OCCURRENCE OF ENTOMOPATHOGENIC FUNGI ASSOCIATED WITH AVOCADO (Persea americana Mill.) SOILS IN COLIMA, MEXICO

José Carlos Rodríguez-Rodríguez, José Pedro Castruita-Domínguez, Beatriz Rodríguez-Vélez, Cecilia Neri-Luna, Miguel Angel Ayala-Zermeño

Abstract


Background: Entomopathogenic fungi (EF) play a key role in the regulation of arthropod populations and biotransformation in natural systems, as well as biological pest control agents in different agroecosystems, including avocado cultivation (Persea americana Mill.), where Mexico is a leader in production and export worldwide. Objective: Determine the presence of EF in soil in commercial avocado orchards in the state of Colima, Mexico. Methodology: Sampling was carried out in three avocado orchards (Piedra rajada, El Guardián, and Montitlán) located in Comala and Cuauhtémoc in the state of Colima, Mexico, from July 2016 to June 2017. Soil samples were collected around avocado trees. Isolation of entomopathogenic fungi was performed using the Galleria mellonella Linnaeus insect trap technique. The isolates were identified considering their micro- and macroscopic characteristics with the taxonomic keys of Humber (2012). Results: A total of 108 samples were collected, of those, 120 isolates were obtained, of which 112 belong to the genus Metarhizium and eight to Beauveria. Implications: The recovered fungi have a great value for the avocado-growing areas of the state of Colima, either for the conservation of natural enemies of soil pests or for their potential use as an alternative to synthetic insecticides. Conclusion: Knowing the native micro-biota of the soil should be considered within biological pest control strategies, since it allows selecting the best adapted species, and including sustainable alternatives for the environment. 

Keywords


Avocado; Agroecosystem; Metarhizium; Beauveria; Galleria mellonella.

Full Text:

PDF

References


Ali-Shtayeh, M.S., Abdel-Basit, B.M.M. and Rana, M.J., 2003. Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area. Mycopathologia, 156, pp. 235–244. https://doi.org/10.1023/a:1023339103522

Araújo, J.P.M. and Hughes, D.P., 2016. Diversity of Entomopathogenic Fungi Which groups conquered the insect body? In: Lovett, B., Leger, R.J.S. (eds.). Advances in genetics, vol 94. Elsevier, Amsterdam, pp. 1–39. https://doi.org/10.1016/bs.adgen. 2016.01.001

Araújo, R.G., Rodríguez-Jasso, R.M., Ruíz, H.A., Pintado, M.M. E. and Aguilar, C.N., 2018. Avocado by-products: Nutritional and functional properties: a review. Trends in Food Science & Technology, 80, pp. 51-60. https://doi.org/10.1016/j.tifs.2018.07.027

Ayala-Zermeño, M.A., Gallou, A., Berlanga-Padilla, A.M., Andrade-Michel. G.Y., Rodríguez-Rodríguez, J.C., Arredondo-Bernal, H.C. and Montesinos-Matías, R., 2017. Viability, purity, and genetic stability of entomopathogenic fungi species using different preservation methods. Fungal Biology, 121, pp. 920–928. https://doi.org/10.1016/j.funbio.2017.07.007

Barelli, L., Waller, A.S., Behie, S.W. and Bidochka, M.J., 2020. Plant microbiome analysis after Metarhizium amendment reveals increases in abundance of plant growth-promoting organisms and maintenance of disease suppressive soil. PLoS ONE, 15, e0231150. https://doi.org/10.1371/journal.pone.0231150

Berlanga-Padilla, A.M., Ayala-Zermeño, M.A., Montesinos-Matías, R. and Rodríguez-Rodríguez, J.C., 2016. Manual de Exploración para la Colecta de Hongos Entomopatógenos. Centro Nacional de Referencia de Control Biológico. Dirección General de Sanidad Vegetal. SAGARPA. SENASICA. Tecomán, Colima, México. pp. 54.

Bidochka, M.J., Kasperski, J.E. and Wild, G.A.M., 1998. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canadian Journal of Botany, 76, pp. 1198–1204. https://doi.org/10.1139/b98-115

Bischoff, J. F., Rehner, S. A. and Humber, R. A., 2009. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia, 101, pp. 508–530. https://doi.org/10.3852/07-202

Botelho, A.B., Alves-Pereira, A., Prado, R., Zucchi, M.I. and Delalibera, I., 2019. Metarhizium species in soil from Brazilian biomes: a study of diversity, distribution, and association with natural and agricultural environments. Fungal Ecology, 41, pp. 289–300. https://doi.org/10.1016/j.funeco.2019.07.004

Bruck, D.J., 2004. Natural occurrence of entomopathogens in Pacific Northwest Nursery soils and their virulence to the Black Vine Weevil, Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae). Environmental Entomology, 33, pp.1335–1343

Carlile, M.J., Watkinson, S.C. and Goodday, G.W., 2001. The Fungi. Academy Press, New York; London. https://doi.org/10.1017/S0953756203237679

Caro, D., Alessandrini, A., Sporchia, F. and Borghesi, S., 2021. Global virtual water trade of avocado. Journal of Cleaner Production, 285, pp. 124917. https://doi.org/10.1016/j.jclepro.2020.124917

Carrillo, D., Dunlap, C.A., Avery, P.B., Navarrete, J., Duncan, R.E., Jackson, M.A., Behle, R.W., Cave, R.D., Crane, J., Rooney, A.P. and Peña, J.E., 2015. Entomopathogenic fungi as biological control agents for the vector of the laurel wilt disease, the redbay ambrosia beetle, Xyleborus glabratus (Coleoptera: Curculionidae). Biological Control, 81, pp. 44–50. https://doi.org/10.1016/j.biocontrol.2014.10.009

Clifton, E.H., Jaronski, S.T., Hodgson, E.W. and Gassmann, A.J., 2015. Abundance of Soil-Borne Entomopathogenic Fungi in Organic and Conventional Fields in the Midwestern USA with an Emphasis on the Effect of Herbicides and Fungicides on Fungal Persistence. PLoS ONE, 10, 7, pp. e0133613. https://doi.org/10.1371/journal.pone.0133613

Couceiro, J.C., Fatoretto, M.B., Demétrio, C.G.B., Meyling, N.V. and Delalibera, Í. Jr., 2021. UV-B Radiation Tolerance and Temperature-Dependent Activity Within the Entomopathogenic Fungal Genus Metarhizium Brazil. Frontiers Fungal Biology, 2, pp. 645737. https://doi:10.3389/ffunb.2021.645737

Cruz-López, D.F., Caamal-Cauich, I., Pat-Fernández, V.G. and Reza-Salgado, J., 2022. Competitiveness of Mexico´s Hass avocado exports in the world market. Revista Mexicana de Ciencias Agrícolas, 13, pp. 355-362. https://doi.org/10.29312/remexca.v13i2.2885

Chandler, D., Hay, D. and Reid, A.P., 1997. Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Applied Soil Ecology, 5, pp. 133–141. https://doi.org/10.1016/S0929-1393(96)00144-8

De Dios-Avila, N., Estrada-Virgen, O., Coronado-Blanco, J., Rios-Velasco, C., Bustillos-Rodríguez, C. and Cambero-Campos, J., 2021, Parasitoids and Entomopathogens Associated with the Avocado Stem, Weevil, Copturus aguacatae (Coleoptera: Curculionidae) in Nayarit, Mexico. Entomological News, 130, 1, 61–69. https://doi.org/10.3157/021.130.0105

Dreher, M. L. and Davenport, A. J., 2013. Hass avocado composition and potential health effects. Critical Reviews in Food Science and Nutrition, 53, pp. 738-750. https://doi.org/10.1080/10408398.2011.556759

FAO. 2021. Recuperado el 5 noviembre, 2021 de: https://www.fao.org/3/cb6196en/cb6196en.pdf

Fisher, J.J., Rehner, S.A. and Bruck, D.J., 2011. Diversity of rhizosphere associated entomopathogenic fungi of perennial herbs, shrubs and coniferous trees. Journal Invertebrate Pathology, 106, pp. 289–295. https://doi.org/10.1016/j.jip.2010.11.001

García-Ávila, C. De J., Trujillo-Arriaga, F.J., López-Buenfil, J.A., González-Gómez, R., Carrillo, D., Cruz, L.F., Ruiz-Galván, I., Quezada-Salinas, A. and Acevedo-Reyes, N., 2016. First Report of Euwallacea nr. fornicatus (Coleoptera: Curculionidae) in Mexico. Florida Entomologist, 99(3), pp. 555–556. https://doi.org/10.1653/024.099.0335

Gebremariam, A., Chekol, Y. and Assefa, F., 2021. Phenotypic, molecular, and virulence characterization of entomopathogenic fungi, Beauveria bassiana (Balsam) Vuillemin, and Metarhizium anisopliae (Metschn.) Sorokin from soil samples of Ethiopia for the development of mycoinsecticide. Heliyon, 7, e07091. https://doi.org/10.1016/j.heliyon.2021.e07091

Goettel, M.S. and Inglis, D., 1997. Fungi: Hyphomycetes. In: Lacey, L.A. (ed.). Manual of Techniques in Insect Pathology. Academic Press, Londres. pp. 213–248

Guo, X.F., 2019. Diversity and community structure of fungi in the roots of Machilus pauhoi in different age groups. Applied Ecology and Environmental Research, 17, pp. 2073–2083. https://doi.org/10.15666/aeer/1702_20732083

Gutiérrez, A., Leclerque, A., Manfrino, R.G., Luz, C., Ferrari, W., Barneche, J., García, J. and López-Lastra, C., 2019. Natural occurrence in Argentina of a new fungal pathogen of cockroaches, Metarhizium argentinense sp. nov. Fungal Biology, 123, pp. 364-372. https://doi.org/10.1016/j.funbio.2019.02.005

Hajek, A.E. and Leger, R.J., 1994. Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39, pp. 293–322

Humber, R.A., 2012. Chapter VI: Identification of entomopathogenic fungi. In: Lacey, L.A. (ed.). Manual of techniques in insect pathology. Academic Press, Londres. pp. 151–186

Klingen, I., Eilenberg, J. and Meadow, R., 2002. Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agriculture Ecosystems and Environment, 91, pp. 191–198. https://doi.org/10.1016/S0167-8809(01)00227-4

Luna, A., López-Martínez, V., Bélgica Pérez-De la O, N.B., Jiménez-García, D., Jones, R. W., Castañeda-Vildozola, Á. and Ruiz-Montiel, C., 2017. Actual and potential distribution of five regulated avocado pests across Mexico, using the maximum entropy algorithm. Florida Entomologist, 100, pp. 92–100. https://doi.org/10.1653/024.100.0114

Maldonado-Zamora, F.I., Ramírez-Dávila, J.F., Rubí-Arriaga, M., Antonio-Némiga, X. and Lara-Díaz, A.V., 2016. Distribución espacial de trips en aguacate en Coatepec Harinas, Estado de México. Revista Mexicana de Ciencias Agrícolas, 7, pp. 845-856. https://doi.org/10.29312/remexca.v7i4.259

Meyling, N.V. and Eilenberg, J., 2006. Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agriculture Ecosystems and Environment, 113, pp. 336–341. https://doi.org/10.1016/j.agee.2005.10.011

Meyling, N.V. and Eilenberg, J., 2007. Ecology of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biological Control, 43, pp. 145–155. https://doi.org/10.1016/j.biocontrol.2007.07.007

Meyling, N.V., 2007. Methods for isolation of entomopathogenic fungi from the soil environment. Laboratory manual. Department of Ecology, Faculty of Life Sciences, University of Copenhagen

Mier, T., Toriello, C. and Ulloa, M., 2002. Hongos microscópicos saprobios y parásitos: métodos de laboratorio. UAM-Xochimilco, UNAM-Instituto de Biología, México D.F.

Montesinos-Matías, R., Ordaz-Hernández, A., Ángel-Cuapio, A., Colin-Bonifacio, Y., García-García, R.E., Ángel-Sahagún, C.A., and Arredondo-Bernal, H.C., 2021. Principal component analysis of the biological characteristics of entomopathogenic fungi in nutrient-limited and cuticle-based media. Journal of Basic Microbiology, 61, pp. 147–156. https://doi.org/10.1002/jobm.202000627

Nataren-Velázquez, J., Ángel-Pérez, A.L., Megchún-García, J.V., Ramírez-Herrera, E. and Meneses-Márquez, I., 2020. Caracterización productiva del aguacate (Persea americana) en la zona de alta montaña Veracruz, México. Revista Iberoamericana de Bioeconomía y Cambio Climático, 6, pp. 1406–1423. https://doi.org/10.5377/ribcc.v6i12.9941

Onofre, S., Miniuk, C., Barros, N. and Azevedo, J., 2001. Pathogenicity of four strains of entomopathogenic fungi against the bovine tick Boophilus microplus. American Journal of Veterinary Research, 62, pp. 1478–1480. https://doi.org/10.2460/ajvr.2001.62.1478

Qayyum, M.A., Saeed, S., Wakil, W., Nawaz, A., Iqbal, N., Yasin, M., Chaurdhry, M.A., Bashir, M.A., Ahmed, N., Riaz, H., Bial, H., Hashem, M. and Alamri, S., 2021. Diversity and correlation of entomopathogenic and associated fungi with soil factors. Journal of King Saud University – Science, 33(6), pp. 101520. https://doi.org/10.1016/j.jksus.2021.101520

Quesada-Moraga, E., Navas-Cortés, J.A., Maranhao, E.A., Ortiz-Urquiza, A. and Santiago-Álvarez, C., 2007. Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycological Research, 111, pp. 947–966. https://doi.org/10.1016/j.mycres.2007.06.006

Rudeen, M.L., Jaronski, S.T., Petzold-Maxwell, J.L. and Gassmann, A.J., 2013. Entomopathogenic fungi in cornfields and their potential to manage larval western corn rootworm Diabrotica virgifera virgifera. Journal Invertebrate Pathology, 114, pp. 329–332. https://doi.org/10.1016/j.jip.2013.09.009

Sabouraud, R.J.A., 1910. Les teignes. Masson. Paris. P.p. 988. https://archive.org/details/lesteignesOOsabo. Consultado el 28/09/2015

SIAP. 2021. Acciones y Programas. Producción mensual Agrícola. Recuperado el 14 septiembre, 2021 de: https://nube.siap.gob.mx/avance_agricola/

Trizelia, T., Armon, N. and Jailani, H., 2015. The diversity of entomopathogenic fungi in the rizosphere of various vegetable crops. Prosiding Seminar Nasional Masyarakat Biodiversitas Indonesia, 1, pp. 998–1004. https://doi.org/10.13057/psnmbi/m010507

Vega, F.E., Goettel, M.S., Blackwell, M., Chandler, D., Jackson, M.A. and Keller, S., 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecology, 2, pp. 149–159. https://doi.org/10.1016/j.funeco.2009.05.001

Velázquez, J.N., Ángel-Pérez, A., Megchún-García, J.V., Herrera, E. and Márquez, I., 2020. Caracterización productiva del aguacate (Persea americana) en la zona de alta montaña Veracruz, México. Revista Iberoamericana de Bioeconomía y Cambio Climático, 6, pp. 1406-1426. https://doi.org/10.5377/ribcc.v6i12.9941

Vukicevich, E., MacDonald, M.D., Lowery, T. and Hart, M., 2020. The effect of vineyard groundcover on the abundance of naturally occurring entomopathogenic fungi isolated using a quantitative Galleria bait method. Rhizosphere, 15, pp. 100232. https://doi.org/10.1016/j.rhisph.2020.100232

Wysoki, M., Van Den Berg, M.A., Ish-Am, G., Gazit, S., Peña, J.E. and Waite, G.K., 2002. Pests and pollinators of avocado. In: Peña, J. E., Sharp, J.L. and Wysoki, M. (eds.). Tropical Fruits Pests and Pollinators: Biology, Economic Importance, Natural Enemies and Control. CABI, Londres. pp. 223-293

Wyrebek, M., Huber, C., Sasan, R.K. and Bidochka, M.J., 2011. Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity. Microbiology, 157, pp. 2904-2911. https://doi.org/10.1099/mic.0.051102-0

Yilma, S., Kebede, D. and Mihrete, T., 2019. Distribution and occurrences of Entomopathogenic fungi in southern and western zones of Ethiopia. International Journal of Current Research and Academic Review, 7, pp. 8–17. https://doi.org/10.20546/ijcrar.2019.710.002

Zimmermann, G., 1986. The Galleria bait method for detection of entomopathogenic fungi in soil. Journal of Applied Entomology, 102, pp. 213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x

Zimmermann, G., 2007. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Science and Technology, 17, pp. 879–920. https://doi.org/10.1080/09583150701593963

Zuluaga-Cárdenas, P.A., Caicedo-Vallejo, A.M, Cardozo-Santamaría, N., Muñoz-Flórez, J.E. and Carabalí-Muñoz, A., 2015. Entomopatógenos asociados a cítricos y su patogenicidad sobre Compsus viridivittatus Guérin-Méneville (Coleoptera: Curculionidae). Corpoica Ciencia y Tecnología Agropecuaria, 16, pp. 293–305. https://doi.org/10.21930/rcta.vol16_num2_art:374




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v26i2.45921

DOI: http://dx.doi.org/10.56369/tsaes.4592



Copyright (c) 2023 José Carlos Rodríguez-Rodríguez, José Pedro Castruita-Domínguez, Beatriz Rodríguez-Vélez, Cecilia Neri-Luna, Miguel Angel Ayala-Zermeño

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.