OBSERVATIONS

ON THE SlTES OF RESPIRATORY

IN THE FOWL DURING

B. MENUAM’

Abstract.

The rate of respiratory

flow method, assessed

and the relative

by cannulating

Birds were exposed 41 to 44

C. Overall.

divisions,

was by about

water

was investigated

of the surfaces

and by recording

in domestic

of the upper

the temperatures

in RWL

from

the whole

at rectal

tract.

I. I, 1.O and 0.3 mg (g. hr. ,C)- ‘. respectively.

fowls by the open-

and lower respiratory at the potential

to Ta from 20 to 40 ‘C and RWL examined the increase

EVAPORATION

PANTING

and S. A. RICHARDS

loss (RWL)

importance

the trachea

THERMAL

and

temperatures

from

tract

evaporating

(Tre) from

the upper

and

There was a rapid increase

in RWL from the whole and from the upper tract at Tre 41.542.5

C, but no comparable

was sites. lower

in ii and

change

from

the lower tract. Temperatures

significantly

nasal and buccal

cavities.

It was concluded

below Ta and Tre (both

43 ‘C) were detected

in the trachea

and in the

but not in the air sacs.

that respiratory

that the air sacs are unlikely

evaporation

occurs

mainly

from the upper tract during

panting

and

to be involved. Air sacs

Thermal

Fowl

Upper

Surface

temperatures

panting respiratory

tract

Water loss

Birds are characteristically panting animals and when exposed to a hot environment a large proportion of the metabolic heat is lost by means of respiratory evaporation. Whereas in the panting mammal this water loss occurs from the surfaces of the upper respiratory tract (Richards, 1970a), the peculiar structure of the avian system raises the possibility that the air sacs may represent additional surfaces which could play an important role in evaporative cooling. This hypothesis has interested avian physiologists for many years (Bert, 1870; Soum, 1896; Victorow, 1909) and has received a good deal of support in recent times, notably by Zeuthen (1942), Salt and Zeuthen (1960) and Salt (1964), but there have been few attempts to examine the problem experimentally. The idea of a function for the air sacs in evaporation has been influenced by the recent demonstration that the flow of gases through the avian lung is ‘uniAccepted

for

puhlicatiotz

’ Present address:

3 June 1975.

Faculty

of Agriculture.

Chiang

Mai University, 39

Chiang

Mai. Thailand.

40

B. MENUAM AND S. A. RICHARDS

lung

vb

db

I

I

lung

(b)

as

-

1. Schematic

diagrams

gas flow. (a) Traditional volumes

of the parts, mesobronchus;

directional’,

neo-

pulmo

pulmo

inspiration expiration

L&g [7 cl Pb__

)

-_--:-

‘_w_iii_

_______ j@ iI

_______

/

Fig.

palaeo-

-

-------

mb

of the avian

respiratory

__,

system,

with arrows

depicting

the direction

of

type, generalized. as given

by

(b) The system of the domestic fowl illustrating the relative air sacs; db, dorsobronchL mb, Duncker (1972). as, anterior

pb, parabronchi;

from caudal

ps, posterior

to cranial

air sacs; t, trachea;

in both phases

vb. ventrobronchi.

of the respiratory

cycle (Bretz

and Schmidt-Nielsen, 1970; Bouverot and Dejours, 1971). Inspired air passes directly by way of the mesobronchi to the posterior air sacs without traversing the gasexchange surfaces. while gas entering the anterior sacs does so from the parenchymal parabronchi and would therefore presumably be saturated with water vapour at the deep body temperature. Since this flow pattern is unchanged during thermal panting (Bretz and Schmidt-Nielsen, 1971; Scheid and Piiper, 1971) the physical conditions within the anterior sacs would appear to preclude the likelihood of significant evaporation there. But if we accept the traditional type of schematic diagram of the avian lung shown in fig. la, it still seems feasible that evaporation might occur from the posterior sacs. This possibility has been examined in the present experiments by partitioning the evaporative water losses from the upper and lower portions of the respiratory tract, and by measuring the temperatures on the potential evaporating surfaces. Methods The experiments

were performed

on 14 domestic

fowls (Babcock

390 hybrids)

aged

SITES OF RESPIRATORY

from 10 to 16 months

and weighing

WATER

between

41

LOSS IN THE FOWL

2.10 and 2.65 kg. Acute

procedures

were carried out under phenobarbitone sodium aneasthesia (150 rng. kg-’ intramuscularly) but in the majority of cases the birds were conscious, 2% lignocaine hydrochloride being given locally for superficial surgery. Birds of this breed are exceptionally

docile and accepted

MEASUREMENT

OF RESPIRATORY

the experimental

WATER

LOSS

conditions

without

distress.

(RWL)

The rate of RWL (transfer rate of water) from the whole respiratory tract (tiRnLo) was determined in an open-flow system sited in a climatic chamber. The bird stood in a steel box (0.33 x 0.30 x 0.18 m; volume 17.8 L) with its head protruding through an opening in the front wall into a perspex head compartment (0.18 x 0.13 x 0.18 m; 4.2 L). A rubber dam collar prevented air flow between the two compartments and a rigid pillory secured the head. The two compartments were clamped together onto an airtight gasket. To measure &lR,,o the head compartment was ventilated at a constant rate of 13 L ArPs.min-’ by means of a diaphragm pump (Capex I, Charles Austin); flow rate was monitored with a rotameter (10X, GEC-Elliot) previously calibrated against a wet gas meter (type B, Parkinson & Cowan). The incoming air was dried by passing it through a vertical column of anhydrous calcium chloride, and the weight increment of a second column on the outlet side was determined during a precisely timed interval (usually 10 min) to an accuracy of 0.1 mg. Duplicate measurements were made at each level of ambient temperature (Ta) and blank determinations were carried out before and after each experiment to correct for incomplete drying of the air. Partitioning of the RWL from the upper and lower portions of the respiratory tract was performed by intubation with a tracheal cannula. (length 110 mm, external diameter 4.5 mm) was inserted

A thin-walled P.V.C. tube into the trachea at the mid

position (70 mm below the glottis); space was approximately equal cannula was stitched to the trachea evaporation from the surfaces

that the total tracheal dead bird (about 4.5 cm3). The When estimating the rate of the point of cannulation

measurements to that in the and the wound of the tract

showed intact closed. above

(tihi,,,) ~ together with a fraction from the skin of the head and part of the neck the bird’s head was inside the head compartment but the cannula passed out through a sealed aperture into the climatic chamber. For the estimation of evaporation from parts of the tract below the point of cannulation (tiloH20), the bird’s head was outside the head compartment but the cannula was inserted inside. The ambient temperature was varied over the range 20-40 “C and monitored continuously, to the nearest 0.1 “C, on a 6-channel potentiometric recorder (Z94B, Elektrolaboratoriet). The core body temperature of the bird (Tre) was recorded to an accuracy of 0.05 “C from a point about 60 mm inside the rectum using a flexible probe of 1.2 mm diameter (type RM6, Ellab). The recorder scanned each channel at intervals of 12 sec. The relative humidity (r.h.), and hence the water vapour pressure (Pa,,,) in the

42

B. MENUAM

air breathed

by the birds,

(1966): percent

AND S. A. RICHARDS

was estimated

r.h. = 100 tiRHLojiiair

from

the formula

of Lasiewski

x d, where ‘?air is the flow rate through

head compartment and d is the density of saturated steam at Ta. The bird was first exposed for more than 1 hr in the laboratory

(mean

et al. the tem-

perature, 20 C; mean barometric pressure, 101 kPa or 758 torr) and then placed in the box with the head compartment in position. A further 30 min then passed while dried air was drawn through the head compartment to remove moisture from ri/rlo Hzo) and to allow the system to reach the feathers (not applicable in measuring equilibrium. A series of control measurements was then taken before the temperature in the climatic chamber was raised. and measurements of RWL were then made at various levels of Tre. When Tre was not stable during a measurement period, the estimated mean value was used in expressing the results. Experiments were terminated before Tre reached 44.0 ‘C in severe conditions, and otherwise within 4 hr. RESPIRATORY

MINUTE

VOLUME

(ii)

The respiratory responses of three of the intact birds were examined during simultaneous measurement of RWL. The body compartment was sealed and used as a whole-body plethysmograph, pressure changes being detected with a differential transducer (UPl, Pye-Ether) and displayed on a recorder (M2. Devices). Tidal volume (VT) varied from about 5 to 30 cm3 and the system was calibrated with an oscillating syringe while an inert body of approximately equal volume to the bird was enclosed inside. \i was expressed as the product of VT and respiratory frequency (f). Observations on one of the birds after cannulation produced no evidence that this procedure itself significantly influenced the respiratory pattern. MEASUREMENT

A separate

OF TEMPERATURES

series of experiments

ON THE RESPIRATORY

was conducted

SURFACES

in order to measure

the temperatures

on the respiratory and pharyngeal surfaces of intact birds during heat-induced panting. The measurements were made by attaching or inserting flexible thermocouple probes (0.6 mm diameter) onto the various surfaces and by recording the temperatures ( &-0.05 C) simultaneously with Tre and Ta (in the climatic chamber). In these experiments the channels were scanned at intervals of 6 sec. Temperatures from the pharynx and upper respiratory tract (parts above the point of cannulation in the previous experiments) were recorded in conscious birds standing in a wooden frame, but those from the lower tract (below the point of previous cannulation) could be recorded only from anaesthetized preparations lying on their sides. Observations were made on a single bird to gain some idea of the effects of anaesthesia and posture on the level of the surface temperatures during panting. Measurements were made from the following sites: (i) at the anterior extremity of the buccal cavity; (ii) at the posterior extremity of the buccal cavity beneath the tongue; (iii) 15 mm inside the nasal cavity; (iv) on the inside of the trachea about 20 mm below the glottis; (v) 60 mm below the glottis; (vi) 130 mm below the glottis; and on the inside of the wall of (vii) the anterior thoracic, (viii) the

SITES OF RESPIRATORY WATER LOSS IN THE FOWL

43

posterior thoracic and (ix) the abdominal air sacs. The air-sac probes were passed through hypodermic needles following the procedure of King and Moloney (1971) and their exact locations were verified by post-mortem dissection. Two miniature thermistor probes (511X, Yellow Springs), which provided an unbroken record of temperature (kO.05 “C), were used in donjunction with a multichannel recorder (M8, Devices), specifically to detect any changes in the surface temperatures during the respiratory cycle. The time constant of the thermistors (200 msec in water) was sufficiently short to allow them to follow the most rapid frequencies achieved in the panting birds (about 250 min-‘) when tested by measuring the difference in temperature between inspired and expired air (about 2 ‘C at Ta 40 “C) at the external nares. In these experiments f was recorded via a balloon-type pneumograph and pressure transducer. Statistical analyses were carried out using the appropriate Student ‘t’ tests and the slopes of the regression lines or regression coefficients were compared using analagous procedures for samples of unequal variances. Results In the five birds used in the experiments that measured ri/lRHzOrTre started to rise at Ta 28 “C (mean Pa,,*o 0.5 kPa or 4 torr) and an increase of Ta to 40 “C

44

’

43

l

c&J *42-

_-0

l

l

.

**

41 =

40 20

24

28

32

36

40

Ta “C I Fig. 2. Rectal temperature (Tre) in the five fowls used for determination of respiratory water loss. as a function of ambient temperature (Ta). Points represent the mean of duplicate measurements on each bird taken during the second hour’s exposure. Regression line for Ta > 28 ‘C: y=36.36+0.19 x; r = 0.936. P < 0.001.

(1.8 kPa, 14 torr) resulted in a rise of Tre from 41.4kO.l to 43.8t_0.1 “C. The overall relationship is presented in fig. 2. Open-mouthed panting, with f in excess of 100 min- 1 began in all of the birds at Tre approximately 41.5 “C.

44

B. MENUAM AND S. A. RICHARDS

Total respiratory evaporation

Figure 3a summarizes the relationship between I\l/IRn20and Tre and table 1 gives the mean results under resting conditions and during severe panting caused by a hyperthermia of 242.7 “C. The maximum change in &JR,,, achieved under the present conditions was 3.6-fold, but it was clear that I\jIRHzoincreased most rapidly in the approximate Tre range of 41.542.5 “C. At higher levels of Tre the rate of increase was slower.

4.0 c

I

T

2

9m

*

3.0 -

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3E

-. * cr’ 2.0 . .E

_/ .

.

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-

.

. .

*

* * .:

1.0 -

h

’

I

4.0’ :. ‘i 2

. .

$2.0-

.

.j._:’

*

.

.

. .

.*

* .

.-I .s

.

3.0 -

.* .

/ 1.0 . . .: . *. . .. ..* /

.

.

.*

’

I

-b /

C

Fig. 3. The rate of respiratory

44.0

43.0

42.0

41.0

water loss as a function

of rectal temperature

(Tre). (a) Water loss from the

whole respiratory tract (tiRH20). Regression lines: y= -71.52+1.77x; r=0.713, P < 0.001 (Tre 41.5425 “C)and y = - 27.01 f0.7 1x;r =0.677, P < 0.01 (Tre > 42.5 “C). Regression coefficients significantly different,

P < 0.001. (b) From

the upper

tract

only

(tihi,,,).

Regression

lines:

y= -65.96+

1.62x; r=0.585,

P42.5 “C). Regression coeffkients significantly different, P < 0.001. (c) From the lower tract only (kilo,,,). Regression line: y= - 11.03 +0.29x; r =0.673, P < 0.001. Regression coefficients for separate ranges of Tre not significantly different.

SITES OF RESPIRATORY WATER LOSS IN THE FOWL

45

The difference between the slopes of the two regression lines in fig. 3a for the ranges Tre 41.5-42.5 “C and Tre 42.5 “C is highly significant (P < 0.001). EVAPORATION FROM THE UPPER RESPIRATORY TRACT

Figure 3b and table 1 summarize the relationship between tihi,,, and Tre in the same five birds as used in the previous experiments. Panting again began at . . 41.441.5 “Cand MhtHzo then increased markedly until about Tre 42.5 “C, after which

TABLE I The rate of water loss from the whole respiratory tract, and from the upper and lower portions of the tract, at rest and near the peak of the panting response to heat. Mean values +S.E. n=number of observations on the same five birds used throughout. Site

Whole tract

Normal breathing ____-I_____

Maximum panting

Tre

Rate of water loss

Tre

Rate of water loss

tact

(mg (g.hr-‘1

(“C)

(mg (g-hr-‘1

41.4 (kO.1) n=15

($3)

43.75 (kO.1) n=15

4.3 (f0.1)

43.9 (,O.I) n=lO

3.2 (kO.1)

Upper tract

41.15 (kO.1) n=lO

0.5 (iO.04)

Lower tract

41.1 (f0.03) n=9

0.8 (+o.l) n=8

the rate of increase declined. The maximum change in Iwhi,,, over the resting level averaged 6.4-fold. The difference between the two regression coefficients in fig. 3b is again highly significant (P < 0.001). EVA~~TION

FROM THE LOWER SPIDERY

TRACT

The relationship between I&o,,, and Tre in the same live birds is presented in fig. 3c and table 1. In these experiments the maximum increase in P&o,,, averaged 2.1-fold. There was no consistent change in P&o,,, at any particular level of Tre, although the panting response was again initiated at about Tre 41.5 “C. Separate regression lines were fitted to the data for various ranges of Tre, but in no case was there a significant difference between the slopes. It is for this reason that only the line best fitting the data for the whole range of Tre is given in fig. 3c.

B. MENUAM AND S. A. RICHARDS

46 RESPIRATORY

MINUTE VOLUME

The mean values of the observations made are summarized in fig. 4. The most rapid increase in ‘? occurred in the approximate range of Tre 41542.5 C (fig. 4a), amounting

to a change

of 4.3-fold.

Thereafter

the rise was somewhat

slower,

the

maximum overall change being 5.6-fold for a rise in Tre of 2.4 “C. Despite the limited date, regression analysis showed that the slope for the range of Tre 41.3342.3 “C was significantly different from that for Tre 42.543.7 “C (P < 0.05). There was a linear relationship in these experiments between ii and QR,,,,, (fig. 4b).

42

43 “c

Tre

F;rRH,O/mdg.hf

I

Fig. 4. Respiratory

minute

loss from the whole Regression r =0.929,

volume (\i) as a function

respiratory

tract

lines: (a) y= -61.49+ P < 0.05 (Tre

(&lR,,,).

1.51x; r=0.964,

42.5 -43.7

“C);

OF THE RESPIRATORY

of (a) rectal temperature

Points

represent

PcO.05

regression

y= -0.34+0.82x; TEMPERATURES

3.0

2.0

44

(Tre 41.3=42.3

coeffkients r=0.987,

and (b) the rate of water

the mean

of 2 or 3 measurements. ‘C) and y= -23.82+0.62x;

significantly

different.

P < 0.05. (b)

P