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Structural–functional aberrations of erythrocytes in the northern red-backed vole (Clethrionomys rutilus Pallas, 1779) that inhabits the zone of influence of the copper smelter (the Middle Ural)

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Abstract

Red blood cell parameters were assessed in a natural population of the northern red-backed vole (Clethrionomys rutilus Pallas, 1779) in the zone of influence of the Kirovgrad Copper Smelter along a gradient of pollution by heavy metals (Cu, Zn, Cd, and Pb) at three catching sites (polluted [Imp] and controls [Bg-1, and Bg-2]). The difference of the smelter area (Imp group of voles) from both background groups (Bg-1 and Bg-2) was proven by means of a set of 13 parameters in univariate and multivariate analyses. Among the detected erythrocyte disturbances, we noted the following: a decrease in activities of Na+,K+-ATPase and antioxidant enzymes (SOD, GSH-Px, and CAT); an increase in the concentration of lipid peroxidation products, in osmotic fragility, and in intravascular hemolysis; interruption of carbohydrate metabolism; and lowered oxygen-carrying capacity. A higher load of Cd (p = 0.0009) and possibly Pb (p = 0.054) in the Imp animals was confirmed by quantitation of heavy metals in the liver. Most erythrocyte parameters (11 out of 13) covaried with individual Cd load by obeying a semilogarithmic dependence; such a relation was not found for Cu, Zn, and Pb. A decrease in the growth rate of structural and functional erythrocyte aberrations (“resistance improvement”) with increasing cadmium load is probably due to compensatory enhancement of the synthesis of metallothioneins in the liver and kidneys and hence a greater proportion of Cd bound to metallothioneins. Problems of differences/similarities in Cd-associated reactivity among the animals are discussed too, taking into account the catching sites (polluted [Imp] and controls [Bg-1, and Bg-2]) and reproductive-age (i.e., immature underyearlings, mature underyearlings, and individuals that overwintered). The persistence of differences in erythrocyte status observed by us between the Imp and background groups after normalization to Cd load may be due to the action of other (unexamined) adverse factors and calls for further ecotoxicological studies.

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Baseline data analyzed in this study are presented in Supplementary Info File 3.

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Acknowledgements

The authors are grateful to the leading engineer of the Laboratory of Ecotoxicology of Populations and Communities E.Kh. Akhunova for measuring the concentrations of HMs.

Funding

This study was supported by the State Contract (No 122021000076-9) of the Institute of Plant and Animal Ecology, the Ural Branch of the Russian Academy of Sciences.

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Natal´ya A. Orekhova carried out hematological tests, statistical processing of data and their interpretation. Yulia A. Davydova and Georgii Yu. Smirnov were responsible for сatching voles, maintenance, and analysis of reproductive-age groups. Natal´ya A. Orekhova and Yulia A. Davydova wrote the main manuscript text. All authors reviewed the manuscript.

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Correspondence to Natal’ya A. Orekhova.

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The authors declare no competing interests.

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The authors declare no conflicts of interest in relation to the work presented.

Ethical approval

All procedures performed on the animals complied with the ethical standards of the Institute of Plants and Animals of Ecology, the Ural Branch of the Russian Academy of Sciences (Protocol No. 3 dated 18 December 2014).

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Orekhova, N.A., Davydova, Y.A. & Smirnov, G.Y. Structural–functional aberrations of erythrocytes in the northern red-backed vole (Clethrionomys rutilus Pallas, 1779) that inhabits the zone of influence of the copper smelter (the Middle Ural). Biometals 36, 847–864 (2023). https://doi.org/10.1007/s10534-022-00478-2

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  • DOI: https://doi.org/10.1007/s10534-022-00478-2

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