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Biological characterization and mating compatibility of Helicoverpa gelotopoeon (D.) (Lepidoptera: Noctuidae) populations from different regions in Argentina

Published online by Cambridge University Press:  27 June 2017

M.I. Herrero ,
S.V. Fogliata ,
A. Vera ,
A. Casmuz ,
D. Sosa Gómez ,
A.P. Castagnaro ,
G. Gastaminza  and
M.G. Murúa
M.I. Herrero
Affiliation:
Instituto de Tecnología Agroindustrial del Noroeste Argentino, Estación Experimental Agroindustrial Obispo Colombres, Consejo Nacional de Investigaciones Científicas y Técnicas (ITANOA-EEAOC-CONICET), Las Talitas 4001, Tucumán, Argentina
S.V. Fogliata
Affiliation:
Instituto de Tecnología Agroindustrial del Noroeste Argentino, Estación Experimental Agroindustrial Obispo Colombres, Consejo Nacional de Investigaciones Científicas y Técnicas (ITANOA-EEAOC-CONICET), Las Talitas 4001, Tucumán, Argentina
A. Vera
Affiliation:
EEAOC, Las Talitas 4001, Tucumán, Argentina
A. Casmuz
Affiliation:
EEAOC, Las Talitas 4001, Tucumán, Argentina
D. Sosa Gómez
Affiliation:
EMBRAPA Soja, Rodovia João Strass, S/N, Acesso Orlando Amaral, CP 231, Londrina, PR 86001-970, Brazil
A.P. Castagnaro
Affiliation:
Instituto de Tecnología Agroindustrial del Noroeste Argentino, Estación Experimental Agroindustrial Obispo Colombres, Consejo Nacional de Investigaciones Científicas y Técnicas (ITANOA-EEAOC-CONICET), Las Talitas 4001, Tucumán, Argentina
G. Gastaminza
Affiliation:
EEAOC, Las Talitas 4001, Tucumán, Argentina
M.G. Murúa*
Affiliation:
Instituto de Tecnología Agroindustrial del Noroeste Argentino, Estación Experimental Agroindustrial Obispo Colombres, Consejo Nacional de Investigaciones Científicas y Técnicas (ITANOA-EEAOC-CONICET), Las Talitas 4001, Tucumán, Argentina
*
*Author for correspondence Phone: (54) 381-521000 Fax: (54) 381-521000 int 154 E-mail: [email protected]
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Abstract

Helicoverpa gelotopoeon, the South American bollworm, is a polyphagous pest of the Heliothinae complex that causes damage to soybean, cotton, and chickpea crops. Some species within this complex have developed resistance to genetically modified crops and insecticides, which has led to increased interest in their genetic diversity and population structure. The objective of this study was to characterize biological and reproductive parameters of two populations of H. gelotopoeon collected in two different provinces of Argentina. Intra- and inter-population crosses revealed that H. gelotopoeon populations from both regions of Argentina did not present evidence of pre-zygotic and post-zygotic incompatibility, suggesting that Tucumán and Córdoba populations of H. gelotopoeon belong to a single wide-ranging species. Our data support the occurrence of substantial gene flow between H. gelotopoeon populations, probably due to the widely documented, long-range migratory capacity of Heliothinae species.

Keywords

South American bollwormbiologyreproductive compatibilityfitnessinsect resistance management
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 1 , February 2018 , pp. 108 - 115
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Copyright © Cambridge University Press 2017 

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References

Ali, A., Choudhury, R.A., Ahmad, Z., Rahman, F., Khan, F.R. & Ahmad, S.K. (2009) Some biological characteristics of Helicoverpa armigera on chickpea. Tunisian Journal of Plant Protection 4, 99–106.Google Scholar
Álvarez Hernández, U., Pérez, L., González, M., Cruz, A., Gómez, J. & Álvarez, J.M. (2010) Biología de Heliothis virescens (Fabricius) en garbanzo (Cicer arietinum L.). Centro Agrícola 37, 89–92.Google Scholar
Arghand, A., Naseri, B., Razmjou, J., Hassanpour, M. & Rahimi Namin, F. (2014) Comparative biological parameters of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) on various corn hybrids. Journal of Entomological Society of Iran 34, 33–35.Google Scholar
Armes, N.J., Jadhav, D.R. & DeSouza, K.R. (1996) A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent. Bulletin of Entomological Research 86, 499–514.Google Scholar
Arneodo, J.D., Balbi, E.I., Flores, F. & Sciocco, A. (2015) Molecular identification of Helicoverpa armigera (Lepidoptera: Noctuidae: Heliothinae) in Argentina and development of a novel PCR-RFLP method for its rapid differentiation from H. zea and H. gelotopoeon . Journal of Economic Entomology 108, 2505–2510.Google Scholar
Asokan, R., Rebijith, K.B., Krishna Kumar, N.K. & Manamohan, M. (2012) Genetic diversity of tomato fruit borer, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) inferred from mitochondrial cytochrome oxidase-I (mtCO-I). Pest Management in Horticultural Ecosystems 18, 29–34.Google Scholar
Behere, G.T., Tay, W.T., Russel, D.A., Heckel, D.G., Appleton, B.R., Kranthi, K.R. & Batterham, P. (2007) Mitochondrial DNA analysis of field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) and of its relationship to H. zea . BMC Evolutionary Biology 7, 117.Google Scholar
Bird, L.J. & Downes, S.J. (2014) Toxicity and cross-resistance of insecticides to Cry2Ab-resistant and Cry2Ab-susceptible Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 107, 1923–1930.CrossRefGoogle ScholarPubMed
Blanco, C.A., Chiaravalle, W., Dalla-Rizza, M., Farias, J.R., García-Degano, M.F., Gastaminza, G., Mota-Sanchez, D., Murúa, M.G., Omoto, C., Pieralisi, B.K., Rodríguez, J., Rodríguez-Maciel, J.C., Terán-Santofimio, H., Terán-Vargas, A.P., Valencia, S.J. & Willink, E. (2016) Current situation of pests targeted by Bt crops in Latin America. Current Opinion in Insect Science 15, 131–138.Google Scholar
Bolsa de Cereales (2016) Panorama Agrícola Semanal. Estimaciones Agrícolas. Relevamiento al 21/07/2016. Available online at http://www.bolsadecereales.com.ar (last accessed 7 March 2017).Google Scholar
Brévault, T., Tabashnik, B.E. & Carrière, Y. (2015) A seed mixture increases dominance of resistance to Bt cotton in Helicoverpa zea . Scientific Reports 5, 9807. Doi: 10.1038/srep09807.Google Scholar
Callahan, P.S. (1958) Behavior of the imago of the corn earworm, Heliothis zea (Boddie), with special reference to emergence and reproduction. Annals of the Entomological Society of America 51, 271–283.Google Scholar
Casmuz, A.S., Cazado, L.E., Scalora, F.S., Tuzza, M.F., Fernández, R.A., Fadda, C., Fadda, L.A., Dami, L., Colledani Toranzo, A., Gómez, C.H., De Felice, M., Vera, M.A. & Gastaminza, G. (2014) Evaluación de diferentes alternativas para el control del complejo de plagas del cultivo de soja. pp. 137–142 in Devani, M.R., Ledesma, F. & Sánchez, J.R. (Eds) El cultivo de la soja en el noroeste argentino. Campaña 2013–2014. Publicación Especial Soja EEAOC N° 50, Las Talitas, Tucumán, Argentina, EEAOC. Available online at http://www.eeaoc.org.ar/publicaciones/categoria/16/461/10Plagas.html (last accessed 7 March 2017).Google Scholar
Cazado, L.E., Casmuz, A.S., Scalora, F.S., Fadda, C., Fernández, R.A., Tuzza, M.F., Fadda, L.A., Dami, L., Colledani Toranzo, A., Jadur, A., Vera, A., Gastaminza, G., López, R. & Ruiz, S. (2014) Comportamiento de la soja Bt frente a las principales plagas insectiles y depredadores en el Noroeste Argentino (NOA). pp. 153–161 in Devani, M.R., Ledesma, F. & Sánchez, J.R. (Eds) El cultivo de la soja en el noroeste argentino. Campaña 2013–2014. Publicación Especial Soja EEAOC N° 50, Las Talitas, Tucumán, Argentina, EEAOC. Available online at http://www.eeaoc.org.ar/publicaciones/categoria/16/463/12Plagas-vs-Bt.html (last accessed 7 March 2017).Google Scholar
Colvin, J., Cooter, R.J. & Patel, S. (1994) Laboratory mating behavior and compatibility of Helicoverpa armigera (Lepidoptera: Noctuidae) originating from different geographical regions. Journal of Economic Entomology 87, 1502–1506.Google Scholar
Czepak, C., Albernaz, K.C., Vivan, L.M., Guimarães, H.O. & Carvalhais, T. (2013) First reported occurrence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesquisa Agropecuária Tropical 43, 110–113. Available online at http://www.revistas.ufg.br/index.php/pat/article/view/23691/13928.Google Scholar
Domingues, F.A., Silva-Brandão, K.L., Abreu, A.G., Perera, O.P., Blanco, C.A., Cônsoli, F.L. & Omoto, C. (2012) Genetic Structure and gene flow among Brazilian populations of Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology 105, 2136–2146.Google Scholar
Endersby, N.M., Hoffmann, A.A., McKechnie, S.W. & Weeks, A.R. (2007) Is there genetic structure in populations of Helicoverpa armigera from Australia? Entomologia Experimentalis et Applicata 122, 253–263.Google Scholar
Farrow, R.A. & Daly, J.C. (1987) Long range movements as an adaptive strategy in the genus Heliothis (Lepidoptera: Noctuidae): a review of its occurrence and detection in four pest species. Australian Journal of Zoology 35, 1–24.Google Scholar
Fichetti, P., Avalos, S., Mazzuferi, V. & Carreras, J. (2009) Lepidópteros asociados al cultivo de garbanzo (Cicer arietinum L.) en Córdoba (Argentina). Boletín de Sanidad Vegetal, Plagas 35, 49–58.Google Scholar
Fogliata, S.V., Vera, A., Gastaminza, G., Cuenya, M.I., Zucchi, M.I., Willink, E., Castagnaro, A.P. & Murúa, M.G. (2016) Hybrid sterility between two populations of Diatraea saccharalis (Lepidoptera: Crambidae) (F.) from different host plant species and regions in Argentina. Bulletin of Entomological Research 26, 1–7.Google Scholar
Forrester, N.W. (1990) Designing, implementing and servicing an insecticide resistance management strategy. Pesticide Science 28, 167–179.Google Scholar
Forrester, N.W., Cahill, M., Bird, L.J. & Layland, J.K. (1993) Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Bulletin of Entomological Research 1, 1–132.Google Scholar
Gao, Y., Wu, K., Gould, F. & Shen, Z. (2009) Cry2Ab tolerance response of Helicoverpa armigera (Lepidoptera: Noctuidae) populations from Cry1Ac cotton planting region. Journal of Economic Entomology 102, 1217–1223.Google Scholar
Giolo, F.P., Rossato Busato, G., Silveira Garcia, M., Manzoni, C.G., Bernardi, O. & Zart, M. (2006) Biologia de Helicoverpa zea (Boddie, 1850) (Lepidoptera: Noctuidae) em duas dietas artificiais. Revista Brasileira de Agrociência 12, 167–171.Google Scholar
Gould, F., Anderson, A., Reynolds, A., Bumgarner, L. & Moar, W. (1995) Selection and genetic analysis of a Heliothis virescens (Lepidoptera: Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. Journal of Economic Entomology 88, 1545–1559.Google Scholar
Gregg, P.C., Fitt, G.P., Zalucki, M.P. & Murray, D.A.H. (1995) Insect migration in an arid continent. II. Helicoverpa spp. in eastern Australia. pp. 151–172 in Drake, V.A. & Gatehouse, A.G. (Eds) Insect Migration: Tracking Resources Through Space and Time. Cambridge, Cambridge University Press.Google Scholar
Groot, A.T., Classen, A., Inglis, O., Blanco, C.A., López, J., Vargas, A.T., Schal, C., Heckel, G. & Schöfl, G. (2011) Genetic differentiation across North America in the generalist moth Helicoverpa virescens and the specialist H. subflexa . Molecular Ecology 20, 2676–2692.Google Scholar
Han, Q. & Caprio, M.A. (2002) Temporal and spatial patterns of allelic frequencies in cotton bollworm (Lepidoptera: Noctuidae). Environmental Entomology 31, 462–468.Google Scholar
Han, Q. & Caprio, M.A. (2004) Evidence from genetic markers suggests seasonal variation in dispersal in Heliothis virescens (Lepidoptera: Noctuidae). Environmental Entomology 33, 1223–1231.Google Scholar
Hardee, D.D., Adams, L.C., Solomon, W.L. & Sumerford, D.V. (2001) Tolerance to Cry1Ac in Populations of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae): Three-Year Summary. Journal of Agricultural and Urban Entomology 18, 187–197.Google Scholar
Hartstack, A.W., Lopez, J.D., Muller, R.A., Sterling, W.L., King, E.G., Witz, J.A. & Eversull, A.C. (1982) Evidence of long range migration of Heliothis zea (Boddie) into Texas and Arkansas. Southwestern Entomologist 7, 188–201.Google Scholar
Iannone, N. & Leiva, P. (1993) Bioecología, umbrales de acción y control de la isoca bolillera Heliothis gelotopoeon Dyar en soja. Carpeta de producción vegetal. Tomo 3, Serie soja, Información 114. Buenos Aires, Argentina, EEA Pergamino.Google Scholar
InfoStat. (2006) InfoStat Version 2006, Manual del Usuario. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. 1st edn. Argentina, Editorial Brujas.Google Scholar
Joyce, A.L., White, W.H., Nuessly, G.S., Solis, M.A., Scheffer, S.J., Lewis, M.L. & Medina, R.F. (2014) Geographic population structure of the sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae), in the southern United States. PLoS ONE 9(10): e110036. Doi: 10.1371/journal.pone.0110036.Google Scholar
Khiaban, N.G., Hejazi, M.S., Irani-Nejad, K.H., Mohammadi, S.A. & Khaghaninia, S. (2010) Genetic variability of geographical populations of the bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), in west and northwest of Iran. Munis Entomology & Zoology 5, 670–676.Google Scholar
Korman, A.K., Mallet, J., Goodenough, J.L., Graves, J.B., Hayes, J.L., Hendricks, D.E., Luttrell, R., Pair, S.D. & Wall, M. (1993) Population structure in Heliothis virescens (Lepidoptera, Noctuidae): an estimate of gene flow. Annals of the Entomological Society of America 86, 182–188.Google Scholar
Kriticos, D.J., Ota, N., Hutchison, W.D., Beddow, J., Walsh, T., Tay, W.T., Borchert, D.M., Paula-Moreas, S.V., Czepak, C. & Zalucki, M.P. (2015) The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PLoS ONE 10, e0133224.Google Scholar
Kruskal, W.H. & Wallis, W.A. (1952) Use of ranks on one-criterion variance analysis. Journal of the American Statistical Association 47, 583–621.Google Scholar
Laster, M.L. & Sheng, C.F. (1995) Search for hybrid sterility for Helicoverpa zea in crosses between the North American H. zea and H. armigera (Lepidoptera: Noctuidae) from China. Journal of Economic Entomology 88, 1288–1291.Google Scholar
Lehmann, E.L. (1975) Nonparametrics: Statistical Methods Based on Ranks. San Francisco, USA, Holden-Day, Inc. Google Scholar
Leite, N.A., Alves-Pereira, A., Corrêa, A.S., Zucchi, M.I. & Omoto, C. (2014) Demographics and genetic variability of the new world bollworm (Helicoverpa zea) and the old world bollworm (Helicoverpa armigera) in Brazil. PLoS ONE 9(11), e113286. doi: 10.1371/journal.pone.0113286.Google Scholar
Li, G.P., Wu, K.M., Gould, F., Wang, J.K., Miao, J., Gao, X.W. & Guo, Y.Y. (2007) Increasing tolerance to Cry1Ac cotton from cotton bollworm, Helicoverpa armigera, was confirmed in Bt cotton farming area of China. Ecological Entomology 32, 366–375.Google Scholar
Liu, F., Xu, Z., Zhu, Y.C., Huang, F., Wang, Y., Li, H., Gao, C., Zhou, W. & Shen, J. (2010) Evidence of field-evolved resistance to Cry1Ac-expressing Bt cotton in Helicoverpa armigera (Lepidoptera: Noctuidae) in northern China. Pest Management Science 66, 155–61.Google Scholar
Liu, Z., Li, D., Gong, P.Y. & Wu, K.J. (2004) Life table studies of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), on different host plants. Environmental Entomology 33, 1570–1576.Google Scholar
Lopez-Edwards, M., Hernandez Mendoza, J.L., Pescador Rubio, A., Molina Ochoa, J., Lezama Gutierrez, R., Hamm, J.J. & Wiseman, B.R. (1999) Biological differences between five populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected from corn in Mexico. Florida Entomologist 82, 254–262.CrossRefGoogle Scholar
MacRae, T.C., Baur, M.E., Boethel, D.J., Fitzpatrick, B.J., Gao, A., Gamundi, J.C., Harrison, L.A., Kabuye, V.T., McPherson, R.M., Miklos, J.A., Paradise, M.S., Toedebusch, A.S. & Viegas, A. (2005) Laboratory and field evaluations of transgenic soybean exhibiting high-dose expression of a synthetic Bacillus thuringiensis Cry 1A gene for control of Lepidoptera. Journal of Economic Entomology 98, 577–587.Google Scholar
Mahon, R.J., Olsen, K.M., Garsia, K.S. & Young, S.R. (2007) Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Journal of Economic Entomology 100, 894–902.Google Scholar
Méndez Barceló, A. (2003) Aspectos biológicos sobre Heliothis virescens (Fabricius) (Lepidoptera: Noctuidae) en la empresa municipal agropecuaria Antonio Guiteras de la zona norte de la provincia de Las Tunas. Fitosanidad 7, 21–25.Google Scholar
Mironidis, G.K. (2014) Development, survivorship and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under fluctuating temperatures. Bulletin of Entomological Research 104, 751–764.Google Scholar
Mitter, C., Poole, R.W. & Matthews, M. (1993) Biosystematics of the Heliothinae (Lepidoptera: Noctuidae). Annual Review of Entomology 38, 207–225.Google Scholar
Monsanto. (2014) Beneficios de INTACTA RR2 PRO, 7p. Available online at http://www.intactarr2pro.com.ar (last accessed 7 March 2017).Google Scholar
Murúa, M.G., Virla, E. & Defagó, V. (2003) Evaluación de cuatro dietas artificiales para la cría de Spodoptera frugiperda (Lepidoptera: Noctuidae) destinada a mantener poblaciones experimentales de himenópteros parasitoides. Boletín de Sanidad Vegetal Plagas 29, 43–51.Google Scholar
Murúa, M.G., Vera, M.T., Abraham, S., Juaréz, M.L., Prieto, S., Head, G.P. & Willink, E. (2008) Fitness and mating compatibility of Spodoptera frugiperda (Lepidoptera: Noctuidae) populations from different host plant species and regions in Argentina. Annals of the Entomological Society of America 101, 639–649.Google Scholar
Murúa, M.G., Scalora, F.S., Navarro, F.R., Cazado, L.E., Casmuz, A., Villagrán, M.E., Lobos, E. & Gastaminza, G. (2014) First record of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Argentina. Florida Entomologist 97, 854–856.Google Scholar
Murúa, M.G., Cazado, L.E., Casmuz, A.S., Herrero, M.I., Villagrán, M.E., Vera, A., Sosa-Gómez, D.R., & Gastaminza, G. (2016) Species from the Heliothinae complex (Lepidoptera: Noctuidae) in Tucumán, Argentina, an update of geographical distribution of Helicoverpa armigera . Journal of Insect Science 16, 1–7.Google Scholar
Naseri, B., Fathipour, Y., Moharramipour, S. & Hosseininaveh, V. (2009) Comparative life history and fecundity of Helicoverpa armigera (Lepidoptera: Noctuidae) on different soybean varieties. Entomological Science 2, 147–154.Google Scholar
Navarro, F.R., Saini, E.D. & Leiva, P.D. (2009) Clave pictórica de polillas de interés agrícola, agrupadas por relación de semejanza. Primera edición. Instituto Nacional de tecnología agropecuaria, INTA. Estación experimental agropecuaria Pergamino y IMyZA – CNIA Castelar, Facultad de Cs Naturales e Instituto ‘Miguel Lillo’, Universidad Nacional de Tucumán, Bs As, Argentina. 100pp.Google Scholar
Navarro, R.V. (1987) Comportamiento de emergencia y reproducción del gusano del jojoto (Heliothis zea Boddie). Agronomía Tropical 37, 55–61.Google Scholar
Nibouche, S., Bues, R., Toubon, J.F. & Poitout, S. (1998) Allozyme polymorphism in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae): comparison of African and European populations. Heredity 80, 438–445.Google Scholar
Pashley, D.P. & Martin, J.A. (1987) Reproductive incompatibility between host strains of the fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 80, 731–733.CrossRefGoogle Scholar
Pashley, D.P., Hardy, T.N., Hammond, A.M. & Mihm, J.A. (1990) Genetic evidence for sibling species within the sugarcane borer (Lepidoptera: Pyralidae). Annals of the Entomological Society of America 83, 1048–1053.Google Scholar
Pastrana, J.A. (2004) Los lepidópteros Argentinos, sus plantas hospedadoras y otros sustratos alimenticios. Buenos Aires, Sociedad Entomológica Argentina ediciones. 334 pp.Google Scholar
Perera, O.P. & Blanco, C.A. (2011) Microsatellite variation in Helicoverpa zea (Boddie) populations in the Southern United States. Southwestern Entomologist 36, 271–286.CrossRefGoogle Scholar
Pérez Contreras, T. (1999) La especialización en los insectos fitógagos: Una regla más que una excepción. Boletín S.E.A. 26, 759–776.Google Scholar
Pérez, J.C. & Suris, M. (2012) Ciclo de vida y reproducción de Heliothis virescens (F.) (Lepidoptera: Noctuidae) sobre garbanzo. Revista de Protección Vegetal 27, 85–89.Google Scholar
Pietrantonio, P.V., Junek, T.A., Parker, R., Mott, D., Siders, K., Troxclair, N., Vargas-Camplis, J., Westbrook, J.K. & Vassiliou, V.A. (2007) Detection and evolution of resistance to the pyrethroid cypermethrin in Helicoverpa zea (Lepidoptera: Noctuidae) populations in Texas. Environmental Entomology 36, 1174–1188.Google Scholar
Pogue, M.G. (2013) Revised status of Chloridea Duncan and (Westwood), 1841, for the Heliothis virescens species group (Lepidoptera: Noctuidae: Heliothinae) based on morphology and three genes. Systematic Entomology 38, 523–542.CrossRefGoogle Scholar
Reisig, D.D. & Reay-Jones, F.P.F. (2015) Inhibition of Helicoverpa zea (Lepidoptera: Noctuidae) growth by transgenic corn expressing Bt toxins and development of resistance to Cry1Ab. Environmental Entomology 44, 1275–85.Google Scholar
Rhainds, M., Gries, G. & Min, M.M. (1999) Size- and density-dependent reproductive success of bagworms, Metisa plana . Entomologia Experimentalis et Applicata 91, 375–383.Google Scholar
Roehrdanz, R.L., Lopez, J.D., Loera, J. & Hendricks, D.E. (1994) Limited mitochondrial-DNA polymorphism in North-American populations of Heliothis virescens (Lepidoptera, Noctuidae). Annals of the Entomological Society of America 87, 856–866.Google Scholar
Rull, J., Abraham, S., Kovaleski, A., Segura, D.F., Islam, A., Wornoayporn, V., Dammalage, T., Santo Tomas, U. & Vera, M.T. (2012) Random mating and reproductive compatibility among Argentinean and southern Brazilian populations of Anastrepha fraterculus (Diptera: Tephritidae). Bulletin of Entomological Research 102, 435–443.Google Scholar
Scalora, F., Casmuz, A., Cazado, L., Socías, G., Tolosa, G., Aralde, M., Aybar Guchea, M., Fadda, L., Gómez, M., Gómez, H., Montaldi, T., Gastaminza, G., Willink, E. & Rodríguez, W. (2012) Evaluación de diferentes insecticidas para el control de la oruga bolillera, H. gelotopoeon Dyar (Lepidoptera: Noctuidae). pp. 147–15 in Devani, M.R., Ledesma, F. & Sánchez, J.R. (Eds) El cultivo de la soja en el noroeste argentino. Campaña 2011/2012. Publicación Especial EEAOC n° 45. Las Talitas, Tuc., Argentina, EEAOC. Available online at http://www.eeaoc.org.ar/upload/publicaciones/archivos/286/20121122085717000000.pdf. (last accessed 7 March 2017).Google Scholar
SENAVE. Servicio Nacional de Calidad y Sanidad Vegetal y de Semillas. (2013). Alerta tras ingreso de peligrosa plaga agrícola. Color ABC, 17 October 2013. Available online at http://www.abc.com.py/edicion-impresa/economia/senaveen-alerta-tras-ingreso-de-peligrosa-plaga-agricola-629240.html (last accessed 7 march 2017).Google Scholar
Sharma, K.C., Bhardwaj, S.C. & Sharma, G. (2011) Systematic studies, life history and infestation by Helicoverpa armigera on tomato in semi arid region of Rajastan. Biological Forum. An International Journal 3, 52–56.Google Scholar
Simmons, A.M. & Lynch, R.E. (1990) Egg production and adult longevity of Spodoptera frugiperda, Helicoverpa zea (Lepidoptera: Noctuidae), and Elasmopalpus lignosellus (Lepidoptera: Pyralidae) on selected adult diets. Florida Entomologist 73, 665–671.Google Scholar
Specht, A., Sosa-Gómez, D.R., Paula-Moraes, S.V. & Yano, S.A.C. (2013) Identificação morfológica e molecular de Helicoverpa armigera (Lepidoptera: Noctuidae) e ampliação de seu registro de ocorrência no Brasil. Pesquisa Agropecuaria Brasileira 48, 689–692.Google Scholar
Tabashnik, B.J., Van Rensburg, J.B.J. & Carriere, R.E. (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology 102, 2011–2025.Google Scholar
Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P. & Behere, G.T. (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8, e80134.Google Scholar
Tay, W.T., Mahon, R.J., Heckel, D.G., Walsh, T.K., Downes, S., James, W.J., Lee, S.F., Reineke, A., Williams, A.K. & Gordon, K.H.J. (2015) Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily A protein. PLoS Genetics 11, e1005534.Google Scholar
Urretabizkaya, N., Vasicek, A. & Saini, E. (2010) Insectos perjudiciales de importancia agronómica. I. Lepidópteros. Instituto Nacional de Tecnología Agropecuaria (INTA). Buenos Aires, Argentina, Universidad Nacional de Lomas de Zamora y Universidad Nacional de La Plata. 77 pp.Google Scholar
Velasco de Stacul, M., Barral, J.M. & Orfila, R.N. (1969) Taxonomía, especificidad y caracteres biológicos diferenciados del complejo de especies denominadas ‘oruga del capullo’ del algodón, ‘oruga de la espiga’ del maíz, ‘oruga del brote’ del tabaco y ‘bolillera’ del lino. Revista de Investigaciones Agropecuarias, INTA, Bs. As., Rep. Argentina. Serie 5. Patología Vegetal 6, 19–68.Google Scholar
Westbrook, J.K. (2008) Noctuid migration in Texas within the nocturnal agro-ecological boundary layer. Integrative and Comparative Biology 48, 99–106.Google Scholar
Westbrook, J.K. & Lopez, J.D. Jr. (2010) Long distance migration in Helicoverpa zea: what we know and need to know. Southwestern Entomologist 35, 355–360.Google Scholar
Wu, K., Um, W., Liang, G. & Gou, Y. (2005) Regional reversion of insecticide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) is associated with the use of Bt cotton in northern China. Pest Management Science 61, 491–498.Google Scholar
Yenagi, B.S., Patil, V.C., Biradar, D.P. & Khadi, B.M. (2012) Molecular diversity of cotton bollworm (Helicoverpa armigera Hübner) using Rapd markers. Middle-East Journal of Scientific Research 11, 61–65.Google Scholar
Zhou, X.F., Faktor, O., Applebaum, S.W. & Coll, M. (2000) Population structure of the pestiferous moth Helicoverpa armigera in the Eastern Mediterranean using RAPD analysis. Heredity 85, 251–256.Google Scholar