Advantages of flight
Birds have developed the power of flight to an extraordinary degree that sets them apart from other vertebrates, and they have done it with minimal loss of other forms of locomotion. Unlike bats, most birds can walk and run, and many can swim and dive well enough to catch fish and squid. Migrating birds fly airline distances over mountains, seas, and deserts, and thus gain access to remote habitats such as the arctic tundra, which are highly productive during a short season, but uninhabitable for several months of the year. On a shorter time scale, wading birds can exploit tidal mudflats, which are inaccessible on foot. Many food sources are accessible only to flying animals, from the "aerial plankton" of flying invertebrates to the fruits of forest trees that rely on birds and bats for dispersal of seeds. Trees, cliffs, and islands provide flying animals with nesting and roosting places where terrestrial predators cannot reach them. Although bats are supreme at catching insects in the dark, birds have the advantage in most other respects, thanks to a unique set of morphological and physiological adaptations.
The bird body plan
All birds share the same basic body plan, with relatively minor variations, despite being adapted to a tremendous range of habitats and lifestyles. Birds have inherited the bipedal body plan of the Archosaur branch of the reptiles, which also includes dinosaurs, pterosaurs, and crocodiles, but they have a number of distinctive modifications to the basic plan. The loss of the long balancing tail of bipedal dinosaurs means that the weight of the upper body no longer acts through the hip joint, but far ahead of it. Bipedal standing and walking with this "unbalanced hip" is made possible by the characteristic bird synsacrum. This is an expanded and elongated pelvis that is fused rather than articulated to the vertebrae. Postural muscles pull downward and forward on the rear end of the synsacrum, which acts as a lever holding the forward part of the body up. The bird ancestor's bipedal stance left the forelimb free to evolve into a wing that is structurally independent of the legs. Unlike bats and pterosaurs, in which the leg supports the inner end of a wing membrane, birds have been free to evolve the legs for perching, walking, running, and swimming, while also being able to use them for other functions altogether, especially catching and manipulating prey.
Birds have no diaphragm like that of mammals. Instead the curved synsacrum and sternum form the two halves of a bellows, which pumps air in and out of the body cavity. The lungs are small and compact, with "air capillaries" through which air is drawn into a system of air sacs beyond the lungs. The air and blood capillaries are arranged transversely to each other to form a "cross-current" arrangement, which is more effective than the dead-end pouches (alveoli) of mammal lungs for extracting oxygen from air at high altitudes.
The bird wing
The evolution of the small archosaur forelimb into a gliding wing required the wing span and surface area to be greatly increased, while retaining sufficient bending and torsional strength to support the weight of the body, suspended from the shoulder joints. The arm skeleton, consisting of the upper arm (humerus) and forearm (radius and ulna) provides the bending strength for the inner half of the wing only. Beyond the hand skeleton, the keratin shafts of the primary flight feathers provide the bending strength of the hand wing. Their bases are tightly bound by connective tissue to the reduced and rudimentary hand skeleton, with no freedom of movement in any direction. The bases of the secondary flight feather shafts are bound to bumps on the back side of the ulna, with some freedom to rotate downward and inward, but not upward or outward. The surface area of the hand wing is made up of the expanded vanes of the primary feathers, while the secondaries make up the area of the inner part of the wing. A leading-edge tendon with an elastic section in the middle joins the shoulder to the wrist, and supports a small triangular membrane ahead of the elbow joint. Smaller covert feathers smooth over the bases of the flight feather shafts, and seal the gaps between them. The free ends of each row of coverts overlap the feathers behind, in the manner of a tiled roof.
All of the aerodynamic force acting on a bird's wing is ultimately collected at the humerus, which has to support bending and twisting loads, with little or no compression or tension. The humerus shaft is a thin-walled, hollow cylinder of large diameter, adapted to carry these loads with a minimum amount of material. The central cavity is connected to the air sac system, and filled with air. Internal struts (trabeculae) prevent buckling of the load-bearing bony wall.
Likewise, the primary and secondary feather shafts are hollow, and filled with a keratin foam (parenchyma) which maintains the shape of the load-bearing keratin walls. The tail feathers are structurally similar to the flight feathers, with their bases attached to the rudimentary tail skeleton (pygostyle). They can be spread fanwise, forming an auxiliary lifting surface, which has been likened to an expandable delta wing, behind the main wing.
Comparison with pterosaurs
Both birds and pterosaurs originated in early Mesozoic times from the ancestral archosaur stock, which also gave rise to crocodiles and dinosaurs. They represent radically different solutions to the mechanical problems of flight, each modifying the basic archosaur body plan in a different way, unrelated to the other. All of the bending loads in a pterosaur's wing were carried by the bones of the arm and hand, ending in one enormously elongated "wing finger" (digit 4). There were no load-bearing keratin structures corresponding to the flight feather shafts of birds. Even those who interpret the parallel ridge patterns on pterosaur wing impressions as "stiffening fibers" concede that these ridges were not connected to the wing skeleton, and therefore could not transmit bending loads to the humerus. Unlike the vanes of flight feathers, the wing membrane had no bending strength, and had to be stretched between two bony supports, the wing finger and the leg. Like modern birds, later pterosaurs (pterodactyls) reduced the tail so that it lost its original function of balancing the weight of the upper body about the hip joint, but unlike birds, pterodactyls did not expand the pelvis to provide an alternative balancing mechanism for bipedal standing and walking. On the ground they must have been quadrupedal, somewhat like vampire bats, although the front "foot" was the end of the metacarpus rather than the wrist, as in bats. As judged by the wing span, pterosaurs ranged from sparrow-sized forms to 20 ft (6 m) pterodactyls. These thrived throughout the Cretaceous period, with even larger forms just at the end. However, all of them had slender bodies and large wings, somewhat like frigate birds. None were heavy-bodied like ducks or auks.
Comparison with bats
Bats are mammals, unrelated to either birds or pterosaurs, and are first known from the Eocene mammal radiation. They have a membrane wing somewhat similar to that of pterosaurs, but with all five digits contributing to the wing structure. Digit 1 (the thumb) projects forward from the wrist and is used for climbing. Digits 2 and 3 together form a stiff panel that allows the outer part of the wing to be pulled forward, creating tension that runs through the membrane to pull against the legs. Digit 3 supports the wing tip, and digits 4
and 5 control the profile shape of the wing membrane. The ankle joints and feet are quite similar to those of pterosaurs, and are used to curl the posterior edge of the wing membrane downward. There are muscles running fore-and-aft in the membrane, which are not attached to the skeleton but are used to flatten the profile shape of the wing. Few bat species are active in full daylight, perhaps because the wing membrane is susceptible to sunburn, or because of bats' dependence on convective cooling. Many bats make seasonal migrations within continental areas, proceeding in many short stages, but bats are apparently not capable of flying as high as birds, nor of covering such long nonstop distances. Whether pterosaurs could match the performance of birds in these respects is unknown.
Flight muscles and sternum
In both birds and bats, the spherical head of the humerus articulates with the shoulder girdle, and is free to swing forward, back, up, and down, and also to rotate about its own axis, within limits set by a complicated arrangement of ligaments. The pectoralis or "breast" muscle of both birds and bats does most of the work in powered flight, by pulling the humerus downward. It inserts on the underside of a ridge that projects forward from the base of the humerus. In birds, the inner end of the pectoralis muscle is attached to the body skeleton along a prominent keel, which projects from the mid-line of the sternum (breastbone), and also along the outer edge of the sternum where it joins the ribs. The humerus is raised
by the supracoracoideus muscle, which is attached to the sternum along the base of the keel, where it is entirely surrounded and covered by the pectoralis muscle. Its tendon runs up the coracoid, through a channel between the bones of the shoulder girdle, and curves over the shoulder joint, to insert on the top side of the humerus.
This arrangement is found only in birds, not in bats, which fly very well without an expanded keel on the sternum. In their case the two pectoralis muscles pull directly against one another, with only a small keel between them, or none at all. This shows that the keel, which is such a prominent and characteristic feature of the bird skeleton, is not a requirement for flapping flight. In bats the humerus is raised by the deltoid group of muscles on the dorsal side, as in other mammals and also in reptiles.
Heat disposal in flight
The flight muscles generate a large amount of heat in flapping flight, and this heat has to be disposed of in a controlled manner to maintain the body temperature within the required limits. Provided that the air temperature is well below the blood temperature, most or all of the excess heat can be lost by convection. Birds do this by passing a copious blood flow just below thinly insulated areas of skin that are exposed to the air flow, especially the sides of the body and the under-sides of the inner parts of the wings. These areas are covered when the wings are folded, thus avoiding loss of heat when the bird is not flying. If the air temperature is too high for convective cooling, the bird opens its beak and flutters the throat pouch, thereby cooling the blood by evaporating water from the upper respiratory tract. Evaporation also takes place from the lining of the air sacs, which penetrate many organs, including the interior of the pectoralis muscles. The keel of the sternum keeps these cavities open when the muscles contract, and its function is probably to permit direct evaporative cooling of the interior of the muscles.
In bats, the huge area of skin exposed to the air flow is ready-made for convective heat disposal. The wing membrane contains a system of blood vessels in which the flow is controlled to regulate body temperature. Most bats rely mainly or wholly on convective cooling, and only resort to evaporative cooling in emergencies.
Muscle power for level flight
Because a bird's body is much denser than air, the flight muscles have to work continuously, accelerating air downward so as to produce an upward reaction that balances the weight. The rate at which work is required (power) to support the weight is highest when the air speed is zero (hovering), and decreases at medium and high speeds. However, additional power is required to overcome the drag of the body, and this increases with speed. Because of their opposite trends, these two components of power produce a characteristic U-shaped curve when added together. There is a well-defined "minimum power speed" at which the mechanical power required to fly is lower than at either slower or faster speeds.
The margin of power available over power required dwindles as the size of the bird increases, eventually defining an upper limit to the mass of viable birds, which appears empirically to be in the region of 35 lb (16 kg). Modern flying birds are restricted to small sizes, when compared with the much wider size range of walking and swimming animals. Antelope-sized birds, such as ostriches and emus, exist but are necessarily flightless. Small birds have sufficient muscle power to fly over a wide range of speeds, but large birds like swans have only just enough power to fly very near the minimum power speed. Birds heavier than any living forms might have been possible under special circumstances in the past, for instance in a combination of landscape and climate that allowed reliable soaring, taking off from slopes in hang-glider fashion.
Metabolic power and aerobic capacity
Physiological experiments measure the metabolic power, which is the rate of consumption of fuel energy, as distinct from the mechanical power, which is the rate at which the muscles do work. A bird's "aerobic capacity" is the maximum sustained metabolic power of which it is capable, and this is determined by the capacity of the heart and lungs, not by the muscles. Only hummingbirds have sufficient aerobic capacity to hover continuously, although many small and medium-sized birds can hover anaerobically for short periods. Some very large birds such as condors have insufficient aerobic capacity for sustained level flight at any speed, and are forced to resort to soaring for sustained flight.
Gulls and ducks float on the surface of the water and use their feet in a fore-and-aft rowing motion, whereas more extremely adapted water birds such as loons and grebes have the legs set far back, and swing them in a more lateral motion, using the feet as hydrofoils. Auks and diving-petrels have wings of reduced size, forcing them to fly rather fast, with high wingbeat frequencies, but they also use their wings for propulsion under water. The aquatic wing motion is quite similar to flight, but at a much reduced frequency, with the wings partly folded. Gannets, petrels, and some albatrosses can also swim under water in this manner to a limited extent, diving a few meters below the surface. Penguins and the great auk (Pinguinus impennis) carried this line of evolution further, with wings too small to fly, but optimized as hydrofoils. The wings of penguins beat up and down (not in a rowing motion) and are convergent on the flippers of sea lions and marine turtles. Frigate birds do not swim or alight on the water at all, although their dispersal movements show that they spend weeks or months at a time over the open ocean, flying day and night.
Takeoff and landing
To take off, a bird has to acquire sufficient air speed over the wings to sustain its weight, either from forward motion, or by flapping the wings relative to the body, or (usually) by a combination of both. Birds up to the size of pigeons or small ducks can jump into the air from a standing start, and accelerate into forward or climbing flight, but larger birds have to run to get flying speed on a level surface. Swans use their large webbed feet alternately in a running motion to help them accelerate over a water surface, while cormorants and pelicans more often use both feet together. Large birds taking off from a tree or cliff drop to convert height into air speed. All birds head into the wind when taking off from the ground or water, as the wind then supplies part of the air speed that they have to acquire. If the wind is strong enough, petrels and albatrosses simply spread their wings and levitate into the air from the crest of a wave.
Landing into wind is obligatory, but newly fledged birds have to learn this, and often make spectacular errors by attempting to land across or down wind. In light winds, most birds slow down when preparing to land, by increasing the frequency and amplitude of the wing beat, tilting the wing-beat plane until the wings are beating nearly horizontally, and spreading and lowering the tail. Any residual downward and forward velocity (relative to the ground) is absorbed by the legs. Glide landings are often possible in moderate wind strengths, even for large birds. The body and wings are tilted up as the bird flares, with one final wing beat sweeping the wings forward almost horizontally, just before the wings are folded. Auks and loons land on water at rather high speeds, lowering their bellies into the water with the feet trailing behind, whereas ducks and swans swing their feet forward and use them like water skis. Gannets often enter the water in a shallow dive rather than alighting on the surface, while petrels and albatrosses slow down while gliding, and drop gently onto the surface. Guillemots (murres) nest on cliff ledges although they are not capable of flying slowly enough to land safely in such places. Their landing technique involves diving toward the cliff at high speed, then pulling up into a near-vertical climb. If this is accurately judged, the guillemot's
speed drops to zero just above the landing ledge, but if not, it has to dive away from the cliff, fly out to sea, and repeat the whole procedure.
The longest known nonstop migration is that of the Alaskan bar-tailed godwit (Limosa lapponica), which flies from the Alaskan Peninsula across the equator to the North Island of New Zealand, a distance of about 6,400 mi (10,300 km). The godwits build up fat before they depart, at the same time reducing the mass of organs such as the digestive system and liver, until about 55% of the total mass consists of fat. Like all long-distance migrants, they supplement the primary fuel (fat) by progressively consuming protein from the flight muscles in the course of the flight, "burning the engine" as the power required decreases. Although the fuel reserves are ample for the distance, this migration is remarkable because it is a formidable feat of navigation, requiring at least eight days and nights of continuous flight. The red knot (Calidris canutus) is another arctic breeding wader that migrates across the equator to high southern latitudes, with nonstop stages lasting several days on some routes. Many small passerine species cross the Mediterranean Sea and the Sahara Desert without stopping, while their American counterparts fly directly from the New England coast to the Caribbean Islands. Even longer distances are flown by species that are able to feed along the way, notably the Arctic tern (Sterna paradisaea), in which some individuals migrate from arctic to antarctic latitudes and back again each year.
Soaring over land
"Soaring" should not be confused with "gliding," which means flight without flapping the wings. The term "soaring" refers to behavior whereby the bird extracts energy from movements of the atmosphere, and uses this in place of work done by the flight muscles. Soaring birds do usually glide, but it is also possible to soar while flapping. Soaring is obligatory for many large birds, because of marginal muscle power. Slope soaring is the simplest method, in which the bird exploits rising air that is deflected upward as the wind blows against a hillside, or some smaller obstruction such as a tree or building. Thermals are vortex structures that float along balloon-like with the wind, containing an updraft in the central core and downdrafts around the outside. A gliding bird can gain height by circling in the core, but is carried along by the wind while doing so. At the top of the thermal, the bird glides off in a straight line, losing height until it finds another thermal and repeats the climb. When thermals are marked by cumulus clouds, soaring birds climb up to the cloudbase level. Away from sea coasts, this may be as high as 7,000 ft (2,000 m) above sea level in temperate latitudes, and higher in drier parts of the tropics and subtropics. Thermal soaring is the characteristic method of cross-country flight in large soaring birds such as storks, pelicans, and migratory eagles, while many raptors also use thermals to patrol in search of food. Lee waves are stationary wave systems that form downwind of hills. They can be exploited to higher altitudes than slope lift or thermals, but the technique is difficult. Canada geese (Branta canadensis) are known to use lee waves when migrating, and it is possible that some migratory swans may also occasionally use this method. Being slower than direct flapping flight, soaring migration is most advantageous to large birds, in which basal metabolism is only a small fraction of the power required for flapping flight. In small birds the energy cost of basal metabolism offsets any direct gains from soaring, because of the longer flight time.
Soaring over the sea
The trade wind zones of the tropical oceans cover a vast area in which the weather is predominantly fair with small, regularly spaced cumulus clouds. These are the visible signs of thermals, which are caused by the air mass being convected toward the equator over progressively warmer water. Although weaker than thermals caused by direct solar heating of a land surface, trade-wind thermals continue reliably at all hours of the day and night, and provide frigate birds with the means to disperse across the oceans without ever alighting on the surface. The middle latitudes, where stronger winds prevail, are the home of the petrels and albatrosses, especially in the southern hemisphere. The medium-sized and large members of this group skim with no apparent effort in and out of the wave troughs, sometimes very close to the surface, sometimes pulling up to 50 ft (15 m) or so, seldom flapping their wings. A petrel or albatross replenishes its air speed with a pulse of kinetic energy each time it pulls up out of the sheltered zone in the lee of a wave, into the unobstructed wind above. As the energy comes from the relative motion between the air and the waves, birds that use this technique are confined to the interface between air and water, just above the surface. Albatrosses can also slope-soar in zero wind by gliding along the leading slopes of moving waves. Pelicans, boobies, and other pelecaniform birds soar over slopes and cliffs when they come ashore to breed, but use mainly flapping flight at sea, as do gulls and auks.
Altitude of bird flight
Most birds fly near the earth's surface most of the time, except for soaring species, which climb to cloudbase or as high as convection allows. With the exception of frigate birds, most seabirds spend their entire lives within 100 ft (30 m) of the sea surface, except when they come to land, and soar in slope lift or thermals. Radar studies reveal that passerines typically fly at heights up to 10,000 ft (3,000 m) above sea level on long migration flights, while waders may fly as high as 20,000 ft (6000 m). The reduced air density at high altitudes requires birds to fly faster than at sea level, and to produce more muscle power, but there may be a small increase in range due to reduced wastage on basal metabolism, caused by the shorter flight time. The "cross-current" lungs of birds appear to give them an advantage over mammals (including bats), when it comes to extracting oxygen from low-density air. Lower air temperatures aloft reduce or eliminate the need for evaporative cooling, but reports of swans migrating at 27,000 ft (8,200m) are apocryphal. Such large birds cannot climb to great heights by muscle power alone. It is conceivable that they could do so by exploiting lee waves, but air temperatures below −58°F (−50°C) would present physiological problems.
Origin of flight
Scientists realized in the nineteenth century that both birds and pterosaurs belong to the same branch of the reptiles as dinosaurs, and it is a matter of definition whether birds actually "are" dinosaurs, or whether they developed as one or more distinct strands of the original archosaur stock. Among living mammals, cobegos, flying squirrels, and their marsupial counterparts suggest an obvious route for the evolution of flying forms from arboreal ancestors. Pterosaurs and birds could have originated in a similar way, if we suppose that there were two parallel groups of small, arboreal archosaurs early in the Mesozoic. One such group, ancestral to the pterosaurs, would initially have resembled a flying squirrel, with a membrane stretched between the fore and hind limbs, and would then have extended the wing span by lengthening the wing finger. The other group, ancestral to birds, would have developed flight feathers from modified scales, extending the wing span and area without involving the legs in the wing support structure. Whether or not this is exactly what occurred, the two groups must have diverged in Triassic times, long before any of the known Jurassic birds or birdlike reptiles.
Flight in past times and on other planets
The two physical factors that most strongly constrain flying animals are gravity and air density. On a planet with stronger surface gravity than Earth, the maximum size of flying animals would be even more restricted than it is here, while a higher air density would ease this limit, irrespective of the atmospheric composition. It is likely that the Mesozoic atmosphere was indeed denser than the modern one, and this helps to explain the prolonged success of pterosaurs with 20 ft (6 m) wing spans. However, the largest pterodactyls, which flourished briefly in the last days of the Cretaceous period, would appear to require a reduction in gravity to make them feasible, and that is more difficult to explain.
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Colin Pennycuick, PhD, FRS