Folia Parasitologica, vol. 64 (2017)

Folia Parasitologica 64:027 (2017) | 10.14411/fp.2017.027

A synoptic review of Caryophyllaeus Gmelin, 1790 (Cestoda: Caryophyllidea), parasites of cyprinid fishes

Daniel Barčák1, Mikuláą Oros1, Vladimíra Hanzelová1, Tomáą Scholz2
1 Institute of Parasitology, Slovak Academy of Sciences, Koąice, Slovak Republic;
2 Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic This article contains supporting information (Table S1) online at http://folia.paru.cas.cz/suppl/2017-64-027.pdf

Tapeworms of the genus Caryophyllaeus Gmelin, 1790 (Caryophyllidea: Caryophyllaeidae), common parasites of cyprinid fishes, are reviewed and taxonomic status of 42 nominal taxa that have been placed in the genus during its long history is clarified. The following seven species occurring in the Palaearctic Region are recognised as valid: C. laticeps (Pallas, 1781), C. auriculatus (Kulakovskaya, 1961), C. balticus (Szidat, 1941) comb. n. (syn. Khawia baltica Szidat, 1941), C. brachycollis Janiszewska, 1953, C. fimbriceps Annenkova-Chlopina, 1919, C. syrdarjensis Skrjabin, 1913, and newly described Caryophyllaeus chondrostomi sp. n. (= C. laticeps morphotype 4 of Bazsalovicsová et al., 2014) from common nase, Chondrostoma nasus (Linnaeus), found in Austria and Slovakia. The new species differs by the paramuscular or cortical position of preovarian vitelline follicles, a large, robust body (up to 64 mm long), conspicuously long vas deferens, flabellate scolex with small wrinkles on the anterior margin, and anteriormost testes located in a relatively short distance from the anterior extremity. Caryophyllaeus kashmirenses Mehra, 1930 and Caryophyllaeus prussicus (Szidat, 1937) comb. n. are considered to be species inquirendae, C. truncatus von Siebold in Baird, 1853 and C. tuba von Siebold in Baird, 1853 are nomina nuda. Data on the morphology, host spectra, distribution and known life-cycles of valid species are provided. Phylogenetic interrelations of four species of the genus including its type species and newly described C. chondrostomi were assessed based on an analysis of sequences of lsrDNA and cox1. A key to identification of all valid species of Caryophyllaeus is also provided.

Keywords: tapeworms, freshwater fish, Cyprinidae, systematics, identification key, phylogenetic relationships, Palaearctic Region

Received: February 8, 2017; Accepted: June 18, 2017; Published online: August 16, 2017



This article contains supporting information (Table S1) online at http://folia.paru.cas.cz/suppl/2017-64-027.pdf


Attachments:

Download fileFP_064_027_Suppl.pdf

File size: 200.46 kB

References

  1. Anderson R.M. 1974a: Population dynamics of the cestode Caryophyllaeus laticeps (Pallas, 1781) in the bream (Abramis brama L.). J. Anim. Ecol. 43: 305-321. Go to original source...
  2. Anderson R.M. 1974b: Mathematical models of host-helminth parasite interactions. In: M.B. Usher and M.H. Williamson (Eds.), Ecological Stability. Chapman and Hall, Ltd., London, pp. 43-69.
  3. Anderson R.M. 1976: Seasonal variation in population dynamics of Caryophyllaeus laticeps. Parasitology 72: 281-305. Go to original source... Go to PubMed...
  4. Annenkova-Chlopina N.P. 1919: [Two new species of parasitic helminths of the genus Caryophyllaeus, found in the intestine of cyprinid fishes.] Izv. Ross. Akad. Nauk, Serie VI, 12: 97-110. (In Russian.)
  5. Ash A., Scholz T., Oros M., Kar P.K. 2011a: Tapeworms (Cestoda: Caryophyllidea), parasites of Clarias batrachus (Pisces: Siluriformes) in the Indomalayan Region. J. Parasitol. 97: 435-459. Go to original source... Go to PubMed...
  6. Ash A., Scholz T., Oros M., Levron C., Kar P.K. 2011b: Cestodes (Caryophyllidea) of the stinging catfish Heteropneustes fossilis (Siluriformes: Heteropneustidae) from Asia. J. Parasitol. 97: 899-907. Go to original source... Go to PubMed...
  7. Baird W. 1853: Catalogue of the Species of Entozoa, or Intestinal Worms, Contained in the Collection of the British Museum.Woodfall and Kinder, London, 132 pp.
  8. Barčák D., Oros M., Hanzelová V., Scholz T. 2014: Phenotypic plasticity in Caryophyllaeus brachycollis Janiszewska, 1953 (Cestoda: Caryophyllidea): does fish host play a role? Syst. Parasitol. 88: 153-166. Go to original source... Go to PubMed...
  9. Bauer O.N., Musselius V.A., Strelkov Y.A. 1973: Diseases of Pond Fishes. Israel Program for Scientific Translations, Jerusalem, 220 pp.
  10. Bazitov A.A. 1979: [Spermatogenesis in Caryophyllaeus fimbriceps and Khawia sinensis (Caryophyllidea).] Mat. Nauchn. Konf. Vsesoyuz. Obshch. Gelmintol. 31: 3-9. (In Russian.)
  11. Bazsalovicsová E., Králová-Hromadová I., Brabec J., Hanzelová V., Oros M., Scholz T. 2014: Conflict between morphology and molecular data: a case of the genus Caryophyllaeus (Cestoda, Caryophyllidea), monozoic tapeworm of cyprinid fishes. Folia Parasitol. 61: 346-352. Go to original source...
  12. Bazsalovicsová E., Králová-Hromadová I., ©tefka J., Scholz T., Hanzelová V., Vávrová S., Szemes T., Kirk R. 2011: Population study of Atractolytocestus huronensis (Cestoda: Caryophyllidea), an invasive parasite of common carp introduced to Europe: mitochondrial cox1 haplotypes and intragenomic ribosomal ITS2 variants. Parasitol. Res. 109: 125-131. Go to original source... Go to PubMed...
  13. Béguin F. 1966: Etude au microscope électronique de la cuticle et de ses structures associées chez quelques cestodes. Essai d'histologie comparée. Z. Zellforsch. 72: 30-46. Go to original source... Go to PubMed...
  14. van Beneden P.J. 1858: Mémoire sur les Vers Intestinaux. C. R. Sci. Soc. Biol., Paris 2: 376 pp.
  15. Biserova N.M., Kuryrev I.A., Jensen K. 2014: GABA in the nervous system of the cestodes Diphyllobothrium dendriticum (Diphyllobothriidea) and Caryophyllaeus laticeps (Caryophyllidea), with comparative analysis of muscle innervation. J. Parasitol. 100: 411-421. Go to original source... Go to PubMed...
  16. Bloch M.E. 1782: Abhandlung von der Erzeugung der Eingeweidewürmer und den Mitteln wieder dieselben: eine von der Königlich Dänischen Societät der Wissenschaften zu Copenhagen gekrönte Preisschrift. S. F. Hesse, Berlin, 54 pp.
  17. Brabec J., Scholz T., Králová-Hromadová I., Bazsalovicsová E., Olson P.D. 2012: Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of non-segmented tapeworms (Platyhelminthes). Int. J. Parasitol. 42: 259-267. Go to original source... Go to PubMed...
  18. Bruňanská M., Drobníková P., Mackiewicz J.S., Nebesářová J. 2013: Reinvestigation of vitellogenesis in Caryophyllaeus laticeps (Pallas, 1781) (Cestoda, Caryophyllidea, Caryophyllaeidae), monozoic tapeworm of Abramis brama (Pisces, Teleostei). Helminthologia 50: 73-81.
  19. Bruňanská M., Kostič B. 2012: Revisiting caryophyllidean type of spermiogenesis in the Eucestoda based on spermatozoon differentiation and ultrastructure of Caryophyllaeus laticeps (Pallas, 1781). Parasitol. Res. 110: 141-149. Go to original source... Go to PubMed...
  20. Calentine R.L., Ulmer M.J. 1961: Khawia iowensis n. sp. (Cestoda: Caryophyllaeidae) from Cyprinus carpio L. in Iowa. J. Parasitol. 47: 795-805. Go to original source...
  21. Chen C.L. 1973: [An Illustrated Guide to the Fish Diseases and Causative Pathogenic Fauna and Flora in Hubei Province.] Science Press, Beijing, 271 pp. (In Chinese.)
  22. Chervy L. 2002: The terminology of larval cestodes or metacestodes. Syst. Parasitol. 52: 1-33. Go to original source... Go to PubMed...
  23. Chervy L. 2009: Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002-2008. Folia Parasitol. 56: 199-230. Go to original source... Go to PubMed...
  24. Chubb J.C. 1982: Seasonal occurrence of helminths in freshwater fishes. Part IV. Adult Cestoda, Nematoda and Acanthocephala. Adv. Parasitol. 20: 1-292. Go to original source... Go to PubMed...
  25. Davydov V.G., Poddubnaya L.G. 1988: [Functional morphology of frontal and uterine glands in cestodes of the order Caryophyllidea.] Parazitologiya 22: 449-457. (In Russian.)
  26. Davydov V.G., Poddubnaya L.G., Kolesnikova G.A. 1994: [Ultrastructure of genital system ducts of Caryophyllaeus laticeps (Cestoda, Caryophyllidea).] Parazitologiya 28: 501-509. (In Russian.)
  27. Demshin N.I. 1984: [Biology of Caryophyllaeus fimbriceps Annenkova-Chlopina, 1919 and Khawia parva (Zmejev, 1936) (Caryophyllidea, Cestoda) - parasites of cyprinid fish.] Parazity Zhivotnykh i Rastenii, AN SSSR: 63-70. (In Russian.)
  28. Dikanović V., Skorić S., Cakić P. 2013: Representatives of tapeworms (Cestoda) of fishes in Belgrade section of the Danube river. In: V. Poleksić (Ed.), VI Int. Conf. Water & Fish. Faculty of Agriculture, University of Belgrade, Belgrade. Abstracts of papers, pp. 402-408.
  29. Dogiel V.A., Bykhovsky B.E. 1939: [Parasites of the Caspian Sea Fishes.] Academy of Sciences of the USSR, Moscow - Leningrad, 151 pp. (In Russian.)
  30. Dubinina M.N. 1962: [Class tapeworms Cestoidea Rud., 1801.] In: B.E. Bykhovskii (Ed.), Key to the Parasites of Freshwater Fish of the USSR. Izd. Akad. Nauk. USSR, Moscow - Leningrad, pp. 384-438. (In Russian.)
  31. Dubinina M.N. 1987: [Class Tapeworms - Cestoda Rudolphi, 1808.] In: O.N. Bauer (Ed.), Key to the Parasites of Freshwater Fishes of the USSR. Nauka, Leningrad, pp. 5-76. (In Russian.)
  32. Evlanov I.A., Kolokolnikova S.E. 1991: [Population ecology of the cestode Caryophyllaeus laticeps (Cestoda, Caryophyllidae) in the bream population.] Zool. Zh. 70: 12-16. (In Russian.)
  33. Evlanov I.A., Kolokolnikova S.E., Kozlovsky S.V. 1992: [Population genetic interrelations in the bream Caryophyllaeus laticeps (Cestoda) system.] Parazitologiya 26: 240-245. (In Russian.)
  34. Fotedar D.N. 1958: On a new caryophyllaeid cestode, Adenoscolex oreini gen. et sp. nov. from fresh-water in Kashmir, and a note on some related genera. J. Helminthol. 32: 11-16. Go to original source...
  35. Froese R., Pauly D. 2016: Fishbase. World Wide Web electronic publication. www.fishbase.org, 10/2016.
  36. Fuhrmann O., Baer J.G. 1925: Zoological results of the third Tanganyika expedition conducted by Dr. W.A. Cunnington, 1904-1905. Report on the Cestoda. Proc. Zool. Soc. London 1925 (No. VI): 79-100.
  37. Georgescu R., Naziru M. 1984: [Health status of fish population in lakes near the capital.] Bul. Cercetari Piscicole, Dimbovita 4: 91-98. (In Romanian, with English summary.)
  38. Gibson D.I. 2013a: Fauna Europaea: Caryophyllidea, Caryophyllaeus laticeps. Fauna Europaea version 2.6.2, www.faunaeur.org.
  39. Gibson D.I. 2013b: Fauna Europaea: Caryophyllidea, Khawia baltica. Fauna Europaea version 2.6.2, www.faunaeur.org.
  40. Gibson D.I. 2013c: Fauna Europaea: Caryophyllidea, Caryophyllaeus brachycollis. Fauna Europaea version 2.6.2, www.faunaeur.org.
  41. Gibson D.I. 2013d: Fauna Europaea: Caryophyllidea, Caryophyllaeus fimbriceps. Fauna Europaea version 2.6.2, www.faunaeur.org.
  42. Gibson D.I., Bray R.A., Harris E.A. (Compilers) 2005: Host-Parasite Database of the Natural History Museum, London. www.nhm.ac.uk.
  43. Gmelin J.F. 1790: Caroli a Linné, Systema Naturae. Tom. I. Pars VI. Beer, Lipsiae, pp. 3021-3910.Goeze J.A.E. 1782: Versuch einer Naturgeschichte der Eingeweidewürmer thierischer Körper. Ph.U. Pape, Blankenburg, 472 pp.
  44. Hanzelová V., Oros M., Barčák D., Miklisová D., Kirin D., Scholz T. 2015: Morphological polymorphism in tapeworms: redescription of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts. Syst. Parasitol. 90: 177-190. Go to original source... Go to PubMed...
  45. Hunter G.W. III. 1927: Notes on the Caryophyllaeidae of North America. J. Parasitol. 14: 16-26. Go to original source...
  46. Hunter G.W. III. 1930: Studies on the Caryophyllaeidae of North America. Illinois Biol. Monogr. 11 (1927), 186 pp. Go to PubMed...
  47. ICZN 1999: International Code of Zoological Nomenclature, Fourth Edition. The International Trust for Zoological Nomenclature, London, 306 pp.
  48. Izvekova G.I., Kuperman B.I., Kuzmina V.V. 1997: Digestion and digestive-transport surfaces in cestodes and their fish hosts. Comp. Biochem. and Physiol. 118A: 1165-1171. Go to original source...
  49. Izvekova G.I., Solovyev M.M. 2013: Activity of digestive hydrolases in fish infected with cestodes. Biol. Bull. Rev. 3: 167-175. Go to original source...
  50. Izvekova G.I., Solovyev M.M., Izvekov E.I. 2011: Effect of Caryophyllaeus laticeps (Cestoda, Caryophyllidea) upon activity of digestive enzymes in bream. Biol. Bull. 2011: 50-56.
  51. Janiszewska J. 1953: Caryophyllaeus brachycollis n. sp. from ciprinoid [sic!] fishes. Zool. Pol. 6: 57-68.
  52. Janiszewska J. 1954: [Caryophyllaeidae of Europe with focus on Poland.] Prace Wroclawskiego Towarzystva Naukowego, Seria B, 66, 74 pp. (In Polish.)
  53. Joyeux C., Baer J.G. 1936: Faune de France, 30. Cestodes. Lechevalier et Fils, Paris, 613 pp.
  54. Karanis P., Taraschewski H. 1993: Host parasite interface of Caryophyllaeus laticeps (Eucestoda, Caryophyllidae) in three species of fish. J. Fish Dis. 16: 371-379. Go to original source...
  55. Katoh K., Standley D.M. 2013: MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780. Go to original source... Go to PubMed...
  56. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Mentjies P., Drummond A. 2012: Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. Go to original source... Go to PubMed...
  57. Kennedy C.R. 1968: Population biology of the cestode Caryophyllaeus laticeps (Pallas, 1781) in dace, Leuciscus leuciscus L., of the River Avon. J. Parasitol. 54: 538-543. Go to original source...
  58. Kennedy C.R. 1969: Seasonal incidence and development of the cestode Caryophyllaeus laticeps (Pallas) in the River Avon. Parasitology 59: 783-794. Go to PubMed...
  59. Kennedy C.R. 1994: The ecology of introductions. In: A.W. Pike and J.W. Lewis (Eds.), Parasitic Diseases of Fish. Samara Publishing Limited, Tresaith, pp. 189-209.
  60. Kennedy C.R. 1998: Aquatic birds as agents of parasite dispersal: a field test of the effectiveness of helminth colonisation strategies. Bull. Scand. Soc. Parasitol. 8: 23-28.
  61. Kennedy C.R., Walker P.J. 1969: Evidence for an immune response by dace, Leuciscus leuciscus, to infections by the cestode Caryophyllaeus laticeps. J. Parasitol. 55: 579-582. Go to original source... Go to PubMed...
  62. Khara H., Sattari M., Nezami S. 2011: Parasites of some bony fishes in Boojagh wetland from the southwest of the Caspian Sea. Caspian J. Environ. Sci. 9: 37-46.
  63. Körting W. 1975: Larval development of Bothriocephalus sp. (Cestoda: Pseudophyllidea) from carp (Cyprinus carpio L.) in Germany. J. Fish Biol. 7: 727-733. Go to original source...
  64. Králová-Hromadová I., Bazsalovicsová E., Bokorová V., Hanzelová V. 2013: Ribosomal ITS2 structure in Caryophyllaeus laticeps and Caryophyllaeus brachycollis (Cestoda: Caryophyllidea), parasites of cyprinid fish. Helminthologia 50: 235-237. Go to original source... Go to PubMed...
  65. Králová-Hromadová I., Bazsalovicsová E., Oros M., Scholz T. 2012: Sequence structure and intragenomic variability of ribosomal ITS2 in monozoic tapeworms of the genus Khawia (Cestoda: Caryophyllidea), parasites of cyprinid fish. Parasitol. Res. 111: 1621-1627. Go to original source... Go to PubMed...
  66. Králová-Hromadová I., Minárik G., Bazsalovicsová E., Mikulíček P., Oravcová A., Pálková L., Hanzelová V. 2015: Development of microsatellite markers in Caryophyllaeus laticeps (Cestoda: Caryophyllidea), monozoic fish tapeworm, using next-generation sequencing approach. Parasitol. Res. 114: 721-726. Go to original source... Go to PubMed...
  67. Kulakovskaya O.P. 1961: [On the fauna of the Caryophyllaeidae (Cestoda, Pseudophyllidea) of the USSR.] Parazitol. Sb. 20: 339-354. (In Russian.)
  68. Kulakovskaya O.P. 1962: [Development of Caryophyllaeidae (Cestoda) in an intermediate host.] Zool. Zh. 41: 986-992. (In Russian, with English summary.)
  69. Kulakovskaya O.P. 1969: [Cestodes of freshwater fish of the Ukrainian SSR.] Summary (Avtoreferat) of D.Sc. thesis. Academy of Sciences of the Ukrainian SSR, Kiev, 45 pp. (In Ukrainian.)
  70. Kulakovskaya O.P., Svirepo B.G. 1967: [Alteration of some blood indices of carp and sazan-carp hybrids on infection with Caryophyllaeidae.] Vest. Zool. 6: 38-42. (In Russian.)
  71. Kulmatycki W.J. 1928: Caryophyllaeus niloticus nov. sp. In: S. Jägerskiöld (Ed.), Results of the Swedish Zoological Expedition to Egypt and the White Nile 1901. Uppsala, pp. 1-19.
  72. Kurbanova A.I., Urazbaev A.N., Yusupov O.Y. 2002: [Changes in parasite fauna of certain fish species in the southern Aral Sea under anthropogenic pressure.] Vestn. Zool. 36: 29-34. (In Russian.)
  73. Lanfear R., Calcott B., Ho S.Y., Guindon S. 2012: PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29: 1695-1701. Go to original source... Go to PubMed...
  74. Littlewood D.T.J., Curini-Galletti M., Herniou E.A. 2000: The interrelationships of Proseriata (Platyhelminthes: Seriata) flatworms tested with molecules and morphology. Mol. Phylogenet. Evol. 16: 449-466. Go to original source... Go to PubMed...
  75. Littlewood D.T.J., Olson P.D. 2001: Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: D.T.J. Littlewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 262-278.
  76. Lockyer A.E., Olson P.D., Littlewood D.T.J. 2003: Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol. J. Linn. Soc. 78: 155-171. Go to original source... Go to PubMed...
  77. Lühe M. 1910: Die Süsswasserfauna Deutschlands. Parasitische Plattwürmer. II. Cestodes. Gustav Fischer Verlag, Jena, 153 pp.
  78. Mackiewicz J.S. 1962: Systematic position of Caryophyllaeus fuhrmanni Szidat, 1937 and Lytocestus alestesi Lynsdale, 1956 (Cestoidea: Caryophyllidea). Rev. Suisse Zool. 69: 729-735. Go to original source...
  79. Mackiewicz J.S. 1968: Vitellogenesis and eggshell formation in Caryophyllaeus laticeps (Pallas) and Caryophyllaeides fennica (Schneider) (Cestoidea: Caryophyllaeidea). Z. Parasitenkd. 30: 18-32. Go to original source... Go to PubMed...
  80. Mackiewicz J.S. 1972: Caryophyllidea (Cestoidea): a review. Exp. Parasitol. 31: 417-512. Go to original source... Go to PubMed...
  81. Mackiewicz J.S. 1974: The genus Caryophyllaeus Gmelin (Cestoidea: Caryophyllidea) in the Nearctic. Proc. Helminthol. Soc. Wash. 41: 184-191.
  82. Mackiewicz J.S. 1994: Order Caryophyllidea van Beneden in Carus, 1863. In: L.F. Khalil, A. Jones and R.A. Bray (Eds.), Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, pp. 21-43.
  83. Mariaux J. 1998: A molecular phylogeny of the Eucestoda. J. Parasitol. 84: 114-124. Go to original source... Go to PubMed...
  84. Mehra H.R. 1930: On a new species of Caryophyllaeus O. F. Müller from Kashmir with remarks on Lytocestus indicus (Moghe) 1925. Proc. 17th Ind. Sci. Congress, pp. 247.
  85. Milbrink G. 1975: Population biology of the cestode Caryophyllaeus laticeps (Pallas) in bream, Abramis brama (L.), and the feeding of fish on oligochaetes. Rep. Inst. Freshw. Res., Drottningholm, Lund 54: 36-51.
  86. Mitterpák J., Huňady J. 1984: [Economic importance of Caryophyllaeus fimbriceps in carp]. Veterinářství 34: 125. (In Slovak.)
  87. Mrázek A. 1901: [Ueber die Larve von Caryophyllaeus mutabilis Rud.] Cbl. Bakteriol., Parasitenkd. Infektionskrankh. 29: 485-491.
  88. Müller O.F. 1787: Verzeichniss der bisher entdeckten Eingeweidewürmer, der Thiere, in welchen sie gefunden worden, und der besten Schriften, die derselben erwähnen. Naturforscher 22: 33-86.
  89. Musselius V., Ivanova N., Laptev V., Apazidi L. 1964: [Khawia sinensis Hsü, 1935 of carp.] Ribov. Ribolovstvo 3: 25-27. (In Russian.)
  90. Nybelin O. 1922: Anatomisch-systematische Studien über Pseudophyllideen. Göteborgs Kungl. Vet. Vitt.-Samh. Handl. 26: 1-228.
  91. Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003: Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int. J. Parasitol. 33: 733-755. Go to original source... Go to PubMed...
  92. Olson P.D., Littlewood D.T.J., Bray R.A., Mariaux J. 2001: Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol. Phylogenet. Evol. 19: 443-467. Go to original source... Go to PubMed...
  93. Olson P.D., Poddubnaya L.G., Littlewood D.T.J., Scholz T. 2008: On the position of Archigetes and its bearing on the early evolution of the tapeworms. J. Parasitol. 94: 898-904. Go to original source... Go to PubMed...
  94. Oros M., Hanzelová V., Scholz T. 2004: The cestode Atractolytocestus huronensis (Caryophyllidea) continues to spread in Europe: new data on the helminth parasite of the common carp. Dis. Aquat. Organ. 62: 115-119. Go to original source... Go to PubMed...
  95. Oros M., Hanzelová V., Scholz T. 2009: Tapeworm Khawia sinensis: review of the introduction and subsequent decline of a pathogen of carp, Cyprinus carpio. Vet. Parasitol. 164: 217-222. Go to original source... Go to PubMed...
  96. Oros M., Hanzelová V., Scholz T., Mackiewicz J.S. 2008: Phylogenetic relationships of the monozoic tapeworms (Eucestoda: Caryophyllidea) inferred from morphological characters. Syst. Parasitol. 70: 1-14. Go to original source... Go to PubMed...
  97. Oros M., Scholz T., Hanzelová V., Mackiewicz J.S. 2010: Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaearctic Region: a useful tool for species identification. Folia Parasitol. 57: 37-46. Go to original source... Go to PubMed...
  98. Pallas P.S. 1781: Bemerkungen über die Bandwürmer in Menschen und Tieren. Neu Nordische Beytrage zur physikalischen und geographischen Erd- und Völker Beschreibung, Naturgeschichte und Ökonomie. Erster Band. J.Z. Logan, St. Peterburg and Leipzig, pp. 39-112.
  99. Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P., Thollesson M. 2008: Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol. Phyl. Evol. 48: 369-371. Go to original source... Go to PubMed...
  100. Poddubnaya L.G. 1995: [Peculiarities of the integument genesis in procercoids of caryophyllidean cestodes.] Parazitologiya 29: 13-18. (In Russian.)
  101. Poddubnaya L.G. 1996: [A development of microtriches in caryophylloid cestodes.] Parazitologiya 30: 126-131. (In Russian.)
  102. Protasova E., Kuperman B., Roytman V., Poddubnaya L. 1990: [Caryophyllidea of the fauna of the USSR.] Nauka, Moscow, 238 pp. (In Russian.)
  103. Rahemo Z.I.F., Mohammad S.A. 2004: Four species of monozoic cestodes from the intestine of cyprinid fishes in Iraq. Dirasat Med. Biol. Sci. 31: 149-155.
  104. Reda E.S.A. 1988: An analysis of parasite fauna of bream, Abramis brama (L.), in Vistula near Warszawa in relation to the character of fish habitat. I. Review of parasite species. Acta Parasitol. Pol. 32: 309-326.
  105. Rehder D.D. 1959: Some aspects of the life of the carp, Cyprinus carpio in the Des Moines River, Boone County, Iowa. Iowa State J. Sci. 34: 11-26.
  106. Richards K.S., Arme C. 1982a: Sensory receptors in the scolex-neck region of Caryophyllaeus laticeps (Caryophyllidea: Cestoda). J. Parasitol. 68: 416-423. Go to original source...
  107. Richards K.S., Arme C. 1982b: The microarchitecture of the structured bodies in the tegument of Caryophyllaeus laticeps (Caryophyllidea: Cestoda). J. Parasitol. 68: 425-432. Go to original source...
  108. Sattari M., Mokhayer B., Khara H., Nezami S., Shafii S. 2007: Occurrence and intensity of parasites in some bonyfish species of Anzali wetland from the southwest of the Caspian Sea. Bull. Eur. Assoc. Fish Pathol. 27: 54-60.
  109. Schaeffner B.C., Jirků M., Mahmoud Z.N., Scholz T. 2011: Revision of Wenyonia Woodland, 1923 (Cestoda: Caryophyllidea) from catfishes (Siluriformes) in Africa. Syst. Parasitol. 79: 83-107. Go to original source... Go to PubMed...
  110. Schmidt G.D. 1986: CRC Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, 675 pp.
  111. Scholz T. 1987: First record of the cestode Monobothrium wageneri Nybelin, 1922 (Caryophyllidea) in Czechoslovakia. Folia Parasitol. 34: 128-130.
  112. Scholz T. 1989: Amphilinida and Cestoda, Parasites of Fish in Czechoslovakia. Academia, Praha, 56 pp.
  113. Scholz T. 1993: On the development of Khawia baltica Szidat, 1942 (Cestoda, Lytocestidae), a parasite of tench, Tinca tinca (L). Folia Parasitol. 40: 99-103.
  114. Scholz T., Brabec J., Králová-Hromadová I., Oros M., Bazsalovicsová E., Ermolenko A., Hanzelová V. 2011: Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitol. 58: 197-223. Go to original source... Go to PubMed...
  115. Scholz T., Kuchta R. 2017: A digest of bony fish tapeworms. Vie milieu - Life Environm. 67 (in press).
  116. Scholz T., Kuchta R., Williams C. 2012: Bothriocephalus acheilognathi. In: P.T.K. Woo and K. Buchmann (Eds.), Fish Parasites. Pathobiology and Protection. Chapter 18. CAB International, Wallingford, pp. 282-297.
  117. Scholz T., Oros M. 2017: Caryophyllidea van Beneden in Carus, 1863. In: J.N. Caira and K. Jensen (Eds.), Planetary Biodiversity Inventory (2008-2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, pp. 47-64.
  118. Scholz T., Oros M., Bazsalovicsová E., Brabec J., Waeschenbach A., Xi B.W., Aydoğdu A., Besprozvannykh V., Shimazu T., Králová-Hromadová I., Littlewood D.T.J. 2014: Molecular evidence of cryptic diversity in Paracaryophyllaeus (Cestoda: Caryophyllidea), parasites of loaches (Cobitidae) in Eurasia, including description of P. vladkae n. sp. Parasitol. Int. 63: 841-850. Go to original source... Go to PubMed...
  119. Scholz T., Oros M., Choudhury A., Brabec J., Waeschenbach A. 2015: New circumscription of freshwater fish parasites Monobothrium Diesing, 1863 and Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea) using morphological and molecular evidence. J. Parasitol. 101: 29-36. Go to original source... Go to PubMed...
  120. Schrank F.P. 1788: Verzeichniss der bisher hinlänglich bekannten Eingeweidewürmer, nebst einer Abhandlung über ihre Anverwandschaften. Johann Baptist Strobl, München, 116 pp.
  121. Sekutowicz S.T. 1934: Untersuchungen zur Entwicklung and Biologie von Caryophyllaeus laticeps (Pall.).] Mem. Acad. Pol. Sci. Lettres, Series B, Sci. Nat. 6: 11-26.
  122. Skrjabin K.I. 1913: Fischparasiten aus Turkestan, I. Hirudinea et Cestodaria. Arch. Naturgesch., Abt. A 79: 1-10.
  123. ©rámek A. 1901: Helminthen der an der zoologischen Station in Podiebrad (Böhmen) untersuchten Fische. Arch. Naturwissenschaft. Landesdurchforsch. Böhmen 11: 94-118.
  124. Stamatakis A. 2006: RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. Go to original source... Go to PubMed...
  125. Stiles C.W., Hassal A. 1912: Index-Catalogue of Medical and Veterinary Zoology. Publication of the U.S., Health Amid Marine-Hospital Service, Washington, 467 pp.
  126. Szidat L. 1937: Über einige neue Caryophyllaeiden aus ostpreussischen Fischen. Z. Parasitenkd. 9: 771-786. Go to original source...
  127. Szidat L. 1941: Über die Caryophyllaeiden-Gattung Khawia H. F. Hsü 1935 und eine neue Art dieser Gattung, Khawia baltica n. spec. Z. Parasitenkd. 12: 120-132. Go to original source...
  128. Timm T. 1972: On the reproduction of Euilyodrilus bedoti (Piquet, 1913) (Oligochaeta, Tubificidae). Eesti NSV Teaduste Akadeemia Toimetised Biologia 21: 235-241. (Cited from Milbrink 1975.)
  129. Vasilevskaya L.K. 1984: [Formation of the caryophyllid fauna of fish in the Pechenezhskii reservoir.] Vestn. Kharskovsk. Univ. 262: 82-83. (In Russian.)
  130. Waeschenbach A., Webster B.L., Littlewood D.T.J. 2012: Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol. Phylogenet. Evol. 63: 834-847. Go to original source... Go to PubMed...
  131. Wardle R.A., McLeod J.A. 1952: The Zoology of Tapeworms. University of Minnesota Press, Minneapolis, 780 pp.
  132. Werle E., Schneider C., Renner M., Volker M., Fiehn W. 1994: Convenient singlestep, one tube purification of PCR products for direct sequencing. Nucl. Acids Res. 22: 4354-4355. Go to original source... Go to PubMed...
  133. Woodland W.N.F. 1923: On some remarkable new forms of Caryophyllaeidae from Anglo-Egyptian Sudan, and a revision of the families of the Cestodaria. Q. J. Microsc. Sci. 67: 435-472
  134. Xi B.W., Barčák D., Oros M., Chen K., Xie J. 2016: The occurrence of the common European fish cestode Caryophyllaeus laticeps (Pallas, 1781) in the River Irtysh, China: a morphological characterization and molecular data. Acta Parasitol. 61: 493-499. Go to original source... Go to PubMed...
  135. Xi B.W., Oros M., Wang G.T., Scholz T., Xie J. 2013: Khawia abbottinae sp. n. (Cestoda: Caryophyllidea) from the Chinese false gudgeon Abbottina rivularis (Cyprinidae: Gobioninae) in China: morphological and molecular data. Folia Parasitol. 60: 141-148. Go to original source... Go to PubMed...
  136. Yamaguti S. 1959: Systema Helminthum, vol. II. The Cestodes of Vertebrates. Keigaku Publishing House, Tokyo, 860 pp.