Prevalence and genetic diversity of avian haemosporidian parasites in wild bird species of the order Columbiformes.
Animal Migration
Animals
Bird Diseases
/ epidemiology
Columbidae
/ parasitology
Columbiformes
/ parasitology
Cytochromes b
/ genetics
Genetic Variation
Global Warming
Haemosporida
/ classification
Host Specificity
Mitochondria
/ genetics
Multiplex Polymerase Chain Reaction
/ veterinary
Phylogeny
Plasmodium
/ genetics
Polymerase Chain Reaction
/ veterinary
Prevalence
Protozoan Infections, Animal
/ epidemiology
Avian malaria
Parasite ecology
Stock dove
Turtle dove
Woodpigeon
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
16
11
2020
accepted:
11
01
2021
pubmed:
2
2
2021
medline:
1
7
2021
entrez:
1
2
2021
Statut:
ppublish
Résumé
Diseases can play a role in species decline. Among them, haemosporidian parasites, vector-transmitted protozoan parasites, are known to constitute a risk for different avian species. However, the magnitude of haemosporidian infection in wild columbiform birds, including strongly decreasing European turtle doves, is largely unknown. We examined the prevalence and diversity of haemosporidian parasites Plasmodium, Leucocytozoon and subgenera Haemoproteus and Parahaemoproteus in six species of the order Columbiformes during breeding season and migration by applying nested PCR, one-step multiplex PCR assay and microscopy. We detected infections in 109 of the 259 screened individuals (42%), including 15 distinct haemosporidian mitochondrial cytochrome b lineages, representing five H. (Haemoproteus), two H. (Parahaemoproteus), five Leucocytozoon and three Plasmodium lineages. Five of these lineages have never been described before. We discriminated between single and mixed infections and determined host species-specific prevalence for each parasite genus. Observed differences among sampled host species are discussed with reference to behavioural characteristics, including nesting and migration strategy. Our results support previous suggestions that migratory birds have a higher prevalence and diversity of blood parasites than resident or short-distance migratory species. A phylogenetic reconstruction provided evidence for H. (Haemoproteus) as well as H. (Parahaemoproteus) infections in columbiform birds. Based on microscopic examination, we quantified parasitemia, indicating the probability of negative effects on the host. This study provides a large-scale baseline description of haemosporidian infections of wild birds belonging to the order Columbiformes sampled in the northern hemisphere. The results enable the monitoring of future changes in parasite transmission areas, distribution and diversity associated with global change, posing a potential risk for declining avian species as the European turtle dove.
Identifiants
pubmed: 33521839
doi: 10.1007/s00436-021-07053-7
pii: 10.1007/s00436-021-07053-7
pmc: PMC7940316
doi:
Substances chimiques
Cytochromes b
9035-37-4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1405-1420Références
Adamik P, Emmenegger T, Briedis M et al (2016) Barrier crossing in small avian migrants: individual tracking reveals prolonged nocturnal flights into the day as a common migratory strategy. Sci Rep 6:21560. https://doi.org/10.1038/srep21560
doi: 10.1038/srep21560
pubmed: 26876925
pmcid: 4753512
Akinpelu AI (2008) Prevalence and intensity of blood parasites in wild pigeons and doves (Family: Columbidae) from Sasha Forest Reserve, Ile-Ife, Nigeria. Asian J Anim Vet Adv 3:109–114. https://doi.org/10.3923/ajava.2008.109.114
doi: 10.3923/ajava.2008.109.114
Applegate JE, Beaudoin RL (1970) Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone. J Wildl Dis 6:443–447. https://doi.org/10.7589/0090-3558-6.4.443
doi: 10.7589/0090-3558-6.4.443
pubmed: 16512154
Atkinson CT, Van Riper C (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: Loye JE, Zuk M (eds.) Bird-parasite interactions: ecology, evolution and behaviour. Oxford Ornithology Series, pp 19–48
Bensch S, Waldenström J, Jonzen N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122. https://doi.org/10.1111/j.1365-2656.2006.01176.x
doi: 10.1111/j.1365-2656.2006.01176.x
pubmed: 17184359
Bensch S, Hellgren O, Peréz-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x
doi: 10.1111/j.1755-0998.2009.02692.x
pubmed: 21564906
Bernotienė R, Palinauskas V, Iezhova T, Murauskaitė D, Valkiūnas G (2016) Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol 163:31–37. https://doi.org/10.1016/j.exppara.2016.01.009
doi: 10.1016/j.exppara.2016.01.009
pubmed: 26821298
Borner J, Pick C, Thiede J, Kolawole OM et al (2016) Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Mol Phylogenet Evol 94:221–231. https://doi.org/10.1016/j.ympev.2015.09.003
doi: 10.1016/j.ympev.2015.09.003
pubmed: 26364971
Boundenga L, Perkins SL, Ollomo B, Rougeron V, Leroy EM, Renaud F, Prugnolle F (2017) Haemosporidian parasites of reptiles and birds from Gabon, Central Africa. J Parasitol 103:330–337. https://doi.org/10.1371/journal.pone.0148958
doi: 10.1371/journal.pone.0148958
pubmed: 28509658
Bunbury N, Barton E, Jones CG, Greenwood AG, Tyler KM, Bell DJ (2007) Avian blood parasites in an endangered columbid: Leucocytozoon marchouxi in the Mauritian Pink Pigeon Columba mayeri. Parasitology 134:797–804. https://doi.org/10.1017/S0031182006002149
doi: 10.1017/S0031182006002149
pubmed: 17201998
Calderon L, Campagna L, Wilke T et al (2016) Genomic evidence of demographic fluctuations and lack of genetic structure across flyways in a long distance migrant, the European turtle dove. BMC Evol Biol 16:237. https://doi.org/10.1186/s12862-016-0817-7
doi: 10.1186/s12862-016-0817-7
pubmed: 27821052
pmcid: 5100323
Carlson J, Martínez-Gómez JE, Valkiūnas G, Loiseau C, Bell DA, Sehgal RN (2013) Diversity and phylogenetic relationships of hemosporidian parasites in birds of Socorro Island, México and their role in the re-introduction of the Socorro Dove (Zenaida graysoni). J Parasitol 99:270–276. https://doi.org/10.1645/GE-3206.1
doi: 10.1645/GE-3206.1
pubmed: 23043349
Chagas CRF, de Oliveira Guimarães L, Monteiro EF et al (2016) Hemosporidian parasites of free-living birds in the São Paulo Zoo, Brazil. Parasitol Res 115:1443–1452. https://doi.org/10.1007/s00436-015-4878-0
doi: 10.1007/s00436-015-4878-0
pubmed: 26677094
Chakarov N, Kampen H, Wiegmann A, Werner D, Bensch S (2020) Blood parasites in vectors reveal a united blackfly community in the upper canopy. Parasites Vectors 13:309. https://doi.org/10.1186/s13071-020-04177-0
doi: 10.1186/s13071-020-04177-0
pubmed: 32539849
pmcid: 7296761
Ciloglu A, Ellis VA, Bernotienė R, Valkiūnas G, Bensch S (2019) A new one-step multiplex PCR assay for simultaneous detection and identification of avian haemosporidian parasites. Parasitol Res 118:191–201. https://doi.org/10.1007/s00436-018-6153-7
doi: 10.1007/s00436-018-6153-7
pubmed: 30536121
Ciloglu A, Ellis VA, Duc M, Downing PA, Inci A, Bensch S (2020a) Evolution of vector transmitted parasites by host switching revealed through sequencing of Haemoproteus parasite mitochondrial genomes. Mol Phylogenet Evol 153:106947. https://doi.org/10.1016/j.ympev.2020.106947
Ciloglu A, Ergen AG, Inci A et al (2020b) Prevalence and genetic diversity of avian haemosporidian parasites at an intersection point of bird migration routes: Sultan Marshes National Park, Turkey. Acta Trop 210:105465. https://doi.org/10.1016/j.actatropica.2020.105465
doi: 10.1016/j.actatropica.2020.105465
pubmed: 32504592
Clark P, Boardman W, Raidal S (2009) Atlas of clinical avian hematology. Wiley-Blackwell, New York
Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol 44:329–338. https://doi.org/10.1016/j.ijpara.2014.01.004
doi: 10.1016/j.ijpara.2014.01.004
pubmed: 24556563
Clark NJ, Clegg SM, Klaassen M (2016) Migration strategy and pathogen risk: non-breeding distribution drives malaria prevalence in migratory waders. Oikos 125:1358–1368. https://doi.org/10.1111/oik.03220
doi: 10.1111/oik.03220
Cornelius JM, Zylberberg M, Breuner CW, Gleiss AC, Hahn TP (2014) Assessing the role of reproduction and stress in the spring emergence of haematozoan parasites in birds. J Exp Biol 217:841–849. https://doi.org/10.1242/jeb.080697
doi: 10.1242/jeb.080697
pubmed: 24265426
Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548. https://doi.org/10.1111/j.1365-2656.2008.01370.x
doi: 10.1111/j.1365-2656.2008.01370.x
pubmed: 18312339
Cramp S (1985) Handbook of the birds of Europe, the Middle East and North Africa. Volume IV, Terns to Woodpeckers. Oxford University Press, Oxford
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
doi: 10.1038/nmeth.2109
pubmed: 22847109
pmcid: 4594756
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
doi: 10.1186/1471-2148-7-214
pubmed: 17996036
pmcid: 2247476
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
doi: 10.1093/molbev/mss075
pubmed: 22367748
pmcid: 3408070
Dubiec A, Podmokła E, Zagalska-Neubauer M, Drobniak SM, Arct A, Gustafsson L, Cichoń M (2016) Differential prevalence and diversity of haemosporidian parasites in two sympatric closely related non-migratory passerines. Parasitology 143:1320–1329. https://doi.org/10.1017/S0031182016000779
doi: 10.1017/S0031182016000779
pubmed: 27173618
Dunn JC, Outlaw DC (2019) Flying into the future: avian haemosporidians and the advancement of understanding host–parasite systems. Parasitology 146:1–10. https://doi.org/10.1017/S003118201900057X
doi: 10.1017/S003118201900057X
Dunn JC, Stockdale JE, Bradford EL et al (2017) High rates of infection by blood parasites during the nestling phase in UK Columbids with notes on ecological associations. Parasitology 144:622–628. https://doi.org/10.1017/S0031182016002274
doi: 10.1017/S0031182016002274
pubmed: 27938431
Earle RA, Batianello SS, Bennet GF, Krecek RC (1993) Histopathology and morphology of the tissue stages of Haemoproteus columbae causing mortality in Columbiformes. Avian Pathol 22:67–80. https://doi.org/10.1080/03079459308418901
doi: 10.1080/03079459308418901
pubmed: 18670998
Ellis VA, Huang X, Westerdahl H et al (2020) Explaining prevalence, diversity, and host specificity in a community of avian haemosporidian parasites. Oikos 129:1314–1329. https://doi.org/10.1111/oik.07280
doi: 10.1111/oik.07280
Emmenegger T, Bauer S, Dimitrov D, Marin JO, Zehtindjiev P, Hahn S (2018) Host migration strategy and blood parasite infections of three sparrow species sympatrically breeding in Southeast Europe. Parasitol Res 117:3733–3741. https://doi.org/10.1007/s00436-018-6072-7
doi: 10.1007/s00436-018-6072-7
pubmed: 30232606
Ferraguti M, Martínez-de la Puente J, Garcia-Longoria L, Soriguer R, Figuerola J, Marzal A (2019) From Africa to Europe: evidence of transmission of a tropical Plasmodium lineage in Spanish populations of house sparrows. Parasites Vectors 12:548. https://doi.org/10.1186/s13071-019-3804-1
doi: 10.1186/s13071-019-3804-1
pubmed: 31753041
pmcid: 6873688
Ferreira Junior FC, Rodrigues RA, Ellis VA, Leite LO, Borges MAZ, Braga EM (2017) Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil. PLoS ONE 12:e0178791. https://doi.org/10.1371/journal.pone.0178791
doi: 10.1371/journal.pone.0178791
pubmed: 28575046
pmcid: 5456369
Figuerola J, Green AJ (2000) Hematozoan parasites and migratory behaviour in waterfowl. Evol Ecol 14:143–153. https://doi.org/10.1023/A:1011009419264
doi: 10.1023/A:1011009419264
Fisher I, Ashpole J, Scallan D, Carboneras C, Proud T (compilers) (2018) International Single Species Action Plan for the conservation of the European Turtle-dove Streptopelia turtur (2018 to 2028). European Commission Technical Report xxx-2018
Foronda P, Valladares B, Rivera-Medina JA, Figueruelo E, Abreu N, Casanova JC (2004) Parasites of Columba livia (Aves: Columbiformes) in Tenerife (Canary Islands) and their role in the conservation biology of the Laurel pigeons. Parasite 11:311–316. https://doi.org/10.1051/parasite/2004113311
doi: 10.1051/parasite/2004113311
pubmed: 15490756
Galen SC, Borner J, Martinsen ES, Schaer J, Austin CC, West CJ, Perkins SL (2018) The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R Soc Open sci 5:171780. https://doi.org/10.1098/rsos.171780
doi: 10.1098/rsos.171780
pubmed: 29892372
pmcid: 5990803
Gernhard T (2008) Yule process. J Theor Biol 253:769–778
doi: 10.1016/j.jtbi.2008.04.005
Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565. https://doi.org/10.7589/0090-3558-23.4.558
doi: 10.7589/0090-3558-23.4.558
pubmed: 3119870
Gu X, Fu YX, Li WH (1995) Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol Biol Evol 12:546–557. https://doi.org/10.1093/oxfordjournals.molbev.a040235
doi: 10.1093/oxfordjournals.molbev.a040235
pubmed: 7659011
Gupta DK, Jahan N, Gupta N (2011) New records of Haemoproteus and Plasmodium (Sporozoa: Haemosporida) of rock pigeon (Columba livia) in India. J Parasit Dis 35:155–168. https://doi.org/10.1007/s12639-011-0044-5
doi: 10.1007/s12639-011-0044-5
pubmed: 23024498
pmcid: 3235393
Haag-Wackernagel D, Moch H (2004) Health hazards posed by feral pigeons. J Infect 48:307–313. https://doi.org/10.1016/j.jinf.2003.11.001
doi: 10.1016/j.jinf.2003.11.001
pubmed: 15066331
Hegemann A, Matson KD, Versteegh MA, Tieleman BI (2012) Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS One 7:e36358. https://doi.org/10.1371/journal.pone.0036358
doi: 10.1371/journal.pone.0036358
pubmed: 22570706
pmcid: 3343055
Hellard E, Cumming GS, Caron A, Coe E, Peters JL (2016) Testing epidemiological functional groups as predictors of avian haemosporidia patterns in southern Africa. Ecosphere 7:e01225. https://doi.org/10.1002/ecs2.1225
doi: 10.1002/ecs2.1225
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. https://doi.org/10.1645/GE-184R1
doi: 10.1645/GE-184R1
pubmed: 15357072
Hellgren O, Waldenström J, Peréz-Tris J et al (2007) Detecting shifts of transmission areas in avian blood parasites - a phylogenetic approach. Mol Ecol 16:1281–1290. https://doi.org/10.1111/j.1365-294X.2007.03227.x
doi: 10.1111/j.1365-294X.2007.03227.x
pubmed: 17391413
Hellgren O, Wood MJ, Waldenström J, Hasselquist D, Ottosson U, Stervander M, Bensch S (2013) Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the garden warbler. J Evol Biol 26:1047–1059. https://doi.org/10.1111/jeb.12129
doi: 10.1111/jeb.12129
pubmed: 23621369
Heym EC, Kampen H, Krone O, Schäfer M, Werner D (2019) Molecular detection of vector-borne pathogens from mosquitoes collected in two zoological gardens in Germany. Parasitol Res 118:2097–2105. https://doi.org/10.1007/s00436-019-06327-5
doi: 10.1007/s00436-019-06327-5
pubmed: 31154526
pmcid: 6611737
Huang X, Huang D, Liang Y et al (2020) A new protocol for absolute quantification of haemosporidian parasites in raptors and comparison with current assays. Parasites Vectors 13:354. https://doi.org/10.1186/s13071-020-04195-y
doi: 10.1186/s13071-020-04195-y
pubmed: 32680557
pmcid: 7368712
Iezhova TA, Dodge M, Sehgal RN, Smith TB, Valkiūnas G (2011) New avian Haemoproteus species (Haemosporida: Haemoproteidae) from African birds, with a critique of the use of host taxonomic information in hemoproteid classification. J Parasitol 97:682–694. https://doi.org/10.1645/GE-2709.1
doi: 10.1645/GE-2709.1
pubmed: 21506819
Jenkins T, Thomas GH, Hellgren O, Owens IPF (2012) Migratory behaviour of birds affects their coevolutionary reationship with blood parasites. Evolution 66:740–751. https://doi.org/10.1111/j.1558-5646.2011.01470.x
doi: 10.1111/j.1558-5646.2011.01470.x
pubmed: 22380437
Jovani R, Tella JL (2006) Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol 22:214–218. https://doi.org/10.1016/j.pt.2006.02.011
doi: 10.1016/j.pt.2006.02.011
pubmed: 16531119
Klei TR, DeGiusti DL (1975) Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. J Wildl Dis 11:130–135. https://doi.org/10.7589/0090-3558-11.1.130
doi: 10.7589/0090-3558-11.1.130
pubmed: 803576
Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23:557–569. https://doi.org/10.1111/j.1420-9101.2009.01920.x
doi: 10.1111/j.1420-9101.2009.01920.x
pubmed: 20070458
Križanauskienė A, Iezhova TA, Sehgal RNM, Carlson JS, Palinauskas V, Bensch S, Valkiūnas G (2013) Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons. Zootaxa 3613:085–094. https://doi.org/10.11646/zootaxa.3616.1.7
Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. J Anim Ecol 80:1196–1206. https://doi.org/10.1111/j.1365-2656.2011.01836.x
doi: 10.1111/j.1365-2656.2011.01836.x
pubmed: 21426343
Lacorte GA, Felix GMF, Pinheiro RRB et al (2013) Exploring the diversity and distribution of Neotropical avian malaria parasites - a molecular survey from Southeast Brazil. PLoS ONE 8:e57770. https://doi.org/10.1371/journal.pone.0057770
doi: 10.1371/journal.pone.0057770
pubmed: 23469235
pmcid: 3585926
Lee KA, Martin LB, Hasselquist D, Ricklefs RE, Wikelski M (2006) Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150:383–392. https://doi.org/10.1007/s00442-006-0537-6
doi: 10.1007/s00442-006-0537-6
pubmed: 16944242
Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
doi: 10.1111/2041-210X.12410
Levin II, Valkiūnas G, Santiago-Alarcon D et al (2011) Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Int J Parasitol 41:1019–1027. https://doi.org/10.1016/j.ijpara.2011.03.014
doi: 10.1016/j.ijpara.2011.03.014
pubmed: 21683082
Levin II, Valkiūnas G, Iezhove 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 98:847–854. https://doi.org/10.1645/GE-3007.1
doi: 10.1645/GE-3007.1
pubmed: 22324933
MalAvi (2020) MalAvi: a database for avian haemosporidian parasites. https://130.235.244.92/Malavi/ Download of the ‘Hosts and Sites Table’, accessed 13.03.2020
Martínez J, Martínez-de La Puente J, Herrero J et al (2009) A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitology 136:713722. https://doi.org/10.1017/S0031182009006118
doi: 10.1017/S0031182009006118
Marx M, Korner-Nievergelt F, Quillfeldt P (2016) Analysis of ring recoveries of European turtle doves Streptopelia turtur - flyways, timing of migration and origins of hunted birds. Acta Orn 51:55–70. https://doi.org/10.3161/00016454AO2016.51.1.005
doi: 10.3161/00016454AO2016.51.1.005
Marzal A, De Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545. https://doi.org/10.1007/s00442-004-1757-2
doi: 10.1007/s00442-004-1757-2
pubmed: 15688214
Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc Royal Soc B 267:2507–2510. https://doi.org/10.1098/rspb.2000.1312
doi: 10.1098/rspb.2000.1312
Merino S, Hennicke J, Martínez J et al (2012) Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 98:388–397. https://doi.org/10.1645/GE-2415.1
doi: 10.1645/GE-2415.1
pubmed: 21992108
Møller AP, Erriyzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953. https://doi.org/10.1023/A:1006516222343
doi: 10.1023/A:1006516222343
PECBMS (2020) Population Trends of Common European Breeding Birds. https://pecbms.info/trends-and-indicators/species-trends/ accessed 23.09.2020
Pulgarín-R PC, Gomez C, Bayly NJ et al (2018) Migratory birds as vehicles for parasite dispersal? Infection by avian haemosporidians over the year and throughout the range of a long-distance migrant. J Biogeogr 46:83–96. https://doi.org/10.1111/jbi.13453
doi: 10.1111/jbi.13453
Quillfeldt P, Arriero E, Martínez J, Masello JF, Merino S (2011) Prevalence of blood parasites in seabirds- a review. Front Zool 8:26. https://doi.org/10.1186/1742-9994-8-26
doi: 10.1186/1742-9994-8-26
pubmed: 22035144
pmcid: 3223496
R Core Team (2016) R: a language and environment for statistical computing. Version 3.2.4. Vienna: R Foundation for Statistical Computing. https://www.Rproject.org/
Rambaut A (2007) FigTree. https://tree.bio.ed.ac.uk/software/figtree/
Reidelbach J, Christl H (2002) A quantitative investigation into the temporal and spatial variations in the emergence of adult blackflies (Diptera: Simuliidae) from the Breitenbach, a small upland stream in Germany. Limnologica 32:206–235. https://doi.org/10.1016/S0075-9511(02)80029-9
doi: 10.1016/S0075-9511(02)80029-9
Reinoso-Pérez MT, Canales-Delgadillo JC, Chapa-Vargas L, Riego-Ruiz L (2016) Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland dominated landscape of the Mexican highland plateau. Parasites Vectors 9:307. https://doi.org/10.1186/s13071-016-1569-3
doi: 10.1186/s13071-016-1569-3
pubmed: 27234000
pmcid: 4882855
Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc Royal Soc B 269:885–892. https://doi.org/10.1098/rspb.2001.1940
doi: 10.1098/rspb.2001.1940
Rintamäki P, Huhta E, Jokimäki J, Squires-Parsons D (1999) Leucocytozoonosis and Trypanosomiasis in Redstarts in Finland. J Wildl Dis 35:603–607. https://doi.org/10.7589/0090-3558-35.3.603
doi: 10.7589/0090-3558-35.3.603
pubmed: 10479101
Rouffaer LO, Steensels M, Verlinden M, Vervaeke M, Boonyarittichaikij R, Martel A, Lambrecht B (2018) Usutu virus epizootic and Plasmodium coinfection in Eurasian Blackbirds (Turdus merula) in Flanders, Belgium. J Wildl Dis 54:859–862. https://doi.org/10.7589/2017-07-163
doi: 10.7589/2017-07-163
pubmed: 29889004
Santiago-Alarcon D, Outlaw DC, Ricklefs RE, Parker PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. Int J Parasitol 40:463–470. https://doi.org/10.1016/j.ijpara.2009.10.003
doi: 10.1016/j.ijpara.2009.10.003
pubmed: 19854196
Scaglione FE, Pregel P, Cannizzo FT, Pérez-Rodríguez AD, Ferroglio E, Bollo E (2015) Prevalence of new and known species of haemoparasites in feral pigeons in northwest Italy. Malar J 14:99. https://doi.org/10.1186/s12936-015-0617-3
doi: 10.1186/s12936-015-0617-3
pubmed: 25888761
pmcid: 4350268
Shurulinkov P, Ilieva M (2009) Spatial and temporal differences in the blood parasite fauna of passerine birds during the spring migration in Bulgaria. Parasitol Res 104:1453–1458. https://doi.org/10.1007/s00436-009-1349-5
doi: 10.1007/s00436-009-1349-5
pubmed: 19190934
Soares L, Young EI, Ricklefs RE (2020) Haemosporidian parasites of resident and wintering migratory birds in The Bahamas. Parasitol Res 119:1563–1572. https://doi.org/10.1007/s00436-020-06646-y
doi: 10.1007/s00436-020-06646-y
pubmed: 32246260
Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23:307–314. https://doi.org/10.1111/j.1600-0587.2000.tb00286.x
doi: 10.1111/j.1600-0587.2000.tb00286.x
Sol D, Jovani R, Torres J (2003) Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135:542–547. https://doi.org/10.1007/s00442-003-1223-6
doi: 10.1007/s00442-003-1223-6
pubmed: 16228253
Tavassoli M, Esmaeilnejad B, Malekifard F, Mardani K (2018) PCR-RFLP detection of Haemoproteus spp. (Haemosporida: Haemoproteidae) in pigeon blood samples from Iran. Bulg J Vet Med 21:429-435. https://doi.org/10.15547/bjvm.2014
Townsend AK, Wheeler SS, Freund D, Sehgal RNM, Boyce WM (2018) Links between blood parasites, blood chemistry, and the survival of nestling American crows. Ecol Evol 8:8779–8790. https://doi.org/10.1002/ece3.4287
doi: 10.1002/ece3.4287
pubmed: 30271545
pmcid: 6157653
Valkiūnas G (2005) Avian malaria parasites and other Haemosporidia. CRC Press
Valkiūnas G, Iezhova TA (2017) Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malar J 16:101. https://doi.org/10.1186/s12936-017-1746-7
doi: 10.1186/s12936-017-1746-7
pubmed: 28253926
pmcid: 5335495
Valkiūnas G, Bairlein F, Iezhova TA, Dolnik OV (2004) Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla. Parasitol Res 93:218–222. https://doi.org/10.1007/s00436-004-1071-2
doi: 10.1007/s00436-004-1071-2
pubmed: 15138804
Valkiūnas G, Bensch S, Iezhova TA, Križanauskienė A, Hellgren O, Bolshakov CV (2006) Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: Microscopy is still essential. J Parasitol 92:418–422. https://doi.org/10.1645/GE-3547RN.1
doi: 10.1645/GE-3547RN.1
pubmed: 16729711
Valkiūnas G, Iezhova TA, Loisseau C, Sehgal RNM (2009) Nested cythochrome b polymerase chain reaction diagnostics detect sporozoites of haemosporidian parasites in peripheral blood of naturally infected birds. J Parasitol 95:1512–1515. https://doi.org/10.1645/GE-2105.1
doi: 10.1645/GE-2105.1
pubmed: 19522549
Valkiūnas G, Iezhova TA, Evans E, Carlson JS, Martínez-Gómez JE, Sehgal RNM (2013) Two new Haemoproteus species (Haemosporida: Haemoproteidae) from columbiform birds. J Parasitol 99:513–521. https://doi.org/10.1645/12-98.1
doi: 10.1645/12-98.1
pubmed: 23240808
von Blotzheim UG, Bauer KM (1994) Handbuch Der Vögel Mitteleuropas, Band. Columbiformes-Piciformes. Aula-Verlag, Wiesbaden, p 9
Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554. https://doi.org/10.1046/j.1365-294X.2002.01523.x
doi: 10.1046/j.1365-294X.2002.01523.x
pubmed: 12144673
Walther EL, Carlson JS, Cornel A, Morris BK, Sehgal RNM (2016) First molecular study of prevalence and diversity of avian haemosporidia in a Central California songbird community. J Ornithol 157:549–564. https://doi.org/10.1007/s10336-015-1301-7
doi: 10.1007/s10336-015-1301-7
Yanga S, Martínez-Goméz JE, Sehgal RNM, Escalante P, Camacho FC, Bell DA (2011) A preliminary survey for avian pathogens in Columbiformes birds on Socorro Island, Mexico. Pac Conserv Biol 17:11–21. https://doi.org/10.1071/PC110011
doi: 10.1071/PC110011
Yoshimura A, Koketsu M, Bando H et al (2014) Phylogenetic comparisons of avian haemospridian parasites from resident and migratory birds in northern Japan. J Wildl Dis 50:235–242. https://doi.org/10.7589/2013-03-071
doi: 10.7589/2013-03-071
pubmed: 24484482
Yule GU (1925) Yule process. Philos Trans R Soc Lond B Biol Sci 213:21–87
doi: 10.1098/rstb.1925.0002
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214. https://doi.org/10.1089/10665270050081478
doi: 10.1089/10665270050081478
pubmed: 10890397
Zwarts L, Bijlsma RG, van der Kamp J, Wymenga E (2009) Living on the edge: wetlands and birds in a changing Sahel. Chapter 32: European turtle dove Streptopelia turtur, 2nd edn. KNNV Publishing, Zeist, pp 378–389
doi: 10.1163/9789004278134_033