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Systematic Parasitology

, Volume 67, Issue 3, pp 187–209 | Cite as

Species of Calydiscoides Young, 1969 (Monogenea: Diplectanidae) from lethrinid fishes, with the redescription of all of the type-specimens and the description of C. euzeti n. sp. from Lethrinus rubrioperculatus and L. xanthochilus off New Caledonia

  • Jean-Lou Justine
Original Paper

Abstract

Type-specimens of all known species of Calydiscoides Young, 1969 from lethrinids, namely C. australis Young, 1969 (type-species), C. difficilis (Yamaguti, 1953) Young, 1969, C. duplicostatus (Yamaguti, 1953) Young, 1969, C. rohdei Oliver, 1984 and C. gussevi Oliver, 1984, were re-examined; the male copulatory organs (MCO) of the type-specimens are figured for comparison. Two groups are distinguished within Calydiscoides: the ‘difficilis’ group, with a massive MCO (C. difficilis and C. rohdei), and the ‘australis’ group, with a branched MCO (C. australis, C. duplicostatus and C. gussevi). Species of Calydiscoides were found in seven species of Lethrinus (Lethrinidae) off New Caledonia, South Pacific. C. australis and C. gussevi from L. miniatus, their type-host, and C. rohdei from L. atkinsoni, its type-host, are re-described from New Caledonian specimens; all were previously known only from off eastern Australia and are new geographical records for New Caledonia. C. euzeti n. sp. is described from specimens collected from L. rubrioperculatus (type-host) and L. xanthochilus off New Caledonia. Specimens from the two hosts have slightly different measurements of the haptoral hard-parts but a similar morphology of the MCO. The new species belongs to the ‘australis’ group and is characterised by its MCO, which is 70–83 μm in length, elongate in shape with a characteristic anterior curved whip.

Keywords

Carmine Picrate Male Copulatory Organ Intestinal Bifurcation Outer Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Résumé

Les spécimens-types de toutes les espèces connues de Calydiscoides Young, 1969 parasites de Lethrinidae, soit C. australis Young, 1969 (espèce-type), C. difficilis (Yamaguti, 1953) Young, 1969, C. duplicostatus (Yamaguti, 1953) Young, 1969, C. rohdei Oliver, 1984, et C. gussevi Oliver, 1984, ont été examinés, et les organes copulateurs mâles (OCM) des spécimens-types sont figurés pour comparaison. Deux groupes sont distingués dans Calydiscoides, le groupe ‘difficilis’, à OCM massif (C. difficilis et C. rohdei), et le groupe ‘australis’, à OCM formé de branches (C. australis, C. duplicostatus et C. gussevi). Des spécimens de Calydiscoides ont été trouvés chez sept espèces de Lethrinus (Lethrinidae) en Nouvelle-Calédonie, Pacifique Sud. C. australis et C. gussevi chez L. miniatus, leur hôte-type, et C. rohdei chez L. atkinsoni, son hôte-type, sont redécrits à partir de spécimens néo-calédoniens. Ces espèces n’étaient connus que d’Australie Orientale et constituent des nouvelles mentions géographiques pour la Nouvelle-Calédonie. C. euzeti n. sp. est décrit à partir de spécimens récoltés chez L. rubrioperculatus (hôte-type) et L. xanthochilus en Nouvelle-Calédonie. Les spécimens des deux hôtes ont des dimensions des parties sclérifiées du hapteur légèrement différentes, mais une morphologie semblable de l’OCM. La nouvelle espèce appartient au groupe ‘australis’ et est caractérisée par son OCM, long de 70–83 μm, allongé, et portant un fouet antérieur courbé caractéristique.

Introduction

Young (1969) proposed Calydiscoides Young, 1969 for diplectanids with four anchors, one ventral bar, two dorsal bars, 14 marginal hooks and two lamellodiscs with concentric lamellae which telescope into each other. The genus was revised by Oliver (1987) and Thoney (1989). Kritsky, Jiménez-Ruiz & Sey (2000) accepted Calydiscoides but pointed out resemblances between certain species of Protolamellodiscus Oliver, 1969 and species of Calydiscoides. Lim (2003) revised Calydiscoides, retained nine valid species and described four additional new species from nemipterids. Calydiscoides appears to be restricted to the Lethrinidae (Table 1) and Nemipteridae (Table 2) of the Indo-Pacific region. Since several Lethrinus species have a complex synonymy which hampers parasitological comparison, it is necessary to update the list of hosts (Tables 12).
Table 1

Species of Calydiscoides Young, 1969 from lethrinids

Species

Host name in original reference

Updated host name

Locality

Material examined

Reference

C. australis Young, 1969

Lethrinus chrysostomus

Lethrinus miniatus*

Eastern Australia*

+*

Young (1969, 1970)

 

Lethrinus chrysostomus

Lethrinus miniatus

Eastern Australia

+

Oliver (1984)

 

Lethrinus miniatus

Lethrinus miniatus

Eastern Australia

 

Rohde et al. (1994, 1995)

  

Lethrinus miniatus

New Caledonia

+

Present work

C. difficilis (Yamaguti, 1953) Young, 1969

Lethrinus sp.*

Lethrinus sp. A (1)

Sulawesi, Indonesia*

+*

Yamaguti (1953)

 

Lethrinus fletus (2)

Lethrinus laticaudis

Eastern Australia

+

Young (1969, 1970)

 

Lethrinus chrysostomus (3)

Lethrinus miniatus

Eastern Australia

 

Oliver (1984)

 

Lethrinus miniatus

Lethrinus miniatus

Eastern Australia

 

Rohde et al. (1994, 1995)

 

Lethrinus nebulosus

Lethrinus nebulosus

Eastern Australia

+

Oliver (1984)

 

Lethrinus reticulatus (5)

? (4)

Eastern Australia

 

Young (1970)

C. duplicostatus (Yamaguti, 1953) Young, 1969

Lethrinus sp. A*

Lethrinus sp. A (1)

Sulawesi, Indonesia*

+*

Yamaguti (1953)

C. gussevi Oliver, 1984

Lethrinus chrysostomus (3)

Lethrinus miniatus*

Eastern Australia

+*

Oliver (1984), Rohde et al. (1994, 1995)

  

Lethrinus miniatus

New Caledonia

+

Present work

C. rohdei Oliver, 1984

Lethrinus mahsena (5)

Lethrinus atkinsoni*

Eastern Australia*

+*

Oliver (1984)

  

Lethrinus atkinsoni

New Caledonia

+

Present work

C. euzeti n. sp.

Lethrinus rubrioperculatus*

 

New Caledonia

+*

Present work

 

Lethrinus xanthochilus

 

New Caledonia

+*

Present work

* Type-host, type-locality, type-material

(1) C. difficilis and C. duplicostatus are from the same host (see text)

(2) Young (1969) mentioned “freshly collected specimens” but did not indicate the host; Young (1970) indicated L. fletus as the host, and USNPC slides 063155 1004-24-25, from Young, dated 1967, are from ‘L. fletus’

(3) Synonymy according to Carpenter & Allen (1989), Randall, Allen & Steene (1990) and Randall & Wheeler (1991)

(4) According to Carpenter & Niem (2001) L. reticulatus Valenciennes does not occur off Australia

(5) Erroneously spelled mashena in Oliver, 1984. Carpenter & Allen (1989) and Randall et al. (1990) indicated that L. mahsena is restricted to the Western Indian Ocean, and that the species found in the West Pacific should now be named L. atkinsoni Seale

Table 2

Species of Calydiscoides Young, 1969 from nemipterids

Species

Host name in original reference

Updated host name

Locality

Reference

C. flexuosus (Yamaguti, 1953) Young, 1969

Synagris taeniopterus (1)

Nemipterus hexodon*

Sulawesi, Indonesia*

Yamaguti (1953)

(as C. indianus Karyakarte & Das, 1978)

Nemipterus japonicus

Nemipterus japonicus

India, West Coast

Karyakarte & Das (1978)

(as C. indicus Venkatanarsaiah & Kulkarni, 1980)

Nemipterus japonicus

Nemipterus japonicus

India, Bay of Bengal

Venkatanarsaiah & Kulkarni (1980)

(as C. indianus Karyakarte & Das, 1978)

Nemipterus japonicus

Nemipterus japonicus

South China

Zhang, Yang & Liu (2001), Zhang et al. (2003)

 

Nemipterus japonicus

Nemipterus japonicus

India, Bay of Bengal

Kritsky et al. (2000)

 

Nemipterus peronii

Nemipterus peronii

Kuwait

Kritsky et al. (2000)

 

Nemipterus bipunctatus

Nemipterus bipunctatus

Kuwait

Kritsky et al. (2000)

C. convolutus (Yamaguti, 1953) n. comb.

Synagris taeniopterus (1)

Nemipterus hexodon*

Sulawesi, Indonesia*

Yamaguti (1953), Present paper

C. japonicus (Pillai & Pillai, 1976) Thoney, 1989

Nemipterus japonicus

Nemipterus japonicus

India

Pillai & Pillai (1976)

C. nemipteris Thoney, 1989

Scolopsis temporalis*

Scolopsis temporalis

Eastern Australia*

Thoney (1989)

C. cymbidioides Ding & Zhang, 1996

Scolopsis taeniopterus*

Scolopsis taenioptera

South China*

Ding & Zhang (1996)

C. monogrammae Lim, 2003

Scolopsis monogramma*

Scolopsis monogramma

Peninsular Malaysia*

Lim (2003)

C. conus Lim, 2003

Scolopsis margaritifer*

Scolopsis margaritifera

Peninsular Malaysia*

Lim (2003)

C. scolopsidis Lim, 2003

Scolopsis margaritifer*

S. margaritifera

Peninsular Malaysia*

Lim (2003)

 

Scolopsis monogramma

S. monogramma

Peninsular Malaysia

Lim (2003)

C. kemamanensis Lim, 2003

Pentapodus setosus*

Pentapodus setosus

Peninsular Malaysia*

Lim (2003)

* Type-host, type-locality

(1) Host synonymy according to Kritsky et al. (2000), not found in Froese & Pauly (2006)

The Lethrinidae is rich, with 39 species and six genera (Carpenter & Allen, 1989); the most speciose genus is Lethrinus with 26–30 species (Froese & Pauly, 2006; Randall, 2005; Sato, 1978), mostly in tropical waters of the Indo-Pacific. In New Caledonia, the lethrinids are one of the most important groups for fisheries (Laboute & Grandperrin, 2000), and 18 species of lethrinids, including 13 species of Lethrinus, have been recorded (Carpenter, 2001).

Twelve species of lethrinids off New Caledonia were examined for parasites (Table 3). Among the nine species of Lethrinus examined, seven species had both Calydiscoides spp. (sometimes several species per fish species) and ancyrocephalids (Haliotrema spp.). Species of Gymnocranius and Gnathodentex each had a species of Lamellodiscus Johnston & Tiegs, 1922, probably new, but no Calydiscoides species or ancyrocephalids.
Table 3

Lethrinids off New Caledonia and their gill monogeneans

Subfamily and species

Examined

Diplectanids

Ancyrocephalids

Others

Monotaxinae

Gnathodentex aurolineatus (Lacépède)

+

Lamellodiscus sp.

0

 

Gymnocranius euanus Günther

+

Lamellodiscus sp.

0

Microcotylid

Gymnocranius grandoculis (Valenciennes)

+

Lamellodiscus sp.

0

Microcotylid

Gymnocranius sp.

    

Monotaxis grandoculis Forsskål

    

Lethrininae

Lethrinus atkinsoni Seale

+

Calydiscoides rohdei

0

 

Lethrinus genivittatus Valenciennes

+

0

0

 

Lethrinus harak Forsskål

+

Calydiscoides spp. (3 spp.)*

Haliotrema sp.

 

Lethrinus laticaudis Alleyne & Macleay

    

Lethrinus lentjan Lacépède

+

Calydiscoides spp. (2 spp.)*

Haliotrema sp.

 

Lethrinus miniatus Schneider

+

Calydiscoides australis

Haliotrema sp.

 
 

Calydiscoides gussevi

  

Lethrinus nebulosus Forsskål

+

Calydiscoides spp. (3 spp.)*

Haliotrema sp.

Microcotylid

Lethrinus olivaceus Valenciennes

    

Lethrinus ravus Carpenter & Randall

+

Calydiscoides sp.*

Haliotrema sp.

 

Lethrinus rubrioperculatus Sato

+

Calydiscoides euzeti n. sp.

Haliotrema (2 spp.)

 

Lethrinus semicinctus Valenciennes

    

Lethrinus variegatus Valenciennes

    

Lethrinus xanthochilus Klunzinger

+

Calydiscoides euzeti n. sp.

Haliotrema sp.

 

* Tol be described in a separate paper

Species of Calydiscoides are apparently restricted, within the Lethrinidae, to the Lethrininae, which includes only Lethrinus. The Monotaxinae (Gnathodentex and Gymnocranius) have only Lamellodiscus spp. Microcotylids were rare and often immature. Several species have also the capsalids Encotyllabe spp. on their pharyngeal teeth

In this investigation, type-specimens of all of the known species of Calydiscoides from lethrinids, namely C. australis Young, 1969 (type-species), C. difficilis (Yamaguti, 1953) Young, 1969, C. duplicostatus (Yamaguti, 1953) Young, 1969, C. rohdei Oliver, 1984 and C. gussevi Oliver, 1984, were re-examined. It was found that the structure of the male copulatory organ (MCO) is sufficient to allow the identification of species of this genus; thus, for the type-specimens, only the MCO, which is sclerotised and well preserved on the type-slides, is described and figured in this paper. A new species of Calydiscoides from Lethrinus rubrioperculatus and L. xanthochilus is described.

Materials and methods

Specimens of Lethrinus spp. were caught with hand-lines on board the R/V ‘Coris’ or spear-fished (see list of stations). Live fish were kept in a container with seawater and immediately brought back to the laboratory. All fish were measured, weighed and photographed. A unique number (JNC) was assigned to each fish. The parasitological material was then assigned a corresponding JNC linked to the respective fish host. Measurements of hosts (FL, fork length; W, weight) are indicated for possible future comparison of parasite prevalence and host age in other localities.

List of stations: Stations are along the barrier reef off Nouméa, New Caledonia, at a distance of about 20 km from the shore, or within the lagoon, with a depth of 2–40 m. Stn H1, 30 July, 2003, Passe de Dumbéa (PDD), 22°20′S, 166°15′E; Stn H2, 6 August, 2003, Récif Toombo (RT), 22°34′S, 166°28′E; Stn H3, 13 August, 2003, RT; Stn H4, 27 August, 2003, PDD; Stn H5, 2 September, 2003, PDD; Stn H6, 27 November, 2003, Off Île Redika, 22°34′S, 166°32′E; Stn H7, 4 December, 2003, Récif Le Sournois (RLS), 22°31′S, 166°26′E; Stn H8, 28 April, 2004, Récif To, 22°30′S, 166°26′; Stn H9, 22 September, 2004, PDD; Stn H10, 29 March, 2005, Off Ever Prosperity Wreck, 22°27′S, 166°21′E; Stn H11, 17 January, 2006, La Régnière, 22°20′S, 166°17′E; Stn H12, 24 January, 2006, RLS; Stn H13, 15 February, 2006, Grande Rade, 22°15′S, 166°25′E; Stn H14, 21 February, 2006, Balise de l’Ilôt Maître, 22°20′S, 166°25′E; Stn H15, 7 March 2006, Ilôt Signal, 22°17′S, 166°17′E; Stn H16, 21 March, 2006, Île Amédée, 22°27′S, 166°26′E.

Fish used for collection of Calydiscoides spp.: L. rubrioperculatus: JNC767, FL 305, W 440, Stn H1; JNC787, FL 285, W 403, Stn H2; JNC821, FL 314, W 573, Stn H3; JNC851, FL 255, W 300, Stn H4; JNC852, FL 295, W 459, Stn H4; JNC866, FL 250, W 267, Stn H5; JNC988, FL 325, W 574, Stn H6; JNC989, FL 308, W 554, Stn H6; JNC1096, FL 245, W 271, Stn H8; JNC1285, FL 270, W 365, Stn H9; JNC1719, FL 310, W 485, Stn H11; JNC1723, FL 260, W 326, Stn H11; JNC1727, FL 290, W 438, Stn H12; JNC1729, FL 270, W 368, Stn H12; JNC1730, FL 230, W 226, Stn H12; JNC1765, FL 221, W 200, Stn 17; L. xanthochilus: JNC1773, FL 530, W 2300, Stn H16; L. atkinsoni: JNC1515, FL 350, W 913, Stn H10; JNC1742, FL 235, W 248, Stn H13; JNC1748, FL 227, W 228, Stn H14; JNC1759, FL 325, W 729, Stn H15; JNC1776, FL 284, W 468, Stn H16; L. miniatus: JNC993, FL 430, W 1450, Stn H7; JNC1514, FL 500, W 2300, Stn H10.

Gills were extracted and examined in seawater using a dissecting microscope. Live monogeneans were individually picked off the gills with fine needles and immediately prepared. Specimens were routinely processed for carmine staining, including an initial flattening between a slide and a covering slide in ethanol (referred to as ‘carmine’ – see Justine, 2005), according to Justine (2005) or with ammonium picrate-glycerine according to Malmberg (1957), but slightly modified (referred to as ‘picrate’ – see Justine, 2005). In rare cases gills were placed in hot 4% formalin, or 70% ethanol, and monogeneans were later removed from the gills with fine needles and processed for carmine staining without flattening; these are referred to as ‘unflattened carmine’. ‘Picrate’ slides were generally made with several worms per slide; carmine slides, including ‘unflattened’ material, were made with a single worm per slide. A few specimens were also examined live in seawater.

Monogeneans were drawn using an Olympus BH2 microscope equipped with a camera lucida and DIC optics. Measurements were taken on the pencil drawings with the help of a custom-made transparent rule previously calibrated with a stage micrometer. Drawings were scanned and redrawn on a computer with Adobe Illustrator. Measurements of the MCOs were taken as the longest length of the organ (Fig. 1). The haptoral hard-parts were measured as indicated in Fig. 1; after a preliminary test to check absence of lateral asymmetry, measurements of the dextral haptoral hard-parts and sinistral equivalents were pooled. Measurements of monogeneans in ammonium picrate preparations and in specimens prepared in ethanol are significantly different (Justine, 2005); in this paper, only measurements of ‘carmine’ specimens are given for soft parts; measurements of ‘carmine’ and ‘picrate’ specimens are both given for sclerotised parts. ‘Unflattened carmine’ specimens were not used for the description. All measurements are given in micrometres as those for the holotype and mean (or, for redescriptions, the mean) followed by the range and number of measurements in parentheses.
Fig. 1

Methods of measurements and nomenclature used (italics) for sclerotised organs of Calydiscoides spp

Abbreviations: MNHN, Muséum National d’Histoire Naturelle, Paris; BMNH, Natural History Museum, London; USNPC, United States National Parasite Collection, Beltsville; MPM, Meguro Parasitological Museum, Tokyo; Helminthological Collection, Institute of Parasitology, České Budějovice, Czech Republic.

Calydiscoides australis Young, 1969

Type-host: Lethrinus miniatus (Lethrinidae).

Type-locality: Heron Island, Queensland, Australia.

Type-specimens: Holotype, USNM 63153; paratypes, USNM 63154, 4 slides 1004-22–23.

Material examined: Four paratype slides; 1 specimen on slide MNHN 187TC Tj127 (type slide of C. gussevi Oliver, 1984) from L. miniatus, Heron Island, Australia (Oliver, 1984); 2 specimens from Lethrinus miniatus, New Caledonia. Material deposited: MNHN, 2 specimens in carmine.

Brief redescription of type-specimens (Fig. 2C)

Paratypes: body length 520–580; ventral hamuli outer length 43–46, inner length 36–40; dorsal hamuli outer length 36–39, inner length 23–26; dorsal bars short, with bifurcate medial extremity and lateral extremity without hook, length 35–40, width 5–6; ventral bar bow-shaped, length 64–68, width 7; ventral lamellodisc width 30–38, dorsal lamellodisc width 28–38; 10 lamellae, including 3 closed rings and 7 crescents, in all lamellodiscs examined. MCO length: no. 1004-20, 61; no. 1004-21, 58; no.1004-22, 57; no. 1004-23, 57; no. 187TC, 60; original description: 57–58.
Fig. 2

Male copulatory organs of type-specimens of all known species of Calydiscoides, figured at same magnification: (A) C. difficilis (Yamaguti, 1953) Young, 1969, holotype, MPM 22559, slide SY 6730; (B) C. rohdei Oliver, 1984, single type-specimen, MNHN slide 188TC; (C) C. australis Young, 1969, paratype, USNPC 63154 slide 1004-21; (D) C. gussevi Oliver, 1984, single type-specimen, MNHN 187TC; (E) C. duplicostatus (Yamaguti, 1953) Young, 1969, holotype, MPM 22559, slide SY 6730; (F) C. euzeti n. sp., holotype, MNHN JNC989A2

Description of the material from New Caledonia (Fig. 3)

[Measurements from 2 specimens in carmine.] Body length 550–700, width 150–170. Anterior region with 3 pairs of head organs and 2 pairs of eye-spots; distance between outer margins of anterior eye-spot pair 26–32, of posterior eye-spot pair 36–37. Haptor differentiated from rest of body, width 140, provided with 2 similar lamellodiscs, 2 pairs of lateral hamuli, 3 bars and 14 marginal hooklets.
Fig. 3

Calydiscoides australis from Lethrinus miniatus, New Caledonia: (A, B) Male copulatory organ; (C, D) Sclerotised vagina; (E, F) Lamellodiscs in ‘polar’ ventral view; (E) dorsal lamellodisc; (F) ventral lamellodisc

Lamellodiscs made up of concentric tubular lamellae. Details of lamellae from centre to periphery (numbering from centre to periphery): 3 complete circles (rings 1–3), 7 incomplete rings (rings 4–10); ring 3 distinctly thicker than all others in ‘polar’ view; rings 4–10 progressively less and less complete, from ring 4 an almost complete circle to ring 10 a short posterior crescent. Ventral and dorsal lamellodiscs similar. Ventral lamellodisc round in shape, with 10 (n = 3) lamellae, length 30, width 35, internal diameter of first ring 11; dorsal lamellodisc round in shape, with 10 (n = 3) lamellae, length 35, width 34, internal diameter of first ring 10.

Ventral hamulus elongate, with tubular outer root and thin flattened inner root, outer length 46–47, inner length 45–47. Dorsal hamulus elongate, with indistinct inner root, outer length 40–41, inner length 25–27. Dorsal (lateral) bars straight; medial extremity bifurcate; lateral extremity blunt, without hook; length 37–41, width of external part 6–7. Ventral bar bow-shaped, with anteriorly recurved extremities, length 71–73, maximum width 7; groove visible on its ventral side.

Pharynx elongate, length 40–41, width 32–33. Oesophagus apparently absent, such that intestinal bifurcation immediately follows pharynx. Caeca simple, terminate blindly at level of posterior margin of vitelline field.

Testis subspherical, intercaecal, length 75–95, width 100–120. Vas deferens emerges from antero-sinistral part of testis, enlarges into wide seminal vesicle; seminal vesicle in middle region of body, forms bends and connect with MCO.

Sclerotised MCO complex, with 2 parts; posterior part elongate, with bifurcate extremity; anterior part connected with base of posterior part, with pointed extremity and membranous element. Total length of MCO 63, width 47–50.

Ovary subequatorial, intercaecal, pre-testicular, encircles right caecum. Ovary width 93, length 50. Oviduct passes medially to form oötype, surrounded by Mehlis’ gland; oötype short, opens into uterus. Uterus dextral. Sclerotised vagina a roughly spherical sac, diameter 40–50, with convoluted undulations (Fig. 3C, D). Vitelline fields extend posteriorly from posterior to pharyngeal level in 2 lateral bands, confluent in post-testicular region and terminate anterior to peduncle.

Comments

The MCO of the type-specimens (Fig. 2C) corresponds well with the original description by Young (1969). Although Young did not examine Yamaguti’s (1953) original specimens, he mentioned that C. australis was closely related to C. duplicostatus (Yamaguti, 1953) but could be differentiated from it by the shape of the copulatory organ and the length of the oesophagus. The present work confirms that the species are different, although the argument regarding oesophageal length is certainly inappropriate for species of Calydiscoides in which the anterior part, observed in live specimens, is susceptible to extreme elongation.

Apart from the MCO morphology, this species is characterised by short dorsal bars without lateral hooks and a relatively short ventral bar; the sclerotised vagina has convoluted undulations on its edge, a structure not found in any other species of Calydiscoides.

The finding of C. australis in New Caledonia on its type-host, L. miniatus, is a new geographical record. C. australis was found only once in two fish examined, and was rare in comparison with C. gussevi Oliver, 1984.

Calydiscoides difficilis (Yamaguti, 1953) Young, 1969

Syn. Lamellodiscus difficilis Yamaguti, 1953

Type-host: Lethrinus sp. (Lethrinidae).

Type-locality: Off Macassar, Celebes (now Ujungpandang, Sulawesi), Indonesia.

Type-specimens: MPM 22559, 1 slide SY 6730. The slide contains the holotype, clearly labelled, and 2 other specimens of C. difficilis. The slide contains also the type-material of C. duplicostatus (holotype and 2 other specimens) and two specimens of an undescribed species of Haliotrema Johnson & Tiegs, 1922 (Ancyrocephalidae).

Material examined: Holotype and other specimens on the type-slide; USNPC 63155, 2 slides 1004-25 and 1004-26, from ‘L. fletus’ (junior synonym of L. laticaudis), Tangalooma, Australia, deposited by Young and probably corresponding to the material mentioned in Young (1969, 1970), each slide with a single specimen; MNHN 186TC Tj126 (from L. nebulosus, Heron Island, Australia, described by Oliver, 1984); USNPC 80220, 1 slide (Dyer, Williams & Williams, 1989), from L. harak, off Okinawa, Japan, with a single specimen; specimens from several species of lethrinids off New Caledonia.

Brief redescription of type-specimens (Fig. 2A) and comment

Holotype: body length 800; ventral hamuli outer length 58, inner length 58; dorsal hamuli outer length 52–55, inner length 39; dorsal bars elongate, with external hook and bifurcate medial extremity, curvature at c.1/3 from external extremity, length 75, width 7; ventral bar bow-shaped, length 115, width 10; ventral lamellodisc 60 in width, with 10 lamellae, including 3 closed rings and 7 crescents. MCO length: holotype 87; other specimens on slide SY 6730 83, 86; no measurement in original description, and figure 24 of Yamaguti (1953) has no scale. MCO of holotype (Fig. 2A) consists of 2 parts, both heavily sclerotised, and corresponds well with original description (Yamaguti, 1953).

In addition to its massive MCO, C. difficilis is characterised by very long dorsal bars, each with an external (lateral) hook and medial bifurcated extremity, and a very long bow-shaped ventral bar.

In Yamaguti (1953), the type-hosts of both C. difficilis and C. duplicostatus are Lethrinus sp., but it is not indicated whether it is the same species or two different undetermined Lethrinus species. The fact that the type-specimens of both species are on the same slide shows that it is the same host for both species.

The MCO of Young’s material (USNPC 63155, slide 1004-25) is massive and larger (length 105) than the type-material.

Oliver (1984) recorded C. difficilis from both L. miniatus and L. nebulosus from the Wistari Reef, Great Barrier Reef, Australia, but deposited a single slide, MNHN 186TC, which is from L. nebulosus. He mentioned shape variations of the MCO.

Slide USNPC 80220 contains a single monogenean from L. harak, off Okinawa, Japan, identified as Protolamellodiscus convolutus (Yamaguti, 1953) by Dyer et al. (1989). The specimen is C. difficilis.

The species name was chosen by Yamaguti to refer to the complicated structure of the MCO; the present author confirms that the structure is complex and very massive. Specimens of C. difficilis from lethrinids off New Caledonia will be described in detail in a separate paper.

Calydiscoides duplicostatus (Yamaguti, 1953) Young, 1969

Syn. Lamellodiscus duplicostatus Yamaguti, 1953

Type-host: Lethrinus sp. (Lethrinidae).

Type-locality: Off Macassar, Celebes (now Ujungpandang, Sulawesi), Indonesia.

Type-specimens: MPM 22559, 1 slide SY 6730. The slide contains the holotype, clearly labelled, and 2 other specimens of C. duplicostatus (see also above).

Material examined: Holotype and other specimens on type-slide; specimens from several species of lethrinids off New Caledonia.

Brief redescription (Figs.2E, 4) and comments

Holotype: body length 520, width 50; haptor width 80; ventral hamuli outer length 47, inner length 47; dorsal hamuli outer length 37, inner length 26; dorsal bar massive, no hook at external extremity, medial extremity bifurcate, length 29–31, width 8; lamellodiscs (Fig. 4) 25 in width, with 10 lamellae, including 3 closed rings and 7 crescents. Sclerotised vagina: a spherical sac, lightly sclerotised, without special differentiation. MCO length: holotype 46, other specimens in SY 6730, 40, 44 (no measurement given in original description); consists of 2 parts and is very complex, with different branched processes on superposed planes; posterior part deeply stained (Fig. 2E).
Fig. 4

Calydiscoides duplicostatus, holotype: lamellodiscs in ‘lateral’ view

The MCO was described by Yamaguti (1953) as “copulatory organ consisting of a slender curved cirrus, a transverse basal piece and a loop-like accessory piece, whose anterior end is produced anteriorly as well as ventrally into a claw-like process”.

This species is easily distinguished by its MCO morphology; the small lamellodiscs are additional characters for its diagnosis.

See above for the new information that C. duplicostatus and C. difficilis share the same undetermined type-host. Specimens of C. duplicostatus from several lethrinids off New Caledonia will be described in detail in a separate paper.

Calydiscoides rohdei Oliver, 1984

Type-host: Lethrinus atkinsoni (Lethrinidae).

Type-locality: Off Heron Island, Queensland, Australia.

Type-specimens: Slide MNHN 188TC Tj128. The slide contains a single specimen.

Material examined: The type-specimen; c.50 specimens from L. atkinsoni, off New Caledonia. Material deposited: Vouchers, MNHN JNC1776; BMNH 2006.12.13.6; USNPC 99430; MPM 18843; HCIP M-426.

Brief redescription of the type-specimen (Fig. 2B) and comments

Type-specimen: Body length 700, width 130; haptor width 90; ventral hamuli outer length 60, inner length 58; dorsal hamuli outer length 53, inner length 37; dorsal bar length 42–45, width 7; ventral bar indistinct; MCO length 98, original description 100–110.

The MCO of the type-specimens corresponds well to the original description by Oliver (1984). Although the original description mentions syntypes (plural) deposited in the MNHN collection, the type slide contains a single specimen; the similarity in the shape of the MCO suggests that this is the specimen described in figure 10 of Oliver (1984).

Description of the material from New Caledonia (Figs. 5, 6)

[Measurements of 11 specimens; method is carmine if not indicated.] Body length 644, 450–880 (n = 7), width 150, 90–190 (n = 7). Anterior region with 3 pairs of head organs and 2 pairs of eye-spots; distance between outer margins of anterior eye-spot pair 33 (18–50, n = 7), of posterior eye-spot pair 35 (22–53, n = 7). Haptor differentiated from rest of body, width 109 (80–130, n = 7), provided with 2 similar lamellodiscs, 2 pairs of lateral hamuli, 3 bars and 14 marginal hooklets.
Fig. 5

Calydiscoides rohdei from Lethrinus atkinsoni, New Caledonia, male organs: (A, D, E) Male copulatory organ, specimens in carmine; (B, C) Male copulatory organ, specimens in picrate. (A, D) dorsal view; (B, C, E) ventral view. (F) Organization of male soft parts, ventral view; dotted line, position of ovary

Fig. 6

Calydiscoides rohdei from Lethrinus atkinsoni, New Caledonia, lamellodiscs and haptoral parts: (A, C) Lamellodiscs of the same individual. (A) Dorsal lamellodisc; (C) Ventral lamellodisc; (B) Dorsal lamellodisc in ‘lateral’ view; (D) Dorsal hamulus; (E) Ventral hamulus; (F) Dorsal bar; (G) Ventral bar. AC, carmine; DG, picrate

Lamellodiscs made up of concentric tubular lamellae. Details of lamellae from centre to periphery (numbering from centre to periphery): 3 complete circles (rings 1–3), 7 incomplete rings (rings 4–10); ring 3 distinctly thicker than all others in ‘polar’ view (Fig. 6A, C) and ‘lateral’ view (Fig. 6B); rings 4–10 progressively less and less complete, from ring 4 an almost complete circle to ring 10 a short posterior crescent. Ventral and dorsal lamellodiscs similar. Ventral lamellodisc round in shape, with 10 (n = 7) lamellae, length 42 (37–46, n = 6), width 40 (38–42, n = 6), internal diameter of first ring 13 (12–14, n = 6); dorsal lamellodisc round in shape, with 10 (n = 4) lamellae, length 42 (40–44, n = 4), width 39 (35–41, n = 4), internal diameter of first ring 13 (13–15, n = 5).

Ventral hamulus elongate, with tubular outer root and thin flattened inner root, outer length in carmine 50 (47–52, n = 4), in picrate 57 (55–60, n = 12), inner length in carmine 54 (52–57, n = 4), in picrate 58 (56–60, n = 12). Dorsal hamulus elongate, with indistinct inner root, outer length in carmine 44 (43–46, n = 5), in picrate 47 (45–50, n = 12), inner length in carmine 29 (27–31, n = 5), in picrate 33 (31–35, n = 12). Dorsal (lateral) bars curved; medial extremity bifurcate; lateral extremity with hook; length in carmine 37 (35–40, n = 12), in picrate 46 (37–57, n = 11), width of external part, in carmine 5 (5–6, n = 12), in picrate 8 (6–10, n = 11). Ventral bar bow-shaped, with anteriorly recurved extremities, length in carmine 67 (60–71, n = 7), in picrate 75 (68–83, n = 7), maximum width in carmine 7 (6–8, n = 7), in picrate 10 (7–12, n = 7); groove visible on its ventral side.

Pharynx elongate, length 49 (47–52, n = 5), width 34 (25–39, n = 5). Oesophagus apparently absent, such that intestinal bifurcation immediately follows pharynx. Caeca simple, terminate blindly at level of posterior margin of vitelline field.

Testis subspherical, intercaecal, length 96 (75–115, n = 5), width 90 (50–120, n = 5). Vas deferens emerges from antero-sinistral part of testis, enlarges into wide seminal vesicle; seminal vesicle in middle region of body, forms bends and connect with MCO (Fig. 5F). Sclerotised MCO complex, with 2 parts; posterior part comprised of heavily sclerotised basal (posterior) region, apparently hollow, with anterior extremity pointed, and distal membranous element; anterior part heavily sclerotised, with anterior extremity bifurcate and pointed; anterior part connects to posterior part at c.1/3 length of latter. Orientation of MCO: posterior part sinistral, anterior part dextral. Extremities of both seminal vesicle and prostatic reservoir cross ventrally anterior part of MCO and connect with anterior extremity of posterior part of MCO (Fig. 5A,B,E). Morphology of MCO is often badly distorted in highly flattened picrate specimens. Total length of MCO in carmine 75 (63–82, n = 7), in picrate 87 (78–93, n = 7); length of posterior part in carmine 62 (52–67, n = 7), in picrate 69 (55–76, n = 4); length of anterior part in carmine 56 (42–60, n = 7), in picrate 64 (55–70, n = 4).

Ovary subequatorial, intercaecal, pre-testicular, encircles right caecum, width 58 (39–70, n = 5), length 40 (33–50, n = 5). Oviduct passes medially to form oötype; oötype surrounded by Mehlis’ gland. short, opens into uterus. Uterus dextral. No sclerotised vagina seen. Vitelline fields extend posteriorly from posterior to pharyngeal level in 2 lateral bands, confluent in post-testicular region and terminate anterior to peduncle.

Comments

Oliver (1984) incompletely described the soft parts and internal anatomy of this species. The anatomy of specimens from New Caledonia is similar to other species from lethrinids with a large vitelline vesicle in the middle of the body. The specimens from New Caledonia correspond well in morphology and measurements with the type-specimen, although the MCO seems smaller in the New Caledonian material. Because only a single type-specimen of this species was available, voucher specimens have been deposited in Museums.

C. rohdei is close to C. difficilis in the massive size of its MCO; it is differentiated from it by the structure of the MCO, and shorter ventral and lateral bars.

The finding of C. rohdei in New Caledonia on its type-host, L. atkinsoni, is a new geographical record.

Calydiscoides gussevi Oliver, 1984

Type-host: Lethrinus miniatus (Lethrinidae).

Type-locality: Heron Island, Queensland, Australia.

Type-specimens: Slide MNHN 187TC Tj127. The slide contains a single specimen of C. gussevi, a broken specimen of C. australis and 6 specimens of an undetermined Haliotrema (Ancyrocephalidae).

Material examined: The type-specimen; c.20 specimens from L. miniatus, off New Caledonia. Material deposited: Vouchers, MNHN JNC1924; BMNH 2006.12.13.8; USNPC 99428; MPM 18842; HCIP M-425.

Brief redescription of the holotype (Fig. 2D) and comment

Type-specimen: Body length 510, width 90; haptor width 100; ventral hamuli outer length 36, inner length 35; dorsal hamuli outer length 32; dorsal bar length 39–41; ventral bar bow-shaped, length 68, width 7; ventral lamellodisc, width 35, with apparently 8–9 lamellae; dorsal lamellodisc, width 35, apparently 8 lamellae; MCO length 38; original description 29–43.

The MCO of the type-specimen corresponds well with the original description by Oliver (1984); however, neither of the MCOs figured in Oliver’s figure 8 is exactly similar to the single specimen deposited and probably correspond to other specimens.

Description of the material from New Caledonia (Fig. 7)

[Measurements on 10 specimens; method is carmine if not indicated.] Body length 606, (530–650, n = 5), width 170 (140–200, n = 5). Anterior region with 3 pairs of head-organs and 2 pairs of eye-spots; distance between outer margins of anterior eye-spot pair 29 (24–33, n = 4), of posterior eye-spot pair 37 (33–44, n = 4). Haptor differentiated from rest of body, width 117 (100–130, n = 5), provided with 2 similar lamellodiscs, 2 pairs of lateral hamuli, 3 bars and 14 marginal hooklets.
Fig. 7

Calydiscoides gussevi from Lethrinus miniatus, New Caledonia: (AD) Male copulatory organ; (E) Connection of seminal vesicle and prostatic vesicle to MCO; (F) Ventral lamellodisc, ‘polar’ ventral view; (G) Dorsal bar; (H) Ventral bar; (I) Dorsal hamulus; (J) Ventral hamulus; (K) Egg in utero, picrate. A, C, ventral view; D, dorsal view. All carmine except K, picrate

Fig. 8

Calydiscoides euzeti n. sp. from its type-host Lethrinus rubrioperculatus: (A) Composite view of body; (B) Male copulatory organ, holotype; cirrus at anterior extremity; (C) Male copulatory organ and insertion of seminal vesicle and prostatic reservoir, paratype; (D) Sclerotised vagina, holotype; (E) Lamellodisc, made up of three closed rings and seven crescents; (F) Ventral hamulus; (G) Dorsal hamulus; (H) Dorsal bar; (I) Ventral bar

Lamellodiscs made up of concentric tubular lamellae. Details of lamellae from centre to periphery (numbering from centre to periphery): 3 complete circles (rings 1–3), 5–7 incomplete rings (rings 4–8 to 4–10 according to specimens); rings 1–3 thicker than incomplete rings; rings after ring 4 progressively less and less complete, from ring 4 an almost complete circle to last ring (8–10) a short posterior crescent. Ventral and dorsal lamellodiscs similar. Ventral lamellodisc round, with 9–10 (n = 6) lamellae, length 31 (28–33, n = 6), width 28 (27–29, n = 6), internal diameter of first ring 7 (7–8, n = 6); dorsal lamellodisc round in shape, with 8 (n = 5) lamellae, length 30 (29–32, n = 5), width 27 (26–28, n = 5), internal diameter of first ring 7 (6–8, n = 5).

Ventral hamulus elongate, with tubular outer root and thin flattened inner root, outer length in carmine 38 (37–40, n = 12), in picrate 41 (40–43, n = 8), inner length in carmine 32 (30–34, n = 6), in picrate 34 (32–36, n = 8). Dorsal hamulus elongate, with indistinct inner root, outer length in carmine 31 (29–33, n = 12), in picrate 33 (31–35, n = 8), inner length in carmine 21 (18–24, n = 5), in picrate 20 (19–23, n = 8). Dorsal (lateral) bars straight; medial extremity bifurcate; lateral extremity blunt, without hook; length in carmine 38 (36–43, n = 12), in picrate 41 (39–43, n = 8), width of external part in carmine 6 (5–7, n = 12), in picrate 7 (5–9, n =  8). Ventral bar bow-shaped, with anteriorly recurved extremities, length in carmine 72 (69–73, n = 6), in picrate 76 (73–80), maximum width in carmine 6 (5–7, n = 6), in picrate 7 (6–8, n = 4); groove visible on its ventral side.

Pharynx elongate, length 37 (34–42, n = 4), width 30 (28–31, n = 4). Oesophagus apparently absent, such that intestinal bifurcation immediately follows pharynx. Caeca simple, terminate blindly at level of posterior margin of vitelline field.

Testis subspherical, intercaecal, length 93 (85–100), width 89 (80–100, n = 5). Vas deferens emerges from antero-sinistral part of testis, enlarges into wide seminal vesicle; seminal vesicle in middle region of body, forms bends and connect with MCO. Prostatic glands connect with MCO.

Sclerotised MCO complex, with 2 branches originating from common trunk; 1 branch simple, pointed, hollow; 1 branch complex, with enlarged extremity and bifurcations which vary with orientation and specimens. [Sometimes the branches are apparently superposed; this is probably the case in the specimen in Fig. 7A, which is more similar to the holotype (Fig. 2D) than the other specimens.] Orientation of MCO: trunk dextral, extremities of branches sinistral. Extremity of prostatic reservoir connects with MCO. Total length of MCO 40 (37–44, n = 6); width measured at mid-length 24 (19–25, n = 6).

Ovary subequatorial, intercaecal, pre-testicular, encircles right caecum. Uterus dextral. No sclerotised vagina seen. Vitelline fields extend posteriorly from posterior to pharyngeal level in 2 lateral bands, confluent in post-testicular region and terminate anterior to peduncle.

Egg in utero elongate with short filament, in picrate 99 (88–105) × 49 (45–53) (n = 10). [In contrast to other species in which egg is rarely seen, almost all specimens on single fish (JNC1514) collected in March, 2005 each carried one egg in the uterus.]

Comments

Oliver (1984) incompletely described the soft parts and internal anatomy of this species. The anatomy of specimens from off New Caledonia is similar to other species of Calydiscoides from lethrinids, with a large vitelline vesicle in the middle of the body. The specimens from New Caledonia correspond well in morphology and measurements to the type-specimen; the MCO of the holotype probably has its two branches superposed, but one specimen from New Caledonia is similar. In contrast to other species, the MCO is not oriented with the common part posterior and the branches anterior, but has rather an ‘oblique’ position with the branches sinistral. Because only a single type-specimen of this species was available, voucher specimens have been deposited in Museums.

The record of C. gussevi off New Caledonia on its type-host, L. miniatus, is a new geographical record. C. gussevi was more abundant than C. australis in the two fish examined.

Calydiscoides euzeti n. sp.

Type-host: Lethrinus rubrioperculatus Sato (Lethrinidae).

Other host: Lethrinus xanthochilus Klunzinger.

Type-locality: Lagoon off Nouméa, New Caledonia.

Site: Between secondary gill lamellae.

Type-specimens: Holotype, slide JNC989A2; 75 paratypes.

Material examined: c.100 specimens.

Material deposited: Holotype and 47 paratypes from L. rubrioperculatus (24 ‘carmine’, 2 ‘unflattened carmine’, 21 ‘picrate’), MNHN; 24 paratypes from L. xanthochilus (9 ‘carmine’, 15 ‘picrate’ in 5 slides, MNHN; paratypes from L. rubrioperculatus, ‘carmine’, BMNH 2006.12.13.9; USNPC 99428; MPM 18841; HCIP M-424.

Prevalence:L. rubrioperculatus 70%; L. xanthochilus 1/1.

Intensity: Up to 30/fish.

Remarks on the hosts: Lethrinus rubrioperculatus is an abundant fish forming small shoals off New Caledonia. Within the lagoon, the species is associated with habitats adjacent to coral, such as seagrass beds. L. xanthochilus is a large species; specimens are solitary (Randall, 2005) and are found in the same area as L. rubrioperculatus.

Etymology: The species is named for Professor Louis Euzet as a testimony to his outstanding career as a parasitologist. Prof. Euzet provided key advice in the early steps of work on this species.

Description (Figs. 89)

Preliminary comparison of specimens from the two hosts Specimens from the two hosts were found to be similar in morphology, but morphometric differences were detected; before determining conspecificity, a comparison of key measurements was undertaken (Table 4). Because measurements of hard parts are affected by the method of preparation (see Justine, 2005), those of specimens in carmine and picrate were considered independently.
Table 4

Comparison of specimens of Calydiscoides euzeti n. sp. from its two hosts

Measurements

Lethrinus rubrioperculatus

L. xanthochilus

Difference μm (%)

Different?

Carmine

Penis total length

73 ± 6.1 (54–83, n = 29)

76 ± 4.2(70–81, n = 9)

3 (4%)

No

Ventral hamulus outer length

50 ± 2.4 (44–55, n = 48)

49 ± 2 (45–52, n = 11)

1 (2%)

No

Dorsal hamulus outer length

42 ± 1.8 (38–46, n = 49)

41 ± 1.5 (39–43, n = 10)

1 (2%)

Yes

Ventral bar length

56 ± 4.3 (48–62, n = 27)

50 ± 3.5 (46–54, n = 6)

6 (10%)

Yes

Dorsal bar length

33 ± 2.3 (27–38, n = 49)

31 ± 0.9 (29–32, n = 14)

2 (6%)

Yes

Picrate

Penis total length

79 ± 4.2 (70–88, n = 23)

84 ± 4.6 (75–89, n = 14)

5 (6%)

Yes

Ventral hamulus outer length

54 ± 1.8 (49–57, n = 42)

53 ± 1.9 (48–57, n = 28)

1 (2%)

Yes

Dorsal hamulus outer length

44 ± 1.4 (41–47, n = 41)

43 ± 1.3 (41–46, n = 28)

1 (2%)

No

Ventral bar length

62 ± 6 (50–70, n = 21)

51 ± 3 (47–57, n = 14)

11 (18%)

Yes

Dorsal bar length

38 ± 3.1 (32–44, n = 41)

32 ± 1.6 (29–35, n = 27)

6 (16%)

Yes

All measurements indicated as the mean ± standard deviation (minimum–maximum, n)

Measurements of left and right elements are pooled for ventral and dorsal hooks and dorsal bars

Result of the statistical test (U test of Mann–Whitney) given in last column

Fig. 9

Calydiscoides euzeti n. sp. Haptors and lamellodiscs. (A) Haptoral parts, carmine in Canada balsam, ventral view (bifurcated extremity of dorsal bars inconspicuous, orientation of hamuli suboptimal); (B, C) Haptoral parts, picrate, ventral view (hamuli well flattened, bifurcated extremity of dorsal bars well visible); (D) Dorsal lamellodisc; (E) Dorsal lamellodisc; (F) ‘Disturbed’ lamellodisc showing rings 1 and 2 separated from others. A, B, D, F, paratypes from Lethrinus rubrioperculatus; C, D, paratypes from Lethrinus xanthochilus. Note shorter bars in C (from L. xanthochilus) than in B (from L. rubrioperculatus)

Statistical tests (Table 4) indicated that the measurements were different for ventral and dorsal hooks length, but the differences were small (c.1 μm) and could not be used for differentiating species. Differences for penis total length were not significant in carmine but were significant in picrate; however, the difference was minimal (5 μm, 5% of the measurement). Differences for ventral bar length and dorsal bar length were significant using both methods; however, differences were only 2–9 μm, thus only 6–16% of the measurements. It was thus considered that the same species occurred in both hosts, and differences in measurements were attributed to intraspecific or host-dependent variation.

Specimens from Lethrinus rubrioperculatus Body elongate, lanceolate, length 600, 735 (600–1,000, n = 25), width 130, 154 (80–190, n = 16). Tegument smooth. Anterior region with 3 pairs of head organs and 2 pairs of eye-spots; distance between outer margins of anterior eye-spot pair 62, 40 (30–62, n = 24), of posterior eye-spot pair 52, 38 (25–53, n = 23). Haptor differentiated from rest of body, width 100, 100 (80–125, n = 14), provided with 2 similar lamellodiscs, 2 pairs of lateral hamuli, 3 bars and 14 marginal hooklets. Hooklet length 9–10.

Lamellodiscs made up of concentric tubular lamellae. Details of lamellae from centre to periphery (numbering from centre to periphery): 3 complete circles (rings 1–3), 7 incomplete rings (rings 4–10); rings 1–4 thicker than 5–10, with ring 3 distinctly thicker than all others; rings 4–10 progressively less and less complete, from ring 4 an almost complete circle to ring 10 a short posterior crescent. Ventral and dorsal lamellodiscs similar but ventral slightly larger than dorsal. Ventral lamellodisc round in shape, with 10 (n = 22) lamellae, length 39, 38 (30–45, n = 21), width 38, 36 (32–41, n = 21), internal diameter of first ring 12, 12 (10–13, n = 22); dorsal lamellodisc round in shape, with 10 (n = 23) lamellae, length 38, 36 (30–44, n = 20), width 36, 33 (29–39, n = 20), internal diameter of first ring 11, 11 (9–14, n = 23). Number of lamellae perfectly stable, 10 in all (n = 55) lamellodiscs examined.

Ventral hamulus elongate, with tubular outer root and thin flattened inner root, outer length in carmine 51, 50 ± 2.4 (44–55, n = 48), in picrate 54 ± 1.8 (49–57, n = 42), inner length in carmine 51, 51 ± 2.1 (45–55, n = 47), in picrate 51 ± 2.0 (44–55, n = 42). Dorsal hamulus elongate, with indistinct inner root, outer length in carmine 44, 42 ± 1.8 (38–46, n = 49), in picrate 44 ± 1.4 (41–57, n = 41), inner length in carmine 30, 29 ± 1.3 (26–32, n = 48), in picrate 30 ± 1.3 (28–33, n = 41). Dorsal (lateral) bars curved posteriorly; curvature c.120°, at mid-length; medial extremity bifurcate; medial ventral and dorsal branches overlapping in moderately flattened (‘carmine’) specimens, not overlapping and very distinct in highly flattened (‘picrate’) specimens (Fig. 4); lateral extremity recurved posteriorly in form of pointed hook. Length of dorsal bars in carmine 34, 33 ± 2.3 (27–38, n = 49), in picrate 38 ± 3.1 (32–44, n = 41), width of external part, in carmine 5, 5 ± 0.5 (4–7, n = 48), in picrate 7 ± 1.0 (5–10, n = 40). Although bifurcate medial extremity often overlaps ventral bar, both branches are dorsal to it, i.e. ventral bar is never surrounded by medial branches of dorsal bars. Ventral bar thick, bow-shaped, with anteriorly recurved extremities, length in carmine 60, 56 (48–62, n = 27), in picrate 62 (50–70, n = 42), maximum width in carmine 7, 6 (5–7, n = 27), in picrate 7 (6–10, n =  20); groove visible on its ventral side, with crescent-shaped incision in middle.

Pharynx elongate, length 60, 50 (35–60, n = 23), width 35, 36 (22–50, n = 23). Oesophagus apparently absent, such that intestinal bifurcation immediately follows pharynx. Caeca simple, terminate blindly at level of posterior margin of vitelline field.

Testis subspherical, intercaecal, length 60, 44 (28–60, n = 19), width 50, 44 (30–58, n = 19). Vas deferens conspicuous, emerges from antero-sinistral part of testis, enlarges into wide seminal vesicle; seminal vesicle in middle region of body, forms bend, then curves posteriorly to connect with male copulatory organ (MCO). Prostatic glands conspicuous, connected with conspicuous reservoir; reservoir follows path of terminal part of seminal vesicle and also curves posteriorly to connect with MCO. Sclerotised MCO complex; 2 sclerotised parts connected at their posterior extremity; posterior part made up of heavily sclerotised basal (posterior) region and thin anterior lamellar part; anterior part made up of heavily sclerotised basal (posterior) region, intermediate region apparently thinly sclerotised with posteriorly directed hook, and anterior elongate whip; whip curved, progressively thinner towards anterior extremity, apparently hollow at least in its basal part. Cirrus (a thinly folded sclerotised membrane) often visible at anterior extremity of whip, curves posteriorly, its posterior extremity becoming thinner and inconspicuous. Orientation of MCO: anterior part always dextral, with whip curving dextrally. Extremities of both seminal vesicle and prostatic reservoir ventrally cross anterior part of MCO and connect with basal region of posterior part of MCO. Total length of MCO in carmine 78, 73 (54–83, n = 29), in picrate 79 (70–88, n = 23); length of posterior part in carmine 45, 51 (37–63, n = 28), in picrate 54 (45–60, n = 23); length of anterior part in carmine 64, 59 (42–68, n = 29), in picrate 66 (54–76, n = 23); these lengths all taken from extremity to extremity, thus not taking in account variations according to whip curvature (Fig. 1).

Ovary subequatorial, intercaecal, pre-testicular, encircles right caecum. Ovary width 80, 59 (35–80, n = 19), length 50, 37 (25–65, n = 19). Oviduct passes medially to form oötype, surrounded by Mehlis’ gland; oötype short, opens into uterus. Uterus dextral. Sclerotised vagina a thinly sclerotised sac of variable shape, with roughly cylindrical sclerotised structure (Fig. 3D); length of sclerotised part 12, 12 (9–16, n = 24). Conspicuous short canal from sclerotised vagina to seminal receptacle; seminal receptacle well developed, sinistral, connected to oötype. Vitelline fields extend posteriorly from posterior to pharyngeal level in 2 lateral bands, confluent in post-testicular region and terminate anterior to peduncle. Bilateral connections from vitelline fields to oötype inconspicuous. Egg in utero rarely seen, elongate, in carmine 90 × 28, in picrate 95 × 52, with filament.

Specimens from Lethrinus xanthochilus

Morphology similar to specimens from L. rubrioperculatus, particularly for the complex MCO. Lamellodiscs identical, with number of lamellae 10 in all (n = 10) lamellodiscs examined. Proportion of the haptoral hard parts slightly different, with shorter ventral and dorsal bars, but similar ventral and dorsal hamuli. Measurements in addition to Table 2: body length 1,046 (820–1,200, n = 7); distance between outer margins of anterior eye-spot pair 34 (28–41, n = 4), of posterior eye-spot pair 40 (26–53, n = 4); pharynx length 57 (43–72, n = 5), width 34 (30–38, n = 5); ventral lamellodisc length 34 (32–39, n = 5), width 35 (35–36, n = 5); dorsal lamellodisc length 33 (30–37, n = 5), width 33 (31–34, n = 5); testis length 72 (55–95, n = 6), width 58 (40–78, n = 6); ovary length 45 (35–50, n = 6), width 74 (50–90, n = 6); egg in utero, in carmine 80 × 25–35 (n =  2), in picrate 95 × 31.

Differential diagnosis

Examination of the type-specimens of all five known species of Calydiscoides from lethrinids (Fig. 2) and specimens from New Caledonia shows that species of Calydiscoides from lethrinids can be classified into two groups (Table 5): (a) the ‘difficilis group’, with a massive and heavily sclerotised MCO, and (b) the ‘australis group’, with a smaller, less sclerotised MCO bearing branched protuberances. The difficilis group includes C. difficilis and C. rohdei; the australis group includes C. australis, C. gussevi and C. duplicostatus. In addition to the MCO structure, the difficilis group is characterised by long ventral and dorsal hamuli, elongate curved dorsal bars with lateral hooks, long ventral bars and large lamellodiscs; the australis group is characterised by smaller dorsal and ventral hamuli, shorter ventral bars and smaller lamellodiscs, and the dorsal bars exhibit variations within this group.
Table 5

Selected morphological characteristics of Calydiscoides spp. from lethrinids

 

‘Difficilis group’

‘Australis group’

C. difficilis

C. rohdei

C. australis

C. duplicostatus

C. gussevi

C. euzeti n. sp.

MCO shape

massive

massive

branched

branched

branched

branched

MCO length

87

98

58

43

38

73

Ventral hamulus length

58

60

45

47

36

50

Dorsal hamulus length

53

53

38

37

32

42

Dorsal bar length

75

43

37

30

40

33

Dorsal bar shape

curved, hooked

curved, hooked

massive, no hook

massive, no hook

massive, no hook

curved, hooked

Ventral bar length

115

c. 75

66

c. 45

68

56

Lamellodisc width

60

47

33

25

35

36

Measurements are rounded means only from the holotype or type-series

C. euzeti n. sp., by the structure of its MCO, clearly belongs to the australis group. It is easily differentiated from all three other members of this group by the structure of its MCO, which has a very distinctive anterior whip (whip-like structures apparently exist in C. australis and C. duplicostatus but they are shorter). In addition, C. euzeti is the only member of the australis group which has elongate, curved dorsal bars with lateral hooks.

Remarks on Calydiscoides

The structure of the telescopic lamellodiscs of Calydiscoides is difficult to interpret on microscope preparations; when the lamellae are regularly arranged and seen from their concentric axis (ventral or dorsal observation of the specimen, ‘polar’ view of the lamellodisc), the lamellodisc is apparent as concentric circles and semicircles; when the lamellodisc is disturbed (‘lateral’ view of lamellodisc), the first lamellae generally exhibit a telescopic structure but the others collapse and the structure is unclear. The same is true for the Pseudorhabdosynochus Yamaguti, 1958 species of the cupatus group, which have central lamellar rings and peripheral rows of rodlets (Hinsinger & Justine, 2006; Justine, 2005). Lim (2003) showed different aspects of the lamellodisc of Calydiscoides spp., and Thoney (1989) provided some scanning electron microscope observations. Lim (2003) discussed the structure of the outermost lamellae of species of Calydiscoides from nemipterids and concluded that the ‘break’ was an optical illusion rather than an actual break. In contrast, the present study establishes that the outermost lamellae (generally from, and including, the fourth lamella) are incomplete in all species of Calydiscoides from lethrinids.

The number of lamellae in lamellodiscs was considered as variable in previous descriptions, but the present study of C. euzeti n. sp. shows that the number can be perfectly stable within a species. The number of 10 lamellae, found in C. euzeti, was the same as in C. australis and C. rohdei; it is variable (8–10) in C. gussevi.

The structure of the soft parts of the male and female organs in species of Calydiscoides appears homogeneous. Although these were not described in C. gussevi and C. rohdei by Oliver (1984), the structure is similar in these species to that found in C. australis and C. euzeti.

Differences between Calydiscoides Young, 1969 and Protolamellodiscus Oliver, 1969, two genera described almost simultaneously, are unclear. Both genera are primarily characterised by the presence of lamellodiscs without paired lamellae, which differentiates them from Lamellodiscus. The differential diagnosis between the two genera based on lamellodisc structure in Oliver (1987, p. 121) is not clear, because it refers to lamellodiscs observed from different orientations. The diagnosis of Calydiscoides in Oliver (1987, p. 121) is congruent with the list of species included and indicates that hosts are lethrinids and nemipterids, but the diagnosis of Protolamellodiscus in Oliver (1987, p. 123) indicates that hosts are serranids and (erroneously) leiognathids, although species included are from the Serranidae, Sparidae and Nemipteridae. Kritsky et al. (2000) suggested that Calydiscoides and Protolamellodiscus could be synonyms, and described Protolamellodiscus senilobatus Kritsky, Jiménez-Ruiz & Sey, 2000 from a sparid.

Egg-shape could be a key character for the differential diagnosis, with Calydiscoides having elongate eggs and Protolamellodiscus having tetrahedral eggs (Oliver, 1987). The present study describes the eggs of C. gussevi for the first time and confirms that eggs are elongate in all species of Calydiscoides from lethrinids in which they were observed. Oliver (1987) transferred Lamellodiscus convolutus Yamaguti, 1953 to Protolamellodiscus. Examination of the type-specimens (MPM 22558 slide SY 6729), apparently not examined by Oliver, shows that the lamellodisc structure is similar to Calydiscoides, with seven concentric and telescopic lamellae, and that the eggs are elongate with a short filament; therefore, L convolutus is herein transferred to Calydiscoides as Calydiscoides convolutus (Yamaguti, 1953) n. comb. After this transfer, the respective host ranges are, for Calydiscoides, exclusively Nemipteridae and Lethrinidae (especially Lethrininae, Lethrinus) and, for Protolamellodiscus, exclusively Sparidae and Serranidae.

Mentions in the literature of Protolamellodiscus species from lethrinids probably correspond to species of Calydiscoides. This is the case for ‘Protolamellodiscus convolutus (Yamaguti, 1953)’ from Lethrinus harak off Okinawa, Japan, recorded by Dyer et al. (1989), which was examined and is a specimen of C. difficilis. It is probably also the case for ‘Protolamellodiscus sp.’ from L. miniatus off Eastern Australia, recorded without description by Rohde, Hayward & Heap (1995).

Other parasites from Lethrinus rubrioperculatus and L. xanthochilus

The following parasites were collected from L. rubrioperculatus: two undetermined species of the ancyrocephalid Haliotrema, undetermined larvae of a gnathiid isopod, and copepods (Caligus cf. mauritanicus; identified by G. A. Boxshall, Natural History Museum, London). An undetermined filiform didymozoid was also found within the gill arch, and pharyngeal teeth bear the capsalid Encotyllabe sp. Limited observations on other organs revealed presence of two species of opecoelid digeneans, including Pseudoplagioporus interruptus Durio & Manter, 1968, in the intestine (determination by Rod Bray, Natural History Museum, London), and larvae of two trypanorhynch cestodes, the tentaculariid Nybelinia sp. and the otobothrid Otobothrium sp. in the body-cavity (determination by Ian Beveridge, University of Melbourne). For L. rubrioperculatus, this makes a total of five parasite species (three monogeneans, one isopod and one copepod) on a single organ, the gill, and a total of 11 species for all organs. The gills of the single L. xanthochilus collected had only a very few undetermined larval copepods in addition to C. euzeti and a species of Haliotrema; Encotyllabe sp. were present on pharyngeal teeth.

Notes

Acknowledgements

Louis Euzet (Sète, France) helped with an early study of the new species. Julie Mounier, volunteer technician, and Charles Beaufrère, Audrey Guérin, Anaïs Guillou, Amandine Marie, Chloé Journo, Violette Justine, Eric Bureau, Maya Robert, Damien Hinsinger, Aude Sigura, Guilhem Rascalou and Géraldine Colli, all students, and Frank Moravec and Susan Lim, visitor scientists, participated in the fishing operations and parasitological survey. Alexia Cron and Kostia Arnone, students, participated in an unfinished study in 2003. Sam Tereua, Miguel Clarque and Napoléon Colombani, captains of the R/V ‘Coris’ provided safe navigation. Gérard Mou Tham (IRD) spear-fished certain specimens. Angelo di Matteo (IRD) provided technical help. Ian Beveridge (Melbourne, Australia), and Geoffrey Boxshall and Rod Bray (NHM, London, England) agreed to study, respectively, cestodes, copepods and digeneans. Kent Carpenter (Old Dominion University, Virginia) kindly identified some of the fish from photographs. Jimmy Cassone (MNHN, Paris), Eric P. Hoberg and Pat Pilitt (USNPC, Beltsville) and Takashi Iwaki (MPM, Tokyo) kindly arranged the loan of type-specimens.

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Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Équipe Biogéographie Marine Tropicale, Unité Systématique, Adaptation, Évolution (CNRS, UPMC, MNHN, IRD)Institut de Recherche pour le DéveloppementNouma CedexNew Caledonia

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