Respiratory Exchange and Evaporative Water Loss in the Flying Budgerigar

Flight is the typical form of avian locomotion. Because it enables birds to move faster and farther under their own power than any other animal, its energy requirements are interesting. These energy requirements presumably are met by oxidative metabolism so that they can be determined from the oxygen consumption, carbon dioxide production and nitrogen excretion of the flying bird.

The energetics of avian flight are not well understood because the concomitant rapid movement of the bird through the air makes measurements difficult to obtain. Oxygen consumption in flight has been measured only for hovering humming-birds (Pearson, 1950; Lasiewski, 1963) and budgerigars flying in turbulent air (Tucker, 1966). Oxygen consumption alone permits a fairly accurate estimate of the energy requirements of flight. Various other methods have been used to estimate the energy requirements of flight (see Dol’nik & Blyumental, 1964; Nisbet, 1963, for review; also Hart & Roy, 1966 a; LeFebvre, 1964; Pearson, 1964). These estimates depend on more tenuous assumptions than estimates based on oxygen consumption, and less confidence can be placed in them.

In this study the energy requirements of ascending, level and descending flight at various speeds are estimated from the oxygen consumption and carbon dioxide production of budgerigars (Melopsittacus undulatus) flying freely in a wind-tunnel. Determinations of respiratory rate and evaporative water loss in flight are included.

Budgerigars are the commonest small parrot of the arid regions of Australia. They are migratory birds and can fly swiftly and steadily for hours (Cayley, 1933)

Budgerigars were trained to fly in a wind-tunnel (Aerolab Supply Co., Hyattsville, Md.) (Text-fig. 1) with a cylindrical, Perspex working section 30 cm. in diameter and 30 cm. long. An electrified grid (wires 1·7 mm. diameter, spaced at 1 cm. intervals) was placed on the floor and at the ends of the working section. Except for a boundary layer about 2 cm. deep, air flow in the working section had a constant velocity. Air speed was adjustable and was measured with a pitot tube or a Short and Mason anemometer 6·5 cm. in diameter. The tunnel was suspended so that its long axis could be tipped from horizontal. Thus, the relation between air velocity and the direction of gravitational force could be changed in the same manner that it changes for a free flying bird during ascending, level and descending flight.

Two budgerigars were used in these studies. They were purchased from a local pet store and were kept in the laboratory in cages measuring 22 × 26 × 40 cm. The weights of the birds varied between 30 and 40 g. throughout the experiments.

During initial training in the wind-tunnel, saturated calcium chloride solution was applied to a bird’s feet to ensure electrical contact with the grid, and the bird was placed in the tunnel with both air flow and the electrified grid off. I then made a rapid movement of my hand outside the tunnel and immediately afterwards gave the bird a momentary shock. Within an hour, the bird learned to flutter off the grid whenever I moved by hand. The wind-tunnel then was turned on, and within a few hours the bird learned to match its flight speed to the tunnel and to stay centred for a few seconds in the tunnel. After a bird had learned to fly for several seconds, it was taught to alight on a perch that could be inserted into the working section. From then on, the bird was never again permitted to land on the grid without receiving a shock. To initiate a flight, a bird was placed on the perch, the wind-tunnel was turned on and the perch was withdrawn. The flight ended when the bird alighted as the perch was replaced.

To measure oxygen consumption and carbon-dioxide production the birds were trained to wear a transparent mask while flying (Plate 1). The mask was made from a cellulose acetate centrifuge tube 25 mm. in diameter. A rubber band compressed four tabs at the rear of the mask around the back of the bird’s head. A flexible vinyl tube (1·07 mm. inside diameter, 0·51 mm. wall) entered the front of the mask and opened behind a baffle. Suction was applied to the tube so that air from the room flowed into the back of the mask, collected the expired respiratory gases and swept them into the tube. The baffle prevented the feathers on the bird’s head from being sucked into the tube. The weight of the tube, mask and rubber band was 1·48 g.

A vacuum system sucked air through the mask at 3·30 l./min. An additional 2·62 l./min. of air entered the vacuum system downstream of the mask. The total air flow was monitored continually with a rotameter and was kept within 2 % of the specified value. The pressures at the inlet and outlet of the rotameter were kept constant, and the rotameter was calibrated for these pressure conditions.

For measurements of oxygen consumption a diaphragm pump moved a sample of air from the vacuum system through a desiccant (Drierite) to a recording Beckman paramagnetic oxygen analyser that gave a full-scale response for a change of 0·005 in fractional concentration of oxygen. The analyser was calibrated to an accuracy of ± 1 % and was equipped with a system regulating absolute pressure, so that the instrument was unresponsive to changes in barometric pressure. The fractional content of oxygen in air entering the mask (⁠⁠) was measured before the mask was placed on the bird and after it was removed. Changes in during an experiment were insignificant. The fractional content of oxygen in air passing through the rotameter (⁠⁠) was recorded as the bird flew with the mask on. These measurements were made at flight speeds between 19 and 48 km./hr. in level flight and at angles of ascent and descent between 5° and 15°. The birds flew at least 5 min. before was measured.

Carbon dioxide production was measured by weighing a carbon dioxide absorbent (Ascarite) before and after it was placed for a measured time in the air flow coming from the flying bird’s mask. The air passed through Drierite before passing through Ascarite. Immediately before or after this procedure a blank value was obtained by passing room air through the empty mask and the Drierite and Ascarite for the same period of time. To obtain the bird’s carbon dioxide production this blank value was subtracted from the total carbon dioxide absorbed while the bird was flying. The blank was always less than 10% of the latter value. Carbon dioxide (100 ml.) injected into the mask at rates both greater and less than the bird’s rate of carbon dioxide production was recovered by the Ascarite within 1 %.

was calculated from equation (2) for five experiments on one bird (P₁) in level flight at 35 km./hr. The bird flew at least 5 min. while was recorded. Then the Ascarite was connected to the circuit without interrupting air flow or flight. Carbon dioxide was absorbed for the next 15 min., the Ascarite was disconnected, and again was recorded for 5 min. This procedure was carried out on only one bird because the other bird would not fly for 25 min. continuously with the mask on.

The mean value of K (−0·220, S.D. = 0·0316) was calculated, and this value and equation (3) were used in all other experiments where oxygen consumption was determined.

To show that there was no leakage of expired air around the back of the mask, the oxygen consumption of a flying bird was measured while air flow through the mask was decreased. The indicated oxygen consumption of the bird did not change as the flow was decreased from 3·30 to 1·9 l./min. Then the flow was decreased in one step to 0·5 l./min., and leakage was clearly evidenced by the low and erratic values for oxygen consumption.

Evaporative water loss during level flight at 35 km./hr. was calculated from the equation

This equation follows from the law of conservation of matter. Birds without masks were trained to sit inside the tunnel on a perch suspended from a thread attached to a torsion balance above the tunnel. They were weighed to the nearest 0·01 g., and immediately thereafter the airflow was started, the perch was drawn up and flight commenced. After a 20 min. flight (or shorter at high temperatures) the airflow was stopped and the perch was lowered. The birds were weighed within 2 min. after cessation of flight. Droppings voided during flight were collected on a gauze screen at the rear of the working section. No more than two droppings were voided during a 20 min. flight. The weight of each dropping was estimated from the mean weight of ten droppings collected under perched birds (mean = 27 mg., S.D. = 10·5). Oxygen consumption and carbon dioxide production were estimated to be the same as for masked birds in level flight at 35 km./hr.

During measurements of change in body weight the wind-tunnel was kept in a room with controlled humidity and temperature. The vapour pressure of water in the room was between 6 and 7 mm. Hg at all temperatures. Temperature was controlled at 18–20°, 29–31° and 36–37° C.

Respiratory rate in flight was measured by placing inside the mask a thermocouple junction made from copper and constantan wire 0.05 mm. in diameter. Each exhalation warmed the junction and was recorded distinctly on an oscillograph. The mask had large perforations in the anterior end so that carbon dioxide was swept away as it was exhaled.

All experiments reported here were carried out at a temperature of 23° C. and a humidity of approximately 50 % unless otherwise specified. All gas volumes pertain to dry gas at 760 mm. Hg and 0° C. unless otherwise specified.

Both birds flew in the wind-tunnel in what appeared to be a normal fashion. They required about 6 weeks of daily training before they would fly continuously for 20 min. or more. The birds were not tested for endurance, but on one occasion a bird was allowed to fly for 2 periods of 30 min. separated by a 3 min. stop. On some days each bird was flown for a total time of 2 hr. over a 6 hr. period. If the birds were not flown for a month or more they remembered how to fly in the tunnel, but required several weeks of training before they again would fly for 20 min.

The birds appeared to fly in the same manner whether masked or not. They did not pull against the tube attached to the mask. One bird (P₁) would fly for the same duration with or without the mask, but the other learned to remove the mask with its feet while in flight. It would fly for about 10 min. before indulging in this exasperating habit, or for a shorter time if the combination of flight speed and angle required a relatively large energy expenditure.

Oxygen consumption was measured after 5 min. or more of flight at speeds between 19 and 48 km./hr., and at angles of ascent and descent between 5 and 15° (Table 1). During the first few minutes of a flight the oxygen-analyser recording changed slowly, but after 5 min. it remained constant for at least the next 20 min. of flight.

At the highest and lowest speeds one of the birds would fly for 5 min. but no longer. The other would not fly for 5 min. Only one bird would fly for 5 min. at an angle of ascent of 5°, and only at speeds below 48 km./hr.

Oxygen consumption was markedly dependent on both flight speed and flight angle, and for each bird at a particular set of conditions it was almost constant from one flight to the next (Table 1, Text-fig. 2). In both level flight and descending flight at 5° oxygen consumption was lower at 35 km./hr. than at higher or lower speeds. At any given speed oxygen consumption was highest during ascending flight and lowest during descending flight.

In five experiments carbon dioxide production and oxygen consumption were measured on one bird (P₁) for the last 15 min. of level flights at least 20 min. long at 35 km./hr. The mean carbon dioxide production was 4·07 ml./g. in 15 min. (S.D. = 0·102) or 0·271 ml. (g. min.)⁻¹. The ratio (RQ) had a mean value of 0·780 (S.D. = 0·0316).

In five other experiments the carbon dioxide production of the same bird was measured from the beginning to the end of a 20 min. flight. The mean amount of carbon dioxide produced was 5·06 ml./g. in 20 min. (S.D. = 0·338). Thus, 0·990 ml./g. or 0·198 ml. (g. min.)⁻¹ were produced during the first 5 min. of flight. The latter figure is lower than the rate of carbon dioxide production during the last 15 min. of flight, and this difference may represent a carbon dioxide deficit associated with the oxygen debt that occurs at the onset of flight (Tucker, 1966). It was impossible to measure oxygen debt in the present experiments because of the time lag inherent in the open-circuit oxygen analysis system.

Respiratory rate was measured during level flights lasting three minutes at speeds between 19 and 48 km./hr. Like oxygen consumption, respiratory rate was lowest at 35 km./hr. and increased at higher or lower speeds (Text-fig. 3). However, for each bird at a particular speed respiratory rate was quite variable from one flight to the next. Respiratory rate did not change significantly after the first 30 sec. of flight.

Evaporative water loss was lowest at 18–20° C and 3-4 times higher at 36–37° C (Table 2). At the latter temperature the birds exhibited several types of behaviour which indicated that they were overheated. After a few minutes of flight their feet, which normally were tucked up close to the body, were lowered so that the naked toes and tarsometatarsus were exposed to the air stream. The birds would not fly for 20 min. at the highest temperatures. One bird (P₁) flew for a mean time of 5·3 min. (S.D. = 0·76); the other flew for 13 min. (S.D. = 1·08). At the end of the flights at the highest temperatures, the birds sat on the perch with their feathers compressed and wings raised so that the sides of the body were exposed. They breathed deeply with open beaks. These sorts of behaviour were not observed after flights lasting 20 min. at lower temperatures.

The energy requirements of a flying bird can be deduced from oxygen consumption, carbon dioxide production and nitrogen excretion (for example, see Kleiber, 1961). Nitrogen excretion was not measured in these studies, so that only the total RQ, not the non-protein RQ, can be calculated. However, a caloric equivalent of oxygen can be estimated from total RQ with negligible error (King & Farner, 1961). It amounts to 4·8 cal./ml. O₂ for the total RQ of 0·780 measured in this study (Lusk, 1931).

The value of the total RQ also permits a reasonable estimate of the proportions of fat and carbohydrate that provide the energy for flight in budgerigars. Protein metabolism in men and dogs does not increase markedly with exercise (Lusk, 1931). If the same is true for budgerigars, approximately 75% of the increase in oxygen consumption associated with flight is used for oxidation of fat, and 72 % of the energy for flight is derived from fat metabolism. The conclusion that fat is the primary fuel of flying budgerigars is consistent with measurements made on other birds (Dol’nik & Blyumental, 1964; George & Berger, 1966) and with Weis-Fogh’s contention (1952) that fat is the only fuel suitable for long-distance flights because of its high caloric content per unit weight.

With the caloric equivalent of oxygen established it is clear from Fig. 2 that the energetic cost of flight is predictable for budgerigars in flight in the wind-tunnel, if both flight speed and angle are known. Further, a budgerigar could choose a combination of flight speed and angle so that it could attain a particular goal with a minimum expenditure of energy. It is interesting to consider various goals and the tactics by which they could be achieved with minimum energy expenditure.

A budgerigar might fly so as to maintain its altitude for the longest possible time. This strategy would be served by level flight at 35 km./hr. A budgerigar flying at this speed uses 21·9 ml. O₂ (g. hr.)⁻¹ or 105 cal. (g. hr.)⁻¹. These figures are 12·8 times the standard metabolic rate of a bird of this size (Lasiewski & Dawson, 1967) and correspond to 1·1 % of body weight consumed as fuel (fat) each hour.

As a flying bird consumes fat and becomes lighter the energetic cost of flight probably decreases. Since some migratory birds may accumulate fat until it makes up half their total weight (Odum, Connell & Stoddard, 1961), the present measurements suggest that such birds should have sufficient fuel for more than 50 hr. of flight. Some migrating birds do appear to fly for this long or longer without feeding (Moreau, 1961 ; Nisbet, Drury & Baird, 1963).

Budgerigars are economical fliers compared to other flying devices. An insect, the migratory desert locust Schistocerca, uses 0.8 % of its body weight as fuel each hour, but other insects that have been investigated use between 7 and 35%. Man-made aircraft ranging from conventional monoplanes to helicopters and jet fighters use between 2 and 36% (Weis-Fogh, 1952).

Estimates of energy expenditure of other birds in flight under various conditions range from 19 to over 2000 cal. (g. hr.)⁻¹ (Nisbet, 1963; Dol’nik & Blyumental, 1964; LeFebvre, 1964; Pearson, 1964; Hart & Roy, 1966a). The most reliable estimates are based on oxygen consumption. Hovering humming-birds use 42 ml. O₂ (gm. hr.)⁻¹ (Lasiewski, 1963), a figure that is a reasonable extrapolation to zero speed of the curve for oxygen consumption of flying budgerigars. Budgerigars flying in turbulent air for 2 min. at speeds between 19 and 33 km./hr. use 35–55 ml. O₂ (g. hr.)⁻¹ (Tucker, 1966), or about twice as much as the birds in this study flying for longer times at 35 km./hr. in smooth air. Other estimates are hard to compare meaningfully with measurements on budgerigars because they are based on either tenuous assumptions or on measurements made under conditions where the birds could land or were flying at unknown velocities. Nisbet (1963) and Dol’nik & Blyumental (1964) after reviewing the literature for birds weighing less than 40 g. estimate flight metabolism during migration at 76 and 140 cal. (g. hr.)⁻¹, respectively. LeFebvre (1964), using a doubly labelled water technique as well as measures of fat loss, estimates that pigeons weighing 384 g. metabolize 57 cal. (g. hr.)⁻¹ during 500 km. cross-country flights. This figure is 13·4 times the standard metabolic rate calculated from Lasiewski and Dawson (1967).

Budgerigars in level flight, even at their most economical speed, use oxygen faster than the maximum rates known for mammals of similar size. Various rodents weighing less than 30 g. and either running in exercise wheels or awakening from torpor use between 12 and 16 ml. O₂ (g. hr.)⁻¹ (Tucker, 1965). Budgerigars use oxygen at 2 or 3 times these rates when they ascend, fly rapidly or slowly, or fly in turbulent air.

A bird might fly so as to cover the longest possible distance for a given energy expenditure. This strategy would be served by level flight at the speed where the ratio of metabolism to flight speed (the cost of transport in cal. (g. km.)⁻¹) is minimum, or 2·9 cal. (g. km.)⁻¹ at 42 km./hr. for budgerigars in the wind-tunnel (Text-fig. 4).

Budgerigars by this measure are more economical fliers than the insects that have been investigated (5-30 cal. (g. km.)⁻¹) and are about the same as man-made aircraft (1-5 cal. (g. km.)⁻¹) (Weis-Fogh, 1952). They are less economical than LeFebvre’s pigeons (0.95 cal. (g. km.)⁻¹), man walking at 4·8 km./hr. (0·78 cal. (g. km.)⁻¹) or horses walking at 4·8 km./hr. (0.57 cal. (g. km.)⁻¹) (Brody, 1945).

The appropriate tactics for gaining or losing altitude with minimum energy expenditure can be identified by considering the efficiencies of ascending and descending flight at an angle of 5° and at various speeds. Efficiency is defined as either total (E_t) or partial (E_p). E_t is the percentage ratio of external work done to total energy expenditure. E_p is the percentage ratio of change in external work done to change in energy expenditure. A discussion of these efficiencies can be found in Kleiber (1961). Both E_t and E_p are determined easily for ascent, since the net work done in ascending is the product of weight and change in altitude. During descent no work is done, and the work done during ascent is dissipated as heat. However, it is useful to reckon the absolute value of the product of weight and change in altitude as the work done in descending, so that values of E_t and E_p can be calculated.

Values of E_t for ascent and descent at 5° and at various flight speeds are interesting because their maxima indicate the speed where a given amount of altitude can be gained or lost with the minimum energy expenditure. In the one budgerigar for which measurements are available, maximum E_t values for both ascent and descent occurred at 42 km./hr. (Text-fig. 4). It should be noted that this speed is higher than the speeds where the rate of energy expenditure is minimum during ascent (24 km./hr.) and descent (35 km./hr.) at 5° (Text-fig. 2). E_t for ascent has a maximum value of only about 5%, but this figure should not be confused with E_t values of about 25% for the total work of mammals (Kleiber, 1961; gross efficiency, Brody, 1945). The bird is doing an unknown amount of additional work while ascending by overcoming the aerodynamic drag force.

Values of E_p (relative to level flight) for birds ascending and descending at 5° at various flight speeds permit several interesting comparisons. For ascent, E_p is more than 50% at the slowest speed of 19 km./hr., drops as speed increases and finally rises to a value of 18 % at 42 km./hr. (Text-fig. 4). Since these figures do not include the work for overcoming drag, they are not directly comparable with E_p values of about 35 % for the total work of mammals (Kleiber, 1961 ; absolute efficiency, Brody, 1945). However, even when drag work is omitted budgerigars flying at speeds below 25 km./hr. have higher E_p values than those for men and dogs climbing on a treadmill (about 35%, calculated from Dill, 1965).

E_p for ascent is the same as that for descent at two speeds−27 and 43 km./hr. This means that at either of these speeds a budgerigar flying at an angle of 5° could ascend to and descend from a given altitude and use no more energy than if it spent the same time in level flight at these speeds. If the bird flies at speeds less than 27 km./hr., E_p for ascent is greater than for descent, and the bird could save energy by alternately ascending and descending.

The above observations on E_t and E_p indicate that energy is conserved when ascending or descending flight at 5° is carried out at appropriate speeds. If the bird employs the strategy of gaining altitude most economically it would fly at 42 km./hr. It is interesting that at this speed it can fly to a given altitude and descend at almost no cost over flying level at the same speed for the same time. This characteristic of avian flight suggests that birds that fly at altitudes of 6100 m. or more (Tucker, 1968) need spend little extra energy ascending to and descending from that level. If a budgerigar flies at speeds less than 27 km./hr. it requires little extra energy to ascend, since E_p for ascent is high. It is interesting that the budgerigar, which is a ground-feeding bird, does much of its ascending flight immediately after take-off, when it has not yet accelerated to normal flight speed. Also, at these slow speeds E_p for ascent is greater than for descent, so that ascending and descending flight is more economical than level flight. These observations may explain why those types of birds with undulating flight (e.g. some finches and woodpeckers) are not noted for their speed.

A maximum value for E_p that includes a change in total external work rate during flight can be calculated and is comparable to E_p values for the total work rate of mammals. A flying bird must work to move through the air, and the total work rate includes the product of the aerodynamic force necessary to move the bird through the air and the flight speed. With budgerigars it is possible to observe the effect on oxygen consumption of a change in aerodynamic force. This change in force can be used to calculate the maximum change in total work rate. Details are given below.

The aerodynamic forces on a flying machine are conventionally resolved into those acting parallel to the relative wind (thrust and drag) and those acting perpendicular to the relative wind and in the vertical plane (lift and a weight component). The magnitude of the relative wind is the speed of the air with respect to the body of the flying machine, and the direction of the relative wind is opposite to the flight direction. Under equilibrium conditions, which apply in this study, lift equals the weight of the flying machine times the cosine of the angle (ϕ) between the relative wind and horizontal. Drag is the sum of a component due to air resistance and a component given by the product of weight and sin ϕ. These relations are reviewed by Jones (1950).

According to these conventional definitions a bird ascending and descending at a constant speed and angle (ϕ) has the same magnitude of lift during ascent and descent. However, drag increases by the product of weight and sin ϕ during ascent and decreases by an equal amount during descent. In addition, there probably is a decrease in the air-resistance component of drag during ascent because the body angle to the relative wind decreases with ascent (Tucker, unpublished). Thus, the total change in drag from descent to ascent is twice the product of weight (W) and sin ϕ, less a component due to a decrease in body angle. Since there is no change in lift, the total change in work rate from descent to ascent is less than 2W sin ϕ multiplied by the speed of the relative wind. Maximum values of E_p, calculated from this change in work rate and the change in energy expenditure, are between 18% and 29 % at speeds between 28 and 48 km./hr. (Text-fig. 4).

Since these values of E_p express the efficiency of a budgerigar working to produce a force acting parallel to the flight direction, they are comparable to the absolute efficiency of a horse pulling a load. Brody (1945) defines absolute efficiency as the ratio of work accomplished to the energy expended above that of walking without the load. The absolute efficiency of horses pulling a load is 34% (Kleiber, 1961). The figures for budgerigars approach this value at high and low flight speeds but are less at intermediate speeds.

In summary, this section has discussed the speeds and angles of flight through which a budgerigar can attain a particular goal most economically. The tactic of flying at 42 km./hr. in level flight or descending or ascending flight at 5° would allow the bird to fly for distance most economically and would allow it to ascend and then descend with little extra cost over level flight for the same time. The duration of flight can be maximized by flying at 35 km./hr. If flying at speeds below 27 km./hr. the bird can ascend with little extra cost over level flight, and undulating flight is more economical than level flight. These observations suggest that when cruising in their natural habitat budgerigars fly at about 42 km./hr.

The behaviour of cruising pigeons is consistent with the finding that there is a single most economical speed for budgerigars flying in the wind-tunnel. Pigeons are known to cruise at a relatively constant air speed regardless of wind conditions (Michener & Walcott, 1967). Whether the air speeds of other species also are relatively constant is at present unknown.

Since the water evaporated by a flying budgerigar comes primarily from the respiratory system, evaporative water loss can be used to estimate the volume of air that ventilates the lungs in a given time. The exhaled air can be no warmer than body temperature, and this temperature determines the maximum amount of water vapour the exhaled air can carry. The water evaporated by the bird in a given time must be distributed in a volume of air that is at least large enough to accommodate this water plus the water content of the inhaled air without exceeding the maximum vapour pressure set by body temperature. This volume of air is a minimum value for lung ventilation, for the actual ventilation would be larger if the expired air were not as warm as body temperature or were not saturated with water. After minimum ventilation is estimated for budgerigars flying at 35 km./hr., the minimum tidal volume and the maximum partial pressure of carbon dioxide in expired air can be calculated (Table 3). In the following discussion these maximum and minimum values for respiratory parameters are assumed to be actual values, since they are the best estimates available.

Several interesting comparisons can be made among and between the estimates in Table 3 and the data for other animals. First, at 20° C. oxygen consumption and ventilation increase proportionally in flight. Oxygen consumption increases by a factor of 4·9, ventilation by a factor of 4·7. This indicates that the budgerigars consumed as oxygen the same proportion of the lung ventilation (6·2 to 6·6 %) whether resting or flying. Ventilation and oxygen consumption also increase proportionally in man during exercise (Dejours, 1964). The partial pressure of carbon dioxide in the expired air of man at rest (32 mm., calculated from Ruch & Patton, 1965) does not differ significantly from that estimated for budgerigars at 20° C., whether resting or flying. Thus, man removes about the same proportion of oxygen from the air ventilating his lungs as do resting or flying budgerigars.

Budgerigars in flight at 20° and 30° C. lose by evaporation about as much water per ml. of oxygen consumed as resting budgerigars and some resting rodents but less water than most resting small birds. Birds weighing 35 g. on the average lose 2·2 mg. water per ml. oxygen consumed at about 25° C. (calculated from Bartholomew & Cade, 1963; Lasiewski & Dawson, 1967). Rodents at 20–30° C. lose between 0·5 and 1·4 mg. water per ml. oxygen consumed (Hudson, 1962).

Pigeons, for which there is reliable information on respiration in flight, are the only birds that can be compared with budgerigars. LeFebvre (1964), using a D₂O¹⁸ method, has estimated evaporative water loss and metabolism of pigeons flying over a distance of 500 km. Hart & Roy (1966b) have telemetered respiratory rate and tidal volume of masked pigeons carrying radio transmitters weighing 8 % of body weight for short flights of 3–14 sec. Values calculated from these two papers are shown in Table 3. The differences between values from these papers are not surprising, considering the differences in techniques and that Hart & Roy’s values are transients that probably are associated with oxygen debt. Budgerigars continue to accumulate an oxygen debt until they have flown more than 44 sec. (Tucker, 1966).

The lung ventilation of pigeons in flight is 13–21 times the resting value at 25° C. The ventilation of pigeons may increase proportionally with oxygen consumption during flight, but the data are not conclusive. Oxygen consumption of pigeons in flight (calculated from LeFebvre) is 13 times the standard value for a bird this size (Lasiewski & Dawson, 1967), and this factor is within the range of those for ventilation. LeFebvre’s pigeons in flight consumed 4·8% of the lung ventilation as oxygen. Resting and flying budgerigars and pigeons had about the same evaporative water loss per ml. oxygen consumed.

It is interesting to consider the water budget of budgerigars during long flights when their rate of evaporative water loss is relatively high and they cannot drink. Budgerigars in nature are migratory (Cayley, 1933), and when flying long distances they (and other species of birds) may face problems of dehydration (Yapp, 1956; 1962). The sole source of water for a flying bird is metabolic water from the oxidation of foodstuffs. For a budgerigar in level flight in a wind-tunnel at 35 km./hr. this amounts to 13 mg. (g. hr.)⁻¹ (assuming 75 % fat and 25 % carbohydrate metabolism). Water is lost by evaporation (20 mg. (g. hr.)⁻¹) and through the faeces (4 mg. (g. hr.)⁻¹, calculated from Cade & Dybas, 1962, assuming faeces are voided 5 times faster during flight than at rest at 20° C.). Thus, the flying budgerigar would have a net water loss of 11 mg. (g. hr.)⁻¹ or 1·1 % body weight per hour. If the bird could tolerate a maximum water loss of 15 % body weight, it could fly about 14 hr. or 490 km. This is an adequate range for most migratory birds, but some species are estimated to fly for 50 hr. or more without drinking (Moreau, 1961 ; Nisbet, Drury & Baird, 1963). It is difficult to see how these birds fly for so long unless they lose water more slowly in flight than budgerigars. Some birds may become dehydrated during migration, but there is good evidence that other birds do not (see Nisbet et al. 1963, for review).

The relation between respiratory rate and wing-beat frequency of birds has drawn speculative statements from many investigators, but few definitive measurements have been made. King (1966) reviews the subject. The following questions may be asked. Are the wing motions and breathing synchronized? If so, is the correspondence 1 to 1? Does expiration correspond to an upstroke or a downstroke of the wings? Except for the budgerigar and the pigeon these questions cannot be answered with certainty for any species. Much of the work reviewed by King is based on questionable methodology, and all of it describes flights of only a few seconds. A recent paper by Hart & Roy (1966b) describes a reliable method of telemetering respiratory parameters of pigeons, but the longest flight lasted only 14 sec. The available evidence suggests that breathing and wing beat are synchronized in the pigeon, crow (Corvus) and duck (Anas). In the pigeon, expiration accompanies downstroke (Hart & Roy, 1966b). In the duck, there may be two wing beats for each breath (Lord, Bellrose & Cochrane, 1962). Fraenkel (1934) concluded that the chaffinch (Fringilla), which weighs 20 g. and is smaller than the above-mentioned birds, had no fixed relation between breathing and wing beats. However, his measurements were made during only a few seconds while the bird fluttered suspended from its beak.

The measurements on the budgerigars show that in this species there is no fixed relation between breathing and wing beats. The wing beat frequency, as measured stroboscopically, was constant at all flight speeds at 840 beats/min. (Tucker, unpublished), yet the respiratory rate changed continuously from one flight speed to another (Text-fig. 3).

Analysis of the relation between body weight, wing-beat frequency and oxygen consumption indicates that a 1 to 1 synchrony of breaths and wing beats probably does not occur in other birds the size of a budgerigar or smaller. Greenewalt (1962) has compiled various dimensional relations for flying animals. His data indicate that the wing-beat frequency of birds is proportional to W^−0·38, where W is body weight. The oxygen consumption of resting birds is proportional to their metabolic rate, and the metabolic rate of a flying bird at the bird’s choice of flight speed can be assumed to be a constant multiple of the standard metabolic rate. Thus, the oxygen consumption of a flying bird should be proportional to W^0·72 (Lasiewski & Dawson, 1967). Oxygen consumption can be assumed to be a constant fraction of lung ventilation, so that ventilation also is proportional to W^0·72. Therefore, the ratio of lung ventilation to wing-beat frequency is proportional to W^1·1. Since lung ventilation is the product of respiratory rate and tidal volume, this ratio equals tidal volume if there is a 1 to 1 synchrony between breaths and wing beats.

A lower limit should be expected for the weight of a bird which can ventilate its lungs efficiently at wing-beat frequency. If respiratory rate equals wing-beat frequency, the ratio of respiratory rate to tidal volume would be proportional to W^−1·48. This ratio influences the efficiency of lung ventilation. The lungs are not efficiently ventilated by a relatively high respiratory rate and a low tidal volume, for under these conditions much of the inspired and expired air contacts only the nasal passages, trachea and other non-respiratory structures that comprise the respiratory dead space.

Budgerigars and chaffinches appear to be below, and pigeons above, the weight limit for synchrony. If budgerigars had breaths synchronized to wing beats and a lung ventilation of 398 ml. (g. hr.)⁻¹ at 20° C. (Table 3) their tidal volume would be only 0·008 ml. (g. breath)⁻¹, or 24% of the value estimated in Table 3. For a 35 g. bird this amounts to a tidal volume of 0·28 ml. The trachea alone of a dead budgerigar contained 0·15 ml., so for synchronous breaths and wing beats the ratio of dead space to tidal volume would be more than 54%. Ventilation of the lungs with such a large ratio is relatively inefficient. In man, the ratio of dead space to tidal volume is less than 28% (see Bouhuys, 1964, for review).

These observations on respiratory rate suggest a mode of operation for the peculiar lungs and air sacs of birds (see King, 1966, for review). It is hard to believe that the contractions of the flight muscles have no influence on ventilation in small birds. These massive muscles insert directly on the sternum, a structure that is involved in ventilation of birds at rest. It may be that the externally measured respiratory rate of flying budgerigars reflects only the relatively slow anterior and posterior movement of air passing through the primary and secondary bronchi of the lungs on the way between the outside and the air sacs. A faster additional rhythm imposed by the flight muscles might cause increased ventilation of tertiary bronchi, air capillaries and some of the air sacs.

A heat budget can be constructed for budgerigars flying at 35 km./hr. in the wind-tunnel at different temperatures. The heat produced by metabolism can be calculated assuming 25% efficiency of conversion of metabolic rate to external work rate (Kleiber, 1961). The remaining energy must be either stored as heat or lost as heat by evaporation, conduction, convection or radiation. Rate of loss by the latter three modes in homeotherms below the thermal neutral zone is often proportional to the difference in temperature between the animal’s body and the air (Newton’s law of cooling; see for example Tucker, 1965). The constant of proportionality, or more generally the ratio of the animal’s heat loss to the temperature difference when body temperature is constant, is called ‘thermal conductance’.

The relative importance of heat storage and of various modes of heat loss in accommodating the metabolic heat production in flying budgerigars is shown in Table 4. At 20° C., 15% of the heat production is lost by evaporation. LeFebvre’s (1964) pigeons lost 13 % of their heat by evaporation of water in flight (25 % efficiency). Hart & Roy’s estimate (1966b) of 17 % for their flying pigeons is incorrect, since they assume an efficiency of o. Using an efficiency of 25 %, their estimate for evaporative heat loss would be 22 % of metabolic heat production in flight. However, this figure has little significance, because Hart & Roy’s birds were probably accumulating an oxygen debt and were probably storing some of their heat production. Under these conditions it is impossible to make a reasonable estimate of heat loss for the birds.

These data indicate that at temperatures near 20° C. flying birds lose about 15 % of their heat production through evaporative water loss. The contention that the heat production of flying birds is dissipated primarily by evaporation (Salt & Zeuthen, 1960; Eliassen, 1963) is not supported. However, at 36–37° C. the evaporative water loss of budgerigars increases by a factor of 3·1 until it accounts for almost 50% of the estimated heat production in flight.

Problems of overheating probably prevent budgerigars from making long flights during many midday hours in their natural environment. Budgerigars in the wind-tunnel at 37° C. became overheated and would not fly for as long as 20 min. Shade temperatures over much of Australia exceed 37° C. daily in the summer, and a flying bird would receive an additional heat load from solar radiation.

The thermal conductance (Table 4) of flying budgerigars is much higher than the values for small birds and mammals at rest, which are less than 1 cal. (g. hr. °C.)^-1 (Lasiewski, 1963). The thermal conductance of resting budgerigars at 20° C. is 1 cal. (g. hr. °C.)⁻¹ (Greenwald, Stone & Cade, 1967). Thus, the flying budgerigar can increase its thermal conductance by a factor of 5. No other animal is known to me that can increase its conductance to this extent. The jack rabbit (Lepus) can increase its conductance by a factor less than 4 (Dawson & Schmidt-Nielsen, 1966), the pocket mouse (Perognathus) by a factor less than 2 (Tucker, 1965). The large increase in conductance for the flying bird is probably related to increased convection and exposure of the thinly feathered undersides of the wings and sides of the thorax during flight. It is interesting that both flying budgerigars extended the unfeathered portions of their legs into the slipstream, but only at 36–37° C. This behaviour probably increased their rates of heat loss.

The generalization that small resting birds cannot dissipate their total metabolic heat production by evaporation alone has been widely accepted, but recently this generalization has been disproven (Lasiewski, Acosta & Bernstein, 1966). My data on evaporation in flight support the conclusion of these authors that many small birds at rest can dissipate their total heat production by evaporation, and suggest that all small birds at rest could accomplish this if they could increase their ventilation to that achieved in flight. For example, a 35 g. bird could dissipate its total standard rate of metabolic heat production by an evaporative loss of 14 ·2 mg. (g. hr.)⁻¹. A flying budgerigar loses water 43 % faster than this at 18–20 ° C., and at 36–37 ° C. it loses water 350% faster.

This study was supported by a Duke Endowment Grant (no. 840926) and a National Science Foundation Grant (no. GB-3350). Mrs Marsha Poirier provided skilful technical assistance.