Syst Parasitol (2014) 88:195–211 DOI 10.1007/s11230-014-9499-y

Monorchiid trematodes of the painted sweetlips, Diagramma labiosum (Perciformes: Haemulidae), from the southern Great Barrier Reef, including a new genus and three new species Emily L. Searle • Scott C. Cutmore Thomas H. Cribb

Received: 5 May 2014 / Accepted: 16 May 2014 Ó Springer Science+Business Media Dordrecht 2014

Abstract Five monorchiid species are reported from Diagramma labiosum Macleay (Perciformes: Haemulidae) collected from Heron Island on the southern Great Barrier Reef (GBR): two described species, Helicometroides longicollis Yamaguti, 1934 and Diplomonorchis kureh Machida, 2005 and three new species, including one new genus, Asymmetrostoma heronensis n. g., n. sp., Lasiotocus arrhichostoma n. sp. and Proctotrema addisoni n. sp. Helicometroides longicollis and D. kureh were previously reported from the closely related species Diagramma pictum (Thunberg) from Japan. Two further monorchiid species known from D. pictum, Genolopa plectorhynchi (Yamaguti, 1934) and Paraproctotrema fusiforme Yamaguti, 1934, appear to be absent from the southern Great Barrier Reef. Previous reports of two other monorchiids from D. labiosum from the GBR, Paramonorcheides pseudocaranxi Dove & Cribb, 1998 and Helicometroides vitellosus (Durio & Manter, 1968), are shown to have been made in error. The high richness of monorchiids and other trematode families in D. labiosum is consistent with that seen in other haemulids elsewhere.

E. L. Searle  S. C. Cutmore  T. H. Cribb (&) School of Biological Sciences, The University of Queensland, Brisbane, QLD, Australia e-mail: [email protected]

Introduction Haemulids are widespread tropical fishes, found in the Atlantic, Pacific and Indian Oceans (Froese & Pauly, 2014). Ten species are known from the Great Barrier Reef (GBR) and the Coral Sea (Randall et al., 1997). Diagramma labiosum Macleay, the subject of this study, is found on the inner and middle reefs of the GBR (Johnson et al., 2001). This species was formerly known as Diagramma pictum (Thunberg) on the GBR, but has become recognised as D. labiosum on the basis of colouration and distributional differences relative to D. pictum sensu stricto (see Johnson et al., 2001). Johnson et al. (2001) recognised the current name as a subspecies, D. pictum labiosum. Although it has never formally been raised to the species level, most current literature refers to this fish as a distinct species, D. labiosum, and this approach is followed here. The trematode fauna of D. labiosum on the GBR is yet to be comprehensively described, although eight species have been reported thus far from five families: Aephnidiogenidae Yamaguti, 1934, Cryptogonimidae Ward, 1917, Monorchiidae Odhner, 1911, Opecoelidae Ozaki, 1925 and Transversotrematidae Witenberg, 1944. Unpublished preliminary examinations suggested that this species is infected with multiple further species of Monorchiidae on the GBR. There are currently four monorchiid species reported from haemulids of tropical Queensland waters: Lasiotocus cacuminatus (Nicoll, 1915) Thomas, 1959 and L. trifolifer (Nicoll, 1915) Thomas, 1959 [both reported



from Pomadasys argenteus (Forsska˚l) by Nicoll (1915)] and Helicometroides vitellosus (Durio & Manter, 1968) and Paramonorcheides pseudocaranxi Dove & Cribb, 1998 [both from Diagramma labiosum, by Durio & Manter (1968) and Dove & Cribb (1998), respectively]. This study further explores the monorchiids of D. labiosum on the southern Great Barrier Reef.

Syst Parasitol (2014) 88:195–211 Table 1 28S rDNA sequence data from GenBank included in phylogenetic analyses GenBank accession number


Cableia pudica Bray, Cribb & Barker, 1996 Diplomonorchis leiostomi Hopkins, 1941


Olson et al. (2003) Olson et al. (2003)

Materials and methods

Lasiotocus typicum (Nicoll, 1912)


Olson et al. (2003)

Specimen preparation and morphological analysis Fishes were caught by line and spear fishing at Heron Island (23°260 S, 151°540 E) on the southern Great Barrier Reef from 1989 to 2005. Trematodes were collected and processed as described by Cribb & Bray (2010). Specimens were preserved in 10% formalin for morphological examination and 100% ethanol for molecular analysis. Specimens for morphological analysis were processed and analysed as described by Cribb et al. (2014). Measurements are in micrometres (lm) and are presented as a range, followed by a mean in parentheses. Where the number of specimens measured for a given morphological feature is fewer than 10, the number measured (n) is given in parentheses. Where length is followed by breadth, the two measurements are separated by ‘9’. All type and voucher specimens are lodged in the Queensland Museum (QM), Brisbane, Australia.

Monorchis monorchis (Stossich, 1890) Provitellus turrum Dove & Cribb, 1998


Tkach et al. (2001) Olson et al. (2003)

DNA sequencing All specimens characterised genetically in this study were collected from D. labiosum from off Heron Island, Queensland Australia. Specimens for molecular analysis were processed according to the protocols used by Cribb et al. (2014). Cycle sequencing was carried out for the partial 28S rDNA region using the primers LSU5, 300F, ECD2, 1200R and 1500R and for the ITS2 rDNA region using 3S, GA1 and ITS2.2 (see Cutmore et al., 2013). Phylogenetic analyses The partial 28S rDNA sequences generated during this study were aligned with those for species of Monorchiidae available on GenBank (Table 1) using MUSCLE version 3.7 (Edgar, 2004) with ClustalW sequence weighting and UPGMA clustering for



Family Monorchiidae



Outgroup Taxa Lissorchis kritskyi Barnhart & Powell, 1979


Curran et al. (2006)

iterations 1 and 2. The resultant alignment was refined by eye using MESQUITE (Maddison & Maddison, 2009) and the ends of each fragment were trimmed to match the shortest sequence in the alignment. Bayesian inference and Maximum Likelihood analyses of the 28S rDNA dataset were conducted to explore relationships among these taxa. Bayesian inference analysis was performed using MrBayes version 3.2.2 (Ronquist et al., 2012), run on the CIPRES portal (Miller et al., 2010). Maximum Likelihood analysis was performed using RAxML version 7.2.8 (Stamatakis et al., 2008). The software jModelTest version 0.1.1 (Posada, 2008) was used to estimate the best nucleotide substitution model for the dataset. Bayesian inference analysis was conducted using the GTR?G model predicted as the best estimator by the Akaike Information Criterion (AIC) in jModelTest. The closest approximation of this model was implemented in the subsequent Maximum Likelihood analysis. 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 (samplefreq = 1,000). Bayesian analysis used the following parameters: nst = 6, rates = gamma, ngammacat = 4, and the priors parameters of the combined dataset were set to ratepr = variable. Samples of substitution model parameters,

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and tree and branch lengths were summarised using the parameters ‘sump burnin = 3,000’ and ‘sumt burnin = 3,000’. These ‘burnin’ parameters were chosen because the log likelihood scores ‘stabilised’ well before 3,000,000 replicates in the Bayesian inference analyses. Nodal support in the Maximum Likelihood analysis was estimated by performing 100 bootstrap pseudoreplicates. A species of Lissorchiidae Magath, 1917 was designated as the functional outgroup.

Results Monorchiids were collected from 22 individuals of D. labiosum from Heron Island. Morphological analysis revealed five distinct morphotypes. Of these, two are interpreted as described species and the remaining three are proposed as new, including one new genus. Monorchiidae Odhner, 1911 Hurleytrematinae Yamaguti, 1958 Helicometroides Yamaguti, 1934 Helicometroides longicollis Yamaguti, 1934 Syn. Hysterorchis vitellosus Durio & Manter, 1968 in part Type-host: Plectorhinchus pictus [Authority not given, see below] (Perciformes: Haemulidae). Type-locality: Off Tarumi, Japan (34°380 N, 135°30 E). New material Host: Diagramma labiosum Macleay (Perciformes: Haemulidae). Locality: Off Heron Island, Queensland, Australia (23°260 S, 151°540 E). Site in host: Intestine. Prevalence: 15 of 22 (68%). Deposition of specimens: 14 voucher specimens (QM G234433–46) lodged in the QM. Molecular sequence data: 28S rDNA, 1 replicate (KJ658287); ITS2 rDNA, 3 replicates (1 submitted KJ658288).


(1,251 9 221). Length/width ratio 3.98–6.85 (5.66): 1. Tegument spined. Forebody 383–1,101 (719) long, occupying 51–67 (60%) of body length. Hindbody 194–687 (450) long. Oral sucker opens ventro-subterminally, spherical to sub-spherical, 30–76 9 38–83 (63 9 63). Ventral sucker in middle third of body, 40–92 (63) in diameter. Oral sucker width to ventral sucker width ratio 1: 0.76–1.39 (0.95). Prepharynx distinct, 85–297 (136) long. Pharynx distinctly smaller than oral sucker, 31–64 9 27–61 (44 9 37). Oesophagus distinct, long, 221–485 (343) in length. Caeca blind, with ends typically obscured by eggs; postcaecal region occupying 19–23 (21)% of body length (n = 3) (Fig. 2). Post-testicular region 55–112 (75) long, occupying 3–10 (6)% of body length. Testes entire, symmetrical, 88–225 9 32–114 (155 9 68). Cirrus-sac extends from mid-way between ventral sucker and testes to mid-way between intestinal bifurcation and ventral sucker before recurving to open into genital atrium sinistrally at level of anterior margin of ventral sucker; maximum measurable (straight-line) length 189–384 (272). Internal seminal vesicle twochambered; posterior chamber larger than anterior chamber. Pars prostatica distinct; prostatic cells not distinct. Eversible ejaculatory duct (cirrus) 46–101 (62) long (n = 7), armed with small spines appearing as pavement-like texture lining duct (Fig. 3). Genital atrium unspined. Common genital pore sinistral, at level of anterior margin of ventral sucker. Ovary deeply lobed, ranging from postero-sinistral to antero-sinistral to ventral sucker, 108–215 9 39–123 (149 9 72). Vitellarium comprising dense lateral follicles extending from just posterior to intestinal bifurcation to level of testes, confluent only in forebody and posterior region of hindbody, separate in mid-body and anterior region of hindbody. Uterus restricted to hindbody, extends posteriorly to level of middle of testes in three or more major broadly spiral coils. Terminal organ unipartite (a straight continuation of the uterus without any diverticulum of any sort), long, without spines. Egg capsules with single long filament; central capsule 23–35 9 11–20 (29 9 16). Excretory vesicle I-shaped, extends to between testes in mid-hindbody. Excretory pore terminal.

Description (Figs. 1–3) Remarks [Measurements based on 59 unflattened, whole mount specimens.] Body elongate, spindle-shaped, with maximum width in hindbody, 685–1,805 9 100–454

In its possession of two symmetrical testes at the posterior end of the body, a follicular vitellarium, a



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Figs. 1–3 Helicometroides longicollis Yamaguti, 1934 ex Diagramma labiosum from Heron Island, line drawings. 1. Whole mount, ventral view. 2. Whole mount, ventral view, showing position of caeca and testes. 3. Terminal genitalia, ventral view. Scale-bars: 1–3, 200 lm


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spiralled uterus not extending posteriorly beyond the testes, and filamented eggs, the present species is in clear agreement with Helicometroides Yamaguti, 1934 as presently recognised by Madhavi (2008). Five species are currently recognised in the genus: H. longicollis Yamaguti, 1934 (type-species), H. atlanticus (Gaevskaya & Aljoshkina, 1983), H. leiperi (Ahmad, 1982), H. pseudovitellosus (Madhavi, 1974) and H. vitellosus (Durio & Manter, 1968). Of these, three are immediately clearly distinct from the present material. Helicometroides atlanticus and H. vitellosus have vitelline follicles extending well anterior to the intestinal bifurcation whereas in the present form they do not reach that level. In H. leiperi the vitelline follicles terminate posteriorly well anterior to the testes, rather than overlapping them as in the present material. The present specimens resemble H. longicollis as originally described from Plectorhinchus pictus from off Japan by Yamaguti (1934). Unusually for Yamaguti’s studies, an authority was not given for ‘‘Plectorhynchus pictus’’. This creates an identification problem in that it is unclear whether the record is from the species that is now known as Diagramma pictum (Thunberg) or Plectorhinchus pictus (Tortonese), both of which occur in the general area from which Yamaguti reported H. longicollis (see Froese & Pauly, 2014). In the absence of other evidence, we predict that the host was D. pictum on the basis of the close relationship of that species to D. labiosum, but the matter remains unresolved. Certainly the morphology of the present specimens, in particular the long prepharynx, the distribution of the vitelline follicles, the position of the testes, the conformation of the ovary and the distinctively spiral uterus, is strongly consistent with H. longicollis. Yamaguti (1934) provided measurements for only one flattened specimen. This was recorded as being 2 mm long which exceeds all the specimens examined here which reached only 1,805 lm in length. Measurements for other body features were similarly slightly larger in Yamaguti’s specimens than recorded here. The larger measurements of Yamaguti (1934) are here attributed to the flattening of his specimen. Given the general similarity of the specimens we conclude that the present specimens are reliably identified as H. longicollis. As with many such identifications, ultimately, molecular testing of the identity of the species involved will be necessary.


The present material also generally resembles H. pseudovitellosus reported by Madhavi (1974) from a ‘‘Lutianus sp.’’ (Lutjanidae) from off India in being less elongate and in having the ovary less elongate and more posterior than is typical in the present material. However, it is possible that some of these differences relate to the fact that Madhavi’s specimens were flattened. The host reported for H. pseudovitellosus requires confirmation. This is the only record of a species of Helicometroides from a lutjanid, whereas most records are from haemulids. Some of the less colourful haemulids (especially Diagramma spp.) resemble lutjanids and it seems at least possible that the host was actually a haemulid. It is thus possible that this species will to be a junior synonym of H. longicollis. Although Durio & Manter (1968) described H. vitellosus from off New Caledonia from an unidentified species of Plectorhinchus as the type-host, they also reported the species from Plectorhinchus pictus, now known as Diagramma labiosum, from off Heron Island (the source of the current specimens). Dr Scott Gardner of the Manter Museum (Nebraska, United States) kindly sent photographs of the specimens of this species lodged by Manter which reveal that two species are involved. The first, from off New Caledonia, is consistent with H. vitellosus as figured by Durio & Manter (1968) from there. The second, the material from off Heron Island, is consistent with the present specimens from the Great Barrier Reef. We therefore conclude that H. vitellosus is not presently known from Australian waters. Monorchiinae Odhner, 1911 Diplomonorchis Hopkins, 1941 Diplomonorchis kureh Machida, 2005 Type-host: Diagramma pictum Thunberg (Perciformes: Haemulidae). Type-locality: Off Amamiooshima, Kagoshima Prefecture, Japan (28°170 N, 129°230 E). New material Host: Diagramma labiosum Macleay (Perciformes: Haemulidae). Locality: Off Heron Island, Queensland, Australia (23°260 S, 151°540 E). Site in host: Intestine. Prevalence: 12 of 22 (55%).



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Figs. 4–5 Diplomonorchis kureh Machida, 2005 ex Diagramma labiosum from off Heron Island, line drawings. 4. Whole mount, ventral view. 5. Terminal genitalia, ventral view. Scale-bars: 4, 100 lm; 5, 50 lm

Deposition of specimens: 14 voucher specimens (QM G234447–60) lodged in the QM. Description (Figs. 4–5) [Measurements based on 25 unflattened, whole mount specimens.] Body ovoid, 372–656 9 222–355 (491 9 278). Length/width ratio 1.51–2.01 (1.77): 1. Tegu-


ment spinose. Forebody 158–251 (202) long (n = 5), occupying 40–48 (44)% of body length (n = 5). Hindbody 189–231 (202) long (n = 5). Oral sucker opens ventro-subterminally, spherical to sub-spherical, 31–91 9 84–121 (71 9 102). Ventral sucker smaller than oral sucker, in mid-body, 42–57 (47) in diameter (n = 5). Oral sucker width to ventral sucker width ratio 1: 0.45–0.56 (0.49) (n = 4). Prepharynx

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short, measurable portion 0–17 (5) long. Pharynx distinctly smaller than oral sucker, 32–51 9 38–57 (38 9 44). Oesophagus distinct, 27–58 (46) long. Caeca blind, terminating at mid-level of testes; post-caecal region occupying 21–31 (25)% of body length. Testes symmetrical, entire, in mid-hindbody, 60–130 9 35–98 (93 9 58). Post-testicular region 63–130 (87) long, occupying 13–24 (18)% of body length. Cirrus-sac large, posterior, dorsal and anterior to ventral sucker, opening into common genital atrium, contains single-chambered oval seminal vesicle, maximum measurable length 97–163 (129). Pars prostatica indistinct; prostatic cells not detected; eversible ejaculatory duct (cirrus) armed with dense, long, fine spines (Fig. 5). Genital atrium unarmed. Common genital pore median, slightly antero-sinistral to ventral sucker. Ovary 3 or 4-lobed, immediately anterior to right testis, postero-dextral to ventral sucker, 59–130 9 33–90 (95 9 70). Vitellarium in 2 distinct, compact masses, antero-medial to testes. Uterus occupies most free space in body, extensive in forebody to level of pharynx, extends posteriorly at least to posterior margin of testes. Terminal organ bipartite, unites with uterus between posterior unarmed part and anterior part which is armed with long fine spines similar to those of cirrus. Egg capsules thin-shelled, without filaments, 19–25 9 9–13 (22 9 11). Excretory vesicle I-shaped, extends to between testes, sometimes to close to posterior end of cirrus-sac, 112–208 (175) long. Excretory pore terminal.

configuration of the vitellarium in two lateral compact masses anterior to the testes, the extent of the uterus from the pharyngeal level into the post-testicular region but not reaching the posterior extremity, the position of the testes which are near the posterior extremity with a small post-testicular region (relative to body length), and in the position at which the caeca terminate, not extending into the post-testicular region. Minor differences detected between Machida’s specimens and ours are here interpreted as relating to the slight flattening of his specimens.


Description (Figs. 6–10)

In its possession of a spinose tegument, two symmetrical extracaecal testes, an ovoid body, a lobed ovary anterior to the testes, an extensive uterus and lateral vitelline follicles restricted to the hindbody in the area of the gonads, the current material is in clear agreement with Diplomonorchis Hopkins, 1941 as presently recognised by Madhavi (2008). There are currently ten species recognised in the genus in a wide range of marine fish families. Of these, just Diplomonorchis leiostomi Hopkins, 1941 (type-species) and D. kureh Machida, 2005 have been reported from haemulids. The current material strongly resembles and is identified as D. kureh [which was described from the closely related Diagramma pictum from off Japan by Machida (2005)] in the position and

[Measurements based on 66 unflattened, whole mount specimens.] Body elongate, with nearly parallel sides and maximum width in mid hindbody, 747–1,374 9 114–266 (1,107 9 186). Length/width ratio 3.88–8.29 (6.03): 1. Tegument spinose. Forebody 299–593 (457) long, occupying 28–54 (41)% of body length. Hindbody 211–805 (598) long. Oral sucker variable in outline, ranging from distinctly wider than long (or deep) to distinctly longer than wide (or deep), opens ventro-subterminally, 64–131 9 89–135 (98 9 106). Ventral sucker smaller than oral sucker, in mid-body, 40–74 (63) in diameter. Oral sucker width to ventral sucker width ratio 1: 0.35–0.67 (0.57). Prepharynx short, 0–27 (10) long. Pharynx distinctly smaller than oral sucker, 32–52 9 35–68 (42 9 53). Oesophagus

Proctotrema Odhner, 1911 Proctotrema addisoni n. sp. Type-host: Diagramma labiosum Macleay (Perciformes: Haemulidae). Type-locality: Off Heron Island, Queensland, Australia (23°260 S, 151°540 E). Site in host: Intestine. Prevalence: 15 of 22 (68%). Deposition of specimens: Holotype (QM G234461) and 14 paratypes (QM G234462–75) lodged in the QM. Molecular sequence data: 28S rDNA, 1 replicate (KJ658291); ITS2 rDNA, 3 replicates (1 submitted KJ658292). Etymology: This species is named for Addison McEwan in recognition of his ongoing support to the first author.



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Figs. 6–10 Proctotrema addisoni n. sp. ex Diagramma labiosum from off Heron Island, line drawings. 6. Whole mount, ventral view. 7. Whole mount, ventral, showing position of caeca and testis. 8. Terminal genitalia, ventral view. 9. Terminal genitalia, lateral, showing eversible cirrus. 10. Terminal genitalia, lateral, showing terminal organ. Scale-bars: 6–8, 200 lm; 9, 100 lm; 10, 200 lm

distinct, 52–152 (107) long. Caeca blind, terminating close to posterior end of body; post-caecal region occupying 3–8 (5)% of body length (Fig. 7).


Testis single, entire, 154–279 9 81–177 (194 9 114). Post-testicular region 72–281 (208) long, occupying 8–26 (20)% of body length. Cirrus-sac extends

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anteriorly from anterior margin of testes to distinctly anterior to ventral sucker where it recurves to open at genital atrium at level of anterior margin of ventral sucker, maximum measurable length 155–344 (267). Pars prostatica distinct. Internal seminal vesicle singlechambered (Fig. 8). Eversible ejaculatory duct (cirrus) armed with conspicuous robust spines (Fig. 10). Genital atrium well-developed, unspined. Common genital pore immediately anterior to ventral sucker, median. Ovary entire, immediately anterior to testis, posterior to ventral sucker, 86–208 9 54–76 (126 9 67). Vitellarium in 2 symmetrical lateral compact masses in ovariotesticular region. Uterus extends to posterior extremity, occupies most of hindbody, opens into posterior end of terminal organ. Terminal organ unipartite, long, armed with large conspicuous spines, opens into genital atrium (Fig. 9). Egg capsules without filaments, 21–27 9 10–15 (23 9 12). Excretory vesicle I-shaped, extends to mid-testis, 152–246 (212) long (n = 5). Excretory pore terminal. Remarks The holotype of this species is a hologenophore sensu Pleijel et al. (2008). That is, the posterior end of the specimen was sacrificed for DNA extraction, generating the sequences referred to above. The anterior end of the specimen which incorporates the complex and distinctive terminal genitalia was stained and mounted and has been deposited in the Queensland Museum. This approach was taken because sequencing of ITS2 rDNA from another specimen from D. labiosum collected from off Heron Island and resembling L. addisoni n. sp. produced a sequence 8 bp different from that reported here. We suspect that this second form represents a distinct and possibly cryptic species, but the morphological material associated with it is not of sufficient quality to allow the matter to be resolved at present. We note that McNamara et al. (2014) reported molecular evidence for the existence of a pair of cryptic species in the chaetodontid Coradion altivelis, also from off Heron Island on the GBR. In that case the potential cryptic species were detected only after the species had been described on the basis of morphology. In the present case the deposition of a hologenophore should assist future resolution of this issue. In having a single testis, unfilamented eggs and a restricted vitellarium, the present species agrees with the Monorchiinae as recognised by Madhavi (2008).


Within the Monorchiinae it agrees with Proctotrema in lacking oral spines, having a single testis in the midhindbody with extensive uterine coils posterior to it, having the ovary and vitelline follicles in the hindbody but anterior to the testis, a unipartite terminal organ, and an unspined genital atrium. This genus was reviewed most recently by Carballo et al. (2011) who recognised just four species consistent with the characters listed above: P. bacilliovatum Odhner, 1911 (type-species), P. amphitruncatum Fischthal & Thomas, 1969, P. bartolii Carballo, Laurenti & Cremonte, 2011 and P. guptai Ahmad & Dhar, 1987. These species incorporate dramatic variation in other features and are easily distinguished from each other and from the present form. Proctotrema bacilliovatum, P. amphitruncatum and P. guptai all have distinctly funnel-shaped oral suckers and deeply lobed ovaries whereas in P. bartolii and the present form the oral sucker is round and the ovary is entire. Proctotrema bartolii differs from the present form in being significantly less elongate, in having suckers of much more nearly equivalent size, and a proportionally less elongate spiny metraterm. The present form differs from all four previously described species of the genus in having the vitelline follicles form two compact masses rather than groups of distinct follicles. In view of these distinctions we have no hesitation in proposing a new species for the present form. The level of variation within this genus raises the question of whether it is likely to be monophyletic. Characters such as lobation of the ovary and the shape of the oral sucker are often used elsewhere as characters for the division of trematode genera. For the present, we accept the prevailing view that the form of the terminal genitalia should have precedence in the characterisation of genera but we think it likely that future molecular analysis will bring about major changes in the taxonomy of this genus. Lasiotocus Looss in Odhner, 1911

Lasiotocus arrhichostoma n. sp. Type-host: Diagramma labiosum Macleay (Perciformes: Haemulidae). Type-locality: Off Heron Island, Queensland, Australia (23°260 S, 151°540 E). Site in host: Intestine.



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Figs. 11–14 Lasiotocus arrhichostoma n. sp. ex Diagramma labiosum from off Heron Island, line drawings. 11. Whole mount, ventral view. 12. Oral sucker, ventral view, showing basket-like muscle fibres. 13. Oral sucker, lateral view, showing basket-like muscle fibres. 14. Terminal genitalia, ventral view. Scale-bars: 11, 400 lm; 12–14, 200 lm

Prevalence: 14 of 22 (64%). Deposition of specimens: Holotype (QM G234476) and 14 paratypes (QM G234477–90) lodged in the QM.


Molecular sequence data: 28S rDNA, 1 replicate (KJ658289); ITS2 rDNA, 1 replicate (KJ658290). Etymology: This species is named for the distinctive morphological structure at the base of the oral sucker;

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‘‘arrhichos’’ meaning basket of the wicker kind, ‘‘stoma’’ meaning mouth of an animal. Description (Figs. 11–14) [Measurements based on 47 unflattened, whole mount specimens.] Body elongate, 812–2,908 9 150–310 (1,862 9 227). Length/width ratio 4.69–11.15 (8.23): 1. Tegument spinose. Forebody 384–1049 (687) long, occupying 28–47 (37)% of body length. Hindbody 376–1,840 (1,087) long. Oral sucker funnel-shaped, opens ventrally sub-terminally, 154–312 9 136–248 (232 9 180). Muscle fibres extending from base of oral sucker to prepharynx just anterior to anterior margin of pharynx, creating prominent and distinctive basket-like structure with similar appearance in lateral and dorsoventral view (Figs. 12, 13). Ventral sucker smaller than oral sucker, in anterior third of body, 69–126 (90) in diameter. Oral sucker width to ventral sucker width ratio 1: 0.37–0.61 (0.50). Prepharynx short, 0–22 (6) long. Pharynx distinctly smaller than oral sucker, 39–65 9 36–63 (51 9 49). Oesophagus 58–128 (84) long. Caeca blind, terminating in posterior hindbody; post-caecal region occupying 12–16 (13)% of body length. Single elliptical testis in middle of hindbody, 108–325 9 83–169 (212 9 118). Post-testicular region 214–833 (562) long, occupying 13–34 (26)% of body length. Cirrus-sac extending from anterior margin of ovary to open into distinct genital atrium at level of anterior margin of ventral sucker; maximum measurable length 339–479 (392). Internal seminal vesicle single-chambered. Eversible ejaculatory duct (cirrus) armed with large conspicuous spines, 170–245 (210) (Fig. 14). Genital atrium unspined. Common genital pore median, immediately anterior to ventral sucker. Ovary 3 to 4-lobed, midway between ventral sucker and testis, 86–214 9 55–166 (154 9 121). Vitelline follicles in lateral fields in ovariotesticular zone. Uterus extends to posterior extremity, occupying entire hindbody. Terminal organ bipartite, unites with uterus at junction between unarmed posterior part and anterior part which is armed with prominent robust spines. Egg capsules without filaments, 22–27 9 10–15 (24 9 12). Excretory vesicle I-shaped, extending into mid-forebody. Excretory pore terminal. Remarks The present material agrees with Lasiotocus as recognised by Madhavi (2008). Key characteristics are the


elongated body shape, relatively small ventral sucker, intestinal bifurcation in the forebody, caeca terminating in the hindbody, genital pore anterior to the ventral sucker, pretesticular ovary, uterus that occupies most of the hindbody, bipartite terminal organ armed with spines, and vitellarium forming symmetrical bunches of follicles at the level of the testis or ovary. The genus has not been revised in any detail recently although numerous authors have commented on problems with the genus (see Madhavi, 2008). The most up-to-date listing of species is that provided by the World Register of Marine Species (WoRMS Editorial Board, 2014). This database recognises 54 species in this genus, making it by far the richest genus in the family and accounting for about a fifth of the species in the Monorchiidae. We reviewed descriptions of all the 54 species. Especially valuable in this context was the work of Bartoli & Bray (2004) which provided comprehensive redescriptions of the type-species of Lasiotocus, L. mulli (Stossich, 1883), Ancylocoelium Nicoll, 1912, A. typicum Nicoll, 1912, and Chrisomon Manter & Pritchard, 1961, C. tropicus (Manter, 1940). These descriptions informed their conclusion that these three genera should be considered synonymous with Lasiotocus. In our view, Lasiotocus as presently constituted contains variation which far exceeds that seen in genera in most other families of trematodes of fishes. In particular we note distinctions between species with round or funnel-shaped oral suckers, entire (or irregular) or deeply and consistently lobed ovaries, vitelline follicles that are follicular and extensive, follicular and highly restricted, or compact masses rather than follicular. Given the potential for molecular data to begin to resolve these issues we see no pressing need to propose new genera for any of these taxa but certainly we doubt seriously that the present constitution of this genus will prove robust. The present form was compared with descriptions of all 54 currently recognised species. The combination of a funnel-shaped oral sucker that is distinctly larger than the ventral sucker, a deeply lobed ovary, and relatively narrowly distributed vitelline follicles serve to distinguish it from all but L. bengalensis Ahmad & Gupta, 1985, L. chaetodipteri Thomas, 1959, L. guptai (Ahmad & Dhar, 1987), L. longitestis Durio & Manter, 1968, L. macrorchis (Yamaguti, 1934), L. maculatus Madhavi, 1974, L. mugilis Overstreet, 1969, L. overstreeti Gupta & Gupta, 1990, L. plectorhynchi (Yamaguti, 1934) and L. truncatus



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(Linton, 1910). However, the present form is clearly distinct from these (and all other species in the genus) in having the excretory vesicle extend to the midforebody and in the distinctive arrangement of muscles running from the posterior end of the oral sucker to the posterior prepharynx. The present species is most similar to three species also reported from haemulids. In addition to the differences mentioned above, it differs: from L. longitestis in being far more elongate and having the testis much smaller relative to the overall size of the body; from L. maculatus in being far more elongate and reaching 2.9 mm as compared with 1.4 mm in length; and from L. plectorhynchi in being again far more elongate, having a proportionally longer forebody, and having the intestinal caeca terminating much closer to the posterior extremity. In view of these distinctions we have no hesitation in proposing the present form as a new species. Asymmetrostoma n. g. Generic diagnosis Body small, elliptical to elongate. Tegument spinose. Oral sucker conspicuously dorsoventrally asymmetrical by being truncated dorsally, opening ventro-subterminally. Ventral sucker smaller than oral sucker, in midbody. Pharynx distinctly smaller than oral sucker. Caeca blind, terminating near posterior extremity. Testis single, ovoid, dorsal, dextral or just posterior to ventral sucker. Cirrus-sac containing single-chambered seminal vesicle and eversible ejaculatory duct (cirrus) armed with long, conspicuous spines. Genital pore median, immediately anterior to ventral sucker. Ovary in posterior forebody, entire to irregularly lobed. Vitelline follicles in ovariotesticular zone. Terminal organ unipartite, posteriorly armed with large, conspicuous spines. Uterus extends from intestinal bifurcation into hindbody. Excretory vesicle tubular, extends to mid-hindbody. Excretory pore terminal. Type-species: Asymmetrostoma heronensis n. g., n. sp. Etymology: This genus is named for the morphological structure of the oral sucker; ‘‘asymmetros’’ meaning asymmetrical, ‘‘stoma’’ meaning mouth of an animal. Asymmetrostoma heronensis n. sp. Type-host: Diagramma labiosum Macleay (Perciformes: Haemulidae).


Type-locality: Off Heron Island, Queensland, Australia (23°260 S, 151°540 E). Site in host: Intestine. Prevalence: 8 of 22 (36%). Deposition of specimens: Holotype (QM G234491) and 11 paratypes (QM G234492–502) lodged in the QM. Etymology: This species is named for the type-locality, Heron Island, Australia. Description (Figs. 15–20) [Measurements based on 24 unflattened, whole mount specimens.] Body shape highly variable, elliptical to elongate, 635–1,256 9 136–314 (839 9 202). Length/ width ratio 3.2–6.10 (4.24): 1. Tegument spinose; spines in clear well-separated rows. Forebody 327–410 (372) long, occupying 47–56 (51)% of body length. Hindbody 247–645 (336) long. Oral sucker distinctly asymmetrical as a result of being truncated dorsally, opening ventro-subterminally, 80–215 9 114–195 (138 9 152) (Figs. 15–17). Ventral sucker smaller than oral sucker, in mid-body, 56–88 (75) in diameter. Oral sucker width to ventral sucker width ratio 1: 0.41–0.60 (0.50). Prepharynx short, measurable portion 0–42 (20) long. Pharynx distinctly smaller than oral sucker, 23–55 9 23–55 (39 9 40). Oesophagus 44–90 (61) long. Caeca blind, extending to midhindbody. Post-caecal region occupying 14–20 (16)% of body length. Testis single, ovoid, dorsal, dextral or just posterior to ventral sucker, 84–95 9 47–86 (90 9 66) (n = 2). Posttesticular region 288–324 (306) long, occupying 36% of body length (n = 2). Cirrus-sac extends anteriorly from dorsal to ventral sucker to open into genital atrium, maximum measurable length 74 (n = 1). Internal seminal vesicle single chambered. Pars prostatica and prostatic cells not detected. Eversible ejaculatory duct (cirrus) armed with long conspicuous spines (Fig. 20). Genital atrium unspined, large. Common genital pore median, immediately anterior to ventral sucker. Ovary entire to irregularly lobed, in posterior forebody, 106–134 9 68–93 (120 9 80) (n = 2). Vitelline follicles in ovariotesticular zone, position varying with extension of body. Uterus fills hindbody to tips of intestinal caeca and forebody to intestinal bifurcation, enters middle of terminal organ anterior to spiny posterior portion. Terminal organ unipartite, posteriorly armed with large, conspicuous, erratic

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Figs. 15–20 Asymmetrostoma heronensis n. g., n. sp. ex Diagramma labiosum from off Heron Island, line drawings. 15. Whole mount, ventral view. 16. Whole mount, lateral view. 17. Oral sucker, ventral view, alternate form. 18. Terminal genitalia, ventral view. 19. Terminal genitalia, lateral, right. 20. Terminal genitalia, lateral, left. Scale-bars: 15, 16, 200 lm; 17–20, 100 lm

spines and anteriorly unarmed (Figs. 18, 19). Egg capsules without filaments, 18–23 9 10–13 (21 9 12). Excretory vesicle extends to mid-hindbody. Excretory pore terminal.

Remarks In its body shape, possession of a single testis, eggs without filaments, and vitellarium in the mid-body,



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Fig. 21 Relationships between monorchiid taxa based on Bayesian inference and Maximum Likelihood analyses of the 28S rDNA dataset. Bayesian inference posterior probabilities are shown above the nodes and Maximum Likelihood bootstrap support values below the nodes; values \ 50 not shown. Out. = Outgroup

this form agrees with the subfamily Monorchiinae, as presently recognised by Madhavi (2008). The present form is distinguished from most of the other 25 genera of the Monorchiinae in having a single testis in the middle third of the body, follicular vitellarium in the middle third of the body (in the gonadal region) and the ovary in the posterior forebody. It appears distinct from species of all existing genera in the unusual asymmetrical oral sucker. It is also distinctive in having the ovary in the posterior forebody; among the Monorchiinae only the species of Allobacciger Hafeezullah & Siddiqi, 1970 and Pseudoproctotrema Yamaguti, 1942 also have such anterior ovaries. Asymmetrostoma heronensis n. g., n. sp. is perhaps most generally similar to the single species of Pseudoproctotrema Yamaguti, 1942, P. parupenei Yamaguti, 1942. However, in P. parupenei the oral sucker is discoid and the vitelline follicles form compact masses. On this basis the present form appears sufficiently distinctive to justify the recognition of a new genus and species.

Helicometroides longicollis, Lasiotocus arrhichostoma n. sp. and Proctotrema addisoni n. sp. In initial analyses of 28S sequences (not shown), which used several apocreadiids as the outgroup, the topology was consistent with the conclusion of Olson et al. (2003) in that the Monorchioidea Odhner, 1911 was the sister taxon to the Lepocreadioidea and that the Lissorchiidae Magath, 1917, represented only by one species of Lissorchis Magath, 1917, was the sister to the Monorchiidae. We thus analysed monorchiid taxa using Lissorchis kritskyi Barnhart & Powell, 1979 as the outgroup. Alignment of the 28S rDNA dataset resulted in 1,258 characters available for analysis. Bayesian inference and Maximum Likelihood analyses produced trees of identical topology with high support for most clades (Fig. 21). ITS2 rDNA sequences for the same three taxa were generated, but did not prove phylogenetically informative. The three sequences reported here differ from each other by 26–40 bp and from all other available monorchiid taxa by 24–39 bp.

Discussion Molecular and phylogenetic results Monorchiids of Diagramma Specimens of three of the five species considered in this study were available for genetic characterisation. Partial 28S and ITS2 rDNA data was generated for


The relatively high prevalences of the five species reported here suggest that the monorchiid fauna of

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Diagramma labiosum has been relatively comprehensively sampled. It was thus surprising that we did not find the two monorchiid species reported previously from D. labiosum on the GBR. Paramonorcheides pseudocaranxi was reported by Dove & Cribb (1998) from the carangid Pseudocaranx dentex (Bloch & Schneider) and D. labiosum. It is of interest to note that in an analysis of host-specificity of GBR fish trematodes, Miller et al. (2011) characterised P. pseudocaranxi as a rare euryxenous species (infecting hosts of multiple families, related only by ecology) due to its apparent infections in both Carangidae and Haemulidae. They suggested that such reports should be treated with scepticism, given that the great majority of GBR fish trematodes are highly host specific, either oioxenous (infecting a single host) or stenoxenous (infecting closely related hosts, e.g. from a single family). Review of the fish dissection records reported by Dove & Cribb (1998) relative to original records reveals that the report from D. labiosum was the result of a simple mistake. All the dissection numbers reported (3000, 3018, 4545 and 5652) were from the type-host, P. dentex. However, an individual of D. labiosum was recorded as dissection number 4546, suggesting that the report was the result of a mis-read label. We conclude that P. pseudocaranxi is not a parasite of D. labiosum. It is evident that this species is known only in carangids, and may now be considered oioxenous. We have also found that the record of H. vitellosus from Diagramma labiosum from the Great Barrier Reef (Durio & Manter, 1968) was spurious. Thus, the five species reported here appear to comprise the only records of monorchiids from D. labiosum. In light of this study there are now seven monorchiid species described from species of Diagramma. Four species have been reported to infect Diagramma pictum from off Japan and New Caledonia: Genolopa plectorhynchi (Yamaguti, 1934) [= Proctotrema plectorhynchi Yamaguti, 1934, Lasiotocus plectorhynchi (Yamaguti, 1934)], Paraproctotrema fusiforme Yamaguti, 1934, Helicometroides longicollis and Diplomonorchis kureh (see Yamaguti, 1934; Machida, 2005; Bray & Justine, 2007). The latter two mentioned species were found in D. labiosum at Heron Island in the present study, whereas the other two are not currently known from the region. Based on the high level of sampling reported here, the current collection data suggest that G. plectorhynchi and P. fusiforme are


absent from Heron Island. Three species of monorchiid reported in this study have not been reported from Japan. However, as the sample sizes from those studies have not been reported, these species cannot be reliably inferred as absent from Japan. Two broad observations emerge from these records. First, the available evidence suggests that the monorchiid fauna of species of Diagramma is quite distinct, with sharing between species of the genus but no reported sharing with any other haemulid (assuming that the Japanese host of H. longicollis is indeed D. pictum). Second, the data suggest that geographic distributions of these trematodes may be either widespread (three species) or apparently localized (four species). In terms of biogeographical analysis, there is only one previous study of the distribution of monorchiids in the region. McNamara et al. (2012) investigated the biogeography of monorchiid species from chaetodontids, and found many differences in species composition across sites from the Tropical Indo-West Pacific in the same chaetodontid fishes. It is evident that much more extensive sampling of haemulids will be necessary before it can be determined whether the patterns for haemulids mirror those of the monorchiids of chaetodontids. Molecular analyses The addition of the three taxa sequenced here brings the total of monorchiid species for which 28S rDNA sequences are available to just eight including, putatively, representatives of just seven of the 40 genera recognised by Madhavi (2008). Although almost all the clades recognised in our analysis had high support, the available sequences are still too few to allow much useful inference. It is interesting to note, however, that one representative of the Hurleytrematinae Yamaguti, 1958 (Helicometroides longicollis) is identified as sister to the remaining taxa whereas the other hurleytrematine species, Provitellus turrum Dove & Cribb, 1998, falls within a strongly supported clade comprising it and five monorchiines. Cableia pudica Bray, Cribb & Barker, 1995 was recognised as a monorchiid only relatively recently (see Bray et al., 2005), when it was identified as a basal monorchiid; the present analysis identifies H. longicollis as the most basal monorchiid for which a 28S rDNA sequence is available. Finally, it is noteworthy that the two putative species of Lasiotocus, L. typicum (Nicoll,



1912) and L. arrhichostoma n. sp., do not form a clade. Given the level of variation incorporated by this large genus as discussed above, this comes as no surprise. However, because no sequence data are available for the type-species of Lasiotocus (L. mulli) or for the many other species in the genus, we consider it premature to propose genus level changes for these taxa. In the main, the new sequences reported here serve to improve the dataset for future analyses and to demonstrate that there remains much to be done with respect to resolving higher relationships in this family. The generation of ITS2 rDNA sequences for three monorchiids here brings the total available for the family to 22. Of these, 17 are for species of just one genus, Hurleytrematoides Yamaguti, 1954. In analysis of Hurleytrematoides, these sequences were found reliable in distinguishing species (McNamara & Cribb, 2011; McNamara et al., 2012). The sequences of Helicometroides longicollis, Lasiotocus addisoni n. sp. and Proctotrema arrhichostoma n. sp. are thus provided in the expectation that they will assist in the future delineation of species in these genera. Richness of trematodes of the Haemulidae This study brings the reported trematode fauna of D. labiosum on the Great Barrier Reef to 12 species, making it one of richest known hosts for trematodes there. Kamiya et al. (2014) have shown that host size correlates strongly with parasite richness across multiple taxa. Diagramma labiosum is a large fish, reaching 90 cm in length (Randall et al., 1997) and this size doubtless explains much of its parasite richness. In addition, however, we note that haemulids are generally rich and sometimes exceptionally rich for trematodes. According to published records, several well-studied species from the western Atlantic (Anisotremus virginicus (Linnaeus), Haemulon flavolineatum (Desmarest), H. plumieri (Lace´pe`de) and H. sciurus (Shaw)) are each reported to harbour over 20 trematode species and in each case from at least ten trematode families; most remarkable is H. sciurus which is reported to harbour 26 species. Notably, in a detailed study of the diet of fishes of the West Indies, Randall (1968) reported wide dietary ranges for many haemulids including, for H. sciurus, a range of annelids (polychaetes), bryozoans, crustaceans (amphipods, crabs, isopods, ostracods, shrimps, stomatopods), echinoderms (echinoids, ophiuroids), fishes,


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molluscs (bivalves, cephalopods, gastropods, scaphopods), sipunculids and tunicates. We suspect that the trematode richness in haemulids is explained significantly by the remarkable breadth of diet of these fishes. Acknowledgements We thank Drs Terry Miller and Rod Bray and Mr Storm Martin for their help with fish collection and Dr Selina Ward for comments on an early version of this manuscript. We also thank Jeff Johnson for advice regarding the current taxonomic status of the host taxa, Dr Scott Gardner for supplying photographs of specimens in his care, and the staff of the Heron Island Research Station for their support over many years. The work was supported by grants to Cribb from the ABRS and the Australian Research Council.

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Monorchiid trematodes of the painted sweetlips, Diagramma labiosum (Perciformes: Haemulidae), from the southern Great Barrier Reef, including a new genus and three new species.

Five monorchiid species are reported from Diagramma labiosum Macleay (Perciformes: Haemulidae) collected from Heron Island on the southern Great Barri...
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