Pliotrema warreni Regan.

Weigmann, Simon, Gon, Ofer, Leeney, Ruth H., Barrowclift, Ellen, Berggren, Per, Jiddawi, Narriman & Temple, Andrew J., 2020, Revision of the sixgill sawsharks, genus Pliotrema (Chondrichthyes, Pristiophoriformes), with descriptions of two new species and a redescription of P. warreni Regan, PLOS ONE 15 (3), pp. 1-56 : 38-50

Pliotrema warreni Regan.

Proposed English vernacular name: Warren's sixgill sawshark.

Proposed German vernacular name: Warrens Sechskiemer-Sägehai.

Figs 26–30 ; Table 4 .

Material examined (18 specimens). Syntype ( BMNH 1905.6.8.9): female, 805 mm TL, off the coast of Natal (kwaZulu–Natal), 73 m depth, received from Dr. E. Warren of the Natal Government Museum. Syntype ( BMNH 1899.2.10.4): heavily dissected female (skeletal parts and remains of flesh and fins only), ~ 704 mm TL, False Bay, Cape of Good Hope, received from Dr. J.D.F. Gilchrist. DAFF01: adult male, 1022 mm TL, FRS 'Africana' Cruise AND00003, Station D00331 (off South Africa: 34.29º S 25.97 º E), collected on 15 May 2014, trawl 081, grid ID S 3659, depth 108 m. DAFF02: presumably adult female, 1176 mm TL, FRS 'Africana' Cruise CCH00009, Station D00743 (off South Africa: 35.59º S 20.82 º E), collected on 01 May 2016, trawl 014, grid ID S 2058, depth 94 m. DAFF03: gravid female, 1277 mm TL, FRS 'Africana' Cruise CCH00009, Station D00802 (off South Africa: 33.90º S 26.45 º E), collected on 17 May 2016, trawl 071, grid ID S 2326, depth 89 m. DMM I-E/4946: female, 785 mm TL, RV 'Ernst Haeckel' Cruise 51, off Mozambique, June to September 1980. ERB 1105: adult female, 1310 mm TL, FRS 'Africana' Cruise Afr-200, Station A 23549 (off South Africa: 35º30' S 20º 20' E), collected on 23 September 2004, trawl no. 018, grid no. 3069, trawl duration 30 min, 137 m depth (photographs only). ERB 1106: subadult male, 945 mm TL, Prawn Trawler, Tugela Bank, 29º14' S 31º31' E, 27 May to 02 June 2006, 10–25 m depth (photographs only). RBINS uncatalogued: adult female, 1300 mm TL, off South Africa, Zululand (SEM images only). SAIAB 186452: juvenile male, 456.4 mm TL, off KwaZulu-Natal, South Africa, 29º10'49.5” S 32º06'24.6” E, 18 August 2010. SAIAB 189132: juvenile female, 405.9 mm TL, off KwaZulu-Natal (Tugela Bank), South Africa, 29º07'30” S 31º45' E, 15 August 2009. SAIAB 208021: female, 925 mm TL, Great fish River mouth, 33º29'43" S 27º08'06" E, Eastern Cape, South Africa, found stranded on the beach, Warren Potts, 09 June 2019. SAM 33313: 1 specimen, taken off Mozambique, 26º19'0.12” S 33º08'60” E, trawl, 366 m depth, 09 June 1994 (photographs only). SAM 37244: two specimens, taken off Mozambique, 22º36'28.8” S 35º42'46.08” E, bottom trawl, 264 m depth, 16 October 2007 (photographs only). Uncatalogued: female, 920 mm TL fresh, RV 'Dr. Fridtjof Nansen', Survey 2007409, Station 61, off Mozambique, 22º 36.48' S 35º42.77' E, 261–264 m depth, bottom trawl # 18, duration 28.4 minutes, 16 Oct 2007 (taken together with three further specimens) (photographs only). USNM 199741: adult female, 1350 mm TL, RV 'Anton Bruun', Cruise 8, Station 396B, International Indian Ocean Expedition Seychelle Islands Program, 1964, off Delagoa Bay, Mozambique, 25.517º S 33.442 º E, 450–455 m depth, 40-ft shrimp trawl, 28 Sep 1964, collector L. W. Knapp (radiographs only). USNM 353830: one specimen, RV 'Africana', Cruise 106, Station A 13997, off South Africa, 33.92º S 26.68 º E, 101 m depth, otter trawl, 20 Sep 1992, collectors L. W. Knapp and P. C. Heemstra (radiographs only).

Diagnosis. A large six-gilled sawshark with the following characters: barbel origin to anterior nostrils 1.4–1.6 times anterior nostrils to symphysis upper jaw; prenarial length 1.3–1.4 times prebarbel length; preoral length 1.8–2.3 times interdorsal space; pectoral-fin anterior margin 1.4–1.5 times dorsal–caudal space; mouth width 3.1–3.9 times spiracle length. First dorsal fin originates about opposite pectoral-fin free rear tips. Lateral trunk dermal denticles tricuspidate, rather flat and imbricated. Color medium to dark brown dorsally with a pronounced yellowish longitudinal stripe; uniform white ventrally; dorsal rostrum surface with two distinct longitudinal dark stripes, lateral rostral teeth dark-edged. Monospondylous centra 53–56; precaudal diplospondylous centra 49–51; total vertebral centra 154–158. Pliotrema warreni clearly differs from both new species in a rostrum that is not constricted between barbel origin and nostrils and barbels that are situated about two thirds way from rostral tip to mouth, with prebarbel length about twice, i.e. 1.7–2.1 times, distance from barbel origin to symphysis of upper jaw (vs. barbels situated about half way from rostral tip to mouth, with prebarbel length about equal, i.e. 1.0–1.1 times, distance from barbel origin to symphysis of upper jaw), prebarbel length 60.2–68.0% vs. 49.4–52.9% of preoral length, preoral length 1.5–1.7 vs. 1.9–2.0 times prebarbel length, and prenarial length 1.3– 1.4 vs. 1.5–1.7 times prebarbel length.

Description. The description is based on the intact syntype BMNH 1905.6.8.9, as well as the four specimens DMM I-E/4946, SAIAB 186452, SAIAB 189132, and SAIAB 208021. Where relevant, ratios are based on horizontal measurements unless otherwise stated. Morphometric measurements and meristics are given in Table 4 .

External morphology. Body firm and slender, depressed forward of gills, abdomen subcircular in cross-section, tail subtriangular in cross-section, deepest at abdomen; not tapering gradually and evenly beyond pectoral fins; snout flattened, greatly extended, saw-like; abdomen elongate, horizontal head length 0.6–0.7 times snout–anterior vent length, pectoral–pelvic space 14.1–21.2% TL; pelvic–caudal space 2.4–2.8 times pelvic-fin length; tail flattened ventrally, elongate, snout–anterior vent length 1.4–1.5 times anterior vent–caudal tip length; caudal peduncle short, dorsal–caudal space 7.5–8.7% TL, caudal peduncle height 3.5–4.7 times in dorsal–caudal space and width 1.2–1.5 times in height; ventrolateral keels well developed, extending from slightly behind level of free rear tip of pelvic fins to beyond origin of ventral lobe of caudal fin, converging strongly near their posterior extremity; no precaudal pit; no median predorsal, postdorsal or preventral caudal grooves ( Fig 26 ).

Head narrow, subtriangular and deepest at sixth gill slit, strongly depressed above eyes, head width 6.3–7.1% TL, 1.2–1.3 times head height. Snout forming a very elongate, blade-like rostrum. Rostrum triangular in dorsal view; not constricted between barbel origin and nostrils, sides of rostrum nearly straight from tip to origin of orbit; tip narrowly rounded; rostrum extending laterally below eyes as a well-defined suborbital ridge along ventrolateral edge of head, terminating somewhat behind level of posterior edge of spiracle ( Fig 27 ).

A slender, filamentous, dorsoventrally flattened barbel originating on the ventrolateral margin about two thirds way from rostral tip to mouth on each side, with prebarbel length 1.7–2.1 times distance from barbel origin to symphysis of upper jaw, 60.2–68.0% of preoral length and 16.5–20.2% TL. Barbel length 1.9–3.5 times in prebarbel length and 1.1–1.8 times in length from barbel origin to symphysis of upper jaw. Preorbital length, horizontally 5.3–6.2 times mouth width, 18.9–21.5 times spiracle length, 2.3–3.0 times first dorsal-fin length, 3.9–4.6 times rostral width at anterior nostrils; extremely narrow in lateral view; preoral length 26.7– 30.2% TL, 3.8–4.4 times head width, 4.4–5.2 times rostral width at anterior nostrils, 5.9–7.6 times rostral width at origin of barbels, 1.5–1.7 times prebarbel length, 1.2–1.2 times prenarial length, and 1.8–2.3 times interdorsal space ( Fig 27 ).

Large lateral rostral teeth of prenarial portion of rostrum variable in length, curved, rather stout, serrated, longest about half way from apex of rostrum to barbel origin; longest tooth immediately anterior to barbels shorter than spiracle length, length 0.5–1.3% TL and 0.5–1.7 times first complete interspace anterior to barbels, width 0.1–0.3% TL; anteriormost tooth close to tip of rostrum small, followed by the first large tooth; large teeth shortest near nostrils, longest rostral tooth posterior to nostrils 0.2–0.8% TL; large teeth absent behind nostrils but interstitial-like teeth present, short to very short and closely set, partially directed almost ventrally, particularly near mouth. Interspaces between large rostral teeth rather regularly sized, about as long as adjacent teeth, with 2–4 smaller, variable interstitial teeth. Rostral tooth counts mostly symmetrical between left and right hand sides; left side with ~21–~34 large teeth, right side with ~21–~34); anterior to barbels left side with ~15–~17 large rostral teeth, right side with ~14–~18, posterior to barbels left side with ~6–~19 large rostral teeth, right side with ~5– ~18; anterior to nostrils left side with ~17–~24 ventral spines, right side with ~16–~27, anterior to barbel origin left side with ~11–~15 ventral spines, right side with ~10–~19; one enlarged ventral spine, distinctly larger than the other ventral spines, present just in front of each nostril. Large rostral teeth ( Fig 28a–28c ) with elongated crown and oval-shaped base, slightly bent to the rear and flattened towards the apex, forming anterior and posterior cutting edges at front and rear, the latter serrated by barbed hooks. Crown base with numerous short longitudinal ridges forming a pronounced transversal crest. Both, anterior and posterior faces of the root are curved outwards from the junction of crown and root towards the base of the root. The basal face shows a deep v-shaped median groove that is antero-posteriorly directed and has an oval-shaped cavity in the center. Large interstitial rostral teeth similar but with somewhat less pronounced serration in specimens of 704 mm TL (heavily dissected syntype BMNH 1899.2.10.4) or larger. Large interstitial rostral teeth without serration in specimens of 456.4 mm TL (juvenile male SAIAB 186452) or smaller. Small interstitial teeth ( Fig 28d and 28e ) with blade-shaped crown and without serration in all specimens. Crown of ventral spines ( Fig 28f ) elongated cone-shaped with a pronounced transversal basal ridge, root with roundish and pedestal-like base. The basal face has a large and deep roundish foramen in the center.

Eyes lateral on head, large, oval, length 2.9–4.0)% TL; skeletal interorbital space 0.8–1.0 times eye length, 8.7–11.7 times in horizontal preorbital length; posterior eye notches and suborbital grooves present. Spiracles moderately large, length 1.2–1.4% TL and 0.3–0.5 times eye length, left spiracle with 10–13 folds, right one with 10–13; spiracles strongly crescentic, oblique, directed posteroventrally from top to bottom, located just posterior to posterior eye notch, separated by a narrow but deep vertical groove along posterior margin of orbit, shorter than eye; upper edge below level of top of eye. Gill slits small, upright, weakly pleated, lateral on head, close to ventral surface, extending slightly onto ventral surface, subequal in length, sixth slit arches around pectoral-fin origin. Mouth large, strongly inferior, broadly arched, symphysis about level with posterior edge of eye, width 4.2–4.9% TL and 1.4–1.7 times in head width; upper labial furrows absent, lower furrows short, 0.5–0.6% TL; corner of mouth partly concealed by lateral muscles of jaw ( Fig 27 ). Teeth unicuspidate, in well-defined series, bases oval and flattened with short but pronounced, narrow median cusp near middle of jaw, no lateral cusps; cusps diminishing in height towards jaw angles, indistinct near jaw corners; about 4–5 series of functional teeth ( Fig 29 ). Median cusp with labial face slightly convex and with both mesial and distal cutting edges weakly bent mesially and distally in occlusal view, respectively. The mesial and distal crown base parts somewhat curve apically. A pronounced and broad, irregularly shaped apron overlaps the junction of crown and root, building a notch at the junction with both mesial and distal crown base parts. Basal ornamentation, striae or reticulations absent, sharp folds present in upper but absent in lower jaw teeth. The lingual face of the cusp is strongly convex, a well-developed uvula is present at the central crown base. The mesial/distal latero-lingual crown faces curve strongly towards the apex of the crown, forming a sharp notch with the uvula. The root is anaulacorhizid and slightly arched without lobation. The outer surface of the root shows up to four large basal foramina, which are mostly ovalshaped. The inner face of the root shows up to six well-developed foramina along the crownroot junction at each side of the uvula. The basal face of the root is flat, partly showing some outer foramina.

Nostrils small, widely separated, subcircular; nostril width 0.6–1.1% TL, 3.1–5.4 times in internarial width, 4.4–6.8 times in mouth width, 5.9–9.2 times in width of rostrum at nostrils; located distinctly forward of level of anterior margin of eye; distance from anterior nostrils to symphysis of upper jaw 1.2–1.4 times internarial space, distance from barbel origin to anterior nostrils 5.5–6.6)% TL. Anterior nasal flaps well developed, leaf-like, extended ventrally beyond nostrils; incurrent and excurrent apertures surrounded by pronounced marginal lobes; no nasoral or circumnarial grooves; no dermal lobes ( Fig 27 ).

Lateral trunk dermal denticles densely set and slightly overlapping, with flat, tricuspidate crowns ( Fig 28g and 28h ). The lateral cusps are rather weakly pronounced but situated quite far anteriorly so that the median cusp is not much longer than the lateral cusps. The median ridge is strongly pronounced and reaches the tip of the median cusp. The lateral ridges are less pronounced and rarely reach the tips of the lateral cusps. The surface of the denticles is only weakly structured by reticulations close to base. Dermal denticles on rostrum fan-shaped, with an obtusely angled, weakly pronounced median cusp and no lateral cusps but with 6–7 strongly pronounced ridges. The surface of the rostral dermal denticles is only weakly structured by reticulations very close to base.

Pectoral fins large, anterior margin weakly convex, 10.7–12.2% TL and 1.3–1.6 times inner margin; apex narrowly rounded; posterior margin weakly concave, directed across horizontal axis at about origin of first dorsal fin; inner margin convex and strongly notched basally; free rear tip angular ( Fig 26 ). Pelvic fins moderately large, anterior margin almost straight to slightly convex, 5.8–6.8% TL, 1.5–1.8 times in first dorsal-fin anterior margin, and 1.4–1.6 times in second dorsal-fin anterior margin; apex narrowly rounded; posterior margin concave; inner margin weakly convex and slightly notched basally; free rear tip broadly rounded; origin distinctly posterior to level free tip of first dorsal fin and well forward of level second dorsal fin origin ( Fig 26 ).

First dorsal fin broad, semifalcate, anterior margin slightly convex; apex narrowly rounded; posterior margin slanting posteroventrally, slightly convex distally, strongly concave in basal three quarters; inner margin straight, free rear tip narrowly pointed; origin about opposite pectoral-fin free rear tips; insertion and free rear tip clearly anterior to level pelvic-fin origins ( Fig 26 ). Second dorsal fin somewhat smaller than first but of similar shape, anterior margin weakly convex, apex very narrowly rounded; posterior margin weakly convex distally, strongly concave near basal three quarters; inner margin straight, free rear tip narrowly pointed; origin clearly behind level pelvic insertions; interdorsal space 1.4–1.6 times first dorsal-fin length, 1.6–1.9 times dorsal–caudal space; second dorsal-fin inner margin 0.8–1.1 times subterminal caudal-fin margin ( Fig 26 ).

Caudal fin short, dorsal margin slightly convex, length 18.0–19.1% TL, 1.0–1.2 times in pelvic–caudal space and 3.7–5.4 times terminal caudal margin; lower post-ventral lobe absent, upper post-ventral margin slightly convex; terminal lobe well developed, caudal terminal margin slightly concave, apices angular ( Fig 26 ). Ventral origin of caudal fin situated anteriorly due to low anterior fin ridge ( Fig 26c ).

Cranium: five anterior-most basiventral cartilages laterally expanded, with curved, dorsally reflected margins. Chondrocranium and cranial nerves highly modified to accomodate the elongated rostrum. Foramen magnum surrounded by crescent-shaped occipital condyles. Dorsal fenestra of the precerebral fossa egg-shaped, notched anteriorly and posteriorly ( Fig 12c ).

Skeletal meristics (from radiographs): monospondylous trunk vertebral centra: 53–56; diplospondylous precaudal centra: 49–51; total precaudal centra: 103–106; caudal centra: 50– 55; total centra: 154–158.

Coloration. Fresh, prior to preservation (ERB 1105, ERB 1106, SAIAB 208021 and Uncatalogued; Fig 30 ): ground color medium to dark brown dorsally with a pronounced yellowish longitudinal stripe; uniform white ventrally; fins translucent dusky, upper post-ventral caudalfin and pelvic-fin posterior margins narrowly edged white, weak white edges also present at posterior margins of pectoral and dorsal fins, as well as terminal caudal-fin margin; rostrum translucent dusky, dark edged and with two distinct longitudinal stripes dorsally; lateral rostral teeth dark-edged; ventrolateral keels white. Color in preservative (other material examined): coloration similar to fresh coloration but yellowish longitudinal dorsal stripe not detectable in all specimens, particularly after long-time storage in ethanol; ventral coloration uniform yellowish instead of white as usual, ventrolateral keels also yellowish; dark edging of rostrum and lateral rostral teeth still pronounced in most specimens but hardly detectable in the intact syntype which is more than 100 years old; longitudinal dorsal rostral stripes still conspicuous in all specimens including the intact syntype. Fresh photographs of one specimen caught off Mozambique and kindly provided by Oddgeir Berg Alvheim, as well as a photograph of one specimen from off South Africa, taken and kindly provided by Frederik Mollen, Elasmobranch Research Belgium, are shown in Fig 30 .

Size. A large sawshark species reaching at least 1360 mm TL but possibly attaining 1700 mm TL [ 14, 15]. Males are adolescent at 700 to 740 mm, mature at 830 mm and grow to at least 1120 mm TL, females are adolescent at around 950 to 1100 mm TL, are mature when over 1100 mm TL and attain at least 1360 mm TL [ 30]. The male specimen ERB 1106 is subadult at 945 mm TL. The size at birth is about 350 mm TL, the litter size 5–7 pups, but up to 17 developing eggs recorded [ 18, 30].

Distribution. Known from off South Africa and southern Mozambique in depths from 26 to 500 m ( Fig 14 ). However, the maximum depth of 500 m is apparently based on erroneous data for the holotype of Pliotrema kajae sp. nov., indicating that the verified maximum depth of P. warreni was 430 m [ 30]. Nevertheless, P. warreni can be found in waters shallower and deeper than this based on specimens ERB 1105 (caught in 10–25 m depth) and one specimen from 915 m depth in the iSAM collection (SAM 33308, catch location 35.035º S 24.0217 º E). Accordingly, the updated depth range for P. warreni is 10–915 m, albeit the species is usually found in 60–430 m depth [ 27, 30]. Pliotrema sp. possibly occurs down to 1080 m depth [ 28] but it is impossible to assign this maximum depth to a certain species nor any verified specimen of Pliotrema . The northernmost verified records of P. warreni are from off southern Mozambique at about 22º S latitude.

Remarks. There are several morphometric differences between the small and large examined specimens of Pliotrema warreni , which might be of ontogenetic nature. However, the number of specimens and coverage of different sizes is too small to reliably detect ontogenetic differences. Nevertheless, like in P. kajae , the total number of large lateral rostral teeth and the number of large lateral rostral teeth posterior to barbels clearly differ between the smaller (405.9–456.4 mm TL) and larger (785–925 mm TL) specimens of P. warreni (total number 34– 34/34–34 vs. 21–23/21–23; number posterior to barbels 18–19/18–18 vs. 6–6/ 5–7). Like in P. kajae , the large interstitial rostral teeth are serrated in large specimens of P. warreni (704 mm TL or larger), whereas all interstitial teeth are unserrated in specimens of 456.4 mm TL or smaller.

Figures

Fig 12. Radiographs of the crania of the three species of Pliotrema in dorsal views. a P. kajae sp. nov., holotype, MNHN 1987–1266, juvenile female, 560 mm TL (image merged from two radiographs), b P. annae sp. nov., holotype, ZMH 26361, presumably adult female, 981 mm TL, c P. warreni, DMM I-E/4946, female, 785 mm TL. https://doi.org/10.1371/journal.pone.0228791.g012

Fig 14. Map of the southwestern Indian Ocean depicting the catch locations of the examined specimens of all three species of Pliotrema. Holotype (white star) and paratypes (white circles) of Pliotrema kajae sp. nov., holotype (gray star) and paratype (gray circle) of Pliotrema annae sp. nov., and intact (black diamond) and dissected (black triangle) syntypes, as well as other specimens (black squares) of Pliotrema warreni. https://doi.org/10.1371/journal.pone.0228791.g014

Fig 26. Pliotrema warreni, syntype, BMNH 1905.6.8.9, female, 805 mm TL, preserved. a lateral, b dorsal, and c ventral views. The photographs were taken and kindly provided by Kevin Webb. https://doi.org/10.1371/journal.pone.0228791.g026

Fig 27. Pliotrema warreni, syntype, BMNH 1905.6.8.9, female, 805 mm TL, preserved. Head in a lateral, b dorsal, and c ventral views. Scale bar: 5 cm. The photographs were taken and kindly provided by Kevin Webb. https://doi.org/10.1371/journal.pone.0228791.g027

Fig 28. Pliotrema warreni, SEM images of rostral teeth and lateral trunk dermal denticles. a–e,g,h SAIAB 208021, female, 925 mm TL; f RBINS uncatalogued, adult female, 1300 mm TL. a–c large lateral rostral tooth in a total and b,c close-up views; d,e small interstitial lateral rostral teeth in d total and e close-up views; f ventral rostral spine in total view; g,h lateral trunk dermal denticles in apical views. Scale bars: a,b,d 1 mm, c,e,g 500 μm, h 100 μm. Image 28f was kindly provided by Frederik Mollen, Elasmobranch Research Belgium, from Herman & Ladeuze [29]. https://doi.org/10.1371/journal.pone.0228791.g028

Fig 29. Pliotrema warreni, RBINS uncatalogued, adult female, 1300 mm TL, SEM images of oral teeth. a–f upper anterolateral teeth in a,b labial, c,d lingual, and e,f basal views; g–l lower anterolateral teeth in g,h labial, i,j lingual, and k, l basal views. The images were kindly provided by Frederik Mollen, Elasmobranch Research Belgium, from Herman & Ladeuze [29]. https://doi.org/10.1371/journal.pone.0228791.g029

Fig 30. Pliotrema warreni, images of specimens in fresh condition. a,b uncatalogued female, 920 mm TL fresh, in a total dorsal and b ventral head views, c ERB 1105, adult female, 1310 mm TL. Note yellowish longitudinal stripe in a,c. The photographs were taken and kindly provided by Oddgeir Berg Alvheim, Institute of Marine Research, Bergen, Norway (a,b) and Frederik Mollen, Elasmobranch Research Belgium (c). https://doi.org/10.1371/journal.pone.0228791.g030