Exploiting the behaviour of wild malaria vectors to achieve high infection with fungal biocontrol agents

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Mnyone, Ladslaus L ^a,b,c   Lyimo, Issa N ^a,d   Lwetoijera, Dickson W ^a   Mpingwa, Monica W ^a   Nchimbi, Nuru ^a   Hancock, Penelope A ^e   Russell, Tanya L ^a,f,g   Kirby, Matthew J ^a,b   Takken, Willem ^b   Koenraadt, Constantianus J M ^b  

^a IFAKARA HEALTH INSTITUTE   (Tanzania)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c SOKOINE UNIVERSITY OF AGRICULTURE   (Tanzania)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF WARWICK   (United Kingdom)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MINERAL OIL;

ANOPHELES; ANOPHELES ARABIENSIS; ANOPHELES FUNESTUS; ANOPHELES GAMBIAE; ARTICLE; BEAUVERIA BASSIANA; BEHAVIOR; DISEASE TRANSMISSION; ENTOMOPATHOGENIC FUNGUS; HOST PARASITE INTERACTION; MALARIA; METARHIZIUM ANISOPLIAE; MYCOSIS; NONHUMAN; SURVIVAL; TANZANIA; ANIMAL; BEAUVERIA; BED NET; BIOLOGICAL CONTROL AGENT; DISEASE CARRIER; FEEDING BEHAVIOR; FEMALE; METARHIZIUM; MICROBIOLOGY; MOSQUITO; PHYSIOLOGY;

ANIMALS; ANOPHELES; BEAUVERIA; BIOLOGICAL CONTROL AGENTS; FEEDING BEHAVIOR; FEMALE; INSECT VECTORS; INSECTICIDE-TREATED BEDNETS; MALARIA; METARHIZIUM; MOSQUITO CONTROL; SURVIVAL ANALYSIS; TANZANIA;

EID: 84858710002     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-87     Document Type: Article

References (46)

1. A research agenda for malaria eradication: vector control. Alonso PL, Besansky NJ, Burkot TR, Collins FH, Hemingway J, James AA, Lengeler C, Lindsay S, Liu Q, Lobo NF, Mnzava A, Tanner M, Zwiebel L, PLoS Med 2011 8 1000401 21311587
2. A research agenda for malaria eradication: basic science and enabling technologies. Baum J, Billker O, Bousema T, Dinglasan R, McGovern V, Mota MM, Mueller I, Sinden R, PLoS Med 2011 8 1000399 21311584
3. Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Kelly-Hope L, Ranson H, Hemingway J, Lancet Infect Dis 2008 8 387 389 10.1016/S1473-3099(08)70045-8 18374633
4. Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, Yangalbe-Kalnone E, Sagnon N, Simard F, Coetzee M, Malar J 2009 8 299 10.1186/1475-2875-8-299 20015411
5. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, Trends Parasitol 2011 27 91 98 10.1016/j.pt.2010.08.004 20843745
6. Mosquitoes score in chemical war. Butler D, Nature 2011 475 19 10.1038/475019a 21734682
7. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. N'Guessan R, Corbel V, Akogbeto M, Rowland M, Emerg Infect Dis 2007 13 199 206 10.3201/eid1302. 060631 17479880 (Pubitemid 46193161)
8. Insecticide resistance status in Anopheles gambiae in southern Benin. Yadouleton AW, Padonou G, Asidi A, Moiroux N, Bio-Banganna S, Corbel V, N'guessan R, Gbenou D, Yacoubou I, Gazard K, Akogbeto MC, Malar J 2010 9 83 10.1186/1475-2875-9-83 20334637
9. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Toure-Balde A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C, Lancet Infect Dis 2011 11 925 932 10.1016/S1473-3099(11)70194-3 21856232
10. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basanez M-G, Ghani AC, PLoS Med 2010 7 1000324 10.1371/journal.pmed.1000324 20711482
11. Fungal pathogen reduces potential for malaria transmission. Blanford S, Chan BHK, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB, Science 2005 308 1638 1641 10.1126/science.1108423 15947189 (Pubitemid 40807515)
12. African water storage pots for the delivery of the entomopathogenic fungus Metarhizium anisopliae to the malaria vectors Anopheles gambiae s.s. and Anopheles funestus. Farenhorst M, Farina D, Scholte EJ, Takken W, Hunt RH, Coetzee M, Knols BGJ, Am J Trop Med Hyg 2008 78 910 916 18541768 (Pubitemid 351980734)
13. An extra-domiciliary method of delivering entomopathogenic fungus, Metharizium anisopliae IP 46 for controlling adult populations of the malaria vector. Lwetoijera DW, Sumaye RD, Madumla EP, Kavishe DR, Mnyone LL, Russell TL, Okumu FO, Anopheles arabiensis. Parasit Vectors 2010 3 18 10.1186/1756-3305-3- 18
14. Infection of the malaria mosquito, Anopheles gambiae, with two species of entomopathogenic fungi: effects of concentration, co-formulation, exposure time and persistence. Mnyone LL, Kirby MJ, Lwetoijera DW, Mpingwa MW, Knols BGJ, Takken W, Russell TL, Malar J 2009 8 309 10.1186/1475-2875-8-309 20030834
15. An entomopathogenic fungus for control of adult African malaria mosquitoes. Scholte EJ, Ng'habi K, Kihonda J, Takken W, Paaijmans K, Abdulla S, Killeen GF, Knols BGJ, Science 2005 308 1641 1642 10.1126/science.1108639 15947190 (Pubitemid 40807516)
16. Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. Farenhorst M, Knols BGJ, Thomas MB, Howard AFV, Takken W, Rowland M, N'Guessan R, PLoS One 2010 5 12081 10.1371/journal.pone.0012081 20711409
17. Fungal infection counters insecticide resistance in African malaria mosquitoes. Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RH, Thomas MB, Koekemoer LL, Knols BGJ, Coetzee M, Proc Natl Acad Sci USA 2009 106 17443 17447 10.1073/pnas.0908530106 19805146
18. The infectivity of the entomopathogenic fungus Beauveria bassiana to insecticide-resistant and susceptible Anopheles arabiensis mosquitoes at two different temperatures. Kikankie CK, Brooke BD, Knols BGJ, Koekemoer LL, Farenhorst M, Hunt RH, Thomas MB, Coetzee M, Malar J 2010 9 71 10.1186/1475-2875-9-71 20210990
19. Viability of GM fungi crucial to malaria control. Koenraadt CJM, Takken W, Science 2011 332 175 21474739
20. Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Lines JD, Myamba J, Curtis CF, Med Vet Entomol 1987 1 37 51 10.1111/j.1365-2915.1987.tb00321.x 2979519
21. Importance of eaves to house entry by anopheline, but not culicine, mosquitoes. Njie M, Dilger E, Lindsay SW, Kirby MJ, J Med Entomol 2009 46 505 510 10.1603/033.046.0314 19496420
22. Studies on house leaving and outside resting of Anopheles gambiae Giles and Anopheles funestus Giles in East Africa. II. The ecodus from houses and the house resting population. Gillies MT, Bull Entomol Res
23. A new resting trap to sample fungus-infected mosquitoes, and the pathogenicity of Lecanicillium muscarium to culicid adults. Luz C, Mnyone LL, Sangusangu R, Lyimo IN, Rocha LFN, Humber RA, Russell TL, Acta Trop 2010 116 105 107 10.1016/j.actatropica.2010.05.001 20452324
24. Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. Hughes WO, Petersen KS, Ugelvig LV, Pedersen D, Thomsen L, Poulsen M, Boomsma JJ, BMC Evol Biol 2004 4 45 10.1186/1471-2148-4-45 15541185 (Pubitemid 39660388)
25. Dose-response and age- and temperature-related susceptibility of the diamondback moth (Lepidoptera: Plutellidae) to two isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Vandenberg JD, Ramos M, Altre JA, Environ Entomol 1998 27 1017 1021 (Pubitemid 128482896)
26. Density-independent feeding success of malaria vectors (Diptera, Culicidae) in Tanzania. Charlwood JD, Smith T, Kihonda J, Heiz B, Billingsley PF, Takken W, Bull Entomol Res 1995 85 29 35 10.1017/S0007485300051981 (Pubitemid 26451297)
27. 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, Mshinda H, Mukabana WR, Moore SJ, PLoS One 2010 5 8951 10.1371/journal.pone.0008951 20126628
28. Impact of promoting longer-lasting insecticide treatment of bed nets upon malaria transmission in a rural Tanzanian setting with pre-existing high coverage of untreated nets. Russell TL, Lwetoijera DW, Maliti D, Chipwaza B, Kihonda J, Charlwood JD, Smith TA, Lengeler C, Mwanyangala MA, Nathan R, Knols BGJ, Takken W, Killeen GF, Malar J 2010 9 187 10.1186/1475-2875-9-187 20579399
29. First report of Metarhizium anisopliae IP 46 pathogenicity in adult Anopheles gambiae s.s. and An. Mnyone LL, Russell TL, Lyimo IN, Lwetoijera DW, Kirby MJ, Luz C, arabiensis (Diptera; Culicidae). Parasit Vectors 2009 2 59 22065788
30. A novel method for standardized application of fungal spore coatings for mosquito exposure bioassays. Farenhorst M, Knols BGJ, Malar J 2010 9 27 10.1186/1475-2875-9-27 20089180
31. Screening mosquito house entry points as a potential method for integrated control of endophagic filariasis, arbovirus and malaria vectors. Ogoma SB, Lwetoijera DW, Ngonyani H, Furer B, Russell TL, Mukabana WR, Killeen GF, Moore SJ, PLoS Neglect Trop D 2010 4 773 10.1371/journal.pntd.0000773
32. A modification to an experimental hut to reduce mosquito eaves-egress. Smith A, Hudson JE, WHO/Mal/72.775 1972:6
33. An age-structured model to evaluate the potential of novel malaria-control interventions: a case study of fungal biopesticide sprays. Hancock PA, Thomas MB, Godfray HCJ, Proc R Soc B-Biol Sci 2009 276 71 80 10.1098/rspb.2008.0689
34. Statics and dynamics of malaria infection in Anopheles mosquitoes. Smith DL, McKenzie FE, Malar J 2004 3 13 10.1186/1475-2875-3-13 15180900 (Pubitemid 39319760)
35. 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, Malar J 2011 10 80 10.1186/1475-2875-10-80 21477321
36. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. Killeen GF, Smith TA, Ferguson HM, Mshinda H, Abdulla S, Lengeler C, Kachur SP, PLoS Med 2007 4 1246 1258 (Pubitemid 47196227)
37. Feeding and resting behaviour of malaria vector, Anopheles arabiensis with reference to zooprophylaxis. Mahande A, Mosha F, Mahande J, Kweka E, Malar J 2007 6
38. Pyrethroid resistance in Anopheles gambiae leads to increased susceptibility to the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Howard AFV, Koenraadt CJM, Farenhorst M, Knols BGJ, Takken W, Malar J 2010 9 168 10.1186/1475-2875-9-168 20553597
39. Tools for delivering entomopathogenic fungi to malaria mosquitoes: effects of delivery surfaces on fungal efficacy and persistence. Mnyone LL, Kirby MJ, Lwetoijera DW, Mpingwa MW, Simfukwe ET, Knols BGJ, Takken W, Russell TL, Malar J 2010 9 246 10.1186/1475-2875-9-246 20799967
40. Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. Bogus MI, Kedra E, Bania J, Szczepanik M, Czygier M, Jablonski P, Pasztaleniec A, Samborski J, Mazgajska J, Polanowski A, J Insect Physiol 2007 53 909 922 10.1016/j.jinsphys.2007.02.016 17512001 (Pubitemid 47313469)
41. Combining fungal biopesticides and insecticide-treated bednets to enhance malaria control. Hancock PA, PLoS Comput Biol 2009 5 1000525 10.1371/journal.pcbi.1000525 19798436
42. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island. Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA, Equatorial Guinea. Malar J 2011 10 184
43. Short Report: insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Govella NJ, Okumu FO, Killeen GF, Am J Trop Med Hyg 2010 82 415 419 10.4269/ajtmh.2010.09-0579 20207866
44. Anopheline and culicine mosquitoes are not repelled by surfaces treated with the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Mnyone LL, Koenraadt CJM, Lyimo IN, Mpingwa MW, Takken W, Russell TL, Parasit Vectors 2010 3 80 10.1186/1756-3305-3-80 20799937
45. Lethal and pre-lethal effects of a fungal biopesticide contribute to substantial and rapid control of malaria vectors. Blanford S, Shi WP, Christian R, Marden JH, Koekemoer LL, Brooke BD, Coetzee M, Read AF, Thomas MB, PLoS One 2011 6 23591 10.1371/journal.pone.0023591 21897846
46. Can fungal biopesticides control malaria? Thomas MB, Read AF, Nat Rev Microbiol 2007 5 377 383 10.1038/nrmicro1638 17426726 (Pubitemid 46605491)