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New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics

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Abstract

Blood samples from 655 passerine birds were collected in rainforests of Ghana and Cameroon and examined both by microscopy and polymerase chain reaction (PCR)-based techniques. The overall prevalence of Plasmodium spp. was 46.6%, as determined by combining the results of both these diagnostic methods. In comparison to PCR-based diagnostics, microscopic examination of blood films was more sensitive in determining simultaneous infection of Plasmodium spp., but both detection methods showed similar trends of prevalence of malaria parasites in the same study sites. Plasmodium (Novyella) lucens n. sp., Plasmodium (Novyella) multivacuolaris n. sp. and Plasmodium (Novyella) parahexamerium n. sp. were found in the olive sunbird Cyanomitra olivacea (Nectariniidae), yellow-whiskered greenbul Andropadus latirostris (Picnonotidae), and white-tailed alethe Alethe diademata (Turdidae), respectively. These parasites are described based on the morphology of their blood stages and a segment of the mitochondrial cytochrome b (cyt b) gene, which can be used for molecular identification and diagnosis of these species. Illustrations of blood stages of new species are given, and phylogenetic analysis identifies DNA lineages closely related to these parasites. Malaria parasites of the subgenus Novyella with small erythrocytic meronts clearly predominate in African passerines. It is probable that the development of such meronts is a characteristic feature of evolution of Plasmodium spp. in African rainforest birds. Subgeneric taxonomy of avian Plasmodium spp. is discussed based on the recent molecular phylogenies of these parasites. It is concluded that a multi-genome phylogeny is needed before revising the current subgeneric classification of Plasmodium. We supported a hypothesis by Hellgren, Križanauskienė, Valkiūnas, Bensch (J Parasitol 93:889–896, 2007), according to which, haemosporidian species with a genetic differentiation of over 5% in mitochondrial cyt b gene are expected to be morphologically differentiated. This study emphasises the importance of employing both PCR-based and microscopic methods in taxonomic, ecological and evolutionary investigations of avian haemosporidian parasites.

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References

  • Bennett GF, Campbell AG (1972) Avian Haemoproteidae. III. Description of Haemoproteus fallisi n. sp. and a review of the haemoproteids of the family Turdidae. Can J Zool 50:1269–1275

    Article  PubMed  CAS  Google Scholar 

  • Bensch S, Pérez-Tris J, Waldensrtöm J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617–1621

    PubMed  CAS  Google Scholar 

  • Bishop MA, Bennett GF (1992) Host-parasite catalogue of the avian haematozoa: supplement 1; bibliography of the avian blood-inhabiting haematozoa: supplement 2. Mem Univ Newfoundland Occas Pap Biol 15:1–244

    Google Scholar 

  • Borrow N, Demey R (2005) Birds of Western Africa. Princeton University Press, Princeton

    Google Scholar 

  • Corradetti A, Garnham PCC, Laird M (1963) New classification of the avian malaria parasites. Parassitologia 5:1–4

    Google Scholar 

  • Durrant KL, Beadell JS, Ishtiaq F, Graves GR, Olson SL, Gering E, Peirce MA, Milensky CM, Schmidt BK, Gebhard C, Fleischer RC (2006) Avian haematozoa in South America: a comparison of temperate and tropical zones. Ornithol Monogr 60:98–111

    Article  Google Scholar 

  • Fallon SM, Ricklefs RE (2008) Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. J Avian Biol 39:514–522

    Article  Google Scholar 

  • Fallon S, Bermingham E, Ricklefs E (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615

    PubMed  Google Scholar 

  • Garnham PCC (1966) Malaria parasites and other Haemosporidia. Blackwell Scientific, Oxford

    Google Scholar 

  • Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565

    PubMed  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). J Parasitol 93:889–896

    Article  PubMed  CAS  Google Scholar 

  • Huff CG (1935) Plasmodium hexamerium, n. sp. from the blue-bird, inoculable to canaries. Am J Hyg 22:274–277

    Google Scholar 

  • Iezhova TA, Valkiūnas G, Barlein F (2005) Vertebrate host specificity of two avian malaria parasites of subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol 91:472–474

    Article  PubMed  Google Scholar 

  • Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88:153–158

    PubMed  Google Scholar 

  • 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. J Parasitol 92:1319–1324

    Article  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Manwell RD (1935) Plasmodium vaughani (Novy and MacNeal). Am J Hyg 21:180–187

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 switched. Mol Phylogenet Evol 47:261–273

    Article  PubMed  CAS  Google Scholar 

  • Morrison DA (2008) Prospects for elucidation the phylogeny of the Apicomplexa. Parasite 15:191–196

    PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) mrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Software available at: <http://www.ebc.uu.se/systzoo/staff/nylander.html>

  • 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

    Google Scholar 

  • Pérez-Tris J, Bensch S (2005) Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131:1–9

    Article  CAS  Google Scholar 

  • Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:972–978

    PubMed  CAS  Google Scholar 

  • Richards FA, Sehgal RNM, Jones HI, Smith TB (2002) A comparative analysis of PCR-based detection methods for avian malaria. J Parasitol 88:819–822

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sehgal RNM, Lovette IJ (2003) Molecular evolution of three avian neurotrophin genes: Implications for proregion functional constraints. J Mol Evol 57:335–342

    Article  PubMed  CAS  Google Scholar 

  • Sehgal RNM, Jones HI, Smith TB (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Mol Ecol 10:2319–2327

    Article  PubMed  CAS  Google Scholar 

  • Sehgal RNM, Jones HI, Smith TB (2005) Blood parasites of some West African birds. J Vet Med Sci 67:295–301

    Article  PubMed  Google Scholar 

  • Sehgal RNM, Hull AC, Anderson NL, Valkiūnas G, Markovets MJ, Kawamura S, Tell LA (2006a) Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporida, Leucocytozoidae) in Diurnal Raptors. J Parasitol 92:375–379

    Article  PubMed  Google Scholar 

  • Sehgal RNM, Valkiūnas G, Iezhova TA, Smith TB (2006b) Blood parasites of chickens in Uganda and Cameroon with molecular descriptions of Leucocytozoon schoutedeni and Trypanosoma gallinarum. J Parasitol 92:1336–1343

    Article  PubMed  CAS  Google Scholar 

  • Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774

    Article  PubMed  CAS  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton

    Google Scholar 

  • Valkiūnas G, Bensch S, Iezhova TA, Križanauskienė A, Hellgren O, Bolshakov CV (2006) Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood hemosporidian parasites: microscopy is still essential. J Parasitol 92:418–422

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S (2007) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res 100:1311–1322

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs RE (2008a) Parasite misidentifications in GenBank: how to minimise their number? Trends Parasitol 24:247–248

    Article  PubMed  CAS  Google Scholar 

  • Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Sehgal RNM, Bensch S (2008b) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94 (in press)

  • Valkiūnas G, Iezhova TA, Loiseau C, Chasar A, Thomas BS, Sehgal RNM (2008c) New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitol Res 103:1213–1228

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Zehtindjiev P, Dimitrov D, Križanauskienė A, Iezhova TA, Bensch S (2008d) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res 102:1185–1193

    Article  PubMed  Google Scholar 

  • 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. J Parasitol 90:191–194

    Article  PubMed  Google Scholar 

  • Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 96:90–94

    Article  PubMed  CAS  Google Scholar 

  • 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 read warbler Acrocephalus arundinaceus. Exp Parasitol 119:99–110

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Alan Warren, Natural History Museum, London for providing the type material of P. vaughani and P. hexamerium and Gillian McIntosh, San Francisco State University for consultations on the Latin language. We would like to thank Anthony Chasar, Tom Dietsch and Augustus Asamoah for help in the field. The present study was supported by the joint NSF-NIH (USA) Ecology of Infectious Diseases Program award EF-0430146, the Lithuanian State Science and Studies Foundation and SYNTHESYS. The investigations described herein comply with the current laws of the USA and Lithuania.

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Correspondence to Gediminas Valkiūnas.

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Valkiūnas, G., Iezhova, T.A., Loiseau, C. et al. New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitol Res 104, 1061–1077 (2009). https://doi.org/10.1007/s00436-008-1289-5

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