Characterizing the differential susceptibility and resistance to insecticides in populations of Chrysodeixis includens and Rachiplusia nu (Lepidoptera: Noctuidae) in Brazil.

Publisher: Published for SCI by Wiley Country of Publication: England NLM ID: 100898744 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1526-4998 (Electronic) Linking ISSN: 1526498X NLM ISO Abbreviation: Pest Manag Sci Subsets: MEDLINE

Original Publication: West Sussex, UK : Published for SCI by Wiley, c2000-

Moths*/drug effects ; Moths*/growth & development ; Insecticides*/pharmacology ; Insecticide Resistance*; Animals ; Brazil ; Larva/growth & development ; Larva/drug effects ; Glycine max

Background: Chrysodeixis includens (Walker) and Rachiplusia nu (Guenée) are major Plusiinae pests of soybean in the Southern Cone region of South America. In recent decades, C. includens was the main defoliator of soybean in Brazil, but from 2021 onwards, R. nu emerged as an important soybean pest in various regions of the country. Here, we characterize the differential susceptibility and resistance to insecticides in these Plusiinae pests from two soybean regions of Brazil.
Results: Except for spinetoram and chlorfenapyr (comparable lethality against both species) and a Bt-based biopesticide (more lethal for C. includens), the tested insecticides showed higher lethality against R. nu than against C. includens, but populations of the same species, even separated by long distances, presented similar resistance levels. For both species, the 90% lethal concentration (LC 90 ) values of most insecticides were higher than the field-recommended dose. Nevertheless, the field-recommended doses of spinetoram, metaflumizone, emamectin benzoate, cyclaniliprole and chlorfenapyr showed comparable control efficacy against both species, whereas indoxacarb, chlorantraniliprole, flubendiamide, teflubenzuron and chlorfluazuron were more lethal for R. nu, and methoxyfenozide and the Bt-based insecticide were more lethal for C. includens. Thiodicarb, methomyl and lambda-cyhalothrin showed low lethality against both species.
Conclusions: Large interspecific differences in the susceptibility to insecticides was found in major Plusiinae pests of soybean in Brazil. Furthermore, variations in susceptibility to insecticides occurred consistently among species and populations, regardless of the collection site and thus despite unequal temporal and spatial exposure to insecticides. These results demonstrate that accurate species identification is essential for effective control of Plusiinae in soybean. © 2024 Society of Chemical Industry.
(© 2024 Society of Chemical Industry.)

Panizzi AR, History and contemporary perspectives of the integrated pest management of soybean in Brazil. Neotrop Entomol 42:119–127 (2013).
Silva SS, Erick MG, Cordeiro JB, de Paiva PM, Dourado RA, Carvalho GH et al., Population expansion and genomic adaptation to agricultural environments of the soybean looper, Chrysodeixis includens. Evol Appl 13:2071–2085 (2020).
Formentini AC, Sosa‐Gómez DR, de Paula‐Moraes SV, de Barros NM and Specht A, Lepidoptera (Insecta) associated with soybean in Argentina, Brazil, Chile and Uruguay. Ciênc Rural 45:2113–2120 (2015).
Dami LC, Herrero MI, Casmuz AS, Alzogaray RA and Gastaminza GA, Fitness and mating compatibility of Chrysodeixis includens (W.) (Lepidoptera: Noctuidae) populations collected in different provinces and crops in Argentina, in Proceeding of the 93rd Brazilian Academy of Sciences, Vol. 93. SciELO Brasil, Rio de Janeiro, p. e20190523 (2021).
Nagoshi RN, Davis JA, Meagher RL, Musser FR, Head GP, Portillo H et al., Evidence for two soybean looper strains in the United States with limited capacity for cross‐hybridization. Genes 14:1509 (2023).
Andrade K, Bueno AF, da Silva DM, Stecca CS, Pasini A and de Oliveira MCN, Bioecological characteristics of Chrysodeixis includens (Lepidoptera: Noctuidae) fed on different hosts. Austral Entomol 55:449–454 (2016).
Marques LH, Castro BA, Rossetto J, Silva OA, Moscardini VF, Zobiole LH et al., Efficacy of soybean's event DAS‐81419‐2 expressing Cry1F and Cry1Ac to manage key tropical lepidopteran pests under field conditions in Brazil. J Econ Entomol 109:1922–1928 (2016).
Muraro DS, Giacomelli T, Stacke RF, Godoy DN, Marçon P, Popham HJR et al., Baseline susceptibility of Brazilian populations of Chrysodeixis includens (Lepidoptera: Noctuidae) to C. Includens Nucleopolyhedrovirus and diagnostic concentration for resistance monitoring. J Econ Entomol 112:349–354 (2019).
Perini CR, Arnemann JA, Cavallin LA, Guedes GA, Marques RP, Valmorbida I et al., Challenges in chemical management of soybean looper (Chrysodeixis includes) using several insecticides. Aust J Crop Sci 13:1723–1730 (2019).
Bacalhau FB, Dourado PM, Horikoshi RJ, Carvalho RA, Semeão A, Martinelli S et al., Performance of genetically modified soybean expressing the Cry1A.105, Cry2Ab2, and Cry1Ac proteins against key lepidopteran pests in Brazil. J Econ Entomol 113:2883–2889 (2020).
dos Santos SR, Specht A, Carneiro E and Casagrande MM, The influence of agricultural occupation and climate on the spatial distribution of Plusiinae (Lepidoptera: Noctuidae) on a latitudinal gradient in Brazil. Rev Bras Entomol 65:e20200103 (2021).
Decker‐Franco C, Blas GS, Balbi EI, Fichetti P, Puebla AF, Toledo AV et al., Genetic diversity of the polyphagous pest Rachiplusia nu across crops and locations in the Argentine pampas. Entomol Exp Appl 171:887–895 (2023).
Barbut K, Révision du genre Rachiplusia Hampson, 1913 (Lepidoptera, Noctuidae, Plusiinae). Bull Soc Entomol Fr 113:445–452 (2008).
Guedes JVC, Perini CR, Stacke RF, Curioletti LE, Arnemann JA and Alende VP, Lagartas da soja: das lições do passado ao manejo do futuro. Rev Plantio Direto 144:10–12 (2015).
Specht A, Sosa‐Gómez DR, Roque‐Specht VF, Valduga E, Gonzatti F, Schuh SM et al., Biotic potential and life tables of Chrysodeixis includens (Lepidoptera: Noctuidae), Rachiplusia nu, and Trichoplusia ni on soybean and forage turnip. J Insect Sci 19:8 (2019).
Horikoshi RJ, Dourado PM, Berger GU, Fernandes DS, Omoto C, Willse A et al., Large‐scale assessment of lepidopteran soybean pests and efficacy of Cry1Ac soybean in Brazil. Sci Rep 11:15956 (2021).
Barrionuevo MJ, Murúa MG, Goane L, Meagher R and Navarro F, Life table studies of Rachiplusia nu (Guenée) and Chrysodeixis (= Pseudoplusia) includens (Walker) (Lepidoptera: Noctuidae) on artificial diet. Fla Entomol 95:944–951 (2012).
Hill JG, Jerez PGP, Linares FJH, Alzogaray RA, Vera MT and Pereira EJG, Field‐evolved resistance of Rachiplusia nu to Cry1Ac Bt soybean in Argentina. Res Square (2023). https://doi.org/10.21203/rs.3.rs-3349674/v1.
Horikoshi RJ, Bernardi O, Godoy DN, Semeão AA, Willse A, Corazza GO et al., Resistance status of lepidopteran soybean pests following large‐scale use of MON 87701 × MON 89788 soybean in Brazil. Sci Rep 11:21323 (2021).
Nardon AC, Mathioni SM, Santos LV and Rosa DD, First record of Rachiplusia nu (Guenée, 1852) (Lepidoptera: Noctuidae) surviving on Bt soybean in Brazil. Entomol Commun 3:ec03028 (2021).
Perini CR, Sosa VI, Koda CE, Silva H, Risso AA, Vasconcelos WNF et al., Genetic structure of two Plusiinae species suggests recent expansion of Chrysodeixis includens in the American continent. Agric For Entomol 23:250–260 (2021).
Greene GL, Lepla NC and Dickerson WA, Velvetbean caterpillar: a rearing procedure and artificial medium. J Econ Entomol 69:488–497 (1976).
Herzog DC, Sampling soybean looper on soybean. In sampling Methods, in Koogan M and Herzog DC, ed. by Entomology S. Spinger, New York, Spinger Series in Experimental Entomology, pp. 141–168 (1980).
Sosa‐Gómez DR, Côrrea‐Ferreira BS, Hoffman‐Campo CB, Corso IC, Oliveira LJ, Moscardi F et al., Manual de identificação de insetos e outros invertebrados da cultura da soja, Vol. 269. Documentos Embrapa Soja, Londrina‐PR, Brazil, pp. 1–102 (2014).
Farias JRB, Nepomuceno AL and Neumaier N, Ecofisiologia da soja, Vol. 48. Circular Técnica Embrapa Soja, Londrina‐PR, Brazil, pp. 1–9 (2007).
Sistema de Agrotóxicos Fitossanitários (Agrofit) (2023). https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons [accessed 08 December 2022].
SAS Institute, Statistical Analysis System: Getting Started with the SAS Learning. SAS Institute, Cary, NC (2000).
Savin NE, Robertson JL and Russell RM, A critical evaluation of bioassay in insecticide research: likelihood ratio tests of dose‐mortality regression. Bull Entomol Soc Am 23:257–266 (1977).
Robertson JL, Savin NE, Preisler HK and Russell RM, Bioassays with Arthropods. CRC Press, Boca Raton, p. 224 (2007).
Abbott WS, A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–266 (1925).
Shapiro SS and Wilk MB, An analysis of variance teste for normality (complete samples). Biometrika 52:591–611 (1965).
Bartlett MS, Properties of sufficiency and statistical tests. Proc R Soc Lond A Math Phys Sci 160:268–282 (1937).
Stacke RF, Giacomelli T, Bronzatto ES, Halberstadt SA, Garlet CG, Muraro DS et al., Susceptibility of Brazilian populations of Chrysodeixis includens (Lepidoptera: Noctuidae) to selected insecticides. J Econ Entomol 112:1378–1387 (2019).
Stacke RF, Godoy DN, Pretto VE, Führ FM, Gubiani PS, Hettwer BL et al., Field‐evolved resistance to chitin synthesis inhibitor insecticides by soybean looper, Chrysodeixis includens (Lepidoptera: Noctuidae), in Brazil. Chemosphere 259:127499 (2020).
Stacke RF, Godoy DN, Halberstadt SA, Bronzatto ES, Giacomelli T, Hettwer BL et al., Inheritance of lambda‐cyhalothrin resistance, fitness costs and cross‐resistance to other pyrethroids in soybean looper, Chrysodeixis includens (Lepidoptera: Noctuidae). Crop Prot 131:105096 (2020).
Machado EP, Garlet CG, Weschenfelder MAG, Führ FM, Godoy DN, Pretto VE et al., Interspecific variation in susceptibility to insecticides by lepidopteran pests of soybean, cotton, and maize crops from Brazil. J Econ Entomol 115:305–312 (2022).
Bernardi O, Sorgatto RJ, Barbosa AD, Domingues FA, Dourado PM, Carvalho RA et al., Low susceptibility of Spodoptera cosmioides, Spodoptera eridania and Spodoptera frugiperda (Lepidoptera: Noctuidae) to genetically‐modified soybean expressing Cry1Ac protein. Crop Prot 58:33–40 (2014).
Manzoni CG, Pogetto MD, Fadin D, da Silva LC and Oliveira RC, Efficacy of Intrepid Edge™ to control Rachiplusia nu (Guenée) (Lepidoptera: Noctuidae) on soybean in Brazil, in Proceedings of the 28th Brazilian Congress of Entomology. Entomological Society of Brazil, Fortaleza, p. 475 (2022).
Theodoro CM, Moreira SCS and Barbosa VO, Eficiência de inseticidas no controle de Rachiplusia nu (Lepidoptera: Noctuidae) em soja Bt, in Proceedings of the 28th Brazilian Congress of Entomology. Entomological Society of Brazil, Fortaleza, p. 474 (2022).
Silva FMA, Júnior SPS, da Fonseca LF, Mezzomo RF, Rodrigues RB, Lodo BN et al., Avaliação da eficácia de Premio (Clorantraniliprole) no controle da lagarta‐falsa‐medideira (Rachiplusia nu) na cultura da soja (Glycine max), in Proceedings of the 28th Brazilian Congress of Entomology. Entomological Society of Brazil, Fortaleza, p. 524 (2022). https://www.seb.org.br/admin/files/book/book_EHI6uWbYHPYr.pdf accessed 08 February 2024.
Pansera‐de‐Araújo MCG, da Cruz IBM, Cavalheiro M and Oliveira AK, Placement of noctuid eggs (Lepidoptera) on soybean plants. Ann Entomol Soc Am 92:702–706 (1999).
Zulin D, Ávila CJ and Schlick‐Souza EC, Population fluctuation and vertical distribution of the soybean looper (Chrysodeixis includens) in soybean culture. American J Plant Sci 9:1544–1556 (2018).
Perini CR, Tabuloc CA, Chiu JC, Zalom FG, Stacke RF, Bernardi O et al., Transcriptome analysis of pyrethroid‐resistant Chrysodeixis includens (Lepidoptera: Noctuidae) reveals overexpression of metabolic detoxification genes. J Econ Entomol 114:274–283 (2021).
Martins GLM and Tomquelski GV, Efficiency of insecticides on Chrysodeixis includens (Lepidoptera: Noctuidae) on soybean crop. Rev Agric Neotrop 2:25–30 (2015).
Sosa‐Gómez DR and Omoto C, Resistência a inseticidas e outros agentes de controle em artrópodes associados à cultura da soja, in Soja: Manejo Integrado De Insetos E Outros Artrópodes‐Praga, ed. by Hoffmann‐Campo CB, Corrêa‐Ferreira BS and Moscardi F. Brasília, Embrapa, pp. 673–723 (2012).
Rimoldi F, Fogel MN, Schneider MI and Ronco AE, Lethal and sublethal effects of cypermethrin and methoxyfenozide on the larvae of Rachiplusia nu (Guenée) (Lepidoptera: Noctuidae). Invertebr Reprod Dev 56:200–208 (2012).
Russo R, Gamundi JC and Alzogaray RA, Evaluation of pyrethroids toxicity in a laboratory strain and a field population of Rachiplusia nu (Lepidoptera: Noctuidae) using two bioassay techniques. Rev Soc Entomol Argent 71:115–123 (2012).
Ferré J and Van Rie J, Biochemistry and genetics of insect resistance to bacillus thuringiensis. Annu Rev Entomol 47:501–533 (2002).
Hernández‐Rodríguez CS, Hernández‐Martínez P, Van Rie J, Escriche B and Ferré J, Shared midgut binding sites for Cry1A. 105, Cry1Aa, Cry1Ab, Cry1Ac and Cry1Fa proteins from bacillus thuringiensis in two important corn pests, Ostrinia nubilalis and Spodoptera frugiperda. PLoS One 8:e68164 (2013).
Yano SAC, Specht A, Moscardi F, Carvalho RA, Dourado PM, Martinelli S et al., High susceptibility and low resistance allele frequency of Chrysodeixis includens (Lepidoptera: Noctuidae) field populations to Cry1Ac in Brazil. Pest Manag Sci 72:1578–1584 (2016).

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Keywords: Plusiinae; chemical control; integrated pest management; soybean looper; tolerance

0 (Insecticides)

Date Created: 20240527 Date Completed: 20241011 Latest Revision: 20241011

20241011

10.1002/ps.8197

38801197