Echinolittorina lineolata (d’Orbigny, 1840)

Reid, David G., 2009, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean 2184, Zootaxa 2184 (1), pp. 1-103 : 28-33

Echinolittorina lineolata (d’Orbigny, 1840)

( Figures 10–13 )

Littorina lineolata d’Orbigny, 1840: 392 (port of Rio de Janeiro [ Brazil]; lectotype ( Bandel & Kadolsky 1982) BMNH 1854.12.4.363/1, Fig. 10A herein, and 12 paralectotypes BMNH 1854.12.4.363/2, seen). Borkowski, 1975: 369–377 (in part, includes E. jamaicensis ). Absalão & Roberg, 1999: 381–395, fig. 1 (penis).

Littorina (Melarhape) lineolata — Mörch, 1876: 138 (as Melaraphe ). Morretes, 1949: 70 (as Melaraphe ).

Littorina (Austrolittorina) lineolata — Rios, 1975: 33, pl. 9, fig. 107. Rios, 1985: 34, pl. 14, fig. 144 (in part, includes E. angustior , E. jamaicensis ). Rios, 1994: 48, pl. 15, fig. 165 (in part, includes E. angustior , E. jamaicensis ).

Nodilittorina (Nodilittorina) lineolata — Bandel & Kadolsky, 1982: 21–23, figs 1A (penis), 3A (operculum), 5 (shell, egg capsule, operculum, radula), 7 (map), 20–22 (shells and radulae). Reid, 1989: 99.

Nodilittorina lineolata — Britton & Morton, 1989: 86, fig. 4-5A (in part, includes E. placida ). Reid, 2002a: 259–281.

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

Littorina lineata —d’Orbigny, 1841: 208–209 (in part, includes E. angustior , E. jamaicensis ; not Lamarck, 1822 = Littoraria tessellata (Philippi, 1847)) . Absalão & Roberg, 1999: 381–395 (not Lamarck, 1822).

Littorina (Melarhaphe) ziczac lineata — Morretes, 1949: 70 (not Lamarck, 1822; as Melaraphe ).

Littorina lineata — Borkowski, 1975: 369–377 (in part, includes E. angustior , E. interrupta ; not Lamarck, 1822).

Littorina (Austrolittorina) lineata — Rios, 1994: 48, pl. 15, fig. 164 (in part, includes E. angustior ; not Lamarck, 1822).

Litorina pusilla Philippi, 1847: 164 , Litorina pl. 3, fig. 23 ( Brazil and Sandwich Is [Hawaiian Is], corrected to Brazil by Bandel & Kadolsky, 1982; types not traced; not Littorina pusilla M’Coy, 1844 ). Küster, 1856: 11, pl. 1, figs 20–22 (pl. 1 1853). Weinkauff, 1883: 220.

Littorina (Melarhaphe) pusilla — Mörch, 1876: 140 (as Melaraphe ). Tryon, 1887: 251, pl. 45, fig. 8 (as Melaraphe ).

Littorina (Melarhaphe) sp. n. Mörch, 1876: 140–141 (as Melaraphe ).

Littorina (Melarhaphe) ziczac — Tryon, 1887: 251 (in part, includes E. angustior , E. interrupta , E. jamaicensis , E. ziczac , Littoraria glabrata ( Philippi, 1846a) ; not Gmelin, 1791; as Melaraphe ). Matthews, 1968: 184 (not Gmelin, 1791). Rios, 1970: 33 (not Gmelin, 1791).

Littorina ziczac — Bequaert, 1943: 14–18 (in part, includes E. ziczac , E. jamaicensis , E. interrupta , E. angustior , E. placida ; not Gmelin, 1791). E. Marcus & E. du B. Marcus, 1963: 7–33, figs 1, 3 (radula), 9 (osphradium), 15–16 (head, penis), 24–25 (oviduct), 28–29 (egg capsule), 30 (juvenile) (not Gmelin, 1791). Matthews & Rios, 1967: 68 (not Gmelin, 1791). Calvo, 1987: 81–83, fig. 39 (radula) (not Gmelin, 1791). Absalão & Roberg, 1999: 381–395 (not Gmelin, 1791). Absalão & Louro, 2002: 115–125 (penis; not seen; not Gmelin, 1791).

Littorina (Melarapha) ziczac — Rehder, 1962: 122 (in part, includes E. angustior , E. placida , E. ziczac ; not Gmelin, 1791).

Littorina (Littorina) ziczac — Rios, 1975: 32, pl. 9, fig. 105 (not Gmelin, 1791). Rios, 1985: 33–34, pl. 14, fig. 143 (in part, includes E. ziczac , E. angustior ; not Gmelin, 1791).

Littorina (Austrolittorina) ziczac — Rios, 1994: 48, pl. 15, fig. 165a (in part, includes E. ziczac ; not Gmelin, 1791).

Littorina ziczac brasiliensis Vermeij & Porter, 1971: 448–449 (replacement name for Litorina pusilla Philippi, 1847 ).

Taxonomic history: d’Orbigny’s (1840) introduction of the name Littorina lineolata was apparently an error for Littorina lineata . In the synonymy he listed ‘ Littorina lineolata, d’Orb., Moll. des Antilles , no. 120’, but that article was not published until 1841 (included in his account of the molluscs of Cuba; see Bandel & Kadolsky 1982) and the name then appeared as Littorina lineata , while in the synonymy of that species the earlier (d’Orbigny 1840) use of lineolata is given as lineata . To compound the confusion, in 1840 he noted that he considered ‘cette espèce’ (i.e. the Brazilian L. lineolata ) to be a variety of L. lineata from the Antilles, but not a distinct species. Both species descriptions (d’Orbigny 1840, 1841) included the vernacular name ‘littorine lineolée’, and in 1841 Littorina lineata was mentioned as having been collected in Brazil. Nevertheless, the introduction of the name is valid in its original spelling.

Since the sweeping synonymy of Tryon (1887), E. lineolata has frequently been referred to as L. ziczac , and there has been persistent confusion with other members of the ‘ ziczac species complex’ (see Remarks on subgenus Amerolittorina ). The name lineolata was only rarely used in its correct sense ( Mörch 1876; Morretes 1949) until its nomenclature was clarified in the revision of the western Atlantic ‘ Nodilittorina ’ species by Bandel & Kadolsky (1982). More frequently this name was incorrectly applied to E. jamaicensis ( Abbott 1964; T.V. Borkowski & M.R. Borkowski 1969) and to E. placida ( Britton & Morton 1989) .

Several authors have claimed that there are more than one Echinolittorina species on the Brazilian mainland. Mörch (1876) gave three, Morretes (1949) two and Borkowski (1975) two, owing to the considerable variation in shell size and coloration. Based on an unpublished thesis by L.E. Lima (1983; not seen), Rios (1985) listed two species and Rios (1994) gave three under the names L. lineolata , L. lineata and L. ziczac (following the nomenclature used by T.V. Borkowski & M.R. Borkowski 1969, for species in Florida). Absalão & Roberg (1999) used these same three names and claimed to have identified differences in penial shape between them (see also Absalão & Louro 2002; not seen), although neither diagnostic allozyme loci nor ecological differentiation were found; the penial differences are likely to have been artefacts of preservation or maturation. An allozyme study of this species from localities along the Brazilian coast found no linkage disequilibrium, supporting the existence of a single species (Andrade, Magahães & Solferini 2003). Heterozygote deficiencies were detected, but these were interpreted as evidence of selection on some loci, and not due to pooling of genetically distinct specimens ( Andrade, Medeiros & Solferini 2005).

The identity of Litorina pusilla gave rise to confusion, because in the original description Philippi (1847) gave as localities both Brazil and Sandwich Islands (Hawaiian Islands). Both Weinkauff (1883) and Tryon (1887) gave only the latter locality (where only the superficially similar E. hawaiiensis (Rosewater & Kadolsky, 1981) occurs; see Reid 2007). Bandel & Kadolsky (1982) restricted the type locality to Brazil, but types could not be found. The preoccupied name was replaced by Vermeij & Porter (1971).

Diagnosis: Shell moderate to small; 9–10 primary spiral grooves; 10–25 narrow grooves above periphery of last whorl, sometimes obsolete; white with narrow oblique or zigzag brown lines. Penis with swollen pointed filament. Copulatory bursa opens at anterior end of straight section of pallial oviduct. Brazil, Uruguay. COI: GenBank AJ622957 , AJ622958 .

Material examined: 48 lots (including 15 penes, 7 sperm samples, 9 pallial oviducts, 4 radulae).

Shell ( Fig. 10 ): Mature shell height 4.0– 17.5 mm. Shape turbinate to high turbinate (H/B = 1.33–1.68, SH = 1.54–2.00); spire whorls moderately rounded, suture distinct; spire often eroded; periphery of last whorl slightly or distinctly angled. Columella short, slightly hollowed and pinched at base; eroded parietal area absent. Sculpture of 9–10 primary spiral grooves on spire whorls; these may remain as incised lines, numbering 10–11 above peripheral rib of last whorl, or may be increased (by interpolation of secondary ribs, Fig. 10L ) to 12–25; in strongly sculptured shells grooves may be up to one third of rib width ( Fig. 10B, C ); peripheral rib usually slightly enlarged and raised; 7–10 faint grooves may be present on base; small adults may be entirely smooth on last whorl ( Fig. 10D, F, G ); spiral microstriae usually absent, rarely visible in widest grooves. Protoconch not seen. Ground colour white, sometimes a spiral black band on spire whorls, paling to wide grey spiral band above periphery on last whorl; pattern of narrow oblique brown lines, often wavy, zigzag or (in small, smooth shells, Fig. 10G ) forming a black herringbone effect with the spiral band above periphery; aperture dark brown with pale band at base and a less distinct pale band at shoulder; columella purple brown.

Animal: Head black, usually a thin unpigmented stripe across snout; tentacle pale at base and around eye, with two longitudinal black lines to half to two-thirds length, black dot at tip; sides of foot pale grey to black. Opercular ratio 0.45–0.54. Penis ( Fig. 11A–E ): filament stout, swollen, pointed, about 0.5–0.6 total length of penis but not sharply differentiated from wrinkled base, sperm groove ends terminally; mamilliform gland about half size of glandular disc, borne together on short projection of base (usually 1, occasionally 0 or 2 mamilliform glands, E. Marcus & E. du B. Marcus 1963; one abnormal specimen with 5 glands seen); penis unpigmented or slightly pigmented at base. Euspermatozoa 64–86 µm; paraspermatozoa ( Fig. 11I–K ) oval, 13–21 µm, containing one large rectangular rod-piece, occasionally slightly projecting, and often 2–4 small rectangular rod-pieces together with one curved or coiled rod-piece, also a few large round granules. Pallial oviduct ( Fig. 11G ): large copulatory bursa opens near anterior end of straight section and extends back to albumen gland. Spawn ( Fig. 11H ): a pelagic capsule 210 µm diameter by 120 µm high, with broad peripheral rim overhanging base, dome-shaped upper side sculptured by 4 concentric rings, containing single ovum 60 µm diameter (E. Marcus & E. du B. Marcus 1963).

Radula ( Fig. 12 ): Relative radula length 2.22–5.0 (see also Meirelles & Matthews-Cascon 2003, who found similar values and no relation between radular length and shell height; as L. ziczac ). Rachidian: length/ width 1.50–3.67, sometimes narrow ( Fig. 12C ); tip of major cusp pointed. Lateral and inner marginal: 4 cusps, tip of major cusp rounded; major cusp may be enlarged, becoming more pointed, innermost and outermost cusp of each tooth then absent ( Fig. 12C, D ). Outer marginal: normal form with 7–8 cusps, or narrowed to a rod with 5 cusps ( Fig. 12C ).

Range ( Fig. 13 ): Brazil and Uruguay. Range limits: Tibau , Ceará , Brazil ( BMNH); Natal, Rio Grande do Norte , Brazil ( BMNH); Torres, Rio Grande do Sul , Brazil ( BMNH); Barra, Rio Grande , Rio Grande do Sul , Brazil ( BMNH 1958.4.10.2); Cabo Sta Maria , Uruguay ( USNM 381695 ); Maldonado , Uruguay ( MNHN) .

The estuaries of the Amazon and la Plata circumscribe the limits of this species. The coastline of Rio Grande do Sul and much of Uruguay is a stretch of about 700 km of exposed sandy beaches without suitable habitat for littorinids, except that provided by artificial substrates (such as the breakwater at Barra).

Habitat: Bare rocks of the littoral fringe and among barnacles and mytilids in upper and mid-eulittoral, on exposed and moderately exposed coasts.

Ecological studies in southeastern Brazil have shown that E. lineolata extends from the mid littoral fringe down to the lower mid eulittoral, with highest densities (up to 500 per 100 cm 2) in the barnacle zone and on exposed shores ( Magalhães 1998; Apolinário, Coutinho & Baeta-Neves 1999). Size usually increases upshore ( Vermeij 1972b), probably because of recruitment in the barnacle zone; in addition mortality of larger individuals increases at lower levels where refuges are scarce ( Magalhães 1998). Juveniles (up to 4 mm) have also been found in sandy algal turf on the sheltered side of a beachrock reef ( Vermeij & Porter 1971). The relative zonation of littorines and barnacles differs on exposed and sheltered shores; in exposure the snails occur together with Chthamalus and just above, whereas in shelter most occur above Chthamalus and Crassostrea and together with Littoraria flava ; zonation is 0.5 m lower in winter (July) when low tides are diurnal ( Oliveira Filho & Mayal 1976). Transfer experiments have revealed active selection of the mid eulittoral zone and caging has shown that grazing reduces microalgal abundance, so food availability may play a role in habitat selection ( Apolinário, Coutinho & Baeta-Neves 1999).

Remarks: Specimens from Uruguay are distinctive, with lower-spired shells that are frequently smooth even when of large size ( Fig. 10J ) or bear weak primary grooves only. Shells from Brazil may be smooth when small, but larger specimens usually bear strong grooves increased by secondary sculpture. The sandy coast of southern Brazil and Uruguay probably limits gene flow between Brazilian and Uruguayan populations. No anatomical or genetic data are available from Uruguayan populations to test their conspecificity.

Dwarf shells of this species from crevices among barnacles are often smooth with a black ‘herringbone’ pattern ( Fig. 10G ). Similar variation has been noted in some members of the E. aspera group in the eastern Pacific, in which small, smooth, dark shells are found in shallow pools at the top of the eulittoral zone and likely represent an ecophenotypic form ( Reid 2002b).

The coiled and twisted inclusions in the paraspermatozoa have been found in six of the seven living sperm samples examined, collected from two localities (Natal and Cabo Frio, Brazil) and in different seasons, so are apparently a natural feature ( Fig. 11I–K ; see Remarks on Lineolittorina above).

There is striking variation in the radula, similar to that found in other Echinolittorina species (see Discussion).

Figures

FIGURE 10. Echinolittorina lineolata. A, Littorina lineolata d’Orbigny, 1840, lectotype, Rio de Janeiro, Brazil (BMNH 1854.12.4.363/1). B, Bara Cunha, 60 km S Natal, Rio Grande do Norte, Brazil (BMNH 20080975). C, E, Curumirin, Rio de Janeiro state, Brazil (MZSP 31267). D, Araruama Point, Cabo Frio, Rio de Janeiro state, Brazil (BMNH 20080976). F, Pernambuco, Brazil (BMNH 1844.8.7.1). G, Pernambuco, Brazil (BMNH 1924.12.3.10). H, Natal, Brazil (BMNH 20080977). I, I. Queimada Grande, São Paulo state, Brazil (MZSP 24919). J, Cabo Polonia, Uruguay (USNM 359202). K, Barra, Rio Grande, Brazil (BMNH 1958.4.10.2). L, I. Sta Barbara, Abrolhos Arch., Brazil (USNM 770002).

FIGURE 11. Echinolittorina lineolata. A–E, penes; E abnormal, with two mamilliform penial glands. F, head and penis. G, pallial oviduct. H, egg capsule (after E. Marcus & E. du B. Marcus 1963). I–K, paraspermatozoa. A, B, Santa Catarina, Brazil (USNM 264059; shell H A = 6.5 mm, B = 6.4 mm). C, Cigarras Beach, São Sebastião, São Paulo state, Brazil (BMNH 20080979; shell H = 7.2 mm). D, I, Araruama Point, Cabo Frio, Rio de Janeiro state, Brazil (BMNH 20080976; shell H = 6.7 mm). E, J, K, Natal, Brazil (BMNH 20080978; shell H E = 7.2 mm). F, Natal, Brazil (BMNH 20080977; shell H = 4.0 mm). G,Ilha de Queimada Grande, São Paulo state, Brazil (MZSP 24919; shell H = 12.9 mm). H, São Paulo state, Brazil. Shading conventions as in Figure 15.

FIGURE 12. Radulae of Echinolittorina lineolata (two views of each radula, flat and at 45°). A, B, normal form; Cigarras Beach, São Sebastião, São Paulo state, Brazil (BMNH 20080979; shell H = 7.2 mm). C, D, narrowed form; Bara Cunha, 60 km S Natal, Rio Grande do Norte, Brazil (BMNH 20080975; shell H = 8.0 mm). Scale bars = 50 µm.

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