Seasonal variations of trace element contents in leaves and bark of horse chestnut (<i>Aesculus hippocastanum</i> L.) in urban and industrial regions in Serbia
Keywords:trace elements, urban parks, Aesculus hippocastanum, biomonitoring, soil pollution
In this study, we examined the ability of horse chestnut (Aesculus hippocastanum L.) to capture heavy metals, and whether its capacity to absorb metals from soil is associated with surrounding ecological characteristics and sources of pollution. We studied the seasonal accumulation of B, Cu, Sr and Zn in leaves and bark, and the chlorophyll content in the common deciduous tree Aesculus hippocastanum L. in four urban parks in Pančevo, Smederevo, Obrenovac and Belgrade (Serbia) affected by different anthropogenic activities. The research included plants from a control site located within the zone of a former oak forest. Our findings suggest that there are potential ecological risks around Smederevo, Belgrade and Obrenovac due to elevated concentrations of B and Zn relative to the average concentrations described for worldwide soils, as well as national regulations. Substantial and toxic foliar accumulation of B was observed in Smederevo and Belgrade, and of Sr in both plant tissues at all sites. However, the Cu and Zn contents in leaves were not enough to meet the physiological needs of plants. Chlorophyll a and the total carotenoid content peaked in August under the most unfavorable conditions of the year, which may be considered as an adaptive mechanism. The obtained results showed the remarkable complexity of environmental conditions and the difficulties A. hippocastanum, as a species, has to overcome. Under conditions of different types of urban and industrial pollution, A. hippocastanum showed great element accumulation potential and could be regarded as both an accumulator and a response indicator, since its leaves are quite susceptible to damage.
Received: December 2, 2016; Revised: January 12, 2017; Accepted: January 31, 2017; Published online: February 2, 2017
How to cite this article: Pavlović M, RakićT, PavlovićD, 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.
Craul PJ. Urban Soils: Application and Practices. New York: John Wiley and Sons, Inc; 1999. 336 p
Oleksyn J, Kloeppel BD, Lukasiewicz S, Karolewski P, Reich PB. Ecophysiology of horse chestnut (Aesculus hippocastanum L.) in degraded and restored urban sites. Pol J Ecol. 2007;55(2):245-60.
Bradl H. Heavy Metals in the Environment: Origin, Interaction and Remediation. 1st ed. London: Academic Press; 2002. 282 p.
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metals toxicity and the environment. NIH-PA. 2012;101:133-64.
Tyrväinen L, Pauleit S, Seeland K, de Vries S. Benefits and uses of urban forests and trees. In: Konijnendijk CC, Nilsson K, Randrup TB, Schipperijn J, editors. Urban Forests and Trees. Berlin: Springer-Verlag, Heidelberg; 2005. p. 81-114.
Grieve IC. Human impacts on soil properties and their implications for the sensitivity of soil systems in Scotland. Catena. 2001;42:361-74.
Jim CY. Trampling impacts of recreationists on picnic sites in a Hong Kong country park. Environ Conserv. 1987;14(2):117-27.
Kirpichtchikova TA, Manceau A, Spadini L, Panfili F, Marcus MA, Jacquet T. Speciation and solubility of heavy metals in contaminated soil using X-ray microfluorescence, EXAFS spectroscopy, chemical extraction, and thermodynamic modeling. Geochim Cosmochim Acta. 2006;70(9):2163-90.
Wuana RA, Okieimen FE. Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology. 2011;2011:402647.
Chibuike GU, Obiora SC. Heavy metal polluted soils: Effects on plants and bioremediation methods. Appl Environ Soil Sci. 2014;2014:752708.
Kabata-Pendias A, Pendias H. Trace Elements in Soil and Plants. 1st ed. Boca Raton FL (USA): CRC Press; 1984. 315 p.
Kloke A, Sauerback DR, Vetter H. The contamination of plants and soils with heavy metals and the transport of metals in terrestrial food chains. In: Nriagu JO, editors. Changing Metal Cycles and Human Health. Berlin: Springer-Verlag, Heidelberg; 1984. p. 113-41.
Madejon P, Ciadamidaro L, Maranon T, Murillo JM. Long-term biomonitoring of soil contamination using poplar trees: accumulation of trace elements in leaves and fruits. Int J Phytoremediat. 2013;15:602-14.
Berlizov AN, Blum OB, Filby RH, Malyuk IA, Tryshyn VV. Testing applicability of black poplar (Populus nigra L.) bark to heavy metal air pollution monitoring in urban and industrial regions. Sci Total Environ. 2007;372:693-706.
Kozlov MV. Sources of variation in concentrations of nickel and copper in mountain birch foliage near a nickel-copper smelter at Monchegorsk, north-western Russia: results of long-term monitoring. Environ Pollut. 2005;135:91-9.
Samecka-Cymerman A, Stankiewicz A, Kolon K, Kempers AJ. Self-organizing feature map (neural networks) as tool to select the best indicator of road traffic pollution (soil, leaves or bark of Robinia pseudoacacia L.). Environ Pollut. 2009;157:2061-65.
Šerbula SM, Kalinović TS, Ilić AA, Kalinović JV, Steharnik MM. Assessment of airborne heavy metal pollution using Pinus spp. and Tilia spp. Aerosol Air Qual Res. 2013;13:563-73.
Tomašević M, Vukmirović Z, Rajšić S, Tasić M, Stevanović B. Characterization of trace metal particles deposited on some deciduous tree leaves in an urban area. Chemosphere. 2005;61:753-60.
Nagajyoti PC, Lee KD, Sreekanth TVM. Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett. 2010;8:199-216.
Schulz H, Popp P, Huhn G, Stärk HJ, Schüürmann G. Biomonitoring of airborne inorganic and organic pollutants by means of pine tree barks. I. Temporal and spatial variations. Sci Total Environ. 1999;232:49-58.
Rossini Oliva S, Mingorance MD. Assessment of airborne heavy metal pollution by aboveground plant parts. Chemosphere. 2006;65:177-82.
Sawadis T, Breuste J, Mitrović M, Pavlović P, Tsigaridas K. Trees as bioindicator of heavy metal pollution in three European cities. Environ Pollut. 2011;59:3560-70.
Tomašević M, Vukmirović Z, Rajšić S, Tasić M, Stevanović B. Contribution to biomonitoring of some trace metals by deciduous tree leaves in urban areas. Environ Monit Assess. 2008;137:393-401.
Baycu G, Tolunay D, Ozden H, Gunebakan S. Ecophysiological and seasonal variations in Cd, Pb, Zn and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environ Pollut. 2006;143:545-54.
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.
Mitrović M, Jarić S, Kostić O, Gajić G, Karadžić B, Djurdjević L, Oberan Lj, Pavlović D, Pavlović M, Pavlović P. Photosynthetic Efficiency of Four Woody Species Growing on Fly Ash Deposits of a Serbian ‘Nikola Tesla – A’ Thermoelectric Plant. Pol J Environ Stud. 2012;21(5):1339-47.
Statistical Office of the Republic of Serbia. Annual report for traffic and telecommunications 2012 [Internet]. Belgrade: Statistical Office of the Republic of Serbia; 2012 [cited 2016 January 12]. Available from: http://www.stat.gov.rs/WebSite/Public/PageView.aspx?pKey=150
Smailagić J, Savović A, Nešić D, Milenković M, Zdravković S. Climatological Analysis of Summer 2012. for Serbia. Seasonal Bulletin. Belgrade: Republic of Serbia, Republic Hydrometeorological Service of Serbia; 2012. 22 p. Serbian.
Dick WA, Cheng L, Wang P. Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biol Biochem. 2000;32:1915-19.
Atterberg A. Die Plastizitat der Tone. Int Mitt Bodenkd. 1911;1:10–43
US Soil Survey Staff. Selected chemical properties. In: Soil survey manual. Handbook 18. Washington: Soil Conservation Service, United States Department of Agriculture; 1993. p. 46-155.
Zayed A, Gowthaman S, Terry N. Phytoaccumulation of trace elements by wetland plants: I. Duckweed. J Environ Qual. 1998;27:715-21.
Hiscox JD, Israelstam GF. A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot. 1979;57:1332-34.
Arnon DI. Copper enzymes in isolated chloroplasts. Polyphenoloxidases in Beta vulgaris. Plant Physiol. 1949;24:1-15.
Wellburn A. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol. 1994;144:307-55.
Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M. Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr. 2010;10(3):268-92.
Bot A, Benites J. The importance of soil organic matter: Key to drought-resistant soil and sustained food prodution. Rome: Food and Agriculture Organization of the United Nations; 2005. 77 p. (FAO Soils Bulletin; 80).
Adriano DC, Weber J, Bolan NS, Paramasivan S, Koo B-J, Sajwan KS. Effects of high rates of fly ash on soil, turfgrass, and groundwater quality. Water Air Soil Pollut. 2002;139:365-85.
Jovanović S. Ecological study of ruderal flora and vegetation in the city of Belgrade. Belgrade: Faculty of Biology, University of Belgrade; 1994. 222 p.
Puskás I, Farsang A. Diagnostic indicators for characterizing urban soils of Szeged, Hungary. Geoderma. 2009;148:267-81.
Kabata-Pendias A, Pendias H. Trace Elements in Soils and Plants. 3rd ed. Boca Raton FL (USA): CRC Press; 2001. 331 p.
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 from the ‘Nikola Tesla - A’ Thermoelectric plant (Obrenovac, Serbia). Arch Biol Sci. 2012;64(1):145-58.
Pavlović P, Mitrović M, Djurdjević L. An ecophysiological study of plants growing on the fly ash deposits from the “Nikola Tesla‐A” thermal power station in Serbia. Environ Manage. 2004;33:654-63.
James WD, Graham CC, Glascock MD, Hanna ASG. Water-leachable boron from coal ashes. Environ Sci Technol. 1982;16:195-97.
Camacho-Cristobal JJ, Rexach J, Gonzalez-Fontes A. Boron in plants: deficiency and toxicity. J Integr Plant Biol. 2008;50(10):1247-55.
Gupta UC. Boron nutrition in crops. Adv Agron. 1979;31:273-307.
Regulations on permitted quantity of hazardous and harmful substances in soil. Official Gazette of Republic of Serbia. 1994;23/1994.
Šerbula SM, Miljković DDJ, Kovačević RM, Ilić AA. Assessment of airborne heavy metal pollution using plant parts and topsoil. Ecotoxicol Environ Saf. 2012;76:209-14.
West HK, Davies MS, Morgan AJ, Herbert RJ. The relationship between Sr and Ca accumulation in the major constituents of a terrestrial community resident on a celestitic (SrSO4) soil in S.W. England. Eur J Soil Biol. 2001;37:333-6.
Stamoulis KC, Assimakopoulos PA, Ioannides KG, Johnson E, Soucacos PN. Strontium-90 concentration measurement in human bones and teeth in Greece. Sci Total Environ. 1999;229:165-82.
Moyen C, Roblin G. Uptake and translocation of strontium in hydroponically grown maize plants, and subsequent effects on tissue ion content, growth and chlorophyll a/b ration: comparison with Ca effects. Environ Exp Bot. 2010;68:247-57.
Hafeez B, Khanif YM, Saleem M. Role of Zinc in Plant Nutrition- A Review. Am J Exp Agric. 2013;3(2):374-91.
Brown P H, Shelp BJ. Boron mobility in plants. Plant Soil. 1997;193:85-101.
Graham RD, Welch RM, Grunes DL, Carey EE, Norvell WA. Effect of zinc deficiency on the accumulation of boron and other mineral nutrients in barley. Soil Sci Soc Am J. 1987;51:652-7.
Nable RO, Banuelos GS, Paull JG. Boron toxicity. Plant Soil. 1997;193:181-98.
Kim ND, Fergusson JE. Seasonal variations in the concentration of cadmium, copper, lead and zinc in leaves of the horse chesnut (Aesculus hippocastanum L.). Environ Pollut. 1994;86:89-97.
Harrison RM, Tilling R, Romero MSC, Harrard S, Jarvis K. A study of trace metals and polyciclyc aromatic hydrocarbons in the roadside environment. Atmos Environ. 2003;37:2391-402.
Baker DE, Seneft JP. Copper. In: Alloway BJ, editors. Heavy metals in soils. London: Blackie Academic and Professional; 1995. p.179-205.
Shacklette HT, Erdman JA, Harms TF. Trace elements in plants foodstuffs. In: Oehme FW, editors. Toxicity of Heavy Metals in the Environment, Part I. New York: Marcel Dekker Inc; 1978. p. 25.
Tsukada H, Takeda TT, Hasegawa H, Hisamatsu S, Inaba J. Uptake and distribution of 90Sr and stable Sr in rice plants. J Environ Radioactiv. 2005;81:221-31.
Scheffer K, Stach W, Vardakis F. Uber die Verteilung der Schwermatallen Eisen. Mangan, Kupfer und Zink in Sommergesternpflanzen. Landwirtsch Forsch. 1978;156(2):326.
Van Bohemen HD, Van de Laak JWH. The influence of road infrastructure and traffic on soil, water, and air quality. Environ Manage. 2003;31(1):50-68.
Fitz WJ, Wenzel WW. Arsenic transformations in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation. J Biotechnol. 2002;99:259-78.
Parkesh D, Puranik RM, Srivastava HS. Inhibition of chlorophyll biosynthesis by cadmium in greening maize leaf segments. Biochem Physiol Pflanz. 1990;186:239-42.
Joshi PC, Swami A. Air pollution induced changes in the photosynthetic pigments of selected plant species. J Environ Biol. 2009;30:295-8.
Seyyednejad SM, Niknejad M, Koochak H. A review of some different effects of air pollution on plants. Res J Environ Sci. 2011;5(4):302-09.
Tripathi AK, Gautam M. Biochemical parameters of plants as indicators of air pollution. J Environ Biol. 2007;28:127-32.
Joshi PC, Swami A. Physiological responses of some tree species under roadside automobile pollution stress around city of Haridwar, India. Environmentalist. 2007;27:365-74.
Giri S, Shrivastava D, Deshmukh K, Dubey P. Effect of air pollution on chlorophyll content of leaves. Curr Agri Res. 2013;1(2):93-8.
Keser G. Effects of irrigation with wastewater on the physiological properties and heavy metal content in Lepidium sativum L. and Eruca sativa (Mill.). Environ Monit Assess. 2013;185: 6209-17.
Dezhban A, Shirvany A, Attarod P, Delshad M, Matinizadeh M, Khoshnevis M. Cadmium and lead effects on chlorophyll fluorescence, chlorophyll pigments and proline of Robinia pseudoacacia. J For Res. 2015:26(2):323-9.
Nabeela F, Murad W, Khan I, Mian IA, Rehman H. Effect of wood ash application on the morphological, physiological and biochemical parameters of Brassica napus L. Plant Physiol Biochem. 2015;95:15-25.
Sai Kachout S, Ben Mansoura A, Ennajah A, Leclerc JC, Ouerghi Z, Karray Bouraoui N. Effects of metal toxicity on growth and pigment contents of annual halophyte (A. hortensis and A. rosea). Int J Environ Res. 2015;9(2):613-20.
Patterson S. The agronomic benefit of pulp mill boiler wood ash. [dissertation]. [Lethbridge]: Agricultural Biotechnology, University of Lethbridge. 2001. 142 p.
Bartley GE, Scolnik PA. Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell. 1995;7(7):1027-38.
Gould KS. Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol. 2004;5:314-20.
Brugnoli E, Cona A, Lauteri M. Xanthophyll cycle components and capacity for non-radiative energy dissipation in sun and shade leaves of Ligustrum ovalifolium exposed to conditions limiting photosynthesis. Photosynth Res. 1994;41:451-63.