Dendronotus robilliardi, Korshunova, Tatiana, Sanamyan, Nadezhda, Zimina, Olga, Fletcher, Karin & Martynov, Alexander, 2016

Korshunova, Tatiana, Sanamyan, Nadezhda, Zimina, Olga, Fletcher, Karin & Martynov, Alexander, 2016, Two new species and a remarkable record of the genus Dendronotus from the North Pacific and Arctic oceans (Nudibranchia), ZooKeys 630, pp. 19-42 : 23-27

Taxon classification Animalia Nudibranchia Dendronotidae

Dendronotus robilliardi sp. n. Figs 2, 3B

Dendronotus albus : Robilliard 1970: 466-470, pl. 64, fig 34, text figs 2-4, 6, 22-24 (excluding part of Geographical section, p. 469-Baja California); Morris et al. 1980: 332-333, part; McDonald 1983: 172, part; Koh 2006: locality information and photo; Lloyd 2007: locality information and photo; Martynov et al. 2015b: 74-75 pp, figs 2 в, г; Ekimova et al. prepublication: 2-10, figs 2 D–F, 3 D–G, 4A (non albus MacFarland, 1966).

Type material.

Holotype, ZMMU Op-568, 35 mm long (live), NW Pacific, Kamchatka, Starichkov Island, 52°47.009' N– 158°36.185'E, 17.09.2015, depth 11.5 m, stones, SCUBA diving, collector N.P. Sanamyan. 1 paratype, ZMMU Op-567, same locality and collectors as holotype. 1 paratype, ZMMU Op-447, same locality and collectors as holotype. 1 paratype (egg mass only), ZMMU Op-570, same locality and collectors. 1 paratype, ZMMU Op-569, NW Pacific, Kamchatka, Zhirovaya Bay, 52°36.767' N– 158°27.318'E, 12.06.2016, depth 18 m, stones, SCUBA diving, collector N.P. Sanamyan.

Type locality.

The NW Pacific, Kamchatka, Russia.

Etymology.

In honour of Gordon Robilliard (Gig Harbor, Washington State, USA), the author of the classic study on the genus Dendronotus , including the description of Dendronotus diversicolor Robilliard, 1970. For a long time Robilliard attempted to resolve status of Dendronotus diversicolor ( Behrens 2006); Dendronotus diversicolor was finally synonymised with Dendronotus albus based on molecular data forty years later by Stout et al. (2010) (see also Discussion below). Here molecular evidence is provided showing the existence of another species in the NW Pacific belonging to the Dendronotus albus complex; therefore, this is a good opportunity to honour the important contributions of Gordon Robilliard to the systematics of the genus Dendronotus , and particularly to the Dendronotus albus species complex problem.

Diagnosis.

5-6 pairs branched dorsolateral appendages, digestive gland penetrates 3-4 pairs of dorsolateral appendages, general colour translucent white, dorsolateral appendages colour variable, orange-copper pigment present or completely lacking, tips opaque white, opaque white stripes on tips of dorsal appendages and tail, central tooth with up to 15 small distinct denticles without furrows, vas deferens short, conical penis.

Description.

Body elongate, 30-35 mm in length (Fig. 2 A–D). 4-5 branched appendages of oral veil, 4-6 appendages of rhinophoral stalks, 11-12 rhinophoral lamellae, unbranched (or with few small branches) rhinophoral lateral papilla present, 5-6 pairs larger branched dorsolateral appendages and 1-3 pairs smaller unbranched appendages reaching tip of tail, 5-10 lip papillae. Dorsolateral appendages with moderate primary stalk and secondary branches, and pointed tertiary branches, digestive gland penetrates 3-4 pairs of dorsolateral appendages including posterior ones (Fig. 2 A–D). Reproductive and anal openings placed laterally on right side.

General colour translucent white with opaque white stripes on oral veil appendages, rhinophoral sheaths, posterior part of dorsum and on tips of dorsal appendages; orange-copper marks in middle part of dorsal and oral processes (Fig. 2 A–C), or absent (Fig. 2D).

Dorsal processes of jaws inclined posteriorly at approximately 60° to longitudinal axis of jaw body and 0.45 of its length (Fig. 2 F–G). Masticatory borders with ridge-like denticles. Radula formula 43 × 3 –9.1.9– 3. Central tooth with up to 15 small distinct denticles (Fig. 2I, J), without furrows. Lateral teeth slightly curved, bearing up to seven distinct long denticles (Fig. 2K).

Reproductive system triaulic (Fig. 3B). Ampulla wide, folded twice. Prostate moderate in size, consists of ca. 19-20 alveolar glands. Vas deferens short, relatively narrow, penial sheath elongate, relatively long, curved, conical penis (Fig. 2H). Vagina narrow, bent, moderate in length, distally expanded into vestibulum. Uterine (insemination) duct short. Bursa copulatrix large, irregularly spherical, stalked, small oval seminal receptaculum placed distally on vestibulum (Fig. 3B).

Biology.

Inhabits stones and rocky bottom. Feeds on the hydroid Abietinaria annulata (Kirchenpauer, 1884).

Distribution.

The type specimens of Dendronotus robilliardi sp. n. originate from the NW Pacific, Kamchatka, Russia. According to the ceratal pattern, a specimen of Dendronotus albus recorded from cold waters of South Korea, 37°7'N, 129°E ( Koh 2006) is also likely to be Dendronotus robilliardi sp. n.; therefore, a very broad distribution of Dendronotus robilliardi sp. n. is expected in the NW Pacific, from the Commander Islands in the north to Korea in the south. According to the morphological data given in Robilliard (1970) and a detailed image by Lloyd (2007) clearly showing up to six pairs of dorsolateral appendages (three of them contain digestive gland branches), the range of Dendronotus robilliardi sp. n. in NE Pacific reaches at least British Columbia and Washington State (San Juan Island). Robilliard and Barr (1974) also presented a record of Dendronotus albus from Alaska without an image. Since Robilliard consistently misidentified Dendronotus albus in his revision (1970) (see Discussion and Table 2), most probably the Alaskan record also belongs to the species Dendronotus robilliardi sp. n. However, the majority of the records Dendronotus albus from California and especially from Baja California ( Robilliard 1970; Behrens 1980, 1991) probably represent true Dendronotus albus . The specimens of Dendronotus albus (= Dendronotus robilliardi sp. n.) which were studied by Robilliard (1970) originated from San Juan Island, Washington State and Albert Head, British Columbia, whereas more southern records were listed according to the information from James Lance only ( Robilliard 1970: 469; Bertsch et al. 1972: 305). A selection of detailed images of several specimens of Dendronotus albus from the type locality of this species, Monterey Bay, California ( McDonald 2016) showing only specimens with four to five pairs (the fifth pair if present is smaller) of dorsolateral appendages is in a full agreement with the first description of true Dendronotus albus (MacFarland, 1966). Sandra Millen (pers. comm.) has distinguished Dendronotus albus sensu Robilliard, 1970 from Dendronotus diversicolor (a synonym of Dendronotus albus , see Table 2) in the British Columbia region. Dendronotus diversicolor was also recorded without an illustration from British Columbia by Lambert (1976). A record of Dendronotus diversicolor by Millen (1989) from Alaska represents the northernmost range of true Dendronotus albus since that specimen had four ceratal pairs plus a small bump, and digestive gland extending in to the two anterior pairs (S. Millen, pers. comm.).

Both Dendronotus robilliardi sp. n. and true Dendronotus albus evidently may co-occur in some localities around at least the British Columbia/Washington waters. Dendronotus albus was recently recorded and illustrated from the Salish Sea (Washington) by Fletcher (2013), geographically thus very close to San Juan Island, the type locality of Dendronotus diversicolor , and from where also Dendronotus " albus " (= Dendronotus robilliardi sp. n.) was already reported by Robilliard (1970). Thus Dendronotus robilliardi sp. n. appears to be a boreal species widely distributed in the northern Pacific and adapted for lower temperatures compared to Dendronotus albus . The latter species is mostly likely distributed in the NE Pacific from British Columbia southwards potentially to Baja California, in warmer temperature conditions.

Remarks.

There is a significant genetic gap between Dendronotus robilliardi sp. n. and the morphologically similar Dendronotus albus (13.6-14.5% for COI gene, 2.3-2.5% for 16S gene) (Fig. 5). According to Carmona et al. (2013) such values can be considered as species- and genus- ‘level’ differences in the nudibranch molluscs. Dendronotus robilliardi sp. n. is also distinguished morphologically from the true Dendronotus albus MacFarland, 1966. Dendronotus albus (including its synonym Dendronotus diversicolor ) has only 4-5 pairs of dorsolateral appendages and the digestive gland penetrates only the two anteriormost pairs of the dorsolateral appendages (see also Discussion). Dendronotus robilliardi sp. n. has 5-9 pairs of dorsolateral appendages and the digestive gland penetrates at least 3-4 pairs of the dorsolateral appendages. In his redescription of Dendronotus albus Robilliard (1970) misidentified this species, as did Ekimova et al. (prepublication): Dendronotus albus sensu Robilliard (1970) shares a larger number of pairs of dorsolateral appendages with Dendronotus robilliardi sp. n. and not with Dendronotus albus (= Dendronotus diversicolor ) and can be referred to this new species. Table 2 outlines the differences between these two species.

Dendronotus robilliardi sp. n. differs both morphologically and according to the genetic distances from its sympatric species Dendronotus dalli (range 12.0-14.0% for COI, and 2.7-3.2 % for 16S), Dendronotus kalikal (range 10.8-12.1% for COI, and 3.2 - 3.4% for 16S), and Dendronotus kamchaticus (range 12.5-13.7% for COI, and 2.8-3.2% for 16S). Another NW Pacific species, Dendronotus primorjensis , also differs from Dendronotus robilliardi sp. n. by external morphology, radular and reproductive features, and by p-distances (range 12.2-13.6% for COI, and 3.2-3.7% for 16S). Minimum interspecific distances of the COI marker separate Dendronotus robilliardi sp. n. from other species with high genetic divergences: 13.0% from Dendronotus dalli , 11.5% from Dendronotus kalikal , 12.9% from Dendronotus kamchaticus , and 12.8% from Dendronotus primorjensis .