Paige, Sarah B; Frost, Simon D W; Gibson, Mhairi A; Jones, James Holland; Shankar, Anupama; Switzer, William M; Ting, Nelson; Goldberg, Tony L
Zoonotic pathogens cause an estimated 70% of emerging and re-emerging infectious diseases in humans. In sub-Saharan Africa, bushmeat hunting and butchering is considered the primary risk factor for human-wildlife contact and zoonotic disease transmission, particularly for the transmission of simian retroviruses. However, hunting is only one of many activities in sub-Saharan Africa that bring people and wildlife into contact. Here, we examine human-animal interaction in western Uganda, identifying patterns of injuries from animals and contact with nonhuman primates. Additionally, we identify individual-level risk factors associated with contact. Nearly 20% (246/1,240) of participants reported either being injured by an animal or having contact with a primate over their lifetimes. The majority (51.7%) of injuries were dog bites that healed with no long-term medical consequences. The majority (76.8%) of 125 total primate contacts involved touching a carcass; however, butchering (20%), hunting (10%), and touching a live primate (10%) were also reported. Red colobus (Piliocolobus rufomitratus tephrosceles) accounted for most primate contact events. Multivariate logistic regression indicated that men who live adjacent to forest fragments are at elevated risk of animal contact and specifically primate contact. Our results provide a useful comparison to West and Central Africa where "bushmeat hunting" is the predominant paradigm for human-wildlife contact and zoonotic disease transmission.
Full Text Available Simian hemorrhagic fever (SHF is a highly lethal disease in captive macaques. Three distinct arteriviruses are known etiological agents of past SHF epizootics, but only one, simian hemorrhagic fever virus (SHFV, has been isolated in cell culture. The natural reservoir(s of the three viruses have yet to be identified, but African nonhuman primates are suspected. Eleven additional divergent simian arteriviruses have been detected recently in diverse and apparently healthy African cercopithecid monkeys. Here, we report the successful isolation in MARC-145 cell culture of one of these viruses, Kibale red colobus virus 1 (KRCV-1, from serum of a naturally infected red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles sampled in Kibale National Park, Uganda. Intramuscular (i.m. injection of KRCV-1 into four cynomolgus macaques (Macaca fascicularis resulted in a self-limiting nonlethal disease characterized by depressive behavioral changes, disturbance in coagulation parameters, and liver enzyme elevations. In contrast, i.m. injection of SHFV resulted in typical lethal SHF characterized by mild fever, lethargy, lymphoid depletion, lymphoid and hepatocellular necrosis, low platelet counts, increased liver enzyme concentrations, coagulation abnormalities, and increasing viral loads. As hypothesized based on the genetic and presumed antigenic distance between KRCV-1 and SHFV, all four macaques that had survived KRCV-1 injection died of SHF after subsequent SHFV injection, indicating a lack of protective heterotypic immunity. Our data indicate that SHF is a disease of macaques that in all likelihood can be caused by a number of distinct simian arteriviruses, although with different severity depending on the specific arterivirus involved. Consequently, we recommend that current screening procedures for SHFV in primate-holding facilities be modified to detect all known simian arteriviruses.
Adam L Bailey
Full Text Available Key biological properties such as high genetic diversity and high evolutionary rate enhance the potential of certain RNA viruses to adapt and emerge. Identifying viruses with these properties in their natural hosts could dramatically improve disease forecasting and surveillance. Recently, we discovered two novel members of the viral family Arteriviridae: simian hemorrhagic fever virus (SHFV-krc1 and SHFV-krc2, infecting a single wild red colobus (Procolobus rufomitratus tephrosceles in Kibale National Park, Uganda. Nearly nothing is known about the biological properties of SHFVs in nature, although the SHFV type strain, SHFV-LVR, has caused devastating outbreaks of viral hemorrhagic fever in captive macaques. Here we detected SHFV-krc1 and SHFV-krc2 in 40% and 47% of 60 wild red colobus tested, respectively. We found viral loads in excess of 10(6-10(7 RNA copies per milliliter of blood plasma for each of these viruses. SHFV-krc1 and SHFV-krc2 also showed high genetic diversity at both the inter- and intra-host levels. Analyses of synonymous and non-synonymous nucleotide diversity across viral genomes revealed patterns suggestive of positive selection in SHFV open reading frames (ORF 5 (SHFV-krc2 only and 7 (SHFV-krc1 and SHFV-krc2. Thus, these viruses share several important properties with some of the most rapidly evolving, emergent RNA viruses.
Kooriyama, Takanori; Hasegawa, Hideo; Shimozuru, Michito; Tsubota, Toshio; Nishida, Toshisada; Iwaki, Takashi
Parasitological surveillance in primates has been performed using coprological observation and identification of specimens from chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania (Mahale). In this study, we conducted coprological surveillance to identify the fauna of parasite infection in five primate species in Mahale: red colobus (Procolobus badius tephrosceles), red-tailed monkeys (Cercopithecus ascanius schmidti), vervet monkeys (Cercopithecus aethiops pygerythrus), yellow baboons (Papio cynocephalus), and chimpanzees. Fecal samples were examined microscopically, and parasite identification was based on the morphology of cysts, eggs, larvae, and adult worms. Three nematodes (Oesophagostomum spp., Strongyloides sp., and Trichuris sp.), Entamoeba coli, and Entamoeba spp. were found in all five primate species. The following infections were identified: Bertiella studeri was found in chimpanzees and yellow baboons; Balantidium coli was found in yellow baboons; three nematodes (Streptopharagus, Primasubulura, an undetermined genus of Spirurina) and Dicrocoeliidae gen. sp. were found in red-tailed monkeys, vervet monkeys, and yellow baboons; Chitwoodspirura sp. was newly identified in red colobus and red-tailed monkeys; Probstmayria gombensis and Troglocorys cava were newly identified in chimpanzees, together with Troglodytella abrassarti; and Enterobius sp. was newly identified in red colobus. The parasitological data reported for red colobus, vervet monkeys, and yellow baboons in Mahale are the first reports for these species.
Samuel D Sibley
Full Text Available Within the Flaviviridae, the recently designated genus Pegivirus has expanded greatly due to new discoveries in bats, horses, and rodents. Here we report the discovery and characterization of three simian pegiviruses (SPgV that resemble human pegivirus (HPgV and infect red colobus monkeys (Procolobus tephrosceles, red-tailed guenons (Cercopithecus ascanius and an olive baboon (Papio anubis. We have designated these viruses SPgVkrc, SPgVkrtg and SPgVkbab, reflecting their host species' common names, which include reference to their location of origin in Kibale National Park, Uganda. SPgVkrc and SPgVkrtg were detected in 47% (28/60 of red colobus and 42% (5/12 red-tailed guenons, respectively, while SPgVkbab infection was observed in 1 of 23 olive baboons tested. Infections were not associated with any apparent disease, despite the generally high viral loads observed for each variant. These viruses were monophyletic and equally divergent from HPgV and pegiviruses previously identified in chimpanzees (SPgVcpz. Overall, the high degree of conservation of genetic features among the novel SPgVs, HPgV and SPgVcpz suggests conservation of function among these closely related viruses. Our study describes the first primate pegiviruses detected in Old World monkeys, expanding the known genetic diversity and host range of pegiviruses and providing insight into the natural history of this genus.
McGraw, W Scott; van Casteren, Adam; Kane, Erin; Geissler, Elise; Burrows, Brittany; Daegling, David J
We collected frequency data on oral processing behaviors during feeding in habituated groups of Western red colobus, Piliocolobus badius, and Western black and white, Colobus polykomos, ranging in the Ivory Coast's Tai National Park. During the sampling period, the diet of red colobus consisted of approximately 75% leaves compared to approximately 47% leaves and buds in black and white colobus. Black and white colobus chewed more frequently per ingestive event than did red colobus. Black and white colobus also employed their anterior teeth much more frequently than did red colobus, a difference attributed to the frequent consumption by C. polykomos of Pentaclethra macrophylla seeds and pods. A material analysis of these food items reveals that both the seed coating and seed flesh are quite soft; however, the pod housing the seeds is very tough. We argue that the pod's toughness, geometry, and fiber orientation collectively result in a food that is very difficult to process, resulting in long handling times and frequent, aggressive use of the incisors. We compare these data with those collected on another Tai primate-the sooty mangabey, Cercocebus atys-and demonstrate that during feeding, both colobine species use their incisors less than the mangabey, but that the cercopithecine chews less than either colobine. Combining data on oral processing behaviors with those on the material properties of items being ingested should lead to more informed interpretations of dentognathic morphology. Copyright © 2015 Elsevier Ltd. All rights reserved.
Murthy, Sripriya; Couacy-Hymann, Emmanuel; Metzger, Sonja; Nowak, Kathrin; De Nys, Helene; Boesch, Christophe; Wittig, Roman; Jarvis, Michael A; Leendertz, Fabian H; Ehlers, Bernhard
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.
Bonnell, Tyler R; Campennì, Marco; Chapman, Colin A; Gogarten, Jan F; Reyna-Hurtado, Rafael A; Teichroeb, Julie A; Wasserman, Michael D; Sengupta, Raja
The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus), testing for: the effects of memory type (Euclidian or landmark based), amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led). Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group's step length, whereas the type of memory had the highest impact on a group's path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.
Tyler R Bonnell
Full Text Available The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus, testing for: the effects of memory type (Euclidian or landmark based, amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led. Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group's step length, whereas the type of memory had the highest impact on a group's path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.
Chapman, Colin A; Schoof, Valérie A M; Bonnell, Tyler R; Gogarten, Jan F; Calmé, Sophie
Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.
Milich, Krista M; Stumpf, Rebecca M; Chambers, Josephine M; Chapman, Colin A
Behavioral flexibility allows primates to cope with environmental variability. Quantifying primate responses to human habitat modifications allows an effective means of assessing coping mechanisms. Within Kibale National Park, Uganda, logging led to reduced primate food availability that still exists almost 50 years after the harvest. Following the predictions of the ideal free distribution theory, primate densities are expected to decrease in areas of lower resource availability so that the resources available per individual are equivalent in logged and old-growth areas. However, counter to what would be predicted by the ideal free distribution theory, red colobus monkeys (Procolobus rufomitratus) occur at similar densities in logged and old-growth areas of Kibale. This suggests that either the ecological differences between the two areas are not sufficient to impact red colobus densities or that animals in logged areas are compensating to changes in resource availability by using different foraging strategies. To test between these hypotheses, we examined four groups of red colobus, two in logged and two in old-growth forests, and compared feeding behavior, feeding tree size, and tree productivity. Females in logged areas fed on resources from a greater number of plant species, fed on fewer resources from each species, and spent more time feeding than those in old-growth areas. By expanding their diet, females in logged areas effectively increased the resources available to them, which may contribute to their ability to maintain similar densities to females in old-growth areas. These findings have implications for an evolutionary understanding of how species deal with environmental change and considerations for conservation practices that determine what areas should be prioritized for protection.
Rothman, Jessica M; Chapman, Colin A; Twinomugisha, Dennis; Wasserman, Michael D; Lambert, Joanna E; Goldberg, Tony L
Physical traits, such as body size, and processes like growth can be used as indices of primate health and can add to our understanding of life history and behavior. Accurately measuring physical traits in the wild can be challenging because capture is difficult, disrupts animals, and may cause injury. To measure physical traits of arboreal primates remotely, we adapted a parallel laser technique that has been used with terrestrial and marine mammals. Two parallel lasers separated by a known distance (4 cm) and mounted onto a digital camera are projected onto an animal. When a photograph is taken, the laser projections on the target provide a scale bar. We validated the technique for measuring the physical traits of identifiable red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda. First, we photographed the tails of monkeys with laser projections and compared these with measurements previously obtained when the animals were captured. Second, we manually measured the distance between two markers placed on tree branches at similar heights to those used by monkeys, and compared them with the measurements obtained through digital photographs of the markers with parallel laser projections. The mean tail length of the monkeys via manual measurements was 63.3+/-4.4 cm, and via remote measurements was 63.0+/-4.1 cm. The mean distance between the markers on tree branches via manual measurements was 13.8+/-3.59 cm, and via remote measurements was 13.9+/-3.58 cm. The mean error using parallel lasers was 1.7% in both cases. Although the needed precision will depend on the question asked, our results suggest that sufficiently precise measurements of physical traits or substrates of arboreal primates can be obtained remotely using parallel lasers.
Wasserman, Michael D; Taylor-Gutt, Alexandra; Rothman, Jessica M; Chapman, Colin A; Milton, Katharine; Leitman, Dale C
Phytoestrogens, or naturally occurring estrogen-mimicking compounds, are found in many human plant foods, such as soybeans (Glycine max) and other legumes. Because the consumption of phytoestrogens may result in both health benefits of protecting against estrogen-dependent cancers and reproductive costs of disrupting the developing endocrine system, considerable biomedical research has been focused on the physiological and behavioral effects of these compounds. Despite this interest, little is known about the occurrence of phytoestrogens in the diets of wild primates, nor their likely evolutionary importance. We investigated the prevalence of estrogenic plant foods in the diets of two folivorous primate species, the red colobus monkey (Procolobus rufomitratus) of Kibale National Park and mountain gorilla (Gorilla beringei) of Bwindi Impenetrable National Park, both in Uganda. To examine plant foods for estrogenic activity, we screened 44 plant items (species and part) comprising 78.4% of the diet of red colobus monkeys and 53 plant items comprising 85.2% of the diet of mountain gorillas using transient transfection assays. At least 10.6% of the red colobus diet and 8.8% of the gorilla diet had estrogenic activity. This was mainly the result of the red colobus eating three estrogenic staple foods and the gorillas eating one estrogenic staple food. All estrogenic plants exhibited estrogen receptor (ER) subtype selectivity, as their phytoestrogens activated ERβ, but not ERα. These results demonstrate that estrogenic plant foods are routinely consumed by two folivorous primate species. Phytoestrogens in the wild plant foods of these two species and many other wild primates may have important implications for understanding primate reproductive ecology.
Ria R Ghai
Full Text Available INTRODUCTION: Soil-transmitted helminths (STHs are a major health concern in tropical and sub-tropical countries. Oesophagostomum infection is considered endemic to West Africa but has also been identified in Uganda, East Africa, among primates (including humans. However, the taxonomy and ecology of Oesophagostomum in Uganda have not been studied, except for in chimpanzees (Pan troglodytes, which are infected by both O. bifurcum and O. stephanostomum. METHODS AND FINDINGS: We studied Oesophagostomum in Uganda in a community of non-human primates that live in close proximity to humans. Prevalence estimates based on microscopy were lower than those based on polymerase chain reaction (PCR, indicating greater sensitivity of PCR. Prevalence varied among host species, with humans and red colobus (Procolobus rufomitratus infected at lowest prevalence (25% and 41% by PCR, respectively, and chimpanzees, olive baboons (Papio anubis, and l'hoest monkeys (Cercopithecus lhoesti infected at highest prevalence (100% by PCR in all three species. Phylogenetic regression showed that primates travelling further and in smaller groups are at greatest risk of infection. Molecular phylogenetic analyses revealed three cryptic clades of Oesophagostomum that were not distinguishable based on morphological characteristics of their eggs. Of these, the clade with the greatest host range had not previously been described genetically. This novel clade infects humans, as well as five other species of primates. CONCLUSIONS: Multiple cryptic forms of Oesophagostomum circulate in the people and primates of western Uganda, and parasite clades differ in host range and cross-species transmission potential. Our results expand knowledge about human Oesophagostomum infection beyond the West African countries of Togo and Ghana, where the parasite is a known public health concern. Oesophagostomum infection in humans may be common throughout Sub-Saharan Africa, and the transmission of
Mbora, David N M; McPeek, Mark A
1. Habitat loss and fragmentation are the principal causes of the loss of biological diversity. In addition, parasitic diseases are an emerging threat to many animals. Nevertheless, relatively few studies have tested how habitat loss and fragmentation influence the prevalence and richness of parasites in animals. 2. Several studies of nonhuman primates have shown that measures of human activity and forest fragmentation correlate with parasitism in primates. However, these studies have not tested for the ecological mechanism(s) by which human activities or forest fragmentation influence the prevalence and richness of parasites. 3. We tested the hypothesis that increased host density due to forest fragmentation and loss mediates increases in the prevalence and richness of gastrointestinal parasites in two forest primates, the Tana River red colobus (Procolobus rufomitratus, Peters 1879) and mangabey (Cercocebus galeritus galeritus, Peters 1879). We focused on population density because epidemiological theory states that host density is a key determinant of the prevalence and richness of directly transmitted parasites in animals. 4. The Tana River red colobus and mangabey are endemic to a highly fragmented forest ecosystem in eastern Kenya where habitat changes are caused by a growing human population increasingly dependent on forest resources and on clearing forest for cultivation. 5. We found that the prevalence of parasites in the two monkeys was very high compared to primates elsewhere. Density of monkeys was positively associated with forest area and disturbance in forests. In turn, the prevalence and richness of parasites was significantly associated with monkey density, and attributes indicative of human disturbance in forests. 6. We also found significant differences in the patterns of parasitism between the colobus and the mangabey possibly attributable to differences in their behavioural ecology. Colobus are arboreal folivores while mangabeys are terrestrial