Environmental Science and Pollution Research

, Volume 25, Issue 24, pp 24111–24124 | Cite as

Phytoavailability, bioaccumulation, and human health risks of metal(loid) elements in an agroecosystem near a lead-zinc mine

  • Liqiang LuoEmail author
  • Yating Shen
  • Xiaofang Wang
  • Binbin Chu
  • Tao Xu
  • Ying Liu
  • Yuan Zeng
  • Jian Liu
Research Article


Soil near a Pb-Zn-Mn mine was polluted by mining, which may have an impact on human health via the food chain. To evaluate the pollution effects, arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), manganese (Mn), lead (Pb), and zinc (Zn) in vegetables were determined by inductively coupled plasma atomic emission and mass spectrometry. Lead species were analyzed by X-ray absorption near-edge structure (XANES). Phytoavailability of the elements was evaluated by bioaccumulation of the elements, the sequential extraction procedure, Pb species, and plant uptakes. The target health quotient (THQ) was calculated to evaluate the human health risks. It was found that (1) high concentrations of As, Cd, Cr, and Pb were detectable in vegetables, and bioaccumulation was in the order of Mn > Zn > Cr > Pb > Cu > As > Cd; (2) phytoavailability of the elements was controlled mainly by the soluble fraction, and a linear relationship observed between the soluble fraction and bioaccumulation; (3) a new Pb-fulvic acid complex (Pb-FA) was identified by XANES in rhizosphere soil, and high content of Pb organic matter (60%) and soluble Pb (18%) were found; (4) both Cd and Zn accumulated in both of the Amaranthaceae and the Apiaceae families, indicating that the plants in the same family have the same bioaccumulation trend for the elements in the same group; (5) agricultural activities and plant growing increased phytoavailability of As, Cd, Cu, Pb, and Zn by decreasing the residual and raising the soluble and extractable fractions; (6) arsenic is top of the high health risks, followed by Pb, Cd, and Mn. Coriander, celery, and spinach were the top three highest health risks in the area.


Phytoavailability Bioaccumulation Pb species X-ray absorption near-edge structure Vegetable Soils Health risks 



We would like to thank Dr. Lesley Egden for her checks and suggestions on the manuscript. The Pb species analyses were conducted in Shanghai Synchrotron Radiation Facility (14U and 15W stations, SSRF) and Beijing Synchrotron Radiation Facility (BSRF).


This work was supported by the National Key Technologies R&D Program of China (Grant No. 2016YFC0600603), the National Natural Science Foundation of China (Grant No. 20775018 & 41201527), the National High Tech R&D Program (Grant No. 2007AA06Z124), and the China Geological Survey (Grant No. DD20160340).

Supplementary material

11356_2018_2482_MOESM1_ESM.docx (982 kb)
ESM 1 (DOCX 981 kb)


  1. Alam MGM, Snow ET, Tanaka A (2003) Arsenic and heavy metal contamination of vegetables grown in Samta village, Bangladesh. Sci Total Environ 308:83–96. CrossRefGoogle Scholar
  2. Alloway BJ (1995) Cadmium. In: Alloway, B.J. (Ed.), Heavy metals in soils,. Blackie Academic & Professional, pp. 122–151, second ed. Glasgow Google Scholar
  3. Anju M, Banerjee DK (2011) Associations of cadmium, zinc, and lead in soils from a lead and zinc mining area as studied by single and sequential extractions. Environ Monit Assess 176:67–85. CrossRefGoogle Scholar
  4. Bortey-Sam N, Nakayama SMM, Ikenaka Y, Akoto O, Baidoo E, Yohannes YB, Mizukawa H, Ishizuka M (2015) Human health risks from metals and metalloid via consumption of food animals near gold mines in Tarkwa, Ghana: estimation of the daily intakes and target hazard quotients (THQs). Ecotoxicol Environ Saf 111:160–167. CrossRefGoogle Scholar
  5. Boshoff M, De Jonge M, Scheifler R, Bervoets L (2014) Predicting As, Cd, Cu, Pb and Zn levels in grasses (Agrostis sp. and Poa sp.) and stinging nettle (Urtica dioica) applying soil–plant transfer models. Sci Total Environ 493:862–871. CrossRefGoogle Scholar
  6. Delcastilho P, Chardon WJ (1995) Uptake of soil cadmium by 3 field crops and its prediction by a PH-dependent FREUNDLICH sorption model. Plant Soil 171:263–266CrossRefGoogle Scholar
  7. Fedotov PS, Kordel W, Miro M, Peijnenburg W, Wennrich R, Huang PM (2012) Extraction and fractionation methods for exposure assessment of trace metals, metalloids, and hazardous organic compounds in terrestrial environments. Crit Rev Environ Sci Technol 42:1117–1171. CrossRefGoogle Scholar
  8. Ferri R, Hashim D, Smith DR, Guazzetti S, Donna F, Ferretti E, Curatolo M, Moneta C, Beone GM, Lucchini RG (2015) Metal contamination of home garden soils and cultivated vegetables in the province of Brescia, Italy: implications for human exposure. Sci Total Environ 518:507–517. CrossRefGoogle Scholar
  9. Fleming M, Tai Y, Zhuang P, McBride MB (2013) Extractability and bioavailability of Pb and As in historically contaminated orchard soil: effects of compost amendments. Environ Pollut 177:90–97. CrossRefGoogle Scholar
  10. GB2762-2012 (2012) Maximum levels of contaminants in foods vol GB2762-2012Google Scholar
  11. Gustafsson JP, Tiberg C, Edkymish A, Kleja DB (2011) Modelling lead(II) sorption to ferrihydrite and soil organic matter. Environ Chem 8:485–492. CrossRefGoogle Scholar
  12. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87. CrossRefGoogle Scholar
  13. Judy JD, Unrine JM, Rao W, Bertsch PM (2012) Bioaccumulation of gold nanomaterials by Manduca sextathrough dietary uptake of surface contaminated plant tissue. Environ Sci Technol 46:12672–12678. CrossRefGoogle Scholar
  14. Kar S, Das S, Jean J-S, Chakraborty S, Liu C-C (2013) Arsenic in the water-soil-plant system and the potential health risks in the coastal part of Chianan Plain, southwestern Taiwan. J Asian Earth Sci 77:295–302. CrossRefGoogle Scholar
  15. Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ Pollut 152:686–692. CrossRefGoogle Scholar
  16. Khan MU, Malik RN, Muhammad S (2013) Human health risk from heavy metal via food crops consumption with wastewater irrigation practices in Pakistan. Chemosphere 93:2230–2238. CrossRefGoogle Scholar
  17. Kurt-Karakus PB (2012) Determination of heavy metals in indoor dust from Istanbul, Turkey: estimation of the health risk. Environ Int 50:47–455 Doi:
  18. Laborda F, Bolea E, Górriz MP, Martín-Ruiz MP, Ruiz-Beguería S, Castillo JR (2008) A speciation methodology to study the contributions of humic-like and fulvic-like acids to the mobilization of metals from compost using size exclusion chromatography–ultraviolet absorption–inductively coupled plasma mass spectrometry and deconvolution analysis. Anal Chim Acta 606(1):1–8. CrossRefGoogle Scholar
  19. Lavado RS, Rodríguez MB, Taboada MA (2005) Treatment with biosolids affects soil availability and plant uptake of potentially toxic elements. Agric, Ecosyst Environ 109:360–364. CrossRefGoogle Scholar
  20. Li ZY, Ma ZW, van der Kuijp TJ, Yuan ZW, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853. CrossRefGoogle Scholar
  21. Lindberg S, Landberg T, Greger M (2004) A new method to detect cadmium uptake in protoplasts. Planta 219:526–532. CrossRefGoogle Scholar
  22. Linde M, Öborn I, Gustafsson JP (2007) Effects of changed soil conditions on the mobility of trace metals in moderately contaminated urban soils. Water Air Soil Pollut 183:69–83. CrossRefGoogle Scholar
  23. Liu XM, Song Q, Tang Y, Li W, Xu J, Wu J, Wang F, Brookes PC (2013) Human health risk assessment of heavy metals in soil-vegetable system: a multi-medium analysis. Sci Total Environ 463:530–540. CrossRefGoogle Scholar
  24. Loutfy N, Fuerhacker M, Tundo P, Raccanelli S, El Dien AG, Ahmed MT (2006) Dietary intake of dioxins and dioxin-like PCBs, due to the consumption of dairy products, fish/seafood and meat from Ismailia city, Egypt. Sci Total Environ 370:1–8. CrossRefGoogle Scholar
  25. Luo L, Chu B, Liu Y, Wang X, Xu T, Bo Y (2014) Distribution, origin, and transformation of metal and metalloid pollution in vegetable fields, irrigation water, and aerosols near a Pb-Zn mine. Environ Sci Pollut Res 21:8242–8260. CrossRefGoogle Scholar
  26. Luo L, Shen Y, Liu J, Zeng Y (2016) Investigation of Pb species in soils, celery and duckweed by synchrotron radiation X-ray absorption near-edge structure spectrometry. Spectrochim Acta Part B: At Spectrosc 122:40–45. CrossRefGoogle Scholar
  27. Marguı́ E, Salvadó V, Queralt I, Hidalgo M (2004) Comparison of three-stage sequential extraction and toxicity characteristic leaching tests to evaluate metal mobility in mining wastes. Anal Chim Acta 524:151–159. CrossRefGoogle Scholar
  28. McAloon KM, Mason RP (2003) Investigations into the bioavailability and bioaccumulation of mercury and other trace metals to the sea cucumber, Sclerodactyla briareus, using in vitro solubilization. Mar Pollut Bull 46:1600–1608. CrossRefGoogle Scholar
  29. Meers E, Samson R, Tack FMG, Ruttens A, Vandegehuchte M, Vangronsveld J, Verloo MG (2007) Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris. Environ Exp Bot 60:385–396. CrossRefGoogle Scholar
  30. Moreno-Jiménez E, Fernández JM, Puschenreiter M, Williams PN, Plaza C (2016) Availability and transfer to grain of As, Cd, Cu, Ni, Pb and Zn in a barley agri-system: impact of biochar, organic and mineral fertilizers. Agric, Ecosyst Environ 219:171–178. CrossRefGoogle Scholar
  31. Nyquist J, Greger M (2009) Response of two wetland plant species to cd exposure at low and neutral pH. Environ Exp Bot 65:417–424. CrossRefGoogle Scholar
  32. Oyeyiola AO, Olayinka KO, Alo BI (2011) Comparison of three sequential extraction protocols for the fractionation of potentially toxic metals in coastal sediments. Environ Monit Assess 172:319–327. CrossRefGoogle Scholar
  33. Pinto E, Almeida AA, Ferreira IMPLVO (2015) Assessment of metal(loid)s phytoavailability in intensive agricultural soils by the application of single extractions to rhizosphere soil. Ecotoxicology and Environmental Safety 113:418–424. CrossRefGoogle Scholar
  34. Pueyo M, Mateu J, Rigol A, Vidal M, López-Sánchez JF, Rauret G (2008) Use of the modified BCR three-step sequential extraction procedure for the study of trace element dynamics in contaminated soils. Environ Pollut 152:330–341. CrossRefGoogle Scholar
  35. Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541. CrossRefGoogle Scholar
  36. Salati S, Quadri G, Tambone F, Adani F (2010) Fresh organic matter of municipal solid waste enhances phytoextraction of heavy metals from contaminated soil. Environ Pollut 158:1899–1906. CrossRefGoogle Scholar
  37. Shaheen SM (2009) Sorption and lability of cadmium and lead in different soils from Egypt and Greece. Geoderma 153:61–68. CrossRefGoogle Scholar
  38. Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74:78–84. CrossRefGoogle Scholar
  39. Shen Y (2014) Distribution and speciation of lead in model plant Arabidopsis thaliana by synchrotron radiation X-ray fluorescence and absorption near edge structure spectrometry. X-Ray Spectrom 43:146–151. CrossRefGoogle Scholar
  40. Shen YT, Song YF (2017) Effects of organic ligands on Pb absorption and speciation changes in Arabidopsis as determined by micro X-ray fluorescence and X-ray absorption near-edge structure analysis. J Synchrotron Radiat 24:463–468. CrossRefGoogle Scholar
  41. Slaveykova VI, Wilkinson KJ, Ceresa A, Pretsch E (2003) Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii. Environ Sci Technol 37:1114–1121. CrossRefGoogle Scholar
  42. Sterckeman T, Carignan J, Srayeddin I, Baize D, Cloquet C (2009) Availability of soil cadmium using stable and radioactive isotope dilution. Geoderma 153:372–378. CrossRefGoogle Scholar
  43. Sterckeman T, Redjala T, Morel JL (2011) Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. Environ Exp Bot 74:131–139. CrossRefGoogle Scholar
  44. Sutherland RA (2010) BCR®-701: a review of 10-years of sequential extraction analyses. Anal Chim Acta 680:10–20. CrossRefGoogle Scholar
  45. Sutherland RA, Tack FMG (2003) Fractionation of Cu, Pb and Zn in certified reference soils SRM 2710 and SRM 2711 using the optimized BCR sequential extraction procedure. Adv Environ Res 8:37–50. CrossRefGoogle Scholar
  46. Tahervand S, Jalali M (2016) Sorption, desorption, and speciation of Cd, Ni, and Fe by four calcareous soils as affected by pH. Environ Monit Assess 188:322. CrossRefGoogle Scholar
  47. Tang W, Zhong H, Xiao L, Tan Q, Zeng Q, Wei Z (2017) Inhibitory effects of rice residues amendment on Cd phytoavailability: a matter of Cd-organic matter interactions? Chemosphere 186:227–234. CrossRefGoogle Scholar
  48. Tian K, Yang J, Sun ZJ, Zhou YM, Xing SC, Feng YP (2017) Preparation of soil certified reference materials for heavy metals in contaminated sites rock and mineral. Analysis 36:82–88Google Scholar
  49. Tiwari KK, Singh NK, Patel MP, Tiwari MR, Rai UN (2011) Metal contamination of soil and translocation in vegetables growing under industrial wastewater irrigated agricultural field of Vadodara, Gujarat, India. Ecotoxicol Environ Saf 74:1670–1677. CrossRefGoogle Scholar
  50. Tokahoglu S, Kartal S (2004) Bioavailability of soil-extractable metals to tea plant by BCR sequential extraction procedure. Instrum Sci Technol 32:387–400. CrossRefGoogle Scholar
  51. Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337. CrossRefGoogle Scholar
  52. Wang P, Kinraide TB, Zhou DM, Kopittke PM, Peijnenburg W (2011) Plasma membrane surface potential: dual effects upon ion uptake and toxicity. Plant Physiol 155:808–820. CrossRefGoogle Scholar
  53. Wang T-J, Pan J, Liu X-L (2016a) Speciation and translocation characteristics of soil heavy metals in the water level fluctuating zone of Pengxi River in three gorges reservoir area rock and mineral. Analysis 35:425–432. CrossRefGoogle Scholar
  54. Wang T-Y, Zhou G-h, Sun B-B, He L, Zeng D-M, Chen Y-D, Ye R (2016b) Soils and Rice in coastal areas, Fujian Province, including influencing factors rock and mineral. Analysis 35:295–301. CrossRefGoogle Scholar
  55. Wang L, Yang L-F, Tan X-Z, Wu Z-H (2017) Determination of cd in environmental geological samples by inductively coupled plasma-mass spectrometry with membrane desolvation rock and mineral. Analysis 36:574–580. CrossRefGoogle Scholar
  56. Zhao Q, An M, Chen H (2018) Research on geochemical characteristics of soil in a chemical industrial factory site in Jinan City[J]. Rock Miner Anal Rock Miner Anal 37:201–208. CrossRefGoogle Scholar
  57. Zhuang P, McBride MB, Xia HP, Li NY, Lia ZA (2009) Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Sci Total Environ 407:1551–1561. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.National Research Center of GeoanalysisBeijingChina

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