Uptake and distribution of Cu, Pb, and Zn in Tilia tomentosa Moench: plant tissue and urban soil interactions
DOI:
https://doi.org/10.2298/ABS250731027RKeywords:
phytoremediation, Tilia tomentosa Moench, potentially toxic elements accumulation, bioconcentration and translocation factors, photosynthetic efficiencyAbstract
Paper description:
- Trees contribute to urban ecosystem services.
- This study analyzed Cu, Pb and Zn concentrations in Tilia tomentosa leaves, roots and associated soil (at 0-10cm and 10-30 cm) in an urban park, avenue and its natural habitat to test its vitality and phytoremediation potential.
- Site-dependent variations were observed for all parameters, especially at the tree-lined avenue at both depths, with Pb and Zn concentrations >200 mg/kg and insignificant Pb soil-leaf transfer.
- The study highlights the importance of species selection, as trees can affect soil’s chemical properties with urban green space planting, thus influencing soil functions and ecosystem service delivery.
Abstract: This study analyzed Cu, Pb, and Zn concentrations in roots and leaves of Tilia tomentosa Moench. and associated soil (at 0-10 cm and 10-30 cm) at Bulevar Nikola Tesla (BNT) and Park Ušće (PU) (Belgrade, Serbia), with Fruška Gora Mt. serving as the control. To evaluate its phytoremediation potential, the bioconcentration (BCFRoot and BCFLeaf) and translocation factors (TF) were calculated. Site-dependent variations were observed for all analyzed parameters, especially at BNT at both depths, with Pb and Zn concentrations greater than 200 mg/kg. Leaf Pb concentrations indicated insignificant soil-leaf transfer. Photosynthetic efficiency measurements in T. tomentosa showed similar mean values within the optimum range for plants at all sites (Fv/Fm > 0.800). This indicates high overall vitality in urban habitats with elevated concentrations of potentially toxic elements, as shown by the absence of statistically significant differences in mean chlorophyll fluorescence values between sites. There was a positive correlation between Cu and Zn levels and Fv/Fm in leaves from all analyzed sites. Thus, the species appears well-adapted to the uptake and accumulation of elements that are vital for optimal photosynthesis and other physiological processes, while photosynthetic efficiency is not significantly impacted by their occasional deficiency.
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References
Oliveira MCQD, Miranda RM, Andrade MF, Kumar P. Impact of urban green areas on air quality: An integrated analysis in the metropolitan area of São Paulo. Environ Pollut. 2025;372:126082. https://doi.org/10.1016/j.envpol.2025.126082
Morel JL, Chenu C, Lorenz K. Ecosystem services provided by soils of urban, industrial, traffic, mining, and military areas (SUITMAs). J Soil Sediments. 2015;15:1659-66. https://doi.org/10.1007/s11368-014-0926-0
Pavlović P, Sawidis T, Breuste J, Kostić O, Čakmak D, Ðordević D, Pavlović D, Pavlović M, Perović V, Mitrović M. Fractionation of Potentially Toxic Elements (PTEs) in Urban Soils from Salzburg, Thessaloniki and Belgrade: An Insight into Source Identification and Human Health Risk Assessment. Int J Environ Res Public Health. 2021a;18:6014. https://doi.org/10.3390/ijerph18116014
Li Y, Feng D, Ji M, Li Z, Zhang R, Gu C. The risk characteristics of heavy metals in urban soil of typical developed cities in China. Environ Monit Assess. 2022;194(2):1-11. https://doi.org/10.1007/s10661-022-09798-9
Madrid L, Díaz-Barrientos E, Reinoso R, Madrid F. Metals in urban soils of Sevilla: seasonal changes and relations with other soil components and plant contents. Eur J Soil Sci. 2004;55:209-17. https://doi.org/10.1046/j.1365-2389.2004.00589.x
Binner H, Sullivan T, Jansen MAK, McNamara ME. Metals in urban soils of Europe: A systematic review. Sci Total Environ. 2023;854:158734. https://doi.org/10.1016/j.scitotenv.2022.158734
Glennon MM, Harris P, Ottesen RT, Scanlon RP, O’Connor PJ. The Dublin SURGE project: geochemical baseline for heavy metals in topsoils and spatial correlation with historical industry in Dublin, Ireland. Environ Geochem Health. 2014;36:235-54. https://doi.org/10.1007/s10653-013-9561-8
Setälä H, Francini G, Allen JA, Jumpponen A, Hui N, Kotze DJ. Urban parks provide ecosystem services by retaining metals and nutrients in soils. Environ Pollut. 2017;231(Pt 1):451-61. https://doi.org/ 10.1016/j.envpol.2017.08.010
Blanusa T, Garratt M, Cathcart-James M, Hunt L, Cameron WFR. Urban hedges: A review of plant species and cultivars for ecosystem service delivery in north-west Europe. Urban For Urban Green. 2019;44:126391. https://doi.org/10.1016/j.ufug.2019.126391
Grote R, Samson R, Alonso R, Amorim JH, Cariñanos P, Churkina G, Fares S, Thiec DL, Niinemets Ü, Mikkelsen TN. Functional traits of urban trees: air pollution mitigation potential. Front Ecol Environ. 2016;14(10):543-50. https://doi.org/10.1002/fee.1426
Sawidis T, Breuste J, Mitrovic M, Pavlovic P, Tsigaridas K. Trees as bioindicator of heavy metal pollution in three European cities. Environ Pollut. 2011;159(12):3560-70. https://doi.org/10.1016/j.envpol.2011.08.008
Mitrović M, Blanusa T, Pavlović M, Pavlović D, Kostić O, Perović V, Jarić S, Pavlović P. Using Fractionation Profile of Potentially Toxic Elements in Soils to Investigate Their Accumulation in Tilia sp. Leaves in Urban Areas with Different Pollution Levels. Sustainability. 2021;13:9784. https://doi.org/10.3390/su13179784
Pavlović M, Rakić T, Pavlović D, Kostić O, Jarić S, Mataruga Z, Pavlović P, Mitrović M. Seasonal variations of trace element contents in leaves and bark of horse chestnut (Aesculus hippocastanum L.) in urban and industrial regions in Serbia. Arch Biol Sci. 2017;69(2):201-14. https://doi.org/10.2298/ABS161202005P
Wolff K, Hansen OK, Couch S, Moore L, Sander H, Logan SA. Tilia cultivars in historic lime avenues and parks in the UK, Estonia and other European countries. Urban For Urban Green. 2019;43:126346. https://doi.org/10.1016/j.ufug.2019.05.008
Andrianjara I, Bordenave-Jacquemin M, Roy V, Cabassa C, Federici P, Carmignac D, Marcangeli Y, Rouhan G, Renard M, Nold F, Lata J-C, Genet P, Planchais S. Urban tree management: Diversity of Tilia genus in streets and parks of Paris based on morphological and genetic characteristics. Urban For Urban Green. 2021;66:127382. https://doi.org/10.1016/j.ufug.2021.127382
Galle JN, Halpern D, Nitoslawski S, Duarte F, Ratti C, Pilla F. Mapping the diversity of street tree inventories across eight cities internationally using open data. Urban For Urban Green. 2021;61:127099. https://doi.org/10.1016/j.ufug.2021.127099
Sjöman H, Busse Nielsen A. Selecting trees for urban paved sites in Scandinavia - A review of information on stress tolerance and its relation to the requirements of tree planners. Urban For Urban Green. 2010;9(4):281-93. https://doi.org/10.1016/j.ufug.2010.04.001
Selmi W, Weber C, Rivière E, Blond N, Mehdi L, Nowak D. Air pollution removal by trees in public green spaces in Strasbourg city, France. Urban For Urban Green. 2016;17:192-201. https://doi.org/10.1016/j.ufug.2016.04.010
Quénéa K, Andrianjara I, Rankovic A, Gan E, Aubry E, Lata JC, Barot S, Castrec-Rouelle M. Influence of the residence time of street trees and their soils on trace element contamination in Paris (France). Environ Sci Pollut Res. 2019;26(10):9785-9795. https://doi.org/10.1007/s11356-019-04405-w
Kostić O, Mitrović M, Knežević M, Jarić S, Gajić G, Djurdjević L, Pavlović P. The potential of four woody species for the revegetation of fly ash deposits of ‘Nikola Tesla-A’ thermoelectric plant (Obrenovac, Serbia). Arch Biol Sci. 2012;64(1):145-58. https://doi.org/10.2298/ABS1201145K
USEPA Method 3052. Microwave assisted acid digestion of siliceous and organically based matrices. In: Test Methods for Evaluating Solid Waste, SW 846. Washington, DC: U.S. Environmental Protection Agency; 1996.
Yoon J, Cao X, Zhou Q, Ma LQ. Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ. 2006;368(2-3):456-64. https://doi.org/10.1016/j.scitotenv.2006.01.016
Biasioli M, Grčman H, Kralj T, Madrid F, Díaz-Barrientos E, Ajmone-Marsan F. Potentially Toxic Elements Contamination in Urban Soils: A Comparison of Three European Cities. J Environ Qual. 2007;36:70-9. https://doi.org/10.2134/jeq2006.0254
Ye J, Li J, Wang P, Ning Y, Liu J, Yu Q, Bi X. Inputs and sources of Pb and other metals in urban area in the post leaded gasoline era. Environ Pollut. 2022;306:119389. https://doi.org/10.1016/j.envpol.2022.119389
Reimann C, de Caritat P. Distinguishing between natural and anthropogenic sources for elements in the environment: regional geochemical surveys versus enrichment factors. Sci Total Environ. 2005;337:91-107. https://doi.org/10.1016/j.scitotenv.2004.06.011
Pavlović D, Pavlović M, Perović V, Mataruga Z, Čakmak D, Mitrović M, Pavlović P. Chemical fractionation, environmental, and human health risk assessment of potentially toxic elements in soil of industrialised urban areas in Serbia. Int J Environ Res Public Health. 2021b;18:9412. https://doi.org/10.3390/ijerph18179412
Nazarpour A, Watts MJ, Madhani A, Elahi S. Source, Spatial Distribution and Pollution Assessment of Pb, Zn, Cu, and Pb Isotopes in urban soils of Ahvaz City, a semi-arid metropolis in southwest Iran. Sci Rep. 2019;9:5349. https://doi.org/10.1038/s41598-019-41787-w
Foroughi M, Weil RR. Soil lead, zinc, and copper in two urban forests as influenced by highway proximity. J Environ Qual. 2025;54(1):275-88. https://doi.org/10.1002/jeq2.20642
Adriano DC. Trace elements in Terrestrial Environments: Biogeochemistry, Bioavailability and Risks of Metals. 2nd ed. New York: Springer; 2001. 867 p. https://doi.org/10.1007/978-0-387-21510-5
Gawlik BW, Bidoglio G, editors. Background values in European soils and sewage sludges PART III, Conclusions, Comments and Recommendations. Luxembourg: European Commission, Directorate-General Joint Research Centre, Institute for Environment and Sustainability; 2006.
Payá Pérez A, Rodríguez Eugenio N. Status of local soil contamination in Europe: Revision of the indicator “Progress in the management Contaminated Sites in Europe”. Report No.: EUR 29124 EN. Luxembourg: Publications Office of the European Union; 2018. https://doi.org/10.2760/093804. JRC107508
Foti L, Dubs F, Gignoux J, Lata J-C, Lerch TZ, Mathieu J, Nold F, Nunan N, Raynaud X, Abbadie L, Barot S. Trace element concentrations along a gradient of urban pressure in forest and lawn soils of the Paris region (France). Sci Total Environ. 2017;598:938-48. https://doi.org/10.1016/j.scitotenv.2017.04.111
Yu S, Zhu YG, Li XD. Trace metal contamination in urban soils of China. Sci Total Environ. 2012;421:17-30. https://doi.org/10.1016/j.scitotenv.2011.04.020
Alloway BJ, editor. Heavy Metals in Soils: Trace Metals and Metalloids in Soils and their Bioavailability. Environ Pollut. Dordrecht: Springer; 2013. https://doi.org/10.1007/978-94-007-4470-7_8
Ballinas M, Barradas VL. The urban tree as a tool to mitigate the urban heat island in Mexico City: A simple phenomenological model. J Environ Qual. 2016;45:157-66. https://doi.org/10.2134/jeq2015.01.0056
van der Putten WH, Bradford MA, Pernilla Brinkman E, van de Voorde TFJ, Veen GF. Where, when and how plant-soil feedback matters in a changing world. Funct Ecol. 2016;30(8):1109-21. https://doi.org/10.1111/1365-2435.12657
Kusiak W, Majka J, Zborowska M, Ratajczak I. Chemical Composition and Related Properties of Lime (Tilia cordata Mill.) Bark and Wood as Affected by Tree Growth Conditions. Materials . 2022;15(11):4033. https://doi.org/10.3390/ma15114033
Andrianjara I, Cabassa C, Lata J-C, Hansart A, Raynaud X, Renard M, Nold F, Genet P, Planchais S. Characterization of stress indicators in Tilia cordata Mill. as early and long-term stress markers for water availability and trace element contamination in urban environments. Ecol Indic. 2024;158:111296. https://doi.org/10.1016/j.ecolind.2023.111296
Kabata-Pendias A, Pendias H. Trace Elements in Soils and Plants. Boca Raton: CRC Press LLC; 2001.
Hrotkó K, Gyeviki M, Sütöriné DM, Magyar L, Mészáros M, Honfi P, Kardos L. Foliar dust and heavy metal deposit on leaves of urban trees in Budapest (Hungary). Environ Geochem Health. 2021;43:1927-40. https://doi.org/10.1007/s10653-020-00769-y
Aničić M, Spasić T, Tomašević M, Rajšić S, Tasić M. Trace elements accumulation and temporal trends in leaves of urban deciduous trees (Aesculus hippocastanum and Tilia spp.). Ecol Indic. 2011;11:824-30. https://doi.org/10.1016/j.ecolind.2010.10.009
Piczak K, Lesniewicz A, Zyrnicki W. Metal concentrations in deciduous tree leaves from urban areas in Poland. Environ Monit Assess. 2003;86(3):273-87. https://doi.org/10.1023/a:1024076504099
Šijačić-Nikolić, M., Stanković, D., Krstić, B., Vilotić, D., Ivetić, V. (2012) The potential of different lime tree (Tilia spp) genotypes for phytoextraction of heavy metals. Genetika. 2012;44(3):537-48. https://doi.org/10.2298/GENSR1203537S
Pilon-Smits E. Phytoremediation. Annu Rev Plant Biol. 2005;56:15-39. https://doi.org/10.1146/annurev.arplant.56.032604.144214
Mataruga Z, Jarić S, Marković M, Pavlović M, Pavlović D, Jakovljević K, Mitrović M, Pavlović P. Evaluation of Salix alba, Juglans regia and Populus nigra as biomonitors of PTEs in the riparian soils of the Sava River. Environ Monit Assess. 2020;192:131. https://doi.org/10.1007/s10661-020-8085-9
Burges A, Alkorta I, Epelde L, Garbisu C. From phytoremediation of soil contaminants to phytomanagement of ecosystem services in metal contaminated sites. Int J Phytoremediat. 2018;20:384-97. https://doi.org/10.1080/15226514.2017.1365340
Bakshe P, Jugade R. Phytostabilization and rhizofiltration of toxic heavy metals by heavy metal accumulator plants for sustainable management of contaminated industrial sites: A comprehensive review. J Hazard Mater Adv. 2023;10:100293. https://doi.org/10.1016/j.hazadv.2023.100293
Popek R, Lukowski A, Bates C, Oleksyn J. Accumulation of particulate matter, heavy metals, and polycyclic aromatic hydrocarbons on the leaves of Tilia cordata Mill. in five Polish cities with different levels of air pollution. Int J Phytoremediation. 2017;19(12):1134-41. https://doi.org/10.1080/15226514.2017.1328394
Björkman O, Demmig B. Photon yield of O₂ evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta. 1987;170:489-504. https://doi.org/10.1007/BF00402983
Sjöman H, Oprea A. Potential of Tilia tomentosa Moench, for use in urban environments in north-west Europe, based on habitat studies in north-east Romania and the Republic of Moldova. Ekológia (Bratislava). 2010;29(4):360-72. https://doi.org/10.4149/ekol_2010_04_360
Chen H, Kardos L, Chen H, Szabó V. Investigating physiological responses and fine particulate matter retention of urban trees in Budapest. City Environ Interact. 2024;24:100182. https://doi.org/10.1016/j.cacint.2024.100182
Dowtin AL, Cregg BC, Nowak DJ, Levia DF. Towards optimized runoff reduction by urban tree cover: A review of key physical tree traits, site conditions, and management strategies. Landsc Urban Plan. 2023;239:104849. https://doi.org/10.1016/j.landurbplan.2023.104849
Hirons AD, Thomas PA. Applied Tree Biology. Oxford, UK: John Wiley & Sons Ltd.; 2018. p. 372-3. https://doi.org/10.1002/9781118296387
Aničić Urošević M, Jovanović G, Stević N, Deljanin I, Nikolić M, Tomašević M, Samson R. Leaves of common urban tree species (Aesculus hippocastanum, Acer platanoides, Betula pendula and Tilia cordata) as a measure of particle and particle-bound pollution: a 4-year study. Air Qual Atmos Health. 2019;12:1081-90. https://doi.org/10.1007/s11869-019-00724-6
Mitrović M, Kostić O, Miletić Z, Marković M, Radulović N, Sekulić D, Jarić S, Pavlović P. Bioaccumulation of Potentially Toxic Elements in Tilia tomentosa Moench. Trees from Urban Parks and Potential Health Risks from Using Leaves and Flowers for Medicinal Purposes. Forests. 2023;14:2204. https://doi.org/10.3390/f14112204
Petrova S, Velcheva I, Nikolov B, Vasileva T, Bivolarski V. Antioxidant Responses and Adaptation Mechanisms of Tilia tomentosa Moench, Fraxinus excelsior L. and Pinus nigra JF. Arnold towards urban air pollution. Forests. 2022;13(10):1689. https://doi.org/10.3390/f13101689
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Copyright (c) 2025 Natalija Radulović, Olivera Košanin, Dragana Pavlović, Danijela Đunisijević Bojović, Marko Perović, Marijana Novaković, Snežana Jarić, Dimitrije Sekulić, Milica Jonjev, Marija Matić, Zorana Miletić, Olga Kostić

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