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Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite



Species of Plasmodium (Plasmodiidae, Haemosporida) are widespread and cause malaria, which can be severe in avian hosts. Molecular markers are essential to detect and identify parasites, but still absent for many avian malaria and related haemosporidian species. Here, we provide first molecular characterization of Plasmodium matutinum, a common agent of avian malaria. This parasite was isolated from a naturally infected thrush nightingale Luscinia luscinia (Muscicapidae). Fragments of mitochondrial, apicoplast and nuclear genomes were obtained. Domestic canaries Serinus canaria were susceptible after inoculation of infected blood, and the long-lasting light parasitemia developed in two exposed birds. Clinical signs of illness were not reported. Illustrations of blood stages of P. matutinum (pLINN1) are given, and phylogenetic analysis identified the closely related avian Plasmodium species. The phylogeny based on partial cytochrome b (cyt b) sequences suggests that this parasite is most closely related to Plasmodium tejerai (cyt b lineage pSPMAG01), a common malaria parasite of American birds. Both these parasites belong to subgenus Haemamoeba, and their blood stages are similar morphologically, particularly due to marked vacuolization of the cytoplasm in growing erythrocytic meronts. Molecular data show that transmission of P. matutinum (pLINN1) occurs broadly in the Holarctic, and the parasite likely is of cosmopolitan distribution. Passeriform birds and Culex mosquitoes are common hosts. This study provides first molecular markers for detection of P. matutinum.

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*Corresponding author: Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania. E-mail:


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Atkinson, C. T., Thomas, N. J. and Hunter, D. B. (2008). Parasitic Diseases of Wild Birds. Wiley-Blackwell, Oxford, UK.
Bennett, G. F., Whiteway, M. and Woodworth-Lynas, C. (1982). A host-parasite catalogue of the avian haematozoa. Memorial University of Newfoundland Occasional Papers in Biology 5, 1243.
Bensch, S., Stjernman, M., Hasselquist, D., Östman, Ö., Hansson, B., Westerdahl, H. and 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 London B 276, 15831589.
Bensch, S., Hellgren, O. and 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, 13531358.
Bensch, S., Canbäck, B., DeBarry, J. D., Johansson, T., Hellgren, O., Kissinger, J. C., Palinauskas, V., Videvall, E. and Valkiūnas, G. (2016). The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biology and Evolution 8, 13611373.
Castro, I., Howe, L., Tompkins, D. M., Barraclough, R. K. and Slaney, D. (2011) Presence and seasonal prevalence of Plasmodium spp. in a rare endemic New Zealand passerine (tieke or Saddleback, Philesturnus carunculatus). Journal of Wildlife Diseases 47, 860867.
Clark, N. J., Clegg, S. M., and Lima, M. R. (2014). A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): New insights from molecular data. International Journal of Parasitology 44, 329338.
Corradetti, A., Neri, I. and Scanga, M. (1960). Segnalazione in Italia di Plasmodium praecox var. matutinum in Turdus iliacus, e separazione di questo plasmodio da Plasmodium praecox come specie distinta: Plasmodium matutinum Huff, 1937. Parassitologia 2, 333343.
Corradetti, A., Morcos, W. M. and Neri, I. (1962). Sulle produzione di forme endoistiocitare nei canarini infettati con il ceppo italiano di Plasmodium matutinum derivato da Turdus iliacus. Parassitologia 4, 105108.
Corradetti, A., Verolini, F. and Neri, I. (1963). Plasmodium (Haemamoeba) giovannolai n. sp. parassita di Turdus merula . Parassitologia 5, 1118.
Cosgrove, C. L., Wood, M. J., Day, K. P. and Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus . Journal of Animal Ecology 77, 540548.
Desser, S. S. and Bennett, G. F. (1993). The genera Leucocytozoon, Haemoproteus and Hepatocystis . In Parasitic Protozoa (ed. Kreier, J. P. and Baker, J. R.), pp. 273307. Academic, New York, USA.
Dimitrov, D., Iezhova, T. A., Zehtindjiev, P., Bobeva, A., Ilieva, M., Kirilova, M., Bedev, K., Sjöholm, C. and Valkiūnas, G. (2016). Molecular characterisation of three avian haemoproteids (Haemosporida, Haemoproteidae), with the description of Haemoproteus (Parahaemoproteus) palloris n. sp. Systematic Parasitology 93, 431449.
Dinhopl, N., Nedorost, N., Mostegl, M. M., Weissenbacher-Lang, C. and Weissenböck, H. (2015). In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitology Research 114, 14551462.
Donovan, T. A., Schrenzel, M., Tucker, T. A., Pessier, A. P. and Stalis, I. H. (2008). Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases. Journal of Veterinary Diagnostic Investigation 20, 304313.
Drovetski, S. V., Aghayan, S. A., Mata, V. A., Lopes, R. J., Mode, N. A., Harvey, J. A. and Voelker, G. (2014). Does the niche breadth or trade-off hypothesis explain the abundance—occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 33223329.
Ewen, J. G., Bensch, S., Blackburn, T. M., Bonneaud, C., Brown, R., Cassey, P., Clarke, R. H. and Pérez-Tris, J. (2012). Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecology Letters 15, 11121119.
Fast, K. M., Walstrom, V. W. and Outlaw, D. C. (2016). Haemosporidian prevalence and parasitemia in the Tufted titmouse (Baeolophus bicolor). Journal of Parasitology 102, 636642.
Ferraguti, M., Martínez-de la Puente, J., Ruiz, S., Soriguer, R. and Figuerola, J. (2013). On the study of the transmission networks of blood parasites from SW Spain: diversity of avian haemosporidians in the biting midge Culicoides circumscriptus and wild birds. Parasites and Vectors 6, 208.
Gabaldon, A. and Ulloa, G. (1977). Plasmodium (Haemamoeba) tejerai sp. n. del pavo domésstico (Meleagris gallopavo) de Venezuela. Boletin de Malariologia y Salud Ambiental 17, 255273.
Gabaldon, A. and Ulloa, G. (1980). Holoendemicity of malaria: an avian model. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 501507.
Garnham, P. C. C. (1966). Malaria parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford, UK.
Hall, T. A. (1999) BioEdit: a user – friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41, 9598.
Hellgren, O., Križanauskienė, A., Hasselquist, D. and Bensch, S. (2011). Low haemosporidian diversity and one key-host species in a bird malaria community on a mid-Atlantic island (São Miguel, Azores). Journal of Wildlife Diseases 47, 849859.
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon , Plasmodium and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.
Hellgren, O., Waldenström, J., Peréz-Tris, J., Szöllösi, E., Hasselquist, D., Križanauskiene, A., Ottosson, U. and Bensch, S. (2007). Detecting shifts of transmission areas in avian blood parasites — a phylogenetic approach. Molecular Ecology 16, 12811290.
Howe, L., Castro, I. C., Schoener, E. R., Hunter, S., Barraclough, R. K. and Alley, M. R. (2012). Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitology Research 110, 913923.
Iezhova, T. A., Valkiūnas, G. and Bairlein, F. (2005). Vertebrate host specificity of two avian malaria parasites of the subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani . Journal of Parasitology 91, 472474.
Ilgūnas, M., Bukauskaitė, D., Palinauskas, V., Iezhova, T. A., Dinhopl, N., Nedorost, N., Weissenbacher-Lang, C., Weissenböck, H. and Valkiūnas, G. (2016). Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malaria Journal 15, 256.
Kimura, M., Darbro, J. M. and Harrington, L. C. (2010). Avian malaria parasites share congeneric mosquito vectors. Journal of Parasitology 96, 144151.
Lauron, E. J., Oakgrove, K. S., Tell, L. A., Biskar, K., Roy, S. W. and 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.
Levin, I. I., Valkiūnas, G., Iezhova, T. A., O’brien, S. L. and 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, 847854.
Mantilla, J. S., Gonzalez, A. D., Lotta, I. A., Moens, M., Pacheco, M. A., Escalante, A. A., Valkiūnas, G., Moncada, L. I., Pérez-Tris, J. and Matta, N. E. (2016). Haemoproteus erythrogravidus n. sp. (Haemosporida, Haemoproteidae): description and molecular characterization of a widespread blood parasite of birds in South America. Acta Tropica 159, 8394.
Martínez-de la Puente, J., Muñoz, J., Capelli, G., Montarsi, F., Soriguer, R., Arnoldi, D., Rizzoli, A. and Figuerola, J. (2015). Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malaria Journal 14, 32.
Martinsen, E. S., Perkins, S. L. and 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, 261273.
Marzal, A. (2012). Recent advances in studies on avian malaria parasites. In: Malaria Parasites (ed. Okwa, O.), pp. 135158. InTech Company, Rijeka, Croatia.
Mata, V. A., da Silva, L. P., Lopes, R. J. and Drovetski, S. V. (2015). The Strait of Gibraltar poses an effective barrier to host-specialised but not to host-generalised lineages of avian Haemosporidia. International Journal of Parasitology 45, 711719.
Moens, M. A., Valkiūnas, G., Paca, A., Bonaccorso, E., Aguirre, N. and Pérez-Tris, J. (2016). Parasite specialization in a unique habitat: hummingbirds as reservoirs of generalist blood parasites of Andean birds. Journal of Animal Ecology 85, 12341245.
Nilsson, E., Taubert, H., Hellgren, O., Huang, X., Palinauskas, V., Markovets, M. Y., Valkiūnas, G. and Bensch, S. (2016). Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris . Journal of Evolutionary Biology 29, 16491878.
Oakgrove, K. S., Harrigan, R. J., Loiseau, C., Guers, S., Seppi, B. and Sehgal, R. N. (2014). Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. International Journal of Parasitology 44, 717727.
Outlaw, D. C. and Ricklefs, R. E. (2014). Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era. Parasitology 141, 12231232.
Palinauskas, V., Žiegytė, R., Ilgūnas, M., Iezhova, T. A., Bernotienė, R., Bolshakov, C. and Valkiūnas, G. (2015). Description of the first cryptic avian malaria parasite, Plasmodium homocircumflexum n. sp., with experimental data on its virulence and development in avian hosts and mosquitoes. International Journal of Parasitology 45, 5162.
Palinauskas, V., Žiegytė, R., Iezhova, T. A., Ilgūnas, M., Bernotienė, R. and Valkiūnas, G. (2016). Description, molecular characterisation, diagnostics and life cycle of Plasmodium elongatum (lineage pERIRUB01), the virulent avian malaria parasite. International Journal of Parasitology 46, 697707.
Pérez-Tris, J. and Bensch, S. (2005). Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131(Pt 1), 1523.
Perkins, S. L. (2014). Malaria's many mates: past, present and future of the systematics of the order Haemosporida. Journal of Parasitology 100, 1125.
Ricklefs, R. E., Medeiros, M., Ellis, V. A., Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., Soares, L., Fecchio, A., Outlaw, D., Marra, P. P., Latta, S. V., Valkiūnas, G., Hellgren, O., Bensch, S. (2017). Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography 44, 11131123.
Ronquist, F. and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbour Laboratory Press, New York, USA.
Santiago-Alarcon, D., MacGregor-Fors, I., Kühnert, K., Segelbacher, G. and Schaefer, H. M. (2016). Avian haemosporidian parasites in an urban forest and their relationship to bird size and abundance. Urban Ecosystems 19, 331.
Sherman, I. W. (ed.) (1998). Malaria: Parasite Biology, Pathogenesis, and Protection. American Society for Microbiology, Washington, USA.
Sijbranda, D. C. (2015) Host-parasite interactions between Plasmodium species and New Zealand birds: prevalence, parasite load and pathology . A thesis presented in partial fulfilment of the requirements for the degree of Master of Veterinary Science in Wildlife Health at Massey University, Palmerston North, New Zealand.
Sijbranda, D. C., Campbell, J., Gartrell, B. D. and Howe, L. (2016). Avian malaria in introduced, native and endemic New Zealand bird species in a mixed ecosystem. New Zealand Journal of Ecology 40, 7279.
Svoboda, A., Marthinsen, G., Pavel, V., Chutný, B., Turčoková, L., Lifjeld, J. T. and Johnsen, A. (2015). Blood parasite prevalence in the Bluethroat is associated with subspecies and breeding habitat. Journal of Ornithology 156, 371380.
Szöllősi, E., Cichoń, M., Eens, M., Hasselquist, D., Kempenaers, B., Merino, S., Nilsson, J. Å., Rosivall, B., Rytkönen, S., Török, J., Wood, M. J. and Garamszegi, L. Z. (2011). Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. Journal of Evolutionary Biology 24, 20142024.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.
Valkiūnas, G. (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, FL, USA.
Valkiūnas, G. and Iezhova, T. A. (2017). Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malaria Journal 16, 101.
Valkiūnas, G., Kazlauskienė, R., Bernotienė, R., Palinauskas, V. and Iezhova, T. A. (2013 a). Abortive long-lasting sporogony of two Haemoproteus species (Haemosporida, Haemoproteidae) in the mosquito Ochlerotatus cantans, with perspectives on haemosporidian vector research. Parasitology Research 112, 21592169.
Valkiūnas, G., Palinauskas, V., Križanauskienė, A., Bernotienė, R., Kazlauskienė, R. and Iezhova, T. A. (2013 b). Further observations on in vitro hybridization of hemosporidian parasites: patterns of ookinete development in Haemoproteus spp. Journal of Parasitology 99, 124136.
Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaitė, D., Dimitrov, D., Bernotienė, R., Zehtindjiev, P., Ilieva, M. and Iezhova, T. A. (2014). Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitology Research 113, 22512263.
Valkiūnas, G., Ilgūnas, M., Bukauskaitė, D., Žiegytė, R., Bernotienė, R., Jusys, V., Eigirdas, V., Fragner, K., Weissenböck, H. and Iezhova, T. A. (2016). Plasmodium delichoni n. sp.: description, molecular characterisation and remarks on the exoerythrocytic merogony, persistence, vectors and transmission. Parasitology Research 115, 26252636.
Vanstreels, R. E., da Silva-Filho, R. P., Kolesnikovas, C. K., Bhering, R. C., Ruoppolo, V., Epiphanio, S., Amaku, M., Ferreira Junior, F. C., Braga, É. M. and Catão-Dias, J. L. (2015). Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research 46, 30.
Walker, D. and Garnham, P. C. (1972). Aberrant Leucocytozoon infection in parakeets. Veterinary Record 91, 7072.
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus . Molecular Ecology 16, 32633273.


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Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite



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