Dietary flexibility of the greater bamboo lemur (Prolemur simus), a specialized feeder, in eastern Madagascar.

The degree of dietary flexibility in primates is species specific; some incorporate a wider array of resources than others. Extreme interannual weather variability in Madagascar results in seasonal resource scarcity which has been linked to specialized behaviors in lemurs. Prolemur simus, for example, has been considered an obligate specialist on large culm bamboo with >60% of its diet composed of woody bamboos requiring morphological and physiological adaptations to process. Recent studies reported an ever-expanding list of dietary items, suggesting that this species may not be an obligate specialist. However, long-term quantitative feeding data are unavailable across this species' range. To explore the dietary flexibility of P. simus, we collected data at two northern sites, Ambalafary and Sahavola, and one southern site, Vatovavy, from September 2010 to January 2016 and May 2017 to September 2018, respectively. In total, we recorded 4022 h of behavioral data using instantaneous sampling of adult males and females from one group in Ambalafary, and two groups each in Sahavola and Vatovavy. We recorded 45 plant species eaten by P. simus over 7 years. We also observed significant differences in seasonal dietary composition between study sites. In Ambalafary, bamboo was the most frequently observed resource consumed (92.2%); however, non-bamboo resources comprised nearly one-third of the diet of P. simus in Sahavola and over 60% in Vatovavy. Consumption of all bamboo resources increased during the dry season at Ambalafary and during the wet season at Vatovavy, but never exceeded non-bamboo feeding at the latter. Culm pith feeding was only observed at Ambalafary, where it was more common during the dry season. We identify P. simus as a bamboo facultative specialist capable of adjusting its feeding behavior to its environment, indicating greater dietary flexibility than previously documented, which may enable the species to survive in increasingly degraded habitats.

Infant survival is significantly impacted by dam- and management-related factors in zoo-managed Eulemur populations.

Due to their potential impact on population growth, many studies have investigated factors affecting infant survival in mammal populations under human care. Here we used more than 30 years of Association of Zoos and Aquariums (AZA) studbook data and contraception data from the AZA Reproductive Management Center, along with logistic regression models, to investigate which factors affect infant survival in four Eulemur species managed as Species Survival Plans® in AZA. Across species, infant survival to 1 month ranged from 65% to 78%. Previous experience producing surviving offspring was positively correlated to infant survival in collared (Eulemur collaris), crowned (Eulemur coronatus), and mongoose (Eulemur mongoz) lemurs. Both dam age and previous use of contraception were negatively correlated to infant survival for collared lemurs, though our results suggest the latter may be confounded with other factors. Blue-eyed black lemurs (Eulemur flavifrons) were affected by birth location, suggesting differences in husbandry that may affect infant survival. These results can be used to assist in reproductive planning or to anticipate the likelihood of breeding success. Population managers may also be able to focus their reproductive planning on younger dams or those with previous experience to predict successful births. Future studies should seek to determine what aspects of previous dam success are most important to infant survival, investigate sire-related factors, and examine factors related to cause of death in infants that may lead to differential survival. Our hope is to present a framework that may be useful for investigating infant survival in other mammal species' breeding programs.

Effects of forest fragmentation on the dietary ecology and activity of a nocturnal lemur community in North West Madagascar.

Deforestation and habitat fragmentation is the primary threat to primate populations. The primates that live within degraded and anthropogenically disturbed habitats typical of fragmented landscapes have to cope with lower availability of resources in comparison to primates in continuous, undisturbed forests. While some species are sensitive to forest fragmentation, some evidence exists to suggest that primates can alter their behavior and adapt to such changes, which enables their survival in suboptimal habitat. In this study, we assessed how forest fragmentation and its associated edge-effects impact the feeding ecology and activity levels of a nocturnal primate community in the Sahamalaza-Iles Radama National Park, North West Madagascar. From March 06, 2019 to May 17, 2022, we collected data on tree and invertebrate phenology at our study site, and feeding ecology and activity for 159 lemur individuals from four species. Fruit and flower availability varied significantly between continuous and fragmented forest, and between forest core and edge areas, with continuous forest exhibiting higher continuous fruit and flower availability. Lemur feeding ecology varied significantly too, as the feeding niches of all four species were significantly different between continuous and fragmented forest and between core and edge areas. However, lemur activity levels were mostly consistent among all forest areas. The results of this study suggest that nocturnal lemurs are able to adapt their dietary ecology in response to the available food sources within their habitat. Due to this flexible ecology and dietary plasticity, the lemurs do not need to significantly alter their behavior in different environments to fulfill their dietary needs. While nocturnal lemurs demonstrate adaptability and flexibility to degraded habitat, it is unclear how far this plasticity will stretch considering that Madagascar's forests are still being cleared at an alarming rate. Urgent conservation action is therefore needed to ensure the future of lemur habitat.

Nutrient balancing in a fruit-specialist primate, the black-and-white ruffed lemur (Varecia variegata).

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.

Seasonal variability in the diet and feeding ecology of black-and-white ruffed lemurs (Varecia variegata) in Ranomafana National Park, southeastern Madagascar.

OBJECTIVES: We characterized the diet and foraging ecology of the black-and-white ruffed lemur (Varecia variegata), a specialized frugivore, and investigated behavioral strategies exhibited in response to seasonal changes in resource availability. MATERIALS AND METHODS: Behavioral data were collected from the same two adjacent communities across 29 months during two observation periods (2007-2008; 2017-2018) in Mangevo, a primary rainforest habitat in southeastern Madagascar. To analyze feeding in the context of energy maximization versus time minimization strategies, we used nonparametric tests to compare plant part constituents, dietary diversity, activity budgets, and canopy strata use between fruit-abundant versus fruit-lean seasons. RESULTS: Individuals dedicated ~30% of their time to feeding year-round, mostly in the middle canopy (11-20 m). Animals fed primarily on fruits (74% of diet), but frugivory decreased and folivory increased markedly during fruit-lean seasons. Abundant season dietary diversity (98 taxa, H' = 0.71-1.37) was greater than lean season diversity (70 taxa, H' = 0.56-1.06), which coincided with less traveling, more resting, and higher canopy use-though interannual variation was observed. CONCLUSIONS: Herein, we describe behavioral and dietary patterns that are concordant with a time minimizing behavioral strategy. Black-and-white ruffed lemur diets comprised lower taxonomic diversity, fewer fruits, and more leaves during fruit-lean months. Further, shifts toward less travel, more resting, and greater use of higher canopy levels during this time were most likely for thermoregulatory benefits.

Sex-Segregated Range Use by Black-and-White Ruffed Lemurs (Varecia variegata) in Ranomafana National Park, Madagascar.

Ranging behavior is one important strategy by which nonhuman primates obtain access to resources critical to their biological maintenance and reproductive success. As most primates live in permanent social groups, their members must balance the benefits of group living with the costs of intragroup competition for resources. However, some taxa live in more spatiotemporally flexible social groups, whose members modify patterns of association and range use as a method to mitigate these costs. Here, we describe the range use of one such taxon, the black-and-white ruffed lemur (Varecia variegata), at an undisturbed primary rain forest site in Ranomafana National Park, Madagascar, and characterize sex differences in annual home range area, overlap, and daily distances traveled. Moreover, we characterize seasonal variability in range use and ask whether ranging behaviors can be explained by either climatic or reproductive seasonality. We found that females used significantly larger home ranges than males, though sexes shared equal and moderate levels of home range overlap. Overall, range use did not vary across seasons, although within sexes, male range use varied significantly with climate. Moreover, daily path length was best predicted by day length, female reproductive state, and sex, but was unrelated to climate variables. While the patterns of range use and spatial association presented here share some similarities with "bisexually bonded" community models described for chimpanzees, we argue that ruffed lemurs best conform to a "nuclear neighborhood" community model wherein nuclear (core) groups share the highest levels of home range overlap, and where these groups cluster spatially into adjacent "neighborhoods" within the larger, communally defended territory.

EthoLoop: automated closed-loop neuroethology in naturalistic environments.

Accurate tracking and analysis of animal behavior is crucial for modern systems neuroscience. However, following freely moving animals in naturalistic, three-dimensional (3D) or nocturnal environments remains a major challenge. Here, we present EthoLoop, a framework for studying the neuroethology of freely roaming animals. Combining real-time optical tracking and behavioral analysis with remote-controlled stimulus-reward boxes, this system allows direct interactions with animals in their habitat. EthoLoop continuously provides close-up views of the tracked individuals and thus allows high-resolution behavioral analysis using deep-learning methods. The behaviors detected on the fly can be automatically reinforced either by classical conditioning or by optogenetic stimulation via wirelessly controlled portable devices. Finally, by combining 3D tracking with wireless neurophysiology we demonstrate the existence of place-cell-like activity in the hippocampus of freely moving primates. Taken together, we show that the EthoLoop framework enables interactive, well-controlled and reproducible neuroethological studies in large-field naturalistic settings.

Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores.

For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber-limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social-group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG-008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce-provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.

Abiotic Factors Affecting the Cathemeral Activity of Eulemur fulvus in the Dry Deciduous Forest of North-Western Madagascar.

Cathemeral primates perform significant amounts of activity during the daylight and dark portions of the 24-h cycle. Most brown lemurs have been reported to be cathemeral. A previous study reported that brown lemurs in Ankarafantsika National Park (ANP) shift their activity pattern from being cathemeral in the dry season to being diurnal in the wet season. From July 2015 to March 2016, we collected data on active behaviour of brown lemurs over 46 full-day and 33 full-night observations, distributed evenly between the dry and wet seasons. This study examined the abiotic factors that potentially allow this seasonal shift from cathemeral to diurnal activity. We analysed the effects of day length (time from sunrise to sunset), nocturnal luminosity, and climatic factors on the diurnal and nocturnal activities of the brown lemurs in ANP using generalized linear mixed models. We found that the brown lemurs were cathemeral regardless of season. Their diurnal activity increased with increasing day length and at high humidity, but decreased on days of high temperature and low lunar luminosity. Their nocturnal activity increased with decreasing day length, during bright nights, at low temperature, and at low humidity. Their diurnal and nocturnal activities decreased during heavy rainfall. These data indicate that the photoperiodic variation entrained their activity rhythm. Bright nights may provide better visibility, advantageous for the detection of predators and food, although it may increase exposure to predators. The modification of activity level with temperature variation can be a behavioural thermoregulation. The high humidity during the wet season probably reduced evaporative cooling, inducing increased body temperature and stimulating water foraging as a potential response to dehydration and active heat dissipation. Investigation on physiological responses to environmental factors is needed to fully understand cathemerality in lemurs. These findings emphasize the flexibility of diurnal and nocturnal activity level of brown lemurs according to the great seasonal variation in tropical dry forests.

Life in a fragment: Evolution of foraging strategies of translocated collared brown lemurs, Eulemur collaris, over an 18-year period.

While the drivers of primate persistence in forest fragments have been often considered at the population level, the strategies to persist in these habitats have been little investigated at the individual or group level. Considering the rapid variation of fragment characteristics over time, longitudinal data on primates living in fragmented habitats are necessary to understand the key elements for their persistence. Since translocated animals have to cope with unfamiliar areas and face unknown fluctuations in food abundance, they offer the opportunity to study the factors contributing to successful migration between fragments. Here, we illustrated the evolution of the foraging strategies of translocated collared brown lemurs (Eulemur collaris) over an 18-year period in the Mandena Conservation Zone, south-east Madagascar. Our aim was to explore the ability of these frugivorous lemurs to adjust to recently colonized fragmented forests. Although the lemurs remained mainly frugivorous throughout the study period, over the years we identified a reduction in the consumption of leaves and exotic/pioneer plant species. These adjustments were expected in frugivorous primates living in a degraded area, but we hypothesize that they may also reflect the initial need to cope with an unfamiliar environment after the translocation. Since fragmentation is often associated with the loss of large trees and native vegetation, we suggest that the availability of exotic and/or pioneer plant species can provide an easy-to-access, nonseasonal food resource and be a key factor for persistence during the initial stage of the recolonization.

Vertical Clinging and Leaping Ahead: How Bamboo Has Shaped the Anatomy and Physiology of Hapalemur.

Hapalemur sps. and Prolemur simus (bamboo lemurs, collectively) stand out from the relatively homogeneous lemurids because they are bamboo feeders and vertical clingers and leapers. This unique diet presents equally unique challenges, like its verticality, toughness, and toxicity. The bamboo lemurs share the generalized anatomy of the other lemurids, but also display some well-documented skeletal adaptations, perhaps to overcome the problems presented by their specialization. Soft-tissue adaptations, however, remain largely unexplored. Explored here are possible soft-tissue adaptations in Hapalemur griseus. We compare H. griseus with other lemurids, Propithecus, Galago, Tarsier, and a tree shrew. Based on the available anatomical and physiological data, we hypothesize that Hapalemur and Prolemur species will have differences in hindlimb morphology when compared with other lemurids. We predict that H. griseus will have more hindlimb muscle mass and will amplify muscle mass differences with increased type II muscle fibers. Relative hindlimb muscle mass in H. griseus is less than other prosimians sampled, yet relative sural muscle mass is significantly heavier (P < 0.01) in H. griseus. Results show that the soleus muscle of H. griseus has a higher amount of type II (fast) fibers in plantarflexors. These findings indicate although H. griseus shares some generalized lemurid morphology, its diet of bamboo may have pushed this generalized lemurid to an anatomical extreme. We suspect additional bamboo-specific adaptations in their anatomy and physiology will be uncovered with further examination into the anatomy of the bamboo lemurs. Anat Rec, 2019. © 2019 Wiley Periodicals, Inc. Anat Rec, 303:295-307, 2020. © 2019 American Association for Anatomy.

Extensive variability in the gut microbiome of a highly-specialized and critically endangered lemur species across sites.

Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black-and-white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on-going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full-day focal animal behavioral follows and collected fecal samples opportunistically across a three-month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea. While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, thereby underscoring the importance of monitoring endangered species at the population-level.

Eulerian videography technology improves classification of sleep architecture in primates.

Sleep is a critically important dimension of primate behavior, ecology, and evolution, yet primate sleep is under-studied because current methods of analyzing sleep are expensive, invasive, and time-consuming. In contrast to electroencephalography (EEG) and actigraphy, videography is a cost-effective and non-invasive method to study sleep architecture in animals. With video data, however, it is challenging to score subtle changes that occur in different sleep states, and technology has lagged behind innovations in EEG and actigraphy. Here, we applied Eulerian videography to magnify pixels relevant to scoring sleep from video, and then compared these results to analyses based on actigraphy and standard infrared videography. We studied four species of lemurs (Eulemur coronatus, Lemur catta, Propithecus coquereli, Varecia rubra) for 12-h periods per night, resulting in 6480 1-min epochs for analysis. Cramer's V correlation between actigraphy-classified sleep and infrared videography-classified sleep revealed consistent results in eight of the nine 12-h videos scored. A sample of the infrared videography was then processed by Eulerian videography for movement magnification and re-coded. A second Cramer's V correlation analysis, between two independent scorers coding the same Eulerian-processed video, found that interobserver agreement among Eulerian videography increased sleep vs. awake, NREM, and REM classifications by 7.1%, 46.7%, and 34.3%, respectively. Furthermore, Eulerian videography was more strongly correlated with actigraphy data when compared to results from standard infrared videography. The increase in agreement between the two scorers indicates that Eulerian videography has the potential to improve the identification of sleep states in lemurs and other primates, and thus to expand our understanding of sleep architecture without the need for EEG.

Use of space and home range characteristics of Lepilemur mittermeieri, an endangered sportive lemur endemic to the Ampasindava peninsula, north-west Madagascar.

Lepilemur mittermeieri, a little-studied sportive lemur of north-west Madagascar, endemic to the Ampasindava Peninsula, faces habitat loss through forest degradation and rapid fragmentation. Understanding its habitat requirement is the first step toward preservation of this threatened forest-dependent species. In this study, we gathered data on the use of space and home range characteristics of L. mittermeieri. We studied individuals from early March to the end of June 2015 and 2016, in three sites of the Ampasindava peninsula. We radio-tracked 15 individuals to obtain detailed information on the size and location of home ranges (around 450 hr of tracking). Direct observation and morphometric measurements provided additional data sets. Both kernel density estimation (KDE) and minimum convex polygon (MCP) methods yielded similar home range sizes (an average of 2.01 ha with KDE method and 1.96 ha with MCP method). We did not find differences in home range size between males and females, with respect to forest type or proximity to the forest edge. Home ranges overlapped and individuals showed low levels of territoriality. We highlighted a sexually-dimorphic trait: males have longer upper canine than females. Our results constitute the first set of ecological information on Lepilemur mittermeieri and could be the basis for a conservation strategy for this endangered species with a very small distribution area.

Species-area relationships of lemurs in a fragmented landscape in Madagascar.

We used species-area relationships (SARs) to investigate the effects of habitat loss on lemur biogeography. We measured species richness via visual surveys on line transects within 42 fragments of dry deciduous forest at the Ambanjabe field site in Ankarafantsika National Park, Madagascar. We measured human disturbance and habitat characteristics within 38 of the 42 fragments. We measured the distance between each fragment and the nearest settlement, continuous forest, and nearest neighboring fragment. We fit 10 candidate SAR models to the data using nonlinear least squares regression and compared them using Akaike's Information Criterion (AIC). To determine how habitat characteristics, as well as area, influenced species richness, we ran a hierarchical partitioning procedure to select which variables to include in generalized additive models (GAMs) and compared them using AIC. Contrary to expectations, we found that lemurs form convex SARs, without a "small island effect", and with the power model being the most likely SAR model. Although we found that four variables (area, survey effort, and total human disturbance, and mean tree height) independently contributed greater than 10% of the variation in lemur species richness, only area was included in the most likely model. We suggest that the power model was the most likely SAR model and our inability to detect a "small island effect" are the result of Microcebus spp. being edge tolerant and capable of dispersing through matrix, scale issues in the study design, and low γ-diversity in the landscape. However, more study is needed to determine what role human disturbance plays in influencing species richness in lemurs.

Pitch control and speed limitation during overground deceleration in lemurid primates.

An animal's fitness is influenced by the ability to move safely through its environment. Recent models have shown that aspects of body geometry, for example, limb length and center of mass (COM) position, appear to set limits for pitch control in cursorial quadrupeds. Models of pitch control predict that the body shape of these and certain other primates, with short forelimbs and posteriorly positioned COM, should allow them to decelerate rapidly while minimizing the risk of pitching forward. We chose to test these models in two non-cursorial lemurs: Lemur catta, the highly terrestrial ring-tailed lemur, and Eulemur fulvus, the highly arboreal brown lemur. We modeled the effects of changes in limb length and COM position on maximum decelerative potential for both species, as well as collecting data on maximal decelerations across whole strides. In both species, maximum measured decelerations fell below the range of pitch-limited deceleration values predicted by the geometric model, with the ring-tailed lemur approaching its pitch limit more closely. Both lemurs showed decelerative potential equivalent to or higher than horses, the only comparative model currently available. These data reinforce the hypothesis that a relatively simple model of body geometry can predict aspects of maximum performance in animals. In this case, it appears that the body geometry of primates is skewed toward avoiding forward pitch in maximal decelerations.

Energy (Im-)Balance in Frugivorous Lemurs in Southern Madagascar: A Preliminary Study in Lemur catta and Eulemur rufifrons × collaris.

The reproductive cycle of several lemur species is synchronized by photoperiodic changes and it is attuned to the seasonal fluctuations in food supply. Nevertheless, irregular periods of food shortage occur in Madagascar, which can result in a negative energy balance and reduced fitness, especially in frugivorous species. Here, we tested whether ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur rufifrons × collaris) use fat stores to maintain their energy balance in a gallery forest of Madagascar (Berenty Reserve). We assessed the energy intake from weight-based estimates of food intake (mouthful count) and macronutrient contents in the diet during dry and wet months. The metabolizable energy ingested by these frugivorous/folivorous species was high during the late wet season, but it was insufficient to meet their energy requirements during the dry season. These preliminary data suggest that these lemurs must store sufficient amount of fat mass during the period of food abundance to meet their maintenance requirements and to cope with the energetic burden of the mating season. Estimates based on models assuming no fiber digestibility during the dry season are consistent with the prediction that brown lemurs should supplement their daytime diet with nighttime feeding in addition to the use of body fat stores.

Maternal reproductive senescence shapes the fitness consequences of the parental age difference in ruffed lemurs.

In humans, pronounced age differences between parents have deleterious fitness consequences. In particular, the number of children is lower when mothers are much older than fathers. However, previous analyses failed to disentangle the influence of differential parental age per se from a direct age effect of each parent. In this study, we analyse the fitness consequences of both parental age and parental age differences on litter size and offspring survival in two closely related species of lemurs living in captivity. As captive lemurs do not choose their reproductive partner, we were able to measure litter size and offspring survival across breeding pairs showing a wide range of parental age differences. However, we demonstrated that the effect of the parental age difference on litter size was fully accounted for by female reproductive senescence because females mating with much younger males were old females. On the other hand, both parental age difference and female reproductive senescence influenced offspring survival. Our results emphasize the importance of teasing apart the effect of parental reproductive senescence when investigating the health and fitness consequences of parental age differences and also provide new insights for conservation programmes of endangered species.

Infant nest and stash sites of variegated lemurs (Varecia rubra): The extended phenotype.

Very few primate species give birth to litters and build nests in which to care for them. Those that do are small-bodied, nocturnal, and solitary. Variegated lemurs are exceptional in that they bear litters in arboreal nests, yet are relatively large-bodied, day-active, and gregarious. Furthermore, they raise their young cooperatively and practice absentee parenting; non-clinging young are transported orally and periodically stashed in arboreal spots that are supportive, sheltered, and usually concealed. Following birth, infant nest and stash trees were mapped, measured, and taxonomically identified in a population of red variegated lemurs in Masoala National Park. About 40 trees were used per litter for nesting and stashing young in adjacent, non-overlapping core areas within the community. These were the largest trees in the forest, even larger than those used for feeding. Furthermore, most occur in valleys and are laced with lianas, creating sites that buffer young from predation, accidental falls, and to some degree, thermal stress. In combination, the number of nest and stash trees used per litter, their characteristics, and their geo-spatial arrangement indicate that such sites are both select and limited in the landscape, exposing the dependence of red variegated lemurs on intact forest canopies for raising non-clinging young within the context of an absentee parenting system. Nest and stash sites are in effect Varecia's extended phenotype. Logging of large trees in Madagascar's eastern rain forests is considered a major factor resulting in local extinctions of variegated lemurs because they rely heavily upon large, mature trees for fruit. However, this study suggests that removal of large trees may more directly precipitate local extinctions by impeding their ability to reproduce. Long-term survival of red variegated lemurs will depend upon efforts to end harmful timber extraction in its remaining stronghold, the Masoala Peninsula.

Evaluating the triplet hypothesis during rhythmic mastication in primates.

Mammalian mastication involves precise jaw movements including transverse movement of the mandible during the power stroke. Jaw elevation and transverse movement are driven by asymmetrical jaw elevator muscle activity, which is thought to include a phylogenetically primitive and conserved triplet motor pattern consisting of: triplet I (balancing side: superficial masseter and medial pterygoid; working side: posterior temporalis), which reaches onset, peak and offset first; and triplet II (working side: superficial masseter and medial pterygoid; balancing side: posterior temporalis), which is active second. Although the presence of a triplet motor pattern has been confirmed in several primate species, the prevalence of this motor pattern - i.e. the proportion of masticatory cycles that display it - has not been evaluated in primates. The present study quantifies the presence and prevalence of the triplet motor pattern in five different primate species, Eulemur fulvus, Propithecus verreauxi, Papio anubis, Macacafuscata and Pan troglodytes, using mean onset, peak and offset time relative to working superficial masseter. In all five of the species studied, the mean triplet motor pattern was observed at peak muscle activation, and in four out of the five species the triplet motor pattern occurred more frequently than expected at random at peak muscle activation and offset. Non-triplet motor patterns were observed in varying proportions at different time points in the masticatory cycle, suggesting that the presence or absence of the triplet motor pattern is not a binomial trait. Instead, the primate masticatory motor pattern is malleable within individual cycles, within individual animals and therefore within species.