Abstract
Spinetoram, a spinosyn insecticide is used to manage lepidopteran pests, including diamondback moth, Plutella xylostella. In addition to determining the lethal effects, identifying low and/or sublethal effects of an insecticide is crucial to understanding the total impact of an insecticide. We assessed the low lethal and sublethal effects of spinetoram on two successive generations of P. xylostella. The initial bioassay results showed that spinetoram exhibited high toxicity against P. xylostella with an LC50 of 0.114 mg L−1 after 48 h exposure. The low lethal (LC25) and sublethal (LC10) concentrations of spinetoram showed significant reduction in pupation rate, pupal weight and adult emergence. The fecundity of F1 generation was significantly lower in LC25 (117.85 eggs/female) and LC10 (121.34 eggs/female) treated group than untreated control (145.32 eggs/female). The intrinsic rates of increase (r) was significantly lower (r = 0.1984 day−1) in spinetoram treated P. xylostella F1 progeny compared to untreated control (r = 0.2394 day−1). Our results suggest that LC10 and LC25 concentration of spinetoram might affect P. xylostella population growth by reducing its survival, development, and reproduction.
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References
APRD (2020). Arthropod pesticide resistance database. Michigan State University, http://www.pesticideresistance.org. Accessed 22 Apr 2020
Ayyanath MM, Cutler GC, Scott-Dupree CD, Sibley PK (2013) Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS ONE 8(9):e74532. https://doi.org/10.1371/journal.pone.0074532
Bacci L, Lupi D, Savoldelli S, Rossaro B (2016) A review of Spinosyns, a derivative of biological acting substances as a class of insecticides with a broad range of action against many insect pests. J Entomol Acarol Res 48(1):40–52
Campos MR, Rodrigues ARS, Silva WM, Silva TBM, Silva VRF, Guedes RNC, Siqueira HAA (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9(8):e103235
Chen X, Ma K, Li F, Liang P, Liu Y, Guo T, Song D, Desneux N, Gao X (2016) Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology 25(10):1841–1848
Chen XD, Seo M, Stelinski LL (2017) Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Protect 98:102–107
Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17(1):26–34
Chi H (2018) TWOSEX-MSChart: a computer program for the age stage, two-sex life table analysis. http://140.120.197.173/Ecology/Download/Twosex-MSChart-exe-B200000.rar
Chi H, Liu HSI (1985) Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sin 24(2):225–240
Chi H, Su H-Y (2006) Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol 35(1):10–21
Chi H, You M, Atlıhan R, Smith CL, Kavousi A, Özgökçe MS, Güncan A, Tuan SJ, Fu JW, Xu YY (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen 40(2):103–124
Deng D, Duan W, Wang H, Zhang K, Guo J, Yuan L, Wang L, Wu S (2019) Assessment of the effects of lethal and sublethal exposure to dinotefuran on the wheat aphid Rhopalosiphum padi (Linnaeus). Ecotoxicology 28(7):825–833
Depalo L, Masetti A, Avilla J, Bosch D, Pasqualini E (2016) Toxicity and residual activity of spinetoram to neonate larvae of Grapholita molesta (Busck) and Cydia pomonella (L.) (Lepidoptera: Tortricidae): semi-field and laboratory trials. Crop Protect 89:32–37
Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Dong J, Wang K, Li Y, Wang S (2017) Lethal and sublethal effects of cyantraniliprole on Helicoverpa assulta (Lepidoptera: Noctuidae). Pestic Biochem Physiol 136:58–63
Dripps J, Olson B, Sparks T, Crouse G (2008) Spinetoram: how artificial intelligence combined natural fermentation with synthetic chemistry to produce a new spinosyn insecticide. Plant Health Prog. https://www.plantmanagementnetwork.org/pub/php/perspective/2008/spinetoram/
Duan DH, Zhang XY, Yang QQ, Hu FJ, Su J, Deng SH, Zhuo JY (2012) Controlling effect of spinetoram against stored-grain insects. Grain Technol Econ 37(6):32–34
Enríquez CLR, Pineda S, Figueroa JI, Schneider MI, Martínez AM (2010) Toxicity and sublethal effects of methoxyfenozide on Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol 103(3):662–667
Finney DJ (1971) Probit analysis. 3rd ed. Cambridge Univ. Press, London
Fisher R (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Fu B, Li Q, Qiu H, Tang L, Zeng D, Liu K, Gao Y (2018) Resistance development, stability, cross‐resistance potential, biological fitness and biochemical mechanisms of spinetoram resistance in Thrips hawaiiensis (Thysanoptera: Thripidae). Pest Manage Sci 74(7):1564–1574
Gao Y, Kim K, Kwon DH, Jeong IH, Clark JM, Lee SH (2018) Transcriptome-based identification and characterization of genes commonly responding to five different insecticides in the diamondback moth, Plutella xylostella. Pestic Biochem Physiol 144:1–9
Gong Y, Xu B, Zhang Y, Gao X, Wu Q (2015) Demonstration of an adaptive response to preconditioning Frankliniella occidentalis (Pergande) to sublethal doses of spinosad: a hormetic-dose response. Ecotoxicology 24(5):1141–1151
Guedes RNC, Walse SS, Throne JE (2017) Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21:47–53
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 Protect 48:29–34
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 Manage Sci 68(8):1184–1190
Hedayati M, Sadeghi A, Maroufpoor M, Ghobari H, Güncan A (2019) Transgenerational sublethal effects of abamectin and pyridaben on demographic traits of Phytonemus pallidus (Banks) (Acari: Tarsonemidae). Ecotoxicology 28(4):467–477
Huang HW, Chi H, Smith CL (2017) Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. J Econ Entomol 111(1):1–9
Lai T, Su J (2011) Effects of chlorantraniliprole on development and reproduction of beet armyworm, Spodoptera exigua (Hübner). J Pest Sci 84(3):381–386
Liang PZ, Ma KS, Chen XW, Tang CY, Xia J, Chi H, Gao XW (2019) Toxicity and sublethal effects of flupyradifurone, a novel butenolide insecticide, on the development and fecundity of Aphis gossypii (Hemiptera: Aphididae). J Econ Entomol 112(2):852–858
Lira EC, Bolzan A, Nascimento ARB, Amaral FSA, Kanno RH, Kaiser IS, Omoto C (2020) Resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to spinetoram: inheritance and cross‐resistance to spinosad. Pest Manag Sci 76(8):2674–2680. https://doi.org/10.1002/ps.5812
Liu D, Jia ZQ, Peng YC, Sheng CW, Tang T, Xu L, Han ZJ, Zhao CQ (2018) Toxicity and sublethal effects of fluralaner on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Pestic Biochem Physiol 152:8–16
Mahmoudvand M, Abbasipour H, Garjan AS, Bandani AR (2011a) Sublethal effects of hexaflumuron on development and reproduction of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Insect Sci 18(6):689–896
Mahmoudvand M, Abbasipour H, Garjan AS, Bandani AR (2011b) Sublethal effects of indoxacarb on the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae). Appl Entomol Zool 46(1):75–80
Mahmoudvand M, Moharramipour S (2015) Sublethal effects of fenoxycarb on the Plutella xylostella (Lepidoptera: Plutellidae). J Insect Sci 15(1):82
Navik O, Ramya RS, Varshney R, Jalali SK, Shivalingaswamy TM, Rangeshwaran R, Lalitha Y, Patil J, Ballal CR (2019) Integrating biocontrol agents with farmer’s practice: impact on diamondback moth, Plutella xylostella (Linnaeus) (Lepidoptera: Plutellidae) and cabbage yield. Egypt J Biol Pest Co 29(1):35
Neto JEL, Amaral MHP, Siqueira HAA, Barros R, Silva PAF (2016) Resistance monitoring of Plutella xylostella (L.) (Lepidoptera: Plutellidae) to risk-reduced insecticides and cross resistance to spinetoram. Phytoparasitica 44(5):631–640
Planes L, Catalán J, Tena A, Porcuna JL, Jacas JA, Izquierdo J, Urbaneja A (2013) Lethal and sublethal effects of spirotetramat on the mealybug destroyer, Cryptolaemus montrouzieri. J Pest Sci 86(2):321–327
Qiu S, Lu Z (2011) Field effect trials on the spinetoram against Noctuidae pests on Brassica oleracea. Shanghai Veg 3:52
Qu Y, Xiao D, Li J, Chen Z, Biondi A, Desneux N, Gao X, Song D (2015) Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24(3):479
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(5):513–520
Ribeiro LMS, Wanderley-Teixeira V, Ferreira HN, Teixeira ÁAC, Siqueira HAA (2014) Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bull Entomol Res 104(1):88–96
Rumbos CI, Dutton AC, Athanassiou CG (2018) Insecticidal effect of spinetoram and thiamethoxam applied alone or in combination for the control of major stored-product beetle species. J Stored Prod Res 75:56–63
Salgado VL (1998) Studies on the mode of action of spinosad: Insect symptoms and physiological correlates. Pestic Biochem Physiol 60(2):91–102
Sial AA, Brunner JF (2010) Toxicity and residual efficacy of chlorantraniliprole, spinetoram, and emamectin benzoate to obliquebanded leafroller (Lepidoptera: Tortricidae). J Econ Entomol 103(4):1277–1285
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(3):274–279
Singh JP, Marwaha KK (2000) Effect of sublethal concentrations of some insecticides on growth and development of maize stalk borer, Chilo partellus (Swinhoe) larvae. Shashpa 7(2):181–186
Sohrabi F, Shishehbor P, Saber M, Mosaddegh MS (2011) Lethal and sublethal effects of buprofezin and imidacloprid on Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Protect 30(9):1190–1195
Song Y, Dong J, Sun H (2013) Chlorantraniliprole at sublethal concentrations may reduce the population growth of the Asian corn borer, Ostrinia furnacalis (Lepidoptera: Pyralidae). Acta Entomol Sin 56(4):446–451
Su C, Xia X (2020) Sublethal effects of methylthio-diafenthiuron on the life table parameters and enzymatic properties of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Pestic Biochem Physiol 162:43
Sun J, Liang P, Gao X (2010) Inheritance of resistance to a new non‐steroidal ecdysone agonist, fufenozide, in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Pest Manage Sci 66(4):406–411
Tamilselvan R, Kennedy JS, Suganthi A (2020) Monitoring the resistance and baseline susceptibility of Plutella xylostella (L.) (Lepidoptera: Plutellidae) against spinetoram in Tamil Nadu. India. Crop Protect 142:105491. https://doi.org/10.1016/j.cropro.2020.105491
Troczka B, Zimmer CT, Elias J, Schorn C, Bass C, Davies TGE, Field LM, Williamson MS, Slater R, Nauen R (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol Biol 42(11):873–880
Ullah F, Gul H, Desneux N, Gao X, Song D (2019a) Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, Aphis gossypii. Entomol Gen 39(3-4):325–337
Ullah F, Gul H, Desneux N, Qu Y, Xiao X, Khattak AM, Gao X, Song D (2019b) Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, Aphis gossypii. Entomol Gen 39(3-4):259–270
Vassilakos TN, Athanassiou CG, Saglam O, Chloridis AS, Dripps JE (2012) Insecticidal effect of spinetoram against six major stored grain insect species. J Stored Prod Res 51(2):69–73
Vassilakos TN, Athanassiou CG, Tsiropoulos NG (2015) Influence of grain type on the efficacy of spinetoram for the control of Rhyzopertha dominica, Sitophilus granarius and Sitophilus oryzae. J Stored Prod Res 64:1–7
Wang D, Gong P, Li M, Qiu X, Wang K (2009) Sublethal effects of spinosad on survival, growth and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae). Pest Manage Sci 65(2):223–227
Wang L, Zhang Y, Xie W, Wu Q, Wang S (2016) Sublethal effects of spinetoram on the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Pestic Biochem Physiol 132:102–107. https://doi.org/10.1016/j.pestbp.2016.02.002
Watson GB, Chouinard SW, Cook KR, Geng C, Gifford JM, Gustafson GD, Hasler JM, Larrinua IM, Letherer TJ, Mitchell JC (2010) A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression. Insect Biochem Mol Biol 40(5):376–384
Wei J, Zhang L, Yang S, Xie B, An S, Liang G (2018) Assessment of the lethal and sublethal effects by spinetoram on cotton bollworm. PLoS ONE 13(9):e0204154. https://doi.org/10.1371/journal.pone.0204154
Whalon ME, Mota-Sanchez D, Hollingworth RM (2008) Analysis of global pesticide resistance in arthropods. In: Whalon ME (Ed.) Global pesticide resistance in arthropods. CABI, Wallingford
Xia H, Chen M, Liu W, Wang J (2013) Field effect trials on the mixture of sulfoxaflor and spinetoram against rice migratory pests. Mod Agrochem 12(3):52–53
Xiao D, Yang T, Desneux N, Han P, Gao X (2015) Assessment of sublethal and transgenerational effects of pirimicarb on the wheat aphids Rhopalosiphum padi and Sitobion avenae. PLoS ONE 10(6):e0128936. https://doi.org/10.1371/journal.pone.0128936
Xu C, Zhang Z, Cui K, Zhao Y, Han J, Liu F, Mu W (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. https://doi.org/10.1371/journal.pone.0156555
Yin XH, Wu QJ, Li XF, Zhang YJ, Xu BY (2008) Sublethal effects of spinosad on Plutella xylostella (Lepidoptera: Yponomeutidae). Crop Protect 27(10):1385–1391
Zhang RM, Dong JF, Chen JH, Ji QE, Cui JJ (2013) The sublethal effects of chlorantraniliprole on Helicoverpa armigera (Lepidoptera: Noctuidae). J Integr Agric 12(3):457–466
Zhang Y, Guo L, Atlihan R, Chi H, Chu D (2019) Demographic analysis of progeny fitness and timing of resurgence of Laodelphax striatellus after insecticides exposure. Entomol Gen 39(3-4):221–230
Zhang Z, Li JH, Gao XW (2012) Sublethal effects of metaflumizone on Plutella xylostella (Lepidoptera: Plutellidae). J Integr Agric 11(7):1145–1150
Zhu Q, He Y, Yao J, Liu Y, Tao L, Huang Q (2012) Effects of sublethal concentrations of the chitin synthesis inhibitor, hexaflumuron, on the development and hemolymph physiology of the cutworm, Spodoptera litura. J Insect Sci 12(1):27
Acknowledgements
We are grateful to the National Bureau of Agricultural Insect Resources (NBAIR), Bengaluru for providing DBM mother culture. This research was sponsored by the Government of India, National Institute of Plant Health Management (NIPHM), Hyderabad. We are grateful to Dr. Hsin Chi, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China, for their statistical assistance with the two-sex life table theory used in this work.
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JSK received funding. JSK, RT and AS designed the experiment. RT and AS performed the experiments and analyzed the data. RT and JSK wrote and reviewed the manuscript. All authors read and approved the manuscript.
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This work was supported by the Government of India, National Institute of Plant Health Management, Hyderabad under grant NIPHM/CPPS/CBE/AEN/2016/R010.
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Tamilselvan, R., Kennedy, J.S. & Suganthi, A. Sublethal and transgenerational effects of spinetoram on the biological traits of Plutella xylostella (L.) (Lepidoptera: Plutellidae). Ecotoxicology 30, 667–677 (2021). https://doi.org/10.1007/s10646-021-02385-7
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DOI: https://doi.org/10.1007/s10646-021-02385-7