Afrolittorina africana

Reid, DG & Williams, ST, 2004, The Subfamily Littorininae (Gastropoda: Littorinidae) in the Temperate Southern Hemisphere: The Genera Nodilittorina, Austrolittorina and Afrolittorina, Records of the Australian Museum 56, pp. 75-122 : 100-106

Afrolittorina africana (Krauss, in Philippi, 1847)

Figs. 15–16, 17A,B, 18

Litorina africana Krauss , in Philippi, 1847: 199, Litorina pl. 4, fig. 10 (Caput Bona Spei [Cape of Good Hope,SouthAfrica;restricted to Algoa Bay, Krauss, 1848]; lectotype ( Janus, 1961) Stuttgart Museum ZI 0050275 (formerly MT 106; fig. 15A; seen) plus 1 paralectotype ZI 0050276; possible paralectotypes Senckenberg Museum SMF 314707/1 (Herbert & Warén, 1999); additional paralectotypes may be in Nationaal Natuurhistorisch Museum, Leiden [van Bruggen, 1992: 83]). Krauss, 1848: 102. Weinkauff, 1878: 37, pl. 4, figs. 5–6. Weinkauff, 1883: 218 (includes A. knysnaensis ).

Littorina africana .— Reeve, 1857: Littorina sp. 37 (in part; pl. 8, fig. 37 is L. unifasciata ). Nevill, 1885: 137. Bartsch, 1915: 120. Tomlin, 1923: 49. Dautzenberg, 1932: 60. Turton, 1932: 132, 133. Kilburn & Rippey, 1982: 50, pl. 10, fig. 1. Potter & Schleyer, 1991: pl. 2.2, 2.3 (radula).

Littorina (Melarhaphe) africana .—Adams & Adams, 1854: 314 (as Melaraphe ). Tryon, 1887: 248–249, pl. 44, figs. 66–67 (as Melaraphe ; in part; figs. 65, 68 are Afrolittorina knysnaensis ; fig. 69 is Echinolittorina quadricincta Mühlfeld, 1824 ). Janus, 1961: 5 (as Melaraphe ).

Littorina (Austrolittorina) africana .— Rosewater, 1970: 423, 476– 477, pl. 364, figs. 11–16, pl. 365, fig. C (penis), pl. 368 (distribution). Kilburn, 1972: 399–401 (probably subspecies of Austrolittorina unifasciata ).

Nodilittorina africana .—Bandel & Kadolsky, 1982: 3. Reid, 2002 b: fig. 2a (penis).

Nodilittorina (? Echinolittorina ) africana .— Reid, 1989: 99, fig. 10i (oviduct) ( A. knysnaensis doubtfully included).

Nodilittorina (Austrolittorina) africana .— Reid, 2002 a: 154.

Afrolittorina africana .— Williams et al., 2003.

Litorina decollata Krauss , in Philippi, 1847: 196; Litorina pl. 4, fig. 3 (Ora Natal Africae [coast of Natal, South Africa]; lectotype ( Janus, 1961) Stuttgart Museum ZI 0050277 (formerly MT 107; fig. 15F; seen) plus 26 paralectotypes ZI 0050278; possible paralectotypes Senckenberg Museum SMF 314709/3 and uncatalogued (Herbert & Warén, 1999); 15 possible paralectotypes MCZ 154113; 2 paralectotypes ZMA; additional paralectotypes may be in Nationaal Natuurhistorisch Museum, Leiden [van Bruggen, 1992: 83]). Krauss, 1848: 102. Küster, 1856: 9, pl. 1, figs. 14–15. Weinkauff, 1878: 28. Weinkauff, 1883: 219 (in part; includes A. knysnaensis ).

Littorina (Melarhaphe) decollata .—Adams & Adams, 1854: 314 (as Melaraphe ). Janus, 1961: 5–6 (as Melaraphe ).

Littorina decollata .—Reeve, 1858: Littorina sp. 92, pl. 17, fig. 92. Sowerby, 1892: 36. Turton, 1932: 132.

Littorina caerulescens .— Tenison Woods, 1879: 65–72 (as coerulescens; not Turbo caerulescens Lamarck, 1822 = Melarhaphe neritoides ; in part; includes Austrolittorina unifasciata , Austrolittorina antipodum , Afrolittorina praetermissa , Littoraria mauritiana , L. undulata , M. neritoides ).

Littorina knysnaensis .— Sowerby,1892: 36 (not Litorina knysnaensis Krauss , in Philippi, 1847 = A. knysnaensis ; in part; includes A. knysnaensis ).

? Littorina perplexa Turton, 1932: 133 , pl. 28, fig. 960 ( Port Alfred , South Africa; holotype OUM, seen).

Taxonomic history. Krauss (1848) described three new littorinids from South Africa, Litorina africana , L. decollata and L. knysnaensis but, owing to his habit of sending specimens and manuscript names to colleagues, the names and descriptions had appeared a year earlier in the monograph of Litorina by Philippi (1847). Krauss was credited with authorship in this earlier publication (see biographical notes on Krauss and discussion of his taxa by Herbert & Warén, 1999). Later authors maintained these taxa as distinct until the first revision by Tryon (1887), who correctly synonymized L. decollata with L. africana (thereby establishing the valid name for this species, despite the page priority of L. decollata ). Among later authors, only Sowerby (1892), Turton (1932) and Janus (1961) have continued to regard L. decollata as a distinct species.

The shells of the two species are usually easily separable, so it is surprising that there has been a long history of confusion and combination of A. africana and A. knysnaensis . Weinkauff (1883) and Tryon (1887) both regarded knysnaensis as a variety of L. africana , whereas Sowerby (1892) combined both under the former name. Bartsch (1915) recognized both species, yet described elongate examples of A. knysnaensis as L. africana tryphena . Although Rosewater (1970) clearly described the characteristic shells of the two species, Hughes (1979) once again combined the two as varieties of L. africana . The evidence for this was that “the complete range of intermediate forms in shell colour and morphology, and the absence of differences in radulae, penial morphology or habitat suggest that these forms represent a dimorphic species showing a genetic cline correlated with latitude” ( Hughes, 1979). The relative proportions of the blue-grey A. africana and brown A. knysnaensis do indeed change from 0 to 100% along the South African coast between False Bay and Natal. However, although the shell of A. knysnaensis can sometimes be pale in colour, the two species remain distinct in shell shape and sculpture. Most significantly, the penes are distinct, particularly in their pigmentation, as observed by Hughes himself. Subsequent authors ( Kilburn, 1972; Bandel & Kadolsky, 1982) retained the two as distinct species, although Reid (1989) doubtfully synonymized them.

The identity of Littorina perplexa , described by Turton (1932) from Port Alfred, is puzzling. Rosewater (1970) listed it in the synonymy of Littorina punctata ( Gmelin, 1791) ” (presently interpreted as a complex of three species, including Echinolittorina punctata ; Reid, 2002 b). Noting that E. punctata s.l. does not occur in South Africa, Kilburn (1972) interpreted L. perplexa as a form of A. africana with a patterned shell. The unique holotype is a beachworn shell 1.9 mm in height, of about two teleoconch whorls, with a low-turbinate shape, weak spiral grooves, eroded apex and well-developed tessellated pattern. At this small size none of the three turbinate littorinids recorded from Port Alfred ( A. africana , A. knysnaensis , Littoraria intermedia [Philippi, 1846]) has been seen to develop a distinct tessellated pattern of this kind, so although Kilburn’s attribution is possible, it can be doubted. The shell does indeed resemble a juvenile specimen of the E. punctata complex, perhaps accidentally transported to Port Alfred.

Reeve (1857) inadvertently described and figured a shell of Austrolittorina unifasciata as Littorina africana , as noted by Smith (1884, as L. mauritiana ). The South African species has occasionally been united with species of Austrolittorina as a single taxon ( Tenison Woods, 1879; see Taxonomic History of Austrolittorina unifasciata ). Kilburn (1972) revived this idea, suggesting that Littorina africana might prove to be a subspecies of Littorina unifasciata , a circumpolar taxon.

Diagnosis. Shell small, turbinate, usually sculptured with fine spiral threads; white with broad blue-grey band above periphery, sometimes with additional fine, pale brown tessellation. Penis with bluntly blade-shaped, red-brown (greyish black when preserved) filament; mamilliform gland on base, but no glandular disc. Pallial oviduct with three consecutive loops of egg groove, in albumen gland, capsule gland and in terminal portion of oviduct.

Material examined. 52 lots (6 AMS, 3 USNM, 38 BMNH, 1 IRSNB, 1 ZMA, 1 MNHNP, 2 NM), including 16 penes, 3 sperm samples, 16 pallial oviducts, 6 radulae.

Shell ( Fig. 15). Mature shell height 3.7–12.0 mm (13.5 mm, Rosewater, 1970). Shape globular to turbinate (H/B = 1.20– 1.66; SH = 1.18–1.91); spire outline slightly concave at apex; whorls well rounded, suture distinct, periphery rounded or slightly angled; moderately solid. Columella pillar straight to slightly concave; columella broad, slightly excavated; eroded parietal area usually absent but may be present in low-spired shells. Sculpture of numerous fine spiral threads and striae (not clearly differentiated into primary grooves, ribs and microstriae); on early teleoconch whorls 8–11 threads visible above suture, with striae between; on last whorl numerous closely spaced coarse striae over entire whorl, of which 15–27 may be raised as narrow cords; periphery not marked by an enlarged rib; sometimes almost smooth with only faint spiral striae; growth lines may be present towards end of last whorl; spire often eroded. Protoconch rarely preserved, about 0.34 mm diameter, 3 whorls. Colour white to cream, with broad spiral band of blue-grey from just below suture to below periphery; darker pattern may be absent, but fine tessellation of yellow or pale brown is often faintly visible over entire surface of last whorl ( Fig. 15G,H); rarely, pattern is developed into conspicuous oblique, spiral or zigzag brown lines ( Fig. 15D,E); eroded spire blackish brown; aperture dark brown with basal white band; first 2 whorls of teleoconch fawn.

Animal. Head and sides of foot grey to black; tentacles with fine black transverse lines (sometimes faint or absent). Opercular ratio 0.37–0.44. Penis ( Fig. 16A–J): filament 0.5– 0.6 total length of penis, bluntly blade-shaped and slightly swollen, coloured red brown in life (dark greyish black in preserved specimens) by subepithelial glandular tissue; sperm groove open almost to filament tip; single mamilliform gland borne on lateral branch of base; glandular disc absent; instead the epithelium around the papilla of the mamilliform gland is tall and glandular; base unpigmented. Euspermatozoa length unknown; paraspermatozoa ( Fig. 16M) spherical to oval, 11–19 µm diameter, containing large spherical granules and single hexagonal or irregular rodbody, rarely projecting from cell. Pallial oviduct ( Fig. 16K,L) with simple loop of albumen gland, followed by large, almost circular loop of capsule gland, of which a small distal part may be differentiated as reddish translucent capsule gland; additional simple loop of glandular material between capsule gland and terminal portion of pallial oviduct; small flexure of egg groove just before opening to mantle cavity; large copulatory bursa separates in a posterior position and continues back to overly capsule gland.

Spawn and development. Not recorded; pelagic spawn and planktotrophic development predicted from dimensions of protoconch and large capsule gland ( Reid, 1989).

Radula ( Fig. 17A,B). Relative radular length 4.1–7.6 (4.03, s.e. 0.33; Potter & Schleyer, 1991). Rachidian: length/width 1.19–1.48; major cusp elongate, rounded to pointed at tip. Lateral and inner marginal: major cusps large, elongate, bluntly rounded to truncate at tip. Outer marginal: 8–10 cusps (10–11; Potter & Schleyer, 1991).

Habitat. Afrolittorina africana dominates the upper shore on open coasts in the Transkei and Natal, reaching densities of up to 6000 m – 2 in the upper barnacle zone ( Dye, 1988). The vertical tidal range is wide, from mean low water of neap tide to the littoral fringe; recruitment occurs on the horizontal platforms of the lower shore and is followed by upward migration (Eyre & Stephenson, 1938; Potter, 1987; Potter & Schleyer, 1991). In Natal, the northern part of the range, the vertical distribution is shifted lower on the shore, perhaps as an effect of higher temperatures (Kilburn & Rippey, 1982; McQuaid & Sherman, 1988; McQuaid, 1992). At East London, where both A. africana and A. knysnaensis are common, the former dominates in the lower parts of the littorinid zone and extends slightly lower on the shore (Eyre et al., 1938). Although most abundant a range of rocky substrates on open coasts, the species can also be found in sheltered estuaries and on wooden posts ( Kilburn, 1972). Juveniles feed on bacteria and diatoms, and adults mainly on lichens and blue-green algae (Potter & Schleyer, 1991).

Range ( Fig. 18). southwestern Indian Ocean from near Cape Town to Natal, southern Mozambique and southeastern Madagascar. The range limits in South Africa are St James, False Bay (34°07'S 18°27'E, BMNH 20030448; Eyre, 1939) and Cape Vidal, Natal (28°08'S 32°33'E, BMNH 20030449), but the species is relatively uncommon (in comparison with the sympatric A. knysnaensis ) further south and east than Port St Johns (31°38'S 29°33'E; Hughes, 1979), and becomes rare at Cape Agulhas ( Stephenson, 1944). To the north of Cape Vidal there is a long stretch of unsuitable sandy coastline, but there are three records from southern Mozambique: Inhaca Island (26°02'S 32°58'S USNM 637363); Tofo (23°51'S 35°33'E, AMS); Morrungulo, near Massinga (23°15'S 35°22'E, NM G4627). The species just reaches southeastern Madagascar, where it is recorded from Ambovombe, (25°11'S 46°05'E, IRSNB) and Flacourt, Fort Dauphin (25°02'S 47°00'E, USNM 678834).

Remarks. This species is variable in shell characters and at least three intergrading forms can be recognized (see Kilburn, 1972, for discussion). The typical form is the largest, a turbinate shell with sculpture varying from incised lines to raised threads ( Fig. 16A,G–L). The colour is white with a broad blue-grey band from below the suture to below the periphery. In the northern part of the range (at Port St Johns, in Natal and Mozambique) this may be overlain by a faint, fine, tessellated pattern of yellow or pale brown ( Fig. 16G–I,K). The form described by Krauss as Litorina decollata is a small, low-spired shell with smooth surface, white with a broad blue-grey band, but no patterning ( Fig. 16B,C,F). Kilburn (1972) noted that the decollata form occurred both sporadically among populations of the typical form and in pure populations, and that its occurrence was not correlated with degree of wave exposure. In BMNH two collections from the same locality, Umngazana, suggest a different correlation. A sample from concrete walls (BMNH 20030418) at this open-coast locality is of the typical form, whereas a sample from flat surfaces and pools (BMNH 20030416) is of the decollata form. In members of the Echinolittorina aspera species group from the eastern Pacific, individuals in pools at the top of the eulittoral zone are stunted and more smooth than those on rocks in the littoral fringe ( Reid, 2002 a). Stunted individuals in pools have also been noted in Littoraria pintado pullata (Carpenter, 1864) ( Reid, 1999) . In both these cases, as in A. africana , the species has planktotrophic development, so that genotypic differentiation between the shell forms is unlikely and an ecophenotypic effect may explain this pattern of small-scale variation.

Another distinctive form with a strong pattern of brown spiral lines, zigzags and coarse tessellation was mentioned by both Kilburn (1972) and Hughes (1979). Specimens collected by Hughes at Umhlanga Rocks, Natal, are small (less than 5 mm), smooth, low-spired and of patulous shape ( Fig. 16D,E; BMNH 20030423). These were found in crevices and contrasted with the common typical form at the same locality (BMNH 20030424). The dimorphism of the shells at this locality is so striking that a pair of sympatric species might be suspected, yet no anatomical differences could be detected in the present study ( Fig. 16G–I). Hughes (1979) pointed out the parallel with the neglecta ecotype of Littorina saxatilis (Olivi, 1792) (equivalent to the “barnacle ecotype” of Reid, 1996). The interpretation of these specimens as an ecophenotype of A. africana is supported by the finding of identical sequences of the 12S mitochondrial gene in both (S.T. Williams, unpublished).

Distinction from the partially sympatric A. knysnaensis is described in the Remarks on that species.

Phylogenetic analysis of morphological characters identified A. africana and A. knysnaensis as sister species on the basis of the tall, secretory epithelium surrounding the mamilliform penial gland (which may serve the function of the absent subepithelial glandular disc), and this is a unique synapomorphy ( Reid, 2002 b). This relationship was supported by DNA-sequence analysis that estimated that the two species may have diverged more than 10 million years ago ( Williams et al., 2003). These two are in turn the sister group of the pair of Australian members of Afrolittorina , and the divergence time between the African and Australian pairs was estimated as 29–55 million years.