Syst Parasitol (2018) 95:479–498
https://doi.org/10.1007/s11230-018-9803-3
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
Rodney A. Bray . Thomas H. Cribb . Scott C. Cutmore
Received: 13 March 2018 / Accepted: 19 May 2018 / Published online: 31 May 2018
Ó The Author(s) 2018
Abstract Digeneans of the lepocreadioid families
Lepocreadiidae Odhner, 1905 and Aephnidiogenidae
Yamaguti, 1934 from Moreton Bay, off southern
Queensland, Australia, are recorded, along with the
erection of a new family, Gibsonivermidae. Molecular
data were generated for all representatives of these
families collected during this study and a phylogram
for members of the superfamily was generated based
on the partial 28S rDNA dataset, placing these species
in context with those previously sequenced. This
phylogenetic analysis demonstrates that the
This article was registered in the Official Register of
Zoological Nomenclature (ZooBank) as urn:lsid:zoobank.org:
pub:907DBCEC-B908-4135-90AA-3950B0F75DD8. This
article was published as an Online First article on the online
publication date shown on this page. The article should be cited
by using the doi number. This is the Version of Record.
This article is part of the Topical Collection Digenea.
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s11230-018-9803-3) contains supplementary material, which is available to authorized
users.
R. A. Bray (&)
Department of Life Sciences, Natural History Museum,
Cromwell Road, London SW7 5BD, UK
e-mail: rab@nhm.ac.uk
T. H. Cribb S. C. Cutmore
School of Biological Sciences, The University of
Queensland, St Lucia, QLD 4072, Australia
monotypic Gibsonivermis Bray, Cribb & Barker,
1997 is isolated from all other lepocreadioids and
supports the erection of Gibsonivermidae n. fam.,
which is defined morphologically, based particularly
on the uniquely elongated male terminal genitalia, the
distribution of the uterus in the forebody and the
presence of a uroproct. Mobahincia teirae n. g., n. sp.
is reported from Platax teira (Forsskål) in Moreton
Bay and off Heron Island and New Caledonia.
Recognition of this new genus is based on molecular
results and the combination of caeca abutting the
posterior body wall and the lack of an anterior body
scoop or flanges. The following lepocreadioid species
are reported from Moreton Bay for the first time:
Bianium arabicum Sey, 1996 in Lagocephalus lunaris
(Bloch & Schneider), Diploproctodaeum cf. monstrosum Bray, Cribb & Justine, 2010 in Arothron hispidus
(Linnaeus), Multitestis magnacetabulum Mamaev,
1970 and Neomultitestis aspidogastriformis Bray &
Cribb, 2003 in Platax teira and Opechona austrobacillaris Bray & Cribb, 1998 in Pomatomus saltatrix
(Linnaeus). Bianium plicitum (Linton, 1928) is
reported from Torquigener squamicauda (Ogilby)
for the first time. Sequences of newly collected
specimens of Austroholorchis sprenti (Gibson, 1987)
indicate that the species forms a clade with other
members of the Aephnidiogenidae, agreeing with its
morphology. The phylogenetic status of all newly
sequenced species is discussed.
123
480
Introduction
During January and July 2016, workshops were held at
the Moreton Bay Research Station at Dunwich on
North Stradbroke Island, off southern Queensland,
Australia, as part of a collaborative study of the
metazoan parasite fauna of the fishes, particularly the
commercially important fishes, of Moreton Bay. The
present work is a report on some of the digeneans
found, framed as an overview of our knowledge of the
closely related families Lepocreadiidae Odhner, 1905
and Aephnidiogenidae Yamaguti, 1934 in Moreton
Bay. The lepocreadioid fauna of Australian and other
Indo-Pacific fishes has been ‘subjected to recent
sustained study’ (Cribb & Bray, 2011). This has been
documented in some 31 articles (see Bray et al., 2009,
and references therein; Bray et al., 2010b; Bray et al.,
2010a); however, much work remains to be done.
Some genera are large and/or complex and require
molecular data to elucidate their status.
Bray & Cribb (2012) divided members of the
Lepocreadiidae Odhner, 1905 as recognised by Bray
(2005) into three families based on a molecular
phylogeny. These three families, the Lepocreadiidae,
Lepidapedidae Yamaguti, 1958 and Aephnidiogenidae Yamaguti, 1934, had previously been considered subfamilies of the Lepocreadiidae (see Bray,
2005). In this paper, we analyse species of two of these
three families found in Moreton Bay. A new family
and a new genus and species are erected. In addition,
this report summarises information from earlier studies in the region. Collections representing specimens
of two lepocreadiid genera (Lepotrema Ozaki, 1932
and Preptetos Pritchard, 1960) and one lepidapedid
genus (Postlepidapedon Zdzitowiecki, 1993) will be
incorporated in genus-specific studies later and are
thus not reported here. Novel 28S and ITS2 rDNA
sequences are reported for all new collections, which
enable the placement of many of the Moreton Bay
species in a wider phylogenetic context.
Materials and methods
Specimen collection and morphological analysis
Fish were collected by line-fishing, spear-fishing,
seine netting and from the commercial tunnel-net
fishery in Moreton Bay, Queensland, Australia. Fish
were euthanised and examined for trematodes, as
123
Syst Parasitol (2018) 95:479–498
described by Cribb & Bray (2010). Those collected
were fixed by pipetting into near-boiling saline and
immediately preserved in formalin or 70% ethanol.
Whole-mounts were stained with Mayer’s paracarmine or Mayer’s haematoxylin, dehydrated in a graded
ethanol series, cleared in beechwood creosote or
methyl salicylate and mounted in Canada balsam.
Measurements were made through a drawing tube on
an Olympus BH-2 microscope, using a Digicad Plus
digitising tablet and Carl Zeiss KS100 software
adapted by Imaging Associates, and are quoted in
micrometres, with the range and the mean in parentheses. The following abbreviations are used:
NHMUK, Natural History Museum, London, UK;
MNHN, Museum National d’Histoire Naturelle, Paris,
France; QM, Queensland Museum Collection, Brisbane, Australia.
Molecular sequencing and phylogenetic analysis
Specimens for molecular analysis were processed
according to the protocols used by Sun et al. (2014).
The complete ITS2 rDNA region was amplified and
sequenced using the primers 3S (Morgan & Blair, 1995)
and ITS2.2 (Cribb et al., 1998) and the partial D1-D3 28S
rDNA region using LSU5 (Littlewood, 1994), 300F
(Littlewood et al., 2000), ECD2 (Littlewood et al., 1997)
and 1500R (Snyder & Tkach, 2001). GeneiousÒ version
10.2.3 (Kearse et al., 2012) was used to assemble and edit
contiguous sequences and the start and end of the ITS2
rDNA region were determined by annotation through the
ITS2 Database (Keller et al., 2009; Ankenbrand et al.,
2015) using the ‘Metazoa’ model.
The partial 28S rDNA sequences generated during
this study were aligned with sequences of related
species of the Lepocreadioidea Odhner, 1905 from
GenBank using MUSCLE version 3.7 (Edgar 2004)
run on the CIPRES portal (Miller et al., 2010), with
ClustalW sequence weighting and UPGMA clustering
for iterations 1 and 2. The resultant alignment was
refined by eye using MESQUITE (Maddison &
Maddison, 2017). The ends of each sequence were
trimmed, and ambiguously aligned regions were
identified and masked manually (those constituting
more than three bases and present in greater than 5% of
the sequences in the dataset).
Bayesian inference and maximum likelihood analyses of the 28S dataset were conducted to explore
relationships among these taxa. Bayesian inference
analysis was performed using MrBayes version 3.2.6
Syst Parasitol (2018) 95:479–498
(Ronquist et al., 2012) and maximum likelihood
analysis using RAxML version 8.2.10 (Stamatakis,
2014), both run on the CIPRES portal. The best
nucleotide substitution model was estimated using
jModelTest version 2.1.10 (Darriba et al., 2012). Both
the Akaike Information Criterion (AIC) and Bayesian
Information Criterion (BIC) predicted the GTR?I?C
model as the best estimator; Bayesian inference and
maximum likelihood analyses were conducted using
the closest approximation to this model. Nodal support
in the maximum likelihood analysis was estimated by
performing 100 bootstrap pseudoreplicates. Bayesian
inference analysis was run over 10,000,000 generations (ngen = 10,000,000) with two runs each
containing four simultaneous Markov Chain Monte
Carlo (MCMC) chains (nchains = 4) and every 1,000th
tree saved. Bayesian inference analysis used the
following parameters: nst = 6, rates = invgamma,
ngammacat = 4, and the priors parameters of the
combined dataset were set to ratepr = variable.
Samples of substitution model parameters and tree
and branch lengths were summarised using the
parameters: sump burnin = 3,000 and sumt burnin =
3,000. Species of the families Cryptogonimidae Ward,
1917 and Apocreadiidae Skrjabin, 1942 were designated as functional outgroup taxa, sensu Bray et al.
(2009).
Family Lepocreadiidae Odhner, 1905
Subfamily Lepocreadiinae Odhner, 1905
Genus Bianium Stunkard, 1930
481
Representative DNA sequences: ITS2 rDNA, four
identical replicates (two in GenBank MH157055MH157056); 28S rDNA, one sequence (GenBank
MH157066).
New measurements: Supplementary Table S1.
Remarks
The new specimens (Fig. 1A) are morphologically
identical to those reported from Moreton Bay by Bray
& Cribb (1998) from Whitley’s toadfish Torquigener
whitleyi (Paradice) and T. pleurogramma. New ITS2
rDNA sequences of specimens from T. squamicauda and
T. pleurogramma were identical. Analysis of the 28S
data showed that this species forms a strongly supported
clade with similar lepocreadiid species from tetraodontiforms (other species of Bianium, Pelopscreadium
Dronen, Blend, Khalifa, Mohamadain & Karer, 2016,
Diplocreadium Park, 1939, Diploproctodaeum La Rue,
1926 and Lobatocreadium Madhavi, 1972); nodal
support for relationships within this clade was weak
(Fig. 2). The two species of Bianium included in the
phylogenetic analyses are paraphyletic with respect to
species of Diplocreadium, Diploproctodaeum and Lobatocreadium. The status of these specimens from
Moreton Bay as identical to Bianum plicitum as
described by Linton (1928) is yet to be tested by DNA
sequence comparison, and we think it highly likely that
forms from eastern Australian waters are not conspecific
with the original specimens from off north-eastern USA.
Bianium arabicum Sey, 1996
Bianium plicitum (Linton, 1928) Stunkard, 1931
Syn. Psilostomum plicitum Linton, 1928
Type-host: Larus argentatus Pontoppidan (Charadriiformes: Laridae), herring gull.
Type-locality: Woods Hole, Massachusetts, USA.
New records:
Hosts: Torquigener squamicauda (Ogilby), brush-tail
toadfish; T. pleurogramma (Regan), weeping toado
(Tetraodontiformes: Tetraodontidae).
Localities: Ex T. squamicauda, Moreton Banks,
Moreton Bay (27°240 S, 153°200 E); ex T. pleurogramma, off Amity, Moreton Bay (27°240 S,
153°260 E).
Site in host: Intestine.
Voucher material: Three specimens in the QM
G237251–3, one in the NHMUK 2018.3.26.1.
Type-host: Lagocephalus lunaris (Bloch & Schneider)
(Tetraodontiformes: Tetraodontidae), lunartail puffer.
Type-locality: Off Kuwait, Arabian Gulf.
New records:
Host: Lagocephalus lunaris.
Locality: Off Wynnum North, Moreton Bay (27°230 S,
153°110 E).
Site in host: Intestine.
Voucher material: Two specimens in the QM
G237254–5, one in the NHMUK 2018.3.26.2.
Representative DNA sequences: ITS2 rDNA, one
sequence (GenBank MH157054); 28S rDNA, one
sequence (GenBank MH157076).
New measurements: Supplementary Table S1.
123
482
Syst Parasitol (2018) 95:479–498
Fig. 1 A, Bianium plicitum (Linton, 1928) ex Torquigener squamicauda, ventral view, uterus in outline; B, Bianium arabicum Sey,
1996 ex Lagocephalus lunaris, ventral view, uterus in outline; C, Mobahincia teirae n. g., n. sp. ex Platax teira, Moreton Bay, ventral
view, uterus in outline; D, Mobahincia teirae n. g., n. sp. ex Platax teira, off Heron Island, ventral view, uterus in outline. Scale-bars: A,
B, 500 lm; C, D, 200 lm
123
Syst Parasitol (2018) 95:479–498
Remarks
In the original description of B. arabicum, Sey (1996)
stated ‘Along the lateral sides of body longitudinal
folds present, bending ventrally and ending at posterior extremity’. The longitudinal folds (flanges) do not
appear to reach the full length of the body in our
specimens (Fig. 1B). When describing specimens
considered to be this species from the silverstripe
blaasop Lagocephalus sceleratus (Gmelin) off New
Caledonia, Bray et al. (2010a) said ‘it has full-length
lateral folds of the body (or scoop-sides), although the
full extent is not always visible on both sides of the
worm’. These authors pointed out the similarity of
these worms to those described from L. lunaris by
Hafeezullah (1970) under the name B. plicitum
(Linton, 1928) from off Chennai (as Madras) in the
Bay of Bengal and by Shen & Tong (1990) under the
name B. dayawanense Shen & Tong, 1990 from Daya
Bay, China [in this case the host is quoted as L. lunaris
spadiceus (Richardson)]. The lateral flanges of the
Bay of Bengal worms are similar to those seen in our
specimens and the dimensions are close to those found
by Sey (1996) and Bray et al. (2010a) (Supplementary
Table S1). The Chinese worms tend to be larger and
the flanges are illustrated as distinct flaps reaching
only to the ventral sucker level. It is not possible to be
certain of the status of all these forms, but it appears
that the Bay of Bengal specimens are more similar to
the worms here considered B. arabicum. This is the
first report of B. arabicum from Moreton Bay.
Analysis of the 28S data showed that this species
forms a strongly-supported clade with similar lepocreadiid species from tetraodontiforms; nodal support for
relationships within this clade were weak (Fig. 2) and,
as discussed above, the two species of Bianium did not
form a clade.
Genus Clavogalea Bray, 1985
Clavogalea trachinoti (Fischthal & Thomas, 1968)
Bray & Gibson, 1990
Syns Stephanostomum trachinoti Fischthal & Thomas,
1968; Opechona pseudobacillaris Fischthal & Thomas, 1970
Type-host: Trachinotus goreensis Cuvier (Perciformes: Carangidae), longfin pompano.
Type-locality: Off Iture, Elmina, Ghana.
483
New records:
Host: Trachinotus coppingeri Günther (Perciformes:
Carangidae), swallowtail dart.
Locality: Off Green Island, Moreton Bay (27°250 S,
153°140 E).
Site in host: Intestine.
Voucher material: Six specimens in the QM
G237275–80.
Representative DNA sequences: ITS2 rDNA, three
replicates (one in GenBank MH157057); 28S rDNA,
one sequence (GenBank MH157067).
Remarks
Bray & Gibson (1990) redescribed the original
specimens of Stephanostomum trachinoti Fischthal
& Thomas, 1968 and its synonym Opechona pseudobacillaris Fischthal & Thomas, 1970, and placed
the species in Clavogalea. Bray & Cribb (1998)
redescribed the worm based on new material from the
large-spotted dart Trachinotus botla (Shaw) off Heron
Island (southern Great Barrier Reef) and T. coppingeri
Günther off northern New South Wales and in
Moreton Bay. Our newly collected material appears
identical to these descriptions. New 28S rDNA data
were identical to sequences reported by Bray et al.
(2009) based on specimens from T. coppingeri
collected off Heron Island. Phylogenetic analysis of
the 28S dataset indicates that, of taxa available for
analysis, this species is most closely related to
Preptetos trulla (Linton, 1907), Prodistomum keyam
Bray & Cribb, 1996, Opechona austrobacillaris Bray
& Cribb, 1998 and Opechona kahawai Bray & Cribb,
2003. These five species formed a clade in the
phylogenetic analysis with C. trachinoti as sister to a
clade of the other four species; however, nodal support
for this topology was poor (Fig. 2).
Genus Diplocreadium Park, 1939
Diplocreadium tangaloomaense Bray, Cribb &
Barker, 1996 (emend.)
Type-host: Paramonacanthus japonicus (Tilesius)
(Tetraodontiformes: Monacanthidae), hairfinned
leatherjacket.
Type-locality: Off Tangalooma, Moreton Bay,
Queensland.
123
484
Syst Parasitol (2018) 95:479–498
Fig. 2 Relationships between members of the seven families of the superfamily Lepocreadioidea based on maximum likelihood
analysis of the partial 28S rDNA dataset. Species from Moreton Bay are shown in bold and clades representing the Enenteridae,
Gorgocephalidae, Gyliauchenidae and Lepidapedidae are collapsed for brevity. Maximum likelihood bootstrap support values are
shown above the nodes and Bayesian inference posterior probabilities below. Support values\80 and\0.80 are not shown. Outgroup
taxa are species of the Apocreadiidae and Cryptogonimidae. Abbreviations: Aephnidiog., Aephnidiogenidae; G, Gibsonivermidae;
Out., outgroup taxa
Remark
This species has not been detected since its original
description and no material is available for molecular
characterisation.
123
Diploproctodaeum monstrosum Bray, Cribb &
Justine, 2010
Type-host: Arothron stellatus (Anonymous) (Tetraodontiformes: Tetraodontidae), stellate puffer.
Syst Parasitol (2018) 95:479–498
485
Type-locality: Off Mermaid Beach, Lizard Island,
Queensland, Australia.
Type-locality: Off Mud Island, Moreton Bay,
Queensland.
Diploproctodaeum cf. monstrosum
Remark
New records
Host: Arothron hispidus (Linnaeus), white-spotted
puffer.
Locality: Off Peel Island, Moreton Bay (27°300 S,
153°200 E).
Site: Intestine.
Voucher material: Three specimens in the QM
G237281–3.
Representative DNA sequences: ITS2 rDNA, two
replicates (one in GenBank MH157059); 28S rDNA,
one sequence (GenBank MH157069).
This species has not been detected since its original
description and no material is available for molecular
characterisation.
Remarks
Bray et al. (2010a) reported this species in Arothron
stellatus and A. mappa from off Lizard Island. They
pointed out that the sequence of ‘Diploproctodaeum sp.’
from A. stellatus off Lizard Island (GenBank FJ788474),
used in the study of Bray et al. (2009), referred to this
species. 28S sequence data generated from the new
Moreton Bay material differs from that sequence by 5
bases. No morphological differences could be detected
between the two collections, but only a relatively small
number of specimens has been collected and the rather
amorphous structure of these worms makes morphological comparisons difficult. Given that the two sites are
only approximately 1,650 km apart, a 5 bp difference in
the 28S rDNA raises the possibility of the presence or
more than one species. However, we consider the current
evidence insufficient to suggest that specimens from
Moreton Bay represent a species distinct from that
occurring on the northern Great Barrier Reef but consider
the issue worthy of further consideration in the light of
additional genetic data from more variable gene regions
(Blasco-Costa et al., 2016). For the present, the designation D. cf. monstrosum seems the best way to draw
attention to these issues.
Diploproctodaeum yosogi Bray, Cribb & Barker,
1996
Type-host: Paramonacanthus japonicus (Tilesius)
(Tetraodontiformes: Monacanthidae), hairfinned
leatherjacket.
Genus Lepocreadioides Yamaguti, 1936
Syn. Bicaudum Bilqees, 1971
Lepocreadioides orientalis Park, 1939
Type-host: Cynoglossus joyneri Günther, red tonguesole (Pleuronectiformes: Cynoglossidae).
Type-locality: Off Simmi Island, North Tyôsen,
Korea.
Remark
This species has not been re-collected from Moreton
Bay since the report from the fourlined tonguesole
Cynoglossus bilineatus (Lacépède) by Bray & Cribb
(1998) and no material is available for molecular
characterisation.
Genus Mobahincia n. g.
Diagnosis
Body broader anteriorly, tapering posteriorly. Tegument spined. Eye-spot pigment scattered at pharyngeal
level. Oral sucker transversely oval, subterminal.
Ventral sucker rounded, smaller than oral sucker, in
anterior quarter of body-length. Prepharynx short.
Pharynx oval. Oesophagus not detected. Intestinal
bifurcation dorsal to anterior part of ventral sucker or
just in forebody. Caeca straight, reaching to posterior
extremity where they abut body wall at base on small
indentations; ani possibly present. Testes two, oval,
entire, tandem contiguous, in mid-hindbody. External
seminal vesicle large, saccular, dorsal to uterus.
Cirrus-sac claviform. Internal seminal vesicle large,
oval, curved. Pars prostatica oval vesicular, lined with
anuclear cell-like bodies. Ejaculatory duct thickwalled muscular, long, complexly folded. Genital
atrium small. Genital pore sinistral to antero-sinistral
to ventral sucker. Ovary multilobate, immediately pretesticular. Seminal receptacle canalicular. Mehlis’
123
486
gland dorsal to ovary. Uterus between ovary and
ventral sucker, intracaecal. Eggs tanned, operculate.
Vitellarium in follicular fields at ventral sucker level
and in hindbody. Parasites in intestine of ephippid
fishes.
Type-species: Mobahincia teirae n. sp.
Etymology: The generic name is a feminine noun
derived from the localities at which this genus has
been found: Moreton Bay (Moba), Heron Island (hi),
New Caledonia (nc).
ZooBank registration: To comply with the regulations
set out in article 8.5 of the amended 2012 version of
the International Code of Zoological Nomenclature
(ICZN, 2012), details of the new genus have been
submitted to ZooBank. The Life Science Identifier
(LSID) for Mobahincia n. g. is urn:lsid:
zoobank.org:act:8543D3CA-81FC-43A7-9ACB-6BA
5DE6D6BA4.
Remarks
The species on which this new genus is based
appears morphologically closely related to members of Diploproctodaeum and Bianium in having
its caeca abutting the posterior body wall, giving
the appearance of ani, the usual condition in
species of the latter genera; however, there is no
indication of an anterior scoop as is usually present
in these taxa. Molecular evidence suggests unambiguously that the new genus is not closely related
to members of these two genera. The exact
relationship of this species is not well resolved in
the phylogram derived from the 28S analyses of the
currently available lepocreadiid sequences (many
relationships within the family have poor support),
but it is clear that it does not resolve within the
well-supported clade which includes Diploproctodaeum and Bianium species (Fig. 2). Following the
key to the Lepocreadiidae produced by Bray
(2005), the species appears closest to members of
Lobatocreadium or Pseudocreadium Layman,
1930; the new genus differs from both in the
presence of long caeca abutting the body-wall and
the terminal excretory pore. The vitellarium is
more extensive in both species of Lobatocreadium
and Pseudocreadium, and in members of the latter
123
Syst Parasitol (2018) 95:479–498
genus the testes are symmetrical. We conclude that
the relationships of this form are best expressed by
the erection of a new genus.
Mobahincia teirae n. sp.
Type-host: Platax teira (Forsskål) (Perciformes:
Ephippidae), longfin batfish.
Type-locality: Four Beacons, Moreton Bay (27°100 S,
153°210 E).
Other localities: Off Heron Island (23°270 S,
151°550 E); Nouméa Fish Market, New Caledonia.
Site in host: Intestine.
Type-material: Holotype QM G237256 and 12 paratypes QM G237257–60, NHMUK 2018.3.26.5–8.
Voucher material: Off Heron Island: QM G237261;
off New Caledonia: MNHN JNC2872F.
Representative DNA sequences: ITS2 rDNA, five
replicates (one in GenBank MH157058); 28S rDNA,
one sequence (GenBank MH157068).
ZooBank registration: To comply with the regulations
set out in article 8.5 of the amended 2012 version of
the International Code of Zoological Nomenclature
(ICZN, 2012), details of the new species have been
submitted to ZooBank. The Life Science Identifier
(LSID) for Mobahincia teirae n. sp. is urn:lsid:zoobank.org:act:7FD7D6C8-D114-4C5E-BEDAE25CB81979E9.
Etymology: The specific epithet is derived from that of
the host species.
Description (Fig. 1C, D)
[Based on 7 ovigerous and seven non-ovigerous
specimens from Moreton Bay, 1 specimen from off
Heron Island and 1 specimen from off New Caledonia;
measurements given in Table 1.] Body broader anteriorly, tapering posteriorly. Body spines small on
anterior ‘shoulders’, much more robust along remainder of body, reach close to posterior extremity. Eyespot pigment scattered at pharyngeal level. Oral sucker
transversely oval, subterminal. Ventral sucker
rounded, smaller than oral sucker, in anterior quarter
of body-length. Prepharynx short, mainly in posterior
concavity of oral sucker. Pharynx oval. Oesophagus
not detected. Intestinal bifurcation dorsal to anterior
Syst Parasitol (2018) 95:479–498
487
Table 1 Measurements and ratios of Mobahincia teirae ex Platax teira
Locality
Moreton Bay (n = 7)
Range
Mean
New Caledonia
(n = 1)
Heron Island
(n = 1)
1,013 9 415
Body
685–1,018 9 344–427
834 9 383
750 9 395
Forebody length
186–234
204
214
221
Pre-oral lobe length
0–5
3
6
5
Oral sucker
104–141 9 148–190
125 9 170
127 9 179
115 9 170
Prepharynx length
0–35
5
0
8
90 9 89
Pharynx
82–100 9 80–105
Oesophagus length
0
Distance from intestinal bifurcation to ventral sucker
(IB-VS)
0–16
4
107 9 97
84 9 86
18
24
0
0
Distance from vitellarium to ventral sucker
0
0
19
0
Ventral sucker
79–112 9 90–122
96 9 103
89 9 98
93 9 99
175 9 56
Cirrus-sac
129–189 9 71–90
158 9 79
121 9 44
Distance from external seminal vesicle to ventral sucker
85–118
102
70
169
Distance from ventral sucker to ovary (VS-Ov)
20–51
34
17
61
Ovary
84–115 9 112–169
102 9 134)
64 9 110
132 9 133
Distance from ovary to anterior testis
0
0
0
0
Anterior testis
118–144 9 123–147
128 9 131
112 9 141
163 9 137
Distance between testes
0
0
0
0
Posterior testis
106–214 9 107–137
157 9 121
125 9 144
209 9 129
Post-testicular distance
112–190
150
128
190
Post-caecal distance
0–25
5
0
0
Eggs
58–70 9 26–41
62 9 34
63 9 23
69 9 33
Width (%)
41.9–59.0
46.5
52.7
41.0
Forebody (%)
21.8–27.2
24.7
28.5
21.8
Sucker length ratio
1:0.67–0.90
1:0.77
1:0.70
1:0.81
Sucker width ratio
1:0.58–0.64
1:0.60
1:0.55
1:0.58
Oral sucker: pharynx width
1:1.72–2.09
1:1.92
1:1.84
1:1.98
Ventral sucker to ovary (%)
2.63–5.02
4.04
2.32
6.06
External seminal vesicle to ventral sucker as % of VS-Ov
283–418
351
403
274
Post-testicular distance (%)
16–20
18
17.1
18.8
Prepharynx (%)
0–16.4
2.34
0
3.51
Oesophagus (%)
0
0
2.37
2.37
Distance IB-VS (%)
0–1.76
0.50
0
0
Vitellarium to ventral sucker distance (%)
0
0
2.47
0
Ovary to anterior testis (%)
0
0
0
0
Distance between testes (%)
0
0
0
0
Cirrus-sac length (%)
16.4–22.0
19.0
16.2
17.2
Pre-vitelline distance
186–234
204
195
221
Pre-vitelline distance (%)
21.8–27.2
24.7
26.0
21.8
Oesophagus length as % of forebody length
0
0
8.33
10.9
Distance IB-VS as % of forebody length
0–7.31
2.02
0
0
Vitellarium to ventral sucker distance as % of
forebody length
0
0
8.66
0
Note: (%), percent of body-length where not otherwise noted; IB-VS, intestinal bifurcation to ventral sucker distance. Where length is
followed by width, the two are separated by an ‘9’
123
488
part of ventral sucker or just in forebody. Caeca
straight, reach to posterior extremity where they abut
body wall at base on small indentations; ani possibly
present.
Testes 2, oval, entire, tandem contiguous, in midhindbody. External seminal vesicle large, saccular,
dorsal to uterus. Cirrus-sac claviform. Internal seminal
vesicle large, oval, curved. Pars prostatica oval
vesicular, lined with anuclear cell-like bodies. Ejaculatory duct thick-walled, muscular, long, complexly
folded. Genital atrium small. Genital pore closely
sinistral to antero-sinistral to ventral sucker.
Ovary multilobate (about 14–20 lobes), immediately
pre-testicular. Seminal receptacle saccular, dorsal to
anterior testis. Laurer’s canal not detected. Mehlis’ gland
dorsal to ovary. Uterus between ovary and ventral sucker,
intracaecal. Eggs tanned, operculate. Vitellarium follicular, in extensive dorsal and ventral fields, from level of
ventral sucker to posterior extremity; fields confluent at
level of testes and in post-testicular region.
Excretory pore terminal; excretory vesicle narrow
posteriorly, widens abruptly and reaches at least to
posterior testes.
Remarks
Several species of Diploproctodaeum are found in
Platax spp., namely D. plataxi Mamaev, 1970, D.
rutellum (Mamaev, 1970) and D. tsubameuo Bray &
Cribb, 2003; all three species have caeca abutting the
body-wall and are often described as having ani
(Mamaev, 1970; Bray & Cribb, 2003a). Other lepocreadiid species from Platax spp., such as Deraiotrema
platacis Machida, 1982, Neomultitestis palauensis
Machida, 1982 and N. aspidogastriformis Bray & Cribb,
2003 are also described as having ani or the appearance
of ani (Machida, 1982; Bray & Cribb, 2003a).
Phylogenetic analysis of the 28S dataset showed
that this species does not form a strongly-supported
clade with any particular clade of lepocreadiids. The
new species was sister to a clade including Neopreptetos arusettae Machida, 1982, Multitestis magnacetabulum Mamaev, 1970 and Neomultitestis aspidogastriformis, the latter two of which are Platax-infecting
species; however, nodal support for this relationship
was poor. The new species was not closely related to
species of other genera which have similar caecal
terminations, namely Diploproctodaeum, Bianium
and Pelopscreadium.
123
Syst Parasitol (2018) 95:479–498
Genus Multitestis Manter, 1931
Multitestis magnacetabulum Mamaev, 1970
Type-host: Platax orbicularis (Forsskål) (first host
listed) (Perciformes: Ephippidae), orbicular batfish.
Type-locality: Gulf of Tonkin.
New records:
Host: Platax teira (Forsskål) (Perciformes: Ephippidae), longfin batfish.
Locality: Four Beacons, Moreton Bay (27°100 S,
153°210 E).
Site in host: Intestine.
Voucher material: Six voucher specimens QM
G237262–7, three NHMUK 2018.3.26.9–11.
Representative DNA sequences: ITS2 rDNA, two
replicates (one in GenBank MH157061); 28S rDNA,
one sequence (GenBank MH157071).
New measurements: Supplementary Table S2.
Remarks
This is the first record of this species from Moreton Bay.
Bray & Cribb (2003a) reported it from Platax teira off
Heron Island and Bray et al. (2009) used sequences from
that collection in their molecular study of the superfamily
Lepocreadioidea. 28S sequence data generated from new
collections from Moreton Bay differed from the Heron
Island specimens (GenBank FJ788485) by a single base.
A single base difference is consistent with the minor
geographical variation found between these locations for
other trematodes (e.g. Cutmore et al., 2016; Brooks et al.,
2017); however, given that this single base difference (an
A to T transversion) is within the in the first 15 bases of
the start of the sequence, and that this base position is an
A in all other taxa included in the analysis, we predict
that the difference in FJ788485 is a sequencing misread.
This species has also been reported from the same host in
the waters off New Caledonia by Bray & Justine (2012).
Genus Neomultitestis Machida, 1982
Neomultitestis aspidogastriformis Bray & Cribb,
2003
Type-host: Platax teira (Forsskål) (Perciformes:
Ephippidae), longfin batfish.
Type-locality: Off Heron Island, Queensland, Australia.
New records
Syst Parasitol (2018) 95:479–498
Host: Platax teira.
Locality: Four Beacons, Moreton Bay (27°100 S,
153°210 E).
Site in host: Intestine.
Voucher material: One voucher specimen lodged in
the QM G237268.
Representative DNA sequences: ITS2 rDNA, one
sequence (GenBank MH157062); 28S rDNA, one
sequence (GenBank MH157072).
New measurements: Supplementary Table S2.
Remarks
Bray & Cribb (2003a) reported this species from
P. teira off Heron Island, and Bray et al. (2009) used
28S rDNA sequences from that collection in their
molecular study of the superfamily Lepocreadioidea.
This is the first report of N. aspidogastriformis from
Moreton Bay. New 28S data generated from Moreton
Bay specimens were identical to those of this species
off Heron Island (GenBank FJ788489).
Genus Opechona Looss, 1907
489
Cribb, 1998). Our specimens from Moreton Bay are
indistinguishable from those described by Bray &
Cribb (1998), and we are confident that the new
specimens are conspecific with those from off Fremantle and Iluka.
New 28S sequence data generated for O. austrobacillaris differs from those of O. kahawai, from Arripis sp.
off Tasmania, by just a single base. Unfortunately, no
ITS2 rDNA sequence data (a superior marker for species
delineation) are available for the Tasmanian species.
Bray & Cribb (2003b) distinguished these two species by
the sucker-ratio and the pseudoesophagus/oesophagus
length ratio, and by the forebody being proportionally
much longer in O. kahawai (40–44 vs 28–35% of body
length) (Supplementary Table S2; Bray & Cribb, 1998).
Given the minor genetic differences, the relationship
between these two morphologically distinct forms
warrants further study. Phylogenetic analysis of the
28S dataset showed these two species of Opechona to be
most closely related to Prodistomum keyam; however,
nodal support for this clade was poor.
Genus Prodistomum Linton, 1910
Opechona austrobacillaris Bray & Cribb, 1998
Prodistomum keyam Bray & Cribb, 1996
Type-host: Pomatomus saltatrix (Linnaeus), tailor
(Perciformes: Pomatomidae).
Type-locality: Off South Mole, Fremantle, Western
Australia.
New material:
Host: Pomatomus saltatrix.
Locality: Off Garden Island, Moreton Bay (27°360 S,
153°200 E).
Site in host: Intestine.
Voucher material: Two specimens in the QM
G237269–70, one in the NHMUK 2018.3.26.3.
Representative DNA sequences: ITS2 rDNA, two
replicates (one in GenBank MH157063); 28S rDNA,
one sequence (GenBank MH157073).
New measurements: Supplementary Table S2.
Type-host: Monodactylus argenteus (Linnaeus) (Perciformes: Monodactylidae), silver moony.
Type-locality: Off Hope Island, Queensland,
Australia.
New records:
Host: Monodactylus argenteus.
Locality: In Port of Brisbane Land Reclamation,
Moreton Bay (27°210 S, 153°110 E); off Amity, Moreton Bay (27°240 S, 153°260 E).
Site in host: Intestine.
Voucher material: Four specimens in the QM
G237271–4, one in the NHMUK 2018.3.26.3.
Representative DNA sequences: ITS2 rDNA, three
identical replicates (one in GenBank MH157064); 28S
rDNA, one sequence (GenBank MH157074).
New measurements: Supplementary Table S2.
Remarks
Remarks
This is the first report of this species from Moreton
Bay. Although the type-locality is off Western Australia, the original description also reported and
described this species from the eastern coast of
Australia, off Iluka in New South Wales (Bray &
Bray & Cribb (1996) and Bray et al. (2009) reported
this host/species combination in Moreton Bay. Bray
et al. (2009) used sequences of this species from this
host in Moreton Bay in their molecular study of the
123
490
superfamily Lepocreadioidea. Molecular data from
new specimens collected in this study were identical to
those (FJ788493) from Bray et al. (2009). Phylogenetic analysis of the 28S dataset showed P. keyam to
be most closely related to Opechona austrobacillaris
and O. kahawai, but with low support (Fig. 2). Bray &
Justine (2012) reported this species from the same host
from the waters around New Caledonia.
Family Gibsonivermidae n. fam.
Diagnosis
Body elongate-oval, flattened. Tegument armed with
small spines. Oral sucker subglobular, subterminal.
Ventral sucker rounded, pre-equatorial. Prepharynx
distinct. Pharynx oval. Oesophagus distinct. Intestinal
bifurcation in mid-forebody. Caeca form uroproct at
posterior extremity. Testes two, lobed to almost entire,
tandem, slightly separated, in mid-hindbody. External
seminal vesicle very elongate, tubular, coiled, reaches
well into hindbody. Cirrus-sac long, attenuated, coiled
proximally. Internal seminal vesicle tubular, coiled.
Pars prostatica long, narrow. Ejaculatory duct elongate, muscular, expands distally. Genital atrium small.
Genital pore dextrally submedian, ventral to pharynx.
Ovary with 4–6 lobes, pretesticular, slightly separated
from anterior testis. Seminal vesicle between ovary
and anterior testis. Uterus pre-ovarian, intercaecal;
lateral slings extend into forebody. Metraterm narrow.
Vitellarium follicular; fields reach from anterior
region of hindbody or ventral sucker to posterior
extremity. Excretory vesicle I-shaped, reaches anterior testis. In intestine of marine teleosts.
Type-genus: Gibsonivermis Bray, Cribb & Barker,
1997.
ZooBank registration: To comply with the regulations
set out in article 8.5 of the amended 2012 version of
the International Code of Zoological Nomenclature
(ICZN, 2012), details of the new family have been
submitted to ZooBank. The Life Science Identifier
(LSID) for Gibsonivermidae n. fam. is urn:lsid:zoobank.org:act:F50B45FB-6B41-44B4-8FD25042D1AD938F.
Remarks
Bray et al. (1997), in proposing Gibsonivermis, stated
that it is ‘not immediately clear to which subfamily
this genus belongs’, and Bray & Cribb (2012)
123
Syst Parasitol (2018) 95:479–498
considered Gibsonivermis a genus ‘incertae sedis
within the superfamily’ Lepocreadioidea and ‘too
enigmatic to allow confident placement’. Barker et al.
(1993) sequenced the D1 domain of the 28S ribosomal
RNA gene of the type-species of this new taxon under
its old name Intusatrium berryi Gibson, 1987 but did
not apparently submit the sequence to GenBank (it is
itemised in the paper). In the early days of the
development of molecular studies, few digenean
sequences were available. The tree produced by
Barker et al. (1993) included two other lepocreadioids,
Gyliauchen sp. (Gyliauchenidae) and Tetracerasta
blepta Watson, 1984 (Aephnidogenidae), which clustered with Gibsonivermis, but they stated that ‘evidence for the monophyly of the two lepocreadiids
[Tetracerasta and Gibsonivermis] was weak’. The
molecular phylogeny inferred from 28S data reported
here confirms that Gibsonivermis does not belong to
any of the six accepted lepocreadioid families (i.e.
Lepocreadiidae, Aephnidiogenidae, Enenteridae, Gorgocephalidae, Gyliauchenidae, Lepidapedidae; see
Bray & Cribb, 2012), constituents of which all form
strongly supported clades. It is distinct enough, both
morphologically and genetically, to warrant the proposal of a new family. In the current analyses, the
Gibsonivermidae was sister to the Lepidapedidae,
with branch lengths between the two families similar
to those found between the Lepocreadiidae and
Aephnidiogenidae, and the Enenteridae and Gyliauchenidae, indicative of a family level distinction.
Gibsonivermis berryi (Gibson, 1987) Bray, Cribb &
Barker, 1997 has several features very unusual for
species within the superfamily, the most striking of
which is the form of the male terminal genitalia
(Fig. 3A, B). The cirrus-sac is elongate, narrow, coiled
proximally and contains a long tubular coiled internal
seminal vesicle, a long narrow pars prostatica and a
muscular ejaculatory duct which widens distally
(Gibson, 1987). The external seminal vesicle is long,
tubular and coiled and merges into the internal seminal
vesicle. Gibson (1987) described a constriction of the
seminal vesicle as it enters the cirrus-sac but stated
that it was only seen in sections. We have not been able
to detect this constriction in whole-mounted worms. If
it is always present, it is obscured by the folds of the
seminal vesicle in the region dorsal to the ventral
sucker in all the specimens we examined. This folding
also usually obscures the precise posterior extent of
the cirrus-sac wall. Other distinguishing features,
Syst Parasitol (2018) 95:479–498
which are rare or absent in other lepocreadioids,
include a uroproct and a significant proportion of the
uterus in the forebody. At present, no other lepocreadioids appear to have characters in any way resembling those of specimens of Gibsonivermis.
The single species of Gibsonivermis is so far
known only from Moreton Bay and off Heron Island
491
on the southern Great Barrier Reef. Bray et al. (1999)
summarised the knowledge of the parasites of the
Sillaginidae and found that no ‘lepocreadiids’ were
reported outside Australian waters, but that in this
region a few unusual, apparently endemic, forms
occurred, namely species of Gibsonivermis, Austroholorchis Bray & Cribb, 1997 and Lepidapedella
Fig. 3 A, Gibsonivermis berryi (Gibson, 1987) ex Sillago ciliata. Holotype, ventral view, uterus in outline; B, Gibsonivermis berryi
(Gibson, 1987) ex Sillago analis. Male terminal genitalia, with ventral sucker and gut in outline. Scale-bars: A, 1,000 lm; B, 500 lm
123
492
Bray, Cribb & Pichelin, 1999. Austroholorchis is
now known to be an aephnidiogenid (see below).
Lepidapedella is an unusual worm, which likewise
does not agree well with any lepocreadioid family,
but shows no morphological similarities to G. berryi,
and was placed in the Lepidapedidae by Bray &
Cribb (2012). The species of endemic Australian
lepocreadioid genera which are not reported from
sillaginids include the lepocreadiids Amphicreadium
Bray & Cribb, 2001, Cliveus Bray & Cribb, 1997 and
Rugocavum Bray & Cribb, 1997, the lepidapedids
Harveytrema Kruse, 1979 and Scaphatrema Bray &
Cribb, 1997, and the unassigned Paraneocreadium
Kruse, 1978 and Jericho Bray & Cribb, 1997 (Kruse,
1978, 1979; Bray & Cribb, 1997a, 2001, 2012). None
of members of these genera exhibit any great
similarity to G. berryi, although the single species
of Paraneocreadium has some extension of the
uterus into the forebody and the testes are lobed
(Kruse, 1978, 1979; Bray & Cribb, 1997a). Considering the recognition that Gibsonivermis warrants a
separate family-level status within the Lepocreadioidea, the phylogenetic status of these other
distinctive, apparent ‘‘southern endemics’’, is of great
interest. Since 1999, only records of opecoelids and
transversotrematids have been added to the known
sillaginid digenean fauna (Aken’Ova, 2003; Aken’Ova et al., 2008; Cutmore et al., 2016).
Genus Gibsonivermis Bray, Cribb & Barker,
1997
Syst Parasitol (2018) 95:479–498
Remark
Gibson (1987) and Bray et al. (1997) reported this
species from the golden-line whiting Sillago analis
Whitley, S. ciliata and the trumpeter whiting S.
maculata Quoy & Gaimard, (Perciformes: Sillaginidae) from Moreton Bay. ITS2 rDNA data were
found to be identical for specimens of this species
infecting S. ciliata from Moreton Bay and off Heron
Island.
Family Aephnidiogenidae Yamaguti, 1934
Genus Austroholorchis Bray & Cribb, 1997
Austroholorchis sprenti (Gibson, 1987) Bray &
Cribb, 1997
Syn. Holorchis sprenti Gibson, 1987
Type-host: Sillago maculata Quoy & Gaimard (Perciformes: Sillaginidae), trumpeter whiting.
Type-locality: Deception Bay, Moreton Bay.
New records:
Host: Sillago ciliata Cuvier.
Locality: Off Dunwich, Moreton Bay (27°290 S,
153°230 E).
Voucher material: Seven specimens in the QM
G237284–90.
Representative DNA sequences: ITS2 rDNA, four
replicates (one in GenBank MH157065); 28S rDNA,
one sequence (GenBank MH157075).
Remarks
Gibsonivermis berryi (Gibson, 1987) Bray, Cribb &
Barker, 1997
Syn. Intusatrium berryi Gibson, 1987
Type-host: Sillago ciliata Cuvier (Perciformes: Sillaginidae), sand whiting.
Type-locality: Deception Bay, off Moreton Bay.
New record:
Host: Sillago ciliata.
Locality: Off Dunwich, Moreton Bay (27°290 S,
153°230 E).
Voucher specimens: Six specimens in the QM
G237291–6.
Representative DNA sequences: ITS2 rDNA, two
replicates (one in GenBank MH157060); 28S rDNA,
one sequence (GenBank MH157070).
123
Gibson (1987) and Bray & Cribb (1997b) reported this
species from Sillago analis, S. ciliata and S. maculata
from Moreton Bay. Analyses of the 28S data generated
during this study indicate that this species forms a
strongly-supported clade with all other included
aephnidiogenids. Within the aephnidiogenid clade,
A. sprenti formed a strongly-supported clade with
species of Aephnidiogenes Nicoll, 1915, Holorchis
Stossich, 1901 and Neolepocreadium Thomas, 1960,
sister to the two freshwater anguilliform-infecting
species Stegodexamene anguillae Watson, 1984 and
Tetracerasta blepta Watson, 1984.
Syst Parasitol (2018) 95:479–498
Phylogenetic results
Alignment of the 28S rDNA dataset (Table 2) yielded
1,299 characters (including indels). Deleted ambiguously aligned regions amounted to 49 bases (less than
4% of the alignment), resulting in a final dataset of
1,250 characters for phylogenetic analysis. Bayesian
inference and maximum likelihood analyses of the
28S rDNA dataset resulted in phylograms with almost
identical topologies (Fig. 2). Only the relationship
between the specimens of Diploproctodaeum monstrosum and Diploproctodaeum cf. monstrosum and
that between Lepidapedoides angustus Bray, Cribb &
Barker, 1996 and Preptetos caballeroi Pritchard 1960
were different. The topology was almost identical (but
expanded relative) to that found by Bray et al. (2009),
in which all lepocreadioid taxa formed a strongly
supported clade to the exclusion of cryptogonimid and
apocreadiid outgroup taxa. The now seven accepted
families each formed monophyletic clades, all of
which were strongly supported; nodal support for
relationships within the familial clades was lower,
especially for those in the lepocreadiid clade. The
type- and only species of the Gibsonivermidae formed
a well-supported clade with the lepidapedids. Most
genera for which there were more than one sequenced
species included formed monophyletic clades (Gorgocephalus Manter, 1966, Holorchis, Hypocreadium
Ozaki, 1936, Lepidapedon Stafford, 1904, Opechona,
Paragyliauchen Yamaguti, 1934 and Proenenterum
Manter, 1954), but several formed notably polyphyletic assemblages (Bianium, Diploproctodaeum
and Preptetos).
Discussion
Our phylogenetic hypotheses are inferred from the
phylogram generated from the 28S rDNA dataset, but
all are supported by morphology. This phylogram
includes the sequences used by Bray et al. (2009) and
Bray & Cribb (2012) in their reviews of the phylogeny
and systematics of lepocreadioids and allows us to set
the Moreton Bay worms in context. The uncontroversial results in the tree are the finding of identical
sequences for Neomultitestis aspidogastriformis and
Clavogalea trachinoti from off Heron Island and in
Moreton Bay and the near identical sequences for
Multitestis magnacetabulum from the same localities;
493
species of several other trematode families have been
shown to be genetically identical between the Great
Barrier Reef and Moreton Bay (Brooks et al., 2017;
Yong et al., 2018). More controversial is the close
molecular similarity of Opechona austrobacillaris
from Moreton Bay and O. kahawai from Tasmanian
waters, which brings into question the status of these
forms. Although morphologically similar, they do
appear to be readily distinguishable. Prodistomum
keyam, O. austrobacillaris and O. kahawai are
included in a moderately-supported clade, which is
poorly resolved internally. Preptetos trulla (Linton,
1907) is in this clade and is clearly not placed in the
correct genus given its distance from the type-species,
P. caballeroi Pritchard, 1960. Preptetos trulla, Prodistomum keyam, O. austrobacillaris and O. kahawai are
also similar morphologically.
Moreton Bay members of the similar, and controversially separated, genera Bianium and Diploproctodaeum formed a well-supported clade, but were
internally poorly resolved and clearly need greater
sampling, both of species and genes, for a convincing
arrangement to emerge. The morphological characteristics that are currently used to separate these genera
are evidently unreliable. The five-base difference in
sequences between D. monstrosum (‘Diploproctodaeum sp.’ in Bray et al., 2009) from off Lizard Island
and D. cf. monstrosum from Moreton Bay indicates
that there are potentially two closely related species in
Queensland waters. However, few specimens have
been collected from either location, and currently
there are not enough morphological or molecular data
to justify the proposal of a new species; this complex
needs further study.
Members of the Lepocreadiidae sensu stricto in
Moreton Bay were divided into two major clades
reflecting the findings reported by Bray et al. (2009),
who labelled the clades as VII and VIII. Clade VII
includes what might be considered ‘typical’ lepocreadiids, mostly occurring in shallow water and, as far as
is known, with a gastropod first intermediate host.
Clade VIII includes many species from reef fishes,
especially tetraodontiform fishes, with just one
resolved life-cycle which utilises a bivalve first
intermediate host (Hassanine, 2006). The distribution
of these clades in terms of their assemblage and the
nature of their hosts is worthy of further exploration,
but a much wider understanding of the genetic
123
494
Syst Parasitol (2018) 95:479–498
Table 2 Collection data and GenBank accession numbers for lepocreadioid species analysed in this study
Species
Host
GenBank
ID
References
Diagramma pictum labiosum
(Macleay)
FJ788468
Bray et al. (2009)
Lepocreadioidea
Aephnidiogenidae Yamaguti, 1934
Aephnidiogenes major Yamaguti, 1934
Austroholorchis sprenti (Gibson, 1987)
Sillago ciliata Cuvier
MH157075
Present study
Holorchis castex Bray & Justine, 2007
Diagramma pictum pictum
(Thunberg)
FJ788476
Bray et al. (2009)
Holorchis gigas Bray & Cribb, 2007
Plectorhinchus chrysotaenia
(Bleeker)
FJ788477
Bray et al. (2009)
Neolepocreadium caballeroi Thomas, 1960
Trachinotus blochii (Lacépède)
FJ788488
Bray et al. (2009)
Stegodexamene anguillae Macfarlane, 1951
Gobiomorphus cotidianus McDowall
KF484005
Herrmann et al.
(2014)
Tetracerasta blepta Watson, 1984
Posticobia brazieri (Smith)
FJ788494
Bray et al. (2009)
Enenterum aureum Linton, 1910
Kyphosus vaigiensis (Quoy &
Gaimard)
AY222232
Olson et al. (2003)
Koseiria xishaensis Gu & Shen, 1983
Kyphosus vaigiensis
AY222233
Olson et al. (2003)
Proenenterum ericotylum Manter, 1954
Aplodactylus arctidens Richardson
FJ788499
Bray et al. (2009)
Proenenterum isocotylum Manter, 1954
Aplodactylus arctidens
FJ788500
Bray et al. (2009)
Sillago ciliata
MH157070
Present study
Enenteridae Yamaguti, 1958
Gibsonivermidae n. fam.
Gibsonivermis berryi (Gibson, 1987)
Gorgocephalidae Manter, 1966
Gorgocephalus kyphosi Manter, 1966
Kyphosus vaigiensis
AY222234
Olson et al. (2003)
Gorgocephalus yaaji Bray & Cribb, 2005
Kyphosus cinerascens (Forsskål)
KU951489
Huston et al.
(2016)
Gorgocephalus sp.
Austrolittorina unifasciata (Gray)
KU951485
Huston et al.
(2016)
Bray et al. (2009)
Gyliauchenidae Fukui, 1929
Affecauda annulata Hall & Chambers, 1999
Naso tuberosus Lacépède
FJ788501
Paragyliauchen arusettae Machida, 1984
Pomacanthus sexstriatus (Cuvier)
FJ788503
Bray et al. (2009)
Paragyliauchen sp.
Centropyge bicolor (Bloch)
FJ788502
Bray et al. (2009)
Petalocotyle adenometra Hall & Cribb, 2000
Prionurus microlepidotus Lacépède
FJ788504
Bray et al. (2009)
Robphildollfusium fractum (Rudolphi, 1819)
Sarpa salpa (Linnaeus)
FJ788505
Bray et al. (2009)
MH157076
Present study
Bianium plicitum (Linton, 1928)
Lagocephalus lunaris (Bloch &
Schneider)
Torquigener pleurogramma (Regan)
MH157066
Present study
Clavogalea trachinoti (Fischthal & Thomas, 1968)
Trachinotus coppingeri Günther
MH157067
Present study
Diplocreadium tsontso Bray, Cribb & Barker, 1996
Balistoides conspicillum (Bloch &
Schneider)
FJ788472
Bray et al. (2009)
Diploproctodaeum momoaafata Bray, Cribb & Barker,
1996
Ostracion cubicus Linnaeus
FJ788474
Bray et al. (2009)
Diploproctodaeum monstrosum Bray, Cribb & Justine,
2010
Arothron stellatus (Anonymous)
FJ788473
Bray et al. (2009)
Diploproctodaeum cf. monstrosum
Arothron hispidus (Linnaeus)
MH157069
Present study
Echeneidocoelium indicum Simha & Pershad, 1964
Echeneis naucrates Linnaeus
FJ788475
Bray et al. (2009)
Lepocreadiidae Odhner, 1905
Bianium arabicum Sey, 1996
123
Syst Parasitol (2018) 95:479–498
495
Table 2 continued
Species
Host
GenBank
ID
References
Hypocreadium patellare Yamaguti, 1938
Balistoides viridescens (Bloch &
Schneider)
FJ788478
Bray et al. (2009)
Hypocreadium picasso Bray, Cribb & Justine, 2009
Rhinecanthus aculeatus (Linnaeus)
FJ788479
Bray et al. (2009)
Hypocreadium toombo Bray & Justine, 2006
Pseudobalistes fuscus (Bloch &
Schneider)
FJ788480
Bray et al. (2009)
Lepidapedoides angustus Bray, Cribb & Barker, 1996
Epinephelus cyanopodus
(Richardson)
FJ788482
Bray et al. (2009)
Lepotrema clavatum Ozaki, 1932
Acanthochromis polyacanthus
(Bleeker)
FJ788483
Bray et al. (2009)
Lobatocreadium exiguum (Manter, 1963)
Pseudobalistes fuscus
FJ788484
Bray et al. (2009)
Mobahincia teirae n. g., n. sp.
Platax teira (Forsskål)
MH157068
Present study
Multitestis magnacetabulum Mamaev, 1970
Platax teira
MH157071
Present study
Neohypocreadium dorsoporum Machida & Uchida, 1987
Chaetodon flavirostris Günther
FJ788487
Bray et al. (2009)
Neomultitestis aspidogastriformis Bray & Cribb, 2003
Platax teira
MH157072
Present study
Neopreptetos arusettae Machida, 1982
Opechona austrobacillaris Bray & Cribb, 1998
Pomacanthus sexstriatus
Pomatomus saltatrix Linnaeus
FJ788490
MH157073
Bray et al. (2009)
Present study
Opechona kahawai Bray & Cribb, 2003
Arripis trutta (Forster)
FJ788491
Bray et al. (2009)
Pelopscreadium spongiosum (Bray & Cribb, 1998)
Ostracion cubicus
FJ788469
Bray et al. (2009)
Preptetos caballeroi Pritchard, 1960
Naso vlamingii (Valenciennes)
AY222236
Olson et al. (2003)
Preptetos trulla (Linton, 1907)
Ocyurus chrysurus (Bloch)
AY222237
Olson et al. (2003)
Prodistomum keyam Bray & Cribb, 1996
Monodactylus argenteus (Linnaeus)
MH157074
Present study
Lepidapedidae Yamaguti, 1958
Bulbocirrus aulostomi Yamaguti, 1965
Aulostomus chinensis (Linnaeus)
FJ788470
Bray et al. (2009)
Intusatrium robustum Durio & Manter, 1968
Bodianus perditio (Quoy &
Gaimard)
FJ788481
Bray et al. (2009)
Lepidapedon beveridgei Campbell & Bray, 1993
Coryphaenoides armatus (Hector)
AJ405263
Bray et al. (2009)
Lepidapedon desclersae Bray & Gibson, 1995
Lepidapedon discoveryi Bray & Gibson, 1995
Mora moro (Risso)
Coryphaenoides armatus
AJ405264
AJ405265
Bray et al. (1999)
Bray et al. (1999)
Lepidapedon elongatum (Lebour, 1908)
Gadus morhua Linnaeus
AJ405266
Bray et al. (1999)
Lepidapedon gaevskayae Campbell & Bray, 1993
Coryphaenoides armatus
AJ405267
Bray et al. (1999)
Lepidapedon rachion (Cobbold, 1858)
Gadus morhua
AJ405260
Bray et al. (1999)
Lepidapedon sommervillae Bray & Gibson, 1995
Coryphaenoides guentheri (Vaillant)
AJ405268
Bray et al. (1999)
Lepidapedon zubchenkoi Campbell & Bray, 1993
Coryphaenoides leptolepis Günther
AJ405269
Bray et al. (1999)
Myzoxenus insolens (Crowcroft, 1945)
Notolabrus tetricus (Richardson)
FJ788486
Bray et al. (2009)
Neolepidapedon smithi Bray & Gibson, 1989
Mora moro
AJ405270
Bray et al. (1999)
Postlepidapedon opisthobifurcatum (Zdzitowiecki, 1990)
Muraenolepis marmorata Günther
KY497957
Sokolov et al.
(2018)
Postlepidapedon uberis Bray, Cribb & Barker, 1997
Choerodon venustus (De Vis)
FJ788492
Bray et al. (2009)
Profundivermis intercalarius Bray & Gibson, 1991
Coryphaenoides armatus
AJ405271
Bray et al. (1999)
Lepomis microlophus (Günther)
AY222241
Olson et al. (2003)
Outgroup taxa
Apocreadiidae Skrjabin, 1942
Homalometron armatum (MacCallum, 1895)
Neoapocreadium splendens Cribb & Bray, 1999
Scolopsis monogramma (Cuvier)
AY222242
Olson et al. (2003)
Paraschistorchis zancli (Hanson, 1953)
Zanclus cornutus (Linnaeus)
AY222240
Olson et al. (2003)
Cryptogonimidae Ward, 1917
123
496
Syst Parasitol (2018) 95:479–498
Table 2 continued
Species
Host
GenBank
ID
References
Adlardia novaecaledoniae Miller, Bray, Goiran, Justine &
Cribb, 2009
Nemipterus furcosus (Valenciennes)
FJ788496
Bray et al. (2009)
Caecincola parvulus Marshall & Gilbert, 1905
Micropterus salmoides (Lacépède)
AY222231
Olson et al. (2003)
structuring of this diverse family is needed before such
an analysis can be completed.
The new status of Gibsonivermis, as the type-genus
for a monotypic family, has been argued above. This
new status is consistent with the observations of Cribb
& Bray (2011) that new trematode families are now
principally recognised from among known taxa rather
than as a result of completely new discoveries. We
suspect that further genetic exploration of unique
trematode taxa will likely lead to more families being
proposed within the Lepocreadioidea.
Acknowledgements We thank John Page and Dave
Thompson for their assistance in the collection of fishes in
Moreton Bay, and all members of the Marine Parasitology
Research Group at the University of Queensland for assistance
with dissections.
Funding RAB, 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.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original
author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
References
Aken’Ova, T. O. (2003). A new species of Podocotyloides
Yamaguti, 1934 (Digenea: Opecoelidae) from a Western
123
Australian temperate marine fish. Systematic Parasitology,
55, 127–133.
Aken’Ova, T. O., Cribb, T. H., & Bray, R. A. (2008). Eight new
species of Macvicaria Gibson and Bray, 1982 (Digenea:
Opecoelidae) mainly from endemic temperate marine
fishes of Australia. ZooKeys, 1, 23–58.
Ankenbrand, M. J., Keller, A., Wolf, M., Schultz, J., & Förster,
F. (2015). ITS2 Database V: Twice as much. Molecular
Biology and Evolution, 32, 3030–3032.
Barker, S. C., Blair, D., Garrett, A. R., & Cribb, T. H. (1993).
Utility of the D1 domain of nuclear 28S rRNA for phylogenetic inference in the Digenea. Systematic Parasitology,
26, 181–188.
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, 295–306.
Bray, R. A. (2005). Family Lepocreadiidae Odhner, 1905. In:
Jones, A., Bray, R. A. & Gibson, D. I. (Eds), Keys to the
Trematoda. Volume 2. Wallingford: CABI Publishing and
The Natural History Museum, pp. 545–602.
Bray, R. A., & Cribb, T. H. (1996). Two species of Prodistomum
Linton, 1910 (Digenea: Lepocreadiidae) from marine
fishes of Australia. Systematic Parasitology, 35, 59–67.
Bray, R. A., & Cribb, T. H. (1997a). Lepocreadiid (Digenea)
species from members of the marine teleost family
Cheilodactylidae from south-western Australia, including
four new genera and five new species. Systematic Parasitology, 37, 27–45.
Bray, R. A., & Cribb, T. H. (1997b). The subfamily Aephnidiogeninae Yamaguti, 1934 (Digenea: Lepocreadiidae), its
status and that of the genera Aephnidiogenes Nicoll, 1915,
Holorchis Stossich, 1901, Austroholorchis n. g., Pseudaephnidiogenes Yamaguti, 1971, Pseudoholorchis Yamaguti, 1958 and Neolepocreadium Thomas, 1960.
Systematic Parasitology, 36, 47–68.
Bray, R. A., & Cribb, T. H. (1998). Lepocreadiidae (Digenea) of
Australian coastal fishes: new species of Opechona Looss,
1907, Lepotrema Ozaki, 1932 and Bianium Stunkard, 1930
and comments on other species reported for the first time or
poorly known in Australian waters. Systematic Parasitology, 41, 123–148.
Bray, R. A., & Cribb, T. H. (2001). Amphicreadium n. g. (Digenea: Lepocreadiidae) from monacanthid fishes (Tetraodontiformes) from the coast of northern Tasmania.
Systematic Parasitology, 49, 205–209.
Bray, R. A., & Cribb, T. H. (2003a). Lepocreadiidae (Digenea)
from the batfish of the genus Platax Cuvier (Teleostei:
Ephippidae) from the southern Great Barrier Reef,
Queensland, Australia. Systematic Parasitology, 55, 1–9.
Syst Parasitol (2018) 95:479–498
Bray, R. A., & Cribb, T. H. (2003b). New species of Opechona
Looss, 1907 and Cephalolepidapedon Yamaguti, 1970
(Digenea: Lepocreadiidae) from fishes off northern Tasmania. Papers and Proceedings of the Royal Society of
Tasmania, 137, 1–5.
Bray, R. A., & Cribb, T. H. (2012). Reorganisation of the
superfamily Lepocreadioidea Odhner, 1905 based on an
inferred molecular phylogeny. Systematic Parasitology,
83, 169–177.
Bray, R. A., Cribb, T. H., & Barker, S. C. (1997). Postlepidapedon Zdzitowiecki, 1993 and Gibsonivermis n. g. (Digenea: Lepocreadiidae) from fishes of the southern Great
Barrier Reef, Australia, and their relationship to Intusatrium Durio & Manter, 1968. Systematic Parasitology,
36, 143–155.
Bray, R. A., Cribb, T. H., & Justine, J.-L. (2010a). Diploproctodaeum spp. (Digenea, Lepocreadiidae) in Australian and
New Caledonian waters including two new species from
Tetraodontiformes and new records of related species. Acta
Parasitologica, 55, 313–326.
Bray, R. A., Cribb, T. H., & Justine, J.-L. (2010b). Multitestis
Manter 1931 (Digenea: Lepocreadiidae) in ephippid and
chaetodontid fishes (Perciformes) in the south-western
Pacific Ocean and the Indian Ocean off Western Australia.
Zootaxa, 2427, 36–46.
Bray, R. A., Cribb, T. H., & Pichelin, S. P. (1999). Two new
species of lepidapedines (Digenea, Lepocreadiidae) from
the King George whiting Sillaginodes punctata (Perciformes, Sillaginidae) from off Kangaroo Island, South
Australia. Acta Parasitologica, 44, 108–114.
Bray, R. A., & Gibson, D. I. (1990). The Lepocreadiidae (Digenea) of fishes of the north-east Atlantic: review of the
genera Opechona Looss, 1907 and Prodistomum Linton,
1910. Systematic Parasitology, 15, 159–202.
Bray, R. A., & Justine, J.-L. (2012). A review of the Lepocreadiidae (Digenea, Lepocreadioidea) from fishes of the
waters around New Caledonia. Acta Parasitologica, 57,
247–272.
Bray, R. A., Waeschenbach, A., Cribb, T. H., Weedall, G. D.,
Dyal, P., & Littlewood, D. T. J. (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.
Brooks, X., Cribb, T. H., Yong, R. Q.-Y., & Cutmore, S. C.
(2017). A re-evaluation of diversity of the Aporocotylidae
Odhner, 1912 in Siganus fuscescens (Houttuyn) (Perciformes: Siganidae) and associated species. Systematic
Parasitology, 94, 717–737.
Cribb, T. H., Anderson, G. R., Adlard, R. D., & Bray, R. A.
(1998). A DNA-based demonstration of a three-host lifecycle for the Bivesiculidae (Platyhelminthes: Digenea).
International Journal for Parasitology, 28, 1791–1795.
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, 1–7.
Cribb, T. H., & Bray, R. A. (2011). Trematode families and
genera: have we found them all? Trends in Parasitology,
27, 149–154.
497
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, 639–652.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012).
jModelTest 2: more models, new heuristics and parallel
computing. Nature Methods, 9, 772.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment
with high accuracy and high throughput. Nucleic Acids
Research, 32, 1792–1797.
Gibson, D. I. (1987). Two new lepocreadiids (Digenea) from
Sillago spp. (Pisces: Sillaginidae) in Australian waters.
Journal of Natural History, 21, 159–166.
Hafeezullah, M. (1970). Lepocreadid trematodes of marine
fishes of India. Parasitology, 61, 345–356.
Hassanine, R. M. E.-S. (2006). The life cycle of Diploproctodaeum arothroni Bray and Nahhas, 1998 (Digenea:
Lepocreadiidae), with a comment on the parasitic castration of its molluscan intermediate host. Journal of Natural
History, 40, 1211–1222.
Herrmann, K. K., Poulin, R., Keeney, D. B., & Blasco-Costa, I.
(2014). Genetic structure in a progenetic trematode: signs
of cryptic species with contrasting reproductive strategies.
International Journal for Parasitology, 44, 811–818.
Huston, D. C., Cutmore, S. C., & Cribb, T. H. (2016). The lifecycle 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.
ICZN (2012). International Commission on Zoological
Nomenclature: Amendment of articles 8, 9, 10, 21 and 78
of the International Code of Zoological Nomenclature to
expand and refine methods of publication. Bulletin of
Zoological Nomenclature, 69, 161–169.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M.,
Sturrock, S., et al. (2012). Geneious Basic: an integrated
and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28,
1647–1649.
Keller, A., Schleicher, T., Schultz, J., Müller, T., Dandekar, T.,
& Wolf, M. (2009). 5.8S-28S rRNA interaction and HMMbased ITS2 annotation. Gene, 430, 50–57.
Kruse, G. O. W. (1978). Trematodes of marine fishes from South
Australia. 1. Paraneocreadium australiense gen. et sp. n.
(Lepocreadiidae). Journal of Parasitology, 64, 398–400.
Kruse, G. O. W. (1979). Trematodes of marine fishes from South
Australia. 4. Harveytrema bisulcatum gen. et sp. n. (Lepocreadiidae). Journal of Parasitology, 65, 918–920.
Linton, E. (1928). Notes on trematode parasites of birds. Proceedings of the United States National Museum, 73, 1–36.
Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped
oysters based on partial 28S rRNA gene sequences.
Molecular Phylogenetics and Evolution, 3, 221–229.
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.
Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species?
123
498
Phylogenetic evidence from site-specific polystome
monogeneans. International Journal for Parasitology, 27,
1289–1297.
Machida, M. (1982). Lepocreadiid trematodes from marine
fishes of Palau. Proceedings of the Japanese Society of
Systematic Zoology, 23, 1–11.
Maddison, W. P., & Maddison, D. R. (2017). Mesquite: a
modular system for evolutionary analysis. Version 3.01
http://mesquiteproject.org.
Mamaev, Y. L. (1970). [Helminths of some commercial fishes in
the Gulf of Tong King.] In: Oshmarin, P. G., Mamaev, Y.
L. & Lebedev, B. I. (Eds), Helminths of Animals of SouthEast Asia. Moscow: Izdatel’stvo Nauka, pp. 127–190 (In
Russian).
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.
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, 609–615.
Olson, P. D., 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, 733–755.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L.,
Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient
Bayesian phylogenetic inference and model choice across a
large model space. Systematic Biology, 61, 539–542.
123
Syst Parasitol (2018) 95:479–498
Sey, O. (1996). Description of Bianium arabicum sp. n. (Trematoda, Lepocreadiidae) from the pufferfish, Lagocephalus lunaris (Bloch et Schneider, 1801) in Kuwait and
a review of the genus Bianium Stunkard, 1930. Parasitologia Hungarica, 28, 13–20.
Shen, J.-W., & Tong, Y.-Y. (1990). Studies on the digenetic
trematodes of fishes from the Daya Bay (Trematoda). Acta
Zootaxonomica Sinica, 15, 385–392 (In Chinese).
Snyder, S. D., & Tkach, V. V. (2001). Phylogenetic and biogeographical relationships among some Holarctic frog lung
flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–1440.
Sokolov, S. G., Khasanov, F. K., & Gordeev, I. I. (2018). New
data on the morphology and phylogenetic connections of
Postlepidapedon
opisthobifurcatum
(Trematoda,
Lepocreadioidea: Lepidapedidae), a parasite of Antarctic
and sub-Antarctic fishes. Helminthologia, 55, 95–101.
Stamatakis, A. (2014). RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies.
Bioinformatics, 30, 1312–1313.
Sun, D., Bray, R. A., Yong, R. Q., Cutmore, S. C., & Cribb, T. H.
(2014). Pseudobacciger cheneyae n. sp. (Digenea:
Gymnophalloidea) from Weber’s chromis (Chromis
weberi Fowler & Bean) (Perciformes: Pomacentridae) at
Lizard Island, Great Barrier Reef, Australia. Systematic
Parasitology, 88, 141–152.
Yong, R. Q.-Y., Cutmore, S. C., Jones, M. K., Gauthier, A.
R. G., & Cribb, T. H. (2018). A complex of the blood fluke
genus Psettarium (Digenea: Aporocotylidae) infecting
tetraodontiform fishes of east Queensland waters. Parasitology International, 67, 321–340.