FOLIA PARASITOLOGICA 54: 203–207, 2007

Haliotrema banana sp. n. (Monogenea: Ancyrocephalidae) from Bodianus perditio (Perciformes: Labridae) off New Caledonia

L.H.S. Lim1 and Jean-Lou Justine2

1Institute of Biological Sciences, University of Malaya, Kuala Lumpur, 50603, Malaysia; 2Équipe Biogéographie Marine Tropicale, Unité Systématique, Adaptation, Évolution (CNRS, UPMC, MNHN, IRD), Institut de Recherche pour le Développement, BP A5, 98848 Nouméa Cedex, Nouvelle-Calédonie

Key words: Monogenea, Ancyrocephalidae, Haliotrema banana, Bodianus perditio, Labridae, New Caledonia

Abstract. Sixteen labrid species, including four Bodianus spp., were examined in New Caledonia (South Pacific) and monogene- ans were found only on Bodianus perditio (Quoy et Gaimard). This species, Haliotrema banana sp. n., is the second Haliotrema species to be described from the labrids, the first being Haliotrema bodiani Yamaguti, 1968 from Bodianus albotaeniatus (Valenciennes), previously designated as B. bilunulatus (Lacépède). The new species is similar to H. bodiani in soft reproductive parts but differs from it in the morphologies of the hard haptoral parts, mainly in the shape of the dorsal bar (bar-shaped vs V- shaped in H. bodiani) and ventral bar. It is similar to Haliotrema spirale Yamaguti, 1968 and Haliotrema minutospirale Yama- guti, 1968 in the shape of the anchors and bars but differs from them in the detailed structures of the copulatory organ and vagi- nal system.

The family Labridae includes fishes commonly the third ancyrocephalid species described from a labrid known as and is the second largest family of species. fish after Gobiidae with 68 genera and 453 species (Randall 2005). In New Caledonia alone, 114 species MATERIALS AND METHODS have been recorded (Fricke and Kulbicki 2006). Al- Specimens of the labrids were caught with hand lines on though the Labridae includes many aquarium fish spe- board R/V “Coris” in various places off the barrier reef, cies, records of monogeneans from labrids are rare and Nouméa, New Caledonia at a distance of about 20–30 km thus far only two species of ancyrocephalids belonging from the shore, in depths of 20–40 m. Live fishes were kept in to two genera, two species of capsalids from two genera a container with sea water and immediately brought back to and one species of microcotylid have been recorded. the laboratory. Gills were extracted and examined in sea water The two ancyrocephalids are Haliotrema bodiani Ya- under a dissecting microscope. Live monogeneans were indi- maguti, 1968 from Bodianus albotaeniatus (Valen- vidually picked up from the gills with fine needles and imme- ciennes) (previously designated as B. bilunulatus) off diately processed. Some monogeneans were flattened on a Hawaii and Sinodiplectanotrema argyrosomus Zhang, slide under a coverslip with a light weight on top and fixed in Yang et Liu, 2001 [type host Argyrosomus aureus, now 70% ethanol. These were later stained in carmine as given in known as Pennahia anea (Bloch) (Sciaenidae)] from Justine (2005). A few specimens were prepared with ammo- Halichoeres nigrescens, off the island of Hainan, China. nium picrate glycerine. Some specimens were collected from The two capsalids are Benedenia bodiani Yamaguti, formalin-fixed gills of B. perditio and monogeneans were 1968 from Bodianus albotaeniatus, off Hawaii and fixed and cleared in ammonium picrate glycerine. Some of these ammonium picrate glycerine fixed specimens were Neobenedenia melleni (MacCallum, 1927) from Bo- washed several times in distilled water to remove the fixative dianus rufus (Linnaeus), while the microcotylid, Micro- and then stained in Gomori’s triple stain. The monogeneans cotyle donavini van Beneden et Hesse, 1863 was col- were drawn with a microscope equipped with a camera lucida. lected from Labrus bergylta Ascanius (junior synonym Drawings were scanned and redrawn on a computer with L. donovani Valenciennes) in the Atlantic, off Europe Adobe Illustrator. Some images were taken using a Leica digi- and on Symphodus mediterraneus Linnaeus in the Medi- tal camera using Leica image analysis software (QWin Plus). terranean Sea (see Yamaguti 1968, Radujkovic and Eu- All measurements (see Fig. 1) were taken on flat specimens zet 1989, Whittington and Horton 1996, Treasurer 1997, and given in micrometres as average and range (minimum and Whittington et al. 2001). maximum) given within parentheses. In the present investigation monogeneans belonging The type specimens of H. bodiani USNPC 975-15, from to Haliotrema Johnston et Tiegs, 1922 were collected the United States National Parasite Collection (USNPC), were from goldspot hogfish, Bodianus perditio (Quoy et examined and hard parts illustrated for comparison (Fig. 2), Gaimard). This new species is the second species of but we were not able to observe and hence not able to illus- Haliotrema to be described from a Bodianus species and trate the soft anatomical parts.

Address for correspondence: L.H.S. Lim, Institute of Biological Sciences, University of Malaya, Kuala Lumpur, 50603, Malaysia. Phone: ++60 3 7967 4368; Fax: ++60 3 7967 4178/4173; E-mail: [email protected]

203 Type specimens of the present species are deposited in the and vitelline ducts, proceeds anteriorly to form oötype, Muséum National d’Histoire Naturelle, Paris (MNHN), the receiving ducts from surrounding Mehlis’ gland, as- Muzium Zoologi Universiti Malaya, Kuala Lumpur (MZUM) cends medially as uterus to open postero-ventrally to and the Helminthological Collection, Institute of Parasitology, copulatory organ. Dextral vaginal system with promi- Biology Centre, Academy of Sciences of the Czech Republic, nent large muscular elongate flask- or pear-shaped distal České Budějovice (HCIP). end traversing into midportion of body; large pore probably opening into thin-walled small seminal recep- RESULTS tacle, thin sclerotized vaginal duct (observed not at tip Although 16 species of labrids were examined only of flask-shaped vagina) probably leaving seminal recep- Bodianus perditio was found to harbour monogeneans. tacle to oviduct. Vitelline system confluent anterior to The other 15 labrid species included three species of haptor. Bodianus, namely B. axillaris (Bennett), B. busellatus T y p e h o s t : Bodianus perditio (Quoy et Gaimard) (Perci- Gomon, and B. loxozonus (Snyder), as well as Cheilinus formes: Labridae). chlorourus (Bloch), C. trilobatus Lacépède, C. undula- S i t e : Between secondary gill lamellae. tus Rüppell, Choerodon fasciatus (Günther), C. graphi- T y p e l o c a l i t y : Barrier reef off Nouméa, New Caledo- cus (De Vis), Coris aygula Lacépède, Epibulus insidia- nia. tor (Pallas), Oxycheilinus diagrammus (Lacépède), O. T y p e s p e c i m e n s : Holotype, MNHN JNC 1028A1; unifasciatus (Streets), Stethojulis strigiventer (Bennett), MNHN, 18 paratypes (JNC996, JNC1003, JNC1027, Thalassoma lutescens Lay et Bennett) and T. nigrofas- JNC1028, JNC1151, JNC1199); MZUM(P), 3 paratypes ciatum Randall. (nos. 578–580); HCIP, 2 paratypes (M-434). M a t e r i a l s t u d i e d : 22 specimens; 20 specimens Haliotrema banana sp. n. Fig. 1A–H measured. Description. Body elongate, length 635 (463–842) P r e v a l e n c e : 75% (26/35). width 176 (128–211), anterior region with 3 pairs of I n t e n s i t y : Up to about 100 monogeneans per fish. cephalic glands of dactylogyrid-type and 2 pairs of pig- C o m p a r a t i v e m a t e r i a l s t u d i e d : Slide USNPC mented eye-spots. Mouth subterminal ventral; pharynx 975-15, Haliotrema bodiani Yamaguti, 1968; the single oval comparatively small; intestine bifurcates posterior slide contains the holotype, clearly marked, and 15 other to pharynx; caeca rejoin posterior to testis and anterior specimens or fragments (all paratypes). to short peduncle. E t y m o l o g y : The species name is after the local name of Haptor set off from body, almost rectangular; length the fish “perroquet banane”. Name in apposition, inde- 89 (72–120) width 124 (103–149), 14 larval type mar- clinable. ginal hooks, similar size, length 13 (12–14); two pairs Remarks on the host. The goldspot hogfish Bo- of anchors with fenestrated shafts; 2 dorsal anchors with dianus perditio is the second largest labrid in New inner length 60 (55–64); outer length 49 (42–55), long Caledonia (after the giant humphead , Cheilinus inner root 24 (18–30), outer root 10 (6–13); point 17 undulatus). It is locally known as “perroquet banane” (13–20); 2 ventral anchors with well-developed roots, (to be translated as “banana parrot fish”) probably be- inner length 63 (58–68), outer length 49 (46–54), long cause it superficially resembles the parrot fishes (family inner root 30 (26–37), outer root 10 (8–12), point 17 Scaridae) by its large scales and brilliant colours, and (10–21); 2 connecting bars: straight dorsal bar, 43 (38– because it is often yellow as a banana. The fish is com- 47) wide; U-shaped ventral bar, 43 (38–49) wide. mon and often seen at the Nouméa market where it is Testis single, round, larger than ovary, postero-dorsal sold with the parrot fishes. to and overlapping ovary; vas deferens leaves antero- medial region of testis, passes along dorsal to loop sinis- Differential diagnosis. This new species is different tral caecum to ventral side, ascends in intercaecal region from H. bodiani in the shape of the bars (Figs. 1, 2) and to anterior part of copulatory organ, loops downwards, the extent of the flask-shaped vaginal system (see fig. distends forming seminal vesicle, narrows to enter ini- 42 in Yamaguti 1968). In H. banana, the flask-like va- tial part of copulatory tube. Single elongate pyriform gina extends beyond the midbody almost to the left side prostatic reservoir prominent, prostatic gland ducts of the body traversing the initial part of the elongate drain into the anterior part of prostatic reservoir; copulatory tube, while in H. bodiani the flask-like va- prostatic duct leaves reservoir to enter initial part of gina is located some distance posterior to the copulatory copulatory tube. Copulatory organ consists of copula- tube and does not extend to beyond the midbody. How- tory tube, length 110 (99–120) with a long base and ever, it is not certain if this is due to different methods sinuous tapering tube and thin filament (accessory of preparation. The copulatory organ of the present spe- piece) at distal tip of tube. cies resembles that of H. bodiani (88 µm) (Figs. 1, 2), Ovary elongate, in mid-body; oviduct arises from an- except that in the present species the copulatory organ is terior of ovary, receives thin vaginal duct from distal larger (110 µm). The anchors of H. banana and those of part (not tip) of the flask-like saccular vagina (see later) H. bodiani are similar but the dorsal bar of the new

204 Lim, Justine: Haliotrema banana sp. n.

Fig. 1. Haliotrema banana sp. n. A – composite illustration, ventral view (pg – prostatic gland; co – copulatory organ; sv – semi- nal vesicle; dvd – distended vas deferens; pr – prostatic reservoir; vd – vas deferens; vab – vaginal bulb; vad – vaginal duct; oo – oötype; mg – Mehlis’ gland; ov – ovary; t – testis); B – dorsal anchor (ir – inner root; or – outer root); C – dorsal bar (wdb – width of dorsal bar); D – ventral anchor (il – inner root length; ol – outer root length; pt – point); E1, E2 – ventral bar (wvb – width of ventral bar); F – marginal hook; G – copulatory tube; H – vagina.

205 DISCUSSION

This new species of Haliotrema has a large flask-

shaped vagina, a small medial ovary, a large round dor-

sal testis with the vas deferens looping the left intestinal

caecum to the ventral side, a simple copulatory organ, a

large prominent prostatic reservoir, four anchors, two

bars and 14 marginal hooks. Klassen (1994) in his

analysis of Haliotrema species from boxfishes proposed

a bodiani group which included H. bodiani, H. balisti-

cus (MacCallum, 1915), H. priacanthi, H. pacificus

(Mizelle et Kritsky, 1969), H. cornutus (Mizelle et Krit-

sky, 1969), H. ornatum Yamaguti, 1968 and H. teuthis

(MacCallum, 1915). The present new species is differ-

ent from the Haliotrema species within the bodiani

group. A prominent flask-shaped vagina as observed in

the present new Haliotrema is found in other Haliot-

rema species not within the bodiani group (Klassen

1994); for instance H. spirale has a vagina of similar

shape, copulatory organ and anchors but belongs to the

spirale group.

This is the third ancyrocephalid species for the

Labridae and the second ancyrocephalid species to be

described from a Bodianus species. The first species, H.

bodiani was described by Yamaguti (1968) from Bo-

dianus bilunulatus (Lacépède) off Hawaii. According to

the latest revision of Bodianus by Gomon (2006), B.

bilunulatus is restricted to the Indian Ocean and Central Fig. 2. Haliotrema bodiani Yamaguti, 1968, hard parts of Pacific, and the host of H. bodiani should now be desig- holotype. A – dorsal anchor; B – dorsal bar; C – ventral an- nated as Bodianus albotaeniatus (Valenciennes) (previ- chor; D – ventral bar; E – copulatory tube; F – vagina. ously considered a subspecies of B. bilunulatus). Gomon (2006) recognized 43 species and 10 subgen- species is bar-shaped while that of H. bodiani is a broad era in Bodianus; interestingly, B. albotaeniatus and B. V-shaped bar. The ventral bar is also different in the perditio, the two species in which monogeneans have two species (Figs. 1, 2). been found, are both members of the subgenus Diasto- Other Haliotrema species with similar large flask- don Bowdich, 1825. No ancyrocephalid has been re- like vaginae include H. cancescens Yamaguti, 1968, H. corded from the other nine subgenera. However, not all ctenochaeti Yamaguti, 1968, H. curvicirrus Yamaguti, members of Diastodon harbour ancyrocephalid mono- 1968, H. flexicirrus Yamaguti, 1968, H. macracantha geneans, shown by their absence in two other species of Yamaguti, 1968, H. palmatum Yamaguti, 1968, H. ser- the subgenus, B. (D.) busellatus and B. (D.) loxozonus, penticirrus Yamaguti, 1968, H. spirale Yamaguti, 1968, which we have examined in New Caledonia. As already while H. brotulae Yamaguti, 1968 (annulocirrus group), noted the capsalids recorded from Bodianus spp. are H. chelicirrus Yamaguti, 1968, H. rectangulare Yama- Benedenia bodiani from B. (D.) albotaeniatus and Neo- guti, 1968, H. priacanthi Yamaguti, 1968 and H. sig- benedenia melleni from B. rufus, a member of the sub- modocirrus Yamaguti, 1968 have smaller vaginal Bodianus. It should be noted that N. melleni is a ‘flasks’ and longer vaginal ducts (Klassen 1994). Based species with wide host specificity and common under on the combination of vaginal ‘flask’, U-shaped ventral culture situations (Whittington and Horton 1996). No bar and copulatory organ, this new species is similar to capsalid has been found on any of the Bodianus spp. nor H. spirale from Brotula multibarbata Temminck et on any of the labrids examined thus far in New Caledo- Schlegel and H. minutospirale Yamaguti, 1968 from nia. However, the report (Zhang et al. 2001) of Sinodi- Parupeneus cyclostomus Lacépède (junior synonym P. plectanotrema argyrosomus, previously described from chryserydros), P. pleurostigma Bennett and P. multifas- the sciaenid, Pennahia anea, on the labrid Halichoeres ciatus Quoy et Gaimard. However, in H. spirale the nigrescens, should be re-evaluated. filament-like accessory piece is more prominent and The paucity of monogeneans on Labridae, despite be- longer while in H. banana the filamentous accessory ing a species-rich family (see Introduction), is further piece is not obvious. Haliotrema minutospirale is dif- corroborated by the fact that of the 16 labrid species ferent from this new species in the shape of the vagina examined in New Caledonia, only one species, B. perdi- as well as in the copulatory organ. tio was found to harbour monogeneans. However, this

206 Lim, Justine: Haliotrema banana sp. n. paucity of monogeneans is not paralleled by other para- Acknowledgements. Identification of all Bodianus specimens sitic groups. Besides H. banana, the gills of B. perditio mentioned in this paper was kindly confirmed (from photo- are inhabited by four species of copepods, Hatschekia graphs) by Martin Gomon (Museum Victoria, Melbourne, Australia), who also provided comments and literature; identi- sp. (Hatschekiidae), Dissonus sp. (Dissonidae), Lepeo- fication of most other labrids was kindly confirmed (from phtheirus sp. (Caligidae) and Lernanthropus sp. (Ler- photographs) by Ronald Fricke (Staatliches Museum für nanthropidae) and one larval gnathiid isopod (Justine, Naturkunde, Stuttgart, Germany). We thank Eric Hoberg personal observation). Eggs of Huffmanela ossicola (USNPC, Beltsville, USA) for providing type specimens. G.A. Justine, 2004, a trichosomoidid described Boxshall (Natural History Museum, London) kindly identified from Bodianus loxozonus (see Justine 2004), were copepods. Louis Euzet (Sète, France) helped with an early found within the arch gill bones and other bones of B. study of these specimens. Julie Mounier, volunteer technician, and Charles Beaufrère, Audrey Guérin, Anaïs Guillou, Aman- perditio (new host record). The digestive tract harbours dine Marie, Chloé Journo, Violette Justine, Eric Bureau, Maya the lepocreadiid digenean Intusatrium robustum Durio Robert, Damien Hinsinger, Géraldine Colli, Lenaïg Hemery et Manter, 1968 (Durio and Manter 1968, Bray and and Aude Sigura, all students, participated in the fishing op- Justine 2006) and an unidentified cucullanid nematode. erations and parasitological survey. Sam Tereua, Miguel Clar- In total the fish harbours nine parasite species, including que and Napoléon Colombani, captains of the RV ‘Coris’ seven in the gills. provided safe navigation. Angelo di Matteo (IRD) provided It is interesting to note that the Gobiidae, the largest technical help. We would like to thank Mr. K.S. Liew for technical assistance in collecting and processing the speci- marine fish family, is also relatively poor in monoge- mens. This project was made possible by the kind assistance nean fauna and has a single Haliotrema species (Sasal et from the staff of the French Embassy in Kuala Lumpur and al. 1998) reported thus far. funds from the French Embassy, Kuala Lumpur.

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Received 15 November 2006 Accepted 5 March 2007

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