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https://doi.org/10.18502/espoch.v4i1.15805
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Luis Fernández
Luis Fernández
Escuela Superior Politécnica de Chimborazo, Facultad de Ciencias, Ingeniería Ambiental, Macas, Ecuador
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Luis Yanchatipán
Luis Yanchatipán
Escuela Superior Politécnica de Chimborazo, Facultad de Ciencias, Ingeniería Ambiental, Macas, Ecuador
Published Date
- Apr 18, 2024
Cadmium in the Soil and its Presence in Cocoa
Abstract
Cadmium is a heavy metal from both natural and anthropogenic sources, whose concentration in the soil poses a real danger to the health of all organisms. In Ecuador, cocoa is an important agricultural product whose demand has grown over time. It is also the main source of livelihood for hundreds of small farmers. However, the presence of cadmium in the soil has become a major concern, as a result, several remediation methods have been proposed to eliminate or neutralize cadmium in the soil The bibliographic review proposes several physicochemical and biological methods capable of neutralizing the mobility of cadmium in the soil. The use of microorganisms capable of storing cadmium is a viable option due to its easy application and low implementation cost. The concentration of cadmium in cocoa beans shows values above the permissible limits established in Regulation No 488/2014 for cocoa products. Although there are no established values for cadmium concentrations in cocoa beans, this regulation can be taken as a reference in order to establish standards for cocoa production in Ecuador.
Keywords: cadmium, cocoa, maximum permissible levels, bioremediation, bioaccumulation.
Resumen
El cadmio, metal pesado proveniente de fuentes naturales como antropogénicas cuya concentración en el suelo supone un peligro real para la salud de todo organismo. En el Ecuador el cacao es un importante producto agrícola cuya demanda ha crecido con el tiempo además de ser el sustento de cientos de pequeños productores, por ello se han planteado varios métodos de remediación que permiten eliminar o en cuyo caso neutralizar la presencia de cadmio en el suelo. La revisión bibliográfica propone diversos métodos fisicoquímicos y biológicos capaces de neutralizar la movilidad del cadmio en el suelo. El uso de microorganismos capaces de almacenar el cadmio supone una opción viable por su fácil aplicación y bajo costo de implementación. La concentración de cadmio en las semillas de cacao muestra valores por encima de los límites permisibles establecidos en Reglamento N 488/2014 para productos derivados del cacao, aunque no exista valores establecido para concentraciones de cadmio en las semillas de cacao, se puede tomar como referencia este reglamento con el fin de establecer normas para la producción de cacao en el Ecuador.
Palabras Clave: Cadmio, Cacao, Máximos Permisibles, Biorremediación, Bioacumulación.
References
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[2] He S, He Z, Yang X, Stoffella PJ, Baligar VC. Soil Biogeochemistry, Plant Physiology, and Phytoremediation of Cadmium-Contaminated Soils. In: Advances in Agronomy. 2015. p. 135–225.
[3] Arroyave CQ, Araque PM, Pelaez J CA. BIOACCUMULATION AND TOXICITY EVALUATION OF CADMIUM AND MERCURY IN LLANERO GRASS (Brachiaria dictyoneura). Vol. 17. 2010.
[4] Peláez-Peláez MJ, Bustamante-Cano JJ, Gómez-López ED. Presencia de cadmio y plomo en suelos y su bioacumulación en tejidos vegetales en especies de brachiaria en el Magdalena Medio colombiano. Luna Azul. 2016 May 15;43:82–101.
[5] León-Villamar F, Calderón-Salazar J, Mayorga-Quinteros E. Estrategias para el cultivo, comercialización y exportación del cacao fino de aroma en Ecuador. Revista Ciencia UNEMI. 2016 Jun;9(18):45–55.
[6] Sanabria R. Toxicidad y acumulación de cadmio en poblaciones de diferentes especies de Artemia. Universidad de Valencia; 2002.
[7] Wu Q, Hendershot WH, Marshall WD, Ge Y. Speciation of cadmium, copper, lead, and zinc in contaminated soils. Commun Soil Sci Plant Anal. 2000 May 11;31(9–10):1129– 1144.
[8] Pardo M. INFLUENCE OF ELECTROLYTE ON CADMIUM INTERACTION WITH SELECTED ANDISOLS AND ALFISOLS. Soil Sci. 1997 Jun 2;162(10):733–740.
[9] Naidu R, Kookana RS, Sumner ME, Harter RD, Tiller KG. Cadmium Sorption and Transport in Variable Charge Soils: A Review. J Environ Qual. 1997 May;26(3):602– 617.
[10] Pardo MT, Guadalix ME. Cadmium sorption by two acid soils as affected by clearing and cultivation. Commun Soil Sci Plant Anal. 1995 Jan 11;26(1–2):289–302.
[11] García I, Simón M, Dorronsoro C, Aguilar J, Martín F, Ortiz I. CONTAMINACIÓN DE SUELOS POR OXIDACIÓN DE LODOS PIRÍTICOS. Edafología. 2000 Sep;7(3):159– 168.
[12] Hooda PS, Alloway BJ. Cadmium and lead sorption behaviour of selected English and Indian soils. Geoderma. 1998 Jun;84(1–3):121–134.
[13] Cala V, de La Flor M, Mencía R. Influencia de las características fisicoquímicas y mineralógicas en la distribución de metales pesados en suelos de cultivo. Boletín de la Sociedad Espa nola de la Ciencia del Suelo. 1997;1(2):205–213.
[14] Ma LQ, Tan F, Harris WG. Concentrations and Distributions of Eleven Metals in Florida Soils. J Environ Qual. 1997 May;26(3):769–775.
[15] Holmgren GGS, Meyer MW, Chaney RL, Daniels RB. Cadmium, Lead, Zinc, Copper, and Nickel in Agricultural Soils of the United States of America. J Environ Qual. 1993 Apr;22(2):335–348.
[16] de Azevedo F. Toxicologia do Mercúrio. Rima. 2003.
[17] Sanità di Toppi L, Gabbrielli R. Response to cadmium in higher plants. Environ Exp Bot. 1999 Apr;41(2):105–130.
[18] Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K. Physiological responses of Lemna trisulca L. (duckweed) to cadmium and copper bioaccumulation. Plant Science. 2001 Oct;161(5):881–889.
[19] Clemens S. Evolution and function of phytochelatin synthases. J Plant Physiol. 2006 Feb;163(3):319–332.
[20] Clemens S, Palmgren MG, Krämer U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 2002 Jul;7(7):309–315.
[21] Hart JJ, Norvell WA, Welch RM, Sullivan LA, Kochian L v. Characterization of Zinc Uptake, Binding, and Translocation in Intact Seedlings of Bread and Durum Wheat Cultivars. Plant Physiol. 1998 Sep 1;118(1):219–226.
[22] Cataldo DA, Garland TR, Wildung RE. Cadmium Uptake Kinetics in Intact Soybean Plants. Plant Physiol. 1983 Nov 1;73(3):844–848.
[23] Mullins GL, Sommers LE. Cadmium and zinc influx characteristics by intact corn (Zea mays L.) seedlings. Plant Soil. 1986 Jun;96(2):153–164.
[24] Homma Y, Hirata H. Kinetics of cadmium and zinc absorption by rice seedling roots. Soil Sci Plant Nutr. 1984 Dec;30(4):527–532.
[25] Watanabe K. Microorganisms relevant to bioremediation. Curr Opin Biotechnol. 2001 Jun;12(3):237–241.
[26] Gadd GM. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology (N Y). 2010 Mar 1;156(3):609–643.
[27] Kirchman DL. Processes in Microbial Ecology. Vol. 1. Oxford University Press; 2018.
[28] Gadd GM. Microbial influence on metal mobility and application for bioremediation. Geoderma. 2004 Oct;122(2–4):109–119.
[29] Valls M, de Lorenzo V. Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev. 2002 Nov;26(4):327–338.
[30] Gadd GM. Interactions of Fungi with Toxic Metals. In: The Genus Aspergillus. Boston, MA: Springer US; 1994. p. 361–374.
[31] Tabak HH, Lens P, van Hullebusch ED, Dejonghe W. Developments in Bioremediation of Soils and Sediments Polluted with Metals and Radionuclides – 1. Microbial Processes and Mechanisms Affecting Bioremediation of Metal Contamination and Influencing Metal Toxicity and Transport. Rev Environ Sci Biotechnol. 2005 Aug;4(3):115–156.
[32] Roberto N, Yong Y, Borges R, Olguín E. Fitorremediación: fundamentos y aplicaciones. Revista Ciencia. 2004;69–83.
[33] Leung A, Foster S. Encyclopedia of common natural ingredients used in food, drugs, and cosmetics. 2nd ed. New York; 1996. 649.
[34] Kalvatchev Z, Garzaro D, Cedezo F. Theobroma cacao L.: Un nuevo enfoque para nutrición y salud. Revista agroalimentaria. 1998;4(6):23–25.
[35] Pérez P, Azcona M. Los efectos del cadmio en la salud. Revista de Especialidades Médico-Quirúrgicas. 2012 Sep;17(3):199–205.
[36] Antoine JMR, Fung LAH, Grant CN. Assessment of the potential health risks associated with the aluminium, arsenic, cadmium and lead content in selected fruits and vegetables grown in Jamaica. Toxicol Rep. 2017;4:181–187.
[37] Gunnar N. ENCICLOPEDIA DE SALUD Y SEGURIDAD EN EL TRABAJO. In: METALES: PROPIEDADES QUIMICAS Y TOXICIDAD. 10th ed. 2013.
[38] Reyes Y, Vergara I, Torres O, Díaz M, González E. Contaminación por metales pesados Implicaciones en salud, ambiente y seguridad alimentaria. Ingeniería Investigación y Desarrollo: I2+D. 2016 Dec;16(2):66–77.
[39] Engbersen N, Gramlich A, Lopez M, Schwarz G, Hattendorf B, Gutierrez O, et al. Cadmium accumulation and allocation in different cacao cultivars. Science of The Total Environment. 2019 Aug;678:660–670.
[40] Maddela NR, Kakarla D, García LC, Chakraborty S, Venkateswarlu K, Megharaj M. Cocoa-laden cadmium threatens human health and cacao economy: A critical view. Science of The Total Environment. 2020 Jun;720:137645.
[41] Casteblanco JA. Técnicas de remediación de metales pesados con potencial aplicación en el cultivo de cacao. La Granja. 2018 Jan 11;27(1):21–35.
[42] Unión Europea-UE. Reglamento (UE) No 488/2014 de la comisión de 12 de mayo de 2014 que modifica el Reglamento (CE) no 1881/2006 por lo que respecta al contenido máximo de cadmio en los productos alimenticios. 2014.
[43] Jiménez C. Global legal status of cadmium in cacao (Theobroma cacao): a fantasy or a reality. Producción + Limpia. 2015 Jun;10(1):89–104.
[44] Pastor S. Niveles de cadmio en el chocolate: NM y ECA, sí; OTC, no. In: 2017 International Symposium on Cocoa Research (ISCR). Lima; 2017.
[45] Argüello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D. Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: A nationwide survey in Ecuador. Science of The Total Environment. 2019 Feb;649:120–127.
[46] Barraza F, Schreck E, Lévêque T, Uzu G, López F, Ruales J, et al. Cadmium bioaccumulation and gastric bioaccessibility in cacao: A field study in areas impacted by oil activities in Ecuador. Environmental Pollution. 2017 Oct;229:950–963.
[47] Hussain A, Ali S, Rizwan M, Zia-ur-Rehman M, Yasmeen T, Hayat MT, et al. Morphological and physiological responses of plants to cadmium toxicity. In: Cadmium toxicity and tolerance in plants. Elsevier; 2019. p. 47–72.
[48] Chang YS, Chang YJ, Lin CT, Lee MC, Wu CW, Lai YH. Nitrogen fertilization promotes the phytoremediation of cadmium in Pentas lanceolata. Int Biodeterior Biodegradation. 2013 Nov;85:709–714.
[49] Huang B, Xin J, Dai H, Liu A, Zhou W, Yi Y, et al. Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environmental Science and Pollution Research. 2015 Jan 15;22(2):1151–1159.
[50] Wang P, Deng X, Huang Y, Fang X, Zhang J, Wan H, et al. Root morphological responses of five soybean [Glycine max (L.) Merr] cultivars to cadmium stress at young seedlings. Environmental Science and Pollution Research. 2016 Jan 24;23(2):1860– 1872.
[51] Monteiro MS, Santos C, Soares AMVM, Mann RM. Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf. 2009 Mar;72(3):811–818.
[52] Tantalean Pedraza E, Huauya Rojas MÁ. Distribución del contenido de cadmio en los diferentes órganos del cacao CCN-51 en suelo aluvial y residual en las localidades de Jacintillo y Ramal de Aspuzana. Revista de Investigación de Agroproducción Sustentable. 2017 Aug 1;1(2):69.
[53] Hirzel J, Retamal-Salgado J, Walter I, Matus I. Cadmium accumulation and distribution in plants of three durum wheat cultivars under different agricultural environments in Chile. J Soil Water Conserv. 2017 Dec 24;72(1):77–88.
[54] Argüello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D. Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: A nationwide survey in Ecuador. Science of The Total Environment. 2019 Feb;649:120–127.
[55] Florida Rofner N, Claudio Melchor Sl, Gómez Bernal R. El pH Y La Absorción De Cadmio En Almendras De Cacao Orgánico (Theobroma Cacao L.) En Leoncio Prado, Huánuco, Peru. Folia Amazónica. 2019 Jan 28;27(1):1–8.
[56] Arévalo-Gardini E, Obando-Cerpa ME, Zú niga-Cernades LB, Arévalo-Hernández CO, Baligar V, He Z. METALES PESADOS EN SUELOS DE PLANTACIONES DE CACAO (Theobroma cacao L.) EN TRES REGIONES DEL PERÚ. Ecología Aplicada. 2016 Dec 22;15(2):81.
[2] He S, He Z, Yang X, Stoffella PJ, Baligar VC. Soil Biogeochemistry, Plant Physiology, and Phytoremediation of Cadmium-Contaminated Soils. In: Advances in Agronomy. 2015. p. 135–225.
[3] Arroyave CQ, Araque PM, Pelaez J CA. BIOACCUMULATION AND TOXICITY EVALUATION OF CADMIUM AND MERCURY IN LLANERO GRASS (Brachiaria dictyoneura). Vol. 17. 2010.
[4] Peláez-Peláez MJ, Bustamante-Cano JJ, Gómez-López ED. Presencia de cadmio y plomo en suelos y su bioacumulación en tejidos vegetales en especies de brachiaria en el Magdalena Medio colombiano. Luna Azul. 2016 May 15;43:82–101.
[5] León-Villamar F, Calderón-Salazar J, Mayorga-Quinteros E. Estrategias para el cultivo, comercialización y exportación del cacao fino de aroma en Ecuador. Revista Ciencia UNEMI. 2016 Jun;9(18):45–55.
[6] Sanabria R. Toxicidad y acumulación de cadmio en poblaciones de diferentes especies de Artemia. Universidad de Valencia; 2002.
[7] Wu Q, Hendershot WH, Marshall WD, Ge Y. Speciation of cadmium, copper, lead, and zinc in contaminated soils. Commun Soil Sci Plant Anal. 2000 May 11;31(9–10):1129– 1144.
[8] Pardo M. INFLUENCE OF ELECTROLYTE ON CADMIUM INTERACTION WITH SELECTED ANDISOLS AND ALFISOLS. Soil Sci. 1997 Jun 2;162(10):733–740.
[9] Naidu R, Kookana RS, Sumner ME, Harter RD, Tiller KG. Cadmium Sorption and Transport in Variable Charge Soils: A Review. J Environ Qual. 1997 May;26(3):602– 617.
[10] Pardo MT, Guadalix ME. Cadmium sorption by two acid soils as affected by clearing and cultivation. Commun Soil Sci Plant Anal. 1995 Jan 11;26(1–2):289–302.
[11] García I, Simón M, Dorronsoro C, Aguilar J, Martín F, Ortiz I. CONTAMINACIÓN DE SUELOS POR OXIDACIÓN DE LODOS PIRÍTICOS. Edafología. 2000 Sep;7(3):159– 168.
[12] Hooda PS, Alloway BJ. Cadmium and lead sorption behaviour of selected English and Indian soils. Geoderma. 1998 Jun;84(1–3):121–134.
[13] Cala V, de La Flor M, Mencía R. Influencia de las características fisicoquímicas y mineralógicas en la distribución de metales pesados en suelos de cultivo. Boletín de la Sociedad Espa nola de la Ciencia del Suelo. 1997;1(2):205–213.
[14] Ma LQ, Tan F, Harris WG. Concentrations and Distributions of Eleven Metals in Florida Soils. J Environ Qual. 1997 May;26(3):769–775.
[15] Holmgren GGS, Meyer MW, Chaney RL, Daniels RB. Cadmium, Lead, Zinc, Copper, and Nickel in Agricultural Soils of the United States of America. J Environ Qual. 1993 Apr;22(2):335–348.
[16] de Azevedo F. Toxicologia do Mercúrio. Rima. 2003.
[17] Sanità di Toppi L, Gabbrielli R. Response to cadmium in higher plants. Environ Exp Bot. 1999 Apr;41(2):105–130.
[18] Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K. Physiological responses of Lemna trisulca L. (duckweed) to cadmium and copper bioaccumulation. Plant Science. 2001 Oct;161(5):881–889.
[19] Clemens S. Evolution and function of phytochelatin synthases. J Plant Physiol. 2006 Feb;163(3):319–332.
[20] Clemens S, Palmgren MG, Krämer U. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 2002 Jul;7(7):309–315.
[21] Hart JJ, Norvell WA, Welch RM, Sullivan LA, Kochian L v. Characterization of Zinc Uptake, Binding, and Translocation in Intact Seedlings of Bread and Durum Wheat Cultivars. Plant Physiol. 1998 Sep 1;118(1):219–226.
[22] Cataldo DA, Garland TR, Wildung RE. Cadmium Uptake Kinetics in Intact Soybean Plants. Plant Physiol. 1983 Nov 1;73(3):844–848.
[23] Mullins GL, Sommers LE. Cadmium and zinc influx characteristics by intact corn (Zea mays L.) seedlings. Plant Soil. 1986 Jun;96(2):153–164.
[24] Homma Y, Hirata H. Kinetics of cadmium and zinc absorption by rice seedling roots. Soil Sci Plant Nutr. 1984 Dec;30(4):527–532.
[25] Watanabe K. Microorganisms relevant to bioremediation. Curr Opin Biotechnol. 2001 Jun;12(3):237–241.
[26] Gadd GM. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology (N Y). 2010 Mar 1;156(3):609–643.
[27] Kirchman DL. Processes in Microbial Ecology. Vol. 1. Oxford University Press; 2018.
[28] Gadd GM. Microbial influence on metal mobility and application for bioremediation. Geoderma. 2004 Oct;122(2–4):109–119.
[29] Valls M, de Lorenzo V. Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev. 2002 Nov;26(4):327–338.
[30] Gadd GM. Interactions of Fungi with Toxic Metals. In: The Genus Aspergillus. Boston, MA: Springer US; 1994. p. 361–374.
[31] Tabak HH, Lens P, van Hullebusch ED, Dejonghe W. Developments in Bioremediation of Soils and Sediments Polluted with Metals and Radionuclides – 1. Microbial Processes and Mechanisms Affecting Bioremediation of Metal Contamination and Influencing Metal Toxicity and Transport. Rev Environ Sci Biotechnol. 2005 Aug;4(3):115–156.
[32] Roberto N, Yong Y, Borges R, Olguín E. Fitorremediación: fundamentos y aplicaciones. Revista Ciencia. 2004;69–83.
[33] Leung A, Foster S. Encyclopedia of common natural ingredients used in food, drugs, and cosmetics. 2nd ed. New York; 1996. 649.
[34] Kalvatchev Z, Garzaro D, Cedezo F. Theobroma cacao L.: Un nuevo enfoque para nutrición y salud. Revista agroalimentaria. 1998;4(6):23–25.
[35] Pérez P, Azcona M. Los efectos del cadmio en la salud. Revista de Especialidades Médico-Quirúrgicas. 2012 Sep;17(3):199–205.
[36] Antoine JMR, Fung LAH, Grant CN. Assessment of the potential health risks associated with the aluminium, arsenic, cadmium and lead content in selected fruits and vegetables grown in Jamaica. Toxicol Rep. 2017;4:181–187.
[37] Gunnar N. ENCICLOPEDIA DE SALUD Y SEGURIDAD EN EL TRABAJO. In: METALES: PROPIEDADES QUIMICAS Y TOXICIDAD. 10th ed. 2013.
[38] Reyes Y, Vergara I, Torres O, Díaz M, González E. Contaminación por metales pesados Implicaciones en salud, ambiente y seguridad alimentaria. Ingeniería Investigación y Desarrollo: I2+D. 2016 Dec;16(2):66–77.
[39] Engbersen N, Gramlich A, Lopez M, Schwarz G, Hattendorf B, Gutierrez O, et al. Cadmium accumulation and allocation in different cacao cultivars. Science of The Total Environment. 2019 Aug;678:660–670.
[40] Maddela NR, Kakarla D, García LC, Chakraborty S, Venkateswarlu K, Megharaj M. Cocoa-laden cadmium threatens human health and cacao economy: A critical view. Science of The Total Environment. 2020 Jun;720:137645.
[41] Casteblanco JA. Técnicas de remediación de metales pesados con potencial aplicación en el cultivo de cacao. La Granja. 2018 Jan 11;27(1):21–35.
[42] Unión Europea-UE. Reglamento (UE) No 488/2014 de la comisión de 12 de mayo de 2014 que modifica el Reglamento (CE) no 1881/2006 por lo que respecta al contenido máximo de cadmio en los productos alimenticios. 2014.
[43] Jiménez C. Global legal status of cadmium in cacao (Theobroma cacao): a fantasy or a reality. Producción + Limpia. 2015 Jun;10(1):89–104.
[44] Pastor S. Niveles de cadmio en el chocolate: NM y ECA, sí; OTC, no. In: 2017 International Symposium on Cocoa Research (ISCR). Lima; 2017.
[45] Argüello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D. Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: A nationwide survey in Ecuador. Science of The Total Environment. 2019 Feb;649:120–127.
[46] Barraza F, Schreck E, Lévêque T, Uzu G, López F, Ruales J, et al. Cadmium bioaccumulation and gastric bioaccessibility in cacao: A field study in areas impacted by oil activities in Ecuador. Environmental Pollution. 2017 Oct;229:950–963.
[47] Hussain A, Ali S, Rizwan M, Zia-ur-Rehman M, Yasmeen T, Hayat MT, et al. Morphological and physiological responses of plants to cadmium toxicity. In: Cadmium toxicity and tolerance in plants. Elsevier; 2019. p. 47–72.
[48] Chang YS, Chang YJ, Lin CT, Lee MC, Wu CW, Lai YH. Nitrogen fertilization promotes the phytoremediation of cadmium in Pentas lanceolata. Int Biodeterior Biodegradation. 2013 Nov;85:709–714.
[49] Huang B, Xin J, Dai H, Liu A, Zhou W, Yi Y, et al. Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environmental Science and Pollution Research. 2015 Jan 15;22(2):1151–1159.
[50] Wang P, Deng X, Huang Y, Fang X, Zhang J, Wan H, et al. Root morphological responses of five soybean [Glycine max (L.) Merr] cultivars to cadmium stress at young seedlings. Environmental Science and Pollution Research. 2016 Jan 24;23(2):1860– 1872.
[51] Monteiro MS, Santos C, Soares AMVM, Mann RM. Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf. 2009 Mar;72(3):811–818.
[52] Tantalean Pedraza E, Huauya Rojas MÁ. Distribución del contenido de cadmio en los diferentes órganos del cacao CCN-51 en suelo aluvial y residual en las localidades de Jacintillo y Ramal de Aspuzana. Revista de Investigación de Agroproducción Sustentable. 2017 Aug 1;1(2):69.
[53] Hirzel J, Retamal-Salgado J, Walter I, Matus I. Cadmium accumulation and distribution in plants of three durum wheat cultivars under different agricultural environments in Chile. J Soil Water Conserv. 2017 Dec 24;72(1):77–88.
[54] Argüello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D. Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: A nationwide survey in Ecuador. Science of The Total Environment. 2019 Feb;649:120–127.
[55] Florida Rofner N, Claudio Melchor Sl, Gómez Bernal R. El pH Y La Absorción De Cadmio En Almendras De Cacao Orgánico (Theobroma Cacao L.) En Leoncio Prado, Huánuco, Peru. Folia Amazónica. 2019 Jan 28;27(1):1–8.
[56] Arévalo-Gardini E, Obando-Cerpa ME, Zú niga-Cernades LB, Arévalo-Hernández CO, Baligar V, He Z. METALES PESADOS EN SUELOS DE PLANTACIONES DE CACAO (Theobroma cacao L.) EN TRES REGIONES DEL PERÚ. Ecología Aplicada. 2016 Dec 22;15(2):81.