Echinolittorina arabica (El Assal, 1990)

Reid, David G., 2007, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean, Zootaxa 1420 (1), pp. 1-161 : 24-28

Echinolittorina arabica (El Assal, 1990)

( Figures 6C, D , 8 , 9 , 10 )

Nodilittorina (Granulilittorina) subnodosa — Rosewater, 1970: 495–496, pl. 383, figs 4–6, pl. 383a (map) (in part, includes E. subnodosa , E. marisrubri ; not Philippi, 1847).

Nodilittorina subnodosa — Biggs, 1973: 355 (not Philippi, 1847).

Nodilittorina arabica El Assal, 1990: 293–298 , figs 2, 3 (operculum), 5 (radula), 6 (penis) ( Arabian Gulf , Saudi Arabia [restricted to Ras Met’eb, Dammam, Saudi Arabia, the locality of the syntypes]; lectotype BMNH 1990089/1 (here designated, Fig. 8L ) and paralectotype BMNH 1990089/2, seen; 4 lectotypes in alcohol, BMNH 1990089/3–6, seen). Reid, 2002a: 259–281 (in part, includes E. marisrubri ).

Nodilittorina (Nodilittorina) arabica — Bosch et al., 1995: 45, fig. 115.

Echinolittorina arabica — Williams et al., 2003: 83 (in part, includes E. marisrubri ).

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

Taxonomic history: Rosewater (1970) considered specimens from the Persian Gulf to be smooth variants of E. subnodosa , and this taxonomy was followed for 20 years. Anatomical study during a larger project (Reid 1989a) indicated that E. subnodosa was distinct from the E. arabica group, although specimens from the Red Sea and Persian Gulf were not then separated. El Assal (1990) made unacknowledged use of information provided by Reid and proceeded to name the species from the Persian Gulf, without any anatomical comparison and making no mention of the similar specimens from the Red Sea. Thereafter, E. arabica was considered to occur in both the Persian Gulf and Red Sea (Bosch et al. 1995; Dekker & Orlin 2000; Reid 2002a) and the sister species of the E. arabica group were only separated following molecular study (Williams & Reid 2004).

Diagnosis: Shell turbinate; smooth with 16–22 minutely granulose threads at and above periphery and rugose suture, or granulose with 2–5 rows of granules at and above periphery; colour grey, cream, orange, brown or black. Persian Gulf and Gulf of Oman. COI: GenBank AJ622981 , AJ622982 .

Material examined: 54 lots (including 13 penes, 2 sperm samples, 6 pallial oviducts, 4 radulae).

Shell ( Fig. 8 ): Mature shell height 5.4–13.9 mm. Shape turbinate to conical (H/B = 1.20–1.53; SH = 1.47–2.11); spire whorls lightly rounded to almost flat, suture distinct; spire profile slightly convex, concave at apex; periphery of last whorl weakly angled. Columella short, concave, slightly hollowed at base; no eroded parietal area; sometimes a pseudumbilicus in large shells. Sculpture granulose, nodulose, rugose or smooth; last whorl of strongly sculptured shells ( Fig. 8A–F, H ): 2–5 rows of granules or nodules, usually most prominent at periphery and shoulder, with granulose threads between; smooth shells ( Fig. 8G, I–L ) with up to16–22 fine minutely or indistinctly granulose threads above periphery; suture and adjacent posterior part of last whorl often coarsely rugose; spiral microstriae cover entire surface, but surface often eroded; base with 5–12 threads or weakly granulose ribs. Protoconch 0.26–0.29 mm diameter, 2.6–2.8 whorls. Colour: pale grey, cream, orange, brown or black, sometimes with broad dark band in middle of whorl and another on base; pattern usually absent, but sometimes a faint spiral pattern of brown marks between granules; aperture brown with pale band at base; columella white.

Animal ( Fig. 9 ): Head grey to black, with or without unpigmented stripe across snout, tentacle pale around eye, with two longitudinal grey to black lines; sides of foot grey to black. Opercular ratio 0.47–0.59. Penis ( Fig. 9A–G ): filament strap-shaped to pointed, sometimes slightly narrowed at base, filament 0.6–0.8 total length of penis, sperm groove extends to tip; mamilliform gland and glandular disc of similar size, borne on short projection of base; penis unpigmented or slightly pigmented at base. Euspermatozoa not known; paraspermatozoa ( Fig. 9J, K ) oval, with 1–2 rod-pieces 14–26 µm, usually one rod-piece strongly projecting and slightly curved, the other shorter and not projecting; cytoplasm filled with large round granules. Pallial oviduct ( Fig. 9H, I ): bursa opening at midpoint of straight section and extending back to albumen gland. Spawn not known. Development predicted to be planktotrophic.

Radula ( Fig. 6C, D ): Relative radula length 2.36–3.92. Rachidian: length/width 1.45–1.70; tip of major cusp pointed. Lateral and inner marginal: major cusp on each of similar size, tips rounded. Outer marginal: 5 cusps.

Range ( Fig. 10 ): Persian Gulf and Gulf of Oman. Range limits: Kuwait (BMNH 20030878); Bushire, Iran (USNM 679285); Ras Mushayrib, United Arab Emirates (BMNH); Hormuz I., Iran (BMNH 20030873); Fujaira, United Arab Emirates (BMNH 20030874); Al Bustan, E of Muscat, Oman (ZMA); Ras al-Hadd, Oman (BMNH 20030872). The southern range limit at Ras al-Hadd and absence from the Arabian Sea coast of the Arabian Peninsula are probably correct, for E. arabica has not been found among the 34 samples of other Echinolittorina species available from between Masirah and Aden.

Habitat and ecology: Echinolittorina arabica occurs on a wide range of hard substrates in the uppermost eulittoral zone and low littoral fringe, but always in sheltered situations. It has been recorded on limestone, beachrock and concrete sea walls. It can be found on the trunks and pneumatophores of the mangrove Avicennia and among saltmarsh plants, and may crawl over firm sand and mud surfaces at low tide (G.R. Feulner, pers. comm.). It is abundant on the extensive black cyanobacterial mats (‘sabkas’) of the Gulf coast of the United Arab Emirates (Biggs 1973). It tolerates salinity of up to 50 ppt and water temperatures of up to 34°C (Biggs 1973).

Remarks: The shell of this species is among the most variable in the genus, ranging from coarsely granulose to smooth. Although available samples differ in their degree of sculpture, it is unclear whether there is any correlation with habitat type. Extremes of sculpture can be found in the same microhabitat (e.g. Fig. 8F and G together in the same mangrove habitat). The great majority of shells are of the smooth type. Despite the sheltered environment, the shells from the cyanobacterial mats on tidal flats of the southern Persian Gulf are of considerable thickness and curiously eroded ( Fig. 8H–K ). In addition, this species is extremely variable in colour and some samples are polymorphic, varying from black to orange or cream. Most samples from the black cyanobacterial mats have black to brown shells, as do those from mangroves, whereas samples from rock substrates are paler brown to orange (BMNH; G.R. Feulner and R. Hornby pers. comm.); this might imply an ecophenotypic effect through diet, or visual selection, and deserves further study. G.R. Feulner (pers. comm.) has suggested that crab predation plays an important role in determining the abundance of this species in the eastern Persian Gulf and Oman. Evidence of damage by crabs can sometimes be seen on the shells, and the shells can be remarkably solid ( Fig. 8J, K ).

Molecular data indicate that E. arabica and E. marisrubri are sister taxa (Williams & Reid 2004) with a close relationship (K2P genetic distance for COI = 6.24%). The geographical range of E. arabica is restricted to the sheltered and relatively eutrophic shores of the Persian and Oman Gulfs. Its absence from the Arabian Sea coast of Oman and Yemen (and perhaps the separation of these sister species) may be attributed to the stronger exposure, or to the summer upwelling that reduces temperatures and imposes a strongly seasonal nutrient regime (Wilson 2000). During low sea-level stands of glacial intervals the Persian Gulf dried out over most of its extent (Sheppard et al. 1992), so that recolonization of this part of the range must have taken place during the Holocene. The ability to live on mangroves and algal mats, and to crawl on mud and sand, are highly unusual in the genus Echinolittorina , and unknown in other IWP species.

There are no obvious anatomical differences between E. arabica and E. marisrubri ; details of the pallial oviduct, the shape of the penis, the curved rods of the paraspermatozoa, and the 5–6 cusps of the outer marginal teeth, are all similar. However, shells of the two are almost always distinct. Typically, those of E. arabica are turbinate with rounded whorls, usually smooth with 16–22 minutely granular threads at and above the periphery ( Fig. 8G, I–L ), sometimes rugose ( Fig. 8E, H ) or occasionally with 2–5 rows of small nodules ( Fig. 8A–C ). In contrast, shells of E. marisrubri are more conical with flatter whorls, bearing three rows of nodules and a beaded rib between each row, and brown to black shells are not known ( Fig. 11A, G–I ). Rare weakly sculptured shells of E. marisrubri have only eight beaded ribs at and above the periphery ( Fig. 11D ). Difficulty may be experienced with some of the most nodulose forms of E. arabica ( Fig. 8C, D, F ) that are similar to moderately nodulose E. marisrubri ( Fig. 11B, C, E ); in the latter there remain fewer ribs (8–13 at and above periphery), and it is the peripheral row of nodules that is largest, whereas in E. arabica the shoulder nodules are largest. Although nuclear genetic data are limited, these shell differences support the recognition of two distinct species. Furthermore, there may be an ecological difference, because the range of E. marisrubri extends into the oligotrophic northern Red Sea.

In the Persian Gulf and Gulf of Oman E. arabica is broadly sympatric with E. millegrana . The latter species predominates in more exposed microhabitats and localities, and its shells can resemble those of granulose forms of E. arabica . The shell of E. millegrana is almost always white, the rounded whorls lack peripheral and shoulder angulation, and the surface is more uniformly granulose (Fig. 72).

Figures

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 8. Echinolittorina arabica. A, B, Hamriya, Sharjah (BMNH 20030871). C, Ras al-Hadd, Oman (BMNH 20030872). D, Hormuz, Iran (BMNH 20030873). E, Fujairah, United Arab Emirates (BMNH 20030874). F, G, Ras al- Khaimah Khor, United Arab Emirates (BMNH 20030875). H, I, United Arab Emirates (BMNH 20030876). J, K, Khor al-Bazm, United Arab Emirates (BMNH 20030877). L, Nodilittorina arabica El Assal, 1990, lectotype, Ras Met’eb, Dammam, Saudi Arabia (BMNH 1990089/1).

FIGURE 9. Echinolittorina arabica. A–G, penes. H, I, pallial oviducts. J, K, paraspermatozoa. A, Kuwait (BMNH 20030878; shell H = 7.8 mm). B–D, J, K, Dubai, United Arab Emirates (BMNH 20030879; shell H B = 6.6 mm, C = 7.0 mm, D = 7.3 mm). E, Ghemeis Peninsula, Abu Dhabi, United Arab Emirates (BMNH 20030880; shell H = 7.6 mm). F, Fujaira, United Arab Emirates (BMNH 20030881; shell H = 7.7 mm). G, Ras al-Khaimah Khor, United Arab Emirates (BMNH 20030875; shell H = 8.4 mm). H, Hamriya, Sharjah, United Arab Emirates (BMNH 20030871; shell H = 7.7 mm). I, Al Bustan, Muscat, Oman (ZMA; shell H = 9.2 mm). Shading conventions as in Figure 3.

FIGURE 10. Distribution of Echinolittorina arabica (solid circles) and E. marisrubri (open circles).

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).