Tyrannosaurus rex Osborn 1905
Creators: name: Snively, Eric
name: Russell, Anthony P.
Publisher: name: Zenodo
Year: 2003
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Reptilia
Dinosauria
Tyrannosauridae
Tyrannosaurus
Tyrannosaurus rex

description: This article develops a functional model for the arctometatarsus that incorporates inferences of soft tissues. Our format follows the logical progression involved in developing and testing a complex hypothesis of locomotion: 1) We first introduce aspects of bone and connective organ function in large terrestrial vertebrates that suggest hypotheses of arctometatarsus morphology and action. 2) Our investigations and results test these proposals and lead inductively to a model of overall arctometatarsus function. 3) Because the model is emergent from the results, we present it in a separate section. 4) The subsequent discussion tests the model against modern analogs and addresses implications of the proposed kinematics for tyrannosaurids. The model therefore acts as a prism that focuses multiple lines of evidence into a coherent functional picture and a fulcrum over which morphological detail facilitates discussion of behavior. Our construction and application of the model exemplify the integrated approach necessary for reconstructing locomotion of extinct vertebrates. Arctometatarsus as an ElasticallyDamped System As with foot structures in modern animals, the arctometatarsus’ role in tyrannosaurid locomotion hinged on the specific morphology of its bones and connective tissues. In vertebrates, tendons that join bone to muscle, and ligaments that connect bone to bone, transmit and dissipate locomotor forces acting on the skeleton (Hildebrand, 1988). Tendons and ligaments are variably elastic, depending on their relative proportions of collagen and elastin proteins (Alexander, 1988) and the magnitude and period of imposed loadings (Pollock, 1991). The bones of the arctometatarsus and its unmineralized tissues would have been elastic to some degree, but understanding its precise function depends, in part, on consideration of locomotor elasticity in modern vertebrates. A number of studies have explicated the locomotor role of elastic ligaments and tendons and their interactions with associated bones. Elastic fore- and hindfoot connective elements store, return, and distribute footfall energies and forces. Ligaments of the feet of humans (Kerr et al., 1987; Alexander, 1988; Deane and Davies, 1995) and the wrists of horses (Rubeli, 1925) are noteworthy examples. Ligaments absorb shock under specific physical conditions. Paradoxically, they display greater strength and resiliency when subject to high magnitude, sudden loadings, such as those incurred during rapid locomotion (Frank and Shrive, 1994). In animals of large body size, the extensibility of connective elements increases because their cross sectional area is lower relative to mass than ligaments and tendons of smaller animals (Pollock, 1991). The ligaments of large vertebrates store and return relatively more elastic strain energy, which increases locomotor efficiency and decreases strain energy transmitted to bones (Pollock, 1991). These conditions probably existed in adult tyrannosaurids, which ranged from two (Paul, 1988) to an upper estimate of eight tons (cross scaling of measurements from fragmentary metatarsals: University of California Museum of Paleontology, locality number V91181). These considerations suggest that elastic mechanisms may have operated efficiently within the tyrannosaurid foot. Two contingencies are critical for assessing possible elastic functions: the type of connective tissues associated with the arctometatarsus and the freedom of movement between metatarsals. These factors lead to hypotheses of anatomy and movement necessary for erecting a comprehensive model of tyrannosaurid arctometatarsus function. Prerequisites for Modeling Arctometatarsus Function: Reconstructing Soft Tissues and Intermetatarsal Displacement Soft tissue reconstruction of extinct vertebrates entails comparison with extant relatives, ideally by bracketing the extinct taxon between modern, derived representatives of its clade and a more archaic living sister group (Bryant and Russell, 1992; Witmer, 1995). Although there are no extant arctometatarsalian theropods, unpreserved tissues are still inferable through broader phylogenetic comparison, mechanical considerations, and universal correlates of soft parts that are present on mineralized structures (Bryant and Seymour, 1990; Bryant and Russell, 1992). Soft tissues leave consistent marks on bone, termed osteological correlates (Witmer, 1995), that are evident in both extant and fossil specimens. Ligament or tendon attachments display two primary correlates: rugosity, and rough or smooth faceted areas. Rugosity marks the location of Sharpey’s fibers, mineralized collagen fibers within the bone that are continuous with fibers of the attaching connective element (Woo et al., 1987). Ligaments and tendons also attach through a gradient of fibrocartilage, mineralized fibrocartilage, and bone. These so-called direct insertions occur on bone surfaces that are smooth and slightly concave (Doglo-Saburoff, 1929). Sutured or closely conforming bones invariably indicate ligament attachments, and more widely spaced adjacent facets may indicate tendon attachments (Gray and Goss, 1959). Using these criteria we identified osteological correlates along intermetatarsal articular surfaces of large theropods. Ligaments would indicate passive elasticity and tendons would signify controlled function. Our study tested the following hypotheses: <b>H1:</b> Connective tissue scars on adjacent tyrannosaurid metatarsals indicate tendons. <b>H2:</b> Scar configuration was identical in tyrannosaurids and in the nonarctometatarsalian theropod, <i>Allosaurus fragilis</i>. Freedom of movement between tyrannosaurid or <i>Allosaurus fragilis</i> metatarsals dictated the function of their associated ligaments or muscles. Therefore, this study sought to test hypotheses of possible intermetatarsal displacement. Preliminary observations of tyrannosaurid metatarsals, and the work of Wilson and Currie (1985) and Holtz (1995), suggested this hypothesized pattern of movement: <b>H3:</b> In the tyrannosaurid metatarsus, the distal end of MT III was free to move anteriorly to a small degree about a pivot point at the proximal end. The proximal articulation between metatarsals, and their associated soft tissues, would constrain this potential displacement of MT III. Detailed consideration of both osteological and soft tissue anatomy was therefore necessary to test the hypotheses and come to a more complete understanding of tyrannosauruid arctometatarsus function. <b>Institutional abbreviations.</b> MOR: Museum of the Rockies, Bozeman, Montana. IVPP: Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China. NMC: National Museum of Canada, Ottawa. PJC: Philip J. Currie, Royal Tyrrell Museum of Palaeontology, Drumheller, Alberta, Canada. TMP: Royal Tyrrell Museum of Palaeontology, Drumheller, Alberta. UCMP: University of California Museum of Paleontology, Berkeley, California. ROM: Royal Ontario Museum, Toronto, Ontario. MATERIALS AND METHODS For comparative purposes, specimens of large and small arctometatarsalian forms were examined at UCMP, MOR, and TMP. Metatarsal specimens of <i>Allosaurus fragilis</i> (MOR 693), and others at MOR and TMP, provided control representatives of the primitive condition for theropods. The specimens (Table 1) were sufficiently complete and well preserved for evaluation of osteological correlate position and/or resolution of possible intermetatarsal movement. Assessment of metatarsus dynamics in tyrannosaurids entailed three related lines of inquiry: 1) We identified and measured osteological correlates of soft tissues in tyrannosaurids and <i>Allosaurus fragilis</i>. The proximity and complexity of joint surfaces tested whether the correlates indicated tendons or ligaments. 2) To ascertain the probable range of motion between elements in physical specimens, we manipulated casts of <i>Tyrannosaurus rex</i> metatarsals. 3) To evaluate intermetatarsal freedom of movement in other tyrannosaurids, we examined com- puted tomographic (CT) images of <i>Albertosaurus sarcophagus</i> and <i>Gorgosaurus libratus</i> metatarsals. Assessment of Osteological Correlates We ascertained the distribution and extent of osteological correlates on theropod metatarsals by identifying probable scars and measuring their areas. Likely correlates of soft tissues were identified on specimens in a satisfactory state of preservation, using the criteria of rugosity and delineated faceting outlined above. Surfaces had to be continuous with cortical bone that had not been taphonomically eroded, to avoid the potential of infilled spongy bone being mistaken for rugosity. Problematic degeneration was not present on the metatarsals chosen for area measurement. We measured the area of the correlates only when their boundaries could be repeatably determined, but because soft tissues are not preserved, our techniques are subject to some inaccuracy. Our results, therefore, reflect the position and relative area of correlates more than their absolute extent. Surface areas of osteological correlates were measured on specimens of <i>Albertosaurus sarcophagus</i> (MOR 657), <i>Allosaurus fragilis</i> (MOR 693), <i>Daspletosaurus torosus</i> (MOR 590), and <i>Tyrannosaurus rex</i> (MOR 555). The bones were wrapped in plastic cling film and attachment surface areas traced with a water-based marking pen. This technique facilitates area measurement of complexly contoured surfaces (Snively, 2000). The cling wrap was removed from the bone, pulled gently taut, and smoothed with a ruler. The markings were then retraced onto white paper and digitized. From these scans we determined the areas of the representations in cm 2 using NIH Object-Image for Macintosh. The average of apparent attachment areas on adjacent bones was used to approximate the cross sectional area of intervening soft tissues. A disarticulated MT IV was not present in MOR 555. To estimate the areas on that bone, first the smaller ratio was found between MT IV and MT III in the other tyrannosaurids. This ratio was then multiplied by the corresponding MT III area in MOR 555. Manipulation of <i>Tyrannosaurus rex</i> Casts Casts of <i>Tyrannosaurus rex</i> metatarsals from the left foot of LACM 7244/23844 (TMP casts: 82.50.7) were positioned in proper articulation and wrapped with elastic bands. Rubber and polyester fiber bungy cords of low stiffness (0.75 meters long when untensed) were stretched and wound twice around the casts at their proximal and distal ends, tightly enough for the ends to be secured together by their plastic hooks (Fig. 2a). The casts were positioned and manipulated in several ways in order to investigate proximal and distal freedom of intermetatarsal movement. <b>Proximal movement.</b> We placed the distal part of the metatarsus on a laboratory bench, alternately on its anterior and posterior surfaces, while we supported and manipulated the proximal end to assess possible intermetatarsal movement in this region. <b>Distal movement with the metatarsus in varying positions.</b> We placed the proximal end of the metatarsus on the bench, with the posterior surface down, and supported the specimen by the third metatarsal. Rotating the metatarsus about its fixed proximal end revealed the passive displacement of MT II and MT IV relative to MT III, with the metatarsus in various positions, ranging from 0 to –90° from the horizontal. (Some of these positions are shown in the silhouettes in Fig. 5.) <b>Intermetatarsal displacement under simulated loading.</b> The entire metatarsus was set on the bench. Taking care not to apply medial or lateral pressure, we pushed down on the dorsal surfaces of MT II and MT IV about 70% of their lengths from their proximal ends. We then lifted the distalmost portion of MT III. This showed the behavior of the outer metatarsals when a greater dorsally directed torque was applied to the distal part of MT III than to the distal ends of the other metatarsals. CT Scanning of Tyrannosaurid Metatarsals The methods described above apply to overall intermetatarsal movements. The topographical and likely functional complexity of the arctometatarsus compelled analysis of movement evident in cross sections at multiple transverse and longitudinal transects. As in clinical practice, the most common nondestructive technique for macroscopic paleontological sectioning is CT scanning. In order to maximize the information from CT scanning and postprocessing visualization techniques, particular care was taken in specimen choice and preparation. TMP 94.12.602, a partial skeleton of <i>Gorgosaurus libratus</i> from the Dinosaur Park Formation (Late Campanian) of Dinosaur Provincial Park, Alberta, has a complete right metatarsus that has not been disarticulated taphonomically or through preparation. This specimen is undistorted and is intermediate in length and robustness between metatarsi of subadult <i>Albertosaurus sarcophagus</i> and adult <i>Tyrannosaurus rex</i>. For these reasons TMP 94.12.602 was deemed a suitable compromise for functional extrapolation to other tyrannosaurids. The specimen was imaged at Children’s Hospital and Health Center, San Diego. Prior to scanning the specimen was encased in plasticine to a depth of 2.5–4 cm to reduce the density gradient between the bone and the surrounding medium, and thus diffraction and scattering artifacts. Once prepared, TMP 94.12.602 was CT scanned at 140 kVp and 170 mA, technique settings that produce good readings from dense bone. The cross sectional data were reconstructed in three dimensions and these reconstructions were further sectioned, viewed, and printed in various orientations for study. Additional CT scans of an <i>Albertosaurus sarcophagus</i> metatarsus (TMP 81.10.1) were performed at the Radiology Department of Foothills Hospital in Calgary, Alberta. A metal frame on the specimen caused diffraction artifacts, which we alleviated by adjusting contrast on the output images. Following this adjustment the shape of intermetatarsal articulation surfaces could be evaluated and possible relative movement determined in a given plane of section. RESULTS Osteological Correlate Reconstruction The following intermetatarsal osteological correlates for soft tissues were identified. The surfaces of all but one scar (in <i>Allosaurus</i>) conform closely to the contours of the facing scar on the adjacent metatarsal. Rugosity indicating Sharpey’s fibers occurs at proximal shaft-to-shaft articular surfaces in specimens of tyrannosaurids (Fig. 4 a–c) and <i>Allosaurus</i> (Fig. 4d). Smooth articular facets extend the MT III-MT II articulation distally in <i>Allosaurus</i> (Fig. 4d). Indications of Sharpey’s fibers are most striking along the distal articular surfaces between the shafts of MT II and MT III in large tyrannosaurids (Fig. 4 a– c), but are not present at these locations in <i>Allosaurus</i> (Fig. 4d). A faceted distal MT III-MT IV articulation occurs in tyrannosaurids (Fig. 4 a–c), but is entirely absent in <i>Allosaurus</i>, in which MT IV shows pronounced lateral angulation (Fig. 4d). Proximal scars are subtriangular in all assessed theropods (Fig. 4), but in <i>Allosaurus</i> are long proximodistally relative to the length of the metatarsus. In all three tyrannosaurids distal articulations are long and taper proximally. The average areas of adjacent distal scars are quite extensive in tyrannosaurids (Table 2). The average distal scar area exceeds the average proximal area by 1.5728 in <i>Daspletosaurus</i> (MOR 590), 1.4029 in <i>Albertosaurus</i> (MOR 657), and by 1.4666 in <i>Tyrannosaurus</i> (MOR 555; Table 2). The intimate conformity of adjacent scars falsifies hypothesis H1, that tendons and muscles rather than ligaments were present between theropod metatarsals. Large distal osteological correlates on tyrannosaurid metatarsals, and their absence in <i>Allosaurus fragilis</i>, falsify the hypothesis (H2) that there were no marked differences in correlate morphology between the taxa. Intermetatarsal Movement 1. Physical manipulation of <i>Tyrannosaurus rex</i> casts. <i>Proximal Movement.</i> Proximally, displacement is greatly constrained by the hooked cross section of MT III and its articulation with anterolateral and posteromedial projections of MT II and MT IV, respectively (Fig. 2b). <i>Distal Movement.</i> The distal portion of the third metatarsal is free to move anteriorly, corroborating hypothesis H3. When the anterior face of the metatarsus is parallel with the ground, only the distal elastic bands prevent this portion of MT III from pivoting towards the floor, with its center of rotation at the proximal clasped articulation. When the posterior surface of the metatarsus faces the ground and the distal and proximal parts of MT III are fixed in position, the distal portions of MT II and MT IV slide ventrally and towards the centerline of MT III. MT II slides in a straight line along its articular surface with MT III. This contrasts with MT IV, which slides in more of an arc along its corresponding surface (Fig 2b). <b>Intermetatarsal displacement under simulated loading.</b> When the posterior surface of the metatarsus again faces down, as just described, but with MT II and MT IV fixed proximally and distally, the same medial sliding motion occurs when the distal part of MT III is forced upwards and the bands stretch. As force is released from MT III, the bands recoil and the metatarsals return to their original articulation positions. <b>2. Freedom of movement inferred from <i>Gorgosaurus libratus</i> and <i>Albertosaurus sarcophagus</i> CT scans.</b> These results show no gross variation in potential movement among the three metatarsi. The CT scanned specimens show the same proximal interlocking morphology as described for <i>Tyrannosaurus rex</i>. In <i>Gorgosaurus libratus</i> (TMP 94.12.602), cross sections along the metatarsus reveal that the distal articulation between MT II and MT III always slants ventromedially at the same angle (Fig. 3a). This indicates that displacement along this articulation will be in one plane, a motion identical to that possible in the physical model (see results for the cast manipulations above). By contrast, the MT IV-MT III articulations in the cross sections are not always in a straight line and the overall angle of the articulation varies with cross section. This corroborates the inference that motion along this articulation would transcribe an arc in the metatarsi of all three tyrannosaurids (Fig. 3b). Kinematic Model of the Tyrannosaurid Arctometatarsus: The Tensile Keystone Hypothesis The above results indicate that ligaments were the connective elements between adjacent tyranno- saurid metatarsals and reveal degrees of freedom and constraint for tyrannosaurid intermetatarsal movement through the ground contact (stance) phase of the step cycle (Figs. 5– 6). These considerations suggest the following pattern of intermetatarsal kinematics when the foot was in contact with the substrate. <i>TABLE 2. Surface areas of intermetatarsal osteological correlates in large theropods</i>. *No distal correlates. Osteological correlate areas in Allosaurus fragilis (MOR 693), Albertosaurus sarcophagus (MOR 657), Daspletosaurus torosus (MOR 590), and Tyrannosaurus rex (MOR 555). Areas are in cm2. Areas of proximal correlates are designated as “Prox.,” and distal correlates as “Distal.” The last row shows the ratios of distal to proximal areas
description: Published as part of <i>Snively, Eric &amp; Anthony P. Russell, 2003, Kinematic Model of Tyrannosaurid (Dinosauria: Theropoda) Arctometatarsus Function, pp. 215-227 in Journal of Morphology 255</i> on pages 215-226, DOI: 10.1002/jmor.10059, http://zenodo.org/record/3736328
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