The Cooling Power Of Pigeon Legs

Flapping flight is a strenuous exercise which in birds requires a metabolic rate an order of magnitude greater than that at rest (Tucker, 1973; Pennycuick, 1975; Torre-Bueno & Larochelle, 1978). Since the maximal mechanical efficiency of muscles is about 25 %, some 75 % or more of the energy used during flight appears as heat. As only a small fraction (<10 %) of the heat produced while flying can be lost by evaporation without risking dehydration (Torre-Bueno, 1978; Biesel & Nachtigall, 1987), prolonged flight requires that most of this heat be dissipated by convection to the moving airstream.

The maintenance of a high body temperature at rest corresponds to a major fraction of the annual energy budget of birds, and plumage is designed to reduce this cost by offering high resistance to thermal exchange (Hart & Roy, 1967). The unfeathered and richly vascularized feet of birds can thus have a particular importance in regulating the rate of body heat loss. Support for this view has been provided by several measurements of heat loss from legs and feet, made mostly in large aquatic birds at rest (Steen & Steen, 1965; Kilgore & Schmidt-Nielsen, 1975). For these birds, the possession of long legs and/or webbed feet and their frequent immersion in a medium of high thermal conductivity obviously requires powerful heat conservation mechanisms (Johansen & Bech, 1983).

The only measurement of the cooling power of the legs during flight also comes from the study of an aquatic bird. Using telemetric measurements of blood flow and arteriovenous temperature differences, Baudinette et al. (1976) have shown that most of the excess heat produced during flight in the herring gull could be lost from the legs and feet. The authors suggested that this mechanism might not apply to species lacking the large surface area represented by the thin webbing of feet, a structure particularly rich in arteriovenous anastomoses (Midtgård, 1980).

Direct measurement of heat loss from bird legs and feet is very difficult at air speeds comparable to those encountered during flight. We have developed an indirect method based on the capacity of the legs and feet to cool a resting bird whose body has been preheated to a temperature near those recorded during flight. Applying this method to domestic pigeons, we have studied the cooling power of their hindlimbs exposed to air currents of various speeds and temperatures. Taking into consideration the differences between sitting in a restraining apparatus and performing in the wild, we have also estimated the contribution of the legs and feet to temperature regulation during flight. Since the pigeon is a terrestrial bird whose legs and feet can seldom, if ever, profit or suffer from immersion in water, it is interesting to compare their degree of cooling power and its control with that of aquatic species.

The experimental system used in this study was designed to bring the body temperature of the pigeon close to that encountered during flight to elicit a comparable recruitment of heat-dissipating mechanisms. Pigeons were heated transiently with a pectoral heating pad to increase their deep cloacal temperature (T_CLOA) to 43·1 ±01°C (x̄ ± S.D.), a steady-state body temperature near those recorded for flying pigeons (Hart & Roy, 1967; Aulie, 1971; Butler, West & Jones, 1977; Hirth, Biesel & Nachtigall, 1987). The pectoral muscle was heated since it is the main site of heat production during flight.

The experiments were performed on nine unanaesthetized domestic pigeons (Columba livia) having a mean body mass of 402 ± 24g (X̄±S.D.). They were purchased from a local breeder and kept at approximately 22°C in cages measuring 60×50×55 cm. Prior to experiments, birds were fasted for 18 h but otherwise had free access to mixed grain. Water was always available. All experiments described in this paper have been conducted with care to avoid pain and discomfort to the animals. Pigeons were gradually accustomed to the experimental apparatus and showed no signs of stress or escape reactions during the experiments.

All experiments were performed according to the same basic protocol. A preweighed pigeon was fitted with sensors, placed into a preheated restraining mould, and heated to the desired T_CLOA. It was then positioned with its legs inside the mould or hanging down in the calorimeter or in the wind-tunnel. The same medium temperatures (5·4 ± 0·4,15·4 ± 0·2 and 25·2 ± 0-2 °C) were used in water and air. Simultaneous recordings of cloacal, pectoral, room and metabolic chamber temperatures, as well as of ⁠, and EWL, were obtained at 1-min intervals for 30 min.

At least three pigeons were used at every temperature tested, each individual being measured at least twice. The intra-individual variability of all the measured variables was similar to their inter-individual variability, allowing free pooling of the data.

During all experiments, the pigeon was lightly restrained in a nearly normal resting posture by a shaped mould made of high-density polyurethane. Only the neck, the head and the unfeathered parts of the legs were covered by the mould (Fig. 1). The legs were kept outside the mould by a rubber ring loosely encircling the leg above the tarsal joint. The mould was placed into a Plexiglas box which fitted tightly onto the calorimeter or the wind tunnel.

The average temperature of the mould was continuously measured and kept within 0·2±0·3°C of the bird’s cloacal temperature by heating wires within the mould. Body heating was achieved through an electrical pad covering the pectoral muscles. The temperature of the skin under the pad was kept in a range (50–55°C) where no signs of stress or tissue damage were observed. Once the desired body temperature (43·1 ± 0·l°C) was reached, heating was stopped. The legs and feet were insulated in a polyurethane box during body heating.

Temperatures were measured with thermistors or copper-constantan thermocouples. The resistance of the thermistors was read via a scanner with a high-precision multimeter (Keithley Instruments, 177) interfaced to a computer (Apple Computers, He) for data treatment. Thermocouples were read using a digital thermometer (Sensortek, BAT-8C). All sensors were individually calibrated with a certified mercury thermometer and their response was described with an appropriate polynomial equation. The inaccuracy of the temperature measurements did not exceed 0·05 °C.

The deep cloacal (intestinal) temperature was determined with a thermistor lightly lubricated with lidocaine jelly, inserted to a depth of at least 5 cm and taped to the tail. The pectoral skin temperature was measured with a 0·4 mm thermocouple implanted subcutaneously over the middle of the right pectoral muscle and fastened to the nearest feather with sewing thread. Prior to implantation, the skin, needle (21 gauge) and sensor were disinfected with a 1 % benzalkonium chloride solution. A lidocaine solution was injected with a small needle (26 gauge) as a topical anaesthetic.

The rates of oxygen consumption and carbon dioxide production were measured in an open-flow system (Fig. 1A). The Plexiglas metabolic chamber covering the pigeon’s head was provided with a 1cm polyurethane foam collar lightly pressed on the bird’s neck to minimize the entry of air from the body mould. The airspace in the chamber (about 380 cm³) was kept at constant temperature (27·2 ± 1·4°C) by heating the inlet gas as needed. A small fan ensured the homogeneity of both temperature and gases in the chamber.

Room air was drawn into the chamber at a controlled rate (1500–1600 ml min⁻¹, at STP) which kept the volume fraction of CO₂ below 1 % and prevented the loss of respiratory gases. A fraction (250ml min⁻¹) of the gases coming into or out of the chamber was dried with Drierite and passed to a paramagnetic oxygen analyser (Beckman Instruments, E2) and to an infrared CO₂ analyser (Beckman Instruments, IR-215A).

The analysers were calibrated before and after each experiment with standard gases. Calibration of the whole system was checked by bleeding pure nitrogen or CO₂ at metered rates into the chamber. All flowmeters were calibrated at operating temperatures and pressures with the bubble meter method (Levy, 1964). The uncertainty in the determinations of and was about 2 %.

The was calculated according to Tucker (1968). Metabolic heat production was obtained from using the caloric equivalent appropriate to the prevailing respiratory exchange ratio ⁠.

The combined evaporative water loss (EWL) from the neck, head and respiratory surfaces was measured in a separate loop into which a fraction of the inlet or outlet gases was drawn at a constant rate (1200 ml min⁻¹, at STP) through a psychrometer designed from ideas provided by Wylie (1979). It consisted of a 4·5 mm diameter Teflon tube into which two small thermistors were inserted, one covered with cotton yarn and dipped in a distilled water reservoir.

The psychrometer was calibrated by flowing various combinations of dry N₂ and water-saturated standard gas through it and through the O₂ analyser. The O₂ content of the gas mixtures could then be used as an accurate estimate of their relative humidity. The temperatures were converted to vapour pressures using the Goff-Gratch equation (Goff, 1963) and then to absolute humidities using the ideal gas law. The inaccuracy in the measurement of water vapour content was about 3 %, as determined by comparison with a gravimetric method using Drierite.

The values of Ḣ_EWL were calculated from the flow rate through the metabolic chamber and from the absolute humidities of the incoming and outgoing gases. Evaporating surfaces were assumed to be at 40°C, giving a latent heat of evaporation of 2·405 kJ g⁻¹ of water.

The effect of exposing the legs and feet to air was investigated by installing the restraining box over a wind tunnel in such a way that the bird’s legs hung into the moving air (Fig. 1B). The air was pushed into the Plexiglas tunnel (10cm wide, 7·5 cm high) through a shaping funnel by mean of a cage blower driven by a variable-speed motor. The wind speed was measured with a hot-wire anemometer (Datametrics, 100 VT). The tunnel provided a low-turbulence air current whose speed was uniform within 2 % at all points more than 0·5 cm from the wall in the working section. The air temperature was measured between the bird’s legs with a thermistor, and it was controlled by placing the whole unit in a temperature-regulated room.

Experiments were conducted at a series of wind speeds between 0 and 75kmh⁻¹. Control birds were also tested at each air temperature with their legs inside the mould. In this case the wind tunnel was turned on for 30min at the highest wind speed used at a given air temperature.

The heat loss from legs and feet was calculated with equation 2 using the values of coefficients A and B determined by direct calorimetric measurements under corresponding conditions (Table 1). Ḣ_STOR was calculated as the product of body mass, tissue specific heat (3·47 J g⁻¹ °C⁻¹; Hart, 1951) and rate of change of T_CLOA obtained from the slope of the linear portion of the cooling curve.

Heat loss from the bare portion of the legs was determined by immersing the legs to the level of the tarsal joint in a calorimeter (Fig. 1A). It consisted of two boxes of Plexiglas separated by insulating material. The calorimeter was immersed in a thermostatted water bath maintained within 0·5 °C of the calorimeter temperature. Temperature homogeneity was ensured using an air-driven magnetic stirrer, and the water volume (1004 ml) was adjusted prior to measurements. The increase (typically less than 2°C) in the calorimeter temperature was measured with a thermistor. The measurements of heat transfer to the calorimeter were corrected for evaporation and parasite heat gain or loss by testing known thermal loads under operating conditions.

The water calorimeter permitted simultaneous determinations of the four main variables of equation 2 and thus allowed the calculation of coefficients A and B (Table 1). With these coefficients, the values of Ḣ_LEG as predicted from the righthand term of equation 2 were within 10 % of those obtained by direct calorimetry.

Our results show that the exposure of legs and feet strongly enhances the ability of a preheated pigeon to dissipate heat at 25°C (Fig. 2). When the legs and feet of the pigeon were kept inside the mould, the body temperature remained essentially constant at all wind speeds. This shows unequivocally that, in our experiments, the body cools primarily as a result of leg exposure. Even in the absence of wind, the contact of the legs and feet with air permitted a significant decline in body temperature. With winds of increasing strength, body cooling was more rapid, with a maximum rate of 0·36°C min⁻¹ at the highest wind speeds. Within minutes, body temperature was brought down in a linear fashion to 40·9 ±0·4°C. Further cooling proceeded at a reduced rate until the body temperature stabilized at 40·3 ± 0·4°C, a normal value for resting pigeons. Similar results were obtained at 15 and 5°C. At a given temperature, the maximum body cooling rates recorded in air were 70–76 % of those measured in water.

The absolute maximum heat loss from the pigeons’ legs and feet exposed to air, as calculated from the linear portion of the cooling curves, averaged 12·0 ±0·3, 11·2 ±0·8 and 9·3 ± 1·0 W at 5, 15 and 25°C, respectively (Fig. 3). The dependence of the maximum heat loss on the wind speed decreased with increasing wind speed (Fig. 3). The decrease was more pronounced at high dissipation levels, and air speeds above 37·5 km h⁻¹ brought no further gain in cooling power. This behaviour is thus different from that predicted for warm cylinders of similar diameter (about 5 mm) having a surface temperature independent of the wind speed. In the range of Reynolds number relevant to our conditions (800 < Re < 5400), the heat loss from such cylinders would be a function of wind speed to the 0·5 power (Kreith & Black, 1980). Should the pigeons’ legs and feet behave in this way, their rate of heat loss would double as the wind speed was augmented from 12·5 to 50 km h⁻¹. Significantly smaller increases were obtained, namely 20, 51 and 77 % at 5, 15 and 25°C, respectively.

Air temperature also had a strong influence on the heat loss from pigeons’ legs and feet (Fig. 4). Heat transfer theories predict that the relationship between the rate of heat loss by forced convection over a dry body and the thermal gradient (AT) between its surface and the ambient fluid temperature will be linear and will extrapolate to the origin. It can be assumed that at moderate rates of heat loss, the surface temperature of the legs and feet will be close to the body temperature in hyperthermic pigeons. Furthermore, the skin of the legs and feet can be considered as a dry surface since its potential for EWL is negligible (Bernstein, 1974). The rate of heat loss observed for a thermal gradient of 18°C and a wind speed of 12·5 kmh⁻¹ can then be used to predict the equations relating Ḣ_LEG and ΔT, taking into account the expected influence of wind speed.

Although the low and moderate values of Ḣ_LEG are close to the predicted curves, departure from linearity becomes apparent as the rate of heat loss approaches its maximum at higher wind speeds. For example, maximum, Ḣ_LEG at 5°C was only 29% greater than that measured at 25 °C, whereas it should have been 125 % greater according to ΔT. It is interesting to note that under still air conditions the experimental curve does not extrapolate to the origin. This is to be expected as the convection coefficient for vertical cylinders increases with the thermal gradient to the 0·25 power when natural convection predominates (Kreith & Black, 1980).

The rates of oxygen consumption of our restrained birds were relatively constant and averaged 1·02 ± 0·10 ml g⁻¹h⁻¹ (corresponding to 2·16 ± 0·18 W) when the pigeons’ feet were exposed to air or water at 15 and 25 °C. These metabolic rates are about 11 % above predicted basal rates and similar to those reported for unrestrained pigeons by Calder & Schmidt-Nielsen (1967; 0·99 ± 0·03 ml g⁻¹ h⁻¹) and Graf (1980; about 1·06mlg⁻¹ h⁻¹), indicating that our restraining conditions were not stressful. However, the of pigeons with their feet exposed to 5°C increased over the experimental period, reaching 1·70 ± 0·26 ml g⁻¹ h⁻¹ (3·71 ± 0·57 W). As the pigeons were then resting calmly and had a body temperature below 39 °C, we attributed this higher metabolic rate to shivering.

During the experiments, the respiratory exchange ratio (R) averaged 0·70 ± 0·01 and showed no dependence on temperature or wind speed.

Panting began during the heating phase when T_CLOA reached about 42·5°C. It ceased almost immediately following immersion of the legs in water, but in air panting often continued for 1–5 min, according to the wind speed and air temperature. It should be pointed out that pigeons with their legs inside the mould panted during the entire experimental period, even if air at 5°C was flowing at high speed a few centimetres below the insulating mould. In still air, the duration of panting depended on the air temperature, ranging from about 10 min (at 5 °C) to over 30min (at 25°C).

Following the exposure of legs and feet to wind at 25 °C, the time course of EWL from the head and respiratory surfaces of pigeons was similar to that of the body temperature, although it was more variable and less sensitive to wind speed and temperature. During the linear decline of T_CLOA at 25°C, EWL averaged 28·7 ± 5·9 mg min⁻¹ (1·15 ± 0·24 W). The highest value of EWL (35·0 ±2·4 mg min⁻¹ or 1·40 ± 0·10 W) was observed when the pigeons’ legs were kept inside the mould during wind-tunnel experiments at 25°C.

EWL was not measured during experiments conducted in air at 5 and 15 °C, and the values of EWL obtained in air at 25 °C were used to estimate H_LEG at 5 and 15 °C. This should produce a slight underestimation of H_LEG (<5 %) since at low temperatures a smaller reliance on EWL was indicated by the earlier arrest of panting.

Our results show that the potential for heat dissipation of the legs and feet in a terrestrial bird can be considerable. In the pigeon, we have observed maximum heat losses from the legs and feet ranging from four to six times the resting metabolic heat production. The cooling power of legs and feet should be particularly useful to a flying pigeon. But how applicable are our results to flight conditions?

Whereas our data were obtained at combinations of temperatures and air speeds which would be encountered by flying pigeons (Michener & Walcott, 1967), they were collected from resting subjects. There is, however, little reason to believe that our experimental system, designed to create thermoregulatory needs similar to those encountered during flight, has conferred to the legs and feet a cooling power unavailable to freely flying birds. The fact that for aerodynamic reasons other body surfaces should be used first for heat dissipation in flying birds is unlikely to limit the maximum capacity of the legs and feet to cool the body core. This view is supported by observations of both vascular anatomy and flight behaviour. The venous blood coming from the flight muscles returns to the heart before going to the heat-dissipating surfaces through independent arteries, thus making the legs and other sites function as parallel, rather than serial, heat exchangers. Furthermore, flight duration in pigeons is greatly reduced at air temperatures higher than 24°C, even in the absence of any solar load, and signs of hyperthermia are observed after landing (Aulie, 1971; Hirth et al. 1987). It would be surprising if birds could suffer from hyperthermia and dehydration during flight without having used the full cooling power of their legs and feet as they readily do under resting conditions.

Another point of importance concerns the degree of exposure of legs and feet to the moving air. For practical reasons, the legs of our pigeons were forced to hang continuously in an almost fully extended position at right angles to the air current. In contrast to many other terrestrial birds (Frost & Siegfried, 1975; Bryant, 1983), pigeons have not been reported to let their legs hang while flying freely during hot days. However, some evidence indicates that flying pigeons regulate the exposure of their legs and feet according to their thermoregulatory needs. On hot days, pigeons flying in the wild often keep their feed extended below the tail, with the toes well spread (unpublished observations). This behaviour may well produce an optimal use of the legs and feet for heat dissipation. The cooling power of the legs and feet has a low sensitivity to wind speeds around normal flight speeds (Fig. 3), suggesting that maximal contact with the main airstream may not be needed. Since fully hanging legs increase the body drag of pigeons by about 15 % (Pennycuick, 1968), the small gain in cooling power obtained by complete extension of the legs could be offset by the increase in heat production due to the muscular work needed to overcome the added drag. Under the conditions prevailing in a wind tunnel, flying pigeons also vary the exposure of their legs and feet according to the air temperature and, at 25°C and above, they hang their legs almost completely (Biesel & Nachtigall, 1987).

The minimum power requirement for a flying pigeon can be estimated from available data collected during flight under natural conditions (LeFebvre, 1964) or in wind tunnels (Butler et al. 1977; Rothe, Biesel & Nachtigall, 1987), as well as from current models of bird flight (Pennycuick, 1968; Tucker, 1973; Greenewalt, 1975; Rayner, 1979). After taking into account the drag and weight attributed to respiratory masks in wind-tunnel studies, all data and models are in remarkably close agreement and predict a minimum flight power of about 25 W for a 400-g pigeon. Assuming, as most authors do, that the mechanical efficiency of muscles during flapping flight is 25 % and that the resting metabolism is an acceptable estimate of the non-muscle metabolism, the rate of heat production during sustained flapping flight in the pigeon would be about 19 W.

Our results suggest that a flying pigeon is able to eliminate large amounts of metabolic heat by forced convection from its hindlimbs. While representing only 7 % of its total skin surface (Walsberg & King, 1978), the legs and feet of a pigeon could dissipate between 50% (at 25 °C) and 65% (at 5 °C) of the total heat produced during flight at air speeds above 37·5 km h⁻¹ (Fig. 3). In the herring gull, a larger bird with webbed feet and relatively long legs, hindlimbs can dissipate some 80 % of the heat produced during flapping flight (Baudinette et al. 1976).

The cooling power of the legs and feet can also be of importance for resting birds. In a perched pigeon, even a slight breeze (12·5 km h⁻¹) at 25°C would allow heat dissipation corresponding to 240 % of the metabolic heat production (Fig. 3). This could facilitate the unloading of heat accumulated during intense flight or exposure to the sun.

In spite of their impressive cooling power, the performance of the pigeon’s legs and feet as heat dissipators appears far from that expected for ideal cylinders. Efficient heat exchangers have a low internal resistance to heat transfer. Thus, their surface temperature is close to their core temperature and depends little on the rate of heat exchange with the environment. Therefore, for a given exchange area and temperature gradient, the main limit to the capacity for convective heat exchange is the resistance of the boundary layer in the ambient fluid near the contact surface. This resistance determines the relationship between the rate of heat exchange and the ambient fluid speed. Under the conditions prevailing in these experiments (see Results), the rate of heat exchange should increase with the square of the wind speed.

The behaviour of pigeon appendages obviously differs from that of ideal warm cylinders, and the value of H_LEG reaches a plateau at relatively low wind speeds. Therefore, the resistance of the boundary layer of air around the legs and feet is not the primary limiting factor of the maximum heat loss. The surface temperature of the legs and feet probably drops at high heat flux, suggesting that the internal transport of heat to the dissipating surface is the limiting step. This view is supported by the observation that, at a given temperature, Ḣ_LEG in stirred water was only 3–5 times as great as in still air, although the thermal conductivities of the two media differ by a factor of at least 20.

The transport of heat to the surface of legs and feet is a function of the rate of heat input by the blood and the thermal resistance of the tissues between the blood vessels and the skin surface. The minimum blood flow to the pigeon legs required to explain the maximal observed heat losses can be estimated by assuming ideal exchange, with blood arriving at cloacal temperature and leaving at ambient temperature. Taking the blood density and specific heat as 105 g ml⁻¹ and 3·77 J g⁻¹ °C⁻¹, respectively, the minimum blood flow to the legs ranges from about 5 ml min⁻¹ (at5°C) to 8 ml min⁻¹ (at25°C). Using the relationship between heat production and cardiac output in resting pigeons (Grubb, 1982), we calculated that the proportion of the cardiac output (140 ml min⁻¹) involved in the blood flow to the feet ranged from 4 % (at 5°C) to 6 % (at 25°C). Even if legs and feet are far from ideal exchangers, it seems unlikely that blood flow is the main limiting factor during flight, since the cardiac output should then be several times larger than at rest (Butler et al. 1977). In the resting gull, 6 % or less of the cardiac output goes to the feet and, during flight, the blood flow to the legs is increased about four times above resting levels (Baudinette et al. 1976).

It must therefore be concluded that the thermal resistance of the leg and foot tissues, rather than that of the boundary layer of air, sets the main limit to the cooling power of pigeon hindlimbs.

Obviously, the possession of a surface with a high potential for heat loss in a homeothermic animal requires mechanisms to adjust its function to differing thermoregulatory needs. When heat conservation is required, pigeons display a variety of behavioural and physiological strategies for reducing heat loss through their pelvic limbs. Sleeping pigeons often lie on their feet or stand on one leg, curling the toes of the other foot and pulling it under feather cover. During flight, pigeons vary the exposure of their legs and feet and can also retract them under the flank feathers (Pennycuick, 1968; Biesel & Nachtigall, 1987). The pigeon leg has two sets of veins, one superficial and presumably recruited for heat dissipation, and the other intimately associated with main arteries and forming a simple countercurrent exchanger to promote heat conservation (Midtgârd, 1981).

Measurements of surface temperature and relative blood flow in pigeons’ feet indicate the presence of vasomotor controls working in accordance with the thermoregulatory needs (Bernstein, 1974). Our data show that the rate of heat loss through legs and feet immersed in a water calorimeter at 5°C attains 17·2 ± 1·8 W in hyperthermic pigeons (cloaca at 42·43°C), whereas it is only 2-2 ± 0-1W in hypothermic subjects (cloaca at 39·40°C). This eightfold range is an order of magnitude less than that reported for birds adapted for contact with water, such as ducks and gulls (Midtgård, 1980) which can decrease the heat loss through their extremities to about 0·5 W (Kilgore & Schmidt-Nielsen, 1975). Nevertheless, the eightfold control range observed in the pigeon, if operating in still air at 5 °C, could reduce the rate of heat loss through the legs and feet from 5·8 to 0·7 W, the latter value corresponding to 34% of the normal resting metabolic rate.

We conclude that the results obtained with the pigeon suggest that exploitation of self-generated or ambient wind conditions and physiological control allow the hindlimbs of a terrestrial bird to work as powerful thermoregulatory organs. Moreover, the capacity of the legs and feet for heat dissipation, which is several times greater than the normal resting heat production, appears to be a major factor determining the range of ambient temperatures over which prolonged flight can be sustained.

The authors wish to thank Michel Ducharme for his helpful contribution to this work, Helga Guderley and Albert Craig for their critical reading of the manuscript, and Céline Dallaire for her skilful graphic work.