Skip to main content
Log in

Responses of Chub (Leuciscus cephalus) Populations to Chemical Stress, Assessed by Genetic Markers, DNA Damage and Cytochrome P4501A Induction

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Indicators of effects at the population level (genetic variation using allozymes) and early indicators of pollution (EROD activity and DNA strand break formation) were analysed in chub (Leuciscus cephalus) living in weakly and heavily contaminated stations of the Rhône River watershed. The genetic erosion was mainly detected in a fish population living in a contaminated small river system, through modifications in allelic and genotypic frequencies for PGM-2 locus and could be linked to a genetic bottleneck and to the reduced gene flow from upstream unable to maintain or restore the genetic diversity. In a contaminated large river system, the genetic diversity for PGM-2 and other loci was maintained and was probably the consequence of a high gene flow from upstream, linked to a sustained drift of larvae and juveniles in the system. A convergent increase of the frequency of the 90 allele at PGM-2 was observed in two contaminated stations compared with the reference station, this trend being confirmed on a more extensive geographic scale over the Rhône River basin. A high level of EROD activity was detected in both contaminated sites but only the fish in the large river system showed a significant DNA damage level compared to the reference population. The low DNA damage level and high hepato-somatic ratio characterized the impacted population of the small river system and could be associated to a chronic high-level exposure of fish to pollutants which selected individuals exhibiting a high level of DNA damage repair. In the two contaminated systems, some genotypes at the PGM-2 and EST-2 loci showed a low level of DNA damage and/or a high EROD activity and may be considered as being tolerant to pollutants. A higher tolerance of the most heterozygous fish was also detected in the contaminated large system and confirmed that a high level of heterozygosity may be necessary for survival in such a system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Agence de l'Eau Rhōne-Méditerranée-Corse (1998). Qualité des cours d'eau. Synthese 1995- 1996. Rapport Agence de l'Eau Rhōne-Méditerranée-Corse, Agence de l'Eau, Lyon.

    Google Scholar 

  • Agence de l'Eau Rhone-Mediterranee-Corse (1999). Qualité des cours d'eau. Resultats 1997. Rapport Agence de l'Eau Rhone-Mediterranee-Corse, Agence de l'Eau, Lyon.

    Google Scholar 

  • Anderson, S., Sadinski, W., Shugart, L., Brussard, P., Depledge, M., Ford, T., Hose, J., Stegeman, J., Suk, W., Wirgin, I. and Wogan, G. (1994). Genetic and molecular ecotoxicology: A research framework. Environ. Health Persp. 102, 3–8.

    Google Scholar 

  • Belfiore, N.M. and Anderson, S.L. (1998). Genetic patterns as a tool for monotoring and assessment of environmental impacts: The example of genetic ecotoxicology. Environ. Monitoring Assess. 51, 465–79.

    Google Scholar 

  • Benton, M.J., Diamond, S.A. and Guttman, S.I. (1994). A genetic and morphometric comparison of Helisoma trivolvis and Gambusia holbrooki from clean and contamined habitats. Ecotox. Env. Saf. 29, 20–37.

    Google Scholar 

  • Bouvet, Y., Bobin, M., Maslin, J.L. and Pattee, E. (1995). The Genetic structure of roach populations in two contrasted Large rivers. Hydrobiologia 303, 229–34.

    Google Scholar 

  • Chagnon, N.L. and Guttman, S.I. (1989). Differential survivorship of allozyme genotypes in mosquitofish populations exposed to copper or cadmium. Environ. Toxicol. Chem. 8, 319–26.

    Google Scholar 

  • Chessel, D., Dolédec, S. and Thioulouse, J. (1995). ADE Version 4: HyperCard Stacks and Programme. Library for the Analysis of Environmental Data. URA CNRS 1451, Université Lyon 1, 69622 Villeurbanne Cedex. Available at http:rrbiomserv.univ-lyon1.frrade-4.html.

  • Cormier, S.M., Racine, R.N., Smith, C.E., Dey, W.P. and Peck, T.H. (1989). Hepatocellular carcinoma and fatty infiltration in the Atlantic tomcod, Microgadus tomcod Walbaum. J. Fish Dis. 12, 105–16.

    Google Scholar 

  • Danzmann, R.G., Ferguson, M.M. and Allendorf, F.W. (1988). Heterozygosity and components of fitness in a strain of rainbow trout. Biol. J. Linn. Soc. 33, 285–304.

    Google Scholar 

  • Depledge, M.H. (1996). Genetic ecotoxicology: An overview. J. Exp. Mar. Biol. Ecol. 200, 57–66.

    Google Scholar 

  • Devaux, A., Flammarion, P., Bernardon, V., Garric, J. and Monod, G. (1998). Monitoring of the chemical pollution of the river Rhone through measurement of DNA damage and cytochrome P4501A induction in chub (Leuciscus cephalus). Mar. Environ. Res. 46, 257–62.

    Google Scholar 

  • Devaux, A., Pesonen, M. and Monod, G. 1997. Alkaline comet assay in rainbow trout hepatocytes. Toxicol. in Vitro 11, 71–9.

    Google Scholar 

  • Diamond, S.A., Newman, M.C., Mulvey, M., Dixon, P.M. and Martinson, D. (1989). Allozyme genotype and time to death of mosquitofish, Gambusia affinis Baird and Girard, during acute exposure to inorganic mercury. Environ. Toxicol. Chem. 8, 613–22.

    Google Scholar 

  • Durand, J.D., Persat, H. and Bouvet, Y. (1999). Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol. Ecol. 8, 989–97.

    Google Scholar 

  • Flammarion, P. and Garric, J. (1997). Cyprinids reference EROD levels in low contaminated rivers: A relevant statistical approach to estimate reference levels for EROD biomarker. Chemosphere 35, 2375–88.

    Google Scholar 

  • Flammarion, P. and Garric, J. (1999). A statistical approach for classifying the extent of EROD induction of fish sampled in clean and contaminated waters. Water Res. 33, 2683–9.

    Google Scholar 

  • Flammarion, P., Migeon, B. and Garric, J. (1998). Statistical analysis of cyprinids EROD data in a large French watershed. Ecotox. Environ. Saf. 40, 144–53.

    Google Scholar 

  • Fletcher, G.L., King, M.J., Kiceniuk, J.W. and Addison, R.F. (1982). Liver hypertrophy in winter flounder following exposure to experimentally oiled sediments. Comp. Biochem. Phys. 73c, 457–62.

    Google Scholar 

  • Forbes, V.E. and Forbes, T.L. (1994). Ecotoxicology in Theory and Practice. London: Chapman and Hall.

    Google Scholar 

  • Foré, S.A., Guttman, S.I., Bailer, A.J., Altfater, D.J. and Counts, B.V. (1995a). Exploratory analysis of population genetic assessment as a water quality indicator. I. Pinephales notatus. Ecotox. Environ. Saf. 30, 24–35.

    Google Scholar 

  • Foré, S.A., Guttman, S.I., Bailer, A.J., Altfater, D.J. and Counts, B.V. (1995b). Exploratory analysis of population genetic assessment as a water quality indicator. II. Compostoma anomalum. Ecotox. Environ. Saf. 30, 36–46.

    Google Scholar 

  • Fossi, M.C., Leonzio, C., Focardi, S., Lari, L. and Renzoni, A. (1991). Modulation of mixed-function oxidase activity in black-headed gulls living in anthropic environments: Biochemical acclimatization or adaptation? Environ. Toxicol. Chem.10, 1179–88.

    Google Scholar 

  • Gillespie, R.B. and Guttman, S.I. (1989). Effects of contaminants on the frequencies of allozymes in populations of the Central Stoneroller. Environ. Toxicol. Chem. 8, 309–17.

    Google Scholar 

  • Gillespie, R.B. and Guttman, S.I. (1993). Correlations between water quality and frequencies of allozyme genotypes in spotfin shiner Notropis spilopteris populations. Environ. Pollut. 81, 147–50.

    Google Scholar 

  • Goksoyr, A. and Forlin, L. (1992). The cytochrome P-450 system in fish, aquatic toxicology and environmental monitoring. Aqua. Toxicol. 22, 287–312.

    Google Scholar 

  • Hebert, P.D.N. and Luiker, M.M. (1996). Genetic effects of contaminant exposure towards an assessment of impacts on animal populations. Sci. of Total Environ. 191, 23–58.

    Google Scholar 

  • Heithaus, M.R. and Laushman, R.H. (1997). Genetic variation and conservation of stream fishes: Influence of ecology, life history, and water quality. Can. J. Fish. Aquat. Sci. 54, 1822–36.

    Google Scholar 

  • Hill, M.O. and Smith, A.J.E. (1976). Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 25, 249–55.

    Google Scholar 

  • Hughes, J.M., Harrison, D.A. and Arthur, J.M. (1991). Genetic variation at the PGI locus in the mosquitofish Gambusia affinis (Poeciliidae) and a possible effect on susceptibility to an insecticide. Biol. J. Linn. Soc. 44, 153–67.

    Google Scholar 

  • Kloepper-Sams, P.J., Swanson, S.M., Marchant, T., Schryer, R. and Owens, J.W. (1994). Exposure of fish to biologically treated bleached-kraft effluent. I. Biochemical, physiological and pathological assessment of rocky mountain white-fish (Prosopium williamsoni) and longnose sucker (Catostomus catostomus). Environ. Toxicol. Chem. 13, 1469–82.

    Google Scholar 

  • Koehn, R.K. and Bayne, B.L. (1989). Towards a physiological and genetical understanding of the energetics of the stress response. Biol. J. Linn. Soc. 37, 157–71.

    Google Scholar 

  • Koehn, R.K., Diehl, W.J. and Scott, T.M. (1988). The differential contribution by individual enzymes of glycosis and protein catabolism to the relationship between heterozygosity and growth rate in the coot clam, Mulinia lateralis. Genetics 118, 121–30.

    Google Scholar 

  • Laroche, J., Durand, J.D., Bouvet, Y., Guinand, B. and Brohon, B. (1999). Genetic structure and differentiation among populations of two cyprinids, Leuciscus cephalus and Rutilus rutilus, in a large European river. Can. J. Fish. Aquat. Sci. 56, 1659–67.

    Google Scholar 

  • Le Louarn, H., Bagliniere, J.L., Marchand, F. and Hamonet, J.M. (1997). Caracteristiques biologiques et ecologiques du chevaine Leuciscus cephalus dans quelques rivieres de la façade atlantique française. INRA, Bull. Scient. et Techn. 29, 30 p.

  • Mc Farland, V.A., Inouye, L.S., Lutz, C.H., Jarvis, A.S., Clarke, J.U. and Mc Cant, D.D. (1999). Biomarkers of oxidative stress and genotoxicity in livers of field-collected brown bullhead, Ameiurus nebulosus. Arch. Environ. Cont. Tox. 37, 236–41.

    Google Scholar 

  • Michelot, J.L., de Alencastro, L.P., Laurent, L., Becker, K. and Granjean, D. (1998). Contamination par les PCB et les métaux lourds de différents cours d'eau de la région Rhône-Alpes et potentialité de réintroduction de la loutre (Lutra lutra L.). Le Bièvre 15, 3–27.

    Google Scholar 

  • Monod, G., Devaux, A. and Rivière, J.L. (1988). Effects of chemical pollution on the activities of hepatic xenobiotic metabolizing enzymes in fish from the river Rhône. Sci. Total Environ. 73, 189–201.

    Google Scholar 

  • Moraga, D. and Tanguy, A. (2000). Genetic indicators of herbicide stress in the pacific oyster Crassostrea gigas under experimental conditions. Environ. Toxicol. Chem. 19(3), 706–11.

    Google Scholar 

  • Mulvey, M., Newman, M.C., Chazal, A., Keklak, M.M., Heagler, M.G. and Hales, L.S. (1995). Genetic and demographic responses of mosquitofish (Gambusia holbrooki Girard 1859) populations stressed by mercury. Environ. Toxicol. Chem. 14, 1411–8.

    Google Scholar 

  • Nadig, S.G., Lee, K.L. and Adams, S.M. (1998). Evaluating alterations of genetic diversity in sunfish populations exposed to contaminants using RAPD assay. Aqua. Toxicol. 43, 163–78.

    Google Scholar 

  • Nevo, E., Lavie, B. and Ben-Shlomo, R. (1983). Selection of allelic isozyme polymorphisms in marine organisms: Pattern, theory, and application. In M.C. Ratazzi, J.G. Scandalios and G.S. Whitt (eds.) Isozymes: Current Topics in Biological and Medical Research, vol. 10, pp. 69–92. New York: Liss.

    Google Scholar 

  • Nevo, E., Pearl, T., Beiles, A. and Wool, D. (1981). Mercury selection of allozyme genotypes in shrimps. Experientia 37, 1152–4.

    Google Scholar 

  • Olive, P.L., Banath, J.P. and Durand, R.E. (1990). Detection of etoposide resistance by measuring DNA damage in individual chinese hamster cells. Nat. Cancer 82, 779–83.

    Google Scholar 

  • Pohl, R.J. and Fouts, J.R. (1980). A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subcellular fractions. Anal. Biochem. 107, 150–5.

    Google Scholar 

  • Shugart, L. and Theodorakis, C. (1994). Environmental genotoxicity: Probing the underlying mechanisms. Environ. Health Persp. 102, 13–7.

    Google Scholar 

  • Shugart, L.R. (1997). Genetic ecotoxicology II: Population genetic structure in mosquitofish exposed in situ to radionuclides. Ecotoxicology 6, 335–54.

    Google Scholar 

  • Shugart, L. and Theodorakis, C. (1998). New trends in biological monitoring: Application of biomarkers to genetic ecotoxicology. Biotherapy 11, 119–27.

    Google Scholar 

  • Silbiger, R.N., Christ, S.A., Leonard, A.C., Garg, M., Lattier, D.L., Dawes, S., Dimsoski, P., McCormick, F., Wessendarp, T., Gordon, D.A., Roth, A.C., Smith, M.K. and Toth, G.P. (1998). Preliminary studies on the population genetics of the central stoneroller (Campostoma anomalum) from the Great Miami River basin, Ohio. Environ. Monit. Assess. 51, 481–95.

    Google Scholar 

  • Singh, N.P., McCoy, M.T., Tice, R.R. and Schneider, E.L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175, 184–91.

    Google Scholar 

  • Sugg, D.W., Bickham, J.W., Brooks, J.A., Lomakin, M.D., Jagoe, C.H., Dallas, C.E., Smith, M.H., Baker, R.J. and Chesser, R.K. (1996). DNA damage and radiocesium in channel catfish from Chernobyl. Environ. Toxicol. Chem. 15, 1057–63.

    Google Scholar 

  • Sugg, D.W., Chesser, R.K., Brooks, J.A. and Grasman, B.T. (1995). The association of DNA damage to concentrations of mercury and radiocesium in largemouth bass. Environ. Toxicol. Chem. 14(4), 661–8.

    Google Scholar 

  • Sullivan, K.B. and Lydy, M.J. (1999). Differences in survival functions of mosquitofish (Gambusia affinis) and sand shiner (Notropis ludibundus) genotypes exposed to pesticides. Environ. Toxicol. Chem. 18(5), 906–11.

    Google Scholar 

  • Tanguy, A., Castro, N.F., Marhic, A. and Moraga, D. (1999). Effects of an organic pollutant tributyltin on genetic structure in the pacific oyster Crassostrea gigas. Mar. Pollut. Bull. 38(7), 550–59.

    Google Scholar 

  • Theodorakis, C.W. and Shugart, L.R. (1997). Genetic ecotoxicology II: Population genetic structure in mosquitofish exposed in situ to radionuclides. Ecotoxicology 6, 335–54.

    Google Scholar 

  • Theodorakis, C.W., Bickham, J.W., Elbl, T., Shugart, L.R. and Chesser, R.K. (1998). Genetics of radionucleotide-contaminated mosquitofish populations and homology between Gambusia affinis and G. holbrooki. Environ. Toxicol. Chem. 17, 1992–8.

    Google Scholar 

  • Theodorakis, C.W., Blaylock, B.G. and Shugart, L.R. (1997). Genetic ecotoxicology I: DNA integrity and reproduction in mosquitofish exposed in situ to radionuclides. Ecotoxicology 6, 205–18.

    Google Scholar 

  • Vigano, L., Arillo, A., Melodia, F., Arlati, P. and Monti, C. (1998). Biomarker responses in Cyprinids of the middle stretch of the river Po, Italy. Environ. Toxicol. Chem. 17, 404–11.

    Google Scholar 

  • Watt, W.B. (1985). Bioenergetics and evolutionary genetics: Opportunities for a new synthesis. Am. Nat. 125, 118–43.

    Google Scholar 

  • Weis, J.S. and Weis, P. (1989). Tolerance and stress in a polluted environment. BioScience 39, 89–95.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Larno, V., Laroche, J., Launey, S. et al. Responses of Chub (Leuciscus cephalus) Populations to Chemical Stress, Assessed by Genetic Markers, DNA Damage and Cytochrome P4501A Induction. Ecotoxicology 10, 145–158 (2001). https://doi.org/10.1023/A:1016637809483

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016637809483

Navigation