Labidodemas quadripartitum, Massin & Samyn & Thandar, 2004

Massin, Claude, Samyn, Yves & Thandar, Ahmed, 2004, The genus Labidodemas (Holothuroidea: Aspidochirotida) revisited, with description of three new species and with re-positioning of Holothuria (Irenothuria) maccullochi Deichmann, 1958, Journal of Natural History 38 (14), pp. 1811-1847 : 1828-1841

Labidodemas quadripartitum sp. nov.

(figure 7A–G; map 4)

Name-bearing type. Holotype RMcA1694/RSAKZN/0196.

Type locality. Sodwana Bay, 1/4 Mile Reef ( Republic of South Africa).

Material examined. Republic of South Africa (KwaZulu-Natal, Sodwana Bay, 1/4 Mile Reef ), February 2001, 12 m depth, coll. Y. Samyn, RMcA1694/ RSAKZN/0196 (holotype) .

Diagnosis. Medium-sized species; body vermiform; dorsal body wall whitish, ventral body wall reddish; calcareous ring ribbon-like; ventral body wall with tables only; dorsal body wall with tables and rods; tables with rim of disc spinose; spire of table low, single cross beam; crown of tables with four huge (occasionally slightly bifurcated) spines, wider than disc diameter.

Description. Specimen 110 mm long and 8 mm wide at its widest point. Body vermiform, tapering anteriorly with mouth and anus terminal. Colour in life similar to colour in alcohol: dorsally whitish yellow, ventrally claret-red. Skin thin (1–2 mm), rather smooth to the touch. Mouth terminal, tentacles retracted; number could not be determined. Anus small, terminal. Anal papillae absent. Ventral side with short but wide brownish tube feet distributed in three rows in ambulacral areas; dorsal side at first sight apparently without tube feet or papillae, but examination of inner body wall reveals large tube feet ampullae in ambulacral areas. Cuvierian tubules absent. Calcareous ring ribbon-like, with radial pieces 2.5 times height of interradials; radial pieces massive, with medial depression for longitudinal muscle, posterior margin slightly concave; interradial pieces brittle, anteriorly with tooth-like projection (figure 7F). Stone canal contorted, ending in large madreporic plate (figure 7G). Gonad not observed.

Ossicles. Dorsal and ventral body wall devoid of buttons. Ventral body wall (figure 7A) with tables only; table disc 45–60 µ m across, perforated by four large central holes and zero to occasionally six peripheral holes; rim of disc spinose, height of spire equal to width of disc, spire with single cross beam and ending in a crown with four huge spines that occasionally bifurcate distally, crown of spines considerably wider than disc. Dorsal body wall with tables and rods (figure 7B, C); tables (figure 7B) with disc 30–60 µ m across, perforated by four large central holes and zero to one peripheral hole, rim of disc moderately to very spinose, spire often reduced to knobs on disc, but occasionally persists as high as width of disc but then with a single cross beam that ends in a fourspined crown, usually not wider than disc; rods, 35–50 µ m long, straight or with slightly undulating margins (figure 7C). Ventral tube feet with tables and rods (figure 7D, E); tables mostly reduced to disc, 33–42 µ m across, perforated by three to four central holes and occasionally a single peripheral one, rim of disc slightly spinose, spire reduced to two or four knobs on surface of disc; rods 33–55 µ m long, branched medially or distally, often perforated by one to several holes.

Etymology. The name quadripartitum refers to the crown of the tables that ends in four huge spines; quadripartitum (Latin) meaning split into four.

Ecology. The single specimen was collected at 12 m depth; over coarse sand under and between several large slabs of dead coral and rock.

Geographical distribution (see map 4). At present only known from the type locality.

Comments. The new species, with its ribbon-like calcareous ring, its ventral side with three rows of tube feet and dorsal side with two rows of tube feet, and its ossicle assemblage, undoubtedly belongs to Labidodemas . Nevertheless, the general body morphology of L. quadripartitum is unique to the genus. The dorsal body wall is yellowish to light brown and at first sight seems devoid of tube feet or papillae; however, inspection of the inner surface of the body wall reveals large tube feet ampullae in all five ambulacra. The ventral body wall is claret-red and has three rows of wide brownish tube feet. Although we have currently only one specimen at our disposal it is unlikely that this species will ever present a body wall that is translucent. The ossicle assemblage reveals that L. quadripartitum is very close to L. semperianum and L. pseudosemperianum , but several differences warrant it new species status. Table 2 lists the differences in the body wall ossicles of the three species.

Labidodemas rugosum ( Ludwig, 1875)

(figure 8A–L; map 5)

Holothuria rugosa Ludwig, 1875: 110 , pl. 7, figure 33d–e; Pearson, 1913: 82 (synonymy and records before 1908).

Holothuria (Holothuria) rugosa ; Panning, 1935a: 75.

Labidodemas rugosum: Rowe, 1969: 133 ; Levin, 1979: 20; James, 1981: 83; Mukhopadhyay, 1991: 408; Rowe and Gates, 1995: 304; Rowe and Richmond, 1997: 302; Massin, 1999: 58, figures 46a–j, 47a–c, 48 (records before 1998); Lane et al., 2000: 489.

Holothuria triremis Sluiter, 1901: 19 , pl. 6, figure 3a–c.

? Holothuria triremis: Pearson, 1913: 82 .

Holothuria (Halodeima) trimensis: Panning, 1931: 119 (lapsus calami for Holothuria triremis Sluiter, 1901 ).

Original name. Holothuria rugosa Ludwig, 1875 .

Name-bearing type. Holotype ZMH E.2625.

Type locality. Samoa (as Navigator Islands).

Current status. Labidodemas rugosum ( Ludwig, 1875) .

Material examined. Samoa, collecting date and depth unknown, coll. Dr Graeffe, ZMH E.2625 (Mus. Godeffroyi 9937, holotype) ; Republic of South Africa (KwaZulu-Natal, Sodwana Bay, 2 Mile Reef ), July 2001, 15 m depth, coll. Y. Samyn, RMcA1695/RSAKZN/0099 (one specimen) ; Indonesia (Celebes Islands, Kudingareng Keke ), 5 October 1994, 2 m depth, coll. C. Massin, IRSNB IG.28251/256 (one specimen) ; Papua New Guinea ( Hansa Bay , Laing Island, L 4), 18 October 1996, reef flat at low tide, under rock, coll. C. Massin, IRSNB IG28455 /55 (one specimen) ; Papua New Guinea ( Hansa Bay , Laing Island, K 3), 20 October 1996, reef flat at low tide, coll. J. M. Ouin, IRSNB IG28455 /62 (two specimens) ; British Indian Ocean Territory (Chagos Archipelago, Diego Garcia ), 7 August 1967, coll. J. D. Taylor, NHM 1969.5 .27.22 (two specimens) ; British Indian Ocean Territory (Chagos Archipelago, Diego Garcia ), 8 August 1967, sublittoral fringe, coll. J. D. Taylor, NHM 1969.5 .27.23.26 (five specimens) .

Diagnosis. See Cherbonnier, 1988: 53–55, figure 19.

Description. Small to medium-sized species; preserved specimens 67–133 mm long and 4–20 mm wide. Body cylindrical, mouth and anus terminal. Colour in life uniform whitish with yellowish tube feet; fading slightly after preservation. Skin thin (1–2 mm thick), but rather gritty to the touch. Mouth terminal surrounded by 20 small, yellowish tentacles. Ventral side with tube feet in three to four rows in median ambulacrum and in two rows in each lateral ambulacrum; some tube feet in interambulacral areas. Dorsal side with whitish papillae and short yellowish tube feet more or less confined to ambulacra, but also scattered in interambulacra. Ampullae of tube feet conspicuous on inner side of body wall. Cuvierian tubules absent. Tentacle ampullae short (1/12 body length). Single, well-developed Polian vesicle (one-sixth of body length). Single, small (4 mm), straight stone canal ending in minute madreporic plate (figure 8L). Calcareous ring composed of huge radial pieces and slender interradials; posterior margin of ring undulating; radial pieces with anterior notch, and central depression for longitudinal muscle; interradial pieces ribbon-like with minute anterior tooth-like projection (figure 8K). Digestive tract filled with rough coral sand and pieces of coral smaller than in L. americanum .

Ossicles. Tentacles with simple, straight or curved, smooth rods, 25–85 µ m long (figure 8A). Ventral and dorsal body wall with similar tables and buttons (figure 8B–E). Table discs 65–90 µ m across, perforated by four large central holes and 6–11 peripheral holes; rim of disc very spinose; margin of disc slightly turned upward; height of spire equal to diameter of disc; spire with four undulating pillars, united by one or two cross beams and terminating in crown consisting of cluster of stout spines; crown occasionally with small central perforation (figure 8B, D). Buttons, 45–85 µ m long, with two to six pairs of irregular holes, margins smooth, but undulating (figure 8C, E). Ventral tube feet with tables and buttons (figure 8F, G): tables similar in shape to those of body wall, but disc only 45–65 µ m across; crown of spines less developed but often perforated by central hole; spire occasionally reduced to knobs on surface of disc (figure 8F); buttons plate-like, surrounding end plate, 70–100 µ m long, generally rim more irregular than that of body wall buttons (figure 8G). Dorsal papillae with tables and buttons: tables similar in shape to those of body wall, but generally smaller (figure 8H); buttons very irregular, often rod-like, generally larger than those of body wall (figure 8J).

Ecology. Found in shallow waters, always less then 20 m deep ( Lane et al., 2000); deposit/detritus feeder; under coral slabs and in and on coarse coral debris. Gut of the South African and Chagos specimens filled with coarse sand.

Geographical distribution (see map 5). If compared with figure 48 in Massin (1999: 61), the following new localities are here added: Republic of South Africa (KwaZulu-Natal), Malaysia, northern part of the Philippines.

Comments. In his revision of the Holothuriidae, Rowe (1969) realized that H. rugosa Ludwig, 1875 , because of its body form and ribbon-like calcareous ring, belongs in Labidodemas . It has been treated as such since then and the present revision corroborates this.

Labidodemas semperianum Selenka, 1867

(figures 9A–J, 10A–H; map 6; figure 11A–L for L. selenkianum ) Labidodemas Semperianum Selenka, 1867: 309 , pl. 17, figures 1–3. Labidodemas semperianum Selenka, 1867 ; Rowe and Richmond, 1997: 302; Massin, 1999: 61 (records before 1998, partim); Lane et al., 2000: 489; Samyn, 2000: 15; Marsh, 2000a: 26; Marsh, 2000b: 101. Labidodemas dubiosum Ludwig, 1875: 98 , pl. 7, figure 25; Lampert, 1885: 110; Théel, 1886: 189. Labidodemas egestosum Sluiter, 1901: 22 .? Labidodemas Selenkianum Semper, 1868: 77 ; Lampert, 1885: 110.? Labidodemas selenkianum ; Théel, 1886: 188. Labidodemas semperlanum: Allen and Steene, 1994: 245 (lapsus calami for L. semperianum ).

Labidodemas semprianum: Arakaki and Fagoonee, 1996: 122 (lapsus calami for L. semperianum ).

? Holothuria pertinax: Sluiter 1887: 186 , pl. 1, figures 1, 2.

Labidodemas pertinax: Rowe and Doty, 1977 : figures 3b, 5g [non L. pertinax ( Ludwig, 1875) ].

Labidodemas sp.: Price and Reid, 1985: 3 (here identified as L. semperianum ).

Holothuria proceraspina Cherbonnier, 1967: 62 , figure 3a–o (syn. nov.); Price, 1982: 11; Tortonese, 1977: 275.

Original name. Labidodemas semperianum Selenka, 1867 .

Name-bearing type. Syntypes ZMG (no number given by Selenka, 1867), MCZ 736 (two specimens). As the syntypes of the ZMG are untraceable (Troester, personal communication), a lectotype and a paralectotype are here designated in the MCZ 736 material: as lectotype the dissected specimen (75 mm long) and as paralectotype the non-dissected specimen (90 mm long) are chosen.

Type locality. Formerly Hawaiian Islands (as Sandwich-Inseln) but now Society Islands according to the designation of lectotype .

Current status. Labidodemas semperianum Selenka, 1867 .

Material examined. Society Islands, collecting date, depth and collector unknown, MCZ 736 (two specimens); Maldives (Male Atoll, Dunidu Island ), 18 March 1964, 4 m depth, coll. F. Ziesenhenne, USNM E11583 (one specimen identified as L. pertinax ) ; Philippine Islands, 26 May 1978, 6– 7 m depth, USNM E24458 (one specimen) ; Indonesia (Sumatra, Pula We´ ), 1980–1981, 2 m depth, sublittoral rock, coll. A. Price, NHM 1999.2148 (one specimen) ; Philippine Islands (La Onoy Gulf, Luzon Island ), 5 April 1989, intertidal, USNM E40771 (one specimen identified as L. rugosum ) ; China, collecting date and depth unknown, coll. Kpt. Schnehagen, ZMH. E. 2933 (one specimen identified as L. pertinax ) ; Fidji, collecting date and depth unknown, coll. Dr Graeffe, ZMH E.2674 (Mus. Godeffroy 1170, holotype of L. selenkianum Semper, 1868 ) .

Diagnosis. Cherbonnier, 1970: 566, figure A–P; present revision. Description. The lectotype and paralectotype are cylindrical, 70X20 and 90X 15 mm, respectively. Both type specimens are grey-white in alcohol; mouth and anus terminal; lectotype with 12 tentacles visible but, most probably the

number is 20 as in all the other species belonging to the genus Labidodemas . Ventral tube feet very long, cylindrical and only present in the ambulacral areas; each ambulacrum with two rows of tube feet in a zigzag pattern, more densely crowded at mid-body and fewer close to mouth and anus. Dorsally tube feet few, dispersed in ambulacral and interambulacral areas; no clear alignment visible. Body wall gritty to the touch. Calcareous ring of the lectotype ribbon-like with large quadrangular radial plates and very thin interradial plates (figure 9A). One huge Polian vesicle (one-third of body length); tentacle ampullae very short (1–2 mm long); stone canal not observed. Vesicles of ventral tube feet prominent. Gonad well developed, made of several very large tubules. Cuvierian tubules absent.

Ossicles. In the ventral body wall of the lectotype tables only (figure 9B), 55–80 µ m across; rim of the table disc spiny with sometimes one very long spine; table disc perforated by four to six central holes and 5–10 peripheral holes; spire low, ending in four to six long spines, most of them bifurcated distally; table crown generally larger than table disc. In the dorsal body wall tables (figure 9C) similar to the ones of the ventral body wall, buttons (figure 9D) 60–75 µ m long, sometimes knobbed, pseudo-buttons (figure 9E) 55–65 µ m long and rods 50–70 µ m long (figure 9F). Number of buttons, pseudo-buttons and rods highly variable from one specimen to the other. In some specimens they seem to be gathered in heaps. Ventral tube feet have tables that are reduced to the spinyedged disc (figure 9G) and rods (figure 9H). End plates more or less 500 µ m across. Dorsal papillae with small rods (figure 9J) and no end plate. Tentacles with rods 20–60 µ m long, very similar to the ones of Labidodemas pseudosemperianum (cf. figure 6G).

The paralectotype (figure 10A, B), the specimens from Maldives (figure 10C) and the Philippines (figure 10D–H) show very few variations from the lectotype. Re-examination of the holotype of Labidodemas selenkianum Semper, 1868 (figure 11A–L) shows somewhat corroded ossicles; the tables have a reduced crown but the general aspect is very similar to that of L. semperianum .

Ecology. Lives under coral slabs and coral rocks in shallow water (0–10 m depth).

Geographical distribution (see map 6). The following new localities are added since Massin’s (1999: 62, figure 50) publication: China, South China Sea, Montebello Islands, Christmas Island; Pitcairn Islands. Moreover, Kenya has to be removed from Massin’s (1999) map, since Humphreys’ (1981) record of L. semperianum (NHM 1979.2.5.229, identified by A. M. Clark) proved to be L. pertinax after examination. Celebes ( Indonesia) also needs to be omitted since Massin’s records (1999) of L. semperianum (RMNH Ech 6087 and IRSNB IG 28251/197) proved to be L. pseudosemperianum and L. pertinax , respectively.

Comments. Labidodemas semperianum , with its wide Indo-Pacific distribution, is one of those species which seems easy to identify due to its very characteristic ossicle assemblage (especially the tables). However, re-examination of material from IRSNB, MCZ, NHM, RMNH and ZMH revealed many misidentifications with, very often, a confusion between L semperianum and L. pertinax . This confusion undoubtedly results from the similar external aspects of both species. As such, when one sample includes several specimens they are often designated under a single species name whereas careful examination of the ossicles of all the specimens in the sample reveals several species.

Cherbonnier (1970) gave a very good description of L. semperianum but, unfortunately, it was based on non-type material from Marshall Islands ( Guam). According to Rowe and Gates (1995), syntypes are housed in the ZMG and the MCZ. The ZMG type series is currently untraceable in the ZMG (Troester, personal communication) whereas MCZ syntypes are available. To stabilize the taxonomy of L. semperianum , we here designate a lectotype and a paralectotype (see name-bearing type). Selenka (1867) examined material from ZMG and MCZ and indicated that all the material was coming from Hawaiian Islands (as Sandwich Inseln). However, on the original label of the two syntypes from MCZ, the locality mentioned is ‘Society Islands’. With the designation of a lectotype among the syntypes from MCZ, the type locality thus can no longer be the Hawaiian Islands but becomes the Society Islands.

Material from Maldives (figure 10C) and the Philippines (figure 10D–H) shows few variations from the type material. A specimen from China (ZMH E 2933) has some tables of the ventral body wall with table crown much larger than table disc. However, unlike L. pseudosemperianum , the spines of the crown are only occasionally divided distally. Moreover, tables reduced to the disc (with spiny edge), coming from the apex of ventral tube feet, have fewer but larger spines than those from ventral tube feet of the holotype of L. spineum .

In terms of ossicle assemblage, the most constant features are: (1) presence of buttons and rods dorsally but not ventrally, (2) rim of table disc spiny and (3) diameter of table crown equal to or slightly larger than diameter of table disc. These characters allow separation of L. semperianum from the two closely allied new species that are here described: L. quadripartitum and L. pseudosemperianum .

After re-evaluation of the original description, Holothuria proceraspina Cherbonnier, 1967 is here recognized as a junior synonym of Labidodemas semperianum . Indeed, the body morphology of H. proceraspina as described by Cherbonnier (1967) —‘Il est entièrement blanc jaunâtre, sauf la partie orale qui est brune tout autour de la bouche. Le tégument est peu épais, lisse, plisse´. Les pieds ventraux sont peu nombreux et dispersés sur les radius et les interradius, à l’exception de la région anale où ils s’alignent sur deux rangs sur le radius médian et sur un rang sur les radius latéraux’ [sic]—the structure of the calcareous ring ( Cherbonnier, 1967: 62, figure 3m) and the ossicle assemblage ( Cherbonnier, 1967: 62, figure 3a–l, o) are typical of Labidodemas . Cherbonnier (1967) implicitly came to the same conclusion as in his remarks he states that the form of the tables are reminiscent of the majority of species under Halodeima and of Holothuria pertinax Ludwig, 1875 (now L. pertinax ). It should, however, be noted that the structure of the calcareous ring of H. proceraspina —‘Couronne calcaire petite mais bien calcifiée, à larges et hautes radiales, à courtes interradiales triangulaires’ [sic.]— conflicts with that of Halodeima (now a subgenus of Holothuria ) (see Rowe, 1969: 137, figure 7a), but Cherbonnier (1967) was correct to recognize that L. pertinax is very close to H. proceraspina . However, L. pertinax differs from H. proceraspina in lacking buttons in the body wall. In fact, four species currently recognized in Labidodemas possess buttons in the body wall: L. semperianum , L. pseudosemperianum , L spineum sp. nov. (for description see below) and L. rugosum ; the ossicle assemblage of the first of these is identical to that of H. proceraspina , hence the decision for synonymy. Re-examination of Labidodemas sp. collected by Price ( Price and Reid, 1985) in Indonesia reveals that this specimen almost certainly is also L. semperianum .

Re-examination of the type material of L. selenkianum Semper, 1868 shows that the ossicles are partly eroded by the preserving fluid. This could explain the reduced table crown and the eroded rim of the table discs. As the general morphological aspect and the ossicle assemblage of the holotype are very close to L. semperianum as the species is here defined, it is tempting to accept the decision of Sluiter (1901) and many authors after him (a.o. Cherbonnier, 1970; Rowe and Gates, 1995), to regard L. selenkianum as a mere synonym of L. semperianum . However, we feel reluctant to base the final judgement on L. selenkianum with only a single specimen (with eroded ossicles) at hand. As such, our list of synonyms of L. semperianum marks L. selenkianum with a question mark. The here, for the very first time, depicted (figure 11) ossicle assemblage of the holotype will, once more material is available, allow definite rejection or acceptance of this species.

Labidodemas spineum sp. nov.

(figures 12A–N, 13A–G; map 4)

Name-bearing type. Holotype NHM 1974.12 .3.42.43 (L~ 125 mm); paratype NHM 1974.12 .3.42.43 (L~ 112 mm).

Type locality. Low Island, Great Barrier Reef, Australia.

Material examined. Australia ( Low Island , Great Barrier Reef), 1973, sand flat ( LWM), coll. P. Gibbs, NHM 1974.12 .3.42.43 under the name L. semperianum (holotype and paratype) .

Diagnosis. Medium-sized species; 20 short tentacles. Ribbon-like calcareous ring. Tables, buttons and rods present in body wall and tube feet. Buttons and rods spiny. Tables with quadrangular or triangular disc, with low spire without cross beam, crown irregular.

Description. The holotype is 125X 11–14 mm and the paratype 112X 8–11 mm. Body cylindrical, worm-like, tapering anteriorly. Colour in alcohol white-beige with both extremities brown; tube feet same colour as body wall. Mouth and anus terminal. Mouth surrounded by 20 short tentacles; anus wide, surrounded by five groups of paired papillae. Ventrally, tube feet restricted to ambulacra; lateral ambulacra with one row of tube feet in a zigzag pattern, median ambulacrum with two rows of tube feet. Dorsally, tube feet present in ambulacral and interambulacral areas, small, arranged in about five to six rows.

Calcareous ring ribbon-like (figure 12A) with large quadrangular radial plates and narrow interradial plates with short anterior projection. Radial plate with small anterior notch and indentation for insertion of longitudinal muscle. Two Polian vesicles, the larger one-seventh of body length. Single stone canal. Tentacle ampullae very short (1 mm long); tube feet ampullae visible on inner side of body wall. Specimens partly eviscerated (gonad, part of intestine and left respiratory tree missing). Presence/absence of Cuvierian tubules could not be ascertained because specimens are partly eviscerated. Segment of digestive tract still present, filled with rough coral sand.

Ossicles. Both dorsal and ventral body wall with tables, rods and buttons. Dorsally, tables irregular with a spiny quadrangular disc (figure 12B) (very often triangular in the paratype; figure 12E), 50–80 µ m across, perforated by four large central holes and 4–10 peripheral ones; four short pillars without cross beam, ending in a crown of spines (figure 12B, E), often irregular (figure 12B). Spire low (figure 12E). Tables of ventral body wall similar to dorsal tables (figure 12G, J) in size and shape, but sometimes reduced to disc only (figure 12G). Buttons spiny (figure 12C, H, K), 35–50 µ m long, with two to four pairs of holes; rods short, 30–35 µ m long, often spiny (figure 12D, F, K), either straight or C-shaped. Some ossicles intermediate between rods and buttons (figure 12H, K). Tube feet with ossicles similar to those of body wall. Tables 45–85 µ m across (figures 12L, N, 13A, D), often reduced to disc only (figure 13A). Buttons 45–55 µ m long (figure 13B, E), rare or absent in dorsal tube feet. Rods spiny, 30–60 µ m long (figures 12M, 13C, F), sometimes branching at extremities (figure 13F). Some ossicles (pseudo-buttons) with intermediate stages between buttons and rods (figure 13C). End plate of dorsal tube feet 125 µ m across. In tentacles small rods, 10–50 µ m long (figure 13G).

Etymology. The name spineum, Latin , means spiny and refers to the numerous spines covering the buttons and the rods from the body wall and the tube feet.

Ecology. No data currently available.

Geographical distribution (see map 4). Only known from the type locality.

Comments. Rods and buttons are similar in holotype and paratype but the tables are quite different. In the holotype, seen from above, they are rugosum - like whereas in the paratype they are pertinax -like. The tables of L. spineum differ from those of L. rugosum by the very low spire without cross beam and from those of L. pertinax by a more irregular crown of spines and the triangular shape of some discs. Labidodemas spineum is very easy to separate from all the other Labidodemas spp. because it is the only species with spiny buttons and rods in the body wall.