Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

Spatial density estimates of Eurasian lynx (Lynx lynx) in the French Jura and Vosges Mountains.

Obtaining estimates of animal population density is a key step in providing sound conservation and management strategies for wildlife. For many large carnivores however, estimating density is difficult because these species are elusive and wide-ranging. Here, we focus on providing the first density estimates of the Eurasian lynx (Lynx lynx) in the French Jura and Vosges mountains. We sampled a total of 413 camera trapping sites (with two cameras per site) between January 2011 and April 2016 in seven study areas across seven counties of the French Jura and Vosges mountains. We obtained 592 lynx detections over 19,035 trap days in the Jura mountains and 0 detection over 6,804 trap days in the Vosges mountains. Based on coat patterns, we identified a total number of 92 unique individuals from photographs, including 16 females, 13 males, and 63 individuals of unknown sex. Using spatial capture-recapture (SCR) models, we estimated abundance in the study areas between 5 (SE = 0.1) and 29 (0.2) lynx and density between 0.24 (SE = 0.02) and 0.91 (SE = 0.03) lynx per 100 km2. We also provide a comparison with nonspatial density estimates and discuss the observed discrepancies. Our study is yet another example of the advantage of combining SCR methods and noninvasive sampling techniques to estimate density for elusive and wide-ranging species, like large carnivores. While the estimated densities in the French Jura mountains are comparable to other lynx populations in Europe, the fact that we detected no lynx in the Vosges mountains is alarming. Connectivity should be encouraged between the French Jura mountains, the Vosges mountains, and the Palatinate Forest in Germany where a reintroduction program is currently ongoing. Our density estimates will help in setting a baseline conservation status for the lynx population in France.

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.

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.

Protected areas in tropical Africa: assessing threats and conservation activities.

Numerous protected areas (PAs) have been created in Africa to safeguard wildlife and other natural resources. However, significant threats from anthropogenic activities and decline of wildlife populations persist, while conservation efforts in most PAs are still minimal. We assessed the impact level of the most common threats to wildlife within PAs in tropical Africa and the relationship of conservation activities with threat impact level. We collated data on 98 PAs with tropical forest cover from 15 countries across West, Central and East Africa. For this, we assembled information about local threats as well as conservation activities from published and unpublished literature, and questionnaires sent to long-term field workers. We constructed general linear models to test the significance of specific conservation activities in relation to the threat impact level. Subsistence and commercial hunting were identified as the most common direct threats to wildlife and found to be most prevalent in West and Central Africa. Agriculture and logging represented the most common indirect threats, and were most prevalent in West Africa. We found that the long-term presence of conservation activities (such as law enforcement, research and tourism) was associated with lower threat impact levels. Our results highlight deficiencies in the management effectiveness of several PAs across tropical Africa, and conclude that PA management should invest more into conservation activities with long-term duration.

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.

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.

Population and group structure of western lowland gorillas (Gorilla gorilla gorilla) at Lokoué, Republic of Congo.

During a 17-month study at the Lokoué clearing in Odzala National Park, Republic of Congo, we identified 377 western lowland gorillas. This population included 31 solitary males, 37 breeding groups, and eight nonbreeding groups. Its age- and sex-class structure was similar to those observed at two other clearings in the same forest block. However, the size of breeding groups varied with site (either clearing or forest sites). At Lokoué, breeding groups (mean size: 8.2 gorillas; range: 3-15) included a single silverback male and, on average, 3.2 adult females. Nonbreeding groups (mean size: 5.5; range: 2-15) were devoid of adult females. Five of the nonbreeding groups were composed predominantly of blackbacks, subadult males, and juveniles, and thus fit the definition of all-male groups previously observed in mountain gorillas. Our study confirms that 1) one-male breeding groups are the norm in western gorillas, and 2) all-male groups occur in this species. Despite frequent changes in members due to migrations of the males, the persistence of these all-male groups indicates that they may play an important role in the life of migrating males. Variations in population structure, and group composition and type among gorilla populations are discussed. However, a further understanding of the evolution of group-living in gorillas requires detailed ecological studies conducted in parallel with studies of the population structure and dynamics of these groups.