Circadian modulation of starvation-induced hypothermia in sheep and goats

Prolonged food deprivation is known to cause a fall in the core body temperature of homeotherms. In various species of small birds and mammals (body mass up to 2-3 kg), it has been shown that starvation-induced hypothermia is modulated by the circadian system, in the sense that hypothermia is observed primarily during the inactive phase of the daily activity cycle (i.e., during the night for diurnal animals and during the day for nocturnal animals), whereas relatively normal temperatures are recorded during the active phase. To investigate whether this modulation occurs also in larger animals, we investigated the effects of 4d food deprivation on the body temperature rhythm of goats and sheep (body mass 30-40 kg). In goats, the body temperature rhythm was found to have a mean level of 39.0°C with a mean daily range of excursion of 0.42°C. The daily oscillation in body temperature persisted during the first day of fasting, but the rhythm was drastically damped, if not eliminated, over the next 3 d as body temperature descended from the baseline level of 39.0 to 38.2°C. In sheep, the rhythm was found to have a mean level of 39.3°C with a mean daily range of excursion of 0.34°C. The daily oscillation in body temperature persisted through the 4 d of food deprivation, even though the mean level of body temperature gradually fell. Temperature fell more during the third and fourth nights than during the third and fourth days. Thus, circadian modulation of starvation-induced hypothermia was observed in sheep but not in goats.     

Daily and estrous rhythmicity of body temperature in domestic cattle

Background

Rhythmicity in core body temperature has been extensively studied in humans and laboratory animals but much less in farm animals. Extending the study of rhythmicity of body temperature to farm animals is important not only from a comparative perspective but also from an economic perspective, as greater knowledge of this process can lead to improvements in livestock production practices. In this study in cattle, we investigated the maturation of the daily rhythm of body temperature in newborn calves, characterized the parameters of the daily rhythm in young cows, and studied the oscillation in body temperature associated with the estrous cycle in adult cows.

Results

We found that the daily rhythm of body temperature is absent at birth but matures fully during the first two months of life. The mature rhythm had a mean level of 38.3°C, a range of excursion of 1.4°C, and was more robust than that of any mammalian species previously studied (90% of maximal robustness). Sexually mature cows also exhibited a robust estrous rhythm of body temperature. An elevation of about 1.3°C was observed every 21 days on the day of estrus. Small seasonal variations in this pattern were observed.

Conclusion

In conclusion, calves exhibit a very robust daily rhythm of body temperature, although this rhythm is absent at birth and develops during the first two months of life. Adult cows exhibit also 21-day rhythmicity in body temperature reflecting the duration of the estrous cycle.

     

The Circadian Rhythm of Body Temperature of the Horse

Rectal temperature of 10 female adult horses was recorded every 2 h for 10 consecutive days under a natural winter photoperiod (9 h of light and 15 h of darkness per day). A robust daily rhythm of body temperature was observed in all animals. The rhythm had a mean level of 38.3°C and a range of excursion of 1.0°C. Temperature started its daily ascent at dawn each day and reached a maximum 14 hours later. Body temperature of 5 of the horses was studied for 10 more days under constant illumination. The rhythm persisted under this condition, although with a slightly longer period of 24.2 h, which confirms the endogenous nature of the rhythm. Despite the fact that the body size of the horse is several orders of magnitude greater than that of rodents, the various parameters of the body temperature rhythm of the horse are similar to those of several species of rodents previously studied.     

Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions

We studied daily rhythmicity of body temperature (T _b) before and during hibernation in Anatolian ground squirrels (Spermophilus xanthoprymnus) under natural and laboratory conditions using surgically implanted temperature loggers. Under both conditions, robust daily T _b rhythmicity with parameters comparable to those of other ground squirrel species was observed before but not during hibernation. Euthermic animals had robust daily T _b rhythms with a mean of 37.0°C and a range of excursion of approximately 4°C. No T _b rhythm was detected during torpor bouts, either because T _b rhythmicity was absent or because the daily range of excursion was smaller than 0.2°C. The general patterns of hibernation that we observed in Anatolian ground squirrels were similar to those previously observed by other investigators in other species of ground squirrels.     

Torpor patterns in the pouched mouse (Saccostomus campestris ; Rodentia): a model animal for unpredictable environments

Patterns of spontaneous and induced daily torpor were measured in the Afrotropical pouched mouse (77–115?g), Saccostomus campestris, in response to photoperiod, temperature, and food deprivation, using temperature telemetry. Photoperiod had no influence on the incidence, depth, or duration of daily torpor in either males and females. Although the testis size index decreased in response to food deprivation and photoperiod by a maximum of 24%, full testis regression did not occur. Torpor bout duration was, on average, 5.3?h, independent of photoperiod and ambient temperature. Males did not enter torpor in response to food deprivation but did in response to low ambient temperature, though significantly less frequently than females. At normothermia, the body temperatures (daily minimum, mean, maximum) of males were significantly lower than those of females. Minimum body temperatures of both males and females during torpor did not fall below 20?°C at an ambient temperature of 15?°C. The patterns of torpor measured here differ from those observed in species from strongly seasonal environments. They suggest adaptation to an environment rendered unpredictable by the El Niño Southern Oscillations. As an aseasonal, opportunistic breeder capable of year-round adaptive hypothermia, the pouched mouse represents an excellent model animal for research on physiological and behavioral adaptations to unpredictable environments.     

Different behavior of body temperature and total locomotor activity daily rhythms during light/dark cycle in stabled Oryctolagus cuniculus

In order to investigate the potential causal link between the rhythm of activity and body temperature, we simultaneously recorded rectal temperature and total locomotor activity in five clinically healthy female rabbits (blue Vienna breed), 12 week old and mean body weight 2.7 ± 0.3. Animals were housed in individual cages (90?×?50?×?35 cm) under natural 12/12 light/dark cycle. Total locomotor activity was monitored for 15 days by an activity data logger. On day 1, 5, 10, and 15 rectal temperature was recorded every 2 h for a 24-h period. Application of single cosinor method showed a nocturnal daily rhythm of rectal temperature with a range of oscillation of about 1 °C, acrophase after dusk and low robustness value. The daily rhythm of locomotor activity showed its acrophase in the middle of the scotophase and a high robustness value. This information improves the knowledge available on the circadian biology of rabbits useful in the evaluation of physiology of this species.     

Geological cycles

Abstract

Deep body temperature (DBT) and heart rate (HR) circadian rhythms were determined by radiotelemetry in 4 mares kept under controlled light and temperature conditions. Ovulations were determined by rectal palpation of their ovaries. Mean DBT values ranged from 35.85 ± .04 to 37.22 ± .02°C The circadian range of oscillation was extremely low, approximately 0.5° C, with time of maximum temperature occurring midway through the dark period. Mean HR values ranged from 36.4 ± 1.7 to 53.0 ±3.6 beats per min. The circadian range of oscillation was also low, less than 15 beats per min with time of maximum HR occurring approximately at the time of lights off. The HR circacadian rhythm peaked before the DBT circadian rhythm by 3 to 8 hrs. Ovulation did not appear to consistently affect DBT and HR circadian rhythms or their phase relationships.     

The daily,weekly, and seasonal cycles of body temperature analyzed at large scale

ABSTRACT

We performed large-scale analyses of circadian and infradian cycles of human body temperature, focusing on changes over the day, week, and year. Temperatures (n= 93,225) were collected using temporal artery thermometers from a Boston emergency department during 2009–2012 and were statistically analyzed using regression with cyclic splines. The overall mean body temperature was 36.7°C (98.1°F), with a 95% confidence interval of 36.7–36.7°C (98.1–98.1°F) and a standard deviation of 0.6°C (1.1°F). Over the day, mean body temperature followed a steady cycle, reaching its minimum at 6:00–8:00 and its maximum at 18:00–20:00. Across days of the week, this diurnal cycle was essentially unchanged, even though activities and sleeping hours change substantially during the weekly cycles of human behavior. Over the year, body temperatures were slightly colder in winter than summer (~0.2°C difference), consistent with most prior studies. We propose these seasonal differences might be due to ambient effects on body temperature that are not eliminated because they fall within the tolerance range of the thermoregulatory system. Over the year, bathyphase (daily time of minimum temperature) appeared to parallel sunrise times, as expected from sunrise’s zeitgeber role in circadian rhythms. However, orthophase (daily time of maximum temperature) and sunset times followed opposite seasonal patterns, with orthophase preceding nightfall in summer and following nightfall in winter. Throughout the year, bathyphase and orthophase remained separated by approximately 12 h, suggesting this interval might be conserved. Finally, although 37.0°C (98.6°F) is widely recognized as the mean or normal human body temperature, analysis showed mean temperature was <37.0°C during all times of day, days of the week, and seasons of the year, supporting prior arguments that the 37.0°C standard has no scientific basis. Overall, this large study showed robust and consistent behavior of the human circadian cycle at the population level, providing a strong example of circadian homeostasis.     

The Circadian Rhythm of Body Temperature of the Horse

Rectal temperature of 10 female adult horses was recorded every 2 h for 10 consecutive days under a natural winter photoperiod (9 h of light and 15 h of darkness per day). A robust daily rhythm of body temperature was observed in all animals. The rhythm had a mean level of 38.3°C and a range of excursion of 1.0°C. Temperature started its daily ascent at dawn each day and reached a maximum 14 hours later. Body temperature of 5 of the horses was studied for 10 more days under constant illumination. The rhythm persisted under this condition, although with a slightly longer period of 24.2 h, which confirms the endogenous nature of the rhythm. Despite the fact that the body size of the horse is several orders of magnitude greater than that of rodents, the various parameters of the body temperature rhythm of the horse are similar to those of several species of rodents previously studied.     

The role of endogenous and exogenous factors in regulation of synchronous emergence of Trichogramma embryophagum Hartig and T. principium Sug. et Sor. (Hymenoptera, Trichogrammatidae)

The interaction of exogenous and endogenous factors affecting the daily rhythm of emergence of adult parasitoids Trichogramma embryophagum and T. princupium from laboratory strains was studied. Under a constant temperature of 20°C and different photoperiods (photophase of 12, 16, or 20 h), both species demonstrated a distinct rhythm; the majority of adults emerged during 4 first hours after light-on. The fraction of individuals emerged during this period depended on the photoperiod and was different in both the species studied. Experiments with non-periodic regimes (constant light or constant darkness, 20°C) demonstrated that the rhythm is based on the endogenous circadian oscillations that are synchronized with the external photoperiod. The time of emergence however, was not rigidly “programmed” and could be modified by the direct influence of the light and temperature Light-on and/or temperature increase (from 20° up to 30° C) induced the emergence of a certain percentage of individuals virtually at any time of the 24-h-long cycle. The magnitude of the response, estimated as the fraction of adults emerged during 2 h after the stimulation, changed daily under the control of the circadian oscillation. Thus, the plasticity of the daily dynamics of emergence was controlled (to a certain extent) by the endogenous rhythm of sensitivity to the stimuli. The interspecific differences in the relative sensitivity to light-on and temperature increase were revealed. When light and temperature stimuli were applied simultaneously, they caused a synergistic effect, exceeding a simple sum of separate impacts. These results demonstrate an important role of exogenous factors in control of the emergence rhythm in Trichogramma and can also be used in elaboration of methods of regulation and synchronization of emergence in these parasitoids.     

The effect of fasting and refeeding on temperature preference,activity and growth of roach, <Emphasis Type="Italic">Rutilus rutilus</Emphasis>

Most fish species are regularly subjected to periods of starvation during which a reduction of energy turnover might be favourable for the animal. This reduction of energy flux may be achieved by changes in thermal behaviour and/or swimming activity. We investigated such behavioural changes during starvation and subsequent refeeding in roach, Rutilus rutilus, with respect to energetic benefits and growth maximisation. Roach, acclimated to a wide range of temperatures (4, 12, 20, 24, 27 and 30 °C), were fed to excess, subjected to 3 weeks of starvation and subsequently refed in order to determine the temperature dependence of feeding rates, growth rates and conversion efficiency (K₁) under control conditions and during compensatory growth. When exposed to a thermal gradient, control animals preferentially selected a temperature of 26.8ǂ.9 °C, which is in the range of the optimal temperatures for feeding, growth and conversion efficiency. Starving fish showed a distinct circadian pattern of the mean selected temperature (MST). They migrated to cooler water in the dark (MST_dark=22.8ǃ.1 °C) but returned to warmer water during daytime. This behaviour may be regarded as a trade-off between the potentially higher food density in warmer water areas and the energetic benefit of selecting cooler water patches. The circadian pattern of MST was gradually abandoned upon refeeding and control values were reached again after 3 weeks. Energetically more effective than behavioural hypothermia was the reduction of swimming activity. During starvation, activity peaks were slightly lower than under control conditions and mean daily activity decreased by about 50%. Swimming velocity, however, was not affected by feeding regime. After a period of starvation fish showed compensatory growth at all temperatures, even below 12 °C, where these animals normally do not grow. This suggests that after a period of starvation the critical temperature for growth shifts to lower values.     

Long-acting neuroleptics used in wildlife management do not impair thermoregulation or physical activity in goats (Capra hircus)

Long-acting neuroleptics commonly are used in wildlife management to decrease stress-related mortality in wild animals, but with possible effects on thermoregulation, which may contribute to residual morbidity and mortality. We investigated the effects of haloperidol (0.01, 0.1, 1 mg kg(-1), n=4), zuclopenthixol (0.1, 1, 10 mg kg(-1), n=4) and perphenazine (0.1, 1, 10 mg kg(-1), n=8), as well as control injections of sunflower oil, on body temperature and physical activity of laboratory goats under hot, cold and thermoneutral ambient temperatures. Implanted data loggers continuously recorded abdominal temperature, and data loggers attached externally on the foreleg recorded movement of unrestrained goats, in a climatic chamber at 35 degrees C, 10 degrees C and 22 degrees C. Cycling ambient temperature between 35 degrees C in daytime and 10 degrees C at night time caused a significant increase in amplitude of the circadian rhythm of body temperature in goats given sunflower oil (P=0.0012, unpaired t-test, n=8), but the administration of zuclopenthixol or perphenazine did not affect this change in amplitude (P>0.05, two-way ANOVA, n=4). Mean daily body temperature after administration of zuclopenthixol or perphenazine, and mean daily activity after zuclopenthixol administration, were not significantly different to those after control injections, at any ambient temperature, for the expected duration of drug activity (all P>0.05, two-way ANOVA, n=4). Thermal response indices, and mean activity, during heat, cold or thermoneutral exposure, of goats for 7 h after haloperidol injection, were not significantly different, at any dose or any ambient temperature, to those following control injections (all P>0.05, repeated measures ANOVA, n=4). Long-acting neuroleptics did not impair activity or thermoregulation of goats subjected to inescapable thermal challenges.     

Age‐depending effects of narcosis and transmitter implantation on circadian body temperature and activity rhythms in mice

Summary

The effects of narcosis and of telemetry transmitter implantation on core temperature and locomotor activity were investigated in female laboratory mice of various age (3, 15 and 52 weeks old). Following surgery a transient hypothermia was observed. The body temperatures measured 30 min after beginning of narcosis were lower in juvenile and in presenile mice (29.6° ±0.8°C resp. 30.0° ±0.2°C) than in adult animals (31.9° ±0.3°C). The following temperature increase was fastest in juvenile mice. Normal body temperature was reached after 6h 20’ already. Adult and presenile mice needed 8h 30’ resp. 7h 30’. The temperature increase seemed to be independent from activity behaviour of the animals. No substantial differences could be obtained whether the transmitters had room or body temperature before implantation and whether the animals were warmed after surgery by an infrared bulb or not. Probably, the temperature increase depended mainly on the elimination rate of the drug.

Normal circadian core temperature and activity rhythms reappeared on average within 5–6 days in juvenile mice and a little faster in adult (4–5 days) as well as in presenile ones (3–4 days). However, interindividual differences in recovery time were more pronounced than age‐dependent variations.

Circadian core temperature and activity patterns were quite similar in all three age classes investigated. Ontogenetic differences concern, besides changes in daily mean values, mainly a temperature amplitude increasing with age, as well as a high percentage of ultradian components in the activity pattern of juvenile mice compared to older ones.

Telemetry systems are widely used for long‐term measurements of core temperature in laboratory animals (Clement et al., 1989; Refinetti and Menaker, 1992). In our investigations of ontogenetic changes of the circadian temperature and activity rhythms in mice we used an integrated telemetry and data acquisition system (Dataquest, Data Sciences Inc., USA). It comprises implantable wireless transmitters, telemetry receivers, a consolidation matrix and a data acquisition system. The aim of a preliminary study was to analyse the effects of narcosis and transmitter implantation. The time required to recover normal values of body temperature and of locomotor activity as well as normal circadian rhythms was determined, considering also ontogenetic variations.     

Summer torpor in African woodland dormiceGraphiurus murinus (Myoxidae: Graphiurinae)

We determined the effect of food availability (presence/absence) and ambient temperature (25/10°C) on daily energy expenditure and the use of activity and torpor in summer-acclimated captiveGraphiurus murinus. Daily energy expenditure declined logarithmically with duration of food deprivation at a mean rate of 11 and 31% per day at 25 and 10°C, respectively. The incidence of torpor in the presence of food at 25°C was low (one in seven individuals) and increased on a single day's exposure to 10°C and with duration of food deprivation. Use of torpor was highest during the day, varied between individuals, and torpor bouts of greater than 24h duration were not noted. With food deprivation, individuals at 25°C initially responded by reducing activity but remained euthermic while the same individuals at 10°C responded by increasing their use of torpor during the light period; this difference in response probably reflects a difference in the relative energetic benefits of torpor at different temperatures.     

Variation in the daily rhythm of body temperature of free-living Arabian oryx (Oryx leucoryx): does water limitation drive heterothermy?

Heterothermy, a variability in body temperature beyond the limits of homeothermy, has been advanced as a key adaptation of Arabian oryx (Oryx leucoryx) to their arid-zone life. We measured body temperature using implanted data loggers, for a 1-year period, in five oryx free-living in the deserts of Saudi Arabia. As predicted for adaptive heterothermy, during hot months compared to cooler months, not only were maximum daily body temperatures higher (41.1 ± 0.3 vs. 39.7 ± 0.1°C, P = 0.0002) but minimum daily body temperatures also were lower (36.1 ± 0.3 vs. 36.8 ± 0.2°C, P = 0.04), resulting in a larger daily amplitude of the body temperature rhythm (5.0 ± 0.5 vs. 2.9 ± 0.2°C, P = 0.0007), while mean daily body temperature rose by only 0.4°C. The maximum daily amplitude of the body temperature rhythm reached 7.7°C for two of our oryx during the hot-dry period, the largest amplitude ever recorded for a large mammal. Body temperature variability was influenced not only by ambient temperature but also water availability, with oryx displaying larger daily amplitudes of the body temperature rhythm during warm-dry months compared to warm-wet months (3.6 ± 0.6 vs. 2.3 ± 0.3°C, P = 0.005), even though ambient temperatures were the same. Free-living Arabian oryx therefore employ heterothermy greater than that recorded in any other large mammal, but water limitation, rather than high ambient temperature, seems to be the primary driver of this heterothermy.     

Circadian Modulation of Cold-Induced Thermogenesis in the Golden Hamster

The relationship between the circadian and homeostatic control of body temperature was studied in golden hamsters maintained under a 14:10 LD cycle. Telemetric records of body temperature showed that body temperature oscillates daily with a low phase during the light section of the LD cycle and a high phase during the dark section. The low phase of the temperature rhythm was found to start two hours after lights on and to last about 8 hours. The high phase was found to start immediately after lights off and to last about 8 hours also. Metabolic heat production was measured by indirect calorimetry during the high phase and the low phase of the body temperature rhythm. Heat production in a thermoneutral environment was higher during the high phase of the body temperature rhythm than during the low phase, but cold-induced thermogenesis was greater during the low phase than during the high phase. This finding suggests that the autonomic thermoregulatory system is more responsive to cold stress during the low phase than during the high phase. Consequently, the daily oscillation of body temperature cannot be explained by an elevation of the thermoregulatory set point during the high phase of the rhythm. The homeostatic and circadian control of body temperature seem to be exerted separately from each other.     

Annual cycle of oxygen consumption (QO 2) in a hibernating animalthe garden dormouse: reduction of the QO 2 and hypothermia following fasting]

A circannual cycle of oxygen consumption (QO2) was observed in active garden dormice maintained during 19 months under external conditions for temperature and lighting. QO2 was minimum in october and maximum in may. In the same animals deprivation of food induced hypothermia and a 23% decrease in QO2 which always preceeded hypothermia. No circannual rhythm was noted in the amplitude of this reduction.     

Circadian Modulation of Cold-Induced Thermogenesis in the Golden Hamster

The relationship between the circadian and homeostatic control of body temperature was studied in golden hamsters maintained under a 14:10 LD cycle. Telemetric records of body temperature showed that body temperature oscillates daily with a low phase during the light section of the LD cycle and a high phase during the dark section. The low phase of the temperature rhythm was found to start two hours after lights on and to last about 8 hours. The high phase was found to start immediately after lights off and to last about 8 hours also. Metabolic heat production was measured by indirect calorimetry during the high phase and the low phase of the body temperature rhythm. Heat production in a thermoneutral environment was higher during the high phase of the body temperature rhythm than during the low phase, but cold-induced thermogenesis was greater during the low phase than during the high phase. This finding suggests that the autonomic thermoregulatory system is more responsive to cold stress during the low phase than during the high phase. Consequently, the daily oscillation of body temperature cannot be explained by an elevation of the thermoregulatory set point during the high phase of the rhythm. The homeostatic and circadian control of body temperature seem to be exerted separately from each other.     

Timing of torpor bouts during hibernation in European hamsters (Cricetus cricetus L.)

Body temperature (T _b) of seven European hamsters maintained at constant ambient temperature (T _a = 8 °C) and constant photoperiod (LD 8:16) was recorded throughout the hibernating season using intraperitoneal temperature-sensitive HF transmitters. The animals spent about 30% of the hibernation season in hypothermia and 70% in inter-bout normothermy. Three types of hypothermia, namely deep hibernation bouts (DHBs), short hibernation bouts (SHBs), and short and shallow hibernation bouts (SSHBs), were distinguished by differences in bout duration and minimal body temperature (T _m). A gradual development of SSHBs from the diel minimum of T _b during normothermy could be seen in individual hamsters, suggesting a stepwise decrease of the homeostatic setpoint of T _b regulation during the early hibernation season. Entry into hibernation followed a 24-h rhythm occurring at preferred times of the day in all three types of hypothermia. DHBs and SHBs were initiated approximately 4 h before SSHBs, indicating a general difference in the physiological initiation of SSHBs on the one hand and DHBs and SHBs on the other. Arousals from SHBs and SSHBs also followed a 24-h rhythm, whereas spontaneous arousals from DHBs were widely scattered across day and night. Statistical analyses of bout length and the interval between arousals revealed evidence for a free-running circadian rhythm underlying the timing of arousals. The results clearly demonstrate that entries into hypothermia are linked to the light/dark-cycle. However, the role of the circadian system in the timing of arousals from DHBs remains unclear. Accepted: 11 December 1996