Duke Lemur Center Research Articles

Paternal behavior in captive fat-tailed dwarf lemurs (Cheirogaleus medius) is preserved under socially relevant conditions.

Fat-tailed dwarf lemurs (Cheirogaleus medius), primates endemic to Madagascar, are obligate hibernators that form stable, lifelong pairs in the wild. Given the temporal constraints imposed by seasonal hibernation, infant dwarf lemurs must grow, develop, and wean within the first two months of life. Maternal as well as paternal infant care, observed in the wild, has been deemed critical for infant survival. Given the importance of fathers' involvement in early infant care, we expect this behavior to persist even under captive conditions. At the Duke Lemur Center, in Durham NC, we observed two families of fat-tailed dwarf lemurs and focused on the behavior of adult males within the first two months of the infants' lives. We report evidence of paternal involvement, including babysitting, co-feeding, grooming, accompanying, and leading infants, consistent with observations from the wild. As expected, paternal babysitting decreased as infants gained independence, while co-feeding increased. Supplemental anecdotes, video recorded by observers, also highlight clear cases of involvement by both parents, and even older siblings, in safeguarding and socializing new infants. We argue that maintaining captive fat-tailed dwarf lemur populations under socially and ecologically relevant conditions facilitates the full expression of physiological and behavioral repertoires. Most importantly, it also allows dwarf lemurs to realize their species' potential and become robust proxies of their wild kin.

Primate hibernation: The past, present, and promise of captive dwarf lemurs.

The dwarf lemurs (Cheirogaleus spp.) of Madagascar are the only obligate hibernators among primates. Despite century-old field accounts of seasonal lethargy, and more recent evidence of hibernation in the western fat-tailed dwarf lemur (Cheirogaleus medius), inducing hibernation in captivity remained elusive for decades. This included the Duke Lemur Center (DLC), which maintains fat-tailed dwarf lemurs and has produced sporadic research on reproduction and metabolism. With cumulative knowledge from the field, a newly robust colony, and better infrastructure, we recently induced hibernation in DLC dwarf lemurs. We describe two follow-up experiments in subsequent years. First, we show that dwarf lemurs under stable cold conditions (13°C) with available food continued to eat daily, expressed shallower and shorter torpor bouts, and had a modified gut microbiome compared to peers without food. Second, we demonstrate that dwarf lemurs under fluctuating temperatures (12-30°C) can passively rewarm daily, which was associated with altered patterns of fat depletion and reduced oxidative stress. Despite the limitations of working with endangered primates, we highlight the promise of studying hibernation in captive dwarf lemurs. Follow-up studies on genomics and epigenetics, metabolism, and endocrinology could have relevance across multidisciplinary fields, from biomedicine to evolutionary biology, and conservation.

Diverse Circular DNA Viral Communities in Blood, Oral, and Fecal Samples of Captive Lemurs.

Few studies have addressed viral diversity in lemurs despite their unique evolutionary history on the island of Madagascar and high risk of extinction. Further, while a large number of studies on animal viromes focus on fecal samples, understanding viral diversity across multiple sample types and seasons can reveal complex viral community structures within and across species. Groups of captive lemurs at the Duke Lemur Center (Durham, NC, USA), a conservation and research center, provide an opportunity to build foundational knowledge on lemur-associated viromes. We sampled individuals from seven lemur species, i.e., collared lemur (Eulemur collaris), crowned lemur (Eulemur coronatus), blue-eyed black lemur (Eulemur flavifrons), ring-tailed lemur (Lemur catta), Coquerel's sifaka (Propithecus coquereli), black-and-white ruffed lemur (Varecia variegata variegata), and red ruffed lemur (Varecia rubra), across two lemur families (Lemuridae, Indriidae). Fecal, blood, and saliva samples were collected from Coquerel's sifaka and black-and-white ruffed lemur individuals across two sampling seasons to diversify virome biogeography and temporal sampling. Using viral metagenomic workflows, the complete genomes of anelloviruses (n = 4), cressdnaviruses (n = 47), caudoviruses (n = 15), inoviruses (n = 34), and microviruses (n = 537) were determined from lemur blood, feces, and saliva. Many virus genomes, especially bacteriophages, identified in this study were present across multiple lemur species. Overall, the work presented here uses a viral metagenomics approach to investigate viral communities inhabiting the blood, oral cavity, and feces of healthy captive lemurs.

Metagenome-assembled microvirus and cressdnavirus genomes from fecal samples of house mice (Mus musculus).

House mice, Mus musculus, are highly adapted to anthropogenic spaces. Fecal samples were collected from house mice entering primate enclosure areas at the Duke Lemur Center (Durham, NC, USA). We identified 14 cressdnavirus and 59 microvirus genomes in these mouse feces.

Tradeoffs between bite force and gape in Eulemur and Varecia.

In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines: Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared to Varecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species: Eulemur flavifrons (n = 6; 3F, 3M), Varecia variegata (n = 5; 3F, 2M), and Varecia rubra (n = 5; 5F). Maximum linear and angular gapes were significantly higher for Varecia compared to Eulemur (p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force-gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggest Varecia has reduced bite force capacities in favor of absolutely wider gapes compared to Eulemur in relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.

Telomere dynamics during hibernation in a tropical primate.

Hibernation is a widespread metabolic strategy among mammals for surviving periods of food scarcity. During hibernation, animals naturally alternate between metabolically depressed torpor bouts and energetically expensive arousals without ill effects. As a result, hibernators are promising models for investigating mechanisms that buffer against cellular stress, including telomere protection and restoration. In non-hibernators, telomeres, the protective structural ends of chromosomes, shorten with age and metabolic stress. In temperate hibernators, however, telomere shortening and elongation can occur in response to changing environmental conditions and associated metabolic state. We investigate telomere dynamics in a tropical hibernating primate, the fat-tailed dwarf lemur (Cheirogaleus medius). In captivity, these lemurs can hibernate when maintained under cold temperatures (11-15°C) with limited food provisioning. We study telomere dynamics in eight fat-tailed dwarf lemurs at the Duke Lemur Center, USA, from samples collected before, during, and after the hibernation season and assayed via qPCR. Contrary to our predictions, we found that telomeres were maintained or even lengthened during hibernation, but shortened immediately thereafter. During hibernation, telomere lengthening was negatively correlated with time in euthermia. Although preliminary in scope, our findings suggest that there may be a preemptive, compensatory mechanism to maintain telomere integrity in dwarf lemurs during hibernation. Nevertheless, telomere shortening immediately afterward may broadly result in similar outcomes across seasons. Future studies could profitably investigate the mechanisms that offset telomere shortening within and outside of the hibernation season and whether those mechanisms are modulated by energy surplus or crises.

Urinary C-peptide and total triiodothyronine as energetic biomarkers for studies of lemurs.

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.

Increased physical activity is not related to markers of cardiometabolic health in two lemur species.

Insufficient physical activity is a major risk factor for cardiometabolic disease (i.e., unhealthy weight gain, heart disease, and diabetes) in humans and may also negatively affect health of primates in human care. Effects of physical activity on energy expenditure and cardiometabolic health are virtually unstudied in nonhuman primates. We investigated physical activity and metabolic markers in 15 adult ring-tailed lemurs (Lemur catta) and 11 Coquerel's sifakas (Propithecus coquereli) at the Duke Lemur Center during a period of low activity in winter when the animals were housed in buildings (with outdoor access) and a period of high activity when individuals were free-ranging in large, outdoor, forested enclosures. We compared body mass, blood glucose, triglycerides, HDL- and LDL-cholesterol, physical activity via accelerometry, and total energy expenditure (TEE) via the doubly labeled water method (in ring-tailed lemurs only) between both conditions. Both species were more active and had a lower body mass in summer. Ring-tailed lemurs had a higher TEE and lower triglyceride levels in summer, whereas sifaka had higher triglyceride levels in summer. Individuals that increased their activity more, also lost more body mass. Individuals that lost more body mass, also had a positive change in HDL-cholesterol (i.e., higher values in summer). Changes in activity were not associated with changes in markers of metabolic health, body fat percentage and TEE (both unadjusted and adjusted for body composition). Older age was associated with lower activity in both species, and decreased glucose in ring-tailed lemurs, but was otherwise unrelated to metabolic markers and, for ring-tailed lemurs, adjusted TEE. Overall, body mass was lower during summer but the increase in physical activity did not strongly influence metabolic health or TEE in these populations.

Seasonal variation in glucose and insulin is modulated by food and temperature conditions in a hibernating primate.

Feast-fast cycles allow animals to live in seasonal environments by promoting fat storage when food is plentiful and lipolysis when food is scarce. Fat-storing hibernators have mastered this cycle over a circannual schedule, by undergoing extreme fattening to stockpile fuel for the ensuing hibernation season. Insulin is intrinsic to carbohydrate and lipid metabolism and is central to regulating feast-fast cycles in mammalian hibernators. Here, we examine glucose and insulin dynamics across the feast-fast cycle in fat-tailed dwarf lemurs, the only obligate hibernator among primates. Unlike cold-adapted hibernators, dwarf lemurs inhabit tropical forests in Madagascar and hibernate under various temperature conditions. Using the captive colony at the Duke Lemur Center, we determined fasting glucose and insulin, and glucose tolerance, in dwarf lemurs across seasons. During the lean season, we maintained dwarf lemurs under stable warm, stable cold, or fluctuating ambient temperatures that variably included food provisioning or deprivation. Overall, we find that dwarf lemurs can show signatures of reversible, lean-season insulin resistance. During the fattening season prior to hibernation, dwarf lemurs had low glucose, insulin, and HOMA-IR despite consuming high-sugar diets. In the active season after hibernation, glucose, insulin, HOMA-IR, and glucose tolerance all increased, highlighting the metabolic processes at play during periods of weight gain versus weight loss. During the lean season, glucose remained low, but insulin and HOMA-IR increased, particularly in animals kept under warm conditions with daily food. Moreover, these lemurs had the greatest glucose intolerance in our study and had average HOMA-IR values consistent with insulin resistance (5.49), while those without food under cold (1.95) or fluctuating (1.17) temperatures did not. Remarkably low insulin in dwarf lemurs under fluctuating temperatures raises new questions about lipid metabolism when animals can passively warm and cool rather than undergo sporadic arousals. Our results underscore that seasonal changes in insulin and glucose tolerance are likely hallmarks of hibernating mammals. Because dwarf lemurs can hibernate under a range of conditions in captivity, they are an emerging model for primate metabolic flexibility with implications for human health.

Characterization of Diverse Anelloviruses, Cressdnaviruses, and Bacteriophages in the Human Oral DNA Virome from North Carolina (USA).

The diversity of viruses identified from the various niches of the human oral cavity-from saliva to dental plaques to the surface of the tongue-has accelerated in the age of metagenomics. This rapid expansion demonstrates that our understanding of oral viral diversity is incomplete, with only a few studies utilizing passive drool collection in conjunction with metagenomic sequencing methods. For this pilot study, we obtained 14 samples from healthy staff members working at the Duke Lemur Center (Durham, NC, USA) to determine the viral diversity that can be identified in passive drool samples from humans. The complete genomes of 3 anelloviruses, 9 cressdnaviruses, 4 Caudoviricetes large bacteriophages, 29 microviruses, and 19 inoviruses were identified in this study using high-throughput sequencing and viral metagenomic workflows. The results presented here expand our understanding of the vertebrate-infecting and microbe-infecting viral diversity of the human oral virome in North Carolina (USA).

Identification of diverse papillomaviruses in captive black-and-white ruffed lemurs (Varecia variegata).

Papillomaviruses (PVs) are host-species-specific and tissue-specific viruses that infect a diverse array of vertebrate hosts, including humans and non-human primates, with varying pathogenic outcomes. Although primate PVs have been studied extensively, no complete genome sequences of PVs from lemurs have been determined to date. Saliva samples from three critically endangered, captive black-and-white ruffed lemurs (Varecia variegata variegata) at the Duke Lemur Center (USA) were analyzed, using high-throughput sequencing, for the presence of oral papillomaviruses. We identified three PVs from two individuals, one of which had a coinfection with two different PVs. Two of the three PVs share 99.6% nucleotide sequence identity, and we have named these isolates "Varecia variegata papillomavirus 1" (VavPV1). The third PV shares ~63% nucleotide sequence identity with VavPV1, and thus, we have named it "Varecia variegata papillomavirus 2" (VavPV2). Based on their E1+E2+L1 protein sequence phylogeny, the VavPVs form a distinct clade. This clade likely represents a novel genus, with VavPV1 and VavPV2 belonging to two distinct species. Our findings represent the first complete genome sequences of PVs found in lemuriform primates, with their presence suggesting the potential existence of diverse PVs across the over 100 species of lemurs.

Forest access restores foraging and ranging behavior in captive sifakas.

Captive wildlife benefit from ecologically informed management strategies that promote natural behaviors. The Duke Lemur Center has pioneered husbandry programs rooted in species' ecology for a diversity of lemurs, including housing social groups in multiacre forest enclosures. We systematically document the foraging and ranging patterns of Coquerel's sifakas (Propithecus coquereli) living in these forest enclosures. Coquerel's sifakas are seasonal frugo-folivores that exhibit striking feeding flexibility in the wild. They are also one of the few members of the Indriidae family to persist in captivity. During all-day follows in the spring and summer of 2consecutive years, we tracked the behavior of 14 sifakas in six forest enclosures. The sifakas' ranging and foraging patterns reflected those of wild sifakas in western Madagascar: On average, DLC sifakas occupied 3-day home ranges of 1.2 ha, traveled 473 m/day, and spent 26% of their time foraging for wild foodstuffs. The sifakas foraged most for young and mature leaves, fruits, nuts, and flowers from 39 plant species, especially red maple (Acer rubrum), tulip poplar (Liriodendron tulipifera), black locust (Robinia pseudoacacia), grapevine (Vitis rotundifolia), hickory (Carya spp.), and white oak (Quercus alba). Foraging patterns varied across seasons, enclosure areas, and groups, potentially reflecting differences in phenology, microhabitats, and individual preferences. While demonstrating that captive-bred primates express wild-like behaviors under ecologically relevant conditions, our results underscore the feeding flexibility of the Coquerel's sifaka. Captive wildlife exhibiting the range of species-specific behaviors are key resources for ecological research and might be best suited for future reintroductions.

Food availability and male deference in the female‐dominant ring‐tailed lemur, Lemur catta

Female dominance, a trait common to some Malagasy lemurs, has been viewed as an adaptation that decreases intersexual feeding competition. A hypothesized relationship exists between male “deference” (male submission in the absence of female aggression) and food availability. Sauther (1993) suggested that male ring‐tailed lemurs at the Duke Lemur Center (Pereira et al., 1990) show more deference to females than do males in the wild owing to food abundance in captivity. To reexamine the link between food availability and male deference, we studied agonism and foraging in two nonwild ring‐tailed lemur (Lemur catta) populations: the Los Angeles Zoo and St. Catherines Island (SCI). On SCI, we collected data under two feeding conditions: Low Provisions (low food availability) and High Provisions (high food availability). As expected, male deference measures at our study sites were more similar to measures of deference from other studies of L. catta in captivity than in the wild. Additionally, the change at SCI from low to high food availability was associated with increased male deference to females. Interestingly, male proximity to females during foraging at this location did not notably change between the low to high food availability conditions, suggesting that males were food competitors of females just as often under both feeding conditions. The increase in male deference under conditions of high food availability on SCI was due to males withdrawing more rapidly from female approaches during agonistic interactions. Hence, where food is more abundant, male L. catta are more likely to show submission to females, which appears to be a self‐serving means of avoiding female aggression. Lemur males who are well‐fed appear less apt to risk female aggression to obtain resources than more nutritionally stressed males. Our results support the view of female dominance in lemurs as an adaptive evolutionary response to conditions of resource limitation.

Seasonal differences in hair growth rates of captive aye-aye, red ruffed, and black-and-white ruffed lemurs.

Hair can be an important source of biological information, providing a record of such things as pollutant exposure, hormonal levels, and stable isotope ratios. Hair as a biological sample is easily accessible, easily stored, and resists degradation. Analysis of hair is particularly useful when studying rare and endangered species, such as lemurs, since it can be sampled noninvasively. However, to better interpret the results of stable isotope or other analyses, it is important to understand hair growth rates. We measured hair growth rates in captive aye-ayes (Daubentonia madagascariensis), red ruffed lemurs (Varecia rubra), and black-and-white ruffed lemurs (Varecia variegata), both in winter (December23, 2013, toJanuary13, 2014) and summer (July 10-31, 2013) at the Duke Lemur Center.Hair growth per week in all three species of lemursdiffered significantly between the boreal summer and boreal winter. The aye-aye, black-and-white ruffed lemur, red ruffed lemur had a mean weekly hair growth of 0.195, 0.209, and 0.232 cm, respectively, in the summer. While the aye-aye, black-and-white ruffed lemur, and red ruffed lemur had a mean weekly hair growth of 0.239, 0.464, and 0.479 cm, respectively, in winter. We found no effect of age on hair growth rates, neither in the boreal summer, nor in the boreal winter for black-and-white ruffed lemurs and red ruffed lemurs. A pregnant black-and-white ruffed female displayed negligible hair growth during the northern winter, suggesting that pregnancy may affect the partitioning of resources away from such things as hair growth.

Energetic costs of hindlimb‐dominated locomotion in sifakas (Propithecus verreauxi)

Human bipedal locomotion is unique, requiring a suite of musculoskeletal adaptations that were acquired gradually throughout hominin evolution. For example, lordotic lumbar spines move the center of mass over the hip joint and resists axial compression, short, laterally‐oriented iliac blades increase the leverage of the hip extensors and abductors, and the adducted hallux facilitates weight transfer during a propulsive toe‐off. Sifakas and other primates occasionally move bipedally in the wild, especially in terrestrial settings, but because they lack specialized anatomy, bipedal locomotion should be less efficient. In this study we test the hypothesis that energy costs differ among sifaka locomotor modes and predict that terrestrial bipedal locomotion is associated with greater energy expenditure than their more habitual mode of arboreal locomotion, vertical clinging and leaping. Bipedal (n=77) and vertical clinging and leaping (n=74) gait cycles were filmed in nine sifakas at the Duke Lemur Center. Locomotor data (stride length, peak body height of the cycle, and velocity) were measured from these videos using ImageJ and used to calculate energy expenditure using published equations. Linear mixed models were used to statistically test the differences in energy expenditure between locomotor modes while accounting for the effects of velocity and repeatedly measuring the same individuals. Results demonstrate that the cost of bipedalism is significantly greater than that of vertical clinging and leaping (p<0.0001). This result supports the idea that the locomotor adaptations in the hominin musculoskeletal system reduce the cost of locomoting bipedally. Furthermore, because sifakas rely on bipedal locomotion in terrestrial settings, these results have conservation implications for understanding the energetic demands of sifaka locomotion in deforested habitats.

Preliminary comparisons of learning across four lemur genera at the Duke Lemur Center

Abstract Lemurs have been relatively understudied in cognitive research despite representing an adaptive radiation and occupying a key phylogenetic position as the most basal extant primate lineage. Many of the existing studies have focused on only one lemur species. We aimed to take a comparative approach by examining learning abilities in 66 lemurs from four genera at the Duke Lemur Center in North Carolina. We used a novel two-action puzzle box to assess inter-species variation in learning speed, task proficiency, and social tolerance during trials. We found differences between genera in the percentage of individuals who had successes, individuals’ latency to touch the apparatus and the number of times an individual observed a group member’s success. Eulemur and Varecia had shorter latencies and were observed more by conspecifics compared to Propithecus and Lemur. Shorter latencies may indicate reduced fear or increased motivation, while higher observation rates suggest more leniency or tolerance around the puzzle boxes. These results may be due to species differences in dominance and rank hierarchies; Propithecus and Lemur are more despotic than Eulemur, where some species exhibit sex co-dominance, and Varecia, which live in groups with high fission-fusion dynamics. We also show that even within these overall relationships, the different genera varied substantially in the temporal trajectory of these learning variables through the study trials. Overall, this comparative study provides preliminary insights into the taxon-specific learning trajectories of lemurs and contributes to the growing body of literature examining lemur cognition.

Body Mass and Tail Girth Predict Hibernation Expression in Captive Dwarf Lemurs.

AbstractHibernation, a metabolic strategy, allows individuals to reduce energetic demands in times of energetic deficits. Hibernation is pervasive in nature, occurring in all major mammalian lineages and geographical regions; however, its expression is variable across species, populations, and individuals, suggesting that trade-offs are at play. Whereas hibernation reduces energy expenditure, energetically expensive arousals may impose physiological burdens. The torpor optimization hypothesis posits that hibernation should be expressed according to energy availability. The greater the energy surplus, the lower the hibernation output. The thrifty female hypothesis, a variation of the torpor optimization hypothesis, states that females should conserve more energy because of their more substantial reproductive costs. Contrarily, if hibernation's benefits offset its costs, hibernation may be maximized rather than optimized (e.g., hibernators with greater fat reserves could afford to hibernate longer). We assessed torpor expression in captive dwarf lemurs, primates that are obligate, seasonal, and tropical hibernators. Across 4.5 mo in winter, we subjected eight individuals at the Duke Lemur Center to conditions conducive to hibernation, recorded estimates of skin temperature hourly (a proxy for torpor), and determined body mass and tail fat reserves bimonthly. Across and between consecutive weigh-ins, heavier dwarf lemurs spent less time in torpor and lost more body mass. At equivalent body mass, females spent more time torpid and better conserved energy than did males. Although preliminary, our results support the torpor optimization and thrifty female hypotheses, suggesting that individuals optimize rather than maximize torpor according to body mass. These patterns are consistent with hibernation phenology in Madagascar, where dwarf lemurs hibernate longer in more seasonal habitats.

Enriched sleep environments lengthen lemur sleep duration.

Characteristics of the sleep-site are thought to influence the quality and duration of primate sleep, yet only a handful of studies have investigated these links experimentally. Using actigraphy and infrared videography, we quantified sleep in four lemur species (Eulemur coronatus, Lemur catta, Propithecus coquereli, and Varecia rubra) under two different experimental conditions at the Duke Lemur Center (DLC) in Durham, NC, USA. Individuals from each species underwent three weeks of simultaneous testing to investigate the hypothesis that comfort level of the sleep-site influences sleep. We obtained baseline data on normal sleep, and then, in a pair-wise study design, we compared the daily sleep times, inter-daily activity stability, and intra-daily activity variability of individuals in simultaneous experiments of sleep-site enrichment and sleep-site impoverishment. Over 164 24-hour periods from 8 individuals (2 of each species), we found evidence that enriched sleep-sites increased daily sleep times of lemurs, with an average increase of thirty-two minutes. The effect of sleep-site impoverishment was small and not statistically significant. Though our experimental manipulations altered inter-daily stability and intra-daily variability in activity patterns relative to baseline, the changes did not differ significantly between enriched and impoverished conditions. We conclude that properties of a sleep-site enhancing softness or insulation, more than the factors of surface area or stability, influence lemur sleep, with implications regarding the importance of nest building in primate evolution and the welfare and management of captive lemurs.

On the modulation and maintenance of hibernation in captive dwarf lemurs

In nature, photoperiod signals environmental seasonality and is a strong selective “zeitgeber” that synchronizes biological rhythms. For animals facing seasonal environmental challenges and energetic bottlenecks, daily torpor and hibernation are two metabolic strategies that can save energy. In the wild, the dwarf lemurs of Madagascar are obligate hibernators, hibernating between 3 and 7 months a year. In captivity, however, dwarf lemurs generally express torpor for periods far shorter than the hibernation season in Madagascar. We investigated whether fat-tailed dwarf lemurs (Cheirogaleus medius) housed at the Duke Lemur Center (DLC) could hibernate, by subjecting 8 individuals to husbandry conditions more in accord with those in Madagascar, including alternating photoperiods, low ambient temperatures, and food restriction. All dwarf lemurs displayed daily and multiday torpor bouts, including bouts lasting ~ 11 days. Ambient temperature was the greatest predictor of torpor bout duration, and food ingestion and night length also played a role. Unlike their wild counterparts, who rarely leave their hibernacula and do not feed during hibernation, DLC dwarf lemurs sporadically moved and ate. While demonstrating that captive dwarf lemurs are physiologically capable of hibernation, we argue that facilitating their hibernation serves both husbandry and research goals: first, it enables lemurs to express the biphasic phenotypes (fattening and fat depletion) that are characteristic of their wild conspecifics; second, by “renaturalizing” dwarf lemurs in captivity, they will emerge a better model for understanding both metabolic extremes in primates generally and metabolic disorders in humans specifically.

The Vocal Repertoire of the Northern Giant Mouse Lemur (Mirza zaza) in Captivity

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.