First Record of Imposex in Euthria cornea (Neogastropoda: Buccinidae) Collected from the Complex Lagoon-Channel of Bizerta

  • Tahani El AyariEmail author
  • Najoua Trigui El Menif


Imposex has been widely used as an indicator of tributyltin (TBT) pollution, despite this, imposex was still not described in some gastropod species. This study reports, for the first time, the occurrence of imposex in Euthria cornea (Linnaeus, 1758) collected from the complex lagoon-channel of Bizerta. Imposex expression in Euthria cornea followed the a-pathway corresponding to the development of a bud penis before the vas deferens. Four stages (VDS1a, VDS2a, VDS3a and VDS4) were recognised in this gastropod. Imposex incidence (I%) was slightly higher in Bizerta Channel (100%) against (92.85%) in Bizerta lagoon without being significant. However, the degree of imposex (RPLI) was significantly higher in Bizerta lagoon 10.92 compared to Bizerta Channel 7.05. Similar was noted for the Vas deferens sequence index (VDSI) 2.76 in Bizerta lagoon and 2.02 in Bizerta Channel. While, female and male penis length (FPL and MPL) were higher in Bizerta Channel, 0.87 mm and 12.34 mm against 0.73 mm and 7.23 mm in Bizerta lagoon, respectively. Sterility was not observed in any Euthria cornea.


Imposex Euthria cornea Indicator Complex lagoon-channel of Bizerta 


Compliance with Ethical Standards

Conflict of Interest

We have no conflict of interest to declare.


  1. Abidli S, Lahbib Y, El Menif NT (2009) Imposex and genital tract malformations in Hexaplex trunculus and Bolinus brandaris collected in the Gulf of Tunis. Bull Mar Sci 85:11–25Google Scholar
  2. Abidli S, Lahbib Y, El Menif NT (2010) Imposex and butyltin concentrations in Bolinus brandaris (Gastropoda: Muricidae) from the northern Tunisian coast. Environ Monit Assess 177:375–384CrossRefGoogle Scholar
  3. Afsar N, Siddiqui G, Ayub Z (2015) Bioindicator Thais carinifera (mollusca, gastropoda): imposex response and consequences along the Pakistan coast during the period from 1993 to 2012. Braz J Oceanogr 63:115–124CrossRefGoogle Scholar
  4. Alzieu C (1991) Environmental problems caused by TBT in France: assessment, regulations, prospects. Mar Environ Res 32(1–4):7–17CrossRefGoogle Scholar
  5. Batista RM, Castro IB, Fillmann G (2016) Imposex and butyltin contamination still evident in Chile after TBT global ban. Sci Total Environ 566–567(Supplement C):446–453. CrossRefGoogle Scholar
  6. Batista-Andrade JA, Caldas SS, Batista RM, Castro IB, Fillmann G, Primel EG (2018) From TBT to booster biocides: levels and impacts of antifouling along coastal areas of Panama. Environ Pollut 234:243–252. CrossRefGoogle Scholar
  7. Blaber S (1970) The occurence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.). Proc Malacol Soc London 39:231–232Google Scholar
  8. Boudouresque CF, Harmelin JG & de Grissac, Jeudy A, (1986) Le Benthos marin de l'île de Zembra (parc national de Tunisie). Gis Posionies (ed) Rapport UNEP-IUCN-RAC/SPA, p 199Google Scholar
  9. Camillo E, Quadros J, Castro Í, Fernandez M (2004) Imposex in Thais rustica (Mollusca: Neogastropoda)(Lamark, 1822) as an indicator of organotin compounds pollution at Maceio coast (Northeastern Brazil). Braz J Oceanogr 52(2):101–105CrossRefGoogle Scholar
  10. da Costa MB, Zamprogno GC, Otegui MBP, de Morais L, Pedruzzi FC, Dalbem GB, da Silva DA, Resende ACB (2017) A temporal and spatial monitoring of organotin pollution in a harborside region of Brazil by imposex and ecological quality ratio using Leucozonia nassa. Environ Monit Assess 189:650CrossRefGoogle Scholar
  11. de Azevedo D, de Almeida Rocha-Barreira C, Matthews-Cascon H, Castro ÍB (2012) Pugilina morio L., a new Imposex exhibitor from south American estuarine environments: approach for a non-lethal method to evaluate Imposex. Bull Environ Contam Toxicol 89:786–792CrossRefGoogle Scholar
  12. Domínguez-Ojeda D, Patrón-Soberano O, Nieto-Navarro J, de Lourdes Robledo-Marenco M, Velázquez-Fernández J (2015) Imposex in Plicopurpura pansa (Neogastropoda: Thaididae) in Nayarit and Sinaloa, Mexico. Revista Mexicana de Biodiversidad 86(2):531–534CrossRefGoogle Scholar
  13. El Ayari T, Abidli S, Lahbib Y, Rodríguez González P, García Alonso J, Trigui-El Menif N (2015) The effect of size and epibiotic barnacles on imposex in Stramonita haemastoma collected from the northern coast of Tunisia. Mar Biol Res 11:313–320CrossRefGoogle Scholar
  14. El Ayari T, Bierne N, Trigui-El Menif N (2018) Imposex incidence in Stramonita haemastoma (Gastropoda: Muricidae) from the Mediterranean and Atlantic coast after tributyltin global ban. J Sea Res 134:10–15CrossRefGoogle Scholar
  15. Erdeleza A, Furdek Turkb M, Štambukc A, Župand I, Pehardaa M (2017) Ecological quality status of the Adriatic coastal waters evaluated by the organotin pollution biomonitoring. Mar Pollut Bull 123:313–323CrossRefGoogle Scholar
  16. Fujinaga K, Ilano A, Hayakari C, Oyama Y, Matsuishi T, Nakao S (2006a) The present state of imposex in several edible whelks in three coasts along Hokkaido. Japan 水産増殖 54(2):179–185Google Scholar
  17. Fujinaga K, Ilano AS, Nomura H, Miranda RT, Nakao S (2006b) Present state of imposex in neptune whelk Neptunea arthritica inhabiting shallow waters around Hokkaido, Japan. Fish Sci 72(5):995–1003. CrossRefGoogle Scholar
  18. Gibbs P, Bryan G (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J Mar Biol Assoc U K 66(4):767–777CrossRefGoogle Scholar
  19. Gibbs PE, Bryan GW (1996) Reproductive failure in the gastropod Nucella Lapillus associated with Imposex caused by tributyltin pollution: a review. In: Champ MA, Seligman PF (eds) Organotin. Springer, DordrechtGoogle Scholar
  20. Gibbs PE, Pascoe PL, Burt GR. (1988) Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. Journal of the Marine Biological Association of the UK 68:715-31Google Scholar
  21. Gibbs PE, Bryan G, Pascoe P, Burt G (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc U K 67(03):507–523CrossRefGoogle Scholar
  22. Gibbs P, Bryan G, Pascoe P, Burt G (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributyltin-induced imposex. J Mar Biol Assoc U K 70(03):639–656CrossRefGoogle Scholar
  23. Gibbs PE, Bryan GW, Pascoe PL (1991) TBT-induced imposex in the dogwhelk, Nucella lapillus: geographic uniformity of the response and effects. Mar Environ Res 32:79-87Google Scholar
  24. Gofas S, Le Renard J, Bouchet Mollusca P (2001) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collections Patrimoines Naturels 50:234–235Google Scholar
  25. Guabloche A, Alvarez J, Rivas R, Hurtado S, Pradel R, Iannacone J (2013) Imposex in the marine snail Xanthochorus Buxea (Broderip, 1833) (Muricidae) from the South American Pacific. Biologist 11(2):237–249Google Scholar
  26. 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(1):85–91. CrossRefGoogle Scholar
  27. Horiguchi, T., H.-S. Cho, H. Shiraishi, M. Kojima, M. Kaya, M. Morita & M. Shimizu, 2001. Contamination by organotin (tributyltin and triphenyltin) compounds from antifouling paints and endocrine disruption in marine gastropods. Riken Review:9–11.Google Scholar
  28. Ide I, Witten E, Fischer J, Kalbfus W, Zellner A, Stroben E, Watermann B (1997) Accumulation of organotin compounds in the common whelk Buccinum undatum and the red whelk Neptunea antiqua in association with imposex. Mar Ecol Prog Ser 152:197–203CrossRefGoogle Scholar
  29. Koukouras A (2010) Check-list of marine species from Greece. Aristotle University of Thessaloniki Assembled in the framework of the EU FP7 PESI projectGoogle Scholar
  30. Lahbib Y, Abidli S, El Menif NT (2008) Imposex level and penis malformation in Hexaplex trunculus from the Tunisian coast. Am Malacol Bull 24:79–89CrossRefGoogle Scholar
  31. Lahbib Y, Abidli S, El Menif NT (2012) TBT pollution in Tunisian coastal lagoons as indicated by imposex in Hexaplex trunculus (Gastropoda: Muricidae). Trans Water Bull 6:17–24Google Scholar
  32. Lahbib Y, El Menif T, Le Penec M, Boumaiza M (2004) Données sur le cycle reproducteur du mollusque gastéropode Hexaplex trunculus (Linné, 1758) de la lagune de Bizerte (Tunisie). Bull Soc Zool Fr 129:407–418Google Scholar
  33. Lahbib Y, Abidli S, Le Pennec M, Flawoer R, El Menif NT (2007) Morphological expression and different stages of imposex in Hexaplex trunculus (Neogastropoda: Muricidae) from Tunisian coasts. Cah Biol Mar 48(4):315–326Google Scholar
  34. Lahbib Y, Abidli S, Chiffoleau J, Averty B, El Menif NT (2010) Imposex and butyltin concentrations in snails from the lagoon of Bizerta (Northern Tunisia). Mar Biol Res 6(6):600–607CrossRefGoogle Scholar
  35. Lahbib Y, Abidli S, González PR, Alonso JIG, El Menif NT (2011) Monitoring of organotin pollution in bizerta channel (Northern Tunisia): temporal trend from 2002 to 2010. Bull Environ Contam Toxicol 86(5):531–534CrossRefGoogle Scholar
  36. Lahbib Y, Abidli S, El Menif NT (2013) TBT pollution in Tunisian coastal lagoons as indicated by imposex in Hexaplex trunculus (Gastropoda: Muricidae). Trans Wat Bull 6:17–24Google Scholar
  37. Laranjeiro F, Sánchez-Marín P, Galante-Oliveira S, Barroso C (2015) Tributyltin pollution biomonitoring under the water frame work directive: proposal of a multispecies tool to assess the ecological quality status of EU water bodies. Ecol Indic 57:525–535CrossRefGoogle Scholar
  38. Laranjeiro F, Sánchez-Marín P, Oliveira IB, Galante-Oliveira S, Barroso C (2018) Fifteen years of imposex and tributyltin pollution monitoring along the Portuguese coast. Environ Pollut 232:411–421CrossRefGoogle Scholar
  39. Lemghich I, Benajiba M (2007) Survey of imposex in prosobranchs mollusks along the northern Mediterranean coast of Morocco. Ecol Indic 7:209–214CrossRefGoogle Scholar
  40. Lopes-dos-Santos R, Galante-Oliveira S, Lopes E, Almeida C, Barroso C (2014) Assessment of imposex and butyltin concentrations in Gemophos viverratus (Kiener, 1834), from São Vicente, Republic of Cabo Verde (Africa). Environ Sci Pollut Res 21(18):10671–10677CrossRefGoogle Scholar
  41. Mensink B, Ten Hallers-Tjabbes C, Kralt J, Freriks I, Boon J (1996) Assessment of imposex in the common whelk, Buccinum undatum (L.) from the eastern Scheldt, the Netherlands. Mar Environ Res 41(4):315–325CrossRefGoogle Scholar
  42. Mensink BP, Kralt H, Vethaak AD, Ten Hallers-Tjabbes CC, Koeman JH, van Hattum B, Boon JP (2002) Imposex induction in laboratory reared juvenile Buccinum undatum by tributyltin (TBT). Environ Toxicol Pharmacol 11(1):49–65CrossRefGoogle Scholar
  43. Minchin D, Oehlmann J, Duggan CB, Stroben E, Keatinge M (1995) Marine TBT antifouling contamination in Ireland, following legislation in 1987. Mar Pollut Bull 30(10):633–639CrossRefGoogle Scholar
  44. Neves R, Echeverria C, Pessoa L, Paiva P, Paranhos R, Valentin J (2013) Factors influencing spatial patterns of molluscs in a eutrophic tropical bay. J Mar Biol Assoc 93:577–589Google Scholar
  45. Nicolaus EM, Barry J (2015) Imposex in the dogwhelk (Nucella lapillus): 22-year monitoring around England and Wales. Environ Monit Assess 187(12):736CrossRefGoogle Scholar
  46. Oehlmann J, Stroben E, Fioroni P (1991) The morphological expression of imposex in Nucella lapillus (Linnaeus) (Gastropoda: Muricidae). J Molluscan Stud 57(3):375–390CrossRefGoogle Scholar
  47. Oehlmann J, Fioroni P, Stroben E, Markert B (1996) Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci Total Environ 188(2):205–223. CrossRefGoogle Scholar
  48. OSPAR (2005) The ecological quality objective on imposex in dog whelks Nucella lapillus. OSPAR, London, pp 1–11Google Scholar
  49. Petracco M, Monteiro Camargo R, Amorim Berenguel T, Patrício de Arruda NCL, del Matto LA, Lund Amado L, Navajas Corbisier T, Castro IB, Turra A (2015) Evaluation of the use of Olivella minuta (Gastropoda, Olividae) and Hastula cinerea (Gastropoda, Terebridae) as TBT sentinels for sandy coastal habitats. Environ Monit Assess 187:440. CrossRefGoogle Scholar
  50. Poli G (1973) Cycle reproducteur de mollusques, lamellibranches et gasteropodes, du Bassin d'Arcachon PhD Thesis, Universite de Paris VIGoogle Scholar
  51. Ramos M (2010) IBERFAUNA. The Iberian fauna databank. Available online at
  52. Rilov G, Benayahu Y, Gasith A (2001) Low abundance and skewed population structure of the whelk Stramonita haemastoma along the Israeli Mediterranean coast. Mar Ecol Prog Ser 218:189–202CrossRefGoogle Scholar
  53. Schulte-Oehlmannm U, Oehlmann J, Fioroni P, Bauer B (1997) Imposex and reproductive failure in Hydrobia ulvae (Gastropoda: Prosobranchia). Mar Biol 128:257–266Google Scholar
  54. Shi H, Huang C, Zhu S, Yu X, Xie W (2005) Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Mar Ecol Prog Ser 204:179–189CrossRefGoogle Scholar
  55. Smith BS (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. J Molluscan Stud 39(5):377–378Google Scholar
  56. Smith PJ (1996) Selective decline in imposex levels in the dogwhelk Lepsiella scobina following a ban on the use of TBT antifoulants in New Zealand. Mar Pollut Bull 32:362–365CrossRefGoogle Scholar
  57. Taylor J (1987) Feeding ecology of some common intertidal neogastropods at Djerba, Tunisia. Vie et milieu 37(1):13–20Google Scholar
  58. Ten Hallers-Tjabbes CC, Kemp JF, Boon JP (1994) Imposex in whelks (Buccinum undatum) from the open North Sea: relation to shipping traffic intensities. Mar Pollut Bull 28(5):311–313CrossRefGoogle Scholar
  59. Terlizzi A, Scuderi D, Fraschetti S, Anderson M (2005) Quantifying effects of pollution on biodiversity: a case study of highly diverse molluscan assemblages in the Mediterranean. Mar Biol 148(2):293–305CrossRefGoogle Scholar
  60. Titley-O'Neal CP, Munkittrick KR, MacDonald BA (2011) The effects of organotin on female gastropods. J Environ Monit 13(9):2360–2388CrossRefGoogle Scholar
  61. Toste R, Fernandez MA, Pessoa IA, Parahyba MA, Dore MP (2011) Organotin pollution at Arraial do Cabo, Rio de Janeiro state, Brazil: increasing levels after the TBT ban. Braz J Oceanogr 59(1):111–117CrossRefGoogle Scholar
  62. Waite ME, Waldock MJ, Thain JE, Smith DJ, Milton SM (1991) Reduction in TBT concentrations in UK estuaries following legislation in 1986-1987. Marine Environ Res 32:98–111CrossRefGoogle Scholar
  63. Yusuff BM (2006) Imposex cases in snails (Thais Spp.) in the West Coast of Peninsular Malaysia. Master Thesis, Universiti Putra MalaysiaGoogle Scholar
  64. Zaouali J (1978) Les peuplements malacologiques de la mer de Bou Grara. Bull Off Natn Pêche Tunisie 2(2):199–209Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Sciences of Bizerta. Laboratory of Environment Bio-monitoring, Group of Fundamental and Applied Malacology (LEB/GFAM)University of CarthageBizertaTunisia

Personalised recommendations