Cadmium immobilization in the soil and accumulation by spinach (Spinacia oleracea) depend on biochar types under controlled and field conditions

  • Muhammad Farooq Qayyum
  • Rabia Abdur Rehman
  • Seemab Liaqat
  • Muhammad Ikram
  • Shafaqat Ali
  • Muhammad RizwanEmail author
  • Muhammad Zia ur RehmanEmail author
  • Muhammad Zafar-ul-Hye
  • Qaiser Hussain
Part of the following topical collections:
  1. Implications of Biochar Application to Soil Environment under Arid Conditions


In the present study, efficiency of different biochars (BCs) on cadmium (Cd) immobilization and its bioavailability to spinach were investigated. In the first experiment, Cd-spiked soil was amended with treatments (T1 = control, T2 and T3 = cotton stalk biochar (CBC) 2% and 5%, T4 and T5 = rice straw biochar 2% and 5%) and incubated for 120 days. In the second experiment, spinach was grown in pots using three soils (a normal soil, a Cd-spiked soil, and a sewage-irrigated soil) after application of CBC and rice straw biochar (RBC) (2% w/w each) in each soil. In the field experiments, spinach was grown at two sites with six treatments including T0 = control, T1 and T2 (RBC 5 and 10 ton ha−1), T3 and T4 (CBC 5 and 10 ton ha−1). The results of our experiments showed a significant impact of BCs on soil pH, EC, soil organic matter, and Cd bioavailability. The plant growth parameters were also influenced positively by application of BC in both pot and field experiments. In field experiments, plant population and fresh biomass at different sites varied significantly. The Cd concentration in plants was lower when grown in treated soils. Moreover, there was a significant increase in soluble Si and phosphorus concentrations in plants and this had significant correlation with Cd concentration in plants.


Cadmium Biochar Silicon Immobilization Spinach 


Funding information

This study was funded by the International Foundation for Science Sweden and The Organization for the Prohibition of Chemical Weapons (OPCW) under grant number C-5591.

Supplementary material

12517_2019_4681_MOESM1_ESM.docx (15 kb)
ESM 1 (DOCX 14.7 kb)


  1. Abbas T, Rizwan M, Ali S, Zia-ur-Rehman M, Qayyum MF, Abbas F, Hannan F, Rinklebe J, Ok YS (2017) Effect of biochar on cadmium bioavailability and uptake in wheat (Triticum aestivum L.) grown in a soil with aged contamination. Ecotoxicol Environ Saf 140:37–47CrossRefGoogle Scholar
  2. Abbas T, Rizwan M, Ali S, Adrees M, Mahmood A, Zia-ur-Rehman M, Ibrahim M, Arshad M, Qayyum MF (2018) Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil. Ecotoxicol Environ Saf 148:825–833CrossRefGoogle Scholar
  3. Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum MF, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197. CrossRefGoogle Scholar
  4. Ahmed W, Ahmed A, Ahmad A et al (2012) Heavy metal contamination in vegetables grown in Rawalpindi, Pakistan. J Chem Soc Pakistan 34:914–919Google Scholar
  5. Alexander PD, Alloway BJ, Dourado AM (2006) Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ Pollut 144:736–745. CrossRefGoogle Scholar
  6. Ali B, Gill RA, Yang S, Gill MB, Ali S, Rafiq MT, Zhou W (2014a) Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotoxicol Environ Saf 110:197–207. CrossRefGoogle Scholar
  7. Ali B, Qian P, Jin R, Ali S, Khan M, Aziz R, Tian T, Zhou W (2014b) Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol Plant 58:131–138. CrossRefGoogle Scholar
  8. Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN (2017) Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res 24:12700–12712CrossRefGoogle Scholar
  9. Beesley L, Marmiroli M (2011) The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environ Pollut 159:474–480. CrossRefGoogle Scholar
  10. Bundschuh J, Litter MI, Parvez F, Román-Ross G, Nicolli HB, Jean JS, Liu CW, López D, Armienta MA, Guilherme LRG, Cuevas AG, Cornejo L, Cumbal L, Toujaguez R (2012) One century of arsenic exposure in Latin America: a review of history and occurrence from 14 countries. Sci Total Environ 429:2–35. CrossRefGoogle Scholar
  11. Callaghan TV, Lindley DK, Ali OM, Nour HAE, Bacon PJ (1989) The effect of water-absorbing synthetic polymers on the stomatal conductance, growth and survival of transplanted Eucalyptus microtheca seedlings in the Sudan. J Appl Ecol 26:663. CrossRefGoogle Scholar
  12. Cao X, Ma L, Gao B, Harris W (2009) Dairy-manure derived biochar effectively sorbs lead and atrazine. Environ Sci Technol 43:3285–3291CrossRefGoogle Scholar
  13. Chintala R, Mollinedo J, Schumacher TE, Malo DD, Julson JL (2014) Effect of biochar on chemical properties of acidic soil. Arch Agron Soil Sci 60:393–404. CrossRefGoogle Scholar
  14. Choppala GK, Bolan NS, Megharaj M, Chen Z, Naidu R (2011) The influence of biochar and black carbon on reduction and bioavailability of chromate in soils. J Environ Qual. CrossRefGoogle Scholar
  15. Cui Y, Zhu Y, Zhai R et al (2005) Exposure to metal mixtures and human health impacts in a contaminated area in Nanning, China. Environ Int 31:784–790. CrossRefGoogle Scholar
  16. Cui L, Li L, Zhang A et al (2011) Biochar amendment greatly reduces rice Cd uptake in a contaminated paddy soil: a two-year field experiment. BioResources 6:2605–2618Google Scholar
  17. Dalir N, Karimian N, Yasrebi J, Ronaghi A (2013) Chemical forms of cadmium in a calcareous soil treated with different levels of phosphorus and cadmium and planted to spinach. Arch Agron Soil Sci 59:559–571. CrossRefGoogle Scholar
  18. Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol Environ Saf 106:164–172. CrossRefGoogle Scholar
  19. Glaser B, Wiedner K, Seelig S, Schmidt HP, Gerber H (2014) Biochar organic fertilizers from natural resources as substitute for mineral fertilizers. Agron Sustain Dev 35:667–678. CrossRefGoogle Scholar
  20. Hernández T, Moreno JI, Costa F (1991) Influence of sewage sludge application on crop yields and heavy metal availability. Soil Sci Plant Nutr 37:201–210CrossRefGoogle Scholar
  21. Huang Y, He C, Shen C, Guo J, Mubeen S, Yuan J, Yang Z (2017) Toxicity of cadmium and its health risks from leafy vegetable consumption. Food Funct 8:1373–1401. CrossRefGoogle Scholar
  22. Hussain A, Murtaza G, Ghafoor A et al (2010) Cadmium contamination of soils and crops by long term use of raw effluent , ground and canal waters in agricultural lands. Int J Agric Biol 12:851–856Google Scholar
  23. Jabeen F, Aslam A, Salman M (2018) Heavy metals toxicity and associated health risks in vegetables grown under soil irrigated with sewage water. Univers J Agric Res 6:173–180. CrossRefGoogle Scholar
  24. Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, Chaurand P, Meunier JD (2015) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu. Planta 241:847–860CrossRefGoogle Scholar
  25. Khalil S, Kakar MK (2011) Agricultural use of untreated urban wastewater in Pakistan. Asian J Agric Rural Dev 1:21–26CrossRefGoogle Scholar
  26. Korndorfer GH, Snyder GH, Ulloa M et al (2001) Calibration of soil and plant silicon analysis for rice production. J Plant Nutr 24:1071–1084. CrossRefGoogle Scholar
  27. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428. CrossRefGoogle Scholar
  28. Ma YL, Matsunaka T (2013) Biochar derived from dairy cattle carcasses as an alternative source of phosphorus and amendment for soil acidity. Soil Sci Plant Nutr 59:628–641. CrossRefGoogle Scholar
  29. Maqbool A, Ali S, Rizwan M, Ishaque W, Rasool N, Rehman MZ, Bashir A, Abid M, Wu L (2018) Management of tannery wastewater for improving growth attributes and reducing chromium uptake in spinach through citric acid application. Environ Sci Pollut Res 25:10848–10856CrossRefGoogle Scholar
  30. McLaughlin H (2009) All biochars are not created equal , and how to tell them apart. In: North American Biochar Conference, Boulder, CO – August 2009. pp 1–36Google Scholar
  31. Muhammad N, Hussain M, Wahedullah KTA, Ali S, Ali A, Aziz R, Rafiq MK, Bachman RT, Al-Wabel MI, Rizwan M (2018) Biochar for sustainable soil and environment: a comprehensive review. Arab J Geosci 11:1–14CrossRefGoogle Scholar
  32. Murtaza G, Ghafoor A, Qadir M (2008) Accumulation and implications of cadmium , cobalt and manganese in soils and vegetables irrigated with city effluent. J Sci Food Agric 107:100–107. CrossRefGoogle Scholar
  33. Namgay T, Singh B, Singh BP (2010) Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize ( Zea mays L.). Aust J Soil Res 48:638. CrossRefGoogle Scholar
  34. Park JH, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348:439–451. CrossRefGoogle Scholar
  35. Qayyum MF, Abid M, Danish S et al (2015) Effects of various biochars on seed germination and carbon mineralization in an alkaline soil. Pak J Agric Sci 51:977–982Google Scholar
  36. Rangabhashiyam S, Anu N, Giri Nandagopal MS, Selvaraju N (2014) Relevance of isotherm models in biosorption of pollutants by agricultural byproducts. In: Relevance of isotherm models in biosorption of pollutants by agricultural byproducts. J. Environ. Chem, EngCrossRefGoogle Scholar
  37. Rehman MZ, Rizwan M, Ghafoor A et al (2015) Effect of inorganic amendments for in situ stabilization of cadmium in contaminated soils and its phyto-availability to wheat and rice under rotation. Environ Sci Pollut Res 22:16897–16906. CrossRefGoogle Scholar
  38. Rehman MZ, Khalid H, Akmal F, Ali S, Rizwan M, Qayyum MF, Iqbal M, Khalid MU, Azhar M (2017) Effect of limestone, lignite and biochar applied alone and combined on cadmium uptake in wheat and rice under rotation in an effluent irrigated field. Environ Pollut 227:560–568CrossRefGoogle Scholar
  39. Rehman MZ, Rizwan M, Khalid H, Ali S, Naeem A, Yousaf B, Liu G, Sabir M, Farooq M (2018) Farmyard manure alone and combined with immobilizing amendments reduced cadmium accumulation in wheat and rice grains grown in field irrigated with raw effluents. Chemosphere 199:468–476CrossRefGoogle Scholar
  40. Riaz M, Khan M, Ali S, Khan MD, Ahmed R, Khan MJ, Rizwan M (2018) Sugarcane waste straw biochar and its effects on calcareous soil and agronomic traits of okra. Arab J Geosci 11:1–7CrossRefGoogle Scholar
  41. Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016a) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879. CrossRefGoogle Scholar
  42. Rizwan M, Ali S, Qayyum MF, Ok YS, Zia-ur-Rehman M, Abbas Z, Hannan F (2016b) Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: a critical review. Environ Geochem Health 39:1–19. CrossRefGoogle Scholar
  43. Rizwan M, Ali S, Qayyum MF, Ibrahim M, Zia-ur-Rehman M, Abbas T, Ok YS (2016c) Mechanisms of biochar-mediated alleviation of toxicity of trace elements in plants: a critical review. Environ Sci Pollut Res 23:2230–2248. CrossRefGoogle Scholar
  44. Rizwan M, Meunier JD, Davidian JC, Pokrovsky OS, Bovet N, Keller C (2016d) Silicon alleviates Cd stress of wheat seedlings (Triticum turgidum L. cv. Claudio) grown in hydroponics. Environ Sci Pollut Res 23:1414–1427CrossRefGoogle Scholar
  45. Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang DC, Zia-ur-Rehman M, Zahir ZA, Rinklebe J, Tack FM, Ok YS (2017) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105CrossRefGoogle Scholar
  46. Rizwan M, Bakhsh A, Li X, Anjum L, Jamal K, Hamid S (2018a) Evaluation of the impact of water management technologies on water savings in the Lower Chenab Canal Command Area, Indus River Basin. Water 10:681. CrossRefGoogle Scholar
  47. Rizwan M, Ali S, Abbas T, Adrees M, Rehman MZ, Ibrahim M, Abbas F, Qayyum MF, Nawaz R (2018b) Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions. J Environ Manage 206:676–683CrossRefGoogle Scholar
  48. Sauvé S, Hendershot W, Allen HE (2000) Solid-solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environ Sci Technol 34:1125–1131. CrossRefGoogle Scholar
  49. Suppadit T, Kitikoon V, Phubphol A, Neumnoi P (2012) Effect of quail litter biochar on productivity of four new physic nut varieties planted in cadmium-contaminated soil. Chil J Agric Res 72:125–132. CrossRefGoogle Scholar
  50. Trakal L, Komárek M, Száková J, Zemanová V, Tlustoš P (2011) Biochar application to metal-contaminated soil: evaluating of Cd, Cu, Pb and Zn sorption behavior using single- and multi-element sorption experiment. Plant Soil Environ 57:372–380CrossRefGoogle Scholar
  51. Uchimiya M, Lima IM, Klasson KT, Wartelle LH (2010) Contaminant immobilization and nutrient release by biochar soil amendment : roles of natural organic matter. Chemosphere 80:935–940. CrossRefGoogle Scholar
  52. Uchimiya M, Wartelle LH, Klasson KT, Fortier CA, Lima IM (2011) Influence of pyrolysis temperature on biochar property and function as a heavy metal sorbent in soil. J Agric Food Chem 59:2501–2510. CrossRefGoogle Scholar
  53. Walkley A (1947) A critical examination of rapid method for determining organic in soils. J Soil Sci 63:252–254Google Scholar
  54. Xu X, Cao X, Zhao L, Wang H, Yu H, Gao B (2013) Removal of Cu, Zn, and Cd from aqueous solutions by the dairy manure-derived biochar. Environ Sci Pollut Res Int 20:358–368. CrossRefGoogle Scholar
  55. Xu G, Sun J, Shao H, Chang SX (2014) Biochar had effects on phosphorus sorption and desorption in three soils with differing acidity. Ecol Eng 62:54–60. CrossRefGoogle Scholar
  56. Younis U, Malik SA, Farooq Qayyum M et al (2015a) Biochar affects growth and biochemical activities of fenugreek ( rigonella corniculata ) in cadmium polluted soil. J Appl Bot Food Qual.
  57. Younis U, Qayyum MF, Shah MHR, Danish S, Shahzad AN, Malik SA, Mahmood S (2015b) Growth, survival, and heavy metal (Cd and Ni) uptake of spinach (Spinacia oleracea) and fenugreek (Trigonella corniculata) in a biochar-amended sewage-irrigated contaminated soil. J Plant Nutr Soil Sci 178:209–217. CrossRefGoogle Scholar
  58. Younis U, Malik SA, Rizwan M, Qayyum MF, Ok YS, Shah MH, Rehman RA, Ahmad N (2016) Biochar enhances the cadmium tolerance in spinach (Spinacia oleracea) through modification of Cd uptake and physiological and biochemical attributes. Environ Sci Pollut Res 23:21385–21394CrossRefGoogle Scholar
  59. Zhan F, Liu M, Guo M, Wu L (2004) Preparation of superabsorbent polymer with slow-release phosphate fertilizer. J Appl Polym Sci. 92:3417–3421. CrossRefGoogle Scholar

Copyright information

© Saudi Society for Geosciences 2019

Authors and Affiliations

  • Muhammad Farooq Qayyum
    • 1
  • Rabia Abdur Rehman
    • 1
  • Seemab Liaqat
    • 1
  • Muhammad Ikram
    • 1
  • Shafaqat Ali
    • 2
  • Muhammad Rizwan
    • 2
    Email author
  • Muhammad Zia ur Rehman
    • 3
    Email author
  • Muhammad Zafar-ul-Hye
    • 1
  • Qaiser Hussain
    • 4
  1. 1.Department of Soil Science, Faculty of Agricultural Sciences & TechnologyBahauddin Zakariya UniversityMultanPakistan
  2. 2.Department of Environmental Sciences and EngineeringGovernment College UniversityFaisalabadPakistan
  3. 3.Institute of Soil and Environmental SciencesUniversity of AgricultureFaisalabadPakistan
  4. 4.Department of Soil Science and Water Conservation DepartmentPMAS Arid Agricultural UniversityRawalpindiPakistan

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