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Hydrobiologia

, Volume 654, Issue 1, pp 83–92 | Cite as

The zebra mussel (Dreissena polymorpha) impacts European bitterling (Rhodeus amarus) load in a host freshwater mussel (Unio pictorum)

  • Philine S. E. zu Ermgassen
  • David C. Aldridge
Primary research paper

Abstract

The European bitterling, Rhodeus amarus, is a non-indigenous fish species in British fresh waters. It lays its eggs in unionid mussels which themselves are vulnerable to fouling by the non-indigenous zebra mussel, Dreissena polymorpha. Observations from an unmanipulated natural system showed that only 27% of zebra mussel-fouled Unio pictorum hosted bitterling, while 47% of unfouled U. pictorum hosted bitterling. We conducted a field experiment in the River Great Ouse catchment, Cambridgeshire, England in May–June 2007 and 2008 to quantify the impact of zebra mussels on bitterling load in host mussels. Zebra mussel-fouled unionids were significantly less likely to host bitterling than unfouled unionids. The number of unionids hosting bitterling did not differ significantly whether the zebra mussels fouling the unionid were alive or dead. Bitterling appeared to discriminate against zebra mussel-fouled unionids less as the 2007 breeding season advanced, potentially because preferred unfouled unionids had a higher bitterling load, and were therefore relatively lower quality hosts than at the start of the breeding season.

Keywords

Invasive species Indirect interaction Amensalism Dreissenidae 

Notes

Acknowledgements

The authors would like to thank Alexandra Zieritz, Nicole Spann, Ben Phalan and Jonathan Gair for their field assistance and Erasmus zu Ermgassen for statistical assistance. We would also like to thank the Environment Agency for data, all at Jones & Sons at St. Ives marina for allowing us access, and Susannah Cass and Francesca Pilotto for assisting with the glycogen analysis. This work was funded by a Natural Environment Research Council studentship to P.S.E.z.E. (NER/S/A/2005/13273) and the British water industry. We thank Carl Smith, John Reynolds and one anonymous reviewer for their comments on earlier versions of this manuscript.

References

  1. Aldridge, D. C., 1997. Reproductive ecology of bitterling (Rhodeus sericeus Pallas) and unionid mussels. PhD thesis. Department of Zoology, University of Cambridge, Cambridge.Google Scholar
  2. Aldridge, D. C., 1999. Development of European bitterling in the gills of freshwater mussels. Journal of Fish Biology 54: 138–151.CrossRefGoogle Scholar
  3. Aldridge, D. C., P. Elliott & G. D. Moggridge, 2004. The recent and rapid spread of the zebra mussel (Dreissena polymorpha) in Great Britain. Biological Conservation 119: 253–261.CrossRefGoogle Scholar
  4. Baker, S. M. & D. J. Hornbach, 1997. Acute physiological effects of zebra mussel (Dreissena polymorpha) infestation on two unionid mussels, Actinonaias ligamentina and Amblema plicata. Canadian Journal of Fisheries and Aquatic Sciences 54: 512–519.CrossRefGoogle Scholar
  5. Baker, S. M. & D. J. Hornbach, 2000. Physiological status and biochemical composition of a natural population of unionid mussels (Amblema plicata) infested by zebra mussels. American Midland Naturalist 143: 443–452.CrossRefGoogle Scholar
  6. Balon, E. K., 1962. Note on the number of Danubian bitterlings developmental stages in mussels. Vestník Československé Spolecnosti Zoologické 26: 250–256.Google Scholar
  7. Bervoets, L., J. Coeck & R. F. Verheyen, 1990. The value of lowland rivers for the conservation of rare fish in Flanders. Journal of Fish Biology 37: 223–224.CrossRefGoogle Scholar
  8. Bogutskaya, N. G. & A. M. Komlev, 2001. Some new data to morphology of Rhodeus sericeus (Cyprinidae: Acheilognathinae) and a description of a new species, Rhodeus colchicus, from west Transcaucasia. Proceedings of the Zoological Institute 287: 81–97.Google Scholar
  9. Candolin, U. & J. D. Reynolds, 2001. Sexual signaling in the European bitterling: females learn the truth by direct inspection of the resource. Behavioral Ecology 12: 407–411.CrossRefGoogle Scholar
  10. Cohen, A. N. & J. T. Carlton, 1998. Accelerating invasion rate in a highly invaded estuary. Science 23: 555–558.CrossRefGoogle Scholar
  11. Copp, G. H., S. Stakenas & P. I. Davison, 2006. The incidence of non-native fishes in watercourses: example of the United Kingdom. Aquatic Invasions 1: 72–75.CrossRefGoogle Scholar
  12. Crawley, M. J., 2002. Statistical computing. Wiley, Chichester, England.Google Scholar
  13. Dahlhoff, E. P., J. H. Stillman & B. A. Menge, 2002. Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integrative and Comparative Biology 42: 862–871.CrossRefGoogle Scholar
  14. DAISIE, 2009. http://www.europe-aliens.org/ (Accessed September 2009).
  15. Davies, C. E., J. Shelley, P. T. Harding, I. F. G. Mclean, R. Gardiner & G. Peirson (eds), 2004. Freshwater fishes in Britain: the species and their distribution. Harley Books, Colchester, UK.Google Scholar
  16. Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers & F. Smith, 1956. Colorimetric method of determination of sugars and related substances. Analytical Chemistry 28: 350–356.CrossRefGoogle Scholar
  17. Hebert, P. D. N., C. C. Wilson, M. H. Murdoch & R. Lazar, 1991. Demography and ecological impacts of the invading mollusc Dreissena polymorpha. Canadian Journal of Zoology 69: 405–409.CrossRefGoogle Scholar
  18. Heschl, A., 1989. Integration of “innate” and “learned” components with IRME for mussel recognition in the European bitterling Rhodeus amarus (Bloch). Ethology 81: 193–208.CrossRefGoogle Scholar
  19. Keller, R. P., P. S. E. zu Ermgassen & D. C. Aldridge, 2009. Vectors and timing of freshwater invasions in Great Britain. Conservation Biology 23: 1526–1534.CrossRefPubMedGoogle Scholar
  20. Levine, J. M., P. B. Adler & S. G. Yelenik, 2004. A meta-analysis of biotic resistance to exotic plant invasions. Ecology Letters 7: 975–989.CrossRefGoogle Scholar
  21. Mackie, G. L., 1991. Biology of the exotic zebra mussel, Dreissena polymorpha, in relation to native bivalves and its potential impact in Lake St. Clair. Hydrobiologia 219: 251–268.Google Scholar
  22. McIvor, A. L. & D. C. Aldridge, 2007. The reproductive biology of the Depressed river mussel, Pseudanodonta complanata (Bivalvia: Unionidae), with implications for its conservation. Journal of Molluscan Studies 73: 259–266.CrossRefGoogle Scholar
  23. Mills, S. C. & J. D. Reynolds, 2002. Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131: 473–478.CrossRefGoogle Scholar
  24. Mills, S. C. & J. D. Reynolds, 2004. The importance of species interactions in conservation: the endangered European bitterling Rhodeus sericeus and its freshwater mussel hosts. Animal Conservation 7: 257–263.CrossRefGoogle Scholar
  25. Mills, S. C., M. I. Taylor & J. D. Reynolds, 2005. Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium approach. Animal Behaviour 70: 31–37.CrossRefGoogle Scholar
  26. Povz, M., 1992. The Red List of endangered Pisces and Cyclostomata in Slovenia. Varstvo Narave 17: 51–59.Google Scholar
  27. Reynolds, J. D., V. J. Debuse & D. C. Aldridge, 1997. Host specialisation in an unusual symbiosis: European bitterlings spawning in freshwater mussels. Oikos 78: 539–545.CrossRefGoogle Scholar
  28. Reynolds, J. D. & H. P. Guillaume, 1998. Effects of phosphate on the reproductive symbiosis between bitterling and freshwater mussels: implications for conservation. Journal of Applied Ecology 35: 575–581.CrossRefGoogle Scholar
  29. Ricciardi, A., 2006. Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Diversity and Distributions 12: 425–433.CrossRefGoogle Scholar
  30. Ricciardi, A., R. J. Neves & J. B. Rasmussen, 1998. Impending extinctions of North American freshwater mussels (Unionida) following the zebra mussel (Dreissena polymorpha) invasion. Journal of Animal Ecology 67: 613–619.CrossRefGoogle Scholar
  31. Riisgård, H., C. Kittner & D. F. Seerup, 2003. Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arenaria) in response to low algal concentration. Journal of Experimental Marine Biology and Ecology 284: 105–127.CrossRefGoogle Scholar
  32. Schaumburg, J., 1989. Zur Ökologie von Stichling Gasterosteus aculeatus L., Bitterling Rhodeus sericeus amarus Bloch, 1782 und oderlischen Leucaspius delineatus (Heckel, 1843)—drei bestandsbedrohten, einheimischen Kleinfischarten. Berichte der Akademie für Naturschutz und Landschaftspflege 13: 145–194.Google Scholar
  33. Schloesser, D. W., T. F. Nalepa & G. L. Mackie, 1996. Zebra mussel infestation of unionid bivalves (Unionidae) in North America. American Zoologist 36: 300–310.Google Scholar
  34. Schloesser, D. W. & W. P. Kovalak, 1991. Infestation of Unionids by Dreissena polymorpha in a power plant canal in Lake Erie. Journal of Shellfish Research 10: 355–359.Google Scholar
  35. Smith, C., M. Reichard, P. Jurajda & M. Przybylski, 2004. The reproductive ecology of the European bitterling (Rhodeus sericeus). Journal of Zoology 262: 107–124.CrossRefGoogle Scholar
  36. Smith, C., J. D. Reynolds, W. J. Sutherland & P. Jurajda, 2000. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behavioural Ecology and Sociobiology 48: 29–35.CrossRefGoogle Scholar
  37. Smith, C., K. Rippon, A. Douglas & P. Jurajda, 2001. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshwater Biology 46: 903–911.CrossRefGoogle Scholar
  38. Sokal, R. R. & F. J. Rohlf, 1995. Biometry (3rd edn). Freeman and Company, New York, USA.Google Scholar
  39. Sowerby, J. C., 1825. Extracts from the minute book of the Linnean Society. Transactions of the Linnean Society of London 14: 585.Google Scholar
  40. Strayer, D. L. & L. C. Smith, 1996. Relationships between zebra mussels (Dreissena polymorpha) and unionid clams during the early stages of the zebra mussel invasion of the Hudson River. Freshwater Biology 36: 771–779.Google Scholar
  41. Van Damme, D., N. Bogutskaya, R. C. Hoffmann & C. Smith, 2007. The introduction of the European bitterling (Rhodeus amarus) to West and Central Europe. Fish and Fisheries 8: 79–106.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Philine S. E. zu Ermgassen
    • 1
  • David C. Aldridge
    • 1
  1. 1.Aquatic Ecology Group, Department of ZoologyUniversity of CambridgeCambridgeUK

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