Abstract
In the current laboratory study, 14 essential oils (EOs) derived from 12 Lamiaceae plant species and their major components were screened for their larvicidal and repellent properties against Aedes albopictus, an invasive mosquito species of great medical importance. The results of toxicity bioassays revealed that the EOs from Thymus vulgaris, Ocimum basilicum, Origanum dictamnus, Origanum majorana, and Origanum vulgare, as well as their major components (terpenes), namely thymol, carvacrol, p-cymene, and γ-terpinene exerted the highest larvicidal effect. Essential oils from Mellisa officinalis, Origanum dictamus, Mentha spicata (chem. piperitenone epoxide), Origanum majorana, and Satureja thymbra were the most potent repellents, with the last two assigned as the best ones. Among the terpenes tested, piperitenone epoxide, carvacrol, thymol, and piperitenone provided the highest level of protection against Ae. albopictus adults. Chemical analysis revealed the presence of a high number of terpenes in the EOs, while in most cases, the biological action of the tested EOs and their major components was in consistency. The most effective EOs and terpenes that were identified through the current laboratory bioassays could be used as alternative agents to control larvae and repel adults of Ae. albopictus.
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References
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corporation, Carol Stream
Adorjan B, Buchbauer G (2010) Biological properties of essential oils: an updated review. Flavour Fragr J 25:407–426
Amer A, Mehlhorn H (2006) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Anees AM (2008) Larvicidal activity of Ocimum sanctum Linn. (Labiatae) against Aedes aegypti (L.) and Culex quinquefasciatus (Say). Parasitol Res 103:1451–1453
Ansari MA, Vasudevan P, Tandon M, Razdan RK (2000) Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour Technol 71:267–271
Barnard DR (1999) Repellency of essential oils to mosquitoes (Diptera: Culicidae). J Med Entomol 36(5):625–629
Beereboom JJ (1996) The synthesis of piperitenone via mesityl oxide and methyl vinyl ketone. J Am Chem Soc 31:2026–2027
Bouguerra N, Djebbar TN, Soltani N (2017) Algerian Thymus vulgaris essential oil: chemical composition and larvicidal activity against the mosquito Culex pipiens. Int J Mosq Res 4(1):37–42
Boulogne I, Petit P, Ozier-Lafontaine H, Desfontaines L, Loranger-Merciris G (2012) Insecticidal and antifungal chemicals produced by plants: a review. Environ Chem Lett 10:325–347. https://doi.org/10.1007/s10311-012-0359-1
Cetin H, Yanikoglu A (2006) A study of the larvicidal activity of Origanum (Labiatae) species from Southwest Turkey. J Vector Ecol 31(1):118–122
Choi WS, Park BS, Ku SK, Lee SE (2002) Repellent activities of essential oils and monoterpenes against Culex pipiens pallens. J Am Mosq Control Assoc 18(4):348–351
Chouin-Carneiro T, Vega-Rua A, Vazeille M, Yebakima A, Girod R, Goindin D, Dupont-Rouzeyrol M, Lourenço-de-Oliveira R, Failloux AB (2016) Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika virus. Plos Neglect Trop D 10(3):e0004543. https://doi.org/10.1371/journal.pntd.0004543
Coleman RE, Robert LL, Roberts LW, Glass JA, Seeley DC, Laughinghouse A, Perkins P, Wirtz RA (1993) Laboratory evaluation of repellents against four anopheline mosquitoes (Diptera: Culicidae) and two phlebotomine sand flies (Diptera: Psychodidae). J Med Entomol 30:499–502
Conti B, Benelli G, Flamini G, Cioni PL, Profeti R, Ceccarini L, Macchia M, Canale A (2012a) Larvicidal and repellent activity of Hyptis suaveolens (Lamiaceae) essential oil against the mosquito Aedes albopictus Skuse (Diptera: Culicidae). Parasitol Res 110:2013–2021
Conti B, Benelli G, Leonardi M, Afifi FU, Cervelli C, Profeti R, Pistelli L, Canale A (2012b) Repellent effect of Salvia dorisiana, S. longifolia, and S. sclarea (Lamiaceae) essential oils against the mosquito Aedes albopictus Skuse (Diptera: Culicidae). Parasitol Res 111:291–299. https://doi.org/10.1007/s00436-012-2837-6
Conti B, Leonardi M, Pistelli L, Profeti R, Ouerghemmi I, Benelli G (2012c) Larvicidal and repellent activity of essential oils from wild and cultivated Ruta chalepensis L. (Rutaceae) against Aedes albopictus Skuse (Diptera: Culicidae), an arbovirus vector. Parasitol Res 112:991–999. https://doi.org/10.1007/s00436-012-3221-2
Conti B, Canale A, Bertoli A, Gozzini F, Pistelli L (2010) Essential oil composition and larvicidal activity of six Mediterranean aromatic plants against the mosquito Aedes albopictus (Diptera: Culicidae). Parasitol Res 107:1455–1461
Daferera DJ, Ziogas BN, Polissiou MG (2000) GC-MS analysis of essential oils from some Greek aromatic plants and their fungitoxicity on Penicillium digitatum. J of Agr Food Chem 48(6):2576–2581
Dias CD, Moraes DFC (2014) Essential oils and their compounds as Aedes aegypti L. (Diptera: Culicidae) larvicides: review. Parasitol Res 113:565–592
El-Akhal F, El Ouali Lalami A, Ez Zoubi Y, Greche H, Guemmouh R (2014) Chemical composition and larvicidal activity of essential oil of Origanum majorana (Lamiaceae) cultivated in Morocco against Culex pipiens (Diptera: Culicidae). Asian Pac J Trop Biomed 4(9):746–750
Enserink M (2008) A mosquito goes global. Science 320:864–866
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London
Fradin MS, Day JF (2002) Comparative efficacy of insect repellents against mosquito bites. New Engl J Med 347:13–18
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 111:2253–2263
Giatropoulos A, Pitarokili D, Papaioannou F, Papachristos DP, Koliopoulos G, Emmanouel N, Tzakou O, Michaelakis A (2013) Essential oil composition, adult repellency and larvicidal activity of eight Cupressaceae species from Greece against Aedes albopictus (Diptera: Culicidae). Parasitol Res 112(3):1113–1123
Govere JM, Durrheim DV (2006) Techniques for evaluating repellents. In: Debboun M, Frances SP, Strickman D (eds) Insect repellents: principles methods and use. CRC Press, Boca Raton
Govindarajan M, Kadaikunnan S, Alharbi SN, Benelli G (2016) Acute toxicity and repellent activity of the Origanum scabrum Boiss. & Heldr. (Lamiaceae) essential oil against four mosquito vectors of public health importance and its biosafety on non-target aquatic organisms. Environ Sci Pollut Res 23:23228–23238
Govindarajan M, Sivakumar R, Rajeswari M, Yogalakshmi K (2012) Chemical composition and larvicidal activity of essential oil from Mentha spicata (Linn.) against three mosquito species. Parasitol Res 110:2023–2032
Gratz NG (2004) Critical review of the vector status of Aedes albopictus. Med Vet Entomol 18:215–227
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and increasingly regulated world. Annu Rev Entomol 51:45–66
James AA (1992) Mosquito molecular genetics: the hands that feed bite back. Science 257:37–38
Kalaivani K, Senthil-Nathan S, Murugesan AG (2012) Biological activity of selected Lamiaceae and Zingiberaceae plant essential oils against the dengue vector Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 110(3):1261–1268
Karamaouna F, Kimbaris A, Michaelakis A, Papachristos D, Papatsakona P, Tsora E (2013) Insecticidal activity of plant essential oils against the vine mealybug, Planococcus ficus. J of Ins Sc 13(142):1–13
Kimbaris AC, González-Coloma A, Andrés MF, Vidali VP, Polissiou MG, Santana-Méridas O (2017) Biocidal compounds from Mentha sp. essential oils and their structure—activity relationships. Chem and Bioders 14(3):e1600270
Klun JA, Khrimian A, Debboun M (2006) Repellent and deterrent effects of SS220, Picaridin and Deet suppress human blood feeding by Aedes aegypti, Anopheles stephensi, and Phlebotomus papatasi. J Med Entomol 43:34–39
Koc S, Oz E, Cetin H (2012) Repellent activities of some Labiatae plant essential oils against the saltmarsh mosquito Ochlerotatus caspius (Pallas, 1771) (Diptera: Culicidae). Parasitol Res 110:2005–2209
Koliopoulos G, Pitarokili D, Kioulos E, Michaelakis A, Tzakou O (2010) Chemical composition and larvicidal evaluation of Mentha, Salvia, and Melissa essential oils against the West Nile virus mosquito Culex pipiens. Parasitol Res 107:327–335
Koutsaviti K, Giatropoulos A, Pitarokili D, Papachristos DP, Michaelakis A, Tzakou O (2014) Greek Pinus essential oils: larvicidal activity and repellency against Aedes albopictus (Diptera: Culicidae). Parasitol Res. https://doi.org/10.1007/s00436-014-4220-2
Kumar S, Wahab N, Warikoo R (2011) Bioefficacy of Mentha piperita essential oil against dengue fever mosquito Aedes aegypti L. Asian Pac J Trop Biomed:85–88
Maia MF, Moore SJ (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malaria J 10(suppl.1):1–15
Manimaran A, Cruz MMJJ, Muthu C, Vincent S, Ignacimuthu S (2012) Larvicidal and knockdown effects of some essential oils against Culex quinquefasciatus Say, Aedes aegypti (L.) and Anopheles stephensi (Liston). Adv Biosci Biotechnol 3:855–862
Mathew J, Thoppil JE (2011) Chemical composition and mosquito larvicidal activities of Salvia essential oils. Pharm Biol 49(5):456–463
Michaelakis A, Papachristos D, Kimbaris A, Polissiou M (2011) Larvicidal evaluation of three Mentha species essential oils and their isolated major components against the West Nile virus mosquito. Hell Plant Prot J 4:35–43
Michaelakis A, Theotokatos SA, Koliopoulos G, Chorianopoulos NG (2007) Essential oils of Satureja species: insecticidal effect on Culex pipiens larvae (Diptera: Culicidae). Molecules 12:2567–2578
Murugan K, Aarthi N, Kovendan K, Panneerselvam C, Chandramohan B, Kumar MP, Amerasan D, Paulpandi M, Chandirasekar R, Devakumar D, Suresh U, Subramaniam J, Higuchi A, Alarfaj A, Marcello Nicoletti M, Mehlhorn H, Benelli G (2015) Mosquitocidal and antiplasmodial activity of Senna occidentalis (Cassiae) and Ocimum basilicum (Lamiaceae) from Maruthamalai hills against Anopheles stephensi and Plasmodium falciparum. Parasitol Res 114:3657–3664. https://doi.org/10.1007/s00436-015-4593-x
Naghibi F, Mosaddegh M, Motamed SM, Ghorbani A (2005) Labiatae family in folk medicine in Iran: from ethnobotany to pharmacology. Iran J Pharm Res 2:63–79
Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378
Oshaghi MA, Ghalandari R, Vatandoost H, Shayeghi M, Kamali-nejad M, Tourabi-Khaledi H, Abolhassani M, Hashemzadeh M (2003) Repellent effect of extracts and essential oils of Citrus limon (Rutaceae) and Melissa officinalis (Labiatae) against main malaria vector, Anopheles stephensi (Diptera: Culicidae). Iran J Public Health 32(4):47–52
Park BS, Choi WS, Kim JH, Kim KH, Lee SE (2005) Monoterpenes from thyme (Thymus vulgaris) as potential mosquito repellents. J Am Mosq Control Assoc 21(1):80–83
Pavela R (2009) Larvicidal property of essential oils against Culex quinquefasciatus Say (Diptera: Culicidae). Ind Crop Prod 30:311–315
Pavela R, Vrchotová N, Tříska J (2009) Mosquitocidal activities of thyme oils (Thymus vulgaris L.) against Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 105:1365–1370
Petrakis EA, Kimbaris AC, Perdikis DC, Lykouressis DP, Tarantilis PA, Polissiou MG (2014) Responses of Myzus persicae (Sulzer) to three Lamiaceae essential oils obtained by microwave-assisted and conventional hydrodistillation. Ind Crops and Prod 62:272–279
Pitarokili D, Michaelakis A, Koliopoulos G, Giatropoulos A, Tzakou O (2011) Chemical composition, larvicidal evaluation, and adult repellency of endemic Greek Thymus essential oils against the mosquito vector of West Nile virus. Parasitol Res 109:425–430
Radwan MA, El-Zemity SR, Mohamed SA, Sherby SM (2008) Larvicidal activity of some essential oils, monoterpenoids and their corresponding N-methyl carbamate derivatives against Culex pipiens (Diptera: Culicidae). Int J Trop Insect Sci 28(2):61–68
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
SPSS Inc. (2004). SPSS 14 for Windows users guide. SPSS Inc., Chicago, IL
Sritabutra D, Soonwera M, Waltanachanobon S, Poungjai S (2011) Evaluation of herbal essential oil as repellents against Aedes aegypti (L.) and Anopheles dirus Peyton & Harrion. Asian Pac J Trop Biomed:s124–s128
Sudakin DL, Trevathan WR (2003) DEET: a review and update of safety and risk in the general population. J Toxicol Clin Toxicol 41:831–839
Sukumar K, Perich MJ, Boobar LR (1991) Botanical derivatives in mosquito control: a review. J Am Mosq Control Assoc 7(2):210–237
Tawatsin A, Asavadachanukorn P, Thavaral U, Wongsinkongman P, Bansidhi J, Boonruad T, Chavalittumrong P, Soonthornchareonnon N, Komalamisra N, Mulla MS (2006) Repellency of essential oils extracted from plants in Thailand against four mosquito vectors (Diptera: Culicidae) and oviposition deterrent effects against Aedes aegypti (Diptera: Culicidae). Southeast Asian J Trop Med Public Health 37(5):915–931
Trabousli AF, Taoubi K, EI-Haj S, Bessiere J, Rammal S (2002) Insecticidal properties of essential plant oils against the mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Manag Sci 58:491–495
Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res 19:303–309
World Health Organization (WHO) (2005) Guidelines for laboratory and field testing of mosquito larvicides. World Health Organization (WHO) communicable disease control, prevention and eradication. WHO pesticide evaluation scheme (WHOPES), Geneva, Switzerland pp 1–41
Yang P, Ma Y (2005) Repellent effect of plant essential oils against Aedes albopictus. J Vector Ecol 30(2):231–234
Zhu J, Zeng X, Yan M, Liu T, Qian K, Han Y, Xue S, Tucker B, Schultz G, Coats J, Rowley W, Zhang A (2006) Adult repellency and larvicidal activity of five plant essential oils against mosquitoes. J Am Mosq Control Assoc 22(3):515–522
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The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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This research has been co-financed by the European Union (EU Environmental Funding Programme LIFE+ Environment Policy and Governance) and Greek national funds through the LIFE CONOPS project (www.conops.gr) “Development and demonstration of management plans against—the climate change enhanced—invasive mosquitoes in S. Europe” (LIFE12 ENV/GR/000466).
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Giatropoulos, A., Kimbaris, A., Michaelakis, Α. et al. Chemical composition and assessment of larvicidal and repellent capacity of 14 Lamiaceae essential oils against Aedes albopictus. Parasitol Res 117, 1953–1964 (2018). https://doi.org/10.1007/s00436-018-5892-9
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DOI: https://doi.org/10.1007/s00436-018-5892-9