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Systematic Parasitology

, Volume 94, Issue 9, pp 941–970 | Cite as

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

  • Scott C. CutmoreEmail author
  • Michael B. Bennett
  • Terrence L. Miller
  • Thomas H. Cribb
Article
Part of the following topical collections:
  1. Cestoda

Abstract

A survey of tapeworms of galeomorph sharks from Moreton Bay (Queensland, Australia) identified a complex of species of Paraorygmatobothrium Ruhnke, 1994 infecting 11 carcharhiniform and two orectolobiform species. Combined morphological and multi-locus molecular analyses (based on the 28S nuclear ribosomal RNA and partial mitochondrial NADH dehydrogenase subunit 1 genes) revealed the presence of 12 species of Paraorygmatobothrium; four species (Paraorygmatobothrium christopheri n. sp., P. harti n. sp., P. sinclairtaylori n. sp. and P. ullmanni n. sp.) are considered to be new to science and are formally described, four represent known species, and four lack sufficient morphological data to allow definitive identification. In contrast to previous records for the genus, four of the species found in this study exhibited low host specificity [P. orectolobi (Butler, 1987) Ruhnke, 2011, P. sinclairtaylori, P. ullmanni and Paraorygmatobothrium sp. 3], three stenoxenic species were each found in two closely-related sharks (P. orectolobi, P. ullmanni and Paraorygmatobothrium sp. 3) and one euryxenic species was found in five species from two shark families (P. sinclairtaylori). One species was found to exhibit mild morphologically plasticity (P. orectolobi), with size range being associated with different shark species. Conversely, collections of almost morphologically indistinguishable specimens from single shark species were found to represent multiple species of Paraorygmatobothrium. The findings of this study indicate that the description of species of this genus on the basis of morphological data alone is problematic and that the inclusion of multi-locus molecular data is essential for future work on Paraorygmatobothrium. Host specificity, morphology and phylogenetic relatedness of species of Paraorygmatobothrium are explored.

Notes

Acknowledgements

We thank Drs Stephen Taylor, Nathan Hart and Jeremy F.P. Ullmann and John Page, Dave Thompson, Tane Sinclair-Taylor and Joanna Stead, for their assistance in the collection of elasmobranch specimens. We thank Dr Susan Theiss for her assistance in the production of SEM images and Dr Tim Ruhnke for providing primers for nad1 sequencing. We also thank the Queensland Shark Control Program for access to the spiral valve of a Carcharias taurus, caught off Rainbow Beach, Queensland, Australia.

Funding

THC and SCC acknowledge the Australian Biological Resources Study (ABRS) for their ongoing support. This study was funded by the ABRS National Taxonomy Research Grant RF215-40.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed.

References

  1. Bernot, J. P., Caira, J. N., & Pickering, M. (2015). The dismantling of Calliobothrium (Cestoda: Tetraphyllidea) with erection of Symcallio n. gen. and description of two new species. Journal of Parasitology, 101, 167–181.CrossRefPubMedGoogle Scholar
  2. Bernot, J. P., Caira, J. N., & Pickering, M. (2016). Diversity, phylogenetic relationships and host associations of Calliobothrium and Symcallio (Cestoda: ‘Tetraphyllidea’) parasitising triakid sharks. Invertebrate Systematics, 30, 616–634.Google Scholar
  3. Butler, S. A. (1987). Taxonomy of some tetraphyllidean cestodes from elasmobranch fishes. Australian Journal of Zoology, 35, 343–371.CrossRefGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. Campbell, R. A., & Beveridge, I. (2002). The genus Acanthobothrium (Cestoda: Tetraphyllidea: Onchobothriidae) parasitic in Australian elasmobranch fishes. Invertebrate Systematics, 16, 237–344.CrossRefGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. Cielocha, J. J., Jensen, K., & Caira, J. N. (2014). Floriparicapitus, a new genus of lecanicephalidean tapeworm (Cestoda) from sawfishes (Pristidae) and guitarfishes (Rhinobatidae) in the Indo-West Pacific. Journal of Parasitology, 100, 485–499.CrossRefPubMedGoogle Scholar
  8. Cutmore, S. C., Bennett, M. B., & Cribb, T. H. (2009). Paraorygmatobothrium taylori n. sp. (Tetraphyllidea: Phyllobothriidae) from the Australian weasel shark Hemigaleus australiensis White, Last & Compagno (Carcharhiniformes: Hemigaleidae). Systematic Parasitology, 74, 49–58.CrossRefPubMedGoogle Scholar
  9. Cutmore, S. C., Bennett, M. B., & Cribb, T. H. (2010). A new tetraphyllidean genus and species, Caulopatera pagei n. g., n. sp. (Tetraphyllidea: Phyllobothriidae), from the grey carpetshark Chiloscyllium punctatum Müller & Henle (Orectolobiformes: Hemiscylliidae). Systematic Parasitology, 77, 13–21.CrossRefPubMedGoogle Scholar
  10. Cutmore, S. C., Theiss, S. M., Bennett, M. B., & Cribb, T. H. (2011). A new phyllobothriid genus and species from the snaggletooth shark, Hemipristis elongata (Carcharhiniformes: Hemigaleidae), from Moreton Bay, Australia. Folia Parasitologica, 58, 187–196.CrossRefPubMedGoogle Scholar
  11. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2011). ProtTest 3: Fast selection of best-fit models of protein evolution. Bioinformatics, 27, 1164–1165.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fyler, C. A. (2011). An extremely hyperapolytic Acanthobothrium species (Cestoda: Tetraphyllidea) from the Japanese wobbegong, Orectolobus japonicus (Elasmobranchii: Orectolobiformes) in Taiwan. Comparative Parasitology, 78, 4–14.CrossRefGoogle Scholar
  14. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.CrossRefPubMedGoogle Scholar
  15. Healy, C. J. (2003). A revision of Platybothrium Linton, 1890 (Tetraphyllidea: Onchobothriidae), with a phylogenetic analysis and comments on host-parasite associations. Systematic Parasitology, 56, 85–139.CrossRefPubMedGoogle Scholar
  16. Jensen, K., & Bullard, S. A. (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.CrossRefPubMedGoogle Scholar
  17. Johnson, J. W. (2010). Fishes of the Moreton Bay Marine Park and adjacent continental shelf waters, Queensland, Australia. Memoirs of the Queensland Museum, 54, 299–353.Google Scholar
  18. Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.CrossRefPubMedGoogle Scholar
  19. Last, P. R., & Stevens, J. D. (2009). Sharks and Rays of Australia (2nd ed.). Collingwood: CSIRO Publishing, 644 pp.Google Scholar
  20. Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution, 3, 221–229.CrossRefPubMedGoogle Scholar
  21. Littlewood, D. T. J., 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.CrossRefPubMedGoogle Scholar
  22. Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology, 27, 1289–1297.CrossRefPubMedGoogle Scholar
  23. 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. Biological Journal of the Linnean Society, 78, 155–171.CrossRefGoogle Scholar
  24. Maddison, W. P., & Maddison, D. R. (2015). Mesquite: A modular system for evolutionary analysis. Version 3.01. http://mesquiteproject.org.
  25. Malek, M., Caira, J. N., & 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.CrossRefPubMedGoogle Scholar
  26. Miller, M. A., Pfeiler, E., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp. 1–8.Google Scholar
  27. 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.CrossRefGoogle Scholar
  28. Palm, H. W., & Caira, J. N. (2008). Host specificity of adult versus larval cestodes of the elasmobranch tapeworm order Trypanorhyncha. International Journal for Parasitology, 38, 381–388.CrossRefPubMedGoogle Scholar
  29. Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., et al. (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371.CrossRefPubMedGoogle Scholar
  30. Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.CrossRefPubMedGoogle Scholar
  31. Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  32. Ruhnke, T. R. (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
  33. Ruhnke, T. R. (1996). Systematic resolution of Crossobothrium Linton, 1889, and taxonomic information on four species allocated to that genus. Journal of Parasitology, 82, 793–800.CrossRefPubMedGoogle Scholar
  34. Ruhnke, T. R. (2011). Tapeworms of elasmobranchs (Part III). A monograph on the Phyllobothriidae (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum, 25, i–xii, 1–208.Google Scholar
  35. Ruhnke, T. R., & Carpenter, S. D. (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.CrossRefPubMedGoogle Scholar
  36. Ruhnke, T. R., Healy, C. J., & Shapero, S. (2006). Two new species of Paraorygmatobothrium (Cestoda: Tetraphyllidea) from weasel sharks (Carcharhiniformes: Hemigaleidae) of Australia and Borneo. Journal of Parasitology, 92, 145–150.CrossRefPubMedGoogle Scholar
  37. Ruhnke, T. R., & Thompson, V. A. (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
  38. Ruhnke, T. R., & Workman, R. E. (2013). Two new species and a new phyllobothriid cestode genus from sharks of the genus Negaprion Whitley (Carcharhiniformes). Systematic Parasitology, 85, 37–48.CrossRefPubMedGoogle Scholar
  39. Sambrook, J., & Russell, D. W. (2001). Molecular cloning: A laboratory manual. Cold Spring Harbor, NY: Harbor Laboratory Press.Google Scholar
  40. Simpfendorfer, C. (1998). Diet of the Australian sharpnose shark, Rhizoprionodon taylori, from northern Queensland. Marine and Freshwater Research, 49, 757–761.CrossRefGoogle Scholar
  41. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology, 57, 758–771.CrossRefPubMedGoogle Scholar
  42. Taylor, S. M., & Bennett, M. B. (2013). Size, sex and seasonal patterns in the assemblage of Carcharhiniformes in a sub-tropical bay. Journal of Fish Biology, 82, 228–241.CrossRefPubMedGoogle Scholar
  43. Vardo-Zalik, A. M., & Campbell, R. A. (2011). Five new species of Acanthobothrium van Beneden, 1849 (Cestoda: Tetraphyllidea) in elasmobranchs from the northwest Atlantic and Gulf of Mexico with first records from smooth-hound sharks and guitarfish. Zootaxa, 2938, 41–64.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Scott C. Cutmore
    • 1
    Email author
  • Michael B. Bennett
    • 2
  • Terrence L. Miller
    • 3
  • Thomas H. Cribb
    • 1
  1. 1.The University of Queensland, School of Biological SciencesBrisbaneAustralia
  2. 2.The University of Queensland, School of Biomedical SciencesBrisbaneAustralia
  3. 3.Fish Health LaboratoryDepartment of FisheriesSouth PerthAustralia

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