Skip to main content
Log in

Ontogenetic dynamics of infection with Diphyllobothrium spp. cestodes in sympatric Arctic charr Salvelinus alpinus (L.) and brown trout Salmo trutta L.

  • CHARR II
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The trophic niches of Arctic charr and brown trout differ when the species occur in sympatry. Their trophically transmitted parasites are expected to reflect these differences. Here, we investigate how the infections of Diphyllobothrium dendriticum and D. ditremum differ between charr and trout. These tapeworms use copepods as their first intermediate hosts and fish can become infected as second intermediate hosts by consuming either infected copepods or infected fish. We examined 767 charr and 368 trout for Diphyllobothrium plerocercoids in a subarctic lake. The prevalence of D. ditremum was higher in charr (61.5%) than in trout, (39.5%), but the prevalence of D. dendriticum was higher in trout (31.2%) than in charr (19.3%). Diphyllobothrium spp. intensities were elevated in trout compared to charr, particularly for D. dendriticum. Large fish with massive parasite burdens were responsible for the high Diphyllobothrium spp. loads in trout. We hypothesize that fish prey may be the most important source for the Diphyllobothrium spp. infections in trout, whereas charr predominantly acquire Diphyllobothrium spp. by feeding on copepods. Our findings support previous suggestions that the ability to establish in a second piscine host is greater for D. dendriticum than for D. ditremum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amundsen, P.-A., 1994. Piscivory and cannibalism in Arctic charr. Journal of Fish Biology 45: 181–189.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Amundsen, P.-A., K. D. Lafferty, R. Knudsen, R. Primicerio, A. Klemetsen & A. M. Kuris, 2009. Food web topology and parasites in the pelagic zone of a subarctic lake. Journal of Animal Ecology 78: 563–572.

    Article  PubMed  Google Scholar 

  • Andersen, K. I. & D. I. Gibson, 1989. A key to three species of larval Diphyllobothrium Cobbold, 1858 (Cestoda: Pseudophyllidea) occurring in European and North American freshwater fishes. Systematic Parasitology 13: 3–9.

    Article  Google Scholar 

  • Bérubé, M. & M. A. Curtis, 1986. Transmission of Diphyllobothrium ditremum to Arctic Char (Salvelinus alpinus) in two Subarctic Quebec lakes. Canadian Journal of Fisheries and Aquatic Sciences 43: 1626–1634.

    Article  Google Scholar 

  • Blanar, C. A., M. A. Curtis & H. M. Chan, 2005. Growth, nutritional composition, and hematology of Arctic charr (Salvelinus alpinus) exposed to toxaphene and tapeworm (Diphyllobothrium dendriticum) larvae. Archives of Environmental Contamination and Toxicology 48: 397–404.

    Article  CAS  PubMed  Google Scholar 

  • Bolnick, D. I., T. Ingram, W. E. Stutz, L. K. Snowberg, O. L. Lau & J. S. Paull, 2010. Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proceedings of the Royal Society B: Biological Sciences 277: 1789–1797.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bylund, G., 1972. Pathogenic effects of a diphyllobothriid plerocercoid on its host fishes. Commentationes Biologicae, Societas Scientiarum Fennica 58: 1–11.

    Google Scholar 

  • 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, Manitoba. University of Manitoba Press, Winnipeg, Manitoba: 395–411.

  • Eloranta, A. P., R. Knudsen & P.-A. Amundsen, 2013. 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.

    Article  Google Scholar 

  • Finstad, A. G., P. A. Jansen & A. Langeland, 2000. Gillnet selectivity and size and age structure of an alpine Arctic char (Salvelinus alpinus) population. Canadian Journal of Fisheries and Aquatic Sciences 57: 1718–1727.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gallagher, C. P. & T. A. Dick, 2010. Trophic structure of a landlocked Arctic char Salvelinus alpinus population from southern Baffin Island, Canada. Ecology of Freshwater Fish 19: 39–50.

    Article  Google Scholar 

  • Halvorsen, O., 1970. Studies of the helminth fauna of Norway XV: on the taxonomy and biology of plerocercoids of Diphyllobothrium Cobbold, 1858 (Cestoda, Pseudophyllidea) from north-western Europe. Nytt Magasin for Zoologi 18: 113–174.

    Google Scholar 

  • Halvorsen, O. & K. Andersen, 1984. The ecological interaction between arctic charr, Salvelinus alpinus (L.), and the plerocercoid stage of Diphyllobothrium ditremum. Journal of Fish Biology 25: 305–316.

    Article  Google Scholar 

  • Halvorsen, O. & K. Wissler, 1973. Studies of the helminth fauna of Norway XXVIII: An experimental study of the ability of Diphyllobothrium latum (L.), D. dendriticum (Nitzsch), and D. ditremum (Creplin) (Cestoda, Pseudophyllidea) to infect paratenic hosts. Norwegian Journal of Zoology 21: 201–210.

    Google Scholar 

  • Hammar, J., 2000. Cannibals and parasites: Conflicting regulators of bimodality in high latitude Arctic char, Salvelinus alpinus. Oikos 88: 33–47.

    Article  Google Scholar 

  • Harrington, L. A., A. L. Harrington, N. Yamaguchi, M. D. Thom, P. Ferreras, T. R. Windham & D. W. Macdonald, 2009. The impact of native competitors on an alien invasive: Temporal niche shifts to avoid interspecific aggression? Ecology 90: 1207–1216.

    Article  PubMed  Google Scholar 

  • Hechinger, R. F., K. D. Lafferty, T. C. Huspeni, A. J. Brooks & A. M. Kuris, 2007. Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151: 82–92.

    Article  PubMed  Google Scholar 

  • Henricson, J., 1977. The abundance and distribution of Diphyllobothrium dendriticum (Nitzsch) and D. ditremum (Creplin) in the char Salvelinus alpinus (L.) in Sweden. Journal of Fish Biology 11: 231–248.

    Article  Google Scholar 

  • 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 

  • Klemetsen, A., P.-A. Amundsen, P. E. Grotnes, R. Knudsen, R. Kristoffersen & M.-A. Svenning, 2002. 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.

    Article  Google Scholar 

  • Klemetsen, A., P.-A. Amundsen, J. B. Dempson, B. Jonsson, N. Jonsson, M. F. O’Connel & 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Knudsen, R. & A. Klemetsen, 1994. Infections of Diphyllobothrium dendriticum, 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Knudsen, R., M. A. Curtis & R. Kristoffersen, 2004. Aggregation of helminths: the role of feeding behavior of fish hosts. Journal of Parasitology 90: 1–7.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Knudsen, R., A. Siwertsson, C. E. Adams, J. Newton & P.-A. Amundsen, 2014. Similar patterns of individual niche use are revealed by different time-integrated trophic tracers (stable isotopes and parasites). Ecology of Freshwater Fish 23: 259–268.

    Article  Google Scholar 

  • Kristoffersen, R., 1993. Parasites in northern salmonids: effects of overpopulation and perturbations in systems with arctic charr (Salvelinus alpinus (L.)) and whitefish (Coregonus lavaretus L. sl) in northern Norway. PhD Thesis. University of Tromsø.

  • Kuhn, J. A., R. Kristoffersen, R. Knudsen, R. Primicerio, & P.-A. Amundsen, 2015. Parasite communities of two three-spined stickleback populations in subarctic Norway—effects of a small spatial-scale host introduction. Parasitology Research 114: 1327–1339.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • L’Abée-Lund, J. H., A. Langeland, B. L. Jonsson, B. Jonsson & O. Ugedal, 1993. Spatial segregation by age and size in Arctic charr: a trade-off between feeding possibility and risk of predation. Journal of Animal Ecology 62: 160–168.

    Article  Google Scholar 

  • L’Abée-Lund, J. H., P. Aass & H. Sægrov, 2002. Long-term variation in piscivory in a brown trout population: effect of changes in available prey organisms. Ecology of Freshwater Fish 11: 260–269.

    Article  Google Scholar 

  • Langeland, A., J. H. L’Abée-Lund, 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.

    Article  Google Scholar 

  • Lester, R. J. G., 2012. Overdispersion in marine fish parasites. Journal of Parasitology 98: 718–721.

    Article  CAS  PubMed  Google Scholar 

  • Locke, S. A., D. J. Marcogliese & E. T. Valtonen, 2014. Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia 174: 253–262.

    Article  PubMed  Google Scholar 

  • Marcogliese, D. J., 2002. Food webs and the transmission of parasites to marine fish. Parasitology 124: S83–S99.

    Article  PubMed  Google Scholar 

  • Münster, J., S. Klimpel, H. O. Fock, K. MacKenzie, & T. Kuhn, 2015. Parasites as biological tags to track an ontogenetic shift in the feeding behaviour of Gadus morhua off West and East Greenland. Parasitology Research 114: 2723–2733.

    Article  PubMed  Google Scholar 

  • Neuhäuser, M. & R. Poulin, 2004. Comparing parasite numbers between samples of hosts. Journal of Parasitology 90: 689–691.

    Article  PubMed  Google Scholar 

  • Nilsson, N.-A., 1963. Interaction between trout and char in Scandinavia. Transactions of the American Fisheries Society 92: 276–285.

    Article  Google Scholar 

  • Pacala, S. & A. Dobson, 1988. The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96: 197–210.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Persson, L., P.-A. Amundsen, A. De Roos, R. Knudsen, R. Primicerio & A. Klemetsen, 2013. Density-dependent interactions in an Arctic char—brown trout system: competition, predation, or both? Canadian Journal of Fisheries and Aquatic Sciences 70: 610–616.

    Article  Google Scholar 

  • Poulin, R., 2000. Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56: 123–137.

    Article  Google Scholar 

  • Poulin, R. & E. T. Valtonen, 2001. Interspecific associations among larval helminths in fish. International Journal for Parasitology 31: 1589–1596.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team, 2014. R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. URL http://www.R-project.org/.

  • Sánchez-Hernández, J. & P.-A. Amundsen, 2015. Trophic ecology of brown trout (Salmo trutta L.) in subarctic lakes. Ecology of Freshwater Fish 24: 148–161.

    Article  Google Scholar 

  • Sharp, G. J. E., A. W. Pike & C. J. Secombes, 1992. Sequential development of the immune response in rainbow trout [Oncorhynchus mykiss (Walbaum, 1792)] to experimental plerocercoid infections of Diphyllobothrium dendriticum (Nitzsch, 1824). Parasitology 104: 169–178.

    Article  PubMed  Google Scholar 

  • Shaw, D. J. & A. P. Dobson, 1995. Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111: S111–S127.

    Article  PubMed  Google Scholar 

  • Strona, G. & K. D. Lafferty, 2013. Predicting what helminth parasites a fish species should have using parasite co-occurrence modeler (PaCo). Journal of Parasitology 99: 6–10.

    Article  PubMed  Google Scholar 

  • Stutz, W. E., O. L. Lau & D. I. Bolnick, 2014. Contrasting patterns of phenotype-dependent parasitism within and among populations of three spine stickleback. The American Naturalist 183: 810–825.

    Article  PubMed  Google Scholar 

  • Timi, J. T., M. A. Rossin, A. J. Alarcos, P. E. Braicovich, D. M. P. Cantatore & A. L. Lanfranchi, 2011. Fish trophic level and the similarity of non-specific larval parasite assemblages. International Journal for Parasitology 41: 309–316.

    Article  CAS  PubMed  Google Scholar 

  • Valtonen, E. T., D. J. Marcogliese & M. Julkunen, 2010. Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162: 139–152.

    Article  CAS  PubMed  Google Scholar 

  • Vik, R., 1964. The genus Diphyllobothrium: An example of the interdependence of systematics and experimental biology. Experimental Parasitology 15: 361–380.

    Article  CAS  PubMed  Google Scholar 

  • Williams, H. H., K. MacKenzie & A. M. McCarthy, 1992. Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries 176: 144–176.

    Article  Google Scholar 

  • Woolhouse, M. E. J., 1998. Patterns in parasite epidemiology: the peak shift. Parasitology Today 14: 428–434.

    Article  CAS  PubMed  Google Scholar 

  • Zelmer, D. A. & H. P. Arai, 1998. The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. Journal of Parasitology 84: 24–28.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks are due to the technical staff and students of the Freshwater Ecology Group at UiT The Arctic University of Norway, for invaluable help during the field work over the years. We thank the guest editor, two anonymous referees and Dana Morton for their constructive comments. Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. government. Financial support was provided by UiT The Arctic University of Norway and the Norwegian Research Council (NFR 213610/F20).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eirik H. Henriksen.

Additional information

Guest editors: M. Power, R. Knudsen, C. Adams, M. J. Hansen, J. B. Dempson, M. Jobling & M. Ferguson / Advances in Charr Ecology and Evolution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Henriksen, E.H., Knudsen, R., Kristoffersen, R. et al. Ontogenetic dynamics of infection with Diphyllobothrium spp. cestodes in sympatric Arctic charr Salvelinus alpinus (L.) and brown trout Salmo trutta L.. Hydrobiologia 783, 37–46 (2016). https://doi.org/10.1007/s10750-015-2589-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2589-2

Keywords

Navigation