Published August 31, 2020 | Version v1
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Impacts of ontogenetic dietary shifts on the food-transmitted intestinal parasite communities of two lake salmonids

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Prati, Sebastian, Henriksen, Eirik Haugstvedt, Knudsen, Rune, Amundsen, Per-Arne (2020): Impacts of ontogenetic dietary shifts on the food-transmitted intestinal parasite communities of two lake salmonids. International Journal for Parasitology: Parasites and Wildlife 12: 155-164, DOI: 10.1016/j.ijppaw.2020.06.002, URL: http://dx.doi.org/10.1016/j.ijppaw.2020.06.002

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References

  • Amundsen, P.-A., Sanchez-Hernandez, J., 2019. Feeding studies take guts - critical review and recommendations of methods for stomach contents analysis in fish. J. Fish. Biol. 95, 1364-1373. https://doi.org/10.1111/jfb.14151.
  • Espinola-Novelo, J.F., Gonzalez, M.T., Pacheco, A.S., Luque, J.L., Oliva, M.E., 2020. Testing for deterministic succession in metazoan parasite communities of marine fish. Ecol. Lett. 23, 631-641. https://doi.org/10.1111/ele.13463.
  • Sanchez-Hernandez, J., Eloranta, A.P., Finstad, A.G., Amundsen, P.-A., 2017. Community structure affects trophic ontogeny in a predatory fish. Ecol. Evol. 7, 358-367. https:// doi.org/10.1002/ece3.2600.
  • Amundsen, P.-A., 1995. Feeding strategy of Arctic charr (Salvelinus alpinus): general opportunist, but individual specialist. Nord. J. Freshw. Res. 71, 150-156.
  • Amundsen, P.-A., Knudsen, R., 2009. Winter ecology of Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) in a subarctic lake, Norway. Aquat. Ecol. 43, 765-775. https://doi.org/10.1007/s10452-009-9261-8.
  • Amundsen, P.-A., Knudsen, R., Kuris, A.M., Kristoffersen, R., 2003. Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102, 285-293. https:// doi.org/10.1034/j.1600-0706.2003.12182.x.
  • Amundsen, P.-A., Knudsen, R., Klemetsen, A., 2007. Intraspecific competition and density dependence of food consumption and growth in Arctic charr. J. Anim. Ecol. 76, 149-158. https://doi.org/10.1111/j.1365-2656.2006.01179.x.
  • Amundsen, P.-A., Lafferty, K.D., Knudsen, R., Primicerio, R., Klemetsen, A., Kuris, A.M., 2009. Food web topology and parasites in the pelagic zone of a subarctic lake. J. Anim. Ecol. 78, 563-572. https://doi.org/10.1111/j.1365-2656.2008.01518.x.
  • Amundsen, P.-A., Lafferty, K.D., Knudsen, R., Primicerio, R., Kristoffersen, R., Klemetsen, A., Kuris, A.M., 2013. New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning. Oecologia 171, 993-1002. https://doi.org/10.1007/s00442-012-2461-2.
  • Amundsen, P.-A., Primicerio, R., Smalas, A., Henriksen, E.H., Knudsen, R., Kristoffersen, R., Klemetsen, A., 2019. Long-term ecological studies in northern lakes-challenges, experiences, and accomplishments. Limnol. Oceanogr. 64, S11-S21. https://doi.org/ 10.1002/lno.10951.
  • Anastasopoulou, A., Mytilineou, C., Lefkaditou, E., Kavadas, S., Bekas, P., Smith, C.J., Papadopoulou, K.N., Christides, G., 2013. The diet and feeding ecology of Conger conger (L. 1758) in the deep waters of the Eastern Ionian Sea. Mediterr. Mar. Sci. 14, 365-368. https://doi.org/10.12681/mms.479.
  • Anderson, M.J., Ellingsen, K.E., McArdle, B.H., 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683-693. https://doi.org/10.1111/j.1461-0248. 2006.00926.x.
  • Anderson, M.J., Crist, T.O., Chase, J.M., Vellend, M., Inouye, B.D., Freestone, A.L., Sanders, N.J., Cornell, H.V., Comita, L.S., Davies, K.F., Harrison, S.P., Kraft, N.J.B., Stegen, J.C., Swenson, N.G., 2011. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19-28. https://doi.org/10.1111/ j.1461-0248.2010.01552.x.
  • Bjornsson, B., 2001. The trophic ecology of arctic char (Salvelinus alpinus) and brown trout (Salmo trutta) in Ellidavatn, a small lake in Southwest Iceland. Limnologica 31, 199-207. https://doi.org/10.1016/S0075-9511(01)80021-9.
  • Brickle, P., MacKenzie, K., Pike, A., 2006. Variations in the parasite fauna of the Patagonian toothfish (Dissostichus eleginoides, Smitt, 1898), with length, season, and depth of habitat around the Falkland Islands. J. Parasitol. 92, 282-291. https://doi. org/10.1645/GE-539R.1.
  • Bush, A.O., Heard Jr., R.W., Overstreet, R.M., 1993. Intermediate hosts as source communities. Can. J. Zool. 71, 1358-1363. https://doi.org/10.1139/z93-186.
  • Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., 1997. Parasitology meets ecology on its own terms: margolis et al. revisited. J. Parasitol. 83, 575. https://doi.org/10. 2307/3284227.
  • Canedo-Arguelles, M., Sgarzi, S., Arranz, I., Quintana, X.D., Ersoy, Z., Landkildehus, F., Lauridsen, T.L., Jeppesen, E., Brucet, S., 2017. Role of predation in biological communities in naturally eutrophic sub-Arctic Lake Myvatn, Iceland. Hydrobiologia 790, 213-223. https://doi.org/10.1007/s10750-016-3031-0.
  • Chen, H.-W., Liu, W.-C., Davis, A.J., Jordan, F., Hwang, M.-J., Shao, K.-T., 2008. Network position of hosts in food webs and their parasite diversity. Oikos 117, 1847-1855. https://doi.org/10.1111/j.1600-0706.2008.16607.x.
  • Choi, J.-H., Choi, S.-H., Kim, J.-B., Park, J.-H., Oh, C.-W., 2008. Feeding ecology of the white-spotted conger eel (Conger myriaster) in the southern sea of Korea. Korean J. Fish. Aquat. Sci. 41, 282-288. https://doi.org/10.5657/kfas.2008.41.4.282.
  • Curtis, M.A., Berube, M., Stenzel, A., 1995. Parasitological evidence for specialized foraging behavior in lake-resident Arctic char (Salvelinus alpinus). Can. J. Fish. Aquat. Sci. 52, 186-194. https://doi.org/10.1139/f95-526.
  • Dick, T., Chambers, C., Gallagher, C.P., 2009. Parasites, diet and stable isotopes of shorthorn sculpin (Myoxocephalus scorpius) from Frobisher bay, Canada. Parasite 16, 297-304. https://doi.org/10.1051/parasite/2009164297.
  • Eloranta, A.P., Knudsen, R., Amundsen, P.-A., 2013. Niche segregation of coexisting Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) constrains food web coupling in subarctic lakes. Freshw. Biol. 58, 207-221. https://doi.org/10.1111/fwb. 12052.
  • Forseth, T., Ugedal, O., Jonsson, B., 1994. The energy budget, niche shift, reproduction and growth in a population of Arctic charr, Salvelinus alpinus. J. Anim. Ecol. 63, 116-126. https://doi.org/10.2307/5588.
  • Gower, J.C., 1966. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53, 325-338. https://doi.org/10.1093/biomet/53. 3-4.325.
  • 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 Mag. Zool. (Oslo) 18, 113-174.
  • Hanzelova, V., Scholz, T., Gerdeaux, D., Kuchta, R., 2002. A comparative study of Eubothrium salvelini and E. crassum (Cestoda: Pseudophyllidea) parasites of Arctic charr and brown trout in alpine lakes. In: Magnan, P., Audet, C., Glemet, H., Legault, M., Rodriguez, M.A., Taylor, E.B. (Eds.), Ecology, Behaviour and Conservation of the Charrs, Genus Salvelinus. Springer Netherlands, Dordrecht, pp. 245-256.
  • Henriksen, E.H., Knudsen, R., Kristoffersen, R., Kuris, A.M., Lafferty, K.D., Siwertsson, A., Amundsen, P.-A., 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. https://doi.org/10.1007/s10750-015-2589-2.
  • Hernandez, A.D., Muzzall, P.M., 1998. Seasonal patterns in the biology of Eubothrium salvelini infecting brook trout in a creek in lower Michigan. J. Parasitol. 84, 1119-1123. https://doi.org/10.2307/3284659.
  • Holmes, J.C., 1990. Helminth communities in marine fishes. In: Esch, G.W., Bush, A.O., Aho (Eds.), Parasite Communities: Patterns and Processes. Springer Netherlands, Dordrecht, pp. 101-130.
  • Hughes, M.R., Hooker, O.E., Van Leeuwen, T.E., Kettle-White, A., Thorne, A., Prodohl, P., Adams, C.E., 2019. Alternative routes to piscivory: contrasting growth trajectories in brown trout (Salmo trutta) ecotypes exhibiting contrasting life history strategies. Ecol. Freshw. Fish 28, 4-10. https://doi.org/10.1111/eff.12421.
  • Jensen, H., Kahilainen, K.K., Amundsen, P.-A., Gjelland, K.O., Tuomaala, A., Malinen, T., Bohn, T., 2008. Predation by brown trout (Salmo trutta) along a diversifying prey community gradient. Can. J. Fish. Aquat. Sci. 65, 1831-1841. https://doi.org/10. 1139/F08-096.
  • Jensen, H., Kiljunen, M., Amundsen, P.-A., 2012. Dietary ontogeny and niche shift to piscivory in lacustrine brown trout Salmo trutta revealed by stomach content and stable isotope analyses. J. Fish. Biol. 80, 2448-2462. https://doi.org/10.1111/j. 1095-8649.2012.03294.x.
  • Johnson, R.L., Blumenshine, S.C., Coghlan, S.M., 2006. A bioenergetic analysis of factors limiting brown trout growth in an Ozark tailwater river. Environ. Biol. Fish. 77, 121-132. https://doi.org/10.1007/s10641-006-9059-7.
  • Kahilainen, K., Lehtonen, H., 2003. Piscivory and prey selection of four predator species in a whitefish dominated subarctic lake. J. Fish. Biol. 63, 659-672. https://doi.org/ 10.1046/j.1095-8649.2003.00179.x.
  • Kennedy, C.R., Bush, A.O., Aho, J.M., 1986. Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205-215. https://doi.org/10.1017/ S0031182000049945.
  • Klemetsen, A., Amundsen, P.-A., Muladal, H., Rubach, S., Solbakken, J.I., 1989. Habitat shifts in a dense, resident Arctic charr Salvelinus alpinus population. Physiol. Ecol. Japan, Spec. 1, 187-200.
  • Klemetsen, A., Amundsen, P.-A., Grotnes, P.E., Knudsen, R., Kristoffersen, R., Svenning, M.-A., 2002. Takvatn through 20 years: long-term effects of an experimental mass removal of Arctic charr, Salvelinus alpinus, from a subarctic lake. In: Magnan, P., Audet, C., Glemet, H., Legault, M., Rodriguez, M.A., Taylor, E.B. (Eds.), Ecology, Behaviour and Conservation of the Charrs, Genus Salvelinus, Developments in Environmental Biology of Fishes. Springer Netherlands, Dordrecht, pp. 39-47. https://doi.org/10.1007/978-94-017-1352-8_3.
  • Klemetsen, A., Amundsen, P.-A., Dempson, J.B., Jonsson, B., Jonsson, N., O'Connell, M.F., Mortensen, E., 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. Ecol. Freshw. Fish 12, 1-59. https://doi.org/10.1034/j.1600-0633.2003.00010.x.
  • Knudsen, R., Curtis, M.A., Kristoffersen, R., 2004. Aggregation of helminths: the role of feeding behavior of fish hosts. J. Parasitol. 90, 1-7. https://doi.org/10.1645/GE-3184.
  • Knudsen, R., Amundsen, P.-A., Nilsen, R., Kristoffersen, R., Klemetsen, A., 2008. Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout. Environ. Biol. Fish. 83, 107-116. https://doi.org/10.1007/s10641-007- 9216-7.
  • Knudsen, R., Primicerio, R., Amundsen, P.-A., Klemetsen, A., 2010. Temporal stability of individual feeding specialization may promote speciation. J. Anim. Ecol. 79, 161-168. https://doi.org/10.1111/j.1365-2656.2009.01625.x.
  • Kristmundsson, A., Richter, S.H., 2009. Parasites of resident Arctic charr, Salvelinus alpinus, and brown trout, Salmo trutta, in two lakes in Iceland. Icel. Agric. Sci. 14.
  • Kuhn, J.A., Frainer, A., Knudsen, R., Kristoffersen, R., Amundsen, P.-A., 2016a. Effects of fish species composition on Diphyllobothrium spp. infections in brown trout - is three-spined stickleback a key species? J. Fish. Dis. 39, 1313-1323. https://doi.org/10. 1111/jfd.12467.
  • Kuhn, J.A., Knudsen, R., Kristoffersen, R., Primicerio, R., Amundsen, P.-A., 2016b. Temporal changes and between-host variation in the intestinal parasite community of Arctic charr in a subarctic lake. Hydrobiologia 783, 79-91. https://doi.org/10.1007/ s10750-016-2731-9.
  • Kuris, A.M., Blaustein, A.R., Alio, J.J., 1980. Hosts as islands. Am. Nat. 116, 570-586. https://doi.org/10.1086/283647.
  • Legendre, P., Legendre, L.F., 2012. Numerical Ecology. In: Developments in Environmental Modelling, third ed. Elsevier, Amsterdam.
  • Locke, S.A., Marcogliese, D.J., Valtonen, T.E., 2014. Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia 174, 253-262. https://doi.org/10.1007/s00442-013-2757-x.
  • Marcogliese, D.J., 2002. Food webs and the transmission of parasites to marine fish. Parasitology 124, 83-99. https://doi.org/10.1017/S003118200200149X.
  • Munoz, G., Zamora, L., 2011. Ontogenetic variation in parasite infracommunities of the clingfish Sicyases sanguineus (Pisces: Gobiesocidae). J. Parasitol. 97, 14-19. https:// doi.org/10.1645/GE-2445.1.
  • Munster, J., Klimpel, S., Fock, H.O., MacKenzie, K., Kuhn, T., 2015. Parasites as biological tags to track an ontogenetic shift in the feeding behaviour of Gadus morhua off West and East Greenland. Parasitol. Res. 114, 2723-2733. https://doi.org/10.1007/ s00436-015-4479-y.
  • Nilsson, P.A., Bronmark, C., 2000. Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88, 539-546. https://doi.org/10.1034/j.1600-0706.2000.880310.x.
  • Okaka, C.E., 1984. Studies on the Biology of Cyathocephalus truncatus (Pallas, 1781) (Cestoda : Spathebothridea) in its Fish and Crustacean Hosts. Doctoral dissertation, University of Leeds.
  • Oksanen, J., Blanchet, G.F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, H.M.H., Szoecs, E., Wagner, H., 2019. Vegan: community ecology package. R package.
  • Pegg, J., Andreou, D., Williams, C.F., Britton, J.R., 2015. Head morphology and piscivory of European eels, Anguilla anguilla, predict their probability of infection by the invasive parasitic nematode Anguillicoloides crassus. Freshw. Biol. 60https://doi.org/10. 1111/fwb.12624. 1977-1987.
  • Perez-Del Olmo, A., Fernandez, M., Raga, J.A., Kostadinova, A., Poulin, R., 2008. Halfway up the trophic chain: development of parasite communities in the sparid fish Boops boops. Parasitology 135, 257-268. https://doi.org/10.1017/S0031182007003691.
  • Poulin, R., 2000. Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. J. Fish. Biol. 56, 123-137. https://doi.org/10.1111/j.1095-8649.2000.tb02090.x.
  • Poulin, R., Leung, T.L.F., 2011. Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166, 731-738. https://doi.org/10.1007/s00442-011- 1906-3.
  • Poulin, R., Valtonen, E.T., 2001. Interspecific associations among larval helminths in fish. Int. J. Parasitol. 31, 1589-1596. https://doi.org/10.1016/S0020-7519(01)00276-4.
  • Prati, S., Henriksen, E.H., Knudsen, R., Amundsen, P.-A., 2020. Seasonal dietary shifts enhance parasite transmission to lake salmonids during ice cover. Ecol. Evol. 10, 4031-4043. https://doi.org/10.1002/ece3.6173.
  • Reiczigel, J., 2003. Confidence intervals for the binomial parameter: some new considerations. Stat. Med. 22, 611-621. https://doi.org/10.1002/sim.1320.
  • Reiczigel, J., Marozzi, M., Fabian, I., Rozsa, L., 2019. Biostatistics for parasitologists - a primer to quantitative parasitology. Trends Parasitol. 35, 277-281. https://doi.org/ 10.1016/j.pt.2019.01.003.
  • Rozsa, L., Reiczigel, J., Majoros, G., 2000. Quantifying parasites in samples of hosts. J. Parasitol. 86, 228-232.
  • Sanchez-Hernandez, J., Servia, M.J., Vieira-Lanero, R., Cobo, F., 2012. Ontogenetic dietary shifts in a predatory freshwater fish species: the brown trout as an example of a dynamic fish species. In: Turker, H. (Ed.), New Advances and Contributions to Fish Biology. IntechOpen. https://doi.org/10.5772/54133.
  • Sanchez-Hernandez, J., Nunn, A.D., Adams, C.E., Amundsen, P.-A., 2019. Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models: ontogenetic dietary shifts. Biol. Rev. 94, 539-554. https://doi.org/10.1111/brv. 12468.
  • Scholz, T., 1999. Life cycles of species of Proteocephalus, parasites of fishes in the Palearctic Region: a review. J. Helminthol. 73, 1-19. https://doi.org/10.1017/ S0022149X99000013.
  • Soldanova, M., Georgieva, S., Rohacova, J., Knudsen, R., Kuhn, J.A., Henriksen, E.H., Siwertsson, A., Shaw, J.C., Kuris, A.M., Amundsen, P.-A., Scholz, T., Lafferty, K.D., Kostadinova, A., 2017. Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. Int. J. Parasitol. 47, 327-345. https://doi.org/10.1016/j.ijpara. 2016.12.008.
  • Tanzola, R.D., Guagliardo, S.E., 2000. Helminth fauna of the Argentine conger, Conger orbignyanus (Pisces: Anguilliformes). Helminthologia 37, 229-232.
  • Thomas, J.D., 1958. Studies on Crepidostomum metoecus (Braun) and C. farionis (muller), parasitic in Salmo trutta L. And S. salar L. In Britain. Parasitology 48, 336-352. https://doi.org/10.1017/S0031182000021296.
  • Thomas, S.M., Kiljunen, M., Malinen, T., Eloranta, A.P., Amundsen, P.-A., Lodenius, M., Kahilainen, K.K., 2016. Food-web structure and mercury dynamics in a large subarctic lake following multiple species introductions. Freshw. Biol. 61, 500-517. https://doi.org/10.1111/fwb.12723.
  • Timi, J.T., Lanfranchi, A.L., 2013. Ontogenetic changes in heterogeneity of parasite communities of fish: disentangling the relative role of compositional versus abundance variability. Parasitology 140, 309-317. https://doi.org/10.1017/ S0031182012001606.
  • Timi, J.T., Luque, J.L., Poulin, R., 2010. Host ontogeny and the temporal decay of similarity in parasite communities of marine fish. Int. J. Parasitol. 40, 963-968. https://doi.org/10.1016/j.ijpara.2010.02.005.
  • Timi, J.T., Rossin, M.A., Alarcos, A.J., Braicovich, P.E., Cantatore, D.M.P., Lanfranchi, A.L., 2011. Fish trophic level and the similarity of non-specific larval parasite assemblages. Int. J. Parasitol. 41, 309-316. https://doi.org/10.1016/j.ijpara.2010.10. 002.
  • Truemper, H.A., Lauer, T.E., 2005. Gape limitation and piscine prey size-selection by yellow perch in the extreme southern area of Lake Michigan, with emphasis on two exotic prey items. J. Fish. Biol. 66, 135-149. https://doi.org/10.1111/j.0022-1112. 2005.00588.x.
  • Valtonen, E.T., Marcogliese, D.J., Julkunen, M., 2010. Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162, 139-152. https://doi.org/10.1007/s00442-009-1451-5.
  • Vik, R., 1964. The genus Diphyllobothrium: an example of the interdependence of systematics and experimental biology. Exp. Parasitol. 15, 361-380. https://doi.org/10. 1016/0014-4894(64)90031-1.
  • Waeschenbach, A., Brabec, J., Scholz, T., Littlewood, D.T.J., Kuchta, R., 2017. The catholic taste of broad tapeworms - multiple routes to human infection. Int. J. Parasitol. 47, 831-843. https://doi.org/10.1016/j.ijpara.2017.06.004.
  • Werner, E.E., Gilliam, J.F., 1984. The ontogenetic niche and species interactions in sizestructured populations. Annu. Rev. Ecol. Systemat. 15, 393-425. https://doi.org/10. 1146/annurev.es.15.110184.002141.
  • Woodward, G., Warren, P.H., 2007. Body size and predatory interactions in freshwaters: scaling from individuals to communities. In: Hildrew, A., Raffelli, D., Edmonds- Brown, R. (Eds.), Body Size: the Structure and Function of Aquatic Ecosystems. Cambridge University Press, Cambridge, pp. 98-117. https://doi.org/10.1017/ CBO9780511611223.007.