Acessibilidade / Reportar erro

Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil

ABSTRACT

This study presents registers of Helicoverpa armigera (Hübner) occurrence to assess its spatial and temporal distribution in Brazil. We used data from collections, especially from the Southern Region, systematic collections in Rio Grande do Sul, occasional collections of caterpillars and adults in different regions of Brazil, as well as literature registers. We conclude that the introduction of H. armigera in Brazil probably occurred before October 2008. We also register that in August 2012 H. armigera was already present from the extreme southern part (Rio Grande do Sul) to the extreme northern part (Amapá) of Brazil.

Keywords:
Old World bollworm; Polyphagous caterpillar; Geographical distribution

In March 2013, the Old World bollworm, Helicoverpa armigera (Hübner), was reported in Brazil (Embrapa, 2013Embrapa, 2013. Nota técnica sobre resultados do trabalho inicial de levantamento da lagarta do gênero Helicoverpa – detecção da espécie Helicoverpa armigera no Brasil. Embrapa Cerrados, Planaltina.). On that occasion, specimens were collected in the states of Bahia, Mato Grosso, Paraná, and Goiás, and also in Distrito Federal, causing damage on corn, soybean, and cotton (Czepak et al., 2013Czepak, 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.; Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.). The identification was based on morphological characters of male genitalia (Czepak et al., 2013Czepak, 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.; Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.) and molecular analysis (Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.). This species is genetically and morphologically closely related to Helicoverpa zea (Boddie), and the identification based on genitalia characters is time-consuming and requires a well-trained taxonomist. These two species are almost indistinguishable when characterization is based on external morphological characters (Hardwick, 1965Hardwick, D.F., 1965. The corn earworm complex. Mem. Entomol. Soc. Canada 97, 5-247.; Pogue, 2004Pogue, M.G., 2004. A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Ann. Entomol. Soc. Am. 97, 1222-1226.; Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.). For these reasons, surveys were performed in different parts of the country to confirm the geographical distribution, using reliable diagnostic methods (inner male genitalia and/or molecular tools), and establish the approximate time of introduction of this pest in Brazil.

The geographical distribution was obtained after identifying field collected larvae, or rearing immatures until the adult phase, or collecting owlet moths with light traps. The occurrence of H. armigera before 2013 in Brazil was investigated through analysis of samples deposited in scientific collections from Embrapa Cerrados, Embrapa Soybean, the Museum of Science and Technology from Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), and the collection of the Universidade de Caxias do Sul, considering mainly the samples collected using light traps in Rio Grande do Sul since 1998 (Teston and Corseuil, 2004Teston, J.A., Corseuil, E., 2004. Diversidade de Arctiinae (Lepidoptera, Arctiidae) capturados com armadilha luminosa, em seis comunidades no Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 48, 77-90.; Specht et al., 2005Specht, A., Teston, J.A., Di Mare, R.A., Corseuil, E., 2005. Noctuídeos (Lepidoptera, Noctuidae) coletados em quatro Áreas Estaduais de Conservação do Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 49, 130-140., 2013aSpecht, A., Ângulo, A.O., Olivares, T.S., Fronza, E., Roque-Specht, V.F., Valduga, E., Albrecht, F., Poletto, G., Barros, N.M., 2013a. Life cycle of Agrotis malefida (Lepidoptera: Noctuidae): a diapausing cutworm. Zoologia 30, 371-378.; Zenker et al., 2010Zenker, M.M., Botton, M., Teston, J.A., Specht, A., 2010. Noctuidae moths occurring in grape orchards in Serra Gaúcha, Brazil and their relation to fruit-piercing. Rev. Bras. Entomol. 54, 288-297.) and systematized monthly collections using light traps, from May 2011 to April 2013, in Pinto Bandeira, RS. The morphological and molecular identifications were performed as described by Pogue (2004)Pogue, M.G., 2004. A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Ann. Entomol. Soc. Am. 97, 1222-1226. and Behere et al. (2008)Behere, G.T., Tay, W.T., Russell, D.A., Batterham, P., 2008. Molecular markers to discriminate among four pest species of Helicoverpa (Lepidoptera: Noctuidae). Bull. Entomol. Res. 98, 599-603..

The PCR-RFLP molecular analysis, was performed with the amplification product corresponding to positions between 2443 and 2953 from the COI gene of Helicoverpa species (Accession number GU188273 from H. armigera mitogenome) and restriction fragment length polymorphism (RFLP) analysis with the BstZ17I endonuclease (Fig. 1), as well as the morphological characters indicate that so far H. armigera occurs in the following states of Brazil: Roraima, Amapá, Piauí, Bahia, Mato Grosso, Mato Grosso do Sul, Distrito Federal, Goiás, Espírito Santo, São Paulo, Paraná, and Rio Grande do Sul (Table 1 and Fig. 1).

Fig. 1
PCR-RFLP agarose gel (1.5%) for COI amplification products (511 b) using BstZ17I endonuclease. Lane 1: 100 bp MW; lanes 2 and 5: undigested product of Helicoverpa zea (Londrina, PR); lanes 3 and 4: digestion product of Helicoverpa armigera (Londrina, PR); lane 6: digestion product of H. armigera; lanes 7–10: undigested product of H. zea (Planaltina, DF); lanes 11–15: digestion product of H. armigera (Luiz Eduardo Magalhães, BA); lanes 16–20: digestion product of H. armigera (Carambeí, PR); lanes 21 and 22: undigested product of H. zea (Arapoti, PR); lanes 23 and 24: digestion product of H. armigera (Sengés, PR); lanes 25–28: digestion product of H. armigera (Taquarituba, SP); lane 29: undigested product of H. zea (Taquarituba, SP); lane 30: 100 bp MW.

Table 1
Helicoverpa spp. in Brazil collections.

We identified one H. armigera specimen in a larval sample collected in Rolândia, Paraná, in October 14, 2008. This was the first time that this species was observed in samples analyzed for the present study. After this, the exam of adults from systematized monthly collections in Pinto Bandeira, RS (extreme southern Brazil) provided the detection of H. armigera on May 4, 2011. In the same year, H. armigera specimens were collected in August (n = 6) and September (n = 1). In 2012, adults of H. armigera were found in February (n = 1), August (n = 4), September (n = 3), October (n = 1), and December (n = 1). In 2013, adults of this species were collected in February (n = 2), March (n = 2), and April (n = 4).

The exam of adults obtained from immatures of H. armigera collected in soybean fields in the extreme northern Brazil (Amapá) confirmed the occurrence of this species since August 8, 2012. Most of Heliothinae larvae collected in soybean fields were H. armigera, a very small proportion of specimens belong to Chloridea virescens (0.2%). Evaluations of collections performed from 1998 (Teston et al., 2006Teston, J.A., Specht, A., Di Mare, R.A., Corseuil, E., 2006. Arctiinae (Lepidoptera, Arctiidae) coletados em unidades de conservação estaduais do Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 50, 280-286.) until 2008 (Zenker et al., 2010Zenker, M.M., Botton, M., Teston, J.A., Specht, A., 2010. Noctuidae moths occurring in grape orchards in Serra Gaúcha, Brazil and their relation to fruit-piercing. Rev. Bras. Entomol. 54, 288-297.; Specht et al., 2013aSpecht, A., Ângulo, A.O., Olivares, T.S., Fronza, E., Roque-Specht, V.F., Valduga, E., Albrecht, F., Poletto, G., Barros, N.M., 2013a. Life cycle of Agrotis malefida (Lepidoptera: Noctuidae): a diapausing cutworm. Zoologia 30, 371-378.) in the Southern Region of Brazil did not reveal the occurrence of H. armigera. We did not find H. zea specimens from immature insects collected in soybean. However, this former species is a soybean pest in United State of America (Swenson et al., 2013Swenson, S.J., Prischmann–Voldseth, D.A., Musser, F.R., 2013. Corn earworms (Lepidoptera: Noctuidae) as pests of soybean. J. Integr. Pest Manage., 4.). All the Helicoverpa samples collected from corn were obtained from corn ear, revealing host preference of Brazilian populations of H. zea for this host plant.

The analysis of insects previously collected and deposited in museums by several authors (Teston and Corseuil, 2004Teston, J.A., Corseuil, E., 2004. Diversidade de Arctiinae (Lepidoptera, Arctiidae) capturados com armadilha luminosa, em seis comunidades no Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 48, 77-90.; Specht et al., 2005Specht, A., Teston, J.A., Di Mare, R.A., Corseuil, E., 2005. Noctuídeos (Lepidoptera, Noctuidae) coletados em quatro Áreas Estaduais de Conservação do Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 49, 130-140., 2013aSpecht, A., Ângulo, A.O., Olivares, T.S., Fronza, E., Roque-Specht, V.F., Valduga, E., Albrecht, F., Poletto, G., Barros, N.M., 2013a. Life cycle of Agrotis malefida (Lepidoptera: Noctuidae): a diapausing cutworm. Zoologia 30, 371-378.; Zenker et al., 2010Zenker, M.M., Botton, M., Teston, J.A., Specht, A., 2010. Noctuidae moths occurring in grape orchards in Serra Gaúcha, Brazil and their relation to fruit-piercing. Rev. Bras. Entomol. 54, 288-297.) suggested that at least in Rio Grande do Sul the introduction of H. armigera occurred after December 2008 and before May 2011. The earliest H. armigera samples mentioned in the published literature are from May 22, 2012 (Leite et al., 2014Leite, 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.) in this study we found one larvae of H. armigera in soybean fields from Rolândia, Paraná in October of 2008. Based on the evidence provided by these data and considering a scenario of introduction of H. armigera in the country before 2008, it is reasonable to infer that this pest had enough time to build up populations detected as outbreaks in the 2012/2013 growing season (Embrapa, 2013Embrapa, 2013. Nota técnica sobre resultados do trabalho inicial de levantamento da lagarta do gênero Helicoverpa – detecção da espécie Helicoverpa armigera no Brasil. Embrapa Cerrados, Planaltina.). In August 2011, six specimens were captured in one sampling date, indicating that populations of this insect were already established in this area. Interestingly, in two consecutive years of monthly sampling a progressive increase of adults captured mainly at the end of the winter (August and September) and at the end of the summer (April) was observed.

The fact that H. armigera was detected from northern to southern Brazil, at least during the 2012/2013 growing season, when substantial damage was reported by several researchers (Czepak et al., 2013Czepak, 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.; Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.; Tay et al., 2013Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G.T., Anderson, C., Downes, S., 2013. A brave new world for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One 8, 1-7.), reveals that the identification of this species in the country was carried out a long time after its introduction, constraining management control decisions to minimize the impact of this pest in several crops. Soon after being reported in Brazil, H. armigera was also found in Paraguay and Argentina (Senave, 2013Senave en alerta tras ingreso de peligrosa plaga agrícola, 2013. ABC Color, 17 de Octubre, Available at: http://www.abc.com.py/edicion-impresa/economia/senave-en-alerta-tras-ingreso-de-peligrosa-plaga-agricola-629240.html.
http://www.abc.com.py/edicion-impresa/ec...
; Murúa et al., 2004Murúa, M.G., Scalora, F.S., Navarro, F.R., Cazado, L.E., Casmuz, A., Villagrán, M.E., Lobos, E., Gastaminza, G., 2004. First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomol. 97, 854-856.), Puerto Rico (North American Plant Protection Organization, 2014North American Plant Protection Organization, 2014. Detection of Old World Bollworm (Helicoverpa armigera) in Puerto Rico, Available: http://www.pestalert.org/oprDetail.cfm?oprID=600 (accessed November 2014).
http://www.pestalert.org/oprDetail.cfm?o...
) and later in USA (http://www.freshfromflorida.com/Divisions-Offices/Plant-Industry/Plant-Industry-Publications/Pest-Alerts/Pest-Alert-The-Old-World-Bollworm).

The late detection of H. armigera after its introduction could be attributed to the high similarity between this species and H. zea, as well as to the scarce number of studies for the identification of pest species, such as insect identification guides and other related publications (Hoffmann-Campo et al., 2012Hoffmann-Campo, C.B., Correa-Ferreira, B.S., Moscardi, F., 2012. Soja: manejo integrado de insetos e outros artrópodes-praga. Embrapa Soja, Londrina.; Sosa-Gómez et al., 2014Sosa-Gómez, D.R., Corrêa-Ferreira, B.S., Hoffmann-Campo, C.B., Corso, I.C., Oliveira, L.J., Moscardi, F., Panizzi, A.R., Bueno, A.F., Hirose, E., Roggia, S., 2014. Manual de identificação de insetos e outros invertebrados da cultura da soja, 3rd ed. Embrapa Soja. Documentos, Londrina, pp. 269.). Moreover, the specific identification of insect species is carried out, almost exclusively, based on external morphology of the adult specimens, which requires rearing immature individuals. This technique is time consuming and, many times, natural enemies kill the immature individuals. Therefore, only some studies of the immature stages of insects (Angulo et al., 2008Angulo, A.O., Olivares, T.S., Weigert, G.T., 2008. Estados inmaduros de lepidópteros nóctuidos de importancia agrícola y forestal en Chile y claves para su identificación (Lepidoptera: Noctuidae), 3rd ed. Universidad de Concepción, Concepción.) and species identification using molecular markers (Gomez-Rolim et al., 2013Gomez-Rolim, A.A.S.G., Yano, S.A.C., Specht, A., Andrade, C.G.T.J., Sosa-Gómez, D.R., 2013. Morphological and molecular characterization of the eggs of some noctuid species associated with soybean in Brazil. Ann. Entomol. Soc. Am. 106, 643-651.), which requires more investments, especially in equipment and specialized technicians, have been performed. However, most of these studies focus on determined taxa, usually genera, and most species continue not having a complete morphological or molecular characterization. These deficiencies are evidenced in many countries, especially in South America, due to a biological megadiversity and lack of taxonomists (Marques and Lamas, 2006Marques, A.C., Lamas, C.J.E., 2006. Taxonomia zoológica no Brasil: estado da arte, expectativas e sugestões de ações futuras. Papeis Avulsos de Zoologia 46, 139-174.). Furthermore, the morphological similarities between H. armigera and H. zea turn the situation even more critical.

In conclusion, the detection of H. armigera as a devastating component in high-value commercial crops, such as cotton and soybean (Czepak et al., 2013Czepak, 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.; Specht et al., 2013bSpecht, 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 Agropecuária Brasileira 48, 689-692.), shows the vulnerability of Brazil and other countries in South America regarding quarantine pests. Additionally, efforts to elucidate invasion paths and origin are essential to design strategies for preventing future pest introduction and adopting science-based policies (Estoup and Guillemaud, 2010Estoup, A., Guillemaud, T., 2010. Reconstructing routes of invasion using genetic data: why, how and so what?. Mol. Ecol. 19, 4113-4130.; Guillemaud et al., 2011Guillemaud, T., Ciosi, M., Lombaert, E., Estoup, A., 2011. Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. C. R. Biol. 334, 237-246.).

Acknowledgments

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial assistance (Processes 403376/2013-0, 476691/2013-3) and José Jairo da Silva for his assistance with molecular techniques.

References

  • Angulo, A.O., Olivares, T.S., Weigert, G.T., 2008. Estados inmaduros de lepidópteros nóctuidos de importancia agrícola y forestal en Chile y claves para su identificación (Lepidoptera: Noctuidae), 3rd ed. Universidad de Concepción, Concepción.
  • Behere, G.T., Tay, W.T., Russell, D.A., Batterham, P., 2008. Molecular markers to discriminate among four pest species of Helicoverpa (Lepidoptera: Noctuidae). Bull. Entomol. Res. 98, 599-603.
  • 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.
  • Embrapa, 2013. Nota técnica sobre resultados do trabalho inicial de levantamento da lagarta do gênero Helicoverpa – detecção da espécie Helicoverpa armigera no Brasil. Embrapa Cerrados, Planaltina.
  • Estoup, A., Guillemaud, T., 2010. Reconstructing routes of invasion using genetic data: why, how and so what?. Mol. Ecol. 19, 4113-4130.
  • Gomez-Rolim, A.A.S.G., Yano, S.A.C., Specht, A., Andrade, C.G.T.J., Sosa-Gómez, D.R., 2013. Morphological and molecular characterization of the eggs of some noctuid species associated with soybean in Brazil. Ann. Entomol. Soc. Am. 106, 643-651.
  • Guillemaud, T., Ciosi, M., Lombaert, E., Estoup, A., 2011. Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. C. R. Biol. 334, 237-246.
  • Hardwick, D.F., 1965. The corn earworm complex. Mem. Entomol. Soc. Canada 97, 5-247.
  • Hoffmann-Campo, C.B., Correa-Ferreira, B.S., Moscardi, F., 2012. Soja: manejo integrado de insetos e outros artrópodes-praga. Embrapa Soja, Londrina.
  • 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.
  • Marques, A.C., Lamas, C.J.E., 2006. Taxonomia zoológica no Brasil: estado da arte, expectativas e sugestões de ações futuras. Papeis Avulsos de Zoologia 46, 139-174.
  • Murúa, M.G., Scalora, F.S., Navarro, F.R., Cazado, L.E., Casmuz, A., Villagrán, M.E., Lobos, E., Gastaminza, G., 2004. First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomol. 97, 854-856.
  • North American Plant Protection Organization, 2014. Detection of Old World Bollworm (Helicoverpa armigera) in Puerto Rico, Available: http://www.pestalert.org/oprDetail.cfm?oprID=600 (accessed November 2014).
    » http://www.pestalert.org/oprDetail.cfm?oprID=600
  • Pogue, M.G., 2004. A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Ann. Entomol. Soc. Am. 97, 1222-1226.
  • Senave en alerta tras ingreso de peligrosa plaga agrícola, 2013. ABC Color, 17 de Octubre, Available at: http://www.abc.com.py/edicion-impresa/economia/senave-en-alerta-tras-ingreso-de-peligrosa-plaga-agricola-629240.html
    » http://www.abc.com.py/edicion-impresa/economia/senave-en-alerta-tras-ingreso-de-peligrosa-plaga-agricola-629240.html
  • Sosa-Gómez, D.R., Corrêa-Ferreira, B.S., Hoffmann-Campo, C.B., Corso, I.C., Oliveira, L.J., Moscardi, F., Panizzi, A.R., Bueno, A.F., Hirose, E., Roggia, S., 2014. Manual de identificação de insetos e outros invertebrados da cultura da soja, 3rd ed. Embrapa Soja. Documentos, Londrina, pp. 269.
  • Specht, A., Teston, J.A., Di Mare, R.A., Corseuil, E., 2005. Noctuídeos (Lepidoptera, Noctuidae) coletados em quatro Áreas Estaduais de Conservação do Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 49, 130-140.
  • Specht, A., Ângulo, A.O., Olivares, T.S., Fronza, E., Roque-Specht, V.F., Valduga, E., Albrecht, F., Poletto, G., Barros, N.M., 2013a. Life cycle of Agrotis malefida (Lepidoptera: Noctuidae): a diapausing cutworm. Zoologia 30, 371-378.
  • 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 Agropecuária Brasileira 48, 689-692.
  • Swenson, S.J., Prischmann–Voldseth, D.A., Musser, F.R., 2013. Corn earworms (Lepidoptera: Noctuidae) as pests of soybean. J. Integr. Pest Manage., 4.
  • Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G.T., Anderson, C., Downes, S., 2013. A brave new world for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One 8, 1-7.
  • Teston, J.A., Corseuil, E., 2004. Diversidade de Arctiinae (Lepidoptera, Arctiidae) capturados com armadilha luminosa, em seis comunidades no Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 48, 77-90.
  • Teston, J.A., Specht, A., Di Mare, R.A., Corseuil, E., 2006. Arctiinae (Lepidoptera, Arctiidae) coletados em unidades de conservação estaduais do Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 50, 280-286.
  • Zenker, M.M., Botton, M., Teston, J.A., Specht, A., 2010. Noctuidae moths occurring in grape orchards in Serra Gaúcha, Brazil and their relation to fruit-piercing. Rev. Bras. Entomol. 54, 288-297.

Publication Dates

  • Publication in this collection
    Jan-Mar 2016

History

  • Received
    03 Nov 2014
  • Accepted
    21 Sept 2015
Sociedade Brasileira De Entomologia Caixa Postal 19030, 81531-980 Curitiba PR Brasil , Tel./Fax: +55 41 3266-0502 - São Paulo - SP - Brazil
E-mail: sbe@ufpr.br