Cyerce cristallina ( Trinchese, 1881 )

Moreno, Karina, Rico, Diane M., Middlebrooks, Michael, Medrano, Sabrina, Valdés, Ángel A. & Krug, Patrick J., 2024, A cryptic radiation of Caribbean sea slugs revealed by integrative analysis: Cyerce ‘ antillensis’ (Sacoglossa: Caliphyllidae) is six distinct species, Zoological Journal of the Linnean Society 200 (4), pp. 940-979 : 952-955

Cyerce cristallina ( Trinchese, 1881)

( Fig 5–8 )

Lobiancoia cristallina Trinchese 1881: 116 ; Pruvot-Fol 1954: 175–179.

Cyerce jheringi Pelseneer 1892: 19–21 , fig. 1; Swennen 1961: 53–58, figs 8–10.

Lobifera cristallina ( Trinchese 1881) – Portmann 1958: 407– 410, fig. 2; Haefelfinger 1960: 329–333.

Cyerce cristallina ( Trinchese 1881) – Marcus and Marcus, 1970: 29–30, figs 39–43; Thompson 1977: 134–135, fig. 31, p. 121 fig. 22h, pl. 1, fig. b; Schmekel and Portmann 1982: 288, fig. 7.98; Perrone 1983: 145–149, figs 1, 2; Clark 1984: 91–92, figs 30, 31; Thompson 1988: 165–169, fig. 6, p. 163, fig. 4d; Minniti et al. 1989: 293–294, fig. 1; Ortea et al. 2009: 113–115, pl. 2d.

Type material

Cyerce cristallina Trinchese 1881 – Holotype untraceable, not at Centro Musei delle Scienze Naturali e Fisiche, Italy. Type locality: Secca della Gaiola, Italy, Mediterranean Sea, 9 April 1881, 4 mm in length.

Cyerce jheringi Pelseneer 1892 – Holotype untraceable. Type locality: Naples , Italy, 8 March 1879, depth 120 m, 35 mm in length.

Material examined

Lauderdale-by-the-Sea, FL, USA, 5 July 2014, one specimen, 5 mm preserved length, isolate MM98 ( CPIC 01135 ). FL, USA, 9 August 2019, one specimen, 12 mm preserved length, isolate B101 . FL, USA, 11 August 2019, one specimen, 13 mm preserved length, isolate B103 .

Range

FL, USA (present study; Marcus and Marcus, 1970), Curaçao ( Marcus and Marcus, 1970), Jamaica ( Thompson 1977), Bermuda ( Clark 1984), Roatan (present study), Canary Islands ( Ortea et al. 2009), Mediterranean Sea ( Portmann 1958, Haefelfinger 1960, Swennen 1961, Schmekel and Portmann 1982, Perrone 1983, Thompson 1988, Minniti et al. 1989).

Description

External morphology: Body pale green to cream, with burgundy patches. Head white in ground colour, with burgundy line between eyespots that branches anteriorly up each rhinophore and forms an arrow-shaped burgundy patch on front of head ( Fig. 6A–D ). White oval patches surround eyes. Rhinophores translucent white, with solid burgundy bands extending up to tips. Oral tentacles translucent white, with fainter burgundy coloration at tips. Notum, foot colour translucent white, with minute white specks along the margin; foot longer and wider than notum, narrowing to a triangular tail.

Pericardium oval, elevated; cream white, with burgundy patch and scattered bright orange spots ( Fig. 6D ). Several bright orange spots outlining dorsal vessels extending from pericardium. Anal papilla bright orange ( Fig. 6A, D ). Cerata inflated, fan shaped, translucent white; surface with opaque granules visible ( Fig. 6A ) and dotted with scattered white and orange spots ( Fig. 6B–D ). Cerata with one burgundy patch at base and a second patch forming a symmetrical cap over the ceratal margin at the tip ( Fig. 6A, B ). White rim along margin formed by dense specks.

Internal morphology: Buccal mass ~ 5 mm in length. Pharyngeal pouch short, sides curved upwards. Twelve radular teeth for a 5-mm-long specimen, five on ascending limb and seven on descending limb ( Fig. 7A ). Radulae of 12-mm-long specimen (isolate B101) and 13-mm-long specimen (isolate B103) each with four teeth on ascending limb and six teeth on descending limb. Ascus containing at least seven pre-radular teeth. Teeth elongated, nearly straight with only slight curve, no pronounced angle. Leading tooth 380 µm long. Each side of cutting edge bearing a row of 17 pointed, triangular denticles, some chipped ( Fig. 7B ). Denticles smaller near base, larger towards subtle inflection point at midpoint of tooth, smaller at tip.

Penis with cylindrical stylet, slightly curved, <100 µm in length, with pointed tip and oval opening ( Fig. 8G ).

Ecology

Specimens of C. cf. cristallina in Florida and Roatan are typically found under rocks and coral rubble during the day, associated with siphonous green algae, but become active nocturnally and frequently associate with the green alga Penicillus capitatus Lamarck 1813 at night in Roatan ( Fig. 6E ; Ariane Dimitris and Mickey Charteris, unpublished data). Although direct feeding has not been confirmed, Pe. capitatus is therefore a potential host alga for C. cf. cristallina given that other Cyerce spp. in the Caribbean feed on Penicillus spp.

Remarks

Trinchese (1881) described Mediterranean C. cristallina with yellow spots scattered over the pericardium, similar to Ortea et al. (2009). Some of our specimens lacked yellow–orange spots on the cerata, whereas others exhibited bright yellow–orange spots across the cerata, pericardium and body, similar to descriptions of Mediterranean specimens by Thompson (1988) and Caribbean specimens by Marcus and Marcus (1970). A trait consistently described for C. cristallina is the bright orange–yellow colour of the anal papilla, located between the pericardium and right rhinophore, also observed in our specimens ( Trinchese 1881, Thompson 1988, Ortea et al. 2009).

The specimen of C. cristallina described by Marcus and Marcus (1970) conformed to our specimens internally and externally, as did the buccal mass illustrated by Swennen (1961) and Marcus and Marcus (1970). The radulae of our specimens also closely resembled that figured by Swennen (1961), in being elongated with recurved square denticles and a blunt tip. The only difference was that the anterior articulation knobs from the radula of the specimen described by Swennen (1961) had an additional projection differing from the articulation knobs of the radulae of our specimens. The description of C. cristallina also included mention of a ‘defenseless penis’ ( Trinchese 1881), whereas Swennen (1961), Marcus and Marcus (1970) and Perrone (1983) all note a bent stylet at the opening of the penis. The stylets illustrated and described by Swennen (1961) and Marcus and Marcus (1970) matched the stylets from our specimens.

The evolutionary relationships between C. cf. cristallina and other Cyerce spp. were not well resolved in our phylogenetic analyses, but C. cf. cristallina was the only Caribbean species that did not belong to the same lineage as the remaining Caribbean species. We were unable to obtain specimens of C. cristallina from the Mediterranean Sea and thus could not assess whether this species is truly amphi-Atlantic in distribution or whether the Mediterranean and Caribbean populations are potentially distinct.

Figures

Figure 5. Haplotype network of phased histone 3 alleles colour-coded by candidate species, with the size of each circle denoting the frequency of the sampled allele. A small black dot indicates an unsampled allele. Each bar crossing a line denotes one nucleotide substitution.

Figure 6. Live specimens of Cyerce cf.cristallina photographed underwater.A, specimen from Pompano, FL, USA. B, side view of crawling specimen from Lauderdale-by-the-Sea, FL, USA, ~2 cm body length. C, D, orange spot morphotype from Roatan (C) and Pompano, FL, USA (D). E, specimen from Roatan nestled in the green alga Penicillus capitatus at night. Photograph credits:Ariane Dimitris (A, B, D) and Mickey Charteris (C, E).

Figure 7. Cyerce cf.cristallina, radular scanning electron micrographs.Specimen from FL, USA, isolate MM98 (CPIC 01135); 5 mm preserved length. A, complete radula minus ascus. B, leading tooth.

Figure 8. Stained and mounted penial stylets of Cyerce species from the Western Atlantic. Black arrow indicates stylet.A, Cyerce nicholasi, isolate 10Bim03. B, Cyerce piercei, isolate KM66. C, Cyerce ellingsonorum, isolate 06Jam05. D, Cyerce antillensis, isolate 10Bim01.E, Cyerce browneveorum, isolate 09Gei01.F, Cyerce willetteorum, isolate 07Stir01.G, Cyerce cf. cristallina, isolate B101.