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Revista Brasileira de Entomologia

Print version ISSN 0085-5626On-line version ISSN 1806-9665

Rev. Bras. entomol. vol.60 no.1 São Paulo Jan./Mar. 2016

https://doi.org/10.1016/j.rbe.2015.09.008 

Short Communications

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

Daniel R. Sosa-Gómeza  * 

Alexandre Spechtb 

Silvana V. Paula-Moraesb 

Adilson Lopes-Limac 

Silvia A.C. Yanoa 

Adriana Michelia 

Elisangela G.F. Moraisd 

Paulo Galloa 

Paulo R.V.S. Pereirae 

José R. Salvadorif 

Marcos Bottong 

Maurício M. Zenkerh 

Wilson S. Azevedo-Filhoi 

aEmbrapa Soja, Londrina, PR, Brazil

bEmbrapa Cerrados, Planaltina, DF, Brazil

cEmbrapa Amapá, Macapá, AP, Brazil

dEmbrapa Roraima, Boa Vista, RR, Brazil

eEmbrapa Trigo, Passo Fundo, RS, Brazil

fFaculdade de Agronomia e Medicina Veterinária, Universidade de Passo Fundo, Passo Fundo, RS, Brazil

gEmbrapa Uva e Vinho, Bento Gonçalves, RS, Brazil

hDepartamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brazil

iLaboratório de Biologia, Centro de Ciências Exatas, da Natureza e de Tecnologia, Universidade de Caxias do Sul, Bento Gonçalves, RS, 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, 2013). 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., 2013; Specht et al., 2013b). The identification was based on morphological characters of male genitalia (Czepak et al., 2013; Specht et al., 2013b) and molecular analysis (Specht et al., 2013b). 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, 1965; Pogue, 2004; Specht et al., 2013b). 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, 2004; Specht et al., 2005, 2013a; Zenker et al., 2010) 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) and Behere et al. (2008).

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. 

Brazilian municipalities/states Geographic coordinates (UPS) Plant or trap collect Species Sampling date Identification
Boa Vista, Roraima 02°53'45" N; 60°39'42" W Soybean H. armigera 05/08/2013 Morphological
Bonfim, Roraima 03°19'55" N; 59°50'44" W Soybean H. armigera 05/08/2013 Morphological
Bonfim, Roraima 03°19'55" N; 59°50'44" W Corn H. armigera , H. zea 05/08/2013 Morphological
Macapá, Amapá 00°14'48" S; 51°17'54" W Soybean H. armigera 08/08/2012 Morphological
Baixada Grande do Ribeiro, Piauí 07°51'01" S; 45°12'49" W Cotton H. armigera 12/05/2013 Morphological
Luís Eduardo Magalhães, Bahia 12°07'12" S; 45°48'41" W Cotton, H. armigera , H. zea 06/2012 Molecular, morphological
Luís Eduardo Magalhães, Bahia 12°07'12" S; 45°48'41" W Soybean H. armigera 06/2012 Molecular, morphological
Roda Velha, Bahia 12°42'9" S; 45°49'30" W Cotton, Soybean H. armigera 21/02/2013 Morphological
Correntina, Bahia 13°27'33" S; 45°44'11" W Cotton H. armigera , H. zea 23/12/2012 Morphological
Correntina, Bahia 13°27'33" S; 45°44'11" W Soybean H. armigera 23/12/2012 Morphological
Nova Mutum, Mato Grosso 13°53'59" S; 55°47'53" W Soybean H. armigera 23/02/2013 Morphological
Diamantino, Mato Grosso 14°21'29" S; 56°23'12" W Soybean H. armigera 21/01/2013 Morphological
Tangará da Serra, Mato Grosso 14°37'44" S; 57°34'32" W Soybean H. armigera 06/03/2013 Morphological
Campo Verde, Mato Grosso 15°28'19" S; 55°08'40" W Soybean H. armigera 08/02/2013 Morphological
Rondonópolis, Mato Grosso 16°42'43" S; 54°39'43" W Cotton H. armigera 11/04/2013 Morphological
Alto Taquari, Mato Grosso 17°50'08" S; 53°27'46" W Soybean H. armigera 14/01/2013 Morphological
Palmeira de Goiás, Goiás 16°39"29" S; 49°56'13" W Soybean H. armigera 23/02/2013 Morphological
Jataí, Goiás 17°56'25" S; 51°47'46" W Soybean H. armigera 23/02/2013 Morphological
Santa Juliana, Minas Gerais 19°21"29" S; 47°28'36" W Cowpea H. armigera 23/02/2013 Morphological
Afonso Cláudio, Espiritu Santo 20°02'55" S; 41°06'18" W Tomato H. armigera 02/03/2014 Morphological
Alegre, Espírito Santo 20°45'45" S 41°32'28" W Tomato H. armigera 02/03/2014 Morphological
Planaltina, Distrito Federal 15°35'05" S; 47°53'14" W Corn, soybean H. zea , H. armigera 03/10/2013 Molecular, morphological
Planaltina, Distrito Federal 15°35'05" S; 47°53'14" W soybean H. armigera 03/10/2013 Molecular, morphological
Brasília, Distrito Federal 15°44'06" S; 47°53'14" W Tomato H. armigera , H. zea 20/11/2013 Morphological
Costa Rica, Mato Grosso do Sul 18°34'49" S; 53°09'08" W Soybean H. armigera 21/12/2013 Morphological
Londrina, Paraná 23°11'44" S; 51°10'34" W Soybean, light trap H. armigera , H. zea 07/02/2013 Molecular, morphological
Rolândia, Paraná 23°17'47.0" S 51°26'01.9" W Soybean H. armigera 10/14/2008 Molecular
Taquarituba, São Paulo 23°42'49" S; 49°11'40" W Soybean H. armigera 03/27/2013 Molecular
Sengés, Paraná 24°07'22" S; 49°28'54" W Soybean H. armigera 03/27/2013 Molecular
Arapoti, Paraná 24°11'52" S; 49°55'12" W Wheat H. zea 03/27/2013 Molecular
Carambei, Paraná 24°59'36" S; 50°08'27" W Soybean H. armigera 03/27/2013 Molecular, morphological
Passo Fundo, Rio Grande do Sul 28°22'55" S; 52°38'96" W Soybean H. armigera , H. zea 20/12/2012 Morphological
Pinto Bandeira, Rio Grande do Sul 29°02'50" S; 51°28'12" W Light trap H. armigera 04/05/2011 Morphological
Espumoso, Rio Grande do Sul 28°43'11" S; 52°47'16" W Soybean H. armigera 21/12/2012 Morphological
Carazinho, Rio Grande do Sul 28°20'26" S; 52°52'57" W Soybean H. armigera , H. gelotopoeon 20/12/2012 Morphological

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., 2006) until 2008 (Zenker et al., 2010; Specht et al., 2013a) 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., 2013). 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, 2004; Specht et al., 2005, 2013a; Zenker et al., 2010) 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., 2014) 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, 2013). 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., 2013; Specht et al., 2013b; Tay et al., 2013), 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, 2013; Murúa et al., 2004), Puerto Rico (North American Plant Protection Organization, 2014) 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., 2012; Sosa-Gómez et al., 2014). 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., 2008) and species identification using molecular markers (Gomez-Rolim et al., 2013), 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, 2006). 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., 2013; Specht et al., 2013b), 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, 2010; Guillemaud et al., 2011).

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.

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Received: November 03, 2014; Accepted: September 21, 2015

* Corresponding author. E-mail:daniel.sosa-gomez@embrapa.br (D.R. Sosa-Gómez).

Conflicts of interest

The authors declare no conflicts of interest.

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