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The invasive freshwater bivalve Limnoperna fortunei in South America: multiannual changes in its predation and effects on associated benthic invertebrates

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Abstract

The invasive golden mussel Limnoperna fortunei is known to strongly affect benthic communities in South American freshwaters, but the evolution of these effects after the early invasion stages is poorly understood. Using predator exclusion (covered with 15- and 40-mm meshes) and inclusion (unprotected) substrates, we investigated the interaction between golden mussels and benthic invertebrate communities at different levels of exposure to predators in the Paraná River delta. Colonization of the substrates was largely dominated by the mussels. Oligochaeta, Nematoda, and Hirudinea were the most abundant accompanying groups, while Rotifera, Tardigrada, Copepoda, Cladocera, Chironomidae, Gastropoda, Hydracarina, Amphipoda, and nauplii appeared sporadically. Regardless of their different trophic modes and functional attributes, the numbers and biomass of associated invertebrates were not only enhanced by protection against predators, but also by the presence of mussel colonies. Enhancement of invertebrate densities associated with mussel colonies was higher on unprotected than protected substrates, suggesting that invertebrate facilitation increases with increasing predation pressure. Comparisons with a similar study carried out a decade earlier suggest that, after two decades of invasion, the reproductive potential of the mussel, the predation pressure on its colonies, and its facilitation effects on other invertebrates have increased in the Paraná River delta.

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References

  • Baba, T. & M. Urabe, 2015. Parasites of Limnoperna fortunei. In Boltovskoy, D. (ed.), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 55–65.

    Google Scholar 

  • Barbosa, N. P. U., F. A. Silva, M. D. de Oliveira, M. A. dos Santos Neto, M. D. de Carvalho & A. V. Cardoso, 2016. Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae): first record in the São Francisco River basin, Brazil. Check List 12: 1846.

    Article  Google Scholar 

  • Benke, A. C., A. D. Huryn, L. A. Smock & J. B. Wallace, 1999. Length–mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. Journal of the North American Benthological Society 18: 308–343.

    Article  Google Scholar 

  • Bertness, M. D. & R. Callaway, 1994. Positive interactions in communities. Trends in Ecology and Evolution 9: 191–193.

    Article  PubMed  CAS  Google Scholar 

  • Boltovskoy, D., 2015. Ecology and environmental impact of Limnoperna fortunei: introduction. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 147–151.

    Google Scholar 

  • Boltovskoy, D. & N. Correa, 2015. Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746: 81–95.

    Article  CAS  Google Scholar 

  • Boltovskoy, D., A. Y. Karatayev, L. E. 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 

  • Bottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-Ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review o some problems in zooplankton production studies. Norwegian Journal of Zoology 24: 419–456.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bruno, J. F. & M. D. Bertness, 2001. Habitat modification and facilitation in benthic marine communities. In Bertness, M. D., S. D. Gaines & M. E. Hay (eds), Marine Community Ecology. Sinauer Associates, Sunderland: 201–218.

    Google Scholar 

  • Bruno, J. F., J. J. Stachowicz & M. D. Bertness, 2003. Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution 18: 119–125.

    Article  Google Scholar 

  • Bujes, C. S., I. Ely & L. Verrastro, 2007. Trachemys dorbigni (Brazilian Slider) diet. Herpetological Review 38: 335.

    Google Scholar 

  • Burlakova, L. E., A. Y. Karatayev & D. K. Padilla, 2006. Changes in the distribution and abundance of Dreissena polymorpha within lakes through time. Hydrobiologia 571: 133–146.

    Article  Google Scholar 

  • Carvalho, D. A., P. A. Collins & C. J. De Bonis, 2013. Predation ability of freshwater crabs: age and prey-specific differences in Trichodactylus borellianus (Brachyura: Trichodactylidae). Journal of Freshwater Ecology 28: 573–584.

    Article  Google Scholar 

  • Cataldo, D., 2015. Trophic relationships of Limnoperna fortunei with adult fishes. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 231–248.

    Google Scholar 

  • Cataldo, D., I. Ó. Farrell, E. M. Paolucci, F. Sylvester & D. Boltovskoy, 2012. Impact of the invasive golden mussel (Limnoperna fortunei) on phytoplankton and nutrient cycling. Aquatic Invasions 7: 91–100.

    Article  Google Scholar 

  • Colautti, R. I., A. Ricciardi, I. A. Grigorovich & H. J. MacIsaac, 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters 7: 721–733.

    Article  Google Scholar 

  • Correa, N., P. Sardiña, P. Perepelizin & D. Boltovskoy, 2015. Limnoperna fortunei colonies: structure, distribution and dynamics. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 119–143.

    Google Scholar 

  • Darrigran, G., 2002. Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biological Invasions 4: 145–156.

    Article  Google Scholar 

  • Feller, R. J. & R. M. Warwick, 1988. Energetics. In Higgins, H. P. & H. Thiel (eds), Introduction to the study of meiofauna. Smithsonian Institution Press, Columbia: 181–196.

    Google Scholar 

  • Ito, K., 2015. Colonization and spread of Limnoperna fortunei in Japan. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 321–332.

    Google Scholar 

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

    Article  Google Scholar 

  • Karatayev, A. Y., D. Boltovskoy, L. E. Burlakova & D. K. Padilla, 2015. Parallels and contrasts between Limnoperna fortunei and Dreissena species. In Boltovskoy, D. (ed.), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 261–297.

    Google Scholar 

  • Kluza, D. A. & K. M. McNyset, 2005. Ecological niche modeling of aquatic invasive species. Aquatic Invaders 16: 1–7.

    Google Scholar 

  • Linares, M. S., M. Callisto & J. C. Marques, 2017. Invasive bivalves increase benthic communities complexity in neotropical reservoirs. Ecological Indicators 75: 279–285.

    Article  Google Scholar 

  • Mansur, M. C. D., C. P. Santos, G. Darrigran, I. Heydrich, C. T. Callil & F. R. Cardoso, 2003. Primeiros dados quali-quantitativos do mexilhão-dourado, Limnoperna fortunei (Dunker), no Delta do Jacuí, no Lago Guaíba e na Laguna dos Patos, Rio Grande do Sul, Brasil e alguns aspectos de sua invasão no novo ambiente. Revista Brasileira de Zoologia 20: 75–84.

    Article  Google Scholar 

  • Marçal, S. F., C. T. Callil & R. C. D. Santos, 2015. Trichoptera (Insecta) in water hyacinth roots: evaluation of the influence of exotic mussel and environmental factors. Acta Limnologica Brasiliensia 27: 341–355.

    Article  Google Scholar 

  • McCullagh, P. & J. A. Nelder, 1983. Generalized Linear Models. Chapman and Hall, London.

    Book  Google Scholar 

  • McEwen, G. F., M. W. Johnson & T. R. Folsom, 1954. A statistical analysis of the performance of the Folsom plankton sample splitter, based upon test observations. Archiv fűr Meteorologie, Geophysyk und Klimatologie A7: 502–527.

    Article  Google Scholar 

  • Nakano, D., T. Kobayashi & I. Sakaguchi, 2010. Predation and depth effects on abundance and size distribution of an invasive bivalve, the golden mussel Limnoperna fortunei, in a dam reservoir. Limnology 11: 259–266.

    Article  CAS  Google Scholar 

  • Nalepa, T. F. & D. W. Schloesser (eds), 2014. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton.

    Google Scholar 

  • Oliveira, M. D., S. K. Hamilton, D. F. Calheiros, C. M. Jacobi & R. O. Latini, 2010. Modeling the potential distribution of the invasive golden mussel Limnoperna fortunei in the Upper Paraguay River system using limnological variables. Brazilian Journal of Biology 70: 831–840.

    Article  CAS  Google Scholar 

  • Oliveira, M. D., M. C. S. Campos, E. M. Paolucci, M. C. D. Mansur & S. K. Hamilton, 2015. Colonization and spread of Limnoperna fortunei in South America. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 333–355.

    Google Scholar 

  • Pastorino, G., G. Darrigran, S. M. Martín & L. Lunaschi, 1993. Limnoperna fortunei (Dunker, 1857) (Mytilidae), nuevo bivalvo invasor en aguas del Río de la Plata. Neotropica 39: 101–102.

    Google Scholar 

  • Pimentel, D. (ed) 2002. Biological invasions. In Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species. CRC Press, Boca Raton.

  • Rojas Molina, F. & V. Williner, 2013. First record of the non-indigenous mussel Limnoperna fortunei (Bivalvia, Mytilidae) as an epibiont of the crab Trichodactylus borellianus (Decapoda, Trichodactylidae). Crustaceana 86: 682–692.

    Article  Google Scholar 

  • Sardiña, P., D. Cataldo & D. Boltovskoy, 2008. The effects of the invasive mussel, Limnoperna fortunei, on associated fauna in South American freshwaters: importance of physical structure and food supply. Fundamental and Applied Limnology/Archiv für Hydrobiologie 173: 135–144.

    Article  Google Scholar 

  • Sardiña, P., E. Chaves & M. Marchese, 2011. Benthic community responses to invasion by the golden mussel, Limnoperna fortunei Dunker: biotic homogenization vs environmental driving forces. Journal of the North American Benthological Society 30: 1009–1023.

    Article  Google Scholar 

  • Simberloff, D., 2003. Confronting introduced species: a form of xenophobia? Biological Invasions 5: 179–192.

    Article  Google Scholar 

  • Smock, L. A., 1980. Relationships between body size and biomass of aquatic insects. Freshwater Biology 10: 375–383.

    Article  Google Scholar 

  • Spaccesi, F. G. & A. R. Capitulo, 2012. Benthic communities on hard substrates covered by Limnoperna fortunei Dunker (Bivalvia, Mytilidae) at an estuarine beach (Río de la Plata, Argentina). Journal of Limnology 71: 144–153.

    Article  Google Scholar 

  • Stanczykowska, A., 1977. Ecology of Dreissena polymorpha (Pall.) (Bivalvia) in lakes. Polskie Archiwum Hydrobiologii 24: 461–530.

    CAS  Google Scholar 

  • Stewart, T. W., J. G. Miner & R. L. Lowe, 1998. 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 

  • Strayer, D. L. & H. M. Malcom, 2006. Long-term demography of a zebra mussel (Dreissena polymorpha) population. Freshwater Biology 51: 117–130.

    Article  Google Scholar 

  • Strayer, D. L. & H. M. Malcom, 2014. Long-term change in the Hudson River´s bivalve populations. In Nalepa, T. F. & D. W. Schloesser (eds), Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton: 71–81.

    Google Scholar 

  • Sylvester, F., 2006. Biología alimentaria y ecología del molusco invasor Limnoperna fortunei (Mytilidae) en el Paraná inferior y Río de la Plata. PhD thesis, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina. 160 p. https://www.opac.bl.fcen.uba.ar. Accessed 5 Mar 2018.

  • Sylvester, F. & P. Sardiña, 2015. Relationships of Limnoperna fortunei with benthic animals. In Boltovskoy, D. (ed), Limnoperna fortunei: The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International Publishing, Cham: 191–210.

    Google Scholar 

  • Sylvester, F., D. Boltovskoy & D. Cataldo, 2007a. Fast response of freshwater consumers to a new trophic resource: predation on the recently introduced Asian bivalve Limnoperna fortunei in the lower Paraná River, South America. Austral Ecology 32: 403–415.

    Article  Google Scholar 

  • Sylvester, F., D. Boltovskoy & D. Cataldo, 2007b. The invasive bivalve Limnoperna fortunei enhances benthic invertebrate densities in South American floodplain rivers. Hydrobiologia 589: 15–27.

    Article  Google Scholar 

  • Torres, M. V., V. Williner & F. Giri, 2012. Size selective predation on an invasive bivalve, Limnoperna fortunei (Mytilidae), by a freshwater crab, Zilchiopsis collastinensis (Trichodactylidae). Journal of Crustacean Biology 32: 698–710.

    Article  Google Scholar 

  • Weber, S. & W. Traunspurger, 2014. Top-down control of a meiobenthic community by two juvenile freshwater fish species. Aquatic Ecology 48: 465–480.

    Article  CAS  Google Scholar 

  • Weber, S. & W. Traunspurger, 2015. The effects of predation by juvenile fish on the meiobenthic community structure in a natural pond. Freshwater Biology 60: 2392–2409.

    Article  Google Scholar 

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Acknowledgements

We thank Mrs. Cintia Cantarini for logistical assistance. Sidinei M. Thomaz and three anonymous reviewers provided very helpful comments on this work. This work was partially financed by grants from the University of Buenos Aires, Argentina [UBA X-020 and 20020100100035] and from the Argentine Agencia Nacional de Promoción Científica y Tecnológica [PICT 2007 1968, PICT 2011 0729, PICT 2012 0070, and PICT 2015 2598] to FS and DB.

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Authors and Affiliations

  1. IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    Daniela Duchini & Demetrio Boltovskoy

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Daniela Duchini, Demetrio Boltovskoy & Francisco Sylvester

  3. Facultad de Ciencias Naturales, Instituto para el Estudio de la Biodiversidad de Invertebrados (IEBI), Universidad Nacional de Salta, Salta, Argentina

    Francisco Sylvester

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  1. Daniela Duchini
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  2. Demetrio Boltovskoy
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  3. Francisco Sylvester
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Correspondence to Francisco Sylvester.

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Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II

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10750_2018_3561_MOESM1_ESM.xlsx

General environmental and sampling data, and results of abundance estimates on all substrates. ESC: Entire substrate colonized by adult mussels; NLM: No large (> 1 mm) mussels present. Note that a few small yet > 1-mm mussels where found in the "no large mussel zone" of some substrates as a result of field procedures (see Materials and Methods in the main text). Supplementary material 1 (XLSX 40 kb)

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Duchini, D., Boltovskoy, D. & Sylvester, F. The invasive freshwater bivalve Limnoperna fortunei in South America: multiannual changes in its predation and effects on associated benthic invertebrates. Hydrobiologia 817, 431–446 (2018). https://doi.org/10.1007/s10750-018-3561-8

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