, Volume 9, Issue 6, pp 399–412 | Cite as

Effects of Endocrine Disruptors on Prosobranch Snails (Mollusca: Gastropoda) in the Laboratory. Part II: Triphenyltin as a Xeno-Androgen

  • Ulrike Schulte-Oehlmann
  • Michaela Tillmann
  • Bernd Markert
  • Jörg Oehlmann
  • Burkard Watermann
  • Sandra Scherf


In laboratory experiments the effects of suspected endocrine disrupting chemicals on freshwater and marine prosobranch species were analysed. In this second of three publications the responses of the freshwater ramshorn snail Marisa cornuarietis and of two marine prosobranchs (the dogwhelk Nucella lapillus and the netted whelk Hinia reticulata) to the xeno-androgenic model compound triphenyltin (TPT) are presented. Marisa and Nucella were exposed via water (nominal concentrations 5–500 ng TPT-Sn/L) and Hinia via sediments (nominal concentrations 50–500 μg TPT-Sn/kg dry wt.) for up to 4 months. Female ramshorn snails but not the two marine species developed imposex in a time and concentration dependent manner (EC10 4 months: 12.3 ng TPT-Sn/L) with a comparable intensity as described for tributyltin. TPT reduced furthermore the fecundity of Marisa at lower concentrations (EC10 4 months: 5.59 ng TPT-Sn/L) with a complete inhibition of spawning at nominal concentrations ≥250 ng TPT-Sn/L (mean measured ±SD: ≥163±97.0 ng TPT-Sn/L). The extension of the pallial sex organs (penis with accessory structures and prostate gland) of male ramshorn snails and dogwhelks were reduced by up to 25% compared to the control but not in netted whelks. Histopathological analyses for M. cornuarietis and H. reticulata provide evidence for a marked impairment of spermatogenesis (both species) and oogenesis (only netted whelks). The test compound induced a highly significant and concentration independent increase in the incidence of hyperplasia on gills, osphradia and other organs in the mantle cavity of N. lapillus indicating a carcinogenic potential of TPT. The results show that prosobranchs are sensitive to endocrine disruption at environmentally relevant concentrations of TPT. Also, M. cornuarietis is a promising candidate for a future organismic invertebrate system to identify endocrine-mimetic test compounds.

endocrine disruptors xeno-androgen triphenyltin imposex snails 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arnold, C.G., Berg, M., Muller, S.R., Dommann, U. and Schwarzenbach, R.P. (1998). Determination of organotin compounds in water, sediments, and sewage sludge using perdeuterated internal standards, accelerated solvent extraction, and large-volume-injection GC/MS. Anal. Chem. 70, 3094-101.Google Scholar
  2. Becker, K., Merlini, L., de Bertrand, N., de Alencastro, L.F. and Tarradellas, J. (1992). Elevated levels of organotins in Lake Geneva: Bivalves as sentinel organism. Bull. Environ. Contam. Toxicol. 48, 37-44.Google Scholar
  3. Becker-van Slooten, K. and Tarradellas, J. (1995). Organotins in Swiss lakes after their ban: Assessment of water, sediment, and Dreissena polymorpha contamination over a four-year period. Arch. Environ. Contam. Toxicol. 29, 384-92.Google Scholar
  4. 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
  5. Bryan, G.W. and Gibbs, P.E. (1991). Impact of low concentrations of tributyltin (TBT) on marine organisms: A review. In M.C. Newman and A.W. McIntosh (eds) Metal Ecotoxicology: Concepts and Applications, pp. 323-61. Ann Arbor, MI: Lewis.Google Scholar
  6. Bryan, G.W., Gibbs, P.E. and 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. J. Mar. Biol. Ass. U.K. 68, 733-44.Google Scholar
  7. Ceulemans, M., Slaets, S. and Adams, F. (1998). Speciation of organotin in environmental sediment samples. Talanta 46, 395-405.Google Scholar
  8. Craig, P.J (ed) (1986). Organometallic compounds in the environment. Principles and reactions. London: Longman.Google Scholar
  9. Crompton, T.R. (1998). Occurrence and analysis of organometallic compounds in the environment. Chichester, New York: John Wiley & Sons.Google Scholar
  10. 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
  11. Federoff, N.E., Young, D., Cowles, J., Spatz, D. and Shamin, M. (1999). TPTH. Environmental Fate and Ecological Risk Assessment. Washington DC: United States Environmental Protection Agency.Google Scholar
  12. Fent, K. (1996). Ecotoxicology of organotin compounds. Crit. Rev. Toxicol. 26, 1-117.Google Scholar
  13. Fent, K. and Hunn, J. (1995). Organotins in freshwater harbors and rivers: Temporal distribution, annual trends and fate. Environ. Toxicol. Chem. 14, 1123-32.Google Scholar
  14. Fent, K. and Meier, W. (1994). Effects of triphenyltin on fish early life stages. Arch. Environ. Contam. Toxicol. 27, 224-31.Google Scholar
  15. Gaines, T.B. and Kimbrough, R.D. (1968). Toxicity of fentin hydroxide to rats. Toxicol. Appl. Pharmacol. 12, 397-403.Google Scholar
  16. Gibbs, P.E., Bebianno, M.J. and Coelho, M.R. (1997). Evidence of the differential sensitivity of neogastropods to tributyltin (TBT) pollution, with notes on a species (Columbella rustica) lacking the imposex response. Environ. Technol. 18, 1219-24.Google Scholar
  17. Gist, G.L. (1998). National Environmental Health Association position on endocrine disrupters—adopted July 2, 1997. J. Environ. Health 60, 21-3.Google Scholar
  18. Horiguchi, T., Shiraishi, H., Shimizu, M., Yamazaki, S. and Morita, M. (1995). Imposex in Japanese gastropods Neogastropoda and Mesogastropoda: Effects of (tributyltin and triphenyltin) from antifouling paints. Mar. Pollut. Bull. 31, 402-5.Google Scholar
  19. Horiguchi, T., Shiraishi, H., Shimizu, M. and Morita, M. (1997a). Imposex in sea snails, caused by organotin tributyltin and triphenyltin pollution in Japan: A survey. Appl. Organomet. Chem. 11, 451-5.Google Scholar
  20. Horiguchi, T., Shiraishi, H., Shimizu, M. and Morita, M. (1997b). Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera. Environ. Pollut. 95, 85-91.Google Scholar
  21. Horiguchi, T., Hyeon-Seo, C., Shiraishi, H., Shibata, Y., Soma, M., Morita, M. and Shimizu, M. (1998). Field studies on imposex and organotin accumulation in the rock shell, Thais clavigera, from the Seto Inland Sea and the Sanriku region, Japan. Sci. Total Environ. 214, 65-70.Google Scholar
  22. Innes, J.R., Ulland, B.M., Valerio, M.G., Petrucelli, L., Fishbein, L., Hart, E.R., Pallotta, A.J., Bates, R.R., Falk, H.L., Gart, J.J., Klein, M., Mitchell, I. and Peters, J. (1969). Bioassay of pesticides and industrial chemicals for tumorigenicity in mice: A preliminary note. J. Natl. Cancer Inst. 42, 1101-14.Google Scholar
  23. Kalbfus, W., Zellner, A., Frey, S. and Knorr, T. (1996). Analytik von Oberflachenwasser, Sediment und Mollusken zur Validierung des biologischen Effektmonitorings. Final report of UBA R&D project 102 40 303/02. Berlin: Federal Environmental Agency.Google Scholar
  24. Kannan, K. and Lee, R.F. (1996). Triphenyltin and its degradation products in foliage and soils from sprayed pecan orchards and in fish from adjacent ponds. Environ. Toxicol. Chem. 15, 1492-9.Google Scholar
  25. Keijzer, T.J.S. and Loch, J.P.G. (1995). Accumulation of HNO3-extractable tin in agricultural and non-agricultural 3 soils by the use of triphenyltin acetate. Water Air Soil Poll. 84, 287-301.Google Scholar
  26. Laughlin, R.B., Johannesen, R.B., French, W., Guard, H. and Brinckman, F.E. (1985). Structure-activity relationships for organotin compounds. Environ. Toxicol. Chem. 4, 343-51.Google Scholar
  27. Lozán, J.L. (1992). Angewandte Statistik für Naturwissenschaftler. Berlin, Hamburg: Parey.Google Scholar
  28. Magee, P.N., Stoner, H.B. and Barnes, J.M. (1957). The experimental production of oedema in the central nervous system of the rat by triethyltin compounds. J. Pathol. Bacterial 73, 107-24.Google Scholar
  29. 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
  30. Nolte, T., Harleman, J.H. and Jahn W. (1995). Histopathology of chemically induced testicular atrophy in rats. Exp. Toxic. Pathol. 47, 267-86.Google Scholar
  31. Oehlmann, J. (2000). Ecotoxicological evaluation of triphenyltin compounds. Report of UBA project 363 01 021. Berlin: Federal Environmental Agency.Google Scholar
  32. 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
  33. Oehlmann, J., Schulte-Oehlmann, U., Tillmann, M. and Markert, B. (2000). Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: Bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 9, 383-97.Google Scholar
  34. Roth, L. (ed) (1988). Wassergefahrdende Stoffe, 7th supplement issue 4/88. Landsberg: Ecomed.Google Scholar
  35. 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
  36. 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
  37. Schulte-Oehlmann, U., Licher, K., Bauer, B. and Oehlmann, J. (1997). Morphologische und histologische Analyse des Geschlechtssystems von Theodoxus fluviatilis (Gastropoda, Neritaceae) unter Berucksichtigung funktionsmorphologischer Aspekte. Zool. Beitr. N.F. 38, 211-31.Google Scholar
  38. Schulte-Oehlmann, U., Tillmann, M., Markert, B. and Oehlmann, J. (2000). Entwicklung eines biologischen Tests mit Marisa cornuarietis (Gastropoda: Prosobranchia) zur Erfassung von Umweltchemikalien mit geschlechtshormonähnlicher Wirkung. Final report of UBA R&D project 216 02 001/04. Berlin: Federal Environmental Agency.Google Scholar
  39. Stroben, E., Oehlmann, J. and Fioroni, P. (1992). The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): A potential biological indicator of tributyltin pollution. Mar. Biol. 113, 625-36.Google Scholar
  40. Sturgeon, R.E. and Siu, K.W.M. (1995). Tin and organotin. In J.W. Kiceniuk and S. Ray (eds) Analysis of contaminants in Edible Aquatic Resources. Series: Food Science and Technology, pp. 225-55, New York: VCH.Google Scholar
  41. US-EPA. (1999). Memorandum TPTH (triphenyltin hydroxide). HED Revised Risk Assessment for the Reregistration Eligibility Decision RED Document, DP barcode D259257. Washington DC: United States Environmental Protection Agency.Google Scholar
  42. Walsh, G.E., McLaughlin, L.L., Lores, E.M., Louie, M.K. and Deans, C.H. (1985). Effects of organotins on growth and survival of two marine diatoms, Skeletonema costatum and Thalassiosira pseudonana. Chemosphere 14, 383-92.Google Scholar
  43. Walsh, G.E., McLaughlin, L.L., Louie, M.K., Deans, C.H. and Lores, E.M. (1986). Inhibition of arm regeneration by Ophioderma brevispina Echinodermata, Ophiuroidea by tributyltin oxide and triphenyltin oxide. Ecotoxicol. Environ. Saf. 12, 95-100.Google Scholar
  44. Weber, E. (1972). Grundri ß der biologischen Statistik, 7th ed. Stuttgart: Fischer.Google Scholar
  45. WHO. (ed) (1980). Tin and organotin compounds: A preliminary review. Environ. Health Criteria 15, 1-109.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Ulrike Schulte-Oehlmann
    • 1
  • Michaela Tillmann
    • 1
  • Bernd Markert
    • 1
  • Jörg Oehlmann
    • 2
  • Burkard Watermann
    • 3
  • Sandra Scherf
    • 3
  1. 1.Fachgruppe Human- und ÖkotoxikologieInternationales Hochschulinstitut Zittau, Lehrstuhl UmweltverfahrenstechnikZittauGermany
  2. 2.Fachgruppe Human- und ÖkotoxikologieInternationales Hochschulinstitut Zittau, Lehrstuhl UmweltverfahrenstechnikZittauGermany
  3. 3.LimnoMarHamburgGermany

Personalised recommendations