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. 2020 Nov 2;238(4):809–827. doi: 10.1111/joa.13350

The endocranial anatomy of Buriolestes schultzi (Dinosauria: Saurischia) and the early evolution of brain tissues in sauropodomorph dinosaurs

Rodrigo T Müller 1,✉, José D Ferreira 2, Flávio A Pretto 1,2, Mario Bronzati 3, Leonardo Kerber 1,2,4
PMCID: PMC7930773  PMID: 33137855

Abstract

Our knowledge on the anatomy of the first dinosaurs (Late Triassic, 235–205 Ma) has drastically increased in the last years, mainly due to several new findings of exceptionally well‐preserved specimens. Nevertheless, some structures such as the neurocranium and its associated structures (brain, labyrinth, cranial nerves, and vasculature) remain poorly known, especially due to the lack of specimens preserving a complete and articulated neurocranium. This study helps to fill this gap by investigating the endocranial cavity of one of the earliest sauropodomorphs, Buriolestes schultzi, from the Upper Triassic (Carnian—c. 233 Ma) of Brazil. The endocranial anatomy of this animal sheds light on the ancestral condition of the brain of sauropodomorphs, revealing an elongated olfactory tract combined to a relatively small pituitary gland and well‐developed flocculus of the cerebellum. These traits change drastically across the evolutionary history of sauropodomorphs, reaching the opposite morphology in Jurassic times. Furthermore, we present here the first calculations of the Reptile Encephalization Quotient (REQ) for a Triassic dinosaur. The REQ of B. schultzi is lower than that of Jurassic theropods, but higher than that of later sauropodomorphs. The combination of cerebral, dental, and postcranial data suggest that B. schultzi was an active small predator, able to track moving prey.

Keywords: brain, computed tomography, endocast, evolution, Sauropodomorpha, Triassic

The first complete endocast of an early dinosaur is presented. The endocranium of Buriolestes schultzi reveals relatively small olfactory bulbs, an elongated olfactory tract, a small pituitary fossa, and well‐developed flocculus of the cerebellum. The data support B. schultzi as an active small predator, which was able to track moving prey. These endocranial traits change drastically across the evolutionary history of sauropodomorphs, reaching the opposite morphology in Jurassic times.

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1. INTRODUCTION

The origin of dinosaurs has been the subject of intensive investigations in the last years. New findings are uncovering the whole skeletal anatomy of the earliest dinosaurs and their closest relatives (Cabreira et al., 2016; Ezcurra et al., 2019; Müller et al., 2018a; Pretto et al., 2018). Details of the endocranial anatomy (and its associated structures) of some early dinosaurs have been accessed with the aid of computed tomography (Bronzati et al., 2017, 2018a; Ezcurra et al., 2019; Pacheco et al., 2019). However, specimens that preserve the whole neurocranium are still rare (Bronzati et al., 2018a), and the complete brain morphology of the earliest dinosaurs has remained unknown.

Here, we studied the morphology of the endocranial cavity and associated soft tissues of the specimen CAPPA/UFSM 0035 of Buriolestes schultzi (Müller et al., 2018a), a sauropodomorph from the dawn of the dinosaur era (c. 233 Ma, Carnian, Late Triassic of Brazil; Langer et al., 2018). The phylogenetic position of B.schultzi (Cabreira et al., 2016; Müller et al., 2018a) makes this dinosaur a key taxon in order to understand the evolution of the endocranial anatomy in dinosaurs. We also complement the original description (Müller et al., 2018a), providing novel details on its endocranial morphology, including a complete cranial endocast and details of its inner ear anatomy. The completeness of CAPPA/UFSM 0035 provides crucial information on the early evolution of the endocranial soft tissues of dinosaurs, including insights on the evolution of the encephalization quotient among early dinosaurs/sauropodomorphs.

1.1. Institutional abbreviations

AMNH, American Museum of Natural History, New York, USA; BP, Evolutionary Studies Institute, Johannesburg, South Africa (previously known as the Bernard Price Institute); CAPPA/UFSM, Centro de Apoio à Pesquisa Paleontológica da Quarta Colônia/Universidade Federal de Santa Maria, São João do Polêsine, Rio Grande do Sul, Brazil; CM, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA; CRILAR, Centro Regional de Investigaciones y Transferencia Tecnológica de La Rioja, Paleontología de Vertebrados, Anillaco, La Rioja, Argentina; GCP, Grupo Cultural Paleontológico de Elche, Museo Paleontológico de Elche, Elche, Spain; IGM, Institute of Geology in Ulaan Baatar, Mongolia; MB.R, Museum für Naturkunde, Berlin, Germany; MCCM, Museo de las Ciencias de Castilla‐La Mancha, Cuenca, Spain; MCNA, Museo de Ciencias naturals de Alava, Alava, Vitoria‐Gasteiz, Spain; MCP, Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil; MCZ, Museum of Comparative Zoology, Harvard, Cambridge, USA; MDT‐PV, Museo Desiderio Torres‐Paleovertebrados, Sarmiento, Chubut, Argentina; MUCPV, Museo de la Universidad Nacional del Comahue, Neuquén, Argentina; NHMUK, Natural History Museum, London, UK; OUMNH, Oxford University Museum of Natural History, Oxford, UK; PULR, Paleontología, Universidad Nacional de La Rioja, La Rioja, Argentina; PVL, Paleontología de Vertebrados, Instituto Miguel Lillo, Tucumán, Argentina; PVSJ, División de Paleontología de Vertebrados del Museo de Ciencias Naturales y Universidad Nacional de San Juan, San Juan, Argentina; SMNS, Staatliches Museum für Naturkunde, Stuttgart, Germany; ULBRA, Universidade Luterana do Brasil, Coleção de Paleovertebrados, Canoas, Brazil; ZPAL, Institute of Paleobiology of the Polish Academy of Sciences in Warsaw, Poland.

2. MATERIAL AND METHODS

2.1. Material

The specimen here described is housed at the Centro de Apoio à Pesquisa Paleontológica da Quarta Colônia, Universidade Federal de Santa Maria (CAPPA/UFSM 0035; Figure 1). It was excavated from the Buriol site (29°39′34.2″S; 53°25′47.4″W), at the municipality of São João do Polêsine, Rio Grande do Sul, Brazil (Müller et al., 2018a). This fossiliferous site belongs to the Santa Maria Formation (upper portion of the Candelária Sequence) of the Paraná Basin (Cabreira et al., 2016). Radioisotopic data from a nearby locality with similar fossiliferous content indicate a Carnian age to the site (c. 233 Ma, Late Triassic; Langer et al., 2018).

FIGURE 1.

FIGURE 1

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Study area and CAPPA/UFSM 0035. (a) Location map of the Buriol site and the surface distribution of the geologic units in the area (Modified from Müller et al., 2018a). (b) Reconstruction of the preserved elements of the skeleton of CAPPA/UFSM 0035 (modified from Müller et al., 2018a). (c) Skull in right lateral view. (d) Three‐dimensional rendering of the skull in right lateral view. (e) Skull in dorsal view. (f) Three‐dimensional rendering of the skull in dorsal view

Although histological analyses were not performed to determine the ontogenetic stage of CAPPA/UFSM 0035, the presence of certain structures related to muscle attachment indicates that it belongs to a non‐juvenile individual—following the histologically investigated ontogenetic series of Asilisaurus kongwe (Griffin & Nesbitt, 2016). These structures are: (i) the anterolateral scar on the femoral head; (ii) the trochanteric shelf on the proximal portion of the femur; (iii) and the scar on the lateral surface of the postacebatular ala of the ilium (see Garcia et al., 2019). Furthermore, CAPPA/UFSM 0035 lacks the patches of longitudinal parallel striations on the external surface of limb bones, which occur in some skeletally immature dinosaurs (see Müller et al., 2019). Fusion between the elements of the braincase has also been used to estimate the ontogenetic age of non‐avian dinosaurs. The firm articulation between elements of the braincase and the articulation of this part of the skull with the skull roof (i.e., frontals, parietals) could thus be an indication that the specimen is not an individual in early ontogenetic stages (e.g., Bronzati & Rauhut, 2018; Galton & Kermack, 2010; Gow, 1990; Nesbitt et al., 2009).

In addition to CAPPA/UFSM 0035, this study also employed CT scan data of Macrocollum itaquii (CAPPA/UFSM 0001b—Müller, 2019) and Gnathovorax cabreirai (CAPPA/UFSM 0009—Pacheco et al., 2019). The specimen of Macrocollum itaquii was unearthed from the Wachholz site (29°36′46.42″S; 53°15′54.06″W), at the municipality of Agudo, Rio Grande do Sul, Brazil (Müller et al., 2015). This fossiliferous site belongs to the Caturrita Formation (upper portion of the Candelária Sequence) of the Paraná Basin and is considered early Norian in age (c. 225 Ma, Late Triassic; Langer et al., 2018). Macrocollum itaquii, a sauropodomorph dinosaur, belongs to the clade Unaysauridae, which is composed exclusively of Norian forms (Müller et al., 2018b). The specimen of Gnathovorax cabreirai was excavated from the Marchezan site (29°37′52′′S; 53°27′02′′W), at the municipality of São João do Polêsine, Rio Grande do Sul, Brazil (Pacheco et al., 2019). Such as the Buriol site, the Marchezan site exposes sedimentary strata of the Santa Maria Formation (upper portion of the Candelária Sequence) of the Paraná Basin and, therefore, it is Carnian in age (c. 233 Ma, Late Triassic; Langer et al., 2018). Gnathovorax cabreirai is a herrerasaurid dinosaur (Pacheco et al., 2019).

2.2. X‐ray computed tomography and three‐dimensional rendering

he specimen CAPPA/UFSM 0035 was scanned using a μCT scan Skyscan™ 1173 at the Laboratório de Sedimentologia e Petrologia of the Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil, using 110 kV and 72 μA. We followed the protocols by Balanoff et al. (2016) to digitally construct the cranial endocast of CAPPA/UFSM 00035. The scan resulted in 3498 tomographic slices, with a voxel size of 34.91 μm. The slices were imported to Avizo 8, and the regions of interest were manually segmented using a WACOM Cintiq 21UX tablet to generate the 3D models.

2.3. Phylogenetic analysis

A phylogenetic analysis was performed in order to verify the influence of the new braincase data (Table 1) of Buriolestes schultzi on the phylogenetic study presented by Müller (2019). The analysis was conducted in the software TNT v.1.1 (Goloboff et al., 2008), and the parameters employed followed that of the original study. The operational taxonomic unit Euparkeria capensis was used as the outgroup, and a heuristic search was conducted using random addition sequence for 1000 replicates of Wagner trees followed by tree bi‐section and reconnection. All characters were treated as having equal weight, and the following characters were treated as ordered: 8, 14, 22, 26, 43, 63, 75, 108, 118, 135, 141, 151, 154, 167, 170, 172, 173, 180, 185, 190, 193, 200, 207, 231, 234, 241, 251, 256, 264, 273, 282, 285, 299, 312, 334, 340, 348, 372, 385, 388, 391, 396, and 404. Following McPhee et al. (2018), characters 199 and 278 were set as inactive.

TABLE 1.

Changes to character scores of Buriolestes schultzi performed here

Character number State in Müller (2019) State here
87 ? 1
88 ? 0
89 ? 0
91 ? 0
95 ? 0
97 ? 1
98 ? 0
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2.4. Reptile Encephalization Quotient

The Reptile Encephalization Quotient (REQ) of Buriolestes schultzi was calculated using Hurlburt’s (1996) modification of the equations Jerison (1973) for reptiles. Because the ratio of the brain‐to‐dural envelope/braincase is unknown for extinct dinosaurs, it is not known what precise fraction of the endocranial cavity was actually occupied by the brain (Hurlburt, 1996). Therefore, following Hurlburt et al. (2013), brain/endocranial volume ratios of 37% and 50% were used. These values are assumed as brain mass. The REQ was calculated following Hurlburt (1996) [REQ = Mbr/(0.00155 × Mbd0.553)], where Mbr and Mbd correspond to brain and body mass, respectively. The REQs were calculated through the mass estimated from the convex hull generated over a 3D model of an assembled skeleton and linear regression of the femoral circumference.

2.5. Body mass estimations

Body mass of Buriolestes schultzi was estimated using three independent methods routinely employed in studies of this nature. The first method was an estimate based on the relation between body mass and femoral circumference (Campione & Evans, 2012; Campione et al., 2014; Christiansen & Fariña, 2004). In this work, we adopted the same equation of Campione et al. (2014): log10BM =2.754 × log10(Cfem) − 0.683, on which BM accounts for body mass and Cfem for femoral circumference.

The second method employed to calculate the body mass of Buriolestes schultzi was a volumetric approach based on convex hulls generated over the 3D model of an assembled skeleton (Brassey et al., 2015; Otero et al., 2019; Sellers et al., 2012). Buriolestes schultzi is known from at least seven specimens (Cabreira et al., 2016; Müller et al., 2018a; personal observation), which together comprise most of the skeleton. For the creation of the model over which volumetric estimates were conducted, the postcranial bones of CAPPA/UFSM 0035 were digitalized using a ZScanner 700 laser scan, with a 0.2‐mm resolution. Elements not preserved in CAPPA/UFSM 0035 were digitally sculpted based on the holotype (ULBRA‐PVT280) or rescaled based on digital scans of other specimens (Table 2). A digital model of the skull was created based on data from the micro‐computed tomography. The most complete of each paired element was mirrored to represent both sides of the skeleton. All bone elements were put in natural position (Figure 2a) using the software Autodesk Meshmixer 3.5 (http://www.meshmixer.com/). After that, the elements were grouped in different units representing body portions to be employed in the creation of the convex hulls (Table 3; Figure 2b). To obtain a tight fit in the convex hull, the cervical series was separated in two portions (separated at the midpoint), an approach similar to that adopted by Brassey et al. (2015). The volume of each independent body segment was calculated using the “convex hull” filter in Meshlab v2016.12 software (Cignoni et al., 2008). Volumes were then converted to mass by applying an overall weighted‐mean body density of 893.36 kg/m3 (Buchner et al., 1997). This particular value of body density was adopted following previous works (Brassey et al., 2015; Sellers et al., 2012), and it is similar to density values estimated for non‐flying Aves (Brassey & Sellers, 2014). The value of body density provided by Buchner et al. (1997) also has the advantage of taking into account the entire body when calculated.

TABLE 2.

Specimens employed to create the model of the skeleton

Element Source specimen Digitalization method
Skull CAPPA/UFSM 0035 µCT
Cervical series CAPPA/UFSM 0035 Laser scanning
Dorsal series CAPPA/UFSM 0035; CAPPA/UFSM 0002 Laser scanning
Sacral series CAPPA/UFSM 0028 Laser scanning
Caudal series CAPPA/UFSM 0268 Laser scanning
Pectoral girdle CAPPA/UFSM 0035 Laser scanning
Humerus CAPPA/UFSM 0268 Laser scanning
Radius/ulna + manus Sculpted Laser scanning
Ilium CAPPA/UFSM 0200 Laser scanning
Pubis + ischium Sculpted Laser scanning
Femur CAPPA/UFSM 0035 Laser scanning
Tibia/fibula CAPPA/UFSM 0035; distal portion sculpted Laser scanning
Pes Sculpted Laser scanning
Ribs CAPPA/UFSM 0035; sculpted Laser scanning
Hemapophyses CAPPA/UFSM 0268 Laser scanning
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FIGURE 2.

FIGURE 2

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Volumetric reconstructions of Buriolestes schultzi. (a) Articulated digitalized skeleton. (b) Minimum convex hulls of pre‐defined body segments. (c) Digital sculpture based on the referred specimens, by Douglas M. Heman

TABLE 3.

Volumes and estimated mass per body segment

Element Volume convex hull (mm3) Estimated body mass (g)
Skull 120,017.0469 107.2184
Cervical 1 20,229.13672 18.0719
Cervical 2 25,400.75 22.69201
Trunk 3,277,680.75 2928.149
Arm (left) 64,599.08203 57.71024
Hand (left) 3408.670654 3.04517
Manual digit 1 (left) 983.973389 0.879042
Manual digit 2 (left) 2544.749512 2.273377
Manual digit 3 (left) 3075.267334 2.747321
Thigh (left) 59,101.36328 52.79879
Shank + metatarsus (left) 154,905.2656 138.3862
Pedal finger 1 (left) 1980.538574 1.769334
Pedal finger 2 (left) 4554.818848 4.069093
Pedal finger 3 (left) 7331.868164 6.549998
Pedal finger 4 (left) 5349.132813 4.778701
Arm (right) 50,725.05469 45.31573
Hand (right) 3410.249512 3.046581
Manual digit 1 (right) 984.731934 0.87972
Manual digit 2 (right) 2545.35498 2.273918
Manual digit 3 (right) 3076.978027 2.748849
Thigh (right) 59,110.08984 52.80659
Shank + metatarsus (right) 130,490.2266 116.5747
Pedal finger 1 (right) 1979.59314 1.768489
Pedal finger 2 (right) 4555.927734 4.070084
Pedal finger 3 (right) 7339.055664 6.556419
Pedal finger 4 (right) 5349.796875 4.779295
Tail 849,272.0625 758.7057
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Finally, a volumetric approach was conducted on a digital 3D sculpture of Buriolestes schultzi made by Brazilian paleoartist Douglas M. Heman (Figure 2c), based on measurements of CAPPA/UFSM 0035 and the holotype (ULBRAPVT280). The watertight model was scaled based on the referred specimens, and the volume was obtained in Meshlab v2016.12. Volume was converted to body mass using the same density adopted for the minimum convex hulls model (see above).

3. RESULTS

3.1. Description and comparison

Details on the peripheral braincase morphology of CAPPA/UFSM 0035 have been previously presented (Müller et al., 2018a; Figure 3). Therefore, we describe the internal morphology and anatomy of the braincase to complement the original description of CAPPA/UFSM 0035 based on computed tomography. The anatomical description of the endocranial casts follows the approach adopted by previous authors (e.g., Paulina‐Carabajal et al., 2019), in which the casts of the endocranial structures will be referred to as if they were the structures themselves. The measurements of the braincase of CAPPPA/UFSM 0035 are presented in the Table 4.

FIGURE 3.

FIGURE 3

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Braincase of CAPPA/UFSM 0035 in dorsal (a), ventral (b), left lateral (c), anterior (d), and posterior (e) views. bp, basipterygoid process; bt, basal tubera; cmcv, groove for the caudal middle cerebral vein; cp, cultriform process; dtr, dorsal tympanic recess; f, frontal; fm, foramen magnum; fo, fenestra ovalis; fob, fossa for the olfactory bulb; fr, floccular recess; ls, laterosphenoid; mf, metotic foramen; oc, occipital condyle; ot, otoccipital; p, parietal; pb, parabasisphenoid; pf, pituitary fossa; pp, paraoccipital process; ppf, postparietal fenestra; pr, prootic; sd, semilunar depression; so, supraoccipital; stf, supratemporal fossa; V, path of the trigeminal nerve

TABLE 4.

Measurements (in mm) of the braincase of CAPPA/UFSM 0035

Dimension Measurement
Frontal maximum anteroposterior length 38
Frontal maximum mediolateral width 17
Frontal minimum mediolateral width 8
Parietal maximum anteroposterior length 20
Parietal maximum mediolateral width 14
Parietal minimum mediolateral width 8
Laterosphenoid maximum anteroposterior length 13
Laterosphenoid maximum dorsoventral height 7.5
Prootic maximum anteroposterior length 11.5
Prootic maximum dorsoventral height 9.5
Supraoccipitals maximum anteroposterior length 12
Supraoccipitals maximum transverse width 16
Otoccipital maximum mediolateral width 16.5
Otoccipital maximum dorsoventral height 13
Parabasisphenoid maximum anteroposterior length 45.5
Parabasisphenoid maximum transverse width 16.5
Pituitary fossa maximum dorsoventral height 3.5
Pituitary fossa maximum transverse width 2.5
Basioccipital maximum anteroposterior length 9
Basioccipital maximum transverse width 13
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3.1.1. Frontal

Both frontals are preserved (Figure 4a,b). They are longer than wide, as in other early dinosaurs (Bronzati et al., 2019). An anteroposteriorly oriented ridge extends along the ventral surface of each frontal. This ridge is arched, with its concave side laterally directed, following the shape of the lateral surface of the bone corresponding to the margin of the orbit (Figure 4b). The ridge bounds the fossae for the olfactory bulb, the elongated and undivided fossa for the olfactory tract, and the anterior half of the fossa for the cerebral hemisphere. The fossae for the olfactory bulb are separated from each other by a shallow crest (Figure 4b), differing from the condition in Macrocollum itaquii (CAPPA/UFSM 0001b) and Panphagia protos (PVSJ 874), on which the crest separating the fossae is more well‐developed dorsoventrally. The length of the elongated fossa for the olfactory tract is about 35% of the total length of the frontal, which resembles the morphology of some early sauropodomorphs (e.g., approximately 30% in Panphagia protos—PVSJ 874 and Saturnalia tupiniquim—MCP 3845 PV, the fossa was possibly longer in the latter but the anterior portion of the frontals are missing). On the other hand, in some later sauropodomorphs (e.g., 10% in Macrocollum itaquii—CAPPA/UFSM 0001b; 11.5% in Unaysaurus tolentinoi—UFSM11069; 20% in Plateosaurus—AMNH FARB 6810), including sauropods (Sereno et al., 2007), this fossa is anteroposteriorly short, reflecting a reduced olfactory tract. The ventral surface of the frontal lacks any indication of blood vessel impressions. In fact, no impressions of the blood vessel are preserved in the endocranial cavity of B.schultzi, which is the typical condition observed in sauropods (Paulina‐Carabajal, 2015). The contact of the frontal with the parietal occurs through a transversely oriented suture (Figure 4a), indicating that these bones are not fused.

FIGURE 4.

FIGURE 4

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Bones of the skull roof of CAPPA/UFSM 0035. Frontals in (a) dorsal and (b) ventral views. Parietals in (c) dorsal and (d) ventral views. dp, depression; fch, fossa for the cerebral hemisphere; fob, fossa for the olfactory bulb; fot, fossa for the olfactory tract; lpp, lateral process of the parietal; orm, orbital margin; orr, orbital roof; ppf, postparietal fenestra; pw, parietal wing; rdg, ridge; rs, raised surface; stf, supratemporal fossa

3.1.2. Parietal

The parietal (Figure 4c,d) roof the posterior portion of the cerebral hemisphere. The ventral surface of each parietal is wider anteriorly, at the contact with the frontals, and it gets progressively narrower posteriorly till the proximal limit of the parietal wings. Indeed, the cerebral hemisphere reaches its maximum lateral expansion at the contact between the frontal and parietal. Medially, the ventral surface of each parietal bears a slightly raised surface that is longitudinally oriented (Figure 4d). A large postparietal fenestra is anteriorly bordered by the posterior margin of the parietal wings, whereas it is posteriorly bounded by the anterior margin of the supraoccipital. The parietals are not fused, as a longitudinal suture is visible between both parietal bones.

3.1.3. Laterosphenoid

The specimen preserves both laterosphenoids. The left one is better preserved (Figure 5a–f). The medial surface of the bone is concave and envelops the lateral surface of the cerebral hemisphere, resembling the general morphology of the laterosphenoid in other sauropodomorphs, such as Saturnalia tupiniquim (MCP 3845‐PV) and Macrocollum itaquii (CAPPA/UFSM 0001a). The anteroventral margin of the bone bears two medially oriented foramina (Figure 5d). The dorsal one corresponds to the posterior margin of the foramen for the cranial nerve IV (trochlear), while the ventral one corresponds to the posterior margin of the foramen for the cranial nerve III (oculomotor). Differently, in the theropod Zupaysaurus rougieri (PULR 076), there is a single slit interpreted as the exit of both nerves (Paulina‐Carabajal et al., 2019). An elongated notch at the posteroventral margin of the ventral process of the laterosphenoid (Figure 5) corresponds to the anterior margin of the foramen for the cranial nerve V (trigeminal).

FIGURE 5.

FIGURE 5

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Bones of the lateral portion of the braincase of CAPPA/UFSM 0035. Laterosphenoid and prootic in lateroventral view (a). Laterosphenoid in lateral (b), medial (c), dorsal (d), ventral (e), and anterior (f) views. Prootic in lateral view (g). alp, anterolateral process; dtr, dorsal tympanic recess; fch, fossa for the cerebral hemisphere; III, path of the oculomotor nerve; IV, path of the trochlear nerve; ls, laterosphenoid; pr, prootic; V, path of the trigeminal nerve; VII, foramen for the facial nerve

3.1.4. Prootic

The right prootic is heavily damaged, whereas the left one is better preserved (Figure 5a,g). The medial surface of the bone forms part of the lateral and the ventral surfaces of the endocranial cavity, encapsulating part of the lateral surface of the hindbrain. Moreover, the prootic delimits the ventral portion of the floccular recess. The anterior margin of the bone is excavated by an elongated notch that corresponds to the posteroventral border of the foramen for the trigeminal nerve (Figure 5a). The notch is followed by a shallow groove that extends posteriorly. Posteriorly, there are two small apertures (Figure 5g) that correspond to passages for the facial nerve (VII). The anterior one is for the palatine branch and the posterior one is for the hyomandibular branch of the facial nerve (Sampson & Witmer, 2007). As in Gnathovorax cabreirai (CAPPA/UFSM 0009), these apertures are slightly ventrally located in relation to the ventral margin of the foramen for the trigeminal nerve. Moreover, in both B.schultzi and G.cabreirai, the anterior foramen is located dorsally and slightly anteriorly relative to the posterior one. In Panphagia protos (PVSJ 874), there is a single foramen for the facial nerve. The posterior surface of the prootic bounds the anterior margin of the fenestra ovalis.

3.1.5. Supraoccipital

Both supraoccipitals are complete and well‐preserved (Figure 6a–c). The bones are fused forming the roof and part of the lateral surface of the braincase surrounding the cerebellum. The supraoccipitals also form the dorsal margin of the foramen magnum. The nuchal crest is transversely expanded along its longitudinal axis (Figure 6a), such as in Panphagia protos (PVSJ 874; Martínez et al., 2013) and Massospondylus carinatus (BP/1/5241; Chapelle & Choiniere, 2018). On the other hand, in Saturnalia tupiniquim (MCP 3845‐PV), Herrerasaurus ischigualastensis (PVSJ 407), and Gnathovorax cabreirai (CAPPA/UFSM 0009), the crest narrows posteriorly. As in Ixalerpeton polesinensis (ULBRA‐PVT059), Silesaurus opolensis (ZPAL Ab III/362/1), and Panphagia protos (PVSJ 874), a deep groove for the caudal middle cerebral vein (=vena occipitalis externa; dorsal head vein; vena capitis dorsalis) occurs on each side of the nuchal crest (Figure 6a). This groove extends from the dorsal surface to the anterolateral surface of the supraoccipital, being anteriorly enclosed by the posterior surface of the parietal wing. A dorsal and marked excavation for the vena occipitalis externa is absent in Gnathovorax cabreirai (CAPPA/UFSM 0009) and Saturnalia tupiniquim (MCP 3845‐PV). The internal cavity of the supraoccipital is laterally constricted at its mid‐length, resulting in an hourglass‐shaped surface (Figure 6b). The ventral extension of the bone, which forms its lateral wall, is medially excavated by the posterodorsal portion of a deep floccular recess (Figure 6c), which resembles the condition in Gnathovorax cabreirai (CAPPA/UFSM 0009), Saturnalia tupiniquim (MCP 3845‐PV; Bronzati et al., 2017), and Lewisuchus admixtus (CRILAR‐Pv 552; Ezcurra et al., 2019). In post‐Carnian sauropodomorphs, this recess is shallow (e.g., Plateosaurus—MB.R.5586‐1; Bronzati et al., 2017), while in theropods, it is generally well developed (Paulina‐Carabajal, 2015).

FIGURE 6.

FIGURE 6

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Bones of the posterior portion of the braincase of CAPPA/UFSM 0035. Supraoccipital in dorsal (a), ventral (b), and anterior (c) views. Otoccipital left lateral (d), posterior (e), and left lateroventral views. cmcv, groove for the caudal middle cerebral vein; fc, fossa cerebelli; fm, foramen magnum; fo, fenestra ovalis; fr, floccular recess; mf, metotic foramen; pp, paraoccipital process; sg, stapedial groove; XII, foramen for the hypoglossal nerve

3.1.6. Otoccipital

Both otoccipitals are preserved. Müller et al. (2018a) commented on a putative suture between the exoccipital and opisthotic on the left side of the skull. However, even with the aid of computed tomography, the suture is difficult to define or it is absent. We therefore consider that the bones are ossified as a single element, the otoccipital (sensu Sampson & Witmer, 2007). Each otoccipital (Figure 6d–f) forms the corresponding lateral border of the foramen magnum. There are several contacts at the anterior margin of the bone. The dorsalmost contact occurs with the supraoccipital, while more ventrally, the bone articulates against the prootic. Ventral to the contact with the prootic, the otoccipital forms the posterior margin of the fenestra ovalis (Figure 6d), which is located at the same anteroventral level in relation to the semilunar depression of the parabasisphenoid. The structure that forms the posterior margin of the fenestra ovalis is the crista interfenestralis, and its ventral tip rests on the dorsal surface of the contact between the basioccipital and the parabasisphenoid. This crest is anteriorly along its dorsoventral axis, resulting in a convex anterior surface (Figure 6f). The shape of this structure resembles that found in other sauropodomorphs, such as Saturnalia tupiniquim (MCP 3845‐PV), Efrasia minor (SMNS 12667; Bronzati & Rauhut, 2018), and Plateosaurus erlenbergiensis (AMNH FARB 6810; Prieto‐Márquez & Norell, 2011). In contrast, the crista interfenestralis is mostly straight in Gnathovorax cabreirai (CAPPA/UFSM 0009). The wide metotic foramen is bounded anteriorly by the crista interfenestralis and posteriorly by the exoccipital pillar (Figure 6f). This foramen possibly represents the path of three cranial nerves: the glossopharyngeal nerve (IX), the vagus nerve (X), and the accessory nerve (XI). There are two exits for the hypoglossal nerve (XII) on the lateral surface of the otoccipital. The exits are located almost on the same dorsoventral plane; however, one is anteriorly located relative to the other. Differently, some sauropods bear only one canal for the hypoglossal nerve (Knoll et al., 2019). The paraoccipital process projects posterolaterally, whereas in sauropods, the paraoccipital process projects laterally.

3.1.7. Parabasisphenoid

The parabasisphenoid (Figure 7a–d) forms the anterior floor of the endocranial cavity. The posterior portion of the dorsal surface of the bone is transversely concave and bears a longitudinal crest that extends until the basioccipital (Figure 7a). The crest separates the floor of the endocranial cavity in two distinct surfaces, following the arrangement of the basioccipital (see below). Anteriorly, the main body of the parabasisphenoid preserves a pituitary fossa at the same anteroposterior level of the basipterygoid process (Figure 7d). The fossa is separated from the floor of the endocranial cavity by a transverse dorsal expansion of the anterior surface of the parabasisphenoid, the dorsum sellae. In anterior view (Figure 7d), the fossa is U‐shaped rather than V‐shaped as in Saturnalia tupiniquim (MCP 3845‐PV; Bronzati et al., 2018a) and Plateosaurus engelhardti (AMNH 6810). The fossa is approximately as wide as deep and anteriorly bounded by the cultriform process. Also, the height of the fossa is less than two times the height of the forebrain, while in sauropods the fossa is about the same height of the forebrain, or even larger (e.g., Edinger, 1942; Paulina‐Carabajal, 2012; Sereno et al., 2007). Additionally, the floor of the fossa lies slightly ventral to the floor of the foramen magnum in B.schultzi, while in sauropods it is far more ventrally located (e.g., Knoll et al., 2019). The pituitary fossa seems vertically oriented, whereas the shape of the pituitary fossa suggests that it was posteroventrally oriented in Gnathovorax cabreirai (CAPPA/UFSM 0009). As in Adeopapposaurus mognai (PVSJ 568; Martínez, 2009), sauropods (e.g., Spinophorosaurus nigerensis—GCP‐CV‐4229; Knoll et al., 2012), and some theropods (e.g., Murusraptor barrosaensis—MCF‐PVPH 411; Paulina‐Carabajal & Currie, 2017), the floor of the pituitary fossa is perforated by a pair of foramina for the internal carotid artery. However, in some theropods (e.g., Piatnitzkysaurus floresi—PVL 4073; Giganotosaurus carolini—MUCPV‐CH 1), these openings are confluent (Paulina‐Carabajal, 2015). On the lateral surface of the parabasisphenoid, posterior to the basipterygoid process, there is an anterior tympanic recess, which extends posterodorsally (Figure 7c). This condition resembles Saturnalia tupiniquim (MCP 3845‐PV), Ixalerpeton polesinensis (ULBRA‐PVT059), and Silesaurus opolensis (ZPAL Ab III/364/1), whereas in Gnathovorax cabreirai (CAPPA/UFSM 0009), the main axis of the recess is dorsoventrally oriented. Posterior to the recess, there is a semilunar depression (Figure 7c). The cultriform process extends anteriorly, and its ventral margin is located below the level of the occipital condyle, like in Gnathovorax cabreirai (CAPPA/UFSM 0009), Saturnalia tupiniquim (MCP 3845‐PV), and Plateosaurus erlenbergiensis (AMNH FARB 6810). On the other hand, in Massospondylus carinatus (BP/1/5241; Chapelle & Choiniere, 2018), Ngwevu intloko (BP/1/4779; Chapelle et al., 2019), and Silesaurus opolensis (ZPAL Ab III/361; Piechowski et al., 2019) both structures are almost on the same longitudinal plane. In Tawa hallae (GR 241; Nesbitt et al., 2009) and Zupaysaurus rougieri (PULR 076; Paulina‐Carabajal et al., 2019), the occipital condyle is just slightly more dorsally located in relation to the cultriform process. The morphology of the cultriform process is similar to that of Saturnalia tupiniquim (MCP 3845‐PV; Bronzati et al., 2018a), bearing a deep longitudinal groove along its dorsal surface (Figure 7a).

FIGURE 7.

FIGURE 7

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Bones of the floor of the braincase of CAPPA/UFSM 0035. Parabasisphenoid and basioccipital in dorsal (a) and ventral (b) views. Parabasisphenoid in (c) left lateral and (d) anterior views. Basioccipital in right lateral view (e). atr, anterior tympanic recess; bp, basipterygoid process; bpr, basisphenoid recess; bt, basal tubera; cp, cultriform process; cr, crest; dlg, dorsal longitudinal groove; ds, dorsum sellae; fec, floor of the endocranial cavity; oc, occipital condyle; pf, pituitary fossa; sd, semilunar depression; ssr, subsellar recess; vlg, ventral longitudinal groove

3.1.8. Basioccipital

The basioccipital (Figure 7a–c,e) forms most of the floor of the endocranial cavity and it is transversely concave in posterior view. Distinct from sauropods, the basicranium is elongated, about to 1.5 times longer than wide (i.e., the length of the basioccipital plus basisphenoid divided by the maximum transverse length of the basal tubera region). The occipital condyle is dorsoventrally compressed (wider than taller). The anterior portion of the basioccipital articulates against the parabasisphenoid through a transversely wide U‐shaped suture (Figure 7b), such as in Efraasia minor (SMNS 12667; Bronzati & Rauhut, 2018). The suture between these bones is V‐shaped in the herrerasaurid Gnathovorax cabreirai (CAPPA/UFSM 0009). The posterior portion of the basioccipital forms the ventral surface of the foramen magnum. The floor of the basioccipital is smooth along its posterior half, but anteriorly it is divided in two lateral surfaces by a low longitudinal crest (=eminentia medullaris; Figure 7a), which seems absent or quite reduced in Gnathovorax cabreirai (CAPPA/UFSM 0009), but is present in several sauropodomorph dinosaurs, such as Adeopapposaurus mognai (PVSJ‐568; Martínez, 2009), Plateosaurus engelhardti (MB.R.4396), and Macrocollum itaquii (CAPPA/UFSM 0001d). These two surfaces form a pair of distinct channels that exit laterally to form the floor of the metotic foramen (Figure 7a).

3.1.9. Cranial endocast

The sigmoidal cranial endocast (Figure 8a–e) differs from the midbrain of Plateosaurus engelhardti (AMNH 6810), which displays larger flexure points in lateral view (Galton, 1985). In fact, the overall form of the endocast is highly reminiscent of that observed in the endocasts of Triassic phytosaurs (Lautenschlager & Butler, 2016). A longitudinal groove divides both olfactory bulbs medially (Figure 8e). The ratio between the greatest linear dimension of the olfactory bulb and the transverse length of the cerebral hemispheres is approximately 0.40 (Table 5). In the sauropodomorph Macrocollum itaquii, this value is approximately 0.54. In sauropods, some variation in the value of this ratio is also observed: Spinophorosaurus =0.41; Camarasaurus =0.61; Diplodocus =0.56; and Sarmientosaurus =0.29. Similar to crocodilians and birds (e.g., Lohman & Smeets, 1993), there are no accessory bulbar formations other than the olfactory bulbs (Figure 8e). The bulbs connect to the cerebral hemispheres by an elongated olfactory tract that accounts for 25% (approximately 14 mm) of the total length (approximately 56 mm) of the reconstructed endocast (Table 5). The lateral expansion of the cerebral hemisphere does not exceed the maximum lateral extension of the lateral semicircular canal (LSC; Figure 8e). A shallow longitudinal groove divides the cerebral hemisphere in two distinct portions. It is difficult to confirm if this groove corresponds to the longitudinal fissure (e.g., Witmer et al., 2008) or if it corresponds to a taphonomic artifact. The anterior dorsal surface of the cerebral hemispheres is slightly depressed in lateral view. A relatively well‐developed dorsal expansion (=dural peak) marks the anterior portion of the cerebellum (Figure 8d), making the limits of the hind‐ and midbrain easily distinguishable in lateral view. On the other hand, the dural expansion is less dorsally developed in Plateosaurus engelhardti (AMNH 6810; Galton, 1985), resulting in a rather straight dorsal margin of this portion of the brain endocast in lateral view (Paulina‐Carabajal et al., 2019). In dorsal view, the hindbrain is “hour‐glass” in shape, as it is constricted at the middle portion. On the lateral surfaces of the anterior half of the cerebellum, there is a well‐developed flocculus (floccular and parafloccular lobe; Figure 8e; Table 5), which resembles the morphology of Saturnalia tupiniquim (MCP‐3845‐PV; Bronzati et al., 2017). In these taxa, the flocculus of the cerebellum fills great portion of the space between the semicircular canals. However, it differs from the extremely enlarged flocculus of Velociraptor mongoliensis (IGM 100/976; King et al., 2020), which fills the entire space between the canals. Differently, in the non‐sauropodan sauropodomorph Ngwevu intloko (BP/1/4779; Chapelle et al., 2019), the flocculus is much less developed, not invading the space between the semicircular canals as in the dinosaurs above mentioned, a condition that also seems true for the herrerasaurid Herrerasaurus ischigualastensis (Stocker et al., 2016, figure S1U). The pituitary gland of B.schultzi (Figure 8d) projects ventrally and it is relatively small (i.e., it does not project more ventrally than the floor of the endocranial cavity) in comparison to the condition of sauropods (Paulina‐Carabajal, 2012) and some theropods (e.g., Zupaysaurus rougieri and Sinraptor dongi; Paulina‐Carabajal & Currie, 2012; Paulina‐Carabajal et al., 2019).

FIGURE 8.

FIGURE 8

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Cranial endocast of CAPPA/UFSM 0035 and other early dinosaurs. Three‐dimensional rendering of the skull of CAPPA/UFSM 0035 in left dorsolateral (a) and posterodorsal (b) views. (c) Neurocranium and cranial endocast of CAPPA/UFSM 0035. Cranial endocast of CAPPA/UFSM 0035 in left lateral (d) and dorsal (e) views. Left inner ear in lateral (f) and dorsal (g) views. Cranial endocasts of Gnathovorax cabreirai (CAPPA/UFSM 0009) (h) and Macrocollum itaquii (CAPPA/UFSM 0001b) (i) in dorsal view. asc, anterior semicircular canal; ch, cerebral hemisphere; cmcv, groove for the caudal middle cerebral vein; co, cochleae; de, dorsal expansion; el, endosseous labyrinth; f, frontal; fl, flocculus; fm, foramen magnum; if, interhemispheric fissure; lsc, lateral semicircular canal; ob, olfactory bulb; ot, olfactory tract; p, parietal; pit, pituitary; pp, paraoccipital process; ppf, postparietal fenestra; psc, posterior semicircular canal; V, trigeminal nerve; VII, facial nerve; XII, hypoglossal nerve

TABLE 5.

Measurements of the cranial endocast of CAPPA/UFSM 0035

Element measured
Maximum anteroposterior length 56 mm
Maximum width 16.7 mm
Minimum width 6.5 mm
Total volume 2.8 ml
Olfactory bulb anteroposterior length 6.8 mm
Olfactory tract anteroposterior length 14 mm
Cerebellum height 10.1 mm
Cerebellum width 8.3 mm
Pontine flexure angle 151.9°
Floccular lobe length 3.3 mm
Angle of floccular lobe orientation 101º
Total floccular volume 0.011 ml
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3.1.10. Inner ear

The preservation status of CAPPA/UFSM 0035 allowed the reconstruction of part of the endosseous labyrinth on the left side of the skull (Figure 8f,g)—the areas corresponding to the semicircular canals and vestibule could be reconstructed, but most of the cochlear portion is missing. With the LSC horizontally aligned, the maximum height of the anterior semicircular canal (ASC) is approximately 1.2, the maximum height of the posterior semicircular canal (PSC). The ASC is taller than the PSC in other early dinosaurs, such as Saturnalia tupiniquim (MCP‐3845‐PV; Bronzati et al., 2017), Gnathovorax cabreirai (Pacheco et al., 2019), and Herrerasaurus ischigualastensis (Stocker et al., 2016). In dorsal view, the angle of divergence between these canals is approximately 80º, such as in Saturnalia tupiniquim (MCP‐3845‐PV; Bronzati et al., 2017). The PSC is arched in dorsal view, with the concave margin posteriorly directed. This condition resembles that of Herrerasaurus ischigualastensis (Stocker et al., 2016), Massospondylus carinatus (Chapelle & Choiniere, 2018), and Gnathovorax cabreirai (Pacheco et al., 2019), whereas in some other sauropodomorphs, this rim is straight (e.g., Plateosaurus sp.—MB.R.5586‐1; unnamed sauropodiform—OUMNH J13596; Bronzati et al., 2017). The crus commune is gently caudally curved. The maximum length of the endosseous cochlear duct is uncertain.

3.2. Phylogenetic analysis

The heuristic search recovered 24 most parsimonious trees of 1555 steps each (consistency index = 0.304; retention index = 0.672). The topology of the strict consensus tree is equivalent to that of Müller (2019) and depicts Buriolestes schultzi as the sister taxon of all other sauropodomorphs (Figure 9).

FIGURE 9.

FIGURE 9

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Reduced strict consensus tree depicting the phylogenetic position of Buriolestes schultzi. Life reconstructions by Márcio L. Castro

3.3. Body mass estimations

Applying the equation based on the relation between body mass and femoral circumference (=43.27 mm in Buriolestes), the resulting estimated body mass for Buriolestes schultzi is 6.65 kg. In the second approach, which is based on convex hulls, the total body mass (i.e., the sum of the masses estimated for each segment) was estimated in 4.35 kg. Finally, the body mass estimated for the 3D sculpture is 4.50 kg.

3.4. Reptile Encephalization Quotient

The volume of the brain endocast (including the olfactory bulbs) of Buriolestes schultzi is approximately 2.8 ml. So, for the body mass estimate based on the femoral circumference, the minimum calculated REQ using 37% of brain endocast volume is 0.51, whereas the maximum calculated REQ using 50% of brain endocast volume is 0.69 (Table 6). For the body mass estimate based on the convex hulls, the minimum calculated REQ using 37% of brain endocast volume is 0.65, whereas the maximum calculated REQ using 50% of brain endocast volume is 0.87. Despite its well‐preserved status, the braincase of CAPPA/UFSM 0035 shows some gentle degree of compression. Therefore, the brain cavity was perhaps a bit more inflated than the reconstructed endocast. As a result, the REQ for B.schultzi might have been a bit higher.

TABLE 6.

Endocranial values, body mass, and REQ of Buriolestes compared to other dinosaurs (modified from Paulina‐Carabajal & Currie, 2017)

Taxon EV (ml) Mbr (ml) 37% Mbr (ml) 50% Mbd (kg) REQ 37% REQ 50% REQ 100%
Buriolestes 2.8 1.67 1.4 4.35 a 0.65 0.87 1.76
Buriolestes 2.8 1.67 1.4 6.65 b 0.51 0.69 1.39
Diplodocus1 110 40.7 55 13,000 0.31 0.41 0.82
Nigersaurus 2 55.3 20.5 27.7 3640 0.31 0.42 0.84
Brachiosaurus 2 186 68.8 93 26,300 0.35 0.47 0.95
Amurosaurus 3 290 107,3 145 2030 2.25 3.04 6.08
Amurosaurus 3 290 107.3 145 4790 1.40 1.89 3.78
Murusraptor 148.2 54.8 74.1 1551 1.33 1.8 3.6
Giganotosaurus 275 101.7 137.5 7000 1.07 1.4 2.9
Carcharodontosaurus 263.6 97.5 131.8 7000 1.03 1.4 2.79
Sinraptor dingi 95 35.1 47.5 1700 0.81 1.1 2.19
Allosaurus 169 62.5 84.5 1400 1.3 1.8 3.28
Allosaurus 188 69.5 93.9 2300 1.8 2.4 3.68
Majungasaurus 106.4 39.4 53.2 1130 1.14 1.54 3.28
Tyrannosaurus 414.2 153.2 207.1 5654 1.8 2.5 4.4
Tyrannosaurus 414.2 153.2 207.1 7000 1.6 2.2 4.49
Troodon 4 41 15.17 20.5 45 2.61 3.53 7.07
Dromiceiomimus 4 87.85 32.50 43.96 125 3.14 4.31 8.60
Dromiceiomimus 4 87.85 32.50 43.96 175 2.61 3.58 7.15
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1Witmer et al. (2008); 2Knoll and Schwarz‐Wings (2009); 3Lauters et al. (2013); 4Hurlburt (1996).

Abbreviations: EV, endocranial volume; Mbd, body mass; Mbr, brain volume; REQ, Reptile Encephalization Quotient.

a

Estimated mass based on convex hull.

b

Estimated mass based on femoral circumference.

4. DISCUSSION

The cranial endocast of Buriolestes sheds light on the early evolution of the brain in sauropodomorph dinosaurs. The olfactory tract of Buriolestes is elongated, differing from the short tract observed in later forms such as the non‐sauropod sauropodomorphs Macrocollum and Ngwewu, and sauropods (Sereno et al., 2007; Witmer et al., 2008). An elongated olfactory tract is observed in saurischians outside Theropoda/Sauropodomorpha, such as the herrerasaurids Gnathovorax (Figure 8h). On the other hand, the olfactory tract of some theropods such as Zupaysaurus and Megapnosaurus does not seem as elongated as that of Buriolestes, indicating great plasticity in the size of this structure among early dinosaurs. Thus, it is still not possible to confirm if the elongated tract of Buriolestes corresponds to the ancestral condition of Sauropodomorpha, with a reduction occurring in later forms during the Late Triassic—Norian (Figure 10); or if the condition of Buriolestes is autapomorphic for this taxon among sauropodomorphs.

FIGURE 10.

FIGURE 10

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Time‐calibrated simplified phylogenetic tree of early dinosaurs (composite from Langer et al., 2014; Müller, 2019; Pacheco et al., 2019) and comparison of selected cranial endocasts in dorsal and left lateral views. Megapnosaurus from Raath (1977); Zupaysaurus from Paulina‐Carabajal et al. (2019); Sinosaurus from Xing et al. (2014); Allosaurus from Rogers (1998); Plateosaurus from Bronzati et al. (2017); Ngwevu from Sereno et al. (2007); Spinophorosaurus from Knoll et al. (2012). The limits of the olfactory tract are approximated. Silhouettes based on the artwork by Márcio L. Castro, Douglas M. Heman, Leonello Calvetti, and Daniel Eskridge

Regarding the olfactory bulbs, the ratio between bulb and cerebrum sizes (olfactory ratio) in Buriolestes is low in comparison to other sauropodomorphs (including sauropods, except Sarmientosaurus). Actually, some sauropods exhibit well‐developed olfactory bulbs, such as Camarasaurus (CM 11338; Witmer et al., 2008), which approaches the olfactory ratio of Tyrannosaurus (Zelenitsky et al., 2009). As the size of the bulbs is a better proxy to estimate olfactory capabilities in dinosaurs than is the size of the olfactory tract (Hughes & Finarelli, 2019; Steiger et al., 2009; Zelenitsky et al., 2009, 2011), there is evidence to suggest an increase in the olfactory capabilities of some later sauropodomorphs when compared to Buriolestes. On the other hand, the reduction of the olfactory tract in the sauropodomorph lineage, as discussed above, could be related to the relative skull reduction experienced by the lineage, especially in sauropods (see Bronzati et al., 2018b). Alternatively, the reduction of the tract in later sauropodomorphs could represent a paedomorphic condition retained in forms with short skulls. For instance, during ontogeny, there is an increase in the length of the olfactory tract among extant crocodilians; whereas early juveniles of crocodilians exhibit shorter tract, adult forms exhibit a much longer tract (Jirak & Janacek, 2017). Conversely, a putative explanation for the increase in the olfactory ratio in the lineage is related to the acquisition of a more complex social behavior, which relies on the olfactory sense in several vertebrate groups (e.g., capability to track chemical secretions; Martín & López, 2012). The oldest evidence of gregarious behavior in sauropodomorphs is an association of three semi‐articulated individuals of Macrocollum from the early Norian (c. 225 Ma) of Brazil (Müller et al., 2018b). This dinosaur bears a relatively high olfactory ratio (0.54) when compared to Buriolestes (0.40). Alternatively, it has also been observed that high olfactory capabilities played an important role in foraging, helping animals to better discriminate between digestible and indigestible plants (Lautenschlager et al., 2012). Hence, the olfactory sense may have been affected by the dietary shift, toward a more omnivorous/herbivorous diet, experienced by sauropodomorphs during the Late Triassic (Barrett & Upchurch, 2007; Bronzati et al., 2019). Another putative explanation for the increase in the olfactory ratio relies on the capability to detect predator chemical cues (Kats & Dill, 1998). A wide range of reptiles exhibit behavioral responses to predator odor, such as avoidance (Webb et al., 2010), slows down (Jackson, 1990), and defense/aggressive behaviors (Phillips & Alberts, 1992).

The presence of an enlarged pituitary gland is well documented for the gigantic sauropods (Balanoff et al., 2010; Knoll et al., 2012; Paulina‐Carabajal, 2012; Sereno et al., 2007). The pituitary gland of Buriolestes is relatively smaller than that of sauropods and other non‐sauropod sauropodomorphs such as Plateosaurus and Ngwevu. For instance, the ventral limit of the pituitary gland extends ventrally in relation to the floor of the endocranial cavity in later sauropodomorphs than it does in Buriolestes (Figure 10). Additionally, the height of the gland in Buriolestes is smaller than the height of the ASC of the inner ear, with the inverse relation being found among later sauropodomorphs, including sauropods (Figure 10) such as Spinophorosaurus (GCP‐CV‐4229; Knoll et al., 2012), Ampelosaurus (MCCM‐HUE‐8741; Knoll et al., 2013), and Sarmientosaurus (MDT‐PV 2; Martínez et al., 2016). Buriolestes corresponds to the first Carnian sauropodomorph for which information on the size of the pituitary gland is available, and the reduced size of this structure in this taxon might be an indicator that pituitary gland increased in size in the sauropodomorph lineage. The small size of this structure in Buriolestes in comparison to sauropods is expected, as a positive allometric relationship between the size of the gland and total body size has been advocated (Edinger, 1942).

The endocast of Buriolestes exhibits a well‐developed flocculus (=floccular fossae lobe, Ferreira‐Cardoso et al., 2017) of the cerebellum, with this structure projecting into the space between the semicircular canals (Figure 8). The condition in Buriolestes reinforces the hypothesis that the presence of a well‐developed flocculus corresponds to the ancestral condition of sauropodomorphs, as this condition is also observed in another of the earliest sauropodomorphs, Saturnalia (Bronzati et al., 2017). In later sauropodomorphs, such as Ngwevu and Plateosaurus, this structure is far less developed (Bronzati et al., 2017; Sereno et al., 2007). Additionally, the flocculus of large‐bodied sauropods is practically indistinguishable in the endocast (e.g., Spinophorosaurus—GCP‐CV‐4229, Knoll et al., 2012; Bonatitan—MACN 821; Paulina‐Carabajal, 2012). Conversely, the presence of an enlarged flocculus is observed in herrerasaurids such as Herrerasaurus (Stocker et al., 2016) and Gnathovorax (Pacheco et al., 2019), and non‐dinosaurian dinosauriforms such as Silesaurus (Piechowski et al., 2019) and Lewisuchus (Ezcurra et al., 2019). The flocculus interprets data gathered by the vestibular portions of the endosseous labyrinth, which are related with the coordination of eye, head, and neck movements, and also gaze stabilization in extant vertebrates (Stocker et al., 2016; Voogd & Wylie, 2004; Witmer et al., 2003). The reduction in size of this structure in Sauropodomorpha has been tentatively assigned to a shift toward a more omnivorous/herbivorous diet (Bronzati et al., 2017), in a scenario where these types of diets would require lower levels of neural processing (=lower floccular volume) for coordinating head and neck movements and gaze stabilization in relation to what is expected for predatory animals. Indeed, among birds, predatory forms have generally more developed flocculus in relation to non‐predatory ones (Ferreira‐Cardoso et al., 2017). In this sense, the level of development of this structure in Buriolestes, alongside the presence of a ziphodont dentition (Müller et al., 2018a), which is typical of faunivorous taxa (Cabreira et al., 2016), is compatible with the scenario proposed for Sauropodomorpha regarding the evolution of the flocculus and feeding behavior (Bronzati et al., 2017). It is however worth mentioning that the size of the floccular fossa might not be a good proxy for estimating the actual size of the floccular lobe of the cerebellum because other soft tissues rather than solely brain tissues can also fill the space of the fossa (Ferreira‐Cardoso et al., 2017; Walsh et al., 2013).

The REQ of Buriolestes is higher than that of sauropods (Figure 11). However, it is still difficult to confidently track changes in brain size in Sauropodomorpha due to the lack of taxa possessing complete endocasts. Nevertheless, the fact that an early member of the clade exhibits an REQ higher than the later representatives suggests a decrease in encephalization in the lineage. Differences in relative brain size between Buriolestes and sauropods are likely related to differences in body size. The presence of relatively smaller brains observed among sauropods corresponds to what is expected for giant animals, as brain and body sizes show negative allometry (Hopson, 1979). Despite the evidence for the presence of a relatively larger brain in Buriolestes when compared to later sauropodomorphs, it is interesting to note that the REQ of this taxon is still lower than that of all other theropods for which the quotient has been calculated (Paulina‐Carabajal & Currie, 2017; Table 6; Figure 11). However, comparisons between the brain size of Buriolestes with that of other Late Triassic dinosaurs is still hampered by the scarce cranial endocasts for dinosaurs of this period, and also by the impossibility of estimating body mass for those taxa for which a complete cranial endocast is available (e.g., Zupaysaurus—Paulina‐Carabajal et al., 2019).

FIGURE 11.

FIGURE 11

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Time‐calibrated Reptile Encephalization Quotient (REQ; 50%) of selected saurischians. See Table 4 for the sources. The REQ of Buriolestes schultzi is based on the average of the estimates presented here. Silhouettes based on the artwork by Douglas M. Heman, Julius Csotonyi, Mohamad Haghani, Scott Hartman, Rodolfo A. Coria, Nobu Tamura, Hum3D Team, and Sereno et al. (2007)

The evidence gathered from the cranial endocast of Buriolestes provides some clues on its autoecology. The olfactory sense was not high (at least when compared to later sauropodomorphs), whereas the flocculus was well developed. Therefore, it is more likely that Buriolestes hunted and tracked prey based on optical capability instead of the olfactory sense. Moreover, the size of the olfactory bulbs does not provide strong support for activity in low‐light conditions (Zelenitsky et al, 2009). Indeed, the tibia is longer than the femur in Buriolestes, which is usually regarded as indicative of cursoriality, a typical condition of fast predators (e.g., deinonychosaurs and troodontids; Persons & Currie, 2016). That said, the combination of dental, postcranial, and cerebral data suggest Buriolestes as an active small predator, which was able to track moving prey (Figure 12). On the other hand, sauropods were non‐cursorial large herbivores, which is the inverse condition when compared to Buriolestes. Hence, this drastic shift may reflect—to some degree—the REQ decrease experienced by sauropodomorph lineage during the Mesozoic. Indeed, it has been observed that predatory mammals have higher encephalization quotients than their preys (Finlay et al., 2001; Jerison, 1973).

FIGURE 12.

FIGURE 12

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Life reconstruction of Buriolestes schultzi preying on a small lepidosauromorph in a Triassic landscape from Brazil. By Márcio L. Castro

5. CONCLUSIONS

The use of computed tomography helped us to investigate and describe the endocranial anatomy of the early sauropodomorph Buriolestes schultzi (Figure 12). The anatomy of the bones forming the neurocranium resembles that of other coeval sauropodomorphs. However, the preservation degree of CAPPA/UFSM 0035 associated with the CT scan technique made it possible to reconstruct the first complete endocast of an early sauropodomorph. In summary, the shape of the endocast of Buriolestes differs from that of post‐Carnian sauropodomorphs by: (i) the elongated olfactory tract; (ii) relatively small olfactory bulbs; (iii) a well‐developed flocculus of the cerebellum; and (iv) relatively small pituitary gland. These traits change drastically across the evolutionary history of sauropodomorphs, reaching the opposite morphology in sauropods. This scenario suggests that neuroanatomical changes were potentially linked to modifications in the body plan of sauropodomorphs, and that they also played an important role in ecological shifts during the evolution of sauropodomorphs. Furthermore, we presented here the first REQ for a Triassic dinosaur (to our knowledge). The result demonstrates that the REQ decreases across the time in the lineage of sauropodomorphs, probably related to the behavioral shift and/or body mass increasing experienced during the Late Triassic. In contrast, the REQ of Buriolestes is lower than that of Jurassic theropods.

AUTHOR CONTRIBUTIONS

R.T.M. conduced the fieldwork, performed the mechanical preparation of the specimen, performed the phylogenetic analysis, and drafted the first version of the manuscript. J.D.F. performed the segmentations, generated the three‐dimensional rendering of the elements, and calculated the Reptile Encephalization Quotient. F.A.P. performed the laser scanning and body mass estimations. L.K. funded the acquisition of the μCT and accompanied the scanning process. M.B. performed additional acquisition of data. All authors contributed to experimental design and wrote the final version of the manuscript.

ACKNOWLEDGMENTS

We thank Fabien Knoll, Logan King, and an anonymous reviewer for valuable comments that greatly improved this manuscript. We also thank the Willi Henning Society, for the gratuity of TNT software. ‬J‬.D.F. is supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. M.B. is supported by the São Paulo Research Foundation (FAPESP 2018/18145‐9). L.K. is supported by the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS 17/2551‐0000816‐2) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 422568/2018‐0; 309414/2019‐9)‬‬.

Müller R.T, Ferreira J.D., Pretto F.A., Bronzati M., & Kerber L.. The endocranial anatomy of Buriolestes schultzi (Dinosauria: Saurischia) and the early evolution of brain tissues in sauropodomorph dinosaurs. J. Anat. 2021;238:809–827. 10.1111/joa.13350

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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