Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Avian Plasmodium in Eastern Austrian mosquitoes

Authors: Ellen Schoener, Sarah Susanne Uebleis, Julia Butter, Michaela Nawratil, Claudia Cuk, Eva Flechl, Michael Kothmayer, Adelheid G. Obwaller, Thomas Zechmeister, Franz Rubel, Karin Lebl, Carina Zittra, Hans-Peter Fuehrer

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Insect vectors, namely mosquitoes (Diptera: Culicidae), are compulsory for malaria parasites (Plasmodium spp.) to complete their life cycle. Despite this, little is known about vector competence of different mosquito species for the transmission of avian malaria parasites.

Methods

In this study, nested PCR was used to determine Plasmodium spp. occurrence in pools of whole individuals, as well as the diversity of mitochondrial cytochrome b gene sequences in wild-caught mosquitoes sampled across Eastern Austria in 2013–2015.

Results

A total of 45,749 mosquitoes in 2628 pools were collected, of which 169 pools (6.43%) comprising 9 mosquito species were positive for avian Plasmodium, with the majority of positives in mosquitoes of Culex pipiens s.l./Culex torrentium. Six different avian Plasmodium lineages were found, the most common were Plasmodium vaughani SYAT05, Plasmodium sp. Linn1 and Plasmodium relictum SGS1. In 2014, mosquitoes of the Culex pipiens complex were genetically identified and Culex pipiens f. pipiens presented with the highest number of avian Plasmodium positives (n = 37; 16.74%). Despite this, the minimum infection rate (MIR) was highest in Culex torrentium (5.36%) and Culex pipiens f. pipiens/f. molestus hybrids (5.26%). During 2014 and 2015, seasonal and annual changes in Plasmodium lineage distribution were also observed. In both years P. vaughani SYAT05 dominated at the beginning of the sampling period to be replaced later in the year by P. relictum SGS1 (2014) and Plasmodium sp. Linn1 (2015).

Conclusions

This is the first large-scale study of avian Plasmodium parasites in Austrian mosquitoes. These results are of special interest, because molecular identification of the taxa of the Cx. pipiens complex and Cx. torrentium enabled the determination of Plasmodium prevalence in the different mosquito taxa and hybrids of this complex. Since pools of whole insects were used, it is not possible to assert any vector competence in any of the examined mosquitoes, but the results are nonetheless valuable in providing an overview of avian Plasmodium species and lineages present in Austria.
Literature
1.
go back to reference Valkiunas G, editor. Avian malaria parasites and other Haemosporidia. Boca Raton: CRC; 2005. Valkiunas G, editor. Avian malaria parasites and other Haemosporidia. Boca Raton: CRC; 2005.
2.
go back to reference Clark NJ, Clegg SM, Lima MR. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol. 2014;44:329–38.CrossRefPubMed Clark NJ, Clegg SM, Lima MR. A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol. 2014;44:329–38.CrossRefPubMed
3.
go back to reference Lalubin F, Deledevant A, Glaizot O, Christe P. Temporal changes in mosquito abundance (Culex pipiens), avian malaria prevalence and lineage composition. Parasit Vectors. 2013;6:307.CrossRefPubMedPubMedCentral Lalubin F, Deledevant A, Glaizot O, Christe P. Temporal changes in mosquito abundance (Culex pipiens), avian malaria prevalence and lineage composition. Parasit Vectors. 2013;6:307.CrossRefPubMedPubMedCentral
4.
go back to reference Marzal A, Bensch S, Reviriego M, Balbontin J, de Lope F. Effects of malaria double infection in birds: one plus one is not two. J Evol Biol. 2008;21:979–87.CrossRefPubMed Marzal A, Bensch S, Reviriego M, Balbontin J, de Lope F. Effects of malaria double infection in birds: one plus one is not two. J Evol Biol. 2008;21:979–87.CrossRefPubMed
5.
go back to reference Ventim R, Ramos JA, Osorio H, Lopes RJ, Perez-Tris J, Mendes L. Avian malaria infections in western European mosquitoes. Parasitol Res. 2012;111:637–45.CrossRefPubMed Ventim R, Ramos JA, Osorio H, Lopes RJ, Perez-Tris J, Mendes L. Avian malaria infections in western European mosquitoes. Parasitol Res. 2012;111:637–45.CrossRefPubMed
6.
go back to reference la Puente Martínez-de, Ferraguti M, Ruiz S, Roiz D, Soriguer RC, Figuerola J. Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malar J. 2016;15:589.CrossRef la Puente Martínez-de, Ferraguti M, Ruiz S, Roiz D, Soriguer RC, Figuerola J. Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malar J. 2016;15:589.CrossRef
7.
go back to reference Hellgren O, Perez-Tris J, Bensch S. A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology. 2009;90:2840–9.CrossRefPubMed Hellgren O, Perez-Tris J, Bensch S. A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology. 2009;90:2840–9.CrossRefPubMed
8.
go back to reference Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, et al. Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography. 2015;38:842–50.CrossRef Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, et al. Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography. 2015;38:842–50.CrossRef
9.
go back to reference Dinhopl N, Nedorost N, Mostegl MM, Weissenbacher-Lang C, Weissenbock H. In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitol Res. 2015;114:1455–62.CrossRefPubMed Dinhopl N, Nedorost N, Mostegl MM, Weissenbacher-Lang C, Weissenbock H. In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitol Res. 2015;114:1455–62.CrossRefPubMed
10.
go back to reference Kimura M, Darbro JM, Harrington LC. Avian malaria parasites share congeneric mosquito vectors. J Parasitol. 2010;96:144–51.CrossRefPubMed Kimura M, Darbro JM, Harrington LC. Avian malaria parasites share congeneric mosquito vectors. J Parasitol. 2010;96:144–51.CrossRefPubMed
11.
go back to reference LaPointe DA, Goff ML, Atkinson CT. Comparative susceptibility of introduced forest dwelling mosquitoes in Hawai’i to avian malaria, Plasmodium relictum. J Parasitol. 2005;91:843–9.CrossRefPubMed LaPointe DA, Goff ML, Atkinson CT. Comparative susceptibility of introduced forest dwelling mosquitoes in Hawai’i to avian malaria, Plasmodium relictum. J Parasitol. 2005;91:843–9.CrossRefPubMed
12.
go back to reference Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P. High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens). PLoS ONE. 2012;7:e34964.CrossRefPubMedPubMedCentral Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P. High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens). PLoS ONE. 2012;7:e34964.CrossRefPubMedPubMedCentral
13.
go back to reference Bensch S, Hellgren O, Perez-Tris J. MalAvi. A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Res. 2009;9:1353–8.CrossRef Bensch S, Hellgren O, Perez-Tris J. MalAvi. A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Res. 2009;9:1353–8.CrossRef
14.
go back to reference Zittra C, Joachim A, Fuehrer H-P. Mosquitoes and Dirofilaria in Austria-a review of the current situation of neobiotic Culicidae and Dirofilariae. Tierärztliche Umschau. 2015;70:126–31. Zittra C, Joachim A, Fuehrer H-P. Mosquitoes and Dirofilaria in Austria-a review of the current situation of neobiotic Culicidae and Dirofilariae. Tierärztliche Umschau. 2015;70:126–31.
15.
go back to reference Zittra C, Obwaller AG, Wimmer V, Berer D, Eigner B, Fuehrer HP. First record of Orthopodomya pulcripalpis (Rondani, 1872) (Diptera: Culicidae) in Austria. Parasitol Res. 2017;116:1781–3.CrossRefPubMedPubMedCentral Zittra C, Obwaller AG, Wimmer V, Berer D, Eigner B, Fuehrer HP. First record of Orthopodomya pulcripalpis (Rondani, 1872) (Diptera: Culicidae) in Austria. Parasitol Res. 2017;116:1781–3.CrossRefPubMedPubMedCentral
16.
go back to reference Becker N, Petrić D, Boase C, Lane J, Zgomba M, Dahl C, Kaiser A. Mosquitoes and their control. Berlin: Springer; 2003.CrossRef Becker N, Petrić D, Boase C, Lane J, Zgomba M, Dahl C, Kaiser A. Mosquitoes and their control. Berlin: Springer; 2003.CrossRef
17.
go back to reference Ferraguti M, Martinez-de la Puente J, Munoz J, Roiz D, Ruiz S, Soriguer R, Figuerola J. Avian Plasmodium in Culex and Ochlerotatus mosquitoes from Southern Spain: effects of season and host-feeding source on parasite dynamics. PLoS ONE. 2013;8:e66237.CrossRefPubMedPubMedCentral Ferraguti M, Martinez-de la Puente J, Munoz J, Roiz D, Ruiz S, Soriguer R, Figuerola J. Avian Plasmodium in Culex and Ochlerotatus mosquitoes from Southern Spain: effects of season and host-feeding source on parasite dynamics. PLoS ONE. 2013;8:e66237.CrossRefPubMedPubMedCentral
18.
go back to reference Inci A, Yildirim A, Njabo K, Duzlu O, Biskin Z, Ciloglu A. Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol. 2012;188:179–84.CrossRefPubMed Inci A, Yildirim A, Njabo K, Duzlu O, Biskin Z, Ciloglu A. Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol. 2012;188:179–84.CrossRefPubMed
19.
go back to reference Martinez-de la Puente J, Munoz J, Capelli G, Montarsi F, Soriguer R, Arnoldi D, et al. Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malar J. 2015;14:32.CrossRefPubMedPubMedCentral Martinez-de la Puente J, Munoz J, Capelli G, Montarsi F, Soriguer R, Arnoldi D, et al. Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malar J. 2015;14:32.CrossRefPubMedPubMedCentral
20.
go back to reference Santiago-Alarcon D, Palinauskas V, Schaefer HM. Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev. 2012;87:928–64.CrossRefPubMed Santiago-Alarcon D, Palinauskas V, Schaefer HM. Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev. 2012;87:928–64.CrossRefPubMed
21.
go back to reference Zele F, Vezilier J, L’Ambert G, Nicot A, Gandon S, Rivero A, et al. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance. Parasit Vectors. 2014;7:437.CrossRefPubMedPubMedCentral Zele F, Vezilier J, L’Ambert G, Nicot A, Gandon S, Rivero A, et al. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance. Parasit Vectors. 2014;7:437.CrossRefPubMedPubMedCentral
22.
go back to reference Ziegyte R, Bernotiene R, Bukauskaite D, Palinauskas V, Iezhova T, Valkiunas G. Complete sporogony of Plasmodium relictum (lineages pSGS1 and pGRW11) in mosquito Culex pipiens pipiens form molestus, with implications to avian malaria epidemiology. J Parasitol. 2014;100:878–82.CrossRefPubMed Ziegyte R, Bernotiene R, Bukauskaite D, Palinauskas V, Iezhova T, Valkiunas G. Complete sporogony of Plasmodium relictum (lineages pSGS1 and pGRW11) in mosquito Culex pipiens pipiens form molestus, with implications to avian malaria epidemiology. J Parasitol. 2014;100:878–82.CrossRefPubMed
23.
go back to reference Valkiunas G, Ziegyte R, Palinauskas V, Bernotiene R, Bukauskaite D, Ilgunas M, et al. Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitol Res. 2015;114:3075–85.CrossRefPubMed Valkiunas G, Ziegyte R, Palinauskas V, Bernotiene R, Bukauskaite D, Ilgunas M, et al. Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitol Res. 2015;114:3075–85.CrossRefPubMed
24.
go back to reference Kazlauskiene R, Bernotiene R, Palinauskas V, Iezhova TA, Valkiunas G. Plasmodium relictum (lineages pSGS1 and pGRW11): complete synchronous sporogony in mosquitoes Culex pipiens pipiens. Exp Parasitol. 2013;133:454–61.CrossRefPubMed Kazlauskiene R, Bernotiene R, Palinauskas V, Iezhova TA, Valkiunas G. Plasmodium relictum (lineages pSGS1 and pGRW11): complete synchronous sporogony in mosquitoes Culex pipiens pipiens. Exp Parasitol. 2013;133:454–61.CrossRefPubMed
25.
go back to reference Zittra C, Flechl E, Kothmayer M, Vitecek S, Rossiter H, Zechmeister T, et al. Ecological characterization and molecular differentiation of Culex pipiens complex taxa and Culex torrentium in eastern Austria. Parasit Vectors. 2016;9:197.CrossRefPubMedPubMedCentral Zittra C, Flechl E, Kothmayer M, Vitecek S, Rossiter H, Zechmeister T, et al. Ecological characterization and molecular differentiation of Culex pipiens complex taxa and Culex torrentium in eastern Austria. Parasit Vectors. 2016;9:197.CrossRefPubMedPubMedCentral
26.
go back to reference Hellgren O, Waldenstrom J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.CrossRefPubMed Hellgren O, Waldenstrom J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.CrossRefPubMed
27.
go back to reference Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.CrossRefPubMedPubMedCentral Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.CrossRefPubMedPubMedCentral
28.
go back to reference Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2011;39:D32–7.CrossRefPubMed Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2011;39:D32–7.CrossRefPubMed
29.
go back to reference White BJ, Andrew DR, Mans NZ, Ohajuruka OA, Garvin MC. West Nile Virus in mosquitoes of northern Ohio, 2003. Am J Trop Med Hyg. 2006;75:346–9.PubMed White BJ, Andrew DR, Mans NZ, Ohajuruka OA, Garvin MC. West Nile Virus in mosquitoes of northern Ohio, 2003. Am J Trop Med Hyg. 2006;75:346–9.PubMed
30.
go back to reference Synek P, Munclinger P, Albrecht T, Votypka J. Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitol Res. 2013;112:839–45.CrossRefPubMed Synek P, Munclinger P, Albrecht T, Votypka J. Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitol Res. 2013;112:839–45.CrossRefPubMed
31.
go back to reference Jarvi SI, Farias ME, Atkinson CT. Genetic characterization of Hawaiian isolates of Plasmodium relictum reveals mixed-genotype infections. Biol Direct. 2008;3:25.CrossRefPubMedPubMedCentral Jarvi SI, Farias ME, Atkinson CT. Genetic characterization of Hawaiian isolates of Plasmodium relictum reveals mixed-genotype infections. Biol Direct. 2008;3:25.CrossRefPubMedPubMedCentral
32.
go back to reference Van Rooyen J, Lalubin F, Glaizot O, Christe P. Avian haemosporidian persistence and co-infection in great tits at the individual level. Malar J. 2013;12:40.CrossRefPubMedPubMedCentral Van Rooyen J, Lalubin F, Glaizot O, Christe P. Avian haemosporidian persistence and co-infection in great tits at the individual level. Malar J. 2013;12:40.CrossRefPubMedPubMedCentral
33.
go back to reference Jarvi SI, Schultz JJ, Atkinson CT. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol. 2002;88:153–8.CrossRefPubMed Jarvi SI, Schultz JJ, Atkinson CT. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol. 2002;88:153–8.CrossRefPubMed
34.
go back to reference Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S. Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res. 2007;100:1311–22.CrossRefPubMed Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S. Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res. 2007;100:1311–22.CrossRefPubMed
35.
go back to reference Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D, et al. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome b gene. J Parasitol. 2012;98:657–65.CrossRefPubMed Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D, et al. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome b gene. J Parasitol. 2012;98:657–65.CrossRefPubMed
36.
go back to reference Valkiunas G, Bensch S, Iezhova TA, Krizanauskiene A, Hellgren O, Bolshakov CV. Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. J Parasitol. 2006;92:418–22.CrossRefPubMed Valkiunas G, Bensch S, Iezhova TA, Krizanauskiene A, Hellgren O, Bolshakov CV. Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. J Parasitol. 2006;92:418–22.CrossRefPubMed
37.
go back to reference Fryxell RTT, Lewis TT, Peace H, Hendricks BBM, Paulsen D. Identification OF avian malaria (Plasmodium sp.) and canine heartworm (Dirofilaria immitis) in the mosquitoes of Tennessee. J Parasitol. 2014;100:455–62.CrossRefPubMed Fryxell RTT, Lewis TT, Peace H, Hendricks BBM, Paulsen D. Identification OF avian malaria (Plasmodium sp.) and canine heartworm (Dirofilaria immitis) in the mosquitoes of Tennessee. J Parasitol. 2014;100:455–62.CrossRefPubMed
38.
go back to reference Ejiri H, Sato Y, Sawai R, Sasaki E, Matsumoto R, Ueda M, et al. Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitol Res. 2009;105:629–33.CrossRefPubMed Ejiri H, Sato Y, Sawai R, Sasaki E, Matsumoto R, Ueda M, et al. Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitol Res. 2009;105:629–33.CrossRefPubMed
39.
go back to reference Kim KS, Tsuda Y. Seasonal changes in the feeding pattern of Culex pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol. 2010;19:5545–54.CrossRefPubMed Kim KS, Tsuda Y. Seasonal changes in the feeding pattern of Culex pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol. 2010;19:5545–54.CrossRefPubMed
40.
go back to reference Kim KS, Tsuda Y, Yamada A. Bloodmeal identification and detection of avian malaria parasite from mosquitoes (Diptera: Culicidae) inhabiting coastal areas of Tokyo Bay, Japan. J Med Entomol. 2009;46:1230–4.CrossRefPubMed Kim KS, Tsuda Y, Yamada A. Bloodmeal identification and detection of avian malaria parasite from mosquitoes (Diptera: Culicidae) inhabiting coastal areas of Tokyo Bay, Japan. J Med Entomol. 2009;46:1230–4.CrossRefPubMed
41.
go back to reference Ishtiaq F, Guillaumot L, Clegg S, Phillimore A, Black R, Owens I, Mundy N, et al. Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol. 2008;17:4545–55.CrossRefPubMed Ishtiaq F, Guillaumot L, Clegg S, Phillimore A, Black R, Owens I, Mundy N, et al. Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol. 2008;17:4545–55.CrossRefPubMed
42.
go back to reference Kim KS, Tsuda Y. Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist for multiple years? Mol Ecol. 2012;21:5374–85.CrossRefPubMed Kim KS, Tsuda Y. Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist for multiple years? Mol Ecol. 2012;21:5374–85.CrossRefPubMed
43.
go back to reference Ejiri H, Sato Y, Kim K-S, Hara T, Tsuda Y, Imura T, et al. Entomological study on transmission of avian malaria parasites in a zoological garden in Japan: bloodmeal identification and detection of avian malaria parasite DNA from blood-fed mosquitoes. J Med Entomol. 2011;48:600–7.CrossRefPubMed Ejiri H, Sato Y, Kim K-S, Hara T, Tsuda Y, Imura T, et al. Entomological study on transmission of avian malaria parasites in a zoological garden in Japan: bloodmeal identification and detection of avian malaria parasite DNA from blood-fed mosquitoes. J Med Entomol. 2011;48:600–7.CrossRefPubMed
44.
go back to reference Atkinson CT, van Riper C. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M, editors. Bird-parasite interactions: ecology, evolution, and behavior. Oxford: Oxford University Press; 1991. Atkinson CT, van Riper C. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M, editors. Bird-parasite interactions: ecology, evolution, and behavior. Oxford: Oxford University Press; 1991.
45.
go back to reference Ilgūnas M, Bukauskaitė D, Palinauskas V, Iezhova TA, Dinhopl N, Nedorost N, et al. Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malar J. 2016;15:256.CrossRefPubMedPubMedCentral Ilgūnas M, Bukauskaitė D, Palinauskas V, Iezhova TA, Dinhopl N, Nedorost N, et al. Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malar J. 2016;15:256.CrossRefPubMedPubMedCentral
46.
go back to reference Allander K, Bennett GF. Prevalence and intensity of haematozoan infection in a population of great tits Parus major from Gotland, Sweden. J Avian Biol. 1994;25:69–74.CrossRef Allander K, Bennett GF. Prevalence and intensity of haematozoan infection in a population of great tits Parus major from Gotland, Sweden. J Avian Biol. 1994;25:69–74.CrossRef
47.
go back to reference Werblow A, Flechl E, Klimpel S, Zittra C, Lebl K, Kieser K. Direct PCR of indigenous and invasive mosquito species: a time-and cost-effective technique of mosquito barcoding. Med Vet Entomol. 2016;30:8–13.CrossRefPubMed Werblow A, Flechl E, Klimpel S, Zittra C, Lebl K, Kieser K. Direct PCR of indigenous and invasive mosquito species: a time-and cost-effective technique of mosquito barcoding. Med Vet Entomol. 2016;30:8–13.CrossRefPubMed
48.
go back to reference Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, et al. Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol. 2011;20:1049–61.CrossRefPubMed Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, et al. Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol. 2011;20:1049–61.CrossRefPubMed
49.
go back to reference Njabo KY, Cornel AJ, Sehgal RNM, Loiseau C, Buermann W, Harrigan RJ, et al. Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa. Malar J. 2009;8:193.CrossRefPubMedPubMedCentral Njabo KY, Cornel AJ, Sehgal RNM, Loiseau C, Buermann W, Harrigan RJ, et al. Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa. Malar J. 2009;8:193.CrossRefPubMedPubMedCentral
50.
go back to reference Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, et al. Host selection by Culex pipiens mosquitoes and West Nile virus amplification. Am J Trop Med Hyg. 2009;80:268–78.PubMed Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, et al. Host selection by Culex pipiens mosquitoes and West Nile virus amplification. Am J Trop Med Hyg. 2009;80:268–78.PubMed
Metadata
Title
Avian Plasmodium in Eastern Austrian mosquitoes
Authors
Ellen Schoener
Sarah Susanne Uebleis
Julia Butter
Michaela Nawratil
Claudia Cuk
Eva Flechl
Michael Kothmayer
Adelheid G. Obwaller
Thomas Zechmeister
Franz Rubel
Karin Lebl
Carina Zittra
Hans-Peter Fuehrer
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-2035-1

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue