Abstract
Owing to the complexity in the chemical composition of plant essential oils, they often display enhanced insecticidal activity when applied as a mixture. Although the insecticidal activity of plant essential oils has been gaining more attention recently, understanding in the mechanism of synergy has not been studied as much. In the present study, insecticidal activity of 28 individual essential oils and their mixtures against the third instar larvae of Spodoptera litura was examined. Among the oils tested, basil oil exhibited the strongest contact toxicity, and mandarin oil displayed the greatest boosting effect when the remaining oils were mixed with basil oil. Estragole and linalool were determined as the major active constituents for the insecticidal activity of basil oil and limonene for mandarin oil from the chemical analyses and compound elimination assay. Based on the LD50 values, the binary mixture of basil and mandarin oils exhibited enhanced toxicity compared to the individual application of the two oils, showing synergy ratios of 1.3 and 1.4 from two statistical models. As for the major active compounds, synergistic interaction was found in tertiary mixture of estragole, linalool, and limonene in the blending ratio of 7:2:7, displaying the same insecticidal activity of the binary mixture of basil and mandarin oils. The synergistic effect was only observed in the tertiary mixture, indicating each compound play crucial roles of the overall contact toxicity. Increased penetration through cuticular layer and amplified neurophysiological response were proposed for the mechanism of synergistic effect.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad M, Ghaffar A, Rafiq M (2013) Host plants of leaf worm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in Pakistan. Asian J Agric Biol 1:23–28
Ahmad M, Gull S (2017) Susceptibility of armyworm Spodoptera litura (Lepidoptera: Noctuidae) to novel insecticides in Pakistan. Can Entomol 149:649–661. https://doi.org/10.4039/tce.2017.29
Benelli G, Govindarajan M, AlSalhi MS et al (2018) High toxicity of camphene and γ-elemene from Wedelia prostrata essential oil against larvae of Spodoptera litura (Lepidoptera: Noctuidae). Environ Sci Pollut Res 25:10383–10391. https://doi.org/10.1007/s11356-017-9490-7
Don-Pedro KN (1996) Investigation of single and joint fumigant insecticidal action of citruspeel oil components. Pestic Sci 46:79–84. https://doi.org/10.1002/(SICI)1096-9063(199601)46:1%3c79::AID-PS319%3e3.0.CO;2-8
Enan EE (2005) Molecular and pharmacological analysis of an octopamine receptor from american cockroach and fruit fly in response to plant essential oils. Arch Insect Biochem Physiol 59:161–171. https://doi.org/10.1002/arch.20076
Feng R, Isman MB (1995) Selection for resistance to azadirachtin in the green peach aphid, Myzus persicae. Experientia 51:831–833. https://doi.org/10.1007/BF01922438
Gaire S, Scharf ME, Gondhalekar AD (2019) Toxicity and neurophysiological impacts of plant essential oil components on bed bugs (Cimicidae: Hemiptera). Sci Rep 9:3961. https://doi.org/10.1038/s41598-019-40275-5
Gammon DW (1980) Pyrethroid resistance in a strain of Spodoptera littoralis is correlated with decreased sensitivity of the CNS in vitro. Pestic Biochem Physiol 13:53–62. https://doi.org/10.1016/0048-3575(80)90082-6
Gandhi K, Patil RH, Srujana Y (2016) Field resistance of Spodoptera litura (Fab.) to conventional insecticides in India. Crop Prot 88:103–108. https://doi.org/10.1016/j.cropro.2016.06.009
Gisi U, Binder H, Rimbach E (1985) Synergistic interactions of fungicides with different modes of action. Trans Br Mycol Soc 85:299–306. https://doi.org/10.1016/S0007-1536(85)80192-3
Gross AD, Bloomquist JR (2018) Pharmacology of central octopaminergic and muscarinic pathways in Drosophila melanogaster larvae: assessing the target potential of GPCRs. Pestic Biochem Physiol 151:53–58. https://doi.org/10.1016/j.pestbp.2018.08.001
Gross AD, Kimber MJ, Day TA et al (2013) Quantitative structure-activity relationships (QSARs) of monoterpenoids at an expressed American cockroach octopamine receptor. In: Beck John J, Coats Joel R, MEK Stephen O Duke (eds) Pest management with natural products. American Chemical Society, Washington
Han Y, Sun Z, Chen W (2019) Antimicrobial susceptibility and antibacterial mechanism of limonene against Listeria monocytogenes. Molecules 25:33. https://doi.org/10.3390/molecules25010033
Hummelbrunner LA, Isman MB (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. https://doi.org/10.1021/jf000749t
Isman MB (2020) Botanical insecticides in the twenty-first century—fulfilling their promise? Annu Rev Entomol 65:233–249. https://doi.org/10.1146/annurev-ento-011019-025010
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Isman MB (2015) A renaissance for botanical insecticides? Pest Manag Sci 71:1587–1590. https://doi.org/10.1002/ps.4088
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19:140–145. https://doi.org/10.1016/j.tplants.2013.11.005
Isman MB, Wan AJ, Passreiter CM (2001) Insecticidal activity of essential oils to the tobacco cutworm, Spodoptera litura. Fitoterapia 72:65–68. https://doi.org/10.1016/S0367-326X(00)00253-7
Kim S-W, Lee H-R, Jang M-J et al (2016) Fumigant toxicity of Lamiaceae plant essential oils and blends of their constituents against adult rice weevil Sitophilus oryzae. Molecules 21:361. https://doi.org/10.3390/molecules21030361
Koul O, Singh R, Kaur B, Kanda D (2013) Comparative study on the behavioral response and acute toxicity of some essential oil compounds and their binary mixtures to larvae of Helicoverpa armigera, Spodoptera litura and Chilo partellus. Ind Crops Prod 49:428–436. https://doi.org/10.1016/j.indcrop.2013.05.032
Langeveld WT, Veldhuizen EJA, Burt SA (2014) Synergy between essential oil components and antibiotics: a review. Crit Rev Microbiol 40:76–94. https://doi.org/10.3109/1040841X.2013.763219
Liu D, Jia Z-Q, Peng Y-C et al (2018) Toxicity and sublethal effects of fluralaner on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Pestic Biochem Physiol 152:8–16. https://doi.org/10.1016/j.pestbp.2018.08.004
Miresmailli S, Bradbury R, Isman MB (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. https://doi.org/10.1002/ps.1157
Murfadunnisa S, Vasantha-Srinivasan P, Ganesan R et al (2019) Larvicidal and enzyme inhibition of essential oil from Spheranthus amaranthroids (Burm.) against lepidopteran pest Spodoptera litura (Fab.) and their impact on non-target earthworms. Biocatal Agric Biotechnol 21:101324. https://doi.org/10.1016/j.bcab.2019.101324
Norris EJ, Johnson JB, Gross AD et al (2018) Plant essential oils enhance diverse pyrethroids against multiple strains of mosquitoes and inhibit detoxification enzyme processes. Insects 9:132. https://doi.org/10.3390/insects9040132
Pavela R (2015a) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitol Res 114:3835–3853. https://doi.org/10.1007/s00436-015-4614-9
Pavela R (2015b) Essential oils for the development of eco-friendly mosquito larvicides: A review. Ind Crops Prod 76:174–187. https://doi.org/10.1016/j.indcrop.2015.06.050
Pavela R (2010) Acute and synergistic effects of monoterpenoid essential oil compounds on the larvae of Spodoptera littoralis. J Biopestic 3:573–578
Pavela R (2016) History, presence and perspective of using plant extracts as commercial botanical insecticides and farm products for protection against insects – a review. Plant Prot Sci 52:229–241. https://doi.org/10.17221/31/2016-PPS
Pavela R, Sedlák P (2018) Post-application temperature as a factor influencing the insecticidal activity of essential oil from Thymus vulgaris. Ind Crops Prod 113:46–49. https://doi.org/10.1016/j.indcrop.2018.01.021
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. https://doi.org/10.1146/annurev-ento-120710-100554
Rose HA (1985) The relationship between feeding specialization and host plants to aldrin epoxidase activities of midgut homogenates in larval Lepidoptera. Ecol Entomol 10:455–467. https://doi.org/10.1111/j.1365-2311.1985.tb00744.x
Shi L, Shi Y, Zhang Y, Liao X (2019) A systemic study of indoxacarb resistance in Spodoptera litura revealed complex expression profiles and regulatory mechanism. Sci Rep 9:14997. https://doi.org/10.1038/s41598-019-51234-5
Tak J-H, Isman MB (2015) Enhanced cuticular penetration as the mechanism for synergy of insecticidal constituents of rosemary essential oil in Trichoplusia ni. Sci Rep 5:12690. https://doi.org/10.1038/srep12690
Tak J-H, Isman MB (2017) Penetration-enhancement underlies synergy of plant essential oil terpenoids as insecticides in the cabbage looper. Trichoplusia ni Sci Rep 7:42432. https://doi.org/10.1038/srep42432
Tak J-H, Jovel E, Isman MB (2017) Synergistic interactions among the major constituents of lemongrass essential oil against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni. J Pest Sci 90:735–744. https://doi.org/10.1007/s10340-016-0827-7
Tharamak S, Yooboon T, Pengsook A et al (2020) Synthesis of thymyl esters and their insecticidal activity against Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci 76:928–935. https://doi.org/10.1002/ps.5598
Tong F, Coats JR (2010) Effects of monoterpenoid insecticides on [3H]-TBOB binding in house fly GABA receptor and 36Cl− uptake in American cockroach ventral nerve cord. Pestic Biochem Physiol 98:317–324. https://doi.org/10.1016/j.pestbp.2010.07.003
Trisyono A, Whalon ME (1999) Toxicity of neem applied alone and in combinations with Bacillus thuringiensis to Colorado potato beetle (coleoptera: chrysomelidae). J Econ Entomol 92:1281–1288. https://doi.org/10.1093/jee/92.6.1281
US EPA (2015) Active ingredients eligible for minimum risk pesticide products. https://www.epa.gov/sites/production/files/2015-12/documents/minrisk-active-ingredients-tolerances-2015-12-15.pdf. Accessed 14 Jan 2021
Wagner H, Ulrich-Merzenich G (2009) Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine 16:97–110. https://doi.org/10.1016/j.phymed.2008.12.018
Wang X, Huang Q, Hao Q et al (2018) Insecticide resistance and enhanced cytochrome P450 monooxygenase activity in field populations of Spodoptera litura from Sichuan, China. Crop Prot 106:110–116. https://doi.org/10.1016/j.cropro.2017.12.020
Wing KD, Schnee ME, Sacher M, Connair M (1998) A novel oxadiazine insecticide is bioactivated in lepidopteran larvae. Arch Insect Biochem Physiol 37:91–103. https://doi.org/10.1002/(SICI)1520-6327(1998)37:1%3c91::AID-ARCH11%3e3.0.CO;2-5
Xue M, Pang Y-H, Wang H-T et al (2010) Effects of four host plants on biology and food utilization of the cutworm, Spodoptera litura. J Insect Sci 10:1–14. https://doi.org/10.1673/031.010.2201
Yang Y, Isman MB, Tak J-H (2020) Insecticidal activity of 28 essential oils and a commercial product containing Cinnamomum cassia bark essential oil against Sitophilus zeamais Motschulsky. Insects 11:474. https://doi.org/10.3390/insects11080474
Yeom H-J, Kang JS, Kim G-H, Park I-K (2012) Insecticidal and acetylcholine esterase inhibition activity of Apiaceae plant essential oils and their constituents against adults of German cockroach (Blattella germanica). J Agric Food Chem 60:7194–7203. https://doi.org/10.1021/jf302009w
Acknowledgement
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2019R1C1C1004834).
Funding
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2019R1C1C1004834).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflicts of interest.
Additional information
Communicated by Antonio Biondi .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kim, S., Yoon, J. & Tak, JH. Synergistic mechanism of insecticidal activity in basil and mandarin essential oils against the tobacco cutworm. J Pest Sci 94, 1119–1131 (2021). https://doi.org/10.1007/s10340-021-01345-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01345-8