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Contamination by Organotins and Its Population-Level Effects Involved by Imposex in Prosobranch Gastropods

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Biological Effects by Organotins

Abstract

A history of the production and use of organotin compounds is briefly introduced. The worldwide use of tributyltin (TBT)- or triphenyltin (TPhT)-based antifouling paints since the mid-1960s has caused extensive contamination in the aquatic environment, especially in the marine environment, which led to contamination of aquatic organisms by these compounds and became a concern in terms of both seafood safety and ecotoxicology. Legislation of TBT- and TPhT-based antifouling paints began in Europe and the U.S.A in the 1980s and in Japan in 1990. An International Convention on the Control of Harmful Anti-fouling Systems on Ships (AFS Convention) for the worldwide ban of TBT- and TPhT-based antifouling paints came into force on 17 September 2008. Organotins have various toxicities to vertebrates and invertebrates; imposex is known to be induced in many gastropod species by TBT and also by TPhT released from antifouling paints on ships and fishing nets. Reproductive failure may be brought about in severely affected stages of imposex, resulting in population decline or mass extinction. Population-level effects involved by imposex and similar phenomena are described in the rock shell (Thais clavigera), the ivory shell (Babylonia japonica), and the giant abalone (Haliotis madaka), with special reference to tissue distributions of TBT, TPhT and their metabolites.

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Abbreviations

AFS Convention:

an International Convention on the Control of Harmful Anti-fouling Systems on Ships

DBT:

dibutyltin

DPhT:

diphenyltin

GC-FPD:

gas chromatography with flame photometric detection

MBT:

monobutyltin

MPhT:

monophenyltin

RXR:

retinoid X receptor

TBT:

tributyltin

TBT-MMC:

tributyltin methyl methacrylate copolymer

TBTO:

bis (tributyltin) oxide

TcHT:

tricyclohexyltin

TPhT:

triphenyltin

TPrT:

tripropyltin

References

  • Alzieu C (1996) Biological effects of tributyltin on marine organisms. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 167–211

    Chapter  Google Scholar 

  • Batley G (1996) The distribution and fate of tributyltin in the marine environment. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 139–166

    Chapter  Google Scholar 

  • Bauer B, Fioroni P, Ide I et al (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 

  • Bech M (2002a) A survey of imposex in muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island, Thailand. Mar Pollut Bull 44:887–896

    Article  CAS  Google Scholar 

  • Bech M (2002b) Imposex and tributyltin contamination as consequence of the establishment of a marina and increasing yachting activities at Phuket Island, Thailand. Environ Pollut 117:421–429

    Article  CAS  Google Scholar 

  • Bennett RF (1996) Industrial manufacture and application of tributyltin compounds. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 21–61

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Blaber SJM (1970) The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.). Proc Malacol Soc Lond 39:231–233

    Google Scholar 

  • Bosselmann K (1996) Environmental law and tributyltin in the environment. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 237–263

    Chapter  Google Scholar 

  • Bryan GW, Gibbs PE, Hummerstone LG et al (1986) The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Assoc UK 66:611–640

    Article  CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR et al (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J Mar Biol Assoc UK 67:525–544

    Article  CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR (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 Assoc UK 68:733–744

    Article  CAS  Google Scholar 

  • Castro LFC, Lima D, Machado A et al (2007) Imposex induction is mediated through the retinoid X receptor signalling pathway in the neogastropod Nucella lapillus. Aquat Toxicol 85:57–66

    Article  CAS  Google Scholar 

  • Coelho MR, Fuentes S, Bebianno MJ (2001) TBT effects on the larvae of Ruditapes decussates. J Mar Biol Assoc U K 81:259–265

    Article  Google Scholar 

  • Féral C, Le Gall S (1983) The influence of a pollutant factor (TBT) on the neurosecretory mechanism responsible for the occurrence of a penis in the females of Ocenebra erinacea. In: Lever J, Boer HH (eds) Molluscan neuro-endocrinology. North Holland, Amsterdam, pp 173–175

    Google Scholar 

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

    Google Scholar 

  • Fretter V (1984) Prosobranchs. In: Wilbur KM (ed) The mollusca, vol 7, reproduction (Tompa AS, Verdonk NH, van den Biggelaar JAM eds). Academic, Orlando, pp 1–45

    Google Scholar 

  • Gibbs PE, Bryan GW (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 66:767–777

    Article  CAS  Google Scholar 

  • Gibbs PE, Bryan GW (1996) TBT-induced imposex in neogastropod snails: masculinization to mass extinction. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 212–236

    Chapter  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc UK 67:507–523

    Article  CAS  Google Scholar 

  • Gibbs PE, Pascoe PL, Burt GR (1988) Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68:715–731

    Article  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributyltin-induced imposex. J Mar Biol Assoc UK 70:639–656

    Article  Google Scholar 

  • Gibbs PE, Spencer BE, Pascoe PL (1991) The American oyster drill, Urosalpinx cinerea (Gastropoda): evidence of decline in an imposex affected population (R. Blackwater, Essex). J Mar Biol Assoc UK 71:827–838

    Article  Google Scholar 

  • Gooding MP, Wilson VS, Folmar LC et al (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 

  • Hall LW Jr, Bushong SJ (1996) A review of acute effects of tributyltin compounds on aquatic biota. In: Champ MA, Seligman PF (eds) Organotin: environmental fate and effects. Chapman & Hall, London, pp 157–190

    Chapter  Google Scholar 

  • Hamada M, Inoue M (1993) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat: 193–195

    Google Scholar 

  • Hamada M, Inoue M (1994) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat: 182–184

    Google Scholar 

  • Hamada M, Inoue M (1995) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat: 204–206

    Google Scholar 

  • Hamada F, Kanazawa T, Yamamoto E (1988) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat 6:110–116

    Google Scholar 

  • Hamada F, Kanazawa T, Yamamoto E (1989) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat 7:103–109

    Google Scholar 

  • Hoch M (2001) Organotin compounds in the environment: an overview. Appl Geochem 16:719–743

    Article  CAS  Google Scholar 

  • Horiguchi T (1993). Imposex caused by organotin compounds in marine gastropods from Japan (PhD thesis, in Japanese). The University of Tokyo, Bunkyo-ku, Tokyo

    Google Scholar 

  • Horiguchi T (2000) Molluscs. In: Kawai S, Koyama J (eds) Problems of endocrine disruptors in fisheries environment. Koseisha-Koseikaku, Tokyo, pp 54–72 (in Japanese)

    Google Scholar 

  • Horiguchi T (2004) Gastropods. In: Takeuchi I, Tanabe S, Hino A (eds) Biological monitoring for anthropogenic chemicals in low dose. Koseisha-Koseikaku, Tokyo, pp 37–67 (in Japanese)

    Google Scholar 

  • Horiguchi T (2012) Ecotoxicological impacts of organotins: an overview. In: Pagliarani A, Trombetti F, Ventrella V (eds) (e-book) Biochemical and biological effects of organotins. Bentham Science, pp 3–24. eISBN: 978-1-60805-265-3, doi:10.2174/97816080526531120101

  • Horiguchi T, Shimizu M (1992) Effects on aquatic organisms, mainly on molluscs. In: Satomi Y, Shimizu M (eds) Organotin pollution and its effects on aquatic organisms. Koseisha-Koseikaku, Tokyo, pp 99–135 (in Japanese)

    Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1994) Imposex and organotin compounds in Thais clavigera and T. bonni in Japan. J Mar Biol Assoc UK 74:651–669

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1995) Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from antifouling paints. Mar Pollut Bull 31:402–405

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1997a) 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, Shiraishi H, Shimizu M et al (1997b) Imposex in sea snails, caused by organotin (tributyltin and triphenyltin) pollution in Japan: a survey. Appl Organomet Chem 11:451–455

    Article  CAS  Google Scholar 

  • Horiguchi T, Takiguchi N, Cho HS et al (2000) Ovo-testis and disturbed reproductive cycle in the giant abalone, Haliotis madaka: possible linkage with organotin contamination in a site of population decline. Mar Environ Res 50:223–229

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Kaya M et al (2002) Tributyltin and triphenyltin induce spermatogenesis in ovary of female abalone, Haliotis gigantea. Mar Environ Res 54:679–684

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Hamada F et al (2006) Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect 114(suppl 1):13–19

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2007) Retinoid X receptor gene expression and protein content in tissues of the rock shell Thais clavigera. Aquat Toxicol 84:379–388

    Article  CAS  Google Scholar 

  • Horiguchi T, Ohta Y, Nishikawa T et al (2008) Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol Toxicol 24:553–562

    Article  Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2010a) Time course of expression of the retinoid X receptor gene and induction of imposex in the rock shell, Thais clavigera, exposed to triphenyltin chloride. Anal Bioanal Chem 396:597–607

    Article  CAS  Google Scholar 

  • Horiguchi T, Urushitani H, Ohta Y et al (2010b) Establishment of a polyclonal antibody against the retinoid X receptor of the rock shell Thais clavigera and its application to rock shell tissues for imposex research. Ecotoxicology 19:571–576

    Article  CAS  Google Scholar 

  • Horiguchi T, Lee JH, Park JC et al (2012) Specific accumulation of organotin compounds in tissues of the rock shell, Thais clavigera. Mar Environ Res 76:56–62

    Article  CAS  Google Scholar 

  • Imai T, Takiguchi N, Horiguchi T (2006) Estimation of the causal factor for declining abalone populations in Jogashima, Kanagawa, Japan. Bull Kanagawa Prefect Fish Technol Cent 1:51–58 (in Japanese)

    Google Scholar 

  • Inoue S, Oshima Y, Nagai K et al (2004) Effect of maternal exposure to tributyltin on reproduction of the pearl oyster (Pinctada fucata martensii). Environ Toxicol Chem 23:1276–1281

    Article  CAS  Google Scholar 

  • Kajikawa A (1984) Sexual characteristics, spawning abilities and their percentage occurrence in populations of Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat 2:31–32

    Google Scholar 

  • Kajikawa A, Yamamoto E, Masutani R (1983) Sexual characteristics and spawning abilities in the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefec Fish Exp Stat 1:16–18

    Google Scholar 

  • Lapota D, Rosenberger DE, Platter-Rieger MF et al (1993) Growth and survival of Mytilus edulis larvae exposed to low levels of dibutyltin and tributyltin. Mar Biol 115:413–419

    Article  CAS  Google Scholar 

  • Laughlin RB Jr (1996) Bioaccumulation of TBT by aquatic organisms. In: Champ MA, Seligman PF (eds) Organotin: environmental fate and effects. Chapman & Hall, London, pp 331–355

    Chapter  Google Scholar 

  • Li Q, Osada M, Takahashi K et al (1997) Accumulation and depuration of tributyltin oxide and its effect on the fertilization and embryonic development in the Pacific oyster, Crassostrea gigas. Bull Environ Contam Toxicol 58:489–496

    Article  CAS  Google Scholar 

  • Maguire RJ (1996) The occurrence, fate and toxicity of tributyltin and its degradation products in fresh water environments. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 94–138

    Chapter  Google Scholar 

  • Marshall DJ, Rajkumar A (2003) Imposex in the indigenous Nassarius kraussianus (Mollusca: Neogastropoda) from South African harbours. Mar Pollut Bull 46:1150–1155

    Article  CAS  Google Scholar 

  • Maruyama T (1992) The regulations of organotin compounds in foreign countries. In: Satomi Y, Shimizu M (eds) Organotin pollution and its effects on aquatic organisms. Koseisha-Koseikaku, Tokyo, pp 154–170 (in Japanese)

    Google Scholar 

  • Mensink B, Boon JP, ten Hallers-Tjabbes CC et al (1997) Bioaccumulation of organotin compounds and imposex occurrence in a marine food chain (Eastern Scheldt, The Netherlands). Environ Technol 18:1235–1245

    Article  CAS  Google Scholar 

  • Nakayama K, Oshima Y, Nagafuchi K et al (2005) Early-life-stage toxicity in offspring from exposed parent medaka, Oryzias latipes, to mixtures of tributyltin and polychlorinated biphenyls. Environ Toxicol Chem 24:591–596

    Article  CAS  Google Scholar 

  • Nishikawa J, Mamiya S, Kanayama T et al (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 APGW amide induces imposex in the mud snail Ilyanassa obsoleta. Peptides 21:1323–1330

    Article  Google Scholar 

  • Oehlmann J, Fioroni P, Stroben E et al (1996) Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci Total Environ 188:205–223

    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 tributyltin. Mar Environ Res 42:161–166

    Article  CAS  Google Scholar 

  • Ruiz JM, Bryan GW, Gibbs PE (1995) Acute and chronic toxicity of tributyltin (TBT) to pediveliger larvae of the bivalve Scrobularia plana. Mar Biol 124:119–126

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Shim WJ, Kahng SH, Hong SH et al (2000) Imposex in the rock shell, Thais clavigera, as evidence of organotin contamination in the marine environment of Korea. Mar Environ Res 49:435–451

    Article  CAS  Google Scholar 

  • Smith BS (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proc Malacol Soc Lond 39:377–378

    Google Scholar 

  • Sole M, Morcillo Y, Porte C (1998) Imposex in the commercial snail Bolinus brandaris in the northwestern Mediterranean. Environ Pollut 99:241–246

    Article  CAS  Google Scholar 

  • Sternberg RM, LeBlanc GA (2006) Kinetic characterization of the inhibition of acyl coenzyme A: steroid acyltransferases by tributyltin in the eastern mud snail (Ilyanassa obsoleta). Aquat Toxicol 78:233–242

    Article  CAS  Google Scholar 

  • Sternberg RM, Hotchkiss AK, LeBlanc GA (2008) Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc. Environ Sci Technol 42:1345–1351

    Article  CAS  Google Scholar 

  • Stewart C (1996) The efficacy of legislation in controlling tributyltin in the marine environment. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 264–297

    Chapter  Google Scholar 

  • Sugita A (1992) History of the use and regulation of organotin compounds in Japan. In: Satomi Y, Shimizu M (eds) Organotin pollution and its effects on aquatic organisms. Koseisha-Koseikaku, Tokyo, pp 9–19 (in Japanese)

    Google Scholar 

  • Takeuchi M (1992) Behavior and distribution of organotin compounds in the marine environment. In: Satomi Y, Shimizu M (eds) Organotin pollution and its effects on aquatic organisms. Koseisha-Koseikaku, Tokyo, pp 56–67 (in Japanese)

    Google Scholar 

  • Tanabe S, Prudente M, Mizuno T et al (1998) Butyltin contamination in marine mammals from north Pacific and Asian coastal waters. Environ Sci Technol 32:193–198

    Article  CAS  Google Scholar 

  • Ten Hallers-Tjabbes CC, Wegener JW, Van Hattum BA et al (2003) Imposex and organotin concentrations in Buccinum undatum and Neptunea antiqua from the North Sea: relationship to shipping density and hydrographical conditions. Mar Environ Res 55:203–233

    Article  Google Scholar 

  • Terlizzi A, Delos AL, Garaventa F et al (2004) Limited effectiveness of marine protected areas: imposex in Hexaplex trunculus (Gastropoda: Muricidae) populations from Italian marine reserves. Mar Pollut Bull 48:188–192

    Article  CAS  Google Scholar 

  • Treuner-Freeman AB, Horiguchi T, Takiguchi N et al (2009) Sublethal effects of tributyltin and triphenyltin on larvae of three species of abalone from Japan. Aust J Ecotoxicol 15:25–34

    Google Scholar 

  • U.S. EPA (1988) Ambient water criteria for tributyltin-1988 (Draft 6/16/1988). Unites States Environmental Protection Agency, Duluth

    Google Scholar 

  • Uki N (1989) Sexual maturation, development and growth in gastropods, and their control. In: Takashima F, Hanyu I (eds) Reproductive biology of fish and shellfish. Midori Shobo, Tokyo, pp 367–417 (in Japanese)

    Google Scholar 

  • Urushitani H, Katsu Y, Ohta Y et al (2011) Cloning and characterization of retinoid X receptor (RXR) isoforms in the rock shell, Thais clavigera. Aquat Toxicol 103:101–111

    Article  CAS  Google Scholar 

  • WHO (1980) Environmental health criteria 15: tin and organotin compounds. World Health Organization, Geneva

    Google Scholar 

  • WHO (1990) Environmental health criteria 116: tributyltin compounds. World Health Organization, Geneva

    Google Scholar 

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Horiguchi, T. (2017). Contamination by Organotins and Its Population-Level Effects Involved by Imposex in Prosobranch Gastropods. In: Horiguchi, T. (eds) Biological Effects by Organotins. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56451-5_4

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