Leprosy in wild chimpanzees.

Humans are considered as the main host for Mycobacterium leprae1, the aetiological agent of leprosy, but spillover has occurred to other mammals that are now maintenance hosts, such as nine-banded armadillos and red squirrels2,3. Although naturally acquired leprosy has also been described in captive nonhuman primates4-7, the exact origins of infection remain unclear. Here we describe leprosy-like lesions in two wild populations of western chimpanzees (Pan troglodytes verus) in Cantanhez National Park, Guinea-Bissau and Taï National Park, Côte d'Ivoire, West Africa. Longitudinal monitoring of both populations revealed the progression of disease symptoms compatible with advanced leprosy. Screening of faecal and necropsy samples confirmed the presence of M. leprae as the causative agent at each site and phylogenomic comparisons with other strains from humans and other animals show that the chimpanzee strains belong to different and rare genotypes (4N/O and 2F). These findings suggest that M. leprae may be circulating in more wild animals than suspected, either as a result of exposure to humans or other unknown environmental sources.

Oesophagostomum stephanostomum causing parasitic granulomas in wild chimpanzees (Pan troglodytes verus) of Taï National Park, Côte d'Ivoire.

Nematodes belonging to the genus Oesophagostomum frequently infect wild chimpanzees (Pan troglodytes) across widely separated field sites. Nodular lesions (granulomas) containing Oesophagostomum are commonly seen in the abdomen of infected chimpanzees post-mortem. At Taï National Park, Côte d'Ivoire, previous studies have identified larvae of a variety of Oesophagostomum spp. in wild chimpanzee stool, based on sequencing of larval DNA, and nodular lesions associated with Oesophagostomum, identified morphologically to the genus level but not sequenced. Here we present three recent cases of parasitic granulomas found post-mortem in chimpanzees at Taï. We complement descriptions of gross pathology, histopathology and parasitology with PCR and sequencing of DNA isolated from the parasitic nodules and from adult worms found inside the nodules. In all three cases, we identify Oesophagostomum stephanostomum as the causative agent. The sequences from this study were identical to the only other published sequences from nodules in nonhuman primates-those from the wild chimpanzees of Gombe, Tanzania.

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.

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.

No Evidence of Gouléako and Herbert Virus Infections in Pigs, Côte d'Ivoire and Ghana.

A recent report suggested that 2 novel bunyaviruses discovered in insects in Côte d'Ivoire caused lethal disease in swine in South Korea. We conducted cell culture studies and tested serum from pigs exposed to mosquitoes in Côte d'Ivoire and Ghana and found no evidence for infection in pigs.

Fatal monkeypox in wild-living sooty mangabey, Côte d'Ivoire, 2012.

We isolated a monkeypox virus from a wild-living monkey, a sooty mangabey, found dead in Taï National Park, Côte d'Ivoire, in March 2012. The whole-genome sequence obtained from this isolate and directly from clinical specimens showed its close relationship to monkeypox viruses from Western Africa.

Absence of frequent herpesvirus transmission in a nonhuman primate predator-prey system in the wild.

Emergence of viruses into the human population by transmission from nonhuman primates (NHPs) represents a serious potential threat to human health that is primarily associated with the increased bushmeat trade. Transmission of RNA viruses across primate species appears to be relatively frequent. In contrast, DNA viruses appear to be largely host specific, suggesting low transmission potential. Herein, we use a primate predator-prey system to study the risk of herpesvirus transmission between different primate species in the wild. The system was comprised of western chimpanzees (Pan troglodytes verus) and their primary (western red colobus, Piliocolobus badius badius) and secondary (black-and-white colobus, Colobus polykomos) prey monkey species. NHP species were frequently observed to be coinfected with multiple beta- and gammaherpesviruses (including new cytomegalo- and rhadinoviruses). However, despite frequent exposure of chimpanzees to blood, organs, and bones of their herpesvirus-infected monkey prey, there was no evidence for cross-species herpesvirus transmission. These findings suggest that interspecies transmission of NHP beta- and gammaherpesviruses is, at most, a rare event in the wild.

New evidence for self-medication in bonobos: Manniophyton fulvum leaf- and stemstrip-swallowing from LuiKotale, Salonga National Park, DR Congo.

The swallowing of entire leaves by apes across Africa without chewing has been observed for over 40 plant species. Here we add evidence for (a) a new site, LuiKotale where leaf-swallowing of Manniophyton fulvum (Euphorbiaceae) is observed in bonobos, (b) a so far unreported ingestion of unchewed stemstrips of M. fulvum, we name stemstrip-swallowing; and (c) a test of some of the requirements put forward by Huffman for the assessment of plants ingested for medical purpose. As ecological correlates we analyzed M. fulvum phenological data and examined 1,094 dung piles collected between 2002 and 2009. By that we assessed availability and choice of leaves. In addition, we provide the first full description of the behavior related to this plant species' use by chimpanzees or bonobos using 56 bouts of M. fulvum ingestion observed between October 2007 and February 2010. With these data we tested and met 4 of the 6 requirements given by Huffman, supporting ingestion of this species as self-medication. Despite species' year-round availability and abundance, M. fulvum was ingested only at specific times, in very small amounts, and by a small proportion of individuals per party. In the absence of our own parasitological data, we used M. fulvum swallowing as evidence for parasite infestation, and seasonality as a proxy for stressors underlying seasonal fluctuation and impacting immune responses. Using these indirect factors available, we investigated conditions for a parasite to develop to its infective stage as well as conditions for the host to cope with infections. Both rain and temperature were good predictors for M. fulvum ingestion. We discuss the use of M. fulvum with respect to its hispidity and subsequent purging properties and provide insight into its ethnomedicinal uses by humans, stimulating speculations about potentially additional pharmacological effects.

Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee.

Tuberculosis (TB) is caused by gram-positive bacteria known as the Mycobacterium tuberculosis complex (MTBC). MTBC include several human-associated lineages and several variants adapted to domestic and, more rarely, wild animal species. We report an M. tuberculosis strain isolated from a wild chimpanzee in Côte d'Ivoire that was shown by comparative genomic and phylogenomic analyses to belong to a new lineage of MTBC, closer to the human-associated lineage 6 (also known as M. africanum West Africa 2) than to the other classical animal-associated MTBC strains. These results show that the general view of the genetic diversity of MTBC is limited and support the possibility that other MTBC variants exist, particularly in wild mammals in Africa. Exploring this diversity is crucial to the understanding of the biology and evolutionary history of this widespread infectious disease.

Carrion fly-derived DNA as a tool for comprehensive and cost-effective assessment of mammalian biodiversity.

Large-scale monitoring schemes are essential in assessing global mammalian biodiversity, and in this framework, leeches have recently been promoted as an indirect source of DNA from terrestrial mammal species. Carrion feeding flies are ubiquitous and can be expected to feed on many vertebrate carcasses. Hence, we tested whether fly-derived DNA analysis may also serve as a novel tool for mammalian diversity surveys. We screened DNA extracted from 201 carrion flies collected in tropical habitats of Côte d'Ivoire and Madagascar for mammal DNA using multiple PCR systems and retrieved DNA sequences from a diverse set of species (22 in Côte d'Ivoire, four in Madagascar) exploiting distinct forest strata and displaying a broad range of body sizes. Deep sequencing of amplicons generated from pools of flies performed equally well as individual sequencing approaches. We conclude that the analysis of fly-derived DNA can be implemented in a very rapid and cost-effective manner and will give a relatively unbiased picture of local mammal diversity. Carrion flies therefore represent an extraordinary and thus far unexploited resource of mammal DNA, which will probably prove useful for future inventories of wild mammal communities.

Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions.

Adenoviruses (AdVs) broadly infect vertebrate hosts, including a variety of nonhuman primates (NHPs). In the present study, we identified AdVs in NHPs living in their natural habitats, and through the combination of phylogenetic analyses and information on the habitats and epidemiological settings, we detected possible horizontal transmission events between NHPs and humans. Wild NHPs were analyzed with a pan-primate AdV-specific PCR using a degenerate nested primer set that targets the highly conserved adenovirus DNA polymerase gene. A plethora of novel AdV sequences were identified, representing at least 45 distinct AdVs. From the AdV-positive individuals, 29 nearly complete hexon genes were amplified and, based on phylogenetic analysis, tentatively allocated to all known human AdV species (Human adenovirus A to Human adenovirus G [HAdV-A to -G]) as well as to the only simian AdV species (Simian adenovirus A [SAdV-A]). Interestingly, five of the AdVs detected in great apes grouped into the HAdV-A, HAdV-D, HAdV-F, or SAdV-A clade. Furthermore, we report the first detection of AdVs in New World monkeys, clustering at the base of the primate AdV evolutionary tree. Most notably, six chimpanzee AdVs of species HAdV-A to HAdV-F revealed a remarkably close relationship to human AdVs, possibly indicating recent interspecies transmission events.

Wild chimpanzees infected with 5 Plasmodium species.

Data are missing on the diversity of Plasmodium spp. infecting apes that live in their natural habitat, with limited possibility of human-mosquito-ape exchange. We surveyed Plasmodium spp. diversity in wild chimpanzees living in an undisturbed tropical rainforest habitat and found 5 species: P. malariae, P. vivax, P. ovale, P. reichenowi, and P. gaboni.

A longitudinal study of urinary dipstick parameters in wild chimpanzees (Pan troglodytes verus) in Côte d'Ivoire.

We performed 796 dip-stick tests on urine from 100 wild West African chimpanzees (Pan troglodytes verus) from 4 habituated groups in the tropical rain forest of Taï National Park, Cote d'Ivoire, to establish reference values for health monitoring. Specific gravity was also measured on 359 urine samples from 62 chimpanzees. The effect of age, sex, group, month, estrus, pregnancy, meat consumption, and acute respiratory disease on pH, leucocytes, protein, blood, hemoglobin, and glucose was examined using ordinal logistic regression. The presence of nitrite, ketones, bilirubin, and urobilinogen in urine was also recorded. Outbreak of acute respiratory disease did not influence any of the urinary parameters. Thirty-seven percent of the samples had a pH <7 and the whole range of pH was found through the year, in all age groups, and in both sexes. Meat consumption lowered the urinary pH. Our results show that all pH levels must be considered normal for the West African chimpanzee subspecies P. troglodytes verus living in the rainforest. We also found a cluster of glucose-positive samples at a specific point in time which was not attributed to diabetes mellitus. These findings highlight that there are differences in normal physiological parameters among wild chimpanzees living in different habitats.

Author Correction: Evidence for Human Streptococcus pneumoniae in wild and captive chimpanzees: A potential threat to wild populations.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Human Respiratory Syncytial Virus and Streptococcus pneumoniae Infection in Wild Bonobos.

Despite being important conservation tools, tourism and research may cause transmission of pathogens to wild great apes. Investigating respiratory disease outbreaks in wild bonobos, we identified human respiratory syncytial virus and Streptococcus pneumoniae as causative agents. A One Health approach to disease control should become part of great ape programs.

Evidence for Human Streptococcus pneumoniae in wild and captive chimpanzees: A potential threat to wild populations.

Habituation of wild great apes for tourism and research has had a significant positive effect on the conservation of these species. However, risks associated with such activities have been identified, specifically the transmission of human respiratory viruses to wild great apes, causing high morbidity and, occasionally, mortality. Here, we investigate the source of bacterial-viral co-infections in wild and captive chimpanzee communities in the course of several respiratory disease outbreaks. Molecular analyses showed that human respiratory syncytial viruses (HRSV) and human metapneumoviruses (HMPV) were involved in the etiology of the disease. In addition our analysis provide evidence for coinfection with Streptococcus (S.) pneumoniae. Characterisation of isolates from wild chimpanzees point towards a human origin of these bacteria. Transmission of these bacteria is of concern because - in contrast to HRSV and HMPV - S. pneumoniae can become part of the nasopharyngeal flora, contributing to the severity of respiratory disease progression. Furthermore these bacteria have the potential to spread to other individuals in the community and ultimately into the population. Targeted vaccination programs could be used to vaccinate habituated great apes but also human populations around great ape habitats, bringing health benefits to both humans and wild great apes.

The effect of climate fluctuation on chimpanzee birth sex ratio.

Climate and weather conditions, such as the North Atlantic Oscillation, precipitation and temperature influence the birth sex ratio (BSR) of various higher latitude species, including deer, elephant seals or northern human populations. Although, tropical regions show only little variation in temperature, climate and weather conditions can fluctuate with consequences for phenology and food resource availability. Here, we evaluate, whether the BSR of chimpanzees, inhabiting African tropical forests, is affected by climate fluctuations as well. Additionally, we evaluate, if variation in consumption of a key food resource with high nutritional value, Coula edulis nuts, is linked to both climate fluctuations and variation in BSR. We use long-term data from two study groups located in Taï National Park, Côte d'Ivoire to assess the influence of local weather conditions and the global climate driver El Niño Southern Oscillation (ENSO) on offspring sex. Côte d'Ivoire has experienced considerable climate variation over the last decades, with increasing temperature and declining precipitation. For both groups we find very similar time windows around the month of conception, in which offspring sex is well predicted by ENSO, with more males following low ENSO values, corresponding to periods of high rainfall. Furthermore, we find that the time spent cracking and feeding on Coula nuts is strongly influenced by climate conditions. Although, some of our analysis suggest that a higher proportion of males is born after periods with higher nut consumption frequency, we cannot conclude decisively at this point that nut consumption may influence shifts in BSR. All results combined suggest that also chimpanzees may experience climate related shifts in offspring sex ratios as response to climate fluctuation.