Low risk of resistance evolution of Spodoptera frugiperda to chlorfenapyr in Brazil

  • Rubens H. Kanno
  • Anderson Bolzan
  • Ingrid S. Kaiser
  • Ewerton C. Lira
  • Fernando S. A. Amaral
  • Aline S. Guidolin
  • Antônio R. B. Nascimento
  • Celso OmotoEmail author
Original Paper


Insecticide resistance is serious problem for Spodoptera frugiperda (Lepidoptera: Noctuidae). Due to intense selection pressure, the evolution of S. frugiperda resistance to major insecticides groups and Bt proteins has already been documented. Therefore, studies to preserve the lifetime of insecticides with unique modes of action such as chlorfenapyr are important in insect resistance management programs. For implementing a proactive resistance management program of S. frugiperda to chlorfenapyr, studies were conducted with field populations collected from major corn-growing regions in Brazil from 2016 to 2018. We aimed to (i) characterize and monitor the susceptibility of field populations, (ii) estimate the frequency of resistance alleles and (iii) evaluate cross-resistance patterns between insecticides and Bt-resistant strains of S. frugiperda to chlorfenapyr. Baseline susceptibility of field population showed a LC50 ranged from 18.3 to 25.1 µg ml−1. The survival rate at the diagnostic concentration ranged from 0 to 8.4%. Using the F2 screen method, the overall estimated resistance allele frequency was 0.0003. No cross-resistance was observed between chlorfenapyr and other insecticides and Bt proteins. Results demonstrated a high susceptibility, low frequency of resistance alleles and lack of cross-resistance. Thus, we concluded there is a low risk of resistance evolution of S. frugiperda to chlorfenapyr in Brazil using the current pest management strategies.


Fall armyworm Baseline susceptibility Susceptibility monitoring F2 screen Cross-resistance Insect resistance management 



We thank Coordination for the Improvement of Higher Education Personnel (CAPES)—Finance Code 001 for granting a scholarship to the first author and the National Council for Scientific and Technological Development (CNPq) for the fellowship to CO (Grant #403851/2013-0). We also thank the Brazilian Insecticide Resistance Action Committee (IRAC-BR) (Grant Project 2975-0) for providing partial financial support for this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animals rights

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Ahmad M, Akhtar KP (2018) Susceptibility of cotton whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) to diverse pesticides in Pakistan. J Econ Entomol 111:1834–1841CrossRefGoogle Scholar
  2. Ahmad M, Iqbal Arif M (2009) Resistance of Pakistani field populations of spotted bollworm Earias vittella (Lepidoptera: Noctuidae) to pyrethroid, organophosphorus and new chemical insecticides. Pest Manag Sci 65:433–439. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Albernaz KC, Merlin BL, Martinelli S et al (2013) Baseline susceptibility to Cry1Ac insecticidal protein in Heliothis virescens (Lepidoptera: Noctuidae) populations in Brazil. J Econ Entomol 106:1819–1824CrossRefPubMedCentralGoogle Scholar
  4. Andow DA, Alstad DN (1998) F2 screen for rare resistance alleles. J Econ Entomol 91:572–578. CrossRefGoogle Scholar
  5. Azambuja R, Degrande PE, dos Santos RO et al (2015) Effect of Bt soybean on larvae of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Agric Sci 7:90–94. CrossRefGoogle Scholar
  6. Bernardi D, Salmeron E, Horikoshi RJ et al (2015a) Cross-resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided Bt maize hybrids in Brazil. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bernardi O, Bernardi D, Ribeiro RS et al (2015b) Frequency of resistance to Vip3Aa20 toxin from Bacillus thuringiensis in Spodoptera frugiperda (Lepidoptera: Noctuidae) populations in Brazil. Crop Prot 76:7–14. CrossRefGoogle Scholar
  8. Bernardi O, Bernardi D, Horikoshi RJ et al (2016) Selection and characterization of resistance to the Vip3Aa20 protein from Bacillus thuringiensis in Spodoptera frugiperda. Pest Manag Sci 72:1794–1802. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bolzan A, Padovez FEO, Nascimento ARB et al (2019) Selection and characterization of the inheritance of resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to chlorantraniliprole and cross-resistance to other diamide insecticides. Pest Manag Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brookes G, Barfoot P (2018) Environmental impacts of genetically modified (GM) crop use 1996-2016: impacts on pesticide use and carbon emissions. GM Crops Food 9:109–139. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brown TM, Bryson PK, Payne GT (1996) Synergism by propynyl aryl ethers in permethrin-resistant tobacco budworm larvae, Heliothis virescens. Pestic Sci 45:323–331.;2-Y CrossRefGoogle Scholar
  12. Burtet LM, Bernardi O, Melo AA et al (2017) Managing fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), with Bt maize and insecticides in southern Brazil. Pest Manag Sci 73:2569–2577CrossRefPubMedCentralGoogle Scholar
  13. Carvalho RA, Omoto C, Field LM et al (2013) Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Céleres (2017) 3rd follow-up on agricultural biotechnology adoption for the 2016/17 crop. Accessed 30 Jan 2019
  15. Comissão Técnica Nacional de Biossegurança (CTNBio) (2019) Liberação Comercial de Soja Geneticamente Modificada Resistente a Insetos e Tolerante a Herbicida, Soja MON 87701 x MON 89788 - Processo n° 01200.001864/2009-00. Accessed 30 Jan 2019
  16. Czepak C, Albernaz KC, Vivan LM et al (2013) Primeiro registro de ocorrência de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) no Brasil. Pesqui Agropecuária Trop 43:110–113CrossRefGoogle Scholar
  17. Day R, Abrahams P, Bateman M et al (2017) Fall armyworm: impacts and implications for Africa. Outlooks Pest Manag 28:196–201CrossRefGoogle Scholar
  18. Dennehy TJ (1987) Decision-making for managing pest resistance to pesticides. In: Ford MG, Holloman DW, Khambay BPS, Sawicki RM (eds) Combating resistance to xenobiotics: biological and chemical approaches. Ellis Horwood, Chichester, pp 118–126Google Scholar
  19. Diez-Rodríguez GI, Omoto C (2001) Herança da resistência de Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) a lambda-cialotrina. Neotrop. Entomol. 30:311–316CrossRefGoogle Scholar
  20. do Nascimento ARB, Fresia P, Cônsoli FL, Omoto C (2015) Comparative transcriptome analysis of lufenuron-resistant and susceptible strains of Spodoptera frugiperda (Lepidoptera: Noctuidae). BMC Genom 16:985. CrossRefGoogle Scholar
  21. do Nascimento ARB, Farias JR, Bernardi D et al (2016) Genetic basis of Spodoptera frugiperda (Lepidoptera: Noctuidae) resistance to the chitin synthesis inhibitor lufenuron. Pest Manag Sci 72:810–815. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Farias JR, Andow DA, Horikoshi RJ et al (2014) Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Prot 64:150–158. CrossRefGoogle Scholar
  23. Ferreira CBS, Andrade FHN, Rodrigues ARS et al (2015) Resistance in field populations of Tetranychus urticae to acaricides and characterization of the inheritance of abamectin resistance. Crop Prot 67:77–83. CrossRefGoogle Scholar
  24. Georghiou GP (1983) Management of resistance in arthropods. In: Georghiou GP, Saito T (eds) Pest resistance to pesticides. Springer, Boston, MA, pp 769–792CrossRefGoogle Scholar
  25. Goergen G, Kumar PL, Sankung SB et al (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE 11:e0165632CrossRefPubMedCentralGoogle Scholar
  26. Herron GA, Rophail J, Wilson LJ (2004) Chlorfenapyr resistance in two-spotted spider mite (Acari: Tetranychidae) from Australian cotton. Exp Appl Acarol 34:315–321. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hunt D, Treacy MF (1998) Pyrrole Insecticides: a new class of agriculturally important insecticides functioning as uncouplers of oxidative phosphorylation. In: Ishaaya I, Degheele D (eds) Insecticides with novel modes of action: mechanism and application. Springer, Berlin, pp 138–151CrossRefGoogle Scholar
  28. Jiang T, Wu S, Yang T et al (2015) Monitoring field populations of Plutella xylostella (Lepidoptera: Plutellidae) for resistance to eight insecticides in China. Florida Entomol 98:65–73. CrossRefGoogle Scholar
  29. Kalleshwaraswamy CM, Asokan R, Swamy HMM et al (2018) First report of the Fall armyworm, Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Manag Hortic Ecosyst 24:23–29Google Scholar
  30. Kasten P Jr, Precetti A, Parra JRP (1978) Dados biologicos comparativos de Spodoptera frugiperda (JE Smith, 1797) em duas dietas artificiais e substrato natural. Rev Agric 53:68–78Google Scholar
  31. Kumela T, Simiyu J, Sisay B et al (2019) Farmers’ knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. Int J Pest Manag 65:1–9CrossRefGoogle Scholar
  32. LeOra-Software (2002) POLO-Plus, POLO for Windows computer program, version 2.0. LeOra-Software, PetalumaGoogle Scholar
  33. Lima Neto JE, Siqueira HÁADE (2017) Selection of Plutella xylostella (L.) (Lepidoptera: Plutellidae) to chlorfenapyr resistance heritability and the number of genes involved. Rev Caatinga 30:1067–1072CrossRefGoogle Scholar
  34. Liu X, Ning Y, Wang H, Wang K (2015a) Cross-resistance, mode of inheritance, synergism, and fitness effects of cyantraniliprole resistance in Plutella xylostella. Entomol Exp Appl 157:271–278. CrossRefGoogle Scholar
  35. Liu X, Wang H-Y, Ning Y-B et al (2015b) Resistance selection and characterization of chlorantraniliprole resistance in Plutella xylostella (Lepidoptera: Plutellidae). J Econ Entomol 108:1978–1985CrossRefGoogle Scholar
  36. Marcon PCRG, Siegfried BD, Spencer T, Hutchison WD (2000) Development of diagnostic concentrations for monitoring Bacillus thuringiensis resistance in European corn borer (Lepidoptera: Crambidae). J Econ Entomol 93:925–930CrossRefGoogle Scholar
  37. McCord E, Yu SJ (1987) The mechanisms of carbaryl resistance in the fall armyworm, Spodoptera frugiperda (J.E. Smith). Pestic Biochem Physiol 27:114–122. CrossRefGoogle Scholar
  38. Montezano DG, Specht A, Sosa-Gómez DR et al (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomol 26:286–301CrossRefGoogle Scholar
  39. Naeem A, Freed S, Jin FL et al (2016) Monitoring of insecticide resistance in Diaphorina citri Kuwayama (Hemiptera: Psyllidae) from citrus groves of Punjab, Pakistan. Crop Prot 86:62–68. CrossRefGoogle Scholar
  40. Nicastro RL, Sato ME, Arthur V, da Silva MZ (2013) Chlorfenapyr resistance in the spider mite Tetranychus urticae: stability, cross-resistance and monitoring of resistance. Phytoparasitica 41:503–513. CrossRefGoogle Scholar
  41. Okuma DM, Bernardi D, Horikoshi RJ et al (2018) Inheritance and fitness costs of Spodoptera frugiperda (Lepidoptera: Noctuidae) resistance to spinosad in Brazil. Pest Manag Sci 74:1441–1448. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pimprale SS, Besco CL, Bryson PK, Brown TM (1997) Increased susceptibility of pyrethroid-resistant tobacco budworm (Lepidoptera: Noctuidae) to chlorfenapyr. J Econ Entomol 90:49–54CrossRefGoogle Scholar
  43. Pogue MG (2002) A world revision of the genus Spodoptera Guenée: (Lepidoptera: Noctuidae). American Entomological Society PhiladelphiaGoogle Scholar
  44. Pomari-Fernandes A, de Freitas Bueno A, Sosa-Gómez D (2015) Helicoverpa armigera: current status and future perspectives in Brazil. Embrapa Soja-Artigo em periódico indexado (ALICE)Google Scholar
  45. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 30 Jan 2019
  46. Robertson JL, Preisler HK, Ng SS et al (1995) Natural Variation: A Complicating Factor in Bioassays with Chemical and Microbial Pesticides. J Econ Entomol 88:1–10CrossRefGoogle Scholar
  47. Robertson JL, Jones MM, Olguin E, Alberts B (2017) Bioassays with arthropods. CRC Press, Boca RatonCrossRefGoogle Scholar
  48. Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380. CrossRefPubMedPubMedCentralGoogle Scholar
  49. SAS Institute (2004) SAS user’s guide: statistics, version 8.2. SAS Institute, Cary, NCGoogle Scholar
  50. Sheppard CD (1995) Oxidative metabolic resistance to cyanopyrethroids in the horn fly (Diptera: Muscidae). J Econ Entomol 88:1531–1535. CrossRefGoogle Scholar
  51. Sheppard CD, Joyce JA (1998) Increased susceptibility of pyrethroid-resistant horn flies (Diptera: Muscidae) to chlorfenapyr. J Econ Entomol 91:398–400CrossRefGoogle Scholar
  52. Sidana J, Singh B, Sharma OMP (2018) Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae), in the maize fields of Karnataka, India. Curr Sci 115:621CrossRefGoogle Scholar
  53. Sims SB, Greenplate JT, Stone TB et al (1996) Monitoring strategies for early detection of Lepidoptera resistance to Bacillus thuringiensis insecticidal proteins. In: Brown TM (ed) Molecular genetics and evolution of pesticide resistance. American Chemical Society, Washigton, pp 229–242CrossRefGoogle Scholar
  54. Sparks TC (2013) Insecticide discovery: an evaluation and analysis. Pestic Biochem Physiol 107:8–17. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sparks TC, Lorsbach BA (2017) Perspectives on the agrochemical industry and agrochemical discovery. Pest Manag Sci 73:672–677CrossRefPubMedCentralGoogle Scholar
  56. Sparks TC, Nauen R (2015) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Specht A, Sosa-Gómez DR, de Paula-Moraes SV, Yano SAC (2013) Identificação morfológica e molecular de Helicoverpa armigera (Lepidoptera: Noctuidae) e ampliação de seu registro de ocorrência no Brasil. Pesqui Agropecuária Bras 48:689–692CrossRefGoogle Scholar
  58. Tabashnik BE (1989) Managing resistance with multiple pesticide tactics: theory, evidence, and recommendations. J Econ Entomol 82:1263–1269CrossRefPubMedCentralGoogle Scholar
  59. Treacy M, Miller T, Black B et al (1994) Uncoupling activity and pesticidal properties of pyrroles. Biochem Soc Trans 22:244–247CrossRefPubMedCentralGoogle Scholar
  60. Uesugi R, Goka K, Osakabe MH (2002) Genetic basis of resistances to chlorfenapyr and etoxazole in the two-spotted spider mite (Acari: Tetranychidae). J Econ Entomol 95:1267–1274CrossRefPubMedCentralGoogle Scholar
  61. Ullah S, Shah RM, Shad SA (2016) Genetics, realized heritability and possible mechanism of chlorfenapyr resistance in Oxycarenus hyalinipennis (Lygaeidae: Hemiptera). Pestic Biochem Physiol 133:91–96. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Van Leeuwen T, Stillatus V, Tirry L (2004) Genetic analysis and cross-resistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol 32:249. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang D, Qiu X, Ren X et al (2009) Resistance selection and biochemical characterization of spinosad resistance in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pestic Biochem Physiol 95:90–94. CrossRefGoogle Scholar
  64. Wang X, Wang J, Cao X et al (2018) Long-term monitoring and characterization of resistance to chlorfenapyr in Plutella xylostella (Lepidoptera: Plutellidae) from China. Pest Manag Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Whalon ME, Mota-Sanchez D, Hollingworth RM (2008) Global pesticide resistance in arthropods. Cabi, WallingfordCrossRefGoogle Scholar
  66. Xi J, Pan Y, Bi R et al (2015) Elevated expression of esterase and cytochrome P450 are related with lambda–cyhalothrin resistance and lead to cross resistance in Aphis glycines Matsumura. Pestic Biochem Physiol 118:77–81. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Yu SJ (1991) Insecticide resistance in the fall armyworm, Spodoptera frugiperda (J.E. Smith). Pestic Biochem Physiol. CrossRefGoogle Scholar
  68. Yu SJ, Nguyen SN, Abo-Elghar GE (2003) Biochemical characteristics of insecticide resistance in the fall armyworm, Spodoptera frugiperda (J.E. Smith). Spodoptera frugiperda. Pestic Biochem Physiol 77:22. CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Entomology and Acarology, Luiz de Queiroz College of Agriculture (ESALQ)University of São Paulo (USP)PiracicabaBrazil

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