Enhancing Attraction of African Malaria Vectors to a Synthetic Odor Blend

Journal of Chemical Ecology

Volumn 42, Issue 6, 2016, Pages 508-516

  Mweresa, Collins K ^a   Mukabana, Wolfgang R ^a,b   Omusula, Philemon ^a,c   Otieno, Bruno ^a   Van Loon, Joop J A ^d   Takken, Willem ^d  

^a INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^b UNIVERSITY OF NAIROBI   (Kenya)

^c MINISTRY OF HEALTH   (Kenya)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Anopheles funestus; Anopheles gambiae; Attractant; Host seeking behavior; Mosquito; Olfaction; Synthetic odor

Indexed keywords

AMMONIA; BAIT; BEHAVIORAL RESPONSE; DISEASE CONTROL; DISEASE VECTOR; MALARIA; MOSQUITO; ODOR; OLFACTION; OPTIMIZATION; ORGANIC ACID; TRAPPING;

KENYA;

ANOPHELES FUNESTUS; ANOPHELES GAMBIAE;

FRAGRANCE;

ANIMAL; ANOPHELES; BIOASSAY; DOSE RESPONSE; DRUG EFFECTS; FEMALE; HOST-SEEKING BEHAVIOR; HUMAN; INSECT VECTOR; MALARIA; PHYSIOLOGY; TRANSMISSION;

ANIMALS; ANOPHELES; BIOLOGICAL ASSAY; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HOST-SEEKING BEHAVIOR; HUMANS; INSECT VECTORS; MALARIA; ODORANTS;

EID: 84976295500     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-016-0711-1     Document Type: Article

References (52)

1. Bayoh MN, Mathias D, Odiere M, Mutuku F, Kamau L, Gimnig J, Vulule J, Hawley W, Hamel M, Walker E (2010) Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9:62
2. Bukhari T, Takken W, Andrew KG, Koenraadt JMC (2011) Efficacy of aquatain, a monomolecular film for the control of malaria vectors in rice paddies. PLoS One 6:e21713
3. Charlwood JD, Tomás EV, Egyir-Yawson A, Kampango AA, Pitts RJ (2012) Feeding frequency and survival of Anopheles gambiae in a rice-growing area in Ghana. Med Vet Entomol 26:263–270
4. Costantini C, Gibson G, Sagnon N, Della Torre A, Brady J, Coluzzi M (1996) Mosquito responses to carbon dioxide in a west African Sudan savanna village. Med Vet Entomol 10:220–227
5. Dekker T, Steib B, Cardé RT, Geier M (2002) L-lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae. Med Vet Entomol 16:91–98
6. Dia I, Diallo D, Duchemin J, Konate YB, Costantini C, Diallo M (2005) Comparisons of human-landing catches and odor-baited entry traps for sampling malaria vectors in Senegal. J Med Entomol 42:104–109
7. Durnez L, Coosemans M (2013) Residual transmission of malaria: An old issue for new approaches, pp. 671–704, Anopheles mosquitoes-New insights into malaria vectors. Intech
8. Gillies MT, Coetzee M (1987) A supplement to the anophelinae of Africa south of the Sahara (Afrotropical region), Johannesburg. S Afr Inst Med Res 55:1–143
9. Hiscox A, Maire N, Kiche I, Silkey M, Homan T, Oria P, Mweresa CK, Otieno B, Ayugi M, Bousema T, Sawa P, Alaii J, Smith T, Leeuwis C, Mukabana WR, Takken W (2012) The SolarMal project: innovative mosquito trapping technology for malaria control. Malar J 11:45
10. Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, Knols BGJ, Takken W, Conway DJ (2009) Optimizing odor-baited trap methods for collecting mosquitoes during the malaria season in the Gambia. PLoS One 4:e8167
11. Kline DL (2006) Traps and trapping techniques for adult mosquito control. Am Mosq Control Assoc 22:490–496
12. Kline D (2007) Semiochemicals, traps/targets and mass trapping technology for mosquito management. Am Mosq Control Assoc 23:241–251
13. Kweka JE, Mahande AN (2009) Comparative evaluation of four mosquitoes sampling methods in rice irrigation schemes of lower Moshi, northern Tanzania. Malar J 8:149
14. Kweka EJ, Eunice AO, Beda JM, Aneth MM, Mramba N, Franklin M (2011) The role of cow urine in the oviposition site preference of culicine and Anopheles mosquitoes. Parasit Vectors 4:184
15. Lindh MJ, Okal MN, Herrera-Varela M, Borg-Karlson A, Torto B, Lindsay SW, Fillinger U (2015) Discovery of an oviposition attractant for gravid malaria vectors of the Anopheles gambiae species complex. Malar J 14:119
16. Logan JG (2008) Why do mosquitoes “choose” to bite some people more than others. outlooks on pest man 14:280–283
17. Logan JG, Birkett MA, Clark SJ, Powers S, Seal NJ, Wadhams LJ, Mordue AJ, Pickett JA (2008) Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes. J Chem Ecol 34:308–322
18. Mathenge EM, Misiani GO, Irungu LW, Ndegwa PN, Smith LW, Killeen GF, Knols BGJ (2005) Comparative performance of the Mbita trap, CDC light trap and the human landing catch in the sampling of Anopheles arabiensis, An. funestus and culicine species in a rice irrigation in western Kenya. Malar J 4:7
19. Mboera LEG (2005) Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan Health Res Bull 7:117–124
20. Mendis K, Rietvelda A, Warsame M, Bosman A, Greenwood B, Wernsdorfer WH (2009) From malaria control to eradication: the WHO perspective. Trop Med & Internl Hlth 14:802–809
21. Menger DJ, Otieno B, de Rijk M, Mukabana WR, van Loon JJ, Takken W (2014) A push-pull system to reduce house entry of malaria mosquitoes. Malar J 13:119
22. Menger D, Omusula P, Holdinga M, Homan T, Carreira A, Vandendaele P, Derycke J, Mweresa CK, Mukabana WR, Van Loon JJA, Takken W (2015) Field evaluation of a push-pull system to reduce malaria transmission. PLoS One 10:e0123415
23. Menger DJ, Omusula P, Wouters K, Oketch C, Carreira AS, Durka M, Derycke JL, Loy DE, Hahn BH, Mukabana WR, Mweresa CK, van Loon JJ, Takken W, Hiscox A (2016) Eave screening and push-pull tactics to reduce house entry by vectors of malaria. AmJTrop Med Hyg 94:868–878
24. Mukabana WR, Mweresa CK, Otieno B, Omusula P, Smallegange RC, Van Loon JJA, Takken W (2012a) A novel synthetic odorant blend for trapping of malaria and other African mosquito species. J Chem Ecol 38:235–244
25. Mukabana WR, Mweresa CK, Otieno B, Omusula P, Orindi B, Smallegange RC, Van Loon JJA, Takken W (2012b) Evaluation of low density polyethylene and nylon for delivery of synthetic mosquito attractants. Parasit Vectors 50:123–133
26. Mwangangi JM, Muturi EJ, Muriu SM, Nzovu J, Midega JT, Mbogo C (2013) The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya Parasit Vectors 6
27. Mweresa CK, Omusula P, Otieno B, Weldegergis BT, Verhulst NO, Dicke M, Van Loon JJA, Takken W, Mukabana RW (2015) Understanding the long-lasting attraction of malaria mosquitoes to odor baits. PLoS One 10:e0121533
28. Ndiath M, Mazenot C, Gaye A, Konate L, Bouganali C, Faye O, Sokhna C, Trape JF (2011) Methods to collect Anopheles mosquitoes and evaluate malaria transmission: a comparative study in two villages in Senegal. Malar J 10:270
29. Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W, Mshinda H, Mukabana WR, Moore SJ (2010a) Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS One 5:e8951
30. Okumu FO, Biswaro L, Mbeleyela E, Killeen GF, Mukabana RW, Moore SJ (2010b) Using nylon strips to dispense mosquito attractants for sampling the malaria vector Anopheles gambiae s.s. J Med Entomol 47:274–282
31. Okumu FO, Madumla E, John A, Lwetoijera D, Sumaye R (2010c) Attracting, trapping and killing disease-transmitting mosquitoes using odor-baited stations - the Ifakara odor-baited stations. Parasit Vectors 3:12
32. Pickett JA, Birkett MA, Dewhirst SY, Logan JG, Omolo MO, Torto B, Pelletier J, Syed Z, Leal WS (2010) Chemical ecology of animal and human pathogen vectors in a changing global climate. J Chem Ecol 36:113–121
33. Qiu YT, Van Loon JJA (2010) Olfactory physiology of blood-feeding vector mosquitoes. Ecol Control Vector-borne Dis 2:39–61
34. Qiu YT, Smallegange RC, Braak CJF, Spitzen J, Van Loon JJA, Jawara M, Milligan P, Galimard AM, Van Beek TA, Knols BGJ, Takken W (2007) Attractiveness of MM-X traps baited with human or synthetic odor to mosquitoes (Diptera: Culicidae) in the Gambia. J Med Entomol 44:970–983
35. Qiu YT, Smallegange RC, Van Loon JJA, Takken W (2011) Behavioural responses of Anopheles gambiae sensu stricto to components of human breath, sweat and urine depend on mixture composition and concentration. Med Vet Entomol 25:247–255
36. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SF, Killeen GF (2011) Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10:80
37. Schmied W, Takken W, Killeen GF, Knols BGJ, Smallegange RC (2008) Evaluation of two counterflow traps for testing behaviour-mediating compounds for the malaria vector Anopheles gambiae s.s. under semi-field conditions in Tanzania. Malar J 7:230
38. Scott TW, Takken W (2012) Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission. Trends Parasitol 28:114–121
39. Smallegange RC, Takken W (2010) Host-seeking behaviour of mosquitoes: responses to olfactory stimuli in the laboratory. Ecol Contl Vector-borne Dis 2:143–180
40. Smallegange RC, Qiu YT, Van Loon JJA, Takken W (2005) Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chem Senses 30:145–152
41. Smallegange RC, Qiu YT, Bukovinszkiné-Kiss G, Van Loon JJA, Takken W (2009) The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol 34:933–943
42. Smallegange RC, Schmied WH, van Roey VNO, Spitzen J, Mukabana WR, Takken W (2010) Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae. Malar J 9:292
43. Smallegange RC, Bukovinszkiné-Kiss G, Otieno B, Mbadi PA, Takken W, Mukabana RW, Van Loon JJA (2012) Identification of candidate volatiles that affect the behavioural response of the malaria mosquito Anopheles gambiae sensu stricto to an active kairomone blend: laboratory and semi-field assays. Physiol Entomol 37:60–71
44. Takken W (2010) Push-pull strategies for vector control. Malar J 9:116
45. Takken W, Knols BGJ (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44:131–157
46. Vale GA, Torr, S.J. (2004) Development of bait technology to control tsetse. The Trypanosomiases, pp 509–523
47. Van Loon JJA, Smallegange RC, Bukovinszkiné-Kiss G, Jacobs F, De Rijk M, Mukabana RW, Verhulst NO, Menger DJ, Takken W (2015) Mosquito attraction: crucial role of carbon dioxide in formulation of a five-component blend of human-derived volatiles. J Chem Ecol 41:567–573
48. Verhulst NO, Andriessen R, Groenhagen U, Bukovinszkiné-Kiss G, Schulz S, Takken W, Van Loon JJA, Schraa G, Smallegange RC (2010) Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLoS One 5:e15829
49. Verhulst NO, Mukabana WR, Takken W, Smallegange RC (2011a) Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae s.s. Entomol Exp Appl 139:170–179
50. Verhulst NO, Mbadi P, Bukovinszkiné-Kiss G, Mukabana RW, Van Loon JJA, Takken W, Smallegange RC (2011b) Improvement of a synthetic lure for Anopheles gambiae using compounds produced by human skin microbiota. Malar J 10:28
51. Wanji S, Theodore T, Sali NA, Caroline A, Tendongfor N, Didier F (2003) Anopheles species of the Mount Cameroon region: biting habits, feeding behaviour and entomological inoculation rates. Trop Med Intl Hlth 8:643–649
52. WHO (1975) Manual on practical entomology in malaria: part II, methods and techniques, WHO division of malaria and other parasitic diseases. Switzerland, Geneva