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Type: Articles
Published: 2012-08-28
Page range: 36–46
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Haemoproteus nucleocondensus n. sp. (Haemosporida, Haemoproteidae) from a Eurasian sogbird, the Great Reed Warbler Acrocephalus arundinaceus

Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Biological Station Rybachy of the Zoological Institute, Russian Academy of Sciences, Rybachy, 238535, Kaliningrad Region, Russia
Nature Research Centre, Institute of Ecology, Akademijos 2, LT-08412, Vilnius, Lithuania
Protozoa avian haemosporidians Haemoproteus new species Acrocephalus arundinaceus microscopy PCR barcoding

Abstract

Haemoproteus (Parahaemoproteus) nucleocondensus n. sp. (Haemosporida, Haemoproteidae) is described from aEurasian songbird, the Great Reed Warbler Acrocephalus arundinaceus based on the morphology of its blood stages andpartial sequences of the mitochondrial cytochrome b gene. Transmission of this haemoproteid occurs in Africa, where theGreat Reed Warblers are infected. Due to unclear reasons, its transmission does not occur at European breeding groundsof this bird, resulting in absence of the parasites in juvenile birds before and during seasonal migration. Haemoproteusnucleocondensus can be readily distinguished from other avian haemoproteids by tiny, compact microgametocyte nucleithat are significantly smaller than macrogametocyte nuclei, a rare character of haemosporidian parasites. By thismorphological feature, the new species is similar to Haemoproteus payevskyi, Haemoproteus micronuclearis, andHaemoproteus nucleofascialis. Haemoproteus nucleocondensus can be readily distinguished from both H. payevskyi andH. micronuclearis, primarily due to its numerous growing gametocytes (size greater than erythrocyte nuclei), which donot touch the envelope of erythrocytes along their entire margin; such gametocytes do not develop in Haemoproteuspayevskyi and H. micronuclearis, but present in H. nucleofascialis. However, microgametocyte nuclei are band-like inshape in the latter parasite; that is not a case in H. nucleocondensus. Illustrations of blood stages of the new species aregiven, and morphological and phylogenetic analyses identify the DNA lineages that are associated with these parasites.Genetic distance between cyt b gene sequences of the new species and H. payevskyi, H. micronuclearis, and H.nucleofascialis is 4.4%, 5.9%, and 8.1%, respectively. Cytochrome b gene sequences (GenBank no. JX026901) can be used for bar-coding in studies of H. nucleocondensus.

References

  1. Asghar, M., Hasselquist, D. & Bensch, S. (2011) Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology, 42, 530–537.

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

    Atkinson, C.T., Forrester, D.J. & Greiner, E.C. (1988) Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. Journal of Parasitology, 74, 228–239.

    Atkinson, C. T. & van Riper, C. III. (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye, J. E. & Zuk, M. (Eds.) Bird-parasite interactions: Ecology, evolution, and behaviour. Oxford University Press, Oxford, U.K, pp. 19–48.

    Bennett, G.F. & Campbell, A.G. (1972) Avian Haemoproteidae. I. Description of Haemoproteus fallisi n. sp. and a review of the haemoproteids of the family Turdidae. Canadian Journal of Zoology, 50, 1269–1275.

    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.

    Bensch, S., Waldenström, J., Jonzén, N., Westerdahl, H., Hansson, B., Sejberg, D. & Hasselquist, D. (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology, 76, 112–122.

    Bensch, S., Hellgren, O. & Pérez-Tris, J. (2009) A public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353–1358.

    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.

    Cardona, C.J., Ihejirika, A. & McClellan, L. (2002) Haemoproteus lophortyx infection in bobwhite quail. Avian Diseases, 46, 249–255.

    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 Parasitologica, 55, 201–209.

    Fernández, M., Rojo, M.A., Casanueva, P., Carrión, S., Hernández, M.A. & Campos, F. (2010) High prevalence of haemosporidians in Reed Warbler Acrocephalus scirpaceus and Sedge Warbler Acrocephalus schoenobaenus in Spain. Journal of Ornithology, 151, 27–32.

    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.

    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.

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

    Hasselquist, D., Östman, Ö., Waldenström, J. & Bensch, S. (2007) Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. Journal of Ornithology, 148, 401–409.

    Hellgren, O., Waldenström, J. & Bensch, S. (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology, 90, 797–802.

    Hellgren, O., Križanauskienė, A., Valkiūnas, G. & Bensch, S. (2007) Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida, Haemoproteidae). Journal of Parasitology, 93, 889–893.

    Iezhova, T.A., Valkiūnas, G., Loiseau, C., Smith, T.B. & Sehgal, R.N.M. (2010) Haemoproteus cyanomitrae sp. nov. (Haemosporida: Haemoproteidae) from a widespread african songbird, the Olive sunbird, Cyanomitra olivacea. Journal of Parasitology, 96, 137–143.

    Iezhova, T.A., Dodge, M., Sehgal, R.N.M., Smith, T.B. & Valkiūnas, G. (2011) New avian Haemoproteus species ( Haemosporida: Haemoproteidae) from African birds, with critique of the use of host taxonomic information in haemoproteid classification. Journal of Parasitology, 97, 682–694.

    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.

    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.

    Levin, I. I., Valkiūnas, G., Santiago-Alarcon, D., Cruz, L.L., Iezhova, T. A., ƠBrein, S.L., Hailer, F., Dearborn, D., Schreiber, 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 for Parasitology, 41, 1019–1027.

    Martinsen, E.S., Paperna, I. & Schall, J.J. (2006) Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitology, 133, 279–288.

    Martinsen, E.M., Perkins, S.L. & 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.

    Marzal, A., de Lopes, F., Navarro, C. & Møller, A.P. ( 2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia, 142, 541–545.

    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.

    Merino, S., Hennicke, J., Martínez, J., Ludynia, K., Torres, R., Work, T.M., Stroud, S., Masello, J.F. & Quillfeldt, P. (2012) Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology, 98, 388–397.

    Miltgen, F., Landau, I., Ratanaworabhan, N. & Yenbutra, S. (1981) Parahaemoproteus desseri n. sp.; Gamétogonie et schizogonie chez l’hôte naturel: Psittacula roseata de Thailande, et sporogonie expérimentale chez culicoides nubeculosus. Annales de Parasitologie Humaine et Comparée, 56,123–130.

    Møller, A.P. & Nielsen, J.T. (2007) Malaria and risk of predation: a comparative study of birds. Ecology, 88, 871–81.

    Nordling, D., Anderson, M., Zohari, S. & Gustafsson, L. (1998) Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London, B, 265, 1291–1298.

    Olias, P., Wegelin, M., Freter, S., Gruber, A.D. & Klopfleisch, R. (2011) Avian malaria deaths in parrots, Europe. Emerging Infectious Diseases, 17, 950–952.

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

    Perkins, S.L. & Schall, J.J. (2002) A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88, 972–978.

    Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Ricklefs, R.E., Fallon, S.M. & Bermingham, E. (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology, 53, 111–119.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Sambrook, J., Fritch, F.J. & Maniatis, T. (2002) Molecular clooning, a labaratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.

    Santiago-Alarcon, D., Outlaw, D.C., Ricklefs, R.E. & Parker. P.G. (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology, 40, 463–470.

    Shurulinkov, P. & Chakarov, N. (2006) Prevalence of blood parasites in different local populations of reed warbler (Acrocephalus scirpaceus) and Great Reed Warbler (Acrocephalus arundinaceus). Parasitology Research, 99, 588–592.

    Shurulinkov, P. & Ilieva, M. (2009) Spatial and temporal differences in the blood parasite fauna of passerine birds during the spring migration in Bulgaria. Parasitology Research, 104, 1453–1458.

    Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

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

    Valkiūnas, G. (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Molecular Ecology, 20, 3084–3086.

    Valkiūnas, G. & Iezhova, T.A. (2004) Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology, 90, 194–196.

    Valkiūnas, G., Iezhova, T. & Chernetsov, N.S. (1994) Haemoproteus payevskyi sp. n. (Haemosporidia: Haemoproteidae) from reed warbler Acrocephalus scirpaceus (Passeriformes). Parazitologiya (St. Petersburg), 28(6), 469–474 (in Russian).

    Valkiūnas, G., Iezhova, T.A., Križanauskienė, A., Palinauskas, V., Sehgal, R.N.M. & Bensch, S. (2008) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology, 94, 1395–1401.

    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.

    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.