Abstract
Using a combination of morphological and molecular data, we describe a new apicomplexan parasite, Isospora svecica sp. n., from the white-spotted bluethroat, Luscinia svecica cyanecula, from the Czech Republic. Oocysts were found in its intestinal tract. Sporulation was exogenous and took 1–3 days. The oocysts were slightly ellipsoidal, of average size 26.17 × 20.33 μm, with a smooth bilayered wall. Micropyle, oocyst residuum, and polar granules were absent. Sporocysts were bottle-shaped, of an average size of 18.82 × 8.82 μm, with a thin, colourless wall. A conspicuous knob-like Stieda body was present. Substieda body was barely visible. Sporocyst residuum was present in the form of granules of various sizes. Sporozoites were banana-shaped and contained large anterior and small posterior refractile bodies. Partial DNA sequences of three genes were obtained from oocysts of Isospora svecica sp. n., being most closely related to other isosporans described from passerines. Little is known about the parasites of the avian family Muscicapidae, including coccidia, a highly prevalent parasitic protist group in all vertebrate classes. Only six species of the genus Isospora have so far been described in Muscicapidae, together with several “Isospora sp.” that in fact most likely represent Isospora lacazei. The newly described Isospora svecica sp. n. differs morphologically from other coccidia reported from muscicapid birds, and represents the first coccidian species described from Luscinia svecica.
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References
Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. PNAS 101:11040–11045
Barnard WP, Ernst JV, Dixon CF (1974) Coccidia of the cotton rat, Sigmodon hispidus, from Alabama. J Parasitol 60:406–414
Barta JR, Schrenzel MD, Carreno RA, Rideout BA (2005) The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. J Parasitol 91:726–727
Berto BP, McIntosh D, Lopez CWG (2014) Studies on coccidian oocysts (Apicomplexa: Eucoccidiorida). Braz J Vet Parasitol 23:1–15
Brooks DR, McLennan DA (1991) Phylogeny, ecology, and behavior. Chicago University Press, Chicago, USA
Carreno RA, Barta JR (1999) An eimeriid origin of isosporoid coccidia with stieda bodies as shown by phylogenetic analysis of small subunit ribosomal RNA gene sequences. J Parasitol 85:77–83
Correia E, Neto JM (2013) Migration strategy of white-spotted bluethroats (Luscinia svecica cyanecula and L. s. nammetum) along the eastern Atlantic route. Ardeola: Rev Ibérica Ornitología 60:245–259
Duszynski DW (1971) Increase in size of Eimeria separata oocysts during patency. J Parasitol 57:948–952
Duszynski DW, Gutiérrez RJ (1981) The coccidia of quail in the United States. J Wildl Dis 17:371–379
Duszynski DW, Wilber PG (1997) A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 83:333–336
Ernst JV, Cooper C Jr, Chobotar B (1969) Isospora boughtoni Volk, 1938 and Isospora sp. (Protozoa: Eimeriidae) from an opossum Didelphis marsupialis. J Wildl Dis 5:406–409
Franzen C, Müller A, Bialek R, Diehl V, Salzberger B, Fätkenheuer G (2000) Taxonomic position of the human intestinal protozoan parasite Isospora belli as based on ribosomal RNA sequences. Parasitol Res 86:669–676
Frenkel JK (1977) Besnoitia wallacei of cats and rodents: with a reclassification of other cyst-forming isosporoid coccidia. J Parasitol 63:611–628
Gardner SI, Duszynski DW (1990) Polymorphism of eimerian oocysts can be a problem in naturally infected hosts: an example from subterranean rodents in Bolivia. J Parasitol 76:805–811
Georgiev BB, Vasileva GP, Bray RA, Gibson DI (2004) The genus Biuterina Fuhrmann, 1902 (Cestoda, Paruterinidae) in the Old World: redescriptions of three species from Palaearctic Passeriformes. Syst Parasitol 57:68–75
Ghimire TR (2010) Redescription of genera of family Eimeriidae Minchin, 1903. Int J Life Sci 4:26–47
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649 Retrieved from: http://www.geneious.com; last accessed on the 18th January 2019
Kučera J (1981) Blood parasites of birds in Central Europe. 3. Plasmodium and Haemoproteus. Folia Parasitologica (Praha) 28:303–312
Kvičerová J, Pakandl M, Hypša V (2008) Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features. Parasitology 135:443–452
Labbé A (1896) Recherches zoologiques, cytologiques et biologiques sur less coccidies. Arch Zool Exp General 24:517–654 In French
Labbé A (1899) Sporozoa. In: Das Tierreich. Eine Zusammenstellung und Kennzeichnung der rezenten Tierformen, Butschli, Berlin, pp 1–180 In German
Lefort V, Longueville JE, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424 Retrieved from: http://www.atgc-montpellier.fr/sms/; last accessed on the 19th January 2019
Levine ND (1982) Isospora passeris n. sp. from the house sparrow Passer domesticus, I. Lacazei, and related apicomplexan protozoa. Trans Am Microsc Soc 101:66–74
Levine ND, Mohan RN (1960) Isospora sp. (Protozoa: Eimeridae) from cattle and its relationship to I. lacazei of the English sparrow. J Parasitol 46:733–741
Long PL, Joyner LP (1984) Problems in the identification of species of Eimeria. J Protozool 31:535–541
Modrý D, Petrželková KJ, Kalousová B, Hasegawa H (2015) Parasites of African great apes. Atlas of coproscopic diagnostics, 1st ed. HPI-Lab, UVPS Brno, Czech Republic
Mutafchiev Y, Kontrimavichus VL, Georgiev BB (2013) Redescriptions and comments on the validity of Acuaria subula and A. skrjabini (Nematoda, Spirurida, Acuariidae), parasites of passerine birds. Acta Parasitol 58:284–296
Mutafchiev Y, Mariaux J, Georgiev BB (2014) Two new species of Quasithelazia Maplestone, 1932 (Nematoda: Acuariidae) from Malaysia, with an amended diagnosis and review of the genus. Syst Parasitol 88:103–117
Ogedengbe ME, El-Sherry S, Ogedengbe JD, Chapman HD, Barta JR (2018) Phylogenies based on combined mitochondrial and nuclear sequences conflict with morphologically defined genera in the eimeriid coccidia (Apicomplexa). Int J Parasitol 48:59–69
Paperna I, Yosef R, Chavatte JM, Landau I (2010) Malarial infections in sedentary and migratory passerine birds in Israel: description of new species. Parassitologia 52:411–422
Paterson AM, Banks J (2001) Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. Int J Parasitol 31:1012–1022
Peev S, Zehtindjiev P, Ilieva M, Träff J, Briedis M, Adamík P (2016) Haemosporidian blood parasite diversity and prevalence in the semi-collared flycatcher (Ficedula semitorquata) from the eastern Balkans. Parasitol Int 65:613–617
Rakhmatullina NK, Svanbaev SK (1972) Infections of wild birds with coccidia. Trudy Instituta Zoologii, Akademaii Nauk Kazhakskoii SSR 33:5–14
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Ryšavý B (1954) Příspěvek k poznání kokcidií našich i dovezených obratlovců. Československá Parasitologie 1:131–174
Sangster G, Alström P, Forsmark E, Olsson U (2010) Multi-locus phylogenetic analysis of Old World chats and flycatchers reveals extensive paraphyly at family, subfamily and genus level (Aves: Muscicapidae). Mol Phylogenet Evol 57:380–392
Scholtyseck E (1954) Untersuchungen uber die bei einheimischen vogelarten vorkommenden Coccidien der Gattung Isospora. Arch Protistenkd 100:91–112 In German
Schwarz RS, Jenkins MC, Klopp S, Miska KB (2009) Genomic analysis of Eimeria spp. populations in relation to performance levels of broiler chicken farms in Arkansas and North Carolina. J Parasitol 95:871–880
Sebaio F, Braga EM, Branquinho F, Fecchio A, Marini MÂ (2012) Blood parasites in passerine birds from the Brazilian Atlantic Forest. Rev Bras Parasitol Vet 21:7–15
Sheather AL (1923) The detection of intestinal protozoa and mange parasites by a flotation technique. J Comp Pathol 36:266–275
Trefancová A, Mácová A, Kvičerová J (2019) Isosporan oocysts in the faeces of bank voles (Myodes glareolus; Arvicolinae, Rodentia): real parasites, or pseudoparasites? Protist 170:104–120
Valkiūnas G, Ilgūnas M, Bukauskaitė D, Palinauskas V, Bernotienė R, Iezhova TA (2017) Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology 144:1726–1735
Acknowledgements
We thank Christopher Mark Steer for language correction of this manuscript. We are grateful to ornithologists Jakub Vlček and Petr Veselý for capture of birds. We also thank Jana Říhová for help during the field studies. We thank John R. Barta (University of Guelph, Ontario, Canada) for providing sequences of primers amplifying the COIII region.
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This work was supported by the Czech Science Foundation (grant number 17-19831S).
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Trefancová, A., Kvičerová, J. Isospora svecica sp. n. (Apicomplexa: Eimeriidae), a new species of coccidium from the white-spotted bluethroat Luscinia svecica cyanecula (Aves: Passeriformes: Muscicapidae). Parasitol Res 118, 3043–3051 (2019). https://doi.org/10.1007/s00436-019-06397-5
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DOI: https://doi.org/10.1007/s00436-019-06397-5