Linking community and disease ecology: the impact of biodiversity on pathogen transmission

The increasing number of zoonotic diseases spilling over from a range of wild animal species represents a particular concern for public health, especially in light of the current dramatic trend of biodiversity loss. To understand the ecology of these multi-host pathogens and their response to environmental degradation and species extinctions, it is necessary to develop a theoretical framework that takes into account realistic community assemblages. Here, we present a multi-host species epidemiological model that includes empirically determined patterns of diversity and composition derived from community ecology studies. We use this framework to study the interaction between wildlife diversity and directly transmitted pathogen dynamics. First, we demonstrate that variability in community composition does not affect significantly the intensity of pathogen transmission. We also show that the consequences of community diversity can differentially impact the prevalence of pathogens and the number of infectious individuals. Finally, we show that ecological interactions among host species have a weaker influence on pathogen circulation than inter-species transmission rates. We conclude that integration of a community perspective to study wildlife pathogens is crucial, especially in the context of understanding and predicting infectious disease emergence events.     

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.     

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.     

A temporal dilution effect: hantavirus infection in deer mice and the intermittent presence of voles in Montana

The effect of intermittently occurring, non-reservoir host species on pathogen transmission and prevalence in a reservoir population is poorly understood. We investigated whether voles, Microtus spp., which occur intermittently, influenced estimated standing antibody prevalence (ESAP) to Sin Nombre hantavirus (SNV, Bunyaviridae: Hantavirus) among deer mice, Peromyscus maniculatus, whose populations are persistent. We used 14 years of data from central Montana to investigate whether ESAP among deer mice was related to vole presence or abundance while controlling for the relationship between deer mouse abundance and ESAP. We found a reduction in deer mouse ESAP associated with the presence of voles, independent of vole abundance. A number of studies have documented that geographic locations which support a higher host diversity can be associated with reductions in pathogen prevalence by a hypothesized dilution effect. We suggest a dilution effect may also occur in a temporal dimension at sites where host richness fluctuates. Preservation of host diversity and optimization of environmental conditions which promote occurrence of ephemeral species, such as voles, may result in a decreased ESAP to hantaviruses among reservoir hosts. Our results may extend to other zoonotic infectious diseases.     

Synanthropy of Wild Mammals as a Determinant of Emerging Infectious Diseases in the Asian–Australasian Region

Humans create ecologically simplified landscapes that favour some wildlife species, but not others. Here, we explore the possibility that those species that tolerate or do well in human-modified environments, or 'synanthropic' species, are predominantly the hosts of zoonotic emerging and re-emerging infectious diseases (EIDs). We do this using global wildlife conservation data and wildlife host information extracted from systematically reviewed emerging infectious disease literature. The evidence for this relationship is examined with special emphasis on the Australasian, South East Asian and East Asian regions. We find that synanthropic wildlife hosts are approximately 15 times more likely than other wildlife in this region to be the source of emerging infectious diseases, and this association is essentially independent of the taxonomy of the species. A significant positive association with EIDs is also evident for those wildlife species of low conservation risk. Since the increase and spread of native and introduced species able to adapt to human-induced landscape change is at the expense of those species most vulnerable to habitat loss, our findings suggest a mechanism linking land conversion, global decline in biodiversity and a rise in EIDs of wildlife origin.     

Ecosystem dynamics, biological diversity and emerging infectious diseases

In this article, we summarize the major scientific developments of the last decade on the transmission of infectious agents in multi-host systems. Almost sixty percent of the pathogens that have emerged in humans during the last 30-40 years are of animal origin and about sixty percent of them show an important variety of host species besides humans (3 or more possible host species). In this review, we focus on zoonotic infections with vector-borne transmission and dissect the contrasting effects that a multiplicity of host reservoirs and vectors can have on their disease dynamics. We discuss the effects exerted by host and vector species richness and composition on pathogen prevalence (i.e., reduction, including the dilution effect, or amplification). We emphasize that, in multiple host systems and for vector-borne zoonotic pathogens, host reservoir species and vector species can exert contrasting effect locally. The outcome on disease dynamics (reduced pathogen prevalence in vectors when the host reservoir species is rich and increased pathogen prevalence when the vector species richness increases) may be highly heterogeneous in both space and time. We then ask briefly how a shift towards a more systemic perspective in the study of emerging infectious diseases, which are driven by a multiplicity of hosts, may stimulate further research developments. Finally, we propose some research avenues that take better into account the multi-host species reality in the transmission of the most important emerging infectious diseases, and, particularly, suggest, as a possible orientation, the careful assessment of the life-history characteristics of hosts and vectors in a community ecology-based perspective.     

Wildlife Trade and Human Health in Lao PDR: An Assessment of the Zoonotic Disease Risk in Markets

Although the majority of emerging infectious diseases can be linked to wildlife sources, most pathogen spillover events to people could likely be avoided if transmission was better understood and practices adjusted to mitigate risk. Wildlife trade can facilitate zoonotic disease transmission and represents a threat to human health and economies in Asia, highlighted by the 2003 SARS coronavirus outbreak, where a Chinese wildlife market facilitated pathogen transmission. Additionally, wildlife trade poses a serious threat to biodiversity. Therefore, the combined impacts of Asian wildlife trade, sometimes termed bush meat trade, on public health and biodiversity need assessing. From 2010 to 2013, observational data were collected in Lao PDR from markets selling wildlife, including information on volume, form, species and price of wildlife; market biosafety and visitor origin. The potential for traded wildlife to host zoonotic diseases that pose a serious threat to human health was then evaluated at seven markets identified as having high volumes of trade. At the seven markets, during 21 observational surveys, 1,937 alive or fresh dead mammals (approximately 1,009 kg) were observed for sale, including mammals from 12 taxonomic families previously documented to be capable of hosting 36 zoonotic pathogens. In these seven markets, the combination of high wildlife volumes, high risk taxa for zoonoses and poor biosafety increases the potential for pathogen presence and transmission. To examine the potential conservation impact of trade in markets, we assessed the status of 33,752 animals observed during 375 visits to 93 markets, under the Lao PDR Wildlife and Aquatic Law. We observed 6,452 animals listed by Lao PDR as near extinct or threatened with extinction. The combined risks of wildlife trade in Lao PDR to human health and biodiversity highlight the need for a multi-sector approach to effectively protect public health, economic interests and biodiversity.     

The ecology of chronic wasting disease in wildlife

Prions are misfolded infectious proteins responsible for a group of fatal neurodegenerative diseases termed transmissible spongiform encephalopathy or prion diseases. Chronic Wasting Disease (CWD) is the prion disease with the highest spillover potential, affecting at least seven Cervidae (deer) species. The zoonotic potential of CWD is inconclusive and cannot be ruled out. A risk of infection for other domestic and wildlife species is also plausible. Here, we review the current status of the knowledge with respect to CWD ecology in wildlife. Our current understanding of the geographic distribution of CWD lacks spatial and temporal detail, does not consider the biogeography of infectious diseases, and is largely biased by sampling based on hunters' cooperation and funding available for each region. Limitations of the methods used for data collection suggest that the extent and prevalence of CWD in wildlife is underestimated. If the zoonotic potential of CWD is confirmed in the short term, as suggested by recent results obtained in experimental animal models, there will be limited accurate epidemiological data to inform public health. Research gaps in CWD prion ecology include the need to identify specific biological characteristics of potential CWD reservoir species that better explain susceptibility to spillover, landscape and climate configurations that are suitable for CWD transmission, and the magnitude of sampling bias in our current understanding of CWD distribution and risk. Addressing these research gaps will help anticipate novel areas and species where CWD spillover is expected, which will inform control strategies. From an ecological perspective, control strategies could include assessing restoration of natural predators of CWD reservoirs, ultrasensitive CWD detection in biotic and abiotic reservoirs, and deer density and landscape modification to reduce CWD spread and prevalence.     

Human–Wildlife Interactions Predict Febrile Illness in Park Landscapes of Western Uganda

Fevers of unknown origin complicate treatment and prevention of infectious diseases and are a global health burden. We examined risk factors of self-reported fever—categorized as “malarial” and “nonmalarial”—in households adjacent to national parks across the Ugandan Albertine Rift, a biodiversity and emerging infectious disease hotspot. Statistical models fitted to these data suggest that perceived nonmalarial fevers of unknown origin were associated with more frequent direct contact with wildlife and with increased distance from parks where wildlife habitat is limited to small forest fragments. Perceived malarial fevers were associated with close proximity to parks but were not associated with direct wildlife contact. Self-reported fevers of any kind were not associated with livestock ownership. These results suggest a hypothesis that nonmalarial fevers in this area are associated with wildlife contact, and further investigation of zoonoses from wildlife is warranted. More generally, our findings of land use–disease relationships aid in hypothesis development for future research in this social-ecological system where emerging infectious diseases specifically, and rural public health provisioning generally, are important issues.     

Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa

Changes in host diversity have been postulated to influence the risk of infectious diseases, including both dilution and amplification effects. The dilution effect refers to a negative relationship between biodiversity and disease risk, whereas the amplification effect occurs when biodiversity increases disease risk. We tested these effects with an influential disease, bovine tuberculosis (BTB), which is widespread in many countries, causing severe economic losses. Based on the BTB outbreak data in cattle from 2005 to 2010, we also tested, using generalized linear mixed models, which other factors were associated with the regional BTB presence in cattle in Africa. The interdependencies of predictors and their correlations with BTB presence were examined using path analysis. Our results suggested a dilution effect, where increased mammal species richness was associated with reduced probability of BTB presence after adjustment for cattle density. In addition, our results also suggested that areas with BTB infection in the preceding year, higher cattle density and larger percentage of area occupied by African buffalo were more likely to report BTB outbreaks. Climatic variables only indirectly influenced the risk of BTB presence through their effects on cattle density and wildlife distribution. Since most studies investigating the role of wildlife species on BTB transmission only involve single-species analysis, more efforts are needed to better understand the effect of the structure of wildlife communities on BTB dynamics.     

Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk

The emergence of several high profile infectious diseases in recent years has focused attention on our need to understand the ecological factors contributing to the spread of infectious diseases. West Nile virus (WNV) is a mosquito-borne zoonotic disease that was first detected in the United States in 1999. The factors accounting for variation in the prevalence of WNV are poorly understood, but recentideas suggesting links between high biodiversity and reduced vector-borne disease risk may help account for distribution patterns of this disease. Since wild birds are the primary reservoir hosts for WNV, we tested associations between passerine (Passeriform) bird diversity, non-passerine (all other orders) bird diversity and virus infection rates in mosquitoes and humans to examine the extent to which bird diversity is associated with WNV infection risk. We found t h at non-passerine species richness (number of non-passerine species) was significantly negatively correlated with both mosquito and human infection rates, whereas there was no significant association between passerine species richness and any measure of infection risk. Our findings suggest that non-passerine diversity may play a role in dampening WNV amplification rates in mosquitoes, minimizing human disease risk.     

Biodiversity in the Lyme-light: ecological restoration and tick-borne diseases in Europe

Biodiversity loss and the emergence of zoonotic diseases are two major global challenges. An urgent question is how ecosystems and wildlife communities can be restored whilst minimizing the risk of zoonotic diseases carried by wildlife. Here, we evaluate how current ambitions to restore Europe’s natural ecosystems may affect the hazard of diseases vectored by the tick Ixodes ricinus at different scales. We find that effects of restoration efforts on tick abundance are relatively straightforward but that the interacting effects of vertebrate diversity and abundance on pathogen transmission are insufficiently known. Long-term integrated surveillance of wildlife communities, ticks, and their pathogens is needed to understand their interactions and to prevent nature restoration from increasing tick-borne disease (TBD) hazard.     

Navigating parasite webs and parasite flow: emerging and re-emerging parasitic zoonoses of wildlife origin

Wildlife are now recognised as an important source of emerging human pathogens, including parasites. This paper discusses the linkages between wildlife, people, zoonotic parasites and the ecosystems in which they co-exist, revisits definitions for 'emerging' and 're-emerging', and lists zoonotic parasites that can be acquired from wildlife including, for some, estimates of the associated global human health burdens. The paper also introduces the concepts of 'parasite webs' and 'parasite flow', provides a context for parasites, relative to other infectious agents, as causes of emerging human disease, and discusses drivers of disease emergence and re-emergence, especially changes in biodiversity and climate. Angiostrongylus cantonensis in the Caribbean and the southern United States, Baylisascaris procyonis in California and Georgia, Plasmodium knowlesi in Sarawak, Malaysia, Human African Trypanosomiasis, Sarcoptes scabiei in carnivores, and Cryptosporidium, Giardia and Toxoplasma in marine ecosystems are presented as examples of wildlife-derived zoonotic parasites of particular recent interest. An ecological approach to disease is promoted, as is a need for an increased profile for this approach in undergraduate and graduate education in the health sciences. Synergy among scientists and disciplines is identified as critical for the study of parasites and parasitic disease in wildlife populations. Recent advances in techniques for the investigation of parasite fauna of wildlife are presented and monitoring and surveillance systems for wildlife disease are discussed. Some of the limitations inherent in predictions for the emergence and re-emergence of infection and disease associated with zoonotic parasites of wildlife are identified. The importance of public awareness and public education in the prevention and control of emerging and re-emerging zoonotic infection and disease are emphasised. Finally, some thoughts for the future are presented.     

The Decline of the Sharp-Snouted Day Frog (Taudactylus acutirostris): The First Documented Case of Extinction by Infection in a Free-Ranging Wildlife Species?

Infectious diseases are increasingly recognized as the cause of mass mortality events, population declines, and the local extirpation of wildlife species. In a number of cases, it has been hypothesized that pathogens have caused species extinctions in wildlife. However, there is only one definitively proven case of extinction by infection, and this was in a remnant captive population of a Polynesian tree snail. In this article, we review the potential involvement of infectious disease in the recent extinction of the sharp-snouted day frog Taudactylus acutirostris. Our review of available evidence suggests that a virulent pathogen of amphibians, Batrachochytrium dendrobatidis, caused a rapid, catastrophic decline of this species, from which it did not recover. We propose that this is the first case of extinction by infection of a free-ranging wildlife species where disease acted as both the proximate and ultimate cause of extinction. This highlights a probable underreporting of infectious disease as a cause of biodiversity loss historically and currently.     

Wildlife Trade and the Emergence of Infectious Diseases

Most recent emerging infectious diseases have been zoonotic in origin. It is our contention that one of the factors responsible for such emergence is the trade in wildlife and bushmeat in particular. This article considers the effect of increasing diversity in the species hunted on the probability of global epidemics such as SARS. In particular, we develop a mathematical model of the probability of such an outbreak in terms of the number of species hunted, the number of susceptibles, and the rate of contact. Hence, we postulate that local biodiversity loss and increasing rates of animal trafficking, and trade and transportation of animals to large cities—where there is a greater potential for person-to-person transmission—may increase the probability of such outbreaks dramatically.     

Detection and characterization of three zoonotic viruses in wild rodents and shrews from Shenzhen city,China

Diverse species of rodents and shrews, which are abundant worldwide, harbor a variety of viruses;some of these are closely related to human viruses and possess zoonotic potential. Previously studies have demonstrated that the mammarenavirus and hantavirus carried by rodents or shrews could cause diseases in human population. To determine the distribution of zoonotic viruses in Shenzhen city, the major city in southern China with a high population density, we analyzed 225 rodents(Rattus norvegicus and Rattus flavipectus) and 196 shrews(Suncus murinus) from urban and rural districts for the presence of mammarenavirus, hantavirus, and hepatitis E virus(HEV) by RT-PCR targeting the conserved regions. The infection rates for mammarenavirus, hantaviruses,and HEV in rodents and shrews were 3.56%, 6.89%, and 1.66%, respectively. Partial genome fragment analysis indicated that mammarenavirus and hantavirus strains had more than 90% and 99% nucleic acid identity with Cardamones virus and Seoul virus, respectively, which cause diseases in humans. Although the present HEV strains identified are typically found worldwide,phylogenetic analysis demonstrated a divergence of 16%. To our knowledge, the present work is the first report of the prevalence of mammarenavirus, hantaviruses, and rat HEV strains in rodents and shrews from Shenzhen city, China. Our findings highlight the zoonotic potential of rodent-and shrew-borne mammarenavirus and hantavirus, and the biodiversity of rat HEV isolates in Shenzhen city. The present work suggests that utilization of good hygiene habits is important to minimize the risk of zoonosis.     

Local Scale Effects of Disease on Biodiversity

To date, ecologists and conservation biologists have focused much of their attention on the population and ecosystem effects of disease at regional scales and the role that diseases play in global species extinction. Far less research has been dedicated to identifying the effects that diseases can have on local scale species assemblages. We examined the role of infectious disease in structuring local biodiversity. Our intention was to illustrate how variable outcomes can occur by focusing on three case studies: the influence of chestnut blight on forest communities dominated by chestnut trees, the influence of red-spot disease on urchin barrens and kelp forests, and the influence of sylvatic plague on grassland communities inhabited by prairie dogs. Our findings reveal that at local scales infectious disease seems to play an important, though unpredictable, role in structuring species diversity. Through our case studies, we have shown that diseases can cause drastic population declines or local extirpations in keystone species, ecosystem engineers, and otherwise abundant species. These changes in local diversity may be very important, particularly when considered alongside potentially corresponding changes in community structure and function, and we believe that future efforts to understand the importance of disease to species diversity should have an increased focus on these local scales.     

Optimization of a Novel Non-invasive Oral Sampling Technique for Zoonotic Pathogen Surveillance in Nonhuman Primates

Free-ranging nonhuman primates are frequent sources of zoonotic pathogens due to their physiologic similarity and in many tropical regions, close contact with humans. Many high-risk disease transmission interfaces have not been monitored for zoonotic pathogens due to difficulties inherent to invasive sampling of free-ranging wildlife. Non-invasive surveillance of nonhuman primates for pathogens with high potential for spillover into humans is therefore critical for understanding disease ecology of existing zoonotic pathogen burdens and identifying communities where zoonotic diseases are likely to emerge in the future. We developed a non-invasive oral sampling technique using ropes distributed to nonhuman primates to target viruses shed in the oral cavity, which through bite wounds and discarded food, could be transmitted to people. Optimization was performed by testing paired rope and oral swabs from laboratory colony rhesus macaques for rhesus cytomegalovirus (RhCMV) and simian foamy virus (SFV) and implementing the technique with free-ranging terrestrial and arboreal nonhuman primate species in Uganda and Nepal. Both ubiquitous DNA and RNA viruses, RhCMV and SFV, were detected in oral samples collected from ropes distributed to laboratory colony macaques and SFV was detected in free-ranging macaques and olive baboons. Our study describes a technique that can be used for disease surveillance in free-ranging nonhuman primates and, potentially, other wildlife species when invasive sampling techniques may not be feasible.     

Deciphering Serology to Understand the Ecology of Infectious Diseases in Wildlife

The ecology of infectious disease in wildlife has become a pivotal theme in animal and public health. Studies of infectious disease ecology rely on robust surveillance of pathogens in reservoir hosts, often based on serology, which is the detection of specific antibodies in the blood and is used to infer infection history. However, serological data can be inaccurate for inference to infection history for a variety of reasons. Two major aspects in any serological test can substantially impact results and interpretation of antibody prevalence data: cross-reactivity and cut-off thresholds used to discriminate positive and negative reactions. Given the ubiquitous use of serology as a tool for surveillance and epidemiological modeling of wildlife diseases, it is imperative to consider the strengths and limitations of serological test methodologies and interpretation of results, particularly when using data that may affect management and policy for the prevention and control of infectious diseases in wildlife. Greater consideration of population age structure and cohort representation, serological test suitability and standardized sample collection protocols can ensure that reliable data are obtained for downstream modeling applications to characterize, and evaluate interventions for, wildlife disease systems.     

Emerging Infectious Diseases in Free-Ranging Wildlife–Australian Zoo Based Wildlife Hospitals Contribute to National Surveillance

Emerging infectious diseases are increasingly originating from wildlife. Many of these diseases have significant impacts on human health, domestic animal health, and biodiversity. Surveillance is the key to early detection of emerging diseases. A zoo based wildlife disease surveillance program developed in Australia incorporates disease information from free-ranging wildlife into the existing national wildlife health information system. This program uses a collaborative approach and provides a strong model for a disease surveillance program for free-ranging wildlife that enhances the national capacity for early detection of emerging diseases.