Extant crocodilians are a highly apomorphic archosaur clade that is ectothermic, yet often achieve large body sizes that can be subject to higher heat loads. Therefore, the anatomical and physiological roles that blood vessels play in crocodilian thermoregulation need further investigation to better understand how crocodilians establish and maintain cephalic temperatures and regulate neurosensory tissue temperatures during basking and normal activities. The cephalic vascular anatomy of extant crocodilians, particularly American alligator (Alligator mississippiensis) was investigated using a differential-contrast, dual-vascular injection technique and high resolution X-ray micro-computed tomography (μCT). Blood vessels were digitally isolated to create representations of vascular pathways. The specimens were then dissected to confirm CT results. Sites of thermal exchange, consisting of the oral, nasal, and orbital regions, were given special attention due to their role in evaporative cooling and cephalic thermoregulation in other diapsids. Blood vessels to and from sites of thermal exchange were studied to detect conserved vascular patterns and to assess their ability to deliver cooled blood to neurosensory tissues. Within the orbital region, both the arteries and veins demonstrated consistent branching patterns, with the supraorbital, infraorbital, and ophthalmotemporal vessels supplying and draining the orbit. The venous drainage of the orbital region showed connections to the dural sinuses via the orbital veins and cavernous sinus. The palatal region demonstrated a vast plexus that comprised both arteries and veins. The most direct route of venous drainage of the palatal plexus was through the palatomaxillary veins, essentially bypassing neurosensory tissues. Anastomotic connections with the nasal region, however, may provide an alternative route for palatal venous blood to reach neurosensory tissues. The nasal region in crocodilians is probably the most prominent site of thermal exchange, as it offers a substantial surface area and is completely surrounded by blood vessels. The venous drainage routes from the nasal region offer routes directly to the dural venous sinuses and the orbit, offering evidence of the potential to directly affect neurosensory tissue temperatures. The evolutionary history of crocodilians is complex, with large-bodied, terrestrial, and possibly endothermic taxa that may have had to deal with thermal loads that likely provided the anatomical building-blocks for such an extensive vascularization of sites of thermal exchange. A clear understanding of the physiological abilities and the role of blood vessels in the thermoregulation of crocodilians neurosensory tissues is not available but vascular anatomical patterns of crocodilian sites of thermal exchange indicate possible physiological abilities that may be more sophisticated than in other extant diapsids.

Squamates use the circulatory system to regulate body and head temperatures during both heating and cooling. The flexibility of this system, which possibly exceeds that of endotherms, offers a number of physiological mechanisms to gain or retain heat (e.g., increase peripheral blood flow and heart rate, cooling the head to prolong basking time for the body) as well as to shed heat (modulate peripheral blood flow, expose sites of thermal exchange). Squamates also have the ability to establish and maintain the same head-to-body temperature differential that birds, crocodilians, and mammals demonstrate, but without a discrete rete or other vascular physiological device. Squamates offer important anatomical and phylogenetic evidence for the inference of the blood vessels of dinosaurs and other extinct archosaurs in that they shed light on the basal diapsid condition. Given this basal positioning, squamates likewise inform and constrain the range of physiological thermoregulatory mechanisms that may have been found in Dinosauria. Unfortunately, the literature on squamate vascular anatomy is limited. Cephalic vascular anatomy of green iguanas (Iguana iguana) was investigated using a differential-contrast, dual-vascular injection (DCDVI) technique and high-resolution X-ray microcomputed tomography (μCT). Blood vessels were digitally segmented to create a surface representation of vascular pathways. Known sites of thermal exchange, consisting of the oral, nasal, and orbital regions, were given special attention due to their role in brain and cephalic thermoregulation. Blood vessels to and from sites of thermal exchange were investigated to detect conserved vascular patterns and to assess their ability to deliver cooled blood to the dural venous sinuses. Arteries within sites of thermal exchange were found to deliver blood directly and through collateral pathways. The venous drainage was found to have multiple pathways that could influence neurosensory tissue temperature, as well as pathways that would bypass neurosensory tissues. The orbital region houses a large venous sinus that receives cooled blood from the nasal region. Blood vessels from the nasal region and orbital sinus show anastomotic connections to the dural sinus system, allowing for the direct modulation of brain temperatures. The generality of the vascular patterns discovered in iguanas were assessed by firsthand comparison with other squamates taxa (e.g., via dissection and osteological study) as well as the literature. Similar to extant archosaurs, iguanas and other squamates have highly vascularized sites of thermal exchange that likely support physiological thermoregulation that “fine tunes” temperatures attained through behavioral thermoregulation.

Body size has thermal repercussions that impact physiology. Large‐bodied dinosaurs potentially retained heat to the point of reaching dangerous levels, whereas small dinosaurs shed heat relatively easily. Elevated body temperatures are known to have an adverse influence on neurosensory tissues and require physiological mechanisms for selective brain and eye temperature regulation. Vascular osteological correlates in fossil dinosaur skulls from multiple clades representing different body‐size classes were identified and compared. Neurovascular canals were identified that differentiate thermoregulatory strategies involving three sites of evaporative cooling that are known in extant diapsids to function in selective brain temperature regulation. Small dinosaurs showed similarly sized canals, reflecting a plesiomorphic balanced pattern of blood supply and a distributed thermoregulatory strategy with little evidence of enhancement of any sites of thermal exchange. Large dinosaurs, however, showed a more unbalanced vascular pattern whereby certain sites of thermal exchange were emphasized for enhanced blood flow, reflecting a more focused thermal strategy. A quantitative, statistical analysis of canal cross‐sectional area was conducted to test these anatomical results, confirming that large‐bodied, and often large‐headed, species showed focused thermal strategies with enhanced collateral blood flow to certain sites of heat exchange. Large theropods showed evidence for a plesiomorphic balanced blood flow pattern, yet evidence for vascularization of the large antorbital paranasal air sinus indicates theropods may have had a fourth site of heat exchange as part of a novel focused thermoregulatory strategy. Evidence presented here for differing thermoregulatory strategies based on size and phylogeny helps refine our knowledge of dinosaur physiology. Anat Rec, 303:1075–1103, 2020. © 2019 American Association for Anatomy

The attachments of jaw muscles are typically implicated in the evolution and shape of the dorsotemporal fenestra on the skull roof of amniotes. However, the dorsotemporal fenestrae of many archosaurian reptiles possess smooth excavations rostral and dorsal to the dorsotemporal fossa which closely neighbors the dorsotemporal fenestra and jaw muscle attachments. Previous research has typically identified this region, here termed the frontoparietal fossa, to also have attachment surfaces for jaw‐closing muscles. However, numerous observations of extant and extinct archosaurs described here suggest that other tissues are instead responsible for the size and shape of the frontoparietal fossa. This study reviewed the anatomical evidence that support soft‐tissue hypotheses of the frontoparietal fossa and its phylogenetic distribution among sauropsids. Soft‐tissue hypotheses (i.e., muscle, pneumatic sinus, vascular tissues) were analyzed using anatomical, imaging and in vivo thermography techniques within a phylogenetic framework using extant and extinct taxa to determine the inferential power underlying the reconstruction of the soft tissues in the skull roofs of dinosaurs, pseudosuchians, and other reptiles. Relevant anatomical features argue for rejection of the default hypothesis—that the fossa was muscular—due to a complete lack of osteological correlates reflective of muscle attachment. The most‐supported inference of soft tissues is that the frontoparietal fossa contained a large vascular structure and adipose tissue. Despite the large sizes and diverse morphologies of these fossae found among dinosaur taxa, these data suggest that non‐avian dinosaurs had the anatomical foundation to support physiologically significant vascular devices and/or vascular integumentary structures on their skull roofs. Anat Rec, 303:1060–1074, 2020. © 2019 Wiley Periodicals, Inc.

The restoration of dinosaur cephalic blood vessels is critical to understanding physiological thermoregulatory strategies in dinosaurs. Cephalic blood vessels of extant diapsids are known to support physiological thermoregulatory capabilities that modulate head and neurosensory tissue temperatures. Given their close phylogenetic relationship to extant diapsids, dinosaurs are hypothesized to have had similar vascular arrangements and physiological abilities. To test this hypothesis, the cephalic vascular anatomy of extant diapsids (turtles, squamates, crocodilians, and birds) was investigated using CT‐scanning, vascular injection, and gross dissection with special attention given to blood vessels within known sites of thermal exchange (oral, nasal, and orbital regions). Vascular osteological evidence in skull bones of both extant and extinct specimens was collected to test hypotheses of vascular anatomy within the heads of dinosaurs. CT data were segmented in Avizo and vascular restorations were made using Maya. The large blood vessels that supply and drain diapsid heads displayed a conserved branching pattern, as the common carotid artery reliably bifurcates into internal and external carotid arteries. Further evidence for the subsequent branching patterns of these blood vessels adds support for a highly conserved diapsid vascular pattern. An important detail for identifying not only the blood vessels forming osteological correlates, but also identifying the blood vessels that passed between soft‐tissues, is the anastomotic connections that each blood vessel shared. For example, within the orbit, evidence for anastomoses between the supraorbital, ophthalmotemporal and branches of the cerebral carotid arteries was found in all three extant clades sampled. This evidence indicates the location of each participating artery and subsequently highlights the course of all three blood vessels back to their parent vessel. Within the narial region, near the maxilla‐premaxilla suture, evidence for anastomotic connections between the maxillary and nasal vessels was found. This anastomosis often included the palatal vessels, indicated by a canal that opened onto the palate. The connection between these vessels would have allowed blood to pass from the palate to the nasal region, or vice‐versa, serving as a potential collateral blood flow pathway to both of these regions. Additionally, some of the blood vessels to the nasal region are branches of the cerebral carotid arteries, which in large dinosaurs do not appear to be emphasized and seem inadequately sized to supply a large nasal region. This indicates that collateral blood flow was important for supplying emphasized sites of thermal exchange in large dinosaurs. When several dinosaur taxa were compared, different foramina sizes highlighted not only the potential diameter of blood vessels supplying sites of thermal exchange, but also which blood vessels supplied a majority of the blood to physiologically relevant regions of the head. Enabled by an understanding of the vascular anatomy of dinosaurs, we can begin to investigate the physiology of sites of thermal exchange and what important role they served in dinosaur thermoregulatory strategies.Support or Funding InformationUnited States National Science Foundation (IOB‐0517257, IOS‐1050154), Ohio University Heritage College of Osteopathic Medicine, Ohio University Student Enhancement Award, Jurassic Foundation Grant‐in‐aid of Research, Ohio Center for Ecological and Evolutionary Studies Research Fellowship, Ohio University Graduate Student Senate Grant–in‐aid of Research, Sigma Xi Grant‐in‐aid of Research, and the University of California Welles Fund.