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Published in: Malaria Journal 1/2009

Open Access 01-12-2009 | Research

Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa

Authors: Kevin Y Njabo, Anthony J Cornel, Ravinder NM Sehgal, Claire Loiseau, Wolfgang Buermann, Ryan J Harrigan, John Pollinger, Gediminas Valkiūnas, Thomas B Smith

Published in: Malaria Journal | Issue 1/2009

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Abstract

Background

The mosquito vectors of Plasmodium spp. have largely been overlooked in studies of ecology and evolution of avian malaria and other vertebrates in wildlife.

Methods

Plasmodium DNA from wild-caught Coquillettidia spp. collected from lowland forests in Cameroon was isolated and sequenced using nested PCR. Female Coquillettidia aurites were also dissected and salivary glands were isolated and microscopically examined for the presence of sporozoites.

Results

In total, 33% (85/256) of mosquito pools tested positive for avian Plasmodium spp., harbouring at least eight distinct parasite lineages. Sporozoites of Plasmodium spp. were recorded in salivary glands of C. aurites supporting the PCR data that the parasites complete development in these mosquitoes. Results suggest C. aurites, Coquillettidia pseudoconopas and Coquillettidia metallica as new and important vectors of avian malaria in Africa. All parasite lineages recovered clustered with parasites formerly identified from several bird species and suggest the vectors capability of infecting birds from different families.

Conclusion

Identifying the major vectors of avian Plasmodium spp. will assist in understanding the epizootiology of avian malaria, including differences in this disease distribution between pristine and disturbed landscapes.
Appendix
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Literature
1.
go back to reference Bennett GF, Peirce MA, Earl RA: Anannotated checklist of the valid avian species of Haemoproteus, Leucocytozoon (Apicomplexa, Haemosporida) and Hepatozoon (Apicomplexa, Haemogregarinidae). Syst Parasitol. 1994, 29: 61-73.CrossRef Bennett GF, Peirce MA, Earl RA: Anannotated checklist of the valid avian species of Haemoproteus, Leucocytozoon (Apicomplexa, Haemosporida) and Hepatozoon (Apicomplexa, Haemogregarinidae). Syst Parasitol. 1994, 29: 61-73.CrossRef
2.
go back to reference Valkiūnas G: Avian Malarial Parasites and Other Haemosporidia. 2005, Taylor and Francis Publishing, London Valkiūnas G: Avian Malarial Parasites and Other Haemosporidia. 2005, Taylor and Francis Publishing, London
3.
go back to reference Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC: Global phylogeographic limits of Hawaii's avian malaria. Proc R Soc Lond B Biol Sci. 2006, 273: 2935-2944. 10.1098/rspb.2006.3671.CrossRef Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC: Global phylogeographic limits of Hawaii's avian malaria. Proc R Soc Lond B Biol Sci. 2006, 273: 2935-2944. 10.1098/rspb.2006.3671.CrossRef
4.
go back to reference Valkiūnas G, Iezhova TA, Loiseau C, Chasar A, Smith TB, Sehgal RNM: New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitol Res. 2008, 103: 1213-1228. 10.1007/s00436-008-1118-x.CrossRefPubMed Valkiūnas G, Iezhova TA, Loiseau C, Chasar A, Smith TB, Sehgal RNM: New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitol Res. 2008, 103: 1213-1228. 10.1007/s00436-008-1118-x.CrossRefPubMed
5.
go back to reference Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O: Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation?. Evolution. 2004, 58: 1617-1621.CrossRefPubMed Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O: Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation?. Evolution. 2004, 58: 1617-1621.CrossRefPubMed
6.
go back to reference Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S: Plasmodium relictum (lineage P-SGS1): Effects on experimentally infected passerine birds. Exp Parasitol. 2008, 120: 372-380. 10.1016/j.exppara.2008.09.001.CrossRefPubMed Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S: Plasmodium relictum (lineage P-SGS1): Effects on experimentally infected passerine birds. Exp Parasitol. 2008, 120: 372-380. 10.1016/j.exppara.2008.09.001.CrossRefPubMed
7.
go back to reference Van Riper C, Van Riper SG, Goff ML, Laird M: The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr. 1986, 56: 327-344. 10.2307/1942550.CrossRef Van Riper C, Van Riper SG, Goff ML, Laird M: The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr. 1986, 56: 327-344. 10.2307/1942550.CrossRef
8.
go back to reference Richner H, Christe P, Oppliger A: Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA. 1995, 92: 1192-1194. 10.1073/pnas.92.4.1192.PubMedCentralCrossRefPubMed Richner H, Christe P, Oppliger A: Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA. 1995, 92: 1192-1194. 10.1073/pnas.92.4.1192.PubMedCentralCrossRefPubMed
9.
go back to reference Beier JC, Perkins PV, Wirtz RA: Blood meal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988, 25: 9-16.CrossRefPubMed Beier JC, Perkins PV, Wirtz RA: Blood meal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol. 1988, 25: 9-16.CrossRefPubMed
10.
go back to reference McConkey GA, Li J, Rogers MJ, Seeley DC, Graczyk TK, Cranfield MR, McCutchan TF: Surveillance of mosquitoes for the malaria parasite responsible for mortality in captive penguins. J Eucar Microbiol. 1996, 43: 393-399. 10.1111/j.1550-7408.1996.tb05049.x. McConkey GA, Li J, Rogers MJ, Seeley DC, Graczyk TK, Cranfield MR, McCutchan TF: Surveillance of mosquitoes for the malaria parasite responsible for mortality in captive penguins. J Eucar Microbiol. 1996, 43: 393-399. 10.1111/j.1550-7408.1996.tb05049.x.
11.
go back to reference Atkinson CT, Dusek RJ, Lease JK: Serological responses and immunity to superinfection with avian malaria in experimentally infected Hawaii Amakihi. J Wildl Dis. 2001, 37: 20-27.CrossRefPubMed Atkinson CT, Dusek RJ, Lease JK: Serological responses and immunity to superinfection with avian malaria in experimentally infected Hawaii Amakihi. J Wildl Dis. 2001, 37: 20-27.CrossRefPubMed
12.
go back to reference Atkinson CT, Van Riper C: Pathogenecity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Bird-parasite interactions. Ecology, evolution, and behavior. Edited by: Loye JE, Zuk M. 1991, Oxford Univ. Press, New York, 19-48. Atkinson CT, Van Riper C: Pathogenecity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Bird-parasite interactions. Ecology, evolution, and behavior. Edited by: Loye JE, Zuk M. 1991, Oxford Univ. Press, New York, 19-48.
13.
go back to reference Bequaert JC: The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part II. Taxonomy, evolution and revision of American genera and species. Entomol Am. 1954, 34: 1-232. Bequaert JC: The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part II. Taxonomy, evolution and revision of American genera and species. Entomol Am. 1954, 34: 1-232.
14.
go back to reference Forrester DJ, Nayar JK, Foster GW: Culex nigripalpus: A natural vector of wild turkey malaria (Plasmodium hermani) in Florida. J Wildl Dis. 1980, 16: 391-394.CrossRefPubMed Forrester DJ, Nayar JK, Foster GW: Culex nigripalpus: A natural vector of wild turkey malaria (Plasmodium hermani) in Florida. J Wildl Dis. 1980, 16: 391-394.CrossRefPubMed
15.
go back to reference Gabaldon AU, Ulloa G, Pulido J: Distribucion geografica, ecologia y etologia de Aedeomyia squamipennis, importante vector natural de malaria aviaria en Venezuela. Bol Dir Malar S Ambien. 1981, 21: 103-113. Gabaldon AU, Ulloa G, Pulido J: Distribucion geografica, ecologia y etologia de Aedeomyia squamipennis, importante vector natural de malaria aviaria en Venezuela. Bol Dir Malar S Ambien. 1981, 21: 103-113.
16.
go back to reference Niles WJ, Fernando MA, Dissanaike AS: Mansonia crassipes as the natural vector of filarioids, Plasmodium gallinaceum and other plasmodia of fowls in Ceylon. Nature. 1965, 205: 411-412. 10.1038/205411a0.CrossRefPubMed Niles WJ, Fernando MA, Dissanaike AS: Mansonia crassipes as the natural vector of filarioids, Plasmodium gallinaceum and other plasmodia of fowls in Ceylon. Nature. 1965, 205: 411-412. 10.1038/205411a0.CrossRefPubMed
17.
go back to reference Telford SR, Nayar JK, Foster GW, Knight JW: Plasmodium forresteri n.sp., from raptors in Florida and southern Georgia: Its distinction from Plasmodium elongatum morphologically within and among host species and by vector susceptibility. J Parasitol. 1997, 83: 932-937. 10.2307/3284292.CrossRefPubMed Telford SR, Nayar JK, Foster GW, Knight JW: Plasmodium forresteri n.sp., from raptors in Florida and southern Georgia: Its distinction from Plasmodium elongatum morphologically within and among host species and by vector susceptibility. J Parasitol. 1997, 83: 932-937. 10.2307/3284292.CrossRefPubMed
18.
go back to reference Ishtiaq F, Guillaumot L, Clegg SM, Phillimore AB, Black RA, Owens IPF, Mundy NI, Sheldon BC: Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol. 2008, 17: 4545-4555. 10.1111/j.1365-294X.2008.03935.x.CrossRefPubMed Ishtiaq F, Guillaumot L, Clegg SM, Phillimore AB, Black RA, Owens IPF, Mundy NI, Sheldon BC: Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol. 2008, 17: 4545-4555. 10.1111/j.1365-294X.2008.03935.x.CrossRefPubMed
19.
go back to reference Ronderos RA, Bachman A: A proposito de1 complejo Mansonia (Diptera-Culicidae). Rev. Sot, Ent, Argentina. 1963, 25: 45-51. Ronderos RA, Bachman A: A proposito de1 complejo Mansonia (Diptera-Culicidae). Rev. Sot, Ent, Argentina. 1963, 25: 45-51.
20.
go back to reference Knight KL, Stone A: A catalog of the Mosquitoes of the World (Diptera, Culicidae). Thomas Say Foundation. 1977, 6: 1-610. Second Knight KL, Stone A: A catalog of the Mosquitoes of the World (Diptera, Culicidae). Thomas Say Foundation. 1977, 6: 1-610. Second
22.
go back to reference Stone A, Knight KL, Starcke H: A synoptic catalogue of the mosquitoes of the world. Thomas Say Found. 1959, 6: 358- Stone A, Knight KL, Starcke H: A synoptic catalogue of the mosquitoes of the world. Thomas Say Found. 1959, 6: 358-
23.
go back to reference Matingly TF: Contributions of the American Entomological Institute: contributions to the mosquito fauna of Southeast Asia. XII. Illustrated keys to the genera of mosquitoes (Diptera, Culicidae). Contrib Am Entomol Inst (Ann Arbor). 1971, 7: 41-84. Matingly TF: Contributions of the American Entomological Institute: contributions to the mosquito fauna of Southeast Asia. XII. Illustrated keys to the genera of mosquitoes (Diptera, Culicidae). Contrib Am Entomol Inst (Ann Arbor). 1971, 7: 41-84.
24.
go back to reference White GB: Studies on the transmission of Bancroftian filariasis in north-eastern Tanzania. Trans R Soc Trop Med Hyg. 1971, 65: 819-829. 10.1016/0035-9203(71)90098-8.CrossRefPubMed White GB: Studies on the transmission of Bancroftian filariasis in north-eastern Tanzania. Trans R Soc Trop Med Hyg. 1971, 65: 819-829. 10.1016/0035-9203(71)90098-8.CrossRefPubMed
25.
go back to reference Service MW: Handbook to the Afrotropical toxorhynchitine and culicine mosquitoes, excepting Aedes and Culex. 1990, British Museum (Natural History) London Service MW: Handbook to the Afrotropical toxorhynchitine and culicine mosquitoes, excepting Aedes and Culex. 1990, British Museum (Natural History) London
26.
go back to reference Belkin JN: The mosquitoes of the South Pacific (Diptera, Culicidae). 1962, University of California Press, Berkeley and Los Angeles, 2: 608 and 412 pp Belkin JN: The mosquitoes of the South Pacific (Diptera, Culicidae). 1962, University of California Press, Berkeley and Los Angeles, 2: 608 and 412 pp
27.
go back to reference Edwards FW: Mosquitoes of the Ethiopian Region. III. Culicine Adults and Pupae. Brit Mus (Nat Hist), London. 1941, 499- Edwards FW: Mosquitoes of the Ethiopian Region. III. Culicine Adults and Pupae. Brit Mus (Nat Hist), London. 1941, 499-
28.
go back to reference Bisby FA, Roskov YR, Ruggiero MA, Orrell TM, Paglinawan LE, Brewer PW, Bailly N, van Hertum J: Species 2000 & ITIS Catalogue of Life: 2007 Annual Checklist Species 2000. Reading, U.K. 2007 Bisby FA, Roskov YR, Ruggiero MA, Orrell TM, Paglinawan LE, Brewer PW, Bailly N, van Hertum J: Species 2000 & ITIS Catalogue of Life: 2007 Annual Checklist Species 2000. Reading, U.K. 2007
29.
go back to reference Haddow AJ: Twenty-four-hour catches on a tower with man as bait, East African Virus Research Institute Report, July, 1962–June 1963. 63pp Nairobi. 1964, 42-46. Haddow AJ: Twenty-four-hour catches on a tower with man as bait, East African Virus Research Institute Report, July, 1962–June 1963. 63pp Nairobi. 1964, 42-46.
30.
go back to reference Haddow AJ, Ssenkubuge Y: Entomological studies from a steel tower in Zika forest, Uganda. Part 1. The biting activity of mosquitoes and tabanids as shown by twenty-four-hour catches. Trans R Entomol Soc Lond. 1965, 117: 215-243.CrossRef Haddow AJ, Ssenkubuge Y: Entomological studies from a steel tower in Zika forest, Uganda. Part 1. The biting activity of mosquitoes and tabanids as shown by twenty-four-hour catches. Trans R Entomol Soc Lond. 1965, 117: 215-243.CrossRef
31.
go back to reference Boorman JPT: Annual Report of the West African Council for Medical Research, Lagos. 1957 Boorman JPT: Annual Report of the West African Council for Medical Research, Lagos. 1957
32.
go back to reference Williams MC, Simpson DIH, Haddow AJ, Knight EM: The isolation of West Nile virus from man and Usutu virus from bird-biting mosquito Mansonia aurites (Theobald) in the Entebbe area of Uganda. Ann Trop Med Parasitol. 1964, 58: 367-374.PubMed Williams MC, Simpson DIH, Haddow AJ, Knight EM: The isolation of West Nile virus from man and Usutu virus from bird-biting mosquito Mansonia aurites (Theobald) in the Entebbe area of Uganda. Ann Trop Med Parasitol. 1964, 58: 367-374.PubMed
33.
go back to reference McClelland GAH, Weitz B: Further observations on the natural hosts of three species of Mansonia Blanchard (Diptera, Culicidae) in Uganda. Ann Trop Med Parasitol. 1960, 54: 300-304.PubMed McClelland GAH, Weitz B: Further observations on the natural hosts of three species of Mansonia Blanchard (Diptera, Culicidae) in Uganda. Ann Trop Med Parasitol. 1960, 54: 300-304.PubMed
34.
go back to reference Rickenbach A, Le Gonidec G, Ravisse P: L'incidence des arbovirus isolés des moustiques dans une région forestière du sud Cameroun, la region de Yaoundé. Bull Soc de Pathol Exot. 1976, 69: 372-381. Rickenbach A, Le Gonidec G, Ravisse P: L'incidence des arbovirus isolés des moustiques dans une région forestière du sud Cameroun, la region de Yaoundé. Bull Soc de Pathol Exot. 1976, 69: 372-381.
35.
go back to reference Sehgal RNM, Jones HI, Smith TB: Blood parasites of some West African rainforest birds. J Vet Med Sci. 2005, 67: 295-301. 10.1292/jvms.67.295.CrossRefPubMed Sehgal RNM, Jones HI, Smith TB: Blood parasites of some West African rainforest birds. J Vet Med Sci. 2005, 67: 295-301. 10.1292/jvms.67.295.CrossRefPubMed
36.
go back to reference Bonnead C, Sepil I, Mila B, Buermann W, Pollinger J, Sehgal RNM, Valkiūnas G, Iezhova TA, Saatchi S, Smith TB: The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. J Trop Ecol. 2009, 25: 1-9. 10.1017/S0266467408005646.CrossRef Bonnead C, Sepil I, Mila B, Buermann W, Pollinger J, Sehgal RNM, Valkiūnas G, Iezhova TA, Saatchi S, Smith TB: The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. J Trop Ecol. 2009, 25: 1-9. 10.1017/S0266467408005646.CrossRef
37.
go back to reference Valkiūnas G, Iezhova TA, Loiseau C, Smith TB, Sehgal RN: New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitol Res. 2009, 104: 1061-77. 10.1007/s00436-008-1289-5.CrossRefPubMed Valkiūnas G, Iezhova TA, Loiseau C, Smith TB, Sehgal RN: New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitol Res. 2009, 104: 1061-77. 10.1007/s00436-008-1289-5.CrossRefPubMed
38.
go back to reference Hijmans RJ, Susan A, Cameron E, Juan AB, Parra I, Peter A, Jones G, Jarvis CD: Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005, 25: 1965-1978. 10.1002/joc.1276.CrossRef Hijmans RJ, Susan A, Cameron E, Juan AB, Parra I, Peter A, Jones G, Jarvis CD: Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005, 25: 1965-1978. 10.1002/joc.1276.CrossRef
39.
go back to reference Smith TB: Resource use by bill morphs of an African Finch: Evidence for Intraspecific Competition. Ecology. 1990, 71: 1246-1257. 10.2307/1938261.CrossRef Smith TB: Resource use by bill morphs of an African Finch: Evidence for Intraspecific Competition. Ecology. 1990, 71: 1246-1257. 10.2307/1938261.CrossRef
40.
go back to reference Sudia WD, Chamberlain RW: Battery operated light trap, an improved model. Mosq News. 1962, 22: 126-129. Sudia WD, Chamberlain RW: Battery operated light trap, an improved model. Mosq News. 1962, 22: 126-129.
41.
go back to reference Jupp PG, McIntosh BM: Ecological studies on Sindbis and West Nile viruses in South Africa. II. Mosquito bionomics. S Afr J Med Sci. 1967, 32: 15-33.PubMed Jupp PG, McIntosh BM: Ecological studies on Sindbis and West Nile viruses in South Africa. II. Mosquito bionomics. S Afr J Med Sci. 1967, 32: 15-33.PubMed
42.
go back to reference Downing JD, Crans WJ: The Ehrenburg pigeon trap as a sampler of Culex mosquitoes for St. Louis encephalitis surveillance. Mosq News. 1977, 37: 48-53. Downing JD, Crans WJ: The Ehrenburg pigeon trap as a sampler of Culex mosquitoes for St. Louis encephalitis surveillance. Mosq News. 1977, 37: 48-53.
43.
go back to reference Biggerstaff BJ: PooledInf Rate: a Microsoft Excel Add-In to compute prevalence estimates from pooled samples. 2006, Fort Collins (CO): Centers for Disease Control and Prevention Biggerstaff BJ: PooledInf Rate: a Microsoft Excel Add-In to compute prevalence estimates from pooled samples. 2006, Fort Collins (CO): Centers for Disease Control and Prevention
44.
go back to reference Pilchart C, Sechan Y, Davies N, Legrand A: PCR and dissection as tools to monitor filarial infection of Aedes polynesiensis mosquitoes in French Polynesia. Filaria J. 2006, 5: 1475-2883. Pilchart C, Sechan Y, Davies N, Legrand A: PCR and dissection as tools to monitor filarial infection of Aedes polynesiensis mosquitoes in French Polynesia. Filaria J. 2006, 5: 1475-2883.
45.
go back to reference Cooper A: DNA from museum specimens. Ancient DNA, Recovery and Analysis of Genetic Material from Paleontological, Archaeological, Museum, Medical and Forensic Specimens. Edited by: Herrmann B, Herrmann S. 1994, Springer, New York, 149-165. Cooper A: DNA from museum specimens. Ancient DNA, Recovery and Analysis of Genetic Material from Paleontological, Archaeological, Museum, Medical and Forensic Specimens. Edited by: Herrmann B, Herrmann S. 1994, Springer, New York, 149-165.
46.
go back to reference Kreader CA: Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol. 1996, 1102-1106. Kreader CA: Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol. 1996, 1102-1106.
47.
go back to reference Waldenström J, Bensch S, Hasselquist D, Ostman O: A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004, 90: 191-194. 10.1645/GE-3221RN.CrossRefPubMed Waldenström J, Bensch S, Hasselquist D, Ostman O: A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004, 90: 191-194. 10.1645/GE-3221RN.CrossRefPubMed
48.
go back to reference Cywinska A, Hunter FF, Hebert PDN: Identifying Canadian mosquito species through DNA barcodes. Med Vet Entomol. 2006, 20: 413-424. 10.1111/j.1365-2915.2006.00653.x.CrossRefPubMed Cywinska A, Hunter FF, Hebert PDN: Identifying Canadian mosquito species through DNA barcodes. Med Vet Entomol. 2006, 20: 413-424. 10.1111/j.1365-2915.2006.00653.x.CrossRefPubMed
49.
go back to reference Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Bio Biotechnol. 1994, 3: 294-299. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Bio Biotechnol. 1994, 3: 294-299.
50.
go back to reference Swofford DL: PAUP*: Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4. 2002, Sinauer Associates, Sunderland, Massachusetts Swofford DL: PAUP*: Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4. 2002, Sinauer Associates, Sunderland, Massachusetts
51.
go back to reference Christensen BM, Barnes HJ, Rowley WA: Vertebrate host specificity and experimental vectors of Plasmodium (Novyella) kempi sp. n. from the eastern wild turkey in Iowa. J Wildl Dis. 1983, 19: 204-213.CrossRefPubMed Christensen BM, Barnes HJ, Rowley WA: Vertebrate host specificity and experimental vectors of Plasmodium (Novyella) kempi sp. n. from the eastern wild turkey in Iowa. J Wildl Dis. 1983, 19: 204-213.CrossRefPubMed
52.
go back to reference Beadell JS, Covas R, Gebhard C, Ishtiaq F, Melo M, Schmidt BK, Perkins SL, Graves GR, Fleischer RC: Host associations and evolutionary relationships of avian blood parasites from West Africa. Intl J Parasitol. 2009, 39: 257-266. 10.1016/j.ijpara.2008.06.005.CrossRef Beadell JS, Covas R, Gebhard C, Ishtiaq F, Melo M, Schmidt BK, Perkins SL, Graves GR, Fleischer RC: Host associations and evolutionary relationships of avian blood parasites from West Africa. Intl J Parasitol. 2009, 39: 257-266. 10.1016/j.ijpara.2008.06.005.CrossRef
53.
go back to reference Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001, 17: 754-755. 10.1093/bioinformatics/17.8.754.CrossRefPubMed Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001, 17: 754-755. 10.1093/bioinformatics/17.8.754.CrossRefPubMed
54.
go back to reference Bahl A, Brunk B, Crabtree J, Fraunholz JM, Gajria B, Grant GR, Ginsburg H, Gupta D, Kissinger JC, Labo P, Li L, Mailman MD, Milgram AJ, Pearson DS, Roos DS, Schug J, Stoeckert CJ, Whetzel P: PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Res. 2003, 31: 212-215. 10.1093/nar/gkg081.PubMedCentralCrossRefPubMed Bahl A, Brunk B, Crabtree J, Fraunholz JM, Gajria B, Grant GR, Ginsburg H, Gupta D, Kissinger JC, Labo P, Li L, Mailman MD, Milgram AJ, Pearson DS, Roos DS, Schug J, Stoeckert CJ, Whetzel P: PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Res. 2003, 31: 212-215. 10.1093/nar/gkg081.PubMedCentralCrossRefPubMed
55.
go back to reference Perkins SL, Schall JJ: A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. J Parasitol. 2002, 88: 972-978.CrossRefPubMed Perkins SL, Schall JJ: A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. J Parasitol. 2002, 88: 972-978.CrossRefPubMed
56.
go back to reference Garnham PCC: Malaria parasites and other Haemosporidia. 1966, Blackwell, Oxford, U.K, 114- Garnham PCC: Malaria parasites and other Haemosporidia. 1966, Blackwell, Oxford, U.K, 114-
58.
go back to reference Escalante AA, Freeland DE, Collins WE, Lal AA: The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Nat Acad Sci USA. 1998, 95: 8124-29. 10.1073/pnas.95.14.8124.PubMedCentralCrossRefPubMed Escalante AA, Freeland DE, Collins WE, Lal AA: The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Nat Acad Sci USA. 1998, 95: 8124-29. 10.1073/pnas.95.14.8124.PubMedCentralCrossRefPubMed
59.
go back to reference Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC: Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol. 2004, 13: 3829-2844. 10.1111/j.1365-294X.2004.02363.x.CrossRefPubMed Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC: Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol. 2004, 13: 3829-2844. 10.1111/j.1365-294X.2004.02363.x.CrossRefPubMed
60.
go back to reference Shute P, Maryon M: Laboratory technique for the study of malaria. 1966, London: J and A Churchill Ltd. C. P. A, 26-28. 2 Shute P, Maryon M: Laboratory technique for the study of malaria. 1966, London: J and A Churchill Ltd. C. P. A, 26-28. 2
61.
go back to reference Strome P, DeSantis L, Leef JL, Beaudoin RL: A convenient technique for the dissection of mosquito salivary glands. Methods Cell Sci. 1980, 6: 9-11. Strome P, DeSantis L, Leef JL, Beaudoin RL: A convenient technique for the dissection of mosquito salivary glands. Methods Cell Sci. 1980, 6: 9-11.
62.
go back to reference Sutcliffe JF: Black fly host location: a review. Can J Zool. 1986, 64: 1041-1053. 10.1139/z86-156.CrossRef Sutcliffe JF: Black fly host location: a review. Can J Zool. 1986, 64: 1041-1053. 10.1139/z86-156.CrossRef
63.
go back to reference DeJong R, Knols BGJ: Olfactory responses of host-seeking An gambiae s.s. Giles (Diptera: Culicidae). Acta Trop. 1995, 59: 333-335. 10.1016/0001-706X(95)00090-2.CrossRef DeJong R, Knols BGJ: Olfactory responses of host-seeking An gambiae s.s. Giles (Diptera: Culicidae). Acta Trop. 1995, 59: 333-335. 10.1016/0001-706X(95)00090-2.CrossRef
64.
go back to reference Oaks SC, Mitchell VS, Pearson GW, Carpenter CCJ: Malaria: Obstacles and Opportunities. 1991, A report of the Institute of Medicine. National Academy Press, Washington, DC Oaks SC, Mitchell VS, Pearson GW, Carpenter CCJ: Malaria: Obstacles and Opportunities. 1991, A report of the Institute of Medicine. National Academy Press, Washington, DC
65.
go back to reference Donnelly MJ, Simard F, Lehmann T: Evolutionary studies of malaria vectors. Trends Parasitol. 2002, 18: 75-80. 10.1016/S1471-4922(01)02198-5.CrossRefPubMed Donnelly MJ, Simard F, Lehmann T: Evolutionary studies of malaria vectors. Trends Parasitol. 2002, 18: 75-80. 10.1016/S1471-4922(01)02198-5.CrossRefPubMed
66.
go back to reference Krzywinski J, Besansky NJ: Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003, 48: 111-139. 10.1146/annurev.ento.48.091801.112647.CrossRefPubMed Krzywinski J, Besansky NJ: Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003, 48: 111-139. 10.1146/annurev.ento.48.091801.112647.CrossRefPubMed
67.
go back to reference Fontenille D, Simard F: Unraveling complexities in human malaria transmission dynamics in Africa through a comprehensive knowledge of vector populations. Comp Immunol Microbial. 2004, 27: 357-375. 10.1016/j.cimid.2004.03.005.CrossRef Fontenille D, Simard F: Unraveling complexities in human malaria transmission dynamics in Africa through a comprehensive knowledge of vector populations. Comp Immunol Microbial. 2004, 27: 357-375. 10.1016/j.cimid.2004.03.005.CrossRef
68.
go back to reference Harbach RE: The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res. 2004, 94: 537-553. 10.1079/BER2004321.CrossRefPubMed Harbach RE: The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res. 2004, 94: 537-553. 10.1079/BER2004321.CrossRefPubMed
69.
go back to reference Morlais I, Mori A, Schneider JR, Severson DW: A targeted approach to the identification of candidate genes determining susceptibility to Plasmodium gallinaceum in Aedes aegypti. Mol Gen Genomics. 2003, 269: 753-764. 10.1007/s00438-003-0882-7.CrossRef Morlais I, Mori A, Schneider JR, Severson DW: A targeted approach to the identification of candidate genes determining susceptibility to Plasmodium gallinaceum in Aedes aegypti. Mol Gen Genomics. 2003, 269: 753-764. 10.1007/s00438-003-0882-7.CrossRef
70.
go back to reference Ricklefs RE, Fallon SM: Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci. 2002, 269: 885-892. 10.1098/rspb.2001.1940.CrossRef Ricklefs RE, Fallon SM: Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci. 2002, 269: 885-892. 10.1098/rspb.2001.1940.CrossRef
71.
go back to reference Ricklefs RE, Fallon SM, Bermingham E: Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol. 2004, 53: 111-119. 10.1080/10635150490264987.CrossRefPubMed Ricklefs RE, Fallon SM, Bermingham E: Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol. 2004, 53: 111-119. 10.1080/10635150490264987.CrossRefPubMed
72.
go back to reference Iezhova TA, Valkiūnas G, Barlein F: Vertebrate host specificity of two avian malaria parasites of subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol. 2005, 91: 472-474. 10.1645/GE-3377RN.CrossRefPubMed Iezhova TA, Valkiūnas G, Barlein F: Vertebrate host specificity of two avian malaria parasites of subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol. 2005, 91: 472-474. 10.1645/GE-3377RN.CrossRefPubMed
73.
go back to reference Gager AG, Loaiza JDR, Dearborn DC, Bermingham E: Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host?. Mol Ecol. 2008, 17: 2552-2561. 10.1111/j.1365-294X.2008.03764.x.CrossRefPubMed Gager AG, Loaiza JDR, Dearborn DC, Bermingham E: Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host?. Mol Ecol. 2008, 17: 2552-2561. 10.1111/j.1365-294X.2008.03764.x.CrossRefPubMed
74.
go back to reference Ricklefs RE, Swanson BL, Fallon SM: Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr. 2005, 75: 543-559. 10.1890/04-1820.CrossRef Ricklefs RE, Swanson BL, Fallon SM: Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr. 2005, 75: 543-559. 10.1890/04-1820.CrossRef
Metadata
Title
Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa
Authors
Kevin Y Njabo
Anthony J Cornel
Ravinder NM Sehgal
Claire Loiseau
Wolfgang Buermann
Ryan J Harrigan
John Pollinger
Gediminas Valkiūnas
Thomas B Smith
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2009
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-8-193

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