ࡱ> q E`bjbjt+t+ AAZ9]  4FFFFhLlF" W"Y"Y"Y"Y"Y"Y"$P$D&}" " }"   8W"FF W"n#!K" f4 %j^qFF+" On the origin and evolution of flapping flight aerodynamics in birds Jeremy M. V. Rayner School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK Present address: School of Biology, University of Leeds, Leeds LS2 9JT, UK Running Head: Evolution of flapping flight Paper to appear in New Perspectives on the origin and early evolution of birds, ed. J. Gauthier, 2000. Special Papers Yale Peabody Museum With 1 table and 1 figure. Address for correspondence: Professor J.M.V. Rayner, School of Biology, University of Leeds, Leeds LS2 9JT, U.K. Tel: +44 113 233 2873 Fax: +44 113 233 2835 e-mail: J.M.V.Rayner@leeds.ac.uk Address after 1st July 1999: Revised 1st February 2000 Abstract Birds are characterized by the ability to move by active flapping flight. This entails the evolution and refinement of a complex interlinked suite of functional adaptations, some of which are known to have been present in Archaeopteryx, the earliest known flying representative of the bird lineage. A flying bird must control its wing movements so that lift contributes a mean forward thrust in addition to supporting weight. Living birds do this in two ways : in the simplest gait, found in fast forward flight, bound wing vorticity is held constant, with modest changes in wing pitch and with flexure of the wrist. This gait, in which the upstroke is aerodynamically active, is consistent with the semi-lunate carpal and the absence of an elevating supracoracoideus in Archaeopteryx, and is primitive in birds. The more complex vortex ring gait, typical of slow flight, is energetically and morphologically more demanding. With its highly flexed and aerodynamically passive upstroke, it is more derived, but evolved rapidly in the avialan radiation in birds, as evidenced by the loss of the tail, the appearance of the alula and the evolution of modern wing tip shapes in Lower Cretaceous birds. Morphological differences between confuciusornithid, enantiornithid and ornithurine birds are indicative of at least two independent radiations during the Mesozoic, with separate modifications of the flight system; ornithothoracine (enantiornithid plus ornithurine) birds were characterized by coevolution of wings and tail for propulsion and control, but confuciusornithids performed both functions with the wings. Introduction Many animals use the aerial medium for locomotion or part of their life cycle. A very diverse range of organismsfrom ballooning spiders to numerous lineages of gliding tetrapodsuse the air for movement, but all of these are passive, relying on the force of gravity or on the movements of the air for their travel. Flying animals are able to generate all or most of the force they need for locomotion by using their wings, and only four groups of animalsinsects, pterosaurs, birds and batshave developed flight as their primary means of locomotion. It is the nature of the evolutionary response to the forces acting on an animal moving in air which defines true flight. Although the most obvious of these forces is the relatively large vertical force which acts against gravity, the more challenging force for an animal to generate is the thrust which propels it forwards against drag. For the purpose of studying flight evolution, I define flight in animals as the ability to generate a useful forward thrust or propulsive force by flapping the wings (Rayner 1991a). The key point is the forward thrust, which as I shall explain here demands not only the evolution of wings, but also the ability to move those wings in a controlled manner. It is the convergent evolution of this particular biomechanical capability that links the four lineages of flying animals. The suite of characters which identify this form of locomotion should include the apomorphies of the various flying clades. In this essay I explore how contemporary studies of flapping flight aerodynamics and biomechanics illuminate the problem of the evolution of birds, and make it possible to define the characters expected to be associated with flight. I do not set out here to review the extensive literature on the evolution of bird flight, to explore all aspects of flight biomechanics and aerodynamics, or to summarize all of the many hypotheses which have been advanced. These are matters I have addressed elsewhere (Rayner 1988a, 1991a), and which are considered by other contributors to this volume. The older literature on bird and flight evolution was summarized by Stephan (1987); see also papers in Hecht et al. (1985); for a recent balanced general review see Dingus & Rowe (1998), and for further summaries see Feduccia (1980, 1996, 1999) and Chatterjee (1997, 1999). I take the above definition of flight as my starting point. This is clearly delineated on a biomechanical basis, and it may not necessarily coincide with any of the recognized clades in bird evolution. It is currently coincident with the Avialae of Gauthier (1986; Gauthier & Padian 1985, 1989) and the Aves of Chiappe (1995; Padian & Chiappe 1998), but this arises largely because the least derived bird as currently accepted is Archaeopteryx, whichas I shall showpossesses at least limited capacity for powered flight, while precursors and the avialan sister group show no features uniquely associated with aerial locomotion. Should greater resolution become available in the fossil record of the origin of birds within theropods, then it should be possible to determine the sequence of acquisition of characters associated with flight, and these may not necessarily match the apomorphies of the flying clade. A case in point is the flight feathers. Archaeopteryx was, until recently, the first animal in the theropodbird lineage to show evidence of feathers, and since its forelimb feathers are morphologically and topographically similar to the flight feathers of extant birds (Heilmann 1916; Heinroth 1923; Rietschel 1985), the possession of feathers was a natural apomorphy of the Avialae. Recently feathers or feather-like integumentary structures have been reported in non-flying theropods, sometimes distant from the avian lineage (Chen et al. 1998; Ji et al. 1998; Xu et al. 1999). Thus possession of feathers is no longer an appropriate avialan character. The apomorphy might be refined to possession of flight feathers able to generate aerodynamic force in flight (or be defined morphologically by fine structure). This in turn requires greater resolution from the fossil record, and highlights the difficulty of identifying the first flying bird even from a hypothetically complete fossil record. The fossil record potentially can, and one hopes in the future will, provide evidence of the morphology of the phylogenetic intermediates in the origin of flapping flight, that is prior to Archaeopteryx (figure 1). From this it should be possible to delineate the intermediate biomechanical, behavioural and autotrophic steps which evolved in parallel to flight morphology. This should have much in common with the recent advances in knowledge of the Upper Jurassic and Cretaceous radiation of flight in birds, to which I return later in this essay. In the absence of a flying proto-avian, many authors have been tempted to develop hypotheses of the morphology and behaviour of such an animal (e.g. Marsh 1880; Williston 1879; Beebe 1915; Reichel 1985; review by Stephan 1987). The debate surrounds the two apparently conflicting arboreal (Darwin 1859; Marsh 1880; and others) and cursorial (Thomas 1879; Williston 1879; von Nopsca 1907, 1923; Ostrom 1974, 1976a, 1979) hypotheses. Particularly persistent have been hypotheses based on the living passive-gliding tetrapods, which normally invoke arboreality. The extent to which these organisms can be informative about the origin of powered flight in birds has attracted considerable debate (the role of gliding in the origin of bats (Pirlot 1977; Rayner 1986, 1991b) seems beyond question in light of the close relationship netweem Dermoptera and megachiropterans, and the good fossil record of gliding in Dermoptera (Beard 1990, 1993; Ducrocq et al. 1992)). Biomechanical arguments addressing the issue of the evolution of flight demonstrate a gliding origin of flight to be persuasive: I and others have shown that derivation of useful force from proto-flapping is straightforward to understand for an animal with pre-adapted gliding wings (Rayner 1985a, 1986; Norberg 1985), and that this confers a strong, and growing, selective advantage as flight develops (Rayner 1985b, 1991a). This does not, however, mean that gliding is the only pathway to flapping flight. Only in birds is a non-arboreal or non-jumping hypothesis for flight evolution considered viable. In this essay I explore some of the alternative hypotheses, and describe how consistent they are with the likely anatomy of a protoavian. Extant gliding tetrapods indicate the broad autotrophic adaptations of such forms, but many of these animals are highly specialized to exploit complex, and relatively recent (i.e. Tertiary), forest habitats. It appears that none of these organisms have evolved their gliding behaviour from bipedal cursorial locomotion comparable to that adopted by theropod dinosaurs, but rather that all have developed wing structures through a jumping, leaping, parachuting pathway. To argue that gliding of this mode is necessarily a precursor to flight is therefore to be circular, especially if such a pathway is unlikely to have applied to birds. On the other hand, gliding is widely used by true flying animals. Most birds and bats, and some of largest insects, can (and do) glide. Gliding and soaring in extant birds is a derived behaviour, concentrated in larger species for which it confers significant energetic and behavioural advances. In general smaller birds and bats do not use soaring flight, although they glide facultatively when appropriate. Gliding is straightforward in a vertebrate which has a wing and a large muscle to hold that wing horizontal against aerodynamic lift. It is not at present possible to identify any Mesozoic bird which must have used gliding or soaring as its primary mode of flight. It is probable that soaring was the main means of cruising flight of larger Cretaceous pterodactyloid pterosaurs owing to their size, but primitive Triassic pterosaurs were relatively small and were unlikely to have been obligate gliders. The same applies to Archaeopteryx, and accordingly to the origin of birds if it is reasonable to assume that this small theropod is indicative of the approximate size range in which flight originated. In this essay I shall demonstrate that an origin of flapping flight through a gliding wing is entirely plausible and consistent with the existing fossil record of birds, and that this hypothesis makes few demands on the palaeobiology or behaviour of protoavians. My argument stops well short of requiring obligate arboreality. It also does not mean that gliding was an essential flight precursor. The evidence for bipedal cursoriality in theropods is strong, although based in the main on morphology of large forms such as Deinonychus and other dromaeosaurs. The protoavian may well have been a small, bipedal cursor. I shall set out here how such an animal might develop flight, but will argue that some recent models of the transition from cursor to flier are not fully consistent with the flight anatomy of Archaeopteryx or with the subsequent radiation and specialization of avian flight morphology. Finally, I raise a number of broader questions associated with the palaeobiology of the first birds and with the evolution of specifically avian characters such as moult. Some at least of these issues are likely to be resolved by further development of the fossil record. Aerodynamics and biomechanics and the evolution of flying birds Flapping flight aerodynamics I have reviewed the aerodynamics of flapping avian flight in other papers (Rayner 1988b, 1991a, 1993, 1995a, b), and for brevity give only a summary of the key points related to flight evolution here. The wings of flying animals act as aerofoils, which generate a lift force perpendicular to the airflow approaching the wing, and which also experiences a drag force in the same direction as the airflow. By flapping the wings, the animal is able to incline the mean lift force forwards, so that in addition to providing an upwards force supporting the weight, it also achieves a forward force which acts as a thrust. This thrust force balances the drag on both the wings and the body, and it is this that allows the animal to fly forwards and level in cruising flight. As I have argued in the preceding section, it is the adaptations associated with the ability to generate thrust which characterize flying animals. Experimental flow visualization of the wakes of birds and bats (review by Rayner 1995a) and high-speed cin-filming of wingbeat kinematics (Rayner 1988b) have shown that there are only two patterns of thrust generation in steady forward flight. I have identified these patterns as two separate gaits, which are analogous to the locomotory gaits of terrestrial mammals, and each of which represents a suite of different morphological, kinematic, anatomical and aerodynamic parameters. The characteristics of the two gaits are summarized in Table 1. The most important factor distinguishing the two gaits is the upstroke; the upstroke cannot contribute useful to thrust, since the wing is travelling upwards (and often backwards) relative to the bird. In the vortex ring gait the upstroke is not used aerodynamically, and generates no lift; as a result the vortex wake shed behind the bird consists of a series of near-circular vortex rings; during the upstroke the wing is sharply flexed and the wrist is twisted, and the wings are raised by active contraction of the supracoracoideus and/or deltoid muscles. In the continuous vortex gait the upstroke is aerodynamically active, and the wing is raised by the aerodynamic lift on the wing surface; trailing vortices are shed continually behind the bird, and to ensure a net thrust force the wing is flexed at the wrist and the wing surface remains near flat throughout the wingbeat. These and other kinematic measures (table 1) enable the two gaits readily to be distinguished. The vortex ring gait is ubiquitous in birds in relatively slow flight, and is the only gait used by many species, particularly those which have relatively low aspect ratio. This is because at low flight speeds, and with short wings, it is inefficient to use the upstroke to generate lift (Rayner 1993). At higher speeds above the minimum power speedthat is in cruising flightit becomes more efficient for longer winged birds to generate lift during the upstroke; although this force retards the animal (it acts as a negative thrust), the bird avoids the energetic cost of starting and stopping lift generation at the start and finish of each downstroke (Rayner 1999). It is remarkable that in extant birds other patterns are not adopted in cruising flight (other patterns may be found in take-off or hovering), but the reason appears to be that these two gaits are the only patterns in which the aerodynamic energy cost of generating thrust simultaneously with supporting the weight can be minimized. Other patterns of wing movements might be able to produce thrust, but only at considerably higher energetic cost: as far as I am aware, no other patterns have evolved. Similar gaits are adopted by bats (with some modification to the geometry of the upstroke because of the elastic wing and the incorporation of the hindlimb in the wing), and pterosaurs with their high aspect ratio and flexing carpo-metacarpal joint were well adapted for use of the continuous vortex gait (Rayner 1989a; Padian & Rayner 1993). It is therefore to be expected that Mesozoic birds will have used one or other of these two gaits in steady, forward flight. Morphological correlates of wingbeat kinematics Flight anatomy in extant birds correlates with flapping gaits, mainly as a consequence of differences in the upstroke (Table 1; also Rayner 1988b). In both gaits the wing should be fully extended in the downstroke to maximize lift, and therefore thrust. Birds using the continuous vortex gait extensively tend to have relatively small M. supracoracoideus, because aerodynamic lift is responsible for wing elevation; the muscle is much larger in species using the vortex ring gait at all speeds (Rayner 1988b). In the continuos vortex gait the wing surface must be kept as close to planar as possible to maximize lift across the whole wingspan, and as a result the bird needs only to flex its wrist; in cruising flight in birds using this gait the elbow and wrist flex relatively little. To minimize upstroke wing drag and inertia in the vortex ring gait the elbow and wrist retract, and the wrist rotates so that feathers are separated. As yet it has not been possible to identify all of the changes with muscle function with speed and gait as predicted by these aerodynamic models, but the bending moments at the wing root agree well between aerodynamic theory and experiment (Rayner 1999). I have predicted (Rayner 1988a, 1991a) that the forces applied by the supracoracoideus to elevate the wing will reduce in faster flight with the continuous vortex gait, and that at some speeds the pectoralis should be active throughout the wingbeat to maintain the posture of the wing. In addition to acting directly as an elevator, the supracoracoideus also rotates the humerus (Poore et al. 1997a, b)which raises the wingtip indirectlyand acts as antagonist to the pectoralis; these functions are likely to be important at all speeds. Biomechanical requirements for flight From the above description of flight aerodynamics it is possible to set out the biomechanical and aerodynamic adaptations which are essential for flight. It is convenient to arrange these in three distinct domains. (1) A flying animal must have wings of aerofoil profile and of sufficient structural strength to generate enough lift to support the weight. (2) It must be able to flap its wings to generate thrust. This demands the abilities to control the position and the pitch of the wing, and to deform the wings appropriately during the upstroke, and will be accompanied by the evolution of large pectoral muscles to depress and elevate the wing. In turn this has implications for the design, and in particular the strength, of the skeleton around the wing articulation. (3) It must be able to control its flight (Maynard Smith 1952). This domain does not necessarily mean that its flight should be aerodynamically stable: birds and bats are rarely designed to have static stability. It does demand sensory mechanisms able to relate its flight path to its environment, and control surfaces able to respond sufficiently rapidly. In most extant birds and bats the primary control surfaces are the wings; in many species the tail also plays an essential role. All the groups of flying animals have evolved flight adaptations in response to these constraints, starting from different morphological Bauplne. As a result there is considerable anatomical variation in the mechanism by which flight is achieved, but because of the strong aerodynamic constraints on flying organisms there is much less diversity in flight morphology, allowing for differences in size (Rayner 1995b, 1996). Aerodynamics and flight in Archaeopteryx Archaeopteryx is the least-derived known flying representative of the Avialae. Its flight morphology is indicative of the gait it used in flapping flight. We do not of course know the wingbeat kinematics or the vortex wake of Archaeopteryx. However, in the anatomy of its wings and pectoral girdle it differs appreciably from extant birds, and from key charactersincluding those used to determine its phylogenetic position (figure 1)it is possible to determine how it must have flown. (1) Wings Archaeopteryx has wings, formed of feathers with stiffened rachis and asymmetric vanes, which are very similar to those of extant birds (see, for example, Rietschel 1985). There is no doubt that these are the wings of a competent flying animal, able to generate a significant lift force. (2) Pectoral girdle Second, and by contrast, it shows a simple pectoral girdle similar to that of non-flying theropods, but with a lateral-facing glenoid; the coracoids are not the solid strut-like braces of modern birds; while some specimens have a furcula, all lack a calcified sternum and a sternal keel (Ostrom 1974). These features suggest relatively weak specialization for flapping flight. The absence of the sternal crest implies that it also lacked the pars thoracicus of the pectoralis; in extant birds this component of the main downstroke muscle attaches to the delto-pectoral crest of the humerus, and pronates the wing during the downstroke as well as contributing to wing depression. The majority of pectoralis fibres originate from the furcula and from tissue surfaces below the humeral joint, and apply a positive vertical or roll moment to the humerus, depressing and protracting the wing with little pronation. Birds require extreme pronation only in slow flight, when it controls the varying vortex strength and flexes the wing surface during the upstroke (Rayner 1988a, b); in fast (cruising) flight the wingbeat is primarily dorso-ventral, the wing remains near planar throughout, and changes in angle of incidence of the wing aerofoils are more moderate (table 1). The absence of a sternal keel implies that early birds (including Archaeopteryx) were unable to fly slowly, but does not constrain their ability in forward cruising flight: the keeled sternum is a derived character which evolved subsequent to Archaeopteryx and is associated with the development of slow flight and manoeuvrability. According to this interpretation, Archaeopteryx might well have been able to depress the wing, but would have been unable to pronate it effectively: it could not have flown slowly. (For an alternative aerodynamic argument against slow flight in Archaeopteryx see Burgers, this volume.) (3) Upstroke musculature Archaeopteryx is also primitive in its upstroke musculature. In extant birds the wing elevator is the M. supracoracoideus, which originates on the sternum along the base of the sternal keel, deep under the pectoralis, and inserts onto the dorsal side of the humerus through a cavity within the humeral joint (the foramen triosseum). Today this arrangement is unique to birds, although it was also present in pterosaurs; it was absent in Archaeopteryx (Ostrom 1974, 1976b), and must therefore have evolved subsequently. Early flying birds may have used other muscles such as the deltoid group to elevate the wing, but if this were the case it is hard to envisage the selective pressures that must have forced the development of a novel muscle system to form the supracoracoideus in place of the deltoid group. In flight an elevator muscle is required only at low speeds (Rayner 1985a, 1986, 1988a, b), and at higher (cruising) flight speeds the wing is elevated by aerodynamic forces. It is likely therefore that Archaeopteryx flew in such a way that it never needed active muscle action to elevate the wing. Again, Archaeopteryx could be capable of steady cruising flight, but it could not fly slowly. (4) Wing flexion The best known of the morphological characters which link Archaeopteryx to the dromaeosaurs is the semi-lunate carpal forming the wrist articulation, which is shared with theropods such as Deinonychus (Ostrom 1974; Gauthier & Padian 1985; Padian 1987); as an individual bone this was lost later in avian evolution as the bones of the manus became fused. This configuration ideally permits flexure of the wrist to sweep the wingtip within the plane of the wing, but prevents rotation of the hand wing out of this plane. This flexure is precisely the movement which occurs during the upstroke in cruising flight in the continuous vortex gait (table 1), but is not the movement found commonly in slow flight in the vortex ring gait or during take-off and landing. Sincelike all tetrapodsArchaeopteryx was capable of dorso-ventral movement of the humerus, this wrist morphology indicates that it was capable of cruising flight, but could not achieve the complex twisting, folding and flexing of the wing which must be used in slow flight. (5) Control and stability With its long bony, frond-like tail counterbalancing the weight of the body in running (see also below), Archaeopteryx was likely to have been statically stable in flight. This minimizes the control movements required for steady flight. The penalty of static stability is that the animal has considerable inertia in response to control. Manoeuvrability and agility are therefore low. This constrains flight abilities, and rather few living animals are defined in this way. Such a design is not, however, surprising in an intermediate flying animal. Flight of Archaeopteryx Without elevator muscles, without longitudinal pectoralis fibres originating from a keeled sternum, and with no ability to deform the wing out of its plane during the upstroke, Archaeopteryx lacked all of the features associated with slow flight in birds with the vortex ring gait: these adaptations and the associated abilities for take off and landing are therefore derived in birds (figure 1). Fast or cruising flight with the continuous vortex gait is less demanding mechanically than slow flight: the forces required from the pectoralis are less extreme, no elevator muscle is needed (Rayner 1986, 1988a, b), mechanical energy demands are less, and the wingbeat geometry is simpler (table 1). Archaeopteryx did have all of the adaptations for forward flight with the continuous vortex gait, and would have been able to flap at reasonably high speeds. Archaeopteryx is unlikely to have been proficient in slow flight, or to have been very agile and manoeuvrable, and its take-offs and landings were probably quite awkward (Rayner 1985a, 1988a, 1991a). Archaeopteryx and flight evolution The implications of this flight pattern in Archaeopteryx are clear. It falls phylogenetically as the theropod which is the closest sister group to all other birds, and is intermediate in morphology between cursorial theropods and birds. For these reasons it is therefore likely to represent an intermediate stage in flight evolution. This means that flight first evolved at relatively high air speeds, and radiated later to encompass slower flight speeds and to improve manoeuvrability and take-off. Selective pressures for slow flight performance were evidently strong, and led to the rapid acquisition of characters associated with use of the vortex ring gait; I discuss below how this sequence of character acquisition is consistent with the phylogeny of Mesozoic birds. The key question is how did early birds, including Archaeopteryx, achieve these high speeds. I estimated (1985a, b) that speeds of the order of 68 m/s were likely for the optimal origin of flight, and these are somewhat higher than a running biped using only its hind limbs for locomotion can be expected to reach. Resolving how cursorial birds might have overcome this speed gap and associated morphological constraints (see below) remains a challenge to explanations of flight evolution in a cursorial animal. The obvious way in which a protoavian can achieve speeds of this order is by gliding. For this reason gliding has become a central tenet of arboreal models of flight evolution. I do not consider that full arboreality is either necessary or likely, and I shall return to discuss this point again below. In this debate the morphology of Archaeopteryx provides an important piece of evidence. A gliding animal can achieve the continuous vortex gait very simply, by flapping the wings and simultaneously flexing the wrist in the upstroke; because aerodynamic lift elevates the wing relative to the body there is no need for active elevating musculature, and the extra force required to depress the wing during the downstroke is not large. Archaeopteryx could accomplish these movements, and the presence of the semi-lunate carpal in dromaeosaurs means that protoavians could as well. Its wrist did not allow extensive rotation of the hand wing (Vasquez 1992, 1994), but I do not accept Vasquezs assertion that the animal could not fly. It means that it could not fly slowly, and could not use the vortex ring gait. In the continous vortex gait which Archaeopteryx could achieve even relatively small wingbeat amplitudes provide useful thrust (Norberg 1985; Rayner 1986); increasing amplitude leads to increasing thrust, and to useful extension of distance travelled even with quite short glides, and therefore to a strong selective advantage for flight (Rayner 1988a, 1991a). This was the selective mechanism underlying the evolution of avian flight. Physiological and behavioural domains in the evolution of flight In a previous section I used a concept of domains to set out the aerodynamic and biomechanical adaptations which are essential for the evolution of flight. The first three of these were associated with flight biomechanics and aerodynamics, as set out above. The other two are more elusive and in the main less tractable from the fossil record, but they are no less essential (see also Rayner (1989b, 1991a). First, a flying animal must have evolved physiological systems capable of mobilizing fuel and oxygen in sufficient quantities, and sufficiently rapidly, to power the flight muscles. Flying birds (and also bats, which in this respect are broadly comparable) experience a substantial locomotor energy demand and must generate locomotor forces which relatively are rather higher than those of almost every other group of vertebrates. Instantaneous energy demands and muscle forces are particularly high in take-off flight (Rayner & Swaddle 2000). There is no reliable information on locomotor physiology of Archaeopteryx or its theropod precursors. This topic has been hotly debated by Speakman (1993) and Ruben (1991, 1993), among others, with little concensus; incipient or established endothermy in theropods would facilitate high levels of metabolic output in early fliers, and there is some evidencesuch as presence of integumentary coverings (see below)which support this. Regardless of the capabilities of avian precursors, the level of mechanical energy output required for flight is inescapable; if the first flying birds had not achieved the physiology of extant birds then presumably they would have been less able to sustain flight. As a result the energy they would need to fly would be greater than birds of today. This places a premium on behavioural strategies which minimize flight energy, and may constrain the extent of flight activity of a protoavian. The most widely used of such energy-minimizing strategies in flying birds today is gliding flight (including soaring and intermittent gliding; Rayner 1985c; Rayner et al. 2000). One consequence of these high levels of metabolic activity in flight is a high body core temperature. Regulation and radiation of this excess heat (Ward et al. 1999) and the associated water loss (Carmi et al. 1992) are major constraints on flying birds, and it is hard to see how they could be escaped by a protoavian developing a similar locomotor pattern. The final adaptive domain covers the suite of autotrophic ecological, behavioural and sensory adaptations which allow an animal to exploit a complex three-dimensional aerial environment. These are factors which can broadly be summarized as palaeobiological; while in Archaeopteryx they have been the focus of a great deal of speculation, there is relatively little hard evidence on which to base adaptive scenarios, but a number of crucial questions stand out. A bird must evolve a highly efficient visual system able to measure its environment (see, for further discussion, Chatterjee 1991, 1997, 1999). At what stage did some of the specialized sensory capacities of extant birdssuch as ultra-violet vision and the use of filoplumes to determine air currentsattain their present level of performance? The ecological communities of extant birds are organized in very different ways to those of terrestrial animals. It is unreasonable to expect this to be purely a characteristic of quaternary birds. How were the communities of Mesozoic birds structured? How tight were the niches into which the first flying birds evolved? The radiation of flying birds Selection for flight An answer to the last of these questions may in time come from the growing fossil record of Cretaceous birds, particularly from China but also from other Upper Jurassic or Cretaceous Lagersttte. When I last reviewed the origin of flight (Rayner 1991a) the approximately 50 MY gap between Archaeopteryx and Ichthyornis and Hesperornis (Marsh 1880) was filled by a single, then unnamed specimen from Spain. It was clear that selection following Archaeopteryx had been concentrated on the flight system, with rapid changes in the forelimb, pectoral girdle and tail, but little change in the hind limbs, but it was possible only to speculate on further details of this transition. There is now a rich, and rapidly growing, record of the Mesozoic radiations of birds (figure 1). Indeed, so quickly is this situation changing as more material is described that any detailed description or phylogeny rapidly becomes outdated. There is now a picture of a rapid radiation of birds after the initial establishment of flight, with at least three significant lineagesConfuciusornithidae, Enantiornithes and Ornithuraeappearing in the mid-Cretaceous and distinguishable at least in part on the basis of characters related to their flying systems. Each shows a considerable degree of specialization, with apparently competent flight performance broadly comparable to that of extant species, albeit with less overall morphological diversity. This is testament to the effectiveness of flying as a means of exploiting the rapidly changing environments of the Cretaceous. It suggests that birds were not greatly inhibited by existing flying organisms (insects and pterosaurs), and may mean that birds were able to capitalize on the contemporaneous evolution of angiosperm plants and of plants with C4 metabolism. Through this period selection on birds acted primarily on the flight system. This is to be expected as the limited flight capacity of the first flying birds as represented by Archaeopteryx is enhanced. This trend was driven primarily by pressure for greater control of flight and for slow flight performance. The continuous vortex gait restricted Archaeopteryx to cruising flight, but rapidly forelimb and pectoral girdle morphology evolve to show the ability to use the vortex ring gait in slow flight. There is a tendency for the forelimb to be simplified, with fusion of the carpo-metacarpus and rapid loss of digits to form the avian manus, and lengthening of the skeletons of both forearm and hand and shortening of the humerus (Dyke & Rayner, this volume). These changes permitted greater control of the geometry of the wing, and in particular of flexure of the wrist and hand wing; they were accompanied by the evolution of mechanisms of wing folding, and by the appearance of the alula (Sanz et al. 1996). In extant birds this feathered first digit is an essential feature of the operation of the wing in slow flapping flight at high lift, as it controls the airflow over the mid point of the wing, and prevents distal propagation of airflow separation from the dorsal surface, and therefore catastrophic loss of lift. Presumably the alula in Mesozoic birds functioned similarly. The mechanism for limited control of the pitch and flexure of the primary wing feathers provided by the digits in Archaeopteryx was overtaken by automatic control of handwing pitch through the flexure of the wrist (Fisher 1957; Vasquez 1992, 1994; Ostrom 1995). The absence of this mechanism in Archaeopteryx implies that its wings remained largely flat, and the presence of the semi-lunate carpal implies that it could not deform the wing surface by rotating the wrist as do extant birds in slow flight (table 1). Subsequent to Archaeopteryx the pectoral girdle is stiffened with the appearance of a strut-like coracoid to brace the humeral joint and wing from the sternum against the large forces imposed by the pectoralis muscle in slow flapping flight. The enlargement of the sternum and the appearance of the keel (carina sterni) is also evidence of a trend to enhanced slow flight: pectoralis muscle fibres originating on the keel are responsible as much for pronation of the wing as for depression during the downstroke, and control of pronation and supination over a large range of angles is required only in slow flight with the vortex ring gait. Archaeopteryx did not possess an elevating supracoracoideus muscle (Ostrom 1976b). This muscle appears subsequently, again in association with development of slow flight and manoeuvrability. In extant birds the antagonistic pair of the pectoralis and supracoracoideus are responsible not only for depression and elevation of the humerus, respectively, but also for rotation about the axis of the humerus (Poore et al. 1997a, b). This rotation contributes in part to pronation and supination of the wing, and in part to depression and elevation of the more distal portion of the wing surface since the humerus is not held parallel to the leading edge of the wing. This component of movement was apparently reduced or absent in Archaeopteryx, which was restricted to a largely dorso-ventral movement of the wing at the humeral joint (above). This movement, combined with in-plane flexure of the wrist (above), is sufficient for flight at cruising speeds with the vortex ring gait. Subsequent selection for slow flight and the use of the vortex ring gait requires greater wingbeat amplitudes and greater pronation of the wing chord, and this was brought about by a rotation of the lines of action of the pectoral muscles on the wing, so that the pectoralis has an anterior/ventral action pronating and depressing the wing, and the supracoracoideus, shifting to run through the triosseal pulley in the humeral joint, supinates and elevates. The stage at which this transition occurred is unclear. It was certainly in place in the Ornithurae, and was probably a feature of Enantiornithes or of Confuciusornithidae (but see below). While Iberomesornis (Sanz et al. 1988, 1992) shows some intermediate characters indicating it is more primitive, I have followed Chiappe (this volume) and Sereno (this volume) in including it with Enantiornithes, possibly as a juvenile. Parallel to these modifications of the forelimb system were dramatic changes to the tail. The theropod tail is primarily concerned with counterbalance of body weight in running, and as the origin of the leg retractor muscles (Gatesy 1990; Gatesy & Dial 1996a, b; Gatesy & Middleton 1997). In this it is similar to the function in lower tetrapods, and in particular in bipedal squamates. In flying birds the tail is generally interpreted as an aerodynamic lifting surface. The force the tail generates has therefore reversed, from a predominant downwards weight (or lateral inertia from lateral flexion) to an upwards lift; the balance of vertical forces on the bird has also changed, from the weight of the tail balancing the weight of the body with the centre of mass anterior to the pelvis, to an upwards aerodynamic force from the tail balancing the lift from the wings acting anterior to the centre of mass. Many extant birds have taken this further, dispensing with the tail as a lifting surface, and either reducing the tail and using the wings as the aerodynamic control surface (as in swifts, Apodidae), retaining the tail for display, communication and sexual selection but eliminating aerodynamic function, or using aerodynamic lift from the tail only in slow flight or manoeuvring. Recent work (W. J. Maybury & Rayner, unpublished) has shown that in starlings, a species with a square, elongated tail, the tail functions to reduce drag and to control airflow over the body in cruising flight, and only generates lift facultatively in slow flight. In other species, for instance the magpie Pica pica, the tail generates lift in cruising flight, and in this and other birds of similar morphology the tail compensates for the reduced area of its relatively short wings. Over the transition from theropod to flying bird the tail rapidly lost much of its weight, as the bony elements shrank to a short pygostyle with the surface of the tail formed of relatively light feathers arising from a bulb of fat surrounding the pygostyle, the bulbus retrici. The feathered bony frond-like tail in Archaeopteryx is unlike that of any other avialan, and is an intermediate between the theropod and avian conditions. It probably had an intermediate function: in running the bony vertebrae displaced behind the pelvis would balance the animals weight, while in flight the frond-like feathers could generate enough lift at least to support the weight of the tail skeleton, with possibly sufficient to contribute to weight support analogous to the magpie; this would depend on the posture of the whole tail in flight, and on whether the posture of individual feathers could be controlled. Archaeopteryx and the magpie are of similar size and aerodynamic morphology; however, this does not necessarily mean that like contemporary magpies Archaeopteryx was arboreal. Rather, I interpret the persistence of the bony tail in this flying organism as evidence that it was a bipedal cursor as well as an active flier. By contrast to changes to forelimb and tail, selection acting on the hind limb for terrestrial locomotion was evidently much weaker. There are relatively few significant alterations in morphology of the hind limb other than those associated with reduction of the tail (Gatesy 1990) to maintain balance with the location of the centre of mass anterior to the pelvis in running, with a subhorizontal orientation of the femur and a tendency to a more upright posture (Gatesy 1990); the proportions of the limb elements remain largely unchanged (Gatesy & Middleton 1997; Dyke & Rayner, this volume). This is indicative of two things. First, the cursorial theropod avialan precursor was already well adapted for efficient terrestrial locomotion, and, second, there were relatively few changes in the mode of non-aerial locomotion: hind limb morphology is not indicative of arboreality in non-ornithothoracine avialans. Aerodynamics and the phylogeny of Mesozoic birds The Ornithurae are the lineage which leads to extant birds, and give rise to no fossil evidence through the Lower Cretaceous. Two other groupsthe Enantiornithes and the Confuciusornithidaediverged in the Upper Jurassic and radiated in the Cretaceous, but do not have extant representatives. Enantiornithes are distinguished primarily by non-flight characters (Padian & Chiappe 1998), and include forms with a range of sizes and flight morphologies, many of which claws and feet for arboreal perching (see also below). At least two taxa, Eoalulavis (Sanz et al. 1996) and Eoenantiornis (Hou et al. 1999), are significant in possessing an alula. The alula is a primitive character of neognaths, which may have originated independently in these species, but is more likely have evolved in Ornithothoraces alongside other adaptations for slow flapping flight (figure 1). It is another feature indicating that the radiation of flight forms to include slow manoeuvrable flight with the vortex ring gait took place subsequent to Archaeopteryx. Its absence in the Confuciusornithidae is significant. Confuciusornithidae The two taxa in this familyConfuciusornis (Hou et al. 1995, 1996; Peters & Qiang 1999) and Changchengornis (Ji et al. 1999)are characterized by unusual humerus morphology and a reduced tail skeleton with a pygostyle; they retain three independently movable digits with a semi-lunate carpal on the second digit, and have a sternum with a shallow keel and a strong furcula. They do not have an alula, and the triosseal canal is absent (Hou, this volume) indicating they had not evolved an elevating supracoracoideus. There is no aerodynamic tail; there was a very short aerodynamically non-functional tail fan, but in Changchengornis and in some individuals of Confuciusornis there are extended ribbon-like streamer feathers which are unlikely to have aerodynamic function but were probably used display or sexual selection; in Confuciusornis this represent the earliest example of sexual dimorphism in birds. The humerus has an enlarged delto-pectoral crest extending for approximately half the length of the humerus, and with a broad circular outline. I propose that this correlates with the absence of a functional tail, alula and an elevating supracoracoideus; these last two structures may then be ornithothoracine characters, as argued above. An important feature of ornithothoracines, which is apparently not shared with confuciusornithids, is the coevolution of the wing and tail into the flight locomotor system (Gatesy & Dial 1996a). This lineage evolved to use two independent aerodynamic surfaces, the wings and the tail, to control stability in flight, moving the wing by combinations of pronation and supination, depression and elevation by supracoracoideus and pectoralis, flexing and rotating the wrist, and controlling airflow over the wing by an alula. This lineage led to modern birds (figure 1), which share this suite of control strategies. By contrast, confuciusornithids appear to have developed along different lines, with the relatively long, high aspect ratio wings being responsible for all propulsion and control, and the tail becoming mechanically redundant. The enlarged delto-pectoral crest of the humerus means that the locations of insertion of fibres from the pectoralis (and possibly the deltoid or a supracoracoideus homologue) are spread over a broader area, thereby giving greater control over the position and posture of the wing. The size of the crest indicates more extensive pronation and supination movements. This would be correlated with the short coracoid in these birds. Although the alula is absent, the third finger probably had the same function in controlling separation of the upper surface airflow (Peters & Qiang 1999). Tailless birds are highly agile and manoeuvrable (compare modern swifts, Apodidae), but aerodynamically are statically unstable. If confuciusornithids were the agile fliers that they appear to be, then like swifts they were probably aerial insectivores; at this relatively early stage in the avian radiation the capacity to evolve advanced neural control and sensory systems essential for this unstable form of flight was already present. Arboreality in Confuciusornithidae is unlikely (Peters & Qiang 1999; Chiappe et al. 1999), and is not necessarily consistent with aerial insectivory or their long, high-aspect-ratio wings. It is tempting to speculate further that this strategy was less successful biomechanically or that it constrained these animals trophically, and further that one or both of these factors explains the absence of confuciusornithids after the Cretaceous. In view of the limited fossil record of this group it is not possible to test these hypotheses at present. Enantiornithines and Ornithurae Through the Upper Jurassic and Lower Cretaceous birds show rapid radiation to new niches. Of these two sister groups, only enantiornithines give rise to a fossil record during this period. They are rather diverse, but are identified as monophyletic by characters unrelated to flight. Their size range includes both small manoeuvrable forms equivalent to extant passeriforms (e.g. Iberomesornis, Eoalulavis, Concornis, Sinornis (Sereno & Rao 1992) Eoenantiornis (Hou & Chen 1999) and Liaoxiornis (Hou et al. 1999)), many of which were arboreal, and some particularly large species (Kurochkin 1999). The impression is of a rapid radiation in Enantiornithines to a variety of aerial niches which in their diversity were broadly equivalent to those of modern birds, and which paralleled the flight radiation in Confuciusornithidae. The status of Ornithurae in these radiations is unclear, and significant diversity in this group may not have appeared until after the late- or end-Cretaceous extinctions of enantiornithines and confuciusornithids. Flightlessness also appears. Some enantiornithids were flightless, as were the Upper Cretaceous Hesperornis (Marsh 1880) and Patagopteryx in the Ornithurae. The status of the Alvarezsauridae is uncertain; most workers (e.g. Perle et al. 1993, 1994, and papers in this volume) have placed this flightless group, with extremely reduced forelimbs, within birds as the sister group to all other birds apart from Archaeopteryx; this would imply that flightlessness evolved very rapidly after the first flying birds. In view of the differences in limb proportions and the paucity of flight-related characters shared by this group and other birds, I tentatively follow Chiappe (this volume) in placing the Alvarezsauridae as the avian sister group within Paraves (figure 1), and not do not regard them as aberrant flightless avialines. Discussion Flight evolution in protoavians The evolution of feathers The discovery of plumaceous feathers in non-avian theropods puts beyond doubt that feathers evolved for some function other than flight, and probably first appeared at a time well before Archaeopteryx. There is insufficient space here to review the many adaptive hypotheses which have been proposed for their origin. Thermoregulation and response to solar radiation (Regal 1975, 1985), water-repellancy (Dyck 1985), display or protection from fighting (Cowen & Lipps 1982) are all plausible possibilities consistent with the uses to which feathers are put by extant birds. It should be noted that these are not hypotheses explaining the evolution of flight; their importance lies in making it possible to separate the origin of feathers (and of the complex endocrinological and cellular mechanisms which build them) from the origin of flight. The compsognathid Sinosauropteryx has proto-feathers along its spine and tail (Chen et al. 1998), the therezinosaur Beipiaosaurus has them on its forelimb (Xu et al. 1999), while the more derived paravians Caudipteryx and Protarchaeopteryx have them also on the forelimb and tail (Ji et al. 1998). If there is no complete feathered body covering, this topography perhaps suggests that proto-feathers played a role in communication, display or behaviour and initially did not have a physiological or biomechanical purpose. As yet there is little information on the microstructure of feathers in non-avialan theropods. It appears that a central rachis and vane are present in the more derived forms and the feathers have lamelliform barbs, but they lack the stiffened rachis and (probably) the interlocking barbs and barbules which make avian contour feathers impermeable to air and give them their aerodynamic integrity. It should be cautioned that the absence of flight feathers may be an artefact of preservation, since only a proportion of the feathers on a living bird are modified for flight, and such feathers may have been present but not preserved in some or all of Sinosauropteryx, Caudipteryx or Protarchaeopteryx. Against this it must be recognized that wing primary and secondary feathers are more likely to fossilize than softer or downy body feathers (as in some specimens of Archaeopteryx and in many other fossil birds specimens), and that such feathers are evidently absent from the wing of Caudipteryx. The development of some use of feathers in thermoregulationas a mechanism either of retaining body heat or differentially radiating excess heatin theropods prior to Archaeopteryx cannot be ruled out, and has generally been accepted to be likely. Other authors in this volume consider the contentious issues of the evolution of avian physiology and the avian lung, and the related question of thermoregulation in dinosaurs. I consider it probable that the grounding of the physiological processes permitting high levels of energy output in locomotion were in place prior to the evolution of flight, perhaps consistent with Reids (1998) intermediate dinosaurs. It seems reasonable to suppose that the modification of at least some of the body integument (homologous to avian contour feathers) was involved in this process. There is currently insufficient information to explore this further. (For an alternative neontological perspective see Randolph (1994).) The key question of the role of feathers in the evolution of flight becomes the origin of the stiffened aerodynamically competent feathers of the wing and tail. It is more likely that the stiffened flight feather evolved from a softer display feather, as the wing became adapted for aerodynamic force generation; in the phylogeny of figure 1 this character would have evolved with the Avialae, between Caudipteryx and/or the Alvarezsauridae and Archaeopteryx. Under a reasonable adaptive scenario, bipedal theropods would have used proto-wings formed of plumaceous feathers to extend jumps, to stabilize running, or to provide some forward force while running. An elongated but soft feather will generate drag (this force would probably be small), but relatively little aerodynamic lift since it would deform easily. Animals with relatively stiffer feathers might generate more lift, and if this lift can be used to contribute usefully to fitness, selection could favour rapid stiffening of feathers. This process could have taken place simultaneously with the development of the pectoral girdle muscles and skeleton associated with the evolution of wingbeat kinematics. This interpretation of flight feathers as an avialan character is consistent with the known fossil record. The evolution of feathers raises a number of interesting biological questions, particularly concerning their maintenance. In extant birds this is totally integrated into endocrine cycles and the life history strategies (Rayner & Swaddle 2000). Feathers are moulted on regular cycles to replace worn-out structures, and, since it has a significant energetic cost and impairs flight ability, moult is scheduled around other critical activities such as reproduction and migration. A range of behaviour patterns are employed to maintain and preen feathers, and for some species this occupies a considerable part of the time. Finally feathers often carry species- or feather-specific parasites and bacteria which coevolved with birds. How did these patterns come into being? Moult patterns of individual feathers have some similarities with patterns of integumentary moult in reptiles and of hair geometry in mammals, and it is possible that the foundations of the moult mechanisms are primitive. Some aspects of the avian moult cycle are specialized in birds, however. At what stage did these evolve? Were they present in Archaeopteryx, as seems likely given its flight feathers would require maintenance, or did they evolve in the feathered non-avialan theropods? Wingbeat kinematics A bird will not enable thrust simply by waving its wings. Padian (1985, 1987; Padian & Chiappe 1998) has emphasized the importance of the evolution of what he terms the flight stroke in the evolution of birds, but does not go as far as to relate this to the kinematics of extant birds. He envisages a posterioranterior slant to wing movement in the downstroke, but this type of wingbeat is characteristic of slow flight (figure 1), and in living birds is associated with active muscle force driving the upstroke. I argue here that these movements are derived. Wing movements must be co-ordinated to control the magnitude and variation of the aerodynamic lift. In the simplest gait, in which the wings generate continuous vortices, three movement sequences are largely decoupled and driven by different mechanisms. Dorso-ventral flapping of the wings driven by the pectoralis parallels flexure of the wrist to sweep the wingtip during the upstroke (but not the downstroke), and pitch of the wing cord (equivalently pronation of the wing surface) varies to control the vortex circulation on the wing. I have argued above that this combination of movements is primitive in birds: dorso-ventral flapping follows naturally from a lateral-facing glenoid; Archaeopteryx shares with dromaeosaurs the semi-lunate carpal associated with wrist flexure; the delto-pectoral crest on the humerus combined with pro-or retraction of the humerus in the shoulder joint forms the mechanism by which the pectoralis controls wing pitch. Take-off mechanics and bird evolution Take-off is generally accepted to be the most demanding mode of flight in extant birds. A climbing take-off from the ground requires the expenditure of substantial mechanical energy and the generation of very levels of muscular and aerodynamic force (Rayner & Swaddle 2000). Aerodynamic lift is close to the limits that an aerofoil can achieve. Many derived extant birds take off from the ground or water surface only with great difficulty, and avoid doing so wherever possible. Take-off provides one of the most significant biomechanical constraints on flight (Rayner 1995b), and is one of the factors which set the upper limit to size in flying animals (Rayner 1996). Yet it is a running take-off which is always envisaged in the evolution of flight in a running cursor. A crucial objection to the cursorial hypothesis for bird evolution since criticism (Abel 1911; Heilmann 1916 and others) of the work of von Nopsca (1907, 1923) has always been its implicit requirement that the aerodynamic and physiological capabilities associated with take-off from the ground should have evolved before the less demanding ability for steady forward flight was in place (Rayner 1991a). I consider this is still a serious, although not insurmountable, difficulty with this hypothesis. Burgers & Chiappe (1999) have developed a simple aerodynamic model of a running take-off in Archaeopteryx, and show how excess aerodynamic lift from a dorso-ventral downstroke would act as a horizontal thrust which would accelerate a running biped. This modelwhich is effectively the same as that of Norberg & Norberg (1971)is an effective demonstration of how a bird achieves a running take-off. It may be a plausible model for take-off in Archaeopteryx, although I have some reservations about this. It should not, however, be interpreted as a model for the evolution of flight. In size and wing outline Archaeopteryx is not primitive: its morphology is sufficiently close to that of modern pigeons and magpies that it probably had comparable flight characteristics. It is not remarkable, therefore, that it was able to take-off. The limitation of this model is in the nature of the thrust force, and its anatomical correlates. The purpose of flapping flight is to generate thrust, and it is reasonable to suppose thrust increased progressively as flight developed. Lift may readily be used as a vertical weight supporting force simply by holding the wings outstretched; by contrast, the generation of a mean thrust by flapping is far more complex, yet the running cursor is expected to develop the capability to produce this thrust force first. Because running speeds are relatively low compared to flight speeds it would not be possible to use the upstroke to generate lift: the animal would have to use the vortex ring gait. However, I have argued above that this gait evolved subsequently, and is not primitive in birds. A modern running bird has all the morphological adaptations in place to generate thrust while taking off at low (=running) flight speeds: these are the characters associated with the vortex ring gait, including the ability to raise the wing in the upstroke by the supracoracoideus. Archaeopteryx however did not have the supracoracoideus. In running it is not evident how it could have elevated its wing, and in a running take-off it would have been travelling too slowly to be able to use the aerodynamic lift which would readily raise its wing in cruising flight. Of course, other muscles could have elevated the wing, and the animal could certainly have done this with the deltoid group. If this were the case, what selective pressure would have encouraged the evolution of the elevating supracoracoideus? I have established above that this appeared later in avian evolution in association with the development of slow flight abilities and the vortex ring gait. Trees up or ground down? For many years since initiated by Darwin (1859), Marsh (1880), Thomas (1879) and Williston (1879), debate on the behavioural correlates of flight evolution has centred on two contrasting and polarized hypotheses: the arboreal and cursorial models of flight evolution. This debate is unhelpful; it stifles other approaches to the subject, and it has done the great disservice of setting camps of workers against one another when in practice they share considerable common ground. I have argued previously (1991a) that these models are inappropriate, and they tell us more about the palaeobiology of the avian antecedent and its habitat than about biomechanical and aerodynamic aspects of flight origins. Any biomechanicist working on this problem will rapidly agree that a gliding origin of flight is entirely plausible on biomechanical grounds: it is best to use the dominant force actingthat of gravityto drive the locomotion, rather than to work against it. (Even running cursors do that!) However, extensive palaeontological evidence makes it clear that neither Archaeopteryx nor its theropod ancestors were arboreal (Ostrom 1974, etc.). Although an arboreal gliding origin of flight in bats is likely (see above), it has not been thoroughly accepted as a component of bird origins. Ostrom (1997) takes me to task for seeking avian ancestors with incipient aerial locomotion, but without the ability to produce thrust. His misconception is that I was not implicating Archaeopteryx as one of these ancestors. Archaeopteryx flew well, and could flap its wings and flex its wrists to generate thrust in cruising flight, butas I have shown aboveit could not fly slowly. I consider that it is hypothetical running theropods which used a certain amount of gliding flight prior to the stage at which wings began to be flapped to generate thrust. We may now have some fossil evidence for this in the forelimbs with distal feathers of Caudipteryx. The further misconception with this debate is the assumption that gliding necessarily implies arboreality. This is the mythical explanation which Ostrom (1997, p. 306) should have tackled. It is arboreality which is the garden path, not gliding. Glides can be very brief. I envisage (Rayner 1985b, 1988a, 1989b, 1991a) a running cursor generating a static lift force from the wings for short periods, probably initially for longitudinal stability, because the centre of mass lies anterior to the pelvis. It may be running over broken ground, and therefore descending at times, it may be jumping while running, or may simply be holding its forelimbs outstretched. At this stage flapping the wings may be valuable for lateral balance and stability, but will not have the controlled kinematics necessary for useful thrust. This mechanism will work at relatively slow speeds, and requires the avian ancestor only to have a wing with a distal surface, presumably feathered, and the muscle (the pectoralis) to keep that wing outstretched against lift. It is then a relatively short step to begin co-ordinated flapping of that wing so that the mean lift vector is inclined forward producing thrust. This could hypothetically model the precursor to the running take-off of Burgers & Chiappe (1999), although the objection of the absence of an elevating supracoracoideus remains. I have shown (Rayner 1988a, 1991a) that along this pathway to the evolution of flapping thrust a bird experiences positive and increasing selection pressure for the evolution of wings, but that selection is far less encouraging for the running cursor with thrust as the initial wing force. Models of this kind are always formulated for still air. They envisage running and flying speeds for a protoavian of Archaeopteryx size around 4 to 8 m/s, with flight speeds towards the upper end of this range but maximum running speeds towards the lower end. Burgers & Chiappe (1999) have gone some way to narrowing the speed gap. It is far easier to remove this gap by assuming that protoavians made use of wind, at even rather low speeds. This is of course an untestable hypothesis; however, the habitats of modern cursorial animals are rarely free of wind! Alternative paradigms for flight evolution Debate about avian flight evolution has rarely extricated itself from the cursorial or arboreal models, or for compromise hypotheses of the type raised here. An alternative biomechanical model for the origin of flight has been put forward recently by Eberl (1996); this is similar to a hypothesis I advancedin part in jestsome while before (Rayner 1985d). This is the idea that flight evolved underwater. This is consistent with the taphonomy of Archaeopteryx in the shallow lagoonal environment of Solnhofen, and also with a possible piscivorous diet. It is also an attractive idea for mechanical reasons, since the density of water is sufficiently high to support most of an animals weight by buoyancy. Several other lineages of tetrapods which have secondarily become obligate swimmers have evolved similar swimming mechanisms using the forelimbs as wings, and effectively flying underwater (ichthyosaurs, plesiosaurs, marine turtles, sea lions). This adaptation is particularly effective and all of these groups are particularly efficient swimmers. It has also evolved independently in several avian groups, some but not all of which have become secondarily flightless (penguins, some alcids), while others can fly in both water and air (some ducks, gannets, some alcids, diving petrels, dippers). Evidently this swimming mode presents rather few mechanical or morphological obstacles. Unfortunately this model cannot explain avian evolution, and the evidence for this comes from the morphology of Archaeopteryx. All wing-propelled underwater fliers in birds have unusually large supracoracoideus muscles to elevate the wing during the upstroke (Rayner 1988b). Yet Archaeopteryx had no supracoracoideus (Ostrom 1976b, and above), and there is no evidence of another wing elevator muscle. Nonetheless, this brief digression is informative. The origin of flight may have followed a pathway appreciably distant from those normally envisaged, or discussed here. Both cursorial and arboreal models, as normally formulated, raise significant difficulties which have yet to be resolved. A combination of unusual, or possibly rapidly changing, environmental conditions may be responsible, and this may make such hypotheses resistant to physical modelling of the kinds reviewed here. Avian phylogeny and flight evolution In this essay I have shown how consideration of the sequence of character acquisition and transitions in the avian phylogeny closely parallels the biomechanical changes essential in the origin and radiation of flight, and indicates an initial origin of flight at relatively high air speeds with the continuous vortex gait, with subsequent radiation to encompass flight at rather slower speeds and the vortex ring gait. Both approaches support one another. In studying macroevolutionary transitions of this kind it is not possible to consider phylogeny and morphological characters in isolation of the evolving biomechanical functions that those characters perform. This risks circularity, since the characters used in determining the phylogeny may vary solely through diversity of the flight system, and it is not always possible to determine basal states or character polarity. In the theropodbird transition this is however not a serious problem, since the basal state is well known from the extensive record of theropods, and Archaeopteryx retains its significance with intermediate dinosaur and bird characters. As I have shown, based on evidence from the bony tail and the forelimb kinematics, it was also intermediate in its locomotor performance. I have also been deliberately equivocal in setting forward an interpretation of the behavioural correlates of the evolution of flight. I have several reasons for this. First, the subject is too polarized, and any argument becomes a hostage to fortune in an unnecessary debate. Second, the theropod fossil record is rich, but is not yet sufficient to confirm all of the claims or fantasies that have been advanced about the relationships, morphology and behaviour of Archaeopteryx and its relatives. Archaeopteryx was not arboreal, and its (larger) ancestors were obligate bipedal cursors. Third, the most contentious issue in any work on flight evolutionthe arboreal/cursorial dichotomyis artificial, and is, in Ostroms words of 1997, a garden path. The suite of hypotheses advanced here are intended as much more than simple compromises between extremes: they should identify the primary biomechanical challenges faced by the first birds, rather than the milieu in which it began to fly. Fourth, it is as much my intention in this essay to raise questions about the palaeobiological background to avian flight evolution as it is to answer them. And fifth, the available material is growing so rapidly that we must all be prepared to reassess hypotheses in the light of new material. The exciting finds of feathered theropods from China are a prime example of this. Nomenclature remains a challenge. I have followed the formal definitions of Padian & Chiappe (1998) and Padian et al. (1999), which encompass the existing fossil record and the established phylogenies for theropods and birds. This current position is consistent with a node-based definition of birds (strictly, of Aves) based on characters associated with flight, and thereforeindirectlydefines birds by their use of flapping flight. This definition of Aves will not necessarily be robust if the future brings finer resolution of transitional locomotor forms. The stem-based definition of Avialae is potentially more flexible in response to anticipated further knowledge of taxa with locomotor habits intermediate between Dromaeosauridae and Archaeopteryx. Whether such animals should colloquially be termed birds will no doubt be a matter of debate. Acknowledgements I am grateful to John Ostrom for the original inspiration to become interested in the evolution of flight in birds, and to Jacques Gauthier for the invitation to present this work at the Symposium in commemoration of Johns enormous contribution to the subject. I thank Luis Chiappe, Gareth Dyke, and Kevin Padian for their advice and assistance, particularly in preparing the phylogeny in figure 1, and Paolo Viscardi, Gareth Dyke, Robert Dudley, Philip Burgers and Mike Benton for commenting on the manuscript. References Abel, O. 1911. Die Vorfahren der Vgel und ihre Lebensweise. Verh. k.-k. zool.-bot. Ges. Wien 61: 144191. Beard, K. C. 1990. Gliding behaviour and palaeoecology of the alleged primate family Paromomyidae (Mammalia, Dermoptera). Nature 345: 340341. Beard, K. C. 1993. Origin and evolution of gliding flight in early Cenozoic Dermoptera (Mammalia, Primatomorpha). In Primates and their relatives in phylogenetic perspective, ed. R. D. E. McPhee, pp. 6390. 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Primitive in birdsKinematics amplitude:>55 little variation with speed3555 downstroke ratio:>0.5~0.5 stroke plane:antero-ventrally slanted from flight axisdorso-ventral (perpendicular to flight axis) upstroke:variable between species flexure at elbow and wrist wing deforms out of plane considerable pro-/supination wrist usually moves anterior to downstroke path (sometimes reversing)uniform and stereotyped flexure at wrist wing remains near-planar little pro-/supination wrist follows downstroke path  AerodynamicsLarge circulation in downstroke; zero circulation in upstroke Downstroke thrust and weight supportConstant circulation in down- and upstrokes Weight support throughout; thrust from downstroke, negative thrust from upstrokeMuscles Muscle (supracoracoideus or ? deltoid) required for upstroke wing elevationAerodynamic lift elevates wing in upstroke Table 1. Aerodynamic, kinematic and morphological characteristics of forward flight gaits in birds. (Hummingbirds are aerodynamically distinct from other birds and do not follow these patterns.)  Figure 1. A consensus phylogeny of birds and related theropods, based on information from Chiappe (1995 and this volume), Ji et al. (1998), Mackovicky & Sues (1998), Padian & Chiappe (1998), Padian et al. (1999) and others. This is not intended as a formal phylogeny, but rather to show how the sequence of acquisition of locomotion-related characters in the lineage is related to the evolution of flight aerodynamics and biomechanics (other characters determining the phylogeny are omitted). X denotes flightless lineages (as placed here, following Chiappe (this volume), Alvarezsauridae would not have had flying ancestors; some phylogenies have placed them as the sister group of Ornithothoraces). Feathers or homologous structures probably evolved more basally within the Theropoda; the location shown for this character is the most derived possible.  Thomas (1879) discussed the origin of birds and pterosaurs in the context of a set of Triassic saurischian dinosaur tracks from South Wales. He argued for a dinosaurbird relationship on the basis of the similarity of the tracks to those of ostriches and emus, following Huxleys Ornithoscelida, and proposed a cursorial origin of bird flight. 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