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Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair-living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair-living, red-bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4-V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red-bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red-bellied lemurs' pair-living, pair-bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair-living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution., (© 2024 The Author(s). American Journal of Primatology published by Wiley Periodicals LLC.)

The urgent need for effective wildlife monitoring solutions in the face of global biodiversity loss has resulted in the emergence of conservation technologies such as passive acoustic monitoring (PAM). While PAM has been extensively used for marine mammals, birds, and bats, its application to primates is limited. Black-and-white ruffed lemurs (Varecia variegata) are a promising species to test PAM with due to their distinctive and loud roar-shrieks. Furthermore, these lemurs are challenging to monitor via traditional methods due to their fragmented and often unpredictable distribution in Madagascar's dense eastern rainforests. Our goal in this study was to develop a machine learning pipeline for automated call detection from PAM data, compare the effectiveness of PAM versus in-person observations, and investigate diel patterns in lemur vocal behavior. We did this study at Mangevo, Ranomafana National Park by concurrently conducting focal follows and deploying autonomous recorders in May-July 2019. We used transfer learning to build a convolutional neural network (optimized for recall) that automated the detection of lemur calls (57-h runtime; recall = 0.94, F1 = 0.70). We found that PAM outperformed in-person observations, saving time, money, and labor while also providing re-analyzable data. Using PAM yielded novel insights into V. variegata diel vocal patterns; we present the first published evidence of nocturnal calling. We developed a graphic user interface and open-sourced data and code, to serve as a resource for primatologists interested in implementing PAM and machine learning. By leveraging the potential of this pipeline, we can address the urgent need for effective primate population surveys to inform conservation strategies., (© 2024 The Authors. American Journal of Primatology published by Wiley Periodicals LLC.)

Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C-peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genus Varecia) as a model. We experimentally manipulated the diet of captive black-and-white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4-week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie-restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at -20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C-peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie-restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations., (© 2023 Wiley Periodicals LLC.)

Ruffed lemurs (Varecia spp.) exhibit a unique suite of behavioral traits compared to other lemur species, which includes their fluid fission-fusion social dynamics, communal rearing of parked litters, and pronounced frugivory in their humid rainforest habitats. Given these traits, and the dense rainforests they inhabit, vocal communication may be key to maintaining social cohesion, coordinating infant care, and/or defending their high-quality food resources. Indeed, they are known for their raucous 'roar-shriek' calls. However, there has been surprisingly little research on vocal communication in Varecia species and only two previously published repertoires, both of which were qualitative descriptions of their calls. In this study, we quantitatively examined the vocal repertoire of wild black-and-white ruffed lemurs (Varecia variegata) at Mangevo, Ranomafana National Park, Madagascar. We characterized 11 call types using 33 bioacoustic parameters related to frequency, duration, tonality, and composition. We also used discriminant function analysis and hierarchical clustering to quantitatively and objectively classify call types within the black-and-white ruffed lemur vocal repertoire. The repertoire consists of both monosyllabic and multisyllabic calls that are individually given or emitted in contagious choruses. Eight of the 11 calls were also used in combination or in larger multi-call sequences. The discriminant function analysis correctly assigned call types with 87% success, though this varied greatly by call type (1-65%). Hierarchical clustering identified 3-4 robust clusters, indicating low clustering structure in the data and suggesting that V. variegata exhibits a graded vocal repertoire. Future work should consider the environmental and behavioral contexts in which calls are used to better understand the function of these call types and combinations., (© 2023. The Author(s), under exclusive licence to Japan Monkey Centre.)

Animals' foraging behavior and dietary choices are, in part, driven by their ultimate function: to meet nutritional demands. However, depending on their degree of dietary specialization and the availability and distribution of food resources in their environment, species may utilize different nutritional strategies. With shifting plant phenology, increasing unpredictability of fruiting, and declining food quality in response to anthropogenic climate change, existing nutritional constraints may become exacerbated. Such changes are especially concerning for Madagascar's endemic fruit specialists given the nutrient-limitation of the island's landscapes. In this study, we examined the nutritional strategy of one such fruit-specialist primate, the black-and-white ruffed lemur (Varecia variegata), over a 12-month period (January to December 2018) in Ranomafana National Park, Madagascar. We hypothesized that Varecia would balance nonprotein energy (NPE) to protein (AP) at a high ratio similar to other frugivorous primates, and that they would prioritize protein intake given their high degree of frugivory. We found that Varecia balance NPE:AP at a ratio of 11:1, higher than in any other primate studied to date; however, diets shifted such that nutrient balancing varied seasonally (12.6:1 abundant-9.6:1 lean). Varecia meet NRC suggested recommendations of 5-8% of calories from protein, despite having a diet mostly comprising fruits. However, seasonal shifts in NPE intakes result in significant energy shortfalls during fruit-lean seasons. Flowers provide an important source of NPE during these periods, with flower consumption best predicting lipid intake, suggesting this species' ability to shift resource use. Nevertheless, achieving adequate and balanced nutrient intakes may become precarious in the face of increasing unpredictability in plant phenology and other environmental stochasticities resulting from climate change., (© 2023 Wiley Periodicals LLC.)

Fathers contribute substantially to infant care, yet the mechanisms facilitating paternal bonding and interactions with infants are not as well understood as they are in mothers. Several hormonal changes occur as males transition into parenthood, first in response to a partner's pregnancy, and next in response to interacting with the newborn. These changes may prepare fathers for parenting and help facilitate and maintain paternal care. Experimental studies with monkeys and rodents suggest that paternal care requires elevated estradiol levels, which increase when a male's partner is pregnant and are higher in fathers than non-fathers, but its role in the expression of paternal behaviors throughout infant development is unknown. To assess estradiol's role in paternal care, we analyzed the relationship between paternal estradiol metabolites and 1) offspring age, and 2) paternal care behavior (holding, carrying, huddling, playing, grooming), in wild, red-bellied lemurs (Eulemur rubriventer). We collected 146 fecal samples and 1597 h of behavioral data on 10 adult males who had newborn infants during the study. Estradiol metabolites increased four-fold in expectant males, and in new fathers they fluctuated and gradually decreased with time. Infant age, not paternal behavior, best predicted hormone levels in new fathers. These results suggest that hormonal changes occur in expectant males with facultative paternal care, but they do not support the hypothesis that estradiol is directly associated with the day-to-day expression of paternal care. Future research should explore estradiol's role in facilitating behaviors, including infant-directed attention and responsiveness, or preparing fathers for infant care generally., Competing Interests: Declaration of competing interest None., (Copyright © 2023 Elsevier Inc. All rights reserved.)

Dispersal is a fundamental aspect of primates' lives and influences both population and community structuring, as well as species evolution. Primates disperse within an environmental context, where both local and intervening environmental factors affect all phases of dispersal. To date, research has primarily focused on how the intervening landscape influences primate dispersal, with few assessing the effects of local habitat characteristics. Here, we use a landscape genetics approach to examine between- and within-site environmental drivers of short-range black-and-white ruffed lemur ( Varecia variegata ) dispersal in the Ranomafana region of southeastern Madagascar. We identified the most influential drivers of short-range ruffed lemur dispersal as being between-site terrain ruggedness and canopy height, more so than any within-site habitat characteristic evaluated. Our results suggest that ruffed lemurs disperse through the least rugged terrain that enables them to remain within their preferred tall-canopied forest habitat. Furthermore, we noted a scale-dependent environmental effect when comparing our results to earlier landscape characteristics identified as driving long-range ruffed lemur dispersal. We found that forest structure drives short-range dispersal events, whereas forest presence facilitates long-range dispersal and multigenerational gene flow. Together, our findings highlight the importance of retaining high-quality forests and forest continuity to facilitate dispersal and maintain functional connectivity in ruffed lemurs.

Vocal communication is an important modality for group-living primates inhabiting dense forest habitats that can hinder visual and olfactory signals. Nevertheless, research on primate vocalizations has historically focused on a narrow subset of haplorhine taxa; comparatively few studies have been focused on strepsirrhines, despite facing similar ecological and social challenges. Ruffed lemurs (Varecia)-a taxon known for their raucous calls-are rainforest specialists that exhibit strong fission-fusion dynamics and communally rear large litters of young. However, surprisingly few studies have examined Varecia vocalizations in the wild, meaning virtually nothing is known about the call types or how they facilitate their unique social and reproductive strategies. Our goal for this study was to examine how various contextual factors such as weather, behavioral state, and subgroup size and composition affected vocal activity across call types in wild black-and-white ruffed lemurs. We conducted focal follows on 31 individuals (two communities) in Mangevo (Ranomafana National Park) from May-August 2019 to record behavioral and vocal activity. We distinguished 11 call types, although three (hum, roar-shriek, chatter) constituted the majority of vocal activity. Calling rates were consistent throughout the day, but decreased with high rainfall. We found sex- and subgroup-specific differences in call usage, likely related to female dominance and subgroup composition, respectively. We identified behavioral contexts that some call types were consistently given in; this can be used to help infer call function. This study provides some of the first quantitative analyses of ruffed lemur vocal communication and lays the groundwork for more systematic hypothesis testing in future studies., (© 2021. Japan Monkey Centre.)

Background: Habitat disturbance affects the biology and health of animals globally. Understanding the factors that contribute to the differential responses of animals to habitat disturbance is critical for conservation. The gut microbiota represents a potential pathway through which host responses to habitat disturbance might be mediated. However, a lack of quantitative environmental data in many gut microbiome (GM) studies of wild animals limits our ability to pinpoint mechanisms through which habitat disturbance affects the GM. Here, we examine the impact of anthropogenic habitat disturbance on the diet and GM of the Critically Endangered black-and-white ruffed lemur (Varecia variegata editorum). We collected fecal samples and behavioral data from Varecia occupying habitats qualitatively categorized as primary forest, moderately disturbed forest, and heavily disturbed forest., Results: Varecia diet and GM composition differed substantially across sites. Dietary richness predicted GM richness across sites, and overall GM composition was strongly correlated to diet composition. Additionally, the consumption of three specific food items positively correlated to the relative abundances of five microbial strains and one microbial genus across sites. However, diet did not explain all of the GM variation in our dataset, and differences in the GM were detected that were not correlated with diet, as measured., Conclusions: Our data suggest that diet is an important influence on the Varecia GM across habitats and thus could be leveraged in novel conservation efforts in the future. However, other factors such as contact with humans should also be accounted for. Overall, we demonstrate that quantitative data describing host habitats must be paired with GM data to better target the specific mechanisms through which environmental change affects the GM., (© 2021. The Author(s).)

The Anthropocene is a major threat to biodiversity worldwide. Human pressures including climate change and emerging infectious diseases are presenting new challenges to wildlife, requiring vigilance and monitoring of wild populations to ensure their persistence. In order to monitor fluctuations in health, baseline data from long-term studies are required. Clinical laboratory data on 80 black-and-white ruffed lemurs ( Varecia variegata ), derived from the capture of 98 individuals spanning six field seasons are presented. Serum biochemical profiles showed variation between years that remained within published reference intervals for the species, with the exception of total bilirubin in 2008, and creatine kinase and chloride in 2019. Serum trace minerals and fat-soluble vitamin values also fluctuated between years and are within ranges seen in other lemur species. These results, combined with previously published data on ectoparasite load and population genetic diversity, suggest that the Mangevo ruffed lemur population is healthy and can provide important and valuable baseline data for comparisons moving forward.

In recent decades Madagascar has experienced significant habitat loss and modification, with minimal understanding of how human land use practices have impacted the evolution of its flora and fauna. In light of ongoing and intensifying anthropogenic pressures, we seek new insight into mechanisms driving genetic variability on this island, using a Critically Endangered lemur species, the black-and-white ruffed lemur (Varecia variegata), as a test case. Here, we examine the relative influence of natural and anthropogenic landscape features that we predict will impose barriers to dispersal and promote genetic structuring across the species range. Using circuit theory, we model functional connectivity among 18 sampling localities using population-based genetic distance (F ST ). We optimized resistance surfaces using genetic algorithms and assessed their performance using maximum-likelihood population-effects mixed models. The best supported resistance model was a composite surface that included two anthropogenic features, habitat cover and distance to villages, suggesting that rapid land cover modification by humans has driven change in the genetic structure of wild lemurs. Primary conservation priority should be placed on mitigating further forest loss and connecting regions identified as having low dispersal potential to prevent further loss of genetic diversity and promote the survival of other moist forest specialists.

Neuroendocrine evidence suggests that paternal care is mediated by hormonal mechanisms, where hormonal changes in expectant and new fathers facilitate infant care. In species with obligate and extensive paternal care such as humans, androgen levels decline once males are paired and have offspring, and in direct response to offspring care. Facultative infant care is widespread in the Order Primates, but the underlying hormonal mechanisms are largely unknown. We found that wild, red-bellied lemurs living in family groups (two adults and their presumed offspring) varied in the amount of care they provided infants. The more fathers invested in helping infants (measured as a composite of carrying, holding, huddling, grooming, and playing), and specifically the more they huddled and groomed with infants, the higher their fecal androgen (fA) levels, contrary to expectations. Carrying was negatively related to fA levels. Helping by subadults and juveniles was not related to their own fA levels. Elevated fA levels during infant dependence have been observed in other vertebrate species, and are thought to reflect reinvestment in mating rather than investment in dependent offspring. However, red-bellied lemurs do not mate until after infants are weaned, and they have long-term pair-bonds, suggesting that elevated fA levels play a role in offspring care. These results support a growing body of research suggesting that elevated androgen levels do not inhibit protective infant care., (Copyright © 2017 Elsevier Inc. All rights reserved.)

Vertebrate gut microbiota form a key component of immunity and a dynamic link between an individual and the ecosystem. Microbiota might play a role in social systems as well, because microbes are transmitted during social contact and can affect host behaviour. Combining methods from behavioural and molecular research, we describe the relationship between social dynamics and gut microbiota of a group-living cooperative species of primate, the red-bellied lemur (Eulemur rubriventer). Specifically, we ask whether patterns of social contact (group membership, group size, position in social network, individual sociality) are associated with patterns of gut microbial composition (diversity and similarity) between individuals and across time. Red-bellied lemurs were found to have gut microbiota with slight temporal fluctuations and strong social group-specific composition. Contrary to expectations, individual sociality was negatively associated with gut microbial diversity. However, position within the social network predicted gut microbial composition. These results emphasize the role of the social environment in determining the microbiota of adult animals. Since social transmission of gut microbiota has the potential to enhance immunity, microbiota might have played an escalating role in the evolution of sociality., (© 2017 The Authors. Journal of Animal Ecology © 2017 British Ecological Society.)

This study presents the first detailed morphometric measurements of wild caught black-and-white ruffed lemurs (Varecia variegata) from the eastern rainforests of Madagascar and aims to quantify the morphological variation present throughout their recognized range. One hundred and forty-four adult and juvenile individuals from 15 sites were sampled for 20 cranial, dental and postcranial morphometric and body mass measurements. Data were collected from an equal number of male and female individuals sampled across seasons over a 7-year period (1999-2002, 2004-2006). Results indicate that adult body mass and morphometric measurements varied between sexes across sites; however, the only significant intersexual difference found was that females possessed, on average, longer tails than males. Contrary to previous studies, significant seasonal variation could not be detected in either male or female body mass or testicular volume (i.e., breeding vs. nonbreeding, food-scarce vs. food-abundant seasons). Measurements did, however, vary significantly by site and subspecies, though clinal variation could not explain these differences. The introduced population from Nosy Mangabe exhibited significantly lower body mass and overall body length than all other populations; however, this distinction may not have been attributable to natural variation, and may have instead resulted from the ecologically restrictive habitat (e.g., unusually high lemur population densities, limited food resources, ecological isolation) of this introduced population. Finally, although fore-to-hindlimb, brachium-to-thigh and hindlimb indices were comparable to previous values, forelimb indices calculated here deviate significantly from previous reports, placing V. variegata within the upper range of lemurid taxa. It is currently unknown whether this is an artifact of sampling methods (i.e., live vs. skeletal specimens) or whether this is an avenue that warrants further investigation.