, Volume 378, Issue 1–3, pp 199–213 | Cite as

Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT-induced effects and their geographical uniformity

  • J. Oehlmann
  • B. Bauer
  • D. Minchin
  • U. Schulte-Oehlmann
  • P. Fioroni
  • B. Markert


Two different tributyltin (TBT)-induced virilisation phenomena in prosobranch snails – intersex in Littorina littorea and imposex in Nucella lapillus – are compared in order to facilitate their simultaneous use in geographical large scale effect monitoring surveys. Imposex in dogwhelks is a more sensitive biomarker and should be used in areas that are only slightly or moderately contaminated with TBT (ambient TBT concentrations < 2.0 ng as Sn l-1). The assessment of intersex intensities in periwinkle populations has considerable advantages in areas with higher TBT concentrations and should be used also wherever dogwhelks are absent irrespective of the TBT exposure level. The intersex index (ISI) and vas deferens sequence (VDS) index are proposed as the most suited parameters for effect monitoring purposes. The geographical uniformity of intersex and imposex is analysed and proven for the coasts of Ireland, France, and Germany. A relative loss of TBT sensitivity in females can be found, but to a varying extent in both species. The implications of this result for biological TBT effect monitoring programmes are discussed in light of the fact that intersex and imposex have both been found to be irreversible. Because it is the objective of these programmes to assess current TBT contaminations and resulting biological effects, only relatively young specimens should be considered in the sampling strategy.

Nucella lapillus Littorina littorea imposex intersex TBT effect monitoring geographical differences 


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  1. Bailey, S. K. & I. M. Davies, 1988. Tributyltin contamination in the Firth of Forth (1975–1987). Sci. Total Envir. 76: 158–192.Google Scholar
  2. Bailey, S. K., 1991. Tributyltin (TBT) contamination of Scottish coastal waters. Unpublished Ph.D. thesis, Napier University, Edinburgh. 379 pp.Google Scholar
  3. Bailey, S. K., I. M. Davies, M. J. C. Harding & A. M. Shanks, 1991. Effects of tributyltin oxide on the dogwhelk Nucella lapillus (L.). Proc. of the Tenth World Meeting of the Organotin Environmental Programme (ORTEP): 7–66.Google Scholar
  4. Bauer, B., M. Brumm-Scholz, U. Deutsch, P. Fioroni, I. Ide, S. Liebe, J. Oehlmann, E. Stroben & B. Watermann, 1993. Basisstudie zur Erfassung pathologischer Effekte von Unterwasseranstrichen bei Schnecken der niedersächsischen Nordseeküste. Final report for ‘Aktion Seeklar’ e.V. (Hamburg) and ‘WWFGermany’ (Frankfurt/M.), Ahrensburg and Münster, 105 pp.Google Scholar
  5. Bauer, B., P. Fioroni, I. Ide, S. Liebe, J. Oehlmann, E. Stroben & B. Watermann, 1995. TBT effects on the female genital system of Littorina littorea: a possible indicator of tributyltin pollution. Hydrobiologia 309: 15–27.Google Scholar
  6. Bauer, B., P. Fioroni, U. Schulte-Oehlmann, J. Oehlmann & W. Kalbfus, (1997). The use of Littorina littorea for tributyltin (TBT) effect monitoring – results from the German TBT survey 1994/95 and laboratory experiments. Envir. Pollut. 96: 299–309.Google Scholar
  7. Bright, D. A. & D. V. Ellis, 1990. A comparative survey of imposex in northeast Pacific neogastropods (Prosobranchia) related to tributyltin contamination, and a choice of a suitable bioindicator. Can. J. Zool. 68: 1915–1924.Google Scholar
  8. Bryan, G. W. & P. E. Gibbs, 1989. Water pollution. In Yearbook of science and technology 1990, McGraw-Hill, New York: 357– 359.Google Scholar
  9. Bryan, G. W. & P. E. Gibbs, 1991. Impact of low concentrations of tributyltin (TBT) on marine organisms: a review. In M. C. Newman & A. W. McIntosh (eds), Metal Ecotoxicology: Concepts and Application. Lewis Publisher, Ann Arbor, 361 pp.Google Scholar
  10. Bryan, G. W., P. E. Gibbs & G. R. Burt, 1988. A comparison of the effectiveness of tri-n-butyltin chloride and five other organotin compounds in promoting the development of imposex in the dogwhelk, Nucella lapillus. J. mar. biol. Ass. U.K. 68: 733–744.Google Scholar
  11. Bryan, G. W., P. E. Gibbs, G. R. Burt & L. G. Hummerstone, 1987. The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J. mar. biol. Ass. U.K. 67: 525–544.Google Scholar
  12. Bryan, G. W., P. E. Gibbs, L. G. Hummerstone & G. R. Burt, 1989. Uptake and transformation of 14C-labelled tributyltin chloride by the dog-whelk, Nucella lapillus: importance of absorption from the diet. Mar. Envir. Res. 28: 247–251.Google Scholar
  13. Ellis, D. V. & L. A. Pattisina, 1990. Widespread neogastropod imposex: a biological indicator of global TBT contamination? Mar. Pollut. Bull. 21: 248–253.Google Scholar
  14. Evans, S. M., A. Hutton, M. A. Kendall & A. M. Samosir, 1991. Recovery in populations of dogwhelks Nucella lapillus (L.) suffering from imposex. Mar. Pollut. Bull. 22: 331–333.Google Scholar
  15. Evans, S. M., T. Leksono & P. D. McKinnell, 1995. Tributyltin pollution – a diminishing problem following legislation limiting the use of TBT-based anti-fouling paints. Mar. Pollut. Bull. 30: 14–21.Google Scholar
  16. Fioroni, P., J. Oehlmann & E. Stroben, 1991. The pseudohermaphroditism of prosobranchs; morphological aspects. Zool. Anz. 226: 1–26.Google Scholar
  17. Gibbs, P. E., G.W. Bryan & P. L. Pascoe, 1991. TBT-induced imposex in the dogwhelk, Nucella lapillus: geographical uniformity of the response and effects. Mar. Envir. Res. 32: 79–87.Google Scholar
  18. Gibbs, P. E., G. W. Bryan, P. L. Pascoe & G. R. Burt, 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. Harding, M. J. C., S. K. Bailey & I. M. Davies, 1992. TBT imposex survey of the North Sea. UK Department of the Environment, Contract PECD 7/8/214, Annex 4: Germany (= Scottish Fisheries Working Paper No. 13/92), 7 pp.Google Scholar
  20. Horiguchi, T., H. Shiraishi, M. Shimizu, S. Yamazaki & M. Morita, 1985. Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): Effects of tributyltin and triphenyltin from antifouling paints. Mar. Pollut. Bull. 31: 402–405.Google Scholar
  21. Kalbfus, W., A. Zellner, S. Frey & T. Knorr, 1996. Analytik von berflächenwasser, Sediment und Mollusken zur Validierung des biologischen Effektmonitorings. Final report of R. & D. project 102 40 303/02, Umweltbundesamt, Berlin, 108 pp.Google Scholar
  22. Kohn, A. J. & K. N. Almasi, 1993. mposex in Australian Conus. J. mar. biol. Ass. U.K. 73: 241–244.Google Scholar
  23. Lozán, J. L., 1992. Angewandte Statistik für Naturwissenschaftler, Parey, Berlin, Hamburg, 237 pp.Google Scholar
  24. Minchin, D., J. Oehlmann, C. B. Duggan, E. Stroben & M. Keatinge, 1995. Marine TBT antifouling contamination in Ireland, following legislation in 1987. Mar. Pollut. Bull. 30: 633–639.Google Scholar
  25. Minchin, D., E. Stroben, J. Oehlmann, B. Bauer, C. B. Duggan & M. Keatinge, 1996. Biological indicators used to map organotin contamination in Cork Harbour, Ireland, Mar. Pollut. Bull. 32: 188–195.Google Scholar
  26. Minchin, D., J. Oehlmann, U. Schulte-Oehlmann, B. Bauer & C. B. Duggan, 1997. Biological indicators used to map organotin contamination from a fishing port, Killybegs, Ireland. Mar. Pollut. Bull. 34: 235–243.Google Scholar
  27. Müller, M. D., L. Renberg & G. Rippen, 1989. Tributyltin in the environment-sources, fate and determination: an assessment of present status and research needs, Chemosphere 18: 2015–2042.Google Scholar
  28. Nias, D. J., S. C. McKillup & K. S. Edyvane, 1993. Imposex in Lepsiella vinosa from Southern Australia. Mar. Pollut. Bull. 26: 380–384.Google Scholar
  29. Oehlmann, J., 1994. Imposex bei Muriciden (Gastropoda, Prosobranchia). Eine ökotoxikologische Untersuchung zu TBTEffekten, Cuvillier Verlag, Göttingen, 167 pp.Google Scholar
  30. Oehlmann, J. & C. Bettin, 1996. TBT-induced imposex and the role of steroids in marine snails. Malacol. Rev. Suppl. 6: 157–161.Google Scholar
  31. Oehlmann, J., P. Fioroni, E. Stroben & B. Markert, 1996a. Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci. Total Envir. 188: 205–223.Google Scholar
  32. Oehlmann, J., I. Ide, B. Bauer, B. Watermann, U. Schulte-Oehlmann, S. Liebe & P. Fioroni, 1996b. Erfassung morphound histopathologischer Effekte von Organozinnverbindungen auf marine Mollusken und Prüfung ihrer Verwendbarkeit für ein zukünftiges biologisches Effektmonitoring. Final report of R. & D. project 102 40 303/01, Umweltbundesamt, Berlin, 194 pp.Google Scholar
  33. Oehlmann, J., S. Liebe, B. Watermann, E. Stroben, P. Fioroni & U. Deutsch, 1994. New perspectives of sensitivity of littorinids to TBT pollution. Cah. Biol. mar. 35: 254–255.Google Scholar
  34. Oehlmann, J., E. Stroben & P. Fioroni, 1991. The morphological expression of imposex in Nucella lapillus (Linnaeus) Gastropoda: Muricidae). J. moll. Stud. 57: 375–390.Google Scholar
  35. Oehlmann, J., E. Stroben & P. Fioroni, 1993. Fréquence et degré d'expression du pseudohermaphrodisme chez quelques Prosobranches Sténoglosses des côtes françaises (surtout de la Baie de Morlaix et de la Manche). 2. Situation jusqu'au printemps de 1992. Cah. Biol. mar. 34: 343–362.Google Scholar
  36. Oslo & Paris Commissions (ed.), 1996. Agenda Item 9 of the Environmental Assessment and Monitoring Committee (ASMO). OSPARCOM, Vila Franca do Campo (=ASMO96/9/8-E), 23 pp.Google Scholar
  37. Saavedra Alvarez, M. M. & D. V. Ellis, 1990. Widespread neogastropod imposex in the northeast Pacific: implications for TBT contamination surveys. Mar. Pollut. Bull. 21: 244–247.Google Scholar
  38. Schulte-Oehlmann, U., J. Oehlmann & E. Stroben, 1993. TBT-induced imposex of Nucella lapillus on Irish coasts in 1990. In J. C. Aldrich (ed.), Quantified Phenotypic Responses in Morphology and Physiology, Proc. 27th European Marine Biology Symposium, Dublin, Ireland, 7–11th September, 1992. JAPAGA, Ashford: 307–311.Google Scholar
  39. Short, J. W., S. D. Rice, C. C. Brodersen & W. B. Stickle, 1989. Occurrence of tri-n-butyltin-caused imposex in the North Pacific marine snail Nucella lima in Auke Bay, Alaska. Mar. Biol. 102: 291–297.Google Scholar
  40. Stewart, C., S. J. de Mora, M. R. L. Jones & M. C. Miller, 1992. Imposex in New Zealand neogastropods. Mar. Pollut. Bull. 24: 204–209.Google Scholar
  41. Stroben, E., 1994. Imposex und weitere Effekte von chronischer TBT-Intoxikation bei einigen Mesogastropoden und Bucciniden (Gastropoda, Prosobranchia). Cuvillier Verlag, Göttingen, 193 pp.Google Scholar
  42. Stroben, E., C. Brömmel, J. Oehlmann & P. Fioroni, 1992a. The genital systems of Trivia arctica and T. monacha (Prosobranchia, Mesogastropoda) and tributyltin induced imposex. Zool. Beitr. 34: 349–374.Google Scholar
  43. Stroben, E., J. Oehlmann & P. Fioroni, 1992b. The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Mar. Biol. 113: 625–636.Google Scholar
  44. Stroben, E., J. Oehlmann & P. Fioroni, 1992c. Hinia reticulate and Nucella lapillus. Comparison of two gastropod tributyltin bioindicators. Mar. Biol. 114: 289–296.Google Scholar
  45. Stroben, E., J. Oehlmann, U. Schulte-Oehlmann & P. Fioroni, 1996. Seasonal variations in the genital ducts of normal and imposexaffected prosobranchs and its influence on biomonitoring indices. Malacol. Rev. Suppl. 6: 173–184.Google Scholar
  46. Ten Hallers-Tjabbes, C. C., J. F. Kemp & J. P. Boon, 1994. Imposex in whelks (Buccinum undatum) from the open North Sea: relation to shipping traffic intensities. Mar. Pollut. Bull. 28: 311–313.Google Scholar
  47. Weber, E., 1972. Grundriß der biologischen Statistik, 7th edition. Fischer, Stuttgart, 422 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • J. Oehlmann
  • B. Bauer
  • D. Minchin
  • U. Schulte-Oehlmann
  • P. Fioroni
  • B. Markert

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