Heavy metal assimilation in maize (Zea mays L.) plants growing near mine tailings

  • María Aurora ArmientaEmail author
  • Margarita Beltrán
  • Sarayth Martínez
  • Israel Labastida
Original Paper


Mining is one of the main economic activities in Mexico, and Hidalgo State is one of the main areas; however, this activity produces wastes, such as mine tailings, that are disposed in deposits and may be dispersed on the soils (e.g., agricultural soils). In this study, the concentrations of As and heavy metals in maize plants cultivated in a greenhouse in two soils influenced by tailings were evaluated. Plants were grown for 165 days in the soils (one of them more polluted due to a closer distance to the tailings) and one control soil close to the study zone. Plants’ growth was evaluated, and after harvesting, they were divided in six parts: root, stalk, plant leaves, cob sheath, corncob and grains. Plants showed depressed development: small height, slow growth and physiological cob immaturity. Assimilation of As and heavy metals by plants was influenced by the concentration of the contaminants but also by the availability of nutrients. Important concentrations of the metals were recorded in the harvestable parts (grain, stalk and cob sheath). The order of accumulation was Zn > Fe > Pb > As > Cd. Cadmium was not detected in grains, but a maximum concentration of As at 1.02 mg/kg and Pb at 3.9 mg/kg was measured in the dry grain. These As and Pb concentrations do not comply with CODEX Alimentarius standards for maize, which states that the cob must be free of heavy metals. In addition, Pb also exceeds the limits established by the Mexican NOM-247-SSA1-2008 regulation.


Arsenic Cadmium Crops Lead Translocation Zimapán 



The authors thank Olivia Cruz and Alejandra Aguayo for their skillful participation in the chemical analyses. We are indebted with two anonymous reviewers for their important suggestions.


Funding was provided by Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (Grant No. IN103114) and Secretaría de Educación Pública, México (UAM-EXB-175).


  1. Ahmed, U. A. R., & Mohamed, H. M. (2009). Effect of microbial inoculation and EDTA on the uptake and translocation of heavy metal by corn and sunflower. Chemosphere, 76, 893–899.CrossRefGoogle Scholar
  2. Andaluz, G. S. (2005). Estudio de los cambios inducidos por la deficiencia de hierro en el proteoma de plantas. Tesis Doctoral. Consejo Superior de Investigaciones Científicas Zaragoza. Departamento de Nutrición Vegetal. España.Google Scholar
  3. Arbaoui, S., Evlard, A., Mhamdi, M. E. W., Campanella, B., Paul, R., & Bettaieb, T. (2013). Potential of kenaf (Hibiscus cannabinus L.) and corn (Zea mays L.) for phytoremediation of dredging sludge contaminated by trace metals. Biodegradation, 24, 563–567.CrossRefGoogle Scholar
  4. Armienta, M. A., Mugica, V., Reséndiz, I., & Gutierrez, M. (2016). Arsenic and metals mobility in soils impacted by tailings at Zimapán, México. Journal of Soils and Sediments, 16, 1267–1278.CrossRefGoogle Scholar
  5. Armienta, M. A., Ongley, L. K., Rodríguez, R., Cruz, O., Mango, H., & Villaseñor, G. (2008). Arsenic distribution in mesquite (Prosopislaevigata) and huizache (Acacia farnesiana) in the Zimapán mining area, México. Geochemistry: Exploration, Environment, Analysis, 8(2), 191–197.Google Scholar
  6. ATDSR, Agency for Toxic Substances and Disease Registry. (2005). Toxicological profile for zinc. U.S. Department of Health and Human Services. Public Health Service.Google Scholar
  7. Baig, J. A., Kazi, T. G., Shah, A. Q., Arain, M. B., Afridi, H. I., Khan, S., et al. (2010). Evaluating the accumulation of arsenic in maize (Zea mays L.) plants from its growing media by cloud point extraction. Food and Chemical Toxicology, 48(11), 3051–3057.CrossRefGoogle Scholar
  8. Ban, Y., Xu, Z., Yang, Y., Zhang, H., Chen, H., & Tang, M. (2017). Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere, 27(2), 283–292.CrossRefGoogle Scholar
  9. Baran, A. (2013). Assessment of Zea mays sensitivity to toxic content of zinc. Polish Journal of Environmental Studies, 22(1), 77–83.Google Scholar
  10. Bashmakov, D. I., Lukatkin, A. S., Revin, V. V., Duchovskis, P., Brazaitytë, A., & Baranauskis, K. (2005). Growth of maize seedlings affected by different concentrations of heavy metals. Ekologija, 2005(3), 22–27.Google Scholar
  11. Beltrán, M. J., & Guerra, V. I. (2013). Cuando los nutrientes se vuelven tóxicos. Resource document. Instituto Nacional de Tecnología Agropecuaria. Retrieved October 14, 2018.
  12. Beltrán, V. M., Vaca, M. M., & González, A. A. (2009). Advances of phytoextraction, chapter 3. In L. G. Torres & R. E. Bandala (Eds.), Remediation of soils and aquifers (pp. 37–58). New York: Nova Science Publishers.Google Scholar
  13. Berardo, A., (2004). Manejo de la fertilización en una agricultura sustentable. Facultad de Ciencias Agrarias INTA Balcarce y Laboratorio de Suelos Fertilab. Informaciones Agronómicas No. 23, agosto.Google Scholar
  14. Burton, K. W., Morgan, E., & Roig, A. (1984). The influence of heavy metals upon the growth of sitka-spruce in South Wales forests. Plant and Soil, 78, 271–282.CrossRefGoogle Scholar
  15. Cantú, A. M. A., Reyes, M. C. A., & Rodríguez, B. L. A. (2010). La fecha de siembra: Una alternativa para incrementar la producción de maíz. Resource document. Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. Retrieved October 28, 2018.
  16. Castro-Larragoitia, J., Kramar, U., & Puchelt, H. (1997). 200 years of mining activities at La Paz/San Luis Potosi/Mexico—Consequences for environment and geochemical exploration. Journal of Geochemical Exploration, 58, 81–91.CrossRefGoogle Scholar
  17. Chan, D. Y., & Hale, B. A. (2004). Differential accumulation of Cd in durum wheat cultivars: uptake and retranslocation as sources of variation. Journal of Experimental Botany, 55, 2571–2579.CrossRefGoogle Scholar
  18. Cieslinski, G., Van Rees, K. C. J., Huang, P. M., Kozak, L. M., Rostad, H. P. W., & Knott, D. R. (1996). Cadmium uptake and bioaccumulation in selected cultivars of durum wheat and flax as affected by soil type. Plant and Soil, 182, 115–124.CrossRefGoogle Scholar
  19. CODEX, Comisión del CODEX Alimentarius del maíz. (1985). Norma del CODEX para el maíz. CODEX Standard 153-1985.Google Scholar
  20. Conor, R. (1980). Metal contamination of foods. Its significance for food quality and human health (3rd ed.). Oxford: Blackwell Science.Google Scholar
  21. Cuevas, G., & Walter, I. (2004). Metales pesados en maíz (Zea mays L.) cultivado en un suelo enmendado con diferentes dosis de compost de lodo residual. Revista Internacional de Contaminación Ambiental, 20(2), 59–68.Google Scholar
  22. Deras, F. H. (2011). Guía técnica del cultivo del maíz. IICA. Resource document. Instituto Interamericano de Cooperación para la Agricultura. Retrieved March 20, 2019.
  23. Dobermann, A., & Fairhurst, T. (2000). Rice: Nutrient disorders & nutrient management. Handbook series (1st ed.). Los Baños: IRRI, International Rice Research Institute.Google Scholar
  24. DOCE, Diario Oficial de las Comunidades Europeas. (2001). Reglamento (CE) No. 466/2001 de la Comisión de 8 de marzo de 2001. L 77/1. Contenido máximo de determinados contaminantes en los productos alimenticios.Google Scholar
  25. EPA, Environmental Protection Agency. (2000). Introduction to phytoremediation. EPA/600/R-99/107 February 2000. National Risk Management Research Laboratory. Office of Research and Development. U.S. Environmental Protection Agency. Cincinnati, Ohio 45268 revised edition, US.Google Scholar
  26. EPA, Environmental Protection Agency. (2003). Test methods. SW-846 7000A index to EPA tests methods, April 2003 revised edition, US.Google Scholar
  27. EPA, Environmental Protection Agency. (2007). Method 3051. microwave assisted acid digestion of sediments, sludges, soils and oils, US.Google Scholar
  28. FAO, Organización de las Naciones Unidas para la Agricultura y la Alimentación. (2009). Norma general del CODEX para los contaminantes y las toxinas presentes en los alimentos y piensos CODEX STAN 193-1995. Retrieved October 16, 2018.
  29. FAO, Organización de las Naciones Unidas para la Alimentación y la Agricultura. (2018). Manejo de suelos arenosos. Retrieved October 27, 2018.
  30. GEH, Gobierno del Estado de Hidalgo. (2016). Actualización del Programa Sectorial de Desarrollo Agropecuario 2011–2016. Secretaría de Planeación, Desarrollo Regional y Metropolitano. Subsecretaría de Planeación para el Desarrollo. Dirección General de Planeación y Prospectiva. Gobierno del Estado de Hidalgo.Google Scholar
  31. González-Cortés, N., Silos-Espino, H., Estrada, C. J. C., Chávez-Muñoz, J. A., & Tejero, J. L. (2016). Características y propiedades del maíz (Zea mays L.) criollo cultivado en Aguascalientes, México. Revista Mexicana de Ciencias Agrícolas, 7(3), 669–680.CrossRefGoogle Scholar
  32. Herrera, A. V., Carrasco, F. C., Sandoval, C. P., & Cortés, C. C. (2017). Transfer of arsenic in the water-soil-maize system of Zea Mays L. of cultivated in the quebrada de Camiña, northern Chile. Revista de la Sociedad Química del Perú, 83, 52–64.Google Scholar
  33. Kabata-Pendias, A. (2011). Trace elements in soil and plants (4th ed.). Boca Raton, FL: CRC Press.Google Scholar
  34. Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soil and plants (3rd ed.). Boca Raton, FL: CRC Press.Google Scholar
  35. Kabata-Pendias, A., & Szteke, B. (2015). Trace elements in abiotic and biotic environments. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
  36. Laperche, V., Logan, T. J., Gaddam, P., & Traina, S. J. (1997). Effect of apatite amendment on plant uptake of Pb from contaminated soil. Environmental Science and Technology, 31(10), 2745–2753.CrossRefGoogle Scholar
  37. Lu, Y., Luo, D., Liu, L., Tan, Z., Lai, A., Liu, G., et al. (2017). Leaching variations of heavy metals in chelator-assisted phytoextraction by Zea mays L. exposed to acid rainfall. Environmental Science and Pollution Research, 24, 1845–1853.CrossRefGoogle Scholar
  38. Martínez, C. M., Ortíz, P. R., & Raigón, D. M. (2017). Contenido de fósforo, potasio, zinc, hierro, sodio, calcio y magnesio, análisis de su variabilidad en accesiones cubanas de maíz. Cultivos Tropicales, 2017(38), 92–101.Google Scholar
  39. Marwa, E., Meharg, A., & Rice, C. M. (2012). Risk assessment of potentially toxic elements in agricultural soils and maize tissues from selected districts in Tanzania. Science of the Total Environment, 416, 180–186.CrossRefGoogle Scholar
  40. Méndez, M., & Armienta, M. A. (2003). Arsenic phase distribution in Zimapán mine tailings, México. Geofísica Internacional, 42(1), 131–140.Google Scholar
  41. Moreno, T. R., Téllez, H. J., & Monroy, F. M. G. (2012). Influencia de los minerales de los jales en la bioaccesibilidad de arsénico, plomo, zinc y cadmio en el distrito minero Zimapán, México. Revista Internacional de Contaminación Ambiental, 28(3), 203–218.Google Scholar
  42. Munive, C. R., Loli, F. O., Azabache, L. A., & Gamarra, S. G. (2018). Phytoremediation with corn (Zea mays L.) and Stevia compost on soils degraded by contamination with heavy metals. Scientia Agropecuaria, 9(4), 551–660.CrossRefGoogle Scholar
  43. NIH, National Institutes of Health. (2016). Hierro. Hoja informativa para consumidores. US. Department of Health & Human Services. Retrieved October 27, 2018.
  44. OECD, Organization for Economic Cooperation and Development. (2006). Test No. 208: Terrestrial plant test: Seedling emergence and seedling growth.Google Scholar
  45. OJEU, Official Journal of the European Union. (2006). Commission regulation (EC) No 1881/2006. L 364/5. Setting maximum levels for certain contaminants in foodstuffs. Retrieved October 26, 2018.
  46. Peuke, A. D., & Rennenberg, H. (2005). Phytoremediation, EMBO reports. European Molecular Biology Organization, 6(6), 497–501.Google Scholar
  47. Pizarro, H. K. (2015). Las comunidades indígenas de Hidalgo. Vol. I, II y III.Instituto de Ciencias Sociales y Humanidades. Fondo editorial UAEH, Universidad Autónoma del Estado de Hidalgo.Google Scholar
  48. Prieto-García, F., Callejas, H. J., Lechuga, M. A., Gaytán, J. C., & Barrado, E. E. (2005). Acumulación en tejidos vegetales de arsénico proveniente de aguas y suelos de Zimapán, estado de Hidalgo, México. Bioagro, 17(3), 135–139.Google Scholar
  49. Puga, P. A., De Mello, P. R., Mattiuz, B., Wyllyam, D. V., & Fonseca, I. M. (2013). Chemical composition of corn and sorghum grains cultivated in Oxisol with different application methods and doses of zinc. Ciencias de Investigación Agraria, 40(1), 97–108.CrossRefGoogle Scholar
  50. Rodríguez-Serrano, M., Martínez de la Casa, N., Romero-Puertas, M. C., del Río, L. A., & Sandalio, L. M. (2008). Toxicidad del cadmio en plantas. Ecosistemas, 17(3), 139–146.Google Scholar
  51. Rosas-Castor, J. M., Guzmán-Mar, J. L., Hernández-Ramírez, A., Garza-González, M. T., & Hinojosa-Reyes, L. (2014). Arsenic accumulation in maize crop (Zea mays): A review. Science of the Total Environment, 488–489, 176–187.CrossRefGoogle Scholar
  52. Ruíz, H. E. A., & Armienta, H. M. A. (2012). Acumulación de arsénico y metales pesados en maíz en suelos cercanos a jales o residuos mineros. Revista Internacional de Contaminación Ambiental, 28(2), 103–117.Google Scholar
  53. Secretaría de Economía. (2017). Minería. Retrieved October 10, 2018.
  54. SEMARNAT, Secretaría del Medio Ambiente y Recursos Naturales. (2000). NOM-021-SEMARNAT-2000. Norma Oficial Mexicana que establece las especificaciones de fertilidad, salinidad y clasificación de suelos, estudio y análisis. Diario Oficial de la Federación.Google Scholar
  55. SEMARNAT, Secretaría del Medio Ambiente y Recursos Naturales. (2004). NOM-147-SEMARNAT/SSA1-2004 Que establece criterios para determinar las concentraciones de remediación de suelos contaminados por arsénico, bario, berilio, cadmio, cromo hexavalente, mercurio, níquel, plata, plomo, selenio, talio y/o vanadio. México: Diario Oficial de la Federación.Google Scholar
  56. Song, W. Y., Sohn, E. J., Martinoia, E., Lee, Y. J., Yang, Y. Y., Yasinski, M., et al. (2003). Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nature Biotechnology, 21, 914–919.CrossRefGoogle Scholar
  57. SS, Secretaría de Salud. (2008). NOM-247-SSA1-2008. Productos y servicios. Cereales y sus productos. Cereales, harinas de cereales, sémolas o semolinas. Alimentos a base de cereales, semillas comestibles, de harinas, sémolas o semolinas o sus mezclas. Productos de panificación. Disposiciones y especificaciones sanitarias y nutrimentales.Google Scholar
  58. Vamerali, T., Bandiera, M., & Mosca, G. (2010). Field crops for phytoremediation of metal-contaminated land. A review. Environmental Chemistry Letters, 8(1), 1–17.CrossRefGoogle Scholar
  59. Zacarías, S. M., Beltrán, V. M., Torres, B. L. G., & González, A. A. (2012a). Assessment of in situ and ex situ phytorestoration with grass mixtures in soils polluted with nickel, copper, and arsenic. Physics and Chemistry of the Earth, 37–39(2012), 52–57.CrossRefGoogle Scholar
  60. Zacarías, S. M., Beltrán, V. M., Torres, B. L. G., & González, A. A. (2012b). A feasibility study of perennial/annual plant species to restore soils contaminated with heavy metals. Physics and Chemistry of the Earth, 37–39(2012), 37–42.CrossRefGoogle Scholar
  61. Zaman, S., Rajonee, A., & Imamul, H. S. (2017). Arsenic in Bangladesh soils and its relationship with water soluble soil organic carbon. Open Journal of Soil Science, 7, 77–85.CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Instituto de GeofísicaUniversidad Nacional Autónoma de México (UNAM)Mexico CityMexico
  2. 2.Departamento de EnergíaUniversidad Autónoma Metropolitana, Unidad AzcapotzalcoMexico CityMexico

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