Nodilittorina pyramidalis (Quoy & Gaimard, 1833)

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 : 81-85

Nodilittorina pyramidalis (Quoy & Gaimard, 1833)

Figs. 2–3, 4A,B, 5

Littorina pyramidalis Quoy & Gaimard, 1833: 482–483 , pl. 33, figs. 12–13, figs. 14–15 (tentacles and foot) (Baie Jervis, Nouvelle-Hollande [Jervis Bay, New South Wales, Australia]; lectotype ( Rosewater, 1970) (fig. 2G), 1 dry paralectotype, 2 paralectotypes in alcohol, MNHNP, seen). Deshayes, 1843: 210. Reeve, 1857: Littorina sp. 14, pl. 2, fig. 14. Tenison Woods, 1879: 69–71.

Litorina pyramidalis .—Philippi, 1846:143, Litorina pl. 2, figs. 10, 12.

Tectarius pyramidalis .—Adams & Adams, 1854: 315. Angas, 1867: 209. Hedley, 1918: M51.

Littorina (Tectus) pyramidalis .— Nevill, 1885: 156.

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

Nodilittorina pyramidalis .— Abbott, 1954: 451, 456 (in part; includes Echinolittorina trochoides ). McMichael, 1959: 27. Iredale & McMichael, 1962: 38. Macpherson & Gabriel, 1962: 90, fig. 119 (in part; includes E. trochoides ). Wilson & Gillett, 1971: 30 (in part; pl. 11, fig. 11, 11a are E. trochoides ). Wilson & Gillett, 1979: 52 (in part; pl. 8, fig. 3 is E. trochoides ; pl. 8, fig. 3a is E. australis [ Gray, 1826]). Jansen, 1995: 31, fig. 95; Reid, 1998: 739, fig. 15.100B, E (oviduct). Reid, 2002 b: figs. 1A, 2B (penis). Williams et al., 2003.

Nodilittorina (Nodilittorina) pyramidalis pyramidalis . — Rosewater, 1970: 424, 481–484, pl. 325, figs. 24, 25, pl. 370, figs. 1, 2, 6, 7, pl. 372 (distribution) (in part; other figures are E. trochoides ).

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

2, fig. 2i, figs. 7k (penis), 10j (oviduct), 14l (radula). Wilson, 1993: 147 (in part; pl. 18, fig. 5a,b are E. trochoides ).

Litorina (Tectarius) nodulosa .—Weinkauff, 1882: 43–44, pl. 5, figs.

5–6 (not Trochus nodulosus Gmelin, 1791 = E. trochoides ). Weinkauff, 1883: 225 (as Tectaria ; not Gmelin, 1791).

Tectarius nodulosus .— Tryon, 1887: 258, pl. 48, fig. 72 (not Gmelin, 1791; in part; includes Echinolittorina tuberculata , E. trochoides , Tectarius antonii ).

Littorina nodulosa .— Etheridge, 1889: 24 (not Gmelin, 1791).

Tectaria nodulosa .—Tate & May, 1901: 389 (not Gmelin, 1791).

Nodilittorina nodulosa .— Fischer, 1967: 47–80 (not Gmelin, 1791; in part; includes E. trochoides ). Fischer, 1969: 119– 129 (not Gmelin, 1791; in part; includes E. trochoides ).

Tectarius tuberculatus .— Iredale, 1924: 243–244 (not Litorina tuberculata Menke, 1828 = Echinolittorina tuberculata ).

Nodilittorina tuberculata .— Allan, 1950: 80, textfig. 19: 7 (not Menke, 1828). Macpherson & Chapple, 1951: 118 (not Menke, 1828).

Taxonomic history. This species has a complex taxonomic history, as a result of the longstanding confusion of at least six littorinid species that have superficially similar nodulose shells. Gmelin (1791) based his Trochus nodulosus on two figures in Chemnitz (1781: pl. 163, figs. 1545, 1546) of shells obtained by Captain Cook in the South Seas. These have been interpreted as examples of the present species (Weinkauff, 1882), which does indeed occur at Cook’s landing place in Botany Bay ( Iredale, 1924). However, if the figure is an accurate representation, the tall spire with small white nodules, nodulose base, narrow columella and rounded anterior lip, together leave little doubt that the species is that now identified as Echinolittorina trochoides (see Remarks below), which could well have been obtained during Cook’s itinerary further north in Australia. Most subsequent authors failed to discriminate between N. pyramidalis , endemic to southeastern Australia, and E. trochoides , widespread in Indo-Malaya, and used the same name for both. Following Weinkauff (1882), some adopted the name nodulosa (e.g., Tryon, 1887; Fischer, 1967), overlooking the fact that it was unavailable, being a junior primary homonym of Trochus nodulosus Solander, 1766 . Iredale (1924) believed that the earliest available name was Litorina tuberculata Menke, 1828 , but this is a westernAtlantic species (included by Gmelin as variety “minor” of his T. nodulosus ; see discussion byAbbott, 1954; Bandel & Kadolsky, 1982). The first available name for a nodulose, western Pacific species is Littorina pyramidalis Quoy & Gaimard, 1833 and this has been widely used in the literature.

At first, the epithet pyramidalis was correctly applied, to include only the present species (Philippi, 1846; Reeve, 1857; Angas, 1867; Nevill, 1885; von Martens, 1897), but from the end of the nineteenth century a broader species concept began to prevail. Tryon (1887) considered that nodulose shells from the western Atlantic and western Pacific were indistinguishable and synonymized them as Tectarius nodulosus . Abbott (1954) used the name Nodilittorina pyramidalis for a supposed single species extending from India to Australia and the Far East (i.e. N. pyramidalis s. st. and E. trochoides ). A similar concept was adopted by Fischer (1967, as N. nodulosa ) and by Rosewater (1970, but with an additional subspecies N. pyramidalis pascua Rosewater, 1970 , on Easter Island, now regarded as a distinct species of Echinolittorina ). It is in this incorrect sense that the name N. pyramidalis has since been generally applied. Meanwhile, some Australian workers had correctly observed that two nodulose species occurred in eastern Australia. This was presumably the basis for the inclusion of both Tectarius malaccanus (Philippi, 1847) (= E. trochoides ) and T. nodulosus (presumably N. pyramidalis ) in Hedley’s (1910) list of Queensland shells.

Iredale & Allan (1940) and Endean et al. (1956) also remarked on the likely presence of two Nodilittorina species in eastern Australia, but without making any taxonomic recommendation. Nevertheless, it was only in 1989 that both N. pyramidalis and N. trochoides appeared in the list of worldwide Littorinidae ( Reid,1989; updated by Reid, 2002 b) and the latter was formally redescribed by Reid (1992, 2002 a). Although some of its characters have been illustrated in phylogenetic studies ( Reid, 1986, 1989, 2002 b; also Reid, 1998), the present account is the first full description of N. pyramidalis .

From the original figure, without locality or details, Littorina duplicata Deshayes, 1850 appears superficially similar to N. pyramidalis ; however, it is a fossil species probably belonging to the family Amberleyidae (based on examination of non-type specimens labelled Littorina duplicata in MNHNP).

Diagnosis. Shell large; two rows of prominent nodules on last whorl, nodules not axially aligned, no nodules on base; blue-grey; aperture brown with two cream bands. Penis with numerous minute mamilliform glands in swollen filament; single large mamilliform gland on base, but no distinct glandular disc. Pallial oviduct with two consecutive loops of egg groove, in albumen and capsule glands; copulatory bursa opens near anterior end of pallial oviduct.

Material examined. 94 lots (56 AMS, 9 USNM, 24 BMNH, 2 IRSNB, 2 ZMA, 1 NMW), including 18 penes, 4 sperm samples, 6 pallial oviducts, 3 radulae.

Shell ( Fig. 2). Mature shell height 8.6–26.8 mm. Shape highturbinate to conical (H/B = 1.23–1.46; SH = 1.59–2.02); shoulder of spire whorls with single row of pointed nodules; single row of nodules on shoulder and another at periphery of final whorl; moderately solid. Columella short, broad, excavated, slightly flared or projecting as a rounded lip anteriorly; eroded parietal area present. Sculpture of fine raised spiral threads over entire surface, 19–25 on final whorl, separated by grooves equal in width to threads, threads weaker towards centre of base; spiral microstriae cover surface, but are frequently eroded; two rows of prominent pointed nodules at shoulder and periphery of final whorl, each 12–25, but not strictly aligned along axial (prosocline) growth lines; axial growth lines prominent, closely spaced, becoming lamellose towards end of final whorl, with no consistent relation to nodules. Protoconch not well preserved, but about 0.4 mm diameter and about 3 whorls. Colour blue-grey, darker where eroded, with whitish nodules; aperture dark brown with two cream bands (corresponding with base and shoulder of whorl).

Animal. Head and sides of foot grey to black; tentacle with two broad (sometimes indistinct) black stripes, sometimes fused to become almost entirely black, pale at tip. Opercular ratio 0.54–0.63. Penis ( Fig. 3A–E): filament relatively short, 0.3–0.5 total length of penis, slightly pointed and usually swollen, sometimes reddish, no constriction differentiating filament from wrinkled base, filament bears numerous papillae (structurally, these are miniature mamilliform penial glands, with mucous reservoir and subepithelial glandular tissue; Reid, 1989); sperm groove open to tip; single large mamilliform gland in short lateral projection of base, surrounded by subepithelial glandular tissue homologous with penial glandular disc (but not separated as a distinct glandular flap, and sometimes only visible by histology); penis unpigmented; penis reduced in size from April to June, but not shed ( Underwood, 1974). Euspermatozoa 117–123 µm; paraspermatozoa ( Fig. 3I,J) are clusters of large spherical granules, 15–25 µm diameter, sometimes with short wedge-shaped or elongate rod bodies visible. Pallial oviduct ( Fig. 3F–H) 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, reddish when fresh; copulatory bursa confined to straight section of pallial oviduct, opening near anterior end.

Spawn and development. Not recorded, but protoconch and large capsule gland indicate pelagic spawn and planktotrophic development; from condition of ovary, spawning at a maximum in January and February ( Underwood, 1974).

Radula ( Fig. 4A,B). Relative radular length 2.3–4.0. Rachidian: length/width 1.25–1.80; major cusp elongate, rounded or pointed at tip. Lateral and inner marginal: major cusps large, elongate, bluntly rounded at tip. Outer marginal: 6–7 cusps.

Habitat. This species is common in the littoral fringe of rocky shores; it is the dominant mollusc above high water of spring tides, extending higher where splash and spray permit ( Endean et al., 1956) and exceptionally up to 12 m above sea level ( Dakin et al., 1948). It thus extends to higher levels than the sympatric Austrolittorina unifasciata , and occurs at lower densities (to 32 m –2 at Cape Banks, NSW; Branch & Branch, 1981). It occurs mainly on ocean coasts and is said to be more common on shores of moderate to high exposure to waves ( Endean et al., 1956), although it can sometimes be found on moderately sheltered shores in inlets and harbours. Quantitative study has failed to find a consistent correlation between density and wave exposure near Sydney ( Chapman, 1995a). On a small scale, the highest densities are associated with microhabitats of deep crevices, cracks and pits, whereas few occur on open rock surfaces ( Chapman, 1994b). Although largely restricted to the top of the shore, animals occur sporadically on the upper mid-shore, where pits and topographic irregularities allow ( Chapman, 1994b). Small specimens have been reported lower on the shore than adults ( Johnston, 1917) and are scarce, so that recruitment appears sparse and probably occurs mainly within pits in the rock ( Underwood, 1974; Chapman, 1994b; Chapman & Underwood, 1994). Dispersion and behaviour have been studied (Chapman & Underwood, 1994; Chapman, 1999).

Range ( Fig. 5). Eastern Australia, from easternmost Victoria to southern Queensland; Lord Howe Island and Norfolk Island. The only record from Victoria is from Mallacoota (37°33'S 149°47'E, AMS C50368; Bennett & Pope, 1953; Macpherson & Gabriel, 1962). The species is abundant along the entire length of the rocky coastline of New South Wales, and is also frequent in southern Queensland as far north as Noosa Heads (26°23'S 153°09'E, AMS C386700). Further north N. pyramidalis has been recorded from only four localities: Urangan, Hervey Bay (25°17'S 152°54'E, AMS C386710), Bustard Bay (24°05'S 151°48'E, AMS C62608), North Keppel Island (23°04'S 150°54'E, AMS C386762 plus 3 more lots) and Ocean Heads, Yeppoon (23°8.5'S 150°46'E, AMS C386768 plus 2 more lots). This species occurs at Lord Howe Island ( AMS C089673; BMNH 1925.5.7.1; USNM 684715; Iredale & Allan, 1940), but is said to be “not common” ( Etheridge, 1889, as Littorina nodulosa ). There is a single old record from Norfolk Island ( AMS C059382, A. Bell, 1910–1911).

Remarks. The shell does not show conspicuous variation ( Fig. 2). Statistically, there are significant differences in shape between shores, but this is not correlated with wave exposure, overall size or population density ( Chapman, 1995a). On one pair of shores at Cape Banks the shell aperture and foot were larger on the wave-exposed shore than on the more sheltered one, but it is not known if this is a general pattern ( Chapman, 1997).

The distributions of N. pyramidalis and the conchologically similar Echinolittorina trochoides are almost mutually exclusive in eastern Australia. The former is characteristic of the eastern overlap zone (Ponder & Wells, 1998), whereas the latter is a widespread tropical species. Based on a survey of the distribution of common intertidal organisms along the Queensland coast, Endean et al. (1956) placed the biogeographic boundary between shores of northern (tropical) and southern (temperate) character at 25°S (Hervey Bay). This is also the southernmost record of E. trochoides (AMS C386753, Point Vernon, Hervey Bay, 25°15'S 152°49'E). These two species have been recorded together at only two localities: Bustard Bay (24°05'S 151°48'E; although in two separate lots: N. pyamidalis AMS C 62608; E. trochoides AMS C 386794) and the Keppel Islands (23°04'S 150°54'E; three formerly mixed lots of the two species in AMS now separated and registered as: C106933 plus 386781, C089660 plus 386787, C386762 plus 386780, numbers of N. pyramidalis plus E. tochoides in these lots are: 31 plus 2, 60 plus 1, 54 plus 33, respectively). Endean et al. (1956) pointed out that this faunistic boundary was not correlated with temperature change and suggested that exposure to wave action was critical. South of 25°S the coast is exposed to strong surf and oceanic swells, whereas to the north it is largely sheltered by the Great Barrier Reef. Presumably other hydrographic factors, such as nutrients and productivity, are also connected with the contrast between oceanic and reef-sheltered coasts. The distribution of N. pyramidalis and E. trochoides north of 25°S does correlate to some extent with wave-exposure. Bustard Bay (where both have been recorded) is semi-exposed ( Endean et al., 1956), whereas in the shelter of nearby Port Curtis only E. trochoides has been found. Yeppoon (and presumably the adjacent Keppel Islands) is an exposed locality ( Endean et al., 1956). Nevertheless, in the southern parts of its range E. trochoides does occur in both exposed and sheltered localities. The seven collections of N. pyramidalis from Yeppoon and the Keppel Islands in AMS are not all precisely dated, but five are pre-1950 and two no later than 1966; it is not known whether this species can still be found there.

The discrimination of N. pyramidalis and E. trochoides is usually straightforward ( Table 2). Their geographical ranges barely overlap and anatomical features are diagnostic. In females, the loop of the egg groove through the capsule gland is present only in N. pyramidalis , whereas a forked copulatory bursa is unique to E. trochoides ( Reid, 1992: fig. 2i) In males, papillae on the penial filament and lack of a discrete glandular disc distinguish N. pyramidalis (cf. E. trochoides, Reid, 1992 : fig. 1j; Reid, 2002 b: fig. 2E). The larger, broader shell and produced anterior lip of N. pyramidalis are the most useful conchological characters, but small shells can be difficult to separate. In the northern parts of its range the shells of N. pyramidalis are smaller; those from Queensland rarely exceed 18 mm and in the three sympatric samples of N. pyramidalis and E. trochoides the largest of the 145 specimens of N. pyramidalis is only 14.8 mm. In these mixed samples the two species are mainly of similar size and separation requires careful examination of aperture shape, coloration and sculpture ( Table 2; for E. trochoides see Reid, 1992: pl. 3a–c; Reid, 2001: fig. 2G, H).

The largest shells of N. pyramidalis are found on Lord Howe Island, where sizes of greater than 23 mm are common.

The phylogenetic relationships of Nodilittorina pyramidalis remain unclear. In a recent analysis of DNAsequence data from two nuclear and two mitochondrial genes, Williams et al. (2003) showed only that it was a member of a large clade including the genera Tectarius , Austrolittorina , Cenchritis and Littoraria . Within this group, the most likely (but still weakly supported) positions were at the base of the clade, or as the sister-group of Tectarius . This latter possibility is intriguing, for it is supported by the unique feature of papillae on the penial filament, shared by N. pyramidalis and the subgenera Tectarius , Tectininus and Echininus of Tectarius (but not the subgenera Liralittorina or Echininiopsis ). Other features such as the form of the outer marginal radular teeth and the loop of the egg groove within the capsule gland, which had been interpreted as evidence for a relationship with Austrolittorina ( Reid, 2002 b) are now known to be convergent ( Williams et al., 2003).