Hidden in plain sight: novel molecular data reveal unexpected genetic diversity among paramphistome parasites (Digenea: Paramphistomoidea) of European water frogs

. 2022 Sep ; 149 (11) : 1425-1438. [epub] 20220617

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35711137

Parasites might represent a helpful tool in understanding the historical dispersion and phylogeography of their hosts. In order to reveal whether the migration routes and diversification of hosts can be traceable in the genetic structures of their parasites, we investigated the diversity of paramphistomoid trematodes of Pelophylax frogs in 2 geographically distant European regions. Water frogs belonging to the genus Pelophylax represent a striking example of a species with a high variety of ecological adaptations and a rich evolutionary history. The parasites were collected from 2 Balkan endemic species, P. epeiroticus and P. kurtmuelleri, and 2 species in Slovakia, P. esculentus and P. ridibundus. While in Slovakia, Pelophylax frogs harboured 2 species, the diplodiscid Diplodiscus subclavatus and the cladorchiid Opisthodiscus diplodiscoides, only the former was recorded in the south-western Balkans. Remarkably high genetic diversity (16 unique mitochondrial cox1 haplotypes, recognized among 60 novel sequences) was observed in D. subclavatus, and subsequent phylogenetic analyses revealed a strong population-genetic structure associated with geographical distribution. We also evidenced the existence of 2 divergent D. subclavatus cox1 haplogroups in the south-western Balkans, which might be associated with the historical diversification of endemic water frogs in the regional glacial microrefugia.

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Aho JM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In Esch GW, Bush AO and Aho JM (eds), Parasite Communities: Patterns and Processes. London, UK: Chapman & Hall, pp. 157–195.

Akın C, Bilgin CC, Beerli P, Westaway R, Ohst T, Litvinchuk SN, Uzzell T, Bilgin M, Hotz H, Guex G-D and Plötner J (2010) Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs were determined by geological processes and climate change in the Late Cenozoic. Journal of Biogeography 37, 2111–2124. PubMed PMC

Alves PV, Assis JCA, López-Hernández D, Pulido-Murillo EA, Melo AL, Locke SA and Pinto HA (2020) A phylogenetic study of the cecal amphistome Zygocotyle lunata (Trematoda: Zygocotylidae), with notes on the molecular systematics of Paramphistomoidea. Parasitology Research 119, 2511–2520. PubMed

Andreas K (2007) Helminthen einheimischer Froschlurche (PhD thesis). Freie Universität, Berlin, Germany.

Bailenger J and Chanseau J (1954) Etude des vers parasites des amphibiens anoures de la region de Bordeaux. Annales de Parasitologie 29, 546–560. PubMed

Barton DP (1999) Ecology of helminth communities in tropical Australian amphibians. International Journal for Parasitology 29, 921–926. PubMed

Beerli P, Hotz H and Uzzell T (1996) Geologically dated sea barriers calibrate a protein clock for Aegean water frogs. Evolution 50, 1676–1687. PubMed

Bellati A, Bassu L, Nulchis V and Corti C (2019) Detection of alien Pelophylax species in Sardinia (western Mediterranean, Italy). BioInvasion Records 8, 8–25.

Besprozvannykh VV, Rozhkovan KV, Ermolenko AV and Izrailskaya AV (2018) Diplodiscus mehrai Pande, 1973 and D. japonicus (Yamaguti, 1936): morphology of developmental stages and molecular data. Helminthologia 55, 60–69. PubMed PMC

Bjelić-Čabrilo O, Popović E and Paunović A (2009) Helminthofauna of Pelophylax kl. esculentus (Linne, 1758) from Petrovaradinski Rit Marsh (Serbia). Helminthologia 46, 107–111.

Blaustein AR and Wake DB (1995) The puzzle of declining amphibian populations. Scientific American 272, 52–57.

Blouin MS, Yowell CA, Courtney CH and Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014. PubMed PMC

Bowles J, Blair D and McManus DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109. PubMed

Bush AO, Lafferty KD, Lotzs JM and Shostakll AW (1997) Parasitology meets ecology on its own terms: Margolis, et al., revisited. Journal of Parasitology 83, 575–583. PubMed

Carlson CJ, Dallas TA, Alexander LW, Phelan AL and Phillips AJ (2020) What would it take to describe the global diversity of parasites? Proceedings of Royal Society B: Biological Sciences 287, 20201841–20201841. PubMed PMC

Čeirāns A, Gravele E, Gavarane I, Pupins M, Mezaraupe L, Rubenina I, Kvach Y, Skute A, Oskyrko O, Nekrasova O, Marushchak O and Kirjushina M (2021) Helminth communities in amphibians from Latvia, with an emphasis on their connection to host ecology. Journal of Helminthology 95, 1–17. PubMed

Chikhlyaev IV, Ruchin AB and Fayzulin AI (2018) Short communication: an overview of the trematode fauna of pool frog Pelophylax lessonae (Camerano, 1882) in the Volga Basin, Russia: 1. Adult stages. Nusantara Bioscience 10, 256–262.

Cichy A, Faltýnková A and Žbikowska A (2011) Cercariae (Trematoda, Digenea) in European freshwater snails – a checklist of records from over one hundred years. Folia Malacologica 19, 165–189.

Cohn L (1904) Helminthologische Mittheilungen II. Archiv für Naturgeschifte 70, 229–252.

Combes C and Gerbaux MT (1970) Recherches éco-parasitologiques sur l'Helminthofauna de Rana ridibunda perezi (Amphibian Anoure) dan l'Est des Pyrenees. Vie et Milieu 21, 121–158.

Combes C and Sarrouy H (1971) Helminthes de Rana ridibunda perezi (Amphibian Anoure) dans la région de Soria. Revista Ibérica de Parasitologia 31, 115–119.

Combes C, Leger N and Vidal D (1973) Inventaire des helminthes de Rana esculenta L. (Amphibien, Anoure) dans ľile de Corse. Annales de Parasitologie Humaine et Comparée 48, 761–766. PubMed

Cordellier M and Pfenninger M (2008) Climate-driven range dynamics of the freshwater limpet, Ancylus fluviatilis (Pulmonata, Basommatophora). Journal of Biogeography 35, 1580–1592.

Cutmore SC, Miller TL, Curran SS, Bennett MB and Cribb TH (2013) Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. Subfam.). Parasitology Research 112, 3063–3074. PubMed

Darriba D, Taboada GL, Doallo R and Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772. PubMed PMC

Dollfus RP (1951) Miscellanea helminthologica maroccana, I. Quelques trematodes, cestodes et acanthocephales. Archives de l'Institut Pasteur du Maroc 4, 104–229.

Dufresnes C, Denoël M, Di Santo L and Dubey S (2017) Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex. Scientific Reports 7, 1–10. PubMed PMC

Dufresnes C, Lauenberger J, Amrhein V, Bühler C, Thiébaud J, Bohnenstengel T and Dubey S (2018) Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland. Biological Journal of the Linnean Society 123, 402–410.

Dufresnes C, Strachinis I, Tzoras E, Litvinchuk SN and Denoël M (2019) Call a spade a spade: taxonomy and distribution of Pelobates, with description of a new Balkan endemic. ZooKeys 859, 131–158. PubMed PMC

Düşen S and Öz M (2013) Helminth fauna of the Eurasian marsh frog, Pelophylax ridibundus (Pallas, 1771) (Anura: Ranidae), collected from Denizli Province, inner-west Anatolia region, Turkey. Helminthologia 50, 57–66.

Frost DR (2021) Amphibian Species of the World. Retrieved from electronic database of American Museum of Natural History. Available at https://amphibiansoftheworld.amnh.org/index.php (Accessed 2 December 2021).

Georgiev B, Biserkov V and Genov T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279–281.

Georgieva S, Soldánová M, Pérez-del-Olmo A, Dangel RD, Sitko J, Sures B and Kostadinova A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 57–72. PubMed

Gomez P (1987) Sobre la helmintofauna de algunas poblaciones españolas, peninsulares e insulares, del género Rana Linnaeus, 1758 (Amphibia: Ranidae) (PhD thesis). Universitat de València, Valencia, Spain.

Grabda-Kazubska B (1980) Opisthodiscus diplodiscoides Cohn, 1904 (Trematoda, Diplodiscidae) in Rana esculenta s.1. in Poland with remarks on its synonymy and geographical distributions. Acta Parasitologica Polonia 27, 145–151.

Graf J and Polls Pelaz M (1989) Evolutionary genetics of the Rana esculenta complex. In Dawley R and Bogart P (eds), Evolution and Ecology of Unisexual Vertebrates. Albany, US: New York State Museum Bulletin, pp. 289–301.

Gratton P, Konopinski MK and Sbordoni V (2008) Pleistocene evolutionary history of the Clouded Apollo (Parnassius mnemosyne): genetic signatures of climate cycles and a ‘time-dependent’ mitochondrial substitution rate. Molecular Ecology 17, 4248–4262. PubMed

Günther R (1990) Die Wasserfrösche Europas. Wittenberg Lutherstadt, Germany: A. Ziemsen Verlag.

Herczeg D, Vörös J, Végvári Z, Kuzmin Y and Brooks DR (2016) Helminth parasites of the Pelophylax esculentus complex (Anura: Ranidae) in Hortobágy National Park (Hungary). Comparative Parasitology 83, 36–48.

Herczeg D, Vörös J, Christiansen DG, Benovics M and Mikulíček P (2017) Taxonomic composition and ploidy level among European water frogs (Anura: Ranidae: Pelophylax) in eastern Hungary. Journal of Zoological Systematics and Evolutionary Research 55, 129–137.

Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913. PubMed

Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B 359, 183–195. PubMed PMC

Hoffmann A, Plötner J, Pruvost NBM, Christiansen DG, Röthlisberger S, Choleva L, Mikulíček P, Cogalniceanu D, Sas-Kovacs I, Shabanov D, Morozov-Leonov S and Reyer H-U (2015) Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe. Molecular Ecology 24, 4371–4391. PubMed

Horsák M, Čejka T, Juřičková L, Beran L, Horáčková J, Hlaváč JČ, Dvořák L, Hájek O, Divíšek J, Maňas M and Ložek V (2021) Check-list and distribution maps of the molluscs of the Czech and Slovak Republics. Retrieved from http://mollusca.sav.sk/malacology/checklist.htm (Accessed 13 December 2021).

Iacob OC (2021) Parasitism with Acanthocephalus ranae in frogs (Pelophylax ridibundus Pallas 1771), from north-east Romania. Helminthologia 58, 68–73. PubMed PMC

Jablonski D, Jandzik D, Mikulíček P, Džukić G, Ljubisavljević K, Tzankov N, Jelić D, Thanou E, Moravec J and Gvoždík V (2016) Contrasting evolutionary histories of the legless lizard slow worms (Anguis) shaped by the topography of the Balkan Peninsula. BMC Evolutionary Biology 16, 99. PubMed PMC

Jones A (2005) Family Diplodiscidae Cohn, 1904. In Jones A, Bray RA and Gibson DI (eds), Keys to the Trematoda, vol. 2. Wallingford, UK: CAB International & The Natural History Museum, pp. 319–324.

Kappes H and Haase P (2012) Slow, but steady: dispersal of freshwater molluscs. Aquatic Sciences 74, 1–14.

Karakaş M (2015) Helminth parasites of Bufo viridis, Rana ridibunda and Hyla arborea collected from the different regions of Turkey. Manas Journal of Agriculture Veterinary and Life Sciences 5, 1–6.

Katoh K, Misawa K, Kuma K and Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066. PubMed PMC

Koehler AV, Springer YP, Keeney DB and Poulin R (2011) Intra- and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biological Journal of the Linnean Society 103, 106–116.

Kolenda K, Pietras-Lebioda A, Hofman S, Ogielska M and Pabijan M (2017) Preliminary genetic data suggest the occurrence of the Balkan water frog, Pelophylax kurtmuelleri, in southwestern Poland. Amphibia-Reptilia 38, 187–196.

Kopřiva J (1957) Die Saugwürmer der Frösche in der Tschechoslowakei. Československá Parasitologie 4, 191–199.

Kuzmin Y, Dmytrieva I, Marushchak O, Morozov-Leonov S, Oskyrko O and Nekrasova O (2020) Helminth species and infracommunities in frogs Pelophylax ridibundus and P. esculentus (Amphibia: Ranidae) in Northern Ukraine. Acta Parasitologica 65, 341–353. PubMed

Leigh JW and Bryant D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.

Librado P and Rozas J (2009) DnaSP v 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452. PubMed

Littlewood DT, Rohde K and Clough KA (1997) Parasite speciation within or between host species? – phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297. PubMed

Littlewood DT, Curini-Galletti M and Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466. PubMed

Litvinchuk SN, Ivanov AY, Lukonina SA and Ermakov OA (2020) A record of alien Pelophylax species and widespread mitochondrial DNA transfer in Kaliningradskaya Oblasť (the Baltic coast, Russia). BioInvasion Records 9, 599–617.

Lymberakis P, Poulokakis N, Manthalou G, Tsigenopoulos CS, Magoulas A and Mylonas M (2007) Mitochondrial phylogeography of Rana (Pelophylax) populations in the Eastern Mediterranean region. Molecular Phylogenetics and Evolution 44, 115–125. PubMed

Martínez-Fernández AR, Simón-Vicente F and Cordero del Campillo M (1988) On the morphology of Opisthodiscus nigrivasis (v. Mehély 1929) Odening, 1959 (Trematoda: Paramphistomidae) of Rana ridibunda. Revista Ibérica de Parasitologia 48, 9–16.

Mazurmovič BN (1957) The interrelationships of parasitic worms in amphibians. Otdelenie Zoologii 73, 204–207.

Mehély L (1929) Opisthodiscus diplodiscoides nigrivasis n. subsp. Ein neuer Saugwurm der ungarischen Fauna. Studia Zoologica 1, 84–90.

Men Q, Han H, Zhao Q, Xia W, Dong H, Zhu S, Wang Z, Li C, Zhu X and Huang B (2016) The prevalence of helminth parasites in Pelophylax nigromaculatus (Anura: Ranidae) from Shanghai, China. Acta Parasitologica 61, 802–807. PubMed

Mideo N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261–268. PubMed

Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ 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. PubMed

Mouritsen K and Andersen C (2017) Worms at war: interspecific parasite competition and host resources alter trematode colony structure and fitness. Parasitology 144, 1530–1542. PubMed

Navarro P and Lluch J (2006) Helminth communities of two green frogs (Rana perezi and Rana saharica) from both shores of the Alboran Sea. Parasite 13, 291–297. PubMed

Niemi GJ and McDonald ME (2004) Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35, 89–111.

Odening K (1959) Über die Diplodiscidae der einheimischen Frösche (Trematoda, Paramphistomatata). Zeitschrift für Parasitenkunde 19, 54–66. PubMed

Okulewicz A, Hildebrand J, Łysowski R, Buńkowska K and Perec-Matysiak A (2014) Helminth communities of green and brown frogs from Poland (Lower Silesia Region). Journal of Herpetology 48, 34–37.

Olson PD, Cribb TH, Tkach VV, Bray RA and Littlewood DT (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755. PubMed

Papežík P, Kubala M, Jablonski D, Doležálková-Kaštánková M, Choleva L, Benovics M and Mikulíček P (2021) Morphological differentiation of endemic water frogs (Ranidae: Pelophylax) from the southwestern Balkans. Salamandra 57, 105–123.

Parmakelis A, Stathi I, Chatzaki M, Simaiakis S, Spanos L, Louis C and Mylonas M (2006) Evolution of Mesobuthus gibbosus (Brullé, 1832) (Scorpiones: Buthidae) in the northeastern Mediterranean region. Molecular Ecology 15, 2883–2894. PubMed

Plasota K (1969) The effect of some ecological factors on the parasitofauna of frogs. Acta Parasitologica Polonica 16, 47–60.

Plötner J (2005) Die westpaläarktischen Wasserfrösche. Bielefeld, DE: Laurenti Verlag.

Plötner J, Uzzell T, Beerli P, Spolsky C, Ohst T, Litvinchuk SN, Guex G-D, Reyer H-U, Pruvost N and Hotz H (2008) Wide-spread unidirectional transfer of mitochondrial DNA: a case in western Palearctic water frogs. Journal of Evolutionary Biology 21, 668–681. PubMed PMC

Plötner J, Uzzell T, Beerli P, Akın C, Bilgin CC, Haefeli C, Ohst T, Köhler F, Schreiber R, Guex G-D, Litvinchuk SN, Westaway R, Reyer H-U and Hotz H (2010) Genetic divergence and evolution of reproductive isolation in eastern Mediterranean water frogs. In Glaubrecht M (ed.), Evolution in Action. Case Studies in Adaptive Radiation and the Origin of Biodiversity. Special Volume From the SPP 1127 ‘Radiations – Genesis of Biological Diversity’ of the DFG. Berlin, DE: Springer, pp. 373–403.

Polis GA, Myers CA and Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology, Evolution, and Systematics 20, 297–330.

Popiołek M, Rozenblut-Kościsty B, Kot M, Nosal W and Ogielska M (2011) Endoparasitic helminths of water frog complex in Poland: do differences exist between the parental species Pelophylax ridibundus and Pelophylax lessonae, and their natural hybrid Pelophylax esculentus? Helminthologia 48, 108–115.

Poulin R (2007) Evolutionary Ecology of Parasites, 2nd Edn. New Jersey, USA: Princeton University Press.

Poulin R and Morand S (2000) The diversity of parasites. The Quarterly Review of Biology 75, 277–293. PubMed

Queiroz MS, Alves PV, López- Hernández D, Anjos LA and Pinto HA (2021) Exploring Neotropical anuran parasites: a morphological, life cycle and phylogenetic study of Catadiscus marinholutzi (Trematoda: Diplodiscidae). Parasitology 148, 798–808. PubMed PMC

Radojičić JM, Krizmanić I, Kasapidis P and Zouros E (2015) Extensive mitochondrial heteroplasmy in hybrid water frog (Pelophylax spp.) populations from Southeast Europe. Ecology and Evolution 5, 4529–4541. PubMed PMC

Rambaut A, Drummond AJ, Xie D, Baele G and Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904. PubMed PMC

Reiczigel J, Marozzi M, Fábián I and Rózsa L (2019) Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology 35, 277–281. PubMed

Rodrigues RAE (2014) Macroparasites of Invasive Xenopus laevis (Amphibia: Anura): Characterization and Assessment of Possible Exchanges with Native Pelophylax perezi in Oeiras Streams, Portugal (PhD thesis). University of Lisboa, Lisboa, Portugal.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA and Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542. PubMed PMC

Rózsa L, Reiczigel J and Majoros G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232. PubMed

Schmitt T (2007) Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology 4, 11. PubMed PMC

Schmitt T and Varga Z (2012) Extra-Mediterranean refugia: the rule and not the exception? Frontiers in Zoology 9, 22. PubMed PMC

Semlitsch RD (2003) Amphibian Conservation. Washington, DC: Smithsonian Institute.

Sey O (1983) Reconstruction of the systematics of the family Diplodiscidae Skrjabin, 1949 (Trematoda: Paramphistomata). Parasitologia Hungarica 16, 63–89.

Sey O (1991) CRC Handbook of the Zoology of Amphistomes. Boca Raton, USA: CRC Press.

Sey O (1988) Scope of and proposal for systematics of the Amphistomida (Lühe, 1909) Odening, 1974 (Trematoda). Parasitologia Hungarica 21, 17–30.

Sey O (2005) Keys to the Identification of the Taxa of the Amphistomes (Trematoda, Amphistomida). Pecs, Hungary: Regional Centre of the Hungarian Academy of Sciences, Veszprem (MTA VEAB)/ University of Pecs.

Simón-Vicente F, Martínez-Fernandez A and Cordero Del Campillo M (1974) Some observations on the redia, cercaria and metacercaria of Opisthodiscus nigrivasis (v. Mehlij, 1929) Odening, 1959 (Trematoda: Paramphistomidae). Journal of Helminthology 48, 187–193. PubMed

Skrjabin KI (1949) Trematodes of Animals and Men, vol. 3. Moscow, RU: Publishing House of the USSR Academic Science.

Snell C, Tetteh J and Evans IH (2005) Phylogeography of the pool frog (Rana lessonae Camerano) in Europe: evidence for native status in Great Britain and for an unusual postglacial colonization route. Biological Journal of the Linnean Society 85, 41–51.

Speybroeck J, Beukema W, Bok B and Voort JV (2016) Field Guide to the Amphibians & Reptiles of Britain and Europe. New York, US: Bloomsbury Publishing Plc.

Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690. PubMed

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313. PubMed PMC

Taberlet P, Fumagalli L, Wust-Saucy AG and Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464. PubMed

Tkach VV, Pawlowski J, Mariaux J and Swiderski Z (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In Littlewood DTJ and Bray RA (eds), Phylogenetic Relationships of Platyhelminthes. Abingdon, UK: Taylor & Francis, pp. 186–193.

Tkach VV, Littlewood DT, Olson PD, Kinsella JM and Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15. PubMed

Vojtková L (1974) Motolice obojžojvelniku ČSSR, I- Dospělé motolice. Brno, CZ: Universita J.E. Purkyně.

Vojtková L and Roca V (1994) Parasites of the frogs and toads in Europe. Part II: Trematoda. Revista Española de Herpetologia 8, 7–18.

Vojtková L and Roca V (1996) Parasites of the frogs and toads in Europe. Part III: Nematoda, Cestoda, Acanthocephala, Hirudinea, Crustacea and Insecta. Revista Española de Herpetologia 10, 13–27.

Vojtková L, Moravec F and Nabelkova L (1963) K dosavadnímu stavu výzkumu helmintofauny obojživelniků ČSSR. Časopis Národního Muzea 9, 121–131.

Wells KD (2007) The Ecology and Behaviour of Amphibians. Chicago, US: The University of Chicago Press.

Wiens JJ, Sukumaran J, Pyron RA and Brown RM (2009) Evolutionary and biogeographic origins of high tropical diversity in Old World frogs. Evolution 63, 1217–1231. PubMed

Yamaguti S (1971) Synopsis of Digenetic Trematodes of Vertebrates, vol. 1. Tokyo, JP: Keigaku Publishing Company.

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