Behavioral thermoregulation in a non human primate: Effects of age and photoperiod on temperature selection
Introduction
Thermoregulation involves the use of autonomic and behavioral mechanisms, that allow the individual to adapt to changes in ambient temperature while maintaining its metabolic rate minimal (Gordon, 1985, Gordon et al., 1986). There is compelling evidence suggesting that deficits in thermoregulation occur in aged humans (Pandolf, 1997, Young and Lee, 1997, Kenney and Munce, 2003) and in laboratory animals (Shefer and Talan, 1997, Florez-Duquet and McDonald, 1998). Indeed, exposure to thermal stress induces a higher susceptibility for hypo- or hyperthermia in the elderly, reflecting deficits in both autonomic and behavioral thermoregulation (Anderson et al., 1996). The elderly have a reduced rate of sweat secretion, reduced metabolic responses and less effective peripheral thermoregulatory responses. Moreover, during daytime, the elderly regulate their indoor ambient temperature less precisely (Collins et al., 1981) and their thermal perception is less sensitive especially in summer (Natsume et al., 1992). The ability to make behavioral adjustments when exposed to low or high temperatures decreases with age and this would greatly contribute to the insufficient thermoregulatory responses and discomfort observed in the elderly (Van Someren et al., 2002). An accurate thermal choice is crucial for optimal energy saving during the night and for a sleep of good quality (Van Someren, 2000, Raymann et al., 2005). Although the impact of altered thermoregulatory responses on morbidity and mortality in the elderly is acknowledged, mechanisms accounting for such functional changes with aging are still unknown.
For a better understanding of age-related alterations in behavioral thermoregulation, we studied temperature selection in a thermal gradient in a non human primate, the mouse lemur (Microcebus murinus). The mouse lemur is a small nocturnal Malagasy prosimian primate. To cope with the seasonality in climatic conditions and food availability that occurs in its natural habitat, the mouse lemur exhibits seasonal rhythms in most of its physiological and behavioral functions studied so far (Perret, 1992, Aujard et al., 1998, Perret and Aujard, 2001b). The biological rhythms of the mouse lemurs are highly dependent on the photoperiod. Day lengths longer than 12 h are stimulatory, leading to sustained activity of both behavioral and physiological functions, including metabolic and reproductive functions, whereas day lengths shorter than 12 h result in complete gonadal regression, fattening and reduced behavioral activities (Perret, 1992). Adaptive traits in thermoregulatory functions have been well documented in this species. The daily rhythm in body temperature is characterized by high levels during the nocturnal period of activity and low levels during the diurnal rest, with a phase of hypothermia occurring during the first half of the daytime (Perret and Aujard, 2001a). Daily hypothermia is a key mechanism for the mouse lemur, that adjusts its energy expenditure through modulation of its body temperature level (Séguy and Perret, 2005b). Thermoregulatory functions vary according to photoperiod and ambient temperature (Aujard et al., 1998, Perret, 1998, Aujard and Vasseur, 2001, Séguy and Perret, 2005b), food availability (Séguy and Perret, 2005b) and social factors (Séguy and Perret, 2005a). Thermoregulatory responses involve the use of nonshivering thermogenesis in this primate which possesses brown adipose tissue (Génin et al., 2003). In addition to advanced autonomic thermoregulatory responses, the mouse lemur has developed particular behaviors that modulate its energy expenditures. Mainly solitary during the night, mouse lemurs sleep in buffered tree holes during the day. The choice for an insulating tree hole increases the energy savings of the animal (Schmid, 1998). In addition, mouse lemurs gather in nests and this nest sharing behavior reduces even more the energy expenditure of each individual. The amount of energy saved by nesting varied according to season (Perret, 1998).
With a life span of 8–10 years in captivity, the mouse lemur has been proposed as one of the main models for the study of Alzheimer’s disease in non human primates (Bons et al., 2006). In this species, cognitive decline associated with cerebral atrophy is observed in both physiological and pathological aging (Dhenain et al., 2003). Some behavioral activity parameters show a decrease with aging (Aujard and Perret, 1998, Némoz-Bertholet and Aujard, 2003). Endocrine functions are also altered with aging. Aged animals show a decrease in sexual hormones (Aujard and Perret, 1998), melatonin (Aujard et al., 2001) and DHEA-S (Perret and Aujard, 2005). Daily and seasonal biological rhythms are altered in aged mouse lemurs. The daily rhythm of locomotor activity is fragmented and of reduced amplitude in aged animals compared to adults (Cayetanot et al., 2005, Aujard et al., 2006). An age-related decrease in amplitude has also been demonstrated in the seasonal rhythms of body mass, basal metabolic rate and testosterone (Perret, 1997, Aujard et al., 2001, Perret and Aujard, 2006). To date, no data is available on thermoregulatory processes in aged mouse lemurs. Owing to the importance of such processes for survival and longevity, further studies are clearly needed.
The present study investigated the effects of aging on behavioral thermoregulation by comparing ambient temperature preference between adult and aged mouse lemurs. Furthermore, experiments were carried out in two different photoperiods to examine the seasonal differences in temperature selection.
Section snippets
Animals
The male gray mouse lemurs (M. murinus) used in this study were born in the laboratory breeding colony of Brunoy (MNHN, France, license approval No A91.114.1). General conditions of captivity were maintained constant: ambient temperature (24–26 °C), relative humidity (55%), and food was available ad libitum (including fresh fruits, a milky mixture and meal worms). In captivity, seasonal variations of physiological functions can be entrained by alternating 6-month periods of long photoperiod (14 h
General activity pattern
Once they were placed in the apparatus and after lights off, all mouse lemurs exhibited a high level of exploratory behaviors revealed by repeated visits in the 5 available nests. Time spent in the nests during the night time varied according to season and age (Fig. 2). In both photoperiods, aged animals spent significantly more time in a nest than adult animals (LP: t (38) = −4.5, p < 0.001; SP: t (38) = −4.48, p < 0.001). Whatever the age category, mouse lemurs spent more time in a nest when exposed to
Discussion
The temperature gradient apparatus was successfully adapted to the mouse lemur. Its natural tendency for exploration and its spontaneous nesting behavior allowed the gathering of Ta selection data throughout the light-dark cycle and in both age categories. Ta selection varied according to photoperiod and age in this primate species. A choice for warm climates was observed in adult mouse lemurs exposed to SP, whereas behavioral thermoregulation in LP did not seem useful for maintenance of
Acknowledgements
This work was supported by Institut de la Longévité et du Vieillissement, Fondation pour la Recherche Médicale and ACI INSERM Neurosciences.
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