Abstract
Changes to Pacific walruses (Odobenus rosmarus divergens) habitat and foraging behavior may affect exposure to both toxic and essential trace elements in walrus tissue. This study measured the trace element concentrations of silver (Ag), arsenic (As), cadmium (Cd), cobalt (Co), copper (Cu), nickel (Ni), total (THg) and methyl mercury (MeHg), selenium (Se), lead (Pb), and zinc (Zn) in walrus skeletal muscle sampled during 2009–2015. Females had significantly higher concentrations of THg (p = 0.021), MeHg (p = 0.037), Cd (p = 0.021), Cu (p = 0.003), and Se (p = 0.001) compared to males. Females with no calf had significantly higher concentrations of Cd compared to females with a calf (p = 0.001) and pregnant females and females with a calf had significantly lower Se concentrations compared to females with a yearling or no calf (p < 0.05). Bering Sea males had significantly higher Ni concentrations (p = 0.001) and significantly lower Se (p = 0.006) and Zn concentrations (p = 0.001) compared to other locations. THg, MeHg, and As tissue concentrations decreased with age (p < 0.01), suggesting these toxic elements are not accumulating in this tissue while Cd increased with age (p < 0.05). The narrower range in element concentrations among pregnant and nursing females may indicate less variation in prey species, and coupled with the reproductive needs for essential elements, suggests they may be more vulnerable to changes in prey availability compared to other walruses.
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References
Agusa T, Yasugi S, Iida A, Ikemoto T, Anan Y, Kuiken T, Osterhaus ADME et al (2011) Accumulation features of trace elements in mass-stranded harbor seals (Phoca vitulina) in the North Sea coast in 2002: the body distribution and association with growth and nutrition status. Mar Pollut Bull 62:963–975. https://doi.org/10.1016/j.marpolbul.2011.02.047
AKDEC (2021) Selenium in fish and shellfish caught in Alaskan waters. Alaska Department of Environmental Conservation, Anchorage, Alaska. https://dec.alaska.gov/eh/vet/fish-monitoring-program/fish-tissue-mercury.aspx.html. Accessed 8 January 2022
Akmajian A, Calambokidis J, Huggins JL, Lambourn D (2014) Age, region, and temporal patterns of trace elements measured in stranded harbor seals (Phoca vitulina richardii) from Washington inland waters. Northwest Nat 95:83–91
Anderson M, Braak CT (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comput Simul 73:85–113. https://doi.org/10.1080/00949650215733
Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83:557–574. https://doi.org/10.1890/12-2010.1
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for Primer: guide to software and statistical methods. Primer-E: Plymouth, UK
Anderson J (2011) Togiak refuge works to prevent fatal walrus plunges. Refuge update. US Fish & Wildlife Service, Hoboken, p 4
Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: statistics reference online. American Cancer Society, Atlanta, pp 1–15
Atwell L, Hobson KA, Welch HE (1998) Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can J Fish Aquat Sci 55:1114–1121
Bełdowska M, Falkowska L (2016) Mercury in marine fish, mammals, seabirds, and human hair in the coastal zone of the southern Baltic. Water Air Soil Pollut 227:52. https://doi.org/10.1007/s11270-015-2735-5
Booth S, Zeller D (2005) Mercury, food webs, and marine mammals: implications of diet and climate change for human health. Environ Health Perspect 113:521–526. https://doi.org/10.1289/ehp.7603
Born EW, Kraul I, Kristensen T (1981) Mercury, DDT and PCB in the Atlantic walrus (Odobenus rosmarus rosmarus) from the Thule District, North Greenland. Arctic 34:255–260
Borque-Espinosa A, Rode KD, Ferrero-Fernández D, Forte A, Capaccioni-Azzati R, Fahlman A (2021) Subsurface swimming and stationary diving are metabolically cheap in adult Pacific walruses (Odobenus rosmarus divergens). J Exp Biol 224:jeb2423. https://doi.org/10.1242/jeb.242993
Bowman KL, Lamborg CH, Agather AM (2020) A global perspective on mercury cycling in the ocean. Sci Total Environ 710:136166. https://doi.org/10.1016/j.scitotenv.2019.136166
Bradley PT (2017) Methods for aquatic life monitoring at the Red Dog Mine site. Alaska Department of Fish and Game, Fairbanks, Alaska
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. Mar Pollut Bull 56:27–41. https://doi.org/10.1016/j.marpolbul.2007.08.010
Burger J, Gochfeld M (2013) Selenium/mercury molar ratios in freshwater, marine, and commercial fish from the USA: variation, risk, and health management. Rev Environ Health 28:129–143. https://doi.org/10.1515/reveh-2013-0010
Chapman PM, Adams WJ, Brooks M, Delos CG, Luoma SN, Maher WA, Ohlendorf HM et al (eds) (2010) Ecological assessment of selenium in the aquatic environment. CRC Press, Boca Raton
Clark D (1987) Selenium accumulation in mammals exposed to contaminated California irrigation drainwater. Sci Total Environ 66:147–168. https://doi.org/10.1016/0048-9697(87)90084-2
Clark CT, Horstmann L, de Vernal A, Jensen AM, Misarti N (2019) Pacific walrus diet across 4000 years of changing sea ice conditions. Quat Res. https://doi.org/10.1017/qua.2018.140
Clark CT, Horstmann L, Misarti N (2020) Zinc concentrations in teeth of female walruses reflect the onset of reproductive maturity. Conserv Physiol 8:coaa029. https://doi.org/10.1093/conphys/coaa029
Clark CT, Horstmann L, Misarti N (2021) Walrus teeth as biomonitors of trace elements in Arctic marine ecosystems. Sci Total Environ 772:145500. https://doi.org/10.1016/j.scitotenv.2021.145500
Cobbina SJ, Chen Y, Zhou Z, Wu X, Zhao T, Zhang Z, Feng W et al (2015) Toxicity assessment due to sub-chronic exposure to individual and mixtures of four toxic heavy metals. J Hazard Mater 294:109–120. https://doi.org/10.1016/j.jhazmat.2015.03.057
Correa L, Castellini JM, Quakenbush LT, O’Hara TM (2015) Mercury and selenium concentrations in skeletal muscle, liver, and regions of the heart and kidney in bearded seals from Alaska, USA: Hg and Se by region in bearded seal heart and kidney. Environ Toxicol Chem 34:2403–2408. https://doi.org/10.1002/etc.3079
da Conceição Nascimento Pinheiro M, do Nascimento JLM, de Lima Silveira LC, da Rocha JBT, Aschner M (2009) Mercury and selenium—a review on aspects related to the health of human populations in the Amazon. Environ Bioindic 4:222–245. https://doi.org/10.1080/15555270903143440
Das K, Dupont A, De Pauw-Gillet M-C, Debier C, Siebert U (2016) Absence of selenium protection against methylmercury toxicity in harbour seal leucocytes in vitro. Mar Pollut Bull 108:70–76. https://doi.org/10.1016/j.marpolbul.2016.04.060
Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, Bratton GR, Taylor RJ et al (2005) Trace elements in tissues of phocid seals harvested in the Alaskan and Canadian Arctic: influence of age and feeding ecology. Can J Zool 83:726–746. https://doi.org/10.1139/z05-053
Dehn L-A, Follmann EH, Thomas DL, Sheffield GG, Rosa C, Duffy LK, O’Hara TM (2006) Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci Total Environ 362:103–123. https://doi.org/10.1016/j.scitotenv.2005.11.012
Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, O’Hara TM (2007) Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol 30:167–181. https://doi.org/10.1007/s00300-006-0171-0
Dietz R, Outridge PM, Hobson KA (2009) Anthropogenic contributions to mercury levels in present-day Arctic animals—a review. Sci Total Environ 407:6120–6131. https://doi.org/10.1016/j.scitotenv.2009.08.036
Dietz R, Sonne C, Basu N, Braune B, O’Hara T, Letcher RJ, Scheuhammer T et al (2013) What are the toxicological effects of mercury in Arctic biota? Sci Total Environ 443:775–790. https://doi.org/10.1016/j.scitotenv.2012.11.046
Dietz R, Letcher RJ, Desforges J, Eulaers I, Sonne C, Wilson S, Andersen-Ranberg E et al (2019) Current state of knowledge on biological effects from contaminants on arctic wildlife and fish. Sci Total Environ 696:133792. https://doi.org/10.1016/j.scitotenv.2019.133792
Dietz R, Letcher RJ, Aars J, Andersen M, Boltunov A, Born EW, Ciesielski TM et al (2022) A risk assessment review of mercury exposure in Arctic marine and terrestrial mammals. Sci Total Environ 829:154445. https://doi.org/10.1016/j.scitotenv.2022.154445
Ewald JD, Kirk JL, Li M, Sunderland EM (2019) Organ-specific differences in mercury speciation and accumulation across ringed seal (Phoca hispida) life stages. Sci Total Environ 650:2013–2020. https://doi.org/10.1016/j.scitotenv.2018.09.299
Fay FH, Merrick RL, Sease JL (1990) Predation on a ringed seal, Phoca hispida, and a black guillemot, Cepphus grylle, by a Pacific walrus Odobenus rosmarus divergens. Mar Mamm Sci 6:248. https://doi.org/10.1111/j.1748-7692.1990.tb00364.x
Fritz L, Brost B, Laman E, Luxa K, Sweeney K, Thomason J, Tollit D et al (2019) A re-examination of the relationship between Steller sea lion (Eumetopias jubatus) diet and population trend using data from the Aleutian Islands. Can J Zool 97:1137–1155. https://doi.org/10.1139/cjz-2018-0329
Frouin H, Loseto LL, Stern GA, Haulena M, Ross PS (2012) Mercury toxicity in beluga whale lymphocytes: limited effects of selenium protection. Aquat Toxicol 109:185–193. https://doi.org/10.1016/j.aquatox.2011.09.021
Gaden A, Stern GA (2010) Temporal trends in beluga, narwhal and walrus mercury levels: links to climate change. A little less Arctic: top predators in the world’s largest Northern Inland Sea, Hudson Bay. Springer, Dordrecht, pp 197–216
Gailer J (2007) Arsenic–selenium and mercury–selenium bonds in biology. Coord Chem Rev 251:234–254. https://doi.org/10.1016/j.ccr.2006.07.018
Gajdosechova Z, Brownlow A, Cottin NT, Fernandes M, Read FL, Urgast DS, Raab A et al (2016) Possible link between Hg and Cd accumulation in the brain of long-finned pilot whales (Globicephala melas). Sci Total Environ 545–546:407–413. https://doi.org/10.1016/j.scitotenv.2015.12.082
Giljov A, Karenina K, Kochnev A (2017) Prey or play: interactions between walruses and seabirds. Acta Ethologica 20:47–57. https://doi.org/10.1007/s10211-016-0248-x
Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338. https://doi.org/10.2307/2333639
Habran S, Debier C, Crocker DE, Houser DS, Das K (2011) Blood dynamics of mercury and selenium in northern elephant seals during the lactation period. Environ Pollut 159:2523–2529. https://doi.org/10.1016/j.envpol.2011.06.019
Habran S, Pomeroy PP, Debier C, Das K (2013) Changes in trace elements during lactation in a marine top predator, the grey seal. Aquat Toxicol 126:455–466. https://doi.org/10.1016/j.aquatox.2012.08.011
Hong YS, Hunter S, Clayton LA, Rifkin E, Bouwer EJ (2012) Assessment of mercury and selenium concentrations in captive bottlenose dolphin’s (Tursiops truncatus) diet fish, blood, and tissue. Sci Total Environ 414:220–226. https://doi.org/10.1016/j.scitotenv.2011.11.021
Houde M, Taranu ZE, Wang X, Young B, Gagnon P, Ferguson SH, Kwan M et al (2020) Mercury in ringed seals (Pusa hispida) from the Canadian Arctic in relation to time and climate parameters. Environ Toxicol Chem 39:2462–2474. https://doi.org/10.1002/etc.4865
Huggins FE, Raverty SA, Nielsen OS, Sharp NE, Robertson JD, Ralston NVC (2009) An XAFS Investigation of mercury and selenium in beluga whale tissues. Environ Bioindic 4:291–302. https://doi.org/10.1080/15555270903404651
Huntington HP, Noongwook G, Bond NA, Benter B, Snyder JA, Zhang J (2013) The influence of wind and ice on spring walrus hunting success on St. Lawrence Island, Alaska. Deep Sea Res Part II Top Stud Oceanogr 94:312–322. https://doi.org/10.1016/j.dsr2.2013.03.016
Ikemoto T, Kunito T, Tanaka H, Baba N, Miyazaki N, Tanabe S (2004) Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch Environ Contam Toxicol 47:402–413. https://doi.org/10.1007/s00244-004-3188-9
Jay CV, Outridge PM, Garlich-Miller JL (2008) Indication of two Pacific walrus stocks from whole tooth elemental analysis. Polar Biol 31:933–943. https://doi.org/10.1007/s00300-008-0432-1
Jay CV, Taylor RL, Fischbach AS, Udevitz MS, Beatty WS (2017) Walrus haul-out and in water activity levels relative to sea ice availability in the Chukchi Sea. J Mamm 98:386–396. https://doi.org/10.1093/jmammal/gyw195
Krey A, Ostertag SK, Chan HM (2015) Assessment of neurotoxic effects of mercury in beluga whales (Delphinapterus leucas), ringed seals (Pusa hispida), and polar bears (Ursus maritimus) from the Canadian Arctic. Sci Total Environ 509–510:237–247. https://doi.org/10.1016/j.scitotenv.2014.05.134
Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47:13385–13394. https://doi.org/10.1021/es403103t
Lian M, Castellini JM, Kuhn T, Rea L, Bishop L, Keogh M, Kennedy SN et al (2020) Assessing oxidative stress in Steller sea lions (Eumetopias jubatus): associations with mercury and selenium concentrations. Comp Biochem Physiol C Toxicol Pharmacol. https://doi.org/10.1016/j.cbpc.2020.108786
Lovvorn JR, Wilson JJ, McKay D, Bump JK, Cooper LW, Grebmeier JM (2010) Walruses attack spectacled eiders wintering in pack ice of the bering sea. Arctic 63:53–56. https://doi.org/10.14430/arctic646
Lowry LF, Fay FH (1984) Seal eating by walruses in the Bering and Chukchi Seas. Polar Biol 3:11–18. https://doi.org/10.1007/BF00265562
Lyytikäinen M, Pätynen J, Hyvärinen H, Sipilä T, Kunnasranta M (2015) Mercury and selenium balance in endangered Saimaa ringed seal depend on age and sex. Environ Sci Technol 49:11808–11816. https://doi.org/10.1021/acs.est.5b01555
Maniscalco JM, Springer AM, Counihan KL, Hollmen T, Aderman HM, Toyukak M Sr (2020) Contemporary diets of walruses in Bristol Bay, Alaska suggest temporal variability in benthic community structure. PeerJ 8:e8735. https://doi.org/10.7717/peerj.8735
Miles AK, Miles AK, Miles AK, Hills S, Hills S, Hills S (1994) Metals in diet of Bering Sea walrus: Mya spp. as a possible transmitter of elevated cadmium and other metals. Mar Pollut Bull 28:456–458. https://doi.org/10.1016/0025-326X(94)90133-3
Mistry HD, Broughton Pipkin F, Redman CWG, Poston L (2012) Selenium in reproductive health. Am J Obstet Gynecol 206:21–30. https://doi.org/10.1016/j.ajog.2011.07.034
Morrison JO, Campbell IT, Brand U (1999) Arsenic pollution and toxicity. Environmental geology. Springer, Netherlands, Dordrecht, pp 36–37
Moulis J-M (2010) Cellular mechanisms of cadmium toxicity related to the homeostasis of essential metals. Biometals 23:877–896. https://doi.org/10.1007/s10534-010-9336-y
Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16:917–927. https://doi.org/10.1002/etc.5620160511
Neitlich PN, Hoef JMV, Berryman SD, Mines A, Geiser LH, Hasselbach LM, Shiel AE (2017) Trends in spatial patterns of heavy metal deposition on national park service lands along the Red Dog Mine haul road, Alaska, 2001–2006. PLoS ONE 12:e0177936. https://doi.org/10.1371/journal.pone.0177936
Nigro M, Leonzio C (1996) Intracellular storage of mercury and selenium in different marine vertebrates. Mar Ecol Prog Ser 135:137–143. https://doi.org/10.3354/meps135137
Noël M, Jeffries S, Lambourn DM, Telmer K, Macdonald R, Ross PS (2016) Mercury accumulation in harbour seals from the Northeastern Pacific ocean: the role of transplacental transfer, lactation, age and location. Arch Environ Contam Toxicol 70:56–66. https://doi.org/10.1007/s00244-015-0193-0
Noren S, Udevitz M, Jay C (2012) Bioenergetics model for estimating food requirements of female Pacific walruses Odobenus rosmarus divergens. Mar Ecol Prog Ser 460:261–275. https://doi.org/10.3354/meps09706
Ojeda ML, Nogales F, Serrano A, Murillo ML, Carreras O (2019) Maternal metabolic syndrome and selenium: Endocrine energy balance during early programming. Life Sci 233:116689. https://doi.org/10.1016/j.lfs.2019.116689
Ojeda ML, Nogales F, Romero-Herrera I, Carreras O (2021) Fetal programming is deeply related to maternal selenium status and oxidative balance; experimental offspring health repercussions. Nutrients 13:2085. https://doi.org/10.3390/nu13062085
Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, et al (2020) vegan: Community Ecology Package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan. Accessed 7 May 2020
Perrot V, Masbou J, Pastukhov MV, Epov VN, Point D, Bérail S, Becker PR et al (2016) Natural Hg isotopic composition of different Hg compounds in mammal tissues as a proxy for in vivo breakdown of toxic methylmercury†. Metallomics 8:170–178. https://doi.org/10.1039/c5mt00286a
Perryman CR, Wirsing J, Bennett KA, Brennick O, Perry AL, Williamson N, Ernakovich JG (2020) Heavy metals in the Arctic: distribution and enrichment of five metals in Alaskan soils. PLoS ONE 15:e0233297. https://doi.org/10.1371/journal.pone.0233297
Peterson SH, Ackerman JT, Costa DP (2015) Marine foraging ecology influences mercury bioaccumulation in deep-diving northern elephant seals. Proc R Soc B Biol Sci 282:20150710. https://doi.org/10.1098/rspb.2015.0710
Ponce RA, Egeland GM, Middaugh JP, Becker PR (1998) Twenty years of trace metal analyses of marine mammals in Alaska: evaluation and summation. Int J Circumpolar Health 57:576–581
Quakenbush LT, Bryan A, Nelson M, Jonathan Snyder (2016a) Pacific walrus (Odobenus rosmarus divergens) Saint Lawrence Island harvest samples analysis, 2012–2014 and 2016a. Alaska Department of Fish and Game, US Fish and Wildlife Service 61 pp. [This report is available on ADFG website]
Quakenbush LT, Crawford JA, Citta JJ, Nelson MN (2016b) Pinniped movements and foraging: village-based walrus habitat use studies in the Chukchi Sea. U.S. Dept. of the Interior, Bureau of Ocean Energy Management, Alaska Outer Continental Shelf Region, Anchorage, Alaska. OCS Study BOEM 2016b-053. 82 pp+ appendices
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 7 May 2020
Rahman MdM, Hossain KFB, Banik S, Sikder MdT, Akter M, Bondad SEC, Rahaman MdS et al (2019) Selenium and zinc protections against metal-(loids)-induced toxicity and disease manifestations: a review. Ecotoxicol Environ Saf 168:146–163. https://doi.org/10.1016/j.ecoenv.2018.10.054
Ray GC, McCormick-Ray J, Berg P, Epstein HE (2006) Pacific walrus: benthic bioturbator of Beringia. J Exp Mar Biol Ecol 330:403–419. https://doi.org/10.1016/j.jembe.2005.12.043
Raymond LJ, Ralston NVC (2009) Selenium’s importance in regulatory issues regarding mercury. Fuel Process Technol 90:1333–1338. https://doi.org/10.1016/j.fuproc.2009.07.012
Rea LD, Castellini JM, Avery JP, Fadely BS, Burkanov VN, Rehberg MJ, O’Hara TM (2020) Regional variations and drivers of mercury and selenium concentrations in Steller sea lions. Sci Total Environ 744:140787. https://doi.org/10.1016/j.scitotenv.2020.140787
Rodrigues J (2009) The increase in the length of the ice-free season in the Arctic. Cold Reg Sci Technol 59:78–101. https://doi.org/10.1016/j.coldregions.2009.05.006
Rosa C, Blake JE, Bratton GR, Dehn L-A, Gray MJ, O’Hara TM (2008) Heavy metal and mineral concentrations and their relationship to histopathological findings in the bowhead whale (Balaena mysticetus). Sci Total Environ 399:165–178. https://doi.org/10.1016/j.scitotenv.2008.01.062
RStudio Team (2022) RStudio: Integrated development environment for R. RStudio, PBC, Boston, MA. https://www.rstudio.com/. Accessed 7 May 2020
Sakai T, Wilbur S (2015) Ultra-trace ICP-MS Analysis of metals in mineral reference materials. Agilent Technologies, Santa Clara. https://www.agilent.com/cs/library/applications/5991-6406EN_AppNote_ICP-MS_MS-7900_mining.pdf. Accessed 15 July 2022
Sakamoto M, Itai T, Yasutake A, Iwasaki T, Yasunaga G, Fujise Y, Nakamura M et al (2015) Mercury speciation and selenium in toothed-whale muscles. Environ Res 143:55–61. https://doi.org/10.1016/j.envres.2015.09.010
Searle SR (1987) Linear models for unbalanced data. Wiley, New York
Seewagen CL, Cristol DA, Gerson AR (2016) Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird. Sci Rep 6:25762. https://doi.org/10.1038/srep25762
Seymour J, Horstmann-Dehn L, Wooller MJ (2014) Proportion of higher trophic-level prey in the diet of Pacific walruses (Odobenus rosmarus divergens). Polar Biol 37:941–952. https://doi.org/10.1007/s00300-014-1492-z
Sheffield G, Grebmeier JM (2009) Pacific walrus (Odobenus rosmarus divergens): differential prey digestion and diet. Mar Mamm Sci 25:761–777. https://doi.org/10.1111/j.1748-7692.2009.00316.x
Singh K, Bjerregaard P, Man Chan H (2014) Association between environmental contaminants and health outcomes in indigenous populations of the Circumpolar North. Int J Circumpolar Health 73:25808. https://doi.org/10.3402/ijch.v73.25808
Spiller HA (2018) Rethinking mercury: the role of selenium in the pathophysiology of mercury toxicity. Clin Toxicol 56:313–326. https://doi.org/10.1080/15563650.2017.1400555
Stern GA, Macdonald RW, Outridge PM, Wilson S, Chételat J, Cole A, Hintelmann H et al (2012) How does climate change influence arctic mercury? Sci Total Environ 414:22–42. https://doi.org/10.1016/j.scitotenv.2011.10.039
Taylor DL, Schliebe S, Metsker H (1989) Contaminants in blubber, liver and kidney tissue of Pacific walruses. Mar Pollut Bull 20:465–468. https://doi.org/10.1016/0025-326X(89)90069-6
Trukhin AM, Simokon MV (2018) Mercury in organs of Pacific walruses (Odobenus rosmarus divergens) from the Bering Sea. Environ Sci Pollut Res 25:3360–3367. https://doi.org/10.1007/s11356-017-0566-1
Trumble SJ, Robinson EM, Noren SR, Usenko S, Davis J, Kanatous SB (2012) Assessment of legacy and emerging persistent organic pollutants in Weddell seal tissue (Leptonychotes weddellii) near McMurdo Sound, Antarctica. Sci Total Environ 439:275–283. https://doi.org/10.1016/j.scitotenv.2012.09.018
Tsygankov VYu, Boyarova MD, Lukyanova ON (2014) Persistent toxic substances in the muscles and liver of the pacific walrus (Odobenus rosmarus divergens Illiger, 1815) from the Bering Sea. Russ J Mar Biol 40:147–151. https://doi.org/10.1134/S1063074014020102
Udevitz MS, Taylor RL, Garlich-Miller JL, Quakenbush LT, Snyder JA (2013) Potential population-level effects of increased haulout-related mortality of Pacific walrus calves. Polar Biol 36:291–298. https://doi.org/10.1007/s00300-012-1259-3
Udevitz MS, Jay CV, Taylor RL, Fischbach AS, Beatty WS, Noren SR (2017) Forecasting consequences of changing sea ice availability for Pacific walruses. Ecosphere 8:e02014. https://doi.org/10.1002/ecs2.2014
USEPA (1998) Method 1630: Methyl mercury in water by distillation, aqueous ethylation, purge and trap, and cold vapor atomic fluorescence spectrometry. United States Environmental Protection Agency. https://www.epa.gov/sites/default/files/2015-08/documents/method_1630_1998.pdf. Accessed 19 October 2020
USEPA (2001) Appendix to method 1631 total mercury in tissue, sludge, sediment, and soil by acid digestion and BrCl oxidation. Unites States Environmental Protection Agency. https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=40001F6A.txt. Accessed 19 October 2020
USEPA (2002) Method 1631, Revision E: Mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry. Unites States Environmental Protection Agency. https://www.epa.gov/sites/default/files/2015-08/documents/method_1631e_2002.pdf. Accessed 19 October 2020
USEPA (2016) Definition and procedure for the determination of the method detection limit, revision 2. United States Environmental Protection Agency. https://www.epa.gov/sites/default/files/2016-12/documents/mdl-procedure_rev2_12-13-2016.pdf. Accessed 1 February 2022.
Vacchina V, Dumont J (2018) Total selenium quantification in biological samples by inductively coupled plasma mass spectrometry (ICP-MS). In: Chavatte L (ed) Selenoproteins. Methods in Molecular Biology, vol 1661. Springer, New York, NY, pp 145–152. https://doi.org/10.1007/978-1-4939-7258-6_10
Wagemann R, Stewart REA, Lockhart WL, Stewart BE, Povoledo M (1988) Trace metals and methyl mercury: associations and transfer in hapr seal (Phoca groenlandica) mothers and their pups. Mar Mamm Sci 4:339–355. https://doi.org/10.1111/j.1748-7692.1988.tb00542.x
Wagemann R, Innes S, Richard PR (1996) Overview and regional and temporal differences of heavy metals in Arctic whales and ringed seals in the Canadian Arctic. Sci Total Environ 186:41–66. https://doi.org/10.1016/0048-9697(96)05085-1
Wagemann R, Trebacz E, Boila G, Lockhart W (1998) Methylmercury and total mercury in tissues of arctic marine mammals. Sci Total Environ 218:19–31. https://doi.org/10.1016/S0048-9697(98)00192-2
Wang X, Luo J, Yuan W, Lin C-J, Wang F, Liu C, Wang G et al (2020) Global warming accelerates uptake of atmospheric mercury in regions experiencing glacier retreat. Proc Natl Acad Sci 117:2049–2055. https://doi.org/10.1073/pnas.1906930117
Wang Q, Zhan S, Liu Y, Han F, Shi L, Han C, Mu W et al (2021) Low-Se diet can affect sperm quality and testicular glutathione peroxidase-4 activity in rats. Biol Trace Elem Res 199:3752–3758. https://doi.org/10.1007/s12011-020-02515-y
Welfinger-Smith G, Minholz JL, Byrne S, Waghiyi V, Gologergen J, Kava J, Apatiki M et al (2011) Organochlorine and metal contaminants in traditional foods from St. Lawrence Island. Alaska J Toxicol Environ Health A 74:1195–1214. https://doi.org/10.1080/15287394.2011.590099
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wood JM, Cheh A, Dizikes LJ, Ridley WP, Rakow S, Lakowicz JR (1978) Mechanisms for the biomethylation of metals and metalloids. Fed Proc U S 37:1
Woshner VM, O’Hara TM, Bratton GR, Beasley VR (2001) Concentrations and interactions of selected essential and non-essential elements in ringed seals and polar bears of arctic Alaska. J Wildl Dis 37:711–721. https://doi.org/10.7589/0090-3558-37.4.711
Zar JH (2014) Spearman rank correlation: overview. In: Balakrishnan N, Colton T, Everett W, Piegorsch F, Ruggeri F, Teugels JL (eds) Wiley StatsRef Statistics Reference Online. https://doi.org/10.1002/9781118445112.stat05964
Zhang Y, Soerensen AL, Schartup AT, Sunderland EM (2020) A global model for methylmercury formation and uptake at the base of marine food webs. Glob Biogeochem Cycles 34:e2019GB00 6348. https://doi.org/10.1029/2019GB006348
Zwolak I, Zaporowska H (2012) Selenium interactions and toxicity: a review. Cell Biol Toxicol 28:31–46. https://doi.org/10.1007/s10565-011-9203-9
Acknowledgements
The authors would like to thank the Alaska Native subsistence hunters of Gambell, Savoonga, Utqiaġvik, and Wainwright for making the tissue samples available and compiling the information on animal sex and female reproductive status. We thank the U.S. Fish and Wildlife Service, Alaska Department of Fish and Game, and the North Slope Borough Department of Wildlife Management for coordinating with the Alaska Native communities and delivering the samples to Baylor University. We thank Lori Quakenbush with the Alaska Department of Fish and Game for her editing and intellectual contributions to the paper. We thank the Baylor University Molecular Biosciences Center, Alejandro Ramirez, and the Baylor University Mass Spectrometry Center for equipment access and support. We finally thank the anonymous reviewers for their helpful comments.
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This research was funded by a grant from the C. Gus Glasscock, Jr. Endowed Fund for Excellence in Environmental Sciences.
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All authors contributed to the study’s conception and design. Acquisition of samples and coordination with Alaska Native subsistence hunters was performed by JS and LH. Material preparation, data collection, and analysis were performed by GG. The first draft of the manuscript was written by GG, and all authors commented on previous versions of the manuscript. Funding was acquired by GG. The project was supervised by ST. All authors read and approved the final manuscript.
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Samples were obtained by the U.S. Fish and Wildlife Services in cooperation with Alaska Native subsistence hunters under a letter of authorization to L. Horstmann.
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Research involving opportunistically attained samples from subsistence harvests is exempt from Institutional Animal Care and Use Committee approval at the University of Alaska Fairbanks. Baylor University Institutional Animal Care and Use Committee deemed approval unnecessary as the research did not involve live animals.
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Godfrey, G.L., Horstmann, L., Snyder, J. et al. Toxic and essential trace element concentrations in Pacific walrus (Odobenus rosmarus divergens) skeletal muscle varies by location and reproductive status. Polar Biol 45, 1271–1289 (2022). https://doi.org/10.1007/s00300-022-03069-6
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DOI: https://doi.org/10.1007/s00300-022-03069-6