Organotin pollution at Arraial do Cabo, Rio de Janeiro State, Brazil: increasing levels after the TBT ban

Toste, Raquel; Fernandez, Marcos Antônio; Pessoa, Igor de Araújo; Parahyba, Mateus Alves; Dore, Marina Pereira

Abstracts

Imposex, an endocrine disruption phenomenon, is a biomarker of tributyltin (TBT) exposure in marine gastropod populations. The occurrence and intensity of the syndrome in populations of the neogastropod Stramonita haemastoma were ascertained at nine sampling stations in October 2008 at Arraial do Cabo, a very important tourist resort in Rio de Janeiro state (Brazil) and part of the Marine Extractive Reserve of Arraial do Cabo. The results obtained made it possible to evaluate the changes which had occurred since the last biomonitoring campaign, undertaken in 2001, at these same stations. Despite the ban on the use of TBT imposed by the Brazilian Navy in 2003, the controls on the use of this agent in Brazil resulting from the establishment of NORMAM 23 by the Navy in 2007 and the complete ban of organotin compounds in antifouling paint formulae by the IMO on a global scale in 2008, imposex was still detected. Instead of the expected reduction, an increase was observed in the areas affected by imposex. Furthermore, populations in the areas seriously affected by imposex in 2001 were absent in the 2008 sampling campaign. These results suggest an increase in TBT pollution in the study area, indicating the inefficacy of legislative measures.

Imposex; Stramonita haemastoma; Forno Harbor; Organotins

O imposex, um fenômeno de desregulação endócrina, é um biomarcador da exposição ao tributilestanho (TBT) em populações de gastrópodes marinhos. A ocorrência e intensidade dessa síndrome nas populações do neogastrópode Stramonita haemastoma foram verificadas em nove estações amostrais em outubro de 2008 em Arraial do Cabo, uma área de grande importância turística no Rio de Janeiro (Brasil) e integrante da Reserva Extrativista Marinha de Arraial do Cabo. Com os resultados obtidos foi possível avaliar as alterações ocorridas desde o último biomonitoramento realizado em 2001, nessas mesmas estações. Mesmo após o banimento do TBT pela Marinha do Brasil em 2003, a entrada em vigor dos controles ao uso deste agente com o estabelecimento da NORMAM 23, no Brasil em 2007 pela Marinha, e o banimento completo do TBT nas fórmulas de tintas antiincrustantes pela IMO em escala global, em 2008, o imposex continua a ser detectado. Ao invés de um declínio esperado, observou-se um aumento da extensão das áreas afetadas pelo imposex. Além disso, observou-se a ausência de populações em áreas que em 2001 estavam gravemente afetadas pelo imposex. Esses resultados sugerem um aumento da poluição por TBT na área de estudo, indicando a ineficácia das medidas legislativas.

Imposex; Stramonita haemastoma; Porto do Forno; Organoestânicos

ANTAQ, Agência Nacional de Transportes Aquaviários (National Agengy of Waterborne Transport). Available on: http://www.antaq.gov.br/portal/estatisticasanuario.asp Consulted in Jan. 28, 2010.
» link
BURTON, E. D.; PHILLIPS, I. R.; HAWKER, D. W. Tributyltin partitioning in sediments: Effect of aging. Chemosphere, v. 63, n. 1: p. 73-81, 2006.
CARVALHO, W. F.; GONZALEZ-RODRIGUEZ, E. Development of primary and bacterial productivity in upwelling waters of Arraial do Cabo region, RJ (Brazil). Brazilian Journal of Oceanography, v. 52, n. 1: p. 35-45, 2004.
CASTRO, Í. B., MEIRELLES, C. A. O., PINHEIRO, J. C. L., MATTHEWS-CASCON, H.; ROCHA-BARREIRA, C. A. The increasing incidence of imposex in Stramonita haemastoma (Mollusca: Gastropoda: Muricidae) after the establishment of the Pecém harbor, Ceará State, Northeast Brazil. Thalassas, v. 21, n. 2: p. 71-75, 2005.
CHAMP, M. A. A review of organotin regulatory strategies, pending actions, related costs and benefits. The Science of the Total Environment, v. 258: p. 21-71, 2000.
CHOI, M.; MOON, H.; EOM, J. Y. J.; CHOI, H. Temporal trend of butyltins in seawater, sediments, and mussels from Busan Harbor of Korea between 2002 and 2007: tracking the effectiveness of tributylin regulation. Archives of Environmental Contamination and Toxicology, v. 58: p. 394-402, 2010.
FENT, K. Ecotoxicology of organotin compounds. Critical Reviews in Toxicology, v. 26, n. 1, p. 1-117, 1996.
FERNANDEZ, M. A.; PINHEIRO, F. M. New approaches for monitoring the marine environment: the case of antifouling paints. International Journal of Environment and Health, v. 1, n. 3: p. 427-448, 2007.
FERNANDEZ, M. A.; PINHEIRO, F. M.; QUADROS, J. P.; CAMILLO, E. An easy, non-destructive, probabilistic method to evaluate the imposex response of gastropod populations. Marine Environmental Research, v. 63: p. 41-54, 2007.
FERNANDEZ, M. A.; OSTRITZ, F.; REZENDE, A. R.; SILVA, S. C.; FOLHA, D. O.; PINHEIRO, F. M. Temporal variability of imposex development in Stramonita haemastoma in Guanabara Bay at a fixed sampling station: results from 1998-2006. In: Environmental and Health World Congress, 2006 Santos, SP, Brazil. Proceedings of Environmental and Health Congress, p. 75-79, 2006.
FERNANDEZ, M. A. S.; WAGENER, A. L. R.; LIMAVERDE, A. C.; SCOFIELD, A. L.; PINHEIRO, F. M.; RODRIGUES, E. Imposex and surface sediment speciation: A combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental Research, v. 59: p. 435-452, 2005.
GALANTE-OLIVEIRA, S.; OLIVEIRA, I.; JONKERS, N.; LANGSTON, W. J.; PACHECO, M.; BARROSO, C. M. Imposex levels and tributyltin pollution in Ria de Aveiro (NW Portugal) between 1997 and 2007: evaluation of legislation effectiveness. Journal of the Environmental Monitoring, 11: p. 1405-1411, 2009.
IMO. Summary of Status of Convection. Available on: www.imo.org/Conventions/mainframe.asp?topic_id=247 . Consulted in Jul. 07, 2010.
IMO, 2001. International Convention on the Control of Harmful Anti-fouling Systems on Ships. Available on: www.imo.org/Conventions/mainframe.asp?topic_id=529 . Consulted in Jul. 07, 2010.
KOTRIKLA, A. Environmental management aspects for TBT antifouling wastes from the shipyards. Journal of Environmental Management, v. 90, n. 1: p. S77-S85. 2009.
LANGSTON, W. J.; POPE, N.D. Determinants of TBT adsorption and desorption in estuarine sediments. Marine Pollution Bulletin, v. 31, n. 1-3, p. 32-43, 1995.
LIMAVERDE, A. M.; WAGENER, A. L. R.; FERNANDEZ, M. A.; SCOFIELD, A. L.; COUTINHO, R. Stramonita haemastoma as bioindicator for organotin contamination in coastal environments. Marine Environmental Research, v. 64: p. 384-398, 2007.
MATHIESSEN, P.; GIBBS, P. E. Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environmental Toxicology and Chemistry, v. 17: p. 37-43, 1998.
MORTON, B. Recovery from imposex by a population of the dogwhelk, Nucella lapillus (Gastropoda: Caenogastropoda), on the southeastern coast of England since May 2004: A 52-month study. Marine Pollution Bulletin, v. 58, n. 10: p. 1530-1538, 2009.
NORMAM 23. Controle de sistemas antiincrustantes danosos em embarcações -Normas da Autoridade Marítima - Marinha do Brasil. 2007. Available on: www.dpc.mar.mil.br/normam/N23/N_23.htm Consulted in Jan. 28, 2010.
OLIVEIRA, I. B. ; RICHARDSON, C. A. ; SOUSA, A. C. ; TAKAHASHI, S. ; TANABE, S. ; BARROSO, C. M. Spatial and temporal evolution of imposex in dogwhelk Nucella lapillus (L.) populations from North Wales, UK. Journal of Environmental Monitoring, v. 11, n. 8: p. 1462-1468, 2009.
PESSOA, I.; FERNANDEZ, M.; TOSTE, R.; DORE, M.; PARAHYBA, M. Imposex in a touristic area in Southeastern Brazilian coast. In: Journal of Coastal Research, SI 56, 2009. Proceedings of the 10th International Coastal Symposium, Lisboa, Portugal: p. 881-884, 2009.
PIGNATELLO, J. J.; XING, B. Mechanisms of slow sorption of organic chemicals to natural particles. Environmental Science and Technology, v. 30, n. 1: p. 1-11, 1996.
PINHEIRO, F. M.; FERNANDEZ, M. A.; FRAGOSO, M. R.; QUADROS, J. P.; CAMILLO, E. Jr.; DOS SANTOS, F. A. Assessing the impacts of organotin compounds in Ilha Grande Bay (Rio de Janeiro, Brazil): Imposex and a multiple-source dispersion model. Journal of Coastal Research, SI 39, 2006. Proceedings of the 8th International Coastal Symposium, SC, Brazil: p. 1383-1388, 2006.
QUEIROZ, L. R.; CASTRO, I. B.; ROCHA-BARREIRA, C. A. New Imposex Development Index (IDI) for Stramonita haemastoma (Mollusca: Muricidae): A Transplantation Experiment in the Brazilian Northeast. Journal of the Brazilian Society of Ecotoxicology, v. 2, n. 3: p. 249-256, 2007.
RIVARO, P.; FRANCHE, R.; LEARDI, R. Seasonal variations in levels of butyltin compounds in mussel tissues samples in an oil port. Journal of Analytical Atomic Spectrometry, v. 11, n. 3, p. 99-106, 1996.
RUIZ, J.M.; BARREIRO, R.; COUCEIRO, L.; QUINTELA, M. Decreased TBT pollution and changing bioaccumulation pattern in gastropods imply butyltin desorption from sediments. Chemosphere, v. 73, n. 8, p. 1253-1257, 2008.
SANTOS, D. M.; ARAÚJO, I. P.; MACHADO, E. C.; CARVALHO-FILHO, M. A. S.; FERNANDEZ, M. A.; MARCHI, M. R.R.; GODOI, A. F. L. Organotin compounds in the Paranaguá Estuarine Complex, Paraná, Brazil: Evaluation of biological effects, surface sediment, and suspended particulate matter. Marine Pollution Bulletin, v. 58, n. 12, p. 1926-1931, 2009.
SHI, H.; HUANG, C.; XIUJUAN, Y. An updated scheme of imposex for Cantharus cecillei (Gastropoda: Buccinidae) and a new mechanism leading to the sterilization of imposex-affected females. Marine Biology, v. 146, n. 4: p. 717-723, 2005.
SOARES, A. L. S. The market and productive chain of fluminense fisheries. In: VIANA, MARCELO, "Diagnosis of the productive chain of marine fisheries in Rio de Janeiro State". FAERJ/SEBRAE - RJ, Rio de Janeiro, 200p. (in portuguese), p. 71-90. 2009.
SOUSA, A.; LARANJEIRO, F.; TAKAHASHI, S.; TANABE, S.; BARROSO, C. M. Imposex and organotin prevalence in a European post-legislative scenario: temporal trends from 2003 to 2008. Chemosphere, v. 77, n. 4: p. 566-573, 2009a.
SOUSA, A.; IKEMOTO, T.; TAKAHASHI, S.; BARROSO, C.; TANABE, S. Distribution of synthetic organotins and total tin levels in Mytilus galloprovincialis along the Portuguese coast. Marine Pollution Bulletin, v. 58, n. 1: p. 1130-1136, 2009b.
SOUSA, A.; MATSUDAIRA, C.; TAKAHASHI, S.; TANABE, S.; BARROSO, C. Integrative assessment of organotin contamination in a southern European estuarine system (Ria de Aveiro, NW Portugal): Tracking temporal trends in order to evaluate the effectiveness of the EU ban. Marine Pollution Bulletin, v. 54, n. 10: p. 1645-1653, 2007.
SPENCE, S. K.; HAWKINS, S. J.; SANTOS, R. S. The mollusc Thais haemastoma - An exhibitor of imposex and potential biological indicator of tributyltin pollution. Marine Ecology, v. 11, n. 2: p. 147-156, 1990.
TALLMON, D.; HOFERKAMP, L. Long-Term Changes in Imposex Frequency in File Dogwinkles, Nucella lima G., and Tributyltin Concentrations in Bay Mussels, Mytilus trossulus G. Bulletin of Environmental Contamination and Toxicology, v. 83, n. 2: p. 235-238, 2009.
RIBEIRO, V. P. Avaliação do potencial da espécie Stramonita haemastoma (Kool, 1987) como indicador biológico de contaminação ambiental por compostos organo-estânicos 2002.108p. Dissertação (Mestrado em Biologia Marinha) - Universidade Federal Fluminense, UFF, Rio de Janeiro.

Publication Dates

Publication in this collection
04 May 2011
Date of issue
Mar 2011

History

Received
04 Feb 2010
Reviewed
26 Apr 2010
Accepted
14 July 2010

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] ANTAQ, Agência Nacional de Transportes Aquaviários (National Agengy of Waterborne Transport). Available on: http://www.antaq.gov.br/portal/estatisticasanuario.asp Consulted in Jan. 28, 2010.
» link

[2] BURTON, E. D.; PHILLIPS, I. R.; HAWKER, D. W. Tributyltin partitioning in sediments: Effect of aging. Chemosphere, v. 63, n. 1: p. 73-81, 2006.

[3] CARVALHO, W. F.; GONZALEZ-RODRIGUEZ, E. Development of primary and bacterial productivity in upwelling waters of Arraial do Cabo region, RJ (Brazil). Brazilian Journal of Oceanography, v. 52, n. 1: p. 35-45, 2004.

[4] CASTRO, Í. B., MEIRELLES, C. A. O., PINHEIRO, J. C. L., MATTHEWS-CASCON, H.; ROCHA-BARREIRA, C. A. The increasing incidence of imposex in Stramonita haemastoma (Mollusca: Gastropoda: Muricidae) after the establishment of the Pecém harbor, Ceará State, Northeast Brazil. Thalassas, v. 21, n. 2: p. 71-75, 2005.

[5] CHAMP, M. A. A review of organotin regulatory strategies, pending actions, related costs and benefits. The Science of the Total Environment, v. 258: p. 21-71, 2000.

[6] CHOI, M.; MOON, H.; EOM, J. Y. J.; CHOI, H. Temporal trend of butyltins in seawater, sediments, and mussels from Busan Harbor of Korea between 2002 and 2007: tracking the effectiveness of tributylin regulation. Archives of Environmental Contamination and Toxicology, v. 58: p. 394-402, 2010.

[7] FENT, K. Ecotoxicology of organotin compounds. Critical Reviews in Toxicology, v. 26, n. 1, p. 1-117, 1996.

[8] FERNANDEZ, M. A.; PINHEIRO, F. M. New approaches for monitoring the marine environment: the case of antifouling paints. International Journal of Environment and Health, v. 1, n. 3: p. 427-448, 2007.

[9] FERNANDEZ, M. A.; PINHEIRO, F. M.; QUADROS, J. P.; CAMILLO, E. An easy, non-destructive, probabilistic method to evaluate the imposex response of gastropod populations. Marine Environmental Research, v. 63: p. 41-54, 2007.

[10] FERNANDEZ, M. A.; OSTRITZ, F.; REZENDE, A. R.; SILVA, S. C.; FOLHA, D. O.; PINHEIRO, F. M. Temporal variability of imposex development in Stramonita haemastoma in Guanabara Bay at a fixed sampling station: results from 1998-2006. In: Environmental and Health World Congress, 2006 Santos, SP, Brazil. Proceedings of Environmental and Health Congress, p. 75-79, 2006.

[11] FERNANDEZ, M. A. S.; WAGENER, A. L. R.; LIMAVERDE, A. C.; SCOFIELD, A. L.; PINHEIRO, F. M.; RODRIGUES, E. Imposex and surface sediment speciation: A combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental Research, v. 59: p. 435-452, 2005.

[12] GALANTE-OLIVEIRA, S.; OLIVEIRA, I.; JONKERS, N.; LANGSTON, W. J.; PACHECO, M.; BARROSO, C. M. Imposex levels and tributyltin pollution in Ria de Aveiro (NW Portugal) between 1997 and 2007: evaluation of legislation effectiveness. Journal of the Environmental Monitoring, 11: p. 1405-1411, 2009.

[13] IMO. Summary of Status of Convection. Available on: www.imo.org/Conventions/mainframe.asp?topic_id=247 . Consulted in Jul. 07, 2010.

[14] IMO, 2001. International Convention on the Control of Harmful Anti-fouling Systems on Ships. Available on: www.imo.org/Conventions/mainframe.asp?topic_id=529 . Consulted in Jul. 07, 2010.

[15] KOTRIKLA, A. Environmental management aspects for TBT antifouling wastes from the shipyards. Journal of Environmental Management, v. 90, n. 1: p. S77-S85. 2009.

[16] LANGSTON, W. J.; POPE, N.D. Determinants of TBT adsorption and desorption in estuarine sediments. Marine Pollution Bulletin, v. 31, n. 1-3, p. 32-43, 1995.

[17] LIMAVERDE, A. M.; WAGENER, A. L. R.; FERNANDEZ, M. A.; SCOFIELD, A. L.; COUTINHO, R. Stramonita haemastoma as bioindicator for organotin contamination in coastal environments. Marine Environmental Research, v. 64: p. 384-398, 2007.

[18] MATHIESSEN, P.; GIBBS, P. E. Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environmental Toxicology and Chemistry, v. 17: p. 37-43, 1998.

[19] MORTON, B. Recovery from imposex by a population of the dogwhelk, Nucella lapillus (Gastropoda: Caenogastropoda), on the southeastern coast of England since May 2004: A 52-month study. Marine Pollution Bulletin, v. 58, n. 10: p. 1530-1538, 2009.

[20] NORMAM 23. Controle de sistemas antiincrustantes danosos em embarcações -Normas da Autoridade Marítima - Marinha do Brasil. 2007. Available on: www.dpc.mar.mil.br/normam/N23/N_23.htm Consulted in Jan. 28, 2010.

[21] OLIVEIRA, I. B. ; RICHARDSON, C. A. ; SOUSA, A. C. ; TAKAHASHI, S. ; TANABE, S. ; BARROSO, C. M. Spatial and temporal evolution of imposex in dogwhelk Nucella lapillus (L.) populations from North Wales, UK. Journal of Environmental Monitoring, v. 11, n. 8: p. 1462-1468, 2009.

[22] PESSOA, I.; FERNANDEZ, M.; TOSTE, R.; DORE, M.; PARAHYBA, M. Imposex in a touristic area in Southeastern Brazilian coast. In: Journal of Coastal Research, SI 56, 2009. Proceedings of the 10th International Coastal Symposium, Lisboa, Portugal: p. 881-884, 2009.

[23] PIGNATELLO, J. J.; XING, B. Mechanisms of slow sorption of organic chemicals to natural particles. Environmental Science and Technology, v. 30, n. 1: p. 1-11, 1996.

[24] PINHEIRO, F. M.; FERNANDEZ, M. A.; FRAGOSO, M. R.; QUADROS, J. P.; CAMILLO, E. Jr.; DOS SANTOS, F. A. Assessing the impacts of organotin compounds in Ilha Grande Bay (Rio de Janeiro, Brazil): Imposex and a multiple-source dispersion model. Journal of Coastal Research, SI 39, 2006. Proceedings of the 8th International Coastal Symposium, SC, Brazil: p. 1383-1388, 2006.

[25] QUEIROZ, L. R.; CASTRO, I. B.; ROCHA-BARREIRA, C. A. New Imposex Development Index (IDI) for Stramonita haemastoma (Mollusca: Muricidae): A Transplantation Experiment in the Brazilian Northeast. Journal of the Brazilian Society of Ecotoxicology, v. 2, n. 3: p. 249-256, 2007.

[26] RIVARO, P.; FRANCHE, R.; LEARDI, R. Seasonal variations in levels of butyltin compounds in mussel tissues samples in an oil port. Journal of Analytical Atomic Spectrometry, v. 11, n. 3, p. 99-106, 1996.

[27] RUIZ, J.M.; BARREIRO, R.; COUCEIRO, L.; QUINTELA, M. Decreased TBT pollution and changing bioaccumulation pattern in gastropods imply butyltin desorption from sediments. Chemosphere, v. 73, n. 8, p. 1253-1257, 2008.

[28] SANTOS, D. M.; ARAÚJO, I. P.; MACHADO, E. C.; CARVALHO-FILHO, M. A. S.; FERNANDEZ, M. A.; MARCHI, M. R.R.; GODOI, A. F. L. Organotin compounds in the Paranaguá Estuarine Complex, Paraná, Brazil: Evaluation of biological effects, surface sediment, and suspended particulate matter. Marine Pollution Bulletin, v. 58, n. 12, p. 1926-1931, 2009.

[29] SHI, H.; HUANG, C.; XIUJUAN, Y. An updated scheme of imposex for Cantharus cecillei (Gastropoda: Buccinidae) and a new mechanism leading to the sterilization of imposex-affected females. Marine Biology, v. 146, n. 4: p. 717-723, 2005.

[30] SOARES, A. L. S. The market and productive chain of fluminense fisheries. In: VIANA, MARCELO, "Diagnosis of the productive chain of marine fisheries in Rio de Janeiro State". FAERJ/SEBRAE - RJ, Rio de Janeiro, 200p. (in portuguese), p. 71-90. 2009.

[31] SOUSA, A.; LARANJEIRO, F.; TAKAHASHI, S.; TANABE, S.; BARROSO, C. M. Imposex and organotin prevalence in a European post-legislative scenario: temporal trends from 2003 to 2008. Chemosphere, v. 77, n. 4: p. 566-573, 2009a.

[32] SOUSA, A.; IKEMOTO, T.; TAKAHASHI, S.; BARROSO, C.; TANABE, S. Distribution of synthetic organotins and total tin levels in Mytilus galloprovincialis along the Portuguese coast. Marine Pollution Bulletin, v. 58, n. 1: p. 1130-1136, 2009b.

[33] SOUSA, A.; MATSUDAIRA, C.; TAKAHASHI, S.; TANABE, S.; BARROSO, C. Integrative assessment of organotin contamination in a southern European estuarine system (Ria de Aveiro, NW Portugal): Tracking temporal trends in order to evaluate the effectiveness of the EU ban. Marine Pollution Bulletin, v. 54, n. 10: p. 1645-1653, 2007.

[34] SPENCE, S. K.; HAWKINS, S. J.; SANTOS, R. S. The mollusc Thais haemastoma - An exhibitor of imposex and potential biological indicator of tributyltin pollution. Marine Ecology, v. 11, n. 2: p. 147-156, 1990.

[35] TALLMON, D.; HOFERKAMP, L. Long-Term Changes in Imposex Frequency in File Dogwinkles, Nucella lima G., and Tributyltin Concentrations in Bay Mussels, Mytilus trossulus G. Bulletin of Environmental Contamination and Toxicology, v. 83, n. 2: p. 235-238, 2009.

[36] RIBEIRO, V. P. Avaliação do potencial da espécie Stramonita haemastoma (Kool, 1987) como indicador biológico de contaminação ambiental por compostos organo-estânicos 2002.108p. Dissertação (Mestrado em Biologia Marinha) - Universidade Federal Fluminense, UFF, Rio de Janeiro.