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.

Training in the Dark: Using Target Training for Non-Invasive Application and Validation of Accelerometer Devices for an Endangered Primate (Nycticebus bengalensis).

Accelerometers offer unique opportunities to study the behaviour of cryptic animals but require validation to show their accuracy in identifying behaviours. This validation is often undertaken in captivity before use in the wild. While zoos provide important opportunities for trial field techniques, they must consider the welfare and health of the individuals in their care and researchers must opt for the least invasive techniques. We used positive reinforcement training to attach and detach a collar with an accelerometer to an individual Bengal slow loris (Nycticebus bengalensis) at the Shaldon Wildlife Trust, U.K. This allowed us to collect accelerometer data at different periods between January-June 2020 and January-February 2021, totalling 42 h of data with corresponding video for validation. Of these data, we selected 54 min where ten behaviours were present and ran a random forest model. We needed 39 15-min sessions to train the animal to wear/remove the collar. The accelerometer data had an accuracy of 80.7 ± SD 9.9% in predicting the behaviours, with 99.8% accuracy in predicting resting, and a lower accuracy (but still >75% for all of them apart from suspensory walk) for the different types of locomotion and feeding behaviours. This training and validation technique can be used in similar species and shows the importance of working with zoos for in situ conservation (e.g., validation of field techniques).

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.

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.

Low Levels of Fruit Nitrogen as Drivers for the Evolution of Madagascar's Primate Communities.

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Habitat degradation and seasonality affect physiological stress levels of Eulemur collaris in littoral forest fragments.

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.