Respiratory Mechanics of Sound Production in Chickens and Geese

Home , Goose, Poultry

J. exp. Bio/. (1978), T*> 229-250 With iSfigurei Printed in Great Britain RESPIRATORY MECHANICS OF SOUND PRODUCTION IN CHICKENS AND GEESE

BY J. H. BRACKENBURY Sub-Department of Veterinary Anatomy, Tennis Court Road, Cambridge, CBz iQS

(Received 21 June 1977)

SUMMARY 1. Air flow, air sac pressure and tracheal pressure were measured in chickens and geese during a variety of different vocal and non-vocal activities. 1 2. Air flow and air sac pressure may rise to 500 ml s" and 60 cmH2O (6 x io3 N/m8) respectively during a crow in the chicken. During a sequence -1 of honks in the goose the corresponding values are 650 ml s and 25 cmH2O (2-5 x 1 o3 N/m2) respectively. 3. The volume of air delivered through the respiratory system during a single crow is more than 400 ml, almost equivalent to the total volume of the lung air sac system. 4. The efficiency of the chicken syrinx as a sound producing instrument, estimated by comparing the sound energy radiated with the energy con- sumed in the expulsion of air during a crow, appears to be less than 2 %. 5. Cutting the paired sternotrachealis muscles had no effect on vocalization. 6. The measured rates of clucking, cheeping and honking in adult chickens, young chicks and adult geese respectively are comparable to the characteristic rates of panting in these animals. This points to a similarity in the nature of the respiratory movements involved in each case. 7. Simultaneous measurement of tracheal flow and pressure indicate that the glottis is capable of controlling air flow over a wide range of values in the presence of high pressures. During defaecation the valve is closed whilst during coughing it is wide open.

INTRODUCTION Gaunt, Stein & Gaunt (1973) and Gaunt, Gaunt & Hector (1976) have compared the mechanical events associated with sound production in a songbird, the starling Sturnus vulgaris, and the chicken Gallus domesticus. They found marked differences between the two types in their ability to regulate respiratory air flow during vocalization. In both cases there were very large increases in air sac pressure but the starling was able to restrict both the air flow rate and the total amount of air used. This was presumably made possible by means of a valvular constriction of the syrinx brought about by the action of the intrinsic syringeal muscles. Gaunt et al. were unable to record air flowdirectl y in the chicken but adduced from recordings of tracheal pressure that the syringeal valve was much less effective in this species. This is probably associated with the lack of intrinsic muscles. On the other hand there was evidence Present address: Department of Biology, University of Salford, Salford, Manchester Ms 4WT. 230 J. H. BRACKENBURY of a very substantial increase in flow resistance during a form of vocalization which they called ' wailing'. This was attributed to the action of the extrinsic muscles of the syrinx, notably the sternotrachealis muscles. The supposed mechanism of these muscles had first been described by Miskimen (1951). By their action, the drum of the syrinx was said to be drawn caudally, which led to an inward bowing of the tympaniform membranes and a narrowing of the syringed lumen. Gaunt et al. also considered whether the movements of the body involved in clucking in chickens represented expiratory pulsations or true in/out breaths. Calder (1970) had shown that trilling in the canary Serinus canaria was accompanied by rapid vibrations of the sternum which he described as 'mini-breaths'. Gaunt et al. doubted this interpretation, believing the movements here, as well as in the chicken, to be expiratory pulsations. The problem, which remains unsolved, has an important bearing on the ability of certain birds to breathe during long periods of continuous high frequency singing. Brackenbury (1977) has discussed the matter in relation to the production of continuous trains of pulsed sounds in the grasshopper warbler Locustella naevia. The main purpose of the present paper is to investigate the relationship between changes in pressure and flow in the lung air sac system of chickens and geese during vocalization, by direct recording. This will include a quantitative assessment of the efficiency of the syrinx as a sound producing organ. In addition, the nature of the respiratory drive involved in pulsed sound production will be studied by comparing mechanical events during clucking and panting. Finally, direct evidence will be presented from a variety of vocal and non-vocal activities, showing that the glottis, as well as the syrinx, is capable of acting as a variable and efficient valve in the respiratory system.

METHODS All recordings were made from standing birds with chronically implanted cannulae and air flow meters. Before surgery birds were anaesthetized with a mixture of equal proportions of 30 % ethyl carbamate (Urethane) and sodium pentobarbitone (Nem- butal) introduced steadily into the wing vein. Chickens (B.W. 2'5-3-3 kg) required 3-4 ml, geese approximately twice this amount. The interdavicular air sac was can- nulated at the base of the neck on the left side in order to avoid the crop. The tracheal flow meter (Fig. 1) is designed on the Pitot principle and is similar to the instrument used by the author for measuring intrapulmonary air flow (Brackenbury, 19726). It can be calibrated in situ in the standing animal (Fig. 2) or post mortem after removal of the trachea. It is introduced into the trachea through two small holes cut in the cartilage and involves minimal obstruction of the flow of air and mucus. Apart from immediate post-operative effects, its presence caused no apparent distress to the animals. Tracheal pressure could be monitored by leading off one arm of the instrument simultaneously to a second manometer. Pressures from both the flow meter and the cannulae were measured using Grass PT5 manometers feeding into a Grass Model 7 polygraph. The frequency response of the pressure recording/polygraph system was mainly limited by the pen oscillograph which was flat from d.c. to 35 Hz and down 3 dB at 75 Hz. A Briiel and Kjaer 4161 microphone connected to a Nagra IV SJS recorder was used for sound recording. Sound signals were led into a Grass 7P3 integratoi Sound production in chickens and geese 231

1 ' i * L iiit ii

Fig. 1. Tracheal flow meter. The device is constructed on the Pitot principle. It consists of two tubes fixed to a half cylinder of plastic which, together with a small sleeve of tubing (i), holds the device in place in the trachea (J1). Air flow (V) produces a pressure difference between the two holes Pj and P, and this is measured by a differential manometer. which produced at the output to the pen recorder a voltage proportional to the average sound pressure level. The frequency response of the sound recording system was flat from 30 Hz to 15 KHz ± 1 dB at a tape speed of "j\ in/s.

RESULTS Chicken Crowing The sound recording in Fig. 3 shows the main features of the normal crow in an unoperated animal. Three introductory notes (marked by arrows) occurring at a rate of 4-5 Hz, lead into a prolonged phase in which the average sound pressure level falls from a maximum of approximately 100 dB measured in front of the animal, to zero. Measured from behind the peak sound level is approximately 95 dB. All sound pressure values are given with reference to 0-0002 dyne/cm2 at a distance of 1 m. The changes in air sac pressure during a crow are shown in Fig. 4. Similar recordings have been presented by Brackenbury (1972 a) and Gaunt et al. (1976). The first half of Fig. 4 shows a sequence of normal breaths leading up to the crow. In the second half the chart speed was increased to show the details of the crow. The main features, including the introductory notes and the prolonged phase, are reflected in the pressure changes. The maximum pressure is slightly less than 60 cmHaO (6x io3 N/m2). The crow takes place during an exceptionally strenuous expiration; Ifis the figure shows, it is not preceded but is followed by a deep inspiration. At the 232 J. H. BRACKENBURY

166 . [Trachea! flowm i J^

Fig. a. Tracheal flow meter. Calibration in situ. This makes use of the technique of artificially ventilating the lung air sac system by means of a measured stream of air led into the interdavicular air sac and out of the mouth. Upper trace: flow rate was measured by a Fleisch pneumotachograph. Lower traces: air sac pressure and flow meter differential. Respiratory movements are indicated before and after the period of calibration, but are inhibited as soon as the air stream is switched on. Time in seconds.

I•e 95

Fig. 3. Chicken. Crowing. Sound recording from normal unoperated animal. The arrows indicate the three typical introductory notes. mrt mi Ti

I s Fig. 4. Chicken. Crowing. Interclavicular air sac pressure. The chart speed was increased from the first half of the recording, showing a sequence of normal breaths, to the second half showing the crow. 234 J. H. BRACKENBURY

60 -i

40-

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gj _ Sound pressure fevell

,§ t — =z § = ^p

e 85 HI 0Q •a

Fig. 5. Chicken. Crowing. Air sac pressure, tracheal pressure and average sound pressure level. Time in seconds. end of the crow the pressure falls dramatically from approximately +4ocmHliO 3 1 a (4 x io N/m ) to approximately -7 cmH20 (7 x io* N/m ). The latter value may be compared to the minimum inspiratory pressure during a normal breath, which is -(1-1-5) cmHjO (ro-i-5 x io2 N/ma). It is noticeable that the area beneath the expiratory wave is many times greater than that enclosed by the inspiratory wave. Since the difference in tidal volume between the two phases cannot be great, the discrepancy must largely reflect an increase in respiratory airway resistance during crowing. Fig. 5. shows simultaneous recordings of air sac pressure, tracheal pressure and 3 2 sound pressure level. The maximum values are 60 cmHaO (6 x io N/m ), 12 cmH20 (i-2X io3 N/ma) and 97 dB respectively. The differences in air sac and tracheal pressure are indicative of the loss in pressure head during air flow through the syrinx. Fig. 6 shows recordings from another individual of tracheal pressure, tracheal air Sound production in chickens and geese 235 -1 l.i-l I 14 \ rvt

-20 I It! ft / ./-•/-< //

Fig. 6. Chicken. Crowing. Tracheal flow, tracheal pressure and average sound pressure level. flow and sound pressure level. The second of the introductory notes is suppressed, though this phenomenon is not unusual (Gaunt et al. 1976). Maximum values are 3 a 1 II cmHgO (I-I x io N/m ), 500 ml s- and 97 dB respectively. All three waveforms are similar showing that sound pressure level is proportional to both pressure and flow rate. The maximum expiratory tidal volume estimated by an approximate integration of the flow curve lies between 400 and 500 ml. These various maxima may be compared with the corresponding values during a normal expiration: 0-5 cmH,0 (0-5 x io* N/m*), 30-40 ml s"1 and 35 ml respectively. Thus these parameters increase by 15-100 x during crowing.

Energy relations during crowing A method for computing the efficiency of the process of converting fluid energy into sound energy during crowing is shown in Fig. 7. This is done for only one particular instant of the crow, namely the point during the declining phase at which the maximum of pressure, flow and sound pressure level coincide (Fig. 6). At this point it is required to compare the rate of fluid energy dissipation during the flow of air through respiratory airways, with the rate of sound energy emission. This ratio will provide 236 J. H. BRACKENBURY

Sound power radiation (Watts) = (2v R2)x |O""'°-16> Fluid power dissipation (Watts) = P(dyne cm-')x K(cm3s-')x 10"7 Efficiency (%)

= 1 : X 100 \ PxVx\0-J J

Syrinx P=dyne cm"2 (1 dynecm-2=l0-' N/m2) Abdominal air sac Interclavicular air sac

Fig. 7. Method for computing the efficiency of the conversion of fluid energy into sound energy during vocalization. Although in general there are two paired thoracic air sacs in birds, the anterior and the posterior, in songbirds the former pair is combined with the interclavicular to make a single unpaired sac, as represented here. an estimate of efficiency. The instantaneous rate of fluid energy dissipation is equivalent to the product of the air sac pressure and the volume flow rate. From Fig. 6 3 2 3 1 these values may be taken as 50 cmH80 (5 x io N/m ) and 450 cm s" (4-5 x io"3 m3/s) respectively. The product is 2-25 Nm/s, or 2-25 W. This figure represents approximately 2000 x the maximum fluid work rate during a normal expiration 1 2 (maximum flow rate 25 ml s" ; maximum air sac pressure 0-5 cmH20 = 0-5 x io N/m8). In order to calculate the rate of sound energy emission it is necessary to specify the nature of the sound pressure field in the vicinity of the bird's head. In similar calculations on human speech it has been assumed that the sound radiates across a hemisphere in front of the head (Sacia, 1925). If this is assumed for the bird (Fig. 7) the area over which sound radiates at a distance of 1 m from the mouth is 2 x n x ioo2 ~ 6 x 10* cm2. A sound pressure level of 97 dB at this distance is equivalent to an energy flux of io~* 3 W. cm"2. The total energy flux is therefore io~*3 x 6 x io1 W = 003 W. The energy conversion efficiency is therefore 0-03/2-25 x 100% = 1-3 %.

Clucking and cheeping Both clucking in the adult and cheeping in the chick are produced by rapid pulsatile movements of the body wall. They normally occur in rapid succession during single expirations (Fig. 8). The maximum air sac pressure achieved during clucking varies Sound production in chickens and geese 237

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2 o

Fig. a. Chicken. Panting, (a) Coelomic pressure changes (uncalibrated) in 15-day-old chick, (ft) Air sac pressure in adult, (c) Air sac pressure during combined sequences of clucking (arrows) and panting. Time in seconds. Sound production in chickens and geese 239

Fig. 10. Chicken. Clucking. Following resection of the sternotrachealis muscles. 1 Time in seconds.

3 a with intensity of effort from 5 to 25 cmH2O (0-5-2-5 x io N/m ) (Fig. 8a). The rate varies somewhat too but is normally 4-5 Hz. The rate of cheeping depends on the age and size of the individual; for a 15-day-old chick weighing 120 g it is 7-8 Hz (Fig. 8c). Each cluck is produced by a rapid spurt of expiratory air flow (Fig. 8b). The total volume of air delivered during a sequence is evidently not very large to judge from the size of the following inspiration.

Comparison of clucking, cheeping and panting Panting, consisting of rapid, shallow breathing movements, is the normal response to hyperthermia in birds. It can be induced experimentally by blowing a stream of warm air over the body. The typical breathing pattern which results consists of a series of alternating periods of panting and more measured breathing (Fig. ga, b). The rate and amplitude of body movements vary somewhat with the intensity of panting; maximum rates are 4-5 Hz in the adult and 6-7 Hz in the chick; they are thus the same as for clucking and cheeping. The similarity between panting and clucking movements is even more evident whenever they occur together in the same sequence (Fig. gc).

Effects of severing the sternotrachealis muscles This operation, which can be conveniently performed during a routine cannulation of the interclavicular air sac, appears to have little effect on sound production. In their essential features, clucking (Fig. 10) and crowing remain unchanged. Fig. 10 also demonstrates that clucking may sometimes be extended well beyond the duration of a single breath.

Growling This is a form of unmodulated vocalization first described by Gaunt et al. (1976). Fig. 11 (a) shows a comparison of the changes in tracheal pressure and flow during a growl and a crow. Although the pressure changes are comparable the flow changes differ by a factor of approximately 2-5. Thus the airway resistance cranial to the syrinx is approximately 2-5 times greater during the growl than during the crow. The difference must be related to the changing size of the glottis. In Fig. 11 (4) an example a growl is shown in which the rise in pressure is accompanied by virtually no rise air flow rate. It must be assumed in this case that the glottis is almost closed. J. H. BRACKENBURY

i__i4 Tracheal pressure t-f j { j / / /'"/- jl j -j | /

Fig. 11. Chicken. Growling, (a) Comparison of tracheal pressure and flow during growl (first arrow) and crow (second arrow). (6) Tracheal pressure and flow during succession of growls (arrows).

Defaecation and preening During both defaecation and vigorous preening, the latter of which may involve fluffing of the feathers and shaking of the body, the glottis is closed. This is shown by the very large increases in tracheal pressure (Fig. 12) which are not accompanied by increases in tracheal flow.

Goose Normal breathing The normal respiratory rate is 7-8 cpm, the expiratory phase being longer and shallower than the inspiratory (Fig. 13). During inspiration, maximum air flow and -1 a negative air sac pressure are 100 ml s and I-O-I^ cmHaO (I-O-I^ x io N/m5i respectively (Fig. 13). During expiration, the corresponding values are 30-35 ml s Sound production in chickens and geese 241

Fig. ia. Chicken. Preening and defaecation. Tracheal pressure and flow during preening (small arrows) and defaecation (large arrow).

a a and 0-3-0-5 cmH2O (0-3-0-5 x io N/m ) respectively. The tidal volume is 100- 140 ml.

Honking Honking frequently occurs in the form of quick successions of sound accompanied by expiratory spurts of air sac pressure and air flow (Fig. 14). In this way it resembles clucking in the chicken. The repetition rate of these sounds is 4-5 Hz. Maximum air 3 s sac pressure and air flow vary from 20-30 cmH2O (2-0-3-0 x io N/m ) and 550- 650 ml s"1 respectively. Compared to a normal expiration, these values represent increases of 40-100 and 17-20 times respectively. The increase in airway resistance is therefore 2-6 times.

Hissing This is not a vocalization in the strict sense. It is produced during long expirations, sometimes lasting for many seconds. Each hiss is preceded by a deep inspiration (Fig. 15 a). The maximum air sac pressure and air flow rate during hissing (10 cmH2O and 200 ml s-1 respectively) are intermediate between those of normal breathing and vocalization. Changes in tracheal pressure are almost identical to the changes in air sac pressure indicating that the syringeal resistance is small. A comparison of maximum pressure and flow excursions during inspiration and expiration shows that the expiratory resistance is approximately 3-4 times as great as the inspiratory. This is com- patible with the view that hissing is caused by a stream of expiratory air escaping from the constricted glottis. It may be noted that following a prolonged session of hissing, a period of half a pninute or more may elapse before the next breath (Fig. 15*). This delay indicates to to

dd s.

-60-

-90-^i

Fig. 13. Goose. Normal breathing. Air sac pressure and tracfaeal flow. Time in seconds. Sound production in chickens and geese 243 (a) '<

Fig. 14. Goose. Honking. Air sac pressure and trachea] flow, (a) Single burst. (6) Three succes- sive bunts (marked by arrows). Time in seconds.

the degree to which the lung air sac system has been aerated by the very large tidal volumes involved in hissing.

Coughing and defaecation

Coughing and defaecation are accompanied by very large (20-30 cmH20) rises in pir sac pressure (Fig. 16a, b), but whilst air flow may rise to 800 ml s-1 during a cough, J. H. BRACKENBURY

I Tracheal Pressure

wmmm iiMfpE _; u Tracheal flowil. I \ \ .

ml/8

Fig. 15. Goose. Hissing, (a) Tracheal pressure, air sac pressure and tracheal flow. Arrows indicate periods of hissing. (6) Intermission of breathing (between arrows) following prolonged session of hissing. Time in seconds. it virtually ceases during defaecation. Fig. i6(a) shows that the changes in air sac and tracheal pressure are identical, and that therefore the syringeal resistance is low. It may be concluded that the glottis is closed during defaecation and fully open during coughing.

Panting The rate of panting is 3-4 Hz, comparable to the rate of honking (Fig. 17). Air 2 a sac pressure varies from ±1 cmH2O (± rox io N/m ) and air flow from ±400 ml s"1. Sound production in chickens and geese 245 (<*) 30-

cmH,O

Fig. 16. Goose. Coughing and defaecation. (a) Tracheal pressure, air sac pressure and tracheal flow during hissing (small arrows) and defaecation (large arrows). (6) Tracheal pressure and flow during coughing. Time in seconds. 246 J. H. BRACKENBURY

Fig. 17. Goose. Panting. Air sac pressure and tracheal flow. Time in seconds.

DISCUSSION Pressure/flow relations The very large increase in air sac pressure during crowing (Figs. 4, 5) is due to an increase in air flow rate per se combined with an increase in airway resistance. Com- pared to a normal expiration the proportional increase in air sac pressure (at least 100 times) is much greater than the proportional increase in flow rate (approximately 15 times). Thus the proportional increase in airway resistance is some 6-7 times. A comparison of air sac and tracheal pressures (Fig. 5) suggests that the syrinx is. responsible for at least 80 % of the airway resistance during crowing. The balance of evidence supports the view that the increase in syringeal resistance is due to a nar rowing of the syringeal lumen concomitant with the vibration of the tympaniform membranes and brought about by a combination of active and passive factors. How- ever, it must also be borne in mind that quite apart from configurational changes in the syrinx, airway resistance in any case increases progressively and continuously with flow rate due to purely aerodynamic factors (Brackenbury, 1971 c). It is assumed here that the increase in such factors is relatively small compared to the changes in the syrinx. Miskimen's (1951) original theory explained the increase in syringeal resistance as being due to the contraction of the sternotrachealis muscles which drew the syringeal drum caudally, so allowing the tympaniform membranes to relax and bulge into the syringeal lumen, this bulging being assisted by high pressure from within the interclavicular air sac. Chamberlain et al. (1968) suggested that, once the narrowing of the lumen had begun in such a manner, a Bernouilli effect came into play which further enhanced the drawing together of the membranes, and so led to an even greater narrowing. Gaunt et al. (1976) subscribed to the theory of the action of the sternotrachealis muscles, but not to the supposed Bernouilli effect. It is clear from the result^ Sound production in chickens and geese 247

Sound

Fig. 18. Clucking and panting. Interpretation of Fig. g(c). A sequence of panting movements superimposed upon a prolonged expiration gives rise to a burst of clucks. The line T represents the threshold pressure above which sounds may be produced. of the present study however (Fig. 10), that the sternotrachealis muscles are not essential for sound production. Smith (1977) has reported the same finding in songbirds. Gaunt et al. (1976), however, have intimated forthcoming evidence that other extrinsic muscles may be involved in sound production in chickens. If it is assumed that one of the pre-conditions for the vibration of the tympaniform membranes is a sufficient velocity of air through the syrinx, this can be achieved in two ways. First, as in songbirds, by a more or less marked constriction of the syrinx which necessitates only moderate increases in volume flow rate and tidal volume. Second, as in the chicken and goose, by a large increase in both volume flow rate and tidal volume accompanied by a much less marked constriction of the syrinx. These were also the conclusions reached by Gaunt, et al. (1976). Whilst Gaunt et al. also assumed the existence of a large volume flowrat e in chickens, they doubted whether this factor alone, in the absence of active factors such as the contraction of the sternotrachealis muscles, would be sufficient to set the membranes into vibration. They endeavoured to repudiate the idea of' passive sound production' on physiological gounds, claiming that whilst it was indeed possible to produce sound experimentally by blowing air into an air sac and out of the trachea, the air sac pressures necessary in order to achieve the result were far in excess of normal physiological pressures. The author has been able to produce sound by such means at flow 1 3 2 rates above 70 ml s" and air sac pressures of 12 cmH2O (1-2 x io N/m ). The latter is larger than the minimal pressures associated with sound production (Fig. 8 a) but certainly falls within the normal range of observed values (5-25 cmH2O) during, for instance, clucking. In any case it can be shown that their argument is not a valid refutation of the passive model. For in the experimental situation which they described, an abnormally large air sac pressure would necessarily be requited in order to produce the level of air flow which is normally associated with the commencement of sound production. This results from the structure of the lung air sac system. Whilst during a normal vocalization all eight (all six in the case of songbirds) air sacs are simultan- fc discharging through the bronchial network of the lung, in the experimental 248 J. H. BRACKENBURY situation only one of these is doing so, usually the interclavicular. Consequently tins' sac alone is being made to produce a total volume flow normally shared between eight sacs, and it follows that the driving pressure must be correspondingly higher. In summary, the present study indicates a significant involvement of passive factors in the production of sound in the chicken and goose syrinx, although it certainly does not rule out an important contribution from the extrinsic muscles. The single most essential factor seems to be the achievement of a sufficiently high velocity air stream past the tympaniform membranes. This is mainly brought about by an increase in volume flow rate, possibly combined with a degree of both passive and active constriction of the syrinx. This constriction is not dependent on the sternotrachealis muscles. It is also apparent that a relationship exists between loudness and flow rate. Audible sound first appears in an experimental situation at a flow rate of about 70 ml s"1. This increases to more than 200 ml s"1 during clucking and to 500 ml s"1 during loud crowing. Honking is louder still and involves a flow rate of more than 600 ml s"1. It must, however, be said that a number of observations do not fit neatly into this hypothesis. First, as during the growl and the wail, certain types of vocalization may be associated with unexpectedly low air flow rates. Second, coughing involves a very large increase in air flow rate but it does so without provoking sound production; the same may be said of the substantial increases in flow rate during panting (Fig. 17). These discrepancies cannot be dealt with by the present study.

Tidal volume The immediate prelude to both honking (Fig. 14) and hissing (Fig. 15) in the goose is an exceptionally deep inspiration. This is not the case with crowing in the chicken (Figs. 4-6). However the volume of air exhaled during the crow is at least 10 times a normal tidal volume. Where does this air come from? From data given by Lasiewski & Calder (1971) it may be estimated that the maximum end-expiratory volume of the lung air sac system of a bird weighing 3-3 kg is about 500 ml. Therefore unless it is assumed that a substantial volume of air is accumulated on top of this volume, over a number of inspirations prior to the crow rather than in a single final inspiration, it must be concluded from the evidence that the crowing effort virtually empties the entire lung air sac system. Energy relations The method shown in Fig. 7 for calculating the efficiency of sound production is only approximate since, on the input side, it only takes into account the fluid work done in moving the air through the respiratory airways. Strictly speaking, the total input is equivalent to the energy consumption of the respiratory muscles. This includes, in addition to the fluid work, energy losses in the contracting muscle itself plus the work done in moving the viscera. Since the fluid factors are so large, however, it is assumed that the error arising from this source is small. The figure of 1 -3 % appears to be very low but in the absence of published measurements on the loudness of song in other species it is not possible to make any comparative estimate of the efficiency of, say, chicken and songbird syrinxes. Preliminary fiel measurements by the author indicate maximum sound pressure levels equivalent Sound production in chickens and geese 249 86, 87, 90 and 97 dB at 1 m in front of the bird in chaffinch, blackbird, robin and thrash respectively. Since in such relatively small birds the power resources of the respiratory apparatus are obviously only a fraction of those of a chicken, it seems clear that their syrinxes must therefore be much more efficient. This superiority in efficiency must be related to the constricting ability of the songbird syrinx which can make possible the production of a high velocity stream of air past the vibrating membranes, without necessitating large volume flow rates and tidal deliveries. Gaunt et al. (1976) estimated that flow rate and tidal volume during distress calling in the starling were only slightly greater than during excited breathing. The view may be advanced therefore, that the acquisition of intrinsic muscles by the songbird syrinx has developed as much in response to a need to produce sounds of sufficient broadcasting power, as to provide a more elaborate song repertoire, which is usually held to be the case. Whilst, as has been shown, the maximum power delivery of the respiratory muscles during a crow must be of the order of 2000 times as large as during a normal respiration, the actual value of 2-25 W is modest compared to the maximum work rate achievable by, say, the locomotory muscles. Thus it may be calculated from data by Berger & Hart (1974) that the metabolic rate during flight of a bird weighing 3-3 kg is about 120 W. This represents approximately 15 times the basal metabolic rate (Calder & King, 1974). Although of course chickens cannot fly, 120 W may be safely assumed as the maximum possible energy output of the flight muscles.

Pulsed sounds Sound modulation occurs very frequently in bird song (Stein, 1968; Greenewalt, 1968). Owing to the limitations of the human auditory system, we are capable of perceiving only the slowest of these changes, such as the various 'churrs', 'rattles', 'trills', 'twitters' and 'tremoloes' mentioned in ornithological manuals. Calder (1970) classified modulations as 'primary' or 'secondary' depending on whether they were produced by the action of the syringeal muscles or the respiratory muscles. Brackenbury (1977) has used the term 'pulse' to signify individual elements in a series of sounds which are audibly and physically separated from one another. Clucking, honking and cheeping all belong to this category. Such sounds are produced by distinct pulsations of air flow arising from the rapid pumping activity of the respiratory muscles. Gaunt et al. (1976) consider that this pumping activity takes the form of a pulsatile expiration; Calder (1970) invoked a series of true 'mini-breaths'. The evidence of the present study suggests that there is a precise relationship between the respiratory movements involved in pulsed sound production on the one hand (Figs. 8. 14) and panting on the other (Figs. 9, 17). In particular, clucking seems to result from the superposition of a series of pant-like movements, perhaps analogous to Calder's mini-breaths, upon a more or less forceful expiration (Figs. 9c, 18). It is suggested that a pulsed sound will only be produced when the level of the pressure (or flow) pulse exceeds a certain threshold (T) (Fig. 18). It is possible, therefore, that the respiratory oscillations involved in clucking, cheeping and honking, as well as Calder's mini-breaths, may all belong to a single species of movement, which in other circumstances may be employed in panting. The rate of this movement, moreover, may be governed by the resonant properties of the llvhole respiratory system (Brackenbury, 1973). It may be mentioned in the context 250 J. H. BRACKENBURY that Crawford & Kampe (1971) have shown that the rate of panting in pigeons is the same as the natural frequency of the chest.

The glottal valve The ability of the glottis to act as an air valve appears to be even more pronounced than that of the syrinx. It ranges from complete closure during defaecation and vigorous preening (Figs. 12,16) to wide dilation during coughing (Fig. 16) and includes separate degrees of closure during hissing (Fig. 15) and growling (Fig. 11). This natur- ally leads to the suggestion that the laryngeal muscles, which control the size of the glottis, could act as a source of sound modulation during vocalization, in addition to the syringeal and respiratory muscles. Although this does not appear to be the case in chickens and geese, it might be capable of explaining the very rapid (50-60 Hz) spurts of air flow (from o to 15 mis"1) observed by Berger & Hart (1968) during trilling in the evening grosbeak Hesperiphona vespertina. Future considerations on the general subject of sound modulation will thus at least have to dismiss the possibility of a role played by the larynx.

This work was supported by a grant from the Science Research Council.

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