Abstract
Mosquitoes have already developed resistance toward most of the commercial synthetic repellents. Therefore, searching for new potential alternatives is the need of the hour. In the study, we evaluated the repellency of six citrus-derived essential oils against Aedes aegypti using the arm-in-cage method. The results showed more than 50 percent repellency up to 4 h exposure time at 1 mg/cm2 area for three Citrus spp. with maximum repellency of 81 percent for C. aurantifolia. Therefore, two of the major constituents of C. aurantifolia EO, namely citral and limonene, were chosen further for the repellency test. The results showed higher efficacy of compounds than crude oil. EC50 for commercial standard repellent DEET was determined for comparison under the same experimental conditions. To understand the possible mode of action of citral, limonene and DEET, in-silico interactions of these compounds with odorant-binding proteins (OBP1 and OBP22) and acetylcholinesterase (AChE) enzymes were studied. The findings revealed positive docking of all of these compounds having affinity values in the range of − 6.0 to − 6.9 kcal/mol. Overall, the study demonstrated that limonene and essential oils of Citrus aurantifolia could be the best potential alternative for synthetic repellents.
Similar content being viewed by others
Availability of Data and Material
Not applicable.
References
Roy DN, Goswami R, Pal A (2017) The Insect repellents: A silent environmental chemical toxicant to the health. Environ Toxicol Pharmacol 50:91–102
Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res Int J Devot Pharmacol Toxicol Eval Nat Product Deriv 19(4):303–309
Soonwera M (2015) Efficacy of essential oils from Citrus plants against mosquito vectors Aedes aegypti (Linn.) and Culex quinquefasciatus (Say). J Agricult Technol 11(3):669–681
Pavela R, Benelli G (2016) Ethnobotanical knowledge on botanical repellents employed in the African region against mosquito vectors–a review. Exp Parasitol 167:103–108
Abiy E, Gebre-Michael T, Balkew M, Medhin G (2015) Repellent efficacy of DEET, MyggA, neem (Azedirachta indica) oil and chinaberry (Melia azedarach) oil against Anopheles arabiensis, the principal malaria vector in Ethiopia. Malar J 14(1):1–6
Bisignano G, Cimino F, Saija A (2011) Biological activities of citrus essential oils. In: Citrus oils: composition, advanced analytical techniques, contaminants, and biological activity, Giovanni, D., Luigi, M., Eds, CRC Press (Taylor and Francis), Florida, USA
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils–a review. Food Chem Toxicol 46(2):446–475
Butnariu M, Bostan C (2011) Antimicrobial and anti-inflammatory activities of the volatile oil compounds from Tropaeolum majus L. (Nasturtium). Afr J Biotechnol 210(31):5900–5909
Mohammadhosseini M (2017) The ethnobotanical, phytochemical and pharmacological properties and medicinal applications of essential oils and extracts of different Ziziphora species. Ind Crop Prod 105:164–192
Khanikor B, Adhikari K, Rabha B (2021) Citrus essential oils: a suite of insecticidal compounds. InCitrus, IntechOpen
Butnariu M (2012) An analysis of Sorghum halepense’s behavior in presence of tropane alkaloids from Datura stramonium extracts. Chem Cent J 6(1):1–7
Rajabi Z, Ebrahimi M, Farajpour M, Mirza M, Ramshini H (2014) Compositions and yield variation of essential oils among and within nine Salvia species from various areas of Iran. Ind Crop Prod 61:233–239
Sarma R, Adhikari K, Mahanta S, Khanikor B (2019) Insecticidal activities of Citrus aurantifolia essential oil against Aedes aegypti (Diptera: Culicidae). Toxicol Rep 6:1091–1096
Leite NR, Krogh R, Xu W, Ishida Y, Iulek J, Leal WS, Oliva G (2009) Structure of an Odorant-Binding Protein from the Mosquito Aedes aegypti suggests a Binding Pocket Covered by a pH-Sensitive “Lid”. PLoS ONE 4(11):1–7
Corbel V, Stankiewicz M, Pennetier C, Fournier D, Stojan J, Girard E, Dimitriv M, Molgo J, Hougard J-M, Lapied B (2009) Evidence for inhibition of cholinesterases in insect and mammalian nervous systems by the insect repellent DEET. BMC Biol 7(47):1–11
Dubey RK, Kumar R, Dubey NK (2007) Evaluation of eupatorium cannabinum Linn. oil in enhancement of shelf life of mango fruits from fungal rotting. World J Microbiol Biotechnol 23(4):467–473
Pushpanathan T, Jebanesan A, Govindarajan M (2008) The essential oil of Zingiber officinalis Linn (Zingiberaceae) as a mosquito larvicidal and repellent agent against the filarial vector Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol Res 102:1289–1291
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge
Webb B, Sali A (2016) Comparative Protein Structure Modeling Using Modeller. Curr Prot Bioinformatics 54:5.6.1-5.6.37
Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallograph 26(2):283–291
Trott O, Olson AJ (2010) Auto Dock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. J Comput Chem 31:455–461
Amer A, Mehlhorn H (2006) Repellency effect of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes. Parasitol Res 99(4):478–490
Deletre E, Martin T, Campagne P, Bourguet D, Cadin A, Menut C, Bonafos R, Chandre F (2013) Repellent, irritant and toxic effects of 20 plant extracts on adults of the malaria vector Anopheles gambiae mosquito. PLoS ONE 8(12):e82103
Giatropoulos A, Papachristos DP, Kimbaris A, Koliopoulos G, Polissiou MG, Emmanouel N, Michaelakis A (2012) Evaluation of bioefficacy of three Citrus essential oils against the dengue vector Aedes albopictus (Diptera: Culicidae) in correlation to their components enantiomeric distribution. Parasitol Res 111(6):2253–2263
Nishimura O, Brillada C, Yazawa S, Maffei ME, Arimura GI (2012) Transcriptome pyrosequencing of the parasitoid wasp Cotesia vestalis: genes involved in the antennal odorant-sensory system. PLoS ONE 7(11):e50664
Dickens JA, Bohbot JD (2013) Mini review: mode of action of mosquito repellents. Pestic Biochem Physiol 106:149–155
Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72(5):698–711
Tsitsanou KE, Thireou T, Drakou CE, Koussis K, Keramioti MV, Leonidas DD, Eliopoulos E, Iatrou K, Zographos SE (2012) Anopheles gambiae odorant binding protein crystal complex with the synthetic repellent DEET: implications for structure based design of novel mosquito repellents. Cell Mol Life Sci 69:283–297
Syed Z, Leal WS (2008) Mosquitoes smell and avoid the insect repellent DEET. Proc Natl Acad Sci (PNAS) 105(36):13598–13603
Khanikor B, Parida P, Yadav PRNS, Borah D (2013) Comparative mode of action of some terpene compounds against octopamine receptor and acetyl cholinesterase of mosquito and human system by the help of homology modeling and Docking studies. J Appl Pharm Sci 3(2):6–12
Acknowledgements
We thank Prof. Probodh Borah, Department of Animal Biotechnology, Assam Agricultural University, for his guidance in in-silico studies. Authors are also very thankful to the Head, Department of Botany, Gauhati University, for helping in identifying the plant materials. Authors are thankful to the Head, Dept. of Zoology, Gauhati University, for necessary help and support.
Funding
The authors received no funding for this work.
Author information
Authors and Affiliations
Contributions
KA wrote the manuscript and did all the experiments. RS did the statistical analysis and aided in the bioinformatics works. BR aided in repellent bioassay, collection of plant materials and extraction of essential oil. BK designed the experiments, supervised the experiments and manuscript. All authors have read and approved the manuscript for submission.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Code Availability
Not applicable.
Ethics Approval and Consent to Participate
Use of human volunteers for the study was approved by the Institutional Animal Ethical Committee Gauhati University (Permit No. IAEC/Per/2019/RF/2019–7). We strictly adhered to the protocols suggested by the committee for the repellency tests. Written informed consent was provided by the participant.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Significance statement
Chemical repellent has posed serious health hazards on the environment and the target insects already developed resistance against the chemical repellent. This manuscript examines and proves the repellent property of Citrus essential oil and the main constituent terpene compounds of Citrus aurantifolia- citral and limonene against Aedes aegypti.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Adhikari, K., Sarma, R., Rabha, B. et al. Repellent Activity of Citrus Essential Oils and Two Constituent Compounds Against Aedes aegypti. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 92, 621–628 (2022). https://doi.org/10.1007/s40011-022-01347-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40011-022-01347-1