Echinolittorina pulchella ( Dunker, 1845 )

Reid, David G., 2011, 2974, Zootaxa 2974, pp. 1-65 : 28-32

Echinolittorina pulchella ( Dunker, 1845)

( Figures 8, 11E, F, 12, 13)

Litorina pulchella Dunker, 1845: 166–167 (Loanda [Luanda, Angola]; 18 syntypes ZMB 108.697, seen; lectotype (here designated) Dunker, 1853: pl. 2, fig. 14, Fig. 12D herein). Dunker, 1853: 12, pl. 2, figs 11–20. Philippi, 1847: 198, Litorina pl. 4, fig. 8. Weinkauff, 1882: 74–75, pl. 10, figs 1, 4. Weinkauff, 1883: 221.

Littorina (Melarhaphe) pulchella —H. Adams & A. Adams, 1854: 314 (as Melaraphe ).

Littorina (Melarhaphe) punctata var. pulchella — Tryon, 1887: 248, pl. 44, fig. 64 (as Melaraphe ).

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

Echinolittorina pulchella — Williams et al., 2003: 83. Williams & Reid, 2004: 2227–2251, fig. 6E (map). Williams & Duda, 2008: fig. 1 (phylogeny). Robin, 2008: 114, fig. 3.

Littorina pulchella — Ardovini & Cossignani, 2004: 21.

Echinolittorina (Amerolittorina) pulchella — Reid, 2009: figs 1, 37 (phylogeny).

Litorina punctata — Dunker, 1853: 11-12, pl. 2, figs 23-25 (in part, includes E. punctata ).

Littorina punctata — Weinkauff, 1868: 274 (in part, includes E. punctata ). Nobre, 1909: 34 (in part, includes E. caboverdensis ; not Gmelin, 1791). Nicklès, 1950: 48–49, fig. 37 (in part, includes E. punctata , E. caboverdensis ). Buchanan, 1954: 34 (not Gmelin, 1791). Edmunds, 1978: 27, fig. 4E (not Gmelin, 1791). Gofas, Afonso & Brandão, 1987: 40–41, fig. 11b (not Gmelin, 1791).

Littorina (Melarhaphe) punctata — Dautzenberg, 1912: 46 (in part, includes E. punctata ; as Melaraphe ). Boettger, 1913: 101 (in part, includes E. punctata ; as Melaraphe ).

Littorina (Austrolittorina) punctata — Rosewater, 1970: 423, 474–476, pl. 364, figs 7, 8 (shell), pl. 367 (map) (in part, includes E. punctata , E. caboverdensis , E. soroziczac and probably Afrolittorina knysnaensis and L. saxatilis ). Kilburn, 1972: 401– 402 (in part, includes E. punctata ). Rosewater, 1981: 24–26, pl. 1E (shell), 3J (operculum), 4L (penis) (in part, includes E. punctata , E. caboverdensis , E. soroziczac ).

Nodilittorina (Echinolittorina) punctata — Reid, 1989: 99 (in part, includes E. punctata , E. caboverdensis ).

Littorina meleagris — Bernard, 1984: 28, pl. 2, fig. 18 (not Beck in Potiez & Michaud, 1838 = E. meleagris ).

Taxonomic history: Dunker (1845) described this species from Angola, where it is the only member of the E. punctata group. In his detailed account of the molluscs of West Africa ( Dunker 1853) he distinguished Litorina punctata and Litorina pulchella , but mistakenly gave both Angola and Senegal as localities for the former. In his Angolan material he used the name Litorina pulchella only for relatively narrow, brightly patterned, smooth shells, and Litorina punctata for the lower-spired, striated shells with more patulous aperture, which are in fact conspecific. The syntypes of Litorina pulchella are the sample that includes the specimens figured by Dunker (1853).

The name L. pulchella was used by early authors (Philippi 1847; Weinkauff 1882, 1883; H. Adams & A. Adams 1854), but it was reduced to a variety of L. punctata by Tryon (1887) and subsequently considered a synonym of that species ( Dautzenberg 1912; Rosewater 1970, 1981; Reid 1989). It was not again considered distinct until reinstated by Reid (2002a). Genetic data have confirmed the separation of the three species of the E. punctata group ( Williams & Reid 2004; Williams & Duda 2008; Reid 2009).

Small black and white specimens of E. pulchella were misidentified as L. meleagris by Bernard (1984).

Diagnosis: Shell with 10–19 incised spiral lines above periphery; black to orange brown with aligned array of white spots. Penis bifurcate, with smooth tapering filament, mamilliform penial gland and glandular disc of similar size on side branch of base. Sierra Leone to northern Namibia. COI: GenBank FN298400 , FN298401 , FN298410 , AM941713 .

Material examined: 58 lots (including 19 penes, 2 sperm samples, 9 pallial oviducts, 4 radulae).

Shell ( Fig. 12): Mature shell height 4.5–18.9 mm. Shape high turbinate and sometimes slightly succineiform (H/B = 1.33–1.60, SH = 1.48–1.78); spire whorls gently rounded; suture distinct; spire profile straight or concave at apex; periphery of last whorl slightly angled. Columella long, hollowed and slightly pinched at base, sometimes broad; eroded parietal area small or absent. Some specimens show 1–6 conspicuous growth interruptions on last whorl. Sculpture of 10–12 primary spiral grooves above periphery (on spire whorls the 1–2 anteriormost are covered by suture); some secondary grooves usually appear (by division) on last whorl, giving totals of 13–19 grooves above and 4–14 below periphery; sculpture usually fine, consisting of incised lines only, sometimes faint or absent; peripheral rib more prominent and 1.5–2 times width of adjacent ribs; spiral microstriae absent, surface shiny. Protoconch 0.34–0.38 mm diameter, 2.6 whorls. Ground colour pale orange brown to black, with regular opisthocline series of white spots; in darkest small shells white spots present at suture, periphery and base only; occasionally spots may fuse to give irregular axial stripes; pale shells sometimes show broad darker brown spiral band from shoulder to periphery and narrow dark band on base; aperture dark brown to black with pale band at base; columella pale to dark brown.

Animal: Head black, no unpigmented stripe across snout; tentacle black or with two longitudinal black stripes, pale around eye and at tip; sides of foot black. Operculum: opercular ratio 0.32–0.36. Penis ( Fig. 13A–E): filament gradually tapering to pointed tip, 0.5–0.7 total length of penis, sperm groove ends terminally; mamilliform gland approximately same size as penial glandular disc, which projects as a lobe, borne together on short projection of base; penis unpigmented or slightly pigmented at base. Euspermatozoa 50–57 µm; paraspermatozoa ( Fig. 13G, H) contain an elongate-fusiform rod-piece 14–21 µm long with rounded ends, projecting from cell, which is packed with large round granules. Pallial oviduct ( Fig. 13F): first loop of albumen gland small; copulatory bursa separates at posterior end of straight section and extends back almost to albumen gland. Spawn not known; pelagic capsules predicted from form of pallial oviduct ( Reid 2002a).

Radula ( Fig. 11E, F): Relative radula length 2.54–5.60. Rachidian: length/width 1.41–1.64; major cusp narrow, tip pointed to slightly rounded. Lateral and inner marginal: 4 cusps; tip of major cusp bluntly rounded or rounded; inner and outer cusps small. Outer marginal: 7–10 cusps; flange on inside and outside of base.

Range ( Fig. 8): Sierra Leone to northern Namibia. Range limits: Cape Shilling Kent, Sierra Leone ( BMNH 1957.9.20.58–67); Monrovia , Liberia ( USNM 703757 ; IRSNB) ; Cotonou, Benin ( USNM 707160 ) ; Cap Esterias, Gabon ( Bernard, 1984: 28, as Littorina meleagris ); Pointe-Noire, Congo ( BMNH; ZMA; MNHN); Rocky Point , Namibia ( SAM A31184) ; Mowe Bay , Namibia ( SAM A31338 ) .

There is a gap in the recorded distribution between Benin and Gabon, including Bioko Island. This corresponds to the head of the Gulf of Guinea where salinity is reduced by the outflows of the rivers Niger and Sanaga ( Longhurst 1962). Records of other littorinids (e.g. E. granosa , Fig. 19) are available from this region, so the gap is probably real, rather than a collection artefact. Nicklès (1947, 1952) did not record it at any localities between Cameroon and Pointe-Noire, Congo. Lawson (1955) did not find it in Cameroon. Lawson & John (1982) reported it to be uncommon “on offshore islands and in Cameroon and Gabon ” without giving precise details. Nevertheless, there are records of E. pulchella in estuarine situations in Sierra Leone and Guinea (see Habitat below).

The southern limit of this species in northern Namibia was discussed by Kilburn (1972; as L. punctata ). Based on material collected by Penrith and Kensley ( SAM) he identified Rocky Point (18°59’S) as the southern limit, where it occurs with A. knysnaensis , here at its northern limit. This has been confirmed by examination of the same material (see also Reid & Williams 2004). In addition, a specimen of E. pulchella is here recorded from a little further south, at Mowe Bay (19°20’S).

Habitat: Abundant on rock (including beachrock, sandstone, granite, shale, concrete) at top of eulittoral and in littoral fringe, also in shallow pools at top of eulittoral; on moderately sheltered and exposed shores.

Most ecological observations have been made in Ghana, where it is abundant in the upper eulittoral and littoral fringe at most sites ( Buchanan 1954; Lawson 1956; Bassindale 1961; Evans 1961; Vermeij 1972a, b, 1973; Edmunds 1978; Evans et al. 1993). Evans (1961) observed the most dense population between mid-tide and highwater neap tide, but most authors have recorded a higher level than this, with maximum level up to 3 m above MHWN on exposed shores ( Bassindale 1961). There is an upshore size increase ( Vermeij 1972a; Edmunds 1978); where small snails occur in the littoral fringe they favour immersion in pools ( Evans 1961). Experimental tests of response to disturbance have shown differing strengths of downslope and upshore movement in snails from vertical surfaces and from pools ( Evans 1961). Substrates include soft shale ( Vermeij 1972b), laterite and schist ( Vermeij 1973). The species is present on both exposed and sheltered coasts ( Lawson 1956; Gauld & Buchanan 1959; Collignon 1960), except where outcrops are affected by sand scour ( Evans et al. 1993).

A broadly sympatric species is E. granosa , which dominates on more sheltered and estuarine shores; where both occur together on exposed coasts E. pulchella usually occupies a slightly lower level than its congener ( Lawson 1956, 1966; Gauld & Buchanan 1959; Lawson & John 1982; John & Lawson 1991). On the rocky shores of Sierra Leone, which are influenced by river outflow, Lawson (1957) noted that it was less common than E. granosa . Here a slightly different pattern of relative zonation was observed by Longhurst (1958), who stated that E. granosa extended slightly lower on the shore than E. pulchella on open coasts; both could be found up to 6 miles from the mouth of the Sierra Leone River, where they were joined by, and eventually replaced by, Littoraria cingulifera . At Conakry, Guinea, E. pulchella is found in the uppermost eulittoral on laterite, where salinity falls to 21‰ in September ( Marchal 1960).

There has been some confusion between E. pulchella and superficially similar Afrolittorina knysnaensis on the shores of Namibia; some records of ‘ L. punctata ’ refer to the latter species ( Penrith & Kensley 1970a), or to both ( Penrith & Kensley 1970b) (see Kilburn 1972; Reid & Williams 2004). North of Rocky Point, and in Angola, E. pulchella occurs alone, and here it has been recorded as common in crevices in quartzite from the littoral fringe down to the top of the barnacle zone ( Kensley & Penrith 1973, 1980).

Remarks: The shell of E. pulchella shows considerable variability, from small, smooth, dark forms to large, striate, pallid ones ( Fig. 12). In some other members of the subgenus Amerolittorina (e.g. E. aspera group, Reid 2002b) specimens from unfavourable habitats, such as shallow pools in the littoral fringe, are small, smooth, darkly patterned and with a more domed spire profile; it has been suggested that this could be the result of an ecophenotypic effect, perhaps mediated through slow growth rate, dietary or salinity effects. The dwarf, smooth, dark shells of E. pulchella ( Fig. 12J) are closely comparable and it can be predicted that such forms predominate on horizontal surfaces and in pools at high tidal levels. Some large shells have dark early whorls and become pallid on the final 1–2 whorls ( Fig. 12A, E). This colour change supports an ecophenotypic effect; such shells could have settled in pools in the littoral fringe before migrating to a more favourable microhabitat. Vermeij (1973) observed that specimens from the littoral fringe are significantly higher-spired than those of same size range from the upper eulittoral on shores in Ghana. In Figure 12 it can be seen that large shells tend to have a more concave spire profile, whereas small ones are more domed. These two observations may be consistent, if slower growth leads to doming and a higher spire ( Vermeij 1980).

This species shows a continental distribution, being restricted to the continental margin of Africa and absent from the islands of the Gulf of Guinea (where it is replaced by E. soroziczac ). The gap in distribution between Benin and Gabon suggests that this species is less tolerant of the reduced salinity in this estuarine region than E. granosa , which is abundant on the coast of Cameroon. This is consistent with the relative scarcity of E. pulchella in Sierra Leone, where the coast is influenced by river outflow ( Lawson 1957). On the other hand E. pulchella can be found in estuaries ( Longhurst 1958) and where salinity falls as low as 21‰ ( Marchal 1960).

The recognition of this species as distinct from the two others in the E. punctata group is supported by their reciprocal monophyly in analyses of COI sequences ( Reid 2009), and by the K2P genetic distance of 3.50% between the two closest, E. pulchella and E. punctata (this exceeds the minimum 2.61–2.70% reported for sister ESUs that are regarded as distinct biological species in this genus; Reid 2009). There are as yet no corroborating nuclear genetic data, although the differences in the range of shell variation could have a nuclear genetic basis. Although E. pulchella and E. punctata share the highest similarity in the COI sequences, their sister relationship did not achieve significant support in an analysis of this gene alone ( Reid 2009); however, in an analysis based on single individuals of each, and with the addition of 12S data, this sister pairing was supported ( Williams & Duda 2008; note transposition of E. punctata A and B in this work).

The shells of the three species of the E. punctata group are very similar and cannot always be distinguished ( Table 1). That of E. pulchella is most similar to E. punctata , but tends to be larger, with less rounded spire whorls, weaker spiral sculpture and often a coarser and more pronounced colour pattern (compare Figs 6 and 12). Reliable distinction depends on genetic data and geographical distribution, for the three species are allopatric. Small, spotted specimens of E. pulchella have been confused with E. peregrinator (e.g. Bernard 1984, as L. meleagris ) and the two are sympatric, but the latter species possesses only a single peripheral groove and a distinct pseudumbilicus. Likewise with black and white pattern, the shell of E. soroziczac is superficially similar, but has a larger number of grooves on the last whorl (22–43, cf. 10–19 in E. pulchella ) and two pale bands within the aperture ( Table 1).

In Namibia, at the southern limit of its range, E. pulchella has been confused with Afrolittorina knysnaensis and the two occur together at Rocky Point ( Kilburn 1972; Reid & Williams 2004). There are pronounced anatomical differences: the penis of A. knysnaensis has a broader, blunt filament and lacks a glandular disc; in its pallial oviduct the capsule gland is thrown into a separate loop. The shells are similar, but the colour pattern of A. knysnaensis is usually of fine brown speckling, often with a broad peripheral black band or black above the periphery (see Reid & Williams 2004 for a detailed account of A. knysnaensis ). Kilburn (1972) believed that the only difference between these species lay in shell colour pattern and interpreted the variation in A. knysnaensis as evidence for their hybridization; however, he also noted that at Rocky Point they remained distinct. The distant phylogenetic relationship between Afrolittorina and Echinolittorina ( Williams et al. 2003) makes the possibility of hybridization remote.