Abstract
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.
Similar content being viewed by others
References
Bailey, S. K. & I. M. Davies, 1988. Tributyltin contamination in the Firth of Forth (1975–1987). Sci. Total Envir. 76: 158–192.
Bailey, S. K., 1991. Tributyltin (TBT) contamination of Scottish coastal waters. Unpublished Ph.D. thesis, Napier University, Edinburgh. 379 pp.
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.
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.
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.
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.
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.
Bryan, G. W. & P. E. Gibbs, 1989. Water pollution. In Yearbook of science and technology 1990, McGraw-Hill, New York: 357– 359.
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.
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.
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.
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.
Ellis, D. V. & L. A. Pattisina, 1990. Widespread neogastropod imposex: a biological indicator of global TBT contamination? Mar. Pollut. Bull. 21: 248–253.
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.
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.
Fioroni, P., J. Oehlmann & E. Stroben, 1991. The pseudohermaphroditism of prosobranchs; morphological aspects. Zool. Anz. 226: 1–26.
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.
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.
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.
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.
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.
Kohn, A. J. & K. N. Almasi, 1993. mposex in Australian Conus. J. mar. biol. Ass. U.K. 73: 241–244.
Lozán, J. L., 1992. Angewandte Statistik für Naturwissenschaftler, Parey, Berlin, Hamburg, 237 pp.
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.
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.
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.
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.
Nias, D. J., S. C. McKillup & K. S. Edyvane, 1993. Imposex in Lepsiella vinosa from Southern Australia. Mar. Pollut. Bull. 26: 380–384.
Oehlmann, J., 1994. Imposex bei Muriciden (Gastropoda, Prosobranchia). Eine ökotoxikologische Untersuchung zu TBTEffekten, Cuvillier Verlag, Göttingen, 167 pp.
Oehlmann, J. & C. Bettin, 1996. TBT-induced imposex and the role of steroids in marine snails. Malacol. Rev. Suppl. 6: 157–161.
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.
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.
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.
Oehlmann, J., E. Stroben & P. Fioroni, 1991. The morphological expression of imposex in Nucella lapillus (Linnaeus) Gastropoda: Muricidae). J. moll. Stud. 57: 375–390.
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.
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.
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.
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.
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.
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.
Stroben, E., 1994. Imposex und weitere Effekte von chronischer TBT-Intoxikation bei einigen Mesogastropoden und Bucciniden (Gastropoda, Prosobranchia). Cuvillier Verlag, Göttingen, 193 pp.
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.
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.
Stroben, E., J. Oehlmann & P. Fioroni, 1992c. Hinia reticulate and Nucella lapillus. Comparison of two gastropod tributyltin bioindicators. Mar. Biol. 114: 289–296.
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.
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.
Weber, E., 1972. Grundriß der biologischen Statistik, 7th edition. Fischer, Stuttgart, 422 pp.
Rights and permissions
About this article
Cite this article
Oehlmann, J., Bauer, B., Minchin, D. et al. Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT-induced effects and their geographical uniformity. Hydrobiologia 378, 199–213 (1998). https://doi.org/10.1023/A:1003218411850
Issue Date:
DOI: https://doi.org/10.1023/A:1003218411850