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.     

Seasonal Changes in Feeding Ecology and Activity Patterns of Two Sympatric Mouse Lemur Species,the Gray Mouse Lemur (<Emphasis Type="Italic">Microcebus murinus</Emphasis>) and the Golden-brown Mouse Lemur (<Emphasis Type="Italic">M. ravelobensis</Emphasis>), in Northwestern Madagascar

Because closely related species are likely to be ecologically similar owing to common ancestry, they should show some degree of differentiation in order to coexist. We studied 2 morphologically similar congeneric species, the golden-brown mouse lemur (Microcebus ravelobensis) and the gray mouse lemur (M. murinus). These species are found in partial sympatry in the dry deciduous forest in northwestern Madagascar. We investigated whether 1) feeding niche differentiation and/or 2) a reduction in locomotor activity during periods of food shortage, which might reflect an energy saving strategy, can explain the coexistence of these 2 lemur species. To obtain feeding and behavioral data, we conducted focal observations of 11 female Microcebus murinus and 9 female M. ravelobensis during 11 months from 2007 to 2008 and collected fecal samples for 6 mo. We monitored the phenology of 272 plant specimens and trapped arthropods to determine food availability. Results revealed interspecific differences in 1) relative proportion of consumed food resources, resulting in a merely partial dietary overlap, and in 2) relative importance of seasonally varying food resources throughout the year. In addition, females of Microcebus murinus showed a reduction in locomotor activity during the early dry season, which might reflect an energy-saving strategy and might further reduce potential competition with M. ravelobensis over limited food resources. To conclude, a combination of interspecific feeding niche differentiation and differences in locomotor activity appears to facilitate the coexistence of Microcebus murinus and M. ravelobensis.     

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.     

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,Population Structure and Habitat Use of Microcebus berthae Compared to Those of Other Sympatric Cheirogalids

We aimed to identify the geographical and biotic limitations of Microcebus berthae, the smallest extant primate. Furthermore we analyzed the mating system of two local populations and their habitat use in relation to microhabitat structures and to those of Microcebus murinus and Cheirogaleus medius, two potentially competing lemur species. The range of Microcebus berthae is restricted to 220 km² in the dry deciduous forest of western Madagascar. A very optimistic estimate of the total population size is ca. 7900 individuals. During a 13-mo mark-recapture study individuals were trapped from May 1995 to May 1996 at permanent trap locations 50 m apart over 2 study areas of ca. 25 ha each. The spacing of trap locations where individuals have been retrapped indicate that males have larger home ranges than those of females, which in concert with multiple intra- and intersexual range overlap indicates a promiscuous mating system. In contrast to the other 2 species, Microcebus berthae maintained specific habitat utilization patterns at 2 sites with different vegetation structures. Their habitat use in relation to vegetation characteristics differed from that of Cheirogaleus medius but not from that of Microcebus murinus. Co-occurrence patterns of Microcebus berthae and M. murinus deviated significantly from random and resembled a checkerboard distribution possibly generated by competitive exclusion. Thus, according to the niche concept, Microcebus berthae seem to be separated from Cheirogaleus medius by differences in food composition and habitat requirements, while they avoid direct competition with M. murinus by spatial separation.     

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.     

Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations

Background

A central question in evolutionary biology is how cryptic species maintain species cohesiveness in an area of sympatry. The coexistence of sympatrically living cryptic species requires the evolution of species-specific signalling and recognition systems. In nocturnal, dispersed living species, specific vocalisations have been suggested to act as an ideal premating isolation mechanism. We studied the structure and perception of male advertisement calls of three nocturnal, dispersed living mouse lemur species, the grey mouse lemur (Microcebus murinus), the golden brown mouse lemur (M. ravelobensis) and the Goodman's mouse lemur (M. lehilahytsara). The first two species occur sympatrically, the latter lives allopatrically to them.

Results

A multi-parameter sound analysis revealed prominent differences in the frequency contour and in the duration of advertisement calls. To test whether mouse lemurs respond specifically to calls of the different species, we conducted a playback experiment with M. murinus from the field using advertisement calls and alarm whistle calls of all three species. Individuals responded significantly stronger to conspecific than to heterospecific advertisement calls but there were no differences in response behaviour towards statistically similar whistle calls of the three species. Furthermore, sympatric calls evoked weaker interest than allopatric advertisement calls.

Conclusion

Our results provide the first evidence for a specific relevance of social calls for speciation in cryptic primates. They furthermore support that specific differences in signalling and recognition systems represent an efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species.     

The lack of female dominance in golden‐brown mouse lemurs suggests alternative routes in lemur social evolution

Female dominance is a well‐known trait of lemurs, although it has not been reported from all species and is still often unexplored, especially in the nocturnal species. We examined the intersexual dominance relationships in Microcebus ravelobensis, a congener of M. murinus who is well known for its female dominance. Given the many similarities in biology, it was predicted that M. ravelobensis should also possess female dominance. Seventeen unfamiliar male–female pairs were formed with animals captured in northwestern Madagascar and kept in a two‐cage setting (one cage for each animal) for up to 1 week. Four encounter experiments were conducted with each pair. In contrast to the expectations, females were not consistently dominant over their male partners. Only 3 of 17 dyads developed a clear agonistic asymmetry, among which were two cases of male dominance and only one case of female dominance. Because body mass differences did not explain the findings, various other possible explanations are discussed. It is suggested that food may not be the driving factor of female dominance in mouse lemurs. Instead, it is hypothesized that species‐specific differences in the quality of sleeping sites (i.e., tree holes) and in social grouping patterns may better explain why some mouse lemur species have female dominance, whereas others like the golden‐brown mouse lemur do not. It is concluded thatthese arguments and hypotheses may even hold true for other solitary foragers and may thereby lead to a better understanding of the variable social evolution in lemurs and primates in general. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

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.     

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.     

Ecological fragmentation effects in mouse lemurs and small mammals in northwestern Madagascar

Habitat loss and fragmentation are major ecological forces threatening animal communities across the globe. These issues are especially true in Madagascar, where forest loss is ongoing. We examined the effects of forest fragmentation on the distribution and abundance of sympatric, endemic gray, and golden-brown mouse lemurs (Microcebus murinus and Microcebus ravelobensis), the endemic western tuft-tailed rat (Eliurus myoxinus), and the invasive black rat (Rattus rattus) in two regions in northwestern Madagascar. We used systematic capture procedures in 40 forest fragments and four continuous forest sites which differed in size, shape, and degree of isolation. With a trapping effort of 11,567 trap nights during two dry seasons (2017–2018), we captured 929 individuals (432 M. ravelobensis, 196 M. murinus, 116 E. myoxinus, and 185 R. rattus). We examined the influence of study region, forest type (fragment vs. continuous), forest size, forest shape, the proportion of 50-m forest edge and distance to continuous forest on the abundance and interaction of the four species. Responses to fragmentation differed strongly between species, but no interaction could be detected between the abundance of the different species. Thus competition within and between native and invasive species may not be regulating abundances in these regions. On the contrary, the abundance of M. ravelobensis and E. myoxinus differed significantly between study regions and was negatively affected by fragmentation. In contrast, there was no evidence of an impact of fragmentation on the abundance of M. murinus. Finally, the invasive R. rattus responded positively to the increasing distance to the continuous forest. In conclusion, the response of small Malagasy mammals to forest fragmentation varies largely between species, and fragmentation effects need to be examined at a species-specific level to fully understand their ecological dynamics and complexity.     

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.     

Effects of landscape and patch-level attributes on regional population persistence

Species responses are influenced by processes operating at multiple scales, yet many conservation studies and management actions are focused on a single scale. Although landscape-level habitat conditions (i.e., habitat amount, fragmentation and landscape quality) are likely to drive the regional persistence of spatially structured populations, patch-level factors (i.e., patch size, isolation, and quality) may also be important. To determine the spatial scales at which habitat factors influence the regional persistence of endangered Ord's kangaroo rats (Dipodomys ordii) in Alberta, Canada, we simulated population dynamics under a range of habitat conditions. Using a spatially-explicit population model, we removed groups of habitat patches based on their characteristics and measured the resulting time to extinction. We used proportional hazards models to rank the influence of landscape and interacting patch-level variables. Landscape quality was the most influential variable followed by patch quality, with both outweighing landscape- and patch-level measures of habitat quantity and fragmentation/proximity. Although habitat conservation and restoration priorities for this population should be in maximizing the overall quality of the landscape, population persistence depends on how this goal is achieved. Patch quality exerted a significant influence on regional persistence, with the removal of low quality road margin patches (sinks) reducing the risk of regional extinction. Strategies for maximizing overall landscape quality that omit patch-level considerations may produce suboptimal or detrimental results for regional population persistence, particularly where complex local population dynamics (e.g., source-sink dynamics) exist. This study contributes to a growing body literature that suggests that the prediction of species responses and future conservation actions may best be assessed with a multi-scale approach that considers habitat quality and that the success of conservation actions may depend on assessing the influences of habitat factors at multiple scales.     

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.     

Bird Community Composition in a Shaded Coffee Agro-ecological Matrix in Puebla,Mexico: The Effects of Landscape Heterogeneity at Multiple Spatial Scales

This study examined the importance of habitat heterogeneity on the avian community composition, and investigated the scale at which species abundances respond to habitat variables. The study was conducted within a diverse landscape matrix of a shaded coffee region in Mexico. To detect at which characteristic spatial scale different species and foraging guilds respond most strongly we analyzed the effect of plot-, patch- and landscape-level variables at different spatial extent (i.e., different kilometer radii) on species composition and foraging guilds. We used redundancy analysis to identify species–environment correlations, and to identify predictor variables that best explained the bird community structure, quantified the influence of plot-, patch- and landscape-level variables on the bird community composition. In addition, we used the 4th-corner method to detect significant relationships between the dietary guilds and plot-, patch- and landscape-level variables. We recorded 12,335 individuals of 181 bird species; 105 bird species were recorded foraging within the shaded coffee plantations. We found that plot- and landscape-level variables significantly explained the bird community composition best across all scales, and were significantly correlated with the abundance of the dietary guilds. In contrast, patch-level variables were less important. Habitat composition variables (i.e., coffee, forest and agricultural area) were among the most important predictors. Canopy structure was more important than other vegetation structure variables in explaining dietary guild structure. Hence, the maintenance of a heterogeneous landscape with a high-quality matrix within an agro-ecological region enhances bird conservation.     

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.     

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.     

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.     

Population, Diet and Conservation of Malayan Flying Lemurs in Altered and Fragmented Habitats in Singapore

The Malayan flying lemur (Cynocephalus variegatus) is a nocturnal mammalian arboreal folivore that inhabits the forests of Southeast Asia. Surveys were conducted from August to November 2003 to estimate the population density of Malayan flying lemurs for the first time in the Singapore Zoological Gardens. The study area consisting of Singapore Zoo and Night Safari was located in the Central Catchment Nature Reserve, where most of Singapore’s remaining natural forest is found. The Zoo consisted of 28 ha of landscaped habitat and the adjacent Night Safari consisted of 40 ha of secondary rainforest. The density estimates of flying lemurs in the Zoo and Night Safari were 15 and 24 individuals respectively. Seven plant species that were the preferred food items and an additional 10 plants that were common in the sites but not eaten by the flying lemurs were analysed to compare the mineral and phytochemical contents. Flying lemurs consumed leaves containing significantly less potassium and nitrogen but higher tannin (p < 0.05). The study shows that flying lemurs are able to survive in altered and fragmented landscapes. Conservation and management strategies are essential to protect the shrinking habitats in Singapore.