Mosquito Attraction: Crucial Role of Carbon Dioxide in Formulation of a Five-Component Blend of Human-Derived Volatiles

Journal of Chemical Ecology

Volumn 41, Issue 6, 2015, Pages 567-573

  van Loon, Joop J A ^a   Smallegange, Renate C ^a   Bukovinszkiné Kiss, Gabriella ^a   Jacobs, Frans ^a   De Rijk, Marjolein ^a   Mukabana, Wolfgang R ^b,c   Verhulst, Niels O ^a   Menger, David J ^a   Takken, Willem ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

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

^c UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

3 methyl 1 butanol; Anopheles gambiae; Behavioral disruption; Butan 1 amine; Carbon dioxide; Kairomone; Olfaction; Trapping

Indexed keywords

ATTRACTANT; BEHAVIORAL RESPONSE; CARBON DIOXIDE; CHEMICAL ECOLOGY; CONCENTRATION (COMPOSITION); INHIBITION; KAIROMONE; MALARIA; MOSQUITO; OLFACTION; TRAPPING; VOLATILE SUBSTANCE;

ANOPHELES GAMBIAE; INSECTA;

CARBON DIOXIDE; INSECT ATTRACTANTS; ISOPENTYL ALCOHOL; PENTANOL; PHEROMONE; VOLATILE ORGANIC COMPOUND;

ANIMAL; ANOPHELES; CHEMISTRY; CHEMOTAXIS; DRUG EFFECTS; FEMALE; HUMAN; MOSQUITO CONTROL; PHYSIOLOGY;

ANIMALS; ANOPHELES; CARBON DIOXIDE; CHEMOTAXIS; FEMALE; HUMANS; MOSQUITO CONTROL; PENTANOLS; PHEROMONES; VOLATILE ORGANIC COMPOUNDS;

EID: 84930867003     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-015-0587-5     Document Type: Article

References (47)

1. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69:44–60
2. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM et al (2011) A research agenda to underpin malaria eradication. PLoS Med 8, e1000406
3. Anton S, Rospars JP (2004) Quantitative analysis of olfactory receptor neuron projections in the antennal lobe of the malaria mosquito, Anopheles gambiae. J Comp Neurol 475:315–326
4. Anton S, Van Loon JJA, Meijerink J, Smid HM, Takken W, Rospars JP (2003) Central projections of olfactory receptor neurons from single antennal and palpal sensilla in mosquitoes. Arthropod Struct Dev 32:319–327
5. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162
6. Bosch O, Geier M, Boeckh J (2000) Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses 25:323–330
7. Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464:66–71
8. Carlson JR, Carey AF (2011) Scent of a human: decoding how a mosquito sniffs out human targets could lead to better traps and repellents that cut malaria’s spread. Sci American 305:76–79
9. Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ (2013) Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619:246–274
10. 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
11. Ellin RI, Farrand RL, Oberst FW, Crouse CL, Billups NB, Koon WS, Musselman NP, Sidell FR (1974) An apparatus for the detection and quantitation of volatile human effluents. J Chromatogr A 100:137–152
12. Geier M, Boeckh J (1999) A new Y-tube olfactometer for mosquitoes to measure the attractiveness of host odours. Entomol Exp Appl 92:9–19
13. Gillies MT (1980) The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull Entomol Res 70:525–532
14. Guo M, Krieger J, Grosse-Wilde E, Missbach C, Zhang L, Breer H (2014) Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the Desert Locust (Schistocerca gregaria). Int J Biol Sci 10:1–14
15. James GA, Casey J, Hyliands D, Mycock G (2004) Fatty acid metabolism by cutaneous bacteria and its role in axillary malodour. World J Microbiol Biotech 20:787–793
16. Kwon HW, Lu T, Rutzler M, Zwiebel LJ (2006) Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 103:13526–13531
17. Liu C, Pitts RJ, Bohbot JD, Jones PL, Wang GR, Zwiebel LJ (2010) Distinct olfactory signaling mechanisms in the malaria vector mosquito Anopheles gambiae. PLoS Biol 8, e1000467
18. Lu T, Qiu YT, Wang G, Kwon J, Rutzler M, Kwon HW, Pitts RJ, Van Loon JJA, Takken W, Carlson JR, Zwiebel LJ (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol 17:1533–1544
19. Mboera LEG, Takken W (1997) Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and management programmes. Med Vet Entomol 85:355–368
20. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB (2014) Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156:1060–1071
21. Menger DJ, Van Loon JJA, Takken W (2014) Assessing the efficacy of candidate mosquito repellents against the background of an attractive source that mimics a human host. Med Vet Entomol doi:. doi:10.1111/mve.12061
22. Min SH, Ai MR, Shin SA, Suh GSB (2013) Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila. Proc Natl Acad Sci U S A 110:E1321–E1329
23. Mukabana WR, Mweresa CK, Otieno B, Omusula P, Smallegange RC, Van Loon JJA, Takken W (2012) A novel synthetic odorant blend for trapping of malaria and other African mosquitoes. J Chem Ecol 38:235–244
24. Mweresa C (2014) Odour-based strategies for surveillance and behavioural disruption of host-seeking malaria and other mosquitoes. PhD thesis, Wageningen University. 277 pp
25. Njiru BN, Mukabana WR, Takken W, Knols BG (2006) Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malar J 5:39
26. Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, Titus E, Munk C, Ngonyani H, Takken W et al (2010) Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PLoS One 5, e8951
27. Qiu YT, Van Loon JJA (2010) Olfactory physiology of blood-feeding vector mosquitoes. In: Takken W, Knols BGJ (eds) Olfaction in vector-host interactions. Wageningen Academic Publishers, Wageningen, pp 39–61
28. Qiu YT, Van Loon JJA, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses 31:845–863
29. 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
30. Rinker DC, Jones PL, Pitts RJ, Rutzler M, Camp G, Sun LJ, Xu PX, Dorset DC, Weaver D, Zwiebel LJ (2012) Novel high-throughput screens of Anopheles gambiae odorant receptors reveal candidate behaviour-modifying chemicals for mosquitoes. Physiol Entomol 37:33–41
31. Schmied WH, Takken W, Killeen GF, Knols BG, 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
32. 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
33. Smallegange RC, Qiu YT, Bukovinszkine-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 35:933–943
34. 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 47:338–344
35. Smallegange RC, Bukovinszkine-Kiss G, Otieno B, Mbadi PA, Takken W, Mukabana WR, 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
36. Smith EA, Macfarlane GT (1996) Studies on amine production in the human colon: enumeration of amine forming bacteria and physiological effects of carbohydrate and pH. Anaerobe 2:285–297
37. 2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol 33:116–122
38. Suer RA (2011) Unravelling the malaria mosquito’s sense of smell: neural and behavioural responses to human-derived compounds. PhD thesis, Wageningen University. 204 pp
39. Torr SJ, Hall DR, Phelps RJ, Vale GA (1997) Methods for dispensing odour attractants for tsetse flies (Diptera: Glossinidae). Bull Ent Res 87:299–311
40. Verhulst N, Beijleveld H, Knols B, Takken W, Schraa G, Bouwmeester H, Smallegange RC (2009) Cultured skin microbiota attracts malaria mosquitoes. Malar J 8:302
41. 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
42. Verhulst NO, Mbadi PA, Bukovinszkiné-Kiss G, Mukabana WR, Van Loon JJA, Takken W, And Smallegange RC (2011a) Improvement of a synthetic lure for Anopheles gambiae using compounds produced by human skin microbiota. Malar J 10:28
43. Verhulst NO, Mukabana WR, Takken W, Smallegange RC (2011b) Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae s.s. Entomol Exp Appl 139:170–179
44. Webster B, Lacey ES, Cardé RT (2015) Waiting with bated breath: opportunistic orientation to human odor in the malaria mosquito, Anopheles gambiae, is modulated by minute changes in carbon dioxide concentration. J Chem Ecol 49:55–66
45. WHO (2013) World Malaria report 2013. Geneva, Switzerland: World Health Organization. 253 pp
46. Williams CR, Bergbauer R, Geier M, Kline DL, Bernier UR, Russell RC, Ritchie SA (2006) Laboratory and field assessment of some kairomone blends for host-seeking Aedes aegypti. J Am Mosq Control Assoc 22:641–647
47. Zwiebel LJ, Takken W (2004) Olfactory regulation of mosquito-host interactions. Insect Biochem Mol Biol 34:645–652