A New Sebecid from the Paleogene of Brazil and the Crocodyliform Radiation after the K–Pg Boundary

A new crocodyliform, Sahitisuchus fluminensis gen. et sp. nov., is described based on a complete skull, lower jaw and anterior cervical vertebrae collected in the São José de Itaboraí Basin of Rio de Janeiro, Brazil. The specimen is one of the best preserved crocodyliforms from Paleocene deposits recovered so far and represents a sebecosuchian, one of the few clades that survived the Cretaceous-Paleogene biotic crisis. The new taxon is found in the same deposit as an alligatoroid, a group that experienced large diversification in the Paleogene. The sebecosuchian record suggests that after the Cretaceous-Paleogene biotic crisis, the less specialized members of this clade characterized by a higher number of teeth compared to the baurusuchid sebecosuchians survived, some having terrestrial habits while others developed a semi-aquatic life style (e.g., Lorosuchus). Starting in the Eocene, sebecid sebecosuchians became specialized with a more accentuated oreinirostry as observed in Sebecus and in Langstonia, but not showing the typical reduced dentition developed by the Cretaceous baurusuchid sebecosuchians. The basal position of Barinasuchus arveloi, a high-snouted Miocene sebecid, indicates the occurrence of an independent lineage sometime after the K-Pg biotic crisis that developed accentuated oreinirostry, suggesting a more complex history of the post-K-Pg crocodyliform radiation.


Introduction
Currently crocodyliforms are worldwide distributed in tropical and subtropical regions in relative low numbers and diversity, consisting of 24 to 30 species (e.g. [1]). All are considered semiaquatic ambushers but their fossil record reveals a much richer evolutionary history in terms of anatomy and ecomorphospaces [2,3]. Particularly during the Cretaceous, the diversity of those reptiles was much higher and they occupied several distinct niches.
As a natural question, researchers tried to understand the crocodyliform decrease in diversity after the Cretaceous-Paleocene (K-Pg) extinction crisis but this discussion is hampered by the scarce nature of their remains in Paleocene deposits (e.g. [4]). Besides the marine dyrosaurids that have survived the K-Pg boundary and diversified during the Paleocene (e.g. [5,6]), there are only a limited number of Paleocene specimens described so far, most of which are fragmentary and poorly preserved (e.g. [4,[7][8][9]). This contrasts with the high abundance of Late Cretaceous crocodyliforms, particularly in Brazil, which is even higher than in other Gondwanan areas.
During the exploration of the São José de Itaboraí Basin (Rio de Janeiro State, Southeast Brazil) that lasted for about five decades and ended in 1984 [10], hundreds of fossil vertebrates were collected ( Figure 1). The vast majority is housed at the Earth Science Museum (now at the Companhia de Pesquisa de Recursos Minerais -CPRM), in Rio de Janeiro, and consists of fragmentary remains representing mainly mammals (e.g. [11,12]). However, some reptiles have also been collected, including the remains of crocodyliforms [13,14], with only one species formally proposed so far [15].
Among the few well preserved and more complete crocodyliform material is an almost complete skull and lower jaw (MCT 1730-R) that was briefly mentioned (but never figured) in the literature [8,13,16] and remained undescribed until now. This specimen represents a new taxon, Sahitisuchus fluminensis gen. et sp. nov., and shows that during the Paleocene the São José de Itaboraí crocodyliform fauna was composed by rather primitive (i.e., Sebecosuchia) and more derived (Alligatoridae) post-K-Pg taxa. Such a combination of sebecosuchians and eusuchians has not been previously reported in any deposit so far.

Nomenclatural Acts
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (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: 322EE489-D9D2-4CE6-9DAF-36E30C03881D. 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.
No permits were required for the described study, which complied with all relevant regulations. See appropriate section of Systematic Paleontology for locality, stratigraphic, repository and specimen number. Derivation of name. Generic name Sahiti comes from the Xavante culture (sahi ti), one of the indigenous Brazilian inhabitants, meaning ''to be angry'' or ''to be brave'', in allusion to warriors; and souchos, refers to the Egyptian crocodile god. Specific name fluminensis is a latinization of fluminense, designation of citizens born in the Rio de Janeiro State.

Systematic Paleontology
Type species. Almost complete skull and lower jaw, proatlas, intercentrum, the axis and the 3 rd cervical vertebra (MCT 1730-R), housed at the Museu de Ciências da Terra, Companhia de Pesquisas de Recursos Minerais (CPRM), Rio de Janeiro, Brazil (cast at the Museu Nacional/UFRJ -MN 4711-V).  Diagnosis. Sebecid crocodyliform with the following autapomorphies: mandible lacking external mandibular fenestra; and odontoid process fused to the axis with vertical anterior surface that lacks medial processes. The new species can be further distinguished from other sebecids by the following combination of characters: infraorbital jugal region with shallow ventrolateral depression (shared with Lorosuchus); shallow elliptical depression on the posterior surface of the quadrate close to the craniomandibular articulation (shared with Sebecus icaeorhinus); rough and rugose dorsal edge of supratemporal fossa (shared with Sebecus icaeorhinus); sharp, semilunate exoccipital posterior processes, directed medially (shared with Ayllusuchus); jugal posterior process higher than anterior process and lateral expanded (shared with Bretesuchus); rough longitudinal ridge on the lateroventral edge of angular and dentary, ending close to the mandibular symphysis level (shared with Bretesuchus, Sebecus).
The premaxillae and the region of the external nares were broken off and the skull was slightly compressed dorsoventrally during preservation. The lower jaw is occluded with the skull and some bones lack the external bone cortex. In dorsal view, the skull of Sahitisuchus fluminensis is elongated, showing two slight constrictions at about the level of the 5th and 11th maxillary alveoli (Figures 2A, B). It differs from Sebecus icaeorhinus and Stolokrosuchus by being comparatively shorter [23,24], but not as short as Lorosuchus [4]. Sahitisuchus does not show the same oreinirostral condition as Sebecus, Barinasuchus, Bretesuchus, Zulmasuchus and Langstonia [8,9,16,23,25].

Cranial bones
The skull-roof is flat and rectangular, being wider than long. The supratemporal fossa is much larger than the supratemporal fenestra (Figures 2A, B). This fossa is about three times smaller than the orbits. The distance between the supratemporal fossae is half that of the frontal inter-orbital width. The dorsal border of this fossa is surrounded by rugosities, forming an elevation that is more developed in the medial and lateral borders. This condition is similar to Sebecus and the peirosaurid Hamadasuchus, differing from any other mesoeucrocodyliforms (sensu Benton & Clark 1988 [20]) known to date. The palpebral bones, which are present as anterior and posterior elements in other sebecids (e.g. Sebecus, Lumbrera form [4,26]) and specially in ''peirosaurids'' (e.g. Lomasuchus, Uberabasuchus, Montealtosuchus) [27][28][29], are not preserved. Even so, the orbit is placed rather laterally, a typical terrestrial sebecid feature, and not laterodorsally as in semi-aquatic crocodyliform morphotypes (e.g., Stolokrosuchus, Lorosuchus [4,24], and extant species). The frontal is broad and triangular, with a low and smooth longitudinal crest running from the middle part to the posterior portion this bone. A longitudinal frontal crest is a common characteristic for many basal mesoeucrocodylian species, which includes some sebecosuchian taxa (e.g. Sebecus; Zulmasuchus; Iberosuchus macrodon; Pepesuchus, Lorosuchus [4,16,23,30]. The frontal ornamentation is similar to that on the maxilla, with the wrinkles starting at the frontal longitudinal crest directed to the lateral margins. The jugal is very large and ornamented like most other cranial bones. The posterior ramus is laterally expanded and higher than the anterior one, an unusual feature within sebecosuchians only previously observed in Bretesuchus [8]. The ventrolateral margin is concave, a unique feature among basal mesoeucrocodylians. The quadratojugal takes part in the cranio-mandibular articulation forming the ''double articulation'' (sensu Buffetaut 1975 [31]), a feature absent in extant eusuchians but observed in all sebecid species and some other not closely related taxa (e.g. Trematochampsa, Libysocushus, Dyrosauridae). The squamosal shows a developed sculptured dorsal posteriorly pointed lobe (the squamosal posterior process or the squamosal prong [32] that is directed posteriorly and does not  form a horn, similar to Hamadasuchus and Lomasuchus [27,32]. Sebecus also shows such a developed process, but differs from Sahitisuchus by a more squared-shape posterior end [23]. The quadrates are massive and mostly unsculptured. The portion of the tympanic cavity formed by the quadrate is not multifenestrated like the one found in protosuchians, notosuchians [33] and baurusuchids (e.g. [34]). It also lacks the oblong concavity, which is characteristic of the Baurusuchidae [34][35][36] but, like Sebecus, Hamadasuchus and recent species, shows only two openings: the small, anterior preotic siphonial foramen, followed by the larger, oval otic incisure. The ventral portion of the tympanic membrane was supported by a low and sharp semicircular crest. The quadrate distal body extends beyond the occipital limits and bears a well-developed sharp crest that runs from the lateral region of the cranioquadrate passage to the end of this bone. A semielliptical shallow concavity in the most distal portion of the quadrate body, just medial to the quadratojugal-quadrate suture and anterior to the cranial-mandibular articulation is very conspicuous in the new species (Figures 2, 5). In ventral view the quadrate exhibits pronounced crests A and A9 [37] for M. adductor mandibulae posterior [38].

Palatal region
The anterior process of the palatine projects over the maxillary palatal shelf with a ''U-shaped'' anterior margin [39], which extends well forward from the anterior margin of the suborbital fenestrae (Figure 3). The pterygoids are broad wingshaped elements, similar to those found in Sebecus (MMP 235), being distinct from the broad quadrangular pterygoid of Zulmasuchus, peirosaurids (e.g. Montealtosuchus, Hamadasuchus) and derived eusuchians. The lateral border of the pterygoid flanges are arched and curved inwards similar to Zulmasuchus [9,16]. In Bretesuchus this curvature is even more accentuated than in the latter species [8]. The pterygoid plate is slightly concave, very large and broad. The basicranium is not verticalized as found in Eusuchia but more verticalized than some basal crocodyliforms forms (e.g. baurusuchids and sphagesaurids) (Figures 3, 5). The choanae are positioned between the palatine and pterygoid, having a low and laminar choanal septum. The choanal groove (or fossa) is circular as the one of Sebecus and Barinasuchus but comparatively smaller than in these taxa.

Occipital region
The occiput is about four times wider than high, which is partially attributed to crushing of the specimen ( Figure 5). On the skull roof, the supraoccipital, this bone is as a relatively small forward pointed triangle which is inserted between the parietals. In  occipital view this bone is relatively large and exhibits a prominent nuchal crest. The latter comprises the insertion point for M. spinalis capitis [40]. The posttemporal fenestrae are not well preserved due to compression, but the preserved part is very reduced with no postoccipital process. The supraoccipital descending portion is acute and reaches the foramen magnum. However, this seems more the product of the compression than to an autapomorphic feature of the new species. The exoccipital has a very distinct mediodorsal process similar to Ayllusuchus. This process is sharp and has a semilunate shape, comprising the insertion point for the M. rectus capitis sublimus and M. spinalis capitis. The basioccipital is trapezoidal and positioned oblique (,45u) relative to the horizontal plane. This bone possesses a median elevated crest (insertion point for the M. rectus capitis anterior). The basisphenoid is short and completely verticalized, being little exposed both in occipital and palatal views. Similar inclination of basisphenoid and basioccipital is also found in some sebecids (e.g. Zulmasuchus and Bretesuchus) and peirosaurids.

Mandible
In ventral view the mandible shows an inverted ''Y-shape'' (Figures 3, 4). The robust mandibular symphysis is formed by the dentaries and splenials and reaches to opposite the fourth maxillary teeth while the dentary teeth are not visible, occupying about 21% of the mandibular length. In lateral view the anterior mandible portion is not as high as those of Bretesuchus and baurusuchids. The splenial forms about one-fourth of the mandibular symphysis and medially covers the Meckelian channel as a vertical and thick bone lamina. The mandibular lateral fenestrae is closed, an unusual feature in crocodyliforms and differing from all other sebecosuchian taxa. The angular exhibits a robust well-developed ventrolateral ridge that runs over almost the entire angular length, probably corresponding to the insertion area for the strongest component of the mandibular adductory musculature (M. adductor mandibulae internus pterygoideus ventralis [38]). The surangular takes part in the glenoid fossa, is stout and slightly ornamented. In lateral view, the suture with the dentary is gently convex. The dorsal margin of this bone is arched. A developed ridge with a smooth dorsal and rugose ventral surface is present below the glenoid fossa ( Figure 3A, B). Except for Bretesuchus, in all other sebecosuchids where this region is preserved this crest is only incipient or poorly developed. With the retroarticular process, this structure is regarded as the probable insertion point for the components of the M. depressor mandibulae component [38,41]. The articular forms about 60% of the glenoid fossa, like in other sebecids but unlike some other sebecosuchians, as in baurusuchids. The retroarticular process shows an elevated lateromedially crest just posterior to the glenoid fossa, a structure that does not allow palinal-propalinal jaw movements. The retroarticular process, formed by the articular and the surangular, is arched with a concave dorsal margin. The most medial posterior part, formed by the articular, is ''tongue shaped''. Seen from posterior view, the posterior margin is inclined ventromedially forming an angle of about 40u relative the horizontal plane. A blunt crest runs longitudinally in the articular portion of this process. The retroarticular foramen aëreum is small and opens close to the medial margin of the retroarticular process, right after the glenoid fossa.

Dentition
The premaxillary teeth are not preserved but at least twelve maxillary teeth must have been present (Figures 4, 6). Due to the fact that the upper and lower jaws are occluded, most of the mandibular teeth are not visible.
The new species has the crocodyliform plesiomorphic pattern of occlusion [3], with the hypertrophied dentary caniniform exposed laterally, occluding in the premaxillary-maxillary fossa, and the following maxillary teeth occluding buccally relative to the mandibular tooth row. The upper dentition is heterodont with three morphological arrangements, all showing serrated carinae formed by true denticles (sensu Langston 1975 [42]) ( Figure 6). The first three maxillary teeth are ziphodont, curved posteriorly with pointed and buccolingually compressed crowns. The second dental morphotype is formed by the following two (perhaps three) teeth that are lanceolate and bear straight (i.e., not posteriorly curved) crowns. They are followed by progressively shorter teeth with blunt apices and a marked constriction between root and crown. The large caniform tooth shows about 3-3,5 denticles per mm ( Figure 6).

Cervical elements
Several of the most anterior cervical elements such as the proatlas, intercentrum and odontoid process are described for first time in Sebecidae (Figures 3, 7). The pro-atlas was displaced over the left pterygoid flange. It is a small and laminar V-shaped bone with a low dorsal crest. Compared to modern crocodilians, this bone is rather conservative differing mainly by being narrower (Figure 3). The intercentrum, the only part identifiable of the atlas, was also displaced, being preserved over the left suborbital fenestra. This bone is robust, not laminar, with two blunt posteriorly directed processes for the first cervical ribs. The axis is preserved associated with a well-developed odontoid process that is similar to the one found in recent taxa by being massive and showing on each side blunt anterior tuberous processes (Figure 7). In the new species the anterior region is vertical and lacks the small medial processes found in at least some recent taxa. Furthermore, the odontoid process is fused with the axis with no visible suture indicating that this is most likely a very old individual [43]. The axis is well developed with a low, blade-like neural spine. The third cervical vertebra is amphicoelous, with a tall spike-like neural spine, inclined posteriorly, with a postspinal lamina that is bifurcated at the base ( Figure 7). As in Sebecus (the only other sebecid where this part of the skeleton was described [17]), the diapophysis is divided by the neurocentral suture and in lateral view, the centrum shows a medial constriction and a trapezoidal shape, with anterior and posterior articulations inclined anteriorly. Among the differences with Sebecus, Sahitisuchus has more robust and broader diapophyses, and the length of the third cervical centrum is subequal compared to the axis.

Discussion and Conclusions
In order to investigate the phylogenetic position of Sahitisuchus fluminensis, we used the data matrix published by Pol et al. 2012 [17], who have considered all well-known sebecid taxa (see Data S1). The analysis was run through TNT, with characters either unordered or ordered and both results show that Sahitisuchus is a member of the Sebecidae (Figure 8). Furthermore, the addition of the new Brazilian taxon collapses the monophyletic genus Sebecus recovered in previous studies [17] and suggests that Barinasuchus occupies a basal position within the Sebecidae relative to Lorosuchus.
The overall crocodyliform record in number of specimens and taxa from Paleocene deposits is rather slim. This low diversity contrasts with the expressive crocodyliform record of the Cretaceous, where a great number of species thrived in a variety of ecological niches, particularly in the Gondwana, such as notosuchians (e.g. Uruguaysuchidae, Sphagesauridae), baurusuchids (e.g. Baurusuchus, Stratiotosuchus, Pabweshi), peirosaurids (e.g. Uberabasuchus, Pepesuchus, Hamadasuchus), mahajangasuchids (e.g. Mahajangasuchus and Kaprosuchus), and other taxa whose phylogenetic position is more controversial [e.g. 44].
Only three crocodyliform lineages are represented either before and after the K-Pg boundary: the marine Dyrosauridae, 1std (d4 ?), first exposed dentary tooth of the right side; 1std (d4 ?) s, first exposed replacement dentary tooth of the left side; d, dentary tooth; fabl, fore-after basal length; lmt, last exposed maxillary tooth; m, maxillary tooth; tch-tooth crown height; -, lack information; ,, estimated measurement. doi:10.1371/journal.pone.0081386.t002 particularly abundant in coastal deposits of Africa [45,46], the semiaquatic Crocodylia, recovered specially by alligatoroids from North and South America [15,[47][48][49][50]; and the terrestrial sebecosuchians (e.g. [17]). Dyrosaurids are very specialized and became quite diversified after the K-Pg boundary, becoming along with sharks the main marine predators after the demise of mosasaurs [6]. Although the Alligatoroidea were already present in the Late Cretaceous this group only diversified after the K-Pg biotic crises (e.g. [39,49]), contrary to what happened with the sebecosuchians that became less diverse (with baurusuchids restricted to Upper Cretaceous [e.g. 34]). So far, the only Paleocene deposit where members of the Alligatoroidea (Eocaiman itaboraiensis [15]) and Sebecosuchia (represented by Sahitisuchus) were recovered is the São José de Itaboraí Basin. Having its origin related to the separation of South America and Africa, resulting in the opening of the South Atlantic Ocean [51], this tectonic feature consists of a small half-graben with a NE-SW major axis of 1.400 m and a sedimentary sequence that reaches a maximum thickness of 125 m [52]. The main fossils described so far are mammals that record one of the earliest phases of the mammalian radiation in South America after the K-Pg biotic crisis (e.g. [53]). The inferred age of the Itaboraí Basin based on the mammalian fauna has been the matter of a recent debate [21,[53][54][55]. Despite this uncertainty, the new crocodyliform is part of the so-called S2 paleofauna, whose age (Itaboraian SALMA [55]) is considered middle Upper Paleocene varying in absolute terms between 61.8 million to 58.5 million years [12] or 58.5 million to 56.5 million years [22].
The co-occurrence of a remnant of the pre-K-Pg sebecosuchian and a post-K-Pg alligatoroid crocodyliform taxon, here represented by Sahitisuchus and Eocaiman [15], respectively, in the Paleocene deposits of the Itaboraí Basin is quite unusual and somewhat surprising. The taphonomic history of those specimens, as of other fossils found in this basin, has been difficult to retrieve, particularly due to the fact that all material was recovered from fissures and not detailed information about their collecting has been recorded. This raises the valid question if all fossils were synchronous [e.g., [56][57]. In the lack of other information, some authors have used the color of the specimens to establish if they came from the same or distinct fissures that stands as a proxy for being regarded synchronous [56].
Regarding the crocodyliforms, it is clear that the sebecid and the alligatorid species came from distinct environments (terrestrial and semi-aquatic, respectively) and represent animals that lived around a freshwater lake before becoming preserved. Among the specimens attributed to Eocaiman, several show distinct colors suggesting that they come from distinct fissures [15]. The material of Sahitisuchus fluminensis is preserved in a greyish colored limestone, similar to some of the Eocaiman material. Furthermore, despite the questions about the correct absolute age, it has been proposed that the calcareous deposits of the São José de Itaboraí Basin were formed in a time span of 2 million years [57][58] or less. Therefore, we can conclude that Sahitisuchus and Eocaiman were either set apart for a comparatively short geological timespan or most likely cooccurred, the last hypothesis favored here.
One possible scenario that could explain the co-occurrence of Sahitisuchus and Eocaiman is that, right after the Cretaceous-Paleogene biotic crisis, only the less specialized crocodyliforms survived (e.g. [59]), except for the marine dyrosaurids that appear not to have been negatively affected by this event (e.g. [6]).
Regarding sebecosuchians, this appears to be correct since the Cretaceous forms show high skulls and a marked specialization in the dentition that is quite reduced. The Cretaceous taxa Baurusuchus and Stratiotosuchus, for example, show only five maxillary teeth opposed to the 10 in the Paleogene Lorosuchus, Bretesuchus and Zulmasuchus, and 12 in Sahitisuchus. Furthermore, Paleocene sebecosuchians represented only by the Sebecidae show the posterior teeth blunt and not specialized as in the Cretaceous sebecosuchians. It is conceivable that the Paleocene sebecosuchians adopted a mixture of semi-aquatic and terrestrial lifestyles and therefore might have at least partially shared the same environments as Paleocene alligatoroids. After the Eocene, sebecosuchians became again more specialized, developing a higher and laterally compressed rostrum as observed in the Eocene Sebecus and the Upper Miocene Langstonia. They further show a trend to reduce dentition (e.g. Sebecus exhibiting nine maxillary teeth), although not approaching the reduction observed in the Cretaceous baurusuchid sebecosuchians.
The unexpected result in the phylogenetic study presented here with the addition of Sahitisuchus to the data matrix published by Pol et al. [17], is the basal position of the high-snouted Barinasuchus. Recovered from Miocene deposits, this very large sebecid is known from the anterior portion of the rostrum only [9]. If its phylogenetic position is correct, this species indicates the presence of a yet another independent sebecid lineage that sometime after the K-Pg biotic crisis developed accentuated oreinirostry (sensu [60]) independently from other sebecids, suggesting a more complex history of the post-K-Pg crocodyliform radiation. Data S1 Phylogenetic Analyses. (DOC) Figure 8. Biochronology of the Crocodylomorpha based on the strict consensus tree obtained by the phylogenetic analysis (see text for details) and recorded temporal range. doi:10.1371/journal.pone.0081386.g008