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Published in: Malaria Journal 1/2003

Open Access 01-12-2003 | Research

Infection of malaria (Anopheles gambiae s.s.) and filariasis (Culex quinquefasciatus) vectors with the entomopathogenic fungus Metarhizium anisopliae

Authors: Ernst-Jan Scholte, Basilio N Njiru, Renate C Smallegange, Willem Takken, Bart GJ Knols

Published in: Malaria Journal | Issue 1/2003

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Abstract

Background

Current intra-domiciliary vector control depends on the application of residual insecticides and/or repellents. Although biological control agents have been developed against aquatic mosquito stages, none are available for adults. Following successful use of an entomopathogenic fungus against tsetse flies (Diptera: Glossinidae) we investigated the potency of this fungus as a biological control agent for adult malaria and filariasis vector mosquitoes.

Methods

In the laboratory, both sexes of Anopheles gambiae sensu stricto and Culex quinquefasciatus were passively contaminated with dry conidia of Metarhizium anisopliae. Pathogenicity of this fungus for An. gambiae was further tested for varying exposure times and different doses of oil-formulated conidia.

Results

Comparison of Gompertz survival curves and LT50 values for treated and untreated specimens showed that, for both species, infected mosquitoes died significantly earlier (p < 0.0001) than uninfected control groups. No differences in LT50 values were found for different exposure times (24, 48 hrs or continuous exposure) of An. gambiae to dry conidia. Exposure to oil-formulated conidia (doses ranging from 1.6 × 107 to 1.6 × 1010 conidia/m2) gave LT50 values of 9.69 ± 1.24 (lowest dose) to 5.89 ± 0.35 days (highest dose), with infection percentages ranging from 4.4–83.7%.

Conclusion

Our study marks the first to use an entomopathogenic fungus against adult Afrotropical disease vectors. Given its high pathogenicity for both adult Anopheles and Culex mosquitoes we recommend development of novel targeted indoor application methods for the control of endophagic host-seeking females.
Appendix
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Literature
1.
go back to reference WHO: WHO expert committee on malaria, WHO Technical Report Series 892. Geneva, Switzerland. 2000 WHO: WHO expert committee on malaria, WHO Technical Report Series 892. Geneva, Switzerland. 2000
2.
go back to reference WHO: Lymphatic filariasis: The disease and its control. 5th report: WHO Expert Committee on Filariasis. Technical Report Series 821. Geneva, Switserland. 1992 WHO: Lymphatic filariasis: The disease and its control. 5th report: WHO Expert Committee on Filariasis. Technical Report Series 821. Geneva, Switserland. 1992
3.
go back to reference Curtis CF: Should the use of DDT be revived for malaria vector control?. Biomédica. 2002, 22: 455-461.CrossRefPubMed Curtis CF: Should the use of DDT be revived for malaria vector control?. Biomédica. 2002, 22: 455-461.CrossRefPubMed
4.
go back to reference Lengeler C: Insecticide-treated bednets and curtains for preventing malaria. Cochrane Library Reports. 1998, 3: 1-70. Lengeler C: Insecticide-treated bednets and curtains for preventing malaria. Cochrane Library Reports. 1998, 3: 1-70.
5.
go back to reference Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P: Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999, 77: 230-234.PubMedCentralPubMed Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P: Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ. 1999, 77: 230-234.PubMedCentralPubMed
6.
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: 181-189. 10.1046/j.1365-2915.2000.00234.x.CrossRefPubMed 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: 181-189. 10.1046/j.1365-2915.2000.00234.x.CrossRefPubMed
7.
go back to reference Zaim M, Guillet P: Alternative insecticides: An urgent need. Trends Parasitol. 2002, 18: 161-163. 10.1016/S1471-4922(01)02220-6.CrossRefPubMed Zaim M, Guillet P: Alternative insecticides: An urgent need. Trends Parasitol. 2002, 18: 161-163. 10.1016/S1471-4922(01)02220-6.CrossRefPubMed
8.
go back to reference Ariee F, Ernst WHO, Sijm DTHM: Natural and synthetic organic compounds in the environment-a Symposium report. Environ Toxicol Pharmacol. 2001, 10: 65-80. 10.1016/S1382-6689(01)00090-4.CrossRef Ariee F, Ernst WHO, Sijm DTHM: Natural and synthetic organic compounds in the environment-a Symposium report. Environ Toxicol Pharmacol. 2001, 10: 65-80. 10.1016/S1382-6689(01)00090-4.CrossRef
9.
go back to reference World Wildlife Fund: Hazards and exposures associated with DDT and synthetic pyrethroids used for vector control. WWF, Toronto, Canada. 1999 World Wildlife Fund: Hazards and exposures associated with DDT and synthetic pyrethroids used for vector control. WWF, Toronto, Canada. 1999
10.
go back to reference Turusov V, Rakitsky V, Tomatis L: Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect. 2002, 110: 125-128.PubMedCentralCrossRefPubMed Turusov V, Rakitsky V, Tomatis L: Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect. 2002, 110: 125-128.PubMedCentralCrossRefPubMed
11.
go back to reference Chandre F, Darriet F, Darder M, Cuany A, Doannio JM, Pasteur N, Guillet P: Pyrethroid resistance in Culex quinquefasciatus from west Africa. Med Vet Entomol. 1998, 12: 359-366. 10.1046/j.1365-2915.1998.00120.x.CrossRefPubMed Chandre F, Darriet F, Darder M, Cuany A, Doannio JM, Pasteur N, Guillet P: Pyrethroid resistance in Culex quinquefasciatus from west Africa. Med Vet Entomol. 1998, 12: 359-366. 10.1046/j.1365-2915.1998.00120.x.CrossRefPubMed
12.
go back to reference Ramaiah KD, Vanamail P, Pani SP, Yuvaraj J, Das PK: The effect of six rounds of single dose mass treatment with diethylcarbamazine or ivermectin on Wuchereria bancrofti infection and its implications for lymphatic filariasis elimination. Trop Med Int Health. 2002, 7: 767-74. 10.1046/j.1365-3156.2002.00935.x.CrossRefPubMed Ramaiah KD, Vanamail P, Pani SP, Yuvaraj J, Das PK: The effect of six rounds of single dose mass treatment with diethylcarbamazine or ivermectin on Wuchereria bancrofti infection and its implications for lymphatic filariasis elimination. Trop Med Int Health. 2002, 7: 767-74. 10.1046/j.1365-3156.2002.00935.x.CrossRefPubMed
13.
go back to reference Burkot T, Ichimori K: The PacELF programme: will mass drug administration be enough?. Trends Parasitol. 2002, 18: 109-115. 10.1016/S1471-4922(01)02221-8.CrossRefPubMed Burkot T, Ichimori K: The PacELF programme: will mass drug administration be enough?. Trends Parasitol. 2002, 18: 109-115. 10.1016/S1471-4922(01)02221-8.CrossRefPubMed
14.
go back to reference Sunish IP, Rajendran R, Mani TR, Munirathinam A, Tewari SC, Hiriyan J, Gajanana A, Satyanarayana K: Resurgence in filarial transmission after withdrawal of mass drug administration and the relationship between antigenaemia and microfilaraemia – a longitudinal study. Trop Med Int Health. 2002, 7: 59-69. 10.1046/j.1365-3156.2002.00828.x.CrossRefPubMed Sunish IP, Rajendran R, Mani TR, Munirathinam A, Tewari SC, Hiriyan J, Gajanana A, Satyanarayana K: Resurgence in filarial transmission after withdrawal of mass drug administration and the relationship between antigenaemia and microfilaraemia – a longitudinal study. Trop Med Int Health. 2002, 7: 59-69. 10.1046/j.1365-3156.2002.00828.x.CrossRefPubMed
16.
go back to reference Lacey LA, Undeen AH: Microbial control of black flies and mosquitoes. Annu Rev Entomol. 1986, 25: 265-296. 10.1146/annurev.en.31.010186.001405.CrossRef Lacey LA, Undeen AH: Microbial control of black flies and mosquitoes. Annu Rev Entomol. 1986, 25: 265-296. 10.1146/annurev.en.31.010186.001405.CrossRef
17.
go back to reference Federici BA: The future of microbial insecticides as vector control agents. J Am Mosq Control Assoc. 1995, 11: 260-268.PubMed Federici BA: The future of microbial insecticides as vector control agents. J Am Mosq Control Assoc. 1995, 11: 260-268.PubMed
18.
go back to reference Becker N, Margalit J: Use of Bacillus thuringiensis israelensis against mosquitoes and blackflies. In: Bacillus thuringiensis, an environmental pesticide: theory and practice. Edited by: Entwistle PF, Cory JS, Bailey MJ, Higgs S. Wiley & Sons, Chichester, 147-170. Becker N, Margalit J: Use of Bacillus thuringiensis israelensis against mosquitoes and blackflies. In: Bacillus thuringiensis, an environmental pesticide: theory and practice. Edited by: Entwistle PF, Cory JS, Bailey MJ, Higgs S. Wiley & Sons, Chichester, 147-170.
19.
go back to reference Fillinger U, Knols BGJ, Becker N: Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and B. sphaericus formulations against the malaria vector Anopheles gambiae in Western Kenya. Trop Med Intl Health. 2003, 8: 37-48. 10.1046/j.1365-3156.2003.00979.x.CrossRef Fillinger U, Knols BGJ, Becker N: Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and B. sphaericus formulations against the malaria vector Anopheles gambiae in Western Kenya. Trop Med Intl Health. 2003, 8: 37-48. 10.1046/j.1365-3156.2003.00979.x.CrossRef
20.
go back to reference Zaim M, Ladonni H, Ershadi MRY, Manouchehri AV, Sahabi Z, Nazari M, Shahmohammadi H: Field application of Romanomermis culicivorax (Mermithidae: Nematoda) to control anopheline larvae in southern Iran. J Am Mosq Control Assoc. 1988, 4: 351-355.PubMed Zaim M, Ladonni H, Ershadi MRY, Manouchehri AV, Sahabi Z, Nazari M, Shahmohammadi H: Field application of Romanomermis culicivorax (Mermithidae: Nematoda) to control anopheline larvae in southern Iran. J Am Mosq Control Assoc. 1988, 4: 351-355.PubMed
21.
go back to reference Undeen AH, Dame DA: Measurement of the effect of microsporidian pathogens on mosquito larval mortality under artificial field conditions. J Am Mosq Control Assoc. 1987, 3: 91-93.PubMed Undeen AH, Dame DA: Measurement of the effect of microsporidian pathogens on mosquito larval mortality under artificial field conditions. J Am Mosq Control Assoc. 1987, 3: 91-93.PubMed
22.
go back to reference Hallmon CF, Schreiber ET, Vo T, Bloomquist MA: Field trials of three concentrations of Laginex TM as a biological larvicide compared to VectobacTM-12AS as a biocontrol agent for Culex quinquefasciatus. J Am Mosq Control Assoc. 2000, 16: 5-8.PubMed Hallmon CF, Schreiber ET, Vo T, Bloomquist MA: Field trials of three concentrations of Laginex TM as a biological larvicide compared to VectobacTM-12AS as a biocontrol agent for Culex quinquefasciatus. J Am Mosq Control Assoc. 2000, 16: 5-8.PubMed
23.
go back to reference Khetan SK: Microbial Pest Control. Marcel Dekker, New York. 2001 Khetan SK: Microbial Pest Control. Marcel Dekker, New York. 2001
24.
go back to reference Shoulkamy MA, Lucarotti CJ: Pathology of Coelomomyces stegomyiae in larval Aedes aegypti. Mycologia. 1998, 90: 559-564.CrossRef Shoulkamy MA, Lucarotti CJ: Pathology of Coelomomyces stegomyiae in larval Aedes aegypti. Mycologia. 1998, 90: 559-564.CrossRef
25.
go back to reference Sweeney AW: Preliminary field tests of the fungus Culicinomyces against mosquito larvae in Australia. Mosq News. 1981, 41: 470-476. Sweeney AW: Preliminary field tests of the fungus Culicinomyces against mosquito larvae in Australia. Mosq News. 1981, 41: 470-476.
26.
go back to reference Clark TB, Kellen W, Fukuda T, Lindgren JE: Field and laboratory studies on the pathogenicity of the fungus Beauvaria bassiana to three genera of mosquitoes. J Invertebr Path. 1968, 11: 1-7.CrossRef Clark TB, Kellen W, Fukuda T, Lindgren JE: Field and laboratory studies on the pathogenicity of the fungus Beauvaria bassiana to three genera of mosquitoes. J Invertebr Path. 1968, 11: 1-7.CrossRef
27.
go back to reference Roberts DW: Coelomomyces, Entomophtora, Beauvaria, and Metarrhizium as parasites of mosquitoes. Misc Publ Entom Soc Am. 1970, 7: 140-155. Roberts DW: Coelomomyces, Entomophtora, Beauvaria, and Metarrhizium as parasites of mosquitoes. Misc Publ Entom Soc Am. 1970, 7: 140-155.
28.
go back to reference Low RE, Kennel EW: Pathogenicity of the fungus Entomophthora coronata in Culex pipiens quinquefasciatus and Aedes taeniorhynchus. Mosq News. 1972, 32: 614-620. Low RE, Kennel EW: Pathogenicity of the fungus Entomophthora coronata in Culex pipiens quinquefasciatus and Aedes taeniorhynchus. Mosq News. 1972, 32: 614-620.
29.
go back to reference Kramer JP: Entomophthora culicis (Zygomycetes, Entomophthorales) as a pathogen of adult Aedes aegypti (Diptera, Culicidae). Aquat Insects. 1982, 4: 73-79.CrossRef Kramer JP: Entomophthora culicis (Zygomycetes, Entomophthorales) as a pathogen of adult Aedes aegypti (Diptera, Culicidae). Aquat Insects. 1982, 4: 73-79.CrossRef
30.
go back to reference Eilenberg J, Damgaard PH, Hansen BM, Pedersen JC, Bresciani J, Larsson R: Natural coprevalence of Strongwellsea castrans, Cystosporogenes deliaradicae, and Bacillus thuringiensis in the host, Delia radicum. J Invertebr Pathol. 2000, 75: 69-75. 10.1006/jipa.1999.4892.CrossRefPubMed Eilenberg J, Damgaard PH, Hansen BM, Pedersen JC, Bresciani J, Larsson R: Natural coprevalence of Strongwellsea castrans, Cystosporogenes deliaradicae, and Bacillus thuringiensis in the host, Delia radicum. J Invertebr Pathol. 2000, 75: 69-75. 10.1006/jipa.1999.4892.CrossRefPubMed
31.
go back to reference Soarés GG: Pathogenesis of infection by the hyphomycetous fungus Tolyplcladium cylindrosporum in Aedes sierrensis and Culex tarsalis (Dipt.: Culicidae). Entomophaga. 1982, 27: 283-300.CrossRef Soarés GG: Pathogenesis of infection by the hyphomycetous fungus Tolyplcladium cylindrosporum in Aedes sierrensis and Culex tarsalis (Dipt.: Culicidae). Entomophaga. 1982, 27: 283-300.CrossRef
32.
go back to reference Scholte E-J, Takken W, Knols BGJ: Pathogenicity of six East African entomopathogenic fungi to adult Anopheles gambiae s.s. (Diptera: Culicidae) mosquitoes. Proc Exp Appl Entomol NEV, Amsterdam. 2003, 14: 25-29. Scholte E-J, Takken W, Knols BGJ: Pathogenicity of six East African entomopathogenic fungi to adult Anopheles gambiae s.s. (Diptera: Culicidae) mosquitoes. Proc Exp Appl Entomol NEV, Amsterdam. 2003, 14: 25-29.
33.
go back to reference Veen KH: Recherches sur la maladie, due a Metharhizium anisopliae chez le criquet pèlerin. PhD-thesis, Landbouwhogeschool Wageningen 68–5. 1968 Veen KH: Recherches sur la maladie, due a Metharhizium anisopliae chez le criquet pèlerin. PhD-thesis, Landbouwhogeschool Wageningen 68–5. 1968
34.
go back to reference Zimmermann G: The entomopathogenic fungus Metahizium anisopliae and its potential as a biocontrol agent. Pestic Sci. 1993, 37: 375-379.CrossRef Zimmermann G: The entomopathogenic fungus Metahizium anisopliae and its potential as a biocontrol agent. Pestic Sci. 1993, 37: 375-379.CrossRef
35.
go back to reference Boucias DR, Pendland JC: Entomopathogenic fungi; Fungi Imperfecti. In: Principles of Insect Pathology. Edited by: Boucias DR, Pendland JC. 1998, Kluwer Academic Publishers, 10:CrossRef Boucias DR, Pendland JC: Entomopathogenic fungi; Fungi Imperfecti. In: Principles of Insect Pathology. Edited by: Boucias DR, Pendland JC. 1998, Kluwer Academic Publishers, 10:CrossRef
36.
go back to reference Roberts DW: Some effects of Metarhizium anisopliae and its toxins on mosquito larvae. In: Insect Pathology & Microbial Control. Edited by: Van der Laan. 1967, Amsterdam, the Netherlands: North-Holland Publishing Company, 243-246. Roberts DW: Some effects of Metarhizium anisopliae and its toxins on mosquito larvae. In: Insect Pathology & Microbial Control. Edited by: Van der Laan. 1967, Amsterdam, the Netherlands: North-Holland Publishing Company, 243-246.
37.
go back to reference Roberts DW: Fungal infections of mosquitoes. In: Le contrôle des moustiques/Mosquito control. Edited by: Aubin A, Belloncik S, Bourassa JP, LaCoursière E, Péllissier M. 1974, La Presse de l'Université du Quebec, Canada, 143-193. Roberts DW: Fungal infections of mosquitoes. In: Le contrôle des moustiques/Mosquito control. Edited by: Aubin A, Belloncik S, Bourassa JP, LaCoursière E, Péllissier M. 1974, La Presse de l'Université du Quebec, Canada, 143-193.
38.
go back to reference Ramoska WA: An examination of the long-term epizootic potential of various artificially introduced mosquito larval pathogens. Mosq News. 1982, 42: 603-607. Ramoska WA: An examination of the long-term epizootic potential of various artificially introduced mosquito larval pathogens. Mosq News. 1982, 42: 603-607.
39.
go back to reference Daoust RA, Roberts DW: Studies on the prolonged storage of Metarhizium anisopliae conidia: effect of temperature and relative humidity on conidial viability and virulence against mosquitoes. J Invertebr Path. 1983, 41: 143-150.CrossRef Daoust RA, Roberts DW: Studies on the prolonged storage of Metarhizium anisopliae conidia: effect of temperature and relative humidity on conidial viability and virulence against mosquitoes. J Invertebr Path. 1983, 41: 143-150.CrossRef
40.
go back to reference Ravallec M, Riba G, Vey A: Sensibilité d' Aedes albopictus (Dipt.: Culicidae) à l'hyhomycète entomopathogène Metarhizium anisopliae. Entomophaga. 1989, 34: 209-217.CrossRef Ravallec M, Riba G, Vey A: Sensibilité d' Aedes albopictus (Dipt.: Culicidae) à l'hyhomycète entomopathogène Metarhizium anisopliae. Entomophaga. 1989, 34: 209-217.CrossRef
41.
go back to reference Kaaya GP: Glossina morsitans morsitans : mortalities caused in adults by experimental infection with entomopathogenic fungi. Acta Trop. 1989, 46: 107-114. 10.1016/0001-706X(89)90004-1.CrossRefPubMed Kaaya GP: Glossina morsitans morsitans : mortalities caused in adults by experimental infection with entomopathogenic fungi. Acta Trop. 1989, 46: 107-114. 10.1016/0001-706X(89)90004-1.CrossRefPubMed
42.
go back to reference Kaaya GP, Munyinyi DM: Biocontrol potential of the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae for tsetse flies (Glossina spp.) at developmental sites. J Invertebr Pathol. 1995, 66: 237-241. 10.1006/jipa.1995.1095.CrossRefPubMed Kaaya GP, Munyinyi DM: Biocontrol potential of the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae for tsetse flies (Glossina spp.) at developmental sites. J Invertebr Pathol. 1995, 66: 237-241. 10.1006/jipa.1995.1095.CrossRefPubMed
43.
go back to reference Maniania NK: A device for infecting adult tsetse flies, Glossina spp., with an entomopathogenic fungus in the field. Biol Control. 1998, 11: 248-254. 10.1006/bcon.1997.0580.CrossRef Maniania NK: A device for infecting adult tsetse flies, Glossina spp., with an entomopathogenic fungus in the field. Biol Control. 1998, 11: 248-254. 10.1006/bcon.1997.0580.CrossRef
44.
go back to reference Mathenge EM, Killeen GF, Oulo DO, Irungu LW, Ndegwa PN, Knols BGJ: Development of an exposure-free bednet trap for sampling Afrotropical malaria vectors. Med Vet Entomol. 2002, 16: 67-74. 10.1046/j.0269-283x.2002.00350.x.CrossRefPubMed Mathenge EM, Killeen GF, Oulo DO, Irungu LW, Ndegwa PN, Knols BGJ: Development of an exposure-free bednet trap for sampling Afrotropical malaria vectors. Med Vet Entomol. 2002, 16: 67-74. 10.1046/j.0269-283x.2002.00350.x.CrossRefPubMed
45.
go back to reference Knols BGJ, Njiru BN, Mathenge EM, Mukabana WR, Beier JC, Killeen GF: MalariaSphere: A greenhouse-enclosed simulation of a natural Anopheles gambiae (Diptera: Culicidae) ecosystem in western Kenya. Malaria J. 2002, 1: 19-10.1186/1475-2875-1-19.CrossRef Knols BGJ, Njiru BN, Mathenge EM, Mukabana WR, Beier JC, Killeen GF: MalariaSphere: A greenhouse-enclosed simulation of a natural Anopheles gambiae (Diptera: Culicidae) ecosystem in western Kenya. Malaria J. 2002, 1: 19-10.1186/1475-2875-1-19.CrossRef
46.
go back to reference Mukabana WR, Takken W, Seda P, Killeen GF, Hawley WA, Knols BGJ: Extent of digestion affects the success of amplifying human DNA from blood meals of Anopheles gambiae (Diptera: Culicidae). Bull Ent Res. 2002, 92: 233-239. 10.1079/BER2002164.CrossRef Mukabana WR, Takken W, Seda P, Killeen GF, Hawley WA, Knols BGJ: Extent of digestion affects the success of amplifying human DNA from blood meals of Anopheles gambiae (Diptera: Culicidae). Bull Ent Res. 2002, 92: 233-239. 10.1079/BER2002164.CrossRef
47.
go back to reference Everitt BS: Statistical methods for medical investigations. New York: Halsted Press. 1994 Everitt BS: Statistical methods for medical investigations. New York: Halsted Press. 1994
48.
go back to reference Gompertz B: On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life continguencies. Phil Trans R Soc. 1825, 513-585. Gompertz B: On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life continguencies. Phil Trans R Soc. 1825, 513-585.
49.
go back to reference Clements AN, Paterson GD: The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecol. 1981, 18: 373-399.CrossRef Clements AN, Paterson GD: The analysis of mortality and survival rates in wild populations of mosquitoes. J Appl Ecol. 1981, 18: 373-399.CrossRef
50.
go back to reference Miller DR, Weidhaas DE, Hall RC: Parameter sensitivity in insect population modeling. J Theor Biol. 1973, 42: 263-274.CrossRefPubMed Miller DR, Weidhaas DE, Hall RC: Parameter sensitivity in insect population modeling. J Theor Biol. 1973, 42: 263-274.CrossRefPubMed
51.
go back to reference Macdonald G: The epidemiology and control of malaria. London: Oxford University Press. 1957 Macdonald G: The epidemiology and control of malaria. London: Oxford University Press. 1957
52.
go back to reference Garrett-Jones C: Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity. Nature. 1964, 204: 1173-1175.CrossRefPubMed Garrett-Jones C: Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity. Nature. 1964, 204: 1173-1175.CrossRefPubMed
53.
go back to reference Takken W, Charlwood JD, Billingsley PF, Gort G: Dispersal and survival of Anopheles funestus and A. gambiae s.l. (Diptera: Culicidae) during the rainy season in southeast Tanzania. Bull EntRes. 1998, 88: 561-566.CrossRef Takken W, Charlwood JD, Billingsley PF, Gort G: Dispersal and survival of Anopheles funestus and A. gambiae s.l. (Diptera: Culicidae) during the rainy season in southeast Tanzania. Bull EntRes. 1998, 88: 561-566.CrossRef
54.
go back to reference Gillies MT: Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means and release experiments. Bull Ent Res. 1961, 52: 99-127.CrossRef Gillies MT: Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means and release experiments. Bull Ent Res. 1961, 52: 99-127.CrossRef
55.
go back to reference Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC: A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg. 2000, 62: 535-544.PubMedCentralPubMed Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC: A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg. 2000, 62: 535-544.PubMedCentralPubMed
56.
go back to reference Kasule FK: A comparison of the life history components of Aedes aegypti (L.) and Culex quinquefasciatus Say (Diptera: Culicidae). Insect Sc Applic. 1986, 7: 143-147. Kasule FK: A comparison of the life history components of Aedes aegypti (L.) and Culex quinquefasciatus Say (Diptera: Culicidae). Insect Sc Applic. 1986, 7: 143-147.
57.
go back to reference Oda T, Eshita Y, Uchida K, Mine M, Kurokawa K, Ogawa Y, Kato K, Tahara H: Reproductive activity and survival of Culex pipiens pallens and Culex quinquefasciatus (Diptera: Culicidae) in Japan at high temperature. J Med Entomol. 2002, 39: 185-190.CrossRefPubMed Oda T, Eshita Y, Uchida K, Mine M, Kurokawa K, Ogawa Y, Kato K, Tahara H: Reproductive activity and survival of Culex pipiens pallens and Culex quinquefasciatus (Diptera: Culicidae) in Japan at high temperature. J Med Entomol. 2002, 39: 185-190.CrossRefPubMed
58.
go back to reference Pathak JPN: Insect Immunity. Dordrecht: Kluwer Academic Publishers. 1993 Pathak JPN: Insect Immunity. Dordrecht: Kluwer Academic Publishers. 1993
59.
go back to reference Schwartz A, Koella JC: Melanization of Plasmodium falciparum and C-25 sephadex beads by field-caught Anopheles gambiae (Diptera: Culicidae) from southern Tanzania. J Med Entomol. 2002, 39: 84-88.CrossRefPubMed Schwartz A, Koella JC: Melanization of Plasmodium falciparum and C-25 sephadex beads by field-caught Anopheles gambiae (Diptera: Culicidae) from southern Tanzania. J Med Entomol. 2002, 39: 84-88.CrossRefPubMed
60.
go back to reference Hurd H: Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol. 2003, 48: 141-161. 10.1146/annurev.ento.48.091801.112722.CrossRefPubMed Hurd H: Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol. 2003, 48: 141-161. 10.1146/annurev.ento.48.091801.112722.CrossRefPubMed
61.
go back to reference Lucarotti CJ: Invasion of Aedes aegypti ovaries by Coelomomyces stegomyiae. J Invertebr Pathol. 1992, 60: 176-184.CrossRef Lucarotti CJ: Invasion of Aedes aegypti ovaries by Coelomomyces stegomyiae. J Invertebr Pathol. 1992, 60: 176-184.CrossRef
62.
go back to reference Debenham ML, Russell RC: The insect pathogenic fungus Culicinomyces in adults of the mosquito Anopheles amictus hilli. J Austr Entomol Soc. 1977, 16: 46-CrossRef Debenham ML, Russell RC: The insect pathogenic fungus Culicinomyces in adults of the mosquito Anopheles amictus hilli. J Austr Entomol Soc. 1977, 16: 46-CrossRef
63.
go back to reference Kramer JP: Pathogenicity of the fungus Entomophthora culicis for adult mosquitoes: Anopheles stephensi and Culex pipiens quinquefasciatus. J NY Entomol Soc. 1983, 91: 177-182. Kramer JP: Pathogenicity of the fungus Entomophthora culicis for adult mosquitoes: Anopheles stephensi and Culex pipiens quinquefasciatus. J NY Entomol Soc. 1983, 91: 177-182.
Metadata
Title
Infection of malaria (Anopheles gambiae s.s.) and filariasis (Culex quinquefasciatus) vectors with the entomopathogenic fungus Metarhizium anisopliae
Authors
Ernst-Jan Scholte
Basilio N Njiru
Renate C Smallegange
Willem Takken
Bart GJ Knols
Publication date
01-12-2003
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2003
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-2-29

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