Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests

Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T _a). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T _sk) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.     

Females go where the food is: does the socio-ecological model explain variation in social organisation of solitary foragers?

The socio-ecological model (SEM) links ecological factors with characteristics of social systems and allows predictions about the relationships between resource distribution, type of competition and social organisation. It has been mainly applied to group-living species but ought to explain variation in social organisation of solitary species as well. The aim of this study was to test basic predictions of the SEM in two solitary primates, which differ in two characteristics of female association patterns: (1) spatial ranging and (2) sleeping associations. Beginning in August 2002, we regularly (re-)captured and marked individuals of sympatric populations of Madame Berthe's and grey mouse lemurs (Microcebus berthae, Microcebus murinus) in Kirindy Forest (Madagascar). We recorded data on spatial patterns, feeding and social behaviour by means of direct observation of radio-collared females. The major food sources of M. berthae occurred in small dispersed patches leading to strong within-group scramble competition and over-dispersed females with a low potential for female associations. In contrast, M. murinus additionally used patchily distributed, high-quality (large) resources facilitating within-group contest competition. The combined influence of less strong within-group scramble and contest as well as between-group contest over non-food resources allowed females of this species to cluster in space. Additionally, we experimentally manipulated the spatial distribution of food sources and found that females adjusted their spatial patterns to food resource distribution. Thus, our results support basic predictions of the SEM and demonstrated that it can also explain variation in social organisation of solitary foragers.     

Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus)

The aim of this study was to investigate reproductive strategies and their consequences in gray mouse lemurs (Microcebus murinus), small solitary nocturnal primates endemic to Madagascar. Previous reports of sexual dimorphism in favor of males and females, respectively, a high potential for sperm competition and pheromonal suppression of mating activity among captive males, led us to investigate mechanisms of intrasexual competition in a wild population. Based on 3 years of mark-recapture data, we demonstrate that sexual dimorphism in this species fluctuated annually as a result of independent changes in male and female body mass. Male body mass increased significantly prior to the short annual mating season. Because their testes increased by 100% in the same period and because their canines are not larger than those of females, we suggest that large male size may be advantageous in searching for estrous females and in enabling them to sustain periods of short-term torpor. In contrast to reports from captive colonies, we found no evidence for two morphologically distinct classes of males. Finally, we also show that most adult males are active throughout the cool dry season that precedes the mating season, whereas most adult females hibernate for several months. This is in contrast to other solitary hibernating mammals, where males typically emerge 1–2 weeks before females. Thus, this first extended field study of M.␣murinus clarified previous conflicting reports on sexual dimorphism and male reproductive strategies in this primitive primate by showing that their apparent deviation from predictions of sexual selection theory is brought about by specific environmental conditions which result in sex-specific life history tactics not previously described for mammals. A general conclusion is that sexual selection can operate more strongly on males without resulting in sexual dimorphism because of independent selection on the same traits in females. Received: 6 July 1997 / Accepted after revision: 28 March 1998     

Role of sex and breeding status in grooming and total tick load of impala

The lesser mouse lemur (Microcebus murinus) is a prosimian primate which presents evidence of sex ratio bias of offspring that agrees with the direction of bias predicted by the local resource competition model for facultative sex ratio adjustment. That is, females overproduced sons when grouped prior to mating, whereas isolated females exhibited the opposite tendency. In this solitary species, social communication relies heavily on urinary chemical signals. To test the hypothesis that sex biases induced by social factors may be linked to urinary cues, isolated females were exposed (n = 76) or not (control group, n = 16) to urinary cues from other reproductively active females from the beginning of the breeding season (induced by long photoperiod) until oestrus. During that period, females were either continuously (n = 17) or partially (n = 59) exposed to chemosignal stimulation. Females in oestrus were placed in contact with a breeding male and subsequently isolated until they gave birth. All females entered oestrus but the timing of oestrus was significantly delayed by 1 week in urine-exposed females. A general depressive effect of long-term urine exposure on fecundity was demonstrated, involving fewer impregnations, higher abortion frequency and smaller litter sizes. Among females giving birth (n = 55) to a total of 129 young, a significant positive correlation was found between sex ratio bias towards males and the duration of urine exposure. However, the shift in sex ratio at birth depended on the duration of urine stimulation during a sensitive period extending from the beginning of the long photoperiod until the beginning of the follicular phase. In the absence of urinary cues during the sensitive period, females significantly overproduced daughters (32% males of 53 newborn). As urine exposure increased during the sensitive phase, the proportion of males in litters increased from 54% males (n = 50) in partially urine-exposed females to a significant bias towards males (69.2% of 26 newborn) in totally exposed females. The biased sex ratio in response to chemical cues did not show consistent relationships with maternal body weight, parity or litter size. Although the intrinsic mechanisms involved in sex-biased conceptions are not known, chemical cues could interact with the photoperiodic control of gonadotropin secretions. Received: 14 January 1995/Accepted after revision: 26 November 1995     

Optional strategies for reduced metabolism in gray mouse lemurs

Among the order of primates, torpor has been described only for the small Malagasy cheirogaleids Microcebus and Cheirogaleus. The nocturnal, gray mouse lemur, Microcebus murinus (approx. 60 g), is capable of entering into and spontaneously arousing from apparently daily torpor during the dry season in response to reduced temperatures and low food and water sources. Mark–recapture studies indicated that this primate species might also hibernate for several weeks, although physiological evidence is lacking. In the present study, we investigated patterns of body temperature in two free-ranging M. murinus during the austral winter using temperature-sensitive data loggers implanted subdermally. One lemur hibernated and remained inactive for 4 weeks. During this time, body temperature followed the ambient temperature passively with a minimum body temperature of 11.5°C, interrupted by irregular arousals to normothermic levels. Under the same conditions, the second individual displayed only short bouts of torpor in the early morning hours but maintained stable normothermic body temperatures throughout its nocturnal activity. Reduction of body temperature was less pronounced in the mouse lemur that utilized short bouts of torpor with a minimum value of 27°C. Despite the small sample size, our findings provide the first physiological confirmation that free-ranging individuals of M. murinus from the humid evergreen littoral rain forest have the option to utilize short torpor bouts or hibernation under the same conditions as two alternative energy-conserving physiological solutions to environmental constraints.