Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-29T06:29:26.041Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular and comparative morphological analysis of central European parasitic flatworms of the superfamily Brachylaimoidea Allison, 1943 (Trematoda: Plagiorchiida)

Published online by Cambridge University Press:  28 January 2016

PETR HENEBERG ,
JILJÍ SITKO  and
JIŘÍ BIZOS
PETR HENEBERG*
Affiliation:
Charles University in Prague, Third Faculty of Medicine, Prague, Czech Republic
JILJÍ SITKO
Affiliation:
Comenius Museum, Moravian Ornithological Station, Přerov, Czech Republic
JIŘÍ BIZOS
Affiliation:
Charles University in Prague, Third Faculty of Medicine, Prague, Czech Republic
*
*Corresponding author: Charles University in Prague, Third Faculty of Medicine, Ruská 87, CZ-100 00 Prague, Czech Republic. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The Brachylaimoidea are digenean parasites of vertebrates, including humans, domestic animals, poultry and wild game. Numerous Brachylaimoidea, particularly adults of Brachylaima and Leucochloridium, are difficult to identify to species. We provide and analyse sequences of two nuclear (18S rDNA, ITS2) and two mitochondrial (CO1, ND1) DNA loci of central European species of the Brachylaimoidea, namely Leucochloridium holostomum, Leucochloridium paradoxum, Leucochloridium perturbatum, Leucochloridium subtilis, Leucochloridium vogtianum, Urotocus rossitensis, Urogonimus macrostomus, Michajlovia migrata, Leucochloridiomorpha lutea, Brachylaima arcuatus, Brachylaima fuscata and Brachylaima mesostoma. We identified three clades in the genus Leucochloridium, which do not correspond to the previously suggested subgenera Neoleucochloridium, Papilloleucochloridium and Leucochloridium. We reject classification of Urotocus and Urogonimus in Leucochloridiinae, and, instead, re-establish the subfamilies Urotocinae and Urogoniminae. We synonymize the genus Renylaima with the genus Brachylaima. We reject M. migrata as a member of Leucochloridiinae sensu stricto or Brachylaimidae suggested by some previous authors. We found that the previously sequenced Glaphyrostomum sp. does not cluster with any hitherto sequenced Brachylaimidae. We also provide comparative measurements of the examined central European Brachylaimoidea, address the the specificity of their localization in the host and discuss their host-specific prevalence and intensity of infections based on the extensive dataset of birds examined in 1962–2015.

Keywords

bursa of FabriciuscloacadiarrhoeaintestinePlatyhelmintheszoonosis
Type
Research Article
Information
Parasitology , Volume 143 , Issue 4 , April 2016 , pp. 455 - 474
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alicata, J. E. (1940). The life cycle of Postharmostomum gallinum, the cecal fluke of poultry. The Journal of Parasitology 26, 135–143.Google Scholar
Allison, L. N. (1943). Leucochloridiomorpha constantiae (Mueller) (Brachylaemidae), its life cycle and taxonomic relationships among digenetic trematodes. Transactions of the American Microscopical Society 62, 127–168.Google Scholar
Bakke, T. A. (1978). Urogonimus macrostomus (Rudolphi, 1803) (Digenea): its taxonomy and morphology as revealed by light and scanning electron microscopy. Canadian Journal of Zoology 56, 2280–2291.Google Scholar
Balozet, L. (1937). Brachylaemus suis Mihi, 1936, trématode de l'intestin du porc. Rôle pathogène et cycle évolutif. Archives de l'Institut Pasteur de Tunis 26, 36–67.Google Scholar
Baruš, V., Ryšavý, B. and Groschaft, J. (1969). The helminths of the turkey (Meleagris gallopavo f. dom) in Cuba. Helminthologia 10, 347–360.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, 165–173.Google Scholar
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, 5125–5144.CrossRefGoogle ScholarPubMed
Butcher, A. R. and Grove, D. I. (2001). Description of the life cycle stages of Brachylaima cribbi n. sp. (Digenea: Brachylaimidae) derived from eggs recovered from human faeces in Australia. Systematic Parasitology 49, 211–221.Google Scholar
Butcher, A. R., Talbot, G. A., Norton, R. E., Kirk, M. D., Cribb, T. H., Forsyth, J. R., Knight, B. and Cameron, A. S. (1996). Locally acquired Brachylaima sp. (Digenea: Brachylaimidae) intestinal fluke infection in two South Australian infants. The Medical Journal of Australia 164, 475–478.Google Scholar
Butcher, A. R., Parasuramar, P. S., Thompson, C. S. and Grove, D. I. (1998). First report of the isolation of an adult worm of the genus Brachylaima (Digenea: Brachylaimidae) from the gastrointestinal tract of a human. International Journal for Parasitology 28, 607–610.Google Scholar
Casey, S. P., Bakke, T. A., Harris, P. D. and Cable, J. (2003). Use of ITS rDNA for discrimination of European green- and brown-banded sporocysts within the genus Leucochloridium Carus, 1835 (Digenea: Leucochloriidae). Systematic Parasitology 56, 163–168.Google Scholar
de Faria Duarte, M. J. (1980). O ciclo evolutivo de Postharmostomum gallinum Witenberg, 1923, no Estado do Rio de Janeiro, Brasil (Trematoda, Brachylaemidae). Revista Brasileira de Biologia 40, 793–809.Google Scholar
Gibson, D. (2015). Fauna Europaea: Gymnophalloidea. Fauna Europaea version 2.6·2. http://www.faunaeur.org/full_results.php?id=16320; cited as 2-Jul-2015.Google Scholar
Gibson, D. I., Jones, A. and Bray, R. A. (2002). Keys to the Trematoda, vol. 1, CABI Publishing and Natural History Museum, Wallingford and London.Google Scholar
Gibson, D. I., Bray, R. A. and Harris, E. A. (2015). Host-parasite database of the Natural History Museum, London. http://www.globalspecies.org/; cited as 23-Jun-2015.Google Scholar
Gvozdev, E. V. (1953). New trematodes of gallinaceous birds of Kazakhsthan. Trudy Instituta Zoologii. Akademiya Nauk Kazakhskoi SSR 1, 175–181. (in Russian)Google Scholar
Harkema, R. (1939). A new species of Brachylaemus from the barred owl. The Journal of Parasitology 25, 277.Google Scholar
Heneberg, P., Rojas, A., Bizos, J., Kocková, L., Malá, M. and Rojas, D. (2014). Focal Philophthalmus gralli infection possibly persists in Melanoides tuberculata over two years following the definitive hosts’ removal. Parasitology International 63, 802–807.Google Scholar
Heneberg, P., Sitko, J. and Bizos, P. (2015). Integrative taxonomy of central European parasitic flatworms of the family Prosthogonimidae Lühe, 1909 (Trematoda: Plagiorchiida). Parasitology International 64, 264–273.Google Scholar
Hodasi, J. K. (1967). Digenetic trematodes from the domestic fowl in Ghana. Journal of Helminthology 41, 329–336.Google Scholar
Iwaki, T., Okamoto, M. and Nakamori, J. (2009). Urogonimus macrostomus (Digenea: Leucochloridiidae) from the rustic bunting, Emberiza rustica, in Japan. Parasitology International 58, 303–305.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, 191–200.Google Scholar
Joyeux, C., Baer, J. G. and Timon-David, J. (1934). Recherches sur les trematodes du genre Brachylaemus Dujardin (syn. Harmostomum Braun). Bulletin Biologique de la France et de la Belgique 68, 385–418.Google Scholar
Locke, S. A., Lapierre, A. R., Byers, K., Proctor, H., McLaughlin, J. D. and Marcogliese, D. J. (2012). Molecular and morphological evidence for the Holarctic distribution of Urogonimus macrostomus (Rudolphi, 1803) Monticelli, 1888 (Digenea: Leucochloridiidae). The Journal of Parasitology 98, 880–882.Google Scholar
Machalska, J. (1978). The morphological variability and taxonomic status of Urogonimus macrostomus (Rudolphi, 1803) (Trematoda, Leucochloridiidae). Acta Parasitologica Polonica 26, 1–9.Google Scholar
Mira, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, S. (2005). Molecular genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801.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, 493–502.Google Scholar
Okulewicz, J. (1991). Trematodes of birds from Lower Silesia. III. Urotocus rossitensis (Mühling, 1898) – New for Poland species of trematode parasitism in passeriform birds. Wiadomości parazytologiczne 37, 471–480. (in Polish)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, 733–755.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, 91–98.Google Scholar
Pojmańska, T. (1973). Michajlovia migrata gen. n., sp. n. (Trematoda, Brachylaimata) – the morphology of the adult. Acta Parasitologica Polonica 21, 9–20.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, 451–474.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, 2535–2540.Google Scholar
Rząd, I., Hofsoe, P., Panicz, R. and Nowakowski, J. K. (2014). Morphological and molecular characterization of adult worms of Leucochloridium paradoxum Carus, 1835 and L. perturbatum Pojmańska, 1969 (Digenea: Leucochloridiidae) from the great tit, Parus major L., 1758 and similarity with the sporocyst stages. Journal of Helminthology 88, 506–510.Google Scholar
Sirgel, W. F. and Mas-Coma, S. (2010). Renylaima capensis n. gen., n. sp. (Trematoda: Brachylaimidae) from the urinary system of the shrew Myosorex varius Smuts, 1832 (Insectivora: Soricidae). Parasitology Research 106, 1443–1453.Google Scholar
Sirgel, W. F., Artigas, P., Bargues, M. D. and Mas-Coma, S. (2012). Life cycle of Renylaima capensis, a brachylaimid trematode of shrews and slugs in South Africa: two-host and three-host transmission modalities suggested by epizootiology and DNA sequencing. Parasites & Vectors 5, 169.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, 512–526.Google ScholarPubMed
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, 2731–2739.Google Scholar
Timon-David, J. (1957). Recherches expérimentales sur le cycle evolutif d'un trematode du genre Urotocus Looss (Digenea, Leucochloridiidae). Annales de Parasitologie Humaine et Comparée 32, 219–242.Google Scholar
Yamaguti, S. (1958). Systema Helminthum, vol. 1. The digenetic trematodes of vertebrates, Interscience Publishers, New York.Google Scholar
Zhukova, A. A., Prokhorova, E. E., Tsymbalenko, N. V., Tokmakova, A. S. and Ataev, G. L. (2012). Molecular genetic analysis of trematodes of the genus Leucochloridium dwelling in the territory of Leningrad Province. Parazitologia 46, 414–419. (in Russian)Google Scholar
Supplementary material: File

Heneberg supplementary material

Heneberg supplementary material 1

Download Heneberg supplementary material(File)
File 64.9 KB