Cartilaginous epiphyses in extant archosaurs and their implications for reconstructing limb function in dinosaurs

Abstract

Extinct archosaurs, including many non-avian dinosaurs, exhibit relatively simply shaped condylar regions in their appendicular bones, suggesting potentially large amounts of unpreserved epiphyseal (articular) cartilage. This "lost anatomy" is often underappreciated such that the ends of bones are typically considered to be the joint surfaces, potentially having a major impact on functional interpretation. Extant alligators and birds were used to establish an objective basis for inferences about cartilaginous articular structures in such extinct archosaur clades as non-avian dinosaurs. Limb elements of alligators, ostriches, and other birds were dissected, disarticulated, and defleshed. Lengths and condylar shapes of elements with intact epiphyses were measured. Limbs were subsequently completely skeletonized and the measurements repeated. Removal of cartilaginous condylar regions resulted in statistically significant changes in element length and condylar breadth. Moreover, there was marked loss of those cartilaginous structures responsible for joint architecture and congruence. Compared to alligators, birds showed less dramatic, but still significant changes. Condylar morphologies of dinosaur limb bones suggest that most non-coelurosaurian clades possessed large cartilaginous epiphyses that relied on the maintenance of vascular channels that are otherwise eliminated early in ontogeny in smaller-bodied tetrapods. A sensitivity analysis using cartilage correction factors (CCFs) obtained from extant taxa indicates that whereas the presence of cartilaginous epiphyses only moderately increases estimates of dinosaur height and speed, it has important implications for our ability to infer joint morphology, posture, and the complicated functional movements in the limbs of many extinct archosaurs. Evidence suggests that the sizes of sauropod epiphyseal cartilages surpassed those of alligators, which account for at least 10% of hindlimb length. These data suggest that large cartilaginous epiphyses were widely distributed among non-avian archosaurs and must be considered when making inferences about locomotor functional morphology in fossil taxa.

Figure 1. Different extant tetrapod clades retain variable amounts of epiphyseal cartilage.

A, Plesiomorphic tetrapod condition, also characteristic of turtles, crocodylians, birds, and likely non-avian dinosaurs. B, Lepidosaurian and therian condition. Modified from Haines .

Figure 2. Phylogenetic framework of extant and extinct archosaur taxa examined in this study including characteristic epiphyseal morphology.

Phylogenetic relationships based on Brochu . †, extinct taxa.

Figure 3. Measurements conducted for quantitative analyses.

A, measurements indicated on left femur of Alligator mississippiensis (American alligator) in medial view: CC, craniocaudal; GL, greatest length; ML, mediolateral. B, GL measurement for avian specimens indicated on left femur of Struthio camelus (ostrich) in cranial view. GL in birds equals the length from the distal condyles to trochanteric shelf (a) plus the length from the same point on the trochanteric shelf to the medial end of the femoral head (b). C, Segmental measurements and joint angles used from non-avian dinosaur speed estimates (adapted from Gatesy et al. [55]).

Figure 4. Changes in epiphyses of Alligator mississippiensis upon skeletonization.

Left femur (OUVC 9407) before (left) and after (right) skeletonization. A and B: proximal end, cranial view. C, D: distal end, caudal view. Abbreviations: ac, articular cartilage; cc, calcified cartilage; lig, scar from ligaments and synovial capsule; lfc, lateral femoral condyle; met, metaphysis; mfc, medial femoral condyle. Scale bar increments equal 0.5 cm.

Figure 5. Changes in epiphyses of Alligator mississippiensis upon skeletonization.

Left distal humerus and proximal ulna (OUVC 9407) before (left) and after (right) skeletonization. A and B: humerus, distal end, cranial view. C, D: ulna, proximal end, cranial view. Abbreviations: icp, intercotylar process; lhc, lateral humeral condyle; mhc, medial humeral condyle; op, olecranon process. Scale bar increments equal 0.5 cm.

Figure 6. Changes in epiphyses of Struthio camelus.

Adult (A–D; OUVC 9438) and subadult (E–H; OUVC 9439) right femora before (left) and after (right) skeletonization. A, B: adult proximal end, cranial view. C, D: adult distal end, caudal view. E, F: subadult proximal end, cranial view. G, H: subadult distal end, caudal view. Abbreviations: cut, cut portion of cartilaginous epiphysis; fov, fovea; icb, intercondylar bridge; lfc, lateral femoral condyle; mfc, medial femoral condyle; tr, femoral trochanter. Scale bar increments equal 0.5 cm.

Figure 7. Condylar surface texture in the distal femora of Struthio camelus.

A: adult (OUVC 9439); B: subadult (OUVC 9438) ostrich. Scale bar equals 1 cm.

Figure 8. Skeletonized femora of living and extinct archosaur taxa illustrating lack of bony condylar structures, suggesting the presence of significant amounts of epiphyseal cartilage.

Postosuchus redrawn from Chatterjee , Leptosuchus modified from Long and Murray ; Triceratops modified from Dodson ; Plateosaurus modified from Galton and Upchurch ; Apatosaurus modified from Ostrom and McIntosh ; Coelophysis modified from Colbert ; Allosaurus modified from Madsen ; Deinonychus modified from Ostrom . Scale bar equals 10 cm.