Allali KE, Achaâban MR, Bothorel B, Piro M, Bouâouda H, Allouchi ME, Ouassat M, Malan A, Pévet P. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Regul Integr Comp Physiol 304: R1044 -R1052, 2013. First published March 13, 2013 doi:10.1152/ajpregu.00466.2012.-In mammals the light-dark (LD) cycle is known to be the major cue to synchronize the circadian clock. In arid and desert areas, the camel (Camelus dromedarius) is exposed to extreme environmental conditions. Since wide oscillations of ambient temperature (Ta) are a major factor in this environment, we wondered whether cyclic Ta fluctuations might contribute to synchronization of circadian rhythms. The rhythm of body temperature (Tb) was selected as output of the circadian clock. After having verified that Tb is synchronized by the LD and free runs in continuous darkness (DD), we submitted the animals to daily cycles of Ta in LL and in DD. In both cases, the Tb rhythm was entrained to the cycle of Ta. On a 12-h phase shift of the Ta cycle, the mean phase shift of the Tb cycle ranged from a few hours in LD (1 h by cosinor, 4 h from curve peaks) to 7-8 h in LL and 12 h in DD. These results may reflect either true synchronization of the central clock by Ta daily cycles or possibly a passive effect of Ta on Tb. To resolve the ambiguity, melatonin rhythmicity was used as another output of the clock. In DD melatonin rhythms were also entrained by the T a cycle, proving that the daily T a cycle is able to entrain the circadian clock of the camel similar to photoperiod. By contrast, in the presence of a LD cycle the rhythm of melatonin was modified by the T a cycle in only 2 (or 3) of 7 camels: in these specific conditions a systematic effect of T a on the clock could not be evidenced. In conclusion, depending on the experimental conditions (DD vs. LD), the daily T a cycle can either act as a zeitgeber or not.camel; circadian clock; body temperature; daily ambient temperature; melatonin; nonphotic entrainment RHYTHMICITY in physiological processes is a fundamental property of all living organisms (32). A number of biological functions display daily and seasonal variations in a way to anticipate and adapt to the upcoming cycling changes in environment (light, temperature, food availability, etc.). In mammals, the circadian clock, located in the suprachiasmatic nuclei of the hypothalamus (SCN), is central for these adaptive processes. This clock is a strong autonomous oscillator cycling with a period close to 24 h under constant conditions (23) and entrained by environmental cues to an exact period of 24 h. Thus SCN play a pivotal role to control numerous circadian biological rhythms such as those of body temperature (T b ), melatonin, or behavioral features. In all mammals studied, the light-dark cycle is the most powerful synchronizer (zeitgeber) of the master clock (for a review see Ref. 15). T b rhythm represents a robust output of the clock, widely used in clinical research to determine pro...
Circadian rhythms in nocturnal and diurnal mammals are primarily synchronized to local time by the light/dark cycle. However, nonphotic factors, such as behavioral arousal and metabolic cues, can also phase shift the master clock in the suprachiasmatic nuclei (SCNs) and/or reduce the synchronizing effects of light in nocturnal rodents. In diurnal rodents, the role of arousal or insufficient sleep in these functions is still poorly understood. In the present study, diurnal Sudanian grass rats, Arvicanthis ansorgei, were aroused at night by sleep deprivation (gentle handling) or caffeine treatment that both prevented sleep. Phase shifts of locomotor activity were analyzed in grass rats transferred from a light/dark cycle to constant darkness and aroused in early night or late night.
In the present work, we have studied daily rhythmicity of body temperature (Tb) in Arabian camels challenged with daily heat, combined or not with dehydration. We confirm that Arabian camels use heterothermy to reduce heat gain coupled with evaporative heat loss during the day. Here, we also demonstrate that this mechanism is more complex than previously reported, because it is characterized by a daily alternation (probably of circadian origin) of two periods of poikilothermy and homeothermy. We also show that dehydration induced a decrease in food intake plays a role in this process. Together, these findings highlight that adaptive heterothermy in the Arabian camel varies across the diurnal light–dark cycle and is modulated by timing of daily heat and degrees of water restriction and associated reduction of food intake. The changed phase relationship between the light–dark cycle and the Tb rhythm observed during the dehydration process points to a possible mechanism of internal desynchronization during the process of adaptation to desert environment. During these experimental conditions mimicking the desert environment, it will be possible in the future to determine if induced high‐amplitude ambient temperature (Ta) rhythms are able to compete with the zeitgeber effect of the light–dark cycle.
To examine a possible control of reproductive seasonality by melatonin, continual-release subcutaneous melatonin implants were inserted 4.5 months before the natural breeding season (October–April) into female camels (Melatonin-treated group). The animals were exposed to an artificial long photoperiod (16L:8D) for 41 days prior to implant placement to facilitate receptivity to the short-day signal that is expected with melatonin implants. The treated and control groups (untreated females) were maintained separately under outdoor natural conditions. Ovarian follicular development was monitored in both groups by transrectal ultrasonography and by plasma estradiol-17β concentrations performed weekly for 8 weeks and then for 14 weeks following implant insertion. Plasma prolactin concentrations were determined at 45 and 15 days before and 0, 14, 28, 56, and 98 days after implant insertion. Plasma melatonin concentration was determined to validate response to the artificial long photoperiod and to verify the pattern of release from the implants. Results showed that the artificial long photoperiod induced a melatonin secretion peak of significantly (P < 0.05) shorter duration (about 2.5 h). Melatonin release from the implants resulted in higher circulating plasma melatonin levels during daytime and nighttime which persisted for more than 12 weeks following implants insertion. Treatment with melatonin implants advanced the onset of follicular growth activity by 3.5 months compared to untreated animals. Plasma estradiol-17β increased gradually from the second week after the beginning of treatment to reach significantly (P < 0.01) higher concentrations (39.2 ± 6.2 to 46.4 ± 4.5 pg/ml) between the third and the fifth week post insertion of melatonin implants. Treatment with melatonin implants also induced a moderate, but significant (P < 0.05) suppressive effect on plasma prolactin concentration on the 28th day. These results demonstrate that photoperiod appears to be involved in dromedary reproductive seasonality. Melatonin implants may be a useful tool to manipulate seasonality and to improve reproductive performance in this species. Administration of subcutaneous melatonin implants during the transition period to the breeding season following an artificial signal of long photoperiod have the potential to advance the breeding season in camels by about 2.5 months.
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