Comparison with fossil and modern squatinoidsnext section
Squatinoids are represented by two monotypical families (Squatinidae, Pseudorhinidae) that comprise Squatina Duméril, 1806 and Pseudorhina Jaekel, 1898, respectively. The family Pseudorhinidae has been erected only recently by Klug and Kriwet (2013) to accommodate the latter genus and its constituent species, P. acanthoderma (Fraas, 1854), P. alifera (von Münster, 1842) and P. frequens (Underwood, 2002). Stratigraphically, these species range from the upper Oxfordian to the lower Tithonian (Upper Jurassic; see Cappetta, 2012). In contrast, all post-Jurassic squatinoids, inclusive of modern angel sharks, have been assigned to Squatina (Squatinidae) (see e.g., Guinot et al., 2012). Klug and Kriwet (2013) estimated the date of the origin of (identifiable characters of) Squatiniformes to lie between 181.74 and 156.2 Ma, and that of Squatinidae to be between 157.59 and 114 Ma, representing ‘soft’ maximum and ‘hard’ minimum age constraints, respectively. The early age of radiation of extant angel shark species was dated at 33.17 ± 9.85 Ma by Stelbrink et al. (2010: Table 6), which overlaps with the Rupelian age of the SVK specimen. In this respect, this particular specimen is of interest in our understanding of modern squatinid diversity as well.
Pseudorhina (i.e., Pseudorhinidae) differs from Squatina (i.e., Squatinidae) by a large number of characters, including a longer anterior fontanelle with a less rounded posterior margin, less concave lateral capsular walls of the otic region and more laterally oriented postorbital processes. Of these three cranial features, only the upper postorbital processes are retained in the SVK chondrocranium. Although not complete in our specimen, the bases of both upper postorbital processes are oriented more anteriorly, which is a morphological feature typical of Squatina (see de Carvalho et al., 2008; Klug and Kriwet, 2013), and consistent with what could be expected for a squatinoid of Oligocene (i.e., post-Jurassic) age. Other characters diagnostic of Pseudorhina comprise proportionally larger vertebral hemicentra, comparably shorter and more tightly connected basiventral processes and a broad labial protuberance (‘apron’ of Cappetta, 1987) of teeth not supported by roots (Claeson, 2008; de Carvalho et al., 2008; Klug and Kriwet, 2013). The relative size of vertebral hemicentra is difficult to assess in the isolated vertebrae from the SVK clay pit, but the anterior vertebrae found at the level that yielded the chondrocranium display relatively robust and long basiventrals (see Fig. 5A-B), which make assignment to Squatina most likely. In addition, squatinoid teeth from the Sint Niklaas Phosphorite Bed are diagnostic of Squatina, in having a slender apron that is supported by the root.
Although chondrocrania of modern angel sharks are generally conservative, de Carvalho et al. (2012) listed several differential characters in three species of Squatina from the southwest Atlantic (i.e., S. argentina (Marini, 1930), S. guggenheim and S. occulta). These include rostral projections, anterior fontanelle, supraorbital crest, upper postorbital process, lower postorbital process, otic capsules, suborbital crest and pterotic process. These diagnostic features prove to be even more revealing when comparing species of Squatina from different geographic origins, which correlates to different clades based on molecular evidence (Stelbrink et al., 2010) (see Figs 6-7-8). In spite of the fact that the SVK chondrocranium is closely similar to those of modern angel sharks, two morphological features might actually fall outside the range of interspecific variation seen in modern Squatina. In the latter, the ventral margin of the occipital region is rectilinear and the occipital hemicentrum is flanked by a pair of swollen occipital condyles that are oriented horizontally, with only their lateral margins slightly bent dorsally (see Fig. 8A-E). In contrast, the ventral margin of the occipital region of the SVK specimen is UUU-shaped and not swollen (see Fig. 8F). Although a broken, slightly oval, wedge-shaped structure is visible ventral to the foramen magnum, there is no clear indication of an occipital hemicentrum in this specimen. However, in modern angel sharks this structure easily detaches in fetal specimens (Claeson and Hilger, 2011) and is only weakly calcified in adults (de Carvalho et al., 2008) which might explain its absence in the SVK specimen. Secondly, the anterior margin of the upper postorbital process is distally expanded in all modern angel sharks (de Carvalho et al., 2012; the present study), forming a completely or nearly closed orbital groove in those species that present a well-developed supraorbital flange (see Figs 6–7; compare de Carvalho et al., 2012). Although the upper postorbital processes are not completely preserved in the SVK specimen, remains of this structure seem rounded in both dorso-ventral and lateral views and thus are not expanded. As a result, the orbital groove was most likely not fully closed. Such horizontal expansion is absent in Jurassic Pseudorhina, and has not yet been observed in Cretaceous species of Squatina either (see Guinot et al., 2012; NHMUK P.12213). Consequently, the distal expansion of the anterior margin of the upper postorbital proces might well represent a derived character for Recent angel sharks only, or at least post-Oligocene ones.
Fig. 6. Interspecific variations in Recent Squatina spp. (A-E) in dorsal view, compared to the fossil specimen (F; IRScNB P.9485). Recent chondrocrania are presented as 3D-reconstructions using CT scanning of S. squatina (A; ERB 1029), S. africana (B; ERB 0971), S. australis (C; ERB 0514), S. dumeril (D; ERB 1026) and S. guggenheim (E; ERB 0881). Species represent the European/North African/Asian (A), South African (B), Australian (C) and North/South American (D-E) clades as defined by Stelbrink et al. (2010). Scale bars equal 20 mm. Abbreviations: AF, anterior fontanelle; CR, cranial roof; EC, epiotic crest; EF, endolymphatic fossa; ELF, endolymphatic foramen; FM, foramen magnum; GB, glossopharygeal base; LPOP, lower postorbital process; OG, orbital groove; OHC, occipital hemicentrum; PEP, preorbital process; RP, rostral projection; SF, supraorbital flange; UPOP, upper postorbital process.
Fig. 7. Interspecific variations in Recent Squatina spp. (A-E) in ventral view, compared to the fossil specimen (F; IRScNB P.9485). Recent chondrocrania are presented as 3D-reconstructions using CT scanning of S. squatina (A; ERB 1029), S. africana (B; ERB 0971), S. australis (C; ERB 0514), S. dumeril (D; ERB 1026) and S. guggenheim (E; ERB 0881). Species represent the European/North African/Asian (A), South African (B), Australian (C) and North/South American (D-E) clades as defined by Stelbrink et al. (2010). Scale bars equal 20 mm. Abbreviations: IX, glossopharygeal nerve foramen; BP, basal plate; GB, glossopharygeal base; ICF, internal carotid artery foramen; LPOP, lower postorbital process; OC, otic capsule; OG, orbital groove; OHC, occipital hemicentrum; PEP, preorbital process; PP, pterotic process; RP, rostral projection; SBC, suborbital crest; UPOP, upper postorbital process.
Fig. 8. Interspecific variations in Recent Squatina spp. (A-E) in occipital view, compared to the fossil specimen (F; IRScNB P.9485). Recent chondrocrania are presented as 3D-reconstructions using CT scanning of S. squatina (A; ERB 1029), S. africana (B; ERB 0971), S. australis (C; ERB 0514), S. dumeril (D; ERB 1026) and S. guggenheim (E; ERB 0881). These represent the European/North African/Asian (A), South African (B), Australian (C) and North/South American (D-E) clades as defined by Stelbrink et al. (2010). Scale bars equal 20 mm. Abbreviations: IX, glossopharygeal nerve foramen; X, vagus nerve foramen; EC, epiotic crest; FM, foramen magnum; LPOP, lower postorbital process; OCC, occipital condyle; OHC, occipital hemicentrum; PEP, preorbital process; UPOP, upper postorbital process; VC, posterior vein foramen; VHJ, ventral margin of hyoid junction.
As a result, the UUU shape of the ventral margin of the occipital region, combined with rounded margins of the upper post orbital process (vs distally expanded), might justify the erection of a new genus to accommodate the SVK chondrocranium. However, in view of the fact that the fossilisation process might have had an impact on the shape of the ventral margin of the occipital region and of the occipital condyles in particular (e.g., shrunk, abraded), and the upper postorbital processes are not completely preserved, we prefer to await the discovery of additional material and/or pieces of evidence (e.g., on brain nerve foramina). Unfortunately, the inner structures of the phosphatic chondrocranium have proved impossible to penetrate by the medical CT scanner available to us.
Oligocene squatinid taxonomy
The fossil record of Squatina comprises at least 35 nominal species, most of them published in the 1800s (Cappetta, 2006). Some are based on (partial) skeletons, but most descriptions rely on isolated teeth or vertebrae only. For isolated material, differential characters are rarely provided and interspecific variation has not been studied. In other cases, new species have been erected merely on the basis of stratigraphic provenance of the material. The naming of new so-called chronospecies, without proper differential diagnosis, was very common at the time, especially for taxa whose (dental) morphology had been quite conservative over time, such as Squatina. Therefore, taxonomic revisions of fossil angel sharks (e.g. Guinot et al., 2012) are called for, particularly post-Mesozoic species. In some cases, assignment of isolated teeth and vertebrae to species is fraught with difficulties, and might even prove impossible (Cappetta, 2012; Herman et al., 2013; the present study). Authors often opt to leave angel shark material in open nomenclature (Squatina sp.), in particular when this originates from strata of Cenozoic age (see Klug and Kriwet, 2013).
However, Oligocene angel shark teeth have often been identified as S. angeloides Van Beneden, 1873 (e.g., Nolf, 1988; Reinecke et al., 2001; Cicimurri and Knight, 2009; Génault, 2012). The same holds true for teeth of Squatina from the SVK clay pit (see van den Bosch, 1981). The original species description by Van Beneden (1873: 384) was based on a collection of unassociated vertebrae from an undocumented locality in Belgium (current whereabouts unknown), not illustrated and described extremely briefly as follows, ‘Squatina angeloïdes. Van Ben. Nous avons des vertèbres en assez grand nombre pour reconstituer une colonne vertébrale plus ou moins complète. Ces vertèbres sont surtout reconnaissable au corps, qui est plus large que haut.’ (We have a large number of vertebrae to reconstruct a vertebral column that is more or less complete. These vertebrae are easy to identify, trunk vertebrae in particular, that are wider than tall). Van Beneden’s description is quite remarkable as new chondrichthyan taxa are rarely based on skeletal elements because such are seldom preserved, especially in strata of Cenozoic age (Mollen, 2010; Mollen and Jagt, 2012). Moreover, isolated skeletal material and, in particular vertebrae, often are undiagnostic, making it unsuitable for describing new taxa. In Van Beneden’s case, we agree that the vertebrae (which are wider than tall) are diagnostic of the genus Squatina, but not of its constituent species (see e.g., Hasse, 1876, 1877, 1882; Ridewood, 1921). Van Beneden, probably aware of this shortcoming, did not provide differential characters to discriminate among species of Squatina. In view of this, we consider S. angeloides to have been based merely on stratigraphic data. Three other angel shark species have been described from Oligocene deposits, all postdating S. angeloides, namely S. beyrichi Noetling, 1885, S. rupeliensis Daimeries, 1889 and S. crecelii Weiler, 1922. The last-named species was based on teeth, whereas the other two were erected on the basis of isolated vertebrae.
Storms (1894) was the first to describe and illustrate teeth (and vertebrae) of Squatina from the Belgian Rupelian (R2c, equalling the Boom Clay Formation, Upper Oligocene), and assigned them to S. angeloides, assuming the vertebrae of Squatina described by Van Beneden had originated from the same level. Although the description provides detailed differential diagnoses with fossil as well as modern angel shark species (at the time, this was very progressive), evidence that teeth and vertebrae stem from the same species of Squatina is lacking. The geographic distribution of modern species of Squatina overlap extensively (Stelbrink et al., 2010), and the material from the Belgian Oligocene might well represent more than a single species.
Unlike Storms (1894), we do not consider the stratigraphic origin of S. angeloides to be beyond doubt. In fact, Van Beneden did not record any stratigraphic data in his description of S. angeloides, nor can the stratigraphic context be deduced from the text beyond doubt. Although Van Beneden’s chapter in Patria Belgica was more or less in reversed stratochronological order, beginning with the Pliocene and ending with the Cretaceous, and most of these sections included references to faunal lists from the same stratum that had been published previously, no clear subdivisions were made in the text, nor was a species list for the Oligocene provided. Moreover, in the text, several species were stated to occur at more than one level, making it unclear which one Van Beneden was discussing at the time. This holds true especially for S. angeloides.
Although rare, most of the elasmobranch skeletal material known from the Belgian Cenozoic originates from the Boom Clay Formation (see Leriche, 1910), supporting Storms’s (1894) assumption. However, in Leriche’s series of papers on fossil fishes from the Belgian Cenozoic, vertebrae of Squatina were recorded from all time intervals; Paleocene (Leriche, 1902: 17; Pl. 1, Figs 21-22), Eocene (Leriche, 1905: 96), Oligocene (Leriche, 1910: 251-252) and Mio-Pliocene (Leriche, 1926: 382, Fig. 163-163a; 383, Fig. 164-164b). A fossil angel shark vertebra donated by Van Beneden to Hasse (1877: 349; 1882: 135), was consistently mislabelled as ‘Pliocaen (Terrain rupel(l)ien)’. Daimeries (1889) noted this conflicting label in Hasse (1882), and favoured the ‘Terrain rupelien’, yet failed to provide arguments for his choice. Subsequently, Daimeries (1889) described this particular specimen as S. rupeliensis, a species erroneously reported by Cappetta (2006: 201) as originating from the Eocene, apparently unaware of Van Beneden’s (1873) description.
In conclusion, the original description of S. angeloides is extremely poor and based on vertebrae of uncertain stratigraphic provenance that are not diagnostic at the species level. The material was not illustrated and its current whereabouts are unknown. In view of the fact that criteria stipulated by the code (ICZN, art. 12.1) are barely met, we consider S. angeloides to be a nomen nudum, and thus unavailable. The same applies for S. rupeliensis the description of which suffers the same shortcomings. However, Daimeries (1889) referred to material mentioned by Hasse (1882). Although a name can be made available by indication (ICZN, art. 12.1), requirements of art. 12.2. are not met. In contrast, Noetling (1885) did provide a proper description of S. beyrichi, inclusive of illustrations and stratigraphic origin of the vertebrae. Although this name is available according to the code, we consider it to be a nomen dubium because angel shark vertebrae are not diagnostic at the species level; in doing so we agree with Cappetta (2006), who rejected the name.