Doris ocelligera ( Bergh, 1881 )

Renau, Mar F., Salvador, Xavier & Moles, Juan, 2024, Molecular and morpho-anatomical assessment of the family Dorididae (Mollusca, Nudibranchia) in the Mediterranean and North-East Atlantic, European Journal of Taxonomy 943, pp. 59-79 : 65-68

Doris ocelligera ( Bergh, 1881)

Figs 1–3 , 4F–H , 5A–C , 6A

Staurodoris ocelligera Bergh, 1881: 95 , pls 11–21.

Doris lutea Risso, 1826: 31 .

Doris ocelligera – Pruvot-Fol 1954: 234. — Schmekel 1968a: 114. — Schmekel & Portmann 1982: 75–77, pls 20.2, 30.8 fig. 7.12. — Ortea et al. 2014: 64–65.

Type locality

Trieste, Italy, the Mediterranean Sea.

Diagnosis

Compressed body, blueish colouration of mantle, sometimes with yellowish mantle margin, tubercles darker. Rhinophores dark yellow. Gills composed of 10 pinnate leaflets. Cusp of outermost lateral teeth extending more than ⅔ of total length. Seminal receptacle spherical, orange. Bursa copulatrix bean-shaped, rose in colour.

Material examined

SPAIN – Catalonia • 2 specs (1 sequenced, 2 dissected: L = 1.2 cm, L = 0.6 cm); Girona, Sant Feliu de Guíxols, Coves Cala Maset ; 41.8098° N, 3.0412° E; 1 m depth; 9 Aug. 2022; Xavier Salvador leg.; GenBank: OR286434 ; ZSM20240260 • 2 specs (1 sequenced); same data as for preceding; 10 Jul. 2022; Xavier Salvador leg.; GenBank: OR286433 ; ZSM20240259 • 1 spec. (sequenced); Girona, L’Escala ; 42.1153° N, 3.1689° E; 12 m depth; 8 Mar. 2015; Xavier Salvador leg.; GenBank: OR286432 ; MCZ395160 .

Description

EXTERNAL MORPHOLOGY ( Fig. 4G ). Body compressed, oval-shaped. Mantle blue to dark green when preserved, yellowish alive; margins and central part of dorsum paler, showing a whitish and violet colouration, respectively. Mantle edge extending, covering foot. Dorsal tubercles protruding, dark blue, homogeneously distributed, but less numerous in margins, and especially concentrated around rhinophores. Spicules seen in tegument by transparency, connecting tubercles. Rhinophores dark yellow, lamellated (6 lamellae); rhinophoral sheaths blue. Gills exposed, blueish-violet in colour, consisting of 10 pinnate leaflets, with a slightly translucid apex.

RADULA ( Fig. 5A–C ). Radular formula 22–32 ×33–37.1.0.1.33. Teeth hook-shaped, cusp acute. First lateral tooth with a width base, short cusp. Inner and outermost lateral teeth thin, smooth. Outermost with a longer cusp, extending more than ⅔ of total length.

DIGESTIVE SYSTEM. Salivary glands sausage-shaped, extending after pharynx to oesophagus. Stomach connects with a caecum and intestine, conformed by fine and translucid tissue. Digestive gland dark grey.

REPRODUCTIVE SYSTEM ( Fig. 6A ). Gonad covering digestive gland, representing three-quarters of viscera. Ampulla sausage-shaped, pink in colour, folded once, end connecting to gonad rather sharp. Vaginal duct short, thin, smooth. Penial sheath thick, conforming to distal part of vas deferens. Proximal prostatic part of vas deferens little folded ( Schmekel & Portmann 1982). Seminal receptacle spherical, orange, connected with bursa copulatrix via a thin duct. Bursa copulatrix bean-shaped, rose, with darker end.

Ecology

Found above the sponge Terpios gelatinosus (Bowerbank, 1866) , copulating with another specimen, smaller and blue. As this nudibranch grazes on the sponge, it sinks into it until totally camouflaged. No sponge spicules were found in the stomach or intestine of the dissected specimen studied. The egg mass is a spiral ribbon of light-yellow eggs, with just over 5000 eggs per cm of ribbon, with a mean diameter of 85 µm ( Ortea et al. 2014). These eggs are already fully capable of development and swimming veliger hatch after 12 days at 16°C ( Schmekel & Portmann 1982).

Distribution

Doris ocelligera is distributed from the North of the Iberian Peninsula to the Savage Islands, Madeira, the Canary Islands, and Cape Verde. It also lives in the Azores Islands ( Azevedo & Gofas 1990) and the Western Mediterranean ( Ortea et al. 2014). Our three samples, including four specimens in total, were collected on the Catalan coast: ZSM20240259 and ZSM 20240260 in Sant Feliu de Guíxols, and MCZ 395160 in L’Escala. No specimens belonging to D. ocelligera were found in the sampling sites of the Nort-East Atlantic (see Fig. 1 ).

Remarks

Living specimens, both the sequenced and the one copulating with it, presented different colourations. The one described and sequenced was dark yellow/brown, whereas the other (only sequenced) was blue. Once fixed in EtOH, both specimens turned into a blueish colouration. The description provided herein matches Bergh’s (1881: 95) description of D. ocelligera : “Dorid, oval in shape, with yellow or orange mantle, with dark ochre to black dots on the top of the most developed tubercles of the notum. The colour of the posterior part is variable, from light blue to black or from black to yellow, and the apex of the eyes is dark. It also presents white rhinophores and blue gills”. Therefore, the blueish morphotype is here attributed to D. ocelligera . Risso’s (1826) description of D. lutea is flimsy, but he described a nudibranch characterized by its mantle’s golden yellow colouration, thus potentially like D. ocelligera . Being a species of small size, D. ocelligera has been confused with juveniles of D. verrucosa . However, when compared, only the morphology of the outer lateral teeth of the radula resembles each other. The reproductive system of D. ocelligera is very different from that of D. verrucosa , which lacks a reduced prostate undifferentiated from the vas deferens and a seminal receptacle with a similar shape as the copulatory bursa and separated from it ( Ortea et al. 2014). Both species differ in the ampulla, which is simply a folded tube in D. ocelligera while elongated and tubular in D. verrucosa (Lima & Simone 2015) . The prostatic part of the vas deferens is less convoluted and shorter in D. ocelligera than in D. verrucosa . Also, the strong retractor muscle observed in the distal part of the vas deferens of D. verrucosa was not observed in D. ocelligera ( Schmekel & Portmann 1982) . Comparing the radular teeth of D. ocelligera (ZSM20240260) and D. verrucosa (ZSM20210044, Fig. 7A–B ), noticeable differences come to light. While the first lateral teeth resemble each other, the inner and outermost lateral teeth exhibit slight differences. In D. verrucosa , the superior part of the innermost lateral teeth presents a thin and high arch before the beginning of the sharp and hook-shaped cusp, whereas in D. ocelligera , this arch is less noticeable. As for the outermost lateral teeth, those from D. verrucosa present a perfect hook shape with a shorter cusp, only extending ⅓ of the total length.

Taking all the characters into account, this species is clearly distinguished from D. verrucosa by the external colouration, the size and shape of the mantle tubercles, the morphology of the lateral teeth, the extension of the outermost lateral teeth cusp, and the shape and size of the reproductive structures.

Figures

Fig. 1. Map of the Iberian Peninsula and North-West Africa showing the sampling localities where specimens of Doris ocelligera (Bergh, 1881) were collected. The purple triangles show the locations where the blueish morphotype specimens were taken, whereas the yellow circles show the locations where the yellow morphotype specimens were collected. Map generated athttps://www.simplemappr.net

Fig. 2. Bayesian phylogenetic tree of Dorididae Rafinesque, 1815 based on the concatenated alignment of COI, 16S, and H3 markers. Posterior probabilities and bootstrap support values are shown above and below branches, respectively. The outgroup used to root the tree was the genus Aphelodoris Bergh, 1879. Green dots indicate nodes with maximum branch support in both analyses. The scale bar indicates substitutions per site. Names of the sequences downloaded from GenBank have not been modified, yet taxa that may belong to a different identity are specified between quotation marks. Specimens sequenced in this study are highlighted in bold.

Fig. 3. Results from ASAP for both COI (top) and 16S (bottom) markers of the alignment of the species within the genus Doris Linnaeus, 1758 based on the phylogenetic tree results. Colour boxes refer to species hypotheses and the dash-line is the threshold (representing a 5–10% genetic divergence distance) in which species hypotheses were selected.

Fig. 4. A. Doris verrucosa Linnaeus, 1758 (ZSM20210044) from Thau, SE France. B–E. Doris berghi (Vayssière, 1901) comb. rest. B. Specimen from Sant Feliu de Guíxols, NE Spain (ZSMMol20210024). C. Specimenfrom Begur,NE Spain (MCZMal395161).D. Specimenfrom GranCanaria (ZSM20240262). E. Specimen from Galicia, NW Spain (ZSM20240261). F–H. Doris ocelligera (Bergh, 1881). F. Specimen from l’Escala, NE Spain (MCZ395160).G. Specimen from Sant Feliu de Guíxols, NE Spain (ZSM20240260). H. Specimen from Sant Feliu de Guíxols, NE Spain (ZSM20240259).

Fig. 5. Scanning electron micrographs of the radular teeth. A–C. Doris ocelligera (Bergh, 1881) (ZSM20240260). D–F. Doris berghi (Vayssière, 1901) comb. rest. (ZSM20240261). Showing first (fl) and subsequent (cl) lateral teeth.

Fig. 6. Schematic drawing of the reproductive systems. A. Doris ocelligera (Bergh, 1881). B. Doris berghi (Vayssière, 1901) comb. rest. Abbreviations: A = ampulla; Bc = bursa copulatrix; Fgl = female glands; Ps = penial sheath; R = seminal receptacle; Vd = vas deferens; Vdu = vaginal duct. The black arrowheads represent the connection of the ampulla to the gonad.

Fig. 7. A–B. Scanning electron micrographs of the radular teeth of Doris verrucosa Linnaeus, 1758, showing first (fl) and subsequent (cl) lateral teeth.