Avian haemosporidians in haematophagous insects in the Czech Republic

Parasitology Research - Tập 112 - Trang 839-845 - 2012
Petr Synek1, Pavel Munclinger1, Tomáš Albrecht1, Jan Votýpka2
1Department of Zoology, Charles University in Prague, Faculty of Science, Prague 2, Czech Republic
2Department of Parasitology, Charles University in Prague, Faculty of Science, Prague 2, Czech Republic

Tóm tắt

The degree to which avian haemosporidian parasites can exploit different vectors as a definitive host has ecological implications for their transmission and biogeography. Studies targeting haemosporidian parasites using precise molecular detection methods are almost lacking in Central Europe, however. Here, we utilized PCR-based molecular methods to detect avian haemosporidians in insect vectors in the Czech Republic. Nine lineages of parasites belonging to three genera, Haemoproteus, Plasmodium, and Leucocytozoon, were detected in pooled samples of insect individuals, of which three lineages had not yet been discovered in previous studies. All three Leucocytozoon lineages were found exclusively in black flies, while five Haemoproteus lineages were found in biting midges. The most abundant insect species Culicoides kibunensis harbored three Haemoproteus lineages, and the second-most numerous species Culicoides segnis even four. The positive mosquitoes of Culex pipiens complex hosted two parasite lineages, one Plasmodium and one Haemoproteus, the latter of which, however, could suggest the aberrant development of this parasite in an unusual invertebrate host. The co-occurrence of Haemoproteus ROFI1 and TURDUS2 lineages in both insects and birds at the same study plot suggests a transmission of these lineages during breeding season of birds.

Tài liệu tham khảo

Albrecht T (2004) Edge effect in wetland-arable land boundary determines nesting success of scarlet rosefinches (Carpodacus erythrinus) in the Czech Republic. Auk 121:361–371 Albrecht T, Schnitzer J, Kreisinger J, Exnerová A, Bryja J, Munclinger P (2007) Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav Ecol 18:477–486 Albrecht T, Vinkler M, Schnitzer J, Poláková R, Munclinger P, Bryja J (2009) Extra-pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine. J Evol Biol 22:2020–2030 Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol 42:530–537 Atkinson CT (1988) Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: potential vectors and prevalence in naturally infected Culicoides (Diptera: Ceratopogonidae). J Med Entomol 74:228–223 Beadell JS, Covas R, Gebhard C, Ishtiaq F, Melo M, Schmidt BK, Perkins SL, Graves GR, Fleischer RC (2009) Host associations and evolutionary relationships of avian blood parasites from West Africa. Int J Parasitol 39:257–266 Bennett GF, Warren M, Cheong WH (1966) Biology of the Malaysian strain of Plasmodium juxtanucleare Versiani and Gomes, 1941. II. The sporogonic stages in Culex (Culex) sitiens Wiedmann. J Parasitol 52:647–652 Bensch S, Hellgren O, Pérez-Tris (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358 Bentz S, Rigaud T, Barroca M, Martin-Laurent F, Bru D, Moreau J, Faivre B (2006) Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Parasitology 133:685–692 Černý O, Votýpka J, Svobodová M (2011) Spatial feeding preferences of ornithophilic mosquitoes, blackflies and biting midges. Med Vet Entomol 25:104–108 Chvála M (1980) Fauna ČSSR 22. Academia, Prague Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548 Desser SS, Bennett GF (1993) The genera Leucocytozoon, Haemoproteus and Hepatocystis. In: Kreier JP (ed) Parasitic protozoa. Vol. 4, 2nd edn. Academic, New York Dimitrov D, Zehtindjiev P, Bensch S (2010) Genetic diversity of avian blood parasites in SE Europe: cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Acta Parasitol 55:201–209 Ejiri H, Sato Y, Sawai R, Sasaki E, Matsumoto R, Ueda M, Higa Y, Tsuda Y, Omori S, Murata K, Yukawa M (2009) Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitol Res 105:629–633 Gager AB, Del Rosario Loaiza J, Dearborn DC, Bermingham E (2008) Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host? Mol Ecol 17:2552–2561 Garvin MC, Greiner EC (2003) Ecology of Culicoides (Diptera: Ceratopogonidae) in southcentral Florida and experimental Culicoides vectors of the avian hematozoan Haemoproteus danilewskyi Kruse. J Wildl Dis 39:170–178 Glaizot O, Fumagalli L, Iritano K, Lalubin F, Van Rooyen J, Christe P (2012) High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens). PLoS One 7:e34964 Hellgren O, Waldenstrom J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802 Hellgren O, Križanauskienė A, Valkiūnas G, Bensch S (2007a) Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 93:889–896 Hellgren O, Waldenstrom J, Perez-Tris J, Szollosi E, Hasselquist D, Križanauskienė A, Ottosson U, Bensch S (2007b) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol Ecol 16:1281–1290 Hellgren O, Bensch S, Malmqvist B (2008) Bird hosts, blood parasites and their vectors-associations uncovered by molecular analyses of blackfly blood meals. Mol Ecol 17:1605–1613 Hellgren O, Križanauskienė A, Hasselquist D, Bensch S (2011) Low haemosporidian diversity and one key-host species in a bird malaria community on a mid-Atlantic island (São Miguel, Azores). J Wildl Dis 47:849–859 Hunninnen AV (1953) Comparative development of Plasmodium relictum oocysts in Anopheles quadrimaculatus, A. albimanus, and Culex pipiens. J Parasitol 39:28–32 Ishtiaq F, Guillaumot L, Clegg SM, Phillimore AB, Black RA, Owens IPF, Mundy NI, Sheldon BC (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17:4545–4555 Kim KS, Tsuda Y (2010) 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 19:5545–5554 Kim KS, Tsuda Y, Sasaki T, Kobayashi M, Hirota Y (2009) Mosquito blood-meal analysis for avian malaria study in wild bird communities: laboratory verification and application to Culex sasai (Diptera: Culicidae) collected in Tokyo, Japan. Parasitol Res 105:1351–1357 Kimura M, Darbro JM, Harrington LC (2010) Avian malaria parasites share congeneric mosquito vectors. J Parasitol 96:144–151 Knowles SCL, Nakagawa S, Sheldon BC (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Funct Ecol 23:405–415 Knowles SC, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol Ecol 20:1062–1076 Križanauskienė A, Hellgren O, Kosatec V, Sokolov L, Bensch S, Valkinūas G (2006) Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. J Parasitol 92:1319–1324 LaPointe DA, Goff ML, Atkinson CT (2005) Comparative susceptibility of introduced forest dwelling mosquitoes in Hawai’i to avian malaria, Plasmodium relictum. J Parasitol 91:843–849 Martínez-de la Puente J, Martínez J, Rivero-de Aguilar J, Herrero J, Merino S (2011) On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges. Mol Ecol 20:3275–3287 Martinsen ES, Waite JL, Schall JJ (2007) Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology 134:483–490 Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261–273 Marzal A, Ricklefs RE, Valkiūnas G, Albayrak T, Arriero E, Bonneaud C, Czirják GA, Ewen J, Hellgren O, Hořáková D, Iezhova TA, Jensen H, Križanauskienė A, Lima MR, de Lope F, Magnussen E, Martin LB, Møller AP, Palinauskas V, Pap PL, Pérez-Tris J, Sehgal RN, Soler M, Szöllosi E, Westerdahl H, Zetindjiev P, Bensch S (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One 6:e21905 Morii T (1992) A review of Leucocytozoon caulleryi infection in chickens. J Protozool Res 2:128–133 Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RN, Valkiūnas G, Russell AF, Smith TB (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol 20:1049–1061 Sato Y, Tamada A, Mochizuki Y, Nakamura S, Okano E, Yoshida C, Ejiri H, Omori S, Yukawa M, Murata K (2009) Molecular detection of Leucocytozoon lovati from probable vectors, black flies (Simuliudae) collected in the alpine regions of Japan. Parasitol Res 104:251–255 Svensson-Coelho M, Ricklefs RE (2011) Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles. J Anim Ecol 80:938–946 Tomás G, Merino S, Martínez-de la Puente J, Moreno J, Morales J, Lobato E (2008) A simple trapping method to estimate abundances of blood-sucking flying insects in avian nests. Anim Behav 75:723–729 Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton Valkiūnas G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Mol Ecol 20:3084–3086 Valkiūnas G, Liutkevicius G, Iezhova TA (2002) Complete development of three species of Haemoproteus (Haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). J Parasitol 88:864–868 Valkiūnas G, Iezhova TA, Križanauskien A, Palinauskas V, Bensch S (2008) In vitro hybridization of Haemoproteus spp.; an experimental approach for direct investigation of reproductive isolation of parasites. J Parasitol 94:1385–1394 Vinkler M, Schnitzer J, Munclinger P, Albrecht T (2012) Phytohaemagglutinin skin-swelling test in scarlet rosefinch males: low-quality birds respond more strongly. Anim Behav 83:17–23 Votýpka J, Synek P, Svobodová M (2009) Endophagy of biting midges attacking cavity-nesting birds. Med Vet Entomol 23:277–280 Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC (2007) Within population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16:3263–3273 Work TM, Washino RK, van Riper C (1990) Comparative susceptibility of Culex tarsalis, Anopheles franciscanus, and Culiseta inornata (Diptera: Culicidae) to Plasmodium relictum (Haemosporidia: Plasmodiiae). J Med Entomol 27:68–71