Echinolittorina ziczac ( Gmelin, 1791 )

Reid, David G., 2009, The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean 2184, Zootaxa 2184 (1), pp. 1-103 : 35-42

Echinolittorina ziczac ( Gmelin, 1791)

( Figures 14 , 15 , 16A, B , 17 )

Trochus ziczac Gmelin, 1791: 3587 ( Barbados (type locality designated by Bequaert 1943); lectotype ( Bandel & Kadolsky 1982) Chemnitz 1781: pl. 166, fig. 1599b, Fig. 14A herein, Zuckerinsuln [West Indies]; no material in Chemnitz Collection in St Petersburg, Martynov 2002; in part, Gmelin also referred to Chemnitz, 1781: pl. 166, fig. 1600a, b, which is probably E. interrupta ).

Litorina ziczac —Philippi, 1847: 162–163, Litorina pl. 3, figs 13, 14 (in part, includes Littoraria tessellata ). Küster, 1856: 22–23, pl. 3, figs 9–11. Weinkauff, 1878: 32 (in part, includes E. interrupta ). Weinkauff, 1883: 220 (in part, includes E. angustior , E. interrupta , E. jamaicensis ).

Littorina (Melarhaphe) ziczac —H. Adams & A. Adams, 1854: 314 (as Melaraphe ). Mörch, 1876: 137–138 (as L. (Melaraphe) ziczak ). Nevill, 1885: 139 (as L. (Melaraphe) ziczak ). Tryon, 1887: 251, pl. 45, figs 5, 7 (in part, includes E. angustior , E. interrupta , E. jamaicensis , E. lineolata , Littoraria glabrata ; as Melaraphe ). von Martens, 1900: 583 (in part, includes Littoraria tessellata ).

Littorina ziczac —Reeve, 1857: sp. 57, pl. 11, fig. 57a, b. Bequaert, 1943: 14–18, pl. 5, figs 1–4 (in part, includes E. lineolata , E. jamaicensis , E. interrupta , E. angustior , E. placida ). Lebour, 1945: 465, fig. 5 (egg capsule and larva) (as zigzac). Abbott, 1954a: 132, pl. 19e (in part, includes E. jamaicensis , E. placida , E. angustior ). Coomans, 1958: 62, pl. 8 (in part, includes E. angustior ). Abbott, 1964: 65–66. Abbott, 1968: 82–83, fig. T.V. Borkowski & M.R. Borkowski, 1969: 408–409, fig. 1 (map), 4C (egg capsule), pl. 66, figs 5, 6. Kaufman & Götting, 1970: 348–349, fig. 34. Borkowski, 1971: fig. 2 (egg capsule). Flores, 1973a: 13–14, pl. 2, figs 1–5. Bandel, 1974a: 97–98, 102–103, 107, figs 8 (shell), 15 and 17 (egg capsule), 18–22 and 45 (radula). Bandel, 1974b: 13, fig. 6C (faecal pellets). Bandel, 1975: 15, pl. 1, figs 1–3 (larval shell). Borkowski, 1975: 369–377, fig. 1C (radula). Bandel, 1984: 11–12, fig. 10 (radula). Janson, 1985: 871–879. Sterrer, 1986: 407, pl. 135. De Jong & Coomans, 1988: 18, pl. 32, fig. 75. Díaz & Puyana, 1994: 125, pl. 34, fig. 403.

Litorina (Melarhaphe) ziczac — Dall, 1889: 146 (as Melaraphe ). Dall & Simpson, 1901: 429 (in part, includes E. angustior ; as Melaraphe ).

Littorina (Melarhaphe) ziczac ziczac — Johnson, 1934: 102 (as Melaraphe ).

Littorina (Melarapha) ziczac — Rehder, 1962: 122 (in part, includes E. angustior , E. lineolata , E. placida ).

Littorina (Littorina) ziczac — Rosewater, 1970: 423. Abbott, 1974: 68, fig. 556, pl. 3, fig. 556. H.E. Vokes & E.H. Vokes, 1983: 14, pl. 4, fig. 1.

Nodilittorina (Nodilittorina) ziczac — Bandel & Kadolsky, 1982: 19–21, figs 5 (shell, egg capsule, operculum, radula), 6 (map), 14 (embryonic shell), 15 (larval shell), 18–19 (shells and radulae), 45.

Nodilittorina ziczac — Britton & Morton, 1989: 86, fig. 4-5G. Redfern, 2001: 29, pl. 14, fig. 118. Reid, 2002a: 259–281, fig. 2C (penis).

Nodilittorina (Echinolittorina) ziczac — Reid, 1989: 99, fig. 2h.

Echinolittorina ziczac — Williams, Reid & Littlewood, 2003: 60–86.

Echinolittorina ziczac A— Williams & Reid, 2004: 2227–2251, fig. 6B (map).

Littorina zigzag d’Orbigny, 1841: 210–211 , pl. 15, figs 5–7, 8 (operculum) (unjustified emendation of Trochus ziczac Gmelin, 1791 ).

Littorina (Melaraphis) zigzag —Arango, 1880: 160 (as zigxag).

Littorina debilis Philippi, 1846a: 140 (no locality; lectotype ( Bandel & Kadolsky 1982) BMNH 1968222/1 and 3 paralectotypes BMNH 1968222/2–4, seen). Reeve, 1857: sp. 70, pl. 14, fig. 70.

Litorina debilis —Küster, 1856: 22, pl. 3, figs 6–8. Weinkauff, 1878: 32. Weinkauff, 1883: 220.

Litorina dorbignyana Philippi, 1847: 162 , Litorina pl. 3, fig. 12 ( Martinique; lectotype (Bandel & Kadolsky 1882) and 3 paralectotypes BMNH 1854.10 .4.130, seen).

Litorina mauritiana var. gracilior Philippi, 1847: 165 , Litorina pl. 3, figs 15, 17a (no locality; lectotype ( Reid & Williams 2004) BMNH 20020038, seen; 2 paralectotypes BMNH 20020039 are probably Austrolittorina fernandezensis ( Rosewater, 1970)) .

Litorina mauritiana var. crassior Philippi, 1847: 165 , Litorina pl. 3, fig. 17b ( Cuba (fig. 15); in part, lectotype ( Reid & Williams 2004) fig. 17a is Austrolittorina unifasciata ( Gray, 1826)) .

Littorina mauritiana — Reeve, 1858: sp. 100, pl. 17, fig. 100 (in part, includes Austrolittorina unifasciata ; not Phasianella mauritiana Lamarck, 1822 = Littoraria mauritiana ).

Litorina mauritiana —Weinkauff, 1882: 97–98, pl. 14, fig. 4 (in part, includes Austrolittorina unifasciata ; not Lamarck, 1822).

Litorina cubana Weinkauff, 1882: 68–69 , pl. 9, figs 2, 3 ( Cuba; types presumed lost). Weinkauff, 1883: 220.

Litorina (Melarhaphe) ziczac var. lineata — Dall & Simpson, 1901: 430 (not Lamarck, 1822 = Littoraria tessellata ; as Melaraphe ).

Taxonomic history: The epithet ziczac has been used in many different ways, and has at various times been applied to all the larger, smooth, black-and-white Echinolittorina species of the western Atlantic. The identity of Gmelin’s (1791) species is not in doubt, because he referred to the adequate figure of Chemnitz (1781; Fig. 14A herein), which was subsequently designated lectotype ( Bequaert 1943). However, Gmelin himself had a broader concept, mentioning (as [variety] β) the indeterminate figure of Lister (1688), and another figure by Chemnitz (1781) that probably represents E. interrupta . The broadest concept of L. ziczac was that of Tryon (1887), who included at least five western Atlantic species under the name, establishing an American tradition that was followed by Bequaert (1943), Abbott (1954a) and Rehder (1962). The modern concept of this species dates from Abbott (1964), T.V. Borkowski & M.R. Borkowski (1969) and Bandel & Kadolsky (1982).

In early works there was also confusion with members of other genera. Philippi (1847) included figures and specimens of Littoraria tessellata under Litorina ziczac . There was also persistent confusion with the Australian Austrolittorina unifasciata (under the incorrect name L. mauritiana ), which has shells superficially similar to white, unstriped forms of E. ziczac (Philippi 1847; Reeve 1858; Weinkauff 1882). Shells and figures of these two species can easily be separated by the single pale apertural band of the former, and two pale bands of the latter (e.g. Philippi 1847: Litorina pl. 3, fig. 17; Reid & Williams 2004).

Variability of the shell resulted in recognition of several taxa within this species. A pale, weakly striped form was named L. debilis Philippi, 1846a , a form with stronger striae and narrow axial stripes was described as Litorina dorbignyana Philippi, 1847 , and a white shell as Litorina cubana Weinkauff, 1882 .

Diagnosis: Shell large; 8–10 primary spiral grooves; up to 60 incised lines on last whorl, sometimes obsolete; white, usually with narrow oblique or zigzag brown lines. Penis with very large mamilliform penial gland entirely filling the base. Pallial oviduct with projection of renal oviduct in centre of spiral of albumen gland. Caribbean Sea, E Florida, Bahamas, Bermuda. COI: GenBank AJ623066 , AJ623067 .

Material examined: 198 lots (including 15 penes, 9 sperm samples, 15 pallial oviducts, 4 radulae).

Shell ( Fig. 14 ): Mature shell height 8.9–28.7 mm. Shape high turbinate (H/B = 1.45–1.68, SH = 1.69–1.94); spire whorls moderately rounded; suture distinct, sometimes becoming channelled and even detached at end of last whorl in largest shells ( Fig. 14G ); spire profile slightly convex; periphery of last whorl rounded or slightly angled. Columella short, slightly hollowed and pinched at base; eroded parietal area absent. Sculpture of 8–10 primary spiral grooves on spire whorls; these remain as narrow incised lines, increasing (by division of interspaces) to 40–60 on last whorl; periphery lacks lines; sculpture occasionally becomes obsolete on last whorl; spiral microstriae absent. Protoconch 0.30–0.31 mm diameter, 2.5–2.6 whorls. Ground colour white, occasionally a broad grey band above periphery, blue grey at apex; pattern of numerous narrow oblique brown to pale grey lines, often zigzag, sometimes obsolete; rarely populations are polymorphic, including shells with white, or pinkish orange, or blackish brown ground colour, if brown ( Fig. 14C ) then paler at suture, periphery and on base, and all colour forms with more or less distinct brown lines; aperture dark brown with pale band at base and at shoulder; columella purple brown.

Animal: Head ( Fig. 15H ) grey to black, usually a thin unpigmented stripe across snout; tentacle pale at base and around eye, with two longitudinal black lines and a black ring at tip, but rarely unpigmented; sides of foot pale grey to black. Opercular ratio 0.36–0.40. Penis ( Fig. 15A–E ): filament leaf-shaped, tapering to tip, about 0.5 total length of penis, separated from wrinkled base by a constriction, medial lip of sperm groove enlarged, groove ends terminally; mamilliform gland very large, entirely filling lateral projection and extending into most of base; penial glandular disc relatively small; penis unpigmented. Euspermatozoa 70–96 µm; paraspermatozoa ( Fig. 15K–M ) almost filled by single large rod-piece (or fused bundle of rods) with rounded ends, 20–51 µm, usually long and projecting from cell, which is packed with large round granules. Pallial oviduct ( Fig. 15F, G ): large copulatory bursa separates at posterior end of straight section and extends back usually to albumen gland; renal oviduct enlarged, first loop posterior to seminal receptacle, another loop projecting into centre of spiral loop of albumen gland before joining with albumen gland and duct from seminal receptacle at presumed point of fertilization; seminal receptacle small, elongate, in a more anterior position than in most congeners; sperm stored both in receptacle and in anterior loop of renal oviduct. Spawn ( Fig. 15I, J ): an asymmetrically biconvex pelagic capsule180– 200 µm diameter, with broad peripheral rim overhanging base, dome-shaped upper side sculptured by 3–5 concentric rings or a spiral ridge, containing single ovum 50 µm diameter ( Lebour 1945: Bermuda; T.V. Borkowski & M.R. Borkowski 1969: Florida; Borkowski 1971: Florida; Bandel 1974a: Colombia).

Radula ( Fig. 16A, B ): Relative radula length 3.25–5.47. Rachidian: length/width 1.17–1.41; tip of major cusp rounded. Lateral and inner marginal: 4 cusps, tip of major cusp rounded or bluntly rounded. Outer marginal: 6–8 cusps.

Range ( Fig. 17 ): Caribbean Sea, Bahamas, eastern Florida , Bermuda. Range limits: Port of Spain, Trinidad ( BMNH) ; Permé, NW Cape Tiburon , Panama ( USNM 664215 ) ; NW Isla Uvita , Limón, Costa Rica ( INBio 3314403 ) ; George Cay, Port Royal , Roatan I., Honduras ( BMNH) ; Isla Mujeres , Quintana Roo, Mexico ( USNM 662318 ) ; Punta del Morro , Veracruz, Mexico ( Britton & Morton 1989); Lobos Reef, 100 km SSE Tampico, Mexico ( USNM 710352 ) ; Key West , Florida ( USNM 435308 ) ; Cape Canaveral Inlet , Florida ( USNM 820427 ) ; San Salvador I., Bahamas ( USNM 749797 ) ; Barbados ( BMNH) ; Devonshire, Bermuda ( BMNH 20080982 ) .

This species is abundant on the islands of the Greater Antilles and throughout the Lesser Antilles as far south as Trinidad. On the mainland shore of the Caribbean Sea it occurs commonly from Venezuela to Costa Rica. It has not been recorded from the sedimentary and eutrophic shores of Nicaragua and Honduras, and in Belize occurs only on offshore islands and cays. It is common on the oceanic eastern side of the Yucatan Peninsula, but absent from the eutrophic seas on the north and west sides, where the water has a high limemud content (H.E. Vokes & E.H. Vokes 1983). It is absent from most of the Gulf of Mexico, but can be found in more exposed and offshore sites in the south. Wiley et al. (1982) recorded it (together with ‘ L. lineolata ’, i.e. E. placida ) from the sparse rocky outcrops in central Veracruz state, and this was confirmed by Britton & Morton (1989: 76). It is also present on the offshore reef bank of Isla Lobos ( Britton & Morton 1989: 287; 3 specs in USNM). Borkowski (1975) reported two dead shells from Galveston, Texas. In Florida it is found only on the oceanic eastern side, as far north as Cape Canaveral. A. Stephenson & T.A. Stephenson (1952) reported a few specimens of ‘ L. ziczac ’ about 100 km further north at Marineland in 1947, but their identification cannot be confirmed. According to T.V. Borkowski & M.R. Borkowski (1969) it is rare north of Jupiter Inlet in Florida. Although now frequent in Bermuda, in the nineteenth century it was reported to be uncommon ( Abbott & Jensen 1967).

Bequaert (1943) appears to have been the first to mention that L. ziczac was “established on the Pacific coast near Panama City, which it reached by means of the Canal,” and this has since been widely quoted (e.g. Coomans 1958; Abbott 1974; Rios 1994). Bequaert’s species concept included at least five black-and-white- striped western Atlantic Echinolittorina species , but there is no evidence that any of them are established in the Eastern Pacific province. Presumably the record is based on confusion with similar Pacific species (see Reid 2002b).

Habitat: Bare rocks of the littoral fringe and uppermost eulittoral, usually on coral rock and limestone, but also recorded from granite and concrete substrates; on sheltered and moderately exposed coasts, in situations with clear oceanic water.

Although there is overlap between the species, especially if the tidal range is small, E. ziczac and E. jamaicensis occupy the lowest levels of all the larger Echinolittorina species , from the mid littoral fringe to the upper eulittoral. For example E. ziczac occurs below E. angustior and E. jamaicensis in Florida (T.V. Borkowski & M.R. Borkowski 1969); below E. tuberculata in Venezuela ( Flores 1973b); below E. tuberculata , E. angustior and E. jamaicensis in Jamaica ( Vermeij 1973a); below E. tuberculata and E. interrupta at Santa Marta, Colombia ( Bandel 1974a; Brattström 1980; Bandel & Wedler 1987) and below E. angustior in Panama ( Brattström 1980). There is variation, for on coral limestone in the Bahamas E. ziczac occupies a level between and overlapping with E. tuberculata above and E. jamaicensis below ( Brattström 1999). Only E. meleagris and E. mespillum occur lower on the shore. In terms of biotic zones, E. ziczac is most frequent in the yellow zone of the upper eulittoral and the black zone of the lower littoral fringe ( Brattström 1992, 1999). In Colombia it is preyed upon by Plicopurpura patula (Linnaeus) , whose occurrence coincides with the lower limit of E. ziczac , and juveniles are found lower on the shore than adults ( Bandel 1974a). It is most frequent in pits, crevices and shaded sites ( Bandel 1974a; Minton & Gochfeld 2001). Yipp & Carefoot (1988) reported that E. ziczac is a less selective grazer than E. tuberculata on beachrock in Barbados and that the zonation of the former expanded upwards after removal of E. tuberculata , suggesting possible competitive effects. Dobson-Moore & Britton (2001) measured bioerosion on a limestone platform in Jamaica.

The species is only moderately euryhaline, tolerating 26–36ppt salinity ( Flores 1973b). Heat coma temperatures are amongst the highest for Caribbean littorinids, in the range 46.9–47°C ( Britton 1992; McMahon 2001; for alternative measures of temperature tolerance see Fraenkel 1968, and Mahieu et al. 1987), which exceeds recorded rock surface temperatures ( Minton & Gochfeld 2001). Individuals survive emersion for between one and seven months ( Mattox 1949; Yipp & Carefoot 1988; Britton 1992).

In Florida the reproductive season is between April and December ( Borkowski 1971), while in Bermuda spawn was found in July and August ( Lebour 1945). Borkowski (1971) found that spawning occurred in the field whenever the tide rose above MHWS, not on a lunar rhythm, and that it could be induced by splash in the laboratory. Growth rate was reported by Borkowski (1974).

Remarks: The distribution and habitat of E. ziczac show it to be an oceanic species, restricted to water of low productivity and nutrient status. This is clearly shown by its restriction to the eastern coast of Florida, its absence from the Gulf of Mexico (except for exposed outcrops and an offshore islet in the southwest), and restriction to the oceanic shores of the eastern Yucatan Peninsula.

Molecular phylogenetic analysis indicates that the sister species of E. ziczac is an undescribed species from the islands in the Gulf of Guinea, West Africa (‘ E. ziczac B’ of Williams & Reid 2004). The average K2P genetic distance for COI between the two is only 2.61%, and 28S data do not support reciprocal monophyly ( Williams & Reid 2004). Nevertheless, there are consistent morphological differences in the dark brown shell colour and smaller penial gland of the eastern Atlantic species. Sister to these is a clade composed of the two eastern Pacific species E. modesta ( Philippi, 1846a) and E. conspersa (Philippi, 1847) . The shells of these two species are similar to that of E. ziczac only in that they are predominantly white; the penes are entirely different, because those of the eastern Pacific species lack a mamilliform gland and are unbranched. However, the oviducts of all four species are identical (and distinct from all congeners) in their enlarged renal oviduct that projects into the loop of the albumen gland and the more forward position of the seminal receptacle (description of eastern Pacific species by Reid 2002b; condition of E. ziczac and sister species not correctly observed by Reid 2002a); these features are therefore synapomorphic for the group. The pair of additional dentacles on the concave anterior edge of the rachidian tooth (inside the pair flanking the main cusp) of E. modesta and E. conspersa ( Reid 2002b) is only weakly and variably present in E. ziczac ( Fig. 16B ).

Colour polymorphism is rare in populations of E. ziczac , black or orange shells having been seen in 5 of 198 samples examined.

The shell of this species is easily distinguished from that of others by its large size, pale colour, rounded periphery and sculpture of numerous fine lines.

Figures

FIGURE 14. Echinolittorina ziczac. A, Trochus ziczac Gmelin, 1791, lectotype figure (b), figure 1599 from Chemnitz (1781), West Indies. B, H, Nenton Point, Nelson’s Dockyard, Antigua (BMNH 20080980). C, Eight-mile Rock, Grand Bahama I., Bahamas (BMNH 20080981). D, G, Rocky Bay, Devonshire, Bermuda (BMNH 20080982). E, F, I, Little Stirrup Cay, Berry Is, Bahamas (BMNH 20080983).

FIGURE 15. Echinolittorina ziczac. A–E, penes. F, G, two views of pallial oviduct, lateral and ventral (with transverse section). H, head. I, J, egg capsules (I after Bandel 1974; J after Borkowski 1971). K–M, paraspermatozoa. A, Playa Huertas, Portabelo, Panama (BMNH 20080984; shell H = 10.0 mm). B, H, K, M, Fort Pierce Inlet, St Lucie Co., Florida, USA (BMNH 20080985; shell H = 10.6 mm). C, D, L, South Water Cay, Belize (BMNH 20080986; shell H C = 12.4 mm, D = 10.4 mm). E–G, Jingle Beach, Priory, Jamaica (BMNH 20080987; shell H E = 12.3 mm, F, G = 19.2 mm). I, Santa Marta, Colombia. J, south Florida, USA. Abbreviations: ag, albumen gland (sparse stipple); b, copulatory bursa (dashed outline; visible by transparency); eg, egg groove (visible by transparency); mpg, mamilliform penial gland, opening through external papilla; mr, mucus reservoir of mamilliform penial gland (visible by transparency); ocg, opaque capsule gland (mid stipple); pf, smooth penial filament; pgd, penial glandular disc; psg, penial sperm groove on antero-dorsal edge of penis; ro, renal oviduct; seg, subepithelial glandular tissue of mamilliform penial gland (visible by transparency); sg, sperm groove of pallial oviduct; sr, seminal receptacle (heavy stipple); tcg, translucent capsule gland (cross-hatched); wb, wrinkled base of penis.

FIGURE 16. Radulae of Echinolittorina species (two views of each radula, flat and at 45°). A, B, E. ziczac; Jingle Beach, Priory, Jamaica (BMNH 20080987; shell H = 12.3 mm). C, D, E. interrupta; Lucea Bay, Jamaica (BMNH 20081008; shell H = 11.5 mm). E, F, E. placida; Marco I., Collier Co., Florida, USA (paratype, BMNH 20081010/2; shell H = 10.9 mm). Scale bars = 50 µm.

FIGURE 17. Distribution of Echinolittorina ziczac from material examined (solid circles) and literature records (open circles; A, Flores 1973a; B, Kaufmann & Götting 1970; C, Britton & Morton 1989).