Environmental Science and Pollution Research

, Volume 23, Issue 16, pp 16047–16055 | Cite as

Spatiotemporal appraisal of TBT contamination and imposex along a tropical bay (Todos os Santos Bay, Brazil)

  • Vanda Artifon
  • Ítalo Braga Castro
  • Gilberto FillmannEmail author
Research Article


A spatiotemporal evaluation of butyltin contamination was performed between 2010 and 2012 along Todos os Santos Bay (Northeast Brazil) using surface sediments, bivalve tissues (Anomalocardia brasiliana and Mytella guyanensis), and imposex occurrence (Stramonita rustica). The spatial study detected high tributyltin (TBT) levels (maximum values of 262 ng Sn g -1 - 21,833 ng Sn g−1 of total organic carbon - for surface sediments and 421 ng Sn g−1 for bivalve tissues) in the innermost part of the bay. The TBT levels detected in M. guyanensis tissues might cause human health risk since local population consumes these organisms. These high concentrations observed in the bivalves might result in ingestions higher than the safe limits established by European Food Safety Authority (250 ng TBT kg−1 day−1). Considering the temporal evaluation, no difference (p > 0.05) was observed between TBT concentrations in sediments obtained during the two sampling campaigns (2010/2011 and 2012). However, the increasing predominance of TBT metabolites (butyltin degradation index (BDI) >1) in more recent sediments indicates further degradation of old TBT inputs. In spite of that, recent inputs are still evident at this region. Nevertheless, a reduction of imposex parameters in S. rustica over the last decade suggests an overall decline in the TBT contamination, at least in the outermost and possible less impacted region of the bay. The TBT contamination is probably reducing due to the national and international legislative restrictions on the use of TBT as antifouling biocide. The contamination levels, however, are still relevant especially in the inner part of Todos os Santos Bay since they are above those that are likely to cause toxicity to the biota.


Antifouling TBT Imposex Mytella guyanensis Human health risk Sediments 



We thank FINEP for the financial support (project no. 01.11.0038.00). V. Artifon was sponsored by CAPES, Í.B. Castro by CAPES (802-16/2012) and FAPERGS (0885/12-1), and G. Fillmann by CNPq (PQ 312341/2013-0). We also thank Vanessa Hatje and Gilmara Eça from the Universidade Federal da Bahia (UFBA) for supplying the samples of campaign 1.


  1. Abidli S, Santos MM, Lahbib Y, Castro LFC, Reis-Henriques MA, Trigui El Menif N (2012) Tributyltin (TBT) effects on Hexaplex trunculus and Bolinus brandaris (Gastropoda: Muricidae): imposex induction and sex hormone levels insights. Ecol Indic 13:13–21CrossRefGoogle Scholar
  2. Azevedo D, Rocha-Barreira C, Matthews-Cascon H, Castro Í (2012) Pugilina morio L., a new imposex exhibitor from South American estuarine environments: approach for a non-lethal method to evaluate imposex. Bull Environ Contamination Toxicol 89:786–792CrossRefGoogle Scholar
  3. Bezerra FJ (2008) O bosque de mangues e a pesca artesanal no Distrito de Acupe (Santo Amaro, Bahia): uma abordagem etnoecológica. Acta Scentarium 30:267–273Google Scholar
  4. Bigatti G, Primost MA, Cledón M, Averbuj A, Theobald N, Gerwinski W, Arntz W, Morriconi E, Penchaszadeh PE (2009) Biomonitoring of TBT contamination and imposex incidence along 4700 km of Argentinean shoreline (SW Atlantic: From 38S to 54S). Mar Pollut Bull 58:695–701CrossRefGoogle Scholar
  5. Birchenough AC, Evans SM, Moss C, Welch R (2002) Re-colonisation and recovery of populations of dogwhelks Nucella lapillus (L.) on shores formerly subject to severe TBT contamination. Mar Pollut Bull 44:652–659CrossRefGoogle Scholar
  6. Burton ED, Phillips IR, Hawker DW (2006) Tributyltin partitioning in sediments: Effect of aging. Chemosphere 63:73–81Google Scholar
  7. Cao D, Jiang G, Zhou Q, Yang R (2009) Organotin pollution in China: an overview of the current state and potential health risk. J Environ Manag 90:S16–S24CrossRefGoogle Scholar
  8. Castro ÍB, Fillmann G (2012) High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environ Toxicol Chem 31:955–960CrossRefGoogle Scholar
  9. 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 52:135–139CrossRefGoogle Scholar
  10. Castro IB, Lima AFA, Braga ARC, Rocha-Barreira CA (2007) Imposex in two muricid species (Mollusca: Gastropoda) from the Northeastern Brazilian coast. J Bra Soc Ecotoxicol 2:81–91CrossRefGoogle Scholar
  11. Castro IB, Perina F, Fillmann G (2012a) Organotin contamination in South American coastal areas. Environ Monit Assess 184:1781–1799CrossRefGoogle Scholar
  12. Castro ÍB, Rossato M, Fillmann G (2012b) Imposex reduction and residual butyltin contamination in southern Brazilian harbors. Environ Toxicol Chem 31:947–954CrossRefGoogle Scholar
  13. Castro IB, Arroyo M, Costa P, Fillmann G (2012c) Butyltin compounds and imposex levels in Ecuador. Arch Environ Contam Toxicol 62:68–77CrossRefGoogle Scholar
  14. Castro IB, Rocha-Barreira C de A, Fernandez MA, Bigatti G (2012d) Transplant bioassay induces different imposex responses in two species of the genus Stramonita. Mar Biol Res 8:397–404CrossRefGoogle Scholar
  15. Cirano M, Lessa GC (2007) Oceanographic characteristics of Baía de Todos os Santos, Brazil. Revista Brasileira de Geofísica 25:363–387CrossRefGoogle Scholar
  16. Culmo RF, Swanson KJ, Brennan WP (2003). Application of the PE2400 CHN elemental analyzer for organic particulate matter in water. Elemental Analysis Newsletter [S.1.], v.31.Google Scholar
  17. Di Toro DM, Rosa LD (1991) Equilibrium partitioning and organic carbon normalization. National Sediment Bioaccumulation Conference, New JerseyGoogle Scholar
  18. Díez S, Abalos M, Bayona JM (2002) Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation. Water Res 36:905–918CrossRefGoogle Scholar
  19. EFSA (2004) Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission to assess the health risks to consumers associated with exposure to organotins in foodstuffs. EFSA J 102:1–119Google Scholar
  20. Felizzola JF, de Luca Rebello Wagener A, Almeida AC, Lin WO (2008) Butyltin speciation in sediments from Todos os Santos Bay (Bahia, Brazil) by GC-PFPD. Quim Nov. 31:89–93Google Scholar
  21. Fernandez MAS, De Luca Rebello Wagener A, Limaverde AM, Scofield AL, Pinheiro FM, Rodrigues EF (2005a) Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Mar Environ Res 59:435–452CrossRefGoogle Scholar
  22. Fernandez MA, Limaverde AM, Scofield AL, de Luca Rebello Wagener A (2005b) Preliminary evaluation of human health risks from ingestion of organotin contamined seafood in Brazil. Braz J Oceanogr 53:75–77CrossRefGoogle Scholar
  23. Galante-Oliveira S, Oliveira I, Jonkers N, et al (2009) Imposex levels and tributyltin pollution in Ria de Aveiro (NW Portugal) between 1997 and 2007: evaluation of legislation effectiveness. J Environ Monit 11:1405–1411Google Scholar
  24. Galante-Oliveira S, Oliveira I, Ferreira N, et al (2011) Nucella lapillus L. imposex levels after legislation prohibiting TBT antifoulants: temporal trends from 2003 to 2008 along the Portuguese coast. J Environ Monit 13:304–312Google Scholar
  25. Genz F, Lessa GC, Cirano M (2006) The impact of an extreme flood upon the mixing zone of the Todos os Santos Bay, Northeastern Brazil. J Coast Res 39:707–712Google Scholar
  26. 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 Assoc U K 67:507–523CrossRefGoogle Scholar
  27. Gipperth L (2009) The legal design of the international and European Union ban on tributyltin antifouling paint: Direct and indirect effects. J Environ Manage 90:S86–S95Google Scholar
  28. Graceli JB, Cena GC, Lopes PF, Zamprogno GC, da Costa MB, Godoi AF, Dos Santos DM, de Marchi MR, dos Santos Fernandez MA (2013) Organotins: a review of their reproductive toxicity, biochemistry, and environmental fate. Reprod Toxicol 36:40–52CrossRefGoogle Scholar
  29. Gray JS (1981) The ecology of marine sediments. Cambridge University Press, New YorkGoogle Scholar
  30. Grimón ROR, Arroyo MF, Freitas DM, Castro ÍB (2016) Tributyltin impacts in Galapagos Islands and Ecuadorian shore: marine protected areas under threat. Mar Policy 69:24–31. doi: 10.1016/j.marpol.2016.03.017 CrossRefGoogle Scholar
  31. Guomundsdóttir LÓ, Ho KKY, Lam JCW, Svavarsson J, Leung KMY (2011) Long-term temporal trends (1992-2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast. Marine Pollution Bulletin. In Press.Google Scholar
  32. Hatje V, Andrade JB (2009) Baía de Todos os Santos: Aspectos Oceanográficos. EDUFBA, Savaldor, p 303Google Scholar
  33. Hoch M (2001) Organotin compounds in the environment—an overview. Appl Geochem 16:719–743CrossRefGoogle Scholar
  34. Hoch M, Schwesig D (2004) Parameters controlling the partitioning of tributyltin (TBT) in aquatic systems. Appl Geochem 19:323–334Google Scholar
  35. Horiguchi T (2009) The endocrine-disrupting effect of organotin compounds for aquatic organisms. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo, pp 125–146CrossRefGoogle Scholar
  36. IMO (2008) Summary of the status of conventions as at 31 May 2007. International Maritime Organization, United Kingdom, Google Scholar
  37. IUPAC (International Union of Pure and Applied Chemistry) (2002) Analytical, applied, clinical, inorganic, and physical chemistry divisions interdivisional working party for harmonization of quality assurance schemes for analytical laboratories. Pure Appl Chem 74:835–855Google Scholar
  38. Jorundsdottir K, Svavarsson K, Leung KMY (2005) Imposex levels in the dogwhelk Nucella lapillus (L.)—continuing improvement at high latitudes. Mar Pollut Bull 51:744–749CrossRefGoogle Scholar
  39. Kotrikla A (2009) Environmental management aspects for TBT antifouling wastes from the shipyards. J Environ Manag 90:S77–S85CrossRefGoogle Scholar
  40. Louppis AP, Georgantelis D, Paleologos EK, Kontominas MG (2010) Determination of tributyltin through ultrasonic assisted micelle mediated extraction and GFAAS: application to the monitoring of tributyltin levels in greek marine species. Food Chemistry. In Press, Accepted ManuscriptGoogle Scholar
  41. Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17:37–43CrossRefGoogle Scholar
  42. Meador JP, Sommers FC, Cooper KA, Yanagida G (2011) Tributyltin and the obesogen metabolic syndrome in a salmonid. Environ Res 111:50–56CrossRefGoogle Scholar
  43. Morabito R, Massanisso P, Quevauviller P (2000) Derivatization methods for the determination of organotin compounds in environmental samples. TrAC Trends Anal Chem 19:113–119CrossRefGoogle Scholar
  44. NORMAM (2007) Normas da Autoridade Marítima para o Controle de Sistemas Anti-incrustantes Danosos em Embarcações—NORMAM/23. Marinha do Brasil, Rio de JaneiroGoogle Scholar
  45. Oehlmann J, Schulte-Oehlmann U (2003) Molluscs as bioindicators. In: Markert BA (ed) Trace metals and other contaminants in the environment bioindicators & biomonitors principles, concepts and applications. Elsevier, Philadelphia, pp 577–635CrossRefGoogle Scholar
  46. Oliveira IB, Richardson CA, Sousa AC, et al (2009) Spatial and temporal evolution of imposex in dogwhelk Nucella lapillus (L.) populations from North Wales, UK. J Environ Monit 11:1462–1468Google Scholar
  47. Oliveira CR, Santos DM, Santos Madureira LA, Marchi MR (2010) Speciation of butyltin derivatives in surface sediments of three southern Brazilian harbors. J Hazard Mater 181:851–856CrossRefGoogle Scholar
  48. Otchere FA (2005) Organochlorines (PCBs and pesticides) in the bivalves Anadara (Senilis) senilis, Crassostrea tulipa and Perna perna from the lagoons of Ghana. Sci Total Environ 348:102–114CrossRefGoogle Scholar
  49. Paz-Villarraga CA, Castro IB, Miloslavich P, Fillmann G (2015) Venezuelan Caribbean Sea under the threat of TBT. Chemosphere 119:704–710CrossRefGoogle Scholar
  50. Pinochet H, Tessini C, Bravo M, Quiroz W, De Gregori I (2009) Butyltin compounds and their relation with organic matter in marine sediments from San Vicente Bay, Chile. Environ Monit Assess 155:341–353CrossRefGoogle Scholar
  51. Pletsch LA, Beretta M, Tania Mascarenhas Tavares MT (2010) Distribuição espacial de compostos orgânicos de estanho em sedimentos costeiros e em Phallusia nigra da baía de Todos os Santos e litoral norte da Bahia - Brasil. Quim Nov. 33(2):451–457Google Scholar
  52. Rittschof D, McClellan-Green P (2005) Molluscs as multidisciplinary models in environment toxicology. Mar Pollut Bull 50:369–373CrossRefGoogle Scholar
  53. Santos DM, Araújo IP, Machado EC, Carvalho-Filho MAS, Fernandez MA, Marchi MRR, Godoi AF (2009) Organotin compounds in the Paranaguá Estuarine Complex, Paraná, Brazil: evaluation of biological effects, surface sediment, and suspended particulate matter. Mar Pollut Bull 58:1926–1931CrossRefGoogle Scholar
  54. Sericano JL, Wade TL, Jackson TJ, Brooks JM, Tripp BW, Farrington JW, Mee LD, Readmann JW, Villeneuve JP, Goldberg ED (1995) Trace organic contamination in the Americas: an overview of the US National Status and Trends and the International Mussel Watch programmes. Mar Pollut Bull 31:214–225CrossRefGoogle Scholar
  55. 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 77:566–573CrossRefGoogle Scholar
  56. Toste R, Fernandez MA, Pessoa I de A, 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 59:111–117CrossRefGoogle Scholar
  57. Toste R, Pessoas IA, Dore DP, Parayba MA, Ferandez MA (2013) Aphallic vas deferens development in females related to the distance from organotin sources? A study with Stramonita haemastoma. Ecotoxicol Environ Saf 91:162–170CrossRefGoogle Scholar
  58. Town RM, Filella M (2002) Implications of natural organic matter binding heterogeneity on understanding lead(II) complexation in aquatic systems. Sci Total Environ 300:143–154CrossRefGoogle Scholar
  59. Waite ME, Waldock MJ, Thain JE, Smith DJ, Milton SM (1991) Reductions in TBT concentrations in UK estuaries following legislation in 1986 and 1987. Mar Environ Res 32:89–111CrossRefGoogle Scholar
  60. Wang J, Yao P, Bianchi TS, Li D, Zhao B, Xingqian C, Pan H, Zhang T, Yu Z (2015) The effect of particle density on the sources, distribution, and degradation of sedimentary organic carbon in the Changjiang Estuary and adjacent shelf. Chem Geol 402:52–67CrossRefGoogle Scholar
  61. 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 50:75–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Vanda Artifon
    • 1
  • Ítalo Braga Castro
    • 1
    • 2
  • Gilberto Fillmann
    • 1
    Email author
  1. 1.Laboratório de Microcontaminantes Orgânicos e Ecotoxicologia Aquática, Instituto de Oceanografia, Universidade Federal do Rio GrandeRio GrandeBrazil
  2. 2.Departamento de Ciências do MarUniversidade Federal de São PauloSantosBrazil

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