Abstract
Concentrations of 22 essential and non-essential trace elements (Be, Al, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Mo, Ag, Cd, Sb, Ba, Tl, Pb, Th, U, and Hg) were measured in the organs of a mother–fetus pair (at the last trimester of pregnancy) of spotted seals from the Sea of Japan. The concentrations of eleven elements are reported for the first time. Eight organs of the pair were examined: lungs, heart, liver, kidneys, intestines, spleen, muscles, and bones. All trace elements detected in the organs of the mother were found also in the organs of the fetus at various concentrations. Placenta is not an effective barrier to prevent non-essential elements from getting into the fetus, but can control entry of some of them, e.g., aluminum, cadmium, and mercury. In most organs of the fetus, the concentrations of toxic trace elements (beryllium, antimony, thorium, and uranium) were noticeably higher than in the same organs of the mother, which indicates that during pregnancy female removes excess of non-essential trace elements by transferring them to the fetal body through the placental barrier.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agusa T, Nomura K, Kunito T, Anan Y, Iwata H, Tanabe S (2011a) Accumulation of trace elements in harp seals (Phoca groenlandica) from Pangnirtung in the Baffin Island, Canada. Mar Pollut Bull 63:489–499. https://doi.org/10.1016/j.marpolbul.2011.02.022
Agusa T, Yasugi S, Iida A, Ikemoto T, Anan Y, Kuiken T (2011b) Accumulation features of trace elements in mass-stranded harbour seal (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
Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184:97–149. https://doi.org/10.1007/0-387-27565-7_3
AMAP (2011) AMAP assessment 2011: mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo 210 pp
Anke M (2004) Vanadium - an element both essential and toxic to plants, animals and humans? Anal Real Acad Nac Farm 70:961–999
Arinola OG, Nwozo SO, Ajiboye JA, Oniye AH (2008) Evaluation of trace elements and total antioxidant status in Nigerian cassava processors. Pak J Nutr 7:770–772. https://doi.org/10.3923/pjn.2008.770.772
Asagba SO (2007) Alterations in activities of tissue enzymes in oral cadmium toxicity. Niger J Sci Env 6:91–102
Asagba SO, Obi FO (2005) A comparative evaluation of the biological effects of environmental cadmium contaminated control diet and laboratory cadmium supplemented test diet. Biometals 18:155–161. https://doi.org/10.1007/s10534-004-4257-2
ATSDR (1999) Toxicological profile for uranium. U.S. Department of Health and Human Services. Agency for Toxic Substances and Disease Registry, Atlanta, GA
Barabasz W, Albinska D, Jaskowska M, Lipiec J (2002) Ecotoxicology of aluminium. Pol J Environ Stud 11:199–203. https://doi.org/10.1023/A:1015474832239
Baranski B, Stetkiewicz I, Trzcinka-Ochocka M, Sitarek K, Szymczak W (1982) Teratogenicity, fetal toxicity and tissue concentration of cadmium administered to female rats during organogenesis. J Appl Toxicol 2:255–259. https://doi.org/10.1002/jat.2550020508
Bates JM, Spate VL, Morris JS, Germain DLS, Galton VA (2000) Effects of selenium deficiency on tissue selenium content, deiodinase activity, and thyroid hormone economy in the rat during development. Endocrinology 141:2490–2500. https://doi.org/10.1210/endo.141.7.7571
Bedwal RS, Bahuguna A (1994) Zinc, copper and selenium in reproduction. Experientia (Basel) 50:626–640. https://doi.org/10.1007/BF01952862
Brookens TJ, Harvey JT, O’Hara TM (2007) Trace element concentrations in the Pacific harbor seal (Phoca vitulina richardii) in central and northern California. Sci Total Environ 372:676–692. https://doi.org/10.1016/j.scitotenv.2006.10.006
Brown TM, Macdonald RW, Muir DCG, Letcher RJ (2018) The distribution and trends of persistent organic pollutants and mercury in marine mammals from Canada’s Eastern Arctic. Sci Total Environ 618:500–517. https://doi.org/10.1016/j.scitotenv.2017.11.052
Bryan CE, Christopher SJ, Balmer BC, Wells RS (2007) Establishing baseline levels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida: implications for non-invasive monitoring. Sci Total Environ 388:325–342. https://doi.org/10.1016/j.scitotenv.2007.07.046
Burrell RE (2003) A scientific perspective on the use of topical silver preparations. Ostomy Wound Manage 49:19–24
Campbell LM, Norstrom RJ, Hobson KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351–352:247–263. https://doi.org/10.1016/j.scitotenv.2005.02.043
Caserta D, Graziano A, Lo Monte G, Bordig G, Moscarini M (2013) Heavy metals and placental fetal-maternal barrier: a mini-review on the major concerns. Eur Rev Med Pharmacol Sci 17:2198–2206
Chater S, Douki T, Favier A, Sakly M, Abdelmelek H (2009) Changes in antioxidant status and biochemical parameters after oral cadmium administration in female rats. Acta Biol Hung 60:79–88. https://doi.org/10.1556/ABiol.60.2009.1.8
Cuvin-Aralar ML, Furness RW (1991) Mercury and selenium interaction: a review. Ecotoxicol Environ Saf 21:348–364. https://doi.org/10.1016/0147-6513(91)90074-Y
Das K, Debacker V, Bouquegneau JM (2000) Metallothioneins in marine mammals. Cell Mol Biol 46:283–294
Das KK, Reddy RC, Bagogi IB, Das S, Bagali S, Mullur L, Khodnapur JP, Biradar MS (2019) Primary concept of nickel toxicity – an overview. J Basic Clin Physiol Pharmacol 30:141–152. https://doi.org/10.1515/jbcpp-2017-0171
Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, Bratton GR, Taylor RJ, O’Hara TM (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
Dietz R, Riget F, Born EW (2000) An assessment of selenium to mercury in Greenland marine animals. Sci Total Environ 245:15–24. https://doi.org/10.1016/S0048-9697(99)00430-1
Dietz R, Sonne C, Basu N, Braune B, O’Hara T (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
Eisler R (1988) Lead hazards to fish, wildlife, and invertebrates: a synoptic review. Biological Report 85. U.S. Fish and Wildlife Service. Lauel, MD
Enomoto S, Hirunuma R (2001) Fetoplacental transport of various trace elements in pregnant rat using the multitracer technique. RIKEN Review 35:31–34 http://www.riken.go.jp/lab-www/library/publication/review/contents.html
Finley JW, Davis CD (1999) Manganese deficiency and toxicity: are high or low dietary amounts of manganese cause for concern? Biofactors 10:15–24. https://doi.org/10.1002/biof.5520100102
Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress and its possible reversal by chelation therapy. Indian J Med Res 128:501–523
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
Fujise Y, Honda K, Tatsukawa R, Mishima S (1988) Tissue distribution of heavy metals in Dall’s porpoises in the Northwestern Pacific. Mar Pollut Bull 19:226–230. https://doi.org/10.1016/0025-326X(88)90236-6
Ganz T (2013) Systemic iron homeostasis. Physiol Rev 93:1721–1741. https://doi.org/10.1152/physrev.00008.2013
Goyer RA (1990) Transpiacental transport of lead. Environ Health Perspect 89:101–105. https://doi.org/10.1289/ehp.9089101
Grajewska A, Falkowska L, Saniewska D, Pawliczka I (2019) Changes in total mercury, methylmercury and selenium blood levels in the different life history stages of the Baltic grey seal (Halichoerus grypus grypus). Sci Total Environ 1:268–277. https://doi.org/10.1016/j.scitotenv.2019.04.204
Great Medical Encyclopedia (1984) Petrovskiy BV (ed) 3rd edition. Soviet Encyclopedia, Moscow, vol 19 536 pp
Greig DJ, Ylitalo GM, Hall AJ, Fauquier DA, Gulland FMD (2007) Transplacental transfer of organochlorines in California sea lions (Zalophus californianus). Environ Toxicol Chem 26:37–44. https://doi.org/10.1897/05-609R.1
Greig DJ, Ylitalo GM, Wheeler EA, Boyd D, Gulland FMD, Yanagida GK, Harvey JT, Hall A (2011) Geography and stage of development affect persistent organic pollutants in stranded and wild-caught harbor seal pups from central. California Sci Total Environ 409:3537–3547. https://doi.org/10.1016/j.scitotenv.2011.05.047
Gundacker C, Hengstschläger M (2012) The role of the placenta in fetal exposure to heavy metals. Wien Med Wochenschr 162:201–206. https://doi.org/10.1007/s10354-012-0074-3
Habran S, Das K, Pomeroy PP, Debier C (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
Hanlon DP, Specht C, Ferm VH (1982) The chemical status of cadmium ion in the placenta. Environ Res 27:89–94. https://doi.org/10.1016/0013-9351(82)90060-3
Hanzel CE, Verstraeten SV (2005) Thallium induces hydrogen peroxide generation by impairing mitochondrial function. Toxicol Appl Pharmacol 216:485–492. https://doi.org/10.1016/j.taap.2006.07.003
Harris H, Pickering IJ, George GN (2003) The chemical form of mercury in fish. Science 301:1203. https://doi.org/10.1126/science.1085941
Hirunuma R, Ozaki T, Endo K, Yasui H, Sakurai H, Enomoto S (2001) Uptake of various elements in selenium deficient rats: Application of the multitracer technique. RIKEN Rev 35:40–44 http://www.riken.go.jp/lab-www/library/publication/review/contents.html
Itano K, Kawai S (1981) Mercury and selenium levels in the striped dolphins in the Pacific coast of Japan. In: Fujiyama T (ed) Studies on the levels of organochlorine compounds and heavy metals in the marine organism. University of the Ryukyus, pp 73–84
Itoh N, Fujita Y, Nakanishi H, Kawai Y, Mayumi T, Hawang GS et al (1996) Binding of Cd to metallothionein in the placenta of Cd-treated mouse. J Toxicol Sci 21:19–27. https://doi.org/10.2131/jts.21.19
Jaishankar M, Mathew BB, Shah MS, Gowda KRS (2014a) Biosorption of few heavy metal ions using agricultural wastes. Journal of Environment Pollution and Human Health 2(1):1–6
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014b) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72. https://doi.org/10.2478/intox-2014-0009
Khan MA, Wang F (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem 28:1567–1577. https://doi.org/10.1897/08-375.1
Koeman JH, Peeters WHM, Koudstaal-Hol CHM, Tjioe PS, De Goeij JJM (1973) Mercury-selenium correlations in marine mammals. Nature 245:385–386. https://doi.org/10.1038/245385a0
Krahn MM, Hanson MB, Schorr GS, Emmons CK, Burrows DG, Bolton JL, Baird RW, Ylitalo GM (2009) Effects of age, sex and reproductive status on persistent organic pollutant concentrations in “Southern Resident” killer whales. Mar Pollut Bull 58:1522–1529. https://doi.org/10.1016/j.marpolbul.2009.05.014
Kubota R, Kunito T, Fujihara J, Tanabe S, Yang J, Miyazaki N (2005) Placental transfer of arsenic to fetus of Dall_s porpoises (Phocoenoides dalli). Mar Pollut Bull 51:845–849. https://doi.org/10.1016/j.marpolbul.2005.01.011
Kuriwaki J, Nishijo M, Honda R, Tawara K, Nakagawa H, Hori E, Nishijo H (2005) Effects of cadmium exposure during pregnancy on trace elements in fetal rat liver and kidney. Toxicol Lett 156:369–376. https://doi.org/10.1016/j.toxlet.2004.12.009
Lahaye V, Bustamante P, Dabin W, Churlaud C, Caurant F (2007) Trace element levels in foetus–mother pairs of short-beaked common dolphins (Delphinus delphis) stranded along the French coasts. Environ Int 33:1021–1028. https://doi.org/10.1016/j.envint.2007.05.008
Leonard A, Gerber GB (1997) Mutagenicity, carcinogenicity and teratogenicity of thallium compounds. Mutat Res Rev 387:47–53. https://doi.org/10.1016/S1383-5742(97)00022-7
Lindenschmidt RC, Sendelbach LE, Witschi HP, Price DJ, Joshi JG (1986) Ferritin and in vivo beryllium toxicity. Toxicol And Applied Pharmacol 82:344–350. https://doi.org/10.1016/0041-008X(86)90211-5
Meador JP, Varanasi U, Robish PA, Chan S (1993) Toxic metals in pilot whale (Globicephala melaena) from stranding in 1986 and 1990 on Cape Cod, Massachusetts. Can J Fish Aquat Sci 50:2698–2706. https://doi.org/10.1139/f93-294
Nehring I, Grajewska A, Falkowska L, Staniszewska M, Pawliczka I, Saniewskaet D (2017) Transfer of mercury and phenol derivatives across the placenta of Baltic grey seals (Halichoerus grypus grypus). Environ Pollut 231:1005–1012. https://doi.org/10.1016/j.envpol.2017.08.094
Nielsen FH (1976) Trace elements in human health and disease. Academic Press, New York
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
O’Hara T, Woshner V, Bratton G (2003) Inorganic pollutants in Arctic marine mammals. In: Vos JG, Bossart BG, Fournier M, O’Shea TJ (eds) Toxicology of marine mammals. Taylor and Francis, London and New York, pp 206–246
Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228. https://doi.org/10.3390/ijms140510197
Pandey G, Mandhuri S (2014) Heavy metals causing toxicity in animals and fishes. Res J Animal Veterinary Fish Sci 2:17–23
Rajagopalan KR (1987) Molybdenum - an essential trace element. Nutr Rev 45:321–328. https://doi.org/10.1111/j.1753-4887.1987.tb00981.x
Ralston NVC, Ralston CR, Blackwell JL III, Raymond LJ (2008) Dietary and tissue selenium in relation to methymercury toxicity. Neurobehav Toxicol 29:802–811. https://doi.org/10.1016/j.neuro.2008.07.007
Rea LD, Castellini JM, Correa L, Fadely BS, O’Hara TM (2013) Maternal Steller sea lion diets elevate fetal mercury concentrations in an area of population decline. Sci Total Environ 454-455:277–282. https://doi.org/10.1016/j.scitotenv.2013.02.095
Saha A, Karnik A, Sathawara N, Kulkarni P, Singh V (2008) Ceruloplasmin as a marker of occupational copper exposure. Journal of Exposure Science and Environmental Epidemiology 18:332–337. https://doi.org/10.1038/jes.2008.2
Shaughnessy PD, Fay FH (1977) A review of taxonomy and nomenclature of North Pacific harbor seals. J Zool 182:385–419. https://doi.org/10.1111/j.1469-7998.1977.tb03917.x
Sokol RZ, Saixi W, Yu-Jui Y, Frank ZS, Elizabeth G, Robert EC (2002) Long-term, low-dose lead exposure alters the gonadotropin-releasing hormone system in the male rat. Environ Health Perspect 110:871–874. https://doi.org/10.1289/ehp.02110871
Sullivan JB Jr (1992) Hazardous materials toxicology: clinical principles of environmental health. Williams & Wilkins, Baltimore
Sunagawa S (1981) Experimental studies on antimony poisoning. Igaku Kenkyu 51:129–142
Thorium (1995) Chemistry Encyclopedia. V.4. Zefirov NS (ed). Moscow, Great Soviet Encyclopedia (In Russian).
Tikhomirov EA, Klevezal GA (1964) Methods for determining the age of some pinnipeds. In: Kleinenberg SE (ed) Determination of the age of commercial pinnipeds and rational use of marine mammals. Science, Moscow, pp 5–20 (In Russian)
Trukhin AM (2005) Spotted seal (In Russian). Dal’nauka, Vladivostok
Trukhin AM (2015) Current abundance of spotted seal (Phoca largha) in Peter the Great Bay (Japan Sea): unstable equilibrium or sustainable growth? Izvestiya TINRO 182:48–54 (In Russian)
Trukhin AM (2019) Spotted seal (Phoca largha) population increase in the Peter the Great Bay, Sea of Japan. Mar Mamm Sci 35:1183–1191. https://doi.org/10.1111/mms.12588
Trukhin AM, Boyarova MD (2013) Chlorinated pesticides in tissues and organs of spotted seals (Phoca largha Pallas, 1811) from the Sea of Japan. Contemp Probl Ecol 6:336–342. https://doi.org/10.1134/S199542551303013X
Trukhin AM, Boyarova MD (2020) Organochlorine pesticides (HCH and DDT) in blubber of spotted seals (Phoca largha) from the western Sea of Japan. Mar Pollut Bull 150:110738. https://doi.org/10.1016/j.marpolbul.2019.110738
Trukhin AM, Kalinchuk VV (2018) Hair mercury concentrations in the spotted seal (Phoca largha) pup from the Sea of Japan. Environ Sci Pollut Res 25:27133–27140. https://doi.org/10.1007/s11356-018-2731-6
Trukhin AM, Slin’ko EN, Kolosova LF (2012) Microelements of the metal group in organs of spotted seal (Phoca largha) from the Japan Sea. Izvestiya TINRO 169:110–117 (In Russian)
Trukhin AM, Kolosova LF, Slin’ko EN (2015) Transfer certain of trace metals from maternal tissues to the fetus in the walruses (Odobenus rosmarus divergens Linnaeus, 1785). Marine mammals of the Holarctic 2:218–221
Ventura-Lima J, Castro MR, Acosta D, Fattorini D, Regoli F, Carvalho LM, Bohrer D, Geracitano LA, Barros DM, Silva RS, Bonan CD, Bogo MR, Monserrat JM (2009) Effects of arsenic (As) exposure on the antioxidant status of gills of the zebrafish Danio rerio (Cypridinae). Comp Biochem Physiol 149:538–543. https://doi.org/10.1016/j.cbpc.2008.12.003
Volosovets AP (2012) On the role of of zinc in clinical pediatrics. Dityachiy likar 5:37–39 (In Russian)
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. Mar Mamm Sci 4:339–355. https://doi.org/10.1111/j.1748-7692.1988.tb00542.x
Weijs L, Dirtu AC, Das K, Gheorghe A, Reijnders PJH, Neels H, Blust R, Covaci A (2009) Interspecies differences for polychlorinated biphenyls and polybrominated diphenyl ethers in marine top predators from the Southern North Sea: Part 1. Accumulation patterns in harbour seals and harbour porpoises. Environ Pollut 157:437–444. https://doi.org/10.1016/j.envpol.2008.09.024
Wolkers H, Lydersen C, Kovacs KM (2004) Accumulation and lactational transfer of PCBs and pesticides in harbor seals (Phoca vitulina) from Svalbard, Norway. Sci Total Environ 319:137–146. https://doi.org/10.1016/S0048-9697(03)00449-2
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
Yang J, Kunito T, Anan Y, Tanabe S, Miyazaki N (2004) Total and subcellular distribution of trace elements in the liver of a mother–fetus pair of Dall’s porpoises (Phocoenoides dalli). Mar Pollut Bull 48:1122–1129. https://doi.org/10.1016/j.marpolbul.2003.12.019
Yang DY, Chen YW, Gunn JM, Belzile N (2008) Selenium and mercury in organisms: interactions and mechanisms. Environ Rev 16:71–92. https://doi.org/10.1139/A08-001
Ylitalo GM, Stein JE, HomT JLL, Tilbury KL, Hall AJ, Rowles T, Greig D, Lowenstine LJ, Gulland FMD (2005) The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus). Mar Pollut Bull 50:30–39. https://doi.org/10.1016/j.marpolbul.2004.08.005
Acknowledgements
The authors are grateful to Leonid Pavin who informed us about the spotted seal carcass found on Russky Island that we used in the study. Many thanks are due to Evgeny Shvetsov for translating the manuscript into English. The map was composed in QGIS 2.4.0 using GADM maps and data (https://gadm.org/data.html).
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
Author information
Authors and Affiliations
Contributions
Conceptualization: MVS AMT
Investigation: MVS AMT
Collection the biological material: AMT
Analysis of samples: MVS
Data interpreted: MVS AMT
Writing—original draft: MVS AMT
Editing after reviewing: MVS AMT
Both authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Disclaimer
The funder had no role in the design of the study; in the collection, analysis, and interpretation of data; or in writing the manuscript.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Simokon, M.V., Trukhin, A.M. Analysis of essential and non-essential trace elements in the organs of a mother–fetus pair of spotted seals (Phoca largha) from the Sea of Japan. Environ Sci Pollut Res 28, 60622–60634 (2021). https://doi.org/10.1007/s11356-021-14971-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14971-7