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Effects of Chaetogaster limnaei limnaei (Oligochaeta, Tubificidae) on freshwater snail communities

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Abstract

From laboratory studies, the relationship between the oligochaete Chaetogaster limnaei limnaei (CL) and its freshwater snail hosts is known to be context-dependent, ranging from mutualistic to parasitic. We monitored snail communities of seven streams in Germany during three seasons of a year and investigated infestation by CL. Some snail species never were infested. In snail species that were infested, size, substratum type, oxygen concentration and species identity were the most important variables explaining the variance in CL infestation. Independent of individual snail size, Bithynia tentaculata, Ancylus fluviatilis and Acroloxus lacustris showed the highest CL abundances. Across species, CL abundances were highest in large individuals on silty substratum at well-oxygenated sites. Reproductive success of snail populations was estimated from proportion of juveniles in populations. This measure of reproductive success of snail populations was inversely related with CL infestation level. These results suggest that CL infestation affects aquatic snails at the population and community level in the field. Differential infestation levels and different impacts of CL infestation between species lead to an asymmetric distribution of positive and negative effects among all snail species present in a habitat. Thus, CL may be an overlooked agent in structuring snail communities.

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References

  • AQEM, 2002. Manual for the application of the AQEM system. http://www.aqem.de/index.php.

  • Arneberg, P., 2001. An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24: 352–358.

    Article  Google Scholar 

  • Arneberg, P., A. Skorping, B. Grenfell & A. F. Read, 1998. Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B 265: 1283–1289.

    Article  PubMed Central  Google Scholar 

  • Backlund, H. O., 1949. En kommensal som äter sitt värddjurs parasiter. Fauna och flora: populär tidskrift för biologi 44: 38–41.

    Google Scholar 

  • Brinkhurst, R. O. & B. G. M. Jamieson, 1971. Aquatic Oligochaeta of the World. Oliver and Boyd, Edinburgh.

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Buston, P. M. & J. Elith, 2011. Determinants of reproductive success in dominant pairs of clownfish: a boosted regression tree analysis. Journal of Animal Ecology 80: 528–538.

    Article  PubMed  Google Scholar 

  • Domisch, S., S. Jähnig, J. P. Simaika, M. Kuemmerlen & S. Stoll, 2015. Application of species distribution models in stream ecosystems: the challenges of spatial and temporal scale, environmental predictors and species occurrence data. Fundamental and Applied Limnology 186: 45–61.

    Google Scholar 

  • Elith, J., J. R. Leathwick & T. Hastie, 2008. Boosted regression trees - a new technique for modelling ecological data. Journal of Animal Ecology 77: 802–813.

    Article  CAS  PubMed  Google Scholar 

  • Faltynkova, A. & W. Haas, 2006. Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitology Research 99: 572–582.

    Article  PubMed  Google Scholar 

  • Fashuyi, S. A. & M. O. Williams, 1977. The role of Chaetogaster limnaei in the dynamics of trematode transmission in natural populations of freshwater snails. Zeitschrift für Parasitenkunde 54: 55–60.

    Article  CAS  PubMed  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). American Midland Naturalist 125: 195–205.

    Article  Google Scholar 

  • Friedman, J., T. Hastie & R. Tibshirani, 2000. Additive logistic regression: a statistical way of boosting. Annals of Statistics 28: 1189–1232.

    Article  Google Scholar 

  • Früh, D., P. Haase, & S. Stoll, 2015. Temperature drives asymmetric competition between alien and indigenous freshwater snails (Physa acuta vs. Physa fontinalis). PeerJ PrePrints 3: e1227.

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Haase, P., S. Lohse, S. Pauls, K. Schindehütte, A. Sundermann, P. Rolauffs & D. Hering, 2004. Assessing streams in Germany with benthic invertebrates: development of a practical standardized protocol for macroinvertebrate sampling and sorting. Limnologica 34: 349–365.

    Article  Google Scholar 

  • Hastie, T., R. Tibshirani & J. Friedman, 2009. The elements of statistical learning: Data mining, inference and prediction. Springer, New York.

    Book  Google Scholar 

  • Hijmans, R. J., S. Phillips, J. R. Leathwick, & J. Elith, 2013. Dismo: species distribution modelling. R package version 08-11. http://CRAN.R-project.org/package=dismo.

  • Höckendorff, S., D. Früh, N. Hormel, P. Haase & S. Stoll, 2015. Biotic interactions under climate warming: temperature-dependent and species-specific effects of the oligochaete Chaetogaster limnaei on snails. Freshwater Science 34: 1304–1311.

    Article  Google Scholar 

  • Hoover, J. J. & M. J. Lodes, 1986. Chaetogaster limnaei (Oligochaeta: Naididae) in Oklahoma. The Southwestern Naturalist 31: 542–544.

    Article  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. J. Boyle, R. R. Sheehy, L. K. Belden & J. M. Wojdak, 2015. Dispersal of a defensive symbiont depends on contact between hosts, host health, and host size. Oecologia 179(2): 307–318.

    Article  PubMed  Google Scholar 

  • 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: 25–33.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Learner, M. A., G. Glochhead & B. D. Hughes, 1978. A review of the biology of British Naididae (Oligochaeta) with emphasis on the lotic environment. Freshwater Biology 8(4): 357–375.

    Article  Google Scholar 

  • Martins, R. T. & R. G. Alves, 2010. Occurrence of Chaetogaster limnaei K. von Baer, 1927 (Oligochaeta, Naididae) associated with Gastropoda mollusks in horticultural channels in Southeastern Brazil. Brazilian Journal of Biology 70: 1055–1057.

    Article  CAS  Google Scholar 

  • Michelson, E. H., 1964. The protective action of Chaetogaster limnaei on snails exposed to Schistosoma mansoni. Journal of Parasitology 50: 441–444.

    Article  CAS  PubMed  Google Scholar 

  • Mrazek, A., 1917. The feeding habits of Chaetogaster limnaei. Sbornik Zoologicky 1: 22–23.

    Google Scholar 

  • R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Rajasekariah, G. R., 1978. Chaetogaster limnaei K von Baer 1872 on Lymnaea tomentosa: Ingestion of Faciola hepatica cercariae. Experientia 34: 1458–1459.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sankurathri, C. S. & 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: 1742–1753.

    Article  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: 642–649.

    Article  Google Scholar 

  • Streit, B., 1974. Populationsdynamik von Chaetogaster limnaei limnaei in einer Population von Ancylus fluviatilis. Archiv für Hydrobiologie Supplement 47: 106–118.

    Google Scholar 

  • Streit, B., 1977. Morphometric relationships and feeding habits of two species of Chaetogaster, Ch. limnaei and Ch. diastrophus (Oligochaeta). Archiv für Hydrobiologie Supplement 48: 424–437.

    Google Scholar 

  • Vaghin, V., 1946. On the biological species of Chaetogaster limnaei, k. Baer. Doklady Akademii Nauk SSSR 51: 481–484.

    Google Scholar 

  • Wagin, V. W. L., 1941. Chaetogaster limnaei K. Baer als Cercarienvertilger. Zoologischer Anzeiger 95: 55–59.

    Google Scholar 

  • Young, M. R., 1974. Seasonal variation in the occurrance of Chaetogaster limnaei limnaei Gruffydd (Oligochaeta) in two of its molluscan hosts in the Worcester-Birmingham canal and its relationship with the digenean parasites of these molluscs. Journal of Natural History 8: 529–535.

    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: 788–791.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study used data that were generated at the Long-Term Ecological Research (LTER) site “Rhine-Main-Observatory”. The comments of three anonymous reviewers helped to improve this manuscript.

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Authors and Affiliations

  1. Department of River Ecology and Conservation, Senckenberg Research Institute and Natural History Museum Frankfurt, 63571, Gelnhausen, Germany

    Stefan Stoll, Nico Hormel, Denise Früh & Jonathan D. Tonkin

  2. Department of Ecotoxicology and Environment, University of Koblenz-Landau, 76829, Landau, Germany

    Stefan Stoll

  3. Environment and Consumer Protection, North Rhine-Westphalia State Agency for Nature, 40221, Düsseldorf, Germany

    Denise Früh

  4. Department of Integrative Biology, Oregon State University, Corvallis, OR, 97331, USA

    Jonathan D. Tonkin

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  1. Stefan Stoll
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  2. Nico Hormel
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Correspondence to Stefan Stoll.

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Handling editor: Marcelo S. Moretti

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Stoll, S., Hormel, N., Früh, D. et al. Effects of Chaetogaster limnaei limnaei (Oligochaeta, Tubificidae) on freshwater snail communities. Hydrobiologia 785, 101–113 (2017). https://doi.org/10.1007/s10750-016-2909-1

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