Skip to main content
Log in

Essential oil composition, adult repellency and larvicidal activity of eight Cupressaceae species from Greece against Aedes albopictus (Diptera: Culicidae)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The present study evaluated leaf essential oils from eight Cupresaceae species; Cupressus arizonica, Cupressus benthamii, Cupressus macrocarpa, Cupressus sempervirens, Cupressus torulosa, Chamaecyparis lawsoniana, Juniperus phoenicea, and Tetraclinis articulata for their larvicidal and repellent properties against Aedes albopictus, a mosquito of great ecological and medical importance. Based on the LC50 values, C. benthamii essential oil was the most active (LC50 = 37.5 mg/L) while the other tested Cupressaceae essential oils provided rather moderate toxicity against larvae (LC50 = 47.9 to 70.6 mg/L). Under the used laboratory conditions, three of the essential oils (C. benthamii, C. lawsoniana, and C. macrocarpa) provided sufficient protection against mosquito adults, equivalent to the standard repellent “Deet” in the 0.2 mg/cm2 dose, while C. macrocarpa assigned as the superior repellent oil in the 0.08 mg/cm2 dose. Chemical analysis of the essential oils using gas chromatography and gas chromatography–mass spectrometry revealed the presence of 125 components.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Achak N, Romane A, Alifriqui M, Markouk M (2009) Chemical composition, organic and mineral contents of leaves of Tetraclinis articulala (Vahl) Masters from the Tensift- Al haouz, marrakech region (Morocco). J Essent Oil Bear Plants 12:198–204

    CAS  Google Scholar 

  • Adams RP (2007) Identification of essential oils components by Gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corp, Carol Stream, Illinois

    Google Scholar 

  • Adams RP, Zanoni TA, Barrero AF, Lara A (1996) Comparisons of the leaf essential oils of Juniperus phoenicea, J. phoenicea subsp. eu-mediterranea Lebr. & Thiv. and J. phoenicea var. rurbinata (Guss.) Parl. J Essent Oil Res 8:367–371

    Article  CAS  Google Scholar 

  • Adams RP, Zanoni TA, Lara A, Barrero AF, Cool LG (1997) Comparisons among Cupressus arizonica Greene, C. benthamii Endl., C. lindleyi Klotz. ex Endl. and C. lusitanica Mill. using leaf essential oils and DNA fingerprinting. J Essent Oil Res 9:303–309

    Article  CAS  Google Scholar 

  • Adorjan B, Buchbauer G (2010) Biological properties of essential oils: an updated review. Flavour Fragr J 25:407–426

    Article  CAS  Google Scholar 

  • Afsharypuor S, Tavakoli P (2005) Essential oil constituents of leaves and fruits of Cupressus arizonica Greene. J Essent Oil Res 17:225–226

    Article  Google Scholar 

  • Amer A, Mehlhorn H (2006a) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472

    Article  PubMed  Google Scholar 

  • Amer A, Mehlhorn H (2006b) Repellency effects of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes. Parasitol Res 99:478–490

    Article  PubMed  Google Scholar 

  • Amer A, Mehlhorn H (2006c) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477

    Article  PubMed  Google Scholar 

  • Angioni A, Barra A, Russo TM, Coroneo V, Dessi S, Cabras P (2003) Chemical composition of the essential oils of Juniperus from ripe and unripe berries and leaves and their antimicrobial activity. J Agric Food Chem 51:3073–3078

    Article  PubMed  Google Scholar 

  • Barnard DR (1999) Repellency of essential oils to mosquitoes (Diptera: Culicidae). J Med Entomol 36:625–629

    PubMed  CAS  Google Scholar 

  • Barrero AF, Herrador MM, Arteaga P, Quílez J, Akssira M, Mellouki F, Akkad S (2005) Chemical composition of the essential oils of leaves and wood of Tetraclinis articulata (Vahl). Masters J Essent Oil Res 17:166–168

    Article  Google Scholar 

  • Barrero AF, Herrador MM, Arteaga P, Quílez J, Sánchez-Fernádez E, Akssira M, Aitigri M, Mellouki F, Akkad S (2006) Chemical composition of the essential oils from leaves of Juniperus phoenicea L. from North Africa. J Essent Oil Res 18:168–169

    Article  CAS  Google Scholar 

  • Carroll JF, Tabanca N, Kramer M, Elejalde NM, Wedge DE, Bernier UR, Coy M, Becnel JJ, Demirci B, Başer KHC, Zhang J, Zhang S (2011) Essential oils of Cupressus funebris, Juniperus communis, and J. chinensis (Cupressaceae) as repellents against ticks (Acari: Ixodidae) and mosquitoes (Diptera: Culicidae) and as toxicants against mosquitoes. J Vector Ecol 36:258–268

    Article  PubMed  Google Scholar 

  • Chanegriha N, Baâliouamer A, Meklati BY, Bonvin JF, Alamercery S (1993) Chemical composition of Algerian Cypress essential oil. J Essent Oil Res 5:671–674

    Article  CAS  Google Scholar 

  • Chanegriha N, Baâliouamer A, Meklati BY, Chretien JR, Keravis G (1997) GC/MS leaf oil analysis of four Algerian Cypress species. J Essent Oil Res 9:555–599

    Article  CAS  Google Scholar 

  • Chantraine JM, Laurent D, Ballivian C, Saavedra G, Ibañez R, Vilaseca LA (1998) Insecticidal activity of essential oils on Aedes aegypti larvae. Phytother Res 12:350–354

    Article  CAS  Google Scholar 

  • Chéiraff I, Ben Jannet H, Hammami M, Khouja ML, Mighri Z (2007) Chemical composition and antimicrobial activity of essential oils of Cupressus arizonica Greene. Biochem Syst Ecol 35:813–820

    Article  Google Scholar 

  • Cheng SS, Chang HT, Lin CY, Chen PS, Huang CG, Chen WJ, Chang ST (2009a) Insecticidal activities of leaf and twig essential oils from Clausena excavata against Aedes aegypti and Aedes albopictus larvae. Pest Manag Sci 65:339–343

    Article  PubMed  CAS  Google Scholar 

  • Cheng SS, Huang CG, Chen YJ, Yu JJ, Chen WJ, Chang ST (2009b) Chemical compositions and larvicidal activities of leaf essential oils from two eucalyptus species. Biores Technol 100:452–456

    Article  CAS  Google Scholar 

  • Clem JR, Havemann DF, Raebel MA (1993) Insect repellent deet (N, N-diethyl-m-toluamide) cardiovascular toxicity in an adult. Ann Pharmacother 27:289–293

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Conti B, Benelli G, Flamini G, Cioni PL, Profeti R, Ceccarini L, Macchia M, Canale A (2012) Larvicidal and repellent activity of Hyptis suaveolens (Lamiaceae) essential oil against the mosquito Aedes albopictus Skuse (Diptera: Culicidae). Parasitol Res 110:2013–2021

    Article  PubMed  Google Scholar 

  • Curtis CF, Lines JD, Ijumba J, Callaghan A, Hill N, Karimzad MA (1987) The relative efficiency of repellents against mosquito vectors of disease. Med Vet Entomol 1:109–119

    Article  PubMed  CAS  Google Scholar 

  • Derwich E, Benziane Z, Boukir A (2010) Chemical composition of leaf essential oil of Juniperus phoenicea and evaluation of its antibacterial activity. Int J Agric Biol 12:199–204

    CAS  Google Scholar 

  • Dob T, Dahmane D, Chelghoum C (2008) Chemical composition of the essential oil of Juniperus phoenicea L. from Algeria. J Essent oil Res 20:15–20

    Article  CAS  Google Scholar 

  • Emami SA, Massoomi H, Maghadam MS, Asili J (2009) Identification of volatile oil components from aerial parts of Chamaecyparis lawsoniana by GC-MS and 13C-NMR methods. J Essent Oils Bear Plants 12:661–665

    CAS  Google Scholar 

  • Emami SA, Fakhrjafary M, Tafaghodi M, Hassanzadeh MK (2010) Chemical composition and antioxidant activities of the essential oils of different parts of Cupressus arizonica Greene. J Essent Oil Res 22:193–199, and references there in

    Article  CAS  Google Scholar 

  • Enserink M (2008) A mosquito goes global. Science 320:864–866

    Google Scholar 

  • Evergetis E, Michaelakis A, Haroutounian SA (2012) Essential oils of Umbelliferae (Apiaceae) family taxa as emerging potent agents for mosquito control. In: Larramendy ML, Soloneski S (eds) Integrated Pest Management and Pest Control – Current and Future Tactics, ISBN 978-953-307-926-4

  • Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London

    Google Scholar 

  • Fradin MS (1998) Mosquitoes and mosquito repellent: a clinician's guide. Ann Intern Med 128:931–940

    PubMed  CAS  Google Scholar 

  • Fradin MS, Day JF (2002) Comparative efficacy of insect repellents against mosquito bites. N Engl J Med 347:13–18

    Article  PubMed  CAS  Google Scholar 

  • Giatropoulos A, Michaelakis A, Koliopoulos G, Pontikakos CM (2012a) Records of Aedes albopictus and Aedes cretinus in Greece from 2009 to 2011. Hell Plant Prot J 5:49–56

    Google Scholar 

  • Giatropoulos Α, Emmanouel N, Koliopoulos G, Michaelakis A (2012b) A study on distribution and seasonal abundance of Aedes albopictus (Diptera: Culicidae) population in Athens, Greece. J Med Entomol 49:262–269

    Article  PubMed  Google Scholar 

  • Giatropoulos A, Papachristos DP, Kimbaris A, Koliopoulos G, Polissiou MG, Emmanouel N, Michaelakis A (2012c) 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

    Article  PubMed  Google Scholar 

  • Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I, Kurečić-Filipović S, Komparak S, Martić R, Đuričić S, Betica-Radić L, Okmadžić J, Vilibić-Čavlek T, Babić-Erceg A, Turković B, Avšić-Županc T, Radić I, Ljubić M, Šarac K, Benić N, Mlinarić-Galinović G (2011) Autochthonous dengue fever in Croatia, August–September 2010. Eurosurveillance 16:19805. Retrieved online from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19805. (last visit 29/11/2012)

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Grandadam M, Caro V, Plumet S, Thiberge M, Souarès Y, Failloux A, Hugues J, Budelot M, Cosserat D, Leparc-Goffart I, Desprès P (2011) Chikungunya Virus, Southeastern France. Emerging Infect Dis 17:910–913

    Article  PubMed  Google Scholar 

  • Gratz NG (2004) Critical review of the vector status of Aedes albopictus. Med Vet Entomol 18:215–222

    Article  PubMed  CAS  Google Scholar 

  • Gu HJ, Cheng SS, Lin CY, Huang CG, Chen WJ, Chang ST (2009) Repellency of essential oils of Cryptomeria japonica (Pinaceae) against adults of the mosquitoes Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Agric Food Chem 57:11127–11133

    Article  PubMed  CAS  Google Scholar 

  • Hemingway J, Field L, Vontas J (2002) An overview of insecticide resistance. Science 298:96–97

    Article  PubMed  CAS  Google Scholar 

  • Inc SPSS (2004) SPSS 14 for Windows user’s guide. SPSS Inc., Chicago

    Google Scholar 

  • Invasive Species Specialist Group (ISSG) (2009). Retrieved online from: http://www.issg.org/database/species/search.asp?st=100ss. (last visit 29/11/2012)

  • Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608

    Article  CAS  Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  PubMed  CAS  Google Scholar 

  • Kassir JT, Mohsen ZH, Mehdi NS (1989) Toxic effects of limonene against Culex quinquefasciatus Say larvae and its interference with oviposition. Anz Schädlingskde Pflanzenschutz Umweltschutz 62:19–21

    Article  Google Scholar 

  • Khan HAA, Akram W, Shehzad K, Shaalan EA (2011) First report of field evolved resistance to agrochemicals in dengue mosquito, Aedes albopictus (Diptera: Culicidae), from Pakistan. Parasit Vectors 4:146–156

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Wahab N, Warikoo R (2011a) Bioefficacy of Mentha piperita essential oil against dengue fever mosquito Aedes aegypti L. Asian Pac J Trop Biomed 1:85–88

    Article  Google Scholar 

  • Kumar P, Mishra S, Malik A, Satya S (2011b) Repellent, larvicidal and pupicidal properties of essential oils and their formulations against the housefly, Musca domestica. Med Vet Entomol 25:302–310

    Article  PubMed  CAS  Google Scholar 

  • La Ruche G, Souarès Y, Armengaud A, Peloux-Petiot F, Delaunay P, Desprès P, Lenglet A, Jourdain F, Leparc-Goffart I, Charlet F, Ollier L, Mantey K, Mollet T, Fournier JP, Torrents R, Leitmeyer K, Hilairet P, Zeller H, Van Bortel W, Dejour-Salamanca D, Grandadam M, Gastellu-Etchegorry M (2010) First two autochthonous dengue virus infections in metropolitan France, September 2010. Eurosurveillance 15:19676. Retrieved online from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19676. (last visit 29/11/2012)

  • Lee HS (2006) Mosquito larvicidal activity of aromatic medicinal plant oils against Aedes aegypti and Culex pipiens pallens. J Am Mosq Control Assoc 22:292–295

    Article  PubMed  Google Scholar 

  • Lim JD, Chung IM, Moon HI (2011) Immunotoxicity activity from various organic solvents extract of Allium genus from South Korea against Aedes aegypti L. Immunopharm Immunot 33:484–487

    Article  CAS  Google Scholar 

  • Louis C (2012) Daily newspaper view of Dengue fever epidemic, Athens, Greece, 1927–1931. Emerg Infect Dis 18:78–82

    Article  PubMed  Google Scholar 

  • Maia MF, Moore SJ (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malar J 10(Suppl 1):S11

    Article  PubMed  CAS  Google Scholar 

  • Malizia RA, Cardell DA, Molli JS, González S, Guerra PE, Grau RJ (2000) Volatile constituents of leaf oils from the Cupressaceae family: part I. Cupressus macrocarpa Hartw., C. arizonica Greene and C. torulosa Don species growing in Argentina. J Essent Oil Res 12:59–63

    Article  CAS  Google Scholar 

  • Mazari K, Bendimerad N, Bekhechi C, Fernadez X (2010) Chemical composition and antimicrobial activity of essential oils isolated from Algerian Juniperus phoenicea L. and Cupressus sempervirens L. J Med Plant Res 4:959–964

    CAS  Google Scholar 

  • Michaelakis A, Papachristos D, Kimbaris A, Koliopoulos G, Giatropoulos A, Polissiou MG (2009) Citrus essential oils and four enantiomeric pinenes against Culex pipiens (Diptera: Culicidae). Parasitol Res 105:769–773

    Article  PubMed  Google Scholar 

  • Milos M, Radonic A, Mastelic J (2002) Seasonal variation in essential oil composition of Cupressus sempervirens L. J Essent Oil Res 14:222–223

    Article  CAS  Google Scholar 

  • Moore M (1993) Cupressus L. In: Tutin TG, Burges NA, Chater AO, Edmondson GR, Heywood WH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europea 1. Cambridge University Press, Cambridge, pp 45–48

    Google Scholar 

  • Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378

    Article  PubMed  CAS  Google Scholar 

  • Newall CA, Anderson LA, Phillipson JD (1996) Herbal Medicines: A guide for Health-Care Proffessionals. The Pharmaceutical Press, London, pp 176–177

    Google Scholar 

  • Papachristos DP, Stamopoulos DC (2002) Repellent, toxic and reproduction inhibitory effects of essential oil vapours on Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). J Stored Prod Res 38:117–128

    Article  CAS  Google Scholar 

  • Papachristos DP, Karamanoli KI, Stamopoulos DC, Menkissoglu-Spiroudi U (2004) The relationship between the chemical composition of three essential oils and their insecticidal activity against Acanthoscelides obtectus (Say). Pest Manag Sci 60:514–520

    Article  PubMed  CAS  Google Scholar 

  • Perumalsamy H, Kim NJ, Ahn YJ (2009) Larvicidal activity of compounds isolated from Asarum heterotropoides against Culex pipiens pallens, Aedes aegypti, and Ochlerotatus togoi (Diptera: Culicidae). J Med Entomol 46:1420–1423

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pohlit AM, Rezende AR, Baldin ELL, Lopes NP, Neto VFA (2011) Plant extracts, isolated phytochemicals, and plant-derived agents which are lethal to arthropod vectors of human tropical diseases—a review. Planta Med 77:618–630

    Article  PubMed  CAS  Google Scholar 

  • Prajapati V, Tripathi AK, Aggarwal KK, Khanuja SPS (2005) Insecticidal, repellent and oviposition-deterrent activity of selected essential oils against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Bioresour Technol 96:1749–1757

    Article  PubMed  CAS  Google Scholar 

  • Qiu H, Jun HW, McCall JW (1998) Pharmacokinetics, formulation, and safety of insect repellent N, N diethyl-3-methylbenzamide (deet): a review. J Am Mosq Control Assoc 14:12–27

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A (2007) Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840–1846

    Article  PubMed  CAS  Google Scholar 

  • Santos SRL, Melo MA, Cardoso AV, Santos RLC, Sousa DP, Cavalcanti SCH (2011) Structure–activity relationships of larvicidal monoterpenes and derivatives against Aedes aegypti Linn. Chemosphere 84:150–153

    Article  PubMed  CAS  Google Scholar 

  • Sedaghat MM, Dehkordi AS, Khanavi M, Abai MR, Mohtarami F, Vatandoost H (2011) Chemical composition and larvicidal activity of essential oil of Cupressus arizonica E.L. Greene against malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Pharmacogn Res 3:135–139

    Article  CAS  Google Scholar 

  • Semmler M, Abdel-Ghaffar F, Al-Rasheid K, Mehlhorn H (2009) Nature helps: from research to products against blood-sucking arthropods. Parasitol Res 105:1483–1487

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sukumar K, Perich MJ, Boobar LR (1991) Botanical derivatives in mosquito control: a review. J Am Mosq Control Assoc 7:210–237

    PubMed  CAS  Google Scholar 

  • Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res 19:303–309

    Article  PubMed  CAS  Google Scholar 

  • Tumen I, Hafizoglu H, Pranovich A, Reunanen M (2010) Chemical constituents of cones and leaves of cypress (Cupressus sempervirens L.) grown in Turkey. Fresen Environ Bul 19:2268–2276

    CAS  Google Scholar 

  • Vourlioti-Arapi F, Michaelakis A, Evergetis E, Koliopoulos G, Haroutounian SA (2012) Essential oils of indigenous in Greece six Juniperus taxa: chemical composition and larvicidal activity against the West Nile virus vector Culex pipiens. Parasitol Res 110:1829–1839

    Article  PubMed  CAS  Google Scholar 

  • 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

Download references

Acknowledgments

The authors would like to thank Prof. B. Galatis (J. & A. N. Diomedes Botanic Garden, University of Athens) for providing the plant material and Dr. I. Vallianatou (J. & A. N. Diomedes Botanic Garden, University of Athens) for the collection and plant identification.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Olga Tzakou or Antonios Michaelakis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Giatropoulos, A., Pitarokili, D., Papaioannou, F. et al. Essential oil composition, adult repellency and larvicidal activity of eight Cupressaceae species from Greece against Aedes albopictus (Diptera: Culicidae). Parasitol Res 112, 1113–1123 (2013). https://doi.org/10.1007/s00436-012-3239-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3239-5

Keywords

Navigation