Sea stars of the genus Henricia Gray, 1840 (Echinodermata, Asteroidea) from Vostok Bay, Sea of Japan

Molecular analysis

We used 16S sequences from this study, or added from GenBank, were partial 16S rRNA nucleotide sequences ranging from 541–606 bp long. We produced an alignment of 632 bp including gaps; 162 sites within the ingroup were variable, and 129 of these were parsimony-informative. Neighbor-Joining tree (Fig. 2) shows well supported clusters for all were partial 16S rRNA nucleotide sequences ranging from 541–606 bp long. We produced an alignment of 632 bp. Uncorrected interspecific distances ranged from 5% (H. lineata –H. uluudax) to 11.5% (H. ohshimai –H. compacta).

Subgenus Henricia Gray, 1840

Type species: Asterias oculata Pennant, 1777

1. Henricia (H.) alexeyi Chichvarkhin & Chichvarkhina, 2017a; Chichvarkhin & Chichvarkhina, 2017b (Fig. 3)

Type locality: Rudnaya Bay, Sea of Japan, Russia.

Examined material: holotype: MIMB–33243, Senkina Shapka pinnacle, Rudnaya Bay, 10–15 m depth, 8 October 2015, leg. A. Chichvarkhin. Paratypes: MIMB–33244, 1 spm, Senkina Shapka pinnacle, Rudnaya Bay, 10–15 m depth, 8 October 2015, leg. A. Chichvarkhin; MIMB- 34803, 1 spm, Vostok Bay, 07 Jul 2017, leg. K. Dudka; MIMB–33241, 1 spm, Vostok Bay, Sea of Japan, Russia, Aug 2015, leg. K. Dudka; MIMB–33242, 1 spm, Vtoraya Priboika Inlet, Vostok Bay, Sea of Japan, Russia, 2 m depth, 25 Aug 2016, leg. I. Ekimova. ZIHU–2405, 3 syntypes of H. ohshimai (Hayashi, 1940), Onagawa shore, 1934.

External anatomy. Small size sea stars, R (long radius, mouth to ray tip) = 19–47 mm, r (short radius, mouth to interradius) = 4–9 mm, mean R: r = 4.7 (R:r of holotype 4.56, R = 20.5, r = 4.5). Rays five, cylindrical, slim, not swollen at base (Fig. 3). Abactinal skeleton open meshed. Abactinal plates oval, rod-shaped with low ridges or tubercles. Papular areas with 1–3 papulae. Abactinal pseudopaxillae (Fig. 3B) with 6–10 spines in two rows covered by thin skin. Abactinal spines short, stout, 300 µm long, 80–100 µm wide, most tapering distally (Fig. 3), bear 1–6 short thick subapical thorns faced upwards.

Superomarginal row well discernible consisting of plates larger than abactinal, with rather high ridges (Figs. 3A, 3C), consists of longitudinally elongated plates. Intermarginal row extended to 2/3 of ray length, second intermarginal row short, consists of eight plates. Intermarginal plates small, round. Inferomarginals plates triangular or sub-quadrate. Superomarginals bear 7–9 spines in two rows. Intermarginal pseudopaxillae with 4–6 spines in two rows. Inferomarginal pseudopaxillae bear 10–12 spines in 2 transversal rows.

Ventrolateral row consists of densely set oval plates. Second ventrolateral row extends to a half of ray length, consists of tiny round plates. Ventrolateral pseudopaxillae bear 3–5 spines in one row. Adambulacrals with 3–4 larger near-furrow spines and three small spines in one irregular row (Fig. 3C, 3D) joined by skin membrane as a crest. Proximally, adambulacral, ventrolateral and inferomarginal spines arranged in crests with skin membrane (Fig. 3D). Deep furrow spine small, single. Oral plates each bear single apical, three marginal, and two suboral spines.

Color in life varies greatly from red to orange. Some specimens with broad darker areas on rays or almost white on disc and proximally on rays (Fig. 3). Anal area darker or same color as background; madreporite lighter or same color as background. Actinal side uniformly orange.

Ecology: inhabits open bays exposed to wave activity at 2–15 m depths. In Rudnaya Bay, specimens were found on sponges apparently damaged by these sea stars (Fig. 3F).

2. Henricia (H.) pacifica Hayashi, 1940 (Fig. 4)

Henricia sanguinolenta—Yavnov, 2010: 125–126 (non Müller, 1776).

Type locality: Tsugaru Strait, Japan.

Examined material: MIMB–33245, (R = 46 mm) Vostok Bay, 10–15 m depth, Aug 2015, leg. I. Krasilnikov. 3 spms, MIMB–33246–33248, (R = 38, 48, 51 mm), Vostok Bay, 10–15 m depth, Aug 2015, leg. I. Krasilnikov; ZIHU–2404, H. pacifica holotype, Tsugaru Strait, Japan.

External anatomy. Medium size sea stars, mean R: r = 4.1 (R:r of holotype 4.2); R = 48–53 mm, r = 11–14 mm, R of holotype 50 mm, r = 12 mm. Rays five, slender, slim, cylindrical (Figs. 4A–4D). Abactinal skeleton open meshed. Abactinal plates oval, rod-shaped with well discernible smooth ridges (Fig. 4G). Abactinal spines set along ridges in groups of 4–10 spines in one row covered by skin membrane, so in dried specimens the spines become poorly distinguishable. Papular areas with 1–3 papulae. Abactinal spines long, tapering, 400 µm long, 100 wide at base, tapering to 30–50 µm distally (Figs. 4H–4K), bear 9–11 tiny thorns on apex and spine shaft and faced upwards or at angle to spine axis.

Superomarginal row discernible consisting of cross-shaped plates similar in size to neighboring plates with no ridges (Figs. 4E–4F). Intermarginal row extended to 2/3 of ray length. Intermarginal plates rod- and crescent-shaped. Inferomarginals plates sub-quadrate. Superomarginals bear 4–5 spines in one row. Intermarginal pseudopaxillae with 4–5 spines in two rows. Inferomarginal pseudopaxillae bear five spines in one transversal rows.

Ventrolateral plates sub-quadrate, smaller than inferomarginals. Pseudopaxillae bear 4–5 spines in one row. Adambulacrals with three larger thick near-furrow spines and four smaller spines in one row. Deep furrow spine thick, single. Oral plates each bear single apical, three large marginal, and three suboral spines.

Color, in life, bloody-red with light whitish tint proximally on rays and on disc, also on ray tips in some specimens (Figs. 4A–4D). Anal area not discernible from background; madreporite yellow. Actinal side uniformly orange.

Ecology: inhabits open bays exposed to wave activity at 15 m depths.

3. Henricia (H.) nipponica Uchida, 1928 (Fig. 5)

Henricia pachyderma, Chichvarkhin & Chichvarkhina, 2017a: fig 4I; Chichvarkhin & Chichvarkhina, 2017b: 27, fig. E. (non Hayashi, 1940)

Type locality: Japan.

Examined material: 6 spms, MIMB–33252–33257, Vostok Bay, July 2015, leg. I. Krasilnikov; 1 spm, MIMB–33814, 4 Oct 2015, A. Chichvarkhin; 5 spms, Vostok Bay, 27 Aug 2016, leg. A. Goloseyev; 1 spm, Vostok Bay, 10 Jul 2017, leg. K. Dudka; 4 spms, Rudnaya Bay, 10 Oct 2015, leg. A. Chichvarkhin; 1 spm Sagami Bay, Misaki Marine Biological Station, Kanagawa, Japan, 3 Jun 2018, leg. A. Chichvarkhin.

External anatomy. R: r = 4.4–5.7, R = 35–50 mm. Rays five, abnormally six, cylindrical (Fig. 5A). Aboral skeleton wide meshed. Most abactinal plates rod-shaped, some branched with well discernible tubercle. Secondary plates of irregular shape in some meshes (Figs. 5B, 5D). Abactinal pseudopaxillae with 4–8 spines in one row. Papular areas with 1–3 papulae (most often three); papulae in live individuals large, 4–5 fold longer than wide (Fig. 5E). Abactinal spines long, 400 µm long, 60–100 µm wide at base, gradually tapering proximally (Figs. 5F–5I), with 8–12 tiny apical and subapical thorns, covered by skin membrane.

Superomarginal row poorly discernible, consists of plates similar to adjacent aborals, bearing 3–5 spines, same as abactinal spines, arranged in one row. Intermarginal row extended to a half of ray length; plates with 4–5 spines in one row. Plates of intermarginal and adjacent marginal rows connected by additional transversal plates. Inferomarginal plates large, transversally elongated, pseudopaxillae bear 8–10 spines in one transversal row.

Ventrolateral plates pillow-shaped, with proximal outgrowth overlaying next proximal plate; pseudopaxillae bear 4–7 spines in one transversal row. Second ventrolateral row consists of smaller round plates bearing 2–3 spines; this row extends to a half of ray length. Adambulacrals with 3–4 larger near-furrow spines and 6–8 smaller spines in two irregular rows (Fig. 5C). Deep furrow spine small, single. Oral plates not fused, each bear single apical, four marginal, and four suboral blunt spines.

Color in life. Abactinal side dirty-orange to brown, actinal side orange, lighter than abactinal side (Fig. 5A). Anal area darker than background; madreporite light creamy.

Ecology: The species was found on rocky substrates at the depths of 1–20 m at water temperature of 2–22° C .

Distribution. Abundant in the northern part of Japan (Hayashi, 1940). Reported here from Russian waters for the first time.

4. Henricia (H.) oculata robusta Djakonov, 1958

Type locality: southern Kurile Islands, Pacific shore.

Examined material: 1 spm (H. oculata neotype) NHMD-71387 (AMUC-AST-223), Treaddur Bay, Ravensport, 15 May 1968, leg. B. Brunn; 2 spms, NHMD-204701, Bay Fire, Isle of Man, Irish Sea, 24 Apr 1968, leg. B. Brunn; 2 spms, NHMD-76378 (ZMUC-AST-214), Plymouth, ca. 50 m, Engelska Kanal, Sep 1931, leg. Th. Horbensen; 1 spm (NHMD), Foró, >1,867 m, 8 Apr 1984, leg. Rostrup; ZIN–15/15340, 2 spms, Korea-Sakhalin Expedition st. 2, 1 Mar 1900, Peter the Great Bay, Bosphorus Eastern Str., 18 m, silt; ZIN–8/15043, 1 spm, Rossinant st. 1555, 3 Sep 1930, 83–86 m, Vladimir Bay, leg. Derjavin; ZIN–26/15052, 2 spms, Toporok st. 2, 16 Aug 1948, Musasi Bank, Sea of Japan, 93–96 m, leg. Ushakov; ZIN–10/15156, 2 spms, Nagasaki, 1901, leg. P.Yu. Schmidt; ZIN–18/15343, 2 spms, Nagasaki Apr 3, 1897, D-r Bunge; ZIN–17/15342, 2 spms, Nagasaki, Dec 12–14 1897, D-r Bunge; ZIN–16/15341, 1 spm, 23 Jul 1898, Nagasaki, D-r Bunge; ZIN–14/15339, 1 spm, 10–-15 Dec 1897, Nagasaki, D-r Bunge.

Diagnosis. Aboral pseudopaxillae comprised of up to 10–20 spines in double row. Spines covered with thick skin membrane. Spines stout, crowned with 15–20 tiny thorns, lateral ribs poorly developed. Abactinal plates arched, suboval, with no ribs, arranged in relatively wide mesh with 1–3 papulae a mesh. Superomarginals larger than aboral plates, T-shaped, with central proximal outgrowth. Inferomarginals large, cross-shaped, elongated transversally. Adambulacral spines 5–6, largest one near furrow spatulate or slightly flattened.

External anatomy: R:r 3.7–4.1 R 45–57 mm, r 11–15 mm. The rays slender not very slim, slightly swollen at base. Whole body covered by thick skin membrane, which looks rather thin in dried specimens. Abactinal plates suboval, rod-shaped, arched, cover adjacent proximal plates (Fig. 1A). Abactinal pseudopaxillae (Fig. 1B) crowned with 10–20 spines arranged in two rows. Papular areas nearly same width/length as average abactinal pseudopaxilla, includes one to three papulae. Abactinal spines covered with thin skin membrane, vary in length, stout, 350–400 µm long, 100 µm wide at base; apex with 15–20 short thorns, lateral ribs poorly developed (Fig. 2); in some individuals, spines short and widened distally, in the others, spines slender and tapering at distal end (Figs. 2A–2C).

Superomarginal row bent dorsally at ray base (Fig. 1C), consists of T-shaped plates with central dorsal outgrowth overlapping adjacent abactinal plates; bear 8–10 spines arranged in 2 rows. In large specimen, two complete or qincomplete intermarginal rows consisting of rod-shaped plates that connected to adjacent marginal rows with similar rod-shaped transversal plates crowned with 6–8 spines in two rows; one of intermarginal row extended to or beyond half ray. In this way, supero- and inferomarginal rows in some specimens (e.g., MIMB-33214, Fig. 1C) are widely separated with two intermarginal rows and two series of additional transversal plates. But in most specimens (Fig. 3D) intermarginal rows and connecting plates are less developed. Inferomarginal row extended over entire ray length, its pseudopaxillae bear 14–20 spines in two transversal rows. Ventrolateral quadratic plates bear 10–13 relatively small spines in 2–3 rows. Second ventrolateral row consists of about 18 transversally elongated rod-shaped plates with low tubercle. Arched adambulacrals with slightly curved small furrow spine, one large slightly flattened to spatulate spine (Figs. 1C, 1D) faced into furrow (but in some individuals, more than one spine is spatulate, Fig. 3F); the other 3–5 gradually smaller spines faced ventrally in one staggered row bearing numerous thorns on apices. Spatulate shape varies because it is constituted by soft tissue, not spine itself. Oral plates not fused, bear 4 marginal and 1–4 suboral spines.

Life coloration varies. Rays orange-red, pink, yellow, some individuals with purple to violet stripes (Figs. 2E, 2F). Madreporite slightly lighter than background.

Ecology. Living sea stars were found off Mednyi Island on rock at depths 5–10 m at water temperature of 4 °C. Probably, they fed on yellow colored sponge, which was detected nearby (Figs. 2E, 2F). In other areas, found at depths >100 m feeding on sponges, detritus, hydrozoans, and bryozoans (Jewett et al., 2015); brooding (Jewett et al., 2015).

Distribution. Amphiboreal species. NE Atlantic: British Islands, Irish Sea, English Channel, North Sea, Faroe Islands, France, Portugal, NW Atlantic: New Brunswick, northern Pacific: British Columbia, Alaska, Aleutian Islands, Commander Islands, Kurile Islands, Sea of Okhotsk, Sea of Japan, Pacific shore of Japan (Hayashi, 1940; Djakonov, 1961; Madsen, 1987; Clark & Jewett, 2010; Jewett et al., 2015). Unknown from Japan: the only specimen found in R. Hayashi’s collection preserved in Hokkaido University belongs to H. aspera Fisher, 1906.

Subgenus Aleutihenricia (Clark & Jewett, 2010)

Type species Henricia rudis Verrill, 1911 (= H. derjugini (Djakonov, 1950)

5. Henricia (A.) granulifera Djakonov, 1958 (Fig. 6; Supplemental Information 1, second sea star, 5–9th seconds)

We identified the specimen in ZIN collection (Fig. 6) identified as H. granulifera and labeled as the ‘holotype’ by Z.I. Baranova. We are designating this specimen as lectotype of Henricia granulifera (Djakonov, 1958). R = 80 mm, r = 19 mm; ZIN–4/14824 transect off Moibesi [Belinskoye, W Sakhalin, Sea of Japan], 30–37 m, 30 Aug 1949.

Henricia granulifera Djakonov, 1958: 311–312, figs. 21, 22; Djakonov, 1961: 27, Pl. 2, fig. 20, Pl. 17, figs. 68, 69; (Yavnov, 2010): 121–122; (Chichvarkhin & Chichvarkhina, 2017a): fig 4K; Chichvarkhin & Chichvarkhina, 2017b: 27, fig. F.

Type locality: Sea of Japan, Tatar Strait near Belinskoye, Sakhalin.

Examined material: 1 spm, MIMB–33251, Vostok Bay, July 2015, leg. I. Krasilnikov; 1 spm. Vostok Bay, 13 July 2017, leg. K. Dudka; 1 spm, ZIN–4/14824 (lectotype of H. granulifera) transect off Moibesi [Belinskoye, W Sakhalin, Sea of Japan], 30–37 m, 30 Aug 1949, Toporok stations #65–66; ZIHU–2411 (holotype of H. reticulata), Onagawa Iigohama, Japan; ZIHU– 2412 (holotype of H. irregularis), Yezo Strait, Albatross 1906 station #5031, 86 fathoms depth, Japan.

External anatomy. Relatively large sea star, R 72 mm, r = 9, R: r = 8. Rays five, abnormally four, cylindrical. Disc small, aboral skeleton wide meshed. Abactinal plates rod-shaped, with 1–2 well discernible tubercles on each, form wide mesh. Small secondary plates of irregular shape in some meshes. Abactinal pseudopaxillae in groups of 3–5 spines in paxilla. Papular areas with 2–4 papulae. Abactinal spines long, 550 µm long, 100 µm wide at base, gradually tapering proximally (Figs. 6H–6P), with about 15 tiny and subapical thorns, some thorns located laterally on spine shaft; lateral thorns faced at an angle to spine shaft; spines not covered by skin membrane.

Marginal rows poorly discernible, consists of similar plates, bearing 3–5 spines; plates with well discernible tubercles. Superomarginal plates higher than adjacent plates, form more discernible bent row. Intermarginal row extended to full ray length. Inferomarginal plates large but not as high as superomarginals.

Ventrolateral plates small, round, with tubercle; bear 5–6 spines in a circle. Adambulacrals with 2–3 larger near-furrow spines and 5–6 smaller spines in two rows (Figs. 6C–6D). Deep furrow spine small, single. Oral plates not fused, each bear single apical, four marginal, and three suboral blunt spines.

Color in life. Abactinal side brown with spine apices orange (Fig. 6A); marginal rows brown as aboral side; ventrolateral, adambulacral, oral and furrow areas orange (Fig. 6B). Anal area small and lighter than background; madreporite bright orange.

Ecology. A single specimen of this species was found on rocky substrate at the depth of 15 m at water temperature of 16 °C.

Distribution. Known for the northwestern part of the Sea of Japan (Chichvarkhin & Chhichvarkhina, 2017), Korea (Shin & Rho, 1996) and Japan (Hayashi, 1940).

Subgenus Setihenricia Chichvarkhin & Chichvarkhina, 2017

Type species Henricia hayashii Djakonov, 1961

6. Henricia (S.) djakonovi Chichvarkhin, 2017 (Fig. 7)

Type locality: Rudnaya Bay, Sea of Japan, Russia

We identified H. pseudoleviuscula specimen in ZIN collection labeled as the “holotype” presumably by Z.I. Baranova. We are designating this specimen as lectotype of Henricia pseudoleviuscula (Djakonov, 1958). R = 41 mm, r = 8 mm; ZIN–1/12815, Toporok station 31, Moneron Is., 14 Aug 1947, 84 m depth.

Examined material: MIMB–331294 4 Jun 2016, Senkina Shapka pinnacle, Rudnaya Bay, 44.36°N 135.83°E, 16 m, leg. A. Chichvarkhin (holotype); MIMB–331304 4 Jun 2016, Senkina Shapka pinnacle, Rudnaya Bay, 44.36°N 135.83°E, 16 m, leg. A. Chichvarkhin (paratype); 11spms, MIMB–33128, MIMB–33131, 23–25 Aug 2015, Vostok Bay, leg. I. Krasilnikov; 1 spm, MIMB–, Vostok Bay, 10 Jul 2017, leg. K. Dudka; ZIN–1/12815, Toporok station 31, Moneron Is., 14 Aug 1947, 84 m depth (lectotype of H. pseudoleviuscula); 2 spms, ZIHU–2397, Bomasiri Shima [N. off Rebun Is., Japan], 1906 (H. reniossa holotype and paratype).

Chichvarkhin & Chichvarkhina (2017a) and Chichvarkhin & Chichvarkhina (2017b) described this species as one of two ‘tiger-striped’ sympatric morphs that co-occur in the northwestern Sea of Japan, while the other form was incorrectly referred to as H. pseudoleviuscula. This study found that both morphotypes had identical sequences, so they more likely represent discontinuous phenotypes of the same species (Fig. 2); both forms cannot be referred as H. pseudoleviuscula (Djakonov, 1961) because the lectotype of the latter possesses very different spines (Figs. 7K, 7L), similar to those of H. reniossa Hayashi, 1941 (Fig. 7M). Thus, our amended description of H. djakonovi here is expanded to include H. pseudoleviuscula sensu (Chichvarkhin, 2017a).

External anatomy. R of holotype = 52 mm, r = 11 mm, R: r = 4.7–5; R = 38. To avoid a future confusion, here we are re-describing H. djakonovi by combining the characters of both forms (i.e., djakonovi and pseudoleviuscula sensu Chichvarkhin, 2017a. mm, r = 7.5 mm in paratype. Rays slender not very slim, slightly swollen at base, tapering to blunt tips. Most abactinal plates (>50%) cross-shaped with two proximal outgrowths covering adjacent plates, their elevated proximal sides form crescent-shaped pseudopaxillae. The other plates triangular or irregular shaped, lacking proximal outgrowths, form round and oval pseudopaxillae. Plates convex without ridges or tubercles. Abactinal surface (Figs. 7A, 7C, 7D) thick, rigid; abactinal plates on disc close-set forming tight reticulation. Abactinal pseudopaxillae bear 20–30 spines, but some smaller pseudopaxillae bear 8–10 spines. Papular areas nearly twice smaller than average abactinal pseudopaxillae, include one or two papulae. Abactinal spines short, stout, 200–240 µm long, 60–100 µm wide, barrel-shaped (Figs. 7F–7J). Apex of most spines massive with few short thorns; apex in some specimens smooth, resembles glass droplet (Fig. 7J).

Superomarginal row bent dorsally at ray base, consists of square pillow-shaped plates. Inferomarginals and ventrolaterals are similarly pillow-shaped. Intermarginal rows consisting of usually one, but up to six, irregular shaped plates, constituting a proximal intermarginal area that provides an inflation of ray base. Superomarginals bear 20–35 spines, same as abactinal spines, arranged in four rows. Inferomarginal row extended over entire ray length (Fig. 7B), its pseudopaxillae bear 30–45 spines in 4–6 transversal rows.

Ventrolateral pseudopaxillae bear 25–30 thorny spines in 4–5 rows. Adambulacrals with 10–11 spines in two transversal rows bearing numerous small thorns on apices; 3–4 larger adambulacrals near furrow spines; size of the other spines facing ventrally gradually decreases outwards from the furrow (Fig. 7E). Deep furrow spine small, single. Oral plates not fused, each bear single apical, four marginal, and four suboral blunt spines.

Color in life. Rays brownish-orange, abactinal side of the disc dark (Fig. 7C). Anal area almost black; madreporite partially creamy, partially brownish. In ethanol-preserved specimens, the madreporite is the same color as abactinal side of disc. Abactinal side of rays marked with dark brown to black spots of irregular shape, some of them look like broad transversal lines. Actinal side is uniformly colored orange-red, same as abactinal background color of rays.

Ecology. The species was found on rocky substrates at the depths of 1–20 m at water temperature 2–22 °C. In aquarium conditions, some were (one was?) kept over 10 months in an aquarium without any macroscopic food supply, which could indicate that they survived by grazing microscopic food, such as encrusting protists or diatoms.

Distribution. Known for the northwestern part of the Sea of Japan from Peter the Great Bay to Oprichnik Bay. Also, reported from Yellow Sea as H. l. leviuscula (Xiao, Liao & Liu, 2011). A species, H. pseudoleviuscula Djakonov, 1958, with similar skeleton pattern lacking the ridges on the plates had been described from Moneron Island in the northwestern Sea of Japan. Life color of this species remains unknown but aboral spines in H. pseudoleviuscula is similar to the spines of type specimens of H. reniossa Hayashi, 1940, that are rather different from H. djakonovi (Figs. 7K–7M).

7. Henricia (S.) hayashii Djakonov, 1961 (Figs. 8A–8N)

Henricia hayashii Djakonov, 1961: 22–23, Pl. 2, fig. 8, Pl. 13, figs. 54–55); Chichvarkhin & Chichvarkhina, 2017a: fig4A; Chichvarkhin & Chichvarkhina, 2017b: 27, fig. H.

? Henricia pseudoleviuscula –Yavnov, 2010: 139–140 (non Djakonov, 1958.

Type locality: Sea of Japan, S off Povorotnyi Bay, Russia.

Examined material: ZIHU–2938 (holotype of H. reniossa f. tohokuensis Hayashi, 1940, Soyomaru 1930 station 630, off Tobisima, 200 m depth, 10 Aug 1930; ZIHU–2401 (holotype and paratypes of H. saghaliensis Hayashi, 1940, 3 broken spms, Albatross 1906, station 5023 Cape Patience, Sakhalin; 15 spms, MIMB–33250, Vostok Bay, Jul 2015, leg. I. Krasilnikov; 9 spms, Vostok Bay, 21 Aug 2016, leg. I. Krasilnikov; 5 spms Rudnaya Bay, 6 Jun 2016, leg. A. Chichvarkhin; H. hayashii det. A.M. Djakonov: 1 spm, ZIN–2/14793, KSE, Toporok st. #117, 22 Sep 1949, Nemoro Sea, 57 m depth, sand, rocks; 1 spm, ZIN–5/15938, Taimyr [vessel], 17 Oct 1812, La Perouse Str, Redun-to Isl., 45°20′N 141°31′E, 40 m depth; 1 spm, ZIN–3/8863, Sea of Japan, st. 219, 1912, leg. Pavlenko; 1 spm, ZIN–4/6038 (marked as paratype of H. hayashii), TIRKh #1521, trawl #1, 21 Aug 1930, Sea of Japan, S off Povorotnyi Bay, 44 m depth, leg. Shurin; 1 spm, ZIN–8/8629, Far-Eastern expedition of Zool. Inst. Ac. Sci., st. 37, 8 Sep 1934, Sea of Japan, Sioukhu [Xiaohu?] Gulf; 1 spm, ZIN–6/15939, s/s Storozh st. 3, 20 Jun 1908, Sea of Japan, Askold Is., 25 m depth, on rocks, leg. Brazhnikova; 1 spm, ZIN–7/15940, s/s Storozh st. 6, 6 Jul 1908, Sea of Japan, Peter the Great Bay, 40-48 ftms depth, on rocks, leg. Brazhnikova; 1 spm, ZIN–6/15939, s/s Storozh st. 3, 20 Jun 1908, Sea of Japan, Askold Is; 1 spm, ZIN, Toporok st. #102, 6 Oct 1948, Moneron Is., 45 m depth, on gravel –more similar to H. djakonovi because of the absence of the ridges on intermarginal pates; 1 spm, ZIN–4/6038 (lectotype of H. hayashii), south off Povorotnyi Cape, Sea of Japan, 21 Aug 1930, 44 m, leg. Shurin.

External anatomy. The specimens, found in Vostok Bay possesses R = 48–50 mm, r = 9 mm, R: r = 5.3–5.3. Rays five, cylindrical, slender. Aboral skeleton closely meshed. A bactinal plates (Fig. 8C) rod-shaped and triangular, tri-lobed, with low but discernible ridge. Abactinal pseudopaxillae reniform with 15–25 spines in two rows (Fig. 8B). Papular areas with 1–3 papulae. Abactinal spines (Figs. 8G–8M) long, 420 µm long, 100–120 µm wide at base, gradually extending proximally, with 10–15 apical and subapical thorns, not covered by skin membrane.

Superomarginal plates similar to adjacent aborals but slightly larger, bear 25–30 spines, arranged in 3–4 irregular rows. Intermarginal row extended to a third of ray length; plates round, with about 10 spines in one row. Inferomarginal plates large, with well discernible ridges transversally elongated, pseudopaxillae bear 15–21 spines in 2–3 irregular rows (Fig. 8C).

Ventrolateral plates small, oval; pseudopaxillae bear 10 spines in two irregular rows. Adambulacrals with four larger near-furrow spines and eight smaller spines in two rows (Fig. 8F). Deep furrow spine small, single, double at distal quarter of ray in some specimens. Oral plates each bear single apical, three marginal, and 1–2 suboral spines.

Color in life. Abactinal side bright orange, actinal side orange, lighter than abactinal (Fig. 8A). Anal area darker than background; madreporite light orange.

Ecology: The species was found on rocky substrate at the depth of 5–20 m at water temperature 16 °C.

Distribution. Known for the northwestern part of the Sea of Japan (Djakonov, 1961). Morphologically similar H. reniossa asiatica (Djakonov, 1958) was described from the northwestern shore of the Sea of Japan (Dzhygit Bay). Known specimens of this H. reniossa asiatica possess similar tightly meshed skeleton with distinct ridges on the inferomarginal plates as in H. hayashii. But it is significantly larger than any H. hayashii specimen that we ever studied (R = 142 mm), and possesses very unusually shaped aboral spines with blunt apex and a number of tiny denticles on it (Fig. 8N).

We identified the specimen imaged on fig. 54 of Djakonov (1961) in Henricia hayashii description in ZIN collection, it was labeled as the “holotype” presumably by ZI Baranova (Fig. 8). We found that this specimen does not possess double deep ambulacral spines (Fig. 8M) as described by Djakonov (1961). Also, we found a specimen identified by Djakonov as H. hayashii with two deep adambulacral spines (Fig. 8N) conforming the original diagnosis. It was the only one specimen with broken ray tip from Moneron Island, i.e., this is the only specimen in which deep spines might be counted earlier by Djakonov and/or Baranova: it is nearly impossible to observe these spines in an undamaged specimen. Therefore, we suppose that double deep adambulacral spine is not a distinctive character in this species, e.g., it is also specific for H. densispina (Sladen, 1878). All studied specimens from continental shore of the Sea of Japan possess single deep spine. Here, we are designating one of these specimens as the lectotype of Henricia hayashii (Djakonov, 1961): ZIN–4/6038, South off Povorotnyi Cape, Sea of Japan, Russia, 21 Aug 1930, 44 m, leg. Shurin.

8. Henricia asiatica Djakonov, 1958 (Fig. 9; Supplemental Information 1, first sea star: 1–5th s)

Henricia reniossa asiatica Djakonov, 1958: 303–305, fig. 14; 1961: 22, pl. 2, fig. 11, pl. 12, figs. 52–53.

Henricia asiatica –Chichvarkhin & Chichvarkhina, 2017a: 208, Fig. 4B; Chichvarkhin & Chichvarkhina, 2017b: 25.

Type locality: Dzhygit Bay, Tatar Str., Sea of Japan, Russia.

We found a specimen (Fig. 9) in ZIN collection identified as H. reniossa asiatica and labeled as the “holotype”. We are designating this specimen as the lectotype of Henricia reniossa asiatica (Djakonov, 1958). R = 142 mm, r = 16 mm; ZIN–2/12820, Opposite Dzhygit Bay, Tatar Strait, 14 Sep 1933, 54 m depth, leg. Kobyakova.

Examined material: lectotype, ZIN–2/12820, Opposite Dzhygit Bay, Tatar Strait, 14 Sep 1933, 54 m depth, leg. Kobyakova; 1 spm, ZIN–7/14192, Kurile Islands, KSE, 22 Sep 1949, Shikotan Is., opposite Anama Bay, 50 m depth; 1 spm, ZIN–8/15941, Sea of Japan, near Kekurnyi Cape [Olga Bay], st. 39/451, 27 Oct 1931, 75–83 m depth, gravel, leg. Tarasov; 1 spm, ZIN, Toporok st. 93, 1949, E off Shikotan Is., 286 m depth leg. Kobyakova & Savelieva; 1 spm, ZIN, Dzhygit Bay, Tatar Str., o/tr [Otter-trawl] 73, 14 Sep 1933, leg. Kobyakova.

The specimen of this large sea star, whichx superficially resembles H. (S.) asiatica (= H. reniossa asiatica), had been recorded with the use of remotely controlled submersible apparatus south-east off the outer part of Vostok Bay (opposite Passek Cape, 42°44.6′N 132°43.8′E) at the depth of 45 m (appendix 1). R of the largest individual is about 90–100 mm, aboral coloration dark orange/mahogany. One of these specimens was associated with with a large mussel, Crenomytilus grayanus (Dunker, 1853), probably filtering plankton from water currents generated by the mollusk.

Brun (1976) reported observations interpreted as suspension feeding in Henricia species, hypothesizing that some Henricia species may engage in rheophilic feeding behavior, i.e., collecting suspended phytoplankton in water currents generated by the sponges. If further supported, this could explain why Henricia individuals are often encountered sitting on the sponges, which has often led to an assumed sponge diet. However, most sponges feed on microbial cells, so it remains to be demonstrated that any Henricia could capture such tiny food items. However, we never observed suspension feeding behavior of any Henricia as Rasmunsen (1965) reported for H. sanguinolenta (O.F. (Müller, 1776). Suspension feeding on phytoplankton is a possible feeding strategy at shallow water habitats but is poorly effective at the depths >100 m, hence this species is likely polyphagous even if they feed on phytoplankton at shallower depths.

External anatomy. large in size, R (long radius: mouth to ray tip) of lectotype 142 mm, r (short radius: mouth to interradius) 16 mm, R:r 8.9; disc small, rays long, slender, subcylindrical, tapering to sharp tips (Fig. 9A). Abactinal plates with no tubercles relatively small forming tight reticulation; plates very close set, appearing almost fused; plates crowned with about 10 blunt spines, each tipped with 5–10 very small thorns (Fig. 9E); papular areas rather small, with 1 papula (Fig. 9D); madreporite small, circular, located about 2/3 way between anus and edge of disc. Superomarginals 1/3 larger than abactinal plates bear 40–45 spines, inferomarginals heigh about twice length; twice as large as superomarginal plates and bearing 45 spines; double series of intermarginals extends about 1/3 of R, each plate bearing 15–25 spines; ventrolateral series extending full length of R. Adambulacrals (Figs. 3D, 3E) each with a single deep furrow spine and 30–35 actinal spines, 5 longer spines at furrow edge, and 10–20 smaller distally grading spines behind (Figs. 9B, 9C). Oral plates with 5 marginal and 4–5 suboral spines; in addition, there are 4–5 thick, blunt spines near the distal edge of plate. Color in life unknown, probably orange.

Distribution. It was reported by Djakonov (1961) from southern Kurile Islands and from the northwestern Sea of Japan including type locality. He also reported this species from Peter the Great Bay because of a confusion of Dzhygit Bay (Tatar Strait, actual type location) vs. Noviy Dzhygit Bay (Russkiy Island, Peter the Great Bay).

9. Henricia (S.) densispina (Sladen, 1878) (Fig. 10)

Type locality: Korean Strait, West coast of Japan.

Examined material: 1 spm, MIMB–33249, Vostok Bay, 20 Jul 2016, leg. A. Goloseyev; 1 spm; Henricia spiculifera as identified by Djakonov: 1 spm, ZIN–61/15229, Lesseis(?)-Data (Datta) Cape, mouth of Tumin Riv. near Imperatorskaya Gavan [Sovetskaya Gavan], 28 May 1909, leg. V. K. Arseniev; Henricia spiculifera det. Djakonov: 1 spm, ZIN–1/15205, Akademii Bay, Okhotsk Sea, 38 m, 17 Aug 1917; 3 spms, ZIN–1/15155, Okhotsk Sea, 50 m, 13 Aug 1918, leg. Meder; 3 spm, MIMB– 34800-34802, Vostok Bay, 06–26 Jul 2017, leg. K. Dudka; H. tacita det. Z.I. Baranova, ex H. leviuscula dyscrita det. A.M. Djakonov: 1 spm, ZIN–20/8457 (ex 8/8457), GGI, 3 Jun 1932, tr. 1, #14, Okhotsk Sea, 118-60 m depth, leg. Polutov; 1 spm, ZIN–23/8455, GGI, s/s Ara, st. 25/1, 4 Sep 1939, Okhotsk Sea, leg. Schmidt; 1 spm, ZIN–6/8454, GGI, s/s Ara, st. 25/8, 6 Sep 1939, Okhotsk Sea, 56°24′N 142°12′E, 80 m depth, leg. Schmidt; H. tacita lectotype: 1 spm, ZIN–14/12800, KSE st. 57, Mordvinova Bay, 2 Sep 1947, 52 m depth, on clay, sand, gravel.

External anatomy. The specimens, which we found in Vostok Bay possesses R = 32.5–55 mm, r = 7–11 mm, R: r = 4.6–5. Rays five, broad at base, tapering. Disc broad. Aboral skeleton widely meshed. Abactinal plates tri-lobed with well discernible tubercles. Abactinal pseudopaxillae with 18–25 spines in 3–5 rows. Papular areas with 1–2 papulae. Abactinal spines slender, 450 µm long, 80–90 µm wide, with 3–4 long fine apical thorns (Figs. 10G– 10K), not covered by skin membrane.

Marginal rows irregular proximally, after a half of ray length well discernible. Superomarginal row, consists of plates similar but slightly larger than adjacent aborals, bearing about 25 spines, same as abactinal spines, arranged in four irregular rows. Intermarginal row extended to full ray length; plates with about 20 spines in one row. Plates of intermarginal row oval, smaller than superomarginals. Inferomarginal plates relatively large, transversally elongated, with ridges. pseudopaxillae bear 30–35 spines in 4–5 irregular rows.

Ventrolateral plates round or oval; pseudopaxillae bear about 20 spines in four irregular rows. Adambulacrals with three larger near-furrow spines and 8–9 smaller spines in three rows (Fig. 9F). Deep furrow spine small, single but double at ray tip (Figs. 10N, 10O). Oral plates each bear single apical, four marginal, and three suboral spines.

Color in life. Abactinal and actinal sides bright orange (Figs. 10A, 10B). Anal area darker than background; madreporite light creamy. Light yellow to orange at near-furrow area.

Ecology. The species was found on rocky substrate at the depth of 10 m at water temperature 20 °C.

Distribution. Known from the northwestern part of the Sea of Japan and South China Sea (Xiao, Liao & Liu, 2011) and Japan (Hayashi, 1940). Similar species previously reported by Djakonov (1961) from Tatar Strait as H. spiculifera and H. densispina likely belongs to a different species possessing short and more stout spines with usually four apical thorns. A species inhabiting the Sea of Japan referred to as H. spiculifera or H. leviuscula spiculifera (Hayashi, 1940; Djakonov, 1961) and probably from South China Sea (Xiao, Liao & Liu, 2011) belong to a distinct species possessing very fine slender spines crowned with 3 long thorns, while in H. densispina the spines are stouter (Xiao, Liao & Liu, 2011).

The specimens from Vostok Bay also resemble H. leviuscula dyscrita (Fisher, 1911) described from California. This name was reported by Djakonov (1948) from the western Pacific, Okhotsk Sea. Later, he did not mention this name in his publications. We found three specimens in ZIN collection identified as H. leviuscula dyscrita, but later they were re-identified as H. tacita Djakonov, 1958. We compared these specimens with the specimen ZIN–14/12800 marked as “H. tacita holotype” presumably by Z.I. Baranova after A.M. Djakonov’s death (although the holotype was not designated for this name by the author): this specimen from Aniva Bay, off Sakhalin Island possess less discernible superomarginal plates, the ridges on proximal marginal plates, and wider rays than re-identified exemplars from Okhotsk Sea, i.e., this specimen strikingly resembles H. reniossa Hayashi, 1940 described from northern Japan, although these two species possess very distinctive abactinal spines. There are four extra “H. leviuscula dyscrita det. Djakonov” specimens from Okhotsk are listed in ZIN catalogue (ZIN–4/3453 and ZIN–10/8450) collected by Ushakov in 1932, but we did not succeed in finding them. All these specimens are likely the syntypes of H. tacita Djakonov, 1958. To avoid future confusion, we are designating the lectotype for H. tacita Djakonov, 1958 with the specimen ZIN–14/12800 because it fully conforms to Djakonov’s original diagnosis and photographed specimen (Djakonov, 1961: Pl. 11, fig. 44).

The specimens from Vostok Bay are different from all specimens mentioned above. They do not possess crescent-shaped pseudopaxillae and smaller papular areas, i.e., do not belong to H. tacita or H. leviuscula dyscrita.

Abundance and spatial distribution of Henricia in Vostok Bay

During 2010, 2014–2017, we recorded 537 individuals of Henricia spp. in Vostok Bay (Table 2). Two of these individuals of Henricia sp. were recorded by a submersible apparatus, although trawling in this area did not allow us to collect any Henricia species. Just three species were found in periodically desalted (32‰ to 2‰) inner part of the bay, while the others were strictly associated with always highly mineralized (appr. 32‰) outer part, and occurred on mainly rocky bottoms but sometimes on a silty substrate.

Discussion

Smirnov’s (2013) review of the invertebrates of Russian Pacific waters estimates that there are 21 echinasterid species reported from the Sea of Japan. Some of them were confirmed to the eastern part of that sea (H. aniva Djakonov, 1958, H. pseudoleviuscula Djakonov, 1958, H. sachalinica Djakonov, 1958, H. tacita Djakonov, 1958, H. orientalis Djakonov, 1950). Some of the listed species are dubious reports, including some that were likely misidentified (H. spiculifera Clark, 1901, H. aspera robusta Djakonov, 1948). Occurrence of deep-water H. reniossa asiatica Djakonov, 1961, which very likely is a distinct species related to a shallow-water H. reniossa Hayashi, 1940, is possible in Peter the Great Bay but we did not find it in Vostok Bay, probably because we focused mostly on shallow depths. Therefore, the total number of species that we have confirmed for Vostok Bay or its vicinity is estimated to be less than or about 15 species. Several Henricia species are known from adjacent waters of Korea and Japan, e.g. H. ohshimai Hayashi, 1940, H. reniossa Hayashi, 1940, H. nipponica Uchida, 1928, so they could also be found here.

In general, Henricia sea stars are common in Vostok Bay. However, H. djakonovi dominates among the others making about 80% of found individuals (Chichvarkhin, 2017a). The second abundant species is H. nipponica (about 15% of found individuals), while the others are rather rare (Table 2). The H. densispina, H. hayashii, and H. granulifera were encountered within this study just once despite the fact that the two latter species were found abundant in Rudnaya Bay, where water salinity is high and remains stable throughout the year. We hypothesize that most Henricia species are intolerant of decreased salinity in the inner part of Vostok Bay, and are restricted to the outer bay where the salinity was closer to oceanic. All species treated here inhabit near-shore rocky areas, with none found on the shallow silty bottom that completely occupies the central part of Vostok Bay and its inner part. The only exceptions were two remotely-recorded exemplars from deeper water on a silty bottom.

Conclusions

This study revealed seven Henricia species that inhabit Vostok Bay, with two additional species suspected as present but not yet sampled. All these species can be clearly identified with DNA barcoding approach using 16S rRNA marker. Morphological characters are also very valuable for identification of most species. Vostok Bay does not constitute a good habitat for high Henricia species diversity because of relatively low salinity water, especially in summer time, less than 30 m depths, and silty bottoms. However, a discovery of a few overlooked species remains possible along the outer shore of the bay.