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Published in: Malaria Journal 1/2020

Open Access 01-12-2020 | Thrush | Research

Geographic and host distribution of haemosporidian parasite lineages from birds of the family Turdidae

Authors: Josef Harl, Tanja Himmel, Gediminas Valkiūnas, Mikas Ilgūnas, Támas Bakonyi, Herbert Weissenböck

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

Haemosporidians (Apicomplexa, Protista) are obligate heteroxenous parasites of vertebrates and blood-sucking dipteran insects. Avian haemosporidians comprise more than 250 species traditionally classified into four genera, Plasmodium, Haemoproteus, Leucocytozoon, and Fallisia. However, analyses of the mitochondrial CytB gene revealed a vast variety of lineages not yet linked to morphospecies. This study aimed to analyse and discuss the data of haemosporidian lineages isolated from birds of the family Turdidae, to visualise host and geographic distribution using DNA haplotype networks and to suggest directions for taxonomy research on parasite species.

Methods

Haemosporidian CytB sequence data from 350 thrushes were analysed for the present study and complemented with CytB data of avian haemosporidians gathered from Genbank and MalAvi database. Maximum Likelihood trees were calculated to identify clades featuring lineages isolated from Turdidae species. For each clade, DNA haplotype networks were calculated and provided with information on host and geographic distribution.

Results

In species of the Turdidae, this study identified 82 Plasmodium, 37 Haemoproteus, and 119 Leucocytozoon lineages, 68, 28, and 112 of which are mainly found in this host group. Most of these lineages cluster in the clades, which are shown as DNA haplotype networks. The lineages of the Leucocytozoon clades were almost exclusively isolated from thrushes and usually were restricted to one host genus, whereas the Plasmodium and Haemoproteus networks featured multiple lineages also recovered from other passeriform and non-passeriform birds.

Conclusion

This study represents the first attempt to summarise information on the haemosporidian parasite lineages of a whole bird family. The analyses allowed the identification of numerous groups of related lineages, which have not been linked to morphologically defined species yet, and they revealed several cases in which CytB lineages were probably assigned to the wrong morphospecies. These taxonomic issues are addressed by comparing distributional patterns of the CytB lineages with data from the original species descriptions and further literature. The authors also discuss the availability of sequence data and emphasise that MalAvi database should be considered an extremely valuable addition to GenBank, but not a replacement.
Appendix
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Literature
1.
go back to reference Valkiūnas G. Avian malaria parasites and other haemosporidia. Boca Raton: CRC Press; 2005. Valkiūnas G. Avian malaria parasites and other haemosporidia. Boca Raton: CRC Press; 2005.
2.
go back to reference Valkiūnas G, Iezhova TA. Keys to the avian malaria parasites. Malar J. 2018;17:1–24. Valkiūnas G, Iezhova TA. Keys to the avian malaria parasites. Malar J. 2018;17:1–24.
3.
go back to reference Bensch S, Stjernman M, Hasselquist D, Örjan Ö, Hannson B, Westerdahl H, et al. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc London Ser B Biol Sci. 2000;267:1583–9. Bensch S, Stjernman M, Hasselquist D, Örjan Ö, Hannson B, Westerdahl H, et al. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc London Ser B Biol Sci. 2000;267:1583–9.
4.
go back to reference Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.PubMed Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.PubMed
5.
go back to reference Waldenström J, Bensch S, Hasselquist D, Östman Ö. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004;90:191–5.PubMed Waldenström J, Bensch S, Hasselquist D, Östman Ö. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004;90:191–5.PubMed
6.
go back to reference Perkins SL, Schall JJ. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol. 2002;88:972–8.PubMed Perkins SL, Schall JJ. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol. 2002;88:972–8.PubMed
7.
go back to reference Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, et al. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol. 2004;13:3829–44.PubMed Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, et al. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol. 2004;13:3829–44.PubMed
8.
go back to reference Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, et al. Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Mol Ecol. 2014;23:3322–9.PubMed Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, et al. Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Mol Ecol. 2014;23:3322–9.PubMed
9.
go back to reference Pacheco MA, Cepeda AS, Bernotienė R, Lotta IA, Matta NE, Valkiūnas G, et al. Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int J Parasitol. 2018;48:657–70.PubMedPubMedCentral Pacheco MA, Cepeda AS, Bernotienė R, Lotta IA, Matta NE, Valkiūnas G, et al. Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int J Parasitol. 2018;48:657–70.PubMedPubMedCentral
10.
go back to reference Bensch S, Hellgren O, Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour. 2009;9:1353–8.PubMed Bensch S, Hellgren O, Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour. 2009;9:1353–8.PubMed
11.
go back to reference Dickinson EC, Christidis L. The Howard and Moore complete checklist of the birds of the world, vol. 2. 4th ed. Eastbourne: Aves Press; 2014. Dickinson EC, Christidis L. The Howard and Moore complete checklist of the birds of the world, vol. 2. 4th ed. Eastbourne: Aves Press; 2014.
12.
go back to reference Sangster G, Alström P, Forsmark E, Olsson U. Multi-locus phylogenetic analysis of Old World chats and flycatchers reveals extensive paraphyly at family, subfamily and genus level (Aves: Muscicapidae). Mol Phylogenet Evol. 2010;57:380–92.PubMed Sangster G, Alström P, Forsmark E, Olsson U. Multi-locus phylogenetic analysis of Old World chats and flycatchers reveals extensive paraphyly at family, subfamily and genus level (Aves: Muscicapidae). Mol Phylogenet Evol. 2010;57:380–92.PubMed
13.
go back to reference Mantilla JS, Matta NE, Pacheco MA, Escalante AA, González AD, Moncada LI. Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (great thrush) in Colombia. J Parasitol. 2013;99:662–8.PubMed Mantilla JS, Matta NE, Pacheco MA, Escalante AA, González AD, Moncada LI. Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (great thrush) in Colombia. J Parasitol. 2013;99:662–8.PubMed
14.
go back to reference Fecchio A, Bell JA, Bosholn M, Vaughan JA, Tkach VV, Lutz HL, et al. An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. J Anim Ecol. 2020;89:423–35.PubMed Fecchio A, Bell JA, Bosholn M, Vaughan JA, Tkach VV, Lutz HL, et al. An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. J Anim Ecol. 2020;89:423–35.PubMed
15.
go back to reference Galen SC, Speer KA, Perkins SL. Evolutionary lability of host associations promotes phylogenetic overdispersion of co-infecting blood parasites. J Anim Ecol. 2019;88:1936–49.PubMed Galen SC, Speer KA, Perkins SL. Evolutionary lability of host associations promotes phylogenetic overdispersion of co-infecting blood parasites. J Anim Ecol. 2019;88:1936–49.PubMed
16.
go back to reference Galen SC, Nunes R, Sweet PR, Perkins SL. Integrating coalescent species delimitation with analysis of host specificity reveals extensive cryptic diversity despite minimal mitochondrial divergence in the malaria parasite genus Leucocytozoon. BMC Evol Biol. 2018;18:128.PubMedPubMedCentral Galen SC, Nunes R, Sweet PR, Perkins SL. Integrating coalescent species delimitation with analysis of host specificity reveals extensive cryptic diversity despite minimal mitochondrial divergence in the malaria parasite genus Leucocytozoon. BMC Evol Biol. 2018;18:128.PubMedPubMedCentral
17.
go back to reference Fecchio A, Pinheiro R, Felix G, Faria IP, Pinho JB, Lacorte GA, et al. Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography (Cop). 2017;41:505–15. Fecchio A, Pinheiro R, Felix G, Faria IP, Pinho JB, Lacorte GA, et al. Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography (Cop). 2017;41:505–15.
18.
go back to reference Fecchio A, Bell JA, Pinheiro RBP, Cueto VR, Gorosito CA, Lutz HL, et al. Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol. 2019;28:2681–93.PubMed Fecchio A, Bell JA, Pinheiro RBP, Cueto VR, Gorosito CA, Lutz HL, et al. Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol. 2019;28:2681–93.PubMed
19.
go back to reference Fecchio A, Wells K, Bell JA, Tkach VV, Lutz HL, Weckstein JD, et al. Climate variation influences host specificity in avian malaria parasites. Ecol Lett. 2019;22:547–57.PubMed Fecchio A, Wells K, Bell JA, Tkach VV, Lutz HL, Weckstein JD, et al. Climate variation influences host specificity in avian malaria parasites. Ecol Lett. 2019;22:547–57.PubMed
20.
go back to reference Lacorte GA, Felix GMF, Pinheiro RRB, Chaves AV, Almeida-Neto G, Neves FS, et al. Exploring the diversity and distribution of neotropical avian malaria parasites–a molecular survey from Southeast Brazil. PLoS ONE. 2013;8:1–9. Lacorte GA, Felix GMF, Pinheiro RRB, Chaves AV, Almeida-Neto G, Neves FS, et al. Exploring the diversity and distribution of neotropical avian malaria parasites–a molecular survey from Southeast Brazil. PLoS ONE. 2013;8:1–9.
21.
go back to reference Oakgrove KS, Harrigan RJ, Loiseau C, Guers S, Seppi B, Sehgal RNM. Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. Int J Parasitol. 2014;44:717–27.PubMed Oakgrove KS, Harrigan RJ, Loiseau C, Guers S, Seppi B, Sehgal RNM. Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. Int J Parasitol. 2014;44:717–27.PubMed
22.
go back to reference Ricklefs RE, Outlaw DC, Svensson-Coelho M, Medeiros MCI, Ellis VA, Latta S. Species formation by host shifting in avian malaria parasites. Proc Natl Acad Sci. 2014;111:14816–21.PubMed Ricklefs RE, Outlaw DC, Svensson-Coelho M, Medeiros MCI, Ellis VA, Latta S. Species formation by host shifting in avian malaria parasites. Proc Natl Acad Sci. 2014;111:14816–21.PubMed
23.
go back to reference Loiseau C, Melo M, Lobato E, Beadell JS, Fleischer RC, Reis S, et al. Insularity effects on the assemblage of the blood parasite community of the birds from the Gulf of Guinea. J Biogeogr. 2017;44:2607–17.PubMedPubMedCentral Loiseau C, Melo M, Lobato E, Beadell JS, Fleischer RC, Reis S, et al. Insularity effects on the assemblage of the blood parasite community of the birds from the Gulf of Guinea. J Biogeogr. 2017;44:2607–17.PubMedPubMedCentral
24.
go back to reference Smith JD, Gill SA, Baker KM, Vonhof MJ. Prevalence and diversity of avian Haemosporida infecting songbirds in southwest Michigan. Parasitol Res. 2018;117:471–89.PubMed Smith JD, Gill SA, Baker KM, Vonhof MJ. Prevalence and diversity of avian Haemosporida infecting songbirds in southwest Michigan. Parasitol Res. 2018;117:471–89.PubMed
25.
go back to reference Dodge M, Guers SL, Sekercioğlu ÇH, Sehgal RNM. North American transmission of hemosporidian parasites in the Swainson’s thrush (Catharus ustulatus), a migratory songbird. J Parasitol. 2013;99:548–54.PubMed Dodge M, Guers SL, Sekercioğlu ÇH, Sehgal RNM. North American transmission of hemosporidian parasites in the Swainson’s thrush (Catharus ustulatus), a migratory songbird. J Parasitol. 2013;99:548–54.PubMed
26.
go back to reference Bishop MA, Bennett GF. Host-parasite catalogue of the avian haematozoa: supplement 1, and Bibliography of the avian blood-inhabiting haematozoa. Mem Univ Nfld Occ Pap Biol. 1992;15:1–243. Bishop MA, Bennett GF. Host-parasite catalogue of the avian haematozoa: supplement 1, and Bibliography of the avian blood-inhabiting haematozoa. Mem Univ Nfld Occ Pap Biol. 1992;15:1–243.
27.
go back to reference Bennett GF, Whiteway M, Woodworth-Lynas C. A Host-parasite Catalogue of the Avian Haematozoa, vol. 5. St. John’s: Dept. of Biology, Memorial University of Newfoundland; 1982. Bennett GF, Whiteway M, Woodworth-Lynas C. A Host-parasite Catalogue of the Avian Haematozoa, vol. 5. St. John’s: Dept. of Biology, Memorial University of Newfoundland; 1982.
28.
go back to reference Schoener ER, Banda M, Howe L, Castro IC, Alley MR. Avian malaria in New Zealand. N Z Vet J. 2014;62:189–98.PubMed Schoener ER, Banda M, Howe L, Castro IC, Alley MR. Avian malaria in New Zealand. N Z Vet J. 2014;62:189–98.PubMed
29.
go back to reference Chvala S, Bakonyi T, Bukovsky C, Meister T, Brugger K, Rubel F, et al. Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003–2005. Vet Microbiol. 2007;122:237–45.PubMed Chvala S, Bakonyi T, Bukovsky C, Meister T, Brugger K, Rubel F, et al. Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003–2005. Vet Microbiol. 2007;122:237–45.PubMed
30.
go back to reference Bakonyi T, Erdélyi K, Ursu K, Ferenczi E, Csörgő T, Lussy H, et al. Emergence of Usutu virus in Hungary. J Clin Microbiol. 2007;45:3870–4.PubMedPubMedCentral Bakonyi T, Erdélyi K, Ursu K, Ferenczi E, Csörgő T, Lussy H, et al. Emergence of Usutu virus in Hungary. J Clin Microbiol. 2007;45:3870–4.PubMedPubMedCentral
31.
go back to reference Chvala S, Kolodziejek J, Nowotny N, Weissenböck H. Pathology and viral distribution in fatal Usutu virus infections of birds from the 2001 and 2002 outbreaks in Austria. J Comp Pathol. 2004;131:176–85.PubMed Chvala S, Kolodziejek J, Nowotny N, Weissenböck H. Pathology and viral distribution in fatal Usutu virus infections of birds from the 2001 and 2002 outbreaks in Austria. J Comp Pathol. 2004;131:176–85.PubMed
32.
go back to reference Weissenböck H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002;8:652–5.PubMedPubMedCentral Weissenböck H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002;8:652–5.PubMedPubMedCentral
33.
go back to reference Hall TA. BioEdit: a user-friendly biological sequences alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8. Hall TA. BioEdit: a user-friendly biological sequences alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.
34.
go back to reference Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.PubMedPubMedCentral Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.PubMedPubMedCentral
35.
go back to reference Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.
36.
go back to reference Harl J, Himmel T, Valkiūnas G, Weissenböck H. The nuclear 18S ribosomal DNAs of avian haemosporidian parasites. Malar J. 2019;18:305.PubMedPubMedCentral Harl J, Himmel T, Valkiūnas G, Weissenböck H. The nuclear 18S ribosomal DNAs of avian haemosporidian parasites. Malar J. 2019;18:305.PubMedPubMedCentral
37.
go back to reference Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:232–5. Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:232–5.
38.
go back to reference Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 32: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.PubMedPubMedCentral Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 32: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.PubMedPubMedCentral
39.
go back to reference Niebuhr CN, Blasco-Costa I. Improving detection of avian malaria from host blood: a step towards a standardised protocol for diagnostics. Parasitol Res. 2016;115:3905–11.PubMed Niebuhr CN, Blasco-Costa I. Improving detection of avian malaria from host blood: a step towards a standardised protocol for diagnostics. Parasitol Res. 2016;115:3905–11.PubMed
40.
go back to reference Howe L, Castro IC, Schoener ER, Hunter S, Barraclough RK, Alley MR. Malaria parasites (Plasmodium spp) infecting introduced, native and endemic New Zealand birds. Parasitol Res. 2012;110:913–23.PubMed Howe L, Castro IC, Schoener ER, Hunter S, Barraclough RK, Alley MR. Malaria parasites (Plasmodium spp) infecting introduced, native and endemic New Zealand birds. Parasitol Res. 2012;110:913–23.PubMed
41.
go back to reference Ferreira FC, Rodrigues RA, Sato Y, Borges MAZ, Braga ÉM. Searching for putative avian malaria vectors in a Seasonally Dry Tropical Forest in Brazil. Parasit Vectors. 2016;9:1–12. Ferreira FC, Rodrigues RA, Sato Y, Borges MAZ, Braga ÉM. Searching for putative avian malaria vectors in a Seasonally Dry Tropical Forest in Brazil. Parasit Vectors. 2016;9:1–12.
42.
go back to reference Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, et al. Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol Lett. 2012;15:1112–9.PubMed Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, et al. Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol Lett. 2012;15:1112–9.PubMed
43.
go back to reference Žiegytė R, Markovets MY, Bernotienė R, Mukhin A, Iezhova TA, Valkiūnas G, et al. The widespread biting midge Culicoides impunctatus (Ceratopogonidae) is susceptible to infection with numerous Haemoproteus (Haemoproteidae) species. Parasit Vectors. 2017;10:1–11. Žiegytė R, Markovets MY, Bernotienė R, Mukhin A, Iezhova TA, Valkiūnas G, et al. The widespread biting midge Culicoides impunctatus (Ceratopogonidae) is susceptible to infection with numerous Haemoproteus (Haemoproteidae) species. Parasit Vectors. 2017;10:1–11.
44.
go back to reference Palinauskas V, Iezhova TA, Križanauskienė A, Markovets MY, Bensch S, Valkiūnas G. Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitol Int. 2013;62:358–63.PubMed Palinauskas V, Iezhova TA, Križanauskienė A, Markovets MY, Bensch S, Valkiūnas G. Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitol Int. 2013;62:358–63.PubMed
45.
go back to reference Nilsson E, Taubert H, Hellgren O, Huang X, Palinauskas V, Markovets MY, et al. Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris. J Evol Biol. 2016;29:1812–26.PubMed Nilsson E, Taubert H, Hellgren O, Huang X, Palinauskas V, Markovets MY, et al. Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris. J Evol Biol. 2016;29:1812–26.PubMed
46.
go back to reference Valkiūnas G, Ilgūnas M, Bukauskaitė D, Chagas CRF, Bernotienė R, Himmel T, et al. Molecular characterization of six widespread avian haemoproteids, with description of three new Haemoproteus species. Acta Trop. 2019;197:1–17. Valkiūnas G, Ilgūnas M, Bukauskaitė D, Chagas CRF, Bernotienė R, Himmel T, et al. Molecular characterization of six widespread avian haemoproteids, with description of three new Haemoproteus species. Acta Trop. 2019;197:1–17.
47.
go back to reference Valkiūnas G, Ilgūnas M, Chagas CRF, Bernotienė R, Iezhova TA. Molecular characterization of swallow haemoproteids, with description of one new Haemoproteus species. Acta Trop. 2020;207:1–10. Valkiūnas G, Ilgūnas M, Chagas CRF, Bernotienė R, Iezhova TA. Molecular characterization of swallow haemoproteids, with description of one new Haemoproteus species. Acta Trop. 2020;207:1–10.
48.
go back to reference Bernotienė R, Palinauskas V, Iezhova T, Murauskaitė D, Valkiūnas G. Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol. 2016;163:31–7.PubMed Bernotienė R, Palinauskas V, Iezhova T, Murauskaitė D, Valkiūnas G. Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol. 2016;163:31–7.PubMed
49.
go back to reference Lotta IA, Valkiūnas G, Pacheco MA, Escalante AA, Hernández SR, Matta NE. Disentangling Leucocytozoon parasite diversity in the neotropics: descriptions of two new species and shortcomings of molecular diagnostics for leucocytozoids. Int J Parasitol Parasites Wildl. 2019;9:159–73.PubMedPubMedCentral Lotta IA, Valkiūnas G, Pacheco MA, Escalante AA, Hernández SR, Matta NE. Disentangling Leucocytozoon parasite diversity in the neotropics: descriptions of two new species and shortcomings of molecular diagnostics for leucocytozoids. Int J Parasitol Parasites Wildl. 2019;9:159–73.PubMedPubMedCentral
50.
go back to reference Galen SC, Borner J, Williamson JL, Witt CC, Perkins SL. Metatranscriptomics yields new genomic resources and sensitive detection of infections for diverse blood parasites. Mol Ecol Resour. 2020;20:14–28.PubMed Galen SC, Borner J, Williamson JL, Witt CC, Perkins SL. Metatranscriptomics yields new genomic resources and sensitive detection of infections for diverse blood parasites. Mol Ecol Resour. 2020;20:14–28.PubMed
51.
go back to reference Ortiz-Catedral L, Brunton D, Stidworthy MF, Elsheikha HM, Pennycott T, Schulze C, et al. Haemoproteus minutus is highly virulent for Australasian and South American parrots. Parasit Vectors. 2019;12:1–10. Ortiz-Catedral L, Brunton D, Stidworthy MF, Elsheikha HM, Pennycott T, Schulze C, et al. Haemoproteus minutus is highly virulent for Australasian and South American parrots. Parasit Vectors. 2019;12:1–10.
52.
go back to reference Bensch S, Pérez-Tris J, Waldenström J, Hellgren O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution (N Y). 2004;58:1617–21. Bensch S, Pérez-Tris J, Waldenström J, Hellgren O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution (N Y). 2004;58:1617–21.
53.
go back to reference Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. New York: Wiley; 2008. Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. New York: Wiley; 2008.
54.
go back to reference Starkloff NC, Kirchman JJ, Jones AW, Winger BM, Huang Y, Pulgarín-R PC, et al. Drivers of community turnover differ between avian hemoparasite genera along a North American latitudinal gradient. Ecol Evol. 2020;10:5402–15.PubMedPubMedCentral Starkloff NC, Kirchman JJ, Jones AW, Winger BM, Huang Y, Pulgarín-R PC, et al. Drivers of community turnover differ between avian hemoparasite genera along a North American latitudinal gradient. Ecol Evol. 2020;10:5402–15.PubMedPubMedCentral
55.
go back to reference Novy FG, MacNeal WJ. Trypanosomes and bird malaria. Proc Soc Exp Biol Med. 1904;2:23–8. Novy FG, MacNeal WJ. Trypanosomes and bird malaria. Proc Soc Exp Biol Med. 1904;2:23–8.
56.
go back to reference Manwell RD. Plasmodium vaughani (Novy and MacNeal). Am J Epidemiol. 1935;21:180–7. Manwell RD. Plasmodium vaughani (Novy and MacNeal). Am J Epidemiol. 1935;21:180–7.
57.
go back to reference Garnham PCC, Duggan AJ. Catalogue of the Garnham collection of malaria parasites and other Haemosporidia. London: Cambridge University Press; 1986. Garnham PCC, Duggan AJ. Catalogue of the Garnham collection of malaria parasites and other Haemosporidia. London: Cambridge University Press; 1986.
58.
go back to reference Manwell RD. Failure of Aedes aegypti and Culex pipiens to transmit Plasmodium vaughani. J Parasitol. 1947;33:167–9.PubMed Manwell RD. Failure of Aedes aegypti and Culex pipiens to transmit Plasmodium vaughani. J Parasitol. 1947;33:167–9.PubMed
59.
go back to reference Garnham PCC. Malaria parasites and other Haemosporidia. Oxford: Blackwell; 1966. Garnham PCC. Malaria parasites and other Haemosporidia. Oxford: Blackwell; 1966.
60.
go back to reference Corradetti A, Scanga M. Plasmodium (Novyella) vaughani subsp. merulae, n. subsp., parassita di Turdus merula, con descrizione del ciclo pre-eritrocitico. Parassitologia. 1972;14:85–93. Corradetti A, Scanga M. Plasmodium (Novyella) vaughani subsp. merulae, n. subsp., parassita di Turdus merula, con descrizione del ciclo pre-eritrocitico. Parassitologia. 1972;14:85–93.
61.
go back to reference Corradetti A, Scanga M. The Plasmodium vaughani—complex. Exp Parasitol. 1973;34:344–9.PubMed Corradetti A, Scanga M. The Plasmodium vaughani—complex. Exp Parasitol. 1973;34:344–9.PubMed
62.
go back to reference Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, et al. Plasmodium spp: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol. 2015;148:1–16.PubMed Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, et al. Plasmodium spp: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol. 2015;148:1–16.PubMed
63.
go back to reference Iezhova TA, Valkiūnas G, Bairlein F. Vertebrate host specificity of two avian malaria parasites of the subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol. 2005;91:472–4.PubMed Iezhova TA, Valkiūnas G, Bairlein F. Vertebrate host specificity of two avian malaria parasites of the subgenus Novyella: Plasmodium nucleophilum and Plasmodium vaughani. J Parasitol. 2005;91:472–4.PubMed
64.
go back to reference Schoener E, Uebleis SS, Butter J, Nawratil M, Cuk C, Flechl E, et al. Avian Plasmodium in Eastern Austrian mosquitoes. Malar J. 2017;16:1–12. Schoener E, Uebleis SS, Butter J, Nawratil M, Cuk C, Flechl E, et al. Avian Plasmodium in Eastern Austrian mosquitoes. Malar J. 2017;16:1–12.
65.
go back to reference Martinsen ES, Waite JL, Schall JJ. Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology. 2007;134:483–90.PubMed Martinsen ES, Waite JL, Schall JJ. Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology. 2007;134:483–90.PubMed
66.
go back to reference Mantilla JS, González AD, Valkiūnas G, Moncada LI, Matta NE. Description and molecular characterization of Plasmodium (Novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland of Colombia. Parasitol Res. 2013;112:4193–204.PubMed Mantilla JS, González AD, Valkiūnas G, Moncada LI, Matta NE. Description and molecular characterization of Plasmodium (Novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland of Colombia. Parasitol Res. 2013;112:4193–204.PubMed
67.
go back to reference Tostes R, Dias RJP, de Oliveira L, Senra MVX, Massard CL, D’Agosto M. Molecular and morphological characterization of a Brazilian lineage of Plasmodium (Novyella) unalis in Turdus spp. (Passeriformes) of the Atlantic Forest, with remarks on new hosts and high genetic variation. J Parasitol. 2018;104:70–8.PubMed Tostes R, Dias RJP, de Oliveira L, Senra MVX, Massard CL, D’Agosto M. Molecular and morphological characterization of a Brazilian lineage of Plasmodium (Novyella) unalis in Turdus spp. (Passeriformes) of the Atlantic Forest, with remarks on new hosts and high genetic variation. J Parasitol. 2018;104:70–8.PubMed
68.
go back to reference Huff CG. Plasmodium hexamerium, n. sp. from the bluebird, inoculable to canaries. Am J Hyg. 1935;22:274–7. Huff CG. Plasmodium hexamerium, n. sp. from the bluebird, inoculable to canaries. Am J Hyg. 1935;22:274–7.
69.
go back to reference Manwell RD. Plasmodium oti and P. hexamerium. J Parasitol. 1949;35:561–5.PubMed Manwell RD. Plasmodium oti and P. hexamerium. J Parasitol. 1949;35:561–5.PubMed
70.
go back to reference Manwell RD. Turkeys and ducks as experimental hosts for Plasmodium hexamerium and P. vaughani. Exp Parasitol. 1952;1:274–82. Manwell RD. Turkeys and ducks as experimental hosts for Plasmodium hexamerium and P. vaughani. Exp Parasitol. 1952;1:274–82.
71.
go back to reference Walther EL, Valkiūnas G, González AD, Matta NE, Ricklefs RE, Cornel A, 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. 2014;113:3319–32.PubMed Walther EL, Valkiūnas G, González AD, Matta NE, Ricklefs RE, Cornel A, 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. 2014;113:3319–32.PubMed
72.
go back to reference Ganser C, Gregory AJ, McNew LB, Hunt LA, Sandercock BK, Wisely SM. Fine-scale distribution modeling of avian malaria vectors in north-central Kansas. J Vector Ecol. 2016;41:114–22.PubMed Ganser C, Gregory AJ, McNew LB, Hunt LA, Sandercock BK, Wisely SM. Fine-scale distribution modeling of avian malaria vectors in north-central Kansas. J Vector Ecol. 2016;41:114–22.PubMed
73.
go back to reference Ishak HD, Dumbacher JP, Anderson NL, Keane JJ, Valkiūnas G, Haig SM, et al. Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS ONE. 2008;3:1–10. Ishak HD, Dumbacher JP, Anderson NL, Keane JJ, Valkiūnas G, Haig SM, et al. Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS ONE. 2008;3:1–10.
74.
go back to reference Pacheco MA, Matta NE, Valkiūnas G, Parker PG, Mello B, Stanley CE Jr, et al. Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Mol Biol Evol. 2017;35:383–403.PubMedCentral Pacheco MA, Matta NE, Valkiūnas G, Parker PG, Mello B, Stanley CE Jr, et al. Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Mol Biol Evol. 2017;35:383–403.PubMedCentral
75.
go back to reference Wolfson F. A strain of Plasmodium praecox (relictum) with highly synchronous matinal sporulation. Am J Epidemiol. 1937;25:177–86. Wolfson F. A strain of Plasmodium praecox (relictum) with highly synchronous matinal sporulation. Am J Epidemiol. 1937;25:177–86.
76.
go back to reference Huff CG. A new variety of Plasmodium relictum from the robin. J Parasitol. 1937;23:400–4. Huff CG. A new variety of Plasmodium relictum from the robin. J Parasitol. 1937;23:400–4.
77.
go back to reference Huff CG, Marchbank DF, Shiroishi T. Susceptibility and resistance of avian and mosquito hosts to strains of Plasmodium relictum isolated from pigeons. J Protozool. 1959;6:46–51. Huff CG, Marchbank DF, Shiroishi T. Susceptibility and resistance of avian and mosquito hosts to strains of Plasmodium relictum isolated from pigeons. J Protozool. 1959;6:46–51.
78.
go back to reference Corradetti A, Neri I, Scanga M. 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. 1960;2:333–43. Corradetti A, Neri I, Scanga M. 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. 1960;2:333–43.
79.
go back to reference Corradetti A, Moroos WM, Neri I. The production of endohistiocytic stages in canaries infected with an Italian strain of Plasmodium matutinum derived from Turdus iliacus. Parassitologia. 1962;4:105–8. Corradetti A, Moroos WM, Neri I. The production of endohistiocytic stages in canaries infected with an Italian strain of Plasmodium matutinum derived from Turdus iliacus. Parassitologia. 1962;4:105–8.
80.
go back to reference Valkiūnas G, Ilgūnas M, Bukauskaitė D, Palinauskas V, Bernotienė R, Iezhova TA. Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology. 2017;144:1726–35.PubMed Valkiūnas G, Ilgūnas M, Bukauskaitė D, Palinauskas V, Bernotienė R, Iezhova TA. Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology. 2017;144:1726–35.PubMed
81.
go back to reference Schoener ER, Harl J, Himmel T, Fragner K, Weissenböck H, Fuehrer H-P. Protozoan parasites in Culex pipiens mosquitoes in Vienna. Parasitol Res. 2019;118:1261–9.PubMedPubMedCentral Schoener ER, Harl J, Himmel T, Fragner K, Weissenböck H, Fuehrer H-P. Protozoan parasites in Culex pipiens mosquitoes in Vienna. Parasitol Res. 2019;118:1261–9.PubMedPubMedCentral
82.
go back to reference Levin II, Colborn RE, Kim D, Perlut NG, Renfrew RB, Parker PG. Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium. Ecol Evol. 2016;6:716–26.PubMedPubMedCentral Levin II, Colborn RE, Kim D, Perlut NG, Renfrew RB, Parker PG. Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium. Ecol Evol. 2016;6:716–26.PubMedPubMedCentral
83.
go back to reference Kimura M, Darbro JM, Harrington LC. Avian malaria parasites share congeneric mosquito vectors. J Parasitol. 2010;96:144–51.PubMed Kimura M, Darbro JM, Harrington LC. Avian malaria parasites share congeneric mosquito vectors. J Parasitol. 2010;96:144–51.PubMed
84.
go back to reference Corradetti A, Verolini F, Neri I. Plasmodium (Haemamoeba) giovannolai n. sp. parassita di Turdus merula. Parassitologia. 1963;5:11–8. Corradetti A, Verolini F, Neri I. Plasmodium (Haemamoeba) giovannolai n. sp. parassita di Turdus merula. Parassitologia. 1963;5:11–8.
85.
go back to reference Corradetti A, Verolini F, Neri I. Studi sull’infezione da Plasmodium (Haemamoeba) giovannolai nel canarino. Parassitologia. 1963;5:73–85. Corradetti A, Verolini F, Neri I. Studi sull’infezione da Plasmodium (Haemamoeba) giovannolai nel canarino. Parassitologia. 1963;5:73–85.
86.
go back to reference Himmel T, Harl J, Pfanner S, Nedorost N, Nowotny N, Weissenböck H. Haemosporidioses in wild Eurasian blackbirds (Turdus merula) and song thrushes (T philomelos): an in situ hybridization study with emphasis on exo-erythrocytic parasite burden. Malar J. 2020;19:1–13. Himmel T, Harl J, Pfanner S, Nedorost N, Nowotny N, Weissenböck H. Haemosporidioses in wild Eurasian blackbirds (Turdus merula) and song thrushes (T philomelos): an in situ hybridization study with emphasis on exo-erythrocytic parasite burden. Malar J. 2020;19:1–13.
87.
go back to reference Ilgūnas M, Bukauskaitė D, Palinauskas V, Iezhova T, Fragner K, Platonova E, et al. Patterns of Plasmodium homocircumflexum virulence in experimentally infected passerine birds. Malar J. 2019;18:174.PubMedPubMedCentral Ilgūnas M, Bukauskaitė D, Palinauskas V, Iezhova T, Fragner K, Platonova E, et al. Patterns of Plasmodium homocircumflexum virulence in experimentally infected passerine birds. Malar J. 2019;18:174.PubMedPubMedCentral
88.
go back to reference Lucena D. Malária aviária I—Plasmodium lutzi n. sp. Parasita da Saracura (Aramides cajanea cajanea, Müller). Biol Bull. 1939;4:27–31. Lucena D. Malária aviária I—Plasmodium lutzi n. sp. Parasita da Saracura (Aramides cajanea cajanea, Müller). Biol Bull. 1939;4:27–31.
89.
go back to reference Gabaldon A, Ulloa G. Las formas exoeritrocíticas de Plasmodium (Haemamoeba) lutzi Lucena, 1939 y presencia de esta especie en Venezuela [parásito de Aramides cajanea cajanea]. Boletín La Dir Malariol y Saneam Ambient. 1976;16:299–312. Gabaldon A, Ulloa G. Las formas exoeritrocíticas de Plasmodium (Haemamoeba) lutzi Lucena, 1939 y presencia de esta especie en Venezuela [parásito de Aramides cajanea cajanea]. Boletín La Dir Malariol y Saneam Ambient. 1976;16:299–312.
90.
go back to reference Renjifo S, Sanmartin C, Zulueta J. A survey of the blood parasites of vertebrates in eastern Colombia. Acta Trop. 1952;9:151–69.PubMed Renjifo S, Sanmartin C, Zulueta J. A survey of the blood parasites of vertebrates in eastern Colombia. Acta Trop. 1952;9:151–69.PubMed
91.
go back to reference González AD, Lotta IA, García LF, Moncada LI, Matta NE. Avian haemosporidians from Neotropical highlands: evidence from morphological and molecular data. Parasitol Int. 2015;64:48–59.PubMed González AD, Lotta IA, García LF, Moncada LI, Matta NE. Avian haemosporidians from Neotropical highlands: evidence from morphological and molecular data. Parasitol Int. 2015;64:48–59.PubMed
92.
go back to reference Carlson ML, Proudfoot GA, Gentile K, Dispoto J, Weckstein JD. Haemosporidian prevalence in northern saw-whet owls Aegolius acadicus is predicted by host age and average annual temperature at breeding grounds. J Avian Biol. 2018;49:1–11. Carlson ML, Proudfoot GA, Gentile K, Dispoto J, Weckstein JD. Haemosporidian prevalence in northern saw-whet owls Aegolius acadicus is predicted by host age and average annual temperature at breeding grounds. J Avian Biol. 2018;49:1–11.
93.
go back to reference Chagas CRF, Valkiūnas G, Guimarães LO, Monteiro EF, Guida FJV, Simões RF, et al. Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar J. 2017;16:1–20. Chagas CRF, Valkiūnas G, Guimarães LO, Monteiro EF, Guida FJV, Simões RF, et al. Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar J. 2017;16:1–20.
94.
go back to reference Kikuth W. Immunbiologische und chemotherapeutische Studien an verschiedenen Stämmen von Vogelmalaria. Zentralblatt Für Bakteriol Parasitenkunde, Infekt Und Hyg. 1931;121:401–9. Kikuth W. Immunbiologische und chemotherapeutische Studien an verschiedenen Stämmen von Vogelmalaria. Zentralblatt Für Bakteriol Parasitenkunde, Infekt Und Hyg. 1931;121:401–9.
95.
go back to reference Valkiūnas G, Palinauskas V, Ilgūnas M, Bukauskaitė D, Dimitrov D, Bernotiené R, et al. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol Res. 2014;113:2251–63.PubMed Valkiūnas G, Palinauskas V, Ilgūnas M, Bukauskaitė D, Dimitrov D, Bernotiené R, et al. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol Res. 2014;113:2251–63.PubMed
96.
go back to reference Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiūnas G. Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa. 2007;1626:39–50. Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiūnas G. Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa. 2007;1626:39–50.
97.
go back to reference Mazza S, Fiora A. Proteosoma de mirlo, Planesticus anthracinus (Burm.) y Leucocytozoon (sic) di Benteveo, Pitangus sulphuratus bolivianus (Latv.) y fueguero Piranga flava (Viell.) de Tumbaya, Jujuy. 5th Reun Soc Argent Patol Reg Norte. 1930;2:993–5. Mazza S, Fiora A. Proteosoma de mirlo, Planesticus anthracinus (Burm.) y Leucocytozoon (sic) di Benteveo, Pitangus sulphuratus bolivianus (Latv.) y fueguero Piranga flava (Viell.) de Tumbaya, Jujuy. 5th Reun Soc Argent Patol Reg Norte. 1930;2:993–5.
98.
go back to reference Coatney GR, Roudabush RL. A catalog and host-index of the genus Plasmodium. J Parasitol. 1936;22:338–53. Coatney GR, Roudabush RL. A catalog and host-index of the genus Plasmodium. J Parasitol. 1936;22:338–53.
99.
go back to reference Bennett GF, Campbell AG. Avian Haemoproteidae. I. Description of Haemoproteus fallisi n. sp. and a review of the haemoproteids of the family Turdidae. Can J Zool. 1972;50:1269–75.PubMed Bennett GF, Campbell AG. Avian Haemoproteidae. I. Description of Haemoproteus fallisi n. sp. and a review of the haemoproteids of the family Turdidae. Can J Zool. 1972;50:1269–75.PubMed
100.
go back to reference Laveran A. Sur une Haemamoeba d’une mésange (Parus major). CR Séances Soc Biol Fil. 1902;54:1121–4. Laveran A. Sur une Haemamoeba d’une mésange (Parus major). CR Séances Soc Biol Fil. 1902;54:1121–4.
101.
go back to reference Cleland SJB, Johnston TH. Descriptions of new haemoprotozoa from birds in New South Wales, with a note on the resemblance between the spermatozoa of certain honeyeaters (Fam. Meliphagidae) and spirochaete-trypanosomes. J Proc R Soc New South Wales. 1909;43:97–103. Cleland SJB, Johnston TH. Descriptions of new haemoprotozoa from birds in New South Wales, with a note on the resemblance between the spermatozoa of certain honeyeaters (Fam. Meliphagidae) and spirochaete-trypanosomes. J Proc R Soc New South Wales. 1909;43:97–103.
102.
go back to reference Valkiūnas GA, Iezhova TA. New species of hemoproteids (Haemosporidia, Haemoproteidae) in passerine birds. Zool Zhurnal. 1992;71:5–15. Valkiūnas GA, Iezhova TA. New species of hemoproteids (Haemosporidia, Haemoproteidae) in passerine birds. Zool Zhurnal. 1992;71:5–15.
103.
go back to reference Valkiunas G, Iezhova T. New species of haemoproteids (Haemosporidia) in passerine birds [in Russian]. Parazitologiya. 1991;25:212–8. Valkiunas G, Iezhova T. New species of haemoproteids (Haemosporidia) in passerine birds [in Russian]. Parazitologiya. 1991;25:212–8.
104.
go back to reference Hellgren O, Križanauskiene A, Valkiūnas G, Bensch S. Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol. 2007;93:889–96.PubMed Hellgren O, Križanauskiene A, Valkiūnas G, Bensch S. Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol. 2007;93:889–96.PubMed
105.
go back to reference Jones W, Kulma K, Bensch S, Cichoń M, Kerimov A, Krist M, et al. Interspecific transfer of parasites following a range-shift in Ficedula flycatchers. Ecol Evol. 2018;8:12183–92.PubMedPubMedCentral Jones W, Kulma K, Bensch S, Cichoń M, Kerimov A, Krist M, et al. Interspecific transfer of parasites following a range-shift in Ficedula flycatchers. Ecol Evol. 2018;8:12183–92.PubMedPubMedCentral
106.
go back to reference Kulma K, Low M, Bensch S, Qvarnström A. Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone. Mol Ecol. 2013;22:4591–601.PubMed Kulma K, Low M, Bensch S, Qvarnström A. Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone. Mol Ecol. 2013;22:4591–601.PubMed
107.
go back to reference Kulma K, Low M, Bensch S, Qvarnström A. Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding. PLoS ONE. 2014;9:1–9. Kulma K, Low M, Bensch S, Qvarnström A. Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding. PLoS ONE. 2014;9:1–9.
108.
go back to reference Ricklefs RE, Fallon SM. Diversification and host switching in avian malaria parasites. Proc R Soc London Ser B Biol Sci. 2002;269:885–92. Ricklefs RE, Fallon SM. Diversification and host switching in avian malaria parasites. Proc R Soc London Ser B Biol Sci. 2002;269:885–92.
109.
go back to reference Coscarón S, Arias CLC. Neotropical Simuliidae (Diptera: Insecta), vol. 3. Sofia: Pensoft publishers; 2007. Coscarón S, Arias CLC. Neotropical Simuliidae (Diptera: Insecta), vol. 3. Sofia: Pensoft publishers; 2007.
110.
go back to reference Hamada N, McCreadie JW, Adler PH. Species richness and spatial distribution of blackflies (Diptera: Simuliidae) in streams of Central Amazonia, Brazil. Freshw Biol. 2002;47:31–40. Hamada N, McCreadie JW, Adler PH. Species richness and spatial distribution of blackflies (Diptera: Simuliidae) in streams of Central Amazonia, Brazil. Freshw Biol. 2002;47:31–40.
111.
go back to reference Fecchio A, Silveira P, Weckstein JD, Dispoto JH, Anciães M, Bosholn M, et al. First record of Leucocytozoon (Haemosporida: Leucocytozoidae) in Amazonia: evidence for rarity in Neotropical lowlands or lack of sampling for this parasite genus? J Parasitol. 2018;104:168–72.PubMed Fecchio A, Silveira P, Weckstein JD, Dispoto JH, Anciães M, Bosholn M, et al. First record of Leucocytozoon (Haemosporida: Leucocytozoidae) in Amazonia: evidence for rarity in Neotropical lowlands or lack of sampling for this parasite genus? J Parasitol. 2018;104:168–72.PubMed
112.
go back to reference Ride W. International code of zoological nomenclature. International Trust for Zoological Nomenclature; 1999. Ride W. International code of zoological nomenclature. International Trust for Zoological Nomenclature; 1999.
113.
go back to reference Mathis CJBMJ, Leger M. Recherches de parasitologie et de pathologie humaines et animales au Tonkin. Masson: University of California; 1911. Mathis CJBMJ, Leger M. Recherches de parasitologie et de pathologie humaines et animales au Tonkin. Masson: University of California; 1911.
114.
go back to reference McClure HE, Poonswad P, Greiner EC, Laird M. Haematozoa in the birds of eastern and southern Asia. St. John’s: Memorial University of Newfoundland; 1978. McClure HE, Poonswad P, Greiner EC, Laird M. Haematozoa in the birds of eastern and southern Asia. St. John’s: Memorial University of Newfoundland; 1978.
115.
go back to reference Fallis AM, Desser SS, Khan RA. On species of Leucocytozoon. Adv Parasitol. 1974;12:1–67.PubMed Fallis AM, Desser SS, Khan RA. On species of Leucocytozoon. Adv Parasitol. 1974;12:1–67.PubMed
116.
go back to reference Travassos Santos Dias JA. Estudos sobre os hematozoarios das aves de Mocambique. I. Leucocytozoon beaurepairei n. sp., parasita do Sagittarius serpentarius (Miller 1779). Bull Soc Estud Mocambique. 1954;87:1–14. Travassos Santos Dias JA. Estudos sobre os hematozoarios das aves de Mocambique. I. Leucocytozoon beaurepairei n. sp., parasita do Sagittarius serpentarius (Miller 1779). Bull Soc Estud Mocambique. 1954;87:1–14.
117.
go back to reference França C. Contribution a l’étude des Leucocytozoon des oiseaux du Portugal. Bull Soc Path Exot. 1912;5:82–6. França C. Contribution a l’étude des Leucocytozoon des oiseaux du Portugal. Bull Soc Path Exot. 1912;5:82–6.
118.
go back to reference Greiner EC. Leucocytozoon maccluri sp. n.(Haemosporida: Leucocytozoidae) from a Thailand thrush, Zoothera marginata Blyth. Zoothera marginata Blyth. J Parasitol. 1976;62:545–7.PubMed Greiner EC. Leucocytozoon maccluri sp. n.(Haemosporida: Leucocytozoidae) from a Thailand thrush, Zoothera marginata Blyth. Zoothera marginata Blyth. J Parasitol. 1976;62:545–7.PubMed
119.
go back to reference Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs RE. Parasite misidentifications in GenBank: how to minimize their number? Trends Parasitol. 2008;6:247–8. Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs RE. Parasite misidentifications in GenBank: how to minimize their number? Trends Parasitol. 2008;6:247–8.
Metadata
Title
Geographic and host distribution of haemosporidian parasite lineages from birds of the family Turdidae
Authors
Josef Harl
Tanja Himmel
Gediminas Valkiūnas
Mikas Ilgūnas
Támas Bakonyi
Herbert Weissenböck
Publication date
01-12-2020
Publisher
BioMed Central
Keywords
Thrush
Plasmodia
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03408-0

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