Environmental Science and Pollution Research

, Volume 24, Issue 5, pp 4990–5000 | Cite as

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

  • Anna Kocoń
  • Beata JurgaEmail author
Research Article


One of the cheapest, environmentally friendly methods for cleaning an environment polluted by heavy metals is phytoextraction. It builds on the uptake of pollutants from the soil by the plants, which are able to grow under conditions of high concentrations of toxic metals. The aim of this work was to assess the possibility of growing and phytoextraction potential of Miscanthus x giganteus and Sida hermaphrodita cultivated on two different soils contaminated with five heavy metals simultaneously: Cd, Cu, Ni, Pb, and Zn. A 3-year microplot experiment with two perennial energy crops, M. x giganteus and S. hermaphrodita, was conducted in the experimental station of IUNG-PIB in Poland (5° 25′ N, 21° 58 ‘E), in the years of 2008–2010. Miscanthus was found more tolerant to concomitant soil contamination with heavy metals and produced almost double biomass than Sida in all three tested years, independent of soil type. Miscanthus collected greater amount of heavy metals (except for cadmium) in the biomass than Sida. Both energy crops absorb high levels of zinc, lower levels of lead, copper, and nickel, and absorbed cadmium at least, generally more metals were taken from the sandy soil, where plants also yielded better. Photosynthesis net rate of Miscanthus was on average 40% higher compared to Sida. Obtained results indicate that M. x giganteus and S. hermaphrodita can successfully be grown on moderately contaminated soil with heavy metals.


Soil contamination Heavy metals Energy crops Biomass yield Phytoextraction 


  1. Anderson‐Teixeira KJ, Davis SC, Masters MDD, Evan H (2009) Changes in soil organic carbon under biofuel crops. GCB Bioenergy 1:75–96CrossRefGoogle Scholar
  2. Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid A, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192CrossRefGoogle Scholar
  3. Assunçao AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360CrossRefGoogle Scholar
  4. Baker AJM (1981) Accumulators and excluders strategies in response of plants to heavy metals. J Plant Nutr 3:643–654CrossRefGoogle Scholar
  5. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  6. Brosse N, Dufour A, Meng XZ, Sun QN, Ragauskas A (2016) Miscanthus: a fast‐growing crop for biofuels and chemicals production. Biofuels Bioprod Biorefin 6:580–598CrossRefGoogle Scholar
  7. Burzyński M, Klobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynthetica 42(4):505–510CrossRefGoogle Scholar
  8. Chłopecka A, Adriano DC (1997) Zinc uptake by plants an amended polluted soils. Soil Sci and Plant Nutr 43:1031–1036CrossRefGoogle Scholar
  9. Di Baccio D, Tognetti R, Sebastiani L, Vitagliano C (2003) Responses of Populus deltoides x Populus nigra (Populus x euramericana) clone I-214 to high zinc concentrations. New Phytol 159:443–452CrossRefGoogle Scholar
  10. DIN 51731. Wood pellet standards. Germany. CERTCO Deutsches, Institut für Normung (DIN) (in German)Google Scholar
  11. European Parliament Directive of The European Parliament and of The Council (2009) of 23 April 2009 on the promotion of the use of energy from renewable sources and amending and subsequently repealing Directives 2001/77/EC and 2003/30/EC. Official Journal of the European Union OJ L 140, 5.6.2009:16–62Google Scholar
  12. Faber A, Kuś J, Matyka M (2008) Crop cultivation for energy production purposes. PKPP Lewiatan, Vattenfall (in Polish)Google Scholar
  13. Farage PK, Blowers DA, Long SP, Baker NR (2006) Low growth temperatures modify the efficiency of light use by photosystem II for CO2 assimilation in leaves of two chilling-tolerant C4 species, Cyperus longus L. and Miscanthus×giganteus. Plant Cell and Environ 29:720–728CrossRefGoogle Scholar
  14. Fischer G, Prieler S, van Velthuizen H (2005) Biomass potentials of miscanthus, willow and poplar: results and policy implications for Eastern Europe, Northern and Central Asia. Biomass Bioenerg 28:119–132CrossRefGoogle Scholar
  15. French CJ, Dickinson NM, Putwain PD (2006) Woody biomass phytoremediation of contaminated brownfield land. Environ Pollul 141:387–395CrossRefGoogle Scholar
  16. Gisbert C, Clemente R, Navarro-Aviñó J, Baixauli C, Ginér A et al (2006) Tolerance and accumulation of heavy metals by Brassicaceae species grown in contaminated soils from Mediterranean regions of Spain. Environ Exp Bot 56:19–27CrossRefGoogle Scholar
  17. Heaton EA, Dohleman FG, Miguez AF, Juvik JA, Lozovaya V, et al. (2010) Chapter 3—Miscanthus: a promising biomass crop in advances in botanical research ed. D Jean-Claude Kader and Michel:75–137 (Academic Press)Google Scholar
  18. Kabala C, Karczewska A, Kozak M (2010) Energetic plants in reclamation and management of degraded soils. Zesz Nauk UP Wroc Rol XCVI 576:97–118Google Scholar
  19. Kabala C, Singh BR (2001) Fractionation and mobility of copper, lead, and zinc in soil profiles in the vicinity of a copper smelter. J Environ Qual 30:485–492CrossRefGoogle Scholar
  20. Kabata-Pendias A, Motowiecka-Terelak T, Piotrowska M, Terelak H, Witek T (1993) Assessment of contamination level of soil and plants with heavy metals and sulphur, IUNG Pulawy Publisher, P(53):1–20 ( in Polish)Google Scholar
  21. Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer Verlang, HeidelbergCrossRefGoogle Scholar
  22. Kabata-Pendias A, Pendias H (2001) Biogeochemistry of trace elements. PWN Warsaw (in Polish)Google Scholar
  23. Kocon A, Matyka M (2012) Phytoextractive potential of Miscanthus x giganteus and Sida hermaphrodita growing under moderate contamination of soil with Zn and Pb. J Food Environ 10(2):1253–1256Google Scholar
  24. Kołodziej B, Antonkiewicz J, Sugier D (2016) Miscanthus x giganteus as a biomass feedstock grown on municipal sewage sludge. Ind Crop Prod 81:72–82CrossRefGoogle Scholar
  25. Koopmans GF, Römkens PFAM, Song J, Temminghoff EJM, Japenga J (2007) Predicting the phytoextraction duration to remediate heavy metal contaminated soils. Water Air Soil Pollut 181:355–371CrossRefGoogle Scholar
  26. Korzeniowska J, Stanislawska-Glubiak E (2015) Phytoremediation potential of Miscanthus x giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res. doi: 10.1007/s11356-015-4439 Google Scholar
  27. Korzeniowska J, Stanislawska Glubiak E, Igras J (2011) Applicability of energy crops for metal phytostabilization of soils moderately contaminated with copper, nickel and zinc. J Food Agric Environ 9(3–4):693–697Google Scholar
  28. Kuboi T, Noguchi A, Yazaki A (1986) Family–dependent cadmium accumulation characteristics in higher plants. Plant Soil 92:405–415CrossRefGoogle Scholar
  29. Laureysens I, De Temmerman L, Hastir T, Van Gysel M, Ceulemans R (2005) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture. II. Vertical distribution and phytoextraction potential. Environ Pollut 133:541–551CrossRefGoogle Scholar
  30. Lewandowski I, Clifton-Brown JC, Scurlock JMO, Huisman W (2000) Miscanthus: European experience with a novel energy crop. Biomass Bioenergy 19:209–227CrossRefGoogle Scholar
  31. Li C, Xiao B, Wang QH, Yao SH, Wu JY (2014) Phytoremediation of Zn and Cr-contaminated soil using two promising energy grasses. Water Air Soil Pollut 225:2027. doi: 10.1007/s11270-014-2027-5 CrossRefGoogle Scholar
  32. Liu J, Li K, Xu J, Zhang Z, Ma T, Lu X, Yang J, Zhu Q (2004) Pb toxicity, uptake and translocation in different rice cultivars. Plant Sci 165:793–802CrossRefGoogle Scholar
  33. Leonardo SD, Capuana M, Arnetoli M, Gabbrielli R, Gonnelli C (2011) Exploring the metal phytoremediation potential of three Populus alba L. clones using an in vitro screening. Environ Sci Pollut Res 18:82–90CrossRefGoogle Scholar
  34. Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad, Pakistan. Pak J Bot 42(1):291–301Google Scholar
  35. Marín F, Sánchez JL, Arauzo J, Fuertes R, Gonzalo A (2009) Semichemical pulping of Miscanthus giganteus. Effect of pulping conditions on some pulp and paper properties. Bioresour Technol 100:3933–3940CrossRefGoogle Scholar
  36. Matyka M (2013) Production and economic aspects of cultivation of perennial crops for energy purposes. Monographs and dissertations. IUNG-PIB Puławy 35:1–98 (in Polish)Google Scholar
  37. McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282CrossRefGoogle Scholar
  38. Meers E, Van Slycken S, Adriaensen K, Ruttens A, Vangronsveld J, Du Laing G, Witters N, FMG T (2010) The use of bio-energy crops (Zea mays) for “phytoattenuation” of heavy metals on moderately contaminated soils: a field experiment. Chemosphere 78:35–41CrossRefGoogle Scholar
  39. Meers E, Vandecasteele B, Ruttens A, Vangronsveld J, Tack FMG (2007) Potential of five willow species (Salix spp.) for phytoextraction of heavy metals. Environ Exp Bot 60:57–68CrossRefGoogle Scholar
  40. Mleczek M, Lukaszewski M, Kaczmarek Z, Rissmann I, Golinski P (2009) Efficiency of selected heavy matals acccumulation by Salix viminalis roots. Environ Exp Bot 65:48–53CrossRefGoogle Scholar
  41. Mojiri A (2011) The potential of corn (Zea mays) for phytoremediation of soil contaminated with cadmium and lead. J Biol Environ Sci 5:17–22Google Scholar
  42. Moosavi SG, Seghatoleslami MJ (2013) Phytoremediation: a review. Adv Agri Biol 1:5–11Google Scholar
  43. Naidu SL, Long SP (2004) Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus x giganteus: an in vivo analysis. Planta 220:145–155CrossRefGoogle Scholar
  44. Nascimento CWA, Xing B (2006) Phytoextraction: a review on enhanced metal availability and plant accumulation. Sci Agric 63(3):299–311 CrossRefGoogle Scholar
  45. Nawab J, Khan S, Aamir M, Shamshad I, Qamar Z et al (2016) Organic amendments impact the availability of heavy metal(loid)s in mine-impacted soil and their phytoremediation by Penisitum americanum and Sorghum bicolor. Environ Sci and Pollut Res 23:2381–2390CrossRefGoogle Scholar
  46. 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 143:123–12sCrossRefGoogle Scholar
  47. Nsanganwimana F, Pourrut B, Waterlot C, Louvel B, Bidar G, Labidi S, Fontaine J, Muchembled J, Lounes-Hadj Sahraoui A, Fourrier H, Douay F (2015) Metal accumulation and shoot yield of Miscanthus x giganteus growing in contaminated agricultural soils: insights into agronomic practices. Agric Ecosyst Environ 213:61–71CrossRefGoogle Scholar
  48. Oleszek W, Terelak H, Maliszewska-Kordybach B, Kukuła S (2003) Soil, food and agroproduct contamination monitoring in Poland. Polish J Environ Stud 12(3):261–268Google Scholar
  49. Pandey VC, Bajpai O, Singh N (2016) Energy crops in sustainable phytoremediation. Renew Sustain Energy Rev 54:58–73CrossRefGoogle Scholar
  50. Peng KJ, Luo CL, Chen YH, Wang GP, Li XD, Shen ZG (2009) Cadmium and other metal uptake by Lobelia chinensis and Solanum nigrum from contaminated soils. Bull Environ Contam Toxicol 83:260–264CrossRefGoogle Scholar
  51. Pikuła D, Stępień W (2007) The influence of soil pH on the uptake of heavy metals by plants. Fragm Agronom 2(94):227–237 (in Polish)Google Scholar
  52. Placek A, Grobelak A, Kacprzak M (2016) Improving the phytoremediation of heavy metals contaminated soil by use of sewage sludge. Int J Phytorem 18:605–618CrossRefGoogle Scholar
  53. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29(4):529–540CrossRefGoogle Scholar
  54. Ruttens A, Boulet J, Weyens N, Smeets K, Adriaensen K, Meers E, Van Slycken S, Tack F, Meiresonne L, Thewys T, Witters N, Carleer R, Dupae J, Vangronsveld J (2011) Short rotation coppice culture of willows and poplars as energy crops on metal contaminated agricultural soils. Int J Phytorem 13:194–207CrossRefGoogle Scholar
  55. Schmidt U (2003) Enhancing phytoextraction: the effects of chemical soil manipulation on mobility, plant accumulation, and leaching of heavy metals. J Environ Qual 32:1939–1954CrossRefGoogle Scholar
  56. Sękara A, Poniedziałek M, Ciura J, Jędrszczyk E (2005) Cadmium and lead accumulation and distribution in the organs of nine crops: implications for phytoremediation. Pol J Environ Stud 14(4):509–516Google Scholar
  57. Spiak Z (1998) The influence of soil pH on plant zinc uptake. Zesz Probl Post Nauk Rol 456:439–443 (in Polish)Google Scholar
  58. Stanislawska-Glubiak E, Korzeniowska J, Kocon A (2012) Effect of the reclamation of heavy metal-contaminated soil on growth of energy willow. Pol J Environ Stud 21(10):187–192Google Scholar
  59. Stanislawska-Glubiak E, Korzeniowska J, Kocon A (2015) Effect of peat on the accumulation and translocation of heavy metals by maize growth in contaminated soils. Environ Sci Pollut Res 22:4706–4714CrossRefGoogle Scholar
  60. Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation, an ecological solution to organic contamination. Ecol Eng 18:647–658CrossRefGoogle Scholar
  61. Techer D, Martinez-Chois C, Laval-Gilly P, Henry S, Bennasroune A et al (2012) Assessment of Miscanthus × giganteus for rhizoremediation of long term PAH contaminated soils. Appl Soil Ecol 62:42–49CrossRefGoogle Scholar
  62. Van Ginneken L, Meers E, Guisson R, Rutterns A, Elst K, Tack FMG, Vangroncveld J, Diels L, Dejonghe W (2007) Phytoremediation for heavy metal-contaminated soils combined with bioenergy production. J Environ Eng Landscape Manage 15(4):227–236Google Scholar
  63. Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794CrossRefGoogle Scholar
  64. Vassilev A, Schwitzguébel JP, Thewys T, van der Lelie D, Vangronsveld J (2004) The use of plants for remediation of metal contaminated soils. Scientific World J 4:9–34CrossRefGoogle Scholar
  65. Wanat N, Austruy A, Joussein E, Soubrand M, Hitmi A et al (2013) Potentials of Miscanthus × giganteus grown on highly contaminated Technosols. J Geochem Explor 126–127:78–84CrossRefGoogle Scholar
  66. Waterlot C, Pruvot CH, Douay F (2011) Effects of phosphorus amendment and the pH of water used for watering on the mobility and phytoavailability of Cd, Pb and Zn in highly contaminated kitchen garden soils. Ecol Eng 37:1081–1093CrossRefGoogle Scholar
  67. Wisz J, Matwiejew A (2005) Biomass—research laboratory in terms of suitability for combustion. Energetyka 9:631–636 (in Polish)Google Scholar
  68. Wrzosek J, Gawroński S, Gworek B (2008) Use of crop plant cultivate for energy and phytoremediation. Ochr Środ i Zas Natur 37:139–151 (in Polish)Google Scholar
  69. 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. doi: 10.1016/j.scitotenv.2006.01.016 CrossRefGoogle Scholar
  70. Zhang L, Zhang H, Guo W, Tian Y, Chen Z, Wei X (2012) Photosynthetic responses of energy plant maize under cadmium contamination stress. Adv Matter Res 356-360:283–286. doi: 10.4028/ CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Plant Nutrition and FertilizationThe Institute of Soil Science and Plant Cultivation - State Research InstitutePuławyPoland

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