, Volume 40, Issue 4, pp 425–430 | Cite as

DDT Strikes Back: Galapagos Sea Lions Face Increasing Health Risks

  • Juan José Alava
  • Sandie Salazar
  • Marilyn Cruz
  • Gustavo Jiménez-Uzcátegui
  • Stella Villegas-Amtmann
  • Diego Paéz-Rosas
  • Daniel P. Costa
  • Peter S. Ross
  • Michael G. Ikonomou
  • Frank A.P.C. Gobas


Dichlorodiphenyltrichloroethane (DDT) is an effective and relatively cheap anti-malaria pesticide which has saved human lives, but also brought Northern wildlife species to the brink of extinction due to its persistence, bioaccumulation in the food-web, and hormone-mimicking characteristics (Carson 1962; Vallack et al. 1998; UNEP 2001; ATSDR 2002; Blus 2003; WHO 2006; Colborn and Carroll 2007; Van den Berg 2008). Thirty-two years after its ban in the US and its inclusion on Schedule 2 of the UN Stockholm Convention on Persistent Organic Pollutants (POPs) because of its damaging health effects in human and wildlife populations (UNEP 2001; ATSDR 2002; WHO 2006; Vallack et al. 1998; Colborn and Carroll 2007; Blus 2003), the WHO has recommitted to the use of the malaria-fighting pesticide DDT in tropical countries because of an increase in malaria cases in tropical countries (e. g., Peru, Bolivia, Paraguay, Brazil, and African nations), where DDT use was halted or low...


Malaria Killer Whale Galapagos Island Southern Elephant Seal Western Antarctic Peninsula 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to the volunteers from the Marine Mammal Center in Santa Barbara (CA, USA) for supporting the cruise expedition and their expertise in sea lion capture. We thank P. Martinez, A. Paras, G. Merlen, and the Galapagos National Park rangers for their assistance during the sampling. The field sampling was possible thanks to the Project Health Status, Genetic and Rescue Techniques of Galapagos Pinnipeds of the Charles Darwin Foundation, and the Galapagos National Park Service. This work is part of the contribution number 2007 of the Charles Darwin Foundation. The export permit of the samples was authorized by the Galapagos National Park.


  1. Alava, J.J., and S. Salazar. 2006. Status and conservation of Otariids in Ecuador and the Galapagos Islands. In Sea lions of the world, ed. A.W. Trites, S.K. Atkinson, D.P. DeMaster, L.W. Fritz, T.S. Gelatt, L. D. Rea, and K.M. Wynne, 495–519. Fairbanks: Alaska Sea Grant College Program, University of Alaska Fairbanks.Google Scholar
  2. Alava, J.J. 2009. Carbon productivity and flux in the marine ecosystems of the Galapagos Marine Reserve based on cetacean abundances and trophic indices. Revista de Biología Marina y Oceanografía 44: 109–122.CrossRefGoogle Scholar
  3. Alava, J.J., S. Salazar, G. Jiménez-Uzcategui, M. Cruz, D. Páez-Rosas, P. Calle, J. Denkinger, P.S. Ross, M. Ikonomou, and F. Gobas. 2010. Biomagnificación de Contaminantes Orgánicos Persistentes (COPs) en el Lobo Marino de Galápagos (Zalophus wolleabeki): Implicaciones para la conservación de la Biodiversidad Marina. 1er Simposio Latinoamericano de Biodiversidad Marina y Costera de Latinoamérica y El Caribe, y 2do Simposio Ecuatoriano de Biodiversidad Marino Costera. Ministerio del Ambiente, Ecuador; Grupo de Trabajo sobre Biodiversidad Marino y Costera del Ecuador. 9–12 Diciembre, 2010, Manta, Ecuador.Google Scholar
  4. Alava, J.J. 2011. Bioaccumulation of pollutants in Galapagos sea lions and marine mammals from British Columbia, Canada. PhD Thesis, School of Resource and Environmental Management, Faculty of Environment, Simon Fraser University, BC, Canada.Google Scholar
  5. Alava, J.J., M.G. Ikonomou, P.S. Ross, D. Costa, S. Salazar, and F.A.P.C. Gobas. 2009. Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in Galapagos sea lions (Zalophus wollebaeki). Environmental Toxicology and Chemistry 28: 2271–2282.CrossRefGoogle Scholar
  6. Alava, J.J., P.S. Ross, M.G., Ikonomou, M. Cruz, G. Jimenez-Uzcategui, S. Salazar, D.P. Costa, S. Villegas-Amtmann, P. Howorth, and F.A.P.C. Gobas. 2011. DDT in endangered Galapagos Sea Lions (Zalophus wollebaeki) from eight rookeries in the Galapagos Islands. Marine Pollution Bulletin (accepted). Google Scholar
  7. ATSDR (Agency for Toxic Substances and Disease Registry). 2002. Toxicological profile for DDT, DDE, DDD, 403. Atlanta, Georgia: Division of Toxicology/Toxicology Information Branch, U.S. Department of Health and Human Services, Public Health Service.Google Scholar
  8. Azeredo, A., J.P.M. Torres, M. de Freitas Fonseca, J.L. Britto, W.R. Bastos, C.E. Azevedo e Silva, G. Cavalcanti, R.O. Meire, et al. 2008. DDT and its metabolites in breast milk from the Madeira River basin in the Amazon, Brazil. Chemosphere 73: S246–S251.Google Scholar
  9. Blasius, M.E., and G.D. Goodmanlowe. 2008. Contaminants still high into-level carnivores in the Southern California Bight: Levels of DDT and PCBs in resident and transient pinnipeds. Marine Pollution Bulletin 56: 1973–1982.CrossRefGoogle Scholar
  10. Blus, L.J. 2003. Organochlorine pesticides. In Handbook of ecotoxicology, ed. D.J. Hoffman, B.A. Rattner, G.A. Burton, and J. Cairns, 313–339. Boca Raton: CRC Press.Google Scholar
  11. Carson, R. 1962. Silent spring. Boston: Houghton Mifflin Company.Google Scholar
  12. Colborn, T., and L.E. Carroll. 2007. Pesticides, sexual development, reproduction, and fertility: Current perspective and future direction. Human and Ecological Risk Assessment 13: 1078–1110.CrossRefGoogle Scholar
  13. De Guise, S., D. Martineau, P. Beland, and M. Fournier. 1998. Effects of in vitro exposure of beluga whale leukocytes to selected organochlorines. Journal of Toxicology and Environmental Health, Part A 55: 479–493.CrossRefGoogle Scholar
  14. Debier, C., G.M. Ylitalo, M. Weise, F. Gulland, D.P. Costa, B.J. Le Boeuf, T. de Tillesse, and Y. Larondelle. 2005. PCBs and DDT in the serum of juvenile California sea lions: Associations with vitamins A and E and thyroid hormones. Environmental Pollution 134: 323–332.CrossRefGoogle Scholar
  15. Del Toro, L., G. Heckel, V.F. Camacho-Ibar, and Y. Schramm. 2006. California sea lions (Zalophus californianus californianus) have lower chlorinated hydrocarbon contents in northern Baja California, Mexico, than in California, USA. Environmental Pollution 142: 83–92.Google Scholar
  16. Denholm, I., G.J. Devine, and M.S. Williamson. 2002. Insecticide resistance on the move. Science 297: 2222–2223.CrossRefGoogle Scholar
  17. Geisz, H.N., R.M. Dickhut, M.A. Cochran, W.R. Fraser, and H.W. Ducklow. 2008. Melting glaciers: A probable source of DDT to the Antarctic Marine Ecosystem. Environmental Science and Technology 42: 3958–3962.CrossRefGoogle Scholar
  18. Guglielmo, F., G. Lammel, and E. Maier-Reimer. 2009. Global environmental cycling of gamma-HCH and DDT in the 1980s—a study using a coupled atmosphere and ocean general circulation model. Chemosphere 76: 1509–1517.Google Scholar
  19. Guillette Jr., L. J., T.S. Gross, G.R. Masson, J.M. Matter, H.F. Percival, and A.R. Woodward. 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.Google Scholar
  20. Hickey, J.J., and D.W. Anderson. 1968. Chlorinated hydrocarbons and eggshell changes in raptorial and fish-eating birds. Science 162: 271–273.CrossRefGoogle Scholar
  21. Iwata, H., S. Tanabe, N. Sakai, A. Nishimura, and R. Tatsukawa. 1994. Geographical distribution of persistent organochlorines in air, water and sediments from Asia and Oceania, and their implications for global redistribution from lower latitudes. Environmental Pollution 85: 15–33.CrossRefGoogle Scholar
  22. Kajiwara, N., K. Kannan, M. Muraoka, M. Watanabe, S. Takahashi, F. Gulland, H. Olsen, A.L. Blankenship, P.D. Jones, S. Tanabe, and J.P. Giesy. 2001. Organochlorine pesticides, polychlorinated biphenyls, and butyltin compounds in blubber and livers of stranded California sea lions, Elephant Seals, and harbor seals from coastal California, USA. Archives of Environmental Contamination and Toxicology 41: 90–99.CrossRefGoogle Scholar
  23. Kannan, K., N. Kajiwara, B.J. Le Boeuf, and S. Tanabe. 2004. Organochlorine pesticides and polychlorinated biphenyls in California sea lions. Environmental Pollution 131: 425–434.CrossRefGoogle Scholar
  24. Kelce, W.R., C.R. Stone, S.C. Laws, L.E. Gray, J.A. Kemppainen, and E.M. Wilson. 1995. Persistent DDT metabolite p,p-DDE is a potent androgen receptor antagonist. Nature 375: 581–585.CrossRefGoogle Scholar
  25. Kunisue, T., M. Muraoka, M. Ohtake, A. Sudaryanto, N.H. Minh, D. Ueno, Y. Higaki, M. Ochi, et al. 2006. Contamination status of persistent organochlorines in human breast milk from Japan: Recent levels and temporal trend. Chemosphere 64: 1601–1608.CrossRefGoogle Scholar
  26. Lahvis, G.P., R.S. Wells, D.W. Kuehl, J.L. Stewart, H.L. Rhinehart, and C.S. Via. 1995. Decreased lymphocyte responses in free-ranging bottlenose dolphins (Tursiops truncatus) are associated with increased concentrations of PCBs and DDT in peripheral blood. Environ. Health Perspectives 103: 67–72.CrossRefGoogle Scholar
  27. Miranda-Filho, K.C., T.L. Metcalfe, C.D. Metcalfe, R.B. Metcalfe, R.B. Robaldo, M.M.C. Muelbert, E.P. Colares, P.E. Martinez, and A. Bianchini. 2007. Residues of persistent organochlorine contaminants in Southern Elephant Seals (Mirounga leonina) from Elephant Island, Antarctica. Environmental Science and Technology 41: 3829–3835.CrossRefGoogle Scholar
  28. Mos, L., M. Cameron, S.J. Jeffries, B.F. Koop, and P.S. Ross. 2010. Risk-based analysis of PCB toxicity in harbor seals. Integrated Environmental Assessment and Management 6: 631–640.CrossRefGoogle Scholar
  29. Roberts, D.R., L.L. Laughlin, P. Hsheih, and Ll.J. Legters. 1997. DDT, global strategies, and a malaria control crisis in South America. Emerging Infectious Diseases 3: 295–302.CrossRefGoogle Scholar
  30. Roberts, D.R., S. Manguin, and J. Mouchet. 2000. DDT house spraying and re-emerging malaria. Lancet 356: 330–332.CrossRefGoogle Scholar
  31. Torres, J.P.M., J. Lailson-Brito, G.C. Saldanha, P. Dorneles, C.E.A. Silva, O. Malm, J.R. Guimarães, A. Azeredo, et al. 2009. Persistent toxic substances in the Brazilian Amazon: Contamination of man and the environment. Journal of the Brazilian Chemical Society 20: 1175–1179.CrossRefGoogle Scholar
  32. UNEP (United Nations Environment Program). 2001. Final act of the conference of plenipotentiaries on the Stockholm convention on persistent organic pollutants, 44. Stockholm, Sweden/Geneva, Switzerland: UNEP/POPS/CONF/4UNEP.Google Scholar
  33. Vallack, H.W., D.J. Bakker, I. Brandt, E. Broström-Lundén, A. Brouwer, K.R. Bull, C. Gough, R. Guardans, et al. 1998. Controlling persistent organic pollutants—what next? Environmental Toxicology and Pharmacology 6: 143–175.CrossRefGoogle Scholar
  34. Van den Berg, H. 2008. Global status of DDT and its alternatives for use in vector control to prevent disease, 31. Geneva, Switzerland: Stockholm Convention on Persistent Organic Pollutants, United Nations Environment Programme, UNEP/POPS/DDTBP.1/2.Google Scholar
  35. Vargas, F.H., R.C. Lacy, P.J. Johnson, A. Steinfurth, R.J.M. Crawford, P.D. Boersma, and D.W. Macdonald. 2007. Modelling the effect of El Niño on the persistence of small populations: The Galápagos penguin as a case study. Biological Conservation 137: 138–148.CrossRefGoogle Scholar
  36. Watkins, G., and F. Cruz. 2007. Galapagos at risk: A socioeconomic analysis of the situation in the Archipelago, 21. Puerto Ayora, Province of Galapagos, Ecuador: Charles Darwin Foundation.Google Scholar
  37. WHO. (World Health Organization). 2006. WHO gives indoor use of DDT a clean bill of health for controlling malaria: WHO promotes indoor residual spraying with insecticides as one of three main interventions to fight malaria. 15 September 2006. World Health Organization, Washington, DC. Accessed 19 Oct 2008.
  38. Wilkening, K.E., L.A. Barrie, and M. Engle. 2000. Trans-Pacific air pollution. Science 290: 65–66.CrossRefGoogle Scholar
  39. Ylitalo, G.M., J.E. Stein, T. Hom, L.L. Johnson, K.L. Tilbury, A.J. Hall, T. Rowles, D. Greig, L.J. Lowenstine, and F.M.D. Gulland. 2005. The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus). Marine Pollution Bulletin 50: 30–39.Google Scholar
  40. Ylitalo, G.M., M. Myers, B.S. Stewart, P.K. Yochem, R. Braun, L. Kashinsky, D. Boyd, G.A. Antonelis, S. Atkinson, A.A. Aguirre, and M.M. Krahn. 2008. Organochlorine contaminants in endangered Hawaiian monk seals from four subpopulations in the Northwestern Hawaiian Islands. Marine Pollution Bulletin 56: 231–244.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2011

Authors and Affiliations

  • Juan José Alava
    • 1
    • 2
  • Sandie Salazar
    • 3
  • Marilyn Cruz
    • 4
  • Gustavo Jiménez-Uzcátegui
    • 3
  • Stella Villegas-Amtmann
    • 5
  • Diego Paéz-Rosas
    • 7
  • Daniel P. Costa
    • 5
  • Peter S. Ross
    • 6
  • Michael G. Ikonomou
    • 6
  • Frank A.P.C. Gobas
    • 1
  1. 1.School of Resource & Environmental ManagementSimon Fraser University 8888BurnabyCanada
  2. 2.Fundacion Ecuatoriana para el Estudio de Mamíferos Marinos (FEMM)GuayaquilEcuador
  3. 3.Charles Darwin FoundationQuitoEcuador
  4. 4.Galápagos Genetics Epidemiology and Pathology Laboratory (GGEPL)Puerto Ayora, Galápagos IslandsEcuador
  5. 5.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaSanta CruzUSA
  6. 6.Institute of Ocean Sciences, Fisheries and Oceans CanadaSidneyCanada
  7. 7.Centro Interdisciplinario de Ciencias MarinasInstituto Politécnico NacionalLa PazMexico

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