Abstract
This study evaluates bioaccumulation and translocation potentials of trace elements (TEs) by Saponaria officinalis L. (soapwort) and Achillea millefolium L. (yarrow) in order to select and optimize phytoremediation methods for the polluted environment of the city of Bor, Serbia. According to the enrichment factor for soil (i.e., 57.9–128.8 for Cd and As), pollution index (i.e., 6.6–84.7 for Cu), pollution load index (2.9–98.8), individual potential risk factors (11.5–5163), and potential ecological risk index values (260–6379), urban and rural soils from the city of Bor were classified as very contaminated with the investigated TEs. The results from all the indices and statistical analysis showed significant ecological risks of Cu, As, and Cd at the investigated sites and urge the need for remediation. The enrichment factor of the plants for As (566.3) and Cd (306.2) indicated a high enrichment level of the herb organs at all the sites. Since there are small differences in metal accumulation index values between the herbs and their parts (root, shoot), soapwort and yarrow can be considered as potential bioindicators. Based on the biological concentration and translocation factors, soapwort can be recommended as a suitable herb for phytoextraction purposes of Pb, As, and Cd polluted areas. Yarrow shows good characteristics for phytoextraction of Cu, Pb, and As from the contaminated soil. Principal component analysis (PCA) and hierarchical cluster analysis (HCA) results indicate their similar origin from atmospheric deposition. Therefore, these herbs can be utilized as a bioindicator and phytoremediator in polluted areas influenced by metallurgical activities to detect possible levels of TEs.
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References
Acevedo-Figueroa D, Jiménez BD, Rodríguez-Sierra CJ (2006) Trace metals in sediments of two estuarine lagoons from Puerto Rico. Environ Pollut 141:336–342
Affholder MC, Prudent P, Masotti V, Coulomb B, Rabier J, Nguyen-The B, Laffont-Schwob I (2013) Transfer of metals and metalloids from soil to shoots in wild rosemary (Rosmarinus officinalis L.) growing on a former lead smelter site: human exposure risk. Sci Total Environ 454–455:219–229
Agyarko K, Darteh E, Berlinger B (2010) Metal levels in some refuse dump soils and plants in Ghana. Plant Soil Environ 56:244–251. https://doi.org/10.17221/13/2010-PSE
Alagić SČ, Šerbula SS, Tošić SB, Pavlović AN, Petrović JV (2013) Bioaccumulation of arsenic and cadmium in birch and lime from the Bor region. Arch Environ Contam Toxicol 65:671–682
Alagić SČ, Tošić SB, Dimitrijević MD, Antonijević MM, Nujkić MM (2015) Assessment of the quality of polluted areas based on the content of heavy metals in different organs of the grapevine (Vitis vinifera) cv. Tamjanika. Environ Sci Pollut Res 22:7155–7175
Alahabadi A, Ehrampoush MH, Miri M, Aval HE, Yousefzadeh S, Ghaffari HR, Ahmadi E, Talebi P, Fathabadi ZA, Babai F, Nikoonahad A, Sharafi K, Hosseini-Bandegharaei A (2017) A comparative study on capability of different tree species in accumulating heavy metals from soil and ambient air. Chemosphere 172:459–467
Antonijević M, Dimitrijević M, Milić S, Nujkić M (2012) Metal concentrations in the soils and native plants surrounding the old flotation tailings pond of the copper mining and smelting complex Bor (Serbia). J Environ Monit 14:866–877
Arpadjan S, Çelik G, Taşkesen S, Güçer Ş (2008) Arsenic, cadmium and lead in medicinal herbs and their fractionation. Food Chem Toxicol 46:2871–2875
Brunetti G, Soler-Rovira P, Farrag K, Senesi N (2009) Tolerance and accumulation of heavy metals by wild plant species grown in contaminated soils in Apulia region, Southern Italy. Plant Soil 318:285–298. https://doi.org/10.1007/s11104-008-9838-3
Bunney S (ed) (1984) The illustrated encyclopedia of herbs their medicinal and culinary uses. Dorset press, New York, pp 53–265 https://archive.org/details/illustratedencyc00bunn
Burken JG, Vroblesky DA, Balouet JC (2011) Phytoforensics, dendrochemistry, and Phytoscreening: new green tools for delineating contaminants from past and present. Environ Sci Technol 45:6218–6226
Burt R (2014) Soil survey field, and laboratory methods manual, soil survey investigations report no. 51, version 2.0. and soil survey staff (ed.). U.S. Department of Agriculture, Natural Resources Conservation Service, www.nrcs.usda.gov
Chai M, Li R, Ding H, Zan Q (2019) Occurrence and contamination of heavy metals in urban mangroves: a case study in Shenzhen, China. Chemosphere 219:165–173
Cheng Z, Chen L-J, Li H-H, Lin J-Q, Yang Z-B, Yang Y-X, Xu X-X, Xian J-R, Shao J-R, Zhu X-M (2018) Characteristics and health risk assessment of heavy metals exposure via household dust from urban area in Chengdu, China. Sci Total Environ 619–620:621–629
Dambiec M, Wojtuń B, Samecka-Cymerman A, Polechońska L, Rudecki A, Kempers AJ (2017) Fluorine and metals in Polygonum arenastrum Bor. From areas influenced by various types of industry. Ecol Indic 82:163–174. https://doi.org/10.1016/j.ecolind.2017.06.053
de Paula PHM, Mateus VL, Araripe DR, Duyck CB, Saint’Pierre TD, Gioda A (2015) Biomonitoring of metals for air pollution assessment using a hemiepiphyte herb (Struthanthus flexicaulis). Chemosphere 138:429–437
Demková L, Árvay L, Bobuíská L, Tomáš J, Stanovič R, Lošák T, Harangozo L, Vollmannová A, Bystrická J, Musilová J, Jobbágy J (2017) Accumulation and environmental risk assessment of heavy metals in soil and plants of four different ecosystems in a former polymetallic ores mining and smelting area (Slovakia). J Environ Sci Health A 52:479–490. https://doi.org/10.1080/10934529.2016.1274169
Dimitrijević MD, Antonijević MM, Dimitrijević VLJ (2002) Oksidacija pirita - posledice i značaj. Hemijska industrija 56:299–316 (In Serbian). http://www.serbia.nb.rs/img//0367-598X/2002/0367-598X0208299D.pdf
Dimitrijević M, Kostov A, Tasić V, Milosević N (2009) Influence of pyrometallurgical copper production on the environment. J Hazard Mater 164:892–899
Dimitrijević MD, Nujkić MM, Alagić SČ, Milić S, Tošić SB (2016) Heavy metal contamination of topsoil and parts of peach-tree growing at different distances from a smelting complex. Int J Environ Sci Technol 13:615–630. https://doi.org/10.1007/s13762-015-0905-z
Ettler V (2016) Soil contamination near non-ferrous metal smelters: a review. Appl Geochem 64:56–74. https://doi.org/10.1016/j.apgeochem.2015.09.020
Figueira R, Tavares PC, Palma L, Beja P, Sérgio C (2009) Application of indicator kriging to the complementary use of bioindicators at three trophic levels. Environ Pollut 157:2689–2696
Galal TM, Shehata HS (2015) Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecol Indic 48:244–251. https://doi.org/10.1016/j.ecolind.2014.08.013
Garcia JH, Li WW, Arimoto R, Okrasinski R, Greenlee J, Walton J, Schloesslin C (2004) Characterization and implication of potential fugitive dust sources in the Paso del Norte region. Sci Total Environ 325:95–112
Guan Y, Shao C, Ju M (2014) Heavy metal contamination assessment and partition for industrial and mining gathering areas. Int J Environ Res Public Health 11:7286–7303. https://doi.org/10.3390/ijerph110707286
Guo B, Liu Y, Zhang F, Hou J, Zhang H, Li C (2018) Heavy metals in the surface sediments of lakes on the Tibetan Plateau, China. Environ Sci Pollut Res 25:3695–3707
Håkanson L (1980) An ecological risk index for aquatic pollution control: a sedimentological approach. Water Res 14:975–1001. https://doi.org/10.1016/0043-1354(80)90143-8
Hoodaji M, Ataabadi M, Najafi P (2012) Biomonitoring of airborne heavy metal contamination, air pollution—monitoring, Modelling, health and control, Ed. Mukesh Khare, InTech Open, pp. 97–122. https://doi.org/10.5772/32963
Hu Y, Wang D, Wei L, Zhang X, Song B (2014) Bioaccumulation of heavy metals in plant leaves from Yanan city of the Loess Plateau, China. Ecotoxicol Environ Saf 110:82–88
Jin X, Jin Y, Mao X-F (2019) Ecological risk assessment of cities on the Tibetan Plateau based on land use/land cover changes—case study of Delingha City. Ecol Indic 101:185–191. https://doi.org/10.1016/j.ecolind.2018.12.050
Kabata-Pendias A (2011) Trace elements in soils and plants, 4th ed. CRC Press, Taylor and Francis Group, LLC Boca Raton, London, New York base.dnsgb.com.ua/files/book/Agriculture/Soil/Trace-Elements-in-Soils-and-Plants.pdf
Kalinović TS, Šerbula SM, Radojević AA, Kalinović JV, Šteharnik MM, Petrović JV (2016) Elder, linden and pine biomonitoring ability of pollution emitted from the copper smelter and the tailings ponds. Geoderma 262:266–275. https://doi.org/10.1016/j.geoderma.2015.08.027
Kalinović TS, Šerbula SM, Kalinović JV, Radojević AA, Petrović JV, Šteharnik MM, Milosavljević JS (2017) Suitability of linden and elder in the assessment of environmental pollution of Brestovac spa and Bor lake (Serbia). Environ Earth Sci 76:178. https://doi.org/10.1007/s12665-017-6485-0
Kalinović JV, Šerbula SM, Radojević AA, Milosavljević JS, Kalinović TS, Šteharnik MM (2019) Assessment of As, Cd, Cu, Fe, Pb, and Zn concentrations in soil and parts of Rosa spp. sampled in extremely polluted environment. Environ Monit Assess 191:15. https://doi.org/10.1007/s10661-018-7134-0
Kastori R, Petrović N Arsenijević-Maksimović I (1997) Teški metali i biljke.Poglavlje u "Teški metali u životnoj sredini" Ed. Kastori R, Novi Sad. (in Serbian)
Kleckerová A, Dočekalová H (2014) Dandelion plants as a biomonitor of urban area contamination by heavy metals, Int. J. Environ Res 8:157–164. https://doi.org/10.22059/IJER.2014.705
Lakshmi T, Geetha RV, Roy A, Kumar S (2011) Yarrow (Achillea millefolium Linn.) a herbal medicinal plant with broad therapeutic use—a review. Int J Pharm Sci Rev Res 9:136–141 www.globalresearchonline.net
Li J, Pu L, Liao Q, Zhu M, Dai X, Xu Y, Zhang L, Hua M, Jin Y (2015) How anthropogenic activities affect soil heavy metal concentration on a broad scale: a geochemistry survey in Yangtze River Delta, Eastern China. Environ Earth Sci 73:1823–1835. https://doi.org/10.1007/s12665-014-3536-7
Lin VS (2015) Research highlights: natural passive samplers—plants as biomonitors. Environ Sci Process Impacts 17:1137–1140. https://doi.org/10.1039/C5EM90016F
Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206
Liu YJ, Zhu YG, Ding H (2007) Lead and cadmium in leaves of deciduous trees in Beijing, China: development of a metal accumulation index (MAI). Environ Pollut 145:387–390
Maanan M, Saddik M, Maanan M, Chaibi M, Assobhei O, Zourarah B (2015) Environmental and ecological risk assessment of heavy metals in sediments of Nador lagoon, Morocco. Ecol Indic 48:616–626. https://doi.org/10.1016/j.ecolind.2014.09.034
Marques APGC, Moreira H, Rangel AOSS, Castro PML (2009) Arsenic, lead and nickel accumulation in Rubus ulmifolius growing in contaminated soil in Portugal. J Hazard Mater 165:174–179
Midhat L, Ouazzani N, Hejjaj A, Ouhammou A, Mandi L (2019) Accumulation of heavy metals in metallophytes from three mining sites (southern Centre Morocco) and evaluation of their phytoremediation potential. Ecotoxicol Environ Saf 169:150–160
Mihaljev Ž, Živkov-Baloš M, Ćupić Ž, Jakšić S (2014) Levels of some microelements and essential heavy metals in herbal teas in Serbia. Acta Pol Pharm Drug Res 71:385–391 https://europepmc.org/article/med/25265817
Mills GA, Greenwood R, Vrana B, Alland IJ, Ocelkae T (2011) J. Measurement of environmental pollutants using passive sampling devices—a commentary on the current state of the art. J Environ Monit 13:2979–2982
Mingorance MD, Valdés B, Oliva SR (2007) Strategies of heavy metal uptake by plants growing under industrial emissions. Environ Int 33:514–520
Monfared SH, Matinizadeh M, Shirvany A, Amiri GZ, Fard RM, Rostami F (2013) Accumulation of heavy metal in Platanus orientalis, Robinia pseudoacacia and Fraxinus rotundifolia. J For Res 24:391–395. https://doi.org/10.1007/s11676-012-0313-x
Nujkić M, Dimitrijević M, Alagić S, Tošić S, Petrović J (2016) Impact of metallurgical activities on the content of trace elements in the spatial soil and plant parts of Rubus fruticosus L. Environ Sci Process Impacts 18:350–360. https://doi.org/10.1039/c5em00646e
Pająk M, Halecki W, Gąsiorek M (2017) Accumulative response of Scots pine (Pinus sylvestris L.) and silver birch (Betula pendula Roth) to heavy metals enhanced by Pb-Zn ore mining and processing plants: explicitly spatial considerations of ordinary kriging based on a GIS approach. Chemosphere 168:851–859
Radojevic AA, Serbula SM, Kalinovic TS, Kalinovic JV, Steharnik MM, Petrovic JV, Milosavljevic SJ (2017) Metal/metalloid content in plant parts and soils of Corylus spp. influenced by mining–metallurgical production of copper. Environ Sci Pollut Res 24:10326–10340
Ranđelović D, Cvetković V, Mihailović N, Jovanović S (2014) Relation between edaphic factors and vegetation development on copper mine wastes: a case study from Bor (Serbia, SE Europe). Environ Manag 53:800–812
Reyes-Bozo L, Godoy-Faúndez A, Herrera-Urbina R, Higueras P, Salazar JL, Valdés-González H, Vyhmeister E, Antizar-Ladislao B (2014) Greening Chilean copper mining operations through industrial ecology strategies. J Clean Prod 84:671–679. https://doi.org/10.1016/j.jclepro.2014.03.088
Rodriguez JH, Wannaz ED, Salazar MJ, Pignata ML, Fangmeier A, Franzaring J (2012) Accumulation of polycyclic aromatic hydrocarbons and heavy metals in the tree foliage of Eucalyptus rostrata, Pinus radiate and Populus hybridus in the vicinityof a large aluminium smelter in Argentina. Atmos Environ 55:35–42. https://doi.org/10.1016/j.atmosenv.2012.03.026
Sadhu K, Adhikari K, Gangopadhyay A (2012) Effect of mine spoil on native soil of Lower Gondwana coal fields: Raniganj coal mines areas, India. Int J Environ Sci 2:1675–1687. https://doi.org/10.6088/IJES.00202030052
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. Biol Trace Elem Res 148:396–408
Serbula SM, Antonijevic MM, Milosevic NM, Milic SM, Ilic AA (2010) Concentrations of particulate matter and arsenic in Bor (Serbia). J Hazard Mater 181:43–51
Serbula SM, Kalinovic TS, Ilic AA, Kalinovic JV, Steharnik MM (2013) Assessment of airborne heavy metal pollution using Pinus spp. and Tilia spp. Aerosol Air Qual Res 13:563–573. https://doi.org/10.4209/aaqr.2012.06.0153
Serbula SM, Radojevic AA, Kalinovic JV, Kalinovic TS (2014) Indication of airborne pollution by birch and spruce in the vicinity of copper smelter. Environ Sci Pollut Res 21:11510–11520
Serbula SM, Milosavljevic JS, Radojevic AA, Kalinovic JV, Kalinovic TS (2017) Extreme air pollution with contaminants originating from the mining–metallurgical processes. Sci Total Environ 586:1066–1075
Sharma RK, Agrawal M, Marshall FM (2008) Heavy metal (Cu, Zn, Cd and Pb) contamination of vegetables in urban India: a case study in Varanasi. Environ Pollut 154:254–263
Stafilov T, Sajn R, Pancevski Z, Boev B, Frontasyeva MV, Strelkova LP (2010) Heavy metal contamination of topsoils around a lead and zinc smelter in the republic of Macedonia. J Hazard Mater 175:896–914
Stefanowicz AM, Stanek M, Woch MW (2016a) High concentrations of heavy metals in beech forest understory plants growing on waste heaps left by Zn-Pb ore mining. J Geochem Explor 169:157–162. https://doi.org/10.1016/j.gexplo.2016.07.026
Stefanowicz AM, Stanek M, Wock MW, Kapusta P (2016b) The accumulation of elements in plants growing spontaneously on small heaps left by the historical Zn-Pb ore mining. Environ Sci Pollut Res 23:6524–6534
Sun X, Fan D, Liu M, Tian Y, Pang Y, Liao H (2018) Source identification, geochemical normalization and influence factors of heavy metals in Yangtze River Estuary sediment. Environ Pollut 241:938–949
Sung M, Lee CY, Lee SZ (2011) Combined mild soil washing and compost-assisted phytoremediation in treatment of silt loams contaminated with copper, nickel, and chromium. J Hazard Mater 190:744–754
Sungur A, Soylak M, Özcan H (2016) Chemical fractionation, mobility and environmental impacts of heavy metals in greenhouse soils from Çanakkale, Turkey. Environ Earth Sci 75:334. https://doi.org/10.1007/s12665-016-5268-3
The Official Gazette of Republic of Serbia, no. 88/2010: the decree on the soil quality monitoring program using indicators for assessing the risks from the soil degradation as well as the methodology for working out the remediation program (in Serbian)
The Official Gazette of Republic of Serbia (2013) Regulation on the conditions for monitoring and requirements of the air quality. (No 11/10, 75/10, 63/13 (in Serbian))
Tian K, Huang B, Xing Z, Hu W (2017) Geochemical baseline establishment and ecological risk evaluation of heavy metals in greenhouse soils from Dongtai, China. Ecol Indic 72:510–520. https://doi.org/10.1016/j.ecolind.2016.08.037
Tomlinson DL, Wilson JG, Harris CR, Jeffery DW (1980) Problems in the assessment of heavy metals levels in estuaries and the formation of a pollution index. Helgoländer Meeresun 33:566–575. https://doi.org/10.1007/BF02414780
Toselli M, Baldi E, Marcolini G, Malaguti D, Quartieri M, Sorrenti G, Marangoni B (2009) Response of potted grapevines to increasing soil copper concentration. Aust J Grape Wine Res 15:85–92. https://doi.org/10.1111/j.1755-0238.2008.00040.x
Urošević S, Vuković M, Pejčić B, Štrbac N (2018) Mining-metallurgical sources of pollution in eastern Serbia and environmental consciousness. Rev Int Contam Ambie 34:103–115. https://doi.org/10.20937/RICA.2018.34.01.09
USEPA U.S. Environmental Protection Agency (1996) Microwave assisted acid digestion of siliceous and organically based matrices, Method 3052, Office of Solid Waste and Emergency Response, U.S. Government Printing Office, Washington, DC. http://www.epa.gov/osw/hazard/1273 testmethods/sw846/pdfs/3052.pdf
Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17. https://doi.org/10.1007/s10311-009-0268-0
WHO (2007) Guidelines for assessing quality of herbal medicines with reference to contaminants and residues. World Health Organization, Geneva
Wu J, Teng Y, Lu S, Wang Y, Jiao X (2014) Evaluation of soil contamination indices in a mining area of Jiangxi, China. PLoS One 9(11):e112917. https://doi.org/10.1371/journal.pone.0112917
Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464
Yuan G-L, Sun T-H, Han P, Li J, Lang X-X (2014) Source identification and ecological risk assessment of heavy metals in topsoil using environmental geochemical mapping: typical urban renewal area in Beijing, China. J Geochem Explor 136:40–47. https://doi.org/10.1016/j.gexplo.2013.10.002
Zhan HY, Jiang YF, Yuan J, Hu XF, Nartey OD, Wang BL (2014) Trace metal pollution in soil and wild plants from lead–zinc smelting areas in Huixian County, Northwest China. J Geochem Explor 147:182–188. https://doi.org/10.1016/j.gexplo.2014.10.007
Acknowledgments
The authors are grateful to the Ministry of Education, Science and Technological Development of Serbia for the financial support (Project No. III46010, OI172031). We would also like to express gratitude to our late Prof. Dr. Mile Dimitrijević whose guidance and supervision made this work possible.
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Nujkić, M., Milić, S., Spalović, B. et al. Saponaria officinalis L. and Achillea millefolium L. as possible indicators of trace elements pollution caused by mining and metallurgical activities in Bor, Serbia. Environ Sci Pollut Res 27, 44969–44982 (2020). https://doi.org/10.1007/s11356-020-10371-5
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DOI: https://doi.org/10.1007/s11356-020-10371-5