Epidemiological study of zoonoses derived from humans in captive chimpanzees

Emerging infectious diseases (EIDs) in wildlife are major threats both to human health and to biodiversity conservation. An estimated 71.8 % of zoonotic EID events are caused by pathogens in wildlife and the incidence of such diseases is increasing significantly in humans. In addition, human diseases are starting to infect wildlife, especially non-human primates. The chimpanzee is an endangered species that is threatened by human activity such as deforestation, poaching, and human disease transmission. Recently, several respiratory disease outbreaks that are suspected of having been transmitted by humans have been reported in wild chimpanzees. Therefore, we need to study zoonotic pathogens that can threaten captive chimpanzees in primate research institutes. Serological surveillance is one of several methods used to reveal infection history. We examined serum from 14 captive chimpanzees in Japanese primate research institutes for antibodies against 62 human pathogens and 1 chimpanzee-borne infectious disease. Antibodies tested positive against 29 pathogens at high or low prevalence in the chimpanzees. These results suggest that the proportions of human-borne infections may reflect the chimpanzee’s history, management system in the institute, or regional epidemics. Furthermore, captive chimpanzees are highly susceptible to human pathogens, and their induced antibodies reveal not only their history of infection, but also the possibility of protection against human pathogens.     

From molecules to dynamic biological communities

Microbial ecology is flourishing, and in the process, is making contributions to how the ecology and biology of large organisms is understood. Ongoing advances in sequencing technology and computational methods have enabled the collection and analysis of vast amounts of molecular data from diverse biological communities. While early studies focused on cataloguing microbial biodiversity in environments ranging from simple marine ecosystems to complex soil ecologies, more recent research is concerned with community functions and their dynamics over time. Models and concepts from traditional ecology have been used to generate new insight into microbial communities, and novel system-level models developed to explain and predict microbial interactions. The process of moving from molecular inventories to functional understanding is complex and challenging, and never more so than when many thousands of dynamic interactions are the phenomena of interest. We outline the process of how epistemic transitions are made from producing catalogues of molecules to achieving functional and predictive insight, and show how those insights not only revolutionize what is known about biological systems but also about how to do biology itself. Examples will be drawn primarily from analyses of different human microbiota, which are the microbial consortia found in and on areas of the human body, and their associated microbiomes (the genes of those communities). Molecular knowledge of these microbiomes is transforming microbiological knowledge, as well as broader aspects of human biology, health and disease.     

Primate dental ecology: How teeth respond to the environment

Teeth are central for the study of ecology, as teeth are at the direct interface between an organism and its environment. Recent years have witnessed a rapid growth in the use of teeth to understand a broad range of topics in living and fossil primate biology. This in part reflects new techniques for assessing ways in which teeth respond to, and interact with, an organism's environment. Long-term studies of wild primate populations that integrate dental analyses have also provided a new context for understanding primate interactions with their environments. These new techniques and long-term field studies have allowed the development of a new perspective-dental ecology. We define dental ecology as the broad study of how teeth respond to, or interact with, the environment. This includes identifying patterns of dental pathology and tooth use-wear, as they reflect feeding ecology, behavior, and habitat variation, including areas impacted by anthropogenic disturbance, and how dental development can reflect environmental change and/or stress. The dental ecology approach, built on collaboration between dental experts and ecologists, holds the potential to provide an important theoretical and practical framework for inferring ecology and behavior of fossil forms, for assessing environmental change in living populations, and for understanding ways in which habitat impacts primate growth and development. This symposium issue brings together experts on dental morphology, growth and development, tooth wear and health, primate ecology, and paleontology, to explore the broad application of dental ecology to questions of how living and fossil primates interact with their environments.     

Rethinking Human–Nonhuman Primate Contact and Pathogenic Disease Spillover

Zoonotic transmissions are a major global health risk, and human–animal contact is frequently raised as an important driver of transmission. A literature examining zooanthroponosis largely agrees that more human–animal contact leads to more risk. Yet the basis of this proposition, the term contact, has not been rigorously analyzed. To understand how contact is used to explain cross-species spillovers, we conducted a multi-disciplinary review of studies addressing human–nonhuman primate (NHP) engagements and pathogenic transmissions and employing the term contact. We find that although contact is frequently invoked, it is employed inconsistently and imprecisely across these studies, overlooking the range of pathogens and their transmission routes and directions. We also examine a related but more expansive approach focusing on human and NHP habitats and their spatial overlap, which can potentially facilitate pathogenic transmission. Contact and spatial overlap investigations cannot, however, explain the processes that bring together people, animals and pathogens. We therefore examine another approach that enhances our understanding of zoonotic spillovers: anthropological studies identifying such historical, social, environmental processes. Comparable to a One Health approach, our ongoing research in Cameroon draws contact, spatial overlap and anthropological–historical approaches into dialog to suggest where, when and how pathogenic transmissions between people and NHPs may occur. In conclusion, we call for zoonotic disease researchers to specify more precisely the human–animal contacts they investigate and to attend to how broader ecologies, societies and histories shape pathogen–human–animal interactions.     

Primates and the Ecology of their Infectious Diseases: How will Anthropogenic Change Affect Host‐Parasite Interactions?

The sudden appearance of diseases like SARS (severe acute respiratory syndrome 1 ), the devastating impacts of diseases like Ebola on both human and wildlife communities, 2 , 3 and the immense social and economic costs created by viruses like HIV 4 underscore our need to understand the ecology of infectious diseases. Given that monkeys and apes often share parasites with humans, understanding the ecology of infectious diseases in nonhuman primates is of paramount importance. This is well illustrated by the HIV viruses, the causative agents of human AIDS, which evolved recently from related viruses of chimpanzees (Pan troglodytes) and sooty mangabeys (Cercocebus atys 5 ), as well as by the outbreaks of Ebola virus, which trace their origins to zoonotic transmissions from local apes. 6 A consideration of how environmental change may promote contact between humans and nonhuman primates and thus increase the possibility of sharing infectious diseases detrimental to humans or nonhuman primates is now paramount in conservation and human health planning.     

The Role of Ecotones in Emerging Infectious Diseases

Recognition of the significance of the boundary between ecological systems, often referred to as the ecotone, has a long history in the ecological sciences and in zoonotic disease research. More recent research in landscape ecology has produced an expanded view of ecotones and elaboration of their characteristics and functions in ecosystems. Parallel research on emerging infectious diseases (EIDs) and the causes of increased rates of pathogen transmission, spread, and adaptation suggests a correspondence between ecotonal processes and the ecological and evolutionary processes responsible for zoonotic and vector-borne emerging infections. A review of the literature suggests that ecotones play a role in a number of the most important EIDs. Yet these are the only diseases for which specific landscape ecological information exists in the literature or disease reports. However, the similar disease ecologies of these with about half of the approximately 130 zoonotic EIDs suggests ecotones, particularly their anthropogenic origination or modification, may be generally associated with ecotones and the global trend of increasing EIDs.     

Cross-Species Pathogen Transmission and Disease Emergence in Primates

Many of the most virulent emerging infectious diseases in humans, e.g., AIDS and Ebola, are zoonotic, having shifted from wildlife populations. Critical questions for predicting disease emergence are: (1) what determines when and where a disease will first cross from one species to another, and (2) which factors facilitate emergence after a successful host shift. In wild primates, infectious diseases most often are shared between species that are closely related and inhabit the same geographic region. Therefore, humans may be most vulnerable to diseases from the great apes, which include chimpanzees and gorillas, because these species represent our closest relatives. Geographic overlap may provide the opportunity for cross-species transmission, but successful infection and establishment will be determined by the biology of both the host and pathogen. We extrapolate the evolutionary relationship between pathogen sharing and divergence time between primate species to generate “hotspot” maps, highlighting regions where the risk of disease transfer between wild primates and from wild primates to humans is greatest. We find that central Africa and Amazonia are hotspots for cross-species transmission events between wild primates, due to a high diversity of closely related primate species. Hotspots of host shifts to humans will be most likely in the forests of central and west Africa, where humans come into frequent contact with their wild primate relatives. These areas also are likely to sustain a novel epidemic due to their rapidly growing human populations, close proximity to apes, and population centers with high density and contact rates among individuals.     

Phylogenetic host specificity and understanding parasite sharing in primates

Understanding how parasites are transmitted to new species is of great importance for human health, agriculture and conservation. However, it is still unclear why some parasites are shared by many species, while others have only one host. Using a new measure of ‘phylogenetic host specificity’, we find that most primate parasites with more than one host are phylogenetic generalists, infecting less closely related primates than expected. Evolutionary models suggest that phylogenetic host generalism is driven by a mixture of host–parasite cospeciation and lower rates of parasite extinction. We also show that phylogenetic relatedness is important in most analyses, but fails to fully explain patterns of parasite sharing among primates. Host ecology and geographical distribution emerged as key additional factors that influence contacts among hosts to facilitate sharing. Greater understanding of these factors is therefore crucial to improve our ability to predict future infectious disease risks.     

Nonhuman primate quarantine: its evolution and practice

Nonhuman primates (NHPs) are imported to the United States for use in research, domestic breeding, and propagation of endangered populations in zoological gardens. During the past 60 years, individuals responsible for NHP importation programs have observed morbidity and mortality typically associated with infectious disease outbreaks. These outbreaks have included infectious agents such as tuberculosis, Herpesvirus sp., simian hemorrhagic fever, and filovirus infections such as the Ebola and Marburg viruses. Some outbreaks have affected both animal and human populations. These epizootics are attributable to a variety of factors, including increased population density, exposure of na?ve populations to new infectious agents, and stress. The practice of quarantining animals arriving in the United States was first applied by individual research programs to improve animal health and ensure the quality of animals entering research programs. The development of government regulations for nonhuman primate quarantine accompanied the recognition that imported NHPs could pose a risk to public health. This article briefly reviews the history of US NHP importation and the factors behind the development of NHP quarantine regulations. The focus is on regulations concerned with infectious disease, public health, and the health of domestic primate colonies. These regulations have had the dual benefit of protecting public health as well as reducing animal morbidity and mortality during importation and quarantine. We review current practices and facilities for nonhuman primate quarantine and identify challenges for the future.     

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.

New Routes to Phylogeography: A Bayesian Structured Coalescent Approximation

Phylogeographic methods aim to infer migration trends and the history of sampled lineages from genetic data. Applications of phylogeography are broad, and in the context of pathogens include the reconstruction of transmission histories and the origin and emergence of outbreaks. Phylogeographic inference based on bottom-up population genetics models is computationally expensive, and as a result faster alternatives based on the evolution of discrete traits have become popular. In this paper, we show that inference of migration rates and root locations based on discrete trait models is extremely unreliable and sensitive to biased sampling. To address this problem, we introduce BASTA (BAyesian STructured coalescent Approximation), a new approach implemented in BEAST2 that combines the accuracy of methods based on the structured coalescent with the computational efficiency required to handle more than just few populations. We illustrate the potentially severe implications of poor model choice for phylogeographic analyses by investigating the zoonotic transmission of Ebola virus. Whereas the structured coalescent analysis correctly infers that successive human Ebola outbreaks have been seeded by a large unsampled non-human reservoir population, the discrete trait analysis implausibly concludes that undetected human-to-human transmission has allowed the virus to persist over the past four decades. As genomics takes on an increasingly prominent role informing the control and prevention of infectious diseases, it will be vital that phylogeographic inference provides robust insights into transmission history.     

A Model for Defining West Nile Virus Risk Perception Based on Ecology and Proximity

West Nile virus (WNV) has made considerable impact as an emerging infectious disease, spreading from coast to coast across North America since 1999. The disease has exhibited great spatial variability in North America, making an ecosystems approach to understanding the local human and vector ecology critical to prevention and control. This study underscores the importance of employing both personal prevention and community participatory approaches to create messages that have been adapted to the local ecology and are designed to reduce the risk of human infection with this mosquito-borne virus. As the virus spreads into new areas, underlying attitudes toward mosquitoes and the local perception of environment/ecology can affect the success of control and prevention measures. This work presents results from focus group discussions conducted in two Colorado counties in 2003, a year of significant WNV activity in the state. Issues addressed include residents’ assessment of risk and how this perception varied by age group and location, use or nonuse of repellents, and community attitudes toward mosquito control in areas with different ecologies and histories of mosquito-borne disease. The need to address individual components of personal prevention, to target prevention to specific audiences, and to disseminate prevention messages through local channels is discussed. The authors propose including aspects of ecology and disease proximity in understanding risk perception and addressing emerging diseases with a prominent ecological component.     

The macroecology of infectious diseases: a new perspective on global‐scale drivers of pathogen distributions and impacts

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.     

Deadly secret: situating the unknowing and knowing of the source of the Ebola epidemic in Northern Uganda

This article critically examines the unknowing of the source of the Ebola epidemic in Northern Uganda, in 2000/1, by asking how this unknowing has been achieved and has shaped the disease situation. Specifically, this article follows my informants’ explanation that soldiers of the Uganda People's Defence Force had brought the disease from the Democratic Republic of the Congo to Uganda. This account is widely rejected as a rumour by scientists, who insist that the source of the epidemic remains unknown. By contrast, I suggest that following these stories, as embodied experiences of the multiple connections between war and epidemics, human and nonhuman lives, provides crucial insights into the political ecology of Ebola in the wider region – a region where, even today, conflict and Ebola outbreaks are intricately interwoven. Understanding how unknowing is achieved and shapes a disease situation directs attention to forms of silent knowing, which illuminate what preparedness means in the political ecology of Ebola.     

A Sensory Ecology of Medicinal Plant Therapy in Two Amazonian Societies

Sensory anthropology has explored sensation as a fruitful but poorly examined domain of cross-cultural research. Curiously, sensory anthropologists have mostly ignored scientific research into sensation, even that which addresses cross-cultural variation. A comparative study in two Amazonian societies (Matsigenka, Yora [Nahua]) documented the role of the senses in medicinal plant therapy and benefited greatly from theoretical insights gleaned from sensory science. The study reveals a complex interweaving of cultural and ecological factors in medicinal plant selection, with sensation standing at the culture--nature nexus linking medical ideas with medical materials. By synthesizing (rather than antagonizing) scientific and anthropological insights, sensation can be understood as a biocultural phenomenon rooted in human physiology yet constructed through individual experience and culture. Overcoming the limitations of a narrowly defined sensory anthropology, sensory ecology is here proposed as a new theoretical perspective for addressing human--environment interactions mediated by the senses.     

Big brains, small worlds: material culture and the evolution of the mind

New developments in neuroimaging have demonstrated that the basic capacities underpinning human social skills are shared by our closest extant primate relatives. The challenge for archaeologists is to explain how complex human societies evolved from this shared pattern of face-to-face social interaction. We argue that a key process was the gradual incorporation of material culture into social networks over the course of hominin evolution. Here we use three long-term processes in hominin evolution-encephalization, the global human diaspora and sedentism/agriculture-to illustrate how the cultural transmission of material culture allowed the 'scaling up' of face-to-face social interactions to the global societies known today. We conclude that future research by neuroimagers and archaeologists will need to investigate the cognitive mechanisms behind human engagement with material culture as well as other persons.     

Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space

The potential for disease transmission at the interface of wildlife, domestic animals and humans has become a major concern for public health and conservation biology. Research in this subject is commonly conducted at local scales while the regional context is neglected. We argue that prevalence of infection at local and regional levels is influenced by three mechanisms occurring at the landscape level in a metacommunity context. First, (1) dispersal, colonization, and extinction of pathogens, reservoir or vector hosts, and nonreservoir hosts, may be due to stochastic and niche‐based processes, thus determining distribution of all species, and then their potential interactions, across local communities (metacommunity structure). Second, (2) anthropogenic processes may drive environmental filtering of hosts, nonhosts, and pathogens. Finally, (3) phylogenetic diversity relative to reservoir or vector host(s), within and between local communities may facilitate pathogen persistence and circulation. Using a metacommunity approach, public heath scientists may better evaluate the factors that predispose certain times and places for the origin and emergence of infectious diseases. The multidisciplinary approach we describe fits within a comprehensive One Health and Ecohealth framework addressing zoonotic infectious disease outbreaks and their relationship to their hosts, other animals, humans, and the environment.     

The Effect of Disease-Induced Mortality on Structural Network Properties

As the understanding of the importance of social contact networks in the spread of infectious diseases has increased, so has the interest in understanding the feedback process of the disease altering the social network. While many studies have explored the influence of individual epidemiological parameters and/or underlying network topologies on the resulting disease dynamics, we here provide a systematic overview of the interactions between these two influences on population-level disease outcomes. We show that the sensitivity of the population-level disease outcomes to the combination of epidemiological parameters that describe the disease are critically dependent on the topological structure of the population’s contact network. We introduce a new metric for assessing disease-driven structural damage to a network as a population-level outcome. Lastly, we discuss how the expected individual-level disease burden is influenced by the complete suite of epidemiological characteristics for the circulating disease and the ongoing process of network compromise. Our results have broad implications for prediction and mitigation of outbreaks in both natural and human populations.     

Introducing One Health to the Ethical Debate About Zoonotic Diseases in Southeast Asia

Pandemic plans recommend phases of response to an emergent infectious disease (EID) outbreak, and are primarily aimed at preventing and mitigating human‐to‐human transmission. These plans carry presumptive weight and are increasingly being operationalized at the national, regional and international level with the support of the World Health Organization (WHO). The conventional focus of pandemic preparedness for EIDs of zoonotic origin has been on public health and human welfare. However, this focus on human populations has resulted in strategically important disciplinary silos. As the risks of zoonotic diseases have implications that reach across many domains outside traditional public health, including anthropological, environmental, and veterinary fora, a more inclusive ecological perspective is paramount for an effective response to future outbreaks.     

Primate Conservation: The Prevention of Disease Transmission

We address the strategies to prevent disease transmission from human to non-human primates in natural settings. Some field research methods, such as gaining close proximity for observation, provisioning for habituation, or reintroducing for repopulation, may place primate subjects at risk for acquiring human-carried diseases. Additional risks arise through inadequate waste disposal or nonhygienic conditions of humans residing at the study site. We describe several disease outbreaks at primate field sites, emphasizing the need for proper protocols to diagnose, to treat, and to prevent recurrence. Finding solutions to the disease transmission problem requires effecting change in the behavior and policies of many individuals, including field researchers, veterinarians, human health care providers, park personnel, government officials, local villagers, and tourists. The prevention of exposure to infectious disease is an important, fundamental aspect of primate conservation; the assurance of good health and longevity in wild primate populations is paramount to the more traditional conservation issues of poaching control and forest protection.