Squatina armata ( Philippi, 1887 )

Kraft, Sebastián, Fernández-Cisternas, Ítalo, Araya, Miguel & Concha, Francisco J., 2024, Redescription of the Chilean angel shark Squatina armata (Philippi, 1887) (Squatiniformes, Squatinidae), European Journal of Taxonomy 932, pp. 112-137 : 117-128

Squatina armata ( Philippi, 1887)

Figs 1–7 ; Table 1

Rhina armata Philippi, 1887: 561 . Type Locality: Iquique, Chile.

Common name

“Angelote” (Spanish), “Chilean angel shark” (English).

Material examined

Neotype (designated here) CHILE • ♂ (1004 mm TL, 10.01 kg); Iquique, near Playa Seremeño ; 20.483722° S, 70.162472° W; caught at approximately 20 m depth by artisanal fishers; 3 Jun. 2019; GenBank: OR544405 (CO1), OR567498 (NADH2), OR557297 (16S); MNHNCL ICT 7625 .

Other material

CHILE • 1 ♂ (1040 mm TL, 11.63 kg); same collection data as for neotype; GenBank: OR544406 (CO1), OR567499 (NADH2), OR557298 (16S); MNHNCL ICT 7626 .

CHILE • 1 ♂ (cleaned jaw, fish TL estimated at 1100 mm); Higuerillas; 32°55′47.51″ S, 71°32′19.95″ W; caught at approximately 40 m depth by artisanal fishers, only head was possible to recover; 18 Mar. 2020; CCM-1228 .

Diagnosis and comparisons

Squatina armata differs from S. californica by the following combination of characters: surface of head between orbits flat in S. armata , while concave in S. californica . Anterior margin of head concave in S. armata , while straight in S. californica . Anterior nasal flaps of S. armata relatively broad with three lobes, outer lobe concave at base with relatively long inner lobe, shorter than outer lobe, central lower margin of nasal flap weakly fringed with narrow and relatively long and straight inner barbel, with spatulated end, while anterior nasal flap simpler in S. californica , with relatively long outer margin with spatulated tip, central margin slightly fringed. Anterior margins of pectoral fins of S. armata softly sinuate, concave anteriorly to posterior margin of head, slightly convex until pectoral fin apex vs almost straight to softly convex in S. californica . Row of medial-dorsal thorns absent in S. armata , single small medial-dorsal thorn right anterior to pelvic girdle, with single row of 30 small central-caudal thorns, not reaching origin of first dorsal fin and five interdorsal thorns, while medial-dorsal, caudal, and interdorsal thorns absent in S. californica . Pectoral thorns form broad patch near pectoral fin apex in adult males of S. armata , while absent in S. californica . Squatina armata has slightly shorter pre-dorsal length (63.1% vs 66.6%, respectively), shorter head width (23.5% vs 25%, respectively), and shorter pectoral fin length (22.1% vs 33.3% TL, respectively). First dorsal fin insertion at 66.6% of TL in S. californica , while at 63.1% TL in S. armata . In S. californica , pre-orbital length equal to first dorsal fin base length, while in S. armata somewhat shorter (3.6% vs 4.2% TL, respectively). First dorsal fin height equal to interorbital distance in S. californica , while larger in S. armata (7.2% vs 9.7% TL, respectively). Colouration of dorsal surface of body in S. armata is brownish, with small white spots and larger darker spots, while is greyish ash dorsally with small whitish spots in S. californica . In the original description of S. californica , there is no mention of any conspicuous spinulation pattern on pectoral fins or head, but prominent in S. armata .

Squatina armata has softly sinuate pectoral fin anterior margins, while in S. argentina this margin is convex and in S. david , S. dumeril , S. guggenheim , S. occulta and S. varii it is straight or slightly convex. Squatina armata has enlarged dorsal thorns organized in one discontinuous line: one medial-dorsal thorn anterior to pelvic girdle; 30 caudal thorns and 5 interdorsal thorns, while S. argentina has dorsal mid-line denticles that are morphologically similar to other trunk denticles and barely organized in a row; S. david lacks enlarged thorns on dorsal mid-line; S. guggenheim has a single row (or multiple in juveniles) over dorsal mid-line, from mid-length of pectoral fin base to origin of first dorsal fin or of caudal fin.

Squatina armata has four pairs of enlarged dermal denticle patches on the head: one first dorsal to the internarial space; one on the pre-orbital area; one on the eye-spiracle space; and one on the interspiracle space; S. argentina has no enlarged denticles on the interspiracular surface; S. david has moderate tubercles above the mouth and eye crests, a smooth oval patch above the mid-point of the mouth in between the eyes; S. dumeril has two clusters on the snout, one anterior and another posterior to the eyes, and a pair of clusters of denticles between the spiracles; S. guggenheim and S. occulta have a pair of enlarged, conical, and morphologically distinct dermal denticles between the spiracles.

Tooth count corresponded to 9–9/10– 10 in Squatina armata , 12–12/12– 12 in S. argentina , and 10– 10/10– 10 in S. david . Squatina armata has a lower vertebrae count (n = 129) than S. argentina (n = 132–136), S. david (135–142), S. dumeril (130–135), and S. varii (n = 138–150).

Squatina armata differs from Squatina argentina , S. dumeril , S. guggenheim and S. varii by having a wider head (23.3–23.5% vs 16.5–19.4% in S. argentina , 16.3–17.4% in S. dumeril , 10.4–21.7% in S. guggenheim , and 16.9–19.2% in S. varii ), and by having a greater width at the pectoral fin origins (17.7–17.8% vs 13.7–15.7% in S. argentina , 13.1–14.2% in S. dumeril , 12.2–16.6% in S. guggenheim and 14.4–15.1% in S. varii ). From S. argentina , S. david , S. dumeril and S. occulta , S. armata differs by having a longer first dorsal fin anterior margin (10.0–10.3% vs 7.5–8.0% in S. argentina , 7.1–8.8% in S. david , 6.4–7.9% in S. dumeril , and 6.7–9.2% in S. occulta ), and by having a larger second dorsal fin anterior margin (9.3–9.4% vs 6.8–7.7% in S. argentina , 7.1–8.3% in S. david , 6.0–7.6% in S. dumeril , and 6.8–8.6% in S. occulta ).

Squatina armata has a shorter pectoral fin length (22.1–23.5%) than S. argentina (32.4–36.7%), S. david (32.7–35.7%), S. guggenheim (27.1–33.6%), S. occulta (26.7–36.6%), and S. varii (33.5–36.0%). Squatina armata has a shorter pelvic fin width (11.2%) than S. argentina (13.0–14.2%), S. david (12.9– 14.4%), S. dumeril (13.1–13.3%), and S. varii (13.8–16.2%). Squatina armata has a greater first dorsal fin height (7.2–7.8%) than S. argentina (4.7–5.6%), S. dumeril (3.3–3.8%), S. guggenheim (2.8–6.4%), and S. occulta (3.3–6.1%). Squatina armata has a shorter pectoral fin inner margin (11.5–11.9%) than S. argentina (17.1–19.8%), S. occulta (13.3–18.9%), and S. varii (17.5–19.4%), but longer than S. david (6.1–8.2%).

Squatina armata differs from S. david , S. dumeril and S. varii by having a greater interorbital distance (9.7–9.8% vs 7.6–8.9% in S. david , 7.7–8.3% in S. dumeril , and 7.8–8.8% in S. varii ), and by having a greater trunk width (22.7–23.3% vs 15.3–19.4% in S. david , 15.3–16.5% in S. dumeril and 16.0–18.2% in S. varii ). From S. argentina , S. occulta , and S. varii , S. armata differs by having a shorter eye length (1.3–1.4% vs 2.3–2.9% in S. argentina and 1.6–3.1% in S. occulta , and 1.5–2.1% in S. varii ) and by having a greater intergill width (11.6% vs 8.2–9.8% in S. argentina , 7.5–10.2% in S. occulta , and 7.9– 10.0% in S. varii ).

Squatina armata has a wider clasper base (2.3–2.5%) than S. argentina (0.8–1.0%), S. dumeril (1.6%), and S. occulta (0.7–1.4%). Squatina armata has a greater second dorsal fin height (6.5–7.3%) than S. argentina (4.0–5.1%), S. dumeril (3.5%), and S. guggenheim (3.2–5.9%). Squatina armata has a shorter dorsal-caudal distance (5.8–6.4%) than S. argentina (7.1–8.5%), S. dumeril (7.3–8.0%), S. occulta (6.2–9.0%), and S. varii (6.9–7.5%).

Squatina armata differs from S. dumeril and S. varii by having a wider mouth (14.0–15.1% vs 10.3– 11.9% in S. dumeril and 11.5–13.0% in S. varii ), and by having a longer pelvic fin length (22.1–22.5% vs 17.9–20.9% in S. dumeril and shorter than S. varii (25.9–28.6%). Compared to S. argentina and S. occulta , S. armata differs by having a greater clasper inner length (20.7–21.6% vs 10.7–10.8% in S. argentina and 8.5–13.6% in S. occulta ), and by having a greater cloacal-caudal length (55.2–56.4% vs 49.2–51.8% in S. argentina and 47.8–53.7% in S. occulta ). Compared to S. david and S. varii , S. armata differs by having a shorter pectoral fin anterior margin (24.9–25.1% vs 27.3–29.4% in S. david and 28.9–30.9% in S. varii ), and by having a shorter second dorsal fin inner length (1.8–2.0% vs 2.6–3.2% in S. david and 2.7–3.2% in S. varii ). Squatina armata has a greater pre-ocular length (6.4–6.5%) than S. argentina (4.4–5.9%) and S. dumeril (5.0–5.7%). Squatina armata has a greater pectoral fin base length (11.5–12.7%) than S. david (8.7–10.9%) and S. dumeril (9.1–10.6%).

Squatina armata has a greater snout-cloacal length (43.3–43.9%), shorter eye height (1%) and shorter pre-spiracular length than S. argentina (48.5–51.5%, 1.3–1.9%, 8.4–9.5%). Squatina armata has a greater spiracle width than S. david (2.1–2.3% vs 0.9–1.2%), a greater pectoral fin posterior margin (20–20.2% vs 12.7–15.9), greater second dorsal fin posterior margin (6.7–7.1% vs 3.3–5.2%) and greater nostril width (1.8–1.9% vs 0.4–0.9%). Squatina armata has a greater orbital head width than S. dumeril (14.1–16.9% vs 11.8–11.9%), as well as a greater dorsal caudal fin margin (12.5–13.1% vs 10.1%), greater internarinal distance (7.0–7.4% vs 5.7–6.0%) and greater pectoral fin width (19.6% vs 14.2–15.7%), while having shorter pre-caudal length than S. dumeril (83.5–85.0% vs 89.3–91.0%), shorter pre-pectoral length (18.0–18.9% vs 22.5–22.7%), shorter pre-pelvic length (36.1–39.0% vs 41.3–44.7%), shorter pelvic (origin)-caudal distance (45.4–44.9% vs 49.7%), shorter interdorsal distance (6.1–6.6% vs 7.0–7.4%), shorter eye-spiracle length (2.5–2.6% vs 3.6–3.7%) and a shorter intergill length (2.8–2.9% vs 3.9%). Morphometric data on S. armata and other South American angel sharks are summarized in Table 1.

Redescription

Morphological measurements of the neotype and complete voucher specimen are summarized in Table 1. The following description is based on the neotype.

COLOURATION. Dorsal surface of body of fresh specimen dark greyish brown, with pairs of prominent, relatively large dark ocelli located on trunk near anterior insertion of pelvic fins, posterior apex of pectoral fins, and tail; white spots on dorsal surface of body, small, scattered. Ventral surface whitish; ventral margins of pectoral fins brownish ( Fig. 1 ). After preservation, the dorsal surface was opaque grey, and the ventral surface was the same as in the fresh specimen.

BODY. Dorsoventrally depressed from head to caudal fin origin.

HEAD. Broad and dorsoventrally depressed; head width about 23.5% of TL, 1.49 times head length (HL). Eyes relatively small, elliptical in shape, positioned dorsolaterally; eye length (EL) 1.3% of TL; eye height (EH) 1.0% of TL; distance between orbits 9.7% of TL, 7.69 times EL. Spiracle length 1.95 times EL. Mouth large, broadly arched, 24.5% of TL, 2.52 times interorbital space; upper labial furrows partially covered by dermal folds; anterior nasal flaps forming semi-oval arch. Nasal aperture presents a posterior nasal flap composed of a single elongated lobe and a relatively broad anterior nasal flap, width 3.5 times the upper lip arch width, composed of an elongated barbel and a broad, low, indented median barbel and a posterior barbel ( Fig. 2 ).

PECTORAL FINS. Large; not fused with head; origin behind 5 th gill slit, length 22.1% of TL, length 1.13 times pectoral fin width; anterior margin of pectoral fins softly sinuate; posterior margin of pectoral fins slightly concave; free rear tip of pectoral fins rounded; pectoral fin base 1.05 times pelvic fin base.

PELVIC AND CAUDAL FINS. Relatively large, triangular, with straight margins; pelvic fins length 22.5% of TL, 2.0 times pelvic fin height. Dorsal fins small, trapezoidal in shape; dorsal fin apex and free rear tip rounded; anterior margin of dorsal fins slightly convex; posterior margin of dorsal fins straight, vertically oriented; interdorsal space 6.1% of TL, 1.05 times dorsal caudal fin margin; second dorsal fin slightly smaller than first dorsal fin. Caudal fin hypocercal, with slightly convex dorsal and pre-ventral margins; lower postventral margin of caudal fin 1.14 times as long as posterior margin; upper post-ventral caudal margin slightly convex; lower postventral caudal margin straight; posterior and ventral tips rounded.

VERTEBRAE AND FIN RADIALS. Total vertebrae count 129; 98 pre-caudal vertebrae; 31 caudal vertebrae. Left pectoral fin with 37 radials and pelvic fins with 30 radials (Supp. file 1.2).

DERMAL DENTICLES AND SPINULATION. Dermal denticles densely covering most of the dorsal surface of the body, absent only on anterior tip of pectoral fins, anterior and posterior insertion of pectoral fins, base and insertion of dorsal fins, insertion of pelvic fins, and dorsal surface of claspers. Dermal denticles on the head ( Fig. 3a ), medial dorsal, and caudal area small ( Figs 3–4 ), with posteriorly oriented conical crowns and four to five longitudinal ridges not reaching the crown apex ( Fig. 4 ). Enlarged denticles with variable crown shapes forming four oval pairs of patches on head: some crowns in the patches blunt, some conical, and others thorn-like, being either postero- or latero-dorsally oriented ( Fig. 3a ); first pair of thorn-like enlarged dermal denticle patches dorsal to internarial space; second patch on pre-orbital area; third patch on eye-spiracle space; and fourth pair on interspiracle space ( Fig. 3a ). A single patch of thorn-like enlarged dermal denticles on apex of each pectoral fin; pectoral fin thorns hook-shaped, posteromedially oriented ( Fig. 3b–c ), lacking ridges, similar in size. A total of 36 thorn-like enlarged dermal denticles forming a single longitudinal row on dorsal surface, of similar size (1.5 mm), lacking longitudinal ridges ( Figs 3d , 4e ): one medial-dorsal thorn, anterior to pelvic girdle; 30 caudal thorns forming a single row; 5 interdorsal thorns forming a single row. Dermal denticles scarce on ventral surface of body. Ventral dermal denticles, small, flattened, with rounded crowns lacking longitudinal ridges, forming patches covering external margins of pectoral and pelvic fins ( Fig. 4g ), scattered near cloaca, forming a narrow patch on each clasper, covering ventral surface of caudal peduncle except for its anterior portion.

DENTITION ( Fig. 5 ). Tooth count 9– 9 in upper jaw, 10– 10 in lower jaw; symphysial teeth absent. Teeth with a single cusp, not serrated; cusps relatively short, lingually bent, drop-shaped; labial face of cusps convex, rounded near base; crown foot broad, projecting laterally on first three series from symphysis on upper teeth, breaking to form a right angle, projecting laterally in the remaining series; roots short, wide, merging from lateral projections of crown feet.

CLASPER EXTERNAL MORPHOLOGY ( Fig. 6a ). Clasper elongated, flattened ventrally, convex dorsally, broad at base, pointed to tip, extending posteriorly less than one-third of clasper inner length beyond pelvic free rear tip. Clasper groove elongated, oblique anteriorly to reach dorsal mid-line of clasper, straight on middle, oblique distally; apopyle visible dorsally; globular cartilaginous rod conspicuous along clasper groove, reaching anterior margin of clasper glans; hypopyle anterior on clasper glans, anterior to rhipidion; rhipidion terminal, elongated, flap-like, projecting laterally from hypopyle to base of cover rhipidion, partially covering dorsal surface of glans. Pseudopera not found near hypopyle on clasper glans; cover rhipidion flap-like, relatively thick, well developed, narrow, width about one-fourth of clasper width at pelvic fin free rear tip, positioned terminally on clasper glans. Pseudosiphon absent.

CLASPER SKELETON ( Fig. 6b–c ). Clasper components surrounding axial cartilage.Axial cartilage elongated, slightly flattened. Dorsal terminal cartilage elongated, narrow, and distally pointed. Dorsal terminal 2 cartilage narrow, flattened, and shorter than dorsal terminal cartilage. Dorsal terminal 3 cartilage small, visible on x-rays but probably lost during preparation. Dorsal marginal cartilage triangular, narrow anteriorly, broadens distally, fused anteriorly with axial cartilage and fused laterally with accessory dorsal marginal cartilage. Accessory dorsal marginal cartilage triangular, longer than dorsal marginal cartilage, posterior apex projected on anterior portion of dorsal terminal 2 cartilage. Ventral terminal cartilage triangular, pointed distally, partially covered by dorsal terminal cartilages in dorsal view. Ventral terminal 2 cartilage broad, outer portion inwardly folded, projected dorsally, partially involving ventral terminal cartilage. Ventral marginal cartilage relatively large, fused proximally with axial cartilage in ventral view, inwardly folded, and projected dorsally.

Molecular analyses

All markers were successfully amplified in both specimens, which had identical haplotypes for the three markers. A fragment of 675 base pairs (bp) was obtained for CO1, 592 bp for 16S, and 1311 bp for NADH2. The NADH2 sequences were new for Squatina armata . Additional n = 18 CO1, n = 18 16S and n = 10 NADH2 GenBank sequences were considered, including CO1 and 16S sequences of other specimens of S. armata from a different locality (Supp. file 1.3). Three CO1 sequences of 658 bp and three 16S sequences of 572 bp were obtained from Stelbrink et al. (2010), while four CO1 sequences of 610 bp were retrieved from the supplementary material of Cañedo-Apolaya et al. (2021). Three unpublished NADH2 sequences of S. armata and three of S. californica were also included.

The fragment consensus lengths after alignment were 610 bp for CO1, 587 bp for 16S and 1044 bp for NADH2. Each gene showed little saturation according to DAMBE and were concatenated (2289 bp, 11 species).

The p-distances calculated for the NADH2 sequences between the neotype of S. armata and other angel sharks ranged between 0.0623 (with S. californica ) and 0.1092 (with S. aculeata ) ( Table 2). The lowest values were obtained between the species from the American continent ( S. armata , S. californica and S. dumeril ). The CO 1, 16S and NADH2 sequences from the neotype and voucher specimen grouped with the other sequences of S. armata in the NJ trees. NJ trees constructed using the CO 1, 16S, and NADH2 datasets also showed S. armata as sister group to all other American species, S. californica and S. dumeril , which formed their own clade ( Fig. 7 ).

The Bayesian inference tree had the single Australian species, S. albipunctata Last & White, 2008 , as a sister group to the remaining ten species, which branched off into two main groups: an American clade ( S. californica and S. dumeril , and S. armata ), and another group composed of a European-African subgroup ( S. aculeata , S. oculata , and S. squatina ) and an Asian subgroup ( S. formosa Shen & Ting, 1972 , S. japonica Bleeker, 1858 , S. nebulosa Regan, 1906 , and S. tergocellatoides Chen, 1963 ) ( Fig. 8 ).

Figures

Fig. 1. Squatina armata (Philippi, 1887), neotype, ♂ (1004 mm total length; MNHNCL ICT 7625), fresh specimen. a. Dorsal view. b. Ventral view.

Fig. 2. Squatina armata (Philippi, 1887), neotype, ♂ (MNHNCL ICT 7625), illustration of the left anterior nasal flap. a. Anterior barbel. b. Median barbel. c. Posterior barbel. Illustrations by IFC.

Fig. 3. Squatina armata (Philippi, 1887), neotype, ♂ (MNHNCL ICT 7625), dorsal thorns. a. Patches of thorns on head forming three pairs; one pair on internarinal space (left one marked a1), second patch on pre-orbital area (a2), third patch on postorbital area (a3), two pairs of interspiracle thorns (a4). b. Single patch of 91–93 thorns on apex of each pectoral fin; thorns hooked, inwardly curved. c. Close-up of a pectoral fin thorn. d. 36 dorsal hooked thorns forming a single row: one medial-dorsal thorn anterior to pelvic girdle followed by 30 caudal thorns and 5 interdorsal thorns (not shown).

Fig. 4. Squatina armata (Philippi, 1887), neotype, ♂ (MNHNCL ICT 7625), dermal denticle shapes and patterns. a. Rostral area, frontal view. b. Interorbital area. c–d. Medial-dorsal denticles in frontal (c) and lateral (d) views. e. Caudal area, la

Fig. 5. Squatina armata (Philippi, 1887), adult ♂, obtained from the fishmarket of Higuerillas, central Chile, date of capture 18 Mar. 2020 (collection code CCM-1228, Chondrolab, Universidad deValparaíso). Close up of individual teeth not to scale.

Fig. 6. Squatina armata (Philippi, 1887) (voucher MNHNCL ICT 7626), clasper morphology.a. External. b–c. Skeletal dorsal (b) and ventral (c) views. Abbreviations: acd = accessory dorsal marginal cartilage; ap = apopyle; ax =axial cartilage; cg = clasper groove; cgl = clasper glans; crh = cover rhipidion; dm = dorsal marginal; dt = dorsal terminal; dt2 = dorsal terminal 2; gcr = globular cartilaginous rod; hyp = hypopyle; rh = rhipidion; vm = ventral marginal cartilage; vt = ventral terminal; vt2 = ventral terminal 2.

Fig. 7 (see previous page). Neighbour-Joining tree of the angel shark CO1, 16S and NADH2 sequences included in this study. Non-American species reduced to one sequence per species for illustrative purposes. Approximate geographic distributions of the species are colour-coded. Sampling location and position in the NJ tree of the Squatina armata (Philippi, 1887) vouchers MNHNCL ICT 7625 (neotype) and MNHNCL ICT 7626 are indicated with orange circles.

Fig. 8. Bayesian inference phylogenetic reconstruction of 11 species ofSquatina Duméril, 1805 for which CO1, 16S and NADH2 sequences were available. Species groups are colour-coded in the phylogeny and the geographic distributions on the map. Sampling location of the S. armata (Philippi, 1887) vouchers MNHNCL ICT 7625 (neotype) and MNHNCL ICT 7626 is indicated with an orange circle.