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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

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Abstract

This study was carried out to examine heavy metal accumulation in rice grains and brassicas and to identify the different controls, such as soil properties and soil heavy metal fractions obtained by the Community Bureau of Reference (BCR) sequential extraction, in their accumulation. In Guangdong Province, South China, rice grain and brassica samples, along with their rhizospheric soil, were collected from fields on the basis of distance downstream from electroplating factories, whose wastewater was used for irrigation. The results showed that long-term irrigation using the electroplating effluent has not only enriched the rhizospheric soil with Cd, Cr, Cu, and Zn but has also increased their mobility and bioavailability. The average concentrations of Cd and Cr in rice grains and brassicas from closest to the electroplating factories were significantly higher than those from the control areas. Results from hybrid redundancy analysis (hRDA) and redundancy analysis (RDA) showed that the BCR fractions of soil heavy metals could explain 29.0 and 46.5 % of total eigenvalue for heavy metal concentrations in rice grains and brassicas, respectively, while soil properties could only explain 11.1 and 33.4 %, respectively. This indicated that heavy metal fractions exerted more control upon their concentrations in rice grains and brassicas than soil properties. In terms of metal interaction, an increase of residual Zn in paddy soil or a decrease of acid soluble Cd in the brassica soil could enhance the accumulation of Cd, Cu, Cr, and Pb in both rice grains and brassicas, respectively, while the reducible or oxidizable Cd in soil could enhance the plants’ accumulation of Cr and Pb. The RDA showed an inhibition effect of sand content and CFO on the accumulation of heavy metals in rice grains and brassicas. Moreover, multiple stepwise linear regression could offer prediction for Cd, Cu, Cr, and Zn concentrations in the two crops by soil heavy metal fractions and soil properties.

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Abbreviations

SOM:

Soil organic matter

CEC:

Cation exchange capability

AFO:

Amorphous Fe oxides

CFO:

Crystalline Fe oxides

ASF:

Acid soluble fraction

RDF:

Reducible fraction

OXF:

Oxidizable fraction

RSF:

Residual fraction

References

  • Acosta JA, Cano AF, Arocena JM, Debela F, Martínez-Martínez S (2009) Distribution of metals in soil particle size fractions and its implication to risk assessment of playgrounds in Murcia City (Spain). Geoderma 149:101–109

    Article  CAS  Google Scholar 

  • Agrawal R, Kumar B, Priyanka K, Narayan C, Shukla K, Sarkar J (2016) Micronutrient fractionation in coal mine-affected agricultural soils, India. Bull Environ Contam Toxicol 96(4):449–457

    Article  CAS  Google Scholar 

  • Anjum NA, Singh HP, Khan MIR, Masood A, Per TS, Negi A, Batish DR, Khan NA, Duarte AC, Pereira E (2015) Too much is bad—an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environ Sci Pollut Res 22:3361–3382

    Article  CAS  Google Scholar 

  • Balen B, Tkalec M, Šikić S, Tolić S, Cvjetko P, Pavlica M, Vidaković-Cifrek Ž (2011) Biochemical responses of Lemna minor experimentally exposed to cadmium and zinc. Ecotoxicology 20:815–826

    Article  CAS  Google Scholar 

  • Bose S, Bhattacharyya AK (2008) Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70:1264–1272

    Article  CAS  Google Scholar 

  • Chang CY, Yu HY, Chen JJ, Li FB, Zhang HH, Liu CP (2014a) Accumulation of heavy metals in leaf vegetables from agricultural soils and associated potential health risks in the Pearl River Delta, South China. Environ Monit Assess 186:1547–1560

    Article  CAS  Google Scholar 

  • Chang H, Buettner SW, Seaman JC, Jaffé PR, Koster Van Groos PG, Li D, Peacock AD, Scheckel KG, Kaplan DI (2014b) Uranium immobilization in an iron-rich rhizosphere of a native wetland plant from the Savannah River Site under reducing conditions. Environmental Science & Technology 48:9270–9278

    Article  CAS  Google Scholar 

  • Chen Y, Wen Y, Chai S (2005) The heavy metal content character of agricultural soil in the Pearl River Delta. [J] Res Environ Sci 3:75–78

    Google Scholar 

  • Chen H, Teng Y, Lu S, Wang Y, Wang J (2015) Contamination features and health risk of soil heavy metals in China. Sci Total Environ 512:143–153

    Article  Google Scholar 

  • Cheng H, Wang M, Wong MH, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148

    Article  CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  Google Scholar 

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  Google Scholar 

  • Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  Google Scholar 

  • Clemente R, Walker DJ, Roig A, Bernal MP (2003) Heavy metal bioavailability in a soil affected by mineral sulphides contamination following the mine spillage at Aznalcóllar (Spain). Biodegradation 14:199–205

    Article  CAS  Google Scholar 

  • Dong D, Feng Q, McGrouther K, Yang M, Wang H, Wu W (2015) Effects of biochar amendment on rice growth and nitrogen retention in a waterlogged paddy field. J Soils Sediments 15:153–162

    Article  CAS  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. Environmental Science & Technology 47:12775–12783

    Article  CAS  Google Scholar 

  • Gerringa L (1990) Aerobic degradation of organic matter and the mobility of Cu, Cd, Ni, Pb, Zn, Fe and Mn in marine sediment slurries. Mar Chem 29:355–374

    Article  CAS  Google Scholar 

  • Gupta N, Khan DK, Santra SC (2012) Heavy metal accumulation in vegetables grown in a long-term wastewater-irrigated agricultural land of tropical India. Environ Monit Assess 184:6673–6682

    Article  CAS  Google Scholar 

  • Hafeez B, Khanif YM, Saleem M (2013) Role of zinc in plant nutrition—a review. American journal of experimental Agriculture 3:374

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Kochian LV (2002) Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiol Plant 116:73–78

    Article  CAS  Google Scholar 

  • Jamali MK, Kazi TG, Arain MB, Afridi HI, Jalbani N, Kandhro GA, Shah AQ, Baig JA (2009) Heavy metal accumulation in different varieties of wheat (Triticum aestivum L.) grown in soil amended with domestic sewage sludge. J Hazard Mater 164:1386–1391

    Article  CAS  Google Scholar 

  • Kapusta-Duch, J., Kusznierewicz, B., Leszczyńska, T., Borczak, B., 2016. Effect of culinary treatment on changes in the contents of selected nutrients and non-nutrients in curly kale (Brassica oleracea Var. acephala). J Food Process Preserv

  • Khaokaew S, Landrot G, Chaney RL, Pandya K, Sparks DL (2012) Speciation and release kinetics of zinc in contaminated paddy soils. Environmental Science & Technology 46:3957–3963

    Article  CAS  Google Scholar 

  • Kidd PS, Dominguez-Rodriguez MJ, Diez J, Monterroso C (2007) Bioavailability and plant accumulation of heavy metals and phosphorus in agricultural soils amended by long-term application of sewage sludge. Chemosphere 66:1458–1467

    Article  CAS  Google Scholar 

  • Kitsopoulos KP (1999) Cation-exchange capacity (CEC) of zeolitic volcaniclastic materials: applicability of the ammonium acetate saturation (AMAS) method. Clay Clay Miner 47:688–696

    Article  CAS  Google Scholar 

  • Komárek M, Vaněk A, Ettler V (2013) Chemical stabilization of metals and arsenic in contaminated soils using oxides—a review. Environ Pollut 172:9–22

    Article  Google Scholar 

  • Konert M, Vandenberghe JEF (1997) Comparison of laser grain size analysis with pipette and sieve analysis: a solution for the underestimation of the clay fraction. Sedimentology 44:523–535

    Article  CAS  Google Scholar 

  • Kubová J, Matúš P, Bujdoš M, Hagarová I, Medved J (2008) Utilization of optimized BCR three-step sequential and dilute HCl single extraction procedures for soil–plant metal transfer predictions in contaminated lands. Talanta 75:1110–1122

    Article  Google Scholar 

  • Kumar M, Furumai H, Kurisu F, Kasuga I (2013) Potential mobility of heavy metals through coupled application of sequential extraction and isotopic exchange: comparison of leaching tests applied to soil and soakaway sediment. Chemosphere 90:796–804

    Article  CAS  Google Scholar 

  • Lam H, Remais J, Fung M, Xu L, Sun SS (2013) Food supply and food safety issues in China. Lancet 381:2044–2053

    Article  Google Scholar 

  • Li Z, Wu L, Luo Y, Christie P (2014) Dynamics of plant metal uptake and metal changes in whole soil and soil particle fractions during repeated phytoextraction. Plant Soil 374:857–869

    Article  CAS  Google Scholar 

  • Liu D, Islam E, Li T, Yang X, Jin X, Mahmood Q (2008a) Comparison of synthetic chelators and low molecular weight organic acids in enhancing phytoextraction of heavy metals by two ecotypes of Sedum alfredii Hance. J Hazard Mater 153:114–122

    Article  CAS  Google Scholar 

  • Liu H, Zhang J, Christie P, Zhang F (2008b) 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

    Article  CAS  Google Scholar 

  • Liu J, Zhang X, Tran H, Wang D, Zhu Y (2011) Heavy metal contamination and risk assessment in water, paddy soil, and rice around an electroplating plant. Environ Sci Pollut Res 18:1623–1632

    Article  CAS  Google Scholar 

  • Liu B, Ma X, Ai S, Zhu S, Zhang W, Zhang Y (2016) Spatial distribution and source identification of heavy metals in soils under different land uses in a sewage irrigation region, northwest China. J Soils Sediments 16:1547–1556

    Article  CAS  Google Scholar 

  • Ljung K, Selinus O, Otabbong E, Berglund M (2006) Metal and arsenic distribution in soil particle sizes relevant to soil ingestion by children. Appl Geochem 21:1613–1624

    Article  CAS  Google Scholar 

  • Lu Y, Jenkins A, Ferrier RC, Bailey M, Gordon IJ, Song S, Huang J, Jia S, Zhang F, Liu X (2015a) Addressing China’s grand challenge of achieving food security while ensuring environmental sustainability. Sci Adv 1:e1400039

    Article  Google Scholar 

  • Lu Y, Song S, Wang R, Liu Z, Meng J, Sweetman AJ, Jenkins A, Ferrier RC, Li H, Luo W (2015b) Impacts of soil and water pollution on food safety and health risks in China. Environ Int 77:5–15

    Article  CAS  Google Scholar 

  • McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159

    Article  CAS  Google Scholar 

  • Mendoza J, Garrido T, Castillo G, Martin NS (2006) Metal availability and uptake by sorghum plants grown in soils amended with sludge from different treatments. Chemosphere 65:2304–2312

    Article  CAS  Google Scholar 

  • Mendoza RE, García IV, de Cabo L, Weigandt CF, de Iorio AF (2015) The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci Total Environ 505:555–564

    Article  CAS  Google Scholar 

  • Meng W, Wang Z, Hu B, Wang Z, Li H, Goodman RC (2016) Heavy metals in soil and plants after long-term sewage irrigation at Tianjin China: a case study assessment. Agric Water Manag 171:153–161

    Article  Google Scholar 

  • Monterroso C, Rodríguez F, Chaves R, Diez J, Becerra-Castro C, Kidd PS, Macías F (2014) Heavy metal distribution in mine—soils and plants growing in a Pb/Zn-mining area in NW Spain. Appl Geochem 44:3–11

    Article  CAS  Google Scholar 

  • Nan Z, Li J, Zhang J, Cheng G (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285:187–195

    Article  CAS  Google Scholar 

  • Nemati K, Bakar NKA, Abas MR, Sobhanzadeh E (2011) Speciation of heavy metals by modified BCR sequential extraction procedure in different depths of sediments from Sungai Buloh, Selangor, Malaysia. J Hazard Mater 192:402–410

    CAS  Google Scholar 

  • Niu L, Yang F, Xu C, Yang H, Liu W (2013) Status of metal accumulation in farmland soils across China: from distribution to risk assessment. Environ Pollut 176:55–62

    Article  CAS  Google Scholar 

  • Ondrasek G, Rengel Z (2012) The role of soil organic matter in trace element bioavailability and toxicity. Abiotic Stress Responses in Plants:403–423

  • Qiu R, Thangavel P, Hu P, Senthilkumar P, Ying R, Tang Y (2011) Interaction of cadmium and zinc on accumulation and sub-cellular distribution in leaves of hyperaccumulator Potentilla griffithii. J Hazard Mater 186:1425–1430

    Article  CAS  Google Scholar 

  • Rakow G (2004) Species origin and economic importance of Brassica. Springer, pp:3–11

  • Roussiez V, Ludwig W, Radakovitch O, Probst J, Monaco A, Charrière B, Buscail R (2011) Fate of metals in coastal sediments of a Mediterranean flood-dominated system: an approach based on total and labile fractions. Estuar Coast Shelf Sci 92:486–495

    Article  CAS  Google Scholar 

  • Sadyś M, Strzelczak A, Grinn-Gofroń A, Kennedy R (2015) Application of redundancy analysis for aerobiological data. Int J Biometeorol 59:25–36

    Article  Google Scholar 

  • Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J Hazard Mater 219–220:1–12

    Article  Google Scholar 

  • Shi XZ, Yu DS, Xu SX, Warner ED, Wang HJ, Sun WX, Zhao YC, Gong ZT (2010) Cross-reference for relating Genetic Soil Classification of China with WRB at different scales. Geoderma 155:344–350

    Article  Google Scholar 

  • Silva EFD, Mlayah A, Gomes C, Noronha F, Charef A, Sequeira C, Esteves V, Marques ARF (2010) Heavy elements in the phosphorite from Kalaat Khasba mine (North-western Tunisia): potential implications on the environment and human health. J Hazard Mater 182:232–245

    Article  Google Scholar 

  • Steiner C, Teixeira WG, Lehmann J, Nehls T, de Macêdo JLV, Blum WE, Zech W (2007) Long term effects of manure, charcoal and mineral fertilization on crop production and fertility on a highly weathered Central Amazonian upland soil. Plant Soil 291:275–290

    Article  CAS  Google Scholar 

  • Sungur A, Soylak M, Yilmaz E, Yilmaz S, Ozcan H (2015) Characterization of heavy metal fractions in agricultural soils by sequential extraction procedure: the relationship between soil properties and heavy metal fractions. Soil Sediment Contam Int J 24:1–15

    Article  CAS  Google Scholar 

  • Teng Y, Wu J, Lu S, Wang Y, Jiao X, Song L (2014) Soil and soil environmental quality monitoring in China: a review. Environ Int 69:177–199

    Article  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • Wong SC, Li XD, Zhang G, Qi SH, Min YS (2002) Heavy metals in agricultural soils of the Pearl River Delta, South China. Environ Pollut 119:33–44

    Article  CAS  Google Scholar 

  • Wong C, Li XD, Zhang G, Qi SH, Peng XZ (2003) Atmospheric deposition of heavy metals in the Pearl River Delta, China. Atmos Environ 37:767–776

    Article  CAS  Google Scholar 

  • Wu F, Dong J, Qian QQ, Zhang G (2005) Subcellular distribution and chemical form of Cd and Cd–Zn interaction in different barley genotypes. Chemosphere 60:1437–1446

    Article  CAS  Google Scholar 

  • Xu, P., Liu, L., Zeng, G., Huang, D., Lai, C., Zhao, M., Huang, C., Li, N., Wei, Z., Wu, H., Zhang, C., Lai, M., He, Y. 2014 Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium. 98:6409–6418

  • Yoneyama T, Ishikawa S, Fujimaki S (2015) Route and regulation of zinc, cadmium, and iron transport in rice plants (Oryza sativa L.) during vegetative growth and grain filling: metal transporters, metal speciation, grain Cd reduction and Zn and Fe biofortification. Int J Mol Sci 16:19111–19129

    Article  CAS  Google Scholar 

  • Yu Y, Huang Y, Zhang W (2012) Changes in rice yields in China since 1980 associated with cultivar improvement, climate and crop management. Field Crop Res 136:65–75

    Article  Google Scholar 

  • Zeng F, Mao Y, Cheng W, Wu F, Zhang G (2008) Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut 153:309–314

    Article  CAS  Google Scholar 

  • Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159:84–91

    Article  CAS  Google Scholar 

  • Zhang M, Liu Z, Wang H (2010) Use of single extraction methods to predict bioavailability of heavy metals in polluted soils to rice. Commun Soil Sci Plant Anal 41:820–831

    Article  CAS  Google Scholar 

  • Zhang W, Lin K, Zhou J, Zhang W, Liu L, Han X (2013) Spatial distribution and toxicity of cadmium in the joint presence of sulfur in rice seedling. Environ Toxicol Pharmacol 36:1235–1241

    Article  CAS  Google Scholar 

  • Zhong X, Zhou S, Zhu Q, Zhao Q (2011) Fraction distribution and bioavailability of soil heavy metals in the Yangtze River Delta—a case study of Kunshan City in Jiangsu Province, China. J Hazard Mater 198:13–21

    Article  CAS  Google Scholar 

  • Zhou H, Zeng M, Zhou X, Liao B, Peng P, Hu M, Zhu W, Wu Y, Zou Z (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

    Article  CAS  Google Scholar 

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Acknowledgements

This work was funded by the Research Fund for the National Natural Science Foundation of China (No. 51039007 and No. 40971054) and the Fundamental Research Funds for the Central Universities. We would like to thank all the members of the research team. In addition, the authors benefited from helpful discussions with Yanting Hu.

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Correspondence to Dongsheng Guan.

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Xiao, L., Guan, D., Peart, M.R. et al. 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 Res 24, 2558–2571 (2017). https://doi.org/10.1007/s11356-016-8028-8

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