Jutta Schmid

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.

Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor

Abstract We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (Tsk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (Ta) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7–8.9 h with a daily mean of 3.4 h, and their Tsk s fell to a minimum of 18.8 °C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 ± 65.4 kJ day−1) was about the same of that of normothermic mouse lemurs in the dry season (115.5 ± 27.3 kJ day−1). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 ± 32.7 kJ day−1 which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between Tsk and Ta (r2=0.37) and with torpor bout length (r2=0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 ± 4.1 ml day−1) was significantly lower than that of mouse lemurs remaining normothermic (19.4 ± 3.8 ml day−1), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus demonstrates that torpor may not only reflect its impact on the daily energy demands, but involve wider adaptive implications such as water requirements.

Spontaneous Daily Torpor in Malagasy Mouse Lemurs

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Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance

Abstract Patterns and energetic consequences of spontaneous daily torpor were measured in the gray mouse lemur (Microcebus murinus) under natural conditions of ambient temperature and photoperiod in a dry deciduous forest in western Madagascar. Over a period of two consecutive dry seasons, oxygen consumption (VO2) and body temperature (Tb) were measured on ten individuals kept in outdoor enclosures. In all animals, spontaneous daily torpor occurred on a daily basis with torpor bouts lasting from 3.6 to 17.6 h, with a mean torpor bout duration of 9.3 h. On average, body temperatures in torpor were 17.3±4.9°C with a recorded minimum value of 7.8°C. Torpor was not restricted to the mouse lemurs’ diurnal resting phase: entries occurred throughout the night and arousals mainly around midday, coinciding with the daily ambient temperature maximum. Arousal from torpor was a two-phase process with a first passive, exogenous heating where the Tb of animals increased from the torpor Tb minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise Tb to normothermic values. Metabolic rate during torpor (28.6±13.2 ml O2 h–1) was significantly reduced by about 76% compared to resting metabolic rate (132.6±50.5 ml O2 h–1). On average, for all M. murinus individuals measured, hypometabolism during daily torpor reduced daily energy expenditure by about 38%. In conclusion, all these energy-conserving mechanisms of the nocturnal mouse lemurs, with passive exogenous heating during arousal from torpor, low minimum torpor Tbs, and extended torpor bouts into the activity phase, comprise an important and highly adapted mechanism to minimize energetic costs in response to unfavorable environmental conditions and may play a crucial role for individual fitness.

Tree Holes Used for Resting by Gray Mouse Lemurs (Microcebus murinus) in Madagascar: Insulation Capacities and Energetic Consequences

I studied the insulation capacity of tree holes used by gray mouse lemurs (Microcebus murinus) in a primary dry deciduous forest in western Madagascar during the cool dry season. Tree holes had an insulating effect, and fluctuations of air temperatures were less extreme inside the holes than outside them. The insulation capacity of the tree holes peaked between 0800 and 1100 hr, when ambient temperatures ranged between 25 and 30°C. To compare tree holes, I calculated the mean difference between the internal temperature )(Ti) and the external temperature (Te) for each tree hole. Thus large differences indicate good insulation capacities. The mean difference of tree holes in living trees was significantly larger than that of tree holes in dead trees, which shows that insulation in living trees is more effective. During the dry season, the insulation capacity of tree holes in living trees decreased and was lowest in July, whereas the insulation capacity of holes in dead trees remained approximately constant. Physiological studies under natural temperature and light condition in Microcebus murinus reveal that daily torpor saves around 40% of the daily energy expenditure compared to normothermia. However, torpor can be maintained only up to the threshold body and ambient temperature of 28°C, whereat Microcebus murinus have to terminate torpor actively. By occupying insulating tree holes, mouse lemurs may stay longer in torpor, which increases their daily energy savings by an extra 5%.

Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar

Abstract Thermoregulation, energetics and patterns of torpor in the pygmy mouse lemur, Microcebus myoxinus, were investigated under natural conditions of photoperiod and temperature in the Kirindy/CFPF Forest in western Madagascar. M. myoxinus entered torpor spontaneously during the cool dry season. Torpor only occurred on a daily basis and torpor bout duration was on average 9.6 h, and ranged from 4.6 h to 19.2 h. Metabolic rates during torpor were reduced to about 86% of the normothermic value. Minimum body temperature during daily torpor was 6.8 °C at an ambient temperature of 6.3 °C. Entry into torpor occurred randomly between 2000 and 0620 hours, whereas arousals from torpor were clustered around 1300 hours within a narrow time window of less than 4 h. Arousal from torpor was a two-step process with a first passive climb of body temperature to a mean of 27 °C, carried by the daily increase of ambient temperature when oxygen consumption remained more or less constant, followed by a second active increase of oxygen consumption to further raise the body temperature to normothermic values. In conclusion, daily body temperature rhythms in M. myoxinus further reduce the energetic costs of daily torpor seen in other species: they extend to unusually low body temperatures and consequently low metabolic rates in torpor, and they employ passive warming to reduce the energetic costs of arousal. Thus, these energy-conserving adaptations may represent an important energetic aid to the pygmy mouse lemur and help to promote their individual fitness.

Different Population Dynamics of Microcebus murinus in Primary and Secondary Deciduous Dry Forests of Madagascar

The goal of this study was to identify causes for lower population densities of mouse lemurs (Microcebus murinus) in secondary than in primary dry deciduous forests of western Madagascar. Variations in the abundance of Microcebus murinus are linked to the capacity to enter energy-saving torpor during the dry season. Under natural conditions in primary forest, Microcebus murinus can maintain daily torpor (and possibly hibernation) as long as body temperatures remain below 28°C. Females are more likely to hibernate than males, resulting in skewed sex ratios of captured Microcebus murinus in the primary forest. In the secondary forest the sex ratio of subjects captured during the dry season is more balanced than in primary forest, indicating that fewer females go into torpor in secondary than in primary forest. Secondary forests have fewer large standing or fallen trees that might provide holes as shelter for Microcebus murinus. Ambient temperatures are higher in secondary than in primary forests and higher outside than inside tree holes. These high ambient temperatures might hinder the ability of Microcebus murinus to maintain torpor for prolonged periods in secondary forests. Mouse lemurs from secondary forest have lower body mass than in primary forest. The year-to-year recapture rate is zero in secondary forest and thus significantly lower than in primary forest. This indicates that survival rates are lower in secondary than in primary forests. Thus, secondary forests may be of limited value as buffer zones or even corridors for mouse lemurs.

Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar

The gray mouse lemur ( Microcebus murinus ) is a small, nocturnal primate endemic to Madagascar and has evolved specific activity patterns to survive the dry season, a period of low food availability and low ambient temperatures. These patterns are sex-specific. I determined seasonal fluctuations of body mass and tail circumference in M. murinus under natural conditions in a dry deciduous forest of western Madagascar in 1994–1995. I compared those variables among individuals during different activity patterns. Based on mark-recapture and monitoring of sleeping sites, 73.1% of adult females but only 18.9% of adult males remained inactive for the several weeks to 4—5 months throughout the cool dry season. Inactive females stored fat before the onset of the inactive phase and lost 31.7% of their mass during the dry winter, but inactive males hardly stored fat, and their body mass did not change between onset and end of the period of inactivity. Duration of inactivity was significantly longer for females than males, due to earlier emergence of males. At the end of inactivity and activity periods, respectively, body masses and tail circumferences did not differ between inactive and active males and females. Thus, M. murinus has evolved two different strategies to survive the cool dry season: being generally active but combined with daily torpor of <24 h, and remaining inactive for days to several weeks, which might be associated with prolonged bouts of torpor.

Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar

I aimed to determine when and under which seasonal environmental conditions gray mouse lemurs (Microcebus murinus), a small nocturnal primate species endemic to Madagascar, utilize daily torpor. Using temperature-sensitive radio collars, I measured skin temperature (Tsk) of free-ranging mouse lemurs under natural conditions. My results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (Ta) during the dry season, but not during the rainy season. Mouse lemurs that remained normothermic had significantly lower body masses (mean: 59.7 g) than individuals that used torpor (mean: 80.2 g). Skin temperatures dropped to 20.9°C and the mean torpor bout duration is 10.3 h. The use of torpor on a given night varied among individuals, whereas the propensity for torpor did not differ significantly between males and females. I found no evidence that Ta can be used to predict whether mouse lemurs will remain normothermic or enter torpor. It appears that the most reliable indicator for the occurrence of torpor in free-ranging Microcebus murinus is time of the year, i.e., photoperiod.

Field Metabolic Rate and the Cost of Ranging of the Red-Tailed Sportive Lemur (Lepilemur Ruficaudatus)

The goal of this study was to describe energy expenses of free ranging Lepilemur ruficaudatus during the dry season in the deciduous forest of western Madagascar. Since all lemur species measured so far have had very low resting metabolic rates (RMR) and some lemur species can go into daily or prolonged torpor, the question was, whether or not resting metabolic rates can be used to predict field metabolic rates (FMR) in lemurs. Doubly-labeled water measurements of FMR in 11 free-ranging L. ruficaudatus showed that these animals had FMR of about 65.6% of the values expected for FMR of eutherian herbivores of similar body mass (mean mass = 723 g). FMR was on average 2.6-3.1 times higher than RMR that had been measured previously as 63.6% of the expected value for RMR of eutherian mammals of similar body mass. The ratio of FMR/RMR matches the ratio found in other eutherian mammals and is consistent with the idea that FMR is a constant multiple of RMR for eutherian mammals over a wide range of body mass. FMR augmented with increasing range size. The present data do not provide evidence that the costs of locomotion were energetically limiting for L.ruficaudatus.