Advertisement

Metal accumulation in populations of Calamagrostis epigejos (L.) Roth from diverse anthropogenically degraded sites (SE Europe, Serbia)

  • Dragana Ranđelović
  • Ksenija Jakovljević
  • Nevena Mihailović
  • Slobodan Jovanović
Article

Abstract

Heavy metal accumulation is recognized as a very important global pollution problem in the last decades. Plant species have been recognized as natural bioindicators of environmental pollution, especially the amount of heavy metals in soils. Moreover, only a limited number of plant species can survive in highly contaminated soils. It is also known that metal accumulation can vary greatly among different populations of the same species. This study examines the chemical composition and accumulation potential of the expansive clonal grass Calamagrostis epigejos at five localities exposed to different levels of anthropogenic pressure. Considerable differences were observed between uptake, translocation, and accumulation of total and available heavy metals, such differences corresponding to soil physico-chemical characteristics and the level of site pollution. The results indicate that Calamagrostis epigejos uptakes a significant portion of the available fraction of heavy metals in the soil and stores it in the roots, thereby exhibiting a certain potential for metal phytostabilization.

Keywords

Heavy metal Anthropogenic pollution Uptake Phytoremediation 

Notes

Acknowledgements

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

Funding Information

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

References

  1. Aiken, S. G., Dore, W. G., Lefkovitch, L. P., & Armstrong, K. C. (1989). Calamagrostis epigejos (Poaceae) in North America, especially Ontario. Canadian Journal of Botany, 67(11), 3205–3321.  https://doi.org/10.1139/b89-400.CrossRefGoogle Scholar
  2. Alloway, B.J. (2013). Heavy Metals in Soils–Trace Metals and Metalloids in Soils and Their Bioavailability. Springer; Dordrecht, The Netherlands.Google Scholar
  3. Alloway, B. J. (1995). Heavy metals in soils. London: Chapman & Hall.  https://doi.org/10.1007/978-94-011-1344-1.CrossRefGoogle Scholar
  4. Al-Wabel, M. I., Sallam, A. E. A. S., Usman, A. R., Ahmad, M., El-Naggar, A. H., El-Saeid, M. H., Al-Faraj, A., El-Enazi, K., & Al-Romian, F. A. (2017). Trace metal levels, sources, and ecological risk assessment in a densely agricultural area from Saudi Arabia. Environmental Monitoring and Assessment, 189(6), 252.  https://doi.org/10.1007/s10661-017-5919-1.CrossRefGoogle Scholar
  5. Antonijević, M. M., Dimitrijević, M. D., Milić, S. M., & Nujkić, M. 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). Journal of Environmental Monitoring, 14(3), 866–877.  https://doi.org/10.1039/c2em10803h.CrossRefGoogle Scholar
  6. Ashraf, M. A., Maah, M. J., & Yusoff, I. (2011). Heavy metals accumulation in plants growing in ex tin mining catchment. International Journal of Environmental Science & Technology, 8(2), 401–416.  https://doi.org/10.1007/BF03326227.CrossRefGoogle Scholar
  7. Baumeister, W., & Ernst, W. H. O. (1978). Mineralstoffe und Pflanzenwachstum. Stuttgart: G Fischer.Google Scholar
  8. Bert, V., Lors, C., Ponge, J. F., Caron, L., Biaz, A., Dazy, M., & Masfaraud, J. F. (2012). Metal immobilization and soil amendment efficiency at a contaminated sediment landfill site: a field study focusing on plants, springtails, and bacteria. Environmental Pollution, 169, 1–11.  https://doi.org/10.1016/j.envpol.2012.04.021.CrossRefGoogle Scholar
  9. Bloemen, M. L., Markert, B., & Lieth, H. (1995). The distribution of Cd, Cu, Pb and Zn in topsoils of Osnabrück in relation to land use. Science of the Total Environment, 166(1), 137–148.  https://doi.org/10.1016/0048-9697(95)04520-B.CrossRefGoogle Scholar
  10. Bose, S., & Bhattacharyya, A. K. (2008). Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere, 70(7), 1264–1272.  https://doi.org/10.1016/j.chemosphere.2007.07.062.CrossRefGoogle Scholar
  11. Bryndová, I., & Kovář, P. (2004). Dynamics of the demographic parameters of the clonal plant Calamagrostis epigejos (L.) Roth in two kinds of industrial deposits (abandoned sedimentation basins in Bukovina and Chvaletice). In P. Kovář (Ed.), Natural recovery of human-made deposits in landscape (biotic interactions and ore/ash-slag artificial ecosystems) (pp. 267–276). Prague: Academia.Google Scholar
  12. Chen, T. B., Zheng, Y. M., Lei, M., Huang, Z. C., Wu, H. T., Chen, H., Fan, K. K., Yu, K., Wu, X., & Tian, Q. Z. (2005). Assessment of heavy metal pollution in surface soils of urban parks in Beijing, China. Chemosphere, 60(4), 542–551.  https://doi.org/10.1016/j.chemosphere.2004.12.072.CrossRefGoogle Scholar
  13. Davies, B. E. (1995). Lead. In B. J. Alloway (Ed.), Heavy metals in soils (pp. 206–223). London: Blackie Academic.  https://doi.org/10.1007/978-94-011-1344-1_9.CrossRefGoogle Scholar
  14. Drakatos, P. A., Kalavrouziotis, I. K., Hortis, T. C., Varnanas, S. P., Drakatos, S. P., Bladenopoulou, S., & Fanariotou, I. N. (2002). Antagonistic action of Fe and Mn in Mediterranean-type plants irrigated with wastewater effluents following biological treatment. International Journal of Environmental Studies, 59(1), 125–132.  https://doi.org/10.1080/00207230211961.CrossRefGoogle Scholar
  15. Dudka, S., & Adriano, D. C. (1997). Environmental impacts of metal ore mining and processing: a review. Journal of Environmental Quality, 26(3), 590–602.  https://doi.org/10.2134/jeq1997.00472425002600030003x.CrossRefGoogle Scholar
  16. Dukić, D. (1960). Reke Beograda i njegove okoline (the rivers of Belgrade and its surroundings). Zbornik Radova Geografskog Instituta, 17, 151–163 (In Serbian).Google Scholar
  17. Ebbs, S. D., & Kochian, L. V. (1997). Toxicity of zinc and copper to Brassica species: implications for phytoremediation. Journal of Environmental Quality, 26(3), 776–781.  https://doi.org/10.2134/jeq1997.00472425002600030026x.CrossRefGoogle Scholar
  18. Eisenhauer, N., Beßler, H., Engels, C., Gleixner, G., Habekost, M., Milcu, A., Partsch, S., Sabais, A. C. W., Scherber, C., Steinbeiss, S., Weigelt, A., Weisser, W. W., & Scheu, S. (2010). Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology, 91(2), 485–496.  https://doi.org/10.1890/08-2338.1.CrossRefGoogle Scholar
  19. Elhottová, D., Krištufek, V., Malý, S., & Frouz, J. (2009). Rhizosphere effect of colonizer plant species on the development of soil microbial community during primary succession on postmining sites. Communications in Soil Science and Plant Analysis, 40(1-6), 758–770.  https://doi.org/10.1080/00103620802693193.CrossRefGoogle Scholar
  20. Ellenberg, H., Weber, H. E., Düll, R., Wirth, V., Werner, W., & Paulissen, D. (1991). Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica 18. Göttingen: Erich Goltze.Google Scholar
  21. FAO. (1974). The Euphrates pilot irrigation project. Methods of soil analysis. Gadeb soil laboratory (a laboratory manual). Rome: Food and Agriculture Organization.Google Scholar
  22. Gajić, G., Pavlović, P., Kostić, O., Jarić, S., Đurđević, L., Pavlović, D., & Mitrović, M. (2013). Ecophysiological and biochemical traits of three herbaceous plants growing on the disposed coal combustion fly ash of different weathering stage. Archives of Biological Sciences, 65(4), 1651–1667.  https://doi.org/10.2298/ABS1304651G.CrossRefGoogle Scholar
  23. Greger, M. (2004). Metal availability, uptake, transport and accumulation in plants. In M. N. Prasad & J. Hagemeyer (Eds.), Heavy metal stress in plants (pp. 1–27). Berlin: Springer.  https://doi.org/10.1007/978-3-662-07743-6_1.Google Scholar
  24. ISO 11047 (1998). Soil quality—determination of cadmium, chromium, cobalt, copper, lead, manganese, nickel and zinc—flame and electrothermal atomic absorption spectrometric methods. Geneva: International Organization for Standardization.Google Scholar
  25. ISO 11261 (1995). Soil quality. Determination of total nitrogen. Modified Kjeldahl method. Geneva: International Organization for Standardization.Google Scholar
  26. ISO 11466. (1995). Soil quality-extraction of trace elements soluble in aqua regia. Geneva: International Organization for Standardization.Google Scholar
  27. Izaguirre-Mayoral, M. L., & Sinclair, T. R. (2005). Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. Annals of Botany, 96(1), 149–158.  https://doi.org/10.1093/aob/mci160.CrossRefGoogle Scholar
  28. Jelenković, R., Milovanović, D., Koželj, D., & Banješević, M. (2016). The mineral resources of the Bor metallogenic zone: a review. Geologia Croatica, 69(1), 143–155.  https://doi.org/10.4154/GC.2016.11.CrossRefGoogle Scholar
  29. John, M. K. (1976). Interelationships between plant cadmium and uptake of some other elements from culture solutions by oats and lettuce. Environmental Pollution, 11(2), 85–95.  https://doi.org/10.1016/0013-9327(76)90021-5.CrossRefGoogle Scholar
  30. Kabata-Pendias, A. (2011). Trace elements in soils and plants. Boca Raton: CRC Press, Taylor & Francis Group.Google Scholar
  31. Koronatova, N. G., & Milyaeva, E. V. (2011). Plant community succession in post-mined quarries in the northern-taiga zone of West Siberia. Contemporary Problems of Ecology, 4(5), 513–518.  https://doi.org/10.1134/S1995425511050109.CrossRefGoogle Scholar
  32. Kovář, P., Štěpánek, J., Kirschner, J. (2004). Clonal diversity of Calamagrostis epigejos (L.) Roth in relation to type of industrial substrate and successional stage. In: Kovář P. (ed.): Natural Recovery of Human-Made Deposits in Landscape (Biotic Interactions and Ore/Ash-Slag Artificial Ecosystems), 285–293.Google Scholar
  33. Lehmann, C. (1997). Clonal diversity of populations of Calamagrostis epigejos in relation to environmental stress and habitat heterogeneity. Ecography, 20(5), 483–490.  https://doi.org/10.1111/j.1600-0587.1997.tb00416.x.CrossRefGoogle Scholar
  34. Lehmann, C., & Rebele, F. (2004a). Evaluation of heavy metal tolerance in Calamagrostis epigejos and Elymus repens revealed copper tolerance in a copper smelter population of C. epigejos. Environmental and Experimental Botany, 51(3), 199–213.  https://doi.org/10.1016/j.envexpbot.2003.10.002.CrossRefGoogle Scholar
  35. Lehmann, C., & Rebele, F. (2004b). Assessing the potential for cadmium phytoremediation with Calamagrostis epigejos: a pot experiment. International Journal of Phytoremediation, 6(2), 169–183.  https://doi.org/10.1080/16226510490454849.CrossRefGoogle Scholar
  36. Lehmann, C., & Rebele, F. (2005). Phenotypic plasticity in Calamagrostis epigejos (Poaceae): response capacities of genotypes from different populations of contrasting habitats to a range of soil fertility. Acta Oecologica, 28(2), 127–140.  https://doi.org/10.1016/j.actao.2005.03.005.CrossRefGoogle Scholar
  37. Lindsay, W. L., & Norvell, W. A. (1978). Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Science Society of America Journal, 42(3), 421–428.  https://doi.org/10.2136/sssaj1978.03615995004200030009x.CrossRefGoogle Scholar
  38. Lux, A., Martinka, M., Vaculík, M., & White, P. J. (2010). Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany, 62(1), 21–37.  https://doi.org/10.1093/jxb/erq281.CrossRefGoogle Scholar
  39. Malcová, R., Albrechtová, J., & Vosátka, M. (2001). The role of the extraradical mycelium network of arbuscular mycorrhizal fungi on the establishment and growth of Calamagrostis epigejos in industrial waste substrates. Applied Soil Ecology, 18(2), 129–142.  https://doi.org/10.1016/S0929-1393(01)00156-1.CrossRefGoogle Scholar
  40. Mattina, M. I., Lannucci-Berger, W., Musante, C., & White, J. C. (2003). Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environmental Pollution, 124(3), 375–378.  https://doi.org/10.1016/S0269-7491(03)00060-5.CrossRefGoogle Scholar
  41. McDonald, R. C., Isbell, R. F., Speight, J. G., Walker, J., & Hopkins, M. S. (1998). Australian soil and land survey field handbook. Canberra: Australian Collaborative Land Evaluation Program.Google Scholar
  42. McKeague, J. A. (1978). Manual on soil sampling and methods of analysis. Ottawa: Canadian Society of Soil Science.Google Scholar
  43. Mitrović, M., Pavlović, P., Lakušić, D., Djurdjević, L., Stevanović, B., Kostić, O., & Gajić, G. (2008). The potential of Festuca rubra and Calamagrostis epigejos for the revegetation of fly ash deposits. Science of the Total Environment, 407(1), 338–347.  https://doi.org/10.1016/j.scitotenv.2008.09.001.CrossRefGoogle Scholar
  44. Muchuweti, M., Birkett, J. W., Chinyanga, E., Zvauya, R., Scrimshaw, M. D., & Lester, J. N. (2006). Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agriculture, Ecosystems & Environment, 112(1), 41–48.  https://doi.org/10.1016/j.agee.2005.04.028.CrossRefGoogle Scholar
  45. Mudrinić, Č. (1975). Primary dispersion aureoles of the antimony deposit stolice (Western Serbia) [in Serbian]. Belgrade: Transactions of the Faculty of Mining and Geology, University of Belgrade.Google Scholar
  46. Nádaská, G., Lesny, J., & Michalik, I. (2010). Environmental aspect of manganese chemistry. Health and Environment Journal, 100702-A, 1–16.Google Scholar
  47. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters, 8(3), 199–216.  https://doi.org/10.1007/s10311-010-0297-8.CrossRefGoogle Scholar
  48. Navarrete, I. A., Gabiana, C. C., Dumo, J. R. E., Salmo, S. G., Guzman, M. A. L. G., Valera, N. S., & Espiritu, E. Q. (2017). Heavy metal concentrations in soils and vegetation in urban areas of Quezon City, Philippines. Environmental Monitoring and Assessment, 189(4), 145.  https://doi.org/10.1007/s10661-017-5849-y.CrossRefGoogle Scholar
  49. Orwin, K. H., Buckland, S. M., Johnson, D., Turner, B. L., Smart, S., Oakley, S., & Bardgett, R. D. (2010). Linkages of plant traits to soil properties and the functioning of temperate grassland. Journal of Ecology, 98(5), 1074–1083.  https://doi.org/10.1111/j.1365-2745.2010.01679.x.CrossRefGoogle Scholar
  50. Peplow, D. (1999). Environmental impacts of mining in Eastern Washington. Washington DC: Center for Water and Watershed studies fact sheet, University of Washington.Google Scholar
  51. Prach, K., & Pyšek, P. (2001). Using spontaneous succession for restoration of human-disturbed habitats: experience from Central Europe. Ecological Engineering, 17(1), 55–62.  https://doi.org/10.1016/S0925-8574(00)00132-4.CrossRefGoogle Scholar
  52. Radosavljević, A. S., Stojanović, N. J., Radosavljević-Mihajlović, S. A., & Kašić, V. (2013). Polymetallic mineralization of the Boranja Orefield, Podrinje Metallogenic District, Serbia: zonality, mineral associations and genetic features. Periodico di Mineralogia, 82(1), 61–87.Google Scholar
  53. Ranđelović, D., Jovanović, S., Mihailović, N., Šajn, R. (2015). The content of manganese in soils and plants of Bor mine overburden site (Serbia, SE Europe). Proceedings of XXIII International Conference ‘Ecological Truth’, 17–20 June 2015, Kopaonik, Serbia, 186–192.Google Scholar
  54. Rebele, F. (2000). Competition and coexistence of rhizomatous perennial plants along a nutrient gradient. Plant Ecology, 147(1), 77–94.  https://doi.org/10.1023/A:1009808810378.CrossRefGoogle Scholar
  55. Rebele, F., & Lehmann, C. (2001). Biological flora of central Europe: Calamagrostis epigejos (L.) Roth. Flora, 196(5), 325–344.  https://doi.org/10.1016/S0367-2530(17)30069-5.CrossRefGoogle Scholar
  56. Rutkowski, L. (2008). A key to identification of vascular plants of lowland Poland. Warszawa: Wydawnictwo Naukowe PWN.Google Scholar
  57. Salminen, R., Batista, M. J., Bidovec, M., Demetriades, A., De Vivo, B., De Vos, W., Duris, M., Gilucis, A., Gregorauskiene, V., Halamic, J., Heitzmann, P., Lima, A., Jordan, G., Klaver, G., Klein, P., Lis, J., Locutura, J., Marsina, K., Mazreku, A., O'Connor, P. J., Olsson, S. A., Ottesen, R.-T., Petersell, V., Plant, J. A., Reeder, S., Salpeteur, I., Sandström, H., Siewers, U., Steenfelt, A., & Tarvainen, T. (2005). Geochemical atlas of Europe. Part 1: background information, methodology and maps. Espoo: Geological Survey of Finland.Google Scholar
  58. Šerbula, S. M., Radojevic, A. A., Kalinovic, J. V., & Kalinovic, T. S. (2014). Indication of airborne pollution by birch and spruce in the vicinity of copper smelter. Environmental Science and Pollution Research, 21(19), 11510–11520.  https://doi.org/10.1007/s11356-014-3120-4.CrossRefGoogle Scholar
  59. Sharma, R. K., & Agrawal, M. (2005). Biological effects of heavy metals: an overview. Journal of Environmental Biology, 26(2), 301–313.Google Scholar
  60. Shenker, M., & Chen, Y. (2005). Increasing iron availability to crops: fertilizers, organo-fertilizers, and biological approaches. Soil Science & Plant Nutrition, 51(1), 1–17.  https://doi.org/10.1111/j.1747-0765.2005.tb00001.x.CrossRefGoogle Scholar
  61. Siedlecka, A. (1995). Some aspects of interactions between heavy metals and plant mineral nutrients. Acta Societatis Botanicorum Poloniae, 64(3), 265–272.CrossRefGoogle Scholar
  62. Somodi, I., Virágh, K., & Podani, J. (2008). The effect of the expansion of the clonal grass Calamagrostis epigejos on the species turnover of a semi-arid grassland. Applied Vegetation Science, 11(2), 187–192.  https://doi.org/10.3170/2008-7-18354.CrossRefGoogle Scholar
  63. StatSoft. (2007). Statistica for Windows, version 8.0. Tulsa: StatSoft Inc..Google Scholar
  64. Stefanowicz, A. M., 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. Ecological Engineering, 83, 328–337.  https://doi.org/10.1016/j.ecoleng.2015.06.034.CrossRefGoogle Scholar
  65. Süss, K., Storm, C., Zehm, A., & Schwabe, A. (2004). Succession in inland sand ecosystems: which factors determine the occurrence of the tall grass species Calamagrostis epigejos (L.) Roth and Stipa capillata L.? Plant Biology, 6(04), 465–476.CrossRefGoogle Scholar
  66. Thornton, I. (1991). Metal contamination of soils in urban areas. In P. Bullock, & P. J. Gregory (Eds.), Soils in the urban environment (pp. 47–75). Oxford: Blackwell Publishing Ltd.,  https://doi.org/10.1002/9781444310603.ch4 CrossRefGoogle Scholar
  67. Tůma, I., Holub, P., & Fiala, K. (2009). Soil nutrient heterogeneity and competitive ability of three grass species (Festuca ovina, Arrhenatherum elatius and Calamagrostis epigejos) in experimental conditions. Biologia, 64(4), 694–704.Google Scholar
  68. Viard, B., Pihan, F., Promeyrat, S., & Pihan, J. C. (2004). Integrated assessment of heavy metal (Pb, Zn, cd) highway pollution: bioaccumulation in soil, Graminaceae and land snails. Chemosphere, 55(10), 1349–1359.  https://doi.org/10.1016/j.chemosphere.2004.01.003.CrossRefGoogle Scholar
  69. Warden, B. T., & Reisenauer, H. M. (1991). Manganese-iron interactions in the plant-soil system. Journal of Plant Nutrition, 14(1), 7–30.  https://doi.org/10.1080/01904169109364180.CrossRefGoogle Scholar
  70. Wohltmann, F. (1903). Chilisalpeter oder Ammoniak? Berlin: Parey.Google Scholar
  71. Zemanová, V., Pavlík, M., Pavlíková, D., Hnilicka, F., & Vondrackova, S. (2016). Responses to Cd stress in two Noccaea species (Noccaea praecox and Noccaea caerulescens) originating from two contaminated sites in Mezica, Slovenia and Redlschlag, Austria. Archives of Environmental Contamination and Toxicology, 70(3), 464–474.  https://doi.org/10.1007/s00244-015-0198-8.CrossRefGoogle Scholar
  72. Zhang, X. Y., Lin, F. F., Wong, M. T., Feng, X. L., & Wang, K. (2009). Identification of soil heavy metal sources from anthropogenic activities and pollution assessment of Fuyang County, China. Environmental Monitoring and Assessment, 154(1), 439–449.  https://doi.org/10.1007/s10661-008-0410-7.CrossRefGoogle Scholar
  73. Zimdahl, R. L., Arvik, J. H., & Hammond, P. B. (1973). Lead in soils and plants: a literature review. Critical Reviews in Environmental Science and Technology, 3(1–4), 213–224.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Dragana Ranđelović
    • 1
  • Ksenija Jakovljević
    • 2
  • Nevena Mihailović
    • 3
  • Slobodan Jovanović
    • 2
  1. 1.Faculty of Mining and Geology, Department of Mineralogy, Crystallography, Petrology and GeochemistryUniversity of BelgradeBelgradeSerbia
  2. 2.Faculty of Biology, Institute of Botany and Botanical GardenUniversity of BelgradeBelgradeSerbia
  3. 3.Institute for the Application of Nuclear Energy – INEPUniversity of BelgradeBelgradeSerbia

Personalised recommendations