Chapter 1 INTRODUCTION

Chapter 1. Introduction

1.1. Preamble Palaeontologists face the challenge of revealing how extinct animals lived in the past using fossil and stratigraphic information. Vertebrate fossils not only comprise bone remains, but also footprints, burrows, coprolites, nests and eggs, amongst others. All of them provide insights. For example, bone remains are useful for the study of anatomy, animal evolution, growth, disease, death condition and skeletal function. Fossil footprints are a better source of information related to behaviour such as estimation of speed and possible inter-intraspecific interactions. In the present study I provide new contributions in two complementary areas: dinosaur ichnology in South America and evolution of pedal function in ornithopod dinosaurs. Both areas use information that can be obtained from dinosaur feet themselves and the sedimentary structures they generated. But before entering the details of this research project, it is useful to present the current state of knowledge about dinosaur footprints in South America and dinosaur pedal biomechanics.

1.2. Dinosaur footprints in South America The study of terrestrial animals through time in South America has been mainly focused on the Triassic and Cretaceous periods, due the particular interest in the origin and extinction of non-avian dinosaurs. However, fewer investigations have been carried out on the Jurassic. During the Jurassic, the megacontinent Pangaea began to fragment in two subcontinents known as Laurasia (North America, Asia and Europe) and Gondwana (Africa, Antarctica, Australia, India and South America), leading to the opening of the Tethys Ocean (Fig. 1-1).

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Figure 1-1. Position of the continents 140 mya, time period when Laurasia and Gondwana begin to rift apart (redrawn from Philippe et al., 2003)

As suggested by numerous findings in North America and Europe, the Laurasian fauna corresponds to the public conception of dinosaur life, with carnivorous theropods and long-necked sauropods as dominant herbivores. However, the skeletal record also indicates a major faunal switch in Laurasia during the Early Cretaceous, with ornithopod dinosaurs replacing sauropods as dominant herbivores (Bakker, 1971; Weishampel and Norman, 1989). In contrast to the Laurasian fauna, the Gondwanan fauna is not well understood due to the scarcity of data available. The separation of landmasses implies evolutionary divergences, thus faunal differences between Laurasia and Gondwana are expected. However, strong similitude between Jurassic African and North American dinosaurs suggest the presence of complex land bridges between both landmasses (Upchurch, 2002). In South America a limited number of Jurassic dinosaur bones and trackbeds are known, mainly from Argentina and Brazil (Bonaparte, 1979, 1986; Leonardi, 1989, 1994; Rich et al., 1999; Weishampel et al., 2004). However, several new Late Jurassic - Early

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Chapter 1. Introduction

Cretaceous trackbeds have been recently discovered in Chile and Peru. These new materials represent a valuable source of information for studying the possible relationships between faunas within Gondwana. The new data will also allow a direct comparison with Laurasian faunas, for example about titanosaurid, iguanodontian and abelisaurid migrations, and about palaeoenvironments. Results could help to identify land bridges and faunal contributions from or toward South America.

1.3. Dinosaur pedal biomechanics

1.3.1. Problematic The biomechanics of dinosaur locomotion has been focused mainly on musculoskeletal studies of the upper part of the hind limb (e.g.; Gatesy, 1990; Heinrich et al., 1993; Carrano, 1998; Carrano and Biewener, 1999). The functional morphology of the hip, femur, tibia-fibula, and tarsus in theropod dinosaurs are particularly well understood (e.g.; Gatesy, 1990; Farlow et al., 2000; Hutchinson and Gatesy, 2000; Hutchinson and Garcia, 2002; Hutchinson, 2004a, 2004b). However, our understanding of dinosaur locomotion as a whole is limited. Other dinosaur groups such as ornithopods, stegosaurids and anquilosaurids, have been less studied. Furthermore, the foot which is an important part of the hind limb, has been almost entirely ignored. Only a few descriptions of dinosaur pedal motion have been attempted (Gatesy et al., 1999; Gatesy, 2001), using computer models and footprints. Feet are the first and last structure to receive the powering forces during locomotion, and their design permits the redistribution of loads through several bones (tarsus, metatarsus and phalanges), ligaments, tendons and fat pads. In extant animals, including humans, techniques such as film-force plates, pressure sensors, strain gauge and Finite Element Analysis (FEA) have been proven useful in determining the distribution, mechanics and magnitude of locomotory forces (e.g.; Hinterhofer et al., 2000; Anderson et al., 2003; Cheung et al., 2004). Although, most of those techniques are obviously not

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Chapter 1. Introduction

applicable to fossils, it is possible to study the functional morphology of the foot in extinct animals in more detail by analysing the trabecular architecture of the tarsus, metatarsus and phalanges in fossil specimens. This is because the trabecular structure reflects the manner in which the bones are loaded in life, and therefore can be used to interpret models of stress distribution (Fig. 1.2).

Figure 1-2. Cross-section of the ischium of a horse. Its internal structure reveals a high similarity with a flat plate loaded at its free end (arrow), but is not a perfect engineering design because the bone tissue has to cope with other vital functions (taken from Currey, 2002).

1.3.2. Adaptive bone remodelling The general shape of a bone is determined genetically. Nevertheless, as a living tissue, a bone responds to changes in loading by modifying its size, density, and internal arrangement (Currey, 2002). Thus, the final morphology of a bone largely depends on its mechanical situation. This relationship between loading and bone structure was first recognized by Wolff (1870), and is popularly known as the “Wolff’s law of bone transformation”. Although this so-called “law” has been refuted (Bertram and Swartz, 1991; Cowin, 1997), several studies have shown that trabecular structure tends to correlate with the direction of the principal strains, while trabecular density and location of compact bone correlate with the magnitude of the shear stresses (e.g.; Hayes et al., 1982; Thomason, 1985; Lanyon, 1990; Biewener et al., 1996). Moreover, strains slightly higher than normal stimulate positive remodelling, and by contrast, lower routine strains lead to bone loss

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(Rubin and Lanyon, 1982). It is important to note that the internal structure of a bone does not present an optimal engineering design for loading (Fig. 1-2), since this tissue has to deal with its vital cellular functions as well, such as gas, nutrient and waste material exchange, and regulation of calcium availability. Therefore, bone structure represents only general loading patterns. However, the identification of these patterns is important because it is usually very difficult to determine what forces are acting on a bone or even less clear what stresses are acting inside it.

1.3.3. Finite element analysis Finite Element Analysis (FEA) is a numerical method based on elastic theory, which describes the response of any structure to loading. This theory is described by differential equations dealing with the relationship between applied force, material stiffness and deformation. These complex mathematical expressions can be solved using computational techniques. Basically, specific computer software transforms a given model (two- or threedimensional) into a mesh of small elements interconnected by nodes. The material properties, loading conditions and external constraints limiting rotation and translation (e.g., constraint from the ground) are then incorporated into the mesh data. This method has been extensively used in engineering to evaluate the mechanical performance of structures, and it has also been applied recently to skeletal function in modern and extinct animals (e.g.; Hinterhofer et al., 2000; Chen et al., 2001; Rayfield et al., 2001; Carrigan et al., 2003; Mazzetta et al., 2004; e.g.; Rayfield, 2004), as well as human orthopaedics and other direct biomedical applications.

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1.4. This research project

1.4.1. Pedal bones and footprints Both osteological and ichnological dinosaur records are abundant, but their connection is poor. This is not only because functional studies on the foot are scarce, as mentioned above, but also because of the historical development of palaeoichnology. A large number of publications related to footprints have documented new tracksites and footprint shapes, and attempted to assign such tracks to trackmakers, usually with little in the way of direct anatomical reference. Most efforts to identify trackmakers have been proven unsuccessful at the species level and indeed are usually problematic even at the family level (Farlow, 1992; Farlow and Lockley, 1993). Although foot morphology is not variable enough to be characteristic of only a particular species, it can reveal information about animal palaeoecology and behaviour. For example, the proportional length of distal versus proximal phalanges can serve to discriminate between terrestrial and arboreal avian and non-avian theropod dinosaurs (Hopson, 2001). Moreover, as the feet are in contact with the substrate, they can leave trackways showing not only soft tissue impressions (pads and scales), but also different walking phases in deeper tracks along with the impression of the full range of digit motion (Gatesy et al., 1999). Thus kinematic data can be obtained. This research project represents another step toward a better integration of skeletal and footprint morphology.

1.4.2. Objectives The objectives of this project are two-fold: (1) to provide information about the fauna from the Late Jurassic - Early Cretaceous in South America by investigating new and previously known tracksites, which correspond to the only available information for this period in South America; and (2) to quantify morphological differences of pedal evolution in ornithopod dinosaurs and to generate stress distribution models for each of these morphologies (digitigrade v/s subunguligrade), in order to study the functional

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implications. Both objectives look for a deeper understanding of dinosaur evolution, exploring new sources of information and analytical techniques.

1.4.3. Methods and techniques This research project required classical descriptive methods (Farlow and Chapman, 1997) for the study of dinosaur footprints, such as photography, measurements, mapping, comparison with other materials, etc. Further details about methods are given in the respective sections of Chapter 2. More elaborated techniques were necessary for the study of pedal morphology in ornithopods. For the quantification of external morphology in pedal phalanges, we used a MicroScribe G2XL (Immersion Corporation M.R.) in combination with the software Rhinoceros 3D v3.0 (Robert Mc Neel & Associates). For the assessment of the internal structure, we examined fragmented bones from various museum collections and we collected Computed Tomography (CT) images with a Somatom AR.SP scanner (Siemmens Corporation). Models to study functional morphology were created and analysed with the Finite Element software Algor v16-17 (Algor, Inc.). Briefly, these FE models were built for static analysis, considering real material properties (bone, cartilage and fat pad) and also loads and constraints using natural parameters that were obtained from the literature. Chapter 3 provides settings, more detailed descriptions and justifications for these techniques.

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1.4.4. Thesis organization The thesis has been written in the form of scientific publications. Chapter 2 is made of three publications, which provide a detailed description of newly and previously discovered ichnological materials from the Late Jurassic - Early Cretaceous of northern Chile and southern Peru. In Chapter 3, two publications give insights into the evolution of pedal function of ornithopod dinosaurs. Section 3.1 focuses on the functional morphology of an isolated phalanx, whereas in section 3.2 we investigate the force distribution in a complete pedal digit (digit III) taking account of the cartilage and fat pad. Finally, in Chapter 4, the conclusions of this research project are summarized and ideas for future work are given.

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1.5. References Anderson IA, MacDiarmid AA, Harris ML, Gillies MR, Phelps R, Walsh WR. 2003. A novel method for measuring medial compartment pressures within the knee joint invivo. Journal of Biomechanics 36:1391-1395. Bakker RT. 1971. The ecology of the brontosaurs. Nature 229:172-174. Bertram JEA, Swartz SM. 1991. The law of bone transformation - a case of crying Wolff. Biological Reviews 66:245-273. Biewener AA, Fazzalari NL, Konieczynski DD, Baudinette RV. 1996. Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19:1-8. Bonaparte JL. 1979. Dinosaurs: a Jurassic assemblage from Patagonia. Science 205:13771379. Bonaparte JL. 1986. The dinosaurs (Carnosaurs, Allosaurids, Sauropods, Cetiosaurids) of the Middle Jurassic of Cerro Cóndor (Chubut, Argentina). Annales de Paléontologie 72:325-386. Carrano MT. 1998. Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology. Paleobiology 24:450-469. Carrano MT, Biewener AA. 1999. Experimental alteration of limb posture in the chicken (Gallus gallus) and its bearing on the use of birds as analogs for dinosaur locomotion. Journal of Morphology 240:237-249. Carrigan SD, Whiteside RA, Pichora DR, Small CF. 2003. Development of a threedimensional finite element model for carpal load transmission in a static neutral posture. Annals of Biomedical Engineering 31:718-725. Chen W-P, Tang F-T, Ju C-W. 2001. Stress distribution of the foot during mid-stance to push-off in barefoot gait: a 3-D finite element analysis. Clinical Biomechanics 16:614-620. Cheung JT, Zhang M, An K. 2004. Effects of plantar fascia stiffness on the biomechanical responses of the ankle-foot complex. Clinical Biomechanics 19:839-846. Cowin SC. 1997. The false premise of Wolff's law. Forma 12:247-262.

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Currey JD. 2002. Bones: Structure and Mechanics. Princeton and Oxford: Princeton University Press. 436 p. Farlow JO. 1992. Sauropod tracks and trackmakers: integrating the ichnological and skeletal records. Zubia 10: 89-138. Farlow JO, Lockley MG. 1993. An osteometric approach to the identification of the makers of early Mesozoic tridactyl dinosaur footprints. In: Lucas SG, Morales M, editors. The Nonmarine Triassic. Alburquerque: New Mexico Museum of Natural History and Science. p 123-131. Farlow JO, Chapman RE. 1997. The scientific study of dinosaur footprints. In: Farlow JO, Brett-Surman MK, editors. The Complete Dinosaur. Bloomington: Indiana University Press. p 519-553. Farlow JO, Gatesy SM, Holtz TR, Hutchinson JR, Robinson JM. 2000. Theropod locomotion. American Zoologist 40:640-663. Gatesy SM. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170-186. Gatesy SM, Middleton KM, Jenkins FAJ. 1999. Three-dimensional preservation of foot movements in Triassic theropod dinosaurs. Nature 399:141-144. Gatesy SM. 2001. Skin impressions of Triassic theropods as records of foot movement. Bulletin of the Museum of Comparative Zoology 156:137-149. Hayes WC, Snyder BM, Levine BM, Ramaswamy S. 1982. Stress-morphology relationships in trabecular bone of the patella. In: Galagher RH, editor. Finite Elements in Biomechanics. New York: Wiley. p 223-267. Heinrich RE, Ruff CB, Weishampel DB. 1993. Femoral ontogeny and locomotor biomechanics of Dryosaurus lettowvorbecki (Dinosauria, Iguanodontia). Zoological Journal of the Linnean Society 108:179-196. Hinterhofer C, Stanek C, Haider H. 2000. The effect of flat horseshoes, raised heels and lowered heels on the biomechanics of the equine hoof assed by finite element analysis (FEA). Journal of Veterinary Medicine A47:73-82.

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Hopson JA. 2001. Ecomorphology of avian and nonavian theropod phalangeal proportions: Implications for the arboreal versus terrestrial origin of bird flight. In: Gauthier J, Gall LF, editors. New perspectives on the origin and early evolution of birds: Proceedings of the International Symposium in Honor of John H Ostrom. New Haven: Peabody Museum of Natural History, Yale University. p 211-235. Hutchinson JR, Gatesy SM. 2000. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26:734-751. Hutchinson JR, Garcia M. 2002. Tyrannosaurus was not a fast runner. Nature 415:10181021. Hutchinson JR. 2004a. Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa. Journal of Morphology 262:421-440. Hutchinson JR. 2004b. Biomechanical modeling and sensitivity analysis of bipedal running ability. II. Extinct taxa. Journal of Morphology 262:441-461. Lanyon LE. 1990. The relationship between functional loading and bone architecture. In: DeRousseau CJ, editor. Primate life history and evolution. New York: Wiley-Liss. p 269-284. Leonardi G. 1989. Inventory and statistics of South American dinosaurian ichnofauna and its palaeobiological interpretation. In: Gillette DD, Lockley MG, editors. Dinosaur Track and Traces. Cambridge: Cambridge University Press. p 165-178. Leonardi G. 1994. Annotated atlas of South American tetrapod footprints (Devonian to Holocene) with appendix on Mexico and Central America. Rio de Janeiro: Companhia de Pesquisa de Recursos Minerais. 248 p. Mazzetta GV, Blanco RE, Cisilino AP. 2004. Finite element modelling of a tooth referred to the genus Giganotosaurus Coria and Salgado, 1995 (Theropoda: Carcharodontosauridae). Ameghiniana 41:619-626. Philippe M, Cuny G, Jaillard E, Barale G, Gomez B, Ouaja M, Thévenard F, Thiébaut M, Von Sengbush P. 2003. The paleoxylological record of Metapodocarpoxylon libanoticum (Edwards) Dupéron-Laudoueneix et Pons and the Gondwana Late

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Jurassic-Early Cretaceous continental biogeography. Journal of Biogeography 30:389-400. Rayfield EJ, Norman DB, Horner CC, Horner JR, Smith PM, Thomason JJ, Upchurch P. 2001. Cranial design and function in a large theropod dinosaur. Nature 409:10331037. Rayfield EJ. 2004. Cranial mechanics and feeding in Tyrannosaurus rex. Proceedings of the Royal Society of London B 271:1451-1459. Rich TH, Vickers-Rich P, Gimenez O, Cuneo R, Puerta P, Vacca P. 1999. A new sauropod dinosaur from Chubut Province, Argentina. In: Tomida Y, Rich TH, Vickers-Rich P, editors. Proceedings of the Second Symposium. Tokio: National Science Museum Monographs. p 61-84. Rubin CT, Lanyon LE. 1982. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. Journal of Experimental Biology 101:187-211. Thomason JJ. 1985. The relationship of trabecular architecture to inferred loading patterns in the third metacarpals of the extinct equids Merychippus and Mesohippus. Paleobiology 11:323-335. Upchurch P. 2002. An analysis of dinosaurian biogeography: evidence for the existence of vicariance and dispersal patterns caused by geological events. Proceedings of the Royal Society of London B 269:613-621. Weishampel DB, Norman DB. 1989. Vertebrate herbivory in the Mesozoic; jaws, plants, and evolutionary metrics. Geological Society of America Special Paper 238:87-100. Weishampel DB, Barrett PM, Coria R, Le Loeuff J, Xing X, Xijin Z, Sahni A, Gomani EMP, Noto CR. 2004. Dinosaur distribution. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria. 2nd ed. London, England: University of California Press. p 517-606. Wolff J. 1870. Über die innere Architektur der Knochen und ihre Bedeurung für die Frage von Knochenwachstum. Virchows Archive on Pathological Anatomy 50:389-450.

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