16.3 N&V Feature MH 13/3/06 11:11 AM Page 292 Vol 440|16 March 2006 NEWS & VIEWS FEATURE DINOSAUR LOCOMOTION Beyond the bones John R. Hutchinson and Stephen M. Gatesy How did dinosaurs stand and move? Computer simulation and other methods have told us much about how dinosaurs did and did not move, but they have not yet reached their full potential. Ray Harryhausen, famous animator of crea- tures in such films as Jason and the Argonauts and The Valley of Gwangi, has written that “I a found dinosaurs to be the ideal subject for stop-motion animation... The fact that nobody Hip joint knew how those huge reptiles had moved or, for that matter, exactly how they looked meant Femur that I could bring them alive without any fear b of criticism”1. Harryhausen indeed showed Knee that nothing brings an extinct animal to life Joint c more than seeing it move. But can walking and Tibia/fibula running dinosaurs be animated with scientific rigour rather than just artistic flair? Dinosaurs Tarsals Ankle joint are excellent study organisms for researchers interested in such aspects of biomechanics as Metatarsals Phalanges the repeated evolution of large size, shifts to and from bipedalism and quadrupedalism2,3, and changes in joint structure, musculature and behaviour4–10. Figure 1 | Tyrannosaurus rex as an example of dinosaur anatomy and locomotion. a, The basic skeletal b Unlike investigators working exclusively on components and joints of the hindlimb. Only the third toe is shown for clarity. , Redundancy allows the limb to assume a range of potential hip heights. c, For each position of the hip with respect to the living animals, palaeobiologists can’t directly foot, a spectrum of internal configurations is possible. record the motion, measure the forces or dissect the soft-tissue anatomy of their study simple metric, because the joints are flexible saurus as consultants for the ‘Dinosaurs: organisms. Rather than consigning this prob- enough to allow the tyrannosaur to lie down. Ancient Fossils, New Discoveries’ exhibit at lem to the unknowable, we can make general Even after a hip position is chosen, a spectrum the American Museum of Natural History19. inferences about individual species11–15, as of poses still remains, because three segments, Having previously avoided complete recon- well as about large-scale patterns of locomotor rather than one or two, span from hip to toes structions in our own research, we wondered evolution3,5,10,16. But specific hypotheses about (Fig. 1c). If a dinosaur’s hip, knee, ankle and whether we could legitimately present our dinosaur motion, mechanics and performance main toe joints can flex and extend through an ‘result’ as a scientific hypothesis rather than (such as speed, acceleration and agility) remain arc of 90ᑻ, variation of each by 1ᑻ increments just a pretty moving picture. We found the controversial7,11,13,15,17,18. Several approaches to would yield more than 67 million possible process humbling — not because creating a the generation and testing of such hypotheses poses. Most of these can be excluded as geo- walking stride for the model was difficult, but are described in Box 1. Here we focus on metrically or biologically implausible. Yet even because (with the aid of the museum’s anima- a recent trend in the field: the increased use in this two-dimensional example, thousands tor, Scott Harris) inventing motion was all too of computer animation and simulation to of possible configurations remain. easy. How would we know which limb poses recreate dinosaur locomotion, taking Tyranno- were off the mark and which were closer to saurus rex as our example. Animation reality? We reluctantly settled on one ani- The availability of sophisticated animation mation that captured the basic principles of Uncertainties and simulation software allows palaeobiolo- animal locomotion (see Movie 1 in Supple- Uncertainty about movement stems directly gists to tackle fundamental questions about mentary Information). Yet we could have from the framework of the animal’s leg. Bony dinosaur locomotion in a new way. However, produced thousands of animations that were articulations (Fig. 1a) provide crucial evi- digital dinosaurs are most commonly seen in no better or worse. Computational tools offer dence, but deciding which subset of potential the popular media, and more often than not tremendous power to generate motion, but we joint positions a dinosaur habitually used to little scientific substance underlies such films now face the new problem of how to choose stand or move is by no means straightforward. and documentaries. Yet making virtual among countless hypotheses. Redundancy in the limb skeleton (what engi- dinosaurs move can be done scientifically. Palaeontologists have two main options neers call excess degrees of freedom) precludes This is an excellent opportunity to let the when confronting redundancy in an articu- a unique solution. For example, how high was public see science in action. lated chain of bones (Fig. 1). The first is to set the hip joint above the ground (Fig. 1b)? The We had first-hand experience of the com- arbitrary constraints on the system to reduce bones alone do not establish this seemingly plexities of animating a walking Tyranno- the number of possibilities. A dinosaur’s 292 © 2006 Nature Publishing Group 16.3 N&V Feature MH 13/3/06 11:11 AM Page 293 NATURE|Vol 440|16 March 2006 NEWS & VIEWS FEATURE Box 1 Traditional approaches to investigating dinosaur locomotion6 are placed on the musculoskeletal system. The GRF increases with speed, and so at top speed ● Comparison with living analogues (for emphasized over soft tissues. Limb-joint the maximum GRF can be used to estimate example, hoofed mammals, birds, elephants redundancy is again a serious problem. the size of the muscles needed to support and rhinoceroses) reveals some broad-brush ● Biomechanical modelling is one of the most the limb13–15. similarities4,7. But there are no rigorous means of rigorous methods to reconstruct how specific testing the choice of analogue and the extent to dinosaurs moved11–15,17,18,20,21. Locomotor Constraints which its characteristics are applicable. Once complexity cannot be captured in simple A range of kinematic (motion-based or geo- analogies are inferred, little further progress is models, however, and the number of unknown metric) and kinetic (force-based) criteria help possible. parameters jumps quickly as models become to exclude certain poses for Tyrannosaurus as ● Bone scaling is a more quantitative method, more complex. The best models are validated by unrealistic. The goal is to constrict the ‘config- revealing how dinosaur bone shape changed data from living animals and analyse unknown uration space’ of poses as narrowly as possible, with size. It has shown that size had the same parameters to see if reasonable values would by sequentially adding constraints that rule influence on dinosaurs as on many mammals2,6,27, drastically change the results. out poses as impossible or unlikely, depending strengthening the conclusion that larger ● Viewing dinosaurs in their evolutionary on the strength of support from studies of the dinosaurs were not as athletic as smaller ones. context tells us much about broad historical locomotion of extant animals. We add kine- Yet this yields little specific information about trends but little about how specific animals matic constraints first. For example, body how any one dinosaur moved. moved. For example, within the theropod segments cannot penetrate each other or the ● Fossil footprints are stunning evidence dinosaurs, which include Tyrannosaurus, surface of the ground, and joints cannot of dinosaur behaviour8,25,28,29, for example tracing the skeletal correlates of limb muscle exceed certain maximal and minimal joint supporting the inference that ancestral dinosaurs attachments reveals a stepwise pattern of angles — in particular, the ankle and knee stood and moved with more erect bipedal limbs change, with the hindlimb attaining its ‘modern’ cannot bend backwards. But a huge configura- than their more sprawling and quadrupedal condition only in animals closely related to extant tion space remains, and many plausible poses ancestors9,10. But estimating speed from birds3,5,6,10,28. Yet how did any one dinosaur fit into cannot be excluded (Fig. 3). footprints has a wide margin of error12, and this trend? Did Tyrannosaurus move its femur Next, kinetic constraints based on biomech- footprints tell us little about how the whole limb through large arcs during walking (like a anical studies are added. First, the GRF is or body moved, because of redundancy within crocodile), as we presume the ancestors of both oriented vertically through its point of appli- the limb skeleton (Fig. 1). of these groups of reptiles did? Or can we identify cation at the foot–ground interface24,25. Sec- ● Functional morphology is a classical aspects of its locomotion that were more derived, ond, poses are excluded in which any joints foundation of locomotion research. It is important closer to the condition in extant birds, such as have unreasonable joint moments incurred by for determining how much motion or what poses keeping the femur more horizontal during the GRF — the hip, knee and ankle require the certain limb joints could allow4,7,9,30. Much like walking, entailing a more crouched limb action of extensor muscles that straighten the scaling approaches, bones are usually configuration? J.R.H. & S.M.G. limb and work against the force of gravity. Again, this constraint is congruent with living limb orientation is often taken for granted (Fig. 2a). In the stance phase, the limb pushes animals16. It excludes the first example pose by duplicating a mammalian, avian or some down on the ground to incur an equal but (Fig. 3a), because the GRF is in front of the other intuitively pleasing pose7,20.