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Biomechanics of ossified tendons in ornithopod dinosaurs

Published online by Cambridge University Press:  08 April 2016

Chris L. Organ
Chris L. Organ*
Affiliation:
Museum of the Rockies, Montana State University, Bozeman, Montana 59717
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Abstract

Spinal ossified tendons are a defining character for Ornithischia, one of the two major clades of dinosaurs. The function of these bony rods has remained a mystery since their first detailed description in 1886. Qualitative approaches to understand ossified tendon function have resulted in different ecological and behavioral interpretations for ornithopod dinosaurs. To evaluate ossified tendon function, this study constructed finite element models of the vertebral column for two ornithopod taxa: Tenontosaurus, which shows the plesiomorphic condition of longitudinally arrayed tendons along the spinous processes, and Brachylophosaurus, which exhibits a lattice of tendons along the spinous processes. Both models predict that ossified tendons stiffened the vertebral column, especially the tail, but the derived lattice of ossified tendons in iguanodontoidean dinosaurs, like Brachylophosaurus, increased spinal stiffness more than the plesiomorphic condition. Caudofemoral muscles that retracted the hindlimb during locomotion attached the femur to the tail in ornithopods. Increased tail stiffness caused by intratendinous ossification may have influenced locomotion by rigidly anchoring M. caudofemoralis longus to the tail, thereby allowing a more forceful retraction of the hindlimb by reducing ventral flexion of the tail during muscle contraction. Ossified tendons may also have been important for storing elastic energy throughout the gait cycle. Moreover, the lattice of ossified tendons stiffened the trunk and tail nearly equally in Brachylophosaurus, indicating the evolution of a postural function by passively supporting the epaxial musculature in maintaining a horizontal vertebral column.

Type
Articles
Information
Paleobiology , Volume 32 , Issue 4 , Fall 2006 , pp. 652 - 665
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alexander, R. M. 1988. Elastic mechanisms in animal movement. Cambridge University Press, New York.Google Scholar
Alexander, R. M., and Jayes, A. S. 1981. Estimates of the bending moments exerted by the lumbar and abdominal muscles of some mammals. Journal of Zoology 194:291–303.CrossRefGoogle Scholar
Bennett, M. B., and Stafford, J. A. 1988. Tensile properties of calcified and uncalcified avian tendons. Journal of Zoology 214:343–351.CrossRefGoogle Scholar
Bennett, M. B., Ker, R. F., Dimery, N. J., and Alexander, R. M. 1986. Mechanical properties of various mammalian tendons. Journal of Zoology, ser. A 209:537–548.Google Scholar
Blob, R. W., and Biewener, A. A. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture. Journal of Experimental Biology 202:1023–1046.CrossRefGoogle ScholarPubMed
Brown, B. 1916. Corythosaurus casuarius: skeleton, musculature and epidermis. Bulletin of the American Museum of Natural History 35:709–716.Google Scholar
Bultynck, P. 1992. An assessment of posture and gait in Iguanodon bernissartensis . Bulletin de l'Institut Royal des Sciences Naturelles de Belgique 63:5–11.Google Scholar
Chen, E. J., Novakofski, J., Jenkins, W. K., and O'Brien, W. D. J. 1996. Young's modulus measurements of soft tissues with application to elasticity imaging. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control 43:191–194.CrossRefGoogle Scholar
Colbert, E. H. 1951. Environment and adaptations of certain dinosaurs. Biology Review 26:265–284.CrossRefGoogle Scholar
Coombs, W. P. J. 1995. Ankylosaurian tail clubs of middle Campanian to early Maastrichtian age from western North America, with description of a tiny tail club from Alberta and discussion of tail orientation and tail club function. Canadian Journal of Earth Sciences 32:902–912.CrossRefGoogle Scholar
Cubo, J., and Casinos, A. 2000. Mechanical properties and chemical composition of avian long bones. European Journal of Morphology 38:112–121.CrossRefGoogle ScholarPubMed
Currey, J. D. 1988. The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. Journal of Biomechanics 21:131–139.CrossRefGoogle ScholarPubMed
Currey, J. D. 1990. Physical characteristics affecting the tensile failure properties of compact bone. Journal of Biomechanics 23:837–844.CrossRefGoogle ScholarPubMed
Currey, J. D. 1999. The design of mineralized hard tissues for their mechanical functions. Journal of Experimental Biology 202:3285–3294.CrossRefGoogle ScholarPubMed
Currey, J. D. 2001. Ontogenetic changes in compact bone material properties. Pp. 19, 1–16 in Cowin, S. C., ed. Bone mechanics handbook. CRC Press, Boca Raton, Fla. Google Scholar
Cyron, B. M., and Hutton, W. C. 1978. The fatigue strength of the lumbar neural arch in spondylolysis. Journal of Bone and Joint Surgery 60B:234–238.Google Scholar
Cyron, B. M., Hutton, W. C., and Troup, J. D. G. 1976. Spondylolytic fractures. Journal of Bone and Joint Surgery 58B:462–466.Google Scholar
Dilkes, D. W. 2000. Appendicular myology of the hadrosaurian dinosaur Maiasaura peeblesorum from the Late Cretaceous (Campanian) of Montana. Transactions of the Royal Society of Edinburgh, Earth Science 90:87–125.CrossRefGoogle Scholar
Dollo, L. 1886. Note sur les ligaments ossifies des dinosauriens de Bernissart. Archives de Biologie 7:249–264.Google Scholar
Forster, C. A. 1990. The postcranial skeleton of the ornithopod dinosaur Tenontosaurus tilletti . Journal of Vertebrate Paleontology 10:273–294.CrossRefGoogle Scholar
Galton, P. M. 1970. The posture of hadrosaurian dinosaurs. Journal of Paleontology 44:464–473.Google Scholar
Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170–186.CrossRefGoogle Scholar
Gatesy, S. M. 1995. Functional evolution of the hindlimb and tail from basal theropods to birds. Pp. 219–234 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Gatesy, S. M. 1997. An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion. Journal of Morphology 234:197–212.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Gatesy, S. M., and Dial, K. P. 1996. Locomotor modules and the evolution of avian flight. Evolution 50:331–340.CrossRefGoogle ScholarPubMed
Guo, X. E. 2001. Mechanical properties of cortical and cancellous bone tissue. Pp. 10, 1–19 in Cowin, S. C., ed. Bone mechanics handbook. CRC Press, Boca Raton, Fla. Google Scholar
Integrated Engineering Software. 2000. Visual Analysis 4. 0. Bozeman, Mont.Google Scholar
Ladd, A. J., Kinney, J. H., Haupt, D. L., and Goldstein, S. A. 1998. Finite-element modeling of trabecular bone: comparison with mechanical testing and determination of tissue modulus. Journal of Orthopedic Research 16:622–628.CrossRefGoogle ScholarPubMed
Lull, R. S., and Wright, N. E. 1942. Hadrosaurian dinosaurs of North America. Geological Society of America Special Paper 40:242.Google Scholar
Martin, R. B., Burr, D. B., and Sharkey, N. A. 1998. Skeletal tissue mechanics. Springer, New York.CrossRefGoogle Scholar
Nigg, B. M., and Herzog, W. 1999. Biomechanics of the musculoskeletal system. Wiley, Chichester, U.K. Google Scholar
Nishi, S. 1938. Muskeln des Rumpfes. Pp. 351–446 in Bolk, L., Göppert, E., Kallius, E., and Lubosch, W., eds. Handbuch der vergleichebnden Anatomie der Wirbeltiere, Bd. 5. Urban und Scwarzenberg, Berlin.Google Scholar
Norman, D. B. 1980. On the ornithischian dinosaur Iguanodon bernissartensis from the lower Cretaceous of Bernissart (Belgium). L'Institut Royal des Sciences Naturelles de Belgique Memoire 178:1–103.Google Scholar
Norman, D. B. 1985. The illustrated encyclopedia of dinosaurs. Salamander Books, London.Google Scholar
Norman, D. B. 1986. On the anatomy of Iguanodon atherfieldensis (Ornithischia: Ornithopoda). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique, Sciences de la Terre 56:281–372.Google Scholar
Organ, C. L. 2006. Thoracic epaxial muscles in living archosaurs and ornithopod dinosaurs. The Anatomical Record, Part A. Discoveries in Molecular, Cellular, and Evolutionary Biology 288A:782–793.CrossRefGoogle Scholar
Organ, C. L., and Adams, J. 2005. The histology of ossified tendon in dinosaurs. Journal of Vertebrate Paleontology 25:602–613.CrossRefGoogle Scholar
Ostrom, J. H. 1964. A reconsideration of the paleoecology of hadrosaurian dinosaurs. American Journal of Science 262:975–997.CrossRefGoogle Scholar
Reilly, S. M., and Elias, J. A. 1998. Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm. Journal of Experimental Biology 201:2559–2574.CrossRefGoogle Scholar
Rigby, B. J., Hirai, N., Spikes, J. D., and Eyring, H. 1959. The mechanical properties of rat tail tendon. Journal of General Physiology 43:265–283.CrossRefGoogle ScholarPubMed
Rothschild, B. M., and Tanke, D. 1992. Paleopathology of vertebrates: insights to lifestyle and health in the geological record. Geoscience Canada 19:73–82.Google Scholar
Roy, M. E., Rho, J.-Y., Tsui, T. Y., Evans, N. D., and Pharr, G. M. 1999. Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. Journal of Biomedical Material Research 44:191–197.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:2137–2147.CrossRefGoogle ScholarPubMed
Silver, F. H., Christiansen, D., Snowhill, Y. C., and Landis, W. J. 2000. The role of mineral in the storage of elastic energy in turkey tendons. Biomacromolecules 1:180–185.CrossRefGoogle ScholarPubMed
Silver, F. H., Freeman, J. W., Horvath, J. W., and Landis, W. J. 2001. Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules 2:750–756.CrossRefGoogle ScholarPubMed
Tsuihiji, T. 2005. Homologies of the transversospinalis muscles in the anterior presacral region of Sauria (crown Diapsida). Journal of Morphology 263:151–178.CrossRefGoogle ScholarPubMed
Vallois, H. V. 1922. Les transformations de la musculature de l'épisome chez les vertébrés. Archives de Morphologie Générale et Experimentale 13:1–538.Google Scholar
Vanden Berge, J. C., and Storer, R. W. 1995. Intratendinous ossification in birds: a review. Journal of Morphology 226:47–77.CrossRefGoogle Scholar
Viidik, A. 1966. Biomechanics and functional adaptation of tendons and joint ligaments. Pp. 17–38 in Evans, F. G., ed. Studies on the anatomy and function of bone and joints. Springer, New York.CrossRefGoogle Scholar