Description, molecular characterization, and patterns of distribution of a widespread New World avian malaria parasite (Haemosporida: Plasmodiidae), Plasmodium (Novyella) homopolare sp. nov.

Abstract

Plasmodium (Novyella) homopolare, a newly described Plasmodium species, was found in a wide range of Passeriformes species in California, USA, and Colombia. This parasite infected more than 20 % of the sampled bird community (N = 399) in California and was found in 3.6 % of birds sampled (N = 493) in Colombia. Thus far, it has been confirmed in North and South America where it is present in numerous species of migratory and resident birds from six families. Based on 100 % matches, or near-100 % matches (i.e., ≤2-nucleotide difference), to DNA sequences previously deposited in GenBank, this parasite is likely also distributed in the Eastern USA, Central America, and the Caribbean. Here, we describe the blood stages of P. homopolare and its mtDNA cytochrome b sequence. P. homopolare belongs to the subgenus Novyella and can be readily distinguished from the majority of other Novyella species, primarily, by the strictly polar or subpolar position of meronts and advanced trophozoites in infected erythrocytes. We explore possible reasons why this widespread parasite has not been described in earlier studies. Natural malarial parasitemias are usually light and co-infections predominate, making the parasites difficult to detect and identify to species when relying exclusively on microscopic examination of blood films. The combined application of sequence data and digital microscopy techniques, such as those used in this study, provides identifying markers that will facilitate the diagnosis of this parasite in natural avian populations. We also address the evolutionary relationship of this parasite to other species of Plasmodium using phylogenetic reconstruction.

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References

  1. Atkinson CT (2008) Chapter 3. Avian malaria. In Parasitic diseases of wild birds, 1st edn. Wiley-Blackwell, Iowa, pp 35–53

    Google Scholar 

  2. Basto N, Rodríguez OA, Marinkelle CJ, Gutierrez R, Matta N (2006) Haemoatozoa in birds from La Macarena National Natural Park (Colombia). Caldasia 28(2):371–377

    Google Scholar 

  3. Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 3:3829–3844

    Article  Google Scholar 

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

  5. Bennett GF, Borrero JI (1976) Blood parasites of some birds from Colombia. J Wildl Dis 12:454–458

    CAS  PubMed  Article  Google Scholar 

  6. Bennett GF, Whitt H, White H (1980) Blood parasites of some Jamaican birds. J Wildl Dis 16:29–38

    CAS  PubMed  Article  Google Scholar 

  7. Bensch S, Sternman M, Hasselquist D, Ostman O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B Biol Sci 267:1583–1589

    CAS  Article  Google Scholar 

  8. 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. Mol Ecol 9:1353–1358. doi:10.1111/j.1755-0998.2009.02692.x

    Article  Google Scholar 

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

    Google Scholar 

  10. Cannell BL, Krasnec KV, Campbell K, Jones HI, Miller RD, Stephens N (2013) The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor). Vet Parasitol 197(1-2):74–84. doi:10.1016/j.vetpar.2013.04.025

    CAS  PubMed  Article  Google Scholar 

  11. Clark GW, Swinehart B (1966) Blood protozoa of passerine birds of the Sacramento (Calif.) region. Bull Wildl Dis Assoc 2:53–54

    Article  Google Scholar 

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

    Google Scholar 

  13. Galindo P, Sousa O (1966) Blood parasites of birds from Almirante, Panama, with ecological notes on the hosts. Rev Biol 14(1):27–46

    Google Scholar 

  14. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci: CABIOS 12(6):543–548

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  16. Greiner EC, Bennett GF, White EM, Coombs RF (1975) Distribution of the avian hematozoa of North America. Can J Zool 53:1762–1787

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  18. 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

    CAS  PubMed  Article  Google Scholar 

  19. Herman CM (1938) The relative incidence of blood protozoa in some birds from Cape Cod. Tr Am Micr Soc 47:132–141

    Article  Google Scholar 

  20. Herman CM, Reeves WC, McClure HE, French EM, Hammon W (1954) Studies on avian malaria in vectors and hosts of encephalitis in Kern County, CA: infections in avian hosts. Am J Trop Med Hyg 3:676–695

    CAS  PubMed  Google Scholar 

  21. Herms WB, Kadner CG, Galindo P, Armstrong DF (1939) Blood parasites of California birds. J Parasitol 25(6):511–512

    Article  Google Scholar 

  22. Hewitt R (1940) Studies on blood protozoa obtained from Mexican wild birds. J Parasitol 26(4):287–295

    Article  Google Scholar 

  23. Ilgūnas M, Palinauskas V, Iezhova TA, Valkiūnas G (2013) Molecular and morphological characterization of two avian malaria parasites (Haemosporida: Plasmodiidae), with description of Plasmodium homonucleophilum n. sp. Zootaxa 3666(1):49–61

    Article  Google Scholar 

  24. Levin II, Valkiūnas G, Iezhova TA, O’Brien SL, Parker PG (2012) Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the Swallow-tailed gull (Lariidae), with remarks on the host range of Hippoboscid-transmitted avian hemoproteids. J Parasitol 98(4):847–854

    PubMed  Article  Google Scholar 

  25. Loiseau C, Iezhova T, Valkiūnas G, Chaser A, Hutchinson W, Buermann T, Smith TB, Sehgal RNM (2010) Spatial variation of hemosporidian parasite infection in African rainforest bird species. J Parasitol 96:21–29

    PubMed  Article  Google Scholar 

  26. Mantilla JS, González AD, Valkiūnas G, Moncada LI, Matta NE (2013a) Description and molecular characterization of Plasmodium (Novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland Colombia. Parasitol Res 112:4193–4204

    PubMed  Article  Google Scholar 

  27. Mantilla JS, Matta NE, Pacheco MA, Escalante AA, González AD, Moncada LI (2013b) Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (Great Thrush) in Colombia. J Parasitol 99(4):662–668

    PubMed  Article  Google Scholar 

  28. Manwell RD (1935) How many species of avian malaria parasites are there? Am J Trop Med 15(3):265–283

    Google Scholar 

  29. Martinsen ES, Blumberg BJ, Eisen RJ, Schall JJ (2008) Avian hemosporidian parasites from northern California oak woodland and chaparral habitats. J Wildl Dis 44(2):260–268

    PubMed  Article  Google Scholar 

  30. Matta NE, Basto N, Gutierrez R, Rodríguez OA, Greiner EC (2004) Prevalence of blood parasites in Tyrannidae (flycatchers) in the eastern plains of Colombia. Mem Inst Oswaldo 99(3):271–274

    Article  Google Scholar 

  31. Muñoz E, Ferrer D, Molina RRA (1999) Prevalence of haematozoa in birds of prey in Catalonia, northeast Spain. Vet Rec 144:623–636

    Google Scholar 

  32. Nylander JAA, Ronquist JP, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    PubMed  Article  Google Scholar 

  33. Perkins SL, Austin CC (2009) Four new species of Plasmodium from New Guinea lizards: integrating morphology and molecules. J Parasitol 95:424–433

    CAS  PubMed  Article  Google Scholar 

  34. Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc London 269:885–892

  35. Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in Southern Missouri. Ecol Monogr 75(4):543–559

    Article  Google Scholar 

  36. Rodríguez OA, Matta NE (2001) Blood parasites in some birds from eastern plains of Colombia. Mem Inst Oswaldo Cruz 96:000–000

    Google Scholar 

  37. Rodríguez OA, Moya H, Matta NE (2009) Avian blood parasites in the National Natural Park Chingaza: high Andes of Colombia. Hornero 24(1):1–6

    Google Scholar 

  38. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. doi:10.1093/bioinformatics/btg180

    CAS  PubMed  Article  Google Scholar 

  39. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Harbour Laboratory Press, New York, 2222

    Google Scholar 

  40. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

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

    CAS  PubMed  Article  Google Scholar 

  42. Sehgal RNM, Hull AC, Anderson NL, Valkiūnas G, Markovets MJ, Kawamura S, Tell LA (2006) Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporida, Leucocytozoidae) in diurnal raptors. J Parasitol 92(2):375–379

    PubMed  Article  Google Scholar 

  43. Sousa OE, Herman CM (1982) Blood parasites of birds from Chiriqui and Panama provinces in the Republic of Panama. J Wildl Dis 16(2):205–221

    Article  Google Scholar 

  44. Super PE, van Riper C (1995) A comparison of avian hematozoan epizootiology in two California coastal scrub communities. J Wildl Dis 31(4):447–461

    CAS  PubMed  Article  Google Scholar 

  45. Swofford D (2001) PAUP* 4.0. Sinauer Associates

  46. Valkiūnas G, Salaman P, Iezhova TA (2003) Paucity of Hematozoa in Colombian birds. J Wildl Dis 39(2):445–448

    PubMed  Article  Google Scholar 

  47. Valkiūnas G, Iezhova TA, Brooks DR, Hanelt B, Brant SV, Sutherlin ME, Causey D (2004) Additional observations on blood parasites of birds in Costa Rica. J Wildl Dis 40(3):555–561

    PubMed  Article  Google Scholar 

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

    Google Scholar 

  49. 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

    PubMed  Article  Google Scholar 

  50. Valkiūnas G, Iezhova TA, Krizankauskiene A, Palinauskas V, Sehgal RN, Bensch S (2008a) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94(6):1395–1401. doi:10.1645/GE-1570.1

    PubMed  Article  Google Scholar 

  51. Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs R (2008b) Parasite identifications in GenBank: how to minimize their number? Trends Parasitol 24(6):247–248

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  53. Valkiūnas G, Iezhova TA, Loiseau C, Smith TB, Sehgal RNM (2009) 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

    PubMed  Article  Google Scholar 

  54. Valkiūnas G, Sehgal RNM, Iezhova TA, Hull AC (2010) Identification of Leucocytozoon toddi group (Haemosporida: Leucocytozoidae), with remarks on the species taxonomy of Leucocytozoids. J Parasitol 96(1):170–177

    PubMed  Article  Google Scholar 

  55. Valkiūnas G, Ashford RW, Bensch S, Killick-Kendrick R, Perkins S (2011) A cautionary note concerning Plasmodium in apes. Trends Parasitol 27(6):231–232

    PubMed  Article  Google Scholar 

  56. Valkiūnas G, Iezhova TA, Evans E, Carlson JS, Martinez-Gomez JE, Sehgal R (2013) Two new Haemoproteus (Haemosporida: Haemoproteidae) species from columbiform birds. J Parasitol 99(3):513–521

    PubMed  Article  Google Scholar 

  57. 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(1):191–194. doi:10.1645/GE-3221RN

    PubMed  Article  Google Scholar 

  58. Young BE, Garvin MC, McDonald DB (1993) Blood parasites in birds from Monteverde, Costa Rica. J Wildl Dis 29(4):555–560

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

Tatjana Iezhova is acknowledged for technical assistance during preparation of the plate of the illustrations. Work in California was partially supported by a grant from the San Francisco State University Arthur Nelson Scholarship and the San Francisco State University Instructionally Related Activities Grant. Work in Colombia was supported by the Departamento Administrativo de Ciencias, Tecnología e Innovación COLCIENCIAS contract no. 359 and ECOPETROL SA. The authors wish to thank the students belonging to the Host-Parasite Relationship Research Group: avian haemoparasite model of the Universidad Nacional de Colombia and the staff of the Unidad Administrativa Especial del Sistema de Parques Nacionales Naturales for support with field logistics and work, as well as the many field assistants who aided in sampling California birds. R. E. Ricklefs’s studies on avian haemosporidians have been supported by the National Geographic Society, the US National Science Foundation, and the Curators of the University of Missouri, with field and laboratory assistance from many individuals. We thank Holly Archer for contributing data from her research on avian malaria in Costa Rican birds.

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Correspondence to Ravinder N. M. Sehgal.

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Walther, E.L., Valkiūnas, G., González, A.D. et al. Description, molecular characterization, and patterns of distribution of a widespread New World avian malaria parasite (Haemosporida: Plasmodiidae), Plasmodium (Novyella) homopolare sp. nov.. Parasitol Res 113, 3319–3332 (2014). https://doi.org/10.1007/s00436-014-3995-5

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Keywords

  • Plasmodium
  • Avian malaria
  • Hematozoa
  • Morphospecies
  • California
  • Colombia