Advertisement

Hydrobiologia

, Volume 680, Issue 1, pp 25–38 | Cite as

The introduced bivalve Limnoperna fortunei boosts Microcystis growth in Salto Grande reservoir (Argentina): evidence from mesocosm experiments

  • Daniel Cataldo
  • Alicia Vinocur
  • Inés O′Farrell
  • Esteban Paolucci
  • Valentín Leites
  • Demetrio Boltovskoy
Primary research paper

Abstract

In order to assess the effects of the introduced bivalve Limnoperna fortunei on water-column properties of Salto Grande reservoir, experiments were conducted using six 400 L mesocosms: 2 with 100 mussels, 2 with 300 mussels, and 2 controls (without mussels). At 0, 1, 2, 3, 7, 14, 21, 28, and 35 days we measured nutrient and chlorophyll a concentrations, counted and identified the phytoplankton, and estimated the density, size, and number of cells of the colonies of Microcystis spp. Cumulative periphyton growth and total accumulated sediments were assessed in all enclosures at the end of the experiment. Throughout the experiment, in the controls ammonia and phosphates dropped to near zero, whereas in the mesocosms with L. fortunei they increased two- to tenfold. Nitrates decreased in all mesocosms. In the presence of the mussel, chlorophyll a and algal cells dropped until day 3 increasing thereafter, whereas in the controls they increased from day 0. Periphyton growth and sediment accumulation were significantly higher in the mesocosms with mussels that in the controls. Cell density, proportion of colonial cells and colony size of Microcystis spp. increased in all enclosures, but these increases were dramatically (and very significantly) higher in enclosures with 100 and, especially, with 300 mussels, than in the controls. Our results indicate that L. fortunei modifies nutrient concentrations and proportions, and promotes aggregation of solitary Microcystis spp. cells into colonies; both these effects can favor blooms of this often noxious cyanobacteria.

Keywords

Introduced bivalves Microcystis blooms South America Limnoperna fortunei 

Notes

Acknowledgments

This study was supported by grants UBA ×020, PICT 25275 and PICT 01968 to DB. Logistical and economic support for field work and sample and data collection were provided by the Environmental Division of Comisión Técnica Mixta de Salto Grande (Argentina-Uruguay).

References

  1. APHA (American Public Health Association), 2005. Standard methods for the examination of water and wastewaters, 21st edn. APHA, Washington: 215–221.Google Scholar
  2. Beron, L., 1990. Features of the limnological behavior of Salto Grande’s reservoir (Argentina-Uruguay). Ecological Modeling 52: 87–102.CrossRefGoogle Scholar
  3. Boltovskoy, D. & D. Cataldo, 1999. Population dynamics of Limnoperna fortumei, an invasive fouling mollusc, in the lower Paraná river (Argentina). Biofouling 14: 255–263.CrossRefGoogle Scholar
  4. Boltovskoy, D., N. Correa, D. Cataldo & F. Sylvester, 2006. Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna fortunei in the Rıo de la Plata watershed and beyond. Biological Invasions 8: 963–974.CrossRefGoogle Scholar
  5. Boltovskoy, D., F. Sylvester, A. Otaegui, V. Leites & D. Cataldo, 2009a. Environmental modulation of reproductive activity of the invasive mussel Limnoperna fortunei in South America: implications for antifouling strategies. Austral Ecology 34: 719–730.CrossRefGoogle Scholar
  6. Boltovskoy, D., A. Karatayev, L. Burlakova, D. Cataldo, V. Karatayev, F. Sylvester & A. Mariñelarena, 2009b. Significant ecosystem-wide effects of the swiftly spreading invasive freshwater bivalve Limnoperna fortunei. Hydrobiologia 636: 271–284.CrossRefGoogle Scholar
  7. Bykova, O., A. Laursen, V. Bostan, J. Bautista & L. McCarthy, 2006. Do zebra mussels (Dreissena polymorpha) alter lake water chemistry in a way that favours Microcystis growth? Science of the Total Environment 371: 362–372.PubMedCrossRefGoogle Scholar
  8. Cartlon, J. T., 1999. The scale and ecological consequences of biological invasions in the World’s oceans. In Sandlund, O. T. (ed.), Invasive Species and Biodiversity Management. Kluwer Academic Publishers, Dordrecht: 195–212.Google Scholar
  9. Cataldo, D. & D. Boltovskoy, 2000. Yearly reproductive activity of Limnoperna fortunei (Bivalvia) as inferred from the occurrence of its larvae in the plankton of the lower Paraná river and the Río de la Plata estuary (Argentina). Aquatic Ecology 34: 307–317.CrossRefGoogle Scholar
  10. Cataldo, D., D. Boltovskoy & M. Pose, 2003. Toxicity of chlorine and three non-oxidizing molluscicides to the invasive pest mussel Limnoperna fortunei. Journal of the American Water Works Association 95: 66–78.Google Scholar
  11. Cataldo, D., D. Boltovskoy, J. Hermosa & C. Canzi, 2005. Temperature dependent larval development rates of Linmoperna fortunei (Mytilidae). Journal of Molluscan Studies 71: 41–46.CrossRefGoogle Scholar
  12. Cataldo, D., I. O′Farrell, E. Paolucci, F. Sylvester & D. Boltovskoy, 2008. Impacto del mejillón dorado Limnoperna fortunei sobre el fitoplancton y los nutrientes. IVX Congreso de la Asociación Ibérica de Limnología, 8–12 septiembre 2008, Universidad de Huelva, Huelva España: 53.Google Scholar
  13. Chalar, G., 2006. Eutrophication′s dynamics on different temporary scales: Salto Grande Reservoir (Argentina-Uruguay). In Tundisi, J. G., T. Matsumura Tundisi & C. S. Galli (eds), Eutrofização na América do Sul: causas, conseqüências e tecnologias de gerenciamento e controle. Instituto Internacional de Ecologia e Gerenciamento Ambiental, Academia Brasileira de Ciências, Conselho Nacional de Desenvolvimento Científico e Tecnológico, InterAcademy Panel on International Issues, Inter American Network of Academies of Sciences, Brasil: 87–101.Google Scholar
  14. Chalar, G., L. De León, M. Paradiso, E. Brugnoli & E. Clemente, 2002. Dinámica de la eutrofización del embalse Salto Grande: Informe del período septiembre de 2000-marzo 2002. Sección Limnología, Facultad de Ciencias, Montevideo: 82.Google Scholar
  15. Chapin, F. S., E. S. Zavaleta, V. T. Eviner, R. L. Naylor, P. M. Vitousek, H. L. Reynolds, D. U. Hooper, S. Lavorel, O. E. Sala, S. E. Hobbie, M. C. Mack & S. Diaz, 2000. Consequences of changing biodiversity. Nature 405: 234–242.PubMedCrossRefGoogle Scholar
  16. Conroy, J. D. & D. A. Culver, 2005. Do dreissenid mussels affect Lake Erie ecosystem stability processes? American Midland Naturalist 153: 20–32.CrossRefGoogle Scholar
  17. da Silva, M. D., M. D. R. Peralta & M. L. T. Mattos, 2003. Determinação de glifosato e ácido aminometilfosfônico em águas superficiais do arroio passo do pilão. Pesticidas: Revista de Ecotoxicologia e Meio Ambiente 13: 19–28.Google Scholar
  18. Darrigran, G., S. M. Martín, B. Gullo & L. Armendáriz, 1998. Macroinvertebrates associated with Limnoperna fortunei (Dunker 1857) (Bivalvia: Mytilidae) in Río de la Plata, Argentina. Hidrobiología 367: 223–230.CrossRefGoogle Scholar
  19. De León, L. & G. Chalar, 2003. Abundancia y diversidad del fitoplancton en el Embalse de Salto Grande (Argentina–Uruguay). Ciclo estacional y distribución espacial. Limnetica 22: 103–113.Google Scholar
  20. De León, L. & J. S. Yunes, 2001. First report of a microcystin-containing bloom of the cianobacterium Microcystis aeruginosa in the La Plata River, South America. Environmental Toxicology 16: 110–112.PubMedCrossRefGoogle Scholar
  21. De León, L., 2003: Floraciones algales de agua dulce: cianobacterias, cianotoxinas. Su relación con la salud. Universidad de la República, Facultad de Ciencias, Uruguay. Retrieved from the web: http://limno.fcien.edu.uy/pdf/Floraciones-de-CIANOBACTERIAS.pdf. Retrieved 02 Feb 2011.
  22. Dionisio Pires, L. M., B. W. Ibelings & E. van Donk, 2010. Zebra mussels as a potential tool in the restoration of eutrophic shallow lakes dominated by toxic cyanobacteria. In Van der Velde, G., S. Rajagopal S. & A. bij de Vaate A. (eds), The Zebra Mussel in Europe. Backhuys Publishers, Leiden: 361–372Google Scholar
  23. Dionisio Pires, L. M., R. Kusserow & E. Van Donk, 2003. Influence of toxic and non-toxic phytoplankton on feeding and survival of Dreissena polymorpha (Pallas) larvae. Hydrobiologia 491: 193–200.CrossRefGoogle Scholar
  24. Fishman, D. B., S. A. Adlerstein, H. A. Vanderploeg, G. L. Fahnenstiel & D. Scavia, 2009. Causes of phytoplankton changes in Saginaw Bay, Lake Huron, during the zebra mussel invasion. Journal of Great Lakes Research 35: 482–495.CrossRefGoogle Scholar
  25. Fulton, R. S. & H. W. Paerl, 1987. Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. Journal of Plankton Research 9: 837–855.CrossRefGoogle Scholar
  26. Gremberghe, I., P. van Vanormelingen, K. Van, C. der Gucht, W. Souffreau, L. Vyverman & De Meester, 2009. Priority effects in experimental populations of the cyanobacterium Microcystis. Environmental Microbiology 11: 2564–2573.PubMedCrossRefGoogle Scholar
  27. Huisman, J., H. C. P. Matthijs & P. M. Visser, 2005. Harmful cyanobacteria. Aquatic ecology series. Springer, Dordrecht: 1–415.CrossRefGoogle Scholar
  28. Inoue, M. H., R. S. Oliveira, J. B. Regitano, C. A. Tormena, V. L. Tornisielo & J. Constantin, 2003. Critérios para avaliação do potencial de lixiviação dos herbicidas comercializados no Estado do Paraná. Planta Daninha 21: 313–323.CrossRefGoogle Scholar
  29. Jakobsen, H. H. & K. W. Tang, 2002. Effects of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquatic Microbial Ecology 27: 261–273.CrossRefGoogle Scholar
  30. Jeong, K. S., D. K. Kim, P. Wigham & G. J. Joo, 2003. Modelling Microcystis aeruginosa bloom dynamics in the Nakdong River by means of evolutionary computation and statistic approach. Ecological Modeling 161: 67–68.CrossRefGoogle Scholar
  31. Juhel, G., J. Davenport, J. O’Halloran, S. Culloty, R. Ramsay, K. James, A. Furey & O. Allis, 2006a. Pseudodiarrhoea in zebra mussels Dreissena polymorpha (Pallas) exposed to microcystins. Journal of Experimental Biology 209: 810–816.PubMedCrossRefGoogle Scholar
  32. Juhel, G., J. Davenport, S. C. O’Halloran, R. M. Culloty, K. F. O’Riordan, A. James, A. Furey & O. Allis, 2006b. Impacts of microcystins on the feeding behaviour and energy balance of zebra mussels, Dreissena polymorpha: a bioenergetics approach. Aquatic Toxicology 79: 391–400.PubMedCrossRefGoogle Scholar
  33. Karatayev, A. Y., D. Boltovskoy, D. K. Padilla & L. E. Burlakova, 2007. The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. Journal of Shellfish Research 26: 205–213.CrossRefGoogle Scholar
  34. Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 2003. Impacts of zebra mussels on aquatic communities and their role as ecosystem engineers. In Leppäkoski, E., S. Gollasch & S. Olenin (eds.), Invasive aquatic species of Europe–distribution impacts and management. Kluwer Academic Publishers, Dordrecht: 433–446.Google Scholar
  35. 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
  36. Knoll, L. B., O. Sarnelle, S. K. Hamilton, C. E. H. Kissman, A. E. Wilson, J. B. Rose & M. R. Morgan, 2008. Invasive zebra mussels (Dreissena polymorpha) increase cyanobacterial toxin concentrations in low-nutrient lakes. Canadian Journal of Fisheries and Aquatic Sciences 65: 448–455.CrossRefGoogle Scholar
  37. Lowe, R. L. & R. W. Pillsbury, 1995. Shifts in benthic algal community structure and function following the appearance of zebra mussel (Dreissena polymorpha) in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21: 558–566.CrossRefGoogle Scholar
  38. Lürling, M., 1999. Grazer-induced coenobial formation in clonal cultures of Scenedesmus obliquus (Chlorococcales, Chlorophyceae). Journal of Phycology 35: 19–23.CrossRefGoogle Scholar
  39. Lürling, M. & E. van Donk, 1997. Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnology and Oceanography 42: 783–788.CrossRefGoogle Scholar
  40. Marker, A. F. H., C. A. Crowther & R. J. M. Gunn, 1980. Methanol and acetone as solvents for estimating chlorophyll a and phaeopigments by spectrophotometry. Archiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie 14: 52–69.Google Scholar
  41. Nalepa, T. F. & D. W. Schloesser (eds.), 1993. Zebra mussels: biology impacts and control. Lewis Publishers, Boca Raton: 145–152.Google Scholar
  42. Nicholls, K. H., L. Heintsch & E. Carney, 2002. Univariate steptrend and multivariate assessments of the apparent effects of P loading reductions and zebra mussels on the phytoplankton of the Bay of Quinte, Lake Ontario. Journal of Great Lakes Research 28: 15–31.CrossRefGoogle Scholar
  43. Paolucci, E., D. Cataldo, C. Fuentes & D. Boltovskoy, 2007. Larvae of the invasive species, Limnoperna fortunei (Bivalvia), in the diet of fish larvae in the Paraná River. Hydrobiologia 589: 219–233.CrossRefGoogle Scholar
  44. Paolucci, E., D. Cataldo & D. Boltovskoy, 2009. Prey selection by larvae of Prochilodus lineatus (Pisces: Curimatidae): indigenous zooplankton versus veligers of the introduced bivalve Limnoperna fortunei (Bivalvia: Mitilidae). Aquatic Ecology 44: 255–267.CrossRefGoogle Scholar
  45. Paolucci, E., E. Thuesen, D. Cataldo & D. Boltovskoy, 2010. Veligers of an introduced bivalve, Limnoperna fortunei, are a new food resource that enhances growth of larval fish in the Paraná River (South America). Freshwater Biology 55: 1831–1844.CrossRefGoogle Scholar
  46. Pastorino, G., G. Darrigran, S. M. Martın & L. Lunaschi, 1993. Limnoperna fortunei (Dunker, 1857) (Mytilidae), nuevo bivalvo invasor en aguas del Río de la Plata. Neotropica 39: 34.Google Scholar
  47. Pimentel, D., L. Lach, R. Zuniga & D. Morrison, 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50: 53–65.CrossRefGoogle Scholar
  48. Pizzolon, L., 1996. Importancia de las cianobacterias como factor de toxicidad en las aguas continentales. Interciencia 21: 239–245.Google Scholar
  49. Quayle, D. B., 1948. Biology of Venerupis pallastra (Montagu). PhD Thesis, University of Glasgow, Scotland: 1–72.Google Scholar
  50. Quirós, R. & L. Luchini, 1983. Características limnológicas del embalse de Salto Grande III: Fitoplancton y su relación con parámetros ambientales. Revista de la Asociación de Ciencias Naturales del Litoral 13: 19–66.Google Scholar
  51. Relyea, R. A., 2006. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 16: 2027–2034.CrossRefGoogle Scholar
  52. Rohrlack, T., E. Dittmann, M. Henning, T. Börner & J. G. Kohl, 1999. Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by the cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology 65: 737–739.PubMedGoogle Scholar
  53. Rojas Molina, F., J. C. Paggi & M. Devercelli, 2009. Zooplanktophagy in the natural diet and selectivity of the invasive mollusk Limnoperna fortunei. Biological Invasions 12: 1647–1659.CrossRefGoogle Scholar
  54. Ruibal Conti, A. L., J. M. Guerrero & J. M. Regueira, 2005. Levels of microcystins in two Argentinean reservoirs used for water supply and recreation: differences in the implementation of safe levels. Environmental Toxicology 20: 263–269.CrossRefGoogle Scholar
  55. 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
  56. Sarnelle, O., A. E. Wilson, S. K. Hamilton, L. B. Knoll & D. E. Raikow, 2005. Complex interactions between the zebra mussel, Dreissena polymorpha, and the harmful phytoplankter, Microcystis aeruginosa. Limnology and Oceanography 50: 896–904.CrossRefGoogle Scholar
  57. Smith, V. H., 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.PubMedCrossRefGoogle Scholar
  58. Sommer, U. Z., M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 455–471.Google Scholar
  59. 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
  60. 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
  61. Sylvester, F., J. Dorado, A. Juárez, D. Boltovskoy & D. Cataldo, 2005. Filtration rates of the invasive pest bivalve Limnoperna fortunei as a function of size and temperature. Hyobiologia 534: 71–80.CrossRefGoogle Scholar
  62. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen. Internationale Vereiningung für Theoretische und Angewandte Limnologie 9: 1–38.Google Scholar
  63. Vanderploeg, H. A., J. R. Liebig & A. A. Gluck, 1996. Evaluation of different phytoplankton for supporting development of zebra mussel larvae (Dreissena polymorpha): the importance of size and polyunsaturated fatty acid content. Journal of Great Lakes Research 22: 36–45.CrossRefGoogle Scholar
  64. Vanderploeg, H. A., J. R. Liebig, W. W. Carmichael, M. A. Agy, T. H. Johengen, G. L. Fahnenstiel & T. F. Nalepa, 2001. Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 58: 1208–1221.CrossRefGoogle Scholar
  65. Venrick, E. L., 1978. How many cells to count? In Sournia, A. (ed.), Phytoplankton manual, UNESCO Press, Paris: 167–180.Google Scholar
  66. von Rückert, G., M. C. Campos & M. E. Rolla, 2004. Alimentação de Limnoperna fortunei (Dunker 1857): taxas de filtração com ênfase ao uso de Cyanobacteria. Acta Scientiarum Biological Scences 26: 421–429.Google Scholar
  67. Wang, X., B. Qin, G. Gao & H. W. Paerl, 2010. Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. Journal of Plankton Research 32: 457–470.CrossRefGoogle Scholar
  68. Weber, C. I., 1973. Recent developments in the measurement of the response of plankton and periphyton to changes in their environment. In Glass, F. (ed.), Bioassay Techniques and Environmental Chemistry. Ann Arbor Science Publishers, Ann Arbor: 119–138.Google Scholar
  69. Wilson, A. E., W. A. Wilson & M. E. Hay, 2006. Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology 72: 7386–7389.PubMedCrossRefGoogle Scholar
  70. Yang, Z., F. X. Kong, H. S. Cao & X. L. Shi, 2005. Observation on colony formation of Microcystis aeruginosa induced by filtered lake water under laboratory conditions. Annales de Limnologie 41: 169–173.CrossRefGoogle Scholar
  71. Zhou, Y., F. Kong, X. Shi & C. Huansheng, 2006. Morphological Response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563: 225–230.CrossRefGoogle Scholar
  72. Znachor, P., T. Jurczack, J. Komárková, J. Jezberová, J. Mankiewicz, K. Kaštovská & E. Zapomělová, 2006. Summer changes in cyanobacterial bloom composition and microcystin concentration in eutrophic Czech reservoirs. Environmental Toxicology 21: 236–243.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Daniel Cataldo
    • 1
    • 2
    • 3
  • Alicia Vinocur
    • 4
  • Inés O′Farrell
    • 1
    • 2
  • Esteban Paolucci
    • 2
    • 3
  • Valentín Leites
    • 5
    • 6
  • Demetrio Boltovskoy
    • 2
    • 3
    • 1
  1. 1.Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y TécnicasBuenos AiresArgentina
  3. 3.Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’Buenos AiresArgentina
  4. 4.Departamento Ecología, Genética y Evolución and Departamento Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  5. 5.Comisión Técnica Mixta Salto GrandeConcordiaArgentina
  6. 6.Comisión Técnica Mixta Salto GrandeSaltoUruguay

Personalised recommendations