Diversity of echinostomes (Digenea: Echinostomatidae) in their snail hosts at high latitudes
Language English Country France Media print-electronic
Document type Journal Article
Grant support
18-18597S
grantová agentura české republiky
háskóli íslands
PubMed
34319230
PubMed Central
PMC8336728
DOI
10.1051/parasite/2021054
PII: parasite210057
Knihovny.cz E-resources
- Keywords
- Europe, Mitochondrial and nuclear DNA, Mollusca, Morphology, North America, Trematoda,
- MeSH
- Echinostomatidae * genetics MeSH
- Ecosystem MeSH
- Snails MeSH
- Humans MeSH
- Trematoda * MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
- North America MeSH
The biodiversity of freshwater ecosystems globally still leaves much to be discovered, not least in the trematode parasite fauna they support. Echinostome trematode parasites have complex, multiple-host life-cycles, often involving migratory bird definitive hosts, thus leading to widespread distributions. Here, we examined the echinostome diversity in freshwater ecosystems at high latitude locations in Iceland, Finland, Ireland and Alaska (USA). We report 14 echinostome species identified morphologically and molecularly from analyses of nad1 and 28S rDNA sequence data. We found echinostomes parasitising snails of 11 species from the families Lymnaeidae, Planorbidae, Physidae and Valvatidae. The number of echinostome species in different hosts did not vary greatly and ranged from one to three species. Of these 14 trematode species, we discovered four species (Echinoparyphium sp. 1, Echinoparyphium sp. 2, Neopetasiger sp. 5, and Echinostomatidae gen. sp.) as novel in Europe; we provide descriptions for the newly recorded species and those not previously associated with DNA sequences. Two species from Iceland (Neopetasiger islandicus and Echinoparyphium sp. 2) were recorded in both Iceland and North America. All species found in Ireland are new records for this country. Via an integrative taxonomic approach taken, both morphological and molecular data are provided for comparison with future studies to elucidate many of the unknown parasite life cycles and transmission routes. Our reports of species distributions spanning Europe and North America highlight the need for parasite biodiversity assessments across large geographical areas.
TITLE: Diversité des Échinostomes (Digenea, Echinostomatidae) chez leurs hôtes mollusques aux latitudes élevées. ABSTRACT: La biodiversité des écosystèmes d’eau douce à l’échelle mondiale laisse encore beaucoup à découvrir, notamment dans la faune parasitaire des trématodes qu’ils abritent. Les parasites trématodes Échinostomes ont des cycles de vie complexes à hôtes multiples impliquant souvent des oiseaux migrateurs comme hôtes définitifs, conduisant ainsi à des distributions étendues. Ici, nous avons examiné la diversité des échinostomes dans les écosystèmes d’eau douce à des latitudes élevées en Islande, Finlande, Irlande et en Alaska (États-Unis). Nous rapportons de séquences de nad1 et d’ADNr 28S morphologiquement et moléculairement à partir d’analyses de données de séquence d’ADNr nad1 et 28S. Nous avons trouvé des échinostomes parasitant les mollusques de 11 espèces des familles Lymnaeidae, Planorbidae, Physidae et Valvatidae. Le nombre d’espèces d’échinostomes dans différents hôtes ne variait pas beaucoup et allait d’une à trois espèces. Sur ces 14 espèces de trématodes, nous avons découvert quatre espèces (Echinoparyphium sp. 1, Echinoparyphium sp. 2, Neopetasiger sp. 5, Echinostomatidae gen. sp.) comme nouvelles pour l’Europe; nous fournissons des descriptions pour les espèces nouvellement signalées et celles qui n’étaient pas précédemment associées à des séquences d’ADN. Deux espèces d’Islande (Neopetasiger islandicus et Echinoparyphium sp. 2) ont été signalées en Islande et en Amérique du Nord. Toutes les espèces trouvées en Irlande sont de nouveaux signalements pour ce pays. Grâce à une approche taxonomique intégrative, des données morphologiques et moléculaires sont fournies à des fins de comparaison avec des études futures afin d’élucider les nombreux cycles de vie et voies de transmission des parasites, qui sont inconnus. Nos données sur la répartition des espèces en Europe et en Amérique du Nord soulignent la nécessité d’évaluer la biodiversité des parasites dans de vastes zones géographiques.
See more in PubMed
Acosta AA, Smit NJ, Silva RJ. 2020. Diversity of helminth parasites of eight siluriform fishes from the Aguapeí River, upper Paraná basin, São Paulo state, Brazil. International Journal for Parasitology: Parasites and Wildlife, 11, 120–128. PubMed PMC
Alberson NR, Rosser TG, Buddenborg SK, Khoo LH, Loker ES, Richardson TD, Woodyard ET, Wise DJ, Pote LM, Griffin MJ. 2017. North and South American haplotypes of Drepanocephalus auritus (Digenea: Echinostomatidae) are released from Biomphalaria havanensis (Mollusca: Planorbidae) inhabiting catfish aquaculture ponds in Mississippi, U.S.A. Comparative Parasitology, 84, 87–101.
Albrecht C, Wolff C, Glöer P, Wilke T. 2008. Concurrent evolution of ancient sister lakes and sister species: the freshwater gastropod genus Radix in lakes Ohrid and Prespa. Hydrobiologia, 615, 157–167.
Albrecht C, Föller K, Clewing C, Hauffe T, Wilke T. 2014. Invaders versus endemics: alien gastropod species in ancient Lake Ohrid. Hydrobiologia, 739, 163–174.
Beaver PC. 1937. Experimental studies on Echinostoma revolutum (Froelich), a fluke from birds and mammals. Illinois Biological Monographs, 15, 1–95.
Beran L, Horsák M. 2002. Gyraulus parvus (Mollusca: Gastropoda) in the Czech Republic. Acta Societatis Zoologicae Bohemicae, 66, 81–84.
Blair D. 1973. Observations and experiments on some larval trematodes of freshwater snails and fish from southern Iceland. Journal of Helminthology, 47, 409–414. PubMed
Blasco-Costa I, Faltýnková A, Georgieva S, Skírnisson K, Scholz T, Kostadinova A. 2014. Fish pathogens near the Arctic Circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology, 44, 703–715. PubMed
Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ. 2016. Molecular approaches to trematode systematics: “best practice” and implications for future study. Systematic Parasitology, 93, 295–306. PubMed
Bondarenko SK, Kontrimavichus VI. 1999. The helminth fauna of Charadriiformes in Alaska: zoogeographical features and origin. Zoologicheskiy Zhurnal, 78, 643–653 (in Russian).
Born-Torrijos A, Paterson RA, van Beest GS, Vyhlídalová T, Henriksen EH, Knudsen R, Kristoffersen R, Amundsen PA, Soldánová M. 2021. Cercarial behaviour alters the consumers functional response of three-spined sticklebacks. Journal of Animal Ecology, 90, 978–988. PubMed
Boulet M, Potvin C, Shaffer F, Breault A. 2005. Conservation genetics of the threatened horned grebe (Podiceps auritus L.) population of the Magdalen Islands, Québec. Conservation Genetics, 6, 539–550.
Brglez J, Valtonen TE. 1987. Trematodes in some anseriform birds from the Island of Hailuoto in the Bay of Bothnia (Finland). Veterinarski Arhiv, 57, 177–182.
Brinkmann A. 1956. Trematoda. The Zoology of Iceland, 2 (11). Copenhagen and Reykjavík: Ejnar Munksgaard.
Burch JB. 1982. Freshwater snails (Mollusca: Gastropoda) of North America. U.S. Environmental Protection Agency: Cincinati.
Canaris AG, Kinsella JM. 2000. Helminth parasites in six species of shorebirds (Charadrii) from Bristol Bay, Alaska, U.S.A. Comparative Parasitology, 67, 250–252.
Canaris AG, Kinsella JM. 2007. Helminth communities of three sympatric species of shorebirds (Charadrii) from four summer seasons at Bristol Bay, Alaska. Journal of Parasitology, 93, 485–490. PubMed
Carlson CJ, Burgio KR, Dougherty ER, Phillips AJ, Bueno VM, Clements CF, Castaldo G, Dallas TA, Cizauskas CA, Cumming GS, Doña J, Harris NC, Jovani R, Mironov S, Muellerklein OC, Proctor HC, Getz WM. 2017. Parasite biodiversity faces extinction and redistribution in a changing climate. Science Advances, 3, e1602422. PubMed PMC
Cordellier M, Pfenninger A, Streit B, Pfenninger M. 2012. Assessing the effects of climate change on the distribution of pulmonate freshwater snail biodiversity. Marine Biology, 159, 2519–2531.
Correa AC, Escobar JS, Durand P, Renaud F, David P, Jarne P, Pointier JP, Hurtrez-Boussès S. 2010. Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of Fascioliasis. BMC Evolutionary Biology, 10, 1–12. PubMed PMC
Cort WW. 1914. Some North American larval trematodes. Illinois Biological Monographs, 1, 1–71.
Cramp S, Simmons KEL. 1983. Handbook of the birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic (Vol. 3). Waders to Gulls. Oxford University Press: Oxford.
Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. PubMed PMC
Detwiler JT, Bos DH, Minchella DJ. 2010. Revealing the secret lives of cryptic species: Examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution, 55, 611–620. PubMed
Detwiler JT, Zajac AM, Minchella DJ, Belden LK. 2012. Revealing cryptic parasite diversity in a definitive host: Echinostomes in muskrats. Journal of Parasitology, 98, 1148–1155. PubMed
Dillon RT, Wethington AR, Rhett JM, Smith TP. 2002. Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebrate Biology, 121, 226–234.
Dreyfuss G, Vignoles P, Abrous M, Rondelaud D. 2002. Unusual snail species involved in the transmission of Fasciola hepatica in watercress beds in central France. Parasite, 9, 113–120. PubMed
Ebbs ET, Loker ES, Brant SV. 2018. Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes. BMC Evolutionary Biology, 18, 103. PubMed PMC
Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. PubMed PMC
Erickson EM, Found-Jackson C, Boyce M. 2017. Habitat associations with counts of declining Western Grebes in Alberta. Canada. Avian Conservation and Ecology, 12, 12.
Faltýnková A, Georgieva S, Kostadinova A, Blasco-Costa I, Scholz T, Skírnisson K. 2014. Diplostomum von Nordmann, 1832 (Digenea: Diplostomidae) in the sub-Arctic: descriptions of the larval stages of six species discovered recently in Iceland. Systematic Parasitology, 89, 195–213. PubMed
Faltýnková A, Georgieva S, Soldánová M, Kostadinova A. 2015. A re-assessment of species diversity within the “revolutum” group of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) in Europe. Systematic Parasitology, 90, 1–25. PubMed
Faltýnková A, Haas W. 2004. Larval trematodes in freshwater molluscs from Elbe to Danube rivers (South-east Germany): before and today. Parasitology Research, 99, 572–582. PubMed
Faltýnková A, Našincová V, Kablásková L. 2007. Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmona) in Central Europe: a survey of species and key to their identification. Parasite, 14, 39–51. PubMed
Faltýnková A, Našincová V, Kablásková L. 2008. Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Systematic Parasitology, 69, 155–178. PubMed
Faltýnková A, Pantoja C, Skírnisson K, Kudlai O. 2020. Unexpected diversity in northern Europe: trematodes from salmonid fishes in Iceland with two new species of Crepidostomum Braun, 1900. Parasitology Research, 119, 2439–2462. PubMed
Faltýnková A, Valtonen ET, Karvonen A. 2008. Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology, 135, 1691–1699. PubMed
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299. PubMed
Fried B, Toledo R. 2009. The biology of echinostomes. From the molecule to the community. Springer: New York. p. 333.
Frolova EN. 1975. Trematode larvae in molluscs in South Karelian lakes. Nauka: Leningrad: (in Russian).
Galaktionov KV, Dobrovolskiy AA. 2003. The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmission and evolution of digenetic trematodes. Kluwer Academic Publishers: Boston, Dordrecht, London.
Garey JR, Wolstenholme DR. 1989. Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA ser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. Journal of Molecular Evolution, 28, 374–387. PubMed
Ganoe LS, Brown JD, Yabsley MJ, Lovallo MJ, Walter WD. 2020. A review of pathogens, diseases, and contaminants of muskrats (Ondatra zibethicus) in North America. Frontiers in Veterinary Science, 7, 233. PubMed PMC
García-Moreno J, Harrison IJ, Dudgeon D, Clausnitzer V, Darwall W, Farrell T, Savy C, Tockner K, Tubbs N. 2014. Sustaining freshwater biodiversity in the Anthropocene, in The global water system in the Anthropocene. Bhaduri A, Bogardi J, Leentvaar J, Marx S, Editors. Springer: Cham. p. 247–270.
Georgieva S, Blasco-Costa I, Kostadinova A. 2017. Molecular characterisation of four echinostomes (Digenea: Echinostomatidae) from birds in New Zealand, with descriptions of Echinostoma novaezealandense n. sp. and Echinoparyphium poulini n. sp. Systematic Parasitology, 94, 477–497. PubMed
Georgieva S, Faltýnková A, Brown R, Blasco-Costa I, Soldánová M, Sitko J, Scholz T, Kostadinova A. 2014. Echinostoma “revolutum” (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasites & Vectors, 7, 520. PubMed PMC
Georgieva S, Kostadinova A, Skírnisson K. 2012. The life-cycle of Petasiger islandicus Kostadinova & Skírnisson, 2007 (Digenea: Echinostomatidae) elucidated with the aid of molecular data. Systematic Parasitology, 82, 177–183. PubMed
Georgieva S, Selbach C, Faltýnková A, Soldánová M, Sures B, Skírnisson K, Kostadinova A. 2013. New cryptic species of the “revolutum” group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors, 6, 64. PubMed PMC
Ginetsinskaya TA, Dobrovolskiy AA. 1964. On the fauna of larval trematodes of freshwater molluscs of the Volga delta. Trudy Astakhanskogo Zapovednika, 9, 64–104 (in Russian).
Glöer P. 2002. Die Süßwassergastropoden Nord-und Mitteleuropas. Bestimmungschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands, Teil 73. ConchBooks: Hackenheim.
Gordy MA, Hanington PC. 2019. A fine-scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution, 9, 3153–3238. PubMed PMC
Gordy MA, Kish L, Tarrabain M, Hanington PC. 2016. A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada. Parasitology Research, 115, 3867–3880. PubMed
Grabda-Kazubska B, Kiseliene V. 1989. Chaetotaxy and excretory system of the cercaria of Echinoparyphium recurvatum (Linstow, 1873) (Digenea, Echinostomatidae). Acta Parasitologica Polonica, 34, 325–335.
Grabda-Kazubska B, Kiseliene V. 1991. The life-cycle of Echinoparyphium mordwilkoi Skrjabin, 1915 (Trematoda, Echinostomatidae). Acta Parasitologica Polonica, 36, 167–173.
Greben OB, Kudlai O, Korol EN, Kornyushin VV, Vasilkovska IB, Kobylinsky VV. 2016. A new record of Chaunocephalus ferox (Digenea, Echinostomatidae) from Ciconia nigra in Ukraine including morphological and molecular data. Vestnik Zoologii, 50, 99–104.
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. Systematic Biology, 59, 307–321. PubMed
Gustafson KD, Kensinger BJ, Bolek MG, Luttbeg B. 2014. Distinct snail (Physa) morphotypes from different habitats converge in shell shape and size under common garden conditions. Evolutionary Ecology Research, 16, 77–89.
Harper WF. 1929. On the structure and life-histories of British fresh-water larval trematodes. Parasitology, 21, 189–219.
Hoberg EP, Galbreath KE, Cook JA, Kutz SJ, Polley L. 2012. Northern host parasite assemblages: History and biogeography on the borderlands of episodic Climate and Environmental Transition. Advances in Parasitology, 79, 1–97. PubMed
Howard C, Stephens PA, Tobias JA, Sheard C, Butchart SHM, Willis SG. 2018. Flight range, fuel load and the impact of climate change on the journeys of migrant birds. Proceedings of the Royal Society: Biological Sciences, 285, 20172329. PubMed PMC
Huffman JE, Fried B. 2012. The biology of Echinoparyphium (Trematoda, Echinostomatidae). Acta Parasitologica, 57, 199–210. PubMed
Iskova NI. 1985. Fauna of the Ukraine, Volume 34, Trematoda, Part 4, Echinostomata. Naukova Dumka: Kiev: (in Russian).
Jenni L, Kéry M. 2003. Timing of autumn bird migration under climate change: Advances in long distance migrants, delays in short-distance migrants. Proceedings of the Royal Society: Biological Sciences, 270, 1467–1471. PubMed PMC
Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SAJ, De Meester L, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM, Mazzeo N, Iglesias C, Reizenstein M, Malmquist HJ, Liu Z, Balayla D, Lazzaro X. 2010. Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia, 646, 73–90.
Jóhannesdóttir L, Arnalds Ó, Brink S, Gunnarsson TG. 2014. Identifying important bird habitats in a sub-arctic area undergoing rapid land-use change. Bird Study, 61, 544–552.
Jouet D, Skírnisson K, Kolářová L, Ferté H. 2010. Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infection Genetics and Evolution, 10, 1218–1227. PubMed
Kanev I, Sorensen B, Sterner S, Fried B. 1998. The identification and characteristics of Echinoparyphium rubrum (Trematoda: Echinostomatidae) based on experimental evidence of the life cycle. Acta Parasitologica, 43, 181–188.
Karmanova EM. 1971. The life-cycle of Petasiger neocomense (Trematoda, Echinostomatidae). Trudy Gelmintologicheskoy Laboratorii, 21, 31–35 (in Russian).
Keeler SP, Huffman JE. 2009. Echinostomes in the second intermediate host, in The Biology of Echinostomes. Toledo R, Fried B, Editors. Springer: New York. p. 61–87.
Kennedy MJ. 1986. Synopsis of the digenea of mammals of North America. Alberta Agriculture, Animal Health Division, Queen’s Printer: Edmonton, Canada.
Khan D. 1960. Studies on larval trematodes infecting freshwater snails in London (U.K.) and some adjoining areas. Part I. – Echinostome cercariae. Journal of Helminthology, 34, 277–304. PubMed
Kiseliene V, Grabda-Kazubska B, Moné H. 1997. On morphology and chaetotaxy of Cercaria abyssicola Wesenberg-Lund, 1934 (Digenea, Echinostomatidae). Acta Parasitologica, 42, 7–11.
Kostadinova A. 2005. Family Echinostomatidae Looss, 1899, in: Keys to the Trematoda, vol 2, Jones A, Bray RA, Gibson DI, Editors. CAB International and the Natural History Museum: Wallingford – London. p. 9–64.
Kostadinova A, Chipev N. 1992. Experimental data on the life-cycle of Petasiger grandivesicularis Ishii, 1935 (Trematoda: Echinostomatidae). Systematic Parasitology, 23, 55–65.
Kostadinova A, Gibson DI. 2000. The systematics of the echinostomes, in Echinostomes as experimental models for biological research. Fried B, Graczyk TK, Editors. Kluwer Academic Publishers: Netherlands. p. 31–57.
Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ. 2003. Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology, 54, 159–176. PubMed
Kostadinova A, Skírnisson K. 2007. Petasiger islandicus n. sp. (Digenea: Echinostomatidae) in the horned grebe Podiceps auritus (L.) (Aves: Podicipedidae) from Iceland. Systematic Parasitology, 68, 217–223. PubMed
Kudlai O, Pantoja C, O’Dwyer K, Jouet D, Skírnisson K, Faltýnková A. 2021. Diversity of Plagiorchis (Trematoda: Digenea) in high latitudes: Species composition and snail host spectrum revealed by integrative taxonomy. Journal of Zoological Systematics and Evolutionary Research 59, 937–962.
Kudlai O, Tkach VV, Pulis EE, Kostadinova A. 2015. Redescription and phylogenetic relationships of Euparyphium capitaneum Dietz, 1909, the type-species of Euparyphium Dietz, 1909 (Digenea: Echinostomatidae). Systematic Parasitology, 90, 53–65. PubMed
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. PubMed PMC
Kuris AM, Hechinger R, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk ND, Torchin ME, Lafferty KD. 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454, 515–518. PubMed
Lack PC. 1986. The atlas of wintering birds in Britain and Ireland. T. & A. D. Poyser: London.
Lafferty KD, Sammond DT, Kuris AM. 1994. Analysis of larval trematode communities. Ecology, 75, 2275–2285.
Laidemitt MR, Brant SV, Mutuku MW, Mkoji GM, Loker ES. 2019. The diverse echinostomes from East Africa: With a focus on species that use Biomphalaria and Bulinus as intermediate hosts. Acta Tropica, 193, 38–49. PubMed PMC
Lawton SP, Lim RM, Dukes JP, Kett SM, Cook RT, Walker AJ, Kirk RS. 2015. Unravelling the riddle of Radix: DNA barcoding for species identification of freshwater snail intermediate hosts of zoonotic digeneans and estimating their inter-population evolutionary relationships. Infection, Genetics and Evolution, 35, 63–74. PubMed
van Leeuwen CHA, Huig N, van der Velde G, van Alen TA, Wagemaker CAM, Sherman CDH, Klaassen M, Figuerola J. 2013. How did this snail get there? Several dispersal vectors inferred for an aquatic invasive species. Freshwater Biology, 58, 88–99.
Lim HK, Heynemann D. 1972. Intramolluscan inter-trematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological control. Advances in Parasitology, 10, 191–268. PubMed
Littlewood DT, Curini-Galletti M, Herniou EA. 2000. The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466. PubMed
Littlewood DT, Rohde K, 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
Lorencová E, Beran L, Horsáková V, Horsák M. 2015. Invasion of freshwater molluscs in the Czech Republic: time course and environmental predictors. Malacologia, 59, 105–120.
Lydeard C, Campbell D, Golz M. 2016. Physa acuta Draparnaud, 1805 should be treated as a native of North America, not Europe. Malacologia, 59, 347–350.
Masero JA, Santiago-Quesada F, Sánchez-Guzmán JM, Villegas A, Abad-Gómez JM, Lopes RJ, Encarnação V, Corbacho C, Morán R. 2011. Long lengths of stay, large numbers, and trends of the Black-tailed Godwit Limosa limosa in rice fields during spring migration. Bird Conservation International, 21, 12–24.
McCarthy AM. 1990. Speciation of echinostomes: evidence for the existence of two sympatric sibling species in the complex Echinoparyphium recurvatum (von Linstow, 1873) (Digenea: Echinostomatidae). Parasitology, 101, 35–42. PubMed
Meier-Brook C. 1983. Taxonomic studies on Gyraulus (Gastropoda: Planorbidae). Malacologia, 24, 1–113.
Miquel J, Martellet MR, Acosta L, Toledo R, Pétavy AF. 2018. Reinvestigation of the sperm ultrastructure of Hypoderaeum conoideum (Digenea: Echinostomatidae). Parasitology Research, 117, 3725–3732. PubMed
Mohanta UK, Watanabe T, Ohari Y, Itagaki T. 2019. Characterization of Echinostoma revolutum and Echinostoma robustum from ducks in Bangladesh based on morphology, nuclear ribosomal ITS2 and mitochondrial nad1 sequences. Parasitology International, 69, 1–7. PubMed
Morgan JAT, Blair D. 1998. Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology, 116, 289–297. PubMed
Našincová V. 1986. Contribution to the distribution of and the life history of Echinostoma revolutum (Trematoda) in central Europe. Věstník Československé společnosti zoologické, 50, 70–80.
Našincová V. 1992. Trematode developmental stages in Czech aquatic snails and life-cycles of selected species of the family Omphalometridae and Echinostomatidae. PhD Thesis, České Budějovice: Institute of Parasitology, Czechoslovak Academy of Sciences, 268 pp.
Nezvalová J. 1970. Contribution to the knowledge of cercariae of south Moravia. Spisy Přírodovědecké Fakulty, Universita J.E. Purkyně v Brně. Purkyně v Brně, 515, 217–252 (in Czech).
Niewiadomska K, Valtonen ET, Siddall R. 1997. Cercariae from Lymnaea stagnalis in lake Kuuhankavesi (central Finland). Acta Parasitologica, 42, 132–137.
Nolan JR, Bergthorsson U, Adema CM. 2014. Physella acuta: atypical mitochondrial gene order among panpulmonates (Gastropoda). Journal of Molluscan Studies, 80, 388–399. PubMed PMC
Odening K. 1962. Bemerkungen zum Exkretionssystem dreier echinostomer Cercarien sowie zur Identität der Gattungen Neoacanthoparyphium Yamaguti und Allopetasiger Yamaguti (Trematoda: Echinostomatidae). Zeitschrift für Parasitenkunde, 21, 521–534. PubMed
Odening K. 1965. Eine echinostome Cercarie mit 29 Kragenstacheln aus Gewässern bei Berlin und die Entwicklung ihres Exkretionssystems. Monatsberichte der Deutschen Akademie der Wissenschaften zu Berlin, 7, 818–822.
Ohama T, Osawa S, Watanabe K, Jukes TH. 1990. Evolution of the mitochondrial genetic code IV. AAA as an asparagine codon in some animal mitochondria. Journal of Molecular Evolution, 30, 329–332. PubMed
Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood TD. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755. PubMed
Pfenninger M, Cordellier M, Streit B. 2006. Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata). BMC Evolutionary Biology, 6, 1–14. PubMed PMC
Pinto HA, Griffin MJ, Quiniou SM, Ware C, Melo AL. 2016. Biomphalaria straminea (Mollusca: Planorbidae) as an intermediate host of Drepanocephalus spp. (Trematoda: Echinostomatidae) in Brazil: a morphological and molecular study. Parasitology Research, 115, 51–62. PubMed
Pulis EE, Tkach VV, Newman RA. 2011. Helminth parasites of the wood frog, Lithobates sylvaticus, in prairie pothole wetlands of the Northern Great Plains. Wetlands, 31, 675–685.
Rambaut A. 2012. Institute of Evolutionary Biology. Molecular evolution, phylogenetics and epidemiology, Vol. FigTree v1 (p. 4). University of Edinburgh.
Rašín K. 1933. Echinoparyphium recurvatum (Linstow, 1873) and its development. Biologické spisy Vysoké školy zvěrolékařské, Brno, 12, 1–104 (in Czech).
Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ, Kidd KA, MacCormack TJ, Olden JD, Ormerod SJ, Smol JP, Taylor WW, Tockner K, Vermaire JC, Dudgeon D, Cooke SJ. 2019. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94, 849–873. PubMed
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, 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
Saadi AJ, Davison A, Wade CM. 2020. Molecular phylogeny of freshwater snails and limpets (Panpulmonata: Hygrophila). Zoological Journal of the Linnean Society, 190, 528–531.
Saito T, Hirano T, Prozorova L, Do VT, Sulikowska-Drozd A, Sitnikova T, Surenkhorloo P, Yamazaki D, Morii Y, Kameda Y, Fukuda H, Chiba S. 2018. Phylogeography of freshwater planorbid snails reveals diversification patterns in Eurasian continental islands. BMC Evolutionary Biology, 18, 1–13. PubMed PMC
Schniebs K, Glöer P, Vinarski M, Hundsdoerfer A. 2011. Intraspecific mophological and genetic variability in Radix balthica (Linnaeus, 1758) (Gastropoda: Basommatophora: Lymnaeidae) with morphological comparison to other European Radix species. Journal of Conchology, 40, 657–678.
Selbach C, Soldánová M, Feld CK, Kostadinova A, Sures B. 2020. Hidden parasite diversity in a European freshwater system. Scientific Reports, 10, 1–14. PubMed PMC
Selbach C, Soldánová M, Georgieva S, Kostadinova A, Kalbe M, Sures B. 2014. Morphological and molecular data for larval stages of four species of Petasiger Dietz, 1909 (Digenea: Echinostomatidae) with an updated key to the known cercariae from the Palaearctic. Systematic Parasitology, 89, 153–166. PubMed
Sitko J, Faltýnková A, Scholz T. 2006. Checklist of the trematodes (Digenea) of birds of the Czech and Slovak Republics. Academia: Prague.
Skírnisson K, Kolářová L. 2008. Diversity of bird schistosomes in anseriform birds in Iceland based on egg measurements and egg morphology. Parasitology Research, 103, 43–50. PubMed
Snyder SD, Tkach VV. 2001. Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–1440. PubMed
Soldánová M, Georgieva S, Roháčová J, Knudsen R, Kuhn JA, Henriksen EH, Amundsen PA. 2017. Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology, 47, 327–345. PubMed
Stanevičiūtė G, Stunžėnas V, Petkevičiūtė R. 2015. Phylogenetic relationships of some species of the family Echinostomatidae Odner, 1910 (Trematoda), inferred from nuclear rDNA sequences and karyological analysis. Comparative Cytogenetics, 9, 257–270. PubMed PMC
Stensgaard A-S, Utzinger J, Vounatsou P, Hürlimann E, Schur N, Saarnak CFL, Simoonga C, Mubita P, Kabatereine NB, Tchuenté L-AT, Rahbek C, Kristensen TK. 2013. Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: Does climate matter? Acta Tropica, 128, 378–390. PubMed
Summers RW, Boland H, Colhoun K, Elkins N, Etheridge B, Foster S, Fox JW, Mackie K, Quinn LR, Swann RL. 2014. Contrasting trans-Atlantic migratory routes of Nearctic purple sandpipers Calidris maritima associated with low pressure systems in spring and winter. Ardea, 102, 139–152.
Tkach VV, Kudlai O, Kostadinova A. 2016. Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology, 46, 171–185. PubMed
Tkach V, Pawlowski J, Mariaux J. 2000. Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology, 30, 83–93. PubMed
Tkach V, Pawlowski J, Mariaux J, Swiderski Z. 2001. Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea, in Interrelationships of platyhelminthes. Littlewood DTJ, Bray RA, Editors. Taylor & Francis: London. p. 186–193.
Tkach VV, Schroeder JA, Greiman SE, Vaughan JA. 2012. New genetic lineages, host associations and circulation pathways of Neorickettsia endosymbionts of digeneans. Acta Parasitologica, 57, 285–292. PubMed
Toledo R, Esteban JG. 2016. An update on human echinostomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 110, 37–45. PubMed
Toledo R, Muñoz-Antolí C, Pérez M, Esteban J. 1998. Larval trematode infections in freshwater gastropods from the Albufera Natural Park in Spain. Journal of Helminthology, 72, 79–82. PubMed
Väyrynen T, Siddall R, Valtonen ET, Taskinen J. 2000. Patterns of trematode parasitism in lymnaeid snails from northern and central Finland. Annales Zoologici Fennici, 37, 189–199.
Vinarski MV, Bolotov IN, Aksenova OV, Babushkin ES, Bespalaya V, Makhrov AA, Nekhaev IO, Vikhrev I. 2021. Freshwater Mollusca of the circumpolar Arctic: a review on their taxonomy, diversity and biogeography. Hydrobiologia, 848, 2891–2918.
deWaard JR, Levesque-Beaudin V, deWaard SL, Ivanova NV, McKeown JTA, Miskie R, Naik S, Perez KHJ, Ratnasingham S, Sobel CN, Sones JE, Steinke C, Telfer AC, Young AD, Young MR, Zakharov EV, Hebert PDN. 2019. Expedited assessment of terrestrial arthropod diversity by coupling Malaise traps with DNA barcoding. Genome, 62, 85–95. PubMed
Welter-Schultes F. 2012. European non-marine molluscs, a guide for species identification. Planet Poster Editions: Göttingen.
Werle E, Schneider C, Volker M, Fiehn W. 1994. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22, 4354–4355. PubMed PMC
Wesenberg-Lund C. 1934. Contributions to the development of the Trematoda Digenea. Part II. The biology of the freshwater cercariae in Danish freshwaters. Mémoirs de l’Académie Royale des Sciences et des Lettres de Danemark, Copenhague, 9, 1–223.
Wikgren BJ. 1956. Studies on Finnish larval flukes with a list of known Finnish adult flukes (Trematoda: Malacocotylea). Acta Zoologica Fennica, 91, 1–106.
Wrona F, Reist JD. 2013. Freshwater ecosystems, in Arctic Biodiversity Assessment. Status and Trends in Arctic Biodiversity. Meltofte H, Editor. Conservation of Arctic Flora and Fauna: Akureyri. p. 335–377.
Zaifman J, Shan D, Ay A, Jimenez AG. 2017. Shifts in bird migration timing in North American long-distance and short-distance migrants are associated with climate change. International Journal of Zoology, 2017, 1–9.
Zdun VI. 1961. Larval trematodes in freshwater molluscs of the Ukraine. Ukrainian Academy of Sciences Press: Kiev: (in Ukrainian).