Micorrizas arbusculares y Trichoderma spp. en la mitigación del cadmio en cacao
Producción del ambiente
Autores/as
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Angela Leonor Palacios Cedeño
Universidad Técnica de Manabí
https://orcid.org/0009-0008-9560-286X
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Edisson Wilfrido Cuenca Cuenca
Universidad Técnica de Manabí
https://orcid.org/0000-0002-5654-8599
DOI:
https://doi.org/10.33936/la_tecnica.v16i2.8554Palabras clave:
biorremediación, inocuidad alimentaria, rizósfera, metales pesados, agroecosistemas tropicales.Resumen
La acumulación de cadmio (Cd) en las almendras de cacao tiene un impacto significativo en la inocuidad, sostenibilidad y competitividad de la cadena cacaotera en Ecuador, especialmente en mercados que imponen límites para el chocolate y sus derivados. Esta revisión crítica y narrativa se centró en la evidencia sobre los hongos micorrízicos arbusculares (HMA) y Trichoderma spp. como herramientas biológicas para modificar la biodisponibilidad, absorción y transferencia de Cd en Theobroma cacao L. La búsqueda se actualizó hasta septiembre de 2026, y el análisis se basó en 47 estudios primarios y 17 referencias adicionales. La evidencia fue más sólida para los HMA, aunque fue importante distinguir entre la reducción de la concentración de Cd, la menor translocación y la dilución por crecimiento. En cuanto a Trichoderma spp., la información sigue siendo escasa, pero ya incluye ensayos controlados en plantas de cacao que muestran respuestas que dependen de la cepa; sin embargo, aún se necesitan validaciones en campo y en las almendras. La aplicación agronómica debe integrar un diagnóstico del suelo, el uso de materiales de baja acumulación, un manejo adecuado de la fertilidad, evaluaciones en múltiples sitios y cosechas, así como la verificación de Cd en almendras tanto fermentadas como secas, sin olvidar considerar los costos, la calidad del grano y la persistencia del efecto microbiano.
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Arévalo-Gardini, E., Arévalo-Hernández, C. O., Baligar, V. C. and He, Z. L. (2017). Heavy metal accumulation in leaves and beans of cacao (Theobroma cacao L.) in major cacao growing regions in Peru. Science of the Total Environment, 605-606, 792-800. https://doi.org/10.1016/j.scitotenv.2017.06.122
Argüello, D., Chavez, E., Gutierrez, E., Pittomvils, M., Dekeyrel, J., Blommaert, H. and Smolders, E. (2023). Soil amendments to reduce cadmium in cacao (Theobroma cacao L.): A comprehensive field study in Ecuador. Chemosphere, 324, 138318. https://doi.org/10.1016/j.chemosphere.2023.138318
Argüello, D., Chavez, E., Lauryssen, F., Vanderschueren, R., Smolders, E. and Montalvo, D. (2019). Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: A nationwide survey in Ecuador. Science of the Total Environment, 649, 120-127. https://doi.org/10.1016/j.scitotenv.2018.08.292
Barraza, F., Moore, R. E. T., Rehkämper, M., Schreck, E., Lefeuvre, G., Kreissig, K., Coles, B. J. and Maurice, L. (2019). Cadmium isotope fractionation in the soil–cacao systems of Ecuador: A pilot field study. RSC Advances, 9, 34011-34022. https://doi.org/10.1039/C9RA05516A
Barraza, F., Schreck, E., Lévêque, T., Uzu, G., López, F., Ruales, J., Prunier, J., Marquet, A. y Maurice, L. (2017). Cadmium bioaccumulation and gastric bioaccessibility in cacao: A field study in areas impacted by oil activities in Ecuador. Environmental Pollution, 229, 950-963. https://doi.org/10.1016/j.envpol.2017.07.080
Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ashraf, M., Ahmed, N. and Zhang, L. (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Frontiers in Plant Science, 10, 1068. https://doi.org/10.3389/fpls.2019.01068
Bravo, D., Leon-Moreno, C., Martínez, C. A., Varón-Ramírez, V. M., Araujo-Carrillo, G. A., Vargas, R., Quiroga-Mateus, R., Zamora, A. and Rodríguez, E. A. G. (2021). The first national survey of cadmium in cacao farm soil in Colombia. Agronomy, 11(4), 761. https://doi.org/10.3390/agronomy11040761
Bravo, D., Quiroga-Mateus, R., López-Casallas, M., Torres, S., Contreras, R., Otero, A. C. M., Araujo-Carrillo, G. A. and González-Orozco, C. E. (2024). Assessing the cadmium content of cacao crops in Arauca, Colombia. Environmental Monitoring and Assessment, 196, 387. https://doi.org/10.1007/s10661-024-12539-9
Carrillo, K., Martínez, M., Ramírez, L., Argüello, D. and Chavez, E. (2023). Cadmium (Cd) distribution and soil-plant relationship in cacao farms in Costa Rica. Environmental Monitoring and Assessment, 195, 1209. https://doi.org/10.1007/s10661-023-11817-2
Cayotopa-Torres, J., Arévalo-López, L., Pichis-García, R., Olivera-Cayotopa, D., Rimachi-Valle, M. y Márquez-Dávila, K. (2021). Nuevos agentes de biorremediación de cadmio: Especies de Trichoderma nativas de la rizósfera de árboles de cacao. Scientia Agropecuaria, 12(2), 155-160. https://doi.org/10.17268/sci.agropecu.2021.017
Chavez, E., He, Z. L., Stoffella, P. J., Mylavarapu, R. S., Li, Y. C., Moyano, B. and Baligar, V. C. (2015). Concentration of cadmium in cacao beans and its relationship with soil cadmium in southern Ecuador. Science of the Total Environment, 533, 205-214. https://doi.org/10.1016/j.scitotenv.2015.06.106
Clemens, S. and Ma, J. F. (2016). Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review of Plant Biology, 67, 489-512. https://doi.org/10.1146/annurev-arplant-043015-112301
Codex Alimentarius Commission. (2022). Code of practice for the prevention and reduction of cadmium contamination in cocoa beans (CXC 81-2022). FAO/WHO. https://www.fao.org/fao-who-codexalimentarius/codex-texts/codes-of-practice/
Cueva-Paredes, D. L., Corazon-Guivin, M. A. y Pezo-Torres, M. N. (2026). Interacción micorrízica arbuscular como estrategia para mitigar cadmio en cacao bajo diferentes agroecosistemas en San Martín. Revista Agrotecnológica Amazónica, 6(2), e1284. https://doi.org/10.51252/raa.v6i2.1284
Del Aguila-Torres, C. E., Pezo-Torres, M. N., Vega-Herrera, S. S., Verde-Girbau, C., Meseth, E., Corazon-Guivin, M. A. and Paz-Urrelo, J. L. (2026). Arbuscular mycorrhizal fungal community shifts driven by heavy metals in cocoa agroecosystems at different crop age. Mycobiology, 54(3), 424-439. https://doi.org/10.1080/12298093.2026.2688575
De Almeida, N. M., de Almeida, A. A. F., de Almeida Santos, N., Mora-Ocampo, I. Y. and Pirovani, C. P. (2023). Leaf proteomic profiles in cacao scion–rootstock combinations tolerant and intolerant to cadmium toxicity. Plant Physiology and Biochemistry, 203, 107987. https://doi.org/10.1016/j.plaphy.2023.107987
De Almeida, N. M., de Almeida, A. A. F., Santos, N. A., do Nascimento, J. L., de Carvalho Neto, C. H., Pirovani, C. P., Ahnert, D. and Baligar, V. C. (2022). Scion–rootstock interaction and tolerance to cadmium toxicity in juvenile Theobroma cacao plants. Scientia Horticulturae, 300, 111086. https://doi.org/10.1016/j.scienta.2022.111086
Dos Santos, M. L. S., de Almeida, A. A. F., da Silva, N. M., Oliveira, B. R. M., Silva, J. V. S., Junior, J. O. S., Ahnert, D. and Baligar, V. C. (2020). Mitigation of cadmium toxicity by zinc in juvenile cacao: Physiological, biochemical, molecular and micromorphological responses. Environmental and Experimental Botany, 179, 104201. https://doi.org/10.1016/j.envexpbot.2020.104201
Espinoza-Echeverría, E. E., Canchingre-Bone, M. E., Andrade-Benalcázar, D. L. and Serrano-Guerrero, S. F. (2023). Presence of cadmium in cocoa (Theobroma cacao L.) soils in the province of Esmeraldas, Ecuador. Sapienza: International Journal of Interdisciplinary Studies, 4(2), e23024. https://doi.org/10.51798/sijis.v4i2.682
Fernández-Paz, J., Cortés, A. J., Hernández-Varela, C. A., Mejía-de-Tafur, M. S., Rodriguez-Medina, C. and Baligar, V. C. (2021). Rootstock-mediated genetic variance in cadmium uptake by juvenile cacao (Theobroma cacao L.) genotypes, and its effect on growth and physiology. Frontiers in Plant Science, 12, 777842. https://doi.org/10.3389/fpls.2021.777842
Ferrol, N., Tamayo, E. and Vargas, P. (2016). The heavy metal paradox in arbuscular mycorrhizas: From mechanisms to biotechnological applications. Journal of Experimental Botany, 67(22), 6253–6265. https://doi.org/10.1093/jxb/erw403
García Porras, G. A., Santos, J. A. dos, Carvalho, M. R. de, Pinzón-Sandoval, E. H., Pereira, A. A. S. and Guilherme, L. R. G. (2025). Addressing cadmium in cacao farmland: A path to safer, sustainable chocolate. Agriculture, 15(4), 433. https://doi.org/10.3390/agriculture15040433
Gil, J. P., López-Zuleta, S., Quiroga-Mateus, R. Y., Benavides-Erazo, J., Chaali, N. and Bravo, D. (2022). Cadmium distribution in soils, soil litter and cacao beans: A case study from Colombia. International Journal of Environmental Science and Technology, 19, 2455-2476. https://doi.org/10.1007/s13762-021-03299-x
Gramlich, A., Tandy, S., Andres, C., Chincheros Paniagua, J., Armengot, L., Schneider, M. and Schulin, R. (2017). Cadmium uptake by cocoa trees in agroforestry and monoculture systems under conventional and organic management. Science of the Total Environment, 580, 677-686. https://doi.org/10.1016/j.scitotenv.2016.12.014
Gramlich, A., Tandy, S., Gauggel, C., López, M., Perla, D., Gonzalez, V. and Schulin, R. (2018). Soil cadmium uptake by cocoa in Honduras. Science of the Total Environment, 612, 370-378. https://doi.org/10.1016/j.scitotenv.2017.08.145
Guarín, D., Martín-López, J. M., Libohova, Z., Benavides-Bolaños, J., Maximova, S. N., Guiltinan, M. J., Spargo, J., da Silva, M., Fernandez, A. and Drohan, P. (2024). Accumulation of cadmium in soils, litter and leaves in cacao farms in the North Sierra Nevada de Santa Marta, Colombia. Geoderma Regional, 36, e00762. https://doi.org/10.1016/j.geodrs.2024.e00762
Haider, F. U., Liqun, C., Coulter, J. A., Cheema, S. A., Wu, J., Zhang, R., Wenjun, M. and Farooq, M. (2021). Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicology and Environmental Safety, 211, 111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Hermosa, R., Viterbo, A., Chet, I. and Monte, E. (2012). Plant-beneficial effects of Trichoderma and of its genes. Microbiology, 158(1), 17-25. https://doi.org/10.1099/mic.0.052274-0
Joya-Barrero, V., Huguet, C. and Pearse, J. (2023). Natural and anthropogenic sources of cadmium in cacao crop soils of Santander, Colombia. Soil Systems, 7(1), 12. https://doi.org/10.3390/soilsystems7010012
Kubier, A., Wilkin, R. T. and Pichler, T. (2019). Cadmium in soils and groundwater: A review. Applied Geochemistry, 108, 104388. https://doi.org/10.1016/j.apgeochem.2019.104388
Lafont-Quiñonez, O., Barrera-Violeth, J. L., Jiménez-Ramírez, A. M. and Royet-Barroso, J. J. (2025). Physiological evaluation of cacao plants (Theobroma cacao L.) inoculated with arbuscular mycorrhizal fungi in soils contaminated by cadmium. Revista Colombiana de Ciencias Hortícolas, 19(2), 1-11. https://doi.org/10.19053/uptc.24223719.18575
Landero-Valenzuela, N., Hernández-Nataren, E., Chávez-Cerón, L., Granados-Echegoyen, C. A., Alonso-Hernández, N., Mayek-Pérez, N., Lara-Viveros, F. M., Ponce-Lira, B. and Calderón-Cortés, N. (2024). Influence of Trichoderma species on the reduction of heavy metal levels in bean plants irrigated with wastewater: A case study from the Mezquital Valley, Hidalgo, Mexico. Renewable Agriculture and Food Systems, 39, e28. https://doi.org/10.1017/S1742170524000231
Letort, F., Chavez, E., Blommaert, H., Campillo, S., Sentenac, S., Tisserand, D., Martin, R., Denti, S. and Sarret, G. (2025). Calcium oxalate crystals in cacao trees and their interactions with cadmium. Plant Physiology and Biochemistry, 220, 109499. https://doi.org/10.1016/j.plaphy.2025.109499
López, J. E., Builes, S., Gil, A., Restrepo, T. I., Aristizábal, A. and Arroyave, C. (2023). Effects of different liming materials on the uptake of cadmium and mineral nutrients in cacao plants. ACS Agricultural Science & Technology, 3, 1139–1147. https://doi.org/10.1021/acsagscitech.3c00296
Luis-Alaya, B., Toro, M., Calsina, R., Ogata-Gutiérrez, K., Gil-Polo, A., Ormeño-Orrillo, E. and Zúñiga-Dávila, D. (2023). Evaluation of the presence of arbuscular mycorrhizae and cadmium content in the plants and soils of cocoa plantations in San Martín, Peru. Diversity, 15(2), 246. https://doi.org/10.3390/d15020246
Malca-Cerna, R. Y., Apolinario, C.-L. A., Israel, C.-C. J., Marielita, A.-I. and Marjory, C.-V. L. (2025). Native strains T. longibrachiatum UCF17-M4 and Trichoderma sp. UCPF2 reduce Cd uptake in cacao CCN51 under controlled conditions. Microbiology Research, 16(6), 130. https://doi.org/10.3390/microbiolres16060130
Mohsenzadeh, F. and Shahrokhi, F. (2014). Biological removing of cadmium from contaminated media by fungal biomass of Trichoderma species. Journal of Environmental Health Science and Engineering, 12, 102. https://doi.org/10.1186/2052-336X-12-102
Moore, R. E. T., Ullah, I., Dunwell, J. M. and Rehkämper, M. (2024). Stable isotope analyses reveal impact of Fe and Zn on Cd uptake and translocation by Theobroma cacao. Plants, 13(4), 551. https://doi.org/10.3390/plants13040551
Nongmaithem, N., Roy, A. and Bhattacharya, P. M. (2016). Screening of Trichoderma isolates for their potential of biosorption of nickel and cadmium. Brazilian Journal of Microbiology, 47(2), 305–313. https://doi.org/10.1016/j.bjm.2016.01.008
Oliva, M., Rubio, K., Epquin, M., Marlo, G. and Leiva, S. (2020). Cadmium uptake in native cacao trees in agricultural lands of Bagua, Peru. Agronomy, 10(10), 1551. https://doi.org/10.3390/agronomy10101551
Oliveira, B. R. M., de Almeida, A. A. F., Pirovani, C. P., Barroso, J. P., Carlos, C. H., Santos, N. A., Ahnert, D., Baligar, V. C. and Mangabeira, P. A. O. (2020). Mitigation of Cd toxicity by Mn in young plants of cacao, evaluated by the proteomic profiles of leaves and roots. Ecotoxicology, 29, 340–358. https://doi.org/10.1007/s10646-020-02178-4
Oliveira, B. R. M., de Almeida, A. A. F., Santos, N. D. A. and Pirovani, C. P. (2022). Tolerance strategies and factors that influence the cadmium uptake by cacao tree. Scientia Horticulturae, 293, 110733. https://doi.org/10.1016/j.scienta.2021.110733
Ortiz-Álvarez, A., Magnitskiy, S., Silva-Arero, E. A., Rodríguez-Medina, C., Argout, X. and Castaño-Marín, Á. M. (2023). Cadmium accumulation in cacao plants (Theobroma cacao L.) under drought stress. Agronomy, 13(10), 2490. https://doi.org/10.3390/agronomy13102490
Oshiquiri, L. H., dos Santos, K. R. A., Ferreira Junior, S. A., Steindorff, A. S., Barbosa Filho, J. R., Mota, T. M., Ulhoa, C. J. and Georg, R. C. (2020). Trichoderma harzianum transcriptome in response to cadmium exposure. Fungal Genetics and Biology, 134, 103281. https://doi.org/10.1016/j.fgb.2019.103281
Pérez-Moncada, U. A., Ramírez-Gómez, M. M., Serralde-Ordóñez, D. P., Peñaranda-Rolón, A. M., Wilches-Ortiz, W. A., Ramírez, L. y Rengifo-Estrada, G. A. (2019). Hongos formadores de micorrizas arbusculares como estrategia para reducir la absorción de cadmio en plantas de cacao (Theobroma cacao). Terra Latinoamericana, 37(2), 121-130. https://doi.org/10.28940/terra.v37i2.479
Ramtahal, G., Umaharan, P., Hanuman, A., Davis, C. and Ali, L. (2019). The effectiveness of soil amendments, biochar and lime, in mitigating cadmium bioaccumulation in Theobroma cacao L. Science of the Total Environment, 693, 133563. https://doi.org/10.1016/j.scitotenv.2019.07.369
Ramtahal, G., Yen, I. C., Bekele, I., Bekele, F., Wilson, L., Maharaj, K. and Harrynanan, L. (2016). Relationships between cadmium in tissues of cacao trees and soils in plantations of Trinidad and Tobago. Food and Nutrition Sciences, 7, 37–43. https://doi.org/10.4236/fns.2016.71005
Sandoval-Pineda, J. F., Pérez, U. A., Rodriguez, A. y Torres-Rojas, E. (2020). Alta presencia de cadmio resulta en baja diversidad de hongos formadores de micorrizas arbusculares asociados a cacao (Theobroma cacao L.). Acta Biológica Colombiana, 25(3), 333-344. https://doi.org/10.15446/abc.v25n3.78746
Shoresh, M., Harman, G. E. and Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21-43. https://doi.org/10.1146/annurev-phyto-073009-114450
Smolders, E. and Mertens, J. (2013). Cadmium. En B. J. Alloway (Ed.), Heavy metals in soils: Trace metals and metalloids in soils and their bioavailability (3.ª ed., pp. 283-311). Springer. https://doi.org/10.1007/978-94-007-4470-7_10
Thomas, E., Atkinson, R., Zavaleta, D., Rodriguez, C., Lastra, S., Yovera, F., Arango, K., Pezo, A., Aguilar, J., Tames, M., Ramos, A., Cruz, W., Cosme, R., Espinoza, E., Chavez, C. R. and Ladd, B. (2023). The distribution of cadmium in soil and cacao beans in Peru. Science of the Total Environment, 881, 163372. https://doi.org/10.1016/j.scitotenv.2023.163372
Vallejos-Torres, G., Torres, S. C., Gaona-Jimenez, N., Saavedra, J., Tuesta, J. C., Tuesta, O. A., Becerra, A. G., Marín, C. and Alguacil, M. M. (2022). The combined effect of arbuscular mycorrhizal fungi and compost improves growth and soil parameters and decreases cadmium absorption in cacao (Theobroma cacao L.) plants. Journal of Soil Science and Plant Nutrition, 22(4), 5174-5182. https://doi.org/10.1007/s42729-022-00992-9
Vallejos-Torres, G., Gaona-Jimenez, N., Alva Arevalo, A., Paredes, C., Lozano, A., Saavedra-Ramírez, J., Arévalo, L. A., Reátegui, K., Mendoza-Caballero, W. and Marín, C. (2023). Cadmium uptake and mycorrhization by cacao clones in agroforestry and monoculture systems of Peruvian Amazon. Bioagro, 35(3), 237-246. https://doi.org/10.51372/bioagro353.7
Vallejos-Torres, G., García-Vallejos, N., Gaona-Jimenez, N., Saavedra-Ramírez, J., Tuesta-Hidalgo, J. C., Tuesta-Hidalgo, O. A., Valdez-Andía, M. J., Ordoñez-Ruiz, K. M. and Baselly-Villanueva, J. R. (2026). Influence of cadmium and arbuscular mycorrhizae on growth and chlorophyll content in Theobroma cacao and Theobroma grandiflorum plants. Advances in Agriculture, 6852295. https://doi.org/10.1155/AIA/6852295
Vanderschueren, R., Argüello, D., Blommaert, H., Montalvo, D., Barraza, F., Maurice, L., Schreck, E., Schulin, R., Lewis, C., Vazquez, J. L., Umaharan, P., Chavez, E., Sarret, G. and Smolders, E. (2021). Mitigating the level of cadmium in cacao products: Reviewing the transfer of cadmium from soil to chocolate bar. Science of the Total Environment, 781, 146779. https://doi.org/10.1016/j.scitotenv.2021.146779
Vanderschueren, R., Wantiez, L., Blommaert, H., Flores, J., Chavez, E. and Smolders, E. (2023). Revealing the pathways of cadmium uptake and translocation in cacao trees (Theobroma cacao L.): A 108Cd pulse-chase experiment. Science of the Total Environment, 869, 161816. https://doi.org/10.1016/j.scitotenv.2023.161816
Vega-Jara, L., Palacin Agüero, J., Farfán Tucto, S., Vangeli, S. and Márquez-Dávila, K. (2025). Mitigation of cadmium accumulation in cocoa beans using arbuscular mycorrhizal fungi, biochar and Callisia repens. Folia Amazonica, 34(2), e34800. https://doi.org/10.24841/fa.v34i2.800
Xin, J. (2024). Enhancing soil health to minimize cadmium accumulation in agro-products: The role of microorganisms, organic matter, and nutrients. Environmental Pollution, 348, 123890. https://doi.org/10.1016/j.envpol.2024.123890
Yaghoubian, Y., Siadat, S. A., Moradi Telavat, M. R., Pirdashti, H. and Yaghoubian, I. (2019). Bio-removal of cadmium from aqueous solutions by filamentous fungi: Trichoderma spp. and Piriformospora indica. Environmental Science and Pollution Research, 26, 7863-7872. https://doi.org/10.1007/s11356-019-04255-6
Zhu, Y. X., Zhuang, Y., Sun, X. H. and Du, S. T. (2023). Interactions between cadmium and nutrients and their implications for safe crop production in Cd-contaminated soils. Critical Reviews in Environmental Science and Technology, 53, 2071-2091. https://doi.org/10.1080/10643389.2023.2210985
Zug, K. L. M., Huamaní Yupanqui, H. A., Meyberg, F., Cierjacks, J. S. and Cierjacks, A. (2019). Cadmium accumulation in Peruvian cacao (Theobroma cacao L.) and opportunities for mitigation. Water, Air, & Soil Pollution, 230, 72. https://doi.org/10.1007/s11270-019-4109-x
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