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Reconstructed neck muscles of large theropod dinosaurs suggest influences on feeding style that paralleled variation in skull mechanics. In all examined theropods, the head dorsiflexor m. transversospinalis capitis probably filled in the posterior dorsal concavity of the neck, for a more crocodilian- than avian-like profile in this region. The tyrannosaurine tyrannosaurids Daspletosaurus and Tyrannosaurus had relatively larger moment arms for lateroflexion by m. longissimus capitis superficialis and m. complexus than albertosaurine tyrannosaurids, and longer dorsiflexive moment arms for m. complexus. Areas of dorsiflexor origination are significantly larger relative to neck length in adult Tyrannosaurus rex than in other tyrannosaurids, suggesting relatively large muscle cross-sections and forces. Tyrannosaurids were not particularly specialized for neck ventroflexion. In contrast, the hypothesis that Allosaurus co-opted m. longissimus capitis superficialis for ventroflexion is strongly corroborated. Ceratosaurus had robust insertions for the ventroflexors m. longissimus capitis profundus and m. rectus capitis ventralis. Neck muscle morphology is consistent with puncture-and-pull and powerful shake feeding in tyrannosaurids, relatively rapid strikes in Allosaurus and Ceratosaurus, and ventroflexive augmentation of weaker jaw muscle forces in the nontyrannosaurids. Anat Rec, 290:934–957, 2007. © 2007 Wiley-Liss, Inc.
Theropod dinosaurs differed substantially in their skull morphology and strengths (Molnar, 1973; Madsen, 1976; Currie and Carpenter, 2000; Madsen and Welles, 2000; Brochu, 2003; Holtz, 2004; Rayfield, 2005a, b; Therrien et al., 2005; Snively et al., 2006). For example, compared with the condition in other large theropods, the tyrannosaurid rostrum is broad and U-shaped (Holtz, 2004) in both frontal and transverse sections, and the posterior portion of the skull is reinforced by hypertrophied skeletal elements that encroach on the orbit and infratemporal fenestra (Henderson, 2003; Holtz, 2004). Fused nasals and the overall breadth of the skull enhanced the strength of the tyrannosaurid cranium over that of other theropods of similar cranial length (Hurum and Sabath, 2003; Rayfield, 2004, 2005a; Snively et al., 2006).
In addition to influences on cranial strength, proportional differences between theropod crania suggest functional variation of craniocervical muscles coursing from the vertebral column to the occiput. Paul (1988) noted that the nuchal crest is transversely expanded in Allosaurus, indicating the insertion of large neck muscles onto the parietals. Bakker (2000) contrasted ventral deflection of the paroccipital processes relative to the occipital condyle in Allosaurus fragilis with their horizontal orientation in Ceratosaurus and most other theropods. This unusual orientation of lever arms was suggestive that Allosaurus co-opted certain neck muscles to enhance the downward strike with the teeth of the upper jaw (Bakker, 2000).
Tyrannosaurids also display derived morphologies that have been associated with neck muscle function. As in Allosaurus, the tyrannosaurid nuchal crest of the parietals is tall and broad (Paul, 1988; Holtz, 2004), which indicates high leverage for large cranial dorsiflexors. Bakker et al. (1986) described differences in basituberal position and scar morphology in tyrannosaurids. Rugose scarring of the basioccipital tuberosities indicated large ventroflexors in Daspletosaurus and Gorgosaurus, whereas Tyrannosaurus (possibly including the described Nanotyrannus specimen; Bakker et al., 1986; Carr, 1999) had more anteriorly positioned and widely spaced basitubera, indicating different lever mechanics from those of other tyrannosaurids. Tyrannosaurid paroccipital processes are often laterally expansive, suggesting relatively greater leverage for lateral flexion of the head than is the case for most other theropods.
Much of this variation is suggestive of varying mechanical contributions to head movement and approaches to prey capture, apprehension, dismemberment, and deglutition. However, morphological attributes of neck muscles associated with these activities have yet to be described in detail or quantified, and their implications assessed with reference to other aspects of head and neck morphology. Herein, we compare the craniocervical and intrinsic cervical muscle attachments in large tyrannosaurids, similarly sized carnosaurs, and the large neoceratosaurian Ceratosaurus (Fig. 1; abelisaurids and spinosaurs have unusual neck osteology, and will be the subject of future studies), and use these data in an assessment of feeding mechanics.
A multivariate study (Snively, 2006) assesses proportions and variation of craniocervical moment arms in large theropods. However, that analysis does not address the relative sizes and consequent cross-sectional areas and force production of individual muscles. Three muscles, the cranial dorsiflexors m. transversospinalis capitis and m. splenius capitis, and the neck dorsiflexor m. transversospinalis cervicis, originate from the neural arches and spines of extant archosaurs. Because the cross-sectional area of homologous muscles is likely to be proportional to the size origins from morphologically homologous points, neural spine and arch height in lateral view can serve as a proxy for cross-sectional areas of these dorsiflexors.
We parsimoniously infer that for homologous and morphologically similar muscle origins, muscle cross-sectional areas in different theropods will be proportional to the size and rugosity of their origin scars (Cleuren and De Vree, 2000; Carpenter and Smith, 2001). This correlation is universally observed and inferred for human muscles, both through analysis of individual and sexual variation (Schwartz, 1995) and interspecifically (Trinkaus et al., 1991). Proximate examples occur for craniocervical muscles among extant theropods. Zusi (1962) indicates that the linear size and area of vertebral muscle attachments is directly correlated with the size of neck muscles in lariform birds. The black skimmer (Rynchops nigra) subjects its neck to high and rapid loadings as it sculls with its lower beak, and strikes and lifts prey out of the water (Bock, 1959). The skimmer has larger neural spines, more robust muscle attachments, and concomitantly larger neck muscles than gulls or terns (Fig. 2; Zusi, 1962). It is, therefore, reasonable to infer that in tyrannosaurids, the size of muscles associated with the neural spines and arches increased in bulk, both relatively and absolutely, in association with increasing size and rugosity of respective origins.
Figure 2. Correlation of vertebral morphology with muscle size in lariform birds. Anatomy of both birds is shown in right lateral view, and scaled to identical neck and collective vertebral lengths. A,B: The black skimmer Rynchops nigra (A) has larger muscle attachments on its anterior cervical vertebrae than the royal tern Thalasseus maximus (B), and larger muscles with greater cross-sectional area. This is evident for m. complexus, rendered here in black. (M. complexus is not dorsally displaced by the neural spines, and its greater size depicted here in the skimmer reflects larger origins and is not an artifact of taller neural spines.) Similar correlations are used to infer relative muscle size in similarly restricted clades of extinct theropods, such as tyrannosaurids. Modified from Zusi (1962).
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Calculated differences in muscle cross-sectional areas are unlikely to be 100% accurate, because more variables than origin area influence muscle cross-sectional size (Jasinoski et al., 2006). However, as a first approximation we can estimate relative areas of muscle cross-sections based on differences in the height of the neural complex (neural arch plus spine). By scaling theropod necks to a unit length and measuring the relative height of the neural arches and spines, we test the following hypothesis with simple statistics: 1) Ha: Neural arch and spine height is relatively greater in larger tyrannosaurids than in smaller ones. H0: There are no significant differences in relative cervical neural arch + spine height in tyrannosaurids across their examined size range.
Allosaurus fragilis is included in these comparisons, although its phylogenetic remoteness from the tyrannosaurids demands cautious statistical interpretations. Descriptive results suggest other hypotheses testable by morphometric analysis. We apply these results and hypotheses to a discussion of the capabilities of theropod neck muscles for dorsiflexion, lateroflexion, ventroflexion, and stabilization during feeding activities.
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Natalie Kuca drafted the muscle reconstructions in Figure 8, and Brian Cooley sculpted the T. rex cranium in Figure 6. This research was supported by Alberta Ingenuity studentships and grants, Jurassic Foundation grants, and Royal Tyrrell Museum Cooperating Society funds to ES, NSERC Discovery grants to APR, and field assessments through University of Calgary Research Services. Sarah Hollighan, Katrin Hammer, Jessica Malcom, Natalie Kuca, Magdelene Leung, Warren Fitch, Sandra Jasinoski, Jim Stemler, and Tanya Samman provided technical support. Ken Stadtman, Dan Chure, Cliff Miles, Margaret Feuerstack, Kieren Shepard, Kevin Seymour, Scott Sampson, Bucky Gates, Dallas Evans, William Ripley, William Simpson, Chris Collins, Carl Mehling, Jim Gardner, Michael Henderson, Scott Williams, and their respective museum staffs provided access to specimens. Suggestions of three anonymous reviewers improved conciseness and clarity of descriptions, statistics, and figures.