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Central European parasitic flatworms of the Cyclocoelidae Stossich, 1902 (Trematoda: Plagiorchiida): molecular and comparative morphological analysis suggests the reclassification of Cyclocoelum obscurum (Leidy, 1887) into the Harrahium Witenberg, 1926

Published online by Cambridge University Press:  10 November 2016

JILJÍ SITKO
Affiliation:
Comenius Museum, Moravian Ornithological Station, Přerov, Czech Republic
JIŘÍ BIZOS
Affiliation:
Third Faculty of Medicine, Charles University, Prague, Czech Republic
PETR HENEBERG*
Affiliation:
Third Faculty of Medicine, Charles University, Prague, Czech Republic
*
*Corresponding author: Third Faculty of Medicine, Charles University, Ruská 87, CZ-100 00 Prague, Czech Republic. E-mail: [email protected]

Summary

Cyclocoelidae Stossich, 1902 are medium-sized to large digenean bird parasites. Although these parasites bear few visible autapomorphic signs, and their diagnostic characters are unstable in response to the pressure applied during preparation, the numerous hitherto suggested re-classifications within the family have not been supported by any molecular analysis. We analyse here cyclocoelids found during the extensive examination of central European birds performed from 1962 to 2016, provide comparative measurements, host spectra, prevalence and intensity, and provide and analyse sequences of four DNA loci of five of the cyclocoelid species. Cyclocoleum Brandes, 1892 appears paraphyletic; thus we suggest the re-classification of Cyclocoleum obscurum (Leidy, 1887) as Harrahium obscurum (Leidy, 1887) Sitko and Heneberg comb. n. Molecular phylogenetics questioned also the validity of Cyclocoelinae Stossich, 1902 and Hyptiasminae Dollfus, 1948, which formed a single clade, whereas Allopyge Johnston, 1913, Prohyptiasmus Witenberg, 1923 and Morishitium Witenberg, 1928 formed another clade. Haematotrephinae Dollfus, 1948 are newly characterized as having a pretesticular or intertesticular ovary that forms a triangle with the testes. Analyses of non-European genera of the Cyclocoelidae and an examination of the position of families within Echinostomata La Rue, 1926 are needed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Bashkirova, E. I. (1950). Family Cyclocoelidae Kossack, 1911. Osnovy Trematodologii 4, 329493.Google Scholar
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle ScholarPubMed
Bray, R. A., Littlewood, D. T. J., Herniov, E. A., Williams, B. and Henderson, R. E. (1999). Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology 119, 51255144.Google Scholar
Buša, V. (1960). Finding of the trematode Hyptiasmus arcuatus (Stossich, 1902) Kossack, 1911 in domestic goose Anser anser dom. (L.) in Slovakia. Biológia 15, 546552 [in Slovak].Google Scholar
Bykhovskaya-Pavlovskaya, I. E. (1949). Variability in morphological characters and its importance in the systematics of trematodes of the family Cyclocoelidae. Parazitologiceskyi Sbornik Zoologiceskego Instituta Akademii Nauk SSSR 11, 960 [in Russian].Google Scholar
Dronen, N. (2007). Revision of the family Cyclocoelidae Stossich, 1902 with the proposal of two new subfamilies and the description of a new species of Morishitium Witenberg, 1928 from the common snipe, Gallinago gallinago, from Texas, U.S.A. Zootaxa 1563, 5568.CrossRefGoogle Scholar
Dronen, N. O. and Blend, C. K. (2015). Updated keys to the genera in the subfamilies of Cyclocoelidae Stossich, 1902, including a reconsideration of species assignments, species keys and the proposal of a new genus in Szidatitreminae Dronen, 2007. Zootaxa 4053, 1100.Google Scholar
Dronen, N. O. and Tkach, V. V. (2014). Key to the species of Morishitium Witenberg, 1928 (Cyclocoelidae), with the description of a new species from the red-billed blue magpie Urocissa erythrorhyncha (Boddaert) (Corvidae) from Guizhou Province, People's Republic of China. Zootaxa 3835, 273282.Google Scholar
Dubois, G. (1959). Revision des Cyclocoelidae Kossack 1911 (Trematoda). Revue Suisse de Zoologie 66, 67147.Google Scholar
Feizullaev, N. A. (1980). Trematody nadsemejstva Cyclocoeloidea: morfologija, biologija, filogenija i sistematika. Elm, Baku, USSR.Google Scholar
Gibson, D. I., Bray, R. A. and Harris, E. A. (2016). Host–parasite Database of the Natural History Museum, London. http://www.globalspecies.org/; cited as 20-Jul-2016.Google Scholar
Harrah, E. C. (1922). North American monostomes primarily from freshwater hosts. Illinois Biological Monographs 7, 162165.Google Scholar
Jacobs, D. E., Zhu, X., Gasser, R. B. and Chilton, N. B. (1997). PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Tropica 68, 191200.CrossRefGoogle ScholarPubMed
Kanev, I., Radev, V. and Fried, B. (2002). Family Cyclocoelidae Stossich, 1902. In Keys to Trematoda 1 (ed. Gibson, D. I., Jones, A. and Bray, R. A.), pp. 131145. CABI Publishing, Wallingford, and The Natural History Museum, London, UK.Google Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.Google Scholar
Kossack, W. F. K. (1911). Über Monostomiden. Zoologische Jahrbücher Abteilung für Systematik, Geographie und Biologie der Tiere 31, 491590.Google Scholar
Libert, C., Jouet, D., Ferte, H., Lemberger, K. and Keck, N. (2012). Air sac fluke Circumvitellatrema momota in a captive blue-crowned motmot (Momotus momota) in France. Journal of Zoo and Wildlife Medicine 43, 689692.Google Scholar
Littlewood, D. T. J. and Bray, R. A. (2001). Interrelationships of the Platyhelminthes. Taylor & Francis, London, UK.Google Scholar
Machalska, J. (1980a). Cyclocoelum polonicum sp. n. (Trematoda, Cyclocoelidae) from the thrushes Turdus philomelos Br. and T. merula L. Acta Parasitologia Polonica 26, 129136.Google Scholar
Machalska, J. (1980b). Helminth fauna of birds of the genus Turdus examined during their spring and autumn migration. I. Digenea. ActaParasitologica Polonica 27, 153172.Google Scholar
Macko, J. K. (1960). On the variability of Haematotrephus lanceolatum (Wedl, 1858) from Numenius phaeophus (L.). Helminthologia 2, 280285 [in German].Google Scholar
Macko, J. K., Špakulová, M., Vasilková, Z. and Oros, M. (2011). Description of new morphological form of Skrjabinocoelum petrowi f. pannoniensis (Trematoda, Cyclocoelidae), a rare parasite of jack snipe (Lymnocryptes minimus, Charadriiformes) in Slovakia. Folia Faunistica Slovaca 16, 7376.Google Scholar
Morgan, J. A. and Blair, D. (1998). Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. International Journal for Parasitology 28, 493502.Google Scholar
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.Google Scholar
Otranto, D., Rehbein, S., Weigl, S., Cantacessi, C., Parisi, A., Lia, R. P. and Olson, P. D. (2007). Morphological and molecular differentiation between Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium chinensis (Sudarikov and Ryjikov, 1951) Tang and Tang, 1978 (Platyhelminthes: Digenea). Acta Tropica 104, 9198.Google Scholar
Řezáč, M., Gasparo, F., Král, J. and Heneberg, P. (2014). Integrative taxonomy and evolutionary history of a newly revealed spider Dysdera ninnii complex (Araneae: Dysderidae). Zoological Journal of the Linnean Society 172, 451474.Google Scholar
Routtu, J., Grunberg, D., Izhar, R., Dagan, Y., Guttel, Y., Ucko, M. and Ben-Ami, F. (2014). Selective and universal primers for trematode barcoding in freshwater snails. Parasitology Research 113, 25352540.Google Scholar
Rząd, I., Sitko, J., Wysocki, D. and Stępniewski, K. (2011). Digenean trematodes from six species of birds (Passeriformes, Piciformes and Strigiformes) from north-western Poland. Wiadomości Parazytologiczne 57, 271276.Google Scholar
Rząd, I., Sitko, J., Sałamantin, R. and Wysocki, D. (2014). Helminth community structure study on urban and forest blackbird (Turdus merula L.) populations in relation to seasonal bird migration on the south Baltic Sea coast (NW Poland). Helminthologia 51, 117129.Google Scholar
Sitko, J. (1969). Findings of trematodes (Trematoda) in wild birds of Czechoslovakia. Acta Societatis Zoologicae Bohemoslovacae 33, 7987.Google Scholar
Sitko, J., Faltýnková, A. and Scholz, T. (2006). Checklist of the Trematodes (Digenea) of birds of the Czech and Slovak Republics. Academia, Prague, Czech Republic.Google Scholar
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Timon-David, J. (1955). Cycle évolutif d´un trematode Cyclocoelidae: Pseudohyptiasmus dollfusi Timon-David, 1950. Recherches expérimentales. Annales de Parasitologie 30, 4361.Google Scholar
Timon-David, J. (1957). Nouvelles recherches expérimentales dur le cycle évolutif du trematode Pseudohyptiasmus dollfusi Timon-David (Digenea: Cyclocoeliidae). Comptes Rendus de la Société de Biologie 151, 592594.Google Scholar
Tkach, V. V., Kudlai, O. and Kostadinova, A. (2016). Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171185.Google Scholar
Vojtěchovská-Mayerová, M. (1952). New findings of parasitic worms in our birds. Acta Societatis Zoologicae Bohemoslovacae 16, 7188 [in Czech, with English summary].Google Scholar
Witenberg, G. G. (1923). The trematodes of the family Cyclocoelidae and a new principle of their systematics. Trudy Gosudarstvennogo Instituta Eksperimentalnoi Veterinarii 1, 84141 [in Russian].Google Scholar
Witenberg, G. G. (1926). Trematoden der Familie Cyclocoelidae Kossack, 1911. Beitrag zur Kenntnis der Helminthenfauna Russlands. Zoologische Jahrbücher. Abteilung für Systematik Ökologie und Geographie der Tiere 52, 103186.Google Scholar
Yamaguti, S. (1971). Synopsis of Digenetic Trematodes of Vertebrates, Vol. I. Keigaku Publishing Company, Tokyo, Japan.Google Scholar
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