Water, Air, & Soil Pollution

, Volume 210, Issue 1–4, pp 231–242

Decreases in Condition and Fecundity of Freshwater Fishes in a Highly Polluted Reservoir

  • Lluís Benejam
  • Josep Benito
  • Emili García-Berthou
Article

Abstract

Despite many efforts for pollution abatement in aquatic ecosystems, there are still some cases of high accumulation of industrial pollutants due to past activities. In Flix reservoir (Ebro River, Spain), there are around 200,000–360,000 tons of industrial pollutants with a high concentration of heavy metals and organochlorides due to the activity of an organochlorine industry during more than half a century. This exceptional amount of pollutants provides a good opportunity (and need) to analyse their effects on fish populations under natural conditions, which is rarely available to ecotoxicologists. We compared the reproductive traits and prevalence of diseases and parasites at this impacted area with a neighbouring upstream reservoir unaffected by the pollution (reference sites) and also to downstream sites. Deformity, eroded fin, lesion and tumour (DELT) anomalies and ectoparasites were clearly more frequent at the impacted area for several fish species (common carp, roach and pumpkinseed). A significant negative impact of Flix reservoir on condition (eviscerated and liver weights, adjusted for fish size with analysis of covariance) and reproductive traits (gonadal weight and number of mature eggs, adjusted for fish size) was also detected for several fish species. The responses to the pollutants were species-specific, and common carp (Cyprinus carpio) was the species with the clearest effects on fitness-related traits at the impacted area, despite also being among the most tolerant to pollution.

Keywords

Heavy metals Organochlorides Common carp Cyprinus carpio Flix reservoir 

References

  1. Adams, S. M. (1999). Ecological role of lipids in the health and success of fish populations. In M. T. Arts & B. C. Wainman (Eds.), The ecological role of lipids in freshwater ecosystems (pp. 132–160). New York: Springer.Google Scholar
  2. Adams, S. M., & Greeley, M. S. (2000). Ecotoxicological indicators of water quality: using multi-response indicators to assess the health of aquatic ecosystems. Water Air and Soil Pollution, 123, 103–115.CrossRefGoogle Scholar
  3. Adams, S. M., Crumby, W. D., Greeley, M. S., Ryon, M. G., & Schilling, E. M. (1992). Relationships between physiological and fish population responses in a contaminated stream. Environmental Toxicology and Chemistry, 11, 1549–1557.CrossRefGoogle Scholar
  4. Amaral, O. C., Otero, R., Grimalt, J. O., & Albaigés, J. (1996). Volatile and semi-volatile organochlorine compounds in tap and riverine waters in the area of influence of a chlorinated organic solvent factory. Water Research, 30, 1876–1884.CrossRefGoogle Scholar
  5. Bagenal, T. B., & Braum, E. (1999). Eggs and early life history. In T. Bagenal (Ed.), Methods for assessment of fish production in fresh waters (pp. 132–160). Oxford: Blackwell.Google Scholar
  6. Barton, B. A., Morgan, J. D., & Vijayan, M. M. (2002). Physiological condition-related indicators of environmental stress in fish. In S. M. Adams (Ed.), Biological indicators of aquatic ecosystem stress (pp. 111–148). Bethesda: American Fisheries Society.Google Scholar
  7. Benejam, L., Benito, J., Ordóñez, J., Armengol, J., & García-Berthou, E. (2008). Short-term effects of a partial drawdown on fish condition in a eutrophic reservoir. Water, Air, & Soil Pollution, 190, 3–11.CrossRefGoogle Scholar
  8. Bieniarz, K., Epler, P., & Sokolowska-Mikolajczyk, M. (1997). Reproduction of fish in conditions disadvantageously altered with the salts of zinc and copper. Archives of Polish Fisheries, 5, 21–30.Google Scholar
  9. Cairns, J. J. (1983). The case for simultaneous toxicity testing at different levels of biological organization. In W. E. Bishop, R. D. Cardwell & B. B. Heidolph (Eds.), Aquatic toxicology and hazard assessment: 6th symposium STP 802 (pp. 111–127). Philadelphia: American Society for Testing and Material.CrossRefGoogle Scholar
  10. Carol, J., Benejam, L., Alcaraz, C., Vila-Gispert, A., Zamora, L., Navarro, E., et al. (2006). The effects of limnological features on fish assemblages of 14 Spanish reservoirs. Ecology of Freshwater Fish, 15, 66–77.CrossRefGoogle Scholar
  11. Carol, J., Zamora, L., & García-Berthou, E. (2007). Preliminary telemetry data on the movement patterns and habitat use of European catfish (Silurus glanis) in a reservoir of the River Ebro, Spain. Ecology of Freshwater Fish, 16, 450–456.CrossRefGoogle Scholar
  12. Carol, J., Benejam, L., Benito, J., & García-Berthou, E. (2009). Growth and diet of European cafish (Silurus glanis) in early and late invasion stages. Fundamental and Applied Limnology, 174, 317–328.CrossRefGoogle Scholar
  13. Carrasco, L., Díez, S., Soto, D., Catalan, J., & Bayona, J. M. (2008). Assessment of mercury and methylmercury pollution with zebra mussel (Dreissena polymorpha) in the Ebro River (NE Spain) impacted by industrial hazardous dumps. Science of the Total Environment, 407, 178–184.CrossRefGoogle Scholar
  14. Chuiko, G. M., Tillitt, D. E., Zajicek, J. L., Flerov, B. A., Stepanova, V. M., Zhelnin, Y. Y., et al. (2007). Chemical contamination of the Rybinsk Reservoir, northwest Russia: Relationship between liver polychlorinated biphenyls (PCB) content and health indicators in bream (Abramis brama). Chemosphere, 67, 527–536.CrossRefGoogle Scholar
  15. Crivelli, A. J. (1981). The biology of the common carp, Cyprinus carpio L. in the Camargue, southern France. Journal of Fish Biology, 18, 271–290.CrossRefGoogle Scholar
  16. de Zwart, D., & Posthuma, L. (2005). Complex mixture toxicity for single and multiple species: proposed methodologies. Environmental Toxicology and Chemistry, 24, 2665–2676.CrossRefGoogle Scholar
  17. Durrieu, G., Maury-Brachet, R., Girardin, M., Rochard, E., & Boudou, A. (2005). Contamination by heavy metals (Cd, Zn, Cu, and Hg) of eight fish species in the Gironde estuary (France). Estuaries, 28, 581–591.CrossRefGoogle Scholar
  18. Eljarrat, E., Martínez, M. A., Sanz, P., Concejero, M. A., Piña, B., Quirós, L., et al. (2008). Distribution and biological impact of dioxin-like compounds in risk zones along the Ebro River basin (Spain). Chemosphere, 71, 1156–1161.CrossRefGoogle Scholar
  19. Farkas, A., Salánki, J., & Varanka, I. (2000). Heavy metal concentrations in fish of Lake Balaton. Lakes & Reservoirs: Research & Management, 5, 271–279.CrossRefGoogle Scholar
  20. Fournie, J. W., Summers, J. K., & Weisberg, S. B. (1996). Prevalence of gross pathological abnormalities in estuarine fishes. Transactions of the American Fisheries Society, 125, 581–590.CrossRefGoogle Scholar
  21. García-Berthou, E. (2001). Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio). Aquatic Sciences, 63, 466–476.CrossRefGoogle Scholar
  22. García-Berthou, E., & Moreno-Amich, R. (1993). Multivariate analysis of covariance in morphometric studies of the reproductive cycle. Canadian Journal of Fisheries and Aquatic Sciences, 50, 1394–1399.CrossRefGoogle Scholar
  23. García-Berthou, E., & Moreno-Amich, R. (2000). Rudd (Scardinius erythrophthalmus) introduced to the Iberian peninsula: feeding ecology in Lake Banyoles. Hydrobiologia, 436, 159–164.CrossRefGoogle Scholar
  24. Grimalt, J. O., Gómez-Belinchón, J. I., Llop, R., & Albaigés, J. (1988). Water-phase distribution of hexachlorobenzene in a deltaic environment (Ebro Delta, Western Mediterranean). Chemosphere, 17, 1893–1903.CrossRefGoogle Scholar
  25. Grimalt, J. O., Sánchez-Cabeza, J. A., Palanques, A., & Catalan, J. (2003). Estudi de la dinàmica dels compostos organoclorats persistents i altres contaminants en els sistemes aquàtics continentals. Catalan Water Agency, Government of Catalonia. http://mediambient.gencat.cat/cat/ciutadans/informacio_ambiental/Flix/estudi.jsp
  26. Has-Schön, E., Bogut, I., & Strelec, I. (2006). Heavy metal profile in five fish species included in human diet, domiciled in the end flow of River Neretva (Croatia). Archives of Environmental Contamination and Toxicology, 50, 545–551.CrossRefGoogle Scholar
  27. Hinck, J. E., Blazer, V. S., Denslow, N. D., Echols, K. R., Gross, T. S., May, T. W., et al. (2007). Chemical contaminants, health indicators, and reproductive biomarker responses in fish from the Colorado River and its tributaries. Science of the Total Environment, 378, 376–402.CrossRefGoogle Scholar
  28. Hoole, D., Bucke, D., Burgess, P., & Wellby, I. (2001). Diseases of carp and other cyprinid fishes. Oxford: Blackwell Science.CrossRefGoogle Scholar
  29. Jobling, S., Beresford, N., Nolan, M., Rodgers-Gray, T., Brighty, G. C., Sumpter, J. P., et al. (2002). Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biology of Reproduction, 66, 272–281.CrossRefGoogle Scholar
  30. Johnson, L. L., Sol, S. Y., Ylitalo, G. M., Hom, T., French, B., Olson, O. P., et al. (1997). Reproductive injury in English Sole (Pleuronectes vetulus) from the Hylebos Waterway, Commencement Bay, Washington. Journal of Aquatic Ecosystem Stress and Recovery, 6, 289–310.CrossRefGoogle Scholar
  31. Karr, J. R., Fausch, K. D., Angermeier, P. L., Yant, P. R., & Schlosser, I. J. (1986). Assessing biological integrity in running waters: a method and its rationale. Champaign: Illinois Natural History Survey.Google Scholar
  32. Laflamme, J. S., Couillard, Y., Campbell, P. G. C., & Hontela, A. (2000). Interrenal metallothionein and cortisol secretion in relation to Cd, Cu, and Zn exposure in yellow perch, Perca flavescens, from Abitibi lakes. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1692–1700.CrossRefGoogle Scholar
  33. Lavado, R., Thibaut, R., Raldua, D., Martin, R., & Porte, C. (2004). First evidence of endocrine disruption in feral carp from the Ebro River. Toxicology and Applied Pharmacology, 196, 247–257.CrossRefGoogle Scholar
  34. Ma, G., Lin, H., & Zhang, W. (1995). Effects of cadmium on serum gonadotropin and growth hormone in common carp (Cyprinus carpio). Journal of Fisheries of China, 19, 120–126.Google Scholar
  35. Marshall, C. T., & Frank, K. T. (1999). The effect of interannual variation in growth and condition on haddock recruitment. Canadian Journal of Fisheries and Aquatic Sciences, 56, 347–355.CrossRefGoogle Scholar
  36. Mendil, D., & Uluozlu, O. D. (2007). Determination of trace metal levels in sediment and five fish species from lakes in Tokat, Turkey. Food Chemistry, 101, 739–745.CrossRefGoogle Scholar
  37. Navarro, A., Quirós, L., Casado, M., Faria, M., Carrasco, L., Benejam, L., et al. (2009). Physiological responses to mercury in feral carp populations inhabiting the low Ebro River (NE Spain), a historically contaminated site. Aquatic Toxicology, 93, 150–157.CrossRefGoogle Scholar
  38. Power, M., Dempson, J. B., Reist, J. D., Schwarz, C. J., & Power, G. (2005). Latitudinal variation in fecundity among Arctic charr populations in eastern North America. Journal of Fish Biology, 67, 255–273.CrossRefGoogle Scholar
  39. Prenter, J., MacNeil, C., Dick, J. T. A., & Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution, 19, 385–390.CrossRefGoogle Scholar
  40. Quirós, L., Ruiz, X., Sanpera, C., Jover, L., & Piña, B. (2008). Analysis of micronucleated erythrocytes in heron nestlings from reference and impacted sites in the Ebro basin (N.E. Spain). Environmental Pollution, 155, 81–87.CrossRefGoogle Scholar
  41. Raldúa, D., Díez, S., Bayona, J. M., & Barceló, D. (2007). Mercury levels and liver pathology in feral fish living in the vicinity of a mercury cell chlor-alkali factory. Chemosphere, 66, 1217–1225.CrossRefGoogle Scholar
  42. Rice, C. D. (2001). Fish immunotoxicology. In D. Schlenk & W. Benson (Eds.), Target organ toxicity in marine and freshwater teleosts. Volume 2—Systems (pp. 96–138). London: CRC.CrossRefGoogle Scholar
  43. Roussel, H., Joachim, S., Lamothe, S., Palluel, O., Gauthier, L., & Bonzom, J. M. (2007). A long-term copper exposure on freshwater ecosystem using lotic mesocosms: Individual and population responses of three-spined sticklebacks (Gasterosteus aculeatus). Aquatic Toxicology, 82, 272–280.CrossRefGoogle Scholar
  44. Sanders, R. E., Miltner, R. J., Yoder, C. O., & Rankin, E. T. (1999). The use of external deformities, erosion, lesions, and tumors (DELT anomalies) in fish assemblages for characterizing aquatic resources: a case study of seven Ohio streams. In T. P. Simon (Ed.), Assessing the sustainability and biological integrity of water resources using fish communities (pp. 225–246). Florida: CRC.Google Scholar
  45. Simon, T. P. (ed). (1999). Assessing the sustainability and biological integrity of water resources using fish communities. Florida: CRC.Google Scholar
  46. Sokal, R. R., & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research. New York: Freeman.Google Scholar
  47. Tabachnick, B. G., & Fidell, L. S. (2001). Using multivariate statistics. Boston: Allyn and Bacon.Google Scholar
  48. Toft, G., Baatrup, E., & Guillette, L. J. (2004). Altered social behavior and sexual characteristics in mosquitofish (Gambusia holbrooki) living downstream of a paper mill. Aquatic Toxicology, 70, 213–222.CrossRefGoogle Scholar
  49. Vila-Gispert, A., & Moreno-Amich, R. (2000). Fecundity and spawning mode of three introduced fish species in Lake Banyoles (Catalunya, Spain) in comparison with other localities. Aquatic Sciences, 62, 154–166.CrossRefGoogle Scholar
  50. Yeom, D. H., Lee, S. A., Kang, G. S., Seo, J., & Lee, S. K. (2007). Stressor identification and health assessment of fish exposed to wastewater effluents in Miho Stream, South Korea. Chemosphere, 67, 2282–2292.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Lluís Benejam
    • 1
  • Josep Benito
    • 1
  • Emili García-Berthou
    • 1
  1. 1.Institute of Aquatic EcologyUniversity of GironaGironaSpain

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