Patterns of mercury accumulation in the organs of bank vole Myodes glareolus (Rodentia, Cricetidae)


Keywords: terrestrial ecosystems pollution; heavy metals; mercury; small mammals; rodents.

Abstract

Mercury (Hg) and its compounds are among the most hazardous environmental pollutants with a high cumulative potential and they can have toxic effects on human and animal health even in low concentrations. Due to the increasing rate of human economic activity and the increase in the amount of Hg in the total cycling of matter, the study of its distribution, transformation, redistribution and accumulation in the abiotic and biotic components of various ecosystems remains important up to the present time. We assessed the content of metal in organs and tissues of the bank vole Myodes (Clethrionomys) glareolus Schreber, 1780 (Rodentia, Cricetidae), a widespread small rodent, caught in different biotopes of forest-steppe and steppe zones of Voronezh region. Measurements of Hg in samples were carried out with a mercury analyzer RA-915+ with the accessory PYRO (Lumex) using the atomic absorption method of cold steam without preliminary sample preparation (the lower limit of mercury detection in samples was 0.001 mg/kg). The sample size was 344 specimens. Mean Hg concentrations ranged from values below the analytical determination threshold to 0.887 mg/kg dry weight in the kidneys, 0.411 in the liver, 0.031 in the muscle tissue, and 0.040 in the brain. A positive correlation was found between the metal content in all possible pairs of organs (except for the “muscle – brain” pair) and a weak negative correlation was found between the Hg level and the mass of the animals. Hg concentrations in the studied organs did not differ between males and females. The metal content in the liver and kidneys of voles from the forest-steppe zone was significantly higher than in those from the steppe zone. Among all studied biotopes (meadow, pine and mixed forest, shrub thickets), the lowest concentrations were observed in animals living in pine forests, while the highest one – in more humidified bush thickets. During the vegetation season, there was a decrease in the average values of animal body mass in the samples and an increase in the content of Hg in the liver and kidneys. The results of the study are relevant in the assessment of atmospheric mercury pollution of terrestrial ecosystems using small mammals, such as Myodes glareolus, as a model object.

References

Bull, K. R., Roberts, R. D., Inskip, M. J., & Goodman, G. T. (1977). Mercury concentrations in soil, grass, earthworms and small mammals near an industrial emission source. Environmental Pollution, 12, 135–140.


Coleman, W. J. K., Engstrom, D. R., Mitchel, C. P. J., Swain, E. B., Monson, B. A., Balogh, S. J., Jeremiason, J. D., Branfireun, B. A., Kolka, R. K., & Almendinger, J. E. (2015). The effects of hydrologic fluctuation and sulfate regeneration on mercury cycling in an experimental peatland. Journal of Geophysical Research: Biogeosciences, 120, 1697–1715.


Cristol, D. A., Brasso, R. L., Condon, A. M., Fovargue, R. E., Friedman, S. L., Hallinger, K. K., Monroe, A. P., & White, A. E. (2008). The movement of aquatic mercury through terrestrial food webs. Science, 320, 335–335.


Eagles-Smith, C. A., Wiener, J. G., Eckley, C. S., Willacker J. J., Evers, D. C., Marvin-DiPasquale, M., Obrist, D., Fleck, J. A., Aiken, G. R., Lepak, J. M., Jackson, A. K., Webster, J. P., Stewart, A. R., Davis, J. A., Alpers, C. N., & Ackerman, J. T. (2016). Mercury in western North America: A synthesis of environmental contamination, fluxes, bioaccumulation, and risk to fish and wildlife. Science of the Total Environmenm, 568, 1213–1226.


Emel'yanova, A. A. (2008). Pitanie evropejskoj ryzhej polyovki verhovij Volgi i smezhnyh territorij. [ Feeding of bank vole in the upper Volga and adjacent territory ]Vestnik TvGU, Seriya Biologiya i Ekologiya, 10, 109–117 (in Russian).


Fedotov, V. I. (Ed.). (2013). Ekologo-geograficheskij atlas-kniga Voronezhskoj oblasti. [ Ecological-geographic atlas of Voroneezh oblast ]Izdatel'stvo Voronezhskogo Gosuniversiteta, Voronezh (in Russian).


Gann, G. L., Powell, C. H., Chumchal, M. M., & Drenner, R. W. (2015). Hg-contaminated terrestrial spiders pose a potential risk to songbirds at Caddo Lake (Texas. Louisiana, USA). Environmental Toxicology and Chemistry, 34, 303–306.


Gerstenberger, S. L., Cross, C. L., Divine, D. D., Gulmatico, M. L., & Rothweiler, A. M. (2006). Assessment of mercury concentrations in small mammals collected near Las Vegas, Nevada, USA. Environmental Toxicology, 21, 583–589.


Gilmour, C. C., Podar, M., Bullock, A. L., Graham, A. M., Brown, S. D., Somenahally, A. C., Johs, A., Hurt, R. A. Jr., Bailey, K. L., & Elias, D. A. (2013). Mercury methylation by novel microorganisms from new environments. Environmental Science and Technology, 47, 11810–11820.


Greenfield, B. K., Hrabik, T. R., Hervey, C. J., & Carpenten, S. R. (2011). Predicting mercury levels in yellow perch of water chemistry, trophic ecology and spatial traits. Canadian Journal of Fisheries and Aquatic Sciences, 58(7), 1419–1429.


Hsu-Kim, H., Kucharzyk, K. H., Zhang, T., & Deshusses, M. A. (2013). Mechanisms regulating mercury bioavailability for methylating microorganisms in the aquatic environment: A critical review. Environmental Science and Technology, 47, 2441–2456.


Kolka, R. K., Mitchell, C. P. J., Jeremiason, J. D., Hines, N. A., Grigal, D. F., Engstrom, D. R., Coleman-Wasik, J. K., Nater, E. A., Swain, E. B., Monson, B. A., Fleck, J. A., Johnson, B., Almendinger, J. E., Branfireun, B. A., Brezonik, P. L., & Cotner, J. B. (2011). Mercury cycling in peatland watersheds. Peatland biogeochemistry and watershed hydrology at the Marcell Experimental Forest. CRC Press, Boca Raton.


Komov, V. T., Gremyachirh, V. A., Sapel'nikov, S. F., & Udodenko, Y. G. (2010). Soderzhanie rtuti v pochvah i v melkih mlekopitayushchih razlichnyh biotopov Voronezhskogo zapovednika [ Content of mercury in soils and small mammals in different biotopes of Voronezh Nature Reserve ] [Rtut' v biosfere: Ekologo-geohimicheskie aspekty]. GEOHI RAN, Moscow. Pp. 281–283 (in Russian).


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). Environmental Monitoring and Assessment, 189, 104.


Lindberg, S., Bullock, R., Ebinghaus, R., Engstrom, D., Feng, X., Fitzgerald, W., Pirrone, N., Prestbo, E., & Seigneur, C. (2007). A synthesis of progress and uncertainties in attributing the sources of mercury in deposition. Ambio, 36(1), 19–32.


Mason, R. P., & Sheu, G. R. (2002). Role of the ocean in the global mercury cycle. Global Biogeochemical Cycles, 16(4), 1093.


Oswald, C. J., Heyes, A., & Branfireun, B. A. (2014). Fate and transport of ambient mercury and applied mercury isotope in terrestrial upland soils: Insights from the metaalicus watershed. Environmental Science and Technology, 48, 1023–1031.


Rimmer, C. C., Miller, E. K., McFarland, K. P., Taylor, R. J., & Faccio, S. D. (2010). Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology, 19(4), 697–709.


Rutkowska, M., Bajger-Nowak, G., Kowalewska, D., Bzoma S., Kalisińska, E., Namieśnik, J., & Konieczka, Р. (2019). Methylmercury and total mercury content in soft tissues of two birdspecies wintering in the Baltic Sea near Gdansk, Poland. Chemosphere, 219, 140–147.


Petkovsek, S. A., Kopusar, N., & Krystufek, B. (2014). Small mammals as biomonitors of metal pollution: A case study in Slovenia. Environmental Monitoring and Assessment, 186, 4261–4274.


Sánchez-Chardi, A., & López-Fuster, M. (2009). Metal and metalloid accumulation in shrews (Soricomorpha, Mammalia) from two protected Mediterranean costal sites. Environmental Pollution, 157, 1243–1248.


Sánchez-Chardi, A., Ribeiro, C. A. O., & Nadal, J. (2009). Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. Chemosphere, 76, 387–394.


Selin, N. E. (2009). Global biogeochemical cycling of mercury: A review. Annual Review of Environment and Resources, 34(1), 43–63.


Shchipanov, N. A., Kupcov, A. V., Kalinin, A. A., Demidova, T. B., Olejnichenko, V. Y., Lyapina, M. G., Aleksandrov, D. Y., Raspopova, A. A., Pavlova, S. V., & Tumas'yan, F. A. (2010). Melkie mlekopitayushchie yugo-vostoka Tverskoj oblasti. Soobshchenie 1. Fauna i biotopicheskoe raspredelenie. [ Small mammals of southeast Tver oblast . Report 1. Fauna and biotopic distribution ] Sibirskij Ekologicheskij Zhurnal, 17(5), 799–806 (in Russian).


Sneddon, J., Clement, R., Riby, P., & Lepp, N. W. (2009). Source-pathway-receptors investigation of the fate of trace elements derived from shot-gun pellets discharged in terrestrial ecosystems managed for game shooting. Environmental Pollution, 157, 2663–2669.


Talmage, S. S., & Walton, B. T. (1993). Food chain transfer and potential renal toxicity of mercury to small mammals at a contaminated terrestrial field site. Ecotoxicology, 2, 243–256.


Tavshunsky, I., Eggert, S. L., & Mitchell, C. P. J. (2017). Accumulation of methylmercury in invertebrates and masked shrews (Sorex cinereus) at an upland forest–peatland interface in Northern Minnesota, USA. Bulletin of Environmental Contamination and Toxicology, 99(6), 673–678.


Tjerngren, I., Karlsson, T., Bjorn, E., & Skyllberg, U. (2012). Potential Hg methylation and MeHg demethylation rates related to the nutrient status of different boreal wetlands. Biogeochemistry, 108, 335–350.


Topashka-Ancheva, M., Metcheva, R., & Teodorova, S. (2003). A comparative analysis of the heavy metal loading of small mammals in different regions of Bulgaria II: Chromosomal aberrations and blood pathology. Ecotoxicology and Environmental Safety, 54(2), 188–193.


Vucetich, L. M., Vucetich, J. A., Cleckner, L. B., Gorski, P. R., & Peterson, R. O. (2001). Mercury concentration in deer mouse (Peromyceus maniculatus) tissues from Isle Royale National Park. Environmental Pollution, 114, 113–118.

Published
2019-11-09
Section
Articles