NATIVE ENTOMOPATHOGENIC NEMATODES IN THE CULTIVATION OF PRICKLY PEAR IN MILPA ALTA, MEXICO

Evert Villanueva-Sánchez, Samuel Ramírez-Alarcón, Clemente Villanueva-Verduzco, José Enrique Herbert-Pucheta

Abstract


Background. Entomopathogenic nematodes (NEP) are found in all ecosystems. Currently, they are one of the most studied ecological alternatives for the biological control of insect pests. In Mexico, there are few reports of their presence in agricultural soils. Objective. To isolate and identify molecularly native specimens of entomopathogenic nematodes from soil samples collected in different prickly pear producing areas in Milpa Alta, Mexico City. Methodology. Isolations were obtained from soil samples using the technique of insect lure (Galleria mellonella or greater wax moth). Molecular techniques of the ribosomal region (ITS1+5.8S+ITS2) were performed for nematode identification. Results. Of the NEP isolates for the genus Steinernema, the phylogenetic analysis (ML; HKY) grouped the sequences of the isolates in the species Steinernema texanum, with 100 % similarity and 81 % similarity between isolates. For Heterorhabditis, the analysis (M; HKY) grouped the sequenced isolates in the species Heterorhabditis atacamensis with 97 % similarity. The results show that the NEP are widely distributed in the study region. Implications. The presence of these isolates in the cultivation of prickly pear (nopalitos) is important since they are a potential biological tool for pest management in the study zone. Conclusion. For the first time, the presence of Steinernema texanum and Heterorhabditis atacamensis is reported in soils cultivated with prickly pear in Milpa Alta, Mexico.

Keywords


Opuntia ficus-indica L.; Steinernema; Heterorhabditis.

Full Text:

PDF

References


Amador, M., Molina, D., Guillen, C., Parajeles, E., Jiménez, K. and Uribe, L., 2015. Utilización del nematodo entomopatógeno Heterorhabditis atacamensis CIA-NE07 en el control del picudo del banano Cosmopolites sordidus en condiciones in vitro. Agronomía Costarricense, 39, pp. 47-60. https://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0377-94242015000300047

Aquino, B. T., Ruiz, V. J. and Iparraguirre, C. M., 2006. Control biológico del picudo negro (Scyphophorus interstitialis Gyllenhal) con nematodos y hongos entomopatógenos en agave en Oaxaca, México. Revista UDO Agrícola, 6, pp. 92-101.

Askary, T. H., 2010. Nematodes as biocontrol agents. In: E. Lichtfouse, eds. Sociology, organic farming, climate change and soil science. Springer, The Netherlands. pp. 347-378. https://doi.org/10.1007/978-90-481-3333-8_13.

Askary, T. H. and Abd-Elgawad, M. M. M., 2017. Beneficial nematodes in agroecosystem: A global perspective. In: Abd-Elgawad M. M. M., Askary, T. H. Coupland, eds. Biocontrol Agents: entomopathogenic and slug parasitic nematodes. CAB International. pp. 3-25. https://doi.org/10.1079/9781786390004.0003.

Bhat, A. H., Chaubey, A. K., and Askary, T. H., 2020. Global distribution of entomopathogenic nematodes, Steinernema and Heterorhabditis. Egyptian Journal of Biological Pest Control, 30, pp. 1-15. https://doi.org/10.1186/s41938-020-0212

Bortoluzzi, L., Alves, L. F. A., Alves, V. S. and Holz, N., 2013. Entomopathogenic nematodes and their interaction with chemical insecticide aiming at the control of banana weevil borer. Cosmopolites sordidus Germar (Coleoptera: Curculionidae). Arquivos do Instituto Biológico, 80, pp. 183-192. https://doi.org/10.1590/S1808-16572013000200007.

Bruno, P., Machado, R.A.R., Glauser, G., Köhler, A. and Campos-Herrera., 2020. Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Scientific Reports, 10, pp. 8257. https://doi.org/10.1038/s41598-020-64945-x

Ciche, T. A., Kim, K. S., Kaufmann, B., Nguyen, K. C. and Hall, D. H., 2008. Cell invasión and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Applied and Environmental Microbiology, 74, pp. 2275-2287. https://doi.org/10.1128/AEM.02646-07.

Cortez-Madrigal, H., Morales-Salvador, P. and Adams, B., 2003. Primer registro en México de Heterorhabditis indicus Poinar. In: Vázquez-García, M., Pérez Domínguez, J. F., lbarra-Cortés, K. H., Balpuesta-León, C. L., Vázquez-Reyes, J. R., Cervantes-Ríos, J. y N. lbarra-Frías, eds. Memorias del XXVI Congreso Nacional de Control Biológico. Sociedad Mexicana de Control Biológico, Texcoco, México. pp. 68-70.

Delgado-Gamboa, J. R., Ruíz-Vega, J., Aquino-Bolaños, T. and Girón-Pablo, S., 2014. Revisión de nematodos entomopatógenos aislados en México. Entomología Mexicana, 1, pp. 284-288.

Díaz-Maderos, P., 2002. Abundancia y distribución de especies de “gallina ciega” (Coleoptera: Melolonthidae), Hongos (Hypomycetes) y nematodos entomopatógenos en los Altos de Jalisco, México. Tesis de Maestría. Área: Biotecnología. Universidad de Colima, Tecomán, México.

Edgington, S., Buddie A. G., Moore, D., France, A., Merino, L. and Hunt, D. J., 2011. Heterorhabditis atacamensis n. sp. (Nematoda: Heterorhabditidae), a new entomopathogenic nematode from the Atacama Desert. Chile Journal of Helminthology, 85, pp. 381-394. https://doi.org/10.1017/S0022149X10000702

Erba?, Z., Gökçe, C., Hazir, S., Demirba?, Z., and Demir, ?., 2014. Isolation and identification of entomopathogenic nematodes (Nematoda: Rhabditida) from the Eastern Black Sea region and their biocontrol potential against Melolontha melolontha (Coleoptera: Scarabaeidae) larvae. Turkish Journal of Agriculture and Forestry, 38, pp. 187-197. https://doi.org/10.3906/tar-1301-42

Fimbres, C.G. and Flores-Lara, Y., 2016. Potencialidad y retos del uso de nematodos entomopatógenos para el control biológico de plagas. Control biológico mediante una asociación simbiótica NEP-bacteria. INVURNUS, 11, pp. 27-36.

Girón, P. S., Ruíz, V. L., Pérez, P. R., Sánchez, G. J. A., and Aquino, B. T., 2012. Isolation of entomopathogenic nematodes and control of Phyllophaga vetula Horn in Oaxaca, México. African Journal of Biotechnology. 11, pp. 16525-16531.

González-Ramírez, M., 2006. Presencia, Identificación y Patogenicidad de nematodos entomopatógenos aislados de suelos del Pacífico Centro Mexicano. In: Delgado-Gamboa, J. R., Ruíz-Vega, J., Aquino-Bolaños, T., and Girón-Pablo, S., 2014. Revisión de nematodos entomopatógenos aislados en México. Entomología Mexicana, 1, pp. 284-288.

Grifaldo-Alcántara, P. F., Alatorre-Rosas, R., Villanueva-Jiménez, J. A., Hernández-Rosas, F., Stock, S. P. and Ramírez-Valverde, G., 2019. Evaluación de dos cepas de nematodos entomopatógenos (Steinernematidae, Heterorhabditidae) para el control del salivazo (Hemiptera: Cercopidae) en caña de azúcar. Nematropica, 49, pp. 83-90.

Grifaldo-Alcantara, P. F., Alatorre-Rosas, R., Silva-Rojas, H. V., Stock, S. P., Hernández-Rosas, F., Vargas- Madriz, H., Azuara-Domínguez, A., and Durán-Trujillo, Y., 2020. Caracterización molecular y morfométrica de Heterorhabditis indica (cepa CP13JA) aislado en el cultivo de caña de azúcar. Tropical and Subtropical Agroecosystems, 23, #64. https://www.revista.ccba.uady.mx/ojs/index.php/TSA/article/view/3278/1449

Hasegawa M., Kishino H., and Yano T., 1985. Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, pp. 160-174.

Hominick, W.M., Reid, A.P., Bohan, D.A. and Briscoe, B. R., 1996. Entomopathogenic nematodes: biodiversity, geographical distribution and the convention on biological diversity. Biocontrol Science Technology, 6, pp. 317-331. https://doi.org/10.1080/09583159631307.

Howlett, B.J., Brownlee, A.G., Guest, D.I., Adcock, G.J. and Mc Fadden, G. I., 1992. The 5S ribosomal RNA gene is linked to large and small subunit ribosomal RNA genes in the oomycetes, Phytophthora vignae, P. cinnamomi, P. megaspera f. sp. glycinae and Saprolegnia ferax. Current Genetics, 22, pp. 455-461. https://doi.org/10.18781/R.MEX.FIT.1601-2.

Joyce, S.A., Reid, A., Driver, F. and Curran, J., 1994. Application of polymerase chain reaction (PCR) methods to the identification of entomopathogenic nematodes. In: Burnell, A.M., Ehlers, R.U., and Masson, J.P., eds. Biotechnology: Genetics of entomopathogenic nematodes bacterium complexes. Proceedings of symposium and workshop, St Patrick’s College, Maynooth, County Kildare, Ireland. Luxembourg, European Commission, DGXII. pp. 178-187.

Kaya, H.K., Agulliera, M.M., Alumai, A., Choo, H.Y., De la Torre, M., Andras, F., Sudershan, G., Hazir, S., Lakatos, T., Pye, A., Wilson, M., Yamanaka, S., Yang, Huaiwan, Y., and Ehlers, R. U., 2006. Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world. Biological Control, 38, pp. 134–155. https://doi.org/10.1016/j.biocontrol.2005.11.004.

Koppenhöfer, M, A., Shapiro-Ilan, D. I. and Hiltpold, I., 2020. Entomopathogenic Nematodes in Sustainable Food Production. Frontiers in Sustainable Food Systems, 4, pp. 1-14. https://doi.org/10.3389/fsufs.2020.00125.

Lewis, E. E., and Clarke, D. J., 2012. Nematodes Parasites and entomopathogens. In: Kaya, H. K., y Vega, F. E., eds. Insect Pathology. Elsevier. pp. 397-398.

Lezama, G., Molina, J. O., Contreras, M. L. O., González, M. R., Trujillo de la L, A. and Rebolledo, O. D., 1996. Susceptibilidad de larvas de Anastrepha ludens (Diptera: Tephritidae) a diversos nematodos entomopatógenos (Steinernematidae y Heterorhabditidae). Vedalia, 3, pp. 31-34.

Lezama-Gutiérrez, R., Hamm, J. J., Molina-Ochoa, J., López-Edwards, M., Pescador-Rubio, A., González-Ramírez, M. and Styer, L. E., 2001. Occurrence of entomopathogens of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Mexican States of Michoacán, Colima, Jalisco and Tamaulipas. Florida Entomologist. 84, pp. 23-30. https://doi.org/10.2307/3496658.

Machado, A. R., P., Bruno, C. M., Arce, C. M., Liechti, N., Bernal, J., Bruggmann, R. and Turlings C. J. 2019. Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminences subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. Taxonomic Description. 69, pp. 652-661. https://doi:10.1099/ijsem.0.003154.

Molina, O. J., Hamm, R., Lezama, G. L., Bojalil, F. J., Arenas, M. V. and González, M. R., 1996. Virulence of six entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) on immature stages of Spodoptera frugiperda (Lepidoptera: Noctuidae). Vedalia, 3, pp. 25-30.

Molina-Ochoa, J., Lezama-Gutiérrez, R., González-Ramírez, M., López-Edwards, M., Rodríguez-Vega, M. A. and Arceo-Palacios, F., 2003. Pathogens and parasitic nematodes associated with populations of fall armyworm (Lepidoptera: Noctuidae) larvae in México. In: Vázquez-García, M., Pérez Domínguez, J. F., Ibarra-Cortes, K., Balpuesta-León, C., Vázquez-Reyes, R., Cervantes-Ríos, J., and Ibarra-Frías, N., eds. Memorias del XXVI Congreso Nacional de Control Biológico. Sociedad Mexicana de Control Biológico, Texcoco, México. pp. 14-17.

Negrete-García, R. 2013. Nematodos entomopatógenos procedentes de la rizósfera de suelos maiceros infestados con gallina ciega Phyllophaga polyphylla. In: Delgado-Gamboa, J. R., Ruíz-Vega, J., Aquino-Bolaños, T. and Girón-Pablo, S., 2014. Revisión de nematodos entomopatógenos aislados en México. Entomología Mexicana, 1, pp. 284-288.

Nguyen, K. B., Shapiro-Ilan, D. I., Stuart, R. J., Mccoy, C. W., James, R. R. and Byron J. A., 2004. Heterorhabditis mexicana n. sp. (Rhabditida: Heterorhabditidae) from Tamaulipas, Mexico, and morphological studies of the bursa of Heterorhabditis spp. Nematology, 6, pp. 231-244. https://doi.org/10.1163/1568541041218031.

Nguyen, K. B., Stuart, R. J., Andalo, V., Gozel, U. and Rogers, M. E., 2007. Steinernema texanum n. sp. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from Texas, USA. Nematology, 9, pp. 379-396.

Pacheco, H. M. L., Reséndiz, M. J. F., and Arriola, P. V, J., 2019. Organismos entomopatógenos como control biológico en los sectores agropecuario y forestal de México: una revisión. Revista Mexicana de Ciencias Forestales, 10, pp. 4-32. https://doi.org/10.29298/rmcf.v10i56.496.

Poinar, G. O., 1990. Taxonomy and biology of Steinernematidae and Heterorhabitidae. In: Gaugler, R. and Kaya, H. K., eds. Entomopathogenic nematodes in biological. Boca Raton. Fl, CRC Press. pp. 23-61.

Ruíz, V. J., Aquino, B. T., Kaya, H. K. and Stock, P., 2003. Colecta y evaluación de nematodos entomopatógenos para el control de gallinas ciegas Phyllophaga vetula (Horn) en Oaxaca, México. Folia Entomologica Mexicana, 42, pp. 169-175.

Shapiro-Ilan, D.I., Hazir, S., and Glazer, I., 2017. Basic and applied research: Entomopathogenic nematodes, in Lacey L.A. Ed., Microbial Control of Insect and Mite Pests: From Theory to Practice, Academic Press, San Diego, CA, pp. 91-105. https://doi.org/10.1016/b978-0-12-803527-6.00006-8.

SIAP (Servicio de Información Agroalimentaria y Pesquera). 2021. Producción agrícola por cultivo y por estado. https://nube.siap.gob.mx/cierreagricola/ 29 de septiembre 2021.

Simard, L., Bélair, G. and Brodeur, J., 2001. Susceptibility of the European chafer (Coleoptera: Scarabaeidae) to entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae). Journal of Nematology, 33, pp. 297-301.

Spiridonov, S. E., Krasomil-Osterfeld, K. and Moens, M., 2004. Steinernema jollieti sp. N. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from the American Midwest, Russian Journal of Nematology, 12, pp. 85-95.

Stock, S. P., Rivera-Orduño, B. and Flores-Lara, T., 2009. Heterorhabditis sonorensis n. sp. (Nematoda: Heterorhabditidae), a natural pathogen of the seasonal cicada Diceroprocta ornea (Walker) (Homoptera: Cicadidae) in the Sonoran desert. Journal of Invertebrate Pathology, 100, pp. 175-184. https://doi.org/10.1016/j.jip.2008.11.011.

Sturhan, D. and Mracek, Z., 2000. Comparison of the Galleria baiting technique and a direct extraction method for recovering Steinernema (Nematoda: Rhabditida) infective-stage juveniles from soil. Folia Parasitologica, 47, pp. 315-318.

Tamura K., Stecher G., Peterson D., Filipski A., and Kumar S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, pp. 2725-2729. https://doi.org/10.1093/molbev/mst197.

Toledo, J., Gurgúa, J. L., Liedo, P., Ibarra, J. E. and Oropeza, A., 2001. Parasitismo de larvas y pupas de la mosca mexicana de la fruta Anastrepha ludens (Loew) (Diptera: Tephritidae) por el nematodo Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae). Vedalia, 8, pp. 27-36.

White, G. F., 1927. A method for obtaining infective nematode larvae from cultures. Science, 66, pp. 302-303. https://doi:10.1126/science.66.1709.302-a

Zhang, Z., Schwartz, S., Wagner, L. and Miller, W., 2000. A greedy algorithm for aligning DNA sequences. Journal Computational Biology, 7, pp. 203-214. https://doi.org/10.1089/10665270050081478.




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v25i3.41237

DOI: http://dx.doi.org/10.56369/tsaes.4123

Bookmark and Share


Copyright (c) 2022 Evert Villanueva-Sánchez, Samuel Ramírez-Alarcón, Clemente Villanueva-Verduzco, José Enrique Herbert-Pucheta

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