Eudistoma okai Sanamyan, 2022

Nishikawa, Teruaki, Tanigawa, Shunta & Namikawa, Hiroshi, 2024, Taxonomy of Eudistoma okai (Urochordata: Ascidiacea) Inhabiting the Pacific Coast of Japan, with a Revised Description of Larvae, Species Diversity 29 (1), pp. 1-7 : 2-6

Eudistoma okai Sanamyan, 2022

[Japanese name: Kinoko-boya ( Oka 1927)] ( Figs 1 , 2 ; Tables 1, 2)

Distoma parvum Oka, 1927: 497 , fig. 958.

Eudistoma parvum (Oka) : Tokioka 1953: 15; Tokioka 1954a: 72–73, pl. 4, figs G–J.

Eudistoma sp. (Kinoko-boya): Nishikawa et al. 2018: 117.

Eudistoma okai Sanamyan, 2022: 279 .

Excluded records.

Eudistoma parvum (Oka) : Kott 1957a: 77, fig. 9; Nishikawa 1980: table 1; Sanamyan 1993: 167–168, fig. 3A; Nishikawa 1995: 585 (only description and photo of colonies from Sakishima Islands, the Ryukyus), pl. 139-9.

Eudistoma sp. (Kinoko-boya): Kosuge 2018: 193–198, figs 1–3, table 1.

Specimens examined. Asajiro Oka’s collection (hereinafter, Oka Collection), Zoological Institute of the Tokyo University of Education , antecedent of the University of Tsukuba (TBK-anim series), now held in the Protochordata collection, National Museum of Nature and Science, Tsukuba (NSMT-Pc series), labelled “ Distoma parva ”: NSMT-Pc 7485 (TBK-anim 18), S 452, Misaki [Sagami Bay], 5 June 1928, not part of the name-bearing type, due to the collection date being after that of the original description (Article72.4.1.1 of the Code), 9 colonies [or their fragments ( Fig. 1A ), the same hereafter), larvae in zooids; NSMT-Pc 7486 (TBK-anim 156), S289, Misaki [Sagami Bay], 17 March 1926, probably part of the type material, based on collection date, 3 colonies, no larvae; NSMT-Pc 7487 (TBK-anim 157), S272, [19]25 (further details illegible), Awa [Southern part of Boso Peninsula], probably part of the type material, based on collection date, 10 colonies, zooids much deteriorated, no larvae . Tokioka (1954a) redescribed the species as E. parvum (Oka) based on “the type specimen kept in the Zoological Institute of the Tokyo University of Education ” (ditto: 69), which indicates that he most likely examined at least the NSMT-Pc 7486 and 7487 specimens, although references to sampling and registration data were omitted. At that time, some additional material of “ Distoma parvum ” may have been available, although none was found in the 1980’s (when T. Nishikawa first examined ascidian specimens in the Zoological Institute of the University of Tsukuba ) . Accordingly, NSMT-Pc 7486 and 7487 should be regarded as at least part of the type series included in Oka’s original description of Distoma parvum , having syntype status since neither the holotype nor lectotype have been fixed (Article 73.2 of the Code ) . The aforementioned specimens are newly recognized herein as syntypes of E. okai (Article 72.7 of the Code).

New material (collected from rocky shores on Boso and Miura Peninsulas by T. Nishikawa , formalin-fixed unless indicated otherwise, and maintained in 70% ethanol): NSMT-Pc 3315, Hamaogi , Kamogawa , Chiba Prefecture, 26 May 2010, 0 m, 13 colonies; NSMT-Pc 3316, Yoshio, Kamogawa, Chiba Prefecture, 27 May 2010, tide pool, 6 colonies; NSMT-Pc 3317, ibid ., 26 July 2010, tide pool, 5 colonies; NSMT-Pc 3318, ibid ., 25 August 2010, tide pool, 10 colonies; NSMT-Pc 3319, ibid ., 23 March 2011, tide pool, 18 colonies; NSMT-Pc 3320, southern coast of Jyogashima Island , Miura, Kanagawa Prefecture, 9 April 2012, 0 m, 11 colonies; NSMT-Pc 3321, ibid ., 24 June 2013, 0 m, 10 colonies; NSMT-Pc 3322, ibid ., 8 July 2013, 0 m, 12 colonies; NSMTPc 3323, ibid ., 17 April 2014, 0 m, 9 colonies; NSMT-Pc 4598, Kohazuki, Onjyuku, Chiba Prefecture, 16 July 2012, 0 m, 2 colonies; NSMT-Pc 4611, Senjyo beach, Sugashima Island, Toba , Mie Prefecture, 2 July 1988, 0 m, 2 colonies; NSMT-Pc 5051–5053, Yoshio, Kamogawa, Chiba Prefecture, 24 March 2011, 0 m, 1 colony, 99.5% ethanol-fixed .

Description of specimens in the Oka Collection, supplementary to descriptions in Oka (1927) and Tokioka (1954a). Colonies, probably incomplete, up to 17 mm thick, each comprising a common tunic sheet bearing one or 2 mushroom-shaped cormidia; cormidium head swollen, roundish and smooth-surfaced, lacking sand grains and shell fragments; peduncle and basal sheet densely impregnated with sand grains and shell fragments, sparsely with fecal pellets; zooids deteriorated, reflecting “colonies ... contain only a small number of perfectly preserved zooids” in Tokioka (1954a: 73); thoracic musculature almost undetectable. One or two larvae found in right peribranchial sac in a few well-preserved zooids of NSNT-Pc 7485; trunk up to 670 µm long, with 3 attachment processes and 4 pairs of lateral ampullae, with a single median ampulla between the ventral-most and middle processes (thus 9 ampullae in total; Fig. 1B ), unlike the figure by Tokioka (1954a: pl. 4, fig. J) showing 4 median ampullae alternating with 3 attachment process (his text lacking the description of larval ampullae).

Description of new material. Colonies growing up to 44 mm × 25 mm across, up to 18 mm thick, each comprising a thin or moderately thick basal sheet bearing one to 20 mushroom-shaped cormidia; cormidium head swollen, roundish and smooth-surfaced, lacking sand grains and shell fragments; peduncle and basal sheet sparsely or densely impregnated with sand grains, shell fragments and fecal pellets in NSMT-Pc 3316, 4598, and 4611. Live colonies with cormidia heads white, peduncles and basal sheet greyish or brownish (due to impregnated foreign matter or fecal pellets); tunic varying from almost transparent to almost opaque whitish, zooids white ( Fig. 2A, B ); after formalin-fixation, tunic and zooids became pale orangish or pale fleshy pink in NSMT-Pc 3317, 3323, 4598, and 4611. Zooids up to 6 mm long, comprising a ca. 1 mm long thorax and the remaining abdomen, with elongated thin posterior extension(s). Branchial and atrial siphons distinct, each with a 6-lobed aperture. Up to 5 larvae almost always in right peribranchial cavity in NSMT-Pc 3315–3317, 3321, and 3322. Thoracic mantle musculature comprising ca. 15–20 longitudinal and ca. 30 (rarely up to 40) transverse bundles on each (visible under stereoscopic or optical microscope). Three stigmatal rows, each containing 18–20 elongated stigmata on each side, including 4 or 5 positioned diagonally along mid-dorsal line in anteriormost row. Tentacles ca. 16, long and short (detailed arrangement unclear); ciliated groove oval, elongated transversely. A well-developed dorsal languet somewhat displaced to left on transverse vessels between first and second, and second and third stigmatal rows. Anus bi-lobed, opening nearly at level of second transverse vessel between second and third stigmatal rows. Stomach smooth-surfaced, occupying posterior ca. one-third to onefifth of abdomen; pericardium (containing heart) at rear end of abdomen. Mature specimens with gonads comprising numerous white testicular follicles; sometimes a few pale orangish eggs along posteriormost part of intestinal loop below stomach. Zooids frequently strobilized into roundish or somewhat elongated buds for asexual reproduction, often including gonadal fragments, detectable only in NSMT-Pc 3315, 3316, and 3318. Larvae up to 650 µm (trunk length) with 3 attachment processes and 4 pairs of lateral ampullae, a single median ampulla between ventralmost and middle processes; less developed larvae with a similar median ampulla, and on each side with an elongated lateral ridge with 4 peaks (probably growing to 4 lateral ampullae).

Remarks. The newly-collected material was quite similar to the detailed redescription given by Tokioka (1954a), based on the Oka’s material, including the thoracic musculature [consisting of “12 to 15 longitudinal and ca. 30 transverse muscles on each side” (ditto: 72)], with the exception of larval morphology (a median and 4 pairs of lateral ampullae), which differed from Tokioka’s figure as stated above, although the latter condition was apparent in the Oka’s material presently studied. The variable impregnation of the tunic and peduncles with sand grains, shell fragments, and fecal pellets was also noted in both the Oka’s and new material, although not alluded to in previous descriptions of the species.

Many colonies registered as NSMT-Pc 3239 were also examined, having been collected from Tsurugi-zaki, southeastern end of Miura Peninsula, located west of the mouth of Tokyo Bay, 2 m depth, by Isamu Soyama on 23 June 1993. These were likely to have been those depicted as “Kinoko-boya E. parvum ” by Nishikawa (1994a: fig. 3 on p. 322, photographed by Mr. Isamu Soyama), although that photo was stated to have been taken in “Moroiso Bay”, also on Miura Peninsula. The colonies were similar to E. okai described above, insofar as they comprised cormidia (white in life) extending from a basal sheet, and the tunic of the peduncles and basal sheet impregnated with sand grains, shell fragments, and fecal pellets. However, they differed from E. okai in the number of transverse muscle bundles (ca. 50 vs. up to 40), as well as in the larval trunk length and ampulla arrangement (up to 520 µm and 4 pairs of lateral ampullae, instead of to 650 µm and 4 pairs of ampullae, including a median element). Because such differences may be of taxonomic significance, the Tsurugi-zaki colonies are called here as E. sp. aff. okai . Future morphological and molecular studies are likely necessary for a proper delimitation of the species.

Implications for the life history of E. okai . Table 1 summarizes monthly changes (presence or absence) in brooding larvae in thorax, gonad condition, and strobilized buds in the colonies of E. okai collected sporadically in different years from the Pacific coasts of Japan, from the Boso Peninsula to Ise Bay, sequential monthly collections throughout the year at a single locality having been unsuccessful thus far. The preliminary results obtained suggest that 1) gonad maturation begins in March at the latest, continuing until June; 2) thoracic larvae, probably shortly before release, are incubated from May to July; 3) asexual reproduction by abdominal strobilation takes place sporadically, bearing little relationship with gonad maturation.

Previous records of “kinoko-boya” or “ E. parvum (Oka) ” not considered applicable to E. okai .

1) “ Eudistoma parvum (Oka) ” by Kott (1957a). This record was based on “one small pillar-shaped colony, 1.5 cm high” from “Long Reef, N[ew]. S[outh]. W[ales].”, East Australia (ditto: 77), the larvae “with 3 anterior suckers [= attachment processes] and median unpaired ampullae dorsally, ventrally, and between the suckers” (ditto: 78). Kott’s colony was clearly distinguishable from E. okai on the basis of larval morphology (4 median ampullae in the former, while a median and 4 pairs of lateral ampullae in the latter). This record was later included under E. laysani by Kott (1990: 214).

2) “ Eudistoma parvum (Oka) ” by Nishikawa (1980) from the coast of Kii Peninsula, Honshu, Japan. The specimens included NSMT-Pc 1344, off Wagu, near Katada , Mie Prefecture, 15 March 1980, ca . 130 m depth, T . Yamamoto coll .; NSMT-Pc 1395, Tasoguchi, Gokasho Bay , Mie Prefecture, 26 July 1979, 5–7 m, T . Nishikawa; and NSMT-Pc 1474, off Kirime-zaki, Inami , Wakayama Prefecture, 18 April 1972, 90 m, T . Yamamoto, all being similar in colony shape to E. okai as described above, but more or less larger with a less developed basal sheet. Live colonies had a pale yellow tunic, including dense brown pigment granules in NSMT-Pc 1395, and the thoracic musculature consisting of rather more transverse bundles (up to 50).

3) “ Eudistoma parvum (Oka) ” by Sanamyan (1993), a single colony from the Peter the Great Bay, Sea of Japan, 4–10 m depth. Because the description lacked larval morphology (larvae absent?), a definitive identification is impossible. Subsequently, Sanamyan (2022: 279) identified the colony as Eudistoma sp. , distinct from E. okai , based on a few small morphological differences from Tokioka (1954a) and “the fact that E. parvum [= E. okai ] has not been previously reported from the Sea of Japan ”, but without new larval information.

4) “ Eudistoma parvum (Oka) ” by Nishikawa (1995) from Kuroshima Island and “ Eudistoma sp. (Kinoko-boya)” by Kosuge (2018) from Ishigakijima Island, Yaeyama Islands, Okinawa Prefecture, intertidal [reference specimens NSMTPc 3313 and 3314, Sakieda Bay, Ishigakijima Island, 31 August 2015, T. Nishikawa coll.; NSMT-Pc 3373, from vertical wall of the “Pitumutukishi” rock, Kabira Bay, Ishigakijima Island, 24 June 1975, T. Nishikawa; NSMT-Pc 3374, Kuroshima Island, 3 June 1988, K. Ito., photograph in Nishikawa (1995: pl. 139-9)]. Tunic of cormidia in life usually striking orange but sometimes variably paler, almost always deeper orange on peduncles, as depicted by Kosuge (2018: fig. 2), densely impregnated with fecal pellets (peduncles and basal sheets), but completely lacking sand grains and shell fragments; larvae in good condition up to 1000 µm trunk length, only bearing 4 median ampullae alternating with 3 attachment processes, lacking lateral ampullae, though some deviation may occur. In having foreign material completely absent inside the tunic (fecal pellets still present) and lateral ampullae of larvae, the Okinawan colonies were distinguishable from E. okai , being more reminiscent of E. laysani sensu Kott (1990: 214–216) from East Australia, “found higher up the intertidal zone”. However, “the separate lobes of living colonies” of the latter were “white with ‘pale Antwerp blue’ iridescence”, with the larval trunk only 0.4 to 0.5 mm long, unlike the usual coloration of the cormidia tunic and larval trunk length in living Okinawan specimens. The taxonomic significance of the differences between the Okinawan colonies and E. laysani sensu Kott will be the subject of a further study.

Comparison of E. okai with other Japanese congeners. Table 2 shows morphological comparisons of E. okai with seven other Japanese congeners. Of the latter, E. snakabri Tokioka, 1954 was treated as a junior synonym of E. angolanum (Michaelsen, 1914) by Kott (1990: 197–199; 1998: 108), but without any discussion. The two species clearly resemble each other in being flat-topped colonies, with a dark-colored and densely sand-impregnated tunic, and large larvae with many lateral ampullae. On the other hand, in E. angolanum “up to 8 zooids are in circles” and have “about 20 circular [muscle] bands” in the thorax ( Kott 1990: 198), whereas in E. snakabri the colony layout was unclear, although the “transverse muscles” were “very numerous (ca. 65 counted in a single zooid) ( Tokioka 1954b: 251). Such differences may be of some taxonomic significance, and the validity of the above synonymy remains in doubt. Okinawan colonies previously identified as E. viride Tokioka, 1955 by Nishikawa (1994b: fig. 2 on p. 280) should now be referred to Sigillina signifera (Sluiter, 1909) (see Nishikawa 1995: 585–586).

Eudistoma okai is clearly distinguishable from Japanese congeners by a combination of several features (colony composed of pedunculated cormidia; tunic white in life and impregnated with sand grains, shell fragments and fecal pellets; many transverse thoracic muscle fibers; larvae with 4 pairs of lateral ampullae and a single median ampulla between ventralmost and middle attachment processes). Nevertheless, specific distinction within the genus Eudistoma remains difficult because of its few distinctive characters. Millar (1975: 221) stated that “the difficulties encountered in characterizing Eudistoma spp. cannot be over-emphasized” because “characteristics of the colony—its shape, colour and test [= tunic] inclusions—afford more reliable characters for species identification than the zooids themselves” (see also Kott 1990: 192). Thus, future taxonomic revisions, in particular using molecular analyses, seem necessary and applicable to world-wide nomenclatural considerations.

Figures

Fig. 1. Eudistoma okai Sanamyan from Misaki, Sagami Bay, 5 June 1928, registered as NSMT-Pc 7485. A, Fragment of colony; B, larva incubated in thorax (tail omitted), two lateral ampullae behind, which were concealed by the frontal lateral ampullae, are not shown. Abbreviations: AP, attachment process; LA, lateral ampulla; MA, median ampulla. Scales:A, 5mm; B, 250µm.

Fig. 2. In situ photos of Eudistoma okai Sanamyan. A, Taken in the rocky intertidal zone at Jyogashima Island, Miura Peninsula, Sagami Bay, 17 April 2014, representative of colonies of NSMT-Pc 3323; B, taken in a very shallow tide pool, Yoshio, Boso Peninsula, 24 March 2011, representative of colonies of NSMT-Pc 5051–5053.