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Bones of Free-Living Ungulates as Indicators of Environmental Contamination by Mercury: A Comparative Study between the Western Carpathians and Zhongar Alatau Cover

Bones of Free-Living Ungulates as Indicators of Environmental Contamination by Mercury: A Comparative Study between the Western Carpathians and Zhongar Alatau

Open Access
|Jun 2025

References

  1. Ajsuvakova, O.P., Tinkov, A.A., Aschner, M., Rocha, J.B., Michalke, B., Skalnaya, M.G., Skalny, A.V., Butnariu, M., Dadar, M., Sarac, I., Aaseth, J. & Bjørklund G. (2020). Sulfhydryl groups as targets of mercury toxicity. Coordin. Chem. Rev., 417, 213343. DOI: 10.1016/j.ccr.2020.213343.
  2. Álvarez-Fernández, N., Cortizas, A.M. & López-Costas O. (2022) Structural equation modelling of mercury intra-skeletal variability on archaeological human remains. Sci. Total Environ., 851, 158015. DOI: 10.1016/j.scitotenv.2022.158015.
  3. Álvarez-Fernández, N., Martínez Cortizas, A., García-López, Z. & López-Costas O. (2021). Approaching mercury distribution in burial environment using PLS-R modelling. Sci. Rep., 11(1), 21231. DOI: 10.1038/s41598-021-00768-8.
  4. Ballová, Z. & Janiga M. (2018). Lead levels in the bones of small rodents from alpine and subalpine habitats in the Tian-Shan Mountains, Kyrgyzstan. Atmosphere, 9(2), 35. DOI: 10.3390/atmos9020035.
  5. Ballová, Z., Janiga, M. & Hančinský R. (2019). Comparison of element concentrations (Ba, Mn, Pb, Sr, Zn) in the bones and teeth of wild ruminants from the West Carpathians and the Tian-Shan Mountains as indicators of air pollution. Atmosphere, 10(2), 64. DOI: 10.3390/atmos10020064.
  6. Bing, H., Zhou, J., Wu, Y., Luo, X., Xiang, Z., Sun, H., Wang, J. & Zhu H. (2018). Barrier effects of remote high mountain on atmospheric metal transport in the eastern Tibetan Plateau. Sci. Total Environ., 628, 687‒696. DOI: 10.1016/j.scitotenv.2018.02.035.
  7. Bjørklund, G., Dadar, M., Mutter, J. & Aaseth J. (2017). The toxicology of mercury: Current research and emerging trends. Environ. Res., 159, 545‒554. DOI: 10.1016/j.envres.2017.08.051.
  8. Blackwell, B.D. & Driscoll C.T. (2015). Deposition of mercury in forests along a montane elevation gradient. Environ. Sci. Technol., 49(9), 5363‒5370. DOI: 10.1021/es505928w.
  9. Butler-Valverde, M.J., DeVault, T.L., Rhodes Jr, O.E. & Beasley J.C. (2022). Carcass appearance does not influence scavenger avoidance of carnivore carrion. Sci. Rep., 12(1), 18842. DOI: 10.1038/s41598-022-22297-8.
  10. Cappelli, J., Frasca, I., García, A., Landete-Castillejos, T., Luccarini, S., Gallego, L., Morimando, F., Varuzza, P. & Zaccaroni M. (2020). Roe deer as a bioindicator: preliminary data on the impact of the geothermal power plants on the mineral profile in internal and bone tissues in Tuscany (Italy). Environ. Sci. Pollut. Res., 27, 36121‒36131. DOI: 10.1007/s11356-020-09708-x.
  11. Cervini-Silva, J., de Lourdes Muñoz, M., Palacios, E., Ufer, K. & Kaufhold S. (2021). Natural incorporation of mercury in bone. J. Trace Elem. Med. Bio., 67, 126797. DOI: 10.1016/j.jtemb.2021.126797.
  12. Chen, L., Wang, H.H., Liu, J.F., Tong, Y.D., Ou, L.B., Zhang, W., Hu, D., Chen, C. & Wang X.J. (2014). Intercontinental transport and deposition patterns of atmospheric mercury from anthropogenic emissions. Atmos. Chem. Phys., 14, 10163–10176. DOI: 10.5194/acp-14-10163-2014.
  13. Chyla, A., Lorenz, K., Gaggi, C. & Renzoni A. (1996). Pollution effects on wildlife: roe deer antlers as non-destructive bioindicator. Environ. Prot. Eng., 3, 65‒70.
  14. Dahmardeh Behrooz, R., Poma, G. & Barghi M. (2022). Non-destructive mercury exposure assessment in the Brandt’s hedgehog (Paraechinus hypomelas): spines as indicators of endogenous concentrations. Environ. Sci. Pollut. Res., 29(37), 56502‒56510. DOI: 10.1007/s11356-022-19926-0.
  15. Dainowski, B.H., Duffy, L.K., McIntyre, J. & Jones P. (2015). Hair and bone as predictors of tissular mercury concentration in the Western Alaska Red Fox, Vulpes vulpes. Sci. Total Environ., 518, 526‒533. DOI: 10.1016/j.scitotenv.2015.03.013.
  16. Demesko, J., Markowski, J., Demesko, E., Słaba, M., Hejduk, J. & Minias P. (2019). Ecotype variation in trace element content of hard tissues in the European roe deer (Capreolus capreolus). Arch. Environ. Con. Tox., 76(1), 76‒86. DOI: 10.1007/s00244-018-0580-4.
  17. Demesko, J., Markowski, J., Słaba, M., Hejduk, J. & Minias P. (2018). Age-related patterns in trace element content vary between bone and teeth of the European roe deer (Capreolus capreolus). Arch. Environ. Con. Tox., 74(2), 330‒338. DOI: 10.1007/s00244-017-0470-1.
  18. Emslie, S.D., Alderman, A., McKenzie, A., Brasso, R., Taylor, A.R., Moreno, M.M., Cambra-Moo, O., Martín, A.G., Silva, A.M., Valera, A., Sanjuán, L.G. & Vila E.V. (2019). Mercury in archaeological human bone: biogenic or diagenetic?. J. Archaeol. Sci., 108, 104969. DOI: 10.1016/j.jas.2019.05.005.
  19. Florencio-Silva, R., da Silva Sasso, G.R., Sasso-Cerri, E., Simões, M.J. & Cerri P.S. (2015). Biology of bone tissue: structure, function, and factors that influence bone cells. Bio. Med. Res. Int., 421746. DOI: 10.1155/2015/421746.
  20. Gerson, J.R., Driscoll, C.T., Demers, J.D., Sauer, A.K., Blackwell, B.D., Montesdeoca, M.R., Shanley, J.B. & Ross D.S. (2017). Deposition of mercury in forests across a montane elevation gradient: Elevational and seasonal patterns in methylmercury inputs and production. J. Geophys. Res.-Biogeo., 122(8), 1922‒1939. DOI: 10.1002/2016JG003721.
  21. Giżejewska, A., Nawrocka, A., Szkoda, J., Żmudzki, J., Jaroszewski, J. & Giżejewski Z. (2016). Variations of selected trace element contents in two layers of red deer antlers. J. Vet. Res., 60(4), 467‒471. DOI: 10.1515/jvetres-2016-0069.
  22. Giżejewska, A., Szkoda, J., Nawrocka, A., Żmudzki, J. & Giżejewski Z. (2017). Can red deer antlers be used as an indicator of environmental and edible tissues’ trace element contamination?. Environ. Sci. Pollut. Res., 24(12), 11630‒11638. DOI: 10.1007/s11356-017-8798-7.
  23. Gnamuš, A., Byrne, A.R. & Horvat M. (2000). Mercury in the soil-plant-deer-predator food chain of a temperate forest in Slovenia. Environ. Sci. Technol., 34(16), 3337‒3345. DOI: 10.1021/es991419w.
  24. Gochfeld, M. (2003). Cases of mercury exposure, bioavailability, and absorption. Ecotox. Environ. Safe., 56(1), 174-179. DOI: 10.1016/S0147-6513(03)00060-5.
  25. Guney, M., Kumisbek, A., Akimzhanova, Z., Kismelyeva, S., Beisova, K., Zhakiyenova, A., Inglezakis, V. & Karaca F. (2021). Environmental partitioning, spatial distribution, and transport of atmospheric mercury (Hg) originating from a site of former chlor-alkali plant. Atmosphere, 12(2), 275. DOI: 10.3390/atmos12020275.
  26. Gworek, B., Dmuchowski, W. & Baczewska-Dąbrowska A.H. (2020). Mercury in the terrestrial environment: A review. Environ. Sci. Europe., 32(1), 1‒19. DOI: 10.1186/s12302-020-00401-x.
  27. Hammer, Ø., Harper, D. & Ryan P. (2001). PAST: Palaeontological Statistics Software Package for Education and Data Analysis. Version 4.03. Palaeontol Electron 4, 9 (computer software).
  28. Janiga, M. & Haas M. (2019). Alpine accentors as monitors of atmospheric long-range lead and mercury pollution in alpine environments. Environ. Sci. Pollut. Res., 26, 2445‒2454. DOI: 10.1007/s11356-018-3742-z.
  29. Janiga, M., Hrehová, Z., Dimitrov, K., Gerasimova, C. & Lovari S. (2016). Lead levels in the bones of snow voles Chionomys nivalis (Martins, 1842) (Rodentia) from European mountains: A comparative study of populations from the Tatra (Slovakia), Vitosha and Rila (Bulgaria). Acta Zool. Bulgar., 68(2), 291‒295.
  30. Jitaru, P. & Adams F. (2004). Toxicity, sources and biogeochemical cycle of mercury. J. Phys., 121, 185‒193. DOI: 10.1051/jp4:2004121012.
  31. Kalisinska, E., Lanocha-Arendarczyk, N. & Podlasinska J. (2021). Current and historical nephric and hepatic mercury concentrations in terrestrial mammals in Poland and other European countries. Sci. Total Environ., 775, 145808. DOI: 10.1016/j.scitotenv.2021.145808
  32. Karaca, F., Kumisbek, A., Inglezakis, V.J., Azat, S., Zhakiyenova, A., Ormanova, G. & Guney M. (2021). DiMIZA: A dispersion modeling based impact zone assessment of mercury (Hg) emissions from coal-fired power plants and risk evaluation for inhalation exposure. Engineering Reports, 3(7), e12357. DOI: 10.1002/eng2.12357.
  33. Komov, V.T., Ivanova, E.S., Poddubnaya, N.Y. & Gremyachikh V.A. (2017). Mercury in soil, earthworms and organs of voles Myodes glareolus and shrew Sorex araneus in the vicinity of an industrial complex in Northwest Russia (Cherepovets). Environ. Monit. Assess., 189, 1‒8. DOI: 10.1007/s10661-017-5799-4.
  34. Kompišová Ballová, Z., Janiga, M., Holub, M. & Chovancová G. (2021). Temporal and seasonal changes in mercury accumulation in Tatra chamois from West Carpathians. Environ. Sci. Pollut. Res., 28(37), 52133‒52146. DOI: 10.1007/s11356-021-14380-w.
  35. Kompišová Ballová, Z., Korec, F. & Pinterová K. (2020). Relationship between heavy metal accumulation and histological alterations in voles from alpine and forest habitats of the West Carpathians. Environ. Sci. Pollut. Res., 27, 36411‒36426. DOI: 10.1007/s11356-020-09654-8.
  36. Lanocha, N., Kalisinska, E., Kosik-Bogacka, D.I., Budis, H. & Noga-Deren K. (2012). Trace metals and micronutrients in bone tissues of the red fox Vulpes vulpes (L., 1758). Acta Theriol., 57, 233‒244. DOI: 10.1007/s13364-012-0073-1.
  37. Lanocha, N., Kalisinska, E., Kosik-Bogacka, D.I., Budis, H., Sokolowski, S. & Bohatyrewicz A. (2013). Comparison of metal concentrations in bones of long-living mammals. Biol. Trace Elem. Res., 152(2), 195‒203. DOI: 10.1007/s12011-013-9615-x.
  38. Lazarus, M., Vicković, I., Šoštarić, B. & Blanuša M. (2005). Heavy metal levels in tissues of red deer (Cervus elaphus) from eastern Croatia. Arh. Hig. Rada Toksiko., 56(3), 233‒240.
  39. Ma, Y., Shang, L., Hu, H., Zhang, W., Chen, L., Zhou, Z., Singh, P.B. & Hu Y. (2021). Mercury distribution in the East Himalayas: Elevational patterns in soils and non-volant small mammals. Environ. Pollut., 288, 117752. DOI: 10.1016/j.envpol.2021.117752.
  40. Maňkovská, B., Oszlányi, J. & Barančok P. (2008). Measurement of the atmosphere loading of the Slovak Carpathians using bryophyte. Ekológia (Bratislava), 27(4), 339‒350.
  41. Martinková, B., Janiga, M. & Pogányová A. (2019). Mercury contamination of the snow voles (Chionomys nivalis) in the West Carpathians. Environ. Sci. Pollut. Res., 26, 35988‒35995. DOI: 10.1007/s11356-019-06714-6.
  42. Mowat, L.D., St. Louis, V.L., Graydon, J.A. & Lehnherr I. (2011). Influence of forest canopies on the deposition of methylmercury to boreal ecosystem watersheds. Environ. Sci. Technol., 45(12), 5178‒5185. DOI: 10.1021/es104377y.
  43. Nawrocka, A., Durkalec, M., Szkoda, J., Filipek, A., Kmiecik, M., Żmudzki, J. & Posyniak A. (2020). Total mercury levels in the muscle and liver of livestock and game animals in Poland, 2009–2018. Chemosphere, 258, 127311. DOI: 10.1016/j.chemosphere.2020.127311.
  44. Pacyna, E.G., Pacyna, J.M., Steenhuisen, F. & Wilson S. (2006). Global anthropogenic mercury emission inventory for 2000. Atmos. Environ., 40(22), 4048‒4063. DOI: 10.1016/j.atmosenv.2006.03.041.
  45. Panagos, P., Jiskra, M., Borrelli, P., Liakos, L. & Ballabio C. (2021). Mercury in European topsoils: Anthropogenic sources, stocks and fluxes. Environ. Res., 201, 111556. DOI: 10.1016/j.envres.2021.111556.
  46. Patra, M. & Sharma A. (2000). Mercury toxicity in plants. Bot. Rev., 66, 379‒422.DOI: 10.1007/BF02868923.
  47. Peers, M.J., Konkolics, S.M., Majchrzak, Y.N., Menzies, A.K., Studd, E.K., Boonstra, R., Boutin, S. & Lamb C.T. (2021). Vertebrate scavenging dynamics differ between carnivore and herbivore carcasses in the northern boreal forest. Ecosphere, 12(8), e03691. DOI: 10.1002/ecs2.3691.
  48. Pirrone, N., Cinnirella, S., Feng, X., Finkelman, R.B., Friedli, H.R., Leaner, J., Mason, R., Mukherjee, A.B., Stracher, G.B., Streets, D.G. & Telmer K. (201). Global mercury emissions to the atmosphere from anthropogenic and natural sources. Atmos. Chem. Phys., 10(13), 5951‒5964. DOI: 10.5194/acp-10-5951-2010,2010.
  49. Rasmussen, L.K., Skytte, L., D’imporzano, P., Orla Thomsen, P., Søvsø, M. & Lier Boldsen J. (2017). On the distribution of trace element concentrations in multiple bone elements in 10 Danish medieval and post-medieval individuals. Am. J. Phys. Anthropol., 162(1), 90‒102. DOI: 10.1002/ajpa.23099.
  50. Rasmussen, K.L., Skytte, L., Pilekær, C., Lauritsen, A., Boldsen, J.L., Leth, P.M. & Thomsen P.O. (2013). The distribution of mercury and other trace elements in the bones of two human individuals from medieval Denmark–the chemical life history hypothesis. Heritage Sci., 1, 1‒13. DOI: 10.1186/2050-7445-1-10.
  51. Ryaboshapko, A., Ilyin, I., Gusev, A. & Afinogenova O. (1998). Mercury in the atmosphere of Europe: concentrations, deposition patterns, transboundary fluxes. Moscow: Meteorological Synthesizing Centre-East.
  52. Schröder, W., Holy, M., Pesch, R., Harmens, H., Ilyin, I., Steinnes, E., Alber, R., Aleksiayenak, Y., Blum, O., Coskun, M., Dam, M., De Temmerman, L., Frolova, M., Frontasyeva, M., Gonzalez Miquelo, L., Grodzinska, K., Jeran, Z., Korzekva, S., Kubin, K., Kvietkus, K., Leblond, S., Liiv, S., Maňkovská, B., Piispanen, J., Rühling, Å., Santamaria, J., Spiric, Z., Suchara, I., Thöni, L., Yurukova, L. & Zechmeister H.G. (2010). Are cadmium, lead and mercury concentrations in mosses across Europe primarily determined by atmospheric deposition of these metals?. J. Soil Sediment., 10, 1572‒1584. DOI: 10.1007/s11368-010-0254-y.
  53. Skibniewska, E.M. & Skibniewski M. (2023). Mercury Contents in the Liver, Kidneys and Hair of Domestic Cats from the Warsaw Metropolitan Area. Appl. Sci., 13(1), 269. DOI: 10.3390/app13010269.
  54. Tajchman, K., Ukalska-Jaruga, A., Bogdaszewski, M., Pecio, M. & Dziki-Michalska K. (2020). Accumulation of toxic elements in bone and bone marrow of deer living in various ecosystems. A case study of farmed and wild-living deer. Animals, 10(11), 2151. DOI: 10.3390/ani10112151.
  55. Tajchman, K., Ukalska-Jaruga, A., Bogdaszewski, M., Pecio, M. & Janiszewski P. (2021). Comparison of the accumulation of macro-and microelements in the bone marrow and bone of wild and farmed red deer (Cervus elaphus). BMC Vet. Res., 17(1), 1‒11. DOI: 10.1186/s12917-021-03041-2.
  56. Townsend, J.M., Driscoll, C.T., Rimmer, C.C. & McFarland K.P. (2014). Avian, salamander, and forest floor mercury concentrations increase with elevation in a terrestrial ecosystem. Environ. Toxicol. Chem., 33(1), 208‒215. DOI: 10.1002/etc.2438.
  57. Travnikov, O. (2005). Contribution of the intercontinental atmospheric transport to mercury pollution in the Northern Hemisphere. Atmos. Environ., 39(39), 7541‒7548. DOI: 10.1016/j.atmosenv.2005.07.066.
  58. Tripathee, L., Guo, J., Kang, S., Paudyal, R., Sharma, C.M., Huang, J., Chen, P., Ghimire, P.S., Sigdel, M. & Sillanpää M. (2020). Measurement of mercury, other trace elements and major ions in wet deposition at Jomsom: The semi-arid mountain valley of the Central Himalaya. Atmos. Res., 234, 104691. DOI: 10.1016/j.atmosres.2019.104691.
  59. Valašková, M. & Janiga M. (2014). Metal contamination in vertebrates from the Tjan-Shan mountains. Oecol. Montana., 23(1), 1‒12.
  60. Yang, Z., Guo, J., Sun, S., Ni, D., Chen, P., Rupakheti, D., Kang, H., Abdullaev, S.F., Abdyzhaparuulu, S. & Kang S. (2023). Spatial distribution and risk assessments of mercury in topsoils of Central Asia. Geosci. Front., 14(4), 101585. DOI: 10.1016/j.gsf.2023.101585.
  61. Zaccaroni, A., Scaravelli, D., De Battisti, R., Zanella, A. & Gelli D. (2008). Toxicological survey of free ranging population of roe deer (Capreolus capreolus) and red deer (Cervus elaphus) by teeth examination. Natura Croatica: Periodicum Musei Historiae Naturalis Croatici, 17(4), 273‒281.
  62. Zhang, H., Yin, R. S., Feng, X. B., Sommar, J., Anderson, C. W., Sapkota, A., Fu, X. & Larssen T. (2013). Atmospheric mercury inputs in montane soils increase with elevation: evidence from mercury isotope signatures. Sci. Rep., 3(1), 3322. DOI: 10.1038/srep03322.
DOI: https://doi.org/10.2478/eko-2025-0001 | Journal eISSN: 1337-947X | Journal ISSN: 1335-342X
Language: English
Page range: 1 - 7
Submitted on: Oct 1, 2024
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Accepted on: Mar 27, 2025
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Published on: Jun 19, 2025
In partnership with: Paradigm Publishing Services
Publication frequency: 2 issues per year

© 2025 Lenka Zábojníková, Samuel Feješ, Berikzhan Oxikbayev, Togzhan Kasymkhanova, Marián Janiga, Zuzana Kompišová Ballová, published by Slovak Academy of Sciences, Institute of Landscape Ecology
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