Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2013-02-18
Page range: 85–94
Abstract views: 18
PDF downloaded: 1

Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons

Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Department of Biology, San Francisco State University, 1600 Holloway Ave., San Francisco, California, 94132
Department of Biology, San Francisco State University, 1600 Holloway Ave., San Francisco, California, 94132
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Protozoa Haemoproteus Parahaemoproteus haemosporidians Columbidae Hippoboscidae Ceratopogonidae barcoding

Abstract

Haemoproteus (Haemosporida, Haemoproteidae) is the largest genus of avian haemosporidian parasites, some species of which cause lethal diseases in birds. Subgenera Parahaemoproteus and Haemoproteus are usually accepted in this genus; these parasites are transmitted by biting midges (Ceratopogonidae) and hippoboscid flies (Hippoboscidae), respectively. As of yet, species of Parahaemoproteus have not been reported to infect doves and pigeons (Columbiformes), parasites of these birds have not been reported to be transmitted by biting midges (Ceratopogonidae). Applying microscopy and PCR based methods, we identified mitochondrial cytochrome b (cyt b) sequences of Haemoproteus sacharovi, a wide-spread parasite of doves and pigeons. Phylogenetic relationships of dove haemoproteids, which traditionally have been classified in the subgenus Haemoproteus, showed that H. sacharovi and H. turtur, common parasites of doves, branch in the clade with Parahaemoproteus species, indicating that these haemoproteids may belong to this subgenus and are likely transmitted by biting midges. This study provides barcodes for H. sacharovi, clarifies the taxonomic positions of H. sa-charovi and H. turtur, and indicates directions for development of classification of avian haemoproteid species. Our anal-ysis shows that the current subgeneric classification of avian haemoproteids is generally effective, but the position of some species may need to be revised.

References

  1. Atkinson, C.T. (1991) Vectors, epizootiology, and pathogenicity of avian species of Haemoproteus (Haemosporina: Haemoproteidae). Bulletin of the Society of Vector Ecology, 16, 109–126.

    Atkinson, C.T. & LaPointe, D.A. (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery, 23, 53–63. http://dx.doi.org/10.1647/2008-059.1

    Baker, J.R. (1966) Haemoproteus palumbis sp. nov. (Sporozoa, Haemosporina) of the English Wood-Pigeon Columba p. palumbus. Journal of Protozoology, 13, 515–519. http://dx.doi.org/10.1111/j.1550-7408.1966.tb01954.x

    Belo, N.O., Pinheiro, R.T., Reis, E.S., Ricklefs, R.E. & Braga, E.M. (2011) Prevalence and lineage diversity of avian haemosporidians from three distinct Cerrado habitats in Brazil. PloS ONE 6(3), e17654. http://dx.doi.org/10.1371/journal.pone.0017654

    Bennett, G.F. & Peirce, M.A. (1988) Morphological form in the avian Haemoproteidae and annotated checklist of the genus Haemoproteus Kruse, 1890. Journal of Natural History, 22, 1683–1696. http://dx.doi.org/10.1080/00222938800771061

    Bensch, S., Stjenman, M., Hasselquist, D., Östman, Ö., Hansson, B., Westerdahl, H. & Torres-Pinheiro, R. (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London Series B, Biological Sciences, 276, 1583–1589. http://dx.doi.org/10.1098/rspb.2000.1181

    Bensch, S., Pérez-Tris, J., Waldenström, J. & Hellgren, O. (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution, 58, 1617–1621. qhttp://dx.doi.org/10.1554/04-026

    Bensch, S., Hellgren, O. & Pérez-Tris, J. (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353–1358. http://dx.doi.org/10.1111/j.1755-0998.2009.02692.x

    Bishop, M.A. & Bennett, G.F. (1992) Host-parasite catalogue of the avian haematozoa: Supplement 1, and Bibliography of the avian blood-inhabiting haematozoa: Supplement 2. Occasional Papers in Biology, Memorial University of Newfoundland, 15, 1–244.

    Corradetti, A., Garnham, P.C.C. & Laird, M. (1963) New classification of the avian malaria parasites. Parassitologia, 5, 1–4.

    Desser, S.S. & Bennett, G.F. (1993) The genera Leucocytozoon, Haemoproteus and Hepatocystis. Parasitic Protozoa, 4, 273–307.

    Fallis, A.M. & Wood, D.M. (1957) Biting midges (Diptera:Ceratopogonidae) as intermediate hosts for Haemoproteus of ducks. Canadian Journal of Zoology, 35, 425–435. http://dx.doi.org/10.1139/z57-033

    Fernandez, M., Rojo, A., Casanueva, P., Carrion, S., Hernandez, A. & Campos, F. (2010) High prevalence of haemosporidians in Reed warbler Acrocephalus scirpaceus and Sedge warbler Acrocephalus shoenobaenus in Spain. Journal of Ornithology, 151, 27–32. http://dx.doi.org/10.1007/s10336-009-0417-z

    Ferrell, S.T., Snowden, K., Marlar, A.B., Garner, M. & Lung, N.P. (2007) Fatal hemoprotozoal infections in multiple avian species in a zoological park. Journal of Zoo and Wildlife Medicine, 38, 309–316. http://dx.doi.org/10.1638/1042-7260(2007)038[0309:FHIIMA]2.0.CO;2

    Garnham, P.C.C. (1966) Malaria parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford, UK, 1114 pp. http://dx.doi.org/10.1126/science.157.3792.1029-a

    Greiner, E.C., Bennett, G.F., White, E.M. & Coombs, R.F. (1975) Distribution of the avian hematozoa of North America. Canadian Journal of Zoology, 53, 1762–1787. http://dx.doi.org/10.1139/z75-211

    Hall, T.A. (1999) BioEdit: A user—friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium, 41, 95–98.

    Hellgren, O., Waldenström, J., Pérez-Tris, J., Szöllősi, E., Hasselquist, D., Križanauskienė, A., Ottosson, U. & Bensch, S. (2007a) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Molecular Ecology, 16, 1281–1290. http://dx.doi.org/10.1111/j.1365-294X.2007.03227.x

    Hellgren, O., Križanauskienė, A., Valkiūnas, G. & Bensch, S. (2007b) Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida, Haemoproteidae). Journal of Parasitology, 93, 889–896. http://dx.doi.org/10.1645/GE-1051R1.1

    Huff, C.G. (1932) Studies on Haemoproteus of Mourning doves. American Journal of Epidemiology, 16, 618–623.

    Križanauskienė, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S. & Valkiūnas, G. (2006) Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. Journal of Parasitology, 92, 1319–1324. http://dx.doi.org/10.1645/GE-873R.1

    Križanauskienė, A., Pérez-Tris, J., Palinauskas, V., Hellgren, O., Bensch, S. & Valkiūnas, G. (2010) Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology, 137, 217–227.

    Krone, O., Waldenström, J., Valkiūnas, G., Lessow, O., Muller, K., Iezhova, T. A., Fickel, J. & Bensch, S. (2008) Haemosporidian blood parasites in European birds of pray and owls. Journal of Parasitology, 94, 709–715. http://dx.doi.org/10.1017/S0031182009991235

    Kumar, S., Tamura, K. & Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150–163. http://dx.doi.org/10.1093/bib/5.2.150

    Levine, N.D. & Cambell, G.R. (1971) A check-list of the species of genus Haemoproteus (Apicomplexa, Plasmodiidae). Journal of Protozoology, 18, 475–484. http://dx.doi.org/10.1111/j.1550-7408.1971.tb03358.x

    Levine, N.D. (1988) The Protozoan Phylum Apicomplexa. Vol. I–II. CRC Press, Boca Raton, Florida, USA, 203pp., 154 pp. http://dx.doi.org/10.1017/S0031182000078926

    Levin, I.I., Valkiūnas, G., Santiago-Alarcon, D., Cruz, L.L., Iezhova, T.A., O´Brien, S.L., Hailer, F., Dearborn, D., Scheiber, E. A., Fleischer, R.C., Ricklefs, R.E. & Parker, P.G. (2011) Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: Evidence from molecular and morphological studies, with a description of Haemoproteus iwa. International Journal of Parasitology, 41, 1019–1027. http://dx.doi.org/10.1016/j.ijpara.2011.03.014

    Levin, I.I., Valkiūnas, G., Iezhova, T.A., O'Brien, S.L. & Parker, P.G. (2012) Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. Journal of Parasitology, 98, 847–854. http://dx.doi.org/10.1645/ge-3007.1

    Martinsen, E.S, Perkins, S. & Schall, J.J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273. http://dx.doi.org/10.1016/j.ympev.2007.11.012

    McClure, H.E., Poonswad, P., Greiner, E.C. & Laird, M. (1978) Haematozoa in the birds of Eastern and Southern Asia. Memorial University of Newfoundland, St. John’s, Canada. 296 pp. http://dx.doi.org/10.2307/3280190

    Novy, F.G. & MacNeal, W.J. (1904) Trypanosomes and bird malaria. American Medicine, 8, 932–934.

    Olias, P., Wegelin, M., Zenker, W., Freter, S., Gruber, A.D. & Klopfleisch, R. (2011) Avian malaria deaths in parrots, Europe. Emerging Infection Diseases, 17, 950–952. http://dx.doi.org/10.3201/eid1705.101618

    Palinauskas, V., Kosarev, V., Shapoval, A., Bensch, S. & Valkiūnas, G. (2007) Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa, 1626, 39–50.

    Perkins, S.L. & Schall, J.J. (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88, 972–978. http://dx.doi.org/10.1645/0022-3395(2002)088[0972:AMPOMP]2.0.CO;2

    Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256. http://dx.doi.org/10.1093/molbev/msn083

    Rashdan, N.A. (1998) Role of Pseudolynchia canariensis in the transmission of Haemoproteus turtur from the migrant Streptopelia turtur to new bird hosts in Egypt. Journal of Egyptian Society for Parasitology, 28, 221–228.

    Ricklefs, R.E., Fallon, S.M. & Bermingham, E. (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology, 53, 111–119. http://dx.doi.org/10.1080/10635150490264987

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. http://dx.doi.org/10.1093/bioinformatics/btg180

    Santiago-Alarcon, D., Outlaw, D.C., Ricklefs, R.E. & Parker, P.G. (2010) High lineage diversity of Haemosporidian parasites in New World doves: multiple colonization of the Galapagos Islands. International Journal of Parasitology, 40, 463–470. http://dx.doi.org/10.1016/j.ijpara.2009.10.003

    Sehgal, R.N.M., Jones, H.I. & Smith, T.B. (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology, 10, 2319–2327. http://dx.doi.org/10.1046/j.1365-294X.2001.01339.x

    Swofford, D.L. (2001) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b. Sinauer Associates, Sunderland, MA.

    Valkiūas, G. (2005) Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, Florida, USA, 946 pp.

    Valkiūnas, G., Iezhova, T.A. & Shapoval, A.P. (2003) High prevalence of blood parasites in hawfinch Coccothraustes coccothraustes. Journal of Natural History, 37, 2647–2652. http://dx.doi.org/10.1080/002229302100001033221

    Valkiūnas, G., Križanauskienė, A., Iezhova, T.A., Hellgren, O. & Bensch, S. (2007) Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. Journal of Parasitology, 93, 680–687. http://dx.doi.org/10.1645/GE-1102R.1

    Valkiūnas, G., Iezhova, T.A., Križanauskienė, A., Palinauskas, V. & Bensch, S. (2008a) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology, 94, 1395–1401. http://dx.doi.org/10.1645/GE-1570.1

    Valkiūnas, G., Iezhova T.A., Loiseau, C., Chasar, A., Thomas, B.S. & Sehgal, R.N.M. (2008b) New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitology Research, 103, 1213–1228. http://dx.doi.org/10.1007/s00436-008-1118-x

    Valkiūnas, G., Zehtindjiev, P., Dimitrov, D., Križanauskienė, A., Iezhova, T.A. & Bensch, S. (2008c) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitology Research, 102, 1185–1193. http://dx.doi.org/10.1007/s00436-008-0892-9

    Valkiūnas, G., Santiago-Alarcon, D., Levin, I.I., Iezhova, T.A. & Parker, P.G. (2010a) A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. Journal of Parasitology, 96, 783–792. http://dx.doi.org/10.1645/GE-2442.1

    Valkiūnas, G., Sehgal, R.N.M., Iezhova, T.A. & Hull, A.C. (2010b) Identification of Leucocytozoon toddi group (Haemosporida: Leucocytozoidae), with remarks on the species taxonomy of Leucocytozoids. Journal of Parasitology, 96, 170–177. http://dx.doi.org/10.1645/GE-2109.1

    Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. & Ottosson, U. (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology, 11, 1545–1554. http://dx.doi.org/10.1046/j.1365-294X.2002.01523.x

    Waldenström, J., Bensch, S., Hasselquist, D. & Östman, Ö. (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology, 90, 191–194. http://dx.doi.org/10.1645/GE-3221RN

    Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiūnas, G. & Bensch, S. (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology, 119, 99–110. http://dx.doi.org/10.1016/j.exppara.2007.12.018

    Zehtindjiev, P., Križanauskienė, A., Scebba, S., Dimitrov, D., Valkiūnas, G., Hegemann, A., Tieleman, I.B. & Bensch, S. (2012) Haemosporidian infections in skylarks (Alauda arvensis): a comparative study on the parasite diversity and prevalence in southern Italy and the Netherlands. European Journal of Wildlife Research, 58, 335–44. http://dx.doi.org/10.1007/s10344-011-0586-y