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Molecular characterisation of three avian haemoproteids (Haemosporida, Haemoproteidae), with the description of Haemoproteus (Parahaemoproteus) palloris n. sp.

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Abstract

DNA barcoding (molecular characterisation) is a useful tool for describing the taxonomy and systematics of organisms. Over 250 species of avian haemosporidian parasites have been described using morphological characters, yet molecular techniques based on polymerase chain reaction (PCR) suggest this diversity is underestimated. Moreover, molecular techniques are particularly useful for the detection of chronic infections and tissue stages of these parasites. Species delimitation is problematic among haemosporidians, and many questions about the mechanisms and patterns of speciation, host specificity and pathogenicity are still unresolved. Accumulation of additional genetic and morphological information is needed to approach these questions. Here, we combine microscopic examination with PCR-based methods to develop molecular characterisation of Haemoproteus (Parahaemoproteus) manwelli Bennett, 1978 and Haemoproteus (Parahaemoproteus) gavrilovi Valkiūnas & Iezhova, 1990, both of which parasitise the bee-eater Merops apiaster L. We also describe a new species, Haemoproteus (Parahaemoproteus) palloris n. sp., from the blood of the willow warbler Phylloscopus trochilus (L.). We performed phylogenetic analyses with a set of mitochondrial cytochrome b (cyt b) gene lineages, which have been linked to parasite morphospecies and are available in the MalAvi database. Our findings show that morphological characters, which have been traditionally used in the description of haemosporidians, exhibit phylogenetic congruence. This study contributes to a better understanding of avian haemosporidian diversity and provides new molecular markers (cyt b and apicoplast gene sequences) for the diagnostics of inadequately investigated haemosporidian infections.

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References

  • Atkinson, C. T. (2008). Haemoproteus. In C. T. Atkinson, N. J. Thomas, & B. C. Hunter (Eds), Parasitic diseases of wild birds. Ames, IA: Wiley-Blackwell, pp. 13–35.

    Chapter  Google Scholar 

  • Bairlein, F. (1995). Manual of field methods. European-African songbird migration network. Institut für Vogelforschung, Wilhelmshaven.

  • Beadell, J. S., Covas, R., Gebhard, C., Ishtiaq, F., Melo, M., Schmidt, K., et al. (2009). Host associations and evolutionary relationships of avian blood parasites from West Africa. International Journal for Parasitology, 39, 257–266.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beadell, J. S., Gering, E., Austin, J., Dumbacher, J. P., Peirce, M. A., Pratt, T. K., et al. (2004). Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology, 13, 3829–3844.

    Article  PubMed  Google Scholar 

  • Bennett, G. F. (1978). Avian Haemoproteidae. 8. The haemoproteids of the bee-eater family (Meropidae). Canadian Journal of Zoology, 56, 1721–1725.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bensch, S., & Åkesson, S. (2003). Temporal and spatial variation of hematozoans in Scandinavian willow warblers. Journal of Parasitology, 89, 388–391.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H., & Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society B: Biological Sciences, 267(1452), 1583–1589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop, M. A., & Bennett, G. F. (1989). The haemoproteids of the avian order Strigiformes. Canadian Journal of Zoology, 67, 2676–2684.

    Article  Google Scholar 

  • Bukauskaitė, D., Žiegytė, R., Palinauskas, V., Iezhova, T. A., Dimitrov, D., Ilgūnas, M., et al. (2015). Biting midges (Culicoides, Diptera) transmit Haemoproteus parasites of owls: evidence from sporogony and molecular phylogeny. Parasites & Vectors, 8, 303.

    Article  Google Scholar 

  • Cannell, B. L., Krasnec, K. V., Campbell, K., Jones, H. I., Miller, R. D., & Stephens, N. (2013). The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor). Veterinary Parasitology, 197, 74–84.

    Article  CAS  PubMed  Google Scholar 

  • Clark, N. J., Adlard, R. D., & Clegg, S. M. (2015). Molecular and morphological characterization of Haemoproteus (Parahaemoproteus) ptilotis, a parasite infecting Australian honeyeaters (Meliphagidae), with remarks on prevalence and potential cryptic speciation. Parasitology Research, 114, 1921–1928.

    Article  PubMed  Google Scholar 

  • Clark, N. J., Clegg, S. M., & Lima, M. R. (2014). A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology, 44, 329–338.

    Article  PubMed  Google Scholar 

  • Coral, A. A., Valkiūnas, G., González, A. D., & Matta, N. E. (2015). In vitro development of Haemoproteus columbae (Haemosporida: Haemoproteidae), with perspectives for genomic studies of avian haemosporidian parasites. Experimental Parasitology, 157, 163–169.

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove, C. L., Day, K. P., & Sheldon, B. C. (2006). Coamplification of Leucocytozoon by PCR diagnostic tests for avian malaria: a cautionary note. Journal of Parasitology, 92, 1362–1365.

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove, C. L., Wood, M. J., Day, K. P., & Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology, 77, 540–548.

    Article  PubMed  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimitrov, D., Zehtindjiev, P., Bensch, S., Ilieva, M., Iezhova, T. A., & Valkiūnas, G. (2014). Two new species of Haemoproteus Kruse, 1890 (Haemosporida, Haemoproteidae) from European birds, with emphasis on DNA barcoding for detection of haemosporidians in wildlife. Systematic Parasitology, 87, 135–151.

    Article  PubMed  Google Scholar 

  • Drovetski, S. V., Aghayan, S. A., Mata, V. A., Lopes, R. J., Mode, N. A., Harvey, J. A., & Voelker, G. (2014). Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Molecular Ecology, 23, 3322–3329.

    Article  PubMed  Google Scholar 

  • Fallon, S. M., Ricklefs, R. E., Swanson, B. L., & Bermingham, E. (2003). Detecting avian malaria: an improved Polymerase Chain Reaction diagnostic. Journal of Parasitology, 89, 1044–1047.

    Article  CAS  PubMed  Google Scholar 

  • Feldman, R. A., Freed, L. A., & Cann, R. L. (1995). A PCR test for avian malaria in Hawaiian birds. Molecular Ecology, 4, 663–673.

    Article  CAS  PubMed  Google Scholar 

  • Ferraguti, M., Martínez-de la Puente, J., Muñoz, J., Roiz, D., Ruiz, S., Soriguer, R., & Figuerola, J. (2013). Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PLoS One, 8, e66237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godfrey, R. D., Fedynich, A. M., & Pence, D. B. (1987). Quantification of haematozoa in blood smears. Journal of Wildlife Diseases, 23, 558–565.

    Article  PubMed  Google Scholar 

  • González, A. D., Lotta, I. A., García, L. F., Moncada, L. I., & Matta, N. E. (2015). Avian haemosporidians from Neotropical highlands: Evidence from morphological and molecular data. Parasitology International, 64, 48–59.

    Article  PubMed  Google Scholar 

  • Greiner, E. C., Mandal, A. K., & Nandi, N. C. (1977). Haemoproteus bennetti sp. n. and a review of the Haemoproteus from Picidae. Journal of Parasitology, 63, 651–656.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hellgren, O., Atkinson, C. T., Bensch, S., Albayrak, T., Dimitrov, D., Ewen, J. G., et al. (2014). Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography, 38, 842–850.

    Article  Google Scholar 

  • 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, 889–896.

    Article  CAS  PubMed  Google Scholar 

  • Hellgren, O., Kutzer, M., Bensch, S., Valkiūnas, G., & Palinauskas, V. (2013). Identification and characterization of the merozoite surface protein 1 (msp1) gene in a host-generalist avian malaria parasite, Plasmodium relictum (lineages SGS1 and GRW4) with the use of blood transcriptome. Malaria Journal, 12, 381.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 a critique of the use of host taxonomic information in hemoproteid classification. Journal of Parasitology, 97, 682–694.

    Article  PubMed  Google Scholar 

  • Ishtiaq, F., Gering, E., Rappole, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., et al. (2007). Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases, 43, 382–398.

    Article  PubMed  Google Scholar 

  • Jarvis, E. D., Mirarab, S., Aberer, A. J., Li, B., Houde, P., Li, C., et al. (2014). Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346, 1320–1331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karadjian, G., Puech, M.-P., Duval, L., Chavatte, J.-M., Snounou, G., & Landau, I. (2013). Haemoproteus syrnii in Strix aluco from France: morphology, stages of sporogony in a hippoboscid fly, molecular characterization and discussion on the identification of Haemoproteus species. Parasite (Paris, France), 20, 32.

  • Križanauskienė, A., Hellgren, O., Kosarev, V., Sokolov, L., Bensch, S., & Valkiunas, G. (2006). Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome B gene sequences. Journal of Parasitology, 92, 1319–1324.

    Article  PubMed  Google Scholar 

  • Križanauskienė, A., Iezhova, T. A., Sehgal, R. N. M., Carlson, J. S., Palinauskas, V., Bensch, S., & Valkiūnas, G. (2013). Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons. Zootaxa, 3613, 85–94.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Lauron, E. J., Oakgrove, K. S., Tell, L. A., Biskar, K., Roy, S. W., & Sehgal, R. N. M. (2014). Transcriptome sequencing and analysis of Plasmodium gallinaceum reveals polymorphisms and selection on the apical membrane antigen-1. Malaria Journal, 13, 382.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, J., Wirtz, R. A., McConkey, G. A., Sattabongkot, J., Waters, A. P., Rogers, M. J., & McCutchan, T. F. (1995). Plasmodium genus-conserved primers for species identification and quantitation. Experimental Parasitology, 81, 182–190.

    Article  CAS  PubMed  Google Scholar 

  • Loiseau, C., Iezhova, T., Valkiūnas, G., Chasar, A., Hutchinson, A., Buermann, W., et al. (2010). Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology, 96, 21–29.

    Article  PubMed  Google Scholar 

  • Mantilla, J. S., González, A. D., Valkiūnas, G., Moncada, L. I., & Matta, N. E. (2013). Description and molecular characterization of Plasmodium (Novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland of Colombia. Parasitology Research, 112, 4193–4204.

    Article  PubMed  Google Scholar 

  • Martínez, J., Martínez-de la Puente, J., Herrero, J., Del Cerro, S., Lobato, E., Rivero-de Aguilar, J., et al. (2009). A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitology, 136, 713–722.

    Article  PubMed  Google Scholar 

  • Martinsen, E. S., 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.

    Article  CAS  PubMed  Google Scholar 

  • Matta, N. E., Pacheco, M. A., Escalante, A. A., Valkiūnas, G., Ayerbe-Quiñones, F., & Acevedo-Cendales, L. D. (2014). Description and molecular characterization of Haemoproteus macrovacuolatus n. sp. (Haemosporida, Haemoproteidae), a morphologically unique blood parasite of black-bellied whistling duck (Dendrocygna autumnalis) from South America. Parasitology Research, 113, 2991–3000.

    Article  PubMed  Google Scholar 

  • Merino, S., Hennicke, J., Martínez, J., Ludynia, K., Torres, R., Work, T. M., et al. (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.

    Article  PubMed  Google Scholar 

  • Olias, P., Wegelin, M., Zenker, W., Freter, S., Gruber, A. D., & Klopfleisch, R. (2011). Avian malaria deaths in parrots, Europe. Journal of Infectious Diseases, 171, 950–952.

    Google Scholar 

  • Ondrejicka, D. A., Locke, S. A., Morey, K., Borisenko, A. V., & Hanner, R. H. (2014). Status and prospects of DNA barcoding in medically important parasites and vectors. Trends in Parasitology, 30, 582–591.

    Article  CAS  PubMed  Google Scholar 

  • Outlaw, D. C., & Ricklefs, R. E. (2014). Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era. Parasitology, 2, 1–10.

    Google Scholar 

  • Palinauskas, V., Iezhova, T. A., Križanauskienė, A., Markovets, M. Y., Bensch, S., & Valkiūnas, G. (2013a). Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitology International, 62, 358–363.

    Article  CAS  PubMed  Google Scholar 

  • Palinauskas, V., Križanauskienė, A., Iezhova, T. A., Bolshakov, C. V., Jönsson, J., Bensch, S., & Valkiūnas, G. (2013b). A new method for isolation of purified genomic DNA from haemosporidian parasites inhabiting nucleated red blood cells. Experimental Parasitology, 133, 275–280.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Poulin, R., & Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology, 24, 24–28.

    Article  CAS  PubMed  Google Scholar 

  • Richard, F. A., Sehgal, R. N. M., Jones, H. I., & Smith, T. B. (2002). A Comparative Analysis of PCR-Based Detection Methods for Avian Malaria. Journal of Parasitology, 88, 819–822.

    Article  CAS  PubMed  Google Scholar 

  • Richardson, D. S., Jury, F. L., Blaakmeer, K., Komdeur, J., & Burke, T. (2001). Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Molecular Ecology, 10, 2263–2273.

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs, R. E., & Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society B: Biological Sciences, 269, 885–892.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ricklefs, R. E., Outlaw, D. C., Svensson-Coelho, M., Medeiros, M. C. I., Ellis, V. A., & Latta, S. (2014). Species formation by host shifting in avian malaria parasites. Proceedings of the National Academy of Sciences of the United States of America, 111, 14816–14821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Silveira, P., Belo, N. O., Lacorte, G. A., Kolesnikovas, C. K. M., Vanstreels, R. E. T., Steindel, M., et al. (2013). Parasitological and new molecular-phylogenetic characterization of the malaria parasite Plasmodium tejerai in South American penguins. Parasitology International, 62, 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Svensson, L. (1992). Identification Guide to European Passerines (4th ed., p. 368). Stockholm: British Trust for Ornithology.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular biology and evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valkiūnas, G. (2005). Avian malaria parasites and other haemosporidia (p. 946). New: CRC PRESS Boca Raton.

    Google Scholar 

  • Valkiūnas, G., Bensch, S., Iezhova, T. A., Križanauskienė, A., Hellgren, O., & Bolshakov, C. V. (2006). Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology, 92, 418–422.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Valkiūnas, G., Iezhova, T. A., Loiseau, C., Chasar, A., Smith, T. B., & 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.

    Article  PubMed  Google Scholar 

  • Valkiūnas, G., Iezhova, T. A., Loiseau, C., & Sehgal, R. N. M. (2009). Nested cytochrome B polymerase chain reaction diagnostics detect sporozoites of hemosporidian parasites in peripheral blood of naturally infected birds. Journal of Parasitology, 95, 1512–1515.

    Article  PubMed  Google Scholar 

  • Valkiūnas, G., Kazlauskienė, R., Bernotienė, R., Palinauskas, V., & Iezhova, T. A. (2013). Abortive long-lasting sporogony of two Haemoproteus species (Haemosporida, Haemoproteidae) in the mosquito Ochlerotatus cantans, with perspectives on haemosporidian vector research. Parasitology Research, 112, 2159–2169.

    Article  PubMed  Google Scholar 

  • Valkiūnas, G., Križanauskienė, A., Iezhova, T. A., Hellgren, O., & Bensch, S. (2007). Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylvid birds, with a description of Haemoproteus parabelopolskyi sp. nov. Journal of Parasitology, 93, 680–687.

    Article  PubMed  Google Scholar 

  • Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaitė, D., Dimitrov, D., Bernotienė, R., et al. (2014). Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitology Research, 113, 2251–2263.

    Article  PubMed  Google Scholar 

  • Ventim, R., Morais, J., Pardal, S., Pérez-Tris, J., Ramos, J. A., & Mendes, L. (2012). Host-parasite associations and host-specificity in haemoparasites of reed bed passerines. Parasitology, 139, 310–316.

    Article  PubMed  Google Scholar 

  • Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D., & Ottusson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Biology and Evolution, 11, 1545–1554.

    Google Scholar 

  • Waldenström, J., Bensch, S., & Ostman, O. (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.

    Article  PubMed  Google Scholar 

  • WHO. (2014). World Malaria Report 2014. Geneva. http://apps.who.int/iris/bitstream/10665/144852/2/9789241564830_eng.pdf?ua=1. Accessed 14 January 2015.

  • Wood, M. J., Childs, D. Z., Davies, A. S., Hellgren, O., Cornwallis, C. K., Perrins, C. M., & Sheldon, B. C. (2013). The epidemiology underlying age-related avian malaria infection in a long-lived host: the mute swan Cygnus olor. Journal of Avian Biology, 44, 12.

    Article  Google Scholar 

  • Zehtindjiev, P., Ivanova, K., Mariaux, J., & Georgiev, B. B. (2013). First data on the genetic diversity of avian haemosporidians in China: cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Gansu Province. Parasitology Research, 112, 3509–3515.

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Karina Ivanova for her help during microscopic examination of material and to Strahil Peev, Konstantin Valchev, Stefan Braianavsci and Iovelina Bedeva for their help in the field work. This is report number 59 for Kalimok field station.

Funding

This study was supported by the European Union Structural Funds project “Postdoctoral Fellowship Implementation in Lithuania” (VP-3.1-ŠMM-01-V-02-004) and the postdoctoral project grant DO02-277 to MI from the Bulgarian Science Fund.

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Authors and Affiliations

  1. Institute of Ecology, Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania

    Dimitar Dimitrov, Tatjana A. Iezhova & Gediminas Valkiūnas

  2. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113, Sofia, Bulgaria

    Dimitar Dimitrov, Pavel Zehtindjiev, Aneliya Bobeva, Mihaela Ilieva, Miroslava Kirilova & Kiril Bedev

  3. Department of Biology, Lund University, Ecology Building, 22362, Lund, Sweden

    Christoffer Sjöholm

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  1. Dimitar Dimitrov
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Correspondence to Dimitar Dimitrov.

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All applicable institutional, national and international guidelines for the care and use of animals were followed. The research was conducted under permissions 213/26.06.2009 and 433/07.03.2012 issued from the Ministry of Evironment and Waters of Bulgaria.

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Dimitrov, D., Iezhova, T.A., Zehtindjiev, P. et al. Molecular characterisation of three avian haemoproteids (Haemosporida, Haemoproteidae), with the description of Haemoproteus (Parahaemoproteus) palloris n. sp.. Syst Parasitol 93, 431–449 (2016). https://doi.org/10.1007/s11230-016-9638-8

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