Daily variation of body temperature, locomotor activity and maximum nonshivering thermogenesis in two species of small rodents
Introduction
In the majority of mammals body temperature (Tb) is not regulated at a constant level over the course of a day, but rather demonstrates a reproducible oscillation (Aschoff (1970), Aschoff (1982); Refinetti, 1999a). The oscillations of Tb may be characterized by different periods and amplitudes. The circadian rhythm has a period of about 24 h (Aschoff, 1967; Fuller et al., 1979) and ultradian rhythm of approximately 2–6 h (Refinetti and Menaker, 1992). Several factors have been shown to play a role in regulation of the circadian rhythm of body temperature. One often-discussed factor is the influence of locomotor activity on the existence and amplitude of body temperature changes. Changes of activity in the circadian rhythm are correlated with body temperature rhythms (Refinetti, 1994; Brown and Refinetti, 1996; Decoursey et al., 1998; Weinert and Waterhouse, 1998; Benstaali et al., 2001). For example, the activity level explains 70% of Tb variation in golden hamsters Mesocricetus auratus (Refinetti, 1994), and the alternation of sleep and waking accounts for 84% of Tb variation in rats (Franken et al., 1992). Most of the authors who studied the correlation between body temperature and activity suggested that activity affected, but did not determine the rhythm of Tb (see Refinetti and Menaker, 1992 for review). Correlation between activity and body temperature in the laboratory mouse was strong only during the light phase and dark–light transition, whereas during the dark phase and light–dark transition the correlation was nonsignificant in many night-active animals (Weinert and Waterhouse, 1998). Moreover, Decoursey et al. (1998) found that the rise in Tb preceded the increase of activity level by about 1 h in golden hamsters and by 20 min in eastern chipmunks Tamias striatus. This suggests that the heat production related to the locomotor activity cannot account for the initial phase of the rise of Tb.
In small mammals, endogenous heat production is mainly achieved through nonshivering thermogenesis (NST), a heat production mechanism liberating chemical energy due to processes that do not involve muscular contractions (Sellers et al., 1954; Heldmaier, 1971; Jansky, 1973). Thus the heat production under conditions of basal metabolism, i.e. at rest in the postabsorptive state and at the ambient temperature of the thermoneutral zone (TNZ) is mostly nonshivering thermogenesis (called obligatory NST). Ambient temperatures below the TNZ elicit the additional nonshivering heat production (regulatory NST) that enables maintaining stable Tb. The capacity of an animal to generate heat by NST can be assessed by injection of noradrenaline (NA) (Hsieh and Carlson, 1957).
If the rise of Tb in circadian rhythm results from an elevated rate of NST, then it is reasonable to predict that NST, measured as metabolic response to noradrenaline (MMRNST), would also show daily variation with maximum response during the rising period of Tb. Daily variation of NST has been reported by few authors (e.g. Haim et al., 1995; Haim and Zisapel, 1999; Jefimow et al., 2000) but we are not aware of any studies comparing daily Tb variations, activity rhythms and NST oscillations. The aim of this study was therefore to test a hypothesis that rodents exhibiting circadian rhythm of Tb also change their response to NA during the day, and that these changes are more important than locomotor activity in shaping daily variation of Tb.
Existence of daily rhythm of body temperature may result from changing rate of heat production or heat dissipation, or a combination of both (Rubal et al., 1992). Assuming that daily rhythm of Tb is determined primarily by the rhythm of regulatory NST, one can predict that the amplitude of MMRNST variation should correlate with the amplitude of Tb variation. Therefore, it would be of interest to measure MMRNST in: (1) animals with clear circadian Tb rhythm during different periods of the day, when Tb is low, increasing, and at the high level and, (2) animals without circadian Tb rhythm. We measured daily changes of body temperature, the respective maximum MMRNST, resting rates of metabolism, and locomotor activity in yellow-necked mice A. flavicollis and root voles M. oeconomus. Mice species are known to have clear-cut circadian Tb rhythm with high amplitude of Tb variation (Rubal et al., 1992; Haim et al., 1995; Weinert and Waterhouse, 1999). On the other hand, vole species are known to have ultradian rhythm of Tb with no- or low-circadian rhythmicity. The amplitude of ultradian Tb oscillation in voles is lower than circadian Tb variation in mice (Moshkin et al., 2001; A. Myrcha and J. Żukowski, pers. comm.).
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Materials and methods
The animals (yellow-necked mice, n=72, and root voles, n=52) used in the experiments were captured near Białystok, Poland in September 1996–1998 and 2002, and acclimated to laboratory conditions for at least 3 months prior to the measurements. Mice were held at ambient temperature of 25°C (±1°C) and photoperiod 12L:12D. Voles were acclimated to the same temperature, but to a longer day, 16L:8D as we were interested in animals with possibly the lowest amplitude of Tb rhythm (long photoperiod
Results
Body temperature of yellow-necked mice measured by telemetry varied in a clear circadian rhythm (Fig. 1A). The lowest Tb values of 36.6±0.21°C were recorded early in the morning at the dark–light transition (08:00), and in the afternoon (16:00; Tb of 36.7±0.18°C; n=8 individuals, 6 values from different days averaged for each individual). Between 16:00 and 21:00 Tb increased abruptly, and at lower rate thereafter, reaching a maximum mean value of 38.1±0.25°C (n=8) at 24:00. This rise of Tb from
Discussion
Our study corroborated the presence of diurnal body temperature variation in yellow-necked mice A. flavicollis, and the lack of circadian Tb rhythm in root voles M. oeconomus. This difference in the circadian course of Tb was not associated with the corresponding difference in locomotor activity. Instead, the pattern of activity was similar in the two species, with elevated values at night. In addition, the increase of activity level in mice observed after commencement of the dark phase was
Acknowledgements
The study was supported by the State Committee for Scientific Research (KBN) grant 6 P04F 006 12. We thank Marek Konarzewski, Gilbert Dryden, and Kerry Foresman for valuable comments and improvement of the earlier draft of the manuscript. Our experiments complied with the current Polish laws.
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