Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7

Current Agricultural Science and Technology ISSN 2317-2436 Faculdade de Agronomia Eliseu Maciel http://periodicos.ufpel.edu.br/ojs2/index.php/CAST Fundada em 1883

Helicoverpa armigera: current status and future perspectives in Brazil Aline Pomari-Fernandes1; Adeney de Freitas Bueno2; Daniel Ricardo Sosa-Gómez2

1Instituto Agrônomico do Paraná (IAPAR), Rodovia Celso Garcia Cid, km 375, Londrina, Paraná, Brasil, 86047-902. E-mail: [email protected] 2Empresa Brasileira de Pesquisa Agropecuária – Embrapa Soja, Caixa Postal 231, Londrina, Paraná, Brasil, 86001-970. E-mail: [email protected]; [email protected]

*Corresponding author: A. F. Bueno Embrapa Soja, PO BOX 231, 86001-970, Londrina, Paraná, Brazil. E-mail: [email protected]

ABSTRACT reducing costs and maximizing productivity. The arrival of H. armigera in Brazil has resulted in a The bollworm armigera is a national debate about the importance of IPM polyphagous first identified in the South adoption. It is a chance to fully implement IPM in American continent in Brazil during the 2012/13 Brazil as it has never been done or seen before in crop season, worrying farmers across the country the history of tropical agriculture. If IPM is leading them to overuse insecticides in an successfully adopted in Brazil, the future attempt to control its outbreaks. However, it is perspective of H. armigera will be that of being a essential to emphasize the importance of the satisfactorily managed pest. In contrast, if only a adoption of Integrated Pest Management (IPM) simplified version of IPM is employed, H. philosophy, since improperly applied insecticides armigera and many other pests will have a will exacerbate pest problem by eliminating the greater chance of surviving and causing severe biological control agents and increase the damage to crops. production cost unnecessarily. Therefore, our work discusses, in more detail, the current status, Keywords: bollworm; Heliothinae; quarantine recommended management, and future pest; polyphagous pest. perspectives of this pest in Brazil. We conclude that, in spite of H. armigera infestation in Brazil, it INTRODUCTION will still be feasible for growers to adopt pest- control measures that have less impact on the Helicoverpa armigera (Hübner) environment in accordance with the standard (: ) is one of the world‘s principles of the IPM philosophy. Within this most important agricultural pests (Tay et al. context, monitoring for pests and initiating 2013). In Brazil, it has been recognized as a control measures only when the pest populations quarantine pest since 1999, and received the A1 reaches the economic thresholds (ET) quarantine pest status in 2008 (Oliveira et al. recommended by research is crucial. These 2003; Lima et al. 2006; Agropec Consultoria, procedures protect crop sustainability, thus 2013). Its occurrence was first reported in the keeping growers competitive in the market while country only in February 2013 (Czepak et al. 2013; 1 http://dx.doi.org/10.18539/cast.v21i1.4234 Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7 Specht et al. 2013). Even though just registered in soybean looper Chrysodeixis includens (Walker) 2013, it is highly possible the pest was present in (Lepidoptera: Noctuidae) has also increased in Brazil before 2013 as H. armigera is difficult to importance and reached the status of a key pest distinguish from other related species of the same in soybean, for example (Bueno et al. 2012). More subfamily Heliothinae ( or even recently, H. armigera is the pest species which has Heliothis virescens, for example) based only on also become prominent among Brazilian soybean morphological characteristics for non-experts. growers (Bueno et al. 2013). Moreover, H. armigera was wide spread in the Into the analysis of H. amigera status, it is country in its first year of occurrence, a important to considerer this pest not only causes distribution pattern usually expected to take defoliation but also attacks plant reproductive many months to occur (Bueno et al. 2014). organs (such as soybean pods). In the 2012/13 The pest identification was performed and 2013/14 crop seasons, high infestations of almost simultaneously and independently by Helicoverpa species larvae were detected in taxonomists Dr. Alexandre Specht and Dr. Vitor different regions of Brazil attacking different Becker (Bueno et al. 2014), based on the crops, resulting in significant economic loss. morphology of male genitalia and confirmed by Initially the species was presumed to be mitochondrial gene sequencing (Specht et al. Helicoverpa zea (Boddie) (Lepidoptera: 2013; Bueno and Sosa-Gómez, 2014). Noctuidae), which is often found in and Identification via male genitalia morphology has crops in Brazil (Degrande and Omoto been used extensively, although Pogue (2004) 2013). Later, high prevalence of H. armigera was reported overlapping ranges in male vesica found in Western Bahia, (an important between H. armigera and H. zea (Tay et al. 2013). agricultural state in Brazil) causing serious Nevertheless, the establishment of an damage to soybean, corn, and especially, invasive species in a new territory can lead to (Czepak et al. 2013; Specht et al. 2013). In most rapid and significant negative economic and cases, this, along with media pressure, led to environmental impacts. Damages of H. armigera growers using insecticide sprays even when the has been reported to be greater than $2 billion pest populations were still low or even annually, excluding socio-economic and nonexistent. These erroneous and abusive environmental costs associated with its control in applications of insecticides only exacerbated the Asia, Europe, Africa, and Australia (Tay et al. problem of pests, mainly due to the elimination of 2013). In Brazil, damage reports reached biological control agents (predators and approximately $0.8 billion in the first crop season parasitoids) that occur naturally. As a (2012/2013) after pest occurrence (Bueno et al. consequence, the recently detected H. armigera 2014). Taking this scenario into consideration, this caterpillars and possibly other pest species such work aims to discuss in more detail the current as Spodoptera spp., despite not being widespread status, recommended management, and future key pests in the country, have been causing perspectives of this pest in Brazil. significant problems for growers. This has brought back the discussion about Helicoverpa armigera: Current status in Brazil the importance of integrated pest management (IPM) in agriculture. This is very important since Caterpillar outbreaks the growing number of caterpillar-attacks on crops such as soybean is mainly due to the Similar to any other caterpillar species, the abandonment of IPM and the overuse of current status of H. armigera may vary among insecticides, applied on a calendar basis, or different crops and regions within the same together with herbicides and fungicides sprayings. country. In Brazil, besides H. armigera, the Other key factors include the lack of monitoring 2

Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7 and quantification of infestation in the field crops. In soybean, for example, it is important to (Bueno et al. 2013). In this current scenario, it is consider that there is a complex of caterpillar necessary to emphasize that improper use of species that can attack plants from the beginning insecticides will only exacerbate this problem and of its development until the reproductive period unnecessarily increase production costs. which must be managed together. Also, H. It is important to clarify that, in some armigera is highly reproductive, with rapid Brazilian states such as Bahia, which are typically development potential; hence, it can give rise to dry and warm, H. armigera occurrence and overlapping generations throughout the crop damage might be higher compared to other cycle, especially in hot and dry years. Therefore, regions of the country. In southern Brazilian under favorable conditions, population levels of states, for example, Helicoverpa spp. prevalence this caterpillar can increase rapidly and cause has been low, even though localized attacks on significant yield loss if not properly managed. green beans, coffee, wheat, and citrus, among The main steps for a good management of other crops, have been reported. the major lepidopteran species include: a) species identification, b) quantification of their attacks on Host plants the field through regular sampling, and c) adoption of the most appropriate integrated- Host species for H. armigera come from a management tactics for every specific situation. broad spectrum of families (>45 families) and The best control methods, right timings, best include >180 plant hosts among which are products, correct rates, and appropriated important agricultural crops such as cotton, technology for pesticide application are examples maize, , pigeon pea, sorghum, sunflower, of important variables that can determine pest soybean, and groundnuts (Fitt 1989; Tay et al. management success. 2013). Generally, in Brazil, the most important crops afflicted by H. armigera include cotton, a) Species identification soybean, corn, green beans, tomatoes, citrus, and pastures. However, in corn, it is common to find Often, the recognition and differentiation mixed infestations of H. zea and H. armigera. In of species is very difficult and impractical to be soybean and cotton, mixed infestations of H. performed as a daily routine in the field. armigera and Heliothis virescens (Fabricius) However, the soybean producer needs to (Lepidoptera: Noctuidae) might also occur. recognize at least the major four groups of Helicoverpa armigera has also been found feeding caterpillars attacking the crops. These caterpillars on weeds such as Conyza bonariensis (Asteraceae) (groups) are: and Rumex. Its polyphagous nature keeps the H. 1) The velvetbean caterpillar: composed of a armigera population high throughout the year single species, A. gemmatalis; due to various host availability and this presents 2) The soybean looper complex: majority are C. some challenges to the pest management. includens (formerly known as Pseudoplusia includens) and Rachiplusia nu; Helicoverpa armigera management 3) The caterpillar complex of the genus Spodoptera; It is important for H. armigera 4) The Heliothinae complex: includes caterpillars management success to consider the whole of the genera Heliothis and Helicoverpa. landscape, including both cropped and non- Insect injury observation in the field can cropped areas, due to the insect polyphagia. help to recognize the pest attacking the plants. Moreover, it also important to point out However, apart from H. armigera, which causes recommendations can differ between different damage to the leaves and pods of the plant, there 3

Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7 are other species of insect pests such as the same area size and at same number of points Spodoptera cosmioides, S. eridania, H. zea, and H. per hectare. virescens, which also cause the same damage as In the sample, the number of that caused by H. armigera on soybean should be recorded after separating the number reproductive structures and can be confused with of small (<1.5 cm length) and large (> or = 1.5 cm H. armigera in the field. Also, the presence of C. length) caterpillars by species (or as a group of includens, and more rarely A. gemmatalis, can caterpillars when separation by species is not also cause some damage to the pods, mainly possible). In addition, defoliation should be when there is a lack of palatable leaves, what can recorded (as percentage; visual). After sampling, lead to misidentification. insecticides, chemical, and/or biological The differentiation of the species applications should be made only when the belonging to the subfamily Heliothinae (Heliothis caterpillar population is equal to or higher than and Helicoverpa genus) requires specific the economic threshold (ET) (Table 1). knowledge of their internal and external Some management measures can be used morphology and is impractical in the field as even before and during sowing of the plants: previously mentioned. Thus, these species should - Pre-sowing and sowing pest management be managed together under field conditions. strategies The correct soybean pest identification - Whenever possible, sequential burndown into these four groups is important for adopting (herbicide) of seedlings must be performed (1st the most appropriate pest management application of herbicide must be between 3 and 4 strategies. The choice of insecticides, biological weeks prior to sowing and the 2nd application control agents, resistant plants, and/or other around the time of sowing). management practices may be different for each - Even when pests are present before group of pests, in order to obtain the highest sowing, insecticides should not be mixed with efficiency of the adopted control. herbicides during burndown. Pests can be controlled using other options such as: seed b) Diagnosis and control treatment with depending on the Lepidoptera species and insecticide used. Another option can To achieve an adequate diagnosis, crops be the adoption of Bt soybean (biotech soybean must be sampled accordingly. For sampling, the expressing Cry1Ac protein). For this technology is farm needs to be divided into homogeneous plots important to emphasize the necessity for the (smaller areas with the same sowing date, same adoption of a refuge area with non-Bt soybeans cultivar, same edaphic condition, etc). In the case (refuge area), according to the current technical of soybean, plots must be no bigger than 400 guidance. There is still some discussion regarding hectares (ha). Smaller plots are desirable when the most appropriate size of the area to be possible, because they will be more cultivated for refuge. For soybeans, the detaining homogeneous. Sampling should be done with the technology companies (industries) recommend a help of ground cloth (1-meter long cloth) and minimum of 20% of the area with non-Bt soybean should be performed with a minimum frequency (refuge). On the other hand, some scientists of once a week and at least at one point in every advocate that in order to increase the durability 10 hectares. It is important for this procedure to of the technology, this refuge area should be be performed from the time of soybean increased to 50%. Regardless of any controversy, emergence until at least the beginning of the R7 it is certain that the adoption of a refuge area is stage. In the beginning, when the ground cloth essential and must be done accurately for it to sampling cannot be used due to the small sized work. plants, visual sampling needs to be performed in 4

Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7

Table 1. Major Economic thresholds used for soybean caterpillars (Bueno et al. 2014) Species Economic Threshold Important Defoliation equal or higher than 30% at crop vegetative stage. Caterpillars (all species) Always favor the use of soft Defoliation equal or higher than 15% insecticides in order to preserve at crop reproductive stage. natural biological control agents. 20 or more caterpillars C. includens e A. gemmatalis ≥1.5cm/meter (ground cloth). When more than 50% of the caterpillars are smaller than 1.5 cm, the use of virus, bacteria or 4 or more caterpillars/meter (ground insecticide of the growth cloth) at crop vegetative stage. regulator group (IGR) should be Caterpillars of the subfamily favored. Heliothinae (Helicoverpa and Heliothis genus) When more than 50% of the caterpillars are equal or bigger 2 or more caterpillars/meter (ground than 1.5 cm, the use of cloth) at crop reproductive stage. insecticides with higher knockdown effect should be favored. Always favor the use of soft Caterpillars of the genus 10 or more caterpillars insecticides in order to preserve Spodoptera ≥1.5cm/meter (ground cloth). natural biological control agents.

A refuge is a system of growing a necessary to ensure that the Bt plants and the percentage of the area (in the same field) with the IPM work together, rather than compete, in non-Bt version of the same crop (preferably one managing pests more appropriately. isoline) in order to reduce the selection of It is important to note that, in general, the resistant insects to that technology. It is most appropriate insecticides to control important to be clear that in the area of refuge, caterpillars in soybeans are those that combine insects (targets of the Bt plant) susceptible to the good efficiency in controlling target pests and toxin need to complete their lifecycle. This will high selectivity against beneficial insects (bees, enable them to cross with possible resistant insect predators, and parasitoids of pests). insects from the Bt area, thereby producing Insecticides from the insect growth regulators heterozygous insects that can be controlled by group, biological products based on virus or the Bt plant. In this regard, overuse of insecticides bacteria (Bt), and some new groups of insecticides in the refuge area; annihilating the population of such as spinosyns and diamides may be better insects; is unacceptable. The refuge area insecticides. On the other hand, insecticides such management must be within the IPM guidelines. as pyrethroids, carbamates, and Technologies such as ground cloth sampling and organophosphates are more noxious to beneficial application of insecticides only when pest and therefore, should be replaced population reaches the ET remain essential in the whenever possible. Furthermore, it is important refuge area as well as in the Bt area. It is to "rotate" the use of insecticides with different

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Pomari-Fernandes et al / Current Agricultural Science and Technology 21 (2015) 1-7 modes of action. This will reduce the selection of in avoiding, or at the least in delaying the loss of resistant insects for a particular insecticide. It is this technology to insect resistance. We might especially important for H. armigera that are very have a chance today to fully implement IPM in easily selected to insecticide resistance (Tay et al. Brazil as it has never been done or seen before in 2013). Furthermore, the use of insecticides based the history of tropical agriculture. If IPM is on a calendar or to coincide with the application adopted successfully in Brazil, the future of herbicides or fungicides is unacceptable. It perspective of H. armigera will be that of being should be avoided to prevent the long-term satisfactory managed like any other pest. intensification of pest problem, mainly due to the Alternatively, if we try to fool ourselves with suppression of natural enemies, selection of simplified version of IPM, H. armigera and many resistant insect lines, and increase in secondary other pests will have a great chance to win the pests. battle against growers and severe damage to Therefore, it is of great importance that crops will occur. different control methods remain available for soybean producers. The integration of these REFERENCES different controls in a harmonic way is crucial for successful pest management. Therefore, even in the era of biotechnology, biological control, Agropec Consultoria. Pragas quarentenárias: pesticides, and other pest control tactics will consulta aos dados sobre pragas quarentenárias continue to be of great importance in controlling presentes e ausentes para o Brasil. 2013. pests such as H. armigera. Available: http://spp.defesaagropecuaria.com/. Accessed 16 April 2014. Helicoverpa armigera: FUTURE PERSPECTIVES IN BRAZIL Bueno AF, Batistela MJ, Bueno RCOF, França-Neto JB, Nishikawac MAN, Filho AL (2011) Effects of Even though H. armigera has triggered integrated pest management, biological control economic losses and an increased use of and prophylactic use of insecticides on the insecticides in its first year in Brazil, this pest can management and sustainability of soybean. Crop be managed with the correct adoption of IPM. Protection, 30: 937-945. The adoption of IPM with the rational use of low- Bueno AF, Sosa-Gómez DR, Mikami AY, Pomari- environmental impact insecticides allows the Fernandes A, Bortolotto OC (2014) Mais temidas. application of detrimental chemical products on Caderno Técnico Cultivar Grandes Culturas Julho crop fields to be reduced (Meissle et al. 2010; 1-11. Tang et al. 2010). In this context, regular Bueno AF, Roggia S, Sosa-Gómez DR, Hoffmann- monitoring of pests and initiating control Campo CB, Bueno RCOF, Pomari AF (2013) Mitos e measures only when the pest populations or Verdades. Cultivar Grandes Culturas, 176: 17-21. percent defoliation reach the ET recommended by research is crucial. These procedures protect crop Bueno AF, Panizzi AR, Côrrea-Ferreira BS, sustainability, thus keeping the soybean growers Hoffman-Campo CB, Sosa-Gómez DR, Gazzoni DL, competitive in the market while reducing costs et al. Histórico e evolução do manejo integrado de and maximizing productivity (Bueno et al. 2011; pragas da soja no Brasil. In: Hoffman-Campo CB, Meissle et al. 2010). Corrêa-Ferreira BS, Moscardi F (Eds.) Soja: Manejo The next years will be the era of integrado de insetos e outros artrópodes-praga. biotechnology in pest management. However, for Brasília, DF: Embrapa, 2012. cap. 1. p. 37-74. this new technology (Bt plants) to succeed, IPM adoption is very important since it will be enable 6

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