Keywords
Steinernema
Heterorhabditis
Cosmopolites sordidus
banano
Steinernema
Heterorhabditis
Cosmopolites sordidus
How to Cite
Abstract
Introduction: In Costa Rica the banana is one of the most important crops in terms of production and exports; the application of pesticides is hence necessary to control the effect of pests on the plantation, such as the Cosmopolites sordidus black weevil. Because of the harmful effects of pesticides on human and environmental health, and the possibility that pests become resistant to these substances, alternatives compatible with the environment, as potential biological controllers, have been investigated to complement the effect of agrochemicals. The entomopathogenic nematodes (EPN) of genera Heterorhabditis and Steinernema have become a focus of study in the field of biological control because of their symbiotic relation with bacteria of genera Photorhabdus and Xenorhabdus, which are a complex capable of eliminating host insects in hours. Objective: The objective was to determine the presence of EPN of genera Heterorhabditis and Steinernema in soil samples taken from banana plantations in the Caribbean region of Costa Rica, and to characterize their habitat. Methods: Sampling points were selected within the plantations and surrounding areas; physicochemical and microbiological analyses were undertaken (pH, acidity, organic matter, Ca, K, Mg, P, Fe, Cu, Zn, Mn, texture, biomass and microbial respiration of the soil, EPN isolation). Variables were analyzed statistically to determine differences between them, in sampling sites, and samples with presence and absence of EPN. A principal-component analysis (PCA) was undertaken using the variables of greater influence in both categories to find their combinations that would explain their presence according to habitat conditions. A discriminant analysis was undertaken to determine the efficiency of the variables selected in the diagnosis of nematode occurrence. Results: The variables related to the presence of EPN were shown to correspond to organic matter, carbon biomass and microbial respiration. Of the samples 38.4 % were found to be positive with respect to the presence of EPN, of which 95 % correspond to genus Steinernema and the remaining 5 % to Heterorhabditis. According to the quadratic discriminant equation, from 81.2 % of the samples without nematodes, six belong to the group with their presence, whereas for those with EPN, 55.0 % (nine of 20) belong to the absence group. Conclusions: No statistical difference was found between the selected sampling habitats (P = 0.4296); the three variables mentioned above were thus determined have an influence on the presence of EPN; their large values indicate favorable conditions for their persistence.
References
Alpízar, M. (2017). Estadísticas de Comercio Exterior Costa Rica, 2016. Promotora del Comercio Exterior de Costa Rica. San José, Costa Rica: PROCOMER.
Amador, M., Molina, D., Guillen, C., Parajeles E., Jiménez, K., & Lorío, L. (2015). Utilización del nemátodo entomopatógeno Heterorhabditis atacamensis CIA-NE-07 en el control del picudo del banano Cosmopolites sordidus en condiciones in vitro. Agronomía Costarricense, 39(3), 47-60.
Andaló, V., Mieko, J., Carvalho, F. J., de Assis, G. A., de Faria, L. S., de Assis, F. A., ... Rosa, F. (2018). Entomopathogenic nematode distribution and edaphoclimatic conditions in the Cerrado of Minas Gerais, Brazil. Applied Entomology and Zoology, 53(1), 129-136. DOI:10.1007/s13355-017-0538-4
Bedding, R. A. (1990). Logistics and strategies for introducing entomopathogenic nematode technology into developing countries. Entomopathogenic Nematodes in Biological Control, 233-246.
Bedding, R. A., & Akhurst, R. J. (1975). A simple technique for the detection of insect paristic rhabditid nematodes in soil. Nematologica, 21(1), 109-110.
Bogantes, D., Flores, L., Castellón, E., & Uribe, L. (2018). Encapsulamiento de nemátodos entomopatógenos en materiales basados en biopolímeros y su efecto sobre Galleria mellonella. Agronomía Costarricense, 42(2), 9-27.
Bouyoucos, G. J. (1962). Hydrometer method improved for making particle size analyses of soils 1. Agronomy Journal, 54(5), 464-465.
Briar, S. S., Grewal, P. S., Somasekhar, N., Stinner, D., & Miller, S. A. (2007). Soil nematode community, organic matter, microbial biomass and nitrogen dynamics in field plots transitioning from conventional to organic management. Applied Soil Ecology, 37(3), 256-266. DOI: 10.1016/j.apsoil.2007.08.004
Carballo, M. (2001). Opciones para el manejo del picudo negro del plátano. Manejo integrado de plagas (Costa Rica), Hoja técnica N° 36. CATIE, 59, 1-4. Recuperado de http://hdl.handle.net/11554/6619
Castillo, L. E., Ruepert, C., & Solis, E. (2000). Pesticide residues in the aquatic environment of banana plantation areas in the north Atlantic zone of Costa Rica. Environmental Toxicology and Chemistry: An International Journal, 19(8), 1942-1950. DOI:10.1002/etc.5620190802
Cerda, H., López, A., Sanoja, O., Sánchez, P., & Jaffé, K. (1996). Atracción olfativa de Cosmopolites sordidus Germar (1824) (Coleoptera: Curculionidae) estimulado por volátiles originados en musáceas de distintas edades y variedades genómicas. Agronomía Tropical, 46(4), 413-429.
CORBANA. (2011). Implementación de Buenas Prácticas Agrícolas para Reducir el Escurrimiento de Plaguicidas en el Cultivo del Banano de la Región Caribe Costarricense [Figura]. Recuperado de: http://cep.unep.org/repcar/proyectos-demostrativos/costa-rica-1/publicaciones-corbana/Estudio%20de%20caso%20Corbana.pdf
CORBANA. (2017). Estadísticas, exportación bananera, Costa Rica. CORBANA Corporación Bananera Nacional. Recuperado de: https://www.corbana.co.cr/banano-de-costa-rica/#estadistica
Cuille, J. (1950). Recherches sur le charançon du bananier, Cosmopolites sordidus, Germ. Serie Tech. 4. Institut des Fruits et Légumes Coloniaux, 225.
De Nardo, E. A., & Grewal, P. S. (2003). Compatibility of Steinernema feltiae (Nematoda: Steinernematidae) with pesticides and plant growth regulators used in glasshouse plant production. Biocontrol Science and Technology, 13(4), 441-448. DOI: 10.1080/0958315031000124495
Ferris, H., Venette, R. C., & Lau, S. S. (1996). Dynamics of nematode communities in tomatoes grown in conventional and organic farming systems, and their impact on soil fertility. Applied Soil Ecology, 3(2), 161-175. DOI:10.1016/0929-1393(95)00071-2
García, D. P. F., & Palomo, A. (1996). Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Spanish soils. Journal of Invertebrate Pathology, 68(1), 84-90. DOI: 10.1006/jipa.1996.0062
Gold, C. S., & Messiaen, S. (2000). El picudo negro del banano Cosmopolites sordidus. Inibap, Plagas de Musa, Hoja Divulgativa, 4, 1-4.
Gold, C. S., Pena, J. E., & Karamura, E. B. (2001). Biology and integrated pest management for the banana weevil Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae). Integrated Pest Management Reviews, 6(2), 79-155. DOI:10.1023/A:1023330900707
Gómez, R. G., & Soto, G. A. (2008). Productos alternativos para el manejo de Cosmopolites sordidus (Coleóptera: Dryophthoridae). Revista Agronomía, 16(2), 45-50.
González, D. N., Chávez, M. A. Á., Gutiérrez, R. L., Cupul, W. C., Ochoa, J. M., & Velasco, E. G. (2018). Suitability of Cordyceps bassiana and Metarhizium anisopliae for biological control of Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) in an organic Mexican banana plantation: laboratory and field trials. Journal of Plant Diseases and Protection, 125(1), 73-81. DOI: 10.1007/s41348-017-0126-4
Griffin, C. T., & Downes, M. J. (1991). Low temperature activity in Heterorhabditis sp. (Nematoda: Heterorhabditidae). Nematologica, 37(1-4), 83-91. DOI:10.1163/187529291X00088
Gutiérrez, T. (2 de julio del 2014). Registro de nematicida descubierto en Costa Rica beneficiará a productores de banano. Recuperado de https://archivo.crhoy.com
Hara, A. H., Gaugler, R., Kaya, H. K., & Lebeck, L. M. (1991). Natural populations of entomopathogenic nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) from the Hawaiian Islands. Environmental Entomology, 20(1), 211-216. DOI: 10.1093/ee/20.1.211
Hiltpold, I. (2015). Prospects in the application technology and formulation of entomopathogenic nematodes for biological control of insect pests. In R. Campos-Herrera (Ed.), Nematode pathogenesis of insects and other pests (pp. 187-205). Switzerland: Springer, Cham.
Horwitz, W. (2000). AOAC official methods of analysis. Gaithersburg, MD: Association of Official Analytical Chemists International. Sections, 50(21), 992-05.
Jenkinson, D. S., & Powlson, D. S. (1976). The effects of biocidal treatments on metabolism in soil-V: A method for measuring soil biomass. Soil Biology and Biochemistry, 8(3), 209-213. DOI:10.1016/0038-0717(76)90005-5
Kanga, F. N., Waeyenberge, L., Hauser, S., & Moens, M. (2012). Distribution of entomopathogenic nematodes in Southern Cameroon. Journal of Invertebrate Pathology, 109(1), 41-51. DOI: 10.1016/j.jip.2011.09.008
Kaya, H. K. (1990). Soil Ecology. In R. Gaugler & H. K. Kaya (Eds.), Entomopathogenic Nematodes in Biological Control (pp. 93-98). Florida, United States: CRC Press.
Kaya, H. K., & Stock, S. P. (1997). Techniques in insect nematology. In L. A. Lacey (Ed.), Manual of techniques in insect pathology (pp. 281-324). United States: Academic Press.
Koppenhöfer, A. M., & Fuzy, E. M. (2006). Effect of soil type on infectivity and persistence of the entomopathogenic nematodes Steinernema scarabaei, Steinernema glaseri, Heterorhabditis zealandica, and Heterorhabditis bacteriophora. Journal of Invertebrate Pathology, 92(1), 11-22. DOI: 10.1016/j.jip.2006.02.003
Kung, S. P. (1990). Abiotic factors affecting the persis-tence of two entomopathogenic nematodes, Steinernema carpocapsae and Steinernema glaseri (Nematoda: Steinernematidae), in the soil (Doctoral dissertation). Rutgers University, New Jersey, USA.
Lawrence, J. L., Hoy, C. W., & Grewal, P. S. (2006). Spatial and temporal distribution of endemic entomopathogenic nematodes in a heterogeneous vegetable production landscape. Biological Control, 37(3), 247-255. DOI: 10.1016/j.biocontrol.2006.02.002
Laznik, Z., Vidrih, M., & Trdan, S. (2012). The effects of different fungicides on the viability of entomopathogenic nematodes Steinernema feltiae (Filipjev), S. carpocapsae Weiser, and Heterorhabditis downesi Stock, Griffin & Burnell (Nematoda: Rhabditida) under laboratory conditions. Chilean Journal of Agricultural Research, 72(1), 62.
Lopes, R. B., Laumann, R. A., Moore, D., Oliveira, M. W., & Faria, M. (2014). Combination of the fungus Beauveria bassiana and pheromone in an attract‐and‐kill strategy against the banana weevil, Cosmopolites sordidus. Entomologia Experimentalis et Applicata, 151(1), 75-85. DOI: 10.1111/eea.12171
Maharaj, K., & Khan, A. (2016). Efficacy of banana spray oil, mineral oil and water formulations of Beauveria bassiana Balsamo for the control of Cosmopolities sordidus Germar (Coleoptera: Curculionidae) in Musa spp. International Journal of Tropical Agriculture, 34(6), 1455-1460.
Marianelli, L., Paoli, F., Torrini, G., Mazza, G., Benvenuti, C., Binazzi, F., ... Priori, S. (2018). Entomopathogenic nematodes as potential biological control agents of Popillia japonica (Coleoptera, Scarabaeidae) in Piedmont Region (Italy). Journal of Applied Entomology, 142(3), 311-318. DOI: 10.1111/jen.12470
Mehlich, A. (1984). Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant. Communications in Soil Science and Plant Analysis, 15(12), 1409-1416. DOI: 10.1080/00103628409367568
Mendez, A., Castillo, L. E., Ruepert, C., Hungerbuehler, K., & Ng, C. A. (2018). Tracking pesticide fate in conventional banana cultivation in Costa Rica: A disconnect between protecting ecosystems and consumer health. Science of the Total Environment, 613, 1250-1262. DOI: 10.1016/j.scitotenv.2017.09.172
Mráček, Z., Bečvář, S., Kindlmann, P., & Jersáková, J. (2005). Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biological Control, 34(1), 27-37. DOI:10.1016/j.biocontrol.2005.03.023
Mwaitulo, S., Haukeland, S., Sæthre, M. G., Laudisoit, A., & Maerere, A. P. (2011). First report of entomopathogenic nematodes from Tanzania and their virulence against larvae and adults of the banana weevil Cosmopolites sordidus (Coleoptera: Curculionidae). International Journal of Tropical Insect Science, 31(3), 154-161. DOI:10.1017/S1742758411000294
Nahar, M. S., Grewal, P. S., Miller, S. A., Stinner, D., Stinner, B. R., Kleinhenz, M. D., ... Doohan, D. (2006). Differential effects of raw and composted manure on nematode community, and its indicative value for soil microbial, physical and chemical properties. Applied Soil Ecology, 34(2-3), 140-151. DOI: 10.1016/j.apsoil.2006.03.011
Navarro, P. D., McMullen II, J. G., & Stock, S. P. (2014). Effect of dinotefuran, indoxacarb, and imidacloprid on survival and fitness of two Arizona-native entomopathogenic nematodes against Helicoverpa zea (Lepidoptera: Noctuidae). Nematropica, 44(1), 64-73.
Nelson, D. W., & Sommers, L. (1982). Total carbon, organic carbon, and organic matter. In A. L. Page (Ed.), Methods of soil analysis. Part 2. Chemical and microbiological properties (pp. 539-579). Madison, Wisconsin USA: Academic Press, American Society of Agronomy Inc y Soil Science of America Inc.
Nguyen, K. B. (2007). Methodolgy, morphology and identification. En K. B. Nguyen & D. J. Hunt (Eds.), Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts (pp 68-118). The Netherlands: Brill Lieden Boston.
Padilla-Cubas, A., Carnero Hernandez, A., & Garcia-del-Pino, F. (2010). Laboratory efficacy against neonate larvae of the banana weevil Cosmopolites sordidus of two indigenous entomopathogenic nematode species from the Canary Islands (Spain). International Journal of Pest Management, 56(3), 211-216. DOI:10.1080/09670870903377576
Peters, A. (2016). Formulation of nematodes. In T. T. Glare & M. E. Moran-Diez (Eds.), Microbial-Based Biopesticides (pp. 121-135). New York, U.S.: Humana Press.
Poinar Jr., G. O., Thomas, G., Haygood, M., & Nealson, K. H. (1980). Growth and luminescence of the symbolic bacteria associated with the terrestrial nematode, Heterorhabditis bacteriophora. Soil Biology and Biochemistry, 12(1), 5-10. DOI: 10.1016/0038-0717(80)90095-4
Portillo-Aguilar, C., Villani, M. G., Tauber, M. J., Tauber, C. A., & Nyrop, J. P. (1999). Entomopathogenic nematode (Rhabditida: Heterorhabditidae and Steinernematidae) response to soil texture and bulk density. Environmental Entomology, 28(6), 1021-1035. DOI:10.1093/ee/28.6.1021
Powers, T. O., Neher, D. A., Mullin, P., Esquivel, A., Giblin‐Davis, R. M., Kanzaki, N., ... Uribe‐Lorío, L. (2009). Tropical nematode diversity: vertical stratification of nematode communities in a Costa Rican humid lowland rainforest. Molecular Ecology, 18(5), 985-996. DOI: 10.1111/j.1365-294X.2008.04075.x
Rodríguez, D., Torres, M., Uribe, L., & Flores, L. (2009). Susceptibilidad de los estadios L2 y L3 de Phyllophaga elenans a una cepa nativa de Heterorhabditis sp. en condiciones de invernadero. Agronomía Costarricense, 33(2), 171-182.
Rossi, J. P., & Quénéhervé, P. (1998). Relating species density to environmental variables in presence of spatial autocorrelation: a study case on soil nematodes distribution. Ecography, 21(2), 117-123. DOI: 10.1111/j.1600-0587.1998.tb00665.x
Rukazambuga, N. D. T. M., Gold, C. S., & Gowen, S. R. (1998). Yield loss in East African highland banana (Musa spp., AAA-EA group) caused by the banana weevil, Cosmopolites sordidus Germar. Crop Protection, 17(7), 581-589. DOI: 10.1016/S0261-2194(98)00056-8
Rukazambuga, N. D. T. M., Gold, C. S., Gowen, S. R., & Ragama, P. (2002). The influence of crop management on banana weevil, Cosmopolites sordidus (Coleoptera: Curculionidae) populations and yield of highland cooking banana (cv. Atwalira) in Uganda. Bulletin of Entomological Research, 92(5), 413-421. DOI:10.1079/BER2002182
Sandoval, D., & Mata, R. (2014). Base de perfiles de suelos de Costa Rica (en línea): Versión 1.2. San José, Costa Rica: Asociación Costarricense de la Ciencia del Suelo (ACCS).
Seenivasan, N., Prabhu, S., Makesh, S., & Sivakumar, M. (2012). Natural occurrence of entomopathogenic nematode species (Rhabditida: Steinernematidae and Heterorhabditidae) in cotton fields of Tamil Nadu, India. Journal of Natural History, 46(45-46), 2829-2843. DOI: 10.1080/00222933.2012.727216
Shapiro-Ilan, D. I., Gouge, D. H., Piggott, S. J., & Fife, J. P. (2006). Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38(1), 124-133. DOI: 10.1016/j.biocontrol.2005.09.005
Shlens, J. (2014). A tutorial on principal component analysis. Cornell University, arXiv preprint arXiv:1404.1100. Retrieved from https://arxiv.org/pdf/1404.1100.pdf?utm_content=bufferb37df&utm_medium=social&utm_source=facebook.com&utm_campaign=buffer
Shunthirasingham, C., Gouin, T., Lei, Y. D., Ruepert, C., Castillo, L. E., & Wania, F. (2011). Current‐use pesticide transport to Costa Rica's high‐altitude tropical cloud forest. Environmental Toxicology and Chemistry, 30(12), 2709-2717. DOI: 10.1002/etc.671
Stock, S. P. (1995). Natural populations of entomopathogenic nematodes in the Pampean region of Argentina. Nematropica, 25(2), 143-148.
Stock, S. P., Pryor, B. M., & Kaya, H. K. (1999). Distribution of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) in natural habitats in California, USA. Biodiversity & Conservation, 8(4), 535-549. DOI: 10.1023/A:1008827422372
Thomas, G. W. (1982). Exchangeable cations. In A. L. Page (Ed.), Methods of soil analysis. Part 2. Chemical and microbiological properties (pp. 159-165). Madison, Wisconsin USA: Academic Press, American Society of Agronomy Inc y Soil Science of America Inc.
Unidad de Registro de Agroquímicos y Equipos de Aplicación (2019). Costa Rica: Servicio Fitosanitario del Estado. Recuperado de: https://www.sfe.go.cr/DocsStatusRegistro/Plaguicidas_aprobados_Ley_8702.pdf
Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry, 19(6), 703-707. DOI: 10.1016/0038-0717(87)90052-6
Young, I. M., Griffiths, B. S., Robertson, W. M., & McNicol, J. (1998). Nematode (Caenorhabditis elegans) movement in sand as affected by particle size, moisture and the presence of bacteria (Escherichia coli). European Journal of Soil Science, 49(2), 237-241.
Zepeda-Jazo, I., Molina-Ochoa, J., Lezama-Gutiérrez, R., Skoda, S. R., & Foster, J. E. (2014). Survey of entomopathogenic nematodes from the families Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in Colima, México. International Journal of Tropical Insect Science, 34(1), 53-57. DOI: 10.1017/S1742758413000416
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2020 Daniela Vidaurre Barahona, Alejandro Rodríguez Morales, Lidieth Uribe Lorío