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.     

Microsatellite markers for paternity testing in fork‐marked lemurs (Phaner furcifer)

We report the development of three new microsatellites and four transferred across‐species for fork‐marked lemurs (Phaner furcifer). Two markers were isolated from Cheirogaleus medius and one from Microcebus murinus. The transferred markers also originate from Cheirogaleus medius and Microcebus murinus. The seven markers were tested on 30 individuals of Phaner furcifer and have proven to be useful for inclusion and exclusion of potential parents. The markers presented here are the first published for application on Phaner furcifer.     

Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.)

We report the development of 13 new microsatellite markers for mouse lemurs (Microcebus sp.). Two markers were isolated from the fat tailed dwarf lemur (Cheirogaleus medius) and 11 from the grey mouse lemur (Microcebus murinus). A total of 561 individuals from four different species of mouse lemurs was genotyped with the newly developed markers. All markers showed Mendelian inheritance in 21 families of mouse lemurs. All markers show polymorphism in several species of mouse lemurs and seven amplified in C. medius. Among these new markers are the first 10 published for M. berthae and the first 11 for M. griseorufus.     

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.     

Comparative Feeding Ecology of Sympatric <Emphasis Type="Italic">Microcebus berthae and M. murinus</Emphasis>

Most Malagasy primate communities harbor a diverse assemblage of omnivorous species. The mechanisms allowing the coexistence of closely related species are poorly understood, partly because only preliminary data on the feeding ecology of most species are available. We provide an exemplary feeding ecology data set to illuminate coexistence mechanisms between sympatric gray and Madame Berthe’s mouse lemurs (Microcebus murinus, M. berthae). We studied their feeding ecology in Kirindy Forest/CFPF, a highly seasonal dry deciduous forest in western Madagascar. Between August 2002 and December 2007, we regularly (re-)captured, marked, and radiotracked females of both species. A combination of direct behavioral observations and fecal analyses revealed that both Microcebus species used fruit, arthropods, gum, insect secretions, and small vertebrates as food sources. However, Microcebus berthae and M. murinus differed in both composition and seasonal variation of their diets. Whereas the diet of Microcebus murinus varied seasonally and was generally more diverse, M. berthae relied mainly on insect secretions supplemented by animal matter. The differences were also reflected in a very narrow feeding niche of Microcebus berthae and a comparatively broad feeding niche of M. murinus. Resource use patterns of Madame Berthe’s and more so of opportunistic gray mouse lemurs broadly followed resource availability within the strongly seasonal dry forest. Feeding niche overlap between the 2 sympatric species was high, indicating that food resource usage patterns did not reflect niche partitioning, but can instead be explained by constraints due to food availability.     

Occurrence of lemurs in landscapes and their species-specific scale responses to habitat loss

Studies on the impact of habitat loss on species occurrence consistently find that the amount of habitat (measured as patch area) is a major determinant of species occurrence at a patch-level. However, patch-level research may fail to detect important patterns and processes only observable at a landscape-level. A landscape-level approach that incorporates species-specific scale responses is needed to better understand what drives species occurrence. Our aim was to determine the landscape-level scale of effect of habitat amount on the occurrence of three species of nocturnal lemurs (Cheirogaleus medius, Microcebus murinus, and M. ravelobensis). We surveyed line transects to determine the occurrence of three lemur species within a fragmented landscape of deciduous dry forest and anthropogenic grassland in northwestern Madagascar. To determine the scale of effect of habitat loss on lemur occurrence, we compared logistic regression models of occurrence against habitat amount among eight different landscape scales using Akaike's Information Criterion values. We found differing scale responses among the lemurs in our study. Occurrence of C. medius responded to habitat amount at scales between 0.5–4 ha, M. murinus at scales between 1 and 4 ha and M. ravelobensis at scales between 0.125 and 4 ha. We suggest that the scale of effect for C. medius is mediated by their ability to hibernate. A relatively lower scale-response for Microcebus spp. likely reflect their omnivorous diet, small habitat requirements, and limited dispersal ability. Differences in scale responses between M. murinus and M. ravelobensis are likely a result of differing dispersal ability and responses to edge effects between these species. Our study is among the first on lemurs to show the value of a landscape-level approach when assessing the effects of habitat loss on species occurrence.     

Reproduction in Coquerel's dwarf lemur (Mirza coquereli)

Most nocturnal Malagasy primates, as well as many diurnal species, are highly endangered in their natural habitat. Captive breeding programs have been established for many species, but detailed information on reproduction is only available for three nocturnal taxa: the mouse lemur (Microcebus murinus), the dwarf lemur (Cheirogaleus medius), and the greater dwarf lemur (Cheirogaleus major). In this study, we present data for another nocturnal Malagasy primate, Coquerel's dwarf lemur (Mirza coquereli), which has been propagated since 1982 at the Duke University Primate Center. Unlike all other Malagasy primates bred in captivity, M. coquereli cycles throughout the year, and is clearly less seasonal in its birth distribution than is C. medius or M. murinus. Estrous intervals ranged between 19 and 30.5 days. Estrus lasted no longer than 1 day. After an average gestation length of 89.2 days, litters of one or two were born. Females cycled for the first time between 8 and 15 months of age, and gave birth for the first time between 12.8 and 33.5 months of age. The earliest mating of a male leading to conception was observed at the age of 17 months. For males and females, an increase in daylength appears to trigger pubertal development. Males had seasonal changes in testicular volume which were not explained by covariation with body weight. Maximum testis size occurred in spring, when breeding activity was highest. The occurrence of year-round reproduction in M. coquereli, and the absence of seasonal fattening and/or hibernation, along with their specialized winter diet, may be correlated. © 1995 Wiley-Liss, Inc.     

A comparative approach to the organization of vocal signals in noctural prosimians

Vocalizations and corresponding behavior patterns were recorded inGalago demidovii (Lorisidae), Microcebus murinus, andCheirogaleus medius (Cheirogaleidae). Physical characteristics of the calls were analyzed and calls correlated with their behavioral context. Based on these correlations an «advertisement» call can be identified in all three species. Interspecific comparison suggest that within the Prosimian suborder there are at least two different evolutionary pathways in the organization of this call and of the vocal repertoires in general. The Lorisid speciesG. demidovii conveys acoustic information mainly in pulsed calls, leading to an extreme amplitude-modulation. Individual characteristics are in temporal patterns of calls.C. medius andM. murinus, the Cheirogaleid species, use tonal calls and encode individual characteristics in frequency patterns. Despite the fundamental similarity in the call-structure of the two Cheirogaleid species different adaptations can be found to meet different ecological needs.     

Biogeography of Dwarf Lemurs: Genetic Evidence for Unexpected Patterns in Southeastern Madagascar

Seven species of dwarf lemurs (Cheirogaleus spp.) are currently recognized after a recent revision of the genus. During a field study in southeastern Madagascar, we observed 3 distinct morphotypes of Cheirogaleus resembling Cheirogaleus medius, C. major and C. crossleyi. In particular, for Cheirogaleus crossleyi southeastern Madagascar was far away from the known distribution range of the species when referring to the recent revision of the genus. In order to clarify the taxonomic status of the 3 morphotypes, we compared field samples from southeastern Madagascar to museum specimens from several locations in Madagascar and to field samples from Kirindy/CFPF, western Madagascar by genetic analyses using the mitochondrial cytochrome b gene. Genetic data yield strong support for 2 of the 3 morphotypes to represent Cheirogaleus medius and C. major. The third morphotype is genetically closely related to Cheirogaleus crossleyi, albeit more distantly than the other 2 morphotypes to the respective reference samples. The genetic distance is related to a considerable geographic distance between the location of our field study and the origin of the respective reference specimen, because Cheirogaleus crossleyi had been reported only from northern Madagascar. Our field observations indicate an isolated population in southeastern Madagascar. We propose to identify them as Cheirogaleus crossleyi and discuss the population genetic and biogeographic considerations supporting this conclusion.     

Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): New insights from stable isotopes

The relationships between resource distribution, type of competition, and consequences for social organization have been formalized in the socioecological model (SEM) which predicts that ecological factors are the main determinants of female distribution. We tested this basic prediction in two solitary primates (Microcebus berthae and M. murinus) which differ in female association patterns. Using stable nitrogen and carbon isotope data of hair samples and food sources we quantified inter‐specific differences in diet. δ¹³C in M. berthae reflected a diet composed mainly of insect secretions. Higher within‐species as well as seasonal variation in δ¹³C of M. murinus indicated a wider trophic niche including plant and animal source food. Constantly elevated δ¹⁵N in M. murinus most likely reflected extended torpor during the lean season. This energy‐saving strategy together with a wider, more opportunistic feeding niche might reduce female competition in this species, facilitating smaller female ranges, and a higher association potential. In contrast, δ¹⁵N fluctuated seasonally in M. berthae, most likely indicating varying amounts of arthropod food in the diet. Intense scramble competition over small and seasonally limited resources might lead to female spatial avoidance and a reduced association potential in M. berthae. Thus, differences in female association patterns between these two solitary foragers are due to different types of competition and overall intensities of intra‐specific competition. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Distribution and Abundance of the World's Smallest Primate,Microcebus berthae,in Central Western Madagascar

The distribution of most recently discovered or described lemur species remains poorly known, but many appear to have small geographical ranges, making them vulnerable to extinction. Research can contribute to future conservation actions on behalf of these species by providing accurate information on local distribution and abundance. The distribution of the world’s smallest primate, the endangered Madame Berthe’s mouse lemur (Microcebus berthae), is limited to the Menabe Central region of western Madagascar. This species was discovered in the 1990s, but many fundamental aspects of its ecology remain unknown. The aims of our study were therefore to determine the actual distribution of Microcebus berthae across the forests of this region, to estimate population density, and to examine the species’ response to anthropogenic activities. We established 35 1-km line transects across Menabe Central, on which we surveyed mouse lemurs by distance sampling and live trapping. Microcebus berthae does not occur in all remaining forests of this small region and its population density is highly heterogeneous, both across its geographic range and locally. Within its area of occupancy, the population of Microcebus berthae not only was distributed according to spatial heterogeneities of the habitat, but also responded to anthropogenic disturbances and varied seasonally. Our results indicate that Microcebus berthae is susceptible to habitat degradation and avoids human environments spatially. As none of the forest remnants in which the species still occurs were officially protected until recently, immediate conservation actions should focus on effectively protecting Kirindy and Ambadira forests.     

Vegetation Thresholds for the Occurrence and Dispersal of <Emphasis Type="Italic">Microcebus griseorufus</Emphasis> in Southwestern Madagascar

Primate populations are declining the world over due to anthropogenic threats, including habitat loss and degradation. This raises the important question of how much habitat degradation a species can cope with. Habitat degradation is pronounced in Madagascar, where most of the human population depends on the direct exploitation of natural resources. We aimed to identify the response of Microcebus griseorufus (the gray-brown mouse lemur) to forest degradation and to define the structural traits of the vegetation that might be crucial for the species’ occurrence in anthropogenic landscapes. We documented the occurrence of Microcebus griseorufus in relation to vegetation structures along a gradient of forest degradation, at the edge of and west of Tsimanampetsotsa National Park in April and May 2007 and from October to December 2015. We confirmed the occurrence of Microcebus griseorufus using trapping and visual surveys, and measured vegetation structure. Logistic regression models showed that Microcebus griseorufus has a threshold response to tree density and the diameter of thick trees. The thresholds of occurrence were at 10–15% of the tree density recorded in intact forest and a mean diameter of trees with a diameter at breast height of >10 cm of 14.3 cm. The definition of such thresholds might help to maintain suitable habitat for this species and other primates living in anthropogenic landscapes, providing connectivity between isolated protected areas and allowing dispersal between populations.     

Morphometrics confirm taxonomic deflation in dwarf lemurs (Primates: Cheirogaleidae), as suggested by genetics

Detailed knowledge of the identity and distributions of extant species is essential for unravelling patterns and mechanisms of biodiversity, and it provides indispensable baseline data for conservation efforts. The taxonomy of the primates of Madagascar (Lemuriformes) has experienced drastic revisions in the last decades, with species numbers skyrocketing, especially in the genera Microcebus, Avahi, and Lepilemur. The dwarf lemurs (genus Cheirogaleus) have received less attention in terms of their taxonomy, even though they are closely related and syntopic with these diverse genera. The last revision of the genus was based on morphological data from museum specimens, and accepted seven species: Cheirogaleus medius, Cheirogaleus major, Cheirogaleus crossleyi, Cheirogaleus adipicaudatus, Cheirogaleus sibreei, Cheirogaleus ravus, and Cheirogaleus minusculus, whereas a more recent multilocus molecular study only detected three lineages: C. medius, C. major, and C. crossleyi. The goal of this study was to reassess the currently accepted taxonomy of the genus by examining six external and 32 craniodental characters of 120 museum specimens and 36 new specimens from the field. This study, in conjunction with a complementary molecular study, revealed lower diversity and a lower number of distinct morphs of dwarf lemurs than previously postulated. We conclude that in our sample there are three distinct morphs in the genus Cheirogaleus that correspond to C. medius, C. major, and C. crossleyi. We formally recognize C. adipicaudatus and C. ravus as synonyms of C. medius and C. major, respectively, and consider C. minusculus and C. sibreei to be potential synonyms of C. medius. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010.     

Evidence on primate phylogeny from ε-globin gene sequences and flanking regions

Phylogenetic relationships among various primate groups were examined based on sequences of -globin genes. -globin genes were sequenced from five species of strepsirhine primates. These sequences were aligned and compared with other known primate -globin sequences, including data from two additional strepsirhine species, one species of tarsier, 19 species of New World monkeys (representing all extant genera), and five species of catarrhines. In addition, a 2-kb segment upstream of the -globin gene was sequenced in two of the five strepsirhines examined. This upstream sequence was aligned with five other species of primates for which data are available in this segment. Domestic rabbit and goat were used as outgroups. This analysis supports the monophyly of order Primates but does not support the traditional prosimian grouping of tarsiers, lorisoids, and lemuroids; rather it supports the sister grouping of tarsiers and anthropoids into Haplorhini and the sister grouping of lorisoids and lemuroids into Strepsirhini. The mouse lemur (Microcebus murinus) and dwarf lemur (Cheirogaleus medius) appear to be most closely related to each other, forming a clade with the lemuroids, and are probably not closely related to the lorisoids, as suggested by some morphological studies. Analysis of the -globin data supports the hypothesis that the aye-aye (Daubentonia madagascariensis) shares a sister-group relationship with other Malagasy strepsirhines (all being classified as lemuroids). Relationships among ceboids agree with findings from a previous -globin study in which fewer outgroup taxa were employed. Rates of molecular evolution were higher in lorisoids than in lemuroids.Correspondence to: M. Goodman     

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.     

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.     

Distribution and Morphological Variation of Microcebus spp. Along an Environmental Gradient in Southeastern Madagascar

The lemurs of Madagascar are known for their extraordinary levels of speciation. However, the mechanisms and environmental conditions that led to this diversity remain obscure. We used 3 species of Microcebus (M. griseorufus, M. murinus, M. rufus) occurring along an environmental gradient as a model to investigate 1) how the different species are distributed in relation to variation in environmental conditions and ecotones; 2) whether or not the morphology of a given species varies in relation to environmental conditions; and 3) whether or not there is evidence for morphological character displacement to reduce congeneric competition in sympatry vs. allopatry. The 3 species of Microcebus show clear associations with specific habitat types. Distributions overlap at ecotones. Nevertheless, the ecotone between dry spiny and gallery forest represents a species boundary between Microcebus griseorufus and M. murinus while the ecotone between dry spiny forest and evergreen humid forest represents the species boundary between M. murinus and M. rufus. Different ambient conditions are not reflected in changes in body measurements of Microcebus murinus living in different vegetation formations. There is no indication for character displacement in sympatry vs. allopatry. Thus, differences in body mass or other morphological characteristics do not contribute to species separation between Microcebus griseorufus and M. murinus. The results confirm the importance of ecotones as species boundaries as a condition postulated for the radiation of lemur and other species on Madagascar. They also demonstrate different habitat affinities of seemingly very similar lemur species and thus illustrate our very limited understanding of the actual selection pressures, adaptations of lemurs to their environments, and their possible response to interspecific competition.     

Effects of Transect Selection and Seasonality on Lemur Density Estimates in Southeastern Madagascar

I investigated how transect type (trails vs. cut transects) and seasonality influenced density estimates for 5 lemur taxa (Avahi laniger, Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus) in the Vohibola III Classified Forest in SE Madagascar. I surveyed tree height and diameter and lemur populations from June 1 to December 28, 2004 along 2 1250-m trails local people used and 2 1250-m transects cut parallel to the trails in primary rain forest. Despite dendrometric variations within and between trails and transects, only density estimates of Hapalemur griseus griseus differed significantly by transect type. The spatial variation may be a result of removal by local people of giant bamboo, which is the main food for Hapalemur griseus griseus, along trails. Conversely, seasonality influenced density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus. The temporal variations may be related to seasonal torpor for Cheirogaleus major and increased detection probabilities during periods of fruit exploitation for Eulemur rubriventer, Microcebus rufus, and Hapalemur griseus griseus. Transect type and seasonality did not affect density estimates for Avahi laniger, which may be related to the highly folivorous and low-energy diet of the nocturnal lemur. Researchers surveying lemurs along line transects should be aware that transect selection may influence density estimates for Hapalemur griseus griseus and that seasonality may influence density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus.