Eugenol, α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors

Abstract

Mosquito-borne diseases represent a deadly threat for millions of people worldwide. Eco-friendly mosquitocides are a priority. In Ayurvedic medicine, Plectranthus species have been used to treat heart disease, convulsions, spasmodic pain and painful urination. In this research, we evaluated the acute toxicity of essential oil from Plectranthus barbatus and its major constituents, against larvae of the malaria vector Anopheles subpictus, the dengue vector Aedes albopictus and the Japanese encephalitis vector Culex tritaeniorhynchus. The chemical composition of P. barbatus essential oil was analyzed by gas chromatography–mass spectroscopy. Nineteen components were identified. Major constituents were eugenol (31.12 %), α-pinene (19.38 %) and β-caryophyllene (18.42 %). Acute toxicity against early third-instar larvae of An. subpictus, Ae. albopictus and Cx. tritaeniorhynchus was investigated. The essential oil had a significant toxic effect against larvae of An. subpictus, Ae. albopictus and Cx. tritaeniorhynchus, with 50 % lethal concentration (LC50) values of 84.20, 87.25 and 94.34 μg/ml and 90 % lethal concentration (LC90) values of 165.25, 170.56 and 179.58 μg/ml, respectively. Concerning major constituents, eugenol, α-pinene and β-caryophyllene appeared to be most effective against An. subpictus (LC50 = 25.45, 32.09 and 41.66 μg/ml, respectively), followed by Ae. albopictus (LC50 = 28.14, 34.09 and 44.77 μg/ml, respectively) and Cx. tritaeniorhynchus (LC50 = 30.80, 36.75 and 48.17 μg/ml, respectively). Overall, the chance to use metabolites from P. barbatus essential oil against mosquito vectors seems promising, since they are effective at low doses and could be an advantageous alternative to build newer and safer mosquito control tools.

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

Fig. 1
Fig. 2

References

  1. Ajaiyeoba EO, Sama W, Essien EE, Olayemi JO, Ekundayo O, Walker TM, Setzer WN (2008) Larvicidal activity of turmerone-rich essential oils of Curcuma longa leaf and rhizome from Nigeria on Anopheles gambiae. Pharm Biol 46:279–282

    Article  CAS  Google Scholar 

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

  3. Amer A, Mehlhorn H (2006b) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499

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

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

  6. Ammon HP, Kemper FH (1982) Ayurveda: 300 years of Indian traditional medicine. Med Welt 33:148–153

    CAS  PubMed  Google Scholar 

  7. Ammon HP, Muller AB (1985) Forskolin: from an ayurvedic remedy to a modern agent. Planta Med 6:473–477

    Article  PubMed  Google Scholar 

  8. Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805

    Article  PubMed  Google Scholar 

  9. Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114(9):3201–3212

    Article  PubMed  Google Scholar 

  10. Benelli G (2016) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res. doi:10.1007/s00436-015-4800-9

  11. Benelli G, Bedini S, Cosci F, Toniolo C, Conti B, Nicoletti M (2015a) Larvicidal and ovideterrent properties of neem oil and fractions against the filariasis vector Aedes albopictus (Diptera: Culicidae): a bioactivity survey across production sites. Parasitol Res 114:227–236

    Article  PubMed  Google Scholar 

  12. Benelli G, Bedini S, Flamini G, Cosci F, Cioni PL, Amira S, Benchikh F, Laouer H, Di Giuseppe G, Conti B (2015b) Mediterranean essential oils as effective weapons against the West Nile vector Culex pipiens and the Echinostoma intermediate host Physella acuta: what happens around? An acute toxicity survey on non-target mayflies. Parasitol Res 114(3):1011–1021

    Article  PubMed  Google Scholar 

  13. Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015c) Old ingredients for a new recipe? Neemcake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol Res 114:391–397

    Article  PubMed  Google Scholar 

  14. Cheng S, Liu J, Tsai K, Chen W, Chang S (2004) Chemical composition and mosquito larvicidal activity of essential oils from leaves of different Cinnamomum osmophloeum provenances. J Agric Food Chem 52:4395–4400

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Choi W, Park B, Ku S, Lee S (2002) Repellent activity of essential oils and monoterpenes against Culex pipiens pallens. J Am Mosq Control Assoc 18:348–351

    CAS  PubMed  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. Conti B, Canale A, Cioni PL, Flamini G, Rifici A (2011) Hyptis suaveolens and Hyptis spicigera (Lamiaceae) essential oils: qualitative analysis, contact toxicity and repellent activity against Sitophilus granarius (L.) (Coleoptera: Dryophthoridae). J Pest Sci 84:219–228

    Article  Google Scholar 

  19. 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 

  20. Dharmagadda VSS, Naik SN, Mittal PK, Vasudevan P (2005) Larvicidal activity of Tagetes patula essential oil against three mosquito species. Bioresour Technol 96(11):1235–1240

    Article  CAS  PubMed  Google Scholar 

  21. Finney DJ (1971) Probit analysis. Cambridge University Press, London, pp 68–72

    Google Scholar 

  22. 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 Pac J Trop Med 3(11):874–877

    Article  CAS  Google Scholar 

  23. Govindarajan M (2013) Chemical composition and mosquitocidal potential of Mentha spicata (Linn.) essential. In: Govil JN, Bhattacharya S (eds) Recent progress in medicinal plants: essential oil III and phytopharmacology. Studium, USA, pp 153–172

    Google Scholar 

  24. Govindarajan M, Sivakumar R (2014) Larvicidal, ovicidal, and adulticidal efficacy of Erythrina indica (Lam.) (family: Fabaceae) against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 113(2):777–791

    Article  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. Govindarajan M, Sivakumar R, Rajeswary M, Yogalakshmi K (2013a) Chemical composition and larvicidal activity of essential oil from Ocimum basilicum (L.) against Culex tritaeniorhynchus, Aedes albopictus and Anopheles subpictus (Diptera: Culicidae). Exp Parasitol 134:7–11

    Article  CAS  PubMed  Google Scholar 

  27. Govindarajan M, Sivakumar R, Rajeswary M, Veerakumar K (2013b) Mosquito larvicidal activity of thymol from essential oil of Coleus aromaticus Benth. against Culex tritaeniorhynchus, Aedes albopictus and Anopheles subpictus (Diptera: Culicidae). Parasitol Res 112(11):3713–3721

    Article  PubMed  Google Scholar 

  28. Jaenson TGT, Palsson K, Borg-Karlson AK (2006) Evaluation of extracts and oils of mosquito (Diptera: Culicidae) repellent plants from Sweden and Guinea-Bissau. J Med Entomol 43:113–119

    Article  CAS  PubMed  Google Scholar 

  29. Keiser J, Maltese MF, Erlanger TE, Bos R, Tanner M, Singer BH, Utzinger J (2005) Effect of irrigated rice agriculture on Japanese encephalitis, including challenges and opportunities for integrated vector management. Acta Trop 95:40–57

    Article  PubMed  Google Scholar 

  30. Kiran SR, Bhavani K, Devi PS, Rao BRR, Reddy KJ (2006) Composition and larvicidal activity of leaves and stem essential oils of Chloroxylon swietenia DC against Aedes aegypti and Anopheles stephensi. Bioresour Technol 97(18):2481–2484

    Article  CAS  Google Scholar 

  31. Kweka EJ, Senthilkumar A, Venkatesalu V (2012) Toxicity of essential oil from Indian borage on the larvae of the African malaria vector mosquito, Anopheles gambiae. Parasit Vect 5:277

    Article  Google Scholar 

  32. Lin CF, Wan SW, Cheng HJ, Lei HY, Lin YS (2006) Autoimmune pathogenesis in dengue virus infection. Viral Immunol 19:127–132

    Article  CAS  PubMed  Google Scholar 

  33. Medhi SM, Reza SDA, Mahnaz K, Reza AM, Abbas H, Fatemeh M, Hassan V (2010) Phytochemistry and larvicidal activity of Eucalyptus camaldulensis against malaria vector, Anopheles stephensi. Asian Pac J Trop Med 3:841–845

    Article  CAS  Google Scholar 

  34. Mehlhorn H (2011) Nature helps. How plants and other organisms contribute to solve health problems, Parasitology Research Monographs. Springer, Berlin, pp 1–372

    Google Scholar 

  35. Mehlhorn H, Schmahl G, Schmidt J (2005) Extract of the seeds of the plant Vitex agnus castus proven to be highly efficacious as a repellent against ticks, fleas, mosquitoes and biting flies. Parasitol Res 95:363–365

    Article  PubMed  Google Scholar 

  36. Mehlhorn H, Al-Rasheid KAS, Al-Quraishy S, Abdel-Ghaffar F (2012) Research and increase of expertise in arachno-entomology are urgently needed. Parasitol Res 110:259–265

    Article  PubMed  Google Scholar 

  37. Murugan K, Vadivalagan C, Karthika P, Panneerselvam C, Paulpandi M, Subramaniam J,Wei H, Al Thabiani A, Saleh Alsalhi M, Devanesan S, Nicoletti M, Paramasivan R, Parajulee MN, Benelli G (2016) DNA barcoding and molecular evolution of mosquito vectors of medical and veterinary importance. Parasitol Res. doi:10.1007/s00436-015-4726-2

  38. Nathan SS (2007) The use of Eucalyptus tereticornis Sm. (Myrtaceae) oil (leaf extract) as a natural larvicidal agent against the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Bioresour Technol 98(9):1856–1860

    Article  CAS  Google Scholar 

  39. Okumu FO, Knols BGJ, Fillinger U (2007) Larvicidal effects of a neem (Azadirachta indica) oil formulation on the malaria vector Anopheles gambiae. Malar J 6:63

    PubMed Central  Article  PubMed  Google Scholar 

  40. Othira JO, Onek LA, Deng LA, Omolo EO (2009) Insecticidal potency of H. spicigera preparations against Sitophilus zeamais (L.) and Tribolium castaneum (Herbst) on stored maize grains. Afr J Agric Res 4:187–192

    Google Scholar 

  41. Papachristos DP, Stamopoulos DC (2003) Selection of Acanthoscelides obtectus (Say) for resistance to lavender essential oil vapour. J Stored Prod Res 39:433–441

    Article  CAS  Google Scholar 

  42. Pavela R (2015a) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187

    Article  CAS  Google Scholar 

  43. Pavela R (2015b) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitol Res 114(10):3835–3853

    Article  PubMed  Google Scholar 

  44. Pavela R, Kaffkova K, Kumsta M (2014) Chemical composition and larvicidal activity of essential oils from different Mentha L. and Pulegium species against Culex quinquefasciatus Say (Diptera: Culicidae). Plant Prot Sci 50:36–42

    CAS  Google Scholar 

  45. Pohilt AM, Rezende AR, Lopes Baldin EL, Lopes NP, de Andrade Neto VF (2011) Plant extracts, isolated phytochemicals, and plant-derived agents which are lethal to arthropod vectors of human tropical diseases—a review. Planta Med 77(6):618–630

    Article  Google Scholar 

  46. Prajapati V, Tripathi AK, Aggrawal 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  CAS  PubMed  Google Scholar 

  47. Rajkumar S, Jebanesan A (2010) Chemical composition and larvicidal activity of leaf essential oil from Clausena dentata (Willd) M. Roam. (Rutaceae) against the chikungunya vector, Aedes aegypti Linn. (Diptera: Culicidae). J Asia Pac Entomol 13:107–109

    Article  CAS  Google Scholar 

  48. Ravi V, Vanajakshi S, Gowda A, Chandramuki A (1989) A laboratory diagnosis of Japanese encephalitis using monoclonal antibodies and correlation of findings with the outcome. J Med Virol 29:221–223

    Article  CAS  PubMed  Google Scholar 

  49. 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  CAS  PubMed  Google Scholar 

  50. Santos GKN, Dutra KA, Barros RA, da Camara CAG, Lira DD, Gusmao NB, Navarro DMAF (2012) Essential oils from Alpinia purpurata (Zingiberaceae): chemical composition, oviposition deterrence, larvicidal and antibacterial activity. Ind Crop Prod 40:254–260

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  52. Senthilkumar A, Venkatesalu V (2010) Chemical composition and larvicidal activity of the essential oil of Plectranthus amboinicus (Lour.) Spreng against Anopheles stephensi; a malarial vector mosquito. Parasitol Res 107:1275–1278

    Article  PubMed  Google Scholar 

  53. Sujitha V, Murugan K, Paulpandi M, Panneerselvam C, Suresh U, Roni M, Nicoletti M, Higuchi A, Madhiyazhagan P, Subramaniam J, Dinesh D, Vadivalagan C, Chandramohan B, Alarfaj AA, Munusamy MA, Barnard DR, Benelli G (2015) Green-synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti. Parasitol Res 114(9):3315–3325

    Article  PubMed  Google Scholar 

  54. Suman DS, Shrivastava AR, Parashar BD, Pant SC, Agrawal OP, Prakash S (2008) Scanning electron microscopic studies on egg surface morphology and morphometrics of Culex tritaeniorhynchus and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 104:173–176

    Article  CAS  PubMed  Google Scholar 

  55. Tiwary M, Naik SN, Tewaryb DK, Mittalc PK, Yadavc S (2007) Chemical composition and larvicidal activities of the essential oil of Zanthoxylum armatum DC (Rutaceae) against three mosquito vectors. J Vector Borne Dis 44:198–204

    CAS  PubMed  Google Scholar 

  56. Traboulsi AF, Taoubi K, El-Haj S, Bessiere JM, Ramal S (2002) Insecticidal properties of essential plant oils against the mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Manag Sci 58:491–495

    Article  CAS  PubMed  Google Scholar 

  57. Wattanachai P, Tintanon B (1999) Resistance of Aedes aegypti to chemical compounds in aerosol insecticide products in different areas of Bangkok, Thailand. Commun Dis J 25:188–191

    Google Scholar 

  58. WHO (2015) Dengue and severe dengue. World Health Organization, Geneva, Fact sheet No. 117

    Google Scholar 

  59. World Health Organization (2005) Guidelines for laboratory and field testing of mosquito larvicides. Communicable disease control, prevention and eradication, WHO pesticide evaluation scheme. WHO, Geneva, WHO/CDS/WHOPES/GCDPP/1.3

  60. World Health Organization (2014) A global brief on vector-borne diseases. WHO/DCO/WHD/2014.1

  61. Zahran HEM, Abdelgaleil SAM (2011) Insecticidal and developmental inhibitory properties of monoterpenes on Culex pipiens L. (Diptera: Culicidae). J Asia Pac Entomol 14:46–51

    Article  CAS  Google Scholar 

  62. Zhu L, Tian Y (2011) Chemical composition and larvicidal activity of Blumea densiflora essential oils against Anopheles anthropophagus: a malarial vector mosquito. Parasitol Res 109:1417–1422

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the professor and head of the Department of Zoology, Annamalai University, for the laboratory facilities provided. We also acknowledge the cooperation of the staff members of the VCRC (ICMR), Pondicherry.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Marimuthu Govindarajan or Giovanni Benelli.

Ethics declarations

All applicable international and national guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Conflict of interest

The authors declare no conflicts of interest. Giovanni Benelli is an Editorial Board Member of Parasitology Research. This does not alter the authors’ adherence to all the Parasitology Research policies on sharing data and materials.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Govindarajan, M., Rajeswary, M., Hoti, S.L. et al. Eugenol, α-pinene and β-caryophyllene from Plectranthus barbatus essential oil as eco-friendly larvicides against malaria, dengue and Japanese encephalitis mosquito vectors. Parasitol Res 115, 807–815 (2016). https://doi.org/10.1007/s00436-015-4809-0

Download citation

Keywords

  • Aedes albopictus
  • Anopheles subpictus
  • Culex tritaeniorhynchus
  • Culicidae
  • GC-MS
  • Mosquito-borne diseases
  • Plant-borne larvicides