Echinolittorina marisrubri, Published, 2007

Reid, David G., 2007, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean, Zootaxa 1420 (1), pp. 1-161 : 17-23

Echinolittorina radiata (Souleyet in Eydoux & Souleyet, 1852)

( Figures 4 , 5 , 6A, B , 7 )

Littorina radiata Souleyet in Eydoux & Souleyet, 1852: 562, pl. 31, figs 46, 47 (Touranne, Cochinchine [Da Nang, Vietnam]; lectotype (Rosewater 1970) BMNH 1854.7.24.389, seen, Fig. 4 N; 2 paralectotypes MNHN, seen). Fischer, 1891: 171. Serène, 1937: 38.

Nodilittorina (Nodilittorina) radiata—Reid, 1989a: 100. Reid, 1992: 200–201, figs 1i (penis), 2h (oviduct), pl. 3d–h.

Nodilittorina (Granulilittorina) radiata— Kurozumi, 1994: 366, pl. 2, fig. 1.

Nodilittorina radiata— Mak, 1995: 53–59, figs 1b, 2b (spawn). Higo et al., 1999: 91. Hasegawa, 2000: 141, pl. 70, fig. 21. Reid, 2001 a: 440–441, figs 2D, E, 3F (penis). Reid, 2002a: 259 –281. Lee & Chao, 2003: 32, pl. 3, fig. 61. Thach, 2005: 54, pl. 8, fig. 28.

Echinolittorina radiata— Williams et al., 2003: 63, 83. Williams & Reid, 2004: 2227–2251.

Litorina exigua Dunker, 1860: 226–227 (Japan; lectotype (Rosewater 1970) Dunker, 1861: pl. 2, fig. 3). Dunker, 1861: 13, pl. 2, fig. 3. Dunker, 1882: 111. Weinkauff, 1882: 95–96, pl. 13, figs 13, 16 (in part; includes E. miliaris ).

Litorina (Tectaria) exigua — Weinkauff, 1883: 226.

Littorina exigua — Pilsbry, 1895: 61.

Nodilittorina (Granulilittorina) exigua — Rosewater, 1970: 500–502, pl. 386, figs 1-6, pl. 387 (map). Fujioka & Kurozumi, 1980: 51–54, fig. 1C.

Granulilittorina exigua — Kuroda et al., 1971: 58, pl. 16, figs 32–34. Higo, 1973: 47. Okutani, 1986: 70–71, figs. Choe, 1992: 291–291, fig. 83. Higo & Goto, 1993: 73.

Nodilittorina exigua — Ohgaki, 1985a: 462. Ohtsuka & Yoshioka, 1985: 232, fig. 4C, D (spawn). Ma, 2004: 33, fig. 12 (map, as N. pyramidalis in error) (in part, includes E. vidua ).

Littorina miliaris — Nevill, 1885: 154 (in part, includes E. natalensis ; not L. miliaris Quoy & Gaimard, 1833 = E. miliaris ).

Litorina (Hamus) granularis — Watson, 1886: 576–577 (not L. granularis Gray, 1839 = E. miliaris ). Pilsbry, 1895: 62 (not Gray, 1839).

Tectarius granularis — Tryon, 1887: 260, pl. 45, fig. 4 (in part, includes E. millegrana , E. miliaris , E. vidua , E. cinerea ; not Gray, 1839). Kuroda & Habe, 1952: 89 (not Gray, 1839). Hirase & Taki, 1954: pl. 79, fig. 10 (not Gray, 1839).

Littorina (Melarhaphe) granularis — von Martens, 1897: 206–207 (as Melarrhaphe ; in part, probably includes E. vidua , E. melanacme ; not Gray, 1839).

Littorina granularis — Yen, 1936a: 2–3 (not Gray, 1839). Yen, 1936b: 191, pl. 16, fig. 17 (not Gray, 1839).

Littorivaga (?) granularis — Kuroda, 1940: 102–102 (not Gray, 1839).

Littorina ( Littorivaga ?) granularis — Kuroda, 1941: 82, pl. 6, fig. 9 (not Gray, 1839).

Nodilittorina granularis — Habe, 1951: 92, pl. 14, figs 7, 8, 16 (not Gray, 1839). Habe, 1955: 206–207, figs 1, 2 (spawn) (not Gray, 1839). Habe, 1956b: 117–121, fig. C (spawn) (not Gray, 1839). Habe, 1958a: 8, pl. 1, fig. 8 (not Gray, 1839). Kojima, 1960: 118, fig. 1 (spawn) (not Gray, 1839). Kira, 1962: 22–23, pl. 12, fig. 24 (not Gray, 1839). Oyama & Takemura, 1963: Nodilittorina fig. 1 (not Gray, 1839).

Tectarius millegranus — Dautzenberg & Fischer, 1905: 151–152 (not Philippi, 1848).

Littorina ( Littorivaga ?) millegrana — Hirase, 1934: 47, pl. 79, fig. 10 (not Philippi, 1848).

Nodilittorina (Granulilittorina) millegrana — Rosewater, 1970: 491–494, pl. 380, figs 2, 3 (in part, includes E. melanacme , E. feejeensis , E. vidua , E. novaezelandiae , E. millegrana , E. reticulata ; not Philippi, 1848).

Taxonomic history: The specific name granularis was applied by Tryon (1887) to a group of at least five Echinolittorina species with granulose shells, but following Watson (1886) and Yen (1936a, b) this name became associated with the present species, and was widely used in the Japanese literature of the mid-twentieth century. However, as first noted by Rosewater (1970), L. granularis Gray, 1839 is a synonym of E. miliaris , endemic to Ascension Island in the southeastern Atlantic. (The type of L. granularis in BMNH is a worn shell without locality, but shows the characteristic sculpture of E. miliaris and the two white apertural bands present in most non-Indo-West-Pacific members of the genus.) Accordingly, Rosewater (1970) revived the name N. exigua for the present species, distinguishing it from a complex of six species under the name N. millegrana . This distinction was based on shell characters alone and was unclear; furthermore the lectotype of L. radiata was figured as a member of the latter group. Among the members of the conchologically similar E. millegrana group, E. radiata is only commonly sympatric with E. vidua , and their separation (but under different names) was already well recognized (e.g. Yen 1936a, b; Kuroda 1941; Habe 1951). Their diagnostic shell characters were further discussed by Ohgaki (1985a). The priority of the name radiata was pointed out by Reid (1989a) and the name and identity of the species established by subsequent redescriptions (Reid 1992, 2001a).

Diagnosis: Shell turbinate; 5–8 granulose ribs at and above periphery, single thread between each rib, granules not aligned in axial series; white with faint fine brown marbled pattern. Japan, Korea, China, Vietnam. COI: GenBank AJ623039 , AJ623040 .

Material examined: 87 lots (including 13 penes, 7 sperm samples, 19 pallial oviducts, 9 radulae).

Shell ( Fig. 4 ): Mature shell height 4.4–12.8 mm. Shape high turbinate (H/B = 1.19–1.51, SH = 1.36– 1.69); spire whorls rounded, suture distinct; spire profile straight; periphery of last whorl weakly angled at periphery and sometimes also at shoulder. Columella concave, hollowed and slightly pinched at base; eroded parietal area; often an imperforate pseudumbilical area adjacent to columella; often a slightly produced anterior lip to aperture. Sculpture of last whorl: 5–8 strongly or weakly granulose ribs at and above periphery; granular sculpture not usually aligned in axial series; ribs usually subequal, but peripheral rib and shoulder rib may be slightly more prominent ( Fig. 4E, J ); single thread between each rib (rarely two or none); spiral microstriae cover entire surface; base with 4–8 ribs; surface usually eroded. Protoconch 0.28–0.30 mm diameter, 2.9 whorls. Colour: dirty white, fawn or pale blue-grey, spire whorls blue-grey to purple-brown; pattern usually faint, sometimes absent, brown marks between granules on ribs, brown marbling over whole surface in darkest shells, but with cream spiral line on base and another adjacent to columella; aperture brown with pale band at base; columella brown.

Animal ( Fig. 5 ): Head ( Fig. 5K–M ) black, with or without unpigmented stripe across snout, tentacle pale around eye, with two longitudinal black lines (sometimes only lower line present); sides of foot grey to black. Opercular ratio 0.46–0.54. Penis ( Fig. 5A–E ): filament stout, lower half wrinkled and not clearly differentiated from wrinkled base, smooth tip bluntly triangular, filament 0.5–0.6 total length of penis, sperm groove ends subterminally; mamilliform gland and glandular disc of similar size, borne on short projection of base; penis unpigmented, or slightly pigmented at base. Euspermatozoa 66–84 µm; paraspermatozoa ( Fig. 5I, J ) spherical to slightly oval, 11–14 µm diameter, containing 1–3(4) rectangular rod-pieces, equal to or shorter than cell diameter, hexagonal in section, and large distinct granules. Pallial oviduct ( Fig. 5F, G ): distal part swollen and bent back beneath straight section; bursa opening near swollen part and extending back to albumen gland. Spawn ( Fig. 5H ) an asymmetrically biconvex pelagic capsule 200–244 µm diameter (160 µm, Habe 1955) with broad peripheral rim, cupola-shaped upper side sculptured by 5–7 concentric rings (Kojima 1960, illustrated a probably aberrant capsule with 3 rings), containing single ovum 50–78 µm diameter (Habe 1955, 1956b; Kojima 1960; Ohtsuka & Yoshioka 1985; Mak 1995). Development predicted to be planktotrophic.

Radula ( Fig. 6A, B ): Relative radula length 2.80–6.49. Rachidian: length/width 1.14–1.42; tip of major cusp rounded. Lateral and inner marginal: major cusp on each of similar size, tips blunt to rounded. Outer marginal: 6–8 cusps.

Range ( Fig. 7 ): Japan, Korea, China, Taiwan, Vietnam. Range limits: Shakotan, Hokkaido, Japan (Ohgaki 1983b); Shimamaki, Hokkaido, Japan (BMNH); Hakodate, Hokkaido, Japan (USNM 276842); Kuroshima, Kagoshima Pref., Japan (Uozumi Colln); Yahazu, Yaku-shima, Kagoshima Pref., Japan (BMNH); Akuseki-jima, Tokara Is, Japan (Kurozumi 1994); Senkaku Is, Japan (Fujioka & Kurozumi 1980); Sokcho, S. Korea (Song et al. 2000); Pusan, S. Korea (BMNH); Inchon, S. Korea (Song et al. 2000); Yantai, near Qingdao, China (BMNH 20030893, ZISP); Tiaoshi, 20 km NW Keelung, Taiwan (BMNH); Longkang, Oluanpi Peninsula, Taiwan (BMNH); Do Son, Hai Phong, Vietnam (BMNH 20030897; MNHN); Nha Trang, Vietnam (BMNH 20010355).

The species appears to occur all around the Yellow Sea; Ma (2004) records it from the entire Chinese coast and Song et al. (2000) from localities in South Korea. The species is rare at Nha Trang, Vietnam, and in the south of Taiwan. On Hokkaido it is common only at the southern tip (Ohgaki 1983b). It is apparently absent from most of the Ryukyu Island chain (absence from Ishigaki noted by Ohgaki 1998), occurring only in the north up to 220 km from the mainland of Kyushu (Kurozumi 1994) and in the south in the Senkaku Islands 150 km northeast of Taiwan (Fujioka & Kurozumi 1980). (A single collection from ‘Okinawa’, NSMT 41643, is probably unreliable.) It is also absent from the Ogasawara Islands. It is therefore a species of continental habitats, absent from oceanic islands.

Habitat and ecology: Juveniles can be found among barnacles in the eulittoral zone, but adults extend upwards into the lower littoral fringe. Substrates include granite, basalt, slate, sandstone, limestone and concrete and the species occurs on both sheltered and exposed coastlines.

Various aspects of the ecology and behaviour of this species have been studied. Its zonation has been described in Hong Kong (Ohgaki 1985a; Williams 1994), China (Fan 1981; Morton 1990; You 1990), Korea (Lee & Hyun 1997) and throughout Japan (Ohgushi 1956; Habe 1958b; Yajima & Kosaka 1979; Tsuchiya 1979; Ohgaki 1985b, c, 1988b; Tanaka et al. 1985). In Hong Kong it is zoned at and above mean high water of spring tides; this is below and in the lower part of the range of E. malaccana and above the level of Littorina brevicula (Ohgaki 1985a; Williams 1994). Field manipulations indicate that competitive interactions between these three littorinids may influence their relative zonation (Dudgeon & Yipp 1986). Compared with the others, E. radiata has only a modest desiccation resistance, showing 50% survival after 31 days (Yipp et al. 1986). Likewise, in Japan it usually occupies a level above L. brevicula (Ohgushi 1956) . At Tanabe Bay in southern Honshu it occurs below E. cecillei and above E. vidua , and occupies both sheltered and exposed sites (Habe 1958b). Vertical zonation is related to the height of waves and shows seasonal variation (Ohgaki 1989). On each tide the animals migrate vertically to remain in the splash zone (Hukuda 1950; Ohgaki 1985c; Kato 1985, 1986a, b) and the vertical range is restored following dislodgement by rain (Ohgaki 1988b). At high tidal levels there may be long periods of quiescence and activity is stimulated by rain (Britton & McMahon 1992).

The breeding season is extended in the southern parts of the range. Spawning occurs in July and August at Asamushi in the north of Honshu (Kojima 1958a, 1960; Hirai 1963). At Shirahama it spawns from mid-June to early September, and egg release is associated with strong waves and high tide, rather than the lunar phase (Ohgaki 1981). In Hong Kong the spawning season lasts from April to October (Mak 1998). Recruits appear in the lower part of the vertical range and mean size of snails is larger at higher levels (Ohgaki 1985b; Tanaka et al. 1985). Mature animals of both sexes and also immature individuals are found at lower levels during the summer, so this migration may be related to feeding or avoidance of environmental stress, rather than spawning (Ohgaki 1988a; Ito et al. 1998). In Hong Kong E. radiata grazes the epilithic biofilm of cyanobacteria (Mak & Williams 1999). Radular length decreases in summer at lower tidal levels as a consequence of increased foraging activity (Ito et al. 2002). Growth rate has been recorded in Hokkaido (Miyamoto et al. 1995), and the relation between total weight, body and shell weight measured (Tokeshi et al. 2000). The frequency of mucus attachment to the substrate at the outer lip has been studied by Wada & Ito (2000).

Remarks: Unusually in the genus Echinolittorina , the distribution of E. radiata lies almost entirely outside tropical latitudes. Under the influence of the warm Tsushima Current in the Japan Sea and the Kuroshio Current flowing up the east coast of Japan, it extends to 43°N in Hokkaido. This is a continental species, absent from the Ryukyu and Ogasawara Islands where marine productivity is low. Phylogeography has been examined in Korea using cytochrome- b sequence data (Song et al. 2000).

Superficially the granulose shell resembles those of the members of the E. millegrana group, but E. radiata does not possess the unique tentacle coloration of that group, nor the curved paraspermatozoan rod-pieces of most of its members. Molecular data do not support a relationship with any other species within the Indo-Pacific radiation (Williams & Reid 2004).

Of the few sympatric species, confusion is only possible with E. vidua ; the shell of E. radiata differs from that of E. vidua (Fig. 59) in its slightly taller spire, profile often slightly angled at periphery and shoulder (rounded in E. vidua ), usually larger and coarsely granulose ribs with single thread between (finer and more numerous ribs and granules in E. vidua ), dirty white colour sometimes with indistinct brown pattern (often distinct brown stripes and tessellation in E. vidua ), slightly produced anterior lip of aperture (rounded in E. vidua ), brown columella and lip (brown columella, but white anterior and inner apertural lip in E. vidua ); the penis, paraspermatozoa, oviduct, egg capsules and head pigmentation are all clearly different in these two species ( Figs 5 , 60). There is also an ecological difference; in Hong Kong only E. radiata is found on the sheltered shore of Tolo Harbour, whereas both occur on exposed coasts (Ohgaki 1985a). In this respect, and in its geographical distribution (e.g. on the Ryukyu Islands) E. vidua is a more oceanic species than E. radiata . This species occurs with others ( E. melanacme , E. tricincta , E. reticulata ) in Taiwan, and with E. melanacme in Vietnam, but confusion should not occur.

Figures

FIGURE 2. Terminology of Echinolittorina shells and radulae. A. E. malaccana. B. E. tricincta. C. E. reticulata. D. E. novaezelandiae. E. Radula of E. pascua in flat view.

FIGURE 4. Echinolittorina radiata. A, Hoi Ha, Mirs Bay, Hong Kong (BMNH 20030888). B, G, Cat Ba Bay, Ha Long Bay, Vietnam (BMNH 20030889). C, O, Otsu, Ibaraki, Japan (BMNH 20030890). D, P, Nogita, Kyushu, Japan (BMNH 20030891). E, J, Haikou, Hainan I., China (BMNH 20030892). F, Yantai, Qingdao, China (BMNH 20030893). H, I, Sai Kung, Hong Kong (BMNH 20030894). K–M, Tsutsu, Tsushima I., Japan (BMNH 20030895). N, Littorina radiata Souleyet, in Eydoux & Souleyet, 1852, lectotype, Touranne, Cochinchine [Da Nang, Vietnam] (BMNH 1854.7.24.389).

FIGURE 5. Echinolittorina radiata. A–E, penes. F, G, pallial oviduct. H, pelagic egg capsule (after Mak, 1995). I, J, paraspermatozoa. K–M, heads. A–C, I, Asamushi, Honshu, Japan (BMNH 20030896; A, B, lateral and medial views of same specimen; shell H A, B = 7.5 mm, C = 7.0 mm). D, Do Son, Hai Phong, Vietnam (BMHH 20030897; shell H = 6.5 mm). E, K–M, Sai Kung, Hong Kong (BMNH 20030894; shell H E = 5.0 mm, K = 5.3 mm, L = 6.4 mm, M = 6.6 mm). F, G, Nejiko, Hirado I., Kyushu, Japan (BMNH 20030898; lateral and medial views of same specimen; shell H = 9.1 mm). H, Hong Kong. J, Aberdeen, Hong Kong (BMNH 20030899). Shading conventions as in Figure 3.

FIGURE 6. Radulae of Echinolittorina species (two views of each radula, flat and at 45°). A, B, E. radiata; Kinkasan I., Miyagi Pref., Japan (BMNH 20050563; shell H = 8.7 mm). C, D, E. arabica; Hamriya, Sharjah (BMNH 20030871; shell H = 8.4 mm). E, F, E. marisrubri new species, paratype; Port Safaga, Egypt (BMNH 20030886; shell H = 10.6 mm). G, H, E. omanensis new species, paratype; Wadi Sayq, Jabal Qamr, Dhofar, Oman (BMNH 20040220; shell H = 14.2 mm). Scale bars = 50 µm.

FIGURE 7. Distribution of Echinolittorina radiata. Literature records: A, Fujioka & Kurozumi (1981); B, Kurozumi (1994); C, Ma (2004); D, Ohgaki (1983b); E, Song et al. (2000).