Amphorina pallida (Alder & Hancock, 1842)

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 pallida (Alder & Hancock, 1842) Figs 1 , 2 , 3 , 4f-g , 7e

Eolis pallida Alder & Hancock, 1842: 35-36.

Eolis minuta Alder & Hancock, 1842: 36.

Eolis picta Alder & Hancock, 1845: fam. 3, pl. 33.

Eolis flavescens Friele & Hansen, 1876: 78.

Eubranchus pallidus (Alder & Hancock, 1842): Edmunds and Kress 1969: 893-896, text figs 1, 3-6.

Amphorina pallida (Alder & Hancock, 1842): Martynov 1998: 775.

Material examined.

NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, town of Smögen, outermost skerries, Pesaskär (58°35'71"N, 11°18'81"E), 16-30 m depth, 14.04.2012, coll. Klas Malmberg (GNM Gastropoda - 8883, two specimens in same lot 10 and 7 mm in length, live, preserved length 7 and 5 mm, respectively). NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, town of Smögen, outermost skerries, Pesaskär (58°07'00"N, 10°83'33"E), 10-30 m depth, 01.05.2012, coll. Klas Malmberg (GNM Gastropoda - 8928, four specimens in same lot, 13, 10, 10, and 8 mm in length, respectively, live, preserved length 9,7,7 and 6 mm, respectively). NE Atlantic, Loch Fyne, Glas Eilean, Scotland, Great Britain (56°00'00"N, 05°22'00"W), 16 m depth, 25.01.2015, coll. Jim Anderson, one specimen (GNM Gastropoda -9094, preserved length 4 mm). NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, town of Smögen, outermost skerries (58°21'00"N, 11°12'00"E), 10-20 m depth, 01.05.2015, coll. Klas Malmberg, four specimens (GNM Gastropoda - 9218, 12 mm in length, live, preserved length 10 mm, GNM Gastropoda - 9219, 14 mm in length, live, preserved length 12 mm, GNM Gastropoda - 9249, 9 mm in length, live, preserved length 7 mm, GNM Gastropoda - 9250, preserved length 3.5 mm). NE Atlantic, Scotland, Loch Fyne, Glas, Eilean, (55°57'00"N, 05°23'00"W), 16 m depth, 25.01.2015, coll. Jim Anderson, one specimen (GNM Gastropoda - 9387, preserved length 10 mm). NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, Väderö Islands (58°34'00"N, 11°04'00"E), 20 m depth, 10.04.2015, coll. Klas Malmberg, five specimens (GNM Gastropoda - 9443, 10 mm in length, live, preserved length 8 mm, GNM Gastropoda - 9444, 9 mm in length, live, preserved length 7 mm, GNM Gastropoda - 9452, 9 mm in length, live, preserved length 6 mm, GNM Gastropoda - 9453, 7 mm in length, live, preserved length 6 mm, GNM Gastropoda - 9454, 11 mm in length, live, preserved length 9 mm). NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, Gullmar Fjord, Släggabåden between Släggö Island, Lysekil and Kristineberg marine station (58°15'70"N, 11°26'60"E), 50-55 m depth, soft clay bottom, 01.06.2017, coll. Kennet Lundin (GNM Gastropoda - 9501, 5 mm in length, live, preserved length 4 mm). NE Atlantic, Skagerrak, Sweden, Region Västra Götaland, Bohuslän county, Ide fjord, close to Svarte Jan lighthouse (59°07'00"N, 11°19'00"E), 20 m depth, 01.09.2015, coll. Klas Malmberg (GNM Gastropoda - 9695, 4 mm in length, live, preserved length 3 mm). NE Atlantic, Northern Ireland, Portaferry (54°23'00"N, 05°35'00"W), 10-20 m depth, soft clay bottom, 14.03.2015, coll. Bernard Picton (GNM Gastropoda - 9597, preserved length 5 mm). NE Atlantic, Northern Ireland, Portaferry (54°23'00"N, 05°35'00"W), 10-25 m depth, soft clay bottom, 10.03.2014, coll. Bernard Picton (GNM Gastropoda - 9601, preserved length 11 mm). NE Atlantic, Norway, Gulen Dive Center (60°57'27.11"N, 5°07'47.10"E), depth 15-20 m, stones, collectors T. A. Korshunova, A. V. Martynov, five specimens (ZMMU Op-708, 17.03.2014, ca. 20 mm in length, live, ca. 8 mm in length, preserved, ZMMU Op-709, 17.03.2014, ca. 15 mm in length, live, ca. 6 mm in length, preserved, ZMMU Op-710, 19.03.2015, 18 mm in length, live, 7 mm in length, preserved, ZMMU Op-711, 07.03.2016, 10 mm in length, live, ca. 5 mm in length, preserved, ZMMU Op-712, 12.5 mm in length, live, ca. 6 mm in length, preserved).

Diagnosis.

Body up to 25 mm; dorsal pigment spots (if present), small and often rounded, forming an almost continuous orange-brownish covering; in specimens with dorsal pigment spots there is never any colouration of the tail; completely pale specimens likewise lack tail spot; light pinkish subapical ring on cerata absent; absence of punctuated white line on external 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 18-41 × 1.1.1, copulative stylet long and bent at the top, seminal receptacle oval without stalk and widened base.

Description.

External morphology. The length of adult specimens may reach 25 mm. The body is narrow. The rhinophores are smooth and 1.5-2 times longer than the oral tentacles. The cerata are relatively long, very broad, with distinctly attenuated apices. Ceratal formula of the specimen ZMMU Op-708 from Norway: right (2, 4, 3, 5; anus, 5, 3, 3, 2, 2) left (1, 3, 3, 5; anus, 4, 4, 3, 2, 2). The foot is narrow, anteriorly without foot corners.

Colour. There are three main and eight subdivisions of colour variations (Fig. 3 ), from completely pale body and cerata without spots to specimens with many small rounded reddish orange/brownish pigment spots on the body and cerata. In specimens with distinct dorsal pigment spots, there is never any pigment on the tail. No specimens with blackish body pigmentation or uniformly bright orange colouration were ever observed. Absence of light pinkish subapical ring on cerata. Absence of line or row of dots of white pigment on external edge of foot. The upper part of the rhinophores are commonly covered with white relatively dense spots, or in some specimens with dense orange-reddish pigment, but without any formation of pigment rings. The oral tentacles are similarly coloured.

Anatomy. Digestive system (Fig. 4 , f3, g3-g7). The jaws are triangularly ovoid. The masticatory processes of the jaws bear a single row of ca. 25 distinct denticles. The radular formula in two studied specimens from Norway (Op-711, Op-712) is 18-31 × 1.1.1. The radular teeth are yellowish. The central tooth is narrow, with low cusp and four or five lateral denticles (three or less on anteriormost eroded teeth), including smaller intercalated denticles that may occur in different parts of the tooth.

Reproductive system. (Fig. 7E ). The ampulla is relatively small, not distinctly swollen (Fig. 7E , am). The prostate is distinct, extremely long and wide (Fig. 7E , pr). It transitions to a penial sheath, which contains a conical penis with a long chitinous stylet, bent in the middle (Fig. 4 , f4). A supplementary ( “penial”) gland is relatively long but thin and inserts into the base of the penis (Fig. 7E , pg). The seminal receptacle is oval (Fig. 7E , rs) without a stalk and widened base. The female gland mass includes mucous and capsular glands (Fig. 7E , fgm).

Distribution and habitats.

Western Mediterranean Sea and all European Atlantic coasts to northern Norway. At the Swedish west coast, living below the halocline.

Remarks.

Morphologically A. pallida differs from A. farrani , A. viriola sp. nov., A. andra sp. nov., and A. linensis by small rounded brownish orange pigment spots on the body (in spotted forms), by small brownish orange spots on the cerata, and by a very large S-shaped prostate.

Minimum uncorrected p-distances of the COI marker which separate the A. pallida from A. viriola sp. nov., A. andra sp. nov., A. linensis , and A. farrani 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 2. The haplotype network based on cytochrome c oxidase subunit I (COI) molecular data showing genetic mutations occurring within species of the genus Amphorina (A). Statistical test of the reliability of the bathymetric distribution patterns (and correlated with depths of brackish and marine environments) of A. viriola sp. nov. (red bar) and A. andra sp. nov. (blue bar) in Swedish waters (B). All specimens of A. viriola sp. nov. occur strictly in a very shallow brackish water layer above the halocline (salinity usually ca. 24 - 25 ‰), whereas in the same geographic region A. andra sp. nov. occur only below the halocline (at ca. 15 m depth) in waters with more stable oceanic salinity at 34 - 35 ‰.

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.