Abstract
Rutaceae are widely recognized for their toxic and repellent activity exerted against mosquitoes. In our research, the essential oils extracted from fresh leaves of wild and cultivated plants of Ruta chalepensis L. (Rutaceae) were evaluated for larvicidal and repellent activity against the Asian tiger mosquito, Aedes albopictus Skuse (Diptera: Culicidae), currently the most invasive mosquito worldwide. In this research, gas chromatography and gas chromatography–mass spectrometry analyses of the essential oils from wild and cultivated plants showed only quantitative differences, in particular relatively to the amounts of ketone derivatives, while the qualitative profile evidenced a similar chemical composition. Both essential oils from wild and cultivated R. chalepensis plants were able to exert a very good toxic activity against A. albopictus larvae (wild plants, LC50 = 35.66 ppm; cultivated plants, LC50 = 33.18 ppm), and mortality was dosage dependent. These data are the first evidence of the toxicity of R. chalepensis against mosquitoes. Furthermore, the R. chalepensis essential oil from wild plants was an effective repellent against A. albopictus, also at lower dosages: RD50 was 0.000215 μL/cm2 of skin, while RD90 was 0.007613 μL/cm2. Our results clearly evidenced that the larvicidal and repellent activity of R. chalepensis essential oil could be used for the development of new and safer products against the Asian tiger mosquito.
Similar content being viewed by others
References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Adams RP (1995) Identification of essential oils components by gas chromatography/mass spectroscopy. Carol Stream, Allured
Al-mazra’awi MS, Ateyyat M (2009) Insecticidal and repellent activities of medicinal plant extracts against the sweet potato whitefly, Bemisia tabaci (Hom.: Aleyrodidae) and its parasitoid Eretmocerus mundus (Hym.: Aphelinidae). J Pest Sci 82:149–154
Amer A, Mehlhorn H (2006a) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Amer A, Mehlhorn H (2006b) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490
Benedict MQ, Levine RS, Hawley WA, Lounibos LP (2007) Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vect Bor Zoon Dis 7:76–85
Benelli G, Flamini G, Canale A, Cioni PL, Conti B (2012a) Toxicity evaluation of different essential oil formulations against the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera Tephritidae). Crop Protect 42:223–229
Benelli G, Flamini G, Canale A, Molfetta I, Cioni PL, Conti B (2012b) Repellence of Hyptis suaveolens L. (Lamiaceae) whole essential oil and major constituents against adults of the granary weevil Sitophilus granarius (L.) (Coleoptera: Dryophthoridae). Bull Insectol 65:177–183
Caminade C, Medlock JM, Ducheyne E, McIntryre KM, Leach S, Baylis M, Morse A (2012) Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. J R Soc Interface 9:2708–2717
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 107:1455–1462
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 UF, 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
Elango G, Rahuman AA, Kamaraj C, Bagavan A, Zahir AA (2011) Efficacy of medicinal plant extracts against malarial vector, Anopheles subpictus Grassi. Parasitol Res 108:1437–1445
Estrada-Franco J (1995) Biology, disease relationship, and control of Aedes albopictus. PAHO technical paper p. 42
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. doi:10.1007/s00436-012-3074-8
Gillij YG, Gleiser RM, Zygadlo JA (2008) Mosquito repellent activity of essential oils of aromatic plants growing in Argentina. Bioresour Technol 99:2507–2515
Gleiser RM, Bonino MA, Zygadlo JA (2011) Repellence of essential oils of aromatic plants growing in Argentina against Aedes aegypti. Parasitol Res 108:69–78
Govindarajan M (2010) Chemical composition and larvicidal activity of leaf essential oil from Clausena anisata (Willd.) Hook. f. ex Benth (Rutaceae) against three mosquito species. Asian Pacif J Tropic Med 2010:874–877
Govindarajan M, Sivakumar R (2012) Adulticidal and repellent properties of indigenous plant extracts against Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Parasitol Res 110:1607–1620
Govindarajan M, Mathivanan T, Elumalai K, Krishnappa K, Anandan A (2011) Mosquito larvicidal, ovicidal, and repellent properties of botanical extracts against Anopheles stephensi, Aedes aegypti, and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 109:353–367
Gratz NG (2004) Critical review of the vector status of Aedes albopictus. Med Vet Entomol 18:215–227
Guarrera PM (1999) Traditional antihelmintic, antiparasitic and repellent uses of plants in Central Italy. J Ethnopharmacol 68:183–192
Hadis LMM, Meknonnen V, Asfar T (2003) Field trials on repellent activity of four plant products against mainly Mansonia population in Western Ethiopia. Phytother Res 17:202–205
Hafeez F, Akram W, Shaalan EA (2011) Mosquito larvicidal activity of citrus limonoids against Aedes albopictus. Parasitol Res 109:221–229
James AA (1992) Mosquito molecular genetics: the hands that feed bite back. Science 257:37–38
Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574
Kamgang B, Marcombe S, Chandre F, Nchoutpouen E, Nwane P, Etang J, Corbelle V, Paupy C (2011) Insecticide susceptibility of Aedes aegypti and Aedes albopictus in Central Africa. Par Vect 4:79
Kamsuk K, Choochote W, Chaithong U, Jitpakdi A, Tippawangkosol P, Riyong D, Pitasawat B (2007) Effectiveness of Zanthoxylum piperitum-derived essential oil as an alternative repellent under laboratory and field application. Parasitol Res 100:339–345
Kauffman WC, Kennedy GG (1989) Toxicity of allelochemicals from wild insect-resistant tomato Lycopersicon hirsutum f. glabratum to Campoletis sonorensis, a parasitoid of Heliothis zea. J Chem Ecol 15:2051–2060
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
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
Konig WA, Hochmuth DH, Joulain D (2001) Terpenoids and related constituents of essential oils. Library of Mass Finder 2.1, Institute of Organic Chemistry, Hamburg, Germany
Koren G, Matsui D, Bailey B (2003) DEET-based insect repellents: safety implications for children and pregnant and lactating women. Canad Med Assoc J 169:209–212
Kovendan K, Arivoli S, Maheshwaran R, Baskar K, Vincent S (2012) Larvicidal efficacy of Sphaeranthus indicus, Cleistanthus collinus and Murraya koenigii leaf extracts against filarial vector, Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol Res 111:1025–1035
Lafferty FW, Stauffer DB (1994) Wiley Registry of Mass Spectral Data, 6th edn. Mass Spectometry Library Search System Bench-Top/PBM, Version 3.10d. Palisade, Newfield
Lapied B, Pennetier C, Apaire-Marchais V, Licznar P, Corbel V (2009) Innovative applications for insect viruses: towards insecticide sensitization. Trends Biotechnol 4:190–198
Mathew N, Anitha MG, Bala TSL, Sivakumar SM, Narmadha R, Kalyanasundaram M (2009) Larvicidal activity of Saraca indica, Nyctanthes arbor-tristis and Clitoria ternatea extracts against three mosquito vector species. Parasitol Res 104:1017–1025
Mendesila E, Tadesseb M, Negashc M (2012) Efficacy of plant essential oils against two major insect pests of coffee (Coffee berry borer, Hypothenemus hampei, and antestia bug, Antestiopsis intricata) and maize weevil, Sitophilus zeamais. Archiv Phytopathol Plant Protect 45:366–372
Moore SJ, Lenglet A, Hill N (2002) Field evaluation of three plant-based insect repellents against malaria vectors in Vaca Diez Province, the Bolivian Amazon. J Am Mosq Control Assoc 18:107–110
National Institute of Standards and Technology (1999) NIST/EPA/NIH Mass Spectral Library, Pc Version 1.7. Perkin Elmer, Norwalk
Noudjou F, Kouninki H, Ngamo LST, Maponmestsem PM, Ngassoum M, Hance T, Haubruge E, Malaisse F, Marlier M, Lognay GC (2007) Effect of site location and collecting period on the chemical composition of Hyptis spicigera Lam. An insecticidal essential oil from North-Cameroon. J Essent Oil Res 19:597–601
Omolo MO, Okinyo D, Ndiege IO, Lwande W, Hassanali A (2004) Repellency of essential oils of some Kenyan plants against Anopheles gambiae. Phytochem 65:2797–2802
Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D (2009) Aedes albopictus, an arbovirus vector: from the darkness to the light. Microb Infect 11:1177–1185
Peng Z, Yang J, Wang H, Simons FER (1999) Production and characterisation of monoclonal antibodies to two new mosquito Aedes aegypti salivary protein. Insect Biochem Mol Biol 29:909–914
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
Pushpanathan T, Jebanesan A, Govindarajan M (2006) Larvicidal, ovicidal and repellent activities of Cymbopogan citrates Stapf (Graminae) essential oil against the filarial mosquito Culex quinquefasciatus (Say) (Diptera: Culicidae). Tropical Biomed 23:208–212
Rahuman AA, Gopalakrishnan G, Ghouse BS, Arumugama S, Himalayan B (2000) Effect of Feronia limonia on mosquito larvae. Fitoterapia 71:553–555
Rai KS (1991) Aedes albopictus in the Americas. Annu Rev Entomol 36:459–484
Rajkumar S, Jebanesan A (2005) Repellency of volatile oils from Moschosma polystachyum and Solanum xanthocarpum against filarial vector Culex quinquefasciatus Say. Tropical Biomed 22:139–142
Reiter P, Sprenger D (1987) The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J Am Mosq Control Assoc 3:494–501
Robert LL, Olson JK (1989) Susceptibility of female Aedes albopictus from Texas to commonly used adulticides. J Am Mosq Control Assoc 5:251–253
Severini C, Romi R, Marinucci M, Rajmond M (1993) Mechanism of insecticide resistance in field populations of Culex pipiens from Italy. J Am Mosq Control Assoc 9:164–168
Skuse F (1894) The banded mosquito of Bengal. Indian Mus Notes 3:20
Strickman D, Frances SP, Debboun M (2009) Put on something natural. In: Prevention of bugs, bites, stings and disease. Oxford University Press, New York
Sudakin DL, Trevathan WR (2003) DEET: a review and update of safety and risk in the general population. J Toxicol Clin Toxicol 41:831
Tabanca N, Demirci B, Kiyan HT, Ali A, Bernier UR, Wedge DE, Khan IA, Başer KHC (2012) Repellent and larvicidal activity of Ruta graveolens essential oil and its major individual constituents against Aedes aegypti. Planta Med 2012:78–90
Tchoumbougang F, Amvam Zollo PH, Fecam Boyom F, Nyegue MA, Bessière JM (2005) Aromatic plants of Tropical Central Africa. XLVIII. Comparative study of the essential oils of four Hyptis species from Cameroon: H. lanceolata Poit., H. pectinata (L.) Poit., H. spicigera Lam. and H. suaveolens Poit. Flavour Fragr J 20:340–343
Tiwary M, Naik SN, Tewary DK, Mittal PK, Yadav S (2007) Chemical composition and larvicidal activities of the essential oil of Zanthoxylum armatum DC (Rutaceae) against three mosquito vectors. J Vect Borne Dis 44:198–204
Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res 19:303–309
WHO (1981) Instruction for determining the susceptibility or resistance of mosquito larvae to insecticide. WHO/VBC/81.807. Control of tropical diseases. World Health Organization, Geneva
WHO (2009) Guidelines for efficacy testing of mosquito repellents for human skin. WHO/HTM/NTD/WHOPES/2009.4. Control of neglected tropical diseases. World Health Organization, Geneva
Yamani AS, Mehlhorn H, Adham FK (2012) Yolk protein uptake in the oocyte of the Asian tiger mosquito Aedes albopictus (Skuse) (Diptera: Culicidae). Parasitol Res 111:1315–1324
Acknowledgments
We would like to thank Angelo Canale (University of Pisa) for his insightful critical comments on an earlier version of the manuscript, Helen Romito (Sant’Anna School of Advanced Studies, Pisa) for the language proofreading, Alessandra Francini (Institute of Life Sciences, Sant’Anna School of Advanced Studies, Pisa) for the statistical advices, Pancrazio Campagna for providing the pictures of R. chalepensis, Giulia Fiore, Isaia Nisoli, Francesca Baroncelli, and Lorenzo Rossi for the superb assistance, and the ten patient volunteers.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Conti, B., Leonardi, M., Pistelli, L. et al. 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 (2013). https://doi.org/10.1007/s00436-012-3221-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-012-3221-2