Abstract
The effective and environmentally sustainable control of mosquitoes is a challenge of essential importance. This is due to the fact that some invasive mosquitoes, with special reference to the Aedes genus, are particularly difficult to control, due to their high ecological plasticity. Moreover, the indiscriminate overuse of synthetic insecticides resulted in undesirable effects on human health and non-target organisms, as well as resistance development in targeted vectors. Here, the leaf essential oil (EO) extracted from a scarcely studied plant of ethno-medicinal interest, Blumea eriantha (Asteraceae), was tested on the larvae of six mosquitoes, including Zika virus vectors. The B. eriantha EO was analyzed by GC and GC-MS. The B. eriantha EO showed high toxicity against 3rd instar larvae of six important mosquito species: Anopheles stephensi (LC50=41.61 μg/ml), Aedes aegypti (LC50=44.82 μg/ml), Culex quinquefasciatus (LC50 =48.92 μg/ml), Anopheles subpictus (LC50=51.21 μg/ml), Ae. albopictus (LC50=56.33 μg/ml) and Culex tritaeniorhynchus (LC50=61.33 μg/ml). The major components found in B. eriantha EO were (4E,6Z)-allo-ocimene (12.8%), carvotanacetone (10.6%), and dodecyl acetate (8.9%). Interestingly, two of the main EO components, (4E,6Z)-allo-ocimene and carvotanacetone, achieved LC50 lower than 10 μg/ml on all tested mosquito species. The acute toxicity of B. eriantha EO and its major constituents on four aquatic predators of mosquito larval instars was limited, with LC50 ranging from 519 to 11.431 μg/ml. Overall, the larvicidal activity of (4E,6Z)-allo-ocimene and carvotanacetone far exceed most of the LC50 calculated in current literature on mosquito botanical larvicides, allowing us to propose both of them as potentially alternatives for developing eco-friendly mosquito control tools.
Similar content being viewed by others
References
Adams RP (2007) 4th Ed. Carol Stream, Illinois: Allured Publishing Corporation; Identification of essential oil components by gas chromatography/mass spectroscopy
Alkofahi A, Rupprecht JK, Anderson JE, Mclaughlin JL, Mikolajczak KL, Scott BA (1989) Search for new pesticides from higher plants. In: Arnason JT, Philogene BJR, Morand P (eds) Insecticides of Plant Origin. American Chemical Society, Washington, DC, pp 25–43
AlShebly MM, AlQahtani FS, Govindarajan M, Gopinath K, Vijayan P, Benelli G (2017) Toxicity of ar-curcumene and epi-β-bisabolol from Hedychium larsenii (Zingiberaceae) malaria, chikungunya and St. Louis encephalitis mosquito vectors. Ecotoxicol Environ Saf 137:149–157
Amer A, Mehlhorn H (2006a) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490
Amer A, Mehlhorn H (2006b) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499
Amer A, Mehlhorn H (2006c) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Amer A, Mehlhorn H (2006d) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477
Baranitharan M, Dhansekaran S, Murugan K, Kovendan K, Gokulakrishnan J (2016) Chemical composition and laboratory investigation of Melissa officinalis essential oil against human malarial vector mosquito, Anopheles stephensi L. (Diptera: Culicidae). J Coast Life Med 4(12):969–973
Baranitharan M, Dhanasekaran S, Kovendan K, Murugan K, Gokulakrishnan J, Benelli G (2017) Coleus aromaticus leaf extract fractions: a source of novel ovicides, larvicides and repellents against Anopheles, Aedes and Culex mosquito vectors? Process Saf Environ Prot 106:23–33
Becker N (2008) Influence of climate change on mosquito development and mosquito-borne diseases in Europe. Parasitol Res 103(Suppl 1):19–28
Becker N, Geier M, Balczun C, Bradersen U, Huber K, Kiel E, Krueger A, Luehken R, Orendt C, Plenge-Boenig A, Rose A, Schaub GA, Tannich E (2013) Repeated introduction of Aedes albopictus into Germany, July to. October 2012. Parasitol Res 112:1787–1790
Benedict MQ, Levine RS, Hawley WA, Lounibos LP (2007) Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector-Borne Zoonotic Dis 7:76–85
Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805
Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114:3201–3212
Benelli G (2016a) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115:23–34
Benelli G (2016b) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer – a brief review. Enzym Microb Technol 95:58–68
Benelli G (2017) Commentary: Data analysis in bionanoscience – issues to watch for. J Clust Sci. doi:10.1007/s10876-016-1143-3
Benelli G, Govindarajan M (2017) 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
Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754
Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115:2131–2137
Benelli G, Pavela R, Maggi F, Petrelli R, Nicoletti M (2017a) Commentary: Making green pesticides greener? The potential of plant products for nanosynthesis and pest control. J Clust Sci. doi:10.1007/s10876-016-1131-7
Benelli G, Pavela R, Iannarelli R, Petrelli R, Cappellacci L, Cianfaglione K, Afshar FH, Nicoletti M, Canale A, Maggi F (2017b) Synergized mixtures of Apiaceae essential oils and related plant-borne compounds: larvicidal effectiveness on the filariasis vector Culex quinquefasciatus Say. Ind Crop Prod 96:186–195
Benelli G, Rajeswary M, Govindarajan M (2017c) Towards green oviposition deterrents? Effectiveness of Syzygium lanceolatum (Myrtaceae) essential oil against six mosquito vectors and impact on four aquatic biological control agents. Environ Sci Poll Res. doi:10.1007/s11356-016-8146-3
Benelli G, Pavela R, Canale A, Cianfaglione K, Ciaschetti G, Conti F, Nicoletti M, Senthil-Nathan S, Mehlhorn H, Maggi F (2017d) Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: synergistic and antagonistic effects. Parasitol Int. doi:10.1016/j.parint.2017.01.012
Bhuiyan MNI, Chowdhury JU, Begum J (2009) Chemical components in volatile oil from Blumea balsamifera(L.) DC. Bangladesh J Botany 38:107–109
Carolina A, Maman M (2016) Larvicidal activity of essential oils from the leaves and fruits of nutmeg (Myristica fragrans Houtt) against Aedes aegypti (Diptera: Culicidae) Turkish. J Agric Food Sci Technol 4(7):552–556
Cheng SS, Chua MT, Chang EH, Huang CG, Chen WJ, Chang ST (2009) Variations in insecticidal activity and chemical composition of leaf essential oils from Cryptomeria japonica at different ages. Biores Technol 100:465–470
Deo PG, Hasan SB, Majumdar SK (1988) Toxicity and suitability of some insecticides for household use. Int Pest Control 30:118–129
Dinesh D, Murugan K, Madhiyazhagan P, Panneerselvam C, Nicoletti M, Jiang W, Benelli G, Chandramohan B, Suresh U (2015) Mosquitocidal and antibacterial activity of green-synthesized silver nanoparticles from Aloe vera extracts: towards an effective tool against the malaria vector Anopheles stephensi? Parasitol Res 114:1519–1529
Dung NX, Loi DT, Hung DT, Leclercq PA (1991) Chemical composition of the oil of Blumea lanceolaria (Roxb.) Druce from Vietnam. J Essent Oil Res 3:285–286
El Ouali LA, El-Akhal F, Maniar S, Ez Zoubi Y, Taghzouti K (2016) Chemical Constituents and larvicidal activity of Essential Oil of Lavandula Stoechas (Lamiaceae) from Morocco against the malaria vector Anopheles Labranchiae (Diptera: Culicidae). J Pharmacogn Phytochem Res 8(3):505–511
El-Akhal F, El Ouali LA, 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
Elango G, Rahuman AA, Bagavan A, Kamaraj C, Zahir AA, Venkatesan C (2009) Laboratory study on larvicidal activity of indigenous plant extracts against Anopheles subpictus and Culex tritaeniorhynchus. Parasitol Res 104:1381–1388
Finney DJ (1971) Probit analysis. Cambridge University Press, London, pp 68–72
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 3:874–877
Govindarajan M, Benelli G (2016a) Artemisia absinthium-borne compounds as novel larvicides: effectiveness against six mosquito vectors and acute toxicity on non-target aquatic organisms. Parasitol Res 115(12):4649–4661
Govindarajan M, Benelli G (2016b) Eco-friendly larvicides from Indian plants: effectiveness of lavandulyl acetate and bicyclogermacrene on malaria, dengue and Japanese encephalitis mosquito vectors. Ecotox Environ Saf 133:395–402
Govindarajan M, Benelli G (2016c) 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 115:2771–2778
Govindarajan M, Benelli G (2016d) Facile biosynthesis of silver nanoparticles using Barleria cristata: mosquitocidal potential and biotoxicity on three non-target aquatic organisms. Parasitol Res 115:925–935
Govindarajan M, Sivakumar R, Rajeswari 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 34:7–11
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 112:3713–3721
Govindarajan M, Rajeswary M, Hoti SL, Bhattacharyya A, Benelli G (2016a) 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
Govindarajan M, Rajeswary M, Arivoli S, Samuel T, Benelli G (2016b) 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 115:1807–1816
Govindarajan M, Rajeswary M, Benelli G (2016c) Chemical composition, toxicity and effects on non-target organisms of Pinus kesiya essential oil: an eco-friendly larvicide against mosquito vectors. Ecotox Environ Saf 129:85–90
Govindarajan M, Shine K, Naiyf S, Alharbi, Benelli G (2016d) 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, Rajeswary M, Benelli G (2016e) 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 19:565–571
Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391
Jahan K, Sukalyan Kumar K, Abdul Bake MD (2014) Evaluation of antimicrobial and cytotoxic activities of the methanolic and petroleum ether extract of Blumea lacera Burm.f in Bangladesh. J Pharmacogn Phytochem 2(6):104–108
Jayaraman M, Senthilkumar A, Adaikala Raj G, Venkatesalu V (2015) Isolation of mosquito larvicidal molecule from the leaves of Clausena anisata. J Exp Sci 6:12–16
Khair A, Ibrahim M, Ahsan Q, Homa Z, Kuddus MR, Rashid RB, Rashid MA (2014) Pharmacological activities of Blumea lacera (Burm. f) DC: a medicinal plant of Bangladesh. Br J Pharm Res 4:1677–1687
Khare CP (2007) Indian medicinal plants—an illustrated dictionary. Springer Science Business Media, LLC. (eds.) 233 Spring Street, New York, NY 10013, USA
Kumar S, Mishra M, Wahab N, Warikoo R (2014) Larvicidal, repellent, and irritant potential of the seed-derived essential oil of Apium graveolens against dengue vector, Aedes aegypti L. (Diptera: Culicidae). Front Public Health 18:147
Laakso I, Seppanen-Laakso T, Hiltunen R, Ekundayo O (1989) Composition of the essential oil of Blumea lacera DC. (Asteraceae) leaves from Nigeria. Flav Frag J 4:73–75
Liang Z, Ying-Juan T, Li Y, Jian-Gou J (2011) Chemical composition and antimicrobial activities of essential oil of Blumea megacephala. EXCLI J 10:62–68
Macêdo ME, Rotraut Consoli AGB, Telma Grandi SM, Anjos AMG, Oliveira AB, Mendes NM, Queiróz RO, Zani CL (1997) Screening of Asteraceae (Compositae) plant extracts for larvicidal activity against Aedes fluviatilis (Diptera: Culicidae). Mem Inst Oswaldo Cruz, Rio de Janeiro 92(4):565–570
Mehlhorn H (ed) (2015) Encyclopedia of parasitology, 4th edn. Springer, New York
Mehta SC, Vardhan H, Saxena SP (1986) Some pharmacological actions of the essential oil of Blumea membranacea. Indian J Physiol Pharmacol 30:149–154
Murugan K, Panneerselvam C, Samidoss CM, Madhiyazhagan P, Suresh U, Roni M, Chandramohan B, Subramaniam J, Dinesh D, Rajaganesh R, Paulpandi M, Wei H, Aziz AT, Saleh Alsalhi M, Devanesan S, Nicoletti M, Pavela R, Canale A, Benelli G (2016a) In vivo and in vitro effectiveness of Azadirachta indica-synthesized silver nanocrystals against Plasmodium berghei and plasmodium falciparum, and their potential against malaria mosquitoes. Res Vet Sci 106:14–22
Murugan K, Aruna P, Panneerselvam C, Madhiyazhagan P, Paulpandi M, Subramaniam J, Rajaganesh R, Wei H, Alsalhi MS, Devanesan S, Nicoletti M, Syuhei B, Canale A, Benelli G (2016b) Fighting arboviral diseases: low toxicity on mammalian cells, dengue growth inhibition (in vitro) and mosquitocidal activity of Centroceras clavulatum-synthesized silver nanoparticles. Parasitol Res 115:651–662
Mwangi JW, Achola KJ, Lwande W, Hassanali A, Laurent R (1994) Constituents of the essential oil of Blumea brevipes (Oliv. and Hiern) Willd. Flav Frag J 9:233–235
Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115:1363–1373
Norikura T, Kojima-Yuasa A, Shimizu M, Huang X, Xu S, Kametani S, Rho S, Kennedy DO, Matsui-Yuasa I (2008). Mechanism of growth inhibitory effect of Blumea balsamifera extract in Hepatocellular Carcinoma. Biosci Biotechnol Biochem 72:1183–1189
Owolabi MS, Lajideh L, Villanueva HE, Setzer WN (2010) Essential oil composition and insecticidal activity of Blumea perrottetiana growing in southwestern Nigeria. Nat Prod Comm 3:1135–1138
Panneerselvam C, Murugan K, Roni M, Aziz AT, Suresh U, Rajaganesh R, Madhiyazhagan P, Subramaniam J, Dinesh D, Nicoletti M, Higuchi A, Alarfaj AA, Munusamy MA, Kumar S, Desneux N, Benelli G (2016) Fern-synthesized nanoparticles in the fight against malaria: LC/MS analysis of Pteridium aquilinum leaf extract and biosynthesis of silver nanoparticles with high mosquitocidal and antiplasmodial activity. Parasitol Res 115:997–1013
Pavela R (2008) Larvicidal activities of some Euro-Asiatic plants against Culex quinquefasciatus Say (Diptera: Culicidae). J Biopest 1:81–85
Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187
Pavela R, Benelli G (2016a) Ethnobotanical knowledge on botanical repellents employed in the African region against mosquito vectors—a review. Exp Parasitol 167:103–108
Pavela R, Benelli G (2016b) Essential oils as eco-friendly biopesticides? Challenges and constraints. Tr Plant Sci 21(12):1000–1007
Pavela R, Govindarajan M (2016) The essential oil from Zanthoxylum monophyllum a potential mosquito larvicide with low toxicity to the non-target fish Gambusia affinis. J Pest Sci. doi:10.1007/s10340-016-0763-6
Pavela R, Vrchotova N, Triska J (2009) Mosquitocidal activities of thyme oils (Thymus vulgaris L.) against Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 105:1365–1370
Pednekar PP, Vakil BV, Sane RT, Datar AG (2012) Antimicrobial activity of essential oil of Blumea eriantha DC against skin pathogens. Int J Pharm Pharm Sci 4:296–299
Pratheeba T, Prabhavathi O, Yuvarajan R, Murugan N, Natarajan D (2015) Identification of mosquitocidal compounds from the leaf extracts of Ocimum gratissimum (lamiaceae) against dengue and chikungunya vector Aedes aegypti (L.). Int J Entomol Res 3:67–79
Sakee U, Maneerat S, Cushnie TP, De-Eknamkul W (2011) Antimicrobial activity of Blumea balsamifera (Lin.) DC. extracts and essential oil. Nat Prod Res 25:1849–1856
Santi E, Simone (2014) Evaluating the toxicity of oil of lemon eucalyptus, Corymbia citriodora (Hook.), against larvae of the Asian tiger mosquito and non-target fish and larval amphibians. Ann Biologia 36:97–105
Senthilkumar A, Kannathasan K, Venkatesalu V (2008) Chemical constituents and Larvicidal property of the essential oil of Blumea mollis (D. Don) Merr. against Culex quinquefasciatus. Parasitol Res 103:959–962
Singh UP, Singh AK, Sarathy RP (2011) Effect of methanolic extracts of Blumea eriantha DC dc leaves on protein metabolism and marker enzymes in streptozotocin induced hyperglycemic animals. Int J of Pharm Sci 4(1):235–238
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 99:115–118
Subramaniam J, Murugan K, Panneerselvam C, Kovendan K, Madhiyazhagan P, Kumar PM, Dinesh D, Chandramohan B, Suresh U, Nicoletti M, Higuchi A, Hwang JS, Kumar S, Alarfaj AA, Munusamy MA, Messing RH, Benelli G (2015) Eco-friendly control of malaria and arbovirus vectors using the mosquitofish Gambusia affinis and ultra-low dosages of Mimusops elengi-synthesized silver nanoparticles: towards an integrative approach? Environ Sci Pollut Res Int 22:20067–20083
Subramaniam J, Murugan K, Panneerselvam C, Kovendan K, Madhiyazhagan P, Dinesh D, Mahesh Kumar P, Chandramohan B, Suresh U, Rajaganesh R, Saleh Alsalhi M, Devanesan S, Nicoletti M, Canale A, Benelli G (2016) Multipurpose effectiveness of Couroupita guianensis-synthesized gold nanoparticles: high antiplasmodial potential, field efficacy against malaria vectors and synergy with Aplocheilus lineatus predators. Environ Sci Poll Res 23:7543–7558
Veni T, Pushpanathan T, Mohanraj J (2016) Ovicidal and larvicidal efficacy of Crataeva magna (lour.) dc. (Family: Capparidaceae) against the Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Int J Pure Appl Zool 4:149–154
Verdian-Rizi M (2009) Chemical composition and Larvicidal activity of the essential oil of Laurus nobilis L. from Iran. Iran J Pharm Sci 5:47–50
Wang SY, Lai WC, Chu FH, Lin CT, Shen SY, Chang ST (2006) Essential oil from the leaves of Cryptomeria japonica acts as a silverfish (Lepisma saccharina) repellent and insecticide. J Wood Sci 52:522–526
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.
Yakob L, Walker T (2016) Zika virus outbreak in the Americas: the need for novel mosquito control methods. Lancet Glob Health S2214-109X(16)00048–6
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
Acknowledgements
We are grateful to H. Mehlhorn and the anonymous reviewers for their useful suggestions on an earlier version of our study. The authors extend their sincere appreciations to the Deanship of Scientific Research at King Saud University for funding this Prolific Research Group (PRG-1437-36). The authors would like to thank Professor and Head, Department of Zoology, Annamalai University, for the laboratory facilities provided.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Benelli, G., Govindarajan, M., Rajeswary, M. et al. Larvicidal activity of Blumea eriantha essential oil and its components against six mosquito species, including Zika virus vectors: the promising potential of (4E,6Z)-allo-ocimene, carvotanacetone and dodecyl acetate. Parasitol Res 116, 1175–1188 (2017). https://doi.org/10.1007/s00436-017-5395-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-017-5395-0