Discovery of Novel Herpes Simplexviruses in Wild Gorillas, Bonobos, and Chimpanzees Supports Zoonotic Origin of HSV-2.

Viruses closely related to human pathogens can reveal the origins of human infectious diseases. Human herpes simplexvirus type 1 (HSV-1) and type 2 (HSV-2) are hypothesized to have arisen via host-virus codivergence and cross-species transmission. We report the discovery of novel herpes simplexviruses during a large-scale screening of fecal samples from wild gorillas, bonobos, and chimpanzees. Phylogenetic analysis indicates that, contrary to expectation, simplexviruses from these African apes are all more closely related to HSV-2 than to HSV-1. Molecular clock-based hypothesis testing suggests the divergence between HSV-1 and the African great ape simplexviruses likely represents a codivergence event between humans and gorillas. The simplexviruses infecting African great apes subsequently experienced multiple cross-species transmission events over the past 3 My, the most recent of which occurred between humans and bonobos around 1 Ma. These findings revise our understanding of the origins of human herpes simplexviruses and suggest that HSV-2 is one of the earliest zoonotic pathogens.

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue.

Many non-human primate species in sub-Saharan Africa are infected with Treponema pallidum subsp. pertenue, the bacterium causing yaws in humans. In humans, yaws is often characterized by lesions of the extremities and face, while T. pallidum subsp. pallidum causes venereal syphilis and is typically characterized by primary lesions on the genital, anal or oral mucosae. It remains unclear whether other T. pallidum subspecies found in humans also occur in non-human primates and how the genomic diversity of non-human primate T. pallidum subsp. pertenue lineages is distributed across hosts and space. We observed orofacial and genital lesions in sooty mangabeys (Cercocebus atys) in Taï National Park, Côte d'Ivoire and collected swabs and biopsies from symptomatic animals. We also collected non-human primate bones from 8 species in Taï National Park and 16 species from 11 other sites across sub-Saharan Africa. Samples were screened for T. pallidum DNA using polymerase chain reactions (PCRs) and we used in-solution hybridization capture to sequence T. pallidum genomes. We generated three nearly complete T. pallidum genomes from biopsies and swabs and detected treponemal DNA in bones of six non-human primate species in five countries, allowing us to reconstruct three partial genomes. Phylogenomic analyses revealed that both orofacial and genital lesions in sooty mangabeys from Taï National Park were caused by T. pallidum subsp. pertenue. We showed that T. pallidum subsp. pertenue has infected non-human primates in Taï National Park for at least 28 years and has been present in two non-human primate species that had not been described as T. pallidum subsp. pertenue hosts in this ecosystem, western chimpanzees (Pan troglodytes verus) and western red colobus (Piliocolobus badius), complementing clinical evidence that started accumulating in Taï National Park in 2014. More broadly, simian T. pallidum subsp. pertenue strains did not form monophyletic clades based on host species or the symptoms caused, but rather clustered based on geography. Geographical clustering of T. pallidum subsp. pertenue genomes might be compatible with cross-species transmission of T. pallidum subsp. pertenue within ecosystems or environmental exposure, leading to the acquisition of closely related strains. Finally, we found no evidence for mutations that confer antimicrobial resistance.

Ungulate management in European national parks: Why a more integrated European policy is needed.

1. Primary objectives of national parks usually include both, the protection of natural processes and species conservation. When these objectives conflict, as occurs because of the cascading effects of large mammals (i.e., ungulates and large carnivores) on lower trophic levels, park managers have to decide upon the appropriate management while considering various local circumstances. 2. To analyse if ungulate management strategies are in accordance with the objectives defined for protected areas, we assessed the current status of ungulate management across European national parks using the naturalness concept and identified the variables that influence the management. 3. We collected data on ungulate management from 209 European national parks in 29 countries by means of a large-scale questionnaire survey. Ungulate management in the parks was compared by creating two naturalness scores. The first score reflects ungulate and large carnivore species compositions, and the second evaluates human intervention on ungulate populations. We then tested whether the two naturalness score categories are influenced by the management objectives, park size, years since establishment, percentage of government-owned land, and human impact on the environment (human influence index) using two generalized additive mixed models. 4. In 67.9% of the national parks, wildlife is regulated by culling (40.2%) or hunting (10.5%) or both (17.2%). Artificial feeding occurred in 81.3% of the national parks and only 28.5% of the national parks had a non-intervention zone covering at least 75% of the area. Furthermore, ungulate management differed greatly among the different countries, likely because of differences in hunting traditions and cultural and political backgrounds. Ungulate management was also influenced by park size, human impact on the landscape, and national park objectives, but after removing these variables from the full model the reduced models only showed a small change in the deviance explained. In areas with higher anthropogenic pressure, wildlife diversity tended to be lower and a higher number of domesticated species tended to be present. Human intervention (culling and artificial feeding) was lower in smaller national parks and when park objectives followed those set by the International Union for the Conservation of Nature (IUCN). 5. Our study shows that many European national parks do not fulfil the aims of protected area management as set by IUCN guidelines. In contrast to the USA and Canada, Europe currently has no common ungulate management policy within national parks. This lack of a common policy together with differences in species composition, hunting traditions, and cultural or political context has led to differences in ungulate management among European countries. To fulfil the aims and objectives of national parks and to develop ungulate management strategies further, we highlight the importance of creating a more integrated European ungulate management policy to meet the aims of national parks.

CD4 receptor diversity in chimpanzees protects against SIV infection.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4+ T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.

Effects of Land cover change on Great Apes distribution at the Lobéké National Park and its surrounding Forest Management Units, South-East Cameroon. A 13 year time series analysis.

Understanding the effects of land cover change on wildlife distribution is very important for resource management and conservation planning. This paper aimed at detecting the effects of land cover change on great apes distribution at the Lobéké National Park and its bounded forest management units (FMUs). Data on great ape nests were collected in the field for the years 2001 and 2014 through distance sampling with line transects. Landsat TM images of South-East Cameroon for the years 2001 and 2014 were acquired from earth explorer and corrected atmospherically for proper visualization. An area of interest comprising the Lobéké National Park and its FMUs was extracted for classification and change detection. A comparison in great apes nest distribution and change per land cover change category was done for both years through point pattern analysis, whereas a time series analysis of the detected land cover change impacts on great apes nest distribution for a period of 13 years was modeled using logistic growth and regression equations in Vensim 7.2. The results could illustrate that, as land cover changes from one cover type in 2001 to another in 2014, increases or decreases in great apes nests were observed within each changed area.

Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest.

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

The socio-economic drivers of bushmeat consumption during the West African Ebola crisis.

Bushmeat represents an important source of animal protein for humans in tropical Africa. Unsustainable bushmeat hunting is a major threat to wildlife and its consumption is associated with an increased risk of acquiring zoonotic diseases, such as Ebola virus disease (EVD). During the recent EVD outbreak in West Africa, it is likely that human dietary behavior and local attitudes toward bushmeat consumption changed in response to the crisis, and that the rate of change depended on prevailing socio-economic conditions, including wealth and education. In this study, we therefore investigated the effects of income, education, and literacy on changes in bushmeat consumption during the crisis, as well as complementary changes in daily meal frequency, food diversity and bushmeat preference. More specifically, we tested whether wealthier households with more educated household heads decreased their consumption of bushmeat during the EVD crisis, and whether their daily meal frequency and food diversity remained constant. We used Generalized Linear Mixed Models to analyze interview data from two nationwide household surveys across Liberia. We found an overall decrease in bushmeat consumption during the crisis across all income levels. However, the rate of bushmeat consumption in high-income households decreased less than in low-income households. Daily meal frequency decreased during the crisis, and the diversity of food items and preferences for bushmeat species remained constant. Our multidisciplinary approach to study the impact of EVD can be applied to assess how other disasters affect social-ecological systems and improve our understanding and the management of future crises.

Locating chimpanzee nests and identifying fruiting trees with an unmanned aerial vehicle.

Monitoring of animal populations is essential for conservation management. Various techniques are available to assess spatiotemporal patterns of species distribution and abundance. Nest surveys are often used for monitoring great apes. Quickly developing technologies, including unmanned aerial vehicles (UAVs) can be used to complement these ground-based surveys, especially for covering large areas rapidly. Aerial surveys have been used successfully to detect the nests of orang-utans. It is unknown if such an approach is practical for African apes, which usually build their nests at lower heights, where they might be obscured by forest canopy. In this 2-month study, UAV-derived aerial imagery was used for two distinct purposes: testing the detectability of chimpanzee nests and identifying fruiting trees used by chimpanzees in Loango National Park (Gabon). Chimpanzee nest data were collected through two approaches: we located nests on the ground and then tried to detect them in UAV photos and vice versa. Ground surveys were conducted using line transects, reconnaissance trails, and opportunistic sampling during which we detected 116 individual nests in 28 nest groups. In complementary UAV images we detected 48% of the individual nests (68% of nest groups) in open coastal forests and 8% of individual nests (33% of nest groups) in closed canopy inland forests. The key factor for nest detectability in UAV imagery was canopy openness. Data on fruiting trees were collected from five line transects. In 122 UAV images 14 species of trees (N = 433) were identified, alongside 37 tree species (N = 205) in complementary ground surveys. Relative abundance of common tree species correlated between ground and UAV surveys. We conclude that UAVs have great potential as a rapid assessment tool for detecting chimpanzee presence in forest with open canopy and assessing fruit tree availability. UAVs may have limited applicability for nest detection in closed canopy forest.

Estimating chimpanzee population size with nest counts: validating methods in Taï National Park.

Successful conservation and management of wild animals require reliable estimates of their population size. Ape surveys almost always rely on counts of sleeping nests, as the animals occur at low densities and visibility is low in tropical forests. The reliability of standing-crop nest counts and marked-nest counts, the most widely used methods, has not been tested on populations of known size. Therefore, the answer to the question of which method is more appropriate for surveying chimpanzee population remains problematic and comparisons among sites are difficult. This study aimed to test the validity of these two methods by comparing their estimates to the known population size of three habituated chimpanzee communities in Taï National Park [Boesch et al., Am J Phys Anthropol 130:103-115, 2006; Boesch et al., Am J Primatol 70:519-532, 2008]. In addition to transect surveys, we made observations on nest production rate and nest lifetime. Taï chimpanzees built 1.143 nests per day. The mean nest lifetime of 141 fresh nests was 91.22 days. Estimate precision for the two methods did not differ considerably (difference of coefficient of variation <5%). The estimate of mean nest decay time was more precise (CV=6.46%) when we used covariates (tree species, rainfall, nest height and age) to model nest decay rate, than when we took a simple mean of nest decay times (CV=9.17%). The two survey methods produced point estimates of chimpanzee abundance that were similar and reliable: i.e. for both methods the true chimpanzee abundance was included within the 95% estimate confidence interval. We recommend further research on covariate modeling of nest decay times as one way to improve the precision and to reduce the costs of conducting nest surveys.

The price of play: self-organized infant mortality cycles in chimpanzees.

Chimpanzees have been used extensively as a model system for laboratory research on infectious diseases. Ironically, we know next to nothing about disease dynamics in wild chimpanzee populations. Here, we analyze long-term demographic and behavioral data from two habituated chimpanzee communities in Taï National Park, Côte d'Ivoire, where previous work has shown respiratory pathogens to be an important source of infant mortality. In this paper we trace the effect of social connectivity on infant mortality dynamics. We focus on social play which, as the primary context of contact between young chimpanzees, may serve as a key venue for pathogen transmission. Infant abundance and mortality rates at Taï cycled regularly and in a way that was not well explained in terms of environmental forcing. Rather, infant mortality cycles appeared to self-organize in response to the ontogeny of social play. Each cycle started when the death of multiple infants in an outbreak synchronized the reproductive cycles of their mothers. A pulse of births predictably arrived about twelve months later, with social connectivity increasing over the following two years as the large birth cohort approached the peak of social play. The high social connectivity at this play peak then appeared to facilitate further outbreaks. Our results provide the first evidence that social play has a strong role in determining chimpanzee disease transmission risk and the first record of chimpanzee disease cycles similar to those seen in human children. They also lend more support to the view that infectious diseases are a major threat to the survival of remaining chimpanzee populations.

Manipulating decay time for efficient large-mammal density estimation: gorillas and dung height.

Large-mammal surveys often rely on indirect signs such as dung or nests. Sign density is usually translated into animal density using sign production and decay rates. In principle, such auxiliary variable estimates should be made in a spatially unbiased manner. However, traditional decay rate estimation methods entail following many signs from production to disappearance, which, in large study areas, requires extensive travel effort. Consequently, decay rate estimates have tended to be made instead at some convenient but unrepresentative location. In this study we evaluated how much bias might be induced by extrapolating decay rates from unrepresentative locations, how much effort would be required to implement current methods in a spatially unbiased manner, and what alternate approaches might be used to improve precision. To evaluate the extent of bias induced by unrepresentative sampling, we collected data on gorilla dung at several central African sites. Variation in gorilla dung decay rate was enormous, varying by up to an order of magnitude within and between survey zones. We then estimated what the effort-precision relationship would be for a previously suggested "retrospective" decay rate (RDR) method, if it were implemented in a spatially unbiased manner. We also evaluated precision for a marked sign count (MSC) approach that does not use a decay rate. Because they require repeat visits to remote locations, both RDR and MSC require enormous effort levels in order to gain precise density estimates. Finally, we examined an objective criterion for decay (i.e., dung height). This showed great potential for improving RDR efficiency because choosing a high threshold height for decay reduces decay time and, consequently, the number of visits that need to be made to remote areas. The ability to adjust decay time using an objective decay criterion also opens up the potential for a "prospective" decay rate (PDR) approach. Further research is necessary to evaluate whether the temporal bias inherent in such an approach is small enough to ignore, given the 10-20-fold increases in precision promised by a PDR approach.