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

Daniel C. Huston, Scott C. Cutmore and Thomas H. Cribb
From the journal Acta Parasitologica


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.


The authors thank the staff of the Lizard Island (Australian Museum) and Moreton Bay (University of Queensland) research stations for their ongoing support of our field expeditions, and our anonymous reviewers for their constructive criticisms which greatly improved the content of this manuscript. We thank the Australian Biological Resources Study (ABRS) for their ongoing support. This study was funded by the ABRS National Taxonomy Research Grant RF215–40 to SC and TH and by a PADI Foundation grant and Systematics Research Fund grant to DH.


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, 149–15810.1007/BF00009620Search in Google Scholar

Ankenbrand M.J., Keller A., Wolf M., Schultz J., Förster F. 2015. ITS2 database V: Twice as much. Molecular Biology and Evolution, 32, 3030–303210.1093/molbev/msv174Search in Google Scholar

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, 238–23410.1017/S0022149X15000280Search in Google Scholar

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, 295–30610.1007/s11230-016-9631-2Search in Google Scholar

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 SpainSearch in Google Scholar

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, 41–4310.1007/s11230-005-5526-3Search in Google Scholar

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 Mary Limología, Universidad Nacional Autónoma de México, 17, 191–203. (In Spanish)Search in Google Scholar

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)Search in Google Scholar

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, 1791–179510.1016/S0020-7519(98)00127-1Search in Google Scholar

Cribb T.H., Bray R.A. 2010. Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology, 76, 1–710.1007/s11230-010-9229-zSearch in Google Scholar PubMed

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, 81–9710.1007/BF00009589Search in Google Scholar

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, 237–24710.1007/s11230-016-9625-0Search in Google Scholar PubMed

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, 168–185Search in Google Scholar

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, 639–65210.1007/s11230-016-9658-4Search in Google Scholar PubMed

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, 3063–307410.1007/s00436-013-3481-5Search in Google Scholar

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–179710.1093/nar/gkh340Search in Google Scholar

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, 399–410Search in Google Scholar

Eysenhardt H. W. 1829. Einiges über eingeweide-würmer. Verhandlungen der Gesellschaft Naturforschender Freunde zu Berlin, 1, 144–152. (In German)Search in Google Scholar

Gibson D. 2013. Schikhobalotrema Skrjabin and Guschanskaja, 1955. Accessed through: World Register of Marine Species at on 2016-11–28Search in Google Scholar

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, 653–66510.1007/s11230-016-9655-7Search in Google Scholar

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, 50–5710.1016/j.gene.2008.10.012Search in Google Scholar

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, 307–31910.1007/s11230-016-9634-zSearch in Google Scholar

Kumar S., Stecher G., Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–187410.1093/molbev/msw054Search in Google Scholar

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, 1695–170110.1093/molbev/mss020Search in Google Scholar

Linton E. 1910. Helminth fauna of the Dry Tortugas. II. Trematodes. Papers from the Tortugas Laboratory of the Carnegie Institute of Washington, 4, 11–98Search in Google Scholar

Littlewood D.T.J. 1994. Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution, 3, 221–22910.1006/mpev.1994.1024Search in Google Scholar

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, 449–46610.1006/mpev.2000.0802Search in Google Scholar

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, 262–278Search in Google Scholar

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, 1289–129710.1016/S0020-7519(97)00086-6Search in Google Scholar

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)Search in Google Scholar

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)Search in Google Scholar

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.Search in Google Scholar

Machida M., Uchida A. 1990. Trematodes from unicornfishes of Japanese and adjacent waters. Memoirs of the National Science Museum, Tokyo, 23, 69–81Search in Google Scholar

Madhavi R. 1979. Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Families Haplosplanchnidae and Haploporidae. Rivista di Parassitologia, 40, 237–248.Search in Google Scholar

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, 175–18410.1079/9780851995878.0175Search in Google Scholar

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. 381–387Search in Google Scholar

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. 1–810.1109/GCE.2010.5676129Search in Google Scholar

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– 172210.1017/S0031182011000576Search in Google Scholar

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, 609–61510.1017/S003118200007709XSearch in Google Scholar

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.87Search in Google Scholar

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, 101–16310.1016/S0065-308X(05)60002-4Search in Google Scholar

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, 3–8010.11646/zootaxa.1265.1.1Search in Google Scholar

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, 733–75510.1016/S0020-7519(03)00049-3Search in Google Scholar

Overstreet R. M. 1969. Digenetic trematodes of marine teleost fishes from Biscayne Bay, Florida. Tulane Studies in Zoology and Botany, 15, 119–176Search in Google Scholar

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, 369–37110.1016/j.ympev.2008.03.024Search in Google Scholar

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, 539–54210.1093/sysbio/sys029Search in Google Scholar

Sambrook J., Russell D. (Eds). 2001. Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 234Search in Google Scholar

Snyder S.D., Tkach V.V. 2001. Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–144010.1645/0022-3395(2001)087[1433:PABRAS]2.0.CO;2Search in Google Scholar

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–131310.1093/bioinformatics/btu033Search in Google Scholar PubMed PubMed Central

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, 778–79110.1093/sysbio/syv033Search in Google Scholar PubMed PubMed Central

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, 231–23910.1007/s11230-015-9576-xSearch in Google Scholar PubMed

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, 16–2610.1016/j.parint.2016.11.008Search in Google Scholar PubMed

Received: 2016-11-29
Revised: 2017-3-3
Accepted: 2017-3-27
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS

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