Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10218–10227 | Cite as

Towards green oviposition deterrents? Effectiveness of Syzygium lanceolatum (Myrtaceae) essential oil against six mosquito vectors and impact on four aquatic biological control agents

  • Giovanni BenelliEmail author
  • Mohan Rajeswary
  • Marimuthu GovindarajanEmail author
Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology


Essential oils (EOs) from plants may be alternative sources of molecules toxic against mosquito vectors of public health relevance. Most of researches in this field focused on EOs as larvicides or ovicides, while limited efforts focused on the exploitation of EOs as oviposition deterrents. In the present study, the larvicidal and oviposition deterrent activity of Syzygium lanceolatum leaf EO was evaluated against six mosquito species, Anopheles stephensi, An. subpictus, Aedes aegypti, Ae. albopictus, Culex quinquefasciatus, and Cx. tritaeniorhynchus. The chemical composition of the S. lanceolatum EO was analyzed by GC-MS analysis, showing the presence of phenyl propanal, β-caryophyllene, α-humulene, and caryophyllene oxide as major constituents. S. lanceolatum EO showed high acute toxicity on An. stephensi (LC50 = 51.20 μg/ml), Ae. aegypti (LC50 = 55.11 μg/ml), Cx. quinquefasciatus (LC50 = 60.01 μg/ml), An. subpictus (LC50 = 61.34 μg/ml), Ae. albopictus (LC50 = 66.71 μg/ml), and Cx. tritaeniorhynchus (LC50 = 72.24 μg/ml) larvae. Furthermore, the EO was effective as oviposition deterrent against the six tested mosquito species, with OAI on An. stephensi, An. subpictus, Ae. aegypti, Ae. albopictus, Cx. quinquefasciatus, and Cx. tritaeniorhynchus reaching −0.83, −0.81, −0.84, −0.83, −0.84, and −0.86, respectively. The toxicity of S. lanceolatum EO against several biological control agents of mosquitoes, including water bugs (Anisops bouvieri and Diplonychus indicus) and fishes (Gambusia affinis and Poecilia reticulata), was extremely low, with LC50 ranging between 4148 and 15,762 μg/ml. Overall, our results pointed out the promising potential of the S. lanceolatum leaf EO as a source of environmental-friendly oviposition deterrents and larvicides effective against a wide number of mosquito species of importance for parasitology.


Biosafety Dengue Filariasis Japanese encephalitis Larvicides Malaria Zika virus 



The authors are grateful to the Professor and Head of the Department of Zoology, Annamalai University for the laboratory provisions granted.

Compliance with ethical standards

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.


G. Benelli is sponsored by PROAPI (PRAF 2015) and University of Pisa, Department of Agriculture, Food and Environment (Grant ID: COFIN2015_22). Funders had no role in the study design, data collection and analyses, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corporation, Carol StreamGoogle Scholar
  2. Ahmed F, Chandra JNNS, Timmaiah NV (2009) An in vitro study on the inhibitory activities of Eugenia jambolana seeds against carbohydrate hydrolyzing enzymes. J Young Pharm 1(4):327–331CrossRefGoogle Scholar
  3. Autran ES, Neves IA, Silva CSB, Santos GKN, Câmara CAG, Navarro DMAF (2009) Chemical composition, oviposition deterrent and larvicidal activity against Aedes aegypti of essential oils from Piper marginatum Jacq. (Piperaceae). Bioresour Technol 100:2284–2288CrossRefGoogle Scholar
  4. Ayyanar M, Subash-Babu P (2012) Syzygium cumini (L.) Skeels: a review of its phytochemical constituents and traditional uses. Asian Pac J Trop Biomed 2(3):240–246CrossRefGoogle Scholar
  5. Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805CrossRefGoogle Scholar
  6. Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114:3201–3212CrossRefGoogle Scholar
  7. Benelli G (2015c) The best time to have sex: mating behavior and effect of daylight time on male sexual competitiveness in the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae). Parasitol Res 114:887–894CrossRefGoogle Scholar
  8. Benelli G (2016a) Spread of Zika virus: the key role of mosquito vector control. Asian Pac J Trop Biomed 6:468–471CrossRefGoogle Scholar
  9. Benelli G (2016b) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115:23–34CrossRefGoogle Scholar
  10. Benelli G (2016c) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer – a brief review. Enzym Microb Technol. doi: 10.1016/j.enzmictec.2016.08.022 Google Scholar
  11. Benelli G, Govindarajan M (2016) Green-synthesized mosquito oviposition attractants and ovicides: towards a nanoparticle-based "lure and kill" approach? J Clust Sci. doi: 10.1007/s10876-016-1088-6 Google Scholar
  12. Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754CrossRefGoogle Scholar
  13. Benelli G, Flamini G, Canale A, Molffeta I, Cioni PL, Conti B (2012) Repellence of Hyptis suaveolens whole essential oil and, major constituents against adults of the granary weevil Sitophilus granarius. Bull Insect 65:177–183Google Scholar
  14. Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015) Old ingredients for a new recipe? Neem cake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol Res 114:391–397CrossRefGoogle Scholar
  15. Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016a) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115:2131–2137CrossRefGoogle Scholar
  16. Benelli G, Pavela R, Canale A, Mehlhorn H (2016b) Tick repellents and acaricides of botanical origin: a green roadmap to control tick-borne diseases? Parasitol Res 115:2545–2560CrossRefGoogle Scholar
  17. Bezerra-Silva PC et al (2016) Evaluation of the activity of the essential oil from an ornamental flower against Aedes aegypti: electrophysiology, molecular dynamics and behavioral assays. PLoS One 11:e0150008CrossRefGoogle Scholar
  18. Bhuiyan NI, Begum J, Nandi NC, Akter F (2010) Constituents of the essential oil from leaves and buds of clove (Syzigium caryophyllatum (L.) Alston). African J Plant Sci 4(11):451–454Google Scholar
  19. Boulos L (1983) Medicinal plants of North Africa. Reference publications, AlgonacGoogle Scholar
  20. Chaubey MK (2012) Responses of Tribolium castaneum (Coleoptera: Tenebrionidae) and Sitophilus oryzae (Coleoptera: Curculionidae) against essential oils and pure compounds. Herba Pol 58:33–45Google Scholar
  21. Cheng SS, Liu JY, Tsai KH, Chen WJ, Chang ST (2004) Chemical composition and mosquito larvicidal activity of essential oils from leaves of different Cinnamomum osmophloeum provenances. J Agric Food Chem 52:4395–4400CrossRefGoogle Scholar
  22. Cheng SS, Liu JY, Huang CG, Hsui YR, Chen WJ, Chang ST (2009) Insecticidal activities of leaf essential oils from Cinnamomum osmophloeum against three mosquito species. Bioresour Technol 100:457–464CrossRefGoogle Scholar
  23. 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 107:1455–1461CrossRefGoogle Scholar
  24. Da Silva RCS, Milet-Pinheiro P, Bezerra da Silva PC, da Silva AG, da Silva MV, Navarro DMAF, Silva NH (2015) (E)-Caryophyllene and α-humulene: Aedes aegypti oviposition deterrents elucidated by gas chromatography-electrophysiological assay of Commiphora leptophloeos leaf oil. PLoS One 9:1–14Google Scholar
  25. Deo PG, Hasan SB, Majumdar SK (1988) Toxicity and suitability of some insecticides for household use. Int Pest Control 30:118–129Google Scholar
  26. Elango G, Rahuman AA, Kamaraj C, Zahir AA, Bagavan A (2010) Studies on effects of indigenous plant extracts on filarial vector Culex tritaeniorhynchus Giles. Parasitol Res 107:167–176CrossRefGoogle Scholar
  27. Finney DJ (1971) Probit analysis. Cambridge University Press, London, pp. 68–72Google Scholar
  28. Gamble JS, Fischer CEC (1923) Flora of the presidency of madras, vol I–III. Adlard and Son, London, pp. 1915–1935Google Scholar
  29. Govindarajan M, Benelli G (2016a) Eco-friendly larvicides from Indian plants: effectiveness of lavandulyl acetate and bicyclogermacrene on malaria, dengue and Japanese encephalitis mosquito vectors. Ecotox Environ Saf 133:395–402CrossRefGoogle Scholar
  30. Govindarajan M, Benelli G (2016b) α-humulene and β-elemene from Syzygium zeylanicum (Myrtaceae) essential oil: highly effective and eco-friendly larvicides against Anopheles subpictus, Aedes albopictus and Culex tritaeniorhynchus (Diptera: Culicidae). Parasitol Res 115:2771–2778CrossRefGoogle Scholar
  31. Govindarajan M, Benelli G (2016c) Artemisia absinthium-borne compounds as novel larvicides: effectiveness against six mosquito vectors and acute toxicity on non-target aquatic organisms. Parasitol Res. doi: 10.1007/s00436-016-5257-1 Google Scholar
  32. Govindarajan M, Rajeswary M, Benelli G (2016a) Chemical composition, toxicity and effects on non-target organisms of Pinus kesiya essential oil: an eco-friendly larvicide against mosquito vectors. Ecotox Environ Safe 129:85–90CrossRefGoogle Scholar
  33. Govindarajan M, Rajeswary M, Hoti SL, Bhattacharyya A, Benelli G (2016b) 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 115:807–815CrossRefGoogle Scholar
  34. Govindarajan M, Rajeswary M, Benelli G (2016c) δ-Cadinene, Calarene and δ-4-Carene from Kadsura heteroclita essential oil as novel larvicides against malaria, dengue and filariasis mosquitoes. Comb Chem High Throughput Screen 19(7):565–571CrossRefGoogle Scholar
  35. Govindarajan M, Rajeswary M, Arivoli S, Samuel T, Benelli G (2016d) Larvicidal and repellent potential of Zingiber nimmonii (J. Graham) Dalzell (Zingiberaceae) essential oil: an eco-friendly tool against malaria, dengue and lymphatic filariasis mosquito vectors? Parasitol Res 115(5):1807–1816CrossRefGoogle Scholar
  36. Govindarajan M, Shine K, Naiyf S, Alharbi NS, Benelli G (2016e) 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. doi: 10.1007/s11356-016-7568-2
  37. Gurib-Fakim A (2006) Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol Asp Med 27:1–93CrossRefGoogle Scholar
  38. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391CrossRefGoogle Scholar
  39. Isman MB (2008) Botanical insecticides: for richer, for poorer. Pest Manag Sci 64:8–11CrossRefGoogle Scholar
  40. Khandagle AJ, Tare VS, Raut KD, Morey RA (2011) Bioactivity of essential oils of Zingiber officinalis and Achyranthes aspera against mosquitoes. Parasitol Res 109:339–343CrossRefGoogle Scholar
  41. Kim H, Chen F, Wu C, Wang X, Chung H, Jin Z (2004) Evaluation of antioxidant activity of Australian tea tree (Melaleuca alternifolia) oil and its components. J Agric Food Chem 52:2849–2854CrossRefGoogle Scholar
  42. Komalamisra Y, Trongtokit Y, Rongsriyam Y, Apiwathnasorn C (2005) Screening for larvicidal activity in some Thai plants against four mosquito vector species. Southeast Asian J Trop Med 36(6):1412–1422Google Scholar
  43. Kramer WL, Mulla MS (1979) Oviposition attractants and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environ Entomol 8:1111–1114CrossRefGoogle Scholar
  44. Lee S, Najiah M, Wendy W, Nadirah M (2009) Chemical composition and antimicrobial activity of the essential oil of Syzygium aromaticum flower bud (clove) against fish systemic bacteria isolated from aquaculture sites. Front Agric China 3(3):332–336CrossRefGoogle Scholar
  45. Mabberly DJ (1997) The plant book. A portable dictionary of the vascular plants, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  46. Mahmoud II, Marzouk MS, Moharram FA, El-Gindi MR, Hassan AM (2001) Acylated flavonal glycoside from Eugenia jambolana leaves. Phytochemistry 58(8):1239–1244CrossRefGoogle Scholar
  47. Maisuthisakul P, Suttajit M, Pongsawatmanit R (2007) Assessment of phenolic content and free radical-scavenging capacity of some Thai indigenous plants. Food Chem 100:1409–1418CrossRefGoogle Scholar
  48. Mehlhorn H (ed) (2015) Encyclopedia of parasitology, 4th edn. Springer, New York 893Google Scholar
  49. Mendonca FAC, Silva KFS, Santos KK, Ribeiro JKAL, Sant'Ana AEG (2005) Activities of some Brazilian plants against larvae of the mosquito Aedes aegypti. Fitoterapia 76:629–636CrossRefGoogle Scholar
  50. Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115:1363–1373CrossRefGoogle Scholar
  51. Nascimento JC et al (2013) Larvicidal activities and chemical composition of essential oils from Piper klotzschianum (Kunth) C. DC. (Piperaceae). Pest Manag Sci 69:1267–1271Google Scholar
  52. Nassar MI, Gaara AH, El-Ghorab AH, Farrag A-RH, Hui Shen H, Huq E, Mabry TJ (2007) Chemical constituents of clove (Syzygium aromaticum, fam. Myrtaceae) and their antioxidant activity. Rev Latinoam Quim 35(3):47–57Google Scholar
  53. Noudogbessi JP, Yedomonhan P, Sohounhloue DCK, Chalchat JC, Figueredo G (2008) Chemical composition of essential oil of Syzygium guineense (Willd.) DC. Var. Guineense (Myrtaceae) from Benin. Rec Nat Prod 2(2):33–38Google Scholar
  54. Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187CrossRefGoogle Scholar
  55. Pavela R, Benelli G (2016a) Ethnobotanical knowledge on botanical repellents employed in the African region against mosquito vectors - a review. Exp Parasitol 167:103–108CrossRefGoogle Scholar
  56. Pavela R, Benelli G (2016b) Essential oils as eco-friendly biopesticides? Challenges and constraints. Tr Plant Sci. doi: 10.1016/j.tplants.2016.10.005 Google Scholar
  57. Pavela R, Canale A, Mehlhorn H, Benelli G (2016) Application of ethnobotanical repellents and acaricides in prevention, control and management of livestock ticks: a review. Res Vet Sci 109:1–9CrossRefGoogle Scholar
  58. Prajapati V, Tripathi AK, Aggarwal KK, Khanuja SPS (2005) Insecticidal, repellent and oviposition-deterrent activity of selected essential oil against Anopheles stephensis, Aedes aegypti and Culex quinquefasciatus. Bioresour Technol 96:1749–1757CrossRefGoogle Scholar
  59. Rajaganesh R, Murugan K, Panneerselvam C, Jayashanthini S, Aziz AT, Roni M, Suresh U, Trivedi S, Rehman H, Higuchi A, Nicoletti M, Benelli G (2016) Fern-synthesized silver nanocrystals: towards a new class of mosquito oviposition deterrents? Res Vet Sci 109:40–51Google Scholar
  60. Raina VK, Srivastava SK, Aggarwal KK, Syamasundar KV, Kumar S (2001) Essential oil composition of Syzygium aromaticum leaf from little Andaman India. Flavour Frag J 16(5):334–336CrossRefGoogle Scholar
  61. Ravi Kiran S, Bhavani K, Sita Devi P, Rajeswara Rao BR, Janardhan Reddy K (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):2481–2484CrossRefGoogle Scholar
  62. Reynertson KA, Basile MJ, Kennelly EJ (2005) Antioxidant potential of seven myrtaceous fruits. Ethnobot Res Appl 3:25–35CrossRefGoogle Scholar
  63. Silva MF et al (2016) Composition and biological activities of the essential oil of Piper corcovadensis (Miq.) C. DC (Piperaceae). Exp Parasitol 165:64–70CrossRefGoogle Scholar
  64. Santos GKN, Dutra KA, Barros RA, Câmara CAG, Lira DD, Gusmão NB, Navarro DM (2012) Essential oils from Alpinia purpurata (Zingiberaceae): chemical composition, oviposition deterrence, larvicidal and antibacterial activity. Ind Crop Prod 40:254–260CrossRefGoogle Scholar
  65. Sivagnaname N, Kalyanasundaram M (2004) Laboratory evaluation of methanolic extract of Atlantia monophylla (family: Rutaceae) against immature stages of mosquitoes and non-target organisms. Mem Inst Oswaldo Cruz 99:115–118CrossRefGoogle Scholar
  66. Stalin N, Swamy PS (2013) Leaf essential oil composition and biochemical activity of an endangered medicinal tree Syzygium caryophyllatum (L.) Alston, (wild black plum). J Essent Oil Bear Pl 17(3):371–379Google Scholar
  67. Stasi LCD, Hiruma-Lima CA (2002) Plantas Medicinais na Amazonia e na Mata Atlantica, 2nd edn. Editora Unesp, Sao PauloGoogle Scholar
  68. Wong KC, Lai FY (1996) Volatile constituents from the fruits of four Syzygium species. Flavour Frag J 11(1):61–66CrossRefGoogle Scholar
  69. 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/1.3Google Scholar
  70. Xue RD, Barnard DR, Ali A (2001) Laboratory and field evaluation of insect repellents as oviposition deterrents against the mosquito Aedes albopictus. Med Vet Entomol 15:126–131CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  2. 2.Unit of Vector Control, Phytochemistry and Nanotechnology, Department of ZoologyAnnamalai UniversityAnnamalainagarIndia

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