SHORT COMMUNICATION ANALYSIS OF RESPIRATORY PATTERN DURING PANTING IN FOWL, GALLUS DOMESTICUS
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1 J. exp. Biol. 116, (1985) 487 Printed in Great Britain The Company of Biologists Limited 1985 SHORT COMMUNICATION ANALYSIS OF RESPIRATORY PATTERN DURING PANTING IN FOWL, GALLUS DOMESTICUS BY M. GLEESON Department of Veterinary Physiology, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh EH9 1QH Accepted 13 November 1984 When exposed to hot environments, birds depend mostly on respiratory evaporative cooling in order to maintain body temperature since cutaneous evaporation is limited for most species because they lack sweat glands. As well as serving this thermoregulatory function the respiratory system must also accommodate the obligatory requirement of adequate gaseous exchange. The hyperthermic bird must increase ventilation rates over evaporative surfaces in the respiratory system and buccopharynx for cooling purposes and yet avoid a severe blood hypocapnia and alkalosis (Calder & SchmidtNielsen, 1968). Recently Bech, Johansen & Maloiy (1979) showed that flamingoes, Phoenicopterus ruber, avoid hypocapnia during panting by restricting hyperventilation to the respiratory deadspace. This is achieved by increasing respiratory frequency, f, but reducing tidal volume, VT, to a value which closely matches the tracheal deadspace volume, VD. AS a result of the diminished VT, carbon dioxide accumulated within the respiratory system and rapid, shallow panting was periodically interrupted by bursts of1 3 deeper breaths which served to flush out the excess carbon dioxide. A similar pattern of breathing has been observed in domestic fowl by Gleeson & Brackenbury (1983). These authors showed that the carbon dioxide accumulated during rapid shallow breathing in the posterior (abdominal) air sacs as a result of the increase in the VD/VT ratio. Other authors have reported an increased f and reduced VT in the panting fowl (Kassim & Sykes, 1982; Arad & Marder, 1983) but the diphasic pattern of breathing during panting has not been adequately described or quantified although its presence is apparent from earlier records of breathing movements in the panting fowl (Romijn & Lokhorst, 1961). Some forms of diphasic panting also occur in other species of bird, although there is considerable variation in the frequency and regularity of the alternating patterns of breathing between species (for a review see Bech et al. 1979). Rectal temperature and ventilatory variables were monitored continuously in six adult female domestic fowl, awake, breathing air and sitting in a plethysmograph similar to that described previously (Brackenbury, Avery & Gleeson, 1982). Ambient temperature, Tarn was controlled at 20 C for 60 min and then raised to 35 C over the Key words: Ventilation, respiratory pattern, chicken, hyperthermia.
2 488 M. GLEESON next 30min. Measurements were made continuously for a further 60min during which time the birds exhibited a typical diphasic panting respiratory pattern. Recordings of inspiratory and expiratory durations, tidal volume and rates of inspiratory and expiratory air flow were recorded on a chart recorder and also on magnetic tape for computeraided analysis, the results of which are shown in Table 1. Fig. 1 shows a plethysmographic record of breathing pattern in a chicken during (A) eupnoea at 20 C and (B,C) panting at 35 C. The diphasic pattern of breathing can quite clearly be distinguished in the panting bird. Brief periods of slower, deeper breaths (referred to as flushouts) periodically interrupt the longer sequences of rapid shallow breathing. The bursts of slower, deeper breathing are usually of 13 breaths duration in the fully panting bird (viz when f >240min~ 1 ). Trace C demonstrates that the sequences of slower breathing always begin with a prolongation of the expiratory phase and a slowing of the rate of expiratory airflow to a value similar to that observed during eupnoea at 20 C (Table 1). This causes a reduction in instantaneous minute volume (Table 1) and indicates a temporary diminution of respiratory drive compared to polypnoea. However the diminution of airflow rate is restricted to the expiration(s) of the flushout phase since the rate of inspiratory airflow is unchanged from that observed during the polypnoeic sequences (Table 1). At the end of each prolonged expiration, the bird breathes in and, if the inspiration is large enough, resumes rapid shallow breathing. Thus, during polypnoea the bird maintains a higher functional residual capacity (FRC) which is periodically deflated to flush out the excess carbon dioxide accumulated in the posterior air sacs. In mammals it has been suggested (Bradley, von Euler, Marttila & Roos, 1975) that the increase in respiratory rate with increased body temperature may be caused by either an increase in the rate of rise of inspiratory activity or a decrease in the inspiratory offswitch threshold, or both in combination. A similar model could be proposed to account for the increase in respiratory frequency observed in the heatstressed bird. However, in the polypnoeic phase in the panting chicken the actual Table 1. Ventilatory variables in awake chickens breathing air at ambient temperatures of20 C and 35 C Body weight (kg) Rectal temperature ( C) Phase duration (s) Breathing frequency f (min~') Tidal volume VT (ml BTPS) Minute volume VE (ml BTPS min" 1 ) Inspiratory duration Tl (s) Expiratory duration TE (a) Mean rate of inspiratoryflow VT/TI (ml BTPS S" 1 ) Mean rate of expiratoryflow VT/TE (ml BTPSS" 1 ) Eupnoea at Tarn of20 C l6(±0l) 415 (±02) 180 (±37) 311 (±24) 560 (±51) 133 (±013) 200 (±054) 234 (±10) 155 (±14) Diphasic panting at Tarn of 35 C Flushout phase Polypnoeic phase 428 (±03) 28 (±07) 160 (±30) 368 (±85) 298 (± 16) 236 (±36) 70 (±05) 869 (± 122) 2086 (± 72) 036 (±011) 0102 (±0007) 127 (±050) 0099 (±0010) 655 (±30) 686 (±17) 186 (±16) 707 (±19) Data based on six animals from the computeraided analysis of 200 breaths (eupnoea), 50 breaths (flushouts) and 400 breaths (polypnoea) from each bird. S.D. in parentheses.
3 Respiratory pattern during panting in fowl 489 Inspiration A Inspiration B 30 ml 30 ml 60s 60s Inspiration 30ml v Q xf 10s Fig. 1. Plethysmographic record of breathing pattern in a chicken, (A) at Tarn of 20 C; (B and C) at Tarn of 35 C, clearly showing the diphasic panting breathing pattern. Note expanded time scale in C. Trace C is not a directly expanded version of Trace B. volume above normal (eupnoeic) FRC at which inspiration is terminated is very similar to that during normothermic eupnoea, since the polypnoeic breathing is already shifted into the inspiratory phase (Fig. 1). Therefore it appears that a decreased offswitch threshold is not a necessary requirement for a model to explain the increase in respiratory rate at elevated ambient temperatures in the chicken. Rather, an increased rate of rise of inspiratory activity in combination with a maintained inspiratory shift is required. The periodic prolonged expirations seen in the panting bird could be brought about by a temporary decrease in the drive to maintain the inspiratory shift, thus allowing deflation to flush out stale air from the posterior air sacs. The tidal volume of the flushouts is variable but on average is 236 ml. Thus, the flushout breaths are still somewhat faster and shallower than those recorded during eupnoea at Tam of 20 C (Table 1). Tidal volumes during the polypnoeic sequences in the panting chicken at Tam of 35 C are, on average, slightly higher than the upper respiratory deadspace volume (56±02ml; N=6 birds) measured postmortem. The volume of the syrinx, trachea, larynx and oral cavity to the base of the beak in each bird was determined by clamping the extrapulmonary primary bronchi at their origin and filling the space with water from a syringe. These values of deadspace volume, however, are slightly smaller than the total upper respiratory deadspace volume. The volumes of the primary bronchi and mediodorsal secondary bronchi were not measured because of the difficulty in filling these tubes with water. Using the measurements of Payne (1970) and King & Molony (1971) and considering the smaller size of the birds used in this study I estimate that volume to be about 05 ml. Therefore a value of 6*1 ml is probably a more accurate estimate of the total upper respiratory deadspace volume in these birds. Careful analysis of tidal volumes as recorded in Trace C (Fig. 1) reveals that some breaths during the polypnoeic phase of panting are actually shallower than the anatomical VD.
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5 Respiratory pattern during panting in fowl 491 The regularity with which the bursts of slower deeper breaths interrupt the polypnoeic sequences is variable both within and between birds; the average duration of each polypnoeic sequence being 16 ± 3 s (Table 1). The duration and depth of the periodic flushouts is also variable and there was no significant correlation between the duration of the polypnoeic sequence and the size or duration of the preceding or following flushout. The diphasic panting pattern of breathing was not affected by subjecting the chickens (N=6) to an atmosphere of pure oxygen or 14% O2 in N 2 (Table 2), indicating that oxygen requirement is not a factor directly responsible for the occurrence of the diphasic pattern. Furthermore, the minute volume, tidal volume and respiratory frequency of the panting chickens were not affected by the Plo 2 in the range mmhg. Bech et al. (1979) suggested that the physiological significance of the regular flushouts observed in the panting flamingo were to maintain an adequate gaseous exchange. However, these findings suggest that oxygen requirement is not directly involved and the most likely physiological significance of the periodic prolonged expirations seen in the panting bird is that they flush out the carbon dioxide accumulated in the respiratory system during the sequences of rapid shallow breathing (Bech et al. 1979; Gleeson & Brackenbury, 1983). Since birds possess intrapulmonary receptors that are sensitive to both static and dynamic changes in local Pco2 (Scheid, Gratz, Powell & Fedde, 1978), these receptors may play a role in the periodic switching of the respiratory pattern and possibly in the initiation of the panting response itself. Measurements of intrapulmonary chemosensitive receptor discharge during panting would help clarify this possibility. REFERENCES ARAD, Z. & MARDER, J. (1983). Acidbase regulation during thermal panting in the fowl (Callus domesticus): comparison between breeds. Comp. Biochem. Pkysiol. 74A, BECH, C, JOHANSEN, K. &MALOIY, G. M. O. (1979). Ventilation and expired gas composition in the flamingo, Phoenicopterus ruber, during normal respiration and panting. Physiol. Zool. 52, BRACKENBURY, J. H., AVERY, P. & GLEESON, M. (1982). Effects of temperature on the ventilatory response to inspired CO2 in unanaesthetized domestic fowl. Respir. Physiol. 49, BRADLEY, G. W., VONEULER, C, MARTTTLA, I. &Roos, B. (1975). A model of the central and reflex inhibition of inspiration in the cat. Biol. Cybernetics 19, CALDER, W. A. & SCHMDTNEILSEN, K. (1968). Panting and blood carbon dioxide in birds. Am.J. Physiol. 215, GLEESON, M. & BRACKENBURY, J. H. (1983). Ventilation, gaseous exchange and air sac gases during moderate thermal panting in domestic fowl. Q.JlExp. Physiol. 68, KASSIM, H. & SYIES, A. H. (1982). The respiratory responses of the fowl to hot climates. J. exp. Biol. 97, KINO, A. S. &MOLONY, V. (1971). The anatomy of respiration. In Physiology and Biochemistry of the Domestic Fowl, Vol. 1, (eds D. J. Bell & B. M. Freeman), p New York: Academic Press. PAYNE, D. C. (1960). Observations on the functional anatomy of the lungs and air sacs of Gallus domesticus. Ph.D. thesis, University of Bristol, U.K. ROMUN, C. & LOKHORST, W. (1961). Climate and poultry. Heat regulation in the fowl. Tijaschr. Diergeneesk. 86, SCHEID, P., GRATZ, R. K., POWELL, F. L. & FEDDE, M. R. (1978). Ventilatory response to CO 2 in birds. II. Contribution by intrapulmonary CO 2 receptors. Respir. Physiol. 35,
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