Volume 90, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Flight behavior of insecticide-resistant and susceptible malaria mosquitoes approaching deltamethrin-treated nets was examined using a wind tunnel. Behavior was linked to resulting health status (dead or alive) using comparisons between outcomes from free-flight assays and standard World Health Organization (WHO) bioassays. There was no difference in response time, latency time to reach the net, or spatial distribution in the wind tunnel between treatments. Unaffected resistant mosquitoes spent less time close to (< 30 cm) treated nets. Nettings that caused high knockdown or mortality in standard WHO assays evoked significantly less mortality in the wind tunnel; there was no excitorepellent effect in mosquitoes making contact with the nettings in free flight. This study shows a new approach to understanding mosquito behavior near insecticidal nets. The methodology links free-flight behavior to mosquito health status on exposure to nets. The results suggest that behavioral assays can provide important insights for evaluation of insecticidal effects on disease vectors.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Steketee RW, Campbell CC, , 2010. Impact of national malaria control scale-up programmes in Africa: magnitude and attribution of effects. Malar J 9: 299.[Crossref] [Google Scholar]
  2. Lim SS, Fullman N, Stokes A, Ravishankar N, Masiye F, Murray CJL, Gakidou E, , 2011. Net benefits: a multicountry analysis of observational data examining associations between insecticide-treated mosquito nets and health outcomes. PLoS Med 8: e1001091.[Crossref] [Google Scholar]
  3. Lengeler C, , 2004. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev 2: CD000363. [Google Scholar]
  4. Lengeler C, , 2004. Insecticide-treated nets for malaria control: real gains. Bull World Health Organ 82: 84. [Google Scholar]
  5. Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Vulule JM, Hawley WA, , 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. II. Study design and methods. Am J Trop Med Hyg 68: 1015. [Google Scholar]
  6. Binka FN, Kubale A, Adjuik M, Williams LA, Lengeler C, Maude GH, Armah GE, Kajihara B, Adiamah JH, Smith PG, , 1996. Impact of permethrin impregnated bednets on child mortality in Kassena-Nankana district, Ghana: a randomized controlled trial. Trop Med Int Health 1: 147154.[Crossref] [Google Scholar]
  7. Kongmee M, Boonyuan W, Achee NL, Prabaripai A, Lerdthusnee K, Chareonviriyaphap T, , 2012. Irritant and repellent responses of Anopheles harrisoni and Anopheles minimus upon exposure to bifenthrin or deltamethrin using an excito-repellency system and a live host. J Am Mosq Control Assoc 28: 2029.[Crossref] [Google Scholar]
  8. Singh K, Rahman SJ, Joshi GC, , 1989. Village scale trial of deltamethrin against mosquitoes. J Commun Dis 21: 339353. [Google Scholar]
  9. Diabate A, Baldet T, Chandre F, Akoobeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM, , 2002. The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae s.l. in Burkina Faso. Am J Trop Med Hyg 67: 617622. [Google Scholar]
  10. Curtis CF, , 1991. Control of Disease Vectors in the Community. London, UK: Wolfe Publishing Ltd., 233. [Google Scholar]
  11. Mosha FW, Lyimo IN, Oxborough RM, Matowo J, Malima R, Feston E, Mndeme R, Tenu F, Kulkarni M, Maxwell CA, Magesa SM, Rowland MW, , 2008. Comparative efficacies of permethrin-, deltamethrin- and alpha-cypermethrin-treated nets, against Anopheles arabiensis and Culex quinquefasciatus in northern Tanzania. Ann Trop Med Parasitol 102: 367376.[Crossref] [Google Scholar]
  12. Darriet F, Robert V, Tho Vien N, Carnevale P, , 1984. Evaluation of the Efficacy of Permethrin-Impregnated Intact and Perforated Mosquito Nets against Vectors of Malaria. WHO Bulletin WHO/VBC 84. Geneva: World Health Organization. [Google Scholar]
  13. Lindsay SW, Adiamah JH, Miller JE, Armstrong JR, , 1991. Pyrethroid-treated bednet effects on mosquitoes of the Anopheles gambiae complex in The Gambia. Med Vet Entomol 5: 477483.[Crossref] [Google Scholar]
  14. Koudou BG, Koffi AA, Malone D, Hemingway J, , 2011. Efficacy of PermaNet® 2.0 and PermaNet® 3.0 against insecticide-resistant Anopheles gambiae in experimental huts in Côte d'Ivoire. Malar J 10: 172.[Crossref] [Google Scholar]
  15. Miller JE, Lindsay SW, Armstrong JR, , 1991. Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in The Gambia. Med Vet Entomol 5: 465476.[Crossref] [Google Scholar]
  16. Mathenge EM, Gimnig JE, Kolczak M, Ombok M, Irungu LW, Hawley WA, , 2001. Effect of permethrin-impregnated nets on exiting behavior, blood feeding success, and time of feeding of malaria mosquitoes (Diptera: Culicidae) in western Kenya. J Med Entomol 38: 531536.[Crossref] [Google Scholar]
  17. Killeen GF, Smith TA, , 2007. Exploring the contributions of bed nets, cattle, insecticides, and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 101: 867880.[Crossref] [Google Scholar]
  18. Cooperband MF, Allan SA, , 2009. Effects of different pyrethroids on landing behavior of female Aedes aegypti, Anopheles quadrimaculatus, and Culex quinquefasciatus mosquitoes (Diptera: Culicidae). J Med Entomol 46: 292306.[Crossref] [Google Scholar]
  19. Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, Chareonviriphap T, , 2000. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol 25: 4861. [Google Scholar]
  20. Achee NL, Sardelis MR, Dusfour I, Chauhan KR, Grieco JP, , 2009. Characterization of spatial repellent, contact irritant, and toxicant chemical actions of standard vector control compounds. J Am Mosq Control Assoc 25: 156167.[Crossref] [Google Scholar]
  21. White GB, Debboun MF, Strickman D, , 2006. Terminology of insect repellents. , eds. Insect Repellents: Principles, Methods and Uses. Boca Raton, FL: CRC Press, 3146.[Crossref] [Google Scholar]
  22. Itoh T, Shinjo G, Kurihara T, , 1986. Studies on wide mesh netting impregnated with insecticides against Culex mosquitos. J Am Mosq Control Assoc 2: 503506. [Google Scholar]
  23. Bogh C, Pedersen EM, Mukoko DA, Ouma JH, , 1998. Permethrin-impregnated bednet effects on resting and feeding behaviour of lymphatic filariasis vector mosquitoes in Kenya. Med Vet Entomol 12: 5259.[Crossref] [Google Scholar]
  24. Grieco JP, Achee NL, Andre RG, Roberts DR, , 2000. A comparison study of house entering and exiting behavior of Anopheles vestitipennis (Diptera: Culicidae) using experimental huts sprayed with DDT or Deltamethrin in the Southern District of Toledo, Belize, C. A. J Vector Ecol 25: 6273. [Google Scholar]
  25. Okumu FO, Moore J, Mbeyela E, Sherlock M, Sangusangu R, Ligamba G, Russell T, Moore SJ, , 2012. A modified experimental hut design for studying responses of disease-transmitting mosquitoes to indoor interventions: the Ifakara experimental huts. PLoS ONE 7: e30967.[Crossref] [Google Scholar]
  26. WHO, 2005. Guidelines for Laboratory and Field Testing of Long-Lasting Insecticidal Mosquito Nets. Geneva: World Health Organization, 18. [Google Scholar]
  27. Mboera LEG, Takken W, , 1999. Odour-mediated host preference of Culex quinquefasciatus in Tanzania. Entomol Exp Appl 92: 8388.[Crossref] [Google Scholar]
  28. Smallegange RC, Knols BGJ, Takken W, , 2010. Effectiveness of synthetic versus natural human volatiles as attractants for Anopheles gambiae (Diptera: Culicidae) sensu stricto. J Med Entomol 47: 338344. [Google Scholar]
  29. Spitzen JS, Smallegange CR, Takken W, , 2008. Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae s.s. in an olfactometer. Physiol Entomol 33: 116122.[Crossref] [Google Scholar]
  30. WHO, 2006. Guidelines for Testing Mosquito Adulticides for Indoor Residual Spraying and Treatment of Mosquito Nets. Geneva: World Health Organization, 70. [Google Scholar]
  31. Carnevale P, Bitsindou P, Diomande L, Robert V, , 1992. Insecticide impregnation can restore the efficiency of torn bed nets and reduce man-vector contact in malaria endemic areas. Trans R Soc Trop Med Hyg 86: 362364.[Crossref] [Google Scholar]
  32. Darriet F, Chandre F, , 2011. Combining piperonyl butoxide and dinotefuran restores the efficacy of deltamethrin mosquito nets against resistant Anopheles gambiae (Diptera: Culicidae). J Med Entomol 48: 952955.[Crossref] [Google Scholar]
  33. N'Guessan R, Asidi A, Boko P, Odjo A, Akogbeto M, Pigeon O, Rowland M, , 2010. 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. Trans R Soc Trop Med Hyg 104: 758765.[Crossref] [Google Scholar]
  34. Hougard JM, Corbel V, N'Guessan R, Darriet F, Chandre F, Akogbeto M, Baldet T, Guillet P, Carnevale P, Traore-Lamizana M, , 2003. Efficacy of mosquito nets treated with insecticide mixtures or mosaics against insecticide resistant Anopheles gambiae and Culex quinquefasciatus (Diptera: Culicidae) in Cote d'Ivoire. Bull Entomol Res 93: 491498.[Crossref] [Google Scholar]
  35. Lines JD, Myamba J, Curtis CF, , 1987. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol 1: 3751.[Crossref] [Google Scholar]
  36. Malima RC, Oxborough RM, Tungu PK, Maxwell C, Lyimo I, Mwingira V, Mosha FW, Matowo J, Magesa SM, Rowland MW, , 2009. Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Med Vet Entomol 23: 317325.[Crossref] [Google Scholar]
  37. Takken W, Knols BGJ, , 1999. Odor-mediated behavior of afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131157.[Crossref] [Google Scholar]
  38. Corbel V, Chabi J, Dabire RK, Etang J, Nwane P, Pigeon O, Akogbeto M, Hougard JM, , 2010. Field efficacy of a new mosaic long-lasting mosquito net (PermaNet (R) 3.0) against pyrethroid-resistant malaria vectors: a multi centre study in Western and Central Africa. Malar J 9: 113.[Crossref] [Google Scholar]
  39. Fane M, Cisse O, Traore CSF, Sabatier P, , 2012. Anopheles gambiae resistance to pyrethroid-treated nets in cotton versus rice areas in Mali. Acta Trop 122: 16.[Crossref] [Google Scholar]
  40. Magesa SM, Wilkes TJ, Mnzava AE, Njunwa KJ, Myamba J, Kivuyo MD, Hill N, Lines JD, Curtis CF, , 1991. Trial of pyrethroid impregnated bednets in an area of Tanzania holoendemic for malaria. Part 2. Effects on the malaria vector population. Acta Trop 49: 97108.[Crossref] [Google Scholar]
  41. Schreck CE, Kline DL, , 1983. Area protection by use of repellent-treated netting against culicoides biting midges. Mosq News 43: 338342. [Google Scholar]
  42. Ruigt GSF, Kerkut GA, Gilbert LI, , 1985. Pyrethroids. , eds. Comprehensive Insect Physiology Biochemistry and Pharmacology, Vol 12. Oxford, UK: Pergamon, 183262. [Google Scholar]
  43. Sawicki R, , 1962. Insecticidal activity of pyrethrum extract and its four insecticidal constituents against house flies. III. Knock-down and recovery of flies treated with pyrethrum extract with and without piperonyl butoxide. J Sci Food Agric 13: 283292.[Crossref] [Google Scholar]
  44. Alzogaray RA, Zerba EN, , 1997. Incoordination, paralysis and recovery after pyrethroid treatment on nymphs III of Triatoma infestans (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz 92: 431435.[Crossref] [Google Scholar]
  45. Bernard CB, Philogene BJR, , 1993. Insecticide synergists: role, importance, and perspectives. J Toxicol Environ Health 38: 199223.[Crossref] [Google Scholar]
  46. Moores G, Bingham G, Gunning R, , 2005. Use of 'temporal synergism' to overcome insecticide resistance. Outlook Pest Manag 16: 79.[Crossref] [Google Scholar]
  47. Ahmad M, Denholm I, Bromilow RH, , 2006. Delayed cuticular penetration and enhanced metabolism of deltamethrin in pyrethroid-resistant strains of Helicoverpa armigera from China and Pakistan. Pest Manag Sci 62: 805810.[Crossref] [Google Scholar]
  48. Young SJ, Gunning RV, Moores GD, , 2006. Effect of pretreatment with piperonyl butoxide on pyrethroid efficacy against insecticide-resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and Bemisia tabaci (Sternorrhyncha: Aleyrodidae). Pest Manag Sci 62: 114119.[Crossref] [Google Scholar]
  49. Bingham G, Strode C, Tran L, Khoa PT, Jamet HP, , 2011. Can piperonyl butoxide enhance the efficacy of pyrethroids against pyrethroid-resistant Aedes aegypti? Trop Med Int Health 16: 492500.[Crossref] [Google Scholar]
  50. Spitzen J, Spoor CW, Grieco F, ter Braak C, Beeuwkes J, van Brugge SP, Kranenbarg S, Noldus LP, van Leeuwen JL, Takken W, , 2013. A 3D analysis of flight behavior of Anopheles gambiae sensu stricto malaria mosquitoes in response to human odor and heat. PLoS ONE 8: e62995.[Crossref] [Google Scholar]
  51. Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, Moore SJ, Rowland M, Sweeney K, Torr SJ, Zwiebel L, Grieco JP, , 2012. Spatial repellents: from discovery and development to evidence-based validation. Malar J 11: 164.[Crossref] [Google Scholar]

Data & Media loading...

Supplementary PDF

Supplementary AVI

Supplementary AVI

Supplementary AVI

  • Received : 19 Dec 2013
  • Accepted : 07 Mar 2014
  • Published online : 04 Jun 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error