Circadian rhythms in body temperature of the pigtailed macaque (Macaca nemestrina) exposed to different ambient temperatures.код для вставкиСкачать
American Journal of Primatology 9:l-13 (1985) Circadian Rhythms in Body Temperature of the Pigtailed Macaque (Macaca nernestrina) Exposed to Different Ambient Temperatures ELLEN C. WURSTER, DAVID E. MURRISH, AND FRANK M. SULZMAN Department of Biological Sciences, University Center at Binghamtoq State University of New York, Binghamton The body and leg skin temperatures of five pigtailed macaques (Macaca nemestrina) were measured at various ambient air temperatures ranging from 22 to 32°C over 24-h periods. The rhythm in core body temperature persisted in all ambient air temperatures, and the rhythm in leg skin temperature was suppressed a t the higher and lower ambient temperatures. This suggests that at the upper and lower regions of the thermoneutral zone, either a rhythm in heat production or a heat loss rhythm other than leg skin temperature is regulating the core body temperature rhythm. It was also found that the mean colonic temperature increased linearly with a n increase in ambient temperature and that a phase relationship existed between ambient temperature and colonic temperature. In addition, as the ambient temperature increased, additional sites along the distal portion of the leg were recruited for vasomotor heat loss. Key words: thermoregulation, Mucucu nemestrina, skin temperature, pigtailed macaque INTRODUCTION Homeotherms maintain a relatively constant core body temperature despite wide changes in the environmental temperature. This thermal balance is achieved by adjusting heat loss and heat production. Vasomotor heat loss is the primary avenue for regulating body temperature within a certain range of ambient air temperatures known as the thermoneutral zone. Below this range, metabolic heat production increases to offset increased heat loss. Above the thermoneutral zone, heat loss is achieved by evaporative means. While core body temperature is carefully regulated, it is not constant. Instead it exhibits a prominent daily variation. Aschoff et a1  found that within the thermoneutral zone the 24-h rhythm in deep body temperature of humans was mainly due to a rhythm in heat loss. These authors showed that the distal regions of the extremities were actively involved in heat loss and showed a rhythm in skin Received August 18, 1984; revision accepted March 26,1985. Address reprint requests to F.M. Sulzman, Department of Biological Sciences, University Center at Binghamton, SUNY, Binghamton, NY 13901. 0 1985 Alan R. Liss, Inc. 2 I Wurster, Murrish, and Sulzman temperature and conductance that were the inverse of the body temperature rhythm. Heat loss through the skin of the hands and feet was minimal during the day but began increasing several hours before subjective night and decreasing shortly after the onset of sleep. At ambient air temperatures above and below the thermoneutral zone, the rhythm in heat loss was suppressed owing to vasodilation or vasconstriction, but the body temperature rhythm persisted [Aschoff et al, 19741. Presumably, the rhythm in metabolism plays the major role in generating the body temperature rhythm below the thermoneutral zone. Nonhuman primates also exhibit a day-night rhythm in body temperature. The squirrel monkey Saimiri sciureus shows a persisting colonic temperature rhythm in various lighting conditions and intensities [Sulzman et al, 19791. The tail is the major site for regulating heat loss in the ambient temperature range of 25-30°C [Stitt & Hardy, 19711, and there is a prominent rhythm in tail skin temperature [Fuller et al, 19791 a t these ambient temperatures. These authors showed that the tail skin temperature was low during the day, increased several hours before lights off, and returned to daytime values during the night. Core body temperature and tail temperature rhythms in a light-dark cycle of 12 h of light and 12 h of dark (LD 12:12) exhibited a tight coupling, and there existed a stable phase relationship between the two rhythms. In constant light, the average period was similar for the two temperatures, but there was a tendency for the rhythms to become uncoupled, suggesting the presence of more than one oscillator in the thermoregulatory timing system. Fuller [ 19841 measured the rhythms in colonic and hypothalamic temperatures of the squirrel monkey at four different ambient temperatures. Although the range of the waveforms was altered, the rhythms persisted at all ambient temperatures. The timing of the waveform was not altered by the changing ambient temperature, suggesting that in these monkeys the environmental temperature does not play a major role in regulating the body temperature rhythm. Sickles et a1 [unpublished data] found an inverse relationship between core temperature and ankle skin temperature rhythms of pigtailed macaques (Macaca nemestrina) in cycles of LD 12:12, LD 1623, and constant light (LL). This suggests that, as Aschoff found in humans, these animals may use their limbs as a regulatory mechanism for the deep body temperature rhythm. To examine the control of the body temperature rhythm in M. nemestrina, we exposed these monkeys to ambient air temperatures ranging from 22 to 32°C and recorded the rhythm in deep body temperature. Skin temperatures at sites along the leg were also measured to determine how the lower extremities are used in regulating the body temperature rhythm in response to varying heat loads placed on the body. METHODS AND MATERIALS Five male pigtailed macaques (Macaca nemestrina) were used. They were juveniles (2-4 yr old) weighing between 4 and 7 kg. The macaques were housed individually in cages in a common room with a n air temperature between 25 and 26°C. Lighting was maintained on a light-dark cycle of 16 h of light and 8 h of dark (LD 16231, with lights on a t 0800 h EST, circadian time (CT) 0, and lights off at 2400 h EST (CT 16). The light intensity was kept a t 600 lux during the light period and 0 lux during the dark period. Monkey chow biscuits, fruit, and water were provided twice daily, and animals were able to feed and drink ad libitum. Body and skin temperatures were measured at ambient temperatures of 22,24, 26, 28, 30, and 32°C. Only four animals were measured at 22 and 32°C. The experiments took place in a walk-in environmental chamber with the ambient Circadian Rhythm of Body Temperature / 3 temperature maintained a t 0.1"C. The light-dark cycle and the illumination were the same a s in the colony housing room. Typically, a n experiment lasted 3 days. A monkey was instrumented in the afternoon of the first day. Data collection began at CT 0 with lights on on the second day and stopped a t CT 24 on the third day, whereupon the monkey was returned to the colony housing room. The monkey was not involved in experiments for a t least a week or more. Skin temperatures were measured at five sites on the leg: toe, foot, ankle, calf, and thigh, using 26-gauge copper-constantan thermocouples. Each thermocouple was attached with surgical tape. The foot thermocouple was attached on the back of the foot between the digit bones. The colonic temperature was measured using a thermocouple inserted approximately 8 cm into the monkey's rectum. The end of the probe was taped to the monkey's tail to prevent expulsion during defecation. The animal also wore a short-sleeved mesh jacket. Handling of monkeys was facilitated by a n injection of ketamine (20 mgkg). The effects lasted between 3 and 4 h. The drug was used only on the first day for instrumenting the monkey and a t the end of the experiment. The monkey was placed in a specially designed restraint chair after attachment of the thermocouples. All monkeys were previously trained to tolerate the chair for prolonged periods. While in the restraint chair, food and water were available ad libitum and fruit was given three times daily. We do not feel that these procedures produce artifacts in the temperature patterns because 1) our animals were extensively trained to tolerate chair restraint before experiments were begun, 2) ketamine is rapidly cleared from the body, and 3) we do not use data until the beginning of the second day in the chair. Further, in experiments with monkeys in restraint chairs [Sulzman e t al, unpublished data], we have observed that after the first 4-6 h in the restraint chair, the rhythms of rest-activity, body temperature, and various skin temperatures are stable for more than a week. Finally, we have done experiments in which the temperatures of monkeys were measured in restraint chairs when ketamine was not used during animal handling. The temperature patterns were the same in both groups. The calibrated thermocouple leads were connected to a ten-channel multiplexer (Omega). Each channel recorded on a strip chart recorder for 20 sec at 3-min intervals. Ambient temperature and light, measured by a light sensor, were also indicated on the recorder. The temperature data were transcribed from the strip chart paper using an Apple computer digitizer. Data points were recorded every 30 min from the 24 h of data, resulting in a total of 48 points per measurement site. Editing and plotting of data was done using a n Apple II+ microcomputer. Standard statistical methods [Snedecor & Cochran, 19671 were used in analyzing the data. An average waveform using temperature data from each monkey was determined. An average waveform consisting of 48 points was obtained by calculating the mean of all temperatures for each 30 min. For example, using the thigh skin temperature of each monkey a t 0800 h, a n average thigh skin temperature for 0800 h was determined. This was done for each 30-min reading, producing a 24 h average waveform for the thigh skin temperature. RESULTS A prominent day-night difference in body temperature was evident in the colonic temperature of monkeys at a n ambient temperature of 26°C (Fig. 1). The decline in body temperature began approximately 4 h before lights off (CT 16 h), and body temperature began to increase 1 h before lights on (CT 24 or 0 h). Colonic tempera- 4 I Wurster, Murrish, and Sulzman 40 3 Y g 39 W + 0 z i 38 20 0 37 36 1 0 8 16 24 CIRCADIAN TIME (HR) Fig. 1. Colonic temperature of one pigtailed macaque for a 24-h period at an ambient air temperature of 26°C. The light-dark cycle is indicated at the top of the figure. Lights on at circadian time (CT) 0 h and lights off at CT 16 h. ture leveled off at a stable daytime level around CT 1.5 h. The difference between the average day and average night body temperatures was about 1.3"C. The average body temperature pattern of the five monkeys at each experimental air temperature is shown in Figure 2. Clear day-night differences in colonic temperatures can be seen a t all ambient temperatures. The average range of the waveform a t each temperature was approximately 1.9"C (see Table I). Although there was little change in the range, as the ambient temperature increased, the daily mean colonic temperature increased. Figure 3 represents the overall 24-h mean for colonic temperature a t each ambient temperature. The correlation coefficient (r) for the regression line of the colonic temperatures in Figure 3 was 0.89, and the r value for the line from just 24°C to 30°C was 0.99. Since ? indicates the proportion of the variance in the sample that is due to correlation between the variables, this value was calculated as a further measure of the influence of ambient temperature on body temperature. Estimates of r2 indicated that 95% of the variance was due to a linear increase in mean body temperature a t air temperatures from 24°C to 30°C and that 75% of the variance was due to a linear increase for all the ambient temperatures. The phase of colonic temperatures appeared to shift with the LD cycle a t the different environmental temperatures (Fig. 2). The estimated time of day a t which body temperature began to decrease to nighttime levels differed with changes in the ambient temperature (Fig. 4).This time was estimated by the intersection of one line drawn through the plateau of the stable daytime temperature and another line through the decreasing temperature region. The decrease to night body temperature began earliest at 32°C and latest 22"C, with the time of the initial decrease beginning later in the day with each 2°C drop in the ambient temperature. An estimate of r2 indicated that in Figure 4,83% of the variance was due to a linear decrease, and a t-test showed that the slope of the line was significantly different from zero (P < 0.01). There also appeared to be a phase delay at 32°C and a phase advance a t 22°C in the time of day that body temperature began to increase. Circadian Rhythm of Body Temperature / 5 39 0 B E 380 s 37- 3d 1 I 40, I $1 30c c I 36- 40 39 40 i 0 6 12 CIRCADIAN TIME (HR) 18 4 Fig. 2. The average waveform of colonic temperature at six ambient temperatures. Each point represents the average standard error of the body temperature of the monkeys at each half-hour measurement. TABLE I. Mean Maximum and Mean Minimum Colonic Temperatures +_ SE and the Range of the Waveform at Six Ambient Temperatures Ambient temperature ("C) 32 30 28 26 24 22 Maximum colonic temperature ("C) Minimum colonic temperature ("C) Range 38.9 k 0.6 39.0 0.3 38.4 +_ 0.4 38.4 t 0.4 38.0 k 0.4 38.3 k 0.2 37.0 k 0.7 37.0 0.5 36.5 t 0.3 36.4 k 0.3 36.3 k 0.3 36.2 k 0.1 1.7 2.0 1.9 2.0 1.7 2.1 AMBIENT TEMP ( C ) Fig. 4. The time of day when the core body temperature of the pigtailed macaques began to decline to nighttime levels at each of the six ambient temperatures. Skin temperatures were measured at various sites on the leg to evaluate the role of the extremities in the alteration of the body temperature rhythm at different ambient temperatures. The colonic, thigh, foot, and ambient temperatures of a representative monkey at 26°C are shown in Figure 5. Although the means differ, the waveforms of the core and thigh are very similar. Both showed an increase in temperature about lights on, a high temperature during the day, a decrease in Circadian Rhythm of Body Temperature / 7 40 0 co 35 TH Y n W 30 I- Fo AM 25 20 0 8 16 24 CIRCADIAN TIME (HR) Fig. 5. The waveforms of the colonic (Co), thigh (TH), and foot (Fo) temperatures of a representative pigtailed monkey at an ambient (AM)temperature of 26°C. TABLE 11. A Comparison of the Mean Skin Temperaturesof Different Sites Along the Legs of Monkeys at an Ambient Temperature of 26°C Site Toe Foot Ankle Calf Thigh Morning 0-8 h 26.8 29.7 31.8 33.5 34.7 f 0.2 f 0.3 f 0.3 f 0.2 * 0.1 Afternoon 8-16 h 27.3 f 0.3 31.0 + 0.3 32.7 f 0.1 33.7 f 0.1 34.8 0.1 * Night 16-24 h 28.1 31.1 32.1 33.2 33.8 f 0.2 f 0.1 f 0.1 f 0.1 & 0.1 Significance (P<O.Ol) N>M N>M; A>M A>M"; A > N A>M; A > N M>A; A > N The 24-h day, beginning at lights on at circadian time 0, was divided into three 8-h sections: morning, afternoon, and night. The last column indicates those values found to be significantly greater (P<O.Ol)by Student's t-test. *P < 0.05. temperature several hours before lights off, and low values at night. In contrast, the waveform of foot skin temperature of this monkey is the inverse of that of the thigh and core. Foot temperature was low throughout the day and began to rise before lights off and approximately a t the time colonic and thigh temperatures began to fall. Higher foot temperatures were measured at night, which then slowly fell to daytime values. The skin temperatures of the thigh and foot of all five monkeys a t three ambient air temperatures are shown in Figure 6. The mean skin temperature of the foot increased markedly as ambient temperature was raised. At 32 and 22"C, there was little day-night difference in the skin temperatures were not significantly different (P < 0.05). At 26°C there was a day-night difference with lower daytime values during the first few hours of light. The mean skin temperatures of each site along the leg at a n ambient temperature of 26°C for three time periods during the circadian day were calculated (Table 11).The toe skin temperature during the night was significantly higher than in the morning. The temperature of the foot a t night and in the afternoon was significantly higher than in the morning. The afternoon 8 I Wurster, Murrish, and Sulzman 37 h 0 34- 0 6 12 18 24 CIRCADIAN TIME (HR) Fig. 6. The average waveforms of the foot skin temperature (upper panel) and the thigh skin temperature (lower panel) at an ambient air temperature of 32,26, and 22°C. ankle and calf temperatures were each significantly greater than both the morning and night temperatures. Both the morning and afternoon thigh temperatures were significantly greater than the night temperature. In Figure 6, the thigh showed a n elevation in skin temperature as the ambient temperature increased. There was a day-night difference with high daytime values and lower nighttime values a t all temperatures. Skin temperatures of the leg showed a direct correlation with ambient temperature. Because of the large individual variation in skin temperatures at the different sites, it is difficult to compare the contribution of each site to the heat budget of the monkeys. However, if one calculates the ratio of core temperature minus mean skin temperature to core temperature minus ambient temperature, one derives a number between 0 and 1which reflects cutaneous vasoconstriction. As the ratio approaches 1, the site is more vasoconstricted, and as it approaches 0, the site is more vasodilated. Figure 7 shows the vasoconstriction ratio for each site a t a given ambient temperature. At all temperatures the ratio for the thigh and calf remained between 0.2 and 0.4,indicating little participation in temperature regulation. For other sites along the leg, as the ambient temperature increased, the temperature became closer to 0, showing that these sites were being recruited for heat dissipation. At 30°C, the upper end of the thermoneutral zone of the pigtailed macaque, the thigh and calf were the warmest, the ankle and foot were almost as warm, and the toe was cooler. Circadian Rhythm of Body Temperature / 9 1.o - 0 I- U a z 0 a 0 II- v) z 0 0 0 v) a > 0.0 22 24 AMBIENT 26 2a 30 32 TEMPERATURE Fig. 7. The vasoconstriction ratio (TB-TOB-TA) of various sites on the legs of five pigtailed macaques maintained at different ambient temperatures. The vasomotor state is represented by this ratio, with the value 1 indicating maximal vasoconstriction and 0 indicating maximal vasodilation. This indicates that the foot and ankle were vasodilated and actively participating in heat dissipation. At 32"C, the vasoconstriction ratios for all sites on the leg were low and approximately the same, indicating that the leg was maximally involved in vasomotor heat loss. At the lower end of the thermoneutral zone, heat must be conserved by minimizing the gradient between ambient temperature and skin temperature. The high ratios for the toe, foot, and ankle at 22°C indicated that these sites were vasoconstricted and being used for heat conservation. DISCUSSION The core body temperature of pigtailed macaques showed a clear day-night difference a t six different ambient temperatures. The range of this rhythm was similar a t the different ambient temperatures, but the maximum and minimum body temperatures and the 24-h mean colonic temperatures increased as the environmental temperature increased. It is possible that as the heat load placed on the animal changed, the set point for the maximum and minimum values also changed, but the range of oscillation of the body temperature rhythm was regulated at a relatively constant value. The observation of a relatively constant range of pigtailed macaque body temperature rhythm differs from the results of two other studies with primates, in which the body temperature rhythm was monitored at different ambient temperatures. Fuller found that the nighttime minimum body temperature of squirrel monkeys was altered significantly by changes in the ambient temperature. However, in contrast to the macaques in the present study, the daytime maximum did not change as much, and the range was inversely related to ambient 10 I Wurster, Murrish, and Sulzman temperature. The range of oscillation of the rectal temperature rhythm of humans has also been shown to depend on the ambient temperature [Aschoff & Pohl, 19701. The range was greatest a t 24°C and smallest a t 20°C and 32°C. The significance of these three different types of regulation is unclear. Ambient temperature also had a n effect on the phase angle relationship between colonic temperature and the light-dark cycle of pigtailed macaques. As the ambient temperature was increased, the time of day when body temperature began decreasing occurred earlier (Fig. 4). In contrast, the phase relationships of both the hypothalamic and colonic temperatures of squirrel monkeys to the light-dark cycle were not altered by changing ambient temperatures [Fuller, 19841. The light-dark cycle of the present study was LD 1623, whereas with squirrel monkeys it was LD 12:12. Although a n LD 12:12 cycle might be more natural for macaques, the timing of the body temperature decrease could be masked by lights off. Masking is defined as any alteration of a n observed rhythm by a n environmental factor without affecting its underlying oscillator. Fuller et a1  found that in a n LD 2:2 cycle, the body temperature rhythm increased to daytime values whenever lights came on, suggesting a masking effect of the light-dark cycle. The waveform of the body temperature rhythm of the pigtailed macaques was similar in a n LD 1 6 3 cycle, LD 12:12 cycle, and in constant light conditions [Sickles et al, unpublished data]. Because body temperature began to decrease several hours before lights off, masking effects of the LD cycle are reduced in a n LD 16:8 cycle, and the phase effect of other environmental factors can be evaluated. The shift in the phase of the body temperature rhythm with changing ambient temperature (Fig. 2) indicates that ambient temperature plays a role in the entrainment mechanism of the circadian timing system. In fact, Aschoff  found that the activity rhythm of M. nemestrina could be entrained by a n ambient temperature cycle. Aschoff and Heise  concluded that in humans the core temperature rhythm is regulated primarily by a rhythm in heat loss. From studies on conductance and skin temperature of the extremities, they showed that rhythm in heat loss accounts for about 75% of the regulation of the rhythm in core temperature and that heat production is involved in only 25% of the regulation. In humans, as well as in other primates, the extremities are the major site for vasomotor heat loss. The skin temperature of the distal regions of the arm and legs in humans have a waveform that is the inverse of that of the colonic temperature waveform, whereas the proximal regions have a waveform similar to the colonic temperature [Aschoff & Heise, 19721. In the present study, the skin temperatures at sites along the leg were measured to evaluate their role in regulating the deep body temperature rhythm. The leg was chosen for technical reasons, but since the arms and legs of humans showed similar temperature patterns [Grant & Pearson, 19381, the results on the leg in this study can probably be applied to the arm as well. Analysis of the waveforms of the skin temperature rhythm of pigtailed macaques showed only a minor role for the limb in regulating the rhythm of deep body temperature at low ambient temperatures. Skin temperature waveform patterns of the thigh and foot were inversely related a t 26°C. The thigh followed the rhythm in core temperature (higher in the day than at night; Table 11), and the foot showed an inverse pattern with morning being the lowest temperature (Table ID. At the temperature extremes, the range of the core temperature rhythm was relatively unaltered, but no rhythm could be discerned for either the thigh or the foot skin temperature. At low ambient temperatures the leg is not involved in generating the rhythm in body temperature. However, a t high ambient temperatures the absence of a skin temperature rhythm does not necessarily mean Circadian Rhythm of Body Temperature / 11 that the leg is not involved in regulating the core temperature rhythm. It is known that in humans in warm temperatures there can be alterations in blood flow [Cooper et al, 1949; Felder et al, 19541 and heat flow [Hertzman, 19531 without changes in skin temperature. Although skin temperature patterns suggest that the leg plays a minor role and because heat and blood flow were not measured in this study, we cannot completely evaluate the role of the leg a t high ambient temperatures. The rhythm in body temperature of the macaque could also be regulated by vasomotor heat loss at other sites of the body. Baker et a1  found that certain regions of the head of Macaca nemestrina showed increased skin temperatures upon arousal and that the distal extremities showed a decrease in skin temperature. It is not known what role the face and head play in regulating the body temperature rhythm in these animals. Respiratory heat loss could also be involved, but no studies have evaluated its role in regulating the body temperature rhythm. Alternatively, a rhythm in heat production may play a more major role in generating the core temperature rhythm in the macaque. Humans in temporal isolation can show internal desynchronization, with the activity and colonic rhythms free running at different periods [Wever, 1979; Czeisler et al, 19801. If the rest-activity rhythm is similar to the rhythm in metabolic heat production, then this observation is consistent with the conclusions of Aschoff and Heise  that the rhythm in heat loss is the primary cause of the colonic temperature rhythm in humans. To date, no spontaneous desynchronization between these two rhythms has been shown to occur in monkeys [Sulzman, et al, 19791. However, the core body and tail skin temperature rhythms of squirrel monkeys do have a tendency to uncouple in constant light [Fuller et al, 19791. Fuller et a1  found that in squirrel monkeys with the suprachiasmatic nuclei (SCN) removed, the activity rhythm ceased but the colonic rhythm persisted (although it was not as regular a s when the SCN were intact). This suggests that although the core temperature rhythm is normally tightly coupled to the activity rhythm, a second oscillator may be timing the rhythm after the removal of the SCN. Additionally, a recent study on Macaca nemestrina by Sickles et a1 [unpublished data] found that in constant light, activity and colonic temperature were tightly synchronized with one another. The synchrony between activity and core temperature rhythms in nonhuman primates suggests that metabolic rate and therefore heat production (as indicated by the activity pattern) may play a larger role in regulation of body temperature than they do in humans. To determine whether another major site is involved in heat loss, or if heat production is regulating the deep body temperature rhythm, more measurements need to be made, especially those of oxygen consumption, to evaluate the extent to which metabolism is involved in the body temperature rhythm. The use of different portions of the leg for heat dissipation or heat conservation with changes in the ambient temperature was estimated by a ratio which reflects vasomotor activity. The thigh and calf temperatures were found to have approximately the same ratio of all ambient temperatures. This indicates that for macaques, like humans [Aschoff & Pohl, 19701, the thigh and calf follow the core temperature and are not active heat dissipators. Compared to the lower extremities, the thigh and calf have a low surface area to volume ratio, suggesting that they are not as effective heat dissipators as the distal regions of the leg. The ankle, foot, and toe play the largest role in heat loss in the leg as seen by the decrease in the vasoconstriction ratio. As the ambient temperature increased, each site was progressively recruited. At 28°C the ankle was recruited for heat dissipation, at 30°C the foot 12 / Wurster, Murrish, and Sulzman became dilated, and at 32°C the toe was finally recruited. Each of these sites may be used a t various times of the day for heat loss, but on the average, as the ambient temperature increased a new site at the distal portion of the leg was being recruited. It has been shown that in Macaca nemestrina, the timing of the waveform, the maximum and minimum temperatures, and the 24-h mean colonic temperatures were altered by changes in the ambient temperature. However, the range of the oscillation is approximately the same at all ambient temperatures studied. The rhythm in leg skin temperature was shown to be affected by ambient temperature, with the rhythm becoming obscured a t the high and low ambient temperatures. These data suggest that although the core body temperature is primarily regulated by a change in heat loss in thermoneutrality, perhaps the circadian rhythm of core temperature of these monkeys (unlike humans) is regulated more by heat production rather than by vasomotor heat loss. CONCLUSIONS 1.The rhythm in core body temperature persisted a t all ambient temperatures. 2. The rhythm in leg skin temperature was suppressed at the higher and lower ambient temperatures. 3. The mean colonic temperature increased linearly with a n increase in ambient temperature. 4.As the ambient temperature increased, additional sites along the distal portion of the leg were recruited for vasomotor heat loss. ACKNOWLEDGMENTS This research was supported by NASA contract NAS2-10621.The authors thank Narinder Bhalla for his help in conducting this study and Bruce Bailey and Mark Haley for their help with programming. Ellen C. Wurster is now with the Physiology Group, School of Biological Sciences, University of Kentucky, Lexington. REFERENCES Aschoff, J. Circadian rhythms: General features and endocrinological aspects. Pp.1-61 in ENDOCRINE RHYTHMS. D.T. Krieger, ed. New York, Raven Press, 1979. Aschoff, J.; Heise, A. Thermal conductance in man: Its dependence on time of day and on ambient temperature. Pp. 334-348 in ADVANCES IN CLIMATIC PHYSIOLOGY. S. Ztoh; K. Ogata; H. Yoshimura, eds. Tokyo, Igaku Shoin, 1972. Aschoff, J.; Pohl, H. Rhythmic variations in energy metabolism. FEDERATION PROCEEDINGS 29(4):1541-1552,1970. Aschoff, J.;Biebach, H.; Heise, A,; Schmidt, T. Day-night variation in heat balance. Pp. 147-172 in HEAT LOSS IN ANIMALS AND MAN. J.L. Monteith; L.E. Mount, eds. London, Butterworths, 1974. Baker, M.; Cronin, M.; Mountjoy, D. Variability of skin temperature in the waking monkey. AMERICAN JOURNAL OF PHYSIOLOGY 230(2):449-455, 1976. Cooper, K.E.; Cross, K.W.; Greenfield, A.D.M.; Hamilton, D.McK.; Scarborough, H. A comparison of methods for gauging the blood flow through the hand. CLINICAL SCIENCE 8:217-234,1949. Czeisler, C.A.; Weitzman, E.D.; Moore-Ede, M.C.; Zimmerman, J.C.; Knauer, R.S. Human sleep: Its duration and organization depend on its circadian phase. SCIENCE 210~1264-1267,1980. Felder, D.; Russ, E.; Montgomery, H.; Horwitz, 0. Relationship in the toe of skin surface temperature to mean blood flow measured with a plethysmograph. CLINICAL SCIENCE 13:251-257,1954. Fuller, C.A. Circadian brain and body temperature rhythms in the squirrel monkey. AMERICAN JOURNAL OF PHYSIOLOGY 246:R242-R246,1984. Fuller, C.A.; Sulzman, F.M.; Moore-Ede, M.C. Circadian control of thermoregulation in the squirrel monkey (Sairniri sciureus). AMERICAN JOURNAL OF PHYSIOLOGY 236:R153-R161,1979. Fuller, C.A.; Sulzman, F.M.; Moore-Ede, M.C. Shift-work and the jet-lag syndrome: Conflicts between environmental and body time. Pp. 305-320 in THE TWENTY-FOUR Circadian Rhythm of Body Temperature / 13 HOUR WORKDAY: PROCEEDINGS OF A SYMPOSIUM ON VARIATION IN WORKSLEEP SCHEDULES. W.P. Colquhoun; M.J. Colligan, eds. Cincinnatti, U.S. Department of Health and Human Services (National Institute of Occupational Safety and Health) publication No. 81-127, 1981. Grant, R.H., Pearson, R.S.B. The blood circulation in the human limb; observations on the differences between the proximal and distal parts and remarks on the regulation of body temperature. CLINICAL SCIENCE 31119-139,1938. Hertzman, A.B. Some relations between skin temperature and blood flow. AMERICAN JOURNAL OF PHYSICAL MEDICINE 32:233-251, 1953. Snedecor, G.W.; Cochran, W.G. STATISTICAL METHODS. Ames, Iowa State University Press, 1967. Stitt, J.T.; Hardy, J.D. Thermoregulation in the squirrel monkey (Saimiri sciureus). JOURNAL OF APPLIED PHYSIOLOGY. 31(1):48-54, 1971. Sulzman, F.M.; Fuller, C.A.; Moore-Ede,M.C. Tonic effects of light on the circadian system of the squirrel -monkey. JOURNAL OF COMPARATIVE PHYSIOLOGY 129:43-50, 1979. Wever, R. THE CIRCADIAN SYSTEM OF MAN. RESULTS OF EXPERIMENTS UNDER TEMPORAL ISOLATION. New York, Springer-Verlag, 1979.