Skip to main content
SpringerLink
Log in

Toxicity and sublethal effects of chlorantraniliprole and indoxacarb on Spodoptera littoralis (Lepidoptera: Noctuidae)

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Chlorantraniliprole and indoxacarb insecticides exhibit good efficiency for control lepidopteran pests. The current study is a comprehensive analysis of the effect of lethal and sublethal concentrations of these insecticides on Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) by using the leaf dipping technique. The LC50 values ranged from 0.06 to 1.07 mg/L, and 0.005 to 0.81 mg/L for chlorantraniliprole and indoxacarb, respectively. Our results showed that the treatment of the 2nd instar larvae with LC50 concentrations of these insecticides significantly increased the length of larval and pupal duration as well as pupal weight in most cases. While, no significant differences have been found in the percentage of hatchability except for LC50 equivalent of indoxacarb. Female behavior regarding calling activity decreased by 50–60% following exposure to the LC50 concentration of both insecticides. Gas chromatography analysis results showed that both insecticides lowered pheromone titer except at chlorantraniliprole LC50 equivalent for (Z,E)-9,12-tetradecadien-l-ol acetate, and indoxacarb LC10 equivalent for (Z)-9-tetradecenyl acetate. Additionally, the activity of mixed-function oxidases and glutathione S-transferase were elevated relative to control. The carboxylesterase activity significantly increased when assayed with both chlorantraniliprole concentrations and indoxacarb LC10 equivalent. These results indicate that chlorantraniliprole and indoxacarb could be effective for S. littoralis control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ando T, Inomata S, Yamamoto M (2004) Lepidopteran sex pheromones. Top Curr Chem 239:51–96

    CAS  PubMed  Google Scholar 

  • Aydin MH, Gürkan MO (2006) The efficacy of spinosad on different strains of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Turk J Biol 30:5–9

    CAS  Google Scholar 

  • Bentley KS, Fletcher JL, Woodward MD (2010) Chlorantraniliprole: an insecticide of the anthranilic diamide class. In: Krieger R (ed) Hayes’ handbook of pesticide toxicology. Academic Press, London, pp 2232–2242

    Google Scholar 

  • Bird LJ (2015) Baseline susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to indoxacarb, emamectin benzoate, and chlorantraniliprole in Australia. J Econ Entomol 108:294–300

    CAS  PubMed  Google Scholar 

  • Bloch G, Hazan E, Rafaeli A (2013) Circadian rhythms and endocrine functions in adult insects. J Insect Physiol 59:56–69

    CAS  PubMed  Google Scholar 

  • Campion DG, Hunter-Jones P, McVeigh LJ, Hall DR, Lester R, Nesbitt BF (1980) Modification of the attractiveness of the primary pheromone component of the Egyptian cotton leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae), by secondary pheromone components and related chemicals. Bull Entomol Res 70:417–434

    CAS  Google Scholar 

  • Cao C, Zhang J, Gao X, Liang P, Guo H (2008) Overexpression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pestic Biochem Physiol 90:175–180

    CAS  Google Scholar 

  • Carter D (1984) Pest lepidoptera of Europe with special reference to the British Isles. Junk Publishers, Dordrecht

    Google Scholar 

  • Crava CM, Bruetting C, Baldwin IT (2016) Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants. BMC Genom 17:1005

    Google Scholar 

  • Cui L, Wang Q, Qi H, Wang Q, Yuan H, Ru C (2018) Resistance selection of indoxacarb in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): cross-resistance, biochemical mechanisms and associated fitness costs. Pest Manag Sci 74:2636–2644

    CAS  PubMed  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    CAS  PubMed  Google Scholar 

  • Dunkelblum E, Kehat M, Harel M, Gordon D (1987) Sexual behaviour and pheromone titre of the Spodoptera littoralis female moth. Entomol Exp Appl 44:241–247

    CAS  Google Scholar 

  • El-Defrawi ME, Tappozada AT, Salama A, El-Khishen SA (1964) Toxicological studies on the Egyptian cotton leafworm prodenia litura F.II. Reversions of Toxaphene resistance in the Egyptian cotton leafworm. J Econ Entomol 18:265–267

    Google Scholar 

  • El-Dewy MEH (2017) Influence of some novel insecticides on physiological and biological aspects of Spodoptera littoralis (Boisduval). Alex Sci Exchange J 38:250–258

    Google Scholar 

  • El-Sheikh EA (2015) Comparative toxicity and sublethal effects of emamectin benzoate, lufenuron and spinosad on Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae). Crop Prot 67:228–234

    CAS  Google Scholar 

  • El-Sheikh ESAM, El-Saleh MA, Aioub AA, Desuky WM (2018) Toxic effects of neonicotinoid insecticides on a field strain of cotton leafworm, Spodoptera littoralis. Asian J Biol Sci 11:179–185

    CAS  Google Scholar 

  • Gamal A, Abdel-Raof E, Hossam E (2009) Resistance stability to spinosad and abamectin in the cotton leafworm, Spodoptera littoralis (Bosid.). Resist Pest Manag Newslett 19:21–26

    Google Scholar 

  • Gamil WE, Mariy FM, Youssef LA, Abdel Halim SM (2011) Effectof Indoxacarb on some biological and biochemical aspects of Spodoptera littoralis Boisd. larvae. Ann Agric Sci 6:121–126

    Google Scholar 

  • Gondhalekar AD, Song C, Scharf ME (2011) Development of strategies for monitoring indoxacarb and gel bait susceptibility in the German cockroach (Blattodea: Blattellidae). Pest Manag Sci 67:262–270

    CAS  PubMed  Google Scholar 

  • Gondhalekar AD, Nakayasu ES, Silva I, Cooper B, Scharf ME (2016) Indoxacarb biotransformation in the German cockroach. Pestic Biochem Physiol 134:14–23

    CAS  PubMed  Google Scholar 

  • Guo L, Desneux N, Sonoda S, Liang P, Han P, Gao X-W (2013) Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Prot 48:29–34

    CAS  Google Scholar 

  • Habing WH, Pabst J, Jackoby WB (1974) Glutathione S transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Google Scholar 

  • Hannig GT, Ziegler M, Marcon PG (2009) Feeding cessation effects of chlorantraniliprole, a new anthranilic diamide insecticide, in comparison with several insecticides in distinct chemical classes and mode-of-action groups. Pest Manag Sci 65:969–974

    CAS  PubMed  Google Scholar 

  • Hansen LG, Hodgson E (1971) Biochemical characteristics of insect microsomes and O-demethylation. Biochem Pharm 20:1569–1578

    CAS  PubMed  Google Scholar 

  • Harder HH, Riley SL, McCann SF, Irving SN (1996) DPXMP062: a novel broad-spectrum, environmentally soft, insect control compound. In: Proceedings of the Brighton conference, Brighton, UK

  • He F, Shiang S, Haili T, Xiao S, Chao Q, Shoumin J, Xiangdong L, Jiwang Z, Xingyin J (2019) Chlorantraniliprole against the black cutworm Agrotis ipsilon (Lepidoptera: Noctuidae): from biochemical/physiological to demographic responses. Sci Rep 9:10328. https://doi.org/10.1038/s41598-019-46915-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hull JJ, Fónagy A (2019) Molecular basis of pheromonogenesis regulation in moths. In: Picimbon J-F (ed) Olfactory concepts of insect control—alternative to insecticides. Springer, Cham, pp 151–202

    Google Scholar 

  • Insecticide Resistance Action Committee, IRAC (2019) IRAC mode of action classification, Ver. 9.3, IRAC Mode of Action Working Group. http://www.MoA-Classification_v9.4_3March20%20.pdf

  • Ishaaya I, Yablonski S, Horowitz AR (1995) Comparative toxicity of two ecdystroids, RH-2485 and RH-5992 on susceptible and pyrethroid resistant strains of the Egyption cotton leafworm, Spodoptera littoralis. Phytoparasit 23:139–145

    CAS  Google Scholar 

  • Lahm GP, Selby TP, Freudenberger JH, Stevenson TM, Myers BJ, Seburyamo G, Smith BK, Flexner L, Clark CE, Cordova D (2005) Insecticidal anthranilic diamides: a new class of potent ryanodine receptor activators. Bioorg Med Chem Lett 15:4898–4906

    CAS  PubMed  Google Scholar 

  • Lahm GP, Cordova D, Barry JD (2009) New and selective ryanodine receptor activators for insect control. Bioorg Med Chem Lett 17:4127–4133

    CAS  Google Scholar 

  • Lai T, Su J (2011) Assessment of resistance risk in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 67:1468–1472

    CAS  PubMed  Google Scholar 

  • Lanka SK, Ottea JA, Beuzelin JM, Stout MJ (2013) Effects of chlorantraniliprole and thiamethoxam rice seed treatments on egg numbers and first instar survival of Lissorhoptrus oryzophilus (Coleoptera: Curculionidae). J Econ Entomol 106:181–188

    CAS  PubMed  Google Scholar 

  • Liu DG, Trumble JT (2005) Interactions of plant resistance and insecticides on the development and survival of Bactericerca cockerelli [Sulc] (Homoptera: Psyllidae). Crop Prot 24:111–117

    Google Scholar 

  • Liu H, Xiao P, Liu Y, He J, Qiu X, Jiao Y (2011) Resistance risk analysis and biochemical mechanism of Spodoptera litura to indoxacarb. Agrochemicals 50:197–200

    CAS  Google Scholar 

  • Mahmoudvand M, Garjan AS, Abbasipour H (2011) Ovicidal effect of some insecticides on the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Chil J Agric Res 71(2):226–230

    Google Scholar 

  • Marco MP, Fabriàs G, Lázaro G, Camps F (1996) Evidence for both humoral and neural regulation of sex pheromone biosynthesis in Spodoptera littoralis. Arch Insect Biochem Physiol 31:157–167

    CAS  Google Scholar 

  • Moustafa MAM, Kákai A, Awad M, Fónagy A (2016) Sublethal effects of spinosad and emamectin benzoate on larval development and reproductive activities of the cabbage moth, Mamestra brassicae L. (Lepidoptera: Noctuidae). Crop Prot 90:197–204

    CAS  Google Scholar 

  • Nesbitt BF, Beevor PS, Cole RA, Lester R, Poppi RG (1973) Sex pheromones of two noctuid moths. Nature 244:208–209

    CAS  Google Scholar 

  • Parsaeyan E, Saber M, Bagheri M (2013) Toxicity of emamectin benzoate and cypermethrin on biological parameters of cotton bollworm, Helicoverpa armigera (Hübner) in laboratory conditions. Crop Prot 2:477–485

    Google Scholar 

  • Percy JE, Weatherston J (1974) Gland structure and pheromone production in insects. In: Birch MC (ed) Pheromones. North Holland Publishing Company, Amsterdam, pp 11–34

    Google Scholar 

  • Raina AK, Jaffe H, Klun JA, Ridgway RL, Hayes DK (1987) Characterization of a neurohormone that controls sex pheromone production in Heliothis zea. J Insect Physiol 33:809–814

    CAS  Google Scholar 

  • SAS (2001) User guide: statistics (Release 8.02). SAS Institute, Cary, NC

    Google Scholar 

  • Sattelle DB, Cordova D, Cheek TR (2008) Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invert Neurosci 8:107–119

    CAS  PubMed  Google Scholar 

  • Shen L-Z, Chen P-Z, Xu Z-H, Deng J-Y, Harris M-K, Wanna R, Wang F-M, Zhou G-X, Yao Z-L (2013) Effect of larvae treated with mixed biopesticide Bacillus thuringiensis—Abamectin on sex pheromone communication system in cotton bollworm, Helicoverpa armigera. Plos One 8:e68756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sial AA, Brunner JF, Garczynski SF (2011) Biochemical characterization of chlorantraniliprole and spinetoram resistance in laboratory-selected obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). Pestic Biochem Physiol 99:274–279

    CAS  Google Scholar 

  • Silvegren G, Löfstedt C, Rosén WQ (2005) Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis. J Insect Physiol 51:277–286

    CAS  PubMed  Google Scholar 

  • Stark JD, Rangus TM (1994) Lethal and sublethal effects of the neem insecticide formulation’,Margosan-O’, on the pea aphid. Pestic Sci 41:155–160

    CAS  Google Scholar 

  • Su J, Lai T, Li J (2012) Susceptibility of field populations of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in China to chlorantraniliprole and the activities of detoxification enzymes. Crop Prot 42:217–222

    CAS  Google Scholar 

  • Tamaki Y, Yushima T (1974) Sex pheromone of the cotton leafworm, Spodoptera littoralis. J Insect Physiol 20:1005–1014

    CAS  PubMed  Google Scholar 

  • The Pherobase. http://www.pherobase.com/

  • Van Asperen K (1962) A study of housefly esterase by means of a sensitive colorimetric method. J Insect Physiol 8:401–416

    CAS  Google Scholar 

  • Vojoudi S, Saber M, Gharekhani G, Esfandiari E (2017) Toxicity and sublethal effects of hexaflumuron and indoxacarb on the biological and biochemical parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Iran. Crop Prot 91:100–107

    CAS  Google Scholar 

  • Wang G, Huang X, Wei H, Fadamiro HY (2011) Sublethal effects of larval exposure to indoxacarb on reproductive activities of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Pest Biochem Physiol 101:227–231

    CAS  Google Scholar 

  • Wing KD, Schnee ME, Sacher M, Connair M (1998) A novel oxadiazine insecticide is bioactivated in lepidopteran larvae. Arch Insect Biochem Physiol 37:91–103

    CAS  Google Scholar 

  • Wing KD, Sacher M, Kagaya Y, Tsurubuchi Y, Mulderig L, Connair M, Schnee M (2000) Bioactivation and mode of action of the oxadiazine indoxacarb in insects. Crop Prot 19:537–545

    CAS  Google Scholar 

  • Yin X-H, Wu Q-J, Li X-F, Zhang Y-J, Xu B-Y (2008) Sublethal effects of spinosad on Plutella xylostella (Lepidoptera: Yponomeutidae). Crop Prot 27:1385–1391

    CAS  Google Scholar 

  • Yu SJ (2004) Detoxification mechanisms in insects. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Berlin, pp 1187–1201

    Google Scholar 

  • Zhao X, Ikeda T, Salgado VL, Yeh JZ, Narahashi T (2005) Block of two types of sodium channels in cockroach neurons by indoxacarb insecticides. Neurotoxicology 26:455–465

    CAS  PubMed  Google Scholar 

  • Zhong H, Li F, Chen J, Zhang J, Li F (2017) Comparative transcriptome analysis reveals host-associated differentiation in Chilo suppressalis (Lepidoptera: crambidae). Sci Rep 7:13778

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by the Science & Technology Development Fund (STDF), Egypt (Project ID; 33353). Author P. B. M. is thankful for the János Bolyai Grant fellowship. We would like to express our special thanks to Dr. Ibrahim S. Ahmed (Faculty of Agriculture, Cairo University, Egypt), Dr. József Fodor (Plant Protection Institute of CAR, Budapest, Hungary) and Dr. J. Joe Hull (USDA, ARS, Maricopa AZ, U.S.A.) for improving the manuscript considerably, including English grammar and styles.

Author information

Authors and Affiliations

  1. Department of Economic Entomology and Pesticides, Faculty of Agriculture, Cairo University, Giza, 12613, Egypt

    Moataz A. M. Moustafa & Yasmin Abdel-Mobdy

  2. Bioassay Department, Central Agricultural Pesticides Laboratory, Agriculture Research Center, Giza, 12618, Egypt

    Eman A. Fouad

  3. Zoology Department, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, 1022, Budapest, Hungary

    Kamirán Áron Hamow, Béla Péter Molnár & Adrien Fónagy

  4. Lendület Evolutionary Group, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, 1022, Budapest, Hungary

    Zsanett Mikó

Authors
  1. Moataz A. M. Moustafa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eman A. Fouad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasmin Abdel-Mobdy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kamirán Áron Hamow
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zsanett Mikó
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Béla Péter Molnár
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Adrien Fónagy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Moataz A. M. Moustafa.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moustafa, M.A.M., Fouad, E.A., Abdel-Mobdy, Y. et al. Toxicity and sublethal effects of chlorantraniliprole and indoxacarb on Spodoptera littoralis (Lepidoptera: Noctuidae). Appl Entomol Zool 56, 115–124 (2021). https://doi.org/10.1007/s13355-020-00721-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-020-00721-7

Keywords

Search

Navigation