Echinolittorina vermeiji ( Bandel & Kadolsky, 1982 )

Reid, David G., 2009, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean 2184, Zootaxa 2184 (1), pp. 1-103 : 79-83

Echinolittorina vermeiji ( Bandel & Kadolsky, 1982)

( Figures 13 , 33G, H , 35 , 36 )

Litorina (Hamus) nodulosa — Watson, 1886: 577–578 (in part, includes E. tuberculata ; not Gmelin, 1791 = E. pascua or E. malaccana group).

Littorina trochiformis var.? E.A. Smith, 1890b: 491 (not Dillwyn, 1817 = a Pacific species).

Tectarius trochiformis — Morretes, 1949: 70 (not Dillwyn, 1817).

Nodilittorina tuberculata helenae — Lopes & Alvarenga, 1955: 164–165, pl. 2, figs 22, 23 (not E.A. Smith, 1890a = E. helenae ). Matthews & Rios, 1967: 68 (not E.A. Smith, 1890a). Matthews & Kempf, 1970: 20 (not E.A. Smith, 1890a).

Nodilittorina (Echinolittorina) tuberculata helenae — Matthews, 1968: 185 (not E.A. Smith, 1890a). Rios, 1970: 33, pl. 6 (not E.A. Smith, 1890a). Rios, 1975: 33, pl. 9, fig. 109 (not E.A. Smith, 1890a).

Nodilittorina helenae ssp. Vermeij, 1972a: 89–101. Vermeij, 1972b: 694.

Nodilittorina (Granulilittorina) miliaris — Rosewater, 1975: 10–11 (in part, includes E. miliaris , E. granosa , E. helenae , Tectarius striatus ).

Nodilittorina (Granulilittorina) miliaris miliaris — Rosewater, 1981: 33–34 (in part, includes E. miliaris ).

Nodilittorina (Echinolittorina) miliaris — Reid, 1989: 99 (in part, includes E. miliaris , E. helenae ).

Nodilittorina (Nodilittorina) vermeiji Bandel & Kadolsky, 1982: 31–32 , figs 5 (shell, operculum, radula), 10 (map), 46–48 (shell and radula) ( Baia de Sueste , Isla Fernando de Noronha, 540 km NE Recife, Brazil; holotype USNM 749819, seen, Fig. 35A herein; 6 paratypes USNM 749820; 11 paratypes BMNH 1887.2.9.1831–3, 1888.6.27.52–5, 1889.2.21.63-6, all seen).

Nodilittorina vermeiji — Rios, 1985: 35, pl. 14, fig. 147. Calvo, 1987: 85–87, fig. 86 (radula). Leal, 1991: 70–71, pl. 1, fig. 1. Rios, 1994: 49, pl. 15, fig. 168. Reid, 2002a: 259–281.

Echinolittorina vermeiji — Williams, Reid & Littlewood, 2003: 60–86. Williams & Reid, 2004: 2227–2251, fig. 6F (map).

Nodilittorina tuberculata — García-Talavera, 1983: 44, 45, 351 (in part, includes E. tuberculata , E. miliaris , E. helenae , E. granosa , Tectarius striatus ; not Menke, 1828).

Taxonomic history: When a nodulose littorinid was first recorded from Fernando de Noronha it was identified as the Caribbean species then known as L. nodulosa (i.e. E. tuberculata , see Taxonomic History of that species) ( Watson 1886) or as a variety of it ( Smith 1890b). Later it was widely identified with L. helenae , which had been described from St Helena ( Smith 1890a) and was usually considered as a subspecies of E. tuberculata (e.g. Lopes & Alvarenga 1955; Matthews & Rios 1967; Rios 1970, 1975; Vermeij 1972a). Rosewater (1975) synonymized all the littorinids of the tropical Atlantic islands (including E. vermeiji , E. miliaris , E. helenae and E. granosa ) under N. miliaris . Subsequently he refined the concept of N. miliaris , separating helenae as a subspecies and provisionally retaining the form from Fernando de Noronha and Trindade in the nominotypical subspecies, originally described from Ascension Island ( Rosewater 1981). García-Talavera (1983) considered that there was but a single nodulose species throughout the tropical Atlantic, N. tuberculata . The present species was named by Bandel & Kadolsky (1982) and distinguished from both E. miliaris and E. helenae . Reid (1989) synonymized all three taxa as N. miliaris because of their variable shells and similar anatomy. However, these were reinstated when small differences in penial form were discovered ( Reid 2002a). DNA sequence data have since supported their recognition as distinct species ( Williams & Reid 2004).

Diagnosis: Shell medium size; sculptured with 2–4 rows of rounded nodules. Penis with large but narrow glandular disc, four times size of adjacent mamilliform gland, filament long and blade-shaped. Atlantic islands off Brazil (Atol das Rocas, Fernando de Noronha, Trindade). COI: GenBank AJ623061 .

Material examined: 23 lots (including 8 penes, 8 pallial oviducts, 4 radulae).

Shell ( Fig. 35 ): Mature shell height 7.6–20.1 mm. Shape turbinate to high turbinate (H/B = 1.17–1.48, SH = 1.40–1.86); spire whorls rounded; suture distinct; spire profile straight to slightly concave; periphery of last whorl rounded or angled. Columella short, wide, hollowed and pinched at base, anterior lip may be slightly produced; eroded parietal and columellar area. Sculpture on spire whorls of 3 spiral rows of nodules, overlain with fine spiral threads, nodules axially aligned; on last whorl usually 4 spiral rows of rounded nodules, of which two peripheral rows (just above and at, or slightly below, periphery) may fuse to form a single row of larger nodules, Fig. 35C, D ); if eroded only peripheral row of nodules may be visible; base with 4–6 cords of which 2 may bear small nodules; narrow spiral threads cover entire surface together with fine spiral microstriae; very large (gerontic) shells become more elongate (suture drops below periphery), primary nodules become smaller (occasionally obsolete) while 1–2 rows of small secondary nodules may develop above periphery ( Fig. 35L ). Protoconch not seen. Ground colour dark brown to black, fading to grey, pale band on base, nodules white; occasionally entire shell black but for white band on base; in gerontic shells with obsolete sculpture the position of the nodules is marked by white spots, giving an oblique tessellated pattern ( Fig. 35L ); aperture dark brown to black with pale band at base; columella purple brown.

Animal: Head black; tentacle pale around eye and at inside of base, with two broad longitudinal black stripes, sometimes fused giving black tentacle with white tip; sides of foot black. Opercular ratio 0.53–0.64, central part sometimes thickened. Penis ( Fig. 36A–F ): filament long, about two-thirds total length of penis, with annular wrinkles for most or part of its length (so not clearly differentiated from wrinkled base), broadening distally (i.e. blade-shaped), sperm groove ends terminally; mamilliform gland less than onequarter size of large but narrow penial glandular disc with folded edge, borne together on large projection of base; penis unpigmented or pigmented at base. Sperm not seen. Pallial oviduct ( Fig. 35G ): copulatory bursa separates at posterior end of straight section and extends back between albumen and capsule glands; additional glandular material present in a swelling around egg groove at anterior end of straight section. Spawn not known; pelagic capsules predicted from form of pallial oviduct ( Reid 2002a).

Radula ( Fig. 33G, H ): Relative radula length 5.94–6.43. Rachidian: length/width 1.47–1.84; tip of major cusp rounded. Lateral and inner marginal: 4 cusps, tip of major cusp rounded. Outer marginal: 8–9(10) cusps.

Range ( Fig. 13 ): Atlantic islands off Brazil. Range limits: Ilha do Cemitério, Atol das Rocas, Brazil ( BMNH 1989064 ) ; Buraco da Raquel , Fernando de Noronha, Brazil ( MZSP 31398 ) ; Bahia de Sueste, Fernando de Noronha , Brazil ( BMNH; USNM 749820 ) ; Ensenada dos Portugueses, Ilha da Trindade , Brazil ( BMNH 1989066 ; MNHN) .

This species has not been recorded from the mainland of Brazil.

Habitat: In littoral fringe and upper eulittoral on volcanic and limestone rocks, on oceanic islands.

Little is known of the ecology of this species. Fernando de Noronha is a volcanic island in the path of the South Equatorial Current, with clear, oceanic water; the shores are devoid of barnacles, oysters and dense algal cover, but the mytilid Brachidontes is present; E. vermeiji ranges from the littoral fringe down to the lower mid-eulittoral ( Eston et al. 1986). Vermeij (1972a) recorded a similar zonation level, and noted an increase in size higher on the shore ( Vermeij 1972b).

Remarks: This is the sister species of E. tuberculata ( Williams & Reid 2004) . Reciprocal monophyly is supported by 12S sequences, but only single sequences are available for COI and 28S ( Williams & Reid 2004). The average K2P genetic distance for COI is 12.75%, which is large for sister species. Both are oceanic species, and their distributions are separated by the Amazonian outflow and long stretches of sedimentary coastline on the South American mainland. The absence of E. vermeiji from the Brazilian mainland (just 270 km from Atol das Rocas, well within the range of planktonic larval dispersal for Echinolittorina ; Reid 2007) emphasizes the oceanic character of this species. Vermeij & Rosenberg (1993) considered E. vermeiji to be most similar to the West African E. granosa and therefore predicted that the former was derived from an eastern Atlantic ancestor. However, a parsimony argument supports a western Atlantic distribution of the common ancestor with E. tuberculata ( Williams & Reid 2004) .

Genetic data are available from Atol das Rocas alone ( Williams & Reid 2004), only about 300 km from the archipelago of Fernando Noronha. The island of Trindade lies 2000 km to the southeast. Although specimens from Trindade are not morphologically distinct from those from the other two island groups, this distance is at the limit of the known range of dispersal across open water of Echinolittorina species ( Reid 2007) , so conspecificity should be tested. Nevertheless, the westward-flowing South Equatorial Current and southward Brazil Current provide a potential route of larvae from the two northern archipelagos to Trindade.

The shell shows a range of variation similar to that of E. tuberculata , from broad to tall, rounded to angled at periphery, and with nodules more or less developed. Unlike E. tuberculata , the nodules are never sharp or spinose, there is no pseudumbilicus, and the nodules are often strikingly white on a black shell. The penial form differs; in E. vermeiji the filament is blade-shaped, the penial glandular disc is a long, narrow, undulating flange, and the lateral branch bearing the glands is longer. The radula differs from that of E. tuberculata , showing more rounded cusps and a broader rachidian; it is unknown whether it shows a similar degree of variation.

Among other Atlantic species, shells are also similar to the nodulose species in the eastern Atlantic, E. miliaris , E. helenae and E. granosa ; these are limited respectively to Ascension Island, St Helena and the African mainland (and islands in the Gulf of Guinea). These three form a monophyletic group that is sister to E. tuberculata and E. vermeiji . Shells are too variable to be reliably distinctive (e.g. Rosewater 1981; Bandel & Kadolsky 1982), but there are small differences in penial form among the three, and none shows the long blade-shaped filament of E. vermeiji .

Both Vermeij (1972a) and Eston et al. (1986) noted the unusually wide zonation on the shore, from the littoral fringe to the lower mid-eulittoral. This cannot be explained by an absence of predators, because three rapanine gastropods have been recorded at Fernando de Noronha ( Eston et al. 1986). This is, however, the only littorinid present, and so may extend its range downwards in the absence of competition. Yipp & Carefoot (1988) have shown that the zonation level of E. tuberculata expands downwards after removal of other littorinids on shores in Barbados.

Figures

FIGURE 13. Distribution of Echinolittorina lineolata (solid circles) and E. vermeiji (solid triangles).

FIGURE 33. Radulae of Echinolittorina species (two views of each radula, flat and at 45°). A–F, E. tuberculata. A, B, normal form; Antigua (BMNH 20081058; shell H = 11.9 mm). C, D, Intermediate form; Oracabessa, Jamaica (BMNH 20081059; shell H = 12.9 mm). E, F, Narrowed form; Silver Sands, Christ Church, Barbados (BMNH 20081039; shell H = 12.7 mm). G, H, E. vermeiji; Buraco da Raquel, Fernando de Noronha, Brazil (MZSP 31398; shell H = 15.5 mm). Scale bars = 50 µm.

FIGURE 35. Echinolittorina vermeiji. A, Nodilittorina (Nodilittorina) vermeiji Bandel & Kadolsky, 1982, holotype, Baia de Sueste, Isla Fernando de Noronha, 540 km NE Recife, Brazil (USNM 749819). B, G, Nodilittorina (Nodilittorina) vermeiji Bandel & Kadolsky, 1982, paratypes, Fernando Noronha, Brazil (BMNH 1889.2.21.63, 1887.2.9.1831). C, E, F, H, Ensenada dos Portugueses, Ilha da Trindade, Brazil (BMNH 1989066). D, Ponta de Santo Antonio, Fernando Noronha, Brazil (BMNH 20081063). I, Ilha da Trindade, Brazil (BMNH 1906.11.1.11). J, K, Ilha do Cemiterio, Atol das Rocas, Brazil (BMNH 1989064). L–N, Buraco da Raquel, Fernando Noronha, Brazil (MZSP 31398).

FIGURE 36. Echinolittorina vermeiji. A–F, penes. G, pallial oviduct. A, B, Porto, Fernando de Noronha, Brazil (MZUSP 31636; shell H A = 6.7 mm, B = 5.7 mm). C, D, Buraco da Raquel, Fernando de Noronha, Brazil (MZSP 31398; shell H C = 12.7 mm, D = 20.1 mm). E–G, Ensenada dos Portugueses, Ilha da Trindade, Brazil (BMNH 1989067; shell H E = 7.6 mm, F = 8.0 mm, G = 8.5 mm). Shading conventions as in Figure 15.