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Long-term population dynamics of Littorina obtusata: the spatial structure and impact of trematodes

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Abstract

There are few examples of host population regulation by macroparasites in stable communities; however, strong impact of parasites on the host individual is obvious in many cases (for example increased mortality, a reduction in fecundity up to the complete castration). Associations between the host populations (periwinkle Littorina obtusata) and prevalence of trematodes was investigated using long-term data (1982–1997) of two L. obtusata populations in the White Sea, northwest Russia. We hypothesized that high prevalence of trematodes will reduce future host population density, and increase mortality. Using a general linear model, we found a significant negative correlation between host population density and the prevalence of the most abundant parasite, Microphallus piriformes in the previous year. We found no correlation between snail reproduction and the prevalence, but observed a significant reduction in middle-aged mollusk abundance which was associated with high prevalence. This indicates the importance of parasite-induced mortality for the dynamics of the host population. There was an association between trematode infection and L. obtusata populations that influence their distribution within littoral zone. The ‘source’ population, located in the lower section of the macrophyte zone, appears to be self-sustaining, controlling the whole population recruitment and dynamics.

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References

  • Albon, S. D., A. Stein, R. J. Irvine, R. Langvatn, E. Ropstad & O. Halvorsen, 2002. The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society B 269: 1625–1632.

    Article  PubMed  CAS  Google Scholar 

  • Berger, V. Ya., 1986. Adaptations of the Marine Mollusks to the Salinity of the Environment. Nauka, Leningrad. (in Russian).

    Google Scholar 

  • Berger, V. Ya., 2007. Production Potential of the White Sea. St. Petersburg Zoological Institute RAS, Saint-Petersburg. (in Russian).

    Google Scholar 

  • Bostanci, A., 2005. Wildlife biology. A devil of a disease. Science 307: 1035.

    Article  PubMed  CAS  Google Scholar 

  • Brown, K. M., B. K. Leathers & D. J. Minchella, 1988. Trematode prevalence and the population dynamic of freshwater pond snails. American Midland Naturalist 120: 289–300.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information—Theoretic Approach, 2nd ed. Springer, New York.

    Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2004. Multimodel inference understanding AIC and BIC in model selection. Sociological Methods & Research 33: 261–304.

    Article  Google Scholar 

  • Daszak, P., A. A. Cunningham & A. D. Hyatt, 2003. Infectious disease and amphibian population declines. Diversity and Distribution 9: 141–150.

    Article  Google Scholar 

  • Duffy, M. A., 2007. Selective predation, parasitism, and trophic cascades in a bluegill–Daphnia–parasite system. Oecologia 153: 453–460.

    Article  PubMed  Google Scholar 

  • Ebert, D., M. Lipsitch & K. L. Mangin, 2000. The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. American Naturalist 156: 459–477.

    Article  Google Scholar 

  • Finner, H. & K. Strassburger, 2002. The partitioning principle: a powerful tool in multiple decision theory. Annals of Statistics 30: 1194–1213.

    Article  Google Scholar 

  • Fredensborg, B. L., K. N. Mouritsen & R. Poulin, 2005. Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series 290: 109–117.

    Article  Google Scholar 

  • Galaktionov, K. V., 1993. The Life Cycles of Trematodes as the Components of Ecosystems. Kola Scientific Centre, Apatity. (in Russian).

    Google Scholar 

  • Ganzha, E. V. & A. I. Granovitch, 2008. Infection with trematode partenites leads to change in penial gland structure in males of littoral mollusks Littorina saxatilis (Olivi) и L. obtusata (L.). Parazitologiya 42: 13–22. (in Russian).

    CAS  Google Scholar 

  • Granovitch, A. I., N. A. Mikhailova & S. O. Sergievsky, 1987. Age-specific peculiarities of prevalence of Littorina obtusata and L. saxatilis populations by the Trematode parasites. Parazitologiya 21: 721–729. (in Russian).

    Google Scholar 

  • Granovitch, A. I., S. O. Sergievsky & I. M. Sokolova, 2000. Spatial and temporal variation of trematode infestation in coexisting populations of intertidal gastropods Littorina saxatilis and L.obtusata in the White Sea. Diseases of Aquatic Organisms 41: 53–64.

    Article  PubMed  CAS  Google Scholar 

  • Granovitch, A. I., E. V. Yagunova, A. N. Maximovich & I. M. Sokolova, 2009. Elevated female fecundity as a possible compensatory mechanism in response to trematode infestation in populations of Littorina saxatilis (Olivi). International Journal for Parasitology 39: 1011–1019.

    Article  PubMed  CAS  Google Scholar 

  • Grixti, J. C., L. T. Wong & S. A. Cameron, 2009. Decline of bumble bees (Bombus) in the North American Midwest. Biological Conservation 142: 75–84.

    Article  Google Scholar 

  • Hernandez, A. D. & M. V. K. Sukhdeo, 2008. Parasites alter the topology of a stream food web across seasons. Oecologia 156: 613–624.

    Article  PubMed  Google Scholar 

  • Hudson, P. J., A. P. Dobson & D. Newborn, 1998. Prevention of population cycles by parasite removal. Science 282: 2256–2258.

    Article  PubMed  CAS  Google Scholar 

  • Huxham, M., D. Raffaelli & A. Pike, 1993. The influence of Cryptocotyle lingua (Digenea: Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prosobranchia); an ecological approach. Journal of Experimental Marine Biology and Ecology 168: 223–238.

    Article  Google Scholar 

  • Jensen, K. H., M. van de Bildt & H. H. Dietz, 2002. Another phocine distemper outbreak in Europe. Science 297: 209.

    Article  PubMed  CAS  Google Scholar 

  • Jokela, J. & C. M. Lively, 1995. Parasites, sex, and early reproduction in a mixed population of freshwater snails. Evolution 49: 1268–1271.

    Article  Google Scholar 

  • Kohler, S. L. & W. K. Hoiland, 2001. Population regulation in an aquatic insect: the role of disease. Ecology 82: 2294–2305.

    Article  Google Scholar 

  • Kohler, S. L. & M. J. Wiley, 1992. Parasite-induced collapse of populations of a dominant grazer in Michigan streams. Oikos 65: 443–449.

    Article  Google Scholar 

  • Kuznetsov, V. V., 1960. The White Sea and biological peculiarities of its flora and fauna. Academy of Sciences USSR, Moscow. (in Russian).

    Google Scholar 

  • Lafferty, K. D., 1993. Effect of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Marine Ecology Progress Series 96: 229–237.

    Article  Google Scholar 

  • Lauckner, G., 1980. Diseases of Mollusca: Gastropoda. In Kinne, O. (ed.), Diseases of Marine Animals, Vol. 1. Biologische Anstalt Helgoland, Hamburg: 311–424.

    Google Scholar 

  • Miller, R. G., 1981. Simultaneous Statistical Inference, 2nd ed. Springer, New York.

    Book  Google Scholar 

  • Poulin, R. & K. N. Mouritsen, 2006. Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80: 183–191.

    Article  PubMed  CAS  Google Scholar 

  • Reid, D. G., 1996. Systematics and Evolution of Littorina. The Ray Society, London.

    Google Scholar 

  • Schloegel, L. M., J.-M. Hero, L. Berger, R. Speare, K. McDonald & P. Daszak, 2006. The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3: 35–40.

    Article  Google Scholar 

  • Schmid-Hempel, P., 2011. Evolutionary Parasitology. Oxford University Press, Oxford.

    Google Scholar 

  • Sergievsky, S. O., A. I. Granovitch & N. A. Mikhailova, 1986. Impact of trematode invasion on survival of mollusks Littorina obtusata (L.) и L.saxatilis (Olivi) under conditions of extremely low salinity. Parazitologiya 20: 202–207. (in Russian).

    Google Scholar 

  • Sokolova, I. M., 1995. Influence of trematodes on the demography of Littorina saxatilis (Gastropoda: Prosobranchia: Littorinidae) in the White Sea. Diseases of Aquatic Organisms 21: 91–101.

    Article  Google Scholar 

  • Sousa, W. P., 1983. Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. Journal of Experimental Marine Biology and Ecology 73: 273–296.

    Article  Google Scholar 

  • Tompkins, D. M., A. M. Dunn, M. J. Smith & S. Telfer, 2010. Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80: 19–38.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to the administration of the Kandalaksha Nature Reserve for their support of our long-term study on Rjazhkov Island. We also wish to thank Prof. V. Berger and Prof. A. Sukhotin (White Sea Biological Station of the Zoological Institute of Russian Academy of Sciences) and M. Levitin (Marine Biological Station of St. Petersburg State University) for providing logistic support, Dr. Sergievsky and Dr. Mikhailova who played a key role in the long-term monitoring of Littorina populations in the White Sea, and all the students who helped us during this study. We also thank unknown referees for providing useful criticism and linguistic corrections of the manuscript. During the work on this manuscript the authors were funded in part by the St. Petersburg University Research Grants No. 1.37.80.2011 and No. 1.0.140.2010 and RFBR Grant No. 12-04-00312a.

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Correspondence to A. I. Granovitch.

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Guest editor: A. A. Sukhotin / Long-term research on marine ecosystems in the White Sea, Russia

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Granovitch, A.I., Maximovich, A.N. Long-term population dynamics of Littorina obtusata: the spatial structure and impact of trematodes. Hydrobiologia 706, 91–101 (2013). https://doi.org/10.1007/s10750-012-1411-7

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  • DOI: https://doi.org/10.1007/s10750-012-1411-7

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