Taxis assays measure directional movement of mosquitoes to olfactory cues

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Lorenz, Lena M ^a   Keane, Aidan ^b   Moore, Jason D ^a,c   Munk, Cristina J ^c   Seeholzer, Laura ^c   Mseka, Antony ^c   Simfukwe, Emmanuel ^c   Ligamba, Joseph ^c   Turner, Elizabeth L ^d   Biswaro, Lubandwa R ^c   Okumu, Fredros O ^c   Killeen, Gerry F ^c,e   Mukabana, Wolfgang R ^f   Moore, Sarah J ^a,c  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c IFAKARA HEALTH INSTITUTE   (Tanzania)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^f UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

Anopheles; Arthropods; Directional movement; Disease control; Field assay; Malaria; Odour; Olfaction; Taxis box

Indexed keywords

CARBON DIOXIDE; CARBOXYLIC ACID;

ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ARTICLE; ASSAY; CONTROLLED STUDY; HIGH THROUGHPUT SCREENING; MALARIA CONTROL; NONHUMAN; ODOR; TAXIS BOX ASSAY;

ANIMALS; ANOPHELES; BEHAVIOR, ANIMAL; DRUG EVALUATION, PRECLINICAL; ENTOMOLOGY; FEMALE; LOCOMOTION; PHEROMONES; SMELL;

ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ARTHROPODA;

EID: 84877006467     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-131     Document Type: Article

References (59)

1. World Health Organization, Handbook for integrated vector management Geneva, Switzerland: World Health Organization 2012
2. Visual and olfactory responses of haematophagous Diptera to host stimuli. Gibson G, Torr SJ, Med Vet Entomol 1999 13 2 23 10.1046/j.1365-2915.1999.00163. x 10194745
3. Insects as chemosensors of humans and crops. van Naters WV, Carlson JR, Nature 2006 444 302 307 10.1038/nature05403 17108954
4. General principles of attraction and competitive attraction as revealed by large-cage studies of moths responding to sex pheromone. Miller JR, McGhee PS, Siegert PY, Adams CG, Huang J, Grieshop MJ, Gut LJ, P Natl Acad Sci USA 2010 107 22 27 10.1073/pnas.0908453107
5. Revisiting the basic reproductive number for malaria and its implications for malaria control. Smith DL, McKenzie FE, Snow RW, Hay SI, PLoS Biol 2007 5 42 10.1371/journal.pbio.0050042 17311470
6. Odorant reception in the malaria mosquito Anopheles gambiae. Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR, Nature 2010 464 66 71 10.1038/nature08834 20130575
7. Malaria vector control: current and future strategies. Takken W, Knols BGJ, Trends Parasitol 2009 25 101 104 10.1016/j.pt.2008.12.002 19168392
8. The European struggle to control Ips typographus-Past, present and future. Vite JP, Holarctic Ecol 1989 12 520 525
9. Potential of mass trapping for long-term pest management and eradication of invasive species. El-Sayed AM, Suckling DM, Wearing CH, Byers JA, J Econ Entomol 2006 99 1550 1564 10.1603/0022-0493-99.5.1550 17066782
10. Potential of «lure and kill» in long-term pest management and eradication of invasive species. El-Sayed AM, Suckling DM, Byers JA, Jang EB, Wearing CH, J Econ Entomol 2009 102 815 835 10.1603/029.102.0301 19610395
11. Potential benefits, limitations and target product-profiles of odor-baited mosquito traps for malaria control in Africa. Okumu FO, Govella NJ, Moore SJ, Chitnis N, Killeen GF, PLoS One 2010 5 11573 10.1371/journal.pone. 0011573 20644731
12. A new odour-baited trap to collect host-seeking mosquitoes. Costantini C, Gibson G, Brady J, Merzagora L, Coluzzi M, Parassitologia 1993 35 5 9 7915027
13. Field testing of different chemical combinations as odour baits for trapping wild mosquitoes in The Gambia. Jawara M, Awolola TS, Pinder M, Jeffries D, Smallegange RC, Takken W, Conway DJ, PLoS One 2011 6 19676 10.1371/journal.pone.0019676 21637337
14. Attracting, trapping and killing disease-transmitting mosquitoes using odor-baited stations-The Ifakara Odor-Baited Stations. Okumu FO, Madumla EP, John AN, Lwetoijera DW, Sumaye RD, Parasit Vectors 2010 3 12 10.1186/1756-3305-3-12 20193085
15. Olfaction-Mosquito receptor for human-sweat odorant. Hallem EA, Fox AN, Zwiebel LJ, Carlson JR, Nature 2004 427 212 213 10.1038/427212a 14724626
16. Female Anopheles gambiae antennae: increased transcript accumulation of the mosquito-specific odorant-binding-protein OBP2. Hoffman SA, Aravind L, Velmurugan S, Parasit Vectors 2012 5 27 10.1186/1756-3305-5-27 22309624
17. Odor discrimination using insect electroantennogram responses from an insect antennal array. Park KC, Ochieng SA, Zhu JW, Baker TC, Chem Senses 2002 27 343 352 10.1093/chemse/27.4.343 12006374
18. Use of olfactometers for determining attractants and repellents. Butler JF, Insect repellents: Principles, Methods and Uses Boca Raton, Florida, USA: CRC Press, Tayler & Francis Group, Debboun M, Frances SP, Strickman D, Boca Raton FL, 2007
19. Behavioural response of the malaria vector Anopheles gambiae to host plant volatiles and synthetic blends. Nyasembe VO, Teal PEA, Mukabana WR, Tumlinson JH, Torto B, Parasit Vectors 2012 5 234 10.1186/1756-3305-5-234 23069316
20. Sustained-flight tunnel for measuring insect responses to wind-borne sex-pheromones. Miller JR, Roelofs WL, J Chem Ecol 1978 4 187 198 10.1007/BF00988054
21. Odor-mediated flight behavior of Anopheles gambiae Giles Sensu Stricto and A. stephensi Liston in response to CO2, acetone, and 1-octen-3-ol (Diptera: Culicidae). Takken W, Dekker T, Wijnholds YG, J Insect Behav 1997 10 395 407 10.1007/BF02765606
22. Using nylon strips to dispense mosquito attractants for sampling the malaria vector Anopheles gambiae s.s. Okumu F, Biswaro L, Mbeleyela E, Killeen GF, Mukabana R, Moore SJ, J Med Ento 2010 47 274 282 10.1603/ME09114
23. The range of attraction of animal baits and carbon dioxide for mosquitoes. Studies in a freshwater area of West Africa. Gillies MT, Wilkes TJ, B Entomol Res 1972 61 389 404 10.1017/S0007485300047295
24. A comparison of the range of attraction of animal baits and of carbon dioxide for some West African mosquitoes. Gillies MT, Wilkes TJ, B Entomol Res 1969 59 441 456 10.1017/S0007485300003412
25. The range of attraction of single baits for some West African mosquitoes. Gillies MT, Wilkes TJ, B Entomol Res 1970 60 225 235 10.1017/S000748530004075X
26. Target product profiles for protecting against outdoor malaria transmission. Killeen GF, Moore SJ, Malaria J 2012 11 17 10.1186/1475-2875-11-17
27. Terminology of insect repellents. White GB, Insect Repellents: Principles, Methods and Uses Boca Raton, Florida, USA: CRC Press, Taylor & Francis Group, Debboun M, Frances SP, Strickman D, Boca Raton FL, 2007 31 46
28. Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W, PLoS One 2010 5 8951 10.1371/journal.pone.0008951 20126628
29. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF, Malaria J 2011 10 80 10.1186/1475-2875-10-80
30. Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AV, Atieli FK, Ondijo SO, Genga IO, Exp Parasitol 1996 82 306 315 10.1006/expr.1996.0038 8631382
31. Analysis of Anopheles arabiensis blood feeding behavior in Southern Zambia during the two years after introduction of insecticide-treated bed nets. Fornadel CM, Norris LC, Glass GE, Norris DE, Am J Trop Med Hyg 2010 83 848 853 10.4269/ajtmh.2010.10-0242 20889878
32. Establishment of a large semi-field system for experimental study of African malaria vector ecology and control in Tanzania. Ferguson HM, Ng'habi KR, Walder T, Kadungula D, Moore SJ, Lyimo I, Russell TL, Urassa H, Mshinda H, Killeen GF, Knols BGJ, Malaria J 2008 7 158 10.1186/1475-2875-7-158
33. The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): A review. Gillies MT, B Entomol Res 1980 70 525 532 10.1017/S0007485300007811
34. Evaluation of low density polyethylene and nylon for delivery of synthetic mosquito attractants. Mukabana WR, Mweresa CK, Omusula P, Orindi BO, Smallegange RC, van Loon JJA, Takken W, Parasit Vectors 2012 5 202 10.1186/1756-3305-5-202 22992518
35. R: A language and environment for statistical computing http://www.R-project.org
36. lme4: Linear mixed-effects models using S4 classes http://CRAN.R-project. org/package=lme4
37. Information theory as an extension of the maximum likelihood principle. Akaike H, Second international symposium on information theory Budapest, Hungary: Akademiai Kiado, Petrov BN, Csaki F, 1973 267 281
38. Simultaneous inference in general parametric models. Hothorn T, Bretz F, Westfall P, Biometrical J 2008 50 346 363 10.1002/bimj.200810425
39. Responses of female Aedes aegypti (Diptera, Culicidae) to host odors and convection currents using an olfactometer bioassay. Eiras AE, Jepson PC, B Entomol Res 1994 84 207 211 10.1017/S0007485300039705
40. 'Infotaxis' as a strategy for searching without gradients. Vergassola M, Villermaux E, Shraiman BI, Nature 2007 445 406 409 10.1038/nature05464 17251974
41. Pheromone source location by flying moths-a supplementary non-anemotactic mechanism. Baker TC, Kuenen LPS, Science 1982 216 424 426 10.1126/science.216. 4544.424 17745868
42. Odour movement, wind direction, and the problem of host-finding by tsetse flies. Brady J, Gibson G, Packer MJ, Physiol Entomol 1989 14 369 380 10.1111/j.1365-3032.1989.tb01105.x
43. Anopheline mosquitoes: vector behaviour and bionomics. Gillies MT, Malaria-Principles and Practices of Malariology Edinburgh: Churchill Livingston, Wernsdorfer WH, McGregor I, 1988 453 485
44. Activation of Anopheles gambiae mosquitos by carbon dioxide and human breath. Healy TP, Copland MJW, Med Vet Entomol 1995 9 331 336 10.1111/j.1365-2915.1995.tb00143.x 7548953
45. Studies on the local distribution and on the methods of host location of some Rhodesian Tabanidae (Diptera). Phelps RJ, Vale GA, J Entomol Soc S Afr 1976 39 67 81
46. Flight of tsetse flies (Diptera: Glossinidae) to and from a stationary ox. Vale GA, B Entomol Res 1977 67 297 303 10.1017/S0007485300011111
47. Sampling range, attraction range, and effective attraction radius-Estimates of trap efficiency and communication distance in Coleopteran pheromone and host attractant systems. Schlyter F, J Appl Entomol 1992 114 439 454 10.1111/j.1439-0418.1992.tb01150.x
48. Effective attraction radius-a method for comparing species attractants and determining densities of flying insects. Byers JA, Anderbrant O, Lofqvist J, J Chem Ecol 1989 15 749 765 10.1007/BF01014716
49. Orientation of Culex mosquitoes to carbon dioxide-baited traps: flight manoeuvres and trapping efficiency. Cooperband MF, Carde RT, Med Vet Entomol 2006 20 11 26 10.1111/j.1365-2915.2006.00613.x 16608486
50. Roles and effects of environmental carbon dioxide in insect life. Guerenstein PG, Hildebrand JG, Annu Rev Entomol 2008 53 161 178 10.1146/annurev.ento.53.103106.093402 17803457
51. Differential responses of mosquito sibling species Anopheles arabiensis and An. quadriannulatus to carbon dioxide, a man or a calf. Dekker T, Takken W, Med Vet Entomol 1998 12 136 140 10.1046/j.1365-2915.1998.00073.x 9622366
52. Blood, sex, and the mosquito-The mechanisms that control mosquito blood-feeding behavior. Klowden MJ, Bioscience 1995 45 326 331 10.2307/1312493
53. Vector olfaction and behaviour. Klowden MJ, Zwiebel LJ, Biology of Disease Vectors Elsevier Academic Press, Marquardt WH, 2 2004 277 287
54. Host-seeking behavior and management of tsetse. Colvin J, Gibson G, Annu Rev Entomol 1992 37 21 40 10.1146/annurev.en.37.010192.000321 1539936
55. A trial to control the tsetse fly, Glossina morsitans centralis, with low densities of odor-baited targets in West Zambia. Knols BGJ, Willemse L, Flint S, Mate A, Med Vet Entomol 1993 7 161 169 10.1111/j.1365-2915.1993.tb00670.x 8481533
56. Semiochemicals, traps/targets and mass trapping technology for mosquito management. Kline DL, J Am Mosquito Contr 2007 23 241 251 10.2987/8756- 971X(2007)23[241:STAMTT]2.0.CO;2
57. Optimization of odour-baited resting boxes for sampling malaria vector, Anopheles arabiensis Patton, in arid and highland areas of Africa. Kweka EJ, Mwang'onde BJ, Mahande AM, Parasit Vectors 2010 3 75 10.1186/1756-3305-3-75 20723243
58. An encounter rate model of bark beetle populations searching at random for susceptible host trees. Byers JA, Ecol Model 1996 91 57 66 10.1016/0304-3800(95)00166-2
59. The use of confidence or fiducial limits illustrated in the case of the binomial. Clopper CJ, Pearson ES, Biometrika 1934 26 404 413 10.1093/biomet/26.4.404