Amphorina farrani (Alder & Hancock, 1844)

Korshunova, Tatiana, Malmberg, Klas, Prkic, Jakov, Petani, Alen, Fletcher, Karin, Lundin, Kennet & Martynov, Alexander, 2020, Fine-scale species delimitation: speciation in process and periodic patterns in nudibranch diversity, ZooKeys 917, pp. 15-50 : 15

Amphorina farrani (Alder & Hancock, 1844) Figs 1 -3 , 4a-c , 7a

Eolis farrani Alder & Hancock, 1844: 164-165; Alder & Hancock, 1845: fam 3, pl. 35.

Galvina farrani (Alder & Hancock, 1844): Bergh 1873: 622; Colgan 1914: 183-185.

Cavolina farrani (Alder & Hancock, 1844): Gray J.E. 1857: 226.

Eubranchus farrani (Alder & Hancock, 1844): O’Donoghue 1926: 128.

Eubranchus farrani : sensu Edmunds & Kress, 1969: forms A & B only: 890, fig. 2 A, B.

Amphorina farrani (Alder & Hancock, 1844): Martynov 1998: 775.

Amphorina alberti Quatrefages, 1844: 146-151, pl. 3, fig. 5, pl. 4, fig. 3.

Aeolis adelaidae Thompson, 1860: 49.

Eolis robertianae Mc'Intosh, 1865: 393.

Eolis tricolor sensu Friele and Hansen 1876, non Forbes 1838.

Non Amphorina alberti sensu Trinchese 1877-1879 and auctt. (= Trinchesia spp.)

Non all forms of Eubranchus farrani sensu Edmunds & Kress, 1969 (mixture of several species)

Non Eubranchus farrani sensu Schmekel and Portmann 1982: 241-243, taf. 14, Fig. 1 - 3 , abb. 7.78 (= Amphorina andra sp. nov. + mixture of species)

Material examined.

Neotype. NE Atlantic, Cornwall, Newlyn Marina, Great Britain and Ireland (50°06'10.00"N 05°32'45.00"W), 10-20 m depth, stones with hydroids, 12.08.2015, coll. David Fenwick (GNM Gastropoda - 9268, preserved length 4.5 mm). Other specimens. NE Atlantic, England, Cornwall, Newlyn Marina (50°06'10.00"N 05°32'45.00"W), 10-20 m depth, stones with hydroids, 12.08.2015, coll. David Fenwick (GNM Gastropoda - 9267, preserved length 3 mm, GNM Gastropoda - 9269, preserved length 2.5 mm, GNM Gastropoda - 9270, preserved length 4 mm, GNM Gastropoda - 9271, preserved length 3.5 mm), GNM Gastropoda - 9273, preserved length 5.5 mm). Mediterranean Sea, France, Banyuls (42°28'58.00"N 03°08'13.00"E), 10-12 m depth,.09.2010, coll. Alexander Martynov and Tatiana Korshunova, one specimen (ZMMM Op-702, 9.5 mm in length, live, preserved length 4 mm). NE Atlantic, Spain, Vigo (42°24'06.00"N 08°72'07.00"E), 5-10 m depth,.09.2010, coll. Tatiana Korshunova and Alexander Martynov, one specimen (ZMMU Op-704, 7.5 mm in length, live, preserved length ca. 4 mm). NE Atlantic, Spain, Vigo (42°24'06.00"N, 08°72'07.00"E), 5-10 m depth, 09.2010, coll. Tatiana Korshunova and Alexander Martynov, one specimen (ZMMU Op-705, 6.5 mm in length, live, preserved length 3 mm).

Diagnosis.

Body up to 20 mm; large dorsal pigment spots, if present, yellow-orange, bright; in specimens with bright yellow orange spots on dorsal side and cerata, a distinct yellow-orange spot or stripe on the tail is always present; completely pale specimens lacking tail spot or stripe; no light pinkish subapical ring on cerata; absence of punctuated white line on edge of foot; cerata commonly moderate in width without distinctly attenuated apices; digestive gland in cerata relatively broad without distinct short branches; up to four anterior rows of cerata; radular formula 35-38 x 1.1.1, copulative stylet short and slightly bent at the top, seminal receptacle pear-shaped without short distinct stalk between reservoir and short wide base.

Description.

External morphology. The live length of the neotype is ca. 10 mm (Fig. 4a ). The length of adult specimens may reach 20 mm and more. The body is narrow. The rhinophores are smooth and 1.5-2 times longer than the oral tentacles. The cerata are relatively long, swollen. Ceratal formula of the neotype: right (1, 3, 3; anus, 3, 3, 2, 1) left (1, 3, 4; anus, 4, 3, 2, 1). The foot is narrow, anteriorly without foot corners.

Colour. There are three main colour morphs with several subdivisions of colour variations (Fig. 3 ), from a completely pale body and cerata with reduced orange-yellow pigment spots, to specimens with distinct orange-yellow spots on the body and a broad subapical orange-yellow ring on each ceras, sometimes with a deep maroon body colour. No specimens with blotches of blackish surface pigmentation have been observed, nor any specimens with uniformly bright orange bodies. Specimens with distinct orange-yellow spots on the body always have an orange-yellow spot or stripe on the tip of the tail. The upper part of the rhinophores is covered with orange pigment and scattered small white dots without a light pinkish pigment ring. The oral tentacles are similarly coloured.

Anatomy. Digestive system (Fig. 4 , a4-a11, c4-c7). The jaws are triangularly ovoid. The masticatory processes of the jaws bear a single row of ca. 20-25 distinct denticles. The radular formula in three studied specimens is 35-38 x 1.1.1. The radular teeth are yellowish. The central tooth is narrow, with a low cusp and 3-7 lateral denticles, including smaller intercalated denticles that may occur in different parts of the tooth.

Reproductive system. (Fig. 7A ). The ampulla is moderate in length and swollen (Fig. 7A , am). The prostate is distinct, moderately long and wide (Fig. 7A , pr). The prostate transitions to a penial sheath, which contains a conical penis with a short, chitinous, very slightly curved stylet (Fig. 4 , a10, a11). A supplementary ( “penial”) gland is relatively short and inserts into the base of the penis (Fig. 7A , pg). The seminal receptacle is relatively small, irregularly oval (Fig. 7A , rs) with a large widened base to which it transits without a distinct stalk. The female gland mass includes mucous and capsular glands (Fig. 7A , fgm).

Distribution and habitats.

Mediterranean Sea and all European Atlantic coasts to Norway. It lives from very shallow water (0-0.5 m) to ca. 20 m.

Remarks.

Morphologically A. farrani differs from the closely related A. andra sp. nov. (which also inhabits waters with normal oceanic salinity) and the brackish A. viriola sp. nov. by the presence of orange-yellow colouration on the tail in spotted forms (see Discussion), the absence of forms with black ground colouration and uniformly bright orange forms (Fig. 3 ). From the exclusively brackish-water species A. viriola sp. nov., A. farrani additionally differs by the absence of light pinkish subapical ceratal colouration. From A. linensis , A. farrani differs by the absence of a distinct dotted white line along the foot edge, orange-yellow and not reddish orange spots (in spotted forms), a smaller number of ceratal rows and the shape of the cerata. From A. pallida , A. farrani differs by the larger size of dorsal spots (in spotted forms), absence of small orange-brownish or brown spots on the cerata, and the smaller number of anterior ceratal rows. In A. farrani , the largest possible number of lateral denticles so far detected on the central teeth is up to seven, compared to up to five in A. andra sp. nov. and up to six in A. viriola sp. nov. The reproductive system of A. farrani differs from all Amphorina (including A. andra sp. nov.) species by the presence of an oval receptaculum seminis with a broad base but without a distinct stalk; from A. viriola sp. nov. and A. linensis by the shape of ampulla; from A. pallida by a considerably shorter prostate gland.

The species Amphorina alberti Quatrefages, 1844 was described the same year as A. farrani (Alder & Hancock, 1844) and morphologically they are essentially similar. Unfortunately, although the name A. alberti in some publications was referenced as a eubranchid (e.g., Bergh 1877; Iredale and O’Donoghue 1923) it was also incorrectly applied for several non-eubranchid Trinchesia species ( Trinchese 1877-1879; Bergh 1882). Eolis farrani was threated as a eubranchid, although its synonymy was partly cleared only after the mid-20th century (e.g., Edmunds and Kress 1969; Thompson and Brown 1984; compare with incorrect lumping synonymy of A. farrani in Iredale and O’Donoghue 1923). Therefore, in order to avoid confusion, the name A. alberti Quatrefages, 1844 was previously suppressed under plenary powers in favour of precedence of the name Eolis farrani Alder & Hancock, 1844 (ICZN 1966). At the same time, the genus name Amphorina , per se, in the original sense of Quatrefages (1844) was left as a potentially available genus name for the group of " Eubranchus farrani " (Heppel 1964), and that previous proposal corroborates well with the modern integrative data presented in this study.

Minimum uncorrected p-distances of the COI marker which separate A. farrani from A. viriola sp. nov., A. andra sp. nov., A. linensis , and A. pallida are 8.92 %, 9.59 %, 10.05 %, and 14.31 % respectively.

Figures

Figure 1. Phylogenetic relationships of nudibranchs Amphorina based on COI + 16 S + H 3 concatenated dataset inferred by Bayesian Inference (BI). The posterior probabilities from BI / bootstrap values for Maximum Likelihood (ML) are shown.

Figure 3. Periodic-like presentation of the colouration variation among all species of the genus Amphorina, representing vertical rows. Three main periods (horizontal rows), each with several subperiods, are recognised according to the principle of spotless body / colourless forms at the bottom to forms with the maximal number of spots / coloured body at the top. Note that different species display fundamentally similar colouration forms, but not all, so some morphs in particular species (e. g., forms with extensive surface pigmentation and dark body in A. farrani, A. linensis, and A. pallida) can either be eventually discovered or do not exist, by some further constraints of the developmental system. Non-observed forms for each particular species are indicated as " unkn " = " unknown ").

Figure 4. Amphorina farrani (Alder & Han cock, 1844) (a-c), A. linensis (Garcia-Gomez, Cervera & Garcia, 1990) (d, e) and A. pallida (Alder & Hancock, 1842) (f-g). (a) A. farrani GNM 9268, UK, a 1, head; a 2, cerata; a 3, tail; a 4, posterior part of radula (SEM, scale bar 20 μm); a 5, posterior part of radula (10 μm); a 6, anterior part of radula (10 μm); a 7, jaw (light microscopy); a 8, jaw (SEM, 100 μm); a 9, jaw details (20 μm); a 10, details of stylet (3 μm); a 11, stylet (30 μm). (b) A. farrani, image from original description of Eolis farrani in Alder, Hancock, 1844 (not in copyright currently), b 1, head; b 2, tail with orange-yellow colouration; b 3, cerata. (c) A. farrani, France, Mediterranean, (external data - ZMMU Op- 702), c 1, head; c 2, tail; c 3, cerata; (internal data - GNM 9278), c 4, posterior part of radula (50 μm); c 5, anterior part of radula (20 μm); c 6, anterior part of radula (20 μm); c 7, jaw (100 μm). (d) A. linensis GNM 9392, Sweden, d 1, head; d 2, tail and cerata. (e) A. linensis ZMMU Op- 707, Mediterranean, Croatia, e 1, head; e 2, tail and cerata; e 3, posterior part of radula (20 μm); e 4, anterior part of radula (20 μm); e 5, anterior part of radula (20 μm); e 6, jaw (light microscopy); e 7, jaw (SEM, 200 μm); e 8, jaw details (50 μm); e 9, stylet details (10 μm); e 10, stylet (100 μm). (f) A. pallida ZMMU Op- 710, Norway, f 1, head; f 2, tail and cerata; f 3, radula (100 μm); f 4, stylet (100 μm); (g) A. pallida ZMMU Op- 712, Norway, g 1, head; g 2, tail and cerata; g 3, posterior part of radula (100 μm); g 4, anterior part of radula (30 μm); g 5, jaw (light microscopy); g 6, jaw (SEM, 100 μm); g 7, jaw details (20 μm).

Figure 7. Reproductive systems, schemes. (A) Amphorina farrani. (B) Amphorina viriola sp. nov.; (C) Amphorina andra sp. nov. (D) Amphorina linensis. (E) Amphorina pallida. Abbreviations: am ampulla, fgm female gland mass, pg penial gland, pr prostate, psh penial sheath, rs receptaculum seminis.