Echinolittorina subnodosa (Philippi, 1847)

Reid, David G., 2007, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean, Zootaxa 1420 (1), pp. 1-161 : 41-44

Echinolittorina subnodosa (Philippi, 1847)

( Figures 15E, F , 16 , 19 , 20 )

Litorina subnodosa Philippi, 1847a : vol. 2: 161, Litorina pl. 3, figs 8, 9 (Mare Rubrum [Red Sea]; lectotype (Rosewater 1970) Philippi, 1847a, Litorina pl. 3, fig. 9 ( Fig. 19H herein); 3 paralectotypes ZMB 2395, seen). Weinkauff, 1882: 93–94, pl. 13, figs 10, 11.

Tectarius subnodosus — H. Adams & A. Adams, 1854: 315.

Littorina subnodosa — Reeve, 1857: sp. 10, pl. 2, fig. 10. Issel, 1869: 191.

Littorina (Nodilittorina) subnodosa — von Martens, 1897: 205.

Nodilittorina (Granulilittorina) subnodosa — Rosewater, 1970: 495–496, pl. 383, figs 1–3, pl. 383a (map) (in part, includes E. arabica , E. marisrubri ).

Nodilittorina (Nodilittorina) subnodosa — Reid, 1989a: 100.

Nodilittorina subnodosa — Reid, 2002a: 259–281.

Echinolittorina subnodosa — Williams et al., 2003: 83.

Echinolittorina subnodosa A—Williams & Reid, 2004: 2227–2251.

Litorina nodosa — Weinkauff, 1883: 226 (in part, includes E. australis , E. natalensis , E. malaccana group; not Gray, 1839 = E. australis ).

Tectarius nodosus — Tryon, 1887: 259, pl. 47, fig. 65 (in part, includes E. australis , E. natalensis , E. miliaris ; not Gray, 1839). Moazzo, 1939: 183 (not Gray, 1839).

Tectarius armatus — Safriel & Lipkin, 1964: 187 (not Tectaria armata Issel, 1869 = Perrinia stellata A. Adams, 1864 , Trochidae ).

Nodilittorina (Nodilittorina) natalensis — Sabelli & Taviani, 1984: 95–100, pl. 1 (radula, penis), figs 1, 2 (not Krauss in Philippi, 1847).

Nodilittorina natalensis — Verbinnen & Dirkx, 2005: 111–112, fig. 4 (not Krauss in Philippi, 1847).

Nodilittorina tuberculata — Sharabati, 1984: pl. 6, figs 5, 5a (not Litorina tuberculata Menke, 1828 = E. tuberculata ).

Taxonomic history: The paralectotypes in ZMB were collected by Hemprich & Ehrenberg in the Red Sea (also the source of Philippi’s type material of E. millegrana ) and includes two labels in Philippi’s hand. These three shells resemble Philippi’s (1847a) fig. 8, but none is the figured shell. Confusion with E. natalensis and nodulose forms of the Australian species E. australis may be explained by a similar broad shape and three rows of nodules (Weinkauff 1883, as Litorina nodosa ; followed by Tryon 1887). Following Rosewater (1970) the species was distinguished from these two, but united with E. arabica and E. marisrubri . Sabelli & Taviani (1984) and Verbinnen & Dirkx (2005) separated the two nodulose species in the Red Sea, E. subnodosa and E. marisrubri , but under the names N. natalensis and N. subnodosa respectively, while Sharabati (1984) used N. tuberculata (a western Atlantic species) and N. subnodosa .

Diagnosis: Shell conical, 3 rows of pointed nodules on last whorl, nodules occupying width of one rib only, so not crossed by spiral ribs; 25–31 spiral ribs on last whorl (including base); grey, a brown spiral line connecting each row of white nodules. Red Sea. COI: GenBank AJ623045 , AJ623046 .

Material examined: 25 lots (including 7 penes, 2 sperm samples; 6 pallial oviducts, 2 radulae).

Shell ( Fig. 19 ): Mature shell height 8.1–18.7 mm. Shape conical (H/B = 1.16–1.40; SH = 1.35–1.68); spire whorls lightly rounded, suture distinct; spire profile concave at apex; periphery of last whorl weakly angled. Columella short, concave, hollowed at base; eroded parietal area small or absent. Sculpture of last whorl: 3 rows of pointed nodules at periphery, mid-whorl and shoulder, not axially aligned, numbering 13-19 at periphery; rarely an additional row of small nodules near suture; nodules sometimes become obsolete towards end of last whorl, remaining only as enlarged ribs; rarely entire shell lacks nodules ( Fig. 19B, C ); entire surface with narrow spiral ribs, 16–21 at and above periphery, and microstriae; nodules occupy width of one rib only, so are not crossed by spiral ribs; base with 9–11 ribs, of which up to 4 may be nodulose. Protoconch 0.25–0.27 mm diameter, 2.1–2.2 whorls. Colour: cream to grey, darker grey between shoulder and middle of base; nodules white, each of the 3 major rows connected by a dark brown spiral line; smoother shells sometimes with diffusely marbled or axially zigzag brown pattern; rarely entirely cream or entirely blackbrown ( Fig. 19B, C ); aperture brown, external spiral lines showing through, with pale band at base; columella purple-brown.

Animal ( Fig. 20 ): Head ( Fig. 20G ) grey to black, no unpigmented stripe across snout, tentacle pale around eye and across base, with two longitudinal grey lines extending almost to tip; sides of foot grey to black. Opercular ratio 0.46–0.56. Penis ( Fig. 20A–D ): filament gradually tapering to pointed tip, with fine annular wrinkles for most of its length, filament 0.6–0.7 total length of penis, sperm groove extends to tip; mamilliform gland about half size of glandular disc, borne together on projection of base; penis unpigmented or slightly pigmented at base. Euspermatozoa 107–110 µm; paraspermatozoa ( Fig. 20E ) spherical to oval, 9– 16 µm diameter, filled with large round granules, containing single short rectangular, oval or irregular rodpiece, hexagonal in section and not projecting from cell. Pallial oviduct ( Fig. 20F ): bursa opening at one third to one half length of straight section (from anterior) and extending back to albumen gland. Development predicted to be planktotrophic.

Radula ( Fig. 15E, F ): Relative radula length 2.86–4.96. Rachidian: length/width 1.90–2.25; tip of major cusp pointed. Lateral and inner marginal: tips of major cusps rounded; major cusp of lateral slightly larger than that of inner marginal. Outer marginal: 6–8 cusps.

Range ( Fig. 16 ): Red Sea. Range limits: Suez, Egypt (BMNH 1870.12.26.20); Eilat, Israel (USNM 709145); Jeddah, Saudi Arabia (BMNH); Massawa, Eritrea (IRSNB). Restriction to the Red Sea is likely to be correct, because of the numerous records of other Echinolittorina species from the Gulf of Aden. The lack of records from the southeastern Red Sea is surprising in view of the five records of E. marisrubri and E. millegrana from the Red Sea coast of Yemen, and may indicate a real absence.

Habitat: The habitat includes substrates of coral limestone, beachrock and concrete in the littoral fringe.

Remarks: Throughout most of its range this species occurs in the low nutrient regime characteristic of most of the Red Sea and is therefore considerd to be an oceanic species; only the southernmost record, from Massawa (IRSNB), lies in the part of the Red Sea that is influenced by influx of nutrient-rich water from the Gulf of Aden (Sheppard 2000).

Sequence data from the mitochondrial COI gene show that the sister species of E. subnodosa is E. omanensis (Williams & Reid 2004) , with a K2P genetic distance of 10.9%. Depending upon the calibration used, this corresponds to an age of separation of 2.3 or 4.2 Ma. During the glacial intervals of the Plio-Pleistocene the Red Sea became partly isolated, hypersaline and uninhabitable by most marine organisms, and the most recent recolonization began only about 15000 years ago (Sheppard et al. 1992; Siddall et al. 2003). Although the present distributions of this pair appear to be separated at the mouth of the Red Sea, their speciation therefore cannot be related to recent recolonization and differentiation. The modern distributions of E. subnodosa and E. omanensis suggest that they are isolated by their ecological requirements (for oceanic and upwelling conditions, respectively), and this may have played a role in their speciation. During glacial intervals the strength of the monsoon-driven upwelling on the southern Arabian coast was reduced (Sheppard et al. 1992), and this may have permitted E. subnodosa to survive in a refugium in the Gulf of Aden, outside its present range. Meanwhile, the extent of E. omanensis may have been correspondingly restricted, maintaining the separation between them. A similar geographical pattern is shown by the likely sister-species pair Peasiella isseli (Semper in Issel, 1869) and Peasiella mauritiana (Viader, 1951) , the former limited to the Red Sea and Aden, while the latter is widespread in the western Indian Ocean (Reid & Mak 1998).

Of the seven species of Littorinidae recorded from the Red Sea (Reid 1986a, 2001b, herein; Reid & Mak 1998), four are endemic to the Red Sea and Arabia ( E. marisrubri , E. subnodosa , E. millegrana , Peasiella isseli ), of which three are restricted to the Red Sea and Aden. Although the details of these patterns differ and their likely causes are varied, this emphasizes the distinct ecology and biogeographic history of the Arabian region and its components (Sheppard et al. 1992).

This species is readily distinguished from the others of the E. natalensis group in the western Indian Ocean ( E. natalensis , E. omanensis ) by its broader shell, with three widely-spaced rows of small nodules (the nodules occupying the width of one rib, and therefore not crossed by spiral sculpture) and a pattern of three spiral brown lines. These three species are not know to occur sympatrically and there are no obvious anatomical differences among them. In the Red Sea E. marisrubri is a similar species ( Fig. 11 ) with three rows of nodules, but the shell is smaller, there is a beaded rib between each row of nodules, and the nodules at the periphery are crossed by two spiral threads; penial anatomy and paraspermatozoa differ.

Figures

FIGURE 11. Echinolittorina marisrubri new species. A, Little Aden, Yemen (BMNH 20030882). B, C, Safaga, Egypt (NNML). D, Eilat, Israel (BMNH 20030883). E, H, Red Sea (BMNH 20030884). F, paratype (BMNH 20030886). G, holotype, Port Safaga, Egypt (BMNH 20030885). I, Hind Kadam, Sudan (BMNH 1891.1.31.49).

FIGURE 15. Radulae of Echinolittorina species (two views of each radula, flat and at 45°). A–D, E. natalensis. A, B, Libanona Beach, Tolagnaro, Madagascar (BMNH 20030691; shell H = 8.9 mm). C, D, Tiwi Beach, Kenya (BMNH 20040209; shell H = 9.0 mm). E, F, E. subnodosa; El-Qalawi, 30.5 km S Port Safaga, Egypt (BMNH 20040229; shell H = 14.2 mm). G,H, E. pascua; Hanga Tee, Easter I. (BMNH 20040232; shell H = 14.0 mm). Scale bars = 50 µm.

FIGURE 16. Distribution of Echinolittorina natalensis (open circles), E. omanensis (solid circles) and E. subnodosa (open triangles). Literature records: A, Kilburn (1972); B, Melvill & Standen (1901).

FIGURE 19. Echinolittorina subnodosa. A, no locality [Red Sea] (BMNH 20040224). B, C, Hammam-Fara’un, Gulf of Suez, Egypt (BMNH 20040225). D–F, Mukawwar I., Sudan (BMNH 20040226). G, I, S of Port Sudan Harbour, Sudan (BMNH 20040227). H, Litorina subnodosa Philippi, 1847, lectotype figure, Red Sea (Philippi, 1847, Litorina pl. 3, fig. 9). J, no locality [Red Sea] (BMNH 20040228).

FIGURE 20. Echinolittorina subnodosa. A–D, penes. E, paraspermatozoa. F, pallial oviduct. G, head. A, El-Qalawi, 30.5 km S Port Safaga, Egypt (BMNH 20040229; shell H = 12.5 mm). B, C, F, Mukawwar I., Sudan (BMNH 20040226; shell H B = 13.0 mm, C = 12.3 mm, F = 13.1 mm). D, E, G, Ras Mohammed, S Sinai, Egypt (BMNH 20040230; shell H = 10.3 mm). Shading conventions as in Figure 3.