A tamerican museum Novitates PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3677, 29 pp., 10 figures, 1 table March 4, 2010 The Braincase of Apatosaurus (Dinosauria: Sauropoda) Based on Computed Tomography of a New Specimen with Comments on Variation and Evolution in Sauropod Neuroanatomy AMY M. BALANOFF,1’2 GABE S. BEVER,3* AND TAKEHITO IKEJIRI4 ABSTRACT We describe a previously unreported braincase of the sauropod dinosaur Apatosaurus from the Cactus Park Quarry, Morrison Formation of western Colorado using high-resolution X-ray computed tomography. The digital nature of these data allowed us to prepare and describe the first three-dimensional rendering of the endocranial space in this historically important dinosaur species. Results are compared with a range of taxa drawn from across the sauropod tree revealing previously underappreciated variation in the sauropod neurocranium. Examples of variable characters include the degree of cerebral and pontine flexure, the morphology of the parietal body and superior sagittal sinus and their relationship with the overlying dermal roof, and the conformation of several cranial nerve foramina. We provide preliminary evolutionary hypotheses and discussion for many of these features. The recognition that considerable variation is present in the sauropod neurocranium hopefully will encourage more detailed descriptions of this anatomically complex region, as well as facilitating a synthetic review of the sauropodomorph braincase as these descriptions become available. 1 Division of Paleontology, American Museum of Natural History. 2 Department of Earth and Environmental Sciences, Columbia University. 3 Division of Paleontology, American Museum of Natural History. * Current address: Department of Geology and Geophysics, Yale University, 210 Whitney Avenue, New Haven, CT 06520. 4 Museum of Paleontology and Department of Geological Sciences, University of Michigan, 1109 Geddes Road, Ann Arbor, MI 48109-1079. Copyright © American Museum of Natural History 2010 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3677 INTRODUCTION Institutional abbreviations used in this study: AMNH (American Museum of Natural His¬ The complex nature of the vertebrate brain- tory, New York, New York); BYU (Brigham case makes this region a rich source of Young University, Earth Science Museum, phylogenetically informative data. The brain- Provo, Utah); CM (Carnegie Museum of case and neuroanatomy of sauropod dinosaurs, Natural History, Pittsburgh, Pennsylvania); however, historically have played a relatively HMS (Houston Museum of Natural Science, minor role in shaping hypotheses with regards Houston, Texas); YPM (Yale University, to the phylogenetic and evolutionary history of Peabody Museum of Natural History, New this unique and interesting group. This relative Haven, Connecticut). lack of influence undoubtedly stems from the rarity with which well-preserved cranial mate¬ MATERIALS AND METHODS rial is recovered, with the postcranial elements Specimen traditionally considered diagnostic for refined taxonomic levels within this group (Tidwell and We describe a fairly complete, well-pre¬ Carpenter, 2003; see Wilson, 2002: table 8). served braincase of Apatosaurus (BYU 17096; This preservational gap translates directly to figs. 1, 2), using HRCT. BYU 17096 was the existing disparity in our understanding of collected from the Jurassic Morrison morphological variation for these respective Formation of the Cactus Park BYU Quarry anatomical systems across Sauropoda and in western Colorado. The endocranial space is reinforces the need for detailed anatomical completely infilled with a fine-grained sand¬ description and comparison of whatever crani¬ stone matrix. The allocation of BYU 17096 to al data are available. One way to increase the Apatosaurus is based in part on the hundreds return of anatomical data from a particular of disarticulated and semiarticulated postcra¬ specimen is through the use of high-resolution nial bones diagnosable to Apatosaurus (espe¬ X-ray computed tomography (HRCT). HRCT cially cervicals, dorsals, anterior caudals, and is a nondestructive tool for visualizing internal relatively robust limb bones) that were found structures and is particularly useful for study¬ in the same quarry (Curtice and Wilhite, 1996; ing the complex internal anatomy of a fossilized Foster, 2003). None of the other genera braincase (Carlson et al., 2003). In addition to common in the Morrison Formation, such as providing access to internal cranial features Diplodocus and Camarasaurus, were recovered such as the presence/absence of bony contacts from the Cactus Park Quarry. The diagnosis and processes, HRCT enhances our ability to of BYU 17096 to Apatosaurus also is based on visualize and interpret soft-tissue structures of observed braincase apomorphies discussed in the central nervous, circulatory, and endocrine the Phylogenetic Diagnosis section below. systems that are housed within the braincase. The purpose of this study is to provide a Scanning detailed description of a previously unreported braincase of Apatosaurus that includes the first BYU 17096 was scanned at the University of observations on the internal braincase anatomy Texas High-Resolution X-ray Computed of this taxon. Observed morphologies are Tomography Facility on 14 May 2004 using compared with selected sauropod and outgroup their high-energy system. Scanning was per¬ taxa allowing preliminary assessments of neu- formed using a brass filter and air wedge, a rocranial variation and evolution within voltage of 420 kV, and an amperage of 4.8 mA. Sauropoda. We review the published literature The resulting images were then processed for and explicitly establish baseline evolutionary the removal of ring and streak artifacts using hypotheses for a number of selected neurocra- programs written by Richard Ketcham. The nial features within Sauropoda. The hope is that specimen was scanned along the coronal axis these hypotheses will elicit future testing and for a total of 127 slices at an image resolution of provide the groundwork for more synthetic 1024 X 1024 pixels. The interslice spacing is studies examining broad patterns of neurocra- 1.0 mm, and the slice thickness is 0.8 mm. Each nial evolution within Sauropodomorpha. image has a reconstructed field of view of 2010 BALANOFF ET AL.: BRAINCASE OF APATOSAURUS 3 265 mm. The reconstruction of the endocranial briefly described and illustrated in the late endocast was done with the original 16-bit 19th and early 20th centuries (Marsh, 1880, imagery in the volumetric rendering program 1884; Holland, 1906; Osborn and Mook, 1921; VGStudioMax© 1.2.1. Contrast of the images Ostrom and McIntosh, 1966). An endocast of was increased until the infilled endocranial Diplodocus (AMNH 694) was described by space and bone were easily distinguishable from Marsh (1884, 1896) and reillustrated by each other. The endocranial cavity was selected Hopson (1979). Janensch (1935-36) described using the segmentation tools available in this an endocast of Brachiosaurus as well as two program, separated into its own volume, and diplodocoid taxa, Dicraeosaurus and Tornieria exported as an isosurface. All measurements of (Tornieria is referred to as Barosaurus in the braincase and endocast (including volume) Janensch [1935-36]; however, see Remes were taken in VGStudioMax©. Endocast vol¬ [2006] for updated taxonomy). Many of the ume measurements were taken by calculating more recent descriptions are based on synthetic the volume of negative space of the endocranial endocasts. These include Plateosaurus (Galton, cavity. For ease of description, features of the 1985), Shunosaurus (Chatterjee and Zheng, endocranial cast are referred to by the names of 2002), an early Cretaceous titanosauriform the soft tissues of the brain that they reflect (TMM 40435; Tidwell and Carpenter, 2003), (e.g., cerebrum rather than cast of cerebrum). It and Camarasaurus (Chatterjee and Zheng, is important to note, however, that what 2005; Sereno et al., 2007). A digital endocast actually is preserved is a cast of the endocranial was extracted from HMS 175 and described as space, which also reflects structures other than Diplodocus hayi (Franzosa, 2004), although the the brain, such as meninges and sinuses. This allocation of this specimen to Diplodocus is cast, however, is useful in determining relative questionable (see Harris, 2006). Comparative size and shape of different regions of the brain illustrations of a digital endocast of Diplodocus as well as recognizing the morphology of the also are available in Sereno et al. (2007). cranial nerve roots. The original slice data and movies showing the endocranial cast are DESCRIPTION available at the DigiMorph website (www. digimorph. org/specimens/Apatosaurus_sp). General Features Figures 1, 2 Taxonomic Comparisons BYU 17096 is an articulated braincase that The inclusion of cranial material into phylo¬ is complete in that it includes the right and left genetic analyses of sauropods (e.g., Wilson, orbitosphenoid, laterosphenoid, exoccipital- 2002; Upchurch et al., 2004; Rauhut et al., opisthotic, prootic, and the midline basisphe- 2005) makes the diagnosis of newly discovered noid, basioccipital, and supraoccipital. The material more confident. Previous descriptions paired frontal, parietal, squamosal, and post¬ of cranial material allocated to Apatosaurus orbital also are present as components of the include that of Berman and McIntosh (1978), dermal roof fused to the endochondral ele¬ who described a fairly complete skull (CM ments of the braincase. The braincase is well 11162) of a “probable” Apatosaurus (Berman preserved overall, although the distal extrem¬ and McIntosh, 1998: 21) and a partial braincase ities of several bones and processes are (YPM 1860) from the upper Jurassic Morrison broken. The dermal roofing components are Formation of Colorado. A partly disarticulat¬ better preserved on the right side of the skull. ed braincase is known from Como Bluff, The specimen is large overall (see table 1) and Wyoming (Connely and Hawley, 1998). In the cranial sutures are so tightly fused as to be addition to describing a new braincase of indistinguishable in many cases in external Apatosaurus, we present the only endocast that view (as is common in sauropods; e.g., Tidwell is known for this taxon. and Carpenter [2003], Wilson et al. [2005], The number of endocasts that exist for Remes [2006]). This advanced state of fusion is sauropodomorph taxa is surprisingly large, present in both the dermal roofing and although the majority of these were only endochondral elements, indicating skeletal 4 AMERICAN MUSEUM NOVITATES NO. 3677 supratemporal a A fenestra trochlear foramen trochlear foramen oculomotor \- l / fenestra 4 optic crista foramen ntotical trigeminal fenestra abducens foramen' \ crista ^ prootica lateral basipterygoid olfaGtory cranja| carotid process of process fenestra foramen crista prootica frontoparietal supratemporal fenestra fenestra basipterygoid postparietai I, nuchal process foramen occipital crest condyle basal cramopharyngeal tubera foramen hypoglossal foramina postorbital paroccipital process nuchal occipital crest condyle Fig. 1. Braincase of BYU 17096 in right lateral (A), left lateral (B), dorsal (C), and ventral (D) views. 2010 BALANOFF ET AL.: BRAINCASE OF APATOSAURUS 5 fenestra fenestra lateral postorbital process of / external occipital process foramen •i* foramen magnum occipuai paroccipital condyle process process of crista prootica bas tubera basipterygoid process Fig. 2. Braincase of BYU 17096 in anterior (A) and posterior (B) views. 6 AMERICAN MUSEUM NOVITATES NO. 3677 TABLE 1 Hopson (1979) noted this opening may not Measurements taken from BYU 17096 represent the parietal foramen but rather was All measurements are in mm. possibly filled with part of the cartilaginous endocranium or with a portion of the superior Transverse width of parietals 169.6 sagittal sinus (or a combination of the dorsal Anteroposterior length of parietals 30.2 longitudinal and transverse sinuses; Witmer and Dorsoventral height of supraoccipital 52.0 Ridgely, 2009). The opening in BYU 17096 is Transverse width of supraoccipital 60.8 confluent with the superior sagittal sinus that Transverse width of foramen magnum 24.6 otherwise is enclosed within the paired parietals Dorsoventral height of foramen magnum 27.6 Anteroposterior width of supratemporal fenestra 21.2 (see description of endocast below). The open¬ Transverse length of supratemporal fenestra 39.7 ing also resides at a position homologous to the Anteroposterior length of frontoparietal fenestra 33.6 frontoparietal fontanelle of amniote embryos. Transverse width of frontoparietal fenestra 25.6 Therefore, it is possible that an anterodorsal Anteroposterior length of skull 94.0 expansion of the superior sagittal sinus into the Transverse width of skull across metotic foramina 31.5 space between the developing elements of the Transverse width of skull across paroccipital dermal roof influenced the developmental processes 169.2 dynamics of that region and thus resulted in Anteroposterior length of endocast 72.5 Transverse width of endocast at widest point 49.4 the paedomorphic retention of the frontopari¬ etal fontanelle in the adult skull as the frontoparietal fenestra. maturity for these cranial partitions (but not The shape of the frontoparietal fenestra in necessarily indicative of sexual maturation or BYU 17096 is not perfectly circular but rather maturation of other skeletal regions). The exhibits a brief constriction near its posterior HRCT slices did help considerably in locating margin due to a slight medially directed cur¬ at least some of these sutures by revealing their vature of the parietals (fig. 1C). This constric¬ location deep to the external surface (fig. 3). tion results in an incomplete partitioning of the Their three-dimensional paths could then be fenestra into a relatively large anterior section traced superficially to the external surface of the and a much smaller posterior opening. This specimen. Our ability to do this indicates that partitioning suggests that the frontoparietal the degree of fusion is not uniform along the fenestra may have housed two separate soft- three-dimensional path of these sutures and that bodied structures (positioned anteriorly and cranial fusion often occurs first at the external posteriorly, respectively). The anterior compo¬ surface of the skull and progresses deeper. nent may have housed the parietal (pineal) body, with a dorsal peak of the superior sagittal Dermal Roof sinus filling the posterior partition (see Witmer and Ridgely, 2009). This medial constriction of Frontoparietal Fenestra: The dorsal sur¬ the parietals and associated partitioning of the face of BYU 17096 is formed largely by the frontoparietal fenestra is common in sauropods dermal roofing elements, which overlie the that exhibit this dorsal opening, and a complete anterior two-thirds of the endocranial cavity. The dorsal surface is slightly concave up in division of the fenestra through medial contact overall shape and is dominated by a large of the parietals is known within this group (e.g., central opening that lies at the junction of the Amargasaurus cazauv, Salgado and Calvo, 1992; paired frontals and parietals. This opening Salgado, 1999). This posterior opening gener¬ constitutes a broad communication (table 1) ally is described as the postparietal foramen between the external space dorsal to the cranial (Janensch, 1935-36; Salgado and Calvo, 1992; roof and the endocranial cavity. This commu¬ Salgado, 1999), which was an unambiguous nication often is referred to as the parietal synapomorphy of Dicraeosauridae (Wilson, foramen (e.g., Salgado and Calvo, 1992; 2002) but may be derived for the more inclusive Chatterjee and Zheng, 2002), presumably be¬ Flagellicaudata (Harris and Dodson, 2004; cause of an inferred homology with the parietal Harris, 2006). foramen that houses the pineal body in other Frontals: The frontals are wedge-shaped reptiles (Janensch, 1935-36; Edinger, 1955). bones in dorsal view whose posterior margin is 2010 BALANOFF ET AL.: BRAINCASE OF APATOSAURUS 7 Fig. 3. Two-dimensional HRCT slices through the coronal plane of BYU 17096. Arrows denote the frontal-parietal suture (A), frontal-frontal suture (B), parietal-supraoccipital suture (C), and orbitosphenoid- laterosphenoid suture (D). tapered due to the presence of the frontopa¬ the frontoparietal fenestra and extends to the rietal fenestra to which they contribute (along supratemporal fenestra along a slightly sinu¬ with the parietals; fig. 1C). The frontals are ous trajectory. This suture turns anteriorly relatively shorter anteroposteriorly with their and somewhat ventrally at the lateral edge of length being less than twice their transverse the braincase resulting in the dorsal surface of breadth (Wilson, 2002). The frontals contact the postorbital process being comprised en¬ the orbitosphenoid and laterosphenoid ven- tirely by the frontal (the lateral ends of this trolaterally, parietal posteriorly, postorbital suture he completely rostral to the supratem¬ posterolaterally, and each other medially. The poral fenestra unlike Suuwassea; Harris, frontal-parietal suture, which is clearly visible 2006). The frontal-parietal contact lies near in the HRCT slices (fig. 3A), begins lateral to the suture between the laterosphenoid and AMERICAN MUSEUM NOVITATES NO. 3677 Fig. 4. Two-dimensional HRCT slice through a coronal plane of the braincase of BYU 17096. Dotted line delineates a paired fossa formed within the frontals. prootic (as in most sauropods; Wilson et al., anteriorly, postorbital anterolaterally, parietal 2005) . The frontal-parietal suture is overlap¬ and squamosal posterolaterally, prootic ante- ping for much of its breadth (with the frontals roventrally, exoccipital-opisthotic posteroven- overlying the parietals) before pinching out trally, and supraoccipital posteriorly. Their posterolaterally (fig. 3A). The frontal-frontal median contact is negated by the diameter of suture is present and, as revealed in the CT the frontoparietal fenestra, whose posterior slices, distinctly interdigitating (fig. 3B). This margin is formed by the supraoccipital (see medial contact is sutured but not fully fused as below). The medial margins of the parietals do in dicraeosaurids (Salgado and Calvo, 1992; extend a short distance towards the cranial Wilson, 2002) and possibly Tornieria (Harris, midline thereby constricting (slightly) the 2006) . The frontals form the dorsal margin of frontoparietal fenestra. The parietal along the large anterior fenestra for the olfactory with the postorbital contributes to the supra¬ tracts (see Orbitosphenoid below). A pair of temporal fenestra, which is wider than long bilaterally symmetrical fossae, whose origin is (table 1) and preserved only on the left side of unclear, penetrates the lateral margin of the the skull. The diameter of the supratemporal frontals from within the supratemporal fenestra fenestra (in either direction) is distinctly larger (fig. 4). These fossae extend ventromedially than that of the foramen magnum (table 1; within the frontals before terminating at or Wilson, 2002). The distance separating the near the frontal-parietal suture lateral to the right and left supratemporal fenestrae is frontoparietal fenestra. The frontals fail to greater than the largest diameter of the contribute to the supratemporal fossa (Wilson, supratemporal fenestra (Wilson, 2002). The 2002). supratemporal fenestra faces more laterally Parietals: The parietals are smaller than than dorsally (as in Apatosaurus and Suu- the frontals. The parietals contact the frontals wassea; Harris, 2006). The parietals of BYU 2010 BALANOFF ET AL.: BRAINCASE OF APATOSAURUS 9 17096 contain low arcuate ridges on either side Braincase of the supraoccipital that mark the posterior Supraoccipital: The supraoccipital is a margin of the skull (Wilson et al., 2005). The midline ossification that roofs the posterior parietals overlap the supraoccipital and extend portion of the endocranial cavity. The supra¬ laterally to overlay the exoccipital-opisthotic. occipital contacts the parietals anterodorsally The parietal-exoccipital suture is sinuous as and laterally, and the exoccipital-opisthotic described for Apatosaurus (Berman and ventrolaterally. In dorsal view, the supraoc¬ McIntosh, 1978) and Tornieria (Remes, 2006) cipital underlies the paired parietals along its and unlike the linear suture of Suuwassea lateral margins and forms the posterior (Harris, 2006). A squamosal-supraoccipital margin of the frontoparietal fenestra contact excludes a parietal participation in the (fig. 2B). The anterodorsal margin of the dorsal margin of the posttemporal fenestra (a supraoccipital that borders the frontoparietal diplodocoid synapomorphy; Calvo and fenestra is slightly concave in posterior view Salgado, 1995; Upchurch, 1998; Remes, 2006). (fig. 1C). The anterior surface of the supraoc¬ The occipital process of the parietal is deep, cipital that forms the caudal wall of the being approximately twice the diameter of the posterior portion of the frontoparietal fenestra foramen magnum (Wilson, 2002). is concave, forming a vertical groove that Postorbitals: The left postorbital is more would have housed a dorsal extension of the completely preserved than the right (fig. IB, dural venous sinus system. C). The postorbital contacts the frontal The occiput overall is flat to slightly concave anteromedially, parietal dorsomedially, and (posteriorly) and therefore lacks the convex squamosal medially. The postorbital contrib¬ “supraoccipital wedge” described in some utes to the formation of the supratemporal sauropod braincases (fig. 2B; e.g., eusauropod fenestra through its significant contribution to from India; Wilson et al., 2005). In posterior the postorbital process where it contacts the view, the occiput is rectangular in shape and frontal along its medial surface. The distal compares closely with the high and vaulted ends of both the jugal and squamosal pro¬ occiput described for Apatosaurus (Berman and cesses are broken resulting in the postorbital McIntosh, 1978). The height of the supraoccip¬ lacking the triradiate shape present in ital in posterior view is greater than twice the Apatosaurus and other sauropods (Berman height of the foramen magnum, which appears and McIntosh, 1978). The preserved lengths of to be the plesiomorphic condition for sauro¬ these processes both indicate that they were pods (Wilson, 2002). A distinct nuchal crest broader transversely than anteroposteriorly extends along the midline of the supraoccipital (Wilson, 2002). The postorbital does possess beginning at the posterior margin of the a distinct but short posterior process (Wilson, frontoparietal fenestra and ending at or just 2002). The temporal bar is longer anteropos¬ above the dorsal margin of the foramen teriorly than transversely, and is shifted magnum. A nuchal fossa lies lateral to the ventrally exposing the supratemporal fossa in nuchal crest on either side in the posterior lateral view (Wilson, 2002). occipital plate. Squamosals: The right and left squamo- The supraoccipital forms a contact with the sals are present and contact the parietal exoccipital-opisthotic that begins laterally, medially, postorbital laterally, and exoccipi¬ just dorsal to the base of the paroccipital tal-opisthotic posteromedially. The squamosal process, and curves ventromedially to reach lies in the posterolateral corner of the skull the dorsolateral margin of the foramen mag¬ directly anterior to the paroccipital process of num. The angle of this ventromedial curvature the exocccipital-opisthotic (structure to which is steeper in BYU 17096 than in YPM 1860 the squamosal is firmly fused). The squamosal (Berman and McIntosh, 1978). The supraoc¬ contacts the lateral margin of the parietal cipital forms the dorsal margin of the circular along a relatively complex suture that includes foramen magnum (slight mediolateral com¬ both overlapping (with the squamosal over¬ pression). The external occipital fenestra lies lapping the parietal) and interdigitating re¬ dorsal and lateral to the foramen magnum and gions. is clearly visible in posterior view (fig. 2B). 10 AMERICAN MUSEUM NOVITATES NO. 3677 Fig. 5. Stereo rendering of the braincase of BYU 17096 in ventrolateral view. The squamosal and postorbital have been digitally removed from the braincase. This fenestra pierces the occipital plate at the which is rare in sauropods (Wilson et al., supraoccipital-parietal suture, where it would 2005). have transmitted the external occipital vein The ventral suture with the basioccipital (caudal middle cerebral vein; Witmer and cannot be discerned so it is unclear to what Ridgely, 2009) out of the endocranial cavity degree the exoccipital contributes to the massive and onto the external surface of the occipital occipital condyle and whether the basioccipital plate. The external path of this vein is marked is completely excluded from the ventral margin by a distinct groove that runs ventrolaterally of the foramen magnum. The exoccipitals do from the external occipital fenestra, following form a large proportion of the occipital condyle the general trajectory of the supraoccipital- in YPM 1860 and completely exclude the parietal suture (this external groove often is basioccipital from the ventral margin of the present in birds; Baumel and Witmer, 1993). foramen magnum (Berman and McIntosh, Exoccipital-Opisthotic: The exoccipital 1978). In most sauropods where the relative and opisthotic are fused completely and contribution can be discerned (e.g., Shunosau- therefore described as a single complex. The rus\ Chatterjee and Zheng, 2002), the basioc¬ exoccipital-opisthotic contacts the parietal cipital forms the majority of the occipital dorsally, supraoccipital medially, prootic and condyle. The occipital condyle of BYU 17096 squamosal anteriorly, basioccipital postero- as a whole is hemispherical in shape with a ventrally, and basisphenoid anteroventrally. dorsal surface that is concave up, differing from The exoccipital-opisthotic contributes to the Diplodocus that has a rounded dorsal margin lateral and ventral margins of the foramen (Berman and McIntosh, 1978). The peduncu¬ magnum. The suture with the overlying late occipital condyle is deflected posteroven- supraoccipital is visible and positioned near trally, projecting from the main body of the the dorsoventral midline of the foramen basicranium at an angle of approximately 80° magnum. A distinct prominence lies lateral from the horizontal plane of the skull roof. to the foramen magnum and encompasses The exoccipital-opisthotic forms a promi¬ portions of both the supraoccipital and nent paroccipital process that extends ventro¬ exoccipital-opisthotic. It is unclear whether laterally to contact the squamosal. Rather this structure represents a proatlantal facet, than extending at a distinct posterolateral