Schroederichthys tenuis Springer

Ulisses L. Gomes, Gerhard O. Peters, Marcelo R. de Carvalho & Otto B. F. Gadig, 2006, Anatomical investigation of the slender catshark Schroederichthys tenuis Springer, 1966, with notes on intrageneric relationships (Chondrichthyes: Carcharhiniformes: Scyliorhinidae)., Zootaxa 1119, pp. 29-58 : 32-51

Schroederichthys tenuis Springer , 1966

(Figs. 1-38, Tables 1-5)

Diagnosis. A differential diagnosis of S. tenuis is provided by Springer (1966, 1979; see also Compagno, 1984; Compagno et al, 2005). The genus Schroederichthys is effectively diagnosed in Springer (1966, 1979) and Compagno (1984, 1988).

Coloration. As in most scyliorhinids, Schroederichthys tenuis presents both spots and saddles dorsally, and a mostly white, pale ventral surface (Figs. 1-11). The spots are smaller than eye diameter, dark, rounded, with regular diameters, and distributed both inside and around the saddles. In adults, there are numerous spots within the saddles and surrounding them from head to first dorsal fin. Juveniles have a reduced number of spots inside the saddles and fused spots around them forming continuous lines. White spots are absent in juveniles. There are three types of saddles, primary (1), secondary (2) and subsaddles (S) (Figs. 1-4, 6-11). Primary saddles are dark, conspicuous, and without major differences between mature and immature specimens. Secondary saddles are found posterior to the first dorsal fin, and are not as dark and as well defined as primary saddles; the pre-interdorsal secondary saddle was not found in juveniles. Subsaddles are located on the paired fins below the lateral line in both adults and juveniles. The color pattern of S. tenuis becomes more faded with growth. The saddles have a strong and bold outline containing few rounded spots in younger specimens, but this outline seems to break with growth, becoming very weak or disappearing completely. The spots inside the saddles become more numerous and may eventually surround or outline the saddle.

Size and sexual maturity. According to our material, male specimens of S. tenuis display the first signs of sexual maturity between 335-407 mm TL, as evidenced by the gradual calcification of internal clasper components, and probably reach full maturity at or before 473 mm TL. Based on material examined, the onset of sexual maturity in females seems to be between 217-373 mm TL (Gomes and de Carvalho, 1995). Sexual dimorphism is apparent in mature specimens in the shape of the mouth, which is more angular in females (Figs. 12, 13, respectively).

Dermal denticles. Dermal denticles are divided into three regions, the denticle crown (DCR), pedicel (PED) and base (BAS) (Figs. 14, 15). In adult specimens, the crown presents an acute medial cusp (MCU). On the opposite side there are mostly four (sometimes three) medial ridges (MRI), with central ridges longer than lateral ones. On the external sides of the base of the medial ridges there are reticulated depressions (RED). The lateral expansions (LEX) are rounded (Figs. 14, 15, 18). In juveniles, the crowns present a very acute medial cusp with superficial medial ridges. Small specimens (to about 200 mm TL) present no lateral expansions, which are present in larger specimens of about 470 mm TL (Figs. 16, 17). Both adults and juveniles present short denticle pedicels and radiate denticle bases. Dermal denticles are imbricated in adults, with the medial cusp of an anterior denticle partially covering the medial ridge of a posterior one. However, in juveniles the denticles are scattered with no superposition (Fig. 16). As shown by Springer (1966, 1979), dermal denticles change shape during ontogeny in many species of scyliorhinids, which is confirmed for S. tenuis .

Dentition. The dentition is typically scyliorhinid, with a well-developed primary cusp (PC) flanked by two or three cusplets (PMC) on each side. There is a basal groove (BG) between the root (RT) and the crown (CR) (Figs. 19-25). The transverse ridges (TR) or striae are present on both inner and outer aspects of the cusp and cusplets. The root is secondarily anaulacorhizid, with a fully closed groove, and has two root lobes with a central foramen (CF). Monognathic heterodonty is present, as teeth near the symphisis present well developed primary cusps (Figs. 19-21) while posterior or commissural teeth present a low primary cusp (posteriormost teeth with a very small central cusp; Fig. 25). Gynandric heterodonty was also found - the principal cusp is more slender and developed in males (Fig. 21) than in females, when corresponding teeth are compared (Fig. 22; the same condition was reported for S. bivius by Goztonyi, 1973). The dental formula of the three first adults captured in 1991 could not be determined due to poor preservation. The dental formula of the holotype is 44/34. Variation was detected in tooth numbers between antimeres in both upper and lower jaws; the dental formula for the nine additional specimens is 28-34 (left), 26-36 (right) / 24-28 (left), 23-28 (right) (Table 2).

Vertebral counts. Vertebral counts range from 139-150 total centra, with 32-36 monospondylous and 107-114 diplospondylous centra (Table 3). Stutter zones of alternating long and short centra were not found. No significant differences in counts were found between males and females.

Springer (1979) reports 138 total vertebrae for the holotype.

Head skeleton. The head skeleton is formed by the neurocranium and visceral skeleton (jaws, labial cartilages, hyomandibulae, and branchial arches) (Figs. 26-28). The palatoquadrate (PQ) and the Meckel's cartilage (MC) are somewhat slender. The palatine process (PP) is low and positioned behind the nasal capsule (NC). Two small and slender labial cartilages (LC) are present laterally at midjaw, and contact each other on lower jaw. The branchial arches are slightly inclined posteriorly.

Cranial morphology. The neurocranium is widest at nasal capsules (NC), and most narrow between orbits (OR) (Figs. 29-31; cranial measurements are presented in Table 4). Rostral cartilages are slender and not hypercalcified in adults. Lateral rostral cartilages (LR) and medial rostral cartilage (MR) are fused at their tips, forming the rostral node (RN). These three cartilages form a relatively short rostrum, with its length about onefourth of nasobasal length. Bases of lateral rostral cartilages are fused to the dorsal aspect of nasal capsules (NC) (Figs. 29-31). The nasal capsules are relatively large and somewhat oval, with broadly expanded nasal apertures (NA), and extend posteriorly from the rostral cartilages to the preorbital process (PR) dorsally and orbital notch (ON) ventrally. The anterior (precerebral) fontanelle (AF) is longer than wide, with well-defined margins, and extends anteriorly in between the nasal capsules (Fig. 29). Two small foramina are dorsolaterally situated on each nasal capsule, anterior to the preorbital process (Fig. 29). The nasal fontanelles (NF) are visible ventrally (Fig. 30).

The cranial roof extends posteriorly from the anterior fontanelle, at the level of the external foramen for the preorbital canal (FOE), to the parietal fossa (PRF) (Fig. 29). The dorsally situated external profundus nerve foramina (FPE) are smaller than the external foramen for the preorbital canal (FOE). The cranial roof is broadly arched between orbits, forming the supraorbital crests which are perfurated anteriorly by the large external foramina for the preorbital canal and the external profundus nerve foramina, and by numerous small supraorbital foramina (SOF) along the supraorbital groove (SG) (Fig. 29). The basal plate is flat, and lacks both the ectethmoid condyle and subethmoid fossa (Fig. 30), and is very narrow across the prominent orbital notches (ON). The basal plate originates behind the nasal apertures anteriorly, and extends posteriorly to the level of the stapedial foramen. The greatest width across suborbital shelves (SS), at the level of the postorbital processes (PT), is about two-thirds of nasobasal length. Two pairs of arterial foramina are present posteriorlly on the basal plate, one pair for the internal carotids (ICF) and one for the stapedial arteries (SF). The suborbital shelf is laterally straight.

The orbits are broadly oval in lateral view (Fig. 31). The orbital (or prootic) fissure (ORF) is the largest orbital foramen, located posteroventrally anterior to the otic capsule. The small orbital artery foramen (OF) is ventral to the orbital fissure, and the interorbital canal for posterior cerebral vein (IOC) is anterior to it. The foramen for the efferent spiracular artery (FES) is near the suborbital shelf, anterior to the interorbital canal. Almost directly dorsal to the efferent spiracular artery is the oculomotor nerve foramen (III). The orbitonasal foramen (ONF) is just posterior to the nasal capsule and close to the suborbital shelf. Posterior to the orbitonasal foramen is the well developed optic nerve foramen (II), and directly above it is the foramen for the anterior cerebral vein (FCV). The orbital foramen for the deep ophthalmic nerve (FPI) is located ventrally within the orbit, just dorsal to the orbitonasal foramen. The orbital foramen for the preorbital canal (FOI) is positioned more dorsally near the preorbital process. Posteriorly there are two small foramina, the trochlear nerve foramen (IV) and posterior to it the orbitocerebral foramen for the deep ophthalmic nerve (FPC). The foramen for the superficial ophthalmic nerve (FOC) is located near the postorbital process (PT).

The otic capsules are relatively short, located in between postorbital processes (PT) and occipital region (Figs. 29-31). The otic capsules are not greatly expanded or inflated, their greatest width just greater than one-half of nasobasal length. Dorsally on the otic capsules are the pterotic process (FTP) posterior to the postorbital process, and the sphenopterotic ridge (SR) posterior to the pterotic process. In the center of the otic capsule, the parietal fossa (PRF) bears anteriorly a pair of endolymphatic foramina (FEN) and posteriorly a pair of perilymphatic foramina (FPN). Lateral to these foramina are the anterior semicircular canals (ASC), followed by the posterior semicircular canals (PSC). Laterally, the hyomandibular facet (HF) is well defined, small and horizontally elongate. The opisthotic ridge (ORI) forms the superior margin of the hyomandibular facet. The occipital region presents low and short occiptal condyles (OCC) that do not project posteriorly, with the occipital centrum located in between (OCN). The foramen magnum (FM) is subtriangular. The vagus (X) and glossopharyngeal (IX) nerve foramina are ventrally positioned (Figs. 29, 30, 32).

Hyomandibular and branchial skeleton. The hyomandibular arch is formed by the hyomandibula (HMB), ceratohyal (CH), and basihyal (BH). The hyomandibula is short, about one-half as long as the ceratohyal cartilage. Its ventral extremity articulates with the ceratohyal, and its dorsal aspect articulates with the hyomandibular facet (HF) of the neurocranium (Fig. 31). The ventral portion of the ceratohyal is slightly wider than its dorsal segment, and articulates with the lateral aspect of the basyhial. The basihyal (BH) is a flat plate, widest at its posterior two-thirds, and tapers posteriorly where it contacts the ceratohyals.

The branchial arches are composed of pharyngobranchials (PB), epibranchials (EB), ceratobranchials (CB), hypobranchials (HB), and the basibranchial copula (BBC). There are four independent pharyngobranchials (PB 1-4), all directed posteriorly (Figs. 26, 27, 33). The first and second pharyngobranchials are the longest, and the fourth is the shortest.

The third pharyngobranchial is bifurcated at its base (probably because it incorporates the fourth epibranchial). The fourth and fifth pharyngobranchials may be fused, forming a compound posterior pharyngobranchial element. There are five epibranchials (EB 1-5); the longest are the first and second, while the shortest are the third and fifth. The fourth epibranchial is probably fused to the posterior branch of the third pharyngobranchial (Fig. 33). The five ceratobranchials (CB 1-5) are directed backwards and are about equal in length (Fig. 33). Ceratobranchials 2-3 are widest ventrally where they articulate with the hypobranchials; their ventral segments overlap the anterior portion of the subsequent ceratobranchial. Ceratobranchials 2-4 articulate with hypobranchials ventrally, but ceratobranchial 5 articulates directly with the basibranchial copula (BBC) (Fig. 33). Hypobranchials 2-4 are directed posteriorly towards the basibranchial copula. The first hypobranchial element is lacking, as is an isolated fifth hypobranchial (which is probably incorporated into the basibranchial copula). The second and third hypobranchials are longer and about equal in size, and do not touch the basibranchial copula (their posterior extremities meet each other medially); the fourth hypobranchial is the smallest and its posterior extremity articulates with the anterior portion of the basbranchial copula (Fig. 33). The basibranchial copula is flat, rounded anteriorly, and pointed posteriorly. It articulates laterally with the fourth hypobranchial and the fifth ceratobranchial (Fig. 33).

Claspers. Externally, the claspers are tubular with the glans ending in a pointed extremity. On the clasper shaft, the medial wall (MW, new term) covers the dorsal marginal cartilage (RD) while the lateral wall (LW, new term) covers the ventral marginal cartilage (RV). The clasper groove (CG) is located between the medial and lateral walls (Fig. 34). Anterodorsally, the clasper groove originates at the apopyle (AP), the receiving port of the clasper. Some structures of the external clasper glans are directly supported by skeletal components (Figs. 34, 35). The apex is formed laterally by the lateral terminal margin (LT, new term), which is supported internally by the ventral terminal cartilage, and medially by the medial terminal margin (MT, new term), which is supported by the dorsal terminal cartilage. The rhipidion (RH), situated between the lateral and ventral terminal margins, is an anteroposteriorly elongated flap on the floor of the glans, supported internally by the dorsal terminal 2 cartilage (Fig. 34). The envelope (EN), a medial extension of the lateral wall that covers part of the clasper groove, is a rounded, fleshy and soft flap with no internal support. The exorhipidion (ERH) is a longitudinally elongated and fleshy blade that covers the ventral terminal 2 cartilage and part of the ventral terminal cartilage. It is located laterally between the envelope and the lateral terminal margin (Fig. 34). The cover rhipidion (CRH) is located opposite the exorhipidion, and is an extension of the dorsomedial margin, internally supported by the accessory dorsal marginal cartilage. The pseudosiphon (PSS) is a dorsally opening, blind pocket in the posterior edge of the cover rhipidion, along the medial edge of the clasper. The hypopyle (HP) is the posterior opening of the clasper groove between the cover rhipidion and exorhipidion, anterior to the rhipidion. Dermal denticles (DD) are present on the internal side of the medial wall, envelope, and medial and lateral terminal margins, respectively (Figs. 34, 35).

A single intermediate segment (B1) and beta cartilage (β) are present dorsally in the clasper skeleton, both articulating with the basipterygium (Figs. 36, 37). In dorsal view, the preglans clasper is composed of a pair of semicylindrical marginal cartilages, the dorsal marginal (RD) and the ventral marginal (RV) (Fig. 36). The clasper groove (CG) is located in between the marginal cartilages. In ventral view, the pre-glans clasper is formed by three cartilages, with the axial cartilage (AX), an elongated and flattened rod, fused on both sides to the marginal cartilages (Fig. 37).

Five main cartilages are present in the clasper glans: ventral terminal (TV), ventral terminal 2 (TV 2), dorsal terminal (TD), dorsal terminal 2 (TD 2), and acessory dorsal marginal (RD 2) (Figs. 36, 37). The ventral terminal, the dorsal terminal and the ventral terminal 2 cartilages are lanceolate with pointed apices. The ventral terminal dorsally (Fig. 36), and the ventral terminal 2 ventrally (Fig. 37), are attached to the ventral marginal cartilage. In dorsal view, the subtriangular accessory dorsal marginal cartilage is attached to the dorsal marginal, as is the dorsal terminal cartilage ventrally. The dorsal terminal 2 cartilage lies between the accessory dorsal marginal and the ventral terminal 2, is poorly calcified, and is attached to the floor of the glans. Attached to the dorsal terminal is the small dorsal terminal acessory cartilage (TDA) (Figs. 36, 37). Four small cartilages are visible dorsally (Fig. 37). On the dorsal surface of the accessory dorsal cartilage there are two small elements. The anterior and smallest piece is here termed the accessory marginal cartilage 2 (RD 3). The largest element is here termed the accessory marginal cartilage 3 (RD 4), and is about three times the size of the accessory marginal cartilage 2. Both structures were found also in S. saurisqualus . Dorsally, between the ventral marginal and the ventral terminal 2 cartilages, are two small cartilages here designated the ventral terminal 3 (TV 3) for the internal piece, and the ventral terminal 4 (TV 4) for the external element.

Pectoral skeleton. The pectoral fin skeleton is aplesodic (Fig. 38) with elongated ceratotrichia, which are longer than the fin endoskeleton. The propterygium (PRO) is short with one proximal (PRA), one intermediate (IRA), and one distal (DRA) radial segment. The mesopterygium (MES) is subtriangular, and bears three proximal radial segments fused at their bases. Distally, each proximal radial articulates with one intermediate and one distal radial. The metapterygium (MET) is the largest basal cartilage, articulating with eight proximal radial segments, each with one intermediate and one distal radial segment. The metapterygial axis (MTS) is composed of shorter elements with two segments contacting the metapterygium and two distal segments. There are 12 total radial pieces (pro + meso + metapterygium) (Table 5).

Results and Discussion

Morphological comparisons. Compagno’s (1984) estimate that adults of S. tenuis reach 700 mm TL was based on the Schroederichthys specimen from southeastern Brazil deposited in Hamburg and mistakenly identified as S. tenuis by G. Krefft (see “Introduction” above; Springer, 1979). Specimens of this species ( S. saurisqualus ) that we examined, including the Hamburg individual, measured 578-590 mm TL, and are all sexually mature. Our observations indicate that S. tenuis reaches a maximum total length of probably under 500 mm, and that adults definitely have a strongly attenuated body. Species of Schroederichthys fall within two size classes, one for the small-sized species S. tenuis and S. maculatus (with maximum known total lengths 473 mm and 340 mm, respectively), and one including the large-sized species S. bivius , S. chilensis , and S. saurisqualus (reaching 700 mm TL, 620 mm TL, and 600 mm TL, respectively); we believe, however, that S. saurisqualus is more closely related to S. tenuis and S. maculatus , as detailed below.

According to Springer (1966, 1979) and Compagno (1988), S. chilensis has the highest tooth count (62/56) among congeners, with S. maculatus intermediate (48-53/36-42) and S. tenuis with the lowest number of rows (44/34 in the holotype and 26-34/23-29 in the additional specimens examined; no data were available for S. bivius ). Gosztonyi (1973) described for S. bivius from Argentina the same secondary sexual dimorfism in jaw shape reported here for S. tenuis , which is common among scyliorhinids (Brough, 1937; Nakaya, 1975; Springer, 1979; Gomes and Tomás, 1991; Ellis and Scharley, 1995).

Vertebral counts are less reliable to separate species of Schroederichthys . Vertebral numbers are higher in adults of S. tenuis than in the type specimens (both juveniles), but this is probably artificial as counts in juveniles may be negatively affected by weaker calcification (the types of S. tenuis have 139-141 centra while in adults counts range from 145-150). Compared to S. chilensis (135-139) and S. maculatus (133-145), Table 3 shows no significant differences between them (data also from Springer, 1979; Compagno, 1988). A specimen of S. bivius (MNHN 1990-1020, a mature female) has slightly higher counts at 153 centra (33 monospondylic and 120 diplospondylic).

Neurocranial morphology is fairly distinct between S. chilensis and S. maculatus , as shown by Compagno (1988: fig. 13.6). The cranial topography of S. tenuis is very similar to S. maculatus and S. saurisqualus in being relatively straight between the supraorbital crests, in the shape of the nasal capsules and nasal apertures, size and shape of the anterior fontanelle, width of the basal plate, and in the presence of a longitudinal groove between the anterior fontanelle and the base of the rostral cartilages between the nasal capsules (the neurocranium of S. bivius was not seen). Laterally, the cranial roof as well as the supraorbital crests of S. tenuis are both arched, but in S. chilensis these are straight as described by Leible et al. (1982).

The only description of branchial elements in other species of Schroederichthys is that of Leible et al. (1982) for S. chilensis , which is generally similar to S. tenuis . There are differences mainly in the shape and position of the basihyal (longer than wide and articulating posterolaterally with the ceratohyal in S. tenuis , but wider than long and overlapping the ceratohyal in S. chilensis ). The base of the third pharyngobranchial is not bifurcated in S. chilensis as it is in S. tenuis . The basibranchial cartilage is unsegmented in S. tenuis , and does not articulate with the second and third hypobranchials, whereas in S. chilensis the basibranchial is longer, segmented, and articulates with the second to the fourth hypobranchials.

Compagno (1988) described the accessory dorsal terminal 2 cartilage in carcharhinoid sharks as being present in Rhizoprionodon acutus , Halaelurus buergeri , and Halaelurus natalensis . Cunha and Gomes (1994) described this structure also for Rhizoprionodon lalandii and R. porosus . In the present study the accessory dorsal terminal 2 cartilage, as well as a structure herein termed the accessory dorsal terminal 3 cartilage, were found in Schroederichthys tenuis and S. saurisqualus . Compagno (1988) affirms that the ventral terminal 2 cartilage is absent in S. chilensis and present in S. maculatus ; this cartilage is present in S. tenuis and S. saurisqualus according to our observations. According to Compagno (1988), the ventral terminal 3 is present in several scyliorhinids and Leptocharias , and the ventral terminal 4 cartilage occurs in some Galeus spp. and Halaelurus spp. (both scyliorhinid genera). Both cartilages occur in S. tenuis . Compagno (1988) verified that the exorhipidion is supported internally by the ventral terminal 2 cartilage; however, both S. tenuis and S. saurisqualus have a fleshy exorhipidion without a specific endoskeletal support, and which overlies the ventral terminal and part of the ventral terminal 2 cartilages.

The arrangement of the pectoral skeleton of S. tenuis is similar to S. chilensis as described by Leible et. al (1982) (undescribed for S. maculatus and S. bivius ). The number of radial cartilages increases from pro- to metapterygium in species of Schroederichthys , with S. bivius reaching the highest number and S. tenuis the lowest (Table 5). More data are required to establish if pectoral radial counts are useful to separate species of Schroederichthys .

Phylogenetic relationships within Schroederichthys . According to Melendez et al. (1993), Compagno (1999a) and Compagno et al. (2005), five species of Schroederichthys are presently recognized: S. bivius (Smith, 1838), S. chilensis (Guichenot, 1848), S. maculatus Springer, 1966, S. tenuis Springer, 1966, and S. saurisqualus Soto, 2003. Our study supports preliminary results that S. maculatus , S. tenuis and S. saurisqualus form a monophyletic group, and that S. bivius (Smith, 1838) and S. chilensis (Guichenot, 1848) should be removed from the genus (de Carvalho and Gomes, in prep.). S. maculatus , S. tenuis and S. saurisqualus , as mentioned above, share anteroposteriorly elongated nasal apertures and nasal capsules, bulging nasal capsules that abruptly meet at their dorsal midline leaving a dorsal longitudinal groove, anteriorly oval anterior (precerebral) fontanelle with well-defined margins, presence of a small median protuberance at posterior border of anterior fontanelle, slender and laterally compressed neurocranium, slender basal plate, strongly tapered and elongated postpelvic trunk region, among other characters. These features are considered to be derived within the Scyliorhinidae, even though a posterior median protuberance is present in the anterior fontanelle of some species of Poroderma , Halaelurus , Holohalaelurus , and Haploblepharus (probably independently), and Asymbolus analis also has somewhat bulging and elongated nasal capsules, even though these are distinct from S. maculatus , S. tenuis and S. saurisqualus (Compagno, 1988). The distribution of the ventral terminal 2 cartilage, present in S. maculatus , S. tenuis and S. saurisqualus , is presently unknown within the Scyliorhinidae, as is the accessory dorsal terminal 3 cartilage, reported here in S. tenuis and S. saurisqualus (unknown for S. maculatus ). There are also significant distinctions in the gill arch skeleton of S. tenuis and S. chilensis , but the branchial skeleton of other species of Schroederichthys needs to be described to reveal if it supports the monophyly of S. maculatus , S. tenuis and S. saurisqualus . The nasal flap of S. saurisqualus is broad and more similar to that of S. maculatus than to the elongated nasal flap of S. tenuis , but the phylogenetic significance of nasal flap morphology is questionable, as S. bivius has nasal flaps resembling S. tenuis and S. chilensis has nasal flaps more similar to S. maculatus . Gomes and de Carvalho (1995) reported that the suedelike texture, opacity and color of the egg-capsules of S. maculatus and S. tenuis was derived, a condition later found in S. saurisqualus but not in S. bivius and S. chilensis (Soto, 2003), further corroborating the monophyly of S. maculatus , S. tenuis and S. saurisqualus . Historically, S. bivius and S. chilensis have been placed either in Halaelurus , Scyliorhinus or Schroederichthys (for a review of their classification, see Springer, 1979; Compagno, 1988), but in our view their systematic fate is still undetermined within the family.