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Imposex in Thais gradata as a Biomarker for TBT Contamination on the Southern Coast of Peninsular Malaysia

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Abstract

Thais gradata samples were collected from six locations along the southern shores of Peninsular Malaysia and analyzed for imposex incidence and organotin (butyltins (BTs), including tributyltin, dibutyltin, and monobutyltin, and phenyltins (PTs), including triphenyltin, diphenyltin, and monophenyltin concentrations), in tissue burden. On average, the BT levels were found to be higher than the levels reported a year before for other biota. In contrast, the PT compounds were found to be lower than in the previous report. The present study also classified the morphological expressions of the imposex scheme for this species into seven stages (stage 0 to stage 6) by observing the development of vas deference sequence (VDS) and penis bulk. This latest imposex scheme clearly indicates the mechanism of VDS growth, the structural changes from penis bulk to a penis with flagellum, and from a normal vaginal opening to a swollen vaginal opening. The degree of imposex was assessed using the vas deference sequence index and the percentage of females possessing the imposex characteristics. It was found that locations possessing high imposex levels also tended to show high BT levels in the snail tissue samples. However, correlation analysis did not show a significant relationship among the two parameters. A better result could be obtained if more samples and sampling locations were added in order to prove the hypothesis. The nonsignificant correlation between the shell height and any of the organotin compounds, along with no significant differences between BT levels in female and lower imposex stage samples, suggests that the BT concentration detected was a recent contamination.

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References

  • Anonymous (2008a). Straits of Malacca. http://en.wikipedia.org/wiki/Strait_of_Malacca. Accessed 13 October 2008.

  • Anonymous (2008b). Johor Strait. http://www.mmc.com.my/content.asp?menuid=100013&rootid=100001&parentid=100010. Accessed 13 October 2008.

  • Barroso, C. M., Reis-Henriques, M. A., Ferriera, M. S., Moreira, M. H., et al. (2002). The effectiveness of some compounds derived from antifouling paints in promoting imposex in Nassarius reticulates. Journal of the Marine Biological Association (United Kingdom), 82, 249–255.

    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. Marine Pollution Bulletin, 44, 887–896.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Blaber, S. M. (1970). The occurrence of a penis-like out-growth behind the right tentacle in spent females of Nucella lapillus (L.). Proceedings of the Malacological Society of London, 39, 231–233.

    Google Scholar 

  • Bryan, G. W., Gibbs, P. E., Hummerstone, L. G., Burt, G. R., et al. (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 (United Kingdom), 66, 615–640.

    Google Scholar 

  • DeFur, P. L., Crane, M., Ingersoll, C., & Tattersfield, L. (Eds.) (1999). Endocrine disruption in invertebrates: Endocrinology, testing, and assessment. In: Proceedings of the Workshop on Endocrine Disruption in Invertebrates. 12–15 December 1998. Pensacola: SETAC Press.

  • EIA (2008). Country Analysis Brief—World Oil Transit Chokepoint. (n.a.). http://www.eia.doe.gov/cabs/World_Oil_Transit_Chokepoints/Full.html. Accessed 8 February 2008.

  • Fioroni, P., Oehlmann, J., Stroben, E., et al. (1991). The pseudohermaphroditism of prosobranchs, morphological aspects. Zoologischer Anzeiger, 226, 1–26.

    Google Scholar 

  • Freeman, D. B. (2003). The straits of Malacca: Gateway or gauntlet? Montreal: McGill-Queen's University Press.

    Google Scholar 

  • Gibbs, P. E., & Bryan, G. W. (1996a). Reproductive failure in the gastropod Nucella lapillus associated with imposex caused by tributyltin pollution: A review. In M. A. Champ & P. F. Seligman (Eds.), Organotin. Environmental fate and effects (pp. 259–280). London: Chapman Hall.

    Google Scholar 

  • Gibbs, P. E., & Bryan, G. W. (1996b). TBT-induced imposex in neogastropod snails: Masculinization to mass extinction. In S. J. de Mora (Ed.), Case study of an environmental contaminant (pp. 212–236). Cambridge: Cambridge University Press.

    Google Scholar 

  • Gibbs, P. E., Bryan, G. W., Pascoe, P. L., Burt, G. R., et al. (1987). The use of dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. Journal of Marine Biology Association of United Kingdom, 67, 507–523.

    Article  CAS  Google Scholar 

  • Harino, H., Iwasaki, N., Arai, T., Ohji, M., Miyazaki, N., et al. (2005). Accumulation of organotin compounds in the deep-sea environment of Nankai trough, Japan. Archive Environmental Contamination Toxicology, 49, 497–503.

    Article  CAS  Google Scholar 

  • Harino, H., Arai, T., Ohji, M., Ismail, A., Miyazaki, N., et al. (2008). Organotin contaminations in Malaysia. Coastal Marine Science, 32(1), 96–101.

    Google Scholar 

  • Horiguchi, T., Shiraishi, H., Morita, M., Shimizu, M., et al. (1994). Imposex and organotin compounds in Thais clavigera and T. bronni in Japan. Journal of Marine Biology Association of United Kingdom, 74, 651–669.

    Article  CAS  Google Scholar 

  • Horiguchi, T., Shiraishi, H., Shimizu, M., Morita, M., et al. (1997). Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera. Environmental Pollution, 95, 85–91.

    Article  CAS  Google Scholar 

  • Houston, R. S. (1971). Reproductive biology of Thais emarginata (Deshayes, 1839) and Thais canaliculata (Duclos, 1832). Veliger, 13, 348–357.

    Google Scholar 

  • Huet, M., Fioroni, P., Oehlmann, J., Stroben, E., et al. (1995). Comparison of imposex response in three prosobranch species. Hydrobiologia, 309, 29–35.

    Article  Google Scholar 

  • Ismail, A., Ferdaus, M. Y., Syaizwan, Z. Z., et al. (2004). Imposex in Thais sp. along the Straits of Malacca. In C. Nitithamyong (Ed.), Proceedings of the first joint seminar on coastal oceanography (pp. 189–196). Bangkok: Chulalongkorn University.

    Google Scholar 

  • McClanahan, T. R., & Muthiga, N. A. (1992). Comparative sampling methods for subtidal epibenthic gastropods. Journal of Experimental Marine Biology and Ecology, 164, 87–101.

    Article  Google Scholar 

  • Nias, D. J., McKillup, S. C., Edyvane, K. S., et al. (1993). Imposex in Lepsiella vinosa from Southern Australia. Marine Pollution Bulletin, 26, 380–384.

    Article  CAS  Google Scholar 

  • Oehlmann, J., Stroben, E., Fioroni, P., et al. (1991). The morphological expression of imposex in Nucella lapillus (Linnaeus) (Gastropoda: Muricidae). Journal of Molluscan Studies, 57, 375–390.

    Article  Google Scholar 

  • Poli, G., Salvat, B., Strieff, W., et al. (1971). Aspect particulier de la sexualité chez Ocenebra erinacea. Haliotis, 1, 29–30.

    Google Scholar 

  • Pope, N. D. (1998). The bioavailability of sediment-bound tributyltin (TBT). PhD thesis, University of Plymouth, United Kingdom.

  • Power, A. J., & Keegan, B. F. (2001). The significance of imposex levels and TBT contamination in the red whelk, Neptunea antique (L.), from the offshore Irish Sea. Marine Pollution Bulletin, 42, 761–772.

    Article  CAS  Google Scholar 

  • Ruppert, E. E., Fox, R. S., Barnes, R. B., et al. (2004). Invertebrate anatomy Online: Bellamy japonica Japanese mystery snail. http://webs.lander.edu/rsfox/invertebrates/. Accessed 10 July 2007.

  • Shi, H. H., & Huang, C. J. (2001). Morphological characters of imposex in marine gastropod. Journal of Oceanography Taiwan Strait, 20, 552–555.

    Google Scholar 

  • Shi, H. H., Huang, C. J., Yu, X., Zhu, S., et al. (2004). An updated scheme of imposex for Cantharus cecillei (Gastropoda: Buccinidae) and a new mechanism leading to the sterilization of imposex-affected females. Marine Biology, 146, 717–723.

    Article  Google Scholar 

  • Smith, B. S. (1971). Sexuality in the American mud snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London, 39, 377–378.

    Google Scholar 

  • Smith, B. S. (1981). Tributyltin compounds induced male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsoletus. Journal of Applied Toxicology, 1, 141–144.

    Article  CAS  Google Scholar 

  • Smith, B. S. (1996). Selective decline in imposex levels in the dog-whelk Lepsiella scobina following a ban on the use of TBT antifoulants in New Zealand. Marine Pollution Bulletin, 32, 362–365.

    Article  CAS  Google Scholar 

  • Stewart, C., de Mora, S. J., Jones, M. R. L., Miller, M. C., et al. (1992). Imposex in New Zealand neogastropods. Marine Pollution Bulletin, 24, 204–209.

    Article  CAS  Google Scholar 

  • Strand, J., & Jacobsen, J. A. (2002). Imposex in two sublittoral neogastropods from the Kattegat and Skagerrak: The common whelk Buccinum undatum and the red whelk Neptunea antiqua. Marine Ecology Progress Series, 244, 171–177.

    Article  Google Scholar 

  • Stroben, E., Oehlmann, J., Fioroni, P., et al. (1992). The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): A potential indicator of tributyltin pollution. Marine Biology, 113, 625–636.

    Article  Google Scholar 

  • Stroben, E., Oehlmann, U. S., Fioroni, P., Oehlmann, J., et al. (1995). A comparative method for easy assessment of coastal TBT pollution by the degree of imposex in prosobranchs species. Haliotis, 24, 1–12.

    Google Scholar 

  • Sudaryanto, A., Takahashi, S., Monirith, I., Ismail, A., Muchtar, M., Zheng, J., et al. (2002). Asia Pacific mussel watch: Monitoring of butyltin contamination in coastal waters of Asian developing countries. Environmental Toxicology and Chemistry, 21, 2119–2130.

    Article  CAS  Google Scholar 

  • Sudaryanto, A., Takahashi, S., Iwata, H., Tanabe, S., Ismail, A., et al. (2004). Contamination of butyltin compounds in Malaysian marine environments. Environmental Pollution, 130, 342–358.

    Article  Google Scholar 

  • Swennen, N., Ruttanadakul, S., Ardseungnern, H. R., Singh, B., Mensink, P., Hallers-Tjabbes, C. C., et al. (1997). Imposex in sublittoral and littoral gastropods from the gulf of Thailand and Straits of Malacca in relation to shipping. Environmental Technology, 18, 1245–1254.

    Article  CAS  Google Scholar 

  • Tan, K. S. (1997). Imposex in three species of Thais from Singapore, with additional observations on T. clavigera (Kuster) from Japan. Marine Pollution Bulletin, 34, 577–581.

    Article  CAS  Google Scholar 

  • Tan, K. S. (1999). Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the Straits of Johor: A case study using penis length, area and weight as measures of imposex severity. Marine Pollution Bulletin, 39, 295–303.

    Article  CAS  Google Scholar 

  • Tan, K. S., & Sigurdsson, J. B. (1990). A new species of Thais (Gastropoda: Muricidae) from Singapore and Peninsular Malaysia. Raffles Bulletin of Zoology, 38, 205–212.

    Google Scholar 

  • Tan, K. S., & Sigurdsson, J. B. (1996a). Two new species of Thais (Mollusca: Neogastropoda: Muricidae) from peninsular Malaysia and Singapore, with notes on T. tissoti (Petit, 1852) and T. blanfordi (Melvill, 1893) from Bombay, India. Raffles Bulletin of Zoology, 44, 77–107.

    Google Scholar 

  • Tan, K. S., & Sigurdsson, J. B. (1996b). New species of Thais (Neogastropoda, Muricidae) from Singapore, with a re-description of Thais javanica (Philippi, 1848). Journal of Molluscan Studies, 62, 517–535.

    Article  Google Scholar 

  • Ten Hallers-Tjabbes, C. C., John, F. K., Boon, J. P., et al. (1994). Imposex in whelks (Buccinum undatum) from the open North Sea: Relation to shipping traffic intensities. Marine Pollution Bulletin, 28(5), 311–313.

    Article  Google Scholar 

  • Ten Hallers-Tjabbes, C. C., Wegener, J. W., Van Hattum, B., Kemp, J. F., Ten Hallers, E., Reitsema, T. J., et al. (2003). Imposex and organotin concentrations in Buccinum undatum and Neptunea antiqua from the North Sea: Relationship to shipping density and hydrographical conditions. Marine Environmental Research, 55, 203–233.

    Article  Google Scholar 

  • Tong, S. L., Pang, F. Y., Phang, S. M., Lai, H. C., et al. (1996). Tributyltin distribution in the coastal environment of Peninsular Malaysia. Environmental Pollution, 91, 209–216.

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank Buhari, Faradiella, Shahrizad, Zulfa Hanan, and Zairi for their assistance with the field sampling. We are grateful to Professor Tsuguo Otake and Mrs. Masako Hara for their considerable assistance during the SEM procedure. This work was supported in part by Grants-in-Aid no. 18780141 and 20688008 from the Ministry of Education, Culture, Sports, Science, and Technology of Japan and was cofinanced by eScienceFund grant no. 06-01-04-SF0715 from the Ministry of Science, Technology, and Innovation (MOSTI), Malaysia.

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Mohamat-Yusuff, F., Zulkifli, S.Z., Ismail, A. et al. Imposex in Thais gradata as a Biomarker for TBT Contamination on the Southern Coast of Peninsular Malaysia. Water Air Soil Pollut 211, 443–457 (2010). https://doi.org/10.1007/s11270-009-0314-3

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