Abstract
This study represents the first use of Leucozonia nassa (Mollusca-Gastropoda) in a program of long-term monitoring. Specimens of L. nassa were collected between 2006 and 2014 and analyzed for the occurrence of imposex in two areas in Southeastern Brazil, one control area and another characterized by the presence of many ports and marinas. Imposex was evaluated in nine sites based on the percentage of females exhibiting imposex (I%), relative penis length index and vas deferens sequence index, classical indices to evaluate tributyltin (TBT) impacts. Moreover, this study uses for the first time in a tropical environment the ecological quality ratio (EQR), an approach to verify the imposex levels as an indicator of the impact by organotin compounds according to the EU Water Framework Directive. The results confirm the occurrence of high levels of imposex in L. nassa with all the indices evaluated. Furthermore, the results also indicate that, despite the international ban, antifouling paints based on TBT are still possibly used in Brazil. In addition, this study shows that L. nassa has the characteristics that make it a suitable bioindicator to monitor TBT pollution, and that the use of the EQR may create important data regarding this problem.
Similar content being viewed by others
References
Barroso, C. M., Moreira, M. H., & Bebianno, M. J. (2002). Imposex, female sterility and organotin contamination of the prosobranch Nassarius reticulatus from the Portuguese coast. Marine Ecology Progress Series, 230, 127–135. https://doi.org/10.3354/meps230127.
Bech, M. (2002). A survey of imposex in Muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island Thailand. Marine Pollution Bulletin, 44(9), 887–896. https://doi.org/10.1016/S0025-326X(02)00115-7.
Birchenough, A. C., Barnes, N., Evans, S. M., Hinz, H., Kronke, I., & Moss, C. (2002). A review and assessment of tributyltin contamination in the North Sea, based on surveys of butyltin tissue burdens and imposex/intersex in four species of neogastropods. Marine Pollution Bulletin, 44(6), 534–543. https://doi.org/10.1016/S0025-326X(01)00275-2.
Borges, C. L. L., Castro, I. B., Filmann, G., & Fernandez, M. A. (2013). Organotin pollution from pleasure craft at Paraty, a tourist area in southeastern Brazil: amelioration or interference? Brazilian Journal of Oceanography, 61(3), 177–186. https://doi.org/10.1590/S1679-87592013000300002.
Cacciatore, F., Noventa, S., Antonini, C., Formalewicz, M., Gion, C., Berto, D., Gabellini, M., & Brusà, R. B. (2016). Imposex in Nassarius Nitidus (Jeffreys, 1867) as a possible investigative tool to monitor butyltin contamination according to the Water Framework Directive: A case study in the Venice Lagoon (Italy). Ecotoxicology and Environmental Safety. https://doi.org/10.1016/j.ecoenv.2015.12.039.
Castro, I. B., Lima, A. F., Braga, A. R. C., & Rocha-Barreira, C. A. (2007a). Imposex in two muricid species (Mollusca: Gastropoda) from the northeastern Brazilian coast. Journal of the Brazilian Society of Ecotoxicology, 2(1), 81–91. https://doi.org/10.5132/jbse.2007.01.012.
Castro, I. B., Bemvenuti, C. E., & Fillmann, G. (2007b). Preliminary appraisal of imposex in area under the influence of southern Brazilian harbors. Journal of the Brazilian Society of Ecotoxicology, 2007(1), 73–79. https://doi.org/10.5132/jbse.2007.01.011.
Castro, I. B., Perina, F. C., & Fillmann, G. (2012). Organotin contamination in South American coastal areas. Environmental Monitoring and Assessment, 184(3), 1781–1799. https://doi.org/10.1007/s10661-011-2078-7.
Champ, M. A. (2000). A review of organotin regulatory strategies, pending actions, related costs and benefits. Science of the Total Environment, 258(1-2), 21–71. https://doi.org/10.1016/S0048-9697(00)00506-4.
Costa, M. B., Fernandez, M. A. S., Barbiero, D. C., Melo, F. T. V., Otegui, M. B. P., & Ferreira, B. S. (2008a). First record of imposex in Thais deltoidea (Lamarck, 1822) (Mollusca, Gastropoda, Thaididae) in Vitória, ES. Brazil. Brazilian Journal of Oceanography, 56(2), 145–148. https://doi.org/10.1590/s1679-87592008000200007.
Costa, M. B., Otegui, M. B. P., Barbiero, D. C., & Fernandez, M. A. S. (2008b). Cymatium parthenopeum parthenopeum (Von Salis, 1793) (Mesogastropoda: Ranellidae): a new bioindicator of organotin compounds contamination? Journal of the Brazilian Society of Ecotoxicology, 3(1), 65–69. https://doi.org/10.5132/jbse.2008.01.010.
Costa, M. B., Zamprogno, G. C., Pedruzzi, F. C., Dalbem, G. B., & Tognella, M. M. P. (2013). Assessing the continuous impact of tributyltin from antifouling paints in a Brazilian mangrove area using intersex in Littoraria angulifera (Lamarck, 1822) as biomarker. International Journal of Oceanography, 2013, 1–8. https://doi.org/10.1155/2013/769415.
Costa, M. B., Zamprogno, G. C., Pedruzzi, F. C., De Morais, L., Tognella, M. M. P., Godoi, A. F. L., Santos, D. M., De Marchi, M. R. R., & Fernandez, M. A. (2014a). Differential organotin sensitivity in two species from a ship traffic area in southeastern Brazil. Marine Biology Research, 10(7), 712–724. https://doi.org/10.1080/17451000.2013.850512.
Costa, M.B., Mardegan, B.S., Zamprogno, G.C., Pedruzzi, F.C., De Morais, L, Dalbem, G.B., Silva, D.A., & Graceli, J.B. (2014b). Penis Malformations in Leucozonia nassa (Gmelin, 1792) and Leucozonia ocellata (Gmelin, 1791) in a TBT Contaminated Region from Brazil. Aquatic Science and Technology, 2, 2. doi:https://doi.org/10.5296/ast.v2i2.5697
Couto, D. R., & Pimenta, A. D. (2012). Comparative morphology of Leucozonia from Brazil (Neogastropoda: Buccinoidea: Fasciolariidae). American Malacological Bulletin, 30(1), 103–116. https://doi.org/10.4003/006.030.0108.
Cristale, J., Santos, D. M., Sant'Anna, B. S., Sandron, D. C., Cardoso, S., Turra, A., & Marchi, M. R. R. (2012). Tributyltin in crustacean tissues: analytical performance and validation of method. Journal of the Brazilian Chemical Society, 23(1), 39–45. https://doi.org/10.1590/S0103-50532012000100007.
De Fur, P. L., Crane, M., Ingersoll, C. G., & Tattersfield, L. (1999). In P. L. De Fur, M. Crane, C. G. Ingersoll, & L. Tattersfield (Eds.), Endocrine disruption in invertebrates: endocrinology, testing and assessment. Pensacola: SETAC Press.
EC, (2000). Directive 2000/60/EC of the European Parliament and the Council of 23 October 2000 Establishing a Framework for Community Action in the Field of Water Policy.
EC, (2008). Directive 2008/105/EC of the European Parliament and the Council of the 16 December 2008 on Environmental Quality Standards in the Field of Water Policy, Amending and Subsequently Repealing Directives 82/172/EEC, 83/513/ EEC, 84/156/EEC, 84/491/EEC and 86/280/EEC and Amending Directive 2000/ 60/EC.
El Menif, N.T., Lahbib, Y., Le Pennec, M., Flower, R., & Boumaiza, M. (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, 6, 3. doi: https://doi.org/10.4172/2157-7625.1000210.
Evans, S. M., Hutton, A., Kendall, M. A., & Samosir, A. M. (1991). Recovery in populations of dogwhelks Nucella lapillus (L.) suffering from imposex. Marine Pollution Bulletin, 22(7), 331–333. https://doi.org/10.1016/0025-326X(91)90067-3.
Fent, K. (1996). Organotin compounds in municipal wastewater and sewage sludge: contamination, fate in treatment process and ecotoxicological consequences. Science of the Total Environment, 185(1-3), 151–159. https://doi.org/10.1016/0048-9697(95)05048-5.
Fernandez, M. A., Wagener, A. L. R., Limaverde, A., Scofield, A. L., Pinheiro, F. M., & Rodrigues, E. (2005). Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Marine Environmental Research, 59(5), 435–452. https://doi.org/10.1016/j.marenvres.2004.07.001.
Fernandez, M. A., Pinheiro, F. M., Quadros, J. P., & Camillo Jr., E. (2007). An easy, non-destructive, probabilistic method to evaluate the imposex response of gastropod populations. Marine Environmental Research, 63(1), 41–54. https://doi.org/10.1016/j.marenvres.2006.06.002.
Gibbs, P. E. (1996). Oviduct malformation as a sterilising effect of tributyltin (TBT)-induced imposex in Ocenebra erinacea (Gastropoda: Muricidae). The Malacological Society of London, 62(4), 403–413. https://doi.org/10.1093/mollus/62.4.403.
Gibbs, P. E., & Bryan, G. W. (1986). Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom, 66(04), 767. https://doi.org/10.1017/S0025315400048414.
Gibbs, P. E., & Bryan, G. W. (1987). TBT paints and demise of the dog-whelk Nucella lapillus (Gastropoda). Journal of the Marine Biological Association of the United Kingdom. https://doi.org/10.1109/OCEANS.1987.1160635.
Gibbs, P. E., & Bryan, G. W. (1994). Biomonitoring of tributyltin pollution using the imposex response of neogastropod mollusks. In K. J. M. Kramer (Ed.), Biomonitoring of coastal waters and estuaries (pp. 205–226). Florida: Press Inc..
Godoi, A. F. L., Montone, R. C., & Santiago-Silva, M. (2003). Determination of butyltin compounds in surface sediments from the Sao Paulo State coast (Brazil) by gas chromatography-pulsed flame photometric detection. Journal of Chromatography A, 985(1-2), 205–210. https://doi.org/10.1016/S0021-9673(02)01456-5.
Gooding, M., Gallardo, C., & Leblanc, G. (1999). Imposex in three marine gastropod species in Chile and potential impact on muriciculture. Marine Pollution Bulletin, 38(12), 1227–1231. https://doi.org/10.1016/S0025-326X(99)00167-8.
Lahbib, Y., Abidli, S., González, P. R., Alonso, J. I. G., & Trigui-El Menif, N. (2011). Potential of Nassarius nitidus for monitoring organotin pollution in the lagoon of Bizerta (northern Tunisia). Journal of Environmental Sciences, 23(9), 1551–1557. https://doi.org/10.1016/S1001-0742(10)60582-7.
Laranjeiro, F., Sánchez-Marín, P., Galante-Oliveira, S., & Barroso, C. (2015a). Tributyltin pollution biomonitoring under the Water Framework Directive: proposal of a multi-species tool to assess the ecological quality status of EU water bodies. Ecological Indicators. https://doi.org/10.1016/j.ecolind.2015.04.039.
Laranjeiro, F., Pérez, S., Navarro, P., Carrero, J. A., & Beiras, R. (2015b). The usefulness of a sediment bioassay with the gastropod Nassarius reticulatus in tributyltin monitoring programs. Chemosphere, 139, 550–557. https://doi.org/10.1016/j.chemosphere.2015.07.076.
Matthiessen, P., & Gibbs, P. (1998). Critical appraisal of the evidence for tributyltin mediated endocrine disruption in mollusks. Environmental Toxicology and Chemistry, 17(1), 37–43. https://doi.org/10.1002/etc.5620170106.
Matthiessen, P., Reed, J., & Johnson, M. (1999). Sources and potential effects of copper and zinc concentrations in the estuarine waters of Essex and Suffolk, United Kingdom. Marine Pollution Bulletin, 38(10), 908–920. https://doi.org/10.1016/S0025-326X(99)00090-9.
Miller, K. L., Fernandes, T. F., & Read, P. A. (1999). The recovery of populations of dogwhelks surveying from imposex in the Firth of Forth 1987–1997/98. Environmental Pollution, 106(2), 183–192. https://doi.org/10.1016/S0269-7491(99)00076-7.
Morcillo, Y., & Porte, C. (1998). Monitoring of organotin compounds and their effects in marine molluscs. Trends in Analytical Chemistry, 17(2), 109–116. https://doi.org/10.1016/s0165-9936(97)00115-5.
Nicholson, G. J., & Evans, S. M. (1997). Anthropogenic impacts on the stocks of the common whelk Buccinum undatum (L.) Marine Environmental Research, 44(3), 305–314. https://doi.org/10.1016/S0141-1136(97)00009-3.
Oehlmann, J., Stroben, E., & Fiorini, P. (1991). The morphological expression of imposex in Nucella lapillus (Linnaeus) (Gastropoda: Muricidae). Journal of Molluscan Studies, 57(3), 375–390. https://doi.org/10.1093/mollus/57.3.375.
Oehlmann, J., Stroben, E., Bettin, C., & Fioroni, P. (1992). Proceedings of the 27th European Marine Biology Symposium, pp. 301–305.
Oehlmann, J., Stroben, E. B., Schulte-Oehlmann, U. A., & Bauer, B. (1998). Imposex development in response to TBT pollution in Hinia incrassata (Ström, 1768) (Prosobranchia, Stenoglossa). Aquatic Toxicology, 43(4), 239–260. https://doi.org/10.1016/S0166-445X(98)00058-7.
Pavoni, B., Centanni, E., Valcanover, S., Fasolato, M., Ceccato, S., & Tagliapietra, D. (2007). Imposex levels and concentrations of organotin compounds (TBT and its metabolites) in Nassarius nitidus from the Lagoon of Venice. Marine Pollution Bulletin, 55(10–12), 505–511. https://doi.org/10.1016/j.marpolbul.2007.09.012.
Pessoa, I., Fernandez, M., Toste, R., Dore, M., & Parahyba, M. (2009). Imposex in a touristic area in Southeastern Brazilian coast. Journal of Coastal Research, 56, 881–884.
Power, A. J., & Keegan, B. F. (2001). The significance of imposex levels and TBT contamination in the red whelk, Neptunea antiqua (L.) from the offshore Irish Sea. Marine Pollution Bulletin, 42(9), 761–772. https://doi.org/10.1016/S0025-326X(00)00221-6.
Rato, M., Gaspar, M. B., Takahashi, S., Yano, S., Tanabe, S., & Barroso, C. (2008). Inshore/offshore gradients of imposex and organotin contamination in Nassarius reticulatus (L.) along the Portuguese coast. Marine Pollution Bulletin, 56(7), 1323–1331. https://doi.org/10.1016/j.marpolbul.2008.04.004.
Rilov, G., Gasith, A., Evans, S. M., & Benayahu, Y. (2000). Unregulated use of TBT based- antifouling paints in Israel (eastern Mediterranean): high contamination and imposex levels in two species of marine gastropods. Marine Ecology Progress Series, 192, 229–238. https://doi.org/10.3354/meps192229.
Ruiz, J. M., Barreiro, R., Couceiro, L., & Quintela, M. (2008). Decreased TBT pollution and changing bioaccumulation pattern in gastropods imply butyltin desorption from sediments. Chemosphere, 73(8), 1253–1257. https://doi.org/10.1016/j.chemosphere.2008.07.029.
Sant’anna, B. S., Santos, D. M., Sandron, D. C., Souza, S. C., Marchi, M. R. R., Zara, F. J., & Turra, A. (2012). Hermit crabs as bioindicators of recent tributyltin (TBT) contamination. Ecological Indicators, 14(1), 184–188. https://doi.org/10.1016/j.ecolind.2011.08.010.
Sant’anna, B. S., Santos, D. M., Marchi, M. R., Zara, F. J., & Turra, A. (2014). Surface-sediment and hermit-crab contamination by butyltins in southeastern Atlantic estuaries after ban of TBT-based antifouling paints. Environmental Science and Pollution Research, 21(10), 6516–6524. https://doi.org/10.1007/s11356-014-2521-8.
Santos, M. M., Ten Hallers-Tjabbes, C. C., Santos, A. M., & Vieira, N. (2002). Imposex in Nucella lapillus, a bioindicator for TBT contamination: Re-survey along the Portuguese coast to monitor the effectiveness of EU regulation. Journal of Sea Research, 48(3), 217–223. https://doi.org/10.1016/S1385-1101(02)00166-1.
Santos, M. M., Vieira, N., Reis-Henriques, M. A., Santos, A. M., Gomez-Ariza, J. L., Giraldez, I., & Ten Hallers-Tjabbes, C. C. (2004). Imposex and butyltin contamination off the Oporto Coast (NW Portugal): a possible effect of the discharge of dredged material. Environment International, 30(6), 793–798. https://doi.org/10.1016/j.envint.2004.01.005.
Santos, M. M., Reis-Henriques, M. A., Guillot, R., Lima, D., Franco-Duarte, R., Mendes, I., Queirós, S., & Castro, L. F. C. (2008). Anti-androgenic effects of sewage treatment plant effluents in the prosobranch gastropod Nucella lapillus. Comparative Biochemistry and Physiology, Part C, 148(1), 87–93. https://doi.org/10.1016/j.cbpc.2008.03.012.
Santos, D. M., Sant’Anna, B. S., Sadron, D. C., Souza, S. C., Cristale, J., Marchi, M. R. R., & Turra, A. (2010). Occurrence and behavior of butyltins in intertidal and shallow subtidal surface sediments of an estuarine beach under different sampling conditions. Estuarine, Coastal and Shelf Science, 88(3), 322–328. https://doi.org/10.1016/j.ecss.2010.04.009.
Santos, D. M., Sant’Anna, B. S., Godoi, A. F. L., Turra, A., & Marchi, M. R. R. (2011). Contamination and impact of organotin compounds on the Brazilian coast. In A. C. Ortiz & N. B. Griffin (Eds.), Pollution monitoring (pp. 31–59). New York: Nova Science Publishers. https://doi.org/10.1017/S1755267209990716.
Shi, H. H., Huang, C. J., Zhu, S. X., Yu, X. J., & Xie, W. Y. (2005). Generalized system of imposex and reproductive failure in female gastropods of coastal waters in mainland China. Marine Ecology Progress Series, 304, 179–189. https://doi.org/10.3354/meps304179.
Shim, W. J., Kahng, S. H., Hong, S. H., Kim, N. S., Kim, S. K., & Shim, J. H. (2000). Imposex in the rock shell, Thais clavigera, as evidence of organotin contamination in the marine environment of Korea. Marine Environmental Research, 49(5), 435–451. https://doi.org/10.1016/S0141-1136(99)00084-7.
Shim, W. J., Hong, S. H., Yim, U. H., Kim, N. S., & Oh, J. R. (2002). Horizontal and vertical distribution of butyltin compounds in sediments from ship yards in Korea. Archives of Environmental Contamination and Toxicology, 43(3), 277–283. https://doi.org/10.1007/s00244-002-0156-0.
Sousa, A., Mendo, S., & Barroso, C. (2005). Imposex and organotin contamination in Nassarius reticulatus (L.) along the Portuguese coast. Applied Organometallic Chemistry, 19(3), 315–323. https://doi.org/10.1002/aoc.856.
Sousa, A., Matsudaira, C., Takahashi, S., Tanabe, S., & Barroso, C. (2007). 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, 54(10), 1645–1653. https://doi.org/10.1016/j.marpolbul.2007.07.005.
Sousa, A., Laranjeiro, F., Takahashi, S., Tanabe, S., & Barroso, C. M. (2009). Imposex and organotin prevalence in a European post-legislative scenario: Temporal trends from 2003 to 2008. Chemosphere, 77(4), 566–573. https://doi.org/10.1016/j.chemosphere.2009.06.049.
Stroben, E., Brömmel, C., Oehlmann, J., & Fiorini, P. (1992). Hinia reticulata and Nucella lapillus. Comparison of two gastropod tributyltin bioindicators. Marine Biology, 114(2), 289–296. https://doi.org/10.1007/BF00349532.
Stroben, E., Oehlmann, J., Schulte-Oehlmann, U., & Fioroni, P. (1996). Seasonal variations in the genital ducts of normal and imposex-affected prosobranchs and its influence on biomonitoring indices. Malacological Review Supplement, 6, 173–184.
Swennen, C., Sampantarak, U., & Ruttanadakul, N. (2009). TBT-pollution in the Gulf of Thailand: a re-inspection of imposex incidence after 10 years. Marine Pollution Bulletin, 58(4), 526–532. https://doi.org/10.1016/j.marpolbul.2008.11.028.
Tan, K. S. (1999). Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the Straits of Johor: a case study using penis length, area and weight as measures of imposex severity. Marine Pollution Bulletin, 39(1-12), 295–303. https://doi.org/10.1016/S0025-326X(98)00181-7.
Terlizzi, A., Geraci, S., & Gibbs, P. E. (1999). Tributyltin (TBT)-induced imposex in the neogastropod Hexaplex trunculus in Italian coastal waters: morphological aspects and ecological implications. Italian Journal of Zoology, 66(2), 141–146. https://doi.org/10.1080/11250009909356248.
Teso, V. S., & Penchaszadeh, P. E. (2009). Beach filling and imposex in Olivancillaria deshayesiana (Mollusca: Gastropoda: Olividae) from the coast of Mar del Plata, Argentina. Journal of the Marine Biological Association of the United Kingdom, 89(03), 557. https://doi.org/10.1017/S0025315409002896.
Titley-O’Neal, C. P., Munkittrick, K. R., & Macdonald, B. A. (2011). The effects of organotin on female gastropods. Journal of Environmental Monitoring, 13(9), 2360–2388. https://doi.org/10.1039/C1EM10011D.
Turner, A. (2010). Marine pollution from antifouling paint particles. Marine Pollution Bulletin, 60(2), 159–171. https://doi.org/10.1016/j.marpolbul.2009.12.004.
Vasconcelos, P., Gaspar, M. B., & Barroso, C. M. (2010). Imposex in Bolinus brandaris from the Ria Formosa lagoon (southern Portugal): usefulness of “single-site baselines” for environmental monitoring. Journal of Environmental Monitoring, 12(10), 1823–1832. https://doi.org/10.1039/c0em00261e.
WFD-CIS. (2003). Common implementation strategy for the Water Framework Directive (2000/60/EC). Guidance Document No 5. Transitional and Coastal Waters – Typology, Reference Conditions and Classification Systems. Produced by Working Group 2.4 – COAST.
Acknowledgements
This study was funded by the Support Fund for Science and Technology/Vitoria (FACITEC/PMV) (Process No. 035/2006 and Process No. 2273/2008) and the Foundation for Support of Science and Technology of the State of Espírito Santo (FAPES) (Process 35521724/2006).
Author information
Authors and Affiliations
Corresponding author
Additional information
Highlights
• Use of the Leucozonia nassa (Mollusca-Gastropoda) in a program of long-term monitoring.
• L. nassa has characteristics that make it suitable as an indicator species in programs to monitor TBT.
• This study uses for the first time the Ecological Quality Ratio (EQR) in a tropical environment.
• The results from EQR were corresponding with the classical indexes of imposex.
Electronic supplementary material
ESM 1
(DOCX 18 kb)
Rights and permissions
About this article
Cite this article
da Costa, M.B., Zamprogno, G.C., Otegui, M.B.P. et al. 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, 650 (2017). https://doi.org/10.1007/s10661-017-6367-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-017-6367-7