Cyerce antillensis Engel, 1927

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 : 955-961

Cyerce antillensis Engel, 1927

( Figs 1–5 , 8D , 9–11 )

Cyerce antillensis Engel 1927: 117–118 , fig. 38; Marcus and Marcus 1963: 17–19, figs 22–24;

Marcus and Hughes 1974: 505–506, figs 11, 12; Clark and Defreese 1987: 259–279; Jensen 1993a: 157; Clark 1994: 906; Turner et al. 2020: 42.

Cyerce cf. antillensis Goodheart et al. 2016: 23–25 .

Cyerce habanensis Ortea and Templado 1988: 11–13 , figs 1, 2.

Cyerce sp. 3 Krug et al. 2015: 989–991.

Cyerce sp. 4 Christa et al. 2015: fig. 1b.

Cyerce cf. edmundsi ( Thompson 1977) – Händeler and Wägele 2007: 233–238.

Type material

Cyerce antillensis Engel 1927 – Syntype: Tobago, Caribbean Sea (ZMA.MOLL.137581), 1914–1916, not examined. Four syntypes: (ZMUC GAS-001551), 1 April/ 30 April 1916, not examined. Cyerce habanensis Ortea and Templado 1988 – Holotype: Havana, Cuba (MNCN 15.05/1063), 17 July 1988, depth 1 m, 13 mm in length, not examined. One paratype: (MNCN 15.05/1063), 17 July 1988, depth 1 m, 11 mm in length, not examined. One paratype: private collections of Jesús Ortea, 26 June 1988, depth 1 m, 8 mm in length, not examined.

Material examined

Netherlands Antilles, Caribbean Sea , 16 August / 25 August 2004, one specimen preserved, isolate MM109 A ( LACM 2004.04.9 A) . Bimini, Bahamas, Caribbean Sea , October 2001, one specimen, 5 mm preserved length, isolate 10Bim01 .

Range

Panama, Dominica, Florida, Bahamas, Curaçao (present study), Tobago ( Engel 1927), Cuba ( Ortea and Templado 1988), Cayman Islands ( Turner et al. 2020), Roatan ( Charteris 2022).

Description

External morphology: Body ranging from mustard yellow to pale green ( Fig. 9A, E, F ) and to darker green ( Fig. 9B, D ; see also Turner et al. 2020). Notum, foot colour translucent white, with white speckling along margin ( Fig. 9C ). Head white to pale yellow in ground colour, with greyish patches outlining eyes ( Fig. 9A, E, F ); head darker grey on Cayman Islands specimens ( Fig. 9D ). Rhinophores white to pale yellow, overlaid with grey and burgundy patches and speckled with white dots, most concentrated at tips. Oral tentacles similar in colour pattern to rhinophores.

Pericardium white, raised, irregularly shaped. Anal papilla grey or white, anterior and to the right of pericardium. Dorsal vessels radiating out from pericardial complex, either clear ( Fig. 9A, E ) or capped in white for part of their length ( Fig. 9F ). Two lateral vessels emerging per side, forking, with each branch running to the base of one ceras ( Fig. 9E, F ). Paired posterior vessels running length of notum to base of pointed tail, with short side branches emerging to connect to cerata along body margin.

Cerata partly inflated, fan shaped; translucent, with scattered white specks ( Fig. 9 ). Cerata densely packed with spherical glandular inclusions, ranging from almost translucent to pale yellow and varying within a ceras; darker yellow inclusions usually most concentrated along ceratal margins. Density and number of yellow spherical bodies imparting darker yellow colour to some cerata on individual specimens ( Fig. 9D ). Base of cerata often with a burgundy line extending onto body, typically located dorsomedially on ceras ( Fig. 9A, E ) but missing entirely on some specimens ( Fig. 9F ). Ceratal margin usually crenulate, with pointed extensions outlined with white or yellow specks, sometimes with one or more larger yellow spots of irregular shape.

Internal morphology: Buccal mass <1 mm long; pharyngeal pouch much larger than buccal bulb. One specimen (5 mm body length) with a total of 21 radular teeth, 10 on ascending limb and 11 on descending limb (isolate 10Bim01); second specimen with 11 teeth on ascending limb and 9 on descending limb (isolate LACM 2004.04.9 A; Fig. 10A ). Teeth with distinctively rhomboid shape along cutting edge, extending from long, narrow base, over which previous tooth lies ( Fig. 10A, B ). Tooth angled (25°), tapering to pointed tip with a downward-facing front denticle, giving a blunted appearance to very tip of tooth. Leading tooth 60 µm long on specimen 10Bim01, 67 µm long on specimen LACM 2004.04.9 A ( Fig. 10B ). Leading tooth with a row of 11 denticles distributed evenly along either side of tooth; denticles slightly backward-curving to a point. Ascus with> 10 pre-radular teeth.

Penis with cylindrical stylet at opening; stylet <50 µm in length, with pointed triangular tip and oval opening ( Fig. 8D ).

Ecology

Feeds on H. opuntia , especially in areas of high flow. Not sampled on alternative host algae. Specimens collected from H. opuntia would not feed on Pe. dumetosus .

Reproduction

Reproductive data were obtained for clutches laid by specimens from Sweetings Cay, Bahamas in 2010. Egg masses lacked extracapsular yolk and had one embryo per capsule. The mean ± SEM diameter of uncleaved ova was 62.0 ± 1.7 μm (N = 7) for one clutch and 61.6 ± 2.1 μm (N = 15) for a second clutch. The mean ± SEM larval shell width across the aperture was 101.9 ± 1.3 μm (N = 25) for one clutch. Both egg and larval shell diameters are within the size range for planktotrophic species in Sacoglossa ( Krug et al. 2015). Larvae swam upon hatching, and no metamorphosis was observed.

Remarks

Specimens identified provisionally as ‘ Cyerce antillensis ’ were recovered as six lineages, supported as distinct candidate species by all molecular species delimitation analyses ( Fig. 2 ). The taxon we recognize as C. antillensis was the most widely distributed of the six species, ranging from the northern Bahamas and Florida Keys to Dominica and Curaçao in the south-eastern Caribbean and to Panama in the south-western Caribbean. The type locality ( Tobago) was not sampled in the present study, but was close to sampled localities ( Dominica and Curaçao). Notably, C. antillensis co-occurs with at least three of the other complex members ( C. nicholasi , C. piercei and C. browneveorum ), and its range encompasses the narrow endemic C. willetteorum from Great Stirrup Cay, Bahamas. The overlapping ranges of multiple pseudocryptic species have contributed to the confusion over the identity and ecology of C. antillensis for almost a century.

Engel (1927) described C. antillensis based on several preserved specimens, some mutilated and all lacking their original coloration, which impeded comparison with other species of Cyerce . The syntypes of C. antillensis had a transverse groove across the foot, bifurcated rhinophores, enrolled oral tentacles, penis at the base of the right rhinophore, dorsomedially placed and elevated pericardium, and anal papillae situated anteromedially between the pericardium and right rhinophore ( Engel 1927). However, those characteristics are all shared among the six species recognized here in the C. antillensis complex. The drawings and description of the radula and penial stylet provided in the original description of C. antillensis ( Fig. 11 ) provide the most diagnostic characters for differentiating the name-bearing species C. antillensis from the five candidate species delimited in the present study. The illustration of the radular tooth of C. antillenis matches in all respects that of the species we identify as C. antillensis sensu Engel (1927) , but not any of the other Caribbean species delimited herein. The tooth, as drawn by Engel ( Fig. 11 ), is rhomboid, straight and serrated, with denticles that were visible individually by light microscopy; the tip is blunt, with a slightly pronounced downward-facing cusp. A gentle, lateral indentation, running parallel to the base of the tooth, is also figured. Engel (1927) also reported radular tooth counts of 7 and 11 teeth in the ascending and descending limbs, respectively, from one specimen, 10 and 10 teeth in the ascending and descending limbs of a second specimen, and both having a disordered pile of teeth in the ascus. Thus, only one of our delimited species has a tooth shape and radular count consistent with that described for C. antillensis , allowing a positive identification of this species despite its long history of taxonomic confusion.

Both tooth shape and number are very different in C. cf. cristallina , which has straight, very slender teeth. The tooth shape of C. antillensis was also clearly distinct from that C. nicholasi , C. piercei and C. ellingsonorum , which have thinner, more angled teeth, with differently shaped tips; all those candidate species also have fewer teeth, especially in the ascending limb, than C. antillensis . Overall tooth shape is also markedly different in C. browneveorum , which has thinner, more angled teeth with a wider base; lacks the downward notch at the tip; and has fewer teeth than C. antillensis .

Engel (1927) also described and figured C. antillensis as having a short, pointed stylet at the opening of the penis, comparable to our specimens. In contrast, the long, curved stylet of C. nicholasi is entirely distinct. The stylet of C. piercei was more curved than that figured for C. antillensis , whereas that of C. ellingsonorum had a wider, more open tip. Only the material we identified as C. antillensis has a straight, short, pointed stylet matching the original description. Descriptions of C. antillensis by Marcus and Marcus (1963) and Marcus and Hughes (1974) also match our specimens, including in the internal morphology of radular teeth and the penial stylet; the specimens studied by the Marcuses and colleagues were collected from Halimeda in Curaçao and Barbados, close to the type locality of C. antillensis , and are consistent with our redescription here.

In all respects, the Western Atlantic species we recognize as C. antillensis is also the only species matching the description of C. habanensis . Based on external morphology and radular tooth morphology, we consider C. habanensis a junior synonym of C. antillensis , a conclusion also reached by prior workers ( Valdés et al. 2006, Goodheart et al. 2016). In the original description of C. habanensis, Ortea and Templado (1988) include no details from the original description of C. antillensis , nor do they cite it, suggesting that the original description was never consulted. Likewise, the redescriptions of C. antillensis by Marcus and Marcus (1963) and Marcus and Hughes (1974) are neither cited nor discussed by Ortea and Templado (1988). In the remarks comparing C. antillensis to C. habanensis, Ortea and Templado (1988) draw on details for nominal ‘ C. antillensis ’ only from Thompson (1977), who reported that C. antillensis had light brown cerata with a dark apex, and brown rhinophores, distinct from C. habanensis . However, Thompson (1977) studied preserved specimens from Jamaica, and we show that the common species of Cyerce from Jamaica is an endemic taxon distinct from other complex members. Therefore, Thompson (1977) did not describe C. antillensis sensu Engel (1927) . The radular tooth figured by Thompson (1977) is also distinct from that figured by Engel (1927), matching C. ellingsonorum from Jamaica but not C. antillensis . Thus, the comparison with Jamaican material in the description of C. habanensis was inappropriate and led to the proposal of a new name for C. antillensis .

Morphologically, the species we recognize as C. antillensis is indistinguishable from C. habanensis and conforms to redescriptions of specimens considered ‘ C. antillensis ’ collected on Halimeda near the type locality ( Marcus and Marcus 1963, Marcus and Hughes 1974). Ortea and Templado (1988) described C. habanensis from Cuba as having transparent cerata with two reddish-brown spots, one at the base of the ceras and a second spot lying above the first spot. Marcus and Marcus (1963) and Marcus and Hughes (1974) describe and illustrate cerata with the same shape and spotting patterns. The cerata of our specimens had one reddish-brown spot at the base, and some had a second spot above the first. Ortea and Templado (1988) also described the ceratal margin as slightly angled, with white pigmentation, as in our specimens. The digestive gland was described as dark green through the body, the pericardium as light brown in colour, with white papillae, and the rhinophores as having superficial white pigmentation, all of which are characteristics of our specimens. The tentacles were described as pigmented with brown; in our specimens, tentacles were pale yellow to light brown, with white specks. Internally, the radular morphology described by Ortea and Templado (1988) matches our C. antillensis specimens, although only a rough drawing of the radular tooth was provided in the description of C. habanensis , and no mention of a penial stylet was included.

Ortea and Templado (1988) reported that their material came from H. opuntia and was highly cryptic on it. The C. antillensis specimens studied by Marcus and Marcus (1963) and Marcus and Hughes (1974) also came from Halimeda . Our molecular and ecological data confirm that C. antillensis is the only widespread Caribbean species of Cyerce that consumes the green alga H. opuntia ( Ortea and Templado 1988) . Thus, both morphology and ecology establish that our C. antillensis Engel, 1927 is the same species as C. habanensis Ortea and Templado, 1988 .

The conflicting reports of host use by C. antillensis have contributed to the confusion over the identities of species in the C. antillensis complex. Nominal C. antillensis specimens were reported variously to feed on Pe. dumetosus ( Clark and Busacca 1978, Jensen 1980, 1981, 1983, 1993a, Clark 1984, Clark and Defreese 1987), Udotea ( Jensen 1983, 1993a), Halimeda tuna (J.Ellis & Solander) J.V.Lamouroux 1816 and Halimeda monile (J.Ellis & Solander) J.V.Lamouroux 1816 ( Clark and Defreese 1987) or unidentified Halimeda spp. ( Marcus and Marcus 1963, Marcus and Hughes 1974, Jensen 1980). Here, we show that only C. antillensis specializes on H. opuntia , whereas other complex members feed on Pe. dumetosus , and C. piercei also consumes H. incrassata and Udotea spp. These differences in host use are likely to explain the distinct radular tooth morphology of C. antillensis compared with the remaining complex members, which share a much more similar tooth shape consistent with a common host alga ( Penicillus ).

Our study is consistent with the redescription of C. antillensis by Marcus and Hughes (1974) and with more recent field guides ( Turner et al. 2020, Charteris 2022). External morphology differentiates C. antillensis from the other complex members. The cerata of C. nicholasi , C. piercei and C. browneveorum are all more translucent, narrow and elongated than the cerata of C. antillensis , which are more rounded and typically appear yellow from the spherical inclusions. The darker, more solid yellow to green body of C. antillensis also differentiates this taxon from the remaining members of the complex, which have lighter bodies ranging from pale yellow to mottled white and yellow.

Planktotrophic development can also distinguish C. antillensis from some other complex members ( Table 5 ). Clark and colleagues reported lecithotrophic development and an egg diameter of 112 μm for C. antillensis from the Florida Keys, collected from Penicillus ( Clark and Busacca 1978, Clark and Jensen 1981). We found that C. antillensis Engel, 1927 has smaller, planktotrophic larvae and does not feed on Penicillus . Clark and colleagues did not recognize that ‘ C. antillensis ’ was a species complex and, presumably, reported lecithotrophy from C. browneveorum , the Penicillus -feeding complex member endemic to the Florida Keys. We also found lecithotrophic development in C. nicholasi , which broadly overlaps in range with C. antillensis but is distinguished by larval type, algal host use and morphology. Both C. antillensis and C. piercei had planktotrophic development and fed on Halimeda spp. ; therefore, they could not be distinguished by ecological or reproductive characteristics but were easily differentiated by external and internal morphology.

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 9. Live specimens of Cyerce antillensis. A, specimen from Bimini, Bahamas, showing notum; actual size, 8 mm alive.B, specimen from Cayman Islands photographed underwater by Everett Turner.C, specimen from Bimini, Bahamas, showing ventral surface of foot. D, specimen from Lee Stocking Island, Bahamas; actual size, 9 mm alive.Photograph credit:Anne DuPont.E, specimen from Bimini, Bahamas, showing notum; actual size, 5 mm preserved.F, specimen from Bimini, Bahamas, showing close-up of pericardial complex; actual size, 9 mm alive.

Figure 10. Cyerce antillensis, radular scanning electron micrographs for isolates 10Bim01 (A–C) and MM109A (LACM 2004-04-9A; D, E). A, complete radula, including ascus, from isolate 10Bim01. B, leading tooth. C, close-up of ascus.D, complete radula from isolate MM109A; ascus not present. E, close-up of inset box, showing teeth on ascending limb.

Figure 11. Cyerce antillensis, original drawing from Engel (1927).