Skip to main content

Accumulation of heavy metals in stemwood of forest tree plantations fertilized with different sewage sludge doses


The levels of heavy metals that accumulated in stemwood of mature trees grown for 20 years in a plantation in an abandoned peat quarry in areas that were fertilized with different amounts of domestic sewage sludge (180, 360, and 720 Mg ha−1 on a dry basis) were compared with trees grown in a reference nonfertilized area. Included in the study was a hybrid poplar (Populus tremula × Populus tremuloides) developed for use as an energy crop, three local tree species and one introduced tree species. The concentrations of Cd, Cr, Cu, Ni, Pb and Zn in the stemwood of the trees grown in the fertilized and nonfertilized fields were determined, and found to be significantly lower than their respective concentrations in the soil. Cd and Cr were found only in several wood samples at concentrations close to the limits of detection or qualification; therefore, they were not analyzed further. A correlation analysis suggested that 75% of the correlations between the concentrations of heavy metals in the stemwood and the concentrations in the soil were negative. The ability of trees to accumulate the metals from soil in most cases decreased for Cu and Ni; however, the correlations were not as clear for Pb and Zn. The following sequence for the levels of heavy metals found in the stemwood of the analysed trees was Zn > Pb > Ni > Cu > (Cr, Cd). The results of this study showed that the levels of heavy metals in the studied wood would not exceed the permitted limits of heavy metal pollution in the air and ash when used for energy production.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8


  • Berra M, Dell‘orso M, Mangialardi T, Polini AE, Piga L. (2010). Chemical and environmental characterization of fly ash from woody biomass combustion. Proceedings Venice, Third International Symposium on Energy from Biomass and Waste. Venice, Italy 8-11

  • Bramryd T (2013) Long-term effects of sewage sludge application on the heavy metal concentrations in acid pine (Pinus sylvestris L.) forests in a climatic gradient in Sweden. For Ecol Manage 289:434–444

    Article  Google Scholar 

  • Brunner I, Luster J, Madeleine S, Günthardt-Goerg FB (2008) Heavy metal accumulation and phytostabilisation potential of tree fine roots in a contaminated soil. Environ Pollut 152:559–568

    CAS  Article  PubMed  Google Scholar 

  • Chandra R, Cho W, Kang H. (2016). Phytoextraction potential of four poplar hybrids under greenhouse conditions. Forest Science and Technology, 1–8 (Published online: 03 Aug 2016)

  • Chang FC, Ko CH, Tsai MJ, Wang YN, Chung CY (2014) Phytoremediation of heavy metal contaminated soil by Jatropha curcas. Ecotoxicology 23:1969–1978

    CAS  Article  PubMed  Google Scholar 

  • Dickinson NM, Turner AP, Watmough SA, Lepp NW (1992) Acclimation of trees to pollution stress: cellular metal tolerance traits. Ann Bot 70:569–572

    CAS  Article  Google Scholar 

  • Dimitriou I, Eriksson J, Adler A, Aronsson P, Verwijst T (2006) Fate of heavy metals after application of sewage sludge and wood-ash mixtures to short-rotation willow coppice. Environ Pollut 142:160–169

    CAS  Article  PubMed  Google Scholar 

  • Evangelou Michael WH, Conesa HM, Robinson BH, Schulin R (2012) Biomass Production on Trace Element-Contaminated Land: a Review. Environ Eng Sci 29:9

    Google Scholar 

  • Gradeckas A, Kubertavičienė L, Gradeckas A (1998) Utilization of wastewater sludge as a fertilizer in short rotation forests on cut away peatlands. Baltic Forestry 2:7–13

    Google Scholar 

  • Hazrat A, Ezzat K, Muhammad AS (2013) Phytoremediation of heavy metals—Concepts and applications. Chemosphere 91:869–881

    Article  Google Scholar 

  • Hossain MA, Pukclai Piyatida, Jaime A. Teixeira da Silva, Fujita M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of botany, 37

  • Labrecque M, Train I, Teodorescu S, Daigle S (1995) Effect of wastewater sludge on growth and heavy metal bioaccumulation of two Salix species. Plant Soil 171:303–316

    CAS  Article  Google Scholar 

  • Laureysens I, Blust R, De Temmerman L, Lemmens C, Ceulemans R (2004) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture: I. Seas Var leaf wood bark Conc Environ Pollution 131:485–494

    CAS  Google Scholar 

  • Lettens S, Vandecasteele B, DeVos B, Vansteenkiste D, Verschelde P (2011) Intra- and inter annual variation of Cd, Zn, Mn and Cu in foliage of poplars on contaminated soil. Sci Total Environ 409:2306–2316

    CAS  Article  PubMed  Google Scholar 

  • Lorenc-Plucinska G, Walentynowicz M, Niewiadomska A (2013) Capabilities of alders (Alnus incana and A. glutinosa) to grow in metal-contaminated soil. Ecol Eng 58:214

    Article  Google Scholar 

  • Maciejewska A, Veringa H, Sanders J, Peteves SD. (2006). Co-firing of biomass with coal: constraints and role of biomass pre-treatment. European Communities, 2006. EUR–Scientific and Technical Research Series ISSN 1018-5593

  • McLaughlin MJ (2001) Bioavailability of metals to terrestrial plants. Geoderma 122:143–149

    Google Scholar 

  • Moffat AJ, Armstrong AT, Ockleston J (2001) The optimization of sewage sludge and efluent disposal on energy crops of short rotation hybrid poplar. Biomass Bioenerg 20:161–169

    CAS  Article  Google Scholar 

  • Orlandi M, Pelfini M, Pavan M, Santilli M, Colombini MP (2002) Heavy metals variations in some conifers in Valle d’Aosta (Western Italian Alps) from 1930 to 2000. Microchem J 73:237–244

    CAS  Article  Google Scholar 

  • Perez-Esteban J, Escolastico C, Moliner A, Masaguer A (2013) Chemical speciation and mobilization of copper and zinc in naturally contaminated mine soils with citric and tartaric acids. Chemosphere 90:276–283

    CAS  Article  PubMed  Google Scholar 

  • Pesonen J, Kuokkanen T, Kaipiainen E, Koskela J, Jerkku I, Pappinen A, Villa A (2014) Chemical and physical properties of short rotation tree species. Eur J Wood Products 72:769–777

    CAS  Article  Google Scholar 

  • Pinto E, Aguiar AARM, Ferreira IM (2014) Influence of Soil Chemistry and Plant Physiology in the Phytoremediation of Cu, Mn, and Zn. Crit Rev Plant Sci 33:351–373

    CAS  Article  Google Scholar 

  • Planquart P, Bonin G, Prone A, Massiani C (1999) Distribution, movement and plant availability of trace metals in soils amended with sewage sludge composts: application to low metal loadings. Sci Total Environ 241:161–179

    CAS  Article  Google Scholar 

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal contaminated land by trees–a review. Environ Int 29:529–540

    CAS  Article  PubMed  Google Scholar 

  • Pulford ID, Riddell-Black D, Stewart C (2002) Heavy metal uptake by willow clones from sewage sludge-treated soil: the potential for phytoremediation. Int J Phytorem 4:59–72

    CAS  Article  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    CAS  Article  PubMed  Google Scholar 

  • Reimann C, Arnoldussen A, Finne TE, Nordgulen FKU, Englmaier P (2007) Element contents in mountain birch leaves, bark and wood under different anthropogenic and geogenic conditions. Appl Geochem 22:1549–1566

    CAS  Article  Google Scholar 

  • Salt CA, Hipkin JA, Davidson B. (1996). Phytoremediation — a feasible option at Lanarkshire Steelworks? Proceedings of a discussion meeting, Glasgow, Glimmerveen, I. Institute of chartered foresters, Edingburg, 51

  • Smilde KW (1981) Heavy-metal accumulation in crops grown on sewage sludge amended with metal salts. Plant Soil 62:3–14

    CAS  Article  Google Scholar 

  • Turner AP. (1994). The responses of plants to heavy metals. In: Ross SM. Toxic metals in soil—plant systems. Chichester: Wiley, pp. 153–87

  • Turner AP, Dickinson NM (1993) Survival of Acer pseudoplatanus L. (sycamore) seedlings on metalliferous soils. New Phytology 12:509–521

    Article  Google Scholar 

  • Unterbrunner R, Puschenreiter M, Sommer P, Wieshammer G, Tlustos P, Zupan M, Wenzel WW (2007) Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environ Pollut 148:107–114

    CAS  Article  PubMed  Google Scholar 

  • Wang C, Yang ZF, Yuan XY, Browne P, Chen LX, Ji JF (2013) The influences of soil properties on Cu and Zn availability in soil and their transfer to wheat (Triticum aestivum L.) in the Yangtze River delta region China. Geoderma 193:131–139

    Article  Google Scholar 

  • Watson C. (2002). The phytoremediation potential of Salix: studies of the interaction of heavy metals and willows. PhD thesis, University of Glasgow

  • Wilson B, Pyatt FB (2007) Heavy metal bioaccumulation by the important food plant, Olea europaea L., in an ancient metalliferous polluted area of Cyprus. Bull Environ Contam Toxicol 78:390–394

    CAS  Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations


Corresponding author

Correspondence to Marius Praspaliauskas.

Additional information

The online version is available at

Corresponding editor: Chai Ruihai.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Praspaliauskas, M., Pedisius, N. & Gradeckas, A. Accumulation of heavy metals in stemwood of forest tree plantations fertilized with different sewage sludge doses. J. For. Res. 29, 347–361 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Forest tree plantation
  • Accumulation factor
  • Saturation limit
  • Biosolids
  • Heavy metals
  • Long-term field experiments
  • Biofuels