Thomas R. Gillespie

Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model

Abstract. The ecological-constraints model proposes that increased group size increases within-group feeding competition, necessitating increased travel and, consequently, constraining group size. Previous studies have supported the model for frugivores, but its applicability to folivores remains untested. This study evaluated the generality of the model by re-examining the relationship between day range and group size for a folivorous species for which published accounts have not found a relationship between these factors. This study differs from earlier studies by accounting for variation in food availability, which may drive changes in day range. We quantified the relationships among food availability, day range, and group size for two red colobus groups at Kibale National Park, Uganda. Mean day range and home range were significantly greater for the group of 48 individuals compared to the group of 24 individuals. The large group traveled more and rested less than the small group. The large group also traveled more rapidly than the small group. Food availability significantly predicted mean day range for the large group, but not for the small group. Analyses of covariance demonstrated that the large and small group responded differently to changes in food availability. These observations suggest that the large red colobus group experiences greater levels of within-group feeding competition than the small group. This study provides added support for the generality of the ecological-constraints model and contributes toward an understanding of the mechanisms controlling feeding competition and social organization in primates.

Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates

Recent evidence of emerging human diseases with origins or likely transmission to humans, or both, that involve primates and a greater recognition of the risk of human pathogen transmission to free-ranging primates have raised awareness of the potential impact of zoonotic pathogen transmission on primate conservation and nonhuman primate and human health. As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitats, greater human-primate contact is inevitable and even higher rates of pathogen transmission are likely. Thus interest has grown in collecting baseline data on patterns of parasitic infections in wild primate populations to provide an index of population health and to begin to assess and, to manage disease risks. Primatologists traditionally have been involved with such surveys through noninvasive assessment of gastrointestinal parasites. Unfortunately, previous studies have tended toward divergent methodologies, compromising the potential for longitudinal and comparative work. Here, I provide practical guidelines and standardized methodologies for the noninvasive assessment of gastrointestinal parasites of primates.

Scale Issues in the Study of Primate Foraging: Red Colobus of Kibale National Park

Abstract Diet data have been used to address a number of theoretical issues. We often calculate the proportion of time spent eating different foods (e.g., fruits, leaves) to place species into dietary categories and contrast morphological or behavioral traits among categories. Yet we have little understanding of how flexible species can be in terms of the plant parts and species consumed. To address this issue, we analyzed data on the diets of red colobus monkeys (Procolobus badius) from Kibale National Park, Uganda, to evaluate temporal and spatial variability in the plant parts and species eaten. After considering observer differences and sampling issues, we evaluated how different a groups diet could be if samples were taken in different years. We found that the diet of the same groups showed significant, consistent changes over a 4‐year period. For example, the time spent feeding on leaves increased from 56% in 1994 to 76% in 1998. The plant parts and species eaten by eight groups inhabiting different types of forest (e.g., pristine, logged, riverine) varied among groups. The largest interdemic difference was seen in the use of young leaves (38%). Dietary differences were also found between groups with overlapping home ranges (41–49% overlap). Different subspecies of Procolobus badius also varied in diet; however, this variation was often not of the magnitude documented within Kibale for the same population. The fact that diet can vary considerably over small spatial and short temporal scales within the same species raises the intriguing question as to what level of interspecific difference is biologically significant for addressing particular questions. We conclude that behavioral flexibility blurs our traditional stereotypic assessment of primates; a study of one group that occupies a specific habitat at one point in time may not adequately represent the species. Am J Phys Anthropol 117:349–363, 2002.

Forest Fragmentation as Cause of Bacterial Transmission among Nonhuman Primates, Humans, and Livestock, Uganda

Anthropogenic disturbance increases bacterial transmission.

Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda.

Habitat overlap can increase the risks of anthroponotic and zoonotic pathogen transmission between humans, livestock, and wild apes. We collected Escherichia coli bacteria from humans, livestock, and mountain gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, from May to August 2005 to examine whether habitat overlap influences rates and patterns of pathogen transmission between humans and apes and whether livestock might facilitate transmission. We genotyped 496 E. coli isolates with repetitive extragenic palindromic polymerase chain reaction fingerprinting and measured susceptibility to 11 antibiotics with the disc-diffusion method. We conducted population genetic analyses to examine genetic differences among populations of bacteria from different hosts and locations. Gorilla populations that overlapped in their use of habitat at high rates with people and livestock harbored E. coli that were genetically similar to E. coli from those people and livestock, whereas E. coli from gorillas that did not overlap in their use of habitats with people and livestock were more distantly related to human or livestock bacteria. Thirty-five percent of isolates from humans, 27% of isolates from livestock, and 17% of isolates from gorillas were clinically resistant to at least one antibiotic used by local people, and the proportion of individual gorillas harboring resistant isolates declined across populations in proportion to decreasing degrees of habitat overlap with humans. These patterns of genetic similarity and antibiotic resistance among E. coli from populations of apes, humans, and livestock indicate that habitat overlap between species affects the dynamics of gastrointestinal bacterial transmission, perhaps through domestic animal intermediates and the physical environment. Limiting such transmission would benefit human and domestic animal health and ape conservation.

Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda.

Background Giardia duodenalis is prevalent in tropical settings where diverse opportunities exist for transmission between people and animals. We conducted a cross-sectional study of G. duodenalis in people, livestock, and wild primates near Kibale National Park, Uganda, where human-livestock-wildlife interaction is high due to habitat disturbance. Our goal was to infer the cross-species transmission potential of G. duodenalis using molecular methods and to investigate clinical consequences of infection. Methodology/Principal Findings Real-time PCR on DNA extracted from fecal samples revealed a combined prevalence of G. duodenalis in people from three villages of 44/108 (40.7%), with prevalence reaching 67.5% in one village. Prevalence rates in livestock and primates were 12.4% and 11.1%, respectively. Age was associated with G. duodenalis infection in people (higher prevalence in individuals ≤15 years) and livestock (higher prevalence in subadult versus adult animals), but other potential risk factors in people (gender, contact with domestic animals, working in fields, working in forests, source of drinking water, and medication use) were not. G. duodenalis infection was not associated with gastrointestinal symptoms in people, nor was clinical disease noted in livestock or primates. Sequence analysis of four G. duodenalis genes identified assemblage AII in humans, assemblage BIV in humans and endangered red colobus monkeys, and assemblage E in livestock and red colobus, representing the first documentation of assemblage E in a non-human primate. In addition, genetic relationships within the BIV assemblage revealed sub-clades of identical G. duodenalis sequences from humans and red colobus. Conclusions/Significance Our finding of G. duodenalis in people and primates (assemblage BIV) and livestock and primates (assemblage E) underscores that cross-species transmission of multiple G. duodenalis assemblages may occur in locations such as western Uganda where people, livestock, and primates overlap in their use of habitat. Our data also demonstrate a high but locally variable prevalence of G. duodenalis in people from western Uganda, but little evidence of associated clinical disease. Reverse zoonotic G. duodenalis transmission may be particularly frequent in tropical settings where anthropogenic habitat disturbance forces people and livestock to interact at high rates with wildlife, and this could have negative consequences for wildlife conservation.

GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF UGANDA

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda—the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)—to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.

Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health.

The close phylogenetic relationship between humans and nonhuman primates, coupled with the exponential expansion of human populations and human activities within primate habitats, has resulted in exceptionally high potential for pathogen exchange. Emerging infectious diseases are a consequence of this process that has the capacity to threaten global health and drive primate population declines. Integration of standardized empirical data collection, state-of-the-art diagnostics, and the comparative approach offers the opportunity to create a baseline for patterns of infection in wild primate populations; to better understand the role of disease in primate ecology, behavior, and evolution; and to examine how anthropogenic effects alter the zoonotic potential of various pathogenic organisms. We review these technologies and approaches, including noninvasive sampling in field conditions, and we identify ways in which integrative research activities are likely to fuel future discoveries in primate disease ecology. In addition to considering applied aspects of disease research in primate health and conservation, we review how these approaches are shedding light on parasite biodiversity and the drivers of disease risk across primate species.

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Wild great apes as sentinels and sources of infectious disease

Emerging zoonotic infectious diseases pose a serious threat to global health. This is especially true in relation to the great apes, whose close phylogenetic relationship with humans results in a high potential for microorganism exchange. In this review, we show how studies of the microorganisms of wild great apes can lead to the discovery of novel pathogens of importance for humans. We also illustrate how these primates, living in their natural habitats, can serve as sentinels for outbreaks of human disease in regions with a high likelihood of disease emergence. Greater sampling efforts and improvements in sample preservation and diagnostic capacity are rapidly improving our understanding of the diversity and distribution of microorganisms in wild great apes. Linking non-invasive diagnostic data with observational health data from great apes habituated to human presence is a promising approach for the discovery of pathogens of high relevance for humans.