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.     

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 (T _sk ) 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 (T _a ) 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 T _a 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.     

Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar

We investigated whether or not habitat structure contributes to the separation of two sister species of lemurs and their hybrids. For this, we studied Microcebus murinus and M. griseorufus along a continuous vegetation gradient where populations of the two species occur in sympatry or in allopatry. In allopatry, the two species are generalists without any sign of microhabitat selectivity. In sympatry, both species differed significantly and discriminated against certain habitat structures: M. murinus was found in microhabitats with larger trees than average while M. griseorufus utilized microhabitats with smaller trees. Hybrids between the two species did not show any significant discrimination for or against microhabitat structure and did not differ in their habitat utilization from either parent species. Both species can go into torpor and hibernation. M. griseorufus is seen more frequently during the cool dry season than M. murinus. We assume that M. murinus goes into extended torpor or hibernation more frequently than M. griseorufus. We interpret the different occurrence of large-sized trees in microhabitats of M. murinus as a prerequisite for M. murinus to be able to spend extended periods of time in tree holes that are isolated and allow hibernation at reduced temperature levels.     

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

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 (T _sk) 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 (T _a) 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 T _sk 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 T _sk and T _a (r ²=0.37) and with torpor bout length (r ² =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. Accepted: 29 August 2000     

Habitat Utilization of Three Sympatric Cheirogaleid Lemur Species in a Littoral Rain Forest of Southeastern Madagascar

I compared the habitat utilization in 3 sympatric species of Cheirogaleidae (Microcebus murinus [81 g], Cheirogaleus medius [183 g] and Cheirogaleus major [362 g]) in a littoral rain forest in southeastern Madagascar during 3 rainy seasons. Females of promiscuous Microcebus murinus had small home ranges and the males had large overlapping home ranges. Home ranges of family groups of monogamous Cheirogaleus medius and C. major overlapped extensively. Home ranges of all 3 species overlapped completely in the study area but home range sizes differed among species and correlate positively with body masses. Male Microcebus murinus slept in open vegetation (79%) and alone (71%), whereas female M. murinus and family group members of Cheirogaleus spp. preferred communal sleeping in tree holes. There are significant interspecific differences in the choice of sleeping sites: smaller lemurs chose smaller trees and used more sleeping sites than larger lemurs did. Species also differed significantly in the vertical dimension of forest utilization: Cheirogaleus major used the upper part of the trees, C. medius used the middle parts, and Microcebus murinus used the understory during nocturnal activities. The 3 species differed mainly in vertical habitat utilization and showed vertical stratification.     

Energetics of tropical hibernation

In this field study, the energetic properties of tropical hibernation were investigated by measuring oxygen consumption and body temperature of the Malagasy primate Cheirogaleus medius in their natural hibernacula. These lemurs use tree holes with extremely varying insulation capacities as hibernacula. In poorly insulated tree holes, tree hole temperature and body temperature fluctuated strongly each day (between 12.8 and 34.4°C). The metabolic rate under these conditions also showed large daily fluctuations between about 29.0 ml O₂/h and 97.9 ml O₂/h in parallel with changes in body temperature. In well insulated tree holes in very large trees on the other hand, tree hole temperature and body temperature remained relatively constant at about 25°C. Lemurs hibernating in these tree holes showed a more constant metabolic rate at an intermediate level, but hibernation was interrupted by repeated arousals with peak metabolic rates up to 350 ml O₂/h. The occurrence of these spontaneous arousals proved that the ability for thermoregulation persists during hibernation. Arousals were energetically costly, but much less so than in temperate and arctic hibernators. Despite the decisive influence of tree hole properties on the pattern of body temperature and metabolic rate during hibernation, the choice of the hibernaculum does not seem to be of energetic importance. The overall energetic savings by tropical hibernation amounted to about 70% as compared to the active season (31.5 vs. 114.3 kJ/d). Therefore, tropical hibernation in C. medius is an effective, well-regulated adaptive response to survive unfavourable seasons.     

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

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 (T _b) 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 T _b of animals increased from the torpor T _b minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise T _b 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 T _bs, 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. Received: 8 July 1999 / Accepted: 3 December 1999     

Switching from negative to positive density-dependence among populations of a cobble beach plant

Understanding the co-occurrence of ecologically similar species remains a puzzling issue in community ecology. The species-rich mouse lemurs (Microcebus spec.) are distributed over nearly all remaining forest areas of Madagascar with a high variability in species distribution patterns. Locally, many congeneric species pairs seem to co-occur, but only little detailed information on spatial patterns is available. Here, we present the results of an intensive capture-mark-recapture study of sympatric Microcebus berthae and M. murinus populations that revealed small-scale mutual spatial exclusion. Nearest neighbour analysis indicated a spatial aggregation in Microcebus murinus but not in M. berthae. Although the diet of both species differed in proportions of food categories, they used the same food sources and had high feeding niche overlap. Also, forest structure related to the spatial distribution of main food sources did not explain spatial segregation because parts used by each species exclusively did not differ in density of trees, dead wood and lianas. We propose that life history trade-offs that result in species aggregation and a relative increase in the strength of intra-specific over inter-specific competition best explain the observed pattern of co-occurrence of ecologically similar congeneric Microcebus species.     

Evidence of prolonged torpor in Goodman’s mouse lemurs at Ankafobe forest,central Madagascar

The small-bodied mouse lemurs of Madagascar (Microcebus) are capable of heterothermy (i.e., torpor or hibernation). The expression of these energy-saving strategies has been physiologically demonstrated in three species: M. berthae, the pygmy mouse lemur (daily torpor), M. murinus, the gray mouse lemur (daily torpor and hibernation), and M. griseorufus, the reddish-gray mouse lemur (daily, prolonged torpor and hibernation). Additional evidence, based on radiotracking and seasonal body mass changes, indicated that mouse lemur capabilities for heterothermy extended to M. lehilahytsara, the Goodman’s mouse lemur. In this study, we confirm the use of hibernation in Goodman’s mouse lemurs at a new location, a high-plateau forest fragment in Ankafobe, central Madagascar. Our evidence is based on sleeping site monitoring of radiocollared individuals and the retrieval of three mouse lemurs from inside a tree hole, all of which displayed a lethargic state. Though our data are preliminary and scant, we show that hibernation occurs in high-plateau mouse lemurs, and suggest that a buffered environment (i.e., tree holes instead of nests) may be crucial to avoiding potentially extreme ambient temperatures.     

Taxonomic Revision of Mouse Lemurs (Microcebus) in the Western Portions of Madagascar

The genus Microcebus (mouse lemurs) are the smallest extant primates. Until recently, they were considered to comprise two different species: Microcebus murinus, confined largely to dry forests on the western portion of Madagascar, and M. rufus, occurring in humid forest formations of eastern Madagascar. Specimens and recent field observations document rufous individuals in the west. However, the current taxonomy is entangled due to a lack of comparative material to quantify intrapopulation and intraspecific morphological variation. On the basis of recently collected specimens of Microcebus from 12 localities in portions of western Madagascar, from Ankarana in the north to Beza Mahafaly in the south, we present a revision using external, cranial, and dental characters. We recognize seven species of Microcebus from western Madagascar. We name and describe 3 spp., resurrect a previously synonymized species, and amend diagnoses for Microcebus murinus (J. F. Miller, 1777), M. myoxinus Peters, 1852, and M. ravelobensis Zimmermann et al., 1998.     

Regulation of Torpor in the Gray Mouse Lemur:Transcriptional and Translational Controls and Role of AMPK Signaling

The gray mouse lemur (Microcebus murinus) is one of few primate species that is able to enter daily torpor or prolonged hibernation in response to environmental stresses. With an emerg-ing significance...     

Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (<Emphasis Type="Italic">Microcebus griseorufus</Emphasis>)

Flexibility in physiological processes is essential to adequately respond to changes in environmental conditions. Madagascar is a particularly challenging environment because climatic conditions seem less predictable than in comparative ecosystems in other parts of the world. We used the reddish-gray mouse lemur (Microcebus griseorufus) from the most unpredictable environment in Madagascar as a model to investigate the flexibility of energy saving strategies to cope with the unpredictability of their habitat. For this we measured T _sk of free-ranging mouse lemurs throughout the year using temperature data loggers. M. griseorufus showed a very strong seasonal as well as an individual flexibility in thermoregulation. During the rainy season all M. griseorufus remained normothermic. At the beginning of the dry season individuals started to exhibit different energy saving strategies: irregular short torpor bouts, regular daily torpor, prolonged torpor of a few days, and hibernation over several weeks. The accumulation of sufficient seasonal body fat was the crucial factor determining the thermal behavior of individuals. The observed intraspecific and sex independent variation in thermoregulatory patterns within one population inhabiting the same small geographical area is exceptional and gives M. griseorufus the ability to respond to current environmental as well as individual conditions. This thermal plasticity might be seen as a key to success and survival for M. griseorufus in an extremely unpredictable environment.     

Factors affecting the daily rhythm of body temperature of captive mouse lemurs (<Emphasis Type="Italic">Microcebus murinus</Emphasis>)

Microcebus murinus, a small nocturnal Malagasy primate, exhibits adaptive energy-saving strategies such as daily hypothermia and gregarious patterns during diurnal rest. To determine whether ambient temperature (T_a), food restriction and nest sharing can modify the daily body temperature (T_b) rhythm, T_b was recorded by telemetry during winter in six males exposed to different ambient temperatures (T_a=25, 20, 15°C) and/or to a total food restriction for 3 days depending on social condition (isolated versus pair-grouped). At 25°C, the daily rhythm of T_b was characterized by high T_b values during the night and lower values during the day. Exposure to cold significantly decreased minimal T_b values and lengthened the daily hypothermia. Under food restriction, minimal T_b values were also markedly lowered. The combination of food restriction and cold induced further increases in duration and depth of torpor bouts, minimal T_b reaching a level just above T_a. Although it influenced daily hypothermia less than environmental factors, nest sharing modified effects of cold and food restriction previously observed by lengthening duration of torpor but without increasing its depth. In response to external conditions, mouse lemurs may thus adjust their energy expenditures through daily modifications of both the duration and the depth of torpor.     

Modulation of Gene Expression in Key Survival Pathways During Daily Torpor in the Gray Mouse Lemur,Microcebus murinus

A variety of mammals employ torpor as an energy-saving strategy in environments of marginal or severe stress either on a daily basis during their inactive period or on a seasonal basis during prolonged...     

Seasonal Fluctuations in Body Fat and Activity Levels in a Rain-Forest Species of Mouse Lemur,Microcebus rufus

Seasonal fattening in preparation for the dry season followed by torpor characterizes some members of the family Cheirogaleidae, a group of < 600-g nocturnal Malagasy primates. These behaviors are associated with extreme seasonality in dry forests, where most studies have been conducted. I aimed to determine if the brown mouse lemur (Microcebus rufus), a rain-forest species of cheirogaleid, exhibited similar changes. Between January 1993 and May 1994 I conducted a mark-recapture study on Microcebus rufus in the rain forest of Ranomafana National Park. I monitored body weight and tail circumference for body fat fluctuations and inferred changes in activity levels from presence or absence in the traps. Some individuals of both sexes increased body fat and entered torpor as suggested by their absence from traps for at least 1 month of the dry season. Activity was resumed with body weight reduced by 5–35 g, and tail circumference by 0.4–1.2 cm. Population-level analysis supports these results; highest weight and tail circumference values occurred just before and at the onset of the dry season. Other individuals, predominantly male, exhibited no change in body fat or activity level, and some mouse lemurs increased their body fat over the course of the dry season. Age, social status, and individual response may influence seasonal behavioral strategies. Dry and rain-forest species of mouse lemur adopt similar behaviors to cope with environmental stresses. Mouse lemurs resemble nonprimate, small-bodied mammals, in which behavioral changes related to maintaining energy balance occur during seasonally unfavorable conditions.     

Social System of <Emphasis Type="Italic">Microcebus berthae</Emphasis>, the World’s Smallest Primate

Our goal was to provide a first characterization of the social system of pygmy mouse lemurs (Microcebus berthae), the worlds smallest primate species. During a 4-mo field study of 12 females and 27 males, we combined capture-recapture and morphometric data with detailed behavioral observations of individually marked subjects and genetic paternity analyses of a population in Kirindy Forest, western Madagascar. We describe the social organization of Microcebus berthae as a solitary forager living in an individualized neighborhood system characterized by extensive intra- and intersexual home range overlap of adult individuals within a male-biased population. Male and female pygmy mouse lemurs inhabited home ranges (males: 4.9 ha; females: 2.5 ha) that are more than twice as large as those of sympatric Microcebus murinus. On average, pygmy mouse lemurs of both sexes spent about half of the days sleeping alone. Preliminary analysis of genetic population structure suggests female philopatry and male dispersal. Sleeping associations of variable composition that consisted not preferentially of close relatives and proximity during part of the nightly activity contributed together with regular social interactions to the maintenance of a social network. The spatial distribution pattern of adult males and females, the absence of sexual size dimorphism, relatively large male testicular volume and moderate female estrous synchrony suggest a promiscuous mating system with a high potential for scramble competition. In general, there are many similarities between the social system of Microcebus berthae and those of other Microcebus spp. However, striking differences with sympatric gray mouse lemurs (Microcebus murinus) in female home range size, dispersion and sleeping behavior indicate the existence of species-specific socioecological adaptations in closely related species occupying very similar ecological niches.     

Hibernation in the tropics: lessons from a primate

The Malagasy primate Cheirogaleus medius hibernates in tree holes for 7 months, although ambient temperatures during hibernation rise above 30°C in their natural environment. In a field study we show that during hibernation the body temperature of most lemurs fluctuates between about 10°C and 30°C, closely tracking the diurnal fluctuations of ambient temperature passively. These lemurs do not interrupt hibernation by spontaneous arousals, previously thought to be obligatory for all mammalian hibernators. However, some lemurs hibernate in large trees, which provide better thermal insulation. Their body temperature fluctuates only little around 25°C, but they show regular arousals, as known from temperate and arctic hibernators. The results from this study demonstrate that maximum body temperature is a key factor necessitating the occurrence of arousals. Furthermore, we show that hibernation is not necessarily coupled to low body temperature and, therefore, low body temperature should no longer be included in the definition of hibernation.     

Cytokine and Antioxidant Regulation in the Intestine of the Gray Mouse Lemur (Microcebus murinus) During Torpor

During food shortages, the gray mouse lemur (Microcebus murinus) of Madagascar expe-riences daily torpor thereby reducing energy expenditures. The present study aimed to understand the impacts of torpo...     

Molecular Evidence of Reproductive Isolation in Sympatric Sibling Species of Mouse Lemurs

Recent morphological and molecular phylogenetic studies of mouse lemurs (Microcebus) living in the western and southern regions of Madagascar have shown that specific diversity had been considerably underestimated. In large part, this underestimate was due to the lack of sufficient specimens from given localities to assess properly the level of phenotypic variation within and between populations. The accurate delineation of specific boundaries has no doubt been confounded by the diminutive size, nocturnal habits, and subtle morphological variation characteristic of mouse lemurs, which can make field identification of individuals problematic. We illustrate the use of molecular phylogenetic analysis to reveal reproductive isolation in two sympatric mouse lemur species, Microcebus murinus and M. griseorufus. Their documentation in the Berenty Private Reserve in the extreme south of Madagascar verifies the historically-broad distribution of Microcebus griseorufus, a species recently resurrected from synonomy.     

Relationship Between Microhabitat Structure and Distribution of Mouse Lemurs (Microcebus spp.) in Northwestern Madagascar

Understanding processes affecting the distribution and abundance of organisms is a central issue in ecology and conservation biology. In northwestern Madagascar, we found an uneven distribution pattern of the golden-brown mouse lemur (Microcebus ravelobensis) and the grey mouse lemur (M. murinus). In one area (JBA) the two species lived sympatrically, whereas in another forest area (JBB) Microcebus ravelobensis occurred exclusively. To investigate whether differences in forest structure may explain this uneven distribution, we conducted a microhabitat analysis and related it to specific distribution. In JBA the habitat of Microcebus ravelobensis was characterized by a higher percentage of trees with many lianas and a higher cover of the herb layer, whereas that of M. murinus had a higher number of trees with a diameter at breast height (DBH) >10 cm. The comparison of the forest structure of the microhabitats of the two species between JBA and JBB revealed further differences. The cover of the overstory, the percentage of trees without lianas and the number of larger trees (DBH >10 cm) among the microhabitats were higher for Microcebus murinus in JBA than for M. ravelobensis in JBB whereas the microhabitats of M. ravelobensis at the two sites did not differ concerning these vegetation structures. Differences between the two species coincide with those of resources important for survival. Our results indicate the importance of microhabitat analyses for the understanding of distribution patterns of species and for successful conservation planning.