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Prospects for repellent in pest control: current developments and future challenges

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Abstract

The overall interest in environmentally safe pest control methods and the rise of insecticide resistance in pest populations have prompted medical and agricultural entomology research on insect repellents in recent years. However, conducting research on repellent is challenging for several reasons: (1) the different repellent phenomena are not well defined; (2) it is difficult to test for and quantify repellent; (3) the physiological mechanisms are poorly known; (4) the field efficacy appears to be highly variable. Here, we identified five different types of repellent: expellency, irritancy, deterrency, odor masking and visual masking, and described behavioral bioassays to differentiate between them. Although these categories are currently defined by their behavioral response to different stimuli, we suggest new definitions based on their mechanism of action. We put forward three main hypotheses on the physiological mechanism: (1) a dose effect that modifies the behavior, (2) a repellent mechanism with specific receptors, or (3) inhibition of the transduction of neural information.

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References

  • Abdelgaleil SAM, El-Aswad AF, Nakatani M (2002) Molluscidal and anti-feedant activities of diterpenes from Euphorbia paralias L. Pest Manag Sci 58:479–482

    Article  CAS  PubMed  Google Scholar 

  • Abdullah ZS, Ficken KJ, Greenfield BP, Butt TM (2014) Innate responses to putative ancestral hosts: is the attraction of Western flower thrips to pine pollen a result of relict olfactory receptors? J Chem Ecol 40:534–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abtew A, Subramanian S, Cheseto X, Kreiter S, Tropea Garzia G, Martin T (2015) Repellency of plant extracts against the legume flower thrips Megalurothrips sjostedti (Thysanoptera: Thripidae). Insects 6:608–625

    Article  PubMed  PubMed Central  Google Scholar 

  • Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48(3):417–430

    Article  CAS  PubMed  Google Scholar 

  • Achee N, Sardelis M, Dusfour I, Chauchan K, Grieco J (2009) Characterization of spatial repellent, contact irritant, and toxicant chemical actions of standard vector control compounds. J Am Mosquito Contr 25:156–167

    Article  CAS  Google Scholar 

  • Achee N, Bangs M, Farlow R, Killeen G, Lindsay S, Logan J, Moore S, Rowland M, Sweeney K, Torr S, Zwiebel L, Grieco J (2012) Spatial repellents: from discovery and development to evidence-based validation. Malaria J 11:164–182

    Article  Google Scholar 

  • Adeogun AO, Olojede JB, Oduola AO, Awolola TS (2012) Village-scale evaluation of PermaNet 3.0: anenhanced efficacy combination long-lasting insecticidal net against resistant populations of Anopheles gambiae s.s. MCCE 1:1–9

    Google Scholar 

  • Akhtar Y, Hankin CH, Isman MB (2003) Decreased response to feeding deterrents following prolonged exposure in the larvae of a generalist herbivore, Trichoplusia ni (Lepidoptera: Noctuidae). J Insect Behav 16:811–831

    Article  Google Scholar 

  • Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 67:69–139

    Article  Google Scholar 

  • Amrein H, Thorne N (2005) Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15:673–684

    Article  CAS  Google Scholar 

  • Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant-insect interactions. Curr Opin Plant Biol 4:351–358

    Article  CAS  PubMed  Google Scholar 

  • Bernays EA, Chapman RF (2000) A neurophysiological study of sensitivity to a feeding deterrent in two sister species of Heliothis with different diet breadths. J Insect Physiol 46:905–912

    Article  CAS  PubMed  Google Scholar 

  • Bernier UR, Kline DL, Posey KH (2007) Human emanations and related natural compound that inhibit mosquito host-finding abilities. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. New York, USA, CRC Press, Taylor and Francis Group, pp 77–100

  • Blaney WM, Simmonds MSJ, Ley SV, Anderson JC, Toogood PL (1990) Antifeedant effects of azadirachtin and structurally related compounds on lepidopterous larvae. Entomol Exp appl 743 55(2):149–160

  • Bohbot JD, Fu L, Le TC, Chauchan KR, Cantrell CL, Dickens JC (2011) Multiple activities of insect repellents on odorant receptors in mosquitoes. Med Vet Entomol 25:436–444

    Article  CAS  PubMed  Google Scholar 

  • Borden JH (1997) Disruption of semiochemical-mediated aggregation in bark beetles. In: Cardé ED, Minds AK. Insect pheromone research: new directions. Chapman and Hall, New York, pp 421–438

  • Brown M, Hebert AA (1997) Insect repellents: an overview. J Am Acad Dermatol 36:243–249

    Article  CAS  PubMed  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  PubMed  Google Scholar 

  • Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, Doherty A, Sparks CA, Woodcock CM, Birkett MA, Napier JA, Jones HD (2015) The first crop plant genetically engineered to release an insect pheromone for defence. Scientific reports 5

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 651:175–187

    Article  Google Scholar 

  • Cameron R, Hopper L, Alvarez JM (2016) Use of fluorescence to determine reduction in Bemisia tabaci (Hemiptera: Aleyrodidae) nymph feeding when exposed to cyantraniliprole and imidacloprid through systemic applications. Crop Prot 84:21–26

    Article  CAS  Google Scholar 

  • Chadwick PR, Lord CJ (1977) Tests of pyrethroid vaporising mats against Aedes aegypti (L.) (Diptera: Culicidae). Bull Entomol Res 67:667–674

    Article  CAS  Google Scholar 

  • Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P (2000) Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Med Vet Entomol 14:81–88

    Article  CAS  PubMed  Google Scholar 

  • Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Ann Rev Entomol 48:455–484

    Article  CAS  Google Scholar 

  • Christensen TA, Hildebrand JG (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12:393–399

    Article  CAS  PubMed  Google Scholar 

  • Christensen TA, White J (2000) Representation of olfactory information in the brain. In: Bryant BP, Silver WL. The neurobiology of taste and smell. Wiley-Liss, New York, pp 201–232

  • Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Ann Rev Entomol 52:375–400

    Article  CAS  Google Scholar 

  • Cunningham JP (2012) Can mechanism help explain insect host choice? J Evol Biol 25:244–251

    Article  CAS  PubMed  Google Scholar 

  • Davis EE (1985) Insect repellents: Concepts of their mode of action relative to potential sensory mechanisms in mosquitoes (Diptera: Culicidae). J Med Entomol 22:237–243

    Article  CAS  PubMed  Google Scholar 

  • Davis EE, Sokolove PG (1976) Lactic acid-sensitive receptors on the antennae of the mosquito, Aedes aegypti. J Comp Physiol 105:43–54

    Article  CAS  Google Scholar 

  • de Belle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263(5147):692–695

    Article  PubMed  Google Scholar 

  • De Boer G (2006) The role of the antennae and maxillary palps in mediating food preference by larvae of the tobacco hornworm, Manduca sexta. Entomol Exp Appl 119:29–38

    Article  Google Scholar 

  • De Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19:4520–4532

    PubMed  Google Scholar 

  • De Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  PubMed  Google Scholar 

  • De Gennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, Jasinskiene N, James AA, Vosshall LB (2013) Orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498:487–491

    Article  CAS  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    Article  PubMed  CAS  Google Scholar 

  • Deletre E, Martin T, Campagne P, Bourguet D, Cadin A, Menut C, Bonafos R, Chandre F (2013) Repellent, irritant and toxic effects of 20 plant extracts on adults of the malaria vector Anopheles gambiae mosquito. PLoS ONE 8:12

    Article  CAS  Google Scholar 

  • Deletre E, Chandre F, Barkman B, Menut C, Martin T (2015) Naturally occurring bioactive compounds from four essential oils against Bemisia tabaci whiteflies. Pest Manag Sci. doi:10.1002/ps.3987

    PubMed  Google Scholar 

  • Deletre E, Martin T, Duménil C, Chandre F (2016) DEET and natrural compounds are more effective on Anopheles gambiae resistant strains

  • Dethier VG (1954) The physiology of olfaction in insects. Ann NY Acad Sci 58(2):139–157

    Article  CAS  PubMed  Google Scholar 

  • Dickens JC (2006) Plant volatiles moderate response to aggregation pheromone in Colorado potato beetle. J Appl Entomol 130:26–31

    Article  Google Scholar 

  • Dickens JC, Bohbot JD (2013) Mini review: Mode of action of mosquitoes repellents. Pestic Biochem Phys 106(3):149–155

    Article  CAS  Google Scholar 

  • Dickens JC, Oliver JE, Hollister B, Davis JC, Klun JA (2002) Breaking a paradigm: male produced aggregation pheromone for the Colorado potato beetle. J Exp Biol 205:1925–1933

    PubMed  Google Scholar 

  • Ditzen M, Pellegrino M, Vosshall LB (2008) Insect odorant receptors are molecular targets of the insect repellent DEET. Sciences 319:1838–1842

    Article  CAS  Google Scholar 

  • Dogan EB, Ayres JW, Rossignol PA (1999) Behavioural mode of action of DEET: inhibition of lactic acid attraction. Med Vet Entomol 13:97–100

    Article  CAS  PubMed  Google Scholar 

  • Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822–835

    Article  CAS  PubMed  Google Scholar 

  • Elliott M, Janes NF, Potter C (1978) The future of pyrethroids in insect control. Ann Rev Entomol 23:443–469

    Article  Google Scholar 

  • Finch S, Collier RH (2012) The influence of host and non-host companion plants on the behavior of pest insects in field crops. Entomol Exp Appl 142:87–96

    Article  Google Scholar 

  • Foster SP, Harris MO (1997) Behavioral manipulation methods for insect pest-management. Ann Rev Entomol 42:123–146

    Article  CAS  Google Scholar 

  • Foster SP, Denholm I, Thompson R, Poppy GM, Powell W (2005) Reduced response of insecticide resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off. Bull Entomol Res 95:37–46

    Article  CAS  PubMed  Google Scholar 

  • Fraenkel GS (1959) The ‘raison d’être’ of secondary plant substances. Science 129:1466–1470

    Article  CAS  PubMed  Google Scholar 

  • Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Ann Rev Entomol 55:399–420

    Article  CAS  Google Scholar 

  • Gibson G, Torr SJ (1999) Visual and olfactory responses of haematophagous Diptera to host stimuli. Med Vet Entomol 13:2–23

    Article  CAS  PubMed  Google Scholar 

  • Glendinning JL, Valcic S, Timmermann BN (1998) Maxillary palps can mediate taste rejection of plant allelochemicals by caterpillars. J Comp Phys 183:35–43

    Article  CAS  Google Scholar 

  • Glendinning JI, Brown H, Capoor M, Davis A, Gbedemah A, Long E (2001) A peripheral mechanism for behavioral adaptation to specific “bitter” taste stimuli in an insect. J Neurosci 21:3688–3696

    CAS  PubMed  Google Scholar 

  • Gomez-Martin A, Duistermars BJ, Frye MA, Matthieu LM (2010) Mechanisms of odor-tracking: multiple sensors for enhanced perception and behavior. Front Cell Neurosci 4:1–15

    Google Scholar 

  • Grieco J, Achee N, Sardelis M, Chauchan K, Roberts D (2005) A novel high-troughput screening system to evaluate the behavioural response of adult mosquitoes to chemical. J Am Mosquito Contr 21:404–411

    Article  CAS  Google Scholar 

  • Gupta RK, Bhattacharjee AK (2007) Discovery and design of new arthropod/insect repellents by computer-aided molecular modling. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. CRC Press, Taylor and Francis Group, New York, pp 195–228

  • Ha TS, Smith DP (2009) Odorant and pheromone receptors in insects. Front cell Neurosci 3(10):55–60

    Google Scholar 

  • Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160

    Article  CAS  PubMed  Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711

    Article  CAS  PubMed  Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4(4):266–275

    Article  CAS  PubMed  Google Scholar 

  • Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance inmosquitoes. Insect Biochem Mol Biol 34:653–665

    Article  CAS  PubMed  Google Scholar 

  • Hossaert-McKey M, Bagnères-Urbany AG (2012) Ecologie chimique le language de la nature. France, Le Cherche Midi, Chabreuil A. Lefabvre V

  • Hougard JM, Martin T, Guillet PF, Coosemans M, Itoh T, Akogbeto M, Chandre F (2007) Preliminary field testing of a long-lasting insecticide-treated hammock against Anopheles gambiae and Mansonia spp. (Diptera: Culicidae) in West Africa. J Med Entomol 44:651–655

    Article  PubMed  Google Scholar 

  • Irmisch S, Clavijo McCormick A, Günther J, Schmidt A, Boeckler GA, Gershenzon J, Unsicker SB, Köllner TG (2014) Herbivore-induced poplar cytochrome P450 enzymes of the CYP71 family convert aldoximes to nitriles which repel a generalist caterpillar. Plant J 80(6):1095–1107

    Article  CAS  PubMed  Google Scholar 

  • Isman MB (1994) Botanical insecticides and antifeedants: new sources and perspectives. Pestic Res J 849(6):11–19

    Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Ann Rev Entomol 51:45–56

    Article  CAS  Google Scholar 

  • Isono K, Morita H (2010) Molecular and cellular designs of insect taste receptor system. Front cell Neurosci 4:20

    PubMed  PubMed Central  Google Scholar 

  • Jefferis GS, Marin EC, Stocker RF, Luo L (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414(6860):204–208

    Article  CAS  PubMed  Google Scholar 

  • Jermy T (1990) Prospects of antifeedant approach to pest control—a critical review. J Chem Ecol 16:3151–3166

    Article  CAS  PubMed  Google Scholar 

  • Jilani G, Saxena RC (1990) Repellent and feeding deterrent effects of turmeric oil, sweetflag oil, neem oil, and a neem-based insecticide against lesser grain borer (Coleoptera: Bostrychidae). J Econ Entomol 83(2):629–634

    Article  Google Scholar 

  • Junker RR, Klupsch K, Paulus J (2015) Prior exposure to DEET interrupts positive and negative responses to olfactory cues in Drosophila melanogaster. J Insect Behav 28(1):1–14

    Article  Google Scholar 

  • Kain P, Boyle SM, Tharadra SK, Guda T, Pham C, Dahanukar A, Ray A (2013) Odour receptors and neurons for DEET and new insect repellents. Nature 000:1–8

    Google Scholar 

  • Kaupp UB (2010) Olfactory signaling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200

    CAS  PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  CAS  PubMed  Google Scholar 

  • Khan ZR, Pickett JA (2004) The “push-pull” strategy for stemborer management: a case study in exploiting biodiversity and chemical ecology. In: Gurr GM, Wratten SD, Altieri MA. ecological engineering for pest management: advances in habitat manipulation for arthropods. CABI, Wallington, pp 155–164

  • Khan ZR, Chiliswa P, Ampong-Nyarko K, Smart LE, Polaszek A, Wandera J, Mulaa MA (1997a) Utilisation of wild gramineous plants for management of cereal stemborers in Africa. Int J Trop Insect Sci 17:143–150

    Article  Google Scholar 

  • Khan ZR, Ampong-Nyarko K, Chiliswa P, Hassanali A, Kimani S, lwande WA, Overholt WA, Pickett JA, Smart LE, Woodcock CM (1997) Intercropping increases parasitism of pests. Nature 388:631–632

  • Kim SH (2013) Insect GPCRs and TRP channels: putative targets for insect repellents. Interdi Bio Central 6–12

  • Kimani SM, Chhabra SC, Lwande W, Khan ZR, Hassanali A, Pickett JA (2000) Airborne volatiles from Melinis minutiflora P. Beauv, a non-host plot of the two spotted stem borer. J Essent Oils Res 882(12):221–224

  • Knaden K, Strutz A, Ahsan J, Sachse S, Hansson BS (2012) Spatial representation of odorant valence in an insect brain. Cell 1:392–399

    CAS  Google Scholar 

  • Koul O (2008) Phytochemical and insect control: an antifeedant approach. Crit Rev Plant Sci 27:1–24

    Article  CAS  Google Scholar 

  • Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A 189:519–526

    Article  CAS  Google Scholar 

  • Kwon Y, Kim SH, Ronderos DS, Lee Y, Akitake B, Woodward OM, Guggino WB, Smith DP, Montell C (2010) Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr Biol 20:1672–1678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405(4):543–552

    Article  CAS  PubMed  Google Scholar 

  • Lam PYS, Frazier JL (1991) Rational approach to glucose taste chemoreceptor inhibitors as novel insect antifeedants. ACS Symp 443:400–412

    Article  CAS  Google Scholar 

  • Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    Article  CAS  PubMed  Google Scholar 

  • Leal WS (2007) Molecular-based chemical prospecting of mosquito attractants and repellents. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. CRC Press, Taylor and Francis Group, New York, pp 229–248

  • Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Ann Rev Entomol 58:373–391

    Article  CAS  Google Scholar 

  • Lee Y, Kim SH, Montell C (2010) Avoiding DEET through insect gustatory receptors. Neuron 67–61:903

    Google Scholar 

  • Mac Cain WC, Leach GJ (2007) Repellents used in fabric: the experience of the US military. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. Taylor and Francis Group, New York, pp 103–110

  • Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96(5):713–723

    Article  CAS  PubMed  Google Scholar 

  • Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285–295

    Article  CAS  PubMed  Google Scholar 

  • Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell 109(2):243–255

    Article  CAS  PubMed  Google Scholar 

  • Martel JW, Alford AR, Dickens JC (2005a) Laboratory and greenhouse evaluation oa synthetic host volatile attractant for Colorado potato beetle, Leptinotarsa decemlineata (Say). Agr For Entomol 7:71–78

    Article  Google Scholar 

  • Martel JW, Alford AR, Dickens JC (2005b) Synthetic host volatiles increase efficacy of trap cropping system for management of Colorado potato beetle, Leptinotarsa decemlineata (Say). Agr For Entomol 7:79–86

    Article  Google Scholar 

  • Martin T, Palix R, Kamal A, Deletre E, Bonafos R, Simon S, Ngouajio M (2013) A repellent net as a new technology to protect cabbage crop. J Econ Entomol 106:1699–1706

    Article  CAS  PubMed  Google Scholar 

  • Martin T, Gogo EO, Saidi M, Kamal A, Deletre E, Bonafos R, Simon S, Ngouajio M (2014) Repellent effect of an alphacypermethrin treated net against the whitefly Bemisia tabaci Gennadius. J Econ Entomol 107:684–690

    Article  CAS  PubMed  Google Scholar 

  • Matthews RW, Matthews JR (1978) Insect behavior. USA, Wiley, New York

    Google Scholar 

  • Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3:e305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Messchendorp L, Smid HM, Van Loon JJA (1998) The role of an epipharyngeal sensillum in the perception of feeding deterrents by Leptinotarsa decemlineata larvae. J Comp Physiol 183:255–264

    Article  Google Scholar 

  • Miller JR, Cowles RS (1990) Stimulo-deterrent diversion: a concept and its possible application to onion maggot control. J Chem Ecol 16:3197–3212

    Article  CAS  PubMed  Google Scholar 

  • Miller JR, Siegert PY, Amimo FA, Walker ED (2009) Designation of chemical in terms of the locomotor responses they elicit from insects: an update of Dethier et al. (1960). Ecol Behav.102:2056–2060

  • Montell C (2009) A taste of the Drosophila gustatory receptors. Curr Opin Neurobiol 19:345–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery ME, Nault LR (1977) Comparative response of aphids aphids to the alarm pheromone, (E)—ß farnesene. Entomol Exp Appl 22(3):236–242

    Article  CAS  Google Scholar 

  • Moore SJ, Debboun M (2007) History of insect repellent. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. CRC Press, Taylor and Francis Group, New York, 940:3–29

  • Moore SJ, Lenglet A, Hill N (2007) Plant-based insect repellents. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. CRC Press, Taylor and Francis Group, New York

  • Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642

    Article  CAS  PubMed  Google Scholar 

  • Nalyana G, Moore CB, Schal C (2000) Integration of repellents, attractants, and insecticides in a push pull strategy for managing the cockroach (Dictyoptera: Blatellidae) populations. J Med Entomol 37:427–434

    Google Scholar 

  • Narahashi T (1971) Mode of action of pyrethroids. Bull WHO 44:337–345

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nilsson E, Bengtsson G (2004) Endogenous free fat y acids repel and attract collembolan. J Chem Ecol 30:1431–1443

    Article  CAS  PubMed  Google Scholar 

  • Nolen JA, Bedoukian RH, Maloney RE, Kline DL (2002) Method, apparatus and compositions for inhibiting the human scent tracking ability of mosquitoes in environmentally defined three dimensional spaces. US Patent No. 6,362,235. Patent issued March 26, 2002

  • Nordlund DA (1981) Semiochemicals: a review of the terminology. In: Nordlund DA, Jones RL, Lewis WJ. Semiochemicals: their role in pest control. John Wiley and Sons, New York, pp 13–28

  • Pennetier C, Chabi J, Martin T, Chandre F, Rogier C, Hougard JM, Pages F (2010) New protective battle-dress impregnated against mosquito vector bites. Parasite Vector 3:81

    Article  Google Scholar 

  • Pettersson J (1970) An aphid sex attractant. Insect Syst Evol 1(1):63–73

    Article  Google Scholar 

  • Pickett JA, Wadhams LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Ann Rev 971 Entomol 37:67–90

  • Pike B, Rice M, Sabine B, Zalucki MP (1987) The push-pull strategy-behavioral control of Heliothis. Australian Cotton Grow, May-July, pp 7–9

    Google Scholar 

  • Ramirez GIJ, Logan JG, Loza-Reyes E, Stashenko E, Moores GD (2012) Repellents inhibit P450 enzymes in Stegomyia (Aedes aegypti). PLoS ONE 7:1–8

    Google Scholar 

  • Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27:91–98

    Article  CAS  PubMed  Google Scholar 

  • Ratnadass A, Frenandes P, Avelino J (2012) Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: a review. Agron Sust Dev 32:273–303

    Article  Google Scholar 

  • Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920

    Article  CAS  Google Scholar 

  • Raviv M, Antignus Y (2004) UV radiation effects on pathogens and insect pests of greenhouse-grown crops. Photochem Photobiol 79:219–226

    Article  CAS  PubMed  Google Scholar 

  • Ray A (2015) Reception of odors and repellents in mosquitoes. Curr Opin Neurobiol 34:158–164

    Article  CAS  PubMed  Google Scholar 

  • Regnault-Roger C (1997) The potential of botanical essential oils for insect pest control. Int Pest Manag Rev 2:25–34

    Article  Google Scholar 

  • Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Ann Rev Entomol 57:405–424

    Article  CAS  Google Scholar 

  • REX Consortium (2013) Heterogeneity of selection and the evolution of resistance. Trends Ecol Evol 28:110–118

    Article  Google Scholar 

  • Rodrigues V, Siddiqi O (1981) A gustatory mutant of Drosophila defective in pyranose receptors. Mol Gen Genet 181:406–408

    Article  CAS  PubMed  Google Scholar 

  • Sachse S, Galizia CG (2003) The coding of odor-intensivity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119–2132

    Article  PubMed  Google Scholar 

  • Sanford JL, Shields VDC, Dickens JC (2013) Gustatory receptor neuron responds to DEET and other insect repellents in the yellow fever mosquito, Aedes aegypti. Naturwissenschaften 100:269–273

    Article  CAS  PubMed  Google Scholar 

  • Saxena RC, Khan ZR (1985) Electronically recorded disturbance in feeding behavior of Nephotettix virescens (Homoptera: Cicadellidae) on neem oil-treated rice plants. J Econ Entomol 78:22–226

    Google Scholar 

  • Schoonhoven LM (1987) What makes a caterpillar eat? The sensory codes underlying feeding behaviour. In: Chapman RF, Bernays EA, Stoffo JG. Advances in Chemoreception and Behavior. Springer, New York, pp 69–97

  • Schoonhoven LM (1988) Stereoselective perception of antifeedants in insects. In: Ariens EJ, Van Rensen JJS, Welling W. Stereoselectivity of Pesticides: biological and Chemical Problems. Elsevier, Amsterdam, pp 289–302

  • Schoonhoven LM, Van Loon JJA (1988) Chemoreception and feeding behavior in a caterpillar: towards a model of brain functioning in insects. Entomol Exp Appl 49:123–129

    Article  Google Scholar 

  • Schoonhoven LM, Van Loon JJA (2002) An inventory of taste in caterpillars: each species its own key. Acta Zool Acad Sci H 48:215–263

    Google Scholar 

  • Schoonhoven LM, Blaney WM, Simmonds MSJ (1992) Sensory coding of feeding deterrents in phytophagous insects. In: Bernays EA. insect-plant interactions: feeding and oviposition. CRC Press, Boca Raton, pp 59–79

  • Schrek CE (1977) Techniques for the evaluation of insect repellents: a critical review. Ann Rev Entomol 22:101–119

    Article  Google Scholar 

  • Séjourné J, Plaçais PY, Aso Y, Siwanowicz I, Trannoy S, Thoma V, Tedjakumala SR, Rubin GM, Tchénio P, Ito K, Isabel G, Tanimoto H, Preat T (2011) Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in drosophila. Nat Neurosci 14-903–910

  • Semmelhack JL, Wang JW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459:218–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegert PY, Walker E, Miller JR (2009) Differential behavioral responses of Anopheles gambiae (Diptera: Culicidae) modulate mortality caused by pyrethroid-treated bednets. J Econ Entomolol 102:2061–2071

    Article  CAS  Google Scholar 

  • Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27(44):11966–11977

    Article  CAS  PubMed  Google Scholar 

  • Smith HA, McSorley R (2000) Potential of field corn as barrier crop and eggplant as a trap crop for management of Bemisia argentifolii (Homoptera: Aleyrodidae) on common bean in north Florida. Fla Entomol 83:145–158

    Article  Google Scholar 

  • Steck K, Veit D, Grandy R, Bermudez i, Badia S, Mathews Z, Verschure P, Hansson BS, Knaden M (2012) A high-throughput behavioral paradigm for Drosophila olfaction—the Flywalk. Nat Sci Re. 1031(2):1–9

  • Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista- Llanos S, Wicher D, Sachse S, Knaden M, Becher PG, Seki Y, Hansson BS (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357

    Article  CAS  PubMed  Google Scholar 

  • Sturcow B (1959) Ueber den Geschmackssinn und den Tastinn von Leptinotarsa decemlineata Say (Chrysomelidae). Z Vergl Physiol 42:255–302

    Google Scholar 

  • Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854–859

    Article  CAS  PubMed  Google Scholar 

  • Suh E, Bohbot JZ, Zwiebel LJ (2014) Peripheral olfactory signaling in insects. Curr Opin Insect Sci 6:86–92

    Article  PubMed  PubMed Central  Google Scholar 

  • Syed Z, Leal WS (2008) Mosquitoes smell and avoid the insect repellent DEET. PNAS 36:13598–13603

    Article  Google Scholar 

  • Tauxe GM, MacWilliam D, Boyle SM, Guda T, Ray A (2013) Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155:1365–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawatsin A, Wratten SD, Scott RD, Thavara U, Techadamrongsin Y (2001) Repellency of volatile oils from plants against three mosquito vectors. J Vector Ecol 26:76–82

    CAS  PubMed  Google Scholar 

  • Temu EA, Maxwell C, Munyekenye G, Howard AFV, Munga S, Avicor SW, Poupardin R, Jones JJ, Allan R, Kleinschimidt I, Ranson H (2013) Pyrethroid resistance in Anopheles gambiae, in Bomi County, Liberia, compromises malaria vector control. PLoS ONE 7:9

    Google Scholar 

  • Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14:1065–1079

    Article  CAS  PubMed  Google Scholar 

  • Thorsteinson AJ (1960) Host selection in phytophagous insects. Ann Rev Entomol 5:193–218

    Article  Google Scholar 

  • Togni P, Laumann R, Medeiros M, Sujii E (2010) Odour masking of tomatoe volatiles in host plant selection of Bemisia tabaci biotype B. Entomol Exp Appl 136:164–173

    Article  Google Scholar 

  • Tosh CR, Brogan B. 2014. Control of tomato whiteflies using the confusion effect of plant odours. Agron Sustain Dev 1–11

  • Touhara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Ann Rev Physiol 71:307–332

    Article  CAS  Google Scholar 

  • Tsitoura P, Koussis K, Iatrou K (2015) Inhibition of Anopheles gambiae odorant receptor function by mosquito repellents. J Biol Chem 290(12):7961–7972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turlings TCJ, Gouinguené S, Degen T, Fritzsche-Hoballah ME (2002) The chemical ecology of plant-caterpillar–parasitoid interactions. In: Tscharntke T, Hawkins BA. Multitrophic level interactions. Cambridge University Press, Cambridge, pp 148–173

  • Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Op Plant Biol 12:479–485

    Article  CAS  Google Scholar 

  • Van Mele P, Vayssieres JF, Adandonon A, Sinzogan A (2009) Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa. Physiol Entomol 34:256–261

    Article  Google Scholar 

  • Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991

    Article  CAS  PubMed  Google Scholar 

  • Vet LE, Lenteren JV, Heymans M, Meelis E (1983) An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol Entomol 8(1):97–106

    Article  Google Scholar 

  • Visser JH (1988) Host-plant finding by insects—orientation, sensory input and search patterns. J Insect Physiol 34:259–268

    Article  Google Scholar 

  • Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163

    Article  CAS  PubMed  Google Scholar 

  • Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Sens 36(6):497–498

    Article  Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophilla. Ann Rev Neurosci 30:505–533

    Article  CAS  PubMed  Google Scholar 

  • Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159

    Article  CAS  PubMed  Google Scholar 

  • Wada-Katsumata A, Silverman J, Schal C (2013) Changes in taste neuron support the emergence of an adaptative behavior in cockroaches. Science 340:972–975

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981–991

    Article  CAS  PubMed  Google Scholar 

  • Warthen JD, Morgan ED (1990) Insect feeding deterrents. In: Morgan ED, Mandava NB. CRC Handbook of natural pesticide, Boca Raton, pp 23–134

  • Webster B, Bruce T, Pickett J, Hardie J (2010) Volatiles functioning as host cues in a blend odor become nonhost cues when presented alone to the black bean aphid. Anim Behav 79:451–457

    Article  Google Scholar 

  • Weintraub PG (2009) Physical control: an important tool in pest management programs. In: Ishaaya I, Horowitz AR. Biorational control of arthropods pests. Springer Science, Amsterdan

  • White GB (2007) Terminology of insect repellents, Chapter 2. In: Debboun M, Frances SP, Strickman D. Insect repellents: principles, methods and uses. CRC Press, Taylor and Francis Group, New York

  • WHO (2002) Scaling-up insecticide-treated netting programs in Africa. WHO/CDS/RBM/2002.43

  • WHO (2013) Guidelines for efficacy testing of spatial repellent, Control of neglected tropical diseases. WHO pesticide evaluation scheme, p 58

  • Yadouleton A, Martin T, Padonou G, Chandre F, Asidi A, Djogbenou L, Dabire R, Aikpon R, Boko M, Glitho I, Akogbeto M (2011) Cotton pest management practices and the selection of pyrethroid resistance in Anopheles gambiae population in Northern Benin. Parasite Vector 4:60–69

    Article  Google Scholar 

  • Yarmolinsky DA, Zuker CS, Ryba NJ (2009) Common sense about taste: from mammals to insects. Cell 139:234–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaim M, Aitio A, Nakashima N (2000) Safety of pyrethroid-treated mosquito nets. Med Vet Entomol 14:1–5

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The work was supported by CIRAD, IRD and MUTAVIE, Paris, France.

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Deletre, E., Schatz, B., Bourguet, D. et al. Prospects for repellent in pest control: current developments and future challenges. Chemoecology 26, 127–142 (2016). https://doi.org/10.1007/s00049-016-0214-0

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