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.     

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.     

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 )(T_i ) and the external temperature (T_e ) 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%.     

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.     

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.     

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.     

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.     

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.     

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     

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.     

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.     

The enigma of antipredator behavior in lemurs: Evidence of a large extinct eagle on Madagascar

Numerous zoologists who study diurnal lemurs on Madagascar have noted that they react strongly to the presence of birds of prey. For two of the most intensively studied lemurs, Propithecus verreauxiand Lemur catta,there are few documented cases of raptor predation. Thus, the maintenance of this stereotypic response is enigmatic. Bird bones recovered from cave surface deposits in southwestern Madagascar include the remains of an eagle (Aquila),a genus that has disappeared from Madagascar and that would have been capable of hunting animals the size of adult P. verreauxi and L. catta.The stereotypic response of these two lemurs toward raptors may have been retained from the period when this extinct eagle inhabited the island and is reinforced by rare acts of predation by extant birds of prey.     

Traditional knowledge ofDypsis Fibrosa (Arecaceae) in Eastern Madagascar

Dypsis fibrosa is widespread in eastern Madagascar and local people regard it as one of the most important palms due to its use as thatch. In an interview survey 12 different uses of this palm were reported. Most informants knew only one or two uses, but variance was large. How many uses people know and what they use different palm parts for is correlated to socioeconomic factors such as personal wealth and home village. Comparison of data obtained from interviews and observations showed that there is not always a strict correlation between ethnobotanical data elicited in surveys, actual extent of use, and importance accorded to different plant resources. Informants were generally aware of an human-caused decline inD. fibrosa abundance, but viewed it as inevitable and suggested to replaceD. fibrosa products by other materials. Although local people viewD. fibrosa as very important, motivation for its conservation and sustainable use seems to be low.     

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.     

Ranging Behavior and Possible Correlates of Pair-Living in Southeastern Avahis (Madagascar)

Researchers have proposed several hypotheses to explain pair-living in primates. In particular, when males are not involved in direct parental care, pair-living may be related to female dispersal, infanticide prevention, or male mate/resource defense. We aimed to evaluate, through a better understanding of the ranging patterns of avahis, which hypotheses may best account for pair-living in these nocturnal lemurs. We collected focal observations over 26 nights, June–September 2004, in a littoral forest (Sainte Luce, southeastern Madagascar) on 4 adult radiocollared avahis [Avahi laniger (Tattersall, I. (1982). The Primates of Madagascar. Columbia University Press, New York.) or Avahi meridionalis (Zaramody in Primate Reports 74:9–22, 2006)]. We followed 2 males and 2 females from 2 groups: B, a male-female couple, and A, comprising the parental pair and 1-yr-old female offspring. The adult females birthed in August. We recorded resting and feeding tree points (via global positioning system) for home range calculation through minimum convex polygon and kernel methods. We provide the first quantitative information on the ranging behavior of 2 male and 2 female avahis. Home range/daily path length values (means) are higher than the ones previously reported for the same and other folivorous pair-living lemur species. On average, the 2 females spent more time feeding and traveled shorter distances than the 2 males did. Male–female cohesion (mean values), possibly enhanced by offspring presence, was higher in A and after births than in B and before births, respectively. Although male avahis may be forced into pair-living owing to energy constraints related to size, locomotion, and diet, females might accept pair-living in exchange for indirect territory defense and mate guarding.