Behavioral thermoregulation in a non human primate: Effects of age and photoperiod on temperature selection

Abstract

Deficits in autonomic thermoregulatory capacities have been identified in aged humans and animals, but little is known about the effect of aging on behavioral thermoregulation and the potential effect of season. Preferred ambient temperature (T_a) in a thermal gradient (available T_as from 10 to 30 °C) was measured in the mouse lemur, a nocturnal Malagasy primate. Male mouse lemurs (40 adults and 40 aged) were studied under short (SP, resting season) and long photoperiod (LP, breeding season). Additionally, daily body temperature rhythm was telemetrically recorded in 30 individuals of both age categories. In adults exposed to SP, a choice for warm climates was observed, with a mean diurnal T_a of 26 °C. Day-night differences in selected T_a occurred only in animals exposed to SP. In LP, selection of a warm environment did not seem to be a necessary factor for maintenance of normothermia. Aged animals selected warmer T_as than adults during the night like during the day, whatever the photoperiod. In relation to changes in body temperature rhythm according to age, aged animals would select warmer environments possibly to compensate autonomic deficiencies. Further studies on age-related changes in hormonal and cellular functions involved in energy balance and thermoregulation will help decipher the causes of insufficient responses to thermal stress observed in the elderly.

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.