, Volume 714, Issue 1, pp 13–24 | Cite as

Imposex and butyltin burden in Bolinus brandaris (Mollusca, Gastropoda) and sediment from the Tunisian coast

  • Sami Abidli
  • Youssef Lahbib
  • Pablo Rodríguez González
  • José Ignacio García Alonso
  • Najoua Trigui El Menif
Primary Research Paper


The present study aimed at analyzing the imposex incidence and the presence of butyltins namely tributyltin (TBT) with its di- and mono-substituted metabolites in Bolinus brandaris whole tissues and in surface sediments at seven sites from the Tunisian coast during one campaign in May 2010. Butyltin levels were evaluated using isotope dilution GC–MS. Except the population collected from Zarat site, imposex was found in snails from the remained six sites with a maximal incidence and sterility (closure of the vaginal opening) registered in Carrier bay. Both imposex indices VDSI and RPLI showed a positive correlation with tissue concentrations of TBT. Total butyltin concentrations in sediments were higher in sites located in the vicinity of shipping areas with levels of TBT high enough to cause environmental concern if there is no legislative restriction and enforcement for the sale and use of these chemicals in Tunisia. These results further confirmed that B. brandaris is a good bioindicator of butyltin pollution in the studied areas. In addition, this study provided recent and new data on sediment butyltin concentrations that could serve for long-term monitoring of TBT pollution in Tunisia and the Mediterranean Sea.


Organotins Bolinus brandaris Imposex Bioindicators Sediments Tunisia 



The present study was partially funded by a scholarship attributed to Sami Abidli by the Ministry of High Education and Scientific Research in Tunisia. This work is a result of collaboration between Faculty of sciences of Bizerta (Tunisia) and Faculty of Chemistry (Oviedo, Spain). Authors are grateful to the staff of the Department of Physical and Analytical Chemistry (Oviedo) for their help in butyltins analysis and to the staff of the laboratory of Molecular Genetic, Immunology and Biotechnology (Faculty of Sciences of Tunis) for the lyophilization of biological samples. Finally, we acknowledge the Editor and two anonymous referees for valuable comments and suggestions that greatly improved the manuscript.


  1. Abidli, S., Y. Lahbib & N. Trigui El Menif, 2009a. Effects of TBT on the imposex development, reproduction and mortality in Hexaplex trunculus (Gastropoda: Muricidae). Journal of the Marine Biological Association of the United Kingdom 89: 139–146.CrossRefGoogle Scholar
  2. Abidli, S., Y. Lahbib & N. Trigui El Menif, 2009b. Imposex and genital tract malformations in Hexaplex trunculus and Bolinus brandaris collected in the gulf of Tunis. Bulletin of Marine Science 85: 11–25.Google Scholar
  3. Abidli, S., Y. Lahbib & N. Trigui El Menif, 2011. Imposex and butyltin concentrations in Bolinus brandaris (Gastropoda: Muricidae) from the northern Tunisian coast. Environmental Monitoring and Assessment 177: 375–384.PubMedCrossRefGoogle Scholar
  4. Abidli, S., Y. Lahbib & N. Trigui El Menif, 2012a. Relative growth and reproductive cycle in two populations of Bolinus brandaris (Gastropoda: Muricidae) from northern Tunisia (Bizerta Lagoon and small Gulf of Tunis). Biologia 67: 751–761.CrossRefGoogle Scholar
  5. Abidli, S., M. M. Santos, Y. Lahbib, L. F. C. Castro, M. A. Reis-Henriques & N. Trigui El Menif, 2012b. Tributyltin (TBT) effects on Hexaplex trunculus and Bolinus brandaris (Gastropoda: Muricidae): imposex induction and sex hormone levels insights. Ecological Indicators 13: 13–21.CrossRefGoogle Scholar
  6. Added, A., A. Ben Mammou, S. Abdeljaoued, N. Essonni & F. Fernex, 2003. Caractérisation géochimique des sédiments de surface du golfe de Tunis. Bulletin de l’Institut National des Sciences et Technologies de la Mer de Salammbô 30: 135–142.Google Scholar
  7. Axiak, V., A. J. Vella, D. Micaleff & P. Chircop, 1995. Imposex in Hexaplex trunculus (Gastropoda: Muricidae): first results from biomonitoring of tributyltin contamination in The Mediterranean. Marine Biology 121: 685–691.CrossRefGoogle Scholar
  8. Axiak, V., D. Micallef, J. Muscat, A. Vella & B. Mintoff, 2003. Imposex as a biomonitoring tool for marine pollution by tributyltin: some further observations. Environment International 28: 743–749.PubMedCrossRefGoogle Scholar
  9. Barreiro, R., R. Gonzáles, M. Quintela & J. M. Ruiz, 2001. Imposex, organotin bioaccumulation and sterility of female Nassarius reticulatus in polluted areas of NW Spain. Marine Ecology Progress Series 218: 203–212.CrossRefGoogle Scholar
  10. Blaber, S. J. M., 1970. The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus. Journal of Molluscan Studies 39: 231–233.Google Scholar
  11. Bryan, G. W., P. E. Gibbs, G. R. Burt & L. G. Hummerstone, 1987. The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. Journal of the Marine Biological Association of the United Kingdom 67: 525–544.CrossRefGoogle Scholar
  12. Bryan, G. W., G. R. Burt, P. E. Gibbs & P. L. Pascoe, 1993. Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution before and after TBT restrictions. Journal of the Marine Biological Association of the United Kingdom 73: 913–929.CrossRefGoogle Scholar
  13. Burton, E. D., I. R. Philips & D. W. Hawker, 2004. Sorption and desorption behaviour of tributyltin with natural sediments. Environmental Science and Technology 38: 6694–6700.PubMedCrossRefGoogle Scholar
  14. Castro, I. B. & G. Fillmann, 2012. High TBT and imposex levels in a commercial muricid (Stramonita chocolata) from two Peruvian harbors. Environmental Toxicology and Chemistry 31: 955–960.PubMedCrossRefGoogle Scholar
  15. Castro, I. B., M. Rossato & G. Fillmann, 2012a. Imposex reduction and reminiscent butyltin contamination in Southern Brazilian harbors. Environmental Toxicology and Chemistry 31: 947–954.PubMedCrossRefGoogle Scholar
  16. Castro, I. B., M. F. Arroyo, P. G. Costa & G. Fillmann, 2012b. Butyltin compounds and imposex levels in Ecuador. Archives of Environmental Contamination and Toxicology 62: 68–77.PubMedCrossRefGoogle Scholar
  17. Chiavarini, S. P., P. Massanisso, P. Nicolai, C. Nobili & R. Morabito, 2003. Butyltins concentration levels and imposex occurrence in snails from the Sicilian coasts. Chemosphere 50: 311–319.PubMedCrossRefGoogle Scholar
  18. Couceiro, L., J. Díaz, N. Albaina, R. Barreiro, J. A. Irabien & J. M. Ruiz, 2009. Imposex and gender independent butyltin accumulation in the gastropod Nassarius reticulatus from the Cantabrian coast (N Atlantic Spain). Chemosphere 76: 424–427.PubMedCrossRefGoogle Scholar
  19. Díez, S., M. Abalos & J. M. Bayona, 2002. Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation. Water Research 36: 905–918.PubMedCrossRefGoogle Scholar
  20. Díez, S., E. Jover, J. Albaigés & J. M. Bayona, 2006. Occurrence and degradation of butyltins and wastewater marker compounds in sediments from Barcelona harbor, Spain. Environment International 32: 858–865.PubMedCrossRefGoogle Scholar
  21. El Hamdani, A., J. M. Ferrer & A. M. García Carrascosa, 1998. Imposex in prosobranch molluscs: an indicator of TBT pollution in the Valencian coast (Spain, Western Mediterranean). Cuadernos de Investigacıón Biologica 20: 275–278.Google Scholar
  22. Essid, N., 2008. Caractérisation de la pollution organique et minérale des sédiments de la lagune de Bizerte et impact écologique sur les peuplements des nématodes libres: Etude à grande échelle et au niveau d’un parc mytilicole. Thèse de doctorat en Sciences Biologiques, Faculté des Sciences de Bizerte 303 p.Google Scholar
  23. Fent, K., 1996. Ecotoxicology of organotin compounds. Critical Reviews in Toxicology 26: 1–117.PubMedCrossRefGoogle Scholar
  24. Fioroni, P., J. Oehlmann & E. Stroben, 1991. The pseudohermaphroditism of prosobranchs: morphological aspects. Zoologische Anzeiger 226: 1–26.Google Scholar
  25. Gibbs, P. E. & G. W. Bryan, 1986. Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex undiced by tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 66: 767–777.CrossRefGoogle Scholar
  26. Gibbs, P. E., G. W. Bryan, P. L. Pascoe & G. R. Burton, 1987. The use of the dog-whelk, Nucella lapillus, as an indicator of tri-n-butyltin (TBT) contamination. Journal of the Marine Biological Association of the United Kingdom 67: 507–523.CrossRefGoogle Scholar
  27. Gooding, M. P. & G. A. LeBlanc, 2001. Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta. General and Comparative Endocrinology 122: 172–180.PubMedCrossRefGoogle Scholar
  28. Hoch, M., 2001. Organotin compounds in the environmental an overview. Applied Geochemistry 16: 719–743.CrossRefGoogle Scholar
  29. Jenner, M. G., 1979. Pseudohermaphroditism in Ilyanassa obsoleta (Mollusca: Neogastropoda). Science 205: 1407–1409.PubMedCrossRefGoogle Scholar
  30. Kim, N. S., W. J. Shim, U. H. Yim, S. Y. Ha, J. G. An & K. H. Shin, 2011. Three decades of TBT contamination in sediments around a large scale shipyard. Journal of Hazardous Materials 192: 634–642.PubMedCrossRefGoogle Scholar
  31. Kimbrough, R. D., 1976. Toxicity and health effects of selected organotin compounds: a review. Environmental Health Perspectives 14: 51–56.PubMedCrossRefGoogle Scholar
  32. Lahbib, Y., S. Abidli, M. Le Pennec, R. Flawoer & N. Trigui El Menif, 2007. Morphological expression and different stages of imposex in Hexaplex trunculus (Neogastropoda: Muricidae) from Tunisian coasts. Cahiers de Biologie Marine 48: 315–326.Google Scholar
  33. Lahbib, Y., S. Abidli & N. Trigui El Menif, 2008a. Imposex level and penis malformation in Hexaplex trunculus from the Tunisian coast. American Malacological Bulletin 24: 79–89.CrossRefGoogle Scholar
  34. Lahbib, Y., M. Boumaiza & N. Trigui El Menif, 2008b. Imposex expression in Hexaplex trunculus from the North Tunis Lake transplanted to Bizerta channel (Tunisia). Ecological Indicators 8: 239–245.CrossRefGoogle Scholar
  35. Lahbib, Y., S. Abidli, J. F. Chiffoleau, B. Averty & N. Trigui El Menif, 2009. First record of butyltin body burden and imposex status in Hexaplex trunculus (L.) along the Tunisian coast. Journal of Environmental Monitoring 11: 1253–1258.PubMedCrossRefGoogle Scholar
  36. Lahbib, Y., S. Abidli, J. F. Chiffoleau, B. Averty & N. Trigui El Menif, 2010. Imposex and butyltin concentrations in snails from the lagoon of Bizerta (Northern Tunisia). Marine Biology Research 6: 600–607.CrossRefGoogle Scholar
  37. Lahbib, Y., S. Abidli, P. Rodríguez González, J. Ignacio García Alonso & N. Trigui El Menif, 2011a. Monitoring of organotin pollution in bizerta channel (Northern Tunisia): temporal Trend from 2002 to 2010. Bulletin of Environmental Contamination and Toxicology 86: 531–534.PubMedCrossRefGoogle Scholar
  38. Lahbib, Y., S. Abidli, P. Rodríguez González, J. Ignacio García Alonso & N. Trigui El Menif, 2011b. Potential of Nassarius nitidus for monitoring organotin pollution in the lagoon of Bizerta (northern Tunisia). Journal of Environmental Sciences 23: 1551–1557.CrossRefGoogle Scholar
  39. Lee, R. F., A. O. Valkirs & P. F. Seligman, 1989. Importance of microalgae in the biodegradation of tributyltin in estuarine waters. Environmental Science and Technology 23: 1515–1518.CrossRefGoogle Scholar
  40. Lemghich, I. & M. H. Benajiba, 2007. Survey of imposex in prosobranchs mollusks along the northern Mediterranean coast of Morocco. Ecological Indicators 7: 209–214.CrossRefGoogle Scholar
  41. Maguire, R. J. & R. J. Katz, 1985. Degradation of the tri-n-butyltin species in water and sediment from Toronto Harbor. Journal of Agriculture and Food Chemistry 33: 947–953.CrossRefGoogle Scholar
  42. Martoja, M. & J. M. Bouquegneau, 1988. Murex trunculus: un nouveau cas de pseudo-hermaphrodisme chez un gastéropode prosobranche. Bulletin de la Société Royale des Sciences de Liège 57: 45–58.Google Scholar
  43. Mzoughi, N., G. Lespes, M. Bravo, M. Dachraoui & M. Potin-Gautier, 2005. Organotin speciation in Bizerte lagoon (Tunisia). Science of the Total Environment 349: 211–222.PubMedCrossRefGoogle Scholar
  44. Oehlmann, J., 1994. Imposex bei Muriciden (Gastropoda, Prosobranchia), eine ökotoxikologische Untersuchung zu TBT-Effekten. Cuvillier, Göttingen.Google Scholar
  45. Ouertani, N., R. Hamouda & H. Belayouni, 2006. Study of the organic matter buried in recent sediments of an increasing anoxic environment surrounded by an urban area : the « Lac sud de Tunis». Geo-Eco-Trop 30: 21–34.Google Scholar
  46. Peña, J., M. Uerra, M. J. Gaudencio & M. Kendall, 1988. The occurrence of imposex in the Gastropod Nucella lapillus at sites in Spain and Portugal. Lurralde 11: 445–451.Google Scholar
  47. Pinochet, H., C. Tessini, M. Bravo, W. Quiroz & I. De Gregori, 2009. Butyltin compounds and their relation with organic matter in marine sediments from San Vicente Bay, Chile. Environmental Monitoring and Assessment 155: 341–353.PubMedCrossRefGoogle Scholar
  48. Poppe, G. T. & Y. Goto, 1991. European Seashells, Vol. 1 (Polyplacophora, Caudofoveata, Solenogastra, Gastropoda). Verlag Christa Hemmen, Wiesbaden: 352 pp.Google Scholar
  49. Ramón, M. & M. J. Amor, 2001. Increasing imposex in populations of Bolinus brandaris (Gastropoda: Muricidae) in the north-western Mediterranean. Marine Environmental Research 52: 463–475.PubMedCrossRefGoogle Scholar
  50. Rodríguez-González, P., J. Ignacio García Alonso & A. Sanz-Medel, 2004. Development of a triple spike methodology for validation of butyltin compounds speciation analysis by isotope dilution mass spectrometry Part 2. Study of different extraction procedures for the determination of butyltin compounds in mussel tissue CRM 477. Journal of Analytical Atomic Spectrometry 19: 767–772.CrossRefGoogle Scholar
  51. Rodríguez-González, P., J. Ignacio García Alonso & A. Sanz-Medel, 2005. Single and multiple spike procedures for the determination of butyltin compounds in sediments using isotope dilution GC-ICP-MS. Journal of Analytical Atomic Spectrometry 20: 1076–71084.CrossRefGoogle Scholar
  52. Rodríguez, J. G., O. Solaun, J. Larreta, M. J. B. Segarra, J. Franco, J. I. G. Alonso, C. Sariego, V. Valencia & A. Borja, 2010. Baseline of butyltin pollution in coastal sediments within the Basque Country (northern Spain), in 2007–2008. Marine Pollution Bulletin 60: 139–151.PubMedCrossRefGoogle Scholar
  53. Santos, M. M., M. A. Reis-Henriques, M. N. Vieira & M. Solé, 2006. Triphenyltin and tributyltin, single and in combination, promote imposex in the gastropod Bolinus brandaris. Ecotoxicological and Environmental Safety 64: 155–162.CrossRefGoogle Scholar
  54. Shi, H. H., C. J. Huang, S. X. Zhu, X. J. Yu & W. Y. Xie, 2005. Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Marine Ecology Progress Series 304: 179–189.CrossRefGoogle Scholar
  55. Shim, W. J., J. R. Oh, S. H. Kahng, J. H. Shim & S. H. Lee, 1999. Horizontal distribution of butyltins in surface sediments from an enclosed bay system, Korea. Environmental Pollution 106: 351–357.PubMedCrossRefGoogle Scholar
  56. 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
  57. Smith, P. J., 1996. Selective decline in imposex levels in the dogwhelk Lepsiella scobina following a ban on the use of TBT antifoulants in New Zealand. Marine Pollution Bulletin 32: 362–365.CrossRefGoogle Scholar
  58. Solé, M., Y. Morcillo & C. Porte, 1998. Imposex in the commercial snail Bolinus brandaris in the northwestern Mediterranean. Environmental Pollution 99: 241–246.PubMedCrossRefGoogle Scholar
  59. Stang, P. M. & P. F. Seligman, 1986. Distribution and fate of butyltin compounds in the sediment of San Diego Bay. Proceedings of the Oceans ‘86 Organotin Symposium 4: 1256–1261.Google Scholar
  60. Sternberg, R. M., M. P. Gooding, A. K. Hotchkiss & G. A. LeBlanc, 2010. Environmental endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19: 4–23.PubMedCrossRefGoogle Scholar
  61. Stewart, C., S. J. Mora, M. R. Jones & M. C. Miller, 1992. Imposex in New Zealand neogastropods. Marine Pollution Bulletin 24: 204–209.CrossRefGoogle Scholar
  62. Stroben, E., J. Oehlmann & P. Fioroni, 1992. The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Marine Biology 113: 625–636.CrossRefGoogle Scholar
  63. Terlizzi, A., S. Geraci & P. E. Gibbs, 1999. Tributyltin (TBT)-induced imposex in the Neogastropod Hexaplex trunculus in Italian coastal waters: morphological aspects and ecological implications. Italian Journal of Zoology 66: 141–146.CrossRefGoogle Scholar
  64. Terlizzi, A., S. Geraci & V. Minganti, 1998. Tributyltin (TBT) pollution in the coastal waters of Italy as indicated by imposex in Hexaplex trunculus (Gastropoda: Muricidae). Marine Pollution Bulletin 36: 749–752.CrossRefGoogle Scholar
  65. Terlizzi, A., S. Fraschetti, P. Gianguzza, M. Faimali & F. Boero, 2001. Environmental impact of antifouling technologies: state of art and perspectives. Aquatic Conservation: Marine and Freshwater Ecosystems 11: 311–317.CrossRefGoogle Scholar
  66. Titley-O’Neal, C. P., K. R. Munkittrick & B. A. Macdonald, 2011. The effects of organotin on female gastropods. Journal of Environmental Monitoring 13: 2360–2388.PubMedCrossRefGoogle Scholar
  67. Trigui El Menif, N., Y. Lahbib, M. Le Pennec, R. Flower & M. Boumaiza, 2006. Intensity of the imposex phenomenon—impact on growth and fecundity in Hexaplex trunculus (Mollusca: Gastropoda) collected in Bizerta lagoon and channel (Tunisia). Cahiers de Biologie Marine 47: 165–175.Google Scholar
  68. Vasconcelos, P., S. Carvalho, M. Castro & M. B. Gaspar, 2008. The artisanal fishery for muricid gastropods (banded murex and purple dye murex) in the Ria Formosa lagoon (Algarve coast, southern Portugal). Scientia Marina 72: 287–298.CrossRefGoogle Scholar
  69. Vasconcelos, P., M. B. Gaspar & C. M. Barroso, 2010a. Imposex in Bolinus brandaris from the Ria formosa lagoon (southern Portugal): usefulness of “single-site baselines” for environmental monitoring. Journal of Environmental Monitoring 12: 1823–1832.PubMedCrossRefGoogle Scholar
  70. Vasconcelos, P., P. Moura, M. Castro & M. B. Gaspar, 2010b. Size matters: importance of penis length variation on reproduction studies and imposex monitoring in Bolinus brandaris (Gastropoda: Muricidae). Hydrobiologia 661: 364–375.Google Scholar
  71. Wafo, E., L. Sarrazin, J. L. Monod & P. Rebouillon, 2004. Speciation analysis of butyltin compounds in sediments of the Theoule harbour (France) by GC/AES. Toxicological and Environmental Chemistry 86: 117–126.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sami Abidli
    • 1
  • Youssef Lahbib
    • 1
  • Pablo Rodríguez González
    • 2
  • José Ignacio García Alonso
    • 2
  • Najoua Trigui El Menif
    • 1
  1. 1.Laboratory of Environment Biomonitoring, Faculty of Sciences of Bizerta (FSB)University of CarthageZarzouna, BizertaTunisia
  2. 2.Department of Physical and Analytical Chemistry, Faculty of ChemistryUniversity of OviedoOviedoSpain

Personalised recommendations