Abstract :
[en] Human-induced transformations, including habitat conversion, urban
expansion, and intensified activities in natural habitats, increasingly foster close
encounters between humans and wildlife, raising the risk of zoonotic and
anthropozoonotic disease transmission. This is particularly relevant for non-human
primates, which occupy interfaces along an anthropogenic gradient from forests to
urban contexts. Moreover, due to their close phylogenetic and physiological similarity
to humans, primates are highly susceptible to shared same pathogens. As a result,
human-primate interfaces represent critical hotspots for predicting infectious disease
emergence on a global scale. Yet, despite growing recognition of these risks,
systematic data on infectious diseases in wild primates remain limited, with studies
unevenly distributed across primates’ geographical range and often methodologically
constrained. Moreover, the combined influence of host social structure and features
of human-primate interactions on cross-species transmission is still insufficiently
understood. To improve current knowledge of infectious disease dynamics at the
human-primate interface, this thesis investigates zoonotic pathogens in a synanthropic
population of long-tailed macaques (Macaca fascicularis) in Bali, assessing both
infection risk factors in macaques and modeling the risk for disease transmission to
humans.
To provide a comprehensive overview of zoonotic pathogens identified in
wild Asian primates so far, the first chapter of this thesis presents a systematic review
of reported infections across species. In this systematic review, we synthesized current
evidence on the diversity of zoonotic pathogens, including viruses, bacteria, protozoa,
helminths, and fungi, reported in wild Asian primates, together with their transmission
modes and ecological contexts of occurrence. Through this effort, our analysis
revealed strong taxonomic biases in existing research, with disproportionate attention
directed toward certain primate hosts, particularly the genus Macaca sp., and specific
pathogen groups such as protozoa and helminths. This focus reflects broader
methodological constraints, as the types of samples and diagnostic techniques most
often used tend to favor the detection of gastrointestinal parasites, thereby
overrepresenting pathogens transmitted via the fecal-oral route while
underrepresenting other transmission pathways. By consolidating fragmented
information, this chapter not only identifies priority gaps in the current literature but
also provides the rationale and framework for the empirical screening presented in the
following chapters.
Building on the knowledge gaps identified in the review, the second chapter
reports an empirical screening of zoonotic pathogens in one highly synanthropic long
tailed macaque population inhabiting the Ubud Monkey Forest, Bali. The screening
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design was directly informed by the review, prioritizing both well-reported agents
likely to occur and understudied pathogens. Using a combination of sample types
(blood, nasal swabs, and feces) and complementary diagnostic approaches, including
serological (ELISA tests) and molecular (qPCRs) assays, this integrative screening
strategy allowed us to capture different time windows of infection. It also maximizes
detection across multiple transmission pathways, covering pathogens transmitted via
respiratory (e.g., SARS-CoV-2), fecal-oral (e.g., Rotavirus A), fluid-borne (e.g.,
Herpes B virus), and vector-borne routes (e.g., Dengue virus). The screening revealed
high seroprevalence for several pathogens, particularly Herpes B virus (95% of
individuals tested), Measles morbillivirus (32%), and Rotavirus A (65%), the latter of
which was subsequently selected for quantitative risk modeling in the last chapter.
Beyond this targeted approach, this chapter also coincided with an unexpected fatal
outbreak of Streptococcus equi subsp. zooepidemicus in our study long-tailed
macaque population. We therefore took the opportunity to document the demographic
impacts of this epizootic event and to provide rare insights into bacterial outbreaks in
wild primates, underscoring the value of systematic pathogen monitoring in
synanthropic primate populations.
Because infection risk factors in primates are key to understanding host
pathogen dynamics, the third chapter investigates how host characteristics, social
network position (in grooming network), and human-macaque interaction frequency
predict the richness and presence of gastrointestinal parasite in synanthropic long
tailed macaques living in a high-tourist hotspot. Using direct smear, flotation
techniques, and light microscopy, we measured parasite richness and presence from
opportunistically collected fecal samples on 53 focal individuals gathered over an
extended period (16 months). Combined with behavioral data collected using focal
animal sampling (772 hours of data), we analyzed the influence of individual social
network metrics, dominance rank, sex, and the frequency of human-macaque
interactions on the richness of gastrointestinal parasites and the presence of specific
taxa. We found that individuals with higher social centrality harbored lower parasite
richness, suggesting a potential buffering effect of sociality. Alternatively, this pattern
may also reflect confounding factors such as age-related immune differences that
influence parasitism independently of social exposure. In addition to this overall
association, protozoan taxa showed species-specific patterns linked to particular traits.
For instance, the presence of Iodamoeba sp. increased with the frequency of human
macaque interactions, whereas helminths were not associated with any social or
individual risk factors, underscoring the taxa-specific nature of parasite transmission..
This contrast highlights how differences in parasite life-history traits shape
transmission dynamics and the importance of integrating parasite ecology with host
social context when assessing infection risk at human-primate interfaces.
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In contrast to the previous focus on infection risk in macaques, the fourth
chapter shifts the perspective from host infection risks in macaques to zoonotic
transmission risks for humans. To this end, we developed a stochastic probabilistic
model to estimate the probability of Rotavirus A transmission from macaques to
humans at the Ubud Monkey Forest site in Bali. The model was based on serological
evidence of high Rotavirus A prevalence in macaques, as detected in the previous
chapter. We combined field observations, expert elicitation, and literature data to
parameterize fecal-oral transmission pathways of this virus. The probability of human
infection per visit was estimated at 3.5 × 10⁻³, which appears low at the individual
level but becomes significant when accumulated over the very large number of
visitors to the site (3,500-4,400/day). Environmental and behavioral exposure
parameters, particularly visitor contact with contaminated surfaces and subsequent
hand-to-face contact, emerged as the main drivers of risk. Risk mitigation scenarios
tested in the model highlighted the effectiveness of hand hygiene promotion and the
discontinuation of high-risk practices such as “monkey selfies”. This chapter
illustrates how quantitative risk modeling can serve as a decision-support tool for site
managers, helping to guide context-specific prevention strategies within a One Health
framework, while also offering a transferable framework applicable to other fecal-oral
pathogens in similar contexts of human-primate interactions.
Overall, this thesis adopts an integrated approach to infectious disease risks
at human-primate interfaces, combining a systematic review, empirical pathogen
screening, social network analyses, and quantitative risk modeling. By bringing
together multiple methodological perspectives, it highlights both the diversity of
zoonotic agents circulating in synanthropic long-tailed macaques, as well as the host
and behavioral factors that influence their infection status. Beyond empirical insights,
this work provides a transferable modeling framework to anticipate zoonotic risks and
evaluate prevention strategies in urban and touristic contexts. Taken together, these
findings underscore the value of the interdisciplinary One Health approach for
strengthening surveillance and guiding management strategies at urban human
primate interfaces, thereby promoting safer and more sustainable coexistence between
humans and wildlife.
