Evolution of Flight in Animals 37

Home , Bird flight, Evolution of birds, Flight feather, Insect flight, Insect wing, Origin of avian flight

Evolution of ﬂight in animals

U.M. Lindhe Norberg Department of Zoology, University of Göteborg, Sweden.

Abstract

The evolution of flight in animals has long been debated and different hypotheses have been suggested for their origins. Controversial opinions about morphology, locomotion and flight evolution can, however, be understood by functional approaches, e.g. by biomechanical treatments and aerodynamic models. New fossils of proto-fliers will constantly increase our understanding of how animals evolved flapping flight. Insects may have developed powered flight via ‘surface- skimming’ on water as used by stoneflies and mayflies. Articulated, movable gill-plates were used for underwater swimming and for circulating water over the gills in aquatic nymphal stages of non-flying insects. They were later raised above the water surface for wind-propelled skimming, and beating of the winglets enabled powered skimming. Eventually, flight muscles became stronger and were used for true powered flight. Vertebrates most probably developed flapping flight via gliding intermediates. The conflicting ‘ground-up’ model includes a number of limitations. Several modifications of the various evolutionary steps in the main theories have been suggested, but particular stress has been laid on whether a gliding stage was included or not. In terms of energy, time, and aerodynamics, the gliding model is the most attractive alternative. If the ground-runner began to use hang-gliding on steep slopes, a running mode of life before the animal could fly would be beneficial. Morphological changes must have evolved in small steps over a long time span, and each new modification towards flight must have contributed to fitness long before the proto-flier could fly.

1 Introduction

Flight is one of the most demanding adaptations found in nature because of the physical problems of moving in air. Therefore, fliers in nature have been subjected to strong selection for optimal morphology to increase flight performance and to minimize flight costs. The characteristics of flying animals are low total mass, large surface area and rigidity of wings. Their wings must meet the requirements of strength and rigidity with least possible mass, and their wing form must be coupled with particular flight modes.

The crucial thing in the evolutionary pathway to powered flight is the production of lift and thrust. While aircraft produce thrust with the engine, animals have to flap their wings. The most important parameter affecting the lift and drag coefficient over the entire size range of flying animals and machines is the Reynolds number, which represents the ratio of inertial to viscous forces in a flow. It is Re = ρul/µ, where ρ is the density, µ is the viscosity of the flow, u is the speed and l is a characteristic length (such as wing chord). Low Reynolds number flight and flapping wing dynamics, which are characteristics of animal flight, involve large-scale vortical motion and detached flows. This is why the Strouhal number enters as a second important parameter for the dynamics (a dimensionless value useful for analysing oscillating, unsteady flow and which is a function of the Reynolds number; St = ωa/u, where ω is the oscillation frequency and a is the amplitude, such as wingtip excursion). A flexible wing has superior performance to a rigid aeroplane wing in this situation. An important benefit from flapping wings of animals compared to fixed-wing aircraft is that animals can manoeuvre better and also make compensating wing movements to avoid stall. Animals can also change wing form to meet different flight conditions and requirements. Insects make up the most diverse and numerous animal class with about 750 000 recorded species. Tiny insects operate at Re < 10 and larger insects at Re ≈ 102 −104.At very low Reynolds numbers viscous forces are large and the flow is more laminar, whereas inertial forces increase with increasing size and speed. Birds comprise more than 8000 species and bats about 1000 species. Their Reynolds numbers vary between 104 and 105, whereas the range for aircraft usually is 106–108. If birds only appeared as fossils we would probably have placed them among the class Reptilia. They would have formed another reptile group that could fly. If pterosaurs were alive today, we may have put them a separate class, like birds, and separate from reptiles. But birds are more different from reptiles than pterosaurs, because they have wing feathers. Long fingers and a flexible membrane make up the bat wings, and it is still debated whether the pterosaur wing was made of a flexible membrane or stiff keratin material, or both.

2 Evolution of insect ﬂight

Several theories have been suggested for the origin of flight in insects (summarized in Thomas and Norberg [1]). An early theory is that insects evolved flight by jumping and gliding down from trees, like early birds and bats [2–4]. Flattened outgrowths at the top of the thorax allowed insects to maintain stable flight. Progressively increasing size of the extensions improved glide angle, they became moveable, and incipient flapping eventually led to powered flight, as in the vertebrate model [3, 4]. A second theory suggests that evolution of insect flight may have originated with relatively large, terrestrial, leaping insects, which launch themselves voluntarily into the air, as many modern insects do [5]. Winglets, which were of help, progressively increased for stability, then gliding, partially powered flight, and eventually fully powered flight. The ‘floating hypothesis’ [4–6] suggests that dorsal extensions in tiny insects aided dispersal by convectional air currents and eventually evolved to flapping wings. Kingsolver and Koehl [7] suggested that flaps first evolved for thermoregulation. The most interesting scenario for the evolution of flapping flight in insects, presented by Marden and Kramer [8, 9] and illustrated in Fig. 1, is that powered flight developed via ‘surface-skimming’ on water. Stoneflies and mayflies, for example, often use water-skimming, which could thus be one stage in the origin of flight. Fossil and developmental evidence indicate that insect wings are

Figure 1: Probable steps in the evolution of insect flight according to the ‘surface-skimming’ hypothesis [1, 2]. Top: Articulated, movable gill-plates were used for underwater swimming and for circulating water over the gills in aquatic nymphal stages of non-flying insects. Bottom left: The plates were later raised above the water surface for wind- propelled skimming, and beating of the winglets enabled powered skimming. The figure shows a male stonefly sailing. Bottom right: Female stonefly sailing. The bottom drawings are based on photographs by Marden and Kramer [9]. homologous to specific epipodites (gills, with respiratory function) of crustacean limbs (traced by gene expression; [10, 11]). Steps leading to flight could have been: (1) articulated, movable gill-plates were used for underwater swimming and for circulating water over the gills in aquatic nymphal stages of non-flying insects; (2) gill-plates, functioning as winglets, were raised above the water surface for wind-propelled skimming; (3) beating of the winglets enabled powered skimming; (4) the flight muscles became stronger and used for true powered flight. This hypothesis makes the gill-to-wing transition possible. Modern stoneflies, which are an ancient group that differs little from their Carboniferous ancestors, use skimming in this way and might be regarded as a functional intermediate form. In surface-skimming there are three sources of water drag: (1) friction between leg and water surface film, (2) inertial drag due to continuous acceleration of water out of the moving dimples as the insect skims on, and (3) inertial drag due to the generation of ripples. The weight of the displaced water from the dimples matches the weight of the insect. Thomas and Norberg [6] suggested that the transition from surface-skimming to true powered flight would be greatly enhanced by the ground-effect; reduction of the aerodynamic induced power could be reduced by 50% just after take-off from water.

3 Evolution of vertebrate ﬂight

3.1 Up–down or down–up?

In his comprehensive book The Origin and Evolution of Birds Feduccia [12] summarized and treated the different theories of the origin of ﬂight in birds. Most aspects of early birds were also

WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) Evolution of Flight in Animals 39 discussed in 1999 at the International Symposium in honour of John H. Ostrom in New Haven, Connecticut [13]. Powered flight in birds, as well as in pterosaurs and bats, may have evolved via gliding in tree- living animals, as described by the arboreal (‘trees-down’) theory [12–25], or from hang-gliding on steep slopes [26] (Fig. 2). Morphological changes must have evolved in small steps over a long time span, and each new modification towards flight must have contributed to fitness long before the proto-flier could fly [15–17]. Whether birds evolved flight via a gliding stage (starting from some height or slope) and working with gravity, or from a running cursor, working against gravity, is still intensely debated. Several modifications of the various evolutionary steps in the main theories also are suggested but particular stress has been laid on whether a gliding stage was included or not, and also on the climbing ability in ancient birds. Bock [20, 21] identified the adaptive advantage of each intermediate stage in the arboreal scenario: ground-living insectivorous proto-birds might have begun to forage among bushes and then to climb trees to escape from predators, to roost at night, or to nest. Powered flight then evolved via gliding from trees. But Caple et al. [27] argued that lift could not be produced when a gliding proto-flier began to flap its wings. Norberg [15–17], however, showed that a transition from gliding to active flight is mechanically and aerodynamically quite feasible. By using aerodynamic and optimal foraging theories Norberg showed that, for every step along the hypothetical route from gliding, through stages of incipient flapping, to fully powered flight, there would have been an advantage over previous stages in terms of length and control of the flight path. Asymmetric wing movements would then have been used for slight manoeuvring to correct the glide path. Later, slight flapping was used for the production of thrust. Palm [28] and Homberger and de Silva [29] suggested a variation of the arboreal theory, namely that flight in birds evolved from small arboreal lizards, who were leaping between trees and stretching out their forelimbs before head-up landing on a stem. Increased forelimb area would decrease the braking speed before landing, leading to larger wings. Burgers and Chiappe [30] and Burgers and Padian [31] proposed that the generation of thrust, not lift, was of paramount importance in the origin of bird flight. This is indeed exactly the most important point in Norberg’s [15] detailed aerodynamic model, namely that thrust is produced in a gliding animal with slight flapping, and Rayner [24] also suggested that thrust had to be produced during gliding to flatten out the glide path. Norberg showed mathematically that a net thrust force can be produced even during very slight flapping in a gliding animal while the necessary vertical lift is still produced, resulting in a shallower glide path. Furthermore, an animal (or aircraft) cannot fly unless a lift force, which counteracts gravity, is produced and the simplest way for the proto-bird to attain lift when the wings were still small was to use steep glides from some height. The rival cursorial theory, or ‘ground-up’theory, holds that birds evolved from ground-running and jumping proto-birds which ended up as active fliers without a gliding intermediate stage [27, 32–37]. This theory includes various ideas about the intermediary forms. However, the step from a ground-running and jumping mode of life to active flight seems very difficult because the proto-bird had to work against gravity [15, 23]. In the running animal the aerodynamic drag from extended flapping forelimbs would increase with speed squared and retard it, requiring still more work to reach the speed needed to generate the lift and thrust required for take-off. Longer forelimbs and feathers would further have increased drag and the work necessary for the same speed. Such a proto-flier, that was supposed to flap its wings to add to the running speed and/or for stability and control of the body, must produce not only the power necessary for flapping but also the power needed to run near take-off speed during the intermediate evolutionary stages. This power argument identifies a formidable obstacle to the origin of flight from a cursorial habit.

Gliding animals work with gravity and do not suffer from this negative feedback system, and by gliding reach a high forward speed almost gratis before they begin to flap. The ground-up model for flight evolution may, under certain circumstances, be acceptable but it includes a number of limitations. Neglecting the wing drag, it may be energetically cheaper to run–leap–glide than to run continuously, with the savings increasing for smaller animals [38]. This would thus make sense for an animal running with retracted wings and making regular intermittent leaps followed by shallow glides on extended wings. The savings are, however, much less than those realized in the trees-down scenario. But modern cursorial animals seldom travel so fast in commuting runs; they usually reach only half the speed necessary for take-off. It seems unlikely that the animals had reason to travel so fast except to escape predators, but since each leaping– gliding event involves some deceleration, continuous running would be a better choice [15]. Burgers and Padian [31] proposed that running proto-birds received lift from the ground effect when flapping their wings extensively to produce thrust, but there are some limitations with this scenario [26]. First, thrust is an effect of the resultant aerodynamic force produced, or merely the horizontal, forwardly directed, component of the resulting force from the flapping wings, and cannot be produced independently of lift during flight in air. The vertical component of this resultant is the lift force counteracting gravity. Second, in animals and aircraft flying or hovering close to the ground or water there is an interaction of the vortices on the wings and in the bird’s (or aircraft’s) wake with ground plane. For fixed wings this is modelled by an equal and opposite image-vortex system with no flow normal to the ground plane. For flapping wings this flow may not be steady and inviscid, and the ground boundary layer may separate [39]. The main benefit when flying close to the ground is savings in the induced drag but reducing lift per unit circulation [40]. To produce the vertical lift balancing the weight the animal must increase circulation in ground effect to compensate for the reduced relative airstream owing to the image of the ground effect [39]. Rayner [39] suggested that modern birds supinate (rotate upwards) their wings for this purpose, but proto-birds had limited possibilities for this. The induced drag component becomes a smaller part of the total drag at those high speeds proposed for the running proto-bird. Since total drag increases with speed squared, it is difficult to see how the lift-to-drag ratio could have gradually increased during the evolutionary stages in this scenario [26]. In terms of energy, time, and aerodynamics, the gliding hypothesis seems to be the most attractive alternative [15–17], but arguments are raised about structural limitations in the early proto-birds. Rayner [41], however, demonstrated that the evolution of powered flight through a gliding wing is entirely consistent with the existing fossil record of birds, and that this hypothesis makes few demands on the behaviour and paleobiology of proto-avians.

3.2 Probable steps in the evolution of bird ﬂight

Probable steps and the adaptive advantage of each microevolutionary change that led to the macroevolutionary change from reptile to bird are summarized in Table 1.

3.2.1 Foraging agility The first steps towards aerial locomotion were probably taken from trees or cliffs. Tree-climbing and clinging among branches and leaves in insectivorous proto-birds would have required better control of movements with accompanying improvements in sense organs, neuromuscular control and external morphology [20]. These adaptations increased foraging agility, decreased the risk of being eaten, and thus increased fitness. Similar adaptations may also have occurred in proto-birds moving around on cliffs or steep slopes. Hang-gliding proto-birds would also have benefited from a good running behaviour.

Table 1: Probable steps in the evolution of ﬂight in birds.

Locomotion Goal Adaptations

1. Climbing Foraging, Climbing agility [running] avoiding predators [running agility] 2. Parachuting (steep gliding); More effective foraging, Larger forearm surface [hang-gliding] avoiding predators (propatagium, feathers) 3. Gliding Optimal foraging Larger wings, movements between lower wing loading foraging areas 4. Gliding with some Ability to determine Neuromuscular control, manoeuvrability direction of the glide wing coordination, wing camber 5. Slight flapping flight Movements for stability, Higher aspect ratio, manoeuvres in turning lower wing loading and landing 6. Flapping flight with Better flight performance, Better neuromuscular some manoeuvrability commuting control, more sophisticated wing characters, camber for slow flight 7. Flapping flight with Aerial prey-catching, Highly sophisticated wing high manoeuvrability hovering etc. characters (slots), keeled sternum, musculoskeletal system like that of modern birds

3.2.2 Feathers and gliding surface Extensions of skin would be useful as parachutes if the animal fell or needed to escape. The skin flap in front of the arm skeleton of the bird wing may have originated for this purpose. Different hypotheses have been presented about the evolution of feathers. Bock [42] suggested that feathers developed as insulating devices, and that development of elongated feathers would have reduced the rate of fall and promoted safe landings. Elongated feathers on the forearms could later have acted as gliding surfaces and eventually been developed into primary feathers that give thrust in flapping flight. Another theory is that feathers evolved directly for gliding flight [22]. But Xu et al. [43] reported evidence for proto-feathers in a new basal tyrannosauroid from China; one of the specimens preserves a filamentous integumentary covering, similar to that of other coelurosaurian theropods from western Liaoning, which provides the first direct fossil evidence that tyrannosauroids already had proto-feathers. The authors suggested that this supports the theory that feathers evolved as insulating devices.

3.2.3 Gliding Climbing and gliding may have been used as main types of locomotion during foraging in the early proto-birds. Maximization of net energy gain during foraging in trees might have been a reason for strong selection for increased gliding performance [44, 45]. It costs less energy and

Figure 2: Top: Energy-saving mode of locomotion, which may have been used by arboreal pre- decessors to vertebrate fliers [44, 45]. It costs less energy to climb upwards and then glide down to the next tree than to climb up and down a tree and then run to the next (middle). Hang-gliding (bottom) may be a possible evolutionary stage in the evolution of bird flight [26]. Top and middle figures from [17], courtesy of Springer-Verlag. takes less time to climb up a tree and glide to the next during foraging than to climb up and down each tree and then run to the next tree (Fig. 2). This locomotion mode is used, for example, by woodpeckers, treecreepers, and gliding mammals. Once a glide surface had evolved, the proto- birds’ energy and time demands for locomotion during foraging might have been considerably reduced and their foraging efficiency improved. Because the glide surface was small in the initial stages, the first glides must have been steep with low lift-to-drag ratios. But even steep parachuting jumps from trees (or other heights) reduced the time and energy required for foraging and also permitted the animal to escape predators better. Even a squirrel without a glide membrane leaps among branches and trees and spreads whatever it has to glide on. Such behaviour strongly promotes every incipient skin, hair or feather area for gliding purposes. Zhang and Zhou [46] described the fossil of an enantiornithine bird from the early Cretaceous that has substantial plumage feathers attached to its upper leg (tibiotarsus). They suggested that these feathers, that are curved and relatively long, may be remnants of aerodynamic feathers, in

WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) Evolution of Flight in Animals 43 accordance with the hypothesis that birds went through a four-winged stage during the evolution towards ﬂight [47]. Remnants of leg feathers occurred also in the gliding dinosaur Microraptor [47] and in Archaeopteryx [12].

3.2.4 Hang-gliding Aerodynamically, the hang-gliding scenario is quite possible [26]. The gliding proto-birds then worked with gravity, not against it. The gliding could have started from a running behaviour, which ﬁts in with the ideas of believers of the ground-up theory that proto-birds were ground-dwellers. The problem whether proto-birds could climb trees or not (see below) is then eliminated. Hang-gliding could have begun as a foraging behaviour (Fig. 2, bottom). The proto-bird would not only have got a better overview of the foraging area by gliding over it, but it may also have been easier to surprise a prey (such as some insect or small reptile) from above than when chasing it on ground. When diving down with retracted wings the proto-bird could hit the prey with its own weight, and thus easier kill or paralyse the prey, like many hovering birds of prey and jumping mammals (such as foxes) do.

3.2.5 Stability and neuromuscular control A gliding animal needs good control of movements to be able to retain or adjust flight direction and gliding angle to reach a particular destination. Some characters needed for control and stability may have occurred in the early gliders, as they do among modern gliding animals. The selection pressure for good control and manoeuvrability in the gliding proto-flier may have evolved stepwise and progressively along with the capability of gliding. This includes not only the evolution of larger wings but also wing movement coordination, such as twisting and retraction, following the evolution of better neuromuscular control. True gliding must have been used only for commuting, prey capture on ground or escape and not for catching insects or other animals in air, which would require higher manoeuvrability, which could not have evolved until true flight was well established. Stability and control of movements could/can easily be obtained in several ways (Fig. 3,Table2). The flight of the earliest birds, pterosaurs, bats and flying insects were probably inherently stable, owing to their structural design, whereas they lacked the highly evolved sensory and nervous system required for neuromuscular stability control [48]. Without the inherent self-stability gov- erned by their structure they would have been unable to fly. With increasing evolution of the neuromuscular system, the structurally conditioned stability found in earlier forms became less important, for modern birds do not need to be inherently stable in order to fly. Instead, insta- bility gives higher manoeuvrability, which is of great advantage not only for insectivorous birds and birds of prey but also for flying prey. However, stability is sometimes needed in extant fliers.

3.2.6 Flapping From the beginning, slight flapping was probably used as movements for stability and for manoeuvres in turning and landing. When flapping became more powerful it could also be used to increase the glide path length by providing thrust [15]. This would make locomotion between foraging sites more efficient both in terms of speed and energy savings. Increased wing area reduced wing loading (weight/wing area) and gliding speed, allowing safer landings. Elongation of the wings increased aspect ratio (wingspan2/wing area; a measure of wing shape and aerodynamic efficiency) and lift-to-drag ratio (L/D), resulting in shallower glides. Slight flapping resulted in the production of thrust, used to flatten out the glide, and

(a)

(b) (c)

Figure 3: (a) Pitch, roll and yaw planes. (b) Dihedral angle of the wings controlling roll moments, resulting in roll stability. A roll to the left (left wing down) would increase lift L on the left wing and decrease lift on the right wing because of the higher angle of attack on the left wing. The force difference between the wings will lift the left wing again and restore the bird to the horizontal. (c) Partial retraction of the left wing decreasing left wing and thus lift. L and L are the lift forces and Lv and Lv are their vertical lift components. The positions of the wings are in the middle of the downstroke. Modiﬁed from [17], courtesy of Springer-Verlag.

this, together with the ability to coordinate the movements, eventually led to fully powered horizontal flight. Radiation to different habitats led to different wing forms, and the evolution of more sophisticated wing characters improved the aerodynamic performance (points 6 and 7 in Table 1). There would have been no problems with the transition from gliding to flapping flight in terms of vorticity patterns [3]. For a proto-bird the size of Archaeopteryx with a wingspan of 60 cm and a glide speed of about 7 m/s the wingbeat must be about 6–7 strokes/s [15, 16], given that the duration of the downstroke equals that of the upstroke. However, if the proto-bird had beaten its wings faster during the upstroke than during the downstroke, the wingbeat frequency could be reduced to 2 strokes/s [15, 16]. This flapping behaviour can be seen in, e.g. the Red-Tailed Cockatoo (Calyptorhynchus banksii) in Australia (own observation). Furthermore, Norberg’s [15] model shows that the wingstroke amplitude increases almost linearly with the flapping speed and that it is small at low speeds.

Table 2: Different ways of obtaining stability and control of movements in ﬂying and gliding animals and early forms with slight ﬂapping.

Pitch stability and control (about the body’s transverse axis): Structural adaptation and neuromuscular control 1. A long, sturdy, dorsoventrally flattened tail (as in Archaeopteryx) 2. Downward and upward movements of the tail 3. Fore and aft movements of the wings relative to the centre of gravity Roll stability and control (about the longitudinal axis): Structural adaptation and neuromuscular control 1. Long, broad wings with rounded tips 2. Sweepback and upward deflection of the wings (dihedral) creates restoring moments upon sideslip 3. Twisting the wings in different directions (different angles of attack and hence different amount of lift on the two wings) Yaw stability and control (about the vertical axis): Structural adaptation and neuromuscular control 1. Long, broad wings with rounded tips 2. Tail movements 3. Twisting and flexing the wings to change the drag coefficient

3.2.7 Did proto-birds climb trees? An important question for understanding the origin of bird flight from arboreal ancestors is whether or not proto-birds could climb. Archaeopteryx seems to have been a good bipedal runner [36]. But the free claws on the hands in early birds suggest that they also were climbers [49]; the curvature of the claws of Archaeopteryx is similar to that of modern tree-climbing and perching birds [50]. The young of the hoatzin, which is the only modern bird with claws on free fingers, are bush- and tree-climbers. However, Burgers and Padian [31] argued that highly curved claws would also be positive for cursorial proto-birds by providing constant grip during running. Ruben [51] suggested in a compromise that Archaeopteryx may have been able to alternate easily and quickly between terrestrial and arboreal environments. The basilisc (Basiliscus vittatus) is an example of a very fast-running quadrupedal reptile that can even run over water surfaces to escape predators and climb trees. Furthermore, as mentioned above, a good running ability is compatible with the hang-gliding theory [26]. Arnold [52] concluded that Archeopteryx was unlikely to have used its forelimbs for climbing, but that this is not necessarily excluded for the first fliers. Arnold further suggested that the posteriorly directed thumb of birds indicates a climbing or perching phase around the time when flight evolved. Another argument against the trees-down theory has been the lack of trees in the Solnhofen Limestones (Upper Jurrasic) where all fossils of Archaeopteryx have been found [53]. However, the absence of larger trees does not preclude the origin of flight from arboreal proto-birds, for flight evolution may have been initiated much earlier when the flora was different, or even in other areas. They may also have evolved flight through gliding from other heights or in steep slopes (as suggested above), which would include similar steps with a gliding intermediate. In conclusion, whether or not proto-birds could climb trees is not an interesting question in arguments against the gliding theory.

3.2.8 Did Archaeopteryx fly? Whether Archaeopteryx were capable of powered flight or if they were only advanced gliders is not a simple question. Dominiquez Alonso et al. [54] used computed tomography of the brain and inner ear of Archeopteryx and concluded that this bird had acquired the derived neurological and structural adaptations necessary for flight. Regression analysis shows that the brain volume of Archaeopteryx was between those for modern birds and Diapsid reptiles and archeosaurs. An enlarged forebrain suggests that it had also developed enhanced somatosensory integration needed for a flying behaviour [55]. Archaeopteryx lacked advanced muscular and skeletal characters and the stamina and locomo- tory endurance of modern birds [56]. Osteology of the pectoral girdle indicates that the upstroke was powered primarily by the deltoid muscle [57]. The lack of a morphologically derived supracoracoideus muscle and the skeletal features associated with it, means that Archaeopteryx were apparently incapable of high-velocity rotation of the humerus about its longitudinal axis during the upstroke [56–60]. During the evolution of the avian shoulder the surface of the shoulder-joint (glenoid) under- went a major reorientation from the primitive condition of being directed backwards–downwards to being directed upwards–outwards as in modern birds. In Archaeopteryx the laterally facing glenoid of the shoulder joint was intermediate in orientation between ancestral reptiles and modern birds and provided for a substantial degree of wing elevation. Thus, Archaeopteryx could elevate wings well above the horizontal plane through the shoulder, preparatory to a lift-producing downstroke [58]. The presence of a semilunate wrist-bone (a reptilian character) in Archaeopteryx may have served for automatic supination of the hand [61, 62]. The downstroke was powered by M. pectoralis. It has often been argued that the pectoral muscle was too small for powered flight in Archaeopteryx, because its sternum (breast-bone) lacked a keel. However, the main function of a bony keel of the sternum may not have evolved as a need for increased area of attachment, but to prevent internal air cavities of the pectoral muscles from collapsing when the muscles contract [25]. In modern birds these muscles contain air cavities which are connected to the interclavicular air sacs, providing internal evaporation surfaces for heat without the intervention of the blood stream. In bats, the heat is removed from the muscles primarily by the blood and they lack an ossified sternum keel. Instead bats have a keeled, ossified manubrium of the fore part of the sternum from which a ligamentous sheet extends backwards in the median plane and acts as an increased surface area for the origin of the flight muscles [63]. In Archaeopteryx an additional surface of origin for this muscle may have been formed by the sternum, the clavicles and coracoid bones in the pectoral girdle, the ribs, and ligaments connecting these skeletal elements (as in modern birds) thus providing a relatively large area of attachment. The seventh specimen of Archaeopteryx had an ossified sternum [64], suggesting that the pectoral muscle was not too small for powered flight. Martin [65] reported that Archaeopteryx had a completely avian wrist with four carpal bones, although the typical V-shape of the cuneiform bone was not established, and that the morphology ‘provides direct evidence for the avian motion of the manus [hand] on the radius-ulna [forearm]’. Vazquez [61] compared the wrist of modern birds with that of Archaeopteryx and concluded that Archaeopteryx lacked most of the key features associated with manoeuvrable and advanced flight. He showed elegantly how the wrist in mallard ducks are highly specialized to meet forces during flapping flight; the carpometacarpal bones are formed in such a way that they prevent twisting movements of carpometacarpus, providing a rigid structure. Vazques suggested that this mechanism prevents hyperpronation (extreme downward rotation) during the downstroke in flapping flight and supination (upward rotation) during gliding flight. However, the aerofoil action does not usually function in the way described by Vazquez, so the risk of hyperpronation in the

WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) Evolution of Flight in Animals 47 downstroke is minimal. Neither does any airstream usually meet the upper side of the wings during gliding, causing supination as he suggested. No turbulence above the wings may be strong enough to provide such forces. The problem instead, for a proto-bird like Arcaheopteryx was to obtain overall rigidity in the wing. Rigidity in the arm wing was obtained by the angling of humerus (upper arm) vs. radius-ulna, as in modern birds [17, 66], and rigidity in the hand wing could have been maintained by ligaments in the wrist, as in modern bats (and pterosaurs?). Pennycuick [25] and Ruben [51] suggested that Archaeopteryx could have been ectothermic, like reptiles. This permits only relatively minimal aerobic capacity which may have restricted Archaeopteryx to anaerobically powered, flapping flight of relatively short distance and duration. They would also have been capable of upward take-off from standstill as well as achieving powered flight with less than one-half of the flight-muscle volume of modern birds [51, 67]. Many modern reptiles seem capable of generating particularly high levels of anaerobically supported mechanical power during short bursts [68]. Ruben [51] further suggested that the evolution of avian endothermy is likely to have been accompanied by the development of enlarged flight muscles composed of aerobic muscle fibres for sustained flight. The absence of a sternal crest and a calcified sternum, a simple pectoral girdle similar to that of non-flying theropods (the reptilian ancestors to birds), and with a lateral-facing glenoid (the joint between the upper arm and the shoulder), the downstroke is regarded to be rather weak and dorsoventral, and with little pronation [41]. Based on the inability to produce a rapid upstroke with supinated wings, and on the fact that the downstroke was poor and dorsoventral, Rayner concluded that Archaeopteryx were incapable of slow flight and more adapted for fast cruising flight, with low agility and manoeuvrability. O’Farrell et al. [69] suggested that Archaeopteryx relied substantially on lift enhanced by ground effect. Advanced flight feather characteristics with aerodynamic function, such as vane asymmetry [70], dorsoventral stiffening [71], and backward curvature [72] (Fig. 4), were present in Archaeopteryx. Thus, as in modern birds, Archaeopteryx had the structural asymmetry of the flight feather that are essential for automatic adjustment of the feathers for optimal angle of incidence throughout the wingbeat cycle, despite continuously varying directions and velocities of the relative wind. Vane asymmetry and dorsoventral stiffening indicate that Archaeopteryx were

(a) (b)

Figure 4: (a) The wing of Archaeopteryx lithographica. (b) Automatic separation of hand-wing feathers, forming wing-tip slats. Modiﬁed from [72].

WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) 48 Flow Phenomena in Nature fairly advanced fliers, although these feather characteristics would also be beneficial for a manoeuvrable glider. However, it seems unlikely for flight feathers to have been so strongly curved in a pure glider as it indeed was in Archaeopteryx [72, 73]. Feather asymmetry is highly beneficial for both manoeuvrability and flapping flight, which evolved step-by-step and most probably simultaneously [15–17]. The leading-edge feathers in Archaeopteryx show the curvature that is a prerequisite for the automatic adjustment of angles of incidence at the primaries throughout the downstroke, provided that they separate [72]. Four primary feathers of increasing length made up the leading edge, an ideal arrangement for their separation towards the tip to function as leading- edge slats (Fig. 4). Such slats are high-lift devices, important at take- off when the speed is so low that most of the relative air speed must be achieved by flapping. Archaeopteryx had a wing loading and aspect ratio similar to the “average” modern bird [17], and may thus have been able to use weak, powered cruising flight with some manoeuvrability. It may have used a few wingbeats per second and it may also have used flap-gliding. A ladder or concertina vortex wake may have been produced during flapping, which may have been some intermediate form between line vortices and vortex rings in the evolution of flapping flight [15]. The wing characteristics in Archaeopteryx can be summarized into three crucial points:

1. Archaeopteryx seemed to lack a morphologically derived supracoracoideus muscle to produce a rapid humeral rotation and upstroke, instead, the deltoid muscles may have worked to elevate the wings [58]. However, a rapid upstroke may not have been needed [15, 16]. The presence of a semilunate carpal in the wrist may have served for some automatic supination (upward rotation) of the hand and metacarpus [61]. 2. The wing feathers of Archaeopteryx had stiffened rachis [71], vane asymmetry [70], the structural asymmetry and curved shafts essential for automatic adjustment of the feathers for optimal angles of incidence throughout the wingbeat cycle [72], and the primaries could separate to form wing slots, which can be used as high-lift devices during take-offs [72]. 3. Archaeopteryx had a wing loading and aspect ratio similar to the ‘average’ modern bird [17], and may thus have been able to use weak-powered, cruising, ﬂight with some manoeuvrability.

3.2.9 Other fossil birds A number of new birds from the early Cretaceous have recently been described [74–79], which lend insight into the understanding of the evolution of birds and bird flight and of the flight capabilities of ancient birds. Fossil birds from Late Jurassic and Early Cretaceous demonstrate a number of advanced characteristics that signal an evolutionary progress towards powered flight [60]. Early Cretaceous birds were the first to have a keeled sternum, a strap-like coracoid, and hypocleidium- bearing furcula (the ‘wishbone’ formed by the two clavicles), characters that are characteristic of modern birds. Caudal reduction, reducing overall weight, took place before the evolution of flight and an increase in tail base flexibility can be observed in the evolution of birds [80].

3.3 Evolution of pterosaur and bat ﬂight

Powered flight in pterosaurs and bats most probably evolved via gliding in tree/rock-living animals [15, 17, 23], with the same steps towards flight as described for birds in Table 1. The aerodynamic model presented by Norberg [15, 17] applies to all three flying vertebrate groups. Proto-bats might have been tree-living omnivorous mammals.Adaptations for downward climbing would have required outward and backward directed hind legs as seen in modern bats [23]. The glide membrane might have been outstretched by the four legs and a long tail, like in most microchiropteran bats.

4 Conclusion

Norberg [17] wrote in her book Vertebrate Flight: ‘the behaviour of ancient animals and the evolution of flight will probably always be a subject of contention, and although we may never know for certain if we have found the right answers, we can always distinguish the possible from the impossible, the probable from the improbable’. From aerodynamic considerations, gliding most probably preceded flapping. The animal then worked with gravity, not against it, as in upward leaps from the ground. Norberg’s [15] aerodynamic model applies to the transition from gliding to powered flight regardless of whether gliding occurred from trees or some other elevation, or even followed from short glides in steep slopes (hang-gliding; [26]). With the running–hang-gliding scenario the problem whether proto-birds could climb trees or not is eliminated. Archaeopteryx possessed several characters important for flight. Its osteology, myology and wing form indicate that it was capable of flapping flight. The specific geometry and morphology of the hand-wing feathers are certainly a result of aerodynamic demands; they show a striking similarity with those of modern flying birds. Although some of the flight characteristics were not highly advanced, the available evidences, taken together, indicate that Archaeopteryx was not only a good manoeuvrable glider but also capable of powered flight, even though it may not have been an advanced flapper.

References

[1] Thomas, A.L.R. & Norberg, R.Å., Skimming the surface—the origin of flight in insects? Trends in Ecology and Evolution, 11, pp. 187–188, 1996. [2] Flower, J.W., On the origin of flight in insects. Journal of Insect Physiology, 10, pp. 81–88, 1964. [3] Ellington, C.P.,Limitations on animal flight performance. Journal of Experimental Biology, 160, pp. 71–91, 1991. [4] Brodsky, A.K., The Evolution of Insect Flight, Oxford University Press: Oxford, 1994. [5] Norberg, R.Å., Evolution of flight in insects. Zoologica Scripta, 1, pp. 247–250, 1972. [6] Wigglesworth, V.B., Origin of wings in insects. Nature, 197, pp. 97–98, 1964. [7] Kingsolver, J.G. & Koehl, M.A.R., Aerodynamics, thermoregulation, and the evolution of insect wings: differential scaling and evolutionary change. Evolution, 39, pp. 488–504, 1985. [8] Marden, J.H. & Kramer, M.G., Surface-skimming stoneflies: a possible intermediate stage in insect flight evolution. Science, 266, pp. 427–430, 1994. [9] Marden, J.H. & Kramer, M.G., Locomotor performance of insects with rudimentary wings. Nature, 377, pp. 332–334, 1995. [10] Kukalová-Peck, J., Origin and the evolution of insect wings and their relation to meta- morphosis, as documented by the fossil record. Journal of Morphology, 156, pp. 53–126, 1978. [11] Kukalová-Peck, J., Origin of the insect wing and wing articulation from the arthropodan leg. Canadian Journal of Zoology, 61, pp. 1618–1669, 1983. [12] Feduccia, A., The Origin and Evolution of Birds, Yale University Press: New Haven and London, 1996. [13] Gauthier, J. & Gall, L.F., (eds.) New Perspectives on the Origin and Early Evolution of Birds, Peabody Museum of Natural History, Yale University: New Haven, 2001.

[14] Marsh, O.C., Odontornithes: A Monograph on the Extinct Toothed Birds of North America. Report of the US Geological Exploration of the 40th Parallel, Vol. 7, Government Printing Office: Washington, DC, 1880. [15] Norberg, U.M., Evolution of vertebrate flight: an aerodynamic model for the transition from gliding to flapping flight. American Naturalist, 126, pp. 303–327, 1985. [16] Norberg, U.M., Evolution of flight in birds: aerodynamic, mechanical and ecological aspects. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer. Proc. Int. Archaeopteryx Conf. Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 293–302, 1985. [17] Norberg, U.M., Vertebrate Flight: Mechanics, Physiology, Morphology, Ecology and Evolution, Zoophysiology Series, Vol 27, Springer-Verlag: Berlin and New York, 1990. [18] Darwin, C., The Origin of Species, J. Murray: London, 1859. [19] Heilmann, G., The Origin of Birds, Witherby: London, 1926. [20] Bock, W., The role of adaptive mechanisms in the origin of higher levels of organization. Systematic Zoology, 14, pp. 272–287, 1965. [21] Bock, W., The arboreal origin of avian flight. The Origin of Birds and the Evolution of Flight, ed. K. Padian, California Academy of Science: San Francisco, pp. 57–72, 1986. [22] Feduccia, A., The Age of Birds, Harvard University Press: Cambridge, MA, 1980. [23] Norberg, U.M., On the evolution of flight and wing forms in bats. Bat Flight-Fledermausflug, ed. W. Nachtigall, Biona Report 5, Fischer: Stuttgart, pp. 13–26, 1986. [24] Rayner, J.M.V., Mechanical and ecological constraints on flight evolution. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P.Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 279–288, 1985. [25] Pennycuick, C.J., Mechanical constraints on the evolution of flight. The Origin of Birds and the Evolution of Flight, ed. K. Padian, California Academy of Science: San Francisco, pp. 83–98, 1986. [26] Lindhe Norberg, U.M., Bird flight. Plenary talk at the 23rd International Ornithological Congress, Beijing 2002. Acta Zoologica Sinica, 50, pp. 921–935, 2004. [27] Caple, G., Balda, R.P. & Willis, W.R., The physics of leaping animals and the evolution of preflight. American Naturalist, 121, pp. 455–467, 1983. [28] Palm, S., The Origin of Flapping Flight in Birds, Ballerup, pp. 1–45, 1997. [29] Homberger, D.G. & de Silva, K.N., Functional microanatomy of the feather-bearing integument: implications for the evolution of birds and avian flight. American Zoologist, 40, pp. 553–574, 2001. [30] Burgers, P. & Chiappe, L.M., The wing of Archaeopteryx as a primary thrust generator. Nature, 399, pp. 60–62, 1999. [31] Burgers, P. & Padian, K., Why thrust and ground effect are more important than lift in the evolution of sustained flight. New Perspectives on the Origin and Early Evolution of Birds, eds. J. Gauthier & L.F. Gall, Peabody Museum of Natural History, Yale University: New Haven, pp. 354–359, 2001. [32] Williston, S.W., Are birds derived from dinosaurs? Kansas City Reviews of Science, 3, pp. 457–460, 1879. [33] Nopsca, F., Ideas on the origin of flight. Proceedings of the Zoological Society of London, pp. 223–236, 1907. [34] Nopsca, F., On the origin of flight in birds. Proceedings of the Zoological Society of London, pp. 463–477, 1923.

[35] Ostrom, J.H., Archaeopteryx and the origin of flight. Quarterly Review of Biology, 49, pp. 27–47, 1974. [36] Ostrom, J.H., The cursorial origin of avian flight. The Origin of Birds and the Evolution of Flight, ed. K. Padian, California Academy of Sciences: San Francisco, pp. 73–81, 1986. [37] Padian, K., Running, leaping, lifting off. The Sciences, pp. 10–15, May/June, 1982. [38] Rayner, J.M.V., Cursorial gliding in proto-birds: an expanded version of a discussion contribution. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura- Museums: Eichstätt, Willibaldsburg, pp. 289–292, 1985. [39] Rayner, J.M.V., On aerodynamics and the energetics of vertebrate flapping flight. Fluid Dynamics in Biology, eds. A.Y. Cheer & C.P. van Dam, Contemporary Mathematics, 141, American Mathematical Society Providence, pp. 351–400, 1993. [40] Betz, A., Applied airfoil theory. Aerodynamic Theory, Vol. 4, ed. W.F. Durand, Dover: New York, pp. 1–129, 1963. [41] Rayner, J.M.V., On the origin and evolution of flapping flight aerodynamics in birds. New Perspectives on the Origin and Early Evolution of Birds, eds. J. Gauthier & L.F. Gall, Peabody Museum of Natural History, Yale University: New Haven, pp. 363–385, 2001. [42] Bock, W., On extended wings: another view of flight. Sciences, 23, pp.16–20, 1983. [43] Xu, X., Norell, M.A., Kuang, X., Wang, X., Zhao, Q. & Jia, C., Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature, 431, pp. 680–684, 2004. [44] Norberg, R.Å., Why foraging birds in trees should climb and hop upwards rather than downwards, Ibis, 123, pp. 281–288, 1981. [45] Norberg, R.Å., Optimum locomotion modes for birds foraging in trees. Ibis, 125, pp. 172– 180, 1983. [46] Zhang, F. & Zhou, Z., Leg feathers in an early Cretaceous bird. Nature, 43, p. 925, 2004. [47] Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F. & Du, X., Four-winged dinosaurs from China. Nature, 421, pp. 335–340, 2003. [48] Maynard Smith, J., The importance of the nervous system in the evolution of animal flight. Evolution, VI(1), pp. 127–129, 1952. [49] Yalden, D.W., Forelimb function in Archaeopteryx. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 91–97, 1985. [50] Feduccia, A., Evidence from claw geometry indicating arboreal habits of Archaeopteryx. Science, 259, pp. 790–793, 1993. [51] Ruben, J., Reptilian physiology and the flight capacity of Archaeopteryx. Evolution, 45, pp. 1–17, 1991. [52] Arnold, E.N., Methods inferring unknown aspects of organisms and the behavioral origins of bird flight. New Perspectives on the Origin and Early Evolution of Birds, eds. J. Gauthier & L.F. Gall, Peabody Museum of Natural History,Yale University: New Haven, pp. 195–210, 2001. [53] Viohl, G., Geology of the Sohnhofen lithographic limestones and the habitat of Archaeop- teryx. The Beginnings of Birds. eds, M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 31–44, 1985. [54] Dominiquez Alonso, P., Milner, A.C., Ketcham, R.A., Cookson, M.J. & Rowe, T.B., The avian nature of the brain and inner ear of Archaeopteryx. Nature, 430, pp. 666–669, 2004. [55] Schimizu, T., Evolution of the forebrain in tetrapods, Brain Evolution and Cognition, eds. G. Roth, & M.F. Wulliman, Wiley: New York, pp. 135–184, 2001.

[56] Ostrom, J.H., Poore, S.O. & Goslow, G.E, Jr., Humeral rotation and wrist supination: important functional complex for the evolution of powered flight in birds? Paleontology at the close of the 20th century: Proc. of the 4th Int. Meeting of the Society of Avian Paleontology and Evolution, Washington, DC, 4–7 June 1996, ed. S.L. Olson, Smithsonian Institute Contributions to Paleontology, Vol. 89, pp. 301–309, 1999. [57] Ostrom, J.H., Some hypothetical anatomical stages in the evolution of avian flight. Smithsonian Contribution to Paleobiology, 27, pp. 1–21, 1976. [58] Jenkins, F.A., The evolution of the avian shoulder joint. American Journal of Science, 293A, pp. 253–267, 1993. [59] Poore, S.O., Sánchez-Haiman, A. & Goslow, G.E., Jr., Wing upstroke and the evolution of flapping flight. Nature, 387, pp. 799–802, 1997. [60] Poore, S.O., Ashcroft, A., Sánchez-Haiman, A. & Goslow, G.E., Jr., The contractile pro- perties of the M. supracoracoideus in the pigeon and starling: a case for long-axis rotation of the humerus. Journal of Experimental Biology, 200, pp. 2987–3002, 1997. [61] Vazquez, R.J., Functional osteology of the avian wrist and the evolution of flapping flight. Journal of Morphology, 211, pp. 259–268, 1992. [62] Vazquez, R.J., The automating skeletal and muscular mechanisms of the avian wing (Aves). Zoomorphology, 114, pp. 59–71, 1994. [63] Norberg, U.M., Functional osteology and myology of the wing of Plecotus auritus Linnaeus (Chiroptera). Ark. Zool., 22, pp. 483–543, 1970. [64] Wellnhofer, P., Das Siebte Exemplar von Archaeopteryx aus den Solnhofener Schichten. Archaeopteryx, 11, pp. 1–47, 1993. [65] Martin, L.D., Mesozoic birds and the origin of birds. Origins of the Higher Groups of Tetrapods: Controversy and Consensus, eds. Schultze, H.-P., Trueb, L. Cornell University Press: Ithaca, pp. 485–540, 1991. [66] Norberg, U.M., Bat wing structures important for aerodynamics and rigidity (Mammalia, Chiroptera). Z. Morphol. Tiere, 73, pp. 45–61, 1972. [67] Ruben, J., Powered flight in Arcaheopteryx: response to Speakman. Evolution, 47, pp. 935– 938, 1993. [68] Bennett,A.F. & Ruben, J.A., Endothermy and activity in vertebrates. Science, 206, pp. 649– 654, 1979. [69] O’Farrell, B., Davenport, J. & Kelly, T., Was Archaeopteryx a wing-in-ground effect flier? Ibis, 144, pp. 686–688, 2002. [70] Feduccia, A. & Tordoff, H.B., Feathers of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science, 203, pp. 1021–1022, 1979. [71] Rietschel, S. Feathers and wings of Archaeopteryx, and the question of her flight ability. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 249–260, 1985. [72] Norberg, R.Å., Function of vane asymmetry and shaft curvature in bird flight feathers; inference on flight ability of Archaeopteryx. The Beginnings of Birds, eds. M.K. Hecht, J.H. Ostrom, G. Viohl & P. Wellnhofer, Proc. of the Int. Archaeopteryx Conf., Eichstätt, 1984, Freunde des Jura-Museums: Eichstätt, Willibaldsburg, pp. 303–318, 1985. [73] Norberg, R.Å., Feather asymmetry in Archaeopteryx. Nature, 374, pp. 221–221, 1995. [74] Zhang, F. & Zhou, Z., A primitive Enantiornithine bird and the origin of feathers. Science, 290, pp. 1955–1959, 2000. [75] Zhou, Z. & Zhang, F., Origin of feathers—perspectives from fossil evidence. Sci. Progr., 84, pp. 87–104, 2001.

[76] Zhou, Z. & Zhang, F., Two new ornithurine birds from the Early Cretaceous of western Liaoning, China. Chinese Science Bulletin, 46, pp. 1257–1264, 2001. [77] Zhou, Z. & Zhang, F., Largest bird from the Early Cretaceous and its implications for the earliest avian ecological diversiﬁcation. Naturwiss., 89, pp. 34–38, 2002. [78] Zhang, F., Zhou, Z., Hou, L. & Gu, G., Early diversiﬁcation of birds: Evidence from a new opposite bird. Chinese Science Bulletin, 46, pp. 944–949, 2001. [79] Mayr, G., Pohl, B. & Peters, S., A well-preserved Archaeopteryx specimen with theropod features. Science, 310, pp. 1483–1486, 2005. [80] Gatesy, S.M., The evolutionary history of the theropod caudal locomotor module. New Perspectives on the Origin and Early Evolution of Birds, eds. J. Gauthier & L.F. Gall, Peabody Museum of Natural History, Yale University, New Haven, pp. 333–347, 2001.