, Volume 664, Issue 1, pp 147–162 | Cite as

Winter ecology of shallow lakes: strongest effect of fish on water clarity at high nutrient levels

  • Torben Sørensen
  • Gabi Mulderij
  • Martin Søndergaard
  • Torben L. Lauridsen
  • Lone Liboriussen
  • Sandra Brucet
  • Erik Jeppesen
Primary research paper


While the structuring role of fish in lakes is well studied for the summer season in North temperate lakes, little is known about their role in winter when fish activity and light irradiance potentially are lower. This is unfortunate as the progressing climate change may have strong effects on lake winter temperature and possibly on trophic dynamics too. We conducted an enclosure experiment with and without the presence of fish throughout winter in two shallow lakes with contrasting phosphorus concentrations. In hypertrophic Lake Søbygård, absence of fish led to higher biomass of zooplankton, higher grazing potential (zooplankton:phytoplankton ratio) and, accordingly, lower biomass of phytoplankton and chlorophyll a (Chl a), while the concentrations of total nitrogen (TN), total phosphorus (TP), oxygen and pH decreased. The average size of egg-bearing Daphnia and Bosmina and the minimum size of egg-bearing specimens of the two genera rose. In the less eutrophic Lake Stigsholm, zooplankton and their grazing potential were also markedly affected by fish. However, the decrease in Chl a was slight, and phytoplankton biovolume, pH and the oxygen concentration were not affected. TN was higher when fish were absent. Our results indicate that: (i) there is a notable effect of fish on zooplankton community structure and size during winter in both eutrophic and hypertrophic North temperate lakes, (ii) Chl a can be high in winter in such lakes, despite low light irradiance, if fish are abundant, and (iii) the cascading effects on phytoplankton and nutrients in winter may be more pronounced in hypertrophic lakes. Climate warming supposedly leading to reduced winter mortality and dominance of small fish may enhance the risk of turbid state conditions in nutrient-enriched shallow lakes, not only during the summer season, but also during winter.


Shallow Eutrophic Hypertrophic Lakes Phytoplankton Zooplankton Planktivorous fish Nutrients 



We wish to thank the owners of the lakes, Kirsten and Ove Henriksen (Stigsholm) and Wefri a/s Frijsenborg and Wedellsborg (Søbygård), for permission to set up the experiments. The technical staff at the National Environmental Research Institute, Silkeborg, is gratefully acknowledged for their assistance. We are also grateful to Anne Mette Poulsen for skilful editorial assistance. The study was supported by the projects EU WISER and EU REFRESH, CRES and CLEAR (a Villum Kann Rasmussen Centre of Excellence project).


  1. Adrian, R. & R. Deneke, 1996. Possible impact of mild winters on zooplankton succession in eutrophic lakes of the Atlantic European area. Freshwater Biology 36: 757–770.CrossRefGoogle Scholar
  2. Balayla, D., T. Lauridsen, M. Søndergaard & E. Jeppesen, 2010. Larger zooplankton in Danish lakes after cold winters: are winter fish kills of importance? Hydrobiologia 646: 159–172.CrossRefGoogle Scholar
  3. Bottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-Ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norwegian Journal Zoology 24: 419–456.Google Scholar
  4. Bramm, M. E., M. F. Lassen, L. Liboriussen, M. Ventura & E. Jeppesen, 2009. Fish-zooplankton-phytoplankton interactions in shallow lakes at contrasting irradiance levels with special focus on the winter season. Freshwater Biology 54: 1093–1109.CrossRefGoogle Scholar
  5. Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and composition of plankton. Science 150: 28–35.PubMedCrossRefGoogle Scholar
  6. Brönmark, C., J. Brodersen, B. B. Chapman, A. Nicolle, P. A. Nilsson, C. Skov & L.-A. Hansson, 2010. Regime shifts in shallow lakes: the importance of seasonal fish migration. Hydrobiologia 646: 91–100.CrossRefGoogle Scholar
  7. Brucet, S., D. Boix, X. D. Quintana, E. Jensen, L. W. Nathansen, C. Trochine, M. Meerhoff, S. Gascón & E. Jeppesen, 2010. Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnology and Oceanography 55: 1697–1711.CrossRefGoogle Scholar
  8. Burks, R. L., D. M. Lodge, E. Jeppesen & T. Lauridsen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting littoral zones. Freshwater Biology 47: 343–365.CrossRefGoogle Scholar
  9. Carpenter, S. R. & J. F. Kitchell (eds), 1993. The Trophic Cascade in Lakes. Cambridge University Press, Cambridge.Google Scholar
  10. Cox, E. J., 1996. Identification of Freshwater Diatoms from Live Material. Chapman & Hall, London.Google Scholar
  11. Culver, D. A., M. M. Boucherle, D. J. Bean & J. W. Fletcher, 1985. Biomass of freshwater crustacean zooplankton from length-weight regressions. Canadian Journal of Fisheries and Aquatic Sciences 42: 1380–1390.CrossRefGoogle Scholar
  12. Dumont, H. J., I. Van de Velde & S. Dumont, 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19: 75–97.CrossRefGoogle Scholar
  13. Fowler, J., L. Cohen & P. Jarvis, 1998. Practical Statistics for Field Biology, 2nd ed. Wiley, New York.Google Scholar
  14. George, D. G. & D. P. Hewitt, 1999. The influence of year-to-year variations in winter weather on the dynamics of Daphnia and Eudiaptomus in Esthwaite Water, Cumbria. Functional Ecology 13: 45–54.CrossRefGoogle Scholar
  15. Gliwicz, Z. M., 2003. Between hazards of starvation and risk of predation: ecology of offshore animals. In Kinne, O. (ed.), Excellence of Ecology, Book 12. International Ecology Institute, Oldendorf/Luhe: 379 pp.Google Scholar
  16. Grafen, A. & R. Hails, 2002. Modern Statistics for the Life Sciences. Oxford University Press, Oxford.Google Scholar
  17. Hansen, A.-M., E. Jeppesen, S. Bosselmann & P. Andersen, 1992. Zooplankton i søer-metoder og artsliste. Miljøprojekt nr. 205. Miljøministeriet, Miljøstyrelsen. (in Danish).Google Scholar
  18. Hansson, L.-A., A. Nicolle, J. Brodersen, P. Romare, P. A. Nilsson, C. Brönmark & C. Skov, 2007. Consequences of fish predation, migration, and juvenile ontogeny on zooplankton spring dynamics. Limnology and Oceanography 52: 696–706.CrossRefGoogle Scholar
  19. Havens, K. E., & J. B. Beaver, 2011. Composition, size, and biomass of zooplankton in large productive Florida lakes. Hydrobiologia. doi: 10.1007/s10750-010-0386-5.
  20. Hessen, D. O., P. J. Færøvig & T. Andersen, 2002. Light, nutrients, and P:C ratios in algae grazers performance related to food quality and quantity. Ecology 83: 1886–1898.CrossRefGoogle Scholar
  21. IPCC, 2007. Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.Google Scholar
  22. Jacobsen, L., S. Berg, M. Broberg, N. Jepsen & C. Skov, 2002. Activity and food choice of piscivorous perch (Perca fluviatilis) in a eutrophic shallow lake: a radio-telemetry study. Freshwater Biology 47: 2370–2379.CrossRefGoogle Scholar
  23. Jacobsen, L., S. Berg, N. Jepsen & C. Skov, 2004. Does roach behaviour differ between shallow lakes of different environmental state? Journal of Fish Biology 65: 135–147.CrossRefGoogle Scholar
  24. Jensen, H. S. & F. Ø. Andersen, 1992. Importance of temperature, nitrate and pH for phosphorus from aerobic sediments of four shallow, eutrophic lakes. Limnology and Oceanography 37: 577–589.CrossRefGoogle Scholar
  25. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen, L. J. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 242(343): 151–164.CrossRefGoogle Scholar
  26. Jeppesen, E., J. P. Jensen, C. Jensen, B. Faafeng, D. O. Hessen, M. Søndergaard, T. L. Lauridsen, P. Brettum & K. Christoffersen, 2003. The impact of nutrient state and lake depth on top-down control in lakes: study of 466 lakes from the temperate zone to the Arctic. Ecosystems 6: 315–325.CrossRefGoogle Scholar
  27. Jeppesen, E., J. P. Jensen, M. Søndergaard, M. Fenger-Grøn, K. Sandby, P. H. Møller & H. U. Rasmussen, 2004. Does fish predation influence zooplankton community structure and grazing during winter in north temperate lakes? Freshwater Biology 49: 432–447.CrossRefGoogle Scholar
  28. Jeppesen, E., M. Søndergaard, A. R. Pedersen, K. Jürgens, A. Strzelczak, T. L. Lauridsen & L. S. Johansson, 2007. Salinity induced regime shift in shallow brackish lagoons. Ecosystems 10: 47–57.CrossRefGoogle Scholar
  29. Jeppesen, E., B. Kronvang, M. Meerhoff, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridsen, M. Beklioglu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. Journal of Environmental Quality 38: 1030–1041.CrossRefGoogle Scholar
  30. Jepsen, N. & S. Berg, 2002. The use of winter refuges by roach tagged with miniature radio transmitters. Hydrobiologia 483: 167–173.CrossRefGoogle Scholar
  31. Jespersen, A.-M. & K. Christoffersen, 1987. Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie 109: 445–454.Google Scholar
  32. Jones, J. I. & S. Waldron, 2003. Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshwater Biology 48: 1396–1407.CrossRefGoogle Scholar
  33. Karlsson, J. & C. Sawström, 2009. Benthic algae support zooplankton growth during winter in a clear-water lake. Oikos 118: 539–544.Google Scholar
  34. Keast, A., 1968. Feeding of some Great Lakes fishes at low temperatures. Journal of the Fisheries Research Board of Canada 25: 1199–1218.Google Scholar
  35. Komárek, J. & B. Fott, 1983. Das Phytoplankton des Süßwassers 7, 1: Chlorophyceae (Grünalgen). Ordnung: Chlorococcales. Schweizerbart, Stuttgart.Google Scholar
  36. Koroleff, F., 1976a. Determination of total phosphorus. In Grasshoff, K. (ed.), Methods of Seawater. Verlag Chemie, Weinheim: 168–172.Google Scholar
  37. Koroleff, F., 1976b. Determination of total nitrogen. In Grasshoff, K. (ed.), Methods of Seawater. Verlag Chemie, Weinheim: 123–125.Google Scholar
  38. Lampert, W., 1977. Studies on the carbon balance of Daphnia pulex de Geer as related to environmental conditions. IV. Determination of the “threshold” concentration as a factor controlling the abundance of zooplankton species. Archiv für Hydrobiologie—Supplement 3: 361–368.Google Scholar
  39. Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshwater Biology 48: 418–431.CrossRefGoogle Scholar
  40. McCauley, E., 1984. The estimation of the abundance and biomass of zooplankton in samples. In Downing, J. A. & F. H. Rigler (eds), A Manual on Methods for the Assessment of Secondary Productivityin Fresh Waters, 2nd ed. Blackwell Scientific Publishers, Oxford: 228–265.Google Scholar
  41. Moss, B., 1998. The Ecology of Freshwaters, Man and Medium, Past to Future, 3rd ed. Blackwell Science, Oxford.Google Scholar
  42. Olrik, K. 1991. Planteplanktonmetoder—prøvetagning, bearbejdning og rapportering ved undersøgelser af planteplankton i søer og marine områder. Miljøprojekt nr. 187. Miljøministeriet. Miljøstyrelsen. [Phytoplankton methods—sampling, analyses and reports when analysing phytoplankton in lake and marine waters. Environmental project no. 187. Ministry of the Environment. Danish Environment Protection Agency] (in Danish).Google Scholar
  43. Pace, M. L., J. J. Cole, S. R. Carpenter & J. F. Kitchell, 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution 14: 483–488.PubMedCrossRefGoogle Scholar
  44. Pekcan-Hekim, Z. & J. Lappalainen, 2006. Effects of clay turbidity and density of pikeperch (Sander lucioperca) larvae on predation by perch (Perca fluviatilis). Naturwissenschaften 93: 356–359.PubMedCrossRefGoogle Scholar
  45. Reynolds, C. F., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.Google Scholar
  46. Rudstam, L. G., R. C. Lathrop & S. R. Carpenter, 1993. The rise and fall of a dominant planktivore: direct and indirect effects on zooplankton. Ecology 74: 303–319.CrossRefGoogle Scholar
  47. Ruuhijärvi, J., M. Rask, S. Vesala, A. Westermark, M. Olin, J. Keskitalo & A. Lehtovaara, 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.CrossRefGoogle Scholar
  48. Sokal, R. R. & F. J. Rohlf, 1995. Biometry—The Principles and Practice of Statistics in Biological Research, 3rd ed. W. H. Freeman and Company, New York.Google Scholar
  49. Sommer, U., Z. M. Gliwicz, W. Lambert & A. Duncan, 1986. The PEG-model for seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 433–471.Google Scholar
  50. Sterner, R. W., & J. J. Elser, 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, NJ.Google Scholar
  51. Sterner, R. W., J. J. Elser, E. J. Fee, S. J. Guildford & T. H. Chrzanowski, 1997. The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. American Naturalist 150: 663–684.PubMedCrossRefGoogle Scholar
  52. Søndergaard, M., T. L. Lauridsen, E. Jeppesen & L. Bruun, 1997. Macrophyte-waterfowl interactions: tracking a variable resource and the impact of herbivory on plant growth. In Jeppesen, E., Ma. Søndergaard, Mo. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Ecological Studies, Vol. 131. Springer Verlag, New York: 298–307.Google Scholar
  53. Tikkanen, T. & T. Willén, 1992. Växtplanktonflora. Naturvårdsverket, Eskilstuna (in Swedish).Google Scholar
  54. Urabe, J., M. Kyle, W. Makino, T. Yoshida, T. Andersen & J. J. Elser, 2002. Reduced light increases herbivore production due to stoichiometric effects of light:nutrient balance. Ecology 83: 619–627.CrossRefGoogle Scholar
  55. Vanni, M. J. & D. L. Findley, 1990. Trophic cascades and phytoplankton community structure. Ecology 71: 921–937.CrossRefGoogle Scholar
  56. Vijverberg, J., 1980. Effect of temperature in laboratory studies on development and growth of Cladocera and Copepoda from Tjeukemeer, the Netherlands. Freshwater Biology 10: 317–340.CrossRefGoogle Scholar
  57. Winberg, G. G., 1971. Methods for the Estimation of Production of Aquatic Animals (trans. by A. Duncan). Academic Press, London.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Torben Sørensen
    • 1
    • 2
  • Gabi Mulderij
    • 1
    • 3
  • Martin Søndergaard
    • 1
    • 6
  • Torben L. Lauridsen
    • 1
    • 6
  • Lone Liboriussen
    • 1
  • Sandra Brucet
    • 1
    • 4
  • Erik Jeppesen
    • 1
    • 5
    • 6
  1. 1.Department of Freshwater Ecology, National Environmental Research InstituteAarhus UniversitySilkeborgDenmark
  2. 2.Institute of BiologyUniversity of Southern DenmarkOdense MDenmark
  3. 3.Koeman en Bijkerk BV Ecological Research and ConsultancyHarenThe Netherlands
  4. 4.European Commission, Joint Research Centre, Institute for Environment and SustainabilityIspraItaly
  5. 5.Greenland Climate Research Centre (GCRC), Greenland Institute of Natural ResourcesNuukGreenland
  6. 6.Sino-Danish Research CentreBeijingChina

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