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.     

Use of Vocal Fingerprinting for Specific Discrimination of Gray (Microcebus murinus) and Rufous Mouse Lemurs (Microcebus rufus)

Advertisement calls are often important noninvasive tools for discriminating cryptic species and for assessing specific diversity and speciation patterns in nature. We investigated the contribution of these calls to uncover specific diversity in nocturnal Malagasy lemurs. We compared sexual advertisement and predator advertisement calls of two mouse lemur species, western gray and eastern rufous mouse lemurs (Microcebus murinus and M. rufus, respectively) living in two contrasting habitats (dry deciduous vs. rain forest), and analyzed them statistically. Both species emitted several highly variable whistle calls in the context of predator-avoidance. Intrapopulation variation was high and overlapped interspecific variation. Sexual advertisement calls, given in the mating context, displayed a totally distinct, species-specific acoustic structure. Whereas gray mouse lemurs produced rapidly multifrequency modulated, long trill calls, rufous mouse lemurs gave slowly frequency-modulated short chirp calls. Our results suggest specific status for gray and rufous mouse lemurs and indicate the importance of predation and social needs in shaping vocal communication.     

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.     

Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.     

Feeding Ecology of Sympatric Mouse Lemur Species in Northwestern Madagascar

We performed a comparative pilot study on vertical space use and feeding ecology of 2 closely related sympatric mouse lemur species in northwestern Madagascar. We recorded feeding behavior and the use of vertical forest strata for 6 gray and 4 golden-brown mouse lemur females that we followed for 120 h. We carried out feeding experiments and analyzed fecal samples for food remains. Both species showed no significant difference in use of forest strata. They had a similar overall diet, with insect secretions and gum as main plant food resources; arthropod remains occurred in about half of all fecal samples. Both lemurs used in common >50% of the plant species that each consumed, which accounts for ≥70% of all individual plants used. However, both species used >40% of their feeding plant species exclusively and seemed to differ in their degree of specialization on certain plant species.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

Dynamics of Estrous Synchrony in Captive Gray Mouse Lemurs (Microcebus murinus)

Estrous synchrony in seasonal breeders can in principle be based on and shaped by environmental, internal, and/or social cues. We analyzed the dynamics of estrous synchrony for the first time in a seasonal, nocturnal primate species, the gray mouse lemur (Microcebus murinus). We compared successive estrous cycles and different levels of spatial proximity over two reproductive seasons in a captive population in order to identify possible social influences on estrous synchrony. The females exhibited a marked estrous synchrony at the beginning of each reproductive season, but we found no indication of a process of socially induced synchronization among them. Females housed in the same cage/room were not more strongly synchronized than females housed in different cages/rooms. Moreover, cycles desynchronized from the first to the second estrus of the season. Estrous cycle length did not depend on age, parity, or social housing conditions, but instead mainly on the individuality of the lemurs. This individuality, shown for the first time in a nocturnal primate species, is likely to be based on an endogenous rhythm with a genetic basis. We discuss possible social advantages, e.g., communal rearing, and disadvantages, e.g., mate choice and female-female competition, of estrous synchrony for nocturnal primates living in a dispersed individualized social network, and propose that a moderate flexibility within the individual cycle lengths probably enables the females to compromise between the different socioecological pressures.     

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.     

Mutual mate choice in a female-dominant and sexually monomorphic primate

Sexual dimorphism is common in polygynous species, where intrasexual competition is often thought to drive the evolution of large male body size, and in turn, male behavioral dominance over females. In Madagascar, the entire lemur radiation, which embraces diverse mating systems, lacks sexual dimorphism and exhibits frequent female dominance over males. The evolution of such morphological and behavioral peculiarities, often referred to as "the lemur syndrome," has proven difficult to understand. Among other hypotheses, a potential role of intersexual selection has been repeatedly proposed but hardly ever tested. Here, we investigate whether female choice favors small and compliant males, and whether male choice favors large females in captive gray mouse lemurs (Microcebus murinus). Detailed analysis of a combination of behavioral observations and hormonal data available for both sexes shows that (1) females accept more matings from males with higher fighting abilities, (2) males adjust their investment in intrasexual competition to female fertility, and (3) both male and female strategies are weakly influenced by the body mass of potential partners, in directions contradicting our predictions. These results do not suggest a prominent role of intersexual selection in the evolution and maintenance of the lemur syndrome but rather point to alternative mechanisms relating to male-male competition, specifically highlighting an absence of relationship between male body mass and fighting ability. Finally, our findings add to the growing body of evidence suggesting flexible sex roles, by showing the expression of mutual mate choice in a female-dominant, sexually monomorphic and promiscuous primate.     

Shortened seasonal photoperiodic cycles accelerate aging of the diurnal and circadian locomotor activity rhythms in a primate

The gray mouse lemur (Microcebus murinus), a prosimian primate, exhibits seasonal rhythms strictly controlled by photoperiodic variations. Previous studies indicated that longevity can be altered by long-term acceleration of seasonal rhythms, providing a model for assessing various aspects of aging. To assess the effect of aging and accelerated aging on the circadian system of this primate, we compared the circadian rhythm of the locomotor activity in adult mouse lemurs (2-4.5 years, n = 9), aged mouse lemurs (5-9 years, n = 10), and adult mouse lemurs that had been exposed from birth to a shortened seasonal photoperiodic cycle (2-4.5 years, n = 7). Compared to adult animals, aged mouse lemurs showed a significant increase in intradaily variability and an advanced activity onset. Aging was characterized by a decrease in amplitude, with both a decrease in nocturnal activity and an increase in daytime activity. When maintained in constant dim red light, aged animals exhibited a shortening of the free-running period (22.8 +/- 0.1 h) compared to adult animals (23.5 +/- 0.1 h). A 3- to 5-year exposure to an accelerated seasonal photoperiodic rhythm ("annual" duration of 5 months) in accelerated mouse lemurs produced disturbances of the locomotor activity rhythm that resembled those of aged mouse lemurs, whether animals were studied in entrained or in free-running conditions. The present study demonstrated a weakened and fragmented locomotor activity rhythm during normal aging in this primate. Increasing the number of expressed seasonal cycles accelerated aging of parameters related to circadian rhythmicity in adult animals.     

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.     

Seasonality in Reproduction of <Emphasis Type="Italic">Lepilemur edwardsi</Emphasis>

Sportive lemurs are threatened species in the IUCN Red Data Book. However, quantitative information on their reproduction, urgently required for conservation, has been lacking. We collected first data on reproductive activity of Milne-Edwards’ sportive lemurs in a population inhabiting the dry deciduous forest of the Ankarafantsika National Park in northwestern Madagascar during 1998, 2001, and 2003. The species showed a seasonal reproduction. The main mating season extended from May to June, as indicated by the presence of males with high testes volumes and estrus females. In the mating and early postmating season and in the postparturition season, sexes did not differ in body mass. Females had a significantly higher body mass than males in August and November, indicating pregnancy, which together with the presence of small infants in October and November implies that gravidity in females lasted for about 4–5 mo. All litters consisted of singletons. Individuals with body mass at the lower limit of the population either did not develop measurable testes volumes (males) or were not in estrus (females). They were probably juveniles from the previous birth season that achieved sexual maturity not before their second year after birth. The first data on reproduction suggest a low reproduction rate for Lepilemur edwardsi and a request for a higher conservation status than previously attributed and the need for further management strategies.     

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.     

Female dominance in captive gray mouse lemurs (Microcebus murinus)

Female dominance or female feeding priority seem to be characteristic for many lemur species, but are rare traits in other primates and mammals in general. The nocturnal lemur species, however, are underrepresented in the quantitative studies on social dominance. The aim of this study is to investigate the pattern of intersexual dominance relationships in the gray mouse lemur (Microcebus murinus), a species that is generally thought to possess a number of ancestral lemur traits. The context, distribution, and outcome of intersexual conflicts are analyzed in four captive groups of gray mouse lemurs. Intersexual conflicts occurred in the study groups in different behavioral contexts and were mostly spatial interactions (chasing/fleeing, approach/avoidance). The majority of conflicts were decided, and were in all but one case won by females. This is the first evidence suggesting unconditional female dominance in a cheirogaleid primate. The existence of female dominance in most families of the Lemuriformes suggests it is an ancient trait that evolved in their common ancestor.     

Regulation by Photoperiod of Seasonal Changes in Body Mass and Reproductive Function in Gray Mouse Lemurs (Microcebus murinus): Differential Responses by Sex

Microcebus murinus exhibits highly seasonal biological rhythms to cope with extreme seasonality in availability of resources. To study the role of daylength on seasonal changes in body mass and reproductive function, we exposed male and female gray mouse lemurs to natural, constant, or alternating light cycles for 2 years under constant environmental conditions. When exposed to either constant short (SD: 10 h light/day), long (LD: 14 h light/day), or intermediate (ID: 12 h light/day) daylength, males and females maintained a constant body mass with no spontaneous cyclic variation. We only observed typical seasonal body mass changes in subjects exposed to alternating periods of SD and LD, the weight gain being triggered by SD, whereas weight loss occurred under LD. Reproductive activity in females proceeded from an endogenous rhythm that was expressed under constant daylengths. In contrast, changes in reproductive activity in males depended on daylength variation. In both sexes, SD and LD have direct inhibitory or stimulatory effects on reproductive activity. In females, daylength regulates breeding season by synchronizing an endogenous sexual rhythm with the season, whereas in males, the perception of a critical photoperiod is used to determine the subsequent onset or arrest of their breeding season. These sexual differences in the effect of daylength could be related to sex-specific differences in reproductive constraints.     

Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity

Qualitative observations in several European zoos revealed a high proportion of obese individuals in different species of lemurs. This phenomenon was examined in both subspecies of the ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Data on body weight were obtained from 43 animals in 13 European zoos and were compared with body weights of wild ruffed lemurs. The captive individuals’ mean weight was significantly higher than either of two different samples of wild V. variegata variegata. Using a weight‐based definition of obesity, 46.5% of the individuals in our sample were obese. Neither significant differences in body weight between the two subspecies nor between sexes could be found. Body weight did not correlate with age. The findings are discussed with reference to the feeding ecology of ruffed lemurs and their nutrition in captivity and to implications for captive breeding programs for this species. Zoo Biol 20:261–269, 2001. © 2001 Wiley‐Liss, Inc.     

The gray mouse lemur (Microcebus murinus) as a model for early primate brain evolution

The gray mouse lemur (Microcebus murinus), one of the world’s smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates. As a result, it has been considered a suitable model system for early primate physiology and behavior. Moreover, recent studies have demonstrated that mouse lemurs have comparable cognitive abilities and cortical functional organization as haplorhines. Finally, the small brain size of mouse lemurs provides us with actual lower limits for miniaturization of functional brain circuits within the primate clade. Considering its phylogenetic position and early primate-like traits, the mouse lemurs are a perfect model species to study the early evolution of primate brains.     

Sleeping and Ranging Behavior of the Sambirano Mouse Lemur, <Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>

Primates require secure sleeping sites for periods of rest, but despite their importance, the characteristics of desired sleeping sites are poorly known. Here we investigated the sleeping ecology of a radio-collared population of the Sambirano mouse lemur, Microcebus sambiranensis, during the nonreproductive season in the Anabohazo forest, northwestern Madagascar. We also investigated their ranging behavior and examined the spatial distribution of sleeping sites within the home ranges of the collared individuals. We took measurements of the sleeping tree’s physical characteristics and recorded the number of collared individuals using each sleeping site. We found that M. sambiranensis generally use foliage sleeping sites more frequently than tree holes and individuals slept more frequently in densely foliated trees than in sparsely foliated trees, often alone. We observed no significant differences in home range size or nightly travel distance between males and females; however, home ranges were smaller than those described for other mouse lemur species. Finally, we found that M. sambiranensis sleep peripherally and forage centrally within their home ranges, a behavior not previously described for mouse lemurs. Our results indicate profound differences in the social organization between M. sambiranensis and other mouse lemur species described in the literature, suggesting species-specificity in mouse lemur ecology. Understanding the sleeping ecology and ranging behavior of mouse lemurs is of great importance to their conservation, as these data facilitate the planning of long-term reforestation, habitat management, and population assessment.