Contrasted tolerance of Agrostis capillaris metallicolous and non-metallicolous ecotypes in the context of a mining technosol amended by biochar, compost and iron sulfate

  • Romain Nandillon
  • Manhattan Lebrun
  • Florie Miard
  • Marie Gaillard
  • Stéphane Sabatier
  • Domenico Morabito
  • Sylvain BourgerieEmail author
Original Paper


Metal(loid) contamination of soil, resulting from the mining activities, is a major issue worldwide, due to its negative effects on the environment and health. Therefore, these contaminated soils need to be remediated. One realistic method is the assisted phytostabilization, which aims at establishing a vegetation cover on the soil that will reduce metal(loid) bioavailability and spreading through the prevention of wind erosion and water leaching. In addition, amendments are applied to improve soil conditions and ameliorate plant growth. In this goal, biochar and compost showed good results in terms of amelioration of soil fertility and reduction in lead bioavailability. However, they usually have a negative effect on arsenic. On the contrary, iron sulfate showed capacity to reduce arsenic mobility through interaction with its iron hydroxides. Finally, the choice of the appropriate plant species is crucial for the success of assisted phytostabilization. One good option is to use endemic species, adapted to the metal(loid) stress, with a fast growth and large shoot and root systems. The aims of this study were to (1) evaluate the effects of applying biochar, compost and iron sulfate, alone or combined, to a former mine soil on the soil properties and Agrostis capillaris growth, and (2) assess the difference between two Agrostis capillaris ecotypes, an endemic metallicolous ecotype and a non-metallicolous ecotype. Results of the mesocosm experiment showed that amendment application improved soil properties, i.e., reduced soil acidity, increased nutrient availability and lower metal(loid) stress, the best being the combination biochar–compost–iron sulfate. These ameliorations allowed a better plant growth. Finally, the metallicolous ecotype performed better in terms of growth than the non-metallicolous one and could thus be used in an assisted phytostabilization process on the former mine site.


Agrostis capillaris Biochar Compost Iron sulfate Non-metallicolous Metallicolous 



The authors wish to thank Mr JC. Léger (La Carbonerie) for providing the biochar.


  1. Abewa, A., Yitaferu, B., Selassie, Y. G., & Amare, T. T. (2014). The role of biochar on acid soil reclamation and yield of Teff (Eragrostis tef [Zucc] Trotter) in Northwestern Ethiopia. Journal of Agricultural Science, 6(1), 1.Google Scholar
  2. Adriano, D. C. (2001). Trace elements in terrestrial environments (2nd ed.). New York: Springer.CrossRefGoogle Scholar
  3. Agegnehu, G., Bass, A., Nelson, P., & Bird, M. (2016). Benefits of biochar, compost and biochar–compost for soil quality, maize yield and greenhouse gas emissions in a tropical agricultural soil. Science of the Total Environment, 543, 295–306.CrossRefGoogle Scholar
  4. Ahmad, M., Ok, Y., Kim, B., Ahn, J., Lee, Y., Zhang, M., et al. (2016). Impact of soybean stover- and pine needle-derived biochars on Pb and As mobility, microbial community, and carbon stability in a contaminated agricultural soil. Journal of Environmental Management, 166, 131–139.CrossRefGoogle Scholar
  5. Ahmad, M., Rajapaksha, A., Lim, J., Zhang, M., Bolan, N., Mohan, D., et al. (2014). Biochar as a sorbent for contaminant management in soil and water: A review. Chemosphere, 99, 19–33.CrossRefGoogle Scholar
  6. Alagić, S. Č., Šerbula, S. S., Tošić, S. B., Pavlović, A. N., & Petrović, J. V. (2013). Bioaccumulation of arsenic and cadmium in birch and lime from the Bor region. Archives of Environmental Contamination and Toxicology, 65(4), 671–682.CrossRefGoogle Scholar
  7. Alvarenga, P., de Varennes, A., & Cunha-Queda, A. C. (2014). The effect of compost treatments and a plant cover with Agrostis tenuis on the immobilization/mobilization of trace elements in a mine-contaminated soil. International Journal of Phytoremediation, 16(2), 138–154.CrossRefGoogle Scholar
  8. Alvarenga, P., Gonçalves, A. P., Fernandes, R. M., De Varennes, A., Vallini, G., Duarte, E., et al. (2009a). Organic residues as immobilizing agents in aided phytostabilization: (I) Effects on soil chemical characteristics. Chemosphere, 74(10), 1292–1300.CrossRefGoogle Scholar
  9. Alvarenga, P., Palma, P., De Varennes, A., & Cunha-Queda, A. C. (2012). A contribution towards the risk assessment of soils from the São Domingos Mine (Portugal): Chemical, microbial and ecotoxicological indicators. Environmental Pollution, 161, 50–56.CrossRefGoogle Scholar
  10. Alvarenga, P., Palma, P., Gonçalves, A. P., Fernandes, R. M., De Varennes, A., Vallini, G., et al. (2009b). Organic residues as immobilizing agents in aided phytostabilization: (II) Effects on soil biochemical and ecotoxicological characteristics. Chemosphere, 74(10), 1301–1308.CrossRefGoogle Scholar
  11. Álvarez-Valero, A. M., Sáez, R., Pérez-López, R., Delgado, J., & Nieto, J. M. (2009). Evaluation of heavy metal bio-availability from Almagrera pyrite-rich tailings dam (Iberian Pyrite Belt, SW Spain) based on a sequential extraction procedure. Journal of Geochemical Exploration, 102(2), 87–94.CrossRefGoogle Scholar
  12. Al-Wabel, M. I., Usman, A. R. A., Al-Farraj, A. S., Ok, Y. S., Abduljabbar, A., Al-Faraj, A. I., & Sallam, A. S. (2017). Date palm waste biochars alter a soil respiration, microbial biomass carbon, and heavy metal mobility in contaminated mined soil. Environmental Geochemistry and Health, 41(4), 1705–1722.CrossRefGoogle Scholar
  13. Arienzo, M., Christen, E. W., Quayle, W., & Kumar, A. (2009). A review of the fate of potassium in the soil–plant system after land application of wastewaters. Journal of Hazardous Materials, 164(2–3), 415–422.CrossRefGoogle Scholar
  14. Austruy, A., Wanat, N., Moussard, C., Vernay, P., Joussein, E., Ledoigt, G., et al. (2013). Physiological impacts of soil pollution and arsenic uptake in three plant species: Agrostis capillaris, Solanum nigrum and Vicia faba. Ecotoxicology and Environmental Safety, 90, 28–34.CrossRefGoogle Scholar
  15. Balasoiu, C. F., Zagury, G. J., & Deschenes, L. (2001). Partitioning and speciation of chromium, copper, and arsenic in CCA-contaminated soils: Influence of soil composition. Science of the Total Environment, 280(1–3), 239–255.CrossRefGoogle Scholar
  16. Bart, S., Motelica-Heino, M., Miard, F., Joussein, E., Soubrand, M., Bourgerie, S., et al. (2016). Phytostabilization of As, Sb and Pb by two willow species (S. viminalis and S. purpurea) on former mine technosols. CATENA, 136, 44–52.CrossRefGoogle Scholar
  17. Beesley, L., & Dickinson, N. (2011). Carbon and trace element fluxes in the pore water of an urban soil following greenwaste compost, woody and biochar amendments, inoculated with the earthworm Lumbricus terrestris. Soil Biology & Biochemistry, 43(1), 188–196.CrossRefGoogle Scholar
  18. Beesley, L., Moreno-Jiménez, E., & Gomez-Eyles, J. (2010). Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environmental Pollution, 158(6), 2282–2287.CrossRefGoogle Scholar
  19. Berti, W. W. R., & Cunningham, S. D. (2000). Phytostabilization of metals. In Phytoremediation of toxic metals: Using plants to clean-up the environment (pp. 71–88). New York: Wiley.Google Scholar
  20. Bradshaw, A. D., McNeilly, T. S., & Gregory, R. P. G. (1965). Industrialization, evolution and the development of heavy metal tolerance in plants. In Ecology and the industrial society (Vol. 5, pp. 327–343). Blackwell, Oxford.Google Scholar
  21. Caporale, A. G., Pigna, M., Sommella, A., Dynes, J. J., Cozzolino, V., & Violante, A. (2013). Influence of compost on the mobility of arsenic in soil and its uptake by bean plants (Phaseolus vulgaris L.) irrigated with arsenite-contaminated water. Journal of Environmental Management, 128, 837–843.CrossRefGoogle Scholar
  22. Cattani, I., Fragoulis, G., Boccelli, R., & Capri, E. (2006). Copper bioavailability in the rhizosphere of maize (Zea mays L.) grown in two Italian soils. Chemosphere, 64(11), 1972–1979.CrossRefGoogle Scholar
  23. Clemente, R., Hartley, W., Riby, P., Dickinson, N., & Lepp, N. (2010). Trace element mobility in a contaminated soil 2 years after field-amendment with a greenwaste compost mulch. Environmental Pollution, 158(5), 1644–1651.CrossRefGoogle Scholar
  24. Cui, L., Li, L., Zhang, A., Pan, G., Bao, D., & Chang, A. (2011). Biochar amendment greatly reduces rice Cd uptake in a contaminated paddy soil: A two-year field experiment. BioResources, 6(3), 2605–2618.Google Scholar
  25. Cutler, W. G., El-Kadi, A., Hue, N. V., Peard, J., Scheckel, K., & Ray, C. (2014). Iron amendments to reduce bioaccessible arsenic. Journal of Hazardous Materials, 279, 554–561.CrossRefGoogle Scholar
  26. Dai, H., Chen, Y., Yang, X., Cui, J., & Sui, P. (2017). The effect of different organic materials amendment on soil bacteria communities in barren sandy loam soil. Environmental Science and Pollution Research, 24, 24019–24028.CrossRefGoogle Scholar
  27. Deng, D. M., Shu, W. S., Zhang, J., Zou, H. L., Lin, Z., Ye, Z. H., et al. (2007). Zinc and cadmium accumulation and tolerance in populations of Sedum alfredii. Environmental Pollution, 147(2), 381–386.CrossRefGoogle Scholar
  28. Doubková, P., & Sudová, R. (2016). Limited impact of arbuscular mycorrhizal fungi on clones of Agrostis capillaris with different heavy metal tolerance. Applied Soil Ecology, 99, 78–88.CrossRefGoogle Scholar
  29. Egene, C. E., Van, R. P., Ok, Y. S., Meers, E., & Tack, F. M. G. (2018). Impact of organic amendments (biochar, compost and peat) on Cd and Zn mobility and solubility in contaminated soil of the Campine region after 3 years. The Science of the total environment, 626, 195–202.CrossRefGoogle Scholar
  30. Ernst, W. H. O. (1990). Mine vegetation in Europe. Heavy metal tolerance in plants: Evolutionary aspects, 18, 21–38.Google Scholar
  31. Fahr, M., Laplaze, L., El Mzibri, M., Doumas, P., Bendaou, N., Hocher, V., et al. (2015). Assessment of lead tolerance and accumulation in metallicolous and non-metallicolous populations of Hirschfeldia incana. Environmental and Experimental Botany, 109, 186–192.CrossRefGoogle Scholar
  32. Fresno, T., Moreno-Jiménez, E., & Peñalosa, J. M. (2016). Assessing the combination of iron sulfate and organic materials as amendment for an arsenic and copper contaminated soil. A chemical and ecotoxicological approach. Chemosphere, 165, 539–546.CrossRefGoogle Scholar
  33. Fresno, T., Moreno-Jiménez, E., Zornoza, P., & Peñalosa, J. M. (2018). Aided phytostabilisation of As-and Cu-contaminated soils using white lupin and combined iron and organic amendments. Journal of Environmental Management, 205, 142–150.CrossRefGoogle Scholar
  34. Fresno, T., Peñalosa, J. M., Santner, J., Puschenreiter, M., & Moreno-Jiménez, E. (2017). Effect of Lupinus albus L. root activities on As and Cu mobility after addition of iron-based soil amendments. Chemosphere, 182, 373–381.CrossRefGoogle Scholar
  35. Gunes, A., Pilbeam, D. J., & Inal, A. (2009). Effect of arsenic–phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. Plant and Soil, 314(1–2), 211–220.CrossRefGoogle Scholar
  36. Hartley, W., Dickinson, N. M., Riby, P., & Lepp, N. W. (2009). Arsenic mobility in brownfield soils amended with green waste compost or biochar and planted with Miscanthus. Environmental Pollution, 157(10), 2654–2662.CrossRefGoogle Scholar
  37. Hartley, W., Edwards, R., & Lepp, N. W. (2004). Arsenic and heavy metal mobility in iron oxide-amended contaminated soils as evaluated by short-and long-term leaching tests. Environmental Pollution, 131(3), 495–504.CrossRefGoogle Scholar
  38. Hego, E., Vilain, S., Barré, A., Claverol, S., Dupuy, J. W., Lalanne, C., et al. (2016). Copper stress-induced changes in leaf soluble proteome of Cu-sensitive and tolerant Agrostis capillaris L. populations. Proteomics, 16(9), 1386–1397.CrossRefGoogle Scholar
  39. Herath, I., Kumarathilaka, P., Navaratne, A., Rajakaruna, N., & Vithanage, M. (2014). Immobilization and phytotoxicity reduction of heavy metals in serpentine soil using biochar. Journal of Soils and Sediments, 15(1), 126–138.CrossRefGoogle Scholar
  40. Houba, V. J. G., Lexmond, Th. M., Novozamsky, I., & van der Lee, J. J. (1996). State of the art and future developments in soil analysis for bioavailability assessment. Science of the Total Environment, 178(1–3), 21–28.CrossRefGoogle Scholar
  41. Houben, D., Evrard, L., & Sonnet, P. (2013). Mobility, bioavailability and pH-dependent leaching of cadmium, zinc and lead in a contaminated soil amended with biochar. Chemosphere, 92(11), 1450–1457.CrossRefGoogle Scholar
  42. Huang, H., Yao, W., Li, R., Ali, A., Du, J., Guo, D., et al. (2017). Effect of pyrolysis temperature on chemical form, behavior and environmental risk of Zn, Pb and Cd in biochar produced from phytoremediation residue. Bioresource Technology, 249, 487–493.CrossRefGoogle Scholar
  43. Janus, A., Waterlot, C., Heymans, S., Deboffe, C., Douay, F., & Pelfrêne, A. (2018). Do biochars influence the availability and human oral bioaccessibility of Cd, Pb, and Zn in a contaminated slightly alkaline soil? Environmental Monitoring and Assessment, 190(4), 218.CrossRefGoogle Scholar
  44. Jiang, W., Hou, Q., Yang, Z., Zhong, C., Zheng, G., Yang, Z., et al. (2014). Evaluation of potential effects of soil available phosphorus on soil arsenic availability and paddy rice inorganic arsenic content. Environmental Pollution, 188, 159–165.CrossRefGoogle Scholar
  45. Kabir, E., Ray, S., Kim, K., Yoon, H., Jeon, E., Kim, Y., et al. (2012). Current status of trace metal pollution in soils affected by industrial activities. The Scientific World Journal, 2012, 1–18.CrossRefGoogle Scholar
  46. Khalid, S., Shahid, M., Niazi, N., Murtaza, B., Bibi, I., & Dumat, C. (2016). A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration, 182(Part B), 247–268.Google Scholar
  47. Khan, S., Waqas, M., Ding, F., Shamshad, I., Arp, H. P. H., & Li, G. (2015). The influence of various biochars on the bioaccessibility and bioaccumulation of PAHs and potentially toxic elements to turnips (Brassica rapa L.). Journal of Hazardous Materials, 300, 243–253.CrossRefGoogle Scholar
  48. Kidd, P., Barceló, J., Bernal, M., Navari-Izzo, F., Poschenrieder, C., Shilev, S., et al. (2009). Trace element behaviour at the root–soil interface: Implications in phytoremediation. Environmental and Experimental Botany, 67(1), 243–259.CrossRefGoogle Scholar
  49. Knight, B. P., Chaudri, A. M., McGrath, S. P., & Giller, K. E. (1998). Determination of chemical availability of cadmium and zinc in soils using inert soil moisture samplers. Environmental Pollution, 99(3), 293–298.CrossRefGoogle Scholar
  50. Kumpiene, J., Lagerkvist, A., & Maurice, C. (2008). Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments–a review. Waste Management, 28(1), 215–225.CrossRefGoogle Scholar
  51. Lebrun, M., Miard, F., Nandillon, R., Hattab-Hambli, N., Scippa, G. S., Bourgerie, S., et al. (2018). Eco-restoration of a mine technosol according to biochar particle size and dose application: study of soil physico-chemical properties and phytostabilization capacities of Salix viminalis. Journal of Soils and Sediments, 18(6), 2188–2202.CrossRefGoogle Scholar
  52. Lebrun, M., Miard, F., Nandillon, R., Scippa, G. S., Bourgerie, S., & Morabito, D. (2019). Biochar effect associated with compost and iron to promote Pb and As soil stabilization and Salix viminalis L. growth. Chemosphere, 222, 810–822.CrossRefGoogle Scholar
  53. Lehmann, C., & Rebele, F. (2004). 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.CrossRefGoogle Scholar
  54. Li, H., Liu, Y., Chen, Y., Wang, S., Wang, M., Xie, T., et al. (2016). Biochar amendment immobilizes lead in rice paddy soils and reduces its phytoavailability. Scientific Reports, 6, 31616.CrossRefGoogle Scholar
  55. Liu, L., Li, J., Yue, F., Yan, X., Wang, F., Bloszies, S., et al. (2018). Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere, 194, 495–503.CrossRefGoogle Scholar
  56. Liu, J., Schulz, H., Brandl, S., Miehtke, H., Huwe, B., & Glaser, B. (2012). Short-term effect of biochar and compost on soil fertility and water status of a Dystric Cambisol in NE Germany under field conditions. Journal of Plant Nutrition and Soil Science, 175(5), 698–707.CrossRefGoogle Scholar
  57. Lopareva-Pohu, A., Verdin, A., Garçon, G., Sahraoui, A. L. H., Pourrut, B., Debiane, D., et al. (2011). Influence of fly ash aided phytostabilisation of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environmental Pollution, 159(6), 1721–1729.CrossRefGoogle Scholar
  58. Lu, K., Yang, X., Shen, J., Robinson, B., Huang, H., Liu, D., et al. (2014). Effect of bamboo and rice straw biochars on the bioavailability of Cd, Cu, Pb and Zn to Sedum plumbizincicola. Agriculture, Ecosystems & Environment, 191, 124–132.CrossRefGoogle Scholar
  59. Mackie, K. A., Marhan, S., Ditterich, F., Schmidt, H. P., & Kandeler, E. (2015). The effects of biochar and compost amendments on copper immobilization and soil microorganisms in a temperate vineyard. Agriculture, Ecosystems & Environment, 201, 58–69.CrossRefGoogle Scholar
  60. Madejón, E., De Mora, A. P., Felipe, E., Burgos, P., & Cabrera, F. (2006). Soil amendments reduce trace element solubility in a contaminated soil and allow regrowth of natural vegetation. Environmental Pollution, 139(1), 40–52.CrossRefGoogle Scholar
  61. Mench, M., Bussiere, S., Boisson, J., Castaing, E., Vangronsveld, J., Ruttens, A., et al. (2003). Progress in remediation and revegetation of the barren Jales gold mine spoil after in situ treatments. Plant and Soil, 249(1), 187–202.CrossRefGoogle Scholar
  62. Méndez, A., Gómez, A., Paz-Ferreiro, J., & Gascó, G. (2012). Effects of sewage sludge biochar on plant metal availability after application to a Mediterranean soil. Chemosphere, 89(11), 1354–1359.CrossRefGoogle Scholar
  63. Meng, J., Tao, M., Wang, L., Liu, X., & Xu, J. (2018). Changes in heavy metal bioavailability and speciation from a Pb–Zn mining soil amended with biochars from co-pyrolysis of rice straw and swine manure. Science of the Total Environment, 633, 300–307.CrossRefGoogle Scholar
  64. Meyer, C. L., Kostecka, A. A., Saumitou-Laprade, P., Créach, A., Castric, V., Pauwels, M., et al. (2010). Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytologist, 185(1), 130–142.CrossRefGoogle Scholar
  65. Molnár, M., Vaszita, E., Farkas, É., Ujaczki, É., Fekete-Kertész, I., Tolner, M., et al. (2016). Acidic sandy soil improvement with biochar—A microcosm study. Science of the Total Environment, 563–564, 855–865.CrossRefGoogle Scholar
  66. Nandillon, R., Lahwegue, O., Miard, F., Lebrun, M., Gaillard, M., Sabatier, S., et al. (2019a). Potential use of biochar, compost and iron grit associated with Trifolium repens to stabilize Pb and As on a multi-contaminated technosol. Ecotoxicology and Environmental Safety, 182, 109432.CrossRefGoogle Scholar
  67. Nandillon, R., Lebrun, M., Miard, F., Gaillard, M., Sabatier, S., Villar, M., et al. (2019b). Capability of amendments (biochar, compost and garden soil) added to a mining technosol contaminated by Pb and As to allow poplar seed (Populus nigra L.) germination. Environmental Monitoring and Assessment, 191(7), 465.CrossRefGoogle Scholar
  68. Norini, M. P., Thouin, H., Miard, F., Battaglia-Brunet, F., Gautret, P., Guégan, R., et al. (2019). Mobility of Pb, Zn, Ba, As and Cd toward soil pore water and plants (willow and ryegrass) from a mine soil amended with biochar. Journal of Environmental Management, 232, 117–130.CrossRefGoogle Scholar
  69. Oustriere, N., Marchand, L., Galland, W., Gabbon, L., Lottier, N., Motelica, M., et al. (2016). Influence of biochars, compost and iron grit, alone and in combination, on copper solubility and phytotoxicity in a Cu-contaminated soil from a wood preservation site. Science of the Total Environment, 566–567, 816–825.CrossRefGoogle Scholar
  70. Oustriere, N., Marchand, L., Lottier, N., Motelica, M., & Mench, M. (2017a). Long-term Cu stabilization and biomass yields of Giant reed and poplar after adding a biochar, alone or with iron grit, into a contaminated soil from a wood preservation site. Science of the Total Environment, 579, 620–627.CrossRefGoogle Scholar
  71. Oustriere, N., Marchand, L., Rosette, G., Friesl-Hanl, W., & Mench, M. (2017b). Wood-derived-biochar combined with compost or iron grit for in situ stabilization of Cd, Pb, and Zn in a contaminated soil. Environmental Science and Pollution Research, 24(8), 7468–7481.CrossRefGoogle Scholar
  72. Park, J., Choppala, G., Bolan, N., Chung, J., & Chuasavathi, T. (2011). Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant and Soil, 348(1–2), 439–451.CrossRefGoogle Scholar
  73. Pérez-de-Mora, A., Madejón, P., Burgos, P., Cabrera, F., Lepp, N. W., & Madejón, E. (2011). Phytostabilization of semiarid soils residually contaminated with trace elements using by-products: Sustainability and risks. Environmental Pollution, 159(10), 3018–3027.CrossRefGoogle Scholar
  74. R Development Core Team. (2009). R: A language and environment for statistical omputing. Vienne: R foundation for statistical Computing.Google Scholar
  75. Redman, A. D., Macalady, D. L., & Ahmann, D. (2002). Natural organic matter affects arsenic speciation and sorption onto hematite. Environmental Science and Technology, 36(13), 2889–2896.CrossRefGoogle Scholar
  76. Remon, E. (2006). Tolérance et accumulation des métaux lourds par la végétation spontanée des friches métallurgiques: vers de nouvelles méthodes de bio-dépollution (Doctoral dissertation, Université Jean Monnet-Saint-Etienne).Google Scholar
  77. Renella, G., Landi, L., Ascher, J., Ceccherini, M. T., Pietramellara, G., Mench, M., et al. (2008). Long-term effects of aided phytostabilisation of trace elements on microbial biomass and activity, enzyme activities, and composition of microbial community in the Jales contaminated mine spoils. Environmental Pollution, 152(3), 702–712.CrossRefGoogle Scholar
  78. Rinklebe, J., Shaheen, S. M., & Frohne, T. (2016). Amendment of biochar reduces the release of toxic elements under dynamic redox conditions in a contaminated floodplain soil. Chemosphere, 142, 41–47.CrossRefGoogle Scholar
  79. Rodríguez-Seijo, A., Lago-Vila, M., Andrade, M. L., & Vega, F. A. (2016). Pb pollution in soils from a trap shooting range and the phytoremediation ability of Agrostis capillaris L. Environmental Science and Pollution Research, 23(2), 1312–1323.CrossRefGoogle Scholar
  80. Rodríguez-Vila, A., Forján, R., Guedes, R. S., & Covelo, E. F. (2017). Nutrient phytoavailability in a mine soil amended with technosol and biochar and vegetated with Brassica juncea. Journal of Soils and Sediments, 17(6), 1653–1661.CrossRefGoogle Scholar
  81. Stoltz, E., & Greger, M. (2002). Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environmental and Experimental Botany, 47(3), 271–280.CrossRefGoogle Scholar
  82. Sudová, R., Doubková, P., & Vosátka, M. (2008). Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: Combination of plant clones and fungal isolates from contaminated and uncontaminated substrates. Applied Soil Ecology, 40(1), 19–29.CrossRefGoogle Scholar
  83. Touceda-González, M., Álvarez-López, V., Prieto-Fernández, Á., Rodríguez-Garrido, B., Trasar-Cepeda, C., Mench, M., et al. (2017). Aided phytostabilisation reduces metal toxicity, improves soil fertility and enhances microbial activity in Cu-rich mine tailings. Journal of Environmental Management, 186, 301–313.CrossRefGoogle Scholar
  84. Vangronsveld, J., Colpaert, J. V., & Van Tichelen, K. K. (1996). Reclamation of a bare industrial area contaminated by non-ferrous metals: Physico-chemical and biological evaluation of the durability of soil treatment and revegetation. Environmental Pollution, 94(2), 131–140.CrossRefGoogle Scholar
  85. Walker, D. J., Clemente, R., & Bernal, M. P. (2004). Contrasting effects of manure and compost on soil pH, heavy metal availability and growth of Chenopodium album L. in a soil contaminated by pyritic mine waste. Chemosphere, 57(3), 215–224.CrossRefGoogle Scholar
  86. Warren, G. P., & Alloway, B. J. (2003). Reduction of arsenic uptake by lettuce with ferrous sulfate applied to contaminated soil. Journal of Environmental Quality, 32(3), 767–772.CrossRefGoogle Scholar
  87. Wu, F. Y., Leung, H. M., Wu, S. C., Ye, Z. H., & Wong, M. H. (2009). Variation in arsenic, lead and zinc tolerance and accumulation in six populations of Pteris vittata L. from China. Environmental Pollution, 157(8–9), 2394–2404.CrossRefGoogle Scholar
  88. Wu, F. Y., Ye, Z. H., Wu, S. C., & Wong, M. H. (2007). Metal accumulation and arbuscular mycorrhizal status in metallicolous and nonmetallicolous populations of Pteris vittata L. and Sedum alfredii Hance. Planta, 226(6), 1363–1378.CrossRefGoogle Scholar
  89. Yuan, P., Wang, J., Pan, Y., Shen, B., & Wu, C. (2019). Review of biochar for the management of contaminated soil: Preparation, application and prospect. Science of the Total Environment, 659, 473–490.CrossRefGoogle Scholar
  90. Zhou, R., Liu, X., Luo, L., Zhou, Y., Wei, J., Chen, A., et al. (2017). Remediation of Cu, Pb, Zn and Cd-contaminated agricultural soil using a combined red mud and compost amendment. International Biodeterioration and Biodegradation, 118, 73–81.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.INRA USC1328, LBLGC EA 1207University of OrleansOrléans Cedex 2France
  2. 2.IDDEA, Environmental Consulting EngineeringOlivetFrance
  3. 3.ISTO, UMR 7327BRGMOrléansFrance
  4. 4.Dipartimento di Bioscienze e TerritorioUniversity of MolisePescheItaly

Personalised recommendations