Abstract
The spread of alien molluscs is a serious threat to native biodiversity in fresh waters. Alien freshwater molluscs may deplete the resources of native species and alter the physical structure of the habitat through their shell mass. These changes might have both positive and negative effects on native community members. We investigated the native macroinvertebrate community in relation to the densities of four alien mollusc species (Corbicula fluminea, Dreissena polymorpha, Potamopyrgus antipodarum and Lithoglyphus naticoides) in a sandy flat of Lake Neuchâtel, Switzerland. The habitat examined was dominated by these alien mollusc species. The abundance of the alien molluscs did not directly impact the native community assembly. However, C. fluminea and D. polymorpha influenced the composition and diversity of native macroinvertebrates by transforming the sandy substratum into a partly hard substratum habitat. Substantial differences in community composition between shallow (<3.5 m) and (≥5 m) deep sites were recorded. At shallow sites, the abundance of D. polymorpha was significantly reduced as a result of depth-selective feeding of ducks. A controlled shell decay study revealed that shells of alien molluscs (C. fluminea, D. polymorpha) persist for a longer period in the sediment than those of native molluscs. Consequently, shells of alien molluscs have a long-lasting impact by modifying the sandy habitat. This form of ecosystem engineering favours the occurrence of several native taxa, but is disadvantageous for other taxa with specific habitat requirements, and thus can be regarded as an indirect impact of competition.
Similar content being viewed by others
References
Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
Arndt, E., S. Fiedler & D. Bohme, 2009. Effects of invasive benthic macroinvertebrates on assessment methods of the EU Water Frame Work Directive. Hydrobiologia 635: 309–320.
Baur, B. & S. Schmidlin, 2007. Effects of invasive non-native species on the native biodiversity in the river Rhine. In Nentwig, W. (ed.), Biological Invasions. Springer Verlag, Berlin: 257–273.
Botts, P. S., B. A. Patterson & D. W. Schloesser, 1996. Zebra mussel effects on benthic invertebrates: physical or biotic? Journal of the North American Benthological Society 15: 179–184.
Carter, J. L. & V. H. Resh, 2001. After site selection and before data analysis: sampling sorting and laboratory procedures used in stream benthic macroinvertebrate monitoring programs by USA state agencies. Journal of the North American Benthological Society 20: 658–682.
Chauvaud, L., J. K. Thompson, J. E. Cloern & G. Thouzeau, 2003. Clams as CO2 generators: The Potamocorbula amurensis example in San Francisco Bay. Limnology and Oceanography 48: 2086–2092.
Clarke, K. R., 1993. Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.
Crozet, B., J. C. Pedroli & C. Vaucher, 1980. First findings of Potamopyrgus jenkinsi (Smith) (Mollusca, Hydrobiidae) in western Switzerland. Revue Suisse de Zoologie 87: 807–811.
CSCF, 2010. Presence of Lithoglyphus naticoides. CSCF, Centre Suisse de Cartographie de la Faune, Switzerland [available on internet at http://lepus.unine.ch/carto].
de Leeuw, J. J., M. R. van Eerden & G. H. Visser, 1999. Wintering tufted ducks Aythya fuligula diving for zebra mussels Dreissena polymorpha balance feeding costs within narrow margins of their energy budget. Journal of Avian Biology 30: 182–192.
Diamond, J. M., 1975. Assembly of species communities. In Cody, M. L. & J. M. Diamond (eds), Ecology and Evolution of Communities. Harvard University Press, Cambridge: 342–444.
Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. I. Kawabata, D. J. Knowler, C. Leveque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81: 163–182.
Duelli, P., 1994. Rote Liste der gefährdeten Tierarten in der Schweiz. Bundesamt für Umwelt, Wald und Landschaft, BUWAL, Bern.
Dufrene, M. & P. Legendre, 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.
Gergs, R. & K.-O. Rothhaupt, 2008. Effects of zebra mussels on a native amphipod and the invasive Dikerogammarus villosus: the influence of biodeposition and structural complexity. Journal of the North American Benthological Society 27: 541–548.
Glöer, P., 2002. Süsswassergastropoden Nord-und Mitteleuropas. Bestimmungsschlüssel, Lebensweise, Verbreitung. ConchBooks, Hackenheim.
Glöer, P. & C. Meier-Brook, 1998. Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtungen, Hamburg.
Gonzalez, A., A. Lambert & A. Ricciardi, 2008. When does ecosystem engineering cause invasion and species replacement? Oikos 117: 1247–1257.
Gotelli, N. J., 2000. Null model analysis of species co-occurrence patterns. Ecology 81: 2606–2621.
Gotelli, N. J. & G. R. Graves, 1996. Null Models in Ecology. Smithsonian Institute Press, Washington.
Gotelli, N. J. & D. J. McCabe, 2002. Species co-occurrence: a meta-analysis of J. M. Diamond’s assembly rules model. Ecology 83: 2091–2096.
Grabow, K., 2000. Farbatlas Süsswasserfauna Wirbellose. Eugen Ulmer Verlag, Stuttgart.
Green, R. H., 1980. Role of a unionid clam population in the calcium budget of a small arctic lake. Canadian Journal of Fisheries and Aquatic Sciences 37: 219–224.
Gutierrez, J. L., C. G. Jones, D. L. Strayer & O. O. Iribarne, 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101: 79–90.
Hakenkamp, C. C. & M. A. Palmer, 1999. Introduced bivalves in freshwater ecosystems: the impact of Corbicula on organic matter dynamics in a sandy stream. Oecologia 119: 445–451.
Higgins, S. N. & M. J. Vander Zanden, 2010. What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological Monographs 80: 179–196.
Jones, C. G., J. H. Lawton & M. Shachak, 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957.
Karatayev, A. Y., L. E. Burlakova, T. Kesterson & D. K. Padilla, 2003. Dominance of the Asiatic clam, Corbicula fluminea (Muller), in the benthic community of a reservoir. Journal of Shellfish Research 22: 487–493.
Keller, V. & M. Burkhardt, 2010. Monitoring überwinternde Wasservögel: Ergebnisse der Wasservogelzählungen 2008/09. Schweizerische Vogelwarte, Sempach.
Lechthaler, W. & W. Stockinger, 2005. Trichoptera—Key to Larvae from Central Europe (Electronic Keys & Reference Collections). EUTAXA, Austria.
Leff, L. G., J. L. Burch & J. V. McArthur, 1990. Spatial distribution, seston removal, and potential competitive interactions of the bivalves Corbicula fluminea and Elliptio complanata, in a coastal plain stream. Freshwater Biology 24: 409–416.
Lewin, I. & A. Smolinski, 2006. Rare and vulnerable species in the mollusc communities in the mining subsidence reservoirs of an industrial area (the Katowicka Upland, Upper Silesia, Southern Poland). Limnologica 36: 181–191.
McArdle, B. H. & M. J. Anderson, 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290–297.
Mitchell, M. J., E. L. Mills, N. Idrisi & R. Michener, 1996. Stable isotopes of nitrogen and carbon in an aquatic food web recently invaded by Dreissena polymorpha (Pallas). Canadian Journal of Fisheries and Aquatic Sciences 53: 1445–1450.
Mooney, H. A., R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei & J. K. Waage (eds), 2005. Invasive Alien Species. A New Synthesis. SCOPE 63. Island Press, Washington.
Mörtl, M. & K.-O. Rothhaupt, 2003. Effects of adult Dreissena polymorpha on settling juveniles and associated macroinvertebrates. International Review of Hydrobiology 88: 561–569.
Müller, O. & B. Baur, 2011. Survival of the invasive clam Corbicula fluminea (Müller) in response to winter water temperature. Malacologia 53: 367–371.
Nalepa, T. F., D. L. Fanslow & S. A. Pothoven, 2010. Recent changes in density, biomass, recruitment, size structure, and nutritional state of Dreissena populations in southern Lake Michigan. Journal of Great Lakes Research 36: 5–19.
Nentwig, W. (ed.), 2007. Biological Invasions. Ecological Studies 193. Springer Verlag, Berlin, Germany.
Neubert, E. & H. Nesemann, 1999. Annelida, Clitellata: Branchiobdellida, Acanthobdellea, Hirudinae. Spektrum Akademischer Verlag, Heidelberg.
Oksanen, J., R. Kindt, P. Lengendre, B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2009. Vegan: Community Ecology Package.
Ordonez, A., I. J. Wright & H. Olff, 2010. Functional differences between native and alien species: a global-scale comparison. Functional Ecology 24: 1353–1361.
Pedroli, J.-C., 1978. Note préliminaire sur la croissance de la moule zébrée. Dreissena polymorpha Pallas dans le lac de Neuchâtel. Bulletin de la société neuchâteloise des sciences naturelles 101: 45–52.
Phelps, H. L., 1994. The Asiatic clam (Corbicula fluminea): Invasion and system-level ecological change in the Potomac River Estuary near Washington, DC. Estuaries 17: 614–621.
Podani, J., 2000. Introduction into the Exploration of Multivariate Biological Data. Backhuys Publishers, Leiden.
R Development Core Team, 2009. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org].
Rahel, F. J., 2002. Homogenisation of freshwater faunas. Annual Review of Ecology, Evolution and Systematics 33: 291–315.
Ricciardi, A. & H. J. MacIsaac, 2000. Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology and Evolution 15: 62–65.
Roberts, D. W., 2010. labdsv: Ordination and Multivariate Analysis for Ecology. R Package Version 1.4-1 [available on internet at http://CRAN.R-project.org/package=labdsv].
Sala, O. E., F. S. Chapin, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sanwald, L. F. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker & D. H. Wall, 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–1774.
Sanders, N. J., N. J. Gotelli, N. E. Heller & D. M. Gordon, 2003. Community disassembly by an invasive species. Proceedings of the National Academy of Sciences of the United States of America 100: 2474–2477.
Schmidlin, S. & B. Baur, 2007. Distribution and substrate preference of the invasive clam Corbicula fluminea in the river Rhine in the region of Basel (Switzerland, Germany, France). Aquatic Sciences 69: 153–161.
Schwab, H., 1995. Süsswassertiere—Ein ökologisches Bestimmungsbuch. Klett Verlag, Stuttgart.
SCPE Neuchâtel, 2007–2009. Data on Water Chemistry. Service de la protéction de l’environnement [available on internet at www.les3lacs.ch].
Scrucca, L., 2004. qcc: An R Package for Quality Control Charting and Statistical Process Control. R News 4: 11–17.
Sollberger, H., 1974. Le lac de Neuchâtel (Suisse). Ses eaux, ses sédiments, ses courants sous-lacustres. Ph.D. Thesis, University of Neuchâtel.
Sousa, R., S. C. Dias, L. Guilhermino & C. Antunes, 2008a. Minho River tidal freshwater wetlands: threats to faunal biodiversity. Aquatic Biology 3: 237–350.
Sousa, R., M. Rufino, M. Gaspar, C. Antunes & L. Guilhermino, 2008b. Abiotic impacts on spatial and temporal distribution of Corbicula fluminea (Muller, 1774) in the River Minho Estuary, Portugal. Aquatic Conservation-Marine and Freshwater Ecosystems 18: 98–110.
Sousa, R., J. L. Gutierrez & D. C. Aldridge, 2009. Non-indigenous invasive bivalves as ecosystem engineers. Biological Invasions 11: 2367–2385.
Statzner, B., N. Bonada & S. Doledec, 2008. Biological attributes discriminating invasive from native European stream macroinvertebrates. Biological Invasions 10: 517–530.
Strayer, D. L., 1999. Effects of alien species on freshwater mollusks in North America. Journal of the North American Benthological Society 18: 74–98.
Strayer, D. L., 2010. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55: 152–174.
Strayer, D. L. & H. M. Malcom, 2007. Shell decay rates of native and alien freshwater bivalves and implication for habitat engineering. Freshwater Biology 52: 1611–1617.
Strzelec, M., 2000. The changes in the freshwater snail (Gastropoda) fauna of dam reservoir Gzel (Upper Silesia) and their causes. Acta Universitatis Lodziensis, Folia Limnologica 7: 173–180.
Studemann, D., P. Landolt, M. Sartori, D. Hefti & I. Tomka, 1992. Ephemeroptera. In: Insecta Helvetica—Fauna, Schweizerische Entomologische Gesellschaft 9: 1–173.
Sylvester, F., D. Boltovskoy & D. Cataldo, 2007. The invasive bivalve Limnoperna fortunei enhances benthic invertebrate densities in South American floodplain rivers. Hydrobiologia 589: 15–27.
Tachet, H., P. Richoux, M. Bournaud & P. Usseglio-Polatera, 2006. Invertébrés d’eau douce: systématique, biologie, écologie. CNRS éditions, Paris.
Tittizer, T., F. Schöll, M. Banning, A. Haybach & M. Schleuter, 2000. Aquatische Neozoen im Makrozoobenthos der Binnenwasserstrassen Deutschlands. Lauterbornia 39: 1–172.
Townsend, C. R. & A. G. Hildrew, 1994. Species traits in relation to a habitat templet for river systems. Freshwater Biology 31: 265–275.
Ulrich, W., 2004. Species co-occurrences and neutral models: reassessing J. M. Diamond’s assembly rules. Oikos 107: 603–609.
Ulrich, W., 2006. CoOccurrence—A FORTRAN Program for Species Co-Occurrence Analysis [available on internet at http://www.uni.torun.pl/~ulrichw].
Ulrich, W. & N. J. Gotelli, 2007. Disentangling community patterns of nestedness and species co-occurrence. Oikos 116: 2053–2061.
Ulrich, W. & N. J. Gotelli, 2010. Null model analysis of species associations using abundance data. Ecology 91: 3384–3397.
Waringer, J., 1987. Spatial distribution of Trichoptera larvae in the sediment of an Austrian mountain brook. Freshwater Biology 18: 469–482.
Werner, S. & K.-O. Rothhaupt, 2007. Effects of the invasive bivalve Corbicula fluminea on settling juveniles and other benthic taxa. Journal of the North American Benthological Society 26: 673–680.
Werner, S. & K.-O. Rothhaupt, 2008. Effects of the invasive Asian clam Corbicula fluminea on benthic macroinvertebrate taxa in laboratory experiments. Fundamental and Applied Limnology 173: 145–152.
Werner, S., M. Mortl, H. G. Bauer & K. O. Rothhaupt, 2005. Strong impact of wintering waterbirds on zebra mussel (Dreissena polymorpha) populations at Lake Constance, Germany. Freshwater Biology 50: 1412–1426.
Wetherill, G. B. & D. W. Brown, 1991. Statistical Process Control. Chapman and Hall, New York: 216–218.
Wirth, A., D. Schmera & B. Baur, 2010. Native and alien macroinvertebrate richness in a remnant of the former river Rhine: a source for recolonisation of restored habitats? Hydrobiologia 652: 89–100.
Zapala, M. A. & N. J. Schork, 2006. Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proceedings of the National Academy of Sciences of the United States of America 103: 19430–19435.
Acknowledgments
We thank all SCUBA-divers and volunteers for their help in the field, J.-D. Wicky and G. Bossy of the Canton Fribourg for permitting the survey close to a nature reserve, A. Wagner for determining the Ephemeroptera, P. Stucki, H. Vicentini and B. Lods-Crozet for taxonomical discussions, A. Gander of the nature reserve Grande Cariçaie and V. Keller of the Swiss Ornithological Institute Sempach for information. We are grateful to A. Baur, B. Oertli and two anonymous reviewers for comments on the manuscript and the Freie Akademische Gesellschaft Basel for partial funding.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Koen Martens
Rights and permissions
About this article
Cite this article
Schmidlin, S., Schmera, D. & Baur, B. Alien molluscs affect the composition and diversity of native macroinvertebrates in a sandy flat of Lake Neuchâtel, Switzerland. Hydrobiologia 679, 233–249 (2012). https://doi.org/10.1007/s10750-011-0889-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-011-0889-8