Water, Air, & Soil Pollution

, Volume 218, Issue 1–4, pp 603–610 | Cite as

Uptake and Accumulation of Anthropogenic Os in Free-Living Bank Voles (Myodes glareolus)

  • Ilia Rodushkin
  • Emma Engström
  • Dieke Sörlin
  • Douglas Baxter
  • Birger Hörnfeldt
  • Erik Nyholm
  • Frauke Ecke


Osmium tetroxide (OsO4) is one of the most toxic air contaminants but its environmental effects are poorly understood. Here, for the first time, we present evidence of osmium uptake in a common herbivore (bank vole, Myodes glareolus) in boreal forests of northern Sweden. Voles (n = 22) and fruticose arboreal pendular lichens, the potential main winter food source of the vole, were collected along a spatial gradient to the west of a steelwork in Tornio, Finland at the Finnish–Swedish border. 187Os/188Os isotope ratios increased and osmium concentrations decreased in lichens and voles along the gradient. Osmium concentrations in lichens were 10,000-fold higher than those in voles. Closest to the steelwork, concentrations were highest in kidneys rather than skin/fur that are directly exposed to airborne OsO4. The kidney-to-body weight ratio was higher at the two localities close to the steelwork. Even though based on a small sample size, our results for the first time demonstrate that osmium is taken up, partitioned, and accumulated in mammal tissue, and indicate that high kidney-to-body weight ratios might be induced by anthropogenic osmium.


Boreal forest Herbivore Kidney-to-body weight ratio Metal uptake Spatial gradient 



The project was funded via a grant of VINNOVA (Grant no. P32060-1) and of the Board of Faculty, Luleå University of Technology, to F. Ecke.


  1. Angerbjörn, A., Tannerfeldt, M., Bjärvall, A., Ericson, M., From, J., & Norén, E. (1995). Dynamics of the arctic fox population in Sweden. Annales Zoologici Fennici, 32, 55–68.Google Scholar
  2. Arnborg, T. (1990). Forest types of northern Sweden. Introduction to and translation of “Det nordsvenska skogstypsschemat”. Vegetatio, 90, 1–13.CrossRefGoogle Scholar
  3. Bankowska, J., & Hine, C. (1985). Retention of lead in the rat. Archives of Environmental Contamination and Toxicology, 14, 621–629.CrossRefGoogle Scholar
  4. Ecke, F., Löfgren, O., & Sörlin, D. (2002). Population dynamics of small mammals in relation to forest age and structural habitat factors in northern Sweden. Journal of Applied Ecology, 39, 781–792.CrossRefGoogle Scholar
  5. Engström, E., Stenberg, A., Senioukh, S., Edelbro, R., Baxter, D. C., & Rodushkin, I. (2004). Multi-elemental characterization of soft biological tissues by inductively coupled plasma-sector field mass spectrometry. Analytica Chimica Acta, 521, 123–135.CrossRefGoogle Scholar
  6. Ericson, L. (1977). The influence of voles and lemmings on the vegetation in a coniferous forest during a 4-year period in northern Sweden. Wahlenbergia, 4, 1–114.Google Scholar
  7. Erlinge, S., Göransson, G., Hansson, L., Högstedt, G., Liberg, O., Nilsson, I. N., et al. (1983). Predation as a regulating factor on small rodent populations in southern Sweden. Oikos, 40, 36–52.CrossRefGoogle Scholar
  8. Garty, J. (2001). Biomonitoring atmospheric heavy metals with lichens: theory and application. Critical Reviews in Plant Sciences, 20, 309–371.CrossRefGoogle Scholar
  9. Gebczynska, Z. (1983). Feeding habits. In: K. Petrusewicz (ed.), Ecology of the bank vole: Acta Theriologica, Vol. 28 (S1), 40–49.Google Scholar
  10. Goyer, R. A., Leonard, D. L., Moore, J. F., Rhyne, B., & Krigman, M. R. (1970). Lead dosage and the role of the intranuclear inclusion body. An experimental study. Archives of Environmental Health, 20, 705–711.Google Scholar
  11. Hansson, L. (1978). Small mammal abundance in relation to environmental variables in three Swedish forest phases. Uppsala: The Swedish University of Agricultural Sciences. Studia Forestalia Suecica Nr 147.Google Scholar
  12. Hansson, L. (1985a). Clethrionomys food; generic, specific and regional characteristics. Annales Zoologici Fennici, 22, 315–318.Google Scholar
  13. Hansson, L. (1985b). The food of bank voles, wood mice and yellow-necked mice. In J. R. Flowerdew, J. Gurnell, & J. H. W. Gipps (Eds.), The ecology of woodland rodents: bank voles and wood mice (pp. 141–168). Oxford: Symposia of the Zoological Society of London.Google Scholar
  14. Hayes, T. L., Lindgren, F. T., & Gofman, J. W. (1963). A quantitative determination of the osmium tetroxide–lipoprotein interaction. The Journal of Cell Biology, 19, 251–255.CrossRefGoogle Scholar
  15. Hörnfeldt, B. (1994). Delayed density dependence as a determinant of vole cycles. Ecology, 75, 791–806.CrossRefGoogle Scholar
  16. Hörnfeldt, B. (2004). Long-term decline in numbers of cyclic voles in boreal Sweden: analyses and presentation of hypotheses. Oikos, 107, 376–392.CrossRefGoogle Scholar
  17. Hörnfeldt, B., & Nyholm, N. E. I. (1996). Breeding performance of Tengmalm’s owl in a heavy metal pollution gradient. Journal of Applied Ecology, 33, 377–386.CrossRefGoogle Scholar
  18. Hörnfeldt, B., Carlsson, B. G., Löfgren, O., & Eklund, U. (1990). Effects of cyclic food supply on breeding performance in Tengmalm’s owl. Canadian Journal of Zoology, 68, 522–530.CrossRefGoogle Scholar
  19. Leffler, P. E., & Nyholm, E. I. (1996). Nephrotoxic effects in free-living bank voles in a heavy metal polluted environment. Ambio, 25, 417–420.Google Scholar
  20. Löfgren, O. (1995). Spatial organization of cyclic Clethrionomys females: occupancy of all available space at peak densities? Oikos, 72, 29–35.CrossRefGoogle Scholar
  21. Ma, W. C. (1989). Effect of soil pollution with metallic lead pellets on lead bioaccumulation and organ/body weight alterations in small mammals. Archives of Environmental Contamination and Toxicology, 18, 617–622.CrossRefGoogle Scholar
  22. McLaughlin, A. I. G. (1946). Toxic manifestations of osmium tetroxide. British Journal of Industrial Medicine, 3, 183–186.Google Scholar
  23. Milton, A., Cooke, J. A., & Johnson, M. S. (2003). Accumulation of lead, zinc, and cadmium in a wild population of Clethrionomys glareolus from an abandoned lead mine. Archives of Environmental Contamination and Toxicology, 44, 405–411.CrossRefGoogle Scholar
  24. Najrana, T., Saito, Y., Uraki, F., Kubo, K., & Yamamoto, K. (2000). Spontaneous and osmium tetroxide-induced mutagenesis in an Escherichia coli strain deficient in both endonuclease III and endonuclease VIII. Mutagenesis, 15, 121–125.CrossRefGoogle Scholar
  25. OSHA (Occupational Safety and Health Administration). (1993). Incorporation of General Industry Safety and Health Standards Applicable to Construction Work. Report nr 1993:29 CFR Part 1926, Federal Register #58:35076-35306.Google Scholar
  26. Pulliainen, E., & Keränen, J. (1979). Composition and functions of beard lichen stores accumulated by bank voles, Clethrionomys glareolus Schreb. Aquilo Ser Zoologica, 19, 73–76.Google Scholar
  27. Rodushkin, I., Bergman, T., Douglas, G., Engström, E., Sörlin, D., & Baxter, D. C. (2007a). Authentication of Kalix (N.E. Sweden) vendace caviar using inductively coupled plasma-based analytical techniques: Evaluation of different approaches. Analytica Chimica Acta, 583, 310–318.CrossRefGoogle Scholar
  28. Rodushkin, I., Engström, E., Sörlin, D., Pontér, C., & Baxter, D. C. (2007b). Osmium in environmental samples from Northeast Sweden: Part I. Evaluation of background status. The Science of the Total Environment, 386, 145–158.CrossRefGoogle Scholar
  29. Rodushkin, I., Engström, E., Sörlin, D., Pontér, C., & Baxter, D. C. (2007c). Osmium in environmental samples from Northeast Sweden. Part II. Identification of anthropogenic sources. The Science of the Total Environment, 386, 159–168.CrossRefGoogle Scholar
  30. Sheppeard, H., & Ward, D. J. (1980). Intra-articular osmic acid in rheumatoid arthritis: five years’ experience. Rheumatology and Rehabilitation, 19, 25–29.CrossRefGoogle Scholar
  31. Singh, R., & Krishna, M. (2006). DNA damage induced nucleotide excision repair in Saccharomyces cerevisiae. Molecular and Cellular Biochemistry, 290(1), 103–112.CrossRefGoogle Scholar
  32. Sjörs, H. (1999). The background: Geology, climate and zonation. In H. Rydin, P. Snoeijs, & M. Diekmann (Eds.), Swedish plant geography (pp. 5–14). Uppsala: Svenska Växtgeografiska Sällskapet.Google Scholar
  33. Smith, I. C., Carson, B. L., & Ferguson, T. L. (1974). Osmium: an appraisal of environmental exposure. Environmental Health Perspectives, 8, 201–213.Google Scholar
  34. Smith, I. C., Carson, B. L., & Ferguson, T. L. (1977). Trace metals in the environment. Ann Arbor: Ann Arbor Science.Google Scholar
  35. Spiro, B., Weiss, D. J., Purvis, O. W., Mikhailova, I., Williamson, B. J., Coles, B. J., et al. (2004). Lead isotopes in lichen transplants around a Cu smelter in Russia determined by MC-ICP-MS reveal transient records of multiple sources. Environmental Science & Technology, 38, 6522–6528.CrossRefGoogle Scholar
  36. Thiéry, G., Bernier, J., & Bergeron, M. (1995). A simple technique for staining of cell membranes with imidazole and osmium tetroxide. The Journal of Histochemistry and Cytochemistry, 43, 1079–1084.CrossRefGoogle Scholar
  37. Viro, P. (1974). Age determination in the bank vole Clethrionomys glareolus Schreb. 1780, from the roots of the teeth. Aquilo Ser Zoologica, 15, 33–36.Google Scholar
  38. Viro, P., & Sulkava, S. (1985). Food of the bank vole in northern Finnish spruce forests. Acta Theriologica, 30, 259–266.Google Scholar
  39. Wijnhoven, S., Leuven, R. S. E. W., van der Velde, G., Jungheim, G., Koelemij, E. I., de Vries, F. T., et al. (2007). Heavy-metal concentrations in small mammals from a diffusely polluted floodplain: importance of species- and location-specific characteristics. Archives of Environmental Contamination and Toxicology, 52, 603–613.CrossRefGoogle Scholar
  40. Zar, J. H. (1996). Biostatistical analysis. London: Prentice-Hall, Inc.Google Scholar
  41. Zejda, J. A. N. (1961). Age structure in populations of the bank vole, Clethrionomys glareolus Schreber 1780. Zool Listy, 24, 249–264.Google Scholar
  42. Zejda, J. A. N. (1977). A device to determine the birth date of the bank vole, Clethrionomys glareolus by the length of M1 roots. Folia Zoologica, 26, 207–211.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Ilia Rodushkin
    • 1
    • 2
  • Emma Engström
    • 1
    • 2
  • Dieke Sörlin
    • 2
  • Douglas Baxter
    • 2
  • Birger Hörnfeldt
    • 3
  • Erik Nyholm
    • 4
  • Frauke Ecke
    • 1
    • 3
    • 5
  1. 1.Division of GeosciencesLuleå University of TechnologyLuleåSweden
  2. 2.ALS Scandinavia ABLuleåSweden
  3. 3.Department of Wildlife, Fish and Environmental StudiesSwedish University of Agricultural SciencesUmeåSweden
  4. 4.Department of Ecology and Environmental SciencesUmeå UniversityUmeåSweden
  5. 5.Department of Aquatic Sciences and AssessmentSwedish University of Agricultural SciencesUppsalaSweden

Personalised recommendations