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Comparative assessment of using Miscanthus × giganteus for remediation of soils contaminated by heavy metals: a case of military and mining sites


Contamination of soil by heavy metals is among the important environmental problems due to their toxicity and negative impact to human health and the environment. An effective method for cleaning the soil from heavy metals is phytoremediation using the second-generation bioenergy species Miscanthus × giganteus. The purpose of this research is to study the benefits of M. × giganteus cultivation at the soils taken from the mining and former military sites contaminated by As, Pb, Zn, Co, Ni, Cr, Cu, V, Mn, Sr, and U as well as at the soil artificially contaminated by Zn and Pb, to evaluate the physiological parameters of the plant, to establish peculiarities of the phytoremediation process, and to characterize the behavior of the plant in relation to the nature and concentrations of the metals in the soils. Results showed that M. × giganteus was resistant to heavy metals (tolerance index ≥ 1) and that the greatest portion of metals accumulated in the root system. The morphological parameters of the plant while grown on different soils are influenced by soil type and the content of contaminants. The stress effect while growing M. × giganteus on soil artificially contaminated by Zn and Pb was evaluated by measuring the content of pigments (chlorophylls a, b, and carotenoids) in the plant’s leaves. The decrease in the total content of chlorophylls, Сa + bcar and transpiration rate of water along with the increase in the water absorbing capacity were observed. The accumulation of heavy metals in different parts of the plant was determined; bioaccumulation coefficient and values of translocation factor were calculated. The obtained results showed that M. × giganteus was an excluder plant for nine highly toxic elements (As, Pb, Zn, Co, Ni, Cr, Cu, V, U) and an accumulator species for the moderately dangerous elements (Mn, Sr). Further research will be focused on the extraction of stable stimulated plant-growth–promoting rhizobacteria from the rhizosphere of M. × giganteus and formulation on that base the plant-bacterial associations as well as on the comparison of the plant physiological parameters, biochemical soil activity, and accumulation of heavy metals in the Miscanthus tissues between first and second vegetations.

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  • Almaganbetov N, Grigoruk V (2008) Degradation of soil in Kazakhstan: problems and challenges. In: Simeonov, Sargsyan V (eds) Soil chemical pollution, risk assessment, remediation and security. Springer, pp 309–320.

  • Amanullah M, Ping W, Amjad A, Mukesh KA, Altaf HL, Quan W, Zengqiang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotox Environ Safe 126:111–121.

    Article  CAS  Google Scholar 

  • Amina Н, Araina BA, Abbasi MS, Jahangir TM, Amind F (2018) Comparative study of Zn-phytoextraction potential in guar ( L.) and sesame ( L.): tolerance and accumulation. Geology, Ecology, and Landscapes 2(1):29–38.

  • Antonkiewicz J, Kołodziej B, Bielińska E, Witkowicz R, Tabor S (2018) Using Jerusalem artichoke to extract heavy metals from municipal sewage sludge amended soil. Pol J Environ Stud 27:513–527.

    Article  CAS  Google Scholar 

  • Audet P, Chares C (2007) Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 147:231–237.

    Article  CAS  Google Scholar 

  • Аtabayeva S, Nurmahanova A, Asrandina S, Alybayeva RA, Meldebekova A, Lee T (2017) Effect of copper on physiological and biochemical peculiarities of wheat (Triticum aestivum L.) varieties. Pak J Bot 49(6):2189–2196

    Google Scholar 

  • Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1-4):1–4.

    Article  Google Scholar 

  • Baker AJM, McGrath SP, Reeve RD (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal polluted soils Contaminated soil and water. Lewis Publishers, Boca-Raton, FL, USA, pp 85–107

    Google Scholar 

  • Balsamo RA, Kelly WJ, Satrio JA, Ruiz-Felix MN, Fetterman M, Wynn R, Hagel K (2015) Utilization of grasses for potential biofuel production and phytoremediation of heavy metal contaminated soils. Int J Phytoremediation 17(5):448–455.

    Article  CAS  Google Scholar 

  • Bilandzija N, Jurisic V, Vica N, Leto J, Matin A, Sito S, Kricka T (2017) Combustion properties of Miscanthus x giganteus Biomass-Optimization of harvest time. J Energy Inst 90:528–533.

    Article  CAS  Google Scholar 

  • Biyasheva ZM (2010) Prolonged pollution by heavy metals and radionuclides of the territory adjacent to mining enriched complex in town Tekeli. Bul Kazakh Natl U Ecol Ser 3(29):60–65 (In Russian)

    Google Scholar 

  • Boersma N (2013) The influence of propagation method and stand age on Miscanthus x giganteus performance in Iowa, USA. PhD Dissertation.

  • Chirkova ТV (2002) Physiological basis of plant resistance. Publishing House of St. Petersburg University, St. Petersburg, p 244 (In Russian)

    Google Scholar 

  • Dauber J, Brown C, Fernando AL, Finnan J, Krasuska E, Ponitka J, Styles D, Thran D, Van Groenigen KJ, Weih M, Zah R (2012) Bioenergy from “surplus” land: environmental and socio-economic implications. BioRisk 7:5–50.

    Article  Google Scholar 

  • Diwan H, Ahmad A, Iqbal M (2010) Uptake related parameters as indices of phytoremediation potential. Biologia 65(6):1004–1011.

    Article  CAS  Google Scholar 

  • Gavrilenko VF, Ladygina ME, Khandobina LM (1975) A large practical workshop on plant physiology. High School, Moscow, Russia: 392 рp. (In Russian)

  • Ginneken LV, Meers Е, Guisson R, Ruttens A, Elst K, Tack FMG, Vangronsveld J, Diels L, Dejonghe W (2007) Phytoremediation for heavy metal-contaminated soils combined with bioenergy production. Environ Eng Landsc 15(4):227–236.

    Article  Google Scholar 

  • GOST (1983) Protection of nature. Soil. Classification of chemicals for the pollution control. (In Russian)

  • GOST (1984a) 26213-84. Soil. Determination of humus by the Tyurin method, modified by CINAO. (In Russian)

  • GOST (1984b) Protection of nature. Soil. Methods for sampling and preparation of soil for chemical, bacteriological, helminthological analysis. (In Russian)

  • GOST (1985) 26423-85. Measurement of the actual acidity of the soil was carried out by applying the instrument pH-meter AP50. (In Russian)

  • GOST (1991) 26207-91. Soils. Determination of the mobile compounds of phosphorus and potassium by Kirsanov method, modified by CINAO. (In Russian)

  • Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172(1):479–484.

    Article  CAS  Google Scholar 

  • Heaton EA, Dohleman FG, Miguez AF, Juvik JA, Lozovaya V, Widholm J, Zabotina OA, Mcisaac GF, David MB, Voigt TB, Boersma NN, Long SP (2010) Miscanthus: a promising biomass crop. Adv Bot Res 56:76–137.

    Article  Google Scholar 

  • Il’in VB, Syso AI. (2001) Microelements and heavy metals in soils and plants of Novosibirsk region. SB RAS Press, Novosibirsk, Russia. 229 рр. (In Russian)

  • ISO 10381-6 (2017) Soil Quality-Sampling-Part 6: Guidance on the collection, handling and storage of soil under aerobic conditions for the assessment of microbiological processes, biomass and diversity in the laboratory. Available at: Accessed 03 Sep 2018

  • Issanova G, Saparov A, Ustemirova A (2014) Soil degradation and desertification processes within Kazakhstan. Proceedings of IV International Conference “Ecology of urban areas 2014”, 9-10th October 2014, Zrenjanin, Serbia, pp 429-434

  • Jones MB, Walsh M (2001) Miscanthus for energy and fibre. – Origins and Taxonomy of Miscanthus. James & James Publishers, London, pp 2–9

    Google Scholar 

  • Kabata-Pendias A (2010) Trace elements in soils and plants, 4th edn. CRC Press, Boca Raton, FL, USA, p 548

    Book  Google Scholar 

  • Kharytonov M, Pidlisnyuk V, Stefanovska T, Babinko M, Martynova N, Rula I (2018) The estimation of Miscanthus×giganteus’ adaptive potential for cultivation on the mining and post-mining lands in Ukraine. Environ Sci Pollut Res 26(3):2974–2986.

    Article  CAS  Google Scholar 

  • Khudsar T, Mahmooduzzafar, Iqbal M (2001) Cadmium-induced changes in leaf epidermis, photosynthetic rate and pigment concentrations in Cajanus cajan. Biol Plant 44:59–64.

  • Kidin VV, Deriugin IP, Kobzarenko VI (2008) Workshop on agrochemistry. Colos, Moscow, Russia. 599 рр. (In Russian)

  • Kilpatrick LА (2012) Sustainable growth of Miscanthus on marginal lands amended with flue gas desulfurization gypsum and sewage biosolids. Paper. 12-133766124 ASABE, p 37

  • Kocon A, Jurga B (2017) The evaluation of growth and phytoextraction potential of Miscanthus x giganteus and Sida hermaphrodita on soil contaminated simultaneously with Cd, Cu, Ni, Pb, and Zn. Environ Sci Pollut Res 24(5):4990–5000.

    Article  CAS  Google Scholar 

  • Kocon A, Matyka M (2012) Phytoextractive potential of Miscanthus x giganteus and Sida hermaphrodita growing under moderate pollution of soil with Zn and Pb. J Food Agric Environ 10(2):1253–1256

    CAS  Google Scholar 

  • Kovalchuk VP, Vasiliev VG, Boyko VD, Zosimov LV (2010) Collection of methods for studying soils and plants. XXI century, Кolos, p 252 (In Russian)

    Google Scholar 

  • Kuehl RO (2000) Design of experiments: statistical principles of research design and analysis. 2nd edn. Duxbury press at Brooks /Cole publishing company, CA, USA. 688 pp

  • Kvak V, Stefanovska T, Pidlisnyuk V, Alasmary Z, Kharytonov M (2018) The long-term assessment of Miscanthus x giganteus cultivation in the forest-steppe zone of Ukraine. INMATEH J Agricult Engineer 54(1):113–121

    Google Scholar 

  • Lord R, Atkinson J, Lane A, Scurlock J, Street G (2008) Biomass, remediation, re generation (BioReGen Life Project): reusing brownfield sites for renewable energy crops. ASCE Geotechnical Special Publication 177:527–534. Accessed 20 Jan 2019

  • Maximyuk GP (1948) Application of the Heusler calcimeter for the determination of carbon dioxide. Pochvovedenie AN SSSR, Moscow, Russia, p 126 (In Russian)

    Google Scholar 

  • Meysurova AF, Notov AA, Pungin AV (2018) Photosynthetic pigments in hypogymnia physodes with different metal contents. J Appl Spectrosс 84(6):1037–1043.

  • Nsanganwimana F, Pourrut B, Mench M, Douay F (2014) Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services A review. J Environ Manag 143:123–134.

    Article  CAS  Google Scholar 

  • Nsanganwimana F, Waterlot C, Louvel B, Pourrut B, Douay F (2016) Metal, nutrient and biomass accumulation during the growing cycle of Miscanthus established on metal-contaminated soils. J Soil Sci Plant Nutr 179(2):257–269.

    Article  CAS  Google Scholar 

  • Nurzhanova A, Kalugin S, Zhambakin K (2013) Obsolete pesticides and application of colonizing plant species for remediation of contaminated soils in Kazakhstan. Environ Sci Pollut Res 20:2054–2063.

    Article  CAS  Google Scholar 

  • Panin MS (2002) Chemical ecology. Semipalatinsk, Kazakhstan. 852 рр. (In Russian)

  • Pidlisnyuk V, Erickson L, Kharchenko S, Stefanovska T (2014) Sustainable land management: growing miscanthus in soils contaminated with heavy metals. J Environ Prot 5:723–730.

    Article  CAS  Google Scholar 

  • Pidlisnyuk V, Trogl J, Stefanovska T, Shapoval P, Erickson L (2016) Preliminary results on growing second generation biofuel crop Miscanthus x giganteus at the polluted military site in Ukraine. Nova Biotechnol et Chim 15(1):77–84.

    Article  CAS  Google Scholar 

  • Pidlisnyuk V, Erickson L, Trögl J, Shapoval P, Davis L, Popelka J, Stefanovska T, Hettiarachchi G (2018) Metals uptake behaviour in Miscanthus x giganteus plant during growth at the contaminated soil from the military site in Sliač, Slovakia. Pol J Chem Technol 20(2):1–7.

    Article  CAS  Google Scholar 

  • Podrzeba M, Rusinowski S, Krzyzak J (2018) Macroelements and heavy metals content in energy crops cultivated on contaminated soil under different fertilization- case studies on autumn harvest. Environ Sci Pollut Res 25:12096–12106.

    Article  CAS  Google Scholar 

  • Pogrzeba M, Krzyzak J, Sas-Nowosielska A (2013) Environmental hazards related to Miscanthus x giganteus cultivation on heavy metal contaminated soil. E3S Web of Conferences 1:29006.м29006

  • Pogrzeba M, Krzyżak J, Rusinowski S, Hebner A, Kopielski K, Werle S, Ratman-Kłosińska I (2017) Possibility of using energy crops for phytoremediation of heavy metals contaminated land - a three-year experience. In: Renewable energy sources: engineering, technology, innovation, (eds) Krzysztof Mudryk, Sebastian Werle, ICORES, Springer Proceeding in Wnergy. Cham. pp.33-45.,371-6_4

  • Prasad MN (2003) Practical use of plants for restoration soil polluted by metals. Russ J Plant Physiol 50(1):764–777

    Google Scholar 

  • Rodríguez-Eugenio N, McLaughlin M, Pennock D (2018) Soil Pollution: a hidden reality. Rome, FAO. 142 pp. (Accessed 20 Jan 2019)

  • Rohan D, Mayank V, João P, Paul MS (2013) Spatial distribution of heavy metals in soil and flora associated with the glass industry in North Central India: implications for phytoremediation. Soil Sediment Contam 22(1):1–20.

    Article  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52(364):2115–2126

    Article  CAS  Google Scholar 

  • Shaw JA (1989) Heavy metals tolerance in plants. In: Evolutionary aspects. CRC Press, Florida, USA, p 268

    Google Scholar 

  • Strilchuk YG (2001) Environmental impact assessment of activities at the military polygons and determination the measures for revitalization. In: Radioecology. Protection of the Environment, vol 3, pp 26–33 (In Russian)

    Google Scholar 

  • Tsao DT (2003) Overview of phytotechnologies. In: Scheper T, Tsao D (eds) Advances in biochemical engineering/biotechnology, phytoremediation. Springer-Verlag, Berlin, Germany, pp 1–50.,991-X_1

    Chapter  Google Scholar 

  • Turner JR, Thayer JF (2001) Introduction to analysis of variance: design, analysis, and interpretation. Sage Publications, Inc, Thousand Oaks, CA, USA, p 192

    Book  Google Scholar 

  • Wagner M, Kiesel A, Hastings A, Iqbal Y, Lewandowski I (2017) Novel miscanthus germplasm-based value chains: a life cycle assessment. Front Plant Sci 8:990.

    Article  Google Scholar 

  • Wagner M, Mangold A, Lask J, Kiesel A, Lewandowski I (2018) Economic and environmental performance of miscanthus cultivated on marginal land for biogas production. GCB Bioenergy 11:34–49.

    Article  CAS  Google Scholar 

  • World Reference Base for Soil Resources (2015) IUSS Working Group WRB. International soil classification system for naming soils and creating legends for soil maps. In: World Soil Resources Reports No. 106. FAO, Rome, Italy, p 203

    Google Scholar 

  • Yakovleva NA, Semenyuk AH, Shajgabaev FS (2009) Ecological –hygienic aspects of health state in city Tekeli. Hygiene, epidemiology. Immunobiology 3:41–49 (In Russian)

    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.

  • Zaier H, Ghnaya T, Lakhdar A, Baioui R, Ghabriche R, Mnasri M, Sghair S, Lutts S, Abdelly C, Hanen Z, Taha G, Abelbasset L, Rawdha B, Rim G, Majda M, Hedly A (2010) Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: Tolerance and accumulation. Hazard Mater 183(1-3):609–615.

    Article  CAS  Google Scholar 

  • Zu YQ, Li Y, Chen JJ, Chen HY, Qin L, Schvartz C (2005) Hyper accumulation of Pb, Zn, and Cd in herbaceous grown on lead–zinc mining area in Yunnan, China. Environ Int 31(5):755–762.

    Article  CAS  Google Scholar 

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This research was supported by NATO (Science for Peace and Security Programmer, Multi-Year Project No. G4687) and the Ministry of Education and Science of Kazakhstan (Grant No. AP05131473).

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Nurzhanova, A., Pidlisnyuk, V., Abit, K. et al. Comparative assessment of using Miscanthus × giganteus for remediation of soils contaminated by heavy metals: a case of military and mining sites . Environ Sci Pollut Res 26, 13320–13333 (2019).

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