Siphonaria japonica (Donovan, 1824)

Jenkins, Bruce & Köhler, Frank, 2024, Hidden in plain sight: Systematic review of Indo-West Pacific Siphonariidae uncovers extensive cryptic diversity based on comparative morphology and mitochondrial phylogenetics (Mollusca, Gastropoda), Megataxa 13 (1), pp. 1-217 : 31-34

Siphonaria japonica (Donovan, 1824)

( Figs 13A–L, Q–S , 15B–E )

Patella japonica Donovan 1824 : unpaginated, pl. 76 (type locality: Japan).— Kuroda et al. 1971: 483, pl. 64, fig. 7; White & Dayrat 2012: 64.

Siphonaria cochleariformis Reeve, 1856 : species 28, pl. 6 (type locality: Hainan).

Siphonaria japonica — Hanley 1858b: 152; Paetel 1889: 428; Pilsbry 1920: 141; Abe 1940: 59; Hirase 1941: 94, pl. 121, fig. 12; Kuroda 1941: 137; Hubendick 1945: 27, fig. 34, 36, 39, 41; Kuroda & Habe 1952: 86; Kuroda 1960: 43; Habe & Kikughi 1960: 64; Shikama 1964: 6; Cook 1969: 697; Berry 1977: 197, fig. 19; Galindo 1977: 416; Chambers 1980: 141, 143; Hirano & Inaba 1980: 323; Hirano 1980: 335; Morton & Morton 1983: 298; Zhongyan 2004: 197, fig. 30, 198, pl. 108, fig. E; Chim & Tan 2009: 269; Murty et al. 2013: 104; Dayrat et al. 2014: 266, ‘unit 2’, fig. 3B; Gonzàlez-Wevar et al. 2018: 5, fig. 1.

Siphonaria alterniplicata Grabau & King 1928: 62 (type locality: ‘Peitaiho’).— Hubendick 1946: 62; Galindo 1977: 416; White & Dayrat 2012: 60; Coan et al. 2015: 221, pl. 38 A, B (as “ S. alterniplata ”).

Siphonaria (Sacculosiphonaria) japonica — Hubendick 1946: 42, pl. 2, figs 29–32; Knox 1955: 46; Kira 1962: 201, pl. 69, figs 8a–b; Habe 1971: 15, pl. 4, fig. 16; Yoo 1976: 89, pl. 19, figs 1, 3; Inaba 1983: 145; Christiaens 1980b: 466; Fukuda et al. 1992: 76, pl. 23, figs 360a–b; Chambers et al. 1998: 51; Noseworthy et al. 2007: 90.

Siphonaria (Siphonaria) kurracheensis — Hubendick 1945: 72, 31 fig. 51 (not S. kurracheensis Reeve, 1856 ).

Sacculosiphonaria japonica — Kuroda et al. 1971: 483, pl. 64, fig. 7; Trew 1983: 9.

Siphonaria (Kerguelenella) corallina Christiaens 1980a: 80 , fig. 18.— Christiaens 1980b: 467.

Siphonaria (Sacculosiphon) japonica — Je 1989: 89 (incorrect subsequent spelling of Sacculosiphonaria ).

Material examined. Type material. Neotype of Patella japonica Donovan, 1824 , present designation, from Headland S of Chitose Bch, Boso Peninsula, Japan, 34°59.240’N, 139°58.304’E; coll. B.W. Jenkins, 15 March 2020, JP02-2 ( AM C.584938 [M489, SK308]; Figs 13A , 15D–E ).

Syntypes of Siphonaria cochleariformis Reeve, 1856 ( NHMUK 1981015 , Fig. 13H–K ) .

Syntypes of Siphonaria alterniplicata Grabau & King, 1928 ( MBM 280642 , 72 shells, Peitaino , July 1925; Fig. 13F ) .

Holotype of Siphonaria (Kerguelenella) corallina Christiaens, 1980 from Channel Rock , Hong Kong, China; on corals at 10m depth ( NHMUK 1977170 , Fig. 13G ).

Other, non-type material. Japan, Honshu : Boso Peninsula, Point S of Chitose Beach, 34°59.240’N, 139°58.304’E, JP02-2 ( AM C.585394 9p, AM C.585113 p [SK423], AM C.585934 p [SK425], AM C.585935 p [SK339], AM C.584983 p [SK338], AM C.595953 p [SK566]); seawall Arai Bch, Tateyama 34°59.838’N, 139°51.378’E, JP02-1 ( AM C.585389 10p, AM C.585235 p [SK340]) . China: Hong Kong, Cape D’Aguilar 22°12.28’N, 114°15.38’E ( ZRC.MOL.2001-1768 21p, ZRC.MOL.24905 p [M476, SK283], ZRC.MOL.24903 p [SK403], ZRC. MOL.24904 p [SK404], ZRC.MOL.24906 p [SK405]) .

Taxonomic remarks. Type species of Sacculosiphonaria Hubendick, 1945 by original designation. This name became first available with publication of the original plate 79 (June 1, 1824) not the bound volume (3, 1825). Plates and texts were ‘published monthly, bound yearly’ (Molluscabase Eds. 2022). The original description does not contain an original type designation. The original type material is considered lost as it could not be found at the NHMUK in 2022 (J. Ablett, pers. comm.). The neotype is designated herein to clarify the identity of this nominal species and to designate the type locality (Art. 75.3 of the Code).

Our delineation of this species is based on comparative analyses of the morpho-anatomy and mitochondrial genetics of freshly collected topotypes ( Figs 13B–D ) and geographic series of additional specimens (Tables S1–2). Pilsbry (1920a: 141) treated S. cochleariformis Reeve, 1856 as a junior synonym of S. japonica (Donovan, 1824) . This was followed by Hubendick (1946: 43), Kuroda & Habe (1952), Kuroda (1960), and Dayrat et al. (2014). We maintain this synonymy but note that it requires corroboration through examination of topotypic material, which is currently unavailable. The types of S. cochleariformis ( NHMUK 1981015, Figs13H–K ) closely resemble the figures in the original description of Reeve (1856). These shells also match the original description and figures of P. japonica in Donovan (1824). Moreover, Reeve (1856) appeared to be unaware of the description of S. japonica . Hedley (1915: 752) correctly stated that the record of S. cochleariformis from NSW ( Angas, 1867: 232) is by mistake.

The type locality of S. alterniplicata can be inferred from the title of the work to be ‘Peitaiho’ [ China, Beidaihe District, 39°50′N, 119°29′E] ( Grabau & King, 1928: 62)’. The syntype of S. alterniplicata figured in Coan et al. (2015: 221, fig. 38). The proposed synonymy of S. alterniplicata ( Fig. 13F ) remains to be tested by examination of topotypes.

Siphonaria (Kerguelenella) corallina wasdescribedby Christiaens (1980a: 80) based on five specimens collected from corals and barnacles at 10m depth off Channel Rock, Hong Kong, with the largest specimen lodged as holotype in NHMUK ( Fig. 13G ). Christiaens figured the shell and halfradularowfortheholotype( Christiaens,1980a:80,fig. 18A, C) indicating the radula dentition formula of 19.1.19. No other material is recorded. Unfortunately, no animals are available to confirm anatomical (mainly radula) or assess molecular characteristics. However, examination of the holotype indicates the specimen is a juvenile. It is brownish transparent and has wide and glassy growth lines on the shell consistent with early growth stages in siphonariids. The holotype can be aligned well with the early growth stages of adult specimens of S. japonica ( Fig. 13N ), revealing that shell profile, apex, prominent ribs, and formation of dual siphonal ridge ribs match. By contrast, the holotype cannot be aligned with early growth stages in shells of other co-occurring species, such as S. alba ( Fig. 13M ), S. subatra ( Fig. 13O ) and S. rucuana ( Fig. 13P ). While molecular sequences are required for validation, we postulate that the holotype of S. corallina is a juvenile of S. japonica . Regarding collected depth, it is not uncommon for Siphonaria to occur subtidally (e.g., S. lateralis has been recorded from ‘bottom of a 6 m deep tide pool’ at the Snares Islands ( AM C.586004; coll. D. Horning) and at ‘3 to 4.5m’ at Aerial Cove, MI, Australia (coll. J. Lowry). However, most specimens have been recorded intertidally.

External morphology ( Fig. 13Q ). Foot sole, foot wall, mantle, cephalic folds and pneumostomal lobe all evenly orange in colour; mantle thin, narrower than foot wall, edge thickened lobed with black bands aligning with rib interstices; dark irregular black blotches of pigmentation on foot wall and cephalic lobes, fading to join with mantle, concentrated over centre of cephalic folds; pneumostome long between right adductor muscles and within mantle.

Shell ( Figs 13A–L ; Table S9). Medium sized (max sl mean = 19.4 mm, SD = 1.7 mm, n = 9), circular ovate, height medium, shell thin; apex offset strongly posterior and weakly left, apical sides strongly convex, protoconch direction homostrophic (n = 1), shell whorl dextral; growth striae prominent uneven, radial colour banding faint, exterior pale brown; rib count (mean = 46, SD = 6, n = 5), wavy and bent, pale red brown/grey, ridges narrow, rounded, golden tan, variably raised, uneven, slightly broaden to align with unscalloped shell edge; ~ 20 primary ribs, 2–3 finer secondary ribs between primary ribs, interstices narrow with regular red brown and irregular dark grey/white markings; paired primary ribs form siphonal ridge, protrudes slightly beyond shell edge. Interior: shell lip with white rays aligning under primary/secondary ribs, fade over pale tan shell margin; ADM scar and spatula evenly dark brown, siphonal groove distinct; ADM not prominent, CMS straight; thickening/ whitening of shell lip not apparent.

The neotype ( Fig. 13A ). Shell (sl = 20.5, sw = 16.8, sh = 7.5 mm) elongate ovate, medium; thin, apex offset weakly to posterior and left, exterior uneven, mottled brown with radial banding, interstices with dark grey and reddish flecks, ~ 42 ribs, siphonal ridge clear, formed by adjacent dual ribs. Interior shell lip dark brown strongly corrugated with pale rays aligning under ribs, margin whitish tan, RS ( Fig. 15D ) and SPM ( Fig. 15E ).

Reproductive system ( Figs 15B, D; n = 4). Positioned to the right side of coelom, against foot wall on foot muscle, under the respiratory cavity; epiphallic parts positioned between RAM and BM; GA small, with singular GP through foot wall; AO small, elongated, narrow, centrally bent, bluntly pointed, joined to lower ED and upper GA; ED long, wide, centrally coiled / folded, joins to outer side of GA; GA, AO, ED all white muscular fibrous tissue; EG large elongated, slightly shorter than ED, soft whitish tissue, slightly folded, joins ED; single, long, narrow, coiled flagellum (F1), appears as an extension of wider ED, lays over back of BM; BD and CD junctions into GA close between ED join and GP but in opposing directions, both ducts narrow, long, smooth, whitish, featureless, pass closely together through RAM ( BD over CD) into soft white folded tissues of MG; MG / AG complex medium; CD connecting to AG / MG ducts, BD with folded distal loop and MA, BC very large, embedded in top of MG against AG, elongated spherical, thin whitish translucent test; HD short, large, coiled, links ducts in soft white folded tissues of AG to yellowish granulated HG; AG smaller than HG, sides match curvature of inner foot wall.

Spermatophore ( Figs 15C, E ). Cylindrical, thread-like (length = 13.9 ± 1.5 mm, n = 3), test thin, translucent; head tip tapered bluntly rounded, section containing a white gelatinous core, tapers to a thin flagellum and tip; both sections smooth, 8–12 short barbs on upper flagellum pointing towards head (n = 3); head section smooth, longer thicker than flagellum (head length = 8.3 ± 0.2 mm, n = 3; 60% of SPM length, SD = 6%; flagellum length = 5 ± 1.5; head section width = 195 ± 12 μm; flagellum width = 33 ± 12 μm), 10 SPM tightly coiled in white gelatinous mass in BC of one specimen ( ZRC.MOL.24905 [M476, SK283]).

Radula and jaw. Dentition formula “varies at any rate between 32:1:32 and 40:1:40” ( Hubendick 1946: 43).

Comparative remarks. Siphonaria japonica ( normalis group, unit 2) forms a distinct mitochondrial clade together with its sister species, S. camura sp. nov. ( Figs 1 , 4 ). The minimum distance between S. japonica and S. camura n. sp. is 11.1% in COI (Table S8).

Throughout the range of S. japonica we found four congeners occurring in partial sympatry. Three are sympatric with S. japonica on Honshu: Siphonaria acmaeoides has a more solid, whitish, smoother shell with a more central apex, a smaller AO and BC, and a shorter F1 and short drop-like SPM. Siphonaria sirius has more prominent and raised ribbing with stronger edge scalloping, a larger AO, and SPM without barbs. For comparison with S. sipho refer to that species. Siphonaria camura sp. nov. has a smaller, paler shell with less raised ribbing, strongly offset and hooked apex with weaker edge scalloping, smaller AO and F1, and a larger BC.

Shell, RS,and SPM of ‘ S.cochleariformis’ depicted by Hubendick (1945: 26, fig. 34–36, 28, fig. 43; 1946: 14, fig. 20) from Japan, subsequently reproduced by Berry (1977: 210, fig. 19), correspond well with S. japonica (both taxa are synonyms). However, we found that type specimens of S. cochleariformis ( Fig. 13H–K ) differ from typical S. japonica in being more solid, whitish, unpatterned, and having a thickened margin and raised ribs. However, no topotypic material of S. cochleariformis is available to study and we cannot address its taxonomic status. Figures of the SPM of ‘ S. kurracheensis ’ in Hubendick (1945: 31, fig. 51) are attributed to S. japonica ; the number of barbs corresponds well with features typical of this species whereas flagellum barbs are absent in S. kurracheensis . Figured specimens of S. japonica in Yoo (1976: pl. 19, figs 1, 4) from Korea are misidentifications; fig. 2 and possibly fig. 3 are correctly identified. A record of ‘ S. japonica ’ from Hainan Island ( Hasegawa et al. 2001: 29) is plausible but requires confirmation by dissection and/or DNA sequencing.

Distribution and habitat. Recorded from Hong Kong, Honshu, Taiwan ( Fig. 11 ). In this study, commonly found on exposed rocky shores at various locations on Honshu, in crevices and hollows across the upper littoral level.

Figures

FIGURE 1. Maximum Likelihood phylogram based on analyses of a concatenated sequence data set of 16S and COI. Branches are collapsed at the species level. Branch labels give unit numbers and accepted species names. Numbers on branches indicate branch support employing 10,000 ultrafast bootstraps.Available genus-group names are shown next to their type species. Scale bar indicating modelled sequence divergence.

FIGURE 4. Maximum Likelihood phylogram (partial, species not collapsed). Clades C–F (normalis, lateralis and pectinata groups) of the tree shown in Fig. 1. Branch labels give specimen identifiers for new sequences or Genbank accession numbers for imported sequences from other studies and geographic regions (see Tables S1–S2 for details). Identical haplotypes are merged into single tips. Numbers on branches indicate branch support by employing 10,000 ultrafast bootstraps. Clade names give unit numbers and accepted species names. Scale bar indicating modelled sequence divergence.

FIGURE 11. Occurrence records of S. sipho, S. javanica and S. japonica.

FIGURE 15. Reproductive anatomy of S. javanica, S. obliquata, and S. australis. A. S. javanica. Timor-Leste, Dili, AM C.584795 [M434]. B–E. S. japonica. B–C. Hong Kong, ZRC.MOL.24905 [M476, SK283]. D–E. Honshu, Boso Peninsula, Neotype AM C.584938 [M489, SK308]. F–H. S. obliquata. F–G. NZ, Dunedin, Neotype NMNZ M.331450 [M515, SK421]. H. South Island, West Coast, TS, NMNZ M.331115 [M516, SK422]. I–J. S. australis I–J. NZ, Stewart Is, AM C.585247 [M480, SK284]. Unlabelled scale bars 1 mm.

FIGURE13.Shells of S.japonica.A.Neotype ofPatella japonica, BosoPeninsula,AM C.584938 [M489, SK308].B.AMC.595953 [SK566]. C. AM C.585389 [SK340]. D. AM C.584939 [SK338]. E. AM C. 585935 [SK425]. F. Syntype of S. alterniplicata MBM 280642. G. Holotype of S. corallina NHMUK 1977170. H–K. Syntypes of S. cochleariformis NHMUK 1981015. L. Reeve’s original figure for species 28. M–P. Comparisons of apical sculptures. M. Shell apex of S. alba shown for comparative reasons [M523]. N. Apex of S. corallina superimposed on S. japonica, Hong Kong, ZRC MOL 24904 [M404]. O. Shell apex of S. subatra AM C.584930 [SK349]. P. Apex of S. corallina superimposed on S. rucuana, Hong Kong ZRC 1999-20333 [M523]. Q. Animal of S. japonica. R. In situ S. Protoconch, AM C.585983 [SK339]. Unlabelled scale bars = 10 mm.