Acta Parasitologica

, Volume 62, Issue 3, pp 502–512 | Cite as

Molecular phylogeny of the Haplosplanchnata Olson, Cribb, Tkach, Bray and Littlewood, 2003, with a description of Schikhobalotrema huffmani n. sp.

  • Daniel C. HustonEmail author
  • Scott C. Cutmore
  • Thomas H. Cribb


We describe Schikhobalotrema huffmani n. sp. from Tylosurus crocodilus (Péron and Leseur) (Belonidae) collected off Lizard Island, Great Barrier Reef, Queensland, Australia and Tylosurus gavialoides (Castelnau) collected from Moreton Bay, Queensland. Schikhobalotrema huffmani n. sp., along with Schikhobalotrema ablennis (Abdul-Salam and Khalil, 1987) Madhavi, 2005, Schikhobalotrema acutum (Linton, 1910) Skrjabin and Guschanskaja, 1955 and Schikhobalotrema adacutum (Manter, 1937) Skrjabin and Guschanskaja, 1955 are distinguished from all other species of Schikhobalotrema Skrjabin and Guschanskaja, 1955 in having ventral suckers which bear lateral lobes and have longitudinal apertures. Schikhobalotrema huffmani n. sp. differs from S. ablennis in having an obvious post-vitelline region and a longer forebody. From S. acutum, S. huffmani n. sp. differs in having a prostatic bulb smaller than the pharynx and more anterior testis. From S. adacutum, S. huffmani n. sp. differs in having more prominent ventral sucker lobes, a conspicuous prostatic bulb and a longer forebody. We also report the first Australian record of Haplosplanchnus pachysomus (Eysenhardt, 1829) Looss, 1902, from Mugil cephalus Linnaeus (Mugilidae) collected in Moreton Bay. Molecular sequence data (ITS2, 18S and 28S rDNA) were generated for Schikhobalotrema huffmani n. sp., H. pachysomus and archived specimens of Hymenocotta mulli Manter, 1961. The new 18S and 28S molecular data were combined with published data of five other haplosplanchnid taxa to expand the phylogeny for the Haplosplanchnata. Bayesian inference and Maximum Likelihood analyses recovered identical tree topology and demonstrated the Haplosplanchnata as a well-supported monophyletic group. However, relationships at and below the subfamily level remain poorly resolved.


Haplosplanchnoidea Haplosplanchnidae Haplosplanchnus Hymenocotta Lizard Island Queensland 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abdul-Salam J., Khalil L.F. 1987. Two digeneans from the needlefish Ablennes hians in Kuwait and the description of a new genus and species, Neohaplosplanchnus ablennis (Haplosplanchnidae). Systematic Parasitology, 10, 149–158CrossRefGoogle Scholar
  2. Ankenbrand M.J., Keller A., Wolf M., Schultz J., Förster F. 2015. ITS2 database V: Twice as much. Molecular Biology and Evolution, 32, 3030–3032CrossRefGoogle Scholar
  3. Besprozvannykh V.V., Atopkin D.M., Ngo H.D., Ermolenko A.V, Ha N.V., Tang N.V., Beloded A.Yu. 2016. Morphometric and molecular analyses of two digenean species from the mullet: Haplosplanchnus pachysomus (Eysenhardt, 1892) from Vietnam and Provitellotrema crenimugilis Pan, 1984 from the Russian southern Far East. Journal of Helminthology, 90, 238–234CrossRefGoogle Scholar
  4. Blasco-Costa I., Cutmore S.C., Miller T.L., Nolan M.J. 2016. Molecular approaches to trematode systematics:‘best practice’ and implications for future study. Systematic Parasitology, 93, 295–306CrossRefGoogle Scholar
  5. Blasco-Costa I. 2009. Taxonomy of the Haploporinae Nicoll, 1914 and Bunocotylinae Dollfus, 1950 (Digenea) from Mediterranean mullets (Teleostei): morphological and molecular approaches. PhD thesis, Department of Zoology, Universidad de Valencia, Valencia SpainGoogle Scholar
  6. Bray R.A., Cribb T.H. 2006. Overstreetia olsoni n. sp.(Digenea: Zoogonidae) from the Capricorn silverside Atherinomorus capricornensis (Woodland)(Atherinidae) off Heron Island, southern Great Barrier Reef. Systematic Parasitology, 63, 41–43CrossRefGoogle Scholar
  7. Caballero-Rodríguez G. 1990. Trematodos de peces marinos del Golfo de México y del Mar Caribe II. Familias Haplosplanchnidae y Opecoelidae. Anales del Instituto de Ciencias del Mar y Limología, Universidad Nacional Autónoma de México, 17, 191–203. (In Spanish)Google Scholar
  8. Caballero C., Bavo-Hollis M., Grocott, R.G. 1953. Helmintos de la República de Panamá. VII. Descripción de algunos tremátodos de peces marinos. Anales del Instituto de Biologia, 24, 97–136. (In Spanish)Google Scholar
  9. Cribb T.H., Adlard R.D., Bray R.A. 1998. A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology, 28, 1791–1795CrossRefGoogle Scholar
  10. Cribb T.H., Bray R.A. 2010. Gut wash, body soak, blender and heatfixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology, 76, 1–7CrossRefGoogle Scholar
  11. Cribb T.H., Bray R.A., Barker S.C. 1994. Bivesiculidae and Haplosplanchnidae (Digenea) from fishes of the southern Great Barrier Reef, Australia. Systematic Parasitology, 28, 81–97CrossRefGoogle Scholar
  12. Cribb T.H., Bray R.A., Diaz P.E., Huston D.C., Kudlai O., Martin S.B., et al. 2016. Trematodes of fishes of the Indo–west Pacific: told and untold richness. Systematic Parasitology, 93, 237–247CrossRefGoogle Scholar
  13. Cribb T.H., Bray R.A., Littlewood D.T.J., Pichelin S.P., Herniou E.A. 2001. The Digenea. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. London, Taylor and Francis, 168–185Google Scholar
  14. Cutmore S.C., Diggles B.K., Cribb T.H. 2016. Transversotrema Witenberg, 1944 (Trematoda: Transversotrematidae) from inshore fishes of Australia: description of a new species and significant range extensions for three congeners. Systematic Parasitology, 93, 639–652CrossRefGoogle Scholar
  15. Cutmore S.C., Miller T.L., Curran S.S., Bennett M.B., Cribb T.H. 2013. Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitology Research, 112, 3063–3074CrossRefGoogle Scholar
  16. Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797CrossRefGoogle Scholar
  17. Elwood H.J., Olsen G.J., Sogin M.L. 1985. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution, 2, 399–410PubMedGoogle Scholar
  18. Eysenhardt H. W. 1829. Einiges über eingeweide-würmer. Verhandlungen der Gesellschaft Naturforschender Freunde zu Berlin, 1, 144–152. (In German)Google Scholar
  19. Gibson D. 2013. Schikhobalotrema Skrjabin and Guschanskaja, 1955. Accessed through: World Register of Marine Species at on 2016-11-28Google Scholar
  20. Huston D.C., Cutmore S.C., Cribb T.H. 2016. The life-cycle of Gorgocephalus yaaji Bray and Cribb, 2005 (Digenea: Gorgocephalidae) with a review of the first intermediate hosts for the superfamily Lepocreadioidea Odhner, 1905. Systematic Parasitology, 93, 653–665CrossRefGoogle Scholar
  21. Keller A., Schleicher T., Schultz J., Müller T., Dandekar T., Wolf M. 2009. 5.8 S-28S rRNA interaction and HMM-based ITS2 annotation. Gene, 430, 50–57CrossRefGoogle Scholar
  22. Kudlai O., Pulis E.E., Kostadinova A., Tkach V.V. 2016. Neopsilotrema n. g. (Digenea: Psilostomidae) and three new species from ducks (Anseriformes: Anatidae) in North America and Europe. Systematic Parasitology, 93, 307–319CrossRefGoogle Scholar
  23. Kumar S., Stecher G., Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874CrossRefGoogle Scholar
  24. Lanfear R., Calcott B., Ho S.Y., Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701CrossRefGoogle Scholar
  25. Linton E. 1910. Helminth fauna of the Dry Tortugas. II. Trematodes. Papers from the Tortugas Laboratory of the Carnegie Institute of Washington, 4, 11–98Google Scholar
  26. Littlewood D.T.J. 1994. Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution, 3, 221–229CrossRefGoogle Scholar
  27. 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, 449–466CrossRefGoogle Scholar
  28. Littlewood D.T.J., Olson P. 2001. Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: (Eds D.T.J. Littlewood and R.A. Bray), Interrelationships of the Platyhelminthes, London, Taylor and Francis, 262–278Google Scholar
  29. 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, 1289–1297CrossRefGoogle Scholar
  30. Liu S. 2003. Two new species of Haplosplanchnidae (Digenea) from Liza caranatus from the Taiwan Straits, China. Acta Hydrobiologica Sinica, 5, 531–534. (In Chinese with English summary)Google Scholar
  31. Looss A. 1902. Zur kenntnis der trematodenfauna des Triester Hafens. II. Ueber Monorchis Montic. und Haplosplanchnus n. g. Zentralblatt für Bakteriologie, Parasitenkunde und Infectionskrankheiten, 32, 115–122. (In German)Google Scholar
  32. Machida M., Kuramochi T. 2000. Digenean trematodes from halfbeaks and needlefishes of Japan and adjacent waters. Bulletin of the National Science Museum, Japan. Series A. Zoology, 26, 203–218.Google Scholar
  33. Machida M., Uchida A. 1990. Trematodes from unicornfishes of Japanese and adjacent waters. Memoirs of the National Science Museum, Tokyo, 23, 69–81Google Scholar
  34. Madhavi R. 1979. Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Families Haplosplanchnidae and Haploporidae. Rivista di Parassitologia, 40, 237–248.Google Scholar
  35. Madhavi R. 2005. Superfamily Haplosplanchnoidea Poche, 1926. In: (Eds A. Jones, R.A. Bray and D.I. Gibson) Keys to the Trematoda, Vol. 2. CABI Publishing and the Natural History Museum, Wallingford, 175–184CrossRefGoogle Scholar
  36. Manter H.W. 1937. The status of the trematode genus Deradena Linton with a description of six species of Haplosplanchnus Looss. In: R.-E.S. Schulz and M. P. Gnyedina (Eds) Papers on helminthology published in commemoration of the 30 year jubileum of KJ Skrjabin and the 15th anniversary of the All-Union Institute of Helminthology. Moscow: All-Union Lenin Academy of Agricultural Sciences, pp. 381–387Google Scholar
  37. Miller M.A., Pfeiffer W., 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. 1–8Google Scholar
  38. Miller T.L., Bray R.A., Cribb T.H. 2011. Taxonomic approaches to and interpretation of host specificity of trematodes of fishes: lessons from the Great Barrier Reef. Parasitology, 138, 1710–1722CrossRefGoogle Scholar
  39. Morgan J.A., Blair D. 1995. Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology, 111, 609–615CrossRefGoogle Scholar
  40. Nahhas F. M., Rhodes D.Y., Seeto J. 1997. Digenetic Trematodes of Marine Fishes from Suva, Fiji. Family Haplosplanchnidae Poche, 1926: description of new species, a review and an update. Marine Studies. The University of the South Pacific Technical Report Series 97/4, pp.87Google Scholar
  41. Nolan M.J., Cribb T.H. 2005. The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163CrossRefGoogle Scholar
  42. Nolan M.J., Cribb T.H. 2006. Cardicola Short, 1953 and Braya n. gen.(Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa, 1265, 3–80Google Scholar
  43. Olson P., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755CrossRefGoogle Scholar
  44. Overstreet R. M. 1969. Digenetic trematodes of marine teleost fishes from Biscayne Bay, Florida. Tulane Studies in Zoology and Botany, 15, 119–176Google Scholar
  45. 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, 369–371CrossRefGoogle Scholar
  46. Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542CrossRefGoogle Scholar
  47. Sambrook J., Russell D. (Eds). 2001. Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 234Google Scholar
  48. Snyder S.D., Tkach V.V. 2001. Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–1440CrossRefGoogle Scholar
  49. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313CrossRefGoogle Scholar
  50. Tan G., Muffato M., Ledergerber C., Herrero J., Goldman N., Gil M., Dessimoz C. 2015. Current methods for automated filtering of multiple sequence alignments frequently worsen single-gene phylogenetic inference. Systematic Biology, 64, 778–791CrossRefGoogle Scholar
  51. Trieu N., Cutmore S.C., Miller T.L., Cribb T.H. 2015. A species pair of Bivesicula Yamaguti, 1934 (Trematoda: Bivesiculidae) in unrelated Great Barrier Reef fishes: implications for the basis of speciation in coral reef fish trematodes. Systematic Parasitology, 91, 231–239CrossRefGoogle Scholar
  52. Wee N.Q., Cribb T.H., Bray R.A., Cutmore S.C. 2017. Two known and one new species of Proctoeces from Australian teleosts: variable host-specificity for closely related species identified through multi-locus molecular data. Parasitology International, 66, 16–26CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2017

Authors and Affiliations

  • Daniel C. Huston
    • 1
    Email author
  • Scott C. Cutmore
    • 1
  • Thomas H. Cribb
    • 1
  1. 1.School of Biological SciencesThe University of QueenslandSt LuciaAustralia

Personalised recommendations