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.
Similar content being viewed by others
References
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
de Zwart, D., & Posthuma, L. (2005). Complex mixture toxicity for single and multiple species: proposed methodologies. Environmental Toxicology and Chemistry, 24, 2665–2676.
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.
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.
Farkas, A., Salánki, J., & Varanka, I. (2000). Heavy metal concentrations in fish of Lake Balaton. Lakes & Reservoirs: Research & Management, 5, 271–279.
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.
García-Berthou, E. (2001). Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio). Aquatic Sciences, 63, 466–476.
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.
García-Berthou, E., & Moreno-Amich, R. (2000). Rudd (Scardinius erythrophthalmus) introduced to the Iberian peninsula: feeding ecology in Lake Banyoles. Hydrobiologia, 436, 159–164.
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.
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
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.
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.
Hoole, D., Bucke, D., Burgess, P., & Wellby, I. (2001). Diseases of carp and other cyprinid fishes. Oxford: Blackwell Science.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Simon, T. P. (ed). (1999). Assessing the sustainability and biological integrity of water resources using fish communities. Florida: CRC.
Sokal, R. R., & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research. New York: Freeman.
Tabachnick, B. G., & Fidell, L. S. (2001). Using multivariate statistics. Boston: Allyn and Bacon.
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.
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.
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.
Acknowledgements
This study was financially supported by the Spanish Ministry of the Environment and the Catalan Water Agency (MOBITROF project to J.O. Grimalt), the Spanish Ministry of Education (CGL2006-11652-C02-01/BOS) and the Government of Catalonia (Catalan Government Distinction Award for University Research 2004 to EGB). LB held a doctoral fellowship from the University of Girona. We are also grateful to the stimulating environment of the MOBITROF project, to everybody who assisted in field work and to two anonymous reviewers for helpful comments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Benejam, L., Benito, J. & García-Berthou, E. Decreases in Condition and Fecundity of Freshwater Fishes in a Highly Polluted Reservoir. Water Air Soil Pollut 210, 231–242 (2010). https://doi.org/10.1007/s11270-009-0245-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11270-009-0245-z