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Invasive mussels induce community changes by increasing habitat complexity

  • HABITAT COMPLEXITY
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Abstract

Habitat complexity is among the most important factors affecting the diversity, structure, and density of natural communities. The invasive byssate bivalves zebra mussel (Dreissena polymorpha (Pallas, 1771)) and golden mussel (Limnoperna fortunei (Dunker, 1857)) are sessile suspension feeders that form aggregations (druses), physically changing sediments and increasing habitat complexity, and providing shelter and food for other benthic organisms. In this study, we explored the impact of the change in habitat complexity on benthic community created by druses of L. fortunei and D. polymorpha, formed on various sediments. D. polymorpha was studied in Europe (Naroch Lake, Belarus) and in North America (Glen Lake and Lower Nashotah Lake, USA), and L. fortunei was studied in South America (Río Tercero Reservoir, Argentina). Druses of D. polymorpha or L. fortunei and samples of bare nearby sediment (without druses of exotic mussels) were collected at each sampling site. We found significant changes in species richness, density, biomass, taxonomic, and trophic structure of communities formed in druses compared to the nearby bare sediments. Community taxonomic richness increased threefold, and density increased sevenfold with increasing complexity of habitat from sand to druse. The feeding functional group approach indicated that the impact of increased complexity was reinforced by an increase in food supply in D. polymorpha and L. fortunei druses. Along with increasing species richness and densities, byssate bivalves homogenized benthic communities.

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References

  • Afanasiev, S. A. & A. A. Protasov, 1987. Features of the population of Dreissena in the periphyton communities in the cooling reservoir of a nuclear power station. Hydrobiological Journal 23: 44–51.

    Google Scholar 

  • Almany, G. R., 2004. Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106: 275–284.

    Article  Google Scholar 

  • Beekey, M. A., D. J. McCabe & J. E. Marsden, 2004. Zebra mussels affect benthic predator foraging success and habitat choice on soft sediments. Oecologia 141: 164–170.

    Article  PubMed  CAS  Google Scholar 

  • Bell, S. S., E. D. McCoy & H. R. Mushinsky, 1991. Habitat Structure: The Physical Arrangement of Objects in Space. Chapman & Hall, London.

    Google Scholar 

  • Bially, A. & H. J. Macisaac, 2000. Fouling mussels (Dreissena spp.) colonize soft sediments in Lake Erie and facilitate benthic invertebrates. Freshwater Biology 43: 85–97.

    Article  Google Scholar 

  • Boltovskoy, D., A. Karatayev, L. Burlakova, D. Cataldo, V. Karatayev, F. Sylvester & A. Mariñelarena, 2009. Significant ecosystem-wide effects of the swiftly spreading invasive freshwater bivalve Limnoperna fortunei. Hydrobiologia 636: 271–284.

    Article  Google Scholar 

  • Botts, P. S. & B. A. Patterson, 1996. Zebra mussel effects on benthic invertebrates: physical or biotic? Journal of the North American Benthological Society 15: 179–184.

    Article  Google Scholar 

  • Bray, J. R. & J. T. Curtis, 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27: 325–349.

    Article  Google Scholar 

  • Burlakova, L. E., A. Y. Karatayev & D. K. Padilla, 2005. Functional changes in benthic freshwater communities after Dreissena polymorpha (Pallas) invasion and consequences for filtration. In Dame, R. F. & S. Olenin (eds), The Comparative Roles of Suspension-Feeders in Ecosystems. Springer, Netherlands: 263–275.

    Chapter  Google Scholar 

  • Buschbaum, C., S. Dittmann, J. S. Hong, I. S. Hwang, M. Strasser, M. Thiel, N. Valdivia, S. P. Yoon & K. Reise, 2009. Mytilid mussels: global habitat engineers in coastal sediments. Helgoland Marine Research 63: 47–58.

    Article  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK: 192 pp.

  • Cobb, S. E. & M. C. Watzin, 2002. Zebra mussel colonies and yellow perch foraging: spatial complexity, refuges, and resource enhancement. Journal of Great Lakes Research 28: 256–263.

    Article  Google Scholar 

  • Dame, R. F., 1993. The role of bivalve filter feeder material fluxes in estuarine ecosystems. In Dame, R. F. (ed.), Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. Springer-Verlag, Berlin.

    Google Scholar 

  • Dame, R. F., 1996. Ecology of Marine Bivalves. An Ecosystem Approach. CRC Marine Science Series, Boca Raton.

    Book  Google Scholar 

  • Dittmann, S., 1990. Mussel beds—amensalism or amelioration for intertidal fauna? Helgoland Marine Research 44: 335–352.

    Google Scholar 

  • Downes, B. J., P. S. Lake, E. S. G. Schreiber & A. Glaister, 2000. Habitat structure, resources and diversity: the separate effects of surface roughness and macroalgae on stream invertebrates. Oecologia 123: 569–581.

    Article  Google Scholar 

  • Fairweather, P. G., 1988. Predation creates haloes of bare space among prey on rocky seashores in New-South-Wales. Australian Journal of Ecology 13: 401–409.

    Article  Google Scholar 

  • Flecker, A. S., 1996. Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77: 1845–1854.

    Article  Google Scholar 

  • Fletcher, W. J. & A. J. Underwood, 1987. Interspecific competition among subtidal limpets: effect of substratum heterogeneity. Ecology 68: 387–400.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Izvekova, E. I., 1975. The nutrition and feeding links of the most abundant species of Chironomid larvae in the Uchinskoe reservoir. Summary of the Candidate Dissertation, Moscow State University, Moscow, USSR.

  • Jones, C. G., J. H. Lawton & M. Shachak, 1994. Organisms as ecosystem engineers. Oikos 69: 373–386.

    Article  Google Scholar 

  • Jones, C. G., J. H. Lawton & M. Shachak, 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957.

    Article  Google Scholar 

  • Karatayev, A. Y. & L. E. Burlakova, 1992. Changes in tropic structure of macrozoobenthos of an eutrophic lake, after invasion of Dreissena polymorpha. Biologiya Vnutrennikh Vod 93: 67–71.

    Google Scholar 

  • Karatayev, A. Y. & L. E. Burlakova, 1995. The role of Dreissena in lake ecosystems. Russian Journal of Ecology 26: 207–211.

    Google Scholar 

  • Karatayev, A. Y. & V. P. Lyakhnovich, 1990. Effect of Dreissena polymorpha Pallas on benthic crustaceans (Gammarus lacustris Sars, Pallasea quadrispinosa Sars and Asellus aquaticus L.) in Lukomskoe Lake. In Khmeleva, N. N., et al. (eds), Species Within Their Range: Biology, Ecology and Productivity of Aquatic Invertebrates. Navuka i Tekhnika Press, Minsk: 123–125.

    Google Scholar 

  • Karatayev, A. Y., G. M. Tishchikov & I. V. Karatayeva, 1983. Dreissena polymorpha Pallas as a specific community of benthic animals. Biologiya vnutrennikh vod 61: 18–21.

    Google Scholar 

  • Karatayev, A. Y., V. P. Lyakhnovich, S. A. Afanasev, L. E. Burlakova, V. P. Zakutski, S. M. Lyakhov, M. P. Miroshnichenko, T. G. Moroz, M. Y. Nekrasova, S. P. Nechvalenko, I. A. Skalskaya, T. G. Kharchenko & A. A. Protasov, 1994. The place of species in the ecosystem. In Starobogatov, J. I. (ed.), Freshwater Zebra Mussel Dreissena polymorpha (Pall.) (Bivalvia, Dreissenidae). Systematics, Ecology, Practical Meaning. Nauka Press, Moscow: 180–195.

    Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 1997. The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in Eastern Europe. Journal of Shellfish Research 16: 187–203.

    Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 2002. Impacts of zebra mussels on aquatic communities and their role as ecosystem engineers. In Leppakoski, E., S. Gollach & S. Olenin (eds), Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Kluwer Academic Publishers, Dordreicht.

    Google Scholar 

  • Karatayev, A. Y., D. Boltovskoy, D. K. Padilla & L. E. Burlakova, 2007a. The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. Journal of Shellfish Research 26: 205–213.

    Article  Google Scholar 

  • Karatayev, A. Y., D. K. Padilla, D. Minchin, D. Boltovskoy & L. E. Burlakova, 2007b. Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Biological Invasions 9: 161–180.

    Article  Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova, V. A. Karatayev & D. Boltovskoy, 2010. Limnoperna fortunei vs. Dreissena polymorpha: population densities and benthic community impacts of two invasive freshwater bivalves. Journal of Shellfish Research 29(4): 975–984.

    Article  Google Scholar 

  • Kenkel, N. C. & L. Orlóci, 1986. Applying metric and nonmetric multidimensional scaling to ecological studies: some new results. Ecology 67: 919–928.

    Article  Google Scholar 

  • Kostylev, V. E., J. Erlandsson, M. Y. Ming & G. A. Williams, 2005. The relative importance of habitat complexity and surface area in assessing biodiversity: fractal application on rocky shores. Ecological Complexity 2: 272–286.

    Article  Google Scholar 

  • Lancaster, J. & A. Mole, 1999. Interactive effects of near-bed flow and substratum texture on the microdistribution of lotic macroinvertebrates. Archiv für Hydrobiologie 146: 83–100.

    Google Scholar 

  • Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier, Amsterdam.

    Google Scholar 

  • Levin, S. A., 1992. The problem of pattern and scale in ecology. Ecology 73: 1943–1967.

    Article  Google Scholar 

  • Lohner, R., V. Sigler, C. Mayer & C. Balogh, 2007. A comparison of the benthic bacterial communities within and surrounding Dreissena clusters in lakes. Microbial Ecology 54: 469–477.

    Article  PubMed  Google Scholar 

  • Lvova-Kachanova, A. A. & E. I. Izvekova, 1978. On Dreissena and chironomids from Uchinskoe Reservoir. In Dunaeva, T. N., et al. (eds), Plant and Animal Life in Moscow and Its Environments. Moscow University Press, Moscow: 119–121.

    Google Scholar 

  • Makarevich, T. A., S. E. Mastitsky & Y. V. Savich, 2008. Phytoperiphyton on the shells of Dreissena polymorpha (Pallas) in Lake Naroch. Aquatic Invasions 3: 283–295.

    Article  Google Scholar 

  • Matias, M. G., A. J. Underwood, D. F. Hochuli & R. A. Coleman, 2010. Independent effects of patch size and structural complexity on diversity of benthic macroinvertebrates. Ecology 91: 1908–1915.

    Article  PubMed  Google Scholar 

  • Mayer, C. M., L. G. Rudstam, E. L. Mills, S. G. Cardiff & C. A. Bloom, 2001. Zebra mussels (Dreissena polymorpha), habitat alteration, and yellow perch (Perca flavescens) foraging: system-wide effects and behavioural mechanisms. Canadian Journal of Fisheries and Aquatic Sciences 58: 2459–2467.

    Article  Google Scholar 

  • Merritt, R. W. & K. W. Cummins, 1996. Aquatic Insects of North America. Kendall/Hunt Publ. Co., Dubuque.

    Google Scholar 

  • Merritt, R. W., K. W. Cummins & T. M. Burton, 1984. The role of aquatic insects in the processing and cycling of nutrients. In Resh, V. H. & D. M. Rosenberg (eds), The Ecology of Aquatic Insects. Praeger Scientific, New York.

    Google Scholar 

  • Monakov, A. V., 1998. Feeding of Freshwater Invertebrates. A. N. Severtsov Institute of Ecological and Evolutionary Problems, Russian Academy of Sciences, Moscow, Russia: 318 pp.

  • Monakov, A. V., 2003. Feeding of Freshwater Invertebrates. Kenobi Productions, Ghent: 400 pp.

  • Mörtl, M. & K.-O. Rothhaupt, 2003. Effects of adult Dreissena polymorpha on settling juveniles and associated macroinvertebrates. International Review of Hydrobiology 88: 561–569.

    Article  Google Scholar 

  • Norkko, J., J. E. Hewitt & S. F. Thrush, 2006. Effects of increased sedimentation on the physiology of two estuarine soft-sediment bivalves, Austrovenus stutchburyi and Paphies australis. Journal of Experimental Marine Biology and Ecology 333: 12–26.

    Article  CAS  Google Scholar 

  • Oliveira, M. D., S. K. Hamilton & C. M. Jacobi, 2010. Forecasting the expansion of the invasive golden mussel Limnoperna fortunei in Brazilian and North American rivers based on its occurrence in the Paraguay River and Pantanal wetland of Brazil. Aquatic Invasions 5(1): 59–73.

    Article  Google Scholar 

  • Pianka, E. R., 1988. Evolutionary Ecology. Harper and Row, New York: 356 pp.

  • Radziejewska, T., C. Fenske, B. Wawrzyniak-Wydrowska, P. Riel, A. Wozniczka & P. Gruszka, 2009. The zebra mussel (Dreissena polymorpha) and the benthic community in a coastal Baltic lagoon: another example of enhancement? Marine Ecology: An Evolutionary Perspective 30: 138–150.

    Article  Google Scholar 

  • Rahbek, C. & G. R. Graves, 2001. Multiscale assessment of patterns of avian species richness. Proceedings of the National Academy of Sciences of the United States of America 98: 4534–4539.

    Article  PubMed  CAS  Google Scholar 

  • Ricciardi, A., 1998. Global range expansion of the Asian mussel Limnoperna fortunei (Mytilidae): another fouling threat to freshwater systems. Biofouling 13: 97–106.

    Article  Google Scholar 

  • Ricciardi, A., F. G. Whoriskey & J. B. Rasmussen, 1997. The role of the zebra mussel (Dreissena polymorpha) in structuring macroinvertebrate communities of hard substrata. Canadian Journal of Fisheries and Aquatic Sciences 54: 2596–2608.

    Google Scholar 

  • Ritchie, M. E. & H. Olff, 1999. Spatial scaling laws yield a synthetic theory of biodiversity. Nature 400: 557–560.

    Article  PubMed  CAS  Google Scholar 

  • Robinson, T. B. & C. L. Griffiths, 2002. Invasion of Langebaan Lagoon, South Africa, by Mytilus galloprovincialis—effects on natural communities. African Zoology 37: 151–158.

    Google Scholar 

  • Robson, B. J., 1996. Habitat architecture and trophic interaction strength in a river: Riffle-scale effects. Oecologia 107: 411–420.

    Article  Google Scholar 

  • Ruesink, J. L., H. S. Lenihan, A. C. Trimble, K. W. Heiman, F. Micheli, J. E. Byers & M. C. Kay, 2005. Introduction of non-native oysters: ecosystem effects and restoration implications. Annual Review of Ecology, Evolution & Systematics 36(1): 643–689.

    Article  Google Scholar 

  • Schluter, D. & R. E. Ricklefs, 1993. Species diversity: an introduction to the problem. In Ricklefs, R. E. & D. Schluter (eds), Species Diversity in Ecological Communities: Historical and Geographical Perspectives. The University of Chicago Press, Chicago: 1–12.

    Google Scholar 

  • Schoener, T. W., 1974. Resource partitioning in ecological communities. Science 185: 27–39.

    Article  PubMed  CAS  Google Scholar 

  • Sokolova, N. Y., E. I. Izvekova, A. A. Lvova & M. I. Sakharova, 1980a. Structure, distribution and seasonal dynamics of benthic densities and biomass. Trudy Vsesoyuznogo Gidrobiologicheskogo Obshchestva 23: 7–23.

    Google Scholar 

  • Sokolova, N. Y., E. I. Izvekova, A. A. Lvova & M. I. Sakharova, 1980b. The ecology of mass species of bottom invertebrates. Trudy Vsesoyuznogo Gidrobiologicheskogo Obshchestva 23: 39–131.

    Google Scholar 

  • Sousa, R., C. Antunes & L. Guilhermino, 2007. Species composition and monthly variation of the Molluscan fauna in the freshwater subtidal area of the River Minho estuary. Estuarine Coastal & Shelf Science 75(1/2): 90–100.

    Article  Google Scholar 

  • Sousa, R., J. L. Gutierrez & D. C. Aldridge, 2009. Non-indigenous invasive bivalves as ecosystem engineers. Biological Invasions 11: 2367–2385.

    Article  Google Scholar 

  • Spooner, D. E. & C. C. Vaughn, 2006. Context-dependent effects of freshwater mussels on stream benthic communities. Freshwater Biology 51: 1016–1024.

    Article  CAS  Google Scholar 

  • Statzner, B., E. Fievet, J. Y. Champagne, R. Morel & E. Herouin, 2000. Crayfish as geomorphic agents and ecosystem engineers: Biological behavior affects sand and gravel erosion in experimental streams. Limnology & Oceanography 45: 1030–1040.

    Article  Google Scholar 

  • Stewart, T. W., J. G. Miner & R. L. Lowe, 1998a. Quantifying mechanisms for zebra mussel effects on benthic macroinvertebrates: Organic matter production and shell-generated habitat. Journal of the North American Benthological Society 17: 81–94.

    Article  Google Scholar 

  • Stewart, T. W., J. G. Miner & R. L. Lowe, 1998b. An experimental analysis of crayfish (Orconectes rusticus) effects on a Dreissena-dominated benthic macroinvertebrate community in western Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 55: 1043–1050.

    Article  Google Scholar 

  • Stewart, T. W., J. C. Gafford, J. G. Miner & R. L. Lowe, 1999. Dreissena-shell habitat and antipredator behavior: combined effects on survivorship of snails co-occurring with molluscivorous fish. Journal of the North American Benthological Society 18: 274–283.

    Article  Google Scholar 

  • Strayer, D. L., 1999. Use of flow refuges by unionid mussels in rivers. Journal of North American Benthological Society 18: 468–476.

    Article  Google Scholar 

  • Taniguchi, H. & M. Tokeshi, 2004. Effects of habitat complexity on benthic assemblages in a variable environment. Freshwater Biology 49: 1164–1178.

    Article  Google Scholar 

  • Thorp, J. H. & A. P. Covich, 2001. Ecology and Classification of North American Freshwater Invertebrates. Academic Press, San Diego: 950 pp.

  • Ward, J. M. & A. Ricciardi, 2007. Impacts of Dreissena invasions on benthic macroinvertebrate communities: a meta-analysis. Diversity and Distributions 13: 155–165.

    Article  Google Scholar 

  • Warfe, D. M., L. A. Barmuta & S. Wotherspoon, 2008. Quantifying habitat structure: surface convolution and living space for species in complex environments. Oikos 117: 1764–1773.

    Article  Google Scholar 

  • Wotton, R. S., B. Malmqvist, T. Muotka & K. Larsson, 1998. Fecal pellets from a dense aggregation of suspension-feeders in a stream: An example of ecosystem engineering. Limnology & Oceanography 43: 719–725.

    Article  Google Scholar 

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Acknowledgments

The research was partly supported by grant number 45613 from Wisconsin Department of Natural Resources and University of Wisconsin at Madison. We are thankful to Dr. Demetrio Boltovskoy (Universidad de Buenos Aires, Argentina) for field support in Argentina. We appreciate the help of the Director of the Naroch Biological Station (Belarusian State University) Dr. T. V. Zhukova, and the staff of the Station for assistance in the field in Belarus. We are thankful to Rhonda Mood for identification of Glen Lake samples. We would like to thank Richard C. Lathrop and Heidi Bunk (Wisconsin Department of Natural Resources), James F. Kitchell, M. Jake Vander Zanden, and other faculty and staff of the Center for Limnology (University of Wisconsin-Madison) for providing space, lab and field support in Wisconsin, and Denise Mayer (New York State Museum Field Research Laboratory) for field assistance in New York. Research Foundation of SUNY provided support for LEB during manuscript preparation.

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  1. Great Lakes Center, Buffalo State College, 1300 Elmwood Ave., Buffalo, NY, USA

    Lyubov E. Burlakova & Alexander Y. Karatayev

  2. The Research Foundation of The State University of New York, Buffalo State College, Office of Sponsored Programs, 1300 Elmwood Avenue, Buffalo, NY, USA

    Lyubov E. Burlakova

  3. University Honors College, State University of New York at Buffalo, 106 Capen Hall, Buffalo, NY, USA

    Vadim A. Karatayev

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  1. Lyubov E. Burlakova
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Guest editors: K. E. Kovalenko & S. M. Thomaz / The importance of habitat complexity in waterscapes

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Burlakova, L.E., Karatayev, A.Y. & Karatayev, V.A. Invasive mussels induce community changes by increasing habitat complexity. Hydrobiologia 685, 121–134 (2012). https://doi.org/10.1007/s10750-011-0791-4

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