Environmental Science and Pollution Research

, Volume 25, Issue 17, pp 16991–17001 | Cite as

Reduced bioavailability and plant uptake of polycyclic aromatic hydrocarbons from soil slurry amended with biochars pyrolyzed under various temperatures

  • Xiaomin Zhu
  • Yinshan Wang
  • Yuecan Zhang
  • Baoliang Chen
Research Article


Biochar has high potential for organic pollutant immobilization due to its powerful sorption capacity. Nevertheless, potential risks may exist when biochar-sorbed organic pollutants are bioavailable. A direct plant exposure assay in combination with an organic solvent extraction experiment was carried out in this study to investigate the bioavailability of polycyclic aromatic hydrocarbons (PAHs) with the application of pine needle biochars pyrolyzed under different temperatures (100, 300, 400, and 700 °C; referred as P100–P700 accordingly). Biochar reduced solvent extractability and plant uptake of PAHs including naphthalene (Naph), acenaphthene (Acen), phenanthrene (Phen), and pyrene (Pyr), especially for three- and four-ring PAHs (Phen and Pyr) with high-temperature biochar. Plant uptake assay validates with organic solvent extraction for bioavailability assessment. Sorption of PAHs to biochars reduced plant uptake of PAHs in roots and shoots by lowering freely dissolved PAHs. Aging process reduced the bioavailability of PAHs that were bound to biochar. High pyrolysis temperature can be recommended for biochar preparation for purpose of effectively immobilizing PAHs, whereas application of moderate-temperature biochar for PAH immobilization should concern the potential risks of desorption and bioavailability of PAHs.


Biochar Polycyclic aromatic hydrocarbons Bioavailability Plant uptake Aging Pyrolysis temperature 



This project was supported by the National Natural Science Foundation of China (Grant nos. 21425730, 21537005, 21621005, and 21607125), the National Basic Research Program of China (Grant no. 2014CB441106), and the Postdoctoral Science Foundation of China (Grant no. 2015M581943).

Supplementary material

11356_2018_1874_MOESM1_ESM.doc (71 kb)
ESM 1 (DOC 71 kb)


  1. Abelmann K, Kleineidam S, Knicker H, Grathwohl P, Kogel-Knabner I (2005) Sorption of HOC in soils with carbonaceous contamination: influence of organic-matter composition. J Plant Nutr Soil Sci 168:293–306CrossRefGoogle Scholar
  2. Ahmad M, Rajapaksha AU, Lim JE, Zhang M, Bolan N, Mohan D, Vithanage M, Lee SS, Ok YS (2014) Biochar as a sorbent for contaminant management in soil and water: a review. Chemosphere 99:19–33CrossRefGoogle Scholar
  3. Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265CrossRefGoogle Scholar
  4. Beesley L, Moreno-Jimenez E, Gomez-Eyles JL, Harris E, Robinson B, Sizmur T (2011) A review of biochars' potential role in the remediation, revegetation and restoration of contaminated soils. Environ Pollut 159:3269–3282CrossRefGoogle Scholar
  5. Cai JJ, Song JH, Lee Y, Lee DS (2014) Assessment of climate change impact on the fates of polycyclic aromatic hydrocarbons in the multimedia environment based on model prediction. Sci Total Environ 470:1526–1536CrossRefGoogle Scholar
  6. Cai QY, Mo CH, Wu QT, Katsoyiannis A, Zeng QY (2008) The status of soil contamination by semivolatile organic chemicals (SVOCs) in China: a review. Sci Total Environ 389:209–224CrossRefGoogle Scholar
  7. Cao X, Harris W (2010) Properties of dairy-manure-derived biochar pertinent to its potential use in remediation. Bioresour Technol 101:5222–5228CrossRefGoogle Scholar
  8. Cao XD, Ma LN, Gao B, Harris W (2009) Dairy-manure derived biochar effectively sorbs lead and atrazine. Environ Sci Technol 43:3285–3291CrossRefGoogle Scholar
  9. Chen B, Zhou D, Zhu L (2008a) Transitional adsorption and partition of nonpolar and polar aromatic contaminants by biochars of pine needles with different pyrolytic temperatures. Environ Sci Technol 42:5137–5143CrossRefGoogle Scholar
  10. Chen B, Zhou D, Zhu L, Shen X (2008b) Sorption characteristics and mechanisms of organic contaminant to carbonaceous biosorbents in aqueous solution. Sci China B 51:464–472CrossRefGoogle Scholar
  11. Chen B, Yuan M (2011) Enhanced sorption of polycyclic aromatic hydrocarbons by soil amended with biochar. J Soils Sed 11:62–71CrossRefGoogle Scholar
  12. Chen B, Yuan M, Qian L (2012a) Enhanced bioremediation of PAH-contaminated soil by immobilized bacteria with plant residue and biochar as carriers. J Soils Sed 12:1350–1359CrossRefGoogle Scholar
  13. Chen BL, Xuan XD, Zhu LZ, Wang J, Gao YZ, Yang K, Shen XY, Lou BF (2004) Distributions of polycyclic aromatic hydrocarbons in surface waters, sediments and soils of Hangzhou City, China. Water Res 38:3558–3568CrossRefGoogle Scholar
  14. Chen S, Ke RH, Zha JM, Wang ZJ, Khan SU (2008c) Influence of humic acid on bioavailability and toxicity of benzo k fluoranthene to Japanese Medaka. Environ Sci Technol 42:9431–9436CrossRefGoogle Scholar
  15. Chen Z, Chen B, Chiou CT (2012b) Fast and slow rates of naphthalene sorption to biochars produced at different temperatures. Environ Sci Technol 46:11104–11111CrossRefGoogle Scholar
  16. Chen Z, Chen B, Zhou D, Chen W (2012c) Bisolute sorption and thermodynamic behavior of organic pollutants to biomass-derived biochars at two pyrolytic temperatures. Environ Sci Technol 46:12476–12483CrossRefGoogle Scholar
  17. Chiou CT, Cheng J, Hung W-N, Chen B, Lin T-F (2015) Resolution of adsorption and partition components of organic compounds on black carbons. Environ Sci Technol 49:9116–9123CrossRefGoogle Scholar
  18. Cornelissen G, Gustafsson O, Bucheli TD, Jonker MTO, Koelmans AA, Van Noort PCM (2005) Extensive sorption of organic compounds to black carbon, coal, and kerogen in sediments and soils: mechanisms and consequences for distribution, bioaccumulation, and biodegradation. Environ Sci Technol 39:6881–6895CrossRefGoogle Scholar
  19. Dettenmaier EM, Doucette WJ, Bugbee B (2009) Chemical hydrophobicity and uptake by plant roots. Environ Sci Technol 43:324–329CrossRefGoogle Scholar
  20. Doick KJ, Dew NM, Semple KT (2005) Linking catabolism to cyclodextrin extractability: determination of the microbial availability of PAHs in soil. Environ Sci Technol 39:8858–8864CrossRefGoogle Scholar
  21. Fabbri D, Rombola AG, Torri C, Spokas KA (2013) Determination of polycyclic aromatic hydrocarbons in biochar and biochar amended soil. J Anal Appl Pyrolysis 103:60–67CrossRefGoogle Scholar
  22. Freddo A, Cai C, Reid BJ (2012) Environmental contextualisation of potential toxic elements and polycyclic aromatic hydrocarbons in biochar. Environ Pollut 171:18–24CrossRefGoogle Scholar
  23. Gao YZ, Collins CD (2009) Uptake pathways of polycyclic aromatic hydrocarbons in white clover. Environ Sci Technol 43:6190–6195CrossRefGoogle Scholar
  24. Han X-M, Liu Y-R, Zheng Y-M, Zhang X-X, He J-Z (2014) Response of bacterial pdo1, nah, and C12O genes to aged soil PAH pollution in a coke factory area. Environ Sci Pollut Res 21:9754–9763CrossRefGoogle Scholar
  25. Hauck M, Huijbregts MAJ, Koelmans AA, Moermond CTA, van den Heuvel-Greve MJ, Veltman K, Hendriks AJ, Vethaak AD (2007) Including sorption to black carbon in modeling bioaccumulation of polycyclic aromatic hydrocarbons: uncertainty analysis and comparison to field data. Environ Sci Technol 41:2738–2744CrossRefGoogle Scholar
  26. Jeffery S, Bezemer TM, Cornelissen G, Kuyper TW, Lehmann J, Mommer L, Sohi SP, van de Voorde TFJ, Wardle DA, van Groenigen JW (2015) The way forward in biochar research: targeting trade-offs between the potential wins. Glob Change Biol Bioenergy 7:1–13CrossRefGoogle Scholar
  27. Jeong S, Wander MM, Kleineidam S, Grathwohl P, Ligouis B, Werth CJ (2008) The role of condensed carbonaceous materials on the sorption of hydrophobic organic contaminants in subsurface sediments. Environ Sci Technol 42:1458–1464CrossRefGoogle Scholar
  28. Kang SH, Xing BS (2005) Phenanthrene sorption to sequentially extracted soil humic acids and humins. Environ Sci Technol 39:134–140CrossRefGoogle Scholar
  29. Khan S, Wang N, Reid BJ, Freddo A, Cai C (2013) Reduced bioaccumulation of PAHs by Lactuca satuva L. grown in contaminated soil amended with sewage sludge and sewage sludge derived biochar. Environ Pollut 175:64–68CrossRefGoogle Scholar
  30. Koltowski M, Hilber I, Bucheli TD, Oleszczuk P (2016) Effect of activated carbon and biochars on the bioavailability of polycyclic aromatic hydrocarbons in different industrially contaminated soils. Environ Sci Pollut Res 23:11058–11068CrossRefGoogle Scholar
  31. Kusmierz M, Oleszczuk P (2014) Biochar production increases the polycyclic aromatic hydrocarbon content in surrounding soils and potential cancer risk. Environ Sci Pollut Res 21:3646–3652CrossRefGoogle Scholar
  32. Lamichhane S, Krishna KCB, Sarukkalige R (2016) Polycyclic aromatic hydrocarbons (PAHs) removal by sorption: a review. Chemosphere 148:336–353CrossRefGoogle Scholar
  33. Lehmann J (2007) A handful of carbon. Nature 447:143–144CrossRefGoogle Scholar
  34. Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota - a review. Soil Biol Biochem 43:1812–1836CrossRefGoogle Scholar
  35. Liu L, Chen P, Sun M, Shen G, Shang G (2015) Effect of biochar amendment on PAH dissipation and indigenous degradation bacteria in contaminated soil. J Soils Sed 15:313–322CrossRefGoogle Scholar
  36. Lu L, Zhu L (2009) Reducing plant uptake of PAHs by cationic surfactant-enhanced soil retention. Environ Pollut 157:1794–1799CrossRefGoogle Scholar
  37. Luo L, Lin S, Huang HL, Zhang SZ (2012) Relationships between aging of PAHs and soil properties. Environ Pollut 170:177–182CrossRefGoogle Scholar
  38. Marques M, Mari M, Audi-Miro C, Sierra J, Soler A, Nadal M, Domingo JL (2016) Climate change impact on the PAH photodegradation in soils: characterization and metabolites identification. Environ Int 89-90:155–165CrossRefGoogle Scholar
  39. McLeod PB, Luoma SN, Luthy RG (2008) Biodynamic modeling of PCB uptake by Macoma balthica and Corbicula fluminea from sediment amended with activated carbon. Environ Sci Technol 42:484–490CrossRefGoogle Scholar
  40. Millward RN, Bridges TS, Ghosh U, Zimmerman JR, Luthy RG (2005) Addition of activated carbon to sediments to reduce PCB bioaccumulation by a polychaete (Neanthes arenaceodentata) and an amphipod (Leptocheirus plumulosus). Environ Sci Technol 39:2880–2887CrossRefGoogle Scholar
  41. Northcott GL, Jones KC (2001) Partitioning, extractability, and formation of nonextractable PAH residues in soil. 1. Compound differences in aging and sequestration. Environ Sci Technol 35:1103–1110CrossRefGoogle Scholar
  42. Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986CrossRefGoogle Scholar
  43. Ogbonnaya OU, Adebisi OO, Semple KT (2014) The impact of biochar on the bioaccessibility of C-14-phenanthrene in aged soil. Envion Sci Process Impact 16:2635–2643CrossRefGoogle Scholar
  44. Oleszczuk P, Hale SE, Lehmann J, Cornelissen G (2012) Activated carbon and biochar amendments decrease pore-water concentrations of polycyclic aromatic hydrocarbons (PAHs) in sewage sludge. Bioresour Technol 111:84–91CrossRefGoogle Scholar
  45. Oleszczuk P, Josko I, Kusmierz M, Futa B, Wielgosz E, Ligeza S, Pranagal J (2014) Microbiological, biochemical and ecotoxicological evaluation of soils in the area of biochar production in relation to polycyclic aromatic hydrocarbon content. Geoderma 213:502–511CrossRefGoogle Scholar
  46. Olson PE, Castro A, Joern M, DuTeau NM, Pilon-Smits E, Reardon KF (2008) Effects of agronomic practices on phytoremediation of an aged PAH-contaminated soil. J Environ Qual 37:1439–1446CrossRefGoogle Scholar
  47. Quilliam RS, Rangecroft S, Emmett BA, Deluca TH, Jones DL (2013) Is biochar a source or sink for polycyclic aromatic hydrocarbon (PAH) compounds in agricultural soils? Glob Change Biol Bioenergy 5:96–103CrossRefGoogle Scholar
  48. Reid BJ, Stokes JD, Jones KC, Semple KT (2000) Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ Sci Technol 34:3174–3179CrossRefGoogle Scholar
  49. Ren X, Sun H, Wang F, Cao F (2016) The changes in biochar properties and sorption capacities after being cultured with wheat for 3 months. Chemosphere 144:2257–2263Google Scholar
  50. Renner R (2007) Rethinking biochar. Environ Sci Technol 41:5932–5933CrossRefGoogle Scholar
  51. Singh S, Vashishth A, Vishal (2011) PAHs in some brands of tea. Environ Monit Assess 177:35–38CrossRefGoogle Scholar
  52. Smith KEC, Thullner M, Wick LY, Harms H (2009) Sorption to humic acids enhances polycyclic aromatic hydrocarbon biodegradation. Environ Sci Technol 43:7205–7211CrossRefGoogle Scholar
  53. Styrishave B, Mortensen M, Krogh PH, Andersen O, Jensen J (2008) Solid-phase microextraction (SPME) as a tool to predict the bioavailahility and toxicity of pyrene to the springtail, Folsomia candida, under various soil conditions. Environ Sci Technol 42:1332–1336CrossRefGoogle Scholar
  54. Sun D, Meng J, Chen W (2013a) Effects of abiotic components induced by biochar on microbial communities. Acta Agricul Scandinavica B 63:633–641Google Scholar
  55. Sun K, Kang M, Zhang Z, Jin J, Wang Z, Pan Z, Xu D, Wu F, Xing B (2013b) Impact of Deashing treatment on biochar structural properties and potential sorption mechanisms of Phenanthrene. Environ Sci Technol 47:11473–11481CrossRefGoogle Scholar
  56. Tang J, Petersen EJ, Huang Q, Weber WJ Jr (2007) Development of engineered natural organic sorbents for environmental applications: 3. Reducing PAH mobility and bioavailability in contaminated soil and sediment systems. Environ Sci Technol 41:2901–2907CrossRefGoogle Scholar
  57. Tao S, Xu FL, Liu WX, Cui YH, Coveney RM (2006) A chemical extraction method for mimicking bioavailability of polycyclic aromatic hydrocarbons to wheat grown in soils containing various amounts of organic matter. Environ Sci Technol 40:2219–2224CrossRefGoogle Scholar
  58. Tao Y, Zhang S, Zhu Y-G, Christie P (2009) Uptake and acropetal translocation of polycyclic aromatic hydrocarbons by wheat (Triticum aestivum L.) grown in field-contaminated soil. Environ Sci Technol 43:3556–3560CrossRefGoogle Scholar
  59. Vithanage M, Mayakaduwa SS, Herath I, Ok YS, Mohan D (2016) Kinetics, thermodynamics and mechanistic studies of carbofuran removal using biochars from tea waste and rice husks. Chemosphere 150:781–789CrossRefGoogle Scholar
  60. Wang C, Zou X, Zhao Y, Li B, Song Q, Li Y, Yu W (2016) Distribution, sources, and ecological risk assessment of polycyclic aromatic hydrocarbons in the water and suspended sediments from the middle and lower reaches of the Yangtze River, China. Environ Sci Pollut Res 23:17158–17170CrossRefGoogle Scholar
  61. Wang CP, Sun HW, Chang Y, Song ZG, Qin XB (2011) PAHs distribution in sediments associated with gas hydrate and oil seepage from the Gulf of Mexico. Mar Pollut Bull 62:2714–2723CrossRefGoogle Scholar
  62. Wang L, Xin Y, Zhou ZL, Xu XY, Sun HW (2013) Impact of organic matter properties on sorption domains of phenanthrene on chemically modified geosorbents and synthesized charcoals. J Hazard Mater 244:268–275CrossRefGoogle Scholar
  63. Waqas M, Li G, Khan S, Shamshad I, Reid BJ, Qamar Z, Chao C (2015) Application of sewage sludge and sewage sludge biochar to reduce polycyclic aromatic hydrocarbons (PAH) and potentially toxic elements (PTE) accumulation in tomato. Environ Sci Pollut Res 22:12114–12123CrossRefGoogle Scholar
  64. Wei J, Li J, Huang G, Wang X, Chen G, Zhao B (2016) Adsorptive removal of naphthalene induced by structurally different Gemini surfactants in a soil-water system. Environ Sci Pollut Res 23:18034–18042CrossRefGoogle Scholar
  65. Wen B, Li R-J, Zhang S, Shan X-Q, Fang J, Xiao K, Khan SU (2009) Immobilization of pentachlorophenol in soil using carbonaceous material amendments. Environ Pollut 157:968–974CrossRefGoogle Scholar
  66. Yang Y, Hunter W, Tao S, Gan J (2008) Relationships between desorption intervals and availability of sediment-associated hydrophobic contaminants. Environ Sci Technol 42:8446–8451CrossRefGoogle Scholar
  67. Yu X-Y, Ying G-G, Kookana RS (2009) Reduced plant uptake of pesticides with biochar additions to soil. Chemosphere 76:665–671CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental ScienceZhejiang UniversityHangzhouChina
  2. 2.Zhejiang Provincial Key Laboratory of Organic Pollution Process and ControlHangzhouChina

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