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Sharing the load: a survey of parasitism in the invasive freshwater pulmonate, Physa acuta (Hygrophila: Physidae) and sympatric native snail populations

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Abstract

The highly invasive freshwater snail, Physa acuta, was examined for parasites over temporal and spatial scales. All populations studied had a high prevalence of the parasitic morph of the oligochaete worm, Chaetogaster limnaei. This worm was also found to infect two native snails, Glyptophysa gibbosa and Austropeplea tomentosa, at lower prevalences. Seasonality and collection sites did not significantly influence the worm’s infection dynamics, but strong positive correlations were found between the sizes of P. acuta individuals and both the likelihood of infection and infection intensity. The ectocommensal morph of C. limnaei was found in all three pulmonate species. Physa acuta was infected with two digenean trematode species which were also found in two native snails, Posticobia brazieri and G. gibbosa. One digenean, found within the renal gland of P. acuta, did not significantly influence the presence or infection intensity of the renal gland-dwelling C. limnaei parasitic morph. All parasites infecting P. acuta were also found to be infecting sympatric native freshwater snails. The effects that such host sharing by parasites may have upon the establishment of P. acuta as a successful invader merit further study.

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References

  • Albrecht, C., O. Kroll, E. Moreno Terrazas & T. Wilke, 2009. Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biological Invasions 11(8): 1821–1826.

    Article  Google Scholar 

  • Andrews, J. M., J. N. Childress, T. J. Iakovidis & G. J. Langford, 2015. Elucidating the life history and ecological aspects of Allodero hylae (Annelida: Clitellata: Naididae), a parasitic oligochaete of invasive Cuban tree frogs in Florida. Journal of Parasitology 101(3): 275–281.

    Article  PubMed  Google Scholar 

  • Barbour, M. T., 1977. Chaetogaster limnaei limnaei (Oligochaeta: Naididae) inhabiting the mantle cavity of the pill clam Sphaerium. Transactions of the American Microscopical Society 96(1): 141–142.

    Article  PubMed  CAS  Google Scholar 

  • Bedhomme, S., P. Agnew, Y. Vital, C. Sidobre & Y. Michalakis, 2005. Prevalence-dependent costs of parasite virulence. Plos Biology 3: e262.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blair, D., G. M. Davis & B. Wu, 2001. Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123(7): 229–243.

    Article  Google Scholar 

  • Boray, J., 1964. Studies on the ecology of Lymnaea tomentosa, the intermediate host of Fasciola hepatica. 1. History, geographical distribution, and environment. Australian Journal of Zoology 12(2): 217–230.

    Article  Google Scholar 

  • Buse, A., 1971. Population dynamics of Chaetogaster limnaei vaghini Gruffydd (Oligochaeta) in a field population of Lymnaea stagnalis L. Oikos 22(1): 50–55.

    Article  Google Scholar 

  • Buse, A., 1972. Behavioural aspects of the relationship of Chaetogaster limnaei (Oligochaeta: Naididae) with its gastropod host. Animal Behaviour 20(2): 274–279.

    Article  PubMed  CAS  Google Scholar 

  • Buse, A., 1974. The relationship of Chaetogaster limnaei (Oligochaeta: Naididae) with a variety of gastropod species. Journal of Animal Ecology 43(3): 821–837.

    Article  Google Scholar 

  • Callisto, M., P. Moreno, J. F. Gonçalves Jr, W. R. Ferreira & C. L. Z. Gomes, 2005. Malacological assessment and natural infestation of Biomphalaria straminea (Dunker, 1848) by Schistosoma mansoni (Sambon, 1907) and Chaetogaster limnaei (K. Von Baer, 1827) in an urban eutrophic watershed. Brazilian Journal of Biology 65(2): 217–228.

    CAS  Google Scholar 

  • Conn, D. B., M. N. Babapulle, K. A. Klein & D. A. Rosen, 1994. Invading the invaders: infestation of zebra mussels by native parasites in the St. Lawrence River. Proceedings of the Fourth International Zebra Mussel Conference. Wisconsin Sea Grant Institute, Madison, Wisconsin 515–523.

  • Conn, D. B., A. Ricciardi, M. N. Babapulle, K. A. Klein & D. A. Rosen, 1996. Chaetogaster limnaei (Annelida: Oligochaeta) as a parasite of the zebra mussel Dreissena polymorpha, and the quagga mussel Dreissena bugensis (Mollusca: Bivalvia). Parasitology Research 82(1): 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Cope, N. J. & M. J. Winterbourn, 2004. Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study. Aquatic Ecology 38(1): 83–91.

    Article  Google Scholar 

  • Davies, O. B., 1913. On two new species of Chaetogaster. Proceedings of the Royal Society of Victoria Melbourne 26: 88–98.

    Google Scholar 

  • Dillon, R. T. & A. R. Wethington, 2002. Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebrate Biology 121(3): 226–234.

    Article  Google Scholar 

  • Eng, L. L., 1976. A note on the occurrence of a symbiotic oligochaete, Chaetogaster limnaei, in the mantle cavity of the Asiatic clam. Corbicula manilensis. Veliger 19: 208.

    Google Scholar 

  • Esch, G. W. & J. C. Fernandez, 1994. Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. The American Midland Naturalist 131(2): 209–237.

    Article  Google Scholar 

  • Fernandez, J., T. M. Goater & G. W. Esch, 1991. Population dynamics of Chaetogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). The American Midland Naturalist 125(2): 195–205.

    Article  Google Scholar 

  • Gruffydd, L. D., 1965a. Evidence for the existence of a new subspecies of Chaetogaster limnaei (Oligochaeta). Britain. Journal of Zoology 146(2): 175–196.

    Google Scholar 

  • Gruffydd, L. D., 1965b. The population biology of Chaetogaster limnaei limnaei and Chaetogaster limnaei vaghini (Oligochaeta). Journal of Animal Ecology 34(3): 667–690.

    Article  Google Scholar 

  • Hall, S. R., C. R. Becker, J. L. Simonis, M. A. Duffy, A. J. Tessier & C. E. Cáceres, 2009. Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90(3): 791–801.

    Article  PubMed  Google Scholar 

  • Hopkins, S. R., J. A. Wyderko, R. R. Sheehy, L. K. Belden & J. M. Wojdak, 2013. Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts. Ecology and Evolution 3(13): 4427–4438.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopkins, S. R., L. K. Boyle, L. K. Belden, and J. M. Wojdak., In press. Dispersal of a defensive symbiont depends on contact between hosts, host health, and host size. Oecologia.

  • Ibrahim, M. M., 2007. Population dynamics of Chaetogaster limnaei (Oligochaeta: Naididae) in the field populations of freshwater snails and its implications as a potential regulator of trematode larvae community. Parasitology Research 101(1): 25–33.

    Article  PubMed  Google Scholar 

  • Kataranovski, D., D. Jakovčev & M. Lenhardt, 2000. The first record and description of Chaetogaster limnaei von Baer, 1827 (Naididae, Oligochaeta) on Huso huso fry in Serbia. Helminthologia 37(3): 162–164.

    Google Scholar 

  • Kelly, D. W., R. A. Paterson, C. R. Townsend, R. Poulin & D. M. Tompkins, 2009. Parasite spillback: a neglected concept in invasion ecology? Ecology 90(8): 2047–2056.

    Article  PubMed  CAS  Google Scholar 

  • Khalil, L. F., 1961. On the capture and destruction of miracidia by Chaetogaster limnaei (Oligochaeta). Journal of Helminthology 35(3–4): 269–274.

    Article  PubMed  CAS  Google Scholar 

  • Koch, M., 2004. Aquatic snails and their trematodes in the New England Tablelands (New South Wales): low diversity and unstable population structure explained by unpredictable environmental fluctuations. (PhD thesis) University of New England.

  • Lockyer, A. E., C. S. Jones, L. R. Noble & D. Rollinson, 2004. Trematodes and snails: an intimate association. Canadian Journal of Zoology 82(2): 251–269.

    Article  Google Scholar 

  • McCarthy, A. M., 1990. Speciation of echinostomes: evidence for the existence of two sympatric sibling species in the complex Echinoparyphium recurvatum (von Linstow 1873) (Digenea: Echinostomatidae). Parasitology 101(1): 35–42.

    Article  PubMed  Google Scholar 

  • McKoy, S. A., E. J. Hyslop & R. D. Robinson, 2011. Associations between two trematode parasites, an ectosymbiotic annelid, and Thiara (tarebia) granifera (Gastropoda) in Jamaica. Journal of Parasitology 97(5): 828–832.

    Article  PubMed  Google Scholar 

  • Muñoz-Antoli, C., A. Marin, A. Vidal, R. Toledo & J. G. Esteban, 2008. Euparyphium albuferensis and Echinostoma friedi (Trematoda: Echinostomatidae): experimental cercarial transmission success in sympatric snail communities. Folia Parasitologica 55(2): 122–126.

    Article  PubMed  Google Scholar 

  • Murphy, M. J. & M. Shea, 2013. Survey of the terrestrial and freshwater molluscan fauna of the Pilliga Forest area in northern inland New South Wales. Molluscan Research 33(4): 237–253.

    Article  Google Scholar 

  • Pinder, A., 2001. Notes on the diversity and distribution of Australian Naididae and Phreodrilidae (Oligochaeta: Annelida). Hydrobiologia 463(1–3): 49–64.

    Article  Google Scholar 

  • Rodgers, J. K., G. J. Sandland, S. R. Joyce & D. J. Minchella, 2005. Multispecies interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata). Journal of Parasitology 91(3): 709–712.

    Article  PubMed  Google Scholar 

  • R Development Core Team, 2010. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org

  • Rajasekariah, G., 1978. Chaetogaster limnaei K von Baer 1872 on Lymnaea tomentosa: ingestion of Fasciola hepatica cercariae. Experientia 34(11): 1458–1459.

    Article  PubMed  CAS  Google Scholar 

  • Sankurathri, C. & J. C. Holmes, 1976. Effects of thermal effluents on parasites and commensals of Physa gyrina Say (Mollusca: Gastropoda) and their interactions at Lake Wabamun, Alberta. Canadian Journal of Zoology 54(10): 1742–1753.

    Article  Google Scholar 

  • Simpson, R. D. & J. Stanisic, 1976. Faunal survey of New England. II. The distribution of gastropod molluscs. Memoirs of the Queensland Museum 22(2): 115–139.

    Google Scholar 

  • Schneck, J. L. & B. Fried, 2004. Effects of snail size on encystment of Echinostoma caproni in juvenile Biomphalaria glabrata (NMRI strain) and observations on the survival of infected snails. Journal of Helminthology 78(3): 277–279.

    Article  PubMed  CAS  Google Scholar 

  • Smythe, A. B., K. Forgrave, A. Patti, R. Hochberg & M. K. Litvaitis, 2015. Untangling the ecology, taxonomy, and evolution of Chaetogaster limnaei (Oligochaeta: Naididae) species complex. Journal of Parasitology 101(3): 320–326.

    Article  PubMed  Google Scholar 

  • Stoll, S., D. Früh, B. Westerwald, N. Hormel & P. Haase, 2013. Density dependent relationship between Chaetogaster limnaei limnaei (Oligochaeta) and the freshwater snail Physa acuta (Pulmonata). Freshwater Science 32(2): 642–649.

    Article  Google Scholar 

  • Torchin, M. E., K. D. Lafferty, A. P. Dobson, V. J. McKenzie & A. M. Kuris, 2003. Introduced species and their missing parasites. Nature 421(6923): 628–630.

    Article  PubMed  CAS  Google Scholar 

  • Van Leeuwen, C. H. A., N. Huig, G. Van Der Velde, T. A. Van Alen, C. A. M. Wagemaker, C. D. H. Sherman, M. Klaassen & J. Figuerola, 2013. How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species. Freshwater Biology 58(1): 88–99.

    Article  Google Scholar 

  • Zimmermann, M. R., K. E. Luth & G. W. Esch, 2011. Complex interactions among a nematode parasite (Daubaylia potomaca), a commensalistic annelid (Chaetogaster limnaei limnaei), and trematode parasites in a snail host (Helisoma anceps). Journal of Parasitology 97(5): 788–791.

    Article  PubMed  Google Scholar 

  • Zukowski, S. & K. F. Walker, 2009. Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray. South Australia. Marine and Freshwater Research 60(10): 999–1005.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Dr Winston Ponder of the Australian Museum, for his identification of Posticobia brazieri, Dr Tom Cribb of the University of Queensland, for freely sharing his knowledge regarding the parasites of Posticobia brazieri, Associate Professor Darren Ryder for his suggested study sites, and Sandy Watson and Louise Streeting for their technical assistance. We would also like to thank two anonymous reviewers for their helpful comments and suggestions which greatly improved this manuscript.

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  1. Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, 2351, Australia

    D. Rex Mitchell & Tommy L. F. Leung

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Correspondence to D. Rex Mitchell.

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Mitchell, D.R., Leung, T.L.F. Sharing the load: a survey of parasitism in the invasive freshwater pulmonate, Physa acuta (Hygrophila: Physidae) and sympatric native snail populations. Hydrobiologia 766, 165–172 (2016). https://doi.org/10.1007/s10750-015-2452-5

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  • DOI: https://doi.org/10.1007/s10750-015-2452-5

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