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Long‐term genetic monitoring of populations is essential for efforts aimed at preserving genetic diversity of endangered species. Here, we employ a framework of long‐term genetic monitoring to evaluate the effects of fragmentation and the effectiveness of the establishment of corridors in restoring population connectivity and genetic diversity of mouse lemurs Microcebus ganzhorni. To this end, we supplement estimates of neutral genetic diversity with the assessment of adaptive genetic variability of the major histocompatibility complex (MHC). In addition, we address the challenges of long‐term genetic monitoring of functional diversity by comparing the genotyping performance and estimates of MHC variability generated by single‐stranded conformation polymorphism (SSCP)/Sanger sequencing with those obtained by high‐throughput sequencing (next‐generation sequencing [NGS], Illumina), an issue that is particularly relevant when previous work serves as a baseline for planning management strategies that aim to ensure the viability of a population. We report that SSCP greatly underestimates individual diversity and that discrepancies in estimates of MHC diversity attributable to the comparisons of traditional and NGS genotyping techniques can influence the conclusions drawn from conservation management scenarios. Evidence of migration among fragments in Mandena suggests that mouse lemurs are robust to the process of fragmentation and that the effect of corridors is masked by ongoing gene flow. Nonetheless, results based on a larger number of shared private alleles at neutral loci between fragment pairs found after the establishment of corridors in Mandena suggest that gene flow is augmented as a result of enhanced connectivity. Our data point out that despite low effective population size, M. ganzhorni maintains high individual heterozygosity at neutral loci and at MHC II DRB gene and that selection plays a predominant role in maintaining MHC diversity. These findings highlight the importance of long‐term genetic monitoring in order to disentangle between the processes of drift and selection maintaining adaptive genetic diversity in small populations.

The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations.

Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce. Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees. Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.

Lemurs, lorises, and tarsiers are socially and ecologically diverse primates that include some of the most endangered mammals. We review results of long-term studies of 15 lemur species from 7 sites in Madagascar and 1 species each of loris and tarsier in Indonesia. We emphasize that the existence of long-term study populations is a crucial prerequisite for planning and conducting shorter studies on specific topics, as exemplified by various ecophysiological studies of lemurs. Extended studies of known individuals have revealed variation in social organization within and between ecologically similar species. Even for these primates with relatively fast life histories, it required more than a decade of paternity data to characterize male reproductive skew. The long-term consequences of female rank on reproductive success remain poorly known, however. Long-term monitoring of known individuals is the only method to obtain data on life-history adaptations, which appear to be shaped by predation in the species covered here; long-term studies are also needed for addressing particular questions in community ecology. The mere presence of long-term projects has a positive effect on the protection of study sites, and they generate unique data that are fundamental to conservation measures, such as close monitoring of populations.

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.[PUBLICATION ABSTRACT]

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal southeastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioral observations between 2011 and 2013 on frugivorous collared brown lemurs ( Eulemur collaris ) and folivorous southern bamboo lemurs ( Hapalemur meridionalis ). To estimate the ability of lemurs to use pioneer species, we categorized all plants used for feeding and resting as fast growing, mid-growing, or slow growing. We fitted general linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species ( E. collaris and H. meridionalis ), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to use secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with that for other primate folivores.

The concept of “facilitated restoration” aims at native biodiversity reinstatement with the help of animal seed dispersers attracted by fruiting trees. Yet, large-crowned trees will have to develop in the early stages of restoration; therefore, seed dispersal provided by small generalist mammals and birds that use rapidly growing herbs, shrubs, and small trees at early stages of forest succession would accelerate biodiversity restoration. Due to the elusive lifestyle of these small animals, it is unclear what species can contribute to the early stages of this process. Using the primate genus Microcebus (adult body mass about 60 g) as an example, we illustrate that these small generalists are possible seed dispersers in the early stages of forest restoration, not yet used by larger frugivores. We show that Microcebus spp. dispersed more seeds from herbs, shrubs, and small trees than large frugivorous primate species. These plants tend to have smaller seeds than large tree species and are often pioneer species not considered in forest restoration projects. Facilitating the colonization of restoration plots by generalist small seed dispersers that use shrubby habitats may improve plant diversity by adding a more natural sequence of successional stages towards mature forests in Madagascar and elsewhere in the tropics.

Edge effects are thought to play a key role in fragmented habitats. It is often assumed that edge-avoiding species are more prone to local extinction than non-edge-avoiding species, but there are few data to support this assumption. Also, few data are available on the effects of edges on some groups, and there is little understanding of seasonal changes in edge effect intensity. To better understand the role that edge effects play in fragmented tropical forests, we assessed the distribution of reptiles and amphibians in six littoral rainforest fragments in southeastern Madagascar in 1999 (dry season) and 2000 (wet season). Using randomization tests, we found all three types of edge responses: edge-avoiders, interior-avoiders, and omnipresent species. However, edge responses varied considerably among seasons. For example, some species (e.g., Mantidactylus bicalcaratus, Phelsuma quadriocellata) were strong edge-avoiders in the dry season, but showed no preference for edge or interior habitats during the wet season. Also, edge-avoiding species tended to be more extinction-prone than non-edge-avoiding species. Abiotic data documented significantly higher temperatures and dew point temperatures near edges. Wind speed also tended to be higher and relative humidity tended to be lower near edges. Our results indicate that many amphibians and reptiles respond to altered microclimates near edges and these responses have a strong seasonal component. For many species, edge sensitivity does seem to be correlated with extinction vulnerability and therefore should be of primary consideration in plans to conserve biodiversity in fragmented tropical forests.[PUBLICATION ABSTRACT]