Abstract
This study developed a method to build relationships between chemical fractionations of heavy metals in soils and their accumulations in rice and estimate the respective contribution of each geochemical speciation in the soils from the Yangtze River Delta, China. In contaminated areas, residue and humic acid-bound fractions in soils were the main phases for most heavy metals. The mobility of heavy metals was in this following order: Cd > Pb ≈ Zn > Ni > As ≈ Cr > Hg. Transfer factors calculated by the ratios of specific fractionations of heavy metals in the soil–rice system were used to assess the capability of different metal speciation transfer from soil to rice. The carbonate and Fe/Mn oxyhydroxides bound phase had significant positive correlations with total metal concentrations in rice. Hg uptake by rice might be related to the exchangeable and carbonate-bound fractions of soil Hg. Results of PCA analysis of transfer factors estimated that the labile fractions (i.e. water soluble, exchangeable and carbonate bound) contributed more than 40% of the heavy metal accumulations in rice. Effect of organic matter and residue fraction on metals transfer was estimated to be ~ 25 to ~ 30% while contribution of humic acid and Fe/Mn oxyhydroxides-bound fractions was estimated to be ~ 20 to ~ 30%. Modified risk assessment code (mRAC) and ecological contamination index (ECI) confirmed that the soil samples were polluted by heavy metals. Soil Cd contributed more than 80% of mRAC. Contrarily, the main contributors to ECI were identified as As, Hg, Pb and Zn. The average values of total target hazard quotient (TTHQ) and Risktotal were above 1 and 10–4 respectively, implying people living in the study area were exposed to both non-carcinogenic and carcinogenic risk. As and Pb were the main contributor to high TTHQ value while As, Cd and Cr in rice contributed mostly to Risktotal value. Spatial changes of ecological risk indexes and human health risk indexes showed that the samples with high TTHQ values distributed in the area with high values of mRAC. Likewise, the area with high ECI values and with high carcinogenic risk overlapped.
Similar content being viewed by others
Data availability
The authors do not have permission to share data.
References
Abd Aziz, A., Lee, B.-T., Han, H.-J., & Kim, K.-W. (2019). Assessment of the stabilization of heavy metal contaminants in soils using chemical leaching and an earthworm bioassay. Environmental Geochemistry and Health, 41, 447–460.
Adriano, D. (2001). Trace elements in terrestrial environments: Biogeochemistry, bioavailability, and risks of metals. Springer.
Alan, M., & Kara, D. (2019). Assessment of sequential extraction methods for the prediction of bioavailability of elements in plants grown on agricultural soils near to boron mines in Turkey. Talanta, 200, 41–50.
Alloway, B. J. (2013). Heavy metals in soils. In B. J. Alloway (Ed.), Sources of heavy metals and metalloids in soils (pp. 11–50). Springer.
Bandara, J., Senevirathna, D., Dasanayake, D., Herath, V., Bandara, J., Abeysekara, T., & Rajapaksha, K. H. (2008). Chronic renal failure among farm families in cascade irrigation systems in Sri Lanka associated with elevated dietary cadmium levels in rice and freshwater fish (Tilapia). Environmental Geochemistry and Health, 30, 465–478.
Benson, N. U., Adedapo, A. E., Fred-Ahmadu, O. H., Williams, A. B., Udosen, E. D., Ayejuyo, O. O., & Olajire, A. A. (2018a). New ecological risk indices for evaluating heavy metals contamination in aquatic sediment: A case study of the Gulf of Guinea. Regional Studies in Marine Science, 18, 44–56.
Benson, N. U., Adedapo, A. E., Fred-Ahmadu, O. H., Williams, A. B., Udosen, E. D., Ayejuyo, O. O., & Olajire, A. A. (2018). A new method for assessment of sediment-associated contamination risks using multivariate statistical approach. MethodsX, 5, 268–276.
Bourg, A. C. M., & Loch, J. P. G. (1995). mobilization of heavy metals as affected by pH and redox conditions. In W. Salomons & W. M. Stigliani (Eds.), biogeodynamics of pollutants in soils and sediments: risk assessment of delayed and non-linear responses (pp. 87–102). Springer.
Chanpiwat, P., Hensawang, S., Suwatvitayakorn, P., & Ponsin, M. (2019). Risk assessment of bioaccessible arsenic and cadmium exposure through rice consumption in local residents of themae tao sub-district, northwestern Thailand. Environmental Geochemistry and Health, 41, 343–356.
Chavez, E., He, Z. L., Stoffella, P. J., Mylavarapu, R. S., Li, Y. C., & Baligar, V. C. (2016). Chemical speciation of cadmium: An approach to evaluate plant-available cadmium in ecuadorian soils under cacao production. Chemosphere, 150, 57–62.
CGS. (2005). Geological survey technical standard. China Geological Survey.
Dean, J. R. (2010). Heavy metal bioavailability and bioaccessibility in soil. In S. P. Cummings (Ed.), Bioremediation: Methods and protocols (pp. 15–36). Humana Press.
Dong, H., Feng, L., Qin, Y., & Luo, M. (2019). Comparison of different sequential extraction procedures for mercury fractionation in polluted soils. Environmental Science and Pollution Research, 26, 9955–9965.
Fu, Y., Chen, M., Bi, X., He, Y., Ren, L., Xiang, W., Qiao, S., Yan, S., Li, Z., & Ma, Z. (2011). Occurrence of arsenic in brown rice and its relationship to soil properties from Hainan Island, China. Environmental Pollution, 159, 1757–1762.
Gabarrón, M., Zornoza, R., Martínez-Martínez, S., Muñoz, V. A., Faz, Á., & Acosta, J. A. (2019). Effect of land use and soil properties in the feasibility of two sequential extraction procedures for metals fractionation. Chemosphere, 218, 266–272.
Gusiatin, Z. M., & Kulikowska, D. (2014). The usability of the IR, RAC and MRI indices of heavy metal distribution to assess the environmental quality of sewage sludge composts. Waste Management, 34, 1227–1236.
Hakanson, L. (1980). An ecological risk index for aquatic pollution control: A sedimentological approach. Water Research, 14, 975–1001.
Han, H. J., Lee, J. U., Ko, M. S., & Kim, K. W. (2020). Comparison of five extraction methods for evaluating cadmium and zinc immobilization in soil. Environmental Geochemistry and Health, 42, 4203–4212.
Hoang, H. T., & Baeumle, R. (2019). Complex hydrochemical characteristics of the middle-upper pleistocene aquifer in soc trang province, southern vietnam. Environmental Geochemistry and Health, 41, 325–341.
Huang, Q., Yu, Y., Wan, Y., Wang, Q., Luo, Z., Qiao, Y., Dechun, S., & Li, H. (2018). Effects of continuous fertilization on bioavailability and fractionation of cadmium in soil and its uptake by rice (Oryza sativa L.). Journal of Environmental Management, 215, 13–21.
Hutchinson, J. J., Young, S. D., McGrath, S. P., West, H. M., Black, C. R., & Baker, A. J. M. (2000). Determining uptake of ‘non-labile’ soil cadmium by thlaspi caerulescens using isotopic dilution techniques. New Phytologist, 146, 453–460.
IARC. (2004). IARC monographs on the evaluation of carcinogenic risks to humans. some drinking-water disinfectants and contaminants, including Arsenic, Lyon. France.
Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soils and plants. CRC.
Khaokaew, S., Chaney, R. L., Landrot, G., Ginder-Vogel, M., & Sparks, D. L. (2011). Speciation and release kinetics of cadmium in an alkaline paddy soil under various flooding periods and draining conditions. Environmental Science & Technology, 45, 4249–4255.
Kim, H. S., Kim, Y. J., & Seo, Y. R. (2015). An overview of carcinogenic heavy metal: Molecular toxicity mechanism and prevention. Journal of Cancer Prevention, 20, 232–240.
Ko, M. S., Nguyen, T. H., Kim, Y. G., Linh, B. M., & Kim, K. W. (2020). Assessment and source identification of As and Cd contamination in soil and plants in the vicinity of the Nui Phao Mine, Vietnam. Environmental Geochemistry and Health, 42, 4193–4201.
Kumarathilaka, P., Seneweera, S., Meharg, A., & Bundschuh, J. (2018). Arsenic speciation dynamics in paddy rice soil-water environment: Sources, physico-chemical, and biological factors: A review. Water Research, 140, 403–414.
Landner, L., & Reuther, R. (2005). Speciation, mobility and bioavailability of metals in the environment, metals in society and in the environment: A critical review of current knowledge on fluxes, speciation, bioavailability and risk for adverse effects of copper, chromium, nickel and zinc (pp. 139–274). Springer.
Li, T., Chang, Q., Yuan, X., Li, J., Ayoko, G. A., Frost, R. L., Chen, H., Zhang, X., Song, Y., & Song, W. (2017). Cadmium transfer from contaminated soils to the human body through rice consumption in southern Jiangsu Province, China. Environmental Science: Processes & Impacts, 19, 843–850.
Li, Z., Ma, Z., van der Kuijp, T. J., Yuan, Z., & Huang, L. (2014). A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. Science of The Total Environment, 468–469, 843–853.
Liao, Q., Evans, L. J., Gu, X., Fan, D., Jin, Y., & Wang, H. (2007). A regional geochemical survey of soils in Jiangsu Province, China: Preliminary assessment of soil fertility and soil contamination. Geoderma, 142, 18–28.
Liu, Y., Bello, O., Rahman, M. M., Dong, Z., Islam, S., & Naidu, R. (2017). Investigating the relationship between lead speciation and bioaccessibility of mining impacted soils and dusts. Environmental Science and Pollution Research, 24, 17056–17067.
Long, E. R., Macdonald, D. D., Smith, S. L., & Calder, F. D. (1995). Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management, 19, 81–97.
Luo, P., Xiao, X., Han, X., Ma, Y., Sun, X., Jiang, J., & Wang, H. (2019). Application of different single extraction procedures for assessing the bioavailability of heavy metal(loid)s in soils from overlapped areas of farmland and coal resources. Environmental Science and Pollution Research, 26, 14932–14942.
Luo, X., Yu, S., & Li, X. (2012). The mobility, bioavailability, and human bioaccessibility of trace metals in urban soils of Hong Kong. Applied Geochemistry, 27, 995–1004.
MacDonald, D. D., Ingersoll, C. G., & Berger, T. A. (2000). Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology, 39, 20–31.
Mao, C., Song, Y., Chen, L., Ji, J., Li, J., Yuan, X., Yang, Z., Ayoko, G. A., Frost, R. L., & Theiss, F. (2019). Human health risks of heavy metals in paddy rice based on transfer characteristics of heavy metals from soil to rice. Catena, 175, 339–348.
Marin, A. R., Masscheleyn, P. H., & Patrick, W. H. (1993). Soil redox-pH stability of arsenci species and its influence on arsenic uptake by rice. Plant & Soil, 152, 245–253.
McLaughlin, M. J., Parker, D. R., & Clarke, J. M. (1999). Metals and micronutrients: Food safety issues. Field Crops Research, 60, 143–163.
Meers, E., Du Laing, G., Unamuno, V., Ruttens, A., Vangronsveld, J., Tack, F. M. G., et al. (2007). Comparison of cadmium extractability from soils by commonly used single extraction protocols. Geoderma, 141, 247–259.
MEE. (2018). Soil environmental quality risk control standard for soil contmination of agricultural land. Ministry of Ecology and Environment PRC.
Mohamed, I., Ahamadou, B., Li, M., Gong, C., Cai, P., Liang, W., et al. (2010). Fractionation of copper and cadmium and their binding with soil organic matter in a contaminated soil amended with organic materials. Journal of Soils and Sediments, 10, 973–982.
Moral, R., Gilkes, R. J., & JordÁn, M. M. (2005). Distribution of heavy metals in calcareous and non-calcareous soils in Spain. Water, Air, and Soil Pollution, 162, 127–142.
Muhammad, I., Puschenreiter, M., & Wenzel, W. W. (2012). Cadmium and Zn availability as affected by pH manipulation and its assessment by soil extraction, DGT and indicator plants. Science of The Total Environment, 416, 490–500.
Müller, G. (1969). Index of geoaccumulation in sediments of the Rhine River. The Journal of Geology, 2, 108–118.
Nannipieri, P., Grego, S., & Ceccanti, B. (1990). Ecological significance of the biological activity in soil. Soil Biochemistry, 6, 293–355.
NHCNMPA. (2017). Maximum levels of contaminants in food, GB2762, Beijing.
NHFPC. (2015). 2014 report on Chinese resident’s chronic disease and nutrition. http://en.nhfpc.gov.cn/2015-06/15/c_45788.htm. National Health and Family Planning Commission.
Nolan, A. L., Zhang, H., & McLaughlin, M. J. (2005). Prediction of zinc, cadmium, lead, and copper availability to wheat in contaminated soils using chemical speciation, diffusive gradients in thin films, extraction, and isotopic dilution techniques. Journal of Environmental Quality, 34, 496–507.
Onyatta, J. O., & Huang, P. M. (1999). Chemical speciation and bioavailability index of cadmium for selected tropical soils in Kenya. Geoderma, 91, 87–101.
Pan, X., Yuan, B., Shi, Z., & Dai, Y. (2007). Investigation on dietary status among rural and urban residents in Jiangsu. Jiangsu Journal of Preventive Medicine (China), 18, 6–9.
Pardo, F., Jordán, M. M., Sanfeliu, T., & Pina, S. (2011). Distribution of Cd, Ni, Cr, and Pb in smended soils from licante Province (SE, Spain). Water, Air, & Soil Pollution, 217, 535–543.
Peng, Y., Shen, Y., Ge, M., Pan, Z., Chen, W., & Gong, B. (2019). Efficient extraction of heavy metals from collagens by sulfonated polystyrene nanospheres. Food Chemistry, 275, 377–384.
Phan, K., Phan, S., Se, S., Sieng, H., Huoy, L., & Kim, K. W. (2019). Assessment of water quality and trace metal contaminations in Mondolkiri province in the northeastern part of Cambodia. Environmental Geochemistry & Health, 41, 401–409.
Rahman, F., & Naidu, R. (2009). The influence of arsenic speciation (As-III & As-v) and concentration on the growth, uptake and translocation of arsenic in vegetable crops (silverbeet and amaranth). greenhouse study. Environmental Geochemistry and Health, 31, 115–124.
Reeder, R. J., Schoonen, M. A. A., & Lanzirotti, A. (2006). Metal speciation and its role in bioaccessibility and bioavailability. Reviews in Mineralogy and Geochemistry, 64, 59–113.
Saeedi, M., & Jamshidi-Zanjani, A. (2015). Development of a new aggregative index to assess potential effect of metals pollution in aquatic sediments. Ecological Indicators, 58, 235–243.
Satarug, S., & Moore, M. R. (2004). Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environmental Health Perspectives, 112, 1099–1103.
Shahid, M., Dumat, C., Khalid, S., Niazi, N.K., & Antunes, P.M.C. (2017). Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. In: Pim de Voogt (Ed.), Reviews of environmental contamination and toxicology 241. Springer, pp. 73-137.
Smith, S. L., MacDonald, D. D., Keenleyside, K. A., Ingersoll, C. G., & Jay, F. L. (1996). A preliminary evaluation of sediment quality assessment values for freshwater ecosystems. Journal of Great Lakes Research, 22, 624–638.
Sumalatha, J., Naveen, B. P., & Malik, R. K. (2019). Toxic metals removal from industrial sludge by using different leaching solutions. Journal of the Institution of Engineers (India) Series A, 100, 337–335.
Sun, L., Chen, S., Chao, L., & Sun, T. (2007). Effects of flooding on changes in Eh, pH and speciation of cadmium and lead in contaminated soil. Bulletin of Environmental Contamination and Toxicology, 79, 514–518.
Tan, W., Liu, F., Feng, X., Huang, Q., & Li, X. (2005). Adsorption and redox reactions of heavy metals on Fe–Mn nodules from Chinese soils. Journal of Colloid and Interface Science, 284, 600–605.
Tang, X., Zhu, Y., Cui, Y., Duan, J., & Tang, L. (2006). The effect of ageing on the bioaccessibility and fractionation of cadmium in some typical soils of China. Environment International, 32, 682–689.
Tessier, A., Campbell, P. G. C., & Bisson, M. (1979). Sequential extraction procedure for the sepeciation of particulate trace-metals. Analytical Chemistry, 51, 844–851.
Thanabalasingam, P., & Pickering, W. F. (1986). Arsenic sorption by humic acids. Environmental Pollution Series B, Chemical and Physical, 12, 233–246.
Ure, A. M. (1996). Single extraction schemes for soil analysis and related applications. Science of the Total Environment, 178, 3–10.
U.S. EPA. (2001). Risk assessment guidance for superfund: Volume III—Part A, process for conducting probabilistic risk assessment, Washington DC.
U.S. EPA. (2011). Exposure factors handbook: 2011 Edition, Washington, DC.
Van der Ent, A., Nkrumah, P. N., Tibbett, M., & Echevarria, G. (2019). Evaluating soil extraction methods for chemical characterization of ultramafic soils in Kinabalu Park (Malaysia). Journal of Geochemical Exploration, 196, 235–246.
Wang, S., & Mulligan, C. N. (2009). Enhanced mobilization of arsenic and heavy metals from mine tailings by humic acid. Chemosphere, 74, 274–279.
Wen, Y., Li, W., Yang, Z., Zhang, Q., & Ji, J. (2020a). Enrichment and source identification of Cd and other heavy metals in soils with high geochemical background in the karst region, Southwestern China. Chemosphere, 245, 125620.
Wen, Y., Li, W., Yang, Z., Zhuo, X., Guan, D.-X., Song, Y., et al. (2020b). Evaluation of various approaches to predict cadmium bioavailability to rice grown in soils with high geochemical background in the karst region, Southwestern China. Environmental Pollution, 258, 113645.
Williams, P. N., Villada, A., Deacon, C., Raab, A., Figuerola, J., Green, A. J., et al. (2007). Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environmental Science & Technology, 41, 6854–6859.
Williams, P. N., Zhang, H., Davison, W., Meharg, A. A., Hossain, M., Norton, G. J., et al. (2011). Organic matter-solid phase interactions are critical for predicting arsenic release and plant uptake in Bangladesh paddy soils. Environmental Science & Technology, 45, 6080–6087.
Yang, Q., Shu, W., Qiu, J., Wang, H., & Lan, C. (2004). Lead in paddy soils and rice plants Lechang and its potential health risk around lead/zinc Mine, Guangdong, China. Environment International, 30, 883–889.
Zeng, F., Ali, S., Zhang, H., Ouyang, Y., Qiu, B., Wu, F., et al. (2011). The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environmental Pollution, 159, 84–91.
Zhang, C., Ge, Y., Yao, H., Chen, X., & Hu, M. (2012). Iron oxidation-reduction and its impacts on cadmium bioavailability in paddy soils: A review. Frontiers of Environmental Science & Engineering, 6, 509–517.
Zhang, L., Mo, Z., Qin, J., Li, Q., Wei, Y., Ma, S., et al. (2015). Change of water sources reduces health risks from heavy metals via ingestion of water, soil, and rice in a riverine area, South China. Science of The Total Environment, 530–531, 163–170.
Zhao, M., Wang, C., Li, T., Yi, N., He, X., Wu, H., et al. (2013). Acute risk assessment of cumulative dietary exposure to organophosphorus pesticide among people in Jiangsu province. Journal of Hygiene Research, 42, 844–848.
Funding
This work was supported by grants from the project of Monitoring Technology and Forewarning of Heavy Metal Pollution in Typical Agricultural Land of Jiangsu Province (Grant No. KJXM2016039), and the project of Ecological and Geological Environment Monitoring of Land (Agricultural Land) in Jiangsu Province, and the project of Comprehensive Geological Survey of Modern Demonstration Area in Southern Jiangsu, the National Natural Science Foundation of China (Grant 41673095, 41907141) and the Fundamental Research Funds for the Central Universities (Grant No. Swu 118203).
Author information
Authors and Affiliations
Contributions
Yuanyuan Wang contributed to investigation, methodology, visualization and manuscript writing. Weiwei Xu contributed to conceptualization, data validation and project administration. Jizhou Li contributed to data analysis and interpretation. Yinxian Song contributed to research concept, experiment design, and critical revision of the article. Ming Hua contributed to collection and assembly of data. Wenbo Li contributed to sample collecting and analysing. Yubo Wen contributed to critical revision of the article. Tianyuan Li contributed to critical revision of the article. Xinxing He contributed to sample collecting and analysing.
Corresponding authors
Ethics declarations
Conflict of interest
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this article.
Consent for publication
The authors confirms that the work described has not been published before; that it is not under consideration for publication elsewhere; that its publication has been approved by all co-authors, if any; that its publication has been approved (tacitly or explicitly) by the responsible authorities at the institution where the work is carried out.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, Y., Xu, W., Li, J. et al. Assessing the fractionation and bioavailability of heavy metals in soil–rice system and the associated health risk. Environ Geochem Health 44, 301–318 (2022). https://doi.org/10.1007/s10653-021-00876-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-021-00876-4