Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-26T04:02:32.000Z Has data issue: false hasContentIssue false
  • English
  • Français

Central European parasitic flatworms of the family Renicolidae Dollfus, 1939 (Trematoda: Plagiorchiida): molecular and comparative morphological analysis rejects the synonymization of Renicola pinguis complex suggested by Odening

Published online by Cambridge University Press:  30 June 2016

PETR HENEBERG ,
JILJÍ SITKO ,
JIŘÍ BIZOS  and
ELIZABETH C. HORNE
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
ELIZABETH C. HORNE
Affiliation:
Penguins Eastern Cape Marine Rehabilitation Centre, Cape St. Francis, South Africa
*
*Corresponding author: Charles University in Prague, Third Faculty of Medicine, Ruská 87, CZ-100 00 Prague, Czech Republic. Tel: ++420–775 311 177. Fax: ++420–267 162 710. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The Renicolidae are digenean parasites of piscivorous and molluscivorous birds. Although they exhibit few morphological autapomorphies and are highly variable, the numerous suggested re-classifications within the family have never been supported by any molecular analyses. We address the possible synonymization of species within the Renicola pinguis complex suggested previously by Odening. We provide and analyse sequences of two nuclear (ITS2, 28S rDNA) and two mitochondrial (CO1, ND1) DNA loci of central European species of the Renicolidae, namely Renicola lari, Renicola pinguis and Renicola sternae sp. n., and we also provide first sequences of Renicola sloanei. The combined molecular and comparative morphological analysis confirms the previously questioned validity of the three Renicola spp. of highly similar morphology, which display strict niche separation in terms of host specificity and selectivity. We identify two previously unreported clades within the genus Renicola; however, only one of them is supported by the analysis of adult worms. We also provide comparative measurements of the three examined closely related central European renicolids, and describe the newly proposed tern-specialized species Renicola sternae sp. n., which was previously repeatedly misidentified as Renicola paraquinta. Based on the extensive dataset collected in 1962–2015, we update the host spectrum of Renicolidae parasitizing central European birds (Renicola bretensis, R. lari, Renicola mediovitellata, R. pinguis, Renicola secunda and R. sternae sp. n.) and discuss their host-specific prevalence and intensity of infections.

Keywords

kidneyLittorina littoreaMytilus edulisPlatyhelminthesrenalureter
Type
Research Article
Information
Parasitology , Volume 143 , Issue 12 , October 2016 , pp. 1592 - 1604
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

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
Bykhovskaya-Pavlovskaya, I. E. (1962). [Trematodes of Birds of USSR]. Izdatelstvo Akademii Nauk SSSR, Moscow, Leningrad. (in Russian).Google Scholar
Campbell, N., Cross, M. A., Chubb, J. C., Cunningham, C. O., Hatfield, E. M. and MacKenzie, K. (2007). Spatial and temporal variations in parasite prevalence and infracommunity structure in herring (Clupea harengus L.) caught to the west of the British Isles and in the North and Baltic Seas: implications for fisheries science. Journal of Helminthology 81, 137–146.Google Scholar
Dollfus, R.-P. (1946). Sur un Distome du genre Tamerlania K. I. Skrjabin, 1924, avec un catalogue des trematodes des reins d'oiseaux. Annales de Parasitologie Humaine et Comparée 21, 25–73.Google Scholar
Gibson, D. I. (2008). Family Renicolidae Dollfus, 1939. In Keys to Trematoda 3 (eds. Gibson, D. I., Bray, R. A. and Jones, A.), pp. 591–594. CABI Publishing, Wallingford, and The Natural History Museum, London.CrossRefGoogle Scholar
Gibson, D. I., Bray, R. A. and Harris, E. A. (2005). Host-parasite database of the Natural History Museum, London. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/index.html, cited as 27-Jan-2016.Google Scholar
Hechinger, R. F. and Miura, O. (2014). Two “new” renicolid trematodes (Trematoda: Digenea: Renicolidae) from the California horn snail, Cerithidea californica (Haldeman, 1840) (Gastropoda: Potamididae). Zootaxa 3784, 559–574.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
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
Kennedy, M. J. and Frelier, P. F. (1984). Renicola lari Timon-David, 1933 from the osprey, Pandion haliaetus (L.), from Alberta, Canada. Journal of Wildlife Diseases 20, 350–351.CrossRefGoogle ScholarPubMed
Kharoo, V. K. (2013). A review of the history and classification of the family Renicolidae Dollfus, 1939 (Trematoda: Digenea). Indian Journal of Fundamental and Applied Life Sciences 3, 6–12.Google Scholar
Kostadinova, A. (1993). Trematodes and Trematode Communities in Fish-Eating Birds from the Bulgarian Black Sea Coast. Bulgarian Academy of Sciences, Sofia.Google Scholar
Kostadinova, A. K. (1997). Trematodes of birds of the family Laridae from the Bulgarian Black Sea coast. Acta Zoologica Bulgarica 49, 78–85.Google Scholar
La Rue, G. R. (1957). The classification of digenetic Trematoda: a review and a new system. Experimental Parasitology 6, 306–349.Google Scholar
Lafuente, M., Roca, V. and Carbonell, E. (1998). Trematodes of Audouin's gull, Larus audouinii (Aves, Laridae), from Chararinas Islands (W Mediterranean). Miscellania Zoologica 21, 105–112.Google Scholar
Leonov, V. and Belogurov, O. (1963). Renicola brevivitellata n. sp. from Sterna camtschatica and S. hirundo in Kamchatka. Trudy Geľmintologicheskoi Laboratorii, Akademiya Nauk SSSR 13, 210–211.Google Scholar
Leung, T. L. F., Donald, K. M., Keeney, D. B., Koehler, A. V., Peoples, R. C. and Poulin, R. (2009). Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43, 857–865.CrossRefGoogle Scholar
Litvaitis, M. K. and Rohde, K. (1999). A molecular test of platyhelminth phylogeny? Inferences from partial 28S rDNA sequences. Invertebrate Biology 118, 42–56.Google Scholar
Macko, J. K. (1959). [On the helminth fauna of grebes in Eastern Slovakia]. Československá parasitologie 6, 127–157. (in Slovak).Google Scholar
Macko, J. K. (1961). [Plathelminths and their investigation at most often occurring free-living birds in East Slovakia]. Zborník Východoslovenského Múzea v Košiciach 2–3, 129–154. (in Slovak).Google Scholar
Macko, J. K. (1964). [Trematodes of the Caspian tern (Hydroprogne tschegrava)]. Studia Helminthologica 1, 47–65. (in Slovak).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
Murai, É., Sulgostowska, T., Matskási, I. and Mészáros, F. (1986). Parasitic helminths of vertebrates (fishes, amphibians, reptiles, birds and mammals) in the Kiskunság National Park. In The fauna of the Kiskunság National Park (ed. Mahunka, S.), pp. 61–78. Akadémiai Kiadó, Budapest.Google Scholar
Nekrasov, A. V., Pronin, N. M., Sanzheva, S. D. and Timoshenko, T. M. (1999). [Diversity of helminth fauna in the herring gull (Larus argentatus) from the Baikal Lake: peculiarities of spatial distribution and invasion]. Parazitologiya 33, 426–436. (in Russian).Google Scholar
Oßmann, S. (2008). Untersuchungen zum Helminthenbefall beim Kormoran (Phalacrocorax carbo) ung Graureiher (Ardea cinerea) aus sächsischen Teichwirtschaften – ein Beitrag zu Parasitenbefall, Epidemiologie und Schadwirkung . Dr. med. vet. dissertation. Veterinärmedizinischen Fakultät, Universität Leipzig, Leipzig.Google Scholar
Odening, K. (1962). Neue Trematoden aus Vietnamesischen Vogeln des Berliner Tierparks (Mit einer Revision der Familie Renicolidae). Bijdragen tot de Dierkunde 32, 49–63.Google Scholar
O'Dwyer, K., Faltýnková, A., Georgieva, S. and Kostadinova, A. (2015). An integrative taxonomic investigation of the diversity of digenean parasites infecting the intertidal snail Austrolittorina unifasciata Gray, 1826 (Gastropoda: Littorinidae) in Australia. Parasitology Research 114, 2381–2397.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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Patitucci, K. F., Kudlai, O. and Tkach, V. V. (2015). Nephromonorcha varitestis n. sp. (Digenea: Renicolidae) from the American White Pelican, Pelecanus erythrorhynchos in North Dakota, U.S.A. Comparative Parasitology 82, 254–261.CrossRefGoogle Scholar
Pojmańska, T. and Niewiadomska, K. (2015). Renicola lari – Nephromonorcha lari; which species name is correct? Annals of Parasitology 61, 77–78.Google ScholarPubMed
Reimer, L. W. (2002). Parasitische Würmer (Helminthen) von Seevögeln der Ostseeküste. Seevögel 23, 66–76.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.CrossRefGoogle Scholar
Riley, J. and Owen, R. W. (1972). Renicola glacialis sp. nov., a new trematode from the North sea Fulmar, Fulmarus glacialis (L.) with observations on its pathology. Journal of Helminthology 46, 63–72.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.CrossRefGoogle ScholarPubMed
Rząd, I., Sitko, J., Kavetska, K., Kalisińska, E. and Panicz, R. (2013). Digenean communities in the tufted duck [Aythya fuligula (L., 1758)] and greater scaup [A. marila (L., 1761)] wintering in the north-west of Poland. Journal of Helminthology 87, 230–239.CrossRefGoogle ScholarPubMed
Sato, H., Ihara, S., Inaba, O. and Une, Y. (2010). Identification of Euryhelmis costaricensis metacercariae in the skin of Tohoku hynobiid salamanders (Hynobius lichenatus), Northeastern Honshu, Japan. Journal of Wildlife Diseases 46, 832–842.Google Scholar
Sergeeva, T. P. (1971). [Trematodes of gulls in northern areas of Central Siberia]. Trudy Geľmintologicheskoi Laboratorii Voprosy Biologii, Fiziologii I Biokhimii Geľmintov Zhivotnykh i Rastenii 21, 88–92. (in Russian).Google Scholar
Shyamasundari, K. and Rao, K. H. (1998). Parasitocoenoses of the pond heron Ardeola grayi (Sykes) and the cattle egret Bubulcus ibis coromandus as functions of habitats and habits. Rivista di Parassitologia 15, 225–234.Google Scholar
Sitko, J. (1968). Trematodes of birds of the family Laridae in Czechoslovakia. Věstník Československé společnosti zoologické 32, 275–292.Google Scholar
Sitko, J. (1993). Ecological relations of trematodes infesting lariform birds in the Czech Republic. Přírodovědné práce ústavů Československé akademie věd v Brně 27, 1–98.Google Scholar
Sitko, J. (1995). Seasonal dynamics of trematodes of Larus ridibundus . Helminthologia 32, 78–85.Google Scholar
Sitko, J. and Heneberg, P. (2015). Host specificity and seasonality of helminth component communities in central European grebes (Podicipediformes) and loons (Gaviiformes). Parasitology International 64, 377–388.CrossRefGoogle ScholarPubMed
Sitko, J., Faltýnková, A. and Scholz, T. (2006). Checklist of the Trematodes (Digenea) of Birds of the Czech and Slovak Republics. Academia, Prague.Google Scholar
Skirnisson, K., Guðmundsdóttir, B., Andrésdóttir, V. and Galaktionov, K. V. (2003). ITS1 nuclear rDNA sequences used to clear the life cycle of the morphologically different larvae and adult renicolid (Renicola, Digenea) parasites found in Iceland. Bulletin of the Scandinavian Society for Parasitology 12–13, 50.Google Scholar
Skrjabin, K. I. (1924). Nierentrematoden der Vögel Russlands. Zentralblatt für Bakteriologie 2 62, 80–90.Google Scholar
Storer, R. W. (2000). The Metazoan Parasite Fauna of Grebes (Aves: Podicipediformes) and its Relationship to the Bird's Biology. Museum of Zoology, University of Michigan, Ann Arbor.Google Scholar
Storer, R. W. (2002). The Metazoan Parasite Fauna of Loons (Aves: Gaviiformes), its Relationship to the Bird's Evolutionary History and Biology, and a Comparison with the Parasitefauna of Grebes. Museum of Zoology, University of Michigan, Ann Arbor.Google Scholar
Stunkard, H. W. (1964). Studies on the trematode genus Renicola: observations on the life-history, specificity and systematic position. Biological Bulletin 126, 467–489.Google Scholar
Sudarikov, V. E. and Stenko, R. P. (1984). Trematodes of the family Renicolidae. In Helminths of Farming and Hunting Animals (ed. Sonin, M. D.), pp. 134–189. Nauka, Moscow.Google Scholar
Sulgostowska, T. and Czaplinska, D. (1987). Pasozyty Ptakow – Parasiti Avium. Zeszyt 1. Pierwotniaki I Przywry. Protozoa et Trematoda. Katalog fauny pasozytniczej Polski. Panstwowe Wydawnictwo Naukowe, Wroclaw.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 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, 2731–2739.Google Scholar
Timon-David, J. (1933). Sur une nouvelle espèce de Renicola, trematode parasite du rein des laridés. Bulletin de l'Institute Océanographique, Monaco 616, 1–16.Google Scholar
Tkach, V. V., Pawlowski, J., Mariaux, J. and Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In Interrelationships of Platyhelminthes (eds. Littlewood, D. T. J., Bray, R. A.), pp. 186–193. Taylor & Francis, London.Google Scholar
Wright, C. A. (1954). Trematodes of the genus Renicola from birds in British zoos with description of two new species. Proceedings of the Zoological Society of London 124, 51–61.Google Scholar
Wright, C. A. (1956). Studies on the life history and ecology of the trematode genus Renicola Cohn, 1904. Proceedings of the Zoological Society of London 126, 1–49.Google Scholar
Wright, C. A. (1957). Two kidney flukes from Sudanese birds with a description of a new species. Journal of Helminthology 31, 229–238.CrossRefGoogle ScholarPubMed
Supplementary material: File

Heneberg supplementary material S1

Supplementary Figures and Tables

Download Heneberg supplementary material S1(File)
File 110.3 KB
Supplementary material: File

Heneberg supplementary material S2

Legends to supplementary materials

Download Heneberg supplementary material S2(File)
File 12.5 KB