Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant Anopheles gambiae

10.24072/pcjournal.15 - Peer Community Journal, Volume 1 (2021), article no. e28.

Get full text PDF Peer reviewed and recommended by PCI

The massive use of insecticide-treated nets (ITNs) has drastically changed the environment for malaria vector mosquitoes, challenging their host-seeking behaviour and biting success. Here, we investigated the effect of a brief exposure to an ITN on the biting behaviour of Anopheles gambiae mosquitoes and the interaction between such behaviour and the kdr mutation that confers resistance to pyrethroids. To this aim, we developed a video assay to study the biting behaviour of mosquitoes with similar genetic background, but different kdr locus genotypes (SS i.e. homozygous susceptible, RS i.e. heterozygous and RR i.e. homozygous resistant), after a brief exposure to either control untreated nets or one of two types of pyrethroid-treated nets (deltamethrin or permethrin). In presence of untreated nets, the kdr mutation did not influence mosquito blood feeding success but caused differences in feeding and prediuresis durations and blood meal size. Exposure to deltamethrin ITN decreased the blood feeding success rate of RR and RS mosquitoes, whereas in presence of permethrin ITN, the kdr mutation increased the blood-feeding success of mosquitoes. Exposure to the two types of pyrethroid-treated nets reduced feeding duration, prediuresis duration and blood meal size of all three genotypes. Our study demonstrates a complex interaction between insecticide exposure and the kdr mutation on the biting behavior of mosquitoes, which may substantially impact malaria vector fitness and disease transmission.

Published online:
DOI: 10.24072/pcjournal.15
Diop, Malal M 1; Chandre, Fabrice 1; Rossignol, Marie 1; Porciani, Angélique 1; Chateau, Mathieu 1; Moiroux, Nicolas 1, 2; Pennetier, Cédric 1, 3

1 MIVEGEC, Univ Montpellier, CNRS, IRD, Montpellier, France
2 Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso
3 Institut Pierre Richet (IPR), Bouaké, Côte d’Ivoire
     author = {Diop, Malal M and Chandre, Fabrice and Rossignol, Marie and Porciani, Ang\'elique and Chateau, Mathieu and Moiroux, Nicolas and Pennetier, C\'edric},
     title = {Sub-lethal insecticide exposure affects host biting efficiency of {Kdr-resistant} {<i>Anopheles} gambiae</i>},
     journal = {Peer Community Journal},
     eid = {e28},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.15},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.15/}
TI  - Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant <i>Anopheles gambiae</i>
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.15/
UR  - https://doi.org/10.24072/pcjournal.15
DO  - 10.24072/pcjournal.15
ID  - 10_24072_pcjournal_15
ER  - 
%0 Journal Article
%T Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant <i>Anopheles gambiae</i>
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.15
%R 10.24072/pcjournal.15
%F 10_24072_pcjournal_15
Diop, Malal M; Chandre, Fabrice; Rossignol, Marie; Porciani, Angélique; Chateau, Mathieu; Moiroux, Nicolas; Pennetier, Cédric. Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant Anopheles gambiae. Peer Community Journal, Volume 1 (2021), article  no. e28. doi : 10.24072/pcjournal.15. https://peercommunityjournal.org/articles/10.24072/pcjournal.15/

Peer reviewed and recommended by PCI : 10.24072/pci.zool.100003

[1] Alout, H.; Djègbè, I.; Chandre, F.; Djogbénou, L. S.; Dabiré, R. K.; Corbel, V.; Cohuet, A. Insecticide exposure impacts vector–parasite interactions in insecticide-resistant malaria vectors, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1786 | Article

[2] Alout, H.; Ndam, N. T.; Sandeu, M. M.; Djégbe, I.; Chandre, F.; Dabiré, R. K.; Djogbénou, L. S.; Corbel, V.; Cohuet, A. Insecticide Resistance Alleles Affect Vector Competence of Anopheles gambiae s.s. for Plasmodium falciparum Field Isolates, PLoS ONE, Volume 8 (2013) no. 5 | Article

[3] Alout, H.; Yameogo, B.; Djogbenou, L. S.; Chandre, F.; Dabire, R. K.; Corbel, V.; Cohuet, A. Interplay Between Plasmodium Infection and Resistance to Insecticides in Vector Mosquitoes, Journal of Infectious Diseases, Volume 210 (2014) no. 9, pp. 1464-1470 | Article

[4] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Usinglme4, Journal of Statistical Software, Volume 67 (2015) no. 1, pp. 1-48 | Article

[5] Berticat, C.; Boquien, G.; Raymond, M.; Chevillon, C. Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes, Genetical Research, Volume 79 (2002) no. 1, pp. 41-47 | Article

[6] Briegel, H. Fecundity, Metabolism, and Body Size in Anopheles (Diptera: Culicidae), Vectors of Malaria, Journal of Medical Entomology, Volume 27 (1990) no. 5, pp. 839-850 | Article

[7] Briegel, H.; Lea, A. O.; Klowden, M. J. Hemoglobinometry as a Method for Measuring Blood Meal Sizes of Mosquitoes (Diptera: Culicidae)1, Journal of Medical Entomology, Volume 15 (1979) no. 3, pp. 235-238 | Article

[8] Briegel, H.; Rezzonico, L. Concentration of Host Blood Protein During Feeding by Anopheline Mosquitoes (Diptera: Culicidae)1, Journal of Medical Entomology, Volume 22 (1985) no. 6, pp. 612-618 | Article

[9] Brooks, M.; Kristensen, K.; Benthem, K.; Magnusson, A.; Berg, C.; Nielsen, A.; Skaug, H.; Mächler, M.; Bolker, B. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling, The R Journal, Volume 9 (2017) no. 2, pp. 378-400 | Article

[10] Carrasco, D.; Lefèvre, T.; Moiroux, N.; Pennetier, C.; Chandre, F.; Cohuet, A. Behavioural adaptations of mosquito vectors to insecticide control, Current Opinion in Insect Science, Volume 34 (2019), pp. 48-54 | Article

[11] Cator, L. J.; George, J.; Blanford, S.; Murdock, C. C.; Baker, T. C.; Read, A. F.; Thomas, M. B. ‘Manipulation’ without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1763 | Article

[12] Cator, L. J.; Lynch, P. A.; Read, A. F.; Thomas, M. B. Do malaria parasites manipulate mosquitoes?, Trends in Parasitology, Volume 28 no. 11, pp. 466-470 | Article

[13] Chandre, F.; Darriet, F.; Duchon, S.; Finot, L.; Manguin, S.; Carnevale, P.; Guillet, P. Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae, Medical and Veterinary Entomology, Volume 14 (2000) no. 1, pp. 81-88 | Article

[14] Chouaïbou, M. S.; Fodjo, B. K.; Fokou, G.; Allassane, O. F.; Koudou, B. G.; David, J.-P.; Antonio-Nkondjio, C.; Ranson, H.; Bonfoh, B. Influence of the agrochemicals used for rice and vegetable cultivation on insecticide resistance in malaria vectors in southern Côte d’Ivoire, Malaria Journal, Volume 15 (2016) no. 1, p. 426 | Article

[15] Colvard Jones, J.; Madhukar, B. Effects of sucrose in blood avidity in mosquitoes, Journal of Insect Physiology, Volume 22 (1976) no. 3, pp. 357-360 | Article

[16] Corbel, V.; Chabi, J.; Dabiré, R. K.; Etang, J.; Nwane, P.; Pigeon, O.; Akogbeto, M.; Hougard, J.-M. Field efficacy of a new mosaic long-lasting mosquito net (PermaNet® 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa, Malaria Journal, Volume 9 (2010) no. 1, p. 113 | Article

[17] Corbel, V.; Chandre, F.; Brengues, C.; Akogbéto, M.; Lardeux, F.; Hougard, J.; Guillet, P. Malaria Journal, 3 (2004) no. 1 | Article

[18] Corbel, V.; N’Guessan, R. Distribution, Mechanisms, Impact and Management of Insecticide Resistance in Malaria Vectors: A Pragmatic Review, Anopheles mosquitoes - New insights into malaria vectors, InTech, Rijeka, 2013, pp. 579-633 | Article

[19] Dana, A. N.; Hong, Y. S.; Kern, M. K.; Hillenmeyer, M. E.; Harker, B. W.; Lobo, N. F.; Hogan, J. R.; Romans, P.; Collins, F. H. Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae, BMC Genomics, Volume 6 (2005) no. 1, p. 5 | Article

[20] Desneux, N.; Decourtye, A.; Delpuech, J.-M. The Sublethal Effects of Pesticides on Beneficial Arthropods, Annual Review of Entomology, Volume 52 (2007) no. 1, pp. 81-106 | Article

[21] Diop, M. M.; Moiroux, N.; Chandre, F.; Martin-Herrou, H.; Milesi, P.; Boussari, O.; Porciani, A.; Duchon, S.; Labbé, P.; Pennetier, C. Behavioral Cost & Overdominance in Anopheles gambiae, PLOS ONE, Volume 10 (2015) no. 4 | Article

[22] Firth, D. Bias reduction of maximum likelihood estimates, Biometrika, Volume 80 (1993) no. 1, pp. 27-38 | Article

[23] Garrett-Jones, C.; Shidrawi, G. R. Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology, Bulletin of the World Health Organization, Volume 40 (1969) no. 4, pp. 531-545

[24] Gatton, M. L.; Chitnis, N.; Churcher, T.; Donnelly, M. J.; Ghani, A. C.; Godfray, H. C. J.; Gould, F.; Hastings, I.; Marshall, J.; Ranson, H.; Rowland, M.; Shaman, J.; Lindsay, S. W. The importance of mosquito behavioural adaptations to malaria control in Africa, Evolution, Volume 67 (2013) no. 4, pp. 1218-1230 | Article

[25] Glunt, K. D.; Coetzee, M.; Huijben, S.; Koffi, A. A.; Lynch, P. A.; N'Guessan, R.; Oumbouke, W. A.; Sternberg, E. D.; Thomas, M. B. Empirical and theoretical investigation into the potential impacts of insecticide resistance on the effectiveness of insecticide‐treated bed nets, Evolutionary Applications, Volume 11 (2017) no. 4, pp. 431-441 | Article

[26] Harrell, F. w. c. f. C. D. a. m. o., Available from: https://CRAN.R-project.org/package=Hmisc, 2019

[27] Hauser, G.; Thiévent, K.; Koella, J. C. The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness, Scientific Reports, Volume 9 (2019) no. 1 | Article

[28] Haynes, K. F. Sublethal Effects of Neurotoxic Insecticides on Insect Behavior, Annual Review of Entomology, Volume 33 (1988) no. 1, pp. 149-168 | Article

[29] Hemingway, J.; Hawkes, N. J.; McCarroll, L.; Ranson, H. The molecular basis of insecticide resistance in mosquitoes, Insect Biochemistry and Molecular Biology, Volume 34 (2004) no. 7, pp. 653-665 | Article

[30] Jones, M. D. R.; Gubbins, S. J. Changes in the circadian flight activity of the mosquito Anopheles gambiae in relation to insemination, feeding and oviposition, Physiological Entomology, Volume 3 (1978) no. 3, pp. 213-220 | Article

[31] Killeen, G. F.; McKenzie, F.; Foy, B. D.; Bøgh, C.; Beier, J. C. The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by African mosquito populations, Transactions of the Royal Society of Tropical Medicine and Hygiene, Volume 95 (2001) no. 5, pp. 469-476 | Article

[32] Kosmidis, I., Available from: https://CRAN.R-project.org/package=brglm2, 2019

[33] Lahondère, C.; Lazzari, C. R. Mosquitoes Cool Down during Blood Feeding to Avoid Overheating, Current Biology, Volume 22 (2012) no. 1, pp. 40-45 | Article

[34] Lahondère, C.; Lazzari, C. R. Thermal Stress and Thermoregulation During Feeding in Mosquitoes, Anopheles mosquitoes - New insights into malaria vectors, InTechOpen, 2013 | Article

[35] Lefèvre, T.; Gouagna, L.-C.; Dabire, K. R.; Elguero, E.; Fontenille, D.; Costantini, C.; Thomas, F. Evolutionary lability of odour-mediated host preference by the malaria vectorAnopheles gambiae, Tropical Medicine & International Health, Volume 14 (2009) no. 2, pp. 228-236 | Article

[36] Lefèvre, T.; Thomas, F.; Renaud, F.; Elguero, E.; Fontenille, D.; Gouagna, L.-C.; Dabiré, K. R.; Costantini, C. Beyond Nature and Nurture: Phenotypic Plasticity in Blood-Feeding Behavior of Anopheles gambiae s.s. When Humans Are Not Readily Accessible, The American Journal of Tropical Medicine and Hygiene, Volume 81 (2009) no. 6, pp. 1023-1029 | Article

[37] Lefevre, T.; Ohm, J.; Dabiré, K. R.; Cohuet, A.; Choisy, M.; Thomas, M. B.; Cator, L. Transmission traits of malaria parasites within the mosquito: Genetic variation, phenotypic plasticity, and consequences for control, Evolutionary Applications, Volume 11 (2018) no. 4, pp. 456-469 | Article

[38] Lenth, R.; Singmann, H.; Love, J.; Buerkner, P.; Herve, M., Available from: https://CRAN.R-project.org/package=emmeans, 2019

[39] Liu, N. Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research Directions, Annual Review of Entomology, Volume 60 (2015) no. 1, pp. 537-559 | Article

[40] Lyimo, I. N.; Ferguson, H. M. Ecological and evolutionary determinants of host species choice in mosquito vectors, Trends in Parasitology, Volume 25 (2009) no. 4, pp. 189-196 | Article

[41] Lyimo, I. N.; Haydon, D. T.; Mbina, K. F.; Daraja, A. A.; Mbehela, E. M.; Reeve, R.; Ferguson, H. M. The fitness of African malaria vectors in the presence and limitation of host behaviour, Malaria Journal, Volume 11 (2012) no. 1, p. 425 | Article

[42] Mathenge, E. M.; Gimnig, J. E.; Kolczak, M.; Ombok, M.; Irungu, L. W.; Hawley, W. A. Effect of Permethrin-Impregnated Nets on Exiting Behavior, Blood Feeding Success, and Time of Feeding of Malaria Mosquitoes (Diptera: Culicidae) in Western Kenya, Journal of Medical Entomology, Volume 38 (2001) no. 4, pp. 531-536 | Article

[43] Moiroux, N. Code and data to reproduce analyses in Diop et al. 2019, 2020 | Article

[44] Moiroux, N.; Damien, G. B.; Egrot, M.; Djenontin, A.; Chandre, F.; Corbel, V.; Killeen, G. F.; Pennetier, C. Human Exposure to Early Morning Anopheles funestus Biting Behavior and Personal Protection Provided by Long-Lasting Insecticidal Nets, PLoS ONE, Volume 9 (2014) no. 8 | Article

[45] Moiroux, N.; Gomez, M. B.; Pennetier, C.; Elanga, E.; Djènontin, A.; Chandre, F.; Djègbé, I.; Guis, H.; Corbel, V. Changes in Anopheles funestus Biting Behavior Following Universal Coverage of Long-Lasting Insecticidal Nets in Benin, The Journal of Infectious Diseases, Volume 206 (2012) no. 10, pp. 1622-1629 | Article

[46] N’Guessan, R.; Asidi, A.; Boko, P.; Odjo, A.; Akogbeto, M.; Pigeon, O.; Rowland, M. An experimental hut evaluation of PermaNet® 3.0, a deltamethrin–piperonyl butoxide combination net, against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes in southern Benin, Transactions of the Royal Society of Tropical Medicine and Hygiene, Volume 104 (2010) no. 12, pp. 758-765 | Article

[47] N’Guessan, R.; Corbel, V.; Akogbéto, M.; Rowland, M. Reduced Efficacy of Insecticide-treated Nets and Indoor Residual Spraying for Malaria Control in Pyrethroid Resistance Area, Benin, Emerging Infectious Diseases, Volume 13 (2007) no. 2, pp. 199-206 | Article

[48] O'Reilly, A. O.; Khambay, B. P. S.; Williamson, M. S.; Field, L. M.; WAllace, B. A.; Davies, T. G. E. Modelling insecticide-binding sites in the voltage-gated sodium channel, Biochemical Journal, Volume 396 (2006) no. 2, pp. 255-263 | Article

[49] Parker, J. E. A.; Angarita Jaimes, N. C.; Gleave, K.; Mashauri, F.; Abe, M.; Martine, J.; Towers, C. E.; Towers, D.; McCall, P. J. Host-seeking activity of a Tanzanian population of Anopheles arabiensis at an insecticide treated bed net, Malaria Journal, Volume 16 (2017) no. 1, p. 270 | Article

[50] Parker, J. E.; Angarita-Jaimes, N.; Abe, M.; Towers, C. E.; Towers, D.; McCall, P. J. Infrared video tracking of Anopheles gambiae at insecticide-treated bed nets reveals rapid decisive impact after brief localised net contact, Scientific Reports, Volume 5 (2015) no. 1 | Article

[51] Pates, H.; Curtis, C. Mosquito behavior and vector control, Annual Review of Entomology, Volume 50 (2005) no. 1, pp. 53-70 | Article

[52] Porciani, A.; Diop, M.; Moiroux, N.; Kadoke-Lambi, T.; Cohuet, A.; Chandre, F.; Dormont, L.; Pennetier, C. Influence of pyrethroïd-treated bed net on host seeking behavior of Anopheles gambiae s.s. carrying the kdr allele, PLOS ONE, Volume 12 (2017) no. 7 | Article

[53] Poupardin, R.; Riaz, M. A.; Jones, C. M.; Chandor-Proust, A.; Reynaud, S.; David, J.-P. Do pollutants affect insecticide-driven gene selection in mosquitoes? Experimental evidence from transcriptomics, Aquatic Toxicology, Volume 114-115 (2012), pp. 49-57 | Article

[54] R Development Core Team, , R Foundation for Statistical Computing, Vienna, Austria, 2018

[55] Ranson, H.; N’Guessan, R.; Lines, J.; Moiroux, N.; Nkuni, Z.; Corbel, V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control?, Trends in Parasitology, Volume 27 (2011) no. 2, pp. 91-98 | Article

[56] Raphemot, R.; Rouhier, M. F.; Hopkins, C. R.; Gogliotti, R. D.; Lovell, K. M.; Hine, R. M.; Ghosalkar, D.; Longo, A.; Beyenbach, K. W.; Denton, J. S.; Piermarini, P. M. Eliciting Renal Failure in Mosquitoes with a Small-Molecule Inhibitor of Inward-Rectifying Potassium Channels, PLoS ONE, Volume 8 (2013) no. 5 | Article

[57] Roitberg, B. D. Pouncing spider, flying mosquito: blood acquisition increases predation risk in mosquitoes, Behavioral Ecology, Volume 14 (2003) no. 5, pp. 736-740 | Article

[58] Rund, S. S. C.; Hou, T. Y.; Ward, S. M.; Collins, F. H.; Duffield, G. E. Genome-wide profiling of diel and circadian gene expression in the malaria vectorAnopheles gambiae, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 32 | Article

[59] Sattelle, D. B.; Yamamoto, D. Molecular Targets of Pyrethroid Insecticides, Advances in Insect Physiology Volume 20, Elsevier, 1988, pp. 147-213 | Article

[60] Sawadogo, S. P.; Diabaté, A.; Toé, H. K.; Sanon, A.; Lefevre, T.; Baldet, T.; Gilles, J.; Simard, F.; Gibson, G.; Sinkins, S.; Dabiré, R. K. Effects of Age and Size on <I>Anopheles gambiae</I> s.s. Male Mosquito Mating Success, Journal of Medical Entomology, Volume 50 (2013) no. 2, pp. 285-293 | Article

[61] Scott, T. W.; Takken, W. Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission, Trends in Parasitology, Volume 28 (2012) no. 3, pp. 114-121 | Article

[62] Sherrard-Smith, E.; Griffin, J. T.; Winskill, P.; Corbel, V.; Pennetier, C.; Djénontin, A.; Moore, S.; Richardson, J. H.; Müller, P.; Edi, C.; Protopopoff, N.; Oxborough, R.; Agossa, F.; N’Guessan, R.; Rowland, M.; Churcher, T. S. Systematic review of indoor residual spray efficacy and effectiveness against Plasmodium falciparum in Africa, Nature Communications, Volume 9 (2018) no. 1 | Article

[63] Skovmand, O.; Bonnet, J.; Pigeon, O.; Corbel, V. Median knock-down time as a new method for evaluating insecticide-treated textiles for mosquito control, Malaria Journal, Volume 7 (2008) no. 1, p. 114 | Article

[64] Therneau, T., Available from: https://CRAN.R-project.org/package=coxme, 2018

[65] Toé, K. H.; Jones, C. M.; N’Fale, S.; Ismail, H. M.; Dabiré, R. K.; Ranson, H. Increased Pyrethroid Resistance in Malaria Vectors and Decreased Bed Net Effectiveness, Burkina Faso, Emerging Infectious Diseases, Volume 20 (2014) no. 10 | Article

[66] Toe, K. H.; Müller, P.; Badolo, A.; Traore, A.; Sagnon, N.; Dabiré, R. K.; Ranson, H. Do bednets including piperonyl butoxide offer additional protection against populations of Anopheles gambiae s.l . that are highly resistant to pyrethroids? An experimental hut evaluation in Burkina Fasov, Medical and Veterinary Entomology, Volume 32 (2018) no. 4, pp. 407-416 | Article

[67] Vantaux, A.; Yao, F.; Hien, D. F.; Guissou, E.; Yameogo, B. K.; Gouagna, L.-C.; Fontenille, D.; Renaud, F.; Simard, F.; Constantini, C.; Thomas, F.; Mouline, K.; Roche, B.; Cohuet, A.; Dabiré, K. R.; Lefèvre, T. Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum, bioRxiv, Volume 207183 (2018) | Article

[68] Vézilier, J.; Nicot, A.; Gandon, S.; Rivero, A. Insecticide resistance and malaria transmission: infection rate and oocyst burden in Culex pipiens mosquitoes infected with Plasmodium relictum, Malaria Journal, Volume 9 (2010) no. 1, p. 379 | Article

[69] Walker, E. D.; Edman, J. D. The Influence of Host Defensive Behavior on Mosquito (Diptera: Culicidae) Biting Persistence1, Journal of Medical Entomology, Volume 22 (1985) no. 4, pp. 370-372 | Article

[70] Wouters, W.; van den Bercken, J. Action of pyrethroids, General Pharmacology: The Vascular System, Volume 9 (1978) no. 6, pp. 387-398 | Article

[71] Zwiebel, L.; Takken, W. Olfactory regulation of mosquito–host interactions, Insect Biochemistry and Molecular Biology, Volume 34 (2004) no. 7, pp. 645-652 | Article

Cited by Sources: