Spirobranchus akitsushima, Nishi & Abe & Tanaka & Jimi & Kupriyanova, 2022

Nishi, Eijiroh, Abe, Hirokazu, Tanaka, Katsuhiko, Jimi, Naoto & Kupriyanova, Elena K., 2022, A new species of the Spirobranchus kraussii complex, S. akitsushima (Annelida, Polychaeta, Serpulidae), from the rocky intertidal zone of Japan, ZooKeys 1100, pp. 1-28 : 1

Spirobranchus akitsushima sp. nov.

[Japanese name: Yakko-kanzashi gokai] Figs 2 , 3 , 4 , 5

Pomatoleios crosslandi non Pixell, 1913. - Okuda 1937: 64-67, pl. 2, fig. 1; Onagawa Bay; Utinomi 1956: 41, pl. 21, fig. 3; south of Tohoku.

Pomatoleios kraussii non Baird, 1864. - Imajima and Hartman 1964: 372; Okuda and Imajima 1965: 531; Sawada 1984: 105 [development]; Sawada 1988: 76-77, fig. 5-4, 5-5, 5-6, table 5-3 [reproduction, development]; Imajima 1977: 100-101; Ogasawara Island; 1978: 56; Nii-jima, Izu Islands; 1979a: 178; Kii Peninsula; 1979b: 33; 1984: 165; Oga Peninsula; 1986: 154; Oki Islands; Uchida 1978: 32; Wakayama, Izu, Kochi; Akiyama 1981: 100-101 [distribution, tube characters]; Miura and Kajihara 1984: 343-352; Misaki [distribution, larval development]; Uchida 1992: 369, pl. 71-7; south of central Honshu; Khandeparker et al. 2005; Seto, Wakayama [development]; Horikoshi and Okamoto 2007; Tokyo Bay; Uchida 2008: 180, table 1; Wakayama [distribution].

Pomatoleios kraussii (Baird, 1865)? [sic]. - Imajima 1996: 342, fig. 280; south of Honshu.

Pomatoleios cf. kraussii . - Suzuki et al. 2013: 196, fig. 326.

Spirobranchus kraussii . - Nishi et al. 2017: 96.

Spirobranchus sp. 1. - Kobayashi and Goto 2021: 4-5, figs 2, 3; Wakayama [tube structures, coloration of peduncle, molecular analysis]; Ohno et al. 2021; Echizen, Fukui [distribution].

Material examined.

Holotype: Japan • Sagami Bay , Kamakura, Wakaejima Island; 35.300628°N, 139.550868°E; 4 June 2020; Nishi, E. leg.; intertidal rocky shore (Figs 1D , 2A, B ), collected by hand; GenBank: LC661622, LC661636, LC661650, LC661664 ; CBM-ZW 1127, hologenophore.

Paratypes: Japan • 4 specimens; same collection data as for holotype; GenBank: LC661623 - LC661626, LC661637 - LC661640, LC661651 - LC661654, LC661665 - LC661668 ; CBM-ZW 1128 to 1131, all hologenophores • 6 specimens, including 1 spec. lacking crown; collection site same as for holotype; 3 August, 2020; GenBank: LC661630 - LC661635, LC661644 - LC661649, LC661658 - LC661663 ; CBM-ZW 1135 to 1140, all hologenophores • 3 specimens; Shizuoka, Omaezaki (Fig. 1B ), Todai-shita ; 34.594861°N, 138.225556°E; 4 August 2020; Tanaka, K. leg.; intertidal rocky shore, collected by hand; GenBank: LC661627 - LC661629, LC661641 - LC661643, LC661655 - LC661657, LC661669 - LC661671 ; CBM-ZW 1132 to 1134, all hologenophores .

Non-type material.

Japan • 10 specimens; Sagami Bay, Hayama, Chojagasaki; 35.253254°N, 139.578030°E; 8 June 2020; Nishi, E. leg.; intertidal rocky shore, on vertical rocks (see Figs 1E , 2C, D ); CMNH-ZW 2273, paragenophores • a single specimen; same collection data as above; CMNH-ZW 2274, paragenophore • a single specimen; same collection data as for paratype from Omaezaki CBM-ZW 1132; CMNH-ZW 2275, paragenophore • a single specimen; same collection data as for paratype from Omaezaki CBM-ZW 1132; MSM-INV-21-1, paragenophore • a single specimen; same collection data as for holotype; CMNH-ZW2276, paragenophore • a single specimen; same collection data as for holotype; CMNH-ZW2277, paragenophore • a colony of worms with tubes; same collection data as for paratype CBM-ZW 1135-1140; MSM-INV-21-2, paragenophore • 3 specimens with tubes; Ogasawara, Chichijima Island, Sakaiura; 27.082548°N, 142.207746°E; 28 June 1995; Nishi, E. leg.; intertidal rocky shore, by hand; CMNH-ZW 2278, syngenophores.

Description.

Tubes white, blue, or purple, inside and outside (Fig. 2D, E, G, H, J, K-Q ). Tube (sub)triangular in cross-section, with flattened or pointed median sharp keel (Fig. 2E, H, K-N, P ), laterally with a row of transverse ridges (Fig. 2K, L, P, Q ) and a row of pits below sharp keel (Fig. 2Q ). Internal diameter (minimum, mean, maximum) in adults (Fig. 2Q, R, T, U ) 1.0, 1.45, 2.1 mm (SD 1.34, n = 10 for Kamakura specimens). Outer tube diameter 2.2 to 3.0 mm. A blunt flap over tube mouth (Fig. 2E, M ) for 1.5 to 2.8 mm, 1.2 to 2.5 mm wide, in Kamakura and Hayama specimens (see Fig. 2B, D ). A sharp flap over tube mouth in Sagami Bay and Yokohama specimens (Fig. 2G, H L, P). Juvenile tube with an undeveloped keel (Fig. 2K ). Posterior tabulae rarely found (Fig. 2O ).

Operculum with inversely conical to shallow ampulla, covered with calcareous endplate (Fig. 4A-D, F, G ) 1.4 mm in diameter (holotype), 1.0-1.5 mm in paratypes, without spines or ornamentations, and usually covered with filamentous algae and bryozoans (Fig. 4C, D, G ). Dissected endplate circular in top view, lower part covered with blue membrane (Fig. 4H ), bowl-like in lateral view (Fig. 4I ). Talon absent (e.g., Fig. 5A, E ), slight rounded swellings without bulges or protuberances on underside of calcareous endplates present in some worms (Figs 4H, I , 5B, C, D, F-H ). In dissected endplate rounded swelling length 0.38-0.55 mm (Fig. 5B-D, F-H ).

Peduncle broad, triangular in cross-section, with simple (unbranched) distal lateral wings (Fig. 4D, F, G ) and middle lateral constrictions (Fig. 4F, G , arrowed), rarely branched (Fig. 4E ); ventrally with two lateral dark bands on white background (Fig. 4A ); lateral wings with alternating pale and dark bands (Fig. 4D, F ); inserted at base of radiolar crown left of median line (Fig. 4D, F, G ).

Radioles arranged in two semicircles (Fig. 4C, G, J ). In type specimens, 17 pairs of radioles in holotype, 13-19 pairs in paratypes. In holotype, radioles 1.6-1.8 mm long, distal tip (without pinnules) 0.3 mm, interradiolar membrane extending 1/2 of radioles (Fig. 4G, H, I ). Radiolar eyes 3 or 4 pairs above interradiolar membrane (Fig. 4H, I, K ). Mouth palps present.

Collar and thoracic membranes. Collar trilobed, with extensive ventral lobe covering almost entire crown (Fig. 4A-C ), wide gap between right and left dorso-lateral lobes (Fig. 4D ). Tonguelets folded, leaf-like. Thoracic membranes forming ventral apron across anterior abdominal segment (Fig. 4A-C ).

Thorax with six thoracic uncinigerous segments, juveniles with collar chaetae and adults without. Length 2.0 mm in holotype, 1.6-2.5 in paratypes, width 1.0 mm in holotype, 0.7-1.2 in paratypes. Collar chaetae in juveniles simple limbate and with numerous hairlike processes at the base of distal limbate part ( Spirobranchus chaetae). Apomatus chaetae absent. Thoracic chaetae limbate (Fig. 5I ). Uncini saw-shaped with 9-11 teeth (Fig. 5J ). Ventral ends of thoracic uncinigerous tori widely separated anteriorly, gradually approaching one another toward the end of thorax, thus leaving a triangular depression (Fig. 4A-C ).

Abdomen with 46 chaetigers in holotype, 34 to 60 chaetigers in paratypes. Length 3.6 mm in holotype, 3.0-4.0 mm in paratypes. Two or three achaetous segments in anteriormost abdomen (Fig. 4B, C ). Uncini saw-shaped with 9-11 teeth (Fig. 5L ), incidentally with two teeth above blunt, clearly gouged underneath peg (Fig. 5J ). Abdominal chaetae true trumpet-shaped, abruptly bent distally, with two rows of denticles separated by a hollow groove and forming long lateral spine (Fig. 5K ). Chaetae becoming increasingly longer posteriorly, but posterior capillary chaetae absent. Posterior glandular pad absent.

Colour oblique lateral stripes of alternating white and gray colors sometimes appearing in opercular peduncles of live specimens (Fig. 4A, D, F, G ), these stripes fading in preserved worms. In radiolar crown of worms in Kamakura, Hayama, and Miura Peninsula, the third or fourth of each radiole on dorsal side yellow, particularly above inter-radiolar membrane (Fig. 4A-D, G ), whereas some worms lack this yellow coloration. Ventrally, some radioles yellow, but others brown to black, or reddish (Fig. 4F ). Radiolar eyes dark brown, pale brown, or dark red (Fig. 4C, D, F, G ). Males with creamy white abdomens filled with sperm, females with orange to pale orange abdomens when filled with eggs (Fig. 4B, C ).

Paleo (sub-fossil) and Recent tube aggregations.

Aggregations of Spirobranchus akitsushima sp. nov. were common on vertical natural rocks in Hayama (Fig. 2C, D ) from -10 to +15 cm from MSL, while solitary live worms were also found at -100 to +65 cm from MSL. In Kamakura and Tsurugizaki aggregations were abundant on and below natural rocks and in rock pools (Fig. 2A, B, F, G ). Spirobranchus akitsushima sp. nov. is highly gregarious, sometimes with a density of more than 100 specimens per cm2 (Fig. 2C, D, G ), and the animals form an intertidal belt on concrete blocks and wall steps, extending horizontally for 10 m along the coast of Yokohama (Fig. 2H-J ). At one site in the intertidal of Jogashima, both Recent and sub-fossil tube aggregations were observed within an area of 2 m2 (Fig. 3A, D ). Recent tubes in densities ranging from 1 to> 100 per 102 were found at -110 to +60 cm from MSL, and dense aggregations (> 10 tubes/10 cm2) extending horizontally for ~ 1 m were found at -10 to +20 cm from MSL (Fig. 3D, H ). Small patchy paleo-aggregations were found on vertical rock walls and in tide pools (Fig. 3A, B, E-G ). The sub-fossil tubes of bluish color were entangled (Fig. 3F, G ) and their keels, transversal ridges, and pits, were preserved (Fig. 3E-G ).

Both Recent and sub-fossil tube aggregations were also found in Tsurugizaki. The paleo-aggregations (P1 of Fig. 3I , Fig. 1I , north-eastern one) were 25-30 m away in horizontal distance from the Recent aggregations (C1 of Fig. 3I ). In P2 and P3 of Fig. 3J , numerous aggregations of fossilized tubes were also found in a marine cave (Fig. 3K, L ) 12-15 m away in horizontal distance from the recent aggregation (Figs 1I , 3J ). In P2 and P3, sub-fossil tubes were well preserved (Fig. 3K ). Particularly in P2, these aggregations were separated into two layers, and upper one found at +150 to +210 cm and the lower one approximately +70 to +100 cm from MSL.

Type locality.

Intertidal rocky shore of Kamakura, Sagami Bay, Honshu, Japan.

Etymology.

The specific epithet refers to Akitsushima, another name of Japan in the Nara era, ~ 1,300 years ago, as appeared in Kojiki (The Records of Ancient Matters) and Nihon Shoki (The Chronicle of Japan).

Taxonomic remarks.

Spirobranchus akitsushima sp. nov. is superficially similar to both S. kraussii from South Africa and S. sinuspersicus Pazoki, Rahimian, Struck, Katouzian & Kupriyanova, 2020 from the Persian Gulf. Pazoki et al. (2020) compared S. sinuspersicus and S. kraussii in body length, number of abdominal chaetigers, endplate morphology (shape of talon), peduncular wing morphologies and site of peduncular origin, chaetal distribution pattern, and uncinal teeth distributional pattern (rasp- or saw-shaped). The new Japanese species can also be distinguished by endplate morphology, site of origin of peduncle, and uncinal teeth distributional pattern (Table 3 ). We also compared our new species to two recently described South Asian species, S. bakau Sivenanthan, Shantti, Kupriyanova, Quek, Yap & Teo, 2021 and S. manilensis Sivenanthan, Shantti, Kupriyanova, Quek, Yap & Teo, 2021 in Table 3 ; the authority of S. manilensis was clarified in Read and Fauchald (2021).

Imajima (1996: 342, fig. 280) had recorded Japanese “Yakko-kanzashi” as Pomatoleios kraussii (Baird, 1865)? [sic!] from around Honshu and to the south of it, with a note stating "uncini shape might be different from the one of South Africa, and thus it might be a different species". This inference was also noted in Imajima (1997: 23-24). Detailed observations using SEM images of S. kraussii uncini and chaetae ( Simon et al. 2019) and our new species of Japan (this study) have not shown any differences in morphology and number of teeth of uncini in thorax and abdomen. We distinguish the two species (South African and Japanese) based mainly on the results of genetical analysis and other morphological characters.

Kobayashi and Goto (2021) observed a flap-like structure over the tube mouth in their specimens collected from both Seto, Wakayama and Okinawa. This structure was also observed in the Sagami Bay population of the new species (Fig. 2E, M ). The ventral surface of the peduncle in Seto specimens has a dark coloration with dense pigmentation ( Kobayashi and Goto 2021) as in ones of our new species from Sagami Bay and Omaezaki (Fig. 4D, F, G ). In their Okinawan specimens, the coloration of peduncles was whitish and never heavily pigmented, and lacked lateral banding in some worms ( Kobayashi and Goto 2021). As the coloration of Okinawan worms was observed for ethanol preserved specimens, further comparisons of fresh specimens are needed.

Spirobranchus lirianeae Brandão & dos Santos Brasil, 2020, another species of the S. kraussii -complex from Brazilian waters, has a concave opercular endplate and its talon is with protuberances, while abdominal uncini have 13 or 14 teeth. The subtidal solitary species inhabits tubes with a single sharp longitudinal keel. In S. akitsushima sp. nov. the tube has either a flattened projection of the tube keel (Fig. 2E, M ) or sometimes a single sharp longitudinal keel (Fig. 2H, L, P ), both appearing in the same aggregation. The Japanese new species, while highly gregarious and belt-forming (Figs 2B, C, I , 3D, H ), sometimes forms small aggregations and even solitary specimens have been observed. A similar range of appearances, solitary to highly gregarious, was noted and analyzed by Smith et al. (2012) for the New Zealand S. cariniferus (Gray, 1843). We summarize the new species characters in Table 3 .

Spirobranchus bakau Sivananthan, Shantti, Kupriyanova, Quek, Yap & Teo, 2021, recently described from mangrove roots of the Singapore intertidal zone, has very characteristic tubes with wing-like keel structures and in some cases with lateral keels ( Sivananthan et al. 2021: fig. 2). Adults of the Singaporean species have collar chaetae, which are limbate type only, no Spirobranchus -type chaetae, while thoracic uncini are saw-to-rasp-shaped ( Sivananthan et al. 2021). Its opercular talon is a peg-like structure extending downwards from endplate into the opercular ampulla, terminally bifid or trifid ( Sivananthan et al. 2021). In contrast, our new species has no wing-like keel structures or lateral keels in tubes, collar chaetae are absent in adults, uncini are saw-shaped, and there is no talon on the underside of the opercular endplate.

Spirobranchus manilensis Sivananthan, Shantti, Kupriyanova, Quek, Yap & Teo, 2021 (non Pillai, 1965), originally described from Manila Bay, Philippines, has also characteristic tubes with white to pale brown color, with one to two keels; peduncle with peduncular wings ending in pointed tips; operculum with sub-triangular talon, extending downwards from endplate into tissue of opercular ampulla, with a series of tooth-like serrations along the edge ( Sivananthan et al. 2021). In contrast to this South Asian species, our new Japanese species has a tube with blue coloration (Fig. 2H, L-Q ), a median keel (Fig. 2 L, M, P, Q ), peduncular wings with rounded tips (Fig. 4F, G, E ), and no talon on the underside of the opercular endplate (Fig. 5A-H ).

Spirobranchus akitsushima sp. nov. has peduncles originating from the left side as in S. kraussii ( Simon et al. 2019), in S. lirianeae (see Brandão and dos Santos Brasil 2020), and in S. bakau (see Sivananthan et al. 2021); however, that of S. sinuspersicus originates medially ( Pazoki et al. 2020). Pazoki et al. (2020) noted the differences in peduncular wings between S. kraussii and S. sinuspersicus , the former having a Y-shaped, the latter a V-shaped appearance. Judging from the figures of Brandão and dos Santos Brasil (2020: fig. 2B, C, F, G), lateral wings of the peduncle in S. lirianeae have a V-shaped appearance. Spirobranchus akitsushima sp. nov. has both types of peduncles, which suggests that this character may vary depending on the methods of fixation (e.g., fixed within tubes or without) and necessitates further comparative research.

The upper surface of the endplate is flat and unadorned in all species of the S. kraussii complex, but the talon on the lower surface of the endplate appears useful for species delimitation in the complex. The endplate of the new Japanese species is characteristic as it has no talon (= lacking bulges or ornamentations), while other valid species from South Africa, Persian Gulf, Singapore, Brazil, and the Philippines have distinct talons ( Simon et al. 2019; Brandão and dos Santos Brasil 2020; Pazoki et al. 2020; Sivananthan et al. 2021). Other as yet not formally described populations of the complex either lack a talon ( Sun et al. 2012: Hong Kong) or have one ( Bailey-Brock 1987: Hawaii; Belal and Ghobashy 2012: Suez bay). Among them, the population from Suez Bay has a long talon, extending into base of peduncle ( Belal and Ghobashy 2012). To clarify the taxonomic status of the above populations of S. kraussii complex, a detailed morphological study accompanied by DNA sequence data is warranted.

Figures

Figure 1. Map of collection sites A Japan and adjacent seas B Sagami Bay, Suruga Bay, and Pacific side of Honshu, and collection sites on Miura Peninsula and Yokohama C collection sites of Miura Peninsula and Yokohama D Wakaejima, Kamakura, type locality of Spirobranchus akitsushima sp. nov. E Hayama F Western part of Miura Peninsula, showing Tsurugizaki and Jogashima G Jogashima H close-up view of collection sites of Jogashima I close-up view of Tsurugizaki. Key: ○: paleo-aggregation, ● (red): current distribution. Arrow in H indicates (A) in Fig. 3; P 1 - P 3 and C 1 in I indicates site of (I) and (J) in Fig. 3.

Figure 2. Field view of collection sites, aggregation, tubes of Spirobranchus akitsushima sp. nov. A, B Wakaejima, Kamakura C-E Hayama, Sagami Bay F, G Tsurugizaki, Miura Peninsula H-J Nojima, Yokohama. Aggregation of Yokohama found on concrete wall (I), around mean-sea level, thickness ~ 3 - 5 cm (H, J) K-O tubes of Kamakura population P, Q Ogasawara specimens. Scale bars: 1 mm (K, L, M, N, O, P), 2 mm (Q).

Figure 3. Paleo-aggregations of Spirobranchus akitsushima sp. nov. Jogashima (A-H), and Tsurugizaki (I-L) K close-up view of P 2 of J L close-up of P 3 of J. Paleo-aggregation (P 1 - 3) and current distribution (C 1) in I and J are corresponding to P 1 - P 3 and C 1 in Fig. 1 I.

Figure 4. Type and non-type specimens of Spirobranchus akitsushima sp. nov. A-E, H, I Kamakura specimens F Hayama specimens B, C mature female specimen A ventral view, lateral band of peduncle (arrows) D, F, G dorsal view B, E lateral view E bilobed wing tip (arrows) F, G operculum in dorsal view, middle constriction (arrows) H, I dissected endplate H lower view, covered with a blue membrane I lateral view. Abbreviations: ac, achaetous chaetiger; ap, apron; c, collar; pd, peduncle; w, wing. Scale bars: 1 mm (A, B); 2 mm (C, D, F, G); 0.5 mm (E, H, I).

Figure 5. Scanning electron microscopy images of operculum (A-H) and chaetae (I-M) of Spirobranchus akitsushima sp. nov. A-D ventral view of endplate E-H lateral view. Note that some endplates are with a rounded swelling (sw), B-D. I thoracic capillary chaetae, scales are in close-up J thoracic uncini K abdominal true trumpet-shaped chaetae L abdominal uncini. Scale bars: 0.1 mm (A-H); 0.01 mm (I-L).