Olfactory basis of floral preference of the malaria vector Anopheles gambiae (Diptera: Culicidae) among common African plants

Journal of Vector Ecology

Volumn 39, Issue 2, 2014, Pages 372-383

  Nikbakhtzadeh, Mahmood R ^a   Terbot II, John W ^a   Otienoburu, Philip E ^a   Foster, Woodbridge A ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Anopheles; Odor; Olfactometry; Plant attraction; Plant scent; Sugar feeding

Indexed keywords

ANOPHELES GAMBIAE; CULICIDAE; DIPTERA;

ANIMAL; ANOPHELES GAMBIAE; DISEASE CARRIER; FEEDING BEHAVIOR; MALARIA; ODOR; PHYSIOLOGY; TRANSMISSION;

ANIMALS; ANOPHELES GAMBIAE; FEEDING BEHAVIOR; INSECT VECTORS; MALARIA; ODORS;

EID: 84909968875     PISSN: 10811710     EISSN: 19487134     Source Type: Journal    
DOI: 10.3376/i1081-1710-39-372     Document Type: Article

References (51)

1. Baltussen, E., P. Sandra, F. David, and C. Cramers. 1999. Stir bar sorptive extraction (SBSE), a novel extraction technique for aqueous samples: theory and principles. J. Microcol. Separat. 11: 737-747.
2. Beier, J.C., G.C. Müller, W. Gu, K.L. Arheart, and Y. Schlein. 2012. Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malaria J. 11: 31. doi:10.1186/1475-2875-11-31.
3. Braks, M.A.H., S.A. Juliano, and L.P. Lounibos. 2006. Superior reproductive success on human blood without sugar is not limited to highly anthropophilic mosquito species. Med. Vet. Entomol. 20: 53-59.
4. Carson, C., M.A. Birkett, J.G. Logan, K. Mawa, H.V. Pates, J.A. Pickett, R.T. Rwegoshora, P.K. Tungu, and M.M. Cameron. 2010. Novel use of stir bar sorptive extraction (SBSE) as a tool for isolation of oviposition site attractants for gravid Culex quinquefasciatus. Bull. Entomol. Res. 100: 1-7.
5. David F. and P. Sandra. 2007. Stir bar sorptive extraction for trace analysis. J. Chromatogr. 1152: 54-69.
6. Dobson, H.E.M. 1994. Floral volatiles in insect biology. In: E. Bernays (ed.) Insect-plant Interactions V. Boca Raton: CRC Press. pp. 47-81.
7. Drabble, E. and H. Drabble. 1927. Some flowers and their dipteran visitors. New Phytol. 26: 115-123.
8. Foster, W.A. 1995. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 40: 443-474.
9. Foster, W.A. 2008. Phytochemicals as population sampling lures. J. Am. Mosq. Contr. Assoc. 24: 138-146.
10. Foster, W.A. and W. Takken. 2004. Nectar-related vs. human-related volatiles: behavioral response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding. Bull. Entomol. Res. 94: 145-157.
11. Gary, R.E. and W.A. Foster. 2001. Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 38: 22-28.
12. Gary, R.E. and W.A. Foster. 2004. Anopheles gambiae feeding and survival on honeydew and extra-floral nectar of peridomestic plants. Med. Vet. Entomol. 18: 102-107.
13. Geier, M., O.J. Bosch, and J. Boeckh. 1999. Ammonia as an attractive component of host odour for the yellow fever mosquito, Aedes aegypti. Chem. Senses 24: 647-653.
14. Gouagna, L.C., R.S. Poueme, K.R. Dabiré, J.B. Ouédraogo, D. Fontenille, and F. Simard. 2010. Patterns of sugar feeding and host plant preferences in adult males of An. gambiae (Diptera: Culicidae). J. Vector Ecol. 35: 267-276.
15. Gu, W., G. Müller, Y. Schlein, R.J. Novak, and J.C. Beier. 2011. Natural plant sugar sources of Anopheles mosquitoes strongly impact malaria transmission potential. PLoS One. 6: e15996.
16. Healy, T.P. and P.C. Jepson. 1988. The location of floral nectar sources by mosquitoes: the long range responses of Anopheles arabiensis Patton (Diptera: Culicidae) to Achillea millefolium flowers and isolated floral odour. Bull. Entomol. Res. 78: 651-657.
17. Impoinvil, D.E., J.O. Kongere, W.A. Foster, B.N. Njiru, G.F. Killeen, J.I. Githure, J.C. Beier, A. Hassanali, and B.G. Knols. 2004. Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya. Med. Vet. Entomol. 18: 108-115.
18. Jaenson, T.G.T, K. Pålsson, and A.-K. Borg-Karlson. 2006. Evaluation of extracts and oils of mosquito (Diptera: Culicidae) repellent plants from Sweden and Guinea-Bissau J. Med. Entomol. 43: 113-119.
19. Jhumur, U.S., S. Dötterl, and A. Jürgens. 2008. Floral odors of Silene otites: their variability and attractiveness to mosquitoes. J. Chem. Ecol. 34: 14-25.
20. Jürgens, A., A.C. Webber, and G. Gottsberger. 2000. Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55: 551-558.
21. Kartesz, J.T. 2011. Dactylis glomerata L. ssp. glomerata. In: Biota of North America program. United States Department of Agriculture [Internet]. Available from: URL http://plants.usda.gov/java/profile?symbol=DAGLG.
22. Knudsen, J.T., R. Eriksson, and J. Gershenzon. 2006. Diversity and distribution of floral scent. Bot. Rev. 72: 1-120.
23. Knudsen, J.T., L. Tollsten, and L.G. Bergström. 1993. Floral scents - A checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33: 253-280.
24. Koptur, S. 1992. Extrafloral nectar-mediated interactions between insects and plants. In: E.A. Bernays (ed.). Insect-Plant Interactions. pp. 81-129. CRC Press. Boca Raton.
25. Koptur, S. 2005. Nectar as fuel for plant protectors. In: F.L. Wäckers, P.C.J. Van Rijn, and J. Bruin (eds.) Plant-provided Food for Carnivorous Insects. A protective mutualism and its applications. pp. 75-108. Cambridge Univ. Press, Cambridge.
26. Manda, H., L.C. Gouagna, W.A. Foster, R.R. Jackson, J.C. Beier, J.I. Githure, and A. Hassanali. 2007a. Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malar. J. 6: 113. doi:10.1186/1475-2875-6-113.
27. Manda, H., L.C. Gouagna, E. Nyandat, E.W. Kabiru, R.R. Jackson, W.A. Foster, J.I. Githure, J.C. Beier, and A. Hassanali. 2007b. Discriminative feeding behaviour of Anopheles gambiae s.s. on endemic plants in western Kenya. Med. Vet. Entomol. 21: 103-111.
28. Mauer, D.J. and W.A. Rowley. 1999. Attraction of Culex pipiens pipiens (Diptera: Culicidae) to flower volatiles. J. Med. Entomol. 36: 503-507.
29. Miller, J.R. and K.L. Strickler. 1984. Finding and accepting host plants. In: W.J. Bell and R.T. Cardé (eds.) Chemical Ecology of Insects. pp. 127-157. Sinauer Assoc., Sunderland.
30. Müller, G.C. and Y. Schlein. 2006. Sugar questing mosquitoes in arid areas gather on scarce blossoms that can be used for control. Internat. J. Parasitol. 36: 1077-1080.
31. Müller, G.C., J.C. Beier, S.F. Traore, M.B. Toure, M.M. Traore, S. Bah, S. Doumbia, and Y. Schlein. 2010. Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar. J. 9: doi:10.1186/1475-2875-9-262.
32. Müller, G.C., V.D. Kravchenko, and Y. Schlein. 2008. Decline of Anopheles sergentii and Aedes caspius populations following presentation of attractive toxic (Spinosad) sugar bait stations in an oasis. J. Am. Mosq. Contr. Assoc. 24: 147-149.
33. Nyasembe, V.O. and B. Torto. 2013. Volatile phytochemicals as mosquito semiochemicals. Phytochem. Lett. 8: 196-201.
34. Nyasembe, V.O., P.E. Teal, W.R. Mukabana, J.H. Tumlinson, and B. Torto. 2012. Behavioural response of the malaria vector Anopheles gambiae to host plant volatiles and synthetic blends. Parasit. Vectors 5: 234. doi:10.1186/1756-3305-5-234.
35. Okech, B.A., L.C. Gouagna, G.F. Killeen, B.J. Knols, E.W. Kabiru, J.C. Beier, G. Yan, and J.I. 2003. Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semi-field conditions in western Kenya. J. Med. Entomol. 40: 657-663.
36. Otienoburu, P.E., B. Ebrahimi, P.L. Phelan, and W.A. Foster. 2012. Analysis and optimization of a synthetic milkweed floral attractant for mosquitoes. J. Chem. Ecol. 38: 873-881.
37. Pfannkoch, E., J. Whitecavage, and A. Hoffmann. 2002. Stir bar sorptive extraction: capacity and competition effects. Gerstel AppNote AN/2002/04-7.
38. Raguso, R.A. and E. Pichersky. 1999. A day in the life of a linalool molecule: chemical communication in a plant-pollinator system. Part 1: Linalool biosynthesis in flowering plants. Plant Species Biol. 14: 95-120.
39. Scascighini N, L. Mattiacci, M. D'Alessandro, A. Hern, A.S. Rott, and S. Dorn. 2005. New insights in analysing parasitoid attracting synomones: early volatile emission and use of stir bar sorptive extraction. Chemoecology 15: 97-104.
40. Shu, Y.M., L. Shenglian, and S.M. Phillips. 2006. Dactylis Linnaeus, Sp. Pl. 1: 71. 1753. Flora China 22: 309-310.
41. Stapel, J.O., A.M. Cortesero, C.M. De Moraes, J.H. Tumlinson, and W.J. Lewis. 1997. Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environ. Entomol. 26: 617-623.
42. Stone, C.M. and W.A. Foster. 2013. Plant-sugar feeding and vectorial capacity. In: C.J.M. Koenraadt and W. Takken (eds.) Ecology of vector-parasite interactions, vol. 3., pp. 35-79. Ecology & Control of Vector-Borne Diseases, W. Takken (ed.) Wageningen Academic Publ.
43. Stone, C.M., I.M. Hamilton, and W.A. Foster. 2011. A survival and reproduction trade-off is resolved in accordance with resource availability by virgin female mosquitoes. Anim. Behav. 81: 765-774.
44. Stone, C.M., B.T. Jackson, and W.A. Foster. 2012. Effects of plant-community composition on the vectorial capacity and fitness of the malaria mosquito Anopheles gambiae. Am. J. Trop. Med. Hyg. 87: 727-736.
45. Stone, C.M., R.M. Taylor, B.D. Roitberg, and W.A. Foster. 2009. Sugar deprivation reduces insemination of Anopheles gambiae (Diptera: Culicidae), despite daily recruitment of adults, and predicts decline in model populations. J. Med. Entomol. 46: 1327-1337.
46. Syed, Z. and W.S. Leal. 2009. Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc. Natl. Acad. Sci. 106: 18803-18808.
47. Takken, W. and D.L. Kline. 1989. Carbon dioxide and 1-octen-3-ol as mosquito attractants. J. Am. Mosq. Contr. Assoc. 5: 311-316.
48. Vargo, A.M. and W.A. Foster. 1982. Responsiveness of female Aedes aegypti (Diptera: Culicidae) to flower extracts. J. Med. Entomol. 19: 710-718.
49. Verhulst, N.O., W. Takken, and R.C. Smallegange. 2008. Structural design affects entry response of mosquitoes in olfactometers. Proc. Netherlands Entomol. Soc. Mtg. 19: 129-136.
50. Wäckers, F.L. 2005. Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In: F.L. Wäckers, P.C.J. Van Rijn, and J. Bruin, (eds). Plant-provided Food for Carnivorous Insects. A Protective Mutualism and its Applications. pp. 17-74. Cambridge Univ. Press, Cambridge.
51. Yuval, B. 1992. The other habit: sugar feeding by mosquitoes. Bull. Soc. Vector Ecol. 17: 150-156.