Water, Air, & Soil Pollution

, 229:371 | Cite as

Plant Accumulation of Natural Radionuclides as Affected by Substrate Contaminated with Uranium-Mill Tailings

  • Marko ČerneEmail author
  • Borut Smodiš
  • Marko Štrok
  • Radojko Jaćimović


Environmental concern due to plant accumulation of natural radionuclides is a major concern in uranium mining areas. To evaluate the risk associated with the transfer of radionuclides to edible plants, the uptake of 238U, 226Ra, and 210Pb by Chinese cabbage (Brassica rapa L. subsp. pekinensis (Lour.) Hanelt) grown in soils contaminated with uranium-mill tailings (UMT) was investigated. Test plants were grown under controlled conditions in substrate composed of soil and UMT in different ratios. Activity concentrations of 238U, 226Ra, and 210Pb in substrate, leaves, and roots were measured and the concentration ratios determined. Soil characteristics were determined, since they directly affect bioavailability of radionuclides. Concentration ratios of 238U, 226Ra, and 210Pb in leaves varied from 0.001 to 0.006, 0.024 to 0.172, and 0.004 to 0.011, respectively, and in roots from 0.020 to 0.126, 0.015 to 0.241, and 0.033 to 1.460, respectively. Concentrations of 238U, 226Ra, and 210Pb in leaves and roots were found to correlate with the amount of 238U, 226Ra, and 210Pb in the substrate. A higher amount of 226Ra accumulated in aboveground parts (57–877 Bq kg−1 d. m. for leaves) compared to 238U (0.6–4.7 Bq kg−1 d. m. for leaves) and 210Pb (8–53 Bq kg−1 d. m. for leaves), which were mainly stored in the roots. The relationships between the amount of radionuclides in plants and soil characteristics and their role in radionuclide uptake are discussed and critically evaluated.


Brassica plants Concentration ratio Natural radionuclides Plant accumulation Substrate Mine tailings 



The authors would like to thank the staff of the Rudnik Žirovski vrh company for their cooperation and assistance. The authors also thank Dr. David Heath for his help in reviewing the paper. The support of Dr. Vaupotič for the 222Rn measurements is highly appreciated. The Department of Environmental Sciences of the “Jožef Stefan Institute” is also acknowledged for the management, technical, and analytical support of the study.

Funding Information

The Slovenian Research Agency is acknowledged for its financial support (contract No. P2-0075).


  1. Benedik, L., Klemencic, H., Repinc, U., & Vreček, P. (2003). Uranium and its decay products in samples contaminated with uranium mine and mill wastes. Journal Physics, IV France, 107, 147–150.CrossRefGoogle Scholar
  2. Biasioli, M., Grčman, H., Kralj, T., Madrid, F., Díaz-Barrientos, E., & Ajmone-Marsan, F. (2007). Potentially toxic elements contamination in urban soils: a comparison of three European cities. Journal of Environmental Quality, 36, 70–79.CrossRefGoogle Scholar
  3. Carvalho, F. P., Oliveira, J. M., Neves, M. O., Abreu, M. M., & Vicente, E. M. (2009). Soil to plant (Solanum tuberosum L.) radionuclide transfer in the vicinity of an old uranium mine. Geochemistry: Exploration, Environment Analysis, A, 9, 275–278.Google Scholar
  4. Černe, M., Smodiš, B., Štrok, M., & Jaćimović, R. (2010). Accumulation of 238U, 226Ra and 230Th by wetland plants in a vicinity of U-mill tailings at Žirovski vrh (Slovenia). Journal of Radioanalytical and Nuclear Chemistry, 286, 323–327.CrossRefGoogle Scholar
  5. Černe, M., Smodiš, B., & Štrok, M. (2011). Uptake of radionuclides by a common reed (Phragmites australis (Cav.) Trin. ex Steud.) grown in the vicinity of the former uranium mine at Žirovski vrh. Nuclear Engineering and Design, 241, 1282–1286.CrossRefGoogle Scholar
  6. Chang, P., Kim, K. W., Yoshida, S., & Kim, S. Y. (2005). Uranium accumulation of crop plants enhanced by citric acid. Environmental Geochemistry and Health, 27, 529–538.CrossRefGoogle Scholar
  7. Chang, Y.-T., Hseu, Z.-Y., & Zehetner, F. (2014). Evaluation of phytoavailability of heavy metals to Chinese cabbage (Brassica chinensis L.) in rural soils. The Scientific World Journal. Scholar
  8. Chen, S. B., Zhu, Y. G., & Hu, Q. H. (2005). Soil to plant transfer of 238U, 226Ra and 232Th on a uranium mining-impacted soil from southeastern China. Journal of Environmental Radioactivity, 82, 223–236.CrossRefGoogle Scholar
  9. Choi, M. S., Lin, X. J., Lee, S. A., Kim, W., Kang, H. D., Doh, S. H., Kim, D. S., & Lee, D. M. (2008). Daily intakes of naturally occurring radioisotopes in typical Korean foods. Journal of Environmental Radioactivity, 99, 1319–1323.CrossRefGoogle Scholar
  10. Cochran, W. G., & Cox, G. M. (1992). Experimental designs, second edition. New York: Wiley.Google Scholar
  11. Currie, L. A. (1968). Limits for qualitative detection and quantitative determination. Analytical Chemistry, 40, 586–593.CrossRefGoogle Scholar
  12. Duquène, L., Vandenhove, H., Tack, F., Meers, E., Baeten, J., & Wannijn, J. (2009). Enhanced phytoextraction of uranium and selected heavy metals by Indian mustard and ryegrass using biodegradable soil amendments. Science of the Total Environment, 407, 1496–1505.CrossRefGoogle Scholar
  13. Ebbs, S. D., Brady, D. J., & Kochian, L. V. (1998). Role of uranium speciation in the uptake and translocation of uranium by plants. Journal of Experimental Botany, 49, 1183–1190.CrossRefGoogle Scholar
  14. Ehlken, S., & Kirchner, G. (2002). Environmental processes affecting plant root uptake of radioactive trace elements and variability of transfer factor data: a review. Journal of Environmental Radioactivity, 58, 97–112.CrossRefGoogle Scholar
  15. Ekdal, E., Karali, T., & Sac, M. M. (2006). 210Po and 210Pb in soils and vegetables in Kucuk Menderes basin of Turkey. Radiation Measurements, 41, 72–77.CrossRefGoogle Scholar
  16. Gerzabek, M. H., Strebl, F., & Temmel, B. (1998). Plant uptake of radionuclides in lysimeter experiments. Environmental Pollution, 99, 93–103.CrossRefGoogle Scholar
  17. Gramss, G., Voigt, K.-D., & Bergmann, H. (2004). Plant availability and leaching of (heavy) metals from ammonium-, calcium-, carbohydrate-, and citric acid-treated uranium-mine-dump soil. Journal of Plant Nutrition and Soil Science, 167, 417–427.CrossRefGoogle Scholar
  18. Gregorič, A. (2013). Radon as a tool in geophysical research. PhD thesis, Jožef Stefan International Postgraduate School, Ljubljana, Slovenia.Google Scholar
  19. Hegazy, A. K., Afifi, S. Y., Alatar, A. A., Alwathnani, H. A., & Emam, M. H. (2013). Soil characteristics influence the radionuclide uptake of different plant species. Chemistry and Ecology, 29(3), 255–269.CrossRefGoogle Scholar
  20. Huang, J. W., Blaylock, M. J., Kapulnik, Y., & Ensley, B. D. (1998). Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. Environmental Science and Technology, 32(13), 2004–2008.CrossRefGoogle Scholar
  21. International Atomic Energy Agency-IAEA (2016). Criteria for radionuclide activity concentrations for food and drinking water, IAEA-TECDOC-1788.Google Scholar
  22. Jaćimović, R. (2003). Evaluation of the use of the TRIGA Mark II reactor for the k0-method of activation analysis (in-Slovene), PhD Thesis, University of Ljubljana.Google Scholar
  23. Jaćimović, R., Smodiš, B., Bučar, T., & Stegnar, P. (2003). k0-NAA quality assessment by analysis of different certified reference materials using the KAYZERO/SOLCOI software. Journal of Radioanalytical and Nuclear Chemistry, 257, 659–663.CrossRefGoogle Scholar
  24. Kobal, I., Vaupotič, J., Dujmović, P., Kotnik, J., Gobec, S., & Zorko, B. (2005). Outdoor radon in Slovenia. In: IJS-DP 9270, Jožef Stefan Institute, Ljubljana [in Slovene].Google Scholar
  25. Križman, M., Byrne, A. R., & Benedik, L. (1995). Distribution of 230Th in milling wastes from the Žirovski vrh uranium mine (Slovenia) and its radioecological implications. Journal of Environmental Radioactivity, 26, 223–235.CrossRefGoogle Scholar
  26. Laurette, J., Larue, C., Mariet, C., Brisset, F., Khodja, H., Bourguignon, J., & Carrière, M. (2012). Influence of uranium speciation on its accumulation and translocation in three plant species: Oilseed rape, sunflower and wheat. Environmental and Experimental Botany, 77, 96–107.CrossRefGoogle Scholar
  27. Lauria, D. C., Ribeiro, F. C. A., Conti, C. C., & Loureiro, F. A. (2009). Radium and uranium levels in vegetables grown using different farming management systems. Journal of Environmental Radioactivity, 100, 176–183.CrossRefGoogle Scholar
  28. Liu, W., Zhou, Q., An, J., Sun, Y., & Liu, R. (2010). Variations in cadmium accumulation among Chinese cabbage cultivars and screening for Cd-safe cultivars. Journal of Hazardous Materials, 173, 737–743.CrossRefGoogle Scholar
  29. Madruga, M. J., Brogueira, A., Alberto, G., & Cardoso, F. (2001). 226Ra bioavailability to plants at the Uregiriça uranium mill tailings site. Journal of Environmental Radioactivity, 54, 175–188.CrossRefGoogle Scholar
  30. Marschner, H. (1995). Mineral Nutrition of Higher Plants, 2nd edition, Academic Press, London.CrossRefGoogle Scholar
  31. Nathwani, J. S., & Phillips, C. R. (1979). Adsorption of Ra-226 by soils (I). Chemosphere, 5, 285–291.CrossRefGoogle Scholar
  32. Persson, B. R. R., & Holm, E. (2011). Polonium-210 and lead-210 in the terrestrial environment: a historical review. Journal of Environmental Radioactivity, 102, 420–429.CrossRefGoogle Scholar
  33. Petrescu, L., & Bilal, E. (2003). Plant availability of uranium in contaminated soil from Crucea mine (Romania). Environmental Geosciences, 10(3), 123–135.CrossRefGoogle Scholar
  34. Petrova, R. (2006). Accumulation of natural radionuclides in wooden and grass vegetation from abandoned uranium mines. Opportunities for phytoremediation. In B. J. Merkel & A. Hasche-Berger (Eds.), Uranium in the environment (pp. 507–518). Berlin: Springer-Verlag.CrossRefGoogle Scholar
  35. Pietrzak-Flis, Z., & Skowrońska-Smolak, M. (1995). Transfer of 210Pb and 210Po to plants via root system and above-ground interception. Science of the Total Environment, 162, 139–147.CrossRefGoogle Scholar
  36. Popa, K., Tykva, R., Podracká, E., & Humelnicu, D. (2008). 226Ra translocation from soil to selected vegetation in the Crucea (Romania) uranium mining area. Journal of Radioanalytical and Nuclear Chemistry, 278, 211–213.CrossRefGoogle Scholar
  37. R Development Core Team. (2010). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  38. Ramaswami, A., Carr, P., & Burkhardt, M. (2001). Plant-uptake of uranium: hydroponic and soil system studies. International Journal of Phytoremediation, 3, 189–201.CrossRefGoogle Scholar
  39. Rodríguez, P. B., Tomé, F. V., & Lozano, J. C. (2002). About the assumption of linearity in soil-to-plant transfer factors for uranium and thorium isotopes and 226Ra. The Science of the Total Environment, 284, 167–175.CrossRefGoogle Scholar
  40. Rufyikiri, G., Wannijn, J., Wang, L., & Thiry, Y. (2006). Effects of phosphorus fertilization on the availability and uptake of uranium and nutrients by plants grown on soil derived from uranium mining debris. Environmental Pollution, 141, 420–427.CrossRefGoogle Scholar
  41. Shahandeh, H., & Hossner, L. R. (2002). Role of soil properties in phytoaccumulation of uranium. Water, Air & Soil Pollution, 141, 165–180.CrossRefGoogle Scholar
  42. Shahid, M., Pinelli, E., & Dumat, C. (2012). Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. Journal of Hazardous Materials, 219–220, 1–12.CrossRefGoogle Scholar
  43. Simon, S. L., & Ibrahim, S. A. (1990). Biological uptake of radium by terrestrial plants. In The environmental behavior of radium: technical report series, no. 310. 545–599 (IAEA, 1990).Google Scholar
  44. Soudek, P., Valenová, Š., Benešová, D., & Vanĕk, T. (2007). From laboratory experiments to large scale application-an example of phytoremediation of radionuclides. In N. Marmiroli (Ed.), Advanced science and technology for biological decontamination of sites affected by chemical and radiological nuclear agents (pp. 139–158). New York: Springer.CrossRefGoogle Scholar
  45. Soudek, P., Petrová, Š., Benešová, D., Kotyza, J., Vágner, M., Vaňkova, R., & Vanĕk, T. (2010). Study of soil-plant transfer of 226Ra under greenhouse conditions. Journal of Environmental Radioactivity, 101, 446–450.CrossRefGoogle Scholar
  46. Stegnar, P., Shishkov, I., Burkitbayev, M., Tolongutov, B., Yunsov, M., Radyuk, R., & Salbu, B. (2012). Assessment of the radiological impact of gamma and radon dose rates at former U mining sites in Central Asia. Journal of Environmental Radioactivity, 123, 3–13.CrossRefGoogle Scholar
  47. Stojanović, M. D., Mihajlović, M. L., Milojković, J. V., Lopičić, Z. R., Adamović, M., & Stanković, S. (2012). Efficient phytoremediation of uranium mine tailings by tobacco. Environmental Chemistry Letters, 10, 377–381.CrossRefGoogle Scholar
  48. Štrok, M., & Smodiš, B. (2010). Fractionation of natural radionuclides in soils from the vicinity of a former uranium mine Žirovski vrh, Slovenia. Journal of Environmental Radioactivity, 101, 22–28.CrossRefGoogle Scholar
  49. Štrok, M., & Smodiš, B. (2013). Soil-to-plant transfer factors for natural radionuclides in grass in the vicinity of a former uranium mine. Nuclear Engineering and Design, 261, 279–284.CrossRefGoogle Scholar
  50. Štrok, M., Smodiš, B., & Petrinec, B. (2010). Natural radionuclides in sediments and rocks from Adriatic Sea. Journal of Radioanalytical and Nuclear Chemistry, 286, 303–308.CrossRefGoogle Scholar
  51. Štrok, M., Smodiš, B., & Eler, K. (2011). Natural radionuclides in trees grown on a uranium mill tailings waste pile. Environmental Science and Pollution Research, 18, 819–826.CrossRefGoogle Scholar
  52. Tykva, R., & Podracká, E. (2005). Bioaccumulation of 226Ra in the plants growing near uranium facilities. Nukleonika, 50, S25–S27.Google Scholar
  53. Tyler, G., & Olsson, T. (2001). Plant uptake of major and minor mineral elements as influenced by soil acidity and liming. Plant and Soil, 230, 307–321.CrossRefGoogle Scholar
  54. Vaaramaa, K., Solatie, D., & Aro, L. (2009). Distribution of 210Pb and 210Po concentrations in wild berries and mushrooms in boreal forest ecosystems. Science of the Total Environment, 408, 84–91.CrossRefGoogle Scholar
  55. Vamerali, T., Bandiera, M., & Mosca, G. (2010). Field crops for phytoremediation of metal-contaminated land. A review. Environmental Chemistry Letters, 8, 1–17.CrossRefGoogle Scholar
  56. Vandenhove, H., & Van Hees, M. (2007). Predicting radium availability and uptake from soil properties. Chemosphere, 69, 664–674.CrossRefGoogle Scholar
  57. Vandenhove, H., Sweeck, L., Mallants, D., Vanmarcke, H., Aitkulov, A., Sadyrov, O., Savosin, M., Tolongutov, B., Mirzachev, M., Clerc, J. J., Quarch, H., & Aitaliev, A. (2006). Assessment of radiation exposure in the uranium mining and milling area of Mailuu Suu, Kyrgyzstan. Journal of Environmental Radioactivity, 88, 118–139.CrossRefGoogle Scholar
  58. Vandenhove, H., Van Hees, M., Wannijn, J., Wouters, K., & Wang, L. (2007). Can we predict uranium bioavailability based on soil parameters? Part 2: soil solution uranium concentration is not a good bioavailability index. Environmental Pollution, 145, 577–586.CrossRefGoogle Scholar
  59. Vodnik, D., Grčman, H., Maček, I., van Elteren, J. T., & Kovačevič, M. (2008). The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Science of the Total Environment, 392, 130–136.CrossRefGoogle Scholar
  60. Vreček, P., & Benedik, L. (2002). Determination of 210Pb and 210Po in sediments, water, and plants in an area contaminated with mine waste. Mine, Water and the Environment, 21, 156–159.CrossRefGoogle Scholar
  61. Vreček, P., Benedik, L., & Pihlar, B. (2004). Determination of 210Pb and 210Po in sediment and soil leachates and in biological materials using a Sr-resin column and evaluation of column reuse. Applied Radiation and Isotopes, 60, 717–723.CrossRefGoogle Scholar
  62. Zhu, Y.-G., & Smolders, E. (2000). Plant uptake of radiocaesium: a review of mechanisms, regulation and application. Journal of Experimental Botany, 51(351), 1635–1645.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institute of Agriculture and TourismPorečCroatia
  2. 2.Jožef Stefan InstituteLjubljanaSlovenia
  3. 3.Jožef Stefan International Postgraduate SchoolLjubljanaSlovenia

Personalised recommendations