, Volume 170, Issue 1, pp 275–287 | Cite as

Plasticity in habitat use determines metabolic response of fish to global warming in stratified lakes

  • Susan Busch
  • Georgiy Kirillin
  • Thomas Mehner
Global change ecology - Original research


We used a coupled lake physics and bioenergetics-based foraging model to evaluate how the plasticity in habitat use modifies the seasonal metabolic response of two sympatric cold-water fishes (vendace and Fontane cisco, Coregonus spp.) under a global warming scenario for the year 2100. In different simulations, the vertically migrating species performed either a plastic strategy (behavioral thermoregulation) by shifting their population depth at night to maintain the temperatures occupied at current in-situ observations, or a fixed strategy (no thermoregulation) by keeping their occupied depths at night but facing modified temperatures. The lake physics model predicted higher temperatures above 20 m and lower temperatures below 20 m in response to warming. Using temperature–zooplankton relationships, the density of zooplankton prey was predicted to increase at the surface, but to decrease in hypolimnetic waters. Simulating the fixed strategy, growth was enhanced only for the deeper-living cisco due to the shift in thermal regime at about 20 m. In contrast, simulating the plastic strategy, individual growth of cisco and young vendace was predicted to increase compared to growth currently observed in the lake. Only growth rates of older vendace are reduced under future global warming scenarios irrespective of the behavioral strategy. However, performing behavioral thermoregulation would drive both species into the same depth layers, and hence will erode vertical microhabitat segregation and intensify inter-specific competition between the coexisting coregonids.


Coregonus Bioenergetics Behavioral thermoregulation Microhabitat segregation Diel vertical migration 



This study was financed by the Aquashift Priority Program of the German Research Foundation (DFG, project No. Me 1686/5-2, 5-3) and the German Academic Exchange Service (DAAD, D/08/46923).

Supplementary material

442_2012_2286_MOESM1_ESM.doc (3.8 mb)
Supplementary material 1 (DOC 3920 kb)


  1. Anneville O, Souissi S, Molinero JC, Gerdeaux D (2009) Influences of human activity and climate on the stock-recruitment dynamics of whitefish, Coregonus lavaretus, in Lake Geneva. Fish Manag Ecol 16:492–500CrossRefGoogle Scholar
  2. Appenzeller AR, Leggett WC (1995) An evaluation of light-mediated vertical migration of fish based on hydroacoustic analysis of the diel vertical movements of rainbow smelt Osmerus mordax. Can J Fish Aquat Sci 52:504–511CrossRefGoogle Scholar
  3. Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12:235–239PubMedCrossRefGoogle Scholar
  4. Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672–675PubMedCrossRefGoogle Scholar
  5. Beitinger TL, Fitzpatrick LC (1979) Physiological and ecological correlates of preferred temperature in fish. Am Zool 19:319–329Google Scholar
  6. Berteaux D, Reale D, McAdam AG, Boutin S (2004) Keeping pace with fast climate change: can arctic life count on evolution? Integr Comp Biol 44:140–151PubMedCrossRefGoogle Scholar
  7. Bevelhimer MS, Adams SM (1993) A bioenergetics analysis of diel vertical migration by kokanee salmon, Oncorhynchus nerka. Can J Fish Aqust Sci 50:2336–2349CrossRefGoogle Scholar
  8. Biette RM, Geen GH (1980) Growth of underyearling sockeye salmon (Oncorhynchus nerka) under constant and cyclic temperatures in relation to live zooplankton ration size. Can J Fish Aquat Sci 37:203–210CrossRefGoogle Scholar
  9. Bøhn T, Amundsen PA, Sparrow A (2008) Competitive exclusion after invasion? Biol Invasions 10:359–368CrossRefGoogle Scholar
  10. Brett JR (1971a) Energetic responses of salmon to temperature—Study of some thermal relations in physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am Zool 11:99–113Google Scholar
  11. Brett JR (1971b) Satiation time, appetite, and maximum food intake of sockeye salmon (Oncorhynchus nerka). J Fish Res Bd Can 28:409–415CrossRefGoogle Scholar
  12. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  13. Busch S, Mehner T (2009) Hydroacoustic estimates of fish population depths and densities at increasingly longer time scales. Int Rev Hydrobiol 94:91–102CrossRefGoogle Scholar
  14. Busch S, Johnson BM, Mehner T (2011) Energetic costs and benefits of cyclic habitat switching: a bioenergetics model analysis of diel vertical migration in coregonids. Can J Fish Aquat Sci 68:706–717CrossRefGoogle Scholar
  15. Bystrøm P, Andersson J, Kiessling A, Eriksson LO (2006) Size and temperature dependent foraging capacities and metabolism: consequences for winter starvation mortality in fish. Oikos 115:43–52CrossRefGoogle Scholar
  16. Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 135:131–138. doi: 10.2307/3544421 CrossRefGoogle Scholar
  17. Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526CrossRefGoogle Scholar
  18. DeStasio BT, Hill DK, Kleinhans JM, Nibbelink NP, Magnuson JJ (1996) Potential effects of global climate change on small north-temperate lakes: physics, fish, and plankton. Limnol Oceanogr 41:1136–1149CrossRefGoogle Scholar
  19. Dulvy NK, Rogers SI, Jennings S, Stelzenmüller V, Dye SR, Skjodal HR (2008) Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. J Appl Ecol 45:1–11CrossRefGoogle Scholar
  20. Elliott JA, Bell VA (2011) Predicting the potential long-term influence of climate change on vendace (Coregonus albula) habitat in Bassenthwaite Lake, UK. Freshw Biol 56:395–405CrossRefGoogle Scholar
  21. Fang X, Stefan HG (2009) Simulations of climate effects on water temperature, dissolved oxygen, and ice and snow covers in lakes of the contiguous United States under past and future climate scenarios. Limnol Oceanogr 54:2359–2370CrossRefGoogle Scholar
  22. Fischer RU, Standora EA, Spotila JR (1987) Predator-induced changes in thermoregulation of bluegill, Lepomis macrochirus, from a thermally altered reservoir. Can J Fish Aquat Sci 44:1629–1634CrossRefGoogle Scholar
  23. Fry FEJ (1947) Effects of the environment on animal activity. Univ Toronto Stud Biol Ser 55. Publ Ont Fish Res Lab 68:1–62Google Scholar
  24. Gerten D, Adrian R (2000) Climate-driven changes in spring plankton dynamics and the sensitivity of shallow polymictic lakes to the North Atlantic oscillation. Limnol Oceanogr 45:1058–1066CrossRefGoogle Scholar
  25. Gillooly JF (2000) Effect of body size and temperature on generation time in zooplankton. J Plankton Res 22:241–251CrossRefGoogle Scholar
  26. Gjelland KØ, Bøhn T, Knudsen FR, Amundsen PA (2004) Influence of light on the swimming speed of coregonids in subarctic lakes. Ann Zool Fenn 41:137–146Google Scholar
  27. Gjelland KØ, Bøhn T, Horne JK, Jensvoll I, Knudsen FR, Amundsen PA (2009) Planktivore vertical migration and shoaling under a subarctic light regime. Can J Fish Aquat Sci 66:525–539CrossRefGoogle Scholar
  28. Golosov S, Kirillin G (2010) A parameterized model of heat storage by lake sediments. Environ Model Softw 25:793–801CrossRefGoogle Scholar
  29. Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448CrossRefGoogle Scholar
  30. Graham CT, Harrod C (2009) Implications of climate change for the fishes of the British isles. J Fish Biol 74:1143–1205PubMedCrossRefGoogle Scholar
  31. Helland IP, Freyhof J, Kasprzak P, Mehner T (2007) Temperature sensitivity of vertical distributions of zooplankton and planktivorous fish in a stratified lake. Oecologia 151:322–330PubMedCrossRefGoogle Scholar
  32. Helland IP, Harrod C, Freyhof J, Mehner T (2008) Co-existence of a pair of pelagic planktivorous coregonid fishes. Evol Ecol Res 10:373–390Google Scholar
  33. Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455CrossRefGoogle Scholar
  34. Jacobson PC, Stefan HG, Pereira DL (2010) Coldwater fish oxythermal habitat in Minnesota lakes: influence of total phosphorus, July air temperature, and relative depth. Can J Fish Aquat Sci 67:2002–2013CrossRefGoogle Scholar
  35. Jobling M (1981) Temperature tolerance and the final preferendum—rapid methods for the assessment of optimum growth temperatures. J Fish Biol 19:439–455CrossRefGoogle Scholar
  36. Kahilainen K, Malinen T, Tuomaala A, Lehtonen H (2004) Diel and seasonal habitat and food segregation of three sympatric Coregonus lavaretus forms in a subarctic lake. J Fish Biol 64:418–434CrossRefGoogle Scholar
  37. Karl I, Fischer K (2008) Why get big in the cold? towards a solution to a life-history puzzle. Oecologia 155:215–225PubMedCrossRefGoogle Scholar
  38. Kirillin G (2010) Modeling the impact of global warming on water temperature and seasonal mixing regimes in small temperate lakes. Boreal Environ Res 15:279–293Google Scholar
  39. Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol, SwitzerlandGoogle Scholar
  40. Lusseau D, Williams R, Wilson B, Grellier K, Barton TR, Hammond PS, Thompson PM (2004) Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins. Ecol Lett 7:1068–1076CrossRefGoogle Scholar
  41. Magnuson JJ, Crowder LB, Medvick PA (1979) Temperature as an ecological resource. Am Zool 19:331–343Google Scholar
  42. Medvick PA, Magnuson JJ, Sharr S (1981) Behavioral thermoregulation and social interactions of bluegills, Lepomis macrochirus. Copeia 9–13Google Scholar
  43. Mehner T, Kasprzak P (2011) Partial diel vertical migrations in pelagic fish. J Anim Ecol 80:761–770PubMedCrossRefGoogle Scholar
  44. Mehner T, Kasprzak P, Hölker F (2007) Exploring ultimate hypotheses to predict diel vertical migrations in coregonid fish. Can J Fish Aquat Sci 64:874–886CrossRefGoogle Scholar
  45. Mehner T, Padisak J, Kasprzak P, Koschel R, Krienitz L (2008) A test of food web hypotheses by exploring time series of fish, zooplankton and phytoplankton in an oligo-mesotrophic lake. Limnologica 38:179–188CrossRefGoogle Scholar
  46. Mehner T, Busch S, Helland IP, Emmrich M, Freyhof J (2010) Temperature-related nocturnal vertical segregation of coexisting coregonids. Ecol Freshw Fish 19:408–419CrossRefGoogle Scholar
  47. Mehner T, Schiller S, Staaks G, Ohlberger J (2011) Cyclic temperatures influence growth efficiency and biochemical body composition of vertically migrating fish. Freshw Biol 56:1554–1566CrossRefGoogle Scholar
  48. Mironov DV (2008) Parameterization of lakes in numerical weather prediction. description of a lake model. COSMO technical report 11. Deutscher Wetterdienst, Offenbach am Main, Germany, pp 41Google Scholar
  49. Moore MV, Folt CL, Stemberger RS (1996) Consequences of elevated temperatures for zooplankton assemblages in temperate lakes. Arch Hydrobiol 135:289–319Google Scholar
  50. Nakićenović N, Swart R (2000) Special report on emissions scenarios. a special report of Working Group III of the Intergovernmental Panel on climate change. Nakićenović N, Swart R (eds) Cambridge University Press, CambridgeGoogle Scholar
  51. Neverman D, Wurtsbaugh WA (1994) The thermoregulatory function of diel vertical migration for a juvenile fish, Cottus extensus. Oecologia 98:247–256CrossRefGoogle Scholar
  52. Ohlberger J, Mehner T, Staaks G, Hölker F (2008a) Is ecological segregation in a pair of sympatric coregonines supported by divergent feeding efficiencies? Can J Fish Aquat Sci 65:105–2113CrossRefGoogle Scholar
  53. 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, Coregonus spp. Funct Ecol 22:501–508CrossRefGoogle Scholar
  54. Ohlberger J, Staaks G, Petzoldt T, Mehner T, Hölker F (2008c) Physiological specialization by thermal adaptation drives ecological divergence in a sympatric fish species pair. Evol Ecol Res 10:1173–1185Google Scholar
  55. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915PubMedCrossRefGoogle Scholar
  56. Podrabsky JE, Clelen D, Crawshaw LI (2008) Temperature preference and reproductive fitness of the annual killifish Austrofundulus limnaeus exposed to constant and fluctuating temperatures. J Comp Physiol A 194:385–393CrossRefGoogle Scholar
  57. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692PubMedCrossRefGoogle Scholar
  58. Pritchard JR, Schluter D (2001) Declining interspecific competition during character displacement: summoning the ghost of competition past. Evol Ecol Res 3:209–220Google Scholar
  59. Pulgar JM, Aldana M, Bozinovic F, Ojeda FP (2003) Does food quality influence thermoregulatory behavior in the intertidal fish Girella laevifrons? J Therm Biol 28:539–544CrossRefGoogle Scholar
  60. Räisänen J, Hansson U, Ullerstig A et al (2004) European climate in the late twenty-first century: regional simulations with two driving global models and two forcing scenarios. Clim Dynam 22:13–31CrossRefGoogle Scholar
  61. Reynolds WW (1977) Temperature as a proximate factor in orientation behavior. J Fish Res Bd Can 34:734–739CrossRefGoogle Scholar
  62. Scheuerell MD, Schindler DW (2003) Diel vertical migration by juvenile sockeye salmon: empirical evidence for the antipredation window. Ecology 84:1713–1720CrossRefGoogle Scholar
  63. Schindler DW (1997) Widespread effects of climatic warming on freshwater ecosystems in North America. Hydrol Process 11:1043–1067CrossRefGoogle Scholar
  64. Schurmann H, Steffensen JF, Lomholt JP (1991) The influence of hypoxia on the preferred temperature of rainbow trout Oncorhynchus mykiss. J Exp Biol 157:75–86Google Scholar
  65. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370PubMedCrossRefGoogle Scholar
  66. Southward AJ, Hawkins SJ, Burrows MT (1995) 70 years observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English-channel in relation to rising sea temperature. J Therm Biol 20:127–155CrossRefGoogle Scholar
  67. Stefan HG, Hondzo M, Fang X, Eaton JG, McCormick JH (1996) Simulated long-term temperature and dissolved oxygen characteristics of lakes in the north-central United States and associated fish habitat limits. Limnol Oceanogr 41:1124–1135CrossRefGoogle Scholar
  68. Stevenson RD, Peterson CR, Tsuji JS (1985) The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol Zool 58:46–57Google Scholar
  69. Straile D, Eckmann R, Jungling T, Thomas G, Löffler H (2007) Influence of climate variability on whitefish (Coregonus lavaretus) year-class strength in a deep, warm monomictic lake. Oecologia 151:521–529PubMedCrossRefGoogle Scholar
  70. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870CrossRefGoogle Scholar
  71. Ward AJW, Hensor EMA, Webster MM, Hart PJB (2010) Behavioural thermoregulation in two freshwater fish species. J Fish Biol 76:2287–2298PubMedCrossRefGoogle Scholar
  72. Watson RT (2001) Climate change 2001: Synthesis report a contribution of Working Groups I, II and III to the Third Assessment Report of the Intergovernmental Panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  73. Werner EE (1994) Ontogenetic scaling of competitive relations: size-dependent effects and responses in two anuran larvae. Ecology 75:197–213CrossRefGoogle Scholar
  74. Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Biology and Ecology of FishesLeibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany
  2. 2.Department of EcohydrologyLeibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany

Personalised recommendations