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Sexual Maturity and Life Stage Influences Toxic Metal Accumulation in Croatian Brown Bears

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Abstract

The influence of reproductive and (early) life stages on toxic metal levels was investigated in the brown bear (Ursus arctos), the largest mammalian predator species in Croatia. The purpose was to examine critical clusters in a population that might be at a higher risk of adverse health effects caused by metals as environmental contaminants. Levels of cadmium, mercury and lead in muscle, liver and kidney cortex of 325 male and 139 female bears, quantified by inductively coupled plasma mass spectrometry, were analysed according to distinct bear life stages (young: cub, yearling, subadult; mature: adult). Metal levels did not differ among sexes in young animals (< 4 years), except for mercury in muscles (higher in females), and adult females had higher cadmium and mercury. A trend of renal cadmium accumulation with age in immature male animals disappeared once they reached maturity, whereas for females this trend has only slowly declined in mature compared to immature bears. In early life stage (< 1 year), bear cubs had lower cadmium, comparable mercury, and higher lead in the kidneys than the bears of the following age category (yearlings). Due to a higher proportion of renal lead transfer from the mother to the cub compared with cadmium, it may be that the high burden of cadmium found in kidneys of older females has lower toxicological concern for their cubs than the lead content. Sex, reproductive, and life stages of bears were confirmed as important in assessing toxic metal burden.

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References

  • ATSDR, Agency for Toxic Substances and Disease Registry (2012) Toxicological profile for Cadmium. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. https://www.atsdr.cdc.gov/toxprofiles/tp5.pdf. Accessed 17 July 2017

  • Bartareau TM, Cluff HD, Larter NC (2011) Body length and mass growth of the brown bear (Ursus arctos) in northern Canada: model selection based on information theory and ontogeny of sexual size dimorphism. Can J Zool 89(11):1128–1135

    Article  Google Scholar 

  • Berglund M, Akesson A, Bjellerup P, Vahter M (2000) Metal-bone interactions. Toxicol Lett 112–113:219–225

    Article  Google Scholar 

  • Berlin M, Zalups RK, Fowler BA (2015) Mercury. In: Nordberg GF, Fowler BA, Nordberg M (eds) Handbook on the toxicology of metals, specific metals, vol II, 4th edn. Academic Press, Amsterdam, pp 1013–1075

    Chapter  Google Scholar 

  • Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC, Mateo R, Rodríguez Fariñas N, Rodríguez-Estival J, Patiño Ropero MJ (2012) Mercury exposure and mechanism of response in large game using the Almadén mercury mining area (Spain) as a case study. Environ Res 112:58–66

    Article  CAS  Google Scholar 

  • Binkowski ŁJ, Merta D, Przystupińska A, Sołtysiak Z, Pacoń J, Stawarz R (2016) Levels of metals in kidney, liver and muscle tissue and their relation to the occurrence of parasites in the red fox in the Lower Silesian Forest in Europe. Chemosphere 149:161–167

    Article  CAS  Google Scholar 

  • Bjørklund G, Dadar M, Mutter J, Aaseth J (2017) The toxicology of mercury: current research and emerging trends. Environ Res 159:545–554

    Article  Google Scholar 

  • Burger J, Fossi C, McClellan-Green P, Orlando EF (2007) Methodologies, bioindicators, and biomarkers for assessing gender-related differences in wildlife exposed to environmental chemicals. Environ Res 104(1):135–152

    Article  CAS  Google Scholar 

  • Bushnell PJ, DeLuca HF (1983) The effects of lactose on the absorption and retention of dietary lead. J Nutr 113(2):365–378

    Article  CAS  Google Scholar 

  • Cicnjak L, Huber Đ, Roth HU, Ruff RL, Vinovrški Z (1987) Food habits of brown bears in Plitvice Lakes National Park, Yugoslavia. Int Conf Bear Res Manage 7:221–226

    Google Scholar 

  • Crête M, Potvin F, Walsh P, Benedetti JL, Lefebvre MA, Weber JP, Paillard G, Gagnon J (1987) Pattern of cadmium contamination in the liver and kidneys of moose and white-tailed deer in Québec. Sci Total Environ 66:45–53

    Article  Google Scholar 

  • Dorea JG (2004) Mercury and lead during breast-feeding. Br J Nutr 92(1):21–40

    Article  CAS  Google Scholar 

  • Farkas A, Bidló A, Bolodár-Varga B, Jánoska F (2017) Accumulation of metals in liver tissues of sympatric golden jackal (Canis aureus) and red fox (Vulpes vulpes) in the southern part of Romania. Bull Environ Contam Toxicol 98(4):513–520

    Article  CAS  Google Scholar 

  • Farley SD, Robbins CT (1995) Lactation, hibernation, and mass dynamics of American black bears and grizzly bears. Can J Zool 73(12):2216–2222

    Article  Google Scholar 

  • Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5(2):47–58

    Article  CAS  Google Scholar 

  • Frković A, Huber Đ, Kusak J (2001) Brown bear litter sizes in Croatia. Ursus 12(12):103–106

    Google Scholar 

  • Gamberg M, Braune BM (1999) Contaminant residue levels in arctic wolves (Canis lupus) from the Yukon Territory, Canada. Sci Total Environ 243–244:329–338

    Article  Google Scholar 

  • Gamberg M, Chételat J, Poulain AJ, Zdanowicz C, Zheng J (2015) Mercury in the Canadian arctic terrestrial environment: an update. Sci Total Environ 509–510:28–40

    Article  Google Scholar 

  • Gnamuš A, Byrne AR, Horvat M (2000) Mercury in the soil-plant-deer-predator food chain of a temperate forest in Slovenia. Environ Sci Technol 34:3337–3345

    Article  Google Scholar 

  • Goering PL, Klaassen CD (1984) Resistance to cadmium-induced hepatotoxicity in immature rats. Toxicol Appl Pharmacol 74(3):321–329

    Article  CAS  Google Scholar 

  • Grandjean P, Bellinger D, Bergman A, Cordier S, Davey-Smith G, Eskenazi B, Gee D, Gray K, Hanson M, van den Hazel P, Heindel JJ, Heinzow B, Hertz-Picciotto I, Hu H, Huang TT, Jensen TK, Landrigan PJ, McMillen IC, Murata K, Ritz B, Schoeters G, Skakkebaek NE, Skerfving S, Weihe P (2008) The faroes statement: human health effects of developmental exposure to chemicals in our environment. Basic Clin Pharmacol Toxicol 102(2):73–75

    CAS  Google Scholar 

  • Hermoso de Mendoza García M, Hernández Moreno D, Soler Rodríguez F, López Beceiro A, Fidalgo Alvarez LE, Pérez López M (2011) Sex- and age-dependent accumulation of heavy metals (Cd, Pb and Zn) in liver, kidney and muscle of roe deer (Capreolus capreolus) from NW Spain. J Environ Sci Health A Tox Hazard Subst Environ Eng 46(2):109–116

    Article  Google Scholar 

  • Hernández-Moreno D, de la Casa Resino I, Fidalgo LE, Llaneza L, Soler Rodríguez F, Pérez-López M, López-Beceiro A (2013) Noninvasive heavy metal pollution assessment by means of Iberian wolf (Canis lupus signatus) hair from Galicia (NW Spain): a comparison with invasive samples. Environ Monit Assess 185(12):10421–10430

    Article  Google Scholar 

  • Hissa R (1997) Physiology of the European brown bear (Ursus arctos arctos). Ann Zool Fenn 34:267–287

    Google Scholar 

  • Horiguchi H, Oguma E, Sasaki S, Miyamoto K, Ikeda Y, Machida M, Kayama F (2004) Comprehensive study of the effects of age, iron deficiency, diabetes mellitus, and cadmium burden on dietary cadmium absorption in cadmium-exposed female Japanese farmers. Toxicol Appl Pharmacol 196(1):114–123

    Article  CAS  Google Scholar 

  • Huber Đ, Kulier I, Poljak A, Devčić-Kuhar B (1993) Food intake and mass gain of hand-reared brown bear cubs. Zoo Biol 12:525–533

    Article  Google Scholar 

  • Järup L, Berglund M, Elinder CG, Nordberg G, Vahter M (1998) Health effects of cadmium exposure–a review of the literature and a risk estimate. Scand J Work Environ Health 24(Suppl 1):1–51

    Google Scholar 

  • Kingsley MCS, Nagy JA, Reynolds HV (1988) Growth in length and weight of northern brown bears: differences between sexes and populations. Can J Zool 66(4):981–986

    Article  Google Scholar 

  • Kippler M, Nermell B, Hamadani J, Tofail F, Moore S, Vahter M (2010) Burden of cadmium in early childhood: longitudinal assessment of urinary cadmium in rural Bangladesh. Toxicol Lett 198(1):20–25

    Article  CAS  Google Scholar 

  • Knott KK, Boyd D, Ylitalo GM, O’Hara TM (2012) Lactational transfer of mercury and polychlorinated biphenyls in polar bears. Chemosphere 88(4):395–402

    Article  CAS  Google Scholar 

  • Knott EJ, Bunnefeld N, Huber Đ, Reljić S, Kereži V, Milner-Gulland EJ (2014) The potential impacts of changes in bear hunting policy for hunting organisations in Croatia. Eur J Wildl Res 60(1):85–97

    Article  Google Scholar 

  • Kusak J, Huber Đ (1998) Brown bear habitat quality in Gorski Kotar, Croatia. Ursus 10:281–291

    Google Scholar 

  • Lazarus M, Sekovanić A, Reljić S, Kusak J, Kovačić J, Orct T, Jurasović J, Huber Đ (2014) Selenium in brown bears (Ursus arctos) from Croatia: Relation to cadmium and mercury. J Environ Sci Health A 49:1392–1401

    Article  CAS  Google Scholar 

  • Lazarus M, Sekovanić A, Orct T, Reljić S, Kusak J, Jurasović J, Huber Đ (2017) Apex predatory mammals as bioindicator species in environmental monitoring of elements in Dinaric Alps (Croatia). Environ Sci Poll Res 24:23977–23991

    Article  CAS  Google Scholar 

  • Llop S, Lopez-Espinosa M-J, Rebagliato M, Ballester F (2013) Gender differences in the neurotoxicity of metals in children. Toxicology 311:3–12

    Article  CAS  Google Scholar 

  • Loseto LL, Stern GA, Ferguson SH (2008) Size and biomagnification: How habitat selection explains beluga mercury levels. Environ Sci Technol 42(11):3982–3988

    Article  CAS  Google Scholar 

  • McGrew AK, Ballweber LR, Moses SK, Stricker CA, Beckmen KB, Salman MD, O’Hara TM (2014) Mercury in gray wolves (Canis lupus) in Alaska: Increased exposure through consumption of marine prey. Sci Total Environ 468–469:609–613

    Article  Google Scholar 

  • Medvedev N (1999) Levels of heavy metals in Karelian wildlife, 1989-91. Environ Monit Assess 56:177–193

    Article  CAS  Google Scholar 

  • Medvedev N, Panichev N, Hyvärinen H (1997) Levels of heavy metals in seals of Lake Ladoga and the White Sea. Sci Total Environ 206(2–3):95–105

    Article  CAS  Google Scholar 

  • Millán J, Mateo R, Taggart MA, López-Bao JV, Viota M, Monsalve L, Camarero PR, Blázquez E, Jiménez B (2008) Levels of heavy metals and metalloids in critically endangered Iberian lynx and other wild carnivores from Southern Spain. Sci Total Environ 399(1–3):193–201

    Article  Google Scholar 

  • Neila C, Hernández-Moreno D, Fidalgo LE, López-Beceiro A, Soler F, Pérez-López M (2017) Does gender influence the levels of heavy metals in liver of wild boar? Ecotoxicol Environ Saf 140:24–29

    Article  CAS  Google Scholar 

  • Noël M, Christensen JR, Spence J, Robbins CT (2015) Using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) to characterize copper, zinc and mercury along grizzly bear hair providing estimate of diet. Sci Total Environ 529:1–9

    Article  Google Scholar 

  • 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(1):56–66

    Article  Google Scholar 

  • Nordberg GF, Nogawa K, Nordberg M (2015) Cadmium. In: Nordberg GF, Fowler BA, Nordberg M (eds) Handbook on the toxicology of metals: specific metals, vol II, 4th edn. Academic Press, Amsterdam, pp 667–716

    Chapter  Google Scholar 

  • Oskarsson A, Palminger Hallén I, Sundberg J (1995) Exposure to toxic elements via breast milk. Analyst 120(3):765–770

    Article  CAS  Google Scholar 

  • Oskarsson A, Palminger Hallén I, Sundberg J, Petersson Grawé K (1998) Risk assessment in relation to neonatal metal exposure. Analyst 123(1):19–23

    Article  CAS  Google Scholar 

  • Ramsay MA, Dunbrack RL (1986) Physiological constraints on life history phenomena: the example of small bear cubs at birth. Am Nat 127(6):735–743

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Robillard S, Beauchamp G, Paillard G, Bélanger D (2002) Levels of cadmium, lead, mercury and 137caesium in Caribou (Rangifer tarandus) Tissues from Northern Québec. Arctic 55:1–9

    Article  Google Scholar 

  • Romero MB, Polizzi P, Chiodi L, Das K, Gerpe M (2016) The role of metallothioneins, selenium and transfer to offspring in mercury detoxification in Franciscana dolphins (Pontoporia blainvillei). Mar Pollut Bull 109(1):650–654

    Article  CAS  Google Scholar 

  • Sabolić I, Asif AR, Budach WE, Wanke C, Bahn A, Burckhardt G (2007) Gender differences in kidney function. Pflugers Arch Eur J Physiol 455:397–429

    Article  Google Scholar 

  • Sato I, Yamauchi K, Tsuda S (2016) Long-term survey of cadmium and lead contamination in Japanese black bears captured in Iwate prefecture, Japan. Bull Environ Contam Toxicol 97(6):806–812

    Article  CAS  Google Scholar 

  • Schwartz CC, Miller SD, Haroldson MA (2003) Grizzly bear. In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild mammals of North America: biology, management, and conservation, 2nd edn. Johns Hopkins University Press, Baltimore, pp 556–586

    Google Scholar 

  • Skerfving S, Bergdahl IA (2015) Lead. In: Nordberg GF, Fowler BA, Nordberg M (eds) Handbook on the toxicology of metals, specific metals, vol II, 4th edn. Academic Press, Amsterdam, pp 911–967

    Chapter  Google Scholar 

  • Stoneberg RP, Jonkel CJ (1966) Age determination of black bears by cementum layers. J Wildl Manage 30:411–414

    Article  Google Scholar 

  • Swenson JE, Adamič M, Huber D, Stokke S (2007) Brown bear body mass and growth in northern and southern Europe. Oecologia 153(1):37–47

    Article  Google Scholar 

  • Vahter M, Berglund M, Akesson A, Lidén C (2002) Metals and women’s health. Environ Res Sect A 88:145–155

    Article  CAS  Google Scholar 

  • Vahter M, Åkesson A, Lidén C, Ceccatelli S, Berglund M (2007) Gender differences in the disposition and toxicity of metals. Environ Res 104(1):85–95

    Article  CAS  Google Scholar 

  • Vighi M, Borrell A, Aguilar A (2017) Bone as a surrogate tissue to monitor metals in baleen whales. Chemosphere 171:81–88

    Article  CAS  Google Scholar 

  • Vihnanek Lazarus M, Sekovanić A, Kljaković-Gašpić Z, Orct T, Jurasović J, Kusak J, Reljić S, Huber Đ (2013) Cadmium and lead in grey wolf liver samples: optimization of a microwave-assisted digestion method. Arh Hig Rada Toksikol 64:395–403

    CAS  Google Scholar 

  • Whelton BD, Toomey JM, Bhattacharyya MH (1993) Cadmium-109 metabolism in mice. IV. Diet versus maternal stores as a source of cadmium transfer to mouse fetuses and pups during gestation and lactation. J Toxicol Environ Health 40(4):531–546

    Article  CAS  Google Scholar 

  • Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res Int 23(9):8244–8259

    Article  CAS  Google Scholar 

  • Yoshida M, Ohta H, Yamauchi Y, Seki Y, Sagi M, Yamazaki K, Sumi Y (1998) Age-dependent changes in metallothionein levels in liver and kidney of the Japanese. Biol Trace Elem Res 63(2):167–175

    Article  CAS  Google Scholar 

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Acknowledgments

The help of local hunters and experts with the collection of samples is gratefully acknowledged. The authors thank Dr. Z. Kljaković-Gašpić for valuable comments on the manuscript, and Mr. Makso Herman and Ms. Željana Pavlaković for language editing.

Funding

This research was funded by the Ministry of Science, Education, and Sports of the Republic of Croatia (Grant No. 022-0222148-2135). The Veterinary Faculty team was supported by the European Commission under the “HUNT” project of the 7th Framework Programme for Research and Technological Development (Grant No. 212160), “LIFE DINALP BEAR” project (Grant No. LIFE13 NAT/SI/000550), and the Research Council of Norway under the project “The role of natural resources in sustainable rural livelihoods in the western Balkans. The distribution and flow of costs and benefits” (application No. ES459363). Neither the European Commission nor any person acting on behalf of the Commission is responsible for the use made of the information. The views expressed in this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission.

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Authors and Affiliations

  1. Analytical Toxicology and Mineral Metabolism Unit, Institute for Medical Research and Occupational Health, Ksaverska cesta 2, P.O. Box 291, 10000, Zagreb, Croatia

    Maja Lazarus, Ankica Sekovanić, Tatjana Orct & Jasna Jurasović

  2. Department of Biology, Veterinary Faculty, University of Zagreb, Heinzelova 55, 10000, Zagreb, Croatia

    Slaven Reljić & Đuro Huber

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  1. Maja Lazarus
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  2. Ankica Sekovanić
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  3. Tatjana Orct
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  5. Jasna Jurasović
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Correspondence to Maja Lazarus.

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Lazarus, M., Sekovanić, A., Orct, T. et al. Sexual Maturity and Life Stage Influences Toxic Metal Accumulation in Croatian Brown Bears. Arch Environ Contam Toxicol 74, 339–348 (2018). https://doi.org/10.1007/s00244-017-0487-5

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