Squalus mitsukurii Jordan & Snyder, 1903

Viana, Sarah T. F. L. & Carvalho, Marcelo R. de, 2020, Squalus shiraii sp. nov. (Squaliformes, Squalidae), a new species of dogfish shark from Japan with regional nominal species revisited, Zoosystematics and Evolution 96 (2), pp. 275-311 : 275

Squalus mitsukurii Jordan & Snyder, 1903 Figs 2 , 3C, D , 7E, F , 8B ; Tables 2, 6 Longnose spurdog; Futo-tsunozame (Japanese)

Squalus mitsukurii Jordan and Snyder 1901: 129 (name only); Jordan and Snyder 1903: 629; fig. 3 (original description, illustration; type by original designation; type locality: Misaki, Japan); Zhu 1960: 107, 109-110 (description; Northwest Pacific Ocean); Zhu et al. 1984: 284 (cited; Japan); Parin 1987: 48 (cited; Japan); Siming et al. 1988: 1 (listed; Northwest Pacific Ocean); Compagno and Niem 1998 (in part): 1230 (cited; Northwest Pacific Ocean); Zhu and Meng 2001: 311, 319-321 (cited, description; Northwest Pacific Ocean); Compagno 2002 (in part): 381, 385 (listed, description; Central Pacific Ocean); Nakabo 2002: 156 (listed; Tohoku District, Ryukyu Islands, Okinawa Trough, South China Sea); Compagno et al. 2005a (in part): 78 (description; Japan to Taiwan); Nakabo 2013: 196 (listed; Tohoku District, Ryukyu Islands, Okinawa Trough, South China Sea).

Squalus blainvillei : Zhu and Meng 2001: 311, 315-316 (cited, description; Japan).

Type material.

AMNH 8822 (paratype), female, 248 mm TL; SU 7184 (paratype, identified as S. acanthias ), male, 277 mm TL; SU 7748 (paratype), two females, 240-243 mm TL, male, 247 mm TL (All embryo paratypes taken from the holotype); SU 12793 (holotype), adult female, 710 mm TL, Honshu Island, Misaki, Japan, 35.159430°, 139.493865°, 14104 m depth (uncertain, according to CAS), collectors D. S. Jordan and J.O. Snyder in 1900; SU 12794 (paratype), adult male, 770 mm TL, data same as holotype.

Additional material.

HUMZ 33680, adult female, 760 mm TL, East China Sea, 29°38'N, 134°E; HUMZ 79798, adult female, 835 mm TL, Kyushu-Palau Ridge, 26°46.5'-26°46.6'N, 135°20.3'-135°20.8'E, 340-640 m depth; HUMZ 89858, juvenile female, 705 mm TL, off Hachijo-jima Island, Tokyo, Japan; HUMZ 97463, adult female, 800 mm TL, Ishikari Bay, Tokyo, Japan, 43°12.4'N, 141°08.5'E, 22 m depth; HUMZ 102986, adult female, 1005 mm TL, Central Pacific Ocean, near Northern Mariana Islands, 17°39.4'N, 145°50.3'E, 450 m depth; HUMZ 102987, adult female, 970 mm TL, Central Pacific Ocean, near Northern Mariana Islands, 19°09'N, 142°59'E, 520 m depth; HUMZ 102988, adult female, 1025 mm TL, same locality as HUMZ 102987; HUMZ 113586, adult female, 1120 mm TL, off Shirahama, Shimoda, Shizuoka Prefecture, Japan, 45 m depth; HUMZ 113587, adult female, 990 mm TL, same locality as HUMZ 113586; HUMZ 113588 adult female, 960 mm TL, same locality as HUMZ 113586; NSMT-P 44097, adult female, 740 mm TL, Izu, Honshu, Japan; NSMT-P 44381, adult male, 770 mm TL, off Koura, Suruga Bay, Honshu, Japan; NSMT-P 65518, adult female, 1119 mm TL, Suno-saki Point, Boso Peninsula, Chiba Prefecture, Honshu, Japan, 25 m depth; NSMT-P 77187, adult male, 1000 mm TL, unknown locality; NSMT-P 97762, neonate male, 278 mm TL, Tsushima, Nagasaki Prefecture, Kyusyu, Japan; SU 14245, adult female, 580 mm TL, Hong Kong, China; ZUMT 1360, female embryo, 178 mm TL, off Atami, Kanagawa Prefecture, Japan; ZUMT 21114, female embryo, 190 mm TL, Nagasaki, Japan.

Diagnosis.

Large-sized (710-1120 mm TL for adults) Squalus species that is distinguished from its regional congeners by: body dark grey to black in colour vs. body grey to light grey for S. japonicus vs. brownish-grey for S. brevirostris vs. brown for S. shiraii sp. nov.; dermal denticles tricuspidate and rhomboid (except for S. japonicus ) vs. unicuspid and lanceolate. Squalus mitsukurii is separated from S. japonicus and S. brevirostris when adults by prenarial length 5.6%, 4.1%-5.6%TL (vs. 5.9%, 5.9%-6.8% TL for S. japonicus vs. 4.0%, 3.8%-4.3% TL for S. brevirostris ) and from S. brevirostris and S. shiraii sp. nov. by smaller eyes, its length 3.6%, 3.1%-4.0% TL (vs. 5.0%, 4.2%-5.1% TL for S. brevirostris vs. 4.9%, 4.4%-4.9% TL for S. shiraii sp. nov.) and length of second dorsal-fin spine 0.8-1.1 times length of first dorsal-fin spine (vs. 1.3-1.8 times for S. brevirostris vs. 1.2-1.3 times for S. shiraii sp. nov.). It is further distinct from S. japonicus by smaller preoral length and distance nostril-upper labial furrow (10.3%, 7.6%-10.3% TL and 4.3%, 3.9%-4.5% TL vs. 10.7%, 10.7%-12.2% TL and 4.6%, 4.6%-5.1% TL for S. japonicus ), more elongate first dorsal fin, its base length 8.2%, 7.6%-9.0% TL (vs. 6.7%, 6.6%-7.5% TL for S. japonicus ), broader pectoral fins and head (pectoral-fin posterior margin length 11.7%, 9.9%-12.5% TL and head width at mouth 12.2%, 10.9%-12.2% TL vs. 8.6%, 7.8%-9.2% TL and 9.7%, 9.7%-10.6% TL for S. japonicus ). Squalus mitsukurii differs from S. brevirostris by: pectoral fin with free rear tips rounded and posterior margin straight to weakly concave vs. free rear tips pointed and posterior margin conspicuously concave for S. brevirostris ; shorter pectoral-fin inner margin, its length 9.5%, 7.7%-9.5% TL vs. 10.3%, 9.8%-11.2% TL for S. brevirostris ; postventral caudal margins not uniformly white vs. uniformly white for S. brevirostris .

Description.

External morphology. Body fusiform, markedly humped anteriorly from posterior margin of the spiracle to pelvic fin origin, turning slender posteriorly; body conspicuously robust and stout with head height 1.2 (0.8-1.4) times trunk height and 1.6 (0.9-1.7) times abdomen height and head width 1.2 (1.0-1.6) times trunk width and 1.5 (1.1-2.6) times abdomen width (Fig. 2A-C ). Head flattened anteriorly, conspicuously elongate, its length 24.2% (20.4%-24.4%) TL and broad, its width at mouth 12.2% (10.4%-12.8%) TL. Snout rounded at the tip and noticeably elongate, its preorbital length 7.3% (6.9%-10.7%) TL; prenarial length 1.3 (1.1-1.4) times distance between nostrils to upper labial furrow and 0.5 (0.5-0.6) times preoral length; anterior margin of nostrils wide and bi-lobed; internarial space 1.3 (0.8-1.4) times eye length (Fig. 2D, E ). Eyes elliptical with anterior margin concave and posterior margin notched, placed laterally; eyes large, its length 4.1 (1.6-3.0) times eye height. Prespiracular length 0.5 (0.5-1.0) times prepectoral length and 1.8 (1.5-2.8) times preorbital length. Spiracles crescent, located laterally and behind the eyes; spiracles elongate, its length 0.4 (0.2-0.4) times eye length. Prebranchial length 1.6 (1.0-1.8) times prespiracular length. Gill slits vertical and concave, placed anterior to origin of pectoral fins; gill slits very tall with first gill slit height 1.7% (1.5%-2.8%) TL; fifth gill slit 1.3 (0.7-1.7) times taller than first gill slit.

Preoral length 1.2 (1.0-1.5) times greater than mouth width. Mouth somewhat straight and conspicuously broad (mouth width 1.8, 1.5-2.1 times internarial width and 1.5, 1.2-1.8 times prenarial length); upper labial furrow elongate, its length 2.5% (2.1%-2.7%) TL, bearing a thin fold; lower labial furrow markedly elongate, lacking fold. Teeth unicuspid, flattened labial-lingually, similar in both jaws; teeth somewhat rectangular, very broad at the crown; cusp short, thick, pointed and oblique; mesial cutting edge convex and oblique; distal heel conspicuously rounded; mesial heel sharp; apron thick and small, placed more laterally in the upper teeth and in the midline of crown base in the lower teeth, slightly more elongate in the lower teeth than in the upper teeth; median teeth present on upper jaw in adult paratype only and distinct from the subsequent teeth by: teeth hexagonal with cusp and apron placed more medially; both mesial and distal heels pointed (Fig. 3C, D ). One to two series of functional teeth on upper jaw and two series in lower jaw; 13-0-15 for holotype (13-1-13) teeth rows on upper jaw; 12-0-12 (11-0-11) teeth rows on lower jaw.

Interdorsal space 2.0 (1.9-3.0) times larger than dorsal-caudal space and 0.9 (0.9-1.3) times prepectoral length. Origin of first dorsal fin located prior to vertical traced at pectoral-fin free rear tips. First dorsal fin elongate, its length 1.1 (1.0-1.3) times length of second dorsal fin; first dorsal-fin base length 0.8 (0.7-1.3) times height of first dorsal fin. First dorsal fin conspicuously broad at fin web; first dorsal-fin anterior margin markedly convex and elongate, its length 12.0% (9.3%-13.2%) TL; first dorsal-fin posterior margin concave, its length 9.3% (7.0%-10.6%) TL; first dorsal-fin inner margin elongate, its length 6.2% (5.0%-6.6%) TL; first dorsal-fin apex broadly rounded; first dorsal fin vertical and low, its height corresponding to 1.6 (1.1-1.6) times length of first dorsal-fin inner margin and 1.3 (0.8-1.4) times preorbital length (Fig. 2F, J ). Origin of first dorsal-fin spine anterior to vertical traced at pectoral-fin free rear tips. First dorsal-fin spine thick, its width at base 1.0% (0.5%-1.0%) TL; first dorsal-fin spine elongate, its length 3.9% (2.1%-5.4%) TL) and corresponding to 0.4 (0.3-0.6) times first dorsal fin height, although not reaching first dorsal-fin apex. Pre-second dorsal length 2.5 (2.4-3.1) times prepectoral length. Origin of second dorsal fin behind a vertical traced at pelvic-fin free rear tips. Second dorsal fin broad at fin web with second dorsal-fin apex conspicuously rounded and lobe-like; second dorsal fin small, its length at base 0.9 (0.7-1.3) times first dorsal fin base length; second dorsal fin oblique and low with second dorsal-fin height 1.3 (0.8-1.4) times length of second dorsal-fin inner margin; second dorsal-fin anterior margin convex and elongate, its length 10.2% (7.7%-11.9%) TL; second dorsal-fin posterior margin concave and somewhat falcate, its length 6.3% (4.5%-6.3%) TL; second dorsal-fin inner margin length 5.3% (4.1%-5.9%) TL (Fig. 2G, K ). Second dorsal-fin spine elongate, its length 0.6 (0.5-1.0) times second dorsal fin height and 1.1 (0.8-1.9) times length of first dorsal-fin spine, although never reaching second dorsal-fin apex; second dorsal-fin spine thick, its base width 0.9% (0.7%-1.1%) TL.

Pectoral fins markedly broad and elongate (pectoral-fin posterior margin length 11.7%, 9.2%-12.5% TL), although never extending up to trunk height when adpressed laterally on body; pectoral-fin anterior margin straight; pectoral-fin inner margin convex; pectoral-fin posterior margin weakly concave medially; pectoral-fin apex rounded and lobe-like; pectoral-fin free rear tips rounded, reaching the same length when a horizontal line is traced at pectoral-fin apex (Fig. 2H, L ); pectoral-fin anterior margin large, its length 1.6 (1.4-2.3) times greater than pectoral-fin inner margin length and 1.3 (1.1-1.5) times pectoral-fin posterior margin length. Pectoral-pelvic space 0.9 (0.7-1.1) times pelvic-caudal space. Pelvic fins broad with pelvic-fin anterior and posterior margins convex; pelvic-fin free rear tips rounded and lobe-like; pelvic fin elongate, its length 11.5% (8.4%-12.6%) TL; pelvic fins nearer to second dorsal fin than to first dorsal fin. Adult males with clasper extremely robust and thick; clasper groove medial-dorsally and longitudinal, profound and short, not extending forward to inner margin of the clasper; clasper inner margin length 0.7-1.3 times length of pelvic-fin inner margin; apopyle broad, placed anteriorly in the clasper groove; hypopyle wide, located just above the rhipidion; rhipidion blade-like and evidently slender and elongate, placed at the medial-distal end of the clasper.

Caudal keel prominent and situated laterally in the precaudal peduncle since insertion of second dorsal fin to behind origin of caudal fin. Caudal fin conspicuously slender in the upper caudal lobe; dorsal caudal margin somewhat convex proximally and conspicuously straight distally (Fig. 2I, M ); caudal fin elongate with dorsal caudal margin length 1.0 (0.9-1.1) times head length and 2.0 (1.7-2.0) times larger than length of preventral caudal margin; upper postventral caudal margin straight; lower postventral caudal margin somewhat convex; preventral caudal margin convex, its length 1.9 (1.5-3.8) times length of pelvic-fin inner margin; both posterior and ventral caudal tips rounded and thin; caudal fork discontinuous and conspicuously concave, its width 7.0% (6.1%-7.7%) TL.

Squamation (Fig. 7E, F ). Dermal denticles tricuspid, rhomboid to heart-shaped and imbricate, conspicuously broad at the crown, its length equal to its width; cusps pointed and posterior; lateral cusps often inconspicuous and much shorter than median cusp; median cusp conspicuous and wide; median ridge prominent, tall and thick with anterior furrow oval and profound; anterior margin of the crown broad, convex and arrow-shaped with one small ridge on each side; one to two lateral ridges, thin and smaller than median ridge. Dermal denticles slightly larger and more imbricate in adults than juveniles.

Colouration (Fig. 2 ). Body black dorsally, dark grey ventrally and laterally since first dorsal fin insertion to origin of caudal fin. Dorsal fins blackish, dark grey at fin base near the dorsal-fin spines; lower half of anterior margin of dorsal fins whitish. Dorsal-fin spines brownish anteriorly and white posteriorly and at the tips. Pectoral fins black dorsally and ventrally, although dark grey near pectoral-fin inner margin; pectoral-fin posterior margin fairly white. Pelvic fins dark grey dorsally and ventrally, somewhat dark brown at the fin base; pelvic-fin posterior margins slightly white. Caudal fin black, dark grey near caudal fin origin and proximally over vertebral column; dorsal caudal margin dark grey proximally; postventral caudal margins slightly white, except near the caudal fork; preventral caudal margin blackish. Embryos, neonates and young juveniles differ from adults by having body light grey, dorsal fins light grey with dorsal-fin apex blackish and dorsal-fin free rear tips white, caudal fin light grey with postventral caudal margins broadly white, dark caudal bar conspicuous, black upper caudal blotch prominent and black caudal blotch at the base of lower caudal lobe, located horizontally.

Vertebral counts (Table 6 ). 68 (holotype) 70-72 (other material) diplospondylous vertebrae; 30 (26-31) caudal vertebrae; 116-117 total vertebrae.

Geographical distribution.

Squalus mitsukurii is a regional endemic to the North-western Pacific Ocean with records along the coasts of China, Marianna Islands and Japan. It inhabits continental shelves and upper continental slopes within depth ranges of 22 to 640 m (Fig. 8B ). This species possibly reaches depths of up to 980 m in the Western Pacific Ocean, but it is often caught between 180-300 m depth ( Chen et al. 1979).

Remarks.

Squalus mitsukurii has been misidentified with many nominal species in all oceans and, more particularly, with S. acutirostris , S. hawaiiensis , S. boretzi and S. shiraii sp. nov. in the North Pacific Ocean. Squalus mitsukurii exhibits smaller interdorsal space than S. hawaiiensis (21.1%, 21.1%-25.9% TL vs. 26.7%-30.0% TL), larger first and second dorsal fins (first dorsal-fin base length 8.2%, 7.6%-9.0% TL and second dorsal-fin base length 7.2%, 6.8%-7.9% TL vs. 6.2%-7.4% TL and 4.9%-5.5% TL in S. hawaiiensis ), which corroborates the findings of Daly-Engel et al. (2018). Torso measurements that are suggested as being diagnostic to separate these species in the referred study show minor overlapping and they must be used with caution despite range values of the direct measurements (e.g. pre-first and pre-second dorsal lengths, precaudal length) are somewhat higher in S. hawaiiensis . The Japanese species further exhibit more elongated pectoral fins, its inner margin 9.5%, 7.7%-9.5% TL (vs. 6.4%-7.4% TL in S. hawaiiensis ). Vertebral counts are congruent between these species, which is contrary to Daly-Engel et al. (2018) when comparing data taken from Chen et al. (1979). The latter work possibly included specimens of S. shiraii sp. nov. which is the only Japanese species with the highest number of vertebral counts. Morphologically similar Squalus species tend to exhibit overlapping of vertebral counts as seen here between S. mitsukurii , S. hawaiiensis and S. boretzi , with a few exceptions. Squalus mitsukurii may be separated from S. brevirostris , S. melanurus S. blainvillei and S. grahami by monospondylous vertebrae and from S. blainvillei , S. melanurus and S. montalbani by diplospondylous vertebrae and S. brevirostris , S. shiraii sp. nov., S. blainvillei and S. lalannei by total vertebrae. Precaudal vertebrae separates it from S. shiraii sp. nov., S. blainvillei , S. lalannei and S. montalbani .

Figures

Figure 2. Squalus mitsukurii: lateral (A-C) and ventral (D, E) views; first (F, J) and second (G, K) dorsal fins; pectoral (H, L) and caudal (I, M) fins. SU 12794 (paratype), adult male, 770 mm (A, D, F-I); HUMZ 102988, adult female, 1025 mm TL (B, E, J-M); NSMT-P 97762, neonate male, 278 mm TL (C). Scale bars: 50 mm (A, B, D, E); 25 mm (C); 20 mm (F-M).

Figure 3. Upper (A, C, E, G, I) and lower (B, D, F, H, J) teeth of S. shiraii sp. nov. (A, B; HUMZ 80329), S. mitsukurii (C, D; HUMZ 33680), S. japonicus (E, F; HUMZ 189737), S. brevirostris (G, H; HUMZ 189762) and S. suckleyi (I, J; NSMT-P 92640). Scale bars: 1 mm.

Figure 7. Scanning electron microscopy of the dermal denticles. Squalus shiraii sp. nov. (A, B): HUMZ 149389 (holotype), adult male, 590 mm TL. S. formosus (C, D): CSIRO H- 6816 - 01 (holotype), adult male, 720 mm TL. S. mitsukurii (E, F): HUMZ 102987, adult male, 970 mm TL. S. japonicus (G, H): NSMT-P 44380 (neotype), adult male, 645 mm TL (G); NSMT-P 91127, juvenile female, 410 mm TL (H). S. brevirostris (I, J): NSMT-P 47378, adult female, 600 mm TL (I); KAUM-I 187, adult female, 578 mm TL (J). S. suckleyi (K, L): NSMT P- 92640, adult female, 970 mm TL. Scale bars: 50 μm (B); 100 μm (D, F, L); 200 μm (A, C, E, G-K).

Figure 8. Map of the North-western Pacific Ocean, showing the geographical distribution of Squalus species. A: S. shiraii sp. nov. (red); B: S. mitsukurii (orange); C: S. japonicus (brown); D: S. brevirostris (yellow); E: S. acutirostris (green); F: S. suckleyi (pink). Star: holotype / neotype; Dotted circle: paratypes; Circle: other material.