evolution of ﬂight in animals · 2 evolution of insect ﬂight several theories have been...

Evolution of flight in animals

U.M. Lindhe NorbergDepartment of Zoology, University of Göteborg, Sweden.

Abstract

The evolution of flight in animals has long been debated and different hypotheses have beensuggested for their origins. Controversial opinions about morphology, locomotion and flight evo-lution can, however, be understood by functional approaches, e.g. by biomechanical treatmentsand aerodynamic models. New fossils of proto-fliers will constantly increase our understandingof 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 wereused for underwater swimming and for circulating water over the gills in aquatic nymphal stagesof non-flying insects. They were later raised above the water surface for wind-propelled skim-ming, and beating of the winglets enabled powered skimming. Eventually, flight muscles becamestronger and were used for true powered flight. Vertebrates most probably developed flappingflight via gliding intermediates. The conflicting ‘ground-up’ model includes a number of limi-tations. Several modifications of the various evolutionary steps in the main theories have beensuggested, but particular stress has been laid on whether a gliding stage was included or not. Interms of energy, time, and aerodynamics, the gliding model is the most attractive alternative. Ifthe ground-runner began to use hang-gliding on steep slopes, a running mode of life before theanimal could fly would be beneficial. Morphological changes must have evolved in small stepsover a long time span, and each new modification towards flight must have contributed to fitnesslong before the proto-flier could fly.

1 Introduction

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

www.witpress.com, ISSN 1755-8336 (on-line) WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press

doi:10.2495/1-84564-001-2/1c

Evolution of Flight in Animals 37

The crucial thing in the evolutionary pathway to powered flight is the production of lift andthrust. While aircraft produce thrust with the engine, animals have to flap their wings. The mostimportant parameter affecting the lift and drag coefficient over the entire size range of flyinganimals and machines is the Reynolds number, which represents the ratio of inertial to viscousforces in a flow. It is Re = ρul/µ, where ρ is the density,µ is the viscosity of the flow, u is the speedand l is a characteristic length (such as wing chord). Low Reynolds number flight and flappingwing dynamics, which are characteristics of animal flight, involve large-scale vortical motionand detached flows. This is why the Strouhal number enters as a second important parameter forthe dynamics (a dimensionless value useful for analysing oscillating, unsteady flow and whichis a function of the Reynolds number; St =ωa/u, where ω is the oscillation frequency and a isthe amplitude, such as wingtip excursion). A flexible wing has superior performance to a rigidaeroplane wing in this situation. An important benefit from flapping wings of animals comparedto fixed-wing aircraft is that animals can manoeuvre better and also make compensating wingmovements to avoid stall. Animals can also change wing form to meet different flight conditionsand requirements.

Insects make up the most diverse and numerous animal class with about 750 000 recordedspecies. Tiny insects operate at Re< 10 and larger insects at Re ≈ 102−104.At very low Reynoldsnumbers viscous forces are large and the flow is more laminar, whereas inertial forces increase withincreasing 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 is106–108.

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, wemay have put them a separate class, like birds, and separate from reptiles. But birds are moredifferent from reptiles than pterosaurs, because they have wing feathers. Long fingers and aflexible membrane make up the bat wings, and it is still debated whether the pterosaur wing wasmade 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 Thomasand Norberg [1]). An early theory is that insects evolved flight by jumping and gliding downfrom trees, like early birds and bats [2–4]. Flattened outgrowths at the top of the thorax allowedinsects to maintain stable flight. Progressively increasing size of the extensions improved glideangle, they became moveable, and incipient flapping eventually led to powered flight, as in thevertebrate model [3, 4].

A second theory suggests that evolution of insect flight may have originated with relativelylarge, terrestrial, leaping insects, which launch themselves voluntarily into the air, as many moderninsects 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 dispersalby 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 Mardenand 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 beone stage in the origin of flight. Fossil and developmental evidence indicate that insect wings are


38 Flow Phenomena in Nature

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 swim-ming and for circulating water over the gills in aquatic nymphal stages of non-flyinginsects. Bottom left: The plates were later raised above the water surface for wind-propelled skimming, and beating of the winglets enabled powered skimming. Thefigure shows a male stonefly sailing. Bottom right: Female stonefly sailing. The bottomdrawings are based on photographs by Marden and Kramer [9].

homologous to specific epipodites (gills, with respiratory function) of crustacean limbs (tracedby gene expression; [10, 11]). Steps leading to flight could have been: (1) articulated, movablegill-plates were used for underwater swimming and for circulating water over the gills in aquaticnymphal stages of non-flying insects; (2) gill-plates, functioning as winglets, were raised abovethe water surface for wind-propelled skimming; (3) beating of the winglets enabled poweredskimming; (4) the flight muscles became stronger and used for true powered flight. This hypothesismakes the gill-to-wing transition possible. Modern stoneflies, which are an ancient group thatdiffers little from their Carboniferous ancestors, use skimming in this way and might be regardedas a functional intermediate form.

In surface-skimming there are three sources of water drag: (1) friction between leg and watersurface film, (2) inertial drag due to continuous acceleration of water out of the moving dimplesas the insect skims on, and (3) inertial drag due to the generation of ripples. The weight of thedisplaced 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 greatlyenhanced by the ground-effect; reduction of the aerodynamic induced power could be reduced by50% 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 andtreated the different theories of the origin of flight in birds. Most aspects of early birds were also



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-glidingon steep slopes [26] (Fig. 2). Morphological changes must have evolved in small steps over a longtime span, and each new modification towards flight must have contributed to fitness long beforethe proto-flier could fly [15–17].

Whether birds evolved flight via a gliding stage (starting from some height or slope) andworking 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 suggestedbut particular stress has been laid on whether a gliding stage was included or not, and also on theclimbing ability in ancient birds.

Bock [20, 21] identified the adaptive advantage of each intermediate stage in the arborealscenario: ground-living insectivorous proto-birds might have begun to forage among bushes andthen to climb trees to escape from predators, to roost at night, or to nest. Powered flight thenevolved via gliding from trees. But Caple et al. [27] argued that lift could not be produced when agliding proto-flier began to flap its wings. Norberg [15–17], however, showed that a transition fromgliding to active flight is mechanically and aerodynamically quite feasible. By using aerodynamicand optimal foraging theories Norberg showed that, for every step along the hypothetical routefrom gliding, through stages of incipient flapping, to fully powered flight, there would have beenan advantage over previous stages in terms of length and control of the flight path. Asymmetricwing 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 treesand stretching out their forelimbs before head-up landing on a stem. Increased forelimb areawould 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 mostimportant point in Norberg’s [15] detailed aerodynamic model, namely that thrust is produced in agliding animal with slight flapping, and Rayner [24] also suggested that thrust had to be producedduring gliding to flatten out the glide path. Norberg showed mathematically that a net thrust forcecan be produced even during very slight flapping in a gliding animal while the necessary verticallift 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 theproto-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-runningand 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 froma ground-running and jumping mode of life to active flight seems very difficult because theproto-bird had to work against gravity [15, 23]. In the running animal the aerodynamic dragfrom extended flapping forelimbs would increase with speed squared and retard it, requiring stillmore work to reach the speed needed to generate the lift and thrust required for take-off. Longerforelimbs and feathers would further have increased drag and the work necessary for the samespeed. Such a proto-flier, that was supposed to flap its wings to add to the running speed and/orfor stability and control of the body, must produce not only the power necessary for flapping butalso 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 bygliding 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 butit includes a number of limitations. Neglecting the wing drag, it may be energetically cheaper torun–leap–glide than to run continuously, with the savings increasing for smaller animals [38]. Thiswould thus make sense for an animal running with retracted wings and making regular intermittentleaps followed by shallow glides on extended wings. The savings are, however, much less thanthose realized in the trees-down scenario. But modern cursorial animals seldom travel so fast incommuting runs; they usually reach only half the speed necessary for take-off. It seems unlikelythat 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 effectwhen flapping their wings extensively to produce thrust, but there are some limitations with thisscenario [26]. First, thrust is an effect of the resultant aerodynamic force produced, or merelythe 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 thisresultant is the lift force counteracting gravity. Second, in animals and aircraft flying or hoveringclose 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 oppositeimage-vortex system with no flow normal to the ground plane. For flapping wings this flow may notbe steady and inviscid, and the ground boundary layer may separate [39]. The main benefit whenflying 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 groundeffect 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 thispurpose, but proto-birds had limited possibilities for this. The induced drag component becomesa smaller part of the total drag at those high speeds proposed for the running proto-bird. Sincetotal drag increases with speed squared, it is difficult to see how the lift-to-drag ratio could havegradually increased during the evolutionary stages in this scenario [26].

In terms of energy, time, and aerodynamics, the gliding hypothesis seems to be the mostattractive alternative [15–17], but arguments are raised about structural limitations in the earlyproto-birds. Rayner [41], however, demonstrated that the evolution of powered flight through agliding wing is entirely consistent with the existing fossil record of birds, and that this hypothesismakes 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 themacroevolutionary change from reptile to bird are summarized in Table 1.

3.2.1 Foraging agilityThe first steps towards aerial locomotion were probably taken from trees or cliffs. Tree-climbingand clinging among branches and leaves in insectivorous proto-birds would have required bettercontrol of movements with accompanying improvements in sense organs, neuromuscular controland external morphology [20]. These adaptations increased foraging agility, decreased the risk ofbeing eaten, and thus increased fitness. Similar adaptations may also have occurred in proto-birdsmoving around on cliffs or steep slopes. Hang-gliding proto-birds would also have benefited froma 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 loadingforaging areas

4. Gliding with some Ability to determine Neuromuscular control,manoeuvrability direction of the glide wing coordination,

wing camber5. Slight flapping flight Movements for stability, Higher aspect ratio,

manoeuvres in turning lower wing loadingand landing

6. Flapping flight with Better flight performance, Better neuromuscularsome manoeuvrability commuting control, more sophisticated

wing characters,camber for slow flight

7. Flapping flight with Aerial prey-catching, Highly sophisticated winghigh manoeuvrability hovering etc. characters (slots),

keeled sternum,musculoskeletal systemlike that of modern birds

3.2.2 Feathers and gliding surfaceExtensions of skin would be useful as parachutes if the animal fell or needed to escape. The skinflap in front of the arm skeleton of the bird wing may have originated for this purpose. Differenthypotheses have been presented about the evolution of feathers. Bock [42] suggested that feathersdeveloped as insulating devices, and that development of elongated feathers would have reducedthe rate of fall and promoted safe landings. Elongated feathers on the forearms could later haveacted as gliding surfaces and eventually been developed into primary feathers that give thrust inflapping flight.

Another theory is that feathers evolved directly for gliding flight [22]. But Xu et al. [43] reportedevidence for proto-feathers in a new basal tyrannosauroid from China; one of the specimenspreserves a filamentous integumentary covering, similar to that of other coelurosaurian theropodsfrom western Liaoning, which provides the first direct fossil evidence that tyrannosauroids alreadyhad proto-feathers. The authors suggested that this supports the theory that feathers evolved asinsulating devices.

3.2.3 GlidingClimbing and gliding may have been used as main types of locomotion during foraging in theearly proto-birds. Maximization of net energy gain during foraging in trees might have been areason 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 thenglide 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 evolutionof 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 downeach tree and then run to the next tree (Fig. 2). This locomotion mode is used, for example, bywoodpeckers, treecreepers, and gliding mammals. Once a glide surface had evolved, the proto-birds’ energy and time demands for locomotion during foraging might have been considerablyreduced and their foraging efficiency improved.

Because the glide surface was small in the initial stages, the first glides must have been steepwith low lift-to-drag ratios. But even steep parachuting jumps from trees (or other heights) reducedthe 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 whateverit has to glide on. Such behaviour strongly promotes every incipient skin, hair or feather area forgliding purposes.

Zhang and Zhou [46] described the fossil of an enantiornithine bird from the early Cretaceousthat has substantial plumage feathers attached to its upper leg (tibiotarsus). They suggested thatthese feathers, that are curved and relatively long, may be remnants of aerodynamic feathers, in



accordance with the hypothesis that birds went through a four-winged stage during the evolutiontowards flight [47]. Remnants of leg feathers occurred also in the gliding dinosaur Microraptor[47] and in Archaeopteryx [12].

3.2.4 Hang-glidingAerodynamically, the hang-gliding scenario is quite possible [26]. The gliding proto-birds thenworked with gravity, not against it. The gliding could have started from a running behaviour, whichfits 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 wouldnot only have got a better overview of the foraging area by gliding over it, but it may also havebeen easier to surprise a prey (such as some insect or small reptile) from above than when chasingit on ground. When diving down with retracted wings the proto-bird could hit the prey with its ownweight, and thus easier kill or paralyse the prey, like many hovering birds of prey and jumpingmammals (such as foxes) do.

3.2.5 Stability and neuromuscular controlA gliding animal needs good control of movements to be able to retain or adjust flight direction andgliding angle to reach a particular destination. Some characters needed for control and stabilitymay have occurred in the early gliders, as they do among modern gliding animals. The selectionpressure for good control and manoeuvrability in the gliding proto-flier may have evolved stepwiseand progressively along with the capability of gliding. This includes not only the evolution oflarger wings but also wing movement coordination, such as twisting and retraction, following theevolution 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, whichwould require higher manoeuvrability, which could not have evolved until true flight was wellestablished.

Stability and control of movements could/can easily be obtained in several ways (Fig. 3, Table 2).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 nervoussystem 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 theneuromuscular system, the structurally conditioned stability found in earlier forms became lessimportant, 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 birdsand birds of prey but also for flying prey. However, stability is sometimes needed in extantfliers.

3.2.6 FlappingFrom the beginning, slight flapping was probably used as movements for stability and for manoeu-vres in turning and landing. When flapping became more powerful it could also be used to increasethe glide path length by providing thrust [15]. This would make locomotion between foragingsites more efficient both in terms of speed and energy savings.

Increased wing area reduced wing loading (weight/wing area) and gliding speed, allowingsafer landings. Elongation of the wings increased aspect ratio (wingspan2/wing area; a measureof wing shape and aerodynamic efficiency) and lift-to-drag ratio (L/D), resulting in shallowerglides. 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 onthe left wing and decrease lift on the right wing because of the higher angle of attackon the left wing. The force difference between the wings will lift the left wing againand restore the bird to the horizontal. (c) Partial retraction of the left wing decreasingleft wing and thus lift. L and L′ are the lift forces and Lv and L′

v are their vertical liftcomponents. The positions of the wings are in the middle of the downstroke. Modifiedfrom [17], courtesy of Springer-Verlag.

this, together with the ability to coordinate the movements, eventually led to fully powered hori-zontal flight. Radiation to different habitats led to different wing forms, and the evolution of moresophisticated 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 ofvorticity patterns [3].

For a proto-bird the size of Archaeopteryx with a wingspan of 60 cm and a glide speed ofabout 7 m/s the wingbeat must be about 6–7 strokes/s [15, 16], given that the duration of thedownstroke equals that of the upstroke. However, if the proto-bird had beaten its wings fasterduring the upstroke than during the downstroke, the wingbeat frequency could be reduced to2 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] modelshows that the wingstroke amplitude increases almost linearly with the flapping speed and that itis small at low speeds.



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

Pitch stability and control (about the body’s transverse axis):Structural adaptation and neuromuscular control1. A long, sturdy, dorsoventrally flattened tail (as in Archaeopteryx)2. Downward and upward movements of the tail3. 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 control1. Long, broad wings with rounded tips2. Sweepback and upward deflection of the wings (dihedral) creates

restoring moments upon sideslip3. 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 control1. Long, broad wings with rounded tips2. Tail movements3. 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 whetheror 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]; thecurvature of the claws of Archaeopteryx is similar to that of modern tree-climbing and perchingbirds [50]. The young of the hoatzin, which is the only modern bird with claws on free fingers, arebush- and tree-climbers. However, Burgers and Padian [31] argued that highly curved claws wouldalso 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 quicklybetween terrestrial and arboreal environments. The basilisc (Basiliscus vittatus) is an example ofa very fast-running quadrupedal reptile that can even run over water surfaces to escape predatorsand climb trees. Furthermore, as mentioned above, a good running ability is compatible with thehang-gliding theory [26]. Arnold [52] concluded that Archeopteryx was unlikely to have used itsforelimbs for climbing, but that this is not necessarily excluded for the first fliers. Arnold furthersuggested that the posteriorly directed thumb of birds indicates a climbing or perching phasearound the time when flight evolved.

Another argument against the trees-down theory has been the lack of trees in the SolnhofenLimestones (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, forflight evolution may have been initiated much earlier when the flora was different, or even in otherareas. They may also have evolved flight through gliding from other heights or in steep slopes (assuggested 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 againstthe gliding theory.



3.2.8 Did Archaeopteryx fly?Whether Archaeopteryx were capable of powered flight or if they were only advanced gliders isnot a simple question. Dominiquez Alonso et al. [54] used computed tomography of the brainand inner ear of Archeopteryx and concluded that this bird had acquired the derived neurologicaland structural adaptations necessary for flight. Regression analysis shows that the brain volumeof Archaeopteryx was between those for modern birds and Diapsid reptiles and archeosaurs. Anenlarged forebrain suggests that it had also developed enhanced somatosensory integration neededfor 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 upstrokewas powered primarily by the deltoid muscle [57]. The lack of a morphologically derived supra-coracoideus muscle and the skeletal features associated with it, means that Archaeopteryx wereapparently incapable of high-velocity rotation of the humerus about its longitudinal axis duringthe 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–downwardsto being directed upwards–outwards as in modern birds. In Archaeopteryx the laterally facingglenoid of the shoulder joint was intermediate in orientation between ancestral reptiles and mod-ern birds and provided for a substantial degree of wing elevation. Thus, Archaeopteryx couldelevate wings well above the horizontal plane through the shoulder, preparatory to a lift-producingdownstroke [58]. The presence of a semilunate wrist-bone (a reptilian character) in Archaeopteryxmay 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 musclewas too small for powered flight in Archaeopteryx, because its sternum (breast-bone) lacked akeel. However, the main function of a bony keel of the sternum may not have evolved as a needfor increased area of attachment, but to prevent internal air cavities of the pectoral muscles fromcollapsing when the muscles contract [25]. In modern birds these muscles contain air cavitieswhich are connected to the interclavicular air sacs, providing internal evaporation surfaces forheat without the intervention of the blood stream. In bats, the heat is removed from the musclesprimarily by the blood and they lack an ossified sternum keel. Instead bats have a keeled, ossifiedmanubrium of the fore part of the sternum from which a ligamentous sheet extends backwards inthe 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 thesternum, the clavicles and coracoid bones in the pectoral girdle, the ribs, and ligaments connectingthese 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 pectoralmuscle 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 concludedthat Archaeopteryx lacked most of the key features associated with manoeuvrable and advancedflight. He showed elegantly how the wrist in mallard ducks are highly specialized to meet forcesduring flapping flight; the carpometacarpal bones are formed in such a way that they preventtwisting movements of carpometacarpus, providing a rigid structure. Vazques suggested thatthis mechanism prevents hyperpronation (extreme downward rotation) during the downstroke inflapping flight and supination (upward rotation) during gliding flight. However, the aerofoil actiondoes not usually function in the way described by Vazquez, so the risk of hyperpronation in the



downstroke is minimal. Neither does any airstream usually meet the upper side of the wings duringgliding, causing supination as he suggested. No turbulence above the wings may be strong enoughto provide such forces. The problem instead, for a proto-bird like Arcaheopteryx was to obtainoverall 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 havebeen 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 restrictedArchaeopteryx 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 achievingpowered flight with less than one-half of the flight-muscle volume of modern birds [51, 67]. Manymodern reptiles seem capable of generating particularly high levels of anaerobically supportedmechanical power during short bursts [68]. Ruben [51] further suggested that the evolution ofavian endothermy is likely to have been accompanied by the development of enlarged flightmuscles composed of aerobic muscle fibres for sustained flight.

The absence of a sternal crest and a calcified sternum, a simple pectoral girdle similar to thatof non-flying theropods (the reptilian ancestors to birds), and with a lateral-facing glenoid (thejoint between the upper arm and the shoulder), the downstroke is regarded to be rather weak anddorsoventral, and with little pronation [41]. Based on the inability to produce a rapid upstrokewith supinated wings, and on the fact that the downstroke was poor and dorsoventral, Raynerconcluded that Archaeopteryx were incapable of slow flight and more adapted for fast cruisingflight, with low agility and manoeuvrability. O’Farrell et al. [69] suggested that Archaeopteryxrelied substantially on lift enhanced by ground effect.

Advanced flight feather characteristics with aerodynamic function, such as vane asymme-try [70], dorsoventral stiffening [71], and backward curvature [72] (Fig. 4), were present inArchaeopteryx. Thus, as in modern birds, Archaeopteryx had the structural asymmetry of theflight feather that are essential for automatic adjustment of the feathers for optimal angle of inci-dence throughout the wingbeat cycle, despite continuously varying directions and velocities ofthe 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-wingfeathers, forming wing-tip slats. Modified from [72].



fairly advanced fliers, although these feather characteristics would also be beneficial for a manoeu-vrable glider. However, it seems unlikely for flight feathers to have been so strongly curved ina pure glider as it indeed was in Archaeopteryx [72, 73]. Feather asymmetry is highly benefi-cial for both manoeuvrability and flapping flight, which evolved step-by-step and most probablysimultaneously [15–17]. The leading-edge feathers in Archaeopteryx show the curvature that is aprerequisite for the automatic adjustment of angles of incidence at the primaries throughout thedownstroke, provided that they separate [72]. Four primary feathers of increasing length made upthe 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 lowthat 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 ladderor concertina vortex wake may have been produced during flapping, which may have been someintermediate 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 producea rapid humeral rotation and upstroke, instead, the deltoid muscles may have worked to elevatethe wings [58]. However, a rapid upstroke may not have been needed [15, 16]. The presenceof a semilunate carpal in the wrist may have served for some automatic supination (upwardrotation) of the hand and metacarpus [61].

2. The wing feathers of Archaeopteryx had stiffened rachis [71], vane asymmetry [70], thestructural asymmetry and curved shafts essential for automatic adjustment of the feathersfor optimal angles of incidence throughout the wingbeat cycle [72], and the primaries couldseparate 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 birdsA number of new birds from the early Cretaceous have recently been described [74–79], which lendinsight into the understanding of the evolution of birds and bird flight and of the flight capabilitiesof ancient birds. Fossil birds from Late Jurassic and Early Cretaceous demonstrate a number ofadvanced characteristics that signal an evolutionary progress towards powered flight [60]. EarlyCretaceous 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 ofmodern birds. Caudal reduction, reducing overall weight, took place before the evolution of flightand 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 aerodynamicmodel presented by Norberg [15, 17] applies to all three flying vertebrate groups.

Proto-bats might have been tree-living omnivorous mammals.Adaptations for downward climb-ing 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 mostmicrochiropteran bats.



4 Conclusion

Norberg [17] wrote in her book Vertebrate Flight: ‘the behaviour of ancient animals and theevolution of flight will probably always be a subject of contention, and although we may neverknow for certain if we have found the right answers, we can always distinguish the possible from theimpossible, the probable from the improbable’. From aerodynamic considerations, gliding mostprobably preceded flapping. The animal then worked with gravity, not against it, as in upwardleaps from the ground. Norberg’s [15] aerodynamic model applies to the transition from gliding topowered flight regardless of whether gliding occurred from trees or some other elevation, or evenfollowed from short glides in steep slopes (hang-gliding; [26]). With the running–hang-glidingscenario the problem whether proto-birds could climb trees or not is eliminated.

Archaeopteryx possessed several characters important for flight. Its osteology, myology andwing form indicate that it was capable of flapping flight. The specific geometry and morphologyof the hand-wing feathers are certainly a result of aerodynamic demands; they show a strikingsimilarity with those of modern flying birds. Although some of the flight characteristics werenot highly advanced, the available evidences, taken together, indicate that Archaeopteryx was notonly a good manoeuvrable glider but also capable of powered flight, even though it may not havebeen an advanced flapper.

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