Abstract
We evaluated the chemical composition of thirteen commercially available plant essential oils and their insecticidal activity against the beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Gas chromatography-mass spectrometry was used to characterize the chemical components of the essential oils. A total of 113 compounds were identified, with terpenes (>80%) and aromatic compounds as primary constituents. The toxicity of each pure essential oil was tested separately on third instar larvae and adult beet armyworms by topical application of 0.5 μl oil/ insect. All plant essential oils were found to be harmful to S. exigua, with third instar larvae showing significantly more susceptibility than adults. Essential oils of Cinnamomum zeylanicum and Juniperus virginiana showed the highest toxicity (mortality above 90%) to larvae, while C. zeylanicum and Pogostemon cablin oils were the most harmful compounds (95% mortality) to adults. Cymbopogon winterianus oil caused delayed mortality (similar to the effects of insect growth regulators) as well as malformations in pupae. C. winterianus, Ocimum basilicum and Rosmarinus officinalis oils significantly reduced fecundity, whereas no significant effects were observed on fertility.
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References
Ahmad, M., & Arif, M. I. (2010). Resistance of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) to endosulfan, organophosphorus and pyrethroid insecticides in Pakistan. Crop Prot, 29, 1428–1433.
Alburquerque, B. D., Lima, J. K., Souza, F. H., Silva, I. M., Santos, A. A., Araújo, A. P., Blank, A. F., Lima, R. N., Alves, P. B., & Bacci, L. (2013). Insecticidal and repellence activity of the essential oil of Pogostemon cablin against urban ants species. Acta Trop, 127(3), 181–186.
Alves, T. J. S., Cruz, G. S., Wanderley-Teixeira, V., Teixeira, A. A. C., Oliveira, J. V., Correia, A. A., & Cunha, F. M. (2014). Effects of Piper hispidinervum on spermatogenesis and histochemistry of ovarioles of Spodoptera frugiperda. Biotech Histochem, 89(4), 245–255.
Athanassiou, C.G., Kavallieratos, N.G., Evergetis, E., Katsoula, A., & Haroutounian, S.A., (2012). Insecticidal efficacy of silica gel with Juniperus oxycedrus ssp. Oxycedrus Pinales: Cupressaceae) essential oil against Sitophilus oryzae (Coleoptera: Curculionidae) and Tribolium confusum (Coleoptera: Tenebrionidae). J Econ Entomol, 106(4), 1902–1910.
Athanassiou, C. G., Rani, P. U., & Kavallieratos, N. G. (2014). The use of plant extracts for stored product protection. In D. Singh (Ed.), Advances in plant biopesticides (pp. 347–359). India: Springer.
Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2007). Biological effects of essential oils-A review. Food Chem Toxicol, 46, 446–475.
Baskaran, J., Arshid, G., Elumalai, K., & Krishnappa, K. (2012). Selected plants essential oils against ovicidal activity of armyworm, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Int J Adv Res, 1(1), 18–21.
Bengochea, P., Budia, F., Viñuela, E., & Medina, P. (2014). Are kaolin and copper treatments safe to the olive fruit fly Psyttalia concolor? Journal of Pest Science, 87(2), 351–359.
Caballero, P., Murillo, R., Muñoz, D., & Williams, T. (2009). El nucleopoliedrovirus de Spodoptera exigua (Lepidoptera: Noctuidae) como bioplaguicida: análisis de avances recientes en España. Revista Colombiana Entomología, 35(2), 105–115.
Che, W., Shi, T., Wu, Y., & Yang, Y. (2012). Insecticide resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) from China. J Econ Entomol, 106(4), 1855–1862.
Cheng, S. S., Liu, J. Y., Huang, C. G., Hsui Chen, W. J., & Chang, S. T. (2009). Insecticidal activities of leaf essential oil from Cinnamomum osmophloeum against three mosquito species. Bioresour Technol, 100, 457–464.
Cruz, G.S., Teixeira, V.W., De Oliveira, J.V., Teixeira, A.A.C., Araújo, A.C., Alves, T.J.S., Da Cunha, F.M, & Breda, M.O., (2015). Histological and histochemical changes by clove essential oil upon the gonads of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Int J Morphol, 33 (4), 1393–1400.
Dimetry, N. Z. (2014). Different plant families as bioresource for pesticides. In D. Singh (Ed.), Advances in plant biopesticides (pp. 1–17). India: Springer.
Enan, E. (2001). Insectidal activity of esential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology, Part C, 130, 325–337.
Escobar-Valencia, C., Hernández-Carlos, B., Zayas-Pérez, M.T., Aragón-García, A., Pérez-González, L.E., Hernández-Molina, R., & López-Olguín, J.F., (2007). Actividad antialimentaria de extractos vegetales en el "gusano soldado" Spodoptera exigua (Lepidoptera: Noctuidae). Agricultura Sostenible Vol. 1: Alternativas contra plagas (pp.11–18).
Garzón, A., Medina, P., Amor, F., Viñuela, E., & Budia, F. (2015). Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coocinellidae). Chemosphere, 132, 87–93.
Gillij, Y. G., Gleiser, R. M., & Zygadlo, J. A. (2008). Mosquito repellent activity of essential oils of aromatic plants growing in Argentina. Bioresour Technol, 99, 2507–2515.
Gusmão, N. M. S., Oliveira, J. V., Navarro, D. M., Dutra, K. A., da Silva, W. A., & Wanderley, M. J. A. (2013). Contact and fumigant toxicity and repellency of Eucalyptus citriodora Hook., Eucalyptus staigeriana F., Cymbopogon winterianus Jowitt and Foeniculum vulgare Mill. Essential oils in the management of Callosobruchus maculatus (Fabr.) (Coleoptera: Chrysomelidae, Bruchinae). J Stored Prod Res, 54, 41–47.
Hummelbrunner, L. A., & Isman, M. B. (2001). Acute, sublethal, antifeedant and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura (Lep. Noctuidae). J Agric Food Chem, 49, 715–720.
Islam, R., Khan, R. I., Al-Raeza, S. M., Jeong, Y. T., Song, C. H., & Khalequzzman, M. (2009). Chemical composition and insecticidal properties of Cinnamomum aromaticum (Nees) essential oil against the stored product beetle Callosobruchus maculatus (F.) J Sci Food Agric, 89, 1241–1246.
Isman, M. B. (2006). Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol, 51, 45–66.
Isman, M. B. (2009). Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev, 10(2), 197–204.
Isman, M. B., & Grieneisen, M. L. (2013). Botanical insecticide research: many publications, limited useful data. Trends Plant Sci, 19(3), 140–145.
Isman, M. B., & Machial, C. M. (2006). Pesticides based on plant essential oils: from traditional practice to commercialization. Advances in Phytomedicine, 3, 29–44.
Isman, M. B., & Tak, J. (2017). Inhibition of acetylcholinesterase by essential oils and monoterpenoids: A Relevant mode of action for insecticidal essential oils? Biopesticides International, 13(2), 71–78.
Isman, M. B., Wan, A. J., & Passreiter, C. M. (2001). Insecticidal activity of essential oils to the tobacco cutworm, Spodoptera litura. Fitoterapia, 72, 65–68.
Karr, L. L., & Coats, J. R. (1988). Insecticidal properties of d- limonene. J Pestic Sci, 13, 2287–2290.
Kostyukovsky, M., Rafaeli, A., Gileadi, C., Demchenko, N., & Shaaya, E. (2002). Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci, 58, 1101–1106.
Koul, O., Walia, S., & Dhaliwal, G. S. (2008). Essential oils as green pesticides: Potential and constraints. Biopesticides International, 4(1), 63–84.
Kumar, P., Mishra, S., Malik, A., & Satya, S. (2011). Insecticidal properties of Mentha species: A review. Ind Crop Prod, 34, 802–817.
Lai, T., Li, J., & Su, J. (2011). Monitoring of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) resistance to chlorantraniliprole in China. Pestic Biochem Physiol, 101(3), 198–205.
Lasa, R., Ruiz-Portero, C., Alcázar, M. D., Belda, J. E., Caballero, P., & Williams, T. (2007). Efficacy of optical brightener formulations of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) as a biological insecticide in greenhouses in southern Spain. Biol Control, 40, 89–96.
López, M. D., & Pascual-Villalobos, M. J. (2010). Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crop Prod, 31, 284–288.
Machial, C. M., Shikano, I., Smirle, M., Bradbury, R., & Isman, M. B. (2010). Evaluation of the toxicity of 17 essential oils against Choristoneura rosaceana (Lepidoptera:Tortricidae) and Trichoplusia ni (Lepidoptera: Noctuidae). Pest Manag Sci, 66, 1116–1121.
MAPAMA, Ministry of Agriculture, Food and Environment. (2017). Annual Survey Directory http://www.mapama.gob.es/es/estadistica/temas/publicaciones/anuario-de-estadistica/ Accessed 27.04.2017.
MAPAMA, Ministry of Agriculture, Food and Environment. (2018). European community list of active substance included, excluded and under evaluation. http://www.mapama.gob.es/agricultura/pags/fitos/registro/fichas/pdf/Lista_Sustancias_activas_aceptadas_excluidas.pdf Accessed 21.03.2018.
Medina, P., Budia, F., Estal, P., & Viñuela, E. (2004). Influence of azadirachtin, a botanical insecticide, on Chrysoperla carnea (Stephens) reproduction: toxicity and ultrastructural approach. J Econ Entomol, 97(1), 43–50.
Mills, C., Cleary, B. J., Gilmer, J. F., & Walsh, J. J. (2004). Inhibition of acetylcholinesterase by Tea Tree oil. J Pharm Pharmacol, 56, 375–379.
Miresmailli, S., Bradbury, R., & Isman, M. B. (2006). Comparative toxicity of Rosmarinus officinalis L. essential oil and blends of its major constituents against Tetranychus urticae Koch (Acari: Tetranychidae) on two different host plants. Pest Manag Sci, 62, 366–371.
Mondal, M., & Khalequzzaman, M. (2009). Ovicidal activity of essential oils against Red Flour Beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Journal of Bio –Science, 17, 57–62.
Moulton, J. K., Pepper, D. A., & Dennehy, T. J. (2000). Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Manag Sci, 56(1), 842–848.
Ngoh, P. H., Lionel, E. W. C., Fung, P. Y., Kini, M. R., & Ho, S. H. (1998). Insecticidal and repellent properties of nine volatile constituents of essential oils against the American cockroach, Periplaneta americana (L.) Pest Manag Sci, 54, 261–268.
Niculau, E. S., Alves, P. B., Nogeuira, P. C., Moraes, V. R., Matos, A. P., Bernardo, A. R., Volante, A. C., Fernandes, J. B., da Silva, M. F. G. F., Corrêa, A. G., Blank, A. F., Silva, A. C., & Ribeiro, L. P. (2013). Insecticidal activity of essential oils of Pelargonium graveolens l’Herit and Lippia alba (Mill.) N.E. Brown against Spodoptera frugiperda (J.E.Smith). Quim Nova, 36(9), 1391–1394.
Papachristos, D. P., Kimbaris, A. C., Papadopoulos, N. T., & Polissiou, M. G. (2009). Toxicity of citrus essential oils against Ceratitis capitata (Diptera: Tephritidae) larvae. Ann Appl Biol, 155, 381–389.
Pavela, R. (2005). Insecticidal activity of some essential oils against larvae of Spodoptera littoralis. Fitoterapia, 76, 691–696.
Pavela, R. (2014). Limitations of plants biopesticides. In D. Singh (Ed.), Advances in plant biopesticides (pp. 347–359). India: Springer.
Pichersky, E., Noel, J. P., & Dudareva, N. (2006). Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science, 311, 808–811.
Poitout, S., & Bues, R. (1974). Élevage des chenilles de vinghuit espéces de lépidoptères Noctuidae et de deux espéces d'Arctiidae sur milieu artificiei simple. Particularités de l'élevage selon les espéces Annales de Ecologie Animale, 6, 431–441.
Rossi, Y. E., & Palacios, S. M. (2015). Insecticidal toxicity of Eucalyptus cinerea essential oil and 1,8-cineole against Musca domestica and possible uses according to the metabolic responses of files. Ind Crop Prod, 63, 133–137.
Sabine, J. R. (1975). Exposure to an environment containing the aromatic red cedar, Juniperus virginiana: Procarcinogenic, enzyme-inducing and insecticidal effects. Toxicology, 5, 221–235.
Sharma, R. N., & Saxena, K. N. (1974). Orientation and developmental inhibition in the housefly by certain terpenoids. J Med Entomol, 11, 617–621.
StatPoint Technologies (2013). Statgraphic Centurion XVI (v. 16.2.04) software version 16.2. 04. Virginia: StatPoint Technologies Inc.
Tak, J., & Isman, M. B. (2015). Enhanced cuticular penetration as the mechanism for synergy of insecticidal constituents of rosemary essential oil in Trichoplusia ni. Sci Rep, 5, 12690.
Van der Blom, J., Robledo, A., Torres, S., Sánchez, J. A., & Contreras, M. (2008). Control biológico de plagas en Almería: Revolución verde después de dos décadas. Phytoma, 198, 42–48.
Zhou, C., Liu, Y., Yu, W., Deng, Z., Gao, M., Liu, F., & Mu, W. (2011). Resistance of Spodoptera exigua to ten insecticides in Shandong, China. Phytoparasitica, 39, 315–324.
Zhu, B. C. R., Henderson, G., Yu, Y., & Laine, R. A. (2003). Toxicity and repellency of patchouli oil and patchouli alcohol against Formosan subterranean termites Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). J Agric Food Chem, 51, 4585–4588.
Acknowledgements
This study was partially supported by the Spanish Ministry of Economy, Industry and Competitiveness (project AGL3013-47603-C2-1-R to E. Viñuela and P. Medina). The authors thank CAPES for PDSE scholarship (BEX 7003/15-03) awarded to Thiago J.S. Alves and the help provided by Sergio Estébanez García in the experimental assay and his contributions and suggestions in the current work.
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Murcia-Meseguer, A., Alves, T.J.S., Budia, F. et al. Insecticidal toxicity of thirteen commercial plant essential oils against Spodoptera exigua (Lepidoptera: Noctuidae). Phytoparasitica 46, 233–245 (2018). https://doi.org/10.1007/s12600-018-0655-9
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DOI: https://doi.org/10.1007/s12600-018-0655-9