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The association between parasite infection and growth rates in Arctic charr: do fast growing fish have more parasites?

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Abstract

Trophically transmitted parasites are known to impair fish growth in experimental studies, but this is not well documented in natural populations. For Arctic charr [Salvelinus alpinus (L.)], individual growth is positively correlated with food consumption. However, increased food consumption will increase the exposure to trophically transmitted parasites. Using a correlative approach, we explore the association between parasite abundance and the individual growth of Arctic charr from five lakes within the same watercourse. The studied parasite species differ in their life cycles and cost to the host. We predicted a positive association between parasite abundance and fish growth for parasites of low pathogenicity reflecting high consumption rates, and a negative association at higher parasite abundances for more costly parasites. We found no direct negative associations between parasite abundance and fish growth. The relationship between parasite abundance and growth was linearly positive for the low costly Crepidostomum sp. and concave for the more costly Eubothrium salvelini. In natural fish populations, the negative effects of parasites on fish growth might be outweighed by the energy assimilated from feeding on the intermediate host. However, experimental studies with varying food consumption regimes are needed to determine the mechanisms underlying our observations.

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References

  • Alvarez-Pellitero, P., 2008. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Veterinary Immunology and Immunopathology 126: 171–198.

    Article  CAS  PubMed  Google Scholar 

  • Amundsen, P. A., H. M. Gabler & F. J. Staldvik, 1996. A new approach to graphical analysis of feeding strategy from stomach contents data—modification of the Costello (1990) method. Journal of Fish Biology 48: 607–614.

    Google Scholar 

  • Amundsen, P.-A., R. Knudsen, A. M. Kuris & R. Kristoffersen, 2003. Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 2: 285–293.

    Article  Google Scholar 

  • Amundsen, P.-A., R. Knudsen & A. Klemetsen, 2007. Intraspecific competition and density dependence of food consumption and growth in Arctic charr. The Journal of Animal Ecology 76: 149–158.

    Article  PubMed  Google Scholar 

  • Awachie, J. B., 1968. On the bionomics of Crepidostomum metoecus (Braun, 1900) and Crepidostomum farionis (Müller, 1784) (Trematoda: Allocreadiidae). Parasitology 58: 307–324.

    Article  Google Scholar 

  • Barber, I., S. A. Arnott, V. A. Braithwaite, J. Andrew & F. A. Huntingford, 2001. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proceedings of the Royal Society B 268: 71–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber, I., H. A. Wright, S. A. Arnott & R. J. Wootton, 2008. Growth and energetics in the stickleback-Schistocephalus host parasite system: a review of experimental infection studies. Behaviour 145: 4–5.

    Google Scholar 

  • Bell, G. & A. Burt, 1991. The comparative biology of parasite species diversity: internal helminths of freshwater fish. The Journal of Animal Ecology 60: 1047–1064.

    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 

  • Boyce, N. P. J., 1974. Biology of Eubothrium salvelini (Cestoda: Pseudophyllidea), a parasite of juvenile sockeye salmon (Oncorhynchus nerka) of Babine Lake, British Columbia. Journal of the Fisheries Board of Canada 31: 1735–1742.

    Article  Google Scholar 

  • Boyce, N. P., 1979. Effects of Eubothrium salvelini (Cestoda: Pseudophyllidea) on the growth and vitality of sockeye salmon, Oncorhynchus nerka. Canadian Journal of Zoology 57: 597–602.

    Article  Google Scholar 

  • Bristow, G. A. & B. Berland, 1991. The effect of long-term, low-level Eubothrium sp. (Cestoda, Pseudophyllidea) infection in farmed salmon (Salmo salar L.). Aquaculture 98: 325–330.

    Article  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz, A. W. Shostak, et al., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The 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, Helsinki: 58.

    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: 395–411.

    Google Scholar 

  • des Clers, S., 1991. Functional relationship between sealworm (Pseudoterranova decipiens, Nematoda, Ascaridoidea) burden and host size in Atlantic cod (Gadus morhua). Proceedings of the Royal Society B 245: 85–89.

    Article  PubMed  Google Scholar 

  • Dezfuli, B. S., G. Bosi, J. A. DePasquale, M. Manera & L. Giari, 2016. Fish innate immunity against intestinal helminths. Fish and Shellfish Immunology 50: 274–287.

    Article  CAS  PubMed  Google Scholar 

  • Dobson, A., K. D. Lafferty, A. M. Kuris, R. F. Hechinger & W. Jetz, 2008. Colloquium paper: homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105(Suppl): 11482–11489.

    Article  CAS  PubMed  PubMed Central  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 

  • Gerdeaux, D., M. A. Fillon & L. Van Overmeire, 1995. Arctic charr, Salvelinus alpinus, of Lake Annecy: yield, growth and parasitism by Eubothrium salvelini. Nordic Journal of Freshwater Research 71: 245–251.

    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 

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

    Article  Google Scholar 

  • Henricson, J., 1978. The dynamics of infection of Diphyllobothrium dendriticum (Nitzsch) and D. ditremum (Creplin) in the char Salvelinus alpinus (L.) in Sweden. Journal of Fish Biology 13: 51–71.

    Article  Google Scholar 

  • 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 783: 37–46.

    Article  CAS  Google Scholar 

  • Hernandez, A. D. & P. M. Muzzall, 1998. Seasonal patterns in the biology of Eubothrium salvelini infecting brook trout in a creek in lower Michigan. Journal of Parasitology 84: 1119–1123.

    Article  CAS  PubMed  Google Scholar 

  • Höglund, J. & A. Thuvander, 1990. Indications of non-specific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8: 91–97.

    Article  Google Scholar 

  • Hooker, O. E., T. E. Van Leeuwen & C. E. Adams, 2017. The physiological costs of prey switching reinforce foraging specialization. Journal of Animal Ecology 86: 605–614.

    Article  PubMed  Google Scholar 

  • Ingham, L. & C. Arme, 1973. Intestinal helminths in rainbow trout, Salmo gairdneri (Richardson): absence of effect on nutrient absorption and fish growth. Journal of Fish Biology 5: 309–313.

    Article  Google Scholar 

  • Johnsen, B. O. & A. J. Jensen, 1991. The Gyrodactylus story in Norway. Aquaculture 98: 289–302.

    Article  Google Scholar 

  • Joy, J. E. & E. Madan, 1989. Pathology of black bass hepatic tissue infected with larvae of the tapeworm Proteocephalus ambloplitis. Journal of Fish Biology 35: 111–118.

    Article  Google Scholar 

  • Klemetsen, A., 2013. The most variable vertebrate on Earth. Journal of Ichthyology 53: 781–791.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  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., P.-A. Amundsen & A. Klemetsen, 2010. Arctic charr in sympatry with burbot: ecological and evolutionary consequences. Hydrobiologia 650: 43–54.

    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 

  • Krkosek, M., C. W. Revie, P. G. Gargan, O. T. Skilbrei, B. Finstad & C. D. Todd, 2013. Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean. Proceedings of the Royal Society B 280: 1–8.

    Article  Google Scholar 

  • Kuhn, J. A., R. Knudsen, R. Kristoffersen, R. Primicerio & P. A. Amundsen, 2016. Temporal changes and between-host variation in the intestinal parasite community of Arctic charr in a subarctic lake. Hydrobiologia 783: 79–91.

    Article  Google Scholar 

  • Kuhn, J. A., R. Knudsen, R. Kristoffersen & P.-A. Amundsen, 2017. A simplified method to estimate Diphyllobothrium spp. infection in salmonids. Journal of Fish Diseases 40: 863–871.

    Article  CAS  PubMed  Google Scholar 

  • Lafferty, K. D., 1992. Foraging on prey that are modified by parasites. The American Naturalist 140: 854.

    Article  Google Scholar 

  • Larsson, S. & I. Berglund, 2005. The effect of temperature on the energetic growth efficiency of Arctic charr (Salvelinus alpinus L.) from four Swedish populations. Journal of Thermal Biology 30: 29–36.

    Article  Google Scholar 

  • Lochmiller, R. L. & C. Deerenberg, 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87–98.

    Article  Google Scholar 

  • Lysne, D. A., W. Hemmingsen & A. Skorping, 2006. Is reduced body growth of cod exposed to the gill parasite Lernaeocera branchialis a cost of resistance? Journal of Fish Biology 69: 1281–1287.

    Article  Google Scholar 

  • Nordling, D., M. Andersson, S. Zohari & G. Lars, 1998. Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society B 265: 1291–1298.

    Article  PubMed Central  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, H. Wagner, & M. J. Oksanen, 2013. Package ‘vegan.’ Community ecology package, version 2.9.

  • 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 

  • Pennycuick, L., 1971. Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Zoology 165: 143–162.

    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., 2013. Explaining variability in parasite aggregation levels among host samples. Parasitology 140: 541–546.

    Article  PubMed  Google Scholar 

  • Poulin, R. & S. Morand, 2000. The diversity of parasites. The Quarterly Review of Biology 75: 277–293.

    Article  CAS  PubMed  Google Scholar 

  • Poulin, R., M. A. Curtis & M. E. Rau, 1992. Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105: 265–271.

    Article  Google Scholar 

  • R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. http://www.R-project.org/

  • Saksvik, M., F. Nilsen, A. Nylund & B. Berland, 2001. Effect of marine Eubothrium sp. (Cestoda: Pseudophyllidea) on the growth of Atlantic salmon, Salmo salar L. Journal of Fish Diseases 24: 111–119.

    Article  Google Scholar 

  • Scholz, T., 1999. Life cycles of species of Proteocephalus, parasites of fishes in the Palearctic region: a review. Journal of Helminthology 73: 1–19.

    Article  CAS  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 

  • Sirois, P. & J. J. Dodson, 2000. Influence of turbidity, food density and parasites on the ingestion and growth of larval rainbow smelt Osmerus mordax in an estuarine turbidity maximum. Marine Ecology Progress Series 193: 167–179.

    Article  Google Scholar 

  • Skarstein, F., I. Folstad & S. Liljedal, 2001. Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Canadian Journal of Zoology 79: 271–278.

    Article  Google Scholar 

  • Soldánová, M., S. Georgieva, J. Roháčová, R. Knudsen, J. A. Kuhn, E. H. Henriksen, A. Siwertsson, J. C. Shaw, A. M. Kuris, P.-A. Amundsen, T. Scholz, K. D. Lafferty & A. Kostadinova, 2017. Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology 47: 327–345.

    Article  PubMed  CAS  Google Scholar 

  • Stables, J. N. & L. H. Chappell, 1986. Putative immune response of rainbow trout, Salmo gairdneri, to Diplostomum spathaceum infections. Journal of Fish Biology 29: 115–122.

    Article  Google Scholar 

  • Thomas, J. D., 1958. Studies on Crepidostomum metoecus (Braun) and C. farionis (Müller), parasitic in Salmo trutta L. and S. salar L. in Britain. Parasitology 48: 336–352.

    Article  CAS  PubMed  Google Scholar 

  • Van Der Most, P. J., B. De Jong, H. K. Parmentier & S. Verhulst, 2011. Trade-off between growth and immune function: a meta-analysis of selection experiments. Functional Ecology 25: 74–80.

    Article  Google Scholar 

  • Vik, R., 1957. Studies of the helminth fauna of Norway. I. Taxonomy and ecology of Diphyllobothrium norvegicum n. sp. and the plerocercoid of Diphyllobothrium latum (L.). Nytt Magasin for Zoologi 5: 26–93.

    Google Scholar 

  • Vik, R., 1958. Studies of the helminth fauna of Norway. II. Distribution and life cycle of Cyathocephalus truncatus (Pallas, 1781) (Cestoda). Nytt Magasin for Zoologi 6: 97–110.

    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 

  • Wootton, R. J., 1998. Ecology of teleost fishes. Kluwer, London.

    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. The Journal of Parasitology 84: 24–28.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the following people for field sampling and/or laboratory work: P. A. Amundsen, M. S. Berg, C. Bye, L. Dalsbø, A. P. Eloranta, K. Ø. Gjelland, M. Gabler, B. S. Knudsen, R. Kristoffersen, J. A. Kuhn, K. Johannessen, and K. J. O’Connor. Two anonymous reviewers provided helpful and constructive comments.

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Correspondence to Eirik H. Henriksen.

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Guest editors: C. E. Adams, C. R. Bronte, M. J. Hansen, R. Knudsen & M. Power / Charr Biology, Ecology and Management

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Henriksen, E.H., Smalås, A., Strøm, J.F. et al. The association between parasite infection and growth rates in Arctic charr: do fast growing fish have more parasites?. Hydrobiologia 840, 261–270 (2019). https://doi.org/10.1007/s10750-018-3865-8

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