Abstract
Mosquitoes are well-known vectors of disease and threaten the health of millions of people annually. While synthetic insecticides have been relied on to combat these diseases, insecticide resistance and environmental concerns have directed attention towards novel and more targeted mosquitocides derived from botanicals. Research on the activity of botanical derivatives has focused on mosquito larvae and adults with little attention given to their potential as oviposition deterrents against gravid female mosquitoes. This review explores the influence of chemical and biological factors on deterrence and examines issues relating to environmental persistence and non-target effects. With very few discoveries of new insecticide pathways, the answer to effective mosquito control may well reside within other ancient plant-based organisms that have co-resided and evolved with this ubiquitous pest.
This is a preview of subscription content, access via your institution.
References
Afify A, Galizia G (2015) Chemosensory cues for mosquito oviposition site selection. J Med Entomol 52(2):120–130
Ahbirami R, Zuharah WF, Yahaya ZS, Dieng H, Thiagaletchumi M, Nik F, Ahmad AH, Abu Bakar S (2014) Oviposition deterring and oviciding potentials of Ipomoea cairica L. leaf extract against dengue vectors. Trop Biomed 31(3):456–465
Autran ES, Neves IA, da Silvaa CSB, Santosa GKN, da Câmarab CAG, Navarro DMAF (2009) Chemical composition, oviposition deterrent and larvicidal activities against Aedes aegypti of essential oils from Piper marginatum Jacq. (Piperaceae). Bioresour Technol 100(7):2284–2288
Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114(8):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(9):3201–3212
Benelli G (2016) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115(1):23–34
Benelli G, Beier J (2017) Current vector control challenges in the fight against malaria. Acta Trop 174:91–96
Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115(5):1747–1754
Benelli G, Romano D (2017) Mosquito vectors of Zika virus. Entomol Generalis. https://doi.org/10.1127/entomologia/2017/0496
Benelli G, Conti B, Garreffa R, Nicoletti M (2014) Shedding light on bioactivity of botanical by-products: neem cake compounds deter oviposition of the arbovirus vector Aedes albopictus (Diptera: Culicidae) in the field. Parasitol Res 113(3):933–940
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(1):227–236
Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015b) Old ingredients for a new recipe? Neem cake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol Res 114(2):391–397
Benelli G, Rajeswary M, Govindarajan M (2016a) 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 Pollut Res. https://doi.org/10.1007/s11356-016-8146-3
Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016b) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115(6):2131–2137
Bentley MD, Day JF (1989) Chemical ecology and behavioral aspects of mosquito oviposition. Annu Rev Entomol 34:401–421
Brogdon WG, McAllister JC (1998) Insecticide resistance and vector control. Emerg Infect Dis 4(4):23–26
Canyon DV, Muller R (2013) Oviposition and olfaction responses of Aedes aegypti mosquitoes to insecticides. Trop Biomed 30(4):691–698
Cheah SX, Tay JW, Chan LK, Jaal Z (2013) Larvicidal, oviposition, and ovicidal effects of Artemisia annua (Asterales: Asteraceae) against Aedes aegypti, Anopheles sinensis, and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 112(9):3275–3282
Coria C, Almiron W, Valladares G, Carpinella C, Luduena F, Defago M, Palacios S (2008) Larvicide and oviposition deterrent effects of fruit and leaf extracts from Melia azedarach L. on Aedes aegypti (L.) (Diptera: Culicidae). Bioresour Technol 99(8):3066–3070
D’Mello JP (1997) Handbook of plant and fungal toxicants. CRC, Boca Raton
de Lima GPG, de Souza TM, Freire GP, Farias DF, Cunha AP, Ricardo NMPS, de Morais SM, Carvalho AFU (2013) Further insecticidal activities of essential oils from Lippia sidoides and Croton species against Aedes aegypti L. Parasitol Res 112(5):1953–1958
Elango G, Abdul Rahuman A, Bagavan A, Kamaraj C, Abduz Zahir A, Rajakumar G, Marimuthu S, Santhoshkumar T (2010) Studies on effects of indigenous plant extracts on malarial vector, Anopheles subpictus Grassi (Diptera: Culicidae). Trop Biomed 27(2):143–154
El-Gendy NA, Shaalan EA (2012) Oviposition deterrent activity of some volatile oils against the filaria mosquito vector Culex pipiens. J Entomol 9(6):435–441
Elhag EA (1999) Mosquitocidal and oviposition deterrent effects in medicinal and other plant extract on Culex pipiens L. J King Abdul Aziz Univ 10(1):55–67
Elimam AM, Elmalik KH, Ali FS (2009) Efficacy of leaves extract of Calotropis procera Ait. (Asclepiadaceae) in controlling Anopheles arabiensis and Culex quinquefasciatus mosquitoes. Saudi J Biol Sci 16(2):95–100
Fatima K, Bashar K, Rahman KMZ, Howlader AJ (2011) Oviposition deterrent activity of some indigenous plant leaf extracts on mosquito Culex quinquefasciatus say (Diptera: Culicidae). Bangladesh J Life Sci 23(1):25–31
Hausen BM, Reichling J, Harkenthal M (1999) Degradation products of monoterpenes are the sensitizing agents in tea tree oil. Am J Contact Derm 10(2):68–77
Khandagle AJ, Tare VS, Raut KD, Morey RA (2011) Bioactivity of essential oils of Zingiber officinalis and Achyranthes aspera against mosquitoes. Parasitol Res 109(2):339–343
Kramer WL, Mulla MS (1979) Oviposition attractant and repellents of mosquitoes: oviposition responses of Culex mosquitoes to organic infusions. Environ Entomol 8:1111–1117
Kweka EJ, Lyatuu EE, Mboya MA, Mwang’onde BJ, Mahande AM (2010) Oviposition deterrence induced by Ocimum kilimandscharicum and Ocimum suave extracts to gravid, Anopheles gambiae s.s. (Diptera: Culicidae) in laboratory. J Global Infect Dis 2(3):242–245
Kydonieus AF (1980) Controlled release technologies: methods, theory, and applications, vol 1 and 2. CRC press, Boca Raton
Lindberg CM, Melathopoulos AP, Winston ML (2000) Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymentoptera: Apidae) parasite. J Econ Entomol 93(2):189–198
Madhiyazhagan P, Murugan K, Kumar AN, Nataraj T, Dinesh D, Panneerselvam C, Subramaniam J, Kumar PM, Suresh U, Roni M, Nicoletti M, Alarfaj AA, Higuchi A, Munusamy MA, Benelli G (2015) Sargassum muticum-synthesized silver nanoparticles: an effective control tool against mosquito vectors and bacterial pathogens. Parasitol Res 114(11):4305–4317
Maheswaran R, Ignacimuthu S (2014) Effect of Polygonum hydropiper L. against dengue vector mosquito Aedes albopictus L. Parasitol Res 113(9):3143–3150
Mohsen ZH, Jawad ALM, AL-Chalabi BM, AL-Naib A (1990) Biological activity of Callistemon lanceolatus against Culex quinquefasciatus. Fitoterapia 61(3):270–274
Moretti MDL, Sanna-Passino G, Demontis S, Bazzoni E (2002) Essential oil formulations useful as a new tool for insect pest control. AAPS PharmSciTech 3(2):64–74
Naqqash MN, Gokçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115(4):1363–1373
Nogueira de MAS, Palmerio M (2001) In: Neem and pheromones: practice oriented results on use and production of plant extracts and pheromones in integrated and biological pest control. First Workshop, Uberaba, Brasil, May 15-16, pp. 46
Ouda NA, Al-Chalabi BM, Al-Charchafchi FMR, Mohsen ZH (1998) Insecticidal and ovicidal effects of the seed extract of Atriplex Canescens against Culex quinquefasciatus. Pharm Biol 36(1):69–71
Pandey SK, Upadhyay S, Tripathi AK (2009) Insecticidal and repellent activities of thymol from the essential oil of Trachyspermum ammi (Linn) Sprague seeds against Anopheles stephensi. Parasitol Res 105(2):507–512
Pavela R (2014) Insecticidal properties of Pimpinella anisum essential oils against the Culex quinquefasciatus and the non-target organism Daphnia magna. J Asia Pac Entomol 17(3):287–293
Pavela R (2016) Encapsulation—a convenient way to extend the persistence of the effect of eco-friendly mosquito larvicides. Curr Org Chem 20(25):2674–2680
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 ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21(12):1000–1007
Perera MDB, Hemingway J, Karunaratne SHPP (2008) Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malar J 7:168
Phasomkusolsil S, Soonwera M (2012) The effects of herbal essential oils on the oviposition deterrent and ovicidal activities of Aedes aegypti (Linn.), Anopheles dirus (Peyton and Harrison) and Culex quinquefasciatus (Say). Trop Biomed 29(1):138–150
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(16):1749–1757
Prathibha KP, Raghavendra BS, Vijayan VA (2014) Larvicidal, ovicidal, and oviposition-deterrent activities of four plant extracts against three mosquito species. Environ Sci Pollut Res 21(10):6736–6743
Rajaganesh R, Murugan K, Panneerselvam C, Jayashanthini S, Aziz A, 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 109:40–51
Rajeswary M, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2017) Zingiber cernuum (Zingiberaceae) essential oil as effective larvicide and oviposition deterrent on six mosquito vectors, with little non-target toxicity on four aquatic mosquito predators. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-9093-3
Rajkumar S, Jebanesan A (2005) Oviposition deterrent and skin repellent activities of Solanum trilobatum leaf extract against the malaria vector Anopheles stephensi. J Insect Sci 5:15
Rajkumar S, Jebanesan A (2008) Bioactivity of Chenopodium ambrosioides L. (Family. Chenopodiaceae) against the filariasis vector Culex quinquefasciatus Say (Diptera: Culicidae). Can J Pure Appl Sci 2(1):129–132
Rajkumar S, Jebanesan A (2009) Larvicidal and oviposition activity of Cassia obtusifolia Linn (Family: Leguminosae) leaf extract against malarial vector, Anopheles stephensi Liston (Diptera: Culicidae). Parasitol Res 104(2):337–340
Ramar M, Ignacimuthu S, Paulraj MG (2014) Ovicidal and oviposition response activities of plant volatile oils against Culex quinquefasciatus say. J Entomol Zool Studies 2(4):82–86
Reegan DR, Gandhi MR, Paulraj MG, Ignacimuthu S (2015) Ovicidal and oviposition deterrent activities of medicinal plant extracts against Aedes aegypti L. and Culex quinquefasciatus Say mosquitoes (Diptera: Culicidae). Osong Public Health Res Perspect 6(1):64–69
Satho T, Dieng H, Ahmad MHI, Ellias SB, Abu Hassan A, Abang F et al (2015) Coffee and its waste repel gravid Aedes albopictus females and inhibit the development of their embryos. Parasit Vectors 8:272
Seenivasagana T, Vijayaraghavan R (2010) Oviposition pheromones in haematophagous insects. Vitam Horm 83:597–630
Shaalan EA, Canyon D, Younes MW, Abdel-Wahab H, Mansour AH (2005) A review of botanical phytochemicals with mosquitocidal potential. Environ Inter 31(8):1149–1166
Singh SP, Mittal PK (2013) Mosquito repellent and oviposition deterrent activities of Solanum nigrum seed extract against malaria vector Anopheles stephensi. Online Inter Interdiscip Res J 3(6):326–333
Singh SP, Mittal PK (2015) Mosquito repellent and oviposition deterrent activities of Laggera aurita plant extract against malaria vector Anopheles stephensi. Entomol Appl Sci Lett 2(1):18–22
Soonwera M (2015) Efficacy of essential oil from Cananga odorata (Lamk.) Hook.F. & Thomson (Annonaceae) against three mosquito species Aedes aegypti (L.), Anopheles dirus (Peyton and Harrison), and Culex quinquefasciatus (Say). Parasitol Res 114(12):4531–4543
Sukumar K, Perich MJ, Boobar LR (1991) Botanical derivatives in mosquito control: a review. J Am Mosq Control Assoc 7(2):210–237
Tawatsin A, Asavadachanukorn P, Thavara U, Wongsinkongman P, Bansidhi J, Boonruad T, Chavalittumrong P, Soonthornchareonnon N, Komalamisra N, Mulla MS (2006) Repellency of essential oils extracted from plants in Thailand against four mosquito vectors (Diptera: Culicidae) and oviposition deterrent effects against Aedes aegypti (Diptera: Culicidae). Southeast Asian J Trop Med Public Health 37(5):915–931
Tennyson S, Ravindran KJ, Eapen A, William SJ (2012) Effect of Ageratum houstonianum Mill. (Asteraceae) leaf extracts on the oviposition activity of Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 111(6):2295–2299
Tripathi AK, Upadhyay S, Bhuiyan M, Bhattacharya PR (2009) A review on prospects of essential oils as biopesticide in insect-pest management. J Pharmaco Phytoth 1(5):052–063
Waliwitiya R, Kennedy CJ, Lowenberger CA (2008) Larvicidal and oviposition-altering activity of monoterpenoids, trans-anethole and rosemary oil to the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). Pest Manag Sci 65(3):241–248
Warikoo R, Kumar S (2014) Oviposition altering and ovicidal efficacy of root extracts of Argemone mexicana against dengue vector, Aedes aegypti (Diptera: Culicidae). J Entomol Zool Stud 2(4):11–17
Warikoo R, Kumar S (2015) Investigation on the oviposition-deterrence and ovicidal potential of the leaf extracts of Argemone mexicana against an Indian strain of dengue vector, Aedes aegypti (Diptera: Culicidae). Appl Res J 1(4):208–215
Warikoo R, Wahab N, Kumar S (2011) Oviposition-altering and ovicidal potentials of five essential oils against female adults of the dengue vector, Aedes aegypti L. Parsitol Res 109(4):1125–1131
Yadav R, Tyagi V, Tikar SN, Sharma AK, Mendki MJ, Jain AK, Sukumaran D (2014) Differential larval toxicity and oviposition altering activity of some indigenous plant extracts against dengue and chikungunya vector Aedes albopictus. J Arthropod-Borne Dis 8(2):174–185
Yu KX, Wong CL, Ahmad R, Jantan I (2015) Mosquitocidal and oviposition repellent activities of the extracts of seaweed Bryopsis pennata on Aedes aegypti and Aedes albopictus. Molecules 20(8):14082–14102
Zuharah WF, Ling CJ, Zulkifly N, Fadzly N (2015) Toxicity and sub-lethal effect of endemic plants from family Anacardiaceae on oviposition behavior of Aedes albopictus. Asian Pac J Trop Biomed 5(8):612–618
Acknowledgements
The authors wish to express their sincere appreciation to Dr. Giovanni Benelli for inviting them to write this paper, reading the full manuscript, enhancing its accuracy and clarity and providing valuable criticism.
The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Daniel K. Inouye Asia Pacific Center for Security Studies, the Department of Defense, or the US Government.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Shaalan, E.AS., Canyon, D.V. Mosquito oviposition deterrents. Environ Sci Pollut Res 25, 10207–10217 (2018). https://doi.org/10.1007/s11356-017-0408-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0408-1