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Organochlorine pesticides in green sea turtles (Chelonia mydas) with and without fibropapillomatosis caught at three feeding areas off Brazil

Published online by Cambridge University Press:  12 February 2016

Angélica María Sánchez-Sarmiento ,
Silmara Rossi ,
Franz Zirena Vilca ,
Ralph Eric Thijl Vanstreels ,
Sergio Henrique Monteiro ,
Luiz Américo S. Vale ,
Robson Guimarães Dos Santos ,
Juliana Marigo Open the ORCID record for Juliana Marigo [Opens in a new window] ,
Carolina Pacheco Bertozzi  and
José Henrique Hildebrand Grisi Filho
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Angélica María Sánchez-Sarmiento*
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
Silmara Rossi
Affiliation:
Escola Superior de Agricultura Luiz de Queiroz e Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, Brazil
Franz Zirena Vilca
Affiliation:
Laboratório de Ecotoxicologia, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, Brazil
Ralph Eric Thijl Vanstreels
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
Sergio Henrique Monteiro
Affiliation:
Centro P & D de Proteção Ambiental, Instituto Biológico, São Paulo, Brazil
Luiz Américo S. Vale
Affiliation:
Grupo de Pesquisa em Química Verde e Ambiental, Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil
Robson Guimarães Dos Santos
Affiliation:
Departamento de Oceanografia e Ecologia, Universidade Federal do Espírito Santo, Vitória, ES, Brazil
Juliana Marigo
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
Carolina Pacheco Bertozzi
Affiliation:
Projeto Biopesca, Praia Grande, SP, Brazil
José Henrique Hildebrand Grisi Filho
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
Valdemar Luiz Tornisielo
Affiliation:
Laboratório de Ecotoxicologia, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, Brazil
Eliana Reiko Matushima
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
*
Correspondence should be addressed to:A.M. Sánchez-Sarmiento, Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-270, Brazil email: ang.san.sar@gmail.com
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Abstract

Many factors threaten the survival of marine turtles, such as incidental capture by fisheries, habitat degradation, pollution and diseases. One of the most important diseases is fibropapillomatosis (FP), characterized by the development of benign skin tumours. FP predominantly affects juvenile green sea turtles (Chelonia mydas) and involves a complex multifactorial aetiology. For several years, it has been noted that the prevalence of FP tends to be higher in marine environments under the influence of human activities, leading to the hypothesis that environmental pollutants play a role in the epidemiology of this disease. Organochlorine compounds (OCs) are persistent organic pollutants with immunosuppressive and carcinogenic effects in humans and wildlife. OC levels (α-BHC, β-BHC, α-endosulphan, β-endosulphan, endosulphan sulphate, pp′-DDD, op′-DDD, pp′-DDE, op′-DDE, heptachlor, dicofol and mirex) were quantified through gas chromatography with a micro-electron capture detector (GC-μECD) in liver and fat samples from 64 juvenile green sea turtles. Specimens with and without FP were analysed, after being caught at three feeding areas off the Brazilian coast: Ubatuba, Praia Grande and Vitória. OC levels were comparable to those observed in similar studies, and no consistent difference was observed between sea turtles with and without FP. This study helps to elucidate the contamination profile in sea turtles caught at feeding areas off Brazil and confirms that green sea turtles are exposed to OCs, which may play a negative role in the health of this species.

Keywords

ecotoxicologypersistent organic pollutants (POPs)pollutionsea turtlesSouth-east Braziltumourstoxicity
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 1 , February 2017 , pp. 215 - 223
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Aguilar, A. (1984) Relationship of DDE/ΣDDT in marine mammals to the chronology of DDT input into the ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 840–844.Google Scholar
Aguirre, A.A., Balazs, G.H., Zimmerman, B. and Galey, F.D. (1994a) Organic contaminants and trace metals in the tissues of green turtles (Chelonia mydas) afflicted with fibropapillomas in the Hawaiian islands. Marine Pollution Bulletin 28, 109–114.Google Scholar
Aguirre, A.A., Balazs, G.H., Zimmerman, B. and Spraker, T.R. (1994b) Evaluation of Hawaiian green turtles (Chelonia mydas) for potential pathogens associated with fibropapillomas. Journal of Wildlife Diseases 30, 8–15.Google Scholar
Aguirre, A.A. and Lutz, P.L. (2004) Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator? EcoHealth 1, 275–283.Google Scholar
Almeida, F.V., Centeno, A.J., Bisinoti, M.C. and Jardim, W.F. (2007) Substâncias Tóxicas Persistentes (STP) no Brasil. Quimica Nova 30, 1976–1985.Google Scholar
Ananthaswamy, H. and Pierceall, W.E. (1990) Molecular mechanisms of ultraviolet radiation carcinogenesis. Photochemistry and Photobiology 52, 1119–1136.Google Scholar
Anastassiades, M., Lehotay, S.J., Stajnbaher, D. and Schenck, F.J. (2003) Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. Journal of AOAC International 86, 412–431.CrossRefGoogle ScholarPubMed
Arthur, K., Limpus, C., Balazs, G., Capper, A., Udy, J., Shaw, G., Keuper-Bennett, U. and Bennett, P. (2008) The exposure of green turtles (Chelonia mydas) to tumour promoting compounds produced by the cyanobacterium Lyngbya majuscula and their potential role in the aetiology of fibropapillomatosis. Harmful Algae 7, 114–125.Google Scholar
Balazs, G.H. (1991) Current status of fibropapillomas in the Hawaiian green turtle, Chelonia mydas . In Research plan for marine turtle fibropapilloma. Honololu, HI: US Department of Commerce, National Oceanographic and Atmospheric Administration, National Marine Fisheries Service, pp. 47–51 (NOAA-TM-NMFS-SWFSC-156).Google Scholar
Baptistotte, C. (2007) Caracterização espacial e temporal da fibropapilomatose em tartarugas marinhas da costa brasileira . PhD thesis. Escola Superior de Agricultura Luiz de Queiroz – Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, Brazil.Google Scholar
Castillo, M., González, C. and Miralles, A. (2011) An evaluation method for determination of non-polar pesticide residues in animal fat samples by using dispersive solid-phase extraction clean up and GC-MS. Analytical and Bioanalytical Chemistry 400, 1315–1328.Google Scholar
Chaloupka, M., Work, T.M., Balazs, G.H., Murakawa, S.K.K. and Morris, R. (2008) Cause-specific temporal and spatial trends in green sea turtle strandings in the Hawaiian Archipelago (1982–2003). Marine Biology 154, 887–898.Google Scholar
Ciscato, C.H.P. (2008) Resíduos de praguicidas em amostras de ovo comercializadas na cidade de São Paulo . PhD thesis. Faculdade de Medicina Veterinaria e Zootecnia, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Crain, D.A., Guillete, L.J., Pickford, D.B., Percival, H.F. and Woodward, A.R. (1998) Sex-steroid and thyroid hormone concentrations in juvenile alligators (Alligator mississippiensis) from contaminated and reference lakes in Florida, USA. Environmental Toxicology and Chemistry 17, 446–452.Google Scholar
De Guise, S., Lagacé, A. and Béland, P. (1994) Tumors in St. Lawrence beluga whales (Delphinapterus leucas). Veterinary Pathology 31, 444–449.Google Scholar
De Guise, S., Lagacé, A., Béland, P., Girard, C. and Higgins, R. (1995a) Non-neoplastic lesions in beluga whales (Delphinapterus leucas) and other marine mammals from the St. Lawrence Estuary. Journal of Comparative Pathology 112, 257–271.Google Scholar
De Guise, S., Martineau, D., Béland, P. and Fournier, M. (1995b) Possible mechanisms of action of environmental contaminants on St. Lawrence Beluga Whales (Delphinapterus leucas). Environmental Health Perspectives 103, 73–77.Google Scholar
De Swart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S.H., Van Loveren, H., Vos, J.G., Reijnders, P.J.H. and Osterhaus, A.D.M.E. (1994) Impairment of immune function in harbour seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23, 155–159.Google Scholar
dos Santos, R.G., Martins, A.S., Torezani, E., Baptistotte, C., Farias, J.D., Horta, P.A., Work, T.M. and Balazs, G.H. (2010) Relationship between fibropapollomatosis and environmental quality: a case study with Chelonia mydas off Brazil. Diseases of Aquatic Organisms 89, 87–95.Google Scholar
Ene, A., Su, M., Lemaire, S., Rose, C., Schaff, S., Moretti, R., Lenz, J. and Herbst, L.H. (2005) Distribution of Chelonid fibropapillomatosis associated herpesvirus variants in florida: molecular evidence for infection of turtles following recruitment to neritic developmental habitats. Journal of Wildlife Diseases 41, 489–497.CrossRefGoogle ScholarPubMed
Flint, M., Patterson-Kane, J.C., Limpus, C.J., Work, T.M., Blair, D. and Mills, P.C. (2009a) Postmortem diagnostic investigation of disease in free-ranging marine turtle populations: a review of common pathologic findings and protocols. Journal of Veterinary Diagnosis and Investigation 21, 733–759.Google Scholar
Flint, M., Patterson-Kane, J.C., Mills, P.C. and Limpus, C.J. (2009b) A veterinarian's guide to sea turtle post mortem examination and histological investigation. http://www.uq.edu.au/vetschool/index.html?page5101785.Google Scholar
Foley, A.M., Schroeder, B.A., Redlow, A.E., Fick-Child, K.J. and Teas, W.G. (2005) Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and associations with environmental factors. Journal of Wildlife Diseases 41, 29–41.Google Scholar
Friend, M. and Trainer, D.O. (1970) Polychlorinated byphenil: interaction with duck hepatitis virus. Science 170, 1314–1316.Google Scholar
Gardner, S.C., Pier, M.D., Wesselman, R. and Juárez, J.A. (2003) Organochlorine contaminants in sea turtles from the Eastern Pacific. Marine Pollution Bulletin 46, 1082–1089.Google Scholar
Guillette, L.J. Jr, Brock, J.W., Rooney, A.A. and Woodward, A.R. (1999) Serum concentrations of various environmental contaminants and their relationship to sex steroid concentrations and phallus size in juvenile American alligators. Archives of Environmental Contamination and Toxicology 36, 447–455.Google Scholar
Guillette, L.J. Jr, Gross, T.S., Masson, G.R., Matter, J.M., Percival, H.F. and Woodward, A.R. (1994) Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environmental Health Perspectives 102, 680–688.CrossRefGoogle ScholarPubMed
Hamann, M., Godfrey, M.H., Seminoff, J.A., Arthur, K., Barata, P.C.R., Bjorndal, K.A., Bolten, A.B., Broderick, A.C., Campbell, L.M., Carreras, C., Casale, P., Chaloupka, M., Chan, S.K.F., Coyne, M.S., Crowder, L.B., Diez, C.E., Dutton, P.H., Epperly, S.P., FitzSimmons, N.N., Formia, A., Girondot, M., Hays, G.C., Cheng, I.J., Kaska, Y., Lewison, R., Mortimer, J.A., Nichols, W.J., Reina, R.D., Shanker, K., Spotila, J.R., Tomás, J., Wallace, B.P., Work, T.M., Zbinden, J. and Godley, B.J. (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endangered Species Research 11, 245–269.Google Scholar
Helsel, D.R. (2005) Nondetects and data analysis; statistics for censored environmental data. Hoboken, NJ: John Wiley and Sons.Google Scholar
Herbst, L.H. (1994) Fibropapillomatosis of marine turtles. Annual Review of Fish Diseases 4, 389–425.Google Scholar
Herbst, L.H., Greiner, E.C., Ehrhart, L.M., Bagley, D.A. and Klein, P.A. (1998) Serological association between spirorchidiasis, herpesvirus infection, and fibropapillomatosis in green turtles from Florida. Journal of Wildlife Diseases 34, 496–507.CrossRefGoogle ScholarPubMed
Herbst, L.H., Jacobson, E.R., Klein, P.A., Balazs, G.H., Moretti, R., Brown, T. and Sundenberg, J.P. (1999) Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Veterinary Pathology 36, 551–564.Google Scholar
Herbst, L.H., Jacobson, E.R., Moretti, R., Brown, T., Sunberg, J.P. and Klein, P.A. (1995) Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Diseases of Aquatic Organisms 22, 1–12.Google Scholar
Herbst, L.H. and Klein, P.A. (1995) Green turtle fibropapillomatosis: challenges to assessing the role of environmental cofactors. Environmental Health Perspectives 103, 27–30.Google ScholarPubMed
Hoff, G.L. and Hoff, D.M. (1984) Herpesviruses of reptiles. In Hoff, G.L., Frye, F.L. and Jacobson, E.R. (eds) Diseases of amphibians and reptiles. New York, NY: Plenum Press, pp. 159–167.Google Scholar
Imanishi, J., Nomura, H., Matsubara, M., Kita, M., Won, S-J., Mizutani, T. and Kishida, T. (1980) Effect of polychlorinated biphenyl in viral infections in mice. Infection and Immunity 29, 275–277.Google Scholar
Jacobson, E.R., Buergelt, C., Williams, B. and Harris, R.K. (1991) Herpesvirus in cutaneous fibropapillomas of the green turtle Chelonia mydas . Diseases of Aquatic Organisms 12, 1–6.Google Scholar
Jenssen, B.M., Haugen, O., Sormo, E.G. and Skaare, J.U. (2003) Negative relationship between PCBs and plasma retinol in low-contaminated free-ranging gray seal pups (Halichoerus grypus). Environmental Research 93, 79–87.Google Scholar
Jepson, P.D., Bennett, P.M., Allchin, C.R., Law, R.J., Kuiken, T., Baker, J.R., Rogan, E. and Kirkwood, J.K. (1999) Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. Science of the Total Environment 243/244, 339–348.CrossRefGoogle ScholarPubMed
Keller, J.M. (2013) Exposure to and effects of persistent organic pollutants. In Wyneken, J., Lohmann, K.J. and Musick, J.A. (eds) The biology of sea turtles, volume III. Boca Raton, FL: CRC Press, pp. 285–328.Google Scholar
Keller, J.M., Balazs, G.H., Nilsen, F., Rice, M.R., Work, T.M. and Jensen, B.A. (2014) Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis. Environmental Science and Technology 48, 7807–7816.Google Scholar
Keller, J.M., Kucklick, J.R., Harms, C.A. and McClellan-Green, P.D. (2004a) Organochlorine contaminants in sea turtles: correlations between whole blood and fat. Environmental Toxicology and Chemistry 23, 726–738.Google Scholar
Keller, J.M., Kucklick, J.R., Stamper, M.A., Harms, C.A. and McClellan-Green, P.D. (2004b) Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environmental Health Perspectives 112, 1074–1079.Google Scholar
Keller, J.M., McClellan-Green, P.D., Kucklick, J.R., Keil, D.E. and Peden-Adams, M.M. (2006) Effects of organochlorine contaminants on loggerhead sea turtle immunity: comparison of a correlative field study and vitro exposure experiments. Environmental Health Perspectives 114, 70–76.Google Scholar
Krzystyniak, K., Bernier, J., Hugo, P. and Fournier, M. (1986) Suppression of MHV3 virus-activated macrophages by dieldrin. Biochemical Pharmacology 35, 2577–2586.Google Scholar
Krzystyniak, K., Hugo, P., Flipo, D. and Fournier, M. (1985) Increased susceptibility to mouse hepatitis virus 3 of peritoneal macrophages exposed to dieldrin. Toxicology and Applied Pharmacology 80, 397–408.Google Scholar
Landsberg, J.H., Balazs, G.H., Steidinger, K.A., Baden, D.G., Work, T.M. and Russell, D.J. (1999) The potential role of natural tumor promoters in marine turtle fibropapillomatosis. Journal of Aquatic Animal Health 11, 199–210.Google Scholar
Lazar, B., Maslov, L., Romanic, S.H., Gracan, R., Krauthacker, B., Holcer, D. and Tvrtkovic, N. (2011) Accumulation of organochlorine contaminants in loggerhead sea turtles, Caretta caretta, from the eastern Adriatic Sea. Chemosphere 82, 121–129.Google Scholar
Lee, L. (2013) NADA: non detects and data analysis for environmental data. R package version 1.5–6. http://CRAN.R-project.org/package=NADA.Google Scholar
Magnusson, B. and Örnemark, U. (2014) Eurachem guide: the fitness for purpose of analytical methods – a laboratory guide to method validation and related topics, 2nd edn. ISBN 978-91-87461-59-0. http://www.eurachem.org.Google Scholar
Malarvannan, G., Takahashi, S., Isobe, T., Kunisue, T., Sudaryanto, A., Miyagi, T., Nakamura, M., Yasumura, S. and Tanabe, S. (2011) Levels and distribution of polybrominated diphenyl ethers and organochlorine compounds in sea turtles from Japan. Marine Pollution Bulletin 63, 172–178.Google Scholar
Martineau, D., Lair, S., de Guise, S. and Béland, P. (1995) Intestinal adenocarcinomas in two beluga whales (Delphinapterus leucas) from the estuary of the St. Lawrence River. Canadian Veterinary Journal 36, 563–565.Google Scholar
McKenzie, C., Godley, B.J., Furnes, R.W. and Wells, D.E. (1999) Concentrations and patterns of organochlorine contaminants in marine turtles from Mediterranean and Atlantic waters. Marine Environmental Research 47, 117–135.Google Scholar
McKim, J.M. Jr and Johnson, K.L. (1983) Polychlorinated biphenils and p,p′-DDE in loggerhead and green postyearling Atlantic sea turtles. Bulletin of Environmental Contamination and Toxicology 31, 53–60.Google Scholar
Miao, X-S., Balazs, G.H., Murakawa, S.K.K. and Li, Q.X. (2001) Congener-specific profile and toxicity assessment of PCBs in green turtles (Chelonia mydas) from the Hawaiian Islands. Science of the Total Environment 281, 247–253.Google Scholar
MMA (2006) Development of a national Implementation Plan in Brazil as a first Step to Implement the Stockholm Convention on Persistent Organic Pollutants (POPs). Brasília: Ministério do Meio ambiente, 46 pp.Google Scholar
Orós, J., Gonzáles-Díaz, O.M. and Monagas, P. (2009) High levels of polychlorinated biphenils in tissues of Atlantic turtles stranded in the Canary Islands, Spain. Chemosphere 74, 473–478.Google Scholar
Patrício, A.R., Herbst, L.H., Duarte, A., Vélez-Zuazo, X., Loureiro, N.S., Pereira, N., Tavares, L. and Toranzos, G.A. (2012) Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of General Virology 93, 1035–1045.Google Scholar
R Core Team (2014) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/.Google Scholar
Rossi, S. (2014) Analise da atividade de leucócitos e de bifenilas policloradas aplicada ao estudo da fibropapilomatose em Chelonia mydas (Testudines, Cheloniidae) (Linnaeus 1758). PhD thesis. Escola Superior de Agricultura Luiz de Queiroz – Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, Brazil.Google Scholar
Rybitski, M.J., Hale, R.C. and Musick, J.A. (1995) Distribution of organochlorine pollutants in Atlantic sea turtles. Copeia 2, 379–390.Google Scholar
Santos, A.S.D., Almeida, A.D.P., Santos, A.J.B., Gallo, B.M.G., Giffoni, B., Baptistotte, C., Coelho, C.A., Lima, E.H.S.M., Sales, G., Lopez, G.G., Stahelin, G., Becker, H., Castilhos, J.C., Thomé, J.C.A., Wanderlinde, J., Marcovaldi, M.Â.A.G.D., Mendilaharsu, M.D.L.M.L., Damasceno, M.T., Barata, P.C.R. and Sforza, R. (2011) Informações gerais. In Marcovaldi, M.A.A.G.D., Santos, A.S. and Sales, G. (eds) Plano de Ação Nacional para a Conservação das Tartarugas Marinhas. Brasília: Instituto Chico Mendes de Conservação da Biodiversidade, ICMBio, pp. 48–55 (Série Espécies Ameaçadas no. 25.).Google Scholar
Santos-Neto, E., Azevedo-Silva, C.E., Bisi, T.L., Santos, J., Meirelles, A.C.O., Carvalho, V.L., Azevedo, A.F., Guimarães, J.E. and Lailson-Brito, J. (2014) Organochlorine concentrations (PCBs, DDTs, HCHs, HCB and MIREX) in delphinids stranded at the northeastern Brazil. Science of the Total Environment 472, 194–203.Google Scholar
Seminoff, J.A. (2004) Chelonia mydas. http://www.iucnredlist.org/details/4615/0 (12 January 2012).Google Scholar
Silva, J.D. (2009) Ocorrência de pesticidas organoclorados e bifenilos policlorados em tartarugas marinhas Chelonia mydas. Master thesis. Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Smith, G.M. and Coates, C.W. (1938) Fibro-epithelial growths in the skin in large marine turtles Chelonia mydas . Zoologica 23, 93–98.Google Scholar
Tanabe, S., Subramanian, A.N., Ramesh, A., Kumaran, P.L., Miyazaki, N. and Tatsukawa, R. (1993) Persistent organochlorine residues in dolphins from the Bay of Bengal, south India. Marine Pollution Bulletin 26, 311–316.Google Scholar
Taquet, C., Taquet, M., Dempster, T., Soria, M., Ciccione, S., Roos, D. and Dagorn, L. (2006) Foraging of the green sea turtle Chelonia mydas on seagrass beds at Mayotte Island (Indian Ocean), determined by acoustic transmitters. Marine Ecology Progress Series 306, 295–302.Google Scholar
van de Merwe, J.P., Hodge, M., Olszowy, H.A., Whittier, J.M. and Lee, S.Y. (2010) Using blood samples to estimate persistent organic pollutants and metals in green sea turtles (Chelonia mydas). Marine Pollution Bulletin 60, 579–588.Google Scholar
Van Houtan, K.S., Hargrove, S.K. and Balazs, G.H. (2010) Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS ONE 5, e12900. doi: 10.1371/jornal.pone.0012900.Google Scholar
Weisburger, E.K. (1989) Chemical carcinogenesis in experimental animals and humans. In Sirica, A.E. (ed.) The pathobiology of neoplasia. New York, NY: Plenum Press, pp. 39–56.Google Scholar
Woodward, A.R., Percival, H.F., Jennings, M.L. and Moore, C.T. (1993) Low clutch viability of American alligators on Lake Apopka. Florida Scientist 56, 52–63.Google Scholar
Work, T.M. and Balazs, G.H. (1997) Causes of green turtle (Chelonia mydas) morbidity and mortality in Hawaii. In Epperly, S.S. and Braun, J. (eds) Proceedings of the Seventeenth Annual Sea Turtle Symposium, Orlando, Florida, USA, 4–8 March. National Oceanographic and Atmospheric Administration, pp. 308–309. (NOAA-TM-NMFS-SEFSC-415).Google Scholar
Yogui, G.T., Santos, M.C.O., Bertozzi, C.P. and Montone, R.C. (2010) Levels of persistent organic pollutants and residual pattern of DDTs in small cetaceans from the coast of São Paulo, Brazil. Marine Pollution Bulletin 60, 1862–1867.Google Scholar