Main Article Content

Authors

The greenhouses of Almeria, Spain, represent the largest extension of covered crops in Europe. Larvae of Spodoptera exigua are an important pest in many of these crops and have developed resistance to the majority of insecticides registered in Europe. The nucleopolyhedrovirus (SeMNPV; Baculoviridae) of S. exigua is a native pathogen of this insect. The persistence of the virus is high in the soil of all crops, although its incidence is highest in spring and summer. As many as nine genotypic variants of the virus have been identified in this zone. In terms of pathogenicity, virulence and production of progeny virus occlusion bodies (OBs), mixtures of certain genotypes have greater insecticidal potential than pure genotypes. Production of OBs in vivo can be up to three-fold greater in larvae treated with juvenile hormone analogues. Compounds derived from stilbene have a synergistic activity with OBs in the laboratory and reduce the lethal dosis in the field. The field efficacy of a simple formulation was greater than that offered by treatments of various synthetic insecticides. The virus is currently being mass-produced in a commercial production facility and the process of registration has begun for its use in sweet pepper crops in Almerian greenhouses. The results of these investigations should facilitate the development of SeMNPV as a biological insecticide in other parts of the world, including Latin America.

CABALLERO, P., MURILLO, R., MUÑOZ, D., & WILLIAMS, T. (2009). The nucleopolyhedrovirus of Spodoptera exigua (Lepidoptera: Noctuidae) as a biopesticide: analysis of recent advances in Spain. Revista Colombiana De Entomología, 35(2), 105–115. https://doi.org/10.25100/socolen.v35i2.9200

BARTELT, R. J.; MCGUIRE, M. R.; BLACK, D. A. 1990. Feeding stimulants for the european corn borner (Lepidoptera: Pyrali- dae): additives to starch-based formulation for Bacillus thuringiensis. Environmental Entomology 19: 182-189.

BELDA, J. E. 1994. Biología, ecología y control de Spodoptera exigua en cultivo de pimiento en invernadero. Tesis doctoral, Universidad de Almería, España. 223 p.

BELL, M. R.; KANAVEL, R. F. 1978. Tobacco budworm: deve- lopment of a spray adjuvant to increase effectiveness of a nu- clear polyhedrosis virus. Journal of Economic Entomology 71: 350-352.

BIANCHI, F. J.; SNOEIJING, I.; VAN DER WERF, W.; MANS, R. M.; SMITS, P. H.; VLAK, J. M. 2000. Biological activity of SeMNPV, AcMNPV, and three AcMNPV deletion mutants against Spodoptera exigua larvae (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 75: 28-35.

BURGES, H. D.; JONES, K. A. 1998. Formulation of bacteria, viruses and protozoa to control insects, pp. 33-127. En: Burges, H. D. (Ed.). Formulation of microbial biopesticides: Beneficial microorganisms, nematodes and seed treatments. Kluwer, Dor- drecht, Países Bajos. 496 p.

CABALLERO, P.; ALDEBIS, H. K.; VARGAS-OSUNA E.; SANTIAGO-ÁLVAREZ, C. 1992a. Epizootics caused by a nuclear polyhedrosis virus in populations of Spodoptera exigua in southern Spain. Biocontrol Science and Technology 2: 35-38.

CABALLERO, P.; ZUIDEMA, D.; SANTIAGO-ÁLVAREZ, C.; VLAK, J. M. 1992b. Biochemical and biological characterization of four isolates of Spodoptera exigua nuclear polyhedrosis virus. Biocontrol Science and Technology 2: 145-157.

CABELLO, T. SAÉZ; GÓMEZ, V.; ABAD, M. M.; BELDA, J. J.1990. Problemática fitosanitaria en cultivos hortícolas intensivos de Almería. Agrícola Vergel 104: 640-647.

CERTIS. 2009. Spod-X LC Biological insecticide product webpage. Disponible en: http://www.certisusa.com/products/spod-x- lc-biological-insecticide.htm. Fecha última revisión: 02 marzo 2009.

CHERRY, A.; WILLIAMS, T. 2001. Control de insectos plaga mediante baculovirus, pp. 389-452. En: Caballero, P.; LópezFerber, M.; Williams, T. (Eds.). Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Phytoma-España, S. L., Valencia, España. p. 518.

CHERRY, A. J.; PARNELL, M. A.; GRZYWACZ, D.; JONES, K.A. 1997. The optimization of in vivo nuclear polyhedrosis virus production in Spodoptera exempta (Walker) and Spodoptera exigua (Hubner). Journal of Invertebrate Pathology 70: 50-58.

CUADRADO, I. M.; VIÑUELA, E. 1998. Resistencia a los Pesticidas en los Cultivos Hortícolas. Fundación para la Investigación Agraria en la Provincia de Almería, La Cañada, Almería, España. 212 p.

EUROPEAN COMMISSION. 2006. Annual EU-wide pesticide residues monitoring report. DG ealth and consumers, Bruselas, Bélgica. Disponible en: http:// europa.eu.int/comm/food/fvo/specialreports/ pesticides_index_en.htm. Fecha última revisión: 02 marzo 2009.

FUXA, J. R. 2004. Ecology of insect nucleopolyhedroviruses. Agriculture, Ecosystems and Environment 103: 27-43.

GRANADOS, R. R.; WILLIAMS, K. A. 1986. In vivo infection and replication of baculoviruses, pp. 89-127. En: Granados, R. R.; Federici, B. A. (Eds.). The biology of baculoviruses. Volumen I. CRC Press, Boca Raton, Florida. 275 p.

GRÖNER, A. 1986. Specificity and safety of baculoviruses, pp. 177-202. En: Granados, R. R.; Federici, B. A. (Eds.). The biology of baculoviruses. Volumen I. CRC Press, Boca Raton, Florida. 275 p.

HAMM, J. J. 1999. Interactions in entomology: enhanced infectivity of entomopathogenic viruses by fluorescent brighteners. Journal of Entomological Science 34: 8-16.

IJKEL, W. F.; VAN STRIEN, E. A.; HELDENS, J. G.; BROER, R.; ZUIDEMA, D.; GOLDBACH, R. W.; VLAK, J. M. 1999. Sequence and organization of the Spodoptera exigua multicapsid nucleopolyhedrovirus genome. Journal of General Virology 80: 3289-3304.

JAQUES, R. P. 1985. Stability of insect viruses in the environment, pp. 285-369. En: Maramorosch, K.; Sherman, K. E. (Eds.). Viral Insecticides for Biological Control. Academic Press, New York. p. 809.

JEHLE, J. A.; BLISSARD, G. W.; BONNING, B. C.; CORY, J. S.; HERNIOU, E. A.; ROHRMANN, G. F.; THEILMANN, D. A.; THIEM, S. M.; VLAK, J. M. 2006. On the classification and nomenclature of baculoviruses: a proposal for revision. Archives of Virology 151: 1257-1266.

JONES, K. A.; BURGES, H. D. 1998. Technology of formulation and application, pp. 7-30. En: Burges, H. D. (Ed.). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. Kluwer, Dordrecht, Países Bajos. 496 p.

JUNTA DE ANDALUCÍA. 2006. Anuario de estadísticas agrarias y pesqueras del año 2006. Consejería de Agricultura y Pesca, Junta de Andalucía, España. Disponible en: http://www.juntadeandalucia.es/agriculturaypesca/portal/opencms/portal/DGPAgraria/Estadisticas/estadisticasagrarias?entrada=servicios&servici o=201 Fecha última revisión: 02 marzo 2009.

KILLICK, H. J.; WARDEN, S. J. 1991. Ultraviolet penetration of pine trees and insect virus survival. Entomophaga 36: 87-94.

KOLODNY-HIRSCH, D. M.; SITCHAWAT, T.; JANSARI, J.; CHENRCHAIVACHIRAKUL, A.; KETUNUTI, U. 1997. Field evaluation of a commercial formulation of the Spodoptera exigua (Lepidoptera: Noctuidae) nuclear polyhedrosis virus for control of beet armyworm on vegetable crops in Thailand. Biocontrol Science and Technology 7: 475-488.

LACASA, A. 2004. Manejo de plagas en el cultivo de pimiento en invernaderos mediterráneos, pp. 279-292). En: Fernández, J. M. (Ed.). Producción Hortícola y Seguridad Alimentaria. Ediciones Agrotecnológicas, Madrid, España. 432 p.

LARA, L.; URBANEJA, A. 2002. Control biológico de plagas en pimiento en la provincia de Almería. Horticultura 165: 86-90.

LASA-COVARRUBIAS, R. 2007. Formulation and efficacy of Spodoptera exigua nucleopolyhedrovirus as a biological insecticide for beet armyworm control in the greenhouses of southern Spain. Tesis doctoral, Departamento de Producción Agraria, Universidad Pública de Navarra, Pamplona, España.

LASA, R.; CABALLERO, P.; WILLIAMS, T. 2007a. Juvenil hormone analogs greatly increase the production of a nucleopolyhedrosis. Biological Control 41: 389-396.

LASA, R.; PAGOLA, I.; IBAÑEZ, I.; BELDA, J. E.; WILLIAMS, T.; CABALLERO, P. 2007b. Efficacy of Spodoptera exigua multiple nucleopolyhedrovirus as a biological insecticide for beet armyworm control in greenhouses of southern Spain. Biocontrol Science and Technology 17: 221-232.

LASA, R.; RUIZ-PORTERO, C.; ALCÁZAR, D.; BELDA, J. E.; CABALLERO, P.; WILLIAMS, T. 2007c. Efficacy of optical brightener formulations of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) as a biological insecticide in greenhouses in southern Spain. Biological Control 40: 8996.

LASA, R.; WILLIAMS, T.; CABALLERO, P. 2008. Insecticidal properties and microbial contaminants in Spodoptera exigua nuclopolyhedrovirus (Baculoviridae) stored at different temperatures. Journal of Economic Entomology 101: 42-49.

MASCARENHAS, V. J.; GRAVES, J. B.; LEONARD, B. R.; BURRIS, E. 1998. Susceptibility of field populations of beet armyworm (Lepidoptera: Noctuidae) to commercial and experimental insecticides. Journal of Economic Entomology 91: 827-833.

MOSCARDI, F. 1999. Assessment of the application of baculoviruses for control of Lepidoptera. Annual Review of Entomology 44: 257-289.

MOULTON, J. K.; PEPPER, D. A.; DENNEHY, J.; DUGGER, P.; RICHTER, D. 1999. Studies of resistance of beet armyworm (Spodoptera exigua) to spinosad in field populations from the southern USA and southeast Asia. Proceedings of the Beltwide Cotton Conferences. Orlando, Florida 2: 884-887.

MOULTON, J. K.; PEPPER, D. A.; JANSSON, R. K.; DENNEHY, T. J. 2002. Pro-active management of beet armyworm (Lepidoptera: Noctuidae) resistance to tebufenozide and methoxyfenozide: baseline monitoring risk assessment, and isolation of resistance. Journal of Economic Entomology 95: 414-424.

MUÑOZ, D.; CABALLERO, P. 2000. Persistence and effects of parasitic genotypes in a mixed population of the Spodoptera exigua nucleopolyhedrovirus. Biological Control 19: 259-264.

MUÑOZ, D.; CABALLERO, P. 2001. Diversidad natural de los baculovirus, pp. 95-118. En: Caballero, P.; López-Ferber, M.; Williams, T. (Eds.). Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Phytoma-España, Valencia, España. 518 p.

MUÑOZ, D.; CASTILLEJO, J. I.; CABALLERO, P. 1998. Naturally occurring deletion mutants are parasitic genotypes in a wildtype nucleopolyhedrovirus population of Spodoptera exigua. Applied and Environmental Microbiology 64: 4372-4377.

MUÑOZ, D.; MURILLO, R.; KRELL, P. J.; VLAK, J. M.; CABALLERO, P. 1999. Four genotypic variants of a Spodoptera exigua nucleopolyhedrovirus (Se-SP2) are distinguishable by a hypervariable genomic region. Virus Research 59: 61-74.

MURILLO, R.; MUÑOZ, D.; CABALLERO, P. 2003a. Host range and biological activity of three Spodoptera nucleopolyhedrovirus genotypic variants and the effect of Tinopal LPW on the most active variant. International Journal of Pest Management 49: 147-153.

MURILLO, R.; LASA, R.; GOULSON, D.; WILLIAMS, T.; MUÑOZ, D.; CABALLERO, P. 2003b. Effect of Tinopal LPW on the insecticidal properties and genetic stability of the nucleopolyhedrovirus of Spodoptera exigua (Lepidoptera: Noctuidae). Journal of Economic Entomology 96: 1668-1674.

MURILLO, R.; ELVIRA, S.; MUÑOZ, D.; WILLIAMS, T.; CABALLERO, P. 2006a. Genetic and phenotypic variability in Spodoptera exigua nucleopolyhedrovirus isolates from greenhouse soils in southern Spain. Biological Control 38: 157-165.

MURILLO, R.; MUÑOZ, D.; WILLIAMS, T.; MUGETA, N.; CABALLERO, P. 2006b. Application of the PCR-RFLP method for the rapid differentiation of Spodoptera exigua nucleopolyhedrovirus genotypes. Journal of Virological Methods 135: 1-8.

MURILLO, R.; RUIZ-PORTERO, C.; ALCÁZAR, D.; BELDA, J.E.; WILLIAMS, T.; CABALLERO, P. 2007. Abundance and genetic structure of nucleopolyhedrovirus populations in greenhouse soil reservoirs. Biological Control 42: 216-552.

PINNOCK, D. E.; BRAND, J. R. 1981. A quantitative approach to the ecology of the use of pathogens for insect control, pp. 655-665. En: Burges, H. D. (Ed.). Microbial Control of Pests and Diseases. Academic Press, New York. 949 p.

RODGERS, P. B. 1993. Potential of biopesticides in agriculture. Pesticide Science 39: 117-129.

SHAPIRO, M. 1986. In vivo production of baculovirus, pp. 31-62. En: Granados, R. R.; Federici, B. A. (Eds.). The Biology of Baculoviruses. CRC Press, Boca Raton, Florida. 1424 p.

SHAPIRO, M.; ROBERTSON, J. L. 1992. Enhancement of gypsy moth (Lepidoptera: Lymantriidae) baculovirus activity by optical brighteners. Journal of Economic Entomology 85: 1120-1124.

SMAGGHE, G.; AUDA, M.; VANLAECKE, K.; DEGHEELE, D. 1997. Significance of penetration and metabolism on topical toxicity of diflubenzuron in Spodoptera littoralis and Spodoptera exigua. Entomologia Experimentalis et Applicata 82: 255-260.

SMAGGHE, G.; PINEDA, S.; CARTON, B.; DEL ESTAL, P.; BUDIA, F.; VIÑUELA, E. 2003. Toxicity and kinetics of methoxyfenozide in greenhouse-selected Spodoptera exigua (Lepidoptera: Noctuidae). Pest Management Science 59: 1203-1209. SMITS, P. H. 1987. Nuclear polyhedrosis virus as biological control agent of Spodoptera exigua., Tesis doctoral, Wageningen Agricultural University, Wageningen, Países Bajos.

SMITS, P. H.; VLAK, J. M. 1988. Biological activity of Spodoptera exigua nuclear polyhedrosis virus against S. exigua larvae. Journal of Invertebrate Pathology 51: 107-114.

SMITS, P. H.; VLAK. J. M. 1994. Registration of the first viral insecticide in the Netherlands: the development of Spod-X based on Spodoptera exigua nuclear polyhedrosis virus. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent 59/2A: 385-392.

SMITS, P. H.; VAN DE VRIE, M.; VLAK, J. M. 1987. Nuclear polyhedrosis virus for control of Spodoptera exigua larvae in glasshouse crops. Entomologia Experimentalis et Applicata 43: 73-80.

STANSLY, P. A.; CALVO, F. J.; URBANEJA, A. 2005. Augmentative biological control of Bemisia tabaci biotype ‘‘Q’’ in Spanish greenhouse pepper production using Eretmocerus spp. Crop Protection 24: 829-835.

TORRES-VILA, L. M.; RODRIGUES MOLINA, M. C.; LACASA, A.; PALO, E.; MEJÍAS, M.; GUERRERO, M. 1998. Susceptibilidad de 20 insecticidas de Helicoverpa armígera y Spodoptera exigua en la vega del Guadiana (Extremadura). Boletín de Sanidad Vegetal Plagas 24: 353-362.

THEILMANN, D. A.; BLISSARD, G. W.; BONNING, B.; JEHLE, J. A.; O’REILLY, D. R.; ROHRMANN, G. F.; THIEM, S.; VLAK, J. M. 2005. Baculoviridae, pp. 177-185. En: Fauquet, C. M.; Mayo, M. A.; Maniloff, J.; Desselberger, U.; Ball, L. A. (Eds.). Eighth Report of the International Committee on Taxonomy of Viruses, Elsevier, San Diego, California. 1259 p.

WANG, P.; GRANADOS, R. R. 2000. Calcofluor disrupts the midgut defense system in insects. Insect Biochemistry and Molecular Biology 30: 135-143.

WILLIAMS, T.; CISNEROS, J. 2001. Formulación y aplicación de los baculovirus bioinsecticidas, pp. 313-372. En: Caballero, P.; López-Ferber, M.; Williams, T. (Eds.). Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Phytoma-España, S. L., Valencia, España 518 p.