and Dutil, J.D. (2000) Energetic consequences
of reproduction in Atlantic cod (Gadus morhua)in
relation to spawning level of somatic energy reserves.
Canadian Journal of Fisheries and Aquatic Sciences 57,
815–825.
Langton, R.W. (1982) Diet overlap between Atlantic cod,
Gadus morhua, silver hake, Merluccius bilinearis, and
fifteen other Northwest Atlantic finfish. Fishery Bulletin
80, 745–759.
Langton, R.W. and Bowman, R.E. (1980) Food of fifteen
northwest Atlantic gadiform fishes. NOAA Tech Rep
NMFS-SSRF-740.
Lear, W.H., Baird, J.W., Rice, J.C., Carscadden, J.E., Lilly,
G.R. and Akenhead, S.A. (1986) An examination of
factors affecting catch in the inshore cod fishery of
Labrador and eastern Newfoundland. Canadian Technical
Report of Fisheries and Aquatic Sciences 1469, iv + 71.
Lilly, G.R. (1984) Predation by Atlantic cod on shrimp and
crabs off northeastern Newfoundland in autumn of 1977–
82. ICES CM 1984/G:53.
Lilly, G.R. (1987) Interactions between Atlantic cod (Gadus
morhua) and capelin (Mallotus villosus) off Labrador and
eastern Newfoundland: a review. Canadian Technical
Report of Fisheries and Aquatic Sciences 1567, vii + 37.
Lilly, G.R. (1991) Interannual variability in predation by
cod (Gadus morhua) on capelin (Mallotus villosus) and
other prey off southern Labrador and northeastern
Newfoundland. ICES Marine Science Symposium 193,
133–146.
Lilly, G.R. (1994) Predation by Atlantic cod on capelin on
the southern Labrador and northeast Newfoundland
shelves during a period of changing spatial distributions.
ICES Marine Science Symposium 198, 600–611.
Lilly, G.R. (2001) Changes in size at age and condition of cod
(Gadus morhua) off Labrador and eastern Newfoundland
during 1978–2000. ICES CM 2001/V:15, 34 pp.
Lilly, G.R. and Osborne, D.R. (1984) Predation by Atlantic
cod (Gadus morhua) on short-finned squid (Illex illecebro-
sus) off eastern Newfoundland and in the northeastern Gulf
of St. Lawrence. NAFO SCR Doc 84/108.
Lilly, G.R., Hop, H., Stansbury, D.E. and Bishop, C.A.
(1994) Distribution and abundance of polar cod (Boreogadus
saida) off southern Labrador and eastern Newfoundland.
ICES CM1994/O:6, 21 pp.
Lilly, G.R., Shelton, P.A., Brattey, J., Cadigan, N.G.,
Murphy, E.F. and Stansbury, D.E. (1999) An assessment
of the cod stock in NAFO Divisions 2J + 3KL. DFO Can
Stock Assess. Sec Res Doc 99/42, 165 pp.
Lilly, G.R., Parsons, D.G. and Kulka, D.W. (2000) Was the
increase in shrimp biomass on the Northeast Newfound-
land Shelf a consequence of a release in predation
pressure from cod? Journal of Northwest Atlantic Fisheries
Science 27, 45–61.
Lilly, G.R., Brattey, J., Cadigan, N.G., Healey, B.P. and
Murphy, E.F. (2005) An assessment of the cod (Gadus
morhua) stock in NAFO Divisions 2J3KL in March 2005.
DFO Can Sci Adv Sec Res Doc 2005/018.
Lilly, G.R., Wieland, K., Rothschild, B.J. et al. (2008)
Decline and recovery of Atlantic cod (Gadus morhua)
stocks throughout the North Atlantic. In: Resiliency of
Gadid Stocks to Fishing and Climate Change (eds G.H.
Kruse, K. Drinkwater, J.N. Ianelli, J.S. Link, D.L. Stram,
V. Wespestad and D. Woodby). University of Alaska
Fairbanks, Alaska Sea Grant, pp. 39–66.
Link, J.S. (1999) (Re)Constructing food webs and manag-
ing fisheries. Proceedings of the 16th Lowell Wakefield
Fisheries Symposium – Ecosystem Considerations in Fish-
eries Management. Alaska Sea Grant College Program
Report No. 99-01. University of Alaska Fairbanks,
Fairbanks, Alaska. AK-SG-99-01, pp. 571–588.
Link, J.S. (2002) Does food web theory work for marine
ecosystems? Marine Ecology Progress Series 230, 1–9.
Link, J.S. (2003) A model of aggregate biomass tradeoffs.
ICES Annual Science Conference. Theme Session on Reference
Point Approaches to Management within the Precautionary
Approach, Tallinn, Estonia, ICES CM 2003/Y:08, 28 pp.
Link, J.S. and Almeida, F.P. (2000) An overview and history
of the food web dynamics program of the Northeast Fisheries
Science Center, Woods Hole, Massachusetts. NOAA Tech
Memo NMFS-NE-159.
Link, J. and Burnett, J. (2001) The relationship between
stomach contents and maturity state for major North-
west Atlantic fishes: new paradigms. Journal of Fish
Biology 59, 783–794.
Link, J.S. and Garrison, L.P. (2002a) Trophic ecology of
Atlantic cod Gadus morhua on the Northeast US Conti-
nental Shelf. Marine Ecology Progress Series 227, 109–
123.
Link, J.S. and Garrison, L.P. (2002b) Changes in piscivory
associated with fishing induced changes to the finfish
community on Georges Bank. Fisheries Research 55,
71–86.
Link, J.S., Garrison, L.P. and Almeida, F.P. (2002) Inter-
actions between elasmobranchs and groundfish species
(Gadidae and Pleuronectidae) on the Northeast U.S.
Shelf. I: Evaluating Predation. North American Journal of
Fisheries Management 22, 550–562.
Magnu´ sson, K.G. and Pa
´lsson, O
´.K. (1989) Trophic
ecological relationships of Icelandic cod. Rapports et
Proce
`s-Verbaux des Re
´unions du Conseil International pour
l’Exploration de la Mer 188, 206–224.
Magnu´ sson, K.G. and Pa
´lsson, O
´.K. (1991a) Predator-prey
interactions of cod and capelin in Icelandic waters. ICES
Marine Science Symposium 193, 153–170.
Magnu´ sson, K.G. and Pa
´lsson, O
´.K. (1991b) The predatory
impact of cod on shrimps in Icelandic waters. ICES CM
1991/K:31, 17 pp.
Marshall, C.T., Kjesbu, O.S., Yaragina, N.A., Solemdal, P.
and Ulltang, Ø. (1998) Is spawner biomass a sensitive
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 27
measure of the reproductive and recruitment potential of
Northeast Arctic cod? Canadian Journal of Fisheries and
Aquatic Sciences 55, 1766–1783.
Marshall, C.T., Yaragina, N.A., Lambert, Y. and Kjesbu,
O.S. (1999) Total lipid energy as a proxy for total egg
production by fish stocks. Nature 402, 288–290.
Mayo, R.K., O’Brien, L. and Wigley, S.E. (1998) Assessment
of the Gulf of Maine Atlantic Cod Stock for 1998. NEFSC
CRD 98-13.
McLaren, I., Brault, S., Harwood, J. and Vardy, D. (2001)
Report of the Eminent Panel on Seal Management. Depart-
ment of Fisheries and Oceans, Ottawa, Canada.
Mehl, S. and Sunnana
˚, K. (1991) Changes in growth of
northeast Arctic cod in relation to food consumption in
1984–1988. ICES Marine Science Symposium 193, 109–
112.
Mehl, S. and Yaragina, N.A. (1992) Methods and results in
the joint PINRO-IMR stomach sampling program. In:
Interrelations Between Fish Populations in the Barents Sea
(Proceedings of the 5th PINRO-IMR Symposium,
Murmansk, 12–16 August, 1991). B. Bogstad and
S. Tjelmeland, eds. Institute of Marine Research, Bergen,
Norway, pp. 5–16.
Mello, L.G.S. and Rose, G.A. (2005) Seasonal cycles in
weight and condition in Atlantic cod (Gadus morhua L.)
in relation to fisheries. ICES Journal of Marine Science 62,
1006–1015.
Methven, D.A. (1999) Annotated bibliography of demersal
fish feeding with emphasis on selected studies from the
Scotian Shelf and Grand Banks of the northwestern
Atlantic. Canadian Technical Report of Fisheries and
Aquatic Sciences 2267, 106.
Michalsen, K., Johannesen, E. and Bogstad, B. (2008)
Feeding of mature cod (Gadus morhua L) at the spawning
grounds in Lofoten. ICES Journal of Marine Science,65,
pp. 571–580.
Millar, R.B., Fahrig, L. and Shelton, P.A. (1990) Effect of
capelin biomass on cod growth. ICES CM 1990/G:25, 10 pp.
Molenaar, E.J. (2002) Ecosystem-based fisheries manage-
ment, commercial fisheries, marine mammals and the
2001 Reykjavik Declaration in the context of interna-
tional law. International Journal of Marine and Coastal Law
17, 561–595.
Molenaar, E.J. (2003) Marine mammals: the role of ethics
and ecosystem considerations. Journal of International
Wildlife Law and Policy 6, 31–51.
Mo¨ llmann, C. and Ko¨ster, F.W. (2002) Population dynam-
ics of calanoid copepods and the implications of their
predation by clupeid fish in the Central Baltic Sea.
Journal of Plankton Research 24, 959–977.
Mo¨ llmann, C., Kornilovs, G., Fetter, M., Ko¨ster, F.W. and
Hinrichsen, H.-H. (2003) Marine copepod as a mediator
between climate variability and fisheries in the Central
Baltic Sea. Fisheries Oceanography 12, 360–368.
Mo¨ llmann, C., Kornilovs, G., Fetter, M. and Ko¨ster, F.W.
(2005) Climate, zooplankton, and pelagic fish growth in
the central Baltic Sea. ICES Journal of Marine Science 62,
1270–1280.
Murawski, S.A., Maguire, J.J., Mayo, R.K. and Serchuk,
F.M. (1997) Groundfish stocks and the fishing industry.
In: Northwest Atlantic groundfish: Perspectives on a Fishery
Collapse (eds J. Boreman, B.S. Nakashima, J.A. Wilson
and R.L. Kendall). American Fisheries Society, Bethesda,
MD, USA, pp. 27–70.
Myers, R.A., Hutchings, J.A. and Barrowman, N.J. (1996)
Hypotheses for the decline of cod in the North Atlantic.
Marine Ecology Progress Series 138, 293–308.
Nakken, O. (1994) Causes of trends and fluctuations in the
Arcto-Norwegian cod stock. ICES Marine Science Sympo-
sium 198, 212–228.
Nakken, O., Sandberg, P. and Steinshamn, S.I. (1996)
Reference points for optimal fish stock management. A
lesson to be learned from the Northeast Arctic cod stock.
Marine Policy 20, 447–462.
Narayanan, S., Carscadden, J., Dempson, J.B., O’Connell,
M.F., Prinsenberg, S., Reddin, D.G. and Shackell, N.
(1995) Marine climate off Newfoundland and its influ-
ence on Atlantic salmon (Salmo salar) and capelin
(Mallotus villosus). In: Climate change and northern fish
populations (ed. R.J. Beamish), Canadian Special Publica-
tion in Fisheries and Aquatic Science 121, 461–474.
NEFSC (Northeast Fisheries Science Center). (1998) Status
of fishery resources off the northeastern United States for
1998. NOAA Technical Memorandum NMFS-NE-115,
Woods Hole, Massachusetts. This ‘‘Status of the Stocks’’
is updated regularly on the webpage: http://www.
nefsc.nmfs.gov/sos/ (accessed: 30 October 2004).
Neuenfeldt, S. and Ko¨ ster, F.W. (2000) Trophodynamic
control on recruitment success in Baltic cod: the
influence of cannibalism. ICES Journal of Marine Science
57, 300–309.
Nilssen, K.T., Pedersen, O.-P., Folkow, L.P. and Haug, T.
(2000) Food consumption estimates of Barents Sea harp
seals. NAMMCO Scientific Publications 2, 9–27.
O’Brien, L. (1999) Factors influencing rates of maturation
in the Georges Bank and Gulf of Maine Atlantic Cod
stocks. Journal of Northwest Atlantic Fisheries Science 25,
179–203.
O’Brien, L. and Munroe, N.. (2000) Assessment of the
Georges Bank Atlantic Cod stock for 2000. NEFSC CRD-00-
17.
O’Driscoll, R.L., Schneider, D.C., Rose, G.A. and Lilly, G.R.
(2000) Potential contact statistics for measuring scale-
dependent spatial pattern and association: an example of
northern cod (Gadus morhua) and capelin (Mallotus
villosus). Canadian Journal of Fisheries and Aquatic Sciences
57, 1355–1368.
Pa
´lsson, O
´.K. (1983) The feeding habits of demersal fish in
Icelandic waters. Rit Fiskideildar 7, 1–60.
Pa
´lsson, O
´.K. (1994) A review of the trophic interactions
of cod stocks in the North Atlantic. ICES Marine Science
Symposium 198, 553–575.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
28 No claim to original US government works
Pa
´lsson, O
´.K. (1997) Predator-prey interactions of demer-
sal fish species and capelin (Mallotus villosus) in Icelandic
waters. In: Forage Fishes in Marine Ecosystems (Proceed-
ings of the International Symposium on the Role of
Forage Fishes in Marine Ecosystems). University of
Alaska Sea Grant College Program, University of Alaska,
Fairbanks, Fairbanks, Alaska, Report No 97-01, pp.
105–126.
Parsons, D.G. (2005) Predators of northern shrimp,
Pandalus borealis (Pandalidae), throughout the North
Atlantic. Marine Biology Research 1, 48–58.
Parsons, D.G. and Colbourne, E.B. (2000) Forecasting
fishery performance for northern shrimp (Pandalus
borealis) on the Labrador Shelf (NAFO Divisions 2HJ).
Journal of Northwest Atlantic Fisheries Science 27, 11–20.
Parsons, L.S. and Lear, W.H. (2001) Climate variability
and marine ecosystem impacts: a North Atlantic per-
spective. Progress in Oceanography 49, 167–188.
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. and
Torres, F.C. Jr (1998) Fishing down marine food webs.
Science 279, 860–863.
Ponomarenko, I.Ya. and Yaragina, N.A. (1979) Seasonal
and year-to-year fluctuations in the feeding of the Barents
Sea cod on Euphausiacea in 1947–1977. ICES CM 1979/
G:17, 20 pp.
Ponomarenko, V.P., Ponomarenko, I.Ya. and Yaragina,
N.A. (1978) Consumption of the Barents Sea capelin by
cod and haddock in 1974–1976. ICES CM 1978/G:23,
22 pp.
Popova, O.A. (1962) Some data on the feeding of cod in
the Newfoundland area of the Northwest Atlantic. In:
Soviet Fisheries Investigations in the Northwest Atlantic,
VNIRO-PINRO, Moscow (ed. Y.Y. Marti). (Translated for
US Department of Interior and National Science
Foundation, Washington, DC, by Israel Program of
Scientific Translations, Jerusalem, 1963: pp. 228–248).
Rae, B.B. (1967) The food of cod in the North Sea and
on west of Scotland grounds. Marine Research 1967 (1):
1–68
Rice, J. (1995) Food web theory, marine food webs, and
what climate change may do to northern marine fish
populations. In: Climate Change and Northern Fish Pop-
ulations (ed. R.J. Beamish), Canadian Special Publication in
Fisheries and Aquatic Science 121, 561–568.
Rice, J.C., Shelton, P.A., Rivard, D., Chouinard, G.A. and
Fre
´chet, A. (2003) Recovering Canadian Atlantic cod
stocks: the shape of things to come?. ICES CM 2003/U:06.
Rose, G.A. (2005) On distributional responses of North
Atlantic fish to climate change. ICES Journal of Marine
Science 62, 1360–1374.
Rose, G.A. and O’Driscoll, R.L. (2002) Capelin are good for
cod: can the northern stock rebuild without them? ICES
Journal of Marine Science 59, 1018–1026.
Rose, G.A., deYoung, B., Kulka, D.W., Goddard, S.V. and
Fletcher, G.L. (2000) Distribution shifts and overfishing
the northern cod (Gadus morhua): a view from the ocean.
Canadian Journal of Fisheries and Aquatic Sciences 57,
644–663.
Scharf, F.S., Juanes, F. and Rountree, R.A. (2000) Predator
size-prey size relationships of marine fish predators:
interspecific variation and effects of ontogeny and body
size on trophic-niche breadth. Marine Ecology Progress
Series 208, 229–248.
Schopka, S.A. (1994) Fluctuations in the cod stock off
Iceland during the twentieth century in relation to
changes in the fisheries and environment. ICES Marine
Science Symposium 198, 175–193.
Schweder, T., Hagen, G.S. and Hatlebakk, E. (2000) Direct
and indirect effects of minke whale abundance on cod and
herring fisheries: a scenario experiment for the Greater
Barents Sea. NAMMCO Scientific Publications 2, 120–132.
Serchuk, F.M. and Wigley, S.E. (1992) Assessment and
management of the Georges Bank cod fishery: an
historical review and evaluation. Journal of Northwest
Atlantic Fisheries Science 13, 25–52.
Serchuk, F.M., Grosslein, M.D., Lough, R.G., Mountain,
D.G. and O’Brien, L. (1994) Fishery and environmental
factors affecting trends and fluctuations in the Georges
Bank and Gulf of Maine Atlantic cod stocks: an
overview. ICES Marine Science Symposium 198, 77–109.
Shelton, P.A. (1992) Detecting and incorporating multi-
species effects into fisheries management in the north-
west and south-east Atlantic. South African Journal of
Marine Science 12, 723–737.
Shelton, P.A. and Healey, B.P. (1999) Should depensation
be dismissed as a possible explanation for the lack of
recovery of the northern cod (Gadus morhua) stock?
Canadian Journal of Fisheries and Aquatic Sciences 56,
1521–1524.
Shelton, P.A., Fahrig, L. and Millar, R.B. (1991) Uncertainty
associated with cod-capelin interactions: how much is
too much? NAFO Science Council Studies 16, 13–19.
Sigurjo
´nsson, J., Galan, A. and Vı´kingsson, G. (2000) A
note of stomach contents of minke whales (Balaenoptera
acutorostrata) in Icelandic waters. NAMMCO Scientific
Publications 2, 82–90.
Sissenwine, M.P., Cohen, E.B. and Grosslein, M.D. (1984)
Structure of the Georges Bank ecosystem. Rapports et
Proces-Verbaux des Reunions du Conseil International pour
l’Exploration de la Mer 183, 243–254.
Skaug, H.J., Gjøsæter, H., Haug, T., Lindstrøm, U. and
Nilssen, K.T. (1997) Do minke whales Balaenoptera
acutorostrata exhibit particular prey preferences? Journal
of Northwest Atlantic Fisheries Science 22, 91–104.
Sparholt, H. (1990) An Estimate of the total biomass of fish
in the North Sea. Journal du Conseil International pour
l’Exploration de la Mer 46, 200–210.
Sparholt, H. (1994) Fish species interactions in the Baltic
Sea. Dana 10, 131–162.
Sparholt, H. (1995) Using the MSVPA model to estimate
the right-hand side of the Ricker curve for cod in the
Baltic. ICES Journal of Marine Science 52, 819–826.
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
No claim to original US government works 29
Sparholt, H. (1996a) Causal correlation between recruit-
ment and spawning stock size of central Baltic cod. ICES
Journal of Marine Science 53, 771–779.
Sparholt, H. (1996b) Interaktioner mellem torsk, sild og
brisling i Centrale Østersø. Dr of Science Thesis. (In
Danish). Eget forlag, Fredsvej 8a, 2840 Holte, Denmark.
ISBN 87-985933-0-7.
Sparre, P. (1991) Introduction to multispecies virtual
population analysis. ICES Marine Science Symposium
193, 12–21.
Stefa
´nsson, G., Sku´ladottir, U. and Pe
´tursson, G. (1994)
The use of a stock production type model in evaluating the
offshore (Pandalus borealis) stock of north Icelandic
waters, including the predation of northern shrimp by
cod. ICES CM 1994/K:25.
Stefa
´nsson, G., Sigurjo
´nsson, J. and Vı´kingsson, G. (1997a)
On dynamic interactions between some fish resources and
cetaceans off Iceland based on a simulation model. Journal
of Northwest Atlantic Fisheries Science 22, 357–370.
Stefa
´nsson, G., Hauksson, E., Bo
´gason, V., Sigurjo
´nsson, J.
and Vı´kingsson, G. (1997b) Multispecies interactions in
the C Atlantic. NAMMCO SC/5/ME/13.
Stefa
´nsson, G., Sku´ladottir, U. and Steinarsson, B.Æ.
(1998) Aspects of the ecology of a Boreal System. ICES
Journal of Marine Science 55, 859–862.
Steinarsson, B.Æ. and Stefa
´nsson, G. (1996) Factors
affecting cod growth in Icelandic waters and the resulting
effect on potential yield of cod. ICES CM 1996/G:32.
Stenson, G.B. and Perry, E.A. (2001) Incorporating
uncertainty into estimates of Atlantic cod (Gadus mor-
hua), capelin (Mallotus villosus) and Arctic cod (Boreog-
adus saida) consumption by harp seals (Pagophilus
groenlandicus) in NAFO Divisions 2J3KL. DFO Can Sci
Adv Sec Res Doc 2001/074.
Swain, D.P. (1999) Changes in the distribution of Atlantic
cod (Gadus morhua) in the southern Gulf of St. Lawrence
– effects of environmental change or change in envi-
ronmental preferences? Fisheries Oceanography 8, 1–17.
Swain, D.P. and Sinclair, A.F. (2000) Pelagic fishes and
the cod recruitment dilemma in the Northwest Atlantic.
Canadian Journal of Fisheries and Aquatic Sciences 57,
1321–1325.
Taggart, C.T., Anderson, J., Bishop, C. et al. (1994)
Overview of cod stocks, biology, and environment in
the Northwest Atlantic region of Newfoundland, with
emphasis on northern cod. ICES Marine Science Sympo-
sium 198, 140–157.
Templeman, W. (1966) Marine Resources of Newfoundland.
Fisheries Research Board of Canada, Bulletin 154,
Ottawa, Canada, 170 pp. Bull 154.
Thurow, F. (1997) Estimation of the total fish biomass in
the Baltic Sea during the 20th century. ICES Journal of
Marine Science 54, 444–461.
Tsou, T.S. and Collie, J.S. (2001a) Estimating predation
mortality in the Georges Bank fish community. Canadian
Journal of Fisheries and Aquatic Sciences 58, 908–922.
Tsou, T.S. and Collie, J.S. (2001b) Predation-mediated
recruitment in the Georges Bank fish community. ICES
Journal of Marine Science 58, 994–1001.
Turrell, W., Lavin, A., Drinkwater, K.F., St John, M. and
Watson, J. (eds). 2003. Hydrobiological variability in the
ICES Area, 1990–1999. ICES Marine Science Symposium,
219, 453.
Uzars, D. and Plikshs, M. (2000) Cod (Gadus morhua L.)
cannibalism in the Central Baltic: interannual variability
and influence of recruit abundance and distribution.
ICES Journal of Marine Science 57, 324–329.
Vilhja
´lmsson, H. (2002) Capelin (Mallotus villosus) in the
Iceland-East Greenland-Jan Mayen ecosystem. ICES
Journal of Marine Science 59, 870–883.
Vilhja
´lmsson, H., Hoel, A.H., Agnarsson, S., Arnason, R.,
Carscadden, J.E., Eide, A. and Fluharty, D. et al.. (2005)
Fisheries and aquaculture. In: Arctic Climate Impact
Assessment (eds C. Symon, L. Arris and B. Heal).
Cambridge University Press, Cambridge, pp. 691–780.
Vinogradov, V.I. (1984) Food of silver hake, red hake and
other fishes of Georges Bank and adjacent waters, 1968–
74. NAFO Science Council Studies 7, 87–94.
Walters, C. and Kitchell, J.F. (2001) Cultivation/depensa-
tion effects on juvenile survival and recruitment: impli-
cations for the theory of fishing. Canadian Journal of
Fisheries and Aquatic Sciences 58, 39–50.
Westin, L. and Nissling, A. (1991) Effect of salinity on
spermatozoa motility, percentage of fertilized eggs and
egg development of Baltic cod (Gadus morhua) and
implications for cod stock fluctuations in the Baltic.
Marine Ecology 108, 5–9.
Worm, B. and Myers, R.A. (2003) Meta-analysis of cod-
shrimp interactions reveals top-down control in oceanic
food webs. Ecology 84, 162–173.
Yaragina, N.A. and Marshall, C.T. (2000) Trophic influ-
ences on interannual and seasonal variation of liver
condition index of Northeast Arctic cod (Gadus morhua).
ICES Journal of Marine Science 57, 42–55.
Yaragina, N.A., Bogstad, B. and Kovalev, Yu.A. (2007)
Reconstructing the time series of abundance of North-
east Arctic cod (Gadus morhua), taking cannibalism into
account. Marine Biology Research, pp. 18–19. (extended
abstract) In: Long-term bilateral Russian-Norwegian scien-
tific cooperation as a basis for sustainable management of
living marine resources in Barents Sea (Proceedings of the
12th Norwegian-Russian symposium, Tromsø, 21–22
August, 2007). IMR/PINRO Report Series 5/2007, 212
pp. T. Haug, O.A. Misund, H. Gjøsæter and I. Røttingen,
eds.
Yodzis, P. (2001) Must top predators be culled for the sake
of fisheries? Trends in Ecology and Evolution 16, 78–84.
Zatsepin, V.J. and Petrova, N.S. (1939) The food of the
commercial stocks of cod in the southern part of the
Barents Sea (from observations made in 1934–38).
Trudy Pol Inst Morsk. Rhyb Khoz Okeanogr 1939, 1–170
(Fish Res Board Can Transl Ser No. 498, 1964).
Ecosystem role of cod J S Link et al.
Journal compilation Ó2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–30
30 No claim to original US government works
... The positive relationship between cod exploitation rate and the CPUE of anglerfish, spurdog and the skates and rays were contrary to our expectation that reducing fishing pressure on a 'choke' species would increase the CPUE of other demersal fish. Cod have a broad diet that shifts ontogenetically (Pinnegar et al., 2003;Link et al., 2009) and their diet consists of several species (e.g., whiting, haddock, megrim, Trisopterus spp.) included in this study (ICES, 1997). We did not find evidence in the literature that cod actively predate on spurdog, anglerfish, skates, and rays but we speculate that these species may be released from competition pressure by the removal of cod from the community. ...
Article
Full-text available
The Celtic Sea is a productive fishing ground, therefore identifying the relative importance of fishing and environmental factors on fish stock dynamics is crucial for developing our understanding of sustainable yields and to operationalize Ecosystem Based Fisheries Management (EBFM). We investigated the effect of environmental variables and fishing on the relative abundance inferred from catch-per-unit-effort (CPUE), of twelve demersal stocks (i.e., cod, haddock, whiting, anglerfish, hake, megrim, plaice, sole, lesser-spotted dogfish, spurdog, Trisopterus spp., skates and rays) in the Celtic Sea from 1997 to 2019 (23 years). Annualized time series (1997-2019) of net primary production, bottom temperature, copepod abundance (Calanus finmarchicus and Calanus helgolandicus) and North Atlantic Oscillation index were used to characterize key environmental variables. Fishing exploitation rates (F/FMSY) were used to represent fishing pressure and CPUE trends derived from an International Bottom Trawl Survey (IBTS) were used to infer abundance. We used redundancy analysis to identify key explanatory variables and then dynamic factor analysis to assess their relationships with the CPUE series and identify underlying patterns in the unexplained temporal variation. Our results show that for the majority of demersal fish species, the CPUE trends were strongly influenced by fishing exploitation rates. The gradual reduction in exploitation rates observed throughout the study period most likely led to the partial recovery of cod, spurdog, hake, megrim, plaice, whiting, Trisopterus spp., and the skates and rays. In addition, exploitation patterns on one stock influenced CPUE trends of other demersal stocks (e.g., hake, megrim, plaice, lesser-spotted dogfish, sole). We also observed that the CPUE of whiting, hake and plaice increased when C. finmarchicus were abundant in the plankton. We infer from our findings in the investigated time series that the recovery of cod, spurdog, hake, megrim, plaice, whiting, Trisopterus spp., and the skates and rays in the Celtic Sea remains dependent on controlling fishing mortality, and this would not, at least for now, be confounded by the environmental conditions.
... The Atlantic herring Clupea harengus Linnaeus 1758 is a key species in the Northern Atlantic Ocean (Blaxter & Hunter 1982). It constitutes a major food source for predators, such as cod Gadus morhua Linnaeus 1758, and therefore is of great importance for the respective food webs (Blaxter & Hunter 1982;Link et al., 2009). Furthermore, it is heavily targeted by the fishery industry and has been ranked fourth amongst the most caught species worldwide (FAO 2020). ...
Article
The Atlantic herring Clupea harengus is a small pelagic schooling fish belonging to the Clupeiformes. It constitutes a key species for fisheries and marine ecosystems of the Northern hemisphere. Due to its key importance for fishery several studies refer to the larval development of C. harengus and aim to further understand its reproductive biology. However, not much is known about the skeletal development of herring larvae. This study describes the axial skeleton development of Western Baltic herring. Cartilage and bone formation were traced by clearing and double staining herring larvae with a size spectrum of 6–35 mm. During the yolk-sac phase, the caudal fin starts to differentiate. Then, in the next phase the dorsal fin develops, followed by notochord flexion and anal fin formation. After a phase of pelvic fin development, the transition to the juvenile fish starts. The development of herring is compared to other clupeiforms, especially Alosa sapidissima, Engraulis japonicus and Sardinops melanostictus, for which information was available, and to previous research on herring larvae.
... Given these food-web links, demersal fish recovery would therefore likely negatively impact the present shellfish industries. Studies have shown that large aggregations of cod and shrimp don't coexist in this ecosystem, with increases associated with decreases in the other [3,4,[123][124][125]. This interaction is exacerbated by each species favoring differing environmental conditions such as ocean temperatures [4,[126][127][128][129][130]. ...
Article
Spatial heterogeneity in food web structure and interactions may reconcile spatial variation in population and community dynamics in large marine ecosystems. In order to assess food web contributions to the different community recovery dynamics along the Newfoundland and Labrador shelf ecosystem, we quantified species interactions using stable isotope mixing models and food web metrics within three sub-regions. Representative samples of each species caught in trawls and plankton tows were analyzed for stomach contents and stable isotope ratios (δ15N and δ13C) to parameterize isotope mixing models. Regional variation, highlighted by the diets of three economically important species, was observed such that the southern region demonstrated a variety of trophic pathways of nutrient flow into the higher food web while the diets of fish in the northern regions were typically dominated by one or two pathways via dominant prey species, specifically shrimp (Pandalus sp.) and hyperiids. Food web metrics indicated that the low-diversity northern regions had higher connectance and shorter food chain lengths. This observed regional variation contributes to our understanding of the role of specific forage species to the ecosystem which is an essential contribution towards ecosystem-based management decisions.
... In particular, the Barents Sea holds the largest Atlantic cod (Gadus morhua, Gadidae) stock in the world (Kjesbu et al., 2014) the Northeast Arctic (NEA) cod. NEA cod play a dominant role in the Barents Sea ecosystem as important predators due to their high abundance, wide distribution, long migrations and generalist feeding habits, which influence practically all trophic links (Link et al., 2009). NEA cod also consume a very wide range of food items and can switch to prey that are more abundant in a given season and area (Jakobsen & Ozhigin, 2011). ...
Article
Full-text available
It is commonly accepted that no ecosystem model is the ‘best’, but rather that ecosystem models should be used in ensembles. This is also the case for the Barents Sea ecosystem, where we have used two different ecosystem models to explore the role of the top‐predator Northeast Arctic (NEA) stock of Atlantic cod (Gadus morhua, Gadidae) in the food web. The two models differ in complexity; Gompertz being less complex in terms of food web (7 components) and processes compared to the complex Nordic and Barents Seas Atlantis model (53 components). On the other hand, Gompertz provides thousands of stochastic realizations for each scenario, whereas Atlantis provides only one deterministic simulation. To compare the response to changes in NEA cod on two key prey species, capelin (Mallotus villosus, Osmeridae) and polar cod (Boreogadus saida, Gadidae), we perturbed the historical fishing pressure by ±50% and used the same NEA cod biomass in both models. Even though the links between NEA cod and the prey species are similar in the two models, the results from the study reveal that indirect effects through other food‐web components might be as important as direct predator–prey interactions. Differences in spatial structure and overlap between species also influence the species response to the perturbations. In this study, we focus on the mechanisms that drives the changes in the models, and advise on potential consequences for fisheries management. The two models can complement each other, and the differences between them point to areas where more knowledge is needed.
... Our findings support this trend, with nearly 75% of all herring collected belonging to the fall-spawning component. The adaptive capacity of herring potentially explains why herring stocks in Newfoundland did not collapse with capelin and groundfish stocks in the early 1990 s (Hutchings and Myers, 1994;Link et al., 2009). However, climate warming may lead to an overall reduction or loss of herring phenotypic plasticity as spring-spawning sub-populations decline in abundance (Melvin et al., 2009). ...
Article
Full-text available
Atlantic herring (Clupea harengus; hereafter herring) is a forage fish that transfers energy from lower to higher trophic levels and sustains high-volume fisheries in the North Atlantic. This study aims to improve our understanding of the ecology of Newfoundland herring and its vulnerability to climate change by identifying key prey items and describing adult herring feeding strategies. We compared plankton assemblages to stomach content and stable isotope analyses from herring collected in Trinity Bay, Newfoundland, in late summer and autumn 2017-2019. Six distinct zooplankton communities were identified across all years, with a shift in community structure in September 2018. This shift coincided with a change from fresher, warmer waters (12-17 • C) to more saline, cooler waters (10.5 • C). The most frequently consumed prey items were amphipods (Themisto spp.) and calanoid copepods (primarily Calanus and Temora spp.). Fish eggs, larvae, and juveniles, primarily identified as capelin, were observed in stomach contents in all years. Fish contributed most to diets in 2017, which corresponded with the peak year for larval densities in Trinity Bay, suggesting that piscivory may increase at higher larval densities. Herring were opportunistic feeders, although some individuals exhibited selective feeding on copepods, amphipods, euphausiids, and the early life stages of fishes. Stable isotope analyses supported the finding that herring piscivory is prevalent in eastern Newfoundland. Given its adaptive feeding strategy and wide range of consumed prey, we conclude that adult Newfoundland herring is resilient to bottom-up changes observed in the environment.
... However, their interactions have been little studied (Johannesen et al., 2012). As an adult, cod is a predator of haddock juveniles in the Barents Sea as the weight proportion of haddock in the cod diet is about 6%-14% (ICES, 2008;Link et al., 2009). Predation on haddock juveniles by cod might affect the survival of young haddock; nonetheless, the absolute effect has not been estimated (ICES, 2008;Olsen et al., 2010). ...
Article
Full-text available
Climate change and harvesting can affect the ecosystems' functioning by altering the population dynamics and interactions among species. Knowing how species interact is essential for better understanding potentially unintended consequences of harvest on multiple species in ecosystems. I analyzed how stage-specific interactions between two harvested competitors, the haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua), living in the Barents Sea affect the outcome of changes in the harvest of the two species. Using state-space models that account for observation errors and stochasticity in the population dynamics, I run different harvesting scenarios and track population-level responses of both species. The increasing temperature elevated the number of larvae of haddock but did not significantly influence the older age-classes. The nature of the interactions between both species shifted from predator-prey to competition around age-2 to -3. Increased cod fishing mortality, which led to decreasing abundance of cod, was associated with an increasing overall abundance of haddock, which suggests compensatory dynamics of both species. From a stage-specific approach, I show that a change in the abundance in one species may propagate to other species, threatening the exploited species' recovery. Thus, this study demonstrates that considering interactions among life history stages of harvested species is essential to enhance species' co-existence in harvested ecosystems. The approach developed in this study steps forward the analyses of effects of harvest and climate in multi-species systems by considering the comprehension of complex ecological processes to facilitate the sustainable use of natural resources.
... These stocks often settle to bottom habitat that is already inhabited by older conspecifics. Furthermore, most demersal stocks feed on larger items than pelagic fish of the same size, which allows them to be opportunistic cannibals (Bogstad et al., 1994;Link et al., 2009;Uzars & Plikshs, 2000). Pelagic fish often school together with individuals of similar size (Hoare et al., 2000), thereby effectively limiting the interaction between adults and juve- F I G U R E 5 20-year moving window analyses of correlation coefficients between early growth and cohort abundance. ...
Article
Full-text available
The correct prediction of the shape and strength of density dependence in productivity is key to predicting future stock development and providing the best possible long‐term fisheries management advice. Here, we identify unbiased estimators of the relationship between somatic growth, recruitment and density, and apply these to 80 stocks in the Northeast Atlantic. The analyses revealed density‐dependent recruitment in 68% of the stocks. Excluding pelagic stocks exhibiting significant trends in spawning stock biomass, the probability of significant density dependence was even higher at 78%. The relationships demonstrated that at the commonly used biomass limit of 0.2 times maximum spawning stock size, only 32% of the stocks attained three quarters of their maximum recruitment. This leaves 68% of the stocks with less than three quarters of their maximum recruitment at this biomass limit. Significantly lower recruitment at high stock size than at intermediate stock size was seen in 38% of the stocks. Density dependence in late growth occurred in 54% of the stocks, whereas early growth was generally density‐independent. Pelagic stocks were less likely to exhibit density dependence in recruitment than demersal and benthic stocks. We recommend that both the degree to which productivity is related to density and the degree to which the relationship changes over time should be investigated. Both of these aspects should be considered in evaluations of whether sustainability and yield can be improved by including density dependence in forecasts of the effects of different management actions.
... Atlantic cod is considered a major predator of herring (Hamre, 1988(Hamre, , 1994Link et al., 2009), particularly for the juvenile stage (de Barros & Toresen, 1998;Johansen et al., 2004), and we thus expected to observe a negative effect on herring population. However, we only observed, albeit not significantly, a negative effect of cod on herring after the herring collapse. ...
Article
Full-text available
Both the Norwegian Spring Spawning herring (Clupea harengus) and the Northeast Arctic (NEA) cod (Gadus morhua) are examples of strong stock reduction and decline of the associated fisheries due to overfishing followed by a recovery. Cod and herring are both part of the Barents Sea ecosystem, which has experienced major warming events in the early (1920–1940) and late 20th century. While the collapse or near collapse of these stocks seems to be linked to an instability created by overfishing and climate, the difference of population dynamics before and after is not fully understood. In particular, it is unclear how the changes in population dynamics before and after the collapses are associated with biotic interactions. The combination of the availability of unique long-term time series for herring and cod makes it a well-suited study system to investigate the effects of collapse. We examine how species interactions may differently affect the herring and cod population dynamic before and after a collapse. Particularly we explore, using a GAM modeling approach, how herring could affect cod and vice versa. We found that the effect of cod biomass on herring that was generally positive (i.e., covariation) but the effect became negative after the collapse (i.e., predation or competition). Likewise a change occurred for the cod, the juvenile herring biomass that had no effect before the collapse had a negative effect after. Our results indicate that the population collapses may alter the inter-specific interactions and response to abiotic environmental changes. While the stocks are at similar abundance levels before and after the collapses, the system is potentially different in its functioning and may require different management action.
Article
Full-text available
Toxicity mediated by per- and polyfluoroalkyl substances (PFAS), and especially perfluoroalkyl acids (PFAAs), has been linked to activation of peroxisome proliferator-activated receptors (Ppar) in many vertebrates. Here, we present the primary structures, phylogeny, and tissue-specific distributions of the Atlantic cod (Gadus morhua) gmPpara1, gmPpara2, gmPparb, and gmPparg, and demonstrate that the carboxylic acids PFHxA, PFOA, PFNA, as well as the sulfonic acid PFHxS, activate gmPpara1 in vitro, which was also supported by in silico analyses. Intriguingly, a binary mixture of PFOA and the non-activating PFOS produced a higher activation of gmPpara1 compared to PFOA alone, suggesting that PFOS has a potentiating effect on receptor activation. Supporting the experimental data, docking and molecular dynamics simulations of single and double-ligand complexes led to the identification of a putative allosteric binding site, which upon binding of PFOS stabilizes an active conformation of gmPpara1. Notably, binary exposures of gmPpara1, gmPpara2, and gmPparb to model-agonists and PFAAs produced similar potentiating effects. This study provides novel mechanistic insights into how PFAAs may modulate the Ppar signaling pathway by either binding the canonical ligand-binding pocket or by interacting with an allosteric binding site. Thus, individual PFAAs, or mixtures, could potentially modulate the Ppar-signaling pathway in Atlantic cod by interfering with at least one gmPpar subtype.
Article
Full-text available
In this study, a multispecies gadget model (GadCap) simulating the interactions between the Flemish Cap cod Gadus morhua, redfish Sebastes sp. and shrimp Pandalus borealis has been incorporated as the operating model in a Management Strategy Evaluation (MSE) framework (a4a-FLR), to test the performance of multiple combinations of HCRs for the three stocks when recruitment uncertainty and assessment error are accounted for. The results indicate that due to the strong trophic interactions, it is not possible to achieve the precautionary exploitation of all the stocks at the same time. Maintaining shrimp biomass above the limit reference point (Blim) would require unsustainable fishing pressure on cod and redfish to reduce predation mortality. In contrast, maintaining cod biomass above Blim would involve high predation on and high risk of collapse of the shrimp and redfish stocks. The implementation of alternative two-stage HCRs would reduce predation, resulting in higher productivity and lower probability of collapse for cod and redfish. The results of this study support the need of accounting for species interactions when designing management strategies for a group of interdependent commercial stocks.
Article
Full-text available
Ecological studies were carried out during spring (mainly April-May), summer (June-July) and autumn (August-September) in 1993 and 1994. Four small-type whaling vessels were chartered for operations in four selected sub-areas in Norwegian and adjacent waters. To ensure random sampling of whales, stringent sampling procedures were applied. Results from forestomach analyses indicate a diet where fish play a prominent role during most of the season. Statistical analyses of potential prey preferences indicate a preference for herring Clupea harengus and capelin Mallotus villosus. Given the opportunity to choose, it appears that minke whales will generally favour these two prey species before other species such as krill Thysanoessa spp. and gadoid fish species.
Article
The collapse of northern cod, Gadux morhua, off Newfoundland and Labrador was associated with clearly defined spatial and temporal changes in density and biomass. Between 1981 and 1992, low density research survey tows (<100 kg/tow) increased gradually from 76 to 97% concomitant with a gradual decline in medium density tows (100 500 kg/tow) from 22 to 2%. By contrast, high density tows (>500 kg/tow) remained proportionately constant (~1.5%) until 1992, whereafter they declined to zero. Southward, spatio-temporal changes in stock biomass were unaccompanied by a shift in cod distribution. A simple density composition model provides a biological basis for observed changes in mobile and fixed-gear catch rates, increased catchability of cod with declining stock biomass, and rapid increases in fishing mortality. A nested aggregation model of a small, constant number of dense cod aggregations, each encompassed by, and recruited from, lower density areas, explains how cod vulnerability to fishing can increase with declining stock biomass. A review of recent research identifies excessive fishing mortality as the sole significant cause of northern cod's collapse. Prevention of fishery collapses arguably rests on the dominant question to emerge from this review: what are the effects of fishing on the behaviour, life history, and population biology of exploited fishes?.
Article
Cod (Gadus morhua) on the Banks of Newfoundland have supported one of the world's greatest fisheries for almost 500 years. The fishery has been in decline since the 1960's, and collapsed totally in 1990-91. Using a retrospective monitoring approach, we examined the demersal fish community on the Northeast Newfoundland/Labrador Shelf over the period leading up to the collapse (1978-1991). The study shows that most species, not just the commercial ones, have declined in abundance. Assemblages identified in particular areas showed spatial persistence prior to 1987, but afterwards (and accompanying the stock collapse) their distribution patterns changed markedly on the shelf. In addition to declines in number and biomass, many species showed a significant decrease in average size. Intense and unrelenting fishing pressure seems to have been the prime agent, and the time scale of change has been shorter than the lifespan of the fish involved. While the decline in biomass has produced severe social and economic problems, the fundamental change in the age structure suggested by the decreases in average size may be more serious in the longer term; evidence for this is seen in the fact that, even with a moratorium in effect, the cod stock has continued to decline and has now reached commercial extinction. We conclude that human predation has become a very powerful element in marine ecosystems, and therefore scientific studies relating to exploited fish communities must explicitly include human activities and perceptions in ecosystem analyses.