Chapter 3 Effects of Climate Change and Commercial Fishing on Atlantic Cod Gadus morhua

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From: Nova Mieszkowska, Martin J. Genner, Stephen J. Hawkins, and David W. Sims, Effects of Climate Change and Commercial Fishing on Atlantic Cod Gadus morhua.

In D. W. Sims, editor: Advances in Marine Biology, Vol. 56, Burlington: Academic Press, 2009, pp. 213-273.

ISBN: 978-0-12-374960-4 © Copyright 2009 Elsevier Ltd.

Academic Press.

Author’s personal copy

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Effects of Climate Change and

Commercial Fishing on Atlantic

Cod Gadus morhua

Nova Mieszkowska,* Martin J. Genner,*,† Stephen J. Hawkins,*,‡

and David W. Sims*,§

Contents

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Marine Biology, Volume 56 # 2009

-2881, DOI: 10.1016/S0065-2881(09)56003-8 All rig

iological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouingdomf Biological Sciences, University of Bristol, Bristol BS8 1UG, United Kingdomf Natural Sciences, Memorial Building, Bangor University, Gwynedd LL57 2UW,ingdomiology and Ecology Research Centre, School of Biological Sciences, University of Plrcus, Plymouth PL4 8AA, United Kingdom

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1
.1. B asic biology and global distribution 215
1
.2. G enetic population structure 216
1
.3. T raits in different stocks 218
1
.4. M ovement and activity 219
2. Im
pacts of Climate Change 222
2
.1. B iogeographic changes 224
2
.2. P hysiology 226
2
.3. M etabolic scope for activity 229
2
.4. M aturation and spawning 230
2
.5. E arly life stages 231
2
.6. R ecruitment 233
2
.7. G rowth 237
3. Im
pacts of Fishing 238
3
.1. N orthwest Atlantic stocks 238
3
.2. N ortheast Atlantic stocks 239
3
.3. T he fishing versus climate change debate 244
4. P
opulation-Level Impacts of Fishing and Climate Change 245
4
.1. S tock assessment 245
4
.2. S tock evaluation—An example from the North Sea 246
4
.3. A llee effects and management plans 247
5. M
onitoring Status and Recovery of North Sea Cod: A Case Study 249
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214 Nova Mieszkowska et al.


6. C
oncluding Remarks 250
Ackn
owledgements 252
Refe
rences 252
Abstract

During the course of the last century, populations of Atlantic cod Gadus

morhua L. have undergone dramatic declines in abundance across their biogeo-

graphic range, leading to debate about the relative roles of climatic warming

and overfishing in driving these changes. In this chapter, we describe the

geographic distributions of this important predator of North Atlantic ecosys-

tems and document extensive evidence for limitations of spatial movement and

local adaptation from population genetic markers and electronic tagging. Taken

together, this evidence demonstrates that knowledge of spatial population

ecology is critical for evaluating the effects of climate change and commercial

harvesting. To explore the possible effects of climate change on cod, we first

describe thermal influences on individual physiology, growth, activity and

maturation. We then evaluate evidence that temperature has influenced popu-

lation-level processes including direct effects on recruitment through enhanced

growth and activity, and indirect effects through changes to larval food

resources. Although thermal regimes clearly define the biogeographic range of

the species, and strongly influencemany aspects of cod biology, the evidence that

population declines across the North Atlantic are strongly linked to fishing activity

is now overwhelming. Although there is considerable concern about low spawning

stock biomasses, high levels of fishing activity continues in many areas. Even with

reduced fishing effort, the potential for recovery from low abundance may be

compromised by unfavourable climate and Allee effects. Current stock assess-

ment and management approaches are reviewed, alongside newly advocated

methods for monitoring stock status and recovery. However, it remains uncertain

whether the rebuilding of cod to historic population sizes and demographic

structures will be possible in a warmer North Atlantic.

1. Introduction

Atlantic cod Gadus morhua Linnaeus, 1758 is one of the most widelystudied marine fishes (Fig. 3.1). The species is a major predator in NorthAtlantic ecosystems as well as being a prey item for larger fishes and piscivo-rous marine mammals. It has been exploited as a human food resource forover 1000 years and forms a key component of major fisheries throughout theNorth Atlantic. Its pivotal ecological role, together with its economic impor-tance, has made it a model system for study among marine fishes. Studiesrange from individual physiology, to population ecology, community inter-actions and responses to environmental change, including climate change andfishing. Here, we review these studies and discuss how key aspects of cod

Figure 3.1 Atlantic cod, Gadus morhua Linnaeus 1758. Photograph courtesy of theMarine Biological Association of the UK.

Climate and Fishing Effects on Cod 215


biology are likely to be influenced by changing environments, such as thoseassociated with changes in fishing pressure and climate. We examine theimpacts of these drivers on the current status and potential for future recoveryof stocks, with a focus on the North Sea and evaluate potential managementstrategies to reverse the current global decline in Atlantic cod.

1.1. Basic biology and global distribution

Atlantic cod is an apex predator of North Atlantic continental shelf waters.It feeds mainly on invertebrates and fish. It grows to a maximum of 2 m intotal length, weighs up to 96 kg, matures at between 2 and 4 years of age(O’Brien et al., 1993) and can live for up to 25 years. Females are typicallyhighly fecund, producing an average of 1 million eggs per individual(Cohen et al., 1990). Spawning takes place between December andJune depending on geographic location, and eggs hatch 2–3 weeks later.The pelagic larvae feed on zooplankton for approximately 2 months beforesettling on demersal nursery grounds.

The biogeographic range of cod, like many marine fish species, isprimarily governed by temperature (Coutant, 1987; Sundby, 2000). In theNorth Atlantic Ocean, it is found between 40 and 80 �N over a tempera-ture gradient of �1 to 20 �C. Northern limits occur in Canada and Iceland,and southern limits are reached around New England in the westernAtlantic, and in the Celtic Sea–English Channel in the eastern Atlantic(Fig. 3.2). Key areas of population abundance are Labrador, Newfoundland,southern Greenland, Iceland, the North Sea, the Baltic Sea and the BarentsSea (Bigg et al., 2008; Sundby, 2000). Its depth range extends from shallowwaters to 200 m, although it has been recorded at depths of over 500 m(Cohen et al., 1990).

90�W 60�W 30�W

90�W

60�N

40�N

60�N

40�N

60�W 30�W 0�

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Figure 3.2 The distribution of Atlantic cod in the North Atlantic Ocean (greyshaded area).



1.2. Genetic population structure

Cod live in a diverse and complex marine landscape with contrasting watertemperatures, depths, salinities, substrates and prey availability. In manymarine species, habitat discontinuities can act as barriers to gene flow byrestrictingmovement of adults or larvae (Hauser andCarvalho, 2008).Geneticdifferences between populations can be further promoted by behaviouraltraits, such as adult philopatry, population-specific migratory behaviour orkin aggregation (Pardini et al., 2001). The formation of genetic substructurewill, however, be counteracted to some extent by the capability that adultfishes have to range over long stretches of coastline and open water, and thepelagic dispersal of eggs and larvae (Hauser and Carvalho, 2008).

Identification of geographic and behavioural barriers to gene flow iscritical for stock identification and management. Cod are very patchilydistributed across their range (�7300 km), and molecular markers havehelped to reveal the extent of migration among populations. Several studieshave revealed a broad spatial trend of isolation-by-distance across the NorthAtlantic. In mitochondrial DNA, despite an apparent lack of nucleotidediversity (Arnason and Palsson, 1996), there are large differences in thefrequency of common haplotypes (Arnason, 2004; Carr and Crutcher,1998). Similar patterns have been revealed using restriction fragments ofnuclear genes (Pogson et al., 1995, 2001), and nuclear microsatellite markers(Hutchinson et al., 2001; O’Leary et al., 2007; Pampoulie et al., 2008;Skarstein et al., 2007). The extent of population differences in microsatelliteallele frequencies are such that cod can be reliably assigned to the Baltic Sea,North Sea and the Northeastern Arctic Ocean on the basis of theirgenotypes alone (Nielsen et al., 2001).



1.2.1. Cod population persistenceNearly all studies making temporal comparisons of cod population structureusing archived genetic material have found remarkable stability (Imslandet al., 2004; Jonsdottir et al., 1999, 2001; Lage et al., 2004; Nielsen et al.,2001; Pampoulie et al., 2008). A major change in genetic diversity was,however, found in the heavily fished Flamborough Head population in theNorth Sea between 1954 and 1970. After the decline observed over thisperiod, diversity subsequently increased, and this has been linked to theincursion of new genotypes as new colonists had proportionally greaterreproductive success (Hutchinson et al., 2003). The general natural stabilityof cod populations, however, implies that the present distribution of geneticdiversity has changed little over recent time. Bigg et al. (2008) concludedthe present distribution of cod dates back more than 100,000 years, but bycontrast, using more rapidly evolving microsatellite markers, Pampoulieet al. (2008) calculated the time scale of divergence dates more closely tothat of the Last Glacial Maximum, approximately 20,000 years ago.Although the accuracy of these time scales will depend on methods usedto calibrate evolutionary rates, together these results suggest that the largerscale distribution of genetic diversity pre-dates the last northern hemisphereglacial cycle.

1.2.2. Regional patterns of genetic diversityUsing microsatellite DNA markers, patterns of isolation-by-distance havebeen revealed over spatial scales of approximately 1000–2000 km (Beachamet al., 2002; O’Leary et al., 2007). At smaller scales (<1000 km), however,the extent of stock structure appears closely linked to environmental para-meters and behavioural differences. For example, genetic structure withinthe Northwest Atlantic has been linked to habitat discontinuities, such aschannels and trenches. Lage et al. (2004) found cod on the southernNantucket shoals to be genetically distinct from those on the neighbouringmore northerly offshore Browns Bank and Georges Bank, but there wereno genetic differences apparent between Browns Bank and Georges Bank,despite these being separated by a stretch of deep water that likely acts as abarrier to movement of adult cod (Lage et al., 2004). Here, it is likely that agyre system leads to retention of eggs and larvae on the two offshore banks,but those spawned on the Nantucket shoals do not enter this gyre and areeither retained locally, or are transported southwest. This evidence iscompatible with both larval dispersal and adult habitat fidelity-determiningspatial patterns of genetic diversity (Ruzzante et al., 1998, 1999).

There are several other examples where substantial genetic differenceshave been identified within regions. Populations in the Canadian Arcticsaltwater lakes at the extreme northwest of the species range are stronglygenetically differentiated from Atlantic populations, and show much lower



genetic diversity (Hardie et al., 2006). This evidence is consistent with along period of genetic isolation linked to a habitat barrier. Similarly, strongpatterns of genetic differences have been found between populations in theNorth Sea and the Baltic Sea (Nielsen et al., 2003). In this case, a zone ofadmixture is flanked at each side by non-admixed populations (Nielsenet al., 2003, 2006); this pattern is associated with local adaptation fordiffering salinity regimes. Such extreme population structuring is not alwayscommon within regions, and weak genetic structuring, or genetic homo-geneity, are more typical results of studies employing neutral markers atspatial scales around 1000–2000 km (e.g. Beacham et al., 2002). In somecases, genetic differences between populations have been recovered, butthey are not always directly correlated with known environmental condi-tions or geographic distances. On the northern coast of Norway, forexample, coastal cod have clear spatial genetic structure, but no evidenceof isolation-by-distance ( Jorde et al., 2007). In this case, it would appearthat gradual adult or larval dispersal is unlikely, and instead spatial structurehas formed through sporadic colonization waves of genetically similarindividuals.

The existence of co-occurring populations that are geneticallysegregated has also become apparent. In Norway, there are differencesin otolith shapes between the Arctic offshore cod that overwinter inthe warmer, deeper waters, and the coastal inshore cod that overwinter inthe cooler, shallower water, and early genetic work found that theseoffshore and inshore cod possessed adaptive differences in their haemoglo-bin HBI allele frequency (M�ller, 1966). In the North Sea–Skagerrak areathere is also evidence that the migratory-offshore North Sea stock and thenon-migratory-coastal Skagerrak stock are genetically different, but simi-larly co-occur within inshore waters (Case et al., 2005). Genetically differ-ent offshore migratory and inshore overwintering cod are also present inNewfoundland (Ruzzante et al., 1996a,b), and have been found to differ intheir blood ‘antifreeze’ protein levels, with the inshore cod that experiencethe cooler winter temperatures possessing higher antifreeze protein concen-trations. These genetic differences appear to exhibit interannual stability(Ruzzante et al., 1997, 2000).

1.3. Traits in different stocks

There is an increasing body of evidence suggesting that genetically differentcod stocks differ in adaptive life history traits. In the Skagerrak, wherepopulation structure is apparent at a scale of less than 100 km, there isapparent spatial variability in traits, such as juvenile growth rate that corre-sponds with observed genetic variation (Olsen et al., 2008). In support of anevolutionary explanation for the observed pattern, a range of molecular andbreeding studies have revealed evidence for selection on functional genes.



Several genes show variation at the stock level (Hutchinson, 2008), perhapsthe most studied gene in this context is pantophysin (PanI) (Pogson et al.,2001), formerly synaptophysin (Syp I) (Fevolden and Pogson, 1997). Par-ticular life history traits have been associated with this gene, for example,differences in mean weight, length and growth rates have been shown to bedependent on the PanI genotype around Iceland ( Jonsdottir et al., 2002,2003), and temperature and salinity have been shown to influence the PanIgenotype frequency in the Northeast Atlantic (Case et al., 2005). These fieldresults have been supported by ‘common garden’ experiments showingPanI-dependent differences in growth rate and condition factor of indivi-duals reared to 10 weeks. Although these results may be due to genes linkedto the PanI (Case et al., 2006), the pattern nevertheless suggests that stronglocal adaptation of stocks is present in the natural environment.

1.4. Movement and activity

The movement and activity patterns of predatory fish such as Atlantic codcan be considered a major driver of the spatio-temporal dynamics ofpopulations and communities within ecosystems. Movements such asmigration, dispersal and regional philopatry, when played out over longertemporal scales, not only contribute to observed patterns of populationsub-structuring and connectivity, but will also determine how populationdistribution responds to drivers of climatic change or fishing pressure. Moni-toring movements of cod in relation to environment is therefore relevant tounderstanding the effects of these drivers on cod population re-distributions,with a significant role in future adaptive management regimes.

1.4.1. Adult movementsEarly mark-recapture studies, fishery surveys and fishing reports informed ageneral picture of mature cod annual movements, with migration to spawninggrounds followed by spent cod returning to their feeding grounds afterspawning (Harden Jones, 1968). Although this general model is broadlyapplicable to cod, the emerging paradigm is that their movements bygeographic location and by season are complex, with marked differencesin behaviour even within a region such as the North Sea, for example(Hobson et al., 2007). The recent advances in remote telemetry technologyfor tracking fish, particularly the miniaturization of data-loggers, has enabledthese insights (Arnold and Dewar 2001; Sims, 2008) with adult cod move-ments and activity being recorded over long time periods (>1 year) innearly all the main regions within its geographic range (Clark and Green,1990; Cote et al., 2003; Metcalfe, 2006; Neat and Righton, 2006; Neatet al., 2006; Rillahan et al., 2009; Robichaud and Rose, 2001, 2002, 2003,2004; Steinhausen et al., 2006; Wright et al., 2006). Data-logging storagetags have been attached to cod and used to obtain regionally explicit,



individual-based data on horizontal and vertical movements and thermalhabitat. These studies support the contention that there is not a singleparadigm of extended movement between spawning and foraging areas, asgenerally supposed previously (e.g. Harden Jones, 1968), but rather thatsuch movements vary from individual to individual and from sub-stock tosub-stock (Hobson et al., 2009). Behavioural plasticity is evident for cod inthe extent and timing of migration, in the persistence of spawning orfeeding site fidelity (philopatry), and also in relation to the types of beha-viour displayed on feeding grounds and where and when they occur in thewater column compared with remaining close to the seabed (Hobson et al.,2007, 2009; Neat et al., 2006; Palsson and Thorsteinsson, 2003; Rightonet al., 2001).

Residence and homing behaviour have been shown to be importantfeatures of Atlantic cod behaviour (Hobson et al., 2009). Cod are known toaggregate seasonally to spawn and to feed at particular geographic locations(Metcalfe, 2006). For example, spawning area fidelity shown by aggrega-tions representing more or less distinct groups of fish is a behavioural traitsupported by at least some evidence from genetic and mark-recapturestudies (Metcalfe, 2006). However, the degree to which residence andhoming applies to different populations and to sub-stocks has been foundto vary greatly depending on geographic location. Robichaud and Rose(2004) proposed four categories of populations of Atlantic cod based on thedegree of migration and philopatry. The latter authors identified ‘sedentaryresidents’ that exhibit site fidelity year round, ‘accurate homers’ that returnto spawn in a specific area, ‘inaccurate homers’ that home to a much broaderarea around the original tagging location in the following years, and‘dispersers’ that move and spawn in a more irregular pattern within largegeographical areas (Metcalfe, 2006). It seems coastal areas support residentpopulations more commonly, such as those in the Norwegian fjords, theIcelandic coast and the Canadian east coast (Metcalfe, 2006), whereas theNortheast Atlantic has large subpopulations that home with accuracy com-pared with the Northwest Atlantic that has more inaccurate homers anddispersers (Metcalfe, 2006; Robichaud and Rose, 2004). Nested within thislarger scale complexity, are the variations in individual patterns observedwithin a region and which exemplify the problem with broad categorisationof cod behaviour.

Comprehensive studies of cod movements in the Northeast Atlantichave deployed over 3000 electronic tags in the Barents Sea, the North Sea,the Baltic Sea and on the Icelandic and Faroe Plateau between 2002 and2005, with over 850 tags returned by fishermen, giving more than 130,000days of data (www.codyssey.co.uk). In the North Sea, for example, it ispossible to link horizontal with vertical movement patterns. For individualtracks ranging in duration from 40 to 468 days, cod showed horizontalmovements up to 455 km, however, individuals did not always show signs

http://www.codyssey.co.uk



of migration during winter months, even displaying continuous localisedresidence for up to 360 days (Hobson et al., 2009). This indicates that cod donot always migrate between feeding and spawning grounds. Vertical move-ments showed even greater flexibility, with a variety of movement patternsseen within both periods of residence and directed horizontal movement.Close association with the seabed was seen during both directed horizontalmovements and residency, while midwater oscillations in swimming depthwere also evident during both horizontal movement types. Therefore,vertical patterns in activity alone could not be used to reliably define periodsof migration or localised residence (Hobson et al., 2009). Taken together,the results from studies that have tracked large numbers of individual cod forlong periods suggest that Atlantic cod behaviour is mediated by complexinteractions between biological and ecological factors that result in diversemovements and activities in relation to changing environment (Hobsonet al., 2009; Righton et al., 2001).

1.4.2. Cod thermal habitsElectronic tagging data show that cod occupy depths from 10 to 860 m, andwater temperatures of�1.5 �C in polar fronts off Iceland and in the BarentsSea, to 21 �C when resting on the seabed in the southern North Sea.In terms of cod distributional responses to thermal habitat, such studiesreport, for example, that northern North Sea populations above 57 �Ndo not intermix with southern populations below 56 �N (Neat andRighton, 2007), thus concurring with previous mark-recapture pro-grammes (Righton et al., 2007; Robichaud and Rose, 2004; Wright et al.,2006) and genetic studies (Hutchinson et al., 2001). Within the northernNorth Sea, west Shetland is the warmest and least variable region (<3 �Cvariation) and no cod movement from here to cooler waters has beenrecorded. By contrast, cod released back into the east Shetland and VikingBank populations moved rapidly into cold fronts and prolonged occupancyof cooler waters was recorded (Neat and Righton, 2007). Within thesouthern sector of the North Sea, the German Bight population experiencesa highly variable thermal environment, with intra-annual variation of�14 �C. The greatest acute fluctuations recorded comprised a 7 �C decreaseover 3 days, and a 7 �C increase over a 2-day period. Individuals from thisregion, and the neighbouring eastern English Channel mostly migrated onlyshort distances, or remained resident, despite experiencing water tempera-tures up to 19 �C during late summer and autumn (Neat et al., 2006;Righton et al., 2001). Notably, adult cod only commenced vertical migra-tion in October–November once surface temperatures began to decline(Righton et al., 2001), and during this period some mature individuals havebeen recorded migrating to spawning grounds in the eastern English Channeland Southern Bight (Daan, 1978).



Given the complex behaviour of cod, and in relation to thermal changesand other biological and physical factors operating across the broad range oftemperatures in which it is found, predicting how individual cod willrespond to climate-driven changes in sea temperature, for example, remainschallenging.

1.4.3. Larval dispersalGenetic evidence for reproductively isolated stocks that co-occur on groundsduring non-breeding periods, but that often segregate during spawningseasons, demonstrates the importance of knowledge of spawning and nurseryhabitats for appropriate management. Tests of population genetic differencesusing adult individuals have informed us about the general patterns of spatialand temporal stock structure, but such studies convey little about the relativeimportance of spawning grounds within spatial management units. Tradi-tionally, ichthyoplankton surveys and visual identification of larval speciesidentity have been used for identification of spawning grounds. Indeed, thisapproach has allowed broad-scale mapping across its range of cod spawningareas and the general pattern of egg and larval transport (Brander, 1997).Eggs and larvae, however, can be difficult to separate visually from thoseco-occurring gadoids such as whiting (Merlangius merlangus) and haddock(Melanogrammus aeglefinus) (Fox et al., 2005). Recent developments in molec-ular genetic techniques have enabled reliable identification of cod eggs,revealing, for example, considerable overestimation of cod abundance inthe Irish Sea (Fox et al., 2005; Taylor et al., 2002). This approach has alsoallowed the identification of active spawning grounds in the North Sea(Fox et al., 2008). Importantly, these locations, including the Dogger Bank,German Bight and Moray Firth show close corroboration with spawningareas inferred from historical survey data, implying cod have well-defined,active spawning grounds that have been used by multiple generations.However, to date there is very little available information on the extent oflarval dispersal or retention in relation to these spawning grounds, or the cuesemployed for location and settlement on nursery grounds. Hydrodynamicmodels coupled with in situ ichthyoplankton surveys for model verificationoffer considerable promise for revealing mechanisms of larval dispersal orretention over large spatial scales (van der Molen et al., 2007).

2. Impacts of Climate Change

Global climate has warmed to temperatures unprecedented over thelast 1300 years. Anthropogenic inputs into the atmosphere are now recog-nised as the primary driver (IPCC, 2007). The latest model predictionsindicate that global mean surface temperature will increase by a further



1.1–2.9 �C (low emissions B1 scenario), or 2.4–6.4 �C (high emissions A1FIscenario) (IPCC, 2007). Climatic warming has been observed in marineenvironments across the North Atlantic, and appears to be of a greatermagnitude and duration than any periods in recent history (Fig. 3.3)(IPCC, 2001, 2007; Southward, 1963; Southward and Boalch, 1994;Southward et al., 1988). Marine ecosystems are already responding tothese changes in sea temperature, through polewards shifts in biogeographicranges (Beaugrand et al., 2002; Berge et al., 2005; Griffiths, 2003; Hellberget al., 2001; Mieszkowska et al., 2006, 2007; Zacherl et al., 2003), pheno-logical changes (Genner et al., 2009a; Sims et al., 2001, 2004), and throughalterations in the relative abundance of ectothermic species and the struc-turing of the communities they comprise (Barry et al., 1995; Berge et al.,2005; Genner et al., 2004, 2009b; Hellberg et al., 2001; Mieszkowska et al.,2006; Sagarin et al., 1999; Southward, 1995; Southward et al., 1988).Furthermore, there is burgeoning evidence for climate-driven effects onmarine fishes (Graham and Harrod, 2009). In this section, we explore therole of climate drivers on the biology and ecology of Atlantic cod and, inaddition to description and discussion of the known or potential biologicalimpacts, we identify knowledge gaps where new studies will progress ourunderstanding towards prediction of cod responses to changing environments.

Year

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1870 1890 1910 1930 1950 1970 1990 2010

Figure 3.3 Mean annual sea surface temperatures of the North Atlantic (weightedaverage 5��5� grid squares from 0 to 70 �N). Data derived from the National Oceanicand Atmospheric Administration Kaplan SST data set, and are available at http://www.cdc.noaa.gov/data/timeseries/AMO/.

http://www.cdc.noaa.gov/data/timeseries/AMO/





2.1. Biogeographic changes

Distributional limits of marine fish species are governed to a large extent byregional thermal regimes. The observed thermal occupancy or ‘climateenvelope’ of species is the basis for many models that attempt to predictfuture abundance and distributions (Pearson and Dawson, 2003; Waltheret al., 2002, 2005). Where environmental conditions change to fall withinthe physiological tolerance limits of a species, range extensions are predictedas fish are able to colonize new areas of suitable habitat. In practice,however, the range edge may lie some distance inside this fundamentalniche envelope. This is because population distributions are often influ-enced by additional environmental parameters and biological interactionssuch as competition, predation and prey availability, parasitism and otherfactors such as habitat availability and dispersal ability (Brett and Groves,1979; Davis et al., 1997; Kelsch and Neill, 1990). There is still no generalmodel to describe how thermal physiology of ectotherms and climateinteract to determine biogeography (Chown and Gaston, 1999; Clarke,2003). Clearly, development of such models is a significant challenge forunderstanding and predicting the macroecological responses of fish species.

Data from commercial fishing and research vessel surveys have been usedto explore how the biogeography of cod has changed (Blanchard et al.,2005; Daan, 1994). However, use of abundance data from trawl surveys canbe insensitive to short-term individual variations in distribution (Neat andRighton, 2006) which can make range assessments for spatially structuredstocks problematic (Hutchinson et al., 2001; Metcalfe, 2006; Wright et al.,2006). Both migratory behaviour and density-dependent effects linked toprey abundance can affect geographic distributions (Beaugrand et al., 2003;Blanchard et al., 2003; Moyle and Cech, 2004; Roessig et al., 2004; Swain,1999; Swain et al., 2003). Moreover, other environmental variables such assalinity, storminess, cloud cover and precipitation can strongly influence thedistribution and productivity of marine ecosystems (Bakun, 1996; Stensethet al., 2004) and the phenology of production cycles (Edwards andRichardson, 2004). The stochastic nature of these parameters is reflectedin the annual fluctuations in abundance of cod across its range.

Despite the large diversity of factors that can influence distributions,there is compelling evidence that populations have shown responses toclimate-related thermal changes during the twentieth century. The NorthAtlantic warmed at the basin-scale during the 1920s and 1930s, and duringthis warm period the distributional limits of cod were observed to extendsome 1200 km further north from southern Greenland to Disko Island(northwest Greenland), while the Barents Sea population apparently shiftedeastwards (Hansen, 1949; Jensen and Hansen, 1931). Similarly, Icelandiccod were restricted to spawning on southern shelf regions until the1920s, but afterwards spread to the northern shelf (Sæmundsson, 1934;



Vilhjalmsson, 1997). During a cool period during the 1960 and 1970s, thesechanges were seen to reverse. Cod evidently retracted further south in thecolder conditions and disappeared entirely from coastal waters around DiskoIsland (Buch and Hansen, 1988). Furthermore, the population spawning onthe northern Icelandic shelf declined to minimal levels during this period,presumably due to a shift in abundance centred further south. During thelate 1980s and early 1990s, cooler waters were also present in the NorthwestAtlantic from the Labrador Shelf to the Grand Banks, leading to a suddendecline in cod abundance (Atkinson et al., 1997; de Young and Rose, 1993;Drinkwater, 2002; Rose et al., 1994, 2000; Taggart et al., 1993).Whilst fishing activity may also have played a role in establishing this pattern(Hutchings, 1996; Hutchings and Myers, 1994b; Myers et al., 1996),analyses of blood chemistry (Rose et al., 2000) and genetics (Ruzzanteet al., 2001) also support a biogeographic shift of Northwest Atlantic stocksto lower latitudes at this time.

Apparent northward shifts of both the centre of distribution andthe southern range limit of cod in the southern North Sea in recent yearsare possibly a direct response of individuals to increased seawater tempera-ture over the last decade (Hedger et al., 2004; Perry et al., 2005; Rindorf andLewy, 2006). However, there is no direct evidence to suggest that fish haveactively moved to avoid increasing temperatures (Rindorf and Lewy, 2006).Studies supporting a northward shift in cod have based analyses on theassumption that there is single population in the North Sea that is mostabundant at the range centre, and has decreasing numbers of individualstowards range limits. For species that are more or less in a steady state, andare not changing in abundance or distribution rapidly, this pattern can bebroadly accepted. By contrast, where a single dimension of the nichechanges rapidly, and where there is evidence of population subdivisionand local adaptation, responses may not be straightforward. This may bethe case in the North Sea given some evidence that several discrete stocksare present (Hutchinson et al., 2001; Metcalfe, 2006; Wright et al., 2006),and which appear to have distinct habitat preferences during different lifehistory stages (Righton et al., 2007; Robichaud and Rose, 2004; Wrightet al., 2006). An additional consideration is that individual cod can movelarge distances or remain resident, and behaviour shows great flexibilityacross multiple spatio-temporal scales, resulting in complex spatial dynamics(see Section 1.4.1). Thus, there may not necessarily be a long-term locationfor occupation of the most suitable environmental conditions where thehighest abundance of fish can be found. The case of the North Sea is furthercomplicated by a seasonal inversion of the latitudinal temperature gradient,with the southern North Sea being colder in the winter but warmer in thesummer than the northern North Sea. Furthermore, analysis of North Searesearch survey data suggests that cod have responded to a winter bottomtemperature increase of 1.6 �C over 25 years by moving into deeper water at



an average rate of about 7 m per decade (Dulvy et al., 2008). Together, thisevidence suggests that climate-driven changes to cod distributions may bemore complex than predicted using straightforward ‘climate envelope’approaches.

Observed northward shifts of the southern range limits could also beattributed to local population abundance changes due to fishing pressure,variation in migration between populations (Hedger et al., 2004) or spatialdifferences in the thermal tolerance limits of adult cod leading to localdepletion of stocks (Neat and Righton, 2006; Portner et al., 2008). Thelack of concordant responses to thermal regimes shown by individual cod isconsistent with temperature being only one of the factors determininghabitat choice (Neat and Righton, 2006). Occupancy of space by cod inhistorical habitats has declined from 90% to lower than 50% over the last30 years, and spatial distributions have become increasingly characterized byaggregations in areas of optimal thermal habitat (Blanchard et al., 2005;Horwood et al., 2006; Marshall and Frank, 1994; Myers and Stokes, 1989;Rose and Kulka, 1999). These studies support earlier observations ofdensity-dependent habitat selection in cod (Myers and Stokes, 1989;Swain and Sinclair, 1994), and strongly suggest changing distributionsmay additionally be linked to aggregation behaviour.

2.2. Physiology

Most fish are ectotherms with limited capacity for internal heat regulation(Clarke, 1993). To predict how changes in global climate will affect fishdistributions, it is important to know how physiological functions areinfluenced by temperature variation, and to quantify thermal tolerancethresholds (Guderley, 1990; Portner, 2001, 2002; Portner and Knust,2007; Portner et al., 2001). This individual-level physiological responseextrapolates to population, community and ecosystem-level responses(Roessig et al., 2004). Although temperature is recognised as an importantcontrolling factor for biotic processes, from cellular to ecological levels oforganisation (Fry, 1971), defining thermal optima is a complex process dueto differential effects of temperature on various physiological processes, andon different life history stages. For example, larval fish drifting passivelywithin the plankton may be more vulnerable than juvenile or adult fish thatcan actively move away from unfavourable conditions. Moreover, differentstocks have also been observed to show local adaptation to differing thermalranges (Coutant, 1977, 1987; Daan, 1994; Scott, 1982).

2.2.1. Tolerance limits and thermal preferencesBoth adult and larval cod can tolerate salinities from almost 0% to 35%, butexhibit some preference for 30–35%. They also have a wide thermaltolerance, and have been recorded in waters ranging from �1.5 to 21 �C,



although their temperature range is typically between 0 and 12 �C (Trembleand Sinclair, 1985; Wise, 1961). Despite this apparent broad tolerance, theyare highly sensitive to even slight water temperature variation of �0.3 �C,and individuals seemingly alter their position in the water column tomaintain themselves near their temperature for optimal performance, Topt

(Fig. 3.4) (Herbert and Steffensen, 2005; Rose et al., 1994). Body temperaturehas a significant effect on fitness of cod (Fry, 1947; Huey and Berrigan, 2001),so Topt is expected to correspond to the temperature of maximum fitness,Trmax (Beamish, 1978; Schurmann and Steffensen, 1997). Temperature-fitness curves are asymmetric, however, and therefore body temperaturesgreater than Tmax can lead to stress and rapid fitness decline (Martin andHuey, 2008). The proximity of stressful temperatures to Trmax can result inTopt being lower than Trmax in natural, thermally variable environments. Thismay have important implications for predicting physiological fitness inresponse to future climate warming scenarios.

2.2.2. Sublethal physiological thresholdsIt may not always be possible for a fish to occupy a thermal environmentmatching the temperature of optimal performance, and thermal stress mayresult from exposure to unfavourable temperatures. The first symptoms ofthermal stress are caused by the limited capacity of respiratory systems toprovide sufficient oxygen to body tissue above the pejus temperature Tp

(pejus, meaning getting worse, deleterious) (Frederich and Portner, 2000;Portner, 2001; Portner et al., 2001). This is the threshold beyond which thecardiorespiratory system cannot increase aerobic metabolism and body

0Adult heart rate curve

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Figure 3.4 A schematic diagram of the thermal physiological thresholds of Atlanticcod. See Sections 2.2.1, 2.2.2 and 2.5 for explanations of terms and concepts.



fluids start to become hypoxic. This has been determined experimentally tobe between 13 and 16 �C in adult cod (Fig. 3.4) (Sartoris et al., 2003), andbeyond this range cardiac arrhythmia, if present, can cause a reduction inblood circulation capacity. As a consequence, this results in lower venousoxygen concentrations, onset of anaerobic mitochondrial metabolism, alter-ation of enzymatic rates (Clarke, 1993; Coutant, 1987; Fry, 1971) and asudden decrease in intracellular pH (Van Dijk et al., 1997). This in turn isaccompanied by energetic collapse in white muscle (Foster et al., 1993;Sartoris et al., 2003), reduced scope for whole organism aerobic activity and,ultimately, death at the critical temperature threshold, Tcrit (Lannig et al.,2004; Portner, 2001; Sartoris et al., 2003). Experimental data suggest thatTcrit ranges between 16.0 and 22.2 �C in adult cod populations (Gollocket al., 2006; Lannig et al., 2004; McKenzie, 1938; Portner et al., 2008;Sartoris et al., 2003) and is lower at 15.5–18.0 �C in juveniles (Perez-Casanova et al., 2008; Yin and Blaxter, 1987), although survival uponacute exposure to 20 �C has been demonstrated in controlled laboratoryconditions (Perez-Casanova et al., 2008). This variation in response may bedue to different experimental methodologies, but it could also reflect stock-specific adaptation of cod (Portner et al., 2008).

The highest partial pressure of venous oxygen in southern North Seacod held in laboratory conditions occurs at approximately 5 �C (Lanniget al., 2004), which relates closely to Topt for adult growth. The frequency ofhaemoglobin genotypes in the population can be affected by environmentaltemperature experienced by parental fish, and underlies thermal preferencesin cod (Andersen et al., 2009). Warmer water preferences are associatedwith the Hb-1 genotype (Petersen and Steffensen, 2003), with highestfrequencies of the Hb-1–1 allele found in the southern North Sea(Husebo et al., 2004; Sick, 1965), a region of some of the warmest bottomtemperatures within the cod biogeographic range (Vaz et al., 2007).Although Topt of all haemoglobin genotypes appears to be centred around14 �C ( Jordan et al., 2006), optimal oxygen extraction rates occur below12 �C (Colosimo et al., 2003), which may explain why many cod popula-tions occur in waters below this temperature.

Thermal adaptation generally optimises whole animal aerobic scope towithin a thermal range or window (Portner, 2001, 2002). However, short-term thermal acclimatisation may also allow occupation of specific thermalregimes, such as the 2–3 �C sea surface isotherm characterising the seasonalmigration highway used by cod in the Northwest Atlantic (Rose, 2004b).Evidence for seasonal acclimatisation in cod is not widespread, but hasbeen provided by laboratory trials demonstrating that the thermal limitbeyond which heart rates begin to decline can be elevated by acclimatisationto warmer temperatures (Lannig et al., 2004). This suggests that cod maybe able to buffer the effects of climate-linked sea temperature warmingsufficiently well in the short term, however, as sea temperatures continue



to rise in the region occupied, shifts in distribution may eventually takeplace that prevent exposure to temperatures beyond the pejus temperature.

2.3. Metabolic scope for activity

Metabolic rate is temperature -dependent (Claireaux et al., 2000; Lanniget al., 2004) and cod inhabiting temperate seas need to acclimatize metabol-ically to seasonal fluctuations in sea temperature. The costs of routinemetabolic activity are lower for individuals experimentally exposed tocolder water. In homogeneous water conditions, voluntary activity, meta-bolic rate and oxygen consumption all increase in response to a 2.5 �C risein temperature, leading to a subsequent decrease in scope for activity(Claireaux et al., 1995). When presented with a thermally stratifiedenvironment, however, behavioural changes are exhibited by cod, withindividuals swimming away from thermally stressful locations (Claireauxet al., 2000).

It appears that both swimming speed (Claireaux et al., 1995) and foragingrate (Peck et al., 2003) are also determined by thermal conditions. BetweenJune and August in the southern North Sea, decreased activity and predom-inantly benthic habitation were recorded from electronically tagged adultcod. When sea temperatures cooled, first nocturnal activity, then almostcontinuous activity took place during the following months (Righton et al.,2001). This pattern corresponds with expectations about energy conserva-tion (Arnold and Walker, 1992). When higher temperatures are encoun-tered it would be expected that they would either be avoided (O’Brienet al., 2000), and/or activity reduced, since occupation of higher tempera-tures will increase standard metabolic rate and reduce scope for aerobicactivity (Soofani and Hawkins, 1982; Soofiani and Priede, 1985). Growthalso decreases under such conditions, with individuals apparently switchingto a ‘translucent’ phase where an opaque band is formed during otolithgrowth (Pilling et al., 2007), indicating exposure to unfavourable tempera-tures (Hussy et al., 2004). Earlier onset and increased duration of thetranslucent zone of growth in recent decades has been attributed toincreased spring/summer water temperatures (Beckman and Wilson,1995), indicating that climate warming may be extending the period ofmetabolic stress (Pilling et al., 2007).

Sea surface temperatures have exceeded Topt for short periods duringrecent summers in the southern North Sea, for example. The subsequentdecrease in aerobic and locomotory performance will theoretically havebeen sufficient to impair activity such as to prevent optimal feeding in adultindividuals (Lannig et al., 2004; Portner, 2001; Portner et al., 2001). Thismay explain the seasonal absence of cod in the southern North Sea regiondespite apparent prey availability (Lannig et al., 2004). From these results ithas been suggested that if the climate continues to warm, seasonal



disappearance of cod from some areas may increase in frequency andduration. However, these conclusions assume that Topt does not shift as aresult of acclimation to regional temperature regimes, which may not be thecase of course. Differences in compensatory capacity to specific temperaturechallenges are generally expected for populations inhabiting different watermasses or latitudes as a result of acclimation to local thermal regimes (Clarke,1993), so it is unlikely that specific thermal thresholds will be the same for allcod populations across the biogeographic range.

2.4. Maturation and spawning

Significant correlations between mean annual sea temperatures and age atmaturity have been found for many cod stocks ( Jorgensen, 1990, 1992;O’Brien, 1999; Yoneda and Wright, 2004). Together these results indicatea 1-year reduction in maturation age linked to a 2 �C increase in tempera-ture (Drinkwater, 2002). Hence, closer to the southern range edge of thespecies, maturation is predicted to be at a younger age. This pattern hasimplications for future stock success in warmer climates because smaller,younger fish are less fecund and spawn for shorter periods (Kjesbu et al.,1996), and warmer spring seasons may promote earlier maturation.

Climate-linked sea temperature changes may have direct and indirecteffects on cod energy provisioning and maturation processes that precedespawning. Cod build up energy reserves during summer and autumn, andmature during the winter months. Mature female fish in better conditionprior to spawning tend to be more fecund (Kjesbu et al., 1991), and expendless energy and lose less somatic mass during the spawning season (Lambertand Dutil, 2000; Lloret and Ratz, 2000; Ratz and Lloret, 2003). Hence,these fish are at less risk of subsequent natural mortality (Krivobok andTokareva, 1972; Love, 1958). When energy reserves are low, investment inreproduction by females may be maintained, but at a somatic cost, andreproduction may also be reduced or delayed in extreme conditions to limitsomatic loss. Changes in environmental conditions and subsequent ecolog-ical processes that negatively affect food intake will influence the energybudget and ultimately reduce productivity of the stock (Lambert and Dutil,1997). If fishing pressure and climate change act synergistically to reducethe age and condition of the spawning stock, population fecundity maydecline (Ottersen et al., 2006). Faster development of early life stages andsubsequent higher survival under warmer climatic regimes may, however,counteract any such decline in fecundity.

Peak spawning dates have been found to vary among different Norwe-gian coastal cod populations kept in identical environmental conditions(Ottera et al., 2006). This indicates that spawning time is under geneticcontrol, and could be an adaptation related to environmental conditions intheir source location. Consistent with this evidence, survey data show cod



do not rapidly alter spawning time to match the timing of life history eventsin zooplankton prey species (Beaugrand et al., 2003). This suggests thatstock adaptation may result in a limited capacity for the stock to respondrapidly to climate-driven changes in peak abundance of prey. Thus, it canbe hypothesised that weak year classes following high larval mortality maybecome more common with warming sea temperatures.

Contrary to the assumed random mating strategy of many broadcastspawners, there is evidence for male lekking behaviour in cod (Robichaudand Rose, 2004;Windle and Rose, 2007), and for direct female mate choice(Engen and Folstad, 1999; Rowe and Hutchings, 2003; Rowe et al., 2004;Rudolfsen et al., 2005). In laboratory trials, both males and females displayedhigher reproductive success when mating occurred between larger indivi-duals (Rowe et al., 2007). The observed reduction in the size spectra of wildfish is thus likely to be affecting total reproductive output (Bekkevold, 2006;Bekkevold et al., 2002). Although climate will influence fecundity throughtemperature-related effects on maturation and reproductive success, size-targeted fishing mortality (of the largest fish) is one of the most likelydominant factors negatively affecting subsequent year class strength andrecovery of spawning stock biomass (SSB).

2.5. Early life stages

Cod eggs and larvae suffer high mortality (up to 99.9%) via predation(Campana, 1996; Cushing and Horwood, 1994; Houde, 1989; Leggettand Deblois, 1994; Shepherd and Cushing, 1980). The growth-predationhypothesis predicts a direct relationship between mortality rate and growthrate of early life stages of fishes (Anderson, 1988; Hare and Cowen, 1997),with more rapid egg and larval development promoting metamorphosis atan earlier age, thereby decreasing the duration of pre-juvenile stages(Drinkwater, 2005). Support for this theory has come from both experi-mental and simulation studies on early life stages of cod, and togetherthese show how small changes in early growth rates due to increases intemperature can lead to large increases in numbers surviving to recruitment(Chambers and Leggett, 1987; Houde, 1989; Meekan and Fortier, 1996;Miller et al., 1988; Pepin and Myers, 1991).

Cod eggs are found over a wide range of temperatures, from �1.5 �C inthe Northwest Atlantic, to 9 �C in the Celtic Sea (Geffen et al., 2006), andthere is evidence of local adaptation in development rates (Houde, 1989).Cod eggs from North Sea stocks cannot develop at temperatures less than1.5 �C, while larvae from the Baltic Sea can survive exposure to 1 �C, andeggs from the most northern populations will develop below 0 �C (Geffenet al., 2006; Valerio et al., 1992; Wieland and Jarre-Teichmann, 1997). Eggincubation periods can also vary significantly with temperature (Pauly andPullin, 1988; Pepin et al., 1997). Much of the observed seasonal variance in



egg and larval development times (Pauly and Pullin, 1988) and hatching size(Miller et al., 1988) can also be attributed to thermal conditions, with sizedecreasing as temperature increases. Thermal tolerance experiments,together with knowledge of spawning locations, indicate that it is unlikelythat wild eggs become exposed to lethally high water temperatures imme-diately after release. Egg mortality is probably caused by other processesincluding predation and disease, but egg mortality due to sublethal effects ofincreasing energetic costs at high temperatures may also take place (Nissling,2004).

Optimal temperature for growth (Toptg) undergoes a clear ontogeneticshift in cod (Fig. 3.4) (McCauley, 1977; Reynolds, 1977). Yolk sac larvaehave the lowest Toptg ( Jobling, 1988) while the highest Toptg is for freeswimming larvae and juveniles ( Jobling, 1994; McCauley and Huggins,1979). This ontogenetic difference in Toptg can range from 2 to 11 �Cdepending on the local thermal regime inhabited by the source population(Brander, 1994, 2005; Buckley et al., 2004; Bunn and Fox, 2004; Nissling,2004), but is centred around 7 �C (Buckley et al., 2004). Larval growth ratesincrease as temperature increases between 4 and 14 �C (Caldarone et al.,2003; Laurence, 1978; Otterlei et al., 1999; Steinarsson and Bjornsson,1999) with time to metamorphosis decreasing from 56 days at 4 �C, to23 days at 14 �C (Otterlei et al., 1999). Laboratory estimates of growth ratesmay, however, be dictated in part by indirect thermal effects on foodlimitation, as was observed for Georges Bank cod larvae during an anoma-lously warm period of 1992–1994 (Buckley et al., 2004).

The slowest growing cod larvae are found both in the cold waters of theNortheast Arctic (Otterlei et al., 1999), and in warm water towards thesouthern end of the range (Buckley et al., 2004) including the southernNorth Sea (Pilling et al., 2007). Survival of larvae has been recorded attemperatures as high as 12 �C in the Irish Sea (Geffen et al., 2006). Earlyjuvenile cod from the Irish Sea (Geffen et al., 2006) and those from theNorwegian coastal population exhibit higher Toptg and are heavier at thesame life stage than individuals inhabiting colder waters of the NortheastArctic (G�do and Moksness, 1987; Otterlei et al., 1999). This indicates thatupper pejus (deleterious) temperatures have not been reached, and thattemperature-driven growth relationships seem to be population specific.

Investigations to date indicate that slight warming of the marine climateis likely to enhance egg and larval survival by decreasing the time taken toreach metamorphosis that in turn limits the temporal window of greatestpredation risk. Even stocks close to southern range limits in the centralNorth Sea are likely to show increased survival of early larval stages due towarming of between 1.5 and 4 �C during the twenty-first century (Hulmeet al., 2002). If predator–prey relationships remain unchanged it is possiblethat the survival of young fish may therefore increase. The lagged responsesof cod to climate warming may thus be driven by conditions affecting



survival, growth and food availability during early life stages (O’Brien et al.,2000; Planque and Fredou, 1999; Platt et al., 2003).

2.6. Recruitment

Recruitment success of fish can be dictated by extrinsic stochastic eventssuch as changes in temperature, winds, currents, food availability, preda-tion/parasitism, and intrinsic factors such as variation in adult condition,stock reproductive effort and age structure (Cushing, 1996; Heath andGallego, 1997; Houde, 1989). These factors subsequently affect cod pro-duction, egg viability and survival of the early life stages (Kjesbu et al., 1996;Marshall et al., 1998; Nissling et al., 1998), as well as primary and secondaryproduction of the whole ecosystem (Hooper et al., 2005).

Recent studies indicate that the dominant pattern of recruitment varia-tion may be related to an effect of climate-driven sea temperature changes(Brunel and Boucher, 2007). Such climate-related changes in recruitmentsuccess may occur through one or more of several potential mechanisms,including higher production or survival of pelagic eggs or larvae (Rijnsdorpet al., 2009). Temperature plays a key role in the variation of cod recruit-ment success through a combination of direct and indirect effects (Cushing,1996; Hermann et al., 1965; Ottersen and Loeng, 2000; Sætersdal andLoeng, 1987). Fecundity is lower in mature individuals from northerncod stocks inhabiting colder waters, but given there is no evidence forcompensation through an increase in egg size (Brander, 1994), it appearsthat the cold-induced shift in the energy budget is unfavourable for repro-ductive output (Portner et al., 2001). This is supported by observations ofstrong year classes during warmer years in northern cod stocks (de Youngand Rose, 1993; Drinkwater, 2005; Malmberg and Blindheim, 1994;O’Brien et al., 2000; Ottersen, 1996; Ottersen and Sundby, 1995;Ottersen et al., 1994; Sundby, 2000).

Interannual variation in recruitment success is strongly dependent onseasonal temperatures (Wieland et al., 2000). Temperatures between Februaryand June have most impact on recruitment and subsequent year classstrength in the North Sea. A rise of 0.25 �C has been linked to a 30%reduction in recruitment (Clark et al., 2003). Simulations using the UKHadley Centre HadCM3 climate model reveal an inverse relationshipbetween change in abundance of 1-year-old cod and sea surface tempera-tures the previous spring, implying that climate effects on life stage is key tolater population recruitment success (O’Brien et al., 2000; Planque andFredou, 1999). A broad relationship between temperature regimes andstock success has been proposed by Drinkwater (2005), who suggestedthat recruitment increases as bottom sea temperatures increase until 5 �C,with little subsequent change until 8.5 �C, before a continual decline athigher temperatures. Based on these conclusions, a 2 �C increase in sea



temperature could result in significant declines in cod abundance in theNorth Sea from recent levels, with local extinctions being more likelybeyond a rise of 3 �C (Drinkwater, 2005). This model assumes that theslope of the temperature–recruitment relationship does not vary betweenstocks, does not account for seasonal variation in temperature and does nottake into account fishing mortality, or water column profile and occupancy.Indeed, such factors may explain why temperature–recruitment relation-ships are often weak (Brander, 2000). O’Brien et al. (2000) found nostatistically significant link between environmental temperature and recruit-ment in Northwest Atlantic stocks during the 1980s and 1990s, and re-analyses of recruitment data sets tend to confirm this result (Frank, 1997;Myers, 1998; Myers and Cadigan, 1995a,b; Myers et al., 1995a). In contrast,predictions of climate change impacts on recruitment and SSB in the NorthSea have been constructed using a model that includes fishing mortality,temperature-dependent growth rates, and a temperature-dependent Rickerstock–recruitment function (Clark et al., 2003). This model indicates thatsea temperature affects population dynamics via recruitment rather thanadult growth. Moreover, the model supports the hypothesis that Februaryto June sea surface temperatures most strongly influence recruitment(Dickson et al., 1974; O’Brien et al., 2000; Planque and Fredou, 1999).Under an unchanging climate scenario, the Clark et al. (2003) modelsuggests that both SSB and recruitment should increase over the next50 years if fishing mortality remains constant. However, even under asmall forcing of the climate by þ0.05 �C per decade, which is much lessthan the 1 �Cwarming that has already occurred in UK coastal seas since themid-1980s (Hawkins et al., 2003), SSB and recruitment are predicted todecrease. Under the A1F high emissions scenario (IPCC, 2001) of þ0.26 �Cper decade, North Sea stocks are predicted to virtually disappear if fishingmortality is not reduced (Clark et al., 2003). However, the model has caveats.It is based on linear models that do not fully capture the relationship betweenrecruitment and temperature, and it also does not account for potential rate-limited recruitment at higher temperatures. There is also a lack of spatialrepresentation of adult distributions, including potential for changes inspawning locations over time (Brander, 1994, 1997; Daan, 1978).

Cod recruitment patterns may also reflect temperature-driven variabilityin availability of food resources at lower trophic levels (Rothschild, 1994).It has been demonstrated that peak spawning date in low biomass codpopulations shows strong associations with temperature (Kjesbu et al.,1994; Wieland et al., 2000). In the Northwest Atlantic, higher temperaturesappear to result in earlier annual spawning dates in stocks occupying higherlatitudes, due to accelerated gonad development (Hutchings and Myers,1994a,b). The most northern stock in the Barents Sea also shows a positiverelationship between recruitment and temperature. The opposite relation-ship was observed in stocks located at lower latitudes towards the southern



limits in the North Sea (Daan, 1994; Dickson et al., 1974; Myers, 1998).These relationships were subsequently re-tested and shown not to hold,emphasizing that studies of recruitment may need to step beyond searchingfor straightforward spawner–recruit and temperature–recruitment relation-ships (Myers, 1998).

In the North Sea, changes in the plankton community have been a keydriver of interannual fluctuations in cod dynamics. Long-term changes inrecruitment co-vary with changes in the abundance and body size of zoo-plankton prey with a 1-year time lag, and show a tighter relationship than thatobserved between cod recruitment and sea surface temperature (Beaugrandet al., 2003; Horwood et al., 2006). The relationship holds for both anoma-lously cool and warm periods, such as the gadoid outburst between the mid1960s and 1980s when cool temperatures were associated with high abun-dances of the boreal copepod Calanus finmarchicus. This copepod is a majordietary component of the cod early life stage, and these high abundancesoccurred in parallel with 12 years of high cod recruitment (Fig. 3.5).Conversely, during the warm period of the late 1990s and early 2000s,anomalously low cod recruitment reflected low biomass of C. finmarchicus.Warmer waters appear to have resulted in unfavourable conditions for theoverwintering stage of this copepod (Greene et al., 2003; Heath et al., 1999)and forced a distributional shift to higher latitudes in the North Sea(Beaugrand and Ibanez, 2004). Higher confidence can be placed on theassumptions of these shifts in biogeographic distribution due to the extensivespatial and temporal coverage of the data, and the use of direct observationaldata rather than extrapolations based on putative centres of distribution.

Direct effects of thermal regimes on physiology of larval fish, andindirect effects on their prey availability, are both likely to be importantdrivers of recruitment strength. However, the exact nature of the

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Figure 3.5 Parallel long-term changes in zooplankton fluctuations (with 1-year lag)and cod recruitment in the North Sea. Adapted from Beaugrand et al. (2003).



relationships remains unclear. The abundance and size structure of a popula-tion will depend on a range of factors, including the extent of immigrationand emigration from populations with different thermal tolerances (Simset al., 2001, 2004). In the absence of gene flow, adaptation or local acclima-tization may lead to a contraction of the spawning period and spawning area,causing fish such as cod to become more sensitive to changes in environmen-tal conditions (Ottersen et al., 1994). Heavily exploited populations of codmay therefore display amplified responses to climate change (Planque andFredou, 1999). These complications may lead to difficulties when predictingshort-term outcomes of environmental change on populations (Planque et al.,2003; Rothschild, 1994, 1998).

Biological responses may show strong relationships with large-scaleclimate indices such as the North Atlantic oscillation (NAO) (Broitmanet al., 2008; Drinkwater et al., 2003; Fromentin and Planque, 1996;Ottersen et al., 2001; Stenseth et al., 2002; Walther et al., 2002). Suchclimate indices often incorporate multiple variables and the interactionsbetween them, and thus can capture a complex interplay of weather andclimate-induced variations in the natural environment. As a consequence,they can provide useful assessments of climate fluctuations with which toexplore ecosystem change (Namias and Cayan, 1981; Stenseth et al., 2003).The NAO is the main index of winter atmospheric circulation over theNorth Atlantic. During positive NAO years, warmer winters occur andseawater temperatures are warmer around Northwest Europe. When theNAO switches to a negative phase, winter temperatures are colder in theregion (Hurrell and Van Loon, 1997; Van Loon and Rogers, 1978). Overthe last 25 years, the frequency and magnitude of NAO positive-indexevents have increased and winter sea surface temperatures have becomemilder in British coastal waters. The NAO is predicted to remain in a largelypositive phase in the coming decades.

Relationships between the NAO index, the physical environment of theNortheast Atlantic and biological responses within it have been well estab-lished (Broitman et al., 2008; Hurrell and Van Loon, 1997; Reid et al., 2001;Sims et al., 2001, 2004). Importantly, the NAO index has been linked tochanges in recruitment success of most cod stocks in this region (Ottersenet al., 2001), mainly via the direct effects of environmental temperature onsub-adult growth and survival (Attrill and Power, 2002; Dippner, 1997;Ottersen et al., 1994). When all Northeast Atlantic cod stocks are combinedwithin a single recruitment model, a significant geographic relationshipbetween the strength of the NAO and recruitment emerges, with stock-specific trends also apparent (Stige et al., 2006). Environmental conditionsduring a positive NAO index have been shown to have a negative influencefor southern stocks on both seaboards of the Atlantic, but a positive influ-ence on more northerly stocks (Brander and Mohn, 2004).



2.7. Growth

Experimental studies and analyses of catch statistics show that changes inseawater temperature exert a major influence on growth (Bjornsson andSteinarsson, 2002; Bjornsson et al., 2001; Brander, 1995, 2000; Campana,1996; Campana and Hurley, 1989; Jobling, 1988; Solberg and Tilseth, 1987;Steinarsson and Bjornsson, 1999; Taylor, 1958). As such, temperature isconsidered to be a major determinant of production in cod stocks (Dutiland Brander, 2003). Benthic water temperatures have been shown to accountfor 90% of observed variation in growth rates between cod stocks (Brander,1994, 1995) and to drive annual growth fluctuations within them (Brander,1995; Brander et al., 2003; Campana et al., 1994; Clark et al., 2003; deCardenas, 1996; Drinkwater, 2005). This temperature-dependent variabilityin growth rates is mediated by immediate physiological requirements, andtrade offs between growth and reproduction (Portner et al., 2001).

Free swimming cod tend to select temperatures in which growth rate ismaximised (Claireaux et al., 1995; Magnuson et al., 1979), but it is not alwayspossible for individual fish to maintain themselves within thermally optimalhabitats. Low temperatures result in slower growth rates and a reduction in thephysical condition via direct impacts on rate of food assimilation, and indirecteffects on food supply (Otterlei et al., 1999). The resultant physiological andecological impacts are manifested as a small size-at-age, reduced cohort size, adecline in stock biomass, and surplus energy redirected into reproductiveeffort (Brander, 1995; Campana, 1996; Krohn et al., 1996; May et al., 1965;Taylor, 1958). Meta-analyses of cod populations show that body conditionexhibits a significant increase with warmer mean sea bottom temperatures(Drinkwater, 2005; Ratz and Lloret, 2003). The temperature for optimalgrowth, however, decreases with size and age, and ranges between 14.3 and17.0 �C for newly hatched juveniles, to between 5.9 and 10.0 �C for adults(Bjornsson and Steinarsson, 2002; Bjornsson et al., 2001; Brander et al., 2003;Buckley et al., 2004; Portner et al., 2001). Thus, decreasing growth perfor-mance in adult cod is observed with increasing latitude (Brander, 2004;Portner et al., 2001). Genetic differences between stocks are also likely to beat least partly responsible for the observed spatial differences, as populationdifferences in growth rates have been seen under controlled experimentalconditions (Portner et al., 2001). Such population variation in growth rates andbody size may also be a consequence of fishing, as sustained removal of largerindividuals has resulted in evolutionary selection for individuals maturing atearlier ages and sizes (Gadil and Bossert, 1970; Olsen et al., 2004).

Although studies indicate that as seawater temperatures rise, cod inwarmer climates may experience increased growth rates, such increasesmay be counteracted by food availability, which can explain up to 97%of the variance in growth in wild cod (Chabot and Dutil, 1999). Food-dependent growth rates may become particularly apparent because



exposure to warmer water increases standard metabolic rates. Such negativeeffects on growth may be intensified in conditions of low prey density, asthe temperature of optimal performance can become lowered (Brett andGroves, 1979; Buckley et al., 2004). Since growth and survival of larval fishare implicit to many recruitment hypotheses (Anderson, 1988; Cushing,1990; Ware, 1975), and are affected by climate-driven sea temperaturechanges (Rijnsdorp et al., 2009), predictions of growth rates under futureclimates will clearly require data on prey abundance, and information onprey distribution and sub-adult feeding behaviour (Buckley et al., 2004;Dower et al., 1998; Fiksen and MacKenzie, 2002).

3. Impacts of Fishing

Marine fishing activity in the North Atlantic can be traced back over atleast 1000 years (Barrett et al., 2004, 2008), and there is compelling evidencethat this has severely depleted demersal fish stocks in the region, reflectingglobal trends. Biomass of commercially valuable demersal fish populations isnow estimated to be at only 10% of pre-industrial levels (Worm and Myers,2003), and there has been a concomitant decrease in mean trophic level oflanded fish (Pauly et al., 1998). Atlantic cod abundance in particular hasdeclined dramatically since the onset of commercial fishing. Using historicalrecords of New England cod abundance derived from mid-nineteenthcentury fishing logs, it was estimated that current population biomass nowstands at less than 5% of that in 1852 (Rosenberg et al., 2005). Reconstruc-tions using historical records or proxies have also revealed high levels offisheries exploitation affecting key biological parameters of cod. For exam-ple, by studying cod vertebrae preserved in middens in New England, largedeclines in population body size distributions have been revealed ( Jacksonet al., 2001), changes that have links to the biological effects of commercialfishing (Olsen et al., 2004).

In this section, we describe the impacts of fishing on cod populations ineach of the main regions across its biogeographic range, and bring togetherthese findings with those on climate impacts to evaluate the relative contri-bution of each set of drivers to observed trends.

3.1. Northwest Atlantic stocks

All cod stocks are now generally considered to be either fished at unsustainablelevels, are subject to moratoria following dramatic stock collapses, or haverecovery plans that do not meet ‘precautionary approaches’ advised by theInternational Council for the Exploration of the Seas (ICES) (CEC, 2001;FAO, 2002; Hutchings and Myers, 1994a,b; ICES, 2005, 2006, 2008;



Kuikka et al., 1999;Myers et al., 1997). Arguably themost dramatic collapse ofcod was that seen in the Northwest Atlantic. During 1986 and 1987 recruit-ment was very strong in all cod stocks in this region. As a consequence, fishingmortality (F) increased from 0.5 to>1.0 between 1989 and 1992 for all stocks,except that of the southern Grand Banks (Bishop et al., 1993; Myers et al.,1996). Landings initially increased as SSB was decreasing, a pattern thought tohave been caused by fish at lower population biomass tending to aggregate,perhaps making them easier to capture (Hutchings, 1996; Morgan et al., 1997;Rose and Kulka, 1999). Whatever the mechanism, catches were soon domi-nated by young and small cod (Hutchings and Myers, 1994a,b; Myers et al.,1996). It has been argued that the main factors responsible for the collapseacross many of the cod stocks by 1993 were the ignorance of the relationshipbetween fishing mortality and stock biomass, due to consistent underestima-tion of the proportion of fish harvested annually (Myers et al., 1996), and anunwillingness to cut fishing effort due to the perceived short-term economicconsequences (Rivard and Maguire, 1993; Schiermeier, 2002). Evidenceindicates that incorrect calculations of fishing mortality resulted fromoverestimation of biomass (Steele et al., 1992; Walters and Maguire, 1996),an underestimation of reductions in productivity (Rice and Evans, 1988),overweighting of abundance indices to provide the most optimistic estimatesof SSB (Myers et al., 1996, 1997) and an increase in efficiency of the fishingfleet (Hilborn and Walters, 1992; Walters and Maguire, 1996). No evidencewas found to link abundance of age classes or distributions with water temper-ature, and thus climate change was rejected as a primary driver for the collapseof these cod stocks (Hutchings and Myers, 1994a,b). A decade after themoratorium on cod fishing was introduced in 1992, populations were still athistorically low abundance (Lilly et al., 2003), and even in 2007 the SSBcontinued to have weak representation from all year classes (STECF, 2007).

3.2. Northeast Atlantic stocks

Atlantic cod have a broad distribution on the European continental shelf. Inthis section, however, rather than review stocks in all areas, we focus onthree areas with contrasting habitats and different fates of stocks. First, wedescribe how fishing has impacted cod in the North Sea, a region wheresome of the largest declines have occurred, we then compare this to changesin the Celtic Sea stock, where, in general, cod are found at relatively lowabundance. Finally, we discuss the status of cod in Icelandic waters, wheremanagement structures are different with respect to these other areas.

3.2.1. North SeaThe entire North Sea has been commercially fished since the mid-eigh-teenth century (Cushing, 1988; Smith, 1994), with periods of cessationduring the two World Wars (Beverton and Holt, 1957; Borley, 1923;



Hardy, 1959; Margetts and Holt, 1948). Catchability of cod was high duringthe late 1940s and 1950s, but began to decline in the 1960s as increasedlevels of exploitation caused dense aggregations to be fished out (Gulland,1964). During the ‘gadoid outburst’ of the 1970s, high recruitment led tomassive increases in juvenile cod abundance, with estimated stock sizes of250,000 tonnes (Brander, 1995; Cushing, 1984; Hislop, 1996; Horwoodet al., 2006). This period was associated with cooler waters and increases inthe abundance of the cold water copepod C. finmarchicus, a primary foodsource for pelagic larval cod (Beaugrand et al., 2003). Landings rose until theearly 1990s, then declined before levelling out at record low levels after2003 (Holden, 1978; ICES, 2007; Jennings et al., 1999; Olsen et al., 2004;Rijnsdorp and van Leeuwen, 1996; Rijnsdorp et al., 1996; Fig. 3.6). Theyear class of 1996 was anomalously strong, but it was removed by fishingbefore reaching maturity (Bannister, 2004), indicating that fishing impactson stock dynamics were far outweighing those of climatic variability. Size ofindividual adults also declined across the twentieth century in response toincreased fishing mortality of larger, older cod (Fig. 3.7).

North Sea cod has been managed under joint management agreementsinvolving annual assessments by the European Council of Ministers and theNorwegian government since 1974 (Reeves and Pastoors, 2007). The definedlimits of theNorth Sea include the Skaggerak and easternEnglishChannel, andall cod are treated as one stock for ease of management despite some geneticevidence for multiple populations within the region (Blanchard et al., 2005;

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Figure 3.6 Total estimated catch (in thousands of tonnes) of cod from the North Seasince 1985 including landings and discards. Data: ICES (2008).

Figure 3.7 High numbers of large cod being landed on the fish market at Aberdeen,Scotland. Photograph ca. 1920.



Hutchinson, 2008; Hutchinson et al., 2001; STECF, 2007). The assessmentand total allowable catch (TAC) advice process is conducted under anICES umbrella, and primarily reflects the needs of the main customer, theCommission of the European Communities (Holden, 1994).

TACs have been restricted for the last two decades to allow an estimated30% increase in spawning biomass, but also whilst falling within 15% of theprevious year’s TAC. Data from both research vessel surveys and fisherieslandings data suggest that TACs have been ineffective. By 1992, only 4% ofNorth Sea cod were surviving to maturity at 4 years old due to intensiveharvesting across the year classes (Cook et al., 1997), and the most com-monly caught age classes over the last two decades were immature 1 and2 year olds (Myers et al., 1996; O’Brien et al., 2000). By 2000, SSB hadfallen to around 40,000 tonnes (ICES, 2000), well below the ICES mini-mum biomass limit of 70,000 tonnes, at which stock production wasconsidered as being severely impaired (Horwood et al., 2006). Conclusionsfrom cod recovery scenarios suggested that even a reduction in fishingmortality to a precautionary F ¼ 0.65 per year provided a low probabilitythat stocks would recover to a precautionary biomass level within a decade(STECF, 2007). Moreover, these models did not take into account climatechange in the projections. A narrow window between ‘potential’ and ‘no’recovery was highlighted (Horwood et al., 2006), which may explain whyreductions in fishing effort close to precautionary levels have failed toincrease stock biomass. Repeated recommendations from ICES of eithertotal closure or reductions in fishing mortality of up to 70% duringthe 2000s have resulted in annual re-calculations of TACs and reductions



in the number of days at sea for gill-netting vessels and beam trawlers in the70–99mmand>100mmmesh sectors (ICES, 2003, 2004, 2006, 2007, 2008).

A recovery plan involving TACs to allow a 30% increase in biomass wasfinalized in 2004 for the North Sea, Kattegat, West Scotland and Irish Seastocks. A year later, ICES announced that the recovery plan for cod was notprecautionary (ICES, 2004) and by 2006 the North Sea and NorthwestRegional Advisory Committees had found little evidence of recovery, withstocks still at or close to historically low levels (NSRAC, 2006). Althoughthere have been some indications of improved recruitment with a relativelystrong year class in 2005, no increase in SSB has been observed to date.ICES altered their recommendations from ‘lowest possible catch’ in 2002 to‘zero catch’ from 2004 to 2008 (ICES, 2003, 2004, 2006, 2007, 2008).Interestingly, North Sea cod were listed as being ‘harvested sustainably’ byICES in 2008, but these stocks in 2009 have been categorized as ‘overf-ished’, with fishing mortality ‘above target’ and a recommendation of ‘zerocatch’ (ICES, 2008).

3.2.2. Celtic SeaCod have also been targeted by both single- and mixed-species fisheries inthe Celtic Sea for several centuries (Kurlansky, 1997), but intensive com-mercial fishing began relatively recently in comparison with other NorthAtlantic regions (Pinnegar et al., 2002). Recent assessments have valuedlandings made by the combined international fleet to be approximately£10.5 million per year, with maximum landings occurring during wintermonths (Fisheries Science Services, 2008; ICES, 2006).

Dwindling numbers of pelagic and demersal fish, including cod, in thecoastal Celtic Sea and elsewhere around the UK were of concern as early asthe mid-nineteenth century (Sims and Southward, 2006). During theperiod of modern data collection and assessments, fishing mortality in theCeltic Sea has remained at very high levels since the mid-1980s (FisheriesScience Services, 2008; Worm and Myers, 2003) albeit with a slightdecrease in recent years due to a reduction in the section of the fleettargeting cod since 1999 (ICES, 2006). The stock has been well belowsafe minimum limits since 2004, and even with the recent reduction infishing effort, biomass is continually declining (ICES, 2006, 2008). Despitedeclining stock size and low projected recruitment if present fishing effort ismaintained, a successful management strategy has yet to be put into practicein the Celtic Sea region.

The Celtic Sea cod stock is located close to the southern biogeographiclimit of the species in the Northeast Atlantic. The fish have relatively fastgrowth rates and mature at 2–3 years of age (Armstrong et al., 2001; ICES,2003). Recent poor recruitment rates have been purported to be driven inpart by warming seas, but there is little evidence for climate-driven changesin the biogeographic range or abundance of this stock, and thus fishing is



still recognized as a primary factor determining SSB. In addition to species-level impacts, it is notable that significant declines in the mean trophic levelof catches overall have been observed from the region, consistent withfishing-induced changes to the structure of the whole fish community(Pinnegar et al., 2002).

3.2.3. IcelandThe Icelandic cod stock is one of the largest in the North Atlantic, with amaximum sustainable yield (MSY) of 330,000 tonnes providing annualrevenue in excess of £400 million. The stock is managed as a single unit,although there are discrete regional spawning components (Begg andMarteinsdottir, 2000). Stock size declined throughout the twentiethcentury from a peak of 3.3 million tonnes in 1928 to 600,000 tonnes by1993 (Schopka, 1994), accompanied by a decline in SSB to 120,000 tonnes(Marine Research Institute, 2008). A low stock size was recorded in 2007 ascatches have continued to exceed advised levels, although SSB has shown anincrease in recent years to approximately 230,000 tonnes (Marine ResearchInstitute, 2008). Mean weight at age has decreased significantly to an all-time low in 2007 and 2008, attributed to the lack of capelin as a food sourcein recent years. This weight-at-age trend, in combination with recent poorrecruitment, has led to very low productivity of the current stock (MarineResearch Institute, 2008).

Three so-called ‘cod wars’ have taken place in the waters off Icelandduring the latter half of the twentieth century, in 1958, 1972 and 1975.These hostilities arose as a result of extensions in the offshore spatial extentof the Icelandic fishery exclusion zone and a lack of recognition of thisexpanding zone by vessels from European countries already fishing in thesewaters. The first conflict resulted in an extension of Iceland’s territorialwaters to 12 nautical miles from the coast. Further extensions of theIcelandic fishing zone to 50 nautical miles in 1972 and 200 nautical milesin 1975 resulted in more severe international conflicts. The final confronta-tion was resolved when intervention by the North Atlantic Treaty Organi-zation (NATO) succeeded in brokering an agreement that reduced access toBritish vessels within the 200 nautical mile limit, including closure of fourconservation areas to British fishing activities. Various Icelandic govern-ment acts have since been introduced in an attempt to reverse the trend ofdeclining fish stocks within the 200 nautical mile limit, including TheFisheries Act of 1976 (amended in 1983), Individual Effort Restrictions in1977, The Fisheries Management Act 1990, the Harvest Control Rule in1995 and the current system of TACs. Despite these measures, stock size hasshown no signs of recovery to sustainable levels.

In the early decades of the twentieth century, stock size was stronglycorrelated with environmental changes in the Iceland–Greenland region.The coastal current and Atlantic inflow are thought to exert a strong



influence on annual success of each spawning component via alterations inthe strength of water flow from the main spawning grounds off the north-west coast of Iceland to the main nursery grounds off the north coast (Beggand Marteinsdottir, 2002). Pelagic juveniles are larger and more abundantduring years of stronger current flow and Atlantic inflow, due to bothincreased dispersal and increased abundances of the main prey species ofzooplankton, C. finmarchicus that is brought into the region by the Atlanticinflow (Sundby, 2000). As fishing mortality has steadily increased from 0.16to approximately 1.0 between the 1930s and 2000s, it has exerted anincreasingly dominant influence on the annual stock size of Icelandic cod.Stock models that incorporate both environmental and fishing componentsindicate that substantial reductions in fishing effort are required to permitstock recovery (Baldursson et al., 1996).

3.3. The fishing versus climate change debate

Historically high abundances of North Sea cod during the early 1900s(Eckman, 1953), 1960s and 1970s (Cushing, 1984) have been linked tocooler marine climates, while the recent period of rapid climate warminghas been suggested to have contributed to the observed declines in SSB(Blanchard et al., 2005; Clark et al., 2003; O’Brien et al., 2000; Ottersenet al., 2006; Schiermeier, 2004). During recent decades it is possible thatclimate signals have been overridden by fishing impacts, and recent warmerclimates have exerted additional pressures on already stressed stocks(Graham and Harrod, 2009). However, separating the interactions betweenthe two drivers has proved difficult. Thus, quantifying strengths of compo-nent effects will be challenging, especially between regions that differ incommunity compositions, thermal regimes and habitat structure, and also incod abundance, distributions and behaviour (Neat and Righton 2006;Righton et al., 2001). Despite this, there is a need to more fully understandthe contributive effects of climate change on cod stocks that are already athistorical low abundance due to overexploitation.

Biological responses to environmental changes such as fishing andclimate, for example, can be divided into two categories. Firstly, proximateecological responses that depend upon relationships between physicalfactors and organismal-level processes, population dynamics and commu-nity structure (Harley et al., 2006). Secondly, direct impacts on individualperformance during various life stages through changes in physiology,morphology and behaviour (Mieszkowska et al., 2006, 2007). Theseimpacts lead to population-level responses, which can be additionallyaffected by climate-driven changes in hydrographic processes that affectdispersal of the pelagic larval life stages and recruitment. All of these arelikely to lead to alterations in cod distributions, biodiversity, productivityand micro-evolutionary processes.



4. Population-Level Impacts of Fishing

and Climate Change

Shifts in survival, maturity, fecundity, reproduction, recruitment suc-cess and growth all scale up to the population level. If sufficient numbers ofindividuals display the same response to an external driver, such as climate,then population dynamics are likely to be altered. Such effects of climate arelikely to be observed first within populations located close to the distribu-tional limits, where environmental conditions are most likely to be alreadyapproaching stressful levels (Lewis, 1986, 1996; Orton, 1920; Southward,1995). By contrast, effects of fishing mortality may well affect populationsacross much of their range.

4.1. Stock assessment

SSB is the parameter used to define the size of exploited fish stocks. Bothshort- and long-term variability in SSB may be driven by natural age-structured interactions, including competition between year classes, canni-balism and natural mortality (Bjornstad et al., 1999). The SSB–recruitmentrelationship may be contextualized with respect to underlying environmental,ecological and biological processes that control growth, reproduction andmortality. Supporting this idea, inclusion of age structure data can help toimprove SSB–recruitment models (Marteinsdottir and Thorarinson, 1998).Different age classes may contribute unequally to reproductive output and aspawning stock with a more diverse age structure may exhibit protraction ofthe spawning period due to size or age-dependent factors (Hutchings andMyers, 1994a,b; Marteinsdottir and Petursdottir, 1995). The most commonmethod of determining the spawner–recruitment relationship is the applica-tion of a model such as the Ricker or Beverton–Holt model to a single stock(Myers et al., 2001). Unfortunately, the stock–recruitment curve that isgenerated can be simplistic, and the effects of biological and environmentalfactors can strongly affect this relationship leading to large variations inrecruitment (God�, 2003; Marshall et al., 1998, 2000).

The existence of a relationship between abundance of spawners andnumber of recruits is implicit to SSB calculations (Hilborn and Walters,1992; Myers and Barrowman, 1996), but within-stocks data provide a poorfit to models (Myers and Cadigan, 1995a,b; Myers et al., 1995a,b; Shepherdand Cushing, 1980). Potential reasons for this are pre-recruit mortality(Cushing, 1988; Goodyear and Christensen, 1984; Walters and Collie,1988), model skew caused by outliers (Chen and Paloheimo, 1995) and/orerrors in variablemeasurement (Walters and Ludwig, 1981). There is also thepossibility of high variance in reproductive output among individuals, that



may in turn result in large disparities between effective and observed popu-lation sizes (Hedgecock, 1994), and even large populations may have fewindividuals that effectively contribute to spawning (Hauser and Carvalho,2008). In theory, a minority of individuals that spawn in favourable oceano-graphic conditions can disproportionately contribute to the next generation(Hedgecock, 1994). Finally, migrations affecting stock connectivity are alsonot typically considered when assessing these relationships (Myers et al.,2001).

4.2. Stock evaluation—An example from the North Sea

The ICES Stock Assessment Working Group uses data from commercialcatches, research vessel surveys and time series to evaluate the status of theNorth Sea stock relative to previous years and defined reference points.Information on catch per unit effort, catch-at-age and natural mortality arecompared to an average between 1980 and 1982, and used to calculate SSB(Beare et al., 2005; Sparre, 1991). These parameters are assumed to remainconstant between years. Forecasts of stock status for the forthcoming yearare made for a range of exploitation rates, and presented as a catch-optiontable of resultant SSB from specific fishing mortalities (Reeves and Pastoors,2007). These projections are then peer-reviewed by the ICES AdvisoryCommittee for Fisheries Management before management decisions aremade at the political level.

The use of stock–recruitment methods in fisheries management has beencriticized due to a lack of concordance between the projected model out-puts of stock assessments, and the observed annual variation in reproductivepotential of stocks. The disparity is likely to be due to interannual stochasticfluctuations, which in turn are likely to be largely driven by natural envi-ronmental changes. This highlights the need for stock assessment analyses toinclude survey-based indices of stock abundance (Marshall et al., 1998).In theory, changes in SSB should be able to provide a clear indication ofwhether fishing mortality or climate change is the dominant factor causingthe continual decline observed during the last two decades. If climate-driven effects are the primary cause of the decrease in population abun-dance, years with high observed SSB would be expected to be preceded byhigh survivorship and recruitment of sub-adults (Myers et al., 1996). How-ever, this is not generally observed. In the North Sea, for example, adultstock biomass has declined from the 1960s until recently (2006–2008),despite numbers of recruits-per-spawner being relatively high, indicatingthat the loss of individuals from populations is occurring from the older ageclasses. By contrast, if fishing is the driving force, proportional mortality dueto harvesting would continue to increase during the decline of the stock(Myers et al., 1996). Figures indicate that such fishing mortality hascontinued to increase, despite severe reductions in the TACs issued



(ICES, 2003, 2004, 2006, 2007, 2008). Taken together, this evidencestrongly indicates that overexploitation is the dominant factor causing thecontinuing decline in cod SSB in the North Sea.

4.3. Allee effects and management plans

When population size falls below a critical point, individual fitness may bereduced, causing a decline in population growth rate known as ‘growthdepensation’, with an increase in extinction vulnerability of the populationas a whole (Drake and Lodge, 2006; Myers and Cadigan, 1995a,b; Postet al., 2002). More generally, the correlation between population size andpopulation growth rate is known as the Allee effect (Allee, 1931), and theAllee threshold is reached when the population size either increases ordeclines to an unstable density equilibrium, where the birth rate equalsthe death rate (Berec et al., 2007) (Fig. 3.8). This threshold is unstable, andfor cod, any variation in recruitment or SSB can cause a population that issubject to strong Allee effects to expand, stabilize or collapse (Rose, 2004a,b;Shelton andHealey, 1999; van Kooten et al., 2005). Allee effects can be drivenby numerous causes. In some species, they may be induced by a decreasedprobability of finding a mate, failure of schooling behaviour to preventpredation or decreased foraging efficiency in social foragers at lower popula-tion densities (Courchamp et al., 1999; Stephens and Sutherland, 1999).Fisheries exploitation can induce an Allee effect if fish population-size reduc-tions lead to aggregation, enabling fishers to more efficiently locate andharvest the remaining fish.

Cod may experience Allee effects from low fertilization success andreduced juvenile survival at low population densities (Rowe et al., 2004).As a top predator, Allee effects may also occur if cod feed specifically onsmall individuals of a size-structured prey population, and this leads to adecline in the prey abundance, enhanced intraspecific competition and

Population density

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Figure 3.8 A schematic diagram of theoretical Allee effects on a population. SeeSection 4.3 for explanations of terms and the concept.



ultimately a decline in the adult cod population (de Roos and Persson,2002; de Roos et al., 2003). Equally, Allee effects may act on cod through a‘predator-pit’ scenario. If predators are able to continually maintain codbiomass at low levels, then populations may be unable to produce sufficientrecruits to allow population expansion. Harp seals (Phoca groenlandica) haveconsumed an estimated 88,000 tonnes of cod per annum in the NorthwestAtlantic throughout the second half of the 1990s, many of which are pre-recruits (Stenson et al., 1997). The grey seal (Halichoerus grypus) is alsoreported to be responsible for heavy predation on two Northwest Atlanticstocks (Chouinard et al., 2005; Fu et al., 2001; Trzcinski et al., 2006). NorthSea cod are pre-dated upon by grey seals, but estimated consumption of codonly amounts to approximately 3.7% of the total stock biomass (Hammondand Grellier, 2005). Harbour porpoises (Phocoena phocoena) also feed oncod, and are four times as abundant as harbour seals in the North Sea.Cod populations are therefore exposed to both natural and fisheries-induced depensation.

The debate continues over the existence of fishing-induced Allee effectsin cod. It has been argued that the species does not exhibit any of themechanisms usually associated with the Allee effect (Myers et al., 1995a,b;van Kooten et al., 2005). Instead, it has been suggested that fishing mortalitymay actually enhance juvenile survival due to low spawner densities (Myerset al., 1995a,b). Exclusion of depensation in stock assessment predictions forNorthwest Atlantic stocks gave rise to predictions of an annual growth rateof 19% with zero F and a threefold increase in stock size after 7 years fromthe moratorium in 1993 (Myers et al., 1997). Over a decade on, however,only four stocks have showed any signs of increased abundance, with onlyone experiencing substantial recovery (Shelton et al., 2006).

The potential presence of Allee effects operating on cod populationssuggests that if insufficient information on the life history of the targetspecies is included in management models, the effects of climate changeon fisheries could be vastly underestimated. For populations such as theNorth Sea cod, for example, which have been reduced to levels far belowthe carrying capacity of the system, it is vital that this does not occur. Thecombination of Allee effects and incorrect management could reduce thestock size to a critical level where the population will suddenly crash.Fisheries assessment models generally assume a spawner stock–recruit func-tion whereby recruitment increases with spawner biomass until it reacheseither an asymptote (Beverton–Holt model) or declines (Ricker model).Thus, these models assume that individual reproductive output will actuallyincrease at low fish densities. The inclusion of potential Allee effects intomanagement plans could help to optimise risk management strategies, eventhough Allee thresholds cannot currently be accurately established (Berecet al., 2007). Protection of areas where high densities of cod are presentcould help to prevent Allee effects from occurring.



5. Monitoring Status and Recovery of

North Sea Cod: A Case Study

Monitoring North Sea cod stocks for signs of recovery has provendifficult, not least because catches and bycatches often go unreportedmaking assessment of recovery difficult (ICES, 2004, 2005). The regioncurrently falls within a single ICES management unit, but the existence ofmultiple distinct stocks within the North Sea may obscure the dispropor-tionate decline of some more vulnerable stocks for which separate manage-ment plans may be required (Hutchinson, 2008). Landings may need to besplit into relative contributions from different stocks to allow appropriatemanagement strategies, as recommended by the North Sea Regional Advi-sory Council (NSRAC, 2008). In addition, a range of values of fishingmortality are obtained using multiple research vessel surveys, introducinguncertainty into stock estimations (Blanchard et al., 2005).

Prior to 1988, assessment and forecasting techniques showed largeinterannual variation in performance as the methodology developed, andbetween 1988 and 1995 relatively high performances were obtained. How-ever, since then, there has been a systematic underestimation of fish mortalityand overestimation of the contribution of incoming year classes (Reeves andPastoors, 2007). Similar problems have been encountered in other codstocks (Pastoors, 2005). Under-reporting of landings and the absence ofdiscard data creates uncertainties in catch estimation, although errors in theassessment preceded the problems arising from limited catch data and do notappear to explain the change in model performance. Instead, this may beattributable to the reliance on parameters estimated from earlier timeperiods where the ecosystem may have been in a different state, and/orthat may also have been potentially, at least in part, a consequence of theimpacts of climate change (Beaugrand et al., 2003; Blanchard et al., 2005;O’Brien et al., 2000).

The international aspect and mixed species nature of the North Seafishery have been highlighted as the main factors contributing to the recentpoor state of the North Sea stock (Bannister, 2004), despite efforts to reducefishing mortality at the European scale. A wider ecosystem-based approachis being developed to attempt to account for the mixed species nature ofNorth Sea demersal fisheries (Vinther et al., 2004). However, the process ofdetermining suitable parameters that distinguish relative impacts of fishing,climate change and natural variance is continuing (Blanchard et al., 2005;Rice, 1995, 2000; Rice and Evans, 1988; Rice and Rochet, 2005; Rochetand Trenkel, 2003; Trenkel and Rochet, 2003). Among these approaches issize spectra analysis, a technique that has proven useful for detecting effectsof exploitation on fish stocks, as temporal changes in the index are consistent



with fishery-mediated changes in community structure (Bianchi et al., 2000;Gislason and Rice, 1998; Jennings and Greenstreet, 1999; Murawski andIdoine, 1992; Rice and Gislason, 1996; Shin et al., 2005; Zwanenburg,2000). Even this approach has difficulties, however, as warmer watersexpected due to climate warming may lead to enhanced recruitment ofsmall species, and concomitant shifts in the size spectra. If such issues can beovercome by allowances for discrimination between forcing factors, thensize-based metrics may become useful management tools (Blanchard et al.,2005; Genner et al., 2009b).

There has been little research into the application and utility of closedareas for fishing, and it appears most closures have been designated withoutclear objectives (SGMOS, 2003). At the geographical scale of the ICESrectangle, the lack of high densities of cod suggest that movement of fishingeffort would save few fish (Blanchard et al., 2005). A 10-week closure ofpart of the North Sea in 2001 was deemed ineffective, and data were ofinsufficient resolution to separate any closure effects from additional factors(Council Regulation (EC) No. 259/2001). It has since been concluded thattemporal closures must be used with other management approaches to havea role in the future maintenance of North Sea cod biomass, and would berequired over several years and across larger spatial scales (Horwood et al.,2006; STECF, 2007).

Emerging management ideas include the introduction of OptimumRestorable Biomass to replace MSY as a target reference point (Ainsworthand Pitcher, 2008). This has been suggested as a suitable cost/benefitapproach to restoration of severely depleted fish stocks (Pitcher, 2008) anduses ‘Back To the Future’ simulation models to establish a restorationtrajectory from the present depleted system to a target of an historical systemafter establishing sustainable fishing (Ainsworth and Pitcher, 2008; Pitcher,2008; Pitcher and Forrest, 2004). Several optimal trajectories can besimulated based on restoration targets and economic profit scenarios. Thismultidisciplinary approach to restorative ecology suggests that rebuildingstocks to defined targets is the main goal for fisheries management (Paulyet al., 1998). In contrast, however, the North Sea Regional AdvisoryCouncil has recently issued advice to the European Commission that thecod recovery plan should be reviewed and targets changed from recoverybased on biomass to that based on fishing mortality (NSRAC, 2008).

6. Concluding Remarks

Most recovery plans for fish stocks are less than two decades old, andquantifying potential recovery is still proving difficult (Caddy and Agnew,2004; Caddy and Surette, 2005). Pelagic stocks appear to be responding



more positively than demersal stocks, and comparatively few stocks havebeen restored. The World Summit of Sustainable Development set a targetdate of 2015 for the management of all fish stocks at the level of MSY.No indication was given, however, as to how multi-species fisheries shouldbe managed to attain such a standard, and it is questionable whetherproposed targets are realistic in rapidly changing environments. Addition-ally, there is debate as to whether the focus of management should besustainability within an already depleted system, or the complete restorationand rebuilding of fish stocks to historic levels (Pitcher and Pauly, 1998).Moreover, reconstruction of past ecosystems may be an impossible policygoal if the past ecosystems existed under different climatic regimes (Pitcherand Forrest, 2004).

It is vitally important that the relative contributions of both fishingmortality and climate change on stock biomass, population structure andabundance changes are quantitatively understood to provide accurate andtimely advice for effective fisheries management (Horwood et al., 2006;Rose, 2004a,b). Predicting the effects of climate change on fish productiv-ity, as discussed in earlier sections of this chapter, is difficult due to incom-plete knowledge of the physiological and ecological mechanisms by whichfishes respond to changes in local and regional environmental conditions.Regime shifts also make predictions of future assemblage states problematicas the drivers force the assemblage into a new stable state which may differgreatly from the previous one (Cury et al., 2008; DeYoung et al., 2004;Mantua, 2004). Time series provide a basis for understanding the effects ofenvironmentally driven fluctuations in abundance and production of stocks,and provide the opportunity for deeper insights of the effects of highexploitation pressure (God�, 2003). However, investigations into themacroecological responses of wide ranging fishes such as Atlantic cod areproblematic due to the lack of uniformity in spatial data collection fromcommercial fisheries. In recent years, the availability of research vessel trawldata and standardized fisheries statistics has gone some way to address thisproblem. It is imperative that these data are now combined with detailedphysiological knowledge of the various life history stages, and an under-standing of interactions between cod and their environment, to allow moreaccurate predictions of future stock structure and abundance. Only then wewill be able to determine to what degree observed changes in cod popula-tions have been due to fishing and warming seas, and have the ability tointroduce effective management plans for mitigation of climate change andfisheries impacts.

The review of the European Common Fisheries Policy (CFP) in 2008acknowledges these factors and a Green Paper on the CFP reform sets out avision for European fisheries by 2020, which includes integration with thenew Integrated Maritime Policy and the Marine Strategy FrameworkDirective (CEC, 2009). The urgent need to review fisheries management



as part of the wider maritime environment and associated activities isrecognized (Greenstreet and Rogers, 2006), as are the additional impactsof climate change on exploited marine stocks. Fleet over-capacity is stillidentified as the fundamental problem that needs to be addressed. Moreactive stewardship, including appropriate use of the increasing scientificknowledge base, combined with emergent European and internationalmaritime directives is required if we are to redress the decline in Atlanticcod whilst stocks remain to be conserved.

In a rapidly changing world a precautionary approach is required.Climate change interacts with overfishing to increase the risk of decliningstocks, especially for species of boreal biogeographic origin such as Atlanticcod. Occasional large recruitment events can enable a single annual-breed-ing boreal species, which is dependent on the spring/summer temperatureregime, to persist in the face of climatic change. If longevity and size ofspawning fish are reduced, then persistence becomes less likely as theprobability of a major recruitment event during the lifespan of an individualis much reduced. As we describe in this chapter, it seems clear that climatecan act to exacerbate the deleterious effects of overfishing on marineecosystems; however, in this context, climate change effects should notexcuse overfishing. Moreover, given the mosaic structure of cod popula-tions with complex stochastic responses to climate change, the revolution ofmanagement measures must match the scale of these ecological processes.Management strategies with one size and approach, such as the CFP, willnot sufficiently well accommodate the complexities of cod interactions withchanging environments.

ACKNOWLEDGEMENTS

We thank G. Beaugrand for providing Fig. 3.5 and S. Cotterell for providing critical com-ments on an earlier version of this Chapter.We gratefully acknowledge funding support fromthe UK Department for Environment, Food and Rural Affairs (DEFRA), the UK NaturalEnvironment Research Council (NERC) Oceans 2025 Strategic Research Programmethrough Themes 6 (Science for Sustainable Marine Resources) and 10 (Integrating sustainedobservations for marine environmental monitoring) and The Worshipful Company ofFishmongers. MJG was supported by a Great Western Research Fellowship and DWS byan MBA Senior Research Fellowship.

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Chapter 3 Effects of Climate Change and Commercial Fishing on Atlantic Cod Gadus morhua

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