Taeniogyrus rubrus Yamana, Hirabayashi, Hirai, Dan, and Ogawa, 2022

Yamana, Yusuke, Tanaka, Hayato, Hirabayashi, Isao, Dan, Ichinosuke, Hirai, Atsushi & Ogawa, Akito, 2022, Three New Infaunal Species of Taeniogyrus (Echinodermata: Holothuroidea: Apodida: Chiridotidae: Taeniogyrinae) from Southern Coast of Wakayama, Japan, Species Diversity 27 (1), pp. 139-158 : 152-155

Taeniogyrus rubrus Yamana, Hirabayashi, Hirai, Dan, and Ogawa , sp. nov.

[New Japanese name: Yesuzaki-kuruma-kagi-namako] ( Figs 3C , 7 , 8 ; Tables 6, 7)

Material examined. Holotype: WMNH-INV-2019-299 (length 34.2 mm, width 3.5 mm, collected from Kushimoto on 15 June 2019; INSD accession number LC655785 , 615 bps) . Paratypes: 7 specimens, WMNH-INV-2020-29 (length 23.7 mm, width 2.2 mm, collected from Susami on 4 August 2020; LC655786 , 622 bps), WMNH-INV-2020-33 (length 33.2 mm, width 3.1 mm, collected from Kushimoto on 1 November 2020), WMNH-INV-2021-49 (length 19.7 mm, width 2.0 mm, collected from Kushimoto on 6 August 2021), WMNH-INV-2021-50 (length 30.4 mm, width 2.7 mm, collected from Kushimoto on 6 August 2021), WMNH-INV-2021-51 (length 24.5 mm, width 2.3 mm, collected from Kushimoto on 6 August 2021), WMNH- INV-2021-52 (length 37.1 mm, width 2.2 mm, collected from Kushimoto on 6 August 2021), WMNH-INV-2021-53 (length 28.5 mm, width 2.6 mm, collected from Kushimoto on 6 August 2021).

Diagnosis. Body color red or reddish brown with dark yellowish spots of wheel-papillae along three dorsal interradii. Tentacles ten, with 4–6 digit pairs. With up to 3 Polian vesicles in RI. A band of ciliated funnels situated along with inter-radius near right side midventral longitudinal muscle RI, and a sparse row of ciliated funnels situated along with left side of left ventral longitudinal muscle RII. Funnels strongly curved, like French horn, and with wide opening. Sigmoid-hook ossicles large (all exceed 100 µm in adult animals), without minute spinelet or gap.

Holotype description. Medium-sized body, anesthetized length of holotype specimen (WMNH-INV-2019-299) 34.2 mm (after preservation); cylindrical, straight, or weakly bent downward; slightly tapered toward posterior end ( Table 6). Body color (living and preserved specimens) red or reddish brown. Dark yellowish spots of wheel-papillae locally observed on dorsal inter-radii skin. Mouth anterior; anus posterior; oral disk inclined toward ventral side.

Tentacles ten, non-retractile, with 4–6 pairs digits; sensory cups absent ( Fig. 7C ; Table 6). Tentacles color translucent red in living, pink to whitish in preserving.

Polian vesicles in RI, branched in basal part. In the holotype with 2 Polian vesicles (2.7 mm and 0.9 mm in length) ( Table 6), vesicles shaped globular. Stone canal single, short (0.25 mm long), with a coffee bean-like madreporite (0.15 mm diameter) just behind of IR5 calcareous plate ( Fig. 7I ). Ciliated funnels (1 band) in inter-radius near right side medioventral longitudinal muscle RI ( Fig. 7D ; Table 6); 1 sparse row of ciliated funnels situated along with left side of left ventral longitudinal muscle RII ( Fig. 7D ). Funnels short (0.15 mm), weakly curved (<about 90°), with narrow opening (0.05 mm wide), with very short stalk, and slit with granular layer along proximal side to the funnel base ( Fig. 3C ). Intestine situated along IR5 through anterior to middle body, over left dorsal longitudinal muscle RIV in middle body, straight in IR3 along under side of RIV, no refraction until end of body, turning to anterior side about 1/5 of posterior body, then returning straight to the end in IR3 along upper side of RII. Ovaries or testis in two tubules in middle body, tubules branched in basal part, two tubules present on both sides.

Calcareous ring with 5 thick radial, 5 thick inter-radial plates; distally flattened ends ( Fig. 8A ); except IR5 all with shallow posterior depression and anterior projection, IR1 and IR2 with a blunt projection. IR3 and IR4 with a sharp projection, and low trapezoid anterior projection with slight central notch in RI, and low triangle anterior projection in IR5 ( Fig. 8E, F ).

Body-wall thick (more than 1.5 mm in thickness), containing wheel and sigmoid-hook ossicles ( Fig. 8A–D ; Table 7). Wheel ossicles in dorsal skin present in wheel-papillae, only lined in 3 dorsal inter-radial body walls, range from tentacle base to posterior end ( Fig. 7 ; Table 7). Wheel ossicles small, diameter less than 100 µm (mean 52–68 µm) ( Table 4). Wheel ossicles larger in posterior body than anterior body ( Table 4). Wheel ossicles rounded-hexagonal, 6 thick spokes; narrow rim, inner rim margin approximately parallel to outer margin. Teeth sharp and massive (5 µm in hight in a wheel of 45 µm diameter), 7–15 per inter-spoke area ( Table 7). Spokes widen, widest prior to rim, breadth 17–27% of wheel ossicle diameters ( Fig. 8C ; Table 7). Wheel ossicles small, means 56 µm and 60 µm in anterior and posterior dorsal, respectively ( Table 7).

Sigmoid-hook ossicles in body wall scattered in interradii from anterior to posterior; both sides of longitudinal muscles, pointed end toward inter-radius, open-loop end toward longitudinal muscles ( Fig. 7E ), except tentacles and oral disk. Sigmoid-hook ossicles large, all the hooks exceed 130 µm ( Fig. 8D ; Table 7); thickened, smooth; shank breadths exceed 10–20 µm ( Table 7), pointed end sharpened, no minute tooth or gap on surface ( Fig. 8D ).

Tentacles contain rod ossicles ( Fig. 8B ; Table 7); mostly bifurcate distally, first branches usually 4 or 5, second and third branches developed; distal ends spinous. Rod ossicle length 45–69 µm, rod breadth 3–10 µm in stem central.

Variation including paratypes. Largest paratype specimen (WMNH-INV-2021-52) length 37.1 mm (after preservation) ( Table 6). Body color (living and preserved specimens) red or reddish brown with dark yellowish spots of wheel-papillae locally observed on dorsal inter-radii skin ( Fig. 7A, B ). In the holotype with 2 Polian vesicles, but 1–3 Polian vesicles in seven paratypes ( Table 6) . In individuals with single Polian vesicle, vesicle shaped fusiform (width about 1/4 of length), and in types with 2 or 3 Polian vesicles, vesicles shaped globular. Wheel teeth, 7–18 per radiant (individual means 9–14 in measured three type specimens). Spoke breadth 21–23% of wheel ossicle diameters ( Fig. 8C ; Table 7). Wheel ossicles are small and all the diameter less than 100 µm (individual means 52–68 µm in measured three type specimens) ( Table 7). Wheel ossicles larger in posterior body than anterior body, and significantly different (Kruskal– Wallis test, P <0.05) in one of large specimens (WMNH-INV-2020-33) ( Table 7). However, diameters in anterior and posterior parts are not significantly different in holotype ( Kruskal – Wallis test, P>0.05) . Wheel-papillae easily discharged to outside by stimulus and become hemispherical sucks ( Fig. 7F, G ). Sigmoid-hook large, all the hooks exceed 100 µm (individual means 132–148 µm in measured three type specimens) in the present type series ( Fig. 8D ; Table 7). Sigmoid-hook length significantly different among all measured specimens in anterior ventral, anterior dorsal, and posterior ventral body parts (Kruskal– Wallis test, P s<0.05), not significantly different in posterior dorsal part or between anterior and posterior parts in all measured specimens (Kruskal– Wallis test, P s>0.05). Tentacle rod 56–101 µm in length (means 59–78 µm in different specimens); rod breadth 3–10µm in stem central; ossicle length independent of body size ( Tables 6, 7).

Remarks. As noted above, Taeniogyrus species with wheel-papillae, presently seven Taeniogyrus species and one new species T. flavus which described above, have been reported ( Table 5). Among these congeners, T. yvonnae possess the arrangement of two rows of ciliated funnels which agrees with that of T. rubrus sp. nov. However, T. yvonnae also possess huge hook ossicles mostly exceed 300 µm ( Table 5). Thus, T. flavus sp. nov. is distinguishable from these congeners and described above by the arrangement of two rows of ciliated funnels and its body color ( Table 5). Additionally, T. rubrus sp. nov. has shown a habit of discharging wheel-papillae, which have been reported in partial congeners of Chiridotidae ( Kubota and Inada 2003; Yamana and Tanaka 2017b); but, the adaptive significance of this habit has not been revealed to date. One paratype of this species was found by one of the present authors (Ichinosuke Dan), of the 6th grade student at Kobe-Shimohatadai Elementary School (as at August 2020), during the nature observation meeting held by WMNH and Susami Crustacean Aquarium. At first, it was misidentified as Chiridota rigida Semper, 1867 , which was recently reported from the same site of the Cape Yesu-zaki as new to Japan ( Yamana and Tanaka 2017b) After that, it was also turned out that the holotype specimen had been misidentified as C. rigida too. Although there is a striking resemblance in their external appearances, the anatomical characteristics are obviously different between C. rigida and T. rubrus sp. nov.: the ciliated funnels are situated along the mid-dorsal and left lateral mesentery in C. rigida , moreover C. rigida has 12 tentacles (see Yamana and Tanaka 2017b).

Distribution. Known only from two type localities, in the sandy-gravel sediment at Cape Yesu-zaki (lower intertidal zone) and Kushimoto (5–13 m deep) (where, the specimen numbers were larger than that of Yesu-zaki, but this was not reflected the actual circumstances because of a new law named “Revised Fisheries Act” was enforced from 1 December 2020, which made all the holothurians in Japanese waters must not be able to catch, with an exception of the area Kushimoto, where we applied for a license), Wakayama, southern end of the mainland of Japan.

Etymology. The specific name is derived from the Latin adjective rubrus (meaning red), based on its body color.

DNA barcode sequences. Two specimens of sequence of the mitochondrial CO1 gene, 615 bps and 622 bps were obtained from the holotype (WMNH-INV-2019-299: INSD accession number LC655785 , base frequency A=21.0%, C=13.8%, G=20.3%, T=44.9%) and a paratype specimen (WMNH-INV-2020-29: LC655786 , base frequency A= 21.1%, C=13.7%, G=20.6%, T=44.7%), respectively. In BLAST searches, the closest hits to the partial CO1 sequence are from Chiridota albatrossii Edwards, 1907 ( KX874398 and KX874397 , with 84.9–85.1% similarity in 98–100% coverage) and Taeniogyrus verruculosus ( LC203483 , with 84.1– 84.33% similarity in 99 or 100% coverage). The results of BLAST searches shows that there is a great genetic diversity in present genus. It is suggested that the genus Taeniogyrus containing large diversity both genetically and morphologically, requires for comprehensive taxonomic revision involving the other apodid holothurians in the future.

Figures

Fig. 3. SEM images of ciliated funnels of holotypes of three new Taeniogyrus species. A, T. albulus sp. nov. (WMNH-INV- 2017-100); B, T. flavus sp. nov. (WMNH-INV-2016-135); C, T. rubrus sp. nov. (WMNH-INV-2019-299).

Fig. 7. External and internal morphologies of Taeniogyrus rubrus sp. nov. A–E: paratype (WMNH-INV-2020-33); F–I: paratype (WMNH- INV-2021-50). A, B, Dorsal views of preserved state with anaesthetization and active state without anaesthetization, respectively; C–E, microphotographs of tentacles of left side (viewed from oral disc) (C), ciliated funnels situated along with lm RII (D) (anterior left), and anterior dorsal skin containing ossicles (E); F–I, microphotographs of discharging phase of wheel-papillae (F), discharged wheel-papillae (G), ciliated funnels (H), right internal view of preserved states (I) (anterior right). Abbreviations: ad, anterior dorsal; av, anterior ventral; CR: calcareous ring; fun: ciliated funnels; lm: longitudinal muscle; M: madreporite; pd, posterior dorsal; POL: Polian vesicle; pv, posterior ventral; SC: stone canal; sh, sigmoid-hook ossicle; te, tentacle.

Fig. 8. SEM image of calcareous ring parts and body ossicles of Taeniogyrus rubrus sp. nov. A–D: holotype (WMNH-INV-2019-299); E, F: paratype (WMNH-INV-2021-50). A, Right parts of calcareous ring (viewed from right side, dorsal upper); B–D, rod ossicles from a lateral tentacle (B), wheel ossicles from a wheel papilla of anterior dorsal skin (C), and sigmoid-hook ossicles from anterior dorsal skin (D); E, F, calcareous plates of medioventral RI (E) and mediodorsal IR5 (F) (anterior upper). Abbreviations: ro, rod ossicles; sh, sigmoid-hook ossicles; wh, wheel ossicles; wh', internal side of wheel ossicles.