Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-03-09
Page range: 30-50
Abstract views: 382
PDF downloaded: 45

Phylogenetic relationships, host associations, and three new species of a poorly known group of “tetraphyllidean” tapeworms from elasmobranchs

Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, Connecticut, 06269-3043, U.S.A
Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, Connecticut, 06269-3043, U.S.A.
Platyhelminthes biodiversity phylogeny 28S rDNA morphology taxonomy Australia New Zealand Cestoda


This paper aims to expand understanding of a poorly known group of cestodes that parasitize an intriguingly diverse suite of elasmobranchs. The group’s three currently described members (i.e., Pentaloculum macrocephalum, Pentaloculum hoi, and Zyxibothrium kamienae) parasitize an electric ray, a carpet shark, and a skate, respectively. Pentaloculum grahami n. sp. is described from a second genus of carpet shark, specifically Parascyllium collare, in Australia. Zyxibothrium duffyi n. sp. and Zyxibothrium healyae n. sp. are described from the deep-sea skates Brochiraja asperula and Brochiraja spinifera, respectively off New Zealand. The three new species share distinctive bothridia that bear a small number of large, circular, facial loculi and lateral bands of vitelline follicles that converge posterior to the ovary—features which are found in all other members of these genera. Zyxibothrium healyae n. sp. is unique in possessing three, rather than four or five, facial loculi. Zyxibothrium duffyi n. sp. possesses a combination of five facial loculi and vitelline follicles that stop short of the anterior margin of the proglottid. Pentaloculum grahami n. sp. is the largest member of the group with the greatest number of proglottids. Based on striking similarities in scolex morphology, Pentaloculum and Zyxibothrium have been hypothesized to belong to a distinct subgroup of “tetraphyllideans” provisionally designated as Clade 1. Based on sequence data for the D1–D3 region of the 28S rDNA gene generated for species of Zyxibothrium for the first time, we confirm the reciprocal monophyly of both genera as well as the monophyly of Clade 1 and its status as a distinct lineage among the “Tetraphyllidea”. This work also suggests that the presence of five facial loculi is homoplasious given this character state is found in members of both genera. The new species expand the host associations of Clade 1 to include additional skate and carpet shark genera. Moving forward we would expect to find additional members of this group parasitizing other species of parascyliid carpet sharks as well as other species of the rajid genus Malacoraja and the arhynchobatid genus Brochiraja. Here we have doubled the number of described species in the taxon referred to as Clade 1 while simultaneously expanding our understanding of the morphology and anatomy of its members. This additional information will help inform the ultimate revision of the ordinal classification of the cestodes to address the highly polyphyletic nature of the order “Tetraphyllidea” as it is currently configured.



  1. Abbott, L.M. & Caira, J.N. (2014) Morphology meets molecules: A new genus and two new species of diphyllidean cestodes from the yellowspotted skate, Leucoraja wallacei, from South Africa. Journal of Parasitology, 100, 323–330.
    Alexander, C.G. (1963) Tetraphyllidean and diphyllidean cestodes of New Zealand selachians. Transactions of the Royal Society of New Zealand, 3, 117–142.
    Baer, J.G. (1956) Parasitic helminths collected in west Greenland. Meddelelser om Gronland, 124, 52.
    Beveridge, I. & Campbell, R.A. (2007) Revision of the Grillotia erinaceus (van Beneden, 1858) species complex (Cestoda: Trypanorhyncha), with the description of G. brayi n. sp. Systematic Parasitology, 68, 1–31.
    Bueno, V.M. & Caira, J.N. (2017) Redescription and molecular assessment of relationships among three species of Echeneibothrium (Rhinebothriidea: Echeneibothriidae) parasitizing the yellownose skate, Dipturus chilensis, in Chile. Journal of Parasitology, 103, 268–284.
    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, 193, 1336–1363.
    Caira, J.N., Jensen, K. & Barbeau, E. (2022) Global Cestode Database. Available from: (accessed 28 October 2022)
    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.
    Caira, J.N., Jensen, K. & Ruhnke, T.R. (2017) “Tetraphyllidea” van Beneden, 1850 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. Lawrence, Kansas, pp. 371–400.
    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.
    Campbell, R.A. (1975) Two new species of Echeneibothrium (Cestoda: Tetraphyllidea) from skates in the Western North Atlantic. Journal of Parasitology, 61, 95–99.
    Campbell, R.A. (1977) New tetraphyllidean and trypanorhynch cestodes from deep-sea skates in the western north Atlantic. Proceedings of the Helminthological Society of Washington, 44, 191–197.
    Campbell, R.A. & Andrade, M. (1997) Echinobothrium raschii n. sp. (Cestoda: Diphyllidea) from Rhinoraja longi (Chondrich- thyes, Rajoidei) in the Bering Sea. Journal of Parasitology, 83, 115.
    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.
    Clopton, R.E. (2004) Standard nomenclature and metrics of plane shapes for use in gregarine taxonomy. Comparative Parasitology, 71, 130–140.
    Concha, F.J., Ebert, D. & Long, D.J. (2016) Notoraja martinezi sp. nov., a new species of deepwater skate and the first record of the genus Notoraja Ishiyama, 1958 (Rajiformes: Arhynchobatidae) from the eastern Pacific Ocean. Zootaxa, 4098, 179–190
    Ebert, D.A. & Leslie, R. (2019) Leucoraja elaineae sp. nov., a new rough skate (Rajiformes: Rajidae) from the Western Indian Ocean. Zootaxa, 4691, 225–234.
    Eudy, E., Caira, J.N. & Jensen, K. (2019) A new species of Pentaloculum (Cestoda: “Tetraphyllidea”) from the Taiwan Saddled carpetshark, Cirrhoscyllium formosanum (Orectolobiformes: Parascylliidae). Journal of Parasitology, 105, 303–312.
    Euzet, L. (1956) Une espèce nouvelle d’Echeneibothrium Van Beneden 1850. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 79, 39–41.
    Franzese, S. & Ivanov, V.A. (2020) Two new species of Acanthobothrium Blanchard, 1848 (Cestoda: Onchoproteocephalidea) from rajiform batoids off Argentina. Folia Parasitologica, 67, 016.
    Franzese, S., Mutti, L.D., Tropea, C. & Ivanov, V.A. (2022) Morphological study of members of the genus Echeneibothrium (Cestoda: Rhinebothriidea: Echeneibothriidae) from rajiform skates of the Argentine Sea and analysis of the phylogenetic relationships within the family Echeneibothriidae. Zoologischer Anzeiger, 299, 1–20.
    Hassan, S. (1982) Discobothrium aegyptiacus n. sp., a cestode from Raja circularis in the Mediterranean Sea, Egypt. Journal of the Egyptian Society of Parasitology, 12, 169–173.
    Hayden, B.P. & Campbell, R.A. (1981) Zyxibothrium (Tetraphyllidea: Phyllobothriidae), a new genus of cestodes from skates, with suggestions for diagnoses, classification, and revision of the Rhinebothriinae Euzet, 1953. Journal of Parasitology, 67, 262–267.
    Heller, A.F. (1949) Parasites of cod and other marine fish from the Baie de Chaleur region. Canadian Journal of Research, 27, 243–264.
    Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.
    Ivanov, V.A. (2006) Guidus n. gen. (Cestoda: Tetraphyllidea), with description of a new species and emendation of the generic diagnosis of Marsupiobothrium. Journal of Parasitology, 92, 832–840.
    Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589.
    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
    Keeling, C.P. & Burt, M.D.B. (1996) Echeneibothrium canadensis n. sp. (Tetraphyllidea: Phyllobothriidae) in the spiral intestine of the thorny skate (Raja radiata) from the Canadian Atlantic Ocean. Canadian Journal of Zoology, 74, 1590–1593.
    Keeney, D.B. & Campbell, R.A. (2001) Grillotia borealis sp. n. (Cestoda: Trypanorhyncha) from five species of Bathyraja (Rajiformes: Arhynchobatidae) in the North Pacific Ocean with comments on parasite enteric distribution. Folia Parasitologica, 48, 21–29.
    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.
    Littlewood, D.T., Curini-Galletti, M. & Herniou, E.A. (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.
    Löytynoja, A. (2014) Phylogeny-aware alignment with PRANK. In: Russell, D.J. (Ed.), Multiple Sequence Alignment Methods. Humana Press, Totowa, New Jersey, pp. 155–170.
    McVicar, A.H. (1976) Echinobothrium harfordi sp. nov. (Cestoda: Diphyllidae) from Raja naevus in the North Sea and English Channel. Journal of Helminthology, 50, 31–8.
    Menoret, A. & Ivanov, V.A. (2021) New species of Guidus Ivanov, 2006 (Cestoda: Phyllobothriidea) from Bathyraja magellanica (Philippi) from the Patagonian Continental Shelf of Argentina. Folia Parasitologica, 68, 011.
    Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., Straube, N. & Lakner, C. (2012) Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier, J.C., Musick, J.A. & Heithaus, M.R. (Eds.), Biology of Sharks and Their Relatives 2nd edition. CRC Press, Taylor & Francis Group, Boca Raton, Florida, pp. 31–56.
    Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
    Olsson, P. (1886) Entozoa, iakttagna hos Skandinaviska hafsfiskar. I. Platyelminthes. Lunds Universitatis Årsskrift Mathematik och Naturvetenskap, 3, 59pp.
    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.
    Randhawa, H.S., Saunders, G.W., Scott, M.E. & Burt, M.D.B. (2008) Redescription of Pseudanthobothrium hanseni Baer, 1956 and description of P. purtoni n. sp. (Cestoda: Tetraphyllidea) from different pairs of rajid skate hosts, with comments on the host-specificity of the genus in the northwest Atlantic. Systematic Parasitology, 70, 41–60.
    Rees, G. (1959) Ditrachybothridium macrocephalum gen. nov., sp. nov., a cestode from some elasmobranch fishes. Parasitology, 49, 191–209.
    Rocka, A. & Zdzitowiecki, K. (1998) Cestodes in fishes of the Weddell Sea. Acta Parasitologica Polonica, 43, 64–70.
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
    Ruhnke, T.R., Caira, J.N. & Cox, A. (2015) The cestode order Rhinebothriidea no longer family-less: A molecular phylogenetic investigation with erection of two new families and description of eight new species of Anthocephalum. Zootaxa, 3904, 51–81.
    Schmidt, G.D. (1986) Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, 675 pp.
    Sela, I., Ashkenazy, H., Katoh, K. & Pupko, T. (2015) GUIDANCE2: Accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research, 43, W7–W14.
    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.
    Van Der Spuy, L., Smit, N.J. & Schaeffner, B.C. (2022) Threatened, host-specific affiliates of a red-listed host: Three new species of Acanthobothrium van Beneden, 1849 (Cestoda: Onchoproteocephalidea) from the endangered white skate, Rostroraja alba (Lacépède). International Journal for Parasitology: Parasites and Wildlife, 17, 114–126.
    Weigmann, S., Séret, B. & Stehmann, M.F.W. (2021) Notoraja hesperindica sp. nov., a new colorful deep-sea softnose skate (Elasmobranchii, Rajiformes, Arhynchobatidae) and first generic record from the western Indian Ocean. Marine Biodiversity, 51, 35.
    White, W.T., Last, P.R. & Mana, R.R. (2017) A new species of velvet skate, Notoraja sereti n. sp. (Rajiformes: Arhynchobatidae) from Papua New Guinea. Zootaxa, 4244, 219–230.
    Wilcox, T.P., Zwickl, D.J., Heath, T.A. & Hillis, D.M. (2002) Phylogenetic relationships of the dwarf boas and a comparison of bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution, 25, 361–371.
    Williams, H.H. (1966) The ecology, functional morphology, and taxonomy of Echeneibothrium Beneden, 1849 (Cestoda: Tetraphyllidea), a revision of the genus and comments of Discobothrium Beneden, 1870, Pseudanthobothrium Baer, 1956 and Phormobothrium Alexander, 1963. Parasitology, 56, 227–285.
    Williams, H.H. (1968a) Acanthobothrium quadripartitum sp. nov. (Cestoda: Tetraphyllidea) from Raja naevus in the North Sea and English Channel. Parasitology, 58, 105–110.
    Williams, H.H. (1968b) Phyllobothrium piriei sp. nov. (Cestoda: Tetraphyllidea) from Raja naevus with a comment on its habitat and mode of attachment. Parasitology, 58, 929–937.
    Williams, H.H. (1969) The genus Acanthobothrium Van Beneden, 1849 (Cestoda: Tetraphyllidea). Nytt Magasin for Zoologi, 17, 1–56.
    Wojciechowska, A. (1990a) Onchobothrium antarcticum sp. n. (Tetraphyllidea) from Bathyraja eatonii (Günther, 1876) and a plerocercoid from Notothenioidea (South Shetlands, Antarctic). Acta Parasitologica Polonica, 35, 113–117.
    Wojciechowska, A. (1990b) Pseudanthobothrium shetlandicum sp. n. and P. notogeorgianum sp. n. (Tetraphyllidea) from rays in the regions of the South Shetlands and South Georgia (Antarctic). Acta Parasitologica Polonica, 35, 181–186.
    Wojciechowska, A. (1991a) New species of the genus Phyllobothrium (Cestoda, Tetraphyllidea) from Antarctic batoid fishes. Acta Parasitologica Polonica, 36, 63–68.
    Wojciechowska, A. (1991b) Some tetraphyllidean and diphyllidean cestodes from Antarctic batoid fishes. Acta Parasitologica Polonica, 36, 69–74.