Аннотация

Reproduction is key to the survival and development of a species. Anthropogenic activities release significant amounts of toxic pollutants into the environment. In this study, we aimed to determine effects of heavy metals on some reproductive parameters of the mountain hare.
Female mountain hares (n = 41) were hunted in the reference and industrially polluted areas of Krasnoyarsk Krai during four seasons. Their skeletal muscles, liver, and kidneys were subjected to atomic absorption spectrometry to determine concentrations of lead, cadmium, and mercury.
The contents of lead, cadmium, and mercury were significantly higher in the hares from the contaminated areas compared to the reference sites. According to the results, the exposure to lead, cadmium, and mercury had an impact on the reproductive potential of the female mountain hares. In particular, we established correlations between numbers of embryos and corpora lutea and contents of lead in the kidneys and liver, as well as cadmium in the kidneys. The number of corpora lutea and embryonic losses in the female hares from the contaminated areas were higher than those in the hared from reference areas. However, the numbers of embryos did not differ significantly between the compared areas.
Our study showed that about 40% of the liver samples and 100% of the muscle tissue samples obtained from the hares in the impact zone contained high concentrations of lead and cadmium. Therefore, hunting in these industrially polluted areas may pose a toxic hazard to the indigenous peoples living there. Further research is needed to assess potential and actual fertility, offspring survival, and other important parameters of mountain hare populations exposed to different levels of chemical pollution.

Ключевые слова

Heavy metals, cadmium, lead, mercury, reproduction, warm-blooded animals, corpus luteum, embryo, liver, kidneys, skeletal muscles

ФИНАНСИРОВАНИЕ

The study was conducted in 2023 at the Professor Zhitkov Russian Research Institute of Game Management and Fur Farming (VNIIOZ) as part of the state assignment on “Advancing scientific foundations for sustainable use, assessment, monitoring, and forecasting of hunting bioresources” (No. FNWS-2022-0001) within the Fundamental Research Program for 2021–2030 (Russian Government Decree No. 3684-r of December 31, 2020).

СПИСОК ЛИТЕРАТУРЫ

1. Mukhacheva SV, Bezel' VS. Heavy metals in the mother-placenta-fetus system in bank voles under conditions of environmental pollution from copper plant emissions. Russian Journal of Ecology. 2015;(6):444–453. https://doi.org/10.7868/S0367059715060128; https://elibrary.ru/UIMJKZ
2. Satarug S, Gobe GC, Vesey DA, Phelps KR. Cadmium and lead exposure, nephrotoxicity, and mortality. Toxics. 2020;8(4):86. https://doi.org/10.3390/toxics8040086
3. Kaledin AP, Stepanova MV. Bioaccumulation of trace elements in vegetables grown in various anthropogenic conditions. Foods and Raw Materials. 2023;11(1):10–16. https://doi.org/10.21603/2308-4057-2023-1-551
4. Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, et al. The toxicity of cadmium and resulting hazards for human health. Journal of Occupational Medicine and Toxicology. 2006;1:22. https://doi.org/10.1186/1745-6673-1-22
5. Satarug S, Boonprasert K, Gobe GC, Ruenweerayut R, Johnson, DW, Na-Bangchang K, et al. Chronic exposure to cadmium is associated with a marked reduction in glomerular filtration rate. Clinical Kidney Journal. 2018;12(4):468–475. https://doi.org/10.1093/ckj/sfy113
6. Duan Y, Zhao Y, Wang T, Sun J, Ali W, Ma Y, et al. Taurine alleviates cadmium-induced hepatotoxicity by regulating autophagy flux. International Journal of Molecular Sciences. 2023;24(2):1205. https://doi.org/10.3390/ijms24021205
7. Kumar S, Sharma A. Cadmium toxicity: Effects on human reproduction and fertility. Reviews on Environmental Health. 2019;34(4):327–338. https://doi.org/10.1515/reveh-2019-0016
8. Nishijo M, Nakagawa H, Suwazono Y, Nogawa K, Kido T. Causes of death in patients with Itai-itai disease suffering from severe chronic cadmium poisoning: A nested case – control analysis of a follow-up study in Japan. BMJ Open. 2017;7(7):e015694. https://doi.org/10.1136/bmjopen-2016-015694
9. Ali W, Bian Y, Zhang H, Qazi IH, Zou H, Zhu J, et al. Effect of cadmium exposure during and after pregnancy of female. Environmental Pollutants and Bioavailability. 2023;35(1):2181124. https://doi.org/10.1080/26395940.2023.2181124
10. de Angelis C, Galdiero M, Pivonello C, Salzano C, Gianfrilli D, Piscitelli P, et al. The environment and male reproduction: The effect of cadmium exposure on reproductive function and its implication in fertility. Reproductive Toxicology. 2017;73:105–127. https://doi.org/10.1016/j.reprotox.2017.07.021
11. Manna PR, Stetson CL, Slominski AT, Pruitt K. Role of the steroidogenic acute regulatory protein in health and disease. Endocrine. 2016;51:7–21. https://doi.org/10.1007/s12020-015-0715-6
12. Kutyakov VA, Salmina AB. Metallothioneins as sensors and controls exchange of metals in the cells. Bulletin of Siberian Medicine. 2014;13(3):91–99. (In Russ.). https://doi.org/10.20538/1682-0363-2014-3-91-99; https://elibrary.ru/SXRMYP
13. Espart A, Artime S, Tort-Nasarre G, Yara-Varón E. Cadmium exposure during pregnancy and lactation: Materno-fetal and newborn repercussions of Cd(II), and Cd–metallothionein complexes. Metallomics. 2018;10:1359–1367. https://doi.org/10.1039/c8mt00174j
14. Gundacker C, Hengstschläger M. The role of the placenta in fetal exposure to heavy metals. Wiener Medizinische Wochenschrift. 2012;162(9–10):201–206. https://doi.org/10.1007/s10354-012-0074-3
15. Massanyi P, Bárdos L, Oppel K, Hluchý S, Kovácik J, Csicsai G, et al. Distribution of cadmium in selected organs of mice: Effects of cadmium on organ contents of retinoids and beta-carotene. Acta Physiologica Hungarica. 1999;86(2):99–104.
16. Massanyi P, Toman R, Valent M, Cupka P. Evaluation of selected parameters of a metabolic profile and levels of cadmium in reproductive organs of rabbits after an experimental administration. Acta Physiologica Hungarica. 1995;83(3):267–273.
17. Nad P, Massanyi P, Skalicka M, Koréneková B, Cigankova V, Almášiová V. The effect of cadmium in combination with zinc and selenium on ovarian structure in Japanese quails. Journal of Environmental Science and Health, Part A. 2007;42(13):2017–2022. https://doi.org/10.1080/10934520701629716
18. Nasiadek M, Danilewicz M, Klimczak M, Stragierowicz J, Kilanowicz A. Subchronic exposure to cadmium causes persistent changes in the reproductive system in female Wistar rats. Oxidative Medicine and Cellular Longevity. 2019;2019:6490820. https://doi.org/10.1155/2019/6490820
19. Wang Y, Wang X, Wang Y, Fan R, Qiu C, Zhong S, et al. Effect of cadmium on cellular ultrastructure in mouse ovary. Ultrastructural Pathology. 2015;39(5):324–328. https://doi.org/10.3109/01913123.2015.1027436
20. Ruslee SS, Zaid SSM, Bakrin IH, Goh YM, Mustapha NM. Protective effect of Tualang honey against cadmium-induced morphological abnormalities and oxidative stress in the ovary of rats. BMC Complementary Medicine and Therapies. 2020;20:160. https://doi.org/10.1186/s12906-020-02960-1
21. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: A review. Reproductive Biology and Endocrinology. 2012;10:49. https://doi.org/10.1186/1477-7827-10-49
22. Zhang W, Pang F, Huang Y, Yan P, Lin W. Cadmium exerts toxic effects on ovarian steroid hormone release in rats. Toxicology Letters. 2008;182(1–3):18–23. https://doi.org/10.1016/j.toxlet.2008.07.016
23. Takiguchi M, Yoshihara S. New aspects of cadmium as endocrine disruptor. Environmental Sciences: An International Journal of Environmental Physiology and Toxicology. 2006;13(2):107–116.
24. Johnson MD, Kenney N, Stoica A, Hilakivi-Clarke L, Singh B, Chepko G, et al. Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nature Medicine. 2003;9:1081–1084. https://doi.org/10.1038/nm902
25. Massányi P, Massányi M, Madeddu R, Stawarz R, Lukác N. Effects of cadmium, lead, and mercury on the structure and function of reproductive organs. Toxics. 2020;8(4):94. https://doi.org/10.3390/toxics8040094
26. Rădulescu A, Lundgren S. A pharmacokinetic model of lead absorption and calcium competitive dynamics. Scientific Reports. 2019;9:14225. https://doi.org/10.1038/s41598-019-50654-7
27. Gulson B, Taylor A, Eisman J. Bone remodeling during pregnancy and post-partum assessed by metal lead levels and isotopic concentrations. Bone. 2016;89:40–51. https://doi.org/10.1016/j.bone.2016.05.005
28. Zhang B, Xia W, Li Y, Bassig BA, Zhou A, Wang Y, et al. Prenatal exposure to lead in relation to risk of preterm low birth weight: A matched case-control study in China. Reproductive Toxicology. 2015;57:190–195. https://doi.org/10.1016/j.reprotox.2015.06.051
29. Disha, Sharma S, Goyal M, Kumar PK, Ghosh R, Sharma P. Association of raised blood lead levels in pregnant women with preeclampsia: A study at tertiary centre. Taiwanese Journal of Obstetrics and Gynecology. 2019;58(1): 60–63. https://doi.org/10.1016/j.tjog.2018.11.011
30. Soomro MH, Baiz N, Huel G, Yazbeck C, Botton J, Heude B, et al. Exposure to heavy metals during pregnancy related to gestational diabetes mellitus in diabetes-free mothers. Science of the Total Environment. 2019;656:870–876. https://doi.org/10.1016/j.scitotenv.2018.11.422
31. Taylor CM, Golding J, Emond AM. Adverse effects of maternal lead levels on birth outcomes in the ALSPAC study: A prospective birth cohort study. BJOG: An International Journal of Obstetrics and Gynaecology. 2015;122(3):322–328. https://doi.org/10.1111/1471-0528.12756
32. Yoon J-H, Ahn Y-S. The association between blood lead level and clinical mental disorders in fifty thousand lead-exposed male workers. Journal of Affective Disorders. 2016;190:41–46. https://doi.org/10.1016/j.jad.2015.09.030
33. Bede-Ojimadu O, Amadi CN, Orisakwe OE. Blood lead levels in women of child-bearing age in sub-Saharan Africa: A systematic review. Frontiers in Public Health. 2018;6. https://doi.org/10.3389/fpubh.2018.00367
34. Borja-Aburto VH, Hertz-Picciotto I, Rojas Lopez M, Farias P, Rios C, Blanco J. Blood lead levels measured prospectively and risk of spontaneous abortion. American Journal of Epidemiology. 1999;150(6):590–597. https://doi.org/10.1093/oxfordjournals.aje.a010057
35. Cheng L, Zhang B, Huo W, Cao Z, Liu W, Liao J, et al. Fetal exposure to lead during pregnancy and the risk of preterm and early-term deliveries. International Journal of Hygiene and Environmental Health. 2017;220(6):984–989. https://doi.org/10.1016/j.ijheh.2017.05.006
36. Huang S, Xia W, Sheng X, Qiu L, Zhang B, Chen T, et al. Maternal lead exposure and premature rupture of membranes: A birth cohort study in China. BMJ Open. 2018;8:e021565. https://doi.org/10.1136/bmjopen-2018-021565
37. Kumar S. Occupational and environmental exposure to lead and reproductive health impairment: An overview. Indian Journal of Occupational and Environmental Medicine. 2018;22(3):128–137. https://doi.org/10.4103/ijoem.IJOEM_126_18
38. Rahman A, Kumarathasan P, Gomes J. Infant and mother related outcomes from exposure to metals with endocrine disrupting properties during pregnancy. Science of the Total Environment. 2016;569–570:1022–1031. https://doi.org/10.1016/j.scitotenv.2016.06.134
39. Tyrrell JB, Hafida S, Stemmer P, Adhami A, Leff T. Lead (Pb) exposure promotes diabetes in obese rodents. Journal of Trace Elements in Medicine and Biology. 2017;39:221–226. https://doi.org/10.1016/j.jtemb.2016.10.007
40. Chekhoeva AN, Khamitsaev ZA, Kozaeva AEh, Kadokhova LA. Comprehensive analysis of the impact of heavy metals on obstetric pathology. Medicine. Sociology. Philosophy. Applied research. 2019;(2);31–37. (In Russ.). https://elibrary.ru/INJWUS
41. Nkomo P, Richter LM, Kagura J, Mathee A, Naicker N, Norris SA. Environmental lead exposure and pubertal trajectory classes in South African adolescent males and females. Science of the Total Environment. 2018;628–629:1437–1445. https://doi.org/10.1016/j.scitotenv.2018.02.150
42. Hilderbrand DC, Der R, Griffin WT, Fahim MS. Effect of lead acetate on reproduction. American Journal of Obstetrics and Gynecology. 1973;115(8):1058–1065. https://doi.org/10.1016/0002-9378(73)90554-1
43. Dhir V, Dhand P. Toxicological approach in chronic exposure to lead on reproductive functions in female rats (Rattus norvegicus). Toxicology International. 2010;17(1):1–7.
44. Kolesarova A, Roychoudhury S, Slivkova J, Sirotkin A, Capcarová M, Massanyi P. In vitro study on the effects of lead and mercury on porcine ovarian granulosa cells. Journal of Environmental Science and Health, Part A. 2010;45(3):320–331. https://doi.org/10.1080/10934520903467907
45. Capcarová M, Kolesarova A, Lukac N, Sirotkin A, Roychoudhury S. Antioxidant status and selected biochemical parameters of porcine ovarian granulosa cells exposed to lead in vitro. Journal of Environmental Science and Health, Part A. 2009;44(14):1617–1623. https://doi.org/10.1080/10934520903263678
46. Vigeh M, Smith DR, Hsu P-C. How does lead induce male infertility? Iranian Journal of Reproductive Medicine. 2011;9(1):1–8.
47. Pollet IL, Leonard ML, O’Driscoll NJ, Burgess NM, Shutler D. Relationships between blood mercury levels, reproduction, and return rate in a small seabird. Ecotoxicology. 2017;26:97–103. https://doi.org/10.1007/s10646-016-1745-4
48. Bjørklund G, Chirumbolo S, Dadar M, Pivina L, Lindh U, Butnariu M, et al. Mercury exposure and its effects on fertility and pregnancy outcome. Basic and Clinical Pharmacology and Toxicology. 2019;125(4):317–327. https://doi.org/10.1111/bcpt.13264
49. Global mercury assessment 2013: Sources, emissions, releases, and environmental transport. Geneva: United Nations Environment Programme; 2013. 44 p.
50. Cossa D, Heimbürger L-E, Lannuzel D, Rintoul SR, Butler ECV, Bowie AR, et al. Mercury in the Southern Ocean. Geochimica et Cosmochimica Acta. 2011;75(14):4037–4052. https://doi.org/10.1016/j.gca.2011.05.001
51. Dix-Cooper L, Kosatsky T. Blood mercury, lead and cadmium levels and determinants of exposure among newcomer South and East Asian women of reproductive age living in Vancouver, Canada. Science of the Total Environment. 2018;619–620:1409–1419. https://doi.org/10.1016/j.scitotenv.2017.11.126
52. Zheng N, Wang S, Dong W, Hua X, Li Y, Song X, et al. The toxicological effects of mercury exposure in marine fish. Bulletin of Environmental Contamination and Toxicology. 2019;102:714–720. https://doi.org/10.1007/s00128-019-02593-2
53. Sadripour E, Mortazavi MS, Mahdavi Shahri N. Effects of mercury on embryonic development and larval growth of the sea urchin Echinometra mathaei from the Persian Gulf. Iranian Journal of Fisheries Sciences. 2013;12(4):898–907.
54. Chen YW, Huang CF, Tsai KS, Yang RS, Yen CC, Yang CY, et al. Methylmercury induces pancreatic β-cell apoptosis and dysfunction. Chemical Research in Toxicology. 2006;19(8):1080–1085. https://doi.org/10.1021/tx0600705
55. Sukhn C, Awwad J, Ghantous A, Zaatari G. Associations of semen quality with non-essential heavy metals in blood and seminal fluid: data from the environment and male infertility (EMI) study in Lebanon. Journal of Assisted Reproduction and Genetics. 2018;35:1691–1701. https://doi.org/10.1007/s10815-018-1236-z
56. Ma Y, Zhu M, Miao L, Zhang X, Dong X, Zou XT. Mercuric chloride induced ovarian oxidative stress by suppressing Nrf2-Keap1 signal pathway and its downstream genes in laying hens. Biological Trace Element Research. 2018;185:185–196. https://doi.org/10.1007/s12011-018-1244-y
57. Lundholm CE. Effects of methyl mercury at different dose regimes on eggshell formation and some biochemical characteristics of the eggshell gland mucosa of the domestic fowl. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology. 1995;110(1):23–28. https://doi.org/10.1016/0742-8413(94)00081-K
58. Altunkaynak BZ, Akgül N, Yahyazadeh A, Altunkaynak ME, Türkmen AP, Akgül HM, et al. Effect of mercury vapor inhalation on rat ovary: Stereology and histopathology. Journal of Obstetrics and Gynaecology Research. 2016;42(4):410–416. https://doi.org/10.1111/jog.12911
59. Roychoudhury S, Massanyi P, Slivkova J, Formicki G, Lukac N, Slamecka J, et al. Effect of mercury on porcine ovarian granulosa cells in vitro. Journal of Environmental Science and Health, Part A. 2015;50(8):839–845. https://doi.org/10.1080/10934529.2015.1019805
60. Koli S, Prakash A, Choudhury S, Mandil R, Garg SK. Calcium channels, rho-kinase, protein kinase-c, and phospholipase-c pathways mediate mercury chloride-induced myometrial contractions in rats. Biological Trace Element Research. 2019;187:418–424. https://doi.org/10.1007/s12011-018-1379-x
61. Nakade UP, Garg SK, Sharma A, Choudhury S, Yadav RS, Gupta K, et al. Lead-induced adverse effects on the reproductive system of rats with particular reference to histopathological changes in uterus. Indian Journal of Pharmacology. 2015;47(1):22–26. https://doi.org/10.4103/0253-7613.150317
62. Pulliainen E, Lajunen LHJ, Itamies J, Anttila R. Lead and cadmium in the liver and muscles of the mountain hare (Lepus timidus) in northern Finland. Annales Zoologici Fennici. 1984;21(2):149–152.
63. Kålås JA, Ringsby TH, Lierhagen S. Metals and selenium in wild animals from Norwegian areas close to Russian nickel smelters. Environmental Monitoring and Assessment. 1995;36(3):251–270. https://doi.org/10.1007/BF00547905
64. Venäläinen E-R, Niemi A, Hirvi T. Heavy metals in tissues of hares in Finland, 1980–82 and 1992–93. Bulletin of Environmental Contamination and Toxicology. 1996;56:251–258. https://doi.org/10.1007/s001289900038
65. Zarubin BE, Ekonomov AV, Kolesnikov VV, Shevnina MS, Sergeev AA. The resources of mountain hare in the Kirov region and their use. Far East Agrarian Bulletin. 2021;60(4):87–102. (In Russ.). https://doi.org/10.24412/1999-6837-2021-4-87-102; https://elibrary.ru/WGXKTC
66. Kochkarev PV, Koshurnikova MA, Sergeyev AA, Shiryaev VV. Trace elements in the meat and internal organs of the mountain hare (Lepus timidus L., 1758) in the north of the Krasnoyarsk Region. Food Processing: Techniques and Technology. 2023;53(2):217–230. (In Russ.). https://doi.org/10.21603/2074-9414-2023-2-2436; https://elibrary.ru/YORYWG
67. Ivanter EhV, Korosov AV. Biology of chemical elements. Petrozavodsk: PetrGU; 2010. 104 p. (In Russ.). https://elibrary.ru/QKOJXR
68. The official report “On the state and protection of the environment in Krasnoyarsk Krai in 2022”. Krasnoyarsk, 2022. 321 p. (In Russ.).
69. Potthast K. Residues in meat and meat products. Fleischwirtsch. 1993;73:432–434.
70. Lobkovsky VA, Lobkovskaya LG. The ecological situation around the arrangement of the enterprises of the polar branch of the MMC Norilsk nickel: Current state and forecast. Regional Environmental Issues. 2015;(5):40–43. (In Russ.). https://elibrary.ru/VOGNRN
71. Bazova MM, Koshevoi DV. The assessment of the current state of water quality in the Norilsk industrial region. Arctic: Ecology and Economy. 2017;27(3):49–60. (In Russ.). https://doi.org/10.25283/2223-4594-2017-3-49-60; https://elibrary.ru/ZHQXJT
72. May IV, Kleyn SV, Vekovshinina SA, Balashov SYu, Chetverkina KV, Tsinker MYu. Health risk to the population in Norilsk under exposure of substances polluting ambient air. Hygiene and Sanitation, Russian Journal. 2021;100(5):528–534. (In Russ.). https://doi.org/10.47470/0016-9900-2021-100-5-528-534; https://elibrary.ru/DCTLGR
73. Lezhenin AA, Raputa VF, Yaroslavtseva TV. Numerical analysis of atmospheric circulation and pollution transfer in the environs of Norilsk industrial region. Atmospheric and Oceanic Optics. 2016;29(6):467–471. (In Russ.). https://doi.org/10.15372/aoo20160603; https://elibrary.ru/VZJPDL
74. Onuchin AA, Burenina TA, Zubareva ON, Trefilova OV, Danilova IV. Pollution of snow cover in the impact zone of enterprises in Norilsk industrial area. Contemporary Problems of Ecology. 2014;21(6):1025–1037. (In Russ.). https://elibrary.ru/TAKBWH
75. Kochkarev PV, Mikhailov VV. Complex analysis of heavy metals content in bodies and tissues of the wild reindeer (Rangifer tarandus L. 1758). Bulletin of KSAU. 2016;119(8):21–27. (In Russ.). https://elibrary.ru/WCYUSN
76. Skugland T, Baskin LM, Ehspelien IS, Strand U. Contents of heavy and radioactive metals in different reindeer populations. Lomonosov Geography Journal. 1997;(6):19–24. (In Russ.).
77. Kireeva AV, Kolenchukova OA, Peretiatko OV, Savchenko AP, Temerova VL, Emelyanov VI. Morphological assessment of organs and tissues of small mammals living in the industrial area of Norilsk. Contemporary Problems of Ecology. 2023;30(3):330–342. (In Russ.). https://elibrary.ru/GISADM
78. Ahmed MS, Azam MA, Ahmed KS, Ali H. Accumulation of some heavy metals in selected tissues of cape hare, Lepus capensis from Pakistan. Pakistan Journal of Wildlife Archives. 2016;7(2):11–20.
79. Demirbaş Y, Erduran N. Concentration of selected heavy metals in brown hare (Lepus europaeus) and wild boar (Sus scrofa) from Central Turkey. Balkan Journal of Wildlife Research. 2017;4(2):26–33. https://doi.org/10.15679/bjwr.v4i2.54
80. Beukovi´ D, Vukadinovi´ M, Krstovi´ S, Polovinski-Horvatovi´ M, Jaji´ I, Popovi´ Z, et al. The European hare (Lepus europaeus) as a biomonitor of lead (Pb) and cadmium (Cd) occurrence in the agro biotope of Vojvodina, Serbia. Animals. 2022;12(10):1249. https://doi.org/10.3390/ani12101249
81. Wajdzik M. Contents of cadmium and lead in liver, kidneys and blood of the European hare (Lepus europaeus Pallas) in Malopolska. Journal Acta Scientiarum Polonorum Silvarum Colendarum Ratio et Industria Lignaria. 2006;5(2):135–146.
82. Fidalgo L, de la Cruz B, Goicoa A, Espino L. Accumulation of zinc, copper, cadmium and lead in liver and kidney of the iberian hare (Lepus granatensis) from Spain. Research and Reviews. Journal of Veterinary Sciences. 2016;2(1):15–20.
83. Massányi P, Tataruch F, Slameka J, Toman R, Jurík R. Accumulation of lead, cadmium, and mercury in liver and kidney of the brown hare (Lepuseuropaeus) in relation to the season, age, and sex in the West Slovakian Lowland. Journal of Environmental Science and Health, Part A. 2003;38(7):1299–1309. https://doi.org/10.1081/ese-120021127
84. Kramárová M, Massányi P, Slamecka J, Tataruch F, Jancová A, Gasparik J, et al. Distribution of cadmium and lead in liver and kidney of some wild animals in Slovakia. Journal of Environmental Science and Health, Part A. 2005;40(3):593–600. https://doi.org/10.1081/ESE-200046605
85. Pedersen S, Lierhagen S. Heavy metal accumulation in arctic hares (Lepus arcticus) in Nunavut, Canada. Science of the Total Environment. 2006;368(2–3):951–955. https://doi.org/10.1016/j.scitotenv.2006.05.014
86. Halecki W, Gąsiorek M. Wajdzik M, Pająk M, Kulak D. Population parameters including breeding season of the European brown hare (Lepus europaeus) exposed to cadmium and lead pollution. Fresenius Environmental Bulletin. 2017;26(4):2998–3004.
87. Petrović Z, Teodorović V, Djurić S, Milićević D, Vranić D, Lukić M. Cadmium and mercury accumulation in European hare (Lepus europaeus): Age-dependent relationships in renal and hepatic tissue. Environmental Science and Pollution Research. 2014;21:14058–14068. https://doi.org/10.1007/s11356-014-3290-0
88. Shore RF, Douben PET. The ecotoxicological significance of cadmium intake and residues in terrestrial small mammals. Ecotoxicology and Environmental Safety. 1994;29(1):101–112. https://doi.org/10.1016/0147-6513(94)90035-3
89. Kottferová J, Korénedová B. Distribution of Cd and Pb in the tissues and organs of free-living animals in the territory of Slovakia. Bulletin of Environmental Contamination and Toxicology. 1998;60:171–176. https://doi.org/10.1007/s001289900607
90. Ehykhler V. Poisons in our diet. Moscow: Mir; 1985. 214 p. (In Russ.).
91. Alonso ML, Benedito JL, Miranda M, Castillo C, Hernández J, Shore RF. Arsenic, cadmium, lead, copper and zinc in cattle from Galicia, NW Spain. Science of the Total Environment Journal. 2000;246(2–3):237–248. https://doi.org/10.1016/s0048-9697(99)00461-1
92. Miranda M, Lopez-Alonso M, Castillo C, Hernández J, Benedito JL. Effect of sex on arsenic, cadmium, lead, copper and zinc accumulation in calves. Veterinary and Human Toxicology. 2000;42(5):265–268.
93. Kataev GD. Monitoring of populations of small mammals micromammalia in north taiga of Fennoscandia. Bulletin of Moscow Society of Naturalists. Biological Series. 2015;120(3):3–13. (In Russ.). https://elibrary.ru/VEBWPB
94. Bezel’ VS, Mukhacheva SV. Geochemical ecology of small mammals at industrially polluted areas: is there any effect of reduction in the emissions? Geochemistry International. 2020;65(8):823–832. (In Russ.). https://doi.org/10.31857/S0016752520070043; https://elibrary.ru/OQCKJD
95. Mukhacheva SV. Changes of small mammals communities around а nickel-copper smelter (Harjavalta, Finland). International Journal of Applied and Fundamental Research. 2013;(8–2):145–148. (In Russ.). https://elibrary.ru/QZGTMB
96. Mukhacheva SV. Long-term dynamics of small mammal communities in the period of reduction of copper smelter emissions: 1. Composition, abundance, and diversity. Russian Journal of Ecology. 2021;(1):66–76. (In Russ.). https://doi.org/10.31857/S0367059721010108; https://elibrary.ru/JKTMOH
97. Kataev GD, Suomela J, Palokangas P. Densities of microtinae rodents along a pollution gradientfrom a copper-nickel smelter. Oecologia. 1994;97:491–498. https://doi.org/10.1007/BF00325887
98. Kataev GD. The impact of industrial emissions of copper-nickel smelter complex on the status of populations and communities of small mammals in the Kola Peninsula. Nature Conservation Research. 2017;2(S2):19–27. (In Russ.). https://doi.org/10.24189/ncr.2017.033; https://elibrary.ru/ZDTXCH
99. Mukhacheva SV. Reproduction of the bank vole population Clethrionomys glareolus (Rodentia, Cricetidae) along the gradient of industrial environmental pollution. Zoologicheskiy Zhurnal. 2001;80(12):1509–1517. (In Russ.).
100. Moskvitina NS, Kuranova VN, Savel'ev SV. Abnormalities of embryonal development of vertebrates under the conditions of technogenic environmental pollution. Contemporary Problems of Ecology. 2011;18(4):487–495. (In Russ.). https://elibrary.ru/THJQWB
101. Salomeina NV, Mashak SV. Structural bases of mother-fetus relations at chemical interaction during embryogenesis. Journal of Siberian Medical Sciences. 2012;(1). (In Russ.). https://elibrary.ru/PBZZDZ
102. Mirzoev EB, Kobyalko VO, Gubina OA, Frolova NA. Response of the rat organism to the chronic exposure of cadmium low doses during the antenatal period. Toxicological Review. 2014;127(4):29–33. (In Russ.). https://elibrary.ru/ZCORTR
103. Benitez MA, Mendez-Armenta M, Montes S, Rembao D, Sanin LH, Rios C. Mother-fetus transference of lead and cadmium in rats: involvement of metallothionein. Histology and Histopathology. 2009;24:1523–1530. https://doi.org/10.14670/HH-24.1523
104. Vorobeychik EL, Sadykov OF, Farafontov MG. Ecological standardization of terrestrial ecosystems technogenic pollution (local scale). Yekaterinburg: Nauka; 1994. 280 p. (In Russ.).
105. Lebedeva NV. Ecotoxicology and biogeochemistry of geographic bird populations. Moscow: Nauka; 1999. 199 p. (In Russ.). https://elibrary.ru/RXMSTZ
106. Davletov IZ. Ecology of the beaver in an urban landscape. Kirov: VNIIOZ; 2005. 116 p. (In Russ.).
107. Ivanter EhV, Medvedev NV. Ecological toxicology of natural populations of birds and mammals in the North. Moscow: Nauka; 2008. 228 p. (In Russ.).
108. Ermakov VV, Tyutikov SF, Safonov VA. Biogeochemical indication of microelementoses. Moscow: Russian Academy of Sciences; 2018. 386 p. (In Russ.). https://elibrary.ru/YNHZUT
109. Dvornikov MG, Domskiy IA, Shiryaev VV. Sergeev AA. Ecology, conservation, and use of commercial mammal resources in North-East Europe. Kirov: VESI; 2021. 291 p. (In Russ.). https://elibrary.ru/QOWDLH