Environmental Geochemistry and Health

, Volume 39, Issue 6, pp 1325–1334 | Cite as

Nickel accumulation in paddy rice on serpentine soils containing high geogenic nickel contents in Taiwan

  • Zeng-Yei Hseu
  • Yun-Jie Lai
Original Paper


We investigated the extractability of nickel (Ni) in serpentine soils collected from rice paddy fields in eastern Taiwan to evaluate the bioavailability of Ni in the soils as well as for demonstrating the health risks of Ni in rice. Total Ni concentrations in the soils ranged were 70.2–2730 mg/kg (mean, 472 mg/kg), greatly exceeding the natural background content and soil control standard in Taiwan. Available Ni concentration only accounts for <10% of total soil Ni content; 0.1 N HCl-extractable Ni was the more suitable index for Ni bioavailability in the soil to rice than was diethylenetriaminepentaacetic acid (DTPA)-extractable Ni. The accumulation ability of rice roots was much higher than that of its shoots; however, compared with those reported previously, our brown and polished rice samples contained much higher Ni concentrations, within the ranges of 1.50–4.53 and 2.45–5.54 mg/kg, respectively. On the basis of the provisional tolerable Ni intake for adults recommended by the World Health Organization (WHO), daily consumption of this rice can result in an excessive Ni intake.


Bioavailability Heavy metal Human health Serpentine Ultramafics 



The authors would like to thank the Ministry of Science and Technology of Taiwan, R.O.C., and the Environmental Protection Agency of Taiwan, R.O.C., for financially supporting this research under Grant Nos. MOST 105-2313-B-002-009-MY3 and EPA-100-GA103-02-A240.

Author contributions

Z-YH planned and designed the research, collected soil and rice samples, and wrote the first draft of the manuscript. Y-JL carried out the collection and analyses of the samples. All authors read and approved the final manuscript.


  1. Adriano, D. C. (1986). Trace elements in the terrestrial environment. New York, NY: Springer.CrossRefGoogle Scholar
  2. Alves, S., Trancoso, M. A., Goncalves, M. L. S., & Santos, M. M. C. (2011). A nickel availability study in serpentinised areas of Portugal. Geoderma, 164(3–4), 115–163.Google Scholar
  3. Antić-Mladenović, S., Rinklebe, J., Frohne, T., Stärk, H. J., Wennrich, R., Tomić, Z., et al. (2011). Impact of controlled redox conditions on nickel in a serpentine soil. Journal of Soils and Sediments, 11(3), 406–415.CrossRefGoogle Scholar
  4. Baker, D. E., & Amacher, M. C. (1982). Nickel, copper, zinc, and cadmium. In Page, A. L., Miller, R. H., & Keeney, D. R. (Eds.), Methods of soil analysis, Part 2. Chemical and microbiological methods, 2nd ed (pp. 323–336). Agron. Monogr. 9. Madison, WI: ASA and SSSA.Google Scholar
  5. Becquer, T., Quantin, C., Rotté-Capet, S., Ghanbaja, J., Mustin, C., & Herbillon, A. J. (2006). Sources of trace metals in Ferralsols in New Caledonia. European Journal of Soil Science, 57(2), 200–213.CrossRefGoogle Scholar
  6. Bhattacharyya, P., Chakrabarti, K., Chakraborty, A., Tripathy, S., Kim, K., & Powell, M. A. (2008). Cobalt and nickel uptake by rice and accumulation in soil amended with municipal solid waste compost. Ecotoxicology and Environmental Safety, 69(3), 506–512.CrossRefGoogle Scholar
  7. Bini, C., Maleci, L., & Wahsha, M. (2017). Potentially toxic elements in serpentine soils and plants from Tuscany (Central Italy). A proxy for soil remediation. Catena, 148, 60–66.CrossRefGoogle Scholar
  8. Brooks, R. R. (1987). Serpentine and its vegetation: A multidisciplinary approach. London: Croom Helm.Google Scholar
  9. Cai, F., Ren, J., Tao, S., & Wang, X. (2016). Uptake, translocation and transformation of antimony in rice (Oryza sativa L.) seedlings. Environmental Pollution, 209, 169–176.CrossRefGoogle Scholar
  10. Chang, C. P., Angelier, J., & Huang, C. Y. (2000). Origin and evolution of a mélange: The active plate boundary and suture zone of the Longitudinal Valley, Taiwan. Tectonophysics, 325(1–2), 43–62.CrossRefGoogle Scholar
  11. Cheng, C. H., Jien, S. H., Tsai, H., Chang, Y. H., Chen, Y. C., & Hseu, Z. Y. (2009). Geochemical element differentiation in serpentine soils from the ophiolite complexes, eastern Taiwan. Soil Science, 174(5), 283–291.CrossRefGoogle Scholar
  12. Cheng, C. H., Jien, S. H., Iizuka, Y., Tsai, H., Chang, Y. S., & Hseu, Z. Y. (2011). Pedogenic chromium and nickel partitioning in serpentine soils along a toposequence. Soil Science Society of American Journal, 75(2), 659–668.CrossRefGoogle Scholar
  13. Garnier, J. M., Travassac, F., Lenoble, V., Rose, J., Zheng, Y., Hossain, M. S., et al. (2010). Temporal variations in arsenic uptake by rice plants in Bangladesh: The role of iron plaque in paddy fields irrigated with groundwater. Science of the Total Environment, 408(19), 4185–4193.CrossRefGoogle Scholar
  14. Gee, G. W., & Bauder, J. W. (1986). Particle-size analysis. In Klut, A. (Ed.), Methods of soil analysis, Part 1. Physical and mineralogical methods (pp. 383–411). Agron. Monogr. 9. Madison, WI: ASA and SSSA.Google Scholar
  15. Ho, C. P., Hseu, Z. Y., Chen, N. C., & Tsai, C. C. (2013). Evaluating heavy metal concentration of plants on a serpentine site for phytoremediation applications. Environmental Earth Science, 70(1), 191–199.CrossRefGoogle Scholar
  16. Hseu, Z. Y., & Iizuka, Y. (2013). Pedogeochemical characteristics of chromite in a paddy soil derived from serpentinites. Geoderma, 202–203, 126–133.CrossRefGoogle Scholar
  17. Hseu, Z. Y., Su, S. W., Lai, H. Y., Guo, H. Y., Chen, T. C., & Chen, Z. S. (2010). Remediation techniques and heavy metals uptake by different rice varieties in metals-contaminated soils of Taiwan. New aspects for food safety regulation and sustainable agriculture. Soil Science and Plant Nutrition, 56(1), 31–52.CrossRefGoogle Scholar
  18. Hseu, Z. Y., Watababe, T., Nakao, A., & Funakawa, S. (2015a). Partition of geogenic nickel in paddy soils derived from serpentinites. Paddy and Water Environment, 14(3), 417–426.CrossRefGoogle Scholar
  19. Hseu, Z. Y., Zehetner, F., Ottner, F., & Iizuka, Y. (2015b). Clay mineral transformations and heavy metal release in paddy soils formed on serpentinites in eastern Taiwan. Clays and Clay Minerals, 63(2), 119–131.CrossRefGoogle Scholar
  20. Hseu, Z. Y., Su, Y. C., Zehetner, F., & Hsi, H. C. (2017). Leaching potential of geogenic nickel in serpentine soils from Taiwan and Austria. Journal of Environmental Management, 186(2), 151–157.CrossRefGoogle Scholar
  21. Jien, S. H., Tsai, C. C., Hseu, Z. Y., & Chen, Z. S. (2011). Baseline concentrations of toxic elements in metropolitan park soils of Taiwan. Terrestrial and Aquatic Environmental Toxicology, 5, 1–7.Google Scholar
  22. Johnston, W. R., & Proctor, J. (1981). Growth of serpentine and non-serpentine races of Festuca rubra in solutions simulating the chemical conditions in a toxic serpentine soil. Journal of Ecology, 69(3), 855–869.CrossRefGoogle Scholar
  23. Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soils and plants. New York, NY: CRC Press.Google Scholar
  24. Khan, N., Seshadri, B., Bolan, N., Saint, C. P., Kirkham, M. B., Chowdhury, S., et al. (2016). Root iron plaque on wetland plants as a dynamic pool of nutrients and contaminants. Advances in Agronomy, 138, 1–96.CrossRefGoogle Scholar
  25. Kierczak, J., Pędziwiatr, A., Waroszewski, J., & Modelska, M. (2016). Mobility of Ni, Cr and Co in serpentine soils derived on various ultrabasic bedrocks under temperate climate. Geoderma, 268, 78–91.CrossRefGoogle Scholar
  26. Kyuma, K. (2004). Paddy soil science. Kyoto: Kyoto Univ. Press.Google Scholar
  27. Licina, V., Antic-Mladenovic, S., Kresovic, M., & Rinklebe, J. (2010). Effect of high nickel and chromium background levels in serpentine soil on their accumulation in organs of a perennial plant. Communications in Soil Science and Plant Analysis, 41(4), 482–496.CrossRefGoogle Scholar
  28. Lin, Y. H., Chen, S. S., Chen, M. L., Cheng, C. C., & Chou, S. S. (1996). The investigation of heavy metals (zinc, chromium, nickel) in milled rice. Annual Report of Food and Drug Administration, Taiwan ROC, 14, 289–297.Google Scholar
  29. Lin, H. T., Wong, S. S., & Li, G. C. (2004). Heavy metal content of rice and shellfish in Taiwan. Journal of Food and Drug Analysis, 12, 167–174.Google Scholar
  30. Lindsay, W. L., & Norvell, W. A. (1978). Development of DTPA soil test for Zn, Fe, Mn, Cu. Soil Science Society of American Journal, 42, 421–428.CrossRefGoogle Scholar
  31. McLean, E. O. (1982). Soil pH and lime requirement. In Page, A. L., Miller, R. H., & Keeney, D. R. (Eds.), Methods of soil analysis, Part 2. Chemical and microbiological methods, 2nd ed (pp. 199–224). Agron. Monogr. 9. Madison, WI: ASA and SSSA.Google Scholar
  32. Mehra, O. P., & Jackson, M. L. (1960). Iron oxides removed from soils and clays by a dithionite-citrate system buffered with sodium bicarbonate. Clays and Clay Minerals, 7(3), 317–327.Google Scholar
  33. Naseri, M., Vazirzadeh, A., Kazemi, R., & Zaheri, F. (2015). Concentration of some heavy metals in rice types available in Shiraz market and human health risk assessment. Food Chemistry, 175, 243–248.CrossRefGoogle Scholar
  34. Nelson, D. W., & Sommers, L. E. (1982). Total carbon, organic carbon, and organic matter. In Page, A. L., Miller, R. H., & Keeney, D. R. (Eds.), Methods of soil analysis, Part 2. Chemical and microbiological methods, 2nd ed (pp. 539–557). Agron. Monogr. 9. Madison, WI: ASA and SSSA.Google Scholar
  35. O’Hanley, D. S. (1996). Serpentinites: Records of tectonic and petrological history. New York, NY: Oxford University Press.Google Scholar
  36. Oze, C., Fendorf, S., Bird, D. K., & Coleman, R. G. (2004). Chromium geochemistry of serpentine soils. International Geology Review, 46(2), 97–126.CrossRefGoogle Scholar
  37. Pasha, Q., Malik, S. A., Shaheen, N., & Shah, M. H. (2010). Investigation of trace metals in the blood plasma and scalp hair of gastrointestinal cancer patients in comparison with controls. Clinica Chimica Acta, 411(7–8), 531–539.CrossRefGoogle Scholar
  38. Pollard, A. J., Reeves, R. D., & Baker, A. J. M. (2014). Facultative hyperaccumulation of heavy metals and metalloids. Plant Science, 217–218, 8–17.CrossRefGoogle Scholar
  39. Quantin, C., Ettler, V., Garnier, J., & Šebek, O. (2008). Sources and extractibility of chromium and nickel in soil profiles developed on Czech serpentinites. Comptes Rendus Geoscience, 340(12), 872–882.CrossRefGoogle Scholar
  40. Rahman, M. A., Rahman, M. M., Reichman, S. M., Lim, R. P., & Naidu, R. (2014). Heavy metals in Australian grown and imported rice and vegetables on sale in Australia: Health hazard. Ecotoxicology and Environmental Safety, 100, 53–60.CrossRefGoogle Scholar
  41. Rajapaksha, A. U., Vithanage, M., Oze, C., Bandara, W. M. A. T., & Weerasooriya, R. (2012). Nickel and manganese release in serpentine soil from the Ussangoda Ultramafic Complex, Sri Lanka. Geoderma, 189–190, 1–9.CrossRefGoogle Scholar
  42. Rinklebe, J., Antić-Mladenović, S., Frohne, T., Stärk, H. J., Tomić, Z., & Ličina, V. (2016). Nickel in a serpentine-enriched Fluvisol: Redox affected dynamics and binding forms. Geoderma, 263, 203–214.CrossRefGoogle Scholar
  43. Susaya, J. P., Kim, K. H., Asio, V. B., Chen, Z. S., & Navarrete, I. (2010). Quantifying nickel in soils and plants in an ultramafic area in Philippines. Environmental Monitoring and Assessment, 167(1), 505–514.CrossRefGoogle Scholar
  44. Tang, T., & Miller, D. M. (1991). Growth and tissue composition of rice grown in soil treated with inorganic copper, nickel, and arsenic. Communications in Soil Science and Plant Analysis, 22(19–20), 2037–2045.CrossRefGoogle Scholar
  45. Tashakor, M., Yaacob, W. Z. W., & Mohamad, H. (2011). Speciation and availability of Cr, Ni and Co in serpentine soils of Ranau, Sabah. American Journal of Geosciences, 2(1), 4–9.Google Scholar
  46. Umar, M. A., Ugonor, R., & Kolawole, S. A. (2013). Evaluation of nutritional value of wild rice from Kaduna state, central Nigeria. International Journal of Scientific & Technology Research, 2(7), 140–147.Google Scholar
  47. van der Ent, A., Baker, A. J. M., van Balgooy, M. M. J., & Tjoa, A. (2013). Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): Mining, nickel hyperaccumulators and opportunities for phytomining. Journal of Geochemical Exploration, 128, 72–79.CrossRefGoogle Scholar
  48. Vithanage, M., Rajapaksha, A. U., Oze, C., Rajakaruna, N., & Dissanayake, C. B. (2014). Metal release from serpentine soils in Sri Lanka. Environmental Monitoring and Assessment, 186(6), 3415–3429.CrossRefGoogle Scholar
  49. World Health Organization. (1994). Quality directive of potable water (2nd ed.). Geneva: WHO.Google Scholar
  50. World Health Organization. (1996). Trace elements in human nutrition and health. Geneva: WHO.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Department of Agricultural ChemistryNational Taiwan UniversityTaipeiTaiwan
  2. 2.Apollo Technology Co. LTDTaipeiTaiwan

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