Elysia ornata Swainson 1840

Elysia ornata (Swainson, 1840)

(Figs. 4–5, 6 A, 7–8)

Thallepus ornatus Swainson 1840: 250, 359 (Type locality: undetermined, probably St. Vincent, U.S. Virgin Islands). Dolabrifera (?) ornata (Swainson, 1840) — Pilsbry 1895 –96 [1896]: 126.

Elysia ornata (Swainson, 1840) — Verrill 1901: 28 –29, pl. 4, fig. 5; Engel 1927: 113 –115, figs. 29–30; Pruvot-Fol 1946: 33; Er. Marcus 1957: 414; Ev. Marcus 1976b: 128; Ev. Marcus & Er. Marcus 1963: 20 –21, figs. 27–28, 64; Er. Marcus & Ev. Marcus 1970: 43 –44, figs. 80–83; Marcus 1972a: 292, fig. 18; Bandel 1976: 95 –96, fig. 8 (egg mass); Thompson 1977: 126 –128, figs. 25d–e, 26a; Ev. Marcus & Hughes 1974: 507, fig. 17; Ev. Marcus 1980: 63 –64, figs. 1–3, 38, 44; Jensen & Clark 1983: 5; Díaz Merlano & Puyana Hegedus 1994: 246; Clark 1994: 905; Espinosa & Ortea 2001: 44; García et al. 2002: 50, figs. 2E–F; Espinosa et al. 2005: 56; García et al. 2008: 69 –70; Valdés et al. 2006: 62 –63; Redfern 2013: 282 – 283, fig. 786; Krug et al. 2013: 1106–1108, fig. 1A–E, fig. 2A; Christa et al. 2014: fig. 3; Krug et al. 2015: 990 –991, figs. 3B, 4.

Type material. Thallepus ornatus— type material untraceable.

Material examined. Discovery Bay, Jamaica, 1 March 2006, 2 specimens (LACM 178581–82); Playa Kanoa, Curaçao, 4 Jan 2009, 1 specimen (LACM 178579); Spanish Waters inlet, Curaçao, 9 Jan 2009, 1 specimen (LACM 178580).

Additional material examined. Discovery Bay, Jamaica 1 March 2006, 1 specimen (isolate Eorn_06Jam03); Playa Kanoa, Curaçao, 4 Jan 2009, 1 specimen (isolate Eorn_09Cur01); 5 specimens, Bocas del Toro Panama, 30 July 2015.

Live animal. Brightly colored species, yet cryptic when buried among thalli of the alga Bryopsis; parapodial lines and mottled body coloration renders slugs difficult to see.

External anatomy. Overall color olive green, with black and smaller white spots scattered across head and parapodia; white dots sometimes forming medial line on head (Fig. 5 A–B). Rhinophores short, tapering to a point at rolled tips; surface smooth, lacking dots otherwise scattered across head. Bright white streak extending from base halfway up rhinophores. Distal half of rhinophores orange, with black band at tips. Foot not clearly distinct from parapodia, same green color without spotting. Transverse groove separating underside of head from foot. Parapodia extending to posterior end of body, uniting to form pointed tail. High-arching parapodia forming three siphonal openings when covering dorsum, with middle opening forming a prominent raised chimney halfway along body (Fig. 5 A). Parapodial margin somewhat undulating, with black marginal band slightly separated from orange submarginal band running along both outer and inner edge; some specimens with white dots running between marginal and submarginal band.

Pericardium small with short renopericardial extension, both white with scattered black spots, tiny red-orange dots and brown flecks. Large specimens with three dorsal vessels radiating from each side of renopericardial complex, branching irregularly and repeatedly; side branches anastomosing into complex network lining inner face of each parapodium (Fig. 7). Vessels often spaced at regular intervals, transparent but sometimes highlighted by large white spots or tiny red-orange dots. White reproductive glands visible within tissue of dorsum, divided by wide medial band of clear tissue running length of body to tail.

Internal anatomy. Radula with 9 teeth (LACM 178581), 6 teeth in ascending limb and 3 in descending limb (Fig. 8 A). Leading tooth elongate, widest at mid-length, tapering and slightly curved towards tooth tip, with cusp lacking denticles (Fig. 8 B). Housing depression for interlocking teeth “V”-shaped and extending ½ of tooth length (Fig. 8 B). Base of tooth approximately ⅓ of total tooth length. Ascus containing jumbled heap of discarded teeth (Fig. 8 C).

Penis short and broad, almost as wide as long, devoid of armature (Fig. 6 A). Deferent duct short and thin.

Reproduction and development. Clutches laid by E. ornata from Jamaica and Curaçao contained regularly spaced blobs of white ECY deposited along the inside of the upper face of the egg mass (Fig. 5 C–D). The ECY was deposited as clumps of tiny granules within a thin casing; deterioration of the casing released the granules as larvae developed (Fig. 5 D). In related candidate species from the Pacific, belonging to the “ E. marginata ” complex, ECY was deposited as a continuous black ribbon (“sp. 1”), or as regularly spaced blobs of bright yellow (“sp. 2” from Guam), darker gold (“sp. 3” from Japan), or orange (“sp. 4” from Japan) (Krug et al. 2013).

One clutch laid by a specimen from Curaçao had a mean egg diameter of 59.4 ± 2.6 µm (n = 14 ova), while a clutch deposited by a Jamaican specimen had a mean egg diameter of 55.8 ± 2.2 µm (n = 25 ova). Development is planktotrophic. The encapsulated period was 6 d at room temperature (n = 2 clutches). At hatching, mean larval shell width was 111.1 ± 5.7 µm and 119.6 ± 8.3 µm for two clutches from Jamaica (n = 25 larvae per clutch). A characteristic of this species is the presence of multiple embryos developing within some capsules (Fig. 5 D). Of three clutches laid by specimens from Jamaica, clutch #1 contained primarily 4– 6 eggs per capsule; in clutch #2, most capsules contained 2– 4 eggs; and in clutch #3 (the smallest), capsules held only one egg. All embryos completed development and hatched as veliger larvae.

Host ecology. The only host described in the literature for E. ornata and identified in the present study is Bryopsis, generally B. plumosa. Species of Bryopsis are also the host of the five Indo-Pacific species that form a clade with E. ornata, indicating speciation in this complex was not driven by host shifts.

Phylogenetic relationships. Elysia ornata is a derived member of subclade 3, which includes five tropical Indo-Pacific species: four candidate species in the marginata-grandifolia complex, plus E. rufescens (Fig. 4; Krug et al. 2013). Its sister species (“ E. cf. marginata sp. 2”) is morphologically similar but deposits yellow ECY in its egg masses, and is known from Japan, Guam and Vanuatu. The divergence between E. ornata and E. cf. marginata sp. 2 is ~8%, the minimum inter-specific distance proposed by Krug et al. (2013) for delimiting Elysia spp. using COI barcodes. Subclade 3 likely diversified in the Indo-Pacific prior to colonization of the Caribbean by the ancestor of E. ornata, given its derived position.

Range. Aruba (Valdés et al. 2006), Bahamas (Redfern 2013), Barbados (Ev. Marcus & Hughes 1974), Bermuda (Verrill 1901), Brazil (García et al. 2002, 2008), Colombia (Ev. Marcus 1976b), Costa Rica (Espinosa & Ortea 2001), Cuba (Espinosa et al. 2005), Curaçao (Engel 1927; Ev. Marcus & Er. Marcus 1963; Er. Marcus & Ev. Marcus 1970; present study), Florida (Ev. Marcus 1972a; Jensen & Clark 1983; Clark 1994), Guadeloupe (Valdés et al. 2006), Jamaica (Thompson 1977; present study), St. Vincent (Swainson 1840), Trinidad and Tobago (Valdés et al. 2006). Also recorded from the Eastern Atlantic in the Canary Islands and the Azores (Ortea et al. 2001; Malaquias et al. 2009).

Remarks. Thallepus ornatus was described by Swainson (1840: 250) based on an unpublished drawing by Reverend Lansdown Guilding. The animal was described as “sea green, covered with minute black and white dots; the edges or crests of the reflected mantle have a broad edging of the richest orange, bordered on their outer edge with a line of deep black; the tentacula are also orange, and formed like those of Aplysia.” In another entry Swainson (1840: 359) added “Body more slender and fusiform [than Aplysia]; the lobes of the mantle short, and incapable of being used for swimming; tentacula two, large, ear-shaped; eyes not visible.” This description matches the external morphology and coloration of the species commonly referred to as Elysia ornata in the Caribbean literature (see Ev. Marcus & Er. Marcus 1963; Er. Marcus & Ev. Marcus 1970; Ev. Marcus 1972a; Thompson 1977; Ev. Marcus & Hughes 1974; Espinosa & Ortea 2001; Valdés et al. 2006). Verrill (1901) transferred T. ornatus to Elysia and Ev. Marcus (1980) subsequently re-described as E. ornata based on Caribbean specimens.

However, other genetically distinct Indo-Pacific species have a similar external morphology and anatomy and have been included in the same species (Jensen 1992), thus it is important to determine the type locality of all available names for this species complex. No type locality was specified in the original description of Thallepus ornatus, but because Reverend Guilding [1797–1831] lived in St. Vincent and worked exclusively on Caribbean natural history (Howard & Howard 1985), it is almost certain that the specimen used in the drawing was found in the Caribbean Sea. Two other large species of Elysia feeding on Bryopsis spp. were described from the tropical Pacific. Both have a black band along the parapodial edge and a submarginal orange band similar to those of E. ornata. The first species, E. grandifolia (Kelaart, 1858), was described from Sri Lanka as having black and gold marginal lines along parapodia that fused with the tail (Kelaart 1858). The second species, E. marginata (Pease, 1871) was originally described from the Hawaiian Islands and subsequently from Tahiti as having a white band between the orange and black marginal bands (Pease 1871). Authorities subsequently debated whether E. grandifolia had denticulate teeth (Eliot 1904, 1908; O’Donoghue 1932). Both E. marginata and E. grandifolia were synonymized with E. ornata based on morphological comparisons between Pacific and Caribbean material (Ev. Marcus 1980; Heller & Thompson 1983; Jensen 1992).

Recent integrative taxonomic work revealed that the E. marginata - grandifolia complex contained four candidate species in Pacific, all distinct from each other and from E. ornata by (1) molecular sequence analyses of two genetic loci; (2) external features including color of rhinophores and marginal bands, folding of parapodia into siphonal openings, tail shape, and pattern of dorsal vessels; and (3) color and pattern of ECY (Krug et al. 2013). Elysia ornata is therefore restricted to the Caribbean, and some related Pacific species await formal description.