A Habitat Stronghold on the Precipice: A call‐to‐action for supporting lemur conservation in northeast Madagascar

The northeast of Madagascar is as diverse as it is threatened. The area bordering the Analanjirofo and SAVA regions contains six protected areas and at least 22 lemur species. Many applied research and conservation programs have been established in the region with the aim of ensuring both wildlife and people thrive in the long term. While most of the remaining humid evergreen forest of northeast Madagascar is formally protected, the local human population depends heavily on the land, and unsustainable natural resource use threatens this biodiversity hotspot. Drawing from our collective experiences managing conservation activities and research programs in northeast Madagascar, we discuss the major threats to the region and advocate for eight conservation activities that help reduce threats and protect the environment, providing specific examples from our own programs. These include (1) empowering local conservation actors, (2) ensuring effectively protected habitat, (3) expanding reforestation, (4) establishing and continuing long-term research and monitoring, (5) reducing food insecurity, (6) supporting environmental education, (7) promoting sustainable livelihoods, and (8) expanding community health initiatives. Lastly, we provide a list of actions that individuals can take to join us in supporting and promoting lemur conservation

Human-Modified Landscapes Driving the Global Primate Extinction crisis

The world\u27s primates have been severely impacted in diverse and profound ways by anthropogenic pressures. Here, we evaluate the impact of various infrastructures and human-modified landscapes on spatial patterns of primate species richness, at both global and regional scales. We overlaid the International Union for the Conservation of Nature (IUCN) range maps of 520 primate species and applied a global 100 km2 grid. We used structural equation modeling and simultaneous autoregressive models to evaluate direct and indirect effects of six human-altered landscapes variables (i.e., human footprint [HFP], croplands [CROP], road density [ROAD], pasture lands [PAST], protected areas [PAs], and Indigenous Peoples\u27 lands [IPLs]) on global primate species richness, threatened and non-threatened species, as well as on species with decreasing and non-decreasing populations. Two-thirds of all primate species are classified as threatened (i.e., Critically Endangered, Endangered, and Vulnerable), with ~86% experiencing population declines, and ~84% impacted by domestic or international trade. We found that the expansion of PAST, HFP, CROP, and road infrastructure had the most direct negative effects on primate richness. In contrast, forested habitat within IPLs and PAs was positively associated in safeguarding primate species diversity globally, with an even stronger effect at the regional level. Our results show that IPLs and PAs play a critical role in primate species conservation, helping to prevent their extinction; in contrast, HFP growth and expansion has a dramatically negative effect on primate species worldwide. Our findings support predictions that the continued negative impact of anthropogenic pressures on natural habitats may lead to a significant decline in global primate species richness, and likely, species extirpations. We advocate for stronger national and international policy frameworks promoting alternative/sustainable livelihoods and reducing persistent anthropogenic pressures to help mitigate the extinction risk of the world\u27s primate species

Ape duos and trios: spontaneous cooperation with free partner choice in chimpanzees

The purpose of the present study was to push the boundaries of cooperation among captive chimpanzees (Pan troglodytes). There has been doubt about the level of cooperation that chimpanzees are able to spontaneously achieve or understand. Would they, without any pre-training or restrictions in partner choice, be able to develop successful joint action? And would they be able to extend cooperation to more than two partners, as they do in nature? Chimpanzees were given a chance to cooperate with multiple partners of their own choosing. All members of the group (N = 11) had simultaneous access to an apparatus that required two (dyadic condition) or three (triadic condition) individuals to pull in a tray baited with food. Without any training, the chimpanzees spontaneously solved the task a total of 3,565 times in both dyadic and triadic combinations. Their success rate and efficiency increased over time, whereas the amount of pulling in the absence of a partner decreased, demonstrating that they had learned the task contingencies. They preferentially approached the apparatus when kin or nonkin of similar rank were present, showing a preference for socially tolerant partners. The forced partner combinations typical of cooperation experiments cannot reveal these abilities, which demonstrate that in the midst of a complex social environment, chimpanzees spontaneously initiate and maintain a high level of cooperative behavior

Climatic, social and reproductive influences on behavioural thermoregulation in a female-dominated lemur

It is well-established that social rank in a large group confers a higher adaptive value to a dominant individual relative to others, though there is scant evidence that members of small social groups either have similar social standing or maintain strict dominance. We aimed to determine whether members of small social groups, using the southern bamboo lemur (Hapalemur meridionalis) as a model, gain rank-related benefits. We first established a dominance hierarchy through a network-based analysis of win-loss interactions, which showed that adult females maintained social dominance within their groups, similar to many strepsirrhine species. To address whether dominant individuals gained rank-related benefits, we then explored how social dynamics may permit access to resting huddles, which provide a physiological benefit. Social thermoregulation, i.e. huddling, is a behavioural energy conservation mechanism, and among many mammals is a direct response to decreasing ambient temperatures. As such, huddling behaviour may have evolved among social animals because of its potential direct and indirect benefits. To examine the effect of dominance rank within small social groups on huddling inclusion, we used generalized linear mixed-effects models to predict the likelihood of huddling to occur during resting bouts from climatic (e.g., temperature, precipitation), social (e.g., affiliation, dominance rank, grooming) and reproductive (e.g., access, infant protection) variables. We found that colder temperatures, especially during shorter resting bouts, increased the likelihood of huddling. Grooming between partners with a high discrepancy in rank increased huddling. Additionally, huddling increased during the reproductive season, potentially offering greater opportunity for males to gain favour with sexually receptive females, and also when new-borns were present, providing essential thermal maintenance and potential anti-predator protection to infants. Taken as a whole, our results suggest that even in small social groups, females gain rank-related benefits by controlling access to huddles, i.e., the intrinsic benefits of social thermoregulation

Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis

Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs

Huddling is more important than rest site selection for thermoregulation in southern bamboo lemurs

Resting site selection can have important effects on the behaviour and fitness of organisms. The maintenance of optimal body temperatures (Tb) when faced with environmental variables has often been attributed to either specific microhabitat rest site characteristics or to behavioural strategies. Among many small group living endotherms, social thermoregulation (i.e., huddling) is utilised as a behavioural energy conservation mechanism at low ambient temperatures (Ta), thus decreasing the metabolic cost of maintaining Tb. Though unusual among primates, lemurs are hypometabolic and exhibit a diversity of thermoregulatory strategies; however, objective Tb measurements have thus far been limited to small-bodied lemurs (e.g., Cheirogaleids). As such, we sought to determine whether a medium-sized lemur model, the southern bamboo lemur (Hapalemur meridionalis), would maintain thermoregulation through microhabitat rest site selection, huddling behaviour, or potentially both strategies. Within a degraded littoral forest fragment in southeast Madagascar, we conducted full-day focal observations on three groups of H. meridionalis between January and December 2013. Adult individuals were collared with data-loggers that collected instantaneous skin temperature Tsk (°C). We calculated the mean Tsk of the focal individual during each resting bout, and the proportional rate of huddling between the focal and conspecifics. In addition, we recorded all resting sites utilised ≥15 min and collected standard tree characteristics. We fitted Linear Mixed-Effects Models to determine the thermoregulatory combined effect of specific resting site characteristics, huddling behaviour, and environmental variables on Tsk. Our results showed that lemurs selected tree sites with larger diameter at breast height; however, huddling was most predictive of increasing Tsk whereas resting site characteristics were not included in the best-fit model. It is possible that microhabitat rest site selection is not significant in a degraded forest as the potential environmental buffering is limited, thus thermoregulatory mechanisms are likely best served by behavioural strategies, i.e., social huddling. Key-words: huddling; skin temperature; Hapalemur meridionalis; energy conservation; thermal ecology; southern bamboo lemur; Madagascar; strepsirrhine

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 (bodymass, 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

Does forest management and researchers’ presence reduce hunting and forest exploitation by local communities in Tsitongambarika, south-east Madagascar?

Hunting of wildlife is one of the major threats to biodiversity. For effective conservation programmes in countries where hunting and shifting agriculture are the main sources of subsistence, forest management should aim to reduce hunting pressure and forest exploitation. The presence of researchers has been promoted as one of the main ways to mitigate anthropogenic pressures on wildlife populations. Our aim was to test whether local management and the establishment of a research station had a role in decreasing forest exploitation by local people living adjacent to a recently protected area in south-east Madagascar. We interviewed local people from nine villages at various distances from the recently established research station of Ampasy, in the northernmost portion of the Tsitongambarika Protected Area, to explore how people use the forest, with a particular focus on hunting. We also performed transect surveys to estimate snare and lemur encounter rates before local forest management began, at the establishment of the research station, and 1 year after. The impact of local communities on the forest seems to have decreased since the beginning of forest management, with a further decrease since the establishment of the research station. Participants from villages not involved in the local management were more reluctant to declare their illegal activities. We conclude that a combination of local management and related activities (e.g. installation of a research station) can assist in temporarily reducing forest exploitation by local communities; however, community needs and conservation plans should be integrated to maintain long-term benefits

High energy or protein concentrations in food as possible offsets for cyanide consumption by specialized bamboo lemurs in Madagascar

Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit

Ecological flexibility as measured by the use of pioneer and exotic plants in two lemurids: Eulemur collaris and Hapalemur meridionalis

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal south-eastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches (i.e., dietary guilds) respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioural observations between 2011 and 2013 on frugivorous collared brown lemurs (Eulemur collaris) and folivorous southern bamboo lemurs (Hapalemur meridionalis). In order to estimate the ability of lemurs to use pioneer species, we categorised all plants used for feeding and resting as either ‘fast-growing’, ‘mid-growing’, or ‘slow-growing’. We fitted linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species (E. collaris and H. meridionalis), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to utilise secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with other primate folivores