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A.M. ZOOLOCIST, 2:161-166(1962). GLIDING AND FLIGHT IN THE VERTEBRATES D. B. O. SAVILK Plant. Research Institute, Ottawa In this paper I shall try to review the evolution of gliding and true flight, indicate some refinements of flight in birds, and present some problems that reveal our ignorance. Although engineers and aerodynamicists have made some significant contributions to our understanding of animal flight, their work has largely been unavailable to biologists. Since flight is the most distinctive attribute of birds as a class, the small amount of serious attention given to it by biologists is a matter of concern. Without some understanding of flight it is hard to see how the most can be made of studies in comparative anatomy, physiology, ethology, ecology, evolution, and taxonomy. Some action to remedy this situation is surely overdue. Aerial locomotion is conveniently treated under parachuting, gliding, and flying, although these categories intergrade freely. Soaring might be treated separately, but is legitimately regarded as gliding with the downward gradient balanced by thermal or mechanical updrafts. In the flying fishes (Exocoetus) we find what Gray (1953) calls velocity gliding; they depend on the kinetic energy of their moving bodies. Glides of'50 yards are not uncommon and this distance may be greatly exceeded in turbulent conditions. It has been estimated that such glides require a take-off speed of 30-35 mph, a speed unbelievably high for normal swimming. However, photographs show that, after the body breaks out of the water, the tail continues to drive the fish forward. Thus we have an analogy to a hydroplane rising on to the step. I wish to acknowledge a grant from the Frank M. Chapman Fund of the American Museum of Natural History to defray the cost of attending the A.A.A.S. meeting at Denver to present this paper. All other aerial vertebrates seem to have started as parachuting jumpers. The case for what Heilmann (1926) called the cursorial pro-avis seems scarcely tenable; for a substantial wing development would be needed before it could become adaptive, whereas the slightest fringe of feathers would be adaptive in checking the fall of a parachuter. Parachuting is here used in the sense of Oliver (1951) for a reduced rate of fall with a gradient steeper than 45°. It involves balance but generally little or no steering. It is clearly adaptive in protecting from injury in accidental falls, as an escape mechanism, and in pursuit of prey. A few amphibians have reached this stage but none have progressed further. It was first reported by Wallace in a Malayan frog, Rhacophorus nigropalmatus, to a somewhat sceptical world. This species has recently been studied and filmed by Professor John Hendrickson of Kuala Lumpur, who has shown that it is a competent parachuter, coming down in a stable attitude at about 60° gradient. He states (in litt.) that it seems to have little power of steering, but that as it is evidently very short-sighted such ability might have little value. Cott (1926) made the first important study of an aerial frog. He showed that a Brazilian tree frog, Hyla venulosa, fell slowly, always belly down, at a gradient of about 60°, with the legs spread laterally. The European Hyla arborea and Rana temporaria, of about the same size and structurally no worse equipped to check their fall, fell vertically, gyrating wildly and landing heavily. Thus the first requirement in parachuting seems to be behavioral, through the development of attitude control, rather than structural; but it may be noted that in Rhacophorus we do find long, fully webbed toes and lateral flaps of skin on the limbs. (161) 162 D. B. O. SAVILE Among the reptiles there are several parachuting lizards and some tree snakes (Chrysoplea and Dendrolaphis). Oliver (1951) noted the same distinction between parachuting Anolis carolinensis and the fence lizard (Scleoporus undulatus) that Cott did between his frogs. The latter fell heavily straight down with constant thrashing. The" tree snakes check their descent by pulling in the abdomen and flattening the body, obviously a highly unstable aerodynamic form demanding considerable nervous and muscular control. The only true gliders among living reptiles seem to be the so-called flying dragons (Draco) of Indo-Malaya. Here we have a flattened body with a wing-like membranous extension, supported by the last six or seven ribs and capable of being folded like a fan. Draco volans is a skilled glider that can steer well enough to land on a selected tree; and it must be highly maneuverable, for Hendrickson (in litt.) reports a pair in a courtship chase performing a full roll—a difficult trick even under power. The only reptiles to achieve true flight were the Jurassic and Cretaceous pterosaurs. The wing was mainly supported by an enormously elongated fourth digit. The hind limbs may have been partly included in the patagium, which would have simplified flight control. Smith (1952) has pointed out that the relatively primitive Rhamphorhynchus had a long tail with a horizontal paddle at the tip, which was clearly a stabilizer with a long moment arm to control pitching movements. In the advanced pterosaurs, culminating in Pteranodon, the tail was almost completely suppressed, as in modern birds; this makes it clear that an improved nervous system had allowed inherent stability to be sacrificed for improved maneuverability. A parallel change took place early in birds. Archaeopteryx had a long tail that was typically reptilian except for the paired feathers along the sides; but the Cretaceous birds had an essentially modern tail structure. The pterosaurs were actually perhaps only what the aeronautical engineer would call powered gliders—sailplanes with just enough power for brief use. Whether, as reptiles, they had adequate energy sources for sustained flight cannot be decided. The lack of evidence for adequate flight muscles is more serious. Little Rhamphorhynchus, with a span of perhaps 4 ft, had a flimsy pectoral girdle and a very small sternum. Pteranodon had a larger sternum and a strengthened girdle with a new structure, the notarium, between the scapulae. But Pteranodon had a body about the size of a swan's and a span estimated at 25 ft. I suspect that most of the muscle capacity was needed just to lift the wings as the animal launched itself from a cliff. The notarium perhaps served to keep the wings from lifting too far above the horizontal under the action of air pressure as well as to anchor lifting and trimming muscles. I cannot conceive an animal capable of beating such wings continuously and being light enough to fly at all. If, as their slender beaks suggest, these animals were fish-eaters, they probably soared over cliffs like a gull and over wave crests like an albatross or shearwater. Among mammals we have various parachuters and gliders, but true flight is achieved only in the bats, in which a patagium is extended by greatly elongated radius and second to fourth digits, and embraces most of the hind legs and often the tail. This type of wing structure precludes the aerodynamic refinements that are found in birds. It is thus only to be expected that bats should be slow fliers and generally quite small. In some respects the gliding mammals are more interesting than the bats. It is clear that parachuting has developed repeatedly in arboreal mammals. Active animals that jump from branch to branch must be partly preadapted to parachuting through an improved sense of balance and short reaction time. If a red squirrel (Tamiasciurus hudsonicus) is shaken out of a high tree it spreads its legs and comes down in GLIDING AND FLIGHT the familiar attitude of the flying squirrels. At first it falls almost vertically but later it swerves away at an angle of perhaps 60° and lands quite lightly. The stretched skin between limbs and flank provides enough surface to check and deflect the animal appreciably. Thus any small mammal that can control its attitude is the potential ancestor of a glider. Parachuting must be distinctly adaptive to many active arboreal mammals; and the next step, the development of a true patagium, is a simple adaptation that has occurred several times. Thus we have the cobegos (miscalled "flying lemurs"), the "flying" squirrels, and, in particular, numerous "flying" phalangers. Some of the latter, such as the flying opossum, look astonishingly like a flying squirrel, one of the many marked instances of convergence between marsupials and placentals. In some of the smaller phalangers there is no appreciable patagium, but only a flattened body and flattened tail—these seem to be adequate in a very small, and consequently light, animal. Most of these gliding mammals can evidently land on a selected tree trunk far from the point of take-off, indicating ability both to steer and to pull up into a stall just before striking the tree. The flight of birds is interesting both because it is almost universal in a large class and because of its extreme perfection. The perfection is due mainly to the development of feathers, which allow a mechanical and aerodynamic refinement never achieved by other means. Mechanically, feathers have great resilience, graded flexibility, and high strength to weight ratio. Aerodynamically, they provide smooth contours and streamlined sections; permit the development of slotted wings, which produce high lift at low speed; and allow birds to achieve laminar flow. To appreciate these aerodynamic points we must sketchily review the properties of an airfoil, which is a thickened, generally curved plate of streamline section. Fig. 1 shows the section of a low-speed high-lift 163 airfoil such as a bird wing. When such a foil strikes an airstream at a slight positive angle some lift is produced by positive pressure beneath the foil, but much more is caused by negative pressure above it. The airfoil is, in effect, a venturi (or half venturi), like the throat of a carburetor, filter pump, or atomizer. Air passing through a throat must increase in velocity; and, according to Bernoulli's theorem, this increased velocity must be accompanied by decreased pressure.1 If the angle of attack of the airfoil is slightly increased we get added lift but also added drag. Too great an increase in the angle of attack causes the airstream to break away from the wing in violent eddies. This leads to stall, whereby the wing abruptly loses almost all lift. The stall can be delayed by forcing air over the wing at increased velocity in a flat jet (Fig. 2). This is achieved by means of a slot —the venturi once more. Two types of slot are found in birds. The alula forms a midwing slot; and emarginated primaries form wing-tip slots. Fig. 3 shows the plan of the wing of a catbird (Dumelella carolinensis), which is strongly slotted. The slots of large birds such as vultures, buteos, pelicans and crows are open in level flight; but in small birds they are used mainly in take-off and landing. If we have negative pressure above the wing and positive pressure below it, air will inevitably spill up over the wing tips in vortices, causing an unavoidable induced drag. This is essentially a loss at the wing tip. The upper aircraft in Fig. 4 has an aspect ratio (that is, ratio of span to chord) of 5. Let us arbitrarily suppose the shaded portion to be ineffective due to this tip effect. If we double the span and halve the chord as in the lower plane, giving an aspect ratio of 20, we clearly increase the effective proportion of the wing; thus induced drag varies inversely as aspect ratio. 1 Bernoulli's Theorem: At any two points along the same .streamline in a nonviscous, incompressible fluid in steady flow, the sum of the pressure, the kinetic energy per unit volume, and the potential energy per unit volume has the same value. 164 D. B. O. SAVILE Turbulent Laminar Flow Flow A.R. = 20 FIGS. 1 to 5. FIG. 1. Low-speed airfoil at shallow angle of attack, showing pressure distribution. FIG. 2. Aerodynamic slot in operation. FIG. 3. Highly slotted wing of catbird. FIG. 4. Effect of increased aspect ratio in increasing lift; shaded portion of wing is ineffective. FIG. 5. Distinction between turbulent and laminar flow. If the habitat permits it, a high aspect ratio is generally adopted, the ultimate example being the oceanic soaring birds. In land birds of closed habitat extensive slotting is used as a substitute for high aspect ratio; but the aspect ratio is always increased when conditions permit. It is now becoming clear that the feathered wing gives birds a further aerodynamic advantage almost certainly denied to all other flying animals, and one that has only recently been achieved in aircraft. Under most circumstances a series of eddies forms between the wing and the airstream, as in the left diagram in Fig. 5. This is turbulent flow, in which skin friction is so high that it forms a large proportion of the total drag. Under some conditions it is possible to achieve laminar flow, in which a layer of gas molecules is held against the wing and successive layers slide smoothly over them like the cards of a deck being swept across a table (Fig. 5, right). Usually the first requirement for laminar flow is a very smooth surface—at least as smooth as writing paper. Their relatively rough wing surfaces seemed to preclude all possibility of birds achieving it. However, laminar flow may also be achieved through the process of boundary layer control. This mathematically complex process can be achieved by drawing in air through the upper surface and releasing it from the lower surface. Raspet (I960) has presented evidence, from power availability studies, that this must actually occur in bird wings, a contention supported by the observation that the flight feathers are about seven times as porous to downward-moving as to upward-moving air. These findings may explain the pronounced sweepback that has occurred repeatedly in the wings of fast birds. If laminar flow occurs over the wings and turbulent flow over the body, a reduction in drag presumably results from shortening the GLIDING AND FLIGHT body and tail and sweeping back the wings to stabilize against pitching. I have elsewhere (1957) discussed wing actions and adaptations; most other aspects of flight are qualitatively explained in terms of aircraft aerodynamics. The little remaining space will therefore be given over to discussing some unanswered quantitative problems that must engage the attention of those who believe that taxonomy should reflect the whole biology of the organisms studied. Hamilton (1961) has recently discussed some of these problems, and I know, from correspondence, that various workers in Europe and North America are concerned about them. Here is the sort of problem that we may run into. Bergmann's rule tells us that subspecies at high latitudes are larger than those at low latitudes. This is commonly interpreted as an adaptation for reducing heat loss, the ratio of surface to volume falling with increased body size. How do we measure body size? Often we rely on the length of the bent wing, which may represent merely primary length and not size and weight of body. Hamilton has suggested that humerus length be used as an index of body size. Even when the body really is larger the wing may be disproportionately longer, keeping wing loading nearly constant. Races breeding at high latitudes often make long migrations, which may make a longer wing adaptive. How great an increase in wing area or length will be adaptive in facilitating take-offs or long migrations for races with a given increase in body size? If we managed to measure power consumption in take-off or level flight accurately we might be able to come close to answering such questions. Another vexing set of questions concerns adaptation to changes in altitude. Mountain races are subjected to low temperature, which tends to encourage an increase in body size. They also operate at reduced atmospheric pressure, which may make an increase of wing area adaptive (to keep lift nearly constant) even if body size does not 165 increase. Can we be sure that reduced air pressure does not sometimes impose respiratory limitations that would make a larger wing inadaptive? There may also be changes in habitat density, which will affect the permissible wing changes. If the birds inhabit subalpine parkland the wings are likely to become relatively long; if they inhabit dense krummholtz the wings will probably be short and added lift must then come from increase in the wing chord or from increased slotting; but only a change in length will be revealed by the orthodox bent wing measurement. If we accept the standard atmosphere of the International Commission on Air Navigation as representing pressure change with altitude, we can say that at 5,000 ft the wing area must increase by 16% over that at sea level, and at 10,000 ft by 35%, to maintain equal lift. If wing shape is unchanged the spans will increase by 7.8 and 16.3%. As most of this increase is likely to be in the length of the primaries, the bent wing measurement could show a substantial altitude effect of this sort; but we must obviously be cautious about assuming that a change is actually an air pressure effect. Even if none of the other factors alter wing size, the altitude effect might produce a slightly smaller increase in area than expected. The larger wing may be slightly more efficient because it has less edge in proportion to area than the smaller one, and hence less turbulence at the edges. Moreover, changes in wing size will be mainly advantageous at takeoff; for drag, as well as lift, is reduced at altitude. Thus there might be little or no increase in wing area of sedentary ground feeders, but a substantial increase in very active insectivorous birds like the wood warblers that make thousands of take-offs each day. Obviously we dare not draw sweeping conclusions without considering the whole natural history of the species. REFERENCES Cott, H. B. 1926. Observations on the life-habits of some batrachians and reptiles from the lower 166 D. B. 0. SAVILE Amazon: and a note on some mammals from Marajo Island. Proc. Zool. Soc. London, 2:11591178. Gray, J. 1953. How Animals Move. Cambridge Univ. Press. Hamilton, T. H. 1961. The adaptive significance o£ intraspecific trends of variation in wing length and body size among bird species. Evolution 15: 180-195. Heilmann, G. 1926. The origin of birds. H. F. and G. Witherby, London. Oliver, J. A. 1951. "Gliding" in amphibians and reptiles, with a remark on arboreal adaptation in the lizard Anolis carolinensis carolinensis Voigt. Am. Nat. 35:171-176. Raspet, A. 1960. Biophysics of bird flight. Science 132:191-200. Savile, D. B. O. 1957. Adaptive evolution in the avian wing. Evolution 11:212-224. Smith, J. M. 1952. The importance of the nervous system in the evolution of animal flight. Evolution 6:127-129.