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The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change

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Abstract

Thermal preference and performance provide the physiological frame within which fish species seek strategies to cope with the challenges raised by the low temperatures and low levels of oxygen and food that characterize winter. There are two common coping strategies: active utilization of winter conditions or simple toleration of winter conditions. The former is typical of winter specialist species with low preferred temperatures, and the latter is typical of species with higher preferred temperatures. Reproductive strategies are embodied in the phenology of spawning: the approach of winter conditions cues reproductive activity in many coldwater fish species, while the departure of winter conditions cues reproduction in many cool and warmwater fish species. This cuing system promotes temporal partitioning of the food resources available to young-of-year fish and thus supports high diversity in freshwater fish communities. If the zoogeographic distribution of a species covers a broad range of winter conditions, local populations may exhibit differences in their winter survival strategies that reflect adaptation to local conditions. Extreme winter specialists are found in shallow eutrophic lakes where long periods of ice cover cause winter oxygen levels to drop to levels that are lethal to many fish. The fish communities of these lakes are simple and composed of species that exhibit specialized adaptations for extended tolerance of very low temperatures and oxygen levels. Zoogeographic boundaries for some species may be positioned at points on the landscape where the severity of winter overwhelms the species’ repertoire of winter survival strategies. Freshwater fish communities are vulnerable to many of the shifts in environmental conditions expected with climate change. Temperate and northern communities are particularly vulnerable since the repertoires of physiological and behavioural strategies that characterize many of their members have been shaped by the adverse environmental conditions (e.g. cool short summers, long cold winters) that climate change is expected to mitigate. The responses of these strategies to the rapid relaxation of the adversities that shaped them will play a significant role in the overall responses of these fish populations and their communities to climate change.

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References

  • Adams SM, Mclean RB, Parrotta JA (1982) Energy partitioning in largemouth bass under conditions of seasonally fluctuating prey availability. T Am Fish Soc 111:549–558

    Google Scholar 

  • Amano T, Smithers RJ, Sparks TH, Sutherland WJ (2010) A 250-year index of first flowering dates and its response to temperature changes. Proc R Soc B 277:2451–2457

    PubMed  Google Scholar 

  • Amundsen P, Knudsen R (2009) Winter ecology of Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in a subarctic lake, Norway. Aquat Ecol 43:765–775

    CAS  Google Scholar 

  • Balayla D, Lauridsen TL, Sondergaard M, Jeppesen E (2010) Larger zooplankton in Danish lakes after cold winters: are winter fish kills of importance? Hydrobiologia 646:159–172

    CAS  Google Scholar 

  • Baroudy E, Elliot JM (1994) Racial differences in eggs and juveniles of Windermere charr, Salvelinus alpinus. J Fish Biol 45:407–415

    Google Scholar 

  • Barthel BL, Cooke SJ, Svec JH et al (2008) Divergent life histories among smallmouth bass Micropterus dolomieu inhabiting a connected river-lake system. J Fish Biol 73:829–852

    Google Scholar 

  • Batima P, Batnasan N, Bolormaa B (2004) Trends in river and lake ice in Mongolia, AIACC Working Paper No. 4. In: Assessments of Impacts and Adaptations to Climate Change Project. http://www.aiaccproject.org/working_papers.html

  • Beamish F (1964) Influence of starvation on standard and routine oxygen consumption. Trans Am Fish Soc 93:103–107

    Google Scholar 

  • Benson BJ, Magnuson JJ, Jensen OP, Card VM, Hodgkins G, Korhonen J, Livingstone DM, Stewart KM, Weyhenmeyer GA, Granin NG (2012) Extreme events, trends, and variability in Northern Hemisphere lake-ice phenology (1855–2005). Clim Chang 112:299–323

    Google Scholar 

  • Berg O, Finstad A, Solem O et al (2009) Pre-winter lipid stores in young-of-year Atlantic salmon along a north-south gradient. J Fish Biol 74:1383–1393

    PubMed  CAS  Google Scholar 

  • Berg O, Finstad A, Olsen P et al (2010) Dwarfs and cannibals in the Arctic: production of Arctic char (Salvelinus alpinus (L.)) at two trophic levels. Hydrobiologia 652:337–347

    Google Scholar 

  • Berg OK, Rod G, Solem O, Finstad AG (2011) Pre-winter lipid stores in brown trout Salmo trutta along altitudinal and latitudinal gradients. J Fish Biol 79:1156–1166

    PubMed  CAS  Google Scholar 

  • Binner M, Kloas W, Hardewig I (2008) Energy allocation in juvenile roach and burbot under different temperature and feeding regimes. Fish Physiol Biochem 34:103–116

    PubMed  CAS  Google Scholar 

  • Biro P, Abrahams M, Post J, Parkinson E (2004a) Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proc R Soc B 271:2233–2237

    PubMed  Google Scholar 

  • Biro P, Morton A, Post J, Parkinson E (2004b) Over-winter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1513–1519

    CAS  Google Scholar 

  • Blanchfield P, Tate L, Plumb J et al (2009) Seasonal habitat selection by lake trout (Salvelinus namaycush) in a small Canadian shield lake: constraints imposed by winter conditions. Aquat Ecol 43:777–787

    Google Scholar 

  • Bly JE, Lawson LA, Szalai AJ, Clem LW (1993) Environmental factors affecting outbreaks of winter saprolegniosis in channel catfish, Ictalurus punctatus (Rafinesque). J Fish Dis 16:541–549

    Google Scholar 

  • Borcherding J, Beeck P, DeAngelis DL, Scharf WR (2010) Match or mismatch: the influence of phenology on size-dependent life history and divergence in population structure. J Anim Ecol 79:1101–1112

    PubMed  Google Scholar 

  • Bradshaw W, Holzapfel C (2006) Climate change—evolutionary response to rapid climate change. Science 312:1477–1478

    PubMed  CAS  Google Scholar 

  • Bradshaw W, Holzapfel C (2007) Evolution of animal photoperiodism. Ann Rev Ecol Evol Syst 38:1–25

    Google Scholar 

  • Bradshaw W, Holzapfel C (2010) Light, time, and the physiology of biotic response to rapid climate change in animals. Ann Rev Physiol 72:147–166

    CAS  Google Scholar 

  • Brönmark C, Skov C, Brodersen J et al (2008) Seasonal migration determined by a trade-off between predator avoidance and growth. PLoS ONE 3:e1957

    PubMed  Google Scholar 

  • Buisson L, Grenouillet G (2009) Contrasted impacts of climate change on stream fish assemblages along an environmental gradient. Divers Distrib 15:613–626

    Google Scholar 

  • Bull CD, Metcalfe NB, Mangel M (1996) Seasonal matching of foraging to anticipated energy requirements in anorexic juvenile salmon. Proc R Soc B 263:13–18

    Google Scholar 

  • Byström P, Andersson J, Kiessling A, Eriksson LO (2006) Size and temperature dependent foraging capacities and metabolism: consequences for winter starvation mortality in fish. Oikos 115:43–52

    Google Scholar 

  • Casselman J (2002) Effects of temperature, global extremes and climate warming on year-class production of warmwater, coolwater and coldwater fishes. In: McGinn NA (ed) Fisheries in a changing climate. American Fisheries Society, Bethesda, pp 39–60

  • Chiba S, Arnott S, Conover D (2007) Coevolution of foraging behavior with intrinsic growth rate: risk-taking in naturally and artificially selected growth genotypes of Menidia menidia. Oecologia 154:237–246

    PubMed  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon WT, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York

  • Christie G, Regier H (1988) Measures of optimal thermal habitat and their relationship to yields for four commercial fish species. Can J Fish Aquat Sci 45:301–314

    Google Scholar 

  • Clarke A, Pörtner HO (2010) Temperature, metabolic power and the evolution of endothermy. Biol Rev 85:703–727

    PubMed  Google Scholar 

  • Clilverd H, White D, Lilly M (2009) Chemical and physical controls on the oxygen regime of ice covered arctic lakes and reservoirs. J Am Water Resour Assoc 45:500–511

    CAS  Google Scholar 

  • Condon C, Chenoweth S, Wilson R (2010) Zebrafish take their cue from temperature but not photoperiod for the seasonal plasticity of thermal performance. J Exp Biol 213:3705–3709

    PubMed  Google Scholar 

  • Conover DO, Present TMC (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83:316–324

    Google Scholar 

  • Conover D, Arnott S, Walsh M, Munch S (2005) Darwinian fishery science: lessons from the Atlantic silverside (Menidia menidia). Can J Fish Aquat Sci 62:730–737

    Google Scholar 

  • Cooke S, Grant E, Schreer J et al (2003) Low temperature cardiac response to exhaustive exercise in fish with different levels of winter quiescence. Comp Biochem Phys A 134:159–167

    Google Scholar 

  • Coutant CC (1990) Temperature-oxygen habitat for freshwater and coastal striped bass in a changing climate. T Am Fish Soc 119:240–253

    Google Scholar 

  • Cunjak R (1996) Winter habitat of selected stream fishes and potential impacts from land-use activity. Can J Fish Aquat Sci 53:267–282

    Google Scholar 

  • Cunjak R, Power G (1986) Winter habitat utilization by stream resident Brook Trout (Salvelinus fontinalis) and Brown Trout (Salmo trutta). Can J Fish Aquat Sci 43:1970–1981

    Google Scholar 

  • Danylchuk A, Tonn W (2003) Natural disturbances and fish: local and regional influences on winterkill of fathead minnows in boreal lakes. T Am Fish Soc 132:289–298

    Google Scholar 

  • Danylchuk A, Tonn W (2006) Natural disturbance and life history: consequences of winterkill on fathead minnow in boreal lakes. J Fish Biol 68:681–694

    Google Scholar 

  • Daufresne M, Boet P (2007) Climate change impacts on structure and diversity of fish communities in rivers. Glob Change Biol 13:2467–2478

    Google Scholar 

  • Dawson A, Grimm A (1980) Quantitative seasonal changes in the protein, lipid and energy content of the carcass, ovaries and liver of adult female plaice, Pleuronectes platessa L. J Fish Biol 16:493–504

    CAS  Google Scholar 

  • DeWitt TJSA, Wilson R (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    PubMed  CAS  Google Scholar 

  • Doll P, Zhang J (2010) Impact of climate change on freshwater ecosystems: a global-scale analysis of ecologically relevant river flow alterations. Hydrol Earth Syst Sci 14:783–799

    Google Scholar 

  • Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817

    PubMed  Google Scholar 

  • Dunlop E, Shuter B (2006) Native and introduced populations of smallmouth bass differ in concordance between climate and somatic growth. T Am Fish Soc 135:1175–1190

    Google Scholar 

  • Eaton B, Tonn W, Paszkowski C et al (2005) Indirect effects of fish winterkills on amphibian populations in boreal lakes. Can J Zool 83:1532–1539

    Google Scholar 

  • Elliott JM (1976) The energetics of feeding, metabolism and growth of brown trout (Salmo trutta L.) in relation to body weight, water temperature and ration size. J Anim Ecol 45:923–948

    Google Scholar 

  • Elliott JM, Elliott JA (2010) Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change. J Fish Biol 77:1793–1817

    PubMed  CAS  Google Scholar 

  • Encina L, Granado-Lorencio C (1997) Seasonal variations in the physiological status and energy content of somatic reproductive tissues of chub. J Fish Biol 50:511–522

    Google Scholar 

  • Evans DO (1984) Temperature independence of the annual cycle of standard metabolism in the pumpkinseed. T Am Fish Soc 113:494–512

    Google Scholar 

  • Evans D (2007) Effects of hypoxia on scope-for-activity and power capacity of lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 64:345–361

    CAS  Google Scholar 

  • Fang X, Stefan H (2000) Projected climate change effects on winterkill in shallow lakes in the northern United States. Environ Manag 25:291–304

    Google Scholar 

  • Finstad A, Berg O, Lohrmann A (2003) Seasonal variation in body composition of Arctic char, Salvelinus alpinus, from an ultraoligotrophic alpine lake. Ecol Freshw Fish 12:228–235

    Google Scholar 

  • Finstad A, Ugedal O, Forseth T, Naesje T (2004a) Energy-related juvenile winter mortality in a northern population of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 61:2358–2368

    Google Scholar 

  • Finstad A, Naesje T, Forseth T (2004b) Seasonal variation in the thermal performance of juvenile Atlantic salmon (Salmo salar). Freshwater Biol 49:1459–1467

    Google Scholar 

  • Finstad A, Forseth T, Faenstad T, Ugedal O (2004c) The importance of ice cover for energy turnover in juvenile Atlantic salmon. J Anim Ecol 73:959–966

    Google Scholar 

  • Finstad A, Berg O, Forseth T et al (2010) Adaptive winter survival strategies: defended energy levels in juvenile Atlantic salmon along a latitudinal gradient. P Roy Soc Lond B Bio 277:1113–1120

    Google Scholar 

  • Finstad A, Forseth T, Jonsson B et al (2011) Competitive exclusion along climate gradients: energy efficiency influences the distribution of two salmonid fishes. Glob Change Biol 17:1703–1711

    Google Scholar 

  • Frost WE (1965) Breeding habits of Windermere Charr, Salvelinus Willughbii (Gunther), and their bearing on speciation of these fish. Proc R Soc B 163:232–284

    CAS  Google Scholar 

  • Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, New York, pp 1-98

  • Geiger W (1962) Fischsterben in der Schweiz im Laute der letzten 10 Jahre. Schweizer Fischerei 70:170–173

    Google Scholar 

  • Gerdeaux D (2011) Does global warming threaten the dynamics of Arctic charr in Lake Geneva? Hydrobiologia 660:69–78

    Google Scholar 

  • Gillet C, QueTin P (2006) Effect of temperature changes on the reproductive cycle of roach in Lake Geneva from 1983 to 2001. J Fish Biol 69:518–534

    Google Scholar 

  • Greenbank J (1945) Limnological conditions in ice-covered lakes, especially as related to winter-kill of fish. Ecol Monogr 15:343–392

    Google Scholar 

  • Gunn J (2002) Impact of the 1998 El Nino event on a lake charr, Salvelinus namaycush, population recovering from acidification. Environ Biol Fish 64:343–351

    Google Scholar 

  • Gunn J, Steedman R, Ryder RA (2004) Boreal shield watersheds ecosystem management in a changing environment. CRC Press, Boca Raton

  • Hanson PC, Johnson TB, Schindler DE, Kitchell JF (1997) Fish Bioenergetics 3.0. University of Wisconsin Sea Grant Institute, Madison

  • Hanson K, Hasler C, Cooke S et al (2008) Intersexual variation in the seasonal behaviour and depth distribution of a freshwater temperate fish, the largemouth bass. Can J Zool 86:801–811

    Google Scholar 

  • Hardewig I, Pörtner HO, van Dijk P (2004) How does the cold stenothermal gadoid Lota lota survive high water temperatures during summer? J Comp Physiol B 174:149–156

    PubMed  CAS  Google Scholar 

  • Hasler C, Suski C, Hanson K et al (2009a) Effect of water temperature on laboratory swimming performance and natural activity levels of adult largemouth bass. Can J Zool 87:589–596

    Google Scholar 

  • Hasler C, Suski C, Hanson K et al (2009b) The influence of dissolved oxygen on winter habitat selection by largemouth bass: an integration of field biotelemetry studies and laboratory experiments. Physiol Biochem Zoo 82:143–152

    CAS  Google Scholar 

  • Hasnain SS, Minns CK, Shuter BJ (2010) Key ecological temperature metrics for Canadian freshwater fishes. Ontario Ministry of Natural Resources, Climate Change Research Report 17, Peterborough

  • Hayman R, Bly JE, Paul Levine R, Lobb CJ (1992) Complement deficiencies in channel catfish (Ictalurus punctatus) associated with temperature and seasonal mortality. Fish Shellfish Immun 2:183–192

    Google Scholar 

  • Heermann L, Borderding J (2006) Winter short-distance migration of juvenile fish between two floodplain water bodies of the Lower River Rhine. Ecol Freshw Fish 15:161–168

    Google Scholar 

  • Heermann L, Eriksson L, Magnhagen C, Borcherding J (2009) Size-dependent energy storage and winter mortality of perch. Ecol Freshw Fish 18:560–571

    Google Scholar 

  • Heibo E, Magnhagen C, Vollestad LA (2005) Latitudinal variation in life-history traits in Eurasian perch. Ecology 86:3377–3386

    Google Scholar 

  • Helland IP, Freyhof J, Kasprzak P, Mehner T (2007) Temperature sensitivity of vertical distributions of zooplankton and planktivorous fish in a stratified lake. Oecologia 151:322–330

    PubMed  Google Scholar 

  • Helland IP, Finstad AG, Forseth T et al (2011) Ice-cover effects on competitive interactions between two fish species. J Anim Ecol 80:539–547

    PubMed  Google Scholar 

  • Henderson B, Wong J, Nepszy S (1996) Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci 53:127–133

    Google Scholar 

  • Henderson B, Trivedi T, Collins N (2000) Annual cycle of energy allocation to growth and reproduction of yellow perch. J Fish Biol 57:122–133

    Google Scholar 

  • Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    PubMed  CAS  Google Scholar 

  • Hofmann N, Fischer P (2002) Temperature preferences and critical thermal limits of burbot: implications for habitat selection and ontogenetic habitat shift. T Am Fish Soc 131:1164–1172

    Google Scholar 

  • Hokanson K (1977) Temperature requirements of some percids and adaptations to the seasonal temperature cycle. J Fish Res Bd Canada 34:1524–1550

    Google Scholar 

  • Hölker F (2006) Effects of body size and temperature on metabolism of bream compared to sympatric roach. Anim Biol 56:23–37

    Google Scholar 

  • Hölker F, Breckling B (2005) A spatiotemporal individual-based fish model to investigate emergent properties at the organismal and the population level. Ecol Model 186:406–426

    Google Scholar 

  • Hölker F, Thiel R (1998) Biology of ruffe (Gymnocephalus cernuus (L.)–a review of selected aspects from European literature. J Great Lakes Res 24:186–204

    Google Scholar 

  • Hölker F, Volkmann S, Wolter C et al (2004) Colonization of the freshwater environment by a marine invader: how to cope with warm summer temperatures? Evol Ecol Res 6:1123–1144

    Google Scholar 

  • Holling C (1959) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Can Entomol 91:293–320

    Google Scholar 

  • Holopainen IJ, Hyvärinen H, Piironen J (1986) Anaerobic wintering of crucian carp (Carassius carassius L.)—II. Metabolic products. Comp Biochem Physiol A 83:239–242

    PubMed  CAS  Google Scholar 

  • Huckstorf V, Lewin W, Mehner T (2009) Performance level and efficiency of two differing predator-avoidance strategies depending on nutritional state of the prey. Behav Ecol Sociobiol 63:1735–1742

    Google Scholar 

  • Hurst TP (2007) Causes and consequences of winter mortality in fishes. J Fish Biol 71:315–345

    Google Scholar 

  • Hurst T, Conover D (2003) Seasonal and interannual variation in the allometry of energy allocation in juvenile striped bass. Ecology 84:3360–3369

    Google Scholar 

  • Hurst T, Schultz E, Conover D (2000) Seasonal energy dynamics of young-of-the-year Hudson River striped bass. T Am Fish Soc 129:145–157

    Google Scholar 

  • Huss M, Byström P, Strand A et al (2008) Influence of growth history on the accumulation of energy reserves and winter mortality in young fish. Can J Fish Aquat Sci 65:2149–2156

    Google Scholar 

  • Irmler U, Hölker F, Pfeiffer H et al (2008) Biocoenotic interactions between different ecotypes. In: Fränzle O, Kappen L, Blume HP, Dierssen K (eds) Ecosystem organization of a complex landscape. Long-term research in the Bomhöved Lake District, Germany. Springer, Berlin, pp 147–167

  • Jackson D (2002) Ecological effects of Micropterus introductions: the dark side of bass. In: Ridgway MS, Phillip D (eds) Black Bass: ecology, conservation and management. American Fisheries Society, Bethesda, pp 221–232

  • Jackson LJ, Lauridsen TL, Sondergaard M, Jeppesen E (2007) A comparison of shallow Danish and Canadian lakes and implications of climate change. Freshw Biol 52:1782–1792

    CAS  Google Scholar 

  • Janssen J, Corcoran J (1993) Lateral line stimuli can override vision to determine sunfish strike trajectory. J Exp Biol 176:299–305

    PubMed  CAS  Google Scholar 

  • Jeppesen E, Meerhoff M, Holmgren K et al (2010) Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90

    CAS  Google Scholar 

  • Jobling M (1994) Fish bioenergetics. Chapman and Hall, London

    Google Scholar 

  • Johnson TB, Evans DO (1991) Behaviour, energetics, and associated mortality of young-of-the-year white perch (Morone americana) and yellow perch (Perca flavescens) under simulated winter conditions. Can J Fish Aquat Sci 48:672–680

    Google Scholar 

  • Jurvelius J, Marjomaki T (2008) Night, day, sunset: do fish under snow and ice recognize the difference? Freshw Biol 53:2287–2294

    Google Scholar 

  • Kalff J (2002) Limnology. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Kennedy CR, Shears PC, Shears JA (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123:257–269

    PubMed  CAS  Google Scholar 

  • Kirillin G (2010) Modeling the impact of global warming on water temperature and seasonal mixing regimes in small temperate lakes. Boreal Env Res 15:279–293

    Google Scholar 

  • Kirillin G, Hochschild J, Mironov D et al (2011) FLake-Global: online lake model with worldwide coverage. Environ Model Softw 26:683–684

    Google Scholar 

  • Kirillin G, Leppäranta M, Terzhevik A et al (2012) Physics of seasonally ice-covered lakes: a review. Aquat Sci this issue

  • Kirjasniemi M, Valtonen T (1997) Winter mortality of young-of-the-year pikeperch (Stizostedion lucioperca). Ecol Freshw Fish 6:155–160

    Google Scholar 

  • Kitchell JF, Stewart DJ, Weininger D (1977) Applications of a bioenergetics model to yellow perch (Perca flavescens) and walleye (Stizostedion vilreum vtreum). J Fish Res B Can 34:1922–1935

    Google Scholar 

  • Klemetsen A, Amundsen P, Knudsen R, Hemansen B (1997) A profundal, winter spawning morph of Arctic charr Salvelinus alpinus (L.) in lake Fjellfrøsvatn, northern Norway. Nord J Freshw Res 73:13–23

    Google Scholar 

  • Klemetsen A, Knudsen R, Staldvik FJ, Amundsen PAP (2003) Habitat, diet and food assimilation of arctic charr under the winter ice in two subarctic lakes. J Fish Biol 62:1082–1098

    Google Scholar 

  • Klinger SA, Magnuson JJ, Gallepp GW (1982) Survival mechanisms of the central mudminnow (Umbra limi), fathead minnow (Pimephales promelas) and brook stickleback (Culaea inconstans) for low oxygen in winter. Environ Biol Fish 7:113–120

    Google Scholar 

  • Knopf K, Krieger A, Hölker F (2007) Parasite community and mortality of overwintering young-of-the-year roach (Rutilus rutilus). J Parasitol 93:985–991

    PubMed  Google Scholar 

  • Kobler A, Klefoth T, Arlinghaus R (2008a) Site fidelity and seasonal changes in activity centre size of female pike Esox lucius in a small lake. J Fish Biol 73:584–596

    Google Scholar 

  • Kobler A, Klefoth T, Wolter C et al (2008b) Contrasting pike (Esox lucius L.) movement and habitat choice between summer and winter in a small lake. Hydrobiologia 601:17–27

    Google Scholar 

  • Kolok A (1991) Temperature compensation in 2 centrarchid fishes—do winter quiescent fish undergo cellular temperature compensation? T Am Fish Soc 120:52–57

    Google Scholar 

  • Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems. Cambridge University Press, Cambridge

    Google Scholar 

  • Lappalainen J, Tarkan AS (2007) Latitudinal gradients in onset date, onset temperature and duration of spawning of roach. J Fish Biol 70:441–450

    Google Scholar 

  • Lappalainen J, Vinni M (2001) Movement of age-1 pikeperch under the ice cover. J Fish Biol 58:588–590

    Google Scholar 

  • Larsson S, Forseth T, Berglund I et al (2005) Thermal adaptation of Arctic Charr experimental studies of growth in eleven charr populations from Sweden, Norway and Britain. Freshw Biol 50:363–368

    Google Scholar 

  • Lassalle G, Rochard E (2009) Impact of twenty-first century climate change on diadromous fish spread over Europe, North Africa and the Middle East. Glob Change Biol 15:1072–1089

    Google Scholar 

  • Lehtonen H (1998) Winter biology of burbot (Lota lota L). Mem Soc Fauna Flora Fen 74:45–52

    Google Scholar 

  • Lemke P, Ren J, Alley R et al (2007) Observations: changes in snow, ice and frozen ground. Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, New York

  • Lemly A, Esch G (1984) Effects of the trematode Uvuliver ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J Parasitol 70:475–492

    Google Scholar 

  • Lemons D, Crawshaw L (1985) Behavioural and metabolic adjustments to low temperatures in the largemouth bass (Micropterus salmoides). Physiol Zool 58:175–180

    Google Scholar 

  • Lester NP, Shuter BJ, Abrams PA (2004) Interpreting the Von Bertalanffy model of somatic growth in fishes: the cost of reproduction. Proc R Soc B 271:1625–1631

    PubMed  CAS  Google Scholar 

  • Liang X, Liu J, Huang B (1998) The role of sense organs in the feeding behaviour of Chinese perch. J Fish Biol 52:1058–1067

    Google Scholar 

  • Liboriussen L, Lauridsen TL, Sondergaard M et al (2011) Effects of warming and nutrients on sediment community respiration in shallow lakes: an outdoor mesocosm experiment. Freshw Biol 56:437–447

    CAS  Google Scholar 

  • Lima S, Dill L (1990) Behavioural decisions made under risk of predation—a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Linnansaari T, Cunjak R, Newbury R (2008) Winter behaviour of juvenile Atlantic salmon Salmo salar L. in experimental stream channels: effect of substratum size and full ice cover on spatial distribution and activity pattern. J Fish Biol 72:2518–2533

    Google Scholar 

  • Livingstone D (1997) Break-up dates of Alpine lakes as proxy data for local and regional mean surface air temperatures. Clim Chang 37:407–439

    CAS  Google Scholar 

  • Love R (1974) The chemical biology of fishes. Academic Press, London

    Google Scholar 

  • Mackenzie-Grieve J, Post J (2006) Thermal habitat use by lake trout in two contrasting Yukon Territory lakes. T Am Fish Soc 135:727–738

    Google Scholar 

  • Mackereth R, Noakes D, Ridgway M (1999) Size-based variation in somatic energy reserves and parental expenditure by male smallmouth bass, Micropterus dolomieu. Environ Biol Fish 56:263–275

    Google Scholar 

  • Magnuson J, Crowder L, Medvick P (1979) Temperature as an ecological resource. Am Zool 19:331–343

    Google Scholar 

  • Magnuson J, Beckel A, Mills K, Brandt S (1985) Surviving winter hypoxia—behavioural adaptations of fish in a northern Wisconsin winterkill lake. Environ Biol Fishes 14:241–250

    Google Scholar 

  • Magnuson J, Tonn W, Banerjee A et al (1998) Isolation vs. extinction in the assembly of fishes in small northern lakes. Ecology 79:2941–2956

    Google Scholar 

  • Magnuson J, Robertson D, Benson B et al (2000) Historical trends in lake and river ice cover in the Northern Hemisphere. Science 289:1743–1746

    PubMed  CAS  Google Scholar 

  • McDermid J, Shuter B, Lester N (2010) Life history differences parallel environmental differences among North American lake trout (Salvelinus namaycush) populations. Can J Fish Aquat Sci 67:314–325

    Google Scholar 

  • McGinn N (2002) Fisheries in a Changing Climate. American Fisheries Society, Symposium 32. Bethesda

  • Meding ME, Jackson LJ (2001) Biological implications of empirical models of winter oxygen depletion. Can J Fish Aquat Sci 58:1727–1736

    Google Scholar 

  • Mehner T, Busch S, Helland IP et al (2010) Temperature-related nocturnal vertical segregation of coexisting coregonids. Ecol Freshw Fish 19:408–419

    Google Scholar 

  • Mehner T, Busch S, Clemmesen C et al (2012) Ecological commonalities among pelagic fishes: comparison of freshwater ciscoes and marine herring and sprat. Mar Biol. doi:10.1007/s00227-012-1922-9

    Google Scholar 

  • Meisner J (1990) Effect of climatic warming on the southern margins of the native range of brook trout, Salvelinus fontinalis. Can J Fish Aquat Sci 47:1065–1070

    Google Scholar 

  • Meisner J, Goodier J, Regier H et al (1987) An assessment of the effects of climate warming on Great Lakes basin fishes. J Great Lakes Res 13:340–352

    Google Scholar 

  • Migaud H, Davie A, Taylor J (2010) Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. J Fish Biol 76:27–68

    PubMed  CAS  Google Scholar 

  • Mortensen A, Ugedal O, Lund F (2007) Seasonal variation in the temperature preference of Arctic charr (Salvelinus alpinus). J Therm Biol 32:314–320

    CAS  Google Scholar 

  • Nagel F, Hölker F, Wolter C (2011) In situ estimation of gastric evacuation and consumption rates of burbot (Lota lota) in a summer-warm lowland river. J Appl Ichthyol 27:1236–1241

    Google Scholar 

  • Ng CA, Gray KA (2011) Forecasting the effects of global change scenarios on bioaccumulation patterns in great lakes species. Glob Change Biol 17:720–733

    Google Scholar 

  • Nilsson GE, Renshaw GMC (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139

    PubMed  CAS  Google Scholar 

  • O’Connor CM, Gilmour KM, Arlinghaus R, Hasler CT, Philipp DP, Cooke SJ (2010) Seasonal carryover effects following the administration of cortisol to a wild teleost fish. Physiol Biochem Zool 83:950–957

    PubMed  Google Scholar 

  • Ohlberger J, Staaks G, Petzoldt T et al (2008a) Physiological specialization by thermal adaptation drives ecological divergence in a sympatric fish species pair. Evol Ecol Res 10:1173–1185

    Google Scholar 

  • Ohlberger J, Mehner T, Staaks G, Hölker F (2008b) Temperature-related physiological adaptations promote ecological divergence in a sympatric species pair of temperate freshwater fish. Funct Ecol 22:501–508

    Google Scholar 

  • Oliver J, Holeton G, Chua K (1979) Overwinter mortality of fingerling smallmouth bass in relation to size, relative energy stores and environmental-temperature. T Am Fish Soc 108:130–136

    Google Scholar 

  • Plumb J, Blanchfield P (2009) Performance of temperature and dissolved oxygen criteria to predict habitat use by lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 66:2011–2023

    CAS  Google Scholar 

  • Pörtner H (2006) Climate-dependent evolution of Antarctic ectotherms: an integrative analysis. Deep-Sea Res Pt II 53:1071–1104

    Google Scholar 

  • Pörtner H (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893

    PubMed  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    PubMed  Google Scholar 

  • Pörtner H, Peck M (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779

    PubMed  Google Scholar 

  • Pörtner H, Bennett A, Bozinovic F et al (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79:295–313

    PubMed  Google Scholar 

  • Pörtner H, Schulte P, Wood C, Schiemer F (2010) Niche dimensions in fishes: an integrative view. Physiol Biochem Zool 83:808–826

    PubMed  Google Scholar 

  • Post JR, Evans D (1989) Size-dependent overwinter mortality of young-of-year yellow perch (Perca flavescens)—laboratory, in situ enclosure and field experiments. Can J Fish Aquat Sci 46:1958–1968

    Google Scholar 

  • Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 84:1040–1051

    Google Scholar 

  • Rakowitz G, Kubecka J, Fesl C (2009) Intercalibration of hydroacoustic and mark–recapture methods for assessing the spawning population size of a threatened fish species. J Fish Biol 75:1356–1370

    PubMed  CAS  Google Scholar 

  • Reznick D, Braun B (1987) Fat cycling in the mosquito fish (Gambusia affinis)—fat storage as a reproductive adaptation. Oecologia 73:401–413

    Google Scholar 

  • Ridgway MS, Hurley DA, Scott KA (1990) Effects of winter temperature and predation on the abundance of alewife (Alosa pseudoharengus) in the Bay of Quinte, Lake Ontario. J Great Lakes Res 16:11–20

    Google Scholar 

  • Ruuhijarvi J, Rask M, Vesala S et al (2010) Recovery of the fish community and changes in the lower trophic levels in a eutrophic lake after a winter kill of fish. Hydrobiologia 646:145–158

    CAS  Google Scholar 

  • Salinas S, Munch S (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163

    PubMed  Google Scholar 

  • Sargent J, Tocher D, Bell J (2002) The lipids. In: Halver JE, Hardy RS (eds) Fish nutrition, 3rd edn. Academic Press, New York, pp 181–257

  • Schneider K, Newman R, Card V et al (2010) Timing of walleye spawning as an indicator of climate change. T Am Fish Soc 139:1198–1210

    Google Scholar 

  • Schultz E, Conover D (1997) Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia 109:516–529

    Google Scholar 

  • Scott B, Crossman E (1973) Freshwater fishes of Canada. Fisheries Research Board of Canada, Ottawa

    Google Scholar 

  • Seppanen E, Kuukka H, Huuskonen H, Piironen J (2008) Relationship between standard metabolic rate and parasite-induced cataract of juveniles in three Atlantic salmon stocks. J Fish Biol 72:1659–1674

    Google Scholar 

  • Sharma S, Jackson DA, Minns CK, Shuter BJ (2007) Will northern fish populations be in hot water because of climate change? Glob Change Biol 13:2052–2064

    Google Scholar 

  • Sharma S, Vander Zanden MJ, Magnuson JJ, Lyons J (2011) Comparing climate change and species invasions as drivers of coldwater fish population extirpations. PLoS ONE 6:e22906

    PubMed  CAS  Google Scholar 

  • Shimeno S, Kheyyali D, Takeda M (1990) Metabolic adaptation to prolonged starvation in carp. Nippon Suisan Gakk 56:35–41

    CAS  Google Scholar 

  • Shoup DE, Wahl DH (2011) Body size, food, and temperature affect overwinter survival of age-0 Bluegills. Trans Am Fish Soc 140:1298–1304

    Google Scholar 

  • Shuter BJ, Meisner JD (1992) Tools for assessing the impact of climate change on freshwater fish populations. GeoJournal 28:7–20

    Google Scholar 

  • Shuter BJ, Post JR (1990) Climate, population viability and the zoogeography of temperate fishes. T Am Fish Soc 119:314–336

    Google Scholar 

  • Shuter BJ, MacLean J, Fry F, Regier H (1980) Stochastic simulation of temperature effects on first year survival of smallmouth bass. T Am Fish Soc 109:1–29

    Google Scholar 

  • Shuter BJ, Schlesinger DA, Zimmerman AP (1983) Empirical predictors of annual surface water temperature cycles in North American lakes. Can J Fish Aquat Sci 40:1838–1845

    Google Scholar 

  • Shuter BJ, Ihssen P, Wales D, Snucins E (1989) The effects of temperature, Ph and water hardness on winter starvation of young-of-the-year smallmouth bass Micripterus dolomieui Lacepede. J Fish Biol 35:765–780

    Google Scholar 

  • Shuter BJ, Minns C, Lester N (2002) Climate change, freshwater fish and fisheries: case studies from Ontario and thir use in assessing potential impacts. In: McGinn NA (ed) Fisheries in a changing climate. American Fisheries Society, Bethesda, pp 77–88

    Google Scholar 

  • Shuter BJ, Lester N, LaRose J et al (2005) Optimal life histories and food web position: linkages among somatic growth, reproductive investment, and mortality. Can J Fish Aquat Sci 62:738–746

    Google Scholar 

  • Siikavuopio S, Knudsen R, Amundsen P (2010) Growth and mortality of Arctic charr and European whitefish reared at low temperatures. Hydrobiologia 650:255–263

    Google Scholar 

  • Smith L (2000) Trends in Russian Arctic river-ice formation and breakup. Phys Geogr 21:46–56

    Google Scholar 

  • Somero G (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920

    PubMed  CAS  Google Scholar 

  • Sorensen T, Mulderij G, Sondergaard M et al (2011) Winter ecology of shallow lakes: strongest effect of fish on water clarity at high nutrient levels. Hydrobiologia 664:147–162

    CAS  Google Scholar 

  • Stefan H, Fang X, Eaton J (2001) Simulated fish habitat changes in North American lakes in response to projected climate warming. Trans Am Fish Soc 130:459–477

    Google Scholar 

  • Stonevicius E, Stankunavicius G, Kilkus K (2008) Ice regime dynamics in the Nemunas River, Lithuania. Clim Res 36:17–28

    Google Scholar 

  • Strand J, Aarseth J, Hanebrekke T, Jorgensen E (2008) Keeping track of time under ice and snow in a sub-arctic lake: plasma melatonin rhythms in Arctic charr overwintering under natural conditions. J Pineal Res 44:227–233

    PubMed  CAS  Google Scholar 

  • Suski C, Ridgway M (2009a) Winter biology of centrarchid fishes. In: Cooke SJ, Philipp DP (eds) Centrarchid fishes: diversity, biology and conservation. Wiley-Blackwell, Chichester, pp 210–230

  • Suski C, Ridgway M (2009b) Seasonal pattern of depth selection in smallmouth bass. J Zool 279:119–128

    Google Scholar 

  • Svenning M, Klemetsen A (2007) Habitat and food choice of Arctic charr in Linnevatn on Spitsberen, Svalbad: the first year-round investigation in a High Arctic lake. Ecol Freshw Fish 16:70–77

    Google Scholar 

  • Swales S, Lauzier RB, Levings CD (1986) Winter habitat preferences of juvenile salmonids in two interior rivers in British Columbia. Can J Zool 64:1506–1514

    Google Scholar 

  • Teletchea F, Gardeur J-N, Psenicka M et al (2009) Effects of four factors on the quality of male reproductive cycle in pikeperch Sander lucioperca. Aquaculture 291:217–223

    Google Scholar 

  • Tonn W, Magnuson JJ, Rask M, Toivonen J (1990) Intercontinental comparison of small-lake fish assemblages—the balance between local and regional processes. Am Nat 136:345–375

    Google Scholar 

  • Trenberth K, Jones P, Ambenje P et al (2007) Observations: surface and atmospheric climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB., Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, New York

  • Tschantz D, Crockett E, Niewiarowski P, Londraville R (2002) Cold acclimation strategy is highly variable among the sunfishes (Centrarchidae). Physiol Biochem Zool 75:544–556

    PubMed  Google Scholar 

  • Tsuchida S (1995) The relationship between upper temperature tolerance and final preferendum of Japanese marine fish. J Therm Biol 20:35–41

    Google Scholar 

  • Ultsch G (1989) Ecology and physiology of hibernation and overwintering among fresh-water fishes, turtles, and snakes. Biol Rev 64:435–516

    Google Scholar 

  • Ulvan EM, Finstad AG, Ugedal O, Berg OK (2012) Direct and indirect climatic drivers of biotic interactions: ice-cover and carbon runoff shaping Arctic char Salvelinus alpinus and brown trout Salmo trutta competitive asymmetries. Oecologia 168:277–287

    PubMed  Google Scholar 

  • van Dijk P, van Dijk Staaks et al (2002) The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia 130:496–504

    Google Scholar 

  • van Dijk PLM, Hardewig I, Hölker F (2005) Energy reserves during food deprivation and compensatory growth in juvenile roach: the importance of season and temperature. J Fish Biol 66:167–181

    Google Scholar 

  • Vander Zanden M, Casselman J, Rasmussen J (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467

    CAS  Google Scholar 

  • Vehanen T, Lahti M (2003) Movements and habitat use by pikeperch (Stizostedion lucioperca (L.) in a hydropeaking reservoir. Ecol Freshw Fish 12:203–215

    Google Scholar 

  • Venturelli P, Lester N, Marshall T, Shuter B (2010) Consistent patterns of maturity and density-dependent growth among populations of walleye (Sander vitreus): application of the growing degree-day metric. Can J Fish Aquat Sci 67:1057–1067

    Google Scholar 

  • Vuglinski V (2006) Ice regimes in the rivers of Russia, its dynamics during last decades and possible future changes. In: Saeki H (ed) Proceedings of the 18th IAHR international symposium on ice. Nakanishi Publishing Co. Ltd., Sapporo, pp 93–98

  • Vuorinen J, Himberg M, Lankinen P (1981) Genetic differentiation in Coregonus albula (L.) (Salmonidae) populations in Finland. Hereditas 94:113–121

    Google Scholar 

  • Wang N, Xu X, Kestemont P (2009) Effect of temperature and feeding frequency on growth performances, feed efficiency and body composition of pikeperch juveniles (Sander lucioperca). Aquaculture 289:70–73

    Google Scholar 

  • Wedekind C, Kung C (2010) Shift of spawning season and effects of climate warming on developmental stages of grayling (Salmonidae). Conserv Biol 24:1418–1423

    PubMed  Google Scholar 

  • Weyhenmeyer G, Westoo A, Willen E (2008) Increasingly ice-free winters and their effects on water quality in Sweden’s largest lakes. Hydrobiologia 599:111–118

    CAS  Google Scholar 

  • Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Phil Trans R Soc B 365:2093–2106

    PubMed  Google Scholar 

  • Yeates-Burghart Q, O’Brien C, Cresko W et al (2009) Latitudinal variation in photoperiodic response of the three-spined stickleback Gasterosteus aculeatus in western North America. J Fish Biol 75:2075–2081

    PubMed  CAS  Google Scholar 

  • Zhao Y, Shuter B, Jackson D (2008) Life history variation parallels phylogeographical patterns in North American walleye (Sander vitreus) populations. Can J Fish Aquat Sci 65:198–211

    Google Scholar 

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Acknowledgments

We would like to thank Christof Engelhardt, Georgiy Kirllin and Heike Zimmermann-Timm for organizing the Winter Limnology Meeting in Liebenburg and the participants for the stimulating atmosphere. We thank P. Abrams, S. Cooke, J. Magnuson, C. K. Minns and H. A. Regier for their insightful reviews of earlier drafts of the manuscript. Support for this work was provided by the Climate Change Program of the Ontario Ministry of Natural Resources, the Natural Sciences and Engineering Research Council of Canada and the University of Toronto.

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Shuter, B.J., Finstad, A.G., Helland, I.P. et al. The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change. Aquat Sci 74, 637–657 (2012). https://doi.org/10.1007/s00027-012-0274-3

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