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Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributyltin-induced imposex

Published online by Cambridge University Press:  11 May 2009

P.E. Gibbs
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB
G.W. Bryan
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB
P.L. Pascoe
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB
G.R. Burt
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB

Abstract

Imposex (the development of male sex organs on the female) has been studied in the European sting winkle, Ocenebra erinacea. In common with studies of other gonochoristic stenoglossan gastropods, the evidence gained from surveys of the south-west regions of England and Brittany (France) indicates that the phenomenon is a response to tributyltin (TBT) pollution. Close to sources of TBT, O. erinacea females exhibit structural abnormalities of the oviduct as a result of advanced imposex, including absence of a genital papilla and a normal vulva, a deformed bursa copulatrix and the presence of a longitudinal split. Copulation and capsule formation would appear to be inhibited in the worst-affected females. Such curtailment of breeding activity would result in population decline: direct evidence of the extinction of O. erinacea close to harbours, as is known for N. lapillus, is generally wanting for British shores, but the decline of the species in the Bay of Arcachon in France is attributable to TBT pollution.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1990

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References

Abel, R., Hathaway, R.A., King, N.J., Vosser, J.L. & Wilkinson, T.G., 1987. Assessment and regulatory actions for TBT in the U.K. In Oceans ‘87. Conference Record, vol. 4. International Organotin Symposium, pp. 13141319. New York: Institute of Electrical and Electronics Engineers.Google Scholar
Alzieu, C., 1986. TBT detrimental effects on oyster culture in France - evolution since antifouling paint regulation. In Oceans ‘86. Conference Record, vol. 4. Organotin Symposium, pp. 11301134. New York: Institute of Electrical and Electronics Engineers.Google Scholar
Blaber, S.J.M., 1970. The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.). Proceedings of the Malacological Society of London, 39, 231233.Google Scholar
Bright, D.A. & Ellis, D.V., 1990. A comparative survey of imposex in NE Pacific neogastropods (Prosobranchia) related to tributyltin contamination, and a choice of suitable bioindicator. Canadian Journal of Zoology, 241245.Google Scholar
Bryan, G.W., Gibbs, P.E. & Burt, G.R., 1988. A comparison of the effectiveness of tri-n-butyltin chloride and five other organotin compounds in promoting the development of imposex in the dog-whelk, Nucella lapillus. journal of the Marine Biological Association of the United Kingdom, 68, 733744.CrossRefGoogle Scholar
Bryan, G.W., Gibbs, P.E., Burt, G.R. & Hummerstone, L.G., 1987. The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. Journal of the Marine Biological Association of the United Kingdom, 67, 525544.Google Scholar
Bryan, G.W., Gibbs, P.E., Huggett, R.J., Curtis, L.A., Bailey, D.S. & Dauer, D.M., 1989. Effects of tributyltin pollution on the mud snail, Ilyanassa obsoleta, from the York River and Sarah Creek, Chesapeake Bay. Marine Pollution Bulletin, 20, 458462.CrossRefGoogle Scholar
Bryan, G.W., Gibbs, P.E., Hummerstone, L.G. & Burt, G.R., 1986. The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom, 66, 611640.Google Scholar
Bryan, G.W., Gibbs, P.E., Hummerstone, L.G. & Burt, G.R., 1989. Uptake and transformation of 14C-labelled tributyltin chloride by the dog-whelk, Nucella lapillus: importance of absorption from the diet. Marine Environmental Research, 28, 241245.CrossRefGoogle Scholar
Cleary, J.J. & Stebbing, A.R.D., 1987. Organotins in the water column - enhancement in the surface microlayer. In Oceans ‘87. Conference Record, vol. 4. International Organotin Symposium, pp. 14051410. New York: Institute of Electrical and Electronics Engineers.Google Scholar
Féral, C., 1976 a. Analyse expérimentale de la morphogénèse et du cycle du pénis chez les femelles d'Ocenebra erinacea, espèce gonochorique. Haliotis, 6, 267271.Google Scholar
Féral, C., 1976b. Etude statistique de la présence d'un tractus génital mâle externe chez les femelles d'un Mollusque Gasteropode gonochorique: Ocenebra erinacea (L.). Cahiers de Biologie Marine, 17, 6176.Google Scholar
Féral, C., 1976c. Répartition géographique des femelles a tractus génital mâle externe chez Ocenebra erinacea (L.), espèce gonochorique. Haliotis, 7, 2930.Google Scholar
Féral, C., 1980a. Variations dans l'évolution du tractus génital mâle externe des femelles de trois Gastéropodes Prosobranches gonochoriques de stations Atlantiques. Cahiers de Biologie Marine, 21, 479491.Google Scholar
Féral, C., 1980b. Influence de la qualité de l'eau de mer sur la différentiation d'un tractus génital mâle externe chez les femelle d'un Mollusque Gastéropode gonochorique: Ocenebra erinacea L. Compte Rendu Hebdomadaire des Séances de l'Académie des Sciences, 291, 775778.Google Scholar
Féral, C. & Le Gall, S., 1982. Induction experimentale par un polluant marin (le tributylétain), de l'activité neuroendocrine contrôlant la morphogénèse du pénis chez les femelles d'Ocenebra erinacea (Mollusque, Prosobranche gonochorique). Compte Rendu Hebdomadaire des Séances de l'Académie des Sciences, 295, 627630.Google Scholar
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 of Ocenebra erinacea. In Molluscan Neuro-endocrinology. Proceedings of the International Minisymposium on Molluscan Endocrinology, 1982 (ed. I., Lever and H.H., Boer), pp. 173175. Amsterdam: North Holland Publishing Company.Google Scholar
Fretter, V., 1941. The genital ducts of some British stenoglossan prosobranchs. Journal of the Marine Biological Association of the United Kingdom, 25, 173211.CrossRefGoogle Scholar
Fretter, V., 1946. The genital ducts of Theodoxus, Lamellaria and Trivia, and a discussion on their evolution in the prosobranchs. journal of the Marine Biological Association of the United Kingdom, 26, 312351.Google Scholar
Fretter, V. & Graham, A., 1984. The prosobranch molluscs of Britain and Denmark. Part 8 Neogastropoda. journal of Molluscan Studies, supplement 15, 435556.Google Scholar
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. Journal of the Marine Biological Association of the United Kingdom, 66, 767777.Google Scholar
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. International Organotin Symposium, pp. 14821487. New York: Institute of Electrical and Electronics Engineers.Google Scholar
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. Journal of the Marine Biological Association of the United Kingdom, 67, 507523.CrossRefGoogle Scholar
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. Journal of the Marine Biological Association of the United Kingdom, 68, 715731.CrossRefGoogle Scholar
Hancock, D.A., 1960. The ecology of the molluscan enemies of the edible mollusc. Proceedings of the Malacological Society of London, 34, 123143.Google Scholar
Houston, R.S., 1971. Reproductive biology of Thais emarginata (Deshayes, 1839) and Thais canaliculata (Duclos, 1832). Veliger, 13, 348357.Google Scholar
Johansson, J., 1953. On the genital organs of some mesogastropods: Cerithium vulgatum Brug., Triphora perversa (L.) and Melanella (Eulima) intermedia (Cantr.). Contributions to the phylogeny of the pallial gonoducts of the Prosobranchia. Zoologiska Bidrag från Uppsala, 30, 123.Google Scholar
Key, D. & Davidson, P.E., 1981. A review of the development of the Solent oyster fishery, 1972–80. Laboratory Leaflets. Fisheries Laboratory, Lowestoft, no. 52, 37 pp.Google Scholar
Lee, R.F., 1986. Metabolism of bis (tributyltin) oxide by estuarine animals. In Oceans ‘86. Conference Record, vol. 4. Organotin Symposium, pp. 11821188. New York: Institute of Electrical and Electronics Engineers.Google Scholar
Poli, G., Salvat, B. & Strieff, W., 1971. Aspect particulier de la sexualité chez Ocenebra erinacea. Haliotis, 1, 2930.Google Scholar
Smith, B.S., 1971. Sexuality in the American mud-snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London, 39, 377378.Google Scholar
Smith, B.S., 1980. The estuarine mud snail, Nassarius obsoletus: abnormalities in the reproductive system. Journal of Molluscan Studies, 46, 247256.Google Scholar
Smith, B.S., 1981a. Reproductive anomalies in stenoglossan snails related to pollution from marinas. Journal of Applied Toxicology, 1, 1521.CrossRefGoogle ScholarPubMed
Smith, B.S., 1981b. Male characteristics on female mud snails caused by antifouling bottom paints. Journal of Applied Toxicology, 1, 2225.CrossRefGoogle ScholarPubMed
Smith, B.S., 1981c. Tributyltin compounds induce male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsoleta. Journal of Applied Toxicology, 1, 141144.CrossRefGoogle ScholarPubMed
Smith, B.S., 1981d. Male characteristics in female Nassarius obsoletus: variations related to locality, season and year. Veliger, 23, 212216.Google Scholar
Spence, S.K., Hawkins, S.J. & Santos, R.S., The mollusc Thais haemastoma - an exhibitor of ‘imposex’ and potential indicator of tributyltin pollution. Marine Ecology, Naples, in press.Google Scholar