Respiration in Exercising Fowl: I. Oxygen Consumption, Respiratory Rate and Respired Gases

Many studies have been made of respiration in flying birds (see Butler & Woakes, 1980) but the respiratory activity of running birds has received scant attention. Several workers have examined the energetics of avian running (see brief reviews by Bamford & Maloiy, 1980 and Brackenbury & Avery, 1980) but Kiley, Kuhlmann & Fedde (1979) are the only authors to have measured changes in respiratory characteristics in a running bird, in this case the duck. In the present paper we report the results of an investigation of the respiratory responses of hens subjected to graded work loads on a treadmill at normal and elevated air temperatures. These experiments were designed to elicit a response to variable combinations of internal (metabolic) and external heat loads.

Six adult female domestic fowl (mean b.w. 2-2 kg) which had been raised free-range before purchase were subjected to two weeks preliminary training on a treadmill, followed by eighteen weeks regular exercising during which each animal performed B average of two 10 min runs per day at speeds of 1·24−4·3 h^-1 (0·35−1·2 ^{m 8-1}). The running surface of the treadmill measured 153x43 cm and was enclosed on three sides by 1 m high Perspex walls. Between experiments the birds were housed in open cages and maintained on a diet of mixed cereals. Environmental temperature was varied over two ranges: normal (20±2 °C) and high (32 ±2 °C), the latter being produced by directing a blow heater into the treadmill chamber before and sometimes during exercise.

• Oxygen consumption and carbon dioxide production were measuMd by a technique similar to that used by Brackenbury & Avery (1980) in a study of Energetics of domestic cocks. Expired gases were collected from a loose-fitting plastic mask secured by rubber bands behind the comb and upper neck of the bird. The mask was connected to a 1 m length of 0·5 cm diameter tubing through which air was drawn at 8−30 1 min^-1 by a pump connected in series with a dry gas meter. Samples of the collected gas were drawn at ca. 0·2 1 min^-1 through two pairs of Drierite columns into a Beckman LB2 infra-red CO₂ analyser and a Beckman OM-n paramagnetic oxygen analyser, the calibrations of which were checked regularly against precision gas mixtures (P. K. Morgan Ltd, Kent, England). The and of the gas were displayed continuously on a Grass model 7 pen-recorder adjusted to give a 2·5 cm pen deflexion for a 1 % change in gas concentration. and were calculated by multiplying the fractional change in gas composition (Fig. 1 a) by the flow rate reduced to STPD conditions. The mean RQs were close to unity (see Results), consequently no correction factor for ⁠, due to the unequal exchange of gases, was required.

  Fig. 1.

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  Examples of original recordings of (a) concentration of O₂ in the gas collected from the mask during the determination of $V˙o2$⁠; W changes in P_O2 of the expired gas; (c) expired P_O2 displayed on expanded time scale to show the rapid drop in gas pressure due to the arrival of gas from the lung; below, the air pressure changes in the air sac, recorded by means of a manometer, indicate the phases of respiration; (d) interclavicular air sac P_O2. Arrows indicate the beginning and end of each run. All data are taken from separate exercises at 3·6 km h^-1 in air temperatures of 20 ± 2 °C.

  Fig. 1.

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  Examples of original recordings of (a) concentration of O₂ in the gas collected from the mask during the determination of $V˙o2$⁠; W changes in P_O2 of the expired gas; (c) expired P_O2 displayed on expanded time scale to show the rapid drop in gas pressure due to the arrival of gas from the lung; below, the air pressure changes in the air sac, recorded by means of a manometer, indicate the phases of respiration; (d) interclavicular air sac P_O2. Arrows indicate the beginning and end of each run. All data are taken from separate exercises at 3·6 km h^-1 in air temperatures of 20 ± 2 °C.

• Breath-to-breath changes in expired were measured in animals wearing a second type of mask that fitted tightly over the beak and nostrils and was connected to the atmosphere by a short length of 0·5 cm diameter tubing through which the animal breathed. The inner end of the tube was shaped to fit inside the partially opened beak, thereby preventing leakage of expired gases. A sample of gas was drawn from the tube at ca. 0·2 1 min^-1 directly into the heated inlet tube of a second O₂ analyser ; in these conditions the rise time of the gas analyser was ca. 0·1 s and the expired waveform could be faithfully duplicated during rest and exercise (Fig. 1b, c).

• Interclavicular sac was continuously monitored via plastic cannulae (int. diam. 0·35 cm) permanently sewn into the air sacs of four animals (Fig. i d). A sample was drawn from the sac at ca. 20 ml min^-1 through Drierite and the sampling delay was approximately 12 s. End-tidal and were finally expressed in BTPS conditions.

• Respiratory frequency (f) was measured using the same loose-fitting mask as described under (i). Air was drawn through the mask at a convenient flow rate and variations in the temperature of the stream due to inhalation and exhalation were detected by a thermistor and displayed on the pen-recorder.

Gas exchange, and f were measured in four separate series of experiments performed in identical conditions; simultaneous monitoring of all these variables would have imposed undue discomfort on the animals. Each variable was continuously recorded before, during and immediately after the exercise. The animals received no artificial stimulation to running, apart from occasional prompting from an operator seated throughout the experiment near the open end of the treadmill chamber. The exercise was begun as soon as the animals appeared rested on the treadmill. During high-temperature experiments this meant that the animals had probably not reached a condition of full thermal equilibrium with the chamber environment before exercise and part of the measured increase in respiratory rate oberved during exercise would therefore have occurred even if exercise had not taken place. However, measurements on the animals left for 10−15 min on the treadmill without exercise demonstrated that the changes in f were minor compared to those induced by the exercise.

The resting rose from 8·96 ± 0·4 ml O, STPD kg^-1 min^-1 when the animals were seated outside the treadmill chamber to 15·20 ml kg^-1 min^-1 when placed on the treadmill before a run. During the first minute of exercise rose rapidly and achieved a steady state value within the next 2·3 min (Fig. 2). At the start of lowspeed runs there was a transient overshoot in ⁠, similar to that measured in flying pigeons (Butler, West & Jones, 1977), but this was not observed at the highest speed* (3·6 and 4·3 km h^-1). The steady-state -speed relationship was approximately linear up to 3 km h^-1 with a slope (incremental cost of locomotion) of 0·46 ml O₂ kg^-1 m^-1 but this rose to 0·77 ml kg^-1 m^-1 at higher speeds (Fig. 3). At high temperatures increased by a further 15 ml kg^-1 min^-1 at 2·9, 3·6 and 4·3 km h^-1 (Fig. 2). The mean pre-exercise and exercise RQs were 0·97 (± 0·02 s.E.) and 0·96 (±0·015 ^S-^E-) respectively.

Both at rest and during exercise the expired remained first at atmospheric then fell rapidly to its end-tidal value, indicating that there was little mixing of dead space and lung gases (Fig. 1,c). The resting ⁠, taking into account the fact that the end-tidal plateau was not perfectly flat, was 106·9 ± 0·4 S E-Torr. The resting was 0·8±0·4 S.E. Torr. Like ⁠, and both ^rose rapidly at the start of rcise, reaching steady-state values within a few minutes (Fig. 2). The steady-state and rose in a parallel manner with running speed, maintaining the same difference as at rest (Fig. 3). At 32 + 2 °C increased by a further 3-4 Torr at die highest speeds (Fig. 3) but reliable measurements of mean could not be obtained since the animals frequently displayed bursts of rapid pant-like breathing which was apparently so shallow that the lung gas failed to register fully on the gas analyser. This was not due to slowness of response of the gas analyser, since, as in similar cases described in resting hyperthermic birds (Bech, Johansen & Maloiy, 1979; Brackenbury, Avery & Gleeson, 1980), the zero or atmospheric gas level registered immediately after each expiration, as it did during normal-temperature exercise (Fig. 1 c).

Respiratory frequency increased throughout exercise except at 1·24 and 2·15 km in normal air temperatures where there was a slight overshoot at the beginning Exercise (Fig. 4). The mean f measured over the last 5 min of exercise rose with speed and air temperature (Figs. 3, 4). After exercise at normal temperatures, f declined immediately, reaching within 25 % of its pre-exercise value after 2−3 min (Fig. 4). At 32 ±2 °C, f continued to rise after exercise; following the most intense exercise, vigorous panting was maintained for up to 40 min.

The running performance of female fowl shows several points of difference from that of the male fowl studied by Brackenbury & Avery (1980). First, the maximum sustained running speed of the hens was only half that achieved by the cocks (9 km h^-1) although it was considerably greater than the maximum speed of 2·4 km h^-1 tolerated by hens in Van Kampen’s (1976) study. Second, the maximum steady-state of the hens, equivalent to eight times their resting metabolic rate, was 36% less than that found in the males which was 12 times their resting metabolic rate. This disparity in metabolic scope may be in part related to natural variation between the two different populations involved in the respective studies, but there appear to be real differences in physiological and/or biomechanical performance. The hens were in regular laying condition and the diversion of energy resources to egg production must to some extent have narrowed the metabolic scope for activity. Also hens were extremely reluctant to run during the hour preceding oviposition and care was taken to avoid experimentation at this particular time.

At normal temperature the -speed relationship of cocks was linear over the entire speed range investigated, 2−9 km h^-1. A similar relationship has been found in rhea, turkey, guinea fowl, bobwhite, chukar, goose (Fedak, Pinshow & Schmidt-Nielsen, 1974), ostrich (Fedak & Seeherman, 1979) and Marabou stork (Bamford & Maloiy, 1980). The -speed relationship of hens was linear up to 3 km h^-1 (Fig. 3) and the incremental cost of locomotion was almost identical to that predicted by the equation of Taylor (1977). Although the incremental cost of locomotion rose at higher speeds, the over this range was almost indistinguishable from that of the males. It is possible that the change in the incremental cost of locomotion above 3 km h^-1 is related to a transition in gait from walking to true running (involving an airborne phase between steps) as has been shown to be the case in human locomotion (Margaria et al. 1963). This would suggest that whereas cocks are capable of true running over a large range of speeds, hens are only just capable of running, or are extremely unwilling to run at faster speeds.

Both genders showed an increase in the cost of locomotion at elevated temperatures (Fig. 3). In each case the maximum additional cost was similar (12·5−15·0 ml O₂ STPD kg^-1 min^-1) although it was incurred at a much lower speed in hens (3·4 km h^-1) than in cocks (6−7 km h^-1). If, as Brackenbury and Avery proposed, a significant part of the additional cost is accountable to the extra work done by the respiratory muscles in hyperventilating the lung air sac system, the preceding comparison Íuggests that hens suffer hyperthermal stress at considerably lighter work loads than nale birds.

Minute volume was not measured in the present study but the observed increases in end-tidal and interclavicular sac during exercise (Figs 1−3) indicate that the lungs are ventilated in excess of metabolic requirements. Piiper, Drees & Scheid (1970) found a similar differential between the end-tidal and interclavicular sac gases of resting fowl as was shown in this study. This differential probably results from the mixing, within the mesobronchus, of the relatively stale gas from the cranial sacs (interclavicular, cranial thoracic and cervical) with relatively fresh gas that has leaked along the mesobronchus from the caudal sacs (caudal thoracic and abdominal) during expiration. Moreover, the observation that this differential was consistently maintained at different grades of exercise argues against the suggestion made by Duncker (1971) that activity brings about a change in the pattern of lung ventilation, namely a switching of ventilation from the neopulmo to the palaeopulmo.

Fig. 3. shows that the degree of lung hyperventilation increases progressively with work rate and is greater at elevated air temperatures. Exactly how this affects the overall oxygen extraction of the respiratory system cannot be assessed since the minute volume is unknown, although it seems likely that the extraction falls progressively with work load both at normal and raised air temperatures. Kiley et al. (1979) reported that ducks running on a treadmill at speeds of 0·9 and 1·47 km h^-1 hyperventilated, and this produced a fall in both interclavicular sac and arterial ⁠. These authors concluded that the primary stimulus to hyperventilation was a rise in body temperature, and Flandrois, Lacour & Osman (1971) arrived at a similar conclusion in regard to exercising dogs. The latter displayed a two-phase increase in ventilation : an initial rapid rise in both f and at the start of the exercise, stimulated by afferent activity in muscle and joint proprioceptors (neurogenic drive), and a delayed, much slower increase in f and due to rising body temperature (hyperthermal drive). A two-stage increase in f can be recognized in fowl during normal temperature exercise (Fig. 4) and was also shown by flying pigeons (Butler et al. 1977) and barnacle geese (Butler & Woakes, 1980). However, it was not evident in the ducks of Kiley et al. nor in fowl performing high-temperature exercise (Fig. 4): this does not mean that a neurogenic component to the ventilatory drive was lacking but more probably that it was masked by the powerful hyperthermal drive.

From measurements of oxygen consumption and minute volume, Bernstein (1976) showed that in the crow Corvus ossifragus oxygen extraction remained unchanged during flight at an air temperature of 20 °C but fell from 0·195 to 0·132 at 25 °C. Evidently at 20 °C the crow is capable of maintaining thermal balance by heat transfer through the skin, whereas at the same temperature the exercising fowl must augment heat loss through the respiratory system. Barnacle geese may resemble fowl more closely than crows in this respect, since Butler & Woakes observed that they began panting immediately after flight despite relatively low air temperatures (10·13 °C), presumably as a result of increased body temperature ; whilst Kiley et al. noted that running ducks became hyperthermic even at 8 °C.

This work was supported by the Science and Agricultural Research Councils.