In vitro effect of cocoa leachates on growth and development of Moniliophthora roreri ([Cif.] H.C. Evans et al.) isolated from Theobroma cacao (L.)

Evaluación in vitro de lixiviados de cacao sobre el crecimiento y desarrollo de Moniliophthora roreri ([Cif.] H.C. Evans et al.) aislado de Theobroma cacao (L.)

Main Article Content

Sandra Victoria Gómez-Gutierrez
Camilo Rubén Beltrán-Acosta
Sandra Gómez-Caro

Abstract

The cocoa crop is part of the peasant’s economic activity and agroforestry systems in many regions of Colombia and the world. Its yields are diminished by phytosanitary problems, being the frosty pod rot caused by the fungus Moniliophthora roreri, the most limiting disease with decreases in production of over 90%. In this study, samples of cocoa leachates from commercial producing farms were characterized and the antifungal activity of sterilized, non-sterilized, and filtered cocoa leachates against M. roreri was evaluated under in vitro conditions, at concentrations of 1, 2, 5, 10, and 15%. Monosporic isolates of the pathogen were obtained from diseased fruits collected from cocoa-producing farms in the municipality of Yacopi in Cundinamarca, Colombia. The effect of leachates on M. roreri conidial germination, mycelial growth, and inoculum production was evaluated. It was found that non-sterilized cocoa leachates at all concentrations caused 100% reduction on the three variables evaluated, while sterilized leachates generated the same effect at concentrations of 10 and 15%. Filtered leachates showed no inhibitory effect on the radial growth of the pathogen, but they caused a reduction of conidial germination of 89.9, 90.5 and 95.9% at concentrations of 5, 10, and 15%. The presence of malic, citric, and ascorbic acids, compounds such as NH4, PO4, and NO3, and elements such as Ca, K, Na, Mg, and Cl in the evaluated leachates was identified using high-efficiency liquid chromatography and physicochemical analysis. This research showed the potential of cocoa leachates, even at low concentrations, for the control of M. roreri, which can be attributed to the action of specific compounds such as those found in chromatographic tests.

Keywords:

Downloads

Download data is not yet available.

Article Details

References (SEE)

Aguilera Rodríguez, I., R.M. Pérez Silva, and A. Marañón Reyes. 2010. Determinación de sulfato por el método turbidimétrico en aguas y aguas residuales. Validación del método. Rev. Cuba. Quim. 22(3), 39-44.

Álvarez, E., J. Cortés, and G. Ceballos. 2010. Alternativas para el manejo de la Sigatoka negra en plátano Dominico Hartón (AAB) mediante el uso de lixiviados y productos biológicos. MusaLAC 1(2), 3-5.

Álvarez, E., C. Grajales, J. Villegas, and J. Loke. 2001. CIAT informe anual. Control del mildeo polvoso (Sphaerotheca panosa var. rosae) en rosa, usando un lixiviado de compost del raquis de plátano (Musa AAB). CIAT, Palmira, Colombia.

Álvarez, E., A. Pantoja, L. Gañán, and G. Ceballos. 2015. Current status of Moko disease and black sigatoka in Latin America and the Caribbean, and options for managing them. Publication 404. CIAT, Cali, Colombia.

Arana-Sánchez, A., L.E. Segura-García, M. Kirchmayr, I. Orozco-Ávila, E. Lugo-Cervantes, and A. Gschaedler-Mathis. 2015. Identification of predominant yeasts associated with artisan Mexican cocoa fermentations using culture-dependent and culture-independent approaches. World J. Microbiol. Biotechnol. 31, 359-369. Doi: https://doi.org/10.1007/s11274-014-1788-8

Arenas, A., D. López, E. Álvarez, G. Llano, and J. Loke. 2004. Efecto de prácticas ecológicas sobre la población de Ralstonia solanacearum Smith, causante de Moko de plátano. Fitopatol. Colomb. 28(2), 76-80.

Arcos-Méndez, M.C., L. Martínez-Bolaños, G. Ortíz-Gil, M. Martínez-Bolaños, and C.H. Avendaño-Arrazate. 2019. Efecto in vitro de extractos vegetales contra la moniliasis (Moniliophthora roreri) del cacao (Theobroma cacao L.). Agric. Trop. 5(1), 19-24.

Ardhana, M.M. and G.H. Fleet. 2003. The microbial ecology of cocoa bean fermentations in Indonesia. Int. J. Food Microbiol. 86(1-2), 87-99. Doi: https://doi.org/10.1016/S0168-1605(03)00081-3

Barrera Necha, L.L. and L.J. García Barrera. 2008. Actividad antifúngica de aceites esenciales y sus compuestos sobre el crecimiento de Fusarium sp. aislado de papaya (Carica papaya). Rev. UDO Agrícola 8(1), 33-41.

Bailey, B.A., H.C. Evans, W. Phillips-Mora, S.S. Ali, and L.W. Meinhardt. 2018. Moniliophthora roreri, causal agent of cacao frosty pod rot. Mol. Plant Pathol. 19(7), 1580-1594. Doi: https://doi.org/10.1111/mpp.12648

Bateman, R.P., E. Hidalgo, J. García, C. Arroyo, G.M. Ten Hoopen, V. Adonijah, and U. Krauss. 2005. Application of chemical and biological agents for the management of frosty pod rot (Moniliophthora roreri) in Costa Rican cocoa (Theobroma cacao). Ann. Appl. Biol. 147, 129-138. Doi: https://doi.org/10.1111/j.1744-7348.2005.00012.x

Bele, L., D. Kra Kouamé, K. Patrice Assiri, and H. Atta Diallo. 2018. Antifungal activity of banana rachis leachate on some fungi responsible for banana (Musa acuminate Colla) post-harvest diseases. Int. J. Environ. Agric. Res. 4(3), 1-6. Doi: https://doi.org/10.5281/zenodo.1213546

Boubakri, H. 2017. The role of ascorbic acid in plant–pathogen interactions. pp. 255-271. In: Anwar Hossain, M., S. Munné-Bosch, D.J. Burritt, P. Diaz-Vivancos, M. Fujita, and A. Lorence (eds.). Ascorbic acid in plant growth, development and stress tolerance. Springer, Cham, Switzerland. Doi: https://doi.org/10.1007/978-3-319-74057-7_10

Bubici, G., M. Kaushal, M.I. Prigigallo, C. Gómez-Lama, and J. Mercado-Blanco. 2019. Biological control agents against Fusarium wilt of banana. Front. Microbiol. 10, 616. Doi: https://doi.org/10.3389/fmicb.2019.00616

Camu, N., T. De Winter, K. Verbrugghe, I. Cleenwerck, P. Vandamme, J.S. Takrama, M. Vancanneyt, and L. De Vuyst. 2007. Dynamics and biodiversity of populations of lactic acid bacteria and acetic acid bacteria involved in spontaneous heap fermentation of cocoa beans in Ghana. Appl. Environ. Microbiol. 73(6), 1809-1824. Doi: https://doi.org/10.1128/AEM.02189-06

Carr, J.G., P.A. Davies, and J. Dougan. 1979. Cocoa fermentation in Ghana and Malaysia: Further microbial methods and results. University of Bristol Research Station, London.

Carrasquero D., A. and P. Castillo. 2002. Determinación conductimétrica de cloruros en extractos de saturación de suelos. Agron. Trop. 52(4), 555-563.

Carrera-Sánchez, K., L. Mosquera Paredes, and M. Leiva-Mora. 2014. Protocolo para el aislamiento de Moniliophthora roreri (Cif y Par) Evans et al. en frutos de cacao cv. ‘Nacional’ de la Amazonía ecuatoriana. Biotecnol. Vegetal 14(3), 147-150.

Ceballos, I., S. Mosquera, M. Ángulo, J.J. Mira, L.E. Argel, D. Uribe-Velez, M. Romero-Tabarez, S. Orduz-Peralta, and V. Villegas. 2012. Cultivable bacteria population associated with leaves of banana and plantain plants and their antagonistic activity against Mycosphaerella fijiensis. Microb. Ecol. 64, 641-653. Doi: https://doi.org/10.1007/s00248-012-0052-8

Chang, H.-T., Y.-H. Cheng, C.-L. Wu, S.-T. Chang, T.-T. Chang, and Y.-C. Su. 2008. Antifungal activity of essential oil and its constituents from Calocedrus macrolepis var. formosana Florin leaf against plant pathogenic fungi. Bioresour. Technol. 99, 6266-6270. Doi: https://doi.org/10.1016/j.biortech.2007.12.005

Chuah, T.S., Y.Y. Tan, and B.S. Ismail. 2010. In vitro evaluation of the antifungal activity of some essential oils on post-harvest fungal pathogens of tropical fruits. Plant Prot. Q. 25(4), 162-164.

Correa Álvarez, J., S. Castro Martínez, and J. Coy. 2014. Estado de la moniliasis del cacao causada por Moniliophthora roreri en Colombia. Acta Agron. 63(4), 388-399. Doi: https://doi.org/10.15446/acag.v63n4.42747

D’Angelo, E., J. Crutchfield, and M. Vandiviere. 2001. Rapid, sensitive, microscale determination of phosphate in water and soil. J. Environ. Qual. 30(6), 2206-2209. Doi: https://doi.org/10.2134/jeq2001.2206

Dorna, H., A. Rosińska, and D. Szopińska. 2021. The effect of acetic acid treatments on the quality of stored carrot (Daucus carota L.) seeds. Agronomy 11(6), 1176. Doi: https://doi.org/10.3390/agronomy11061176

Egan, M.J., Z.-Y. Wang, M.A. Jones, N. Smirnoff, and N.J. Talbot. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. USA 104(28), 11772-11777. Doi: https://doi.org/10.1073/pnas.0700574104

Evans, H.C., K.A. Holmes, and A.P. Reid. 2003. Phylogeny of the frosty pod rot pathogen of cocoa. Plant Pathol. 52(4), 476-485. Doi: https://doi.org/10.1046/j.1365-3059.2003.00867.x

Fedecacao. 2021. Así se comportó la producción de cacao por departamentos en el 2020. In: https://www.fedecacao.com.co/post/copy-of-design-a-stunning-blog; consulted: March, 2021.

Flood, J. and R. Murphy (eds.). 2004. Cocoa futures—A source book of some important issues confronting the cocoa industry. Commodities Press, Chinchina, Colombia.

Fox, J. and S. Weisberg. 2019. An R companion to applied regression. 3rd ed. Sage, Oaks, CA. URL: https://socialsciences.mcmaster.ca/jfox/Books/Companion/

Fromm, I. 2016. From small chocolatiers to multinationals to sustainable sourcing: a historical review of the Swiss chocolate industry. pp. 71-87. In: Squicciarini, M.P. and J. Swinnen (eds.). The economics of chocolate. Oxford University Press, Oxford, UK.

Fujiwara, A., H. Shimura, C. Masuta, S. Sano, and T. Inukai. 2013. Exogenous ascorbic acid derivatives and dehydroascorbic acid are effective antiviral agents against Turnip mosaic virus in Brassica rapa. J. Gen. Plant Pathol. 79, 198-204. Doi: https://doi.org/10.1007/s10327-013-0439-5

Garcia-Armisen, T., Z. Papalexandratou, H. Hendryckx, N. Camu, G. Vrancken, L. De Vuyst, and P. Cornelis. 2010. Diversity of the total bacterial community associated with Ghanaian and Brazilian cocoa bean fermentation samples as revealed by a 16S rRNA gene clone library. Appl. Microbiol. Biotechnol. 87, 2281-2292. Doi: https://doi.org/10.1007/s00253-010-2698-9

Huang, Y.H., R.C. Wang, C.H. Li, C.W. Zuo, Y.R. Wei, L. Zhang, and G.J. Yi. 2012. Control of Fusarium wilt in banana with Chinese leek. Eur. J. Plant Pathol. 134, 87-95. Doi: https://doi.org/10.1007/s10658-012-0024-3

ICCO, International Cocoa Organization. 2020. Production of cocoa beans. Quarterly Bulletin of Cocoa Statistics 46(4), In: https://www.icco.org/wp-content/uploads/Production-QBCS-XLVI-No-4.pdf; consulted: February, 2019.

In, Y.-W., J.-J. Kim, H.-J. Kim, and S.-W. Oh. 2013. Antimicrobial activities of acetic acid, citric acid and lactic acid against Shigella species. J. Food Saf. 33(1), 79-85. Doi: https://doi.org/10.1111/jfs.12025

Jaimes, Y.Y., C. González, J. Rojas, O.E. Cornejo, M.F. Mideros, S. Restrepo, C. Cilas, and E.L. Furtado. 2016. Geographic differentiation and population genetic structure of Moniliophthora roreri in the principal cocoa production areas in Colombia. Plant Dis. 100(8), 1548-1558. Doi: https://doi.org/10.1094/PDIS-12-15-1498-RE

Jaimes Suárez, Y. and F. Aranzazu Hernández. 2010. Manejo de las enfermedades del cacao (Theobroma cacao L.) en Colombia, con énfasis en monilia (Moniliophthora roreri). Corpoica-La Suiza, Rionegro, Colombia.

Jung, K.-H., S.K. Yoo, S.-K. Moon, and U.-S. Lee. 2007. Furfural from pine needle extract inhibits the growth of a plant pathogenic fungus, Alternaria mali. Mycobiology 35(1), 39-43.

Kamel, S.M., M.M.I. Afifi, F.S. El-shoraky, and M.M. El-Sawy. 2014. Fulvic acid: A tool for controlling powdery and downy mildews in cucumber plants. Int. J. Phytopathol. 3(2), 101-108. Doi: https://doi.org/10.33687/phytopath.003.02.0866

Kang, H.-C., Y.-H. Park, and S.-J. Go. 2003. Growth inhibition of a phytopathogenic fungus, Colletotrichum species by acetic acid. Microbiol. Res. 158(4), 321-326. Doi: https://doi.org/10.1078/0944-5013-00211

Krauss, U., E. Hidalgo, R. Bateman, V. Adonijah, C. Arroyo, J. García, J. Crozier, N.A. Brown, G.M. ten Hoopen, and K.A. Holmes. 2010. Improving the formulation and timing of application of endophytic biocontrol and chemical agents against frosty pod rot (Moniliophthora roreri) in cocoa (Theobroma cacao). Biol. Control 54(3), 230-240. Doi: https://doi.org/10.1016/j.biocontrol.2010.05.011

Li, J., P. Trivedi, and N. Wang. 2016. Field evaluation of plant defense inducers for the control of citrus Huanglongbing. Phytopathology 106(1), 37.46. Doi: https://doi.org/10.1094/PHYTO-08-15-0196-R

Lozada, B.S., L.V. Herrera, J.A. Perea, E. Stashenko, and P. Escobar. 2012. Efecto in vitro de aceites esenciales de tres especies de Lippia sobre Moniliophthora roreri (Cif. y Par.) Evans et al., agente causante de la moniliasis del cacao (Theobroma cacao L.). Acta Agron. 61(2), 102-110.

Mainer, Y. 2009. Control de la Sigatoka negra (Mycosphaerella fijiensis) del plátano con productos naturales (lixiviado y antagonistas). MSc. thesis. Institut National d’Horticulture et du Paysage, Université d’Angers, Angers, France.

Marín Marín, P. and A.E. Bustillo Parley. 2002. Pruebas microbiológicas y fisico - químicas para el control de calidad de los hongos entomopatógenos. pp. 72-89. In: Mem. Curso Internacional Teórico- Práctico sobre Entomopatógenos, Parasitoides y otros Enemigos Naturales de la Broca del Café. Cenicafé, Chinchiná, Colombia.

Mogollón Ortiz, A.M. and J. Castaño-Zapata. 2010. Evaluación in vitro de lixiviados del raquis del plátano sobre Paracercospora fijiensis (Morelet) Deighton. Agronomía 18(2), 17-23.

Morgunov, I.G., S.V. Kamzolova, E.G. Dedyukhina, T.I. Chistyakova, J.N. Lunina, A.A. Mironov, N.N. Stepanova, O.N. Shemshura, and M.B. Vanshtein. 2017. Application of organic acids for plant protection against phytopathogens. Appl. Microbiol. Biotechnol. 101, 921-932. Doi: https://doi.org/10.1007/s00253-016-8067-6

Nielsen, D.S., O.D. Teniola, L. Ban-Koffi, M. Owusu, T.S. Anderson, and W.H. Holzapfel. 2007. The microbiology of Ghanaian cocoa fermentations analyzed using culture-dependent and culture-independent methods. Int. J. Food Microbiol. 114(2), 168-186. Doi: https://doi.org/10.1016/j.ijfoodmicro.2006.09.010

Okiyama, D.C.G., S.L.B. Navarro, and C.E.C. Rodrigues. 2017. Cocoa shell and its compounds: applications in the food industry. Trends Food Sci. Technol. 63, 103-112. Doi: https://doi.org/10.1016/j.tifs.2017.03.007

Osorio Gutiérrez, L.A., J. Castaño-Zapata, and L.B. Gutiérrez Ríos. 2012. Eficacia in-vitro de lixiviados de plátano sobre Fusarium oxysporum Schlecht, causante de la pudrición de raíces de arveja (Pisum sativum Linneo). Agronomía 20(1), 17-25.

Ostovar, K. and P.G. Keeney. 1973. Isolation and characterization of microorganisms involved in the fermentation of Trinidad’s cocoa beans. J. Food Sci. 38(4), 611-617. Doi: https://doi.org/10.1111/j.1365-2621.1973.tb02826.x

Ouattara, H.G., S. Reverchon, S.L. Niamke, and W. Nasser. 2011. Molecular identification and pectate lyase production by Bacillus strains involved in cocoa fermentation. Food Microbiol. 28(1), 1-8. Doi: https://doi.org/10.1016/j.fm.2010.07.020

Özer, N., M. Mirik, and A. Citir. 2002. Effects of extracts from some medicinal plants and composts on pectolytic enzymes produced in liquid culture and on onion seeds by Aspergillus niger and Fusarium oxysporum f. sp. cepae. J. Turk. Phytopathol. 31(3), 137-154.

Özer, N. and N.D. Köycü. 2006. The ability of plant compost leachates to control black mold (Aspergillus niger) and to induce the accumulation of antifungal compounds in onion following seed treatment. BioControl 51, 229-243. Doi: https://doi.org/10.1007/s10526-005-1035-1

Pacheco-Montealegre, M.E., L.L. Dávila-Mora, L.M. Botero-Rute, A. Reyes, and A. Caro-Quintero. 2020. Fine resolution analysis of microbial communities provides insights into the variability of cocoa bean fermentation. Front. Microbiol. 11, 650. Doi: https://doi.org/10.3389/fmicb.2020.00650

Papalexandratou, Z., G. Falony, E. Romanens, J.C. Jimenez, F. Amores, H.-M. Daniel, and L. De Vuyst. 2011. Species diversity, community dynamics, and metabolite kinetics of the microbiota associated with traditional Ecuadorian spontaneous cocoa bean fermentations. Appl. Environ. Microbiol. 77(21), 7698-7714. Doi: https://doi.org/10.1128/AEM.05523-11

Papalexandratou, Z., T. Lefeber, B. Bahrim, O.S. Lee, H.M. Daniel, and L. De Vuyst. 2013. Hanseniaspora opuntiae, Saccharomyces cerevisiae, Lactobacillus fermentum, and Acetobacter pasteurianus predominate during well-performed Malaysian cocoa bean box fermentations, underlining the importance of these microbial species for a successful cocoa bean fermentation process. Food Microbiol. 35(2), 73-85. Doi: https://doi.org/10.1016/j.fm.2013.02.015

Penagos Muñetón, A., A. Parra Coronado, A.L. Leguizamon García, A.O. Herrera Arévalo, C.R. Beltran Acosta, C.S. Pinilla Dativa, C.M. Sánchez Sáenz, E. Baquero López, E. Torres Rojas, H.A. Cordoba Novoa, J. Torres Bazurto, J.A. Cáceres Zambrano, J.E. Ospina Noreña, J.A. Ladino Orjuela, J.F. Soler Arias, J.C. Barrientos Fuentes, L.A. Valderrama Flórez, L.E. Ramírez Chamorro, M.C. Henao Toro, M.F. Bejarano Hernández, P.A. Bermeo Fúquene, R. Villalobos Rebolledo, S. Gómez Caro, S.V. Gómez Gutiérrez, and S. Magnitskiy. 2019. Guía técnica para el cultivo de cacao en los municipios Nilo y Yacopí (Cundinamarca). Universidad Nacional de Colombia; Agrosavia. Bogota.

Peña Hernández, Y., G. Santacruz de León, and H. Charcas Salazar. 2012. Calidad del agua en pozos de la red de monitoreo del acuífero del valle de San Luis Potosí, México. Aqua-LAC 4(1), 49-59. Doi: https://doi.org/10.29104/phi-aqualac/2012-v4-1-06

Pereira, G.V.M., V.T. Soccol, and C.R. Soccol. 2016. Current state of research on cocoa and coffee fermentations. Curr. Opin. Food Sci. 7, 50-57. Doi: https://doi.org/10.1016/j.cofs.2015.11.001

Pérez-Vicente, L.F. 2018. Moniliophthora roreri H.C. Evans et al. and Moniliophthora perniciosa (Stahel) Aime: impact, symptoms, diagnosis, epidemiology and management. Rev. Protec. Veg. 33(1), 1-13.

Petlamul, W. and P. Prasertsan. 2012. Evaluation of strains of Metarhizium anisophilae and Beauveria bassiana against Spodoptera litura in the basis of their virulence, germination rate, conidia production, radial growth and enzyme activity. Mycobiology 40(2), 111-116. Doi: https://doi.org/10.5941/MYCO.2012.40.2.111

Phillips-Mora, W., M.C. Aime, and M.J. Wilkinson. 2007. Biodiversity and biogeography of the cacao (Theobroma cacao) pathogen Moniliophthora roreri in tropical America. Plant Pathol. 56(6), 911-922. Doi: https://doi.org/10.1111/j.1365-3059.2007.01646.x

Phillips-Mora, W., J. Castillo, U. Krauss, E. Rodríguez, and M. Wilkinson. 2005. Evaluation of cacao (Theobroma cacao) clones against seven Colombian isolates of Moniliophthora roreri from four pathogen genetic groups. Plant Pathol. 54(4), 483-490. Doi: https://doi.org/10.1111/j.1365-3059.2005.01210.x

Phillips-Mora, W., A. Coutiño, C.F. Ortiz, A.P. López, J. Hernández, and M.C. Aime. 2006a. First report of Moniliophthora roreri causing frosty pod rot (moniliasis disease) of cocoa in Mexico. Plant Pathol. 55(4), 584-584. Doi: https://doi.org/10.1111/j.1365-3059.2006.01418.x

Phillips-Mora, W., J. Cawich, W. Garnett, and M.C. Aime. 2006b. First report of frosty pod rot (moniliasis disease) caused by Moniliophthora roreri on cacao in Belize. Plant Pathol. 55(4), 584-584. Doi: https://doi.org/10.1111/j.1365-3059.2006.01378.x

Phillips-Mora, W. and M.J. Wilkinson. 2007. Frosty pod of cacao: A disease with a limited geographic range but unlimited potential for damage. Phytopath. 97(12), 1644-1647. Doi: https://doi.org/10.1094/PHYTO-97-12-1644

Pinzón Usuche, J.O., J. Rojas Ardila, F. Rojas, O.D. Ramírez, F. Moreno, and G. Antolinez Castro. 2012. Guía técnica para el cultivo del cacao. 5th ed. Fedecacao, Bogota.

Pohl, P., H. Stecka, and P. Jamroz. 2012. Fast and interference free determination of calcium and magnesium in honeys by solid phase extraction followed by flame atomic absorption spectrometry. J. Braz. Chem. Soc. 23(4), 710-717. Doi: https://doi.org/10.1590/S0103-50532012000400017

R Development Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. In: http://www.R-project.org/

Ramírez, S. 2013. Efectividad de extractos vegetales en el manejo de la Moniliasis (Moniliophthora roreri) del cacao (Theobroma cacao L.) en México. PhD thesis. Universidad Nacional de Costa Rica, Heredia, Costa Rica.

Ritz, C., F. Baty, J.C. Streibig, and D. Gerhard. 2015. Dose-response analysis using R. PLos ONE 10(12), e0146021. Doi: https://doi.org/10.1371/journal.pone.0146021

Roldán Pérez, G. and J.J. Ramírez Restrepo. 2008. Fundamentos de limnología neotropical. 2nd ed. Editorial Universidad de Antioquia; Universidad Católica de Oriente; ACCEFYN, Medellin, Colombia.

Sánchez Mora, F.D. and F.R. Garcés Fiallos. 2012. Moniliophthora roreri (Cif. y Par.) Evans et al. en el cultivo de cacao. Sci. Agropecu. 3(3), 249-258. Doi: https://doi.org/10.17268/sci.agropecu.2012.03.06

Sánchez-Mora, F., J. Zambrano Montufar, J. Vera Chang, R. Ramos Remache, F. Garcés Fiallos, and G. Vásconez Montúfar. 2014. Productividad de clones de cacao tipo nacional en una zona del bosque húmedo tropical de la provincia de Los Ríos, Ecuador. Cienc. Tecnol. 7(1), 33-41. Doi: https://doi.org/10.18779/cyt.v7i1.134

Schwan, R.F., M.C.D. Vanetti, D.O. Silva, A. Lopez, and C.A. Moraes. 1986. Characterization and distribution of aerobic, spore-forming bacteria from cacao fermentation in Bahia. J. Food Sci. 51(6), 1583-1584. Doi: https://doi.org/10.1111/j.1365-2621.1986.tb13872.x

Sikirou, R., A. Zannou, G. Gbèhounou, F. Tosso, and F.A. Komlan. 2010. Fungicide effect of banana column juice on tomato southern blight caused by Sclerotium rolfsii: Technical and economic efficiency. Afr. J. Agric. Res. 5(23), 3230-3238.

Soumahoro, S., H.G. Ouattara, M. Droux, W. Nasser, S.L. Niamke, and S. Reverchon. 2020. Acetic acid bacteria (AAB) involved in cocoa fermentation from Ivory Coast: species diversity and performance in acetic acid production. J. Food Sci. Technol. 57(5), 1904-1916. Doi: https://doi.org/10.1007/s13197-019-04226-2

Suárez Contreras, L.Y. and A.L. Rangel Riaño. 2013. Aislamiento de microorganismos para control biológico de Moniliophthora roreri. Acta Agron. 62(4), 370-378.

Tello Espinoza, P. and G. Fernández Villagómez. 2012. Evaluación de la generación de lixiviados en pacas impermeabilizadas de residuos sólidos urbanos. Experimento a gran escala. Rev. Int. Contam. Ambie. 28(Suppl. 1), 83-87.

Viesser, J.A., G.V. Melo Pereira, D.P. Carvalho Neto, G.R. Favero, J.C. Carvalho, A. Goés-Neto, H. Rogez, and C.R. Soccol. 2021. Global cocoa fermentation microbiome: revealing new taxa and microbial functions by next generation sequencing technologies. World. J. Microbiol. Biotechnol. 37, 118. Doi: https://doi.org/10.1007/s11274-021-03079-2

Wacher Rodarte, M.C. 2011. Microorganismos y chocolate. Revista Digital Universitaria 12(4), 3-9.

Weltzien, H. 1991. Biocontrol of foliar fungal diseases with compost extracts. pp. 430-450. In: Andrews, J.H. and S.S. Hirano (eds.). Microbial ecology of leaves. Springer Verlag, New York. Doi: https://doi.org/10.1007/978-1-4612-3168-4_22

Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York.

Wickham, H., R. François, L. Henry, and K. Müller. 2021. dplyr: A grammar of data manipulation. R package version 1.0.6. https://CRAN.R-project.org/package=dplyr

Yang, J., J. Huang, C. Wang, and Y. Feng. 2015. Effects of Allium tuberosum juice on the activities of two cell wall degrading enzymes produced by Fusarium oxysporum f. sp. cubense. J. Zhongkai Univ. Agric. Eng. 28, 64-66.

Yin, X., K. Chen, H. Cheng, X. Chen, S. Feng, Y. Song, and L. Liang. 2022. Chemical stability of ascorbic acid integrated into commercial products: A review on bioactivity and delivery technology. Antioxidants 11(1), 153. Doi: https://doi.org/10.3390/antiox11010153

Zeitsch, K. 2000. Applications of furfural. pp. 98-103. In: Zeitsch, K.J. (ed.) Sugar series. Vol. 13. Elsevier, Amsterdam. Doi: https://doi.org/10.1016/S0167-7675(00)80014-7

Zheng, H., Q. Zhang, J. Quan, Q. Zheng, and W. Xi. 2016. Determination of sugars, organic acids, aroma components, and carotenoids in grapefruit pulps. Food Chem. 205, 112-121. Doi: https://doi.org/10.1016/j.foodchem.2016.03.007

Citado por: