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Hydrobiologia

, Volume 817, Issue 1, pp 431–446 | Cite as

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

  • Daniela Duchini
  • Demetrio Boltovskoy
  • Francisco Sylvester
INVASIVE SPECIES II

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.

Keywords

Argentina Limnoperna fortunei Benthic invertebrates Facilitation Multiannual changes Predation 

Notes

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.

Supplementary material

10750_2018_3561_MOESM1_ESM.xlsx (41 kb)
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)

References

  1. 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
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Bertness, M. D. & R. Callaway, 1994. Positive interactions in communities. Trends in Ecology and Evolution 9: 191–193.CrossRefPubMedGoogle Scholar
  5. 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
  6. Boltovskoy, D. & N. Correa, 2015. Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746: 81–95.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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
  9. 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.CrossRefGoogle Scholar
  10. 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
  11. Bruno, J. F., J. J. Stachowicz & M. D. Bertness, 2003. Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution 18: 119–125.CrossRefGoogle Scholar
  12. Bujes, C. S., I. Ely & L. Verrastro, 2007. Trachemys dorbigni (Brazilian Slider) diet. Herpetological Review 38: 335.Google Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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
  19. Darrigran, G., 2002. Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biological Invasions 4: 145–156.CrossRefGoogle Scholar
  20. 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
  21. 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
  22. 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.CrossRefGoogle Scholar
  23. 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
  24. Kluza, D. A. & K. M. McNyset, 2005. Ecological niche modeling of aquatic invasive species. Aquatic Invaders 16: 1–7.Google Scholar
  25. Linares, M. S., M. Callisto & J. C. Marques, 2017. Invasive bivalves increase benthic communities complexity in neotropical reservoirs. Ecological Indicators 75: 279–285.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. McCullagh, P. & J. A. Nelder, 1983. Generalized Linear Models. Chapman and Hall, London.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Nalepa, T. F. & D. W. Schloesser (eds), 2014. Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd ed. CRC Press, Boca Raton.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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
  34. 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
  35. Pimentel, D. (ed) 2002. Biological invasions. In Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species. CRC Press, Boca Raton.Google Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. Simberloff, D., 2003. Confronting introduced species: a form of xenophobia? Biological Invasions 5: 179–192.CrossRefGoogle Scholar
  40. Smock, L. A., 1980. Relationships between body size and biomass of aquatic insects. Freshwater Biology 10: 375–383.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Stanczykowska, A., 1977. Ecology of Dreissena polymorpha (Pall.) (Bivalvia) in lakes. Polskie Archiwum Hydrobiologii 24: 461–530.Google Scholar
  43. 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.CrossRefGoogle Scholar
  44. Strayer, D. L. & H. M. Malcom, 2006. Long-term demography of a zebra mussel (Dreissena polymorpha) population. Freshwater Biology 51: 117–130.CrossRefGoogle Scholar
  45. 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
  46. 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.
  47. 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
  48. 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.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. Weber, S. & W. Traunspurger, 2014. Top-down control of a meiobenthic community by two juvenile freshwater fish species. Aquatic Ecology 48: 465–480.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina
  3. 3.Facultad de Ciencias Naturales, Instituto para el Estudio de la Biodiversidad de Invertebrados (IEBI)Universidad Nacional de SaltaSaltaArgentina

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