Potential of urban trees for mitigating heavy metal pollution in the city of Novi Sad, Serbia

  • Amela Greksa
  • Branka Ljevnaić-Mašić
  • Jasna GrabićEmail author
  • Pavel Benka
  • Vasa Radonić
  • Boško Blagojević
  • Mirjana Sekulić


The current study analyzed heavy metal (HM) concentrations in the urban soil and tree leaves in the city of Novi Sad, Serbia, with the aim to identify specific tree species with good HM bioaccumulative abilities that can mitigate HM pollution in urban areas. Zinc (Zn), copper (Cu) and lead (Pb) were selected for the analysis of tree leaves and soil at 16 locations close to urban roads, main boulevards and high-traffic streets. Leaf material of four most common tree species: Platanus × acerifolia (Aiton) Willd., Celtis occidentalis L., Tilia argentea L. and Quercus robur L. and soil samples were analyzed with the aim to identify the potential hotspots and sources of pollution. Analysis of variance (ANOVA) and t test was applied to the available data sets to find differences between the HM concentrations in the analyzed trees and soil samples. Geographic information system (GIS) mapping was used for visualization of the concentration distributions and illustration of the HM contaminated hotspots. Bioconcentration factors (BCF) were calculated and they showed that the plants of the species Celtis occidentalis L. have the ability to retain Cu, the species Quercus robur L. retains mostly Zn, Tilia argentea L. accumulates Pb, while Platanus x acerifolia (Aiton) Willd. retains the smallest amount of the tested HMs.


Heavy metals Urban pollution Bioconcentration factor Copper Zinc Lead 



This paper was realized as a part of the project: Contribution of Urban Greenery in Mitigation of Climate Changes and Pollution (No 142-451-2695/2017-01/02) and financed by the Provincial Secretariat for Higher Education and Scientific Research of the Autonomous Province of Vojvodina, Serbia.


  1. Aksoy, A., & Öztürk, M. (1996). Phoenix dactylifera L. as a biomonitor of heavy metal pollution in Turkey. Journal of Trace and Microprobe Techniques, 14(3), 605–614.Google Scholar
  2. Alahabadi, A., Ehrampoush, M. H., Miri, M., Aval, H. E., Yousefzadeh, S., Ghaffari, H. R., et al. (2017). A comparative study on capability of different tree species in accumulating heavy metals from soil and ambient air. Chemosphere, 172, 459–467. Scholar
  3. Allaway, W. H. (1968). Agronomic controls over the environmental cycling of trace elements. In A. G. Norman (Ed.), Advances in Agronomy, vol. 20 (pp. 235–274). New York: Academic Press.Google Scholar
  4. Çelik, A., Kartal, A. A., Akdoğan, A., & Kaska, Y. (2005). Determining the heavy metal pollution in Denizli (Turkey) by using Robinio pseudo-acacia L. Environment international, 31(1), 105–112. Scholar
  5. De Smith, M., Goodchild, M., & Longley, P. (2018). Geospatial Analysis - a comprehensive guide to principles, techniques and software tools. 6th ed. Accessed 25 July 2019.
  6. Flanagan, J. T., Wade, K. J., Currie, A., & Curtis, D. J. (1980). The deposition of lead and zinc from traffic pollution on two roadside shrubs. Environmental Pollution, 1, 17–22.Google Scholar
  7. Flora of North America Editorial Committee, eds. 1993+. Flora of North America North of Mexico. 20+ vols. New York and Oxford.Google Scholar
  8. Gilman, E. F. (1990). Tree root growth and development. I. form, spread, depth and periodicity. Journal of Environmental Horticulture, 8(4), 215–220.Google Scholar
  9. Hu, Y., Wang, D., Wei, L., Zhang, X., & Song, B. (2014). Bioaccumulation of heavy metals in plant leaves from Yan′an city of the Loess Plateau. China. Ecotoxicology and environmental safety., 110, 82–88. Scholar
  10. Imperato, M., Adamo, P., Naimo, D., Arienzo, M., Stanzione, D., & Violante, P. (2003). Spatial distribution of heavy metals in urban soils of Naples city (Italy). Environmental pollution, 124(2), 247–256. Scholar
  11. ISO 11466:1995, Soil quality - extraction of trace elements soluble in aqua regia, International Organization for Standardization, Genève, Switzerland.Google Scholar
  12. Kalra, Y. (1998). Handbook of reference methods for plant analysis. Boca Raton: CRC Press.Google Scholar
  13. Latif, A., Bilal, M., Asghar, W., Azeem, M., Ahmad, M. I., Abbas, A., et al. (2018). Heavy metal accumulation in vegetables and assessment of their potential health risk. Journal of Environmental Analytical Chemistry, 5(1), 234. Scholar
  14. Law on Air Protection, Official Gazette Republic of Serbia, No. 36/2009, and 10/2013. (n.d.) Accessed 20 of June 2019.
  15. Liang, J., Fang, H. L., Zhang, T. L., Wang, X. X., & Liu, Y. D. (2017). Heavy metal in leaves of twelve plant species from seven different areas in Shanghai, China. Urban Forestry & Urban Greening, 27(2017), 390–398. Scholar
  16. Louhar, G., Yadav, R., Malik, R. S., & Yadav, S. (2019). Depth wise distribution of heavy metals in different soil series of Northwestern India. International Journal of Current Microbiology and Applied Sciences, 8(2), 2817–2826. Scholar
  17. Marjanović, M. D., Vukčević, M. M., Antonović, D. G., Dimitrijević, S. I., Jovanović, Đ. M., et al. (2009). Heavy metals concentration in soils from parks and green areas in Belgrade. Journal of the Serbian Chemical Society., 74(6), 697–706.CrossRefGoogle Scholar
  18. Mihailović, A., Vučinić, M., Vasić, J., Ninkov, S., Erić, N., Ralević, M., et al. (2014). Multivariate analysis of the contents of metals in urban snow near traffic lanes in Novi Sad, Serbia. Journal of the Serbian Chemical Society, 79(2), 265–276. Scholar
  19. Mihailović, A., Budinski-Petković, L., Popov, S., Ninkov, J., Vasin, J., Ralević, N. M., & Vučinić Vasić, M. (2015). Spatial distribution of metals in urban soil of Novi Sad, Serbia: GIS based approach. Journal of Geochemical Exploration, 150, 104–114. Scholar
  20. Monfared, S. H., Matinizadeh, M., Shirvany, A., Amiri, G. Z., Fard, R. M., & Rostami, F. (2013). Accumulation of heavy metal in Platanus orientalis, Robinia pseudoacacia and Fraxinus rotundifolia. Journal of forestry research, 24(2), 391–395. Scholar
  21. Morgenroth, J. (2011). Root growth response of Platanus orientalis to porous pavements. Arboriculture & Urban Forestry, 37(2), 45–50.Google Scholar
  22. Mrkajic, V., Stamenkovic, M., Males, M., Vukelic, D., & Hodolic, J. (2010). Proposal for reducing problems of the air pollution and noise in the urban environment. Carpathian Journal of Earth and Environmental Sciences, 5(1), 49–56.Google Scholar
  23. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters, 8(3), 199–216. Scholar
  24. Official Gazette of the Republic of Serbia, RS No. 88/2010. Regulation оn the programme of systematic monitoring of soil quality via indicators for assessment of soil degradation risk and methodology for creation of remediation programmes. _kvaliteta_zemljista.pdf. Accessed 25 July 2019.
  25. Padmavathiamma, P. K., & Li, L. Y. (2007). Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollution, 184, 105–126. Scholar
  26. Pajević, S., Borišev, M., Nikolić, N., Arsenov, D. D., Orlović, S., & Župunski, M. (2016). Phytoextraction of heavy metals by fast-growing trees: a review. In A. Ansari, S. Gill, R. Gill, G. Lanza, & L. Newman (Eds.), Phytoremediation. Cham: Springer.Google Scholar
  27. Pavlović, L., Nešić, L., Belić, M., Manojlović, M., Ćirić, V., Tunguz, V., et al. (2015). The content of heavy metals in the Boulevard soil in Novi Sad, Serbia. Sixth International Scientific Agricultural Symposium “Agrosym 2015”, Jahorina, Bosnia and Herzegovina, October 15-18th, Book of Proceedings, pp.1413-1418, ref.16. Accessed 25 July 2019.
  28. Prasad, M. N. V. (Ed.). (2004). Heavy metal stress in plants: from biomolecules to ecosystems. Berlin: Springer.Google Scholar
  29. Rademacher, P. (2001). Atmospheric heavy metals and forest ecosystems. Federal Research Centre for Forestry and Forest Products (BFH), CLRTAP. Accessed 25 July 2019.
  30. Ratul, A. K., Hassan, M., Uddin, M. K., Sultana, M. S., Akbor, M. A., & Ahsan, M. A. (2018). Potential health risk of heavy metals accumulation in vegetables irrigated with polluted river water. International Food Research Journal, 25(1), 329–338.Google Scholar
  31. Rehman, K., Fatima, F., Waheed, I., & Akash, M. S. H. (2018). Prevalence of exposure of heavy metals and their impact on health consequences. Journal of Cell Biochemistry, 119(1), 157–184. Scholar
  32. Roncevic, N., Siriski, J., Darmati, D., Dordevic, M., Kristoforovic-Ilic, M., Vajagic, L., Vojinovic-Miloradov, M., & Pakov, S. (1995). Exposure of the population of Novi Sad and the surrounding areas to lead. In U. Förstner, W. Salomons, & P. Mader (Eds.), Heavy Metals. Environmental Science. (pp. 373–376). Berlin: Springer.CrossRefGoogle Scholar
  33. Rosa, D. D., Tres, G., Broti-Rissato, B., Lorenzetti, E., Francisco Guimarães, V., & Feiden, A. (2018). Rooting platanus (Platanus acerifolia (Aiton) Willd.) cuttings in Marechal Cândido Rondon - PR, Brazil: influence of lesions at cutting bases and depth of planting. Acta Agronómica, 67(1), 109–113. Scholar
  34. Sawidis, T., Breuste, J., Mitrovic, M., Pavlovic, P., & Tsigaridas, K. (2011). Trees as bioindicator of heavy metal pollution in three European cities. Environmental Pollution, 159(12), 3560–3570. Scholar
  35. Sawidis, T., Krystallidis, P., Veros, D., & Chettri, M. (2012). A study of air pollution with heavy metals in Athens city and Attica basin using evergreen trees as biological indicators. Biological trace element research, 148(3), 396–408. Scholar
  36. SEPA – Serbian Agency for Environmental Protection (2015). Annual report on the state of air quality in the Republic of Serbia, Republic of Serbia Ministry of Environmental Protection, Environmental Protection Agency, Belgrade. Accessed 25 July 2019.
  37. SEPA – Serbian Agency for Environmental Protection (2016). Annual report on the state of air quality in the Republic of Serbia, Republic of Serbia Ministry of Environmental Protection, Environmental Protection Agency, Belgrade. Accessed 25 July 2019.
  38. Serbula, S. M., Miljkovic, D. D., Kovacevic, R. M., & Ilic, A. A. (2012). Assessment of airborne heavy metal pollution using plant parts and top soil. Ecotoxicology and Environmental Safety., 76, 209–214. Scholar
  39. Serbula, S. M., Kalinovic, T. S., Ilic, A. A., Kalinovic, J. V., & Steharnik, M. M. (2013). Assessment of airborne heavy metal pollution using Pinus spp. and Tilia spp. Aerosol and Air Quality Research, 13(2013), 563–573. Scholar
  40. Šichorová, K., Tlustoš, P., Száková, J., Kořínek, K., & Balík, J. (2004). Horizontal and vertical variability of heavy metals in the soil of a polluted area. Plant, Soil and Environment, 50(12), 525–534.CrossRefGoogle Scholar
  41. Simon, E., Baranyai, E., Braun, M., Cserháti, C., Fábián, I., & Tóthmérész, B. (2014). Elemental concentrations in deposited dust on leaves along an urbanization gradient. Science of the Total Environment, 490, 514–520. Scholar
  42. Singh, H., Savita, Sharma, R., Sinha, S., Kumar, M., Kumar, P., et al. (2017). Physiological functioning of Lagerstroemia speciosa L. under heavy roadside traffic: an approach to screen potential species for abatement of urban air pollution. 3. Biotech, 7(61), 1–10. Scholar
  43. Škrbić, B., & Đurišić-Mladenović, N. (2013). Distribution of heavy elements in urban and rural surface soils: the Novi Sad city and the surrounding settlements, Serbia. Environmental monitoring and assessment, 185(1), 457–471. Scholar
  44. STATISTICA 7.0. StatSoft 2004, University License, University of Novi Sad.Google Scholar
  45. Šućur, K. M., Aničić, M. P., Tomašević, M. N., Antanasijević, D. Z., Perić-Grujić, A. A., & Ristić, M. Đ. (2010). Urban deciduous tree leaves as biomonitors of trace element (As, V and Cd) atmospheric pollution in Belgrade, Serbia. Journal of the Serbian Chemical Society, 75(10), 1453–1461.CrossRefGoogle Scholar
  46. Suzuki, K., Yabuki, T., & Ono, Y. (2009). Roadside Rhododendron pulchrum leaves as bioindicators of heavy metal pollution in traffic areas of Okayama, Japan. Environmental monitoring and assessment, 149(1-4), 133–141. Scholar
  47. Szyczewski, P., Siepak, J., Niedzielski, P. & Sobczynski, T. (2009). Research on heavy metals in Poland. Polish Journal of Environmental Studies, 18(5).Google Scholar
  48. Tomašević, M., Rajšić, S., Đorđević, D., Tasić, M., Krstić, J., & Novaković, V. (2004). Heavy metals accumulation in tree leaves from urban areas. Environmental Chemistry Letters, 2(3), 151–154. Scholar
  49. Tóth, G., Hermannb, T., Da Silva, M. R., & Montanarella, L. (2016). Heavy metals in agricultural soils of the European Union with implications for food safety. Environment International, 88, 299–309. Scholar
  50. Tutin, T. G., Heywood, V. H., Burges, N. A., Valentine, D. H., Walters, S. M., & Webb, D. A. (Eds.). (1964-1980). Flora Europaea I-V. Cambridge: Cambridge University press.Google Scholar
  51. Tyler, G. (2005). Changes in the concentration of major, minor and rare earth elements during leaf senescence and decomposition in a Fagus sylvatica forest. Forest Ecology and Management, 206, 167–177. Scholar
  52. Ugolini, F., Tognetti, R., Raschi, A., & Bacci, L. (2013). Quercus ilex L. as bioaccumulator for heavy metals in urban areas: effectiveness of leaf washing with distilled water and considerations on the trees distance from traffic. Urban forestry & urban greening, 12(4), 576–584. Scholar
  53. Wang, L., Liu, L. Y., Gao, S. Y., Hasi, E., & Wang, Z. (2006). Physicochemical characteristics of ambient particles settling upon leaf surfaces of urban plants in Beijing. Journal of Environmental Sciences, 18(5), 921–926.CrossRefGoogle Scholar
  54. Wang, L. K., Chen, J. P., Hung, Y. T., & Shammas, N. K. (2017). Heavy metals in the environment. New York: CRC Press, Taylor & Francis Inc..Google Scholar
  55. Wang, L. K., Hung, Y.-T., Chen, J. P., Wang, M. H. S., & Shammas, N. K. (2017a). Remediation of heavy metals in the environment. New York: CRC Press, Taylor & Francis Inc..Google Scholar
  56. Watson, G. W., & Hewitt, A. M. (2012). The relationship between structural root depth and vigor of urban trees. Arboriculture & Urban Forestry, 38(1), 13–17.Google Scholar
  57. Wells, C. E., Townsend, K. S., Caldweel, J. D., Ham, D. L., Smiley, E. T., & Sherwood, M. (2005). Effects of planting depth on landscape tree survival and girdling root formation. Arboriculture & Urban Forestry, 32, 305–311. Scholar
  58. Wu, Y., Peng, X., & Hu, X. (2013). Vertical distribution of heavy metal in soil of abandoned vehicles dismantling area. Asian journal of chemistry, 25(15), 8423–8426.CrossRefGoogle Scholar
  59. Wuana, R. A. & Okieimen, F. E. (2011). Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology, 2011, Article ID 402647. doi:,CrossRefGoogle Scholar
  60. Zaikov, G. E., Weisfeld, L. I., Lisitsyn, E. M., & Bekuzarova, S. A. (2017). Heavy metals and other pollutants in the environment: biological aspects. Toronto: Apple Academic Press.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Faculty of AgricultureUniversity of Novi SadNovi SadSerbia
  2. 2.BioSense InstituteUniversity of Novi SadNovi SadSerbia
  3. 3.Swedish University of Agricultural SciencesUmeåSweden
  4. 4.Faculty of Technical SciencesUniversity of Novi SadNovi SadSerbia

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