, Volume 9, Issue 3, pp 267–277 | Cite as

Mercury Concentrations in Hair from Neonatal and Juvenile Steller Sea Lions (Eumetopias jubatus): Implications Based on Age and Region in this Northern Pacific Marine Sentinel Piscivore

  • J. Margaret CastelliniEmail author
  • Lorrie D. Rea
  • Camilla L. Lieske
  • Kimberlee B. Beckmen
  • Brian S. Fadely
  • John M. Maniscalco
  • Todd M. O’Hara
Original Contribution


Mercury is a global contaminant of concern for the fetus and the neonate of piscivores. Methylmercury, produced within marine ecosystems, is of particular concern as a readily absorbed neurotoxicant transported across the blood brain barrier and transplacentally. In the North Pacific Ocean, Steller sea lions are broadly distributed apex predators and, as such, integrate complex food webs and the associated exposure and possible adverse effects of toxic and infectious agents. Hair, including lanugo, was examined using regional and age groupings to assess mercury concentrations in young Alaskan Steller sea lions. The highest concentrations of mercury occurred in the youngest animals, likely via in utero exposure. Based on the adverse developmental outcomes of methylmercury toxicity this specific cohort is of concern. Regionally, higher concentrations of mercury were observed in the endangered western population of Steller sea lions and mirrored patterns observed in human biomonitoring studies of Alaskan coastal communities. These data have broader implications with respect to human and ecosystem health as Steller sea lions rely on similar prey species and foraging areas as those targeted by commercial fisheries and subsistence users and are therefore valuable sentinels of marine ecosystem health.


mercury methylmercury hair neonate pup marine sentinel Steller sea lion toxicology ecotoxicology ecosystem health 



We thank the field research teams of both the Alaska Department of Fish and Game and the National Marine Mammal Laboratory (NMFS/NOAA), the staff of the Alaska SeaLife Center (ASLC), and the crews of the R/V Medeia, P/V Stimson, P/V Wolstad, R/V Tiglax, M/V Pacific Star, and the R/V Norseman. We thank Darce Holcomb of the Wildlife Toxicology Laboratory, University of Alaska Fairbanks, for assistance with sample analysis and Tom Gelatt of the National Marine Mammal Laboratory for providing manuscript comments. Funding has been provided through NOAA Cooperative Agreements NA17FX1079, NA04NMF4390170, and NA07NMF4390312. In addition, this publication was made possible by Grant Number 5P20RR016466 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH). Sample collection described here was part of ongoing Steller sea lion research conducted by the Alaska Department of Fish and Game, The National Marine Mammal Laboratory and the Alaska SeaLife Center under MMPA permits #358-1564, 358-1769, 358-1888, 782-1889, and 881-18900-02 and under ADFG ACUC #03-002 and #06-07 and ASLC IACUC Protocol 07-001.


  1. Aguirre AA, Tabor GM (2004) Introduction: Marine vertebrates as sentinels of marine ecosystem health. EcoHealth 1:236-238.Google Scholar
  2. Airey D (1983) Mercury in human hair due to environment and diet: A review. Environmental Health Perspectives 52:303-316.PubMedCrossRefGoogle Scholar
  3. Anderson PJ, Piatt JF (1999) Community reorganization in the Gulf of Alaska following ocean climate regime shift. Marine Ecology Progress Series 189:117-123.CrossRefGoogle Scholar
  4. Ashwell-Erickson S, Fay FH, Elsner R, Wartzok D (1986) Metabolic and hormonal correlates of molting and regeneration of pelage in Alaskan harbor and spotted seals (Phoca vitulina and Phoca largha). Canadian Journal of Zoology 64:1086-1094.CrossRefGoogle Scholar
  5. Basu N, Scheuhammer AM, Sonne C, Letcher RJ, Born EW, Dietz R (2009) Is dietary mercury of neurotoxicological concern to wild polar bears (Ursus maritimus)? Environmental Toxicology and Chemistry 28:133-140.PubMedCrossRefGoogle Scholar
  6. Beckmen KB, Duffy LK, Zhang X, Pitcher KW (2002) Mercury concentrations in the fur of Steller sea lions and northern fur seals from Alaska. Marine Pollution Bulletin 44:1130-135.PubMedCrossRefGoogle Scholar
  7. Bemis JC, Seegal RF (1999) Polychlorinated biphenyls and methylmercury act synergistically to reduce rat brain dopamine content in vitro. Environmental Health Perspectives 107:879-885.PubMedCrossRefGoogle Scholar
  8. Bickham JW, Patton JC, Loughlin TR (1996) High variability for control region sequences in a marine mammal: Implications for conservation and biogeography of Steller sea lions. Journal of Mammalogy 77:95-108.CrossRefGoogle Scholar
  9. Bossart GD (2006) Marine mammals as sentinel species for oceans and human health. Oceanography 19 (2):134-137.CrossRefGoogle Scholar
  10. Brookens TJ, Harvey JT, O’Hara T (2007) Trace element concentrations in the Pacific harbor seal (Phoca vitulina richardii) in central and northern California. Science of the Total Environment 372:676-692.PubMedCrossRefGoogle Scholar
  11. Brookens TJ, O’Hara TM, Taylor RT, Bratton GR, Harvey JT (2008) Total mercury body burden in Pacific harbor seal, Phoca vitulina richardii, pups from central California. Marine Pollution Bulletin 56:27-41.PubMedCrossRefGoogle Scholar
  12. Budtz-Jørgensen E, Grandjean P, Jørgensen PJ, Weihe P, Keiding N (2004) Association between mercury concentrations in blood and hair in methylmercury-exposed subjects at different ages. Environmental Research 95:385-393.PubMedCrossRefGoogle Scholar
  13. Burbacher TM, Rodier PM, Weiss B (1990) Methylmercury and developmental neurotoxicity: a comparison of effects in humans and animals. Neurotoxicology and Teratology 12:191-202.PubMedCrossRefGoogle Scholar
  14. Burek KA, Gulland FMD, Sheffield G, Beckmen KB, Keyes E, Spraker T, et al. (2005) Infectious disease and the decline of Steller sea lions (Eumetopias jubatus) in Alaska, USA: insights from serological data. Journal of Wildlife Diseases 41:512-524.PubMedGoogle Scholar
  15. Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: Correlations with potential for anaerobic function. Journal of Comparative Physiology 143:191-198.Google Scholar
  16. Castellini JM, Meiselman HJ, Castellini MA (1996) Understanding and interpreting hematocrit measurements in pinnipeds. Marine Mammal Science 12:251-264.CrossRefGoogle Scholar
  17. Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Research Bulletin 55(2):197-203.PubMedCrossRefGoogle Scholar
  18. Clarkson TW (1994) The toxicology of mercury and its compounds. In: Mercury Pollution: Integration and Synthesis, Watras CJ, Hackabee JW (editors), Boca Raton, FL: CRC Press, pp 631–642.Google Scholar
  19. Custodio HM, Broberg K, Wennberg M, Jansson J-H, Vessby B, Hallmans G, et al. (2004) Polymorphisms in glutathione-related genes affect methylmercury retention. Archives of Environmental Health 59:588-595.PubMedCrossRefGoogle Scholar
  20. Das K, Siebert U, Gillet A, Dupont A, Di-Poï C, Fonfara S, et al. (2008) Mercury immune toxicity in harbor seals: links to in vitro toxicity. Environmental Health 7:52-68.PubMedCrossRefGoogle Scholar
  21. Davidson PW, Myers GJ, Cox C, Wilding GE, Shamlaye CF, Huang LS, et al. (2006) Methylmercury and neurodevelopment: Longitudinal analysis of the Seychelles child development cohort. Neurotoxicology and Teratology 28:529-535.PubMedCrossRefGoogle Scholar
  22. Davidson PW, Strain JJ, Myers GJ, Thurston SW, Bonham MP, Shamlaye CF, et al. (2008) Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. NeuroToxicology 29:767-775.PubMedCrossRefGoogle Scholar
  23. Debes F, Budtz-Jørgensen E, Weihe P, White RF, Grandjean P (2006) Impact of prenatal methylmercury on neurobehavioral function at age 14 years. Neurotoxicology and Teratology 28:536-547.PubMedCrossRefGoogle Scholar
  24. DeMaster DP, Trites AW, Clapham P, Mizroch S, Wade P, Small RJ, et al. (2006) The sequential megafaunal collapse hypothesis: Testing with existing data. Progress in Oceanography 68:329-342.CrossRefGoogle Scholar
  25. Dietz R, Basu N, Braune B, O’Hara T, Scheuhammer T, Sonne C (2011a) What are the toxicological effects of mercury in arctic biota? In: AMAP Assessment 2011: Mercury in the Arctic, Outridge P, Dietz R, Wilson S (editors), Oslo, Norway: Arctic Monitoring and Assessment Programme (AMAP), pp 113–137.Google Scholar
  26. Dietz R, Born EW, Rigét F, Aubail A, Sonne C, Drimmie R, et al. (2011a) Temporal trends and future predictions of mercury concentrations in northwest Greenland polar bear (Ursus maritimus) hair. Environmental Science and Technology 45:1458-1465.CrossRefGoogle Scholar
  27. Fritz L, Gelatt T (2010) Surveys of Steller sea lions in Alaska, June–July 2010. In: Memorandum to the Record, National Marine Mammal Laboratory, National Marine Fisheries Service 7600 Sand Point Way NE, Seattle, WA 98115 31 pp. Accessed Jan 3, 2011.
  28. Gulland F (1999) Stranded seals: Important sentinels. Journal of the American Veterinarian Medical Association 214(8):1191-1192.Google Scholar
  29. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. (1997) Cognitive deficit in 7-year-old children with pre-natal exposure to methylmercury. Neurotoxicology and Teratology 19:417-428.PubMedCrossRefGoogle Scholar
  30. Gundacker C, Komarnicki G, Jagiello P, Gencikova A, Dahmen N, Wittmann KJ, et al. (2007) Glutathione-S-transferase polymorphism, metallothionein expression, and mercury levels among students in Austria. Science of the Total Environment 385: 37-47.PubMedCrossRefGoogle Scholar
  31. Holmes AL, Wise SS, Goertz CEC, Dunn JL, Gulland FMD, Gelatt T, et al. (2008) Metal tissue levels in Steller sea lion (Eumetopias jubatus) pups. Marine Pollution Bulletin 56:1416-1421.PubMedCrossRefGoogle Scholar
  32. Jones D, Ronald K, Lavigne DM, Frank R, Holdrinet M, Uthe JF (1976) Organochlorine and mercury residues in the harp seal (Pagophilus groenlandicus). Science of the Total Environment 5:181-195.PubMedCrossRefGoogle Scholar
  33. King JC, Gelatt TS, Pitcher KW, Pendelton, GW (2007) A field-based method for estimating age in free-ranging Steller sea lions (Eumetopias jubatus) less than twenty-four months of age. Marine Mammal Science 23(2):262-271.CrossRefGoogle Scholar
  34. Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010a) Hematology of Southern Beaufort Sea polar bears (2005-2007): Biomarker for an arctic ecosystem health sentinel. EcoHealth 7(3):307-320.PubMedCrossRefGoogle Scholar
  35. Kirk CM, Amstrup S, Swor R, Holcomb D, O’Hara TM (2010b) Morbillivirus and Toxoplasma exposure and association with hematological parameters for Southern Beaufort Sea polar bears: potential response to infectious agents in a sentinel species. EcoHealth 7(3):321-331.PubMedCrossRefGoogle Scholar
  36. Knott KK, Schenk P, Beyerlein S, Boyd D, Ylitalo GM, O’Hara TM (2011) Blood-based biomarkers of selenium and thyroid status indicate possible adverse biological effects of mercury and bichlorinated biphenyls in Southern Beaufort Sea polar bears. Environmental Research 111:1124-1136.PubMedCrossRefGoogle Scholar
  37. Lalancette A, Morin Y, Measures L, Fournier M (2003) Contrasting changes of sensitivity by lymphocytes and neutrophils to mercury in developing grey seals. Developmental and Comparative Immunology 27:735-747.PubMedCrossRefGoogle Scholar
  38. Lieske CL, Moses SK, Castellini JM, Klejka J, Hueffer K, O’Hara TM (2011) Toxicokinetics of mercury in blood compartments and hair of fish-fed sled dogs. Acta Veterinaria Scandinavica 53:66. doi: 10.1186/175-0147-53-66. Online Dec 7, 2011.Google Scholar
  39. Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respiratory Physiology 9:277-286.CrossRefGoogle Scholar
  40. Loughlin TR (1998) The Steller sea lion: a declining species. Bioshphere Conservation 1:91-98.Google Scholar
  41. Loughlin TR, Perlov AS, Vladimirov VA (1992) Range-wide survey and estimation of total number of Steller sea lions in 1989. Marine Mammal Science 8:220-239.CrossRefGoogle Scholar
  42. Mathews EA, Womble JN, Pendleton GW, Jemison LA, Maniscalco JM, Streveler G (2011) Population growth and colonization of Steller sea lions in the Glacier Bay region of southeastern Alaska: 1970s–2009. Marine Mammal Science 27(4):852-880.CrossRefGoogle Scholar
  43. Merrick RL (1997) Current and historical roles of apex predators in the Bering Sea ecosystem. Journal of Northwest Atlantic Fishery Science 22:343-355.CrossRefGoogle Scholar
  44. Merrick RL, Loughlin TR, Calkins DG (1987) Decline in abundance of the northern sea lion (Eumetopias jubatus) in Alaska, 1956–86. Fisheries Bulletin 85:351-365.Google Scholar
  45. National Research Council (1996) The Bering Sea Ecosystem. Washington, DC: The National Academies Press 308 pp.Google Scholar
  46. National Marine Fisheries Service (1997) Threatened fish and wildlife: change in listing status of Steller sea lions under the endangered species act. Federal Register 62:24345-24355.Google Scholar
  47. National Marine Fisheries Service (2008) Recovery plan for the Steller sea lion (Eumetopias jubatus). Revision. National Marine Fisheries Service, Silver Spring, MD. 325 pp.Google Scholar
  48. Oken E, Wright RO, Kelinman KP, Bellinger D, Amarasirwardena CJ, Hu H, et al. (2005) Maternal fish consumption, hair mercury, and infant cognition in a US cohort. Environmental Health Perspectives 113(10):1376-1380.PubMedCrossRefGoogle Scholar
  49. Oskarsson A, Palminger HI, Sundberg J (1995) Exposure to toxic elements via breast milk. Analyst 120(3):765-770.PubMedCrossRefGoogle Scholar
  50. Oskarsson A, Palminger HI, Sundberg J, Petersson Grawé K (1998) Risk assessment in relation to neonatal metal exposure. Analyst 123(1):19-23.PubMedCrossRefGoogle Scholar
  51. Phillips CD, Bickham JW, Patton JC, Gelatt TS (2009) Systematics of Steller sea lions (Eumetopias jubatus): subspecies recognition based on concordance of genetics and morphometrics. Occasional Papers, Museum of Texas Tech University 283:1–15.Google Scholar
  52. Pitcher KW, Burkanov VN, Calkins DG, Le Boeuf BJ, Mamaev EG, Merrick RL, et al. (2001) Spatial and temporal variation in the timing of births of Steller sea lions. Journal of Mammalogy 82(4):1047-1053.CrossRefGoogle Scholar
  53. Rawson AJ, Patton GW, Hofmann S, Pietra GG, Johns L (1993) Liver abnormalities associated with chronic mercury accumulation in stranded Atlantic bottlenose dolphins. Ecotoxicology and Environmental Safety 25:41-47.PubMedCrossRefGoogle Scholar
  54. Rea LD, Banks AR, Farley SD, Stricker CA, Fadely BS, Pitcher KW (2011) Regional differences in age of weaning in Steller sea lions determined using stable isotopes of carbon and nitrogen. Alaska Marine Science Symposium, Jan 17–20, 2011, Anchorage, Alaska.Google Scholar
  55. Reddy ML, Dierauf LA, Gulland FMD (2001) Marine mammals as sentinels of ocean health. In: CRC Handbook of Marine Mammal Medicine, Dierauf LA, Gulland FMD (editors), Boca Raton, FL: CRC Press, pp 3–14.CrossRefGoogle Scholar
  56. Rice DC (2008) Overview of modifiers of methylmercury neurotoxicity: Chemicals, nutrients, and the social environment. Neurotoxicology 29:761-766.PubMedCrossRefGoogle Scholar
  57. Risher J, DeWoskin R (1999) Health effects: relevance to public health In: Toxicological Profile for Mercury, Atlanta, GA: US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry (ATSDR), pp 220–300. Accessed Dec 29, 2011.
  58. Roegge CS, Wang VC, Powers BE, Klintsova AY, Villareal S, Greenough WT, et al. (2004) Motor impairment in rats exposed to PCBs and methylmercury during early development. Toxicological Sciences 77:315–24.PubMedCrossRefGoogle Scholar
  59. Ryan PB, Burke TA, Cohen Hubal EA, Cura JJ, McKone TE (2007) Using biomarkers to inform cumulative risk assessment. Environmental Health Perspectives 115(5):833-840.PubMedCrossRefGoogle Scholar
  60. Sinclair EH, Zeppelin TK (2002) Seasonal and spatial differences in diet in the western stock of Steller sea lions (Eumetopias jubatus). Journal of Mammalogy 83:973-990.CrossRefGoogle Scholar
  61. Springer AM, Estes JA, van Vliet GB, Williams TM, Doak DF, Danner EM, et al. (2003) Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? Proceedings of the National Academy of Sciences of the United States of America 100:12223-12228.PubMedCrossRefGoogle Scholar
  62. State of Alaska Epidemiology Bulletin (2010) Alaska hair biomonitoring program update, July 2002–May 2010. Division of Health, Department of Health and Social Services. 3601 C Street, Ste 540, Anchorage, AK, 99503. Bulletin 18, June 24, 2010. Accessed Dec 29, 2011.
  63. Thompson DR (1996) Mercury in birds and terrestrial mammals. In: Environmental Contaminants in Wildlife. Interpreting Tissue Concentrations. Nelson Beyer W, Heinz GH, Redmon-Norwood AW (editors) SETAC Special Publications Series, New York: CRC Press, pp 341–356.Google Scholar
  64. Trites AW, Donnelly CP (2003) The decline of Steller sea lions in Alaska: a review of the nutritional stress hypothesis. Mammal Review 33:3-28.CrossRefGoogle Scholar
  65. Trites AW, Livingston PA, Mackinson S, Vasconcellos C, Springer AM, Pauly D (1999) Ecosystem change and the decline of marine mammals in the eastern Bering Sea: testing the ecosystem shift and commercial whaling hypotheses. Fisheries Centre Research Reports 7, Vancouver, British Columbia, Canada: The Fisheries Centre, University of British Columbia. 106 pp.Google Scholar
  66. Wagemann R, Stewart REA, Lockhart WL, Stewart BE, Provoledo M (1988) Trace metals and methyl mercury: associations and transfer in harp seal (Phoca groenlandica) mothers and their pups. Marine Mammal Science 4:339-355.CrossRefGoogle Scholar
  67. Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Handbook of Ecotoxicology Second ed. Hoffman DJ, Rattner BA, Burton GA Jr., Cairns J Jr. (editors), Boca Raton, FL: Lewis Publishers pp 409–464.Google Scholar
  68. World Health Organization (1990) Environmental health criteria for methylmercury: Evaluation of human health risks. In: Environmental Health Criteria 101, Geneva, Switzerland: International Programme on Chemical Safety (IPCS). Accessed Dec 29, 2011.
  69. Woshner V, Knott K, Wells R, Willetto C, Swor R, O’Hara T (2008) Mercury and selenium in blood and epidermis of bottlenose dolphins (Tursiops truncates) from Sarasota Bay, FL: Interaction and relevance to life history and hematological parameters. EcoHealth 5:360-370.PubMedCrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2012

Authors and Affiliations

  • J. Margaret Castellini
    • 1
    Email author
  • Lorrie D. Rea
    • 2
  • Camilla L. Lieske
    • 3
  • Kimberlee B. Beckmen
    • 2
  • Brian S. Fadely
    • 4
  • John M. Maniscalco
    • 1
    • 5
  • Todd M. O’Hara
    • 3
    • 6
  1. 1.Institute of Marine Science, School of Fisheries and Ocean SciencesUniversity of Alaska FairbanksFairbanksUSA
  2. 2.Division of Wildlife ConservationAlaska Department of Fish and GameFairbanksUSA
  3. 3.Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA
  4. 4.National Marine Mammal LaboratoryAlaska Fisheries Science Center, NOAA FisheriesSeattleUSA
  5. 5.Alaska SeaLife CenterSewardUSA
  6. 6.Department of Biology and Wildlife, College of Natural Science and MathematicsUniversity of Alaska FairbanksFairbanksUSA

Personalised recommendations