Lost before found: A new species of whaler shark Carcharhinus obsolerus from the Western Central Pacific known only from historic records

Carcharhinus obsolerus is described based on three specimens from Borneo, Thailand and Vietnam in the Western Central Pacific. It belongs to the porosus subgroup which is characterised by having the second dorsal-fin insertion opposite the anal-fin midbase. It most closely resembles C. borneensis but differs in tooth morphology and counts and a number of morphological characters, including lack of enlarged hyomandibular pores which are diagnostic of C. borneensis. The historic range of C. obsolerus sp. nov. is under intense fishing pressure and this species has not been recorded anywhere in over 80 years. There is an urgent need to assess its extinction risk status for the IUCN Red List of Threatened Species. With so few known records, there is a possibility that Carcharhinus obsolerus sp. nov. has been lost from the marine environment before any understanding could be gained of its full historic distribution, biology, ecosystem role, and importance in local fisheries.


Introduction
The life sciences rely on a strong taxonomic underpinning of the faunal groups being investigated, without which it is extremely difficult to put such research into the correct context [1,2]. However, the discovery of species has infinite possibilities, and it is not always possible to predict where taxonomic discoveries or problems lie. Chondrichthyan fishes (sharks, rays and chimaeras) are a prime example where in recent decades, taxonomy of this group has undergone somewhat of a renaissance. More than 180 new chondrichthyan species were formally described between 2002 and 2012 [2], with more than 80 new species formally described since 2012. Thus, more than 20% of the extant species of sharks and rays have been described since 2002. The discovery of species new to science are made in a number of ways, ranging from exploration into deeper waters and more remote locations, e.g. [3,4], to detailed taxonomic revisions of specific groups yielding higher diversity than previously thought, e.g. [5,6]. Add a1111111111 a1111111111 a1111111111 a1111111111 a1111111111

Ethics statement
The specimens upon which the new species is based were collected over 80 years ago and are deposited in the Academy of Natural Sciences, Philadelphia (ANSP) and the Naturhistorisches Museum, Vienna (NMW). Permission to examine them was obtained from both museums, and two ANSP specimens were formally loaned to the Australian National Fish Collection (CSIRO). No new material was collected for this study.

Comparative material
Specimens of closely related congeneric taxa examined for comparison were (see Acknowledgments for institutional names): Carcharhinus borneensis (Bleeker) (

Morphology
External morphometric measurements were taken by digital vernier calipers to one tenth of a millimetre (mm) from specimens preserved in 70% ethanol. Measurement terminology follows [16,20] except for total length (TL) and additional direct (point-to-point) measurements which were taken, i.e. pre-first-dorsal-fin-length (PD1), head length (HDL), prebranchial length (PG1), preorbital length (POB), prenarial snout length (PRN). Direct measurements are used in the description if not otherwise stated. Fin origin was deemed to be the point of greatest angle (as used by [19]). Note that in [21] for C. borneensis, the fin origins, particularly those of the dorsal and anal fins, were determined to be further forward on the body, at the start of the short ridge before these fins. This explains the differences between the length, base length and anterior margin of the first dorsal, second dorsal and anal fins reported in [21] and our data. Dentitional terms follow [16,19,20]. Cranial morphology follows [16] and is based on radiograph of the head of one of the paratypes (ANSP 77121). The holotype and paratypes of the new species were measured in full (Table 1). In the description and diagnosis, values for the holotype are given first, followed by the ranges for the paratypes in parantheses.

Meristics
Vertebral terminology, method of counting and vertebral ratios follow [16,20,22]. Meristics were taken from radiographs of the type specimens. Counts were obtained separately for trunk (monospondylous), precaudal (monospondylous + diplospondylous to origin of upper lobe of caudal fin) and caudal (centra of the caudal fin) vertebrae. Tooth row counts were made in situ.

Nomenclatural acts
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new name contained herein is available under that Code from the electronic edition of this article. This published work and the nomenclatural act it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSID (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix "http://zoobank.org/". The LSID for this publication is: urn:lsid:zoobank.org:pub: ADB5D2F7-3D61-4085-8869-5BF815D9DAD5. The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: PubMed Central, LOCKSS.

Genus Carcharhinus Blainville
Type species. Carcharias melanopterus Quoy & Gaimard, under suspension of the Rules by the ICZN [31]. Definition. Adapted from [19]: Small to large carcharhinids with the following combination of characters: an internal nictitating lower eyelid; no spiracles (rarely present in juveniles as minute vestiges); short labial furrows, their length less than 1% TL, the lower barely or not visible when mouth is closed; snout short to moderately long, preoral length always less than 10% TL; internarial distance at least 2.5 times nostril width; teeth blade-like with single cusps, although basal margins of cusps may have enlarged serrae; cusps of upper teeth serrated or smooth; total number files of teeth in upper or lower jaws less than 40; midpoint of first dorsal-fin base usually closer, or at least as close to, pectoral-fin free tip than to pelvic-fin origin; height of second dorsal fin never more than 55% height of first dorsal fin, 60-120% of height of anal fin; second dorsal fin more or less opposite anal fin, its origin usually in front of midpoint of anal-fin base, but rarely over posterior third of anal-fin base; upper and lower precaudal pits present, upper better developed, crescent shaped, wider than long, with a well-defined anterior edge; caudal peduncle without lateral dermal ridges.  10.0-15.1 times in head length; no row of enlarged hyomandibular pores alongside each mouth corner; upper anterior teeth broadly triangular and serrated, with large and coarse (non-lobate) serrations basally; lower anterior teeth with narrower, mostly straight cusps; cusps of upper and lower anterolateral teeth with apical margin slightly recurved; no lateral cusplets; total tooth row counts 27-31/26-29; posterior edge of the mandibular plate with an elongate and crescentic indentation; second dorsal-fin origin well posterior of anal-fin origin, about opposite anal-fin midbase, second dorsal-fin origin to analfin origin 1.3-2.5% TL, 0.3-0.6 times second dorsal-fin base; first dorsal fin triangular, not falcate, origin about opposite first third of pectoral-fin inner margin length, free rear tip just anterior to pelvic-fin origins, length 1.7-1.9 times height, inner margin 1.9-2.5 in base; second dorsal fin much smaller than first, slightly smaller than anal fin; base 1. Description. Body moderately slender (Fig 1), trunk subcircular and almost pear-shaped in section at first dorsal-fin base, length of trunk from fifth gill slits to vent 1.07 in holotype (1.06-1.09 in paratypes) times head length. Predorsal, interdorsal and postdorsal ridges absent from midline of back, lateral ridges absent from body. Caudal peduncle relatively slender, rounded-hexagonal in section at second dorsal-fin insertion, postdorsal and postventral spaces flattened, lateral surfaces subangular; height of caudal peduncle at 2 nd dorsal-fin insertion 1.07 (1.16-1.40) times its width, 2.08 (1.43-1.48) times in dorsal-caudal space. Precaudal pits present; upper pit a deep, arcuate and crescentic depression; lower pit a much shallower crescentic depression.

New species description
Head length to 5 th gill opening 0.76 (0.77) times in pectoral-pelvic space. Head narrow and slightly flattened, ellipsoidal-lenticular in shape in cross-section at eyes. Outline of head in lateral view undulated dorsally, nearly straight on snout, moderately convex above gills (Fig 2A); weakly convex ventrally along lower jaws and beneath gills. In dorsoventral view, head parabolic ( Fig 2B); gill septa expanded slightly outwards. No distinctly enlarged hyomandibular pores adjacent to mouth corners. Snout moderately short, preoral snout length 1.07 (0.90-1.04) times mouth width; tip rounded in dorsoventral view and very weakly indented anterior to nostrils; snout bluntly pointed in lateral view, nearly straight above to weakly convex above and convex below. A narrow, longitudinal band of enlarged pores posterior to eye, almost entirely situated in the whitish ventral colouration (i.e. below the waterline).
Upper jaw gradient monognathic heterodonty present in all tooth groups; one small, welldeveloped symphysial tooth present. Anterior teeth (Figs 4A, 4B and 5A) narrow with somewhat linear lower distal crown margins and weekly notched basal margins; mesial crown edges somewhat linear, not convex with apical portion of crowns slightly reflexed; serrations coarser basally and weaker apically. Anterolateral files with considerably more oblique crowns; distal margins notched with strong basal/apical bifurcation of crown; basal margins more coarsely serrated, no enlarged distal serrae present and serrations gradient from outer basal margins to crown notches; lower portion of crowns noticeably serrated, decreasing but present apically; mesial margins linear, not convex with apical portion of crowns slightly recurved mesially; serrations slightly coarser basally, decreasing but present apically. Lateroposterior files with considerably more oblique crowns than laterals; distal margins deeply notched; serrations coarser basally; mesial margins slightly more posteriorly arcuate and lacking mesial recurvature apically.
Lower jaw gradient monognathic heterodonty present but weak in all tooth groups; one small, well-developed symphysial tooth present. Anterior teeth (Figs 4C, 4D and 5B) with narrow, erect, triangular cusps, moderate in height and not noticeably elongated with strongly acuminate apical portions; distal edge of crowns slightly angular and weakly notched; mesial edges of crowns somewhat concave with apical portion slightly recurved mesially; contour of roots not crescentic or arched with evident root lobes; distal and mesial cusp edges moderately serrated; coarser basally. Lateral files more noticeably notched with slightly more angular distal margins; crown feet coarsely serrated on both distal and mesial margins; slightly heavier distally; lower crown portion with slightly acuminate apical margins and moderately serrated edges, decreasing but present apically. Lateroposterior files increasingly angular with heavier distal notches; distal basal margins heavily serrated, less so on mesial margins; lower crown portions moderately serrated, decreasing but present apically; lower cusp portion slightly crescentic with apical portions recurved mesially.
Rostral cartilages moderately slender, not hypercalcified, rostral fenestrae relatively large, rostral tip truncate, not pointed; nasal capsules broad, anterior margins nearly straight; anterior fontanelle moderately expanded, posterior border with a distinct indentation centrally; preorbital processes large, somewhat triangular at tip, relatively narrow based; postorbital processes long and slender; orbits large ( Fig 6).
Lateral trunk denticles small, slightly imbricate, broad, tricuspid (Fig 7); crowns usually slightly wider than long (sparser smaller denticles slightly longer than wide), with 3 prominent longitudinal ridges (medial ridge slightly stronger and more pronounced) that extend entire length of crown onto cusps; medial cusp short but strong, much shorter than rest of crown, flanked by a pair of slightly shorter lateral cusps.
Pectoral fins short and relatively broad, weakly falcate; anterior margin moderately convex, apices narrowly rounded; posterior margin very weakly concave; free rear tip moderately rounded to somewhat angular, inner margin weakly convex; base broad about 57 (55-59)% of fin length; length from origin to rear tip 1.26 (1.20-1.24) times anterior margin length; larger in area to first dorsal fin; origin under fourth gill slit; fin apex posterior to free rear tip when fin is elevated and adpressed to body. Pelvic fins small, triangular and not falcate; length of anterior margin 0.50 (0.41-0.42) of pectoral-fin anterior margin; area about 1.5 times that of anal fin; anterior margin nearly straight; apex rounded angular; posterior margin nearly straight; free rear tip bluntly rounded, inner margin nearly straight.
First dorsal fin relatively small, moderately long-based, broad and triangular, not falcate; anterior margin weakly convex; apex moderately rounded; posterior margin distally straight and basally moderately concave; free rear tip acutely pointed, inner margin nearly straight; origin situated posterior to pectoral-fin insertion by about a third of the pectoral-fin inner margin length, midpoint of base 1.72 (1.93-2.68) times closer to pectoral insertions than pelvic origins; free rear tip anterior to pelvic-fin origins by about an eye length; posterior margin arching posteroventrally from apex, then abruptly to near free tip; insertion posterior to dorsal-fin apex.  Anal fin apically narrow and strongly falcate; slightly larger than second dorsal fin; height 1.49 (1.17-1.25) times second dorsal-fin height, base length 1.21 (1.11-1.17) times second dorsal-fin base; anterior margin moderately convex; apex narrowly rounded; posterior margin deeply notched at slightly less than a right angle; free rear tip acutely pointed, inner margin nearly straight; origin well anterior to second dorsal-fin origin; insertion about level with second dorsal-fin midbase, anterior to fin apex; free rear tip in front of lower caudal-fin origin by a length slightly more than its inner margin length; posterior margin slanting anterodorsally and then abruptly posterodorsally. Anal-fin base expanded anteriorly as very short preanal ridges (obscure), less than a quarter length of rest of base. Anal-fin base 1 Caudal fin narrow-lobed and asymmetrical, with short terminal lobe and prominent but moderately long, non-falcate ventral lobe; dorsal caudal margin proximally and distally convex, and slightly concave just anterior to subterminal notch, with prominent lateral undulations; preventral margin moderately convex, tip of ventral caudal-fin lobe narrowly rounded; lower postventral margin weakly concave; upper postventral margin straight; subterminal notch a narrow, deep slot; subterminal margin nearly straight; terminal margin irregular and weakly concave, lobe formed by these margins angular, tip of tail narrowly rounded.    Colour. In preservative: dorsal surface of head, trunk and tail grey, graduating to pale ventral colouration on midlateral surfaces. Demarcation between light and dark surfaces of head strong (light ventral colour just visible in dorsoventral view of head), extending along lateral angle of the snout anteriorly to level of nostrils, extending dorsoposteriorly to level of upper margin of eye; then extending very gradually ventroposteriorly to about upper edge of first gill slit; waterline more diffuse over gills, almost at level of upper margins; gill slit membranes mostly pale; margins of gill slits narrowly pale edged. Demarcation between dorsal and ventral coloration becoming diffuse above pectoral fins; extending diffusely along abdomen and tail at about midlateral level; pale area continuing onto base of caudal fin. Fins without any obvious dark or light markings. First dorsal fin grey, lower margin of free tip pale. Second dorsal grey, posterior margin slightly paler. Anal fin slightly paler grey. Caudal fin grey, terminal and ventral lobes slightly darker. Pectoral fins grey on both surfaces, posterior margins diffusely paleedged. Pelvic fins pale grey, much paler on ventral surfaces basally. Eyes blackish; nictitating membrane pale.

Size
Only known from the three type specimens, a late-term embryo 339 mm TL and two juvenile females 370 and 433 mm TL. Size at birth likely close to 340 mm TL, since late-term embryo was fully developed and 370 mm TL juvenile had a faint umbilical scar.

Distribution
Uncertain; collection records indicate southern South China Sea (Gulf of Thailand, Vietnam, Malaysian Borneo).

Etymology
The specific name is Latin for 'extinct' (obsolerus) in allusion to the fact that the species has not been recorded in many decades. Proposed English vernacular name: Lost Shark.

Discussion
Carcharhinus obsolerus can be readily separated from most of its congeners by the relative position of the second dorsal and anal fins, and its low vertebral count. The second dorsal-fin origin of C. obsolerus is about level with the mid anal-fin base, a feature shared by C. borneensis, C. cerdale, C. macloti, and C. porosus, and occasionally in C. hemiodon [19,24]. While the second dorsal-fin origin of C. sealei is often posterior to its anal-fin origin, it is never level with the mid anal-fin base [12]. In contrast, the remaining 29 species in this genus have the origin of the second dorsal fin either level with, or anterior to the origin of the anal fin. The relative positions of the second dorsal and anal fin do not vary ontogenetically based on other closely related species [12,21]. Thus, this character is considered a key character for separating these taxa.
Finally, in Carcharhinus obsolerus and C. borneensis, the indentation in the posterior edge of the mandibular plate (rear Meckel's cartilage) is elongated and shallow (Figs 3 and 11A). In contrast, this indentation is shorter and deeper in C. cerdale, C. porosus and C. macloti ( Fig  11B-11D).
Although [19] considered the three specimens of C. obsolerus conspecific with C. porosus, he stated that decision was "despite the seemingly improbable distribution for a small, essentially tropical, littoral shark" and that adult specimens are required. In contrast, [15] and subsequently [16] considered it a distinct, undescribed species, based on morphometrics and cranial morphology. However, due to the broad scope of [15,16], these differences were not specified. More recently, [18] considered these three specimens as questionably an undescribed species but the data provided was largely taken from [19] with no additional insights provided. The decision to allocate these three specimens to a new taxon in this paper was not purely a different interpretation to the work of [19]. An important consideration when examining the C. porosus treatment in [19] is that it represents two taxa, C. porosus and C. cerdale which was subsequently resurrected as a valid species separate from C. porosus by [14].
The taxonomic decision made in this study to formally describe these three specimens as a new species carefully considered the information in all of the aforementioned publications and new insights gained from examination of these specimens. The need for obtaining adult specimens alluded to by [19] was an appropriate conclusion to make at that time. Prior to 1982, there had been very few detailed biodiversity surveys or investigation of catch composition in coastal fisheries in the South-east Asian region. Thus the lack of adult records could easily be linked to inadequate collecting in the area it occurred. However, in recent decades there has been numerous detailed biodiversity and fisheries surveys in the South-east Asian region which have revealed no further specimens of this species. This is an important consideration as it changes the context of the conclusions made by [19] and those made in this study. The lack of additional specimens despite the numerous comprehensive surveys in the species known range possibly suggest that this species is extinct.
Morphological differences between C. obsolerus and C. porosus, from the Western Atlantic only, found in this study are considered compelling enough to consider them separate species. This is strengthened by the cranial differences found as well as the detailed dental comparisons made (see S2 Table).

Distribution
The distribution of Carcharhinus obsolerus is uncertain. Given that this species has not been seen in many decades, a better understanding of the distribution of this species is unlikely unless archaeological or paleontological records are found. While Baram in Sarawak is likely an accurate collection locality, both Bangkok and Ho Chi Minh City specimens may have been caught in other South-east Asian locations and brought into these cities where bigger markets exist. Thus, there is a possibility it had a much more restricted distribution than the three known specimens allude to, but it cannot be ruled out that it had a wider distribution in the South-east Asian region.

Conservation implications
Carcharhinus obsolerus n. sp. has not been collected or identified in the field since 1934. Extensive fish market surveys conducted during the past two decades have found no recent specimens of this species. It was not recorded in surveys of chondrichthyan fishes around Borneo, including in Baram where one of the paratypes were collected [34], or during market surveys in areas adjacent to its range, including Indonesia [35] and the Philippines [17,36].
While the lack of contemporary records of C. obsolerus is of great concern for its conservation status, there is a possibility that further specimens are identified in the future. The rediscovery of C. borneensis in 2004 in Sarawak, Borneo [21] demonstrates that "lost" marine species may still be extant despite a long absence of records. That species had not been recorded since 1937.
The lack of records restricts an accurate assessment of the life history parameters and habitat requirements of C. obsolerus. Species of the C. porosus subgroup are relatively small-bodied, but available biological data implies limited productivity. Carcharhinus porosus reaches sexual maturity at 6 years, with a longevity of 12 years, and a slow growth rate (k <0.10) [37]. Litter size in that species ranges 2-9, with a gestation period of~1 year [38]. Similarly, a gravid female C. borneensis contained 6 pups [21], also suggesting limited fecundity.
Species of the C. porosus subgroup generally occur in shallow coastal waters [33], which are accessible to fisheries. The areas from which the three known C. obsolerus specimens were collected, Thailand, Vietnam, and Borneo, are subject to intense, largely unregulated coastal fisheries. The combination of limited biological productivity, and occurrence in shallow coastal habitats exposed to intense fishing, elevates extinction risk for this group, including C. obsolerus.
Supporting information S1 Table. Vertebral and tooth count summaries for the genus Carcharhinus. Ranges for number of precaudal and total centra, and upper and lower teeth (with number of specimens included in range in parantheses) for members of the genus Carcharhinus. Species groupings follow a combination of information provided in [19] and molecular results in [30]; note these are only provisional subgroupings pending a more detailed phylogenetic revision of this genus. (XLSX) S2