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Evaluating Hair as a Predictor of Blood Mercury: The Influence of Ontogenetic Phase and Life History in Pinnipeds

  • Sarah H. PetersonEmail author
  • Elizabeth A. McHuron
  • Stephanie N. Kennedy
  • Joshua T. Ackerman
  • Lorrie D. Rea
  • J. Margaret Castellini
  • Todd M. O’Hara
  • Daniel P. Costa
Article

Abstract

Mercury (Hg) biomonitoring of pinnipeds increasingly utilizes nonlethally collected tissues such as hair and blood. The relationship between total Hg concentrations ([THg]) in these tissues is not well understood for marine mammals, but it can be important for interpretation of tissue concentrations with respect to ecotoxicology and biomonitoring. We examined [THg] in blood and hair in multiple age classes of four pinniped species. For each species, we used paired blood and hair samples to quantify the ability of [THg] in hair to predict [THg] in blood at the time of sampling and examined the influence of varying ontogenetic phases and life history of the sampled animals. Overall, we found that the relationship between [THg] in hair and blood was affected by factors including age class, weaning status, growth, and the time difference between hair growth and sample collection. Hair [THg] was moderately to strongly predictive of current blood [THg] for adult female Steller sea lions (Eumetopias jubatus), adult female California sea lions (Zalophus californianus), and adult harbor seals (Phoca vitulina), whereas hair [THg] was poorly predictive or not predictive (different times of year) of blood [THg] for adult northern elephant seals (Mirounga angustirostris). Within species, except for very young pups, hair [THg] was a weaker predictor of blood [THg] for prereproductive animals than for adults likely due to growth, variability in foraging behavior, and transitions between ontogenetic phases. Our results indicate that the relationship between hair [THg] and blood [THg] in pinnipeds is variable and that ontogenetic phase and life history should be considered when interpreting [THg] in these tissues.

Keywords

Harbor Seal Elephant Seal Northern Elephant Seal Keratinized Tissue Pinniped Species 
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.

Notes

Acknowledgments

Animals were handled under National Marine Fisheries Service (NMFS) permit no. 14636 (northern elephant seals), NMFS permit no. 555-1870 and 373-1686 (harbor seals), United States Fish and Wildlife permit no. 81640-2009-041 and 81640-2011-002 (harbor seals), National Park Service permit no. PORE-2011-SCI-0003 (harbor seals), NMFS permit no. 17952, 14676, 16087, and 17115 (California sea lions), NMFS permit no. 358-1769, 358-1888, 14325, and 14325 (Steller sea lions), and approved Institutional Animal Care and Use Committee protocols from the University of California, Santa Cruz, San Jose State University, the University of Alaska Fairbanks, and the Alaska Department of Fish and Game. We thank the many volunteers, students, and technicians who made this work possible. We especially thank J. Harvey, P. Ponganis, M. Tift, K. Prager, J. Lloyd-Smith, L. Correa, A. Grimes, G. Johnson, J. Harley, A. Christ, P. Robinson, C. Goetsch, X. Rojas-Rocha, D. Crocker, P. Morris, the rangers at Año Nuevo State Reserve, S. Melin, R. DeLong, and J. Harris, as well as the National Marine Mammal Laboratory (Alaska Fisheries Science Center/National Oceanic and Atmospheric Administration) for support. Financial support was provided by funds to S. H. P. and E. A. M from the Friends of Long Marine Laboratory, the Earl and Ethel Myers Oceanographic and Marine Biology Trust, the PADI Foundation, the University of California Natural Reserve System Mildred Mathias Graduate Student Research Grant Program, the Rebecca and Steve Sooy Graduate Fellowship in Marine Mammals, the Achievement Rewards for College Scientists Foundation Northern California Chapter, Grant no. N00014-13-1-0134 and N00014-10-1-0356 to D. P. C. from the Office of Naval Research, the U.S. Geological Survey Western Ecological Research Center to J. T. A, and by NOAA cooperative agreement funds to L. D. R., T. M. O., and the Alaska Department of Fish and Game through Grant no. NA13NMF4720041. The use of trade, product, or firm names in the publication is for descriptive purposes only and does not imply endorsement by the United States government.

References

  1. Ackerman JT, Eagles-Smith CA, Takekawa JY et al (2008) Mercury concentrations in blood and feathers of prebreeding Forster’s terns in relation to space use of San Francisco Bay, California, USA, habitats. Environ Toxicol Chem 27:897–908CrossRefGoogle Scholar
  2. Ackerman JT, Eagles-Smith CA, Herzog MP (2011) Bird mercury concentrations change rapidly as chicks age: toxicological risk is highest at hatching and fledging. Environ Sci Technol 45:5418–5425CrossRefGoogle Scholar
  3. Aschner M, Aschner JL (1990) Mercury neurotoxicity: mechanisms of blood-brain barrier transport. Neurosci Biobehav Rev 14:169–176CrossRefGoogle 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). Can J Zool 64:1086–1094CrossRefGoogle Scholar
  5. Basu N, Scheuhammer AM, Sonne C et al (2009) Is dietary mercury of neurotoxicological concern to wild polar bears (Ursus maritimus)? Environ Toxicol Chem 28:133–140CrossRefGoogle Scholar
  6. Bearhop S, Ruxton GD, Furness RW (2000) Dynamics of mercury in blood and feathers of great skuas. Environ Toxicol Chem 19:1638–1643CrossRefGoogle Scholar
  7. Bigg MA (1969) The harbour seal in British Columbia. Fisheries Research Board of Canada, OttawaGoogle Scholar
  8. Bond AL, Diamond AW (2009) Total and methyl mercury concentrations in seabird feathers and eggs. Arch Environ Contam Toxicol 56:286–291CrossRefGoogle Scholar
  9. Boness DJ, Bowen WD, Oftedal OT (1994) Evidence of a maternal foraging cycle resembling that of otariid seals in a small phocid, the harbor seal. Behav Ecol Sociobiol 4:95–104CrossRefGoogle Scholar
  10. Braune BM (1987) Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch Environ Contam Toxicol 16:217–224CrossRefGoogle Scholar
  11. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35CrossRefGoogle Scholar
  12. Castellini MA, Castellini JM (1989) Influence of hematocrit on whole blood glucose levels: New evidence from marine mammals. Am J Physiol 256:R1220–R1224Google Scholar
  13. Castellini JM, Rea LD, Lieske CL et al (2012) 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. Ecohealth 9:267–277CrossRefGoogle Scholar
  14. Champagne CD, Crocker DE, Fowler MA, Houser DS (2012) Fasting physiology of the pinnipeds: the challenges of fasting while maintaining high energy expenditure and nutrient delivery for lactation. In: McCue MD (ed) Comparative physiology of fasting, starvation, and food limitation. Springer, San Antonio, pp 309–336CrossRefGoogle Scholar
  15. Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36:609–662CrossRefGoogle Scholar
  16. Coltman DW, Bowen WD, Boness DJ, Iverson SJ (1997) Balancing foraging and reproduction in the male harbour seal, an aquatically mating pinniped. Anim Behav 54:663–678CrossRefGoogle Scholar
  17. Correa L, Rea LD, Bentzen R et al (2014) Assessment of mercury and selenium tissular concentrations and total mercury body burden in 6 Steller sea lion pups from the Aleutian Islands. Mar Pollut Bull 82:175–182CrossRefGoogle Scholar
  18. Costa DP (1991) Reproductive and foraging energetics of high latitude penguins, albatrosses and pinnipeds: implications for life history patterns. Am Zool 31:111–130CrossRefGoogle Scholar
  19. Costa DP, Le Boeuf BJ, Huntley AC, Ortiz CL (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool 209:21–33CrossRefGoogle Scholar
  20. Daniel R (2003) The timing of moulting in wild and captive Steller sea lions (Eumetopias jubatus). Master’s thesis. University of British Columbia, VancouverGoogle Scholar
  21. Das K, Debacker V, Pillet S et al (2003) Heavy metals in marine mammals. In: Vos JG, Bossart GD, Fournier M, O’Shea TJ (eds) Toxicology of marine mammals. Taylor & Francis, New York, pp 135–167Google Scholar
  22. Day RD, Segars AL, Arendt MD et al (2007) Relationship of blood mercury levels to health parameters in the loggerhead sea turtle (Caretta caretta). Environ Health Perspect 115:1421Google Scholar
  23. Dietz R, Riget F, Born EW et al (2006) Trends in mercury in hair of Greenlandic polar bears (Ursus maritimus) during 1892–2001. Environ Sci Technol 40:1120–1125CrossRefGoogle Scholar
  24. Dietz R, Born EW, Rigét F et al (2011) Temporal trends and future predictions of mercury concentrations in northwest Greenland polar bear (Ursus maritimus) hair. Environ Sci Technol 45:1458–1465CrossRefGoogle Scholar
  25. Dietz R, Sonne C, Basu N et al (2013) What are the toxicological effects of mercury in Arctic biota? Sci Total Environ 443:775–790CrossRefGoogle Scholar
  26. Eagles-Smith CA, Ackerman JT, Adelsbach TL et al (2008) Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA. Environ Toxicol Chem 27:2136–2153CrossRefGoogle Scholar
  27. Eagles-Smith CA, Ackerman JT, Yee J, Adelsbach TL (2009) Mercury demethylation in waterbird livers: dose-response thresholds and differences among species. Environ Toxicol Chem 28:568–577CrossRefGoogle Scholar
  28. Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. North Am Fauna 74:1–279CrossRefGoogle Scholar
  29. Finkelstein ME, Grasman KA, Croll DA et al (2007) Contaminant-associated alteration of immune function in black-footed albatross (Phoebastria nigripes), a north Pacific predator. Environ Toxicol Chem 26:1896–1903CrossRefGoogle Scholar
  30. Freeman HC, Sangalang GB (1977) A study of the effects of methyl mercury, cadmium, arsenic, selenium, and a PCB, (Aroclor 1254) on adrenal and testicular steroidogeneses in vitro, by the gray seal Halichoerus grypus. Arch Environ Contam Toxicol 5:369–383CrossRefGoogle Scholar
  31. Furness RW, Muirhead SJ, Woodburn M (1986) Using bird feathers to measure mercury in the environment: Relationships between mercury content and moult. Mar Pollut Bull 17:27–30CrossRefGoogle Scholar
  32. Gentry RL (1971) Social behavior of the Steller sea lion. Doctoral dissertation. University of California, Santa CruzGoogle Scholar
  33. Gray R, Canfield P, Rogers T (2008) Trace element analysis in the serum and hair of Antarctic leopard seal, Hydrurga leptonyx, and Weddell seal, Leptonychotes weddellii. Sci Total Environ 399:202–215CrossRefGoogle Scholar
  34. Habran S, Debier C, Crocker DE et al (2010) Assessment of gestation, lactation and fasting on stable isotope ratios in northern elephant seals (Mirounga angustirostris). Mar Mammal Sci 26:880–895CrossRefGoogle Scholar
  35. Habran S, Debier C, Crocker DE et al (2011) Blood dynamics of mercury and selenium in northern elephant seals during the lactation period. Environ Pollut 159:2523–2529CrossRefGoogle Scholar
  36. Harris HH, Pickering IJ, George GN (2003) The chemical form of mercury in fish. Science 301:1203CrossRefGoogle Scholar
  37. Hartman CA, Ackerman JT, Herring G et al (2013) Marsh wrens as bioindicators of mercury in wetlands of Great Salt Lake: do blood and feathers reflect site-specific exposure risk to bird reproduction? Environ Sci Technol 47:6597–6605Google Scholar
  38. Harvey JT, Goley D (2011) Determining a correction factor for aerial surveys of harbor seals in California. Mar Mammal Sci 27:719–735CrossRefGoogle Scholar
  39. Ikemoto T, Kunito T, Watanabe I et al (2004) Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seals (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ Pollut 127:83–97CrossRefGoogle Scholar
  40. Jeffries S, Brown RF, Harvey JT (1993) Techniques for capturing, handling and marking harbour seals. Aquat Mamm 19:21–25Google Scholar
  41. Lavoie RA, Baird CJ, King LE et al (2014) Contamination of mercury during the wintering period influences concentrations at breeding sites in two migratory piscivorous birds. Environ Sci Technol 48(23):13694–13702CrossRefGoogle Scholar
  42. Le Boeuf BJ, Crocker DE, Costa DP et al (2000) Foraging ecology of northern elephant seals. Ecol Monogr 70:353–382CrossRefGoogle Scholar
  43. Lewis SA, Furness RW (1991) Mercury accumulation and excretion in laboratory reared black-headed gull Larus ridibundus chicks. Arch Environ Contam Toxicol 21:316–320CrossRefGoogle Scholar
  44. Lieske CL, Moses SK, Castellini JM et al (2011) Toxicokinetics of mercury in blood compartments and hair of fish-fed sled dogs. Acta Vet Scand 53:66CrossRefGoogle Scholar
  45. Ling JK (2012) The skin and hair of the southern elephant seal, Mirounga leonina (Linn.). IV. Annual cycle of pelage follicle activity and moult. Aust J Zool 60:259–271CrossRefGoogle Scholar
  46. Lowry LF, Frost KJ, Ver Hoef JM, DeLong RA (2001) Movements of satellite-tagged subadult and adult harbor seals in Prince William Sound, Alaska. Mar Mamm Sci 17:835–861CrossRefGoogle Scholar
  47. Mason RP, Choi AL, Fitzgerald WF et al (2012) Mercury biogeochemical cycling in the ocean and policy implications. Environ Res 119:101–117CrossRefGoogle Scholar
  48. McDonald BI, Ponganis PJ (2013) Insights from venous oxygen profiles: oxygen use and management in diving California sea lions. J Exp Biol 216:3332–3341CrossRefGoogle Scholar
  49. McHuron EA, Harvey JT, Castellini JM et al (2014) Selenium and mercury concentrations in harbor seals (Phoca vitulina) from central California: health implications in an urbanized estuary. Mar Pollut Bull 83(1):48–57CrossRefGoogle Scholar
  50. McHuron EA, Peterson SH, Ackerman JT, Melin SR, Harris JD, Costa DP (2015) Effects of age, colony, and sex on mercury concentrations in California sea lions. Arch Environ Contam Toxicol (this issue)Google Scholar
  51. McLaren I (1993) Growth in pinnipeds. Biol Rev 68:1–79CrossRefGoogle Scholar
  52. Melin SR, DeLong RL, Thomason JR (2000) Attendance patterns of California sea lion (Zalophus californianus) females and pups during the nonbreeding season at San Miguel Island. Mar Mamm Sci 16(1):169–185CrossRefGoogle Scholar
  53. Merrick RL, Loughlin TR (1997) Foraging behavior of adult female and young-of-the-year Steller sea lions in Alaskan waters. Can J Zool Can Zool 75:776–786CrossRefGoogle Scholar
  54. Monteiro LR, Furness RW (1997) Accelerated increase in mercury contamination in north Atlantic mesopelagic food chains as indicated by time series of seabird feathers. Environ Toxicol Chem 16:2489–2493CrossRefGoogle Scholar
  55. O’Hara TM, Hanns C, Woshner VM et al (2008) Essential and nonessential elements in the bowhead whale: epidermis-based predictions of blubber, kidney, liver and muscle tissue concentrations. J Cetacean Res Manag 10:107–117Google Scholar
  56. Peterson SH, Hassrick JL, Lafontaine A et al (2014) Effects of age, adipose percent, and reproduction on PCB concentrations and profiles in an extreme fasting North Pacific marine mammal. PLoS One 9:e96191CrossRefGoogle Scholar
  57. Peterson SH, Ackerman JT, Costa DP (2015) Marine foraging ecology influences mercury bioaccumulation in deep-diving northern elephant seals. Proc Royal Soc B 282:20150710. doi:  10.1098/rspb.2015.0710 CrossRefGoogle Scholar
  58. Pitcher KW, Calkins DG (1981) Reproductive biology of Steller sea lions in the Gulf of Alaska. J Mammol 62:599–605CrossRefGoogle Scholar
  59. Rea LD, Castellini JM, Correa L et al (2013) Maternal Steller sea lion diets elevate fetal mercury concentrations in an area of population decline. Sci Total Environ 454:277–282CrossRefGoogle Scholar
  60. Rea LD, Christ A, Hayden A, et al. (2015) Age-specific vibrissae growth rates: A tool for determining the timing of ecologically important events in Steller sea lions. Mar Mamm Sci 1–21Google Scholar
  61. Robinson PW, Costa DP, Crocker DE et al (2012) Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data rich species, the northern elephant seal. PLoS One 7:e36728CrossRefGoogle Scholar
  62. Ronald K, Tessaro SV, Uthe JF et al (1977) Methylmercury poisoning in the harp seal (Pagophilus groenlandicus). Sci Total Environ 8:1–11CrossRefGoogle Scholar
  63. Ronald K, Frank RJ, Dougan J, Braun HE (1984) Pollutants in harp seals (Phoca groenlandica). II. Heavy metals and selenium. Sci Total Environ 38:153–166CrossRefGoogle Scholar
  64. Sakamoto M, Kubota M, Matsumoto S et al (2002) Declining risk of methylmercury exposure to infants during lactation. Environ Res 90:185–189CrossRefGoogle Scholar
  65. Soria ML, Sanz P, Martínez D et al (1992) Total mercury and methylmercury in hair, maternal and umbilical blood, and placenta from women in the Seville area. Bull Environ Contam Toxicol 48:494–501CrossRefGoogle Scholar
  66. Sunderland EM, Mason RP (2007) Human impacts on open ocean mercury concentrations. Global Biogeochem Cycles 21:GB4022Google Scholar
  67. Van de Ven WSM, Koeman JH, Svenson A (1979) Mercury and selenium in wild and experimental seals. Chemosphere 8:539–555CrossRefGoogle Scholar
  68. Wagemann R, Stewart REA, Lockhart WL et al (1988) Trace metals and methyl mercury: associations and transfer in harp seal (Phoca Groenlandica) mothers and their pups. Mar Mamm Sci 4:339–355CrossRefGoogle Scholar
  69. Wang W, Evans RD, Hickie BE et al (2014) Methylmercury accumulation and elimination in mink (Neovison vison) hair and blood: results of a controlled feeding experiment using stable isotope tracers. Environ Toxicol Chem 33:2873–2880CrossRefGoogle Scholar
  70. Williams TM, Rutishauser M, Long B et al (2007) Seasonal variability in otariid energetics: implications for the effects of predators on localized prey resources. Physiol Biochem Zool 80:433–443CrossRefGoogle Scholar
  71. Worthy GAJ, Morris PA, Costa DP, Le Boeuf BJ (1992) Moult energetics of the northern elephant seal (Mirounga angustirostris). J Zool 227:257–265CrossRefGoogle Scholar
  72. Woshner V, Knott K, Wells R et al (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 5:360–370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Sarah H. Peterson
    • 1
    Email author
  • Elizabeth A. McHuron
    • 1
  • Stephanie N. Kennedy
    • 2
    • 5
  • Joshua T. Ackerman
    • 3
  • Lorrie D. Rea
    • 4
  • J. Margaret Castellini
    • 5
  • Todd M. O’Hara
    • 5
  • Daniel P. Costa
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, Santa CruzSanta CruzUSA
  2. 2.Division of Wildlife ConservationAlaska Department of Fish and GameFairbanksUSA
  3. 3.U.S. Geological Survey, Western Ecological Research CenterDixonUSA
  4. 4.Institute of Northern Engineering, Water and Environmental Research CenterUniversity of Alaska FairbanksFairbanksUSA
  5. 5.Wildlife Toxicology Laboratory, Department of Veterinary MedicineUniversity of Alaska FairbanksFairbanksUSA

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