Dactylogyrids (Platyhelminthes: Monogenoidea) Infecting the Gill Lamellae of Flatheads (Scorpaeniformes: Platycephalidae), with Proposal of Platycephalotrema n. gen. and Descriptions of New Species from Australia and Japan

Abstract

Platycephalotrema n. gen. (Dactylogyridae) is proposed for four new species and 5 previously described species parasitizing the gills of flatheads (Scorpaeniformes: Platycephalidae) as follows: Platycephalotrema ogawai n. sp. (type species) from Platycephalus sp. 1 (type host) and Platycephalus sp. 2, both of Nakabo & Kai (2013) (locally known as “Yoshino-gochi” and “Ma-gochi,” respectively) (Japan); Platycephalotrema austrinum n. sp. from Platycephalus endrachtensis Quoy & Gaimard (type host) and Platycephalus sp. (Australia); Platycephalotrema bassensis (Hughes, 1928) n. comb. from Platycephalus bassensis Cuvier (Australia); Platycephalotrema koppa n. sp. from Platycephalus fuscus Cuvier (Australia); Platycephalotrema macassarensis (Yamaguti, 1963) n. comb. from Platycephalus indicus (Linnaeus) (China, Macassar); Platycephalotrema mastix n. sp. from P. fuscus and P. endrachtensis (Australia); Platycephalotrema platycephali (Yin & Sproston, 1948) n. comb. from P. indicus (China) and P. fuscus (Australia); Platycephalotrema sinensis (Yamaguti, 1963) n. comb. from Cociella punctata (Cuvier) (China); Platycephalotrema thysanophrydis (Yamaguti, 1937) n. comb. from Inegocia japonica (Cuvier), Inegocia ochiaii Imamura, and Cociella crocodilus (Cuvier) (Japan, China). Other species requiring further study but potentially members of Platycephalotrema include Ancyrocephalus vesiculosus Murray, 1931, Haliotrema indicum Tripathi, 1957, Haliotrema swatowensis Yao, Wang, Xia, & Chen, 1998, and Haliotrema pteroisi Paperna, 1972. The primary features differentiating Platycephalotrema include species having: (1) tandem gonads (testis postgermarial); (2) two prostatic reservoirs, each emptying independently into the base of the male copulatory organ; (3) a dextral vaginal pore and large vaginal vestibule; (4) dorsal and ventral pairs of morphologically similar anchors; (5) a ventral bar with spatulate ends; (6) a dorsal bar with bifurcated ends, and (7) absence of an accessory piece. The new species are described, and P. thysanophrydis is redescribed based on newly collected and museum specimens.

1. Introduction

The Platycephalidae (Scorpaeniformes) is currently comprised of 88 species commonly known as flatheads. All but one species occur in the brackish and marine waters of the Indo-Pacific Ocean; the Guinea flathead Solitas gruveli (Pellegrin) occurs in the eastern Atlantic Ocean off Africa. The family includes 18 genera: Platycephalus (with 21 species); Thysanophrys (11 species); Onigocia (9 species); Rogadius (8 species); Cociella, Sorsogona and Sunagocia (5 species each); Cymbacephalus, Grammoplites and Ratabulus (4 species each); Inegocia and Suggrundus (3 species each); and Kumococius, Papilloculiceps, Solitas, Leviprora, Ambiserrula and Elates (all monotypic) [1]. Although flatheads have a wide distribution within the Indo-Pacific Region and are economically important as recreational and commercial fishes in parts of the region [2], studies dealing with their dactylogyrid parasites are limited. To date, only seven dactylogyrid species have been described from five of the 88 species of flatheads listed in Eschmeyer’s Catalog of Fishes [1].

The present paper, in part, represents the fourth installment recording the monogenoidean fauna of Moreton Bay, Queensland, Australia, and was supported by an Australian Biological Resources Study Grant to Drs. Thomas Cribb and Scott Cutmore at the University of Queensland, St. Lucia, Australia. Previous installments included the monogenoids infecting three species of beloniform fishes [3], two gerreid species [4] and two species of lutjanids and a monodactylid [5]. In addition to including the proposal of a new dactylogyrid genus and description of three new species occurring on flatheads from Moreton Bay, a description of a new species and a new geographic record for a previously described species from flatheads occurring in the Seto Inland Sea of Japan are provided.

2. Materials and Methods

Four dusky flatheads Platycephalus fuscus Cuvier and a single bar-tailed flathead Platycephalus endrachtensis Quoy & Gaimard were collected by various methods from Moreton Bay, Queensland, Australia, during January 2016 as part of a survey to determine the diversity of the parasite fauna infecting the fishes of the bay. Hosts were transported alive to the Moreton Bay Research Station located in Dunwich, North Stradbroke Island, Queensland, where they were euthanized and identified using Johnson [6]; gill baskets were immediately removed and placed in hot (60 °C) sea water to relax and kill the attached helminths; a volume of 10% formalin, equal to that of the sea water of each container, was then added for fixation in 5% formalin. When necessary, excess fluid was decanted, and the fixed gills and sediments from each fish were placed in separate vials, labeled, and shipped to Idaho State University for study.

Flatheads from Japan were commercially fished from the Seto Inland Sea, purchased from local fish markets, identified based on Nakabo & Kai [7], and frozen or placed on ice in plastic bags until examination for parasites. Monogenoids from the Japanese flatheads were fixed in AFA under coverslip pressure or in hot 5% formalin, stained in Heidenhain’s iron hematoxylin, dehydrated through a graded ethanol series and mounted in Canada balsam from xylene. These specimens were subsequently deposited in the Meguro Parasitological Museum Collection (MPM), from which they were placed on loan to the authors for the present study.

Dactylogyrids collected in Australia were subsequently removed from the gills or sediment using a small probe and dissecting microscope. Some specimens were mounted unstained in Gray & Wess medium for study of sclerotized structures; other specimens were stained with Gomori’s trichrome, VanCleave’s hematoxylin, or Heidenhain’s iron hematoxylin and mounted in Canada balsam for determination of internal anatomy.

Illustrations were prepared with the aid of a camera lucida or microprojector. Measurements, all in micrometers, represented straight-line distances between extreme points and were expressed as the range followed by the mean and number (n) of structures measured in parentheses. Body length included that of the haptor.

Except for Platycephalus sp. 1 and Platycephalus sp. 2, both of Nakabo & Kai [7] and locally known respectively as “Yochino-gochi” and “Ma-gochi” in Japan, scientific names of all fishes were verified in Fricke et al. [1].

Type and voucher specimens of helminths collected for the present study were deposited in the Queensland Museum (QM), Brisbane, Australia; the Meguro Parasitological Museum (MPM), Tokyo, Japan; and the University of Nebraska State Museum, Harold W. Manter Laboratory (HWML), Lincoln, Nebraska as indicated in the species’ accounts. The following museum specimens were also examined: 11 syntypes (2 in serial sections), Ancyrocephalus vesiculosus Murray, 1931, Museums Victoria, Melbourne, Australia (NMV) F 60389; 3 syntypes, Ancyrocephalus platycephali Yamaguti, 1953, MPM 23204 (SY6718); 4 syntypes, Ancyrocephalus thysanophrydis Yamaguti, 1937, MPM 23107 (SY0262); 21 voucher specimens, Haliotrema thysanophrydis (Yamaguti, 1937) Bychowsky & Nagibina, 1971, MPM 21470, 21471; 2 voucher specimens, Pseudohaliotrema thysanophrydis (Yamaguti, 1937) Young, 1968, National Museum of Natural History, National Invertebrate Zoology Collection, Washington D.C., USA, USNM 1356609; 3 voucher specimens, Pseudohaliotrema platycephali (Yin & Sproston, 1948) Young, 1968, USNM 1356610, 1356611; 3 voucher specimens, Haliotrema platycephali Yin & Sproston, 1948, The Natural History Museum, London (BMNH) 1984.7.19.69; 3 vouchers, unidentified Dactylogyridae (identified herein as Platycephalotrema ogawai n. sp.), MPM 31091 (F0293–0295); 5 voucher specimens, unidentified Dactylogyridae [identified herein as Platycephalotrema thysanophyrydis (Yamaguti, 1937) n. comb.], MPM 31090 (F0287–0291).

In the ensuing sections of this paper, the following abbreviations for host and parasite genera beginning with the letter “P” are utilized: Pl. for Platycephalus; Pt. for Platycephalotrema; and Ps. for Pseudohaliotrema. In order to minimize confusion, these abbreviations were only used after the respective generic name was first used within a given passage.

3. Results

• Subclass Polyonchoinea Bychowsky, 1937
• Order Dactylogyridea Bychowsky, 1937
• Dactylogyridae Bychowsky, 1933

3.1. Platycephalotrema n. gen.

3.1.1. Diagnosis

Body fusiform, slightly flattened dorsoventrally, comprising body proper (cephalic region, trunk, and peduncle) and haptor. Tegument smooth. Two terminal, two bilateral cephalic lobes; three pairs of bilateral head organs; bilateral groups of unicellular cephalic glands prepharyngeal, pharyngeal and/or postpharyngeal. Eyespots four, infrequently absent; granules small, ovate. Mouth subterminal, prepharyngeal; pharynx a muscular bulb; esophagus short to non-existent; intestinal ceca two, confluent posterior to gonads, lacking diverticula. Genital pore midventral, immediately posterior to intestinal bifurcation. Gonads intercecal, tandem (germarium pretesticular). Testis entire; vas deferens apparently looping dorsoventrally left intestinal cecum; seminal vesicle a simple dilation of distal vas deferens at level of male copulatory organ (MCO). Two generally large prostatic reservoirs; each having duct independently entering base of MCO; contents of anterior (or ventral) reservoir dense, usually comprising two zones of secretory material differing in density and stain preference; contents of posterior (or dorsal) reservoir nearly transparent, resisting stain. MCO a sclerotized tube, often with complex distal end; accessory piece absent. Germarium entire; oviduct, uterus not observed; Mehlis’ gland present. Vaginal pore dextral, submarginal; vagina comprising large distal vestibule often with sclerotized components and from which the vaginal canal extends posteriorly toward ootype. Seminal receptacle not observed or indistinct. Vitellarium throughout trunk, except absent from regions of other reproductive organs. Globose haptor with bilateral lobes and armed with dorsal and ventral anchor/bar complexes, seven pairs of similar hooks having normal dactylogyrid distribution; vesicle filled with granular product usually associated with each of ventral and/or dorsal anchor. Dorsal and ventral anchors similar in size, shape; each with elongate superficial root, large base, short slightly arcing shaft, elongate point. Ventral bar simple, with spatulate ends; dorsal bar with bifurcated ends. Each hook with protruding blunt thumb, slender shank comprised of one subunit. Parasites of fishes assigned to the Platycephalidae.

3.1.2. Taxonomic Summary

Type species: Platycephalotrema ogawai n. sp. from Platycephalus sp. 1 & Platycephalus sp. 2, (both of Nakabo & Kai [7], two apparently undescribed or unidentified species locally known in Japan as “Yoshino-gochi” and “Ma-gochi”, respectively) (Scorpaeniformes: Platycephalidae) (Japan).

Other species: Platycephalotrema austrinum n. sp. from Pl. endrachtensis Quoy & Gaimard and Platycephalus sp. (Australia); Platycephalotrema bassensis (Hughes, 1928) n. comb. from Pl. bassensis Cuvier (Australia); Platycephalotrema koppa n. sp. from Pl. fuscus Cuvier (Australia); Platycephalotrema macassarensis (Yamaguti, 1963) n. comb. from Pl. indicus (Linnaeus) (China, Macassar); Platycephalotrema mastix n. sp. from Pl. fuscus and Pl. endrachtensis (Australia); Platycephalotrema platycephali (Yin & Sproston, 1948) n. comb. from Pl. indicus (China); Platycephalotrema sinensis (Yamaguti, 1963) n. comb. from Pl. punctatus Cuvier [now Cociella punctata (Cuvier)] (China); Platycephalotrema thysanophrydis (Yamaguti, 1937) n. comb. from Thysanophrys japonicus (Tilesius) [an ambiguous synonym of Pl. japonicus Cuvier, now Inegocia japonica (Cuvier)], Inegocia ochiaii Imamura, and Cociella crocodilus (Cuvier) (Japan, China).

Likely congeners requiring further investigation: Ancyrocephalus vesiculosus Murray, 1931 from Pl. bassensis (Cuvier) (Australia); Haliotrema indicum Tripathi, 1957 from Pl. insidiator (Forsskål) (now Pl. indicus) (India); Haliotrema pteroisi Paperna, 1972 from Pterois volitans (Linnaeus) (Red Sea); Haliotrema swatowensis Yao, Wang, Xia, & Chen, 1998 from Pl. indicus (China).

Etymology: The generic name (neuter) reflects the family of fishes, the Platycephalidae, species of which harbor members of the new genus.

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3.1.3. Remarks

Platycephalotrema n. gen. is characterized by dactylogyrids possessing a combination of the following features: (1) tandem gonads (testis postgermarial); (2) a copulatory complex lacking an accessory piece; (3) two prostatic reservoirs, each emptying independently into the base of the MCO; (4) the anterior prostatic reservoir usually containing two zones of secretion, each zone differing in density and stain affinity; (5) a dextral vaginal pore; (6) a large vaginal vestibule usually with sclerotized components; (7) dorsal and ventral pairs of morphologically similar anchors, each anchor with an elongate point, a short slightly arcing shaft, and a large base having a comparatively long superficial root and a short knob-like deep root; (8) a ventral bar with spatulate ends; (9) a dorsal bar with bifurcated ends; (10) seven pairs of hooks with a normal dactylogyrid distribution; (11) each hook having a protruding blunt thumb and a uniform slender shank comprised of a single subunit; and (12) haptoral reservoirs usually associated with each of the ventral and/or dorsal anchors. Currently, the genus is restricted to species parasitic on the gill lamellae of marine scorpaeniform fishes assigned to the Platycephalidae. Accordingly, all dactylogyrid species previously described and reported from marine scorpaeniform fishes and included in either Ancyrocephalus Creplin, 1839 or Haliotrema Johnston & Tiegs, 1922, are likely members of Platycephalotrema, although four of these species require further study before transfers can be made (see respective species accounts below).

With the exception of host preference, all of the above features can be found in members of other dactylogyrid genera. Platycephalotrema most closely resembles Parancylodiscoides Caballero y C. & Bravo-Hollis, 1961 as revised by Kritsky [8] and Lethrinitrema Lim & Justine, 2011, both with marine species parasitizing ephippid and serranid fishes (Parancylodiscoides spp.) and lethrinid fishes (Lethrinitrema spp.). Members of the three genera share the following features: (1) presence of haptoral reservoirs; (2) two elongate prostatic reservoirs, (3) a dextral vaginal pore; (4) a comparatively large vaginal vestibule; (5) hooks with protruding thumbs and shank of a single subunit; and (6) absence of an accessory piece in the copulatory complex. The accessory piece of Lethrinitrema spp. described by Lim & Justine [9] may or may not be present in respective Lethrinitrema spp., and when present, it appears to comprise a part of the distal end of the MCO rather than a free structure. Platycephalotrema differs from Parancylodiscoides by its species usually having sclerotized components associated with the vaginal vestibule (absent in Parancylodiscoides spp.); a prostatic reservoir frequently containing two zones of secretory product, each varying in density and stain affinity (contents of individual prostatic reservoirs in Parancylodiscoides spp. uniform); and by having tandem gonads, testis postgermarial (gonads juxtaposed, germarium lying to right of testis in Parancyodiscoides spp.) (see [8]). The new genus differs from Lethrinitrema by its species having haptoral reservoirs associated with the dorsal anchors (reservoirs associated with the ventral anchors in Lethrinitrema spp.); morphologically similar dorsal and ventral anchors (dorsal and ventral anchors dissimilar in Lethrinitrema spp.); a dorsal bar with bifurcated ends (ends of the dorsal bar entire in Lethrinitrema spp.); and by lacking lateral grooves along the length of the ventral anchors (present in Lethrinitrema spp.) (see [9]).

3.2. Platycephalotrema ogawai n. sp.

3.2.1. Description (Figure 1)

Greatest width of body proper usually in posterior trunk at level of testis. Cephalic region with well-developed medial and bilateral cephalic lobes. Four eyespots apparently lacking lenses; posterior pair of eyespots larger, slightly farther apart than those of anterior pair; accessory chromatic granules few or usually absent in cephalic region. Pharynx subspherical to subovate. Peduncle slightly tapered posteriorly; haptor with two pairs of lateral lobes, each with subterminal hook. Ventral and dorsal anchors similar; each with elongate superficial root, short knob-like deep root, slightly arced short shaft, elongate point. Ventral bar dorsoventrally flattened, with prominent spatulate ends. Dorsal bar variable in width along its length, with bifurcated ends having unequal limbs. Hook with uniform shank, conspicuous protruding blunt thumb; filamentous hook (FH) loop nearly shank length. MCO with base shaped as inverted o-choko glass, broad tubular slightly undulating shaft, distal coiled end having weakly sclerotized flap. Testis subspherical; proximal vas deferens not observed; seminal vesicle a fusiform dilation of distal vas deferens, anterodextral to MCO. Prostates not observed; prostatic reservoirs large. Anterior (ventral) prostatic reservoir usually containing two zones of granules; proximal zone dense, distal zone nearly translucent. Germarium spherical; oviduct, ootype, uterus not observed; Mehlis’ gland well developed, lying just anterior to germarium. Vaginal pore surrounded by sphincter-like muscle; vaginal vestibule complex, with sclerotized units, often showing serrated edge; vaginal canal delicate. Seminal receptacle apparently absent. Vitellarium dense, coextensive with intestinal ceca; transverse vitelline duct anterior to Mehlis’ gland. Eggs not observed.

3.2.2. Measurements

Measurements are of specimens collected from the type host, Platycephalus sp. 1. Body 1247–1710 (1468; n = 14); greatest width of trunk 322–432 (371; n = 18). Haptor 212–272 (241; n = 15) wide. Ventral anchor 73–83 (79; n = 23) long; dorsal anchor 71–79 (75; n = 23) long. Ventral bar 70–91 (81; n = 24) long; dorsal bar 70–96 (86; n = 16) long. Hook 13–15 (14; n = 11) long. Pharynx 88–119 (98; n = 20) wide. MCO 116–133 (125; n = 27) long. Testis 83–155 (131; n = 18) long, 90–155 (126; n = 18) wide. Germarium 117–170 (139; n = 17) long, 120–178 (146; n = 17) wide.

3.2.3. Taxonomic Summary

Type host: Platycephalus sp. 1 of Nakabo & Kai [7] (locally known as “Yoshino-gochi” [ヨシノゴチ]) (Platycephalidae).

Type locality: Seto Inland Sea, Hiuchi-nada (34°06’ N, 133°21’ E), Japan (host purchased at the market of the Imabari Fishery Cooperative, Imabari City, Ehime Prefecture), 24 May 2018.

Other records: Platycephalus sp. 1: Seto Inland Sea, Utsumi-chō, off Yoko-shima Island, Fukuyama City, Hiroshima Prefecture, Japan (34°21.5’ N, 133°16.5’ E), 23 February 2019. Platycephalus sp. 2 of Nakabo & Kai (2013) [locally known as “Ma-gochi” (マゴチ)]: Seto Inland Sea, Utsumi-chō, off Yoko-shima Island, Fukuyama City, Hiroshima Prefecture, Japan (34°21.5’ N, 133°16.5’ E), 19 February 2017; North Pacific or Mikawa Bay off Tahara, Aichi Prefecture (coordinates not available), Japan, 14 May 1981. Platycephalus sp. (host identified as “Ma-gochi” in MPM records but probably not distinguished between Platycephalus sp. 1 and Platycephalus sp. 2 (collected by Dr. Kusuo Iwata, Fukuoka University), Sea of Japan, off Kyushu (coordinates not available), Japan, 7 July 1978.

Infection site: Gill lamellae.

Specimens studied: Holotype, MPM 21468 (A6679); 27 paratypes, MPM 21468 (A6678–A6680); 14 voucher specimens (from Platycephalus sp. 1), MPM 21522, QM G238134, G238135, HWML 216008; 62 voucher specimens (from Platycephalus sp. 2), MPM 21469 (A6681–A6683), 21051 (A6249–A6255).

Etymology: This species is named for our friend and colleague, Dr. Kazuo Ogawa, Director of the Meguro Parasitological Museum, in recognition of his extensive work on the Monogenoidea and in appreciation for allowing us to examine specimens of the species that he collected in 1981.

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3.2.4. Remarks

Platycephalotrema ogawai n. sp. is the type species of the genus.

3.3. Platycephalotrema koppa n. sp.

3.3.1. Description (Figure 2)

Greatest width of body proper usually near midlength of trunk. Cephalic region with well-developed medial and bilateral cephalic lobes. Eyespots four, apparently lacking lenses; members of posterior pair larger, closer together than those of anterior pair; accessory chromatic granules absent or very few in cephalic region. Pharynx ovate; esophagus short or absent. Peduncle moderately long, slightly tapered posteriorly; haptor with two pairs of lateral lobes, each with subterminal hook. Ventral and dorsal anchors similar; each with elongate superficial root, short knob-like deep root, slightly arced to straight short shaft, elongate point. Ventral bar with long spatulate ends. Dorsal bar variable in width along its length, with unequal terminal limbs. Hook with uniform shank, conspicuous protruding blunt thumb; FH loop nearly shank length. MCO with inverted-cup-shaped base, slightly tapering tubular shaft, distal end having two unequal projections and weakly sclerotized flap. Testis ovate; proximal vas deferens not observed; seminal vesicle a fusiform dilation of distal vas deferens, lying to right of MCO; proximal portion of ejaculatory duct narrow, giving rise to wide distal portion before entering base of MCO. Prostates not observed; prostatic reservoirs large; anterior (ventral) reservoir usually containing two zones of granules with proximal zone dense, distal zone nearly translucent; posterior (dorsal) reservoir smaller than and often obscured by anterior reservoir, with fine reticulate to granular contents. Germarium spherical; oviduct, ootype, Mehlis’ gland not observed; uterus delicate diverted to left of large vaginal vestibule. Vaginal pore surrounded by delicate sphincter-like muscle; vaginal vestibule with anterior sclerotized rod-like unit; vaginal canal not observed. Seminal receptacle apparently absent. Vitellarium dense, coextensive with intestinal ceca; transverse vitelline duct anterior to germarium. Eggs not observed.

3.3.2. Measurements

Body 701–912 (801; n = 5); greatest width of trunk 130–177 (147; n = 6). Haptor 136–151 (144; n = 5) wide. Ventral anchor 68–79 (73; n = 9) long; dorsal anchor 66–77 (71; n = 9) long. Ventral bar 66–78 (72; n = 7) long; dorsal bar 74–81 (77; n = 6) long. Hook 13–15 (14; n = 20) long. Pharynx 44–54 (48; n = 7) wide. MCO 87–107 (96; n = 11) long. Testis 59–81 (70; n = 6) long, 36–52 (45; n = 6) wide. Germarium 44–57 (51; n = 7) long, 39–54 (47; n = 7) wide.

3.3.3. Taxonomic Summary

Type host: Dusky flathead, Platycephalus fuscus Cuvier (Platycephalidae).

Type locality: Moreton Bay off Green Island, Queensland, Australia (27°26′ S, 153°20′ E), 12 January 2016.

Other records: Pl. fuscus: Moreton Bay off Dunwich, North Stradbroke Island, Queensland, Australia (27°50’ S, 153°40’ E), 18 January 2016; Moreton Bay near Port of Brisbane, Queensland, Australia (27°23’ S, 153°11’ E), 19 January 2016.

Infection site: Gill lamellae.

Specimens studied: Holotype, QM G238120; 21 paratypes, QM G238121–G238129, HWML 216001, 216002, 216003, MPM 21520.

Etymology: The specific name (koppa), a noun, is derived from an archaic letter-like-numeral character (Ҁ) of Cyrillic script known as koppa and here refers to the basic shape of the MCO.

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3.3.4. Remarks

Platycephalotrema koppa n. sp. is easily differentiated from all congeners by possessing two large projections and a conspicuous delicate flap at the distal end of the MCO. It is closest morphologically to Pt. platycephali (Yin & Sproston, 1948) n. comb., from which it differs by having elongate spatulate ends of the ventral bar (ends of ventral bar comparatively short in Pt. platycephali; see [10,11]).

Four specimens of the dusky flathead were collected and examined for monogenoids during the survey of the parasites infecting the fishes of Moreton Bay, Australia. Prevalence of Pt. koppa n. sp. in the four fishes was 100%.

3.4. Platycephalotrema mastix n. sp.

Syn. Pseudohaliotrema thysanophrydis of Young [12].

3.4.1. Description (Figure 3)

Greatest width of body proper usually near midlength of trunk. Cephalic region with well-developed pairs of bilateral and terminal cephalic lobes. Eyespots four, apparently lacking lenses; members of posterior pair larger, equidistant or slightly closer together than those of anterior pair; accessory chromatic granules usually absent in cephalic region. Pharynx subspherical; esophagus short to absent. Peduncle moderately long, slightly tapered posteriorly; haptor subtrapezoidal, tapering posteriorly. Ventral anchor with elongate broad superficial root, short knob-like deep root, slightly arcing short shaft, elongate point. Dorsal anchor with elongate depressed superficial root, short deep root, straight or slightly arcing shaft, elongate point. Ventral bar with long spatulate ends. Dorsal bar variable in width along its length, with two posterior subterminal humps, bifurcated ends having short ventral limbs and flattened truncate dorsal limbs. Hook with uniform shank and conspicuous protruding thumb; FH loop nearly shank length. MCO with base shaped as an inverted wine glass, slightly tapered and loosely coiled shaft having a short delicate keel along its midlength; coil comprising about 1 ½ counterclockwise rings. Testis ovate; proximal vas deferens not observed; seminal vesicle a small fusiform dilation of distal vas deferens lying just posterior and dextral to genital pore; proximal portion of ejaculatory duct narrow, giving rise to inflated distal portion before entering base of MCO. Prostates lying lateral and dorsal to vitelline field from about level of genital pore posteriorly to that of vaginal pore, extending lateral to or obscured by vitellarium; prostatic reservoirs large; anterior (ventral) reservoir usually containing two zones of granules with proximal zone dense, distal zone nearly translucent; posterior (dorsal) reservoir smaller than and often obscured by anterior reservoir, with fine reticulate to granular contents. Germarium spherical; oviduct, ootype, Mehlis’ gland, uterus not observed. Small vesicle apparently serving as seminal receptacle lying to left of anterior end of germarium. Vaginal pore located at proximal end of lateral tegumental depression; vaginal vestibule with two anterior sclerotized units; vaginal canal not observed. Vitellarium dense, coextensive with intestinal ceca; transverse vitelline duct anterior to germarium. Eggs not observed.

3.4.2. Measurements

Respective measurements of the specimen collected from Pl. endrachtensis in Moreton Bay follow in brackets those from the type host. Body 684–733 (711; n = 3) [906–907 (n = 1)] long; greatest width of trunk 125–129 (127; n = 3) [177–178 (n = 1)]. Haptor 106–121 (115; n = 3) [141–142 (n = 1)] wide. Ventral anchor 54–55 (n = 1) [56–57 (n = 1)] long; dorsal anchor 53–54 (n = 1) [53–54 (n = 1)] long. Ventral bar 54–70 (63; n = 4) [65–66 (n = 1)] long; dorsal bar 55–60 (57; n = 3) long. Hook 13–15 (14; n = 4) [12–14 (13; n = 3)] long. Pharynx 39–41 (40; n = 3) [56–57 (n = 1)] wide. MCO 85–109 (97; n = 2) [105–106 (n = 1)] long. Testis 51–63 (59; n = 3) [73–74 (n = 1)] long, 27–42 (35; n = 3) [48–49 (n= 1)] wide. Germarium 53–56 (54; n = 3) [60–61 (n = 1)] long, 45–53 (49; n = 3) [50–51 (n = 1)] wide.

3.4.3. Taxonomic Summary

Type host: Dusky flathead, Platycephalus fuscus Cuvier (Platycephalidae).

Type locality: Moreton Bay off Green Island, Queensland, Australia (27°26′ S, 153°20′ E), 12 January 2016.

Other records: Pl. fuscus: Moreton Bay near Port of Brisbane, Queensland, Australia (27°23’ S, 153°11’ E), 19 January 2016. Pl. endrachtensis: Moreton Bay off Peel Island, Queensland, Australia (27°24’ S, 153°20’ E), 14 January 2016.

Previous record: Pl. fuscus: Moreton Bay, Queensland, Australia as Pseudohaliotrema thysanophrydis (Yamaguti, 1937) Young, 1968 [12].

Infection site: Gill lamellae.

Specimens studied: Holotype, QM G238130; 3 paratypes, QM G238131, HWML 216004, 216005; voucher specimen (from Pl. endrachtensis), HWML 216006; 2 voucher specimens identified as Ps. thysanophrydis by Young [12] from Pl. fuscus, USNM 1356609.

Etymology: The specific name, a noun, is derived from Greek (mastix = a whip) and refers to the shape of the MCO.

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3.4.4. Remarks

Platycephalotrema mastix n. sp. most closely resembles Pt. thysanophrydis (Yamaguti, 1937) n. comb. In both species, the MCO is an elongate tube comprising a minimally to loosely coiled shaft and a slightly expanded base. Platycephalotrema mastix n. sp. differs from Pt. thysanophrydis by having an MCO with a larger diameter throughout its length, shorter anchor roots, a ventral bar with slender flattened ends (ends of ventral bar broadly spatulate in Pt. thysanophrydis), and a dorsal bar with rudimentary ventral limbs of the bifurcated ends (ventral limbs of the dorsal bar of Pt. thysanophrydis massive and bilobed).

Young [12] transferred Ancyrocephalus thysanophrydis Yamaguti, 1937 to Pseudohaliotrema based on five specimens of a dactylogyrid he collected from Pl. fuscus in Moreton Bay, Australia. Young [12] clearly did not have access to Yamaguti’s type specimens when he made the species determination as indicated in the list of specimens examined during his study. However, examination of two voucher specimens that Young [12] deposited in the USNM (1356609) revealed that they belonged to Pt. mastix n. sp. Therefore, the present accounts of Pt. mastix n. sp. on Pl. fuscus in Moreton Bay are not new host or geographic records for the species but represent the first accurate identification of the species from this host and locality.

During the present study, Pt. mastix n. sp. occurred concurrently with Pt. koppa n. sp. on two of the four specimens of Pl. fuscus (prevalence = 50%) and with Pt. austrinum n. sp. on the single specimen of Pl. endrachtensis examined during the survey of the parasites found in the fishes of Moreton Bay, Australia.

3.5. Platycephalotrema austrinum n. sp.

Syns Pseudohaliotrema platycephali of Young [12]; Pseudohaliotrema platicephali of Young [12] (lapsus).

3.5.1. Description (Figure 4)

Greatest width of body proper near midlength of trunk at level of vaginal pore. Cephalic region with well-developed pairs of bilateral and medial cephalic lobes. Eyespots four, apparently lacking lenses; members of posterior pair slightly larger, closer together than those of anterior pair; accessory chromatic granules absent. Pharynx subspherical; esophagus short to absent. Peduncle slightly tapered posteriorly; haptor subtrapezoidal to subrectangular. Anchors similar; each with elongate superficial root, short knob-like deep root, slightly arcing short shaft, elongate point. Ventral bar with slightly expanded spatulate ends. Dorsal bar variable in width along its length, with two posterior humps, bifurcated ends having truncate ventral and dorsal limbs; ventral limb shorter than dorsal limb. Hook with uniform shank and conspicuous protruding thumb; FH loop nearly shank length. MCO with base shaped as an inverted o-choko glass, slightly tapered shaft having complex termination, delicate distal flap. Testis subspherical; proximal vas deferens not observed; seminal vesicle a small fusiform dilation of distal vas deferens lying to right of MCO; ejaculatory duct entering base of MCO. Prostates not observed; prostatic reservoirs large; anterior (ventral) reservoir containing two zones of granules with proximal zone dense, distal zone nearly translucent; posterior (dorsal) reservoir smaller than and partially obscured by anterior reservoir, with comparatively clear contents. Germarium pyriform; oviduct, ootype, Mehlis’ gland, uterus not observed. Vaginal pore located at proximal end of lateral tegumental depression; vaginal vestibule with two posterior sclerotized units, numerous anterior ridges often not visible in individual specimens; vaginal canal not observed. Seminal receptacle apparently absent. Vitellarium dense, coextensive with intestinal ceca; transverse vitelline duct anterior to germarium. Eggs not observed.

3.5.2. Measurements

Body 922–1,203 (1062; n = 2) long; greatest width of trunk 194–251 (222; n = 2). Haptor 150–161 (156; n = 2) wide. Ventral anchor 72–73 (n = 2) long; dorsal anchor 64–72 (68; n = 2) long. Ventral bar 70–71 (n = 2) long; dorsal bar 73–76 (74; n = 2) long. Hook 13–15 (14; n = 2) long. Pharynx 49–57 (53; n = 2) wide. MCO 103–107 (105; n = 2) long. Testis 65–66 (n = 1) long, 54–55 (n = 1) wide. Germarium 71–72 (n = 1) long, 66–67 (n = 1) wide.

3.5.3. Taxonomic Summary

Type host: Bar-tailed flathead, Platycephalus endrachtensis Quoy & Gaimard (Platycephalidae).

Type locality: Swan River Estuary near Perth, Western Australia.

Other record: Pl. endrachtensis: Moreton Bay off Peel Island, Queensland, Australia (27°24’ S, 153°20’ E), 14 January 2016.

Previous records: Platycephalus sp.: Moreton Bay, Queensland, Australia as Pseudohaliotrema platicephali (Yin & Sproston, 1948) Young, 1968 (sic) [12].

Infection site: Gill lamellae.

Specimens studied: Holotype, paratype, BMNH 1984.7.19.69; voucher specimen (from Pl. endrachtensis in Moreton Bay), QM G238132; voucher specimen [collected by P. C. Young from Pl. indicus (now Pl. australis) from Moreton Bay, Queensland, Australia], USNM 1356610; 2 voucher specimens (collected by P. C. Young from Platycephalus sp. from Moreton Bay, Queensland, Australia), USNM 1356611.

Etymology: The specific name (an adjective) is from Latin (austrinus = southern or Australian) and refers to the locations from which the parasite specimens were collected.

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3.5.4. Remarks

The description of Platycephalotrema austrinum n. sp. is based on two of three dactylogyrid specimens collected by Dr. Alan Williams (Western Australian Fisheries, Perth) from Platycephalus endrachtensis in 1984, identified by Dr. Rod Bray (The Natural History Museum, London) as Haliotrema platycephali Yin & Sproston, 1948, and deposited in the BMNH (1984.7.19.69). The third specimen present on the BMNH slide lacks a haptor, possesses a morphologically different MCO, and remains unidentified. A published account of these specimens was not found during the literature search.

Young [12] reported Pseudohaliotrema platycephali (Yin & Sproston) Young, 1968 from Pl. fuscus, Pl. indicus, and an unidentified species of Platycephalus from Moreton Bay, Queensland, Australia. Dactylogyrids deposited by Young [12] in the USNM included one voucher specimen from Pl. indicus (USNM 1356610) and two voucher specimens from Platycephalus sp. (USNM 1356611); none of his specimens from Pl. fuscus were apparently submitted to the USNM for deposition. Examination of the available voucher specimens revealed that those from Platycephalus sp. were conspecific with Pt. austrinum n. sp. and that Young’s specimen from Pl. indicus could not be identified but may represent an undescribed species. Finally, it should be mentioned that the platycephalid fishes of Australia recently have undergone significant taxonomic revision [13] and that those previously identified as Pl. indicus from the Moreton Bay area are now Pl. australis Imamura.

During the present study, a single specimen of Pt. austrinum n. sp. was collected from the gills of Pl. endrachtensis from Moreton Bay. Although this finding represents the first recorded occurrence of the nominal species in the bay, it technically does not represent a new geographic record for the parasite. Young’s [12] report of Ps. platycephali (now Pt. austrinum n. sp.) serves as the first recorded occurrence of the species in the bay.

3.6. Platycephalotrema macassarensis (Yamaguti, 1963) n. comb.

Syns Ancyrocephalus platycephali Yamaguti, 1953; Ancyrocephalus macassarensis Yamaguti, 1963; Haliotrema macassarensis (Yamaguti, 1963) Bychowsky & Nagibina, 1971; Haliotrema macassariensis of Bychowsky & Nagibina [11] (lapsus).

3.6.1. Measurements

Body 663–838 (750; n = 2); greatest width of body proper (anterior trunk) 127–142 (135; n = 2). Haptor 125–155 (140; n = 3) wide. Ventral anchor 61–66 (64; n = 3) long; dorsal anchor 56–59 (58; n = 3) long. Ventral bar 60–63 (61; n = 3) long; dorsal bar 60–68 (65; n = 3) long. Hook 12–13 (n = 4) long. Pharynx 36–43 (40; n = 3) wide. MCO 62–64 (63; n = 3) long. Testis 81–82 (n = 1) long, 42–43 (n = 1) wide. Germarium 49–50 (n = 1) long, 50–51 (n = 1) wide.

3.6.2. Taxonomic Summary

Type host: Bartail flathead, Platycephalus indicus (Linnaeus) (Platycephalidae).

Type locality: Macassar, Celebes.

Previous records: Pl. indicus: Macassar, Celebes as Ancyrocephalus platycephali Yamaguti, 1953 [14]; South China Sea off Hainan, China as Haliotrema macassariensis Yamaguti, 1963 (lapsus) [11]; Guangdong Province, China as Haliotrema macassarensis [15].

Infection site: Gill lamellae.

Specimens studied: 3 syntypes, Ancyrocephalus platycephali Yamaguti, 1953, MPM 23204 (SY6718; labeled paratypes: Notes on the slide containing the three specimens indicate that paratypes of Ancyrocephalus platycephali Yamaguti, 1953 were present. However, Yamaguti [14] did not specifically identify a holotype or paratypes for this species. According to Dr. K. Ogawa (personal communication), personnel at the MPM designated the specimen drawn as the whole mount by Dr. Yamaguti as the holotype and the remaining specimens were considered the paratypes, which is against the rules presented in the International Code of Zoological Nomenclature (ICZN) [16]. The specimens on which the original description was based are all syntypes according to Article 73 of the ICZN).

3.6.3. Remarks

This species was originally described as Ancyrocephalus platycephali by Yamaguti [14]. In order to remove secondary homonymy, Yamaguti [17] renamed the species A. macassarensis when he transferred the senior Haliotrema platycephali Yin & Sproston, 1948 to Ancyrocephalus. Later, Bychowsky & Nagibina [11] transferred A. macassarensis and returned A. platycephali of Yin & Sproston [10] to Haliotrema. Retention of “macassarensis” for the specific name of Yamaguti’s species was required after Bychowsky & Nagibina’s [11] taxonomic acts, because the two helminth species remained congeners.

Haliotrema macassarensis is now transferred to Platycephalotrema as Pt. macassarensis (Yamaguti, 1963) n. comb. based on the presence of two large prostatic reservoirs, tandem gonads, a dextral vaginal pore, a large vaginal vestibule, a copulatory complex lacking an accessory piece, and a haptoral armament morphologically similar to that of other species currently assigned to the genus (Figure 5). Neither Yamaguti [14] nor Bychowsky & Nagibina [11] reported the presence of haptoral reservoirs associated with the ventral or dorsal anchors, and examination of the three syntypes did not clearly reveal their presence. Yamaguti [14] mentioned two “muscle bundles” lying near the “end of the dorsal (superficial) root of the dorsal hook (anchor)” in the original description, but no such structures were depicted by Bychowsky & Nagibina [11]. In the available syntypes of A. platycephali Yamaguti, 1953, the structures referenced by Yamaguti [14] were visible and appeared to contain comparatively course fibers that differed from the muscle fibers of muscles entering the haptor from the peduncle. Nonetheless, it was unclear in the syntypes if the structures mentioned by Yamaguti [14] are muscle bundles or vesicles containing fibrous secretions.

Bychowsky & Nagibina [11] recorded H. macassarensis from Pl. indicus in the South China Sea off Hainan, while the type locality of the species (Macassar, Celebes) lies approximately 5,700 km distant. Within the Indo-Pacific Region, Puckridge et al. [2], looking at cryptic diversity between populations of flatheads, recognized that eight lineages of Pl. indicus existed using COI barcoding and that specimens of Pl. indicus from the northwest Pacific (including the waters off Korea, Japan, and China) showed major genetic differences from those collected from Indonesia. These findings suggested that the platycephalid hosts of the dactylogyrids from off Hainan, China and off Macassar may represent different, albeit cryptic, flathead species. Concordantly, the helminths reported by Yamaguti [14] and Bychowsky & Nagibina [11] may also represent different but morphologically similar species, an idea probably requiring molecular analyses of the helminths from the two locations for confirmation.

Comparison of Bychowsky & Nagibina’s [11] drawings with the available syntypes of A. platycephali Yamaguti, 1953 showed minimal morphological differences between the Russian account and the syntypes. However, Bychowsky & Nagibina [11] depicted a series of fine lines associated with the terminal half of the MCO in their figure 2B, whereas similar lines were not mentioned or shown in the original description by Yamaguti [14]. However, our examination of the syntypes of A. platycephali Yamaguti, 1953 revealed that the lines shown by Bychowsky & Nagibina [11] likely represented thin apparently sclerotized ridges occurring along or within the wall of the genital atrium rather than being directly associated with the MCO.

3.7. Platycephalotrema thysanophrydis (Yamaguti, 1937) n. comb.

Syns Ancyrocephalus thysanophrydis Yamaguti, 1937; Haliotrema thysanophrydis (Yamaguti, 1937) Bychowsky & Nagibina, 1971; Haliotrema thysanophridis (Yamaguti, 1937) Bychowsky & Nagibina, 1971 (lapsus).

3.7.1. Redescription (Figure 6)

Greatest width of body proper in posterior trunk or near midlength of trunk. Cephalic region with well-developed pairs of terminal and bilateral cephalic lobes. Eyespots usually absent; numerous free chromatic granules in cephalic region. Pharynx subspherical; esophagus short to absent. Peduncle short, slightly tapered posteriorly; haptor subhexagonal, with three bilateral pairs of lobes each containing haptoral hook near tip. Ventral and dorsal anchors similar; each with elongate superficial root, short deep root, slightly arcing short shaft, elongate point. Ventral bar bowed, with broad spatulate ends. Dorsal bar with globose bilobed subterminal ventral limbs, flattened dorsal terminal limbs. Hook with uniform shank and protruding depressed thumb; FH loop nearly shank length. MCO with small fusiform base having proximal collar, delicate slightly coiled shaft recurved distally. Testis ovate to subspherical; proximal vas deferens not observed; seminal vesicle a small fusiform dilation of distal vas deferens lying to left of distal portion of MCO; ejaculatory duct directed posteriorly from seminal vesicle to base of MCO dorsal to prostatic reservoirs. Prostates not observed. Prostatic reservoirs large, overlying each lying each other to right of MCO; ventral reservoir containing dense staining secretory product; dorsal reservoir often obscured by ventral prostatic reservoir, containing nearly translucent contents. Germarium variable in shape, displaced to right side of body immediately anterior to testis. Oviduct, ootype, Mehlis’ gland, uterus, seminal receptacle not observed. Vaginal pore dextral; vaginal vestibule large, often extending to left intestinal cecum, lacking sclerotized components; vaginal canal not observed. Vitellarium dense, coextensive with intestinal ceca; transverse vitelline duct anterior to germarium. Eggs not observed.

3.7.2. Measurements

Body 697–1,088 (918; n = 25); greatest width of body proper 155–272 (220; n = 25). Haptor 158–216 (181; n = 25) wide. Ventral anchor 79–89 (85; n = 24) long; dorsal anchor 84–100 (92; n = 22) long. Ventral bar 64–78 (72; n = 13) long; dorsal bar 71–98 (83; n = 14) long. Hook 12–13 (n = 14) long. Pharynx 40–56 (47; n = 23) wide. MCO 120–164 (148; n = 17) long. Testis 100–207 (159; n = 23) long, 102–194 (139; n = 24) wide. Germarium 48–118 (82; n = 24) long, 51–107 (80; n = 24) wide.

3.7.3. Taxonomic Summary

Type host: Japanese flathead, Thysanophrys japonicus (Tilesius) [now Inegocia japonica (Cuvier), a possible mis-identification of Cociella crocodilus (Cuvier) (see Remarks)] (Platycephalidae).

Type locality: Tarumi, Hyogo Prefecture, Japan.

Previous records: T. japonicus (= Inegocia japonica): Inland Sea near Tarumi, Hyogo Prefecture, Japan, 3 August 1936 [18]. Cocius crocodilus (Tilesius) [as Coccius crocodilus (Tilesius) (lapsus); now Cociella crocodilus]: Yellow Sea as Haliotrema thysanophridis (Yamaguti, 1937) Bychowsky & Nagibina, 1971 (sic) [11].

Current records: Cociella crocodilus [standard Japanese name is “Ine-gochi” (イネゴチ) and known within the local region as “Me-kochi” (メコチ)]: Seto Inland Sea, Hiuchi-nada, Imabari City, Ehime Prefecture (purchased at the market of the Imabari Fishery Cooperative), Japan (34°06’ N, 133°21’ E), 23 June 2015; Seto Inland Sea, Utsumi-chō, off Yoko-shima Island, Fukuyama City, Hiroshima Prefecture, Japan (34°21.5’ N, 133°16.5’ E), 19 February 2017, 26 February 2019. Inegocia ochiaii Imamura [host identified as “Wani-gochi” (ワニゴチ) in MPM records and collected by Dr. Kusuo Iwata (Fukuoka University)]: Sea of Japan, off Kyushu (coordinates not available), Japan, 10 May 1978.

Infection site: Gill lamellae.

Specimens studied: 4 syntypes, MPM 23107 (SY0262); 47 voucher specimens, MPM 21470, 21471, 21521, QM G238133, HWML 216007; 5 voucher specimens (collected by Dr. K. Iwata), MPM 31090 (F0287–0291).

3.7.4. Remarks

Platycephalotrema thysanophrydis is currently known to parasitize three species of platycephalid fishes. Yamaguti [18] described the species from the gills of the Japanese flathead Thysanophrys japonicus (Tilesius) (now Inegocia japonica) from the Seto Inland Sea off Tarumi, Hyogo Prefecture, Japan. However, the name of the host was written, presumably by Dr. Yamaguti, as メコチ (= “Me-kochi”) on the slide label of the syntypes (MPM 23107). While the Japanese flathead and the crocodile flathead Cociella crocodilus are sympatric in the Seto Inland Sea, the local Japanese name “Me-kochi” currently refers to the latter species and not to I. japonica within the region from which Yamaguti [18] collected the fish host (see [19]). The helminth was subsequently reported from the crocodile flathead from the Yellow Sea off China by Bychowsky and Nagibina [11], and during the course of the present study, it was found on the gill lamellae of this flathead from the Seto Inland Sea of Japan.

The search for other published or unpublished records of dactylogyrids infesting flatheads resulted in the finding of five specimens of a dactylogyrid deposited by Dr. K. Iwata (Fukuoka University) in the collection of the Meguro Parasitological Museum (MPM 31090); these specimens also were identified herein as Pt. thysanophrydis. Museum records indicate that Dr. Iwata collected his specimens from a fish locally known as “Wani-gochi” (ワニゴチ), which recently was described as Inegocia ochiaii Imamura by Imamura [20]. Whereas the three species of flatheads currently recorded as hosts for Pt. thysanophrydis have overlapping geographic ranges (see [21]) and assuming all previous host identifications were correctly determined, Pt. thysanophrydis is the only species of Platycephalotrema known to infect fishes assigned to more than one platycephalid genus, and its occurrence on I. ochiaii represents a new host record for the species. It should be mentioned, however, that the taxonomy of some flathead fishes has recently undergone significant revision and that identification of many platycephalid species is often difficult, suggesting that a re-examination of the dactylogyrids infecting the two previously mentioned species of Inegocia should be conducted in order to confirm the comparatively low host specificity exhibited by Pt. thysanophrydis.

Young [12] identified a dactylogyrid from the gills of Pl. fuscus from Moreton Bay, Queensland, Australia, as Pseudohaliotrema thysanophrydis (Yamaguti, 1937) Young, 1968. Examination of two of Young’s voucher specimens deposited in the USNM (1356609) revealed that the identification of the parasite as Ps. thysanophrydis was erroneous, and that the specimens instead represented Pt. mastix n. sp. Platycephalotrema thysanophrydis is differentiated from Pt. mastix sp. n. by having an elongate uniform shaft of the MCO, while that of Pt. mastix sp. n. has a comparatively larger diameter and a short keel along the outer surface near its midlength (compare Figure 3d and Figure 6d).

3.8. Platycephalotrema platycephali (Yin & Sproston, 1948) n. comb.

Syns Haliotrema platycephali Yin & Sproston, 1948; Ancyrocephalus platycephali (Yin & Sproston, 1948) Yamaguti, 1963; Pseudohaliotrema platycephali (Yin & Sproston, 1948) Young, 1968; Pseudohaliotrema platicephali and Haliotrema platicephali both of Young [12] (both lapsus).

3.8.1. Taxonomic Summary

Type host: Bartail flathead, Platycephalus indicus (Linnaeus) (Platycephalidae).

Type locality: Chusan Region of the East China Sea, China.

Previous records: Pl. indicus: Chusan Region of the East China Sea, China [10]; South China Sea off Shanghai, China [11]; Fujian, Guangdong, Guangxi, China [15]; Weihai, Shangdong Province, China [22]. Pl. fuscus: Moreton Bay, Queensland, Australia [12,23].

Infection site: Gill lamellae.

3.8.2. Remarks

This species was described as Haliotrema platycephali by Yin & Sproston [10] from the gills of Platycephalus indicus collected from the Chusan Region of the South China Sea. Bychowsky & Nagibina [11] subsequently reported the species from the same host in the South China Sea off Shanghai. Haliotrema platycephali was herein transferred to Platycephalotrema based on it having two large prostatic reservoirs each emptying separately into the base of the MCO, tandem gonads, a dextral vaginal pore, a large vaginal vesicle, a copulatory complex lacking an accessory piece, paired haptoral vesicles associated with the dorsal anchors, and the common features of the haptoral armament. It differs from all of its congeners by the complex distal end of the MCO (see figure 28 in [10]; figure 1B in [11]).

The report of Pt. platycephali by Bychowsky & Nagibina [11] in China appears to be the only valid account of the species since its original description by Yin & Sproston [10]. Young’s [12] report of the species (as Pseudohalitotrema plalticephali) on Pl. fuscus from Moreton Bay, Australia, is likely erroneous. During the present study, the species was not found parasitizing the four specimens of Pl. fuscus examined for dactylogyrids from Moreton Bay.

3.9. Platycephalotrema sinensis (Yamaguti, 1963) n. comb.

Syns Ancyrocephalus thysanophrydis of Yin & Sproston [10] (nec Yamaguti [18]); Ancyrocephalus sinensis Yamaguti, 1963.

3.9.1. Taxonomic summary

Type host: Spotted flathead, Platycephalus punctatus Cuvier [now Cociella punctata (Cuvier)] (Platycephalidae).

Type locality: Sen-Chia-Men, Chusan Region, East China Sea, China.

Previous record: There have been no other records except that of Yin & Sproston [10].

Infection site: Gill lamellae.

3.9.2. Remarks

Yin & Sproston [10] reported Ancyrocephalus thysanophrydis from the spotted flathead collected from the Chusan Region of the East China Sea. Yamaguti [17] believed that Yin & Sproston’s specimens were not conspecific with those he described in 1937 as A. thysanophrydis and, as a result, renamed the former specimens A. sinensis. Yamaguti [17] listed the following reasons for the renaming of Yin & Sproston’s specimens: 1) differences in the structure of the dorsal bar (differences not specified); 2) the presence of two prostatic reservoirs (one reported by Yamaguti [18], but see the description and remarks herein for Platycephalotrema thysanophrydis); and 3) the presence of a genitointestinal canal (genitointestinal canal not mentioned, presumed absent in A. thysanophrydis by Yamaguti [18]). Yamaguti [17] apparently had in mind additional differences as indicated by his use of “etc.” at the end of his list, but these were not provided in his justification for the renaming.

Although the features used to differentiate A. sinensis from A. thysanophrydis on the surface appear to justify Yamaguti’s [17] actions, the two nominal species nonetheless may be synonyms. Yin & Sproston [10] did not examine the type specimens of A. thysanophrydis for comparison. As a result, they had some doubt that their specimens were conspecific with this species when they stated that “the dorsal bar has its ends deeply tri-fid…; the upper ramus is bent slightly forwards, and the two lower point obliquely backwards in different planes,” whereas Yamaguti [18] simply described the dorsal bar as being straight. However, examination of the two available syntypes of A. thysanophrydis revealed that the dorsal bars are straight with tri-fid ends (ventral limb actually bilobed) similar to that described by Yin & Sproston [10]. The shape of the dorsal bar in the available voucher specimens of Pt. thysanophrydis from Japan conforms to that shown by Yin & Sproston [10] (compare Figure 6c with figure 25 in Yin & Sproston [10]). While two prostatic reservoirs were not visible in the two syntypes, both were observed in the voucher specimens collected from Cociella crocodilus from Japan during the present study. In the latter specimens, the posterior (dorsal) reservoir contained a nearly transparent material that often-precluded observation of the vesicle, further suggesting that this vesicle was missed by Yamaguti [18]. Finally, the presence of a genitointestinal canal as reported by Yin & Sproston [10] for their specimens is clearly erroneous. A genitointestinal canal is an apparent synapomorphy for the Infrasubclass Oligonchoinea (see [24,25]), whereas it does not occur in members of the Subclass Polyonchoinea, to which dactylogyrid species belong [26,27]. Thus, there is a high probability that Pt. sinensis is a synonym of Pt. thysanophrydis. In order to minimize potential synonyms, however, formal proposal of synonymy is not made pending new collections of dactylogyrids infecting the spotted flathead.

3.10. Platycephalotrema bassensis (Hughes, 1928) n. comb.

Syn. Ancyrocephalus bassensis Hughes, 1928.

3.10.1. Taxonomic Summary

Type host: Southern sand flathead, Platycephalus bassensis Cuvier (Platycephalidae).

Type locality: Port Phillip Bay, Australia.

Previous records: Pl. bassensis: Port Phillip Bay, Australia [28]. Murray [29] reported this species from Pl. bassensis but did not provide a specific locality from which the host and its parasite were collected other than indicating in the introduction to the paper that most of the fishes were from “Southern Australian waters.” However, Murray [29] described two other parasites from Pl. bassensis which she clearly indicates were from Port Phillip Bay, Victoria, Australia. It seems likely, therefore, that her specimens of A. bassensis also originated from this locality.

Infection site: Gill lamellae.

3.10.2. Remarks

Specimens of this species were not available for study. Attempts to locate the type specimens used by Hughes [28] for the description of the species and the voucher specimens reported by Murray [29], included inquiries to the Queensland Museum (Brisbane), Museums Victoria (Melbourne), South Australian Museum (Adelaide), Australian Museum (Sydney), and The Natural History Museum (London). All attempts were unsuccessful.

Inconsistencies regarding the dorsoventral axis of the body in the respective descriptions and figures exist in both accounts of the species by Hughes [28] and Murray [29]. For example, in her figure 3 (labeled a ventral view), Hughes [28] shows the so-called prostate (apparently a prostatic reservoir) lying to the right of the MCO, while in the description she states that the structure lies to the left of the penis. In her figure 3, the vas deferens and seminal vesicle are shown to be within the left side of the body (as occurs in other dactylogyrids), but the germarium is suggested to dorsally overlap the anterior end of the testis (germarium usually ventral to testis in other dactylogyrids with overlapping gonads). Similar inconsistencies occur in the account of the species provided by Murray [29]. Here, she states that the vas deferens is “slightly to the right” and joins the seminal vesicle on the right side of the body (opposite that reported by Hughes [28] and what usually occurs in other dactylogyrids); she describes two ducts arising from the seminal vesicle, one of which extends directly to the base of the MCO, while the other duct passes to the right side of the MCO where it joins a small rounded body (labeled an accessory vesicular seminalis). However, in her figures 2 and 10, the accessory vesicular seminalis lies to the left of the MCO, assuming the figures are in ventral views. In the description, Murray [29] reports two prostatic glands (= prostatic reservoirs) (position not provided), but shows them to be to the left of the MCO in her figures 2 and 10. Similar to the report of Hughes [28], her figures 2 and 10 suggest that the germarium dorsally overlaps the testis and that the uterus lies dorsal to the vas deferens (uterus ventral to the ducts of the male reproductive system in other dactylogyrids).

These inconsistencies clearly demonstrate the need for a redescription of the species. Nonetheless, Ancyrocephalus bassensis is transferred to Platycephalotrema as Pt. bassensis (Hughes, 1928) n. comb., based on the presence of two prostatic reservoirs [29]; tandem, slightly overlapping gonads; and a dextral vaginal pore (assuming the dorsoventral axes reported by Hughes [28] and Murray [29] are erroneously depicted), a large vaginal vestibule, and absence of an accessory piece in the copulatory complex.

3.11. Dactylogyrids from Scorpaeniform Fishes that Are Potential Members of Platycephalotrema n. gen.

3.12. Ancyrocephalus vesiculosus Murray, 1931

3.12.1. Measurements

Body 716–946 (808; n = 5); greatest width of trunk 160–231 (190; n = 7). Haptor 139–161 (150; n = 5) wide. Ventral anchor 46–49 (47; n = 4) long; dorsal anchor 43–47 (45; n = 3) long. Ventral bar 49–52 (51; n = 3) long; dorsal bar 49–51 (50; n = 4) long. Hook 12–14 (13; n = 6) long. Pharynx 39–52 (46; n = 7) wide. MCO 36–49 (42; n = 7) long. Testis 57–99 (85; n = 6) long, 75–119 (98; n = 6) wide. Germarium 49–73 (65; n = 4) long, 35–56 (43; n = 4) wide.

3.12.2. Taxonomic Summary

Type host: Southern sand flathead, Platycephalus bassensis Cuvier (Platycephalidae).

Type locality: Port Phillip Bay, Victoria, Australia.

Previous record: There have been no previous records other than that of the original description by Murray [29]. Hooper [30] lists Pl. arenarias Ramsay & Ogilby (now Pl. endrachtensis, see [31]) as a host for A. vesiculosus in his Appendix 1 (Checklist of parasites from Australian flathead fishes), where he erroneously credits Murray [29] and Yamaguti [17] for the record. However, no published accounts of Pl. arenarias or Pl. endrachtensis serving as hosts for this parasite were found during an exhaustive literature search.

Infection site: Gill lamellae.

Specimens studied: 9 syntypes (7 whole-mounts and 2 transversely sectioned syntypes), Museums Victoria, Melbourne, Victoria, Australia (MV) F60389.

3.12.3. Remarks

Ancyrocephalus vesiculosus could not be assigned to Platycephalotrema with certainty. Murray [29] collected this species from two of “about” 50 Platycephalus bassensis she examined from Port Phillip Bay in southern Australia. The species was described as having the usual number and distribution of haptoral sclerites found in dactylogyrids, four haptoral vesicles lying in relation to the anchors, tandem gonads (testis post-germarial), a trilobed prostate (prostatic reservoirs were not mentioned), a chitinous tube lying in connection with the MCO, and a vaginal pore on the left side of the body just anterior to the germarium.

Examination of the available syntypes of A. vesiculosus confirmed the presence of four haptoral vesicles, the number and position of the hooks and anchor/bar complexes in the haptor (Figure 7), and presence of tandem gonads, but the presence of the trilobed prostate could not be confirmed. It appears that the dorsoventral axis of the helminth was reversed in the original description. Although the vaginal pore and vestibule were difficult to see in the syntypes, an indication of the former on the right side of the body was present. That the dorsoventral axis of the body was reversed in the original description was further supported by Murray’s drawing of the whole mount showing the vas deferens along the right side of the body (vas deferens usually extending along the left side of the body in dactylogyrids) and the germarium ventrally overlain by the testis (testis usually dorsal to the germarium in dactylogyrids).

Murray [29] described a “chitinous tube” ventral to the MCO as indicated in her figure 1A of the copulatory complex. The nature and function of the tube was not determined in the available syntypes, although it did not appear to be “chitinous” (or sclerotized) as stated by Murray [29]. It may represent a descending portion of the ejaculatory duct, but this requires confirmation.

The original description of this species was apparently based on more specimens than the seven whole mounts and two transversely sectioned syntypes that were available for study. None of the available syntypes represented the specimen on which Murray’s whole-mount drawing was based, and Murray [29] did not indicate the total number of specimens available to her. Based on the above observations, this species clearly requires redescription in order to determine its taxonomic position within the Dactylogyridae.

3.13. Haliotrema indicum Tripathi, 1957

Syn. Ancyrocephalus indicum (Tripathi, 1957) Yamaguti, 1963.

3.13.1. Taxonomic Summary

Type host: Bartail flathead, Platycephalus insidiator (Forsskål) [now Pl. indicus (Linnaeus)] (Platycephalidae).

Type locality: Estuary of Matla River at Canning and Hooghly River, India.

Previous record: There have been no other records except that of the original description [32].

Infection site: Not indicated (probably gill lamellae).

3.13.2. Remarks

Specimens of this species were not available, and the type specimens apparently have not survived (see [33,34]). The original description of Haliotrema indicum is inadequate, and if valid, the species requires redescription. Tripathi [32] indicated in his remarks that H. indicum most closely resembled H. platycephali of Yin & Sproston [10], differing from it in the morphology of the vagina and in the size of the MCO. Tripathi [32] described the vagina of H. indicum as a “bowl-shaped structure, whose outer margin is frayed.” Although Yin & Sproston [10] mention the presence of a vagina, they did not provide a detailed description of it, while stating that the female ducts were obscured by the cells of the vitelline field. Yin & Sproston’s [10] whole-mount drawing also showed no details of the vagina or vaginal vestibule, suggesting that Tripathi’s use of it for differentiating H. indicum from Yin & Sproston’s species lacks merit.

That both H. indicus and H. platycephali were described from the same host, that Tripathi’s descriptive account lacks specificity, and that the drawing of the MCO provided by Tripathi [32] in his whole-mount figure of H. indicus superficially resembles that provided by Yin & Sproston [10] for H. platycephali, suggests that the two species are synonyms. Formal proposal of synonymy, however, must await new collections of the dactylogyrids parasitizing Pl. indicus in both China and India.

3.14. Haliotrema swatowensis Yao, Wang, Xia, & Chen, 1998

3.14.1. Taxonomic Summary

Type host: Bartail flathead, Platycephalus indicus (Linnaeus) (Platycephalidae).

Type locality: South China Sea, off Nanao Island, Guangdong Province, China.

Previous record: There has been no other record except that of the original description [35].

Infection site: Gill lamellae.

3.14.2. Remarks

The type specimens of this species were not available for study. Haliotrema swatowensis represents the fourth dactylogyrid species recorded from the bartail flathead and the second from this host in the South China Sea. Other species include H. platycephali (now Platycephalotrema platycephali), Ancyrocephalus macassarensis (now Pt. macassarensis), and H. indicum. The original description of H. swatowensis is comprised solely of measurements of the body, pharynx, and haptoral and copulatory structures and drawings of the haptoral sclerites, MCO, and vagina. Yao et al. [35] differentiated H. swatowesis from H. platycephali by stating that the two species differed “in the structure and size of the copulatory organ.” However, the MCO of H. swatowensis depicted by Yao et al. [35] resembles that of H. platycephali as depicted by Yin & Sproston [10] and Bychowsky & Nagibina [11]. Finally, Yao et al. [35] showed jagged (or frayed) margins in their drawing of the vagina, which resembled the frayed vaginal margin mentioned by Tripathi [32] for H. indicum. These observations suggested that Pt. platycephali, H. indicum, and H. swatowensis were possible synonyms (see also the Remarks for H. indicum above). However, determination of synonymy among these nominal species would require a more extensive collection of the dactylogyrid parasites infecting Pl. indicus from throughout its geographic range. Platycephalotrema macassarensis is excluded from this group of species by having a simple tubular termination of the MCO.

3.15. Haliotrema pteroisi Paperna, 1972

3.15.1. Taxonomic Summary

Type host: Red lionfish, Pterois volitans (Linnaeus) [a probable mis-identification of the devil firefish, Pterois miles (Bennett)] (Scorpaenidae).

Type locality: Southwest Gulf of Eilat (Gulf of Aqaba).

Previous record: There have been no other records except that of the original description [36].

Infection site: Gill lamellae.

3.15.2. Remarks

Although its host is not a member of the Platycephalidae, this species was included among the potential members of Platycephalotrema because of its similar haptoral sclerites to those of species presently assigned to the genus, presence of a dextral vaginal pore, and absence of an accessory piece in the copulatory complex. Paperna [36] did not mention the presence of prostatic reservoirs in this species, which at this time prevented transfer of the species to Platycephalotrema.

Colorni & Diamant [37] reported an unidentified species of Haliotrema on the gills of the devil firefish, Pterois miles (Bennett), collected from “Eilat’s North Beach,” and Tuttle et al. [38] found Haliotrema sp. on the gills of red lionfish, Pterois volitans, from the Philippines. No mention was made in either of these papers that voucher specimens of the respective helminths were deposited in a museum collection, and a direct attempt to obtain specimens from Dr. Tuttle failed. Thus, new collections of the dactylogyrids infecting P. miles and P. volitans will be necessary to determine the generic placement of H. pteroisi within the Dactylogyridae.

As far as we know, H. pteroisi is the only other identified dactylogyrid species known to parasitize a marine scorpaeniform fish.

Finally, it should be mentioned that the type host of H. pteroisi was likely mis-identified by Paperna [36] as P. volitans. Pterois volitans is apparently restricted to the waters of the western Pacific and eastern Indian Ocean. In the waters of the western Indian Ocean including that of the Gulf of Eilat, P. volitans is replaced by P. miles [21].

4. Discussion

The Dactylogyridae includes several genera that have become known as “taxonomic wastebaskets,” each containing generally nondescript species lacking unique features that would allow their reassignment within the family. Among these genera are Ancyrocephalus and Haliotrema, both of which have long been known or suspected to be unnatural. In 1955, Gussev [39] recommended that Ancyrocephalus be referred to as “sensu lato” because of its wide range of species infecting both marine and freshwater fishes (50+ species according to Bychowsky & Nagibina [40]. Bychowsky and Nagibina [40] provided a diagnosis for Ancyrocephalus (sensu stricto), to which they assigned only two of the 50+ species to the genus: Ancyrocephalus paradoxus Creplin, 1839 and Ancyrocephalus percae Ergens, 1966, both infecting freshwater percid fishes of the Palearctic. Similarly, Haliotrema, with approximately 150 nominal species infecting marine fishes assigned to 33 teleost families representing six orders: the Perciformes, Tetraodontiformes, Ophidiiformes, Scorpaeniformes, Siluriformes, and Beryciformes [41], was characterized as a taxonomic wastebasket by Klassen [42]. Unlike Ancyrocephalus, however, determination of the taxonomic boundaries of Haliotrema (sensu stricto) has not been accomplished.

Recent proposals of new dactylogyrid genera have narrowed Haliotrema and reduced the number of species assigned to Ancyrocephalus (sensu lato). The proposal herein of Platycephalotrema n. gen. and transfer of five species previously assigned to Ancyrocephalus and/or Haliotrema has further reduced the diversity of species in the two genera. These actions followed the proposals of Ligophorus Euzet & Suriano, 1977 for two previously described species of Haliotrema [43]; Euryhaliotrema Kritsky & Boeger, 2002 for nine previously described species of Haliotrema [44]; Euryhaliotrematoides Plaisance & Kritsky, 2004 (now Euryhaliotrema) for three previously described species of Haliotrema [45]; Haliotrematoides Kritsky, Yang, & Sun, 2009 for 15 previously described species of Haliotrema [46]; and Lethrinitrema for three previously described species of Haliotrema [9]. Three additional species of Haliotrema and one species previously assigned by various authors to Haliotrema and Ancyrocephalus were transferred to Euryhaliotrema, and a species of Haliotrema was transferred to Haliotrematoides by Kritsky [47], further reducing the number of species assigned to the genus. The proposals of Volsellituba Řehulková, Justine, & Gelnar, 2010 and Pennulituba Řehulková, Justine, & Gelnar, 2010 by Řehulková et al. [48] have further limited the taxonomic borders of Haliotrema (sensu lato) and Ancyrocephalus (sensu lato) by preventing the assignments of these and other unrelated species to these genera.

Ancyrocephalus (sensu stricto) as proposed by Bychowsky & Nagibina [40] appears to represent a natural taxon, although further investigation is needed to determine if additional nominal species should be included within it. On the other hand, the absence of a clear definition of Haliotrema (sensu stricto) continues to hinder the understanding of the relationships among the remaining species assigned to it. While proposal of new genera, such as Platycephalotrema n. gen., might continue to reduce the unnatural composition of Haliotrema, investigations to define the genus in its strict sense are required. Until this is achieved, new species lacking well-defined or unique characteristics will likely continue to be added to the genus, further complicating the taxonomy of the taxon.