Helgoländer Meeresuntersuchungen

, Volume 50, Issue 3, pp 299–317 | Cite as

TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level

  • C. Bettin
  • J. Oehlmann
  • E. Stroben


Tributyltin (TBT) exposure at different concentrations (5, 60, and 100 ng TBT as Sn/l) induces a concentration- and time-dependent imposex (=pseudohermaphroditism) development in femaleNucella lapillus andHinia reticulata. In both species the average imposex stage, termed as vas deferens sequence (VDS) index, and the average female penis length increases with increasing TBT concentration and duration of TBT exposure. Testosterone added at a concentration of 500 ng/l induces a faster and more intensive imposex development compared to that induced by the TBT concentrations used in the present experiments. Radioimmunological determination of endogenous steroid content reveals increasing testosterone titres in female gastropods exposed to TBT which correlate with the TBT concentration used and the duration of the experiment. The most marked and highest increase of the endogenous testosterone level is exhibited by females, of both species exposed to testosterone. Simulataneous exposure to TBT and to the antiandrogen cyproterone acetate which suppresses imposex development completely inN. lapillus and reduces imposex development strongly inH. reticulata proves that the imposex-inducing effects of TBT are mediated by an increasing androgen level and are not caused directly by the organotin compound itself. Further-more, TBT-induced imposex development can be suppressed in both snails by adding estrogens to the aqueous medium. These observations suggest that TBT causes an inhibition of the cytochrome P-450 dependent aromatase system which catalyses the aromatization of androgens to estrogens. The increase of the androgen content or the shift of the androgen-estrogen balance in favour of androgens induces the development of pseudohermaphroditism in marine prosobranchs. Artificial inhibition of the cytochrome P-450 dependent aromatase system using SH 489 (1-methyl-1,4-androstadiene-3,17-dione) as a steroidal aromatase inhibitor and flavone as a nonsteroidal aromatase inhibitor induces imposex development inN. lapillus as well as inH. reticulata.


Testosterone Aromatase Inhibitor Cyproterone Cyproterone Acetate Pseudohermaphroditism 
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.

Literature Cited

  1. Blaber, S. J. M. 1970. The occurrence of a penis-like outgrowth behind the right tentacle in spent females ofNucella lapillus (L.). — Proc. malac. Soc. Lond.39, 231–233.Google Scholar
  2. Bryan, G. W., Gibbs, P. E., Huggett, R. J., Curtis, L. A., Bailey, D. S. & Dauer, D. M., 1989. Effects of tributyltin pullution on the mud snail,Ilyanassa obsoleta, from York Rive and Sarah Creek, Chesapeake Bay. — Mar. Pollut. Bull.20, 458–462.Google Scholar
  3. Cardwell, R. D. & Sheldon, A. W., 1986. A risk assessment concerning the fate and effects of tributyltins on the aquatic environment. In: Oceans ’86 Conference Record. Vol.4; Organotin Symposium, Washington, D.C. IEEE Service Center, Piscataway, N.J., 1117–1129.Google Scholar
  4. Chagot, D., Alzieu, C., Sanjuan, J. & Grizel, H., 1990. Sublethal and histopathological effects of trace levels of tributyltin fluoride on adult oystersCrassostrea gigas. — Aquat. living Resour.3, 121–130.Google Scholar
  5. De Longcamp, D., Lubet, P. & Drosdowsky, M., 1974. The in vitro biosynthesis of steroids by the gonad of the mussel (Mytilus edulis). — Gen. comp. Endocrinol.22, 116–127.PubMedGoogle Scholar
  6. Evans, D. W. & Laughlin, R. B., 1984. Accumulation of bis(tributyltin) oxide by the mud crab,Rhithropanopeus harrasii. — Chemosphere13, 213–219.CrossRefGoogle Scholar
  7. Fent, K., 1991. Bioconcentration and elimination of tributyltin chloride by embryos and larvae of minnowsPhoxinus phoxinus. — Aquat. Toxicol.20, 147–158.Google Scholar
  8. Fent, K. & Meier, W., 1992. Tributyltin-induced, effects on early life stages of minnowsPhoxinus phoxinus. — Archs environ. Contam. Toxicol.22, 428–438.Google Scholar
  9. Féral, C., 1974. Étude comparée des populations d’Ocenebra erinacea (L.) de Granville et d’Arcachon. — Haliotis,4, 123–134.Google Scholar
  10. Féral, C., 1976a. Étude statistique de la présence d’un tractus génital mâle externe chez les femelles d’un Mollusque Gastéropode gonochorique:Ocenebra erinacea (L.). — Cah. Biol. mar.17, 61–76.Google Scholar
  11. Féral, C., 1976b. Analyse expérimental de la morphogenèse et du cycle du pénis chez les femelles d’Ocenebra erinacea espèce gonochorique. — Haliotis,6, 267–271.Google Scholar
  12. Féral, C., 1976c. Répartition géographique des femelles à tractus génital mâle externe chezOcenebra erinacea (L.), espèce gonochorique. — Haliotis7, 29–30.Google Scholar
  13. Féral, C., 1980. Variations dans l’évolution du tractus génital mâle externe des femelles de trois Gastéropodes Prosobranches gonochoriques de stations atlantiques. — Cah. Biol. mar.21, 479–491.Google Scholar
  14. Féral, C. & Le Gall, S., 1983. The influence of a pollutant factor (tributyltin) on the neuroendocrine mechanism responsible for the occurrence of a penis in the females ofOcenebra erinacea. In: Molluscan neuro-endocrinology. Ed. by J. Lever & H. H. Boer. North-Holland Publ. Comp., Amsterdam, 173–175.Google Scholar
  15. Fioroni, P., Oehlmann, J. & Stroben, E., 1991. The pseudohermaphroditism of prosobranchs; morphological aspects. — Zool. Anz.226, 1–26.Google Scholar
  16. Gibbs, P. E. & Bryan, G. W., 1986. Reproductive failure in populations of the dog-whelk,Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. — J. mar. biol. Ass. U.K.66, 767–777.Google Scholar
  17. Gibbs, P. E. & Bryan, G. W., 1987. TBT paints and the demise of the dog-whelk,Nucella lapillus (Gastropoda). In: Oceans ’87 Conference Record. Vol.4: Organotin Symposium, Halifax, Nova Scotia. IEEE Service Center, Piscataway, N.J., 1482–1487.Google Scholar
  18. Gibbs, P. E., Bryan, G. W., Pascoe, P. L. & 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, 507–523.Google Scholar
  19. Gibbs, P. E., Pascoe, P. L. & Burt, G. R., 1988. Sex change in the female dog-whelk,Nucella lapillus induced by tributyltin from antifouling paints. — J. mar. biol. Ass. U.K.68, 715–731.Google Scholar
  20. Hall, L. W. & Pinkney, A. E., 1985. Acute and sublethal effects of organotin compounds in aquatic biota: an interpretative literature evaluation. — CRC crit. Rev. Toxicol.14, 159–209.Google Scholar
  21. Henderson, D. 1987. Aromatase inhibitors: their biochemistry and clinical potential. — J. Steroid Biochem.27, 905–914.CrossRefPubMedGoogle Scholar
  22. Ibrahim, A.-R. & Abul-Hajj, Y. J., 1990. Aromatase inhibition by flavonoids. — J. Steroid Biochem. molec. Biol.,37, 257–260.PubMedGoogle Scholar
  23. Jenner, M. G., 1979. Pseudohermaphroditism: a newly recognized sexual phenomenon inIlyanassa obsolete and other Neogastropoda. — Diss. Abstr. int.40B, 117.Google Scholar
  24. Joosse, J., 1984. Recent progress in endocrinology of molluscs. In: Biosynthesis, metabolism and mode of action in invertebrate hormones. Ed. by J. Hoffmann & M. Porchet. Springer, Berlin, 19–35.Google Scholar
  25. Joosse, J. & Geraerts, W. P. M., 1983. Endocrinology. In: The Mollusca. Ed. by A. S. M. Saleuddin & K. M. Wilbur, Acad. Press, London,4, 317–406.Google Scholar
  26. Kirchin, M. A., Wiseman, A. & Livingstone, D. R., 1988. Studies on the mixed-function oxygenase system of the marine bivalveMytilus edulis. — Mar. environ. Res.24, 117–118.CrossRefGoogle Scholar
  27. Langston, W. J., Burt, G. R. & Mingjiang, Z., 1987. Tin and organotin in water, sediments, and benthic organisms of Poole Harbour. — Mar. Pollut. Bull.18, 634–639.Google Scholar
  28. Laughlin, R. B., French, W. & Guard, H. E., 1986. Accumulation of bis(tributyltin) oxide by the marine musselMytilus edulis. — Environ. Sci. Technol.20, 884–890.Google Scholar
  29. Lee, R. F., 1985. Metabolism of tributyltin oxide by crabs, oysters and fish. — Mar. environ. Res.17, 145–148.CrossRefGoogle Scholar
  30. Lee, R. F., 1986. Metabolism of bis(tributyltin)oxide by estuarine animals. In: Oceans ’86 Conference Record. Vol.4: Organotin Symposium, Washington, D.C. IEEE Service Center, Piscataway, N.J., 1182–1188.Google Scholar
  31. Le Guellec, D., Thiard, M.-C., Remy-Martin, J. P., Deray, A., Gomot, L. & Adessi, G. L., 1987. In vitro metabolism of androstenedione and identification of endogenous steroids inHelix aspersa. —Gen. comp. Endocrinol.66, 425–433.PubMedGoogle Scholar
  32. Livingstone, D. R., Arnold, R., Chipman, K., Kirchin, M. A. & Marsh, J., 1990. The mixed-function oxygenase system in molluscs: metabolism, responses to xenobiotics and toxicity. — Océanis16, 331–347.Google Scholar
  33. Livingstone, D. R., Kirchin, M. A. & Wiseman, A., 1989. Cytochrome P-450 and oxidative metabolism in molluscs. — Xenobiotica19, 1041–1062.PubMedGoogle Scholar
  34. Lupo di Prisco, C. & Dessi’Fulgheri, F., 1975. Alternative pathways of steroid biosynthesis in gonads and hepatopancreas ofAplysia depilans. — Comp. Biochem. Physiol.50B, 191–195.Google Scholar
  35. Martin, R. C., Dixon, D. G., Maguire, R. J., Hodson, P. V. & Tkacz, R. J., 1989. Acute toxicity, uptake depuration and tissue distribution of tri-n-butyltin in rainbow trout,Salmo gairdneri. — Aquat. Toxicol.15, 37–52.CrossRefGoogle Scholar
  36. Oehlmann J., Stroben, E. & Fioroni, P., 1991. The morphological expression of imposex inNucella lapillus (Linnaeus) (Gastropoda: Muricidae). — J. moll. Stud.57, 375–390.Google Scholar
  37. Oehlmann, J., Stroben, E. & Fioroni, P., 1992. The rough tingleOcenebra erinacea (Gastropoda: Muricidae): an exhibitor of imposex in comparison toNucella lapillus. — Helgoländer Meeresunters.46, 311–328.CrossRefGoogle Scholar
  38. Oehlmann, J. Stroben, E. & Fioroni, P., 1996. Tributyltin (TBT) effects onOcinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. — Zool. Anz. (In press).Google Scholar
  39. Payne, E. Smith, J. F., Cope, B. C. & McGowan, L. T., 1991. Studies on the role of liver cytochrome P-450 and oestradiol metabolism in the effects of nutrition and phenobarbital on ovulation rate in the ewe. — Reprod. Fertil. Dev.3, 725–736.CrossRefPubMedGoogle Scholar
  40. Smith, B. S., 1971. Sexuality in the American mud snail,Nassarius obsoletus Say. — Proc. malac. Soc. Lond.39, 377.Google Scholar
  41. Smith, B. S., 1980. The estuarine mud snail,Nassarius obsoletus: abnormalities in the reproductive system. — J. moll. Stud.46, 247–256.Google Scholar
  42. Smith, B. S., 1981a. Male characteristics in the femaleNassarius obsoletus: variations related to locality, season and year. — Veliger23, 212–216.Google Scholar
  43. Smith, B. S., 1981b. Reproductive anomalies in stenoglossan snails related to pollution from marinas. — J. appl. Toxicol.1, 15–21.PubMedGoogle Scholar
  44. Smith, B. S., 1981c. Male characteristics on female mud snails caused by antifouling bottom paints. —J. appl. Toxicol.1, 22–25.PubMedGoogle Scholar
  45. Smith, B. S., 1981d. Tributyltin compounds induce male characteristics on female mud snailsNassarius obsoletus=Ilyanassa obsoleta. — J. appl. Toxicol.1, 141–144.PubMedGoogle Scholar
  46. Spooner, N., Gibbs, P. E., Bryan, G. W. & Goad, L. J., 1991. The effect of tributyltin upon steroid titres in the female dogwhelk,Nucella lapillus, and the development of imposex. — Mar. environ. Res.32, 37–49.CrossRefGoogle Scholar
  47. Stroben, E., Oehlmann, J. & Bettin, C., 1991. TBT-induced imposex and the role of steroids in marine snails. In: Proceedings of the Tenth World Meeting ORganoTin Environmental Programme (ORTEP) Association, Berlin, September 26/27, 1991. Vlissingen, ORTEP Ass., 68–73.Google Scholar
  48. Stroben, E., Oehlmann, J. & Fioroni, P., 1992a. The morphological expression of imposex inHinia reticulata (Gastropoda: Buccinidae): a potential biological indicator of tributyltin pollution. —Mar. Biol.113, 625–636.CrossRefGoogle Scholar
  49. Stroben, E., Oehlmann, J., 1992b.Hinia reticulata andNucella lapillus-comparison of two TBT bioindicators. — Mar. Biol.114, 289–296.CrossRefGoogle Scholar
  50. Thain, J. E., 1986. Toxicity of TBT to bivalves: effects on reproduction, growth and survival. In: Oceans ’86 Conference Record. Vol.4: Organotin Symposium Washington, D. C. IEEE Service Center, Piscataway, N.J., 1306–1313.Google Scholar
  51. Thain, J. E. & Waldock, M. J., 1986. The impact of tributyltin (TBT) antifouling paints on molluscan fisheries. — Wat. Sci. Technol.18, 193–202.Google Scholar

Copyright information

© Biologische Anstalt Helgoland 1996

Authors and Affiliations

  • C. Bettin
    • 1
  • J. Oehlmann
    • 2
  • E. Stroben
    • 1
  1. 1.Institut für Spezielle Zoologie und Vergleichende EmbryologieUniversität MünsterMünsterGermany
  2. 2.Lehrstuhl für UmweltverfahrenstechnikInternationales Hochschulinstitut (IHI) ZittauZittauGermany

Personalised recommendations