Introduction

There are about 40 species, belonging to six genera in two subfamilies, Lethrininae and Monotaxinae, within the Lethrinidae (see Carpenter & Allen, 1989). The most speciose genus is Lethrinus Cuvier, with 26–30 species (Froese & Pauly, 2010; Randall, 2005; Sato, 1978) in tropical waters of the Indo-Pacific region. Only L. atlanticus Valenciennes occurs in the Atlantic Ocean, off West Africa. Off New Caledonia, 13 species of Lethrinus have been recorded (Randall, 2005).

Lethrinid species, particularly those caught off New Caledonia, harbour a variety of monogeneans, including Encotyllabe sp. (Capsalidae) on the pharyngeal teeth, and various species of microcotylids, diplectanids and ancyrocephalids on the gills (Justine, 2007, 2010). Microcotylid species are rare and usually immature. Diplectanids from lethrinids include species of Calydiscoides Young, 1969 on Lethrinus spp. (Lethrininae) and Lamellodiscus Johnston & Tiegs, 1922 on Gymnocranius spp. and Gnathodentex spp. (both Monotaxinae) (Justine, 2007; Justine & Briand, 2010; Rascalou & Justine, 2007). To date, there are only three Haliotrema spp. (Ancyrocephalidae) described from Lethrinus spp., i.e. H. chrysostomi Young, 1968 from L. chrysostomus (Richardson) [now L. miniatus (Forster)] and also from a haemulid, Plectorhinchus pictus (Thunberg) [now Diagramma picta (Thunberg)], off Australia; H. fleti Young, 1968 from L. fletus Whitley [now L. laticaudis Alleyne & Macleay], L. laticaudis, L. miniatus and L. nebulosus (Forsskål) off Australia (see Young, 1968); and H. lethrini (Yamaguti, 1937) Young, 1968 from L. haematopterus (Bleeker) off Japan and L. miniatus off Australia.

Ancyrocephalid species were collected from nine species of Lethrinus off New Caledonia, namely L. harak (Forsskål), L. lentjan (Lacépède), L. miniatus, L. nebulosus, L. obsoletus (Forsskål), L. ravus Carpenter & Randall, L. rubrioperculatus Sato, L. variegatus Valenciennes and L. xanthochilus Klunzinger. However, only sufficient numbers of specimens were collected from L. rubrioperculatus for descriptions. Thus far, no ancyrocephalid species have been recovered from members of the Monotaxinae (Table 1).

Table 1 Ancyrocephalid and diplectanid monogeneans found on the gills of members of the Lethrinidae (Lethrininae and Monotaxinae) off New Caledonia
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In this paper, we describe two new monogenean species from L. rubrioperculatus and propose a new genus to accommodate them. We have also re-examined the type-specimens of H. chrysostomi and H. fleti from Lethrinus spp., H. australe Johnston & Tiegs, 1922 (type-species) from Upeneus signatus (Günther) [now Parupeneus signatus (Günther)] (Mullidae) (type-host) and voucher specimens of several Haliotrema spp. from lethrinids and mullids for comparative purposes (see below).

Materials and methods

Specimens of Lethrinus rubrioperculatus, (“spotcheek emperor”; local name “bossu rond”) were caught with hand lines on board the R/V “Coris” in the waters (depth of 10–40 m) off New Caledonia, in both the lagoon and along the barrier reef 20 km off Nouméa. Live fish were kept in an icebox with refrigerated 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 parasite material was then assigned a corresponding JNC linked to the respective fish host.

Gills were extracted and examined in seawater with a dissecting microscope. Live monogeneans were individually picked off the gills with fine needles and immediately prepared for staining with carmine by an initial flattening between a slide and a coverslip in 70% ethanol (Justine, 2005). Some specimens were fixed in modified ammonium picrate-glycerine (Malmberg, 1957; Lim, 1991), examined unstained using phase contrast microscopy, and later washed and stained in Gomori’s trichrome stain. A few specimens were also examined live in seawater.

Monogeneans were drawn with an Olympus BH2 microscope and a Leitz DM2500 microscope, both equipped with a camera lucida. Drawings were scanned and redrawn on a computer with Adobe Illustrator. Alternatively, microscope images of the hard and soft body parts were captured, using a Leica digital camera (3.3MP) (on a DM2500) and QWin Plus image analysis software, and drawn on a digitising tablet (WACOM) using Adobe Illustrator software. In this paper only one species is fully illustrated, since both are similar in their non-sclerotised anatomical structures.

Measurements of the haptoral and reproductive hard-parts (parameters measured indicated in Fig. 2) were made on flattened, stained or unstained specimens cleared in ammonium picrate glycerine using the measuring option in QWin software. The measurements are given as the mean and range (within parentheses) in micrometres, with the length first followed by the width. The terms ‘posterior glandular mass’ and ‘opisthaptoral reservoirs’ were used by Young (1968) to refer to the peduncular glands and the haptoral reservoirs, respectively.

The type- and voucher specimens of Haliotrema spp. (see list below) re-examined in this study were obtained from: MNHN (Muséum National d’Histoire Naturelle, Paris); BMNH (Natural History Museum, London), USNPC (United States National Parasite Collection, Beltsville); UMZP (University of Malaya, Kuala Lumpur); and AMS (Australian Museum, Sydney).

Museum specimens examined in this study

Haliotrema australe Johnston & Tiegs, 1922, holotype and paratype on slide AMS W883.

Haliotrema chrysostomi Young, 1968, 2 paratypes, USNPC 61283: 1 slide marked ‘paratype 1’ from Lethrinus chrysostomus; 1 slide marked ‘paratype 4’ from Plectorhinchus pictus.

Haliotrema fleti Young, 1968, 2 paratypes, USNPC 61285, from L. fletus: 3 slides, marked as ‘paratype 2’, ‘paratype 1 anterior end’, and ‘paratype 1 posterior end’.

Haliotrema sp., 3 vouchers, BMNH 1994.8.10.98-100 (1 slide) (leg. I. Al-Mathal), from L. lentjan, Arabian Gulf, probably belonging to 2 or 3 species [together with specimens of Calydiscoides difficilis (Yamaguti, 1953) Young, 1969 (see Rascalou & Justine, 2007)].

Haliotrema spp., MNHN, 10–15 species, mostly unidentified, from mullids off New Caledonia: Parupeneus barberinoides (Bleeker) (JNC2415); P. ciliatus (Lacépède) (JNC1916, JNC2525); P. cyclostomus (Lacépède) (JNC1599, JNC1922); P. heptacanthus (Lacépède) (JNC1075, JNC2984); P. indicus (Shaw) (JNC2444); P. multifasciatus (Quoy & Gaimard) (JNC1005, 1205, 1224, 1420, 2413, 2445); P. pleurostigma (Bennett) (JNC2443); P. spilurus (Bleeker) (JNC2444); Upeneus tragula (Richardson) (JNC2428, JNC2429).

Haliotrema leporinum Sun, Yang & Kritsky, 2007 (emend.), marked paratype, MNHN JNA41, from Acanthurus nigrofuscus (Forsskål), South China Sea (Sun et al., 2007).

Haliotrema pratasense Sun, Yang & Kritsky, 2007 (emend.), marked paratype, MNHN JNA42, from Acanthurus olivaceus Bloch & Schneider, South China Sea (Sun et al., 2007).

Lethrinitrema n. g.

Diagnosis. Ancyrocephalidae Bychowsky, 1937 [sensu Gusev (1978)]. Body elongate, flattened dorsoventrally; haptor not well demarcated from body. Three pairs of head organs; 2 pairs of dorsal eye-spots. Mouth subterminal, ventral. Pharynx muscular. Intestine bifurcates just posterior to pharynx; 2 intestinal caeca, confluent posterior to testis, forming cyclocoel, but extend further posteriorly as 2 diverticula. Haptor small in relation to body proper, armed with dorsal and ventral pairs of anchors, dorsal and ventral connecting bars and 14 larval-type hooks. Ventral anchors with superficial lateral groove on each lateral side and well-developed inner root with crown-like piece on its tip. Dorsal anchors without lateral grooves. Dorsal and ventral connecting bars well developed. Two pear-shaped haptoral reservoirs, each associated with ventral anchor; elongate tubular extension of each reservoir bifurcates prior to entering lateral groove along each side of ventral anchor (Fig. 2A). Gonads intercaecal, tandem. Testis postovarian. Vas deferens originates from anterior region of testis, passes ovary dorsally, loops around sinistral caecum to ventral side, distends to form seminal vesicle, ascends and enters initial part (base) of copulatory tube. Two elongate, pyriform prostatic reservoirs; prostatic duct connects with base of male copulatory organ. Male copulatory organ a simple, short, tapered copulatory tube with wide initial part, sometimes with distal, slightly sclerotised accessory piece. Ovary elongate, smaller than testis, at mid-body. Oviduct arises from anterior side of ovary, receives duct from vagina (seminal receptacle not observed) and right and left vitelline ducts, forms oötype surrounded by Mehlis’ gland-cells. Female duct continues to ascend medially as uterus; uterine pore opens ventrally near atrium of male copulatory organ. Prominent, muscular vaginal bulb, dextrolateral; duct from vagina connects with oviduct; seminal receptacle not observed. Vitelline system approximately co-extensive with intestinal caeca; anterior confluence of lateral vitelline fields just posterior to intestinal bifurcation, medial confluence just anterior to ovary and posterior confluence just posterior to cyclocoel but anterior to haptor. Parasitic on gills of lethrinid fishes (Perciformes).

Type-species: Lethrinitrema gibbus n. sp. from Lethrinus rubrioperculatus off New Caledonia.

Other species (see Table 2 for synonyms of fish names):

Table 2 Distribution patterns of the present five species of Lethrinitrema n. g.
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Lethrinitrema dossenus n. sp. from Lethrinus rubrioperculatus, off New Caledonia.

Lethrinitrema chrysostomi (Young, 1968) n. comb. from Lethrinus miniatus and allegedly (see below) Diagramma picta (Haemulidae), off Australia.

Lethrinitrema fleti (Young, 1968) n. comb. from Lethrinus laticaudis, L. miniatus and L. nebulosus off Australia.

Lethrinitrema lethrini (Yamaguti, 1937) n. comb. from Lethrinus haematopterus off Japan and L. miniatus off Australia.

Remarks

Members of Lethrinitrema n. g. possess four anchors, one ventral and one dorsal connecting bars, 14 morphologically similar marginal hooks, tandem gonads (ovary pretesticular), a non-sclerotised muscular, dextrolateral vaginal bulb, a male copulatory organ lacking an accessory piece or with a thinly sclerotised accessory piece, and a ventral male genital pore. These characteristics can also be found in many ancyrocephalids, particularly in Haliotrema spp. (see Lim & Justine, 2007). In fact, many previously described species exhibiting these features were assigned as Haliotrema, resulting in Haliotrema spp. being distributed on a wide diversity of marine fish species. Haliotrema is the ‘catch-all’ genus for many of the marine monogeneans with four anchors, two bars and 14 marginal hooks, whereas Ancyrocephalus Creplin, 1839 (sensu stricto) seems to be its freshwater counterpart.

Lethrinitrema spp. can be distinguished from the other marine ancyrocephalids by having two pear-shaped haptoral reservoirs, in which the elongate tubular extension bifurcates prior to contact with the superficial lateral grooves along both sides of the ventral anchors (Fig. 2A). In this study we have also examined several undescribed Lethrinitrema spp. from other Lethrinus spp. off New Caledonia (see ‘Introduction’) and have re-examined type- and voucher specimens of Haliotrema spp. from lethrinids, H. australe (holotype and paratype), Haliotrema spp. from several mullids and Haliotrema and Haliotrema-like species from different fishes off New Caledonia (see list above). Except for the Lethrinitrema spp. and Haliotrema spp. from lethrinids (see re-assignments below), all the other monogeneans examined are devoid of haptoral reservoirs. In the new species of Lethrinitrema (described below), the caeca form a cyclocoel just posterior to testis and continue as two posterior gut diverticula. Yamaguti (1963) pointed out differences in the intestinal pattern between the original description of H. australe compared with the holotype, and differentiated Haliotrema (with ‘intestinal crura apparently separate, but actually united separately’) from Ancyrocephalus (with ‘intestinal crura not united posteriorly’). We can thus safely consider that species of Lethrinitrema n. g., with two haptoral reservoirs and ventral anchors with lateral grooves, are distinct and different from Haliotrema (sensu stricto) spp. (see below).

It should be noted that the apparent absence of haptoral reservoirs could be due to the method of collection, specimen preparation or the condition of the specimens during collection. According to the literature, there are other ancyrocephalids with two haptoral reservoirs: Allomurraytrema spari (Yamaguti 1958) Byrnes, 1986 [syn. of A. robustum (Murray, 1931)], Calceostomella inermis (Parona & Perugia, 1889) Palombi, 1943, Cichlidogyrus halli typicus El-Naggar & Kearn, 1989, Chauhanellus australis Kearn & Whittington, 1994, C. youngi Kearn & Whittington, 1994, Hamatopeduncularia arii Yamaguti 1953, H. major Kearn & Whittington, 1994 and H. pearsoni Kearn & Whittington, 1994 (see Wong et al., 2008). There are also ancyrocephalids with four haptoral reservoirs, and they include members of Sundatrema Lim & Gibson, 2009, Parancylodiscoides Caballero & Bravo-Hollis, 1961, Bravohollisia Bychowsky & Nagibina, 1970, Caballeria Bychowsky & Nagibina, 1970, Ancyrocephaloides Yamaguti, 1938 and Placodiscus Paperna, 1972, as well as Haliotrema kurodai Ogawa & Egusa, 1978 and Neocalceostomoides brisbanensis Whittington & Kearn, 1995 (see Lim, 1995b; Lim & Gibson, 2008a, 2009; Wong et al., 2008). Placodiscus was proposed for species with four ‘opisthaptoral refractile bodies’ or ‘plaques’ from sparids (Paperna, 1972), which are probably haptoral reservoirs. Ogawa & Egusa (1978) suggested that H. kurodai, which is also from a sparid, Acanthopagrus schlegeli (Bleeker), might eventually be re-assigned; Placodiscus is a likely designation. These ancyrocephalids differ from the present new species and from each other not only in the shape and size of their anchors and haptors (e.g. anchors with expanded outer roots in Chauhanellus spp., a digitate haptor in Hamatopeduncularia spp. and a large circular haptor in Neocalceostomatoides spp.) but also in the presence or absence of superficial grooves in the anchors (e.g. no grooves in species of Haliotrema, Chauhanellus and Hamatopeduncularia vs lateral grooves in all four anchors of Bravohollisia, Caballeria and Ancyrocephaloides spp. vs lateral grooves only in the ventral anchors of Lethrinitrema spp.). The species with haptoral reservoirs also differ in the way the haptoral reservoir tubular extension opens to the exterior. In Chauhanellus, Caballeria and Ancyrocephaloides spp., each non-bifurcate tubular extension of the four haptoral reservoirs enters a concealed, crevice-like opening on one side of the anchor into a bifurcate channel within the anchor, which directs the secretions into left and right grooves of the anchors (Lim, 1994, 1995a, b, 1996; Lim & Gibson, 2008a; Wong et al., 2008). In the case of the two new species of Lethrinitrema, the two extremities of the bifurcate tubular extension of the haptoral reservoirs are associated with the lateral grooves of the ventral anchor (Figs. 2A, 3A). In species such as Parancylodiscoides chaetodipteri Caballero & Bravo-Hollis, 1961, Neocalceostomoides brisbanensis, Cichlidogyrus halli typicus, Tetraonchus monenteron Diesing, 1858 and Sundatrema langkawiense Lim & Gibson, 2009, the haptoral reservoirs open directly to the exterior close to the site where the anchor point exits the body and the anchors do not have grooves (Lim & Gibson, 2009). All these monogeneans differ from Lethrinitrema spp. in their hosts; Lethrinitrema spp. are found on members of Lethrinus (Lethrinidae), whereas Sundatrema and Parancylodicoides spp. are found on ephippids, Ancyrocephaloides spp. on triacanthids, Bravohollisia spp. and Caballeria spp. on pomadasyids, Cichlidogyrus spp. on cichlids, Neocalceostomatoides, Chauhanellus and Hamatopeduncularia spp. on ariids, and Placodiscus spp., Allomurraytrema spp. and Haliotrema kurodai on sparids. Lim (1995b), Wong et al. (2008) and Lim & Gibson (2008a) proposed that the secretions stored in the haptoral reservoirs of the different species of Bravohollisia, Caballeria and Ancyrocephaloides assist in attachment and locomotion, with the net-like secretions acting as a belay device. Although no net-like secretions have been observed in the Lethrinitrema specimens examined, the same may be true for members of this genus.

The status of dactylogyridean monogeneans with four anchors has been controversial (cf. Kritsky & Boeger, 1989; Lim et al., 2001). In agreement with authors, such as Bychowsky & Nagibina (1978), Gusev (1978) and many more recent workers (e.g. Dmitrieva et al., 2009; Lim et al., 2001; Le Roux & Avenant-Oldewage, 2009; Lim & Gibson, 2008a, b, 2009; Lim & Justine, 2007; Marcotegui & Martorelli, 2009; Pariselle & Euzet, 2009), we recognise the Ancyrocephalidae, and we include Lethrinitrema n. g. within this family.

Lethrinitrema gibbus n. sp.

Type-host: Lethrinus rubrioperculatus Sato (Lethrinidae).

Type-locality: Lagoon off Nouméa, New Caledonia.

Type-specimens: Holotype JNC988B4 and 13 paratypes, [JNC1424 A1.01, JNC 1016 A7, JNC 1016 A2, JNC 988 B1, JNC 988 B2, JNC 989 A6, JNC 1422 A1, JNC 1422 A1, JNC 1113 A1, JNC 1728.01-03, JNC 1270.08-09], MNHN; 2 paratypes, 2011.1.5.1-2, BMNH; 2 paratypes, 104124, 104125, USNPC; 14 paratypes, [2010.01(P)-06(P), 2010.11(P), 2010.12(P)-2010.18(P)], MZUM(P).

Material studied: 34 specimens studied; 14 specimens measured.

Etymology: The species name gibbus, a noun (Latin for ‘hump’), refers to the local name of lethrinids, ‘bossus’, meaning ‘humpback’.

Description (Figs. 1–2)

Body leaf-like, 1,288 (1,191–1,458) × 204 (158–236). Three pairs of head organs; four pairs of pigmented eyespots. Mouth subterminal, ventral. Pharynx ovoid. Intestine bifurcates just posterior to pharynx; caeca unite just posterior to testis, continue posteriorly as 2 diverticula. Haptor small, not well demarcated, wider than long, 64 (53–79) × 127 (96–181). Fourteen larval-type hooks, length 12 (11–13). Dorsal anchors, inner length 31 (29–31), outer length 22 (21–23), well-developed inner roots 12 (11–14), outer root 3 (2–4), point 15 (12–16); ventral anchors, inner length 21 (19–22), inner root 12 (9–13) with crown-like piece, outer length 23 (22–24), outer root 4 (3–6), point 8 (7–9); superficial lateral groove along both sides of ventral anchors from shaft to point. Dorsal bar V-shaped, 45 (41–48) × 4 (3–5); ventral bar with posterior prominence, 41 (37–46) × 9 (7–11). Two pear-shaped haptoral reservoirs, each with elongate, tubular extension which bifurcates distally prior to entering lateral groove on each side of ventral anchor (Fig. 2A).

Fig. 1
figure 1

Composite illustration of Lethrinitrema gibbus n. g., n. sp. from Lethrinus rubrioperculatus, dorsal view

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Fig. 2
figure 2

Sclerotised parts of Lethrinitrema gibbus n. g., n. sp. A, ventral anchors; B, ventral bar; C, dorsal anchor; D, dorsal bar; E, hook; F, male copulatory organ; G, vaginal system; H, parameters measured

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Testis ovoid to bilobed, postovarian. Vas deferens leaves anterior region of testis, passes ovary dorsally, loops around sinistral caecum to ventral side, distends to form seminal vesicle, narrows, ascends and then enters initial part (base) of copulatory tube. Two elongate, pyriform prostatic reservoirs; prostatic duct connects with base of male copulatory organ. Male copulatory organ consists of simple tapered copulatory tube, length 40 (40–45), with long base (or initial part), recurved distally; thin accessory piece arises from distal end of tube. Prostatic gland ducts drain into anterior part of prostatic reservoir. Ovary in mid-body, smaller than testis. Vaginal bulb dextrolateral, muscular; vaginal duct leaves vaginal bulb and unites with oviduct; seminal receptacle not observed. Oviduct arises from anterior side of ovary, receives vaginal duct and both right and left vitelline ducts, ascends as oötype surrounded by Mehlis’ gland-cells, continues to ascend medially as uterus; uterine pore opens ventrally near atrium of male copulatory organ. Vitelline system approximately co-extensive with intestinal caeca; anterior confluence of lateral vitelline fields just posterior to intestinal bifurcation, medial confluence just anterior to ovary and posterior confluence just posterior to cyclocoel but anterior to haptor.

Differential diagnosis

L. gibbus n. sp. is the type-species for Lethrinitrema n. g. This species differs from previously described monogeneans with four anchors in having a combination of a pair of haptoral reservoirs with a bifurcate, tubular extension, ventral anchors with a lateral superficial groove on both sides, a prominent muscular vaginal bulb and a simple tapered copulatory tube (see ‘Remarks’ for Lethrinitrema n. g.).

Lethrinitrema dossenus n. sp.

Type-host: Lethrinus rubrioperculatus Sato (Lethrinidae).

Type-locality: Lagoon off Nouméa, New Caledonia.

Type-specimens: Holotype JNC988B3 and 16 paratypes, [JNC 984 A1, JNC 1064 A5.01-03, JNC 1424 A1.02-05, JNC 1016 A5.01-03, JNC1728.04, JNC1728.05, JNC1728.06, JNC1720.07 & JNC1720.08] MNHN; 2 paratypes, 2011.1.5.3-4, BMNH; 2 paratypes, 104122, 104123, USNPC; 12 paratypes, [2010.07(P)-10(P), 2010.19(P)–2010.26(P)], MZUM(P).

Material studied: 33 specimens studied; 13 specimens measured.

Etymology: The species name dossenus, a noun (Latin for ‘humpback’), refers to the local name of lethrinids, ‘bossus’, meaning ‘humpback’.

Description (Fig. 3)

Body leaf-like, 1,148 (970–1,546) × 152 (121–201). Haptor wider than long, 62 (42–91) × 92 (75–123). Fourteen larval type hooks, length 12 (11–13). Dorsal anchors, inner length 32 (30–33), outer length 24 (23–25), well-developed inner roots 2 (11–14), outer root 3 (2–3), point 13 (11–15); ventral anchors, inner length 20 (20–21), outer length 21 (20–24), inner root 12 (11–13) with crown-like piece at tip, outer root 3 (2–3), point 10 (8–13), with lateral groove on each side of shaft to point. Dorsal bar 32 (32–33) × 5 (3–5); ventral bar 37 (35–39) × 7 (6–8). Two pear-shaped hyaline haptoral reservoirs with distal tubular extension bifurcate, as in L. gibbus.

Fig. 3
figure 3

Sclerotised parts of Lethrinitrema dossenus n. g., n. sp. A, ventral anchor; B, ventral bar; C, dorsal anchor; D, dorsal bar; E, hooks; F, male copulatory organ

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Arrangement of male and female organs similar to L. gibbus. Male copulatory organ consists of funnel-shaped copulatory tube, length 25 (24–30), short initial part and inconspicuous accessory piece at its distal end. Prominent dextrolateral muscular vaginal bulb, as in L. gibbus.

Differential diagnosis

This species differs from L. gibbus n. sp. in the shape and size of the copulatory tube: in L. dossenus it is a short, funnel-like tube (24–30 μm in length) with short initial part and a lightly sclerotised (inconspicuous) accessory piece, whereas in L. gibbus the copulatory tube (40–45 μm in length) has a recurved distal tip, long initial part and a thin accessory piece (cf. Fig. 4E, F). The present species is also different from L. gibbus in the shape and size of the dorsal connecting bar (Table 3). Although there is some overlap, it also has dorsal anchors with shorter recurved points of 13 (11–15) μm, compared to 15 (12–16) μm in L. gibbus, and ventral anchors with a longer point of 10 (8–13) μm, compared to 8 (7–9) μm in L. gibbus.

Fig. 4
figure 4

Sclerotised male copulatory organs of four species of Lethrinitrema n. g. A, B, L. chrysostomi (Young, 1968) n. comb., USNPC 61283 (A, ‘paratype 4’; B, ‘paratype 1’); C, D, L. fleti (Young, 1968) n. comb., USNPC 61285 (C, ‘paratype 1’, D, ‘paratype 2’); E, L. gibbus n. sp.; F, L. dossenus n. sp.

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Table 3 Selected measurements of species of Lethrinitrema n. g. from different sources
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Lethrinitrema chrysostomi(Young, 1968) n. comb.

Syn. Haliotrema chrysostomi Young, 1968

Type-host: Lethrinus chrysostomus Richardson [now L. miniatus (Forster)] (Lethrinidae).

Other host: Plectorhinchus pictus (Thunberg) [now Diagramma picta (Thunberg)] (Haemulidae) (Young, 1968; Table 2).

Material studied: Paratype from L. miniatus; paratype from P. pictus.

Brief redescription (Fig. 4)

Measurements given in Table 3. Two haptoral reservoirs, 15 × 11 (‘paratype 1’), 12×7 (‘paratype 4’) (length 27–38 in original description). Testis 70 × 35 (‘paratype 1’). Measurements of anchors not possible because of poor orientation.

Comments

There are discrepancies between the measurements in the description given by Young (1968) and our measurements of the paratypes. However, measurements of the original figures of Young (1968) using the given scale-bar correspond to our measurements of the paratypes (Table 3). Rohde et al. (1994) also provided a drawing of the male copulatory organ of Haliotrema chrysostomi from Lethrinus miniatus, and the length of the male copulatory organ in their figure 11 is 32 μm, which is comparable to our measurements of the paratypes and our measurement of the original figure of Young.

From our examination of the two paratypes of H. chrysostomi, we have to accept Young’s interpretation that the specimens from L. miniatus (Lethrinidae) and Plectorhinchus pictus (Haemulidae) are the same species, since the paratypes from the two host species are similar, particularly in the structure of the male copulatory organ. P. pictus (Thunberg) is now designated as Diagramma picta, although Plectorhinchus pictus (Tortonese) nec (Thunberg) is valid. We have examined several specimens of D. picta, and several species of Plectorhinchus, from off New Caledonia, but we have not found any ancyrocephalids, although other monogeneans were present on the gills. The work of Young is not without fish misidentifications (Justine et al., 2009 ) and lethrinids can be easily confused for small haemulids; hence, the presence of Lethrinitrema chrysostomi on a haemulid needs to be confirmed.

Lethrinitrema fleti(Young, 1968) n. comb.

Syn. Haliotrema fleti Young, 1968

Type-host: Lethrinus fletus Whitney [now L. laticaudis Alleyne & Macleay] (Lethrinidae)

Other hosts: Lethrinus chrysostomus Richardson [now L. miniatus (Forster)] (see Rohde et al., 1994; Young, 1968); L. nebulosus (Forsskål) (see Zhang et al., 2001, 2003) (Table 2).

Material studied: Two paratypes from L. fletus.

Brief redescription (Fig. 4)

Measurements given in Table 3. Two haptoral reservoirs, 80 × 25 (‘paratype 1’), 70 × 25 (‘paratype 2’) (original description: 57–79). Testis 200 × 70 (‘paratype 2’). Measurements of anchors not possible because of poor orientation. Male copulatory organ in both specimens similar.

Comments

The measurements of Haliotrema fleti in the original text of Young (1968) do not correspond with either those obtained from the type-specimens or those obtained by measuring the original illustrations, particularly that of the haptoral reservoirs (Table 3). This species has the largest haptoral reservoirs, compared with the other species examined in this study. Rohde et al. (1994) also provided a drawing of the male copulatory organ of H. fleti from Lethrinus miniatus, but gave no other information; the curved length of the male copulatory organ, measured on their figure 11, is 55 μm.

Lethrinitrema chrysostomi n. comb., L. fleti n. comb., L. gibbus n. sp. and L. dossenus n. sp. can be distinguished on the basis of their male copulatory tube (Table 3; Fig. 4). In L. chrysostomi the copulatory tube is 29–30 μm long, with a terminal ‘hook’ (‘swollen complex tip’ in the original description); in L. fleti the copulatory tube is 44–48 μm long, with a crest at mid-length, probably similar to the spiral piece around the tube in the original drawing given by Young (1968); in L. gibbus it is 40–45 μm long, with a recurved distal extremity and a thin, distal accessory piece; and in L. dossenus it is a short (24–30 μm), funnel-shaped tube, with a lightly sclerotised distal accessory piece. According to Young (1968), the accessory piece is absent in L. chrysostomi, although the ‘hook’ at the extremity of the male copulatory organ could be interpreted as an accessory piece similar to the reduced accessory piece in L. gibbus and L. dossenus.

Lethrinitrema lethrini(Yamaguti, 1937) n. comb.

Syns Ancyrocephalus lethrini Yamaguti, 1937; Haliotrema lethrini (Yamaguti, 1937) Young, 1968

We were unable to examine the type-specimens of Haliotrema lethrini from Lethrinus haematopterus. However, this species possesses features [two haptoral reservoirs and a copulatory tube described as a ‘slender, curved, chitinous tube enclosed proximally in a muscular pouch’ (Yamaguti, 1937)], which are similar to those of the new species described above. H. lethrini is herein re-assigned as Lethrinitrema lethrini n. comb. (Table 2). This species is easily distinguished from the other four species of Lethrinitrema by the length of its copulatory tube (150 μm) and the shape of its anchors (see Yamaguti, 1937).

Discussion

There are five species of Lethrinitrema, L. dossenus n. sp., L. gibbus n. sp., L. fleti n. comb., L. chrysostomi n. comb. and L. lethrini n. comb. with the characteristics summarised in Table 4. In L. chrysostomi, L. fleti, L. gibbus and L. dossenus the caeca form two posterior gut diverticula which extend back from the cyclocoel; this feature was not mentioned in the description of L. lethrini. These two posterior gut diverticula are not visible in the specimens deposited by Young (1968) but are mentioned in the descriptions. The haptoral reservoirs of L. fleti are larger than in other species. L. lethrini is the largest species and L. chrysostomi the smallest (Table 3). The five species also differ in the detailed morphology of their male copulatory organs (Fig. 4) and bars, in particular, the size of the ventral bar (Table 3), which is wider in L. fleti than in the other species.

Table 4 Some characteristics of Lethrinitrema spp.
Full size table

We could ascertain that the five known species of Lethrinitrema have two haptoral reservoirs (Table 4) and a similar male copulatory organ in the form of a simple, tapering tube either without an accessory piece or with an inconspicuous accessory piece (Fig. 4). There is, however, a need to collect and re-examine specimens of the reassigned species, and in particular the two species described by Young (1968), in order to determine whether their internal anatomy is similar to that of the two new species, whether their haptoral reservoirs have a distal bifurcation and whether lateral grooves are present on their ventral anchors. In the paratype specimens examined, the anchors were not well oriented and we could not check for the presence of the ‘crown’ on the inner roots of the ventral anchors or for lateral grooves.

To date, many of the species assigned to Haliotrema spp., which are restricted to particular host groups, have been reassigned. For example, species of Ligophorus Euzet & Suriano, 1977 are restricted to mugilids; Euryhaliotrematoides spp. and Aliatrema spp. to chaetodontids; Volsellituba spp. and Pennulituba spp. to Mulloidichthys spp. (Mullidae); Haliotrematoides spp. to lutjanids, caesionids, haemulids and sparids; and Euryhaliotrema spp. to sciaenids, sparids, haemulids and lutjanids (Euzet & Suriano, 1977; Mendoza-Franco et al., 2009; Kritsky & Boeger, 2002; Kritsky et al., 2009; Plaisance & Kritsky, 2004; Rehulková et al., 2010). All known Lethrinitrema spp. are found on members of Lethrinus (Lethrinidae), although, as indicated above, L. chrysostomi has also been reported on a haemulid. The occurrence of Lethrinitrema spp. only on species of Lethrinus suggests a history of host-parasite co-evolution. We have several other species of Lethrinitrema collected off New Caledonia (which are undescribed due to insufficient numbers of specimens), all from other Lethrinus spp. (see ‘Introduction’), and there are also possibly two or three Lethrinitrema spp. on Lethrinus lentjan (Lacépède) in the Arabian Gulf (judging from BMNHN slide 1994.8.10.98-100, which we examined). The geographical distribution of Lethrinitrema spp. probably extends from off Japan to South-Eastern Australian waters, and from the Red Sea to New Caledonian waters, following the distribution range of Lethrinus spp. It would be of biogeographical interest to check the parasites of L. atlanticus in the Atlantic.