ABSTRACT:

Spodoptera cosmioides Walker is a polyphagous insecticide-resistant species found in various regions of Brazil. Despite occurring at low densities, it is considered a potential pest of cotton, soybean, and bean crops in the Brazilian cerrado. This work investigated the comparative biology of S. cosmioides in the commercial transgenic cotton NuOPAL (Bollgard I, Evento 531) and the conventional isoline variety DeltaOPAL. The experiment was conducted under laboratory conditions (26 ± 1°C; relative humidity: 70 ± 10%; photoperiod: 12h), using newly-hatched and individualized larvae. We evaluated the duration and viability of immature stages, duration of the biological cycle, pupal weight, sex ratio, percentage of deformed adults and of adults trapped in the pupal case, adult longevity, fecundity, and egg viability. The biological parameters observed showed no significant differences between the two varieties studied, which enabled high consumption, high assimilation, high fecundity, and viability for S. cosmioides.

KEYWORDS:
Gossypium hirsutum; transgenic plants; Bollgard; CryIAc

RESUMO:

Spodoptera cosmioides Walker é uma espécie polífaga, resistente a inseticidas em várias regiões do país e, apesar de ocorrer em baixas densidades, é considerada uma praga potencial para as culturas de algodão, soja e feijão no cerrado. Neste trabalho, estudou-se a biologia comparada de S. cosmioides sobre o cultivar transgênico comercial de algodoeiro NuOPAL (Bollgard I, Evento 531) e sobre o cultivar isolinha convencional DeltaOPAL. O experimento foi desenvolvido em condições de laboratório (26 ± 1°C; UR: 70 ± 10%; fotofase: 12h) a partir de lagartas recém-eclodidas e individualizadas. Foram avaliados a duração e a viabilidade das fases imaturas, a duração do ciclo biológico, o peso de pupas, a razão sexual, a porcentagem de deformação de adultos e de adultos não liberados dos invólucros pupais, a longevidade de adultos, a fecundidade e viabilidade de ovos. Os parâmetros biológicos observados não diferiram significativamente em relação às duas cultivares, que proporcionaram alto consumo, alta assimilação, alta fecundidade e viabilidade à S. cosmioides.

PALAVRAS-CHAVE:
Gossypium hirsutum; planta transgênica; Bollgard; CryIAc

INTRODUCTION

Cotton production in Brazil has increased considerably with the advancement of technology, allowing the country to move from being the world’s largest importer to the second largest exporter in 12 years (ABRAPA, 2016ASSOCIAÇÃO BRASILEIRA DOS PRODUTORES DE ALGODÃO (ABRAPA). O algodão no Brasil. Associação Brasileira dos Produtores de Algodão. 2015. Available from: Available from: http://www.abrapa.com.br/estatisticas/Paginas/Algodao-no-Brasil.aspx . Access on: Sep. 19 2016.
http://www.abrapa.com.br/estatisticas/Pa... ; SEVERINO et al. 2019SEVERINO, L.S.; RODRIGUES, S.M.M.; CHITARRA, L.G.; LIMA FILHO, J.; CONTINI, E.; MOTA, M.; MARRA, R.; ARAÚJO, A. Produto: ALGODÃO - Parte 01: Caracterização e Desafios Tecnológicos. Série Desafios do Agronegócio Brasileiro (NT3). EMBRAPA Algodão. 2019. Available from: Available from: https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109655/1/SerieDesafiosAgronegocioBrasileiroNT3Algodao.pdf . Access on: Jan. 20 2020.
https://www.alice.cnptia.embrapa.br/alic... ). With an average production volume close to 2.7 million tons (CONAB, 2019COMPANHIA NACIONAL DE ABASTECIMENTO (CONAB). Planilhas de custo de produção. Séries históricas. 2019. Available from: Available from: https://www.conab.gov.br/info-agro/custos-de-producao/planilhas-de-custo-de-producao/itemlist/category/414-planilhas-de-custos-de-producao-series-historicas . Access on: May 26 2019.
https://www.conab.gov.br/info-agro/custo... ), the country ranks among the top five world producers alongside countries like India, China, Pakistan, and the USA (SEVERINO et al. 2019SEVERINO, L.S.; RODRIGUES, S.M.M.; CHITARRA, L.G.; LIMA FILHO, J.; CONTINI, E.; MOTA, M.; MARRA, R.; ARAÚJO, A. Produto: ALGODÃO - Parte 01: Caracterização e Desafios Tecnológicos. Série Desafios do Agronegócio Brasileiro (NT3). EMBRAPA Algodão. 2019. Available from: Available from: https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109655/1/SerieDesafiosAgronegocioBrasileiroNT3Algodao.pdf . Access on: Jan. 20 2020.
https://www.alice.cnptia.embrapa.br/alic... ).

Insect pests are an important agronomic problem in this crop, causing great economic damage annually. The use of chemical products for pest control can reach up to 25% of the production cost (EMBRAPA MEIO AMBIENTE, 2016EMBRAPA MEIO AMBIENTE. Algodão Bt. 2016. Available from: Available from: http://www.cnpma.embrapa.br/projetos/index.php3?sec=bioss:::23 . Access on: Sep. 19 2016.
http://www.cnpma.embrapa.br/projetos/ind... ).

The availability of genetically modified cotton cultivars represented a significant advance in pest control in the last two decades (SANTOS; TORRES, 2010SANTOS, R.L.; TORRES, J.B. Produção da proteína Cry1Ac em algodão transgênico e controle de lagartas. Revista Brasileira de Ciências Agrárias, v.5, p.509-517, 2010.). Genetically modified plants increase production (BETZ et al., 2000BETZ, F.S.; HAMMOND, B.G.; FUCHS, R.L. Safety and advantages of Bacillus thuringiensis: protected plants to control insect pests. Regulatory Toxicology and Pharmacology, v.32, n.2, p.156-173, 2000. https://doi.org/10.1006/rtph.2000.1426
https://doi.org/https://doi.org/10.1006/... ), lower levels of mycotoxins (DOWD, 2000DOWD, P.F. Indirect reduction of ear molds and associated mycontoxins in Bacillus thuringiensis corn under controlled and open field conditions: utility and limitations. Journal of Economic Entomology, v.93, n.6, p.1669-1679, 2000. https://doi.org/10.1603/0022-0493-93.6.1669
https://doi.org/https://doi.org/10.1603/... ), and reduce the use of insecticides (ROMEIS et al., 2006ROMEIS, J.; MEISSLE, M.; BIGLER, F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology, v.24, n.1, p.63-71, 2006. https://doi.org/10.1038/nbt1180
https://doi.org/https://doi.org/10.1038/... ) while favoring the maintenance of natural enemies (GOULD, 1998GOULD, F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology, v.43. p.701-726, 1998. https://doi.org/10.1146/annurev.ento.43.1.701
https://doi.org/https://doi.org/10.1146/... ), in addition to helping in pest control and contributing to delay the evolution of resistance (MASCARENHAS; LUTTRELL, 1997MASCARENHAS, V.J.; LUTTRELL, R.G. Combined effect of sublethal exposure to cotton expressing the endotoxin protein of Bacillus thuringiensis and natural enemies on survival of bollworm (Lepidoptera: Noctuidae) larvae. Environmental Entomology, v.26, n.4, p.939-945, 1997. https://doi.org/10.1093/ee/26.4.939
https://doi.org/https://doi.org/10.1093/... ). Therefore, the use of genetically modified cultivars is considered a tactic compatible with the Integrated Pest Management of cotton crops.

Genetically modified plants with the genes of Bacillus thuringiensis var. kurstaki (Bt) express toxic proteins (alpha-endotoxins) during sporulation, which have a lethal effect when ingested by Diptera and Lepidoptera larvae (SCHNEPF et al., 1998SCHNEPF, E.; CRICKMORE, N.; VAN RIE, J.; LERECLUS, D.; BAUM, J.; FEITELSON, J.; ZEIGLER D.R.; DEAN, D. H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews, v.62, n.3, p.775-806, 1998.). The first commercial transgenic cotton (Bt) cultivar, known as Bollgard or Bollgard I, was produced in 1989 and commercially released in the USA and Australia in 1996/97. In Brazil, its release occurred in 2005 (CTNBio, 2005COMISSÃO TÉCNICA NACIONAL DE BIOSSEGURANÇA (CTNBIO). Parecer Técnico prévio conclusivo nº 513/2005. In: REUNIÃO ORDINÁRIA DA CTNBIO, 86., [S.l.]. 2005. 53p.). Until 2013, the planting of transgenic cotton cultivars in Brazil corresponded to 47% of the planted area (GRAVINA, 2013GRAVINA, M. Uma década de transgênicos no Brasil: avanços e perspectivas. Monsanto em campo. 2013. Available from: Available from: http://www.portaldoagronegocio.com.br/artigo/uma-decada-de-transgenicos-no-brasil-avancos-e-perspectivas-3582 . Access on: Sep. 19 2016.
http://www.portaldoagronegocio.com.br/ar... ). Brazil currently has about 940 thousand ha planted with transgenic cotton (ISAAA, 2017INTERNATIONAL SERVICE FOR THE ACQUISITION OF AGRI-BIOTECH APPLICATIONS (ISAAA). Situação global dos cultivos transgênicos em 2017 (resumo executivo). 2017. Available from: Available from: https://cib.org.br/isaaa-2018/ . Access on: May 06 2019.
https://cib.org.br/isaaa-2018/... ).

Bollgard I (NuOPAL) cotton expresses the Cry1Ac protein, which provides resistance to some caterpillars that attack cotton crops in Brazil: Heliothis virescens (tobacco budworm), Pectinophora gossypiella (pink bollworm), and Alabama argillacea (cotton leafworm) (BARROSO; HOFFMANN, 2007BARROSO, P.A.V.; HOFFMANN, L.V. Algodoeiro geneticamente modificado. In: FREIRE, E.C. (Ed.). Algodão no Cerrado do Brasil. Brasília: Associação Brasileira de Produtores de Algodão, 2007. p.141-174.). Currently, Bollgard II cotton is available in Brazil and expresses two Bt proteins, Cry1Ac and Cry2Ab2, both specific and toxic to some caterpillars.

Cry1Ac toxicity is not effective in suppressing Spodoptera frugiperda and S. eridania (ADAMCZYK et al., 1998ADAMCZYK, J.J.; MASCARENHAS, V.J.; CHURCH, G.E.; LEONARD, B.R.; GRAVES, J.B. Susceptibility of conventional and transgenic cotton bolls expressing the Bacillus thuringiensis Cry1Ac δ-endotoxin to fall armyworm (Lepidoptera: Noctuidae) and beet armyworm (Lepidoptera: Noctuidae) injury. Journal of Agricultural Entomology, v.15, n.3, p.163-171, 1998.), increasing the tolerance of these species to the consumption of this cultivar (ADAMCZYK; SUMERFORD, 2001ADAMCZYK, J.J.; SUMERFORD, D.V. Potential factors impacting season-long expression of Cry1Ac in 13 commercial varieties of Bollgard cotton. Journal of Insect Science, v.1, p.1-6, 2001.). Consequently, outbreaks of these pest species in Bollgard cotton require applications of foliar insecticides to keep these populations below the level of economic damage (HOOD, 1997HOOD, E. The fall armyworm: and I thought I had it made. In: BELTWIDE COTTON CONFERENCES. Proceedings…New Orleans: National Cotton Council , 1997. p.1223-1224.; SMITH, 1997SMITH, R.H. An extension entomologist’s 1996 observations of Bollgard (Bt) technology. In: BELTWIDE COTTON CONFERENCES. Proceedings…New Orleans: National Cotton Council , p. 856-857, 1997.).

The joint expression of Cry1Ac and Cry2Ab2 proteins (Bollgard II) suppresses populations of the Spodoptera and Helicoverpa species (MONSANTO, 2016MONSANTO 2016. BOLLGARD II RR FLEXTM. Manual técnico do produto. Available from: Available from: http://www.bollgard2rrflex.com.br/wp-content/uploads/2014/01/manual-bollgard-2-rr372 flex.pdf . Access on: Sep. 20 2016.
http://www.bollgard2rrflex.com.br/wp-con... ). Different pest species present distinct responses to the use of Bt technologies since mortality varies according to the target species and the expressed proteins. ADAMCZYK et al. (2008ADAMCZYK, J.J.; GREENBERG, S.; ARMSTRONG, S.; MULLINS, W.J.; BRAXTON, L.B.; LASSITER, R.B.; SIEBERT, M.W. Evaluation of Bollgard® II and WideStrike™ technologies against beet and armyworms. In: BELTWIDE COTTON CONFERENCES, Proceedings… New Orleans: National Cotton Council, 2008. p.1049.) evaluated the Bollgard I, Bollgard II, and WideStricke technologies regarding the mortality of S. frugiperda and S. eridania and reported that the different species presented distinct responses to the cultivars.

Spodoptera cosmioides has been reported as a species with high damage potential for several important crops due to its high polyphagy and voracity (QUINTELA et al., 2007QUINTELA, E.D.; TEIXEIRA, S.M.; FERREIRA, S.B.; GUIMARÃES, W.F.F.; OLIVEIRA, L.F.C.; CZEPAK, C. Desafios do manejo integrado de pragas da soja em grandes propriedades no Brasil Central. Embrapa Arroz e Feijão, 2007. (Comunicado Técnico 149).; FARIA, 2010FARIA, C. Lagarta preta é novo tipo de praga que ataca a soja. Jornal Correio do Estado, Campo Grande, 05 abr. 2010. Available from: Available from: https://www.correiodoestado.com.br/noticias/lagarta-preta-e-novo-tipo-de-praga-que-ataca-a-soja/3270/ . Access on: Sep. 20 2016.
https://www.correiodoestado.com.br/notic... ; LINK, 2010LINK, D. Escuras e vorazes. Cultivar Grandes Culturas, v.129, p.18-20, 2010. Avaliable from: Avaliable from: https://www.grupocultivar.com.br/revistas/225 . Access on: May 26 2019
https://www.grupocultivar.com.br/revista... ). Despite its high degree of polyphagy, it is considered a pest in some crops, especially in those that use excessively broad-spectrum insecticides (HABIB et al., 1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ). S. cosmioides, together with S. eridania, form the main group of caterpillars that attack soybean pods, assuming importance from the beginning of the reproductive phase of this crop (GAZZONI; YORINORI, 1995GAZZONI, D.L.; YORINORI, J.T. Manual de identificação de pragas e doenças da soja. Brasília: EMBRAPA-SPI. 1995. (Manuais de Identificação de Pragas e Doenças, 1).). In addition, in the states of São Paulo, Paraná, and Santa Catarina, outbreaks of this insect caused severe damage to crops of economic interest, such as cotton and soy (HABIB et al., 1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ), apple (NORA; REIS FILHO, 1988NORA, I.; REIS-FILHO, W. Damage to apple (Malus domestica, Bork.) caused by Spodoptera spp. (Lepidoptera: Noctuidae). Acta Horticultura, v.232, p.209-212, 1988. https://doi.org/10.17660/ActaHortic.1988.232.28
https://doi.org/https://doi.org/10.17660... ), and onion (BAVARESCO et al., 2003BAVARESCO, A.; GARCIA, M.S.; GRÜTZMACHER, A.D.; FORESTI, J.; RINGENBERG, R. Biologia comparada de Spodoptera cosmioides (Walk.) (Lepidoptera: Noctuidae) em cebola, mamona, soja e feijão. Ciência Rural, v.33, n.6, p.993-998, 2003. https://doi.org/10.1590/S0103-84782003000600001
https://doi.org/https://doi.org/10.1590/... ).

PORTILLO et al. (1991PORTILLO, H.E.; PITRE, H.N.; MECKENSTOCK, D.; ANDREWS, K.L. Langosta: a lepidopterous pest complex (Lepidoptera: Noctuidae) on sorghum and maize in Honduras. Florida Entomologist, v.74, n.2, p.287-296, 1991. https://doi.org/10.2307/3495308
https://doi.org/https://doi.org/10.2307/... ; 1996PORTILLO, H.E.; PITRE, H.N.; MECKENSTOCK, D.H.; ANDREWS, K.L. Oviposition preference of Spodoptera latifascia (Lepidoptera: Noctuidae) for sorghum, maize and non-crop vegetation. Florida Entomologist, v.79, n.4, p.552-562, 1996. https://doi.org/10.2307/3496068
https://doi.org/https://doi.org/10.2307/... ) associated the most significant damages of this insect to corn crops cultivated in areas that adopted weed chemical control, since these weeds were used as food by caterpillars. LEITE et al. (2008LEITE, R.M.V.B.C.; CASTRO, C.; ZITO, R.K. (Eds.) Girassol no Brasil. Londrina: Embrapa Soja, 2005. (Embrapa Soja. Documentos, 298).) reported a strong outbreak of S. cosmioides in the 2007 sunflower harvest, leading to the loss of significant areas of this crop in Goiás, mainly in the south of the state.

Despite its potential as a pest of various important crops, knowledge about the S. cosmioides biology in cotton cultivars is still insufficient. With the introduction of new cultivars and the increased adoption of crops with transgenic varieties, it is essential to know their influence on the biological cycle of the insect, mainly to provide information about larval survival or viability and monitor the emergence of populations resistant to these plants.

The knowledge of insect biology is fundamental for the development of effective management strategies, following the Integrated Pest Management (PARRA, 2000PARRA, J.R.P. A biologia de insetos e o manejo de pragas: Da criação em laboratório à aplicação em campo. In: GUEDES, J.V.C.; COSTA, I.D.; CASTIGLIONI, E. Bases e técnicas do manejo de insetos. Santa Maria: UFSM/CCR/DFS; Pallotti, 2000. p.1-29.). Thus, the present study aimed to compare biological aspects of S. cosmioides in the transgenic cotton cultivar NuOPAL (Bollgard I) and the non-genetically modified isoline cultivar DeltaOPAL.

MATERIAL AND METHODS

This research was carried out at the Biological Control Laboratory of the Phytosanitary Department of the School of Agricultural and Veterinary Studies (Faculdade de Ciências Agrárias e Veterinárias - FCAV) of Universidade Estadual Paulista (UNESP), Jaboticabal campus, using refrigerated incubators (BOD) maintained at a temperature of 25 ± 1°C, 70 ± 10% relative humidity, and 12 hours of photoperiod in all laboratory tests.

The commercial cultivars used in this work were DeltaOPAL and NuOPAL. The leaves used to feed the caterpillars during the experiments were obtained from cultivars planted in a field following agronomic recommendations normally used in cotton cultivation.

Rearing S. cosmioides in laboratory conditions

S. cosmioides caterpillars were collected in cotton cultivar DeltaPine Acala 90, established in the experimental area of UNESP, Jaboticabal campus. The insects were placed in plastic containers (12 cm diameter × 9 cm height) with their base covered with filter paper and the top closed with a voile cover to provide aeration and prevent the harmful proliferation of microorganisms. The caterpillars fed on cotton leaves from the cultivar DeltaPine Acala 90, collected from the upper third of the plants, washed in a 0.15% sodium hypochlorite solution and then with abundant water. The choice of cultivar aimed to avoid possible pre-imaginal conditioning in the subsequent tests with the other cultivars (Bt cultivar and its isoline). The leaves were changed according to the consumption by the caterpillars so that there was no lack of food.

Pupae were separated by sex, according to BUTT; CANTU (1962BUTT, B.A.; CANTU, E. Sex determination of lepidopterous pupae. Washington: United States Department of Agriculture, 1962. (Agricultural Research Service, ARS 33-75).). Ten newly hatched females and males were placed in cylindrical PVC cages (20 cm height × 19.5 cm diameter) with the base sealed with polyethylene discs (21.5 cm diameter) and the top covered with voile fixed by elastics to promote the emergence and reproduction of adults. These cages were internally covered with white paper, where the females laid eggs.

The adults were fed a 10% honey solution absorbed in hydrophilic cotton placed on a plastic lid (4.5 cm diameter) at the bottom of the cage.

Papers with eggs were removed from the cages daily, and the eggs were placed in a plastic container covered with voile. After the caterpillars hatched, cotton leaves from the cultivar DeltaPine Acala 90 were supplied, as previously mentioned.

Biological parameters of S. cosmioides fed with conventional and transgenic cotton leaves

We used a completely randomized design (CRD) with two treatments consisting of the cotton genotypes DeltaOpal and NuOpal (Bollgard I), each with 40 repetitions (neonate caterpillars) to assess the duration and viability of immature stages and 10 repetitions (10 couples individualized in cages) for parameters related to the adult phase, such as longevity and reproduction.

Insects from the F2 generation of laboratory rearing were used to evaluate the biological parameters of the larval phase. After hatching, the caterpillars were separated in Petri dishes lined with filter paper and kept on leaves of the cultivars analyzed, with this food always available. These Petri dishes were cleaned daily with the removal of feces and changing of the filter paper.

The pupae were weighed and separated by sex (according to BUTT; CANTU, 1962BUTT, B.A.; CANTU, E. Sex determination of lepidopterous pupae. Washington: United States Department of Agriculture, 1962. (Agricultural Research Service, ARS 33-75).) 24 hours after pupation and transferred to plastic containers (7.5 cm diameter × 5 cm height) where they remained until emerging as adults. The sex ratio was obtained using the formula proposed by SILVEIRA NETO et al. (1976SILVEIRA NETO, S.; NAKANO, O.; BARBIN, D.; VILLA NOVA, N.A. Manual de Ecologia dos insetos. São Paulo: Agronômica Ceres, 1976.).

To analyze the biological parameters of adults, each repetition consisted of placing a couple of S. cosmioides in a cylindrical PVC cage (20 cm height × 19.5 diameter) lined with white paper (for egg-laying), with the base sealed with polyethylene discs (21.5 cm diameter) lined with filter paper and the top covered with voile fixed with elastics.

We evaluated the duration and viability of immature stages, duration of the life cycle, pupal weight, sex ratio, percentage of deformed adults and of adults trapped in the pupal case, adult longevity, fecundity, and egg viability.

The data gathered from the different biological parameters were analyzed by the F test (ANOVA), and the treatment means were compared using the Tukey test at a 5% probability level in the ASSISTAT 7.7 software.

RESULTS AND DISCUSSION

The mean duration of the larval phase was approximately 25 days in both cultivars (Table 1), with 100% viability in caterpillars fed with leaves of the cultivar NuOPAL and 90% in those fed with DeltaOPAL (Table 2). HABIB et al. (1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ) identified a shorter duration of the larval phase of S. ­cosmioides reared in the cultivar IAC-20 - 13.4 days to complete the phase in the temperature range of 22.3 - 30.4°C, with 95% viability. SARRO (2006SARRO, F. B. Biologia comparada de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em milho e em cultivares de algodoeiro. 2006. viii, 98 f. Thesis (Doctor’s degree) - Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, 2006. Available from: Available from: https://repositorio.unesp.br/bitstream/handle/11449/105423/sarro_fb_dr_botfca.pdf?sequence=1&isAllowed=y . Access on: May 26 2019.
https://repositorio.unesp.br/bitstream/h... ) studied the biology of Spodoptera frugiperda in cotton and detected a larval phase of 22 days in the cultivar DeltaOPAL, with 100% viability.

BAVARESCO et al. (2003BAVARESCO, A.; GARCIA, M.S.; GRÜTZMACHER, A.D.; FORESTI, J.; RINGENBERG, R. Biologia comparada de Spodoptera cosmioides (Walk.) (Lepidoptera: Noctuidae) em cebola, mamona, soja e feijão. Ciência Rural, v.33, n.6, p.993-998, 2003. https://doi.org/10.1590/S0103-84782003000600001
https://doi.org/https://doi.org/10.1590/... ) found a significant difference in the duration of the larval phase of S. cosmioides among different host plants - 20.2 days for castor oil plant, 22.3 days for onion, and 28 days for soybean, with viability of 77.3, 74.0, and 45.3%, respectively. The results obtained in this work and those cited in the literature demonstrate that caterpillars of the genus Spodoptera, especially S. cosmioides, develop better by feeding on cotton leaves than on soybean leaves, which is a crop frequently associated with this species.

The average duration of the pre-pupa phase was two days in both cultivars, with 100% viability (Table 1). This value is higher than that found for S. cosmioides in the cultivar IAC-20, with 1.3 and 1.4 days for males and females, respectively (HABIB et al., 1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ). Working with S. frugiperda, SARRO (2006SARRO, F. B. Biologia comparada de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em milho e em cultivares de algodoeiro. 2006. viii, 98 f. Thesis (Doctor’s degree) - Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, 2006. Available from: Available from: https://repositorio.unesp.br/bitstream/handle/11449/105423/sarro_fb_dr_botfca.pdf?sequence=1&isAllowed=y . Access on: May 26 2019.
https://repositorio.unesp.br/bitstream/h... ) obtained a similar result - 2.3 days for the pre-pupal phase in the DeltaOPAL cultivar, with 100% viability.

The pupal phase lasted, on average, 13.6 days in the cultivar DeltaOPAL and 13.1 days in NuOPAL, with 69.4 and 77.5% viability, respectively (Table 1). HABIB et al. (1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ) noted a shorter duration (9.5 days) in the cultivar IAC-20, while SARRO (2006SARRO, F. B. Biologia comparada de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em milho e em cultivares de algodoeiro. 2006. viii, 98 f. Thesis (Doctor’s degree) - Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, 2006. Available from: Available from: https://repositorio.unesp.br/bitstream/handle/11449/105423/sarro_fb_dr_botfca.pdf?sequence=1&isAllowed=y . Access on: May 26 2019.
https://repositorio.unesp.br/bitstream/h... ) identified a mean duration of 10 days for the pupal phase of S. frugiperda in the DeltaOPAL cultivar, with 92% viability.

The average pupal weight in both cultivars was approximately 450 mg (Table 1). This result is much higher than that found by HABIB et al. (1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ), who detected an average weight of 249 mg in the cultivar IAC-20. SARRO (2006SARRO, F. B. Biologia comparada de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) em milho e em cultivares de algodoeiro. 2006. viii, 98 f. Thesis (Doctor’s degree) - Universidade Estadual Paulista, Faculdade de Ciências Agronômicas, 2006. Available from: Available from: https://repositorio.unesp.br/bitstream/handle/11449/105423/sarro_fb_dr_botfca.pdf?sequence=1&isAllowed=y . Access on: May 26 2019.
https://repositorio.unesp.br/bitstream/h... ) reported low average weight, around 184 mg, for S. frugiperda fed with the cultivar DeltaOPAL. The high viability in the larva and pupa phases and the expressive weight gain in the pupa phase indicate that the cultivars analyzed are well accepted for consumption by the caterpillars and have high assimilation in the immature stages of S. cosmioides.

The duration of the S. cosmioides larva-adult period was approximately 40 days in the two cultivars analyzed (Table 1).

The sex ratio was 0.40 in the cultivar DeltaOPAL and 0.45 in NuOPAL, not affecting the proportion of emergence between sexes, which was around 1:1 in the studied cultivars.

As for adult longevity, females were more long-lived than males, presenting a mean of approximately 8.5 days, 2 days longer than males (Table 2). HABIB et al. (1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ) identified higher longevity (13.2 days) when the caterpillars fed on leaves of the cultivar IAC-20.

Total fecundity varied between 1541.1 and 1910.7 eggs in the cultivars DeltaOPAL and NuOPAL, respectively (Table 2), although these results did not differ statistically at the 5% probability level. HABIB et al. (1982HABIB, M.E.M.; PALEARI, L.M.; AMARAL, M.E.C. Effect of three larval diets on the development of the armyworm, Spodoptera latifascia Walker, 1856 (Noctuidae, Lepidoptera). Revista Brasileira de Zoologia, v.1, n.3, p.177-182, 1982. https://doi.org/10.1590/S0101-81751982000300007
https://doi.org/https://doi.org/10.1590/... ) reported a lower total reproductive capacity for S. cosmioides, with 1309 eggs per female, on average, in the cotton cultivar IAC-20. In a study on lepidopteran biology, JOHANSSON (1964JOHANSSON, A.S. Feeding and nutrition in reproductive processes in insects. Symposia of the Royal Entomological Society of London, v. 2, p. 43-55, 1964.) stated that feeding different cultivars of the same plant species to the insects can influence egg-laying. Also, according to this author, the variation in the amount of food consumed or even physical or chemical differences in the food are responsible for these effects on reproduction.

The cotton cultivar NuOPAL presented the highest percentage of deformed adults (29%) and adults trapped in the pupal case (13%) (Table 2). This finding demonstrates that, although the caterpillars fed heavily on this cultivar, this consumption probably led to nutritional deficiencies or compounds harmful to the development of S. cosmioides. LARA (1991LARA, F.M. Princípios de resistência de plantas a insetos. São Paulo: Ícone, 1991.) points out that nutritional inadequacy generally influences the reproductive capacity of females, resulting in reduced fertility, in addition to affecting the mortality rate in the metamorphosis to the adult phase. New studies should be conducted to investigate the action of the cultivar NuOPAL on the physiology of the adult S. cosmioides.

CONCLUSIONS

The results obtained for all parameters analyzed in the two cultivars did not show a statistically significant difference at the 5% probability level. Thus, we can conclude that the consumption of the NuOPAL and DeltaOPAL cultivars does not harm the survival and reproduction of this insect.

The NuOPAL and DeltaOPAL cotton cultivars fed to the caterpillars acted similarly on the biology of S. ­cosmioides, providing high viability, high fecundity, and similar duration of life stages. In addition, leaf consumption of both cultivars was high during the larval phase. As this is the stage in which S. cosmioides damages the cotton crop, outbreaks of this insect would justify the use of foliar insecticides, which would not be desirable from an economic point of view. Furthermore, the inefficacy of the Cry1Ac endotoxin expressed by NuOPAL (Bollgard I) in suppressing the larval phase of S. cosmioides may select this species, which, on a longer-term, could become more prevalent in crops since they have several hosts widely grown during the year and could migrate between them.

Acknowledgements:

Not applicable.

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