Skip to main content
Log in

Bitter-sensitive gustatory receptor neuron responds to chemically diverse insect repellents in the common malaria mosquito Anopheles quadrimaculatus

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Female mosquitoes feed on blood from animal hosts to obtain nutritional resources used for egg production. These contacts facilitate the spread of harmful human diseases. Chemical repellents are used to disrupt mosquito host-seeking and blood-feeding behaviors; however, little is known about the gustatory sensitivity of mosquitoes to known repellents. Here, we recorded electrical responses from gustatory receptor neurons (GRNs) housed within the labellar sensilla of female Anopheles quadrimaculatus to N,N-diethyl-3-methylbenzamide (DEET), picaridin, IR3535, 2-undecanone, p-menthane-3,8-diol, geraniol, trans-2-hexen-1-ol, quinine, and quinidine. A bitter-sensitive GRN responded to all tested repellents and quinine, a known feeding deterrent. Responses of the bitter-sensitive neuron to quinine and an isomer, quinidine, did not differ. Delayed bursts of electrical activity were observed in response to continuous stimulation with synthetic repellents at high concentrations. Electrophysiological recordings from bitter-sensitive GRNs associated with mosquito gustatory sensilla represent a convenient model to evaluate candidate repellents.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ali A, Demirci B, Kiyan HT, Bernier UR, Tsikolia M, Wedge DE, Khan IA, Baser KHC, Tabanca N (2013) Biting deterrence, repellency, and larvicidal activity of Ruta chalepensis (Sapindales: Rutaceae) essential oil and its major individual constituents against mosquitoes. J Med Entomol 50:1267–1274

    Article  CAS  PubMed  Google Scholar 

  • Barasa SS, Ndiege IO, Lwande W, Hassanali A (2002) Repellent activities of stereoisomers of p-menthane-3,8-diols against Anopheles gambiae (Diptera: Culicidae). J Med Entomol 39:736–741

    Article  CAS  PubMed  Google Scholar 

  • Barton VM (2003) Trypsin modulating oostatic factor (TMOF) and non-peptidic analogs as novel insecticides and arthropod repellents. MSc thesis, North Carolina State University pp vii + 76

  • Boeckh J, Breer H, Geier MM, Hoever F, Kruger B, Nentwig G, Sass H (1996) Acylated 1,3-aminopropanols as repellents against bloodsucking arthropods. Pestic Sci 48:359–373

    Article  CAS  Google Scholar 

  • Bohbot JD, Dickens JC (2010) Insect repellents: modulators of mosquito odorant receptor activity. PLoS One 5:e12138

    Article  PubMed  PubMed Central  Google Scholar 

  • Carroll SP, Loye J (2006) PMD, a registered botanical mosquito repellent with DEET–like efficacy. J Am Mosq Control Assoc 22:507–514

    Article  PubMed  Google Scholar 

  • Clements AN (1992) The biology of mosquitoes: volume 1. Madras: Chapman & Hall, London, Glasgow, New York, Tokyo, Melbourne, pp 220–250

  • Clements AN (1999) The biology of mosquitoes: volume 2. CABI Publishing, Wallingford, pp 502–519

    Google Scholar 

  • Curtis CF, Lines JD, Lu B, Renz A (1991) Natural and synthetic repellents. In: Curtis CF (ed) Control of disease vector in the community. Wolfe Publishing Ltd, London, pp 75–92

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Debboun M, Frances SP, Strickman D (2014) Insect repellents handbook. CRC Press, Boca Raton

    Google Scholar 

  • DeGennaro 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  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Foster WA (1995) Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol 40:443–474

  • French AS, Sellier M-J, Moutaz AA, Guigue A, Chabaud MA, Reeb PD, Mitra A, Grau Y, Soustelle L, Marion-Poll F (2015) Dual mechanism for bitter avoidance in Drosophila. J Neurosci 35:3990–4004

    Article  CAS  PubMed  Google Scholar 

  • Guha L, Seenivasagan T, Tanvir Iqbal S, Agrawal OP, Parashar BD (2014) Behavioral and electrophysiological responses of Aedes albopictus to certain acids and alcohols present in human skin emanations. Parasitol Res 113:3781–3787

    Article  PubMed  Google Scholar 

  • Hodgson ES, Lettvin JY, Roeder KD (1955) The physiology of a primary chemoreceptor unit. Science 122:417–418

    Article  CAS  PubMed  Google Scholar 

  • Isono K, Morita H (2010) Molecular and cellular designs of insect taste receptor system. Front Cellu Neurosci 4:1–16

    Google Scholar 

  • Jeong YT, Shim J, Oh SR, Yoon HI, Kim CH, Moon SJ, Montell C (2013) An odorant-binding protein required for suppression of sweet taste by bitter chemicals. Neuron 79:725–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones PL, Pask GM, Rinker DC, Zwiebel LJ (2011) Functional agonism of insect odorant receptor ion channels. Proc Natl Acad Sci USA 108:8821–8825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler S, Vlimant M, Guerin PM (2013) The sugar meal of the African malaria mosquito Anopheles gambiae and how deterrent compounds interfere with it: a behavioural and neurophysiological study. J Exp Biol 216:1292–1306

    Article  CAS  PubMed  Google Scholar 

  • Kessler S, González J, Vlimant M, Glauser G, Guerin PM (2014) Quinine and artesunate inhibit feeding in the African malaria mosquito Anopheles gambiae: the role of gustatory organs within the mouthparts. Physiol Entomol 39:172–182

    Article  CAS  Google Scholar 

  • Klun JA, Khrimian A, Debboun M (2006) Repellent and deterrent effects of SS220, picaridin, and DEET suppress human blood feeding by Aedes aegypti, Anopheles stephensi, and Phlebotomus papatasi. J Med Entomol 43:34–39

    CAS  PubMed  Google Scholar 

  • Kuthiala A, Gupta RK, Davis EE (1992) Effect of the repellent DEET on the antennal chemoreceptors for oviposition in Aedes aegypti (Diptera: Culicidae). J Med Entomol 29:639–643

    Article  CAS  PubMed  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 

  • Lee Y, Kim SH, Montell C (2010) Avoiding DEET through insect gustatory receptors. Neuron 67:555–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Licciardi S, Herve JP, Darriet F, Hougard JM, Corbel V (2006) Lethal and behavioural effects of three synthetic repellents (DEET, IR3535, and KBR 3023) on Aedes aegypti mosquitoes in laboratory assays. Med Vet Entomol 20:288–293

    Article  CAS  PubMed  Google Scholar 

  • Lupi E, Hatz C, Schlagenhauf P (2013) The efficacy of repellents against Aedes, Anopheles, Culex and Ixodes spp.—a literature review. Travel Med Infect Dis 11:374–411

    Article  PubMed  Google Scholar 

  • Maia MF, Moore SJ (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malaria J 10:S11

    Article  CAS  Google Scholar 

  • Manguin S, Carnivale P, Mouchet J (2008) Biodiversity of Malaria in the World. Libbey J (ed), Eurotext, Paris

  • Marchio F (1996) Insect repellent 3535 a new alternative to DEET. SÖFW-J 122:478–485

    CAS  Google Scholar 

  • Robert LL, Santos-Ciminera PD, Andre RG, Schultz GW, Lawyer PG, Nigro J, Masuoka P, Wirtz RA, Neely J, Gaines D, Cannon CE, Pettit D, Garvey CW, Goodfriend D, Roberts DR (2005) Plasmodium-infected Anopheles mosquitoes collected in Virginia and Maryland following local transmission of Plasmodium vivax malaria in Loudoun County, Virginia. J Am Mosq Control Assoc 21:187–193

    Article  PubMed  Google Scholar 

  • Roe RM (2004) Method of repelling insects. US patent application 20040242703, Kind Code A1

  • 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 

  • Schreck CE, Gilbert IH, Weidhaas DE, Posey KH (1970) Spatial action of mosquito repellents. J Econ Entomol 63:1576–1578

    Article  CAS  PubMed  Google Scholar 

  • Sparks JT, Dickens JC (2016) Electrophysiological responses of gustatory receptor neurons on the labella of the common malaria mosquito Anopheles quadrimaculatus Say (Diptera: Culicidae). J Med Entomol (In press)

  • Syed Z, Leal WS (2008) Mosquitoes smell and avoid the insect repellent DEET. Proc Natl Acad Sci USA 105:13598–13603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trigg JK (1996) Evaluation of eucalyptus-based repellent against Anopheles spp in Tanzania. J Am Mosq Control Assoc 12:243–246

    CAS  PubMed  Google Scholar 

  • Tsitoura P, Koussis K, Iatrou K (2015) Inhibition of Anopheles gambiae odorant receptor function by mosquito repellents. J Biol Chem. doi:10.1074/jbc.M114.632299

    PubMed  PubMed Central  Google Scholar 

  • Weldon PJ, Kramer C, Coleman B, Bernier U (2011) Anointing chemicals and hematophagous arthropods: responses by ticks and mosquitoes to citrus (Rutaceae) peel exudates and monoterpene components. J Chem Ecol 37:348–359

    Article  CAS  PubMed  Google Scholar 

  • Witting-Bissinger BE, Stumpf CF, Donohue KV, Apperson CS, Roe RM (2008) Novel arthropod repellent, BioUD, is an efficacious alternative to deet. J Med Entomol 45:891–898

    Article  CAS  PubMed  Google Scholar 

  • Xia Y, Wang G, Buscariollo D, Pitts RJ, Wenger H, Zwiebel LJ (2008) The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proc Natl Acad Sci USA 105:6433–6438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu P, Choo Y, De La Rosa A, Leal WS (2014) Mosquito odorant receptor for DEET and methyl jasmonate. Proc Natl Acad Sci USA 111:16592–16597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported in part by a grant to J.C.D. from the Deployed War Fighter Protection (DWFP) Research Program funded by the Department of Defense through the Armed Forces Pest Management Board (AFPMB). The authors are thankful for a critical review provided by Dr. Jonathan D. Bohbot, Department of Entomology, The Hebrew University, Rehovot, Israel.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph C. Dickens.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sparks, J.T., Dickens, J.C. Bitter-sensitive gustatory receptor neuron responds to chemically diverse insect repellents in the common malaria mosquito Anopheles quadrimaculatus . Sci Nat 103, 39 (2016). https://doi.org/10.1007/s00114-016-1367-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-016-1367-y

Keywords

Navigation