Factors influencing a common but neglected blood parasite prevalence in breeding populations of passerines
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články
PubMed
39865904
PubMed Central
PMC12089444
DOI
10.1017/s0031182025000095
PII: S0031182025000095
Knihovny.cz E-zdroje
- Klíčová slova
- Acrocephalidae, Apicomplexa, Lankesterellidae, Paridae, avian haemoparasites, coccidia, host–parasite interaction, passerines,
- MeSH
- chov MeSH
- Haemosporida * izolace a purifikace MeSH
- nemoci ptáků * parazitologie epidemiologie MeSH
- Passeriformes * parazitologie MeSH
- prevalence MeSH
- protozoální infekce zvířat * epidemiologie parazitologie MeSH
- sexuální faktory MeSH
- věkové faktory MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
The occurrence of avian blood protists is affected by multiple factors that include the characteristics of the hosts, the vectors, the parasites, as well as the environmental factors. This study provides an insight into some of the factors that influence the prevalence of avian Lankesterella, neglected but common blood parasites in breeding populations of common passerines. The highest prevalences of Lankesterella infection were observed in 1 great tit (Parus major) population at 63%, 1 blue tit (Cyanistes caeruleus) population at 49% and a sedge warbler (Acrocephalus schoenobaenus) population at 33%. Prevalence was found to be significantly influenced by sampling site followed by host age, species and sex. Julian date had no significant effect on Lankesterella prevalence. Prevalence data from different sampling sites can reveal different patterns and should be combined critically. Higher prevalence in adults suggest that the infections are chronic, which helps the parasite to persist in host populations. The differences between sexes might be related to different exposure to the transmitting vectors (e. g., mites or mosquitoes) during breeding.
Zobrazit více v PubMed
Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, del CJ, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA, Hoppenrath M, James TY, Karnkowska A, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJ, Lara E and Le Gall L (2018) Revisions to the Classification, nomenclature, and diversity of Eukaryotes. Journal of Eukaryotic Microbiology 66, 4–119. doi:10.1111/jeu.12691. PubMed DOI PMC
Biedrzycka A, Kloch A, Migalska M and Bielański W (2013) Molecular characterization of putative Hepatozoon sp. from the sedge warbler (Acrocephalus schoenobaenus). Parasitology 140, 695–698. doi:10.1017/S0031182012002004. PubMed DOI
Calero-Riestra M and García JT (2016) Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the Tawny pipit, Anthus campestris. Malaria Journal 15, 1–11. PubMed PMC
Castaño‐Vázquez F and Merino S (2022) Differential effects of environmental climatic variables on parasite abundances in blue tit nests during a decade. Integrative Zoology 17, 511–529. PubMed PMC
Cepák J, Klvaña P, Škopek J, Schropfer L, Jelínek M, Hořák D, Formánek J and Zárybnický J eds (2008) Atlas Migrace Ptáků České Republiky a Slovenska. Praha: Aventinum.
Chagas CRF, Binkienė R and Valkiūnas G (2021b) Description and molecular characterization of two species of avian blood parasites, with remarks on circadian rhythms of avian haematozoa infections. Animals 11, 3490. doi:10.3390/ani11123490. PubMed DOI PMC
Chagas CRF, Harl J, Preikša V, Bukauskaitė D, Ilgūnas M, Weissenböck H and Valkiūnas G (2021a) Lankesterella (Apicomplexa, Lankesterellidae) blood parasites of Passeriform birds: Prevalence, molecular and morphological characterization, with notes on sporozoite persistence in vivo and development in vitro. Animals 11, 1451. doi:10.3390/ANI11051451. PubMed DOI PMC
Che-Ajuyo NMA, Liu B, Deng Z, Rao X, Dong L and Liang W (2023) Sex-biased, but not plumage color-based, prevalence of haemosporidian parasites in free-range chickens. Parasitology International 93, 102722. PubMed
Desser SS (1993) The Haemogregarinidae and Lankesterellidae. New York, USA: Parasitic protozoa, Academic Press, 4(2), 265–269. doi:10.1016/B9780-12-426014-6.50009-0 DOI
Drechsler RM, Belliure J and Megía-Palma R (2021) Phenological and intrinsic predictors of mite and haemacoccidian infection dynamics in a Mediterranean community of lizards. Parasitology 148, 1328–1338. PubMed PMC
Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA and Voelker G (2014) Does the niche breadth or trade‐off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 3322–3329. PubMed
Eastwood JR, Peacock L, Hall ML, Roast M, Murphy SA, da Silva AG and Peters A (2019) Persistent low avian malaria in a tropical species despite high community prevalence. International Journal for Parasitology: Parasites and Wildlife 8, 88–93. PubMed PMC
Ellis VA, Huang X, Westerdahl H, Jönsson J, Hasselquist D, Neto JM, Nilsson J-Å, Nilsson J, Hegemann A, Hellgren O and Bensch S (2020) Explaining prevalence, diversity and host specificity in a community of avian haemosporidian parasites. Oikos 129, 1314–1329.
Emmenegger T, Alves JA, Rocha AD, Costa JS, Schmid R, Schulze M and Hahn S (2020) Population- and age-specific patterns of haemosporidian assemblages and infection levels in European bee-eaters (Merops apiaster). International Journal for Parasitology 50, 1125–1131. PubMed
Fecchio A, Clark NJ, Bell JA, Skeen HR, Lutz HL, De La Torre GM, Vaughan JA, Tkach VV, Schunck F, Ferreira FC, Braga ÉM, Lugarini C, Wamiti W, Dispoto JH, Galen SC, Kirchgatter K, Sagario MC, Cueto VR, González-Acuña D and Wells K (2021) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecology and Biogeography 30, 2393–2406. doi:10.1111/geb.13390. DOI
Fecchio A, Lima MR, Silveira P, Ribas ACA, Caparroz R and Marini MÂ (2015) Age, but not sex and seasonality, influence Haemosporida prevalence in White-banded Tanagers (Neothraupis fasciata) from central Brazil. Canadian Journal of Zoology 93, 71–77. doi:10.1139/cjz-2014-0119. DOI
Fialová M, Santolíková A, Brotánková A, Brzoňová J and Svobodová M (2021) Complete life cycle of Trypanosoma thomasbancrofti, an avian trypanosome transmitted by Culicine mosquitoes. Microorganisms 9, 2101. doi:10.3390/microorganisms9102101. PubMed DOI PMC
Granthon C and Williams DA (2017) Avian malaria, body condition, and blood parameters in four species of songbirds. The Wilson Journal of Ornithology 129, 492–508.
Grieves LA, Balogh L, Kelly TR and MacDougall-Shackleton EA (2023) Haemosporidian infection prevalence varies temporally and spatially and Leucocytozoon infections are male biased in Song Sparrows. Ornithology 140, ukad008. doi:10.1093/ornithology/ukad008. DOI
Griffiths R, Double MC, Orr K and Dawson RJ (1998) A DNA test to sex most birds. Molecular Ecology 7, 1071–1075. doi:10.1046/j.1365-294x.1998.00389.x. PubMed DOI
Huang X, Jönsson J and Bensch S (2020) Persistence of avian haemosporidians in the wild: A case study to illustrate seasonal infection patterns in relation to host life stages. International Journal for Parasitology 50, 611–619. PubMed
Keckeisen C, Šujanová A, Himmel T, Matt J, Nedorost N, Chagas CRF, Weissenböck H and Harl J (2024) Isospora and Lankesterella parasites (Eimeriidae, Apicomplexa) of Passeriform birds in Europe: Infection rates, phylogeny, and pathogenicity. Pathogens 13, 337. doi:10.3390/pathogens13040337. PubMed DOI PMC
Knowles SCL, Wood MJ, Alves R, Wilkin TA, Bensch S and Sheldon BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20, 1062. PubMed
Kuznetsova A, Brockhoff PB and Christensen RHB (2017) lmerTest Package: Tests in linear mixed effects models. Journal of Statistical Software 82, 1–26. doi:10.18637/jss.v082.i13. DOI
Martínez J, Merino S, Badás EP, Almazán L, Moksnes A and Barbosa A (2018) Hemoparasites and immunological parameters in snow bunting (Plectrophenax nivalis) nestlings. Polar Biology 41, 1855–1866. doi:10.1007/s00300-018-2327-0. DOI
Maziarz M, Broughton RK and Wesołowski T (2017) Microclimate in tree cavities and nest-boxes: Implications for hole-nesting birds. Forest Ecology and Management 389, 306–313.
McCurdy DG, Shutler D, Mullie A and Forbes MR (1998) Sex-biased parasitism of avian hosts: Relations to blood parasite taxon and mating system. Oikos 82, 303–312. doi:10.2307/3546970. DOI
Megía-Palma R, Martínez J, Nasri I, Cuervo JJ, Martín J, Acevedo I, Belliure J, Ortega J, García-Roa R, Selmi S and Merino S (2016) Phylogenetic relationships of Isospora, Lankesterella, and Caryospora species (Apicomplexa: Eimeriidae) infecting lizards. Organisms Diversity and Evolution 16, 275–288. doi:10.1007/s13127-015-0253-3. DOI
Megía-Palma R, Paranjpe D, Reguera S, Martínez J, Cooper RD, Blaimont P, Merino S and Sinervo B (2018) Multiple color patches and parasites in Sceloporus occidentalis: Differential relationships by sex and infection. Current Zoology 64, 703–711. doi:10.1093/cz/zoy007. PubMed DOI PMC
Merino S, Martínez J, Martínez-de la Puente J, Criado-Fornelio Á, Tomás G, Morales J and García-Fraile S (2006) Molecular characterization of the 18S rDNA gene of an avian Hepatozoon reveals that it is closely related to Lankesterella. Journal of Parasitology 92, 1330–1335. PubMed
Norris K, Anwar M and Read AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. Journal of Animal Ecology 63, 601–610. doi:10.2307/5226. DOI
Norris K and Evans MR (2000) Ecological immunology: Life history trade-offs and immune defence in birds. Behavioral Ecology 11, 19–26. doi:10.1093/beheco/11.1.19. DOI
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/.
Rodriguez MD, Doherty PF, Piaggio AJ and Huyvaert KP (2021) Sex and nest type influence avian blood parasite prevalence in a high-elevation bird community. Parasites and Vectors 14, 145. doi:10.1186/s13071-021-04612-w. PubMed DOI PMC
Schultz A, Underhill LG, Earlé RA and Underhill G (2010) Infection prevalence and absence of positive correlation between avian haemosporidian parasites, mass and body condition in the Cape Weaver Ploceus capensis. Ostrich 81, 69–76. doi:10.2989/00306521003690630. DOI
Slowinski SP, Geissler AJ, Gerlach N, Heidinger BJ and Ketterson ED (2022) The probability of being infected with haemosporidian parasites increases with host age but is not affected by experimental testosterone elevation in a wild songbird. Journal of Avian Biology. doi:10.1111/jav.02819. DOI
Storchová L and Hořák D (2018) Life-history characteristics of European birds. Global Ecology and Biogeography 27, 400–406. doi:10.1111/geb.12709. DOI
Svobodová M, Čepička I, Zídková L, Kassahun A, Votýpka J, Peške L, Hrazdilová K, Brzoňová J, Voříšek P and Weidinger K (2023) Blood parasites (Trypanosoma, Leucocytozoon, Haemoproteus) in the Eurasian sparrowhawk (Accipiter nisus): Diversity, incidence and persistence of infection at the individual level. Parasites & Vectors 16, 15. doi:10.1186/s13071-022-05623-x. PubMed DOI PMC
Svobodová M, Weidinger K, Peške L, Volf P, Votýpka J and Voříšek P (2015) Trypanosomes and haemosporidia in the buzzard (Buteo buteo) and sparrowhawk (Accipiter nisus): Factors affecting the prevalence of parasites. Parasitology Research 114, 551–560. PubMed
Synek P, Popelková A, Koubínová D, Šťastný K, Langrová I, Votýpka J and Munclinger P (2016) Haemosporidian infections in the Tengmalm’s Owl (Aegolius funereus) and potential insect vectors of their transmission. Parasitology Research 115, 291–298. PubMed
Valkiūnas G (2005) Avian Malaria Parasites and Other Haemosporidia. London: CRC Press.
Valkiūnas G, Bairlein F, Iezhova TA and 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. Parasitology Research 93, 218–222. PubMed
Venkatachalam AKSB, Čepička I, Hrazdilová K and Svobodová M (2023) Host specificity of passerine Lankesterella (Apicomplexa: Coccidia). European Journal of Protistology 90, 126007. doi:10.1016/j.ejop.2023.126007. PubMed DOI
Ventim R, Tenreiro P, Grade N, Encarnaçao P, Araújo M, Mendes L and Ramos JA (2012) Characterization of haemosporidian infections in warblers and sparrows at south-Western European reed beds. Journal of Ornithology 153, 505–512.
Votýpka J, Synek P and Svobodová M (2009) Endophagy of biting midges attacking cavity nesting birds. Medical and Veterinary Entomology 23, 277–280. PubMed
Wilkinson LC, Handel CM, Van Hemert C, Loiseau C and Sehgal RN (2016) Avian malaria in a boreal resident species: Long-term temporal variability, and increased prevalence in birds with avian keratin disorder. International Journal for Parasitology 46, 281–290. PubMed
Wood MJ, Cosgrove CL, Wilkin TA, Knowles SC, Day KP and Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273. PubMed
Yang G, Peng Y, Wang H, Huang X and Dong L (2023) Nowhere to escape: The cross‐age avian haemosporidian exposure of migrants in northeast China. Journal of Avian Biology 2023, e03091. doi:10.1111/jav.03091. DOI
Yusupova DA, Schumm YR, Sokolov AA and Quillfeldt P (2023) Haemosporidian blood parasites of passerine birds in north-western Siberia. Polar Biology 46, 497–511.
Zuk M and McKean KA (1996) Sex differences in parasite infections: Patterns and processes. International Journal for Parasitology 26, 1009–1024. PubMed