Skip to main content

Advertisement

Log in

Co-culture of Salix viminalis and Trifolium repens for the phytostabilisation of Pb and As in mine tailings amended with hardwood biochar

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Metal(loid) soil pollution causes environmental and health issues, and thus those sites need to be remediated. This can be done through phytostabilization, in combination with biochar amendment. The objectives were to investigate the potential of Salix viminalis L. associated with Trifolium repens L. for the phytostabilization of biochar-amended contaminated soils by assessing (1) the tolerance of both plants to metal(loid)s, through the biomass production, (2) the concentrations of metal(loid)s in plant parts and (3) the concentrations of metal(loid)s in soil pore water and percolation waters. Results showed that plant growth affected soil pore water Physico-chemical properties and metal(loid) mobility. When comparing the mono- and poly-cultures, although pH was higher with the polyculture than the monoculture, the decrease in Pb mobility did not differ. Moreover, the leachate analysis showed that As concentration in the soil particles leached from the soil was higher in the polyculture condition, while Pb concentration was the highest in the willow vegetated condition. Finally, willow dry weight was not affected by the presence of clover, while clover dry weight was lower when it was grown with willow. In conclusion, the results showed that the willow and clover polyculture was not better than the monoculture of these two species for the phytomanagement of a former mine site amended with biochar.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arienzo, M., Adamo, P., & Cozzolino, V. (2004). The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. The Science of the Total Environment, 319, 13–25.

    Article  CAS  Google Scholar 

  • Badri, D. V., & Vivanco, J. M. (2009). Regulation and function of root exudates. Plant, Cell & Environment, 32(6), 666–681.

    Article  CAS  Google Scholar 

  • Bart, S., Motelica-Heino, M., Miard, F., Joussein, E., Soubrand, M., Bourgerie, S., & Morabito, D. (2016). Phytostabilization of As, Sb and Pb by two willow species (S. viminalis and S. purpurea) on former mine technosols. CATENA, 136, 44–52.

    Article  Google Scholar 

  • Beesley, L., Inneh, O. S., Norton, G. J., Moreno-Jimenez, E., Pardo, T., Clemente, R., & Dawson, J. J. C. (2014). Assessing the influence of compost and biochar amendments on the mobility and toxicity of metals and arsenic in a naturally contaminated mine soil. Environmental Pollution, 186, 195–202.

    Article  CAS  Google Scholar 

  • Beesley, L., Marmiroli, M., Pagano, L., Pigoni, V., Fellet, G., Fresno, T., Vamerali, T., Bandiera, M., & Marmiroli, N. (2013). Biochar addition to an arsenic contaminated soil increases arsenic concentrations in the pore water but reduces uptake to tomato plants (Solanum lycopersicum L.). Science of the Total Environment, 454–455, 598–603.

    Article  Google Scholar 

  • Ben Rebah, F., Prévost, D., & Tyagi, R. D. (2002). Growth of alfalfa in sludge amended soils and inoculated with rhizobia produced in sludge. Journal of Environmental Quality, 31, 1339–1348.

    Article  Google Scholar 

  • Bidar, G., Garçon, G., Pruvot, C., Dewaele, D., Cazier, F., Douay, F., & Shirali, P. (2007). Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: Plant metal concentration and phytotoxicity. Environmental Pollution, 147, 546–553.

    Article  CAS  Google Scholar 

  • Bolan, N., Kunhikrishnan, A., Thangarajana, R., Kumpiene, J., Park, J., Makino, T., Kirkham, M. B., & Scheckel, K. (2014). Remediation of heavy metal(loid)s contaminated soils or to immobilize? Journal of Hazardous Materials, 266, 141–166.

    Article  CAS  Google Scholar 

  • Bonanno, G. (2011). Trace element accumulation and distribution in the organs of Phragmites australis (common reed) and biomonitoring applications. Ecotoxicology and Environmental Safety, 74, 1057–1064.

    Article  CAS  Google Scholar 

  • Broos, K., Uyttebroek, M., Mertens, J., & Smolders, E. (2004). A survey of symbiotic nitrogen fixation by white clover grown on metal contaminated soils. Soil Biology & Biochemistry, 36, 633–640.

    Article  CAS  Google Scholar 

  • Cantrell, K., Hunt, P., Uchimiya, M., Novak, J., & Ro, K. (2012). Impact of pyrolysis temperature and manure source on physicochemical characteristics of biochar. Bioresource Technology, 107, 419–428.

    Article  CAS  Google Scholar 

  • Castaldi, P., Silvettia, M., Manzanob, R., Brundua, G., Roggeroa, P. P., & Garaua, G. (2018). Mutual effect of Phragmites australis, Arundo donax and immobilization agents on arsenic and trace metals phytostabilization in polluted soils. Geoderma, 314, 63–72.

    Article  CAS  Google Scholar 

  • Chen, G., Zou, X., Zhou, Y., Zhang, J., & Owens, G. (2014). A short-term study to evaluate the uptake and accumulation of arsenic in Asian willow (Salix sp.) from arsenic-contaminated water. Environmental Science and Pollution Research, 21, 3275–3284.

    Article  CAS  Google Scholar 

  • Chen, J., Shafi, M., Wang, Y., Wu, J., Ye, Z., Liu, C., Zhong, B., Guo, H., He, L., & Liu, D. (2016a). Organic acid compounds in root exudation of moso bamboo (Phyllostachys pubescens) and its bioactivity as affected by heavy metals. Environmental Science and Pollution Research, 23, 20977–20984.

    Article  CAS  Google Scholar 

  • Chen, L., Gao, S., Zhu, P., Liu, Y., Hu, T., & Zhang, J. (2013). Comparative study of metal resistance and accumulation of lead and zinc in two poplars. Physiologia Plantarum, 151, 390–405.

    Article  Google Scholar 

  • Chen, Z., Tian, Y., Zhang, Y., Song, B., Li, H., & Chen, Z. (2016b). Effects of root organic exudates on rhizosphere microbes and nutrient removal in the constructed wetlands. Ecological Engineering, 92, 243–250.

    Article  Google Scholar 

  • Chintala, R., Mollinedo, J., Schumacher, T., Malo, D., & Julson, J. (2013). Effect of biochar on chemical properties of acidic soil. Arch. Agron. Soil Sci., 60, 393–404.

    Article  Google Scholar 

  • Craven, D., Isbell, F., Manning, P., Connolly, J., Bruelheide, H., Ebeling, A., Roscher, C., van Ruijven, J., Weigelt, A., & Wilsey, B. (2016). Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought. Philosophical Transactions of the Royal Society of London. Series B, 371, 20150277.

    Article  Google Scholar 

  • Desjardins, D., Brereton, N. J. B., Marchand, L., Brisson, J., Pitre, F. E., & Labrecque, M. (2018). Complementarity of three distinctive phytoremediation crops for multiple-trace element contaminated soil. Science of the Total Environment, 610–611, 1428–1438.

    Article  Google Scholar 

  • Dhankher, O. P., Li, Y. J., Rosen, B. P., Shi, J., Salt, D. E., Senecoff, J. F., Sashti, N. A., & Meagher, R. B. (2002). Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma glutamylcysteine synthetase expression. Nature Biotechnology, 20, 1140–1145.

    Article  CAS  Google Scholar 

  • Dong, J., Mao, W., Zhang, G., Wu, F., & Cai, Y. (2007). Root excretion and plant tolerance to cadmium toxicity—A review. Plant, Soil and Environment, 53, 193–200.

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. The Scientific World Journal. 1–18.

  • Feng, Q., Zhang, Z., Chen, Y., Liu, L., Zhang, Z., & Chen, C. (2013). Adsorption and desorption characteristics of arsenic on soils: Kinetic, equilibrium, and effect of Fe(OH)3 colloid, H2SiO3 colloid and phosphate. Procedia Environmental Sciences, 18, 26–36.

    Article  CAS  Google Scholar 

  • Gerhardt, K., Gerwing, P., & Greenberg, B. (2017). Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Science, 256, 170–185.

    Article  CAS  Google Scholar 

  • 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, 1450–1457.

    Article  CAS  Google Scholar 

  • Houben, D., Pircar, J., & Sonnet, P. (2012). Heavy metal immobilization by cost-effective amendments in a contaminated soil: Effects on metal leaching and phytoavailability. Journal of Geochemical Exploration, 123, 87–94.

    Article  CAS  Google Scholar 

  • Kidd, P., Barceló, J., Bernal, M., Navari-Izzo, F., Poschenrieder, C., Shilev, S., Clemente, R., & Monterroso, C. (2009). Trace element behaviour at the root-soil interface: Implications in phytoremediation. Environmental and Experimental Botany, 67, 243–259.

    Article  CAS  Google Scholar 

  • Kouki, S., Saidi, N., & M’hiriHafiane, F. A. (2015). A comparative study of nutrients, cadmium, and chromium bioremoval efficiencies of three emergent macrophytes from a metal-contaminated wastewater. Clean: Soil, Air, Water, 43, 1531–1537.

    CAS  Google Scholar 

  • Laghlimi, M., Baghdad, B., Hadi, H. E., & Bouabdli, A. (2015). Phytoremediation mechanisms of heavy metal contaminated soils: A review. Journal of Ecology, 5, 375–388.

    Google Scholar 

  • Lebrun, M., Macri, C., Miard, F., Hattab-Hambli, N., Motelica-Heino, M., Morabito, D., & Bourgerie, S. (2017). Effect of biochar amendments on As and Pb mobility and phytoavailability in contaminated mine technosols phytoremediated by Salix. Journal of Geochemical Exploration, 182, 149–156.

    Article  CAS  Google Scholar 

  • Lebrun, M., Miard, F., Hattab-Hambli, N., Bourgerie, S., & Morabito, D. (2018a). Assisted phytoremediation of a multi-contaminated industrial soil using biochar and garden soil amendments associated with Salix alba or Salix viminalis: Abilities to stabilize As, Pb and Cu. Water, Air, and Soil Pollution, 229, 163.

    Article  Google Scholar 

  • Lebrun, M., Miard, F., Nandillon, R., Hattab-Hambli, N., Scippa, G. S., Bourgerie, S., & Morabito, D. (2018b). 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.

    Article  CAS  Google Scholar 

  • Lebrun, M., Miard, F., Nandillon, R., Léger, J. C., Hattab-Hambli, N., Scippa, G. S., Bourgerie, S., & Morabito, D. (2018c). Assisted phytostabilization of a multicontaminated mine technosol using biochar amendment: Early stage evaluation of biochar feedstock and particle size effects on As and Pb accumulation of two Salicaceae species (Salix viminalis and Populus euramericana). Chemosphere, 194, 316–326.

    Article  CAS  Google Scholar 

  • Li, L., Tilman, D., Lambers, H., & Zhang, F.-S. (2014). Plant diversity and over yielding: Insights from belowground facilitation of intercropping in agriculture. New Phytologist, 203, 63–69.

    Article  Google Scholar 

  • Lone, M. I., He, Z. L., Stoffella, P. J., & Yang, X. (2008). Phytoremediation of heavy metal polluted soils and water: Progress and perspectives. Journal of Zhejiang University Science B, 9, 210–220.

    Article  CAS  Google Scholar 

  • Lopareva-Pohu, A., Verdin, A., Garçon, G., Sahraoui, A. L. H., Pourrut, B., Debiane, D., Waterlot, C., Laruelle, F., Bidar, G., Douay, F., & Shirali, P. (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, 1721–1729.

    Article  CAS  Google Scholar 

  • Lu, Q., Li, J., Chen, F., Liao, M., Lin, L., Tang, Y., Liang, D., Xia, H., Yunsong Lai, Y., Wang, X., Chen, C., & Ren, W. (2017). Effects of mutual intercropping on the cadmium accumulation in accumulator plants Stellaria media, Malachium aquaticum, and Galium aparine. Environmental Monitoring and Assessment, 189, 622.

    Article  Google Scholar 

  • Luo, L., Qi, S., Peng, L., & Xie, X. (2017). Enhanced phytoremediation capacity of a mixed-species plantation of Eucalyptus globulus and Chickpeas. Journal of Geochemical Exploration, 182, 201–205.

    Article  CAS  Google Scholar 

  • Margesin, R. (2004). Bioremediation of petroleum TPHs-polluted soils in extreme temperature environments. Soil Biology, 1, 215–226.

    Article  CAS  Google Scholar 

  • Marks, E., Alcañiz, J., & Domene, X. (2014). Unintended effects of biochars on short term plant growth in a calcareous soil. Plant and Soil, 385, 87–105.

    Article  CAS  Google Scholar 

  • Mary, G. S., Sugumaran, P., Niveditha, S., Ramalakshmi, B., Ravichandran, P., & Seshadri, S. (2016). Production, characterization and evaluation of biochar from pod (Pisum sativum), leaf (Brassica oleracea) and peel (Citrus sinensis) wastes. The International Journal of Recycling of Organic Waste in Agriculture, 5, 43–53.

    Article  Google Scholar 

  • Mench, M., Lepp, N., Bert, V., Schwitzguébel, J. P., Gawronski, S. W., Schöder, P., & Vangronsveld, J. (2010). Successes and limitations of phytotechnologies at field scale: Outcomes, assessment and outlook from COST Action 859. Journal of Soils and Sediments, 10, 1039–1070.

    Article  CAS  Google Scholar 

  • Mench, M., Manceau, A., Vangronsveld, J., Clijsters, H., & Mocquot, B. (2000). Capacity of soil amendments in lowering the phytoavailability of sludge-borne zinc. Agron., 20, 383–397.

    Article  Google Scholar 

  • Molnàr, M., Vaszita, E., Farkas, E., Ujaczki, E., Fekete-Kertész, I., Tolner, H., Kleberez, O., Kirchkeszner, C., Gruiz, K., Uzinger, N., & Feigl, V. (2016). Acidic sandy soil improvement with biochar—A microcosm study. Science of the Total Environment, 563–564, 855–865.

    Article  Google Scholar 

  • Nagajyoti, P., Lee, K., & Sreekanth, T. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters, 8, 199–216.

    Article  CAS  Google Scholar 

  • Nandillon R, Lahwegue O, Miard F, Lebrun M, Gaillard M, Sabatier S, Battaglia-Brunet F, Morabito D Bourgerie S (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.

  • Nandillon R, Lebrun M, Miard F, Gaillard M, Sabatier S, Villar M, Bourgerie S, Morabito D (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.

  • Nandillon R, Miard F, Lebrun M, Gaillard M, Sabatier S, Bourgerie S, Battaglia-Brunet F, Morabito D (2019c) Effect of Biochar and Amendments on Pb and As Phytotoxicity and Phytoavailability in a Technosol. CLEAN–Soil, Air, Water, 47(3): 1800220.

  • Ogundiran, M. B., Mekwunyeia, N. S., & Adejumo, S. A. (2018). Compost and biochar assisted phytoremediation potentials of Moringa oleifera for remediation of lead contaminated soil. J. of Environ. Chem. Eng., 6, 2206–2213.

    Article  CAS  Google Scholar 

  • Paz-Ferreiro, J., Lu, H., Fu, S., Mendez, A., & Gasco, G. (2014). Use of phytoremediation and biochar to remediate heavy metal polluted soils: A review. Solid Earth, 5(1), 65–75.

    Article  Google Scholar 

  • Pérez-Esteban, J., Escolasito, C., Moliner, A., Masaguer, A., & Ruiz-Fernandez, J. (2014). Phytostabilization of metals in mine soils using Brassica juncea in combination with organic amendments. Plant and Soil, 377, 97–109.

    Article  Google Scholar 

  • Pourrut, B., Shahid, M., Dumat, C., Winterton, P., & Pinelli,. (2011). Eric lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology, 213, 113–136.

    CAS  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. R foundation for statistical Computing, Vienne, Austria.

  • Rees, F., Germain, C., Sterckeman, T., & Morel, J. L. (2015). Plant growth and metal uptake by a non-hyperaccumulating species (Lolium perenne) and a Cd-Zn hyperaccumulator (Noccaea caerulescens) in contaminated soils amended with biochar. Plant and Soil, 395, 57–73.

    Article  CAS  Google Scholar 

  • Reubens, B., Poesen, J., Danjon, F., Geudens, G., & Muys, B. (2007). The role of fine and coarse roots in shallow slope stability and soil erosion control with a focus on root system architecture: A review. Trees-Struct. Funct., 21, 385–402.

    Article  Google Scholar 

  • Salam, M. M. A., Kaipiainen, E., Mohsin, M., Villa, A., Kuittinen, S., Pulkkinen, P., Pelkonen, P., Mehtätalo, L., & Pappinen, A. (2016). Effects of contaminated soil on the growth performance of young Salix (Salix schwerinii E. L. Wolf) and the potential for phytoremediation of heavy metals. Journal of Environmental Management, 183, 467–477.

    Article  CAS  Google Scholar 

  • Seshadri, B., Bolan, N., & Naidu, R. (2015). Rhizosphere-induced heavy metal (loid) transformation in relation to bioavailability and remediation. Journal of Soil Science and Plant Nutrition, 15, 524–548.

    Google Scholar 

  • Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation: Role of synthetic and natural organic ligands. Journal of Hazardous Materials, 219–220.

  • Stolte, J., Tesfai, M., Oygarden, L., Kvaerno, S., Keizer, J., Verheijen, F., Panagos, P., Ballabio, C. and Hessel, R. (2016). Soil threats in Europe: status, methods, drivers and effects on ecosystem services: Deliverable 2.1 RECARE project. European Commission DG Joint Research Centre.

  • Uren, N. C. (2007). Types, Amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In R. Pinton, Z. Varanini, & P. Nannipieri (Eds.), The rhizosphere: Biochemistry and organic substances at the soil-plant interface (pp. 1–21). Taylor and Francis Group.

    Google Scholar 

  • Yin, D., Wang, X., Chen, C., Peng, B., Tan, C., & Li, H. (2016). Varying effect of biochar on Cd, Pb and As mobility in a multi-metal contaminated paddy soil. Chemistry, 152, 196–206.

    CAS  Google Scholar 

  • Zhang, H., & Selim, H. M. (2008). Reaction and transport of arsenic in soils: Equilibrium and kinetic modelling. Advances in Agronomy, 98, 45–115.

    Article  CAS  Google Scholar 

  • Zimmer, D., Kruse, J., Baum, C., Borca, C., Laue, M., Hause, G., Meissner, R., & Leinweber, P. (2011). Spatial distribution of arsenic and heavy metals in willow roots from a contaminated floodplain soil measured by X-ray fluorescence spectroscopy. Science of the Total Environment, 409, 4094–4100.

    CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Ingrid Girardeau and Louis De Lary De Latour (DPSM/BRGM) for giving us the authorization to study the former Pontgibaud mine and Mr. JC. Léger (La Carbonerie) for the supply of biochar. We also wanted to thank the National Association of Research and Technology (ANRT) for funding R. Nandillon's thesis.

Funding

National Association of Research and Technology (ANRT) for funding R. Nandillon's thesis.

Author information

Authors and Affiliations

Authors

Contributions

RN & ML contributed to conceptualization, methodology, and writing-original draft. FM was involved in methodology. MG & SS contributed to validation. FB-B, DM & SB were involved in conceptualization, validation, supervision, writing-review, and editing.

Corresponding author

Correspondence to Sylvain Bourgerie.

Ethics declarations

Consent to participate

Not applicable.

Data availability

Not applicable.

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nandillon, R., Lebrun, M., Miard, F. et al. Co-culture of Salix viminalis and Trifolium repens for the phytostabilisation of Pb and As in mine tailings amended with hardwood biochar. Environ Geochem Health 44, 1229–1244 (2022). https://doi.org/10.1007/s10653-021-01153-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-021-01153-0

Keywords

Navigation