The Significance of Mutagenicity as a Criterion in Ecotoxicological Evaluations

  • W. K. de Raat
  • G. J. Vink
  • A. O. Hanstveit
Part of the Environmental Science Research book series (ESRH, volume 39)


To date environmental mutagenesis has been a predominantly anthropocentric discipline of toxicology. It is ultimately motivated by the fear of human exposure to carcinogens and mutagens. Exposure of and effects in other organisms are regarded as relevant as far as they indicate exposure of and effects in humans. The ecotoxicologically relevant effects, i.e., changes of the structure and function (quality) of ecosystems caused by environmental pollution with mutagens, receive far less attention. Nevertheless, only these effects justify the inclusion of mutagenicity as a criterion in ecotoxicological evaluations. Both these effects and the extent to which they support an ecotoxicological role of mutagenicity tests, are the central themes of this paper.

First, a short treatment of ecotoxicology and the characteristic differences between this branch of toxicology and human toxicology is given; ecotoxicological evaluations for the aquatic environment will be briefly touched upon. Then the ecotoxicologically relevant effects of mutagens in aquatic ecosystems will be discussed. They can be split up into two groups: those that will not and those that will escape detection in an adequate set of conventional ecotoxicity tests. The first includes effects on division rate of unicellular organisms, reproduction of multicellular organisms, and survival; the second, cancer and the long-term (multigeneration) effects of an increased mutational load. It is concluded that, with respect to the first group of effects, mutagenicity tests can only be used as prescreening, alerting, and supporting tests; mutagenicity may play a role in its own right with respect to cancer and increased mutational load.

Additional arguments for the inclusion of mutagenicity in ecotoxicological evaluations are provided for by the actual pollution and effects encountered in the aquatic environment.


Mytilus Edulis Sister Chromatid Exchange Conventional Test Unicellular Organism Mutational Load 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Albert, R.E., J. Lewtas, S. Nesnow, T.W. Thorslund, and E. Anderson (1983) Comparative potency method for cancer risk assessment: Application to diesel particulate emissions. Risk Analysis 3:101–117.CrossRefGoogle Scholar
  2. 2.
    Alink, G.M., E.M.H. Frederix-Wolters, M.A. van der Gaag, J.F. van de Kerkhoff and C.L.M. Poels (1980) Induction of sister chromatic exchanges in fish exposed to Rhinewater. Mutat. Res. 78:369–374.PubMedCrossRefGoogle Scholar
  3. 3.
    Bayne, B.L., D.A. Brown, K. Burns, D.R. Dixon, A. Ivanovici, D.R. Livingstone, D.M. Lower, M.N. Moore, A.R.D. Stebbing, and J. Widdows (1985) The Effects of Stress and Pollution on Marine Animals. Praeger Press, New York.Google Scholar
  4. 4.
    Bergman, H.L., R.A. Kimerle, and A.W. Maki (1986) Environmental Hazard Assessment of Effluents. SETAC Special Publication Series. Pergamon Press, New York.Google Scholar
  5. 5.
    Bitton, G., and B.J. Dutka, eds. (1986) Toxicity Testing Using Microorganisms, Vol. 1. CRC Press, Inc., Boca Raton, Florida.Google Scholar
  6. 6.
    Brown, K.W., and K.C. Donnelly (1984) Mutagenic activity of run-off and leachate water from hazardous waste land treatment. Envir. Poll. 35:229–246.CrossRefGoogle Scholar
  7. 7.
    Brunetti, R., J. Gola, and F. Majone (1986) Sister-chromatid exchange in developing eggs of Mytilus galloprovincialis Bivalvia. Mutat. Res. 174:207–212.CrossRefGoogle Scholar
  8. 8.
    Cairns, J., K.L. Dickson, and A.W. Maki, eds. (1978) Estimating the Hazard of Chemical Substances to Aquatic Life, American Society for Testing and Materials (ASTM), Philadelphia.Google Scholar
  9. 9.
    Connell, D.W. and G.J. Miller (1984) Chemistry and Ecotoxicology of Pollution, Environmental Science and Technology Series, Wiley Interscience, New York.Google Scholar
  10. 10.
    Conway, R.A., ed. (1982) Environmental Risk Analysis for Chemicals. Van Nostr and Reinhold Environmental Engineering Series, Van Nostrand Reinhold, New York.Google Scholar
  11. 11.
    Conway, R.A. (1982) Introduction to environmental risk analysis. In Environmental Risk Analysis for Chemicals, R.A. Conway, ed., Van Nostr and Reinhold, New York.Google Scholar
  12. 12.
    Couch, J.A., W.P. Schoor, L. Courtney, and W. Davis (1984) Effects of Carcinogens, Mutagens and Teratogens on Non-Human Species (Aquatic Animals). Final Report, Project 3, NCI/EPA Collaborative Program, U.S. EPA, Gulf Breeze, Florida.Google Scholar
  13. 13.
    Dixon, D.R., and K.R. Clarke (1982) Sister-chromatid exchange: A sensitive method for detecting damage caused by exposure to environmental mutagens in the chromosomes of adult Mytilus edulis. Mar. Biol. Lett. 3:163–172.Google Scholar
  14. 14.
    Dixon, D.R. (1986) Promotoceres triqueter: A test system for environmental mutagenesis. In The Effects of Stress and Pollution on Marine Animals. Praeger Press, New York.Google Scholar
  15. 15.
    Dixon, D.R. (1982) Aneuploidy in mussel embryos (Mytilusedulis) originating from a polluted dock. Mar. Biol. Lett. 3:155–161.Google Scholar
  16. 16.
    Ellenton, J.A., M.F. McPherson, and K.L. Mans (1983) Mutagenicity studies on herring gulls from different locations on the Great Lakes. 2. Mutagenic evaluation of extracts of herring gull eggs in a battery of in-vitro mammalian and microbial tests. J. Toxic. Env. Health 12:325–336.CrossRefGoogle Scholar
  17. 17.
    Fang, T., T.-H. Ma, G. Lin, J. Ho, J. Dai, R. Zhou, D. Chen, Y. Ou, and J. Cui (1983) Preliminary report on the development of a bioassay for detection on mutagens in sea water. Envir. Exp. Bot. 23:303–310.CrossRefGoogle Scholar
  18. 18.
    Gaag, M.A. van der, A. Noordsij, and J.P. Oranje (1982) Presence of mutagens in Dutch surface water and effects of water treatment processes for drinking water preparation. In Mutagens in Our Environment, M. Sorsa and H. Vainio, eds. Alan R. Liss, New York.Google Scholar
  19. 19.
    Gaag, M.A. van der, A. Noordsij, and C.L.M. Poels (1982) Mutagenicity of River Rhinewater in The Netherlands and influence of several water treatment processes on the mutagenic effect. Mutat. Res. 97:231–232.Google Scholar
  20. 20.
    Guttmann-Bass, N., M. Bairey-Albuqeurque, S. Ulitzur, A. Chartrand, and C. Rav-Acha (1987) Effects of chlorine and chlorine dioxide on mutagenic activity of Lake Kinnereth water. Env. Sci. Tech. 21:252–260.CrossRefGoogle Scholar
  21. 21.
    Harrison, F.L., and J.M. Jones (1982) An in-vivo sister-chromatid exchange assay in the larvae of the mussel Mytilus edulis: Response to three mutagens. Mutat. Res. 105:235–242.PubMedCrossRefGoogle Scholar
  22. 22.
    Heartlein, M.W., D.M. Demarini, A.J. Katz, J.C. Means, M.J. Plewa, and H.E. Brochman (1981) Mutagenicity of municipal water obtained from an agricultural area. Env. Mut. 3:519–530.CrossRefGoogle Scholar
  23. 23.
    Hoffmann, G.R. (1982) Mutagenicity testing in environmental toxicology. Env. Sci. Tech. 16:560A-574A.CrossRefGoogle Scholar
  24. 24.
    Hoof, F., van and J. Verheyden (1981) Mutagenic activity in the Meuse River in Belgium. Sci. Total Env. 20:15–22.Google Scholar
  25. 25.
    Hooftman, R.N., and G.J. Vink (1981) Cytogenetic effects on the eastern mudminnow, Umbrapy gmeae, exposed to ethylmethanesulphonate, benzo(a)pyrene and river water. Ecotox. Env. Safety 5:261–269.CrossRefGoogle Scholar
  26. 26.
    Hooftman, R.N., and W.K. de Raat (1982) Induction of nuclear anomalies (micronuclei) in the peripheral blood erythrocytes of the eastern mudminnow Umbra pygmaeaby ethylmethanesulphonate. Mutat. Res. 104:147–152.PubMedCrossRefGoogle Scholar
  27. 27.
    Hooftman, R.N. (1981) The induction of chromosome aberrations in Notobranchius rachowi (Pisces: Cyprinodontidae) after treatment with ethylmethanesulphonate or benzo(a)pyrene. Mutat. Res. 191:347.CrossRefGoogle Scholar
  28. 28.
    Hopke, P.K., M.J. Plewa, and P. Stapleton (1987) Reduction of mutagenicity of municipal waste waters by land treatment. Sci. Total Env. 66:193–202.CrossRefGoogle Scholar
  29. 29.
    Hueck-van derPlas, E.H., ed. (1981) Disposal of chemical waste in the marine environment. Implications of the International Dumping Conventions. Chemosphere 10(6).Google Scholar
  30. 30.
    ICPEMC (1988) Testing for mutagens and carcinogens: The role of short-term genotoxicity assays. ICPEMC Publication No. 16. Mutat. Res. 205:3–12 (and other papers in this issue of Mutation Research).Google Scholar
  31. 31.
    Jabar, M.A., M.A. Salama, and A. Salem (1984) The detection of mutagenic pollutants in marine organisms of Kuwait. Water Air Soil Poll. 22:131–142.Google Scholar
  32. 32.
    Kadhim, M., and J.M. Parry (1984) The detection of mutagenic chemicals in the tissues of shellfish exposed to oil pollution. Mutat. Res. 136:93–105.PubMedCrossRefGoogle Scholar
  33. 33.
    Kamiya, A., and J. Ose (1987) Study of the behaviour of mutagens in waste water and emission gas from a municipal incinerator evaluated by means of the Ames assay. Sci. Total Env. 65:109–120.CrossRefGoogle Scholar
  34. 34.
    Karim Ahmed, A., and G.S. Domiquez (1982) The development of testing requirements under the toxic substances control act. In Environmental Risk Analysis for Chemicals, R.A. Conway, ed., Van Nostr and Reinhold, New York.Google Scholar
  35. 35.
    Kelly, J.J., and M.B. Maddock (1985) In-vitro induction of unscheduled DNA synthesis by genotoxic carcinogens in the hepatocytes of the oyster toadfish Opsanus-tau. Arch. Env. Contam. Tox. 14:555–564.CrossRefGoogle Scholar
  36. 36.
    Kinae, N., T. Hashizume, T. Nakita, I. Tomita, I. Kimura, and H. Kanamori (1981) The toxicity of pulp and paper mill effluents. 2. Mutagenicity of the extracts of the liver from spotted sea trout Nibea mitsukurjii. Water Res. 15:25–30.CrossRefGoogle Scholar
  37. 37.
    Klekowski, E.J., and D.M. Poppel (1976) Ferns potential in-situ bioassay systems for aquatic-borne mutagens. Am. Fern. J. 66:75–79.CrossRefGoogle Scholar
  38. 38.
    Klekowski, E.J. (1976) Mutational load in a fern population growing in a polluted environment. Am. J. Bot. 63:1024–1030.CrossRefGoogle Scholar
  39. 39.
    Kligerman, A.D., S.E. Bloom, and W.M. Howell (1975) Umbralimi: A model for the study of chromosome aberrations in fishes. Mutat. Res. 31:225.PubMedGoogle Scholar
  40. 40.
    Kligerman, A.D. (1979) Induction of sister-chromatid exchanges in the central mudminnow following in vivo exposure to mutagenic agents. Mutat. Res. 64:205.PubMedGoogle Scholar
  41. 41.
    Kocan, R.M., K.M. Sabo, and M.L. Landolt (1985) Cytotoxicity/genotoxicity: The application of cell culture techniques to measurement of marine sediment pollution. AquaticTox. 6:165–177.Google Scholar
  42. 42.
    Kooijman, S.A.L.M. (1985) Toxicity at population level. In Proceedings of the ESA/SETAC Symposium on Multispecies Toxicity Testing, J. Cairns, ed. Pergamon, New York.Google Scholar
  43. 43.
    Koojiman, S.A.L.M. (1984) On the dynamics of chemically stressed populations: The deduction of population consequences from effects on individuals. Ecotox. Env. Safety 8:254.CrossRefGoogle Scholar
  44. 44.
    Kooijman, S.A.L.M. (1987) A safety factor for LC50 values allowing for differences in sensitivity among species. Water Res. 3:269–276.CrossRefGoogle Scholar
  45. 45.
    Kreijl, C.F. van, H.J. Kool, M. de Vries, H.J. Kranen, and E. de Greef (1980) Mutagenic activity in the Rivers Rhine and Meuse in The Netherlands. Sci. Total Env. 15:137–147.CrossRefGoogle Scholar
  46. 46.
    Kreijl, C.F. van, A.C. van den Burg, and W. Sloof (1982) Accumulation of mutagenic activity in bile fluid of River Rhine fish. In Mutagens in Our Environment, M. Sorsa and H. Vainio, eds. Alan R. Liss, New York.Google Scholar
  47. 47.
    Kringstad, K.P., P.O. Ljungquist, F. de Sousa, and L.M. Stromberg (1981) Identification and mutagenic properties of some chlorinated aliphatic compounds in the spent liquor from kraft pulp chlorination. Env. Sci. Tech. 15:562–566.CrossRefGoogle Scholar
  48. 48.
    Kuiper, J. (1982) The use of enclosed plankton communities in aquatic ecotoxicology. Thesis, Agricultural University, Wageningen, The Netherlands.Google Scholar
  49. 49.
    Langi, A., and M. Priha (1988) Mutagenicity in pulp and paper mill effluents and in recipient. Water Sci. and Tech. 20:143–152.Google Scholar
  50. 50.
    Leisinger, T., A.M. Cook, R. Hutter, and J. Nuesch, eds. (1981) Microbial Degradation of Xenobiotics and Recalcitrant Compounds. Academic Press, London.Google Scholar
  51. 51.
    Maddock, M.B., H. Northup, and T.J. Ellingham (1986) Induction of sister-chromatid exchanges and chromosomal abberations in hematopoietic tissue of a marine fish following in-vivo exposure to genotoxic carcinogens. Mutat. Res. 172:165–176.PubMedCrossRefGoogle Scholar
  52. 52.
    Maki, A.W., K.L. Dickson, and J. Cairns, Jr., eds. (1980) Biotransformation and Fate of Chemicals in the Aquatic Environment. American Society for Microbiology, Washington, D.C.Google Scholar
  53. 53.
    Malins, D.C., B.B. McClain, J.T. Landahl, M.S. Myers, M.M. Krahn, D.W. Brown, S.-L. Chan, and W.T. Roubal (1988) Neoplastic and other diseases in fish in relation to toxic chemicals: An Overview. Aquatic Tox. 11:43–67.CrossRefGoogle Scholar
  54. 54.
    Maruoka, S., S. Yamanaka, and Y. Yamamoto (1986) Isolation of mutagenic components by high-performance liquid chromatography from XAD extract of water from the Nishitakase River, Kyoto City, Japan. Sci. Total Env. 57:29–38.CrossRefGoogle Scholar
  55. 55.
    Maruoka, S., and S. Yamanaka (1982) Mutagenicity in Salmonella typhimurium tester strains of XAD-2 resin ether extracts recovered from Katsura River water in Kyoto City, Japan and its fractions. Mutat. Res. 102:13–26.PubMedCrossRefGoogle Scholar
  56. 56.
    McCain, B.B., D.W. Brown, M.M. Krahn, M.S. Myers, R.C. Clark, Jr., S.-L. Chan, and D.C. Malins (1988) Marine pollution problems, North American West coast. Aquat. Tox. 11:143–162.CrossRefGoogle Scholar
  57. 57.
    Meier, J.R., W.F. Blazak, E.S. Ricio, B.E. Stewart, D.F. Bishop, and L.W. Condie (1987) Genotoxie properties of municipal waste waters in Ohio. Arch. Env. Cont. Tox. 16:671–680.CrossRefGoogle Scholar
  58. 58.
    Mersch-Sundermann, V., N. Diekgiesser, K. Koetter, and M. Harre (1988) The mutagenicity of surface water, waste water and drinking water in the Rhine-Neckar region with the Salmonella microsome Ames-test. Zentralbl. Bakteriol. Mikrobiol. Hyg. Ser. B 185:397–410.Google Scholar
  59. 59.
    Miller, E.C., and J.A. Miller, 1972 The mutagenicity of chemical carcinogens: Correlation, Problems and Interpretations. In Chemical Mutagens, Vol. I A. Hollaender, ed., Plenum Publishing Corp., New York.Google Scholar
  60. 60.
    Mix, M.C. (1986) Cancerous diseases in aquatic animals and their association with environmental pollutants: A critical literature review. Mar. Env. Res. (special issue), 20:1–141.CrossRefGoogle Scholar
  61. 61.
    Mix, M.C. (1988) Shellfish diseases in relation to toxic chemicals. Aquat. Tox. 11:29–42.CrossRefGoogle Scholar
  62. 62.
    Muellerschoen, H., and H.G. Miltenburger (1988) Detection of mutagens in water samples using the cell line V79. Vom Wasser. 71:195–206.Google Scholar
  63. 63.
    Osborne, L.L., R.W. Davies, K.R. Dixon, and R.L. Moore (1982) Mutagenic activity of fish and sediments in the Sheep River Alberta Canada. Water Res. 16:889–902.CrossRefGoogle Scholar
  64. 64.
    Pancorbo, O.C, P.J. Lein, and R.D. Blevins (1987) Mutagenic activity of surface waters adjacent to a nuclear fuel processing facility. Arch. Env. Contam. Tox. 16:531–537.CrossRefGoogle Scholar
  65. 65.
    Parry, J.M., D.J. Tweats, and MA.J. Al-Mossawi (1976) Monitoring the marine environment for mutagens. Nature 246:538–540.CrossRefGoogle Scholar
  66. 66.
    Pesch, G.G., C.E. Pesch, and A.R. Malcolm (1981) Neanthes arenaceondentata, a cytogenetic model for marine genetic toxicology. Aquat. Tox. 1:301–312.CrossRefGoogle Scholar
  67. 67.
    Prein, A.E., G.M. Thie, G.M. Alink, J.H. Koeman, and C.L.M. Poels (1978) Cytogenic changes in fish exposed to water of the River Rhine. Sci. Total. Env. 9:287–292.CrossRefGoogle Scholar
  68. 68.
    Raat, W.K. de, A.O. Hanstveit, and J.F. de Kreuk (1985) The role of mutagenicity testing in the ecotoxicological evaluation of industrial discharges into the aquatic environment. Food & Chem. Tox. 23:33–41.CrossRefGoogle Scholar
  69. 69.
    Rappaport, S.M., M.G. Richard, M.C. Hollstein, and R.E. Talcott (1979) Mutagenic activity in organic waste water concentrates. Env. Sci. Tech. 13:957–961.CrossRefGoogle Scholar
  70. 70.
    Reinhard, M., M. Goodman, and K.E. Mortelmans (1982) Occurrence of brominated alkylphenol polyethoxy carboxylates in mutagenic waste water concentrates. Env. Sci. Tech. 16:351–362.CrossRefGoogle Scholar
  71. 71.
    Saxena, J., D.J. Schwartz, and M.W. Neal (1979) Occurrence of mutagens/carcinogens in municipal waste waters and their removal during advanced waste water treatment. In Proceedings of Water Reuse Symposium, AWWA Research Foundation, Denver, Colorado, Vol. 3, 2209–2229.Google Scholar
  72. 72.
    Sims, R.C., J.L. Sims, and R.R. Dupont (1988) Human health effect assays. J. Water Poll. Cont. Fed. 16:1093–1106.Google Scholar
  73. 73.
    Sims, R.C., J.L. Sims, and R.R. Dupont (1985) Human health effect assays. J. Water Poll. Cont. Fed. 57:728–742.Google Scholar
  74. 74.
    Slooff, W., J.A.M. van Oers, and D. de Zwart (1986) Margins of uncertainty in ecotoxicological hazard assessment Env. Tox. Chem 5:841–852.CrossRefGoogle Scholar
  75. 75.
    Slooff, W. (1983) A study on the usefulness of feral fish as indicators for the presence of chemical carcinogens in Dutch surface waters. Aquat. Tox. 3:127–139.CrossRefGoogle Scholar
  76. 76.
    Slooff, W., and C.F. van Kreijl (1982) Monitoring the Rivers Rhine and Meuse in The Netherlands for mutagenic activity using the Ames test in combination with rat or fish liver homogenates. Aquatic Tox. 2:89–98.CrossRefGoogle Scholar
  77. 77.
    Spacie, A., and J.L. Hamelink (1985) Bioaccumulation. In Fundamentals of Aquatic Toxicology, G.M. Randand S.R. Petrocelli, eds., Hemisphere, Washington, D.C.Google Scholar
  78. 78.
    Swanson, S., and K. Peterson (1988) Development of Guidelines for Testing Pesticide Toxicity to Non-target Plants. Environment Canada, SRC Publication No. E-901–20-E-81.Google Scholar
  79. 79.
    Suzuki, J., T. Sadamasu, and S. Suzuki (1982) Mutagenic activity of organic matter in urban river sediment. Env. Pollut., Ser. A, Ecol. Biol. 29:91–100.CrossRefGoogle Scholar
  80. 80.
    Timourian, H., J.S. Felton, D.H. Stuermer, S. Healy, P. Berry, and M. Tompkins (1982) Mutagenic and toxic activity of environmental effluents from underground coal gasification experiments. J. Tox. Env. Health 9:975–994.CrossRefGoogle Scholar
  81. 81.
    TNO (the Dutch Organization for Applied Scientific Research) (1980) Degradability, Ecotoxicity and Bioaccumulation. The Determination of the Possible Effects of Chemicals and Wastes on the Aquatic Environment. Government Publishing Office, The Hague.Google Scholar
  82. 82.
    Vargas, V.M., V.E.P. Motta, and J.A.P. Henriques (1988) Analysis of mutagenicity of waters under the influence of petrochemical industrial complexes by the Salmonella-microsome test. Rev. Bras. Genet. 11:505–518.Google Scholar
  83. 83.
    Venegas, W., I. Hermosilla, J.F. Gavilan, R. Naveas, and P. Carrasco (1987) Larval stages of the anuran amphibian Caudiverbera caudiverbera: A biological model for studies of genotoxic agents. Bol. Soc. Biol. Conception 58:171–180.Google Scholar
  84. 84.
    Vethaak, A.D. (1985) Inventory to the Presence of Dish Diseases in Relation to Pollution in Dutch Coastal Waters (in Dutch). Report of the Netherlands Institute for Fishery Research. IJmuiden, No. CA 85–01.Google Scholar
  85. 85.
    Walden, C.C. (1981) Biological effects on pulp and paper-mill effluents. In Advances in Biotechnology, Vol. 2., M. Moo-Young and C.W. Robinson, eds., Pergamon Press, Canada.Google Scholar
  86. 86.
    West, W.R., P.A. Smith, G.M. Booth, and M.L. Lee (1988) Isolation and detection of genotoxic components in a Black River sediment. Env. Sci. Tech. 22:224–228.CrossRefGoogle Scholar
  87. 87.
    Zahn, R.K., G. Zahn-Daimler, W.E.G. Muller, M.L. Michaelis, B. Kurelec, M. Rijavec, R. Batel, and N. Bihari (1983) DNA damage by PAH and repair in a marine sponge. Sci. Total. Env. 26:137–156.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • W. K. de Raat
    • 1
  • G. J. Vink
    • 1
  • A. O. Hanstveit
    • 1
  1. 1.Division of Technology for Society TNOBiological DepartmentDelftThe Netherlands

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