Echinolittorina natalensis (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 : 31-37

Echinolittorina natalensis (Krauss in Philippi, 1847)

( Figures 13 , 14 , 15A–D , 16 )

Litorina natalensis Krauss in Philippi , 1847a: vol. 2: 160, Litorina pl. 3, fig. 4 (Ora Natal in Africa australi [coast of Natal, South Africa]; lectotype (Janus 1961: pl. 3, figs 7, 8) SMNS ZI0050942 ( Fig. 13M ), seen; 13 paralectotypes SMNS ZI0050943, not seen; 17 probable paralectotypes SMNH 4971; 2 additional ex Krauss lots SMF (Herbert & Warén 1999), not seen; additional ex Krauss material possibly in NNML (van Bruggen 1992), not seen). Krauss, 1848: 102. Weinkauff, 1882: 92–93, pl. 13, figs 6, 7.

Tectarius natalensis — H. Adams & A. Adams, 1854: 315. Bartsch, 1915: 120. Dautzenberg, 1932: 61. Barnard, 1963: 191, fig. 37b (radula), 37c. Kensley, 1973: 66, fig. 202.

Littorina natalensis — Reeve, 1858: sp. 102, pl. 18, fig. 102a, b.

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

Tectarius (Nodilittorina) natalensis — Janus, 1961: 7, pl. 3, figs 7, 8.

Nodilittorina (Nodilittorina) natalensis — Rosewater, 1970: 489–490, pl. 376, figs 1–6, pl. 377 (map) (in part, includes E. omanensis ). Kilburn, 1972: 405. Reid, 1989a: 100.

Nodilittorina natalensis — Kilburn & Rippey, 1982: 51, pl. 10, fig. 5. Potter & Schleyer, 1991: 1–15, pl. 2.5 (radula). Reid, 2002a: 259–281 (in part, includes E. omanensis ).

Echinolittorina natalensis — Williams et al., 2003: 83 (in part, includes E. omanensis ). Williams & Reid, 2004: 2227– 2251.

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

Tectarius nodosus — Tryon, 1887: 259, pl. 47, fig. 67 (in part, includes E. australis , E. subnodosa , E. miliaris ; not Gray, 1839).

Nodilittorina nodulosa — Fischer, 1969: 119–129 (in part, includes N. pyramidalis , E. omanensis , E. malaccana , E. austrotrochoides , E. cecillei , E. marquesensis , E. wallaceana ; not Gmelin, 1791 = E. malaccana group or E. pascua ). Fischer, 1971: 31–32 (in part, includes E. omanensis , E. malaccana ; not Gmelin, 1791).

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

Tectarius malaccanus — Dautzenberg, 1923: 49 (not Philippi, 1847). Dautzenberg, 1929: 495–496 (not Philippi, 1847). Dautzenberg, 1932: 61 (not Philippi, 1847).

Taxonomic history: Despite its superficial similarity to nodulose species in other parts of the world, this species has had a relatively uncomplicated taxonomic history and most authors have accepted it as distinct since its description. Weinkauff (1883; followed by Tryon 1887) considered it conspecific with the larger E. subnodosa from the Red Sea, and united these two under the name Litorina nodosa , together with nodulose forms of E. australis from Australia. These three taxa were clearly distinguished by Rosewater (1970). Until now, nodulose shells from southern Arabia have generally been included with E. natalensis (Rosewater 1970; Mienis 1973; Bosch et al. 1995; Reid 2002a), but these are here described as E. omanensis . Surprisingly, no authors appear to have synonymized E. natalensis with members of the E. malaccana group and confusion between them has been minimal. It is not clear why Dautzenberg (1923, 1929, 1932) separated T. natalensis and T. malaccanus from Madagascar; the only nodulose species known to occur there is E. natalensis . Nevertheless, Fischer (1969, 1971) continued to maintain that N. nodulosa (= E. malaccana group) occurred in the western Indian Ocean, based on Dautzenberg (1929) and a misidentification of the Arabian E. omanensis .

Diagnosis: Shell conical, 3 rows of pointed nodules on last whorl, peripheral nodules crossed by 2 spiral ribs; 15–24 sharp spiral threads on last whorl (including base); grey, brown or black with white nodules. South and East Africa, Madagascar. COI: GenBank AJ623019 , AJ623020 .

Material examined: 60 lots (including 17 penes, 3 sperm samples; 12 pallial oviducts, 1 sample of egg capsules, 4 radulae).

Shell ( Fig. 13 ): Mature shell height 6.3–15.8 mm. Shape conical (H/B = 1.26–1.66; SH = 1.56–1.98); spire whorls lightly rounded, suture distinct; spire profile almost straight, slightly concave at apex; periphery of last whorl weakly angled. Columella short, concave, hollowed at base; small eroded parietal area. Sculpture of last whorl: 3 rows of pointed nodules at periphery, mid-whorl and shoulder, aligned to form 12–18 axial series; entire surface with sharp spiral threads, 10–15 at and above periphery, and microstriae; peripheral nodules crossed by 2 spiral threads; base with 5–9 nodulose threads; in strongly sculptured shells ( Fig. 13A ) the axially aligned nodules form varix-like ridges; in smooth shells ( Fig. 13F–H ) the nodules become obsolete on last whorl, remaining only as 1–3 slightly raised ribs. Protoconch 0.23–0.25 mm diameter, 2.3–2.4 whorls. Colour: purple-brown (fading to grey-pink), orange-brown at apex, nodules white; in darkest shells an irregular axial pattern of black and grey stripes ( Fig. 13I ); in smooth shells the positions of the 3 rows of nodules may be marked by bands of black and white spots ( Fig. 13F ); aperture brown to black with pale band at base; columella purple-brown to black.

Animal ( Fig. 14 ): Head black, no unpigmented stripe across snout, tentacle pale around eye and inner side of base, with two longitudinal grey to black lines, usually partly fused and extending to half tentacle length, but sometimes extending full length, or tentacle black with unpigmented tip; sides of foot mottled black or all black. Opercular ratio 0.49–0.58. Penis ( Fig. 14A–G ): 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 equal to or smaller than glandular disc, borne together on projection of base; penis unpigmented or slightly pigmented at base. Euspermatozoa 114–121 µm; paraspermatozoa ( Fig. 14I, J ) spherical to oval, 10–14 µm diameter, filled with large round granules, containing single short rectangular rodpiece, hexagonal in section and not projecting from cell. Pallial oviduct ( Fig. 14H ): bursa opening at one third to one half length of straight section (from anterior) and extending back to albumen gland. Spawn ( Fig. 14K– M ): an asymmetrically biconvex pelagic capsule 220–285 µm diameter with broad peripheral rim on which faint diagonal striations can sometimes be seen, cupola-shaped upper side sculptured by 5–6 spiral or concentric rings (rings occasionally absent in aberrant capsules), containing single ovum 88–100 µm diameter. Development predicted to be planktotrophic.

Radula ( Fig. 15A–D ): Relative radula length 2.67–8.0 (mean 4.55, Potter & Schleyer 1991). Rachidian: length/width 1.89–3.85, sometimes narrow ( Fig. 15A ); tip of major cusp pointed. Lateral and inner marginal: tips of major cusps rounded; major cusp of lateral slightly ( Fig. 15C, D ) or considerably ( Fig. 15A, B ) larger than that of inner marginal; outermost cusp of inner marginal may be absent ( Fig. 15A ). Outer marginal: 5–6 cusps.

Range ( Fig. 16 ): Southwestern Indian Ocean from South Africa to Kenya, Madagascar and Seychelles. Range limits: Cove Rock, East London, South Africa (Kilburn 1972); Umngazana Head, South Africa (BMNH); Bazaruto I., Mozambique (NM J7152); Wimbi, Pemba, Mozambique (BMNH 20060279); Oysterbay, Dar es Salaam, Tanzania (BMNH 20060284); Datamu, 20 miles N Mombasa, Kenya (BMNH); Picard, Aldabra (BMNH); Mahé, Seychelles (IRSNB); Baie de Diego Suarez, Madagascar (IRSNB); Tolagnaro, Madagascar (BMNH 20030691); Toliara, Madagascar (IRSNB); Europa Atoll (IRSNB). The species is apparently rare in the Seychelles; only a single shell has been recorded and its occurrence requires confirmation. It does occur on the atolls of Europa and Aldabra, but was not recorded in a survey of the littorinids of the Comores (Warmoes et al. 1990). Occurrence between Bazaruto in southern Mozambique and Dar es Salaam, and in western Madagascar, is apparently sporadic. The southern limit is East London, where a single shell was recorded by Kilburn (1972).

Habitat and ecology: This species occurs on a variety of substrates, including coral limestone, beachrock, sandstone, conglomerate, granite and concrete. It is abundant in the littoral fringe on shores of moderate to high exposure. In Natal E. natalensis occupies a zone between Littoraria glabrata in the littoral fringe and Afrolittorina africana lower on the shore, and prefers eroded sandstone (Eyre & Stephenson 1938; Kilburn 1972); it occurs mainly in crevices, and reaches densities of 2000 per m 2 (Potter 1987). At Inhaca Island it is found at and above MHWS on calcareous sandstone, in a zone between the same two sympatric littorinids, at densities of up to to 1000 per m 2, and only on exposed shores (Kalk 1958). At Toliara, Madagascar, it is found on eroded limestone cliffs, but not on concrete (Plante 1964; as Tectarius malaccanus ). Translocation, diet and competition for food have been studied by Potter (1987) and Potter & Schleyer (1991).

Remarks: Although found mainly on the continental shores of East Africa and Madagascar, this species can be classed as oceanic in character, because it occurs in areas of low primary productivity (Rutgers University Primary Productivity Study) and on shores that are often exposed to strong wave action. To the south, its distribution in South Africa is extended by the warm Agulhas Current and is presumably ultimately limited by low temperatures. Elsewhere, the lack of records from central Mozambique, the eastern and western coasts of Madagascar, and to the north of the records in Kenya, can be ascribed to lack of suitable habitat on these predominantly sedimentary coastlines (Myers & Whittington 2000; Cooke et al. 2000; Carbone & Accordi 2000). The westward-flowing South Equatorial Current may prevent the colonization of the Mascarene Islands.

The small shell with three rows of nodules is usually easily recognized and unlikely to be confused with any other within its area of distribution. However, the nodules occasionally become weak on the last whorl. A distinctive regional form occurs in western Madagascar, from Ile Sainte Marie to Tolagnaro, in which the spire is normal and nodulose, but the last whorl may be macroscopically smooth (retaining spiral threads), with a black-and-white striped or marbled pattern ( Fig. 13F–I ). These smooth shells superficially resemble E. biangulata from the eastern Indian Ocean (Fig. 44) and E. tricincta from the western Pacific (Fig. 48). However, they occur together with typically nodulose shells and intermediates, and no anatomical differences can be detected. Precise dates of collection are not available for the studied museum specimens of this smooth form, but most were collected in the late nineteenth and early twentieth century. Recent collecting in Ile Sainte Marie, Tamatave and Tolagnaro (pers. obs. 2003) revealed no entirely smooth shells among abundant normal forms, and only a low frequency (less than 5%) of moderately smooth types ( Fig. 13F ). There may also be an ecophenotypic component to sculptural variation, because shells from limestone substrates are the most strongly sculptured ( Fig. 13A–C ). On a sea wall in Dar es Salaam strongly sculptured shells (similar to those in Fig. 13A–C ) were found on blocks of coral limestone, whereas shells on an immediately adjacent stretch of concrete wall were more smooth (resembling those in Fig. 13D, G ; pers. obs. 2006).

This species shows more striking radular variation than any of its IWP congeners. Of the four radulae examined, only one from Tolagnaro, Madagascar, was found with extreme reduction of the rachidian and enlargement of the lateral tooth cusps ( Fig. 15A, B ) and this occurred on a sandstone substrate together with an individual with a radula of normal type (similar to that illustrated in Fig. 15C, D from limestone in Kenya). Similar variation occurs in E. australis , and the possibility of ecophenotypic plasticity deserves investigation (see Discussion) .

There are no obvious anatomical differences between the three allopatric species E. natalensis , E. omanensis and E. subnodosa , although shells of each are almost always distinctive. Molecular evidence supports their recognition as separate species, with E. natalensis sister to the other two (Williams & Reid 2004). Of the three, those most similar in shell characters are the nodulose forms of E. natalensis and E. omanensis . Echinolittorina omanensis ( Fig. 17 ) is a narrower shell; there are usually two rows of rounded nodules on the last whorl (three rows of more pointed ‘prickly’ nodules in E. natalensis ); the nodules in the peripheral row are axially elongate and crossed by three or four spiral ribs (two spiral threads on peripheral nodules of E. natalensis ); the base is rarely nodulose; the spiral sculpture is of 10–16 spiral ribs on the last whorl (15–24 sharp spiral threads in E. natalensis ). Confusion between E. natalensis and E. subnodosa is less likely; the latter ( Fig. 19 ) has a larger shell, concave spire profile and three widely-spaced rows of pointed nodules.

Figures

FIGURE 13. Echinolittorina natalensis. A–C, Tiwi Beach, Kenya (BMNH 20040209). D, J, K, North Pier, Durban, South Africa (BMNH 20040210). E, F, Ankarena, Île Ste Marie, Madagascar (BMNH 20030679). G, H, no locality [probably eastern Madagascar] (MNHN). I, L, N, Libanona Beach, Tolagnaro, Madagascar (BMNH 20030691). M, Litorina natalensis Krauss in Philippi, 1847, lectotype, Natal, South Africa (SMNS ZI.0050942).

FIGURE 14. Echinolittorina natalensis. A–G, penes. H, pallial oviduct. I, J, paraspermatozoa. K–M, pelagic egg capsules. A, Amanzimtoti, Kwazulu-Natal, South Africa (BMNH 20040211; shell H = 6.3 mm). B, C, Ankarena, Île Ste Marie, Madagascar (BMNH 20030679; shell H B = 10.8 mm, C = 10.5 mm). D, E, K–M, North Pier, Durban, South Africa (BMNH 20040210; shell H D = 10.0 mm, E = 9.4 mm). F, I, J, Oysterbay, Dar-es-Salaam, Tanzania (BMNH 20040212; shell H = 6.5 mm). G, H, Libanona Beach, Tolagnaro, Madagascar (BMNH 20030691; shell H G = 7.8 mm, H = 10.0 mm). Shading conventions as in Figure 3.

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 17. Echinolittorina omanensis new species. A, B, Merca, Somalia (HUJ 30002). C, F, M, Mirbat, Dhofar, Oman (BMNH 20040213). D, Mughsayl I., Dhofar, Oman (BMNH 20040214). E, Karachi, Pakistan (BMNH 20040215). G,H, W Mughsayl I., Dhofar, Oman (BMNH 20040217). I, Karachi, Pakistan (BMNH 20040216). J, holotype, Wadi Sayq, Jabal Qamr, Dhofar, Oman (BMNH 20040218). K, L, Mukalla, Aden, Yemen (BMNH 20040221).

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).