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Revista Brasileira de Fruticultura

versão impressa ISSN 0100-2945

Rev. Bras. Frutic. vol.36 no.2 Jaboticabal abr./jun. 2014 



Occurrence of Helicoverpa armigera (Hübner, 1808) on citrus in the state of Sao Paulo, Brazil1


Ocorrência de Helicoverpa armigera (Hübner, 1808) em citros no estado de São Paulo, Brasil



Regiane Cristina Oliveira de Freitas BuenoI; Pedro Takao YamamotoII; Marina Mouzinho CarvalhoIII; Nádia Maebara BuenoIV

IDRª. Professora Assistente Doutor do Depto de Proteção de Plantas - UNESP, Campus Botucatu, Botucatu-SP. Autor para correspondência. E-mail:
IIDR. Professor do Depto de Entomologia e Acarologia - ESALQ, Piracicaba-SP. E-mail:
IIIEng.ª Agr.ª Mestranda em Agronomia: Proteção de Plantas - UNESP, Campus Botucatu, Botucatu-SP. E-mail:
IVEng.ª Agr.ª Mestranda em Agronomia: Proteção de Plantas - UNESP, Campus Botucatu, Botucatu-SP. E-mail:




The occurrence of Helicoverpa armigera (Hübner, 1808) was first reported in citrus orchard in the state of São Paulo (SP). High infestation levels of H. armigera were observed in October 2012, in the city of Botucatu, SP. The larvae was fed of all parts of the plants. The injuries on the leaves caused drastic reduction in the leaf area and the fruits attack occurred from an early stage of development to the ripe fruit. Thus, the first occurrence of H. armigera in this citrus culture adds to the list of hosts of this pest, and is of great importance, because it confirms H. armigera potential dispersion and polyphagia.

Index terms: Quarantine pest, Heliothinae, Lepidoptera, Noctuidae, citrus.


A ocorrência de Helicoverpa armigera (Hübner, 1808) foi relatada pela primeira vez em pomar comercial de cítrus no Estado de São Paulo (SP). Altos níveis de infestação de H. armigera foram observados em outubro de 2012, na cidade de Botucatu-SP. As larvas alimentaram-se em todas as partes de plantas. As lesões nas folhas causaram drástica redução da área foliar, e o ataque aos frutos ocorreu a partir do estágio inicial de desenvolvimento até a fase do fruto maduro. Assim, o relato da primeira ocorrência de H. armigera acrescenta a cultura de citros à lista de hospedeiros desta praga, e é de grande importância, pois confirma a polifagia e o potencial de dispersão de H. armigera.

Termos para indexação: Praga quarentenária, Heliothinae, Lepidoptera, Noctuidae, citros.



Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae) is important polyphagous agricultural insect pest, highly mobile and has a worldwide distribution; inhabits diverse ecological habitats and is the most important insect pest occurring in the developing world that causes heavy yield losses of a diverse range of dicot and monocot crops (PRIYA et al., 2012). It has been recorded as a damaging pest on 181 cultivated and wild plant species in at least 45 families (SRIVASTAVA et al., 2010). This fact can be attributed to its high fertility, migration behavior, high adaptability to various climatic conditions and the development of resistance to broad range of insecticides (NASERI et al., 2010). Almost 30% of all pesticides used worldwide are directed against this insect pest (JOUBENA et. al., 2012). But, the repeated use of synthetic chemicals to manage this pest has resulted in resurgence and outbreak, resistance to insecticides, elimination of existing natural enemies in addition to polluting soil, water, air and food (BASKAR; IGNACIMUTHUA, 2012). Until the moment H. armigera has not been recorded in the Americas, being considered quarantine pest in Brazil (REED 1965; MORAL GARCIA, 2006). However, this species was highlighted as the most damaging pest to crops such as soybeans, cotton, tomatoes and corn in 2011/2012 crop season in several Brazilian agricultural regions with economic losses estimated at around R$ 140.00/ha in soybean crop in 2012/2013 (CZEPAK et al., 2013). The H. armigera adult has a wingspan of approximately 40 mm. The forewings have a yellowish color, with a darker cross-sectional stripe, dispersed dark spots and a highlighted comma-shaped spot on the bottom of the wings. The hindwings are paler in color with a darker border. Throughout the adult stage, which lasts from 12 to 15 days, each female is able to lay an average of 1,000 to 1,500 eggs. The moths have a preference for oviposition on the upper face of the leaves and/or rough and pubescent surfaces, with eggs laid isolated (SRINIVASAN et al., 2013). The larvae vary in color from green to black, with longitudinal stripes. The larval stage lasts from 13 to 25 days and comprises 5 instars. When fully developed, the larvae can measure up to 50 mm in length. The last-instar larvae leave the plant/fruits where the eggs were laid and migrate to the soil, where they pupate. This stage lasts approximately 14 days, according to the temperature variations. The caterpillars have light brown head capsule with white lines on the side and there is hairiness. From the 4th instar in the fourth segment there is presence of abdominal, dark and conspicuous tubercles. Another peculiar characteristic of H. armigera is the presence of integument with slightly coriaceous texture, very different from the other species Heliothinae (CZEPAK, 2013). Considering the importance of H. armigera in Brazilian territory this present study reports the occurrence of this species in a commercial citrus orchard, confirming its polyphagous habits, aiming at expanding the available information about this species. High densities were found in October 2012 on a farm located in Botucatu, State of São Paulo, Brazil (latitude: 22º 53' 09'' S; longitude: 48º 26' 42'' E; altitude: 804 m). In the infested orchard, there were plots with plant varieties at different development stages, from the flowering stage to that of fully ripe fruits ready to be harvested. The larvae showed no feeding preference, consuming whatever food was available, i.e., leaves, ripe and unripe fruits as well as weeds spontaneously occurring in the orchards (Figure 1). The H. armigera attack was severe and caused losses near 100% in plantations where it was found. The H. armigera larvae were collected and transported to the Entomology Laboratory of the São Paulo State University (Universidade Estadual Paulista - UNESP), Botucatu, São Paulo, where they were maintained under an artificial diet and controlled temperature until the emergence of the adults, for their identification. The insects were identified as belonging to the species H. armigera after molecular analysis. To perform the molecular analysis of H. armigera, the moths were stored in sealed containers with silica gel at -20ºC. Molecular characterization was performed by amplification of partial sequences of genes of cytochrome c oxidase (subunits I and II) and cytochrome B. The DNA extraction was performed based on salts of CTAB and the amplifications were performed with primer pairs: LCO 1490-J-1514. Two mtDNA primer sets were designed for COI and Cyt b. The primer set COI-F02 (5' CTC AAA TTA ATT ACT CCC CAT C 3') and COI-R02 (5' GGAGGTAAG TTT TGG TAT CAT T 3') was used to amplify 511 base pairs (bp) of partial COI. The primer set Cytb-F02 (5' GAA TCC TTT AATTTAAAATATAC 3') and Cytb-R02 (5' AAA TAT GGG TTA GTTAAA GTT AA 3') was used to amplify 434 bp of partial Cyt b. PCR conditions had the following profile: 94º C for 4 min (one cycle), 30 s each of 94º C, 50º C and 1 min at 72º C (35 cycles) followed by a final extension cycle of 72º C for 10 min (BEHERE et al., 2007).

The present study is the first report of H. armigera occurrence in citrus crops, adding this crop to the list of H. armigera hosts. This result is of great relevance in confirming the adaptive and dispersive potentials of this pest. This insect represents a serious threat to citrus crops, because in addition to the damage caused in that crop, the moth damage can hinder the following year's production. Taking action to characterize the magnitude of the problem and proposing integrated pest-management strategies is important for its successful control.



BASKAR, K.; IGNACIMUTHUA, S. Antifeedant, larvicidal and growth inhibitory effects of ononitol monohydrate isolated from Cassia tora L. against Helicoverpa armigera (Hub.) and Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Chemosphere, Los Angeles, v. 88, n.4, p.384-388, 2012.         [ Links ]

BEHERE, G.T.; TAY, W.T.; RUSSELL, D.A.; HECKEL, D.G.; APPLETON, B.R.; KRANTHI, K.R.; BATTERHAM, P. Mitochondrial DNA analysis of field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) and of its relationship to H. zea. BMC Evolutionary Biology, New York, v.7, n. 117, p. 1-20, 2007.         [ Links ]

CZEPAK, C.; ALBERNAZ, K. C.; VIVAN, L. M.; GUIMARÃES, H. O.; CARVALHAIS, T. Primeiro registro de ocorrência de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) no Brasil. Pesquisa Agropecuária Tropical, Goiânia, v.43, p.110–113, 2013.         [ Links ]

JOUBENA, N.; AGNOLETB, S.; LORENZC, S.; SCHONEA, S. E.; ELLINGERB, R.; SCHNEIDERB, B. Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proceedings of the National Academy of Sciences of the United States of America, Washington, v. 109, n. 38, p.15206-15211, 2012.         [ Links ]

MORAL GARCIA, F. J. Analysis of the spatiotemporal distribution of Helicopverpa armigera (Hübner) in tomato field using a stochastic approach. Biosystems Engineering, Bedford, v. 93, n.3, p. 253-259, 2006.         [ Links ]

NASERI, B.;FATHIPOUR, Y.; MOHARRAMIPOUR, S.; HOSSEININAVEH, V.; GATEHOUSE, A. M. Digestive proteolytic and amylolytic activities of Helicoverpa armigera in response to feeding on different soybean cultivars. Pest Management Science, Weinheim, v. 66, n. 12, p. 1.316-1.323, 2010.         [ Links ]

PRIYA, G. N.; OJHA, A.; KAJLA, M. K.; RAJ, A.; RAJAGOPAL, R. Host Plant Induced Variation in Gut Bacteria of Helicoverpa armigera. Plos One, Hyderabad, v.7, n. 1, p. 307-318, 2012.         [ Links ]

REED, W. Heliothis armigera (Hb.) (Noctuidae) in western Tanganyika: II. Ecology and natural and chemical control. Bulletin of Entomological Research, Cambridge, v. 56, n.1, p. 127-140, 1965.         [ Links ]

SRINIVASAN, R.; SU, F.-C.; HUANG, C.C. Oviposition dynamics and larval development of Helicoverpa armigera on a highly preferred unsuitable host plant, Solanum viarum. Entomologia Experimentalis et Applicata, Amsterdam , v. 147, p. 217-224, 2013.         [ Links ]

SRIVASTAVA, C. P.; NITIN, J.; TRIVEDI, T.P. Forecasting of Helicoverpa armigera populations and impact of climate change. Indian Journal of Agricultural Sciences, New Delhi, v. 80, n.1, p. 3-10, 2010.         [ Links ]



Recebido em:02-10-2013.
Aceito para publicação em: 06-02-2014



1 (Trabalho 357-13).

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