Cartilaginous Epiphyses in Extant Archosaurs and Their Implications for Reconstructing Limb Function in Dinosaurs

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.

[1]  R. Owen.  A monograph on the British fossil reptilia of the Mesozoic formations , 1874 .

[2]  E. Cope.  On the Saurians Recently Discovered in the Dakota Beds of Colorado , 1878, The American Naturalist.

[3]  O. C. Marsh.  Principal characters of American Jurassic dinosaurs; Part VI, Restoration of Brontosaurus. , 1883, American Journal of Science.

[4]  H. Osborn,et al.  Additional characters of the great herbivorous dinosaur Camarasaurus. Bulletin of the AMNH ; v. 10, article 12. , 1898 .

[5]  J. B. Hatcher.  Diplodocus (Marsh): its osteology, taxonomy, and probable habits, with a restoration of the skeleton , 1901, Memoirs of the Carnegie Museum.

[6]  O. P. Hay.  On the Habits and the Pose of the Sauropodous Dinosaurs, Especially of Diplodocus , 1908, The American Naturalist.

[7]  Haines Rw.  The Primitive Form of Epiphysis in the Long Bones of Tetrapods. , 1938 .

[8]  R. Haines.  The Primitive Form of Epiphysis in the Long Bones of Tetrapods. , 1938, Journal of anatomy.

[9]  R. Haines.  The structure of the epiphyses in Sphenodon and the primitive form of secondary centre. , 1939, Journal of anatomy.

[10]  Haines Rw.  The structure of the epiphyses in Sphenodon and the primitive form of secondary centre. , 1939 .

[11]  B. Brown,et al.  The Structure and Relationships of Protoceratops , 1940 .

[12]  R. Haines,et al.  Epiphysial structure in lizards and marsupials. , 1941, Journal of anatomy.

[13]  R. S. Lull,et al.  Hadrosaurian Dinosaurs of North America , 1942 .

[14]  R. Haines.  THE EVOLUTION OF EPIPHYSES AND OF ENDOCHONDRAL BONE , 1942 .

[15]  B. Brown,et al.  Studies of the phytosaurs Machaeroprosopus and Rutiodon. Bulletin of the AMNH ; v. 88, article 2 , 1947 .

[16]  P. Dodson,et al.  Marsh's Dinosaurs: The Collections from Como Bluff , 1999 .

[17]  Carl Gans,et al.  Biology of the Reptilia , 1969 .

[18]  W H Simon,et al.  Scale effects in animal joints. I. Articular cartilage thickness and compressive stress. , 1970, Arthritis and rheumatism.

[19]  P. Galton,et al.  THE POSTURE OF HADROSAURIAN DINOSAURS , 1970 .

[20]  C. Gans,et al.  Biology of the Reptilia. Volume 3: Morphology C , 1970 .

[21]  R. Bakker.  Ecology of the Brontosaurs , 1971, Nature.

[22]  W. Coombs.  Sauropod habits and habitats , 1975 .

[23]  J. H. Ostrom.  On a new specimen of the lower Cretaceous theropod dinosaur Deinonychus antirrhopus , 1976 .

[24]  J. Madsen.  Allosaurus Fragilis: a Revised Osteology , 1976 .

[25]  John Goodfellow,et al.  Scientific foundations of orthopaedics and traumatology , 1980 .

[26]  R. A. Thulborn.  Speeds and gaits of dinosaurs , 1982 .

[27]  C. W. McCutchen,et al.  Lubrication of and by Articular Cartilage , 1983 .

[28]  R. Reid.  The histology of Dinosaurian bone and its possible bearing on Dinosaurian physiology , 1984 .

[29]  K. Schmidt-Nielsen,et al.  Scaling, why is animal size so important? , 1984 .

[30]  F. Hainsworth.  Scaling: why is animal size so important? , 1985 .

[31]  A. Russell,et al.  Structure and function of the pectoral girdle and forelimb of Struthiomimus altus (Theropoda: Ornithomimidae) , 1985 .

[32]  S. Chatterjee,et al.  Postosuchus, a New Thecodontian Reptile from the Triassic of Texas and the Origin of Tyrannosaurs , 1985 .

[33]  R. M. Alexander,et al.  Mechanics of posture and gait of some large dinosaurs , 1985 .

[34]  R. Bakker.  The Dinosaur Heresies , 1986 .

[35]  G. Paul,et al.  Predatory Dinosaurs of the World: A Complete Illustrated Guide , 1988 .

[36]  Tony Thulborn,et al.  Gaits of dinosaurs , 1989 .

[37]  K. Padian,et al.  The Beginning of the Age of Dinosaurs , 1989 .

[38]  David D. Gillette,et al.  Dinosaur tracks and traces , 1990 .

[39]  K. Holmes,et al.  Sexually transmitted diseases in the AIDS era. , 1991, Scientific American.

[40]  P. Sereno.  Basal Archosaurs: Phylogenetic Relationships and Functional Implications , 1991 .

[41]  R. M. Alexander.  How Dinosaurs Ran , 1991 .

[42]  B. Hall.  Bone matrix and bone specific products , 1991 .

[43]  C. Ruff,et al.  Use of biplanar radiographs for estimating cross‐sectional geometric properties of mandibles , 1992, The Anatomical record.

[44]  J. Baumel.  Handbook of avian anatomy: nomina anatomica avium. 2nd ed. , 1993 .

[45]  R. Albrecht,et al.  Evidence of the Growth Plate and the Growth of Long Bones in Juvenile Dinosaurs , 1993, Science.

[46]  R. E. Heinrich,et al.  Femoral ontogeny and locomotor biomechanics of Dryosaurus lettowvorbecki (Dinosauria, Iguanodontia) , 1993 .

[47]  P. Sereno,et al.  Dinosaurian precursors from the Middle Triassic of Argentina: Lagerpeton chanarensis , 1994 .

[48]  T. Holtz.  The arctometatarsalian pes, an unusual structure of the metatarsus of Cretaceous Theropoda (Dinosauria: Saurischia) , 1995 .

[49]  J. Thomason,et al.  Functional Morphology in Vertebrate Paleontology , 1998 .

[50]  Juvenile Skeletal Structure and the Reproductive Habits of Dinosaurs , 1996, Science.

[51]  Peter Dodson,et al.  The Horned Dinosaurs: A Natural History , 1996 .

[52]  Stephen M. Gatesy,et al.  Bipedalism, flight, and the evolution of theropod locomotor diversity , 1997 .

[53]  F Eckstein,et al.  Non-invasive determination of cartilage thickness throughout joint surfaces using magnetic resonance imaging. , 1997, Journal of biomechanics.

[54]  Kevin Padian,et al.  The origin and early evolution of birds , 1998 .

[55]  M. Carrano,et al.  Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology , 1998, Paleobiology.

[56]  R. E. Heinrich,et al.  Skeletal allometry and interlimb scaling patterns in mustelid carnivorans , 1998, Journal of morphology.

[57]  Borjana Mikic,et al.  Epigenetic mechanical factors in the evolution of long bone epiphyses , 1998 .

[58]  Paul C. Sereno,et al.  Early Evolution and Higher-Level Phylogeny of Sauropod Dinosaurs , 1998 .

[59]  M. Carrano.  What, if anything, is a cursor? Categories versus continua for determining locomotor habit in mammals and dinosaurs , 1999 .

[60]  P. Christiansen.  Long bone scaling and limb posture in non-avian theropods: Evidence for differential allometry , 1999 .

[61]  Kenneth Carpenter,et al.  Eggs, Nests, and Baby Dinosaurs: A Look at Dinosaur Reproduction , 1999 .

[62]  Body mass estimation in armoured mammals: cautions and encouragements for the use of parameters from the appendicular skeleton , 1999 .

[63]  M. Carrano,et al.  Titanosaurs and the origin of “wide-gauge” trackways: a biomechanical and systematic perspective on sauropod locomotion , 1999, Paleobiology.

[64]  K. Carpenter.  MARSH'S DINOSAURS: THE COLLECTIONS FROM COMO BLUFF , 2001 .

[65]  John R. Hutchinson,et al.  Adductors, abductors, and the evolution of archosaur locomotion , 2000, Paleobiology.

[66]  R. Blob.  Interspecific scaling of the hindlimb skeleton in lizards, crocodilians, felids and canids: does limb bone shape correlate with limb posture? , 2000 .

[67]  Per Christiansen,et al.  Forelimb posture in neoceratopsian dinosaurs: implications for gait and locomotion , 2000, Paleobiology.

[68]  S. Yerby,et al.  Dinosaurian growth patterns and rapid avian growth rates , 2001, Nature.

[69]  C. Brochu.  PROGRESS AND FUTURE DIRECTIONS IN ARCHOSAUR PHYLOGENETICS , 2001, Journal of Paleontology.

[70]  J. Horner,et al.  Dinosaurian growth rates and bird origins , 2001, Nature.

[71]  M. Carrano,et al.  Implications of limb bone scaling, curvature and eccentricity in mammals and non‐avian dinosaurs , 2001 .

[72]  Mariano Garcia,et al.  Tyrannosaurus was not a fast runner , 2002, Nature.

[73]  Richard J. Smith.  Skeletal form and function , 2002 .

[74]  J. M. Starck,et al.  Bone microstructure and developmental plasticity in birds and other dinosaurs , 2002, Journal of morphology.

[75]  H. Kronenberg,et al.  Developmental regulation of the growth plate , 2003, Nature.

[76]  R. Fariña,et al.  Giants and Bizarres: Body Size of Some Southern South American Cretaceous Dinosaurs , 2004 .

[77]  J. Hutchinson,et al.  Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa , 2004, Journal of morphology.

[78]  Matthew F. Bonnan.  Morphometric analysis of humerus and femur shape in Morrison sauropods: implications for functional morphology and paleobiology , 2004, Paleobiology.

[79]  John R Hutchinson,et al.  Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa , 2004, Journal of morphology.

[80]  R. Elsey,et al.  Femoral dimensions and mid‐thigh circumference in Alligator mississippiensis , 2004 .

[81]  R. Mulkern,et al.  Age-related vascular changes in the epiphysis, physis, and metaphysis: normal findings on gadolinium-enhanced MRI of piglets. , 2004, AJR. American journal of roentgenology.

[82]  J. Robins,et al.  Range of motion in the forelimb of the theropod dinosaur Acrocanthosaurus atokensis , and implications for predatory behaviour , 2005 .

[83]  Jeffrey A. Wilson,et al.  The Sauropods: Evolution and Paleobiology , 2005 .

[84]  Jeffrey A. Wilson,et al.  One Overview of Sauropod Phylogeny and Evolution , 2005 .

[85]  G. Erickson.  Assessing dinosaur growth patterns: a microscopic revolution. , 2005, Trends in ecology & evolution.

[86]  B. MacFadden,et al.  Body size in mammalian paleobiology : estimation and biological implications , 2005 .

[87]  K. C. Rogers.  “Sauropod Histology: Microscopic Views on the Lives of Giants” , 2005 .

[88]  P. Senter.  Function in the stunted forelimbs of Mononykus olecranus (Theropoda), a dinosaurian anteater , 2005, Paleobiology.

[89]  J. Hutchinson,et al.  Analysis of hindlimb muscle moment arms in Tyrannosaurus rex using a three-dimensional musculoskeletal computer model: implications for stance, gait, and speed , 2005, Paleobiology.

[90]  L. Alcalá,et al.  A Giant European Dinosaur and a New Sauropod Clade , 2006, Science.

[91]  J. Hutchinson,et al.  Dinosaur Locomotion: Beyond the bones , 2006, Nature.

[92]  C. Meyer,et al.  Super sizing the giants: first cartilage preservation at a sauropod dinosaur limb joint , 2007, Journal of the Geological Society.

[93]  K. Padian,et al.  The opisthotonic posture of vertebrate skeletons: postmortem contraction or death throes? , 2007, Paleobiology.

[94]  L. Witmer.  2 The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils , 2007 .

[95]  P. Senter.  Analysis of forelimb function in basal ceratopsians , 2007 .

[96]  K. Witter,et al.  Articular cartilage in the knee joint of the African elephant, Loxodonta africana, Blumenbach 1797 , 2008, Journal of morphology.

[97]  J. Hutchinson,et al.  Constraint-Based Exclusion of Limb Poses for Reconstructing Theropod Dinosaur Locomotion , 2009 .

[98]  R. Alexander,et al.  A dynamic similarity hypothesis for the gaits of quadrupedal mammals , 2009 .

[99]  R. McN. Alexander,et al.  The thickness of the walls of tubular bones , 2009 .

[100]  D. Suzuki,et al.  Shape of articular surface of crocodilian (Archosauria) elbow joints and its relevance to sauropsids , 2010, Journal of morphology.

[101]  O. C. Marsh.  The Dinosaurs of North America , 2010 .

[102]  R. Elsey,et al.  Calcified cartilage shape in archosaur long bones reflects overlying joint shape in stress‐bearing elements: Implications for nonavian dinosaur locomotion , 2010, Anatomical record.

[103]  J. Farlow,et al.  The Complete Dinosaur , 2012 .