Diet of the Brown Mouse Lemur (Microcebus rufus) in Ranomafana National Park, Madagascar

The conventional notion is that small-bodied primates should be highly insectivorous in order to obtain protein and other nutrients from a food source that is more easily digestible than plant matter. I studied feeding behavior of Microcebus rufus for 16 months in the east coast rainforest of Ranomafana National Park. I determined the diet primarily through analysis of 334 fecal samples from live-trapped individuals. They consumed a mixed diet basically of fruit and insects year-round. I identified 24 fruits, while 40–52 remain unidentified. Bakerella, a high-lipid epiphytic semiparasitic plant, was in 58% of fecal samples that contained fruit seeds, and was consumed year-round irrespective of general resource availability. It served both as a staple and keystone resource. Fruit was less frequently totally absent from fecal samples of individual mouse lemurs than insect matter was. For Microcebus rufus, fruit may be a primary source of energy, not just complementary to insects. Fruit consumption increased in quantity and diversity during the latter part of the rainy season and the very early part of the dry season, when fruit production was relatively high. This pattern in fruit feeding is similar to that for mouse lemurs in the west coast dry forests and is related to specific nutritional needs dictated by the highly seasonal character of the life cycle. Coleoptera were present in 67% of samples examined and were consumed year-round by the subjects, but insect consumption did not increase during the rainy season when insect abundance was highest.     

Spatial distribution and population composition of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar, and its implications for social organization

Through a 16-mo mark-recapture trap study, I examined aspects of spatial distribution and population composition in the brown mouse lemur, Microcebus rufus, a 42 g nocturnal strepsirhine. The study took place in the rainforest of Ranomafana National Park in southeastern Madagascar. Sherman live traps were set monthly for a variable number of nights in a quasi-grid 50 m apart. Captured individuals were marked for future identification and released at site of capture. More males than females were captured overall (102 versus 72) and at 83% of trap sites. Trap sex ratio fluctuated significantly over the course of the study. It was particularly male-biased between June and August (3.9:1), when more previously uncaptured males than females (14 versus 6) entered the trap population. Some of these males remained in the trap population. Although the average number of individuals captured was not significantly different between the first four and last four months of the study, the composition of the population changed. The female population, however, changed less: 28.9% of all females captured in the first four months of the study were recaptured in the last four months, compared to 9.7% of males. It is suggested that the pattern of appearance of new individuals and disappearance of others, both predominantly male, may indicate migratory activity. Furthermore, an average of eight individuals were captured at each trap site (approximately 70% of traps captured more than five), suggesting a high degree of spatial overlap. The average number of male and female individuals captured in each trap (5.5 males versus 2.5 females), the average number of trap sites at which males and females were captured (3.6 versus 2.4), and the average number of captures for males and females (9.8 versus 5.7) all differed significantly between the sexes.     

Assessing reproductive profiles in female brown mouse lemurs (Microcebus rufus) from Ranomafana National Park,southeast Madagascar,using fecal hormone analysis

Studies on reproductive endocrinology in wild primate populations have greatly increased in the last decades owing to the development of noninvasive techniques that can be applied under field conditions. However, small‐bodied nocturnal species are not well represented on the long list of primates surveyed in the wild, and reproductive inferences regarding these animals in their natural habitats have not benefited from direct observations of hormonal changes. We collected fecal samples from female brown mouse lemurs (Microcebus rufus) in a southeastern rainforest of Madagascar in order to determine whether or not fecally excreted steroid levels show a consistent pattern of change during the reproductive season and are a useful complement to reproductive observations in wild‐trapped individuals. Initial data show variation in reproductive hormone levels before and after estrus and estimated day of parturition. Elevated levels of excreted estradiol (E₂) were observed around the time of estrus, whereas high levels of fecal progesterone (P) were seen during later stages of pregnancy and around parturition. A more complete picture of reproductive profiles in female mouse lemurs, and how they may change over the life span, can be obtained if hormone analyses are used to supplement field observations. Am. J. Primatol. 71:439–446, 2009. © 2009 Wiley‐Liss, Inc.     

Timely estrus in wild brown mouse lemur females at Ranomafana National Park, southeastern Madagascar

The small-bodied nocturnal mouse lemurs (genus Microcebus) occupy a variety of habitats in Madagascar. Gray (M. murinus) and brown (M. rufus) mouse lemurs have been widely studied both in the wild and captivity. Whereas captive studies revealed an endogenous regulation of reproduction entrained by photoperiod, field studies have suggested that reproductive activation could be affected by additional climatic, physical, or social conditions. I collected data on wild brown mouse lemur females at Ranomafana between 2004 and 2008 to determine: 1) the timing of estrus and estrous periodicities across multiple seasons, and 2) whether additional factors such as body mass, age, or rainfall are correlated with onset of reproduction. In mouse lemur females at Ranomafana, the first seasonal estrus occurs 3-4 weeks after the vernal equinox. I report ~1 month's intra-population variation in the timing of estrus and inter-annual estrous intervals with periodicities of ~365 days. There were significant differences between the onset of reproduction across years. Estrous onset was uncorrelated with body mass, but there was an apparent age effect. There was a significant negative correlation between August rainfall and onset of reproduction when 2004 data were removed from the analysis. Results from this study are consistent with the notion that timing of estrus is photoperiod-dependent. As in captivity, intra-population variation in estrous onset is ~4 weeks in length. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments.     

Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur ( Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur ( Microcebus rufus) in Eastern Madagascar

To investigate for the first time the relationship between contrasting patterns of seasonal changes of the environment and activity, body mass and reproduction for small nocturnal primates in nature, we compared a population of golden brown mouse lemur (Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar and of the brown mouse lemur (Microcebus rufus) in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions. Golden brown mouse lemurs (GBML) were active during the whole period (May to December) irrespective of changing environmental conditions. In contrast, a part of the population of brown mouse lemurs (BML) showed prolonged seasonal torpor, related to body mass during periods of short day length and low ambient temperatures. Differences between species might be due to differences in ambient temperature and food supply. Body weight and tail thickness (adipose tissue reserve) did not show prominent differences between short and long photoperiods in GBML, whereas both differ significantly in BML, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species showed a seasonal reproduction. The rate of growth and size of the testes were similar and preceded estrous onset in both species suggesting a photoperiodic control of reproduction in males. The estrous onset in females occurred earlier in GBML than in BML. Estrous females were observed over at least 4 months in the former, but in only 1 month in the latter species. Intraspecific variation of estrous onset in GBML may be explained by body mass. Interspecific variation of female reproduction indicates species-specific differences in the control of reproduction. Thus, environmentally related differences in annual rhythms between closely related small nocturnal lemurs emerged that allow them to cope with contrasting patterns of seasonal changes in their habitats.     

Aspects of reproduction in the eastern rufous mouse lemur (Microcebus rufus) and their implications for captive management

The eastern rufous mouse lemur is one of the smallest primate species. It inhabits the eastern rain forest of Madagascar. Its reproductive biology has not been examined because of its rarity in laboratories. We present the first data on reproduction and variation in reproductive success from a breeding colony of wild‐caught Microcebus rufus. The eastern rufous mouse lemur shows a seasonal change in testicular size and in the occurrence of estrus. Females had 2.5 cycles (range, one to four) per season. The estrous cycle length was 59 days (range, 51–66), the duration of vaginal opening during estrus was 7.5 days (range, 5–8), receptivity occurred on the third day of estrus, gestation length was 56.5 days (range, 56–57), litter size was two neonates (range, one to three). The frequency and duration of mating behavior varied widely among the pairs. Copulation seemed to occur on a single day per estrus within the first to fourth hour after light change to red light. In four cases (three pairs), copulation lasted between 15 and 240 seconds. Breeding success can be increased by choosing mates carefully. Microcebus rufus seems to be a seasonal breeder like its sibling species Microcebus murinus. In wild‐caught animals, males seemed to adapt quickly (first season) to the conditions of captivity, whereas in the females, individual variation (first to third season) in reproductive activity was observed. Air humidity of >60% seems to facilitate the breeding success in wild‐caught pairs. First pregnancy and successful rearing of offspring occurred in the second and fourth year of captivity in two of three females. Wild‐caught eastern rufous mouse lemurs seemed to demonstrate variation in adapting to the conditions of captivity with regard to sex and individuality. Zoo Biol 20:157–167, 2001. © 2001 Wiley‐Liss, Inc.     

Similarities,differences, and seasonal patterns in the diets ofEulemur rubriventer andEulemur fulvus rufus in the Ranomafana National Park,Madagascar

I studied the diets of two sympatric species ofEulemur (E. fulvus rufus andE. rubriventer) in the Ranomafana National Part in southeastern Madagascar from July 1988 through August 1989. Both species were highly frugivorous throughout the year and devoted similar amounts of time to feeding daily; the composition of their diets were similar. Three aspects of both lemur species' diets were correlated with seasonal food availability: changes in interspecific dietary overlap, the length of feeding bouts, and the amount of time devoted to feeding daily. Throughout the year neither species had a more diverse or more folivorous diet than its sympatric congener. However, there were several consistent year-round differences between their diets.E. f. rufus initiated more feeding bouts daily that were shorter in duration than those ofE. rubriventer. E. f. rufus also consistently exploited more unripe fruits and mature leaves thanE. rubriventer did throughout the study.E. f. rufus migrated from the study site during a period of fruit scarcity. These dietary patterns are discussed here in regard to feeding patterns observed in other sympatric congeneric primate species, whether these dietary differences can contribute to these two species' ability to coexist, and how differences in diet may be influenced by differences in social structure. I suggest that subtle, consistent differences in diet and seasonal dietary differences are sufficient to allow these two species to coexist.     

Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar

The mating system and social organization of the gray mouse lemur (Microcebus murinus) was investigated in two three-month field studies (covering a period before, during, and after the first mating season) in Ampijoroa, northwestern Madagascar. The spatial and temporal distribution of the sexes within a population was studied using mark/recapture techniques and radiotelemetry to assess possible contest or scramble competition between the males. Sociality was inferred from the occurrence and probability of nocturnal social encounters, the temporal stability of daily sleeping groups, and nocturnal ranging patterns of co-sleepers. Males and females were evenly distributed in the study area within a network of highly overlapping home ranges. No indications were found for the spatial monopolization of the females by certain dominant males. Males and females had spatial access to several potential mates; the mating system is therefore characterized as a multi-male/multi-female system. Male home range sizes increased during the first mating season, which was interpreted as an indicator for scramble competition between the males. Competitive mate searching, sperm competition, and temporary mate guarding as well as female mate choice are suggested as the most probable reproductive strategies. Over the course of the study the animals lived continually within the study area, and most females formed stable individualized sleeping associations. Females that slept together shared a higher percentage of their home range than did females that slept at different sites. It is suggested that this network of social relationships should be described as a dispersed but individualized neighborhood.     

Social organization of the golden brown mouse lemur (Microcebus ravelobensis)

Our study provides the first data on the social organization of the golden brown mouse lemur, a nocturnal primate discovered in northwestern Madagascar in 1994. The study was carried out in two 6-month field periods during the dry season, covering time before and during the mating season. The spatial and temporal distributions of the sexes in the population were investigated by mark/recapture and radiotelemetry. Focal observations and the determination of sleeping associations provided further insights into the sociality of this solitary forager. High intra- and intersexual home-range overlaps occurred throughout the study. In general, individuals of both sexes had spatial access to more than one conspecific of the same and the opposite sex. We found no indication for spatial monopolization of females by certain males. These results suggest a dispersed multimale/multifemale system with a promiscuous mating pattern. Individuals showed temporal stability in their home range locations and interacted regularly with conspecifics. Five sleeping groups were identified during the study period: one female group and four mixed-sex groups. Even though sleeping sites were changed frequently, sleeping-group compositions remained stable over time. Thermoregulatory constraints are the most likely explanation for sleeping-group composition with members of both sexes in this species. Mixed-sex sleeping groups can be described as the basic social unit within this dispersed multimale/multifemale society.     

Lemur habitat and dental senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.     

Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar

We investigated the sleeping site ecology of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar during the second half of the dry season with respect to the type, quality, and usage pattern of the sleeping sites, as well as to social sleeping habits and response to potential threats. The type and quality of the sleeping sites differed between the two species. M. murinus used protected wooden shelters (tree holes) more frequently than M. ravelobensis, and M. ravelobensis used a broader variety of less protected sites (e.g., branches, lianas, and leaves) than M. murinus. Whereas male M. murinus usually slept alone, and female M. murinus mostly slept in groups, both sexes of M. ravelobensis slept in mixed-sex sleeping groups. M. murinus relied on crypsis in their sleeping sites, whereas M. ravelobensis regularly showed a flight response to the approach of an observer. This behavioral difference could indicate an adaptation to a higher predation risk in less protected sleeping sites. Whereas female M. murinus showed a high site fidelity, male M. murinus and both sexes of M. ravelobensis frequently changed their sleeping sites, which may also be interpreted as an antipredator strategy. The results are discussed with respect to three possible ecological explanations: interspecies competition, restricted resource availability, and niche differentiation. The latter is the most likely explanation for these interspecific differences.     

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     

Experimental evidence for olfactory predator recognition in wild mouse lemurs

Although primates have remarkable olfactory capabilities, their ability for olfactory predator recognition is still understudied. We investigated this cognitive ability in wild gray and golden-brown mouse lemurs (Microcebus murinus and M. ravelobensis) that were confronted with four different olfactory stimuli, derived from two Malagasy predators (fossa and barn owl) and two local nonpredator species (brown lemur and sifaka). The predator response was tested (1) in a systematic cage setup and (2) in a two-way choice experiment with two Sherman traps on platforms in the forest (stimulus trap vs. nonstimulus trap). For part 1, the study animals were housed in cages during habituation and 5 days of experiments. One stimulus was tested per night and was presented underneath a drinking bottle. The changes in the time spent close to the stimulus and the drinking time at the bottle were used as indicators of predator recognition. A timidity score was established by classifying the strength of the antipredator response during the experiment. The study animals spent significantly less time drinking and less time in the stimulus area when confronted with fossa odor compared with the other stimuli. The timidity score was significantly higher during the fossa stimulus compared with the nonpredator and the control stimuli. The two-way choice experiments revealed a complete avoidance of the fossa odor, which was not found with the other stimuli. Thus, wild mouse lemurs showed clear signs of olfactory predator recognition in the case of the fossa in both experiments, but no signs of avoidance to the other presented stimuli. The lack of owl avoidance may be explained by less or no aversive metabolites in the owl stimulus or by lower significance for olfactory recognition of aerial predators. Furthermore, the results showed slight differences between the two mouse lemur species that may be linked to differences in their ecology.     

Patterns of male scent-marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

Scent-marking behavior has been well documented in many primate species. Three common functions attributed to scent-marking in males of multi-male/multi-female lemur species include: 1) advertisement of individual identity, 2) territorial defense, and 3) reproductive suppression. We examined the average number of scent-marks per hour exhibited daily by adult male sifakas (Propithecus edwardsi) and found that patterns of scent-marking changed with season, natal status, and dominance status. Males in single-male groups scent-marked at the highest rate, followed by dominant males, males of equal status, and subordinate males. Non-natal males generally scent-marked at higher rates than natal males, and adult males living in a natal group without a parent marked at higher rates than males living with a parent. All males scent-marked at higher rates in the migration season compared to the other seasons. These patterns were consistent with territorial defense and advertisement to females, and the suggestion that these chemical signals impart information concerning status. Since scent-marking behavior tracked seasons and varied with both dominance and natal status, it may serve multiple functions in males.     

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

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. Accepted: 2 November 1999     

Reproductive Schedules of Female <Emphasis Type=Italic>Microcebus rufus</Emphasis> at Ranomafana National Park,Madagascar

I examined the reproductive status of female brown mouse lemurs (Microcebus rufus) from October 2005 to early January, 2006 at Ranomafana National Park, an eastern rain forest in Madagascar. I employed intensive capture/mark/recapture techniques to track individual changes in vaginal morphology and body mass and collected vaginal smears for individuals with open vaginas. I observed moderate estrous synchrony (vaginal openings between October 11 and November 18), with clusters of females showing strong estrous synchrony (6 of 15 on or around October 15, and 3 of 15 on or around October 25). My findings weakly support the proximity hypothesis—that closer females will enter estrus simultaneously—and offer virtually no support for the notion that body mass influences the timing of estrus in brown mouse lemurs. Females gave birth during the second and third weeks of December. Two females showing signs of abortion or perinatal death of offspring also showed renewed vaginal swelling in late December, suggesting that some form of polyestry, i.e., as reproductive compensation for infant loss, exists at Ranomafana. I discuss the implications of the data, in conjunction with other evidence of polyestry in wild mouse lemurs, in light of data on patterns of seasonality at Ranomafana and other sites. More data are needed to determine the frequency and pattern of polyestry in Microcebus rufus.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.