Squalus shiraii, Viana & Carvalho, 2020

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 shiraii sp. nov. Figs 1 , 3A-B , 7A-B , 8A ; Tables 1, 6

Holotype.

HUMZ 149389, adult male, 590 mm TL, Okinawa Trough, 25°37'28"N, 126°05'35"E to 25°38'12"N 126°07'83"E. Collected on 2 August 1994 by unknown collector.

Paratypes.

HUMZ 80329, adult female, 770 mm TL, East China Sea, 25°33.8'N, 126°25.2'E, 310 m depth, longline, collected on 4 December 1978 by T. Kanayama; HUMZ 80330, juvenile male, 365 mm TL, locality and collection data same as HUMZ 80329; HUMZ 80331, adult female, 755 mm TL, locality and collection data same as HUMZ 80329; HUMZ 101718, adult male, 685 mm TL, off north-west of Okinawa-jima Island, Japan, collected in July 1983 by K. Nakaya; HUMZ 146165, adult male, 600 mm TL, 31°58.5'N, 173°09.5'E, 390 m depth, longline, collected on 21 February 1997; HUMZ 149391, adult male, 623 mm TL, locality and collection data same as holotype; HUMZ 149392, adult male, 595 mm TL, locality and collection data same as holotype; HUMZ 149394, adult male, 623 mm TL, locality and collection data same as holotype; HUMZ 149395, adult male, 595 mm TL, locality and collection data same as holotype; HUMZ 149426, adult male, 630 mm TL, locality and collection data same as holotype; HUMZ 149434, adult male, 580 mm TL, Okinawa Trough, 25°40'32"N, 126°14'18"E to 25°41'43"N, 126°16'08"E, collected on 2 August 1994 by unknown collector; HUMZ 149438, adult male, 605 mm TL, locality and collection data same as HUMZ 149434.

Type locality.

Okinawa Trough, Japan, 25°37'28"N, 126°05'35"E to 25°38'12"N, 126°07'83"E, 2 August 1994, unknown collector.

Additional material.

HUMZ 495, juvenile female, 350 mm TL, unknown locality; HUMZ 39991, juvenile male, 260 mm TL, unknown locality.

Diagnosis.

Single values correspond to the holotype and range to paratypes, respectively. A Squalus species that is separated from its regional congeners by: first dorsal fin conspicuously upright (vs. first dorsal fin prone); pectoral-fin posterior margin falcate (vs. not falcate); upper and lower caudal lobes markedly slender with dorsal and ventral caudal tips pointed and broadly white (vs. upper and lower caudal lobes wide with dorsal and ventral caudal tips rounded and greyish in colour); dermal denticles lanceolate, except for S. brevirostris (vs. tricuspidate); smaller claspers with clasper outer length 3.3%, 3.3%-3.4% TL and clasper inner length 6.3%, 5.9%-6.3% TL (vs. 4.5%-4.9% TL, 6.9%-8.4% TL for S. mitsukurii vs. 4.8%, 4.3%-5.6% TL and 7.5%, 7.2%-9.1% TL for S. japonicus ; vs. 3.9%, 3.9%-5.1% TL and 7.1%, 7.0%-8.1% TL for S. brevirostris ). Squalus shiraii sp. nov. further differentiates from S. mitsukurii by more elongate eyes, its length 4.9%, 4.4%-4.9% TL (vs. 3.6%, 3.1%-4.0% TL) and smaller fifth gill slit, its length 1.7%, 1.7%-2.1% TL (vs. 2.3%, 2.2%-2.6% TL). It is separated from S. japonicus and S. brevirostris by prenarial length 5.5%, 5.4%-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 width of first dorsal-fin spine 0.9%, 0.9%-0.9% TL (vs. 0.7%, 0.5%-0.8% TL for S. japonicus vs. 0.7%, 0.5%-0.7% TL for S. brevirostris ). Squalus shiraii sp. nov. further differs from S. japonicus by shorter snout, its preorbital length 7.9%, 7.4%-7.9% TL (vs. 8.7%, 8.7%-9.3% TL for S. japonicus ), smaller preoral length 10.4%, 9.4%-10.4% TL (vs. 10.7%, 10.7%-12.2% TL), larger first dorsal fin, its base length 7.7%, 7.7%-8.7% TL and first dorsal-fin posterior margin length 9.2%, 9.0%-9.3% TL (vs. 6.7%, 6.6%-7.5% TL and 7.8%, 6.7%-8.6% TL for S. japonicus ) and wider pectoral fin, its posterior margin length 10.0%, 10.0%-11.7% TL (vs. 8.6%, 7.8%-9.2% TL). It is separated from S. brevirostris by wider internarial space, its width 4.8%, 4.1%-4.8% TL (vs. 3.6%, 3.4%-3.8% TL for S. brevirostris ), smaller second dorsal fin with inner margin length 3.6%, 3.2%-4.1% TL (vs. 5.0%, 4.8%-5.7% TL), shorter pectoral-fin inner margin, its length 7.3%, 7.3%-8.3% TL (vs. 10.3%, 9.8%-11.2% TL) and narrower caudal fin, its width at caudal fork 6.4%, 5.7%-6.4% TL (vs. 6.6%, 6.6%-7.3% TL). Squalus shiraii is distinguished from S. formosus regardless of maturity by having more elongate precaudal (78.3%, 78.6%-80.5% TL), pre-second (60.5%, 61.1%-63.4% TL) and pre-first (30.5%, 29.6%-31.2% TL) dorsal length (vs. 77.6%-78.3% TL, 59.4%-59.7% TL and 28.1%-29.0% in S. formosus ).

Description.

Single values correspond to the holotype and range to paratypes, respectively.

External morphology. Body elongate (590-770 mm maximum TL in adults), fusiform and robust, arched dorsally from anterior margin of the eye to insertion of first dorsal fin, turning straight from abdomen to caudal fin (Fig. 1A-C ); body equally deep from head to abdomen with head height 0.9 (0.9-1.0) times trunk height and 0.9 (0.8-1.0) times abdomen height; body with its greatest width at head (head width 1.1 (1.0-1.2) times trunk width and 1.3 (1.2-1.5) times abdomen width. Head flattened anterior-dorsally, arched posterior-dorsally and elongate, its length 24.1% (21.9%-23.9%) TL. Snout conspicuously obtuse at tip and large (preorbital length 7.9%, 7.4%-8.1% TL) (Fig. 1D-E ); anterior margin of nostrils strongly broad and bi-lobed, its distance to snout tip 1.1 (1.1-1.3) times its distance to upper labial furrow; prenarial length 0.5 (0.5-0.6) times preoral length; internarial space 1.0 (0.8-1.1) times eye length. Eyes oval and enlarged, its length 3.1 (1.9-3.4) times eye height; eyes with anterior margin convex and posterior margin slightly notched. Prespiracular length 1.7 (1.7-1.7) times preorbital length and 0.6 (0.6-0.6) times prepectoral length. Spiracles crescent and large, its length 1.5% (1.0%-1.3%) TL, located laterally behind the eyes. Gill slits tall and somewhat vertical, placed anteriorly to pectoral-fin origin; fifth gill slit height 1.4 (1.1-1.7) times first gill slit height.

Preoral length 1.3 (1.3-1.5) times mouth width and 0.4 (0.4-0.5) times head length. Upper labial furrow short (its length 0.5, 0.4-0.5 times eye length) with thick and small fold; lower labial furrow elongate with inconspicuous fold. Mouth arched and broad, its width 1.5 (1.3-1.4) times prenarial length and 1.7 (1.5-1.7) times internarial space. Teeth similar in both jaws; upper teeth smaller than lower teeth; teeth with cusp oblique, thick and small; mesial cutting edge slightly convex; distal heel rounded; mesial heel notched; apron short and heavy (Fig. 3A, B ). Two and two to three series of functional teeth in the upper and lower jaws, respectively, 13-14 for holotype (13-14 for paratypes) teeth rows on upper jaw and 11-11 (11-12) teeth rows on lower jaw.

Origin of first dorsal fin over the vertical line traced at pectoral-fin insertion. First dorsal fin elongate, its length 1.5 (1.4-1.7) times height of first dorsal fin; first dorsal fin conspicuously tall, its height 1.7 (1.5-1.8) times first dorsal-fin inner margin length; first dorsal-fin anterior margin convex, posterior margin straight in the upper half and conspicuously concave in the lower half; first dorsal-fin apex rounded and evidently slender at the fin web; first dorsal-fin free rear tip triangular and first dorsal-fin inner margin short, its length 0.6 (0.5-0.7) times first dorsal-fin base length (Fig. 1F, J ). First dorsal-fin spine thick with base width 0.9% (0.9-0.9%) TL and elongate (first dorsal-fin spine length 0.5, 0.4-0.5 times height of first dorsal fin), although never reaching first dorsal-fin apex. Interdorsal space 1.0 (1.0-1.2) times prepectoral length and 2.3 (2.2-2.8) times dorsal-caudal space. Pre-second dorsal length 2.0 (2.0-2.1) times pre-first dorsal length. Second dorsal fin elongate, its length 0.9 (0.7-0.9) times length of first dorsal fin; second dorsal fin tall, its height 1.6 (1.4-1.8) times second dorsal-fin inner margin length; second dorsal-fin anterior margin convex; second dorsal-fin posterior margin strongly concave and falcate; second dorsal-fin apex rounded and lobe-like; second dorsal-fin inner margin small, its length 0.5 (0.5-0.6) times second dorsal-fin base length (Fig. 1G, K ). Second dorsal-fin spine thick with base width 0.7% (0.7%-0.8%) TL; second dorsal-fin spine elongate, its length 0.9 (0.7-0.9) times height of second dorsal fin and 1.3 (1.2-1.6) times length of first dorsal-fin spine, although not reaching second dorsal-fin apex.

Prepectoral length 3.0 (2.8-2.9) times preorbital length. Pectoral fins with anterior and inner margins conspicuously convex; pectoral-fin posterior margin markedly concave; pectoral-fin apex and free rear tips rounded and lobe-like; pectoral-fin apex conspicuously transcending the horizontal line traced at pectoral-fin free rear tip (Fig. 1H, L ); pectoral fins markedly falcate and broad with pectoral-fin posterior margin 1.0 (0.4-1.0) times trunk height; pectoral-fin anterior margin 2.0 (1.7-2.0) times pectoral-fin inner margin length and 1.4 (1.4-3.2) times pectoral-fin posterior margin length. Prepelvic length 1.8 (2.0-2.2) times prepectoral length. Pelvic fins located slightly nearer to the first dorsal fin than the second dorsal fin. Pelvic fins with margins straight and apex rounded; pelvic-fin free rear tips rounded to slightly pointed, thin and lobe-like. Adult males with clasper somewhat transcending the pelvic fin; clasper inner length 1.2 (0.3-1.2) times pelvic-fin inner margin length; clasper groove medial-dorsally and vertical, profound and elongate; apopyle broad, located anteriorly in the clasper groove; hypopyle broad, located anterior to rhipidion; rhipidion blade-like, thin and small, placed at the medial-distal end of the clasper.

Pelvic-caudal space 1.4 (1.1-1.6) times pectoral-pelvic space. Caudal keel evident laterally in the caudal peduncle from second dorsal fin free rear tip to caudal-fin origin. Caudal fin with conspicuously thin upper and lower caudal lobes (Fig. 1I, M ); caudal fork concave with its width corresponding to 6.4% (5.7%-6.4%) TL; dorsal caudal margin straight and markedly elongate, its length 0.9 (0.9-1.0) times head length and 2.1 (1.9-2.1) times length of preventral caudal margin; upper postventral margin straight on its upper half and slightly convex on its lower half; lower postventral margin convex; preventral caudal margin convex and short, its length 1.8 (2.1-2.3) times length of pelvic-fin inner margin; dorsal caudal tip rounded; ventral caudal tip markedly pointed.

Squamation (Fig. 7A, B ). Dermal denticles lanceolate and imbricate, broad at the crown base (conspicuously broad in females); length of dermal denticles larger than its width (although it is about equal to its width in females); denticles with median cusp slightly pointed lateral cusps inconspicuous; median and lateral ridges thick; median and lateral ridge bifurcated anteriorly; anterior furrow conspicuously profound and oval.

Colouration (Fig. 1 ). Body brown dorsally, light brown laterally, although whitish latero-ventrally from the pelvic fin to the caudal fin and pale ventrally. Dorsal fins brownish, somewhat light brown at dorsal fin base; first dorsal-fin inner margin white; second dorsal-fin posterior margin fairly white at its lower half; second dorsal-fin apex somewhat dark brown. Dorsal-fin spines brownish anterior-laterally and white at the tip. Pectoral fins dark brown, whitish ventrally at pectoral-fin base; pectoral-fin posterior margin fairly white (not uniform); pectoral-fin apex broadly white. Pelvic fins brown and whitish at the pelvic-fin base; pelvic-fin anterior and posterior margins slightly white. Caudal fin dark brown at upper and lower caudal lobes, whitish over vertebral column; postventral caudal margins white, except at the caudal fork where it is dark brown; dorsal and ventral caudal tips broadly white; preventral caudal margin white; dark caudal stripe and bar inconspicuous; black upper caudal blotch somewhat evident in adults. Juveniles with body light brown dorsally, pale lateral and ventrally; first and second dorsal-fin posterior margins slightly white at its lower half; dorsal-fin apex blackish to dark brown at the tip; pectoral fins light brown to reddish-brown with pectoral-fin posterior margins and apex broadly white; pelvic fins light brown to reddish-brown; caudal fin dark brown with postventral caudal margins broadly white, except at the caudal fork; dorsal and ventral caudal tips broadly white; conspicuous upper black caudal blotch in the midline of dorsal caudal margin; lower caudal lobe with oblique black marking at the origin of lower caudal lobe; small black caudal bar at the caudal fork.

Vertebral counts (Table 6 ). 47 for holotype (44-48 for paratypes) monospondylous vertebrae; 93 (91-94) precaudal vertebrae; 122 (120-123) total vertebrae.

Etymology.

This species is named after Dr. Shigeru M. Shirai, Japanese ichthyologist from Tokyo University of Agriculture, for his valuable contributions to Systematics of Squaliformes.

Vernacular.

Shirai’s spurdog; Hiretaka-tsunozame (Japanese).

Geographical distribution.

This species is apparently a Japanese endemic, occurring in the shallow waters of the upper continental slope off Southern Japan in the North-western Pacific Ocean at 310-390 m depth (Fig. 8A ).

Remarks.

Squalus shiraii sp.nov. is often misidentified with S. mitsukurii due to similarities concerning the general shape of body, pectoral and caudal fins and snout length. However, it clearly differs from this species in addition to the characters provided in the diagnosis above by having an obtuse snout, dorsal and ventral caudal tips conspicuously pointed, upper and lower caudal lobes markedly tapered, pectoral fins conspicuously falcate, dermal denticles lanceolate and unicuspidate (vs. snout rounded, dorsal and ventral caudal tips rounded, upper and lower caudal lobes broad, pectoral fins not falcate, dermal denticles rhomboid and tricuspidate in S. mitsukurii ). Squalus shiraii sp. nov. has body brown in colour, postventral and preventral caudal margins whitish, dorsal and ventral caudal tips broadly white and black upper caudal blotch evident in adults. S. mitsukurii has body conspicuously black to dark grey and caudal fins black throughout with post-ventral caudal margin fairly whitish and black upper caudal blotch not evident in adults.

Two recently described species, S. hawaiiensis and S. boretzi , are also morphologically similar to S. mitsukurii , but were supported as distinct according to molecular and morphological data in Daly-Engel et al. (2018) and Dolganov (2019). These species are apparently sympatric in the Hawaiian-Emperor Seamount Chain that runs across the North Pacific Ocean on about 6000 km from the Kamchatka Peninsula, Russia down to Hawaii, USA (Domier et al. 2017). Squalus shiraii sp. nov. share with S. hawaiiensis a more elongate snout that is more evident when considering the ratio prenarial length/inner-nostril labial furrow space (1.2, 1.1-1.3 for S. shiraii sp. nov. vs. 1.3, 1.1-1.1 for S. hawaiiensis ), body robust and presence of black upper caudal blotch, but morphometrics and vertebral counts support that they are conspicuously distinct as provided in the diagnosis above. Squalus shiraii sp. nov. may be further distinguished from the Hawaiian species by shorter pre-second dorsal length 60.5%, 61.1%-63.4% TL (vs. 63.6%-67.0% TL for S. hawaiiensis ), pre-vent length 47.3%, 46.8%-48.7%TL (vs. 50.4%-53.6% TL for S. hawaiiensis ), prepelvic length (44.1%, 44.5%-46.8%TL (vs. 48.6%-52.4% TL for S. hawaiiensis ) and interdorsal space (23.8%, 24.0%-25.7%TL (vs. 26.7%-30.0% TL for S. hawaiiensis ). Other differences include height of second dorsal fin, clasper length and head width at mouth (refer to Daly-Engel et al. 2018 for comparisons). Squalus shiraii sp. nov. has lanceolate dermal denticles and dorsal fins markedly tall and upright (vs. tricuspidate, low and oblique dorsal fins in S. hawaiiensis ). It also has shorter pectoral-caudal space than S. hawaiiensis and S. boretzi (19.6%, 17.1%-22.9% TL vs. 23.6%-27.7% TL for S. hawaiiensis vs. 25.2%-30.6% TL for S. boretzi ). More detailed comparisons with S. boretzi were not accomplished here because we could not yet have access to the full original description of this species that is so far available in Russian only.

Some characteristics of S. shiraii are very similar to those of S. formosus . However, the Japanese species bears much smaller dorsal and pelvic fins and it has larger pre-first, pre-second and pre-caudal length. Other differences with the Taiwanese species include larger snout (preorbital and prenarial length), smaller and thinner second dorsal-fin spine, smaller spiracle and lower gill slits and dermal denticles lanceolate (vs. weakly tricuspidate; Fig. 7C, D ). Squalus formosus is easily identified by the presence of white anterior margin of the first dorsal fin which is absent in the Japanese species. Vertebral counts further help to separate Squalus shiraii sp. nov. from other congeners, including precaudal vertebrae in S. mitsukurii , S. japonicus and S. brevirostris , as well as S. blainvillei , S. lalannei , S. montalbani , S. grahami , S. bahiensis , S. bassi , S. hawaiiensis and S. boretzi and total vertebrae in S. mitsukurii , S. japonicus , S. brevirostris , S. blainvillei , S. lalannei , S. montalbani , S. grahami , S. bahiensis , S. melanurus , S. hawaiiensis and S. boretzi . Other morphometric differences are also observed between S. shiraii and S. formosus and S. hawaiiensis regardless of maturity stage by more elongate snout (prenarial length 5.5%, 5.4%-5.6% TL vs. 4.5%-4.9% TL for S. formosus vs. 4.8%-5.1% TL for S. hawaiiensis ), first dorsal-fin height 8.1%, 7.9%-8.8% TL (vs. 9.0%-10.0% TL for S. formosus vs. 6.9%-7.7% TL for S. hawaiiensis ), second dorsal-fin anterior margin, its length 10.7%, 9.7%-11.3% TL (vs. 11.9%-12.6% TL for S. formosus vs. 6.7%-7.4% TL for S. hawaiiensis ).

Comparative material.

Squalus hawaiiensis : USNM 62450, adult female, unknown TL, Honolulu market, Oahu Island, Hawaii, USA; USNM 62467, adult female, 745 mm TL, locality same as USNM 62450. Type material of Squalus formosus : CSIRO H 6816-01 (holotype), adult male, 720 mm TL, Tashi fish Market, North-eastern Taiwan; CSIRO H 6292-10 (paratype), juvenile female, 335 mm TL, same locality as holotype.

Figures

Figure 1. Squalus shiraii sp. nov.: lateral (A-C) and ventral (D, E) views; first (F) and second (G) dorsal fins; pectoral (H) and caudal (I) fins. HUMZ 149389 (holotype), adult male, 590 mm TL (A, D, F-I); HUMZ 80329 (paratype), adult female, 770 mm TL (B); HUMZ 80330 (paratype), juvenile male, 365 mm TL (C, E). Scale bars: 50 mm (A-E); 20 mm (F-I).

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.