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.

Which temporal resolution to consider when investigating the impact of climatic data on population dynamics? The case of the lesser horseshoe bat (Rhinolophus hipposideros).

Climatic variables are often considered when studying environmental impacts on population dynamics of terrestrial species. However, the temporal resolution considered varies depending on studies, even among studies of the same taxa. Most studies interested in climatic impacts on populations tend to average climatic data across timeframes covering life cycle periods of the organism in question or longer, even though most climatic databases provide at least a monthly resolution. We explored the impact of climatic variables on lesser horseshoe bat (Rhinolophus hipposideros) demography based on count data collected at 94 maternity colonies from 2000 to 2014 in Britanny, France. Meteorological data were considered using different time resolutions (month, life cycle period and year) to investigate their adequacy. Model averaging was used to detect significant predictors for each temporal resolution. Our results show that the finest temporal resolution, e.g. month, was more informative than coarser ones. Precipitation predictors were particularly decisive, with a negative impact on colony sizes when rainfall occurred in October, and a positive impact for June precipitations. Fecundity was influenced by April weather. This highlights the strong impact of climatic conditions during crucial but short time periods on the population dynamics of bats. We demonstrate the importance of choosing an appropriate time resolution and suggest that analogous studies should consider fine-scale temporal resolution (e.g. month) to better grasp the relationship between population dynamics and climatic conditions.

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.

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.

Post-release dispersal in animal translocations: social attraction and the "vacuum effect".

Animal translocations are human-induced colonizations that can represent opportunities to contribute to the knowledge on the behavioral and demographic processes involved in the establishment of animal populations. Habitat selection behaviors, such as social cueing, have strong implications on dispersal and affect the establishment success of translocations. Using modeling simulations with a two-population network model (a translocated population and a remnant population), we investigated the consequences of four habitat selection strategies on post-translocation establishment probabilities in short- and long-lived species. Two dispersal strategies using social cues (conspecific attraction and habitat copying) were compared to random and quality-based strategies. We measured the sensitivity of local extinctions to dispersal strategies, life cycles, release frequencies, remnant population and release group sizes, the proportion of breeders and the connectivity between populations. Our results indicate that social behaviors can compromise establishment as a result of post-release dispersal, particularly in long-lived species. This behavioral mechanism, the "vacuum effect", arises from increased emigration in populations that are small relative to neighboring populations, reducing their rate of population growth. The vacuum effect can drive small remnant populations to extinction when a translocated group is large. In addition, the magnitude of the vacuum effect varies non-linearly with connectivity. The vacuum effect represents a novel form of the behaviorally mediated Allee effect that can cause unexpected establishment failures or population extinctions in response to social cueing. Accounting for establishment probabilities as a conditional step to the persistence of populations would improve the accuracy of predicting the fates of translocated or natural (meta)populations.

Long-term trends in survival of a declining population: the case of the little owl (Athene noctua) in the Netherlands.

The little owl (Athene noctua) has declined significantly in many parts of Europe, including the Netherlands. To understand the demographic mechanisms underlying their decline, we analysed all available Dutch little owl ringing data. The data set spanned 35 years, and included more than 24,000 ringed owls, allowing detailed estimation of survival rates through multi-state capture-recapture modelling taking dispersal into account. We investigated geographical and temporal variation in age-specific survival rates and linked annual survival estimates to population growth rate in corresponding years, as well as to environmental covariates. The best model for estimating survival assumed time effects on both juvenile and adult survival rates, with average annual survival estimated at 0.258 (SE = 0.047) and 0.753 (SE = 0.019), respectively. Juvenile survival rates decreased with time whereas adult survival rates fluctuated regularly among years, low survival occurring about every 4 years. Years when the population declined were associated with low juvenile survival. More than 60% of the variation in juvenile survival was explained by the increase in road traffic intensity or in average temperature in spring, but these correlations rather reflect a gradual decrease in juvenile survival coinciding with long-term global change than direct causal effects. Surprisingly, vole dynamics did not explain the cyclic dynamics of adult survival rate. Instead, dry and cold years led to low adult survival rates. Low juvenile survival rates, that limit recruitment of first-year breeders, and the regular occurrence of years with poor adult survival, were the most important determinants of the population decline of the little owl.

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.

Roles of survival and dispersal in reintroduction success of Griffon vulture (Gyps fulvus).

The success of reintroduction programs greatly depends on the amount of mortality and dispersal of the released individuals. Although local environmental pressures are likely to play an important role in these processes, they have rarely been investigated because of the lack of spatial replicates of reintroduction. In the present study, we analyzed a 25-year data set encompassing 272 individuals released in five reintroduction programs of Griffon Vultures (Gyps fulvus) in France to examine the respective roles of survival and dispersal in program successes and failures. We use recent developments in multi-strata capture-recapture models to take into account tag loss in survival estimates and to consider and estimate dispersal among release areas. We also examined the effects of sex, age, time, area, and release status on survival, and we tested whether dispersal patterns among release areas were consistent with habitat selection theories. Results indicated that the survival of released adults was reduced during the first year after release, with no difference between sexes. Taking into account local observations only, we found that early survival rates varied across sites. However when we distinguished dispersal from mortality, early survival rates became equal across release sites. It thus appears that among reintroduction programs difference in failure and success was due to differential dispersal among release sites. We revealed asymmetrical patterns of dispersal due to conspecific attraction: dispersers selected the closest and the largest population. We showed that mortality can be homogeneous from one program to another while, on the contrary, dispersal is highly dependent on the matrix of established populations. Dispersal behavior is thus of major interest for metapopulation restoration and should be taken into account in planning reintroduction designs.