Elevation of Testosterone Level in Periwinkle Snail Tympanotonus fuscatus var radula Exposed to Bis-Tributyltin Oxide (TBTO)
Main Article Content
Abstract
Bis (tri-n-butyltin) oxide (TBTO) is an organotin biocide used in marine antifouling paints to prevent encrustation of marine organisms on the hull of ships. The release of tributyltin (TBT) from hull of ships represents one of the main problems of direct, diffuse and continue contamination of the marine environment. To assess the effect of TBT pollution in Warri Harbour, Periwinkle snails, Tympanotonus fuscatus var radula an important shellfish in the
Niger Delta ecological zone was exposed to sublethal concentrations (0.1, 1.0, 10 and 20μg/L) of TBTO using direct sediment toxicity bioassay to determine TBT bioaccumulation and its effects on testosterone levels. Tissue analysis for TBT was done using Solid Phase Extraction (SPE) and gas chromatography with flame ionization detection (GC-FID) after derivatization with Grignard reagent pentyl magnesium chloride. The study employed the Organization for Economic Development and Cooperation (OECD) Guideline 218 protocol. Tissue analysis of T. fuscatus var radula for TBT was found to be significantly low for TBT. Serum analysis of the Periwinkles snail after 10, 20 and 30days exposure period to varying TBTO concentrations showed increased significantly (p<0.05) free testosterone levels with increased concentration and exposure durations. TBT induced elevated testosterone in snails may be indicative of imposex expression an irreversible sexual abnormality in female molluscs. The observations in this study showed that T. fuscatus var radula is susceptible to imposex development and may affect their reproductive ability which may lead to population decline.
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Ogbomida, E. T., & Ezemonye, L. I. (2013). Elevation of Testosterone Level in Periwinkle Snail Tympanotonus fuscatus var radula Exposed to Bis-Tributyltin Oxide (TBTO) . The Bioscientist Journal, 1(2), 147-157. Retrieved from https://bioscientistjournal.com/index.php/The_Bioscientist/article/view/56
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This work is licensed under a Creative Commons Attribution 4.0 International License.
References
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Alzieu, C. (2000). Impact of tributyltin on marine invertebrates. Ecotoxicology. 9:71-76.
Amr, F.A. (2004). Biological studies on the use of some invertebrates as bioindicator of pollution by one of oil drevatives. M.Sc. Thesis. Faculty of Science, Al-Azhar University, Egypt.
Axiak, V., Vella, A.J., Agius, D., Bonnici,
P., Cassar, G., Cassone, R., Chircop,
P., Micallef, D., Mintoff, B. and Sammut, M. (2000). Evaluation of Environmental Levels and Biological Impact of TBT in Malta (central Mediterranean). Science of Total Environment., 258: 89-97.
Bettin, C., Oehlmann, J. and Stroben, E. (1996). TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgol Meeresunter., 50: 299–317.
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, London 39: 231-233.
Borg, W., Shackleton, C., Pahuja, S.L and Hochburg, R.B. (1995). Long-lived testosterone esters in the rat. Proc Natl Acad Sci USA 92:1545–1549.
Bortoli, A., Troncon, A., Dariol S., Pellizzato, F. and Pavoni, B. (2003).
Butyltins and phenyltins in biota and sediments from the Lagoon of Venice. Oceanologia 45:7–23.
Bryan, G. W., Gibbs, P. E., Burt, G.R and Hummerstone, L.G. (1987). The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: Long-term field and laboratory experiments. J. Mar. Biol. Assoc. U.K. 67:525-544.
Bryan, G. W., Gibbs, P. E., Hummerstone, L. G. and Burt, G. R. (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.
Chiavarini, S., Massanisso, P., Nicolai, P., Nobili, C. and Morabito, R. (2003). Butyltins concentration levels and imposex occurence in snails from the Sicilian coasts (Italy). Chemosphere., 50: 311–319.
Courant, F., Antignac, J.P., Maume, D., Monteau, F., Andersson, A.M., Skakkebaek, N., Andre, F. and Le Bizec, B. (2007). Exposure assessment of prepubertal children to steroid endocrine disrupters 1. Analytical strategy for estrogens measurement in plasma at ultra-trace level. In Analytica Chimica Acta, vol. 586 (1-2): 105-114.
de Mora, S.J. (1996). Tributyltin: case study of an environmental contaminant. Camb. Environ. Chem. Ser. 8: 389.
deFur, P.L., Crane, M., Ingershold, C. and Tattersfield, L. (1999). Endocrine Disruption in Invertebrates: Endocrinology, Testing and Assessment. Society of Environmental Toxicology and Chemistry, Pensacola, FL, USA.
Fent, K and Stegeman, J.J. (1993). Effects of tributyltin in vivo on hepatic cytochrome P-450 forms in marine fish. Aquatic Toxicology 24:219.
Fernandez, M.A., De Luca Rebello
Wagener, A., Limaverde, A.M.,
154
Scofield, A.L., Pinheiro, F.M. and Rodrigues, E. (2005). Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental
Research., 59: 435-452.
Fioroni, P., Oehlmann, J and Stroben, E. (1991). The pseudohermaphroditism of prosobranchs; Morphological aspects. Zoologischer Anzeiger. 226, 1-26.
Goldberg, E. D. (1986). TBT - an environmental dilemma.
Environment 28: 17-44.
Gooding, M.P., Gallardo, C.S and Leblanc, G.A. (1999). Imposex in three marine gastropod species in Chile and potential impact on muriciculture. Mar. Poll. Bull., 38: 1227-1231.
Gooding, M.P., Wilson, V.S., Folmar,
L.C., Marcovich, D.T and LeBlanc, G.A. (2003). The Biocide Tributyltin
Reduces the Accumulation of Testosterone as Fatty Acid Esters in the Mud Snail (Ilyanassa obsoleta). Environ Health Perspect., 111: 426430.
Hall, Jr W., Scott, M.C., killen, W.D and Unger, M.A. (2000). A probabilistic ecological risk assessment of tributyltin in surface waters of the Chesapeake Bay watershed. Human Ecol. 6: 141-179.
International Maritime Organization. (2001). Final Act. International Conference on the Control of Harmful Anti-Fouling Systems for Ships, 1-5 October 2001.Report No. AFS/CONF/25. London:
International Maritime Organization.
Jenner, M.G. (1979). Pseudohermaphroditism in Ilyanassa obsoleta (Mollusca:Neogastropoda). Science. 205: 1407–1409.
Jobling, S., Coey, S., Whitmore, J. G., Kime, D. E., Van Look, K. J. W.,
McAllister, B. G., Beresford, N., Henshaw, A.C., Brighty, G., Tyler,
C.R. and Sumpter, J.P. (2002). Wild Intersex Roach (Rutilus rutilus) Have Reduced Fertility. Biology of
Reproduction., 67: 515 - 524.
Kishimoto, Y. (1973). Fatty acid esters of testosterone in rat brain: identification, distribution and some properties of enzymes which synthesize and hydrolyze the esters. Arch Biochem Biophys., 159:528– 542.
LeBlanc, G.A. and Bain, L.J. (1997). Chronic toxicity of environmental contaminants: Sentinels and biomarkers. Environ Health Perspect 105:65–80.
Linley-Adams, G. (1999). The accumulation and impact of organotins on marine mammals, seabirds and fish for human consumption. A report for WWF-UK, Project no. 98054. 26p.
Livingstone, D.R and Farrar, S.V. (1985). Responses of the Mixed-Function Oxidase System of Some Bivalve and Gastropod Mollusks to Exposure to Polynuclear Aromatic and Other Hydrocarbons. Mar. Environ. Res. 17: 101-105.
Matthiessen, P. and Gibbs, P.E. (1998). Critical appraisals of the evidence for tributyltin mediated endocrine disruption in mollusks. Environ. Toxicol. Chem., 17: 37 - 43.
Matthiessen, P., Waldock, R., Thain, J.E., Waite, M.E and Scrope-Howe, S. (1995). Changes in the periwinkle (Littorina littorea) populations following the ban on TBT-based antifoulings on small boats in the United Kingdom. Ecotoxicol Environ Saf. 30: 180–194.
Meador, J.P. (1997). Comparative toxicokinetics of tributyltin in five marine species and its utility in predicting bioaccumulation and acte toxicity. Aqua.Toxicol., 37(4): 307326.
Michel, P., Averty, B., Andral, B., Chiffoleau, J.F. and Galgani, F.
155
(2001). Tributyltin along the coasts of Corsica (Western Mediterranean): a persistent problem. Mar. Pollut. Bull. 42 (11): 1128– 1132.
Nash, J.P., Kime, D.E., Van, V.L.T., Wester, P.W., Brion, F., Maack, G., Stahlschmidt, A.P and Tyler, C.R. (2004). Long-term exposure to environmental concentrations of the pharmaceutical ethynlestradiol causes reproductive failure in fish. Environ. Health. Perspect., 112: 1725 - 1733.
Nicholson, G.J and Evans, S.M. (1997). Anthropogenic Impacts on the Stock of the Common Whelk Buccinum undatum (L.) Marine
Environmental Research. 44(3): 305314.
Oberdörster, E. and McClellan-Green, P.
(2000). The neuropeptide
APGWamide induces imposex in the mud snail (Ilyanassa obsoleta) Peptides., 21:1323–1330.
OECD. (OECD) Guidelines for testing of chemicals. (2002). Sediment water chironomid toxicity test using spiked sediment. Revised draft guideline 218, December 2002, Paris.
Oehlmann, J., Stroben, E and Fioroni, P. (1993). Hormonal disorders and tributyltin-induced imposex in marine snails. In: Quantified Phenotypic Responses in
Morphology and Physiology (Aldrich JC, ed). Proceedings of the 27th
European Marine Biology
Symposium, 7-11 September 1992, Dublin, Ireland. Ashford,
Ireland:Japaga Publishers, 301-305.
Otitoloju, A.A. (2002). Evaluation of the joint-action toxicity of binary mixtures of heavy metals against the mangrove periwinkle Tympanotonus fuscatus var radula (L.). Ecotoxicol. Environ. Saf. 53: 404-415.
Parks, L.G., Cheek, A.O., Denslow, N.D., Heppell, S.A., McLachlan, J.A. and LeBlanc, G.A. (1999). Fathead minnow (Pimphales promelas) vitellogenin: purification, characterization and quantitative immunoassay for the detection of estrogenic compounds. Comp
Biochem Physiol., C 123:113–125.
Peterle, T.J. (1991). Wildlife Toxicology. Van Nostrand Reinhold, New York, USA.
Ronis, M. J. J and Mason, A. Z. (1996). The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: Effects of tributyltin. Mar. Environ. Res. 42:
161-166.
Rosenberg, D.W and Drummond, G.S. (1983) Direct in virro effects of bis(tributyl) tin oxide on hepatic cytochrome P-450. Biochem. pharmacol. 32: 3823-3829.
Santos, M. M., Castro, L. F. C., Vieira, M. N., Micael, J., Morabito, R.,
Massanisso, P and Reis-Henriques, M. A. (2005). New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp. Biochem. Physiol. C. 141: 101-109.
Smith, B. S. (1981). Tributyltin compounds induce male characteristics on female mud snails. Nassarius obsoletus, Ilyanassa obsoleta. Journal of Applied
Toxicology, 3: 141-144
Spooner, N. and Goad, L. J. (1990). Steroids and imposex of the dog whelk Nucella lapillus. Proc. 3. International Organotin Symposium.
Spooner, N., Gibbs, P.E., Bryan, G.W. and Goad, L.J. (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.
Stroben, E., Oehlmann, J. and Bettin, C. (1991). TBT-induced imposex and the role of steroids in marine snails. Proceedings, 10th World Meeting of ORTEP (Organotin Environmental Programme) Association, Berlin, Germany September 26–27, 1990, pp 68–73.
156
Tanabe, S. (1999). Butyltin Contamination in Marine Mammals – A Review. Marine Pollution Bulletin., 39 (1-12): 62-72.
Ten Hallers-Tjabbes, C. C., Kemp, J. F and Boon, J. P. (1994). Imposex in whelks (Buccinum undatum) from the open North Sea: relation to shipping traffic. Marine pollution bulletin 28:311-313.
Terlizzi, A., Delos, A.L., Garaventa, F., Faimali, M. and Geraci, S. (2004). Limited effectiveness of marine protected areas: imposex in Hexaplex trunculus (Gastropoda: Muricidae) populations from Italian marine reserves. Mar Pollut Bull., 48:188– 192.
Tokolo, C.A. (1988). Studies on the Toxicity of some Nigerian Crude oil against Tympanotonus fuscatus var radula L. under different salinity regimes. M.Sc. Thesis. University of Lagos Nigeria.
WHO (1990). Tributyltin compounds. Environmental health criteria. 116, World Health Organisation, Geneva. ISBN 92 4 157116 0
World Health Organization (WHO). (1980). Tin and organotin compounds: a preliminary review. In: Environmental Health Criteria 15, Geneva: World Health Organization,
Switzerland. Solbe, J. F and De, L. G. (1995). Handbook of
Ecotoxicology edited by Peter Calins.
Published by Blackwell Science Limited, pp: 64-68.
Zucker, R.M., Massaro, E. J. and Elstein, K.H. (1992). The reversibility of tributyltin-induced toxicity in vitro as a function of concentration and duration of exposure (C x T). Environmental Research., 57: 107-116.
Alzieu, C. (1998). Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast. Manag. 40 (1), 23–36.
Alzieu, C. (2000). Impact of tributyltin on marine invertebrates. Ecotoxicology. 9:71-76.
Amr, F.A. (2004). Biological studies on the use of some invertebrates as bioindicator of pollution by one of oil drevatives. M.Sc. Thesis. Faculty of Science, Al-Azhar University, Egypt.
Axiak, V., Vella, A.J., Agius, D., Bonnici,
P., Cassar, G., Cassone, R., Chircop,
P., Micallef, D., Mintoff, B. and Sammut, M. (2000). Evaluation of Environmental Levels and Biological Impact of TBT in Malta (central Mediterranean). Science of Total Environment., 258: 89-97.
Bettin, C., Oehlmann, J. and Stroben, E. (1996). TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgol Meeresunter., 50: 299–317.
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, London 39: 231-233.
Borg, W., Shackleton, C., Pahuja, S.L and Hochburg, R.B. (1995). Long-lived testosterone esters in the rat. Proc Natl Acad Sci USA 92:1545–1549.
Bortoli, A., Troncon, A., Dariol S., Pellizzato, F. and Pavoni, B. (2003).
Butyltins and phenyltins in biota and sediments from the Lagoon of Venice. Oceanologia 45:7–23.
Bryan, G. W., Gibbs, P. E., Burt, G.R and Hummerstone, L.G. (1987). The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: Long-term field and laboratory experiments. J. Mar. Biol. Assoc. U.K. 67:525-544.
Bryan, G. W., Gibbs, P. E., Hummerstone, L. G. and Burt, G. R. (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.
Chiavarini, S., Massanisso, P., Nicolai, P., Nobili, C. and Morabito, R. (2003). Butyltins concentration levels and imposex occurence in snails from the Sicilian coasts (Italy). Chemosphere., 50: 311–319.
Courant, F., Antignac, J.P., Maume, D., Monteau, F., Andersson, A.M., Skakkebaek, N., Andre, F. and Le Bizec, B. (2007). Exposure assessment of prepubertal children to steroid endocrine disrupters 1. Analytical strategy for estrogens measurement in plasma at ultra-trace level. In Analytica Chimica Acta, vol. 586 (1-2): 105-114.
de Mora, S.J. (1996). Tributyltin: case study of an environmental contaminant. Camb. Environ. Chem. Ser. 8: 389.
deFur, P.L., Crane, M., Ingershold, C. and Tattersfield, L. (1999). Endocrine Disruption in Invertebrates: Endocrinology, Testing and Assessment. Society of Environmental Toxicology and Chemistry, Pensacola, FL, USA.
Fent, K and Stegeman, J.J. (1993). Effects of tributyltin in vivo on hepatic cytochrome P-450 forms in marine fish. Aquatic Toxicology 24:219.
Fernandez, M.A., De Luca Rebello
Wagener, A., Limaverde, A.M.,
154
Scofield, A.L., Pinheiro, F.M. and Rodrigues, E. (2005). Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental
Research., 59: 435-452.
Fioroni, P., Oehlmann, J and Stroben, E. (1991). The pseudohermaphroditism of prosobranchs; Morphological aspects. Zoologischer Anzeiger. 226, 1-26.
Goldberg, E. D. (1986). TBT - an environmental dilemma.
Environment 28: 17-44.
Gooding, M.P., Gallardo, C.S and Leblanc, G.A. (1999). Imposex in three marine gastropod species in Chile and potential impact on muriciculture. Mar. Poll. Bull., 38: 1227-1231.
Gooding, M.P., Wilson, V.S., Folmar,
L.C., Marcovich, D.T and LeBlanc, G.A. (2003). The Biocide Tributyltin
Reduces the Accumulation of Testosterone as Fatty Acid Esters in the Mud Snail (Ilyanassa obsoleta). Environ Health Perspect., 111: 426430.
Hall, Jr W., Scott, M.C., killen, W.D and Unger, M.A. (2000). A probabilistic ecological risk assessment of tributyltin in surface waters of the Chesapeake Bay watershed. Human Ecol. 6: 141-179.
International Maritime Organization. (2001). Final Act. International Conference on the Control of Harmful Anti-Fouling Systems for Ships, 1-5 October 2001.Report No. AFS/CONF/25. London:
International Maritime Organization.
Jenner, M.G. (1979). Pseudohermaphroditism in Ilyanassa obsoleta (Mollusca:Neogastropoda). Science. 205: 1407–1409.
Jobling, S., Coey, S., Whitmore, J. G., Kime, D. E., Van Look, K. J. W.,
McAllister, B. G., Beresford, N., Henshaw, A.C., Brighty, G., Tyler,
C.R. and Sumpter, J.P. (2002). Wild Intersex Roach (Rutilus rutilus) Have Reduced Fertility. Biology of
Reproduction., 67: 515 - 524.
Kishimoto, Y. (1973). Fatty acid esters of testosterone in rat brain: identification, distribution and some properties of enzymes which synthesize and hydrolyze the esters. Arch Biochem Biophys., 159:528– 542.
LeBlanc, G.A. and Bain, L.J. (1997). Chronic toxicity of environmental contaminants: Sentinels and biomarkers. Environ Health Perspect 105:65–80.
Linley-Adams, G. (1999). The accumulation and impact of organotins on marine mammals, seabirds and fish for human consumption. A report for WWF-UK, Project no. 98054. 26p.
Livingstone, D.R and Farrar, S.V. (1985). Responses of the Mixed-Function Oxidase System of Some Bivalve and Gastropod Mollusks to Exposure to Polynuclear Aromatic and Other Hydrocarbons. Mar. Environ. Res. 17: 101-105.
Matthiessen, P. and Gibbs, P.E. (1998). Critical appraisals of the evidence for tributyltin mediated endocrine disruption in mollusks. Environ. Toxicol. Chem., 17: 37 - 43.
Matthiessen, P., Waldock, R., Thain, J.E., Waite, M.E and Scrope-Howe, S. (1995). Changes in the periwinkle (Littorina littorea) populations following the ban on TBT-based antifoulings on small boats in the United Kingdom. Ecotoxicol Environ Saf. 30: 180–194.
Meador, J.P. (1997). Comparative toxicokinetics of tributyltin in five marine species and its utility in predicting bioaccumulation and acte toxicity. Aqua.Toxicol., 37(4): 307326.
Michel, P., Averty, B., Andral, B., Chiffoleau, J.F. and Galgani, F.
155
(2001). Tributyltin along the coasts of Corsica (Western Mediterranean): a persistent problem. Mar. Pollut. Bull. 42 (11): 1128– 1132.
Nash, J.P., Kime, D.E., Van, V.L.T., Wester, P.W., Brion, F., Maack, G., Stahlschmidt, A.P and Tyler, C.R. (2004). Long-term exposure to environmental concentrations of the pharmaceutical ethynlestradiol causes reproductive failure in fish. Environ. Health. Perspect., 112: 1725 - 1733.
Nicholson, G.J and Evans, S.M. (1997). Anthropogenic Impacts on the Stock of the Common Whelk Buccinum undatum (L.) Marine
Environmental Research. 44(3): 305314.
Oberdörster, E. and McClellan-Green, P.
(2000). The neuropeptide
APGWamide induces imposex in the mud snail (Ilyanassa obsoleta) Peptides., 21:1323–1330.
OECD. (OECD) Guidelines for testing of chemicals. (2002). Sediment water chironomid toxicity test using spiked sediment. Revised draft guideline 218, December 2002, Paris.
Oehlmann, J., Stroben, E and Fioroni, P. (1993). Hormonal disorders and tributyltin-induced imposex in marine snails. In: Quantified Phenotypic Responses in
Morphology and Physiology (Aldrich JC, ed). Proceedings of the 27th
European Marine Biology
Symposium, 7-11 September 1992, Dublin, Ireland. Ashford,
Ireland:Japaga Publishers, 301-305.
Otitoloju, A.A. (2002). Evaluation of the joint-action toxicity of binary mixtures of heavy metals against the mangrove periwinkle Tympanotonus fuscatus var radula (L.). Ecotoxicol. Environ. Saf. 53: 404-415.
Parks, L.G., Cheek, A.O., Denslow, N.D., Heppell, S.A., McLachlan, J.A. and LeBlanc, G.A. (1999). Fathead minnow (Pimphales promelas) vitellogenin: purification, characterization and quantitative immunoassay for the detection of estrogenic compounds. Comp
Biochem Physiol., C 123:113–125.
Peterle, T.J. (1991). Wildlife Toxicology. Van Nostrand Reinhold, New York, USA.
Ronis, M. J. J and Mason, A. Z. (1996). The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: Effects of tributyltin. Mar. Environ. Res. 42:
161-166.
Rosenberg, D.W and Drummond, G.S. (1983) Direct in virro effects of bis(tributyl) tin oxide on hepatic cytochrome P-450. Biochem. pharmacol. 32: 3823-3829.
Santos, M. M., Castro, L. F. C., Vieira, M. N., Micael, J., Morabito, R.,
Massanisso, P and Reis-Henriques, M. A. (2005). New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp. Biochem. Physiol. C. 141: 101-109.
Smith, B. S. (1981). Tributyltin compounds induce male characteristics on female mud snails. Nassarius obsoletus, Ilyanassa obsoleta. Journal of Applied
Toxicology, 3: 141-144
Spooner, N. and Goad, L. J. (1990). Steroids and imposex of the dog whelk Nucella lapillus. Proc. 3. International Organotin Symposium.
Spooner, N., Gibbs, P.E., Bryan, G.W. and Goad, L.J. (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.
Stroben, E., Oehlmann, J. and Bettin, C. (1991). TBT-induced imposex and the role of steroids in marine snails. Proceedings, 10th World Meeting of ORTEP (Organotin Environmental Programme) Association, Berlin, Germany September 26–27, 1990, pp 68–73.
156
Tanabe, S. (1999). Butyltin Contamination in Marine Mammals – A Review. Marine Pollution Bulletin., 39 (1-12): 62-72.
Ten Hallers-Tjabbes, C. C., Kemp, J. F and Boon, J. P. (1994). Imposex in whelks (Buccinum undatum) from the open North Sea: relation to shipping traffic. Marine pollution bulletin 28:311-313.
Terlizzi, A., Delos, A.L., Garaventa, F., Faimali, M. and Geraci, S. (2004). Limited effectiveness of marine protected areas: imposex in Hexaplex trunculus (Gastropoda: Muricidae) populations from Italian marine reserves. Mar Pollut Bull., 48:188– 192.
Tokolo, C.A. (1988). Studies on the Toxicity of some Nigerian Crude oil against Tympanotonus fuscatus var radula L. under different salinity regimes. M.Sc. Thesis. University of Lagos Nigeria.
WHO (1990). Tributyltin compounds. Environmental health criteria. 116, World Health Organisation, Geneva. ISBN 92 4 157116 0
World Health Organization (WHO). (1980). Tin and organotin compounds: a preliminary review. In: Environmental Health Criteria 15, Geneva: World Health Organization,
Switzerland. Solbe, J. F and De, L. G. (1995). Handbook of
Ecotoxicology edited by Peter Calins.
Published by Blackwell Science Limited, pp: 64-68.
Zucker, R.M., Massaro, E. J. and Elstein, K.H. (1992). The reversibility of tributyltin-induced toxicity in vitro as a function of concentration and duration of exposure (C x T). Environmental Research., 57: 107-116.