Cyerce nicholasi, Moreno & Rico & Middlebrooks & Medrano & Valdés & Krug, 2024

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 : 961-964

Cyerce nicholasi sp.nov.

( Figs 1–5 , 8A , 12 , 13 )

ZooBank registration: lsid:zoobank.org:act: DA9D52FA-9103- 4430-8B46-C66C1F7D1F86

Cyerce antillensis – Clark and Defreese 1987: 259–279; Clark 1994: 906; Krug et al. 2015: 989–991; Goodheart et al. 2016: 23–25.

Type material

Holotype: Little San Salvador , Bahamas, Caribbean Sea, July 2007, 4 mm preserved length, ( LACM 3842 ; isolate 07 LSS02 ).

Additional material examined

Bimini, Caribbean Sea , July 2010, one specimen preserved, isolate 10Bim03 .

Range

Bahamas, Dominica, Panama (present study).

Description

External morphology: Body colour pale yellow–green; notum flecked with minute burgundy or brown specks ( Fig. 12 ). Head white to pale green, flecked with burgundy or brown speckles. Small burgundy patch between eyes, extending as thin line up to the base of each rhinophore, giving appearance of arched eyebrows. Rhinophores and tentacles smooth, translucent, frosted with white patches and brown specks.

Pericardium round, heavily papillose; brown to burgundy ground colour, with white papillae ( Fig. 12B, C ). Anal papilla white, anterior and to the right of pericardium. Dorsal vessels capped in grey when first extending from the pericardial sac; paired posterior vessels running length of notum to base of pointed tail, with short side branches emerging to connect to cerata along body margin ( Fig. 12B, C ). Lateral vessels not clearly visible. Cerata flat, narrow, elongated; translucent, with large white patches scattered across surface.Small burgundy or brown oval-shaped patch at base of ceras; larger, brown oval patch surrounded by fine yellow ring located near tip of ceras ( Fig. 12A–C ). Ceratal margin extending into crenulate white rim of rounded, finger-like protrusions. On some specimens, outer face of cerata covered in tan to brown patches and with long brown streaks ( Fig. 12D ).

Internal morphology: One specimen (4 mm body length) with 15 radular teeth, 8 on the ascending limb and 7 on the descending limb, and ≥ 17 pre-radular teeth in the ascus ( LACM 3842 , isolate 07 LSS02 ); leading tooth was 145 μm long. Second specimen (2 mm body length) with 13 teeth, 4 on the ascending limb and 9 on the descending limb, and a dense jumble of pre-radular teeth in the ascus (isolate 10 BIM03 ); leading tooth with damaged tip, next tooth on ascending limb was 115 μm long ( Fig. 13A–C ). Teeth of moderate depth, slightly angled down towards blunt tip. Cutting edge with row of 10 rectangular denticles distributed evenly along either side of tooth, each 3 μm wide ( Fig. 13B ) .

Penis with long, curved stylet with oval opening ( Fig. 8A ). Stylet measuring 175 μm long and 7 μm wide at opening (isolate 10 BIM 03).

Ecology

Specimens were collected on Pe. dumetosus in Sweetings Cay and Great Stirrup Cay, Bahamas and in Bocas del Toro, Panama. Slugs fed on Pe. dumetosus in the laboratory. Both specimens from Bimini, Bahamas were collected from R. phoenix , an alga closely related to Penicillus , which is also occasionally used as a host by the Penicillus -specialist E. papillosa ( Krug et al. 2016) . The lone specimen from San Salvador, Bahamas was collected from H. goreaui beneath a shaded coral overhang.

Reproduction

Data were obtained for one clutch laid by a specimen collected from Penicillus in Sweetings Cay, Bahamas in 2004. The egg mass lacked extracapsular yolk and had one embryo per capsule. The mean ± SEM larval shell width across the aperture was 308.3 ± 4.3 μm (N = 7) for one clutch, in the size range for lecithotrophic species in Sacoglossa ( Krug et al. 2015). Larvae had the morphological characteristics of lecithotrophy, including an enlarged propodium, eyespots and crawling behaviour upon hatching, although no spontaneous metamorphosis was observed.

Etymology

Named in honour of Nicholas, the pet boa constrictor of P.J.K., who waited patiently for his return from many field trips over 34 years. The bifid rhinophores of Cyerce are reminiscent of Nick’s forked tongue, and boas radiated in the Caribbean, as did this lineage of Cyerce , making a fitting namesake for a lifelong companion.

Remarks

Cyerce nicholasi has probably been widely confused with C. antillensis Engel, 1927 given the many reports of C. antillensis - like specimens feeding on Penicillus . Both species share a wide range spanning the Bahamas, Dominica and Panama; however, no specimens of C. nicholasi have yet been sampled in Florida, where C. antillensis and at least two other complex members occur. Algal host use easily distinguished the two common species: C. nicholasi feeds primarily on Pe. dumetosus and the related alga R. phoenix , whereas C. antillensis specializes on H. opuntia . However, given that multiple species in the C. antillensis complex feed on Penicillus and Rhipocephalus , host use is not a diagnostic character for C. nicholasi .

Limited developmental data also suggest that C. nicholasi can be distinguished from C.antillensis and some other complex members by larval type. Larval shell size for Sweetings Cay specimens of C. nicholasi indicates lecithotrophic development, whereas C. antillensis and C. piercei were both planktotrophic and also overlap with C. nicholasi in the Bahamas. Development mode may thus be a potentially useful character for differentiating the species where they are sympatric; however, given that poecilogony occurs in Caribbean sacoglossans, larval type can be unreliable for identifying a species without intensive population-level sampling ( Krug 2009, Ellingson and Krug 2016). The high degree of population genetic structure in C. nicholasi (lecithotrophic) is consistent with the predicted reduction in dispersal potential conferred by short-lived lecithotrophic larvae, in comparison to the lack of structure in C. antillensis (planktotrophic).

Externally, the shape and appearance of cerata and the body colour distinguish C. nicholasi from C. antillensis , while the penial stylet is entirely different in shape and size. Radular tooth morphology is also notably different. In C. nicholasi , teeth are much shallower, more pointed yet blunt at the very tip, and have square, flat-edged denticles; in comparison, in C. antillensis the teeth are rhomboid, deeper, taper to a point and have backcurving pointed denticles.

Distinguishing C. nicholasi from the remaining four species in the C. antillensis complex is more challenging, although all were genetically distinct. The long, curved penial stylet of C. nicholasi was the most diagnostic character, clearly different from the short, straight stylet of C. ellingsonorum , the short, curved stylet of C. piercei or the wide, curved stylet of C. willetteorum . Radular morphology also differentiates C. nicholasi (straight tooth, blunt tip, small square denticles) from C. piercei and C. browneveorum (angled tooth, tapered tip, denticles angled outwards), C. ellingsonorum (more teeth, large square denticles) and C. willetteorum (irregularly angled and shaped denticles) ( Table 5 ).

Figures

Figure 1. Western Atlantic sampling sites; for more details, see Table 1. Top panel shows southern Florida peninsula and eastern Caribbean; bottom panel shows expanded view of inset box.

Figure 2. Consensus phylogenetic tree for Cyerce and Sohgenia based on maximum likelihood (ML) analysis of three concatenated loci. Percentages corresponding to significant bootstrap support are given below branches, and posterior probabilities from Bayesian inference (BI) analysis are shown in bold above branches. Capital letters label three key supported nodes. Haplotypes are coded by date–location–specimen number on terminals. Results of four species delimitation analyses are indicated by vertical bars; horizontal shaded bars enclose specimens grouped as species entities by all methods.

Figure 3. Histogram of pairwise Tamura–Nei (TrN)-corrected COI distances, showing barcoding gap; white bars denote intraspecific distances and black bars interspecific distances, based on automated barcode gap discovery (ABGD) and assemble species by automatic partitioning (ASAP) analyses.

Figure 4. Network of COI haplotypes colour coded by location, with the size of each circle denoting frequency.Black dots indicate unsampled haplotypes. Each bar crossing a line denotes one nucleotide substitution. A, Cyerce antillensis. B, Cyerce nicholasi.

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 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.

Figure 12. Live specimens of Cyerce nicholasi. A, specimen from Penicillus dumetosus in Sweetings Cay, Bahamas (isolate 07Swe01); actual body length, 4 mm. B, specimen from Rhipocephalus phoenix in Bimini, Bahamas (isolate 10Bim02); actual body length, 3 mm preserved. C, specimen from Pe.dumetosus in Bocas del Toro, Panama (isolate 15Pan02); actual body length, 5 mm. D, alternative view of specimen 15Pan02, showing brown lines along ceratal margin.

Figure 13. Cyerce nicholasi, radular scanning electron micrographs of isolate 10Bim03, 2 mm preserved body length. A, complete radula, with ascus attached to descending limb.B, leading tooth, showing damaged tip.C, close-up view of ascus, showing used teeth encased in tissue.