Skip to main content

Relationship between genotoxicity, mutagenicity, and fish community structure in a contaminated stream

Abstract

Genotoxic responses (chromosomal damage, DNA strandbreakage) of redbreast sunfish (Lepomis auritis)populations exposed to industrial effluent andmutagenicity of the associated sediments weredetermined in order to compare them to changes incommunity structure. Data were collected from areference stream and East Fork Poplar Creek (EFPC), afirst-order stream which originates on the grounds ofthe Department of Energy Y-12 Plant at Oak Ridge, TN. This stream is contaminated with mercury, PCBs, andnumerous other compounds. Previous studies have shownthat sediment contaminant concentrations, as well asphysiological biomarker responses of the local fishpopulations, are highest at the headwaters of EFPC anddecrease with increasing distance from the DOEfacility as contaminant loading decreases. Chromosomal damage was measured by flow cytometry – asreflected by variation in cellular DNA content – andstrand breakage was determined by agarose gelelectrophoresis using blood as the source of DNA. Mutagenicity was determined by theSalmonella/microsome assay using organic solventextracts of sediment surface samples. Community levelresponses included community diversity and percentpollution-tolerant species. Biomarker responses andmutagenicity were found to be highest at theheadwaters of EFPC, and tended to decrease withincreasing distance from the effluent. In general,biomarker responses appeared to be correlated withmutagenicity of the sediment, and both of theserelated to fish community disturbance and level ofstream contamination. Because responses at severallevels of biological organization show similarpatterns of downstream effects, this suggests thatthere may be a causal relationship betweencontamination and biological effects.

This is a preview of subscription content, access via your institution.

References

  • Adams, S.M., K.L. Shepard, M.S Greeley., B.D. Jimenez, M.G Ryon, L.R. Shugart, J.F. McCarthy & D.E. Hinton, 1989. The use of bioindicators for assessing the effects of pollutant stress on fish. Mar. Environ. Res. 28: 459–464.

    Google Scholar 

  • Adams, S.M., W.D. Crumby, M.S. Greeley, L.R. Shugart & C.F. Saylor, 1989. Responses of fish populations and communities to pulp-mill effluents – a holistic assessment. Ecotox. Environ. Saf. 24: 347–360.

    Google Scholar 

  • Adams, S.M., W.D. Crumby, M.S. Greeley Jr., M.G. Ryan, & E.M. Shiling, 1992. Relationships between physiological and fish population responses in a contaminated stream. Environ. Toxicol. Chem. 11: 1549–1557.

    Google Scholar 

  • Adams, S.M., K.D. Ham, M.S. Greeley, R.F. LeHew, D.E. Hinton & C.F. Saylor, 1996. Downstream gradients in bioindicator responses: Point source contaminant effects on fish health. Can. J. Fish. Aquat. Sci. 53: 2177–2187.

    Google Scholar 

  • Ames, B.N., J. McCann & E. Yamasaki, 1975. Methods for detecting carcinogens and mutagens with the Salmonella/mammalian-microsome mutagenicity test. Mut. Res. 31: 347–364.

    Google Scholar 

  • Ashby, J., 1991. Determination of the genotoxic status of a chemical. Mut. Res. 248: 221–231.

    Google Scholar 

  • Barja, G., 1998. Mitochondrial free radical production and aging in mammals and birds. Ann. NY Acad. Sci. 854: 224–238.

    Google Scholar 

  • Bickham, J.W., 1990. Flow cytometry as a technique to monitor the effects of environmental genotoxins on wildlife populations. In: S. Sandhu, W.R. Lower, F.J. DeSerres, W.A. Suk & R.R. Tice (eds), In Situ Evaluation of Biological Hazard of Environmental Pollutants, Environmental Research Series Vol. 38. Plenum Press, New York, pp. 97–108.

    Google Scholar 

  • Bickham, J.W., J.A. Mazet, J. Blake, M.J. Smolen, Y. Lou & B.E. Ballachey, 1998. Flow cytometric determination of genotoxic effects of exposure to petroleum in mink and sea otters. Ecotoxicology 7: 191–199.

    Google Scholar 

  • Black, M.C., J.R. Ferrell, R.C. Homing & L.K. Martin, Jr., 1996. DNA strand breakage in freshwater mussels (Anodonta granis) exposed to lead in the laboratory and field. Environ. Toxicol. Chem. 15: 802–808.

    Google Scholar 

  • Custer, T.W., J.W. Bickham, T.B. Lyne, T. Lewis, L.A. Ruedas, C.M. Custer & M.J. Melancon, 1994. Flow cytometry for monitoring contaminant exposure in black-crowned night herons. Arch. Environ. Contam. Toxicol. 27: 176–179.

    Google Scholar 

  • DeMarini, D.M., D.A. Bell, J.G. Levine, M.L. Shelton & A. Abu-Shakra, 1993. Molecular analysis of mutations induced at the his3052 allele of Salmonella by single chemicals and complex mixtures. Environ. Health Perspec. 101: 207–212, Suppl. 3.

    Google Scholar 

  • Donnelly, K.C., J.C. Thomas & K.W. Brown, 1995. Mutagenic potential of environmental-samples before and after remediation of a solvent-contaminated site. Environ. Toxicol. Chem. 14(8): 1281–1286.

    Google Scholar 

  • Espina, N.G. & P. Weis, 1995. DNA-repair in fish from polluted estuaries. Mar. Environ. Res. 39: 309–312.

    Google Scholar 

  • Feeley, M.M., 1995. Biomarkers for Great Lakes priority contaminants: Halogenated aromatic hydrocarbons. Environ. Health Perspect. 103: 7–16, Suppl. 9.

    Google Scholar 

  • Freeman, S.E. & B.D. Thompson, 1990. Quantitation of ultraviolet radiation-induced cyclobutyl pyrimidine dimers in DNA by video and photographic densitometry. Anal. Bioch. 186: 222–228.

    Google Scholar 

  • Freidberg, E.C., 1985. DNA Repair. Plenum Press, New York.

    Google Scholar 

  • Hinzman, R.L. (ed.), 1993. Second report on the Oak Ridge Y-12 plant biological monitoring and abatement program for East Fork Poplar Creek. Y/TS-888 Report. Oak Ridge Y-12 Plant, Oak Ridge, TN.

    Google Scholar 

  • Hollander, M. and D.A. Wolfe, 1973. Nonparametric Statistical Methods. John Wiley & Sons, New York.

    Google Scholar 

  • Huggett, R.J., R.A. Kimerle, P.M. Mehrle, Jr. & H.L. Bergman (eds), 1992. Biomarkers: Biochemical, Physiological, and Histological Markers of Anthropogenic Stress. Lewis Publishers, Boca Raton, FL.

    Google Scholar 

  • Kampf, G. and K. Eichhorn, 1983. DNA strand breakage by different radiation qualities and relations to cell killing. Stud. Biophys. 93: 17–26.

    Google Scholar 

  • Karr, J.R., 1991. Biological integrity – a long-neglected aspect of water-resource management. Ecol. Appl. 1(1): 66–84.

    Google Scholar 

  • Kedwards, T.J., S.J. Maund & P.F. Chapman, 1999. Community level analysis of ecotoxicological field studies: I. Biological monitoring. Environ. Toxicol. Chem. 18: 149–157.

    Google Scholar 

  • Krebs, C.J., 1989. Ecological Methodology. Harper and Collins Publishers, New York.

    Google Scholar 

  • Kraft, G., W. Kraft-Weyrather, S. Ritter, M. Scholz & T. Stanton, 1989. Cellular and subcellular effects of heavy ions: a comparison of induction of strand breaks and chromosomal aberrations with the incidence of inactivation and mutation. Ad. Space Res. 9: 641–648.

    Google Scholar 

  • Lamb, T., J.W. Bickham, T.B. Lyne & J.W. Gibbons, 1995. The slider turtle as an environmental sentinel: Multiple tissue assays using flow cytometric analysis. Ecotoxicology 4: 5–13.

    Google Scholar 

  • Maron, D.M. & B.N. Ames, 1983. Revised methods for the Salmonella mutagenicity test. Mut. Res. 113: 173–215.

    Google Scholar 

  • Nadig, S.G., K.L. Lee & S.M. Adams, 1998. Evaluating alterations of genetic diversity in sunfish populations exposed to contaminants using RAPD assay. Aquat. Toxicol. 43(2–3): 163–178.

    Google Scholar 

  • Newman, M.C. & C.H. Jagoe (eds), 1996. Ecotoxicology: A Hierarchical Treatment. Lewis Publishers, Boca Raton, FL.

    Google Scholar 

  • Ohio EPA, 1988. Biological Criteria for the Protection of Aquatic Life: Volume II: Users Manual for Biological Field Assessment of Ohio Surface Waters. Division of Water Quality Monitoring and Assessment, Columbus, OH.

    Google Scholar 

  • Olive, P.L., 1998. The role of DNA single-and double-strand breaks in cell killing by ionizing radiation. Radiat. Res. 150: S42–S51, Suppl. S.

    Google Scholar 

  • Plafkin, J.L., M.T. Barbour, K.D. Porter, S.K. Gross & R.M. Hughes, 1989. Rapid Bioassessment Protocols for Use in Streams and Rivers. Benthic Macroinvertebrates and Fish. U.S. Environmental Protection Agency, EPA-440/4-891001.

  • Roesijadi, G. 1994. Metallothionein induction as a measure of response to metal exposure in aquatic animals. Environ. Health. Persp. 102: 91–95, Suppl. 12.

    Google Scholar 

  • Shugart, L.R., M.K. Gustin, D.M. Laird & D.A. Dean. 1989. Susceptibility of DNA in aquatic organisms to strand breakage: Effect of X-rays and gamma radiation. Mar. Environ. Res. 28: 339–343.

    Google Scholar 

  • Shugart, L.R., J. Bickham, G. Jackim, G. McMahon, W. Ridley, J. Stein & S. Steinert, 1992. DNA alterations. In: R.J. Huggett, R.A. Kimerle, P.M. Mehrle, Jr. & H.L. Bergman (eds), Biomarkers: Biochemical, Physiological, and Histological markers of Anthropogenic Stress. Lewis Publishers, Boca Raton, FL. pp. 125–154.

    Google Scholar 

  • Steinert, S.A., R. Streib-Montee, J.M. Leather & D.B. Chadwick, 1998. DNA damage in mussels at sites in San Diego Bay. Mutat. Res.-Fund. Mol. M. 399:(1) 65–85.

    Google Scholar 

  • Suter, G.W. 1993. A critique of ecosystem health concepts and indexes. Environ. Toxicol. Chem. 12: 1533–1539.

    Google Scholar 

  • Theodorakis, C.W., B.G. Blaylock & L.R. Shugart, 1996. Genetic ecotoxicology I.: DNA integrity and reproduction in mosquitofish exposed in situ to radionuclides. Ecotoxicology 5: 1–14.

    Google Scholar 

  • Theodorakis, C.W. & L.R. Shugart, 1993. Detection of genotoxic insult as DNA strand breaks in fish blood cells by agarose gel electrophoresis. Environ. Toxicol. Chem. 13: 1023–1031.

    Google Scholar 

  • Theodorakis, C.W., S.J. D'surney, J.W. Bickham, T.B. Lyne, B.P. Bradley, W.E. Hawkins, W.L. Farkas, J.F. McCarthy & L.R. Shugart, 1992. Sequential expression of biomarkers in bluegill sunfish exposed to contaminated sediment. Ecotoxicology 1: 45–73.

    Google Scholar 

  • USEPA SW846 version 2. Test Methods for Evaluating Solid Waste: Physical/Chemical Methods. National Technical Information Service. Dec 1997.

  • VanWinkle, W., K.A. Rose, K.O. Winemiller, D.L. DeAngelis, S.W. Christensen, R.G. Otto & B.J. Shuter, 1993. Linking life-history theory, environmental setting, and individual-based modeling to compare responses of different fish species to environmental change. T. Am. Fish. Soc. 122: 459–466.

    Google Scholar 

  • Vindelov, L.L., I.J. Christianson, N. Keiding, M. Prang-Thomsen & N.I. Nissen, 1983. Long-term storage of samples for flow cytometric DNA analysis. Cytometry 3: 317–320.

    Google Scholar 

  • Vindelov, L.L. & I.J. Christensen, 1990. A review of techniques and results obtained in one laboratory by an integrated system of methods designed for routine clinical flow cytometric DNA analysis. Cytometry 11: 753–770.

    Google Scholar 

  • Ward, J.F., 1988. DNA damage produced by ionizing radiation in mammalian cells: Identities, mechanisms of formation, and repairability. Prog. Nucl. Acid. Res. Mol. Biol. 35: 95–125.

    Google Scholar 

  • Wickliffe, J.K. & J.W. Bickham, 1998. Flow cytometric analysis of hematocytes from brown pelicans (Pelecanus occidentalis) exposed to planar halogenated hydrocarbons and heavy metals. Bull. Environ. Contam. Toxicol. 61: 239–246.

    Google Scholar 

  • Wirgin, I. & J.R. Waldman, 1998. Altered gene expression and genetic damage in North American fish populations. Mutat. Res.-Fund. Mol. M. 399: 193–219.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Theodorakis, C.W., Swartz, C.D., Rogers, W.J. et al. Relationship between genotoxicity, mutagenicity, and fish community structure in a contaminated stream. Journal of Aquatic Ecosystem Stress and Recovery 7, 131–143 (2000). https://doi.org/10.1023/A:1009971330138

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009971330138

  • genotoxicity
  • DNA damage
  • community structure
  • mutagenicity
  • Lepomis auritis