Squalus suckleyi ( Girard, 1854 )

Ebert, David A., White, William T., Goldman, Kenneth J., Compagno, Leonard J. V., Daly, Toby S., Engel, - & Ward, Robert D., 2010, Resurrection and redescription of Squalus suckleyi (Girard, 1854) from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae), Zootaxa 2612, pp. 22-40 : 28-34

Squalus suckleyi ( Girard, 1854)

Spotted spiny dogfish

Fig. 1 ; Table 2

Spinax (Acanthias) suckleyi Girard, 1854 : p. 196. “Specimens about twenty nine inches long.” ( Girard, 1854) from Fort Steilacomb, Puget Sound, Washington Territory, United States of America.

Acanthias suckleyi : Suckley, 1860: p. 367.

Acanthias sucklii : Girard, 1858: p. 368.

Acanthias vulgaris: Bleeker, 1853: p. 21; Ishikawa & Matsuura, 1897: p. 61.

Squalus acanthias : Jordan & Gilbert, 1881: p. 458; Jordan & Gilbert, 1883: p. 17; Schmidt, 1904: p. 287; Pavlenko, 1910: p. 11; Berg, 1911: p. 71; Soldatov & Lindberg, 1930: p. 16; Bigelow & Schroeder, 1934: p. 17, fig. 16; Roedel & Ripley, 1950: p. 27, 61, fig. 45; Herald & Ripley, 1951: 321–322; Roedel, 1953: p. 23, fig. 20; Okada, 1955: p. 21, fig.; Roedel, 1962: p. 22; Jensen, 1966: p. 527–554, fig. 1; Ueno, 1971: p. 69; Ketchen, 1972: 1717; Miller & Lea, 1972: pp. 34, 38, fig.; Hart, 1973: pp. 44–47, fig.; Ketchen, 1975: 43; Anderson et al., 1979: 257; Hubbs et al., 1979: p. 3; Castro, 1983: p. 55, fig.; Eschmeyer et al., 1983: p. 23, pl. 2; Masuda et al., 1984: p. 9, pl. 10–G; Ketchen, 1986: p. 1–88, fig. 1; Amaoka et al., 1989: p. 256.; Orlov, 1998: tab. 2; Mecklenburg et al., 2002: p. 88, fig.; Nakabo, 2002: p. 155; Ebert, 2003: p. 63–66, fig.; Tok, 2004: tab. 2, p. 132; Compagno et al., 2005: p. 73, plate 3; Stevenson et al., 2007: 20

Squalus mitsukurii: Tanaka, 1908 : p. 236; Tanaka, 1917: pp. 471–474, pl. 130 (368, 369, 370); Jordan & Metz, 1913: p. 4, fig. 2.

Squalus suckleyi : Jordan & Hubbs, 1925: 105; Fang & Wang, 1932: p. 246; Walford, 1935: p. 42, fig. 40; Schultz, 1936: p. 131; Clemens & Wilby, 1946: p. 59, fig. 19; Mori, 1952: p. 22; Clemens & Wilby, 1961: p. 81, fig.22.

Squalus sucklii: Gill, 1862 : p. 499; Jordan & Starks, 1895: p. 789; Jordan & Evermann, 1896: p. 54; Jordan & Gilbert, 1899: p. 434; Evermann & Goldsborough, 1907: p. 228; Starks & Morris, 1907: p. 168; Garman, 1913: pp. 194–195; Halkett, 1913: p. 41; Starks, 1917: p. 152, fig. 62; Daniel, 1934: pp. 37, 154, fig. 147.

Squalus wakiyae: Tanaka, 1918 : p. 475.

Neotype. CAS 227267, adult male 674 mm TL, Hood Canal, Puget Sound, Washington, USA, 30 m depth, 47°22′ N, 123° 0 5′ W, 55 m, 0 3 August 2007.

Other material. 11 specimens. CAS 227268, adult male 760 mm TL, CAS 227269, adult male 691 mm TL, CAS 227270, adult male 703 mm TL, CAS 227271, adult male 805 mm TL, CAS 227272, adult male 725 mm TL, Central/South Puget Sound, Washington, USA, 15 m depth, 47°22′ N, 122°24′ W, 110 m, 28 September 2007; CAS 227273, adult male 707 mm TL, North Puget Sound, Washington, USA, 2007; CAS 21424, male 380 mm TL, San Francisco Bay, California; CAS 25319, female 213 mm TL, Puget Sound, Washington State, USA; DAE 990624–01, male 360 mm TL, Monterey Bay, California, USA; DAE 990624– 0 2, female 316 mm TL, Monterey Bay, California, USA; DAE 990624–03, female 332 mm TL, Monterey Bay, California, USA.

Diagnosis. A large-sized, slender bodied Squalus with the following combination of characters: body slender, trunk height 10.8 (8.3–12.0)% TL; snout rounded, somewhat blunted at apex, relatively short, prenarial length 1.4 (1.3–1.5) times mouth width, preoral length 2.0 (2.1) times prenarial length, 9.1 (8.6– 9.5)% TL; eye moderate-sized, length 3.8 (3.2–3.9)% TL; anterior nasal flap simple, secondary lobe absent; dorsal fins small, raked; first dorsal originates just posterior to free-rear tip of pectoral fin, first dorsal-fin spine moderate, relatively narrow-based; pectoral fin lobe-like, not or weakly falcate; flank denticles broadly unicuspidate to weakly tricuspidate; adult maximum size at least 1300 mm TL.

Description. Body fusiform, slender, nape somewhat humped; deepest near first dorsal-fin spine, maximum trunk height equal to trunk width; head short 23.0 (21.1–23.0)% TL; dorsal–caudal space, 11.1 (10.7–11.6)% TL. Head somewhat broad, its width 1.0 (1.0–1.1) times trunk width; depressed forward of spiracles, becoming somewhat subtriangular towards pectoral-fin origin; length 3.8 (3.6–3.9) in pre-vent length; height 0.6 times width. Snout relatively short, rounded, somewhat blunted at apex; prenarial length 1.4 (1.3–1.5) times mouth width, prenarial length 1.2 (1.2–1.3) times eye length, 0.6 times interorbital space; prenarial length 2.0 (2.1–2.1) in preoral length.

Eye oval, moderate-sized, length 3.8 (4.1–4.4) in head, 2.3 (1.7–2.2) times its height; strongly notched posteriorly. Spiracle moderate-sized, broadly crescentic, with a shallow lobe-like fold on posterior margin, and about equidistant between snout tip and pectoral-fin origin, 0.5; greatest diameter nearly equidistant to eye-spiracle length. Gill slits directed slightly anterodorsally from bottom to top; first four near equal in size, fifth slightly longer, height of fifth slit 2.2 (2.0–2.6)% TL. Mouth almost transverse, upper jaw weakly concave, width 1.4 (1.4–1.6) in preoral length; upper labial furrows about 1.6 (1.2–1.7) times length of lower furrows; prominent postoral groove, subequal in length to upper labial furrows, extending posterolaterally from angle of jaws. Teeth oblique, bladelike, and similar in upper and lower jaws; upper teeth unicuspid, interlocking, blade-like, cusps directed strongly laterally, low; tooth base broader than length of its cusp; two series of functional teeth in upper jaw, three (sometimes two) series in lower jaw; teeth in upper jaw (range from left to right including median tooth if present) (13–15) – (0–1) – (12–14), total upper tooth counts range from 26–29; lower jaw (11–14) – (9–13), total lower tooth counts range from 20–27. Nostrils small, almost transverse; anterior nasal flap single lobed; lobe broadly triangular and somewhat flattened; internarial space 2.3 (2.3–2.5) in preoral length, 3.5 (3.4–3.5) times nostril length.

Dermal denticles on flank below first dorsal fin very small, loosely spaced and non-imbricate; crowns elevated, quadrate, broadly unicuspidate with pronounced median ridge; median ridge commencing anterior of rest of crown, with a mesial furrow developing anteriorly and converging rapidly towards posterior tip of crown; posterior portion of cusp strongly produced, pungent; lateral portion of crown very short; denticles mostly unicuspidate with some weakly tricuspidate.

First dorsal fin small, raked, broadly rounded apically; anterior margin relatively straight; upper posterior margin almost straight, not vertical, instead directed very slightly anterodorsally from bottom to top, very weakly concave near free rear tip; free rear tip very thick basally, short; inner margin of fin almost straight; origin posterior to free-rear tip of pectoral fins; first dorsal-fin midpoint pectoral-fin insertion closer to pectoral-fin origin than to pelvic-fin origin; fin-spine origin slightly posterior to pectoral-fin free rear tips; spine base relatively narrow, exposed anteriorly well below junction of spine and soft portion of fin; spine tapering slightly distally, anterior margin almost straight; spine shorter than exposed portion of second dorsalfin spine; pre-first dorsal length 2.9 (2.8–3.0) times in TL; first dorsal-fin length 2.0 (2.0–2.2) times its height, 1.1 (1.0–1.2) times second dorsal-fin length; first dorsal-fin height 2.0 (2.0–2.1) times second dorsal-fin height.

Second dorsal fin small, strongly raked; anterior margin moderately convex, apex broadly rounded; posterior margin moderately concave; free rear tip moderately elongate, inner margin length 1.5 (1.4–1.6) times fin height; second dorsal-fin length 3.8 (3.7–3.8) times its height; exposed spine length 1.1 (1.0–1.2) in height of fin; fin-spine origin over free rear tip of pelvic fins; exposed second spine broad-based; spine robust, acutely pointed distally, curving slightly posteriorly, tapering rapidly just above point of exposure, spine tip not extending to level of insertion of fin; interdorsal space about equidistant in prepectoral length, 1.5 (1.5– 1.8) in pre-first dorsal length; interdorsal ridge weak.

Pectoral fin moderate, anterior margin slightly greater than length, moderately convex; inner margin moderately convex, length 6.5 (5.6–7.4)% TL; apex broadly rounded, lobe-like, not or weakly falcate; posterior margin moderately concave, free rear tip broadly rounded; fin base very short, 2.5 (2.1–2.5) in length of anterior margin. Pelvic fins moderate-sized, anterior and posterior margins nearly straight, apex broadly rounded, free rear tip somewhat acute. Caudal peduncle very long, tapering slightly to caudal fin; subcircular in cross-section anteriorly, slightly depressed and broadly semicircular posteriorly; dorsal precaudal pit weakly developed, ventral pit absent; lateral keels well developed, originating below or slightly posterior to second dorsal-fin insertion, terminating just posterior to lower caudal-fin insertion; pelvic–caudal space 0.9 (0.9–1.1) in pectoral–pelvic space, 1.1 (1.0–1.2) in prepectoral length; dorsal–caudal space 2.0 (1.8– 2.0) in interdorsal length. Caudal fin relatively short, dorsal margin nearly straight, apex broadly rounded; apex of lower lobe narrowly angular; dorsal caudal margin 1.4 (1.3–1.4) in head length; length of lower caudal lobe 1.8 (1.8–1.9) in upper lobe length. Spiral valve count range from non-voucher specimens: 12–13. Vertebral count range from non-voucher specimens: 97–106.

Genetics. The average length of the COI region sequenced was 650.4 bp, with lengths ranging from 593– 652 bp (the large majority of samples were sequenced for all 652 bp of the DNA barcode region). The neighbour joining tree of K2P distances ( Figure 2 ) clearly shows separation into two clades, one comprising S. suckleyi and one comprising S. acanthias , with 98% bootstrap support for the two clades. The S. suckleyi clade included all the North Pacific specimens, from Japan and from the west coast of Canada and the United States. The S. acanthias clade included all specimens from the North Atlantic ( Iceland, the United Kingdom, and the east coast of the United States), the South Atlantic ( Uruguay and Argentina) and the South Pacific ( Chile, New Zealand and Australia). Within species genetic diversities were 0.109±0.036% and 0.176±0.041% for S. suckleyi and S. acanthias respectively. There was no evidence of spatial structuring within either clade, although the potential for structuring is limited given the low diversities. The most common haplotype in S. acanthias , the species with the higher within species diversity, is found in specimens from all localities, from Iceland to Tasmania. Between–species diversity was 5–6 fold greater at 0.765±0.307%. Within the 652 bp COI region, there were four fixed and therefore diagnostic nucleotide base substitutions between the species, all for third-base synonymous mutations. These were, S. suckleyi followed by S. acanthias , at positions 226 A–G, 406 G–A, 514 C–T and 628 G–A (all positions numbered within the 652 bp barcode region).

Coloration. Gray dorsally, with conspicuous white spots present on their flanks, becoming lighter ventrally; the fins adults and juveniles are without white edges or other prominent markings. Coloration is similar in neonates and younger juveniles except for white-edge along posterior margin of pectoral–fins, on apex and posterior margin of dorsal-fins, and along caudal–fin margins.

Distribution. Endemic to the North Pacific, from the Koreas and Japan, northward to Russia (Kamchatka, Sea of Okhotsk and Sakhalin), the Bering Sea and the Aleutian Islands, and eastwards in the Gulf of Alaska, British Columbia and Washington south to southern Baja California. In North America, S. suckleyi is extremely common off British Columbia and Washington, but decline in abundance off the Oregon and California coasts. It occurs in a wide depth range from very shallow waters in some areas down to depths of at least 1236 m ( Ebert, 2003). Squalus suckleyi appears to prefer water temperatures between 7 and 15°C, and often makes longitudinal and depth migrations to follow this temperature preference ( Ebert, 2003).

Etymology. The species name is in honor of George Suckley who collected the specimens used by Charles Girard in his original description.

Common names. North Pacific spiny dogfish, spotted spiny dogfish, or spiny dogfish.

Size and sexual maturity. Squalus suckleyi is a viviparous species with yolk-sac dependency, with litters of up to 20, but with most averaging between 2–12. Litter size and size at birth are correlated with the size of the female. Males mature between 700–800 mm total length (TL) and for females 800–1000 mm TL. Maximum size is about 1070 mm for males and at least 1300 mm for females ( Ebert, 2003).

Life history. Considerable differences exist in published vital rate estimates for Squalus acanthias ( Fordham et al., 2006) . Age and growth studies have shown large discrepancies in growth rates from different geographic locations. For example, in the northwest Atlantic Nammack et al. (1985) provided a growth coefficient (k) of 0.11 yr -1 and 0.15 yr -1 for females and males, respectively. In the North Pacific, several age and growth studies have been conducted providing growth coefficients ranging from 0.031 to 0.034 yr -1 for females and from 0.067 to 0.092 yr -1 for males ( Ketchen, 1975; Jones & Geen, 1977). Saunders & McFarlane (1993) provided a growth coefficient for Squalus acanthias (= S. suckleyi ) off British Columbia for the sexes combined of 0.044 yr -1. Growth coefficients from other geographic locations such as the Black Sea are similar to those from the North Atlantic, ranging from 0.13 to 0.17 yr -1 and 0.17 to 0.2 yr -1 for females and males, respectively ( Avsar, 2001; Demirhan & Sehyan, 2007).

Accompanying the differences in growth rates are differences in longevity and in age at first reproduction. In the northwest Atlantic the median age at maturity is 12 and six years for females and males, respectively ( Nammack et al., 1985), while median age at maturity in the North Pacific is 35.5 and 18.5 for females and males, respectively ( Saunders & McFarlane, 1993; Cindy Tribuzio, NOAA Fisheries Auke Bay Laboratory, pers. comm.).

The order of magnitude in the differences in growth rates between the North Pacific and other geographic locations around the world cannot be explained by differences in techniques or be due to a lack of validation. In fact, ages have been validated with OTC and bomb radiocarbon dating for S. suckleyi in the eastern North Pacific ( McFarlane & Beamish, 1987; McFarlane & King, 2009; Campana et al., 2006) and for S. acanthias via bomb radiocarbon in the northwest Atlantic ( Campana et al., 2006). Similarly, the significant differences at median age at maturity that accompany these different growth rates cannot be explained by differing assessment techniques.

The reason for such differences in vital rates between the North Pacific and other geographic locations has never been elucidated. Discussions have centered on potential environmental or ecosystem differences, however, no data have been brought to bear for that argument. Our data show a much more parsimonious and viable explanation for these differences; that Squalus acanthias group species in the North Pacific constitute a different species (= S. suckleyi ) than S. acanthias in other geographic locations. Tagging studies show that S. suckleyi in the North Pacific can migrate thousands of miles from British Columbia to Japan and Mexico ( McFarlane & King, 2003). This information suggests that S. suckleyi in the North Pacific are a single stock, which is supported by our genetic analysis.

Remarks. The Squalus acanthias subgroup is one of the more taxonomically problematic shark groups as its members are very similar in external appearance. Differences in external morphology between S. acanthias ( Fig. 3 ) and S. suckleyi ( Fig. 1 ) are subtle and intraspecific variations within individuals of the same maturity class are likely to mask these differences. The broad geographic ranges of these two species, particularly S. acanthias , are likely to contribute to the intraspecific variation and future research should focus on defining this variation across the known ranges. There are few external morphometric characters to separate these two nominal species, e.g. lower dorsal-fin spines, position of the first dorsal-fin spine relative to the inner rear tip of the pectoral fin. In the present study we found that S. suckleyi had a slightly shorter, more broadly–rounded to acute snout than S. acanthias which tends to have a slightly longer and more acute snout. Also, we found the following morphometric ratios to differ between S. suckleyi and S. acanthias : pelvic–fin midpoint to first dorsal-fin insertion (PDI) 14.0 (13.2–15.1)% versus 9.3 (8.7–9.8)%, pelvic-fin midpoint to second dorsal-fin insertion (PDO) 7.6 (5.0–9.1)% versus 10.0 (9.3–10.4)%, first dorsal-fin midpoint to pectoral–fin insertion (DPI) 11.2 (9.7–12.4)% versus 9.8 (9.3–10.7)%, and first dorsal-fin midpoint to pelvic–fin origin (DPO) 14.7 (12.0–15.0)% versus 12.4 (10.7–13.5)%. The DPI and DPO ratios found in the present study indicate that although there may be some overlap the first dorsal-fin midpoint is proportionally slightly more posterior to the pectoral-fin insertion and pelvic fin origin. This finding is somewhat consistent with that of Jordan & Evermann (1896), although these authors observed that the position of the first dorsal-fin spine was more posterior to the pectoral-fin. Our findings also indicate that the pelvic-fin is proportionally closer to the second dorsal-fin in S. suckleyi while in S. acanthias it is closer to the first dorsal fin. This finding is consistent with those of Bigelow & Schroeder (1957) and Garrick (1960). Jones & Geen (1976) found similar results, but concluded that these differences were due to the effects of length and sex for individual specimens.

Although most external morphological characters appeared to overlap between North Pacific and North Atlantic forms, meristic characters such as vertebral counts consistently reveal a distinct separation between these two forms. In the present study we found the total number of vertebral counts to be slightly lower in S. suckleyi (mean = 99, range = 97–106) than those found in S. acanthias (mean =112, range = 109–116); a finding consistent with other studies ( Springer & Garrick, 1964; Jones & Geen, 1976).

In this study, we designate a recently collected specimen as the neotype for Squalus suckleyi (CAS 227267). We have followed the requirements of the International Code of Zoological Nomenclature in designating the holotype. The designated neotype was collected from the type locality of Puget Sound, the syntypes are lost and not available, a detailed diagnosis and description is provided, and differences between the closest related species ( S. acanthias ) are provided. Given that the Squalus acanthias group requires further taxonomic revision, particularly the Black Sea population, the designation of a neotype for this species will be beneficial for future taxonomic work.

The results of our molecular analysis were congruent with results from other studies comparing within- and between-species diversity at CO 1 in the genus Squalus (5- 6 X difference in magnitude; Ward et al. 2005). The use of molecular tools in recent years has helped to shed light on many difficult taxonomic questions ( Hillis 1987; Avise 2004; Hauser 2009), including problematic elasmobranchs. Two North Pacific shark species, Somniosus pacificus Bigelow & Schroeder, 1944 and Lamna ditropis Hubbs & Follet, 1947 , were long thought to be synonymous with the morphologically similar, but taxonomically distinct North Atlantic species S. microcephalus ( Bloch & Schneider, 1801) and L. nasus ( Bonnaterre, 1788) , respectively ( Ebert, 2003). Interestingly, both these species were not considered to be distinct from their North Atlantic congeners until the middle of the last century while S. suckleyi had been described as distinct nearly 100 years earlier. Subsequent molecular studies have shown both S. pacificus and L. ditropis to be genetically distinct ( Naylor et al., 1997; Murray et al., 2008).

The present study is a descendant of Ward et al. (2005, 2007), which was part of a large-scale project to revise the taxonomy of the genus Squalus in the Indo-Australasian region using both morphological and molecular techniques. Despite the lack of evidence in a 1976 allozyme paper (Jones and Green), newer studies have argued for the taxonomic distinction of S. acanthias in the North Pacific based on molecular evidence ( Hauser 2009; Verissimo et al. 2010). In particular, a recent analysis of the global population structure of this species using both mitochondrial and nuclear markers recovered a unique genetic clade in the North Pacific ( Verissimo et al. 2010), results that are highly consistent with ours.

Future research on this subgroup of Squalus needs to address the conservation and management implications emanating from the results of this study. Squalus acanthias is currently listed as Vulnerable by the IUCNs Red List of Threatened Animals ( Fordham et al., 2006). The North Pacific populations included in this assessment should now be treated as a separate species, Squalus suckleyi , and should be assessed separately, while the assessment for S. acanthias should be updated to reflect this change. Current management strategies for these two species, especially in North American waters, should be revised in light of these findings.

Figures

FIGURE 1. Squalus suckleyi, neotype (CAS 227267, adult male 674 mm TL). A, Lateral view; B, Ventral view of the head.

FIGURE 2. Neighbour joining tree for COI divergences of specimens of Squalus suckleyi and S. acanthias. Kimura 2 parameter distances used and distance bar given. Bootstrap values> 70 % shown. Specimen designations as in Appendix I.

FIGURE 3. Squalus acanthias: A, Lateral view of CSIRO H 1214 (female 678 mm TL); B, Ventral view of head of CSIRO H 4876 – 01 (adult male 616 mm TL).