Austrolittorina unifasciata ( Gray, 1826 )

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 : 86-92

Austrolittorina unifasciata ( Gray, 1826)

Figs. 4C,D, 6–8, 25A,B

Littorina unifasciata Gray, 1826: 483 ( Australia; restricted to King George Sound, Western Australia ( Rosewater, 1970); lectotype ( Rosewater, 1970) BMNH 1968373/1 (fig. 6A) plus 1 paralectotype BMNH 1968373/2, seen). Angas, 1865: 172. Tenison Woods, 1878: 36. Guiler, 1958: 139. Haacke, 1885: 504–505 (in part, includes Afrolittorina praetermissa ). Wilson & Gillett, 1979: 52, pl. 8, fig. 6, 6a.

Litorina unifasciata .— Menke, 1844: 57.

Melarhaphe unifasciata .— Iredale, 1915: 447 (in part; includes A. antipodum ). Hedley, 1916: 186 (as Melaraphe ). Hedley, 1918: M51. May, 1921: 48. May, 1923: 49, pl. 22, fig. 19. Cotton & Godfrey, 1938: 10. Macpherson & Chapple, 1951: 118 (as Melaraphe ). Kershaw, 1955: 307 (as Melaraphe ). Wilson & Gillett, 1971: 30, pl. 11, fig. 12, 12a (as Melaraphe ).

Melarapha unifasciata .— McMichael, 1959: 27. Macpherson & Gabriel, 1962: 87, fig. 115.

Littorina (Austrolittorina) unifasciata unifasciata .— Rosewater, 1970: 423, 467–470, pl. 325, figs. 17–18, 326, fig. 5, pl. 359, figs. 1–5, pl. 360, figs. 1–4, pl. 361, figs.A (radula), C (penis), pl. 362 (distribution).

Nodilittorina (Nodilittorina) unifasciata unifasciata .—Bandel & Kadolsky, 1982: 37.

Littorina (Austrolittorina) unifasciata .—Ludbrook & Gowlett- Holmes, 1989: 564, fig. 11.19j, k. Wilson, 1993: 146–147, pl.

18, fig. 3.

Nodilittorina (Nodilittorina) unifasciata .— Reid, 1989: 100, pl.

2, fig. 2j.

Nodilittorina unifasciata .— Jansen, 1995: 31, fig. 94. Reid, 1998: 739, fig. 15.100D (penis). Reid, 2002 b: fig. 1c.

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

Austrolittorina unifasciata .— Williams et al., 2003.

Littorina diemenensis Quoy & Gaimard, 1833: 479–480 ; pl. 33, figs. 8–10 (la partie sud de la Nouvelle-Hollande, de l’île de Van-Diémen et même de la Nouvelle-Zélande [southern Australia, Tasmania and New Zealand]; restricted to Tasmania ( Rosewater, 1970); lectotype ( Rosewater, 1970) MNHNP 10.2× 5.9 mm plus 11 dry paralectotypes plus 11 dry paralectotypes plus 82 alcohol paralectotypes plus 39 alcohol paralectotypes, all MNHNP, seen; in part; from locality New Zealand, includes L. antipodum ). Deshayes, 1843: 209. Reeve, 1858: Littorina sp. 94, pl. 17, fig. 94. Nevill, 1885: 141.

Littorina (Melarhaphe) diemenensis .—Adams & Adams, 1854: 314 (as Melaraphe ).

Melarapha diemenensis .—Iredale & McMichael, 1962: 38.

Litorina acuta Menke, 1843: 9 (Western Australia; types presumed lost; synonymized with Littorina unifasciata Gray, 1826 , by Menke, 1844).

Litorina mauritiana .—Philippi, 1847: 165; Litorina pl. 3, fig. 17a (not Phasianella mauritiana Lamarck, 1822 = Littoraria mauritiana ; in part; figs. 15 and 17b are Echinolittorina ziczac ( Gmelin, 1791) , also includes Littoraria mauritiana ). Weinkauff, 1882: 97–98 (not Lamarck, 1822; pl. 14, fig. 4 is E. ziczac ; also includes L. mauritiana ). Weinkauff, 1883: 220 (not Lamarck, 1882; in part; includes L. mauritiana ). Watson, 1886: 574 (not Lamarck, 1822; in part; includes L. mauritiana ). Verco, 1908: 8 (not Lamarck, 1822). Hedley, 1910: 355.

Littorina mauritiana .—Reeve,1858: Littorina sp. 100 (not Lamarck, 1822; in part; fig. 100 is Echinolittorina ziczac ( Gmelin, 1791) , also includes Littoraria mauritiana ). Angas, 1867: 209 (not Lamarck, 1822; in part; includes Littoraria mauritiana ). Smith, 1884:60–61 (not Lamarck, 1822; in part; includes Austrolittorina antipodum ). Gatliff, 1887: 60 (not Lamarck, 1822). Tate & May, 1901: 389 (in part; includes Afrolittorina praetermissa ). Pritchard & Gatliff, 1902: 909–91 (not Lamarck, 1822; in part; includes Littoraria mauritiana , A. antipodum ).

Littorina (Melarhaphe) mauritiana .— Tryon, 1887: 247, pl. 44, figs.

72, 73, 75 (as Melaraphe ; not Lamarck, 1822; in part; figs. 70, 74 are A. cincta ; fig. 71 is E. ziczac ; also includes A. antipodum , L. mauritiana ).

Littorina diemenensis var. mauritiana .— Etheridge, 1889: 24 (not Lamarck, 1822).

Melarhaphe mauritiana .— Iredale, 1912: 223 (not Lamarck, 1822).

Litorina diemensis Philippi, 1847:195 , 196, Litorina pl. 4, fig. 1 (unjustified emendation of Littorina diemenensis Quoy & Gaimard, 1833 , because original spelling is quoted, and emended spelling is used twice and in index; in part; includes Austrolittorina antipodum ). Küster, 1856: 18, pl. 2, figs. 23–24 (in part; includes A. antipodum ). Weinkauff, 1878: 31. Weinkauff, 1883: 218 (in part; includes A. antipodum , A. cincta , Echinolittorina novaezelandiae [ Reeve, 1857]).

Litorina mauritiana var. crassior Philippi, 1847: 165 ; Litorina pl. 3, figs. 15, 17a [ Cuba (fig. 15); other localities mentioned (not specifically for var. crassior ) are Mauritius; Nova Hollandia ( Australia); Ducee’s Island (Ducie Island); restricted to Australia ( Rosewater, 1970); lectotype (here designated) Philippi, 1847: fig. 17 (left; 17a in text); in part; fig. 15 is said to come from Cuba and therefore probably Echinolittorina ziczac ( Gmelin, 1791) , probably also includes Littoraria mauritiana ( Lamarck, 1822) ].

Littorina africana .— Reeve, 1857: Littorina sp. 37, pl. 8, figs. 37a,b (not Krauss, in Philippi, 1847; in part; includes Afrolittorina africana ).

Littorina laevis .—Reeve, 1858: Littorina sp. 95, pl. 17, fig. 95 (not Philippi, 1846 = Littoraria mauritiana ).

Littorina caerulescens .— Tenison Woods, 1879: 65–72 (as coerulescens; not Turbo caerulescens Lamarck, 1822 = Melarhaphe neritoides (Linnaeus, 1758) ; in part; includes A. antipodum , Afrolittorina praetermissa , A. africana , Littoraria mauritiana , L. undulata (Gray, 1839) , M. neritoides ).

Littorina diemenensis var. pseudolaevis Nevill,1885: 141 (New South Wales; Port Jackson [ Sydney Harbour , New South Wales]; types in ZSI, not seen).

Taxonomic history. This species has a complex taxonomic history, owing to longstanding confusion with several littorinids with similar smooth, white shells. Although the species was first described by Gray in 1826, for the rest of the century the name Littorina unifasciata was generally considered a junior synonym of Littorina mauritiana . The misidentification of the present species as L. mauritiana originated with Philippi (1847), who was deceived by Lamarck’s (1822) inadequate description of Phasianella mauritiana and by Delessert’s (1841) poor figure of one of Lamarck’s shells, which does indeed resemble A. unifasciata . The species described by Lamarck (1822) is an endemic of Mauritius and the southwestern Indian Ocean, as correctly recognized by Nevill (1885; see Rosewater, 1970, for detailed discussion and lectotype designation), and now classified as a species of Littoraria ( Reid, 1986) . Philippi’s (1847) concept of Litorina mauritiana may not have included actual specimens of Littoraria mauritiana (although he did refer to Delessert’s figure), because he had himself described that species as Littorina laevis Philippi, 1846 , from an unknown locality, and figured it accurately in his monograph (Philippi, 1847: Litorina pl. 6, fig. 6). Nevertheless, his concept did not include A. unifasciata alone. He recognized two named varieties, Litorina mauritiana var. crassior and var. gracilior . One of the two figures of var. crassior (fig. 17a) is a typical shell of A. unifasciata , but the other (fig. 15) was said to come from Cuba. The latter figure is indeterminate, but if the locality is correct then it can only be Echinolittorina ziczac . Philippi’s var. gracilior was illustrated by a single figure (fig. 17b); the original shell from the Cuming Collection has been discovered in the BMNH and is undoubtedly a specimen of E. ziczac , distinguished by its elongate shape, almost smooth surface and two white bands within the aperture. Shells of E. ziczac with the normal zigzag pattern are distinctive, but occasional white shells such as this one do bear a superficial resemblance to A. unifasciata . An incomplete accompanying label in Philippi’s hand bears the name L. mauritiana from the Isle of Jua—”.

This is interpreted as “Juan Fernández”, and the two other specimens in the syntypic series are probably A. fernandezensis (distinction from A. unifasciata based on shells alone is sometimes impossible). It appears, then, that Philippi based his L. mauritiana var. gracilior on a mixture of E. ziczac and A. fernandezensis , both of which are indeed usually more elongate than typical A. unifasciata . It is curious that neither the locality nor Cuming are mentioned by Philippi in his brief remark on var. gracilior . However, among the localities for Litorina mauritiana he lists “insula Ducee’s in Oc. Pacifico (Cuming)”. This is a reference to Ducie Island in Polynesia, where none of these species occurs. Conceivably, Philippi may have confused the two Pacific localities of Ducie Island and the Juan Fernández Islands. Following Philippi’s (1847) misuse of the name L. mauritiana , the name was generally applied to theAustralian species and unifasciata only returned to common use after the differences between the species of Gray and Lamarck were pointed out by Iredale (1915).

Austrolittorina unifasciata has also sometimes been known by the name Littorina diemenensis Quoy & Gaimard, 1833 . These authors described their species from Australia, l’île de Van-Diémen (i.e. Tasmania) and New Zealand, and therefore must have included not only A. unifasciata but also A. antipodum , for only the latter occurs in New Zealand. However, all known type specimens are A. unifasciata , in agreement with the type locality that was restricted to Tasmania by Rosewater (1970). Philippi (1847) accepted L. diemenensis as a distinct species (and was followed by Küster, 1856; Weinkauff, 1878, 1883), but distinguished it from his concept of L. mauritiana only by its smaller size. Philippi also described a still smaller species, found only in New Zealand, as Litorina antipodum . Nevertheless, confusion between A. unifasciata and A. antipodum continued and the two were considered conspecific by several subsequent authors (see Taxonomic History of A. antipodum ).

The white-shelled, mainly large, Southern Hemisphere littorinids have often been combined as a single species. Tenison Woods (1879) first expressed this view, and in its most extreme form, combining A. unifasciata , A. antipodum , Afrolittorina praetermissa , Afrolittorina africana , Littoraria mauritiana and even the European Melarhaphe neritoides into a single taxon for which he used the name Littorina caerulescens (= M. neritoides ). This choice of name was justified by quoting Deshayes (1843), although in fact the quote was from Quoy & Gaimard (1833), who compared their L. diemenensis with L. caerulescens and concluded that they were distinct. Tryon (1887) also had a broad concept, including A. unifasciata , A. antipodum , A. cincta and Littoraria mauritiana under the name Littorina mauritiana . In his monograph of the Indo-Pacific members of the family, Rosewater (1970) recognized three subspecies of Littorina unifasciata , the typical one from Australia, subsp. antipodum from New Zealand, and subsp. fernandezensis from the Juan Fernández Islands. Kilburn (1972) went further, suggesting that Afrolittorina africana was probably an additional subspecies of this supposed circumpolar taxon. Only in 1989 were these taxa all listed as distinct species, although without formal redescription ( Reid, 1989).

The types of Nevill’s var. pseudolaevis have not been examined, but he cited Reeve’s (1858) fig. 95, which is L. unifasciata .

Bandel & Kadolsky (1982) included Litorina cubana Weinkauff, 1882 in the synonymy of L. unifasciata , citing the spiral sculpture and lack of colour markings, and accordingly corrected its type locality to Australia. However, the original description also mentioned a turreted spire and two pale bands within a brown aperture; these features are never seen in L. unifasciata , and unequivocally identify this species as Echinolittorina ziczac . This western Atlantic species does occasionally show spiral striae and absence of colour pattern, and it occurs in Cuba. The original figure of Weinkauff (1882: pl. 9, figs. 2–3) is unrecognizable, and types are presumed lost, but the author cited plate 3, figure 17 of Philippi (1847), which is of L. unifasciata and E. ziczac , as discussed above.

Diagnosis. Shell moderately large; sculpture of spiral striae; white with indistinct broad band of blue-grey above periphery. Penis with broad, wrinkled filament; glandular disc and mamilliform gland on base. Pallial oviduct with two consecutive loops of egg groove, in albumen and capsule glands.

Material examined. 167 lots (108 AMS, 31 USNM, 19 BMNH, 2 IRSNB, 3 ZMA, 2 MNHNP, 2 NMW), including 18 penes, 7 sperm samples, 7 pallial oviducts, 4 radulae.

Shell ( Fig. 6, 25A,B). Mature shell height 3 ( Nwe, 1974) to 24.9 mm. Shape turbinate to tall-spired (H/B = 1.23–1.83; SH = 1.25–2.16); spire outline straight to slightly convex; whorls gently rounded, suture slightly impressed, periphery slightly angled; solid. Columella pillar slightly concave; columella slightly excavated; eroded parietal area present; outer lip of aperture usually minutely lirate just within margin. Sculpture of 10–12 primary spiral grooves above periphery, that remain as equidistant incised lines throughout growth of shell, continuing faintly on base, occasionally becoming obsolete on final whorl; strong spiral microstriae cover surface; surface, especially spire, often eroded; growth lines weak. Protoconch rarely preserved, 0.36 mm diameter, 3 whorls. Colour white with a more or less distinct broad band of blue-grey above periphery; apex brownish, second and third whorls of teleoconch marked by 5–9 fine spiral brown lines on grey ground ( Fig. 25A,B), but lined pattern always disappears on larger shells; aperture dark brown with basal white band.

Animal. Head and sides of foot black; tentacles grey to black, usually with indistinct transverse lines, sometimes a paler longitudinal streak, unpigmented around eye only. Opercular ratio 0.37–0.53. Penis ( Fig. 7A–F): filament approximately 0.6–0.7 total length of penis, but not distinctly demarcated from wrinkled base, broad, sometimes swollen, bluntly pointed, surface with reticulate wrinkles (in life and preserved); sperm groove opens subterminally; single large, often narrow, mamilliform gland and adjacent flap of penial glandular disc borne together on lateral branch of base; penis unpigmented; penis does not show annual regression ( Nwe, 1974; Underwood, 1974). Euspermatozoa 61–69 µm; paraspermatozoa ( Fig. 7I,J) are spherical clusters of large spherical granules, 13–17 µm diameter, usually with 1–2 rod bodies of short cylindrical or arcuate or irregular shape (occasionally indistinct or possibly absent), not projecting from cell. Pallial oviduct ( Fig. 7G) with simple loop of albumen gland, followed by large, almost circular loop of capsule gland, opaque pink, within which portion adjacent to egg groove (translucent capsule gland) is differentiated as a ring; copulatory bursa confined to straight section of pallial oviduct, opening near anterior end.

Spawn and development. Spawn ( Fig. 7H) a transparent pelagic capsule 240 µm diameter containing a single ovum 100 µm diameter, capsule with roughened dome surrounded by circumferential skirt with median ridge described from Sydney by Rudman (1996); smaller capsules 100–140 µm, with ovum 80 µm, described from vicinity of Adelaide by Nwe (1974); development planktotrophic; breeding throughout the year near Adelaide ( Nwe, 1974); year-round recruitment recorded in Tasmania (Chen & Richardson, 1987); females mature from October to May at Cape Banks ( NSW) with peak spawning from December to March ( Underwood, 1974).

Radula ( Fig. 4C,D). Relative radular length 3.5–4.8. Rachidian: length/width 1.21–1.62; major cusp elongate, rounded at tip. Lateral and inner marginal: major cusps large, elongate, bluntly rounded at tip or rectangular. Outer marginal: 6–8 cusps.

Habitat. This species is ubiquitous and abundant on most of the temperate shores of Australia and has been included in numerous ecological surveys and field experiments. It can be found on any hard substrate, including schist, granite, sedimentary rock, concrete and even wooden piers ( Nwe, 1974). On exposed coasts it is abundant in the littoral fringe up to the highest level of spring tides (reaching higher levels with stronger wave action) and in the upper barnacle zone, whereas juveniles are present at lower levels among barnacles and Pyura ( Dakin et al., 1948; Guiler, 1951; Bennett & Pope, 1953, 1960; Underwood, 1981; Wells, 1984; Chen & Richardson, 1987). On sheltered shores it extends lower, almost to low water of neap tides ( Endean et al., 1956), but is absent from sites of extreme shelter ( Guiler, 1952a; Womersley & Edmonds, 1958; Branch & Branch, 1981). Densities can be remarkably high on shores of moderate exposure (to 9600 m 2 at Cape Banks, NSW), resulting in extreme intraspecific competition for food ( Branch & Branch, 1981). On a small scale, the species shows a patchy distribution both within and between shores, but some trends have been identified: snails are largest in the upper and lowermost parts of the tidal range, and density is negatively correlated with size; animals are clustered in pits and crevices, and are more common on horizontal surfaces and where barnacles are present; there is no relation between density and exposure of the shore ( Britton et al., 1991; Chapman, 1994a; Underwood & Chapman, 1996). The food consists of microalgae, sporelings and lichens ( Branch & Branch, 1981; Jernakoff, 1983). Detailed studies of movement (Underwood & Chapman, 1985, 1989), foraging ( Chapman, 2000), behaviour following transplant ( Chapman, 1986, 1999), dispersion in relation to microtopography (Underwood & Chapman, 1989, 1992) and aggregation behaviour ( Chapman, 1995b, 1998; Chapman & Underwood, 1996) have been done in New South Wales. Over its extensive geographical range, it is microsympatric with N. pyramidalis in New South Wales and southern Queensland (but that species extends higher in the littoral fringe), with Afrolittorina praetermissa in Victoria, Tasmania and South Australia (but that species occurs at lower levels, in more cryptic habitats, and is common on more sheltered shores), and with Echinolittorina australis ( Gray, 1826) in Western Australia.

Range ( Fig. 8). Temperate and subtropical coastline of Australia, Tasmania and Lord Howe Island. In Western Australia there are numerous records as far north as North West Cape (21°45'S 114°10'E, AMS C387269), which was given as the northwestern limit of this species by Wells (1980), and a single specimen from Barrow Island is present in WAM (F.E. Wells, pers. comm.). There is a record from still further north at Cape Keraudren (19°57'S 119°45'E, coll. F. Haddrill, 1976, AMS C389557), but this is considered doubtful (F.E. Wells, pers. comm.). A lot from Vansittart Bay in the far north of WA (Coll. W. Burrows, AMS C45183) is certainly unreliable (this may perhaps be the source of the northwestern extralimital record on the distribution map by Rosewater, 1970: pl. 362). There are no records from the Great Australian Bight between the Archipelago of the Recherche, WA (34°15'S 112°50'E, AMS C69337) and Point Sinclair, SA (32°06'S 133°00'E, AMS C387947), but this is probably a collecting artefact resulting from the inaccessibility of this coastline. Further east there are abundant records from the coastlines of South Australia, Victoria, Tasmania and New South Wales, as far north as Point Cartwright and Noosa Heads in southern Queensland (26°23'S 153°09'E, AMS C386963, C107999). Endean et al. (1956) noted that the northern limit in Queensland was associated with wave action; at Noosa and southwards the species was abundant on exposed shores, but to the north it was replaced on sheltered shores by Echinolittorina vidua (Gould, 1859) (as Melarhaphe melanacme ). Only a single reliable lot has been seen from further north, at Yeppoon (23°08'S 158°44'E, 6 specimens, collected in 1952, AMS C387974), and this is also an exposed locality; to the north the coast is sheltered by the Great Barrier Reef. Rosewater (1970: pl. 362) plotted a record in the vicinity of Cooktown, but gave no details in the text and this record is considered unreliable. The species is common on Lord Howe Island (5 lots AMS, 3 lots BMNH), where shells reach unusually large size, and there is a single record from Elizabeth Reef (29°56'S 159°04'E, USNM 767443, not seen). In Tasmania it is common on the east coast and islands of Bass Strait, sporadic on the sheltered north coast and in the south, but is absent from the exposed west coast (Bennett & Pope, 1960; contrary to Kershaw, 1958, who may have confused the species with Afrolittorina praetermissa ). Whether this absence from western Tasmania is a consequence of the strong exposure, or of the low sea temperatures produced by the cold current of the West Wind Drift, is not known.

Remarks. The size and shape of the shell show significant variation ( Fig. 6). Size gradients on the shore have been mentioned above; adult size has been said to be larger in either sheltered ( Nwe, 1974) or exposed sites ( Branch & Branch, 1981), but no consistent correlation of size with wave-exposure was found in a well-replicated survey of shores at Cape Banks, New South Wales ( Chapman, 1994a). As in many littorinids, sexual dimorphism has been reported, the males being smaller ( Nwe, 1974). An early study at a single site reported a relatively larger shell aperture on the exposed side of a wall (Bassingthwaighte & Foulds, 1985), but although supported by at least one comparison between shores of contrasting exposure ( Chapman, 1997), this may not be a general pattern ( McMahon, 1992). Indeed, Chapman (1995a) emphasized that variation in shape within shores was as great as that between shores, and found no consistent correlations with density, size or exposure; the only consistent pattern was a decrease in relative aperture size at higher levels on the shore. Functional interpretations of intraspecific variation in littoral gastropods have suggested that tall shells with small apertures contain and conserve larger reserves of water, that these are more resistant to crushing by predators, and that enlarged apertures improve tenacity when wave action is strong. However, experimental tests failed to support these suggestions for A. unifasciata ( Chapman, 1997) . The planktotrophic mode of larval development implies high gene flow within and between nearby shores, so it is likely that the differences described are the result of phenotypic plasticity rather than genotypic adaptation ( McMahon, 1992; Chapman, 1995a). One possibility is a direct effect of growth rate (determined by time available for feeding) on shell shape; slower growth at high levels on the shore might produce the more elongate form ( Chapman, 1997).

This well-known species is unlikely to be confused with any of the littorinids with which it is sympatric. Shells of A. fernandezensis , endemic to the Juan Fernández and Desventuradas Islands off Chile, are so similar that they are sometimes indistinguishable; usually they are slightly more elongate than A. unifasciata and the margin of the aperture is more distinctly lirate. Shells of A. antipodum , found in New Zealand, are smaller, more tall-spired and have a more pronounced bluish peripheral band (see Remarks on A. antipodum ). The penes of all three species are diagnostic.

The molecular analysis of Williams et al. (2003) showed that the sister species of A. unifasciata is A. fernandezensis . The authors explained this interesting trans-Pacific relationship as a case of dispersal from Australia to the east, because the estimated age of the divergence (13–30 million years) was later than the breakup of Gondwana that might have provided a vicariant explanation. They did, however, point out that the distance across the Pacific is too great for larval dispersal under the present-day current regime, so that it may have been accomplished by use of formerly emergent seamounts as stepping stones.