Skip to main content
SpringerLink
Log in

Accumulation of trace elements in Tussilago farfara colonizing post-flotation tailing sites in Serbia

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The purpose of this study was to examine the accumulation potential of spontaneously developed Tussilago farfara populations colonizing sites with different levels of anthropogenic pollution. Physical characteristics of the soil are presented, together with the concentrations of macroelements and microelements (Ca, Mg, Fe, S, Al, Pb, Zn, Cu, Cd, Mn, As, Sb, Ag, Ti, and Sr) in both soil and plants. The biological concentration, accumulation, and translocation factors were used to assess the potential for heavy metal accumulation. Considerable differences were found among assessions from unevenly contaminated habitats, particularly in comparison with an unpolluted site. In line with the ore’s characteristics, substrate samples from polluted sites were heavily contaminated with Pb, Zn, As, and Sb. Increased levels of microelements were also detected in plant samples from flotation tailings. Despite active absorption of Zn, Cu, Cd, Mn, and Sr by the plants from mining sites, the detected quantities of these elements in all samples were below the hyperaccumulation threshold. However, the obtained results indicate that the use of T. farfara from such sites in traditional medicine could pose a risk to human health due to accumulation of several toxic elements in the plant’s aboveground tissues. Additionally, as a successful primary colonizer and stabilizer of technogenic substrates, T. farfara has an important role in the initial phases of revegetation of highly contaminated sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adriano DC (1986) Trace elements in terrestrial environments. Springer, New York

    Google Scholar 

  • Alloway BJ (1995) Heavy metals in soils. Blackie Academic and Professional, Chapman and Hall, London

    Google Scholar 

  • Anonymous (2010) Uredba o programu sistemskog praćenja kvaliteta zemljišta, indikatorima za ocenu rizika od degradacije zemljišta i metodologiji za izradu remedijacionih programa. Služ Glas 88/2010

  • Anonymous (2016) Uredba o utvrđivanju državnog programa sanacije zagađenja Kostajničke reke, Korenite i Jadra usled izlivanja jalovine sa flotacijskih deponija rudnika antimona “Stolice”. Služ Glas 39/2016

  • Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    CAS  Google Scholar 

  • Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc Natl Acad Sci USA 96:3404–3411

    CAS  Google Scholar 

  • Barać N, Škrivanj S, Mutić J, Manojlović D, Bukumirić Z, Živojinović D, Petrović R, Ćorac A (2016) Heavy metals fractionation in agricultural soils of Pb/Zn mining region and their transfer to selected vegetables. Water Air Soil Pollut 227:481

    Google Scholar 

  • Baroni F, Boscagli A, Protano G, Riccobono F (2000) Antimony accumulation in Achillea ageratum, Plantago lanceolata and Silene vulgaris growing in an old Sb-mining area. Environ Pollut 109(2):347–352

    CAS  Google Scholar 

  • Bhattacharya A, Routh J, Jacks G, Bhattacharya P, Mörth M (2006) Environmental assessment of abandoned mine tailings in Adak, Västerbotten district (northern Sweden). Appl Geochem 21(10):1760–1780

    CAS  Google Scholar 

  • Blake RE, Walter LM (1999) Kinetics of feldspar and quartz dissolution at 70–80°C and near-neutral pH: effects of organic acids and NaCl. Geochim Cosmochim Acta 63(13–14):2043–2059

    CAS  Google Scholar 

  • Bradl H (2005) Sources and origins of heavy metals. In: Bradl H (ed) Heavy metals in the environment: origin, interaction and remediation, vol 6. Elsevier, pp 1–27

  • Cabala J, Teper L (2007) Metalliferous constituents of rhizosphere soils contaminated by Zn–Pb mining in southern Poland. Water Air Soil Pollut 178(1–4):351–362

    CAS  Google Scholar 

  • Carvajal M, Alcaraz CF (1998) Why titanium is a beneficial element for plants. J Plant Nutr 21(4):655–664

    CAS  Google Scholar 

  • Conesa HM, Faz Á, Arnaldos R (2007a) Initial studies for the phytostabilization of a mine tailing from the Cartagena-La Union Mining District (SE Spain). Chemosphere 66(1):38–44

    CAS  Google Scholar 

  • Conesa HM, Robinson BH, Schulin R, Nowack B (2007b) Growth of Lygeum spartum in acid mine tailings: response of plants developed from seedlings, rhizomes and at field conditions. Environ Pollut 145(3):700–707

    CAS  Google Scholar 

  • Cui S, Zhou Q, Chao L (2007) Potential hyperaccumulation of Pb, Zn, Cu and Cd in endurant plants distributed in an old smeltery, Northeast China. Environ Geol 51(6):1043–1048

    CAS  Google Scholar 

  • Cvetković V, Šarić K, Pécskay Z, Gerdes A (2016) The Rudnik Mts. Volcano-intrusive complex (Central Serbia): an example of how magmatism controls metallogeny. Geol Croat 69(1):89–100

    Google Scholar 

  • Dahmani-Muller H, Van Oort F, Gelie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109(2):231–238

    CAS  Google Scholar 

  • Dumon JC, Ernst WHO (1988) Titanium in plants. J Plant Physiol 133:203–209

    CAS  Google Scholar 

  • Euro+Med (2006-) Euro+Med PlantBase—the information resource for Euro-Mediterranean plant diversity. http://ww2.bgbm.org/EuroPlusMed/ Accessed 28 July 2019

  • FAO (1974) The Euphrates pilot irrigation project. Methods of soil analysis. Gadeb soil laboratory (a laboratory manual). Food and Agriculture Organization, Rome

    Google Scholar 

  • Fernández-Caliani JC, Barba-Brioso C, González I, Galán E (2009) Heavy metal pollution in soils around the abandoned mine sites of the Iberian Pyrite Belt (Southwest Spain). Water Air Soil Pollut 200(1–4):211–226

    Google Scholar 

  • Filella M, Belzile N, Chen YW (2002) Antimony in the environment: a review focused on natural waters: I. Occurrence. Earth Sci Rev 57(1–2):125–176

    CAS  Google Scholar 

  • Gajić M (1975) Tussilago L. In: Josifović M (ed) Flora SR Srbije, vol 7. SANU, Belgrade, p 130

    Google Scholar 

  • Ghosh J, Midday M, Maity D (2017) Tussilago farfara L., a promising ethnomedicinal plant of Sikkim. Exploratory Anim Med Res 7(1):100–103

    Google Scholar 

  • GISD 2019 Global invasive species database. http://www.issg.org/database Accessed 7 Apr 2019

  • Guan TX, He HB, Zhang XD, Bai Z (2011) Cu fractions, mobility and bioavailability in soil-wheat system after Cu-enriched livestock manure applications. Chemosphere 82(2):215–222

    CAS  Google Scholar 

  • He M (2007) Distribution and phytoavailability of antimony at an antimony mining and smelting area, Hunan, China. Environ Geochem Health 29(3):209–219

    CAS  Google Scholar 

  • Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS version 7.5. http://www.diva-gis.org/ Accessed 10 Apr 2019

  • Horowitz AJ (1991) A primer on sediment-trace element chemistry. Lewis, Chelsea

    Google Scholar 

  • Huang RQ, Gao SF, Wang WL, Staunton S, Wang G (2006) Soil arsenic availability and the transfer of soil arsenic to crops in suburban areas in Fujian Province, Southeast China. Sci Total Environ 368(2–3):531–541

    CAS  Google Scholar 

  • ISO 11261 (1995) Soil quality. Determination of total nitrogen. Modified Kjeldahl method. International Organization for Standardization, Geneva

    Google Scholar 

  • ISO 11466 (1995) Soil quality-extraction of trace elements soluble in aqua regia. International Organization for Standardization, Geneva

    Google Scholar 

  • Janković SR (1990) Rudna ležišta Srbije- regionalni metalogenetski položaj, sredine stvaranja i tipovi ležišta. Republički društveni fond za geološka istraživanja, Beograd

    Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC, Boca Raton

    Google Scholar 

  • Kashem M, Singh B (2001) Metal availability in contaminated soils: I. effect of flooding and organic matter on changes in Eh, pH and solubility of Cd, Ni and Zn. Nutr Cycl Agroecosyst 61(3):247–255

    CAS  Google Scholar 

  • Kříbek B, Majer V, Veselovský F, Nyambe I (2010) Discrimination of lithogenic and anthropogenic sources of metals and sulphur in soils of the central-northern part of the Zambian Copperbelt Mining District: a topsoil vs. subsurface soil concept. J Geochem Explor 104(3):69–86

    Google Scholar 

  • Kulhari A, Sheorayan A, Bajar S, Sarkar S, Chaudhury A, Kalia RK (2013) Investigation of heavy metals in frequently utilized medicinal plants collected from environmentally diverse locations of north western India. SpringerPlus 2(1):676

    Google Scholar 

  • Lehmann C (1997) Clonal diversity of populations of Calamagrostis epigejos in relation to environmental stress and habitat heterogeneity. Ecography 20(5):483–490

    Google Scholar 

  • Lindsay WL (1972) Zinc in soils and plant nutrition. Adv Agron 24:147–186

    CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42(3):421–428

    CAS  Google Scholar 

  • Liu XH, Gao YT, Sardar K, Duan G, Chen AK, Ling L, Zhao L, Liu ZH, Wu XK (2008) Accumulation of Pb, Cu, and Zn in native plants growing on contaminated sites and their potential accumulation capacity in Heqing, Yunnan. J Environ Sci 20:1469–1474

    CAS  Google Scholar 

  • Liu Z, Hamuti A, Abdulla H, Zhang F, Mao X (2016) Accumulation of metallic elements by native species thriving in two mine tailings in Aletai, China. Environ Earth Sci 75(9):781

    Google Scholar 

  • Lorenz K, Lal R (2007) Stabilization of organic carbon in chemically separated pools in reclaimed coal mine soils in Ohio. Geoderma 141(3–4):294–301

    CAS  Google Scholar 

  • Margon A, Mondini C, Valentini M, Ritota M, Leita L (2013) Soil microbial biomass influence on strontium availability in mine soil. Chem Spec Bioavailab 25(2):119–124

    CAS  Google Scholar 

  • McDonald RC, Isbell RF, Speight JG, Walker J, Hopkins MS (1998) Australian soil and land survey field handbook. Australian Collaborative Land Evaluation Program, Canberra

    Google Scholar 

  • McKeague JA (1978) Manual on soil sampling and methods of analysis. Canadian Society of Soil Science, Ottawa

    Google Scholar 

  • Mendez MO, Maier RM (2008) Phytoremediation of mine tailings in temperate and arid environments. Rev Environ Sci Biol 7(1):47–59

    CAS  Google Scholar 

  • Mitsunobu S, Harada T, Takahashi Y (2006) Comparison of antimony behavior with that of arsenic under various soil redox conditions. Environ Sci Technol 40(23):7270–7276

    CAS  Google Scholar 

  • Mudrinić Č (1975) Primary dispersion aureoles of the antimony deposit stolice (Western Serbia). Transactions of the Faculty of Mining and Geology. University of Belgrade, Belgrade

    Google Scholar 

  • Mudrinić Č (1978) Geohemijske karakteristike Sb-As asocijacije u Srpsko-Makedonskoj provinciji. Dissertation, University of Belgrade

  • Myerscough PJ, Whitehead FH (1966) Comparative biology of Tussilago farfara L., Chamaenerion angustifolium (L.) Scop., Epilobium montanum L. and Epilobium adenocaulon Hausskn. New Phytol 65(2):192–210

    Google Scholar 

  • Nan Z, Li J, Zhang J, Cheng G (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285(1–3):187–195

    CAS  Google Scholar 

  • Nedelcheva A, Kostova N, Sidjimov A (2015) Pyrrolizidine alkaloids in Tussilago farfara from Bulgaria. Biotechnol Biotechnol Equip 29(sup1):S1–S7

    CAS  Google Scholar 

  • Olujić J, Karović J (1970-1980) Osnovna geološka karta SFRJ 1:100000, List Višegrad. Savezni geološki zavod, Beograd

  • Osmani M, Bani A, Gjoka F, Pavlova D, Naqellari P, Shahu E, Duka I, Echevarria G (2018) The natural plant colonization of ultramafic post-mining area of Përrenjas, Albania. Period Mineral 87:135–146

    Google Scholar 

  • Papludis AD, Alagić SČ, Milić SM (2018) Manganese in the system soil-plant: phytoremediation aspects. Zašt Mater 59(3):385–393

    Google Scholar 

  • Pequerul A, Pérez C, Madero P, Val J, Monge E (1993) A rapid wet digestion method for plant analysis. In: Fragoso MAC, Van Beusichem ML, Houwers A (eds) Optimization of plant nutrition, Developments in plant and soil sciences, vol 53. Springer, Dordrecht, pp 3–6

    Google Scholar 

  • Pezeshki SR (2001) Wetland plant response to flooding. Environ Exp Bot 46(3):299–312

    Google Scholar 

  • Pichtel J, Kuroiwa K, Sawyerr HT (2000) Distribution of Pb, Cd and Ba in soils and plants of two contaminated sites. Environ Pollut 110(1):171–178

    CAS  Google Scholar 

  • Pugh RE, Dick DG, Fredeen AL (2002) Heavy metal (Pb, Zn, Cd, Fe, and Cu) contents of plant foliage near the Anvil Range lead/zinc mine, Faro, Yukon Territory. Ecotoxicol Environ Safe 52(3):273–279

    CAS  Google Scholar 

  • Qi C, Wu F, Deng Q, Liu G, Mo C, Liu B, Zhu J (2011) Distribution and accumulation of antimony in plants in the super-large Sb deposit areas, China. Microchem J 97(1):44–51

    CAS  Google Scholar 

  • Radosavljević SA, Stojanović JN, Radosavljević-Mihajlović AS, Kašić VD (2013) Polymetallic mineralization of the Boranja orefield, Podrinje Metallogenic District, Serbia: zonality, mineral associations and genetic features. Period Mineral 82(1):61–87

    Google Scholar 

  • Ranđelović D, Jakovljević K, Mihailović N, Jovanović S (2018) Metal accumulation in populations of Calamagrostis epigejos (L.) Roth from diverse anthropogenically degraded sites (SE Europe, Serbia). Environ Monit Assess 190(4):183

    Google Scholar 

  • Rengel Z (2015) Availability of Mn, Zn and Fe in the rhizosphere. J Soil Sci Plant Nutr 15(2):397–409

    CAS  Google Scholar 

  • Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168(2):305–312

    CAS  Google Scholar 

  • Rieuwerts J, Thornton I, Farago M, Ashmore M (1998) Quantifying the influence of soil properties on the solubility of metals by predictive modelling of secondary data. Chem Spec Bioavailab 10(3):83–94

    CAS  Google Scholar 

  • Rodríguez L, Ruiz E, Alonso-Azcárate J, Rincón J (2009) Heavy metal distribution and chemical speciation in tailings and soils around a Pb–Zn mine in Spain. J Environ Manag 90(2):1106–1116

    Google Scholar 

  • Sasmaz A, Sasmaz M (2009) The phytoremediation potential for strontium of indigenous plants growing in a mining area. Environ Exp Bot 67(1):139–144

    CAS  Google Scholar 

  • Shacklette HT, Erdman JA, Harms TF (1978) Trace elements in plant foodstuffs. In: Oehme FM (ed) Toxicity of heavy metals in the environments, part I. Marcel Dekker, New York, p 25

    Google Scholar 

  • Shi X, Zhang X, Chen G, Chen Y, Wang L, Shan X (2011) Seedling growth and metal accumulation of selected woody species in copper and lead/zinc mine tailings. J Environ Sci 23(2):266–274

    CAS  Google Scholar 

  • Stefanowicz AM, Kapusta P, Błońska A, Kompała-Bąba A, Woźniak G (2015) Effects of Calamagrostis epigejos, Chamaenerion palustre and Tussilago farfara on nutrient availability and microbial activity in the surface layer of spoil heaps after hard coal mining. Ecol Eng 83:328–337

    Google Scholar 

  • Stojanović JN, Radosavljević-Mihajlović AS, Radosavljević SA, Vuković NS, Pačevski AM (2016) Mineralogy and genetic characteristics of the Rudnik Pb-Zn/Cu, Ag, Bi,W polymetallic deposit (Central Serbia)—new occurrence of Pb(Ag) Bi sulfosalts. Period Mineral 85:121–135

    Google Scholar 

  • Stoltz E, Greger M (2002) Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environ Exp Bot 47(3):271–280

    CAS  Google Scholar 

  • Thiers B (2019) Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ih (continuously updated) Accessed 2 Apr 2019

  • Ullrich SM, Ramsey MH, Helios-Rybicka E (1999) Total and exchangeable concentrations of heavy metals in soils near Bytom, an area of Pb/Zn mining and smelting in Upper Silesia, Poland. Appl Geochem 14(2):187–196

    CAS  Google Scholar 

  • Uminska R (1993) Cadmium contents of cultivated soils exposed to contamination in Poland. Environ Geochem Health 15:15–19

    CAS  Google Scholar 

  • Vaculík M, Jurkovič Ľ, Matejkovič P, Molnárová M, Lux A (2013) Potential risk of arsenic and antimony accumulation by medicinal plants naturally growing on old mining sites. Water Air Soil Pollut 224(5):1546

    Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Google Scholar 

  • van Reeuwijk LP (ed) (1995) Procedures for soil analysis, technical paper 8, 5th edn. International Soil Reference and Information Centre, Wageningen

    Google Scholar 

  • Walker DJ, Bernal MP (2008) The effects of olive mill waste compost and poultry manure on the availability and plant uptake of nutrients in a highly saline soil. Bioresour Technol 99(2):396–403

    CAS  Google Scholar 

  • Wong JWC, Ip CM, Wong MH (1998) Acid-forming capacity of lead–zinc mine tailings and its implications for mine rehabilitation. Environ Geochem Health 20(3):149–155

    CAS  Google Scholar 

  • Yanqun Z, Yuan L, Schvartz C, Langlade L, Fan L (2004) Accumulation of Pb, Cd, Cu and Zn in plants and hyperaccumulator choice in Lanping lead–zinc mine area, China. Environ Int 30(4):567–576

    Google Scholar 

  • 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(2–3):456–464

    CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Mr. Raymond Dooley for the linguistic editing.

Funding

The Ministry of Education, Science and Technological Development of the Republic of Serbia supported this research through grants 173030, 176016, and 172019.

Author information

Authors and Affiliations

  1. Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade, Belgrade, 11000, Serbia

    Ksenija Jakovljević, Tomica Mišljenović & Slobodan Jovanović

  2. Vinča Institute of Nuclear Sciences, University of Belgrade, Belgrade, 11000, Serbia

    Jelena Savović

  3. Faculty of Physical Chemistry, University of Belgrade, Belgrade, 11000, Serbia

    Dragan Ranković

  4. Institute for Technology of Nuclear and other Mineral Raw Materials, Belgrade, 11000, Serbia

    Dragana Ranđelović

  5. Institute for the Application of Nuclear Energy (INEP), University of Belgrade, Belgrade, 11080, Serbia

    Nevena Mihailović

Authors
  1. Ksenija Jakovljević
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomica Mišljenović
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jelena Savović
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dragan Ranković
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dragana Ranđelović
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nevena Mihailović
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Slobodan Jovanović
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ksenija Jakovljević.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jakovljević, K., Mišljenović, T., Savović, J. et al. Accumulation of trace elements in Tussilago farfara colonizing post-flotation tailing sites in Serbia. Environ Sci Pollut Res 27, 4089–4103 (2020). https://doi.org/10.1007/s11356-019-07010-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-07010-z

Keywords

Search

Navigation