Ziminella salmonacea ( Couthouy, 1838 )

Ziminella salmonacea ( Couthouy, 1838) View in CoL

( Figs 3 A–C View FIG , 4–6)

Eolis salmonacea Couthouy, 1838: 68–69 View in CoL , pl. 1, fig. 2.

Ziminella circapolaris Korshunova et al., 2017: 22-23 View in CoL View Cited Treatment , fig. 13 – syn. nov.

For a full list of synonyms see McDonald [2009].

Type material. For Z. salmonacea the type material is not known [ Martynov, 2006]. The type material for Z. circapolaris syn. nov. ( Holotype ZMMU Op- 598) is hosted at Zoological Museum of Lomonosov Moscow State University.

Material studied. Barents Sea, 70°58’N 37°07’E, 161– 170 m depth, coll. Knipowitsch N. 19.07.1899, ZIN24520 View Materials (4 spm). Barents Sea , Teriberskaya Guba , 110–146 m depth, coll. Knipowitsch N., 21.07.1894, ZIN24526 View Materials (1 spm). Barents Sea , Novaya Zemlya , Gorbovy Isl. , 11 m depth, coll. Ushakov P. V., Gorbunov, 04.09.1927, ZIN24527 View Materials (2 spm). Barents Sea, 69°34’30.0”N 32°00’31.0”E, 202 m depth, coll. Knipowitsch N., 13.07.1899, ZIN24528 View Materials (3 spm). Barents Sea, 74°08’N 20°00’E, 155 m depth, coll. Knipowitsch N., 16.04.1900, ZIN24529 View Materials (1 spm). Barents Sea, 74°08’N 20°00’E, 155 m depth, coll. Knipowitsch N., 16.04.1900, ZIN24530 View Materials (1 spm). Barents Sea, Novaya Zemlya, 72°29N 51°21’E, 73–74 m depth, coll. Knipowitsch N., 19.07.1901, ZIN24531 View Materials (2 spm). Barents Sea, 70°58’N 37°07’E, 161–170 m depth, coll. Knipowitsch N., 19.07.1899, ZIN24532 View Materials (1 spm). Barents Sea, Ura Bay , 69°23’00.0”N 32°55’00.0”E, 271 m depth, coll. Knipowitsch N., 26.05.1901, ZIN24533 View Materials (1 spm). Kara Sea, 80°1.5’N 73°20’E, 41 m depth, coll. Vagin, 18.08.1934, ZIN24535 View Materials (2 spm). Barents Sea, Kola Bay , 220 m depth, coll. Knipowitsch N., 11.06.1898, ZIN24537 View Materials (1 spm). Barents Sea, Ura Bay, 235 m depth, coll. Knipowitsch N., 17.06.1902, ZIN24540 View Materials (1 spm). Barents Sea, 69°18’14.8”N 33°41’57.4”E, 72 m depth, coll. Knipowitsch N., 28.06.1898, ZIN24545 View Materials (1 spm). Franz Josef Land, Heiss Is., 5–7 m in depth, coll. Pushkin, 01.02.1982, ZIN63736 View Materials (1 spm). NW Atlantic, off Newfoundland, 48°55.5’N 50°31.4’W, 230–237 m depth, coll. Nesis K.N., 14.07.1959, ZIN63739 View Materials (3 spm). Western Greenland, 69°55’1”N 51°16.2”W, 7 m depth, coll. Sirenko B.I., 21.07.1993, ZIN63740 View Materials (12 spm). Barents Sea, Novaya Zemlya, Gorbovy Isl., 11 m depth, coll. Ushakov P. V., 04.09.1927, ZIN63741 View Materials (3 spm). Franz Josef Land, Apollonov Is., 3–4 m depth, coll. Averintsev, 30.09.1992, ZIN63746 View Materials (1 spm) GoogleMaps .

Type locality. Charles River , Massachusetts, USA .

Description. External morphology (based on studied specimens): Body length up to 40 mm. Body wide. Foot wide, anterior corners short, rounded. Notal edge well-developed, continuous, forming short elevation above lateral body sides. Oral tentacles elongated, conical. Rhinophores smooth to rugose, longer and thinner than oral tentacles. Cerata in distinct rows, attached directly to well-defined notal edge. Cerata fusiform to cylindrical, lateral cerata much smaller than dorsal. Digestive gland diverticula filling more than half of ceratal volume. Anal opening on right side below notal edge, at beginning of posterior half of body. Reproductive opening on right side, on anterior part of body, surrounded by slightly folded region.

Coloration [after Kuzirian, 1977; 1979; Roginskaya, 1987]: Background body color milky-white. Oral tentacles and rhinophores beige to light orange with distal white stripe. Cerata orange-tan to deep red-brown, distal tip with white ring.

Internal morphology (based on studied specimens): Jaws oval-triangular with well-developed masticatory border bearing several rows of low blunt denticles or elevations. Radular formula: 19–32 × 1.1.1. Rachidian teeth massive, triangular. Central cusp strong, conical and elongated, non-compressed by adjacent denticles. From 4 to 11 small sharp and slightly curved denticles on each side of cusp, commonly from 6 to 9, denticles of about same size. Lateral teeth narrow, slightly curved blades with variable denticulation. From 0 to 29 denticles on inner side, locating at base, on first half or on entire length of tooth. Reproductive system diaulic. Ampulla long, narrow and convoluted. Vas deferens extremely long with slightly expanded prostatic part. Penis conical to slightly folded. Seminal receptacle absent.

Distribution. This species possesses a wide geographic and bathymetric distribution in the North Atlantic and adjacent Arctic waters. Based on Kuzirian [1979], Roginskaya [1987], Korshunova et al. [2017], and the material from BOLD and ZIN collections, the known range of Z. salmonacea includes Massachusetts, Maine, Bay of Fundy, New Brunswick, Newfoundland, Western Greenland, waters off Canadian Arctic Archipelago, Iceland, Northern Norway, Svalbard, Franz Josef Land and the Barents, the White and the Kara seas, on depths from 3 to 271 m.

Remarks. Our morphological and molecular data suggest that Z. salmonacea and Z. circapolaris should be considered a single species. Ziminella circapolaris was described based on specimens from the Franz Josef Land, as it “forms a separate sister clade to Z. salmonacea ” [ Korshunova et al., 2017: 22].According to Korshunova et al. [2017] these two species differ in the denticulation of the lateral teeth, as in Z. circapolaris the “denticulation runs up to very end of the lateral teeth, and the teeth are always denticulated”, while in Z. salmonacea the denticles are restricted to the first half of the laterals [ Korshunova et al., 2017: 23]. Finally, it was noted that the separate status of Z. circapolaris is “concordant with a considerable level of endemism of the nudibranch fauna of Franz Josef Land” [ Korshunova et al., 2017: 23]. Our data suggests that none of above-mentioned arguments could be used to delineate these species. First of all, the specimen from BOLD database (HLC-30139) collected from the Canadian Arctic, has the same haplotype as Z. circapolaris ( Fig. 2A View FIG ), rejecting the idea of endemic status for the latter. Although Z. salmonacea and Z. circapolaris (with an inclusion of HLC-30139) formed two distinct clades on the BI tree, the ML analysis did not separate them ( Fig. 2B View FIG , Fig. S1). The validity of Ziminella circapolaris was not supported by the species delimitation analysis (even if we consider HLC-30139 represents the same species), and this species also does not show any difference from Z. salmonacea in sequenced nuclear markers (H3). Finally, we have studied a large collection of Z. salmonacea deposited in ZIN, including the slides with isolated radulae ( Tables S1, S 4). Accordingly, the lateral teeth denticulation varies greatly in specimens collected across distant localities, in a single locality (including Franz Josef Land) or even at the same site ( Fig. 4, 5 View FIG ). In fact, several specimens from Franz Josef Land possess weakly denticulated ( Table S4, Figs 5 B, C View FIG ) or even almost smooth ( Table S4, Figs 5 D, G, H View FIG ) lateral teeth. At the same time, dense denticulation was observed in a specimen from Severnaya Zemlya Is. ( Table S4, Figs 5 J–L View FIG ). Specimens from the North-West Atlantic and western Arctic sectors also showed variability in denticulation ( Fig. 4, Table S4) and the same has already been reported for the specimens of Z. salmonacea collected close to the type locality [ Morse, 1971]. Moreover, in the SEM image of Z. salmonacea radula provided by Korshunova et al. [2017], the denticulation reaches the top of the lateral teeth [ Korshunova et al., 2017: fig. 15G]. Thus, we consider this variability to be intraspecific rather than interspecific. It was previously suggested that this variation could be ontogenetic, as Morse [1971] indicated that lateral teeth commonly have fewer denticles on the anterior part of the radular ribbon. In our material, this tendency is not traceable overall ( Table S4), although in some radulae the anterior radular portion may possess denser denticulation of the lateral teeth.

Ziminella salmonacea shows minor but consistent morphological differences with other species of the genus. From Z. abyssa it differs by consistently fewer number of denticles on the rachidian teeth (from 10 to 19 in Z. abyssa ), also in the latter species the lateral teeth never have well-developed denticles ( Fig. 7). In Ziminella japonica and Z. vrijenhoeki the lateral teeth have much wider base, with denticulation always occurring in the first half of its internal edge ( Fig. 9 View FIG ) [ Valdés et al., 2018]. Also, Z. japonica has different coloration with distinct orange to reddish dorsal surface and rhinophores ( Figs 3F, G View FIG ).