New transitional fossil from late Jurassic of Chile sheds light on the origin of modern crocodiles

We describe the basal mesoeucrocodylian Burkesuchus mallingrandensis nov. gen. et sp., from the Upper Jurassic (Tithonian) Toqui Formation of southern Chile. The new taxon constitutes one of the few records of non-pelagic Jurassic crocodyliforms for the entire South American continent. Burkesuchus was found on the same levels that yielded titanosauriform and diplodocoid sauropods and the herbivore theropod Chilesaurus diegosuarezi, thus expanding the taxonomic composition of currently poorly known Jurassic reptilian faunas from Patagonia. Burkesuchus was a small-sized crocodyliform (estimated length 70 cm), with a cranium that is dorsoventrally depressed and transversely wide posteriorly and distinguished by a posteroventrally flexed wing-like squamosal. A well-defined longitudinal groove runs along the lateral edge of the postorbital and squamosal, indicative of a anteroposteriorly extensive upper earlid. Phylogenetic analysis supports Burkesuchus as a basal member of Mesoeucrocodylia. This new discovery expands the meagre record of non-pelagic representatives of this clade for the Jurassic Period, and together with Batrachomimus, from Upper Jurassic beds of Brazil, supports the idea that South America represented a cradle for the evolution of derived crocodyliforms during the Late Jurassic.


Scientific Reports
| (2021) 11:14960 | https://doi.org/10.1038/s41598-021-93994-z www.nature.com/scientificreports/ Locality and horizon. The holotype and referred specimens of Burkesuchus were collected from beds of the Toqui Formation, cropping out in the mountains flanked by the Maitenes and Horquetas rivers, south of General Carrera Lake (Fig. 1). The rock succession consists of a 300-320 m thick sequence of conglomerates with intercalated tuffs. Burkesuchus fossils occur in an approximately 100 m succession of alternating green volcaniclastic pebbly sandstones and sandy sedimentary breccias, with intercalations of lapilli tuffs and red ignimbrites with eroded tops. The U-Pb SHRIMP age of 147 ± 1.0 Ma was obtained from zircon samples from the ignimbrite that immediately underlies the fossil-bearing levels, indicating a Tithonian age (latest Jurassic) for Burkesuchus and its associated fauna 11,12 . Other fossil vertebrates currently documented from these beds include titanosauriform and diplodocoid sauropods, along with the herbivorous theropod Chilesaurus diegosuarezi 13-15 . Description. Available specimens of Burkesuchus indicate a relatively small animal roughly 70 cm long; this is based on comparisons with complete skeletons of Protosuchus richardosoni 16 (see Table 1).
Cranium. Burkesuchus exhibits a dorsoventrally compressed braincase and cranium that is transversely wide at the posterior margin. The posterior margin of the squamosal, quadrate and quadratojugal slope strongly posteroventrally, a condition different from the subvertical orientation present in "protosuchians" and notosuchians 17,18 (Fig. 2E,F). The cranial roof is strongly ornamented by pits and grooves ( Fig. 2A,B). The frontals are fused and show a midline longitudinal ridge, as in notosuchians and basal neosuchians 19 . In dorsal view the frontals are subtriangular in contour with strongly anteriorly convergent lateral margins. The contact with the nasals is interdigitated, forming a "W"-shaped suture. The frontals are notably short and delimit the anteromedial margin of the supratemporal fenestrae. The fenestrae are proportionally small and ovoid in contour, similar to Sichuanosuchus 20 . The supratemporal fossae of Burkesuchus exhibit a small supratemporal foramen at the anterolateral margin. The laterosphenoid is widely exposed in the supratemporal fossa. In dorsal view the postorbital is gently convex and is anteroposteriorly short, representing half the length of the squamosal. It shows a squared-off anterolateral margin with a short projection, and a concave anterior margin. In dorsal view, the cranial table is transversely wide.
In lateral view the postorbital shows a rod-like descending process, as typical in modern crocodilians 4,19,21 . The postorbital contact for the quadratojugal is narrow, constituting a derived mesoeucrocodylian condition 22,23 . The quadratojugal looks stout and anteroposteriorly expanded. The anterodorsal corner of the quadratojugal exhibits a well-defined excavation, which probably hosted the fleshy component of m. depressor auricular superior, m. levator auricular superior, and the lining muscle responsible for movements of the upper earlids 24,25 . The quadrate is notably elongate and posteroventrally extended, and shows a pair of deep excavations along its dorsal surface (albeit not fully laterally facing as in "protosuchians" 21 ). The subtympanic foramen is wide, well-defined and located anterodorsally with respect to the otic incisure. A narrow ridge along the dorsal margin of the quadrate is here considered as the possible ventral limit of the periotic fossa, and thus, as the anterior extension of the tympanic membrane.
A well-defined longitudinal groove runs along the lateral edge of postorbital and squamosal, indicative of an anteroposteriorly extensive upper earlid 21 . The squamosal is strongly flexed posteroventrally, forming an expanded wing that partially covers the meatal chamber. The squamosal wing delimits the posterior opening of the meatal chamber, which is reduced to a small duct. The external auditory meatus is deeply sunk into the squamosal, being mostly covered laterally by this bone. www.nature.com/scientificreports/ On the posteromedial corner of quadrate there exist a conspicuous foramen aereum. The squamosal and quadrate are in near contact with one another along their posterior surfaces, leaving a small canal that may represent a precursor of the eusuchian cranioquadrate foramen 26 .
The occipital surface faces posterodorsally. The supraoccipital is small, subtriangular in contour and with a prominent nuchal crest. The otoccipital is relatively small, and lacks the expanded ventrolateral surface present in "protosuchians" 22 . The paraoccipital processes are dorsoventrally narrow and bear a small lateroventral tubercle, as in some basal neosuchian crocodyliforms 3,27 . The squamosal is widely exposed on the occipital plane ( Fig. 2C,D), extending laterally and ventrally well beyond the level of paraoccipital processes. This peculiar condition of the squamosal appears unique in Burkesuchus among crocodyliforms. An expanded squamosal may be also observed in the "protosuchians" Orthosuchus and "Notochampsa", but it is not sigmoid in contour, and is not strongly deflected nor appressed to the quadrate 23 . The paraoccipital process delimits the vagi foramina (including the openings of the IX, X, XI nerves). Cranial nerve XII exhibits a double exit. The foramen magnum is transversely wide and is dorsally delimited by crests.
Vertebrae. The available cervical neural arch is dorsoventrally tall and with a high neural spine that is anteriorly inclined. The postspinal fossa is well-excavated and teardrop-shaped. In lateral view, a well-developed accessory centroprezygapophyseal lamina is present (Fig. 3A). Dorsal vertebrae are amphicoelous, with articular surfaces of centra sub-circular in outline, as occurs in neosuchians 4 . Neural arches are dorsoventrally tall, and have a long, sub-rectangular shaped neural spine, representing more than twice the dorsoventral height of respective centrum ( Fig. 3B-D). The neural canal is notably wide. There are no spinoprezygapophyseal or spinopostzygapophyseal laminae. The articular surfaces of the prezygapophyses are transversely wider than anteroposteriorly long and reniform in contour, with a notched anterior margin. A well-developed interpostzygapophyseal lamina is present.
Pectoral girdle. The scapula is transversely robust (Fig. 4A). As in basal crocodyliforms (e.g., Orthosuchus 23 ), the acromial process of Burkesuchus is prominent and associated with a well-developed acromial ridge that is distally extended through the centre of the scapular blade. The glenoid facet is ventrally facing and dorsally bound by a prominent lip, a condition reminiscent of certain mesoeucrocodylians (e.g., Notosuchus, Yacarerani, Caiman 28 ). In contrast, the coracoidal portion of the glenoid facet is posteriorly oriented and devoid of prominent edges. This later condition resembles that of basal crocodyliforms (e.g., Orthosuchus 23 ) and differs from the posterodorsally oriented coracoidal glenoid facet of mesoeucrocodylians (e.g., Notosuchus, Yacarerani, Caiman 28 ). The ventral process of coracoid is notably elongate and relatively narrow, with a strongly expanded distal end.
Forelimb. The length of humerus represents 68% of the maximum width of the cranium, compared with 75% in Protosuchus 16 . It is straight in cranial view, but gently sigmoid in side view ( Fig. 4B-E). The humerus of Burkesuchus shows a prominent proximolateral expansion, as occurs in mesoeucrocodylians 29 . However, its proximal end lacks features diagnostic of notosuchians (e.g., presence of a deep circular depression on the posterior surface of the proximal humerus, medially displaced proximal one-third of the deltopectoral crest, with www.nature.com/scientificreports/ a medially tilted distal end, and deltopectoral crest anterolaterally delimited by a well-defined concavity) 28 . The deltopectoral crest is prominent, subtriangular in lateral view and strongly anteromedially projected, as occurs in Orthosuchus 23 . The ulna is transversely compressed and shows a proximally rounded and well-defined olecranon ( Fig. 4F-I). The proximal end of ulna exhibits well-developed proximal cotyles and an intercotylar crest and process, suggesting the presence of complex elbow movements, as in extant crocodilians 30 . It lacks the processes to accommodate the radius, thus differing from ziphosuchians 28 .
Hind limb. The femur is known from a referred specimen (Fig. 5). Its shaft is relatively gracile and sigmoid in all views, with major axes of both proximal and distal ends meeting at an angle close to 50°. This condition is intermediate between that of non-eusuchian crocodyliforms (between 17° and 45°3 1 ) and living crocodiles (between 60° and 65°3 2 ). The 4th trochanter is prominent and the basitrochanteric fossa is deep and well-defined, indicating a deep anchoring for the Mm. caudofemoralis longus and brevis. The distal end of the bone exhibits  www.nature.com/scientificreports/ highly asymmetrical distal condyles that are posterolaterally oriented. The lateral condyle is about two times larger than the medial condyle and is more ventrally extended, resulting in an asymmetric distal femur.
Osteoderms. Cervical osteoderms are subquadrangular in contour, with the lateral third ventrally inclined ( Fig. 3E,F). Trunk osteoderms, instead, are subrectangular in contour, with the anteroposterior length being half the transverse width. They are devoid of a dorsal keel and anterolateral prongs. Cranially, they exhibit a well-defined articular facet for the preceding osteoderm, representing approximately 1/3 of its entire length. The dorsal surface is ornamented by small, randomly distributed pits. Notably, trunk osteoderms are considerably enlarged with respect to the remaining skeletal elements. For example, they are transversely as wide as the cranium, a condition different from basal crocodyliforms (e.g., Protosuchus 16 ) in which the osteoderms represent a quarter of the posterior transverse width of cranium. In this regard, Burkesuchus is closer to the proportions seen in basal mesoeucrocodylians (e.g., Sarcosuchus 33 ). In contrast to both "protosuchians" and notosuchians, Burkesuchus exhibits a postorbital with a rod-like descending process, dorsoventrally low meatal chamber and reduced quadrate pneumaticity, and dorsal end of quadrate strongly forwardly oriented 18,36 , constituting synapomorphies uniting the Chilean taxon with Eusuchia. However, Burkesuchus retains several plesiomorphic features reminiscent of "protosuchians", which support its position outside Eusuchia, including: relatively small and subtriangular-shaped frontals that contribute little to the margin of the supratemporal fenestra; reduced postorbital when compared with squamosal in dorsal view; and supratemporal foramen relatively small and located at the anterolateral corner of the supratemporal fenestra 36,37 .

Burkesuchus and its implications for the evolution of meatal chamber in mesoeucrocodylians. Skull anatomy of Burkesuchus looks intermediate between that of "protosuchians" and neosuchian
crocodyliforms with regard to the meatal chamber, earlid position, and general cranial shape.
Burkesuchus is similar to derived mesoeucrocodylians in exhibiting a meatal chamber that is anteriorly dorsoventrally low (due to the reduction of both the anterodorsal process of quadratojugal and descending process of postorbital), the posterior closure of the meatal chamber (due to of the posteroventral flexing of the squamosal and its close relation with the quadrate), and in having an extensive groove for the earlid on both the postorbital and squamosal. This morphology sharply contrasts with that of "protosuchians" (e.g., Protosuchus, Hemiprotosuchus, Orthosuchus) in which the meatal chamber is dorsoventrally deep, the external auditory meatus is completely opened posteriorly, and the sulcus for the upper earlid is not posteriorly extended on the lateral margin of squamosal 21,36,37 . Burkesuchus also differs from basal notosuchians (e.g., Araripesuchus), in which the In the latter taxon, the external auditory meatus is only partially exposed in side view, different from the well-exposed condition of "protosuchians", notosuchians and peirosaurids (e.g., Araripesuchus, Hamadasuchus 21 ). Burkesuchus also differs from early neosuchians such as Shamosuchus and Allodaposuchus 38 in that the latter exhibit a straight outer margin of squamosal. However, in these two neosuchians and Burkesuchus the squamosal bears a ventrally directed lamina that in crocodilians contacts the posterodorsal surface of the quadrate posteriorly, resulting in a bony enclosure of the meatal chamber 21 . In Burkesuchus as well as in some basal neosuchians (e.g., Allodaposuchus, Goniopholis, Hylaeochampsa, Goniopholis, Anteophthalmosuchus 3,39-41 ) there exists a small otic aperture on the posterior surface of the cranium. In the above mentioned taxa both the squamosal and quadrate are not in contact posterior to the otic opening, thereby resulting in the formation of a cranioquadrate passage between the squamosal, quadrate, and exoccipital bones 21 (Fig. 7). In extant crocodiles, the cranioquadrate passage is almost closed and represented by the cranioquadrate foramen that provides passage for one branch of cranial nerve VII, the orbitotemporal artery, and the lateral cephalic vein 42 . www.nature.com/scientificreports/ Authors regard the closing of the cranioquadrate canal as diagnostic of mesoeucrocodylians 4,19 . However, in almost all eusuchians the cranioquadrate canal is delimited dorsally by the squamosal lamina, ventrally by the quadrate, and posteromedially by the otoccipital, whereas in neosuchians this canal is enclosed by the quadrate and otoccipital 19,39 . In Burkesuchus a small fissure separates the squamosal from the quadrate, leaving a slight, laterally opened cranioquadrate canal. Further, it has relatively small otoccipital and paraoccipital processes that are narrow and poorly laterally projected. In this way, the otoccipital does not form part of the cranioquadrate closure (Fig. 7). A similar condition was previously reported for goniopholidid neosuchians 39,41 . It is possible that the condition in Burkesuchus and goniopholidids represents an intermediate stage between the entirely opened meatal chamber of basal crocodyliforms (e.g., "protosuchians" and notosuchians) and the enclosed cranioquadrate foramen of extant crocodiles.
Burkesuchus and its implications for the evolution of ear pneumaticity in crocodilians. The cranium of extant crocodiles is characterized by a pneumatic system that ontogenetically develops through the expansion of diverticula from the middle ear cavity. Diverticula penetrate most bones of the posterior part of the cranium and mandible, being linked with an elaborate system of cavities and tubes to the throat 42 . In "protosuchians" and notosuchians there are multiple subtympanic foramina that represent a plesiomorphic state for the clade 43 . It is known that in extant forms the single subtympanic foramen and its associated diverticulum have resonant functions 44 . Thus, the complex pneumatic morphology of basal crocodyliforms has been associated with an advanced auditory sensitivity and directionality 21,45 . In eusuchians the multiple foramina are reduced in the quadrate to just a single foramen 26 . This foramen represents the entrance of the siphonium, a hollow stem consisting of connective tissue and epithelium that contacts the articular bone of the mandible with the quadrate and continues through this bone until it exits through a foramen, the siphonial aperture, into the tympanic recess 46 . These extraordinary modifications are correlated with the acoustical coupling of both middle ears to aid in augmenting certain frequencies via a pressure difference, probably associated with the aquatic habits of living forms 45 . The presence of a single foramen on the quadrate for the entrance of the siphonium in Burkesuchus suggests that this complex siphonial system was already developed in this basal mesoeucrocodylian.
Burkesuchus paleoecology. The anatomy of the braincase helps to recognize some palaeoecological features in Burkesuchus that may be important for understanding the habits of the first mesoeucrocodylians.
Burkesuchus, as in some other basal neosuchians such as Allodaposuchus and Hylaeochampsa, exhibits an enlarged posterior exposure of the squamosal and the retention of a ventral tubercle on the paraoccipital processes of the otoccipital, features that are indicative of a thick and robust anchoring of the M. depressor mandibulae, the only jaw abductor, and consequently a strong jaw opener 47,48 . However, the small size of the supratemporal fenestra and supratemporal foramen in Burkesuchus may indicate a more restricted attachment area for the adductor muscles of the jaw 4,49 . This kind of reduced supratemporal fenestra and fossae suggests a weaker force of jaw adduction for catching, killing and tearing large prey 47,50 . In living crocodylians, the capability of catching, killing and tearing large prey is accompanied by the capacity for torsional feeding and a stronger bite for holding and crushing prey during rolling, which necessarily includes an increasing need for more powerful adductor musculature 4 . It is usually regarded that strong musculature associated with holding prey by rolling is correlated with a solid rostrum and extensive secondary palate in eusuchians 4,49 . Burkesuchus, in having relatively small supratemporal fossae and supratemporal fenestra, suggests that rostrum and palate adaptations typical of eusuchian crocodiles were probably absent in this basal mesoeucrocodylian.
The postcranial anatomy of Burkesuchus provides some inferences on its ecology. As noted in the description, the scapulocoracoid glenoid shows an intermediate condition between basal crocodyliforms and modern crocodilians. However, the presence of a prominent lip on the scapular facet and the posteriorly oriented coracoid facet suggest that the humerus was unable of important dorsal excursion and points to a plesiomorphically more upright posture of the forelimb when compared with extant crocodilians 6,51 .
In contrast with the forelimb, the femur of Burkesuchus closely resembles the condition of extant crocodiles. This element shows an accentuated sigmoid curvature (contrasting with the straighter condition of more basal crocodilians and notosuchians) and strongly asymmetrical distal end, features correlated with a sprawling posture 52,53 .
In this sense, the presence of a well-developed fourth trochanter, basitrochanteric fossa and muscle scars indicate well-developed Mm. caudofemoralis longus and brevis (see 52,54 ). This contrasts with the condition of basal crocodyliforms and notosuchians in which these scars are not prominent 31 . Its reduction is usually correlated with progressive reduction of the tail-based musculature and reflects a knee-based limb retraction of upright posture and parasagittal gait [56][57] . In modern crocodiles the caudofemoral musculature is a critical component of the locomotor apparatus, because it produces wide arcs of femoral retraction and is important on femoral rotation 55 .
The femur of Burkesuchus shows features indicative of a sprawling stance and gait used by modern crocodiles when swimming and upon entering the water, as well as tail-based locomotion of extant crocodilians in water 32 . These features and behaviors were probably already present in Burkesuchus. By contrast, the forelimb indicates a more upright posture than shown in extant crocodiles. It is possible that the acquisition of sprawling posture in crocodilians was not acquired simultaneously in both fore-and hind limbs, but was decoupled. Although speculative, it is possible that the hind limbs, which tend to be more important for locomotion in living crocodiles, changed their shape before the forelimbs. It is possible that Burkesuchus illustrates this intermediate condition with somewhat upright forelimbs and sprawling hind limbs.
Burkesuchus expands the taxonomic diversity of Jurassic crocodylomorphs. Nevertheless, its body size falls within the size range (i.e., less than 1 m in whole length) that was usual for most Triassic and Jurassic terrestrial crocodyliforms. The position of Burkesuchus among mesoeucrocodylians, in tandem with other basal members of this clade, such as the aquatic Atoposauridae, indicates that basal neosuchians also diversified in the context of small body size regime. This constraint on body size was released in marine forms of Jurassic age, as well as in different clades during the Cretaceous (the terrestrial baurusuchids, peirosaurids and sphagesaurids, and the fresh-water pholidosaurids 58 ). We are unable to explain the biological reasons for the retention of small sizes among basal terrestrial crocodyliforms, but competition with ecologically dominant theropod dinosaurs cannot be ruled out.
Burkesuchus constitutes one of the few records of non-aquatic, mesoeucrocodylians for the Jurassic Period, and alongside the advanced neosuchian Batrachomimus, from Pastos Bons Formation, NE Brazil 10 , supports the idea that South America is crucial for evaluating further the radiation and evolution of crocodyliforms during the Late Jurassic.