Hierarchical social modularity in gorillas.

Modern human societies show hierarchical social modularity (HSM) in which lower-order social units like nuclear families are nested inside increasingly larger units. It has been argued that this HSM evolved independently and after the chimpanzee-human split due to greater recognition of, and bonding between, dispersed kin. We used network modularity analysis and hierarchical clustering to quantify community structure within two western lowland gorilla populations. In both communities, we detected two hierarchically nested tiers of social structure which have not been previously quantified. Both tiers map closely to human social tiers. Genetic data from one population suggested that, as in humans, social unit membership was kin structured. The sizes of gorilla social units also showed the kind of consistent scaling ratio between social tiers observed in humans, baboons, toothed whales, and elephants. These results indicate that the hierarchical social organization observed in humans may have evolved far earlier than previously asserted and may not be a product of the social brain evolution unique to the hominin lineage.

Vaccinating captive chimpanzees to save wild chimpanzees.

Infectious disease has only recently been recognized as a major threat to the survival of Endangered chimpanzees and Critically Endangered gorillas in the wild. One potentially powerful tool, vaccination, has not been deployed in fighting this disease threat, in good part because of fears about vaccine safety. Here we report on what is, to our knowledge, the first trial in which captive chimpanzees were used to test a vaccine intended for use on wild apes rather than humans. We tested a virus-like particle vaccine against Ebola virus, a leading source of death in wild gorillas and chimpanzees. The vaccine was safe and immunogenic. Captive trials of other vaccines and of methods for vaccine delivery hold great potential as weapons in the fight against wild ape extinction.

Origin of the human malaria parasite Plasmodium falciparum in gorillas.

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.

Pandemic human viruses cause decline of endangered great apes.

Commercial hunting and habitat loss are major drivers of the rapid decline of great apes [1]. Ecotourism and research have been widely promoted as a means of providing alternative value for apes and their habitats [2]. However, close contact between humans and habituated apes during ape tourism and research has raised concerns that disease transmission risks might outweigh benefits [3-7]. To date only bacterial and parasitic infections of typically low virulence have been shown to move from humans to wild apes [8, 9]. Here, we present the first direct evidence of virus transmission from humans to wild apes. Tissue samples from habituated chimpanzees that died during three respiratory-disease outbreaks at our research site, Côte d'Ivoire, contained two common human paramyxoviruses. Viral strains sampled from chimpanzees were closely related to strains circulating in contemporaneous, worldwide human epidemics. Twenty-four years of mortality data from observed chimpanzees reveal that such respiratory outbreaks could have a long history. In contrast, survey data show that research presence has had a strong positive effect in suppressing poaching around the research site. These observations illustrate the challenge of maximizing the benefit of research and tourism to great apes while minimizing the negative side effects.

Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas.

Chimpanzees and gorillas are the only nonhuman primates known to harbor viruses closely related to HIV-1. Phylogenetic analyses showed that gorillas acquired the simian immunodeficiency virus SIVgor from chimpanzees, and viruses from the SIVcpz/SIVgor lineage have been transmitted to humans on at least four occasions, leading to HIV-1 groups M, N, O, and P. To determine the geographic distribution, prevalence, and species association of SIVgor, we conducted a comprehensive molecular epidemiological survey of wild gorillas in Central Africa. Gorilla fecal samples were collected in the range of western lowland gorillas (n = 2,367) and eastern Grauer gorillas (n = 183) and tested for SIVgor antibodies and nucleic acids. SIVgor antibody-positive samples were identified at 2 sites in Cameroon, with no evidence of infection at 19 other sites, including 3 in the range of the Eastern gorillas. In Cameroon, based on DNA and microsatellite analyses of a subset of samples, we estimated the prevalence of SIVgor to be 1.6% (range, 0% to 4.6%), which is significantly lower than the prevalence of SIVcpzPtt in chimpanzees (5.9%; range, 0% to 32%). All newly identified SIVgor strains formed a monophyletic lineage within the SIVcpz radiation, closely related to HIV-1 groups O and P, and clustered according to their field site of origin. At one site, there was evidence for intergroup transmission and a high intragroup prevalence. These isolated hot spots of SIVgor-infected gorilla communities could serve as a source for human infection. The overall low prevalence and sporadic distribution of SIVgor could suggest a decline of SIVgor in wild populations, but it cannot be excluded that SIVgor is still more prevalent in other parts of the geographical range of gorillas.

Western gorilla space use suggests territoriality.

The evolutionary origins of how modern humans share and use space are often modelled on the territorial-based violence of chimpanzees, with limited comparison to other apes. Gorillas are widely assumed to be non-territorial due to their large home ranges, extensive range overlap, and limited inter-group aggression. Using large-scale camera trapping, we monitored western gorillas in Republic of Congo across 60 km2. Avoidance patterns between groups were consistent with an understanding of the "ownership" of specific regions, with greater avoidance of their neighbours the closer they were to their neighbours' home range centres. Groups also avoided larger groups' home ranges to a greater extent, consistent with stronger defensive responses from more dominant groups. Our results suggest that groups may show territoriality, defending core regions of their home ranges against neighbours, and mirror patterns common across human evolution, with core areas of resident dominance and larger zones of mutual tolerance. This implies western gorillas may be a key system for understanding how humans have evolved the capacity for extreme territorial-based violence and warfare, whilst also engaging in the strong affiliative inter-group relationships necessary for large-scale cooperation.

Wave-like spread of Ebola Zaire.

In the past decade the Zaire strain of Ebola virus (ZEBOV) has emerged repeatedly into human populations in central Africa and caused massive die-offs of gorillas and chimpanzees. We tested the view that emergence events are independent and caused by ZEBOV variants that have been long resident at each locality. Phylogenetic analyses place the earliest known outbreak at Yambuku, Democratic Republic of Congo, very near to the root of the ZEBOV tree, suggesting that viruses causing all other known outbreaks evolved from a Yambuku-like virus after 1976. The tendency for earlier outbreaks to be directly ancestral to later outbreaks suggests that outbreaks are epidemiologically linked and may have occurred at the front of an advancing wave. While the ladder-like phylogenetic structure could also bear the signature of positive selection, our statistical power is too weak to reach a conclusion in this regard. Distances among outbreaks indicate a spread rate of about 50 km per year that remains consistent across spatial scales. Viral evolution is clocklike, and sequences show a high level of small-scale spatial structure. Genetic similarity decays with distance at roughly the same rate at all spatial scales. Our analyses suggest that ZEBOV has recently spread across the region rather than being long persistent at each outbreak locality. Controlling the impact of Ebola on wild apes and human populations may be more feasible than previously recognized.

Potential for Ebola transmission between gorilla and chimpanzee social groups.

Over the past decade Ebola hemorrhagic fever has emerged repeatedly in Gabon and Congo, causing numerous human outbreaks and massive die-offs of gorillas and chimpanzees. Why Ebola has emerged so explosively remains poorly understood. Previous studies have tended to focus on exogenous factors such as habitat disturbance and climate change as drivers of Ebola emergence while downplaying the contribution of transmission between gorilla or chimpanzee social groups. Here we report recent observations on behaviors that pose a risk of transmission among gorilla groups and between gorillas and chimpanzees. These observations support a reassessment of ape-to-ape transmission as an amplifier of Ebola outbreaks.

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.

The Final (Oral Ebola) Vaccine Trial on Captive Chimpanzees?

Could new oral vaccine technologies protect endangered wildlife against a rising tide of infectious disease? We used captive chimpanzees to test oral delivery of a rabies virus (RABV) vectored vaccine against Ebola virus (EBOV), a major threat to wild chimpanzees and gorillas. EBOV GP and RABV GP-specific antibody titers increased exponentially during the trial, with rates of increase for six orally vaccinated chimpanzees very similar to four intramuscularly vaccinated controls. Chimpanzee sera also showed robust neutralizing activity against RABV and pseudo-typed EBOV. Vaccination did not induce serious health complications. Blood chemistry, hematologic, and body mass correlates of psychological stress suggested that, although sedation induced acute stress, experimental housing conditions did not induce traumatic levels of chronic stress. Acute behavioral and physiological responses to sedation were strongly correlated with immune responses to vaccination. These results suggest that oral vaccination holds great promise as a tool for the conservation of apes and other endangered tropical wildlife. They also imply that vaccine and drug trials on other captive species need to better account for the effects of stress on immune response.

African origin of the malaria parasite Plasmodium vivax.

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

Non-random walks in monkeys and humans.

Principles of self-organization play an increasingly central role in models of human activity. Notably, individual human displacements exhibit strongly recurrent patterns that are characterized by scaling laws and can be mechanistically modelled as self-attracting walks. Recurrence is not, however, unique to human displacements. Here we report that the mobility patterns of wild capuchin monkeys are not random walks, and they exhibit recurrence properties similar to those of cell phone users, suggesting spatial cognition mechanisms shared with humans. We also show that the highly uneven visitation patterns within monkey home ranges are not entirely self-generated but are forced by spatio-temporal habitat heterogeneities. If models of human mobility are to become useful tools for predictive purposes, they will need to consider the interaction between memory and environmental heterogeneities.

Transmission of infectious diseases en route to habitat hotspots.

BACKGROUND: The spread of infectious diseases in wildlife populations is influenced by patterns of between-host contacts. Habitat "hotspots"--places attracting a large numbers of individuals or social groups--can significantly alter contact patterns and, hence, disease propagation. Research on the importance of habitat hotspots in wildlife epidemiology has primarily focused on how inter-individual contacts occurring at the hotspot itself increase disease transmission. However, in territorial animals, epidemiologically important contacts may primarily occur as animals cross through territories of conspecifics en route to habitat hotspots. So far, the phenomenon has received little attention. Here, we investigate the importance of these contacts in the case where infectious individuals keep visiting the hotspots and in the case where these individuals are not able to travel to the hotspot any more. METHODOLOGY AND PRINCIPAL FINDINGS: We developed a simulation epidemiological model to investigate both cases in a scenario when transmission at the hotspot does not occur. We find that (i) hotspots still exacerbate epidemics, (ii) when infectious individuals do not travel to the hotspot, the most vulnerable individuals are those residing at intermediate distances from the hotspot rather than nearby, and (iii) the epidemiological vulnerability of a population is the highest when the number of hotspots is intermediate. CONCLUSIONS AND SIGNIFICANCE: By altering animal movements in their vicinity, habitat hotspots can thus strongly increase the spread of infectious diseases, even when disease transmission does not occur at the hotspot itself. Interestingly, when animals only visit the nearest hotspot, creating additional artificial hotspots, rather than reducing their number, may be an efficient disease control measure.

Consequences of non-intervention for infectious disease in African great apes.

Infectious disease has recently joined poaching and habitat loss as a major threat to African apes. Both "naturally" occurring pathogens, such as Ebola and Simian Immunodeficiency Virus (SIV), and respiratory pathogens transmitted from humans, have been confirmed as important sources of mortality in wild gorillas and chimpanzees. While awareness of the threat has increased, interventions such as vaccination and treatment remain controversial. Here we explore both the risk of disease to African apes, and the status of potential responses. Through synthesis of published data, we summarize prior disease impact on African apes. We then use a simple demographic model to illustrate the resilience of a well-known gorilla population to disease, modeled on prior documented outbreaks. We found that the predicted recovery time for this specific gorilla population from a single outbreak ranged from 5 years for a low mortality (4%) respiratory outbreak, to 131 years for an Ebola outbreak that killed 96% of the population. This shows that mortality rates comparable to those recently reported for disease outbreaks in wild populations are not sustainable. This is particularly troubling given the rising pathogen risk created by increasing habituation of wild apes for tourism, and the growth of human populations surrounding protected areas. We assess potential future disease spillover risk in terms of vaccination rates amongst humans that may come into contact with wild apes, and the availability of vaccines against potentially threatening diseases. We discuss and evaluate non-interventionist responses such as limiting tourist access to apes, community health programs, and safety, logistic, and cost issues that constrain the potential of vaccination.

Modelling the mobility of living organisms in heterogeneous landscapes: does memory improve foraging success?

Thanks to recent technological advances, it is now possible to track with an unprecedented precision and for long periods of time the movement patterns of many living organisms in their habitat. The increasing amount of data available on single trajectories offers the possibility of understanding how animals move and of testing basic movement models. Random walks have long represented the main description for micro-organisms and have also been useful to understand the foraging behaviour of large animals. Nevertheless, most vertebrates, in particular humans and other primates, rely on sophisticated cognitive tools such as spatial maps, episodic memory and travel cost discounting. These properties call for other modelling approaches of mobility patterns. We propose a foraging framework where a learning mobile agent uses a combination of memory-based and random steps. We investigate how advantageous it is to use memory for exploiting resources in heterogeneous and changing environments. An adequate balance of determinism and random exploration is found to maximize the foraging efficiency and to generate trajectories with an intricate spatio-temporal order, where travel routes emerge without multi-step planning. Based on this approach, we propose some tools for analysing the non-random nature of mobility patterns in general.

Modeling the spatial distribution and fruiting pattern of a key tree species in a neotropical forest: methodology and potential applications.

BACKGROUND: The movement patterns of wild animals depend crucially on the spatial and temporal availability of resources in their habitat. To date, most attempts to model this relationship were forced to rely on simplified assumptions about the spatiotemporal distribution of food resources. Here we demonstrate how advances in statistics permit the combination of sparse ground sampling with remote sensing imagery to generate biological relevant, spatially and temporally explicit distributions of food resources. We illustrate our procedure by creating a detailed simulation model of fruit production patterns for Dipteryx oleifera, a keystone tree species, on Barro Colorado Island (BCI), Panama. METHODOLOGY AND PRINCIPAL FINDINGS: Aerial photographs providing GPS positions for large, canopy trees, the complete census of a 50-ha and 25-ha area, diameter at breast height data from haphazardly sampled trees and long-term phenology data from six trees were used to fit 1) a point process model of tree spatial distribution and 2) a generalized linear mixed-effect model of temporal variation of fruit production. The fitted parameters from these models are then used to create a stochastic simulation model which incorporates spatio-temporal variations of D. oleifera fruit availability on BCI. CONCLUSIONS AND SIGNIFICANCE: We present a framework that can provide a statistical characterization of the habitat that can be included in agent-based models of animal movements. When environmental heterogeneity cannot be exhaustively mapped, this approach can be a powerful alternative. The results of our model on the spatio-temporal variation in D. oleifera fruit availability will be used to understand behavioral and movement patterns of several species on BCI.

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.