Bioconcentration and translocation of Cd and Hg in a tomato (Solanum lycopersicum) from cultivated soils in southeastern Brazil

  • Clara A. I. Lima
  • Inacio A. Pestana
  • Lucas S. AzevedoEmail author
  • Daniel P. Ribeiro
  • Marcelo G. Almeida
  • Claudia L. Prins
  • Claudio R. Marciano
  • Cristina M. M. Souza


Food is the main source of toxic metals like mercury (Hg) and cadmium (Cd) to humans. This study evaluated the accumulation and translocation of Cd and Hg in a soil-plant system in four tomato plantations and assessed the risk associated with ingestion of these metals. Ten soil samples (rhizosphere) and 10 samples of plant tissues (leaf, ripe fruit, green fruit, and roots) were collected in each plantation. Spatial variation in Cd and Hg concentrations was negligible. The Cd level in rhizosphere was lower in comparison with that of plant tissues. Hg levels in rhizosphere were similar to roots and higher than the value observed in aerial parts of plants. The Cd bioconcentration factor was approximately five times higher compared to that of Hg. Approximately 93% and 48.6% of Cd and Hg accumulated in roots reached aerial parts, respectively. Our results indicate that tomato readily absorbs Cd accumulated in soil, translocating it to aerial parts. Comparatively, the absorption of Hg is not efficient. Levels of Cd in tomatoes were over 17 times higher than the maximum residual levels in 57.5% of ripe fruits and in 27.5% of green tomatoes.


Agricultural soil Mercury Cadmium Tomato Risk assessment 



The authors thank the Laboratory of Environmental Sciences of the State University of the North of Rio de Janeiro (Laboratório de Ciências Ambientais, LCA, da Universidade Estadual Norte Fluminense, UENF) for metal determinations.

Funding information

C.M.M. Souza received financial support from the Carlos Chagas Filho Research Support Foundation of the State of Rio de Janeiro (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, FAPERJ; C-26/111.368/2012). This study was also financed in part by Coordenação de Aperfeiçoamento de Pessoa de Nível Superior – Brazil (CAPES) – Finance Code 001.


  1. Agência Nacional de Vigilância Sanitária (ANVISA) (2013) Provides for the MERCOSUR Technical Regulation on Maximum Limits of Inorganic Contaminants in Foods. Resolution RDC n. 42, of August 29, 2013, ANVISA, Brasilia, Brazil.Google Scholar
  2. Agency for Toxic Substances and Disease Registry (ATSDR) (2017) U.S. Department of Health and Human Services. Priority list of hazardous substances. Digital report. Accessed 4 Dec 2016.
  3. Ahmad, P., Nabi, G., & Ashraf, M. (2011). Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. South African Journal of Botany, 77, 36–44.CrossRefGoogle Scholar
  4. Ahmad, A., Hadi, F., & Ali, N. (2015). Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytor, 17, 56–65.CrossRefGoogle Scholar
  5. Behring, S. B. (2007). Influência do manejo do solo e da dinâmica da água no sistema de produção do tomate de mesa: subsídios a sustentabilidade agrícola do Noroeste Fluminense. PhD thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.Google Scholar
  6. Benavides, M. P., Gallego, S. M., & Tomaro, M. L. (2005). Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17, 21–34.CrossRefGoogle Scholar
  7. Bonanno, G., Vymazal, J., & Cirelli, G. L. (2018). Translocation, accumulation and bioindication of trace elements in wetland plants. SciTotal Environ, 631-632, 252–261.Google Scholar
  8. Bothe, H., & Słomka, A. (2017). Divergent biology of facultative heavy metal plants. Journal of Plant Physiology, 219, 45–61.CrossRefGoogle Scholar
  9. Câmara, V. M., Campos, R. C., Perez, M. A., Tambelini, A. T., & Klein, C. H. (1986). Teores de mercúrio no cabelo: um estudo comparativo em trabalhadores da lavoura de cana-de-açúcar com exposição pregressa aos fungicidas organo-mercuriais no município de Campos-RJ. Cad Saúde Pública, 2, 359–372.CrossRefGoogle Scholar
  10. Camargo, F. P., & Filho, W. P. C. (2008). Produção de tomate de mesa no Brasil, 1990-2006: contribuição da área e da produtividade. Horicultura Brasileira, 26, 1018–1021.Google Scholar
  11. Carvalho, C. R. F., Ponciano, N. J., Souza, P. M., Souza, C. L. M., & Sousa, E. F. (2014). Economic feasibility and risk tomato production in the municipality of Cambuci/RJ, Brazil. Ciência Rural, 44, 2293–2299.CrossRefGoogle Scholar
  12. Chen, J., & Yang, Z. M. (2012). Mercury toxicity, molecular response and tolerance in higher plants. Biometals, 25, 847–857.CrossRefGoogle Scholar
  13. Chinese Environmental Protection Administration (CEPA). (1990). Elemental background values of soils in China. Beijing: Environmental Science Press of China.Google Scholar
  14. Chojnacka, K., Chojnacki, A., Górecka, H., & Górecki, H. (2005). Bioavailability of heavy metals from polluted soils to plants. Sci Total Environ, 337, 175–182.CrossRefGoogle Scholar
  15. Ciminelli, V. S. T., Gasparon, M., Ng, J. C., Silva, G. C., & Caldeira, C. L. (2017). Dietary arsenic exposure in Brazil: The contribution of rice and beans. Chemosphere, 168, 996–1003.CrossRefGoogle Scholar
  16. Clemens, S. (2006). Toxic metal accumulation responses to exposure and mechanisms of tolerance in plants. Biochim, 8, 707–1719.Google Scholar
  17. Conselho Nacional do Meio Ambiente (CONAMA). (2009). Resolution no. 420 of 28 December 2009. Accessed 28 December 2016.
  18. Dziubanek, G., Baranowska, R., Ćwielag-Drabek, M., Spychała, A., Piekut, A., Rusin, M., & Hajok, I. (2017). Cadmium in edible plants from Silesia, Poland, and its implications for health risk in populations. Ecotoxicology and Environmental Safety, 142, 8–13.CrossRefGoogle Scholar
  19. Fadigas, S. F., Amaral Sobrinho, N. B., Mazur, N., Anjos, L. H. C., & Freixo, A. A. (2006). Proposição de valores de referência para a concentração natural de metais pesados em solos brasileiros. Revista Brasileira de Engenharia Agrícola e Ambiental, 10, 699–705.CrossRefGoogle Scholar
  20. Food and Agriculture Organization of the United Nations (FAO). (2009). CODEX general standard for contaminants and toxins in food and feed (pp. 193–1995). CODEX STAN Accessed 27 Jan 2017.
  21. Food and Agriculture Organization of The United Nations (FAOSTAT), World Productivity (2013) Accessed 04 Set 2017.
  22. Gresens, R. L. (1967). Composition-volume relationships of metasomatism. Chemical Geology, 2, 47–55.CrossRefGoogle Scholar
  23. Instituto Brasileiro de Geografia e Estatística (IBGE). (2010). Household per capita food purchase per group, subgroups and products. Family Budget Research in, 2008–2009.Google Scholar
  24. Jesus, T. B., Carvalho, C. E. V., Ferreira, A. G., Siqueira, E. M., & Machado, A. L. S. (2012). Mercury distribution in muscular tissue of a tropical carnivorous fish (Hoplias malabaricus) from four lakes in the north of Rio de Janeiro state, SE Brazil. Journal of the Brazilian Society of Ecotoxicology, 7, 37–42.CrossRefGoogle Scholar
  25. Kabata-Pendias, A. (2010). Trace elements in soils and plants (4th ed.). Taylor & Francis Group, CRC Press: Boca Raton.CrossRefGoogle Scholar
  26. Kachenko, A. G., & Singh, B. (2006). Heavy metal contamination in vegetables grown in urban and metal smelter contaminated sites in Australia. Water, Air, and Soil Pollution, 169, 101–123.CrossRefGoogle Scholar
  27. Lacerda, L. D., Paraquetti, H. H. M., Rezende, C. E., Silva, L. F. F., Silva Filho, E. V., Marins, R. V., & Ribeiro, M. G. (2002). Mercury concentrations in bulk atmospheric deposition over the coast of Rio de Janeiro Southeast Brazil. Journal of the Brazilian Chemical Society, 13, 165–169.CrossRefGoogle Scholar
  28. Liu, X., Zhong, L., Meng, J., Wang, F., Zhang, J., Zhi, Y., Zeng, L., Tang, X., & Xu, J. (2018). A multi-medium chain modeling approach to estimate the cumulative effects of cadmium pollution on human health. Environmental Pollution, 239, 308–317.CrossRefGoogle Scholar
  29. Lu, L., Tian, S., Yang, X., Wang, X., Brown, P., Li, T., & He, Z. (2008). Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. Journal of Experimental Botany, 59, 3203–3213.CrossRefGoogle Scholar
  30. Lugon-Moulin, N., Ryan, L., Donini, P., & Rossi, L. (2006). Cadmium content of phosphate fertilizers used for tobacco production. Agronomy for Sustainable Development, 26, 151–155.CrossRefGoogle Scholar
  31. Marrugo-Negrete, J., Durango-Hernández, J., Pinedo-Hernández, J., Olivero-Verbel, J., & Díez, S. (2015). Phytoremediation of mercury-contaminated soils by Jatropha curcas. Chemosphere, 127, 58–63.CrossRefGoogle Scholar
  32. Marrugo-Negrete, J., Durango-Hernández, J., Pinedo-Hernández, J., Enamorado-Montes, G., & Díez, S. (2016). Mercury uptake and effects on growth in Jatropha curcas. Journal of Environmental Sciences, 48, 120–125.CrossRefGoogle Scholar
  33. McLaughlin MJ, Singh BR (1999). Cadmium in soils and plants. In: McLaughlin M.J., Singh B.R. (eds) Cadmium in soils and plants. Developments in Plant and Soil Sciences Springer Dordrecht 85:1–9.Google Scholar
  34. Mnisi, R. L., Ndibewu, P. P., Mafu, L. D., & Bwembya, G. C. (2017). Bioaccessibility and risk assessment of essential and non-essential elements in vegetables commonly consumed in Swaziland. Ecotoxicology and Environmental Safety, 144, 396–401.CrossRefGoogle Scholar
  35. Moreno-Jiménez, E., Peñalosa, J. M., Esteban, E., & Carpena-Ruiz, R. O. (2007). Mercury accumulation and resistance to mercury stress in Rumex induratus and Marrubium vulgare grown in perlite. Journal of Plant Nutrition and Soil Science, 170, 485–494.CrossRefGoogle Scholar
  36. National Food Safety Standard of Maximum Levels of Contaminants in Foods (CHINA). (2014). Beijing. Accessed 27 January 2017.Google Scholar
  37. Nazar, R., Iqbal, N., Masood, A., Iqbal, M., Khan, R., Syeed, S., & Khan, N. A. (2012). Cadmium toxicity in plants and role of mineral nutrients in its alleviation. American Journal of Plant Sciences, 3, 1476–1489.CrossRefGoogle Scholar
  38. Park, B. J., Lee, J. H., & Kim, W. I. (2011). Influence of soil characteristics and arsenic, cadmium, and lead contamination on their accumulation levels in rice and human health risk through intake of rice grown nearby abandoned mines. J Korean Soc Appl Bi, 54, 575–582.CrossRefGoogle Scholar
  39. Patra, M., & Sharma, A. (2000). Mercury toxicity in plants. The Botanical Review, 66, 379–422.CrossRefGoogle Scholar
  40. Patra, M., Bhowmik, N., Bandopadhyay, B., & Sharma, A. (2004). Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environmental and Experimental Botany, 52, 199–223.CrossRefGoogle Scholar
  41. R Core Team. (2018). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  42. Rehman, Z. U., Khan, S., Brusseau, M. L., & Shah, M. T. (2016). Lead and cadmium contamination and exposure risk assessment via consumption of vegetables grown in agricultural soils of five-selected regions of Pakistan. Chemosphere, 168, 1589–1596.CrossRefGoogle Scholar
  43. Rempe, E. F., Amorim, L. A., Vasconcelos Neto, R. (2010). Information collection on mercury including environmental standards in Brazil. 4th Meeting of the Mercury Lamps Working Group. Technical Chamber of Health Environmental Sanitation and Waste Management of the National Environment Council. Department of Environmental Health Surveillance and Occupational Health Brasília, Brazil.Google Scholar
  44. Rice, K. M., Walker, E. M., Jr., Wu, M., Gillette, C., & Blough, E. R. (2014). Environmental mercury and its toxic effects. Journal of Preventive & Public Health, 47, 74–83.CrossRefGoogle Scholar
  45. Rodríguez, E., Peralta-Videa, J. R., Israr, M., Sahi, S. V., Pelayo, H., Sáchez-Salcido, B., & Gardea-Torresdey, J. L. (2009). Effect of mercury and gold on growth, nutrient uptake, and anatomical changes in Chilopsis linearis. Environmental and Experimental Botany, 65, 253–262.CrossRefGoogle Scholar
  46. Ruiz, O. N., Hussein, H. S., Terry, N., & Daniell, H. (2003). Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiology, 132, 1344–1352.CrossRefGoogle Scholar
  47. Santos, E. J., Herrmann, A. B., Frescura, V. L. A., & Curtius, A. J. (2005). Simultaneous determination of As, Hg, Sb, Se and Sn in sediments by slurry sampling axial view inductively coupled plasma optical emission spectrometry using on-line chemical vapor generation with internal standardization. Journal of Analytical Atomic Spectrometry, 20, 538–543.CrossRefGoogle Scholar
  48. Silva-Filho, E. V., Machado, W., Oliveira, R. R., Sella, S. M., & Lacerda, L. D. (2006). Mercury deposition through litterfall in an Atlantic Forest at Ilha Grande, Southeast Brazil. Chemosphere, 65, 2477–2484.CrossRefGoogle Scholar
  49. Singh, A., & Prasad, S. M. (2014). Effect of agro-industrial waste amendment on Cd uptake in Amaranthus caudatus grown under contaminated soil: an oxidative biomarker response. Ecotoxicology and Environmental Safety, 100, 105–113.CrossRefGoogle Scholar
  50. Tellez-Plaza, M., Navas-Acien, A., Menke, A., Crainiceanu, C. M., Pastor-Barriuso, R., & Guallar, E. (2012). Cadmium exposure and all-cause and cardiovascular mortality in the U.S. general population. Environmental Health Perspectives, 120, 1017–1022.CrossRefGoogle Scholar
  51. Tkalec, M., Prebeg, T., Roje, V., Pevalek-Kozlina, B., & Ljubešić, N. (2008). Cadmium induced responses in duckweed Lemna minor L. Acta Physiologiae Plantarum, 30, 881–890.CrossRefGoogle Scholar
  52. Tkalec, M., Stefanic, P. P., Cvjetko, P., Sikic, S., Pavlica, M., & Balen, B. (2014). The effects of cadmium-zinc interactions on biochemical responses in tobacco seedlings and adult plants. PLoS One, 9, 1–13.CrossRefGoogle Scholar
  53. Tran, T. A., Vassileva, V., Petrov, P., & Popova, L. P. (2013). Cadmium-induced structural disturbances in Pisum sativum leaves are alleviated by nitric oxide. Turkish Journal of Botany, 37, 698–707.Google Scholar
  54. Ulrich, B., & Sumner, M. E. (1991). Soil acidity. Berlin, Germany: Springer-Verlag.CrossRefGoogle Scholar
  55. Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S. Fourth edition. New York: Springer. Accessed 10 April 2016.CrossRefGoogle Scholar
  56. Yoon, J., Cao, X., Zhou, Q., & Ma, Q. L. (2006). Accumulation of Pb Cu and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment, 368, 456–464.CrossRefGoogle Scholar
  57. Yu, H., Li, J., & Luan, Y. (2018). Meta-analysis of soil mercury accumulation by vegetables. Scientific Reports, 8, 1261.CrossRefGoogle Scholar
  58. Zhang, J., & Liu, C. L. (2002). Riverine composition and estuarine geochemistry of particulate metals in China – weathering features anthropogenic impact and chemical fluxes. Estuarine, Coastal and Shelf Science, 54, 1051–1070.CrossRefGoogle Scholar
  59. Zhao, X., & Wang, D. (2010). Mercury in some chemical fertilizers and the effect of calcium superphosphate on mercury uptake by corn seedlings (Zea mays L.). Journal of Environmental Sciences (China), 22, 1184–1188.CrossRefGoogle Scholar
  60. Zoffoli, H., Amaral-Sobrinho, N. M. B., Luisi, M. V., Zonta Marcon, G., & Tólon-Becerra, A. (2013). Inputs of heavy metals due to agrochemical use in tobacco fields in Brazil’s southern region. Environmental Monitoring and Assessment, 185, 2423–2437.CrossRefGoogle Scholar
  61. Zu, Y. Q., Li, Y., Chen, J. J., Chen, H. Y., Qin, L., & Schvartz, C. (2005). Hyperaccumulation of Pb Zn and Cd in herbaceous grown on lead–zinc mining area in Yunnan China. Environment International, 31, 755–762.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Clara A. I. Lima
    • 1
  • Inacio A. Pestana
    • 1
  • Lucas S. Azevedo
    • 1
    Email author
  • Daniel P. Ribeiro
    • 1
  • Marcelo G. Almeida
    • 1
  • Claudia L. Prins
    • 2
  • Claudio R. Marciano
    • 3
  • Cristina M. M. Souza
    • 1
  1. 1.Laboratório de Ciências Ambientais (LCA), Centro de Biociências e Biotecnologia (CBB)Universidade Estadual do Norte Fluminense Darcy RibeiroRio de JaneiroBrazil
  2. 2.Laboratório de Fitotecnia (LFIT), Centro de Ciências e Tecnologias Agropecuárias (CCTA)Universidade Estadual do Norte Fluminense Darcy RibeiroRio de JaneiroBrazil
  3. 3.Laboratório de solos (LSOL), Centro de Ciências e Tecnologias Agropecuárias (CCTA)Universidade Estadual do Norte Fluminense Darcy RibeiroRio de JaneiroBrazil

Personalised recommendations