Cestoda) in Cultured Common Carp in the Czech Republic Confirms Its Recent Expansion in Europe

Home , Caryophyllidea, Cestoda

The occurrence of the non-native tapeworm Khawia japonensis (Yamaguti, 1934) (Cestoda) in cultured common carp in the Czech Republic confirms its recent expansion in Europe

Tomáš Scholz1,*, Daniel Barčák2 and Mikuláš Oros2 1Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic 2Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia *Corresponding author E-mail: [email protected] Received: 29 January 2018 / Accepted: 13 May 2018 / Published online: 14 June 2018 Handling editor: Andrew David

Abstract

Invasive parasites represent a serious problem due to their capacity to threaten local populations of native (often endemic) hosts, and fishes in breeding facilities. Tapeworms (Cestoda) are extremely adapted (they lack any gut and circulatory system) parasitic flatworms some of which have colonised new geographical regions as a result of unintentional transfer of hosts infected with these parasites. The highest number of invasive parasites within this host-parasite system is among tapeworms parasitizing common carp (Cyprinus carpio L.), which has also been introduced globally. In the present study, we report another record of the Asian non-native fish tapeworm Khawia japonensis (Yamaguti, 1934) (Cestoda: Caryophyllidea) from common carp in Europe. Previous records of this cestode from Italy (Po River basin) and Slovakia (Danube River basin) and its present finding in the Czech Republic (Elbe River basin) confirms recent expansion of the parasite in Europe. Potential impacts of this non-native parasite on common carp in commercial breeding fisheries should be carefully studied. Key words: Parasitic flatworms, Caryophyllidea, Cyprinus carpio, fishponds, Elbe River basin

Introduction with mortality or any obvious decline of host fitness, induces serious local histopathological lesions on Tapeworms (Cestoda) are frequent and widely distri- intestine mucosa (Molnár et al. 2003; Kappe et al. buted intestinal parasites of cultured and wild fish 2006; Gjurcevic et al. 2012). These three species can globally (Williams and Jones 1994; Scholz and Kuchta thus be considered as invasive parasites. In contrast, 2017). Among fish tapeworms, caryophyllideans are the effect of K. japonensis on its definitive fish host the most common parasites of common carp, Cyprinus is still unknown. carpio Linnaeus, which is the most important fish in The Asian fish tapeworm Khawia japonensis was freshwater aquaculture in temperate Europe and Asia described as Caryophyllaeus japonensis from common (Froese and Pauly 2018). Four of these tapeworms, carp in Japan (Figure 1), and its original distribution Atractolytocestus huronensis Anthony, 1958; Khawia included eastern and south eastern Asia (Japan, Amur sinensis Hsü, 1935; K. japonensis (Yamaguti, 1934), River basin in Russia, and Vietnam) (Yamaguti 1934; and possibly Caryophyllaeus fimbriceps Annenkova- Demshin 1978; Protasova et al. 1990; Scholz et al. Chlopina, 1919, have spread from their original 2001, 2011a). Just recently, this rather neglected distribution and colonised new regions including carp parasite that had not previously attracted the new continents (Oros et al. 2004, 2009, 2011; Scholz attention of veterinarians, appeared in Europe: in et al. 2011a). Two of these species, C. fimbriceps common carp from a small irrigation canal in the Po and K. sinensis, are potentially lethal pathogens of carp River basin, northern Italy (Scholz et al. 2011b), and fry (Bauer et al. 1973; Mitterpák and Huňady 1984); from farmed common carp in breeding fishponds in and A. huronensis, which has not been connected the Danube River basin, eastern Slovakia (Oros et al.

303 T. Scholz et al.

2015). In the present report, we present the third record of this non-native parasite in another principal river basin of Europe, which indicates the potential for K. japonensis to invade new geographical regions.

Methods Tapeworms were found in the anterior intestine of one of two common carp, Cyprinus carpio (host code TS-2976; total length of 45 cm) from Velký Tisý fishpond (49º3′42″N; 14º42′55″E) near Třeboň exa- mined on 20 October 2016; and one of eight carp (host code TS-2982; total length of 50 cm) from Horusický fishpond (49º09′23″N; 14º40′37″E) near Veselí nad Lužnicí (both fishponds in South Bohemia, Czech Republic; Elbe River basin) on 26 October 2017. Tapeworms were gently rinsed in a saline solution and the specimen found in 2016 was divided into three parts: the anterior and posterior regions were fixed in hot (almost boiling) 4% formaldehyde solution, whereas the middle part was placed in molecular- grade 99% ethanol. The anterior and posterior parts of the first specimen, i.e. the hologenophore (Figure 2), and the entire, gravid specimen found in 2017, were stained with Mayer’s carmine, mounted in Canada balsam and deposited in the helminthological collection of the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice (Coll. No. IPCAS C-348/1). Genomic DNA was extracted from the middle Figure 1. Distribution of the non-native Khawia japonensis body part of the 2016 specimen (field no. TS-2976a) (Yamaguti, 1934) in A – North America, B – Europe, C – Japan using the DNeasy® Blood & Tissue Kit (QIAGEN, (only the type locality is shown). Number indicates year of first occurrence in a given country, or year of publication of such Hilden, Germany) according to the manufacturer´s finding if it is in parentheses. *, ** Specimens misidentified as instructions. The target D1–D3 region of the large Caryophyllaeus sp. by Wilson (1957) and C. laticeps by Rehder rDNA subunit (lsrDNA) was amplified by using (1959), respectively, in fact represent Khawia iowensis (syn. K. LSU5 and 1500R primers (Littlewood et al. 2000; japonensis) (see Calentine and Ulmer 1961 and Mackiewicz 1970). Only first records of K. japonensis occurrence in a state are Olson et al. 2003) expecting a length of approxima- pointed out, for further geo-referenced data see Supplementary telly 1,600 bp. The PCR amplification was initiated material Table S1. by denaturation for 5 min at 94 °C, followed by 30 cycles of 1 min at 94 °C, 1 min at 55 °C, 2 min at 72 °C, and terminated by 10 min at 72 °C. The purification of PCR products was described in detail and KP790244), K. parva from Russia (JN004267), by Brabec et al. (2012). Sanger sequencing was K. rossittensis from Japan and Slovakia (JN004259 and performed at GATC Biotech (Cologne, Germany) JN004260), K. saurogobii from China (JN004262), using both PCR primers and internal primer 900F and K. sinensis from China, Japan, Slovakia and (Olson et al. 2003). Contiguous sequences were United Kingdom (JN004265, JN004264, JN004261, assembled and inspected for ambiguous and erro- and EU343740). A sequence of Khawia baltica neously sequenced bases using the software platform (JN004266) was not included in the comparison Geneious® (Kearse et al. 2012). The BLAST algorithm because this species in fact belongs to the genus was employed to compare the originally acquired Caryophyllaeus (see Barčák et al. 2017). sequence (acc. no. MH237608) with respective sequences of the congeneric species available in GenBank: Results specifically K. armeniaca from Armenia (JN004257), K. cf. armeniaca from Portugal (JN004263), The tapeworms found in common carp from two K. japonensis from Japan and Slovakia (JN004258 fishponds in South Bohemia possess morphological

304 The occurrence of Khawia japonensis in cultured common carp in the Czech Republic characteristics typical of K. japonensis: an afossate scolex lacking apical and lateral structures, with frilled anterior margin and wedge-shaped projections, only slightly wider than the neck, extensive vitelline follicles separated to preovarian and postovarian groups, with a few follicles present alongside the ovarian arms, and the testes reaching anteriorly at approximately same level as anteriormost vitelline follicles (Figure 2). Moreover, morphometrical comparison of both specimens from the Czech Republic with vouchers of K. japonensis from Asia (Japan and Vietnam), North America (USA) and Europe (Italy and Slovak Republic) showed no obvious differences. Species identification was also confirmed by molecular data.

Morphology Morphological description was based on one complete, gravid specimen (Figure 2), and the anterior and posterior parts of one non-gravid specimen, i.e. a worm without intrauterine eggs: Body subtle, 24 mm long, maximum width (0.91/1.30 mm) at level of anteriormost testes and vitelline follicles (Figure 2A), then narrowing toward posterior end. Scolex cuneifimbriate, i.e. having anterior margin fringed with wedge-shaped projections (Figure 2A), slightly widened, 0.96/1.40 mm. Testes oval to almost Figure 2. Specimen of Khawia japonensis (Yamaguti, 1934) spherical, 63–142 × 58–128 μm (n = 30). Distance of from common carp (Cyprinus carpio), Czech Republic found in anteriormost testes from anterior extremity short, 2017. A – anterior part of body. B – posterior part of body. 1.10/1.57 mm (Figure 2A). First testes begins at Abbreviations: amte – anteriormost testis, amvf – anteriormost approximately same level, i.e. just slightly posterior vitelline follicle, cs – cirrus-sac, ga – genital atrium, ieg – intrauterine egg, ov – ovary, pvf – postovarian vitelline follicle, (50/90 μm) to first vitelline follicles (Figure 2A). te – testes, ut – uterus, vf – vitelline follicle. Scale bars 500 µm. Posteriorly testes reach middle part of cirrus-sac. Microphotographs by R. Kuchta. Cirrus-sac voluminous, oval to subspherical, 540/670 × 351/650 μm, muscular, containing ejaculatory duct and cirrus; its width represents 45/57% of body width at DNA analysis level of cirrus-sac (39/50% of maximum body The partial sequence (D1–D3 regions) of lsrDNA width). Ovary follicular, 0.63/1.10 mm wide; arms was 1,568 bp long and 100% identical with both 1.02–1.95 mm long, 104–340 μm wide (Figure 2B). available sequences of K. japonensis from Lake Vagina tubular, ventral to uterus, proximally enlarged Onuma, Hokkaido, Japan and a fish breeding facility to form seminal receptacle (107/400 × 53/470 μm), near Brzotín village, Slovakia. Unfortunately, no distally joining with uterus to form common molecular data are available for K. japonensis from uterovaginal duct. Genital pores separated, close to the type locality: Lake Biwa, Honshu, Japan. Pairwise each other, opens into genital atrium. Preovarian sequence identity between the originally obtained vitelline follicles lateral and median, surrounding sequence presented herein and the remaining species testes, variable in shape and size, 73–205 × 55–140 μm of Khawia ranged from 92.1 % (K. armeniaca from (n = 30). Anteriormost follicles begin 1.01/1.52 mm Armenia) to 97.4 % (both specimens of K. rossittensis from anterior margin of scolex (Figure 2A), extend from Japan and Slovakia). posteriorly to ovary, with few follicles lateral to ovarian lobes; postovarian follicles present (Figure 2B). Discussion Uterus forms several loops between ovary and posterior part of cirrus-sac (Figure 2B); uterine region In contrast to another Asian carp tapeworm, 1.6/3.4 mm long. Intrauterine eggs 45–53 × 30–33 μm Schyzocotyle acheilognathi (Yamaguti, 1934) (syn. (n = 10). Bothriocephalus acheilognathi; order Bothriocepha-

305 T. Scholz et al. lidea), which is invasive and able to infect an Recently, this cestode has colonised three major extremely wide spectrum of unrelated fishes (Scholz river basins in Europe, having escaped from fish et al. 2012; Kuchta et al. 2018), all invasive or cultures to free waters (Scholz et al. 2011b), which potentially invasive caryophyllideans of carp have a makes its effective control and eradication problematic. strict (oioxenous) or narrow (stenoxenous) host Moreover, pathogenicity of K. japonensis, perhaps specificity (Scholz et al. 2011a; Scholz and Oros intensity-dependent as in congeneric species K. 2017). As tapeworms are entirely dependent on the sinensis (Bauer et al. 1973), is thus far unknown. presence of both definitive and intermediate hosts, a Calentine and Ulmer (1961) recorded a maximum narrow host spectrum may limit their ability to intensity of infection of 624 (immature) specimens, colonise larger areas. However, caryophyllidean but provided no information about the impact on cestodes of carp use similar species of globally host health. Such intensities in a fish appears to be occurring naidids as intermediate hosts (Mackiewicz rare since 9 other fish from the same collection sites 1972; Demshin 1978; Scholz 1991), and common and over a nine-month period had a maximum mean carp has also been distributed worldwide for intensity of only 35 worms. However, considering the aquaculture, game fishing, or as ornamental pond situation of heavily infected farmed young carp, fish (i.e. japanese “koi” or “nishikigoi”). These tape- potentially burdened by low hygiene and poor worms can therefore easily complete their life cycle nutrition as in the case of Caryophyllaeus fimbriceps in newly colonised areas. (see Mitterpák and Huňady 1984), the impact of any Caryophyllidean cestodes of carp differ markedly introduced parasite is unpredictable. from each other in their colonisation success. Caryo- Since K. japonensis has recently been found in phyllaeus fimbriceps, described from the Caspian regions where intensive research on fish parasites Sea region, has been reported only from central and has been carried out, it is unlikely that the parasites eastern Europe and may be autochthonous there have been there for longer but at a low prevalence. It (Barčák et al. 2017). Interestingly, this species may is therefore alarming that this parasite has colonised have disappeared completely because there have three distinct watersheds in Europe within a few been no reliable records of its occurrence for several years (Figure 1). decades (see Barčák et al. 2017). Khawia sinensis, described from China, has successfully colonised Acknowledgements Europe, including the British Isles, and has also been Valuable comments of an anonymous reviewer are much appreciated. reported from North America (Scholz et al. 2011a). The authors are obliged to staff of the Fisheries Třeboň, South However, its expansion does not seem to be continuing, Bohemia, for providing carp for their parasitological examination unlike Atractolytocestus huronensis which is currently and to Jan Brabec and Roman Kuchta (both Institute of Parasitology, the most frequent cestode in common carp, with BC CAS, Budweis, Czech Republic) for help with molecular analysis and taking pictures of K. japonensis, respectively. reports from a number of European countries (Oros Financial support of the Czech Science Foundation (project No. et al. 2011). This tapeworm had been imported to P505/12/G112) and the Institute of Parasitology, BC CAS (RVO: North America together with its specific host from 60077344), Slovak Grant Agency VEGA (project VEGA 2/159/16) Eastern Asia, most probably before or around the and project “Centre of Excellence for Parasitology” (code ITMS: 26220120022), supported by the Research and Development Opera- middle of the 20th century; it was originally described tional Programme funded by the ERDF (0.3), is much appreciated. from common carp from an impoundment of the Huron River (Michigan, USA) by Anthony (1958). References Khawia iowensis was originally found in Cyprinus carpio in Kansas (USA) (Wilson 1957), but was mis- Amin OM (1986) Caryophyllaeidae (Cestoda) from Lake Fishes in identified as Caryophyllaeus sp. (see Mackiewicz Wisconsin with a description of Isoglaridacris multivitellaria sp. n. from Erimyzon sucetta (Catostomidae). Proceedings of the 1970). Calentine and Ulmer (1961) provided a Helminthological Society of Washington 53: 48–58 description of a new species, K. iowensis, from the Anthony JD (1958) Atractolytocestus huronensis n. gen., n. sp. same host in Iowa (USA), which was later syno- (Cestoda: Lytocestidae) with notes on its morphology. nymised with K. japonensis by Scholz et al. (2011a). Transactions of the American Microscopical Society 77: 383– Therefore, records of tapeworms designated as 390, https://doi.org/10.2307/3223860 Anthony JD (1963) Parasites of Eastern Wisconsin fishes. Wisconsin K. iowensis in North America (USA – California, Academy of Sciences, Arts and Letters 52: 83–95 Illinois, Iowa, Kansas, Minnesota, Nebraska, North Barčák D, Oros M, Hanzelová V, Scholz T (2017) A synoptic review Dakota, Oklahoma, Oregon, Tennessee, South Dakota, of Caryophyllaeus Gmelin, 1790 (Cestoda: Caryophyllidea), Wisconsin, Canada – Manitoba, Ontario, Mexico – parasites of cyprinid fishes in the Palaearctic Region. Folia Rio Grande basin; see Supplementary material Table Parasitologica 64: 027, https://doi.org/10.14411/fp.2017.027 Bauer ON, Musselius VA, Strelkov YA (1973) Diseases of Pond S1) represent the first evidence of non-natural Fishes. Israel Program for Scientific Translations, Jerusalem, expansion of K. japonensis to a new continent. 220 pp

306 The occurrence of Khawia japonensis in cultured common carp in the Czech Republic

Brabec J, Scholz T, Králová-Hromadová I, Baszalovicsová E, Olson Oros M, Hanzelová V, Scholz T (2004) The cestode Atractolyto- PD (2012) Substitution saturation and nuclear paralogs of cestus huronensis (Caryophyllidea) continues to spread in commonly employed phylogenetic markers in the Caryo- Europe: new data on the helminth parasite of the common carp. phyllidea, an unusual group of non-segmented tapeworms Diseases of Aquatic Organisms 62: 115–119, https://doi.org/10. (Platyhelminthes). International Journal for Parasitology 42: 3354/dao062115 259–267, https://doi.org/10.1016/j.ijpara.2012.01.005 Oros M, Hanzelová V, Scholz T (2009) Tapeworm Khawia sinensis: Calentine RL (1984) Biology of Archigetes (Caryophyllaeidae) in review of the introduction and subsequent decline of a pathogen Limnodrilus hoffmeisteri (Tubificidae). Proceedings of the of carp, Cyprinus carpio. Veterinary Parasitology 164: 217–222, Helminthological Society of Washington 52: 109–112 https://doi.org/10.1016/j.vetpar.2009.05.010 Calentine RL, Ulmer MJ (1961) Khawia iowensis n. sp. Cestoda: Oros M, Králová-Hromadová I, Hanzelová V, Bruňanská M, Caryophyllaeidae from Cyprinus carpio L. in Iowa. Journal of Orosová M (2011) Atractolytocestus huronensis (Cestoda), a Parasitology 47: 795–805, https://doi.org/10.2307/3275474 new invasive parasite of common carp in Europe. In: Sanders Dechtiar AO (1972) New parasite records for lake Erie fish. Great JD, Peterson SB (eds), Carp: Habitat, Management and Diseases. Lakes Fishery Commission, Technical Report 17, pp 1–20 Nova Science Publishers, New York, NY, USA, pp 85–97 Demshin NI (1978) О биологии Khawia japonensis (Caryophyllidea, Oros M, Barčák D, Bazsalovicsová E, Hanzelová V (2015) Another Cestoda) – паразита амурского сазана [Biology of Khawia invasive Asian fish tapeworm, Khawia japonensis (Yamaguti, japonensis (Caryophyllidea, Cestoda) – a parasite of the Amur 1934), increasing distribution range in Europe. Parasitology carp]. Parazitologiya 12: 493–496 Research 114: 2035–2039, https://doi.org/10.1007/s00436-015-4447-6 Forstie MD, Holloway HL (1984) Parasites of fish from James and Pérez-Ponce de León G, Choudhury A (2005) Biogeography of Sheyenne Rivers, Jamestown Reservoir Complex, and Lake helminth parasites of freshwater fishes in Mexico: the search for Ashtabula in North Dakota. Prairie Naturalist 16: 11–20 patterns and processes. Journal of Biogeography 32: 645–659, Froese R, Pauly D. (Eds) (2018) FishBase. World Wide Web https://doi.org/10.1111/j.1365-2699.2005.01218.x electronic publication. www.fishbase.org (accessed April 2018). Protasova E, Kuperman B, Roytman V, Poddubnaya L (1990) Gjurcevic E, Beck A, Drasner K, Stanin D, Kuzir S (2012) Pathogenicity Kариофиллиды фауны СССР [Caryophyllidea of the fauna of of Atractolytocestus huronensis (Cestoda) for cultured common carp the USSR]. Nauka, Moscow, 238 pp (Cyprinus carpio L.). Veterinarski Arhiv 82: 273–282 Rehder DD (1959) Some aspects of the life of the carp, Cyprinus Kappe A, Seifert T, El-Nobi G, Brauer G (2006) Occurrence of carpio in the Des Moines River, Boone County, Iowa. Iowa Atractolytocestus huronensis (Cestoda, Caryophyllaeidae) in State College Journal of Science 34: 11–26 German pond-farmed common carp Cyprinus carpio. Diseases Robinson GL, Jahn LA (1980) Some observation of fish parasites in of Aquatic Organisms 70: 255–259, https://doi.org/10.3354/dao070255 pool 20, Mississippi River. Transactions of the American Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock Microscopical Society 99: 206–212, https://doi.org/10.2307/3225708 S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Scholz T (1991) Early development of Khawia sinensis Hsü, 1935 Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: An (Cestoda: Caryophyllidea). Folia Parasitologica 38: 133–142 integrated and extendable desktop software platform for the Scholz T, Kuchta R (2017) A digest of bony fish tapeworms. Vie et organization and analysis of sequence data. Bioinformatics 28: Milieu 67: 43–58 1647–1649, https://doi.org/10.1093/bioinformatics/bts199 Scholz T, Oros M (2017) Caryophyllidea van Beneden in Carus, Kuchta R, Choudhury A, Scholz T (2018) Asian fish tapeworm: the 1863. In: Caira JN, Jensen K (eds), Planetary Biodiversity most successful invasive parasite in freshwaters. Trends in Inventory (2008–2017): Tapeworms from Vertebrate Bowels of Parasitology 34: 511–523, https://doi.org/10.1007/s11230-018-9796-y the Earth. University of Kansas, Natural History Museum, Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The inter- Special Publication No. 25, Lawrence, KS, USA, pp 47–64 relationships of Proseriata (Platyhelminthes: Seriata) flatworms Scholz T, Brabec J, Králová-Hromadová I, Oros M, Bazsalovicsová tested with molecules and morphology. Molecular Phylogenetics E, Ermolenko A, Hanzelová V (2011a) Revision of Khawia spp. and Evolution 16: 449–466, https://doi.org/10.1006/mpev.2000.0802 (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a Mackiewicz JS (1964) Variations and host-parasite relationships of key to their identification and molecular phylogeny. Folia caryophyllaeids (Cestoidea) from fish of Lake Texoma, Marshall Parasitologica 58: 197–223, https://doi.org/10.14411/fp.2011.020 County, Oklahoma. Journal of Parasitology 50: 31 Scholz T, Binh TT, Dezfuli BS (2011b) Khawia japonensis (Cestoda: Mackiewicz JS (1969) Penarchigetes oklensis gen. et sp. n. and Caryophyllidea): another invasive parasite of carp, Cyprinus Biacetabulum carpiodi sp. n. (Cestoidea: Caryophyllaeidae) carpio L., imported to Europe. Journal of Fish Diseases 34: from catostomid fish in North America. Proceedings of the 943–949, https://doi.org/10.1111/j.1365-2761.2011.01311.x Helminthological Society of Washington 36: 119–126 Scholz T, Kuchta R, Williams C (2012) Bothriocephalus achelognathi. Mackiewicz JS (1970) Edlintonia ptychocheila gen. n. sp. n. In: Woo PTK, Buchmann K (eds), Fish Parasites. Pathobiology (Cestoidea: Capengentidae) and other caryophyllid tapeworms and protection. CAB International, Wallingford, Chapter 18, pp from cyprinid fishes of North America. Proceedings of the 282–297, https://doi.org/10.1079/9781845938062.0282 Helminthological Society of Washington 37: 110–118 Scholz T, Shimazu T, Olson PD, Nagasawa K (2001) Caryophylli- Mackiewicz JS (1972) Caryophyllidea (Cestoidea): a review. dean tapeworms (Platyhelminthes: Eucestoda) from freshwater Experimental Parasitology 31: 417–512, https://doi.org/10.1016/ fishes in Japan. Folia Parasitologica 48: 275–288, https://doi.org/ 0014-4894(72)90103-8 10.14411/fp.2001.046 Mitterpák J, Huňady J (1984) K ekonomickej závažnosti Caryo- Sutherland DR (1989) Seasonal distribution and ecology of three phyllaeus fimbriceps u kaprovitých rýb. [Economic importance helminth species infecting carp (Cyprinus carpio) in northwest of Caryophyllaeus fimbriceps in carp]. Veterinářství 34: 125 Iowa, USA. Canadian Journal of Zoology 67: 692–698, Molnár K, Majoros G, Csaba G, Szekely C (2003) Pathology of https://doi.org/10.1139/z89-100 Atractolytocestus huronensis Anthony, 1958 (Cestoda, Caryo- Sutherland DR, Holloway HL (1979) Parasites of fish from the phyllaeidae) in Hungarian pond-farmed common carp. Acta Missouri, James, Sheyenne, and Wild Rice Rivers in North Parasitologica 48: 222–228 Dakota. Proceedings of the Helminthological Society of Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Washington 46: 128–134 Phylogeny and classification of the Digenea (Platyhelminthes: Szalai AJ (1989) Factors affecting community structure, transmission, Trematoda). International Journal for Parasitology 33: 733–755, and regulation of fish-parasites in Dauphin lake, Manitoba. PhD https://doi.org/10.1016/S0020-7519(03)00049-3 Thesis, The University of Manitoba, Winnipeg, Manitoba, 297 pp

307 T. Scholz et al.

US Fish & Wildlife Service (2009) Survey of Pathogens and Williams H, Jones A (1994) Parasitic Worms of Fish. Taylor & Parasites in Fish from Devils Lake and Lake Ashtabula in North Francis Ltd., London, 593 pp Dakota and Lake Traverse, South Dakota. Bozeman Fish Health Wilson WD (1957) Parasites of fishes from Leavenworth County Center Bozeman, Montana, 78 pp State Lake, Kansas. Transactions of the Kansas Academy of Williams DD (1977) A key to caryophyllaeid cestodes of Wisconsin Science 60: 393–399, https://doi.org/10.2307/3626394 fishes. Iowa State Journal of Research 51: 471–477 Yamaguti S (1934) Studies on the helminth fauna of Japan. Part 4. Williams DD (1980) Caryophyllidean tapeworms and their hosts. Cestodes of fishes. Japanese Journal of Zoology 6: 1–112 Reports on the Fauna and Flora of Wisconsin No. 17. The Museum of Natural History, Stevens Point, Winsconsin, pp 1–25

Supplementary material The following supplementary material is available for this article: Table S1. The primary geo-referenced data of K. japonensis occurence in Japan, Europe and N. America. This material is available as part of online article from: http://www.reabic.net/journals/bir/2018/Supplements/BIR_2018_Scholz_etal_Table_S1.xlsx

308