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Endocrine disruption in prosobranch molluscs: evidence and ecological relevance

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Abstract

Prosobranch snails represent almost 50% of all recent molluscs, are ubiquitously distributed, play important roles in various ecosystems and exhibit a variety of reproductive modes and life-cycle-strategies. Many of them attain life spans of several years, which in combination with their limited ability to metabolize organic chemicals, may contribute to the fact that prosobranchs constitute one of the most endangered taxonomic groups in aquatic ecosystems. Although it is not yet known to what extent endocrine disrupting chemicals (EDCs) contribute to this situation, the case of tributyltin (TBT) and its population-level impact on prosobranchs demonstrates the general susceptibility of these invertebrates. The existing evidence for comparable population-level effects in prosobranch snails by other androgens, antiandrogens, and estrogens is critically reviewed. The example of TBT demonstrates the difficulty to prove an endocrine mode of action for a given chemical. Although it is generally accepted that TBT causes imposex and intersex in prosobranch snails as a result of endocrine disruption, the detailed biochemical mechanism is still a matter of debate. The strengths and weaknesses of the five competing hypotheses are discussed, together with previously unpublished data. Finally, the ecological relevance of EDC effects on the population and community level and the application of prosobranchs for the assessment of EDCs are addressed.

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References

  • Albanis T, Allera A, Bachmann J, Barbaglio A, Berntsson P, Dittmann N, Carnevali DC, Ciceri F, Dagnac T, Duft M, Falandysz J, Galassi S, Hala D, Janer G, Jeannot R, Jobling S, King I, Klingmüller D, Kloas W, Kusk KO, Lavado R, Lo S, Lutz I, Oehlmann J, Oredsson S, Porte C, Rand-Weaver M, Sakkas V, Schmitt C, Schulte-Oehlmann U, Sugni M, Tyler X, van Aerle R, van Ballegoy C, Wollenberger (2006) Executive summary on the project results of COMPRENDO—Comparative Research on Endocrine Disrupters (EU project no. EVK1-CT-2002-00129). Available online under http://www.comprendo-project.org

  • Andersen HR, Bonefeld-Jørgensen EC, Nielsen F, Jarfeldt K, Jayatissa MN, Vinggaard AM (2006) Estrogenic effects in vitro and in vivo of the fungicide fenarimol. Toxicol Lett 163:142–152

    Article  CAS  Google Scholar 

  • Bauer B, Fioroni P, Ide I, Liebe S, Oehlmann J, Stroben E, Watermann B (1995) TBT effects on the female genital system of Littorina littorea: a possible indicator of tributyltin pollution. Hydrobiologia 309:15–27

    Article  CAS  Google Scholar 

  • Barata C, Porte C, Baird DJ (2004) Experimental designs to assess endocrine disrupting effects in invertebrates—a review. Ecotoxicology 13:511–517

    Article  CAS  Google Scholar 

  • Barroso CM, Moreira MH, Bebianno MJ (2002a) Imposex, female sterility and organotin contamination of the prosobranch Nassarius reticulatus from the Portuguese coast. Mar Ecol Prog Ser 230:127–135

    Google Scholar 

  • Barroso CM, Reis-Henriques MA, Ferreira MS, Moreira MH (2002b) The effectiveness of some compounds derived from antifouling paints in promoting imposex in Nassarius reticulatus. J Mar Biol Assoc UK 82:249–255

    Article  CAS  Google Scholar 

  • Barroso CM, Reis-Henriques MA, Ferreira M, Gibbs PE, Moreira MH (2005) Organotin contamination, imposex and androgen/oestrogen ratios in natural populations of Nassarius reticulatus along a ship density gradient. Appl Organometallic Chem 19:1141–1148

    Article  CAS  Google Scholar 

  • Bettin C, Oehlmann J, Stroben E (1996) TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgoländer Meeresuntersuchungen 50:299–317

    Article  Google Scholar 

  • Birchenough AC, Evans SM, Moss C, Welch R (2002) Re-colonisation and recovery of populations of dogwhelks Nucella lapillus (L.) on shores formerly subject to severe TBT contamination. Mar Pollut Bull 44:652–659

    Article  CAS  Google Scholar 

  • Chuang KH, Lee YF, Lin WJ, Chu CY, Altuwaijri S, Wan YJY, Chang C (2005) 9-cis-retinoic acid inhibits androgen receptor activity through activation of retinoid X receptor. Mol Endocrinol 19:1200–1212

    Article  CAS  Google Scholar 

  • Crothers JH (1985) Dog-whelks: an introduction to the biology of Nucella lapillus (L.). Field Stud 6:291–360

    Google Scholar 

  • Davies IM, Minchin A (2002) Quality assurance of imposex and intersex measurements in marine snails. J Environ Monit 4:788–790

    Article  CAS  Google Scholar 

  • DeFur PL, Crane M, Ingersoll C, Tattersfield L (eds) (1999) Endocrine disruption in invertebrates: endocrinology, testing, and assessment. In: Proceedings of the workshops on endocrine disruption in invertebrates, 12–15 December 1998, Noordwijkerhout, SETAC Press, Pensacola, The Netherlands

  • Di Benedetto P (2005) Investigations in imposex development in marine prosobranchs. Diploma thesis. Johann Wolfgang Goethe University, Faculty Biological Sciences. Frankfurt, Germany [in German]

  • Dorn A (ed) (2000) Reproductive biology of invertebrates, vol 10, Part A and B. Wiley, New York

    Google Scholar 

  • Duft M, Schulte-Oehlmann U, Weltje L, Tillmann M, Oehlmann J (2003b) Stimulated embryo production as a parameter of estrogenic exposure via sediments in the freshwater mudsnail Potamopyrgus antipodarum. Aquat Toxicol 64:437–449

    Article  CAS  Google Scholar 

  • Duft M, Schmitt C, Bachmann J, Brandelik C, Schulte-Oehlmann U, Oehlmann J (2006) Prosobranch snails as test organisms for the assessment of endocrine active chemicals—an overview and a guideline proposal for a reproduction test with the freshwater mudsnail Potamopyrgus antipodarum. Ecotoxicology, DOI: 10.1007/s10646-006-0106-0

  • Durica DS, Wu X, Anilkumar G, Hopkins PM, Chung ACK (2002) Characterisation of crab EcR and RXR homologs and expression during limb regeneration and oocyte maturation. Mol Cell Endocrinol 189:59–76

    Article  CAS  Google Scholar 

  • Féral C, Le Gall S (1982) Induction expérimentale par un polluant marin (le tributylétain), de l’activité neuroendocrine contrôlant la morphogenèse du pénis chez les femelles d’Ocenebra erinacea (Mollusque Prosobranche gonochorique). Comptes Rendus de l’Académie des Sciences Paris, Série III 295:627–630

    Google Scholar 

  • Fioroni P, Oehlmann J, Stroben E (1991) The pseudohermaphroditism of prosobranchs; morphological aspects. Zool Anz 226:1–26

    Google Scholar 

  • Følsvik N, Berge JA, Brevik EM, Walday M (1999) Quantification of organotin compounds and determination of imposex in populations of dogwhelks (Nucella lapillus) from Norway. Chemosphere 38:681–691

    Article  Google Scholar 

  • Gibbs PE, Bebianno MJ, Coelho MR (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 18:1219–1224

    CAS  Google Scholar 

  • Gooding MP, LeBlanc GA (2001) Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta. Gen Comp Endocrinol 122:172–180

    Article  CAS  Google Scholar 

  • Gooding MP, LeBlanc GA (2004) Seasonal variation in the regulation of testosterone levels in the eastern mud snail (Ilyanassa obsoleta). Invertebr Biol 123:237–243

    Article  Google Scholar 

  • Gooding MP, Wilson VS, Folmar LC, Marcovich DT, LeBlanc GA (2003) The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta). Environ Health Perspect 111:426–430

    Article  CAS  Google Scholar 

  • Gruner HE (ed) (1993) Textbook special zoology, vol 1: invertebrates. Part 3: Mollusca, Sipunculida, Echgiurida, Annelida, Onychophora, Tardigrada, Pentastomida, 5th edn. Gustav Fischer, Jena, Stuttgart, New York [in German]

    Google Scholar 

  • Gruner HE, Hannemann HJ, Hartwich G, Kilias R (1993) Urania’s animal kingdom, vol 1: Invertebrates 1 (Protozoa to Echiurida). Urania, Leipzig, Jena, Berlin [in German]

  • Hagger JA, Depledge MH, Oehlmann J, Jobling S, Galloway TS (2006) Is there a causal association between genotoxicity and the imposex effect? Environ Health Perspect 114 (Suppl 1):20–26

    Google Scholar 

  • Heidrich DD, Stockelbroeck S, Klingmüller D (2001) Inhibition of human cytochrome P450 aromatase activity by butyltins. Steroids 66:763–769

    Article  CAS  Google Scholar 

  • Heller J (1990) Longevity in mollusks. Malacologia 31:259–295

    Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M, Morita M (1997) 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

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Takiguchi N, Kaya M, Shiraishi H, Morita M (2005) Continuing observation of disturbed reproductive cycle and ovarian spermatogenesis in the giant abalone, Haliotis madaka from an organotin-contaminated site of Japan. Mar Pollut Bull 51:817–822

    Article  CAS  Google Scholar 

  • Huet M, Paulet YM, Clavier J (2004) Imposex in Nucella lapillus: a ten year survey in NW Brittany. Mar Ecol Prog Ser 270:153–161

    Google Scholar 

  • Janer G, Lyssimachou A, Bachmann J, Oehlmann J, Schulte-Oehlmann U, Porte C (2006) Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: the effect of xenoandrogenic compounds. Steroids 71:435–444

    Article  CAS  Google Scholar 

  • Jha AN, Hagger JA, Hill SJ (2000) Tributyltin induces cytogenetic damage in the early life stages of the marine mussel, Mytilus edulis. Environ Mol Mutagen 35:343–350

    Article  CAS  Google Scholar 

  • Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Schulte-Oehlmann U, Pawlowski S, Braunbeck T, Turner AP, Tyler CR (2004) Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquat Toxicol 66:207–222

    Article  CAS  Google Scholar 

  • Jorundsdottir K, Svavarsson K, Leung KMY (2005) Imposex levels in the dogwhelk Nucella lapillus (L.)—continuing improvement at high latitudes. Mar Pollut Bull 51:744–749

    Article  CAS  Google Scholar 

  • Jungbluth JH, von Knorre D (1995) Red list of inland molluscs [Snails (Gastropoda) and mussels (Bivalvia)] in Germany. Mitteilungen der Deutschen Malakologischen Gesellschaft 56/57:1–17 [in German]

    Google Scholar 

  • Kluytmans JH, Brands F, Zandee D (1988) Interactions of cadmium with the reproductive cycle of Mytilus edulis. Mar Environ Res 24:189–192

    Article  CAS  Google Scholar 

  • Lafont R, Mathieu M (2006) Steroids in aquatic invertebrates. Ecotoxicology, DOI: 10.1007/s10646-006-0113-1

  • Lagadic L, Coutellec MA, Caquet T (2006) Endocrine disruption in pulmonate molluscs: few evidences, many challenges. Ecotoxicology, DOI: 10.1007/s10646-006-0114-0

  • Lee RF (1985) Metabolism of tributyltin oxide by crabs, oysters and fish. Mar Environ Res 17:145–148

    Article  CAS  Google Scholar 

  • Legierse KCHM, Sijm DTHM, van Leeuwen CJ, Seinen W, Hermens JLM (1998) Bioconcentration kinetics of chlorobenzenes and the organophosphorus pesticide chlorthion in the pond snail Lymnaea stagnalis—a comparison with the guppy Poecilia reticulata. Aquat Toxicol 41:301–323

    Article  CAS  Google Scholar 

  • Lu M, Horiguchi T, Shiraishi H, Shibata Y, Abo M, Okubo A, Yamazaki S (2002) Determination of testosterone in an individual shell of Thais clavigera by ELISA. Bunseki Kagaku 51:21–27

    Article  CAS  Google Scholar 

  • Maran C, Centanni E, Pellizzato F, Pavoni B (2006) Organochlorine compounds (polychlorinated biphenyls and pesticides) and polycyclic aromatic hydrocarbons in populations of Hexaplex trunculus affected by imposex in the Lagoon of Venice, Italy. Environ Toxicol Chem 25:486–495

    Article  CAS  Google Scholar 

  • Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in molluscs. Environ Toxicol Chem 17:37–43

    Article  CAS  Google Scholar 

  • Matthiessen P, Waldock R, Thain JE, Waite ME, Scrope-Howe S (1995) Changes in periwinkle (Littorina littorea) populations following the ban on TBT-based antifoulings on small boats in the United Kingdom. Ecotoxicol Environ Saf 30:180–194

    Article  CAS  Google Scholar 

  • Nishikawa J, Mamiya S, Kanayama T, Nishikawa T, Shiraishi F, Horiguchi T (2004) Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ Sci Technol 38:6271–6276

    Article  CAS  Google Scholar 

  • Oberdörster E, McClellan-Green P (2000) The neuropeptide APGWamide induces imposex in the mud snail, Ilyanassa obsoleta. Peptides 21:1323–1330

    Article  Google Scholar 

  • Oberdörster E, McClellan-Green P (2002) Mechanisms of imposex induction in the mud snail, Ilyanassa obsoleta: TBT as a neurotoxin and aromatase inhibitor. Mar Environ Res 54:715–718

    Article  Google Scholar 

  • Oberdörster E, Romano J, McClellan-Green P (2005) The neuropeptide APGWamide as a penis morphogenic factor (PMF) in gastropod molluscs. Integr Comp Biol 45:28–32

    Article  Google Scholar 

  • Oehlmann J, Schulte-Oehlmann U (2003) Molluscs as bioindicators. In: Markert BA, Breure AM, Zechmeister HG (eds) Bioindicators and biomonitors—principles, concepts and applications. Elsevier, Amsterdam, Lausanne, New York, pp 577–635

    Google Scholar 

  • Oehlmann J, Schulte-Oehlmann U, Tillmann M, 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 9:383–397

    Article  CAS  Google Scholar 

  • Oehlmann J, Schulte-Oehlmann U, Bachmann J, Oetken M, Lutz I, Kloas W, Ternes TA (2006) Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ Health Perspect 114(Suppl 1):127–133

    Google Scholar 

  • Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J (2004) Evidence for endocrine disruption in invertebrates. Int Rev Cytol 236:1–44

    Article  CAS  Google Scholar 

  • Oslo, Paris Commissions (ed) (1996) Agenda item 9 of the environmental assessment and monitoring committee (ASMO). OSPAR, Vila Franca (=ASMO 96/9/8-E)

  • Powell EN, Cummins H (1985) Are molluscan maximum life spans determined by long-term cycles in benthic communities? Oecologia 67:177–182

    Article  Google Scholar 

  • Purchon RD (1968) The biology of the Mollusca. Pergamon Press, Oxford

    Google Scholar 

  • Ramasamy MS, Murugan A (2002) Imposex in muricid gastropod Thais biserialis (Mollusca: Neogastropoda: Muricidae) from Tuticorin harbour, southeast coast of India. Indian J Mar Sci 31:243–245

    CAS  Google Scholar 

  • Rittschof D, McClellan-Green P (2005) Molluscs as multidisciplinary models in environment toxicology. Mar Pollut Bull 50:369–373

    Article  CAS  Google Scholar 

  • Ronis MJJ, Mason AZ (1996) The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: effects of tributyl tin. Mar Environ Res 42:161–166

    Article  CAS  Google Scholar 

  • Saitoh M, Yanase T, Morinaga H, Tanabe M, Mu YM, Nishi Y, Nomura M, Okabe T, Goto K, Takayanagi R, Nawata H (2001) Tributyltin or triphenyltin inhibits aromatase activity in the human granulosa-like tumor cell line KGN. Biochem Biophys Res Commun 289:198–204

    Article  CAS  Google Scholar 

  • Santos MM, ten Hallers-Tjabbes CC, Vieira N, Boon JP, Porte C (2002) Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar Environ Res 54:661–665

    Article  CAS  Google Scholar 

  • Santos MM, Castro LFC, Vieira MN, Micael J, Morabito R, Massanisso P, Reis-Henriques MA (2005) New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp Biochem Physiol C: Toxicol. Pharmacol 141:101–109

    Article  CAS  Google Scholar 

  • Sayer CD, Hoare DJ, Simpson GL, Henderson ACG, Liptrot ER, Jackson MJ, Appleby PG, Boyle JF, Jones JI, Waldock MJ (2006) TBT causes regime shift in shallow lakes. Environ Sci Technol 40:5269–5275

    Article  CAS  Google Scholar 

  • Schulte-Oehlmann U, Bettin C, Fioroni P, Oehlmann J, Stroben E (1995) Marisa cornuarietis (Gastropoda, Prosobranchia) A potential TBT bioindicator for freshwater environments. Ecotoxicology 4:372–384

    Article  CAS  Google Scholar 

  • Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J, Watermann B, Scherf S (2000) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part II: Triphenyltin as a xeno-androgen. Ecotoxicology 9:399–412

    Article  CAS  Google Scholar 

  • Schulte-Oehlmann U, Tillmann M, Casey D, Duft M, Markert B, Oehlmann J (2001) Xeno-estrogenic effects of bisphenol A in prosobranchs (Mollusca: Gastropoda: Prosobranchia). UWSF—Zeitschrift für Umweltchemie und Ökotoxikologie 13:319–333 [in German]

    Google Scholar 

  • Schulte-Oehlmann U, Oetken M, Bachmann J, Oehlmann J (2004) Effects of ethinyloestradiol and methyltestosterone in prosobranch snails. In: Kümmerer K (ed.) Pharmaceuticals in the environment. Sources, fate, effects and risks, 2nd edn. Springer, Berlin, Heidelberg, New York, pp 233–247

    Google Scholar 

  • Shi HH, Huang CJ, Zhu SX, Yu XJ, Xie WY (2005) Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Mar Ecol Prog Ser 304:179–189

    Google Scholar 

  • Spence SK, Bryan GW, Gibbs PE, Masters D, Morris L, Hawkins SJ (1990) Effects of TBT contamination on Nucella populations. Funct Ecol 4:425–432

    Article  Google Scholar 

  • Spooner N, Gibbs PE, Bryan GW, Goad LJ (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

    Article  CAS  Google Scholar 

  • St. Jean SD, Pelletier E, Courtenay SC (2002) Hemocyte functions and bacterial clearance affected in vivo by TBT and DBT in the blue mussel Mytilus edulis. Mar Ecol Prog Ser 236:163–178

    CAS  Google Scholar 

  • Strand J, Asmund G (2003) Tributyltin accumulation and effects in marine molluscs from West Greenland. Environ Pollut 123:31–37

    Article  CAS  Google Scholar 

  • Straw J, Rittschof D (2004) Responses of mud snails from low and high imposex sites to sex pheromones. Mar Pollut Bull 48:1048–1054

    Article  CAS  Google Scholar 

  • Stroben E, Oehlmann J, Bettin C (1991) TBT-induced imposex and the role of steroids in marine snails. In: Jonker JA (eds) Proceedings of the 10th world meeting of the organotin environmental programme (ORTEP) association, Berlin, September 26/27, 1991. ORTEP, Vlissingen, pp 68–73

  • Stroben E, Oehlmann J, Fioroni P (1992) Hinia reticulata and Nucella lapillus. Comparison of two gastropod tributyltin bioindicators. Mar Biol 114:289–296

    Article  Google Scholar 

  • Taylor JD, Miller JA (1989) The morphology of the osphradium in relation to feeding habits in meso- and neogastropods. J Molluscan Stud 55:227–237

    Article  Google Scholar 

  • Tillmann M (2004) Sediment toxicological investigations using gastropods and insects, with special emphasis on endocrine active substances. Cuvillier, Göttingen [in German]

    Google Scholar 

  • Tillmann M, Schulte-Oehlmann U, Duft M, Markert B, Oehlmann J (2001) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part III: Cyproterone acetate and vinclozoline as antiandrogens. Ecotoxicology 10:373–388

    Article  CAS  Google Scholar 

  • Waldock R, Rees HL, Matthiessen P, Pendle MA (1999) Surveys of the benthic infauna of the Crouch Estuary (UK) in relation to TBT contamination. J Mar Biolog Assoc UK 79:225–232

    Article  Google Scholar 

  • Werner EA, DeLuca HF (2001) Metabolism of a physiological amount of all-trans-retinol in the vitamin A-deficient rat. Arch Biochem Biophys 393:262–270

    Article  CAS  Google Scholar 

  • Woin P, Bronmark C (1992) Effects of DDT and MCPA (4-chloro-2-methylphenoxyacetic acid) on reproduction of the pond snail Lymnaea stagnalis. Bull Environ Contam Toxicol 48:7–13

    Article  CAS  Google Scholar 

  • Young WF, Whitehouse P, Johnson I, Sorokin N (2002) Proposed predicted-no-effect-concentrations (PNECs) for natural and synthetic steroid oestrogens in surface waters. Research and Development, Technical Report P2-T04/1. Environment Agency, Bristol, UK

  • Zheng RH, Wang CG, Zhao Y, Zu ZH, Chen YX (2005) Effect of tributyltin, benzo(a)pyrene and their mixture exposure on the sex hormone levels in gonads of cuvier (Sebastiscus marmoratus). Environ Toxicol Pharmacol 20:361–367

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Dr. Jochen Koop (Federal Institute of Hydrology, Koblenz, Germany) for abundance data of snails in the River Elbe and to two anonymous reviewers for their valuable comments. Financial support was provided by the European Union (COMPRENDO project, contract EVK1-CT−2002-00129) and the Federal Environmental Agency Berlin (project code 299 24 275).

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Oehlmann, J., Di Benedetto, P., Tillmann, M. et al. Endocrine disruption in prosobranch molluscs: evidence and ecological relevance. Ecotoxicology 16, 29–43 (2007). https://doi.org/10.1007/s10646-006-0109-x

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