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Insights from new cestodes of the crocodile shark, Pseudocarcharias kamoharai (Lamniformes: Pseudocarchariidae), prompt expansion of Scyphyophyllidum and formal synonymization of seven phyllobothriidean genera – at last!

Published online by Cambridge University Press:  02 March 2020

J.N. Caira Open the ORCID record for J.N. Caira [Opens in a new window] ,
K. Jensen Open the ORCID record for K. Jensen [Opens in a new window] ,
C. Hayes  and
T.R. Ruhnke
J.N. Caira*
Affiliation:
Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N Eagleville Road, Unit 3043, Storrs, Connecticut06269-3043, USA
K. Jensen
Affiliation:
Department of Ecology & Evolutionary Biology, Biodiversity Institute, University of Kansas, 1200 Sunnyside Avenue, Lawrence, Kansas66045, USA
C. Hayes
Affiliation:
Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N Eagleville Road, Unit 3043, Storrs, Connecticut06269-3043, USA
T.R. Ruhnke
Affiliation:
Department of Biology, West Virginia State University, Institute, West Virginia25112-1000, USA
*
Author for correspondence: J.N. Caira, E-mail: janine.caira@uconn.edu
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Abstract

Three new cestode species are described from the crocodile shark (Pseudocarcharias kamoharai) in Ecuador. All three were examined with light and scanning electron microscopy. The unique combination of morphological features in one of the new species prompted formal investigation of the non-monophyly of Paraorygmatobothrium relative to the morphologically similar genera Doliobothrium, Guidus, Marsupiobothrium, Nandocestus, Orectolobicestus, Ruhnkecestus and Scyphophyllidium. Sequence data generated for part of the 28S rDNA gene were subjected to maximum likelihood (ML) analysis. The resulting tree led to the synonymization of six of these seven genera with Scyphophyllidium, and transfer of their species to the latter genus. With the new species, the number of described members of Scyphophyllidium is now 45. The diagnosis of Scyphophyllidium is revised to accommodate these species. In addition, to expedite future descriptions, eight categories of Scyphophyllidium species are circumscribed, based largely on bothridial features. Scyphophyllidium timvickiorum n. sp. is a category 1 species. Beyond being the smallest category 1 species, it bears, rather than lacks, apical suckers and lacks, rather than bears, strobilar scutes. The two other new species are members of Clistobothrium. Clistobothrium amyae n. sp. differs from its congeners in bothridial shape, elongate cephalic peduncle and tiny size. Clistobothrium gabywalterorum n. sp. differs from the two of its congeners that also possess foliose bothridia in overall size and testis number. Despite their substantial morphological differences, the ML tree indicates they are sister taxa. Both are unique among their congeners in possessing cephalic peduncle spinitriches. The diagnosis of Clistobothrium is revised accordingly.

Keywords

Phyllobothriideanew speciesphylogenyelasmobranchcestodesynonymies

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Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e132
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Beer, A, Ingram, T and Randhawa, HS (2019) Role of ecology and phylogeny in determining tapeworm assemblages in skates (Rajiformes). Journal of Helminthology 93, 738–751.CrossRefGoogle Scholar
Beveridge, I and Campbell, RA (1988) Cetorhinicola n. g., Shirleyrhynchus n. g. and Stragulorhynchus n. g., three new genera of trypanorhynch cestodes from elasmobranchs in Australian waters. Systematic Parasitology 12, 47–60.CrossRefGoogle Scholar
Brooks, DR, Marques, F, Perroni, C and Sidagis, C (1999) Scyphophyllidium uruguayense n. sp. (Eucestoda: Tetraphyllidea) in Mustelus mento (Cope, 1877) (Chondrichthyes: Carcharhiniformes: Triakidae) from La Paloma, Uruguay. Journal of Parasitology 85, 490–494.CrossRefGoogle Scholar
Bueno, VM and Caira, JN (2017) Redescription and molecular assessment of relationships among three species of Echeneibothrium (Rhinebothriides: Echeneibothriidae) parasitizing the yellownose skate, Dipturus chilensis, in Chile. Journal of Parasitology 103, 268–284.CrossRefGoogle Scholar
Butler, SA (1987) Taxonomy of some tetraphyllidean cestodes from elasmobranch fishes. Australian Journal of Zoology 35, 343–371.CrossRefGoogle Scholar
Caira, JN and Durkin, SM (2006) A new genus and species of tetraphyllidean cestode from the spadenose shark, Scoliodon laticaudus, in Malaysian Borneo. Comparative Parasitology 73, 42–48.CrossRefGoogle Scholar
Caira, JN and Runkle, LS (1993) Two new tapeworms from the goblin shark Mitsukurina owstoni off Australia. Systematic Parasitology 26, 81–90.CrossRefGoogle Scholar
Caira, JN, Jensen, K, Yamane, Y, Isobe, A and Nagasawa, K (1997) On the tapeworms of Megachasma pelagios: description of a new genus and species of lecanicephalidean and additional information on the trypanorhynch Mixodigma leptaleum. pp. 181–191in Yano, K, Morrissey, JF, Yabumoto, Y and Nakaya, K (Eds) Biology of the megamouth shark. Kanagawa, Japan, Tokai University Press.Google Scholar
Caira, JN, Jensen, K and Healy, CJ (1999) On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology 42, 77–151.CrossRefGoogle ScholarPubMed
Caira, JN, Jensen, K and Healy, CJ (2001) Interrelationships among tetraphyllidean and lecanicephalidean cestodes. pp. 135–158in Littlewood, DTJ and Bray, RA (Eds) Interrelationships of the platyhelminthes. London, UK, Taylor & Francis.Google Scholar
Caira, JN, Malek, M and Ruhnke, T (2011) A new genus of Phyllobothriidae (Cestoda: Tetraphyllidea) in carcharhiniform sharks from Iran and Australia. Journal of Helminthology 85, 40–50.CrossRefGoogle ScholarPubMed
Caira, JN, Jensen, K, Waeschenbach, A, Olson, PD and Littlewood, DTJ (2014a) Orders out of chaos—molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. International Journal for Parasitology 44, 55–73.CrossRefGoogle Scholar
Caira, JN, Jensen, K, Waeschenbach, A and Littlewood, DTJ (2014b) An enigmatic new tapeworm, Litobothrium aenigmaticum, sp. nov. (Platyhelminthes: Cestoda: Litobothriidea), from the pelagic thresher shark with comments on development of known Litobothrium species. Invertebrate Systematics 28, 231–243.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Compagno, LJV (1984) FAO Species Catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 1. Hexanchiformes to Lamniformes. FAO Fisheries Synopsis 125, 1–249.Google Scholar
Compagno, LJV and Niem, VH (1998) Hemiscylliidae. Longtail carpetsharks. pp. 1249–1259in Carpenter, KE and Niem, VH (Eds) FAO identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Rome, FAO.Google Scholar
Cutmore, SC, Bennett, MB and Cribb, TH (2009) Paraorygmatobothrium taylori n. sp. (Tetraphyllidea: Phyllobothriidae) from the Australian weasel shark Hemigaleus australiensis White, Last & Compagno (Carcharhiniformes: Hemigaleidae). Systematic Parasitology 74, 49–58.CrossRefGoogle Scholar
Cutmore, SC, Theiss, SM, Bennett, MB and Cribb, TH (2011) Hemipristicola gunterae gen. n., sp. n. (Cestoda: Tetraphyllidea: Phyllobothriidae) from the snaggletooth shark, Hemipristis elongata (Carcharhiniformes: Hemigaleidae), from Moreton Bay, Australia. Folia Parasitologica 58, 187–196.CrossRefGoogle Scholar
Cutmore, SC, Bennett, MB, Miller, TL and Cribb, TH (2017) Patterns of specificity and diversity in species of Paraorygmatobothrium Ruhnke, 1994 (Cestoda: Phyllobothriidae) in Moreton Bay, Queensland, Australia, with the description of four new species. Systematic Parasitology 94, 941–970.CrossRefGoogle ScholarPubMed
Dailey, MD (1969) Litobothrium alopias and L. coniformis, two new cestodes representing a new order from elasmobranch fishes. Proceedings of the Helminthological Society of Washington 36, 218–224.Google Scholar
Dailey, MD (1971) Litobothrium gracile sp. n. (Eucestoda: Litobothridea) from the Sand Shark (Odontaspis ferox). Journal of Parasitology 57, 94–96.CrossRefGoogle Scholar
Dailey, MD and Vogelbein, W (1990) Clistobothrium carcharodoni gen. et sp. n. (Cestoda, Tetraphyllidea) from the spiral valve of the great white shark (Carcharodon carcharias). Journal of the Helminthological Society of Washington 57, 108–112.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
de Carvalho, MR, Lovejoy, N and Rosa, RS (2003) Potamotrygonidae (River stingrays). pp. 22–28in Reis, RE, Kullander, SO and Ferraris, CJ Jr. (Eds) Checklist of the freshwater fishes of South and Central America. Porto Alegre, Brazil, EDIPUCRS.Google Scholar
Euzet, L (1959) Recherches sur les cestodes tétraphyllides des sélaciens des cotes de France. Université de Montpellier, Montpellier, France, p. 263.Google Scholar
Euzet, L (1994) Order Tetraphyllidea Carus, 1863. pp. 149–194in Khalil, LF, Jones, A and Bray, RA (Eds) Keys to the cestode parasites of vertebrates. Wallingford, UK, CAB International.Google Scholar
Ghoshroy, S and Caira, JN (2001) Four new species of Acanthobothrium (Cestoda: Tetraphyllidea) from the whiptail stingray Dasyatis brevis in the Gulf of California, Mexico. Journal of Parasitology 87, 354–372.CrossRefGoogle ScholarPubMed
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Ivanov, VA (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.CrossRefGoogle Scholar
Jensen, K and Bullard, SA (2010) Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. International Journal for Parasitology 40, 889–910.CrossRefGoogle ScholarPubMed
Kurochkin, VB and Slankis, AJ (1973) New representative and the composition of the order Litobothridea Dailey, 1969 (Eucestodes). (in Russian). Parasitologia 7, 503–507.Google Scholar
Last, PR and Stevens, D (2009) Sharks and Rays of Australia, 2nd ed.Collingwood, Australia, CSIRO Publ., 644 pp.Google Scholar
Linton, E (1889) Notes on Entozoa of marine fishes of New England, with descriptions of several new species. Annual Report of the Commissioner of Fish and Fisheries (1886) 14, 453–511.Google Scholar
Linton, E (1897) Notes on cestode parasites of fishes. Proceedings of the United States National Museum 20, 423–456.CrossRefGoogle Scholar
Linton, E (1922) A new cestode from the maneater and mackerel sharks. Proceedings of the United States National Museum 61, 1–16.CrossRefGoogle Scholar
Littlewood, DTJ, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466.CrossRefGoogle ScholarPubMed
Löytynoja, A and Goldman, N (2010) webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics, 11, 579.CrossRefGoogle ScholarPubMed
Malek, M, Caira, JN and Haseli, M (2010) Two new species of Paraorygmatobothrium Ruhnke, 1994 (Cestoda: Tetraphyllidea) from the carcharhinid shark Carcharhinus cf. dussumieri (Müller & Henle) in the Persian Gulf. Systematic Parasitology 76, 59–68.CrossRefGoogle Scholar
Marques, FPL, Brooks, DR and Lasso, CA (2001) Anindobothrium n. gen. (Eucestoda: Tetraphyllidea) inhabiting marine and freshwater potamotrygonid stingrays. Journal of Parasitology 87, 666–672.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8 in Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, 14 November 2010.CrossRefGoogle Scholar
Olson, PD and Caira, JN (2001) Two new species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from thresher sharks in the Gulf of California, Mexico, with redescriptions of two species in the genus. Systematic Parasitology 48, 159–177.CrossRefGoogle ScholarPubMed
Palm, HW (2004) The Trypanorhyncha Diesing, 1863. i–x, 710 pp. Bogor, Indonesia, PKSPL-IPB Press.Google Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Randhawa, HS (2011) Insights using a molecular approach into the life cycle of a tapeworm infecting great white sharks. Journal of Parasitology 97, 275–280.CrossRefGoogle ScholarPubMed
Randhawa, HS and Brickle, P (2011) Larval parasite gene sequence data reveal cryptic trophic links in life cycles of porbeagle shark tapeworms. Marine Ecology Progress Series 431, 215–222.CrossRefGoogle Scholar
Reyda, FB (2008) Intestinal helminths of freshwater stingrays in southeastern Peru, and a new genus and two new species of cestode. Journal of Parasitology 94, 684–699.CrossRefGoogle Scholar
Rocka, A and Zdzitowiecki, K (1998) Cestodes in fishes of the Weddell Sea. Acta Parasitologica 43, 64–70.Google Scholar
Ruhnke, TR (1993) A new species of Clistobothrium (Cestoda: Tetraphyllidea), with an evaluation of the systematic status of the genus. Journal of Parasitology 79, 37–43.CrossRefGoogle Scholar
Ruhnke, TR (1994) Paraorygmatobothrium barberi n. g., n. sp. (Cestoda: Tetraphyllidea), with amended descriptions of two species transferred to the genus. Systematic Parasitology 28, 65–79.CrossRefGoogle Scholar
Ruhnke, TR (1996) Systematic resolution of Crossobothrium Linton, 1889, and taxonomic information on four species allocated to that genus. Journal of Parasitology 82, 793–800.CrossRefGoogle ScholarPubMed
Ruhnke, TR (2011) A monograph on the Phyllobothriidae (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum, 25, i–xii, 1–208.Google Scholar
Ruhnke, TR and Carpenter, SD (2008) Two new species of Paraorygmatobothrium Ruhnke, 1994 (Tetraphyllidea: Phyllobothriidae) from the smooth-hound Mustelus mustelus (L.) and the gummy shark M. antarcticus Günther (Carcharhiniformes: Triakidae). Systematic Parasitology 71, 213–222.CrossRefGoogle Scholar
Ruhnke, TR and Thompson, VA (2006) Two new species of Paraorygmatobothrium (Tetraphyllidea: Phyllobothriidae) from the lemon sharks Negaprion brevirostris and Negaprion acutidens (Carcharhiniformes: Carcharhinidae). Comparative Parasitology 73, 35–41.CrossRefGoogle Scholar
Ruhnke, TR and Workman, RE (2013) Two new species and a new phyllobothriid cestode genus from sharks of the genus Negaprion Whitley (Carcharhiniformes). Systematic Parasitology 85, 37–48.CrossRefGoogle Scholar
Ruhnke, TR, Caira, JN and Carpenter, SD (2006a) Orectolobicestus n. g. (Cestoda: Tetraphyllidea), with the description of five new species and the transfer of Phyllobothrium chiloscyllii to the new genus. Systematic Parasitology 65, 215–233.CrossRefGoogle Scholar
Ruhnke, TR, Healy, CJ and Shapero, S (2006b) Two new species of Paraorygmatobothrium (Cestoda: Tetraphyllidea) from weasel sharks (Carcharhiniformes: Hemigaleidae) of Australia and Borneo. Journal of Parasitology 92, 145–150.CrossRefGoogle Scholar
Ruhnke, TR, Caira, JN and Pickering, M (2017) Phyllobothriidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. pp. 305–326in Caira, JN and Jensen, K (Eds) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Lawrence, Kansas, USA,University of Kansas, Natural History Museum, Special Publication no. 25.Google Scholar
Ruhnke, TR, Daniel, V and Jensen, K (2020) Four new species of Paraorygmatobothrium from sharks of the Gulf of Mexico and the Atlantic Ocean, with comments on their host specificity. Journal of Parasitology 106, 133–156.CrossRefGoogle ScholarPubMed
Southwell, T (1912) A description of ten new species of cestode parasites from marine fishes of Ceylon, with notes on other cestodes from the same region. Ceylon Marine Biological Report 1, 259–278.Google Scholar
Subhapradha, CK (1955) Cestode parasites of fishes of Madras Coast. Indian Journal of Helminthology 7, 41–132.Google Scholar
Sukumaran, J and Holder, MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571.CrossRefGoogle ScholarPubMed
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.CrossRefGoogle Scholar
van Beneden, PJ (1850) Recherches sur la faune littorale de Belgique. Les vers cestoides, considérés sous le rapport physiologique, embryogénique et zooclassique. Mémoires de l'Academie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique 25 (Suppl. 201–204), 1–199.Google Scholar
van Beneden, PJ (1858) Mémoire sur les vers intestinaux. Supplément aux Comptes rendus des séances de l'Académie des Sciences, tome II. Paris, France, J.B. Baillière et Fils, 376 pp.Google Scholar
Watson, DE and Thorson, TB (1976) Helminths from elasmobranchs in Central American fresh waters. pp. 629–640in Thorson, TB (Ed) Investigations of the ichthyofauna of Nicaraguan Lakes. Lincoln, Nebraska, USA, University of Nebraska Press.Google Scholar
Wojciechowska, A (1991) Some tetraphyllidean and diphyllidean cestodes from Antarctic batoid fishes. Acta Parasitologica Polonica 36, 69–74.Google Scholar
Woodland, WNF (1927) A revised classification of the tetraphyllidean Cestoda, with descriptions of some Phyllobothriidae from Plymouth. Proceedings of the Zoological Society of London 95, 519–548.Google Scholar
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Zoology 6, 1–112.Google Scholar
Yamaguti, S (1935) Studies on the helminth fauna of Japan. Part 6. Cestodes of birds, I. Japanese Journal of Zoology 6, 183–232.Google Scholar
Yamaguti, S (1952) Studies on the helminth fauna of Japan. Part 49. Cestodes of fishes, II. Acta Medicinae Okayama 8, 1–76.Google Scholar
Zwickl, DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Vol. PhD Dissertation, The University of Texas at Austin, Austin, TX, p. 115.Google Scholar