Resolving the effect of climate change on fish populations

Resolving the effect of climate change on fish populations

Adriaan D. Rijnsdorp, Myron A. Peck, Georg H. Engelhard, Christian Mollmann,and John K. Pinnegar

Rijnsdorp, A. D., Peck, M. A., Engelhard, G. H., Mollmann, C., and Pinnegar, J. K. 2009. Resolving the effect of climate change on fish populations. –ICES Journal of Marine Science, 66: 1570–1583.

This paper develops a framework for the study of climate on fish populations based on first principles of physiology, ecology, andavailable observations. Environmental variables and oceanographic features that are relevant to fish and that are likely to be affectedby climate change are reviewed. Working hypotheses are derived from the differences in the expected response of different speciesgroups. A review of published data on Northeast Atlantic fish species representing different biogeographic affinities, habitats, andbody size lends support to the hypothesis that global warming results in a shift in abundance and distribution (in patterns of occur-rence with latitude and depth) of fish species. Pelagic species exhibit clear changes in seasonal migration patterns related to climate-induced changes in zooplankton productivity. Lusitanian species have increased in recent decades (sprat, anchovy, and horse mack-erel), especially at the northern limit of their distribution areas, while Boreal species decreased at the southern limit of their distri-bution range (cod and plaice), but increased at the northern limit (cod). Although the underlying mechanisms remain uncertain,available evidence suggests climate-related changes in recruitment success to be the key process, stemming from either higher pro-duction or survival in the pelagic egg or larval stage, or owing to changes in the quality/quantity of nursery habitats.

Keywords: climate change, eco-physiology, ecosystem, fish, population dynamics.

Received 15 August 2008; accepted 9 February 2009; advance access publication 2 April 2009.

A. D. Rijnsdorp: Wageningen IMARES (Institute for Marine Resources and Ecosystem Studies), PO Box 68, 1970 AB IJmuiden, The Netherlands, andAquaculture and Fisheries Group, Department of Animal Science, Wageningen University, PO Box 338, 6700 AH, Wageningen, The Netherlands.M. A. Peck and C. Mollmann: Institute of Hydrobiology and Fisheries Science, University of Hamburg, Olbersweg 24, 22767 Hamburg, Germany.G. H. Engelhard and J. K. Pinnegar: Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft NR33 0HT, England, UK.Correspondence to A. D. Rijnsdorp: tel: þ31 317 487191; fax: þ31 317 487326; e-mail: [email protected].

IntroductionResolving the effect of climate change on fish populations is com-plicated, because climate change affects a multitude of environ-mental factors that may affect various processes at differentlevels of biological organization (Harley et al., 2006; Lehodeyet al., 2006; Tasker, 2008). For example, even if the effect ofchanges in an environmental factor on the physiology of an organ-ism is known, it will be difficult to evaluate the outcome of thisorganism-level physiological response at the population or ecosys-tem level (MacKenzie and Koster, 2004). Statistical analysis ofavailable time-series revealed changes in distribution and abun-dance of fish species that correlate with environmental variables(Perry et al., 2005; Weijerman et al., 2005; Heath, 2007).However, statistical correlations do not necessarily indicate under-lying processes (Koster et al., 2005).

It may be argued that it will be impossible to detect generalitiesin the response of fish populations to climate change, because thenumber of influential factors is too large and individual speciesmay differ too widely in their response. Nevertheless, we believethat it is possible to derive common patterns by developinghypotheses about the effect of climatic factors (abiotic variables)on fish populations, based on first principles and by takingaccount of different levels of biological organization (fromcellular- and organism-level eco-physiology to population- and

ecosystem-level responses; Figure 1). In this paper, we (i) reviewthe environmental variables and oceanographic features relevantto fish that are most likely to be affected by climate change, (ii)derive theoretical expectations from first principles and physio-logical and ecological theory, (iii) derive working hypotheses forfuture research, and (iv) review the empirical evidence from aselection of well-studied species in the Northeast Atlantic ecosys-tems against such a theoretical background.

Effects of climate change on the abiotic marineenvironmentThe effects of climate change are expected to differ in both magni-tude and direction among geographic areas (IPCC, 2007).Northern high-latitude areas will experience the largest increasein air temperature associated with the melting of sea ice (ACIA,2004). Intermediate increases in air temperature are expected forthe northern Nordic, Barents, and Baltic Seas, and the smallestincreases are expected in more southern areas, including theNorth and Mediterranean Seas. Ocean temperature will followincreases in air temperature, although to a lesser extent, owingto the high heat storage capacity of water masses. Shallow areaswill exhibit larger increases in sea temperatures than deeperwaters. In western Europe, the frequency of very cold wintersand of very hot summers is expected to decrease and increase,

# 2009 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved.For Permissions, please email: [email protected]

1570

respectively (Hulme et al., 2002). Changes in the strength and pre-vailing direction of wind over European marine areas remainuncertain, although the expectation is that there will be an increasein average and extreme windspeeds over northern Europe (Hulmeet al., 2002). Precipitation and river run-off are expected toincrease in northern Europe and decrease in southern Europe(Frei et al., 2006). In addition, the seasonality of run-off willchange, increasing in winter, but decreasing in spring in northwes-tern Europe. In warmer regions, such as the Mediterranean, differ-ences in the magnitude of river run-off between winter andsummer will increase (IPCC, 2007).

Climate change will affect a range of abiotic factors that aretightly linked to the production and distribution of fish popu-lations, and these climate-driven biotic changes will likely differbetween the open ocean, shelf seas, and coastal waters (Waltheret al., 2002; Lehodey et al., 2006). Although the importance ofthe various environmental factors varies regionally, some generalconclusions can be reached. Temperature, because of its pervasiveeffect on organisms, is important in all regions. Stratification(resulting from the interplay between temperature and windfor-cing) will also be an important factor in all regions, owing tothe effect of stratification on the vertical structure of marine eco-systems and on bottom-up processes. Changes in wind strengthand direction not only influence mixing and water circulation inthe open ocean, but also affect the strength of upwelling withinshelf and coastal regions. Sea ice is only of direct relevance inthe more northern regions, such as the Barents and Baltic Seas.In general, changes in salinity will have less of a direct effectupon most organisms, although salinity is a very importantabiotic factor in the Baltic, where it affects the buoyancy of eggsand early life stages of the prey species of fish (MacKenzie et al.,2007). The increase in carbon dioxide emissions has resulted inan increase in CO2 concentrations in the oceans (IPCC, 2007),reducing oceanic pH and changing the saturation horizons of ara-gonite, calcite, and other minerals essential to calcifying organisms(Feely et al., 2004).

Climate change and effects on fish populations andexploited ecosystems: theoretical expectationsFish have complex life cycles, comprising several distinct life-history stages (egg, larva, juvenile, and adult; Figure 1), each ofwhich may be affected in different ways by climate change. Over

their lifespan, fish typically increase in body size by a factor of105 (Rothschild, 1986), and successive life-history stages mayrequire spatially separated habitats. A prerequisite for populationpersistence is connectivity among habitats required by successivelife stages, allowing the survivors to mature and return to thespawning grounds to reproduce successfully (Figure 2; life-cycleclosure: Sinclair, 1988). Within these stage-specific habitats, fishmust experience suitable abiotic conditions, find food forgrowth, and find shelter to escape from predation or disease.Demersal and pelagic species differ in their habitat requirements.Pelagic species remain within the three-dimensional pelagichabitat (although some species, such as herring, require specificdemersal habitats for spawning), whereas demersal speciesdisplay a distinct transition from the three-dimensional pelagicrealm of (eggs and) larvae to the two-dimensional habitat of thedemersal stages. During their life-history transitions, augmented

Figure 1. Climate change will affect fish populations on all levels oforganization.

Figure 2. Complex life cycle and life-cycle closure of (a) demersaland (b) pelagic fish species. Fish life-history stages inhabit differenthabitats and demonstrate ontogenetic niche shifts. Pelagic fishremain in the pelagic habitat throughout their life cycle, but stagesmay inhabit different water masses. Demersal fish are characterizedby a pelagic egg and/or larval stage and a demersal juvenile andadult stage. At major habitat shifts, individuals may be lost (vagrants,dashed arrows). Relative habitat size may differ among the stages andmay form a bottleneck in determining population abundance.

Resolving effects of climate change on fish populations 1571

through hydrographic transport or directed migration, animalsmay be lost from the population (dashed arrows in Figure 2).Because the life cycle is embedded in a geographical setting, thesize of the various habitats differs, which could result in bottle-necks at specific life-history stages (dashed squares in Figure 2).

Climate-driven changes in fish populations may result fromfour, often interlinked, mechanisms: (i) a physiological responseto changes in environmental parameters, such as temperature,(ii) a behavioural response, such as avoiding unfavourable con-ditions and moving into new suitable areas, (iii) populationdynamics, through changes in the balance between rates of mor-tality, growth, and reproduction in combination with dispersal,which could result in the establishment of new populations innew areas, or abandonment of traditional sites, (iv) ecosystem-level changes in productivity and/or trophic interactions. Inaddition, (v) commercial exploitation greatly affects the abun-dance and distribution of fish and may interact with the effectsof climate change. In the following sections, we expand uponeach of these five themes with regard to potential climate effectsto derive a suite of testable hypotheses.

Physiological responseAt the individual level, direct changes in the environmental factors(such as local temperatures) will invoke changes in physiologicalrates. Insight regarding such eco-physiological responses will becrucial to interpret the mechanisms underlying observed changesin distribution or patterns of behaviour. Species can only toleratea specific range of environmental conditions that, among otherfactors, places constraints upon their range of distribution. Fry(1971) proposed how different environmental factors can loadmetabolic costs and affect the metabolic scope. Recently, Portnerand Knust (2007) demonstrated that the partial oxygen pressure(PO2) within blood provided a direct measure of metabolicscope (Figure 3). Low levels of blood PO2 outside of pejus temp-eratures (pejus ¼ getting worse) reflect the reduction in aerobicscope, limiting the energy available for activity, growth, reproduc-tion, and other vital rates. Pejus temperatures are not fixed, but canbe modified to some extent by population-specific adaptation tolocal environmental conditions (arrows in Figure 3). Differences

exist in the tolerance of extreme temperatures within species(e.g. related to differences in acclimation) and/or betweenspecies (differences in thermal physiology). For example, areview of the upper and lower lethal temperatures of variousmarine fish species indicated that thermal tolerance changedmarkedly with latitude (MAP, unpublished data). The range of tol-erable temperatures was narrower in fish inhabiting high and lowlatitudes and wider for fish inhabiting intermediate latitudes(MAP, unpublished data). Although caution must be taken notto oversimplify the estimates of thermal preference gauged fromfish in the field (because other environmental factors can modifypreferred temperatures), patterns of change in tolerance maygive a first approximation of the relative effects of climate-driventemperature changes (Figure 4a). The relationship also allows usto use the geographical distributions of species (Arctic, Boreal,Lusitanian, Tropical, Atlantic) as a classification scheme to evalu-ate the expected response.

There is evidence of an ontogenetic shift in temperature toler-ance of a species (Figure 4b), such that optimum temperatures forgrowth decrease with increasing body size of juveniles and adults(Fonds et al., 1992; Imsland et al., 1996; Yamashita et al., 2001;

Figure 3. At the cellular level, optimal and suboptimal temperaturesare reflected by changes in the rates of aerobic and anaerobicmetabolism. Optimal temperatures coincide with the highest levelsof PO2. Pejus temperatures (Tpejus) denote the onset of limits inaerobic scope and increased energy demands. Critical temperaturesare those where aerobic scope is zero, anaerobic metabolism ismeasurable and, at the upper Tcritical, cellular-level stress proteins areproduced. At higher temperatures (Tdeath), denaturation and deathoccur. Arrows denote population-specific adaptation (after Portnerand Knust, 2007).

Figure 4. Conceptual diagram of the changes in suitable habitats(based on water temperature) with (a) latitude of the species and/orpopulation and (b) by life stage. The arrow (a) denotes a range oftolerable temperatures measured for adults during maturation andspawning. Data in a and b are from MAP (unpublished data) andIrvin (1974).

1572 A. D. Rijnsdorp et al.

Peck et al., 2003; Portner and Farrel, 2008). This mechanism canexplain the ontogenetic shift in habitats observed in several fishspecies where young stages occur in shallower waters than older,larger stages (Heincke’s Law; Heincke, 1913). In some species,eggs and larvae have been observed to have a narrower range oftolerable temperatures than other life-history stages (specificallyjuveniles) making these early life stages more vulnerable tochanges in temperature (Irvin, 1974; Portner and Farrel, 2008).If this is a general phenomenon, it may provide a powerful basisfor predicting the potential response of a species to changes intemperature, but further research is needed to test its generality.The sensitivity of larval stages to climate change may be furtherincreased, because of their small body size, which will makethem less capable of selecting and migrating towards a suitablehabitat, and because of their reasonably high (mass-specific) meta-bolic rates and lower energy reserves. This will make them morevulnerable to mortality during periods of adverse environmentalcondition, such as periods of food shortage.

Several authors have stated that marine fish are likely to be lessaffected by an increase in oceanic CO2 and a correspondingdecrease in pH compared with invertebrate groups, such as mol-luscs and corals (Feely et al., 2004; Orr et al., 2005; Fabry et al.,2008). However, laboratory studies have revealed that manipu-lation of pH and CO2 can have dramatic consequences on thephysiology, metabolism, and reproductive biology of fish, withegg fertilization and survival of early developmental phasesbeing primarily affected (Ishimatsu et al., 2005).

It is worth noting that responses at higher levels of organization(population, community, and ecosystem) to climate change areultimately driven via differences in physiological responses thataffect trophodynamic relationships. For example, physiologicalresponses to a change in temperature can differ betweenprimary, secondary, and tertiary consumers, thereby influencingtrophic coupling (Freitas et al., 2007) via changes in productivityor phenological shifts and match–mismatch dynamics (Cushing,1990).

Behavioural responseOrganism-level responses, such as changes in behaviour, can resultfrom changes in key abiotic factors, such as temperature or O2, butthe presence (and/or strength) of the response will depend on theability of the animal to detect environmental gradients and navi-gate accordingly. In contrast to early feeding larvae of tropicalmarine fish, which can exhibit reasonably strong swimmingcapacity (Leis, 2006), larvae of most temperate marine fishspecies have no, or very limited, swimming ability. Temperatemarine fish larvae can respond to reasonably intense environ-mental signals (e.g. turbulence avoidance; Franks, 2001), buthave little capacity to avoid unfavourable environments thatrequires swimming over large (km) distances.

In later (juvenile and adult) life stages, individual fish canclearly respond to a change in temperature (Woodhead, 1964;Berghahn, 2000) and often exhibit active temperature preference(Tsuchida, 1995). Some elasmobranchs are extremely sensitive totemperature variation (e.g. they can respond to changes of,0.0018C; Brown, 2003) and some sharks move to deeper waterbefore the onset of severe storms (Heupel et al., 2003).Naturally, even for individuals in these later life stages that havestrong swimming capacity, knowledge of the location of optimalhabitats will not be perfect. Field studies on thermal habitatsrevealed that fish may inhabit and occupy areas with suboptimal

temperatures even if areas with more optimal temperatures arewithin reach (Neat and Righton, 2007), but optimal habitats willalso be determined by other factors such as food. Behaviouralchanges can have unexpected consequences. For example,because of an increase in temperature, fish swimming speedincreases (Peck et al., 2006). In addition, fish can behave differentlyin response to oncoming fishing gear making them more (or less)vulnerable to capture (Winger, 2005). Finally, at longer temporalscales, climate-driven changes in temperature can modify thephenology of annual migrations to feeding and/or spawninggrounds, as already observed (Carscadden et al., 1997; Simset al., 2004), and predicted (Huse and Ellingsen, 2008), for tem-perate marine species. It can be inferred that the behaviouralresponse to changes in environmental conditions will depend onthe rate of change and/or the spatial scale over which conditionschange relative to fish body size or developmental stage becausethe capacity for avoidance responses increases with increasingbody size.

Population dynamic responseProductivity of fish populations, in terms of biomass, is deter-mined by recruitment, growth, and mortality. Most commercialspecies are broadcast spawners producing millions of eggs(Rothschild, 1986). Mortality rates of early life-history stages arevery high and variable, generating large fluctuations in annualrecruitment. Relatively small changes in growth and mortalityrates during the egg and larval phases can have a large effect onthe recruitment success of populations (Figure 5; Houde, 1987).Because the early life-history stages are likely to be more sensitive

Figure 5. Population-level effects of climate: relationship betweenthe ratio of individual growth rate (G, % d21) and mortality rate(Z, % d21). Increase in the biomass of cohorts and successfulrecruitment is only possible when Z/G , 1.0. Body sizes at whichthis occurs differ among species. The grey area denotes the range oftrajectories calculated for early life stages of five marine fish speciesby Houde (1987). A variety of responses to climate change is possible.The critical body size (size at Z/G ¼ 1.0) (a) may shift or (b)recruitment may fail, represented when Z/G is always .1.


to climate change (see the section on “Behavioural response”), weexpect that climate change will have a major effect on the distri-bution and abundance of fish through its influence on recruit-ment. The mechanism will be either the match–mismatchbetween the timing of reproduction relative to the production oflarval food and/or predators (Cushing, 1990; van der Veer et al.,2000; Platt et al., 2003; Temming et al., 2007), or the connectivity(retention or transport) between spawning and nursery areas(Sinclair, 1988; Wilderbuer et al., 2002).

Interstock comparisons indicated a dome-shaped pattern in therelationship between recruitment strength and spawning tempera-ture experienced during the spawning season, with maximumrecruitment at an intermediate temperature in cod and sprat(Brander, 2000; MacKenzie and Koster, 2004). In cod, this temp-erature was close to the optimal temperature for larval growth(Brander, 2000). However, the effects of climate on recruitmentare not limited to processes acting during the egg and larvalstages, but may extend to later (juvenile and adult) life stages.For example, year-class strength in sprat appears to be establishedduring the post-larval or juvenile period (Koster et al., 2003), andlow growth rates and poor condition of juvenile sprat can resultfrom top-down control of their zooplankton prey resources(Baumann et al., 2007).

Productivity will also be influenced by the effect of temperatureon growth rate (Brander, 1995; Teal et al., 2008). In a comparativestudy of 15 cod stocks, sevenfold differences in the productivityamong stocks corresponded to the differences in the temperatureof the environment (Dutil and Brander, 2003). Fish species aregenerally plastic in their age and size at sexual maturity. Anincrease in juvenile growth, as well as an increase in temperature,may result in a decrease in the length and/or age of first matu-ration, affecting growth of adults as surplus energy is channelledinto reproduction at an earlier age and/or smaller size (Heinoet al., 2002).

Mortality may be high when temperature conditions reachextreme values. Low temperatures during winter may increase mor-tality, especially of smaller fish that have reasonably fewer energyreserves compared with larger conspecifics (Post and Evans, 1989;Sogard, 1997). During severe winters in the North Sea, high mor-tality has been reported for Lusitanian species, such as sole andconger eel, but only rarely for Boreal species, such as cod, plaice,and dab (Woodhead, 1964). Mortality may also be high duringhypoxic (or anoxic) conditions, as has been reported for theKattegat (Diaz, 2001). Although mass mortalities during summerin relation to harmful algal blooms (Yin et al., 1999; Heil et al.,2001) have been reported elsewhere, no records are known for theNortheast Atlantic. Climate change may have the most dramatic(negative) effects on the productivity of fish populations by increas-ing the frequency of these “episodic” extreme events.

For some broadcast spawning fish species, there is evidence thatthe size of populations is determined by the size and availability ofspawning and/or nursery habitats (Rijnsdorp et al., 1992; Gibson,1994; Sparholt, 1996; MacKenzie et al., 2000). Limits on the avail-ability of these habitats may act as a bottleneck for population size(and/or productivity). In these cases, the focus should be on theeffect of climate change on the critical life-history stage(s).Whether this relationship is applicable will depend on the relativesize of the habitat in relation to that of other life-history stages andis determined by the specific geographic setting.

Life-cycle closure may be affected if climate change influencesthe connectivity between the habitats of successive life-history

stages (Sinclair, 1988). For instance, changes in ocean climatemay affect the transport of eggs and larvae between the spawninggrounds and the nursery areas (Corten, 1986; van der Veer et al.,2000; Wilderbuer et al., 2002), or the climate effect on thetiming of spawning migrations may influence the arrival of theadults at the spawning grounds (Sims et al., 2004).

Ecosystem responseClimate change can affect all trophic levels of marine ecosystems,eventually resulting in changes in the productivity and distributionof fish stocks. On the lower trophic levels, climate is expected toaffect primary and secondary productivity through its effect onphysiological rates of species, the availability of nutrients (upwel-ling or stratification), and the advection of water into shelf areasand enclosed basins. On a qualitative level, the increase inaverage and extreme winds over European marine areas mayincrease upwelling, enhance primary production, and eventuallyincrease fish productivity (Dickson et al., 1988; Jahncke et al.,2004; Rykaczewski and Checkley, 2008). A further effect will bethe translocation of deep-water species into shelf seas (Blanchardand Vandermeirsch, 2005). Within shelf areas, increasedwarming will result in earlier water mass stratification (if notbalanced by increased wind-mixing), which will affect the timingof the spring bloom and the level and composition of primary pro-duction. Primary productivity may also be influenced by changesin precipitation and river run-off. In areas where coastal pro-duction is enhanced by nutrient input (from either organicmatter or nutrients through rivers), changes in precipitation willlikely affect coastal fish production. Hence, an increase in riverrun-off into the Bay of Biscay may enhance the productivity ofsole, whereas a decrease in run-off into the Mediterranean Seacould result in a decrease in the productivity of sole in thatregion (Salen-Pickard et al., 2002; Le Pape et al., 2003;Darnaude et al., 2004).

Climate-driven changes in the level of primary productivity willlikely be accompanied by phenological changes that affect lowertrophic level coupling and eventually the recruitment success ofmarine fish (Cushing, 1990). Changes in phenology and a resultingtrophic mismatch have been reported for the North Atlanticplankton community where the level of response differs through-out the community and the seasonal cycle, resulting in a mismatchbetween trophic levels and functional groups (Beaugrand et al.,2003; Platt et al., 2003; Edwards and Richardson, 2004). Thistrophic mismatch can finally affect fish stock recruitment, asreported for the North Sea cod/Calanus finmarchicus interaction(Durant et al., 2005). To some extent, biophysical modellingapproaches can be used to identify “mediator chains” (Dippner,2006) describing how climate-induced changes in physicalfactors (e.g. stratification) are propagated up the foodweb toaffect processes (e.g. match–mismatch dynamics) important tothe survival of marine fish (Daewel et al., 2008a, b).

Beyond a strict bottom-up control, a number of differentcontrol patterns exists within foodwebs (i.e. top-down and wasp-waist controls) and climate-induced changes will depend on theprevailing control pattern, illustrated in Figure 6, making it chal-lenging to predict how climate change will affect marine fishstocks within those foodwebs (Stenseth et al., 2002; Jenningset al., 2008). There is a continuing discussion on whether ecosys-tems are primarily regulated by bottom-up or top-down processes(Frank et al., 2007). The traditional view in marine ecology of abottom-up control (Strong, 1992) is supported by a number of


recent studies (Ware and Thomson, 2005; Greene and Pershing,2007). Other studies, however, suggest that the dominance ofbottom-up control can switch to top-down control, resulting introphic cascades initiated by overfishing (Worm and Myers,2003; Frank et al., 2005; Daskalov et al., 2007; Mollmann et al.,2008). Moreover, recent studies emphasize the simultaneousimportance of both climate- (bottom-up) and fisheries-induced(top-down) effects in marine ecosystem reorganizations(Mollmann et al., 2008, 2009). The strength of these processesalso appears to depend on foodweb complexity and thermal con-ditions (Frank et al., 2007), and may oscillate between bottom-upand top-down controls (Hunt et al., 2002; Hunt and McKinnell,2006). The control change can be triggered by both climatechanges and overfishing (Litzow and Ciannelli, 2007; Casiniet al., 2008a, b). Therefore, predicting the effect of climatechanges on marine ecosystem development, and hence the pro-ductivity of different fish stocks, particularly in light of theadditional (interacting) pressure of exploitation, will be a grandchallenge for the future (Greene and Pershing, 2007).

Effects of fishingFisheries might interact with climate change in causing changes infish populations, through various mechanisms. Climate changecould affect the distribution of particular species and hence theirsusceptibility to particular fishing fleets, becoming more or less“catchable” as a result. Similarly, climate-related distributionshifts may affect the protective capabilities of closed-areas,because species or life stages may shift outside the boundaries ofthe protected area and hence become vulnerable to fishing (e.g.the North Sea Plaice Box—Van Keeken et al., 2007).

Extensive fishing may cause fish populations to become morevulnerable to short-term natural climate variability (O’Brienet al., 2000; Walther et al., 2002; Beaugrand et al., 2003;Anderson et al., 2008), by making such populations less able to“buffer” against the effects of the occasional poor year classes.During recent decades, there has been a clear, positive correlationbetween temperature and recruitment in Northeast Arctic cod;however, this link was weak or non-existent in earlier periods(Ottersen and Stenseth, 2001). A major implication is thatfishery-induced impoverishment of stock structure (reduced andfewer ages and smaller sizes) can increase the sensitivity of a pre-viously “robust” stock to climate change (Ottersen et al., 2006).Conversely, long-term climate change may make stocks more vul-nerable to fishing, by reducing the overall carrying capacity of thestock, such that it might not be sustained at, or expected to recoverto, levels observed in the past (Jennings and Blanchard, 2004).

Fishing will have a major influence on the size structure andspecies composition of fish assemblages and thus will affect preda-tor–prey relationships (Rice and Gislason, 1996; Daan et al.,2005). Fishing will interact with global warming, because bodysize generally increases with latitude (Belk and Houston, 2002)and small fish species may take advantage of the removal of thelarger predatory fish (Daan et al., 2005). Fishing may also affectecosystem control causing bottom-up systems to becometop-down controlled systems (see the section “Ecosystemresponse”). How climate change will interact with fishing willdepend on the species affected and eventually on the prevailingpatterns of ecosystem structure and function (Heath, 2005).Hence, the response of ecosystems under climate and fishingpressure is currently difficult to predict.

Figure 6. (a) Propagation of climate-induced changes at the bottom of the foodweb depends on dominance of bottom-up control (lowerpanel) or a top-down-induced cascade pattern (upper panel); (b) schematic on a potential control change in the upper trophic levels ofmarine ecosystems (y-axis: moving correlation between two trophic levels, positive correlation coefficients indicating bottom-up control,negative coefficients indicating top-down control). Overfishing and/or climate change (arrow) may induce a change from the original state, i.e.bottom-up control (Strong, 1992) to top-down control, potentially inducing multilevel trophic cascades. The velocity and strength of thechange, i.e. the vulnerability of an ecosystem for a control change, depends on the level of biodiversity and the ambient temperature (Franket al., 2007; Litzow and Ciannelli, 2007).


Working hypothesesThe response of fish populations to climate change will differbetween species. The difference may be related to their adaptationsto the environmental conditions in their respective habitats. Assuch, the biogeographic affinities of the species may be used as aproxy for the expected response to a change in temperature [seeYang (1982) on biogeographic affinities of North Sea fishspecies]. Populations living at the border of the distributionrange are expected to live close to the limits of their range of phys-iological tolerance, so will be more vulnerable to changes in abioticconditions than populations living in the centre of the distributionarea (Miller et al., 1991). Because water temperature is correlatedwith water depth, fish may move into deeper water duringsummer to avoid the warmer water in shallow areas (Dulvyet al., 2008). This leads to the first set of working hypotheses:

H1a: Populations at the limits of their latitudinal range willexhibit stronger responses than those occurring within habitatsin the centre of their latitudinal distribution;

H1b: Northerly species at the southern limits of their distri-bution will decrease in abundance and southerly species willincrease at their northern limit;

H1c: Northerly species are expected to retreat into deeper,cooler waters, in response to an increase in surface watertemperature.

We expect that the response of species to climate change will beinfluenced by their habitat requirements (pelagic, demersal, anddeep-water species), life-history characteristics (short- or long-lived; specialist or generalist), and trophic position within the eco-system (apex predators or forage fish). Although many “pelagic”fish species have early life stages residing in the “demersal” habitatsand vice versa, fish that are strictly pelagic (all life stages) inhabitwater masses with certain abiotic conditions that may change intheir spatial distribution, due to climate change, whereas strictlydemersal fish may have specific habitat requirements that are geo-graphically fixed owing to seabed characteristics. Environmentalconditions tend to be more unvarying at greater depths, althoughdeep-water fish may be influenced indirectly by changes in pro-ductivity above them (food availability) and by changes in deep-water currents. Generalists can adapt to the prevailing patternsof food availability, whereas specialists are strongly dependenton the prospects of particular prey organisms. Short-livedspecies characterized by high reproductive rates (so-calledr-strategists) are likely to track the changes in their environmentrelatively rapidly, whereas the responses of long-lived species(K-strategists) will be slower (Perry et al., 2005). The ability totrack the changes in their environment will apply to an improve-ment and a deterioration of the environmental conditions. Thisleads to the following hypotheses:

H2a: Pelagic and demersal species will differ in their responses,because the former can more easily follow changes in watermasses than the latter, which have more geographically fixedhabitat requirements;

H2b: Deep-water fish species may be less affected by climatechange than shelf or coastal species;

H2c: Fish species with narrow dietary preferences will be moresensitive to climate change, than generalists;

H2d: Short-lived species will exhibit stronger responses and willbe better equipped to adapt to changes in their environmentthan long-lived species.

Populations can survive in systems where suitable habitats forthe different life-history stages are available and are connected,allowing life-cycle closure (Sinclair, 1988). If the habitat for acertain life-history stage is spatially restricted, a change inhabitat suitability of this stage will make the species more sensitiveto climate change than those that do not have spatially restrictedhabitat requirements. Populations living in areas with a large het-erogeneity in environmental conditions, or that migrate over largedistances, will more likely be able to survive by selecting the appro-priate environments than those living in large areas with a morehomogeneous environment. This leads to the followinghypotheses:

H3a: Species with spatially restricted habitat requirementsduring part of their life history will be more sensitive toclimate change than those without specific habitatrequirements;

H3b: Fish populations in oceanographic systems with a highvariety of mesoscale features will display less influence ofclimate change.

Fishing will reduce the size and age structure of a populationand reduce its bet-hedging capabilities that would allow it totrack conditions suitable for the survival of eggs and larvae(Rothschild, 1986; Ottersen et al., 2006). In addition, fishingmay result in a reduction in genetic variability, which would nega-tively affect the possibilities of an evolutionary response to climatechange and the ability of depleted stocks to recover (Andersonet al., 2008).

H4: Fish stocks under intense exploitation will be more vulner-able to climate change than those experiencing low fishingpressure.

The ecosystem response to climate change will depend on theresponse of the individual species and the resulting effect on tro-phodynamic interactions among species. Different species withina foodweb will not all respond in the same way to climatechange. Species-rich systems, characterized by many weak,readily interchangeable feeding links, rather than a few stronglinks, are likely to be more stable, because different species maytake over vacant ecological functions (Link, 2002) and may bemore resilient (Frank et al., 2007) in the face of climate change.Climate change will not necessarily result in gradual and predict-able changes in fish populations and ecosystem state. Ecosystemsmay exhibit multiple stable equilibria and climate change maypush systems into a new equilibrium (Scheffer and Carpenter,2003). Once a “regime shift” has occurred, it may be disproportio-nately difficult to return to the original state (Beaugrand, 2004;Daskalov et al., 2007; Mollmann et al., 2008).

H5a: Ecosystems with simple trophic structure will exhibitmore rapid responses to climate change than ecosystems withmore complex trophic structure;

H5b: Changes in ecosystem structure caused by climate changemay be abrupt.


The introduction of non-native species to a marine ecosystem,and their subsequent establishment, may cause effects that rangefrom almost undetectable to catastrophic (e.g. the complete dom-ination and displacement of native communities; Eno et al., 1997).Improved environmental conditions, as well as new shippingroutes, will facilitate the spread of warm-water fish species andpathogens. New species may be introduced to the Arctic,because of ice-free shipping routes (ACIA, 2004), and further colo-nization of the Mediterranean Sea by tropical species might beanticipated, because of the Suez Canal.

H6: Because of improved local conditions, an increasednumber of exotic warm-water fish species (and fish pathogens)will become established in European waters.

Observed changes in distribution and abundanceIn this section, changes in distribution, abundance, and growth ofa selection of fish species in the northeastern Atlantic are reviewed(Table 1) against the background of the above working hypotheses.Species were selected for which sufficient data were available (com-mercial species) and that represented different “ecotypes” combin-ing the biogeographic affinity (Lusitanian, Boreal, Atlantic),habitats (pelagic or demersal; Atlantic or shelf), and longevity(short, medium, long).

Changes in abundance and distribution of northeasternAtlantic marine species support hypothesis 1. Lusitanian specieshave increased in recent decades (sprat, anchovy, and horse mack-erel), especially at the northern limit of their distribution areas,while Boreal species generally decreased at the southern limit oftheir distribution range (cod and plaice), but increased at thenorthern limit (cod). A shift in distribution to deeper waterswas recorded in the Boreal species cod and plaice (Hedger et al.,2004; Perry et al., 2005; van Keeken et al., 2007; Dulvy et al., 2008).

Comparison of the changes in distribution between pelagic anddemersal species provides support for hypothesis 2. For the pelagicspecies, changes in distribution patterns have been observed thatare related to climate-induced changes in the distribution oftheir food (herring: Toresen and Østvedt, 2000; Corten, 2001a,b; horse mackerel: Borges et al., 1996; Iversen et al., 2002; mackerel:Reid et al., 2001; ICES, 2007). Changes in plankton have beenlinked to changes in climate (Beaugrand et al., 2002; Richardsonand Schoeman, 2004). A comparison between demersal andpelagic species tentatively suggests that changes in the distributionof the former are smaller than those of the latter. The northwardshifts in cod have been related to the transport of eggs andlarvae, but not to a northward movement of the demersal stages(Rindorf and Lewy, 2006).

With regard to the underlying mechanisms, the available evi-dence suggests that the observed changes in productivity are atleast in part related to a climate-related change in recruitment(herring, anchovy, sprat, cod, plaice, and sole), either owing tohigher production or survival in the egg or larval stage (herring,anchovy, sprat, cod) or to a change in the quality/quantity ofthe nursery habitat (plaice and sole). In sole and plaice, there isevidence that the timing of spawning is influenced by the tempera-ture during the spawning period (Teal et al., 2008). In the westernAtlantic, such an effect is also reported for cod (Hutchings andMyers, 1994). The negative relationship between recruitmentand temperature in sole in the North Sea contrasts with theexpected positive relationship in this Lusitanian species.

Temperature-related changes in growth have been reported forcod (Brander, 1995; Dutil and Brander, 2003) and 0-group soleand plaice (Teal et al., 2008). The mean length of sole, aLusitanian species, has increased in autumn, because of an increasein growth rate, and there has also been an increase in the length ofthe growing season. However, no change in mean length wasobserved in plaice, a Boreal species that exhibited an increasedgrowth rate early in the season, but reduced growth rate duringsummer when temperature exceeded their optimal temperature.Growth rate of older age groups of sole and plaice exhibited adome-shaped pattern since the late 1950s, with relatively highgrowth rates between the mid-1960s and the mid-1980s, whichwere not correlated with changes in temperature (Millner andWhiting, 1996; Rijnsdorp and van Leeuwen, 1996). The availabledata do not allow a quantitative comparison of the relativeeffects of the climate-induced changes in recruitment and injuvenile and adult growth rates on productivity. The results ofthe selected species did not allow hypotheses 3–5 to be tested.

With regard to the hypothesis about invasive species (H6),there is strong evidence that increasing connectivity between geo-graphically distinct areas may result in major changes in ecosys-tems. The opening of the Suez Canal in 1869 allowed entry ofIndo-Pacific and Red Sea biota into the southeasternMediterranean Sea, where these so-called lessepsian migrantsnow dominate the fish community (50–90% of fish biomass).For many decades, this migration was very limited, partlybecause of extremely high salinity within the Suez Canal, wheredry salt valleys had existed previously. With a warming trend ofthe seawater and a significant drop in the Canal’s salinity to“normal” marine levels (Mavruk and Avsar, 2007), recordnumbers of newly established non-native fish species have beenobserved recently in the southeastern Mediterranean Sea, resultingin the creation of a human-assisted Erythrean (Red Sea) bioticprovince (Goren and Galil, 2005). Trans-located fish species,such as the round goby, have also become established in theBaltic Sea (Karlson et al., 2007).

DiscussionWe propose a framework for the study of the effect of climatechange on fish populations (Figure 1) and derive a set of testablehypotheses based on first principles. Similar to Harley et al. (2006),the framework recognizes that climatic factors will affect successivelife-history stages (eggs, larvae, juveniles, and adults) in differentways and via processes acting at all levels of biological organization(from physiological responses of individual organisms topopulation-level disturbances and to ecosystem-level/trophody-namic effects). The different levels of organization can be viewedas a mechanistic chain. Population-level processes will onlyoperate within the appropriate physiological envelope of abioticconditions. Equally, ecosystem-level processes will only be relevantwhen life-cycle closure is possible within the specific geographiclocation providing interconnection among suitable habitats ofsuccessive life-history stages. This framework structures the analy-sis of the published data and provides the basis for modellingstudies to test hypotheses. In our analysis, we have mainlyfocused on the effects of temperature, although other factorsmay be incorporated.

Knowledge of the eco-physiology of different life stages willprovide a strong basis to infer the response of a species to achange in temperature (and other climate-driven changes inabiotic factors). It will allow us to define the bioclimate envelope


Table 1. Review of the observed changes in distribution, abundance, and production related to climate change in a selection ofcommercially exploited species of contrasting ecotypes.

Change Comments Source

Pelagic species1. Atlantic herring, Clupea harengus: Shelf, Boreal, Medium

Herring populations exhibit multidecadalvariations

Multidecadal variations related to climate variations(Russel cycle) and fisheries. Great salinity anomalyaffected larval transport in North Sea. Recruitmentrelated to temperature; positive relationship innorthern population (Norwegian spring-spawningherring)

Corten (1986, 2001b), Alheit andHagen (1997), Toresen andØstvedt (2000), and MacKenzieet al. (2007)

Norwegian spring spawners: changes inoverwintering, feeding, and spawning areas;more northerly distribution in North Sea withwarmer temperatures

Distribution changes related to changes in fooddistribution

Toresen and Østvedt (2000), Corten(2001a, b), and Holst et al. (2002)

2. Anchovy, Engraulis encrasicolus: Shelf, Lusitanian, ShortIncrease in abundance in northern areas

(North Sea). Decrease in Bay of BiscayIncrease in North Sea may be temperature-related.

Change in Bay of Biscay related to fishing. Role ofclimate is uncertain

Boddeke and Vingerhoed (1996) andMacKenzie et al. (2007)

3. Sprat, Sprattus sprattus: Shelf, Lusitanian, ShortIncrease in abundance and production in

Baltic; stock collapse in Black SeaIncreased recruitment at higher temperature (and

reduced cod predation) at northern limit anddecrease at higher temperature at southern limit(Black Sea)

Koster et al. (2003), MacKenzie andKoster (2004), Daskalov et al.(2007), and Mollman et al. (2008)

4. Mackerel, Scomber scombrus: Atlantic, Atlantic, LongNorthward shift in spawning and feeding

areas. Earlier spawning. Increased variation inrecruitment

– Reid et al. (2001) and ICES (2007)

5. Horse mackerel, Trachurus trachurus: Atlantic, Atlantic–Lusitanian, LongIncrease in northern areas resulting from

change in migration to feeding areas– Borges et al. (1996) and Iverson et al.

(2002)Demersal species

6. Atlantic cod, Gadus morhua: Shelf, Boreal, LongIncrease in abundance in northern areas at

higher water temperaturesArcto-Norwegian cod: increase in recruitment at

higher temperatures (overfishing increasedsensitivity of the relationship). Temperature-relatedshifts in spawning sites

Planque and Fredou (1999), Ottersenet al. (2006), and Heath (2007)

Growth Body growth is strongly temperature-related Brander (1995)Productivity changes in Baltic related to

inflow of saline Atlantic waterVolume of spawning habitat where eggs and larvae

can survive depends on inflow of saline water fromNorth Sea

Sparholt (1996) and MacKenzie et al.(2000)

Decrease in abundance in southern areas(and also North Sea)

Recruitment related to climate effects onzooplankton production and to temperature

O’Brien et al. (2000) and Beaugrandet al. (2003)

Northward shift in distribution within NorthSea

Likely resulting from different fishing pressure andlocal survival of eggs/larvae

Hedger et al. (2004), Perry et al.(2005), and Rindorf and Lewy(2006)

Shift to deeper waters in North Sea No evidence of cod actively swimming north or todeeper water

Hedger et al. (2004) and Neat andRighton (2007)

7. Plaice, Pleuronectes platessa: Shelf, Boreal, LongDistribution shifted to deeper waters (North

Sea)Temperature is a likely cause, although other factors

may have contributedPerry et al. (2005) and Van Keeken

et al. (2007)Decrease in abundance in southern nursery

grounds (Bay of Biscay)– Desaunay et al. (2006)

Recruitment negatively related totemperature in waters around the UK

– Fox et al. (2000)

Timing of spawning advanced in warm years(North Sea)

– Teal et al. (2008)

Changes in growth do not correlate withtemperature, except in 0-groups

Growth related to population abundance,eutrophication, and bottom trawling. Growth of0-groups determined by temperature

Rijnsdorp and van Leeuwen (1996)and Teal et al. (2008)

8. Sole, Solea solea: Shelf, Lusitanian, LongRecruitment related to river run-off (Bay of

Biscay, Mediterranean Sea)Nursery habitat quality/quantity increases Salen-Picard et al. (2002), Le Pape

et al. (2003), and Darnaude et al.(2004)

Continued


and evaluate the change in habitat suitability for the different lifestages (Pearson and Dawson, 2003), or evaluate whether observedtemperature changes may be responsible for the change in thepopulation abundance, such as for the eelpout in the WaddenSea (Portner and Knust, 2007). Although we have mainly dealtwith temperature, climate change may also affect oxygen, salinity,and ocean pH. These factors may load the metabolic scope anddecrease the tolerance range of the organism (Fry, 1971), sub-sequently making it more vulnerable to climate change.

Eco-physiological data can also indicate whether species orspecies-groups may differ in sensitivity to change in temperatureaffecting trophic relationships. A review of experimental data onthe optimum temperature and temperature tolerance ranges of anumber of fish and (epi-)benthic species revealed clear speciesdifferences, suggesting that an increase in temperature wouldresult in a shift in the predation pressure from cod and gobies tobrown shrimps (Freitas et al., 2007). If the temperature sensitivityof species groups (e.g. autotrophs and heterotrophs; ectothermsand endotherms; and taxonomic groups of different complexity)differ in a systematic manner, this will provide a basis for predict-ing how a temperature change may affect species and species inter-actions. Research into differences in sensitivity among species(groups), as well as the underlying mechanism, is needed.

Although climate change may influence the vital rates/pro-ductivity of a fish stock (growth, mortality, and recruitment), wesuggest that early life-history stages will be most sensitive to theeffects of climate change. The underlying mechanisms may differamong species or stocks and will depend on the trophic position(Frank et al., 2007). The importance of processes affecting earlylife-history stages in determining the productivity of a fish stockis corroborated by a literature review of a selected number of well-studied species in the Northeast Atlantic indicating the importanceof temperature effects on the level of recruitment (Table 1).Moreover, (multi-)decadal changes in ocean climate have beendriving changes in recruitment and productivity in the NorthAtlantic and Pacific Ocean (Lehodey et al., 2006).Climate-related changes in growth of recruited life-history stagesmay influence fish productivity (Dutil and Brander, 2003;Lehodey et al., 2006), although this effect may be confounded bya change in the intra- or interspecific competition for food.Global warming will reduce the probability of low winter tempera-tures, resulting in a better survival of both southern species andfish of small body size (Post and Evans, 1989). A critical test ofwhether this inference holds true remains to be done. Moststudies in the literature have focused on a specific part of the lifecycle and have not attempted to study all processes in an integrated

manner. Dutil and Brander (2003) distinguished between temp-erature effects on growth and recruitment, but were not able tomeasure recruitment independent of the growth rate before therecruitment to the fisheries.

Given the complexity of the problem, where climate change is amultifaceted driver and the response of affected fish populationtoo is multifaceted, we believe that scientific progress will benefitfrom an approach where a priori hypotheses are formulatedbased on first principles of the relevant levels of organization.The hypotheses proposed here are by no means complete. Theyshould rather be regarded as a first set of hypotheses. Thesehypotheses seek to compare species and species-groups that havecontrasting ecological characteristics and are thus likely to differin their sensitivity to climate change. The classification of speciesinto ecotypes based on biogeographic affinity, habitat require-ment, and life-history characteristics may be an important startingpoint. The review of a number of well-studied fish species in theNortheast Atlantic did not allow us to test all working hypotheses,but supported the hypothesis that species exhibited distributionalshifts (latitude and depth) in response to a temperature increaseand that the response of pelagic species is stronger than that ofdemersal species, corroborating a number of recent studies ofchanges in fish assemblages (Attrill and Power, 2002; Borja et al.,2002; Beare et al., 2004; Genner et al., 2004).

We argue that understanding the complex effects of climate ona species will require an integrated life-cycle approach that exam-ines the importance of different mechanisms acting on all lifestages and identifies those developmental stages and mechanismsmost critical for life-cycle closure and recruitment. Examples ofthis type of approach include the body of work performed onBaltic cod and sprat (Koster et al., 2003, 2005; Mollmann et al.,2008), which highlights the possible complex feedbacks amongelements of our framework (i.e. effects of physiology on behaviour,behaviour on top-down processes, and climate-driven physicalforcing on bottom-up processes).

AcknowledgementsThis study was carried out as part of the European Union FP6project RECLAIM (Contract 044133). The critical comments oftwo anonymous reviewers are gratefully acknowledged.

ReferencesACIA. 2004. Impacts of a Warming Arctic. Arctic Climate Impact

Assessment (ACIA). Cambridge University Press, Cambridge,UK. 139 pp.

Table 1. Continued

Change Comments Source

Recruitment negatively related totemperature in North Sea and positively in theBristol Channel

– Rijnsdorp et al. (1992) andHenderson and Seaby (2005)

Timing of spawning advanced in warm years(North Sea)

– Teal et al. (2008)

Length at end of first year increases withtemperature. Changes in growth of older fishdo not correlate with temperature

Growth of 0-group determined by temperature andlength of growing season. Growth of older agegroups related to population abundance,eutrophication, and bottom trawling

Millner and Whiting (1996) and Tealet al. (2008)

Ecotypes were defined as a combination of the following characteristics: habitat (pelagic or demersal; Atlantic or Shelf); biogeographic affinity (Atlantic,Lusitanian, or Boreal); and longevity (long, medium, or short).


Alheit, J., and Hagen, E. 1997. Long-term climate forcing of Europeanherring and sardine populations. Fisheries Oceanography, 6:130–139.

Anderson, C. N. K., Hsieh, C-H., Sandin, S. A., Hewitt, R., Hollowed,A., Beddington, J., May, R. M., et al. 2008. Why fishing magnifiesfluctuations in fish abundance. Nature, 452: 835–839.

Attrill, M. J., and Power, M. 2002. Climatic influence on a marine fishassemblage. Nature, 417: 275–278.

Baumann, H., Peck, M. A., Gotze, E., and Temming, A. 2007. Starvingearly juvenile sprat, Sprattus sprattus L., in Western Baltic coastalwaters: evidence from combined field and laboratory observationsin August/September 2003. Journal of Fish Biology, 70: 863–866.

Beare, D. J., Burns, F., Greig, A., Jones, E. G., Peach, K., Kienzle, M.,McKenzie, E., et al. 2004. Long-term increases in prevalence ofNorth Sea fishes having southern biogeographic affinities. MarineEcology Progress Series, 284: 269–278.

Beaugrand, G. 2004. The North Sea regime shift: evidence, causes,mechanisms and consequences. Progress in Oceanography, 60:245–262.

Beaugrand, G., Brander, K. M., Lindley, J. A., Souissi, S., and Reid,P. C. 2003. Plankton effect on cod recruitment in the North Sea.Nature, 426: 661–664.

Beaugrand, G., Reid, P. C., Ibanez, F., Lindley, J. A., and Edwards, M.2002. Reorganisation of North Atlantic marine copepod biodiver-sity and climate. Science, 296: 1692–1694.

Belk, M. C., and Houston, D. D. 2002. Bergmann’s rule in ectotherms:a test using freshwater fishes. American Naturalist, 160: 803–808.

Berghahn, R. 2000. Response to extreme conditions in coastal areas:biological tags in flatfish otoliths. Marine Ecology ProgressSeries, 192: 277–285.

Blanchard, F., and Vandermeirsch, F. 2005. Warming and exponentialabundance increase of the subtropical fish Capros aper in the Bay ofBiscay (1973–2002). Comptes Rendus Biologies, 328: 505–509.

Boddeke, R., and Vingerhoed, B. 1996. The anchovy returns to theWadden Sea. ICES Journal of Marine Science, 53: 1003–1007.

Borges, M. D. F., Silva, A., Abaunza, P., Eltink, A., Lucio, P., Walsh, M.,Poulard, J. C., et al. 1996. Changes in horse mackerel (Trachurustrachurus) catch distribution in the Northeast Atlantic. ICESDocument CM 1996/S: 26. 8 pp.

Borja, A., Uriarte, A., and Egana, J. 2002. Environmental factors andrecruitment of mackerel, Scomber scombrus L. 1758, along theNorth-east Atlantic coast of Europe. Fisheries Oceanography, 11:116–127.

Brander, K. 2000. Effects of environmental variability on growth andrecruitment in cod (Gadus morhua) using a comparative approach.Oceanologica Acta, 23: 485–496.

Brander, K. M. 1995. The effect of temperature on growth of Atlanticcod (Gadus morhua L.). ICES Journal of Marine Science, 52: 1–10.

Brown, B. R. 2003. Sensing temperature without ion channels. Nature,421: 495–495.

Carscadden, J., Nakashima, B. S., and Frank, K. T. 1997. Effects of fishlength and temperature on the timing of peak spawning in capelin(Mallotus villosus). Canadian Journal of Fisheries and AquaticSciences, 54: 781–787.

Casini, M., Hjelm, J., Molinero, J-C., Lovgren, J., Cardinale, M.,Bartolino, V., Belgrano, A., et al. 2008a. Trophic cascadespromote threshold-like shifts in pelagic marine ecosystems.Proceedings of the National Academy of Sciences of the UnitedStates of America, 106: 97–202.

Casini, M., Lovgren, J., Hjelm, J., Cardinale, M., Molinero, J. C., andKornilovs, G. 2008b. Multi-level trophic cascades in a heavilyexploited open marine ecosystem. Proceedings of the RoyalSociety of London, Series B—Biological Sciences, 275: 1793–1801.

Corten, A. 1986. On the causes of recruitment failure of herring in thecentral and northern North Sea in the years 1972–1978. Journal duConseil International pour l’Exploration de la Mer, 42: 281–294.

Corten, A. 2001a. Herring and climate. PhD thesis, RijksuniversiteitGroningen, The Netherlands. 228 pp.

Corten, A. 2001b. Northern distribution of North Sea herring as aresponse to high water temperatures and/or low food abundance.Fisheries Research, 50: 189–204.

Cushing, D. 1990. Plankton production and year-class strength in fishpopulations: an update of the match/mismatch hypothesis.Advances in Marine Biology, 26: 249–293.

Daan, N., Gislason, H., Pope, J. G., and Rice, J. C. 2005. Changes in theNorth Sea fish community: evidence of indirect effects of fishing?ICES Journal of Marine Science, 62: 177–188.

Daewel, U., Peck, M. A., Kuhn, W., St John, M. A., Alekseeva, I., andSchrum, C. 2008b. Coupling ecosystem and individual-basedmodels to simulate the influence of environmental variability onpotential growth and survival of larval sprat (Sprattus sprattus L.)in the North Sea. Fisheries Oceanography, 17: 333–351.

Daewel, U., Peck, M. A., Schrum, C., and St John, M. A. 2008a. Anapproach for including the effects of climate-driven forcing onprey fields in larval fish IBMs. Journal of Plankton Research, 30:1–5.

Darnaude, A. M., Salen-Picard, C., Polunin, N. V. C., andHarmelin-Vivien, M. L. 2004. Trophodynamic linkage betweenriver runoff and coastal fishery yield elucidated by stable isotopedata in the Gulf of Lions (NW Mediterranean). Oecologia, 138:325–332.

Daskalov, G. M., Grishin, A. N., Rodionov, S., and Mihneva, V. 2007.Trophic cascades triggered by overfishing reveal possible mechan-isms of ecosystem regime shifts. Proceedings of the NationalAcademy of Sciences of the United States of America, 104:10518–10523.

Desaunay, Y., Guerault, D., Le Pape, O., and Poulard, J. C. 2006.Changes in occurrence and abundance of northern/southern flat-fishes over a 20-year period in a coastal nursery area (Bay ofVilaine) and on the eastern continental shelf of the Bay of Biscay.Scientia Marina, 70: 193–200.

Diaz, R. J. 2001. Overview of hypoxia around the world. Journal ofEnvironmental Quality, 30: 275–281.

Dickson, R. R., Kelly, P. M., Colebrook, J. M., Wooster, W. S., andCushing, D. H. 1988. North winds and production in the easternNorth Atlantic. Journal of Plankton Research, 10: 151–169.

Dippner, J. W. 2006. Future aspects in marine ecosystem modelling.Journal of Marine Systems, 61: 246–267.

Dulvy, N. K., Rogers, S. I., Jennings, S., Stelzenmuller, V., Dye, S. R.,and Skjoldal, H. R. 2008. Climate change and deepening of theNorth Sea fish assemblage: a biotic indicator of warming seas.Journal of Applied Ecology, 45: 1029–1039.

Durant, J. M., Hjermann, Ø., Anker-Nilssen, T., Beaugrand, G.,Mysterud, A., Pettorelli, N., and Stenseth, N. C. 2005. Timingand abundance as key mechanisms affecting trophic interactionsin variable environments. Ecology Letters, 8: 952–958.

Dutil, J. D., and Brander, K. 2003. Comparing productivity of NorthAtlantic cod (Gadus morhua) stocks and limits to growth pro-duction. Fisheries Oceanography, 12: 502–512.

Edwards, M., and Richardson, A. J. 2004. Impact of climate change onmarine pelagic phenology and trophic mismatch. Nature, 430:881–884.

Eno, N. C., Clark, R. A., and Sanderson, W. G. 1997. Non-nativemarine species in British waters: a review and directory. JointNature Conservation Committee (JNCC). 136 pp.

Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C. 2008. Impacts ofocean acidification on marine fauna and ecosystem processes. ICESJournal of Marine Science, 65: 414–432.

Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J.,and Millero, F. J. 2004. Impact of anthropogenic CO2 on theCaCO3 system in the oceans. Science, 305: 362–366.

Fonds, M., Cronie, R., Vethaak, A. D., and van der Puyl, P. 1992.Metabolism, food-consumption and growth of plaice


(Pleuronectes platessa) and flounder (Platichthys flesus) in relationto fish size and temperature. Netherlands Journal of SeaResearch, 29: 127–143.

Fox, C. J., Planque, B. P., and Darby, C. D. 2000. Synchrony in therecruitment time-series of plaice (Pleuronectes platessa L) aroundthe United Kingdom and the influence of sea temperature.Journal of Sea Research, 44: 159–168.

Frank, K. T., Petrie, B., Choi, J. S., and Leggett, W. C. 2005. Trophiccascades in a formerly cod-dominated ecosystem. Science, 308:1621–1623.

Frank, K. T., Petrie, B., and Shackell, N. L. 2007. The ups and downs oftrophic control in continental shelf ecosystems. Trends in Ecologyand Evolution, 22: 236–242.

Franks, P. J. S. 2001. Turbulence avoidance: an alternate explanation ofturbulence-enhanced ingestion rates in the field. Limnology andOceanography, 46: 959–963.

Frei, C., Scholl, R., Fukutome, S., Jurg Schmidli, J., and Vidale, P. L.2006. Future change of precipitation extremes in Europe: inter-comparison of scenarios from regional climate models. Journalof Geophysical Research, 111, D06105. doi:10.1029/2005JD005965.

Freitas, V., Campos, J., Fonds, M., and van der Veer, H. W. 2007.Potential impact of temperature change on epibenthic predator–bivalve prey interactions in temperate estuaries. Journal ofThermal Biology, 32: 328–340.

Fry, F. E. J. 1971. The effect of environmental factors on animalactivity. In Fish Physiology, 6, pp. 1–98. Ed. by W. S. Hoar, andD. J. Randall. Academic Press, New York.

Genner, M. J., Sims, D. W., Wearmouth, V. J., Southall, E. J.,Southward, A. J., Henderson, P. A., and Hawkins, S. J. 2004.Regional climate warming drives long-term community changesof British marine fish. Proceedings of the Royal Society ofLondon, Series B, 271: 655–661.

Gibson, R. N. 1994. Does habitat quality and quantity affect therecruitment of juvenile flatfish? Netherlands Journal of SeaResearch, 32: 191–206.

Goren, M., and Galil, B. S. 2005. A review of changes in the fish assem-blages of Levantine inland and marine ecosystems following theintroduction of non-native fishes. Journal of AppliedIchthyology, 21: 364–370.

Greene, C. H., and Pershing, A. J. 2007. Climate drives sea change.Science, 315: 1084–1085.

Harley, C. D. G., Hughes, A. R., Hultgren, K. M., Miner, B. G., Sorte,C. J. B., Thornber, C. S., Rodriguez, L. F., et al. 2006. The impacts ofclimate change in coastal marine systems. Ecology Letters, 9:228–241.

Heath, M. R. 2005. Changes in the structure and function of the NorthSea fish foodweb 1973–2000, and the impacts of fishing andclimate. ICES Journal of Marine Science, 62: 847–868.

Heath, M. R. 2007. Responses of fish to climate fluctuations in theNortheast Atlantic. In The Practicalities of Climate Change:Adaptation and Mitigation. Proceedings of the 24th Conferenceof the Institute of Ecology and Environmental Management,Cardiff, 14–16 November 2006, pp. 102–116. Ed. by L. E.Emery. Institute of Ecology and Environmental Management,Winchester, Hampshire, UK.

Hedger, R., McKenzie, E., Heath, M., Wright, P., Scott, B., Gallego, A.,and Bridson, J. 2004. Analysis of the spatial distributions of maturecod (Gadus morhua) and haddock (Melanogrammus aeglefinus)abundance in the North Sea (1980–1999) using generalised addi-tive models. Fisheries Research, 70: 17–25.

Heil, C. A., Glibert, P. M., Al-Sarawi, M. W., Faraj, M., Behbehani, M.,and Husain, M. 2001. First record of a fish-killing Gymnodiniumsp. bloom in Kuwait Bay, Arabian Sea: chronology and potentialcauses. Marine Ecology Progress Series, 214: 15–23.

Heincke, F. 1913. Investigations on the plaice. I. The plaice fishery andprotective regulations. Rapports et Proces-Verbaux des Reunionsdu Conseil International pour l’Exploration de la Mer, 17: 1–153.

Heino, M., Dieckmann, U., and Godø, O. R. 2002. Measuring prob-abilistic reaction norms for age and size at maturation.Evolution, 56: 669–678.

Henderson, P. A., and Seaby, R. M. 2005. The role of climate in deter-mining the temporal variation in abundance, recruitment andgrowth of sole Solea solea in the Bristol Channel. Journal of theMarine Biological Association of the UK, 85: 197–204.

Heupel, M. R., Simpfendorfer, C. A., and Hueter, R. E. 2003. Runningbefore the storm: blacktip sharks respond to falling barometricpressure associated with Tropical Storm Gabrielle. Journal ofFish Biology, 63: 1357–1363.

Holst, J. C., Dragesund, O., Hamre, J., Misund, O. A., and Østvedt,O. J. 2002. Fifty years of herring migrations in the NorwegianSea. ICES Marine Science Symposia, 215: 352–360.

Houde, E. D. 1987. Fish early life dynamics and recruitment variabil-ity. American Fisheries Society Symposium, 2: 17–29.

Hulme, M., Jenkins, G. L., Lu, X., Turnpenny, J. R., Mitchell, T. D.,Jones, R. G., Lowe, J., et al. 2002. Climate Change Scenarios forthe United Kingdom: the UKCIP02 Scientific Report, Tyndall.Centre for Climate Change Research, School of EnvironmentalSciences, University of East Anglia, Norwich, UK. 120 pp.

Hunt, G. L., and McKinnell, S. 2006. Interplay between top-down,bottom-up, and wasp-waist control in marine ecosystems.Progress in Oceanography, 68: 115–124.

Hunt, G. L., Stabeno, P., Walters, G., Sinclair, E., Brodeur, R. D., Napp,J. M., and Bond, N. A. 2002. Climate change and control of thesoutheastern Bering Sea pelagic ecosystem. Deep Sea Research II,49: 5821–5853.

Huse, G., and Ellingsen, I. 2008. Capelin migrations and climatechange—a modelling analysis. Climate Change, 87: 177–197.

Hutchings, J. A., and Myers, R. A. 1994. Timing of cod reproduction—interannual variability and the influence of temperature. MarineEcology Progress Series, 108: 21–31.

ICES. 2007. Report of the Working Group on the Assessment ofMackerel, Horse Mackerel, Sardine and Anchovy (WGMHSA).ICES Document CM 2007/ACFM: 31.

Imsland, A. K., Sunde, L. M., Folkvord, A., and Stefansson, S. O. 1996.The interaction of temperature and fish size on growth of juvenileturbot. Journal of Fish Biology, 49: 926–940.

IPCC. 2007. Climate Change 2007: the Physical Science Basis.Contribution of Working Group I to the Fourth AssessmentReport of the Intergovernmental Panel on Climate Change.Cambridge University Press, Cambridge, UK.

Irvin, D. N. 1974. Temperature tolerance of early development stagesof Dover sole, Solea solea (L.). In Proceedings of an InternationalSymposium on the Early Life History of Fish, DunstaffnageMarine Research Laboratory, Oban, Scotland, 17–23 May 1973,pp. 449–463. Ed. by J. H. S Blaxter. Springer Verlag, New York.

Ishimatsu, A., Hayashi, M., Lee, K. S., Kikkawa, T., and Kita, J. 2005.Physiological effects on fishes in a high-CO2 world. Journal ofGeophysical Research: Oceans, 110: C09S09. doi:10.1029/2004JC002564.

Iversen, S. A. D., Skogen, M., and Svendsen, E. 2002. Availability ofhorse mackerel (Trachurus trachurus) in the north-eastern NorthSea, predicted by the transport of Atlantic water. FisheriesOceanography, 11: 245–250.

Jahncke, J., Checkley, D. M., and Hunt, G. L. 2004. Trends in carbonflux to seabirds in the Peruvian upwelling system: effects of windand fisheries on population regulation. Fisheries Oceanography,13: 208–223.

Jennings, S., and Blanchard, J. L. 2004. Fish abundance with no fishing:predictions based on macroecological theory. Journal of AnimalEcology, 73: 632–642.


Jennings, S., Melin, F., Blanchard, J. L., Forster, R. M., Dulvy, N. K.,and Wilson, E. W. 2008. Global-scale predictions of communityand ecosystem properties from simple ecological theory.Proceedings of the Royal Society of London, Series B, 275:1375–1383.

Karlson, A. M. L., Almqvist, G., Skora, K. E., and Appelberg, M. 2007.Indications of competition between non-indigenous round gobyand native flounder in the Baltic Sea. ICES Journal of MarineScience, 64: 479–486.

Koster, F. W., Mollmann, C., Hinrichsen, H-H., Wieland, K.,Tomkiewicz, J., Kraus, G., Voss, R., et al. 2005. Baltic cod recruit-ment—the impact of climate variability on key processes. ICESJournal of Marine Science, 62: 1408–1425.

Koster, F. W., Mollmann, C., Neuenfeldt, S., Vinther, M., St John,M. A., Tomkiewicz, J., Voss, R., et al. 2003. Fish stock developmentin the central Baltic Sea (1976–2000) in relation to variability inthe environment. ICES Marine Science Symposia, 219: 294–306.

Le Pape, O., Chauvet, F., Desaunay, Y., and Guerault, D. 2003.Relationship between interannual variations of the river plumeand the extent of nursery grounds for the common sole (Soleasolea, L.) in Vilaine Bay: effects on recruitment variability.Journal of Sea Research, 50: 177–185.

Lehodey, P., Alheit, J., Barange, M., Baumgartner, T., Beaugrand, G.,Drinkwater, K., Fromentin, J. M., et al. 2006. Climate variability,fish, and fisheries. Journal of Climate, 19: 5009–5030.

Leis, J. M. 2006. Are larvae of demersal fishes plankton or nekton?Advances in Marine Biology, 51: 57–141.

Link, J. S. 2002. Does food web theory work for marine ecosystems?Marine Ecology Progress Series, 230: 1–9.

Litzow, M. A., and Ciannelli, L. 2007. Oscillating trophic controlinduces community reorganisation in a marine ecosystem.Ecology Letters, 10: 1124–1134.

MacKenzie, B. R., Gislason, H., Mollmann, C., and Koster, F. W. 2007.Impact of 21st century climate change on the Baltic Sea fish com-munity and fisheries. Global Change Biology, 13: 1–20.

MacKenzie, B. R., Hinrichsen, H. H., Plikshs, M., Wieland, K., andZezera, A. S. 2000. Quantifying environmental heterogeneity:habitat size necessary for successful development of cod Gadusmorhua eggs in the Baltic Sea. Marine Ecology Progress Series,193: 143–156.

MacKenzie, B. R., and Koster, F. W. 2004. Fish production and climate:sprat in the Baltic Sea. Ecology, 85: 784–794.

Mavruk, S., and Avsar, D. 2007. Non-native fishes in theMediterranean from the Red Sea, by way of the Suez Canal.Reviews in Fish Biology and Fisheries, 18: 251–262.

Miller, J. M., Burke, J. S., and Fitzhugh, G. R. 1991. Early life historypatterns of Atlantic North American flatfish: likely (and unlikely)factors controlling recruitment. Netherlands Journal of SeaResearch, 27: 261–275.

Millner, R. S., and Whiting, C. L. 1996. Long-term changes in growthand population abundance of sole in the North Sea from 1940 tothe present. ICES Journal of Marine Science, 53: 1185–1195.

Mollmann, C., Diekmann, R., Muller-Karulis, B., Kornilovs, G.,Plikshs, M., and Axe, P. 2009. Reorganization of a large marineecosystem due to atmospheric and anthropogenic pressure: adiscontinuous regime shift in the Central Baltic Sea. GlobalChange Biology, 15: 1377–1393.

Mollmann, C., Muller-Karulis, B., Kornilovs, G., and St John, M. A.2008. Effects of climate and overfishing on zooplankton dynamicsand ecosystem structure: regime shifts, trophic cascade and feed-back loops in a simple ecosystem. ICES Journal of MarineScience, 65: 302–310.

Neat, F., and Righton, D. 2007. Warm water occupancy by North Seacod. Proceedings of the Royal Society of London, Series B, 274:789–798.

O’Brien, C. M., Fox, C. J., Planque, B., and Casey, J. 2000. Climatevariability and North Sea cod. Nature, 404: 142.

Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A.,Gnanadesikan, A., et al. 2005. Anthropogenic ocean acidificationover the twenty-first century and its impact on calcifying organ-isms. Nature, 437: 681–686.

Ottersen, G., Hjermann, D. Ø., and Stenseth, N. C. 2006. Changes inspawning stock structure strengthen the link between climate andrecruitment in a heavily fished cod (Gadus morhua) stock.Fisheries Oceanography, 15: 230–243.

Ottersen, G., and Stenseth, N. C. 2001. Atlantic climate governsoceanographic and ecological variability in the Barents Sea.Limnology and Oceanography, 46: 1774–1780.

Pearson, R. G., and Dawson, T. P. 2003. Predicting the impacts ofclimate change on the distribution of species: are bioclimate envel-ope models useful? Global Ecology and Biogeography, 12:361–371.

Peck, M. A., Buckley, L. J., and Bengtson, D. A. 2006. Effects of temp-erature and body size on the swimming velocity of larval and juven-ile Atlantic cod (Gadus morhua): implications for individual-basedmodeling. Environmental Biology of Fishes, 75: 419–429.

Peck, M. A., Buckley, L. J., Caldarone, E. M., and Bengtson, D. A. 2003.Effects of food consumption and temperature on growth rate andbiochemical-based indicators of growth in early juvenile Atlanticcod (Gadus morhua) and haddock (Melanogrammus aeglefinus).Marine Ecology Progress Series, 251: 233–243.

Perry, A. L., Low, P. J., Ellis, J. R., and Reynolds, J. D. 2005. Climatechange and distribution shifts in marine fishes. Science, 308:1912–1915.

Planque, B., and Fredou, T. 1999. Temperature and the recruitment ofAtlantic cod (Gadus morhua). Canadian Journal of Fisheries andAquatic Sciences, 56: 2069–2077.

Platt, T., Fuentes-Yaco, C., and Frank, K. T. 2003. Spring algal bloomand larval fish survival. Nature, 423: 398–399.

Portner, H. O., and Farrell, A. P. 2008. Physiology and climate change.Science, 322: 690–692.

Portner, H. O., and Knust, R. 2007. Climate change affects marinefishes through the oxygen limitation of thermal tolerance.Science, 315: 95–97.

Post, J. R., and Evans, D. O. 1989. Size-dependent overwinter mortalityof young-of-the-year yellow perch (Perca flavescens)—laboratory,in situ enclosure, and field experiments. Canadian Journal ofFisheries and Aquatic Sciences, 46: 1958–1968.

Reid, D. G., Walsh, M., and Turrell, W. R. 2001. Hydrography andmackerel distribution on the shelf edge west of the Norwegiandeeps. Fisheries Research, 50: 141–150.

Rice, J., and Gislason, H. 1996. Patterns of change in the size spectra ofnumbers and diversity of the North Sea fish assemblage, as reflectedin surveys and models. ICES Journal of Marine Science, 53:1214–1225.

Richardson, A. J., and Schoeman, D. S. 2004. Climate impact onplankton ecosystems in the Northeast Atlantic. Science, 305:1609–1612.

Rijnsdorp, A. D., van Beek, F. A., Flatman, S., Miller, J. M., Riley, J. D.,Giret, M., and de Clerk, R. 1992. Recruitment of sole, Solea solea(L.), in the Northeast Atlantic. Netherlands Journal of SeaResearch, 29: 173–192.

Rijnsdorp, A. D., and van Leeuwen, P. I. 1996. Changes in growth ofNorth Sea plaice since 1950 in relation to density, eutrophication,beam-trawl effort, and temperature. ICES Journal of MarineScience, 53: 1199–1213.

Rindorf, A., and Lewey, P. 2006. Warm, windy winters drive cod northand homing of spawners keeps them there. Journal of AppliedEcology, 43: 445–453.

Rothschild, B. J. 1986. Dynamics of Marine Fish Populations. HarvardUniversity Press, Cambridge, MA, USA.

Rykaczewski, R. R., and Checkley, D. M. 2008. Influence of oceanwinds on the pelagic ecosystem in upwelling regions. Proceedings


of the National Academy of Sciences of the United States ofAmerica, 105: 1965–1970.

Salen-Picard, C., Darnaude, A. M., Arlhac, D., and Harmelin-Vivien,M. L. 2002. Fluctuations of macrobenthic populations: a linkbetween climate-driven river run-off and sole fishery yields inthe Gulf of Lions. Oecologia, 133: 380–388.

Scheffer, M., and Carpenter, S. 2003. Catastrophic regime shifts in eco-systems: liking theory to observation. Trends in Ecology andEvolution, 18: 648–656.

Sims, D. W., Wearmouth, V. J., Genner, M. J., Southward, A. J., andHawkins, S. J. 2004. Low-temperature-driven early spawningmigration of a temperate marine fish. Journal of Animal Ecology,73: 333–341.

Sinclair, M. 1988. Marine Populations: an Essay on PopulationRegulation and Speciation. University of Washington Press, Seattle.

Sogard, S. M. 1997. Size-selective mortality in the juvenile stage ofteleost fishes: a review. Bulletin of Marine Science, 60: 1129–1157.

Sparholt, H. 1996. Causal correlation between recruitment and spawn-ing stock size of central Baltic cod? ICES Journal of Marine Science,53: 771–779.

Stenseth, N. C., Mysterud, A., Ottersen, G., Hurrell, J. W., Chan, K-S.,and Lima, M. 2002. Ecological effects of climate fluctuations.Science, 297: 1292–1296.

Strong, D. R. 1992. Are trophic cascades all wet? Differentiation anddonor-control in speciose ecosystems. Ecology, 73: 747–754.

Tasker, M. (Ed.) 2008. The effects of climate change on the distri-bution and abundance of marine species in the OSPAR maritimearea. ICES Cooperative Research Report, 293. 45 pp.

Teal, L. R., de Leeuw, J. J., van der Veer, H. W., and Rijnsdorp, A. D.2008. Effects of climate change on growth of 0-group sole andplaice. Marine Ecology Progress Series, 358: 219–230.

Temming, A., Floeter, J., and Ehrich, S. 2007. Predation hot spots:large scale impact of local aggregations. Ecosystems, 10: 865–876.

Toresen, R., and Østvedt, O. J. 2000. Variation in abundance ofNorwegian spring-spawning herring (Clupea harengus,Clupeidae) throughout the 20th century and the influence of cli-matic fluctuations. Fish and Fisheries, 1: 231–256.

Tsuchida, S. 1995. The relationship between upper temperature toler-ance and final preferendum of Japanese marine fish. Journal ofThermal Biology, 20: 35–41.

Van Keeken, O. A., Van Hoppe, M., Grift, R. E., and Rijnsdorp, A. D.2007. The implications of changes in the spatial distribution of

juveniles for the management of North Sea plaice (Pleuronectes pla-tessa). Journal of Sea Research, 57: 187–197.

Van der Veer, H. W., Berghahn, R., Miller, J. M., and Rijnsdorp, A. D.2000. Recruitment in flatfish, with special emphasis on NorthAtlantic species: progress made by the Flatfish Symposia. ICESJournal of Marine Science, 57: 202–215.

Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee,T. J. C., Fromentin, J. M., et al. 2002. Ecological responses to recentclimate change. Nature, 416: 389–395.

Ware, D. M., and Thomson, R. E. T. 2005. Bottom-up ecosystemtrophic dynamics determine fish production in the NortheastPacific. Science, 308: 1280–1284.

Weijerman, M., Lindeboom, H. J., and Zuur, A. F. 2005. Regime shiftsin marine ecosystems of the North Sea and Wadden Sea. MarineEcology Progress Series, 298: 21–39.

Wilderbuer, T. K., Hollowed, A. B., Ingraham, W. J., Spencer, P. D.,Conners, M. E., Bond, N. A., and Walters, G. E. 2002. Flatfishrecruitment response to decadal climatic variability and ocean con-ditions in the eastern Bering Sea. Progress in Oceanography, 55:235–247.

Winger, P. D. 2005. Effect of environmental conditions on the naturalactivity rhythms and bottom trawl catchability of Atlantic cod(Gadus morhua). Dissertation Abstracts International Part B.Science and Engineering, 66: 153.

Woodhead, P. M. J. 1964. The death of North Sea fish during thewinter of 1962/63, particularly with reference to the sole, Solea vul-garis. Helgolander Wissenschaftlichen Meeresuntersuchungen, 10:283–299.

Worm, B., and Myers, R. A. 2003. Meta-analysis of cod-shrimp inter-actions reveals top-down control in oceanic food webs. Ecology, 84:162–173.

Yamashita, Y., Tanaka, M., and Miller, J. M. 2001. Ecophysiology ofjuvenile flatfish in nursery grounds. Journal of Sea Research, 45:205–218.

Yang, J. 1982. The dominant fish fauna in the North Sea and its deter-mination. Journal of Fish Biology, 20: 635–643.

Yin, K. D., Harrison, P. J., Chen, J., Huang, W., and Qian, P. Y. 1999.Red tides during spring 1998 in Hong Kong: is El Nino responsible?Marine Ecology Progress Series, 187: 289–294.

doi:10.1093/icesjms/fsp056


Resolving the effect of climate change on fish populations

Documents

Transcript of Resolving the effect of climate change on fish populations