Introduction

Sphenacodontidae represented a major component of early Permian terrestrial ecosystems as apex predators (Olson 1961, 1966, 1977). These synapsids were widely distributed in North America and Western Europe, though their remains are most common in the United States (Eberth 1985; Olson 1962; Reisz 1986; Romer and Price 1940). Sphenacodontids are also well known for being the closest relatives of therapsids, so their study is crucial to understand the early evolution of synapsids (Amson and Laurin 2011; Fröbisch et al. 2011; Hopson 1991; Kemp 1982; Reisz et al. 1992; Sidor and Hopson 1998). Six sphenacodontid genera are currently recognized: Sphenacodon Marsh, 1878, Dimetrodon Cope, 1878a, Ctenospondylus Romer, 1936, Secodontosaurus Romer, 1936, Ctenorhachis Hook and Hotton, 1991, and Cryptovenator Fröbisch, Schoch, Müller, Schindler, and Schweiss, 2011 (Berman 1977, 1978; Berman et al. 2001, 2004b; Eberth 1985; Evans et al. 2009; Fröbisch et al. 2011; Hook and Hotton 1991; Olson 1962; Reisz et al. 1992; Romer and Price 1940; Sidor and Hopson 1995). All these taxa were discovered in the United States except for two recently described German forms: Dimetrodon teutonis Berman, Reisz, Martens, and Henrici, 2001 from the Lower Rotliegend of Thuringia (Berman et al. 2001, 2004b) and Cryptovenator hirschbergeri Fröbisch, Schoch, Müller, Schindler, and Schweiss, 2011 from the Gzhelian of the Saar-Nahe Basin (Fröbisch et al. 2011). Additional taxa were named on fragmentary material: the Late Carboniferous Macromerion schwarzenbergii (Frič, 1875), from the Czech Republic (Romer 1945); the latest Carboniferous-earliest Permian Neosaurus cynodus (Gervais, 1869), from France (Romer and Price 1940) and the early Permian Bathygnathus borealis Leidy, 1854 from Canada (Case 1905) and “Sphenacodon” britannicus from the United Kingdom (Paton 1974). Even if these taxa are sphenacodontids, their validity has been questioned (Eberth 1985). Other potential sphenacodontids are Steppesaurus gurleyi Olson and Beerbower, 1953, Eosyodon hudsoni Olson, 1962, and Gorgodon minutus Olson, 1962, all from the early Permian of the USA. The three of them were originally described as early representatives of the therapsids (Olson 1962; Olson and Beerbower 1953), but they have since been reinterpreted as badly deformed sphenacodontid specimens (Sidor and Hopson 1995). Given the absence of anatomical evidence supporting these claims, a detailed redescription of this material is necessary. For now, none of these taxa will be considered in this study.

The only French sphenacodontid known to date is the so-called Neosaurus cynodus represented by a single partial maxilla and its impression, HN004 2009-00-1, collected in “Autunian” red beds of the La Serre Massif area, Eastern France. This specimen has a complex taxonomic history. It was originally described by Coquand (1857, 1858) as pertaining to the German diapsid Protorosaurus speneri on the basis of its thecodont dentition. After re-examining this specimen, however, Gervais (1869) rejected Coquand's identification, because Protorosaurus differs in having equally separated teeth (i.e., no diastema) and no caniniform teeth. Gervais then erected a new species for HN004 2009-00-1 that he included tentatively in the genus Geosaurus, a Jurassic thalattosuchian, as ?Geosaurus cynodus.

Following the discovery of new sphenacodontid material in the United States, Baur and Case (1899) pointed out that “Geosaurus” cynodus is definitely not a crocodylomorph, but more likely an early synapsid (“pelycosaur”). They also noted that it is seemingly distinct from the ophiacodontid Stereorachis dominans, from the nearby Autun Basin. Case (1907) was more skeptical about its assignment, but recognized “Geosaurus” cynodus as similar to his “poliosaurids”, a group interpreted now as a mix of ophiacodontids and sphenacodontids (Romer and Price 1940).

On the basis of a restudy of HN004 2009-00-1, Thévenin (1910) provisionally assigned Geosaurus cynodus to Stereorachis, but conceded nevertheless its closer affinities with the small Dimetrodon natalis, rather than Stereorachis dominans, based on its compressed cutting teeth. Similarly, later authors compared ?Geosaurus cynodus to both ophiacodontids and sphenacodontids (e.g., Huene 1925; Nopcsa 1923; Watson 1917), as several members of Ophiacodontidae were indeed placed in Sphenacodontidae and vice versa at this time.

In a discussion of Dimetrodon and its relatives, Nopcsa (1923) erected a new genus, Neosaurus, to accommodate Gervais' (1869) species. Though Nopcsa gave no justification, this was later accepted by Romer and Price (1940). They regarded Neosaurus as a primitive sphenacodontid, but unusual in retaining a high number of precaniniforms and a low number of postcaniniforms, but comparable to Dimetrodon natalis in size and in having a weak maxillary step. They suggested the species Neosaurus cynodus might actually pertain to one of the better-known sphenacodontids, Sphenacodon or Dimetrodon-at that time, no skull material was referred to Ctenospondylus. Romer and Price (1940) also proposed an alternative hypothesis in which Neosaurus would have arisen independently from European “haptodontines”, because of their similar reduced number of postcaniniforms.

Neosaurus has not been restudied since then, although frequently mentioned in the literature (e.g., Berman et al. 2000b; Devillers 1961; Eberth 1985; Heyler 1969, 1987; Langston 1963; Watson 1954; Reisz 1986). Most followed Romer and Price's (1940) statements, except Heyler (1969, 1987) and Campy et al. (1983), who did not even cite their work, and Eberth (1985) who more thoroughly discussed the validity of Neosaurus (see below). So far, the name Neosaurus appeared only once in the French literature, in a review based on Romer and Price's (1940) monograph (Devillers 1961). It was otherwise mentioned as Protosorus speneri [sic!] by Campy et al. (1983) and Farjanel (1989) and as ?Stereorachis by Heyler (1969, 1987).

Finally, the validity of Neosaurus cynodus was discussed by Eberth (1985) in the light of new data regarding major ontogenetic changes of the maxilla shape and tooth count within the genus Sphenacodon. Eberth (1985) stated that the diagnostic features listed by Romer and Price (1940) might be explained if the holotype of N. cynodus is a juvenile of one of the better known, deep-snouted sphenacodontids, Sphenacodon, Ctenospondylus, or Dimetrodon (as already suspected by the latter authors). However, Eberth (1985: 38) also stated that “[w]hile it may be argued that generic assignment of these forms is impossible on the basis of the present material, and that the names are invalid, retaining the generic names as paleogeographical convenience terms is desirable”.

Because it is the second ever described sphenacodontid species (after Bathygnathus borealis), Neosaurus cynodus requires an accurate redescription of its holotype and a re-evaluation of its taxonomic status in order to clarify sphenacodontid nomenclature. Furthermore, the examination of newly prepared, overlooked cranial material from the early Permian Viala Formation suggests sphenacodontids occurred also in the Lodève Basin. A left dentary (MNHN.F.LOD213) collected by Jacques Garric was first mentioned by Heyler (1969) as an indeterminate tetrapod, and by Heyler (2008) as a possible caseid, following the discovery of caseids in the Rodez (Sigogneau-Russell and Russell 1974) and Lodève (Werneburg et al. 2007) basins. Heyler (2008) claimed to have been unable to locate this specimen when he reorganized the MNHN collections from the Lodève Basin between 1996 and 2004. Fortunately, Daniel Heyler had given it before to Jean-Sébastien Steyer (CNRS-MNHN) who entrusted it to Renaud Vacant (MNHN) for preparation. Two undescribed dentaries (UM 5902, 5903) collected by Paul Ellenberger in 1986 were also found in the collections of the Université Montpellier 2 with the help of Suzanne Jicquel (UM), which were prepared in great part by Renaud Vacant and in part by the author.

Institutional abbreviations.—AMNH, American Museum of Natural History, New York, USA; ANSP, Academy of Natural Sciences of Drexel University, Philadelphia, USA; CNRS, Centre National de la Recherche Scientifique, Paris, France; HN, Muséum d'Histoire Naturelle de Besançon, Besançon, France; MCZ, Museum of Comparative Zoology, Harvard, USA; MNHN, Muséum National d'Histoire Naturelle, Paris, France; UM, Université Montpellier 2, Hérault, France; YPM, Yale Peabody Museum, New Haven, USA.

Fig. 1.

Sphenacodontid synapsid Neosaurus cynodus (Gervais, 1869), holotype, from Moissey, Late Gzhelian—Asselian. A. Left maxilla (HN004 2009-00-1A) in lateral view. B. Corresponding impression (HN004 2009-00-1B) in lateral view. Drawings by Peggy Vincent.

Systematic palaeontology

Remarks.—The terminology used in the descriptions found below follows the standardized nomenclature proposed by Smith and Dodson (2003) for vertebrate dentition.

Fig. 2.

Sphenacodontid synapsid Neosaurus cynodus (Gervais, 1869), holotype (HN004 2009-00-1), from Moissey, Late Gzhelian-Asselian. Schematic comparison between the structure preserved in bone and impression.

Fig. 3.

Unidentified sphenacodontids. A. Sphenacodontidae indet. 1, left dentary (MNHN.F.LOD213), from Saint-Julien, Sakmarian, in lateral view. B. Sphenacodontidae indet. 2, right dentary (UM 5902), from Le Capitoul, Sakmarian, in medial view. C, D. Sphenacodontidae indet. 3, right dentary (UM 5903), from Saint-Julien, Sakmarian, in lateral (C) and medial (D) views. Photographs (C₁, D₁), explanatory drawings (C₂, D₂).

Discussion

Taxonomy

Taxonomic status of Neosaurus cynodus.—Romer and Price (1940) provided a diagnosis for Neosaurus cynodus with the following characters: (i) low maxillary step, (ii) four precaniniform teeth, and (iii) ten postcaniniform teeth. The combination of primitive and derived sphenacodontian features led them to emphasize its probable intermediate position between their “Haptodus” (now paraphyletic; see Laurin 1993) and other sphenacodontids, a view followed by subsequent authors (Berman 1978; Currie 1979; Reisz 1986). Their diagnosis was, however, justifiably questioned by Eberth (1985: 37) in his restudy of the cranial anatomy of Sphenacodon ferocior. Indeed, he noted that diagnostic characters of the dentition and maxilla, on which Romer and Price (1940) relied, vary considerably during ontogeny in both S. ferocior and S. ferox. The maxilla, for instance, expands ventrally at the level of the caniniforms but narrows more anteriorly in such a way that the tooth row forms a kind of step anterior to the caniniforms and becomes increasingly concave posteroventrally. In the youngest individuals of S. ferox and S. ferocior, the step and concavity of the tooth row are therefore barely present, whereas they become prominent features in the largest individuals according to Eberth (1985: 33, fig. 36). He concluded that the three diagnostic characters offered by Romer and Price (1940) should be discarded, arguing that they may reflect the juvenile stage of the holotype of N. cynodus.

The lack of serrations on the marginal dentition of HN004 2009-00-1, despite its fairly good preservation, shows that Neosaurus cynodus is distinct from at least Bathygnathus borealis (ASNP 9524), Dimetrodon incisivus (AMNH FR 4116), and D. semiradicatus (AMNH FR 4001).

In conclusion, there are no features to distinguish Neosaurus from all other sphenacodontids because a juvenile stage of development of the holotype cannot be ruled out, and because the lack of axial material precludes an assignment to one or another of the better known genera of the family (i.e., Sphenacodon, Ctenospondylus, Dimetrodon, and Secodontosaurus). Therefore, despite minor disagreements with previous comparisons, this work supports the conclusion of Eberth (1985) in considering the species Neosaurus cynodus as a nomen dubium and its holotype HN004 2009-00-1 as a Sphenacodontidae indeterminate.

Table 1.

Precaniniform (prec.) and postcaniniform (postc.) counts in sphenacodonts. A plus sign indicates minimum values for taxa in which the complete tooth count is unknown.

Identification of MNHN.F.LOD213, UM 5902, and UM 5903.—Examination of these specimens offers no support for assignment to any of the previously described sphenacodontid taxa. This is mainly because many features of the feeding apparatus (jaws and dentition) of sphenacodontids are not only related with each other, but are also dependent on size and ontogeny (Eberth 1985; Reisz et al. 1992; Romer and Price 1940) and are therefore of little help in taxonomy (contra Fröbisch et al. 2011). In addition, poor preservation precludes the detection of serrations on their teeth. MNHN.F.LOD213, UM 5902, and UM 5903 are, therefore, considered as Sphenacodontidae indeterminate.

Paleoecology and paleoenvironments

Sphenacodontids are a major component of North American early Permian tetrapod faunas (Olson 1958, 1961, 1977; Romer and Price 1940; Vaughn 1966, 1970), but they remain exceedingly rare in Europe. The restriction of Sphenacodon to New Mexico and Dimetrodon and Ctenospondylus to northern Texas had long been explained by the presence of a geographical barrier precluding faunal exchanges (Romer and Price 1940). Subsequent discoveries in the Four Corners area (where Arizona, Colorado, New Mexico, and Utah meet) but also in Ohio have indicated that the biogeography of these genera is more complex and cannot be merely explained by the presence of a fluctuating seaway. Ctenospondylus and Dimetrodon material have indeed been collected from lower Permian deposits of the Four Corners (Sumida et al. 1999; Vaughn 1964, 1966). Dimetrodon has been also found in earlier strata from New Mexico that may be Pennsylvanian (Berman 1977, 1993; Vaughn 1970). In addition, Sphenacodon is not restricted to New Mexico as a result of finds from Arizona (Vaughn 1966) and Utah (Sumida et al. 1999), although this genus is still unknown in Texas. Vertebrate assemblages that were previously considered as typical of northern Texas have been found in many areas of the Four Corners (Vaughn 1966, 1970). Similar assemblages have been recognized in the uppermost Pennsylvanian to lower Permian Dunkard Group of the Tri-State area (where Ohio, West Virginia, and Pennsylvania meet), which has yielded specimens referred to a distinct species of Ctenospondylus, C. ninevehensis, and to Dimetrodon cf. limbatus (Berman 1978; Olson 1970, 1975). Several hypotheses have been proposed to explain the biogeographical evolution of the Tri-State and Midcontinent vertebrate fauna, such as the presence of a faunal corridor or some kind of selective geographical barrier, but none of them could be directly tested because Upper Pennsylvanian to lower Permian outcrops are lacking in the Central United States (Berman 1978).

Regardless, these discoveries led Vaughn (1966, 1970) to suggest that the Midcontinental Seaway separating the Four Corners and Texas acted at most as a filter and instead proposed that these differences in relative abundances are the result of different paleoecological preferences. Dimetrodon was for instance labeled as a “truly deltaic marker” (Vaughn 1970) that would have preferred lowland coastal areas in contrast to the more upland Sphenacodon (Vaughn 1966), a hypothesis confirmed by Olson (1958, 1977). Indeed, Olson (1958) discovered that Dimetrodon also occurs in channel deposits, but that it is especially common among lacustrine vertebrate assemblages where it is represented by isolated, complete bones and partly articulated skeletons on the margins, but only by isolated, fragmentary remains in offshore deposits. Dimetrodon was a common inhabitant of early Permian flood plains (Olson 1958, 1977; Sander 1987, 1989). It was the largest and one of the most abundant predators at that time, preying upon other large vertebrates living in lakes or in their vicinities, including xenacanthids or Diplocaulus (Olson 1961, 1977). The limited data regarding the taphonomy of Ctenospondylus indicates that it was a rare component of an amphibious to aquatic pond or lake fauna and that its remains had been transported a relatively short distance before being deposited (Berman 1978). These data suggest that Ctenospondylus had a similar ecology.

Regarding the ecology of sphenacodontids, two localities are informative: the lower Permian Richards Spur (or Fort Sill) locality, Oklahoma, and the Bromacker Quarry, Germany, in which sphenacodontid remains are rare in comparison with other tetrapods (Berman et al. 2001, 2004b; Evans et al. 2009). Both localities have yielded an abundant and diverse tetrapod fauna, including dissorophoid temnospondyls, “microsaur” lepospondyls, Seymouria, diadectids, bolosaurid parareptiles, captorhinid eureptiles, and caseid, varanopid, and sphenacodontid synapsids (e.g., Heaton 1979; Boy and Martens 1991; Modesto 1996; Berman et al. 1998, 2000a, b, 2001, 2004a, b, 2011; Sumida et al. 1998; Sullivan and Reisz 1999; Eberth et al. 2000; Sullivan et al. 2000; Reisz and Sutherland 2001; Kissel et al. 2002; Reisz et al. 2002; Reisz 2005; Maddin et al. 2006; Müller et al. 2006; Anderson et al. 2008, 2009; Evans et al. 2009; Henrici et al. 2011; Fröbisch and Reisz 2012; Anderson and Bolt 2013). These terrestrial assemblages indicate an “upland” paleoenvironment for both the Richards Spur and Bromacker localities in contrast with the contemporaneous more lowland faunas of North America (Eberth et al. 2000). Stratigraphic and sedimentological data suggest a depositional environment in which sheet flooding alternated seasonally with the sedimentation of suspended fines in temporary lakes and ponds, in association with a hot, semi-arid climate, for the Tambach Formation at Bromacker (Eberth et al. 2000). There is little information regarding the depositional environment of the fissure-fill deposits of Richards Spur, but streams or standing bodies of water were apparently rare in this area (Olson 1991; Sullivan and Reisz 1999). Even if these two localities share many taxa, the Bromacker tetrapod assemblage was recognized as an original, early stage in the development of a modern terrestrial trophic ecosystem dominated by plantivorous tetrapods (Eberth et al. 2000). This is not the case of the Richards Spur tetrapod assemblage. It is easy to distinguish these two assemblages using the relative abundance of tetrapods. Diadectids are the most frequent tetrapods in Bromacker (Eberth et al. 2000) whereas captorhinids overwhelmingly dominate in Richards Spur (Sullivan and Reisz 1999). Sphenacodontids are the most common synapsids in Bromacker, with one species represented by five specimens, whereas only a single varanopid specimen has been recovered (Berman et al. 2001, 2004b). Conversely, varanopids are not uncommon in Richards Spur (Evans et al. 2009; Maddin et al. 2006), whereas sphenacodontids are scarce (Evans et al. 2009).

The abundance of sphenacodontids appears therefore to be strongly environmentally controlled, a suggestion that may account in large part for their rarity in Europe (Table 2). Though the Gorges de Moissey locality has yielded an interesting macroflora, the only animal remains it has produced consist of indeterminate bivalve internal casts and the holotype of Neosaurus cynodus (Coquand 1857, 1858; Corsin and Devaux 1959; Ogérien 1867; Pidancet 1863). The lower Viala Formation, which has yielded the Lodève sphenacodontids, offers much greater palaeoecological information. These specimens were collected from the α and β bone breccias in which disarticulated bones are mixed together and embedded in a red silty matrix. These breccias resulted, according to Garric (2002), from marked water level fluctuations, causing the death en masse of the aquatic fauna, notably branchiosaurids, during droughts. Larger, more resistant bones would have been deposited with reworked bones as water levels rose. The proximity of channels to the breccias is underlined by the dominance of aquatic and amphibious vertebrate remains in the lower Viala Formation. Their remains may have been transported by strong currents that resulted in their complete disarticulation and breakage. The Viala fauna, therefore, lived in a proximal floodplain environment, very close to stream channels. Although uncommon in Europe, the association of sphenacodontids with xenacanthids, branchiosaurids, and eryopoids (Heyler 1997; personal observations) in the Viala Formation also occurs in the Late Stephanian Kounov Member, Western Bohemia (Štamberg and Zajíc 2008) and in the Gzhelian-Asselian Remigiusberg Formation, Saar-Nahe Basin (Fröbisch et al. 2011). If the Viala Formation is Sakmarian, then this association persisted during the early Permian. Xenacanthids, eryopoids, and sphenacodontids are commonly associated in the early Permian of Texas and Oklahoma, where they played a major role in the local floodplain to lacustrine ecosystems (Olson 1958, 1961, 1977).

Table 2.

Distribution of Late Carboniferous-Early Permian sphenacodonts in Europe. Taxa for which column “S” is checked are sphenacodontids. Note that Datheosaurus might not be a sphenacodont at all (Frederik Spindler, personal communiation 2012).

The Bromacker vertebrate assemblage differs in the absence of an aquatic component (Eberth et al. 2000). This more terrestrial assemblage comprises dozens of partial to subcomplete articulated skeletons that indicates that these tetrapods lived instead in a distal floodplain, far from potential sources of transport. Although streams and standing bodies of water were present according to sedimentary and palaeontological data, the good drainage and the semi-arid climate of the region would have prevented the establishment of aquatic (or even amphibious) vertebrate populations (Eberth et al. 2000). During floods, individuals that were not able to escape would have been buried or trapped in mud before dying from exhaustion-similar but rarer examples are known from contemporaneous deposits from Texas (Sander 1989). In this case, there would have been little or no transport.

Despite the proximity of fluvial channels, the tetrapod footprint assemblages in the lower part of the Viala Formation suggest that more upland taxa were also present. These tracks have been attributed to branchiosaurids, eryopoids, eupelycosaurs, and “edaphosaurs” (Gand 1987, 1989). These putative “edaphosaurs” (a taxon formerly considered to include Caseidae and Edaphosauridae), although not confirmed by a body fossil record, are represented by a few tracks referred to the ichnospecies Ichniotherium cottae. Recently, however, Voigt et al. (2007) have been able to identify the diadectid Diadectes absitus as the trackmaker of Ichniotherium cottae through a detailed comparison of limb remains and tracks from Bromacker. Though diadectids are relatively abundant in upland areas (Eberth et al. 2000), they are much rarer in lowlands (Olson 1958, 1977; Sander 1987, 1989).

The Viala vertebrate assemblage is therefore definitely typical of lowlands, with xenacanthids, branchiosaurids, and eryopoids living in shallow lakes and ponds subjected to drought and sphenacodontids living in marginal areas, preying upon other vertebrates (Fig. 4). They probably fed also upon diadectids that would have ventured into this area. Sphenacodontids, eryopoids, and xenacanthids were at the apex of the food chain, feeding potentially upon all other vertebrates.

Conclusions

Although not common, sphenacodontids were represented only by Neosaurus cynodus from the La Serre Horst area, which was thought to represent a distinct species. Re-examination of its holotype shows that it cannot be diagnosed below the family level, as an indeterminate sphenacodontid. Three additional specimens from the Lodève Basin are also described as indeterminate members of this family. Their association with xenacanthids and eryopoids confirms the close biogeographic affinities of Europe and North America during the early Permian.

Fig. 4.

Hypothetical trophic web for the lower Viala Formation based on relative size and functional morphology. Primary producers are poorly known, but a callipterid has been recently described from the Viala Formation (Galtier and Broutin 2008).