The mercury and low molecular-weight antioxidants levels in ungulates of the Republic of Karelia
- Authors: Kalinina S.N.1, Ilyukha V.A.2, Komov V.T.2, Zaitseva I.A.1, Baishnikova I.V.1, Panchenko D.V.1, Antonova E.P.1
-
Affiliations:
- Institute of biology of Karelian Research Centre of Russian Academy of Sciences
- Papanin Institute for Biology of Inland Waters Russian Academy of Sciences
- Issue: Vol 60, No 3 (2024)
- Pages: 234-243
- Section: EXPERIMENTAL ARTICLES
- URL: https://cijournal.ru/0044-4529/article/view/648076
- DOI: https://doi.org/10.31857/S0044452924030022
- EDN: https://elibrary.ru/YXVQXW
- ID: 648076
Cite item
Abstract
The high toxicity of mercury (Hg) poses a danger to the environment and humans, but studies of the concentration of this metal in organisms of terrestrial ecosystems are few. Ecotoxicologists also pay little attention to studying the role of antioxidant vitamins in protecting cells from toxic metals. The Republic of Karelia is one of the northwestern regions of Russia, the biogeochemical features of which can contribute to an increase in the mobility and bioavailability of Hg in food chains. The purpose of the work was to determine the concentration of Hg in the liver, kidneys, muscle and hair of ungulate mammals of the Republic of Karelia (wild boar Sus scrofa L. and moose Alces alces L.) and to analyze the relationship between the level of this toxic metal and the content of low molecular-weight antioxidants – reduced glutathione, retinol and α-tocopherol. Species and tissue-specific of the studied parameters in wild boars and moose are noted. The observations discovered by other researchers that omnivorous species accumulate more Hg in their tissues compared to herbivores, and also that this toxic metal is predominantly accumulated in the kidneys, while muscles contain a minimal amount, have been confirmed. Hg concentrations in most samples of liver and kidney of wild boars and in all samples of these same organs of moose were within the limits recorded for domestic pigs and deer, respectively. The levels of Hg we recorded in the tissues and hair of wild boars and moose were generally comparable to or lower than the levels of this metal noted in animals from other regions of Russia and other countries of the world. In wild boars and moose of Karelia, no statistically significant relationships were found between the Hg level and the content of the studied antioxidants in the internal organs. Moose were characterized by a higher content of α-tocopherol in the body than wild boars, which is a feature of this type of herbivorous ungulate mammal. The results of the study indicate a relatively low level of mercury pollution in terrestrial ecosystems in Karelia.
Keywords
Full Text

About the authors
S. N. Kalinina
Institute of biology of Karelian Research Centre of Russian Academy of Sciences
Author for correspondence.
Email: cvetnick@yandex.ru
Russian Federation, Petrozavodsk
V. A. Ilyukha
Papanin Institute for Biology of Inland Waters Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Borok
V. T. Komov
Papanin Institute for Biology of Inland Waters Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Borok
I. A. Zaitseva
Institute of biology of Karelian Research Centre of Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Petrozavodsk
I. V. Baishnikova
Institute of biology of Karelian Research Centre of Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Petrozavodsk
D. V. Panchenko
Institute of biology of Karelian Research Centre of Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Petrozavodsk
E. P. Antonova
Institute of biology of Karelian Research Centre of Russian Academy of Sciences
Email: cvetnick@yandex.ru
Russian Federation, Petrozavodsk
References
- WHO (2017) Ten chemicals of major health concern. http://www.who.int/ipcs/assessment/public_health/chemicals_phc/en/index.html
- Kalisińska E (ed.) (2019) Mammals and birds as bioindicators of trace element contaminations in terrestrial environments: an ecotoxicological assessment of the Northern Hemisphere. – Springer.
- Gworek B, Dmuchowski W, Baczewska-Dąbrowska AH (2020) Mercury in the terrestrial environment: A review. Environ Sci Eur 32(1): 1–19. https://doi.org/10.1186/s12302-020-00401-x
- UKHSA (2022) Elemental Mercury and Inorganic Mercury: Toxicological Overview. https://www.gov.uk/government/publications/mercury-properties-incident-management-and-toxicology/elemental-mercury-and-inorganic-mercury-toxicological-overview#ref4
- Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–17. https://doi.org/10.1579/0044–7447(2007)36[12: EOEMOT]2.0.CO;2
- Isaksson C (2010) Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth 7(3):342–350. https://doi.org/10.1007/s10393-010-0345-7
- Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicol 101(1):13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
- Defo MA, Pierron F, Spear PA, Bernatchez L, Campbell PGC, Couture P (2012) Evidence for metabolic imbalance of vitamin A2 in wild fish chronically exposed to metals. Ecotoxicol Environ Safety 85:88–95. https://doi.org/10.1016/j.ecoenv.2012.08.017
- Rodríguez-Estival J, Martinez-Haro M, Monsalve-González L, Mateo R (2011) Interactions between endogenous and dietary antioxidants against Pb-induced oxidative stress in wild ungulates from a Pb polluted mining area. Sci Total Environ 409:2725–2733. https://doi.org/10.1016/j.scitotenv.2011.04.010
- Rodríguez-Estival J, Taggart MA, Mateo R (2011) Alterations in vitamin A and E levels in liver and testis of wild ungulates from a lead mining area. Arch Environ Contam Toxicol 60(2):361–371. https://doi.org/10.1007/s00244-010-9597-z
- Engin KN (2009) Alpha-tocopherol: looking beyond an antioxidant. Mol Vision 15:855.
- Peraza AM, Ayala-Fierro F, Barber DS, Casarez E, Rael L (1998) Effects of micronutrients on metal toxicity. Environ Health Persp 106:(Suppl.1):1–27. https://doi.org/10.1289/ehp.98106s1203
- Debier C, Larondelle Y (2005) Vitamins A and E: metabolism, roles and transfer to offspring. Br J Nutr 93:153–174. https://doi.org/10.1079/BJN20041308
- Alpsoy L, Yildirim A, Agar G (2009) The antioxidant effects of vitamin A, C, and e on aflatoxin B1-induced oxidative stress in human lymphocytes. Toxicol Industr Health 25:121–127. https://doi.org/10.1177/0748233709103413
- Pereira AA, van Hattum B, Brouwer A (2012) Hepatic retinoid levels in seven fish species (teleosts) from a tropical coastal lagoon receiving effluents from iron-ore mining and processing. Environment Toxicol Chem 31:408–416. https://doi.org/10.1002/etc.740
- Wayland M, Smits JEG, Gilchrist HG, Marchant T, Keating J (2003) Biomarker responses in nesting, common eiders in the Canadian arctic in relation to tissue cadmium, mercury and selenium concentrations. Ecotoxicol 12:225–237. https://doi.org/10.1023/A:1022506927708
- 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(23):13385–13394. https://doi.org/10.1021/es403103t
- Zillioux EJ, Porcella DB, Benoit JM (1993) Mercury cycling and effects in freshwater wetland ecosystems. Environ Toxicol Chem 12:2245–2264. https://doi.org/10.1002/etc.5620121208
- Medvedev N (1999) Levels of heavy metals in Karelian wildlife, 1989–91. Environ Monit Assess 56:177–193. https://doi.org/10.1023/A:1005988511058
- Eltsova L, Ivanova E (2021) Total mercury level in tissues of commercial mammalian species (wild boar, moose) of the Russky Sever National Park (North-West of Russia). In E3S Web of Conferences (Vol. 265, p. 05009). EDP Sciences
- Степанова ИК, Комов ВТ (1996) Ртуть в абиотических и биотических компонентах озер Северо-Запада России. Экология 3:198–203. [Stepanova IK, Komov VT (1996) Mercury in abiotic and biotic components of lakes in Northwestern Russia. Ecology 3:198–203. (In Russ)].
- Prosekov AYu, Altshuler OG, Kurbanova MG (2021) Quality and Safety of Game Meat from the Biocenosis of the Beloosipovo Mercury Deposit (part 2). Food Proc: Techniq Technol 51(4):654–663. https://doi. org/10.21603/2074-9414-2021-4-654-663
- Горбунов АВ, Ляпунов СМ, Ермолаев БВ (2019) Распределение ртути в природных и урбанизированных средах Карелии. Экология человека 4:10–17. [Gorbunov AV, Lyapunov SM, Yermolaev BV (2019) Distribution of mercury in natural and urban environments of Karelia. Hum Ecol 4:10–17. (In Russ)].
- Немова НН (2005) Биохимическая адаптация накопления ртути у рыб. М.: Наука, 164 с. [Nemova NN (2005) Biochemical adaptation of mercury accumulation in fish. M.: Nauka, 164 p. (In Russ)].
- Zaitseva IA, Baishnikova IV, Panchenko DV, Kalinina SN, Ilyina TN, Antonova EP (2023) The Content of Retinol, α-Tocopherol and Glutathione in Tissues of the Wild Boar (Sus scrofa L.) Inhabiting the Northwest of Russia. J Evol Biochem Physiol 59(3):744–755. https://doi.org/10.1134/S0022093023030092
- Matschke GH (1967) Aging European wild hogs by dentition. J Wildl Manag 31(1):109–113.
- Moore CD, Fahlman A, Crocker DE, Robbins KA, Trumble SJ (2015) The degradation of proteins in pinniped skeletal muscle: viability of post-mortem tissue in physiological research. Conserv Physiol 3(1):1–8. https://doi.org/10.1093/conphys/cov019
- Назаренко ИИ, Кислоева ИВ, Кашина ЛИ (1986) Атомно- адсорбционное определение ртути в водах после сорбционного концентрирования на полимерном тиоэфире. Журн аналитич хим 11(8):1385–1390. [Nazarenko II, Kisloeva IV, Kashina LI (1986) Atomic adsorption determination of mercury in waters after sorption concentration on a polymer thioether. J Analytical Chem 11(8):1385–1390. (In Russ)].
- Скурихин ВН, Двинская ЛМ (1989) Определение α-токоферола и ретинола в плазме крови сельскохозяйственных животных методом микроколоночной высокоэффективной жидкостной хроматографии. Сельскохозяйственная биология 4:127–129. [Skurihin VN, Dvinskaya LM (1989) Determination of α-tocopherol and retinol in the blood plasma of farm animals using microcolumn high-performance liquid chromatography. Agricult Biol 4:127–129. (In Russ)].
- Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192–205
- Lowry OH, Rosenbrough NJ, Farr AL, Randan RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275.
- Унгуряну ТН, Гржибовский АМ (2011) Краткие рекомендации по описанию, статистическому анализу и представлению данных в научных публикациях. Экология человека 5:55–60. [Unguryanu TN, Grzhibovskii AM (2011) Brief recommendations for the description, statistical analysis and presentation of data in scientific publications. Hum Ecol 5:55–60. (In Russ)].
- Wisconsin Veterinary Diagnostic Laboratory (WVDL) (2015) Normal range values for WVDL Toxicology.
- Данилов ПИ (2017) Охотничьи звери Карелии (экология, ресурсы, управление, охрана). Петрозаводск: Карельский научный центр, 388 с. [Danilov PI (2017) Game animals of Karelia (ecology, resources, management, protection). Petrozavodsk: Karel Sci Centr, 388 p. (In Russ)].
- Ballari SA, Barrios-García MN (2014) A review of wild boar (Sus scrofa) diet and factors affecting food selection in native and introduced ranges. Mammal Rev 44(2):124–134. https://doi.org/10.1111/mam.12015
- Филонов КП (1983) Лось. М.: “Лесная промышленность”, 248 с. [Filonov KP (1983) Moose. M.: “Lesnaya promyshlennostʼ”, 248 s. (In Russ.)]
- Squadrone S, Robetto S, Orusa R, Griglione A, Falsetti S, Paola B, Abete MC (2022) Wildlife hair as bioindicators of metal exposure. Biol Trace Elem Res 200(12):5073–5080. https://doi.org/10.1007/s12011-021-03074-6
- Tomza-Marciniak A, Pilarczyk B, Drozd R, Pilarczyk R, Juszczak-Czasnojć M, Havryliak V, Podlasinska J, Udała J (2023) Selenium and mercury concentrations, Se: Hg molar ratios and their effect on the antioxidant system in wild mammals. Environment Pollut 322:121234. https://doi.org/10.1016/j.envpol.2023.121234
- Lazarus M, Crnić AP, Bilandžić N, Kusak J, Reljić S (2014) Cadmium, lead and mercury exposure assessment among Croatian consumers of free-living game. Archiv Industr Hygien Toxicol 65(3). https://doi.org/10.2478/10004-1254-65-2014-2527
- Piskorovà L, Vasilkovà Z, Krupicer I (2003) Heavy Metal Residues in Tissues of Wild Boar (Sus scrofa) and Red Fox (Vulpes vulpes) in the Central Zemplin Region of the Slovak Republic. Czech J Anim Sci 48:134–138.
- Demirbaş Y, Erduran N (2017) Concentration of selected heavy metals in brown hare (Lepus europaeus) and wild boar (Sus scrofa) from central Turkey. Balk J Wildl Res 4:26–33. https://doi.org/10.15679/bjwr.v4i2.54
- Bilandzić N, Sedak M, Dokic M, Simic A (2010) Heavy Metal Concentrations in Tissues of Wild Boar of Continental Croatia. Int J Environ Protect 2:6–9.
- Бондарев АЯ (2012) Токсиканты в организмах волка и некоторых других млекопитающих Алтайского края. Вестник Алтайского государственного аграрного университета 91(5):44–49. [Bondarev AYa (2012) Toxicants in the organisms of the wolf and some other mammals of the Altai Territory. Bull Altai State Agr Univ 91(5):44–49. (In Russ)].
- Курченко ГА (2002) Оценка содержания ртути в органах животных и окружающей среде [Белгородская обл.]. Экологическая безопасность в АПК. Реферативный журнал 1:5–5. [Kurchenko GA (2002) Assessment of mercury content in animal organs and the environment [Belgorod region]. Environment Saf Agricult. Abstract J 1:5–5. (In Russ.)]
- Agrawal S, Flora G, Bhatnagar P, Flora SJS (2014) Comparative oxidative stress, metallothionein induction and organ toxicity following chronic exposure to arsenic, lead and mercury in rats. Cell Mol Biol 60(2):13–21. http://cellmolbiol.org/index.php/CMB/article/view/530
- Hussain S, Atkinson A, Thompson SJ, Khan AT (1999) Accumulation of mercury and its effect on antioxidant enzymes in brain, liver, and kidneys of mice. J Environ Sci Health B34(4):645–660. https://doi.org/10.1080/03601239909373219
- Sauer JM, Waalkes MP, Hooser SB, Baines AT, Kuester RK, Sipes IG (1997) Tolerance induced by all-trans-retinol to the hepatotoxic effects of cadmium in rats: role of metallothionein expression. Toxicol Appl Pharmacol 143(1):110–119. https://doi.org/10.1006/taap.1996.8050
- Alasia D, Emem-Chioma P, Ojeka S (2020) An evaluation of the mitigating effects of α-tocopherol (vitamin E) and ascorbic acid (vitamin C) on the renal function and histology of adult male albino Wistar rats with sub-acute lead acetate exposure. Occup Dis Environ Med 8:35–49. https://doi.org/10.4236/odem.2020.82003
- Ильина ТН, Руоколайнен ТР, Белкин ВВ, Баишникова ИВ (2011) Токоферол в физиологических адаптациях млекопитающих различного экогенеза. Труды Карельского научного центра РАН 3:49–56. [Ilʼina TN, Ruokolainen TR, Belkin VV, Baishnikova IV (2011) Tokoferol v fiziologicheskih adaptatsiyah mlekopitayushchih razlichnogo ekogeneza [Tocopherol in physiological adaptations of mammals of different ecogenesis]. Proc Karelian Sci Center RAS3:49–56. (In Russ.)]
- Combs Jr GF, McClung JP (2016) The vitamins: fundamental aspects in nutrition and health. Academic press.
- Traber MG (2013) Mechanisms for the prevention of vitamin E excess. J Lipid Res 54:2295–2306. https://doi.org/10.1194/jlr.R032946
- Vertuani S, Angusti A, Manfredini S (2004) The antioxidants and pro-oxidants network: an overview. Curr Pharm Des 10:1677–1694. https://doi.org/10.2174/1381612043384655
- Tesoriere L, Bongiorno A, Pintaudi AM, D'Anna R, D'Arpa D, Livrea MA (1996) Synergistic interactions between vitamin A and vitamin E against lipid peroxidation in phosphatidylcholine liposomes. Arch Biochem Bioph 326(1):57–63. https://doi.org/10.1006/abbi.1996.0046
- Majchrzak D, Fabian E, Elmadfa I (2006) Vitamin A content (retinol and retinyl esters) in livers of different animals. Food Chem 98(4):704–710. https://doi.org/10.1016/j.foodchem.2005.06.035
Supplementary files
