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Ecotoxicology

, Volume 9, Issue 6, pp 383–397 | Cite as

Effects of Endocrine Disruptors on Prosobranch Snails (Mollusca: Gastropoda) in the Laboratory. Part I: Bisphenol A and Octylphenol as Xeno-Estrogens

  • Jörg Oehlmann
  • Ulrike Schulte-Oehlmann
  • Michaela Tillmann
  • Bernd Markert
Article

Abstract

The effects of suspected endocrine disrupting chemicals on freshwater and marine prosobranch species were analysed in laboratory experiments. In this first publication, the responses of the freshwater snail Marisa cornuarietis and of the marine prosobranch Nucella lapillus to the xeno-estrogenic model compounds bisphenol A (BPA) and octylphenol (OP) are presented at nominal concentration ranges between 1 and 100 μg/L. Marisa was exposed during 5 months using adult specimens and in a complete life-cycle test for 12 months. In both experiments, the xeno-estrogens induced a complex syndrome of alterations in female Marisa referred to as “superfemales” at the lowest concentrations. Affected specimens were characterised by the formation of additional female organs, an enlargement of the accessory pallial sex glands, gross malformations of the pallial oviduct section resulting in an increased female mortality, and a massive stimulation of oocyte and spawning mass production. The effects of BPA and OP were comparable at the same nominal concentrations. An exposure to OP resulted in inverted U-type concentration response relationships for egg and spawning mass production. Adult Nucella from the field were tested for three months in the laboratory. As in Marisa, superfemales with enlarged accessory pallial sex glands and an enhancement of oocyte production were observed. No oviduct malformations were found probably due to species differences in the gross anatomical structure of the pallial oviduct. A lower percentage of exposed specimens had ripe sperm stored in their vesicula seminalis and additionally male Nucella exhibited a reduced length of penis and prostate gland when compared to the control. Because statistically significant effects were observed at the lowest nominal test concentrations (1 μg BPA or OP/L), it can be assumed that even lower concentrations may have a negative impact on the snails. The results show that prosobranchs are sensitive to endocrine disruption at environmentally relevant concentrations and that especially M. cornuarietis is a promising candidate for a future organismic invertebrate model to identify endocrine-mimetic test compounds.

endocrine disruptors xeno-estrogens bisphenol A octylphenol snails 

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References

  1. Ahel, M., Giger, W. and Koch, M. (1994a). Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment—I. Occurrence and transformations in sewage treatment. Water Res. 28, 1131-42.Google Scholar
  2. Ahel, M., Giger, W. and Schaffner, C. (1994b). Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment—II. Occurrence and transformation in rivers. Water Res. 28, 1143-52.Google Scholar
  3. Andersen, H.R., Andersson, A.M., Arnold, S.F., Autrup, H., Barfoed, M., Beresford, N.A., Bjerregaard, P., Christiansen, L.B., Gissel, B., Hummel, R., Jorgensen, E.B., Korsgaard, B., Le Guevel, R., Leffers, H., McLachlan, J., Moller, A., Nielsen, J.B., Olea, N., Oles-Karasko, A., Pakdel, F., Pedersen, K.L., Perez, P., Skakkebaek, N.E., Sonnenschein, C., Soto, A.M., Sumpter, J.P., Thorpe, S.M. and Grandjean, P. (1999a). Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. Environ. Health Perspect. 107, (Suppl. 1), 89-108.Google Scholar
  4. Andersen, H.R., Halling-Sorensen, B. and Kusk, K.O. (1999b): A parameter for detecting estrogenic exposure in the copepod Acartia tonsa. Ecotoxicol. Environ. Saf. 44, 56-61.Google Scholar
  5. Ashby, J., Tinwell, H. and Haseman, J. (1999). Lack of effects for low dose levels of bisphenol A and diethylstilbestrol on the prostate gland of CF1 mice exposed in utero. Regul. Toxicol. Pharmacol. 30, 156-66.Google Scholar
  6. Bauer, B., Fioroni, P., Ide, I., Liebe, S., Oehlmann, J., Stroben, E. and Watermann, B. (1995). TBT effects on the female genital system of Littorina littorea: A possible indicator of tributyltin pollution. Hydrobiologia 309, 15-27.Google Scholar
  7. Bauer, B., Fioroni, P., Schulte-Oehlmann, U., Oehlmann, J. and Kalbfus, W. (1997). The use of Littorina littorea for tributyltin TBT effect monitoring—Results from the German TBT survey 1994/1995 and laboratory experiments. Environ. Pollut. 96, 299-309.Google Scholar
  8. Bettin, C., Oehlmann, J. and Stroben, E. (1996). TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgolander Meeresunters. 50, 299-317.Google Scholar
  9. BUA. (1991). Nonylphenol. Stoffbericht des Beratergremiums für umweltrelevante Altstoffe (BUA). Weinheim: VCH.Google Scholar
  10. BUA. (1997). Bisphenol A (2,2-Bis-(4-hydroxyphenyl propan). Stoffbericht 203 des Beratergremiums für umweltrelevante v Altstoffe (BUA). Stuttgart: S. Hirzel.Google Scholar
  11. Cagen, S.Z., Waechter, J.M., Dimond, S.S., Breslin, W.J., Butala, J.H., Jekat, F.W., Joiner, R.L., Shiotsuka, R.N., Veenstra, G.E. and Harris, L.R. (1999). Normal reproductive organ development in Wistar rats exposed to bisphenol A in the drinking water. Regul. Toxicol. Pharmacol. 30, 130-9.Google Scholar
  12. Caspers, N. (1998). No estrogenic effects of bisphenol A in Daphnia magna STRAUS. Bull. Environ. Contam. Toxicol. 61, 143-8.Google Scholar
  13. CES. (1993). Uses, fate and entry to the environment of nonylphenol ethoxylates. Report for the Department of the Environment UK by Consultants in Environmental Sciences Ltd, Beckenham.Google Scholar
  14. Clark, L.B., Rosen, R.T., Hartman, T.G., Louis, J.B., Suffet, I.H., Lippincott, R.L. and Rosen, J.D. (1992). Determination of alkylphenol ethoxylates and their acetic acid derivates in drinking water by particle beam liquid chromatography/mass spectrometry. Int. J. Environ. Anal. Chem. 147, 167-80.Google Scholar
  15. deFur, P.L., Crane, M., Ingersoll, C. and Tattersfield, L. (eds). (1999). Endocrine disruption in invertebrates: Endocrinology, testing, and assessment. In Proceedings of the Workshops on Endocrine Disruption in Invertebrates, 12-15 Dec. 1998, Noordwijkerhout, The Netherlands. Pensacola, FL: SETAC Press.Google Scholar
  16. Dodds, E.C. and Lawson, W. (1936). Synthetic estrogenic agents without the phenanthrene nucleus. Nature 137, 996.Google Scholar
  17. Dodds, E.C. and Lawson, W. (1938). Molecular structure in relation to oestrogenic activity. Compounds without a phenanthrene nucleus. Proc. Royal Soc. London B. 125, 222-32.Google Scholar
  18. Environment Agency. (1998). Endocrine-disrupting substances in wildlife: A review of the scientific evidence and strategic response— Environment Agency, Bristol. Publication No. HO-11/97–100-B-BANP.Google Scholar
  19. Gibbs, P.E., Bryan, G.W., Pascoe, P.L. and Burt, G.R. (1987). The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin TBT contamination. J. Mar. Biol. Ass. U.K. 67, 507-23.Google Scholar
  20. Giesy, J.P., Pierens, S.L., Snyder, E.M., Miles-Richardson, S., Kramer, V.J., Snyder, S.A., Nichols, K.M. and Villeneuve, D.A. (2000). Effects of 4-nonylphenol on fecundity and biomarkers of estrogenicity in fathead minnows (Pimephales promelas). Environ. Toxicol. Chem. 19, 1368-77.Google Scholar
  21. Gist, G.L. (1998). National Environmental Health Association position on endocrine disrupters-adopted July 2, 1997. J. Environ. Health 60, 21-3.Google Scholar
  22. Greim, H. (1998). Hormonahnlich wirkende Stoffe in der Umwelt. Nachr. Chem. Tech. Lab. 46, 63-6.Google Scholar
  23. Howard, P.H. (1989). Handbook of Environmental Fate and Exposure Data for Organic Chemicals. Vol. I: Large Production and Priority Pollutants. Chelsea: Lewis Publ.Google Scholar
  24. Howdeshell, K.L., Hotchkiss, A.K., Thayer, K.A., Vandenbergh, J.H. and vom Saal, F.S. (1999). Exposure to bisphenol A advances puberty. Nature 401, 763-4.Google Scholar
  25. Jobling, S. and Sumpter, J.P. (1993). Detergent components in sewage effluent are weakly oestrogenic to fish: An in vitro study using rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat. Toxicol. 27, 361-72.Google Scholar
  26. Kloas, W., Lutz, I. and Einspanier, R. (1999). Amphibians as a model to study endocrine disruptors: II. Estrogenic activity of environmental chemicals in vitro and in vivo. Sci. Total Environ. 225, 59-68.Google Scholar
  27. Krishnan, A.V., Starhis, P., Permuth, S.F., Tokes, L. and Feldman, D. (1993). Bisphenol A: An estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132, 2279-86.Google Scholar
  28. Laws, S.C., Carey, S.A., Ferrell, J.M., Bodman, G.J. and Cooper, R.L. (2000). Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol. Sci. 54, 154-67.Google Scholar
  29. Lozán, J.L. (1992). Angewandte Statistik für Naturwissenschaftler. Berlin, Hamburg: Parey.Google Scholar
  30. Lutz, I. and Kloas, W. (1999). Amphibians as a model to study endocrine disruptors: I. Environmental pollution and estrogen receptor binding. Sci. Total Environ. 225, 49-57.Google Scholar
  31. Marquardt, H. and Schafer, S.G. (eds). (1994). Lehrbuch der Toxikologie. Mannheim, Leipzig, Wien, Zurich: Bibliographisches Institut Wissenschaftsverlag.Google Scholar
  32. Matthiessen, P. and Gibbs, P.E. (1998). Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ. Toxicol. Chem. 17, 37-43.Google Scholar
  33. Oehlmann, J. (1994). Imposex bei Muriciden (Gastropoda, Prosobranchia), eine okotoxikologische Untersuchung zu TBT-Effekten. Gottingen, Cuvillier.Google Scholar
  34. Oehlmann, J., Stroben, E. and Fioroni, P. (1988). Zur Anatomie und Histologie des Fortpflanzungssystems von Nucella lapillus (L., 1758). Zool. Anz. 221, 101-16.Google Scholar
  35. Oehlmann, J., Stroben, E. and Fioroni, P. (1991). The morphological expression of imposex in Nucella lapillus (LINNAEUS (Gastropoda: Muricidae). J. Moll. Stud. 57, 375-90.Google Scholar
  36. Oehlmann, J., Fioroni, P., Stroben, E. and Markert, B. (1996). Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): Imposex development, sterilization, sex change and population decline. Sci. Total Environ. 188, 205-23.Google Scholar
  37. Rippen, G. (1999). Handbuch Umweltchemikalien. Stoffdaten, Prufverfahren, Vorschriften, 3rd ed., 49th supplement issue. Landsberg, Ecomed.Google Scholar
  38. Schulte-Oehlmann, U., Fioroni, P., Oehlmann, J. and Stroben, E. (1994). The genital system of Marisa cornuarietis (Gastropoda, Ampullariidae)—A morphological and histological analysis. Zool. Beitr. N.F. 36, 59-81.Google Scholar
  39. Schulte-Oehlmann, U., Bettin, C., Fioroni, P., Oehlmann, J. and Stroben, E. (1995). Marisa cornuarietis (Gastropoda, Prosobranchia): a potential TBT bioindicator for freshwater environments. Ecotoxicology 4, 372-84.Google Scholar
  40. Sharpe, R.M., Fisher, J.S., Millar, M.M., Jobling, S. and Sumpter, J.P. (1995). Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ. Health Perspect. 103, 1136-43.Google Scholar
  41. Soto, A.M., Justicia, H., Wray, J.W. and Sonnenschein, C. (1991). p-Nonylphenol, an estrogenic xenobiotic released from ‘modified’ polystyrene. Environ. Health Perspect. 92, 167-73.Google Scholar
  42. Takao, T., Nanamiya, W., Nagano, I., Asaba, K., Kawabata, K. and Hashimoto, K. (1999). Exposure with the environmental estrogen bisphenol A disrupts the male reproductive tract in young mice. Life Sci. 65, 2351-7.Google Scholar
  43. vom Saal, F.S., Cooke, P.S., Buchanan, D.L., Palanza, P., Thayer, K.A., Nagel, S.C., Parmigiani, S. and Welshons, W.V. (1998). A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health 14, 239-60.Google Scholar
  44. Weber, E. (1972). Grundri ß der biologischen Statistik, 7th ed. Stuttgart: Fischer.Google Scholar
  45. White, R., Jobling, S., Hoare, S.A., Sumpter, J.P. and Parker, M.G. (1994). Environmentally persistant alkylphenolic compounds are estrogenic. Endocrinology 135, 175-82.Google Scholar
  46. Yamakoshi, Y., Otani, Y., Fujii, S. and Endo, Y. (2000). Dependence of estrogenic activity on the shape of the 4-alkyl substituent in simple phenols. Biol. Pharm. Bull. 23, 259-61.Google Scholar
  47. Zou, E. and Fingeman, M. (1997). Synthetic estrogenic agents do not interfere with sex differentiation but do inhibit molting of the Cladoceran Daphnia magna. Bull. Environ. Contam. Toxicol. 58, 596-602.Google Scholar
  48. Zou, E. and Fingeman, M. (1999). Effects of estrogenic agents on chitobiase activity in the epidermis and hepatopancreas of the fiddler crab, Uca pugilator. Biol. Ecotoxicol. Environ. Saf. 42, 185-90.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Jörg Oehlmann
    • 1
  • Ulrike Schulte-Oehlmann
    • 2
  • Michaela Tillmann
    • 2
  • Bernd Markert
    • 2
  1. 1.Fachgruppe Human- und ÖkotoxikologieInternationales Hochschulinstitut Zittau, Lehrstuhl UmweltverfahrenstechnikZittauGermany
  2. 2.Fachgruppe Human- und ÖkotoxikologieInternationales Hochschulinstitut Zittau, Lehrstuhl UmweltverfahrenstechnikZittauGermany

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