The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest.

To understand the evolutionary histories and conservation potential of wild animal species it is useful to assess whether taxa are genetically structured into different populations and identify the underlying factors responsible for any clustering. Landscape features such as rivers may influence genetic population structure, and analysis of structure by sex can further reveal effects of sex-specific dispersal. Using microsatellite genotypes obtained from noninvasively collected fecal samples we investigated the population structure of 261 western lowland gorillas (WLGs) (Gorilla gorilla gorilla) from seven locations spanning an approximately 37,000 km(2) region of mainly continuous rain forest within Central African Republic (CAR), Republic of Congo and Cameroon. We found our sample to consist of two or three significantly differentiated clusters. The boundaries of the clusters coincided with courses of major rivers. Moreover, geographic distance detoured around rivers better-explained variation in genetic distance than straight line distance. Together these results suggest that major rivers in our study area play an important role in directing WLG gene flow. The number of clusters did not change when males and females were analyzed separately, indicating a lack of greater philopatry in WLG females than males at this scale.

Comparative life history patterns of female gorillas.

OBJECTIVES: Several theories have been proposed to explain the impact of ecological conditions on differences in life history variables within and between species. Here we compare female life history parameters of one western lowland gorilla population (Gorilla gorilla gorilla) and two mountain gorilla populations (Gorilla beringei beringei). MATERIALS AND METHODS: We compared the age of natal dispersal, age of first birth, interbirth interval, and birth rates using long-term demographic datasets from Mbeli Bai (western gorillas), Bwindi Impenetrable National Park and the Virunga Massif (mountain gorillas). RESULTS: The Mbeli western gorillas had the latest age at first birth, longest interbirth interval, and slowest surviving birth rate compared to the Virunga mountain gorillas. Bwindi mountain gorillas were intermediate in their life history patterns. DISCUSSION: These patterns are consistent with differences in feeding ecology across sites. However, it is not possible to determine the evolutionary mechanisms responsible for these differences, whether a consequence of genetic adaptation to fluctuating food supplies ("ecological risk aversion hypothesis") or phenotypic plasticity in response to the abundance of food ("energy balance hypothesis"). Our results do not seem consistent with the extrinsic mortality risks at each site, but current conditions for mountain gorillas are unlikely to match their evolutionary history. Not all traits fell along the expected fast-slow continuum, which illustrates that they can vary independently from each other ("modularity model"). Thus, the life history traits of each gorilla population may reflect a complex interplay of multiple ecological influences that are operating through both genetic adaptations and phenotypic plasticity.

Population dynamics of western gorillas at Mbeli Bai.

Long-term studies of population dynamics can provide insights into life history theory, population ecology, socioecology, conservation biology and wildlife management. Here we examine 25 years of population dynamics of western gorillas at Mbeli Bai, a swampy forest clearing in Nouabalé-Ndoki National Park, the Republic of Congo. The Mbeli population more than doubled from 101 to 226 gorillas during the study. After adjusting for a net influx of gorillas into the study population, the increase represents an inherent growth rate of 0.7% per year, with 95% confidence limits between -0.7% and 2.6%. The influx of gorillas mainly involved immigration of individuals into existing study groups (social dispersal), but it also included the appearance of a few previously unknown groups (locational dispersal). The average group size did not change significantly during the study, which is consistent with the possibility that western gorillas face socioecological constraints on group size, even when the population is increasing. We found no significant evidence of density dependence on female reproductive success or male mating competition. The distribution of gorillas among age/sex categories also did not change significantly, which suggests that the population had a stable age structure. Our results provide evidence of population stability or growth for some western gorillas (albeit within a small area). The results highlight the value of law enforcement, long-term monitoring, and protected areas; but they do not diminish the importance of improving conservation for this critically endangered species.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Physical maturation, life-history classes and age estimates of free-ranging western gorillas--insights from Mbeli Bai, Republic of Congo.

Physical maturation and life-history parameters are seen as evolutionary adaptations to different ecological and social conditions. Comparison of life-history patterns of closely related species living in diverse environments helps to evaluate the validity of these assumptions but empirical data are lacking. The two gorilla species exhibit substantial differences in their environment, which allows investigation into the role of increased frugivory in shaping western gorilla life histories. We present behavioral and morphological data on western gorilla physical maturation and life-history parameters from a 12.5-year study at Mbeli Bai, a forest clearing in the Nouabalé-Ndoki National Park in northern Congo. We assign photographs of known individuals to different life-history classes and propose new age boundaries for life-history classes in western gorillas, which can be used and tested at other western gorilla research sites. Our results show that western gorillas are weaned at a later age compared with mountain gorillas and indicate slower physical maturation of immatures. These findings support the risk-aversion hypothesis for more frugivorous species. However, our methods need to be applied and tested with other gorilla populations. The slow life histories of western gorillas could have major consequences for social structure, mortality patterns and population growth rates that will affect recovery from population crashes of this critically endangered species. We emphasize that long-term studies can provide crucial demographic and life-history data that improve our understanding of life-history evolution and adaptation and help to refine conservation strategies.

Guns, germs, and trees determine density and distribution of gorillas and chimpanzees in Western Equatorial Africa.

We present a range-wide assessment of sympatric western lowland gorillas Gorilla gorilla gorilla and central chimpanzees Pan troglodytes troglodytes using the largest survey data set ever assembled for these taxa: 59 sites in five countries surveyed between 2003 and 2013, totaling 61,000 person-days of fieldwork. We used spatial modeling to investigate major drivers of great ape distribution and population trends. We predicted density across each taxon's geographic range, allowing us to estimate overall abundance: 361,900 gorillas and 128,700 chimpanzees in Western Equatorial Africa-substantially higher than previous estimates. These two subspecies represent close to 99% of all gorillas and one-third of all chimpanzees. Annual population decline of gorillas was estimated at 2.7%, maintaining them as Critically Endangered on the International Union for Conservation of Nature and Natural Resources (IUCN) Red List. We quantified the threats to each taxon, of which the three greatest were poaching, disease, and habitat degradation. Gorillas and chimpanzees are found at higher densities where forest is intact, wildlife laws are enforced, human influence is low, and disease impacts have been low. Strategic use of the results of these analyses could conserve the majority of gorillas and chimpanzees. With around 80% of both subspecies occurring outside protected areas, their conservation requires reinforcement of anti-poaching efforts both inside and outside protected areas (particularly where habitat quality is high and human impact is low), diligent disease control measures (including training, advocacy, and research into Ebola virus disease), and the preservation of high-quality habitat through integrated land-use planning and implementation of best practices by the extractive and agricultural industries.

Mothers may shape the variations in social organization among gorillas.

When mothers continue to support their offspring beyond infancy, they can influence the fitness of those offspring, the strength of social relationships within their groups, and the life-history traits of their species. Using up to 30 years of demographic data from 58 groups of gorillas in two study sites, this study extends such findings by showing that mothers may also contribute to differences in social organization between closely related species. Female mountain gorillas remained with their sons for significantly longer than western gorillas, which may explain why male philopatry and multimale groups are more common among mountain gorillas. The presence of the putative father and other familiar males did not vary significantly between species, and we found only limited support for the socio-ecological theory that the distribution of adult males is influenced by the distribution of females. Within each gorilla species, variations in those distributions may also reflect the different stages in the typical life cycle of a group. Collectively, our results highlight the potentially far-reaching consequences of maternal support that extends beyond infancy, and they illustrate the opportunity to incorporate additional factors into phylogenetic analyses of variations in social organization, including studies of human evolution.

Indicators of success for smart law enforcement in protected areas: A case study for Russian Amur tiger (Panthera tigris altaica) reserves.

Although considerable conservation resources have been committed to develop and use law enforcement monitoring and management tools such as SMART, measures of success are ill-defined and, to date, few reports detail results post-implementation. Here, we present 4 case studies from protected areas with Amur tigers (Panthera tigris altaica) in Russia, in which indicators of success were defined and evaluated at each. The ultimate goal was an increase in tiger numbers to 1 individual/100 km(2) at each site. We predicted that improvements in law enforcement effectiveness would be followed by increases in prey numbers and, subsequently, tiger numbers. We used short-term and long-term indicators of success, including: (i) patrol team effort and effectiveness; (ii) catch per unit effort indicators (to measure reductions in threats); and (iii) changes in target species numbers. In addition to implementing a monitoring system, we focused on improving law enforcement management using an adaptive management process. Over 4 years, we noted clear increases in patrol effort and a partial reduction in threats. Although we did not detect clear trends in ungulate numbers, tiger populations remained stable or increased, suggesting that poaching of tigers may be more limiting than prey depletion. Increased effectiveness is needed before a clear reduction in threats can be noted, and more time is needed before detecting responses in target populations. Nonetheless, delineation of concrete goals and indicators of success provide a means of evaluating progress and weaknesses. Such monitoring should be a central component of law enforcement strategies for protected areas.

Identifying conservation successes, failures and future opportunities; assessing recovery potential of wild ungulates and tigers in Eastern Cambodia.

Conservation investment, particularly for charismatic and wide-ranging large mammal species, needs to be evidence-based. Despite the prevalence of this theme within the literature, examples of robust data being generated to guide conservation policy and funding decisions are rare. We present the first published case-study of tiger conservation in Indochina, from a site where an evidence-based approach has been implemented for this iconic predator and its prey. Despite the persistence of extensive areas of habitat, Indochina's tiger and ungulate prey populations are widely supposed to have precipitously declined in recent decades. The Seima Protection Forest (SPF), and broader Eastern Plains Landscape, was identified in 2000 as representing Cambodia's best hope for tiger recovery; reflected in its designation as a Global Priority Tiger Conservation Landscape. Since 2005 distance sampling, camera-trapping and detection-dog surveys have been employed to assess the recovery potential of ungulate and tiger populations in SPF. Our results show that while conservation efforts have ensured that small but regionally significant populations of larger ungulates persist, and density trends in smaller ungulates are stable, overall ungulate populations remain well below theoretical carrying capacity. Extensive field surveys failed to yield any evidence of tiger, and we contend that there is no longer a resident population within the SPF. This local extirpation is believed to be primarily attributable to two decades of intensive hunting; but importantly, prey densities are also currently below the level necessary to support a viable tiger population. Based on these results and similar findings from neighbouring sites, Eastern Cambodia does not currently constitute a Tiger Source Site nor meet the criteria of a Global Priority Tiger Landscape. However, SPF retains global importance for many other elements of biodiversity. It retains high regional importance for ungulate populations and potentially in the future for Indochinese tigers, given adequate prey and protection.

Improving effectiveness of protection efforts in tiger source sites: Developing a framework for law enforcement monitoring using MIST.

Wild tigers are in a critical state with an estimated population decline of more than 95% over the past century. Improving the capacity and effectiveness of law enforcement in reducing poaching of tigers is an immediate priority to secure remaining wild populations in source sites. From 2008-2010, standardized patrol-based law enforcement monitoring (LEM) was established under the Tigers Forever Program across 8 key tiger sites in order to improve and evaluate law enforcement interventions. Patrol-based monitoring has the distinct advantage of providing regular and rapid information on illegal activities and ranger performance, although, until recently, it has received relatively little scrutiny from the conservation community. The present paper outlines a framework for implementation of LEM in tiger source sites using MIST, a computerized management information system for ranger-based data collection. The framework addresses many of the technical, practical and institutional challenges involved in the design, implementation, sustainability and evaluation of LEM. Adoption of such a framework for LEM is a cost-effective strategy to improve the efficiency of law enforcement efforts, to increase the motivation of enforcement staff and to promote the accountability of law enforcement agencies in addressing threats to tigers. When combined with independent, systematic and science-based monitoring of tigers and their prey, LEM has great potential for evaluating the effectiveness of protection-based conservation investments.

Monitoring great ape and elephant abundance at large spatial scales: measuring effectiveness of a conservation landscape.

Protected areas are fundamental to biodiversity conservation, but there is growing recognition of the need to extend beyond protected areas to meet the ecological requirements of species at larger scales. Landscape-scale conservation requires an evaluation of management impact on biodiversity under different land-use strategies; this is challenging and there exist few empirical studies. In a conservation landscape in northern Republic of Congo we demonstrate the application of a large-scale monitoring program designed to evaluate the impact of conservation interventions on three globally threatened species: western gorillas, chimpanzees and forest elephants, under three land-use types: integral protection, commercial logging, and community-based natural resource management. We applied distance-sampling methods to examine species abundance across different land-use types under varying degrees of management and human disturbance. We found no clear trends in abundance between land-use types. However, units with interventions designed to reduce poaching and protect habitats--irrespective of land-use type--harboured all three species at consistently higher abundance than a neighbouring logging concession undergoing no wildlife management. We applied Generalized-Additive Models to evaluate a priori predictions of species response to different landscape processes. Our results indicate that, given adequate protection from poaching, elephants and gorillas can profit from herbaceous vegetation in recently logged forests and maintain access to ecologically important resources located outside of protected areas. However, proximity to the single integrally protected area in the landscape maintained an overriding positive influence on elephant abundance, and logging roads--even subject to anti-poaching controls--were exploited by elephant poachers and had a major negative influence on elephant distribution. Chimpanzees show a clear preference for unlogged or more mature forests and human disturbance had a negative influence on chimpanzee abundance, in spite of anti-poaching interventions. We caution against the pitfalls of missing and confounded co-variables in model-based estimation approaches and highlight the importance of spatial scale in the response of different species to landscape processes. We stress the importance of a stratified design-based approach to monitoring species status in response to conservation interventions and advocate a holistic framework for landscape-scale monitoring that includes smaller-scale targeted research and punctual assessment of threats.

Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla).

Within-group female relationships, and relationships between females and adult males have not been described for wild western lowland gorillas. New data are presented here from Mbeli Bai in the Nouabale-Ndoki National Park, Republic of Congo. Nine groups were observed over a continuous 2-year period, and affiliative and agonistic interactions, as well as time spent by females and adult males in proximity to each other were recorded. Affiliative behavior was extremely rare in the bai, and measures of proximity between individuals were inconclusive because of the small sample sizes. Rates of agonistic interaction among females were highly variable between groups. The majority of agonistic interactions were undecided, and the supplant rate was low. Evidence for an agonistic dominance hierarchy is weak. The data do not support hypotheses that increased frugivory in western lowland gorillas raises levels of within-group contest competition; however, the need for intersite comparisons is stressed. In contrast, rates of agonistic behavior between females and silverback males were higher and more consistent between groups. Agonistic relationships between males and females conformed with patterns seen in mountain gorillas, where male protection from intraspecific aggression is important. The benefit females gain by forming long-term cooperative alliances appears to be small, and is likely outweighed by reproductive advantages associated with male protection.