- Email: [email protected]
Responses to cold stress in two species of australian quail, Coturnix pectoralis and Coturnix chinensis
Camp. Biorhem. Ph,siol. Vol. 91A. No. 3. pp. 543-548, 1988 Printedin Greal B&in
0
0300-9629188 $3.00 + 0.00 1988 PergamonPressplc
RESPONSES TO COLD STRESS IN TWO SPECIES OF AUSTRALIAN QUAIL, COTURNIX PECTORALIS AND CO TURNIX CHINENSIS JULIE T.
School of Biological
R.
Sciences, Flinders
ROBERTS*
(Received Abstract-l.
The responses
and R. V.
BAUDINETTE
University of South Australia, Telephone: (067) 73-2592
Bedford
Park, SA 5042, Australia.
22 March 1988)
to cold stress of two
species of Australian quail, stubble quail, Colurnix
pectoralis, and king quail, Coturnix chinensis, were assessed. 2. Body temperature (Ts), rate of oxygen consumption (V,,), heart rate (fh), respiration
rate (f,) and intensity of shivering measured by electromyographic voltage were recorded over a range of ambient temperatures of - 3-30°C. 3. Most individuals of both species were able to maintain Ts constant over this range of TA although some king quail had lowered T, at TA < 5°C. 4. Shivering intensity and V,, showed an inverse curvilinear relationship to TA and shivering was directly related to Vo,. The frequency of shivering appeared unrelated to TA 5. Heart rate (fh) and_& tended to be inversely related to TA and directly correlated with I’,,. 6. The responses of the two species were qualitatively very similar. 7. The response of stubble quail to noradrenaline suggests that non-shivering thermogenesis does not occur in this-species.
possesses histological characteristics typical of mammalian brown fat. In mammals, a thermogenic response to exogenous noradrenaline indicates the capacity for non-shivering thermogenesis. However, no thermogenic response has been demonstrated, in the avian species which have been studied, to exogenous noradrenaline (Hart, 1962; Chaffee et al., 1963; Freeman, 1966; Allen and Marley, 1967; Marley and Stephenson, 1968, 1969; Allen et al., 1969, 1970), adrenaline (Freeman, 1970a, b; Hissa and Palokangas, 1970; Palokangas and Hissa, 1971), or 5-hydroxytryptamine (Freeman, 1970a, b). In this study, simultaneous recordings of ambient temperature ( TA), body temperature (r,), respiration rate (f,), heart rate (fh), rate of oxygen consumption (V,,) and electromyographic activity of the pectoral musculature were made to investigate thermoregulatory responses of stubble quail, Coturnix pectoralis, and king quail, Coturnix chinensis, at ambient temperatures within and below thermal neutrality. The zone of thermal neutrality is 30-35°C for stubble quail and 28-35°C for king quail (Roberts and Baudinette, 1986). The responses of these closely related species of different body weights and from different habitats, to cold stress, were compared. Non-shivering thermogenesis was examined in stubble quail.
INTRODUCTION
Stubble quail are endemic to Australia and are found in some of the driest regions of the continent. The king quail is a geographic race of a pan-Asian species and occurs in wet grasslands (Blakers et al., 1984). Both species would be exposed, at some times of the year, to overnight temperatures at or below freezing. King quail have a body weight of only half that of the stubble quail. Therefore, one might expect the smaller species to have more difficulty maintaining body temperature at low ambient temperatures. The maintenance of homeothermy in birds, under conditions of cold stress, is dependent on behavioural, metabolic, insulative and cardiovascular adjustments. Heat production is augmented by the calorigenic processing of food, by exercise, shivering and, possibly, non-shivering thermogenesis. The importance of shivering to avian thermoregulation during cold stress has been investigated by a number of workers (Steen and Enger, 1957; Hart, 1962; West, 1965; West et al., 1968; Chaplin, 1976; Hohtola, 1981, 1982; Saarela and Vakkuri, 1982; Barre, 1984; Saarela et al., 1984; Marjakangas et aI., 1984; Barnas and Rautenberg, 1984; Barnas et aI., 1984). The evidence for the presence of non-shivering thermogenesis in birds is inconclusive. Brown adipose tissue, which in mammals is associated with nonshivering thermogenesis, was not found in the studies of Freeman (1967) or Johnston (1971). However, more recently, Oliphant (1983) has described, in ruffed grouse and black-capped chickadees, fat which *Present address: New England,
Department Armidale,
of Physiology, University NSW 2351, Australia.
MATERIALS AND METHODS
Quail were maintained indoors in individual cages (0.3m2) on a 12L/l2D photoperiod at ambient temperatures close to 25°C. During experiments, Ts was monitored via a chromel/alumel thermocouple (0.46 mm diameter) inserted I cm into the hindgut and read on a Comark Electronic Thermometer coupled to a chart recorder. Fine gold-plated electrodes were implanted, under local
of
543
544
JULIE T.
R.
ROBERTSand
anaesthesia, in the pectoral musculature. The pectoral electrodes were led into a Grass amplifier (Model TP5) and then to a Grass polygraph (Model 79D) and used for recording of respiration rate, heart rate and the electrical activity of the pectoral musculature. Data were obtained for eight stubble quail (mean body weight 126.1 k 4.4 g) and 12 king quail (mean body weight 49.6 + 1.7 g). Post-absorptive birds were placed inside Plexiglas chambers (0.145 m diameter; 0.1555 m high for king quail and 0.265 m high for stubble quail) in a controlled temperature room in the dark. An open-flow system was used to determine rates of oxygen consumption (I’,,). Air was drawn through large drying columns containing silica gel and into parallel animal and control chambers. The rate of flow was maintained at 0.8 l/min through a previously calibrated rotameter (Fischer and Porter). A Taylor Servomex oxygen analyser (Model OA.184 in conjunction with a servomex Ratio-Box Type 288) was used to monitor the difference in partial pressures of oxygen in sub-samples of the air streams and the output recorded on a potentiometric chart recorder. Vo, was calculated according to the following formula, and corrected to standard dry gas conditions.
where: pE is the flow rate from the chamber, Flat and FEot are the fractional oxygen contents in room and exhalent air respectively, and RQ is the respiratory quotient taken as 0.85. The birds were weighed before and after the experiment, and mass-specific rates (f’,,/m) calculated from interpolated body weights. Ambient temperature was monitored by a 30-ga copper/constantan thermocouple inserted through a sealed port in the top of the chamber and connected to a chart recorder. All thermocouples were calibrated against a NATA standard mercury-in-glass thermometer. The gas analyser was initially calibrated from changes in pressure within the analysis cell, but for daily calibrations, a mixture of 0, in N,, and pure N, were used. The controlled temperature room could be maintained only as low as 2°C and to achieve temperatures lower than this, air was cooled in a copper coil immersed in an ice-salt mixture before being introduced to the chamber. Temperatures down to -4°C could thus be maintained within 0.2% At each ambient temperature, several 10 set samples of electrical activity, within periods of steady-state oxygen consumption, were used to calculate mean heart and respiratory rates, and electromyographic activity. The humidity inside the metabolic chamber typically varied from 40-50% at TA < 0°C to =Z15% at TA= 25°C. King quail showed some tendency to become hypothermic if initially subjected to low ambient temperatures. It appeared that the handling of the animals during the installation of the electrodes and the use of topical anaesthetic led to an initial lowering of body temperature from which the birds could not recover spontaneously if immediately exposed to low ambient temperatures. Data from such birds were discarded, and for subsequent experiments with king quail, ambient temperatures were gradually reduced from levels within thermal neutrality. The time course for the experiments was between 8 and 12 hr. Six stubble quail (mean body weight 107.1 &-1.6g) were used to investigate the effect of noradrenaline on rates of oxygen consumption. Each animal was placed in a metabolism chamber and vo, determined as described previously. T, was maintained at 23.5”C, well below the zone of thermal neutrality. When a stable rate of oxygen consumption had been established, the bird was removed from the chamber, the noradrenaline in 1 ml of sterile saline was injected subcutaneously, and the animal replaced. A stable rate of oxygen consumption was then again obtained. The noradrenaline dose used was that of Heldmaier (1971, in Nell, 1979): dose (mg/kg) = 6.6 M (g)-0.4’8,a level
R. V. BAUDINETTE
previously shown to be effective in mammals. In the same six animals, the above procedure was repeated using control injections of isotonic saline. RESULTS Body temperature and rate of oxygen consumption
Body temperature in stubble quail showed little change with decreasing TA in this study. However, mean TB at TA less than or equal to 0°C (T, = 41.2”C) was significantly lower than mean Ts recorded in previous studies within the thermal neutral zone (Roberts and Baudinette, 1986). Some king quail demonstrated a decrease in TB at TA < 5°C and, as for stubble quail, the mean r, at TA less than or equal to 0°C (TB = 40.9”C) was significantly lower than previously recorded within thermal neutrality (Fig. 1). Rates of oxygen consumption showed a qualitatively similar pattern to that observed in noninstrumented birds at night (Roberts and Baudinette, 1986), but levels tended to be slightly higher at equivalent temperatures (Fig. 2). For both species, the relationship between TA and Vo, below thermal neutrality was curvilinear, with the data for stubble quail being best described by a power curve (y = 10.85x -“.42; r,,,, = 0.89) and that for king quail most closely fitting a monoexponential function (y = 9.03 e-0,03-r;rcorr= 0.94). Respiration rate
The variability in rates of breathing among individuals generally increased as TA decreased. For both species, meanf, at TA less than or equal to 0°C
k 0
A
-5
KO
I
I
I
I
5
15
25
35
AMBIENT
TEMPERATURE
(‘C)
Fig. I. The effect of ambient temperature on body temperature showing the lowering of body temperature which occurred at low ambient temperatures in some king quail. SQ is stubble quail; KQ is king quail.
545
to cold stress in Australian quail
Responses
$0” I -5
I 5
AMBIENT
1 15
0% I 25
35
o-l,
TE~J~PERATURE(~C)
2
Fig. 2. The effect of decreasing ambient temperature on oxygen consumption. The relationship was curvilinear for both species. SQ is stubble quail; KG is king quail.
(63.4 and 90.0 breaths/min for stubble and king quail, respectively) were significantly higher than their respective rates of 47.7 and 52.6 within thermal neutrality (Fig. 3). Higher metabolic rates were correlated with elevated respiration rates (Fig. 4). Shivering activity The intensity of shivering as measured by the peak-to-peak electromyographic voltage, increased markedly below 15°C (Fig. 5). The relationship between rA and the amplitude of shivering was best described by a monoexponential function in both stubble quail (y = 148.35 e-o.o7x; r,,,, = 0.84) and king quail (y = 119.18 e-“,MX; r,,,, = 0.75). Shivering activity was almost continuous at TA < 0°C becoming gradually less frequent until at TA = 10°C it occurred
,
,
,
,
,
,
,
3
4
5
8
7
9
9
OXYGEN
(
10
CONSUMPTION
( ml.02
(g.h)-l
)
Fig. 4. The relationship between breathing rate and oxygen consumption. Breathing rate tended to increase with increased oxygen consumption. SQ is stubble quail; KQ is king quail.
50-70% of the recorded time and had virtually ceased by TA = 22°C. That shivering contributes to body temperature and increased oxygen consumption in both quail species is apparent from Fig. 6. The mean frequency of shivering activity was 19/set and appeared unrelated to TA. 200
so
1 0 0
150 -I
_
100
> 2
50
2
c
i= J
,,,,
-5
5
16
25
i
5
0
0
I
I
t
I
I
-5
5
15
25
35
a 200x E 9 150-
35
KO
z v) loo-
50-
o-5
-5
5
AMBIENT
oJ,
I
I
5
15
AMBIENT
I
25
TEMPERATURE
1
35 (‘C)
Fig. 3. The effect of ambient temperature on breathing SQ is stubble quail; KQ is king quail.
rate.
15
25
TEMPERATURE
35 (‘Cl
Fig. 5. The effect of decreasing ambient temperature on shivering activity, showing the curvilinear nature of the shivering response. Shivering activity was measured as the peak-to-peak electromyographic voltage. SQ is stubble quail; KQ is king quail.
JULIE T.
546
R.
ROBERTS and
R. V. BAUDINETTE
5
,
IOOJ, 1
2
,
,
,
,
,
,
,
,
,
,
, 8
, 8
, 10
23456788
700-l
2ooJ,
I
234567 OXYGEN
I
I
8
I
a
,
IO
, 234507
,
OXYGEN
CONSUMPTION
( ml.02(g.h)-1
CONSUMPTION
(m1.02
1
Fig. 6. The effect of shivering activity on oxygen consumption, demonstrating the increase in oxygen consumption with increased shivering activity. SQ is stubble quail; KQ is king quail. Heart rate
The response of heart rate (Fig. 7) is very variable between individuals. In general, stubble quail showed a marked increase in fh with decreasing TA, and there
(g.h)_l)
Fig. 8. The relationship between heart rate and oxygen consumption. The relationship is linear for stubble quail with king quail showing more variability. SQ is stubble quail; KQ is king quail.
was some correlation betweenf, and V,, (Fig. 8). In king quail, these correlations were not as apparent (Figs 7 and 8). Both species showed elevated mean values at TA less than or equal to 0°C (350.1 and 540.9 beats/mm for stubble and king quail, respectively, compared with 225.2 and 372.2 beats/min, respectively, in thermal neutrality). Noradrenaline response
The rate of oxygen consumption ( vo2) prior to the noradrenaline injection was 2.07 + 0.05 ml O,/g/hr. Doses of noradrenaline of 0.9 mg/kg lowered V,, by 23% to 1.59 + 0.06 ml O2/g/hr. The V,, following the injections of saline alone was not significantly different from the controls at 2.15 + 0.09 ml O,/g/hr.
-5
J
-5 AMBIENT
5
15
I
I
5
15
25
I
25
TEMPERATURE
35
1 35 1°C)
Fig. 7. Changes in heart rate with decreasing ambient temperature, showing the tendency of heart rate to increase with decreasing ambient temperature. SQ is stubble quail; KQ is king quail.
DISCUSSION
Over the range of ambient temperatures employed in this study, no major change in body temperature was observed even at sub-zero temperatures, except in the case of some individual king quail. However, for both species, T, at TA less than or equal to 0°C was significantly lower than values previously recorded within thermal neutrality. It appears unlikely that either stubble or king quail undergo regular temporary hypothermia under natural conditions. In both species, the rate of oxygen consumption increases curvilinearly as T, decreases below the thermal neutral zone. Chaplin (1976) reports a similar response in the black-capped chickadee although most workers have reported a linear relationship. The transition from insulative adjustments to an increase in heat production (the lower critical temperature) seems to be abrupt in both stubble and king quail (Roberts and Baudinette, 1986).
Responses to cold stress in Australian quail Responses of avian f, to decreasing T,, below thermal neutrality, appear to vary between species.
Some, such as the burrowing owl (Coulombe, 1970) and the speckled mousebird (Bartholomew and Trost, 1970) have a relatively constant f,. In the Pekin duck (Beth et al., 1984) and the kittiwake (Brent er al., 1983)x decreased with TA from 20-22°C down to 0 and 6”C, respectively. In other species, for example hummingbirds (Hargrove and Gessaman, 1973) the cowbird (Lustick, 1970) and the pigeon (Bouverot et al., 1976), an inverse relationship exists and this pattern was also observed in stubble and king quail. The magnitude of shivering in stubble and king quail, as evidenced by the amplitude (voltage) of electromyographic activity, tended to be an inverse curvilinear function of TA and a direct linear function of Vo,. Chaplin (1976) reports a similar finding although other workers (Steen and Enger, 1957; Hart, 1962; West, 1965; West et al., 1968; Hissa and Palokangas, 1970) found that the relationship between TA and shivering activity was linear. Saarela and Vakkuri (1982) did not find a linear correlation between the intensity of shivering and Vo,, although Hohtola (1982) reports a correlation between electromyographic intensity (expressed as mean rectified value) and Vo2. The two-fold increase in the amplitude of shivering, observed in this study, has also been reported for pigeons (Steen and Enger, 1957) and the titmouse (Hissa and Palokangas, 1970). The frequency of electromyographic activity has been found to increase with decreasing TA in some species such as the pigeon (Steen and Enger, 1957) where it doubled between TA of 13°C and T, of -22-24°C and the evening grosbeak (West et al., 1968). Stubble and king quail, however, showed little variation in frequency, a phenomenon reported also for the common grackle (West et al., 1968). Hohtola (1982) found that the frequency of electromyographic activity was not related to Vo,. An inverse relationship exists between TA and fh for both stubble and king quail at ambient temperatures below thermal neutrality. A similar relationship has been observed for other avian species (Bartholomew et al., 1962; Lasiewski and Dawson, 1964; Hudson and Brush, 1964; Brush, 1965; Owen, 1969; Bartholomew and Trost, 1970; Coulombe, 1970; Wooley and Owen, 1977; Flynn and Gessaman, 1979; Beth et al., 1984; Brent et al., 1984). Some of these workers observed a strong correlation between fh and Vo,. A stronger correlation between fh and VP2 was observed for stubble quail than for king quatl. The reduction in Vo, following the injection of exogenous noradrenaline in stubble quail is consistent with that observed for some other avian species: the newly hatched fowl (Freeman, 1966; Allen and Marley, 1967; Marley and Stephenson, 1968, 1969, 1975; Allen et al., 1969, 1970) adult Japanese quail (Freeman, 1970b) and the titmouse (Hissa and Palokangas, 1970). This response was not observed in the black-headed gull (Pakolangas and Hissa, 1971). The dose-dependent nature of the response has been demonstrated by Hissa and Rautenberg (1974) but no satisfactory explanation has been suggested for this effect. From the results of the experiments on
547
stubble quail, there is no evidence of non-shivering thermogenesis playing a role in body temperature regulation below thermal neutrality. SUMMARY
King quail showed a greater tendency to hypothermia under experimental conditions than did stubble quail and this is most likely to be due to the smaller size of king quail. Below thermal neutrality, both species showed an inverse relationship between T, and fh, f,,V,, and the magnitude of shivering, with the relationship being curvilinear for V,, and shivering
activity. The responses
cold stress were qualitatively
of the two species to
similar.
REFERENCES
Allen D. J. and Marley E. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmacol. Chemother. 31, 290-312.
Allen D. J., Garg K. N. and Marley E. (1969) Hypothermia due to a-methyl-noradrenaline in young chickens. Br. J. Pharmucol. Chemother. 36, 195P-197P.
Allen D. J., Garg K. N. and Marley E. (1970) Mode of action of a-methyl-noradrenaline on temperature and oxygen consumption in young chickens. Br. J. Pharmacol. Chemother. 38, 667687.
Bamas G. and Rautenberg W. (1984) Respiratory responses to shivering produced by external and central cooling in the pigeon: &J&err A&h. 401, 228-232. Bamas G.. Nomoto S. and Rautenberu W. (1984) Cardiovascular’ and blood gas responses to-shivering produced by external and central cooling the pigeon. PpGgers Arch. 401, 223-227. Barre H. (1984) Metabolic and insulative changes in winterand summer-acclimatized King penguin chicks. J. camp. Physiol. 154B, 3 17-324. Bartholomew G. A., Hudson J. W. and Howell T. R. (1962) Body temperature, oxygen consumption, evaporative water loss, and heart rate in the poor-will. Condor 64, 117-125. Bartholomew G. A. and Trost C. H. (1970) Temperature regulation in the speckled mouse bird, Colius striatus. Condor 72, 141-146.
Beth C., Johansen K., Brent R. and Nichol S. (1984) Ventilatory and circulatory changes during cold exposure in the Pekin duck Anas platyrhynchos. Resp. Physiol. 57, 103-l 12.
Blakers M., Davies S. J. J. F. and Reilly P. N. (1984) The Atlas of Australian Birak. Melbourne University Press, Melbourne. Bouverot P., Hildwein G. and Oulhen P. (1976) Ventilatory and circulatory 0, convection at 40000m in pigeon at natural or cold temperature. Resp. Physiol. 28, 371-385. Brent R., Rasmussen J. G., Beth C. and Martini S. (1983) Temperature dependence of ventilation and O,-extraction in the Kittiwake, Rissa tridactyla. Experientia 39, 1092-1093. Brush A. (1965) Temperature relations of California quail. Comp. Biochem. Physiol. 15, 399421. Chaffee R. R. J., Mayhew W. W., Drebein M. and Cassuto Y. (1963) Studies on thermogenesis in cold-acclimated birds. Can. J. Biochem. Physiol. 41, 2215-2220. Chaplin S. B. (1976) The physiology of hypothermia in the black-capped chickadee, Parus atricapillus. J. camp. Physiol. 112B, 335-355. Coulombe H. N. (1970) Physiological and physical aspects of temperature regulation in the burrowing owl, Speotyto cunicularia. Comp. Biochem. Physiol. 35, 307-337.
548
JULIE T.
R.
ROBERTSand
Flynn R. K. and Gessaman R. A. (1979) An evaluation of heart rate as a measure of daily metabolism in pigeons (Columba liuia). Comp. Biochem. Physiol. 63A, 51 l-514. Freeman B. M. (1966) The effects of cold, noradrenalin and adrenalin upon the oxygen consumption and carbohydrate metabolism of the young fowl (Gallus domestic&). Comp. Biochem. Physiol. 18; 369-382. Freeman B. M. (1967) Some effects of cold on the metabolism of the fowiduring the perinatal period. Comp. Biochem. Physiol. 20, 179-193.
Freeman B. M. (1970a) Thermoregulatory mechanisms of the neonate fowl. Comp. Biochem. Physiol. 33, 219-230. Freeman B. M. (1970b) Some aspects of thermoregulation in the adult Japanese quail (Cofurnix coturnix japonica). Comp. Biochem. Physiol. 34, 871-881.
Hargrove J. L. and Gessaman J. A. (1973) An evaluation of respiratory rate as an indirect monitor of free-living metabolism. In Ecological Energetics of Homeotherms: A View Compatible with Ecological Modeling (Edited by Gessaman J. A.), pp. 77-85. Utah State University Press, Logan. Hart J. S. (1962) Seasonal acclimatization in four species of small wild birds. Physiol. 2001. 35, 224-236. Hissa R. and Palokangas R. (1970) Thermoregulation in the titmouse (Parus major L.). Comp. Biochem. Physiol. 33, 941-953.
Hissa R. and Rautenberg W. (1974) The influence of centrally applied noradrenaline on shivering and body temperature-in the pigeon. J. Physiol. 238, 421435. _ Hohtola E. ( 1981) Tonic immobility and shivering in birds: evolutionary implications. Physiol. Behau. 27,475480. Hohtola E. (1982) Thermal and electromyographic correlates of shivering thermogenesis in the pigeon. Comp. Biochem. Physiol. 73A, 159-166. Hudson J. W. and Brush A. H. (1964) A comparative study of the cardiac and metabolic performance of the dove, Zenaidura macroura, and the quail, Lophortyx californicus. Comp. Biochem. Physiol. 12, 157-170. Johnston D. W. (1971) The absence of brown adipose tissue in birds. Comp. Biochem. Physiol. 4OA, 1107-i108. Lasiewski R. C. and Dawson W. R. (1964) Phvsioloaical responses to temperature in the common nighthawk. Condor 66, 477-490.
Lustick S. (1970) Energetics and water regulation in the cowbird (Molothrus ater obscurus). Physiol. Zool. 43, 27&287.
Marjakangas A., Rintamaki H. and Hissa R. (1984) Thermal responses in the capercaillie Tetrao urogallus and the
R. V. BAUDINETTE black grouse Lyrurus terrix roosting in the snow. Physiol. Zool. 57, 99-104.
Marley E. and Stephenson J. D. (1968) Intracerebral microinfusions of amines in young chickens. J. Physiol. 196, 116P-117P. Marley E. and Stephenson J. D. (1969) Effects of some catecholamines infused into the hypothalamus of young chickens. Br. J. Pharmacol. Chemorher. 36, 194P-195P. Marley E. and Stephenson J. D. (1975) Effects of noradrenaline infused into the chick hypothalamus on thermoregulation below thennoneutrality. J. Physiol. 245, 289-304. No11 U. G. (1979) Body temperature, oxygen consumption,
noradrenaline response and cardiovascular adaptations in the flying fox, Rousettus aegyptiacus. Comp. Biochem. Physiol. 63A, 79-88. Oliphant L. W. (1983) First observations of brown fat in birds. Condor 85, 350-354. Owen R. B. Jr (1969) Heart rate, a measure of metabolism in blue-winaed teal. Camp. Biochem. Phvsiol. 31.431-436. Palokangas R. and Hissa-R. (1971) Thkrmoregulation in young black-headed gull Larus ridibundus L. Comp. Biochem. Physiol. 3!3A, 743-750. Roberts J. R. and Baudinette R. V. (1986) Thermoregulation, oxygen consumption and water turnover in Stubble quail, Coturnix pectoralis, and King quail Coturnix chinensis. Aust. J. Zool. 34, 2533.
Saarela S., Rintamaki H. and Saarela M. (1984) Seasonal variation in the dynamics of ptiloerection and shivering correlated changes in the metabolic rate and body temperature of the pigeon. J. camp. Physiol. 154B, 47-53. Saarela S. and Vakkuri 0. (1982) Photoperiod-induced changes in temperature-metabolism curve, shivering threshold and body temperature in the pigeon. Experienlia 38, 373-374.
Steen J. and Enger P. S. (1957) Muscular heat production in pigeons during exposure to cold. Am. J. Physiol. 191, 157-158. West G. C. (1965) Shivering and heat production in wild birds. Physiol. Zool. 38, 11I-120. West G. C., Funke E. R. R. and Hart J. S. (1968) Power spectral density and probability analysis of electromyograms in shivering birds. Can. J. Physiol. Pharmacol. 46, 703-706.
Wooley J. B. Jr and Owen R. B. Jr (1977) Metabolic rates and heart rate-metabolism relationships in the black duck (Anus rubripes). Comp. Biochem. Physiol. S7A, 363-367.
0
0300-9629188 $3.00 + 0.00 1988 PergamonPressplc
RESPONSES TO COLD STRESS IN TWO SPECIES OF AUSTRALIAN QUAIL, COTURNIX PECTORALIS AND CO TURNIX CHINENSIS JULIE T.
School of Biological
R.
Sciences, Flinders
ROBERTS*
(Received Abstract-l.
The responses
and R. V.
BAUDINETTE
University of South Australia, Telephone: (067) 73-2592
Bedford
Park, SA 5042, Australia.
22 March 1988)
to cold stress of two
species of Australian quail, stubble quail, Colurnix
pectoralis, and king quail, Coturnix chinensis, were assessed. 2. Body temperature (Ts), rate of oxygen consumption (V,,), heart rate (fh), respiration
rate (f,) and intensity of shivering measured by electromyographic voltage were recorded over a range of ambient temperatures of - 3-30°C. 3. Most individuals of both species were able to maintain Ts constant over this range of TA although some king quail had lowered T, at TA < 5°C. 4. Shivering intensity and V,, showed an inverse curvilinear relationship to TA and shivering was directly related to Vo,. The frequency of shivering appeared unrelated to TA 5. Heart rate (fh) and_& tended to be inversely related to TA and directly correlated with I’,,. 6. The responses of the two species were qualitatively very similar. 7. The response of stubble quail to noradrenaline suggests that non-shivering thermogenesis does not occur in this-species.
possesses histological characteristics typical of mammalian brown fat. In mammals, a thermogenic response to exogenous noradrenaline indicates the capacity for non-shivering thermogenesis. However, no thermogenic response has been demonstrated, in the avian species which have been studied, to exogenous noradrenaline (Hart, 1962; Chaffee et al., 1963; Freeman, 1966; Allen and Marley, 1967; Marley and Stephenson, 1968, 1969; Allen et al., 1969, 1970), adrenaline (Freeman, 1970a, b; Hissa and Palokangas, 1970; Palokangas and Hissa, 1971), or 5-hydroxytryptamine (Freeman, 1970a, b). In this study, simultaneous recordings of ambient temperature ( TA), body temperature (r,), respiration rate (f,), heart rate (fh), rate of oxygen consumption (V,,) and electromyographic activity of the pectoral musculature were made to investigate thermoregulatory responses of stubble quail, Coturnix pectoralis, and king quail, Coturnix chinensis, at ambient temperatures within and below thermal neutrality. The zone of thermal neutrality is 30-35°C for stubble quail and 28-35°C for king quail (Roberts and Baudinette, 1986). The responses of these closely related species of different body weights and from different habitats, to cold stress, were compared. Non-shivering thermogenesis was examined in stubble quail.
INTRODUCTION
Stubble quail are endemic to Australia and are found in some of the driest regions of the continent. The king quail is a geographic race of a pan-Asian species and occurs in wet grasslands (Blakers et al., 1984). Both species would be exposed, at some times of the year, to overnight temperatures at or below freezing. King quail have a body weight of only half that of the stubble quail. Therefore, one might expect the smaller species to have more difficulty maintaining body temperature at low ambient temperatures. The maintenance of homeothermy in birds, under conditions of cold stress, is dependent on behavioural, metabolic, insulative and cardiovascular adjustments. Heat production is augmented by the calorigenic processing of food, by exercise, shivering and, possibly, non-shivering thermogenesis. The importance of shivering to avian thermoregulation during cold stress has been investigated by a number of workers (Steen and Enger, 1957; Hart, 1962; West, 1965; West et al., 1968; Chaplin, 1976; Hohtola, 1981, 1982; Saarela and Vakkuri, 1982; Barre, 1984; Saarela et al., 1984; Marjakangas et aI., 1984; Barnas and Rautenberg, 1984; Barnas et aI., 1984). The evidence for the presence of non-shivering thermogenesis in birds is inconclusive. Brown adipose tissue, which in mammals is associated with nonshivering thermogenesis, was not found in the studies of Freeman (1967) or Johnston (1971). However, more recently, Oliphant (1983) has described, in ruffed grouse and black-capped chickadees, fat which *Present address: New England,
Department Armidale,
of Physiology, University NSW 2351, Australia.
MATERIALS AND METHODS
Quail were maintained indoors in individual cages (0.3m2) on a 12L/l2D photoperiod at ambient temperatures close to 25°C. During experiments, Ts was monitored via a chromel/alumel thermocouple (0.46 mm diameter) inserted I cm into the hindgut and read on a Comark Electronic Thermometer coupled to a chart recorder. Fine gold-plated electrodes were implanted, under local
of
543
544
JULIE T.
R.
ROBERTSand
anaesthesia, in the pectoral musculature. The pectoral electrodes were led into a Grass amplifier (Model TP5) and then to a Grass polygraph (Model 79D) and used for recording of respiration rate, heart rate and the electrical activity of the pectoral musculature. Data were obtained for eight stubble quail (mean body weight 126.1 k 4.4 g) and 12 king quail (mean body weight 49.6 + 1.7 g). Post-absorptive birds were placed inside Plexiglas chambers (0.145 m diameter; 0.1555 m high for king quail and 0.265 m high for stubble quail) in a controlled temperature room in the dark. An open-flow system was used to determine rates of oxygen consumption (I’,,). Air was drawn through large drying columns containing silica gel and into parallel animal and control chambers. The rate of flow was maintained at 0.8 l/min through a previously calibrated rotameter (Fischer and Porter). A Taylor Servomex oxygen analyser (Model OA.184 in conjunction with a servomex Ratio-Box Type 288) was used to monitor the difference in partial pressures of oxygen in sub-samples of the air streams and the output recorded on a potentiometric chart recorder. Vo, was calculated according to the following formula, and corrected to standard dry gas conditions.
where: pE is the flow rate from the chamber, Flat and FEot are the fractional oxygen contents in room and exhalent air respectively, and RQ is the respiratory quotient taken as 0.85. The birds were weighed before and after the experiment, and mass-specific rates (f’,,/m) calculated from interpolated body weights. Ambient temperature was monitored by a 30-ga copper/constantan thermocouple inserted through a sealed port in the top of the chamber and connected to a chart recorder. All thermocouples were calibrated against a NATA standard mercury-in-glass thermometer. The gas analyser was initially calibrated from changes in pressure within the analysis cell, but for daily calibrations, a mixture of 0, in N,, and pure N, were used. The controlled temperature room could be maintained only as low as 2°C and to achieve temperatures lower than this, air was cooled in a copper coil immersed in an ice-salt mixture before being introduced to the chamber. Temperatures down to -4°C could thus be maintained within 0.2% At each ambient temperature, several 10 set samples of electrical activity, within periods of steady-state oxygen consumption, were used to calculate mean heart and respiratory rates, and electromyographic activity. The humidity inside the metabolic chamber typically varied from 40-50% at TA < 0°C to =Z15% at TA= 25°C. King quail showed some tendency to become hypothermic if initially subjected to low ambient temperatures. It appeared that the handling of the animals during the installation of the electrodes and the use of topical anaesthetic led to an initial lowering of body temperature from which the birds could not recover spontaneously if immediately exposed to low ambient temperatures. Data from such birds were discarded, and for subsequent experiments with king quail, ambient temperatures were gradually reduced from levels within thermal neutrality. The time course for the experiments was between 8 and 12 hr. Six stubble quail (mean body weight 107.1 &-1.6g) were used to investigate the effect of noradrenaline on rates of oxygen consumption. Each animal was placed in a metabolism chamber and vo, determined as described previously. T, was maintained at 23.5”C, well below the zone of thermal neutrality. When a stable rate of oxygen consumption had been established, the bird was removed from the chamber, the noradrenaline in 1 ml of sterile saline was injected subcutaneously, and the animal replaced. A stable rate of oxygen consumption was then again obtained. The noradrenaline dose used was that of Heldmaier (1971, in Nell, 1979): dose (mg/kg) = 6.6 M (g)-0.4’8,a level
R. V. BAUDINETTE
previously shown to be effective in mammals. In the same six animals, the above procedure was repeated using control injections of isotonic saline. RESULTS Body temperature and rate of oxygen consumption
Body temperature in stubble quail showed little change with decreasing TA in this study. However, mean TB at TA less than or equal to 0°C (T, = 41.2”C) was significantly lower than mean Ts recorded in previous studies within the thermal neutral zone (Roberts and Baudinette, 1986). Some king quail demonstrated a decrease in TB at TA < 5°C and, as for stubble quail, the mean r, at TA less than or equal to 0°C (TB = 40.9”C) was significantly lower than previously recorded within thermal neutrality (Fig. 1). Rates of oxygen consumption showed a qualitatively similar pattern to that observed in noninstrumented birds at night (Roberts and Baudinette, 1986), but levels tended to be slightly higher at equivalent temperatures (Fig. 2). For both species, the relationship between TA and Vo, below thermal neutrality was curvilinear, with the data for stubble quail being best described by a power curve (y = 10.85x -“.42; r,,,, = 0.89) and that for king quail most closely fitting a monoexponential function (y = 9.03 e-0,03-r;rcorr= 0.94). Respiration rate
The variability in rates of breathing among individuals generally increased as TA decreased. For both species, meanf, at TA less than or equal to 0°C
k 0
A
-5
KO
I
I
I
I
5
15
25
35
AMBIENT
TEMPERATURE
(‘C)
Fig. I. The effect of ambient temperature on body temperature showing the lowering of body temperature which occurred at low ambient temperatures in some king quail. SQ is stubble quail; KQ is king quail.
545
to cold stress in Australian quail
Responses
$0” I -5
I 5
AMBIENT
1 15
0% I 25
35
o-l,
TE~J~PERATURE(~C)
2
Fig. 2. The effect of decreasing ambient temperature on oxygen consumption. The relationship was curvilinear for both species. SQ is stubble quail; KG is king quail.
(63.4 and 90.0 breaths/min for stubble and king quail, respectively) were significantly higher than their respective rates of 47.7 and 52.6 within thermal neutrality (Fig. 3). Higher metabolic rates were correlated with elevated respiration rates (Fig. 4). Shivering activity The intensity of shivering as measured by the peak-to-peak electromyographic voltage, increased markedly below 15°C (Fig. 5). The relationship between rA and the amplitude of shivering was best described by a monoexponential function in both stubble quail (y = 148.35 e-o.o7x; r,,,, = 0.84) and king quail (y = 119.18 e-“,MX; r,,,, = 0.75). Shivering activity was almost continuous at TA < 0°C becoming gradually less frequent until at TA = 10°C it occurred
,
,
,
,
,
,
,
3
4
5
8
7
9
9
OXYGEN
(
10
CONSUMPTION
( ml.02
(g.h)-l
)
Fig. 4. The relationship between breathing rate and oxygen consumption. Breathing rate tended to increase with increased oxygen consumption. SQ is stubble quail; KQ is king quail.
50-70% of the recorded time and had virtually ceased by TA = 22°C. That shivering contributes to body temperature and increased oxygen consumption in both quail species is apparent from Fig. 6. The mean frequency of shivering activity was 19/set and appeared unrelated to TA. 200
so
1 0 0
150 -I
_
100
> 2
50
2
c
i= J
,,,,
-5
5
16
25
i
5
0
0
I
I
t
I
I
-5
5
15
25
35
a 200x E 9 150-
35
KO
z v) loo-
50-
o-5
-5
5
AMBIENT
oJ,
I
I
5
15
AMBIENT
I
25
TEMPERATURE
1
35 (‘C)
Fig. 3. The effect of ambient temperature on breathing SQ is stubble quail; KQ is king quail.
rate.
15
25
TEMPERATURE
35 (‘Cl
Fig. 5. The effect of decreasing ambient temperature on shivering activity, showing the curvilinear nature of the shivering response. Shivering activity was measured as the peak-to-peak electromyographic voltage. SQ is stubble quail; KQ is king quail.
JULIE T.
546
R.
ROBERTS and
R. V. BAUDINETTE
5
,
IOOJ, 1
2
,
,
,
,
,
,
,
,
,
,
, 8
, 8
, 10
23456788
700-l
2ooJ,
I
234567 OXYGEN
I
I
8
I
a
,
IO
, 234507
,
OXYGEN
CONSUMPTION
( ml.02(g.h)-1
CONSUMPTION
(m1.02
1
Fig. 6. The effect of shivering activity on oxygen consumption, demonstrating the increase in oxygen consumption with increased shivering activity. SQ is stubble quail; KQ is king quail. Heart rate
The response of heart rate (Fig. 7) is very variable between individuals. In general, stubble quail showed a marked increase in fh with decreasing TA, and there
(g.h)_l)
Fig. 8. The relationship between heart rate and oxygen consumption. The relationship is linear for stubble quail with king quail showing more variability. SQ is stubble quail; KQ is king quail.
was some correlation betweenf, and V,, (Fig. 8). In king quail, these correlations were not as apparent (Figs 7 and 8). Both species showed elevated mean values at TA less than or equal to 0°C (350.1 and 540.9 beats/mm for stubble and king quail, respectively, compared with 225.2 and 372.2 beats/min, respectively, in thermal neutrality). Noradrenaline response
The rate of oxygen consumption ( vo2) prior to the noradrenaline injection was 2.07 + 0.05 ml O,/g/hr. Doses of noradrenaline of 0.9 mg/kg lowered V,, by 23% to 1.59 + 0.06 ml O2/g/hr. The V,, following the injections of saline alone was not significantly different from the controls at 2.15 + 0.09 ml O,/g/hr.
-5
J
-5 AMBIENT
5
15
I
I
5
15
25
I
25
TEMPERATURE
35
1 35 1°C)
Fig. 7. Changes in heart rate with decreasing ambient temperature, showing the tendency of heart rate to increase with decreasing ambient temperature. SQ is stubble quail; KQ is king quail.
DISCUSSION
Over the range of ambient temperatures employed in this study, no major change in body temperature was observed even at sub-zero temperatures, except in the case of some individual king quail. However, for both species, T, at TA less than or equal to 0°C was significantly lower than values previously recorded within thermal neutrality. It appears unlikely that either stubble or king quail undergo regular temporary hypothermia under natural conditions. In both species, the rate of oxygen consumption increases curvilinearly as T, decreases below the thermal neutral zone. Chaplin (1976) reports a similar response in the black-capped chickadee although most workers have reported a linear relationship. The transition from insulative adjustments to an increase in heat production (the lower critical temperature) seems to be abrupt in both stubble and king quail (Roberts and Baudinette, 1986).
Responses to cold stress in Australian quail Responses of avian f, to decreasing T,, below thermal neutrality, appear to vary between species.
Some, such as the burrowing owl (Coulombe, 1970) and the speckled mousebird (Bartholomew and Trost, 1970) have a relatively constant f,. In the Pekin duck (Beth et al., 1984) and the kittiwake (Brent er al., 1983)x decreased with TA from 20-22°C down to 0 and 6”C, respectively. In other species, for example hummingbirds (Hargrove and Gessaman, 1973) the cowbird (Lustick, 1970) and the pigeon (Bouverot et al., 1976), an inverse relationship exists and this pattern was also observed in stubble and king quail. The magnitude of shivering in stubble and king quail, as evidenced by the amplitude (voltage) of electromyographic activity, tended to be an inverse curvilinear function of TA and a direct linear function of Vo,. Chaplin (1976) reports a similar finding although other workers (Steen and Enger, 1957; Hart, 1962; West, 1965; West et al., 1968; Hissa and Palokangas, 1970) found that the relationship between TA and shivering activity was linear. Saarela and Vakkuri (1982) did not find a linear correlation between the intensity of shivering and Vo,, although Hohtola (1982) reports a correlation between electromyographic intensity (expressed as mean rectified value) and Vo2. The two-fold increase in the amplitude of shivering, observed in this study, has also been reported for pigeons (Steen and Enger, 1957) and the titmouse (Hissa and Palokangas, 1970). The frequency of electromyographic activity has been found to increase with decreasing TA in some species such as the pigeon (Steen and Enger, 1957) where it doubled between TA of 13°C and T, of -22-24°C and the evening grosbeak (West et al., 1968). Stubble and king quail, however, showed little variation in frequency, a phenomenon reported also for the common grackle (West et al., 1968). Hohtola (1982) found that the frequency of electromyographic activity was not related to Vo,. An inverse relationship exists between TA and fh for both stubble and king quail at ambient temperatures below thermal neutrality. A similar relationship has been observed for other avian species (Bartholomew et al., 1962; Lasiewski and Dawson, 1964; Hudson and Brush, 1964; Brush, 1965; Owen, 1969; Bartholomew and Trost, 1970; Coulombe, 1970; Wooley and Owen, 1977; Flynn and Gessaman, 1979; Beth et al., 1984; Brent et al., 1984). Some of these workers observed a strong correlation between fh and Vo,. A stronger correlation between fh and VP2 was observed for stubble quail than for king quatl. The reduction in Vo, following the injection of exogenous noradrenaline in stubble quail is consistent with that observed for some other avian species: the newly hatched fowl (Freeman, 1966; Allen and Marley, 1967; Marley and Stephenson, 1968, 1969, 1975; Allen et al., 1969, 1970) adult Japanese quail (Freeman, 1970b) and the titmouse (Hissa and Palokangas, 1970). This response was not observed in the black-headed gull (Pakolangas and Hissa, 1971). The dose-dependent nature of the response has been demonstrated by Hissa and Rautenberg (1974) but no satisfactory explanation has been suggested for this effect. From the results of the experiments on
547
stubble quail, there is no evidence of non-shivering thermogenesis playing a role in body temperature regulation below thermal neutrality. SUMMARY
King quail showed a greater tendency to hypothermia under experimental conditions than did stubble quail and this is most likely to be due to the smaller size of king quail. Below thermal neutrality, both species showed an inverse relationship between T, and fh, f,,V,, and the magnitude of shivering, with the relationship being curvilinear for V,, and shivering
activity. The responses
cold stress were qualitatively
of the two species to
similar.
REFERENCES
Allen D. J. and Marley E. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmacol. Chemother. 31, 290-312.
Allen D. J., Garg K. N. and Marley E. (1969) Hypothermia due to a-methyl-noradrenaline in young chickens. Br. J. Pharmucol. Chemother. 36, 195P-197P.
Allen D. J., Garg K. N. and Marley E. (1970) Mode of action of a-methyl-noradrenaline on temperature and oxygen consumption in young chickens. Br. J. Pharmacol. Chemother. 38, 667687.
Bamas G. and Rautenberg W. (1984) Respiratory responses to shivering produced by external and central cooling in the pigeon: &J&err A&h. 401, 228-232. Bamas G.. Nomoto S. and Rautenberu W. (1984) Cardiovascular’ and blood gas responses to-shivering produced by external and central cooling the pigeon. PpGgers Arch. 401, 223-227. Barre H. (1984) Metabolic and insulative changes in winterand summer-acclimatized King penguin chicks. J. camp. Physiol. 154B, 3 17-324. Bartholomew G. A., Hudson J. W. and Howell T. R. (1962) Body temperature, oxygen consumption, evaporative water loss, and heart rate in the poor-will. Condor 64, 117-125. Bartholomew G. A. and Trost C. H. (1970) Temperature regulation in the speckled mouse bird, Colius striatus. Condor 72, 141-146.
Beth C., Johansen K., Brent R. and Nichol S. (1984) Ventilatory and circulatory changes during cold exposure in the Pekin duck Anas platyrhynchos. Resp. Physiol. 57, 103-l 12.
Blakers M., Davies S. J. J. F. and Reilly P. N. (1984) The Atlas of Australian Birak. Melbourne University Press, Melbourne. Bouverot P., Hildwein G. and Oulhen P. (1976) Ventilatory and circulatory 0, convection at 40000m in pigeon at natural or cold temperature. Resp. Physiol. 28, 371-385. Brent R., Rasmussen J. G., Beth C. and Martini S. (1983) Temperature dependence of ventilation and O,-extraction in the Kittiwake, Rissa tridactyla. Experientia 39, 1092-1093. Brush A. (1965) Temperature relations of California quail. Comp. Biochem. Physiol. 15, 399421. Chaffee R. R. J., Mayhew W. W., Drebein M. and Cassuto Y. (1963) Studies on thermogenesis in cold-acclimated birds. Can. J. Biochem. Physiol. 41, 2215-2220. Chaplin S. B. (1976) The physiology of hypothermia in the black-capped chickadee, Parus atricapillus. J. camp. Physiol. 112B, 335-355. Coulombe H. N. (1970) Physiological and physical aspects of temperature regulation in the burrowing owl, Speotyto cunicularia. Comp. Biochem. Physiol. 35, 307-337.
548
JULIE T.
R.
ROBERTSand
Flynn R. K. and Gessaman R. A. (1979) An evaluation of heart rate as a measure of daily metabolism in pigeons (Columba liuia). Comp. Biochem. Physiol. 63A, 51 l-514. Freeman B. M. (1966) The effects of cold, noradrenalin and adrenalin upon the oxygen consumption and carbohydrate metabolism of the young fowl (Gallus domestic&). Comp. Biochem. Physiol. 18; 369-382. Freeman B. M. (1967) Some effects of cold on the metabolism of the fowiduring the perinatal period. Comp. Biochem. Physiol. 20, 179-193.
Freeman B. M. (1970a) Thermoregulatory mechanisms of the neonate fowl. Comp. Biochem. Physiol. 33, 219-230. Freeman B. M. (1970b) Some aspects of thermoregulation in the adult Japanese quail (Cofurnix coturnix japonica). Comp. Biochem. Physiol. 34, 871-881.
Hargrove J. L. and Gessaman J. A. (1973) An evaluation of respiratory rate as an indirect monitor of free-living metabolism. In Ecological Energetics of Homeotherms: A View Compatible with Ecological Modeling (Edited by Gessaman J. A.), pp. 77-85. Utah State University Press, Logan. Hart J. S. (1962) Seasonal acclimatization in four species of small wild birds. Physiol. 2001. 35, 224-236. Hissa R. and Palokangas R. (1970) Thermoregulation in the titmouse (Parus major L.). Comp. Biochem. Physiol. 33, 941-953.
Hissa R. and Rautenberg W. (1974) The influence of centrally applied noradrenaline on shivering and body temperature-in the pigeon. J. Physiol. 238, 421435. _ Hohtola E. ( 1981) Tonic immobility and shivering in birds: evolutionary implications. Physiol. Behau. 27,475480. Hohtola E. (1982) Thermal and electromyographic correlates of shivering thermogenesis in the pigeon. Comp. Biochem. Physiol. 73A, 159-166. Hudson J. W. and Brush A. H. (1964) A comparative study of the cardiac and metabolic performance of the dove, Zenaidura macroura, and the quail, Lophortyx californicus. Comp. Biochem. Physiol. 12, 157-170. Johnston D. W. (1971) The absence of brown adipose tissue in birds. Comp. Biochem. Physiol. 4OA, 1107-i108. Lasiewski R. C. and Dawson W. R. (1964) Phvsioloaical responses to temperature in the common nighthawk. Condor 66, 477-490.
Lustick S. (1970) Energetics and water regulation in the cowbird (Molothrus ater obscurus). Physiol. Zool. 43, 27&287.
Marjakangas A., Rintamaki H. and Hissa R. (1984) Thermal responses in the capercaillie Tetrao urogallus and the
R. V. BAUDINETTE black grouse Lyrurus terrix roosting in the snow. Physiol. Zool. 57, 99-104.
Marley E. and Stephenson J. D. (1968) Intracerebral microinfusions of amines in young chickens. J. Physiol. 196, 116P-117P. Marley E. and Stephenson J. D. (1969) Effects of some catecholamines infused into the hypothalamus of young chickens. Br. J. Pharmacol. Chemorher. 36, 194P-195P. Marley E. and Stephenson J. D. (1975) Effects of noradrenaline infused into the chick hypothalamus on thermoregulation below thennoneutrality. J. Physiol. 245, 289-304. No11 U. G. (1979) Body temperature, oxygen consumption,
noradrenaline response and cardiovascular adaptations in the flying fox, Rousettus aegyptiacus. Comp. Biochem. Physiol. 63A, 79-88. Oliphant L. W. (1983) First observations of brown fat in birds. Condor 85, 350-354. Owen R. B. Jr (1969) Heart rate, a measure of metabolism in blue-winaed teal. Camp. Biochem. Phvsiol. 31.431-436. Palokangas R. and Hissa-R. (1971) Thkrmoregulation in young black-headed gull Larus ridibundus L. Comp. Biochem. Physiol. 3!3A, 743-750. Roberts J. R. and Baudinette R. V. (1986) Thermoregulation, oxygen consumption and water turnover in Stubble quail, Coturnix pectoralis, and King quail Coturnix chinensis. Aust. J. Zool. 34, 2533.
Saarela S., Rintamaki H. and Saarela M. (1984) Seasonal variation in the dynamics of ptiloerection and shivering correlated changes in the metabolic rate and body temperature of the pigeon. J. camp. Physiol. 154B, 47-53. Saarela S. and Vakkuri 0. (1982) Photoperiod-induced changes in temperature-metabolism curve, shivering threshold and body temperature in the pigeon. Experienlia 38, 373-374.
Steen J. and Enger P. S. (1957) Muscular heat production in pigeons during exposure to cold. Am. J. Physiol. 191, 157-158. West G. C. (1965) Shivering and heat production in wild birds. Physiol. Zool. 38, 11I-120. West G. C., Funke E. R. R. and Hart J. S. (1968) Power spectral density and probability analysis of electromyograms in shivering birds. Can. J. Physiol. Pharmacol. 46, 703-706.
Wooley J. B. Jr and Owen R. B. Jr (1977) Metabolic rates and heart rate-metabolism relationships in the black duck (Anus rubripes). Comp. Biochem. Physiol. S7A, 363-367.