Parasitology Research

, 103:1213 | Cite as

New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification

  • Gediminas ValkiūnasEmail author
  • Tatjana A. Iezhova
  • Claire Loiseau
  • Anthony Chasar
  • Thomas B. Smith
  • Ravinder N. M. Sehgal
Original Paper


Plasmodium (Novyella) megaglobularis n. sp. was recorded in the olive sunbird Cyanomitra olivacea, and Plasmodium (Novyella) globularis n. sp. and Haemoproteus (Parahaemoproteus) vacuolatus n. sp. were found in the yellow-whiskered greenbul Andropadus latirostris in rainforests of Ghana and Cameroon. These parasites are described based on the morphology of their blood stages and a segment of the mitochondrial cytochrome 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 deoxyribonucleic acid (DNA) lineages closely related to these parasites. Traditional taxonomy of avian pigment-forming haemosporidians of the families Plasmodiidae and Haemoproteidae is discussed based on the recent molecular phylogenies of these parasites. We conclude that further work to increase the number of precise linkages between haemosporidian DNA sequences and their corresponding morphospecies is needed before revising the current classification of haemosporidians. This study emphasises the value of both the polymerase chain reaction and microscopy in the identification of avian haemosporidian parasites.


Plasmodium Infected Erythrocyte Pigment Granule Mature Erythrocyte Haemosporidian Parasite 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are grateful to Dr. Alan Warren, Natural History Museum, London, for providing the type material of P. rouxi and P. bertii. We would like to thank Augusutus Asamoah and Dr. Erasmus Owusu of the Ghana Wildlife Society for support 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.


  1. 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 50:1269–1275PubMedCrossRefGoogle Scholar
  2. Bennett GF, Peirce MA (1990) The haemoproteids of the avian orders Musophagiformes (the turacos) and Trogoniformes (the trogons). Can J Zool 68:2465–2467CrossRefGoogle Scholar
  3. Bennett GF, Garnham PCC, Fallis AM (1965) On the status of the genera Leucocytozoon Ziemann, 1898 and Haemoproteus Kruse, 1890 (Haemosporidia: Leucocytozoidae and Haemoproteidae). Can J Zool 43:927–932PubMedCrossRefGoogle Scholar
  4. 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 58:1617–1621PubMedGoogle Scholar
  5. 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 15:1–244Google Scholar
  6. Borrow N, Demey R (2005) Birds of Western Africa. Princeton University Press, Princeton, NJGoogle Scholar
  7. Corradetti A, Garnham PCC, Laird M (1963) New classification of the avian malaria parasites. Parassitologia 5:1–4Google Scholar
  8. Fallon S, Bermingham E, Ricklefs E (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615PubMedGoogle Scholar
  9. Gabaldon A, Ulloa G (1978) Subespecie de Haemoproteus rotundus Oliger, 1956 (Haemosporina: Haemoproteidae) presente en Venezuela. Bol Dir Malariol San Amb 18:165–174Google Scholar
  10. Gabaldon A, Ulloa G (1981) A new species of the subgenus Novyella (Haemosporina, Plasmodiidae) from Aramides cajanea (Gruiformes, Rallidae). In: Canning EV (ed) Parasitological topics. A presentation volume to P. C. C. Garnham on the occasion of his 80th birthday, Special Publication no. 1. Allen Press, Lawrence, pp 100–105Google Scholar
  11. Garnham PCC (1966) Malaria parasites and other Haemosporidia. Blackwell, OxfordGoogle Scholar
  12. Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565PubMedGoogle Scholar
  13. 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 93:889–896PubMedCrossRefGoogle Scholar
  14. 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 91:472–474PubMedCrossRefGoogle Scholar
  15. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  16. Levine ND, Campbell GR (1971) A check-list of the species of the genus Haemoproteus (Apicomplexa, Plasmodiidae). J Protozool 18:475–484PubMedGoogle Scholar
  17. 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 134:483–490PubMedCrossRefGoogle Scholar
  18. 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 Phyl Evol 47:261–273CrossRefGoogle Scholar
  19. Nylander JAA (2004) mrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Software available at:
  20. 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 1626:39–50Google Scholar
  21. Pérez-Tris J, Bensch S (2005) Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131:1–9CrossRefGoogle Scholar
  22. Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:972–978PubMedGoogle Scholar
  23. Rashdan NA (1998) Role of Pseudolynchia canariensis in the transmission of Haemoproteus turtur from the migrant Streptopelia turtur to new bird host in Egypt. J Egypt Soc Parasitol 28:221–228PubMedGoogle Scholar
  24. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  25. Sehgal RNM, Lovette IJ (2003) Molecular evolution of three avian neurotrophin genes: Implications for proregion functional constraints. J Mol Evol 57:335–342PubMedCrossRefGoogle Scholar
  26. Sehgal RNM, Jones HI, Smith TB (2001) Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Mol Ecol 10:2319–2327PubMedCrossRefGoogle Scholar
  27. Sehgal RNM, Jones HI, Smith TB (2005) Blood parasites of some West African birds. J Vet Med Sci 67:295–301PubMedCrossRefGoogle Scholar
  28. 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 92:375–379PubMedCrossRefGoogle Scholar
  29. Sehgal RNM, Valkiūnas G, Iezhova TA, Smith TB (2006b) Blood parasites of chickens in Uganda and Cameroon with molecular description of Leucocytozoon schoutedeni and Trypanosoma gallinarum. J Parasitol 92:1336–1343PubMedCrossRefGoogle Scholar
  30. Sergent E, Sergent E, Catanei A (1928) Sur un parasite nouveau du paludisme des oiseaux. C R Hebd Séances Acad Sci Paris 186:809–811Google Scholar
  31. Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774PubMedCrossRefGoogle Scholar
  32. Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton, FLGoogle Scholar
  33. Valkiūnas G, Liutkevičius G, Iezhova TA (2002) Complete development of three species of Haemoproteus (Haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). J Parasitol 88:864–868PubMedGoogle Scholar
  34. 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 92:418–422PubMedCrossRefGoogle Scholar
  35. Valkiūnas G, Križanauskienė A, Iezhova TA, Hellgren O, Bensch S (2007a) Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. J Parasitol 93:680–687PubMedCrossRefGoogle Scholar
  36. Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S (2007b) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitol Res 100:1311–1322PubMedCrossRefGoogle Scholar
  37. Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs RE (2008a) Parasite misidentifications in GenBank: how to minimise their number? Trends Parasitol 24:247–248PubMedCrossRefGoogle Scholar
  38. Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Bensch S (2008b) In vitro hybridization of Haemoproteus spp.: an experimental approach for direct investigation of reproductive isolation of parasites. J Parasitol 94 (in press)Google Scholar
  39. Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Sehgal RNM, Bensch S (2008c) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94 (in press)Google Scholar
  40. 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 102:1185–1193PubMedCrossRefGoogle Scholar
  41. 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 90:191–194PubMedCrossRefGoogle Scholar
  42. Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 96:90–94PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Gediminas Valkiūnas
    • 1
    Email author
  • Tatjana A. Iezhova
    • 1
  • Claire Loiseau
    • 2
  • Anthony Chasar
    • 2
  • Thomas B. Smith
    • 3
  • Ravinder N. M. Sehgal
    • 2
  1. 1.Institute of EcologyVilnius UniversityVilniusLithuania
  2. 2.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  3. 3.Center for Tropical ResearchUniversity of California, Los AngelesLos AngelesUSA

Personalised recommendations