Comparative toxicity of spinetoram to Trialeurodes vaporariorum Westwood and its parasitoid Encarsia formosa Gahan
Abstract
The role of selective new generation bionsecticides, beside their effectiveness against key pests, relies on their safety to beneficial arthropods. Spinetoram, a semi-synthetic analogue of the microbial-derived bioinsecticide spinosad is registered worldwide for application to numerous crops, but its ecotoxicological risk assessment to beneficial arthropods has hardly been documented. Moreover, this is the first report regarding the toxic effects of spinetoram on a pest- the greenhouse whitefly Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), and/or its successful biocontrol agent, parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae). In laboratory conditions we assessed the acute toxicity of spinetoram insecticide (25% a.i.) to adults, nymphs and eggs of the greenhouse whitefly, as well as to adult and pupal stage of the parasitoid. In all concentration-response bioassays, the spinetoram insecticide was applied to tobacco leaves settled onto 1% agar layer in ventilated Petri dishes using a Potter spray tower. The acute toxicity parameters of spinetoram on adults of both pest and parasitoid were evaluated in residual contact bioassays, while whitefly eggs and nymphs, and pupae of the parasitoid were topically treated with a series of spinetoram concentrations, covering a range of 10-90% mortality. The lethal effects of spinetoram on parasitoid E. formosa was assessed through Selectivity ratio (SR) estimations, showing the ratios beetween median Lethal Concentrations (LC50s) estimated for the parasitoid, compared to LC50s estimated for the pest. The following LC50 values were evaluated: 4.593, 15.027 and 11.73 mg a.i./l for whitefly adults, nymphs and eggs, respectively, and 0.686 and 1.715 mg a.i./l for parasitoid adults and pupae, respectively. The calculated SR estimations were less than 1, indicating that spinetoram insecticide is non-selective towards the both tested stages of the parasitoid E. formosa. A more complete understanding of spinetoram impact on E. formosa within whitefly integrated management requires further evaluation of the sublethal effects and greenhouse trials, with an emphasis on population-level responses.
References
Abbes, K., Biondi, A., Kurtulus, A., Ricupero, M., Russo, A., Siscaro, G. ... Zappala, L. (2015). Combined nontarget effects of insecticide and high temperature on the parasitoid Bracon nigricans. PloS ONE, 10(9), e0138411. doi:10.1371/journal.pone.0138411
Abd-Ella, A.A. (2015). Susceptibility of the pomegranate whitefly, Siphoninus phillyreae (Haliday)(Homoptera: Aleyrodidae) and its parasitoid, Encarsia inaron (Walker) (Hymenoptera: Aphelinidae) to certain insecticides under laboratory conditions. Egyptian Journal of Biological Pest Control, 25(3), 689-695.
Albajes, R., Lodovica Gullino, M., van Lenteren, J. C., & Elad, Y. (Eds.). (1999). Integrated pest and disease management in greenhouse crops. Dordrecht, Netherlands: Kluwer Academic Publisher.
Bacci, L., Crespo, A.L., Galvan, T.L., Pereira, E.J., Picanco, M.C., Silva, G.A., & Chediak, M. (2007). Toxicity of insecticides to the sweetpotato whitefly (Hemiptera: Aleyrodidae) and its natural enemies. Pest Management Science, 63(7), 699-706. doi.org/10.1002/ps.1393
Biondi, A., Mommaerts, V., Smagghe, G., Vinuela, E., Zappala, L., & Desneux, N. (2012). The non-target impact of spinosyns on beneficial arthropods. Pest Management Science, 68(12), 1523-1536. doi: 10.1002/ps.3396. doi: 10.1002/ps.3396
Biondi, A., Zappala, L., Stark, J.D., & Desneux, N. (2013). Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One, 8(9), e76548. doi: 10.1371/journal.pone.0076548
Chandler, D., Bailey, A. S., Tatchell, G. M., Davidson, G., Greaves, J., & Grant, W. P. (2011). The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 1987-1998. doi:10.1098/rstb.2010.0390
Chloridis, A., Downard, P., Dripps, J.E., Kaneshi, K., Lee, L.C., Min, Y.K., & Pavan, L.A. (2007). Spinetoram (XDE-175): a new spinosyn. In The BCPC congress, Proceedings of the XVI International Plant Protection Congress (pp 44-49). Glasgow, UK: British Crop Production Council.
Copping, L.G., & Menn, J.J. (2000). Biopesticides: a review of their action, applications and efficacy. Pest Management Science, 56(8), 651-676. doi:10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81-106. doi.org/10.1146/annurev.ento.52.110405.091440
Dripps, J.E., Boucher R.E., Chloridis A., Cleveland C.B., DeAmicis C.V., Gomez L.E. … Watson, G.B. (2011). The spinosyn insecticides. In O. L´opez & J. G. Fernandez-Bolanos (Eds), Green trends in insect control, Green chemistry series, Vol. 11 (pp 163-212). London, UK: Royal Society of Chemistry.
Drobnjaković, T., & Marčić, D. (2021). Effects of spirotetramat insecticide on life history traits and population growth of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 31(6), 604-618. doi: 10.1080/09583157.2021.1873248
Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., & Bošković, J. (2018). Sublethal effects of NeemAzal-T/S botanical insecticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 28(1), 1-19. doi:10.1080/09583157.2017.1409336
Drobnjaković, T., Prijović, M., Milenković, S. & Marčić, D. (2019). Sublethal effects of Beauveria bassiana-based mycopesticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 29(10), 991-1008. doi:10.1080/09583157.2019.16352
EPPO (2004). Side-effects on Encarsia formosa, PP1/142(2). Efficacy evaluation of plant protection products. Paris, France: Europian and Mediterranean Plant Protection Organisation.
Finney, D. J. (1971). Probit analysis. Cambridge, UK: University Press.
Gerling, D., Alomar, O., & Arno, J. (2001). Biological control of Bemisia tabaci using predators and parasitoids. Crop Protection, 20(9), 779–799. doi:10.1016/S0261-2194(01)00111-9
Giunti, G., Benelli, G., Palmeri, V., Laudani, F., Ricupero, M., Ricciardi, R., ... Campolo, O. (2022). Non-target effects of essential oil-based biopesticides for crop protection: impact on natural enemies, pollinators, and soil invertebrates. Biological Control, 176, 105071. doi:10.1016/j.biocontrol.2022.105071
Hassan, S.A., Hafes, B., Degrande, P.E., & Herai, K. (1998). The side-effects of pesticides on the egg parasitoid Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae), acute dose-response and persistence tests. Journal of Applied Entomology, 122(1-5), 569-573. doi.org/10.1111/j.1439-0418.1998.tb01547.x
Hernandez, R, Guo, K., Harris, M., & Liu, T.X. (2011). Effects of selected insecticides on adults of two parasitoid species of Liriomyza trifolii: Ganaspidium nigrimanus (Figitidae) and Neochrysocharis formosa (Eulophidae). Insect Science, 18(5), 512–520. doi.org/10.1111/j.1744-7917.2010.01391.x
Hoddle, M.S., van Driesche, R.G., Lyon, S.M., & Sanderson, J.P. (2001). Compatibility of insect growth regulators with Eretmocerus eremicus for whitefly control on poinsettias: I. Laboratory assays. Biological Control, 20(2), 122-131. doi:10.1006/bcon.2000.0885
Hoddle, M.S., van Driesche, R.G., & Sanderson, J.P. (1998). Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43, 645-649. doi:10.1146/annurev.ento.43.1.645
IRAC (2023). The IRAC mode of action classification online. Retrieved from: https://irac-online.org/modes-of-action/
Kapantaidaki, D. E., Sadikoglou, E., Tsakireli, D., Kampanis, V., Stavrakaki, M., Schorn, C. … Tsagkarakou, A. (2018). Insecticide resistance in Trialeurodes vaporariorum populations and novel diagnostics for kdr mutations. Pest Management Science, 74(1), 59-69. doi: 10.1002/ps.4674
Kumar, J., Ramlal, A., Mallick, D., & Mishra V. (2021). An overview of some biopesticides and their importance in plant protection for commercial acceptance. Plants, 10(6), 1185. doi: 10.3390/plants10061185
Lefebvre, M., Bostanian, N.J., Thistlewood, H.M., Mauffette, Y., & Racette, G. (2011). A laboratory assessment of the toxic attributes of six ‘reduced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). Chemosphere, 84(1), 25-30. doi.org/10.1016/j.chemosphere.2011.02.090
Li, S.J., Xue, X., Ahmed, M.Z., Ren, S.X., Du, Y.Z., Wu, J.H. … Qiu, B. L. (2011). Host plants and natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in China. Insect Science, 18(1), 101-120. doi.org/10.1111/j.1744-7917.2010.01395.x
Mota-Sanchez, D. & Wise, J.C. (2023). Arthropod pesticide resistance database. Retrieved from https://www.pesticideresistance.org/
Parsaeyan, E., Saber, M., Safavi, S.A., Poorjavad, N., & Biondi, A. (2020). Side effects of chlorantraniliprole, phosalone and spinosad on the egg parasitoid, Trichogramma brassicae. Ecotoxicology, 29, 1052-1061. doi: 10.1007/s10646-020-02235-y
Patra, B., & Kumar Hath, T. (2022). Insecticide resistance in whiteflies Bemisia tabaci (Gennadius): Current global status. Insecticides. In Ramon Eduardo Rebolledo Ranz (Ed), Insecticides – Impact and benefits of its use for humanity (chapter 19). Temuco, Chile: Universidad de La Frontera. doi: 10.5772/intechopen.101954
Peterson, R.K.D. (2006). Comparing ecological risks of pesticides: the utility of a risk quotient ranking approach across refinements of exposure. Pest Management Science, 62, 46-56. doi: 10.1002/ps.1126
Preetha, G., Stanley, J., Suresh, S., & Samiyappan, R. (2010). Risk assessment of insecticides used in rice on mired bug, Cyrtorhinus lividipennis Reuter, the important predator of brown planthopper, Nilaparvata lugens (Stal). Chemosphere, 80(5), 498-503. doi:10.1016/j.chemosphere.2010.04.070
Ricupero, M., Abbes, K., Haddi, K., Kurtulus, A., Desneux, N., Russo, A. … Zappala, L. (2020). Combined thermal and insecticidal stresses on the generalist predator Macrolophus pygmaeus. Science of the Total Environment, 729, 138922. doi: 10.1016/j.scitotenv.2020.138922
Robertson, J.L., Russell, R.M., Preisler, H.K., & Savin, N.E. (Eds). (2007). Bioassays with arthropods (2nd ed). Boca Raton, FL, USA: CRC Press.
Robertson, J.L., & Worner, S.P. (1990). Population toxicology: suggestion for laboratory bioassays to predict pesticide efficacy. Journal of Economic Entomology, 83(1), 8-12. doi.org/10.1093/jee/83.1.8
Şengonca, C., & Liu, B. (2001). Infuence of mixed biocide GCSC-BtA on the pupae and adult stages of Apanteles plutellae Kurd. (Hym., Braconidae) and its host. Plutella xylostella (L.) (Lep., Plutellidae). Journal of Pesticide Science, 74(6), 145-149. doi.org/10.1046/j.1439-0280.2001.01033.x
Shankarganesh, K., Ricupero, M., & Sabtharishi S. (2022). Field evolved insecticide resistance in the cotton mealybug Phenacoccus solenopsis and its direct and indirect impacts on the endoparasitoid Aenasius arizonensis. Scientific Reports 12, 16764. doi: 10.1038/s41598-022-20779-3
Shimokawatoko Y., Sato, N., Yamaguchi, T., & Tanaka, H. (2012). Development of the novel insecticide spinetoram (DIANAR). Retrieved from https://www.sumitomochem.co.jp/english/rd/report/files/docs/01_2012e.pdf
Srivastava, M., Bosco, L., Funderburk, J., & Olson, S., & Weiss, A. (2008). Spinetoram is compatible with the key natural enemy of Frankliniella species thrips in pepper. Plant Health Progress, 9(1), 30. doi:10.1094/PHP-2008- 0118-02-RS
Stark, J.D., & Banken, J.A.O. (1999). Importance of population structure at the time of toxicant exposure. Ecotoxicology and Environmental Safety, 42(3), 282-287.
Stark, J.D., Tanigoshi, L., Bounfour, M., & Antonelli, A. (1997). Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicology and Environmental Safety, 37(3), 273-279. doi.org/10.1006/eesa.1997.1552
Sugiyama, K., Katayama, H., & Saito, T. (2011). Effect of insecticides on the mortalities of three whitefly parasitoid species, Eretmocerus mundus, Eretmocerus eremicus and Encarsia formosa (Hymenoptera: Aphelinidae). Applied Entomology and Zoology, 46(3), 311–317. doi.org/10.1007/s13355-011-0044-z
van Lenteren, J.C., & Martin, G. (1999). Biological control of whiteflies. In R. Albajes, M. Lodovica Gullino, J.C. van Lenteren, & Y. Elad (Eds.), Integrated pest and disease management in greenhouse crops (pp 202-215). Dordrecht, Netherlands: Kluwer.
Villaverde, J. J., Sevilla-Moran, B., Sandin-Espana, P., Lopez-Goti, C., & Alonso-Prados, J. L. (2014). Biopesticides in the framework of the European pesticide regulation (EC) no. 1107/2009. Pest Management Science, 70, 2-5. doi:10.1002/ps.3663
Williams, T., Valle, J., & Viňuela, E. (2003). Is the naturally derived insecticide SpinosadR compatible with insect natural enemies? Biocontrol Science and Technology, 13(5), 459-475. doi.org/10.1080/0958315031000140956
Ministry of Science, Technological Development and Innovation of the Republic of Serbia, Grant No. 451-03-47/2023-01/200214
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