Reduced Cd, Pb, and As accumulation in rice ( Oryza sativa L.) by a combined amendment of calcium sulfate and ferric oxide Research Article First Online: 20 November 2019 Abstract
A combined amendment (CF) consisting of 90% calcium sulfate (CaSO
4) and 10% ferric oxide (Fe 2O 3) was used to investigate the feasibility, active principles, and possible mechanisms of the immobilization of heavy metals in paddy soil. A soil incubation experiment, two consecutive pot trials, and a field experiment were conducted to evaluate the effectiveness and persistence of CF on metal(loid) immobilization. Soil incubation experiment results indicated that the application of CF significantly decreased the concentrations of cadmium (Cd), lead (Pb), and arsenic (As) in soil solution. CF treatments simultaneously reduced the accumulation of Cd, Pb, and As in two consecutive pot trials. The total Cd, Pb, and As concentrations in the rice grains were respectively 0.02, 2.08, and 0.62 mg kg −1 in the control treatment in the second year, which exceeded the safety limits of contaminants in food products in China. However, a high amount of CF amendment (CF-H, 0.3%) effectively decreased Cd, Pb, and As by 75.0%, 75.5%, and 46.8%, respectively. Further, with the CF amendment, the bioavailable Cd and Pb in the soil and the accumulation of Cd, Pb, and As in rice grain in the field experiment were also significantly decreased. The concentrations of Cd, Pb, and As in grains were respectively 0.02, 0.03, and 0.39 mg kg −1 in the control treatment in the field experiment, which decreased to 0.01, 0.01, and 0.22 mg kg −1 with CF addition, suggesting that grains produced in the field could pose less health risk. In conclusion, these results implied that CF was an effective and persistent combined amendment to immobilize heavy metals in soil and thereby can reduce the exposure risk of metal(loid)s associated with rice consumption. Keywords Cadmium Lead Arsenic Rice ( Oryza sativa L.) Paddy soil Immobilization
Responsible editor: Roberto Terzano
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) contains supplementary material, which is available to authorized users. https://doi.org/10.1007/s11356-019-06765-9 Notes Funding information
This work was supported by the National Natural Science Foundation of China (41671312) and National Key Technology R&D Program (2015BAD05B04).
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Afroz H, Su SM, Carey MP, Meharg AA, Meharg C (2019) Inhibition of microbial methylation via
in the rhizosphere: arsenic speciation in the soil to plant continuum. Environ Sci Technol 53(7):3451–3463.
https://doi.org/10.1021/acs.est.8b07008 CrossRef Google Scholar
Ahmad M, Lee SS, Yang JE (2012) Effects of soil dilution and amendments (mussel shell, cow bone, and biochar) on Pb availability and phytotoxicity in military shooting range soil. Ecotox Environ Safe 79:225–231.
https://doi.org/10.1016/j.ecoenv.2012.01.003 CrossRef Google Scholar
Anikwe MAN, Eze JC, Ibudialo AN (2016) Influence of lime and gypsum application on soil properties and yield of cassava (
Manihot esculenta Crantz.
) in a degraded Ultisol in Agbani, Enugu Southeastern Nigeria. Soil Till Res 158:32–38.
https://doi.org/10.1016/j.still.2015.10.011 CrossRef Google Scholar
Antoniadis V, Alloway BJ (2002) The role of dissolved organic carbon in the mobility of Cd, Ni and Zn in sewage sludge-amended soils. Environ Pollut 117(3):515–521.
https://doi.org/10.1016/s0269-7491(01)00172-5 CrossRef Google Scholar
Babel S, Kurniawan TA (2003) Low-cost adsorbents for heavy metals uptake from contaminated water: a review. J Hazard Mater 97(1):219–243.
https://doi.org/10.1016/S0304-3894(02)00263-7 CrossRef Google Scholar
Banza CLN, Nawrot TS, Haufroid V (2009) High human exposure to cobalt and other metals in Katanga, a mining area of the Democratic Republic of Congo. Environ Res 109:745–752.
https://doi.org/10.1016/j.envres.2009.04.012 CrossRef Google Scholar
Bian R, Joseph S, Cui L (2014) A three-year experiment confirms continuous immobilization of cadmium and lead in contaminated paddy field with biochar amendment. J Hazard Mater 272:121–128.
https://doi.org/10.1016/j.jhazmat.2014.03.017 CrossRef Google Scholar
Bolan NS, Adriano DC, Duraisamy P (2003) Immobilization and phytoavailability of cadmium in variable charge soils. III. Effect of biosolid compost addition. Plant Soil 256 (1): 231–241.
https://doi.org/10.1023/a:1026288021059 CrossRef Google Scholar
Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorus in soils. Soil Sci 59:39–45.
https://doi.org/10.1097/00010694-194501000-00006 CrossRef Google Scholar
Bremner JM, Tabatabai MA (1972) Use of an ammonia electrode for determination of ammonium in Kjeldahl analysis of soils. Commun Soil Sci Plan 3(2):159–165.
https://doi.org/10.1080/00103627209366361 CrossRef Google Scholar
Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124 (1–2): 3–22.
https://doi.org/10.1016/j.geoderma.2004.03.005 CrossRef Google Scholar
Cao Z, Qin M, Lin X (2018) Sulfur supply reduces cadmium uptake and translocation in rice grains (
Oryza sativa L.
) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environ Pollut 238:76–84.
https://doi.org/10.1016/j.envpol.2018.02.083 CrossRef Google Scholar
Chang Y, Hsi H, Hseu Z (2013) Chemical stabilization of cadmium in acidic soil using alkaline agronomic and industrial by-products. J Environ Sci Heal A 48:1748–1756.
https://doi.org/10.1080/10934529.2013.815571 CrossRef Google Scholar
Chen Z, Zhu YG, Liu WJ (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (
Oryza sativa L.
) roots. New Phytol 165:91–97.
https://doi.org/10.1111/j.1469-8137.2004.01241.x CrossRef Google Scholar
Chen JS, Li J, Zhang Y, Zong H, Lei NF (2015) Clonal integration ameliorates the carbon accumulation capacity of a stoloniferous herb, Glechoma longituba, growing in heterogenous light conditions by facilitating nitrogen assimilation in the rhizosphere. Ann Bot-london 115(1):127–136.
https://doi.org/10.1093/aob/mcu207 CrossRef Google Scholar
de Livera J, McLaughlin MJ, Hettiarachchi GM (2011) Cadmium solubility in paddy soils: Effects of soil oxidation, metal sulfides and competitive ions. Sci Total Environ 409:1489–1497.
https://doi.org/10.1016/j.scitotenv.2010.12.028 CrossRef Google Scholar
Derakhshan Nejad Z, Jung MC, Kim KH (2017) Remediation of soils contaminated with heavy metals with an emphasis on immobilization technology. Environ Geochem Hlth 40:927–953.
https://doi.org/10.1007/s10653-017-9964-z CrossRef Google Scholar
Drahota P, Grosslová Z, Kindlová H (2014) Selectivity assessment of an arsenic sequential extraction procedure for evaluating mobility in mine wastes. Anal Chim Acta 839:34–43.
https://doi.org/10.1016/j.aca.2014.06.022 CrossRef Google Scholar
Fan J, Hu Z, Ziadi N (2010) Excessive sulfur supply reduces cadmium accumulation in brown rice (
Oryza sativa L.
). Environ Pollut 158(2):409–415.
https://doi.org/10.1016/j.envpol.2009.08.042 CrossRef Google Scholar
Feng X, Han L, Chao D (2017) Ionomic and transcriptomic analysis provides new insight into the distribution and transport of cadmium and arsenic in rice. J Hazard Mater 331:246–256.
https://doi.org/10.1016/j.jhazmat.2017.02.041 CrossRef Google Scholar
Fisher JC, Wallschläger D, Planer-Friedrich B (2008) A new role for sulfur in arsenic cycling. Environ Sci Technol 42:81–85.
https://doi.org/10.1021/es0713936 CrossRef Google Scholar
Friesl W, Horak O, Wenzel W W (2004) Immobilization of heavy metals in soils by the application of bauxite residues: pot experiments under field conditions. J Plant Nutr Soil Sc 167(1): 54–59.
https://doi.org/10.1002/jpln.200320941 CrossRef Google Scholar
Fu Y, Yang X, Shen H (2018) Root iron plaque alleviates cadmium toxicity to rice (
Oryza sativa L.
) seedlings. Ecotox Environ Safe 161:534–541.
https://doi.org/10.1016/j.ecoenv.2018.06.015 CrossRef Google Scholar
Fulda B, Voegelin A, Kretzschmar R (2013) Redox-controlled changes in cadmium solubility and solid-phase speciation in a paddy soil As affected by reducible sulfate and copper. Environ Sci Technol 47:12775–12783.
https://doi.org/10.1021/es401997d CrossRef Google Scholar
González V, García I, Moral FD, Simón M (2012) Effectiveness of amendments on the spread and phytotoxicity of contaminants in metal–arsenic polluted soil. J Hazard Mater 205-206(none):72–80.
https://doi.org/10.1016/j.jhazmat.2011.12.011 CrossRef Google Scholar
Guo J, Li Y, Hu C (2018) Ca-containing amendments to reduce the absorption and translocation of Pb in rice plants. Sci Total Environ 637-638:971–979.
https://doi.org/10.1016/j.scitotenv.2018.05.100 CrossRef Google Scholar
Honma T, Ohba H, Kaneko-Kadokura A (2016) Optimal soil Eh, pH, and water management for simultaneously minimizing arsenic and cadmium concentrations in rice grains. Environ Sci Technol 50:4178–4185.
https://doi.org/10.1021/acs.est.5b05424 CrossRef Google Scholar
Hu Y, Li JH, Zhu YG (2005) Sequestration of As by iron plaque on the roots of three rice (
Oryza sativa L.
) cultivars in a low-P soil with or without P fertilizer. Environ Geochem Hlth 27:169–176.
https://doi.org/10.1007/s10653-005-0132-5 CrossRef Google Scholar
Huang J, Wang S, Lin J (2013) Dynamics of cadmium concentration in contaminated rice paddy soils with submerging time. Paddy Water Environ 11:483–491.
https://doi.org/10.1007/s10333-012-0339-x CrossRef Google Scholar
Jia Y, Huang H, Sun GX, Zhao FJ, Zhu YG (2012) Pathways and relative contributions to arsenic volatilization from rice plants and paddy soil. Environ Sci Technol 46: 8090–8096.
https://doi.org/10.1021/es300499a CrossRef Google Scholar
Kameda K, Hashimoto Y, Wang S (2017) Simultaneous and continuous stabilization of As and Pb in contaminated solution and soil by a ferrihydrite-gypsum sorbent. J Hazard Mater. 327:171–179.
https://doi.org/10.1016/j.jhazmat.2016.12.039 CrossRef Google Scholar
Kim HB, Kim SH, Jeon EK, Kim DH, Tsang DCW, Alessi DS, Kwon EE, Baek K (2018a) Effect of dissolved organic carbon from sludge, rice straw and spent coffee ground biochar on the mobility of arsenic in soil. Sci Total Environ 636:1241–1248.
https://doi.org/10.1016/j.scitotenv.2018.04.406 CrossRef Google Scholar
Kim HS, Seo B, Kuppusamy S (2018b) A DOC coagulant, gypsum treatment can simultaneously reduce As, Cd and Pb uptake by medicinal plants grown in contaminated soil. Ecotox Environ Safe 148:615–619.
https://doi.org/10.1016/j.ecoenv.2017.10.067 CrossRef Google Scholar
Kirk MF, Roden EE, Crossey LJ (2010) Experimental analysis of arsenic precipitation during microbial sulfate and iron reduction in model aquifer sediment reactors. Geochim Cosmochim Ac. 74:2538–2555.
https://doi.org/10.1016/j.gca.2010.02.002 CrossRef Google Scholar
Kim KR, Owens G, Kwon SL (2010) Influence of Indian mustard (
) on rhizosphere soil solution chemistry in long-term contaminated soils: A rhizobox study. J Environ Sci (01):102–109.
Lafferty BJ, and Loeppert RH (2005) Methyl arsenic adsorption and desorption behavior on iron oxides. Environ Sci Technol 39: 2120–2127.
Lai YC, Syu CH, Wang PJ (2018) Field experiment for determining lead accumulation in rice grains of different genotypes and correlation with iron oxides deposited on rhizosphere soil. Sci Total Environ 610-611:845–853.
https://doi.org/10.1016/j.scitotenv.2017.08.034 CrossRef Google Scholar
Lambrechts T, Couder E, Bernal MP, Faz Á, Iserentant A, Lutts S (2011) Assessment of heavy metal bioavailability in contaminated soils from a former mining area (La Union, Spain) using a rhizospheric test. Water Air Soil Poll 217(1-4):333–346.
https://doi.org/10.1007/s11270-010-0591-x CrossRef Google Scholar
Lee S, Kim EY, Park H (2011) In situ stabilization of arsenic and metal-contaminated agricultural soil using industrial by-products. Geoderma 161:1–7.
https://doi.org/10.1016/j.geoderma.2010.11.008 CrossRef Google Scholar
Lei K, Giubilato E, Critto A (2016) Contamination and human health risk of lead in soils around lead/zinc smelting areas in China. Environ Sci Pollut R 23:13128–13136.
https://doi.org/10.1007/s11356-016-6473-z CrossRef Google Scholar
Li P, Wang X, Zhang T (2009) Distribution and accumulation of copper and cadmium in soil–rice system as affected by soil amendments. Water Air Soil Poll 196:29–40.
https://doi.org/10.1007/s11270-008-9755-3 CrossRef Google Scholar
Li Z, Ma Z, van der Kuijp TJ (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468-469:843–853.
https://doi.org/10.1016/j.scitotenv.2013.08.090 CrossRef Google Scholar
Liao J, Wen Z, Ru X (2016) Distribution and migration of heavy metals in soil and crops affected by acid mine drainage: public health implications in Guangdong Province, China. Ecotox Environ Safe 124:460–469.
https://doi.org/10.1016/j.ecoenv.2015.11.023 CrossRef Google Scholar
Liu H, Zhang J, Christie P (2008) Influence of iron plaque on uptake and accumulation of Cd by rice (
Oryza sativa L.
) seedlings grown in soil. Sci Total Environ 394:361–368.
https://doi.org/10.1016/j.scitotenv.2008.02.004 CrossRef Google Scholar
Liu N, Jørgensen U, Lærke PE (2013) Quality determination of biomass for combustion: a new high-throughput microwave digestion method prior to elemental analysis by inductively coupled plasma–optical emission spectroscopy. Energ Fuel 27:7485–7488.
https://doi.org/10.1021/ef4016747 CrossRef Google Scholar
Lomax C, Liu WJ, Wu L, Xue K, Xiong J, Zhou J, McGrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytologist 193(3):665–672.
https://doi.org/10.1111/j.1469-8137.2011.03956.x CrossRef Google Scholar
Meng J, Tao M, Wang L, Liu X, Xu J (2018) Changes in heavy metal bioavailability and speciation from a Pb-Zn mining soil amended with biochars from co-pyrolysis of rice straw and swine manure. Sci Total Environ 633:300–307.
https://doi.org/10.1016/j.scitotenv.2018.03.199 CrossRef Google Scholar
Mohamed BA, Ellis N, Kim CS, Bi X (2017) The role of tailored biochar in increasing plant growth, and reducing bioavailability, phytotoxicity, and uptake of heavy metals in contaminated soil. Environ Pollut 230:329–338.
https://doi.org/10.1016/j.envpol.2017.06.075 CrossRef Google Scholar
Nishida S, Duan G, Ohkama-Ohtsu N (2016) Enhanced arsenic sensitivity with excess phytochelatin accumulation in shoots of a SULTR1;2 knockout mutant of Arabidopsis thaliana (L.) Heynh. Soil Sci Plant Nutr 62:367–372.
https://doi.org/10.1080/00380768.2016.1150790 CrossRef Google Scholar
Nzihou A, Sharrock P (2010) Role of phosphate in the remediation and reuse of heavy metal polluted wastes and sites. Waste Biomass Valori 1:163–174.
https://doi.org/10.1007/s12649-009-9006-x CrossRef Google Scholar
Obiora SC, Chukwu A, Davies TC (2016) Heavy metals and health risk assessment of arable soils and food crops around Pb–Zn mining localities in Enyigba, southeastern Nigeria. J Afr Earth Sci 116:182–189.
https://doi.org/10.1016/j.jafrearsci.2015.12.025 CrossRef Google Scholar
O"Day PA, Vlassopoulos D, Root R, Rivera N (2004) The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions. P Nati Acad Sci USA 101(38): 13703–13708.
https://doi.org/10.1073/pnas.0402775101 CrossRef Google Scholar
Riley D, Barber SA (1970) Salt accumulation at the soybean (Glycine max. (L.e merr.) root-soil interface). Soil Sci Soc Am J, 1970 34(1):154–155.
https://doi.org/10.2136/sssaj1970.03615995003400010042x CrossRef Google Scholar
Saalfield SL, Bostick BC (2009) Changes in iron, sulfur, and arsenic speciation associated with bacterial sulfate reduction in ferrihydrite-rich systems. Environ Sci Technol 43:8787–8793.
https://doi.org/10.1021/es901651k CrossRef Google Scholar
Samiullah M, Aslam Z, Rana AG, Abbas A, Ahmad W (2018) Alkali-activated boiler fly ash for Ni(II) removal: characterization and parametric study. Water Air Soil Poll 229(4):113–113.
https://doi.org/10.1007/s11270-018-3758-5 CrossRef Google Scholar
Seyfferth AL, Webb SM, Andrews JC (2010) Arsenic localization, speciation, and co-occurrence with iron on rice (
Oryza sativa L.
) roots having variable Fe coatings. Environ Sci Technol 44:8108–8113.
https://doi.org/10.1021/es101139z CrossRef Google Scholar
Shi GL, Lu HY, Liu JZ, Lou LQ, Tang XJ, Wu YH, Ma HX (2017) Periphyton growth reduces cadmium but enhances arsenic accumulation in rice (
) seedlings from contaminated soil. Plant and Soil 421:137–146.
https://doi.org/10.1007/s11104-017-3447-y CrossRef Google Scholar
Shirazi MA, Boersma L (1984) A unifying quantitative analysis of soil texture 1. Soil Sci Soc Am J 48(1):142.
https://doi.org/10.2136/sssaj1984.03615995004800010026x CrossRef Google Scholar
Sljivic HM, Bergant M, Jankovic S (2018) Assessment of Pb, Cd and Hg soil contamination and its potential to cause cytotoxic and genotoxic effects in human cell lines (CaCo-2 and HaCaT). Environ Geochem Hlth 40:1557–1572.
https://doi.org/10.1007/s10653-018-0071-6 CrossRef Google Scholar
Srivastava S, Akkarakaran JJ, Sounderajan S (2016) Arsenic toxicity in rice (
Oryza sativa L.
) is influenced by sulfur supply: impact on the expression of transporters and thiol metabolism. Geoderma 270:33–42.
https://doi.org/10.1016/j.geoderma.2015.11.006 CrossRef Google Scholar
Takahashi Y, Minamikawa R, Hattori KH (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044.
https://doi.org/10.1021/es034383n CrossRef Google Scholar
Tan XF, Liu YG, Gu YL, Zeng GM, Hu XJ, Wang X, Hu X, Guo YM, Zeng XX, Sun ZC (2015) Biochar amendment to lead-contaminated soil: effects on fluorescein diacetate hydrolytic activity and phytotoxicity to rice. Environ Toxicol Chem 34(9):1962–1968.
https://doi.org/10.1002/etc.3023 CrossRef Google Scholar
Udeigwe TK, Eze PN, Teboh JM (2011) Application, chemistry, and environmental implications of contaminant-immobilization amendments on agricultural soil and water quality. Environ Int 37(1):258–267.
https://doi.org/10.1016/j.envint.2010.08.008 CrossRef Google Scholar
Wang L, Luo L, Ma Y (2009) In situ immobilization remediation of heavy metals-contaminated soils: a review. J Appl Ecol 20:1214–1222
http://dx.doi.org/ Google Scholar
Wu S, Kuschk P, Wiessner A (2013) Sulphur transformations in constructed wetlands for wastewater treatment: a review. Ecol Eng. 52:278–289.
https://doi.org/10.1016/j.ecoleng.2012.11.003 CrossRef Google Scholar
Xiao L, Guan D, Peart MR, Chen Y, Li Q (2017) The respective effects of soil heavy metal fractions by sequential extraction procedure and soil properties on the accumulation of heavy metals in rice grains and brassicas. Environ Sci Pollut R 24(3):2558–2571.
https://doi.org/10.1007/s11356-016-8028-8 CrossRef Google Scholar
Xu RK, Zhao AZ, Yuan JH, Jiang J (2012) pH buffering capacity of acid soils from tropical and subtropical regions of china as influenced by incorporation of crop straw biochars. J Soil Sediment 12(4): 494–502.
https://doi.org/10.1007/s11368-012-0483-3 CrossRef Google Scholar
Yang J, Liu Z, Wan X (2016a) Interaction between sulfur and lead in toxicity, iron plaque formation and lead accumulation in rice plant. Ecotox Environ Safe 128:206–212.
https://doi.org/10.1016/j.ecoenv.2016.02.021 CrossRef Google Scholar
Yang Y, Zhang W, Qiu H (2016b) Effect of coexisting Al(III) ions on Pb(II) sorption on biochars: role of pH buffer and competition. Chemosphere 161:438–445.
https://doi.org/10.1016/j.chemosphere.2016.07.007 CrossRef Google Scholar
Yang Y, Chen J, Huang Q (2018) Can liming reduce cadmium (Cd) accumulation in rice (
Oryza sativa L.
) in slightly acidic soils? A contradictory dynamic equilibrium between Cd uptake capacity of roots and Cd immobilisation in soils. Chemosphere 193:547–556.
https://doi.org/10.1016/j.chemosphere.2017.11.061 CrossRef Google Scholar
Zhai X, Li Z, Huang B (2018) Remediation of multiple heavy metal-contaminated soil through the combination of soil washing and in situ immobilization. Sci Total Environ 635:92–99.
https://doi.org/10.1016/j.scitotenv.2018.04.119 CrossRef Google Scholar
Zhang D, Yuan Z, Wang S (2015) Incorporation of arsenic into gypsum: relevant to arsenic removal and immobilization process in hydrometallurgical industry. J Hazard Mater 300:272–280.
https://doi.org/10.1016/j.jhazmat.2015.07.015 CrossRef Google Scholar
Zhou H, Zhou X, Zeng M, Liao BH, Liu L, Yang WT, Wu YM, Qiu QY, Wang YJ (2014) Effects of combined amendments on heavy metal accumulation in rice (
Oryza sativa L.
) planted on contaminated paddy soil. Ecotoxicol Environ Saf 101(1):226–232.
https://doi.org/10.1016/j.ecoenv.2014.01.001 CrossRef Google Scholar
Zhou H, Zeng M, Zhou X (2015) Heavy metal translocation and accumulation in iron plaques and plant tissues for 32 hybrid rice (
Oryza sativa L.
) cultivars. Plant Soil 386:317–329.
https://doi.org/10.1007/s11104-014-2268-5 CrossRef Google Scholar
Zhu YG, Sun GX, Lei M (2008) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42:5008–5013.
https://doi.org/10.1021/es8001103 CrossRef Google Scholar
Zhu F, Hou JT, Xue S, Wu C, Wang QL, Hartley W (2017) Vermicompost and gypsum amendments improve aggregate formation in bauxite residue. Land Degrad Dev 28:2109–2120.
https://doi.org/10.1002/ldr.2737 CrossRef Google Scholar
Zhao FJ, Harris E, Yan J, Ma JC, Wu LY, Liu WJ, McGrath SP, Zhou JZ, Zhu YG (2013a) Arsenic methylation in soils and its relationship with microbial
abundance and diversity, and As speciation in rice. Environ SciTechnol 47: 7147–7154.
https://doi.org/10.1021/es304977m CrossRef Google Scholar Copyright information
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