On the taxonomy of the first record of rare deep-water rough shark species of Oxynotidae (Chondrichthyes: Squaliformes) in the western Indian Ocean

An immature female specimen of rough shark was collected south of Reunion Island in the Madagascar Basin in 2009 aboard R/V Dr. Fridtjof Nansen, representing the first official record of the family Oxynotidae in the western Indian Ocean. The specimen is herein identified as Oxynotus sp. due to morphological differences with its closely similar congeners O. centrina and O. bruniensis regarding morphometrics, shape of dorsal, pectoral and caudal fins, shape of the head and colouration, refuting the hypothesis of occurrence of these two species in the region. These results indicate that Oxynotus sp. is possibly an undescribed species. A general description of the external morphology, external morphometrics and photographs of Oxynotus sp. are provided. The specimen has a hepatosomatic index of 36.33% which reveals that it was possibly approaching maturation, suggesting that a viable population of Oxynotus sp. exists in the western Indian Ocean. Intraspecific variations in O. centrina from the Mediterranean Sea and eastern Atlantic Ocean are also noticed, requiring further taxonomic scrutiny.


INTRODUCTION
Oxynotidae is a monotypic family of small to medium sized rare deep-water rough sharks with endemic regional geographical distributions on continental and insular shelves and upper continental slopes of the Atlantic and Pacific Oceans (Ebert et al. 2013).The occurrence of Oxynotidae and records of its representatives in the western Indian Ocean were speculative (e.g., Ebert 2013Ebert , 2015;;Ebert & van Hees 2015;Compagno 2016;Weigmann 2016) till recently in Fricke et al. (2018).Members of Oxynotidae are characterized by having a body triangular in cross-section, conspicuously deep, arched dorsally and flattened ventrally at trunk, rough skin with large dermal denticles, head small and wide, snout blunt at tip and short with fringed anterior margin of nostrils, mouth circular with papillose lips and ventrally located, eyes rounded and conspicuously large, located laterally, spiracles large and crescent, located behind eyes, dorsal fins sail-like, conspicuously upright and tall, dorsal-fin spines conical, thick and markedly small, located prior to each dorsal fin and never transcending the fin apex, pectoral fins leaf-like, pointed distally at apex, and inconspicuous free-rear tips, lateral ridges prominent at trunk, caudal fin small and broadly sub-triangular with inconspicuous lower caudal lobe and evident subterminal notch.It bears teeth dissimilar in both jaws, upper teeth smaller than lower teeth, upper teeth thin and lanceolate, lower teeth broad and bladelike (Compagno 1999).

MATERIAL AND METHODS
The southern Indian Ocean seamounts cruise expedition was undertaken aboard the R/V Dr. Fridtjof Nansen along the southwestern Indian Ridge between 12 November and 19 December 2009.During this cruise, a single specimen of Oxynotus sp. was captured on 14 November 2009 during Trawl 1, Station 2, Madagascar Basin, south of Reunion Island, Event 7, at a maximum depth of 600m using a pelagic Ǻkra trawl net fitted with a multisampler.The Ǻkra trawl net used was a Flytetrål 152 MSK x 3200mm, with a 20m net mouth opening (Rogers et al. 2010).Prior to each trawl, ice-trays and labels were prepared for sorting.Once on deck, samples were emptied into large trays containing ice.A small amount of seawater was added to the trays to prevent the samples freezing to the ice.Specimen of Oxynotus sp. was labelled by tying a label to the fish using string, then either fixed in a 4% formalin solution or frozen (Rogers et al. 2010).This specimen was later donated and logged at the South African Institute for Aquatic Biodiversity (SAIAB) where further curatorial procedures such as identification and cataloguing took place, and put through a series of 10% and 50% ethanol solutions, before finally being preserved in 70% ethanol solution.
Skin sample measuring 1cm 2 was taken from below first dorsal fin (right side) for analysis of dermal denticles.Liver weight and conditions follow Capapé et al. (1999).Hepatosomatic index (HIS) was calculated using the formula HSI (%) = liver weight (g) / dressed weight (g) X 100.Specimen was photographed in dorsal, lateral, and ventral views as well as individual body parts (e.g., fins, liver) using digital camera.Photographs of dermal denticles were taken using stereoscope microscope attached to digital camera at the Scottish Association for Marine Science.Map of collecting locality of examined specimen was generated using QGIS 2.14.2 Essen (QGIS Development Team, QGIS Geographic Information System, Open Source Geospatial Foundation Project; http://qgis.osgeo.org/)and Google Earth (http:// www.google.co.uk/intl/en_uk/earth).
Institutional abbreviations are in accordance to Sabaj (2016).

Family Oxynotidae Gill, 1863 Genus Oxynotus Rafinesque, 1810
Oxynotus sp.Images 1-6, Table 1 Material examined: SAIAB 192249, juvenile female, 519mm TL, south of Reunion Island, Madagascar Basin, General description of external morphology: External measurements for Oxynotus sp. are provided in Table 1.Body robust and triangular in cross-section, conspicuously deep at trunk and abdomen, and thin at precaudal peduncle; body arched dorsally from head to abdomen, flattened ventrally at trunk with lateral ridges prominent at trunk; body wide from head to abdomen and narrow at precaudal penduncle.Head small, narrow anteriorly and wide posteriorly, markedly arched anterior-dorsally.Snout blunt at tip and short with nostrils broad and horizontal with anterior margin of nostrils elongated, wide and fringed distally.Eyes elliptical horizontally and conspicuously large, located laterally with prominent supraorbital and infraorbital ridges and inconspicuous knob.Spiracles large, subcrescent, thin and vertical, situated posterior to eyes.Mouth large and transverse, constricted and circular with papillose and fleshy lips, located ventrally; preoral cleft elongate, thick, distally rounded, situated medially in the upper lip.Upper teeth smaller and thinner than lower teeth; upper teeth compressed and triangular, conspicuously slender at crown and crown vertically elongated, unicuspid with pointed cusp, mesial and distal cutting edges straight; upper teeth irregularly distributed in mouth; lower teeth compressed and interlocked, broadly triangular at crown, crown vertically low, unicuspid with small serrations in the blades, mesial and distal cutting edges sigmoid.Gill slits markedly tall and vertical.Dorsal fins sail-like and triangular, conspicuously upright, tall and broad at fin web; anterior and posterior margins of first and second dorsal fins straight; apex and free rear tips of first and second dorsal fins pointed.Dorsalfin spines conical, thick and markedly small, located prior to each dorsal fin and never transcending the fin apex; first dorsal-fin spine directed forwardly and second dorsal-fin spine directed backwardly.Pectoral fins leaf-like and wide, placed laterally; pectoral-fin anterior and inner margins markedly convex; pectoralfin posterior margin somewhat straight and slightly concave distally; pectoral-fin apex pointed distally; pectoral-fin free-rear tips inconspicuous.Pelvic fins sub-quadrangular and wide, located ventrally just prior to caudal fin; pelvic-fin margins straight; pelvic-fin apex and free rear tips rounded.Caudal fin small and subtriangular with inconspicuous lower caudal lobe and evident subterminal notch; caudal fork inconspicuous; dorsal caudal margin straight; preventral caudal margin somewhat convex; terminal caudal margin straight; postventral caudal margins straight; posterior, ventral and subterminal caudal tips rounded.
Dermal denticles markedly large, measuring 1mm width across tips of lateral cusps.Denticles heavy, sparsely distributed with different sizes throughout, and positioned in right angle to the longitudinal body axis.Denticles crown-like with four pointed cusps distally, including two lateral cusps and two median cusps.Median cusps comprised of one anterior cusp and one posterior cusp.Anterior median cusp much more elongate than remaining cusps.Posterior median cusp small and hook-like.Large denticles with three thin anterior ridges, although a single anterior ridge is shown in small denticles.Lateral ridges thin and small.Crown base of denticles conspicuously broad.
Body brownish laterally and ventrally with large black blotches dorso-laterally throughout head, trunk and tail; black botches also found ventrally at head posterior to mouth till vertical traced at insertion of pectoral fins.Dorsal fins brownish, dorsal-fins posterior margin and free rear tips white.Pectoral fins brown dorsally and blackish ventrally with pectoral-fin anterior and posterior margins broadly white.Pelvic fins dark brown with black blotch ventrally; pelvic-fin anterior and posterior margins whitish.Caudal fin dark brown with postventral caudal margins slightly white, black caudal strip prominent and black caudal blotch evident in the preventral caudal margin.
Biological traits.The specimen weighed a total of 1.944kg.The liver is markedly heavy with total weight of 518g, entirely occupying the abdominal cavity.It comprises two asymmetrical lobes, somewhat cylindrical, triangular in cross-section, pointed distally and convex proximally.Liver lobes are conspicuously elongate with right lobe measuring 275mm and left lobe 262mm in length.The hepatosomatic index (HSI) for the specimen is 36.33%.According to Capapé et al. (1999) adult females show HSI ranging from 23%-42% while Megalofanou & Damalas (2004) noticed 18.8% HSI for a gravid female of O. centrina, supporting that HSI considerably decreases in breeding females.The hepatosomatic index in the immature female of Oxynotus sp.comprises twice that of gravid females of O. centrina.Capapé et al. (1999) stated that the HSI of O. centrina increases as juveniles approach maturation, taking this into account the high HSI of Oxynotus sp.indicates that the specimen was possibly approaching maturation at the time of capture.Thus, a viable population of Oxynotus sp. may exist within the Madagascar Basin, although this is the only official record of this species and family from the region suggesting that the population is rather small and vulnerable.

DISCUSSION
The Oxynotus specimen from the western Indian Ocean is herein identified as Oxynotus sp.throughout the body dorsal, lateral and ventrally (vs.body greyish-white with brown or reddish-brown blotches throughout the body in O. centrina).Oxynotus sp. has head, preorbital, pre-branchial, prespiracular and prepelvic lengths greater than in O. centrina.The former species also shows pre-vent length, pelvic-caudal space, trunk width, interorbital space, postventral caudal margin length much greater than in O. centrina.Other differences in external measurements between Oxynotus sp. and O. centrina are noticed for preoral length, height of fifth gill slit, length of first dorsal-fin anterior and posterior margins, height of pelvic fin, dorsal-caudal and pectoral-pelvic space, height of eyes.Bass et al. (1976) stated that the interdorsal space as percentage of precaudal length in specimens from the southeastern Atlantic Ocean (e.g., Angola, Namibia and South Africa) is smaller than those from the northeastern Atlantic Ocean and Mediterranean Sea.According to Yano & Matusuura (2002), interdorsal space as percentage of precaudal length overlaps in O. centrina and the specimen of Oxynotus from Namibia (29.1%-34.6%PCL vs. 30.1% PCL).Oxynotus sp. from the western Indian Ocean shows a much smaller interdorsal space, corresponding to 25.8% PCL, which is in accordance to the results of Bass et al. (1976) and against those of Yano & Matusuura (2002).It is important to notice, however, that the measurement provided in Yano & Matusuura (2002) for the Namibian specimen was calculated from the illustration taken from Bass et al. (1976), which might have interfered in their results.When the interdorsal space is calculated as percentage of total length, Oxynotus sp.(20.7% TL) and O. caribbaeus (19.2% TL) taken from Yano & Matsuura (2002) overlap with those of O. centrina (18.0%-21.0%TL).Interdorsal space in Oxynotus sp.clearly differs from those of O. bruniensis (12.7% TL), O. japonicus (16.7% TL) and O. paradoxus (21.9% TL) taken from Yano & Matsuura (2002).
Besides interdorsal space, Oxynotus sp. is separated from O. bruniensis sensu Ogilby (1893), Cadenat & Blache (1981), Last & Stevens (2009) (1986), andCompagno et al. (1991).Preliminary comparative morphological observations in O. centrina reveal strong intraspecific variations between specimens from the eastern and western Mediterranean Sea as well as northeastern Atlantic Ocean regarding shape of dorsal and pectoral fins, body colouration and body depth.External measurements also vary for trunk height, interorbital and internarial spaces, mouth width, preoral length and heights of first and fifth gill slits, length of first dorsal-fin base, and length of second dorsal-fin posterior margin (see Table 1).These variations possibly represent the existence of another nominal species distinct from O. centrina in this region as well.Oxynotus salviani Risso, 1827 described from Nice, France has been in synonymy with O. centrina without detailed taxonomic examination in Krefft & Tortonese (1973), demanding verification.Divergences on the morphometric methodology applied in earlier accounts on species of Oxynotus (e.g., Yano & Murofushi 1985;Myagkov 1986;Yano & Matsuura 2002;Kousteni & Megalofonou 2016) and the present study exist, and may have interfered in the assumptions pointed out in the present study, indicating that a standardization of external measurements for Oxynotus species is essential for future comparative purposes.The differences and intraspecific variations observed in the external morphology among species of the genus, however, denote that the taxonomy of the group is more complex than previously noticed.Re-evaluation of these morphological aspects combined with molecular analysis of species of Oxynotus, especially Oxynotus sp. and O. centrina, is urgently required in order to elucidate if Oxynotus sp. is a valid species and if O. centrina comprises a species with broad geographical distribution and strong intraspecific variations or if it has been misidentified with other regional congeners (e.g., O. paradoxus).
Oxynotus sp. is a rare deep-water species, possibly comprising a small and vulnerable population with scattered endemic distribution in the western Indian Ocean.Fishery trends are currently shifting from targeting coastal habitats to abyssal basins where fish stocks are still widely available for exploitation, including the Madagascar Basin where this species occurs.Thus, it is assumed that Oxynotus sp. may occasionally be caught as by-catch during bottom trawls by commercial vessels in this region, as it is noticed for its congeners elsewhere, including O. centrina, O. bruniensis, and O. japonicus (Francis 2003;Yano 2004;Bradaï et al. 2007).Moreover, the high HSI of this species provided in this study indicates that the population of Oxynotus sp. is approaching the breeding stage of the life cycle, making this species even more vulnerable to fishing threats.It is of urgent conservation concern to consider Oxynotus sp. as a species vulnerable to overfishing, even though fisheries have no apparent economic interest in rough sharks.
due to inherent differentiation in external morphology and morphometrics with specimens of O. centrina and O. bruniensis.Oxynotus sp. is distinct from O. centrina from the Mediterranean Sea and northeastern Atlantic Ocean by having body much more robust and deeper from head to tail with heights of head, trunk, tail and caudal peduncle greater in length than in O. centrina (vs.body slender and low in O. centrina), knob behind eyes inconspicuous (vs.conspicuous in O. centrina), dorsal fins with posterior margin straight and apex directed upwardly (vs.conspicuously concave and apex directed posteriorly in O. centrina), pectoral fins broad with apex slightly pointed (vs.thin with apex conspicuously pointed and thin in O. centrina), and caudal fin with lower caudal lobe inconspicuous or small (vs.lower caudal lobe conspicuous in O. centrina).Oxynotus sp. also differs by having smaller dorsal-caudal space than those of O. centrina, and body brownish with many black blotches Image 5. Dermal denticles of Oxynotus sp.(SAIAB 192249, juvenile female, 519mm TL) taken from below first dorsal fin.A: dorsal view; B: anterior view; C: posterior view, showing posterior median cusp; D: anterior view of a large denticle.
and Ebert (2013) by having body dark brown with black blotches present from head to tail (vs.body sandy light brown with no evident black blotches in O. bruniensis), supraorbital and infraorbital ridges conspicuous (vs.inconspicuous in O. bruniensis), head markedly convex anterior-dorsally (vs.markedly concave anterior-dorsally in O. bruniensis), spiracles vertical (vs.spiracles rounded in O. bruniensis), and dorsal fin with apex pointed (vs.apex rounded in O. bruniensis).It is further distinct from O. bruniensis by having interdorsal space 1.67 times second dorsalfin base length (vs.interdorsal space 0.93 times second dorsal-fin base length in O. bruniensis, taken from Yano & Matsuura 2002).These findings support that O. bruniensis recognized in the Eastern Indian Ocean in Ebert (2013) and Weigmann (2016) has no occurrence in the western Indian Ocean.Oxynotus sp. may represent a species distinct from the Mediterranean O. centrina and possibly an undescribed species.The present study clarifies that this species occurs in the Madagascar Basin from off south Reunion Island