Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bioaccumulation of Heavy Metals (Pb, Cd, Cr, Cu) in Fine Roots Under Three Species of Alders (Alnus spp.) Plantation at Different Soil Substrates Addition on the Reclaimed Combustion Wastes Landfill


In the study, we have analysed the impact of lead (Pb), cadmium (Cd), chromium (Cr) and copper (Cu) on fine root biomass and the associated level of bioacumulation heavy metals in fine roots under alder plantings (Alnus incana, A. glutinosa and A. viridis) growing on technosols developed from combustion wastes and extremely poor quaternary sands excavated by sand mining. The control sites were located in natural habitats in the Bieszczady Mountains within the natural range of the occurrence of the investigated alder species. Results showed that the bioaccumulation index of heavy metals in the alder roots depended on technosol properties, in particular, pH and texture, and, to a lesser extent, on the total content of heavy metals in soil. Additionally, it was found that in some concentration ranges, Pb and Cr had a stimulating effect on the growth of fine roots.

This is a preview of subscription content, log in to check access.

Fig. 1


  1. Adriano, D. C., Wenzel, W. W., Vangronsveld, J., & Bolan, N. S. (2004). Role of assisted natural remediationin environmental cleanup. Geoderma, 122, 121–142.

  2. Allen, H.E., Huang, C.P., Bailey, G.W., Bowers A.R. (1995). Metal speciation and contamination of soil. Boca Raton, Lewis Publishers

  3. Alvarenga, P., Palma, P., Gonçalves, A. P., Fernandes, R. M., De Varennes, A., & Vallini, G. (2000). Organic residues as immobilizing agents in aided phytostabilization: (II) effects on soil biochemical and cotoxicological characteristics. Chemosphere, 74, 1301–1308.

  4. Asokan, P., Saxena, M., Asolekar, S.R. (2005). Coal combustion residues—environmental implications and recycling potentials. Resources, Conservation and Recycling, 43, 239-262

  5. Bendtfeldt, E. S., Burger, J. A., & Daniels, W. L. (2001). Quality of amended mine soils after sixteen years. Soil Science Society of America Journal, 65, 1736–1744.

  6. Böhm, W. (1979). Methods of studying root systems. In Ecological Studies (Vol. 33). Berlin: Springer.

  7. Borken, W., Kossmann, G., & Matzner, E. (2007). Biomass, morphology and nutrient contents of fine roots in four Norway spruce stands. Plant and Soil, 292, 79–93.

  8. Brunner, I., Luster, J., Gunthardt-Goerg, M., & Frey, B. (2008). Heavy metal accumulation and phytostabilisation potential of tree fine roots in a contaminated soil. Environmental Pollution, 152, 559–568.

  9. Čermák, P. (2008). Forest reclamation of dumpsites of coal combustion by-products (CCB). Journal of Forest Science, 54, 273–280.

  10. Chen, H., Harmon, M. E., Sexton, J., & Fasth, B. (2002). Fine-root decomposition and N dynamics in coniferous forests of the Pacific Northwest, U.S.A. Journal of Forest Research, 32, 320–331.

  11. Chodak, M., & Niklińska, M. (2010). The effect of different tree species on the chemical and microbial properties of reclaimed mine soils. Biology and Fertility of Soils, 46, 555–566.

  12. Cole, D. W., Compton, J., Van Miegroet, H., & Homann, P. (1990). Changes in soil properties and site productivity caused by red alder. Water, Air, and Soil Pollution, 54, 231–246.

  13. Dang, Z., Liu, C., Haigh, M.J (2002). Mobility of heavy metals associated with the natural weathering of coal mine spoils. Environmental Pollution, 118, 419-426

  14. Dellantonio, A., Fitz, W., Repmann, F., Wenzel, W. (2010). Disposal of Coal Combustion Residues in Terrestrial Systems: Contamination and Risk Management. Journal of Environment Quality, 39, 761-775

  15. Domínguez, M., Madrid, F., Marańón, T., & Murillo, J. (2009). Cadmium availability in soil and retention in oak roots: potential for phytostabilization. Chemosphere, 76, 480–486.

  16. Haigh, M.J. (1992). Problems in the reclamation of coal-mine disturbed lands in Wales. International Journal of Surface Mining, Reclamation and Environment, 6, 31-37

  17. Haynes, R.J. (2009) Reclamation and revegetation of fly ash disposal sites – Challenges and research needs. Journal of Environmental Management. 90, 43-53

  18. Józefowska, A., Woś, B., & Pietrzykowski, M. (2016). Tree species and soil substrate effects on soil biota during early soil forming stages at afforested mine sites. Applied Soil Ecology, 102, 70–79.

  19. Jung, K., Duan, M., House, J., & Chang, S. (2014). Textural interfaces affected the distribution of roots, water, and nutrients in some reconstructed forest soils in the Athabasca oil sands region. Ecological Engineering, 64, 240–249.

  20. Juwarkar, A., Jambulkar, H., (2009). Assessment of bioaccumulation of heavy metals by different plant species grown on fly ash dump Ecotoxicology Environmental Safety, 72, 1122-1128

  21. Kabata-Pendias, A., & Pendias, H. (1992). Trace elements in soil and plants (2nd ed.). Boca raton: CRC Press.

  22. Kabata-Pendias, A., & Pendias, H. (1999). Biogeochemia pierwiastków śladowych. Warszawa: Wydawnictwo Naukowe PWN.

  23. Kahle, H. (1993). Response of roots of trees to heavy metals. Environmental and Experimental Botany, 33, 99–119.

  24. Knoche, D., Embacher, A., & Katzur, J. (2002). Water and element fluxes of red oak ecosystems during stand development on post-mining sites (Lusatian Lignite District). Water, Air, and Soil Pollution, 141, 219–231.

  25. Krzaklewski, W., Pietrzykowski, M., & Woś, B. (2012). Survival and growth of alders (Alnus glutinosa (L.) Gaertn. and Alnus incana (L.) Moench) on fly ash technosols at different substrate improvement. Ecological Engineering, 49, 35–40.

  26. Leitgib, L., Kálmán, J., & Gruiz, K. (2007). Comparison of bioassays by testing whole soil and their water extract from contaminated sites. Chemosphere, 66, 428–434.

  27. Lorenc-Plucińska, G., Walentynowicz, M., & Niewiadomska, A. (2013). Capabilities of alders (Alnus incana and A. glutinosa) to grow in metal-contaminated soil. Ecological Engineering, 58, 214–227.

  28. Markkola, A. M., Tarvainen, O., & Ahonen-Jonnarth, U. (2002). Urban polluted forest soils induce elevated root peroxidase activity in Scots pine (Pinus sylvestris L.) seedlings. Environmental Pollution, 116, 73–278.

  29. Massey, H.F., Barnhisel, R.I. (1972). Copper, nickel, and zinc released from acid coal mine spoil materials of eastern Kentucky. Soil Science, 113:3. 

  30. Naidu, R., Sumner, M. E., & Harter, R. D. (1998). Sorption of heavy metals in strongly weathered soils: an overview. Journal of Environmental Geochemistry and Health, 20, 5–9.

  31. Pietrzykowski, M.,  Krzaklewski, W. (2007). Soil organic matter, C and N accumulation during natural succession and reclamation in an opencast sand quarry (southern Poland). Archives of Agronomy and Soil Science, 53, 473-483

  32. Pietrzykowski, M., Socha, J., & Woś, B. (2010). Biomass and deformation of the Scots pine (Pinus sylvestris L.) root systems in reclaimed open-cast mining pit and dumping ground conditions. Sylwan, 154, 107–116.

  33. Pietrzykowski, M., Woś, B., & Haus, N. (2013). Scots pine needles macro-nutrient (N, P, K, Ca, Mg and S) supply at different reclaimed mine soil substrates - as an indicator of the stability of developed forest ecosystems. Environmental Monitoring and Assessment, 185, 7445–7457.

  34. Pietrzykowski, M., Socha, J., & van Doorn, N. S. (2014). Linking heavy metal bioavailability (Cd, Cu, Zn and Pb) in Scots pine needles to soil properties in reclaimed mine areas. Science of the Total Environment, 470, 501–510.

  35. Pietrzykowski, M., Gruba, P., & Sproull, G. (2017a). The effectiveness of Yellow lupine (Lupinus luteus L.) green manure cropping in sand mine cast reclamation. Ecological Engineering, 102, 72–79.

  36. Pietrzykowski, M., Woś, B., Pająk, M., & Likus-Cieślik, J. (2017b). Assessment of tree vitality, biomass and morphology of Scots pine (Pinus sylvestris L.) root systems growing on reclaimed landfill waste after zinc and lead flotation. Forest Research Papers, 78, 323–331.

  37. Rosenvald, K., Kuznetsova, T., Ostonen, I., Truu, M., Truu, J., Uri, V., & Lõhmus, K. (2011). Rhizosphere effect and fine-root morphological adaptations in a chronosequence of silver birch stands on reclaimed oil shale post-mining areas. Ecological Engineering, 37, 1027–1034.

  38. Singh, B. (1998). Contribution of forest fine roots in reclamation of semiarid sodic soils. Arid Soil Research and Rehabilitation, 12, 207–222.

  39. Soil Science Division Staff. (2017). Soil Science Division Staff. Soil survey manual. In C. Ditzler, K. Scheffe, & H. C. Monger (Eds.), USDA Handbook 18. Washington, D.C: Government Printing Office.

  40. Šourková, M., Frouz, J., & Santruckova, H. (2005). Accumulation of carbon, nitrogen and phosphorus during soil formation on alder spoil heaps after brown-coal mining, near Sokolov (Czech Republic). Geoderma, 124, 203–214.

  41. Sparks, D. L. (1995). Environmental soil chemistry. San Diego: Academic Press.

  42. Sroka, K., Chodak, M., Klimek, B., & Pietrzykowski, M. (2017). Effect of black alder (Alnus glutinosa) admixture to Scots pine (Pinus sylvestris) plantations on chemical and microbial properties of sandy mine soils. Applied Soil Ecology, 124, 62–68.

  43. Strawn, D. G., & Sparks, D. L. (2000). Effects of soil organic matter on the kinetics and mechanisms of Pb(II) sorption and desorption in soil. Soil Science Society of America Journal, 64, 144–156.

  44. Świątek, B., Woś, B., Chodak, M., Maiti, S. K., Józefowska, A., & Pietrzykowski, M. (2019a). Fine root biomass and the associated C and nutrient pool under the alder (Alnus spp.) plantings on reclaimed technosols. Geoderma, 337, 1021–1027.

  45. Świątek, B., Chodak, M., & Pietrzykowski, M. (2019b). Estimation of fine root biomass of alders growing on technosols using two different methods. Communications in Soil Science and Plant Analysis, 50, 474–481.

  46. Van Miegroet, H., & Cole, D. W. (1984). The impact of nitrification on soil acidification and cation leaching in a red alder ecosystem. Journal of Environmental Quality, 13, 586–590.

  47. Woś, B., & Pietrzykowski, M. (2015). Simulation of birch and pine litter influence on early stage of reclaimed soil formation process under controlled conditions. Journal of Environmental Quality, 44, 1091–1098.

Download references

Author information

Correspondence to Bartłomiej Świątek.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Świątek, B., Woś, B., Gruba, P. et al. Bioaccumulation of Heavy Metals (Pb, Cd, Cr, Cu) in Fine Roots Under Three Species of Alders (Alnus spp.) Plantation at Different Soil Substrates Addition on the Reclaimed Combustion Wastes Landfill. Water Air Soil Pollut 230, 297 (2019).

Download citation


  • Bioaccumulation index
  • Mine soils
  • Heavy metals
  • Lead
  • Cadmium