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Hydrobiologia

, Volume 783, Issue 1, pp 65–78 | Cite as

A specialised cannibalistic Arctic charr morph in the piscivore guild of a subarctic lake

  • Rune Knudsen
  • Karl Øystein Gjelland
  • Antti P. Eloranta
  • Brian Hayden
  • Anna Siwertsson
  • Per-Arne Amundsen
  • Anders Klemetsen
CHARR II

Abstract

Arctic charr (Salvelinus alpinus) is generally considered an inferior piscivore compared to brown trout (Salmo trutta). However, we demonstrate that a recently described profundal spawning piscivore PP-morph of Arctic charr in a subarctic lake has evolved typical piscivore traits (i.e. large jaws, robust skulls), similar to the co-occurring brown trout but different from the sympatric littoral spawning omnivore LO-morph of Arctic charr. A few large-sized LO-morph, most large-sized PP-morph and trout constitute the piscivore guild, but they differed in prey fish selection. Of the fish-eating deep-water PP-morph, 52% had consumed charr, with a peak during the polar night period (68–80% in November–January). In contrast, the LO-morph and trout were mainly (~90%) inter-specific piscivores eating stickleback. Consequently, the PP-morph was the main charr predator and started to feed on fish at a smaller size and took larger prey relative to their body length than the trout. Stable isotope (δ13C, δ15N) ratios reflect the dietary specialisations in the upper-water (LO-morph, trout) and the deep-water (PP-morph) environments, besides the piscivorous behaviour of the PP-morph and trout. The existence of a shallow-water piscivore (trout) may explain the origin of this PP-morph, taking benefit of underutilised resources of small-sized Arctic charr in the deep-water habitat.

Keywords

Profundal Tri-morphism Salvelinus alpinus Brown trout Salmo trutta Prey fish 

Notes

Acknowledgments

We acknowledge the fieldwork assistance from our Department Engineers: Cesilie Bye, Laina Dalsbø and Karin S. Johannessen, and former Master-students: Kristin Johansen, Sigrid Skoglund, Aslak Smalås and John F. Strøm. Marianne Simonsen has placed landmarks on the photographs for the analyses of the morphological traits. Sigrid Skoglund made the drawing of the head of Arctic charr. We also thank the Guest Editor and the Assistant Editor for their support, and R.N. Sinnatamby and one anonymous referee for very constructive and helpful reviews.

Supplementary material

10750_2015_2601_MOESM1_ESM.docx (1.9 mb)
Supplementary material 1 (DOCX 1914 kb)

References

  1. Adams, C. E., D. Fraser, F. A. Huntingford, R. B. Greer, C. M. Askew & A. F. Walker, 1998. Trophic polymorphism amongst Arctic charr from Loch Rannoch, Scotland. Journal of Fish Biology 52: 1259–1271.CrossRefGoogle Scholar
  2. Alekseyev, S. S., V. P. Samusenok, A. N. Matveev & M. Y. Pichugin, 2002. Diversification, sympatric speciation, and trophic polymorphism of Arctic charr Salvelinus alpinus complex, in Transbaikalia. Environmental Biology of Fishes 64: 97–114.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., 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
  5. Amundsen, P.-A., M.-A. Svenning & S. I. Siikavuopio, 1999. An experimental comparison of cannibalistic response in different Arctic charr (Salvelinus alpinus (L.)) stocks. Ecology of Freshwater Fish 8: 43–48.CrossRefGoogle Scholar
  6. Amundsen, P.-A., R. Knudsen & A. Klemetsen, 2008. Seasonal and ontogenetic variations in resource use of two sympatric Arctic charr morphs. Environmental Biology of Fishes 83: 45–56.CrossRefGoogle Scholar
  7. Andersson, J., P. Bystrom, D. Claessen, L. Persson & A. M. De Roos, 2007. Stabilization of population fluctuations due to cannibalism promotes resource polymorphism in fish. American Naturalist 169: 820–829.CrossRefPubMedGoogle Scholar
  8. Bøhn, T., P.-A. Amundsen, O. Popova, Y. S. Reshetnikov & F. J. Staldvik, 2002. Predator avoidance by coregonids: can habitat choice be explained by size-related prey vulnerability? Archive führ Hydrobiologia Special Issues Advances in Limnology 57: 183–197.Google Scholar
  9. Byström, P., P. Ask, J. Andersson & L. Persson, 2013. Preference for cannibalism and ontogenetic constraints in competitive ability of piscivorous top predators. PLoS ONE 8: e70404.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Claessen, D., A. M. De Roos & L. Persson, 2000. Dwarfs and giants: cannibalism and competition in size-structured populations. American Naturalist 155: 219–237.CrossRefPubMedGoogle Scholar
  11. Claessen, D., C. Van Oss, A. M. De Roos & L. Persson, 2002. The impact of size-dependent predation on population dynamics and individual life history. Ecology 6: 1660–1675.CrossRefGoogle Scholar
  12. DeGraaf, M., E. Dejen, J. W. M. Osse & F. A. Sibbing, 2008. Adaptive radiation of Lake Tana’s (Ethiopia) Labeobarbus species flock (Pisces, Cyprinidae). Marine and Freshwater Research 59: 391–407.CrossRefGoogle Scholar
  13. Elliott, J. M., 2011. A comparative study of the relationship between light intensity and feeding ability in brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus). Freshwater Biology 56: 1962–1972.CrossRefGoogle Scholar
  14. Elliott, J. M. & M. A. Hurley, 2000. Daily energy intake and growth of piscivorous brown trout, Salmo trutta. Freshwater Biology 44: 237–245.CrossRefGoogle Scholar
  15. Eloranta, A. P., R. Knudsen & P.-A. Amundsen, 2013a. Niche segregation of coexisting Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) constrains food web coupling in subarctic lakes. Freshwater Biology 58: 207–221.CrossRefGoogle Scholar
  16. Eloranta, A. P., H. L. Mariash, M. Rautio & M. Power, 2013b. Lipid-rich zooplankton subsidise the winter diet of benthivorous Arctic charr (Salvelinus alpinus) in a subarctic lake. Freshwater Biology 58: 2541–2554.CrossRefGoogle Scholar
  17. Eloranta, A. P., K. K. Kahilainen, P.-A. Amundsen, R. Knudsen, C. Harrod & R. I. Jones, 2015. Lake size and fish diversity determine resource use and trophic position of a top predator in high-latitude lakes. Ecology and Evolution 5: 1664–1675.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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
  19. Frandsen, F., H. J. Malmquist & S. S. Snorrason, 1989. Ecological parasitology of polymorphic Arctic charr, Salvelinus alpinus (L.), in Thingvallavatn. Iceland. Journal of Fish Biology 34: 281–297.CrossRefGoogle Scholar
  20. Fraser, D., C. E. Adams & F. A. Huntingford, 1998. Trophic polymorphism among Arctic charr Salvelinus alpinus L., from Loch Ericht. Scotland. Ecology of Freshwater Fish 7: 184–191.CrossRefGoogle Scholar
  21. Fraser, D., F. A. Huntingford & C. E. Adams, 2008. Foraging specialisms, prey size and life-history patterns: a test of predictions using sympatric polymorphic Arctic charr (Salvelinus alpinus). Ecology of Freshwater Fish 17: 1–9.CrossRefGoogle Scholar
  22. Gislason, D., M. Ferguson, S. Skulason & S. S. Snorrason, 1999. Rapid and coupled phenotypic and genetic divergence in Icelandic Arctic char (Salvelinus alpinus). Canadian Journal of Fisheries and Aquatic Science 56: 2229–2234.CrossRefGoogle Scholar
  23. Gjelland, K. Ø., T. Bøhn, J. K. Horne, I. Jensvoll, F. R. Knudsen & P.-A. Amundsen, 2009. Planktivore vertical migration and shoaling under a subarctic light regime. Canadian Journal of Fisheries and Aquatic Science 66: 525–539.CrossRefGoogle Scholar
  24. Hayden, B., C. Harrod & K. K. Kahilainen, 2014. Dual fuels: intra-annual variation in the relative importance of benthic and pelagic resources to maintenance, growth and reproduction in a generalist salmonid fish. Journal of Animal Ecology 83: 1501–1512.CrossRefPubMedGoogle Scholar
  25. Henriksen, E. H., R. Knudsen, R. Kristoffersen, A. M. Kuris, K. D. Lafferty, A. Siwertsson & P.-A. Amundsen, 2016. Ontogenetic dynamics of infection with Diphyllobothrium spp. cestodes in sympatric Arctic charr Salvelinus alpinus (L.) and brown trout Salmo trutta L. Hydrobiologia. doi: 10.1007/s10750-015-2589-2.Google Scholar
  26. Hestdahl, H.I., 2013. Temporal differences in reproductive development of two morphs of Arctic charr (Salvelinus alpinus). Master-theses (in Norwegian), UiT the Arctic University of Norway.Google Scholar
  27. Jackson, L. J., S. R. Carpenter, J. Manchester-Neesvig & C. A. Stow, 2001. PCB congeners in Lake Michigan coho (Oncorhynchus kisutch) and Chinook (Oncorhynchus tshawytscha) salmon. Environmental Science & Technology 35: 856–862.CrossRefGoogle Scholar
  28. Jensen, H., K. K. Kahilainen, P.-A. Amundsen, K. O. Gjelland, A. Tuomaala, T. Malinen & T. Bøhn, 2008. Predation by brown trout (Salmo trutta) along a diversifying prey community gradient. Canadian Journal of Fisheries and Aquatic Sciences 65: 1831–1841.CrossRefGoogle Scholar
  29. Jonsson, B. & N. Jonsson, 2001. Polymorphism and speciation in Arctic charr. Journal of Fish Biology 58: 605–638.CrossRefGoogle Scholar
  30. Jørgensen, L. & A. Klemetsen, 1995. Food resource partitioning of Arctic charr, Salvelinus alpinus (L.) and three-spined stickleback, Gasterosteus aculeatus L., in the littoral zone of lake Takvatn in northern Norway. Ecology of Freshwater Fish 4: 77–84.CrossRefGoogle Scholar
  31. Juanes, F., 2003. The allometry of cannibalism in piscivorous fishes. Canadian Journal of Fisheries and Aquatic Sciences 60: 594–602.CrossRefGoogle Scholar
  32. Kahilainen, K. & H. Lehtonen, 2002. Brown trout (Salmo trutta L.) and Arctic charr (Salvelinus alpinus (L.)) as predators on three sympatric whitefish (Coregonus lavaretus (L.)) forms in the subarctic Lake Muddusjarvi. Ecology of Freshwater Fish 11: 158–167.CrossRefGoogle Scholar
  33. Kahilainen, K. & K. Østbye, 2006. Morphological differentiation and resource polymorphism in three sympatric whitefish Coregonus lavaretus (L.) forms in a subarctic lake. Journal of Fish Biology 68: 63–79.CrossRefGoogle Scholar
  34. Klemetsen, A., 2010. The charr problem revisited: exceptional phenotypic plasticity promotes ecological speciation in postglacial lakes. Freshwater Reviews 3: 49–74.CrossRefGoogle Scholar
  35. 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
  36. Klemetsen, A., J. M. Elliott, R. Knudsen & P. Sørensen, 2002. Evidence for genetic differences in the offspring of two sympatric morphs of Arctic charr. Journal of Fish Biology 60: 933–950.CrossRefGoogle Scholar
  37. Klemetsen, A., P.-A. Amundsen, J. B. Dempson, B. Jonsson, N. Jonsson, M. F. O’Connell & E. Mortensen, 2003. 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
  38. Klemetsen, A., R. Knudsen, R. Primicerio & P.-A. Amundsen, 2006. Divergent, genetically based feeding behaviour of two sympatric Arctic charr, Salvelinus alpinus (L.), morphs. Ecology of Freshwater Fish 15: 350–355.CrossRefGoogle Scholar
  39. 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
  40. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Knudsen, R., P.-A. Amundsen, R. Primicerio, A. Klemetsen & P. Sørensen, 2007. Contrasting niche-based variation in trophic morphology within Arctic charr populations. Evolutionary Ecology Research 9: 1005–1021.Google Scholar
  42. Knudsen, R., P.-A. Amundsen, R. Nilsen, R. Kristoffersen & A. Klemetsen, 2008. Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout. Environmental Biology of Fishes 83: 107–116.CrossRefGoogle Scholar
  43. Knudsen, R., A. Siwertsson, C. E. Adams, M. Garduño-Paz, J. Newton & P.-A. Amundsen, 2011. Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures. Evolutionary Ecology 25: 589–604.CrossRefGoogle Scholar
  44. Knudsen, R., H. Johnsen, B.-S. Sæther & S. I. Siikavuopio, 2015. Divergent growth patterns between juveniles of two sympatric Arctic charr morphs with contrasting depth gradient niche preferences. Aquatic Ecology 49: 33–42.CrossRefGoogle Scholar
  45. Knudsen, R., P.-A. Amundsen, A. Siwertsson, A. Eloranta, B. Hayden & A. Klemetsen, 2016. Parallel evolution of profundal Arctic charr morphs in two contrasting fish communities. Hydrobiologia. doi: 10.1007/s10750-016-2647-4.Google Scholar
  46. L’Abée-Lund, J. H., A. Langeland & H. Sægrov, 1992. Piscivory by brown trout Salmo trutta L and Arctic charr Salvelinus alpinus (L.) in Norwegian lakes. Journal of Fish Biology 41: 91–101.CrossRefGoogle Scholar
  47. L’Abée-Lund, J. H., P. Aass & H. Sægrov, 2002. Long-term variation in piscivory in a brown trout population: effects of changes in available prey organisms. Ecology of Freshwater Fish 11: 260–269.CrossRefGoogle Scholar
  48. Losos, J. B., 2010. Adaptive radiation, ecological opportunity, and evolutionary determinism. American Naturalist 175: 623–639.CrossRefPubMedGoogle Scholar
  49. Magnusson, K. P. & M. M. Ferguson, 1987. Genetic-analysis of 4 sympatric morphs of Arctic charr, Salvelinus alpinus, from Thingvallavatn, Iceland. Environmental Biology of Fishes 20: 67–73.CrossRefGoogle Scholar
  50. Martin, C. H. & P. C. Wainwright, 2011. Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of cyprinodon pupfish. Evolution 65: 2197–2212.CrossRefPubMedGoogle Scholar
  51. Mittelbach, G. G. & L. Persson, 1998. The ontogeny of piscivory and its ecological consequences. Canadian Journal of Fisheries and Aquatic Sciences 55: 1454–1465.CrossRefGoogle Scholar
  52. Muir, A. M., M. J. Hansen, C. R. Bronte & C. C. Krueger, 2016. If Arctic charr Salvelinus alpinus is ‘the most diverse vertebrate’, what is the lake charr Salvelinus namaycush? Fish and Fisheries. doi: 10.1111/faf.12114.Google Scholar
  53. Oleinik, A. & L. Skurikhina, 2010. Mitochondrial DNA diversity and relationships of endemic charrs of the genus Salvelinus from Lake Kronotskoye (Kamchatka Peninsula). Hydrobiology 650: 145–159.CrossRefGoogle Scholar
  54. Öhlund, G., P. Hedström, S. Norman, C. L. Hein & G. Englund, 2015. Temperature dependence of predation depends on the relative performance of predators and prey. Proceedings of the Royal Society B 282: 20142254.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Pavlov, S. D., K. V. Kuzishchin, M. A. Gruzdeva, A. L. Senchukova & E. A. Pivovarov, 2013. Phenetic diversity and spatial structure of chars (Salvelinus) of the Kronotskaya riverine lacustrine system (Eastern Kamchatka). Journal of Ichthyology 53: 662–686.CrossRefGoogle Scholar
  56. Persson, L., P.-A. Amundsen, A. M. De Roos, A. Klemetsen, R. Knudsen & R. Primicerio, 2007. Culling prey promotes predator recovery – alternative states in a whole-lake experiment. Science 316: 1743–1746.CrossRefPubMedGoogle Scholar
  57. Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.CrossRefGoogle Scholar
  58. Power, M., M. F. O’Connell & J. B. Dempson, 2005. Ecological segregation within and among Arctic char morphotypes in Gander Lake, Newfoundland. Environmental Biology of Fishes 73: 263–274.CrossRefGoogle Scholar
  59. R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  60. Robinson, B. & 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
  61. Salmenkova, E., V. Omel’chenko, O. Radchenko, N. Gordeeva, G. Rubtsova & N. Romanov, 2005. Genetic divergence of chars of the genus Salvelinus from Kronotsky Lake (Kamchatka Peninsula). Russian Journal of Genetics 41: 897–906.CrossRefGoogle Scholar
  62. Sandlund, O. T., K. Gunnarsson, P. Jónasson, B. Jonsson, T. Lindem, K. P. Magnusson, H. J. Malmquist, H. Sigurjonsdottir, S. Skúlason & S. S. Snorrasson, 1992. The Arctic charr Salvelinus alpinus in Thingvallavatn. Oikos 64: 305–351.CrossRefGoogle Scholar
  63. Schliewen, U., D. Tautz & S. Päbo, 1994. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 306–308.CrossRefGoogle Scholar
  64. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, UK.Google Scholar
  65. Schoener, T. W., 1970. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51: 408–418.CrossRefGoogle Scholar
  66. Seehausen, O. & C. E. Wagner, 2014. Speciation in freshwater fishes. Annual Review of Ecology, Evolution, and Systematics 45: 621–651.CrossRefGoogle Scholar
  67. Siwertsson, A., R. Knudsen, C. E. Adams, K. Præbel & P.-A. Amundsen, 2013. Parallel and non-parallel morphological divergence amongst foraging specialists in European whitefish (Coregonus lavaretus). Ecology and Evolution 3: 1590–1602.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Siwertsson, A., B. Refsnes, A. Frainer, P.-A. Amundsen & R. Knudsen, 2016. Parallel parasite communities in Arctic charr morphs with similar trophic niches. Hydrobiologia. doi: 10.1007/s10750-015-2563-z.
  69. Skoglund, S., A. Siwertsson, P.-A. Amundsen & R. Knudsen, 2015. Morphological divergence between three Arctic charr morphs – the significance of the deep-water environment. Ecology and Evolution 5: 3114–3129.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Skúlason, S. & T. B. Smith, 1995. Resource polymorphism in vertebrates. Trends in Ecology and Evolution 10: 366–370.CrossRefPubMedGoogle Scholar
  71. Skúlason, S., D. L. G. Noakes & S. S. Snorrason, 1989. Ontogeny of trophic morphology in 4 sympatric morphs of Arctic charr Salvelinus alpinus in Thingvallavatn, Iceland. Biological Journal of the Linnean Society 38: 281–301.CrossRefGoogle Scholar
  72. Smalås, A., P.-A. Amundsen & R. Knudsen, 2013. Contrasting life history strategies between sympatric Arctic charr morphs, Salvelinus alpinus. Journal of Ichtyology 53: 856–866.CrossRefGoogle Scholar
  73. Snorrason, S. S., S. Skúlason, B. Jonsson, H. J. Malmquist, P. M. Jonasson, O. T. Sandlund & T. Lindem, 1994. Trophic specialization in Arctic charr Salvelinus alpinus (Pisces; Salmonidae): morphological divergence and ontogenetic niche shifts. Biological Journal of the Linnean Society 52: 1–18.CrossRefGoogle Scholar
  74. Svenning, M. A. & R. Borgstrøm, 2005. Cannibalism in Arctic charr: do all individuals have the same propensity to be cannibals? Journal of Fish Biology 66: 957–965.CrossRefGoogle Scholar
  75. Turner, B. J. D. D., T. M. Bunt Duvernell & M. G. Barton, 2008. Reproductive isolation among endemic pupfishes (Cyprinodon) on San Salvador Island, Bahamas: microsatellite evidence. Biological Journal of the Linnean Society 95: 566–582.CrossRefGoogle Scholar
  76. Verspoor, E., D. Knox, R. Greer & J. Hammar, 2010. Mitochondrial DNA variation in Arctic charr (Salvelinus alpinus (L.)) morphs from Loch Rannoch, Scotland: evidence for allopatric and peripatric divergence. Hydrobiologia 650: 117–131.CrossRefGoogle Scholar
  77. Warnes, G. R., 2013. gmodels: Various R programming tools for model fitting. R package version 2.15.4.1. Includes R source code and/or documentation contributed by B. Bolker, T. Lumley, R.C. Johnson. http://CRAN.R-project.org/package=gmodels.

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Rune Knudsen
    • 1
  • Karl Øystein Gjelland
    • 2
  • Antti P. Eloranta
    • 3
    • 4
  • Brian Hayden
    • 5
  • Anna Siwertsson
    • 1
  • Per-Arne Amundsen
    • 1
  • Anders Klemetsen
    • 1
  1. 1.Department of Arctic and Marine BiologyUiT The Arctic University of NorwayTromsøNorway
  2. 2.Norwegian Institute for Nature ResearchFram CentreTromsøNorway
  3. 3.Aquatic Ecology DepartmentNorwegian Institute for Nature Research (NINA)TrondheimNorway
  4. 4.Department of Biological and Environmental SciencesUniversity of JyväskyläJyväskyläFinland
  5. 5.Biology DepartmentUniversity of New BrunswickFrederictonCanada

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