Water, Air, & Soil Pollution

, 230:263 | Cite as

Effects of Walnut Leaves Biochars on Lead and Zinc Fractionation and Phytotoxicity in a Naturally Calcareous Highly Contaminated Soil

  • Parvin Kabiri
  • Hamidreza MotaghianEmail author
  • Alireza Hosseinpur
Full research paper


The aim of this study was to investigate the impact of incorporating Walnut leaves (WL) and their biochars produced at three temperatures (200, 400, and 600 °C) on fractionation, availability and maize indices in a naturally calcareous highly contaminated soil of Central Iran. A pot experiment was conducted considering soils treated with 0, 0.5, 1, and 2% (w/w) of WL and their derived biochars. After maize (Zea mays L.) planting, shoot and root dry matter and Pb and Zn concentration in shoots and roots and DTPA-extractable and fractions of Zn and Pb in soils were determined. Results showed showed that biochar amendments substantially modified the partitioning of Zn and Pb from easily available forms to less available forms. The results showed that DTPA-extractable of Zn and Pb and their bioaccumulation were reduced upon the addition of biochars produced at different temperatures and application rates in a calcareous soil. Treating soil with 2% biochar produced at 600 °C increased significantly shoot and root dry matter by 131.4% and 116.7%, respectively and reduced the bioavailability of Zn and Pb (DTPA-TEA extraction) by 49.1%, and 34.9%, respectively (P < 0.05) in comparison to the control. Therefore, biochars were able to reduce metals contamination in treatments and increase maize dry matter. Biochar decreased Zn and Pb concentration in plant tissues and promoted gradual maize growth responses through changing metals fractions. Therefore, biochar as a sorbent for contaminants can assist in maize to mitigate and phytostabilize Zn and Pb in highly contaminated soils.


Bioavailability Maize Phytostabilization Phytoremediation 


Funding information

This study supported by funds allocated by the Vice President for research of Shahrekord University.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11270_2019_4316_MOESM1_ESM.docx (740 kb)
ESM 1 (DOCX 739 kb)


  1. Ahmad, M., Moon, D. H., Vithanage, M., Koutsospyros, A., Lee, S. S., Yang, J. E., Lee, S. E., Jeon, C., & Ok, Y. S. (2014a). Production and use of biochar from buffalo weed (Ambrosia trifida L.) for trichloroethylene removal from water. Journal of Chemical Technology & Biotechnology, 89(1), 150–157.CrossRefGoogle Scholar
  2. Ahmad, M., Rajapaksha, A. U., Lim, J. E., Zhang, M., Bolan, N., Mohan, D., Vithanage, M., Lee, S. S., & Ok, Y. S. (2014b). Biochar as a sorbent for contaminant management in soil and water: a review. Chemosphere, 99, 19–33.CrossRefGoogle Scholar
  3. Ali, A., Guo, D., Zhang, Y., Sun, X., Jiang, S., Guo, Z., Huang, H., Liang, W., Li, R., & Zhang, Z. (2017). Using bamboo biochar with compost for the stabilization and phytotoxicity reduction of heavy metals in mine-contaminated soils of China. Scientific Reports, 7(1), 2690.CrossRefGoogle Scholar
  4. Al-Wabel, M. I., Al-Omran, A., El-Naggar, A. H., Nadeem, M., & Usman, A. R. (2013). Pyrolysis temperature induced changes in characteristics and chemical composition of biochar produced from conocarpus wastes. Bioresource Technology, 131, 374–379.CrossRefGoogle Scholar
  5. Al-Wabel, M. I., Usman, A. R. A., El-Naggar, A. H., Aly, A. A., Ibrahim, H. M., Elmaghraby, S., & Al-Omran, A. (2015). Conocarpus biochar as a soil amendment for reducing heavy metal availability and uptake by maize plants. Saudi Journal of Biological Sciences, 22, 503–511.Google Scholar
  6. ASTM. (2007). D1762–84: Standard Method for Chemical Analysis of Wood Charcoal. West Conshohocken: American Society for Testing and Materials international.Google Scholar
  7. Awasthi, A. K., Li, J., Pandey, A. K., & Khan, J. (2019). An overview of the potential of bioremediation for contaminated soil from municipal solid waste site. In Emerging and eco-friendly approaches for waste management (pp. 59–68). Singapore: Springer.CrossRefGoogle Scholar
  8. Beesley, L., & Marmiroli, M. (2011). The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environmental Pollution, 159, 474–480.CrossRefGoogle Scholar
  9. Bonanno, G. (2011). Trace element accumulation and distribution in the organs of Phragmites australis (common reed) and biomonitoring applications. Ecotoxicology and Environmental Safety, 74(4), 1057–1064.CrossRefGoogle Scholar
  10. Bonanno, G., & Giudice, R. L. (2010). Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecological Indicators, 10(3), 639–645.CrossRefGoogle Scholar
  11. Bourke, J., Manley-Harris, M., Fushimi, C., Dowaki, K., Nunoura, T., & Antal, M. J. (2007). Do all carbonized charcoals have the same chemical structure? 2. A model of the chemical structure of carbonized charcoal. Industrial & Engineering Chemistry, 46(18), 5954–5967.CrossRefGoogle Scholar
  12. Brewer, C. E., Hu, Y. Y., Schmidt-Rohr, K., Loynachan, T. E., Laird, D. A., & Brown, R. C. (2012). Extent of pyrolysis impacts on fast pyrolysis biochar properties. Journal of Environmental Quality, 41(4), 1115–1122.CrossRefGoogle Scholar
  13. Buscaroli, A. (2017). An overview of indexes to evaluate terrestrial plants for phytoremediation purposes. Ecological Indicators, 82, 367–380.CrossRefGoogle Scholar
  14. Campbell, C.R., & Plank, C.O. (1998). Preparation of plant tissue for laboratory analysis, in: Kalra, Y.P. (ed). Handbook of reference methods for plant analysis. CRC press. Pp. 37-50.Google Scholar
  15. Cao, X., Ma, L., Gao, B., & Harris, W. (2009). Dairy-manure derived biochar effectively sorbs lead and atrazine. Environmental Science & Technology, 43(9), 3285–3291.CrossRefGoogle Scholar
  16. Cheng, J., Li, Y., Gao, W., Chen, Y., Pan, W., Lee, X., & Tang, Y. (2018). Effects of biochar on Cd and Pb mobility and microbial community composition in a calcareous soil planted with tobacco. Biology and Fertility of Soils, 54(3), 373–383.CrossRefGoogle Scholar
  17. Chintala, R., Schumacher, T. E., McDonald, L. M., Clay, D. E., Malo, D. D., Papiernik, S. K., Clay, S. A., & Julson, J. (2014). Phosphorus sorption and availability from biochars and soil/biochar mixtures. Clean-Soil Air Water, 42(5), 626–634.CrossRefGoogle Scholar
  18. Crombie, K., Mašek, O., Sohi, S. P., Brownsort, P., & Cross, A. (2013). The effect of pyrolysis conditions on biochar stability as determined by three methods. GCB Bioenergy, 5(2), 122–131.CrossRefGoogle Scholar
  19. Dai, S., Li, H., Yang, Z., Dai, M., Dong, X., Ge, X., Sun, M., & Shi, L. (2018). Effects of biochar amendments on speciation and bioavailability of heavy metals in coal-mine-contaminated soil. Human and Ecological Risk Assessment: An International Journal, 24(7), 1–14.CrossRefGoogle Scholar
  20. Eid, E. M., & Shaltout, K. H. (2014). Monthly variations of trace elements accumulation and distribution in above-and below-ground biomass of Phragmites australis (Cav.) Trin. Ex Steudel in Lake Burullus (Egypt): a biomonitoring application. Ecological Engineering, 73, 17–25.CrossRefGoogle Scholar
  21. Fryda, L., & Visser, R. (2015). Biochar for soil improvement: evaluation of biochar from gasification and slow pyrolysis. Agriculture, 5(4), 1076–1115.CrossRefGoogle Scholar
  22. Gaskin, J. W., Steiner, C., Harris, K., Das, K. C., & Bibens, B. (2008). Effect of low-temperature pyrolysis conditions on biochar for agricultural use. Transactions of the ASABE, 51(6), 2061–2069.CrossRefGoogle Scholar
  23. Gee, G., & Bauder, J. (1986). Particle size analysis. In A. Klute (Ed.), Methods of soil analysis, part 1, physical and mineralogical methods 2nd ed. (pp. 404–407). Madison: American Society of Agronomy-Soil Science Society of America.Google Scholar
  24. Godo, G. H., & Reisenauer, H. M. (1980). Plant effect on soil manganese availability. Soil Science Society of America Journal, 44, 993–995.CrossRefGoogle Scholar
  25. 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
  26. Huang, M., Li, Z., Luo, N., Yang, R., Wen, J., Huang, B., & Zeng, G. (2019). Application potential of biochar in environment: Insight from degradation of biochar-derived DOM and complexation of DOM with heavy metals. Science of the Total Environment, 646, 220–228.CrossRefGoogle Scholar
  27. Jia, Y. F., Steele, C. J., Hayward, I. P., & Thomas, K. M. (1998). Mechanism of adsorption of gold and silver species on activated carbons. Carbon, 36(9), 1299–1308.CrossRefGoogle Scholar
  28. Jiang, J., Xu, R. K., Jiang, T. Y., & Li, Z. (2012). Immobilization of Cu(II), Pb(II) and Cd(II) by the addition of rice straw derived biochar to a simulated polluted Ultisol. Journal of Hazardous Materials, 229, 145–150.CrossRefGoogle Scholar
  29. Jones, J. R. J., & Case, V. W. (1990). Sampling, handling, and analyzing plant tissue samples. In R. L. Westerman (Ed.), Soil testing and plant analysis (pp. 389–428). SSSA/ASA: Madison (WI).Google Scholar
  30. Joseph, S.D., Downie, A., Munroe, P., Crosky, A., & Lehmann, J. (2007). Biochar for carbon sequestration, reduction of greenhouse gas emissions and enhancement of soil fertility; a review of the materials science. In: Proceedings of the Australian Combustion Symposium pp. 130–133.Google Scholar
  31. Kabata-Pendias, A., & Pendias, H. (2011). Trace elements in soils and plants. Third Ed. (p. 331). London: CRC Press. Boca Raton.Google Scholar
  32. Karami, N., Clemente, R., Moreno-Jiménez, E., Lepp, N. W., & Beesley, L. (2011). Efficiency of green waste compost and biochar soil amendments for reducing lead and copper mobility and uptake to ryegrass. Journal of Hazardous Materials, 191, 41–48.CrossRefGoogle Scholar
  33. Kumar, A., Tsechansky, L., Lew, B., Raveh, E., Frenkel, O., & Graber, E. R. (2018). Biochar alleviates phytotoxicity in Ficus elastica grown in Zn-contaminated soil. Science of the Total Environment, 618, 188–198.CrossRefGoogle Scholar
  34. Lehmann, J. (2007). A handful of carbon. Nature, 447, 143–144.CrossRefGoogle Scholar
  35. Lei, S., Shi, Y., Qiu, Y., Che, L., & Xue, C. (2019). Performance and mechanisms of emerging animal-derived biochars for immobilization of heavy metals. Science of the Total Environment, 646, 1281–1289.CrossRefGoogle Scholar
  36. Li, J. (2002). Ph.D. thesis. University of Western Australia. Perth.Google Scholar
  37. Liang, J., Yang, Z., Tang, L., Zeng, G., Yu, M., Li, X., Wu, H., Qian, Y., Li, X., & Luo, Y. (2017). Changes in heavy metal mobility and availability from contaminated wetland soil remediated with combined biochar-compost. Chemosphere, 181, 281–288.CrossRefGoogle Scholar
  38. 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, 421–428.CrossRefGoogle Scholar
  39. Liu, T., Liu, B., & Zhang, W. (2014). Nutrients and heavy metals in biochar produced by sewage sludge pyrolysis: Its application in soil amendment. Polish Journal of Environmental Studies, 23(1), 271–275.Google Scholar
  40. Liu, Y., He, Z., & Uchimiya, M. (2015). Comparison of biochar formation from various agricultural by-products using FTIR spectroscopy. Modern Applied Science, 9(4), 246–253.CrossRefGoogle Scholar
  41. Liu, H., Xu, F., Xie, Y., Wang, C., Zhang, A., Li, L., & Xu, H. (2018). Effect of modified coconut shell biochar on availability of heavy metals and biochemical characteristics of soil in multiple heavy metals contaminated soil. Science of the Total Environment, 645, 702–709.CrossRefGoogle Scholar
  42. Lu, Y., Zhu, F., Chen, J., Gan, H., & Guo, Y. (2007). Chemical fractionation of heavy metals in urban soils of Guangzhou, China. Environmental Monitoring and Assessment, 134, 429–439.CrossRefGoogle Scholar
  43. Lu, H., Zhang, W., Yang, Y., Huang, X., Wang, S., & Qiu, R. (2012). Relative distribution of Pb2+ sorption mechanisms by sludge-derived biochar. Water Research, 46(3), 854–862.CrossRefGoogle Scholar
  44. Lu, K., Yang, X., Gielen, G., Bolan, N., Ok, Y. S., Niazi, N. K., Xu, S., Yuan, G., Chen, X., Zhang, X., & Liu, D. (2017). Effect of bamboo and rice straw biochars on the mobility and redistribution of heavy metals (Cd, Cu, Pb and Zn) in contaminated soil. Journal of Environmental Management, 186, 285–292.CrossRefGoogle Scholar
  45. Lu, H. P., Li, Z. A., Gascó, G., Méndez, A., Shen, Y., & Paz-Ferreiro, J. (2018). Use of magnetic biochars for the immobilization of heavy metals in a multi-contaminated soil. Science of the Total Environment, 622, 892–899.CrossRefGoogle Scholar
  46. Lwin, C. S., Seo, B. H., Kim, H. U., Owens, G., & Kim, K. R. (2018). Application of soil amendments to contaminated soils for heavy metal immobilization and improved soil quality-a critical review. Journal of Soil Science and Plant Nutrition, 64, 156–167.CrossRefGoogle Scholar
  47. Ma, Y., & Rate, A. W. (2007). Metals adsorbed to charcoal are not identifiable by sequential extraction. Environmental Chemistry, 4(1), 26–34.CrossRefGoogle Scholar
  48. Marques, A. P., Oliveira, R. S., Rangel, A. O., & Castro, P. M. (2008). Application of manure and compost to contaminated soils and its effect on zinc accumulation by Solanum nigrum inoculated with arbuscular mycorrhizal fungi. Environmental Pollution, 151(3), 608–620.CrossRefGoogle Scholar
  49. Mohan, D., Abhishek, K., Sarswat, A., Patel, M., Singh, P., & Pittman, C. U. (2018). Biochar production and applications in soil fertility and carbon sequestration–a sustainable solution to crop-residue burning in India. RSC Advances, 8(1), 508–520.CrossRefGoogle Scholar
  50. Mosa, A. A., El-Ghamry, A., Al-Zahrani, H., Selim, E. M., & El-Khateeb, A. (2017). Chemically modified biochar derived from cotton stalks: characterization and assessing its potential for heavy metals removal from wastewater. Environment, Biodiversity and Soil Security, 1, 33–45.Google Scholar
  51. Motaghian, H. R., & Hosseinpur, A. R. (2015). Rhizosphere effects on Cu availability and fractionation in sewage sludge amended calcareous soils. Journal of Plant Nutrition and Soil Science, 178, 713–721.CrossRefGoogle Scholar
  52. Park, J. H., Choppala, G. K., Bolan, N. S., Chung, J. W., & Chuasavathi, T. (2011). Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant and Soil, 348, 439–451.CrossRefGoogle Scholar
  53. Park, J. H., Choppala, G., Lee, S. J., Bolan, N., Chung, J. W., & Edraki, M. (2013). Comparative sorption of Pb and cd by biochars and its implication for metal immobilization in soils. Water, Air and Soil Pollution, 224(12), 1711–1723.CrossRefGoogle Scholar
  54. Patra, J. M., Panda, S. S., & Dhal, N. K. (2017). Biochar as a low-cost adsorbent for heavy metal removal: A review. International Journal of Research in BioSciences, 6, 1–7.Google Scholar
  55. Ruiz, E., Alonso-Azcárate, J., Rodríguez, L., & Rincón, J. (2009). Assessment of metal availability in soils from a Pb-Zn mine site of south-Central Spain. Soil and Sediment Contamination, 18(5), 619–641.CrossRefGoogle Scholar
  56. Sarwar, N., Imran, M., Shaheen, M. R., Ishaque, W., Kamran, M. A., Matloob, A., Rehim, A., & Hussain, S. (2017). Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere, 171, 710–721.CrossRefGoogle Scholar
  57. Song, W., & Guo, M. (2012). Quality variations of poultry litter biochar generated at different pyrolysis temperatures. Journal of Analytical and Applied Pyrolysis, 94, 138–145.CrossRefGoogle Scholar
  58. Sparks, D. L., Page, A. L., Helmke, P. A., Loeppert, R. H., Soltanpour, P. N., Tabatabai, M. A., Johnston, C. T., & Sumner, M. E. (1996). Methods of soil analysis. In Part 3: Chemical methods. Madison: Soil Science Society of America.Google Scholar
  59. Sposito, G., Lund, L. J., & Chang, A. C. (1982). Trace metal chemistry in arid-zone field soils amended with sewage sludge: I. fractionation of Ni, Cu, Zn, Cd, and Pb in solid phases. Soil Science Society of America Journal, 46, 260–265.CrossRefGoogle Scholar
  60. Suliman, W., Harsh, J. B., Abu-Lail, N. I., Fortuna, A. M., Dallmeyer, I., & Garcia-Perez, M. (2016). Influence of feedstock source and pyrolysis temperature on biochar bulk and surface properties. Biomass and Bioenergy, 84, 37–48.CrossRefGoogle Scholar
  61. Tabachnick, B. G., & Fidell, L. S. (2012). Using multivariate statistics, 6th ed. (pp. 54–55). New Jersey: Pearson Publisher.Google Scholar
  62. Temminghoff, E. J. M., Van der Zee, S. E. A. T. M., & De Haan, F. A. M. (1998). Effects of dissolved organic matter on the mobility of copper in a contaminated sandy soil. Eurasian Journal of Soil Science, 49(4), 617–628.CrossRefGoogle Scholar
  63. Tessier, A., Campbell, P. G., & Bisson, M. (1979). Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51, 844–851.CrossRefGoogle Scholar
  64. Uchimiya, M. (2014). Changes in nutrient content and availability during the slow pyrolysis of animal wastes. In Z. He & H. Zhang (Eds.), Applied manure and nutrient chemistry for sustainable agriculture and environment (pp. 53–68). Dordrecht: Springer.CrossRefGoogle Scholar
  65. Uchimiya, M., Chang, S., & Klasson, K. T. (2011a). Screening biochars for heavy metal retention in soil: role of oxygen functional groups. Journal of Hazardous Materials, 190, 432–441.CrossRefGoogle Scholar
  66. Uchimiya, M., Wartelle, L. H., Klasson, K. T., Fortier, C. A., & Lima, I. M. (2011b). Influence of pyrolysis temperature on biochar property and function as a heavy metal sorbent in soil. Journal of Agricultural and Food Chemistry, 59(6), 2501–2510.CrossRefGoogle Scholar
  67. Uchimiya, M., Ohno, T., & He, Z. (2013). Pyrolysis temperature-dependent release of dissolved organic carbon from plant, manure, and biorefinery wastes. Journal of Analytical and Applied Pyrolysis, 104, 84–94.CrossRefGoogle Scholar
  68. Vamvuka, D., Sfakiotakis, S., & Pantelaki, O. (2019). Evaluation of gaseous and solid products from the pyrolysis of waste biomass blends for energetic and environmental applications. Fuel, 236, 574–582.CrossRefGoogle Scholar
  69. Weis, J. S., Glover, T., & Weis, P. (2004). Interactions of metals affect their distribution in tissues of Phragmites australis. Environmental Pollution, 131, 409–415.CrossRefGoogle Scholar
  70. Yathavakulasingam, T., Mikunthan, T., & Vithanage, M. (2016). Acceleration of lead phytostabilization by maize (Zea mays) in association with Gliricidiasepium biomass. Chemical and Environmental Systems Modeling Research Group. National Institute of Fundamental Studies, 2, 16–21.Google Scholar
  71. Zemberyova, M., Zwaik, A. A. H., & Farkasovska, I. (1998). Sequential extraction for the speciation of some heavy metals in soils. Journal of Radioanalytical and Nuclear Chemistry, 229, 56–71.CrossRefGoogle Scholar
  72. Zhang, G., Guo, X., Zhao, Z., He, Q., Wang, S., Zhu, Y., Yan, Y., Liu, X., Sun, K., Zhao, Y., & Qian, T. (2016). Effects of biochars on the availability of heavy metals to ryegrass in an alkaline contaminated soil. Environmental Pollution, 218, 513–522.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Soil Science, College of AgricultureShahrekord UniversityShahrekordIran

Personalised recommendations