Skip to main content
Top
Published in: Malaria Journal 1/2011

Open Access 01-12-2011 | Research

Reduction in host-finding behaviour in fungus-infected mosquitoes is correlated with reduction in olfactory receptor neuron responsiveness

Authors: Justin George, Simon Blanford, Michael J Domingue, Matthew B Thomas, Andrew F Read, Thomas C Baker

Published in: Malaria Journal | Issue 1/2011

Login to get access

Abstract

Background

Chemical insecticides against mosquitoes are a major component of malaria control worldwide. Fungal entomopathogens formulated as biopesticides and applied as insecticide residual sprays could augment current control strategies and mitigate the evolution of resistance to chemical-based insecticides.

Methods

Anopheles stephensi mosquitoes were exposed to Beauveria bassiana or Metarhizium acridum fungal spores and sub-lethal effects of exposure to fungal infection were studied, especially the potential for reductions in feeding and host location behaviours related to olfaction. Electrophysiological techniques, such as electroantennogram, electropalpogram and single sensillum recording techniques were then employed to investigate how fungal exposure affected the olfactory responses in mosquitoes.

Results

Exposure to B. bassiana caused significant mortality and reduced the propensity of mosquitoes to respond and fly to a feeding stimulus. Exposure to M. acridum spores induced a similar decline in feeding propensity, albeit more slowly than B. bassiana exposure. Reduced host-seeking responses following fungal exposure corresponded to reduced olfactory neuron responsiveness in both antennal electroantennogram and maxillary palp electropalpogram recordings. Single cell recordings from neurons on the palps confirmed that fungal-exposed behavioural non-responders exhibited significantly impaired responsiveness of neurons tuned specifically to 1-octen-3-ol and to a lesser degree, to CO2.

Conclusions

Fungal infection reduces the responsiveness of mosquitoes to host odour cues, both behaviourally and neuronally. These pre-lethal effects are likely to synergize with fungal-induced mortality to further reduce the capacity of mosquito populations exposed to fungal biopesticides to transmit malaria.
Appendix
Available only for authorised users
Literature
1.
go back to reference Hemingway J, Ranson H: Insecticide resistance to insect vectors of human disease. Annu Rev Entomol. 2000, 45: 371-391. 10.1146/annurev.ento.45.1.371.CrossRefPubMed Hemingway J, Ranson H: Insecticide resistance to insect vectors of human disease. Annu Rev Entomol. 2000, 45: 371-391. 10.1146/annurev.ento.45.1.371.CrossRefPubMed
2.
go back to reference Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M: Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000, 14: 1-9. 10.1046/j.1365-2915.2000.00211.x.CrossRef Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M: Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol. 2000, 14: 1-9. 10.1046/j.1365-2915.2000.00211.x.CrossRef
3.
go back to reference Hargreaves K, Hunt RH, Brooke BD, Mthembu J, Weeto MM, Awolola TS, Coetzee M: Anopheles arabiensis and Anopheles quadriannulatus resistance to DDT in South Africa. Med Vet Entomol. 2003, 17: 417-422. 10.1111/j.1365-2915.2003.00460.x.CrossRefPubMed Hargreaves K, Hunt RH, Brooke BD, Mthembu J, Weeto MM, Awolola TS, Coetzee M: Anopheles arabiensis and Anopheles quadriannulatus resistance to DDT in South Africa. Med Vet Entomol. 2003, 17: 417-422. 10.1111/j.1365-2915.2003.00460.x.CrossRefPubMed
4.
go back to reference Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, Taylor ME, Small G, Hemingway J, Coetzee M: Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res. 2001, 91: 265-272. 10.1079/BER2001108.CrossRefPubMed Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, Taylor ME, Small G, Hemingway J, Coetzee M: Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res. 2001, 91: 265-272. 10.1079/BER2001108.CrossRefPubMed
5.
go back to reference Awolola TS, Brooke BD, Hunt RH, Coetzee M: Resistance of the malaria vector Anopheles gambiae to pyrethroid insecticides, in south-western Nigeria. Ann Trop Med Parasitol. 2002, 96: 849-852. 10.1179/000349802125002581.CrossRefPubMed Awolola TS, Brooke BD, Hunt RH, Coetzee M: Resistance of the malaria vector Anopheles gambiae to pyrethroid insecticides, in south-western Nigeria. Ann Trop Med Parasitol. 2002, 96: 849-852. 10.1179/000349802125002581.CrossRefPubMed
6.
go back to reference Diabate A, Brengues C, Baldet T, Dabire KR, Hougard JM, Akogbeto M, Kengne P, Simard F, Guillet P, Hemingway J, Chandre F: The spread of Leu-Phe-kdr mutation through Anopheles gambiae complex in Burkino Faso: genetic introgression and de novo phenomena. Trop Med Int Health. 2004, 9: 1267-1273. 10.1111/j.1365-3156.2004.01336.x.CrossRefPubMed Diabate A, Brengues C, Baldet T, Dabire KR, Hougard JM, Akogbeto M, Kengne P, Simard F, Guillet P, Hemingway J, Chandre F: The spread of Leu-Phe-kdr mutation through Anopheles gambiae complex in Burkino Faso: genetic introgression and de novo phenomena. Trop Med Int Health. 2004, 9: 1267-1273. 10.1111/j.1365-3156.2004.01336.x.CrossRefPubMed
7.
go back to reference Abdalla H, Matambo TS, Koekemoer LL, Mnzava AP, Hunt RH, Coetzee M: Insecticide susceptibility and vector status of natural populations of Anopheles arabiensis from Sudan. Trop Med Hyg. 2007, 102: 263-271.CrossRef Abdalla H, Matambo TS, Koekemoer LL, Mnzava AP, Hunt RH, Coetzee M: Insecticide susceptibility and vector status of natural populations of Anopheles arabiensis from Sudan. Trop Med Hyg. 2007, 102: 263-271.CrossRef
8.
go back to reference Ranson H, Abdalla H, Badolo A, Guelbeogo WM, Kerah-Hizoumbe C, Yangalbe-Kalnone E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae: data from the Þrst year of a multicountry study highlight the extent of the problem. Malar J. 2009, 8: 299-10.1186/1475-2875-8-299.PubMedCentralCrossRefPubMed Ranson H, Abdalla H, Badolo A, Guelbeogo WM, Kerah-Hizoumbe C, Yangalbe-Kalnone E, Sagnon N, Simard F, Coetzee M: Insecticide resistance in Anopheles gambiae: data from the Þrst year of a multicountry study highlight the extent of the problem. Malar J. 2009, 8: 299-10.1186/1475-2875-8-299.PubMedCentralCrossRefPubMed
9.
go back to reference Kikankie CK, Brook BD, Knols BGJ, Koekemoer LL, Farenhorst M, Hunt RH, Thomas MB, Coetzee M: The infectivity of the entomopathogenic fungus Beauveria bassiana to insecticide-resistant and susceptible Anopheles arabiensis at two different temperatures. Malar J. 2010, 9: 71-10.1186/1475-2875-9-71.PubMedCentralCrossRefPubMed Kikankie CK, Brook BD, Knols BGJ, Koekemoer LL, Farenhorst M, Hunt RH, Thomas MB, Coetzee M: The infectivity of the entomopathogenic fungus Beauveria bassiana to insecticide-resistant and susceptible Anopheles arabiensis at two different temperatures. Malar J. 2010, 9: 71-10.1186/1475-2875-9-71.PubMedCentralCrossRefPubMed
10.
go back to reference Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RC, Thomas MB, Koekemoer LL, Knols BGJ, Coetzee M: Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc Natl Acad Sci USA. 2009, 106: 17443-17447. 10.1073/pnas.0908530106.PubMedCentralCrossRefPubMed Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RC, Thomas MB, Koekemoer LL, Knols BGJ, Coetzee M: Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc Natl Acad Sci USA. 2009, 106: 17443-17447. 10.1073/pnas.0908530106.PubMedCentralCrossRefPubMed
11.
go back to reference Achonduh OA, Tondje PR: First report of pathogenicity of Beauveria bassiana RBL1034 to the malaria vector, Anopheles gambiae s.l. (Diptera: Culicidae) in Cameroon. African J Biotechnol. 2008, 7: 931-935. Achonduh OA, Tondje PR: First report of pathogenicity of Beauveria bassiana RBL1034 to the malaria vector, Anopheles gambiae s.l. (Diptera: Culicidae) in Cameroon. African J Biotechnol. 2008, 7: 931-935.
12.
go back to reference Mohanty SS, Raghavendra K, Rai U, Dash AP: Efficacy of female Culex quinquefasciatus with entomopathogenic fungus Fusarium pallidoroseum. Parasitol Res. 2008, 103: 171-174. 10.1007/s00436-008-0946-z.CrossRefPubMed Mohanty SS, Raghavendra K, Rai U, Dash AP: Efficacy of female Culex quinquefasciatus with entomopathogenic fungus Fusarium pallidoroseum. Parasitol Res. 2008, 103: 171-174. 10.1007/s00436-008-0946-z.CrossRefPubMed
13.
go back to reference De Paula AR, Brito ES, Pereira CR, Carrera MP, Samuels RI: Susceptibility of adult Aedes aegypti (Diptera: Culicidae) to infection with Metarhizium anisopliae and Beauveria bassiana: prospects for Dengue control. Biocont Sci Techn. 2008, 18: 1017-1025. 10.1080/09583150802509199.CrossRef De Paula AR, Brito ES, Pereira CR, Carrera MP, Samuels RI: Susceptibility of adult Aedes aegypti (Diptera: Culicidae) to infection with Metarhizium anisopliae and Beauveria bassiana: prospects for Dengue control. Biocont Sci Techn. 2008, 18: 1017-1025. 10.1080/09583150802509199.CrossRef
14.
go back to reference Blanford S, Chan BH, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB: Fungal pathogen reduces potential for malaria transmission. Science. 2005, 308: 1638-1641. 10.1126/science.1108423.CrossRefPubMed Blanford S, Chan BH, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB: Fungal pathogen reduces potential for malaria transmission. Science. 2005, 308: 1638-1641. 10.1126/science.1108423.CrossRefPubMed
15.
go back to reference Scholte E-J, Ng'habi K, Kihonda J, Takken W, Paaijmans K, Abdulla S, Killeen GF, Knols BG: An entomopathogenic fungus for control of adult African malaria mosquitoes. Science. 2005, 308: 1641-1642. 10.1126/science.1108639.CrossRefPubMed Scholte E-J, Ng'habi K, Kihonda J, Takken W, Paaijmans K, Abdulla S, Killeen GF, Knols BG: An entomopathogenic fungus for control of adult African malaria mosquitoes. Science. 2005, 308: 1641-1642. 10.1126/science.1108639.CrossRefPubMed
16.
17.
go back to reference Hancock PA, Thomas MB, Godfray HCJ: An age-structured model to evaluate the potential of novel malaria-control interventions: a case study of fungal biopesticide sprays. Proc Roy Soc (London). 2009, 276: 71-80. 10.1098/rspb.2008.0689.CrossRef Hancock PA, Thomas MB, Godfray HCJ: An age-structured model to evaluate the potential of novel malaria-control interventions: a case study of fungal biopesticide sprays. Proc Roy Soc (London). 2009, 276: 71-80. 10.1098/rspb.2008.0689.CrossRef
18.
go back to reference Maehara N, He HY, Shimazu M: Maturation feeding and transmission of Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) by Monochamus alternatus (Coleoptera: Cerambycidae) inoculated with Beauveria bassiana (Deuteromycotina: Hyphomycetes). J Econ Entomol. 2007, 100: 49-53. 10.1603/0022-0493(2007)100[49:MFATOB]2.0.CO;2.CrossRefPubMed Maehara N, He HY, Shimazu M: Maturation feeding and transmission of Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) by Monochamus alternatus (Coleoptera: Cerambycidae) inoculated with Beauveria bassiana (Deuteromycotina: Hyphomycetes). J Econ Entomol. 2007, 100: 49-53. 10.1603/0022-0493(2007)100[49:MFATOB]2.0.CO;2.CrossRefPubMed
19.
go back to reference Tefera T, Pringle KL: Food consumption by Chilo partellus (Lepidoptera: Pyralidae) larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of natural versus artificial diets on mortality and mycosis. J Invertebr Pathol. 2003, 84: 220-225. 10.1016/j.jip.2003.11.001.CrossRefPubMed Tefera T, Pringle KL: Food consumption by Chilo partellus (Lepidoptera: Pyralidae) larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of natural versus artificial diets on mortality and mycosis. J Invertebr Pathol. 2003, 84: 220-225. 10.1016/j.jip.2003.11.001.CrossRefPubMed
20.
go back to reference Arthurs SA, Thomas MB: Effects of a mycoinsecticide on feeding and fecundity of the brown locust, Locustana pardalina. Biocont Sci Techn. 2000, 10: 321-329. 10.1080/09583150050044592.CrossRef Arthurs SA, Thomas MB: Effects of a mycoinsecticide on feeding and fecundity of the brown locust, Locustana pardalina. Biocont Sci Techn. 2000, 10: 321-329. 10.1080/09583150050044592.CrossRef
21.
go back to reference Ekesi S, Maniania NK: Susceptibility of Megalurothrips sjostedti development stages to Metarhizium anisopliae and the effects of infection on feeding, adult fecundity, egg fertility and longevity. Entomol Exp Appl. 2000, 94: 229-236. 10.1046/j.1570-7458.2000.00624.x.CrossRef Ekesi S, Maniania NK: Susceptibility of Megalurothrips sjostedti development stages to Metarhizium anisopliae and the effects of infection on feeding, adult fecundity, egg fertility and longevity. Entomol Exp Appl. 2000, 94: 229-236. 10.1046/j.1570-7458.2000.00624.x.CrossRef
22.
go back to reference Ganassi S, Grazioso P, Moretti A, Sabatini MA: Effect of the fungus Lecanicillium lecanii on survival and reproduction of the aphid Schizaphis graminum. Biocontrol. 2010, 55: 299-312. 10.1007/s10526-009-9250-9.CrossRef Ganassi S, Grazioso P, Moretti A, Sabatini MA: Effect of the fungus Lecanicillium lecanii on survival and reproduction of the aphid Schizaphis graminum. Biocontrol. 2010, 55: 299-312. 10.1007/s10526-009-9250-9.CrossRef
23.
go back to reference Dembilio O, Quesada-Moraga E, Santiago-Alvarez C: Potential of an indigenous strain of the entomopathogenic fungus Beauveria bassiana as a biological control agent against the Red Plam Weevil, Rhynchophorus ferrugineus. J Invertebr Pathol. 2010, 104: 214-221. 10.1016/j.jip.2010.04.006.CrossRefPubMed Dembilio O, Quesada-Moraga E, Santiago-Alvarez C: Potential of an indigenous strain of the entomopathogenic fungus Beauveria bassiana as a biological control agent against the Red Plam Weevil, Rhynchophorus ferrugineus. J Invertebr Pathol. 2010, 104: 214-221. 10.1016/j.jip.2010.04.006.CrossRefPubMed
24.
go back to reference Shi WB, Feng MG: Effect of fungal infection on reproductive potential and survival time of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol. 2009, 48: 229-237. 10.1007/s10493-009-9238-2.CrossRefPubMed Shi WB, Feng MG: Effect of fungal infection on reproductive potential and survival time of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol. 2009, 48: 229-237. 10.1007/s10493-009-9238-2.CrossRefPubMed
25.
go back to reference Daniel C, Wyss E: Susceptibility of different life stages of the European cherry fruit fly, Rhagoletis cerasi to entomopathogenic fungi. J Appl Entomol. 2009, 133: 473-483. 10.1111/j.1439-0418.2009.01410.x.CrossRef Daniel C, Wyss E: Susceptibility of different life stages of the European cherry fruit fly, Rhagoletis cerasi to entomopathogenic fungi. J Appl Entomol. 2009, 133: 473-483. 10.1111/j.1439-0418.2009.01410.x.CrossRef
26.
go back to reference Hajek AE, Lund J, Smith MT: Reduction in fitness of female Asian longhorned beetle (Anoplophora glabripennis) infected with Metarhizium anisopliae. J Invertebr Pathol. 2008, 98: 198-205. 10.1016/j.jip.2007.12.003.CrossRefPubMed Hajek AE, Lund J, Smith MT: Reduction in fitness of female Asian longhorned beetle (Anoplophora glabripennis) infected with Metarhizium anisopliae. J Invertebr Pathol. 2008, 98: 198-205. 10.1016/j.jip.2007.12.003.CrossRefPubMed
27.
go back to reference Seyoum E, Bateman RP, Charnley AK: The effect of Metarhizium anisopliae var acridum on haemolymph energy reserves and flight capability in the desert locust, Shistocerca greagaria. J Appl Entomol. 2002, 126: 119-124. 10.1046/j.1439-0418.2002.00609.x.CrossRef Seyoum E, Bateman RP, Charnley AK: The effect of Metarhizium anisopliae var acridum on haemolymph energy reserves and flight capability in the desert locust, Shistocerca greagaria. J Appl Entomol. 2002, 126: 119-124. 10.1046/j.1439-0418.2002.00609.x.CrossRef
28.
go back to reference Seyoum E, Moore D, Charnley AK: Reduction in flight activity and food consumption by the desert locust, Schistocerca gregaria, after infection with Metarhizium flavoviride. J Appl Entomol. 1994, 118: 310-315. 10.1111/j.1439-0418.1994.tb00805.x.CrossRef Seyoum E, Moore D, Charnley AK: Reduction in flight activity and food consumption by the desert locust, Schistocerca gregaria, after infection with Metarhizium flavoviride. J Appl Entomol. 1994, 118: 310-315. 10.1111/j.1439-0418.1994.tb00805.x.CrossRef
29.
go back to reference Arthurs SA, Thomas MB: Investigation into behavioral changes in Schistocerca gregaria following infection with a mycoinsecticide: implications for susceptibility to predation. Ecol Entomol. 2001, 26: 227-234. 10.1046/j.1365-2311.2001.00317.x.CrossRef Arthurs SA, Thomas MB: Investigation into behavioral changes in Schistocerca gregaria following infection with a mycoinsecticide: implications for susceptibility to predation. Ecol Entomol. 2001, 26: 227-234. 10.1046/j.1365-2311.2001.00317.x.CrossRef
30.
go back to reference Thomas MB, Blanford S, Gbongbui C, Lomer CJ: Experimental studies to evaluate spray applications of a mycoinsecticide against the rice grasshopper, Hieroglyphus danganesis, in northern Benin. Entomol Exp Appl. 1998, 87: 93-102. 10.1046/j.1570-7458.1998.00309.x.CrossRef Thomas MB, Blanford S, Gbongbui C, Lomer CJ: Experimental studies to evaluate spray applications of a mycoinsecticide against the rice grasshopper, Hieroglyphus danganesis, in northern Benin. Entomol Exp Appl. 1998, 87: 93-102. 10.1046/j.1570-7458.1998.00309.x.CrossRef
31.
go back to reference Sewify GH, Hashem MY: Effects of the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin on cellular defence response and oxygen uptake of the wax moth Galleria mellonella L. (Pyralidae). J Appl Entomol. 2001, 125: 533-536. 10.1046/j.1439-0418.2001.00564.x.CrossRef Sewify GH, Hashem MY: Effects of the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin on cellular defence response and oxygen uptake of the wax moth Galleria mellonella L. (Pyralidae). J Appl Entomol. 2001, 125: 533-536. 10.1046/j.1439-0418.2001.00564.x.CrossRef
32.
go back to reference Pedrini N, Villaverde ML, Fuse CB, Dal Bello GM, Juarez MP: Beauveria bassiana infection alters colony development and defensive secretions of the beetles Tribolium castaneum and Ulomoides dermestoides (Coleoptera: Tenebrionidae). J Econ Entomol. 2010, 103: 1094-1099. 10.1603/EC10072.CrossRefPubMed Pedrini N, Villaverde ML, Fuse CB, Dal Bello GM, Juarez MP: Beauveria bassiana infection alters colony development and defensive secretions of the beetles Tribolium castaneum and Ulomoides dermestoides (Coleoptera: Tenebrionidae). J Econ Entomol. 2010, 103: 1094-1099. 10.1603/EC10072.CrossRefPubMed
33.
go back to reference Howard AFV, N'Guessan R, Koendraadt CJM, Asidi A, Farenhorst M, Akogbeto M, Thomas MB, Knols BGJ, Takken W: The entomopathogenic fungi Beauveria bassiana reduces instantaeneous blood feeding in wild multi-insecticide-resistant Culex quinquefasciatus mosquitoes un Benin, West Africa. Parasit Vectors. 2010, 3: 87-10.1186/1756-3305-3-87.PubMedCentralCrossRefPubMed Howard AFV, N'Guessan R, Koendraadt CJM, Asidi A, Farenhorst M, Akogbeto M, Thomas MB, Knols BGJ, Takken W: The entomopathogenic fungi Beauveria bassiana reduces instantaeneous blood feeding in wild multi-insecticide-resistant Culex quinquefasciatus mosquitoes un Benin, West Africa. Parasit Vectors. 2010, 3: 87-10.1186/1756-3305-3-87.PubMedCentralCrossRefPubMed
34.
go back to reference Scholte EJ, Knols BGJ, Takken W: Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J Invertebr Pathol. 2006, 91: 43-49. 10.1016/j.jip.2005.10.006.CrossRefPubMed Scholte EJ, Knols BGJ, Takken W: Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J Invertebr Pathol. 2006, 91: 43-49. 10.1016/j.jip.2005.10.006.CrossRefPubMed
35.
go back to reference Takken W, Knols BGJ: Odor mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol. 1999, 44: 131-157. 10.1146/annurev.ento.44.1.131.CrossRefPubMed Takken W, Knols BGJ: Odor mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol. 1999, 44: 131-157. 10.1146/annurev.ento.44.1.131.CrossRefPubMed
36.
go back to reference Hall DR, Beevor PS, Cork A, Nesbitt BF, Vale GA: 1-octen-3-ol, a potent olfactory stimulant and attractant for tsetse isolated from cattle odors. Insect Sci Appl. 1984, 5: 335-339. Hall DR, Beevor PS, Cork A, Nesbitt BF, Vale GA: 1-octen-3-ol, a potent olfactory stimulant and attractant for tsetse isolated from cattle odors. Insect Sci Appl. 1984, 5: 335-339.
37.
go back to reference Cork A, Park KC: Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts. Med Vet Entomol. 1996, 10: 269-276. 10.1111/j.1365-2915.1996.tb00742.x.CrossRefPubMed Cork A, Park KC: Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts. Med Vet Entomol. 1996, 10: 269-276. 10.1111/j.1365-2915.1996.tb00742.x.CrossRefPubMed
38.
go back to reference Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon WH, Pitts JR, van Loon JA, Takken W, Carlson JR, Zwiebel LJ: Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol. 2007, 17: 1533-1544. 10.1016/j.cub.2007.07.062.PubMedCentralCrossRefPubMed Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon WH, Pitts JR, van Loon JA, Takken W, Carlson JR, Zwiebel LJ: Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol. 2007, 17: 1533-1544. 10.1016/j.cub.2007.07.062.PubMedCentralCrossRefPubMed
39.
go back to reference Bell AS, Blandford S, Jenkins N, Thomas MB, Read AF: Real-time quantitative PCR for analysis of candidate fungal biopesticides against malaria: Technique validation and first applications. J Invertebr Pathol. 2009, 100: 160-168. 10.1016/j.jip.2009.01.006.PubMedCentralCrossRefPubMed Bell AS, Blandford S, Jenkins N, Thomas MB, Read AF: Real-time quantitative PCR for analysis of candidate fungal biopesticides against malaria: Technique validation and first applications. J Invertebr Pathol. 2009, 100: 160-168. 10.1016/j.jip.2009.01.006.PubMedCentralCrossRefPubMed
40.
go back to reference Bischoff JF, Rehner SA, Humber RA: A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia. 2009, 101: 508-528.CrossRef Bischoff JF, Rehner SA, Humber RA: A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia. 2009, 101: 508-528.CrossRef
41.
go back to reference Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M: Biological control of locusts and grasshoppers. Annu Rev Entomol. 2001, 46: 667-702. 10.1146/annurev.ento.46.1.667.CrossRefPubMed Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M: Biological control of locusts and grasshoppers. Annu Rev Entomol. 2001, 46: 667-702. 10.1146/annurev.ento.46.1.667.CrossRefPubMed
42.
go back to reference Ghaninia M, Hansson BS, Ignell R: The antennal lobe of the African malaria mosquito, Anopheles gambiae-innervation and three-dimensional reconstruction. Arthr Struct Dev. 2007, 36: 23-39. 10.1016/j.asd.2006.06.004.CrossRef Ghaninia M, Hansson BS, Ignell R: The antennal lobe of the African malaria mosquito, Anopheles gambiae-innervation and three-dimensional reconstruction. Arthr Struct Dev. 2007, 36: 23-39. 10.1016/j.asd.2006.06.004.CrossRef
43.
go back to reference Stensmyr MC, Dekker T, Hansson BS: Evolution of the olfactory code in the Drosophila melanogaster subgroup. Proc Biol Sci. 2003, 270: 2333-2340. 10.1098/rspb.2003.2512.PubMedCentralCrossRefPubMed Stensmyr MC, Dekker T, Hansson BS: Evolution of the olfactory code in the Drosophila melanogaster subgroup. Proc Biol Sci. 2003, 270: 2333-2340. 10.1098/rspb.2003.2512.PubMedCentralCrossRefPubMed
44.
go back to reference Qiu YT, Van Loon JJA, Takken W, Meijerink J, Smid HM: Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses. 2006, 31: 845-863. 10.1093/chemse/bjl027.CrossRefPubMed Qiu YT, Van Loon JJA, Takken W, Meijerink J, Smid HM: Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses. 2006, 31: 845-863. 10.1093/chemse/bjl027.CrossRefPubMed
45.
go back to reference Gillies MT: The role of carbon dioxide in host finding by mosquitoes (Diptera; Culicidae): a review. Bull Entomol Res. 1980, 70: 525-532. 10.1017/S0007485300007811.CrossRef Gillies MT: The role of carbon dioxide in host finding by mosquitoes (Diptera; Culicidae): a review. Bull Entomol Res. 1980, 70: 525-532. 10.1017/S0007485300007811.CrossRef
46.
go back to reference Dekker T, Takken W, Carde RT: Structure of host odour plumes influences catch of Anopheles gambiae s.s. and Aedes aegypti in a dual-choice olfactometer. Physiol Entomol. 2001, 26: 124-134. 10.1046/j.1365-3032.2001.00225.x.CrossRef Dekker T, Takken W, Carde RT: Structure of host odour plumes influences catch of Anopheles gambiae s.s. and Aedes aegypti in a dual-choice olfactometer. Physiol Entomol. 2001, 26: 124-134. 10.1046/j.1365-3032.2001.00225.x.CrossRef
47.
go back to reference Cooperband MF, Cardé RT: Orientation of Culex mosquitoes to carbon dioxide-baited traps: flight maneuvers and trapping efficiency. Med Vet Entomol. 2006, 26: 11-26.CrossRef Cooperband MF, Cardé RT: Orientation of Culex mosquitoes to carbon dioxide-baited traps: flight maneuvers and trapping efficiency. Med Vet Entomol. 2006, 26: 11-26.CrossRef
48.
go back to reference Kwon JY, Dahanukar A, Weiss LA, Carlson JR: The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA. 2007, 104: 3574-3578. 10.1073/pnas.0700079104.PubMedCentralCrossRefPubMed Kwon JY, Dahanukar A, Weiss LA, Carlson JR: The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA. 2007, 104: 3574-3578. 10.1073/pnas.0700079104.PubMedCentralCrossRefPubMed
49.
go back to reference Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB: Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature. 2007, 445: 86-90. 10.1038/nature05466.CrossRefPubMed Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB: Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature. 2007, 445: 86-90. 10.1038/nature05466.CrossRefPubMed
50.
go back to reference Vosshall LB, Hansson BS: A unified nomenclature system for the insect olfactory coreceptor. Chem Senses. 2011, 36: 497-498. 10.1093/chemse/bjr022.CrossRefPubMed Vosshall LB, Hansson BS: A unified nomenclature system for the insect olfactory coreceptor. Chem Senses. 2011, 36: 497-498. 10.1093/chemse/bjr022.CrossRefPubMed
51.
go back to reference Xia Y, Wang G, Buscariollo D, Pitts RJ, Wenger H, Zwiebel LJ: The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proc Natl Acad Sci USA. 2008, 105: 6433-6438. 10.1073/pnas.0801007105.PubMedCentralCrossRefPubMed Xia Y, Wang G, Buscariollo D, Pitts RJ, Wenger H, Zwiebel LJ: The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proc Natl Acad Sci USA. 2008, 105: 6433-6438. 10.1073/pnas.0801007105.PubMedCentralCrossRefPubMed
52.
go back to reference Kershaw MJ, Moorhouse ER, Bateman R, Reynolds SE, Charnley AK: The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. J Invertebr Pathol. 1999, 74: 213-223. 10.1006/jipa.1999.4884.CrossRefPubMed Kershaw MJ, Moorhouse ER, Bateman R, Reynolds SE, Charnley AK: The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. J Invertebr Pathol. 1999, 74: 213-223. 10.1006/jipa.1999.4884.CrossRefPubMed
53.
go back to reference Hajek AE, St Leger RJ: Interactions between fungal pathogens and insect hosts. Annu Rev Entomol. 1994, 39: 293-322. 10.1146/annurev.en.39.010194.001453.CrossRef Hajek AE, St Leger RJ: Interactions between fungal pathogens and insect hosts. Annu Rev Entomol. 1994, 39: 293-322. 10.1146/annurev.en.39.010194.001453.CrossRef
54.
go back to reference Hung H, Bouchias DG: Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua. J Invertebr Pathol. 1992, 60: 152-158. 10.1016/0022-2011(92)90089-M.CrossRef Hung H, Bouchias DG: Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua. J Invertebr Pathol. 1992, 60: 152-158. 10.1016/0022-2011(92)90089-M.CrossRef
55.
go back to reference Elliot SL, Horton CM, Blanford S, Thomas MB: Impacts of fever on locust life-history traits: costs or benefits?. Biol Lett. 2005, 1: 181-184. 10.1098/rsbl.2004.0279.PubMedCentralCrossRefPubMed Elliot SL, Horton CM, Blanford S, Thomas MB: Impacts of fever on locust life-history traits: costs or benefits?. Biol Lett. 2005, 1: 181-184. 10.1098/rsbl.2004.0279.PubMedCentralCrossRefPubMed
56.
go back to reference Zhao H, Charnley AK, Wang ZK, Yin YP, Li YL, Li ZL, Peng GX, Xia YX: Identification of an extracellular acid trehalase and its gene involving in fungal pathogenesis from Metarizium anisopliae. J Biochem. 2006, 140: 319-327. 10.1093/jb/mvj159.CrossRefPubMed Zhao H, Charnley AK, Wang ZK, Yin YP, Li YL, Li ZL, Peng GX, Xia YX: Identification of an extracellular acid trehalase and its gene involving in fungal pathogenesis from Metarizium anisopliae. J Biochem. 2006, 140: 319-327. 10.1093/jb/mvj159.CrossRefPubMed
Metadata
Title
Reduction in host-finding behaviour in fungus-infected mosquitoes is correlated with reduction in olfactory receptor neuron responsiveness
Authors
Justin George
Simon Blanford
Michael J Domingue
Matthew B Thomas
Andrew F Read
Thomas C Baker
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2011
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-10-219

Other articles of this Issue 1/2011

Malaria Journal 1/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.