Squalus suckleyi (Girard, 1854)

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 suckleyi (Girard, 1854) Figs 3I, J , 6F , 7K, L , 8F ; Tables 5, 6 Spotted spiny dogfish; Northeast Pacific spiny dogfish

Acanthias vulgaris : Müller and Henle 1841: 83-84 (revision; North Pacific Ocean).

Spinax (Acanthias) suckleyi Girard 1854: 196 (original description; no types originally designated or known; Fort Steilacoom, Puget Sound, Washington State, The United States of America).

Squalus suckleyi Fowler 1941: 258-260 (description; North Pacific Ocean); Ebert et al. 2010: 22-40 (re-description, DNA barcoding, designation of neotype; North Pacific Ocean); Ward et al. 2007: 119 (cited; North Pacific Ocean); Naylor et al. 2012: 57 (DNA barcoding; North Pacific Ocean); Orlov et al. 2012: 1-12 (life history; North Pacific Ocean); Ebert et al. 2013: 78, 95 (cited, description; Northeast Pacific Ocean).

Squalus acanthias : Bigelow and Schroeder 1957: 30 (revision; Northwest Pacific Ocean); Jones and Geen 1976: 2500-2506 (taxonomy; North Pacific Ocean); Ward et al. 2007: 118-130 (DNA barcoding; North Pacific Ocean).

Squalus acanthias suckleyi : Myagkov and Kondyurin 1986: 1-18 (cited; North Pacific Ocean); Bass et al. 1976: 10 (cited; North Pacific Ocean).

Squalus wakiyae Tanaka 1917: 471-475, pl. 130, figs 368-370 (original description; illustrated; type by original designation from Watanoha, Japan; Northwest Pacific Ocean).

Squalus acanthias not Linnaeus: Zhu 1960: 107-109 (description; Northwest Pacific Ocean); Zhu and Meng 2001: 310-313 (description; Northwest Pacific Ocean); Nakabo 2002: 155 (listed; Japan); Nakabo 2013: 194 (listed; Japan); Shinohara et al. 2014: 233 (listed; Northwest Pacific Ocean); Dyldin 2015: 56-57 (listed; Northwest Pacific Ocean).

Type material.

CAS 227267, adult male, 674 mm TL, Hood Canal, Puget Sound, Washington State, The United States of America, 47°22'N, 123°05'E, 30 m depth. Collected on 3 August 2007. Neotype designated in Ebert et al. (2010).

Additional material.

HUMZ 75718, juvenile female, 500 mm TL, Usujiri, Mimamikayakabie, Hokkaido, Japan; HUMZ 81094, adult female, 565 mm TL, Usujiri, Mimamikayakabie, Hokkaido, Japan; HUMZ 87733, juvenile male, 495 mm TL, off Shiretoko, Hokkaido, Japan; HUMZ 87752, juvenile female, 455 mm TL, off Muroran, Hokkaido, Japan; HUMZ 90963, adult female, 784 mm TL, Notori Misaki oki, Japan; HUMZ 107865, juvenile female, 465 mm TL, off Sekinai, Kumaishi, Hokkaido, Japan; HUMZ 107869, adult female, 650 mm TL, off Sekinai, Kumaishi, Hokkaido, Japan; HUMZ 123859, adult male, 815 mm TL, north Japan, 44°00.1'N, 155°00.1'E; NSMT-P 10540, adult female, 625 mm TL, Northern Japan, Japan; NSMT-P 42569, adult male, 597 mm TL, unknown locality; NSMT-P 61090, adult female, 915 mm TL, Northern Japan, Japan; NSMT-P 74887, juvenile male, 445 mm TL, Northern Japan, Japan; NSMT-P 77186, adult male, 835 mm TL, unknown locality; NSMT-P 79501, adult male, 740 mm TL, Northern Japan, Japan; NSMT-P 92640, adult female, 740 mm TL, Northern Japan, Japan; ZUMT 3231, neonate male, 272 mm TL, Nagasaki, Japan; ZUMT 4684, neonate male, 265 mm TL, Tokyo Fish Market, Tokyo, Japan; ZUMT 4685, neonate female, 270 mm TL, Tokyo Fish Market, Tokyo, Japan; ZUMT 10536, neonate female, 120 mm TL; ZUMT 10789, neonate female, 238 mm TL, Hokkaido, Japan; ZUMT 36806, neonate female, 202 mm TL, Sakhalin Island, Russia; ZUMT 36807, neonate female, 200 mm TL, Sakuharin, Japan; ZUMT 36825, neonate female, 202 mm TL, Sakhalin Island, Russia; ZUMT 36836, neonate female, 202 mm TL, Sakuharin, Japan; ZUMT 40117, neonate male, 257 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 41539, neonate male, 284 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 45801, neonate male, 270 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46116, neonate male, 284 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46123, neonate male, 254 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46124, neonate male, 288 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46151, neonate male, 272 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46670, neonate male, 258 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46671, neonate female, 250 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46672, neonate male, 230 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46673, neonate female, 260 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46674, neonate male, 270 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 46675, neonate male, 245 mm TL, Uozu, Toyama Prefecture, Japan; ZUMT 51256, neonate female, 165 mm TL, East China Sea.

Diagnosis.

A large-sized Squalus species (650-952 mm maximum TL in adults) that can be differentiated from all its congeners (except S. acanthias ) and including the Japanese species by: presence of rows of white spots dorsally on each side of the body (vs. absence of white spots) (Fig. 6F ); anterior nasal flap unilobed (vs. bi-lobed); first dorsal fin origin located conspicuously behind the vertical line traced at pectoral-fin free rear tips (vs. first dorsal fin origin located before the vertical line); dermal denticles arrow-shaped (Fig. 7K, L ) (vs. denticles rhomboid or lanceolate). It is further distinguished from the Japanese species by: shorter distance between pelvic and caudal fins 20.7%-22.6% TL, except with S. acutirostris (vs. 25.5%-27.3% TL for S. shiraii vs. 23.7%-27.0% TL for S. mitsukurii vs. 26.4%-28.0% TL for S. japonicus vs. 24.6%-29.4% TL for S. brevirostris ); small first dorsal fin (except for S. japonicus ), its length 11.7%-12.4% TL (vs. 12.6%-13.4% TL for S. shiraii vs. 12.7%-14.9% TL for S. mitsukurii vs. 12.3%-13.6% TL for S. japonicus vs. 13.0%-14.7% TL for S. brevirostris vs. 14.1%-15.0% TL for S. acutirostris ); lower dorsal fins with first dorsal fin height 5.9%-6.7% TL, except with S. japonicus and S. acutirostris (vs. 7.9%-8.2% TL for S. shiraii vs. 6.9%-9.8% TL for S. mitsukurii vs. 7.3%-8.2% TL for S. brevirostris ) and second dorsal fin height 3.6%-4.9% TL (except for S. mitsukurii and S. acutirostris ) (vs. 5.6%-5.9% TL for S. shiraii vs. 5.4%-6.5% TL for S. japonicus vs. 5.7%-6.9% TL for S. brevirostris ); conspicuously smaller dorsal-fin spines with first dorsal-fin spine length 1.0%-2.0% TL (vs. 3.6%-4.3% TL for S. shiraii vs. 3.1%-5.4% TL for S. mitsukurii vs. 3.0%-3.8% TL for S. japonicus vs. 3.1%-4.2% TL for S. brevirostris vs. 2.7%-2.8% TL for S. acutirostris ) and second dorsal-fin spine 1.9%-3.2% TL, except with S. acutirostris (4.3%-5.1% TL for S. shiraii vs. 3.4%-5.3% TL for S. mitsukurii vs. 4.7%-5.6%TL for S. japonicus vs. 4.6%-6.6% TL for S. brevirostris ). It also has smaller interdorsal space 19.2%-22.1% TL than from S. shiraii sp. nov. (23.8%-25.7% TL), S. japonicus (22.5%-24.8% TL) and S. brevirostris (23.3%-27.2% TL) and S. acutirostris (24.6%-28.3% TL) and more elongate pre-first dorsal length 32.6%-34.8% TL than S. shiraii sp. nov. (29.9%-31.2% TL), S. mitsukurii (28.3%-32.4% TL), S. brevirostris (28.9%-31.7% TL, and S. acutirostris (31.8%-32.3% TL). It is further separated from its regional congeners by smaller number of precaudal (71-73) and diplospondylous vertebrae (58-62) (vs. larger number of vertebrae for S. shiraii sp. nov. 91-94 and 72-77 vs. 86-90 and 70-72 for S. mitsukurii vs. 80-88 and 65-75 for S. japonicus , vs. 78-89 and 66-72 for S. brevirostris ).

Geographical distribution.

This species is found in temperate and adjacent Arctic waters of the North Pacific Ocean from Washington state and California, USA to Canada (east side) and South Korea to Russia (west side) ( Veríssimo et al. 2010; Lee et al. 2016; Dyldin and Orlov 2018). In Japan, reports are from Hokaiddo, Notori Misaki oki and Uozu as well as Tokyo from where specimens were obtained in the local fish market. It occurs more commonly in temperate waters of Northern Japan (Fig. 8E ).

Remarks.

Molecular genetic data has supported the taxonomic separation between the morphologically similar species S. acanthias Linnaeus, 1758, that bears circumglobal distribution and S. suckleyi (e.g. Ward et al. 2007; Veríssimo et al. 2010; Ebert et al. 2010; Naylor et al. 2012; Lee et al. 2016). The latter species is a regional endemic to the North Pacific Ocean with distribution ranging from Korea to Japan (western side) and from California to Canada (east side). Morphological separation between these two species is still unreliable as no efficient diagnostic features were provided as yet. Lindberg and Legeza (1956) suggested that the ratio pelvic-fin midpoint to first dorsal-fin insertion (PDI) and pelvic-fin midpoint to second dorsal-fin insertion (PDO) comprise diagnostic characters as well as the first dorsal-fin midpoint to pectoral-fin insertion (DPI) and first dorsal-fin midpoint to pelvic-fin origin ( Ebert et al. 2010); however, these parameters are subject to bias due to the midpoint definition that relies on subjectivity. Squamation , colouration and vertebral counts, however, separate S. acanthias and S. suckleyi (Table 6 ). The latter species exhibits dermal denticles with a median ridge forming an acute angle or right angle when perpendicular to the body axis (vs. in parallel for S. acanthias ). It is easily distinguished from S. acanthias by having body conspicuously dark grey dorsally with very few white spots distributed dorsally in a single row on each side of the body (vs. light grey body with many white spots in two rows). Specimens of S. suckleyi from Japan are also distinct from S. acanthias occurring elsewhere by having smaller number of vertebrae (monospondylous, diplospondylous, precaudal and total vertebrae; see Springer & Garrick, 1964 for S. acanthias ), corroborating Ebert et al. (2010).

Additional characteristics of S. suckleyi include: dermal denticles arrow-shaped and unicuspid, small and not imbricated with a single ridge (lateral ridges absent); ridge very prominent, narrower distally than proximally with furrow anterior and profound; ridge very tall and convex, forming 45 degrees angle with horizontal axis of the body; crown base strongly broad and diamond-like with four prominent pedicels; dermal denticles conspicuously expanded laterally at the crown (Fig. 7K, L ). A single adult male shows few dermal denticles with weak lateral cusps, although lateral ridges are still absent. Colouration of Japanese specimens consists of body dark grey dorsally with very few and inconspicuous white spots (1-6 pairs), rounded, distributed symmetrically in a single row on each side and laterally at the body; white spots commonly absent in some large specimens, although clearly evident in young juveniles; white to greyish-white ventrally. Both dorsal fins grey, brownish in the apex, slightly darker from the apex tip to the midline of the posterior margin, white distally at posterior margin and free rear tips; fin base slightly white; dorsal spines dark brown, white at the tip. Pectoral fins dark grey dorsally and ventrally with white posterior margin, although not uniform. Pelvic fins also dark grey with posterior and inner margins slightly white. Caudal fin grey, darker at the tip of the dorsal lobe and in the lower caudal lobe, white over vertebral column; proximal end of dorsal caudal margin white; postventral caudal margins narrowly white; preventral caudal margin slightly white; black caudal stripe conspicuous above vertebral column.

Variations of diet and reproduction, as well as migration pattern, spatial distribution and size composition, were noticed in populations of S. suckleyi between the East and West sides of the North Pacific Ocean ( Orlov et al. 2012 a,b; Yano et al. 2017), suggesting that this species may comprise more than one fishing stock rather than a single one as supported in Ebert et al. (2010). In contrast to S. acanthias , this species has low migration movements and usually inhabits the pelagic zones up to 200 m depth with two possibly distinct populations observed throughout the North Pacific Ocean ( Yano et al. 2017). Emperor Seamout Chain works as a biogeographic barrier between the East and West sides whose belt-shaped pelagic zone exhibits low probability of presence of S. suckleyi , according to Yano et al. (2017).

A single nominal species of spotted spiny dogfish, Squalus wakiyae Tanaka, 1917, was described from the North-western Pacific Ocean and it has been placed under synonymy with S. acanthias and S. suckleyi in Fowler (1941), White et al. (2007c), Ebert et al. (2010) and the present study, as no apparent differences in morphology and genetic data are noticed between the west and east populations of S. suckleyi . Morphometric variations, however, are noticed when comparing the neotype (taken from Ebert et al. 2010) to specimens from off Japan and Russia: greater prepelvic length than in specimens from the NWPO (51.5% TL for neotype vs. 47.2%-50.6% TL); greater pre-vent length (54.9% TL vs. 50.1%-53.6% TL); narrower mouth (6.2% TL vs. 6.9%-8.2% TL); lower head height (6.5% TL vs. 7.8%-10.6% TL); pectoral fin broader at the base (6.4% TL vs. 3.5%-4.9% TL); lower second dorsal fin in S. suckleyi (3.0% TL vs. 3.6%-5.0% TL). A larger number of comparative representatives are required to re-evaluate these variations between populations of S. suckleyi and should include additional characteristics, such as dentition and vertebral counts.

Comparative material.

S. acanthias : BMNH 1879.10.9.64, adult female, 620 mm TL, off east coast, The United States of America; BMNH 1929.10.20.1, adult female, 875 mm TL, United Kingdom; BMNH 1931.4.27.2, adult female, 800 mm TL, United Kingdom; BMNH 1936.8.26.17, adult male, 635 mm TL, near Strait of Magellan, Argentina; BMNH 1950.7.26.2, juvenile female, 570 mm TL, Republic of Ireland; BMNH 1976.7.30.20, juvenile female, 523 mm TL, France, Mediterranean Sea; BMNH 1999.5.4.4, juvenile male, 550 mm TL, Falkland Islands; NMW 50119, adult female, 910 mm TL, Dalmatien, Croatia; NMW 59659, juvenile male, 345 mm TL, The North Sea; CSIRO H 2921-01, adult female, 605 mm TL, upper Pitt Water, near Shark Point, Tasmania, Australia; NMW 84781, juvenile female, 525 mm TL, Trieste, Italy; NSMT-P 41928, adult female, 715 mm TL, Atlantic Ocean; HUMZ 151302, juvenile male, 520 mm TL, off Namibia; HUMZ 30295, adult male, 660 mm TL, off Patagonia, Argentina; HUMZ 65447, adult male, 755 mm TL, New Zealand; SAIAB 21877, juvenile male, 590 mm TL, Cape Columbine, South Africa; SAIAB 25317, adult male, 640 mm TL, west coast of South Africa.

Figures

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 6. Squalus acutirostris (A-E): HUMZ 74990, juvenile female, 536 mm TL in lateral (A) and ventral (B) views; first (C) and second (D) dorsal fins and caudal fin (E). S. suckleyi in lateral view (F): HUMZ 90963, adult female, 784 mm TL. Scale bars: 50 mm (A, B, F); 20 mm (C-E).

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.