Behavioral adjustments of endangered Barbary macaques (Macaca sylvanus) living at the edge of an agricultural landscape in Morocco.

Transition zones between natural and human-altered spaces are eroding in most terrestrial ecosystems. The persistence of animals in shared landscapes depends in part on their behavioral flexibility, which may involve being able to exploit human agricultural production. As a forest-dependent species, the Barbary macaque (Macaca sylvanus) is affected by the progressive conversion of forest-adjacent lands into crops. We explore how Barbary macaque behavior differs between groups living in a forest at the edge of agricultural zones (hereafter "disturbed groups") and groups inhabiting undisturbed forests (hereafter "natural groups"). We compare the diets, activity-budgets, home range sizes, daily path lengths, and sleeping site locations of the groups. We also quantify anthropogenic disturbances (i.e., rates of encounter with humans and dogs) and investigate relationships between such disturbances and the diets and activity budgets of macaques through multiple co-inertia analysis. Disturbed groups included high proportions of cultivated food items in their diet and encountered over 0.5/h anthropogenic disturbances. Activity-budgets differed between disturbed and natural groups and were mostly influenced by diets, not anthropogenic disturbances. Disturbed groups spent more time feeding and less time resting than natural ones. Patterns of space use differed markedly between groups, with disturbed groups displaying smaller home ranges, shorter daily path length, and much higher reutilization of sleeping sites than natural groups. This study highlights the dietary and behavioral flexibility of Barbary macaques living in human-altered environments. Their patterns of space use suggest a reduction in energy expenditure in the disturbed groups due to the inclusion of cultivated food items in their diet possibly leading to increased foraging efficiency. However, the high rates of anthropogenic encounters, including aggressive ones, are likely stressful and may potentially induce extra energy costs and lead to macaque injuries. This could result in demographic costs for crop-foraging groups, threatening the conservation of this endangered species.

The genetic impact of an Ebola outbreak on a wild gorilla population.

BACKGROUND: Numerous Ebola virus outbreaks have occurred in Equatorial Africa over the past decades. Besides human fatalities, gorillas and chimpanzees have also succumbed to the fatal virus. The 2004 outbreak at the Odzala-Kokoua National Park (Republic of Congo) alone caused a severe decline in the resident western lowland gorilla (Gorilla gorilla gorilla) population, with a 95% mortality rate. Here, we explore the immediate genetic impact of the Ebola outbreak in the western lowland gorilla population. RESULTS: Associations with survivorship were evaluated by utilizing DNA obtained from fecal samples from 16 gorilla individuals declared missing after the outbreak (non-survivors) and 15 individuals observed before and after the epidemic (survivors). We used a target enrichment approach to capture the sequences of 123 genes previously associated with immunology and Ebola virus resistance and additionally analyzed the gut microbiome which could influence the survival after an infection. Our results indicate no changes in the population genetic diversity before and after the Ebola outbreak, and no significant differences in microbial community composition between survivors and non-survivors. However, and despite the low power for an association analysis, we do detect six nominally significant missense mutations in four genes that might be candidate variants associated with an increased chance of survival. CONCLUSION: This study offers the first insight to the genetics of a wild great ape population before and after an Ebola outbreak using target capture experiments from fecal samples, and presents a list of candidate loci that may have facilitated their survival.

Transdisciplinary Bioblitz: Rapid biotic and abiotic inventory allows studying environmental changes over 60 years at the Biological Field Station of Paimpont (Brittany, France) and opens new interdisciplinary research opportunities.

BACKGROUND: The Biological Field Station of Paimpont (Station Biologique de Paimpont, SBP), owned by the University of Rennes and located in the Brocéliande Forest of Brittany (France), has been hosting student scientific research and field trips during the last 60 years. The study area of the SBP is a landscape mosaic of 17 ha composed of gorse moors, forests, prairies, ponds and creeks. Land use has evolved over time. Historical surveys by students and researchers focused on insects and birds. With this study, we aimed to increase the range of taxa observations, document changes in species composition and landscape and provide a basis for interdisciplinary research perspectives. We gathered historical data, implemented an all-taxon biodiversity inventory (ATBI) in different habitats of the SBP study area, measured abiotic factors in the air, water and soil and performed a photographical landscape observation during the BioBlitz held in July 2017. NEW INFORMATION: During the 24 h BioBlitz, organised by the SBP and the EcoBio lab from the University of Rennes and the French National Center of Scientific Research (CNRS), different habitats were individually sampled. Seventy-seven experts, accompanied by 120 citizens and 12 young people participating in the European Volunteer Service, observed, identified and databased 660 species covering 5 kingdoms, 8 phyla, 21 classes, 90 orders and 247 families. In total, there were 1819 occurrences including records identified to higher taxon ranks, thereby adding one more kingdom and four more phyla. Historical data collection resulted in 1176 species and 4270 occurrences databased. We also recorded 13 climatic parameters, 10 soil parameters and 18 water parameters during the BioBlitz. Current habitats were mapped and socio-ecological landscape changes were assessed with a diachronic approach using 32 historical photographs and historical maps. The coupling of historical biodiversity data with new biotic and abiotic data and a photographic comparison of landscape changes allows an integrative understanding of how the SBP changed from agriculturally-used land to a managed natural area within the last 60 years. Hence, this BioBlitz represents an important holistic sampling of biodiversity for studies on trophic webs or on trophic interactions or on very diverse, but connected, habitats. The integration of social, biotic and abiotic data opens innovative research opportunities on the evolution of socio-ecosystems and landscapes.

Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females.

Social dispersal is an important feature of population dynamics. When female mammals occur in polygynous groups, their dispersal decisions are conditioned by various female-, male-, and group-related factors. Among them, the influence of disease often remains difficult to assess. To address this challenge, we used long-term monitoring data from two gorilla populations (Gorilla gorilla gorilla) affected by infectious skin disease lesions. After controlling for other potentially influential factors, we investigated to which extent disease avoidance drives the dispersal decisions of gorilla females. We showed that the infection of a silverback of a breeding group by the skin disease increased the probability of adult females to emigrate. Moreover, adult females avoided breeding groups with a high prevalence of skin disease by emigrating from them and immigrating into healthier ones. Age of the breeding group was also an important factor. Adult females left older groups, near the end of a male tenure, to join younger ones led by younger fully grown silverbacks that could be of high reproductive and protective value. Our study highlights that, although females select for high-quality males, disease avoidance is a critical driver of their dispersion decision.

From groups to communities in western lowland gorillas.

Social networks are the result of interactions between individuals at different temporal scales. Thus, sporadic intergroup encounters and individual forays play a central role in defining the dynamics of populations in social species. We assessed the rate of intergroup encounters for three western lowland gorilla ( Gorilla gorilla gorilla) groups with daily observations over 5 years, and non-invasively genotyped a larger population over four months. Both approaches revealed a social system much more dynamic than anticipated, with non-aggressive intergroup encounters that involved social play by immature individuals, exchanges of members between groups likely modulated by kinship, and absence of infanticide evidenced by infants not fathered by the silverback of the group where they were found. This resulted in a community composed of groups that interacted frequently and not-aggressively, contrasting with the more fragmented and aggressive mountain gorilla ( G. beringei beringei) societies. Such extended sociality can promote the sharing of behavioural and cultural traits, but might also increase the susceptibility of western lowland gorillas to infectious diseases that have decimated their populations in recent times.

Role of Calcium Signaling in GA101-Induced Cell Death in Malignant Human B Cells.

GA101/obinutuzumab is a novel type II anti-CD20 monoclonal antibody (mAb), which is more effective than rituximab (RTX) in preclinical and clinical studies when used in combination with chemotherapy. Ca2+ signaling was shown to play a role in RTX-induced cell death. This report concerns the effect of GA101 on Ca2+ signaling and its involvement in the direct cell death induced by GA101. We reveal that GA101 triggered an intracellular Ca2+ increase by mobilizing intracellular Ca2+ stores and activating Orai1-dependent Ca2+ influx in non-Hodgkin lymphoma cell lines and primary B-Cell Chronic Lymphocytic Leukemia (B-CLL) cells. According to the cell type, Ca2+ was mobilized from two distinct intracellular compartments. In Raji, BL2, and B-CLL cells, GA101 induced a Ca2+ release from lysosomes, leading to the subsequent lysosomal membrane permeabilization and cell death. Inhibition of this calcium signaling reduced GA101-induced cell death in these cells. In SU-DHL-4 cells, GA101 mobilized Ca2+ from the endoplasmic reticulum (ER). Inhibition of ER replenishment, by blocking Orai1-dependent Ca2+ influx, led to an ER stress and unfolded protein response (UPR) which sensitized these cells to GA101-induced cell death. These results revealed the central role of Ca2+ signaling in GA101's action mechanism, which may contribute to designing new rational drug combinations improving its clinical efficacy.

Using demographic characteristics of populations to detect spatial fragmentation following suspected ebola outbreaks in great apes.

OBJECTIVES: Demographic crashes due to emerging diseases can contribute to population fragmentation and increase extinction risk of small populations. Ebola outbreaks in 2002-2004 are suspected to have caused a decline of more than 80% in some Western lowland gorilla (Gorilla gorilla gorilla) populations. We investigated whether demographic indicators of this event allowed for the detection of spatial fragmentation in gorilla populations. MATERIALS AND METHODS: We collected demographic data from two neighbouring populations: the Lokoué population, suspected to have been affected by an Ebola outbreak (followed from 2001 to 2014), and the Romani population, of unknown demographic status before Ebola outbreaks (followed from 2005 to 2014). RESULTS: Ten years after the outbreak, the Lokoué population is slowly recovering and the short-term demographic indicators of a population crash were no longer detectable. The Lokoué population has not experienced any additional demographic perturbation over the past decade. The Romani population did not show any of the demographic indicators of a population crash over the past decade. Its demographic structure remained similar to that of unaffected populations. DISCUSSION: Our results highlighted that the Ebola disease could contribute to fragmentation of gorilla populations due to the spatially heterogeneous impact of its outbreaks. The demographic structure of populations (i.e., age-sex and group structure) can be useful indicators of a possible occurrence of recent Ebola outbreaks in populations without known history, and may be more broadly used in other emerging disease/species systems. Longitudinal data are critical to our understanding of the impact of emerging diseases on wild populations and their conservation.

Is diet flexibility an adaptive life trait for relictual and peri-urban populations of the endangered primate Macaca sylvanus?

Habitat loss, fragmentation and urban expansion may drive some species to marginal habitats while others succeed in exploiting urban areas. Species that show dietary flexibility are more able to take advantage of human activities to supplement their diet with anthropogenically abundant and accessible resources. The Barbary macaque (Macaca sylvanus) is an endangered species due to the loss of its habitat, and human pressure. The population of Gouraya National Park (Algeria) lives in a relictual habitat that constitutes about 0.6% of the species range. In addition, this population is a unique case where urban expansion favours contact zones between Barbary macaque habitats and a big city (Bejaia). We quantified the dietary composition of Gouraya macaques over an annual cycle with the objective to understand how diet flexibility of this species may help it adapt to a relictual habitat or cope with urban expansion. We recorded the phenology of plant species every month. This study shows that Gouraya macaques, compared to those living in other forest types of the distribution area, are under lower seasonal constraints. They consume a greater amount of fruit and seeds that are available throughout much of the year, and a lesser amount of costly to find and extract subterranean foods. Therefore the Gouraya relictual habitat appears as a favourable environment compared to other major habitats of that species. This study also shows that colonizing peri-urban zones increases the availability and species richness of diet resources for Barbary macaques as they consume more human foods and exotic plants than in farther sites. Adult males eat more human foods than adult females and immatures do. The exploitation of high-energy anthropogenic food could favour macaque population growth and expansion towards the city center associated with human/macaque conflicts. We recommend applying management actions to restore macaques back to their natural habitat.

How Ebola impacts social dynamics in gorillas: a multistate modelling approach.

Emerging infectious diseases can induce rapid changes in population dynamics and threaten population persistence. In socially structured populations, the transfers of individuals between social units, for example, from breeding groups to non-breeding groups, shape population dynamics. We suggest that diseases may affect these crucial transfers. We aimed to determine how disturbance by an emerging disease affects demographic rates of gorillas, especially transfer rates within populations and immigration rates into populations. We compared social dynamics and key demographic parameters in a gorilla population affected by Ebola using a long-term observation data set including pre-, during and post-outbreak periods. We also studied a population of undetermined epidemiological status in order to assess whether this population was affected by the disease. We developed a multistate model that can handle transition between social units while optimizing the number of states. During the Ebola outbreak, social dynamics displayed increased transfers from a breeding to a non-breeding status for both males and females. Six years after the outbreak, demographic and most of social dynamics parameters had returned to their initial rates, suggesting a certain resilience in the response to disruption. The formation of breeding groups increased just after Ebola, indicating that environmental conditions were still attractive. However, population recovery was likely delayed because compensatory immigration was probably impeded by the potential impact of Ebola in the surrounding areas. The population of undetermined epidemiological status behaved similarly to the other population before Ebola. Our results highlight the need to integrate social dynamics in host-population demographic models to better understand the role of social structure in the sensitivity and the response to disease disturbances.

Effect of habitat quality on diet flexibility in Barbary macaques.

Barbary macaques live in extreme temperate environments characterized by strongly seasonal resource availability. They are mainly terrestrial while foraging, harvesting food from the herbaceous layer. These monkeys are threatened mainly because of anthropogenic habitat degradation. We studied the adaptive capacities of wild groups of Barbary macaques that lived in different cedar forests undergoing varying extents of grazing pressure from domestic livestock. In all three sites, diet varied seasonally. Heavy grazing led to a significant decrease in herbaceous production and species richness. As a consequence, the monkeys' diet in this poor habitat showed a decreased plant species richness. Moreover, it incorporated fewer above-ground herbaceous resources, and a greater proportion of subterranean resources (especially hypogeous fungi and subterranean invertebrates such as earthworms, eggs and adults of earwigs, and ant's larvae) than the diet of monkeys inhabiting ungrazed forest. Cedar bark, cedar strobiles, earthworms, and earwigs were part of the monkeys' diet only in grazed forest. Monkeys in heavily grazed forest compensated for a lack of herbaceous foods by eating subterranean foods preferentially to tree and shrub products. The foods they consumed take longer to harvest and process than the seeds or leaves consumed by Barbary macaques in less heavily grazed forest habitats. Our results suggest that monkeys do differ in their diets according to the degree of habitat change induced by human activities. They also highlight the dietary flexibility of Barbary macaques as a key element that allows them to cope with degraded habitats. We later compare the dietary adjustments of Barbary macaques facing environmental change to dietary strategies of other macaques and temperate-zone primates.

Effect of habitat quality on the ecological behaviour of a temperate-living primate: time-budget adjustments.

Barbary macaques, like other non-human primates living in highly seasonal temperate environments, display high monthly variations in their diet. In addition, their diet changes according to the habitat type they colonize and to the degree of habitat degradation due to resource exploitation by local people, in particular through pastoralism. We studied the time-budget adjustments of wild Barbary macaques in three cedar-oak forests impacted by different intensities of grazing pressure from goats and sheep. We examined how diet variations influenced the time monkeys spent in their activities and their day range lengths (i.e. their energy costs). At three studied sites, diet composition and time budgets showed marked seasonal variations. Diet composition had a strong influence on monkeys' time budget. In the forest where pastoralism was the highest, diet included a greater proportion of underground resources, shrub fruit and acorns, which led to an increase in the time spent foraging and moving, as well as an important increase in day range lengths. Energy costs were therefore higher in a degraded environment than in a suitable habitat. The monkeys living in forests subjected to pastoralism took advantage of increased day lengths to spend more time searching for food. However, in the forest with the highest pastoralism pressure, although monkeys spent more time foraging, they spent less time feeding than monkeys at the other sites. In addition, they appeared to have reached the limits of the available time they could devote to these activities, as their diurnal resting time was at its lowest level over several months. Temperature variations did not appear to modify monkeys' time budgets. In the least favourable habitat, saving time from resting activity allowed monkeys to maintain a relatively high level of social activity, partly linked to rearing constraints.

Recovery potential of a western lowland gorilla population following a major Ebola outbreak: results from a ten year study.

Investigating the recovery capacity of wildlife populations following demographic crashes is of great interest to ecologists and conservationists. Opportunities to study these aspects are rare due to the difficulty of monitoring populations both before and after a demographic crash. Ebola outbreaks in central Africa have killed up to 95% of the individuals in affected western lowland gorilla (Gorilla gorilla gorilla) populations. Assessing whether and how fast affected populations recover is essential for the conservation of this critically endangered taxon. The gorilla population visiting Lokoué forest clearing, Odzala-Kokoua National Park, Republic of the Congo, has been monitored before, two years after and six years after Ebola affected it in 2004. This allowed us to describe Ebola's short-term and long-term impacts on the structure of the population. The size of the population, which included around 380 gorillas before the Ebola outbreak, dropped to less than 40 individuals after the outbreak. It then remained stable for six years after the outbreak. However, the demographic structure of this small population has significantly changed. Although several solitary males have disappeared, the immigration of adult females, the formation of new breeding groups, and several birth events suggest that the population is showing potential to recover. During the outbreak, surviving adult and subadult females joined old solitary silverbacks. Those females were subsequently observed joining young silverbacks, forming new breeding groups where they later gave birth. Interestingly, some females were observed joining silverbacks that were unlikely to have sired their infant, but no infanticide was observed. The consequences of the Ebola outbreak on the population structure were different two years and six years after the outbreak. Therefore, our results could be used as demographic indicators to detect and date outbreaks that have happened in other, non-monitored gorilla populations.

Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques.

Habitat, diet and leaf chemistry are compared between Japanese and Barbary macaques to reveal the similarities and differences in dietary adaptations of temperate primates living at the eastern and western extremes of the genus Macaca. Tree species diversity and proportion of fleshy-fruited species are much higher in Japan than in North Africa. Both species spend considerable annual feeding time on leaves. Japanese macaques prefer fruits and seeds over leaves, and Barbary macaques prefer seeds. These characteristics are adaptive in temperate regions where fruit availability varies considerably with season, since animals can survive during the lean period by relying on leaf and other vegetative foods. The two species are different with respect to the higher consumption of herbs by Barbary macaques, and the leaves consumed contain high condensed and hydrolysable tannin for Barbary but not for Japanese macaques. Barbary macaques supplement less diverse tree foods with herbs. Because of the low species diversity and high tannin content of the dominant tree species, Barbary macaques may have developed the capacity to cope with tannin. This supports the idea that digestion of leaves is indispensable to survive in temperate regions where fruit and seed foods are not available for a prolonged period during each year.

How Ebola impacts genetics of Western lowland gorilla populations.

BACKGROUND: Emerging infectious diseases in wildlife are major threats for both human health and biodiversity conservation. Infectious diseases can have serious consequences for the genetic diversity of populations, which could enhance the species' extinction probability. The Ebola epizootic in western and central Africa induced more than 90% mortality in Western lowland gorilla population. Although mortality rates are very high, the impacts of Ebola on genetic diversity of Western lowland gorilla have never been assessed. METHODOLOGY/PRINCIPAL FINDINGS: We carried out long term studies of three populations of Western lowland gorilla in the Republic of the Congo (Odzala-Kokoua National Park, Lossi gorilla sanctuary both affected by Ebola and Lossi's periphery not affected). Using 17 microsatellite loci, we compared genetic diversity and structure of the populations and estimate their effective size before and after Ebola outbreaks. Despite the effective size decline in both populations, we did not detect loss in genetic diversity after the epizootic. We revealed temporal changes in allele frequencies in the smallest population. CONCLUSIONS/SIGNIFICANCE: Immigration and short time elapsed since outbreaks could explain the conservation of genetic diversity after the demographic crash. Temporal changes in allele frequencies could not be explained by genetic drift or random sampling. Immigration from genetically differentiated populations and a non random mortality induced by Ebola, i.e., selective pressure and cost of sociality, are alternative hypotheses. Understanding the influence of Ebola on gorilla genetic dynamics is of paramount importance for human health, primate evolution and conservation biology.

Influence of male morphology on male mating status and behavior during interunit encounters in western lowland gorillas.

The western lowland gorilla (Gorilla gorilla gorilla) is one of the most sexually dimorphic primate species. Mature males are twice the size of females and have grey fur on their backs and a fibrous, adipose crest on their heads. Such traits are likely to have evolved by sexual selection, either because they confer advantages during male-male fights or because females prefer males with more dimorphic traits. We developed photogrammetric methods for distance collection of morphological data from silverback males frequenting the Lokoué forest clearing in Odzala-Kokoua National Park, Republic of the Congo. Body length, head-crest size, musculature development, and extent of the grey color on the back were assessed in 87 nonbreeding and breeding mature males. Behavioral data were also collected during 312 male-male encounters involving 67 mature males in order to estimate their level of aggressiveness. The number of females belonging to a mature male positively correlated with the male crest size, body length, and musculature. Whereas morphological variables did not significantly affect the intensity of male-male encounters, the number of females attending male-male encounters strongly affected the number of agonistic displays by the two males. We discuss the mechanisms through which males with more exaggerated traits could obtain a mating advantage, namely male-male fights or female mate choice.

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla).

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.

Yaws disease in a wild gorilla population and its impact on the reproductive status of males.

We evaluated the prevalence of skin lesions in a gorilla population in the Republic of Congo. The observed lesions were typical of yaws, a treponematosis described in gorillas and humans living in tropical regions. Among the 377 gorillas identified, 17% presented skin lesions, mainly on their faces. The worst cases presented physical handicaps because of the deep lesions. As in humans, lesions break out when individuals are young. Lesions were more prevalent among males than females above 8 years old. This sex-bias prevalence could result from the behavioral characteristics of males through a greater exposure to wounds. Lesions were also more prevalent in unmated adult males (either solitaries or those living in nonbreeding groups) than in males leading breeding groups. In the case of the latter, nonaffected and affected leading males had a similar number of infants and juveniles. Still, none of the leading males ever presented serious handicaps because of the skin lesions. This suggests that adult females could favor males without lesions. Finally, lesions were more prevalent among immature animals in nonbreeding groups than in breeding groups, suggesting that either young animals with lesions disperse earlier from their natal groups, or that the disease spreads faster in nonbreeding groups. Our results provide some insights into the spread of a disease in a wild population. Further studies are required to determine if the vigor of males affects the development of the disease and if affected individuals experience social discrimination inducing a negative impact on population dynamics.

Living in nonbreeding groups: an alternative strategy for maturing gorillas.

The one-male reproductive strategy implies that maturing males are temporarily excluded from reproduction. In gorillas, these excluded males live either solitarily or in nonbreeding groups (NBGs) that are devoid of adult females. The dynamics of NBGs are not well known. In this study, which was conducted on a gorilla population (Gorilla gorilla gorilla) of 377 individuals that visited the Lokoué clearing in the Republic of Congo, we detail how the NBGs formed, and analyze their dynamics according to age-sex classes, the relatedness of members, and the origin and destination of transferring individuals. We discuss the potential benefits gained by individuals living in these groups. The NBGs included mainly immature males, most of which appeared to have migrated voluntarily from their natal groups. Some individuals (including juvenile females) came from disbanded breeding groups (BGs). Migrants preferentially joined NBGs that included a silverback male. Their dispersal patterns were not determined by their degree of relatedness, but they tended to associate with related silverbacks. In this way, the migrants could enhance their protection against predators and gain experience with different environmental conditions. By tolerating and protecting offspring, aging silverbacks could enhance their inclusive fitness. Finally, young and healthy silverbacks could increase their likelihood of forming a future BG when unrelated females joined them.