Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Evidence of MHC class I and II influencing viral and helminth infection via the microbiome in a non-human primate.

Until recently, the study of major histocompability complex (MHC) mediated immunity has focused on the direct link between MHC diversity and susceptibility to parasite infection. However, MHC genes can also influence host health indirectly through the sculpting of the bacterial community that in turn shape immune responses. We investigated the links between MHC class I and II gene diversity gut microbiome diversity and micro- (adenovirus, AdV) and macro- (helminth) parasite infection probabilities in a wild population of non-human primates, mouse lemurs of Madagascar. This setup encompasses a plethora of underlying interactions between parasites, microbes and adaptive immunity in natural populations. Both MHC classes explained shifts in microbiome composition and the effect was driven by a few select microbial taxa. Among them were three taxa (Odoribacter, Campylobacter and Prevotellaceae-UCG-001) which were in turn linked to AdV and helminth infection status, correlative evidence of the indirect effect of the MHC via the microbiome. Our study provides support for the coupled role of MHC diversity and microbial flora as contributing factors of parasite infection.

RADseq data reveal a lack of admixture in a mouse lemur contact zone contrary to previous microsatellite results.

Microsatellites have been a workhorse of evolutionary genetic studies for decades and are still commonly in use for estimating signatures of genetic diversity at the population and species level across a multitude of taxa. Yet, the very high mutation rate of these loci is a double-edged sword, conferring great sensitivity at shallow levels of analysis (e.g. paternity analysis) but yielding considerable uncertainty for deeper evolutionary comparisons. For the present study, we used reduced representation genome-wide data (restriction site-associated DNA sequencing (RADseq)) to test for patterns of interspecific hybridization previously characterized using microsatellite data in a contact zone between two closely related mouse lemur species in Madagascar (Microcebus murinus and Microcebus griseorufus). We revisit this system by examining populations in, near, and far from the contact zone, including many of the same individuals that had previously been identified as hybrids with microsatellite data. Surprisingly, we find no evidence for admixed nuclear ancestry. Instead, re-analyses of microsatellite data and simulations suggest that previously inferred hybrids were false positives and that the program NewHybrids can be particularly sensitive to erroneously inferring hybrid ancestry. Combined with results from coalescent-based analyses and evidence for local syntopic co-occurrence, we conclude that the two mouse lemur species are in fact completely reproductively isolated, thus providing a new understanding of the evolutionary rate whereby reproductive isolation can be achieved in a primate.

The Influence of Seasonal Availability of Young Leaves on Dietary Niche Separation in Two Ecologically Similar Folivorous Lemurs.

Traditional socio-ecological models consider that folivorous primates experience limited feeding competition due to the low quality, high abundance, and even distribution of leaves. Evidence from several folivorous species that experience similar constraints to frugivores does not support this hypothesis. The sympatric lemur genera Avahi (Indriidae) and Lepilemur (Lepilemuridae) are good models to understand how food availability constrains folivores since they are both nocturnal, folivorous, and have a comparable body mass. Here we investigate how two nocturnal folivorous primates, Avahi meridionalis and Lepilemur fleuretae, living in the lowland rain forest of Tsitongambarika, South-East Madagascar, partition their dietary niche and are influenced by seasonality of young leaves. To account for food availability, we collected annual phenological data on 769 trees from 200 species. We also collected behavioural data on 5 individuals per lemur species from August 2015 to July 2016 via continuous focal sampling. We found the phenological profile to be seasonal with peaks of leaf flushing, flowering, and fruiting occurring in the austral summer. The two species showed limited dietary overlap (37% rich period, 6% lean period), and A. meridionalis showed higher feeding time and longer daily distances travelled during the rich period. Lepilemur fleuretae showed a dietary shift during the lean period, relying more on mature leaves (73.3% during the lean period, 13.5% during the rich period) but maintaining similar activity levels between seasons. The time spent feeding on food items by A. meridionalis was positively correlated with the nitrogen content and negatively correlated with polyphenols during the rich period. We highlighted a clear effect of the seasonality of young leaves on the diet, nutritional content, activity patterns, and daily distances travelled by two folivorous species, which can be linked to nutrient balancing and time-minimising versus energy-maximising strategies.

The function of geophagy in Nepal gray langurs: Sodium acquisition rather than detoxification or prevention of acidosis.

OBJECTIVES: Geophagy has several hypothesized functions, among them (1) detoxification of plant secondary compounds, for example, tannins, (2) buffering stomach pH to alleviate acidosis caused by high sugar intake, and (3) supplementing the diet with mineral nutrients. We tested these hypotheses in Nepal gray langurs (Semnopithecus schistaceus), a foregut fermenter for which fruits and leaves dominate the diet at different times of the year. MATERIALS AND METHODS: We collected data on feeding time per food item for 21 unprovisioned adult langurs at Ramnagar, Nepal, for 1 year using instantaneous sampling (773 observation hours). We combined these data with relative sugar and tannin content of food items to estimate diet content. We collected rainfall data to distinguish the wet season (May-September) from the dry season (October-April). We collected soil samples from consumption and control sites to test for pH and sodium, potassium, magnesium, and calcium concentrations. RESULTS: Langurs consumed soil from two sources: termite structures (in almost all months) and river banks and beds (mainly in the dry season). Soil feeding was not positively correlated with dietary tannin or sugar content (GLMM). Soil pH was not high enough to buffer stomach contents. Only sodium was significantly higher in consumed soil. DISCUSSION: The most likely function of geophagy was the acquisition of sodium. This conclusion is consistent with reports for other animals. Buffering stomach pH, an often-suggested function for animals with ruminant-like digestion, was not supported. Detoxification, often proposed for animals with a diet high in secondary compounds, was also not supported.

Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past.

Phylogeographic analysis can be described as the study of the geological and climatological processes that have produced contemporary geographic distributions of populations and species. Here, we attempt to understand how the dynamic process of landscape change on Madagascar has shaped the distribution of a targeted clade of mouse lemurs (genus Microcebus) and, conversely, how phylogenetic and population genetic patterns in these small primates can reciprocally advance our understanding of Madagascar's prehuman environment. The degree to which human activity has impacted the natural plant communities of Madagascar is of critical and enduring interest. Today, the eastern rainforests are separated from the dry deciduous forests of the west by a large expanse of presumed anthropogenic grassland savanna, dominated by the Family Poaceae, that blankets most of the Central Highlands. Although there is firm consensus that anthropogenic activities have transformed the original vegetation through agricultural and pastoral practices, the degree to which closed-canopy forest extended from the east to the west remains debated. Phylogenetic and population genetic patterns in a five-species clade of mouse lemurs suggest that longitudinal dispersal across the island was readily achieved throughout the Pleistocene, apparently ending at ∼55 ka. By examining patterns of both inter- and intraspecific genetic diversity in mouse lemur species found in the eastern, western, and Central Highland zones, we conclude that the natural environment of the Central Highlands would have been mosaic, consisting of a matrix of wooded savanna that formed a transitional zone between the extremes of humid eastern and dry western forest types.

Determinants of terrestrial feeding in an arboreal primate: The case of the southern bamboo lemur (Hapalemur meridionalis).

OBJECTIVES: The proximate and ultimate determinants that may have prompted some primates to shift from an arboreal to terrestrial feeding niche, whether due to environmental change, seasonality, and/or predation pressure, are poorly understood. Within a fragmented littoral forest in southeast Madagascar, an arboreal strepsirrhine population spends a large proportion of time on the ground, thus we aimed to identify which factors influence terrestrial feeding. METHODS: From January to December 2013, we conducted 103 full-day focal follows on three social groups of southern bamboo lemurs H. meridionalis. We continuously recorded feeding time on all arboreal and terrestrial items, as well as whether the focal individual was under the canopy or exposed, and the distance to their nearest conspecific neighbor. All observed food items were collected and analyzed for macronutrient content. Daily climatic variables (temperature, precipitation), resource seasonality, daily path length (DPL), along with dietary and predation risk proxies, were used as fixed effects in a linear mixed model, with the daily proportion of terrestrial feeding as the dependent variable. RESULTS: Our model indicated that daily terrestrial feeding increased at cooler temperature, was associated with reduced DPL, and the intake of dietary metabolizable energy increased as terrestrial feeding increased. All other fixed effects were not significant predictors. DISCUSSION: Our study provides a window into the ultimate determinants of niche expansion: ancestral primates, in absence of their primary resources, may have initially descended to the ground in peripheral population range areas where the benefits (e g., nutritional pay-off) out-weighed the costs.

Nutritional consequences of folivory in a small-bodied lemur (Lepilemur leucopus): Effects of season and reproduction on nutrient balancing.

OBJECTIVES: Small-bodied folivores are rare because processing leaves often requires extensive gut adaptations and lengthy retention times for fiber fermentation. However, the <1 kg nocturnal white-footed sportive lemurs (Lepilemur leucopus) persist on a leaf-based diet. We investigated how extrinsic (i.e., seasonality in temperature and food availability) and intrinsic factors (i.e., reproductive state) influence nutrient intake and explored how nutrient and energy needs are met in this species. MATERIALS AND METHODS: We conducted full night focal follows across all seasons and analyzed nutrients in all items eaten by adults of both sexes to investigate nutrient intake and nutritional priorities in L. leucopus. We estimated digestible protein content, as this is a biologically more meaningful measure than crude protein. RESULTS: Protein intake was constant across seasons, while non-protein energy and dry matter intake increased from the hot wet to the cold dry season. Males and females did not differ in their nutrient or apparent energy intake irrespective of female reproductive state. DISCUSSION: We conclude that these animals prioritize protein over non-protein energy intake as dietary protein is in limited supply, and that thermoregulation poses higher energetic costs than reproduction in this species. While protein intake did not differ across female reproductive states, the relative protein content of the diet was highest during the lactation period, indicating that the balance of non-protein to protein intake may be more important than absolute intake. Dry matter intake was high compared to other folivorous primates, indicating that L. leucopus follows an intake rather than an efficiency strategy to meet its energy requirements. Am J Phys Anthropol 160:197-207, 2016. © 2016 Wiley Periodicals, Inc.

Cheating on the mutualistic contract: nutritional gain through seed predation in the frugivorous bat Chiroderma villosum (Phyllostomidae).

Most frugivorous bats are efficient seed dispersers, as they typically do not damage seeds and transport them over long distances. In contrast, bats of the phyllostomid genus Chiroderma cheat fig trees by acting more as seed predators than as seed dispersers. The bats initially separate seeds from fruit pulp in the mouth. After extracting the juice from the fruit pulp, they thoroughly chew the seeds and spit out small seed fragments in a pellet. Consequently, the faeces contain almost no viable seeds. We compared the nutrient content of intact fig seeds with ejecta and faecal samples from both Chiroderma villosum and the 'conventional' frugivorous bat Artibeus watsoni. We show that C. villosum can extract nutrients from the seeds, especially protein and fat. The processing time of figs showed no significant difference between the two bat species. Food-choice experiments showed that C. villosum preferred fig species with more seeds over those with fewer seeds. This preference, in combination with the specialized seed-chewing behaviour, leads to an increased nutrient intake per fig. This unique strategy enables C. villosum to satisfy its nutritional requirements with a lower number of figs than other species, which decreases the amount of energy necessary for foraging flights as well as the predation risk during foraging.

Morphological variability or inter-observer bias? A methodological toolkit to improve data quality of multi-researcher datasets for the analysis of morphological variation.

OBJECTIVES: The investigation of morphological variation in animals is widely used in taxonomy, ecology, and evolution. Using large datasets for meta-analyses has dramatically increased, raising concerns about dataset compatibilities and biases introduced by contributions of multiple researchers. MATERIALS AND METHODS: We compiled morphological data on 13 variables for 3073 individual mouse lemurs (Cheirogaleidae, Microcebus spp.) from 25 taxa and 153 different sampling locations, measured by 48 different researchers. We introduced and applied a filtering pipeline and quantified improvements in data quality (Shapiro-Francia statistic, skewness, and excess kurtosis). The filtered dataset was then used to test for genus-wide sexual size dimorphism and the applicability of Rensch's, Allen's, and Bergmann's rules. RESULTS: Our pipeline reduced inter-observer bias (i.e., increased normality of data distributions). Inter-observer reliability of measurements was notably variable, highlighting the need to reduce data collection biases. Although subtle, we found a consistent pattern of sexual size dimorphism across Microcebus, with females being the larger (but not heavier) sex. Sexual size dimorphism was isometric, providing no support for Rensch's rule. Variations in tail length but not in ear size were consistent with the predictions of Allen's rule. Body mass and length followed a pattern contrary to predictions of Bergmann's rule. DISCUSSION: We highlighted the usefulness of large multi-researcher datasets for testing ecological hypotheses after correcting for inter-observer biases. Using genus-wide tests, we outlined generalizable patterns of morphological variability across all mouse lemurs. This new methodological toolkit aims to facilitate future large-scale morphological comparisons for a wide range of taxa and applications.

Non-structural genes of novel lemur adenoviruses reveal codivergence of virus and host.

Adenoviruses (AdVs) are important human and animal pathogens and are frequently used as vectors for gene therapy and vaccine delivery. Surprisingly, there are only scant data regarding primate AdV origin and evolution, especially in the most basal primate hosts. We detect and sequence AdVs from faeces of two Madagascan lemur species. Complete genome sequence analyses define a new AdV species with a particularly large gene encoding a protein of unknown function in the early gene region 3. Unexpectedly, the new AdV species is not most similar to human or other simian AdVs but to bat adenovirus C. Genome characterisation shows signals of virus-host codivergence in non-structural genes, which show lower diversity than structural genes. Outside a lemur species mixing zone, recombination less frequently separates structural genes, as in human adenovirus C. The evolutionary history of lemur AdVs likely involves both a host switch and codivergence with the lemur hosts.

Fruit scent as an honest signal for fruit quality.

BACKGROUND: Fleshy fruits evolved to be attractive to seed dispersers through various signals such as color and scent. Signals can evolve through different trajectories and have various degrees of reliability. The strongest substrate on which reliable signals can evolve is when there is an inherent link between signal and reward, rendering cheating costly or impossible. It was recently proposed that aliphatic esters in fruit scent may be predictive of sugar content due to their synthesis from products of sugar fermentation. We test this hypothesis on a case study of wild fig species (Ficus tiliifolia) from Madagascar, which relies on seed dispersal by lemurs. RESULTS: We found a strong positive correlation between signal (esters) and reward (sugar). We also found that non-esters, including direct fermentation products, in fruit scent do not indicate sugar levels, which implies that this relationship is not simply a product of fruit maturation wherein more mature fruits emit more scent and contain more sugar. CONCLUSIONS: While based on a single taxon, these results strongly support the hypothesis that a biochemical link between ester synthesis and sugar may render the ester fraction of fruit scent an honest signal for fruit quality, with consequences for animal sensory and feeding ecology, and the evolution of plants in the context of seed dispersal.

Anthropogenic Disturbance Impacts Gut Microbiome Homeostasis in a Malagasy Primate.

Increasing anthropogenic disturbances in Madagascar are exerting constrains on endemic Malagasy lemurs and their habitats, with possible effects on their health and survival. An important component of health is the gut microbiome, which might be disrupted by various stressors associated with environmental change. We have studied the gut microbiome of gray-brown mouse lemurs (Microcebus griseorufus), one of the smallest Malagasy primates and an important model of the convergent evolution of diseases. We sampled two sites: one situated in a national park and the other consisting of a more disturbed site around human settlement. We found that more intense anthropogenic disturbances indeed disrupted the gut microbiome of this lemur species marked by a reduction in bacterial diversity and a shift in microbial community composition. Interestingly, we noted a decrease in beneficial bacteria (i.e., members of the Bacteroidaceae family) together with a slight increase in disease-associated bacteria (i.e., members of the Veillonellaceae family), and alterations in microbial metabolic functions. Because of the crucial services provided by the microbiome to pathogen resistance and host health, such negative alterations in the gut microbiome of mouse lemurs inhabiting anthropogenically disturbed habitats might render them susceptible to diseases and ultimately affecting their survival in the shrinking biodiversity seen in Madagascar. Gut microbiome analyses might thus serve as an early warning signal for pending threats to lemur populations.

A framework for testing the impact of co-infections on host gut microbiomes.

Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases.

Regional, seasonal and interspecific variation in 15N and 13C in sympatric mouse lemurs.

Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson's rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these "rules" and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses (δ(15)N and δ(13)C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ(13)C values, indicating that M. griseorufus feeds more on C(4) and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ(15)N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.

Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar.

We investigated whether or not habitat structure contributes to the separation of two sister species of lemurs and their hybrids. For this, we studied Microcebus murinus and M. griseorufus along a continuous vegetation gradient where populations of the two species occur in sympatry or in allopatry. In allopatry, the two species are generalists without any sign of microhabitat selectivity. In sympatry, both species differed significantly and discriminated against certain habitat structures: M. murinus was found in microhabitats with larger trees than average while M. griseorufus utilized microhabitats with smaller trees. Hybrids between the two species did not show any significant discrimination for or against microhabitat structure and did not differ in their habitat utilization from either parent species. Both species can go into torpor and hibernation. M. griseorufus is seen more frequently during the cool dry season than M. murinus. We assume that M. murinus goes into extended torpor or hibernation more frequently than M. griseorufus. We interpret the different occurrence of large-sized trees in microhabitats of M. murinus as a prerequisite for M. murinus to be able to spend extended periods of time in tree holes that are isolated and allow hibernation at reduced temperature levels.

Camera-trap data do not indicate scaling of diel activity and cathemerality with body mass in an East African mammal assemblage.

Diel activity patterns of animal species reflect constraints imposed by morphological, physiological, and behavioral trade-offs, but these trade-offs are rarely quantified for multispecies assemblages. Based on a systematic year-long camera-trap study in the species-rich mammal assemblage of Lake Manyara National Park (Tanzania), we estimated activity levels (hours active per day) and circadian rhythms of 17 herbivore and 11 faunivore species to determine the effects of body mass and trophic level on activity levels and cathemerality (the degree to which species are active throughout the day and night). Using generalized least squares and phylogenetic generalized least squares analyses, we found no support for the hypothesis that trophic level is positively associated with activity levels. We found no support for activity levels to scale positively with body mass in herbivores or to differ between ruminants and nonruminants; in faunivores, we also did not detect relationships between body mass and activity levels. Cathemerality was positively associated with activity levels but did not scale significantly with body mass. Overall, our findings caution against trophic level or body mass-associated generalized conclusions with regard to diel activity patterns.

Comparative ecology of Guinea baboons (Papio papio).

Thorough knowledge of the ecology of a species or population is an essential prerequisite for understanding the impact of ecology on the evolution of their respective social systems. Because of their diversity of social organizations, baboons (Papio spp.) are a useful model for comparative studies. Comparative ecological information was missing for Guinea baboons (Papio papio), however. Here we provide data on the ecology of Guinea baboons in a comparative analysis on two geographical scales. First, we compare climate variables and land cover among areas of occurrence of all six baboon species. Second, we describe home range size, habitat use, ranging behaviour, and diet from a local population of Guinea baboons ranging near the Centre de Recherche de Primatologie (CRP) Simenti in the Niokolo-Koba National Park, Senegal. Home ranges and daily travel distances at Simenti varied seasonally, yet the seasonal patterns in their daily travel distance did not follow a simple dry vs. rainy season pattern. Chemical food composition falls within the range of other baboon species. Compared to other baboon species, areas occupied by Guinea baboons experience the highest variation in precipitation and the highest seasonality in precipitation. Although the Guinea baboons' multi-level social organization is superficially similar to that of hamadryas baboons (P. hamadryas), the ecologies of the two species differ markedly. Most Guinea baboon populations, including the one at Simenti, live in more productive habitats than hamadryas baboons. This difference in the ecology of the two species contradicts a simple evolutionary relation between ecology and social system and suggests that other factors have played an additional role here.

Secondary seed removal in a degraded forest habitat in Madagascar.

Forest restoration is a prime goal within the 2021-2030 UN "Decade of Ecosystem Resoration". As part of these activities, natural regeneration has to be promoted for biological as well as for economic reasons. For this, the processes of seed dispersal, seed predation and germination have to be understood in the original as well as in degraded vegetation formations. We used seed removal experiments to assess post-dispersal processes that influence recruitment along a gradient of forest degradation in Madagascar analyzing seeds of three animal dispersed tree species. The percentage of seeds consumed or dispersed, declined from forest (28.6%) to degraded forest (17.2%) to savanna (10.8%). Only three out of 1080 seeds were cached and remained intact during the 14-day experiment. All three seeds were cached in the forest habitat and none in the degraded forest and savanna. The low percentage of seeds removed may be due to the lack of endemic rodents caching seeds, as only introduced rats were recorded in the area. The species-poor fauna of potential secondary seed dispersers of the region and especially in the degraded areas might represent an obstacle for diverse regeneration in degraded regions of Madagascar.

Physiology: hibernation in a tropical primate.

The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.