Hydrobiologia

, Volume 650, Issue 1, pp 43–54 | Cite as

Arctic charr in sympatry with burbot: ecological and evolutionary consequences

  • Rune Knudsen
  • Per-Arne Amundsen
  • Anders Klemetsen
CHARR

Abstract

The trophic niche and parasite infection of Arctic charr (Salvelinus alpinus) were explored in two lakes with sympatric burbot (Lota lota) and two lakes without burbot in subarctic Norway. The CPUE of burbot and charr were similar in one lake, but burbot had a low population density in the other. Burbot were benthivorous in both lakes. Other co-occurring species like brown trout (Salmo trutta), Atlantic salmon parr (Salmo salar), grayling (Thymallus thymallus) and minnow (Phoxinus phoxinus) were also benthivores. At high densities, benthivorous burbot forced the whole Arctic charr population to utilise mainly the limnetic trophic niche. In contrast, at low burbot density or without burbot present, Arctic charr were primarily benthivorous in the littoral zone. Thus, a clear interactive segregation in diet was observed between Arctic charr and burbot at high burbot densities. There was also a high predation pressure from burbot on young Arctic charr along the benthic zones. The extensive use of zooplankton as prey caused a high parasite infection pressure of copepod transmitted Diphyllobothrium spp. larvae, with the potential for high negative impact on the Arctic charr population. As the benthivore trophic niche was occupied by burbot, the ecological opportunities for polymorphism with benthivorous ecotypes or morphs of Arctic charr were probably prevented. Therefore, the sympatry with burbot seems to have large ecological and evolutionary consequences for this Arctic charr population compared with neighbouring lakes where burbot is absent.

Keywords

Interactive segregation Predation Salvelinus alpinus Lota lota Diphyllobothrium parasites 

Notes

Acknowledgements

We thank Laina Dalsbø, Jan Evjen, Pål-Arne Bjørn and Pål Sørensen for field sampling and laboratory assistance.

References

  1. Adams, C. E. & F. A. Huntingford, 2002. The functional significance of inherited differences in feeding morphology in a sympatric polymorphic population of Arctic charr. Evolutionary Ecology 16: 15–25.CrossRefGoogle Scholar
  2. Adams, C. E. & F. A. Huntingford, 2004. Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr. Biological Journal of the Linnean Society 81: 611–618.CrossRefGoogle Scholar
  3. Amundsen, P.-A., 1994. Piscivory and cannibalism in Arctic charr. Journal of Fish Biology 45: 181–189.CrossRefGoogle Scholar
  4. Amundsen, P.-A. & A. Klemetsen, 1988. Diet, gastric evacuation rates and food-consumption in a stunted population of Arctic charr, Salvelinus alpinus L., in Takvatn, northern Norway. Journal of Fish Biology 33: 697–709.CrossRefGoogle Scholar
  5. Amundsen, P.-A. & R. Knudsen, 2009. Winter ecology of Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in a subarctic lake. Aquatic Ecology 43: 765–775.CrossRefGoogle Scholar
  6. Amundsen, P.-A., H.-M. Gabler & F. J. Staldvik, 1996. A new approach to graphical analyses of feeding strategy from stomach contents data – modification of the Costello (1990) method. Journal of Fish Biology 48: 607–614.Google Scholar
  7. Amundsen, P.-A., R. Knudsen, A. M. Kuris & R. Kristofferesen, 2003. Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102: 285–293.CrossRefGoogle Scholar
  8. Amundsen, P.-A., R. Knudsen & A. Klemetsen, 2007. Intraspecific competition and density dependence of food consumption and growth in Arctic charr. Journal of Animal Ecology 76: 149–158.CrossRefPubMedGoogle Scholar
  9. Amundsen, P.-A., R. Knudsen & A. Klemetsen, 2008. Seasonal and ontogenetic variations in resource use by two sympatric Arctic charr morphs. Environmental Biology of Fishes 83: 45–55.CrossRefGoogle Scholar
  10. Barber, I., D. Hoare & J. Krause, 2000. Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10: 131–165.CrossRefGoogle Scholar
  11. Baumgärtner, D. & K. O. Rothhaupt, 2005. The impact of predation by burbot (Lota lota L.) on the macroinvertebrate community in the littoral zone of a large lake. Aquatic Ecology 39: 79–92.CrossRefGoogle Scholar
  12. Bush, A. O., K. D. Lafferty, J. M. Lotz & A. W. Shostak, 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583.CrossRefPubMedGoogle Scholar
  13. Claessen, D., J. Andersson, L. Persson & A. M. de Roos, 2008. The effect of population size and recombination on delayed evolution of polymorphism and speciation in sexual populations. American Naturalist 172: E18–E34.CrossRefPubMedGoogle Scholar
  14. Curtis, M. A., 1984. Diphyllobothrium spp. and the Arctic charr: parasite acquisition and its effects on a lake resident population. In Johnson, L. & B. I. Burns (eds), Biology of the Arctic charr. Proceedings of the International Symposium on a Arctic charr, Winnipeg, Mannitoba, May 1981. University of Manitoba Press, Winnipeg: 395–411.Google Scholar
  15. Finstad, A. G., O. Ugedal & O. K. Berg, 2006. Growing large in a low grade environment: size dependent foraging gain and niche shifts to cannibalism in Arctic char. Oikos 112: 73–82.CrossRefGoogle Scholar
  16. Forseth, T., O. Ugedal, B. Jonsson & I. A. Fleming, 2003. Selection on Arctic charr generated by competition from brown trout. Oikos 101: 467–478.CrossRefGoogle Scholar
  17. Fratt, T. W., D. W. Coble, F. Copes & R. E. Bruesewitz, 1997. Diet of burbot in Green Bay and western Lake Michigan with comparison with other waters. Journal of Great Lakes Research 23: 1–10.CrossRefGoogle Scholar
  18. Giacomini, H. C., P. De Marco & M. Petrere, 2009. Exploring community assembly through an individual-based model for trophic interactions. Ecological Modeling 220: 23–39.CrossRefGoogle Scholar
  19. Gregersen, F., P. Aass, L. A. Vollestad & J. H. L’Abee-Lund, 2006. Long-term variation in diet of Arctic charr, Salvelinus alpinus, and brown trout, Salmo trutta: effects of changes in fish density and food availability. Fisheries Management and Ecology 13: 243–250.CrossRefGoogle Scholar
  20. Haugen, T. O. & T. A. Rygg, 1996. Food- and habitat-segregation in sympatric grayling and brown trout. Journal of Fish Biology 49: 301–318.CrossRefGoogle Scholar
  21. Henricson, J., 1978. The dynamics of infection of Diphyllobothrium dendriticum (Nitzsch) and D. ditremum (Creplin) in char Salvelinus alpinus, (L.) in Sweden. Journal of Fish Biology 13: 51–71.CrossRefGoogle Scholar
  22. Hesthagen, T., K. Hindar, B. Jonsson, J.-O. Ousdal & H. Holthe, 1995. Effects of acidification on normal and dwarf Arctic charr Salvelinus alpinus (L.) in a Norwegian lake. Biological Conservation 74: 115–123.CrossRefGoogle Scholar
  23. Hindar, K. & B. Jonsson, 1982. Habitat and food segregation of dwarf and normal Arctic charr (Salvelinus alpinus) from Vangsvatnet Lake, western Norway. Canadian Journal of Fisheries and Aquatic Sciences 39: 1030–1045.CrossRefGoogle Scholar
  24. Hirvonen, H., E. Ranta, J. Piironen, A. Laurila & N. Peuhkuri, 2000. Behavioural responses of naive Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos 88: 191–199.CrossRefGoogle Scholar
  25. Hofmann, N. & P. Fischer, 2001. Seasonal change in abundance and age structure of burbot Lota lota (L.) and stone loach Barbatula barbatula (L.) in the littoral zone of a large pre-alpine lake. Ecology of Freshwater Fish 10: 21–25.CrossRefGoogle Scholar
  26. Hofmann, N. & P. Fischer, 2002. Temperature preferences and critical thermal limits of burbot: implications for habitat selection and ontogenetic habitat shift. Transactions of the American Fisheries Society 131: 1164–1172.CrossRefGoogle Scholar
  27. Jansen, P. A., H. Slettvold, A. G. Finstad & A. Langeland, 2002. Niche segregation between Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta): an experimental study of mechanisms. Canadian Journal of Fisheries and Aquatic Sciences 59: 6–11.Google Scholar
  28. Jonsson, B. & N. Jonsson, 2001. Polymorphism and speciation in Arctic charr. Journal of Fish Biology 58: 605–638.CrossRefGoogle Scholar
  29. Kahilainen, K. & H. Lehtonen, 2003. Piscivory and prey selection of four predator species in a whitefish dominated subarctic lake. Journal of Fish Biology 63: 659–672.CrossRefGoogle Scholar
  30. Klemetsen, A., P.-A. Amundsen, H. Muladal, S. Rubach & J. I. Solbakken, 1989. Habitat shifts in a dense, resident Arctic charr Salvelinus alpinus population. Physiology and Ecology, Japan 1(Supplement): 187–200.Google Scholar
  31. Klemetsen, A., P.-A. Amundsen, R. Knudsen & B. Hermansen, 1997. A profundal, winter-spawning morph of Arctic charr Salvelinus alpinus (L.) in Lake Fjellfrøsvatn, northern Norway. Nordic Journal of Freshwater Research 73: 13–23.Google Scholar
  32. Klemetsen, A., P.-A. Amundsen, P. E. Grotnes, R. Knudsen, R. Kristoffersen & M. A. Svenning, 2002a. Takvatn through 20 years: long-term effects of an experimental mass removal of Arctic charr Salvelinus alpinus, from a subarctic lake. Environmental Biology of Fishes 64: 39–47.CrossRefGoogle Scholar
  33. Klemetsen, A., J. M. Elliot, R. Knudsen & P. Sørensen, 2002b. Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr. Journal of Fish Biology 60: 933–950.CrossRefGoogle Scholar
  34. Klemetsen, A., P.-A. Amundsen, J. B. Dempson, B. Jonsson, N. Jonsson, M. F. O’Connell & E. Mortensen, 2003a. Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12: 1–59.CrossRefGoogle Scholar
  35. Klemetsen, A., R. Knudsen, F. J. Staldvik & P.-A. Amundsen, 2003b. Habitat, diet and food assimilation of Arctic charr under the winter ice in two subarctic lakes. Journal of Fish Biology 62: 1082–1098.CrossRefGoogle Scholar
  36. Klemetsen, A., R. Knudsen, R. Primicerio & P.-A. Amundsen, 2006. Divergent natural selection on the feeding behaviour of two sympatric Arctic charr (Salvelinus alpinus) morphs. Ecology of Freshwater Fish 15: 350–355.CrossRefGoogle Scholar
  37. Knudsen, R. & A. Klemetsen, 1994. Infections of Diphyllobothrium dendriticum and D. ditremum (Cestoda), and Cystidicola farionis (Nematoda) in a north Norwegian population of Arctic charr (Salvelinus alpinus) during winter. Canadian Journal of Zoology 72: 1922–1930.CrossRefGoogle Scholar
  38. Knudsen, R., A. Klemetsen & F. Staldvik, 1996. Parasites as indicators of individual feeding specialization in Arctic charr during winter in northern Norway. Journal of Fish Biology 48: 1256–1265.CrossRefGoogle Scholar
  39. Knudsen, R., H.-M. Gabler, A. M. Kuris & P.-A. Amundsen, 2001. Selective predation on parasitized prey – a comparison between two helminth species with different life-history strategies. Journal of Parasitology 87: 941–945.CrossRefPubMedGoogle Scholar
  40. Knudsen, R., P.-A. Amundsen & A. Klemetsen, 2003. Inter- and intra-morph patterns in helminth communities of sympatric whitefish morphs. Journal of Fish Biology 62: 847–859.CrossRefGoogle Scholar
  41. Knudsen, R., M. A. Curtis & R. Kristoffersen, 2004. Aggregation of helminths: the role of feeding behaviour of fish hosts. Journal of Parasitology 90: 1–7.CrossRefPubMedGoogle Scholar
  42. Knudsen, R., A. Klemetsen, P.-A. Amundsen & B. Hermansen, 2006. Incipient speciation through niche expansion: an example from the Arctic charr in a subarctic lake. Proceedings of the Royal Society, B 273: 2291–2298.CrossRefGoogle Scholar
  43. Knudsen, R., P.-A. Amundsen, R. Primicerio, A. Klemetsen & P. Sørensen, 2007. Contrasting niche-based variation on trophic morphology within Arctic charr populations. Evolutionary Ecology Research 9: 1005–1021.Google Scholar
  44. Knudsen, R., R. Primicerio, P.-A. Amundsen & A. Klemetsen, 2010. Temporal stability of individual feeding specialization may promote speciation. Journal of Animal Ecology 79: 161–168.CrossRefPubMedGoogle Scholar
  45. Krebs, C. J., 1999. Ecological methodology. Harper Collins Publishers, New York, NY: 654.Google Scholar
  46. Laakkonen, M. V. M. & H. Hirvonen, 2007. Is boldness towards predators related to growth rate in naive captive-reared Arctic charr (Salvelinus alpinus)? Canadian Journal of Fisheries and Aquatic Science 64: 665–671.CrossRefGoogle Scholar
  47. Langeland, A., J. H. L’Aeelund, B. Jonsson & N. Jonsson, 1991. Resource partitioning and niche shift in Arctic charr Salvelinus alpinus and brown trout Salmo trutta. Journal of Animal Ecology 60: 895–912.CrossRefGoogle Scholar
  48. McLaughlin, R. L., 2001. Behavioural diversification in brook charr: adaptive responses to local conditions. Journal of Animal Ecology 70: 325–337.CrossRefGoogle Scholar
  49. Nilsson, N.-A., 1965. Food segregation between salmonid species in North Sweden. Report of the Institute of Freshwater Research. Drottningholm 2: 58–78.Google Scholar
  50. Nilsson, N.-A., 1967. Interactive segregation between fish species. In Gerking, S. D. (ed.), The Biological Basis of Freshwater Fish Production. Blackwell, Oxford, UK: 295–313.Google Scholar
  51. Østbye, K., P.-A. Amundsen, L. Bernatchez, A. Klemetsen, R. Knudsen, R. Kristoffersen, T. F. Næsje & K. Hindar, 2006. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Molecular Ecology 15: 3983–4001.CrossRefPubMedGoogle Scholar
  52. Prolux, R. & P. Magnan, 2004. Contribution of phenotypic plasticity and heredity to the trophic polymorphism of lacustrine brook charr (Salvelinus fontinalis M.). Evolutionary Ecology Research 6: 503–522.Google Scholar
  53. Robinson, B. W. & K. J. Parsons, 2002. Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1819–1833.CrossRefGoogle Scholar
  54. Ross, S. T., 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia 2: 352–388.CrossRefGoogle Scholar
  55. Roughgarden, J. & J. Diamond, 1986. Overview: the role of species interactions in community ecology. In Diamond, J. & T. J. Case (eds), Community Ecology. Princeton University Press, Princeton, NJ: 333–343.Google Scholar
  56. Saksgård, R. & T. Hesthagen, 2004. A 14-year study of habitat use and diet of brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus) in Lake Atnsjoen, a subalpine Norwegian lake. Hydrobiologia 521: 187–199.CrossRefGoogle Scholar
  57. Sandlund, O. T., K. Gunnarsson, P. M. Jonasson, B. Jonsson, T. Lindem, K. P. Magnusson, H. J. Malmquist, H. Sigurjonsdottir, S. Skulason & S. S. Snorrason, 1992. The Arctic charr Salvelinus alpinus in Thingvallavatn. Oikos 64: 305–351.CrossRefGoogle Scholar
  58. Savino, J. F. & M. Henry, 1991. Feeding rate of slimy sculpin and burbot on young lake charr in laboratory reefs. Environmental Biology of Fishes 31: 275–282.CrossRefGoogle Scholar
  59. Schluter, D., 1993. Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74: 699–709.CrossRefGoogle Scholar
  60. Schoener, T. W., 1974. Resource partitioning in ecological communities. Science 185: 27–39.CrossRefPubMedGoogle Scholar
  61. Schram, S. T., T. B. Johnson & M. J. Seider, 2006. Burbot consumption and relative abundance in the Apostle Island region of Lake Superior. Journal of Great Lakes Research 32: 798–805.CrossRefGoogle Scholar
  62. Skúlason, S. & T. B. Smith, 1995. Resource polymorphism in vertebrates. Trends in Ecology and Evolution 10: 366–370.CrossRefGoogle Scholar
  63. Skúlason, S., S. S. Snorrason, D. Ota & D. L. G. Nokes, 1993. Genetical based differences in foraging behavior among sympatric morphs of Arctic charr (Pisces Salmonidae). Animal Behaviour 45: 1179–1192.CrossRefGoogle Scholar
  64. Svärdson, G., 1976. Interspecific population dominance in fish communities of Scandinavian lakes. Report of the Institute of Freshwater Research. Drottningholm 55: 144–171.Google Scholar
  65. Svenning, M. A. & R. Borgstrøm, 1995. Population structure in landlocked Spitsbergen Arctic charr. Sustained by cannibalism? Nordic Journal of Freshwater Research 71: 424–431.Google Scholar
  66. Tolonen, A., J. Kjellmann & J. Lappalainen, 1999. Diet overlap between burbot (Lota lota (L.)) and whitefish (Coregonus lavaretus (L.)) in a subarctic lake. Annales Zologici Fennici 36: 205–214.Google Scholar
  67. Vamosi, S. M., 2005. On the role of enemies in divergence and diversification of prey: a review and synthesis. Canadian Journal of Zoology 83: 894–910.CrossRefGoogle Scholar
  68. Wallace, R. K., 1981. An assessment of diet-overlap indexes. Transactions of the American Fisheries Society 110: 72–76.CrossRefGoogle Scholar
  69. Wang, N. & A. Appenzeller, 1998. Abundance, depth distribution, diet composition and growth of perch (Perca fluviatilis) and burbot (Lota lota) larvae and juveniles in the pelagic zone of Lake Constance. Ecology of Freshwater Fish 7: 176–183.CrossRefGoogle Scholar
  70. Westgaard, J. I., A. Klemetsen & R. Knudsen, 2004. Genetic differences between two sympatric morphs of Arctic charr Salvelinus alpinus (L.) confirmed by microsatellite DNA. Journal of Fish Biology 65: 1185–1191.CrossRefGoogle Scholar
  71. Wilson, A. D. M. & R. L. McLaughlin, 2007. Behavioural syndromes in brook charr, Salvelinus fontinalis: prey-search in the field corresponds with space use in novel laboratory situations. Animal Behaviour 74: 689–698.CrossRefGoogle Scholar
  72. Wootton, R. J., 1998. Ecology of Teleost Fishes, 2nd ed. Kluwer Academic Publishers, Dordrecht: 378.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Rune Knudsen
    • 1
  • Per-Arne Amundsen
    • 1
  • Anders Klemetsen
    • 1
  1. 1.Department of Arctic and Marine BiologyUniversity of TromsøTromsøNorway

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