Sub-lethal effects of lufenuron exposure on spotted bollworm Earias vittella (Fab): key biological traits and detoxification enzymes activity

  • Muhammad Hafeez
  • Saad JanEmail author
  • Muhammad Nawaz
  • Ehsan Ali
  • Bahar Ali
  • Muhammad Qasim
  • G. Mandela Fernández-Grandon
  • Muhammad Shahid
  • Mo WangEmail author
Research Article


Spotted bollworm, Earias vittella, is one of the most serious and devastating insect pests of vegetables and cotton. Currently, insecticides are necessary for its control in nearly all crop systems. In this paper, we evaluate the sub-lethal effects of lufenuron on biological traits and activity of detoxification enzymes: cytochrome P450 monooxygenases, esterase, and glutathione S-transeferase (GST) in second instar larvae of E. vittella. Results showed that sub-lethal concentrations (LC15 and LC40 of lufenuron), prolonged larval period (at LC40 = 13.86 ± 1.22 day, LC15 = 13.14 ± 1.15 day, control = 12.28 ± 0.7), pupal duration (LC40 = 11.1 ± day, LC15 = 11.8 ± 0.28 day, control = 9.40 ± 0.52), and extended mean generation time (LC40 = 27.3 ± 0.43 LC15 = 29.0 ± 1.19 day, control = 26.0 ± 0.65). Sub-lethal exposure significantly prolonged the pre-adult stage, decreased pupal weight, and reduced adult longevity in the parent (F0) and F1 generation. Moreover, the fecundity and egg viability were significantly lowered in parental and F1 generations at both sub-lethal concentrations compared to the control. While no significant effects were noted on reproductive parameters such as the intrinsic rate of increase (r), finite rate of increase (λ), and net reproduction rate (R0) of F1 generation when compared to the control. Only mean generation time (T) in F1 at LC15 was significantly longer compared to the LC40 and control (LC40 = 3.79 ± 0.37, LC15 = 32.28 ± 1.55 day, control = 29.79 ± 0.55). Comparatively, the activities of cytochrome P450 monooxygenases and esterase were higher than GST in treated populations. The increase in resistance development against insecticides may possibly because of elevated activity of detoxification enzymes. These results provide useful information for monitoring resistance in integrated pest management (IPM) programs for E. vittella.


Biological parameters Spotted bollworm IGR Earias vittella Sub-lethal concentrations Biochemical mechanism 



We are grateful to Dr. Hsin Chi (Department of Plant Production and Technologies, Faculty of Agricultural Sciences and Technologies, Omer Halisdemir University, Turkey), for two-sex life table theory used in this work.


  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. CrossRefGoogle Scholar
  2. Ahmad M, 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. CrossRefGoogle Scholar
  3. Ahmad M, Iqbal Arif M, Ahmad M (2007) Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Prot 26:809–817. CrossRefGoogle Scholar
  4. Ahmad S, Ansari MS, Khan N, Hasan F (2017) Toxic effects of insecticides on the life table and development of Earias vittella (Lepidoptera: Noctuidae) on okra. Int J Trop Insect Sci 37:30–40. CrossRefGoogle Scholar
  5. Akca I, Ayvaz T, Yazici E, Smith C, Chi H (2015) Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. J Econ Entomol 108:1466–1478CrossRefGoogle Scholar
  6. Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12. CrossRefGoogle Scholar
  7. Aliabadi FP, Álvarez-León EE (2016) Lethal and sublethal effects of a chitin synthesis inhibitor, lufenuron, against Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). J Crop Prot 5:203–214CrossRefGoogle Scholar
  8. Alinejad M, Kheradmand K, Fathipour Y (2014) Sublethal effects of fenazaquin on life table parameters of the predatory mite Amblyseius swirskii (Acari: Phytoseiidae). Exp Appl Acarol 64:361–373. CrossRefGoogle Scholar
  9. Arain MS, Shakeel M, Elzaki MEA, Farooq M et al (2018) Association of detoxification enzymes with butene-fipronil in larvae and adults of Drosophilia melanogaster. Environ Sci Pollut Res 25:10006–10013CrossRefGoogle Scholar
  10. Arora MS, Salokhe SG, MSN (2012) Effect of sub-lethal concentrations of lufenuron on growth, development and reproductive performance of tribolium castaneum (Herbst). Int J Appl Biol Pharm Technol 3:111–122Google Scholar
  11. Bass C, Field LM (2011) Gene amplification and insecticide resistance. Pest Manag Sci 67:886–890CrossRefGoogle Scholar
  12. Bilal M, Freed S, Ashraf MZ, Zaka SM, Khan MB (2018) Activity of acetylcholinesterase and acid and alkaline phosphatases in different insecticide-treated Helicoverpa armigera (Hübner). Environ Sci Pollut Res 25:22903–22910. CrossRefGoogle Scholar
  13. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One 8:e76548. CrossRefGoogle Scholar
  14. Carrie’re Y, Deland JP, Roff DA, Vincent C (1994) Life-history costs associated with the evolution of insecticide resistance. Proc R Soc Lond Ser B Biol Sci 258:35–40CrossRefGoogle Scholar
  15. Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17:26–34. CrossRefGoogle Scholar
  16. Chi H (2017) TWOSEXeMSChart: a computer program for the age-stage, two-sex life table analysis. National Chung Hsing University, Taichung, Taiwan.
  17. Chi H, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sin 24:225–240Google Scholar
  18. Chi H, Yang T (2003) Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ Entomol 32:327–333. CrossRefGoogle Scholar
  19. Cordeiro EMG, de Moura ILT, Fadini MAM, Guedes RNC (2013) Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite oligonychus ilicis? Chemosphere 93:1111–1116. CrossRefGoogle Scholar
  20. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. CrossRefGoogle Scholar
  21. Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Monographs on statistics and applied probability, No. 57. Chapman and Hall, London, 436 pGoogle Scholar
  22. EFSA (2015) European Food Safety Authority. The 2013 European Union report on pesticide residues in food. EFSA J doi:
  23. Evangelista WS Jr, Torres JB, Silva-Torres C (2002) Toxicidade de lufenuron para Podisus nigrispinus (Dallas) (Hetero-ptera: Pentatomidae). Neotrop Entomol 31:319–326CrossRefGoogle Scholar
  24. Fonseca APP, Marques EJ, Torres JB, Silva LM, Siqueira HÁA (2015) Lethal and sublethal effects of lufenuron on sugarcane borer Diatraea flavipennella and its parasitoid Cotesia flavipes. Ecotoxicology 24:1869–1879. CrossRefGoogle Scholar
  25. Gelbic I, Adel MM, Hussein HM (2011) Effects of nonsteroidal ecdysone agonist RH-5992 and chitin biosynthesis inhibitor lufenuron on Spodoptera littoralis (Boisduval, 1833). Cent Eur J Biol 6:861–869. Google Scholar
  26. Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat 119:803–823. CrossRefGoogle Scholar
  27. Guedes RNC, Cutler GC (2014) Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci 70:690–697CrossRefGoogle Scholar
  28. Hafeez M, Liu S, Jan S, Ali B, Shahid M, Fernández-Grandon GM, Nawaz M, Ahmad A, Wang M (2018) Gossypol-induced fitness gain and increased resistance to deltamethrin in beet armyworm, Spodoptera exigua (Hübner). Pest Manag Sci 75:683–693. CrossRefGoogle Scholar
  29. Han W, Zhang S, Shen F, Liu M, Ren C, Gao X (2012) Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (Lepidoptera: Plutellidae). Pest Manag Sci 68:1184–1190. CrossRefGoogle Scholar
  30. Huang YB, Chi H (2012) Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci 19:263–273. CrossRefGoogle Scholar
  31. Ishaaya I, Kontsedalov S, Horowitz AR (2005) Biorational insecticides: mechanism and cross-resistance. Arch Insect Biochem Physiol 58:192–199CrossRefGoogle Scholar
  32. Jan MT, Abbas N, Shad SA, Saleem MA (2015) Resistance to organophosphate, pyrethroid and biorational insecticides in populations of spotted bollworm, Earias vittella (Fabricius) (Lepidoptera: Noctuidae), in Pakistan. Crop Prot 78:247–252. CrossRefGoogle Scholar
  33. Karuppaiah V, Srivastava C, Subramanian S, Čupr P (2017) Variation in insecticide detoxification enzymes activity in Spodoptera litura (Fabricius) of different geographic origin. J Entomol Zool Stud 5:770–773Google Scholar
  34. Lakshmi A (1993) Pesticides in India: risk assessment to aquatic ecosystems. Sci Total Environ 134:243–253. CrossRefGoogle Scholar
  35. Mahmoudvand M, Abbasipour H, Garjan AS, Bandani AR (2011) Sublethal effects of hexaflumuron on development and reproduction of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Insect Sci 18:689–696. CrossRefGoogle Scholar
  36. Medina P, Smagghe G, Budia F, del Estal P, Tirry L, Viñuela E (2002) Significance of penetration, excretion, and transovarial uptake to toxicity of three insect growth regulators in predatory lacewing adults. Arch Insect Biochem Physiol 51:91–101. CrossRefGoogle Scholar
  37. Meng QW, Wang JJ, Shi JF, Guo WC, Li GQ (2018) Effect of teflubenzuron ingestion on larval performance and chitin content in Leptinotarsa decemlineata. Am J Potato Res 95:463–472CrossRefGoogle Scholar
  38. Moreno PR, Nakano O (2002) Atividade de buprofezin sobre a cigarrinha verde dofeijoeiro Empoasca kraemeri (Ross & Moore, 1957) (Hemiptera, cicadellidae) em condicoes de laboratorio (13) Activity of buprofezin on the green leafhopper Empoasca kraemeri (Ross & Moore, 1957) (Hemiptera, . Sci Agric 59:475–481Google Scholar
  39. Perveen F, Miyata T (2000) Effects of sublethal dose of chlorfluazuron on ovarian development and oogenesis in the common cutworm Spodoptera litura (Lepidoptera: Noctuidae). Ann Entomol Soc Am 93:1131–1137.[1131:EOSDOC]2.0.CO;2Google Scholar
  40. Qu C, Zhang W, Li F, Tetreau G, Luo C, Wang R (2017) Lethal and sublethal effects of dinotefuran on two invasive whiteflies, Bemisia tabaci (Hemiptera: Aleyrodidae). J Asia Pac Entomol 20:325–330. CrossRefGoogle Scholar
  41. Rahman MA, Uddin MM, Rahman MM (2016) Comparative efficacy of different tactics for the Management of Okra Shoot and Fruit Borer, Earias Vittella (Fab.) under Field condition. Int J Appl Sci Biotechnol.
  42. Rehan A, Freed S (2015) Fitness cost of methoxyfenozide and the effects of its sublethal doses on development, reproduction, and survival of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Neotrop Entomol 44:513–520. CrossRefGoogle Scholar
  43. Rezaei M, Shariatifar N, Shoeibi S, Amir Ahmadi M, Jahed Khaniki G (2017) Simultaneous determination of residue from 58 pesticides in the wheat flour consumed in Tehran, Iran by GC/MS. Iran J Pharm Res 16:1048–1058Google Scholar
  44. Robertson JL, Russell RM, Savin NE (1980) POLO: a User’s guide to Probit or logit analysis. General Technical Report PSW-038.
  45. Rugno GR, Zanardi OZ, Yamamoto PT (2015) Are the pupae and eggs of the lacewing Ceraeochrysa cubana (Neuroptera: Chrysopidae) tolerant to insecticides? J Econ Entomol 108:2630–2639. CrossRefGoogle Scholar
  46. Sáenz-de-cabezón FJ, Pérez-moreno I, Zalom FG, Marco V (2006) Effects of Lufenuron on Lobesia botrana (Lepidoptera: Tortricidae) egg, larval, and adult stages. J Econ Entomol 99:427–431. CrossRefGoogle Scholar
  47. Salokhe SG, Pal JK, Mukherjee SN (2003) Effect of sublethal concentrations of flufenoxuron on growth, development and reproductive performance of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Invertebr Reprod Dev 43:141–150CrossRefGoogle Scholar
  48. Santos MS, Zanardi OZ, Pauli KS, Forim MR, Yamamoto PT, Vendramim JD (2015) Toxicity of an azadirachtin-based biopesticide on Diaphorina citri Kuwayama (Hemiptera: Liviidae) and its ectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). Crop Prot 74:116–123. CrossRefGoogle Scholar
  49. Schneider MI, Smagghe G, Gobbi A, Viñuela E (2003) Toxicity and pharmacokinetics of insect growth regulators and other novel insecticides on pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a parasitoid of early larval instars of lepidopteran pests. J Econ Entomol 96:1054–1065. CrossRefGoogle Scholar
  50. Schneider MI, Maggheg S, Pineda SVE (2008) The ecological impact of four IGR insecticides in adults of Hyposoter didymator (Hym., Ichneumonidae): Pharmacol Approach. Ecotoxicology 17:181–188CrossRefGoogle Scholar
  51. Seth RK, Kaur JJ, Rao DK, Reynolds SE (2004) Effects of larval exposure to sublethal concentrations of the ecdysteroid agonists RH-5849 and tebufenozide (RH-5992) on male reproductive physiology in Spodoptera litura. J Insect Physiol 50:505–517. CrossRefGoogle Scholar
  52. Tao XY, Xue XY, Huang YP et al (2012) Gossypol-enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide. Mol Ecol 21:4371–4385. CrossRefGoogle Scholar
  53. Thara S, Kingsley S, Revathi N (2009) Impact of neem derivatives on egg hatchability of okra fruit borer, Earias vittella fab. (Lepidoptera: Noctuidae). Int J Plant Prot 2:95–97Google Scholar
  54. Tian X, Sun X, Su J (2014) Biochemical mechanisms for metaflumizone resistance in beet armyworm, Spodoptera exigua. Pestic Biochem Physiol 113:8–14. CrossRefGoogle Scholar
  55. Tuan SJ, Lin YH, Yang CM, Atlihan R, Saska PCH (2016) Survival and reproductive strategies in two-spotted spider mites: demographic analysis of arrhenotokous parthenogenesis of Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 109:502–509CrossRefGoogle Scholar
  56. van Asperen K (1962) A study of housefly esterases by means of a sensitive colorimetric method. J Insect Physiol 8:401–416. CrossRefGoogle Scholar
  57. Wang X, Huang Q, Hao Q, Ran S, Wu Y, Cui P, Yang J, Jiang C, Yang Q (2018) Insecticide resistance and enhanced cytochrome P450 monooxygenase activity in field populations of Spodoptera litura from Sichuan, China. Crop Prot 106:110–116. CrossRefGoogle Scholar
  58. Wen Y, Liu Z, Bao H, Han Z (2009) Imidacloprid resistance and its mechanisms in field populations of brown planthopper, Nilaparvata lugens Stål in China. Pestic Biochem Physiol 94:36–42. CrossRefGoogle Scholar
  59. Wilson TG, Cryan JR (1997) Lufenuron, a chitin-synthesis inhibitor, interrupts development of Drosophila melanogaster. J Exp Zool 278:37–44.<37::AID-JEZ4>3.0.CO;2-7 CrossRefGoogle Scholar
  60. Wu S, Yang Y, Yuan G, Campbell PM, Teese MG, Russell RJ, Oakeshott JG, Wu Y (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 41:14–21. CrossRefGoogle Scholar
  61. Xu L, Wu M, Han Z (2014) Biochemical and molecular characterization and expression of cytochrome P450 CYP6AY1. Pestic Biochem Physiol 43:1021e1027Google Scholar
  62. Yang Y, Wu Y, Chen S, Devine GJ, Denholm I, Jewess P, Moores GD (2004) The involvement of microsomal oxidases in pyrethroid resistance in Helicoverpa armigera from Asia. Insect Biochem Mol Biol 34:763–773. CrossRefGoogle Scholar
  63. Young SJ, Gunning RV, Moores GD (2006) Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Manag Sci 62:114–119. CrossRefGoogle Scholar
  64. Yu SJ (1984) Interactions of allelochemicals with detoxication enzymes of insecticide-susceptible and resistant fall armyworms. Pestic Biochem Physiol 22:60–68. CrossRefGoogle Scholar
  65. Zarate N, Díaz O, Martínez AM, Figueroa JI, Schneider MI, Smagghe G, Viñuela E, Budia F, Pineda S (2011) Lethal and sublethal effects of methoxyfenozide on the development, survival and reproduction of the fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 40:129–137. CrossRefGoogle Scholar
  66. Zhan Y, Fan S, Zhang M, Zalom F (2015) Modelling the effect of pyrethroid use intensity on mite population density for walnuts. Pest Manag Sci 71:159–164. CrossRefGoogle Scholar
  67. Zhang RM, Jang EB, He SCJ (2015) Lethal and sublethal effects of cyantraniliprole on Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Pest Manag Sci 71:250–256CrossRefGoogle Scholar
  68. Zhao Y, Wang Q, Ding J, Wang Y, Zhang Z, Liu F, Mu W (2018) Sublethal effects of chlorfenapyr on the life table parameters, nutritional physiology and enzymatic properties of Bradysia odoriphaga (Diptera: Sciaridae). Pestic Biochem Physiol 148:93–102CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Muhammad Hafeez
    • 1
  • Saad Jan
    • 2
    Email author
  • Muhammad Nawaz
    • 3
  • Ehsan Ali
    • 1
  • Bahar Ali
    • 1
  • Muhammad Qasim
    • 4
  • G. Mandela Fernández-Grandon
    • 5
  • Muhammad Shahid
    • 6
  • Mo Wang
    • 1
    Email author
  1. 1.Hube Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.Department of Agriculture Entomology sectionBacha Khan University CharsaddaCharsaddaPakistan
  3. 3.Cereal Crop Research InstituteNowsheraPakistan
  4. 4.College of Plant Protection Fujian Agriculture and Forest UniversityFuzhouChina
  5. 5.Natural Resources InstituteUniversity of GreenwichKentUK
  6. 6.Department of Agriculture and Agribusiness ManagementUniversity of KarachiKarachiPakistan

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