Abstract
Monomethylmercury (MeHg+) is an environmental pollutant, which at sufficiently high exposures, has induced neurotoxicosis in several animal species, including humans. Adverse neurological effects due to gestational exposure are of particular concern as MeHg+ readily crosses the blood–brain and placental barriers. The degree to which environmental concentrations in marine prey affect free-living piscivorous wildlife, however, remains largely undetermined. We examined associations of gestational exposures to mercury on neurodevelopment and survival using hair and blood concentrations of total mercury ([THg]) in a stranded population of Pacific harbor seal pups from central California. A positive association was determined for the presence of abnormal neurological symptoms and increasing [THg] in blood (P = 0.04), but not hair. Neither hair nor blood [THg] was significantly associated with survival, or the neurodevelopmental milestone ‘free-feeding’, which was measured from the onset of hand-assisted feeding to the time at which pups were able to consume fish independently. Both hair and blood [THg] exceeded threshold values considered potentially toxic to humans and other mammalian wildlife species. The higher [THg] in blood associated with abnormal neurological symptoms may indicate an adverse effect of this pollutant on neurodevelopment in harbor seal pups. These data have broader implications with respect to human health and public policy as harbor seals and humans consume similar fish species, and it is possible that safeguard levels established for marine mammals could also extend to human populations that regularly consume fish.
Similar content being viewed by others
References
Basu N, Scheuhammer AM, Bursian SJ, Elliott J, Rouvinen-Watt K, Chan HM (2007) Mink as a sentinel species in environmental health. Environmental Research 103:130-144
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
Brookens TJ (2006) Trace element concentrations in the Pacific harbor seal, Phoca vitulina richardii, in central and northern California. M.Sc. Thesis, Department of Marine Science, Moss Landing Marine Laboratories and California State University Monterey Bay, Moss Landing, CA, p 103
Brookens TJ, Harvey, JT, O’Hara TM (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
Brookens TJ, O’Hara TM, Taylor RJ, 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
Castellini JM, Rea LD, Lieske CL, Beckmen KB, Fadely BS, Maniscalco JM, O’Hara TM (2012) Mercury concentrations in hair from neonatal and juvenile stellar sea lions (Eumetopias jubatus): Implications based on age and region in this northern pacific marine sentinel piscivore. EcoHealth 3:267-277
Castoldi AF, Coccini T, Ceccatelli, S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Research Bulletin 55:197-203
Castoldi AF, Onishchenko N, Johansson C, Coccini T, Roda E, Vahter M, Ceccatelli S, Manzo L (2008) Neurodevelopmental toxicity of methylmercury: Laboratory animal data and their contribution to human risk assessment. Regulatory Toxicology and Pharmacology 51:215-229
Centers for Disease Control and Prevention (CDC) (2014) National Biomonitoring Program: Biomonitoring Summary. Mercury. CAS No. 7439-97-6. http://www.cdc.gov/biomonitoring/Mercury_BiomonitoringSummary.html (accessed May 17, 2014)
Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Critical Reviews in Toxicology 36:609-662
Colegrove KM, Greig DJ, Gulland FMD (2005) Causes of live strandings of northern elephant seals (Mirounga angusirostris) and Pacific harbor seals (Phoca vitulina) along the central California coast, 1992–2001. Aquatic Mammals 3:1–10
Davidson PW, Strain JJ, Myers GJ, Thurston SW, Bonham MP, Shamlaya CF, Stokes-Riner A, Wallace JMW, Robson PJ, Duffy EM, Georger LA, Sloane-Reeves J, Cernichiari E, Canfield RL, Cox C, Huang LS, Janciuras J, Clarkson TW (2008) Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. Neurotoxicology 29:767-775
Davis JA, Hetzel F, Oram JJ, McKee LJ (2007) Polychlorinated biphenyls (PCBs) in San Francisco Bay. Environmental Research 105:67-86
Davis JA, Schiff K, Melwani AR, Bezalel SN, Hunt JA, Allen RM, Ichikawa G, Bonnema A, Heim WA, Crane D, Swenson S, Lamerdin C, Stephenson M (2011) Contaminants in fish from the California coast, 2009: Summary report on year one of a two-year screening survey. A report of the Surface Water Ambient Monitoring Program (SWAMP). California State Water Resources Control Board, Sacramento, CA
Dietz R, Basu N, Braune B, O’Hara T, Scheuhammer T, Sonne C (2011). What are the toxicological effects of mercury in arctic biota? In: Outridge P, Dietz R, Wilson W (Eds) AMAP Assessment 2011: Mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway
Evers DC, Han Y-J, Driscoll CT, Kamman NC, Goodale MW, Lambert KF, Holsen TM, Chen CY, Clair TA, Butler T (2007) Biological mercury hotspots in the northeastern United States and southeastern Canada. BioScience 57:29-43
Gibble CM (2011) Food habits of harbor seals (Phoca vitulina richardii) in San Francisco Bay, California. M.Sc. Thesis, Department of Marine Science, Moss Landing Marine Laboratories and California State University Monterey Bay, Moss Landing, CA, p 61
Grandjean P, Landrigan PJ (2006) Developmental neurotoxicity of industrial chemicals. Lancet 368:2167-2178
Grigg EK, Allen SG, Green DE, Markowitz H (2004) Harbor seal, Phoca vitulina richardii, population trends in the San Francisco Bay estuary, 1970-2002. California Fish and Game 20: 51-70
Gulland FMD, Hall AJ (2005) The role of infectious disease in influencing status and trends. In: Reynolds JE, Ragen (Eds) Marine Mammal Research: Conservation Beyond Crisis. Johns Hopkins University Press, Baltimore, MD
Harvey JT, Brown RF, Mate BR (1990) Abundance and distribution of harbor seals (Phoca vitulina) in Oregon, 1975–1983. Northwestern Naturalist 71:65-71
Health Canada (1984) Methylmercury in Canada Vol. II. Ministry of National Health and Welfare, Ottawa, Canada
Horvat M, Gibicar D (2005) Speciation of mercury: Environment, food, clinical, and occupational health. In: Handbook of Elemental Speciation, Handbook of Elemental Speciation II: Species in the Environment, Food, Medicine and Occupational Health, Cornelis R, Crews H, Heurmann K (Eds), Sussex (UK): John Wiley & Sons Ltd.
Huber HR, Jeffries SJ, Brown RF, Delong RL, Vanblaricom G (2001) Correcting aerial survey counts of harbor seals (Phoca vitulina richardsi) in Washington and Oregon. Marine Mammal Science 17:276–293
Johansson C, Castoldi AF, Onishchenko N, Manzo L, Vahter M, Ceccatelli S (2007) Neurobavioural and molecular changes induced by methylmercury exposure during development. Neurotoxicity Research 11:241-260
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 polychlorinated biphenyls in Southern Beaufort Sea polar bears. Environmental Research 111:1124-1136
Kopec, DA, Harvey JT (1995) Toxic pollutants, health indices, and population dynamics of harbor seals in San Francisco Bay, 1989-1992. Moss Landing Marine Laboratories Technical Publication, 96–4
Lander ME, Harvey JT, Gulland FM (2003) Hematology and serum chemistry comparisons between free-ranging and rehabilitated harbor seal (Phoca vitulina richardsi) pups. Journal of Wildlife Diseases 39:600-609
Lowry MS, Carretta JV, Forney KA (2008) Pacific harbor seal census in California during May-July 2002 and 2004. California Fish and Game 94:180-193
Mahaffey KR (2000) Recent advances in recognition of low-level methylmercury poisoning. Current Opinion in Neurology 13:699-707
Mayfield DB, Johnson MS, Burris JA, Fairbrother A (2013) Furthering the derivation of predictive wildlife toxicity reference values for use in soil cleanup decisions. Integrated Environmental Asssessment and Management 9999:1-14
McHuron EA (2012) Health implications of mercury, selenium, and a red pelage in Pacific harbor seals (Phoca vitulina richardii) off central California. M.Sc. Thesis, Department of Marine Science, Moss Landing Marine Laboratories and California State University Monterey Bay, Moss Landing, CA, p 112
McHuron EA, Harvey JT, Castellini JM, Stricker CA, O’Hara TM (2014) Selenium and mercury concentrations in harbor seals (Phoca vitulina) from central California: Health implications in an urbanized estuary. Marine Pollution Bulletin 83:48-57
Muelbert MMC, Bowen WD, Iverson SJ (2003) Weaning mass affects changes in body composition and food intake in harbor seal pups during the first month of independence. Physiology and Biochemical Zoology 76:418-427
Myers GJ, Davidson PW (1998) Prenatal methylmercury exposure and children: neurologic, developmental, and behavioral research. Environmental Health Perspectives 106:841-847
National Research Council (2000) Toxicological effects of methylmercury, Washington DC: The National Academy Press, pp 1-364
Neale JCC, Gulland FMD, Schmelzer KR, Harvey JT, Berg EA, Allen SG, Greig DJ, Grigg EK, Tjeerdema RS (2005) Contaminant loads and hematological correlates in the harbor seal (Phoca vitulina) of San Francisco Bay, California. Journal of Toxicology and Environmental Health, Part A 68:617-633
Newland CM, Donlin WD, Paletz EM, Banna KM (2006) Developmental behavioral toxicity of methylmercury: consequences, conditioning, and cortex. In: Animal Models of Cognitive Impairment, Levin ED, Buccafusco JJ (Eds), Boca Raton (FL): CRC Press
Nuttall KL (2006) Interpreting hair mercury levels in individual patients. Annals of Clinical and Laboratory Science 36:248-261
O’Hara TM, O’Shea TJ (2005) Assessing impacts of environmental contaminants. In: Reynolds JE, Ragen (Eds) Marine Mammal Research: Conservation Beyond Crisis. Johns Hopkins University Press, Baltimore, MD
Pilsner JR, Lazarus AL, Nam DH, Letcher RJ, Sonne C, Dietz R, Basu N (2010) Mercury-associated DNA hypomethylation in polar bear brains via the LUminometric Methylation Assay: a sensitive method to study epigenetics in wildlife. Molecular Ecology 19:307-314
Rea LD, Castellini JM, Correa L, Fadely BS, O’Hara TM (2013) Maternal Stellar sea lion diets elevate fetal mercury concentrations in an area of population decline. Science of the Total Environment 454-455:277-282
Sakamoto M, Kakita A, Wakabayashi K, Takahashi H, Nakano A, Akagi H (2002) Evaluation of changes in methylmercury accumulation in the developing rat brain and its effects: a study with consecutive and moderate dose exposure throughout gestation and lactation periods. Brain Research 949:51-59
Scheuhammer AM, Basu N, Evers DC, Heinz GH, Sandheinrich MB, Bank MS (2011) Ecotoxicology of mercury in fish and wildlife: recent advances. In: Mercury in the Environment: Pattern and Process, Bank M (editor), Berkeley, CA: University of California Press
Shaw SD (2002) An investigation of persistent organic pollutants (POP’s) and heavy metals in tissues of harbor seals and grey seals in the Gulf of Maine. Final report to the Maine Department of Env. Protection pp 1-17
Sydeman WJ, Allen SG (1999) Pinniped population dynamics in central California: correlations with sea surface temperature and upwelling indices. Marine Mammal Science 15:446-461
USEPA (US Environmental Protection Agency) (1997) Mercury Study Report to Congress, Volume VII: Characterization of human health and wildlife risks from mercury exposure in the United States. EPA-452/R-97-009. http://www.epa.gov/ttn/oarpg/t3/reports/volume7.pdf (accessed March 25, 2014)
Wagemann R, Stewart REA, Lockhart WL, Stewart BE, Povoledo 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
Weiss B, Cory-Slechta DA (1994) Assessment of behavioral toxicity In: Principles and Methods of Toxicology, 5 th edition, A. Wallace Hayes (Ed), Raven Press, NY
WHO (World Health Organization) (1990) Environmental Health Criteria for methylmercury: effects on man. In: Environmental Health Criteria 101, Geneva, Switzerland: International Programme on Chemical Safety (IPCS). http://www.inchem.org/documents/ehc/ehc/ehc101.htm#PartNumber:10 (accessed February 14, 2014)
Wiener JG, Krabbenhoft, Heinz DP, Scheuhammer AM (2003) Ecotoxicology of Mercury, Chapter 16 In: Hoffman, BA, Rattner GA, Burton GA Jr., (Eds) Handbook of Ecotoxicology, 2nd edition. CRC Press, Boca Raton, FL
Woshner V, Knott K, Wells R, Willetto C, Swor R, O’Hara TM (2008) Mercury and selenium in blood and epidermis of bottlenose dolphins (Tursiops truncatus) from Sarasota Bay, FL: interaction and relevance to life history and hematologic parameters. EcoHealth 5:360-370
Zheng W, Aschner M, Ghersi-Egea JF (2003) Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicology And Applied Pharmacology 192:1-11
Acknowledgements
We thank the staff and volunteers at TMMC for their assistance in sample collections and neurological data acquisition, the Wildlife Toxicology Laboratory (UAF) for accommodating their expert knowledge and use of Milestone DMA-80 Direct Mercury Analyzers, and Dr. Christina Hansen for her analysis of blood [THg]. We also thank Dr. Larissa Minicucci, DVM/MPH Program Director at the University of Minnesota, College of Veterinary Medicine for her gracious support of this project. This research was conducted under MMPA permit No. 932-1905/MA-009526 Gulland F. as part of standard protocols with subsamples provided for this diagnostic assessment.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Van Hoomissen, S., Gulland, F.M.D., Greig, D.J. et al. Blood and Hair Mercury Concentrations in the Pacific Harbor Seal (Phoca vitulina richardii) Pup: Associations with Neurodevelopmental Outcomes. EcoHealth 12, 490–500 (2015). https://doi.org/10.1007/s10393-015-1021-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-015-1021-8