Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T05:24:54.208Z Has data issue: false hasContentIssue false
  • English
  • Français

A new genus and species of the trematode family Gyliauchenidae Fukui, 1929 from an unexpected, but plausible, host, Kyphosus cornelii (Perciformes: Kyphosidae)

Published online by Cambridge University Press:  13 March 2019

Daniel C. Huston Open the ORCID record for Daniel C. Huston [Opens in a new window] ,
Terrence L. Miller ,
Scott C. Cutmore  and
Thomas H. Cribb
Daniel C. Huston*
Affiliation:
The University of Queensland, School of Biological Sciences, Brisbane, QLD 4072, Australia
Terrence L. Miller
Affiliation:
Department of Primary Industries and Regional Development, Fish Health Laboratory, South Perth, WA 6151, Australia
Scott C. Cutmore
Affiliation:
The University of Queensland, School of Biological Sciences, Brisbane, QLD 4072, Australia
Thomas H. Cribb
Affiliation:
The University of Queensland, School of Biological Sciences, Brisbane, QLD 4072, Australia
*
Author for correspondence: Daniel Huston, E-mail: Daniel.Huston@uqconnect.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The Enenteridae Yamaguti, 1958 and Gyliauchenidae Fukui, 1929 exhibit an interesting pattern of host partitioning in herbivorous fishes of the Indo-West Pacific. Enenterids are known almost exclusively from fishes of the family Kyphosidae, a group of herbivorous marine fishes common on tropical and temperate reefs. In contrast, gyliauchenids are found in most of the remaining lineages of marine herbivorous fishes, but until the present study, had never been known from kyphosids. Here we report on the first species of gyliauchenid known from a kyphosid. Endochortophagus protoporus gen. nov., sp. nov. was recovered from the Western buffalo bream, Kyphosus cornelii (Whitley, 1944), collected off Western Australia. Kyphosus cornelii also hosts an enenterid, Koseiria allanwilliamsi Bray & Cribb, 2002, and is thus the first fish known in which enenterids and gyliauchenids co-occur. Molecular phylogenetic analyses place the new species close to those of Affecauda Hall & Chambers, 1999 and Flagellotrema Ozaki, 1936, but there is sufficient morphological evidence, combined with the unusual host, to consider it distinct from these genera. We discuss factors which may have contributed to the host partitioning pattern observed between enenterids and gyliauchenids.

Keywords

Biodiversitydigeneahost compatibilityhost encounterIndo-West PacificPlatyhelminthessystematicstaxonomy
Type
Research Article
Information
Parasitology , Volume 146 , Issue 7 , June 2019 , pp. 937 - 946
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Jahdali, M and Hassanine, RE-S (2012) The life cycle of Gyliauchen volubilis Nagaty, 1956 (Digenea: Gyliauchenidae) from the Red Sea. Journal of Helminthology 86, 165–172.Google Scholar
Bray, RA and Cribb, TH (2001) A review of the family Enenteridae Yamaguti, 1958 (Digenea), with descriptions of species from Australian waters, including Koseiria huxleyi n. sp. Systematic Parasitology 48, 1–29.Google Scholar
Bray, RA and Cribb, TH (2002) Further observations on the Enenteridae Yamaguti, 1958 (Digenea, Lepocreadioidea) of the Indo-West Pacific region, including a new species from Western Australia. Acta Parasitologica 47, 208–223.Google Scholar
Bray, RA and Cribb, TH (2012) Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Systematic Parasitology 83, 169–177.Google Scholar
Bray, RA, Waeschenbach, A, Cribb, TH, Weedall, GD, Dyal, P and Littlewood, D (2009) The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitologica 54, 310–329.Google Scholar
Bray, RA, Cribb, TH and Cutmore, SC (2018) Lepocreadiidae Odhner, 1905 and Aephnidiogenidae Yamaguti, 1934 (Digenea: Lepocreadioidea) of fishes from Moreton Bay, Queensland, Australia, with the erection of a new family and genus. Systematic Parasitology 95, 479–498.Google Scholar
Cable, RM (1954) Studies on marine digenetic trematodes of Puerto Rico. The life cycle in the family Haplosplanchnidae. The Journal of Parasitology 40, 71–76.Google Scholar
Cheal, A, Emslie, M, Miller, I and Sweatman, H (2012) The distribution of herbivorous fishes on the great barrier reef. Marine Biology 159, 1143–1154.Google Scholar
Choat, JH and Clements, KD (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annual Review of Ecology and Systematics 29, 375–403.Google Scholar
Choat, JH, Clements, KD and Robbins, WD (2002) The trophic status of herbivorous fishes on coral reefs. I: dietary analyses. Marine Biology 140, 613–623.Google Scholar
Choat, JH, Robbins, WD and Clements, KD (2004) The trophic status of herbivorous fishes on coral reefs. II: food processing modes and trophodynamics. Marine Biology 145, 445–454.Google Scholar
Clements, KD and Choat, JH (1995) Fermentation in tropical marine herbivorous fishes. Physiological Zoology 68, 355–378.Google Scholar
Clements, KD and Choat, JH (1997) Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus. Marine Biology 127, 579–586.Google Scholar
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago and London: University of Chicago Press.Google Scholar
Cribb, TH and Bray, RA (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76, 1–7.Google Scholar
Cribb, TH, Adlard, RD and Bray, RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28, 1791–1795.Google Scholar
Cribb, TH, Bray, RA, Diaz, PE, Huston, DC, Kudlai, O, Martin, SB, Yong, RQ-Y and Cutmore, SC (2016) Trematodes of fishes of the Indo-West Pacific: told and untold richness. Systematic Parasitology 93, 237–247.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.Google Scholar
Dyer, WG, Williams, EH Jr and Williams, LB (1988) Digenetic trematodes of marine fishes of Okinawa, Japan. The Journal of Parasitology 74, 638–645.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Fidopiastis, PM, Bezdek, DJ, Horn, MH and Kandel, JS (2006) Characterizing the resident, fermentative microbial consortium in the hindgut of the temperate-zone herbivorous fish, Hermosilla azurea (Teleostei: Kyphosidae). Marine Biology 148, 631–642.Google Scholar
Gomon, MF, Bray, DJ and Kuiter, RH (2008). Fishes of Australia's Southern Coast. Melbourne: Reed New Holland, Museum Victoria.Google Scholar
Goto, S and Matsudaira, Y (1918) On Dissotrema papillatum n. gen., n. sp. an amphistomoid parasite from a marine fish. Journal of the College of Science, Imperial University of Tokyo 39, 1–19.Google Scholar
Hall, KA and Cribb, TH (2004) Ptychogyliauchen, a new genus of Gyliauchenidae (Platyhelminthes: Digenea) from siganid fishes of the Indo-West Pacific. Invertebrate Systematics 18, 607–625.Google Scholar
Hall, KA and Cribb, TH (2005 a) Family Gyliauchenidae Fukui, 1929. In Jones, A, Bray, R and Gibson, D (eds), Keys to the Trematoda, vol. 2. Wallingford: CABI Publishing and the Natural History Museum, pp. 665–678.Google Scholar
Hall, KA and Cribb, TH (2005 b) Revision of Telotrema ozaki, 1933 (Digenea: Gyliauchenidae Fukui, 1929), including the description of a new species from an acanthurid fish from the great barrier reef, Queensland, Australia. Zootaxa 1071, 1–18.Google Scholar
Hall, KA and Cribb, TH (2007) Rediagnosis of Ichthyotrema caballero & Bravo-Hollis, 1952 (Digenea: Gyliauchenidae Fukui, 1929), including the redescription of I. vogelsangi Caballero & Bravo-Hollis, 1952. Zootaxa 1549, 63–68.Google Scholar
Hall, KA and Cribb, TH (2008) Revision of Flagellotrema ozaki, 1936 (Digenea, Gyliauchenidae Fukui, 1929), including the description of two species from acanthuroid fishes from the great barrier reef, Queensland, Australia. Zootaxa 1718, 1–35.Google Scholar
Hassanine, RE-S, Al-Zahrani, D, Touliabah, HE-S and Youssef, E (2016) The life cycle of Hexangium sigani Goto & Ozaki, 1929 (Digenea: Microscaphidiidae) from the Red Sea. Journal of Helminthology 90, 539–546.Google Scholar
Hughes-Stamm, SR, Cribb, TH and Jones, MK (1999) Structure of the tegument and ectocommensal microorganisms of Gyliauchen nahaensis (Digenea: Gyliauchenidae), an inhabitant of herbivorous fish of the great barrier reef, Australia. The Journal of Parasitology 85, 1047–1052.Google Scholar
Huston, DC, Cutmore, SC and Cribb, TH (2016) The life-cycle of Gorgocephalus yaaji Bray & Cribb, 2005 (Digenea: Gorgocephalidae) with a review of the first intermediate hosts for the superfamily Lepocreadioidea Odhner, 1905. Systematic Parasitology 93, 653–665.Google Scholar
Huston, DC, Cutmore, SC and Cribb, TH (2018) Isorchis cannoni n. sp. (Digenea: Atractotrematidae) from great barrier reef rabbitfishes and the molecular elucidation of its life cycle. Journal of Helminthology 92, 604–611.Google Scholar
Jones, MK, Hughes-Stamm, SR, East, RM and Cribb, TH (2000) Ultrastructure of the digestive tract of Gyliauchen nahaensis (Platyhelminthes, Digenea), an inhabitant of the hindgut of herbivorous fishes. Journal of Morphology 246, 198–211.Google Scholar
Knudsen, SW and Clements, KD (2013) Revision of the fish family Kyphosidae (Teleostei: Perciformes). Zootaxa 3751, 1–101.Google Scholar
Knudsen, SW and Clements, KD (2016) World-wide species distributions in the family Kyphosidae (Teleostei: Perciformes). Molecular Phylogenetics and Evolution 101, 252–266.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Littlewood, DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution 3, 221–229.Google Scholar
Littlewood, DTJ, Rohde, K and Clough, KA (1997) Parasite speciation within or between host species? – phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297.Google 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.Google Scholar
Martin, SB, Huston, DC, Cutmore, SC and Cribb, TH (2018) A new classification for deep-sea opecoelid trematodes based on the phylogenetic position of some unusual taxa from shallow-water, herbivorous fishes off south-west Australia. Zoological Journal of the Linnean Society, zly081. https://doi.org/10.1093/zoolinnean/zly081Google Scholar
Miller, MA, Pfeiffer, W and 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
Morgan, JA and 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, 609–615.Google Scholar
Mountfort, DO, Campbell, J and Clements, KD (2002) Hindgut fermentation in three species of marine herbivorous fish. Applied and Environmental Microbiology 68, 1374–1380.Google Scholar
Nahhas, FM and Wetzel, JA (1995) Digenetic trematodes of marine fishes from Suva, Fiji: the family Gyliauchenidae Ozaki, 1933. Journal of the Helminthological Society of Washington 62, 117–130.Google Scholar
Nelson, JS (2006). Fishes of the World, 4 Edn. Hoboken, New Jersey, USA: John Wiley & Sons.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.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.Google Scholar
Rimmer, D and Wiebe, W (1987) Fermentative microbial digestion in herbivorous fishes. Journal of Fish Biology 31, 229–236.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Sambrook, J and Russell, D (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press New.Google Scholar
Snyder, SD and Tkach, VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology 87, 1433–1440.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.Google Scholar
Sturm, EA and Horn, MH (1998) Food habits, gut morphology and pH, and assimilation efficiency of the zebraperch Hermosilla azurea, an herbivorous kyphosid fish of temperate marine waters. Marine Biology 132, 515–522.Google Scholar
Wee, NQ-X, Cribb, TH, Bray, RA and Cutmore, SC (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, 16–26.Google Scholar
WoRMS (2018) Gyliauchenidae Fukui, 1929. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=108437 on 2018–11–22.Google Scholar