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Nocturnal hypothermia in the Inca dove, Scardafella inca
Corap. Biochem. Physiol., 1967, Vol. 23, pp. 243 to 253. Pergamon Press. Printed in Great Britain
NOCTURNAL HYPOTHERMIA IN THE INCA DOVE, SCARDAFELLA INCA RICHARD E. MAcMILLEN and CHARLES H. T R O S T * Department of Zoology, Pomona College, Claremont, California 91711, U.S.A.
(Received 27 April 1967)
A b a t r a c t - - 1 . When deprived of food and/or water Inca doves experience
pronounced nocturnal hypothermia, the depth of which is independent of Ta and reflects nutritional state. 2. Nocturnal hypothermia results in considerable conservation of both energy and water, the magnitude depending upon depth of hypothermia. 3. Body temperature fluctuations operate on a strict circadian schedule even in the absence of photoperiodic dues, denoting precise endogenous control.
INTRODUCTION
THE SMALL size (40-50 g) of the Inca dove, an inhabitant of desert settlements in
the southwestern United States, imparts potential problems relating to energetics and water economy. The high diurnal water requirements, however, are readily met by the abundant fresh water afforded by its urban environment (MacMillen & Trost, 1966). In addition, and even during heat stress, the Inca dove's thermoregulatory and metabolic performances are geared to an appropriate compromise between heat production and evaporative cooling, thereby ensuring an optimal degree of water and energy balance throughout the day (MacMillen & Trost, 1967). However, at night avian behavioral limitations preclude feeding and drinking, thereby potentially exposing the birds to lengthy periods of continual energy and water drain. Birds commencing the nocturnal period in a well-fed, well-watered condition become extremely quiescent at night and decrease metabolic rates slightly, resulting in a significant decrease in body temperature with a concomitant decrease in pulmocutaneous water loss (op. dt., 1967). The nocturnal demands on water and energy balance of Inca doves would be still further accentuated during periods of inclement weather: (1) diurnal periods of excessive heat necessitating nearly continuous evaporative cooling could well leave the birds in a state of negative water balance at dusk; or (2) rainy weather and/or periods of low food supply combined with cold could result in Inca doves commencing the nocturnal period with unusually low energy reserves. *Present address: Department of Zoology, University of California, Los Angeles, California 90024, U.S.A. 243
244
RICHARD E. MACMILLEN AND CHARLES H . TROST
The circadian body temperature lability of well-fed and well-watered birds
(op. cit., 1967) suggests the possibility of still greater nocturnal depressions of body temperatures when normal food and/or water intakes are restricted. Such depressions could result in reduced energy and water expenditures, which would physiologically decrease the severity of otherwise demanding nights. This study undertakes, therefore, to explore the role of nocturnal hypothermia in the energy and water metabolism of the Inca dove. MATERIALS AND METHODS
Experimental animals The sixteen adult Inca doves employed in this study were collected in Tucson, Pima County, Arizona, between September 1964 and July 1965. The birds were shipped by air to California where, except during measurements, they were housed individually in a windowless room on a 12-hr photoperiod (lights on from 06.00 to 18.00 hr). Between periods of measurement the birds were provided in excess with tap water for drinking and mixed bird seed for food. The mean body weight of the doves after several weeks in captivity was 44-2 _+S.D. 3-1 g.
Measurements The parameters measured included simultaneous measurements in constant darkness of ambient temperature (TA), body temperature (TB), oxygen consumption and pulmocutaneous water loss. One bird was placed in each of two 1 U.S. gal metal respirometer chambers equipped with ports for the introduction and removal of air and for thermocouples. Oxygen consumption was measured with a Beckman Model E2 paramagnetic oxygen analyzer in an open air system, with a flow rate of 500 cm3/min. T A and TB were determined with copper-constantan thermocouples connected to a recording potentiometer; T B was measured by means of a thermocouple surgically implanted in the pectoral musculature. Pulmocutaneous water loss was determined gravimetrically by passing expired air through a desiccating tube containing calcium chloride. T n was controlled within + 0.5°C by placing animals in respirometer chambers inside an insulated constanttemperature cabinet. A detailed discussion of the precise methodology employed appears in an earlier study of thermoregulation and water loss in the Inca dove (MaeMillen & Trost, 1967).
Effects of food and/or water restriction To test the combined long-term effects of food and water deprivation on the parameters to be measured, two well-fed and well-watered Inca doves were placed separately in respirometer chambers at T = 20 + 0.5°C in the constant-temperature cabinet and in complete darkness at 11.00 hr. They remained under these conditions for 49 hr during which T B was measured alternately for 5-min intervals for each bird; oxygen consumption and pulmocutaneous water loss were measured simultaneously for 1-hr periods at the middle of what had previously been the
NOCTURNAL HYPOTHERMIA I N INCA DOVE
245
12-hr light and the 12-hr dark periods (measurements were made at 14.00, 22.00, 11.00, 22.00 and 11.00 hr during the 49-hr period). The birds were weighed at the beginning of the experiment and at the end; body weights during the measurements of oxygen consumption and pulmocutaneous water loss were interpolated. Well-fed and well-watered Inca doves were also placed in darkened respirometer chambers for 49-hr periods at T A = 10°C and 30°C, to test the relationship between nocturnal hypothermia and T A. TB was measured continually, and oxygen consumption was measured at the middle of what had previously been the light and dark periods. To test the effects of food deprivation and water deprivation separately, birds were deprived of either food or water for 24 hr under the usual 12-hr photoperiod, and provided with the other commodity in excess. At 12.00 hr, following the 24 hr of deprivation, and in the middle of the light period, the birds were placed in darkened respirometer chambers in the constant-temperature cabinet where they remained for an additional 24 hr at T A = 20°C. T B was recorded continually. RESULTS Body temperature
When removed from a regular 12-hr photoperiod and placed in continual darkness for 49 hr without food and water and at TA = 20°C, Inca doves exhibit a synchronous circadian body temperature lability (Fig. 1). This lability is characterized by highest T B during what had previously been the middle of the light period and lowest T B during what had previously been the middle of the dark 45
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FIG. 1. Circadian fluctuations in body temperatures of six Inca doves held in the dark for 49 hr without food and water at Ta = 20°C. Each dot represents the Ta of a single animal, and TB of each animal is represented at 30-min intervals. T h e solid horizontal bars represent the duration of the dark portion of the 12-hr photoperiod to which the animals had been subjected prior to the experiment; the spaces between the bars indicate the light portion.
246
RICHARD R. MAcMILLEN AND CHARLES H. TROST
period; the depth of nocturnal hypothermia increased progressively during the two consecutive nights of the experiment. Table 1 indicates mean T B during the middles of what had previously been the light and the dark periods throughout the 49-hr experiment. TABLE 1--MEAN
BODY TEMPERATURES OF SIX INCA DOVES TAKEN AT 1 2 - h r
INTERVALS AND
HELD IN THE DARI
12.00 1 42-7
24.00 13 38.8
12.00 25 40"6
24.00 37 35"1
12.00 49 39"8
Even when in complete darkness and tested separately, entry into hypothermia was synchronous with clock time and began about 2 hr prior to what had been the beginning of the dark period. Arousal was equally synchronous and was initiated sufficiently in advance of the start of what had been the light period that arousal was essentially complete by the time the lights would normally have gone on.
Oxygen consumption and pulmocutaneous water loss T h e rates of oxygen consumption during the 49-hr of food and water deprivation and in darkness reflect very closely the circadian cycle in TB (Fig. 2). During °' ,,,8,
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FIG. 2. Rates of oxygen consumption measured at approximately 12-hr intervals in Inca doves held in the dark for 49 hr without food and water at Ta = 20°C. The horizontal lines represent the means. Vertical lines indicate the extremes. The rectangles inclose the intervals .Y_+t0.gs S.E. The numbers represent: the numbers of birds measured at each interval (the numbers of measurements at each interval). The solid bar indicates the duration of the dark period to which the animals had been subjected prior to the experiment. the first and second nights of the experiment oxygen consumption was significantly reduced to 80 and 58 per cent, respectively, of the first midday measurement, denoting a considerable energy saving (see Table 2 for absolute diurnal and nocturnal values). T h e mean rate of oxygen consumption of the second night was significantly lower than that of the first night. T h e mean rate of oxygen consumption for each successive midday measurement was progressively but insignificantly lower.
247
N O C T U R N A L H Y P O T H E R M I A I N I N C A DOVE
Like the measurements of oxygen consumption during the 49-hr period, the rates of pulmocutaneous water loss also fluctuated directly with circadian changes in TB (Fig. 3). The first and second nights' values were reduced to 55 and 36 per IO e~ s
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FIG. 3. Rates of pulmocutaneous water loss measured at approximately 12-hr intervals in Inca doves held in the dark for 49 hr without food and water at T A = 20°C. Symbols as in Fig. 2.
cent, respectively, of the first day's value. Although not quite significantly lower than the first night's rate of water loss, the second night's rate was significantly lower than any of the midday values (see Table 2 for absolute diurnal and nocturnal values).
Relationship between nocturnal hypothermia, T B and body weight The depth of nocturnal hypothermia was directly related to changes in body weight experienced prior to commencing an experiment. Figure 4 indicates the 45 40
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FIG. 4. T h e courses of body temperatures of seven Inca doves previously kept for varying lengths of time without food and water, and then held in continuous darkness at T a = 20°C. T h e numbers represent the interpolated body weights of individual birds (expressed as per cent of original body weight since last in a wellfed, well-watered state) when the level of deepest nocturnal hypothermia was attained. T h e solid bar indicates the duration of the dark period of the previous 12-hr photoperiod.
248
RICHARD E. MACMILLEN AND CHARLES H. TROST
courses of TB at T A = 20°C in seven representative Inca doves with various weight histories prior to the experimental routine: some were allowed to commence the 24-hr experiment in a well-fed and well-watered condition, while others had been deprived of food and water for varying lengths of time (up to 24 hr) prior to the experiment. It is clear that the depth of nocturnal hypothermia is directly related to the amount of body weight lost since last in a well-fed and well-watered state. In addition, successful spontaneous arousal, at least at T A = 20°C, appears to be limited to those birds experiencing no more than about 15 per cent loss in weight from the well-fed, well-watered state (Fig. 4). The lowest T B achieved with what would have been an ensuing successful arousal if food, water and light had been available was 28.5°C in a bird whose interpolated body weight in the midpoint of hypothermia was 85 per cent of its well-fed, well-watered weight. This bird aroused to a TB of 35°C at 06.00 hr (previously the beginning of its photoperiod), but then, with darkness continuing, entered a deep hypothermia with TB reaching a low of 25.5°C at 12.00 hr. Both this bird and another, which failed to arouse and which ultimately reached a T B of 22°C, were incapable of spontaneous arousal at T A = 20°C, even when shaken vigorously. However, when removed from the experimental situation and placed under heat lamps, both birds recovered fully and, after eating and drinking, were capable of normal thermoregulation. One bird, which had lost nearly 20 per cent of its initial well-fed, well-watered weight in the midpoint of hypothermia, entered hypothermia at an extremely fast rate and ultimately died. In Fig. 5 is shown the relationship between the depth of nocturnal hypothermia and the interpolated body weight of the bird at the time of achieving its lowest TB. As indicated in this figure, nocturnal hypothermia can be induced by either prior I~
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FIO. 5, The relationship between weight lost since las~ in a well-fed and/or wellwatered state and the low TB attained during nocturnal hypothermia at T A = 20°C. The solid circles represent birds experiencing prior food deprivation and prior food and water deprivation; hollow circles represent birds experiencing prior water deprivation. food restriction, prior food and water restriction, or prior water restriction; all restrictions result in weight loss and produce hypothermia, the depth of which is directly related to weight loss. In mourning doves MacMillen (1962) has suggested that water deprivation results in cessation of feeding, and Schmid (1965) indicates
NOCTURNALHYPOTI-IEI~IIAIN INCADOVE
249
that wetting of crop contents was necessary to initiate digestion. A similar situation most likely occurs in the very water-dependent Inca doves, and it is presumed that much of the weight loss resulting from water deprivation is indirectly a result of the inability to process foods. Thus, nocturnal hypothermia resulting from food and/or water restriction very likely is a response to the same stimulus, i.e. weight loss due to energy drain. Because of this likelihood all of the data in Fig. 5 are considered as results of the same phenomenon, and have together been analyzed by the method of least squares; the equation derived from this analysis and predicting this relationship is: y = - 28.16 + 0.70x, where y is the low T B attained during nocturnal hypothermia and x is the interpolated relative body weight when that T B was attained. Relationship between nocturnal hypothermia and T a To test the relationship between the depth of nocturnal hypothermia and TA, initially well-fed and well-watered Inca doves were placed for 49 hr in darkened respirometer chambers at T A = 10 °, 20 ° and 30°C. Figure 6 indicates this relationship, and shows that nocturnal hypothermia at T A = 10 ° and 20°C tends to be I-: IOO De
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FIG. 6. T h e r e l a t i o n s h i p b e t w e e n w e i g h t lost since last in a well-fed, w e l l - w a t e r e d state a n d t h e d e p t h of n o c t u r n a l h y p o t h e r m i a at T21 = 10 °, 20 ° a n d 30°C. H o l l o w squares r e p r e s e n t this relationship at T 4 = 30°C, solid circles at T a = 20°C a n d stars at T a = 10°C.
much deeper per loss in body weight than at TA = 30°C. These data lend themselves to analysis of covariance which reveals that the relationship between the depth of nocturnal hypothermia and weight loss is not significantly different at TA = 10°C and 20°C, while, at T a = 30°C, the relationship is significantly different to that at the other two Tjs. The equations describing these relationships at the three temperatures and derived by the method of least squares is as follows: TA = 10°C: y = -19.42+0.59x, TA = 20°C: y = -11-37+0.52x, TA = 30°C: y = -20.31+0.19x, where y is the low T B and x is the interpolated body weight at the time of that T B.
250
RICHARD E. MACMILLEN AND CHARLES H. TROST
A l t h o u g h t h e d e p t h o f n o c t u r n a l h y p o t h e r m i a a p p e a r s to b e i n d e p e n d e n t o f TA, at least at l o w t e m p e r a t u r e s , t h e rates o f o x y g e n c o n s u m p t i o n , w h e t h e r n o r m o t h e r m i c o r h y p o t h e r m i c , are v e r y d e p e n d e n t u p o n T,a ( F i g . 7). A n a l y s i s of c o v a r i a n c e 5 t
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reveals that the slopes of oxygen consumption at T A = 10 °, 20 ° and 30°C arc all highly significantly different. T h e s e slopes of oxygen consumption are described by the following equations derived by the method of least squares: TA = 10°C: TA = 20°C: T~ = 30°C:
y = -2-57+0.15x, y = -2.67+0.13x, y = -5.85+0-19x,
where y represents the rate of oxygen consumption and x is the T B at that rate. TABLE 2--MEAN
B O D Y T E M P E R A T U R E S , RATES O F O X Y G E N C O N S U M P T I O N A N D P U L M O C U T A N E O U S
W A T E R LOSS MEASURED A T VARIOUS I N T E R V A L S T H R O U G H O U T A 20 ° AND
Time, hr 14.00 Hour of experiment 3 Body temperatures, °C T a = 10°C 40.9 (4) T A = 20°C 41.4 (5) T A = 30°C 40.9 (4) Oxygen consumption, (cm3/g)/hr T~ = 10°C 3-3 (8) T A = 20°C 2-6 (10) T A = 30°C 1"8 (8) Pulmocutaneous water loss, % body wt/day T a = 10°C 5'0 (4) T A = 20°C 6-9 (4) T a = 30°C 8-2 (4)
49-hr
P E R I O D , A N D A T T A = 1 0 °,
30°C* 22.00 11
11.00 24
22.00 35
11.00 48
37.4 (5) 38.2 (9) 38.8 (5)
40.5 (5) 40.9 (9) 40.6 (5)
33.0 (2) 34.0 (9) 36.6 (5)
38.5 (2) 38.9 (8) 39.2 (5)
2.9 (10) 2.0 (18) 1'5 (10)
3.6 (10) 2.5 (18) 1"6 (10)
2-6 (8) 1.5 (18) 1'0 (10)
3.4 (4) 2.4 (16) l-5 (10)
3"4 (5) 3"8 (9) 5'9 (5)
5-9 (5) 5-2 (9) 6"4 (5)
3'2 (4) 2"5 (9) 4"1 (5)
4.3 (2) 4'8 (7) 5"6 (5)
* T h e numbers in parentheses represent the number o f birds measured except for measurements of oxygen consumption, where the numbers in parentheses represent the numbers of oxygen consumption measurements (two measurements on each bird).
N O C T U R N A L H Y P O T H E R M I A I N I N C A DOVE
251
In Table 2 are indicated mean TB and rates of oxygen consumption and pulmocutaneous water loss as measured for all Inca doves at TA = 10 °, 20 ° and 30°C, and at approximately 12-hr intervals throughout the 49-hr period. DISCUSSION It was previously demonstrated that Inca doves characteristically become hyperthermic in response to diurnal heat stress, occasionally undergoing an increase in T B to as high as 47°C without apparent harm (MacMillen & Trost, 1967). The present study, in addition, indicates that the same birds may, under certain circumstances, experience a decrease in TB during the night to as low as 30°C. Thus, while considered homeothermic and with good physiological control of thermoregulation, Inca doves may on occasion exhibit circadian body temperature fluctuations which are at least of equal magnitude to those of poikilotherms living in the same area and which are dependent primarily upon behavioral control. While the value of diurnal hyperthermia is primarily that of water conservation, nocturnal hypothermia results both in energy andwater conservation, the amounts depending upon the depth of hypothermia (Figs. 1, 2 and 3). Although hypothermia can be induced either by food and/or water restriction (Fig. 5), it is believed that the ultimate response is due to drain of energy reserves, since it is unlikely that doves can mechanically process food in the crop without access to drinking water. Such an energy drain, as well as continual water expenditure, results in loss of body weight during the night, producing nocturnal hypothermia, the depth of which is directly related to the amount of weight lost since last in a well-fed and well-watered state (Fig. 4). Most birds known to employ hypothermia, either nocturnally or seasonally, have T~s while hypothermic which vary by only 1° to 3°C from T~ (Pearson, 1960). Such is not the condition in Inca doves where nocturnal T B is largely independent of Ta, and appears to be dictated by nutritional state (Fig. 4). Thus we hesitate to apply the term 'torpor' to hypothermic Inca doves, as this term is best applicable when TB fluctuates with T A (MacMillen, 1965). Rather, the phenomenon in Inca doves appears to be an exaggeration of the usual nocturnal decrease in Ts so characteristic of diurnal birds (see King & Farner, 1960, for extensive discussion). That the depth of nocturnal hypothermia is dictated more directly by nutritional state than by T a, at least at TA < 30°C, is indicated in Fig. 6. However, the nocturnal energy drain of hypothermic birds is directly related to T A (Fig. 7), so that birds starting the night with similar energy levels will become more profoundly hypothermic under conditions of lower T A. Even in the absence of external clues, the T B fluctuations of Inca doves tested independently maintains a strict circadian periodicity, reflecting closely the temporal aspects of the photoperiod to which they previously had been subjected (Fig. 1). Such precise endogenous control, doubtless entrained by seasonal changes in photoperiod, ensures that birds will be fully aroused and alert by dawn, not susceptible to predation, and ready to replenish energy and water expended during
252
RICHARD E. MAcMILLEN AND CHARLES H . TROST
the night. However, only those birds which had lost no more than 15 per cent of the well-fed, well-watered weight were able to arouse spontaneously. Thus birds failing to arouse ultimately developed TB close to T A and were incapable of endogenous control of thermoregulation. However, under natural circumstances in the desert, even these birds most likely would be subjected to postdawn solar warming. Such warming, as in the application of external heat in the laboratory, could result in full arousal and, if the birds could then find food and water, would yield an additional opportunity for survival. The incidence of nocturnal hypothermia in non-captive Inca doves is unknown, however field and laboratory observations suggest that nocturnal depressions of more than 2-3°C are not nightly occurrences. At 01.00 hr on the morning of 29 January 1966 in Tucson, Arizona, and with T A = 8°C many Inca doves were observed roosting in trees. They generally roosted 10-12 ft above the ground, in groups of three to five birds sleeping with bodies pressed tightly together. Such huddling behavior would yield a more favorable surface-volume relationship, thereby minimizing heat loss and energy drain. When disturbed the birds were quite capable of coordinated movement, indicating high T B. A singly roosting Inca dove, found within reach, had a cloacal TB, 15 sec after capture, of 39-7°C, well within the typical well-fed, well-watered nocturnal range (see Fig. 1). Thus profound nocturnal hypothermia, previously unreported in Columbiformes, appears in the Inca dove to be largely an emergency device which is always on hand to be called upon, and to whatever degree circumstances demand. The occurrence and the characteristics of this hypothermia reflect very closely the store of energy and/or water reserves, and therefore ensure minimal expenditures when these commodities are in least supply. Steen (1958) has reported an apparently similar occurrence of nocturnal hypothermia in six species of small, newly captured Norwegian Passeriformes during cold winter nights. Steen's observations, together with these on the Inca dove, suggest that nocturnal hypothermia, rather than being confined to a few insectivorous or nectar-feeding birds, may be a quite common aspect of the physiological repertoire of small birds in general, during periods of stress. SUMMARY When removed from a 12-hr photoperiod to continuous darkness at TA = 20°C and without food and water, Inca doves experience circadian fluctuations in rib which reflect very closely the temporal aspects of the previous photoperiod. The fluctuations consist of high diurnal T B alternating with nocturnal hypothermia whose depth increases progressively on consecutive nights. Although nocturnal hypothermia can be induced by either food and/or water restriction, its depth appears to be largely dictated by energy level and is independent of T A. The lowest T B routinely observed during nocturnal hypothermia was 30°C, occurring at a weight of approximately 85 per cent of the well-fed, well-watered state. Below 85 per cent, birds become extremely hypothermic and lose endogenous control of thermoregulation.
NOCTURNAL H Y P O T H E R M I A I N INCA DOVE
253
Nocturnal hypothermia results in considerable saving in both energy and water, the magnitude depending u p o n depth of hypothermia. I t is herein looked u p o n as an emergency device enhancing survival through ~ h a t otherwise would be physiologically demanding nights and while operating on low energy and water budgets.
Acknowledgements--This investigation was supported by National Science Foundation Grant GB-2459. We are grateful to Dr. L. H. Blankenship, Mr. J. C. Truett and Mr. G. L. Richardson of the Cooperative Wildlife Unit, University of Arizona, for aid in obtaining birds. In addition we are most appreciative of aid and advice received in statistical treatment of some of the data from Dr. D. L. Bentley and Mr. J. J. Crowley, Department of Mathematics, Pomona College, who were supported in part by National Institutes of Health Grant 2G-945. REFERENCES KING J. R. & EARNERD. S. (1960) Energy metabolism, thermoregulation and body temperature. In Biology and Comparative Physiology of Birds (Edited by MARSHALL A. J.) Vol. 2, pp. 215-288. Academic Press, New York. MAcMILLEN R. E. (1962) The minimum water requirements of mourning doves. Condor 64, 165-166. MAcMILLEN R. E. (1965) Aestivation in the cactus mouse, Peromyscus eremicus. Comp. Biochem. Physiol. 16, 227-24-8. MACMILLEN R. E. & TROST C. H. (1966) Water economy and salt balance in white-winged and Inca doves. Auk 83, 441456. MAcMILLEN R. E. & TROST C. H. (1967) Thermoregulation and water loss in the Inca dove. Comp. Biochem. Physiol. 20, 263-273. PEARSON O. P. (1960) Torpidity in birds. Bull. Mus. comp. Zool. Harv. 124, 93-103. SCHMIDW. D. (1965) Energy intake of the mourning dove, Zenaidura macroura marginella. Science, N . Y . 150, 1171-1172. STUN J. (1958) Climatic adaptation in some small northern birds. Ecology 39, 625-629.
NOCTURNAL HYPOTHERMIA IN THE INCA DOVE, SCARDAFELLA INCA RICHARD E. MAcMILLEN and CHARLES H. T R O S T * Department of Zoology, Pomona College, Claremont, California 91711, U.S.A.
(Received 27 April 1967)
A b a t r a c t - - 1 . When deprived of food and/or water Inca doves experience
pronounced nocturnal hypothermia, the depth of which is independent of Ta and reflects nutritional state. 2. Nocturnal hypothermia results in considerable conservation of both energy and water, the magnitude depending upon depth of hypothermia. 3. Body temperature fluctuations operate on a strict circadian schedule even in the absence of photoperiodic dues, denoting precise endogenous control.
INTRODUCTION
THE SMALL size (40-50 g) of the Inca dove, an inhabitant of desert settlements in
the southwestern United States, imparts potential problems relating to energetics and water economy. The high diurnal water requirements, however, are readily met by the abundant fresh water afforded by its urban environment (MacMillen & Trost, 1966). In addition, and even during heat stress, the Inca dove's thermoregulatory and metabolic performances are geared to an appropriate compromise between heat production and evaporative cooling, thereby ensuring an optimal degree of water and energy balance throughout the day (MacMillen & Trost, 1967). However, at night avian behavioral limitations preclude feeding and drinking, thereby potentially exposing the birds to lengthy periods of continual energy and water drain. Birds commencing the nocturnal period in a well-fed, well-watered condition become extremely quiescent at night and decrease metabolic rates slightly, resulting in a significant decrease in body temperature with a concomitant decrease in pulmocutaneous water loss (op. dt., 1967). The nocturnal demands on water and energy balance of Inca doves would be still further accentuated during periods of inclement weather: (1) diurnal periods of excessive heat necessitating nearly continuous evaporative cooling could well leave the birds in a state of negative water balance at dusk; or (2) rainy weather and/or periods of low food supply combined with cold could result in Inca doves commencing the nocturnal period with unusually low energy reserves. *Present address: Department of Zoology, University of California, Los Angeles, California 90024, U.S.A. 243
244
RICHARD E. MACMILLEN AND CHARLES H . TROST
The circadian body temperature lability of well-fed and well-watered birds
(op. cit., 1967) suggests the possibility of still greater nocturnal depressions of body temperatures when normal food and/or water intakes are restricted. Such depressions could result in reduced energy and water expenditures, which would physiologically decrease the severity of otherwise demanding nights. This study undertakes, therefore, to explore the role of nocturnal hypothermia in the energy and water metabolism of the Inca dove. MATERIALS AND METHODS
Experimental animals The sixteen adult Inca doves employed in this study were collected in Tucson, Pima County, Arizona, between September 1964 and July 1965. The birds were shipped by air to California where, except during measurements, they were housed individually in a windowless room on a 12-hr photoperiod (lights on from 06.00 to 18.00 hr). Between periods of measurement the birds were provided in excess with tap water for drinking and mixed bird seed for food. The mean body weight of the doves after several weeks in captivity was 44-2 _+S.D. 3-1 g.
Measurements The parameters measured included simultaneous measurements in constant darkness of ambient temperature (TA), body temperature (TB), oxygen consumption and pulmocutaneous water loss. One bird was placed in each of two 1 U.S. gal metal respirometer chambers equipped with ports for the introduction and removal of air and for thermocouples. Oxygen consumption was measured with a Beckman Model E2 paramagnetic oxygen analyzer in an open air system, with a flow rate of 500 cm3/min. T A and TB were determined with copper-constantan thermocouples connected to a recording potentiometer; T B was measured by means of a thermocouple surgically implanted in the pectoral musculature. Pulmocutaneous water loss was determined gravimetrically by passing expired air through a desiccating tube containing calcium chloride. T n was controlled within + 0.5°C by placing animals in respirometer chambers inside an insulated constanttemperature cabinet. A detailed discussion of the precise methodology employed appears in an earlier study of thermoregulation and water loss in the Inca dove (MaeMillen & Trost, 1967).
Effects of food and/or water restriction To test the combined long-term effects of food and water deprivation on the parameters to be measured, two well-fed and well-watered Inca doves were placed separately in respirometer chambers at T = 20 + 0.5°C in the constant-temperature cabinet and in complete darkness at 11.00 hr. They remained under these conditions for 49 hr during which T B was measured alternately for 5-min intervals for each bird; oxygen consumption and pulmocutaneous water loss were measured simultaneously for 1-hr periods at the middle of what had previously been the
NOCTURNAL HYPOTHERMIA I N INCA DOVE
245
12-hr light and the 12-hr dark periods (measurements were made at 14.00, 22.00, 11.00, 22.00 and 11.00 hr during the 49-hr period). The birds were weighed at the beginning of the experiment and at the end; body weights during the measurements of oxygen consumption and pulmocutaneous water loss were interpolated. Well-fed and well-watered Inca doves were also placed in darkened respirometer chambers for 49-hr periods at T A = 10°C and 30°C, to test the relationship between nocturnal hypothermia and T A. TB was measured continually, and oxygen consumption was measured at the middle of what had previously been the light and dark periods. To test the effects of food deprivation and water deprivation separately, birds were deprived of either food or water for 24 hr under the usual 12-hr photoperiod, and provided with the other commodity in excess. At 12.00 hr, following the 24 hr of deprivation, and in the middle of the light period, the birds were placed in darkened respirometer chambers in the constant-temperature cabinet where they remained for an additional 24 hr at T A = 20°C. T B was recorded continually. RESULTS Body temperature
When removed from a regular 12-hr photoperiod and placed in continual darkness for 49 hr without food and water and at TA = 20°C, Inca doves exhibit a synchronous circadian body temperature lability (Fig. 1). This lability is characterized by highest T B during what had previously been the middle of the light period and lowest T B during what had previously been the middle of the dark 45
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FIG. 1. Circadian fluctuations in body temperatures of six Inca doves held in the dark for 49 hr without food and water at Ta = 20°C. Each dot represents the Ta of a single animal, and TB of each animal is represented at 30-min intervals. T h e solid horizontal bars represent the duration of the dark portion of the 12-hr photoperiod to which the animals had been subjected prior to the experiment; the spaces between the bars indicate the light portion.
246
RICHARD R. MAcMILLEN AND CHARLES H. TROST
period; the depth of nocturnal hypothermia increased progressively during the two consecutive nights of the experiment. Table 1 indicates mean T B during the middles of what had previously been the light and the dark periods throughout the 49-hr experiment. TABLE 1--MEAN
BODY TEMPERATURES OF SIX INCA DOVES TAKEN AT 1 2 - h r
INTERVALS AND
HELD IN THE DARI
12.00 1 42-7
24.00 13 38.8
12.00 25 40"6
24.00 37 35"1
12.00 49 39"8
Even when in complete darkness and tested separately, entry into hypothermia was synchronous with clock time and began about 2 hr prior to what had been the beginning of the dark period. Arousal was equally synchronous and was initiated sufficiently in advance of the start of what had been the light period that arousal was essentially complete by the time the lights would normally have gone on.
Oxygen consumption and pulmocutaneous water loss T h e rates of oxygen consumption during the 49-hr of food and water deprivation and in darkness reflect very closely the circadian cycle in TB (Fig. 2). During °' ,,,8,
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FIG. 2. Rates of oxygen consumption measured at approximately 12-hr intervals in Inca doves held in the dark for 49 hr without food and water at Ta = 20°C. The horizontal lines represent the means. Vertical lines indicate the extremes. The rectangles inclose the intervals .Y_+t0.gs S.E. The numbers represent: the numbers of birds measured at each interval (the numbers of measurements at each interval). The solid bar indicates the duration of the dark period to which the animals had been subjected prior to the experiment. the first and second nights of the experiment oxygen consumption was significantly reduced to 80 and 58 per cent, respectively, of the first midday measurement, denoting a considerable energy saving (see Table 2 for absolute diurnal and nocturnal values). T h e mean rate of oxygen consumption of the second night was significantly lower than that of the first night. T h e mean rate of oxygen consumption for each successive midday measurement was progressively but insignificantly lower.
247
N O C T U R N A L H Y P O T H E R M I A I N I N C A DOVE
Like the measurements of oxygen consumption during the 49-hr period, the rates of pulmocutaneous water loss also fluctuated directly with circadian changes in TB (Fig. 3). The first and second nights' values were reduced to 55 and 36 per IO e~ s
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cent, respectively, of the first day's value. Although not quite significantly lower than the first night's rate of water loss, the second night's rate was significantly lower than any of the midday values (see Table 2 for absolute diurnal and nocturnal values).
Relationship between nocturnal hypothermia, T B and body weight The depth of nocturnal hypothermia was directly related to changes in body weight experienced prior to commencing an experiment. Figure 4 indicates the 45 40
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FIG. 4. T h e courses of body temperatures of seven Inca doves previously kept for varying lengths of time without food and water, and then held in continuous darkness at T a = 20°C. T h e numbers represent the interpolated body weights of individual birds (expressed as per cent of original body weight since last in a wellfed, well-watered state) when the level of deepest nocturnal hypothermia was attained. T h e solid bar indicates the duration of the dark period of the previous 12-hr photoperiod.
248
RICHARD E. MACMILLEN AND CHARLES H. TROST
courses of TB at T A = 20°C in seven representative Inca doves with various weight histories prior to the experimental routine: some were allowed to commence the 24-hr experiment in a well-fed and well-watered condition, while others had been deprived of food and water for varying lengths of time (up to 24 hr) prior to the experiment. It is clear that the depth of nocturnal hypothermia is directly related to the amount of body weight lost since last in a well-fed and well-watered state. In addition, successful spontaneous arousal, at least at T A = 20°C, appears to be limited to those birds experiencing no more than about 15 per cent loss in weight from the well-fed, well-watered state (Fig. 4). The lowest T B achieved with what would have been an ensuing successful arousal if food, water and light had been available was 28.5°C in a bird whose interpolated body weight in the midpoint of hypothermia was 85 per cent of its well-fed, well-watered weight. This bird aroused to a TB of 35°C at 06.00 hr (previously the beginning of its photoperiod), but then, with darkness continuing, entered a deep hypothermia with TB reaching a low of 25.5°C at 12.00 hr. Both this bird and another, which failed to arouse and which ultimately reached a T B of 22°C, were incapable of spontaneous arousal at T A = 20°C, even when shaken vigorously. However, when removed from the experimental situation and placed under heat lamps, both birds recovered fully and, after eating and drinking, were capable of normal thermoregulation. One bird, which had lost nearly 20 per cent of its initial well-fed, well-watered weight in the midpoint of hypothermia, entered hypothermia at an extremely fast rate and ultimately died. In Fig. 5 is shown the relationship between the depth of nocturnal hypothermia and the interpolated body weight of the bird at the time of achieving its lowest TB. As indicated in this figure, nocturnal hypothermia can be induced by either prior I~
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FIO. 5, The relationship between weight lost since las~ in a well-fed and/or wellwatered state and the low TB attained during nocturnal hypothermia at T A = 20°C. The solid circles represent birds experiencing prior food deprivation and prior food and water deprivation; hollow circles represent birds experiencing prior water deprivation. food restriction, prior food and water restriction, or prior water restriction; all restrictions result in weight loss and produce hypothermia, the depth of which is directly related to weight loss. In mourning doves MacMillen (1962) has suggested that water deprivation results in cessation of feeding, and Schmid (1965) indicates
NOCTURNALHYPOTI-IEI~IIAIN INCADOVE
249
that wetting of crop contents was necessary to initiate digestion. A similar situation most likely occurs in the very water-dependent Inca doves, and it is presumed that much of the weight loss resulting from water deprivation is indirectly a result of the inability to process foods. Thus, nocturnal hypothermia resulting from food and/or water restriction very likely is a response to the same stimulus, i.e. weight loss due to energy drain. Because of this likelihood all of the data in Fig. 5 are considered as results of the same phenomenon, and have together been analyzed by the method of least squares; the equation derived from this analysis and predicting this relationship is: y = - 28.16 + 0.70x, where y is the low T B attained during nocturnal hypothermia and x is the interpolated relative body weight when that T B was attained. Relationship between nocturnal hypothermia and T a To test the relationship between the depth of nocturnal hypothermia and TA, initially well-fed and well-watered Inca doves were placed for 49 hr in darkened respirometer chambers at T A = 10 °, 20 ° and 30°C. Figure 6 indicates this relationship, and shows that nocturnal hypothermia at T A = 10 ° and 20°C tends to be I-: IOO De
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much deeper per loss in body weight than at TA = 30°C. These data lend themselves to analysis of covariance which reveals that the relationship between the depth of nocturnal hypothermia and weight loss is not significantly different at TA = 10°C and 20°C, while, at T a = 30°C, the relationship is significantly different to that at the other two Tjs. The equations describing these relationships at the three temperatures and derived by the method of least squares is as follows: TA = 10°C: y = -19.42+0.59x, TA = 20°C: y = -11-37+0.52x, TA = 30°C: y = -20.31+0.19x, where y is the low T B and x is the interpolated body weight at the time of that T B.
250
RICHARD E. MACMILLEN AND CHARLES H. TROST
A l t h o u g h t h e d e p t h o f n o c t u r n a l h y p o t h e r m i a a p p e a r s to b e i n d e p e n d e n t o f TA, at least at l o w t e m p e r a t u r e s , t h e rates o f o x y g e n c o n s u m p t i o n , w h e t h e r n o r m o t h e r m i c o r h y p o t h e r m i c , are v e r y d e p e n d e n t u p o n T,a ( F i g . 7). A n a l y s i s of c o v a r i a n c e 5 t
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reveals that the slopes of oxygen consumption at T A = 10 °, 20 ° and 30°C arc all highly significantly different. T h e s e slopes of oxygen consumption are described by the following equations derived by the method of least squares: TA = 10°C: TA = 20°C: T~ = 30°C:
y = -2-57+0.15x, y = -2.67+0.13x, y = -5.85+0-19x,
where y represents the rate of oxygen consumption and x is the T B at that rate. TABLE 2--MEAN
B O D Y T E M P E R A T U R E S , RATES O F O X Y G E N C O N S U M P T I O N A N D P U L M O C U T A N E O U S
W A T E R LOSS MEASURED A T VARIOUS I N T E R V A L S T H R O U G H O U T A 20 ° AND
Time, hr 14.00 Hour of experiment 3 Body temperatures, °C T a = 10°C 40.9 (4) T A = 20°C 41.4 (5) T A = 30°C 40.9 (4) Oxygen consumption, (cm3/g)/hr T~ = 10°C 3-3 (8) T A = 20°C 2-6 (10) T A = 30°C 1"8 (8) Pulmocutaneous water loss, % body wt/day T a = 10°C 5'0 (4) T A = 20°C 6-9 (4) T a = 30°C 8-2 (4)
49-hr
P E R I O D , A N D A T T A = 1 0 °,
30°C* 22.00 11
11.00 24
22.00 35
11.00 48
37.4 (5) 38.2 (9) 38.8 (5)
40.5 (5) 40.9 (9) 40.6 (5)
33.0 (2) 34.0 (9) 36.6 (5)
38.5 (2) 38.9 (8) 39.2 (5)
2.9 (10) 2.0 (18) 1'5 (10)
3.6 (10) 2.5 (18) 1"6 (10)
2-6 (8) 1.5 (18) 1'0 (10)
3.4 (4) 2.4 (16) l-5 (10)
3"4 (5) 3"8 (9) 5'9 (5)
5-9 (5) 5-2 (9) 6"4 (5)
3'2 (4) 2"5 (9) 4"1 (5)
4.3 (2) 4'8 (7) 5"6 (5)
* T h e numbers in parentheses represent the number o f birds measured except for measurements of oxygen consumption, where the numbers in parentheses represent the numbers of oxygen consumption measurements (two measurements on each bird).
N O C T U R N A L H Y P O T H E R M I A I N I N C A DOVE
251
In Table 2 are indicated mean TB and rates of oxygen consumption and pulmocutaneous water loss as measured for all Inca doves at TA = 10 °, 20 ° and 30°C, and at approximately 12-hr intervals throughout the 49-hr period. DISCUSSION It was previously demonstrated that Inca doves characteristically become hyperthermic in response to diurnal heat stress, occasionally undergoing an increase in T B to as high as 47°C without apparent harm (MacMillen & Trost, 1967). The present study, in addition, indicates that the same birds may, under certain circumstances, experience a decrease in TB during the night to as low as 30°C. Thus, while considered homeothermic and with good physiological control of thermoregulation, Inca doves may on occasion exhibit circadian body temperature fluctuations which are at least of equal magnitude to those of poikilotherms living in the same area and which are dependent primarily upon behavioral control. While the value of diurnal hyperthermia is primarily that of water conservation, nocturnal hypothermia results both in energy andwater conservation, the amounts depending upon the depth of hypothermia (Figs. 1, 2 and 3). Although hypothermia can be induced either by food and/or water restriction (Fig. 5), it is believed that the ultimate response is due to drain of energy reserves, since it is unlikely that doves can mechanically process food in the crop without access to drinking water. Such an energy drain, as well as continual water expenditure, results in loss of body weight during the night, producing nocturnal hypothermia, the depth of which is directly related to the amount of weight lost since last in a well-fed and well-watered state (Fig. 4). Most birds known to employ hypothermia, either nocturnally or seasonally, have T~s while hypothermic which vary by only 1° to 3°C from T~ (Pearson, 1960). Such is not the condition in Inca doves where nocturnal T B is largely independent of Ta, and appears to be dictated by nutritional state (Fig. 4). Thus we hesitate to apply the term 'torpor' to hypothermic Inca doves, as this term is best applicable when TB fluctuates with T A (MacMillen, 1965). Rather, the phenomenon in Inca doves appears to be an exaggeration of the usual nocturnal decrease in Ts so characteristic of diurnal birds (see King & Farner, 1960, for extensive discussion). That the depth of nocturnal hypothermia is dictated more directly by nutritional state than by T a, at least at TA < 30°C, is indicated in Fig. 6. However, the nocturnal energy drain of hypothermic birds is directly related to T A (Fig. 7), so that birds starting the night with similar energy levels will become more profoundly hypothermic under conditions of lower T A. Even in the absence of external clues, the T B fluctuations of Inca doves tested independently maintains a strict circadian periodicity, reflecting closely the temporal aspects of the photoperiod to which they previously had been subjected (Fig. 1). Such precise endogenous control, doubtless entrained by seasonal changes in photoperiod, ensures that birds will be fully aroused and alert by dawn, not susceptible to predation, and ready to replenish energy and water expended during
252
RICHARD E. MAcMILLEN AND CHARLES H . TROST
the night. However, only those birds which had lost no more than 15 per cent of the well-fed, well-watered weight were able to arouse spontaneously. Thus birds failing to arouse ultimately developed TB close to T A and were incapable of endogenous control of thermoregulation. However, under natural circumstances in the desert, even these birds most likely would be subjected to postdawn solar warming. Such warming, as in the application of external heat in the laboratory, could result in full arousal and, if the birds could then find food and water, would yield an additional opportunity for survival. The incidence of nocturnal hypothermia in non-captive Inca doves is unknown, however field and laboratory observations suggest that nocturnal depressions of more than 2-3°C are not nightly occurrences. At 01.00 hr on the morning of 29 January 1966 in Tucson, Arizona, and with T A = 8°C many Inca doves were observed roosting in trees. They generally roosted 10-12 ft above the ground, in groups of three to five birds sleeping with bodies pressed tightly together. Such huddling behavior would yield a more favorable surface-volume relationship, thereby minimizing heat loss and energy drain. When disturbed the birds were quite capable of coordinated movement, indicating high T B. A singly roosting Inca dove, found within reach, had a cloacal TB, 15 sec after capture, of 39-7°C, well within the typical well-fed, well-watered nocturnal range (see Fig. 1). Thus profound nocturnal hypothermia, previously unreported in Columbiformes, appears in the Inca dove to be largely an emergency device which is always on hand to be called upon, and to whatever degree circumstances demand. The occurrence and the characteristics of this hypothermia reflect very closely the store of energy and/or water reserves, and therefore ensure minimal expenditures when these commodities are in least supply. Steen (1958) has reported an apparently similar occurrence of nocturnal hypothermia in six species of small, newly captured Norwegian Passeriformes during cold winter nights. Steen's observations, together with these on the Inca dove, suggest that nocturnal hypothermia, rather than being confined to a few insectivorous or nectar-feeding birds, may be a quite common aspect of the physiological repertoire of small birds in general, during periods of stress. SUMMARY When removed from a 12-hr photoperiod to continuous darkness at TA = 20°C and without food and water, Inca doves experience circadian fluctuations in rib which reflect very closely the temporal aspects of the previous photoperiod. The fluctuations consist of high diurnal T B alternating with nocturnal hypothermia whose depth increases progressively on consecutive nights. Although nocturnal hypothermia can be induced by either food and/or water restriction, its depth appears to be largely dictated by energy level and is independent of T A. The lowest T B routinely observed during nocturnal hypothermia was 30°C, occurring at a weight of approximately 85 per cent of the well-fed, well-watered state. Below 85 per cent, birds become extremely hypothermic and lose endogenous control of thermoregulation.
NOCTURNAL H Y P O T H E R M I A I N INCA DOVE
253
Nocturnal hypothermia results in considerable saving in both energy and water, the magnitude depending u p o n depth of hypothermia. I t is herein looked u p o n as an emergency device enhancing survival through ~ h a t otherwise would be physiologically demanding nights and while operating on low energy and water budgets.
Acknowledgements--This investigation was supported by National Science Foundation Grant GB-2459. We are grateful to Dr. L. H. Blankenship, Mr. J. C. Truett and Mr. G. L. Richardson of the Cooperative Wildlife Unit, University of Arizona, for aid in obtaining birds. In addition we are most appreciative of aid and advice received in statistical treatment of some of the data from Dr. D. L. Bentley and Mr. J. J. Crowley, Department of Mathematics, Pomona College, who were supported in part by National Institutes of Health Grant 2G-945. REFERENCES KING J. R. & EARNERD. S. (1960) Energy metabolism, thermoregulation and body temperature. In Biology and Comparative Physiology of Birds (Edited by MARSHALL A. J.) Vol. 2, pp. 215-288. Academic Press, New York. MAcMILLEN R. E. (1962) The minimum water requirements of mourning doves. Condor 64, 165-166. MAcMILLEN R. E. (1965) Aestivation in the cactus mouse, Peromyscus eremicus. Comp. Biochem. Physiol. 16, 227-24-8. MACMILLEN R. E. & TROST C. H. (1966) Water economy and salt balance in white-winged and Inca doves. Auk 83, 441456. MAcMILLEN R. E. & TROST C. H. (1967) Thermoregulation and water loss in the Inca dove. Comp. Biochem. Physiol. 20, 263-273. PEARSON O. P. (1960) Torpidity in birds. Bull. Mus. comp. Zool. Harv. 124, 93-103. SCHMIDW. D. (1965) Energy intake of the mourning dove, Zenaidura macroura marginella. Science, N . Y . 150, 1171-1172. STUN J. (1958) Climatic adaptation in some small northern birds. Ecology 39, 625-629.