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Pugilina morio L., a New Imposex Exhibitor from South American Estuarine Environments: Approach for a Non-Lethal Method to Evaluate Imposex

Abstract

This is the first report on imposex occurrence in Pugilina morio. Imposex levels in P. morio from Ceará River Estuary were assessed by a non-lethal method. The obtained imposex parameters were: percentage = 37.1 %, female penis length index (FPLI) = 0.93 mm, relative penis length index (RPLI) = 6.5 %, and vas deferens sequence index (VDSI) = 1.0. Because imposex is induced by tributyltin, and P. morio is widely distributed on the East coast of South America, the species can be used as a tributyltin contamination sentinel in these estuaries. Additionally, a non-lethal method of evaluating imposex minimized the impact on the population of P. morio from sample collection, as all organisms were returned to the environment.

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References

  1. Abbott RT, Dance SP (1982) Compendium of seashells. Odyssey Publications, Perth

    Google Scholar 

  2. Almeida E, Diamantino TC, de Sousa O (2007) Marine paints: the particular case of antifouling paints. Prog Org Coat 59:2–20

    Article  CAS  Google Scholar 

  3. Alzieu C (2000) Environmental impact of TBT: the French experience. Sci Total Environ 258:99–102

    Article  CAS  Google Scholar 

  4. Barroso CX, Matthews-Cascon H (2009) Distribuição espacial e temporal da malacofauna no estuário do rio Ceará, Ceará, Brasil. Panameric J Aqua Sci 4:79–86

    Google Scholar 

  5. Bigatti G, Carranza A (2007) Phenotypic variability associated with the occurrence of imposex in Odontocymbiola magellanica from Golfo Nuevo, Patagonia. J Mar Biol Ass U K 87:1–5

    Article  Google Scholar 

  6. Blaber SJM (1970) The occurence of a penis-like out grow behid the right tentacle in spent females of Nucella lapillus (L.). Proc Malacol Soc London 39:231–233

    Google Scholar 

  7. Castro ÍB, Fillmann G (2012) High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environ Toxicol Chem 31:955–960

    Article  CAS  Google Scholar 

  8. Castro IB, Meirelles CAO, Matthews-Cascon H, Fernandez MAS (2004) Thais (Stramonita) rustica (Lamarck, 1822) (Mollusca: Gastropoda: Thaididae), a potential bioindicator of contamination by organotin Northeast Brazil. Braz J Oceanogr 52:135–139

    Article  Google Scholar 

  9. Castro IB, Bemvenuti CE, Fillmann G (2007a) Preliminary appraisal of imposex in areas under the influence of Southern Brazilian Harbors. J Braz Soc Ecotoxicol 2:73–79

    Article  Google Scholar 

  10. Castro IB, Lima AFA, Braga ARC, Rocha-Barreira CA (2007b) Imposex in two muricid species (Mollusca: Gastropoda) from the Northeastern Brazilian Coast. J Braz Soc Ecotoxicol 2:81–91

    Article  Google Scholar 

  11. Castro IB, Arroyo M, Costa Pc, Fillmann G (2012a) Butyltin compounds and imposex levels in ecuador. Arch Environ Contam Toxicol 62:68–77

    Article  CAS  Google Scholar 

  12. Castro IB, Perina F, Fillmann G (2012b) Organotin contamination in South American coastal areas. Environ Monit Assess 184:1781–1799

    Article  CAS  Google Scholar 

  13. Castro IB, Rocha-Barreira CdA, Fernandez MA, Bigatti G (2012c) Transplant bioassay induces different imposex responses in two species of the genus Stramonita. Mar Biol Res 8:397–404

    Article  Google Scholar 

  14. Champ MA (2000) A review of organotin regulatory strategies, pending actions, related costs and benefits. Sci Total Environ 258:21–71

    Article  CAS  Google Scholar 

  15. Fernandez MA, Pinheiro FM, de Quadros JP, Camillo J (2007) An easy, non-destructive, probabilistic method to evaluate the imposex response of gastropod populations. Mar Environ Res 63:41–54

    Article  CAS  Google Scholar 

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

    Google Scholar 

  17. Galante-Oliveira S, Oliveira I, Jonkers N, Langston WJ, Pacheco M, Barroso CM (2009) Imposex levels and tributyltin pollution in Ria de Aveiro (NW Portugal) between 1997 and 2007: evaluation of legislation effectiveness. J Environ Monit 11:1405–1411

    Article  CAS  Google Scholar 

  18. Gibbs PE (1993) Phenotypic changes in the progeny of Nucella lapillus (Gastropoda) transplanted from an exposed shore to sheltered inlets. Malacol Soc Lond 59:187–194

    Google Scholar 

  19. Gibbs PE, Bryan GM (1987) TBT paints and demise of the dog-whelk Nucella lapillus (Gastropoda). J Mar Biol Ass UK 68:1482–1487

    Google Scholar 

  20. Gibbs PE, Bryan GM, Pascoe PL, Burt GR (1987) The use of dog-whelk Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Ass UK 67:507–523

    Article  CAS  Google Scholar 

  21. Horiguchi T, Kojima M, Hamada F, Kajikawa A, Shiraishi H, Morita M, Shimizu M (2006) Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect 114:13–19

    Article  Google Scholar 

  22. Huet M, Fioroni P, Oehlmann J, Stroben E (1995) Comparison of imposex response in 3 prosobranch species. Hydrobiologia 309:29–35

    Article  Google Scholar 

  23. Kotrikla A (2009) Environmental management aspects for TBT antifouling wastes from the shipyards. J Environ Manage 90:S77–S85

    Article  CAS  Google Scholar 

  24. Lima AFA, Castro IB, Rocha CA (2006) Imposex induction in Stramonita haemastoma floridana (Conrad, 1837) (Mollusca: Gastropoda: Muricidae) submitted to an organotin contaminated diet. Braz J Oceanogr 24:85–90

    Google Scholar 

  25. Matthews-Cascon H (1990) Notas sobre a espécie Pugilina morio (Linnaeus, 1758) no nordeste brasileiro. Arq Cien Mar 13: 191–192

  26. Matthews-Cascon H (2003) Observations on the reproduction of Pugilina morio (Linnaeus, 1758) (Mollusca: Gastropoda: Melongenidae). The Veliger 46:267–274

    Google Scholar 

  27. Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17:37–43

    Article  CAS  Google Scholar 

  28. Nakayama A, Segner H, Kawai S (2009) Immunotoxic effects of organotin compounds in teleost fish. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo, pp 207–218

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  30. Quintela M, Barreiro R, Ruiz JM (2002) Dumpton Syndrome reduces the tributyltin (TBT) sterilising effect on Nucella lapillus (L.) by limiting the development of the imposed vas deferens. Mar Environ Res 54:657–660

    Article  CAS  Google Scholar 

  31. Rittschof D, McClellan-Green P (2005) Molluscs as multidisciplinary models in environment toxicology. Mar Pollut Bull 50:369–373

    Article  CAS  Google Scholar 

  32. Robin A (2008) Encyclopedia of marine gastropod. IKAN Unterwasser-Archiv, Paris

    Google Scholar 

  33. Smith BS (1971) Sexuality in the American mud-snail Nassarius obsoletus Say. Proc Malacol Soc London 39:377–378

    Google Scholar 

  34. Smith BS (1981) Tributyltin compounds induce male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsoleta. J Appl Toxicol 1:141–144

    Article  CAS  Google Scholar 

  35. Sousa A, Laranjeiro F, Takahashi S, Tanabe S, Barroso CM (2009) Imposex and organotin prevalence in a European post-legislative scenario: Temporal trends from 2003 to 2008. Chemosphere 77:566–573

    Article  CAS  Google Scholar 

  36. Sternberg R, Gooding M, Hotchkiss A, LeBlanc G (2010) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19:4–23

    Article  CAS  Google Scholar 

  37. Stroben E, Oehlmann J, Fioroni P (1992a) Hinia reticulata and Nucella lapillus: comparison of 2 gastropod tributyltin bioindicators. Mar Biol 114:289–296

    Article  Google Scholar 

  38. Stroben E, Oehlmann J, Fioroni P (1992b) The morphological expression of imposex in Hinia reticulata (Gastropoda, Buccinidae): a potential indicator of tributyltin pollution. Mar Biol 113:625–636

    Article  Google Scholar 

  39. Takahashi S, Tanabe S, Takeuchi I, Miyazaki N (1999) Distribution and specific bioaccumulation of butyltin compounds in a marine ecosystem. Arch Environ Contam Toxicol 37:50–61

    Article  CAS  Google Scholar 

  40. tem Hallers-Tjabbes CC, Kemp JF, Boom JP (1994) Imposex in whelks (Buccinum undatum) from the open North Sea: relation to shipping traffic intensities. Mar Pollut Bull 28:311–313

    Article  Google Scholar 

  41. Titley-O’Neal CP, Munkittrick KR, MacDonald BA (2011) The effects of organotin on female gastropods. J Environ Monit 13:2360–2388

    Article  Google Scholar 

  42. Yang J, Miyazaki N, Kunito T, Tanabe S (2006) Trace elements and butyltins in a Dall’s porpoise (Phocoenoides dalli) from the Sanriku coast of Japan. Chemosphere 63:449–457

    Article  Google Scholar 

  43. Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology–past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104

    Article  CAS  Google Scholar 

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Correspondence to Ítalo Braga Castro.

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de Azevedo, D., de Almeida Rocha-Barreira, C., Matthews-Cascon, H. et al. 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, 786–792 (2012). https://doi.org/10.1007/s00128-012-0779-4

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Keywords

  • Organotin
  • Estuaries
  • Harbor
  • TBT