Partial redescriptions of three holothurians with “ hook papillae ” (Apodida Chiridotidae): Taeniogyrus japonicus (Marenzeller, 1882), T. dendyi (Mortensen 1925), Scoliorhapis theelii (Heding, 1928) Author Yamana, Yusuke 0000-0002-8764-5850 Wakayama Prefectural Museum of Natural History, Funoo 370 - 1, Kainan, Wakayama 642 - 0001, Japan. yamanayusuke 39 @ gmail. com; https: // orcid. org / 0000 - 0002 - 8764 - 5850 & Laboratorio de Sistemática y Ecología de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM)., Circuito Ext. s / n, Ciudad Universitaria, Mexico City, CP. 04510, México. yamanayusuke39@gmail.com Author Yamamoto, Masaki Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644 - 0023, Japan. & Present address: Graduate School of Science, The University of Tokyo, 7 - 3 - 1 Hongo, Bunkyo-ku, Tokyo 113 - 0033, Japan. m-yamamoto @ g. ecc. u-tokyo. ac. jp Author Ota, Yuzo San'in Kaigan Geopark Museum of the Earth and Sea, 1794 - 4 Makidani, Iwami, Tottori 681 - 0001, Japan. Author Kohtsuka, Hisanori Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238 - 0225, Japan. Author Omori, Akihito Marine Biological Station, Sado Island Center for Ecological Sustainability, Niigata University, 87 Tassha, Sado, Niigata 952 - 2135, Japan. Author Iwasaki, Kazuma Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644 - 0023, Japan. Author Setiamarga, Davin H. E. 0000-0002-3854-4893 Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644 - 0023, Japan. & The University Museum, The University of Tokyo, 7 - 3 - 1 Hongo, Bunkyo-ku, Tokyo 113 - 0033, Japan. davin @ wakayama. kosen-ac. jp; https: // orcid. org / 0000 - 0002 - 3854 - 4893 davin@wakayama.kosen-ac.jp text Zootaxa 2022 2022-05-19 5138 4 351 387 journal article 55447 10.11646/zootaxa.5138.4.1 653f12df-811e-4693-ac19-50f7b109d51a 1175-5326 6571612 409D80E7-AAEA-4636-8798-0DB7A56BCC5E Scoliodota japonica ( Marenzeller, 1882 ) [Japanese name: Ibo-kagi-namako (Iwami and other Japanese form); and Sado-nadeshiko-namako (Sado form)] ( Figs 2–10 ) Chirodota japonica Marenzeller, 1882: 123–124 ; Lampert 1885: 236 ; Théel 1886: 17 , 33, pl. II, fig. 3. Chirodota japonica von Marenzeller, 1882 : Ludwig 1889 -1892 (1891): 358, pl. I, fig. 6. Toxodora japonica ( Marenzeller, 1882 ) : Östergren 1898: 118 . Scoliodota japonica ( Marenzeller, 1882 ) : Ohshima 1913: 259–261 , pl. 6. figs. 1–3, textfig. A–D; Ohshima 1914: 479–480 . Trochodota japonica ( Marenzeller, 1882 ) : Ohshima 1919: 149 ; Clark 1921: 166 ; Utinomi 1956: 122 , pl. 61. fig. 13; Utinomi 1965: 99 , Textfig. 321; Imaoka 1995: 570 . Imaoka 2010: 55–56 . Taeniogyrus japonicus ( Marenzeller, 1882 ) : O'Loughlin and VandenSpiegel 2010: 84 ; Ota et al. 2021: 143 , fig. 9. Table 6 . Scoliorhapis dianthus Solis-Marin, Komatsu, Soliman, Uchida, Shimotani & Nozaki, 2014: 323–327 , figs 1–3. Non: Chirodota japonica Marenzeller, 1882 : Théel 1886: 17 , 33, pl. 2. fig. 3. = Scoliorhapis theelii Heding, 1928: 319–322 , fig. 69. Non: Scoliodota japonica ( Marenzeller, 1882 ) : Clark 1908: 125 , pl. 7. fig. 5. = Scoliorhapis theelii Heding, 1928: 319–322 , fig. 69. FIG. 2. A–E, lateral views of the Iwami form specimens of Scoliodota japonica ( Marenzeller, 1882 ) . Anaesthetized (A) and preserved (B) states of WMNH-INV-2017-169; preserved states of WMNH-INV-2017-170 (C), WMNH-INV-2017-171 (D), and WMNH-INV-2017-172 (E); anterior left, dorsal upper. Retractor organ of WMNH-INV-2017-170 (F). Tentacles from oral side (G), stone canal from right side (H), and ciliated funnels in left dorsolateral inter-radius (I) of WMNH-INV-2017-169; dorsal upper. Abbreviations: ad, anterior dorsal; av, anterior ventral; ca, calcareous ring; dd, distal digits; ma, madreporite; pd, posterior dorsal; pv, posterior ventral; RI , medioventral calcareous ring; ro, retractor organ; rte, removed tentacle; st, stone canal; te, tentacles. FIG. 3. A–D, microphotograph of preserved skin of the anterior dorsal side Iwami form specimens of adult (A, B) and young (C, D) Scoliodota japonica (Marenzeller) . Containing ossicles in skin of WMNH-INV-2017-169 (A); WMNH-INV-2017-170 (B); WMNH-INV-2017-171 (C); and WMNH-INV-2017-172 (D). Abbreviations: sh, sigmoid-hook ossicle; wh, wheel ossicle. Specimens examined. 4 specimens of Iwami form : WMNH-INV-2017-169 (length 149 mm , width 3.5–7 mm ), from 16 m deep of west side the Haneo Point ( 35°36′16.6″N , 134°20′20.0″E ) on Sept. 13, 2017 ; WMNH-INV- 2017-170 (divided into three parts, length 28+30+ 28 mm , width 3.5–6.5 mm ) from 3 m deep of inside the Tajiri Port ( 35°35′36.8″N , 134°19′03.6″E ) on Sept. 15, 2017 ; WMNH-INV-2017-171 (length 46 mm , width 2.5–3 mm ), and -172 (length 26 mm , width 2.5–5 mm ), from 16 m deep of outside the Tajiri Port ( 35°35′48.9″N , 134°19′01.0″E ), on Sept. 15, 2017 . 13 specimens of Sado form : WMNH-INV-2020-27 (181003b8) (length 104 mm , width 3.7– 5.1 mm ), from 2.0 m deep of Mushizaki ( 38°14'56.0"N 138°30'21.5"E ) on Oct. 3, 2018 ; WMNH-INV-2020-28 (180808) (length 12+? mm, width 2.8 mm , autotomied anterior part only), from 1.0 m deep of Sawane ( 38°00'03.0"N 138°16'26.0"E ) on Aug. 8, 2018 ; WMNH-INV-2018-78–80 (length 18–29 mm , width 2.0– 2.9 mm ), from 1.0 m deep of Sawane on May. 22, 2018 ; WMNH-INV-2019-319 (length 145 mm , width 3.6–6.3 mm ) and WMNH-INV- 2019-324 (length 36 mm , width 3.0– 3.2 mm ) from 2.0 m deep of Mushizaki on Oct. 3, 2018 ; WMNH-INV-2020- 22–26 (length 23–38 mm , width 1.3–2.6 mm ), from 1.0 m deep of Sawane on Oct. 26, 2018 . TABLE 3. Counts and measurements of Scoliodota japonica (Marenzeller) , S. dendyi (Mortensen) comb. nov. , and S. theelii Heding
Registrationa, b, c Locality Type status Gonad state Body size (mm) Length Width Tentacles Counts Tentacle Stone digits canal Polian vesicles
Scoliodota japonica (Marenzeller)
MNW-1192 Eno-sima, Japan Syntype undetected 12+? 2.5 Not measured
INV-2017-169 Haneo, Iwami, Tottori, Japan Non-type ovary 149 3.5–7 10 15–17 1 1
INV-2017-170 Tajiri, Iwami, Tottori, Japan Non-type testis 28+30+28 3.5–6.5 10 17–19 1 1
INV-2017-171 Tajiri, Iwami, Tottori, Japan Non-type immature 46 2.5–3 10 12–14 1 1
INV-2017-172 Tajiri, Iwami, Tottori, Japan Non-type immature 26 2.5–5 10 13–16 1 1
INV-2018-78 Sawane, Sado, Niigata, Japan Non-type ovary 29 2.6 10 12–13 1 1
INV-2018-79 Sawane, Sado, Niigata, Japan Non-type ovary 18 2.9 10 11–12 1 1
INV-2018-80 Sawane, Sado, Niigata, Japan Non-type ovary 20 2.0 10 10–14 1 1
INV-2019-319 Mushizaki, Sado, Niigata, Japan Non-type testis 145 3.6–6.3 10 15–17 1 1
INV-2019-320 Mushizaki, Sado, Niigata, Japan Non-type testis 117 2.4–3.2 10 15–18 1 1
INV-2019-324 Mushizaki, Sado, Niigata, Japan Non-type testis 36 3.0–3.2 10 18–20 1 1
INV-2020-22 Sawane, Sado, Niigata, Japan Non-type ovary 32 1.6–1.8 10 10–13 1 1
INV-2020-23 Sawane, Sado, Niigata, Japan Non-type immature 23 1.4–1.7 10 12–14 1 1
INV-2020-24 Sawane, Sado, Niigata, Japan Non-type immature 38 1.4–2.5 10 10–12 1 1
INV-2020-25 Sawane, Sado, Niigata, Japan Non-type immature 35 1.3–2.6 10 10–12 1 1
INV-2020-26 Sawane, Sado, Niigata, Japan Non-type immature 23 1.8–2.1 10 10–12 1 1
INV-2020-27 (181003b8) Mushizaki, Sado, Niigata, Japan Non-type ovary 104 3.7–5.1 10 12–16 1 1
INV-2020-28 (180808) Sawane, Sado, Niigata, Japan Non-type testis 12+? 2.8 10 15–18 1 1
S. dendyi (Mortensen)
Smallest specimen of ZMUC- HOL-57 Plimmerton, New Zealand Syntype immature 73 2–3 10 8–12 1 1
Largest specimen of ZMUC- HOL-58 Auckland Harbour, New Zealand Syntype ovary 133 5–9 10 10–12 1 1
S. theelii Heding
“♂” specimen of ZMUC- HOL-220 Port Jackson, Australia Syntype testis 45+? 3–7 10 9–12 removed 1
“♀” specimen of ZMUC- HOL-220 Port Jackson, Australia Syntype ovary 32+? 4–8 10 10–14 removed 1
a (MNW) Naturhistorisches Museum Wien, Austria (also reported as 11592) b (INV) Invertebrates collection of Wakayama Prefectural Museum of Natural History (WMNH-INV), Wakayama, Japan c (ZMUC) Zoological Museum of University of Copenhagen, Denmark TABLE 4. Ossicles length (Mean ± sd μm) measured from four Iwami form specimens and five Sado form specimens of Scoliodota japonica (Marenzeller) measured from glass slides
Body part
WMNH No. (Locality) Ossicle type Anterior ventral Posterior ventral Anterior dorsal Posterior dorsal Tentacle
n Length Range n Length Range n Length Range n Length Range n Length Range
INV-2017- 169 (Iwami) Wheel Hook 0 61 - 85±9 - 65–102 0 42 - 96±10 - 72–114 0 65 - 81±7 - 64–95 0 39 - 93±8 - 79–106 0 0 - - - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
INV-2017- 170 (Iwami) Wheel Hook 0 67 - 87±6 - 72–98 0 39 - 100±8 - 84–113 0 62 - 86±8 - 61–103 0 43 - 101±8 - 68–117 0 0 - - - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
INV-2017- 171 (Iwami) Wheel Hook Rod 0 44 0 - 77±12 - - 41–92 - 0 8 0 - 77±11 - - 53–87 - 1 47 0 59 77±8 - 59 61–91 - 0 16 0 - 80±6 - 67–88 - 0 0 0 - - - - - -
INV-2017- 172 (Iwami) Wheel Hook 3 37 53±6 75±7 46–56 59–90 0 32 - 91±6 - 77–99 2 52 54 76±7 51–57 58–88 0 28 - 89±9 - 54–102 0 0 - - - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
INV-2019- 324 (Sado) Wheel Hook 0 22 - 86±6 - 74–96 0 18 - 93±4 - 87–101 0 17 - 86±6 - 71–99 0 12 - 99±5 - 93–107 0 0 - - - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
Wheel 0 - - 0 - - 3 59±5 53–63 0 - - 0 - -
INV-2020-22 (Sado) Hook 25 68±5 59–77 8 63±8 47–71 14 66±5 54–74 6 64±10 51–76 0 - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
Wheel 0 - - 0 - - 1 59 59 0 - - 0 - -
INV-2020-23 (Sado) Hook 22 66±5 62–69 6 67±2 62–69 27 64±5 55–75 5 68±3 63–71 0 - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
......Continued on the next page TABLE 4. (Continued)
Body part
WMNH No. (Locality) Ossicle type Anterior ventral Posterior ventral Anterior dorsal Posterior dorsal Tentacle
n Length Range n Length Range n Length Range n Length Range n Length Range
INV-2020-24 (Sado) Wheel 0 - - 0 - - 0 - - 0 - - 0 - -
Hook 27 65±7 45–78 8 63±2 61–67 19 70±3.6 61–77 7 59±6.5 53–67 0 - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
Wheel 0 - - 0 - - 0 - - 0 - - 0 - -
INV-2020-25 (Sado) Hook 22 86±6 74–96 18 93±4 87–101 17 86±6 71–99 12 99±5 93–107 0 - -
Rod 0 - - 0 - - 0 - - 0 - - 0 - -
Description. In the Iwami form, living body color deep red, with tentacles white, and color gradually fades during preservation ( Fig. 2A–E ). Living body color of small specimens paler than that of large specimens. Mouth and anus terminal. Numerous “hook papillae” present in inter-radius of both dorsal and ventral body skin, through anterior to posterior, low hemisphere form (preserved and living specimens). Color of papillae surfaces (preserved and living specimens) deeper than adjacent body skin. Wheel-papillae absent. Body color of living state white semitransparent to whitish pink in Sado form, with numerous pale-red minute spots with tentacles white ( Fig. 7 ). Ten tentacles, stout, with about 10–20 digits ( Fig. 2G , 7 , Table 3 ); distal digit pair largest. Sensory cups absent. Large retractor muscles or ligaments combined calcareous ring with longitudinal muscles ( Fig.2F ). Calcareous ring inclined toward ventral side, composed of five radial and five inter-radial plates ( Fig. 4A ), these all thick, with complicated three-dimensional structure ( Fig. 5 ). All plates have a posterior depression, which shaped approximately rectangular in ventral side and triangular in dorsal side. Trapezoid anterior projection with central notch in RI , and low triangle anterior projection in IR5 , no perforation present. Other eight plates have an anterior projection on near dorsal end. Polian vesicle single, in RI . Stone canal single, very long and sometimes coiled, with wide madreporite, in IR5 ( Fig. 2H ). Intestine has no loop, situated along IR 5 in anterior to middle body, however posterior end of intestine about a one fifth of total length adhered to body wall in four radii exclusive of RI . Reproductive tubules on both sides of anterior dorsal mesentery, in clusters, branched. One band of crowded ciliated funnels situated on left dorsolateral inter-radius IR3 , along left ventrolateral longitudinal muscle RII , along entire length of body. Additionally, one sparse row of ciliated funnels situated in the right side of dorsal mesentery IR5 present in middle part of the body. Funnels short (approximately 0.15 mm long), without stalk ( Fig. 2I ). In the Iwami form, body wall containing wheel and sigmoid-hook ossicles in two small specimens, but wheel ossicles quite sparse or lacking in two large specimens ( Figs. 3 , 6 , Table 4 ). Wheel ossicles scattered sparsely in anterior to posterior body surface on both radii and inter-radii. Wheel ossicles rounded-hexagonal with six spokes, diameter 46–59 µm. Inner margin of rim parallel to outer margin. Teeth triangular, 9–12 per section, with no discontinuities in tooth series. Spokes 18–22% as broad as diameter of wheel ossicle. Wheel ossicles scattered sparsely in anterior half, lacking in posterior half. Body wall containing sigmoid-hook ossicles in all of Sado form specimens, wheel ossicles completely lacking in adult specimens ( Figs 8 ; 9B–E , Table 4 ). Body wall also containing wheel ossicles in smallest three specimens , scattering sparsely in anterior to posterior body surface on both radii and inter-radii. Wheel ossicles rounded-hexagonal with six spokes, diameter 53–63 µm ( Figs 9F; 9G , Table 4 ). Inner margin of the rim shows slight depression at each corner, however, no discontinuities in tooth series there. Teeth triangle-shaped, 8–11 per radiant, spokes broad, their breadth amounting to 24–29% of wheel ossicle diameter. Sigmoid-hook ossicles thick and large, arranged in circles as “hook papillae,” absent along center of longitudinal muscles. Each papilla contains up to 13 hooks in anterior to middle of body, however hooks lie scattered independently from papillae in posterior body. Sigmoid-hooks without spinelets; open loop strongly wound ( Figs. 6–9 ). Length up to approximately 120 µm (in Iwami) and 110 µm (in Sado), large in large specimens, small in small specimens ( Table 4 ), and significantly larger in posterior than in anterior, in both sides in three specimens (Kruskal-Wallis test, P s <0.05) (with exception of one small specimen: WMNH-INV-2017-171) ( Table 4 ). Tentacles lack ossicles. Comparative materials. NMW-1192 of NHMW , syntype (length 12 mm , width 2.5 mm ), Naturhistorisches Museum Wien, collected by Dr. Körbl in 1875–1876, from east side of Eno-shima, Japan ( Marenzeller 1882 ). The specimen was sent to Drasch and was subsequently labelled as “Drasch 1877”. It was dissected by Marenzeller, and fastened to a glass plate. In the report of Jangoux and De Ridder (1990) , this specimen was also listed with the catalog number 11592. According to Marenzeller (1882) , the original specimen was 3.5 mm in breadth, and estimated to be more than 40 mm in length. However, the syntype is now much smaller than what was previously reported, probably because it dried up in the past. Today the syntype is hard and fragile, internal organs could not be observed, and ossicles appear to have corroded away. Observation of the specimens of Scoliorhapis dianthus . Recently, Solis-Marin et al. (2014) described Scoliorhapis dianthus from the shallow water of Sawane, Sado Island, where the Sado form of T. japonicus examined in this study were also collected. In that study, however, the presence of “hook-papilla” and wheel ossicles were not thoroughly discussed. Therefore, in this study, we conducted a detailed comparison of the body ossicles between the two Sado animals. A new and more detailed photograph of the body ossicles of the originally preserved paratype ( Solis-Marin et al. 2014 ) is shown in Figure 10 . FIG. 4. A–E, SEM images of ossicles and parts of the calcareous ring of the Iwami form specimen of adult Scoliodota japonica (Marenzeller) . WMNH-INV-2017-169, outer surface calcareous ring of right side, dorsal upper (A); ossicles of anterior ventral body wall (B); posterior ventral body wall (C); anterior dorsal body wall (D); and posterior dorsal body wall (E). Abbreviations: an, anterior notch; ap, anterior projection; pd, posterior depression. FIG. 5. A, B, calcareous ring of right side of the Iwami form specimen WMNH-INV-2017-169 of Scoliodota japonica (Marenzeller) . Viewed from anterior side (A); and viewed from posterior side (B). The result of the morphological observation of the paratype specimen of Scoliorhapis dianthus ( sensu Solis- Marin et al ., 2014) is as follows: Body color of preservation material is whitish pink, no “hook papillae” present. The density of the sigmoid-hooks in the skin are uneven, and there was no wheel ossicle present ( Fig. 10 ). However, the lengths of sigmoid-hook ossicles are 100–120 µm (in Solis-Marin et al . 2014 ), or 85–115 µm ( Fig. 10 ), which are close to those in Iwami form (53–117µm) and Sado form (45–107µm) of S. japonica ( Table 4 ). Scoliorhapis dianthus also has retractor organ ( Solis-Marin et al. 2014 ). Because there was no other taeniogyriid species collected from Sawane during our very frequent surveys (more than 10 times), we consider S. dianthus as a malformation or seriously damaged specimens of S. japonica . Remarks. Although the color of animals from Sado differ from the original description and from the Iwami form specimens, other morphological features of their internal organs and ossicles in agreement, including the presence of “hook papillae”, of wheel ossicles in juveniles, and lack tentacle ossicles ( Ohshima 1913 ; 1914 ). Our present observation confirms the morphological characters for ossicles and external body features provided by Marenzeller (1882) and Ohshima (1913 , 1914 ), with an exception of the presence of retractor organ. However, our detailed analyses elucidate the arrangements of the ciliated funnels, the general appearance of the complete body, and shape of the calcareous ring, for which sufficient information was not previously available. In the present materials, the tentacles of specimens fixed without anesthesia were retracted ( Fig. 2C, E ). Therefore, we inferred that this species had retractable tentacles. This detailed, novel information could be useful for the identification of this species, including for future studies aiming at the revision of genus Taeniogyrus . Distribution. This species has only been recorded in Japan from sandy sediment in middle Japan ( Marenzeller 1882 ; Ohshima 1913 , 1914 ); subtidal zone of 3–4 m deep in sandy sediment, Seto Inland Sea in western Japan ( Imaoka 2010 ); west coast of Kyushu Island, Japan ( Murakami 1905 ; Ohshima 1919 ; Utinomi 1956 , 1965 ); and shallow waters of the Sea of Japan in western and northern Japan (present study).