Effect of Sublethal Dose/Concentration on Various Insect Behaviors

Victor George Siahaya


Most of the studies on the impact of insecticides have always used acute toxicity with an indicator of death, whereas the lethal effect cannot fully determine the effect of the insecticide on insects. Overall, the effect of sublethal dose/concentration of insecticides can cause biological effects, disrupt egg number, laying period, larva and pupal weight, development period, life span and fertility rate, in addition to influencing feeding behavior, spawning period, locomotor system and reducing or increasing production and response to pheromones, physiological effects on the reproductive and immune systems and the nutritional status of insects. This suggests that the sublethal effect is very important to form the basis for analysis of insecticide risk. In addition, the sublethal effect also affects the presence of natural enemies and other useful insects, so it is hoped that more studies on their impact on non-target insects are expected.

Keywords: biological effects, natural enemies, pheromones, sublethal effect

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Stark, J.D. and J.E. Banks. 2003. Population‐level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology. 48: 505–519.

Desneux, N., Decourtye, A., and J.M. Delpuech. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review Entomology. 52: 81–106.

Stark, J.D., Jepson, P.C. and D. Mayer. 1995. Limitations to the use of topical toxicity data for predictions of pesticide side effects in the field. Journal of Economic Entomology. 88(5): 1081–1088.

Lee, C.Y. 2000. Sublethal effects of insecticide on longevity, fecundity, and behaviour of insect pests: a review. Bioscience. 11: 107–112.

Singh, J.P. and K.K. Marwaha. 2000. Effects of sublethal concentrations of some insecticides on growth and development of maize stalk borer, Chilo partellus (Swinhoe) larvae. Shashpa. 7: 181–186.

Borgoni, P.C. and J.D. Vendramin. 2005. Sublethal effect of aqueous extracts of Trichilia spp. on Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) development on maize. Neotropical Entomology. 34: 311–317.

Mamood, A.N. and G.D. Waller. 1990. Recovery of learning responses by honey bees following sublethal exposure to permethrin. Physiological Entomology. 15: 55–60.

Lashkari, M.A., Sahragard, A. and M. Ghadamyari. 2007. Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Science. 14: 207–212.

Elzen, G.W., Maldonado, S.N. and M.G. Rojas. 2000. Lethal and sublethal effects of selected insecticides and an insect growth regulator on the boll weevil (Coleoptera: Curculionidae) ectoparasitoid Catolaccus grandis (Hymenoptera: Pteromalidae). Journal of Economic Entomology. 93: 300–303.

Haynes, K.F. 1988. Sublethal effects of neurotoxic insecticides on insect behavior. Annual Review Entomology. 33: 149–168.

Storch, G., Loeck, A.E., Borba, R.S,, Magano, D.A., Moraes, C.L. and C.L. Grutzmacher. 2007. The effect of sub-lethal do.ses of insecticides on artificial diet and caterpillars of Anticarsia gemmatalis (Lepidoptera: Noctuidae). Revista Brasileira de Agrociência. 13: 175–179.

Mahmoudvand, M., Abbasipour, H., Garjan, A.S. and A.R. Bandani 2012. Decrease in pupation and adult emergence of Plutella xylostella (L.) treated with hexaflumuron. Chilean Journal of Agricultural Research. 72: 206–211.

Dong, J., Wang, K., Li Y. and S. Wang. 2016. Lethal and sublethal effects of cyantraniliprole on Helicoverpa assulta (Lepidoptera: Noctuidae). Pesticide Biochemistry and Physiology.

Ootani, M.A., Aguiar, R.W., Ramos, A.C.C., Brito, D.R., Silva, J.B. and J.P. Cajazeira. 2013. Use of essential oils in agriculture. Journal of Biotechnology and Biodiversity. 4: 162–174.

Cruz, G.S., Teixeira, V.W., Oliveira, J.V., Teixeira, A.A.C., Araújo, A.C., Alves, T.J.S., Cunha, F.M. and M.O. Breda. 2015. Histological and histochemical changes by clove essential oil upon the gonads of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). International Journal of Morphology. 33: 1393–1400.

Cruz, G.S., Teixeira, V.W., Oliveira, J.V., Lopes, F.S.C., Barbosa, D.R.S., Breda, M.O., Dutra, K.A., Guedes, C.A., Navarro, D.M.A.F. and A.C.C. Teixeira. 2016. Sublethal effects of essential oils from Eucalyptus staigeriana (Myrtales: Myrtaceae), Ocimum gratissimum (Lamiales: Laminaceae), and Foeniculum vulgare (Apiales: Apiaceae) on the biology of Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Economic Entomology. 109: 660–666.

Bernardi, D., Oabne, S., Bernardi, O., Silva, A., Cunha, U.S., and M.S. Garcia. 2011. Efficiency and sublethal effects of neem on Bonagota salubricola (Meyrick) (Lepidoptera: Tortricidae). Revista Brasileira de Fruticultura. 33: 412–419.

De‐Ling, M.A., Gordh, G. and M.P Zalucki. 2000. Biological effects of azadirachtin on Helicoverpa armigera (Hübner) (Lepidoptera:Noctuidae) fed on cotton and artificial diet. Australian Journal of Entomology. 39: 301–304.

Wei H‐Y and, Du J‐W. 2004. Sublethal effects of larval treatment with deltamethrin on moth sex pheromone communication system of the Asian corn borer Ostrinia furnacalis. Pesticide Biochemistry and Physiology. 80:12–30.

Cutler, G.C. 2013. Insects, insecticides and hormesis: evidence and considerations for study. Dose Response. 11: 154–117.

Rabhi, K.K., Esancy, K., Voisin, A., Crespin, L., Le Corre, J., Tricoire‐Leignel, H., Anton, S. and C. Gadenne. 2012. Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect. PLoS One. 9(12): e114411.

Lalouette, L., Pottier, M., Wycke, M., Boitard, C., Bozzolan, F., Maria, A., Demondion, E., Chertemps, T., Lucas, P., Renault, D., Maibeche, M. and D. Siaussat. 2016. Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environmental Science and Pollution Research. 23: 3073–3085.

Delpuech, J., Gareau, E., Terrier, O. and P. Fouillet. 1998. Sublethal effects of the insecticide chlorpyrifos on ti‐ijz sex pheromonal communication of Trichogramma brassicae. Chemosphere. 36: 1775–1785.

Delpuech, J. and M. Delahaye. 2013. The sublethal effects of deltamethrin on Trichogramma behaviors during the exploitation of host patches. Science of the Total Environment. 447C: 274–279.

Ribeiro, C.R., Zanuncio, T.V., Ramalho, F.S., Silva, C.A.D., Serrão, J.E., and J.C. Zanuncio. 2015. Feeding and oviposition of Anticarsia gemmatalis (Lepidoptera: Noctuidae) with sublethal concentrations of ten condiments essential oils. Industrial Crops and Products. 74: 139–143.

Dewer, Y., Pottier, M.A., Lalouette, L., Maria, A., Dacher, M., Belzunces, L.P., Kairo, G., Renault, D., Maibeche, M., and Siaussat. 2016. Behavioral and metabolic effects of sublethal doses of two insecticides, chlorpyrifos and methomyl, in the Egyptian cotton leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Environmental Science & Pollution Research International. 23: 3086–3096.

Haddi, K., Oliveira, E.E., Faroni, L.R.A., Guedes, D.C., and N.N.S. Miranda. 2015. Sublethal exposure to clove and cinnamon essential oils induces hormetic‐like responses and disturbs behavioral and respiratory responses in Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Economic Entomology.108: 2815-2822

Ratna, Y., Trisyono, Y.A., Untung, K., dan D. Indradewa. 2009. Resurjensi Serangga Hama Karena Perubahan Fisiologi Tanaman dan Serangga Sasaran Setelah Aplikasi Insektisida. Jurnal Perlindungan Tanaman Indonesia 15 (2): 55 – 64.

Ratna, Y., Trisyono, Y.A., Witjaksono, dan D. Indradewa. 2010. Pengaruh Konsentrasi dan Frekuensi Aplikasi Deltametrin Terhadap Resurjensi Nilaparvata lugens. Jurnal Perlindungan Tanaman Indonesia 16 (1): 6–14.

Guedes, R.N.C., Smagghe, G., Stark, J.D., and N. Desneux. 2016. Pesticide‐induced stress in arthropod pests for optimized integrated pest management programs. Annual Review Entomology. 61: 43–62.

Cadogan, B.L., Retnakaran, A., and J.H. Meating. 1997. Efficacy of RH‐5992, a new insect growth regulator against spruce budworm (Lepidoptera: Torticidade) in a boreal forest. Journal Economic Entomology. 90: 551–559.

Seth, R.K., Kaur, J.J., Rao, D.K., and S.E. Reynolds. 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. Journal of Insect Physiology. 50: 505–517.

Elbert, A., Hass, M., Springer, B., Thielert, W., and R. Nauen. 2008. Applied aspects of neonicotinoid uses in crop protection. Pest Management Science. 64: 1099–1105.

Chaimanee, V., Evans. J.D., Chen, Y/, Jackson, C., and J.S. Pettis. 2016. Sperm viability and gene epression in honey bee ueens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. Journal Insect Physiology. 89: 1–8.

Brandt, A., Gorenflo, A., Siede, R., Meiner, M., and R. Buchler. 2016. The neonicotinoids thiacloprid, imidacloprid and clothianidin affect the immune-competence of honey bees (Apis mellifera L.). Journal Insect Physiology 86: 40–47.

Sattelle, D.B., Cordova, D., and T.R. Cheek. 2008. Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invertebrate Neuroscience. 8: 107–119.

Lahm, G.P., Cordova, D., and J.D. Barry. 2009. New and selective ryanodine receptor activators for insect control. Bioorganic and Medicinal Chemistry. 17: 4127–4133.

Xu, C., Zhang, Z., Cui, K., Zhao, Y., Han J., Liu F., and W. Mu. 2016. Effects of sublethal concentrations of cyantraniliprole on the development, fecundity and nutritional physiology of the black cutworm Agrotis ipsilon (Lepidoptera: Noctuidae). PLoS One. 11(6): e0156555.

Hui‐Ling, Y., Xin, X., Gui-in Y., Yi‐Qu C., and W. Xue‐Gui. 2015. Effects of sublethal doses of cyantraniliprole on the growth and development and the activities of detoxifying enzymes in Spodoptera exigua (Lepidoptera: Noctuidae). Acta Entomologica Sinica. 58: 634–641.

Saleem, M.A., and A.R. Shakoori. 1987. Point effects of Dimilin and Ambush on enzyme activies of Tribolium castaneum larvae. Pesticide Biochemistry and Physiology. 29: 127–137.

Shekari, M., Sendi, J.J., Etebari, K., Zibaee, A., and A. Shadparvar. 2008. Effects of Artemisia annua L. (Asteracea) on nutritional physiology and enzyme activities of elm leaf beetle, Xanthogaleruca luteola Mull (Coleoptera: Chrysomelidae). Pesticide Biochemistry and Physiology. 91: 66–74

Zamari, S., Sendi, J.J., and M. Ghadamyari. 2011. Effect of Artemisia annua L. (Asterales: Asteraceae) essential oil on mortality, development, reproduction and energy reserves of Plodia interpunctella (Hubner) (Lepidoptera: Pyralidae). Journal of Fertilizers and Pestcidies. 2: 105–110.

Correia, A.A., Wanderley‐Teixeira, V., Teixeira, A.A.C., Oliveira, J.V., Gonçalves, G.G., Cavalcanti, M.G., Brayner, F.A., and L.C. Alves. 2011. Microscopic analysis of Spodoptera frugiperda (Lepidoptera: Noctuidae) embryonic development before and after treatment with azadirachtin, lufenuron, and deltamethrin. Journal Economic Entomology. 106: 747–755.

Alves, T.J.S., Cruz, G.S., Teixeira, V.W., Teixeira, A.A.C., Oliveira, J.V., Correia, A.A., Câmara, A.A.G., and Cunha, F.M. 2013. Effects of Piper hispidinervum on spermatogenesis and histochemistry of ovarioles of Spodoptera frugiperda. Biotechnic and Histochemistry. 88: 1–11.

Cruz, G.S., Teixeira, V.W., Oliveira, J.V., Correia, A.A., Breda, M.O., Alves, T.J.S., Cunha, F.M., Teixeira, A.A.C., Dutra, K.A., and D.M.A.F. Navarro. 2014. Bioactivity of Piper hispidinervum (Piperales: Piperaceae) and Syzygium aromaticum (Myrtales: Myrtaceae) olis, with or without formulated Bta on the biology and immunology of Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Economic Entomology. 107: 144–153.

Silva, C.T.S., Wanderley‐Teixeira, V., Cunha, F.M., Oliveira, J.V., Dutra, K.A., Navarro, D.M.A.F., and A.A.C. Teixeira. 2016. Biochemical parameters of Spodoptera frugiperda (J. E. Smith, 1979) treated with citronella oil (Cymbopogon wintwrianus Jowitt ex Bor) and its influence on reproduction. Acta Histochemistry. 118: 347–352.

Kammenga, J.E., Busschers, M., Van Straalen, N.M., Jepson, J.P., and J. Bakker. 1996. Stress‐induced fitness reduction is not determined by the most sensitive lifecycle trait. Functional Ecology. 10: 106–111.

Kareiva, P., Stark, J., and U. Wennergren. 1996. Using demographic theory, community ecology and spatial models to illuminate ecotoxicology. In: Baird DJ, Maltby L, Greig‐Smith PW, Douben PET (eds.), Ecotoxicology: Ecological Dimensions. London: Chapman & Hall. pp. 13–23.

Bechmann, R.K. 1994. Use of life tables and LC50 tests to evaluate chronic and acute toxicity effects of copper on the marine copepod Tisbe furcata (Baird). Environmental Toxicology and Chemistry. 13: 1509–1517.

]50] Kerns, D.L., and M.J. Gaylor. 1992. Sublethal effects of insecticides on cotton aphid reproduction and color morph development. Southwestern Entomologist. 17: 245–250.

Kerns, D.L., and M.J. Gaylor. 1993. Induction of cotton aphid outbreaks by insecticides in cotton. Crop Protection. 12: 387–392.

Stark, J.D., and J.A.O. Banken. 1999. Importance of population structure at the time of toxicant exposure. Ecotoxicology and Environmental Safety. 42: 282–287.

Huang, Y.B., and H. Chi. 2013. Life tables of Bactrocera cucurbitae (Diptera: Tephritidae): with an invalidation of the jackknife technique. Journal of Applied Entomology. 137: 327–339.

Stark, J.D., and J.E. Banks. 2016. Developing demographic toxicity data: optimizing effort for predicting population outcomes. PeerJ. 4: e2067.

Han, W., Zhang, S., Shen, F., Liu, M., Ren, C., and X. Gao. 2012. Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (Lepidoptera: Plutellidae). Pest Management Science. 68: 1184–1190.

Song, Y., Dong, J., and H. Sun. 2013. Chlorantraniliprole at sublethal concentrations may reduce the population growth of the Asian corn borer, Ostrinia furnacalis (Lepidoptera: Pyralidae). Acta Entomologica Sinica. 56: 446–451.

Yin, X.H., Wu, Q.J., Li, X.F., Zhang, Y.J., and B.Y. Xu. 2009. Demographic changes in multigeneration Plutella xylostella (Lepidoptera: Plutellidae) after exposure to sublethal concentrations of spinosad. Journal of Economic Entomology. 102: 357–365.

Wang, D., Wang, Y.M., Liu, H.Y., Xin, Z., and M. Xue. 2013. Lethal and sublethal effects of spinosad on Spodoptera exigua (Lepidoptera: Noctuidae). Journal of Economic Entomology. 106: 1825–1831.

Breda, M.O., Oliveira, J.V., Marques, E.M., Ferreira, R.G., and M.F. Santana. 2011. Botanical insecticides applied on Aphis gossypii and its predator Cycloneda sanguinea on naturally colored cotton. Pesquisa Agropecuária Brasileira. 46: 1424–1431.

Andrade, L.H., Oliveira, J.V., Breda, M.O., Marques, E.J., and I.M.M. Lima. 2012. Effects of botanical insecticides on the instantaneous population growth rate of Aphis gossypii Glover (Hemiptera: Aphididae) in cotton. Acta Scientiarum Agronomy. 34: 119–124.

Venzon, M., Rosado, M.C., Pallini, A., Fialho, A., and C.J. Pereira. 2007. Lethal and sublethal toxicity of neem on green peach aphid and on its predator Eriopis conexa. Pesquisa Agropecuária Brasileira. 42: 627–631.

Wright, D.J., and R.H.J. Verkerk. 1995. Integration of chemical and biological control systems for arthropods: evaluation in a multitrophic context. Pesticide Science. 44: 207–218.

Ono, E.K. 2014. Lethal and sublethal effects of insect growth regulators over the predator Ceraeochrysa cubana (Hagen, 1861) (Neuroptera: Chrysopidae) under laboratory conditions. Dissertação de mestrado, Escola Superior de Agricultura “Luiz de Queiroz”, Piracicaba, SP, Brasil. 48 p.

Ohba, S.Y., Ohashi, K., Pujiyati, E., Higa, Y., Kawada, H., Mito, N., and M. Takagi. 2013. The effect of Pyiriproxyfen as a “population growth regulator” against Aedes albopictus under semifield conditions. PLoS One. 8: e67045.

Carvalho, G.A., Godoy, M.S., Parreira D.S., Lasmar, O., Souza, J.R., and V.F. Moscardini. 2010. Selectivity of growth regulators and neonicotinoids for adults of Trichogramma pretiosum (Hymenop-tera: Trichogrammatidae). Revista Colombiana de Entomología 36:195-201

Rill, S.M., Grafton‐Cardwell, E.E., and J.G. Morse. 2008. Effects of two insect growth regulators and a neonicotinoid on various life stages of Aphytis melinus (Hymenoptera: Aphelinidae). BioControl. 53: 579–587.

Garzón, A., Medina, P., Amor, F., Viñuela, E., and F. Budia. 2015. Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chisoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae).Chemosphere. 132:87-93

Fonseca, A.P.P., Marques, E.J., Torres, J.B., Silva, L.M., and H.A.A. Siqueira 2015. Lethal and sublethal effects of lufenuronon sugarcane borer Diatraea flavipennella and its parasitoid Cotesia flavipes. Ecotoxicology. 24: 1869–1879.

Trindade, R.C.P., Lima, I.S., Sant'Ana, A.E.G., Broglio, S.M.F., and P.P. Silva. 2013. Action of plants extract on Trichogramma galloi (Hymenoptera: Trichogrammatidae). Comunicata Scientiae. 4: 255–262.

Silva, A.B., Batista, J.L., and C.H. Brito. 2009. Influence of product of plant origin on oviposition and embryonic development of Euborellia annulipes (Dermaptera: Anisolabididae). Environmental Engineering. 6: 54–65.

Frazier, M., Mullin, C., Frazier, J., and S. Ashcraft. 2008. What have pesticides got to do with it? American Bee Journal, Hamilton. 521–523.

DOI: http://dx.doi.org/10.30598/ajibt.v10i1.1296


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