Abstract
The codling moth Cydia pomonella is the major pest of apple orchards worldwide. Chemical insecticides are commonly used against pests; however, increased number of resistance cases highlights the urgent need for alternative control methods. Plant-derived essential oils are promising alternatives to chemical insecticides. Although they show great efficacies under laboratory conditions, their efficacy are lower in the field; requiring their formulation. Methyl-eugenol (ME) is a plant essential oil with insecticidal activity; however, knowledge on the efficacy of formulated forms and mode of action of ME is limited. Here, we developed two formulations of ME, an emulsion oil in water (EW) and an emulsifiable concentrate (EC). Bioassays on neonate larvae revealed a limited efficacy of non-formulated ME with the highest mortality of 34.1% at 15% concentration at 120 h after the application. The mortality caused by EW formulation without ME led to a maximum of 10% mortality, while the mortality caused by EW formulation with ME varied between 26.7 and 100% for the lowest and highest concentrations, respectively. As the EC formulation without ME led to 90% mortality, no further bioassay on the EC formulation of ME was conducted. EW formulation of ME showed strong contact toxicity against C. pomonella larvae after 120 h of application (LC50 = 40.5 µL/cm2). Since ME is known to inhibit acetylcholinesterase, the relative expression levels of AChE-1 and AChE-2 genes were examined in ME-exposed surviving larvae upon its plain application. Only AChE-1 was upregulated with a five-fold increase 24 h after treatment, which might be the reason for the survival of the larvae. Overall, the EW formulation of ME has great potential against codling moth. Further studies under field conditions will be helpful to use this essential oil in integrated pest management programs.
Graphical abstract
Similar content being viewed by others
Data availability
The datasets are available from the corresponding author on reasonable request.
References
Aara A, Chappidi V, Ramadas MN (2020) Antioxidant activity of eugenol in piper betel leaf extract. J Family Med Prim Care 9:327
Alkan M (2020) Chemical composition and insecticidal potential of different Origanum spp. (Lamiaceae) essential oils against four stored product pests. Turkish J Entomol 44:149–163
Alkan M, Ertürk S (2020) Insecticidal efficacy and repellency of trans-anethole against four stored-product insect pests. J Agric Sci 26:64–70
Anonymous (2021). https://food.ec.europa.eu/document/download/ba0347f1-c401-4423-8a8d-f353a916daac_en. Accessed 09 Oct 2022
Araújo Couto HGS, Blank AF, Oliveira Silva AME, Nogueira PCL, Arrigoni-Blank MF, Nizio DAC, Pinto JAO (2019) Essential oils of basil chemotypes: major compounds, binary mixtures, and antioxidant activity. Food Chem 293:446–454
Ashrafudoulla M, Mizan MFR, Ha AJW, Park SH, Ha SD (2020) Antibacterial and antibiofilm mechanism of eugenol against antibiotic resistance Vibrio parahaemolyticus. Food Microbiol 91:103500
Beers EH, Stuckling DM, Prokopy RJ, Avila J (2003) Ecology and management of apple arthropod pests. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses, 1st edn. CABI Publishing, Wallingford, UK, pp 489–514
Benelli G, Pavela R, Maggi F, Petrelli R, Nicoletti M (2017) Commentary: making green pesticides greener? The potential of plant products for nanosynthesis and pest control. J Clust Sci 28:3–10
Benitez NP, Meléndez León EM, Stashenko EE (2009) Eugenol and methyl eugenol chemotypes of essential oil of species Ocimum gratissimum L. and Ocimum campechianum Mill. from Colombia. J Chromatogr Sci 47:800–803
Borges DF, Lopes EA, Moraes ARF, Soares MS, Visôtto LE, Oliveira CR, Valente VMM (2018) Formulation of botanicals for the control of plant-pathogens: a review. Crop Prot 110:135–140
Cai R, Hu M, Zhang Y, Niu C, Yue T, Yuan Y, Wang Z (2019) Antifungal activity and mechanism of citral limonene and eugenol against Zygosaccharomyces rouxii. LWT-Food Sci Technol 106:50–56
Cassanelli S, Reyes M, Rault M, Manicardi GC, Sauphanor B (2006) Acetylcholinesterase mutation in an insecticide-resistant population of the codling moth Cydia pomonella (L.). Insect Biochem Mol Biol 36:642–653
Chang CL, Cho IK, Li QX (2009) 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 102:203–209
Chen MH, Dorn S (2010) Microsatellites reveal genetic differentiation among populations in an insect species with high genetic variability in dispersal, the codling moth Cydia pomonella (L.) (Lepidoptera: Tortricidae). Bull Entomol Res 100:75–85
Chen HJ, Liao Z, Hui XM, Li GQ, Li F, Han ZJ (2009) Ace2, rather than ace1, is the major acetylcholinesterase in the silkworm, Bombyx mori. Insect Sci 16:297–303
Chericoni S, Prieto JM, Iacopini P, Cioni P, Morelli I (2005) In vitro activity of the essential oil of Cinnamomum zeylanicum and eugenol in peroxynitrite-induced oxidative processes. J Agric Food Chem 53:4762–4765
da Silva BC, Melo DR, Franco CT, Maturano R, Fabri RL, Daemon E (2020) Evaluation of eugenol and (e)-cinnamaldehyde insecticidal activity against larvae and pupae of Musca domestica (Diptera: Muscidae). J Med Entomol 57:181–186
Dawkar VV, Barage SH, Barbole RS, Fatangare A, Grimalt S, Haldar S, Heckel DG, Gupta VS, Thulasiram HV, Svatoš A, Giri AP (2019) Azadirachtin-A from Azadirachta indica impacts multiple biological targets in cotton bollworm Helicoverpa armigera. ACS Omega 4:9531–9541
Dobrat W, Martijn A (1995) CIPAC handbook volume G: analysis of technical and formulated pesticides. Collaborative International Pesticides Analytical Council
Doğan C, Hänniger S, Heckel DG, Coutu C, Hegedus DD, Crubaugh L, Groves RL, Amutkan Mutlu D, Suludere Z, Bayram Ş, Toprak U (2021) Characterization of calcium signaling proteins from the fat body of the Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): implications for diapause and lipid metabolism. Insect Biochem Mol Biol 133:103549
Dorn S, Schumacher P, Abivardi C, Meyhöfer R (1999) Global and regional pest insects and their antagonists in orchards: spatial dynamics. Agric Ecosyst Environ 1422:1–8
Dwivedy AK, Kumar M, Upadhyay N, Dubey NK (2015) Green chemistry in agricultural pest management programmes. Med chem S 2:005. https://doi.org/10.4172/2161-0444.1000005
Eddleston M, Street JM, Self I, Thompson A, King T, Williams N, Naredo G, Dissanayake K, Yu LM, Worek F, John H, Smith S, Thierman H, Harris JB, Clutton RE (2012) A role of solvents in the toxicity of agricultural organophosphorus insecticides. Toxicology 294(2–3):94
Farag MA, Ezzat SM, Salama MM, Tadros MG, Serya RAT (2016) Anti-acetylcholinesterase activity of essential oils and their major constituents from four Ocimum species. Z Naturforsch C 71:393–402
Feng J, Zhang Q, Liu Q, Zhu Z, McClements DJ, Jafari SM (2018) Application of nanoemulsions in formulation of pesticides. Nanoemulsions. Academic Press, pp 379–413
Fournier D (2005) Mutations of acetylcholinesterase which confer insecticide resistance in insect populations. Chem Biol Interact 157:257–261
Gašić S, Tanović B (2013) Biopesticide formulations, possibility of application and future trends. Pestic Fitomed 28:97–102
González Armijos MJ, Viteri Jumbo L, D’Antonino Faroni LR, Oliveira EE, Flores AF, Haddi K (2019) Fumigant toxicity of eugenol and its negative effects on biological development of Callosobruchus maculatus L. Rev Mexicana Cienc Agric 36:5–15
Govindarajan M, Rajeswary M, Hoti SL, Bhattacharyya A, Benelli G (2016) Eugenol α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors. Parasitol Res 115:807–815
Güney G, Cedden D, Hänniger S, Heckel DG, Coutu C, Hegedus DD, Amutkan Mutlu D, Suludere Z, Sezen K, Güney E, Toprak U (2021) Silencing of an ABC transporter, but not a cadherin, decreases the susceptibility of Colorado potato beetle larvae to Bacillus thuringiensis ssp. tenebrionis Cry3Aa toxin. Arch Insect Biochem Physiol 108:e21834
Hatagekimana A, Erler F (2020) Comparative repellent activity of single, binary and ternary combinations of plant essential oils and their major components against Sitophilus oryzae L. (Coleoptera: Curculionidae). J Plant Dis Prot 127:873–881
Hazra DK, Karmakar R, Poi R, Bhattacharya S, Mondal S (2017) Recent advances in pesticide formulations for eco-friendly and sustainable vegetable pest management: a review. Arch Agric Environ Sci 2:232–237
Hedlund J, Longo SB, York R (2020) Agriculture, pesticide use, and economic development: a global examination (1990–2014). Rural Sociol 85:519–544
Ismail AR, Ooi TL, Salmiah A (2004) Environment friendly palm-based inert ingredient for EW-insecticide formulations. MPOB TT No. 236: MIS No. 243
Isman MB (2017) Bridging the gap: moving botanical insecticides from the laboratory to the farm. Ind Crops Prod 110:10–14
Isman MB (2020) Bioinsecticides based on plant essential oils: a short overview. Z Naturforsch C 75:179–182
Isman MB, Miresmailli S, Machial C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev 10:197–204
Jaramillo-Colorado BE, Pino-Benitez N, González-Coloma A (2019) Volatile composition and biocidal (antifeedant and phytotoxic) activity of the essential oils of four Piperaceae species from Choco-Colombia. Ind Crops Prod 138:111463. https://doi.org/10.1016/j.indcrop.2019.06.026
Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M (2017) Molecular targets for components of essential oils in the insect nervous system-a review. Molecules 23:34
Ju D, Mota-Sanchez D, Fuentes-Contreras E, Zhang YL, Wang XQ, Yang XQ (2021) Insecticide resistance in the Cydia pomonella (L): global status, mechanisms, and research directions. Pestic Biochem Physiol 178:104925
Kadoić Balaško M, Bažok R, Mikac KM, Lemic D, Pajač Živković I (2020) Pest management challenges and control practices in codling moth: a review. InSects 11:38
Kitulagodage M, Astheimer LB, Buttemer WA (2008) Diacetone alcohol, a dispersant solvent, contributes to acute toxicity of a fipronil-based insecticide in a passerine bird. Ecotoxicol Environ Saf 71:597–600. https://doi.org/10.1016/j.ecoenv.2007.11.001
Kothari SK, Bhattacharya AK, Ramesh S (2004) Essential oil yield and quality of methyl eugenol rich Ocimum tenuiflorum Lf (syn. O. sanctum L.) grown in south India as influenced by method of harvest. J Chromatogr A 1054:67–72
Lee SE, Lee BH, Choi WS, Park BS, Kim JG, Campbell BC (2001) Fumigant toxicity of volatile natural products from Korean spices and medicinal plants towards the rice weevil. Sitophilus oryzae (L). Pest Manag Sci 57:548–553
Software LeOra (2002) Polo-PC: a user’s guide to probit and logit analysis. LeOra Software, Berkeley, CA, USA
Li SJ, Guo YF, Li YF, Zhang XJ (2012) Research progress on stability mechanism of pesticide emulsion in water. Mod Agrochem 11:6–10
Li AS, Iijima A, Huang J, Li QX, Chen Y (2020) Putative mode of action of the monoterpenoids linalool, methyl eugenol, estragole, and citronellal on ligand-gated ion channels. Engineering 6:541–545
Lina EC, Widhianingrum I, Putri ME, Evalia NF, Makky M (2018) Insecticidal activity of Piper aduncum fruit and Tephrosia vogelii leaf mixed formulations against Plutella xylostella (L.) (Lepidoptera: Plutellidae). J Biopestic 11:69–75
Lucia A, Guzmán E (2021) Emulsions containing essential oils, their components or volatile semiochemicals as promising tools for insect pest and pathogen management. Adv Colloid Interface Sci 287:102330
Maliszewska J, Tęgowska E (2018) Toxicity of insecticide carrier solvent: effect of xylene on hemolymph biochemical parameters in Blaberus giganteus L. Pol J Environ Stud 27(5):2385–2390
Marchese A, Barbieri R, Coppo E, Orhan IE, Daglia M, Nabavi SF, Morteza I, Mohammad A, Nbabvi SM, Ajami M (2017) Antimicrobial activity of eugenol and essential oils containing eugenol: a mechanistic viewpoint. Crit Rev Microbiol 43:668–689
Mossa ATH, Abdelfattah NAH, Mohafrash SMM (2017) Nanoemulsion of camphor (Eucalyptus globules) essential oil, formulation, characterization and insecticidal activity against wheat weevil, Sitophilus granaries. Asian J Crop Sci 9:50–62
Mota-Sanchez D, Wise JC, Poppen RV, Gut LJ, Hollingworth RM (2008) Resistance of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), larvae in Michigan to insecticides with different modes of action and the impact on field residual activity. Pest Manag Sci 64:881–890
Ngamo TL, Goudoum A, Ngassoum MB, Ngassoum M, Lognay G, Malaisse F, Hance T (2007) Chronic toxicity of essential oils of 3 local aromatic plants towards Sitophilus zeamais Motsch (Coleoptera: Curculionidae). Afr J Agric Res 2:164–167
Obeng-Ofori D, Reichmuth C (1997) Bioactivity of eugenol a major component of essential oil of Ocimum suave (Wild.) against four species of stored-product Coleoptera. Int J Pest Manag 43:89–94
Olea AF, Bravo A, Martínez R, Thomas M, Sedan C, Espinoza L, Carrasco H (2019) Antifungal activity of eugenol derivatives against Botrytis cinerea. Molecules 24:1239
Pang YP (2014) Insect acetylcholinesterase as a target for effective and environmentally safe insecticides. Adv Insect Phys 46:435–494
Pascual-Villalobos MJ, Guirao P, Díaz-Baños FG, Cantó-Tejero M, Villora G (2019) Oil in water nanoemulsions of botanical active substances. In: Koul O (ed) Nano-biopesticides today and future perspectives. Academic Press, London, UK, pp 223–248
Park YL, Tak JH (2016) Essential oils for arthropod pest management in agricultural production systems. Essential oils in food preservation, flavor and safety. Academic Press, pp 61–70
Pathirana HNKS, Wimalasena SHMP, De Silva BC, Hossain S, Heo G (2019) Antibacterial activity of clove essential oil and eugenol against fish pathogenic bacteria isolated from cultured olive flounder (Paralichthys olivaceus). Slov Vet Res 56:31–38
Pillmoor JB, Wright K, Terry AS (1993) Natural products as a source of agrochemicals and leads for chemical synthesis. Pestic Sci 39:131–140
Purkait A, Biswas S, Saha S, Hazra DK, Roy K, Biswas PK, Ghosh SK, Kole RK (2019) Formulation of plant based insecticides, their bio-efficacy evaluation and chemical characterization. Crop Prot 125:104907
Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424
Shayestehmehr H, Karimzadeh R, Feizizadeh B, Iranipour S (2021) Spatial distribution of Cydia pomonella (Lepidoptera: Tortricidae) populations and its relation with topographic variables. Appl Entomol Zool 56:187–197
Skandrani D, Gaubin Y, Vincent C, Beau B, Murat JC, Soleilhavoup JP, Croute F (2006) Relationship between toxicity of selected insecticides and expression of stress proteins (HSP, GRP) in cultured human cells: effects of commercial formulations versus pure active molecules. Biochim Biophys Acta 1760(1):95
Sparks TC, Lorsbach BA (2017) Perspectives on the agrochemical industry and agrochemical discovery. Pest Manag Sci 73:672–677
Sparks TC, Crossthwaite AJ, Nauen R, Banba S, Cordova D, Earley F, Ebbinghaus-Kintscher U, Fujioka S, Hirao A, Karmon D, Kennedy R, Nakao T, Popham HJR, Salgado V, Watson GB, Wedel BJ, Wessels FJ (2020) Insecticides, biologics and nematicides: updates to IRAC’s mode of action classification - a tool for resistance management. Pestic Biochem Physiol 167:104587
Srivastava AK, Srivastava SK, Syamsundar KV (2005) Bud and leaf essential oil composition of Syzygium aromaticum from India and Madagascar. Flavour Fragr J 20:51–53
Tan KH, Nishida R (2012) Methyl eugenol: its occurrence, distribution, and role in nature, especially in relation to insect behavior and pollination. J Insect Sci 12:56
Thapa S, Lv M, Xu H (2017) Acetylcholinesterase: a primary target for drugs and insecticides. Mini Rev Med Chem 17:1665–1676
Toprak U, Bayram Ş, Gürkan MO (2006) Comparative biological activities of a plaque-purified variant and a Turkish native isolate of SpliNPV-B against Spodoptera littoralis (Lepidoptera: Noctuidae). Pest Manag Sci 62:57–63
Toprak U, Baldwin D, Erlandson M, Gillott C, Harris S, Hegedus DD (2013) In vitro and in vivo application of RNA interference for targeting genes involved in peritrophic matrix synthesis in a lepidopteran system. Insect Sci 20:92–100
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115. https://doi.org/10.1093/nar/gks596
Vargas-Méndez LY, Sanabria-Flórez PL, Saavedra-Reyes LM, Merchan-Arenas DR, Kouznetsov VV (2019) Bioactivity of semisynthetic eugenol derivatives against Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae infesting maize in Colombia. Saudi J Biol Sci 26:1613–1620
Voudouris CC, Sauphanor B, Franck P, Reyes M, Mamuris Z, Tsitsipis JA, Vontas J, Margaritopoulos JT (2011) Insecticide resistance status of the codling moth Cydia pomonella (Lepidoptera: Tortricidae) from Greece. Pestic Biochem Physiol 100:229–238
Waghmare JT, Ware AM, Momin SA (2007) Neem oil as pesticide. J Dispers Sci Technol 28:323–328
Wei ZH, Liu M, Hu C, Yang XQ (2020) Overexpression of glutathione S-transferase genes in field λ-cyhalothrin-resistant population of Cydia pomonella: reference gene selection and expression analysis. J Agric Food Chem 68(21):5825–5834. https://doi.org/10.1021/acs.jafc.0c01367
WHO (2016) Manual on development and use of FAO and WHO specifications for pesticides / FAO Plant Production and Protection Paper 228. First edition - third revision. – Geneva: WHO Press. FAO/WHO. http://apps.who.int/iris/bitstream/handle/10665/246192/WHO-HTM-NTD-WHOPES-2016.4-eng.pdf?sequence=1. Accessed 06 Apr 2020
Wu XM, Feng JG, Ma C (2013) Pesticide preparation processing experiment. Chemical Industry Press, Beijing, pp 15–18
Yang X, Li X, Zhang Y (2013) Molecular cloning and expression of CYP9A61: a chlorpyrifos-ethyl and lambda-cyhalothrin-inducible cytochrome P450 cDNA from Cydia pomonella. Int J Mol Sci 14(12):24211–24229. https://doi.org/10.3390/ijms141224211
Zhao R, Song R, Sun G, Liu S, Li B, Cao Y, Li Y (2020) Cutoff Ostwald ripening stability of eugenol-in-water emulsion by co-stabilization method and antibacterial activity evaluation. Food Hydrocoll 107:105925
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
MA: conceptualization; data curation; methodology; investigation; formal analysis; writing—original draft. AÖ: conceptualization; investigation; writing—original draft. AY: conceptualization; methodology; writing—original draft. CY: conceptualization. Eİ: methodology; investigation; formal analysis; writing—original draft; writing—review and editing. SE: conceptualization; data curation; methodology; investigation; formal analysis; writing—review and editing. UT: conceptualization; data curation; methodology; writing—review and editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Alkan, M., Özdem, A., Yılmaz, A. et al. Emulsion oil in water formulation of methyl-eugenol increases its insecticidal activity against Cydia pomonella L. (Lepidoptera: Tortricidae). Appl Entomol Zool 58, 139–148 (2023). https://doi.org/10.1007/s13355-023-00815-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13355-023-00815-y