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Investigating factors influencing infant physical and social development is important to elucidate primate adaptations and life history evolution. Infant sifakas exhibit a puzzling mismatch between dental precocity and relatively slow postnatal growth, but only anecdotal reports of infant development are available for a comparative appraisal of their early life history and maturation. We therefore collected behavioral data on mother–infant dyads of 16 infant Verreaux’s sifakas (Propithecus verreauxi) from 3 birth cohorts in Kirindy Forest to assess how the infant’s age, sex, mother’s age, and environmental variation influence the infant’s development until weaning. We found that somatic growth rates differed between the sexes, with females growing faster than males. Infants began ingesting solid food as early as 3 weeks of age, which is extremely early for a primate of this size and much earlier than in Lemuridae. Social behavior emerged at a later age than motor skills. Despite pronounced variation in the timing and occurrence of various infant activities, none of them differed between the sexes, except that male infants were more engaged in grooming others than females. Infant sifakas did not develop faster than other lemurs despite the extra available energy gained from ingesting solid food at an early age, but their mothers carry them for a relatively long period, perhaps because vertical clinging and leaping is a locomotor style that requires prolonged physical maturation. The adaptive significance of their dental precocity remains elusive, however. Thus, further studies are required to understand how developmental schedules have coevolved with ecological and anatomical factors.

The gut microbiome is gaining recognition for its role in primate nutrition, but we stand to benefit from microbiome comparisons across diverse hosts and environmental conditions. We compared gut microbiome structure in four lemur species from four phylogenetic lineages, including 9 individual mouse lemurs (Microcebus danfossi), 6 brown lemurs (Eulemur fulvus), 20 sifakas (Propithecus coquereli), and a single sportive lemur (Lepilemur grewcockorum). In northwestern Madagascar, these species are sympatric, but use different feeding strategies to cope with environmental challenges, including relying on tree gums and insects (mouse lemurs), and some vs. significant leaf matter (brown lemurs vs. sifakas and sportive lemurs). From one fecal sample collected per lemur in the dry season in the Anjajavy Forest, we determined gut microbiome diversity, variability, and membership via 16S rRNA sequencing. The lemurs harbored strongly species-specific gut microbiomes. Brown lemurs showed more diverse and generalized consortia; mouse lemurs, sifakas, and the sportive lemur had less diverse consortia with more distinct memberships. Consistent with their fallback foods, mouse lemur microbiomes included taxa putatively associated with gum and insect digestion, whereas those of sifakas and the sportive lemur showed stronger and distinct signatures of leaf fiber and secondary compound metabolism. These results point to feeding strategy, intertwined with host phylogeny, as a driver of gut microbiome composition, but highlight real-time dietary specificity as a contributing driver of microbiome diversity. While illuminating how gut microbiomes facilitate host nutrition on challenging foods, these results help explain how ecologically diverse primates living in sympatry may differentially cope with seasonal or stochastic lean times.

Habitat loss and fragmentation pose a significant threat to many primate species worldwide, yet community-level responses are complex and nuanced. Despite repeated calls from primatologists and the wider conservation community to increase monitoring initiatives that assess long-term population dynamics, such studies remain rare. Here we summarize results from a longitudinal study set in the littoral forests of southeast Madagascar. Littoral forests are a useful model for monitoring lemur population dynamics, as they are relatively well studied and their highly fragmented nature enables the effect of forest size and anthropogenic impacts to be examined. This study focuses on three Endangered nocturnal lemur species—Avahi meridionalis, Cheirogaleus thomasi, and Microcebus tanosi—across three forest fragments of different size and with different usage histories. Between 2011 and 2018, we walked 285 km of line transect and recorded 1968 lemur observations. Based on distance sampling analysis our results indicate that nocturnal lemurs respond to forest patch size and to levels of forest degradation in species-specific ways. The largest species, A. meridionalis, declined in density and encounter rate over time across the three study forests. C. thomasi populations appeared stable in all three fragments, with densities increasing in the most degraded forest. M. tanosi encounter rates were extremely low across all study fragments but were lowest in the most heavily degraded forest fragment. Our results emphasize the importance of localized pressures and species-specific responses on population dynamics. Monitoring population trends can provide an early warning signal of species loss and species-specific responses can inform crucial intervention strategies.

Hunting is one of the greatest threats to nonhuman primates worldwide. Despite Madagascar’s status as a primate mega-diversity country, a critical lack of information on the hunting of lemurs at the national scale persists. Here, we synthesize the current state of knowledge of the annual rates of household-level lemur hunting near ten protected areas, representing most ecoregions in Madagascar. We examine geographic and taxonomic variation in lemur hunting, including an analysis of hunting relative to species density, extinction risk, and intrinsic ecological characteristics of species. We found that lemurs are commonly hunted across Madagascar; the rural households in our study ate, on average, more than one lemur each year, or a median of 4.1% of the lemur species’ population size where densities are known. However, this pressure varied significantly across sites and species, reaching its highest levels in the northeastern rainforest region. While hunting levels are concerning for numerous threatened species, hunting pressure was driven primarily by species availability, and among ecological traits, small body size was related to increased hunting; however, conservation status showed no such relationship. This first national-level assessment of hunting, including one-third of Madagascar’s lemur species and more than a tenth of the world’s primates, identifies regional variation and lemur taxa at acute risk from hunting—important steps toward developing targeted strategies to conserve one of the world’s most threatened groups of vertebrates.

A key aspect of a primate’s ecology is its food source, the very nature of which is spatially and seasonally dependent and may be affected by anthropic pressures. One of the most endangered, yet best-studied, strepsirrhine primates is the ring-tailed lemur (Lemur catta), a species that has experienced significant human-induced habitat loss over many decades. To help understand feeding variability across time and space, I present a literature review of plant species (and parts) fed on by ring-tailed lemurs at nine sites in Madagascar: Ambatotsirongorongo, Andringitra Massif, Anja Reserve, Antserananomby, Berenty Reserve, Beza Mahafaly Special Reserve, Cap Sainte-Marie, Tsaranoro Valley Forest, and Tsimanampetsotsa National Park. I gathered literature using keyword searches on Google Scholar ( https://scholar.google.com/ ) and verified scientific names using the “Catalogue of the Plants of Madagascar” ( http://legacy.tropicos.org/Project/Madagascar ). From 24 studies, I identify 221 genera and 241 species of consumed plants, with 92 genera and 70 species consumed at two or more sites. Based on the available distribution data, 63% of species are endemic and 22% native. Sixty-seven plants are known only by Malagasy common names and excluded from analyses. When authors identify the plant tissue consumed, 52% of species in the diet are represented by a single tissue type, typically leaves (mature and immature) or fruit (ripe or unripe). This review highlights the importance of studying multiple populations when creating dietary summaries of species and should prove valuable to those exploring ecological trends and habitat use by ring-tailed lemurs.

Detailed knowledge of a species’ vocal repertoire is an essential component for the interpretation of its social interactions and behavior. In the case of cryptic nocturnal primates, vocalizations are also a valuable tool for species identification, and possibly to discriminate between the sexes and/or group memberships during noninvasive field identification, monitoring, and conservation efforts. Here we describe the vocal repertoire of the northern giant mouse lemur, Mirza zaza, a small nocturnal primate endemic to northwest Madagascar, and analyze the repertoire to identify vocalizations for field identification and monitoring. We recorded vocalizations of a captive population of 40 M. zaza individuals at the Duke Lemur Center, USA, with detailed observations of call-associated behaviors of eight individuals in two groups. Based on their acoustic structure, we identified 10 different call types, which were correctly classified (92.8%) by a discriminant function analysis. The described adult call types occurred in the context of advertisement, alarm, affiliative behavior, agonistic behavior, and locomotion. Nine of these call types were already present in infants. To aid call classification, we used the acoustic structure of calls to construct a set of call classification rules for M. zaza. Among the loud vocalizations that were candidates for acoustic monitoring we document significant sex differences in the acoustic structure of trill calls of M. zaza, and significant differences between two groups in their loud whistle calls. The vocal repertoire described here will not only form the basis for future comparative and phylogenetic studies of lemur vocalizations; it will also enable rapid identification of this species for noninvasive acoustic surveys in their natural habitat to assess and monitor population densities and establish range boundaries, thus aiding conservation efforts for this threatened lemur species.

With the predicted increase in extreme weather events as a result of global climate change, animals living in dry or seasonally dry habitats are likely to experience dramatic fluctuations in water availability from season to season and year to year. Understanding how animals respond to short-term changes in water availability is paramount for future conservation and management of water-dependent wild populations. We investigated how short-term changes to the availability of water influenced habitat use of four groups of red-fronted lemurs (Eulemur rufifrons) in a dry deciduous forest in western Madagascar using detailed spatial data collected from GPS collars over 15 weeks. We experimentally manipulated water availability in the habitat and compared ranging patterns of the lemurs during the experiments to those before and after the experiments. Lemur groups shifted the intensity of their habitat use relative to changes in natural and experimental water availability. Specifically, lemurs were more likely to spend time in areas near experimental water sources during the experiment than in the same areas without water. Lemurs were less likely to spend time near previous habitual water sources when experimental water sources were available. We observed shifts in ranging intensity in response to natural changes to water availability when waterholes disappeared across the dry season. Our findings support the importance of water for shaping wild animal ranging patterns. We propose that water should be a primary consideration in future studies of habitat use, especially given the potential for climate change and human land use to further alter water availability for wild animals.

Intergroup encounters are common in nonhuman primates and can vary from affiliative to aggressive. We extracted data from the literature to test five different hypotheses: 1) where there are group size differences between opposing groups, whether the larger group is more likely to win an intergroup encounter than the smaller group; 2) whether the likelihood of a group engaging in aggressive intergroup encounters increases with group size; and 3–5) whether dominant, older individuals, and/or males are more likely to participate aggressively in intergroup encounters than subordinate, younger individuals and/or females. Our data set comprised 52 studies on 31 primate species (3 lemur species, 5 New World monkeys, 19 Old World monkeys, and 4 apes). We found that the larger group is more likely to win an encounter against a smaller group than vice versa. We found no significant relationship between group size and propensity to be aggressive during intergroup encounters. We found weak/no support for the effect of age, dominance rank, and sex on the frequency of aggression displayed toward outgroup individuals during intergroup encounters. Species- and population-specific differences in inter- and intragroup competition and in the degree of the unequal distribution of resources across group members may explain why age, dominance rank, and sex are not strong predictors of aggression during intergroup encounters.

Effective, targeted management and conservation plans for wildlife populations require reliable population sampling and estimation. Unfortunately, robust, comprehensive primate population estimates are often lacking, particularly for rare, elusive species. Historically, population estimates of primates have relied on labor-intensive line-transect sampling and distance estimation techniques. We used occupancy sampling to estimate the probability of occupancy and detection of seven lemur species in Ranomafana National Park, Madagascar, and explore relationships between occupancy and detection and landscape, habitat, and co-occurring species variables. We detected and provide estimates of occupancy and/or detection for seven lemur species in a World Heritage Site: Ranomafana National Park, Madagascar. We found habitat type was an important variable explaining occupancy patterns for detection of golden bamboo lemur (Hapalemur aureus), as well as red bellied lemur (Eulemur rubriventer) and black-and-white ruffed lemur (Varecia variegata). The presence of free-ranging dogs (Canis familiaris) was an important factor in several competing models for red-bellied lemurs and eastern lesser bamboo lemurs (Hapalemur griseus), highlighting the threat posed by this exotic predator to primates. While some estimates had error values overlapping zero, reflecting the rarity and low detection of these species, these results indicate the importance of protecting multiple forest types to maintain lemur biodiversity and the underappreciated conservation threat of invasive species in Madagascar.

Temperature, rainfall, and resource availability may vary greatly within a single year in primate habitats. Many primate species show behavioral and physiological adaptations to this environmental seasonality, including changes to their diets and activity. Sahamalaza sportive lemurs (Lepilemur sahamalaza) inhabit the northwest of Madagascar and have been studied only during the dry, colder period of the year. We investigated potential effects of climate seasonality on this species by collecting behavioral data between October 2015 and August 2016, encompassing both the warmer wet and the colder dry seasons. We collected 773.15 hours of behavioral data on 14 individual sportive lemurs to investigate year-round activity budgets, ranging behavior, and sleeping site locations. Additionally we recorded temperature and rainfall data at our study site to describe the environmental conditions during the study period. The study individuals significantly decreased their time spent traveling and increased their time spent resting in the dry season compared to the wet season. Although home range size and path lengths did not differ over the study period, sleeping locations were significantly different between seasons as the lemurs focused on more confined areas in colder periods. Overall, the results indicate that Sahamalaza sportive lemur behavior varies with season, in line with reports for other primates. Electronic supplementary material The online version of this article (10.1007/s10764-018-0059-1) contains supplementary material, which is available to authorized users.

Forest loss, fragmentation, and anthropization threaten the survival of forest species all over the world. Shifting agriculture is one of these threatening processes in Madagascar. However, when its cycle is halted and the land is left to regenerate, the resulting growth of secondary forest may provide a viable habitat for folivorous and omnivorous lemur species. We aimed to identify the response of nocturnal lemurs to different successional stages of regenerating secondary, degraded mature, and mature forest across a mosaic-type landscape. We surveyed four nocturnal lemur species (Avahi laniger, Microcebus cf. simmonsi, Allocebus trichotis, and Daubentonia madagascariensis) in four forest types of varying habitat disturbance in northeastern Madagascar. We estimated densities in mature and regenerating secondary forest for the eastern woolly lemur (Avahi laniger) and mouse lemur (Microcebus cf. simmonsi), two sympatric species with folivorous and omnivorous diets respectively. We did not estimate densities of Allocebus trichotis and Daubentonia madagascariensis owing to small sample size; however, we observed both species exclusively in mature forest. We found higher population densities of A. laniger and M. cf. simmonsi in secondary than in mature forest, showing the potential of regenerating secondary forest for lemur conservation. Several environmental factors influenced the detectability of the two lemur species. While observer and habitat type influenced detection of the eastern woolly lemur, canopy height and vine density influenced detection of mouse lemurs. Understanding how different species with different diets interact with anthropogenically impacted habitat will aid future management decisions for the conservation of primate species.

Frugivorous primates in the family Lemuridae, the largest seed dispersers in Madagascar, often modify their behavior dramatically to cope with seasonal fluctuations in food availability and climate. Such behavioral strategies influence seed dispersal distances and seed shadows, which determine seed fate, gene flow, and the geographical range expansion of plant populations. To examine seasonal variation in seed shadows generated by the common brown lemur (Eulemur fulvus), I combined data on movements of a wild group of lemurs in northwestern Madagascar from full-day observations made twice weekly for 1 year and full-night observations made once a fortnight during the dry season, with gut passage times for three captive individuals in a Malagasy zoo. During the rainy season, brown lemurs increased traveling effort (mean daily path lengths: 1172 ± SE 59 m), adopting a high-cost/high-yield foraging strategy to maximize harvest under periods of fruit abundance; this resulted in long seed dispersal distances (median: 170 ± MAD 77 m). During the dry season, daily path lengths (mean: 469 ± SE 30 m) were shorter owing to midday resting and consumption of water-rich succulent leaves, probably to avoid overheating and dehydration. These behaviors led to short-distance seed dispersal (median: 75 ± MAD 47 m). Although brown lemurs moved nocturnally during the dry season (mean nightly path lengths: 304 ± SE 58 m), nocturnal seed dispersal distances were short (median: 34 ± MAD 21 m). This seasonal variation in seed shadows might cause different population dynamics for rainy- and dry-season-fruiting species of large-seeded plants that depend on brown lemurs for seed dispersal. Additionally, lemur-facilitated seed dispersal distances were shorter than those of large frugivores elsewhere in the world. Therefore, lemur-mediated seed dispersal systems are likely to be vulnerable to forest fragmentation, which can isolate new recruits and prevent gene flow among plant metapopulations.

Anthropogenic disturbances have resulted in declines of seed-dispersing primate frugivores in tropical forests. Previous work has suggested that loss of seed dispersal by large frugivores may have a negative impact on ecosystem carbon storage by reducing tree biomass. However, we know little about the potential impacts of losing frugivores in Madagascar’s diverse rainforest ecosystem. Understanding the effects of frugivore extinction on carbon loss is relevant in Madagascar, where threatened lemur taxa are the only dispersers of many large-seeded plant species. Using a dataset of tree species composition and traits from the southeastern rainforests of Ranomafana National Park, we examined whether seed size and lemur-dependent dispersal are positively associated with above-ground tree biomass. We then simulated different scenarios of population declines of large-seeded trees (>10 mm seed length) dependent on lemur-mediated seed dispersal, to examine potential directional changes in carbon storage capacity of Malagasy forests under lemur loss. Lemur-dispersed tree species, which have large seeds, had higher above-ground biomass than other species. Our simulations showed that the loss of large frugivorous primates in Madagascar may decrease the forest’s potential to store carbon. These results demonstrate the importance of primate conservation for maintaining functioning ecosystems and forest carbon stocks in one of the world’s hottest hotspots of biodiversity.

Dietary data are used to categorize species diets, but these categorizations do not take into account the mutability of food resources in time or space, the level of interspecific competition in various communities as these resources change, nor the dietary flexibility of species. In this study, we assess the diets of three sympatric species, Eulemur rufifrons, Propithecus edwardsi, and Varecia variegata, in the Vatoharanana site in Ranomafana National Park, Madagascar. We determine dietary diversity, overlap, and interannual variation with data collected from 2001 to 2003. We then compare results on food preference and time feeding with data collected on each species in the late 1980s and early 1990s to determine whether these findings are consistent over the long term. We found little interannual variation in the proportion of time spent eating particular plant parts for each of the lemur species during the three study years (2001–2003), and between the earlier and current study. Food items were not always consumed based solely on availability. Dietary diversity was lower in the two frugivorous species (V. variegata and E. rufifrons) compared with the folivorous species (P. edwardsi), and V. variegata and E. rufifrons were more likely to focus their feeding time on one particular genus and plant part in each year. The study species used different strategies to deal with food, particularly fruit, shortages such as a plastic social structure (V. variegata), habitat shifting (E. rufifrons), and dietary switching (P. edwardsi). Although there was low dietary overlap between the study species, they depended on a small number of shared fruits in each of the study years (Chrysophyllum, Syzygium, Ocotea, Plagioscyphus), which may indicate some potential for interspecific competition. Because these lemur species, like all primates, lead relatively long lives (avg. >30 years) and have slow rates of aging, longitudinal studies are needed to test hypotheses reliant on basic dietary information.

Phylogeographic barriers, together with habitat loss and fragmentation, contribute to the evolution of a species’ genetic diversity by limiting gene flow and increasing genetic differentiation among populations. Changes in connectivity can thus affect the genetic diversity of populations, which may influence the evolutionary potential of species and the survival of populations in the long term. We studied the genetic diversity of the little known Northern rufous mouse lemur (Microcebus tavaratra), endemic to Northern Madagascar. We focused on the population of M. tavaratra in the Loky–Manambato region, Northern Madagascar, a region delimited by two permanent rivers and characterized by a mosaic of fragmented forests. We genotyped 148 individuals at three mitochondrial loci (D-loop, cytb, and cox2) in all the major forests of the study region. Our analyses suggest that M. tavaratra holds average genetic diversity when compared to other mouse lemur species, and we identified two to four genetic clusters in the study region, a pattern similar to that observed in another lemur endemic to the region (Propithecus tattersalli). The main cluster involved samples from the two mountain forests in the study region, which were connected until recently. However, the river crossing the study region does not appear to be a strict barrier to gene flow in M. tavaratra. Finally, the inferred demographic history of M. tavaratra suggests no detectable departure from stationarity over the last millennia. Comparisons with codistributed species (P. tattersalli and two endemic rodents, Eliurus spp.) suggest both differences and similarities in the genetic clusters identified (i.e., barriers to species dispersal) and in the inferred demographic history. These comparisons suggest that studies of codistributed species are important to understand the effects of landscape features on species and to reconstruct the history of habitat changes in a region.

Extensive areas of forest are cleared every year to establish new agricultural land in the tropics, resulting in a catastrophic loss in habitat for the world’s primates. A prominent example of this process is Madagascar, where an increasing demand for arable land has led to the once-forested landscape to be now dominated by agricultural areas used for the cultivation of food and cash crops. Despite the prominence of these plantations throughout Madagascar, their suitability as a habitat to support endemic lemur populations remains unclear. Here, we assessed lemur presence in vanilla plantations, Madagascar’s principal export crop, within the northeastern Sava region with the use of line transects. We confirmed the presence of five lemur species, four of which were nocturnal cheirogaleids, in these vanilla plantations. Intensively farmed vanilla plantations and those in existing stands of vegetation supported at least one species of lemur. Furthermore, lemurs were significantly more likely to be present in plantations grown close or adjacent to natural forest fragments, compared to more intensively farmed, anthropogenic sites. In comparison, we observed eight lemur species in natural forest fragment sites in close proximity to the vanilla plantation sites, four of which we did not observe in any of the plantation sites. Our results provide evidence of lemurs using vanilla plantations and show that vanilla plantations may act as extensions of suitable habitat for lemurs, suggesting that they may also function as matrices between isolated forest fragments through which gene flow can occur. These are important and encouraging findings for both lemur conservation and for sustainable agroforestry undertaken by local farming communities.

Sympatric species are known to host the same parasites species. Nevertheless, surveys examining parasite assemblages in sympatric species are rare. To understand how parasite assemblages in sympatric host species differ in a given locality, we used a noninvasive identification method based on high-throughput sequencing. We collected fecal samples from sympatric species in Ranomafana National Park, Madagascar, from September to December in 2010, 2011, and 2012 and identified their parasites by metabarcoding, sequencing a region of the small ribosomal subunit (18S) gene. Our survey included 11 host species, including endemic primates, rodents, frogs, gastropods, and nonendemic rats and dogs. We collected 872 samples, of which 571 contained nematodes and 249 were successfully sequenced. We identified nine putative species of parasites, although their correspondence to actual parasite species is not clear as the resolution of the marker gene differs between nematode clades. For the host species that we successfully sampled with 10 or more positive occurrences of nematodes, i.e., mouse lemurs (Microcebus rufus), black rats (Rattus rattus), and frogs (Anura), the parasite assemblage compositions differed significantly among host species, sampling sites, and sampling years. Our metabarcoding method shows promise in interrogating parasite assemblages in sympatric host species and our results emphasize the importance of choosing marker regions for parasite identification accuracy.

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

Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit.

Geographic patterns of biodiversity result from broad-scale biogeographic and present-day ecological processes. The aim of this study was to investigate the relative importance of biogeographic history and ecology driving patterns of diversity in modern primate communities in Madagascar. I collected data on endemic lemur species co-occurrence from range maps and survey literature for 100 communities in protected areas. I quantified and compared taxonomic, phylogenetic, and functional dimensions of intra- and intersite diversity. I tested environmental and geographic predictors of diversity and endemism. I calculated deforestation rates within protected areas between the years 2000 and 2014, and tested if diversity is related to forest cover and loss. I found the phylogenetic structure of lemur communities could be explained primarily by remotely sensed plant productivity, supporting the hypothesis that there was ecological differentiation among ecoregions, while functional-trait disparity was not strongly related to environment. Taxonomic and phylogenetic diversity also increased with increasing topographic heterogeneity. Beta diversity was explained by both differences in ecology among localities and potential river barriers. Approximately 3000 km2 were deforested in protected areas since the year 2000, threatening the most diverse communities (up to 31%/park). The strong positive association of plant productivity and topographic heterogeneity with lemur diversity indicates that high productivity, rugged landscapes support greater diversity. Both ecology and river barriers influenced lemur community ecology and biogeography. These results underscore the need for focused conservation efforts to slow the loss of irreplaceable evolutionary and ecological diversity.

Primate vocalizations convey a variety of information to conspecifics. The acoustic traits of these vocalizations are an effective vocal fingerprint to discriminate between sibling species for taxonomic diagnosis. However, the vocal behavior of nocturnal primates has been poorly studied and there are few studies of their vocal repertoires. We compiled a vocal repertoire for the Endangered Sambirano mouse lemur, Microcebus sambiranensis, an unstudied nocturnal primate of northwestern Madagascar, and compared the acoustic properties of one of their call types to those of M. murinus and M. rufus. We recorded vocalizations from radio-collared individuals using handheld recorders over 3 months. We also conducted an acoustic survey to measure the vocal activity of M. sambiranensis in four forest habitat types at the study site. We identified and classified five vocalization types in M. sambiranensis. The vocal repertoires of the three Microcebus species contain very similar call types but have different acoustic properties, with one loud call type, the whistle, having significantly different acoustic properties between species. Our acoustic survey detected more calls of M. sambiranensis in secondary forest, riparian forest, and forest edge habitats, suggesting that individuals may prefer these habitat types over primary forest. Our results suggest interspecific differences in the vocal repertoire of mouse lemurs, and that these differences can be used to investigate habitat preference via acoustic surveys.

Evidence of historic predation is important to understand the role that predators play in molding fundamental aspects of primate biology. We examined the geographic demise of Prolemur simus from the perspective of its past behavioral ecology. Using paleontological data from the Late Pleistocene–Holocene deposits at Ankarana Massif, northern Madagascar, we test the hypothesis that 1) multiple predators preyed on P. simus in the past and 2) the dietary preferences and habitat preferences of subfossil P. simus were similar to its extant counterpart. We examined 381 subfossil craniodental remains of P. simus from Ankarana. We used dental eruption and macrowear to assign craniodental remains to relative age classes, and carbon (δ13C) and nitrogen (δ15N) stable isotope values in bone collagen to assess variation in this species’ diet and habitat. Skeletal evidence of predation suggests that multiple predators consumed P. simus in the past. Evidence for carnivoran predatory activity includes punctures on the viscerocranium, posterior neurocranium, and angle of the mandible. Evidence for raptor predatory activity includes talon nicks, punctures, and “can-opener” perforations within the orbits or palate. Stable isotope data suggest that the diet of P. simus was remarkably similar among localities inhabited by this species before human arrival, despite varied environmental conditions. These data suggest that P. simus was likely codistributed with large-culmed bamboo in the past as it is today. The synergistic effects of predation and habitat change may explain the biogeographic retreat of P. simus to its present-day distribution in eastern Madagascar. The study of predator–primate dynamics and interactions across contiguous and fragmented forests will increase our understanding of the impact of such dynamics on primate evolution, and improve primate conservation efforts more broadly.

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.

Population decline and fragmentation often lead to reduced genetic diversity and population differentiation. Habitat destruction throughout Madagascar has caused population decline and extinction of many endemic species. Lemur populations, including those of the largest extant lemur, Indri indri, have been fragmented into remaining forest patches. We assessed the level of genetic diversity in indri populations in three protected reserves by genotyping a total of 43 individuals at 17 microsatellite loci. Genetic diversity in terms of heterozygosity was high in all three reserves, with no differences between reserves. Population structure and F ST analyses revealed Analamazaotra Forest Station and the Torotorofotsy Conservation Area, which are separated by ca. 18 km to be genetically differentiated from each other with some admixture. Betampona Strict Nature Reserve, which is separated from the other reserves by ca. 130 km, exhibited clear population genetic differentiation, with no signs of admixture with the other reserves. Our genetic diversity estimates are similar to those for other Indridae in similar habitats and may reflect past rather than current population processes, given that populations have declined recently. Our results suggest that Betampona may be genetically isolated and that it is important to maintain gene flow between remaining populations to prevent loss of genetic diversity for the future conservation of Indri indri.

Primate populations, including Madagascar’s lemurs, are threatened worldwide and conservationists need accurate population estimates to develop targeted conservation plans. We sought to fill knowledge gaps for three lemur taxa —white-fronted brown lemur (Eulemur albifrons); eastern woolly lemur (Avahi laniger); and Allocebus/Microcebus, a category combining observations of hairy-eared dwarf lemurs (Allocebus trichotis) and mouse lemurs (Microcebus spp.)— in northeastern Madagascar by estimating their density, examining how their encounter rates and densities vary across three different forest types, and monitoring trends in encounter rates and densities at resurveyed sites, using data from surveys at six forest sites over a 4-year period (2010–2013). Landscape density for white-fronted brown lemur, eastern woolly lemur, and Allocebus/Microcebus was 21.5 (SE 3.67), 57.7 (SE 9.17), and 39.1 (SE 9.55) individuals/km2, respectively. There was no difference in density estimates at intact and intermediately degraded forest sites; however, we encountered white-fronted brown lemurs more often in intact forest (1.64 ± SE 0.40 individuals/km) than in intermediately degraded and degraded forest (0.15 ± SE 0.06 and 0.16 ± SE 0.06 individuals/km). In addition, we encountered white-fronted brown lemurs at lower rates in 2013 (0.15 ± SE 0.06 individuals/km) compared to 2010 (0.82 ± SE 0.12 individuals/km) at a resurveyed site. Our findings emphasize that primate researchers must account for variation in how lemur encounter rates and densities differ between intact and degraded forests, and although we observed a decline in white-fronted brown lemur encounter rate at our resurveyed site, we caution that changes in lemur encounter rates may simply reflect lower detection rates rather than lower density. Future research should focus on using conventional distance sampling techniques, which are infrequently used in primate studies, to provide more robust density estimates as a way to accurately assess trends and the effects of anthropogenic pressures on lemur populations.

The identification of critical, limited natural resources for different primate species is important for advancing our understanding of behavioral ecology and toward future conservation efforts. The aye-aye (Daubentonia madagascariensis) is an Endangered nocturnal lemur with adaptations for accessing structurally defended foods: continuously growing incisors; an elongated, flexible middle finger; and a specialized auditory system. In some seasons, ca. 90% of the aye-aye’s diet consists of two structurally defended resources: 1) the larvae of wood boring insects, extracted after the aye-aye gnaws through decomposing bark (deadwood), and 2) the seeds of Canarium trees. Aye-ayes have very large individual home ranges relative to most other lemurs, possibly owing to limited resource availability. Identification of limiting dietary factor(s) is critical for our understanding of aye-aye behavioral ecology and future conservation efforts. To investigate whether aye-ayes equally access all deadwood resources within their range, we surveyed two 100 × 100 m forest plots within the territories of two aye-ayes at Sangasanga, Kianjavato, Madagascar. Only 2 of 150 deadwood specimens within the plots (1.3%) appeared to have been accessed by the aye-ayes. To test whether any external or internal deadwood properties explain aye-aye foraging preferences we recorded species, height and diameter, and quantified the internal tree density using a 3D acoustic tomograph for each foraged and nonforaged deadwood resource within the plots, plus 13 specimens (5 foraged and 8 nonforaged) outside the plots. We did not detect any statistically significant preferences for species, diameter, or height. However, results from the acoustic analysis tentatively indicated that aye-ayes are more likely to forage in trees with greater internal (≥6 cm from the bark) densities. This interior region may function as a sounding board in the tap-foraging process to help aye-ayes accurately identify potential grub-containing cavities in the outer 1–4 cm of deadwood.

Genetic data can be combined with ecological data to study the demographic history of a species, identify landscape features that influence migration patterns, and guide conservation efforts. Perrier’s sifaka (Propithecus perrieri) is a Critically Endangered, rare, and elusive social lemur living in a very restricted, fragmented landscape. To assess the effect of habitat loss and fragmentation on the genetic diversity of the Perrier’s sifaka population we examined 24 microsatellite markers genotyped for 67 samples corresponding to 42 individuals. Perrier’s sifaka shows a low current effective population size (ca. 52–105) and a strong heterozygosity excess, suggesting a historically large but dwindling population. Moreover, we identified a pattern of isolation by distance, typical of continuous habitat, suggesting that sifakas were still able to cross the grasslands between forest fragments in the recent past. Our study calls for a unified conservation plan covering the two protected areas where the species is still present, if not the whole area of its past distribution. Further studies inferring the past demographic history of Perrier’s sifaka may confirm the population decline and shed light on its potential causes.

An organism’s body size is intrinsically related to its metabolic requirements, life history profile, and ecological niche. Previous work in primates generally, and lemurs specifically, has shown that body size often correlates with ecological parameters related to temperature and energy availability in the environment, although other studies indicate the absence of any such patterns in lemurs. Here we test hypotheses that predict that body mass in Eulemur should covary with 1) overall food availability or resource seasonality and/or 2) temperature, i.e., Bergmann’s rule. We use data from 722 wild true lemurs to identify population-specific body mass for 27 populations representing 11 of the 12 described Eulemur species, and derive climatic data for each population from the WorldClim database. We use phylogenetic generalized least squares models to evaluate these hypotheses and find that body mass significantly negatively correlates with annual mean temperature and positively correlates with standard deviation of temperature, but does not significantly correlate with annual rainfall or number of dry months. These results indicate that body mass distribution across populations in Eulemur is consistent with Bergmann’s rule, but does not track resource seasonality as seen in other lemurs, e.g., Propithecus. We suggest that the fact that body mass in various lemur radiations correlates with different environmental variables may result in these patterns being obscured when such taxa are combined in a single analysis. This may help explain why some previous work has found little evidence of ecogeographical correlates with body mass across all Lemuriformes.

Recent comparative studies on the evolution of mammalian sociality came to opposite conclusions regarding the direction and drivers of evolutionary transitions in social organization, particularly concerning the evolution of pair-living among primates. Because the genus Eulemur is one of the few exceptional primate genera that contain both group- and pair-living species, eulemurs offer a rare opportunity to illuminate the processes driving social diversity among species with very similar life histories and ecologies. The aims of our study were therefore 1) to reconstruct the evolution of social organization in eulemurs with new demographic and phylogenetic data and 2) to evaluate several hypotheses about the evolution of pair-living with data from our long-term study of Eulemur rufifrons and published data on other eulemurs. Our review of published data confirmed that E. mongoz and E. rubriventer are pair-living, whereas the 10 other species of Eulemur live in groups with multiple adult males and females. Furthermore, pair-living evolved at least once among eulemurs from group-living ancestors. The available comparative evidence indicated that this evolutionary transition was probably not driven by male infanticide, social instability, or singular ecological factors. Instead, we propose that female competition has favored small female group size and that this effect may have been exacerbated by interspecific competition with sympatric congeners in the ancestors of the pair-living species. In conclusion, we confirmed that the evolution of pair-living from group-living ancestors among true lemurs is exceptional, but not unique, among mammals, and that commonly invoked hypotheses for the evolution of pair-living do not appear to be supported for this genus.

All habitats of Madagascar go through a dry season from April to September each year, resulting in a period of fruit scarcity lasting up to 6 months and creating selection pressure for adaptation to fluctuations in resources. Some Cheirogaleid lemurs, including mouse lemurs (Microcebus), use daily torpor and long-term hibernation during this period, saving energy through inactivity. Capture–recapture studies in some mouse lemur populations have suggested a pattern of biased sex ratio throughout the winter as a result of females hibernating while most males remain active. We studied winter activity in a captive population of Microcebus lehilahytsara, Goodman’s mouse lemur, in a large enclosure at Zoo Zurich, Switzerland using capture–recapture methods to determine how this behavior varies with sex and age, and what this pattern suggests about the ultimate cause of torpor use in this clade. Our results suggest that Goodman’s mouse lemurs use torpor to avoid seasonal food shortage, even though they experience less extreme seasonal variability of food availability than western dry forest mouse lemurs. Male and female Goodman’s mouse lemurs are equally capable of winter torpor, and most remaining active individuals are young that have not sufficiently fattened. This suggests that the “ideal” winter behavior for both males and females is torpor, which ultimately avoids periods of seasonal food scarcity.

The evolution of the high level of microendemism in Madagascar’s biota remains poorly understood. Allopatric speciation or adaptations to local conditions along continuous gradients are two mechanisms that could have contributed to the extraordinary radiation of lemurs. Here we tested whether mouse lemurs (Microcebus griseorufus) occurring across three adjacent but distinct vegetation formations (ranging from dry forest to spiny bush) in southwestern Madagascar showed signs of genetic differentiation that could be interpreted as incipient speciation and adaptation to different environmental conditions using analysis of molecular variance and distance-based redundancy analysis. In the context of a mark-recapture study, mouse lemurs were captured with Sherman live traps set eight times for four nights per trapping session in standardized trapping grids in the three vegetation formations between October 2007 and February 2009. For genetic analyses, we used tissue samples from 41 female and 35 male M. griseorufus. Genetic differentiation between demes as estimated by amplified fragment length polymorphism (AFLP) data (as parental markers) and mitochondrial D-loop sequences (as maternally inherited markers) was more pronounced in philopatric females than in males, which are the dispersing sex in this species. In single-factor analyses, isolation-by-ecology had about the same statistical effect as isolation by distance, but isolation-by-ecology was no longer significant once isolation by distance was taken into account. Despite some differentiation between local demes, STRUCTURAMA, a Bayesian approach for inferring population structure from genetic data, assigned all individuals to a single population. Thus, we did not find evidence for incipient ecological speciation as a result of adaptation to the three investigated habitat types on a small geographic scale based on the available samples.

Nonhuman primates differ widely in various aspects of their ecology and are thus particularly suitable for studying the mechanisms underlying interspecies differences in taste perception. Therefore, we assessed taste preference thresholds as well as relative preferences for five food-associated sugars in three adult black-and-white ruffed lemurs (Varecia variegata variegata) using two-bottle choice tests of brief duration (1 min). We found that the subjects significantly preferred concentrations as low as 25 mM sucrose and fructose, and 50 mM glucose, maltose, and lactose over tap water. When given a choice between all binary combinations of the same five saccharides presented at equimolar concentrations of 50, 100, and 200 mM, respectively, the subjects displayed marked preferences for individual sugars in the following order: sucrose > fructose > glucose ≥ maltose ≥ lactose. The sensitivity of the black-and-white ruffed lemurs to the five saccharides falls into the same range as that reported in other primates. The pattern of relative preferences for food-associated sugars was found to be largely similar to that reported in platyrrhine primates and in human subjects, but differed from that reported in a catarrhine primate. Taken together, the results of the present study support the notions that the taste sensitivity in primates for food-associated sugars may correlate with phylogenetic relatedness, with body mass, and with lactose content in milk. Further, the results support the notion that relative preferences for food-associated sugars in primates, but not necessarily their sweet-taste sensitivity, may correlate with dietary specialization.

Diarrhea-associated viruses are common causes of morbidity in humans in developing countries; however, they have seldom been studied in wild primates despite their pathogenic and zoonotic potential. This is of particular concern in Madagascar, one of the world’s poorest and most biodiverse countries. To improve our understanding of diarrhea-associated viruses in human and nonhuman wild primates in Madagascar, we noninvasively collected fecal samples from 7 of the 12 lemur species of Ranomafana National Park, Madagascar and concurrently sampled humans living in proximity to the lemurs. We used standard molecular techniques to screen 84 lemur and 107 human samples for viral groups commonly associated with diarrheal disease in human populations: adenovirus, enterovirus, rotavirus, and norovirus (genogroups GI and GII). Of the seven lemur taxa examined, all were positive for one or more viral group and humans were positive for all viral groups. Norovirus GII was the most common, found in 27 % of lemurs and 37 % of humans, followed by adenovirus, found in 25 % of lemurs and 35 % of humans. The high prevalence (30–50 %) of most viral groups in mouse lemurs (Microcebus rufus) highlights their potential to serve as sentinals of pathogen spillover from humans to wild lemur populations. These results improve our understanding of the diversity and prevalence of key viral taxa in lemur and associated human populations. Further characterization of these viral group sequences has the potential to reveal novel viruses in lemurs and humans in Madagascar and would be needed to determine the zoonotic potential of the viruses detected.