Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2021-07-12

A revision of the Rhoptrobothriidae (Cestoda: “Tetraphyllidea”)

Department of Ecology & Evolutionary Biology and the Biodiversity Institute, University of Kansas, 1200 Sunnyside Ave., Lawrence, KS 66045, USA.
Department of Ecology & Evolutionary Biology and the Biodiversity Institute, University of Kansas, 1200 Sunnyside Ave., Lawrence, KS 66045, USA.
Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269-3043, USA.
new species Myzophyllobothrium nagasawai n. sp. Myzocephalus Rhoptrobothrium Rhoptrobothriidae eagle rays Platyhelminthes

Abstract

The Rhoptrobothriidae are one of the more enigmatic families of cestodes of elasmobranchs. Opinions on the taxonomic status of the family’s three original genera (i.e., Myzophyllobothrium, Rhoptrobothrium, and Myzocephalus) have varied over the 115 years since they were erected. Some authors have considered all three valid, others have considered Rhoptrobothrium to be a synonym of Myzopyllobothrium or a genus inquirendum, yet others have considered Myzocephalus to be a synonym of the phyllobothriid genus Thysanocephalum. All three genera were established for specimens collected from eagle rays off Sri Lanka. The erection of Mixophyllobothrium for two specimens from a cowtail stingray off India three decades ago added additional confusion to the situation, with some authors considering it valid and others a synonym of Myzocephalus. These disagreements stem largely from differences in interpretation of the complex morphology of the scolex of members of these genera. Furthermore, with the exception of Rhoptrobothrium comprising four species, each genus is monotypic. All but Rhoptrobothrium has not been considered in detail for nearly a century, largely because of a lack of available material. The taxonomic status of these genera is assessed here based on light and scanning electron microscopy, and molecular data generated from new material collected from eagle rays off Indonesian and Malaysian Borneo, Japan, Sri Lanka, and Viet Nam. Morphological work indicates that the genera differ largely only in the degree of folding of the four remi that extend from the cephalic peduncle. A molecular phylogeny based on sequence data for the D1–D3 region of the 28S rRNA gene, which include new data for eight specimens of four species, indicates that Myzophyllobothrium, Myzocephalus, and Rhoptrobothrium are not mutually monophyletic. The latter two genera and Mixophyllobothrium are considered synonyms of Myzophyllobothrium and five species are transferred to that genus. Myzophyllobothrium okamuri n. comb. is considered a species inquirendum. Myzophyllobothrium nagasawai n. sp. is described from Aetobatus narutobiei off Japan. Myzophyllobothrium narinari n. comb. is re-described based on newly collected cestodes from the type host and locality (i.e., Aetobatus ocellatus off Sri Lanka). Despite consisting of only a single genus, the family status of the group is retained in recognition of the unusual configuration of the scolex, which bears four biloculate bothridia and four remi extending from the cephalic peduncle. The ordinal placement of the family remains uncertain, but affinities with the Phyllobothriidea, rather than “Tetraphyllidea” are considered.

References

  1. Baer, J.G. & Euzet, L. (1962) Revision critique des cestodes tétraphyllides décrits par T. Southwell (1re partie). Bulletin de la Societe Neuchateloise des Sciences Naturelles, 85, 143–172.

  2. Beveridge, I. (1990) Taxonomic revision of Australian Eutetrarhynchidae Guiart (Cestoda: Trypanorhyncha). Invertebrate Taxonomy, 4, 785–845. https://doi.org/10.1071/IT9900785

  3. Beveridge, I. & Justine, J.L. (2007) Pseudolacistorhynchus nanus n. sp. (Cestoda: Trypanorhyncha) parasitic in the spiral valve of the zebra shark, Stegostoma fasciatum (Hermann, 1783). Transactions of the Royal Society of South Australia, 131, 175–181. https://doi.org/10.1080/03721426.2007.10887081

  4. Caira, J.N., Bueno, V. & Jensen, K. (2021) Emerging global novelty in phyllobothriidean tapeworms (Cestoda: Phyllobothriidea) from sharks and skates (Elasmobranchii). Zoological Journal of the Linnean Society, zlaa185.  https://doi.org/10.1093/zoolinnean/zlaa185

  5. Caira, J.N., Jensen, K. & Barbeau, E. (2020a) Global Cestode Database. Available from: http://www.elasmobranchs.tapewormdb.uconn.edu (accessed 10 January 2021)

  6. Caira, J.N., Jensen, K., Hayes, C. & Ruhnke, T.R. (2020c) Insights from new cestodes of the crocodile shark, Pseudocarcharias kamoharai (Lamniformes: Pseudocarchariidae), prompt expansion of Scyphyophyllidium and formal synonymization of seven phyllobothriidean genera—at last! Journal of Helminthology, 94, e132. https://doi.org/10.1017/S0022149X20000036

  7. Caira, J.N., Jensen, K. & Healy, C.J. (1999) On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology, 42, 77–151. https://doi.org/10.1023/a:1006192603349

  8. Caira, J.N., Jensen, K. & Healy, C.J. (2001) Interrelationships among Tetraphyllidean and Lecanicephalidean cestodes. In: Littlewood, D.T.J. & Bray, R.A. (Eds.), Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 135–158.

  9. Caira, J.N., Jensen, K., Pickering, M., Ruhnke, T.R. & Gallagher, K.A. (2020b) Intrigue surrounding the life-cycles of species of Clistobothrium (Cestoda: Phyllobothriidea) parasitising large pelagic sharks. International Journal for Parasitology, 50, 1043–1055. https://doi.org/10.1016/j.ijpara.2020.08.002

  10. Caira, J.N., Jensen, K. & Ruhnke, T.R. (2017) “Tetraphyllidea” van Beneden, 1849 relics. In: Caira, J.N. & Jensen, K. (Eds.), Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25. University of Kansas, Natural History Museum, Lawrence, Kansas, pp. 371–400.

  11. Caira, J.N., Jensen, K., Waeschenbach, A., Olson, P.D. & Littlewood, D.T.J. (2014) Orders out of chaos—molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. International Journal for Parasitology, 44, 55–73. https://doi.org/10.1016/j.ijpara.2013.10.004

  12. Campbell, R.A. & Beveridge, I. (2002) The genus Acanthobothrium (Cestoda: Tetraphyllidea: Onchobothriidae) parasitic in Australian elasmobranch fishes. Invertebrate Systematics, 16, 237–344. https://doi.org/10.1071/it01004

  13. Chervy, L. (2009) Unified terminology for cestode microtriches: A proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitologica, 56, 199–230. https://doi.org/10.14411/fp.2009.025

  14. Coleman, G.M., Beveridge, I. & Campbell, R.A. (2019) Caulobothrium pedunculatum sp. nov., a new species of cestode (Platyhelminthes) parasitic in Australian stingrays (Elasmobranchii: Batoidea). Transactions of the Royal Society of South Australia, 143, 167–174. https://doi.org/10.1080/03721426.2019.1624932

  15. Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. https://doi.org/10.1038/nmeth.2109

  16. Deshmukh, R.A. (1979) On three new species of Uncibilocularis Southwell, 1925 (Cestoda: Onchobothriidae) from marine fishes with a key to the species of the genus. Proceedings of the National Academy of Sciences, India, 49 (B), 227–236.

  17. Deshmukh, R.A. & Shinde, G.B. (1979) Three new species of Tetragonocephalum Shipley and Hornell, 1905 (Cestoda: Tetragonocephalidae) from marine fishes of west coast of India. Bioresearch, 3, 19–23.

  18. Euzet, L. (1994) Order Tetraphyllidea Carus, 1863. In: Khalil, L.F., Jones, A. & Bray, R.A. (Eds.), Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, pp. 149–194.

  19. Fernando, D., Bown, R.M.K., Tanna, A., Gobiraj, R., Ralicki, H., Jockusch, E.L., Ebert, D.A., Jensen, K. & Caira, J.N. (2019) New insights into the identities of the elasmobranch fauna of Sri Lanka. Zootaxa, 4585 (2), 201–238. https://doi.org/10.11646/zootaxa.4585.2.1

  20. Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. https://doi.org/10.1080/10635150390235520

  21. Hahn, C., Bachmann, L. & Chevreux, B. (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Research, 41, e129. https://doi.org/10.1093/nar/gkt371

  22. Haseli, M. (2013) Trypanorhynch cestodes from elasmobranchs from the Gulf of Oman, with the description of Prochristianella garshaspi n. sp. (Eutetrarhynchidae). Systematic Parasitology, 85, 271–279. https://doi.org/10.1007/s11230-013-9425-8

  23. Haseli, M. & Palm, H.W. (2015) Dollfusiella qeshmiensis n. sp (Cestoda: Trypanorhyncha) from the cowtail stingray Pastinachus sephen (Forsskål) in the Persian Gulf, with a key to the species of Dollfusiella Campbell & Beveridge, 1994. Systematic Parasitology, 92, 161–169. https://doi.org/10.1007/s11230-015-9592-x

  24. Hassan, S.H. (1983) Acanthobothrium manteri sp. n. a tetraphyllidean cestode (Oncobothriidae [sic]) from Dasyatis sephen. Journal of the Egyptian Society of Parasitology, 13, 75–80.

  25. Hornell, J. (1912) New cestodes from Indian fishes. Records of the Indian Museum, 7, 197–204.

  26. ICZN. (1999) International Code of Zoological Nomenclature, 4th edition. The International Trust for Zoological Nomenclature, London, 306 pp.

  27. Jensen, K. & Caira, J.N. (2006) The status of Rhoptrobothrium Shipley et Hornell, 1906 (Cestoda: Tetraphyllidea), with redescription of the type species, R. myliobatidis, and description of three new species from two species of Aetomylaeus (Myliobatiformes: Myliobatidae) from Malaysian Borneo. Folia Parasitologica, 53, 189–207. https://doi.org/10.14411/fp.2006.025

  28. Jensen, K. & Caira, J.N. (2008) A revision of Uncibilocularis Southwell, 1925 (Tetraphyllidea: Onchobothriidae) with the description of four new species. Comparative Parasitology, 75, 157–173. https://doi.org/10.1654/4347.1

  29. Joyeux, C. & Baer, J.G. (1961) Classe de Cestodes. Cestoidea Rudolphi. In: Baer, J.-G., de Beauchamp, P., Caullery, M., Euzet, L., Gontcharoff, M., Grass, P.-P. & Joyeux, C. (Eds.), Trait de Zoologie. Anatomie, systématique, biologie. Tome IV. Plathelminthes, Mésozoaires, Acanthocéphales, Némertiens. Masson et Cie, Paris, pp. 347–560.

  30. Khambata, F.S. & Bal, D.V. (1954) Studies on the cestodes of marine fishes from Bombay. Part I - On the genus Balanobothrium Hornell, 1912 (Cestoda), with a description of a new species. Journal of the Zoological Society of India, 6, 101–110.

  31. Kuchta, R. & Caira, J.N. (2010) Three new species of Echinobothrium (Cestoda: Diphyllidea) from Indo-Pacific stingrays of the genus Pastinachus (Rajiformes: Dasyatidae). Folia Parasitologica, 57, 185–196. https://doi.org/10.14411/fp.2010.025

  32. Last, P.R., White, W.T., de Carvalho, M.R., Séret, B., Stehmann, M.F.W. & Naylor, G.J.P. (2016) Rays of the World. Cornell University Press, Ithaca, New York, 790 pp.

  33. Linton, E. (1892) The anatomy of Thysanocephalum crispum, Linton, a parasite of the tiger shark. Report of the United States Commissioner of Fish and Fisheries for 1888, 1892, 543–556.

  34. Löytynoja, A. & Goldman, N. (2010) webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics, 11, 579. https://doi.org/10.1186/1471-2105-11-579

  35. Maleki, L., Malek, M. & Palm, H.W. (2013) Two new species of Acanthobothrium (Tetraphyllidea: Onchobothriidae) from Pastinachus cf. sephen (Myliobatiformes: Dasyatidae) from the Persian Gulf and Gulf of Oman. Folia Parasitologica, 60, 448–456. https://doi.org/10.14411/fp.2013.048

  36. Maleki, L., Malek, M. & Rastgoo, A. (2018) Acanthobothrium chabahariensis n. sp. (Cestoda: Onchoproteocephalidea) in the cowtail stingray Pastinachus cf. sephen (Myliobatiformes: Dasyatidae) from the Gulf of Oman, Iran. Journal of Genetic Resources, 4, 114–121. https://doi.org/10.22080/jgr.2019.15565.1120

  37. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T. & Last, P.R. (2012) A DNA sequence–based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bulletin of the American Museum of Natural History, 367, 1–262. https://doi.org/10.1206/754.1

  38. Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755. https://doi.org/10.1016/s0020-7519(03)00049-3

  39. 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. Molecular Phylogenetics and Evolution, 48, 369–371. https://doi.org/10.1016/j.ympev.2008.03.024

  40. Reyda, F., Healy, C., Haslach, A., Ruhnke, T., Aprill, T., Bergman, M., Daigler, A., Dedrick, E., Delgado, I., Forti, K., Herzog, K., Russell, R. & Willsey, D. (2016) A new genus of rhinebothriidean cestodes from batoid elasmobranchs, with the description of five new species and two new combinations. Folia Parasitologica, 63, 038. https://doi.org/10.14411/fp.2016.038

  41. Roohi Aminjan, A. & Malek, M. (2017) Two new species of Tetragonocephalum (Cestoda: Lecanicephalidea) from Pastinachus sephen (Myliobatiformes: Dasyatidae) from the Gulf of Oman. Folia Parasitologica, 64, 014. https://doi.org/10.14411/fp.2017.014

  42. Ruhnke, T.R., Caira, J.N. & Pickering, M. (2017) Phyllobothriidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. In: Caira, J.N. & Jensen, K. (Eds.), Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25. University of Kansas, Natural History Museum, Lawrence, Kansas, pp. 305–326.

  43. Schaeffner, B.C. & Beveridge, I. (2012) Description of a new trypanorhynch species (Cestoda) from Indonesian Borneo, with the suppression of Oncomegoides and the erection of a new genus Hispidorhynchus. Journal of Parasitology, 98, 408–414. https://doi.org/10.1645/GE-2859.1

  44. Schaeffner, B.C. & Beveridge, I. (2013) Dollfusiella Campbell & Beveridge, 1994 (Trypanorhyncha: Eutetrarhynchidae) from elasmobranchs off Borneo, including descriptions of five new species. Systematic Parasitology, 86, 1–31. https://doi.org/10.1007/s11230-013-9435-6

  45. Schmidt, G.D. (1986) CRC Handbook of Tapeworm Identification. CRC Press Inc., Boca Raton, Florida, 675 pp.

  46. Shinde, G.B. & Chincholikar, L.N. (1980) Mixophyllobothrium okamuri gen. nov. sp. nov. (Cestoda: Tetraphyllida) from Trygon sephen at Ratnagiri, India. Rivista di Parassitologia, 41, 413–417.

  47. Shinde, G.B. & Deshmukh, R.A. (1979) On a new species of Flapocephalus Deshmukh R. A., 1977 (Cestoda: Lecanicephalidae Braun, 1900) from a marine fish at Veraval, west coast of India. Rivista di Parassitologia, 40, 295–298.

  48. Shipley, A.E. & Hornell, J. (1906) Report on the cestode and nematode parasites from the marine fishes of Ceylon. Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar (Herdman), Part V, 43–96.

  49. Southwell, T. (1925) A monograph on the Tetraphyllidea with notes on related cestodes. Memoirs of the Liverpool School of Tropical Medicine, New Series, 2, 1–368.

  50. Southwell, T. (1929) A monograph on cestodes of the order Trypanorhyncha from Ceylon and India. Part I. Ceylon Journal of Science, Section B, Zoology and Geology, 15, 169–312.

  51. Tkach, V.V., Littlewood, D.T.J., Olson, P.D., Kinsella, J.M. & Swiderski, Z. (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology, 56, 1–15. https://doi.org/10.1023/A:1025546001611

  52. Van der Auwera, G., Chapelle, S. & De Wachter, R. (1994) Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Letters, 338, 133–136. https://doi.org/10.1016/0014-5793(94)80350-1

  53. Verma, S.C. (1928) Some cestodes from Indian fishes, including four new species of Tetraphyllidea and revised keys to the genera Acanthobothrium and Gangesia. Allahabad University Studies, 4, 119–176.

  54. Wardle, R.A. & McLeod, J.A. (1952) The Zoology of Tapeworms. University of Minnesota Press, Minneapolis, Minnesota, 780 pp.

  55. Yamaguti, S. (1954) Parasitic worms mainly from Celebes. Part 6. Cestodes of fishes. Acta Medicinae Okayama, 8, 353–374.

  56. Yamaguti, S. (1959) Systema Helminthum. Volume II. The Cestodes of Vertebrates. Interscience Publishers, Inc., New York, New York, 860 pp.

  57. Zschoche, M., Caira, J.N. & Fyler, C.A. (2011) A new species of Acanthobothrium van Beneden, 1850 (Tetraphyllidea: Onchobothriidae) from Pastinachus atrus (Macleay) (Batoidea: Dasyatidae) in Australian waters, with a reassessment of the host associations of Acanthobothrium spp. parasitising Pastinachus spp. Systematic Parasitology, 78, 109–116. https://doi.org/10.1007/s11230-010-9279-2