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Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes

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Abstract

Trophically-transmitted parasites can affect intermediate host behaviors, resulting in spatial differences in parasite prevalence and distribution that shape the dynamics of hosts and their ecosystems. This variability may arise through differences in physical habitats or biological interactions between parasites and their hosts, and may occur on very fine spatial scales. Using a pseudophyllidean cestode (Schistocephalus solidus) and the threespine stickleback (Gasterosteus aculeatus) as a model parasite–host complex, we investigated the association of infection with host diet composition and stomach fullness in different habitats of two large lakes in southwest Alaska. To become infected, the fish must consume pelagic copepods infected with the parasite’s procercoid stage, so we predicted higher infection rates of fish in offshore habitats (where zooplankton are the primary prey) compared to fish from the littoral zone. Sticklebacks collected from the littoral and limnetic zones were assayed for parasites and their stomach contents were classified, counted, and weighed. Contrary to our prediction, permutational multivariate analysis of variance and principal components analysis revealed that threespine sticklebacks in the littoral zone, which consumed a generalist diet (pelagic zooplankton and benthic invertebrates), had higher parasite prevalence and biomass intensity than conspecifics in the limnetic zone, which consumed zooplankton. These results, consistent in two different lakes, suggest that differences in parasite prevalence between habitats may have been determined by a shift in host habitat due to infection, differential host mortality across habitats, differential procercoid prevalence in copepods across habitats, or a combination of the three factors. This paradoxical result highlights the potential for fine spatial variability in parasite abundance in natural systems.

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Fig. 1: Study sites
Fig. 2: Individual diet components
Fig. 3: Diet composition ordination
Fig. 4: Parasite biomass intensities

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Acknowledgements

We thank Jason Ching and Harry Rich Jr. for assistance with specimen collection, Brian Harmon and Hannah Stapleton for sample processing, Julian Olden for analytical insight, and Harry Rich Jr. for his knowledge of Iliamna Lake birds. Thanks to Chelsea Wood and five reviewers for helpful comments that improved this manuscript. Funding for this project was provided by the Clarence H. Campbell Endowed Lauren Donaldson Scholarship in Ocean and Fishery Sciences, the Achievement Rewards for College Scientists (ARCS) Foundation Seattle Chapter via the Barton Family, the H. Mason Keeler Endowment, the Richard and Lois Worthington Endowment, and the Richard T. Whiteleather Fisheries B.S. 1935 Endowed Scholarship. The long-term research on the ecology of these lakes has been supported by many agencies but especially the National Science Foundation’s BioComplexity Program, and Coupled Natural and Human Systems Program, the Gordon and Betty Moore Foundation, and the Pacific seafood processing industry. Permits for the capture and handling of fish were provided by the Alaska Department of Fish and Game and the University of Washington’s IACUC.

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Correspondence to Martin C. Arostegui.

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Table 3 Summary information. Threespine stickleback metrics for each habitat/lake group. Parasite biomass intensity, fullness, and fork length are reported as the mean +/− 1 standard deviation. Parasite burden and lateral plate count are reported as the mode. Significant difference is determined by the corresponding statistical test and post-hoc multiple comparison test listed in the methods. Lake/habitat groups are abbreviated as follows: Aleknagik Littoral (ALIT), Aleknagik Limnetic (ALIM), Iliamna Littoral (ILIT), Iliamna Limnetic (ILIM).

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Arostegui, M.C., Hovel, R.A. & Quinn, T.P. Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes. Environ Biol Fish 101, 501–514 (2018). https://doi.org/10.1007/s10641-018-0719-1

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  • DOI: https://doi.org/10.1007/s10641-018-0719-1

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