Essential oils (EOs) are plant metabolites with important insecticidal effects. Nevertheless, information on the efficacy of the major substances on aphids and their natural enemies is still missing. The objective of this paper is, therefore, to identify the efficacy of selected EO majority substances-β-citronellol, carvacrol, isoeugenol, and linalool, including their binary mixtures-on the mortality and fertility of the aphid Metopolophium dirhodum, an important cereal pest. The best efficacy was proven for the binary mixture of β-citronellol and linalool (1:1 ratio), for which the estimated LC50(90) is 0.56(1.58) mL L-1. This binary mixture applied in sublethal concentrations significantly reduced aphid fertility. It was found that the phenomenon can be attributed to β-citronellol, as the females treated with LC30 laid 45.9% fewer nymphs, on average, compared to the control. Although β-citronellol and linalool, including their 1:1 mixture, showed very good efficacy on aphid mortality, they were, on the other hand, very friendly to the larvae of Aphidoletes aphidimyza and Chrysoperla carnea, which are important aphid predators. Based on our results, the newly discovered synergically acting binary mixture β-citronellol/linalool can be recommended as an efficient substance suitable for the further development of botanical insecticides used against aphids.

Crop Research Institute 161 06 Prague Czech Republic

Department of Plant Biotechnology College of Life Sciences and Biotechnology Korea University Seoul 02841 Republic of Korea

Department of Plant Protection Czech University of Life Sciences Prague 165 00 Prague Czech Republic

Zobrazit více v PubMed

Turek C., Stintzing F.C. Impact of different storage conditions on the quality of selected essential oils. Food Res. Int. 2012;46:341–353. doi: 10.1016/j.foodres.2011.12.028. DOI

El Asbahani A., Miladi K., Badri W., Sala M., Aït Addi E.H., Casabianca H., El Mousadik A., Hartmann D., Jilsale A., Renaud F.N.R., et al. Essential oils: From extraction to encapsulation. Int. J. Pharm. 2015;483:220–243. doi: 10.1016/j.ijpharm.2014.12.069. PubMed DOI

Kesraoui S., Andrés M.F., Berrocal-Lobo M., Soudani S., Gonzalez-Coloma A. Direct and indirect Effects of Essential Oils for Sustainable Crop Protection. Plants. 2022;11:2144. doi: 10.3390/plants11162144. PubMed DOI PMC

Bassolé I.H.N., Juliani H.R. Essential Oils in Combination and Their Antimicrobial Properties. Molecules. 2012;17:3989–4006. doi: 10.3390/molecules17043989. PubMed DOI PMC

Turek C., Stintzing F.C. Stability of Essential Oils: A Review. Compr. Rev. Food Sci. Food Saf. 2013;12:40–53. doi: 10.1111/1541-4337.12006. DOI

Buckle J. Clinical Aromatherapy—E-Book. Churchill Livingstone; Edinburgh, Scotland: 2014. Essential oils in practice.

Isman M.B. Commercial development of plant essential oils and their constituents as active ingredients in bioinsecticides. Phytochem. Rev. 2019;19:235–241. doi: 10.1007/s11101-019-09653-9. DOI

Hedden P., Harrewijn P., van Oosten A.M., Piron P.G.M. Natural terpenoids as messengers. A multidisciplinary study of their production, biological functions and practical applications. Ann. Bot. 2002;90:299–300. doi: 10.1093/aob/mcf187. DOI

Pavela R., Benelli G. Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci. 2016;21:1000–1007. doi: 10.1016/j.tplants.2016.10.005. PubMed DOI

Pavela R. Acute Toxicity and Synergistic and Antagonistic Effects of the Aromatic Compounds of Some Essential Oils Against Culex quinquefasciatus Say Larvae. Parasitol. Res. Founded Z. Parasitenkd. 2015;114:3835–3853. doi: 10.1007/s00436-015-4614-9. PubMed DOI

Ikbal C., Pavela R. Essential Oils as Active ingredients of Botanical insecticides Against Aphids. J. Pest Sci. 2019;92:971–986. doi: 10.1007/s10340-019-01089-6. DOI

Machial C.M., Shikano I., Smirle M., Bradbury R., Isman M.B. Evaluation of The Toxicity of 17 Essential Oils Against Choristoneura Rosaceana (Lepidoptera: Tortricidae) and Trichoplusia Ni (Lepidoptera: Noctuidae) Pest Manag. Sci. 2010;66:1116–1121. doi: 10.1002/ps.1988. PubMed DOI

Lengai G.M.W., Muthomi J.W., Mbega E.R. Phytochemical Activity and Role of Botanical Pesticides in Pest Management for Sustainable Agricultural Crop Production. Sci. Afr. 2020;7:e00239. doi: 10.1016/j.sciaf.2019.e00239. DOI

Bakkali F., Averbeck S., Averbeck D., Idaomar M. Biological Effects of Essential Oils—A Review. Food Chem. Toxicol. 2008;46:446–475. doi: 10.1016/j.fct.2007.09.106. PubMed DOI

Pavela R. Encapsulation—A Convenient Way to Extend the Persistence of the Effect of Eco-Friendly Mosquito Larvicides. Curr. Org. Chem. 2016;20:2674–2680. doi: 10.2174/1385272820666151026231851. DOI

Ibrahim S.S. Horticultural Crops. New India Publishing Agency; New Delhi, India: 2020. Essential Oil Nanoformulations as a Novel Method for insect Pest Control in Horticulture.

Abdelgaleil S.A.M., Al-nagar N.M.A., Abou-Taleb H.K., Shawir M.S. Effect of Monoterpenes, Phenylpropenes and Sesquiterpenes on Development, Fecundity and Fertility of Spodoptera littoralis (Boisduval) Int. J. Trop. insect Sci. 2022;42:245–253. doi: 10.1007/s42690-021-00539-y. DOI

Castilhos R.V., Grützmacher A.D., Coats J.R. Acute Toxicity and Sublethal Effects of Terpenoids and Essential Oils on The Predator Chrysoperla Externa (Neuroptera: Chrysopidae) Neotrop. Entomol. 2018;47:311–317. doi: 10.1007/s13744-017-0547-6. PubMed DOI

Yildirim E., Emsen B., Kordali S. Insecticidal Effects of Monoterpenes on Sitophilus Zeamais Motschulsky (Coleoptera: Curculionidae) J. Appl. Bot. Food Qual. 2013;86:198–204. doi: 10.5073/JABFQ.2013.086.027. DOI

Zhou L., Li C., Zhang Z., Li X., Dong Y., Cao H. Biological Activity and Safety Evaluation of Monoterpenes against the Peach Aphid (Myzus Persicae Sulzer) (Hemiptera: Aphididae) Int. J. Trop. insect Sci. 2021;41:2747–2754. doi: 10.1007/s42690-021-00454-2. DOI

Lee H.-W., Lee S.-G., Lee H.-S. Active Component Isolated from Eugenia Caryophyllata Leaves and Its Structural Analogues Show Insecticidal Properties Against Pochazia Shantungensis. Appl. Biol. Chem. 2016;59:609–614. doi: 10.1007/s13765-016-0200-9. DOI

Ling Chang C., Kyu Cho I., Li Q.X. insecticidal Activity of Basil Oil, Trans-Anethole, Estragole, and Linalool to Adult Fruit Flies of Ceratitis Capitata, Bactrocera Dorsalis, and Bactrocera Cucurbitae. J. Econ. Entomol. 2009;102:203–209. doi: 10.1603/029.102.0129. PubMed DOI

Steve D. Wratten Effects of Feeding Position of the Aphids Sitobion Avenae and Metopolophium Dirhodum on Wheat Yield and Quality. Ann. Appl. Biol. 1978;90:11–20. PubMed

Jezewska M. Transmission of barley yellow dwarf luteovirus isolates MAV and PAV by cereal aphid Metopolophium dirhodum. J. Plant Prot. Res. 1998;38:5–10.

Gong P., Li X., Wang C., Zhu S., Li Q., Zhang Y., Li X., Li G., Liu E., Gao H., et al. The Sensitivity of Field Populations of Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) to Seven insecticides in Northern China. Agronomy. 2021;11:1556. doi: 10.3390/agronomy11081556. DOI

Hummelbrunner L.A., Isman M.B. Acute, Sublethal, Antifeedant, and Synergistic Effects of Monoterpenoid Essential Oil Compounds on the Tobacco Cutworm, Spodoptera litura (Lep., Noctuidae) J. Agric. Food Chem. 2001;49:715–720. doi: 10.1021/jf000749t. PubMed DOI

Levchenko M.A., Silivanova E. A Synergistic and Antagonistic Effects of insecticide Binary Mixtures against House Flies (Musca Domestica) Regul. Mech. Biosyst. 2019;10:75–82. doi: 10.15421/021912. DOI

Jandricic S.E. Oviposition Behavior of The Biological Control Agent Aphidoletes Aphidimyza (Diptera: Cecidomyiidae) in Environments with Multiple Pest Aphid Species (Hemiptera: Aphididae) Biol. Control. 2013;65:235–245. doi: 10.1016/j.biocontrol.2013.01.013. DOI

Carrillo M., Elanov P. The potential of Chrysoperla carnea as a biological control agent of Myzus persicae in glass houses. Annl. Appl. Biol. 2004;32:433–439.

Costa A.V., Pinheiro P.F., de Queiroz V.T., Rondelli V.M., Marins A.K., Valbon W.R., Pratissoli D. Chemical Composition of Essential Oil from Eucalyptus Citriodora Leaves and insecticidal Activity Against Myzus Persicae and Frankliniella Schultzei. J. Essent. Oil-Bear. Plants. 2015;18:374–381. doi: 10.1080/0972060X.2014.1001200. DOI

Tabari M.A., Youssefi M.R., Esfandiari A., Benelli G. Toxicity of Β-Citronellol, Geraniol and Linalool from Pelargonium Roseum Essential Oil against the West Nile and Filariasis Vector Culex Pipiens (Diptera: Culicidae) Res. Vet. Sci. 2017;114:36–40. doi: 10.1016/j.rvsc.2017.03.001. PubMed DOI

Demirel S. Geraniol and Β-Citronellol Participate in The Vasorelaxant Effects of Rosa Damascena Miller Essential Oil on The Rat Thoracic Aorta. Fitoterapia. 2022;161:105243. doi: 10.1016/j.fitote.2022.105243. PubMed DOI

Da Silva M.J., Julio A.A., Dos Santos K.T. Sn(Scpii/Scp)-Catalyzed Β-Citronellol Esterification: A Brønsted Acid-Free Process for Synthesis of Fragrances At Room Temperature. Catal. Sci. 2015;5:1261–1266. doi: 10.1039/C4CY01069H. DOI

Szczepanik M., Zawitowska B., Szumny A. Insecticidal Activities of Thymus Vulgaris Essential Oil and Its Components (Thymol and Carvacrol) against Larvae of Lesser Mealworm, Alphitobius Diaperinus Panzer (Coleoptera: Tenebrionidae) Allelopath. J. 2012;30:129–142.

Aandersen A. Final report on the safety assessment of sodium p-chloro-m-cresol, p-chloro-m-cresol, chlorothymol, mixed cresols, m-cresol, o-cresol, p-cresol, isopropyl cresols, thymol, o-cymen-5-ol, and carvacrol. Int. J. Toxicol. 2006;25:29–127. doi: 10.1080/10915810600716653. PubMed DOI

Huang Y., Ho S.-H., Lee H.-C., Yap Y.-L. Insecticidal Properties of Eugenol, Isoeugenol and Methyleugenol and Their Effects on Nutrition of Sitophilus zeamais motsch. (Coleoptera: Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) J. Stored Prod. Res. 2002;38:403–412. doi: 10.1016/S0022-474X(01)00042-X. DOI

Kuo S.-C., Chuang S.-K., Lin H.-Y., Wang L.-H. Study of The Aerosol Fragrances of Eugenol Derivatives in Cananga Odorata Using Diffuse Reflectance infrared Fourier Transform Spectroscopy and Gas Chromatography. Anal. Chim. Acta. 2009;653:91–96. doi: 10.1016/j.aca.2009.08.034. PubMed DOI

Topal F. Anticholinergic and Antidiabetic Effects of Isoeugenol from Clove (Eugenia Caryophylata) Oil. Int. J. Food Prop. 2019;22:583–592. doi: 10.1080/10942912.2019.1597882. DOI

Zarlaha A., Kourkoumelis N., Stanojkovic T.P., Kovala-Demertzi D. Cytotoxic Activity of Essential Oil and Extracts of Ocimum Basilicum Against Human Carcinoma Cells. Molecular Docking Study of Isoeugenol as A Potent Cox and Lox inhibitor. Dig. J. Nanomater. Biostruct. 2014;9:907–917.

Rastogi S.C., Johansen J.D. Significant Exposures to Isoeugenol Derivatives in Perfumes. Contact Dermat. 2008;58:278–281. doi: 10.1111/j.1600-0536.2007.01283.x. PubMed DOI

Herman A., Tambor K., Herman A. Linalool Affects the Antimicrobial Efficacy of Essential Oils. Curr. Microbiol. 2016;72:165–172. doi: 10.1007/s00284-015-0933-4. PubMed DOI

Ebadollahi A. Evaluation of The Toxicity of Satureja intermedia C.A. Mey Essential Oil to Storage and Greenhouse insect Pests and A Predator Ladybird. Foods. 2020;9:712. doi: 10.3390/foods9060712. PubMed DOI PMC

Pavela R., Sedlák P. Post-Application Temperature as A Factor influencing the insecticidal Activity of Essential Oil from Thymus Vulgaris. Ind. Crops Prod. 2018;113:46–49. doi: 10.1016/j.indcrop.2018.01.021. DOI

Corbett J.R. The Biochemical Mode of Action of Pesticides. Academic Press; Cambridge, MA, USA: 1974. DOI

Pavela R. Sublethal Effects of Some Essential Oils on The Cotton Leafworm Spodoptera Littoralis(Boisduval) J. Essent. Oil Bear. Plants. 2012;15:144–156. doi: 10.1080/0972060X.2012.10644030. DOI

Hategekimana A., Erler F. Fecundity and Fertility inhibition Effects of Some Plant Essential Oils and Their Major Components Against Acanthoscelides Obtectus Say (Coleoptera: Bruchidae) J. Plant Dis. Prot. 2020;127:615. doi: 10.1007/s41348-020-00311-3. DOI

Richard A. Integrated Pest Management: Concepts, Tactics, Strategies and Case Studies. Cambridge University Press; Cambridge, UK: 2008. Weinzierl integrating Pesticides with Biotic and Biological Control for Arthropod Pest Management.

Novák M., Pavela R., Spinozzi E., Ferrati M., Petrelli R., Maggi F., Ricciardi R., Benelli G. Lethal and Sublethal Effects of Carlina Oxide on the Aphid Metopolophium dirhodum and Its Non-Target Impact on Two Biological Control Agents. J. Pest Sci. 2024 doi: 10.1007/s10340-024-01768-z. DOI

Abbott W.S. A Method of Computing the Effectiveness of an insecticide. 1925. J. Am. Mosq. Control. Assoc. 1987;3:302–303. PubMed

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