BACKGROUND: The cabbage moth, Mamestra brassicae, is a polyphagous pest that attacks several crops. Here, the sublethal and lethal effects of chlorantraniliprole and indoxacarb were investigated on the developmental stages, detoxification enzymes, reproductive activity, calling behavior, peripheral physiology, and pheromone titer of M. brasssicae. Methods: To assess pesticide effects, the second instar larvae were maintained for 24 h on a semi-artificial diet containing insecticides at their LC10, LC30, and LC50 concentrations. RESULTS: M. brassicae was more susceptible to chlorantraniliprole (LC50 = 0.35 mg/L) than indoxacarb (LC50 = 1.71 mg/L). A significantly increased developmental time was observed with both insecticides at all tested concentrations but decreases in pupation rate, pupal weight, and emergence were limited to the LC50 concentration. Reductions in both the total number of eggs laid per female and the egg viability were observed with both insecticides at their LC30 and LC50 concentrations. Both female calling activity and the sex pheromone (Z11-hexadecenyl acetate and hexadecenyl acetate) titer were significantly reduced by chlorantraniliprole in LC50 concentration. Antennal responses of female antennae to benzaldehyde and 3-octanone were significantly weaker than controls after exposure to the indoxocarb LC50 concentration. Significant reductions in the enzymatic activity of glutathione S-transferases, mixed-function oxidases, and carboxylesterases were observed in response to both insecticides.

Animal Ecology and Tropical Biology University of Würzburg 97070 Würzburg Germany

Department of Bioassay Central Agricultural Pesticides Laboratory Agricultural Research Center Giza 12618 Egypt

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

Department of Plant Protection Biology Swedish University of Agricultural Sciences 23053 Uppsala Sweden

Plant Protection Institute Centre for Agricultural Research Eötvös Lóránd Research Network 1022 Budapest Hungary

Plant Virus and Vector Interactions Crop Research Institute 16106 Prague Czech Republic

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Shi B.C., Gong Y.J., Lu H. The identification and control of Mamestra brassicae (L.) (Lepidoptera: Noctuidae) China Veget. 2005;9:56.

Cartea M., Padilla G., Vilar M., Velasco P. Incidence of the major Brassica pests in North-western Spain. J. Econ. Entomol. 2009;102:767–773. doi: 10.1603/029.102.0238. PubMed DOI

Savary S., Willocquet L., Pethybridge S.J., Esker P., McRoberts N., Nelson A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019;3:430–439. doi: 10.1038/s41559-018-0793-y. PubMed DOI

Cartea M.E., Francisco M., Lema M., Soengas M., Velasco P. Resistance of cabbage (Brassica oleracea capitata Group) crops to Mamestra brassicae. J. Econ. Entomol. 2010;103:1866–1874. doi: 10.1603/EC09375. PubMed DOI

Devetak M., Vidrih M., Trdan S. Cabbage moth (Mamestra brassicae L.) and bright-line brown-eyes moth (Mamestra oleracea L.)-presentation of the species, their monitoring and control measures. Acta Agric. Sloven. 2010;95:149–156. doi: 10.2478/v10014-010-0011-3. DOI

Mazurkiewicz A., Tumialis D., Jakubowska M. Biological control potential of native entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) against Mamestra brassicae L. (Lepidoptera: Noctuidae) Agriculture. 2020;10:388. doi: 10.3390/agriculture10090388. DOI

Tabashnik B.E., Mota-sanchez D., Whalon M.E., Hollingworth R.M., Carriere Y. Defining terms for proactive management of resistance to Bt crops and pesticides. J. Econ. Entomol. 2014;107:496–507. doi: 10.1603/EC13458. PubMed DOI

Bentley K.S., Fletcher J.L., Woodward M.D. Chlorantraniliprole: An insecticide of the anthranilic diamide class. In: Krieger R., editor. Hayes’ Handbook of Pesticide Toxicology. Academic Press; London, UK: 2010. pp. 2232–2242.

Liu Y., Gao Y., Liang G., Lu Y. Chlorantraniliprole as a candidate pesticide used in combination with the attracticides for lepidopteran moths. PLoS ONE. 2017;12:e0180255. doi: 10.1371/journal.pone.0180255. PubMed DOI PMC

Nehare S., Moharil M.P., Ghodki B.S., Lande G.K., Bisane K.D., Thakare A.S., Barkhade U.P. Biochemical analysis and synergistic suppression of indoxacarb resistance in Plutella xylostella L. J. Asia Pac. Entomol. 2010;13:91–95. doi: 10.1016/j.aspen.2009.12.002. DOI

Pereira N.C. Evaluation of the toxic effect of insecticide chlorantraniliprole on the silkworm (Lepidoptera: Bombycidae) Open J. Anim. Sci. 2013;3:343–353.

Shono T., Zhang L., Scott J.G. Indoxacarb resistance in the housefly, Musca domestica. Pestic. Biochem. Physiol. 2004;80:106–112. doi: 10.1016/j.pestbp.2004.06.004. DOI

Tsurubuchi Y., Karasawa A., Nagata K.T., Shono T., Konno Y. Insecticidal activity of oxadiazine insecticide indoxacarb and its N-decarbomethoxylated metabolite and their modulations of voltage-gated Na+ channels. Appl. Entomol. Zool. 2001;36:381–385. doi: 10.1303/aez.2001.381. DOI

Wing K.D., Sacher M., Kagaya Y., Tsurubuchi Y., Mulderig L., Connair M., Schnee M. Bioactivation and mode of action of the oxadiazine indoxacarb in insects. Crop Prot. 2000;19:537–545. doi: 10.1016/S0261-2194(00)00070-3. DOI

Brugger K.E., Cole P.G., Newman I.C., Parker N., Scholz B., Suvagia P., Walker G., Hammond T.G. Selectivity of chlorantraniliprole to parasitoid wasps. Pest Manag. Sci. 2010;66:1075–1081. doi: 10.1002/ps.1977. PubMed DOI

Dinter A., Brugger K., Bassi A., Frost N.M., Woodward M.D. Chlorantraniliprole (DPX-E2Y45, DuPont Rynaxypyr, Coragen, and Altacor insecticide)—A novel anthranilic diamide insecticide demonstrating low toxicity and low risk for beneficial insects and predatory mites. IOBC/WPRS Bull. 2008;35:128–135.

Gontijo L.M., Celestino D., Queiroz O.S., Narciso R., Guedes C., Picanço M.C. Impacts of azadirachtin and chlorantraniliprole on the developmental stages of pirate bug predators (Hemiptera: Anthocoridae) of the tomato pinworm Tuta absoluta (Lepidoptera: Gelechiidae) Fla. Entomol. 2015;98:59–64. doi: 10.1653/024.098.0111. DOI

Lahm G.P., Cordova D., Barry J.D. New and selective ryanodine receptor activators for insect control. Bioorg. Med. Chem. 2009;17:4127–4133. doi: 10.1016/j.bmc.2009.01.018. PubMed DOI

Lahm G.P., Stevenson T.M., Selby T.P., Freudenberger J.H., Cordova D., Flexner L., Bellin C.A., Dubas C.M., Smith B.K., Hughes K.A., et al. RynaxypyrTM: A new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator. Bioorg. Med. Chem. Lett. 2007;17:6274–6279. doi: 10.1016/j.bmcl.2007.09.012. PubMed DOI

Sattelle D.B., Cordova D., Cheek T.R. Insect ryanodine receptors: Molecular targets for novel pest control chemicals. Invertebr. Neurosci. 2008;8:107–119. doi: 10.1007/s10158-008-0076-4. PubMed DOI

Guo L., Desneux N., Sonoda S., Liang P., Han P., Gao X.-W. Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Prot. 2013;48:29–34. doi: 10.1016/j.cropro.2013.02.009. DOI

Wing K.D., Andaloro J.T., McCann S.F., Salgado V.L. Indoxacarb and the sodium channel blocker insecticides: Chemistry, physiology, and biology in insects. In: Gilbert L.I., editor. Comprehensive Molecular Insect Science. Elsevier; Amsterdam, The Netherlands: 2005. pp. 31–53.

Zhao X., Ikeda T., Salgado V.L., Yeh J.Z., Narahashi T. Block of two subtypes of sodium channels in cockroach neurons. NeuroToxicology. 2005;26:455–465. doi: 10.1016/j.neuro.2005.03.007. PubMed DOI

Lapied B., Grolleau F., Sattelle D.B. Indoxacarb, an oxadiazine insecticide, blocks insect neuronal sodium channels. Br. J. Pharmacol. 2001;132:587–595. doi: 10.1038/sj.bjp.0703853. PubMed DOI PMC

Desneux N., Decourtye A., Delpuech J.M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007;52:81–106. doi: 10.1146/annurev.ento.52.110405.091440. PubMed DOI

de Franca S.M., Breda M.O., Barbosa D.R.S., Araujo A.M.N., Guedes C.A. Biological Control of Pest and Vector Insects. IntechOpen; London, UK: 2017. The sublethal effects of insecticides in insects; pp. 23–39.

Gesraha M.A., Ebeid A.R. Impact of indoxacarb and sulfurformulation on aphid and three specific predators in Okra fields. Bull. Natl. Res. Cent. 2021;45:10. doi: 10.1186/s42269-020-00464-z. DOI

He F., Sun S., Tan H., Sun X., Qin C., Ji S., Li X., Zhang J., Jiang X. Chlorantraniliprole against the black cutworm Agrotis ipsilon (Lepidoptera: Noctuidae): From biochemical/physiological to demographic responses. Sci. Rep. 2019;9:10328. doi: 10.1038/s41598-019-46915-0. PubMed DOI PMC

Monteiro H.R., Pestana J.L.T., Novais S.C., Soares A.M.V.M., Lemos M.F.L. Toxicity of the insecticides spinosad and indoxacarb to the non-target aquatic midge Chironomus riparius. Sci. Total Environ. 2019;666:1283–1291. doi: 10.1016/j.scitotenv.2019.02.303. PubMed DOI

Moustafa M.A.M., Fouad E.A., Abdel-Mobdy Y., Hamow K.Á., Mikó Z., Molnár B.P., Fónagy A. Toxicity and sublethal effects of chlorantraniliprole and indoxacarb on Spodoptera littoralis (Lepidoptera: Noctuidae) Appl. Entomol. Zool. 2021;56:115–124. doi: 10.1007/s13355-020-00721-7. DOI

Awad M., Ibrahim E.S., Osman E.I., Elmenofy W.H., Mahmoud A.M., Atia M.A.M., Moustafa M.A.M. Nano-insecticides against the black cutworm Agrotis ipsilon (Lepidoptera: Noctuidae): Toxicity, development, enzyme activity, and DNA mutagenicity. PLoS ONE. 2022;17:e0254285. doi: 10.1371/journal.pone.0254285. PubMed DOI PMC

Wang Q., Rui C., Wang Q., Wang L., Li F., Nahiyoon S.A., Yuan H., Cui L. Mechanisms of Increased Indoxacarb Toxicity in Methoxyfenozide-Resistant Cotton Bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) Toxics. 2020;8:71. doi: 10.3390/toxics8030071. PubMed DOI PMC

Zhang Q., Liu Y.Q., Wyckhuys K.A.G., Liang H.S., Desneux N., Lu Y.H. Lethal and sublethal effects of chlorantraniliprole on Helicoverpaarmigera adults enhance the potential for use in attract-and-kill control strategies. Entomol. Gen. 2021;41:111–120. doi: 10.1127/entomologia/2020/1104. DOI

Zhang D.W., Dai C.C., Ali A., Liu Y.Q., Pan Y., Desneux N., Lu Y.H. Lethal and sublethal effects of chlorantraniliprole on the migratory moths Agrotis ipsilon and Agrotis segetum: New perspectives for pest management strategies. Pest Manag. Sci. 2022;78:4105–4113. doi: 10.1002/ps.7029. PubMed DOI

Zhu W., Wang J., Zhang Y. The Mechanism of Chlorantraniliprole Resistance and Detoxification in Trichogramma chilonis (Hymenoptera: Trichogrammatidae) J. Insect Sci. 2022;22:7. doi: 10.1093/jisesa/ieac044. PubMed DOI PMC

Yu S.J. Detoxification Mechanisms in Insects. In: Capinera J.L., editor. Encyclopedia of Entomology. Springer; Berlin/Heidelberg, Germany: 2004. pp. 1187–1201.

Vojoudi S., Saber M., Gharekhani G., Esfandiari E. Toxicity and sublethal effects of hexaflumuron and indoxacarb on the biological and biochemical parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Iran. Crop Prot. 2017;91:100–107. doi: 10.1016/j.cropro.2016.09.020. DOI

Nagy B. Rearing of European corn borer (Ostrinia nubilalis Hbn.) on a simplified artificial diet. Acta Phytopathol. Acad. Sci. Hung. 1970;5:73–79.

Moustafa M.M.A., Kákai A., Awad M., Fónagy A. Sublethal effects of spinosad and emamectin benzoate on larval development and reproductive activities of the cabbage moth, Mamestra brassicae L. (Lepidoptera: Noctuidae) Crop Prot. 2016;90:197–204. doi: 10.1016/j.cropro.2016.09.004. DOI

Xu L., Zhao J., Xu D., Xu G., Gu Z., Xiao Z., Dewer Y., Zhang Y. Application of transcriptomic analysis to unveil the toxicity mechanisms of fall armyworm response after exposure to sublethal chlorantraniliprole. Ecotoxicol. Environ. Saf. 2022;230:113145. doi: 10.1016/j.ecoenv.2021.113145. PubMed DOI

Moustafa M.A.M., Elmenofy W.H., Osman E.A., El-Said N.A., Awad M. Biological impact, oxidative stress and adipokinetic hormone activities of Agrotis ipsilon in response to bioinsecticides. Plant Prot. Sci. 2022;58:326–337. doi: 10.17221/46/2022-PPS. DOI

Hansen L.G., Hodgson E. Biochemical characteristics of insect microsomes: N-and O-demethylation. Biochem. Pharmacol. 1971;20:1569–1578. doi: 10.1016/0006-2952(71)90285-1. PubMed DOI

Van Asperen K. A study of housefly esterases by means of a sensitive colorimetric method. J. Insect Physiol. 1962;8:401–416. doi: 10.1016/0022-1910(62)90074-4. DOI

Habing W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974;249:7130–7139. doi: 10.1016/S0021-9258(19)42083-8. PubMed DOI

Hull J.J., Brent C.S., Choi M.-Y., Mikó Z., Fodor J., Fónagy A. Molecular and Functional Characterization of Pyrokinin-Like Peptides in the Western Tarnished Plant Bug Lygus hesperus (Hemiptera: Miridae) Insects. 2021;12:914. doi: 10.3390/insects12100914. PubMed DOI PMC

Molnár B.P., Tóth Z., Kárpáti Z. Synthetic blend of larval frass volatiles repel oviposition in the invasive box tree moth, Cydalima perspectalis. J. Pest Sci. 2017;90:873–885. doi: 10.1007/s10340-017-0837-0. DOI

Ephrussi B., Beadle G.W. Development of eye colors in Drosophila: Transplantation experiments on the interaction of vermilion with other eye colors. Genetics. 1936;22:65–75. doi: 10.1093/genetics/22.1.65. PubMed DOI PMC

Jacquin E., Nagnan P., Frerot B. Identification of hairpencil secretion from male Mamestra brassicae (L.) (Lepidoptera: Noctuidae) and electroantennogram studies. J. Chem. Ecol. 1991;17:239–246. doi: 10.1007/BF00994436. PubMed DOI

Ulland S., Ian E., Stranden M., Borg-Karlson A.-K., Mustaparta H. Plant Volatiles Activating Specific Olfactory Receptor Neurons of the Cabbage Moth Mamestra brassicae L. (Lepidoptera, Noctuidae) Chem. Senses. 2008;33:509–522. doi: 10.1093/chemse/bjn018. PubMed DOI

Wei S., Xiao X., Wei L., Li L., Li G., Liu F., Xie J., Yu J., Zhong Y. Development and comprehensive HS-SPME/GC-MS analysis optimization, comparison, and evaluation of different cabbage cultivars (Brassica oleracea L. var. capitata L.) volatile components. Food Chem. 2020;15:128166. doi: 10.1016/j.foodchem.2020.128166. PubMed DOI

Finney D.J. Probit Analysis. Cambridge University Press; Cambridge, UK: 1971.

Gomez A.K., Gomez A.A. Statistical Procedures for Agricultural Research. John Wiley and Sons; New York, NY, USA: 1984. pp. 295–310.

Kandil M.A., Abdel-kerim R.N., Moustafa M.A.M. Lethal and sublethal effects of bio-and chemical insecticides on the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) Egypt. J. Biol. Pest Cont. 2020;30:76. doi: 10.1186/s41938-020-00278-1. DOI

Kong F., Song Y., Zhang Q., Wang Z., Liu Y. Sublethal Effects of Chlorantraniliprole on Spodoptera litura (Lepidoptera: Noctuidae) Moth: Implication for Attract-And-Kill Strategy. Toxics. 2021;9:20. doi: 10.3390/toxics9020020. PubMed DOI PMC

Hafeez M., Li X., Ullah F., Zhang Z., Zhang J., Huang J., Fernández-Grandon G.M., Khan M.M., Siddiqui J.A., Chen L., et al. Down-Regulation of P450 genes enhances susceptibility to indoxacarb and alters physiology and development of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) Front. Physiol. 2022;9:884447. doi: 10.3389/fphys.2022.884447. PubMed DOI PMC

Lai T., Su J. Assessment of resistance risk in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag. Sci. 2011;67:1468–1472. doi: 10.1002/ps.2201. PubMed DOI

Bird L.J. Baseline susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to indoxacarb, emamectin benzoate, and chlorantraniliprole in Australia. J. Econ. Entomol. 2015;108:294–300. doi: 10.1093/jee/tou042. PubMed DOI

Cui L., Wang Q.Q., Qi H.L., Wang Q.Y., Yuan H.Z., Rui C.H. Resistance selection of indoxacarb in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): Cross-resistance, biochemical mechanisms and associated fitness costs. Pest. Manag. Sci. 2018;74:2636–2644. doi: 10.1002/ps.5056. PubMed DOI

El-Dewy M. Influence of some novel insecticides on physiological and biological aspects of Spodoptera littoralis (Boisduval) Alexandria Sci. Exch. J. 2017;38:250–258.

Wang Z., Wang N., Yu Q., Xue C. Sublethal effects of an indoxacarb enantiomer insecticide on Plutella xylostella caterpillar and Chrysoperla sinica predator. Ecotoxicol. Environ. Saf. 2017;249:114400. doi: 10.1016/j.ecoenv.2022.114400. PubMed DOI

Xu Z., Cao G.C., Dong S.L. Changes of sex pheromone communication systems associated with tebufenozide and abemectin resistance in diamond-back moth Plutella xylostella (L.) J. Chem. Ecol. 2010;36:526–534. doi: 10.1007/s10886-010-9785-3. PubMed DOI

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. Effect of larvae treated with mixed Biopesticide Bacillus thuringiensis—Abamectin on sex pheromone communication system in cotton Bollworm, Helicoverpa armigera. PLoS ONE. 2013;8:e68756. doi: 10.1371/journal.pone.0068756. PubMed DOI PMC

Bloch G., Hazan E., Rafaeli A. Circadian rhythms and endocrine functions in adult insects. J. Insect Physiol. 2013;59:56–69. doi: 10.1016/j.jinsphys.2012.10.012. PubMed DOI

Hull J.J., Fónagy A. Molecular basis of pheromonogenesis regulation in moths. In: Picimbon J.-F., editor. Olfactory Concepts of Insect Control—Alternative to Insecticides. Springer Nature; Geneva, Switzerland: 2019. pp. 151–202.

Raina A.K. Neuroendocrine control of sex pheromone biosynthesis in Lepidoptera. Annu. Rev. Entomol. 1993;38:329–349. doi: 10.1146/annurev.en.38.010193.001553. PubMed DOI

Wei H.-Y., Du J.-W. Sublethal effects of larval treatment with delta-methrin on moth sex pheromone communication system of the Asian corn borer, Ostrinia furnacalis. Pest Biochem. Physiol. 2004;80:12–20. doi: 10.1016/j.pestbp.2004.05.001. DOI

Stark J.D., Rangus T.M. Lethal and sublethal effects of the neem insecticide formulation, Margosan-O, on the pea aphid. Pestic. Sci. 1994;41:155–160. doi: 10.1002/ps.2780410212. DOI

Mahmoudvand M., Garjan A.S., Abbasipour H. Ovicidal effect of some insecticides on the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae) Chil. J. Agric. Res. 2011;71:226–230. doi: 10.4067/S0718-58392011000200007. DOI

Nozad-Bonab Z., Hejazi M.J., Iranipour S., Arzanlou M. Lethal and sublethal effects of some chemical and biological insecticides on Tuta absoluta (Lepidoptera: Gelechiidae) eggs and neonates. J. Econ. Entomol. 2017;110:1138–1144. doi: 10.1093/jee/tox079. PubMed DOI

Wang G., Huang X., Wei H., Henry Y., Fadamiro H.Y. Sublethal effects of larval exposure to indoxacarb on reproductive activities of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae) Pestic. Biochem. Physiol. 2011;101:227–231. doi: 10.1016/j.pestbp.2011.09.010. DOI

Wu S.-X., Chen Y., Lei Q., Peng Y.-Y., Jiang H.-B. Sublethal Dose of β-Cypermethrin Impairs the Olfaction of Bactrocera dorsalis by Suppressing the Expression of Chemosensory Genes. Insects. 2022;13:721. doi: 10.3390/insects13080721. PubMed DOI PMC

Tappert L., Pokorny T., Hofferberth J., Ruther J. Sublethal doses of imidacloprid disrupt sexual communication and host finding in a parasitoid wasp. Sci. Rep. 2017;7:42756. doi: 10.1038/srep42756. PubMed DOI PMC