A Comparative Analysis of Polybrominated Diphenyl Ethers and Polychlorinated Biphenyls in Southern Sea Otters that Died of Infectious Diseases and Noninfectious Causes

  • Kurunthachalam Kannan
  • Emily Perrotta
  • Nancy J. Thomas
  • Kenneth M. Aldous


Southern sea otters (Enhydra lutris nereis) from the California coast continue to exhibit a slower population regrowth rate than the population in Alaska. Infectious diseases have been identified as a frequent cause of death. Infectious diseases caused by varied pathogens including bacteria, fungi, and parasites were suggestive of compromised immunological health of mature animals in this population. To test the hypothesis that elevated exposure to immunotoxic contaminants such as polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) contribute to disease susceptibility via immunosuppression, we determined concentrations of PBDEs and PCBs in livers of 80 adult female sea otters that died of infectious diseases, noninfectious causes, or emaciation. Concentrations of PBDEs and PCBs in sea otter livers varied widely (10–26,800 ng/g and 81–210,000 ng/g, lipid weight, respectively). Concentrations of PBDEs in sea otters were some of the highest values reported for marine mammals so far. Although PCB concentrations in sea otters have declined during 1992–2002, the mean concentration was at the threshold at which adverse health effects are elicited. Concentrations of PBDEs and PCBs were significantly correlated, suggesting co-exposure of these contaminants in sea otters. No significant association was found between the concentrations of PBDEs and the health status of sea otters. Concentrations of PCBs were significantly higher in otters in the infectious disease category than in the noninfectious category, suggesting an association between elevated PCB concentrations and infectious diseases in Southern sea otters.



This study was funded by a grant from the Monterey Bay Sanctuary Foundation.


  1. Bacon CE, Jarman WM, Estes JA, Simon M, Norstrom R (1999) Comparison of organochlorine contaminants among sea otter (Enhydra lutris) populations in California and Alaska. Environ Toxicol Chem 18:452–458CrossRefGoogle Scholar
  2. Beineke A, Siebert U, Mclachlan M, Bruhn R, Thron K, Failing K, Muller G, Baumgartner W (2005) Investigations of the potential influence of environmental contaminants on the thymus and spleen of harbor porpoises (Phocoena phocoena). Environ Sci Technol 39:3933–3938CrossRefGoogle Scholar
  3. Brown FR, Winkler J, Visita P, Dhaliwal J, Petreas M (2006) Levels of PBDEs, PCDDs, PCDFs and coplanar PCBs in edible fish from California coastal waters. Chemosphere 64:276–286CrossRefGoogle Scholar
  4. California Department of Fish and Game (CDFG) (2001) Sea otter. California’s living marine resources, a status report. Available at http://www.dfg.ca.gov/mrd/status/sea_otter.pdf
  5. DeMaster DP, Marzin C, Jameson RJ (1996) Estimating the historical abundance of sea otters in California. Endangered Species Update 13:79–81Google Scholar
  6. De Swart RL, Ross PS, Vos JG, Osterhaus ADME (1996) Impaired immunity in harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a long-term feeding study. Environ Health Perspect 104:823–828CrossRefGoogle Scholar
  7. Estes JA (1990) Growth and equilibrium in sea otter populations. J Anim Ecol 59:385–401CrossRefGoogle Scholar
  8. Estes JA, Hatfield BB, Ralls K, Ames J (2003) Causes of mortality in California sea otters during periods of population growth and decline. Mar Mamm Sci 19:198–216CrossRefGoogle Scholar
  9. Fowles JR, Fairbrother A, Baecher-Steppan L, Kerkvliet NI (1994) Immunologic and endocrine effects of the flame retardant pentabromodiphenyl ether (DE-71) in C57BL/6J mice. Toxicol 26:49–61CrossRefGoogle Scholar
  10. Hall AJ, Hugunin K, Deaville R, Law RJ, Allchin CR, Jepson PD (2006) The risk of infection from polychlorinated biphenyl exposure in the harbor porpoise (Phocoena phocoena): a case-control approach. Environ Health Perspect 114:704–711CrossRefGoogle Scholar
  11. Hanni KD, Mazet JAK, Gulland FMD, Estes J, Staedler M, Murray MJ, Miller M, Jessup DA (2003) Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters. J Wildlife Dis 39:837–850Google Scholar
  12. Hites RA (2004) Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environ Sci Technol 38:945–956CrossRefGoogle Scholar
  13. Ikonomou MG, Rayne S, Addison RF (2002) Exponential increases of the brominated flame retardants, polybrominated diphenyl ethers, in the Canadian arctic from 1981 to 2000. Environ Sci Technol 36:1886–1892CrossRefGoogle Scholar
  14. Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ (2005) Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environ Toxicol Chem 24:238–348CrossRefGoogle Scholar
  15. Johnson-Restrepo B, Kannan K, Addink R, Adams DH (2005a) Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in a pelagic foodweb of Florida coastal waters. Environ Sci Technol 39:8243–8250CrossRefGoogle Scholar
  16. Johnson-Restrepo B, Kannan K, Rapaport DP, Rodan BD (2005b) Polybrominated diphenyl ethers and polychlorinated biphenyls in human adipose tissue from New York. Environ Sci Technol 39:5177–5182CrossRefGoogle Scholar
  17. Kajiwara N, Kannan K, Muraoka M, Watanabe M, Takahasi S, Gulland F, Olsen H, Blankenship AL, Jones PD, Tanabe S, Giesy JP (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. Arch Environ Contam Toxicol 41:90–99CrossRefGoogle Scholar
  18. Kajiwara N, Ueno D, Takahashi A, Baba N, Tanabe S (2004) Polybrominated diphenyl ethers and organochlorines in archived northern fur seal samples from the Pacific coast of Japan, 1972-1998. Environ Sci Technol 38:3804–3809CrossRefGoogle Scholar
  19. Kajiwara N, Kamikawa S, Ramu K, Ueno D, Yamada TK, Subramanian A, Lam PKS, Jefferson TA, Prudente M, Chung K-H, Tanabe S (2006) Geographical distribution of polybrominated diphenyl ethers (PBDEs) and organochlorines in small cetaceans from Asian waters. Chemosphere 64:287–295CrossRefGoogle Scholar
  20. Kannan K, Tanabe S, Borrell A, Aguilar A, Focardi S, Tatsukawa R (1993) Isomer-specific analysis and toxic evaluation of PCBs in striped dolphins affected by an epizootic in the western Mediterranean Sea. Arch Environ Contam Toxicol 25:227–233CrossRefGoogle Scholar
  21. Kannan K, Guruge KS, Thomas NJ, Tanabe S, Giesy JP (1998) Butyltin residues in southern sea otters (Enhydra lutris nereis) found dead along California coastal waters. Environ Sci Technol 32:1169–1175CrossRefGoogle Scholar
  22. Kannan K, Blankenship AL, Jones PD, Giesy JP (2000) Toxicity reference values for the toxic effects of polychlorinated biphenyls to aquatic mammals. Hum Ecol Risk Assess 6:181–201CrossRefGoogle Scholar
  23. Kannan K, Kajiwara N, Watanabe M, Nakata H, Thomas N, Stephenson M, Jessup DA, Tanabe S (2004a) Profiles of polychlorinated biphenyl congeners, organochlorine pesticides, and butyltins in southern sea otters and their prey. Environ Toxicol Chem 23:49–56CrossRefGoogle Scholar
  24. Kannan K, Kajiwara N, Le Boeuf BJ, Tanabe S (2004b) Organochlorine pesticides and polychlorinated biphenyls in California sea lions. Environ Pollut 131:425–434CrossRefGoogle Scholar
  25. Kannan K, Ramu K, Kajiwara N, Sinha RK, Tanabe S (2005a) Organochlorine pesticides, polychlorinated biphenyls and polybrominated diphenyl ethers in Irrawaddy dolphins from India. Arch Environ Contam Toxicol 49:415–420CrossRefGoogle Scholar
  26. Kannan K, Yun SH, Evans TJ (2005b) Chlorinated, brominated and perfluorinated contaminants in livers of polar bears from Alaska. Environ Sci Technol 39:9057–9063CrossRefGoogle Scholar
  27. Kannan K, Reiner JL, Yun S-H, Perrotta EE, Tao L, Johnson-Restrepo B, Rodan BD (2005c) Polycyclic musk compounds in higher trophic level aquatic organisms and humans from the United States. Chemosphere 61:693–700CrossRefGoogle Scholar
  28. Kannan K, Perrotta E, Thomas NJ (2006a) Association between perfluorinated compounds and pathological conditions in southern sea otters. Environ Sci Technol 40:4943–4948CrossRefGoogle Scholar
  29. Kannan K, Agusa T, Perrotta E, Thomas NJ, Tanabe S (2006b) Comparison of trace-element concentrations in livers of diseased, emaciated, and non-diseased southern sea otters from the California coast. Chemosphere 65:2160–2167CrossRefGoogle Scholar
  30. Kreuder C, Miller MA, Jessup DA, Lowenstine LJ, Harris MD, Ames JA, Carpenter TE, Conrad PA, Mazet JAK (2003) Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001. J Wildlife Dis 39:495–509Google Scholar
  31. Lahvis GP, Wells RS, Kuehl DW, Stewart JL, Rhinehart HL, Via CS (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 Perspect 103:67–72CrossRefGoogle Scholar
  32. Law RJ, Allchin CR, Mead LK (2005) Brominated diphenyl ethers in the blubber of twelve species of marine mammals stranded in the UK. Mar Pollut Bull 50:344–359CrossRefGoogle Scholar
  33. Law RJ, Allchin CR, Bennett ME, Morris S, Rogan E (2002) Polybrominated diphenyl ethers in two species of marine top predators from England and Wales. Chemosphere 46:673–681CrossRefGoogle Scholar
  34. Lebeuf M, Gouteux B, Measures L, Trottier S (2004) Levels and temporal trends (1988-1999) of polybrominated diphenyl ethers in beluga whales (Delphinapterus leucas) from the St. Lawrence estuary, Canada. Environ Sci Technol 38:2971–2977Google Scholar
  35. Loganathan BG, Kannan K (1994) Global organochlorine contamination trends: an overview. Ambio 23:187–191Google Scholar
  36. Muir DCG, Backus S, Derocher AE, Dietz R, Evans TJ, Gabrielsen GW, Nagy J, Norstrom RJ, Sonne C, Stirling I, Taylor MK, Letcher RJ (2006) Brominated flame retardants in polar bears (Ursus maritimus) from Alaska, the Canadian Arctic, East Greenland and Svalbard. Environ Sci Technol 40:449–455CrossRefGoogle Scholar
  37. Nakata H, Kannan K, Jing L, Thomas N, Tanabe S, Giesy JP (1998) Accumulation patterns of organochlorine pesticides and polychlorinated biphenyls in southern sea otters (Enhydra lutris nereis) found stranded along coastal California, USA. Environ Pollut 103:45–53CrossRefGoogle Scholar
  38. Oros DR, Hoover D, Rodigari F, Crane D, Sericano J (2005) Levels and distribution of polybrominated diphenyl ethers in water, surface sediments, and bivalves from the San Francisco Estuary. Environ Sci Technol 39:33–41CrossRefGoogle Scholar
  39. Otter Project (2005) available at http://www.otterproject.org
  40. Pattersson A, van Bavel B, Engwall M, Jimenez B (2004) Polybrominated diphenyl ethers and methoxylated tetrabromodiphenylethers in cetaceans from the Mediterranean Sea. Arch Environ Contam Toxicol 47:542–550CrossRefGoogle Scholar
  41. Perrotta E (2005) Concentrations of effects of environmental contaminants on the health of California sea otters. Master’s thesis, State University of New York at Albany, New YorkGoogle Scholar
  42. Ramu K, Kajiwara N, Tanabe S, Lam PKS, Jefferson TA (2005) Polybrominated diphenyl ethers (PBDEs) and organochlorines in small cetaceans from Hong Kong waters: levels, profiles and distribution. Mar Pollut Bull 51:669–676CrossRefGoogle Scholar
  43. Schwartz J, Aldridge B, Blanchard M, Mohr FC, Stott J (2005) The development of methods for immunophenotypic and lymphocyte function analyses for assessment of southern sea otter (Enhydra lutris nereis) health. Vet Immunol Immunopathol 104:1–14CrossRefGoogle Scholar
  44. Shapiro ED (1989) Analytic strategies in hospital epidemiology: case-control studies. Infect Control Hosp Epidemiol 10:167–169CrossRefGoogle Scholar
  45. She J, Petreas M, Winkler J, Visita P, McKinney M, Kopec D (2002) PBDEs in the San Francisco Bay area: measurements in harbor seal blubber and human breast adipose tissue. Chemosphere 46:697–707CrossRefGoogle Scholar
  46. Stapleton HM, Dodder NG, Kucklick JR, Reddy CM, Schantz MM, Becker PR, Gulland F, Porter BJ, Wise SA (2006) Determination of HBCD, PBDEs and MeO-BDEs in California sea lions (Zalophus californianus) stranded between 1993 and 2003. Mar Pollut Bull 52:522–531CrossRefGoogle Scholar
  47. Thomas NJ, Cole RA (1996) The risk of disease and threats to the wild population. Endangered Species Update 13:24–28Google Scholar
  48. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Kurunthachalam Kannan
    • 1
  • Emily Perrotta
    • 1
  • Nancy J. Thomas
    • 2
  • Kenneth M. Aldous
    • 1
  1. 1.Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, School of Public HealthState University of New York at AlbanyNew YorkUSA
  2. 2.US Geological Survey-Biological Resources DivisionNational Wildlife Health CenterMadisonUSA

Personalised recommendations