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
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
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
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
Baroudy E, Elliot JM (1994) Racial differences in eggs and juveniles of Windermere charr, Salvelinus alpinus. J Fish Biol 45:407–415
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
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
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
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
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
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
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
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
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
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
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
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
Bradshaw W, Holzapfel C (2006) Climate change—evolutionary response to rapid climate change. Science 312:1477–1478
Bradshaw W, Holzapfel C (2007) Evolution of animal photoperiodism. Ann Rev Ecol Evol Syst 38:1–25
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
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
Buisson L, Grenouillet G (2009) Contrasted impacts of climate change on stream fish assemblages along an environmental gradient. Divers Distrib 15:613–626
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
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
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
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
Clarke A, Pörtner HO (2010) Temperature, metabolic power and the evolution of endothermy. Biol Rev 85:703–727
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
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
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
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
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
Coutant CC (1990) Temperature-oxygen habitat for freshwater and coastal striped bass in a changing climate. T Am Fish Soc 119:240–253
Cunjak R (1996) Winter habitat of selected stream fishes and potential impacts from land-use activity. Can J Fish Aquat Sci 53:267–282
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
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
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
Daufresne M, Boet P (2007) Climate change impacts on structure and diversity of fish communities in rivers. Glob Change Biol 13:2467–2478
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
DeWitt TJSA, Wilson R (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
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
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
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
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
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
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
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
Evans DO (1984) Temperature independence of the annual cycle of standard metabolism in the pumpkinseed. T Am Fish Soc 113:494–512
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
Fang X, Stefan H (2000) Projected climate change effects on winterkill in shallow lakes in the northern United States. Environ Manag 25:291–304
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
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
Finstad A, Naesje T, Forseth T (2004b) Seasonal variation in the thermal performance of juvenile Atlantic salmon (Salmo salar). Freshwater Biol 49:1459–1467
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
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
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
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
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
Gerdeaux D (2011) Does global warming threaten the dynamics of Arctic charr in Lake Geneva? Hydrobiologia 660:69–78
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
Greenbank J (1945) Limnological conditions in ice-covered lakes, especially as related to winter-kill of fish. Ecol Monogr 15:343–392
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
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
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
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
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
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
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
Heermann L, Eriksson L, Magnhagen C, Borcherding J (2009) Size-dependent energy storage and winter mortality of perch. Ecol Freshw Fish 18:560–571
Heibo E, Magnhagen C, Vollestad LA (2005) Latitudinal variation in life-history traits in Eurasian perch. Ecology 86:3377–3386
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
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
Henderson B, Wong J, Nepszy S (1996) Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci 53:127–133
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
Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916
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
Hokanson K (1977) Temperature requirements of some percids and adaptations to the seasonal temperature cycle. J Fish Res Bd Canada 34:1524–1550
Hölker F (2006) Effects of body size and temperature on metabolism of bream compared to sympatric roach. Anim Biol 56:23–37
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
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
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
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
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
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
Hurst TP (2007) Causes and consequences of winter mortality in fishes. J Fish Biol 71:315–345
Hurst T, Conover D (2003) Seasonal and interannual variation in the allometry of energy allocation in juvenile striped bass. Ecology 84:3360–3369
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
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
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
Janssen J, Corcoran J (1993) Lateral line stimuli can override vision to determine sunfish strike trajectory. J Exp Biol 176:299–305
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
Jobling M (1994) Fish bioenergetics. Chapman and Hall, London
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
Jurvelius J, Marjomaki T (2008) Night, day, sunset: do fish under snow and ice recognize the difference? Freshw Biol 53:2287–2294
Kalff J (2002) Limnology. Prentice Hall, Englewood Cliffs
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
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
Kirillin G, Hochschild J, Mironov D et al (2011) FLake-Global: online lake model with worldwide coverage. Environ Model Softw 26:683–684
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
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
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
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
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
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
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
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
Kolok A (1991) Temperature compensation in 2 centrarchid fishes—do winter quiescent fish undergo cellular temperature compensation? T Am Fish Soc 120:52–57
Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems. Cambridge University Press, Cambridge
Lappalainen J, Tarkan AS (2007) Latitudinal gradients in onset date, onset temperature and duration of spawning of roach. J Fish Biol 70:441–450
Lappalainen J, Vinni M (2001) Movement of age-1 pikeperch under the ice cover. J Fish Biol 58:588–590
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
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
Lehtonen H (1998) Winter biology of burbot (Lota lota L). Mem Soc Fauna Flora Fen 74:45–52
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
Lemons D, Crawshaw L (1985) Behavioural and metabolic adjustments to low temperatures in the largemouth bass (Micropterus salmoides). Physiol Zool 58:175–180
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
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
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
Lima S, Dill L (1990) Behavioural decisions made under risk of predation—a review and prospectus. Can J Zool 68:619–640
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
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
Love R (1974) The chemical biology of fishes. Academic Press, London
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
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
Magnuson J, Crowder L, Medvick P (1979) Temperature as an ecological resource. Am Zool 19:331–343
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
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
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
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
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
Mehner T, Busch S, Helland IP et al (2010) Temperature-related nocturnal vertical segregation of coexisting coregonids. Ecol Freshw Fish 19:408–419
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
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
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
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
Mortensen A, Ugedal O, Lund F (2007) Seasonal variation in the temperature preference of Arctic charr (Salvelinus alpinus). J Therm Biol 32:314–320
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
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
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
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
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
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
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
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
Pörtner H (2006) Climate-dependent evolution of Antarctic ectotherms: an integrative analysis. Deep-Sea Res Pt II 53:1071–1104
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
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97
Pörtner H, Peck M (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779
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
Pörtner H, Schulte P, Wood C, Schiemer F (2010) Niche dimensions in fishes: an integrative view. Physiol Biochem Zool 83:808–826
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
Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 84:1040–1051
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
Reznick D, Braun B (1987) Fat cycling in the mosquito fish (Gambusia affinis)—fat storage as a reproductive adaptation. Oecologia 73:401–413
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
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
Salinas S, Munch S (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163
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
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
Scott B, Crossman E (1973) Freshwater fishes of Canada. Fisheries Research Board of Canada, Ottawa
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
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
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
Shimeno S, Kheyyali D, Takeda M (1990) Metabolic adaptation to prolonged starvation in carp. Nippon Suisan Gakk 56:35–41
Shoup DE, Wahl DH (2011) Body size, food, and temperature affect overwinter survival of age-0 Bluegills. Trans Am Fish Soc 140:1298–1304
Shuter BJ, Meisner JD (1992) Tools for assessing the impact of climate change on freshwater fish populations. GeoJournal 28:7–20
Shuter BJ, Post JR (1990) Climate, population viability and the zoogeography of temperate fishes. T Am Fish Soc 119:314–336
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
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
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
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
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
Siikavuopio S, Knudsen R, Amundsen P (2010) Growth and mortality of Arctic charr and European whitefish reared at low temperatures. Hydrobiologia 650:255–263
Smith L (2000) Trends in Russian Arctic river-ice formation and breakup. Phys Geogr 21:46–56
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
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
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
Stonevicius E, Stankunavicius G, Kilkus K (2008) Ice regime dynamics in the Nemunas River, Lithuania. Clim Res 36:17–28
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
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
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
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
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
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
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
Tsuchida S (1995) The relationship between upper temperature tolerance and final preferendum of Japanese marine fish. J Therm Biol 20:35–41
Ultsch G (1989) Ecology and physiology of hibernation and overwintering among fresh-water fishes, turtles, and snakes. Biol Rev 64:435–516
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
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
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
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
Vehanen T, Lahti M (2003) Movements and habitat use by pikeperch (Stizostedion lucioperca (L.) in a hydropeaking reservoir. Ecol Freshw Fish 12:203–215
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
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
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
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
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
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
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
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
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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DOI: https://doi.org/10.1007/s00027-012-0274-3