Eurasian beaver (Castor fiber) is a well-established faunal element in the Czech Republic, even though, historically, its populations were almost eradicated in this region. Nowadays, its distribution and population density are well monitored; nonetheless, the beaver's parasites, as potential threats to the environment, are often neglected in wildlife management. Therefore, we investigated the endoparasitic helminth diversity of 15 beaver individuals from three collection sites in the Czech Republic. Three parasite species were collected: Stichorchis subtriquetrus (Digenea), Travassosius rufus, and Calodium hepaticum (Nematoda), of which the two nematode species were reported for the first time from C. fiber in the Czech Republic. The highest prevalence and intensity of infection were observed in S. subtriquetrus (P = 93%, I = 1-138), while the two other species were collected only from one beaver individual. Subsequent analysis of the genetic diversity of the specimens using highly variable genetic markers revealed a weak population structure among the individuals collected from different beaver hosts. There was only a weak association of COI haplotypes with geography, as the haplotypes from the Berounka basin formed homogeneous groups, and individuals from the Dyje basin and Morava partially shared a haplotype. Even though common population genetic markers (i.e., microsatellites) did not reveal any structure in the hosts, our results suggest that the genetic diversity of their parasites may shed more light on population partition and the historical migration routes of Eurasian beavers.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 613 00 Brno Czech Republic

Department of Zoology Faculty of Sciences Comenius University in Bratislava Mlynská dolina Ilkovičova 6 842 15 Bratislava Slovakia

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Alves MEM, Martins FDC, Bräunig P, Pivoto FL, Sangioni LA, Vogel FSF (2018) Molecular detection of Cryptosporidium spp. and the occurrence of intestinal parasites in fecal samples of naturally infected dogs and cats. Parasitol Res 117(9):3033–3038. https://doi.org/10.1007/s00436-018-5986-4 PubMed DOI

Andersen DC, Shafroth PB (2010) Beaver dams, hydrological thresholds, and controlled floods as a management tool in a desert riverine ecosystem, Bill Williams River. Arizona. Ecohydrol 3(3):325–338. https://doi.org/10.1002/eco.113 DOI

Åhlen PA, Sjöberg G, Stéen M (2021) Parasitic fauna of Eurasian beavers (Castor fiber) in Sweden (1997–1998). Acta Vet Scand 63:23. https://doi.org/10.1186/s13028-021-00588-w PubMed DOI PMC

Bajer A, Bednarska M, Sinski E (1997) Wildlife rodents from different habitats as reservoir for Cryptosporidium parvum. Acta Parasitol 42:191–194

Barlow AM, Gottstein B, Mueller N (2011) Echinococcus multilocularis in an imported captive European beaver (Castor fiber) in Great Britain. Vet Rec 169(13):339. https://doi.org/10.1136/vr.d4673 PubMed DOI

Bowles J, McManus DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol Biochem Parasitol 57:231–240. https://doi.org/10.1016/0166-6851(93)90199-8 PubMed DOI

Britton JR (2012) Introduced parasites in food webs: new species, shifting structures? Trends Evol Ecol 28:93–99. https://doi.org/10.1016/j.tree.2012.08.020 DOI

Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4):575–583. https://doi.org/10.2307/3284227 PubMed DOI

Bystrianska J, Papajová I, Šmiga Ľ, Šoltys J, Majláthová V, Majláth I, Gomboš F, Kleban J (2020) First report on parasites of European beavers in Slovak Republic. Parasitol Res 120(1):355–358. https://doi.org/10.1007/s00436-020-06943-6 PubMed DOI

Campbell-Palmer R, Girling S, Pizzi R, Hamnes IS, Øines Ø, Del-Pozo J (2013) Stichorchis subtriquetrus in a free-living beaver in Scotland. Vet Rec 173(3):72. https://doi.org/10.1136/vr.101591 PubMed DOI

Ćirović D, Pavlović I, Ivetić V, Milenković M, Radović I, Savić B (2009) Reintroduction of the European beaver (Castor fiber L.) into Serbia and return of its parasite: the case of Stichorchis subtriquetrus. ArchBiol Sci Belgr 61:141–114. https://doi.org/10.2298/ABS0901141C DOI

Crawford J, Liu Z, Nelson T, Nielsen C, Bloomquist C (2008) Microsatellite analysis of mating and kinship in beavers (Castor canadensis). J Mammal. 89:575–581. https://doi.org/10.1644/07-MAMM-A-251R1.1 DOI

Criscione CD, Blouin MS (2006) Minimal selfingm few clones, and no among-host genetic structure in hermaphroditic parasite with asexual larval propagation. Evolution 60:553–562 PubMed

Criscione CD, Cooper B, Blouin MS (2006) Parasite genotypes identify source populations of migratory fish more accurate than fish genotypes. Ecology 87:823–828. https://doi.org/10.1890/0012-9658(2006)87[823:PGISPO]2.0.CO;2 PubMed DOI

Demiaszkiewicz AW, Lachowicz J, Kuligowska I, Pyziel AM, Bełżecki G, Miltko R, Kowalik B, Gogola W, Giżejewski Z (2014) Endoparasites of the European beaver (Castor fiber L. 1758) in northeastern Poland. Bull Vet Inst Pulawy 58:223–227. https://doi.org/10.2478/bvip-2014-0033 DOI

Drózdż J, Demiaszkiewicz AW, Lachowicz J (2000) Travassosius rufus (Trichostrongylidae) – new for Poland nematode of beavers and comments about helminthofauna of these animals. Wiad Parazytol 46:365–368 PubMed

Drózdż J, Demiaszkiewicz AW, Lachowicz J (2004) Endoparasites of the beaver Castor fiber (L.) in northeast Poland. Helminthologia 41:99–101

Dunn AM (2009) Parasites and biological invasions. Adv Parasitol 68:161–184. https://doi.org/10.1016/S0065-308X(08)00607-6 PubMed DOI

Erickson AB (1944) Parasites of beavers, with a note on Paramphistomum castori Kofoid and Park, 1937 a synonym of Stichorchis subtriquetrus. Am Midl Nat 31:625–630. https://doi.org/10.2307/2421411 DOI

Ernst M, Putnová L, Štohl R, Matoušková J (2017) Comparison of Czech and Latvian Beaver Population by Microsatellite Analysis and Genetic Differences between Castor fiber and Castor canadensis. Transylv Rev 25(21):5339–5349 RIV/00216305:26620/17:PU125379 - rvvi.cz

Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multi locus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x PubMed DOI PMC

Fanelli A, Ghirardi M, Meneguz PG et al (2020) First Report of Obeliscoides cuniculi in the European Rabbit (Oryctolagus cuniculus). Acta Parasit 65:787–789. https://doi.org/10.2478/s11686-020-00203-4 DOI

Flowers JR (1996) Three amphistome cercariae (Paramphistomidae) from North Carolina. J Elisha Mitchell Sci Soc 112(2):80–86

Frosch C, Kraus RHS, Angst C, Allgöwer R, Michaux J, Teubner J, Nowak C (2014) The genetic legacy of multiple beaver reintroductions in Central Europe. PLoS ONE 9(5):e97619. https://doi.org/10.1371/journal.pone.0097619 PubMed DOI PMC

Fuehrer HP, Igel P, Auer H (2011) Capillaria hepatica in man—an overview of hepatic capillariosis and spurious infections. Parasitol Res 109(4):969–979. https://doi.org/10.1007/s00436-011-2494-1 PubMed DOI

Fuehrer HP (2014a) An overview on the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 1—Muroidea. Parasitol Res 113(2):619–640. https://doi.org/10.1007/s00436-013-3691-x PubMed DOI

Fuehrer HP (2014b) An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 2—Mammalia (excluding Muroidea). Parasitol Res 113:641–651. https://doi.org/10.1007/s00436-013-3692-9 PubMed DOI

Gasser RB, Chilton NB, Hoste H, Stevenson LA (1994) Species identification of trichostrongyle nematodes by PCR-linked RFLP. Int J Parasitol 24(2):291–293 DOI

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

Ghasemikhah R, Mirhendi H, Kia E, Mowlavi G, Sarmadian H, Meshgi B, Golestan B, Mobedi I (2011) Morphological and morphometrical description of Trichostrongylus species isolated from domestic ruminants in Khuzestan Province, Southwest Iran. Iran J Parasitol 6(3):82–88 PubMed PMC

Ghosh S, Debnath A, Sil A, De S, Chattopadhyay DJ, Das P (2000) PCR detection of Giardia lamblia in stool: targeting intergenic spacer region of multicopy rRNA gene. Mol Cell Probes 14(3):181–189. https://doi.org/10.1006/mcpr.2000.0302 PubMed DOI

Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda, vol I. CABI Publishing, Wallingford DOI

Girling SJ, Naylor A, Fraser M, Campbell-Palmer R (2019) Reintroducing beavers Castor fiber to Britain: a disease risk analysis. Mammal Rev 49:300–323. https://doi.org/10.1111/mam.12163 DOI

Gontero C, Fanaelli A, Zanet S, Giuseppe Meneguz P, Tizzani P (2020) Exotic species and autochthonous parasites: Trichostrongylus retortaeformis in Eastern cottontail. Life 10:31. https://doi.org/10.3390/life10040031 DOI PMC

Heidecke D (1989). Ökologische bewertung von Biberhabitaten Säugetierkd Inf 3(13):13–28

Joszt L (1964) The helminth parasites of European beaver, Castor fiber L., in Poland. Acta Parasitol Pol 12:85–88

Khalil M (1922) Travassosius rufus: a nematode (Trichostrongylidae) parasitic in the stomach of the Norwegian beaver. Ann Mag Nat Hist 10:281–289 DOI

Kleiman DG (1977) Monogamy in mammals. Quart Rev Biol 52:39–69 DOI

Kostkan V, Lehky J (1997) The Litovelske Pomoravi floodplain forest as a habitat for the reintroduction of the European beaver (Castor fiber) into the Czech Republic. Glob Ecol Biogeogr Lett 6:307–310. https://doi.org/10.2307/2997744 DOI

Kostkan V, Šíma J, Uhlíková J, Vorel A (2014) Program péče o bobra evropského. Ochr přír 69(1):10–14

Koubková B, Baruš V, Koubek P (2002) Stichorchis subtriquetrus (Digenea: Cladorchidae) - back to the fauna of the Czech Republic after 200 years. Helminthologia 39:155–158

Leigh J, Bryant D (2015) PopART: Full-Feature Software for Haplotype Network Construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410 DOI

Litvinov VF, Lesko AG (2007) Helminthiasis of European beaver of the Dnieper river basin, Vescì Akademìì navuk BSSR. Seryâ Biâlag navuk 3:120–122

Louhi K-R, Karvonen A, Rellstab C, Jokela J (2010) Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Inf Gen Evol 10:1271–1277. https://doi.org/10.1016/j.meegid.2010.08.013 DOI

Máca O, Pavlásek I, Vorel A (2015) Stichorchis subtriquetrus (Digenea: Paramphistomatidae) from Eurasian beaver (Castor fiber) in the Czech Republic. Parasitol Res 114:2933–2939. https://doi.org/10.1007/s00436-015-4495-y PubMed DOI

Maloň J (2012) Ekologie bobra evropského v podmínkách střední Evropy. Palacký University, Olomouc

Martínez-Aquino A, Chan-Martin AJ, García-Teh JG, Ceccarelli FS, Aguirre-Macedo ML (2019) Metacercariae of Haplorchis pumilio (Looss, 1896) in Carassius auratus (Linnaeus, 1758) from Mérida City, Yucatán, Mexico: a cointroduced parasite. BioInvasions Rec 8(3):712–728. https://doi.org/10.3391/bir.2019.8.3.29 DOI

Mažeika V, Paulauskas A, Balčiauskas L (2003) New data on the helminth fauna of rodents of Lithuania. Acta Zoo Litu 13:41–47. https://doi.org/10.1080/13921657.2003.10512542 DOI

McKown RD, Veatch JK, Robel RJ, Upton SJ (1995) Endoparasites of beaver (Castor canadensis) from Kansas. J Helminthol Soc W 62:89–93

M’Gonigle LK, Shen JJ, Otto SP (2009) Mutating away from your enemies: The Evolution of Mutation Rate in a Host–parasite system. Theor Popul Biol 75:301–311. https://doi.org/10.1016/j.tpb.2009.03.003 PubMed DOI

Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, Chiba S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35(7):793–801. https://doi.org/10.1016/j.ijpara.2005.02.014 PubMed DOI

Miura O, Torchin ME, Kuris AM, Hechinger RF, Chiba S (2006) Introduced cryptic species of parasites exhibit different invasion pathways. Proc Natl Acad Sci U.S.A. 103:19818–19823. https://doi.org/10.1073/pnas.0609603103 PubMed DOI PMC

Moravec F (2013) Parasitic nematodes of freshwater fishes of Europe. Academia, Prague

Ondračková M, Bartáková V, Kvach Y, Bryjová A, Trichkova T, Ribeiro F, Carassou L, Martens A, Masson G, Zechmeister T, Jurajda P (2021) Parasite infection reflects host genetic diversity among non-native populations of pumpkinseed sunfish in Europe. Hydrobiologia 848:2169–2187. https://doi.org/10.1007/s10750-020-04410-y DOI

Orlov IV (1941) Study of the life-cycle of the trematode Stichorchis subtriquetrus Rud., parasitising beavers. DAN SSSR 31:642–644

Orlov IV (1946) Novaâ trematoda kišečnika rečnogo bobra Psilotrema castoris nov. sp. In: Gel’mintologičeskij Sbornik. Izdatel’stvo Akademii Nauk SSSR, Moskva, Leningrad, pp 199–201

Orlov IV (1948) Studies on the helminth fauna of beavers. In: Parazitofauna i zabolevaniya dikikh zhivotnykh. Glav Upr po zapovednikam, pp 114–125

Orlov IV, Dinesman LG (1948) Distribution of larval Stichorchosis in molluscs of the Usmanki River. In: Parazitofauna zabolevantya dikih zhivot. Nauka Publishing House, Moscow

Orlov IV, Romanova NP (1953) Studies on developmental cycle of gastric nematoides in Travassosius rufus Khalil, 1922. Dokl Akad Nauk SSSR 91(3):703–704 PubMed

Pantoja C, Scholz T, Luque JL, Jones A (2019) First molecular assessment of the interrelationships of cladorchiid digeneans (Digenea: Paramphistomoidea), parasites of Neotropical fishes, including descriptions of three new species and new host and geographical records. Folia Parasitologica 66(011). https://doi.org/10.14411/fp.2019.011

Paziewska A, Bednarska M, Niewęgłowski H, Karbowiak G, Bajer A (2007) Distribution of Cryptosporidium and Giardia spp. in neglected species of protected and game mammals from north-eastern Poland. Ann Agric Environ Med 14:265–270 PubMed

Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x DOI

Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update. Bioinformatics 28(19):2537–2539. https://doi.org/10.1093/bioinformatics/bts460 PubMed DOI PMC

Poulin R (1999) Body size vs abundance among parasite species: positive relationships? Ecography 22:246–250 DOI

Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390. https://doi.org/10.1016/j.tree.2004.05.002 PubMed DOI

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x PubMed DOI PMC

Różycki M, Bilska-Zając E, Kochanowski M, Grądziel-Krukowska K, Zdybel J, Karamon J, Wiśniewski J, Cencek T (2020) First case of Trichinella spiralis infection in beavers (Castor fiber) in Poland and Europe. Int J Parasitol Parasites Wildl 11:46–49. https://doi.org/10.1016/j.ijppaw.2019.11.005 PubMed DOI

Reslová N, Škorpíková L, Slaný M, Pozio E, Kašný M (2017) Fast and reliable differentiation of eight Trichinella species using a high resolution melting assay. Sci Rep 7:16210. https://doi.org/10.1038/s41598-017-16329-x PubMed DOI PMC

Romashov VA, Safonov VG (1965) Effect of helminthiasis on populations of European beaver. In: Materiali Nauchnoi Konfferencii Vsesojuznogo Obshesstva Gelmintologii, Part 1, pp 187-192. Romashov VA (1969) Helminth fauna of European beaver in its aboriginal colonies of Eurasia. Acta Parasitol Pol 17:55–64

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: dna sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248 PubMed DOI

Rozsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J parasitol 86:228–232. https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2 PubMed DOI

Ryzhikov KM, ed. (1978) Cestoda and Trematoda. In: Determination key for helminths parasitizing rodents in the USSR. Nauka Publishing House, Moscow

Sager H, Konjević D, Grubešić M, Janicki Z, Severin S, Beck R (2005) Stichorchis subtriquetrus in European beaver from Croatia: first report. Eur J Wildl Res 51:63–64. https://doi.org/10.1007/s10344-004-0076-6 DOI

Segliņa Z, Bakasejevs E, Deksne G, Spuņģis V, Kurjušina M (2015) New finding of Trichinella britovi in a European beaver (Castor fiber) in Latvia. Parasitol Res 114(8):3171–3173. https://doi.org/10.1007/s00436-015-4557-1 PubMed DOI

Šimková A, Řehulková E, Rasoloariniaina JR, Jorissen MWP, Scholz T, Faltýnková A, Mašová Š, Vanhove MPM (2018) Transmission of parasites from introduced tilapias: a new threat to endemic Malagasy ichthyofauna. Biol Invasions 21:803–819. https://doi.org/10.1007/s10530-018-1859-0 DOI

Simon LJ (2006) Solving beaver flooding problems through the use of water flow control devices. In: Proceedings of the Vertebrate Pest Conference (Vol. 22, No. 22), pp 174–180. https://doi.org/10.5070/V422110285

Škorpíková L, Reslová N, Magdálek J, Vadlejch J, Kasny M (2020). The use of high resolution melting analysis of ITS-1 for rapid differentiation of parasitic nematodes Haemonchus contortus and Ashworthius sidemi. Sci Rep 10. https://doi.org/10.1038/s41598-020-73037-9

Skrjabin KI (1949) Trematodes of animals and man. Principles of trematodology, vol 3. Izdatelstvo Akademii Nauk SSSR, Moscow

Sroka J, Giżejewski Z, Wójcik-Fatla A, Stojecki K, Bilska-Zając E, Dutkiewicz J, Cencek T, Karamon J, Zając V, Kusyk P, Dąbrowska J, Kochanowski M (2015) Potential role of beavers (Castor fiber) in contamination of water in the Masurian Lake District (north-eastern Poland) with protozoan parasites Cryptosporidium spp. and Giardia duodenalis. Bull Vet Inst Pulawy 59:219–228. https://doi.org/10.1515/bvip-2015-0033 DOI

Sun L, Müller-Schwarze D, Schulte BA (2000) Dispersal pattern and effective population size of the beaver. Canad J Zool 7:393–398 DOI

Vengušt G, Bidovec A, Vergles Rataj A, Žele D (2009) Stichorchis subtriquetrus in two beavers (Castor fiber) from Slovenia. Helminthologia 46:59–61. https://doi.org/10.2478/s11687-009-0011-1 DOI

Vorel A, Šíma J, Uhlíková J, Peltánová A, Minariková T, Švanyga J (2013). Program péče o bobra evropského v České republice. AOPK a MŽP. https://www.zachranneprogramy.cz/bobr-evropsky/program-pece-pp/?action=download&aId=3680 . Accessed 20.6.2021

Vorel A, Válková L, Hamšíková L, Malon J, Korbelová J (2008) The Eurasian beaver population monitoring status in the Czech Republic. Nat Croat: Period Musei Hist Nat Croat 17(4):217–232

Wang W, Durden LA, Shao R (2020) Rapid host expansion of an introduced parasite, the spiny rat louse Polyplax spinulosa (Psocodea: Phthiraptera: Polyplacidae), among endemic rodents in Australia. Parasites Vectors 13:83. https://doi.org/10.1186/s13071-020-3957-y PubMed DOI PMC

Wróbel M (2020) Population of Eurasian beaver (Castor fiber) in Europe. Glob Ecol Conserv 23:e01046. https://doi.org/10.1016/j.gecco.2020.e01046 DOI

Závodná M, Sandland GJ, Minchella DJ (2008) Effects of intermediate host genetic background on parasite transmission dynamics: A case study using Schistosoma mansoni. Exp Parasitol 120:57–61. https://doi.org/10.1016/j.exppara.2008.04.021 PubMed DOI PMC