Abstract
The phytoremediation efficiency is largely depends on the bioavailability of heavy metal in soil. The activity of earthworms and oxidation of elemental sulfur (S0) in soil has influence on heavy metal speciation transformation in soil. By conducting pot experiment, we examined the possibility of enhancing phytoextraction efficiency of lead (Pb) in soil by ryegrass (Lolium perenne L.) with application of both S0 and earthworms. Results showed that the addition of S0 decreased soil pH and increased soil CEC, while a slight trend of decrease for soil pH and increase for CEC was found with earthworm application. In soil treated with earthworms, the addition of S0 increased the concentration of DTPA-extractable Pb by 9.9~20.8%. The concentration of diffusive gradients in thin film (DGT)-extractable Pb was increased by 26.31~32.9% with S0 and earthworm addition. In soil treated with earthworms, the addition of S0 increased the concentration of Pb in shoots of ryegrass by 55.7~110.4% and the translocation factor of Pb in ryegrass was also increased by S0 addition. Our results suggested that the combination application of earthworms and S0 could be an effective way to enhance the remediation efficiency of ryegrass for Pb-contaminated soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and the supporting information files.
References
Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98(12):2243–2257. https://doi.org/10.1016/j.biortech.2005.12.006
Ardestani MM, Giska I, van Gestel CAM (2019) The effect of the earthworm Lumbricus rubellus on the bioavailability of cadmium and lead to the springtail Folsomia candida in metal-polluted field soils. Environ Sci Pollut Res Int 26(27):27816–27822. https://doi.org/10.1007/s11356-019-05969-3
Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727. https://doi.org/10.1016/j.ecoenv.2019.02.068
Cui Y, Dong Y, Li H, Wang Q (2004) Effect of elemental sulphur on solubility of soil heavy metals and their uptake by maize. Environ Int 30(3):323–328. https://doi.org/10.1016/S0160-4120(03)00182-X
DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions: state of the art and innovation in phytoremediation. Int J Mol Sci 20(14):3421. https://doi.org/10.3390/ijms20143412
Davlson W, Zhang H (1994) In situspeciation measurements of trace components in natural waters using thin-film gels. Nature 367(6463):546–548. https://doi.org/10.1038/367546a0
EPA US (1995) Test methods for evaluating solid waste
Gharmali AE, Rada A, Meray ME, Nejmeddine A (2002) Study of the effect of earthworm Lumbricus terrestris on the speciation of heavy metals in soils. Environ Technol 23(7):775–780. https://doi.org/10.1080/09593332308618368
Hernandez-Soriano MC, Jimenez-Lopez JC (2012) Effects of soil water content and organic matter addition on the speciation and bioavailability of heavy metals. Sci Total Environ 423:55–61
Iqbal M, Puschenreiter M, Oburger E, Santner J, Wenzel WW (2012) Sulfur-aided phytoextraction of Cd and Zn by Salix smithiana combined with in situ metal immobilization by gravel sludge and red mud. Environmental Pollution 170(NOV.):222–231. https://doi.org/10.1016/j.envpol.2012.07.008
Jiang B, Yini MA, Shan J, Guo H (2011) Transformation of ~(14)C-Labelled soil organic matter by the geophagous earthworm Metaphire guillelmi. Ecology and Environmental Sciences
Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34(9):1778–1783. https://doi.org/10.1021/es990697s
Kızılkaya R (2004) Cu and Zn accumulation in earthworm Lumbricus terrestris L. in sewage sludge amended soil and fractions of Cu and Zn in casts and surrounding soil. Ecol Eng 22(2):141–151. https://doi.org/10.1016/j.ecoleng.2004.04.002
Kooch Y, Jalilvand H (2008) Earthworms as ecosystem engineers and the most important detritivors in forest soils. Pakistan Journal of Biological Sciences : PJBS 11:819–825. https://doi.org/10.3923/pjbs.2008.819.825
Kravitz H (2004) Lead poisoning. Annu Rev Med 55:209–222. https://doi.org/10.1016/j.chaos.2008.09.043
Li FL, Qiu Y, Xu X, Yang F, Wang Z, Feng J, Wang J (2020) EDTA-enhanced phytoremediation of heavy metals from sludge soil by Italian ryegrass (Lolium perenne L.). EcotoxicolEnviron Safety 191:110185. https://doi.org/10.1016/j.ecoenv.2020.110185
Liu X, Hu C, Zhang S (2005) Effects of earthworm activity on fertility and heavy metal bioavailability in sewage sludge. Environ Int 31(6):874–879. https://doi.org/10.1016/j.envint.2005.05.033
Liu L, Li W, Song W, Guo M (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219. https://doi.org/10.1016/j.scitotenv.2018.03.161
Lock K, Janssen CR (2001) Ecotoxicity of zinc in spiked artificial soils versus contaminated field soils. Environ Sci Technol 35(21):4295. https://doi.org/10.1021/es0100219
Ma Y, Dickinson N, Wong M (2002) Toxicity of Pb/Zn mine tailings to the earthworm Pheretima and the effects of burrowing on metal availability. Biol Fertil Soils 36(1):79–86. https://doi.org/10.1007/s00374-002-0506-0
Mishra GK (2017) Microbes in heavy metal remediation: a review on current trends and patents. recent patents on biotechnology 11 (3):188-196. https://doi.org/10.2174/1872208311666170120121025
Murakami I, Ibaraki I (2008) Phytoextraction by a high-Cd-accumulating rice: Reduction of Cd content of soybean seeds. Environ Sci Technol 2008,42(16) (-):6167-6172. 10.1021/es8001597
Quevauviller P (1998) Operationally defined extraction procedures for soil and sediment analysis I. Standardization. TrAC Trends Anal Chem 17(5):289–298. https://doi.org/10.1016/S0165-9936(97)00119-2
Ruiz E, Alonso-Azcárate J, Rodríguez L (2011) Lumbricus terrestris L. activity increases the availability of metals and their accumulation in maize and barley. Environ Pollut 159(3):722–728. https://doi.org/10.1016/j.envpol.2010.11.032
Ruud CO, Bussiere JF, Green RE (2003) Isolation and characterization of Pseudomonas resistant to heavy metals contaminants. Int J Pharm Sci Rev Res 35(164):164–167
Séguin V, Gagnon C, Courchesne F (2004) Changes in water extractable metals, pH and organic carbon concentrations at the soil-root interface of forested soils. Plant Soil 260:1–17. https://doi.org/10.1023/B:PLSO.0000030170.49493.5f
Silbergeld, and Ellen, K. (1997) Preventing lead poisoning in children. Annu Rev Public Health 18:187–210. https://doi.org/10.2307/3433104
Sizmur T, Hodson ME (2009) Do earthworms impact metal mobility and availability in soil? – a review. Environ Pollut 157(7):1981–1989. https://doi.org/10.1016/j.envpol.2009.02.029
Sun L, Ke S, Lizheng S, Dechao D, Hong Z, Yafei S, Qin Q, Xue Y (2021) Influence of elemental sulfur on cadmium bioavailability, microbial community in paddy soil and Cd accumulation in rice plants. Sci Rep 11(1):11468. https://doi.org/10.1038/s41598-021-91003-x
Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51(7):844–851. https://doi.org/10.1021/ac50043a017
Tichý R, Fajtl J, Kužel S, Kolář L (1996) Use of elemental sulphur to enhance a cadmium solubilization and its vegetative removal from contaminated soil. Nutr Cycl Agroecosyst 46(3):249–255. https://doi.org/10.1007/BF00420560
Udovic M, Lestan D (2007) The effect of earthworms on the fractionation and bioavailability of heavy metals before and after soil remediation. Environ Pollut 148(2):663–668. https://doi.org/10.1016/j.envpol.2006.11.010
Wang YP, Li QB, Hui W, Shi JY, Lin Q, Chen XC, Chen YX (2008) Effect of sulphur on soil Cu/Zn availability and microbial community composition. J Hazard Mater 159(2-3):385–389. https://doi.org/10.1016/j.jhazmat.2008.02.029
Wen B, Hu XY, Liu Y, Wang WS, Feng MH, Shan XQ (2004) The role of earthworms (Eisenia fetida) in influencing bioavailability of heavy metals in soils. Biol Fertil Soils 40(3):181–187. https://doi.org/10.1007/s00374-004-0761-3
Wenger K, Kayser A, Gupta SK, Furrer G, Schulin R (2002) Comparison of NTA and elemental sulfur as potential soil amendments in phytoremediation. Journal of Soil Contamination 11(5):655–672. https://doi.org/10.1080/20025891107023
Wu J, Zhang C, Xiao L, Motelica-Heino M, Ren Z, Deng T, Dai J (2020) Impacts of earthworm species on soil acidification, Al fractions, and base cation release in a subtropical soil from China. Environ Sci Pollut Res Int 27(27):33446–33457. https://doi.org/10.1007/s11356-019-05055-8
Yanai J, Zhao F, Mcgrath S, Kosaki T (2006) Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens. Environ Pollut 139(1):167–175. https://doi.org/10.1016/j.envpol.2005.03.013
Yong SO, Usman A, Sang SL, El-Azeem S, Choi B, Hashimoto Y, Yang JE (2011) Effects of rapeseed residue on lead and cadmium availability and uptake by rice plants in heavy metal contaminated paddy soil. Chemosphere 85(4):677–682. https://doi.org/10.1016/j.chemosphere.2011.06.073
Yu X, Cheng J, Wong MH (2005) Earthworm–mycorrhiza interaction on Cd uptake and growth of ryegrass. Soil Biol Biochem 37(2):195–201. https://doi.org/10.1016/j.soilbio.2004.07.029
Zeng XB, Xu JM, Huang QR, Tang SR, Li YT, Li FB, Zhou DM, Wu ZJ (2013) Some deliberations on the issues of heavy metals in farmlands of China. Acra Pedologia Sinica 50(1):186–194 (in Chinese)
Zhang J, Yang N, Geng Y, Zhou J, Lei J (2019) Effects of the combined pollution of cadmium, lead and zinc on the phytoextraction efficiency of ryegrass (Lolium perenne L.). RSC Adv 9(36):20603–20611. https://doi.org/10.1039/C9RA01986C
Funding
This work was supported by the Shanghai Agriculture Applied Technology Development Program, China (2020-02-08-00-12-F01457, G20190301, T20180414), Natural Science Foundation of Shanghai (21ZR1443300), and Excellent Team Program of Shanghai Academy of Agricultural Sciences (Nongkechuang 2017(A-03)).
Author information
Authors and Affiliations
Contributions
Lijuan Sun, Peiyun Gong and Yong Xue designed the experiment, wrote the manuscript. Ke Song and Dechao Duan conducted the soil analysis. Chen Xu helped revised the manuscript. Hong Zhang and Yafei Sun helped analyze all of the data. Qin Qin and Weiguang Lv helped measuring Pb concentration in plant.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Elena Maestri
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 163 kb)
Rights and permissions
About this article
Cite this article
Sun, L., Gong, P., Song, K. et al. Combination application of elemental sulfur and earthworm increased the lead (Pb) uptake by ryegrass (Lolium perenne L.) in contaminated agricultural soil. Environ Sci Pollut Res 29, 23315–23322 (2022). https://doi.org/10.1007/s11356-021-17592-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-17592-2