Assessment of As, Cd, Cu, Fe, Pb, and Zn concentrations in soil and parts of Rosa spp. sampled in extremely polluted environment

  • Jelena V. Kalinovic
  • Snezana M. SerbulaEmail author
  • Ana A. Radojevic
  • Jelena S. Milosavljevic
  • Tanja S. Kalinovic
  • Mirjana M. Steharnik


This research was conducted in order to determine As, Cd, Cu, Fe, Pb, and Zn concentrations in soil and parts of wild rose (Rosa spp., predominantly Rosa canina L.) in the Bor area, known for more than 100 years of mining and pyrometallurgical production of copper, as well as to determine the possibility of its usage as an environmental indicator or for phytoremediation. The results showed that the sampled soils were highly contaminated with As and Cu, since the obtained concentrations exceeded the corresponding limit and remediation values. The soil samples from the sites which were closest to the Mining-Metallurgical Complex or in the prevailing wind directions were most enriched with the analyzed elements. According to the element analysis in the parts of Rosa spp., branches, leaves, and roots contained higher concentrations of the studied elements than the fruits. Based on the values of the biological factors, it can be concluded that Rosa spp. restricted the absorption of the elements from the soil. Since the absorption rates from soil to roots were low for all the studied elements, Rosa spp. was not suitable for the phytoextraction or phytostabilization. Statistically significant positive correlations of the elements in the soil and parts of Rosa spp. indicated their anthropogenic origin. Differences in the element concentrations in the plant parts and the soil samples from the background and the sites which were under the influence of the emissions from the Mining–Metallurgical Complex indicated that Rosa spp. had a potential for usage in biomonitoring.


Environmental pollution Copper smelter Rosehips Rosa spp. Biomonitoring Biological factors 



Our thanks go to English language teacher Mara Manzalovic fromTechnical Faculty in Bor (University of Belgrade) for providing language help.

Funding information

This study was financially supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Projects No. 46010 and 33038).

Supplementary material

10661_2018_7134_MOESM1_ESM.doc (364 kb)
ESM 1 (DOC 364 kb)


  1. Angelov, G., Boyadzhieva, S. S., & Georgieva, S. S. (2014). Rosehip extraction: Process optimization and antioxidant capacity of extracts. Central European Journal of Chemistry, 12(4), 502–508.CrossRefGoogle Scholar
  2. Baker, A. J. M. (1981). Accumulators and excluders – Strategies in the response of plant to heavy metals. Journal of Plant Nutrition, 3(1–4), 643–654.CrossRefGoogle Scholar
  3. Başgel, S., & Erdemoğlu, S. B. (2006). Determination of mineral and trace elements in some medicinal herbs and their infusions consumed in Turkey. Science of the Total Environment, 359, 82–89.CrossRefGoogle Scholar
  4. Bravo, S., Amorós, J. A., Pérez-de-los-Reyes, C., García, F. J., Moreno, M. M., Sánchez-Ormeño, M., & Higueras, P. (2017). Influence of the soil pH in the uptake and bioaccumulation of heavy metals (Fe, Zn, Cu, Pb and Mn) and other elements (Ca, K, Al, Sr and Ba) in vine leaves, Castilla-La Mancha (Spain). Journal of Geochemical Exploration, 174, 79–83.Google Scholar
  5. Christou, A., Theologides, C. P., Costa, C., Kalavrouziotis, I. K., & Varnavas, S. P. (2017). Assessment of toxic heavy metals concentrations in soils and wild and cultivated plant species in Limni abandoned copper mining site, Cyprus. Journal of Geochemical Exploration, 178, 16–22.CrossRefGoogle Scholar
  6. da Silva, W. R., da Silva, F. B. V., Araújo, P. R. M., & do Nascimento, C. W. A. (2017). Assessing human health risks and strategies for phytoremediation in soils contaminated with As, Cd, Pb, and Zn by slag disposal. Ecotoxicology and Environmental Safety, 144, 522–530.Google Scholar
  7. Damascos, M. A., Arribere, M., Svriz, M., & Bran, D. (2008). Fruit mineral contents of six wild species of the north Andean Patagonia, Argentina. Biological Trace Element Research, 125, 72–80.CrossRefGoogle Scholar
  8. Demir, F., & Özcan, M. (2001). Chemical and technological properties of rose (Rosa canina L.) fruits grown wild in Turkey. Journal of Food Engineering, 47, 333–336.CrossRefGoogle Scholar
  9. Desideri, D., Meli, M. A., & Roselli, C. (2010). Determination of essential and non-essential elements in some medicinal plants by polarised X ray fluorescence spectrometer (EDPXRF). Microchemical Journal, 95, 174–180.CrossRefGoogle Scholar
  10. Enuneku, A., Biose, E., & Ezemonye, L. (2017). Levels, distribution, characterization and ecological risk assessment of heavy metals in road side soils and earthworms from urban high traffic areas in Benin metropolis, southern Nigeria. Journal of Environmental Chemical Engineering, 5, 2773–2781.CrossRefGoogle Scholar
  11. Ercisli, S. (2005). Rose (Rosa spp.) germplasm resources of Turkey. Genetic Resources and Crop Evolution, 52, 787–795.CrossRefGoogle Scholar
  12. Ercisli, S. (2007). Chemical composition of fruits in some rose (Rosa spp.) species. Food Chemistry, 104, 1379–1384.CrossRefGoogle Scholar
  13. Favas, P. J. C., Pratas, J., & Prasad, M. N. V. (2013). Temporal variation in the arsenic and metal accumulation in the maritime pine tree grown on contaminated soils. International journal of Environmental Science and Technology, 10, 809–826.CrossRefGoogle Scholar
  14. Figurska-Ciura, D., Bronkowska, M., Orzeł, D., Styczyńska, M., Wyka, J., Łoźna, K., Biernat, J., & Żechałko-Czajkowska, A. (2010). Cadmium content in plant products cultivated near a copperworks. Polish Journal of Environmental Studies, 19(6), 1383–1390.Google Scholar
  15. Gentscheva, G. D., Stafilov, T., & Ivanova, E. H. (2010). Determination of some essential and toxic elements in herbs from Bulgaria and Macedonia using atomic spectrometry. Eurasian Journal of Analytical Chemistry, 5(2), 104–111.Google Scholar
  16. Ghaderian, S. M., & Ravandi, A. A. G. (2012). Accumulation of copper and other heavy metals by plants growing on Sarcheshmeh copper mining area, Iran. Journal of Geochemical Exploration, 123, 25–32.CrossRefGoogle Scholar
  17. Hamurcu, M., Özcan, M. M., Dursun, N., & Gezgin, S. (2010). Mineral and heavy metal levels of some fruits grown at the roadsides. Food and Chemical Toxicology, 48, 1767–1770.CrossRefGoogle Scholar
  18. IARC Monographs. (2012). Arsenic, metals, fibres, and dusts volume 100 C. a review of human carcinogens. IARC monographs on the evaluation of carcinogenic risks to humans. Lyon: International Agency for Research on Cancer.Google Scholar
  19. ISO, International Standard (2005). ISO 10390:2005. Soil quality: Determination of pH, Geneva.Google Scholar
  20. Kabata-Pendias, A. (2011). Trace Elements in Soils and Plants (4th ed.). Boca Raton: CRC Press.Google Scholar
  21. Kabata-Pendias, A., & Mukherjee, A. B. (2007). Trace elements from soil to human. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  22. Kabata-Pendias, A., & Pendias, H. (2001). Trace Elements in Soil and Plants (3rd ed.). Boca Raton: CRC Press.Google Scholar
  23. Kader, M., Lamb, D.T., Wang, L., Megharaj, M., Naidu, R. (2017). Zinc-arsenic interactions in soil: Solubility, toxicity and uptake. Chemosphere, 187, 357–367.Google Scholar
  24. Kader, M., Lamb, D. T., Wang, L., Megharaj, M., & Naidu, R. (2018). Copper interactions on arsenic bioavailability and phytotoxicity in soil. Ecotoxicology and Environmental Safety, 148, 738–746.Google Scholar
  25. Kalinovic, T. S., Serbula, S. M., Radojevic, A. A., Kalinovic, J. V., Steharnik, M. M., & Petrovic, J. V. (2016). Elder, linden and pine biomonitoring ability of pollution emitted from the copper smelter and the tailings ponds. Geoderma, 262, 266–275.CrossRefGoogle Scholar
  26. Kalinovic, T. S., Serbula, S. M., Kalinovic, J. V., Radojevic, A. A., Petrovic, J. V., Steharnik, M. M., & Milosavljevic, J. S. (2017). Suitability of linden and elder in the assessment of environmental pollution of Brestovac spa and Bor lake (Serbia). Environmental Earth Sciences, 76(4), 178.CrossRefGoogle Scholar
  27. Kalra, Y. P. (1998). Handbook of reference methods for plant analysis. Boca Raton: CRC Press.Google Scholar
  28. Kara, D. (2009). Evaluation of trace metal concentrations in some herbs and herbal teas by principal component analysis. Food Chemistry, 114, 347–354.CrossRefGoogle Scholar
  29. Koz, B., Cevik, U., & Akbulut, S. (2012). Heavy metal analysis around Murgul (Artvin) copper mining area of Turkey using moss and soil. Ecological Indicators, 20, 17–23.CrossRefGoogle Scholar
  30. Kwiatkowska-Malina, J. (2018). Functions of organic matter in polluted soils: The effect of organic amendments on phytoavailability of heavy metals. Applied Soil Ecology, 123, 542–545.CrossRefGoogle Scholar
  31. Malik, J., Frankova, A., Drabek, O., Szakova, J., Ash, C., & Kokoska, L. (2013). Aluminium and other elements in selected herbal tea plant species and their infusions. Food Chemistry, 139, 728–734.CrossRefGoogle Scholar
  32. Mao, Y., Sang, S., Liu, S., & Jia, J. (2014). Spatial distribution of pH and organic matter in urban soils and its implications on site-specific land uses in Xuzhou, China. Comptes Rendus Biologies, 337, 332–337.CrossRefGoogle Scholar
  33. Marbaniang, D., & Chaturvedi, S. S. (2014). Assessment on Cr, Cd, As, Ni and Pb uptake and phyremediation potential of Scirpus mucronatus. International Journal of scientific research and management (IJSRM), 2(6), 965–969.Google Scholar
  34. McCauley, A., Jones, C., & Olson-Rutz, K. (2017). Soil pH and organic matter. Nutrient management module No. 8. Bozeman: Montana State University.Google Scholar
  35. Mendoza, R. E., García, I. V., de Cabo, L., Weigandt, C. F., & de Iorio, A. F. (2015). The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River basin (Argentina). Science of the Total Environment, 505, 555–564.CrossRefGoogle Scholar
  36. Mingorance, M. D., Valdés, B., & Oliva, S. R. (2007). Strategies of heavy metal uptake by plants growing under industrial emissions. Environment International, 33, 514–520.CrossRefGoogle Scholar
  37. Munson, R. D. (1998). Principles of plant analysis. In Y. P. Kalra (Ed.), Handbook of reference methods for plant analysis (pp. 1–24). Boca Raton: CRC Press.Google Scholar
  38. Nagaraju, A., & Karimulla, S. (2002). Accumulation of elements in plants and soils in and around Nellere mica belt, Andhra Pradesh, India – A biogeochemical study. Environmental Geology, 41, 852–860.CrossRefGoogle Scholar
  39. Nouri, J., Lorestani, B., Yousefi, N., Khorasani, N., Hasani, A. H., Seif, F., & Cheraghi, M. (2011). Phytoremediation potential of native plants grown in the vicinity of Ahangaran lead–zinc mine (Hamedan, Iran). Environmental Earth Sciences, 62, 639–644.CrossRefGoogle Scholar
  40. Özcan, M. M., Ünver, A., Uçar, T., & Arslan, D. (2008). Mineral content of some herbs and herbal teas by infusion and decoction. Food Chemistry, 106, 1120–1127.CrossRefGoogle Scholar
  41. Petrova, S., Yurukova, L., & Velcheva, I. (2014). Possibilities of using deciduous tree species in trace element biomonitoring in an urban area (Plovdiv, Bulgaria). Atmospheric Pollution Research, 5, 196–202.CrossRefGoogle Scholar
  42. Radojevic, A. A., Serbula, S. M., Kalinovic, T. S., Kalinovic, J. V., Steharnik, M. M., Petrovic, J. V., & Milosavljevic, J. S. (2017). Metal/metalloid content in plant parts and soils of Corylus spp. influenced by mining–metallurgical production of copper. Environmental Science and Pollution Research, 24, 10326–10340.CrossRefGoogle Scholar
  43. Reglero, M. M., Monsalve-González, L., Taggart, M. A., & Mateo, R. (2008). Transfer of metals to plants and red deer in an old lead mining area in Spain. Science of the Total Environment, 406, 287–297.CrossRefGoogle Scholar
  44. Regulation No. 88/10 (2010). The official gazette of republic of Serbia, no. 88/2010: The soil quality monitoring programme using indicators for assessing the risks from the soil degradation as well as the methodology for working out the remediation programme (in Serbian).Google Scholar
  45. Sekeroglu, N., Ozkutlu, F., Kara, M., & Ozguven, M. (2008). Determination of cadmium and selected micronutrients in commonly used and traded medicinal plants in Turkey. Journal of the Science of Food and Agriculture, 88, 86–90.CrossRefGoogle Scholar
  46. Serbula, S. M., Miljkovic, D. D., Kovacevic, R. M., & Ilic, A. A. (2012). Assessment of airborne heavy metal pollution using plant parts and topsoil. Ecotoxicology and Environmental Safety, 76, 209–214.CrossRefGoogle Scholar
  47. Serbula, S. M., Kalinovic, T. S., Ilic, A. A., Kalinovic, J. V., & Steharnik, M. M. (2013a). Assessment of airborne heavy metal pollution using Pinus spp. and Tilia spp. Aerosol and Air Quality Research, 13(2), 563–573.CrossRefGoogle Scholar
  48. Serbula, S. M., Kalinovic, T. S., Kalinovic, J. V., & Ilic, A. A. (2013b). Exceedance of air quality standards resulting from pyro-metallurgical production of copper: A case study, Bor (eastern Serbia). Environmental Earth Sciences, 68(7), 1989–1998.CrossRefGoogle Scholar
  49. Serbula, S. M., Ilic, A. A., Kalinovic, J. V., Kalinovic, T. S., & Petrovic, N. B. (2014). Assessment of air pollution originating from copper smelter in Bor (Serbia). Environmental Earth Sciences, 71, 1651–1661.CrossRefGoogle Scholar
  50. Serbula, S. M., Milosavljevic, J. S., Radojevic, A. A., Kalinovic, J. V., & Kalinovic, T. S. (2017). Extreme air pollution with contaminants originating from the mining–metallurgical processes. Science of the Total Environment, 586, 1066–1075.CrossRefGoogle Scholar
  51. Shiyab, S. (2018). Phytoaccumulation of copper from irrigationwater and its effect on the internal structure of lettuce. Agriculture, 8(2), 29.CrossRefGoogle Scholar
  52. Tokalıoğlu, Ş. (2012). Determination of trace elements in commonly consumed medicinal herbs by ICP-MS and multivariate analysis. Food Chemistry, 134, 2504–2508.CrossRefGoogle Scholar
  53. U.S. EPA. (1996). Acid digestion of sediments, sludges, and solids (3050B). Washington: United States Environmental Protection Agency.Google Scholar
  54. U.S. EPA. (2000). Abandoned mine site characterization and cleanup handbook. Contributor: Nick Ceto, Shahid Mahmud. Region 10. Seattle: United States Environmental Protection Agency.Google Scholar
  55. USDA. (1996). Soil quality information sheet, Soil quality indicators: Organic matter. Washington D.C.: United States Department of Agriculture (USDA), Natural Resources Conservation Service (NRCS).Google Scholar
  56. USDA. (1998). Soil quality information sheet, Soil quality indicators: pH. Washington D.C.: United States Department of Agriculture (USDA), Natural Resources Conservation Service (NRCS).Google Scholar
  57. Vural, A. (2015). Biogeochemical characteristics of Rosa canina grown in hydrothermally contaminated soils of the Gümüşhane Province, Northeast Turkey. Environmental Monitoring and Assessment, 187, 486.CrossRefGoogle Scholar
  58. WHO. (2007). WHO guidelines for assessing quality of herbal medicines with reference to contaminants and residues. Geneva: World Health Organization.Google Scholar
  59. Xiao, R., Wang, S., Li, R., Wang, J. J., & Zhang, Z. (2017). Soil heavy metal contamination and health risks associated with artisanal gold mining in Tongguan, Shaanxi, China. Ecotoxicology and Environmental Safety, 141, 17–24.CrossRefGoogle Scholar
  60. Živkov–Baloš, M., Mihaljev, Ž., Ćupić, Ž., Jakšić, S., Apić, J., Ljubojević, D., & Prica, N. (2014). Determination of some essential elements in herbal teas from Serbia using atomic spectrometry (AAS). Savremena Poljoprivreda, 63(4–5), 394–402.Google Scholar
  61. Zseni, A., Goldie, H., & Bárány-Kevei, I. (2003). Limestone pavements in Great Britain and the role of soil cover in their evolution. Acta Carsologica, 32/1(5), 57–67.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Jelena V. Kalinovic
    • 1
  • Snezana M. Serbula
    • 1
    Email author
  • Ana A. Radojevic
    • 1
  • Jelena S. Milosavljevic
    • 1
  • Tanja S. Kalinovic
    • 1
  • Mirjana M. Steharnik
    • 2
  1. 1.University of Belgrade, Technical Faculty in BorBorSerbia
  2. 2.Mining and Metallurgy Institute BorBorSerbia

Personalised recommendations