Allometric scaling and seasonality in the epidemics of wildlife diseases

We present a susceptibles-exposed-infectives (SEI) model to analyze the effects of seasonality on epidemics, mainly of rabies, in a wide range of wildlife species. Model parameters are cast as simple allometric functions of host body size. Via nonlinear analysis, we investigate the dynamical behavior of the disease for different levels of seasonality in the transmission rate and for different values of the pathogen basic reproduction number (R(0)) over a broad range of body sizes. While the unforced SEI model exhibits long-term epizootic cycles only for large values of R(0), the seasonal model exhibits multiyear periodicity for small values of R(0). The oscillation period predicted by the seasonal model is consistent with those observed in the field for different host species. These conclusions are not affected by alternative assumptions for the shape of seasonality or for the parameters that exhibit seasonal variations. However, the introduction of host immunity (which occurs for rabies in some species and is typical of many other wildlife diseases) significantly modifies the epidemic dynamics; in this case, multiyear cycling requires a large level of seasonal forcing. Our analysis suggests that the explicit inclusion of periodic forcing in models of wildlife disease may be crucial to correctly describe the epidemics of wildlife that live in strongly seasonal environments.     

Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence

Pathogens that can be transmitted between different host species are of fundamental interest and importance from public health, conservation and economic perspectives, yet systematic quantification of these pathogens is lacking. Here, pathogen characteristics, host range and risk factors determining disease emergence were analysed by constructing a database of disease-causing pathogens of humans and domestic mammals. The database consisted of 1415 pathogens causing disease in humans, 616 in livestock and 374 in domestic carnivores. Multihost pathogens were very prevalent among human pathogens (61.6%) and even more so among domestic mammal pathogens (livestock 77.3%, carnivores 90.0%). Pathogens able to infect human, domestic and wildlife hosts contained a similar proportion of disease-causing pathogens for all three host groups. One hundred and ninety-six pathogens were associated with emerging diseases, 175 in humans, 29 in livestock and 12 in domestic carnivores. Across all these groups, helminths and fungi were relatively unlikely to emerge whereas viruses, particularly RNA viruses, were highly likely to emerge. The ability of a pathogen to infect multiple hosts, particularly hosts in other taxonomic orders or wildlife, were also risk factors for emergence in human and livestock pathogens. There is clearly a need to understand the dynamics of infectious diseases in complex multihost communities in order to mitigate disease threats to public health, livestock economies and wildlife.     

Genome sequence of the first human adenovirus type 14 isolated in China

Emergent pathogens may be examined rapidly at high resolution on a molecular level using genomics, allowing an understanding of their evolution. China is a unique environment for studying pathogens, having a large, dense, and generally closed population. Human adenovirus type 14 (HAdV-14) was originally identified as an acute respiratory disease (ARD) pathogen in The Netherlands (1955), with a second isolation in England (1957). Since then, few reports of this virus appeared until an ARD pathogen with a similar genome caused multiple outbreaks in the United States (2006 to 2009). This report presents the first genome of HAdV-B14 isolated in China (2010). As China experienced two recent outbreaks of an emergent ARD pathogen, HAdV-B55, containing much of the HAdV-B14 genome, the availability of this HAdV-B14 sequence will facilitate studies of the epidemiology of these pathogens, as well as provide a foundation for studying adenovirus evolution and the genesis of emergent pathogens. These observations may be invaluable in predicting possible recombination between wild-type viruses and adenoviral gene delivery vectors, including adenovirus vaccines.     

Ixodes ricinus, transmitted diseases and reservoirs

The tick Ixodes ricinus has been recorded in most Italian regions especially in thermo-mesophilous woods and shrubby habitats where the relative humidity allow the tick to complete its 3 year developmental cycle, as predicted for the European climatic ranges. This tick acts both as vector and reservoir for a series of wildlife zoonotic pathogens, especially the agents of Lyme diseases, Tick borne encephalitis and Human Granulocytic Ehrlichiosis, which are emerging in most of Europe. To assess the spatial distribution of these pathogens and the infection risk for humans and animals within the territory of the Province of Trento, we carried out a long term study using a combination of eco-epidemiological surveys and mathematical modelling. An extensive tick collection with a GIS based habitat suitability analysis allowed us to identify the areas where tick occurs at various density. To identify the areas with higher infection risk, we estimated the values of R0 for Borrelia burgdorferi s.l., TBE virus and Anaplasma phagocytophila under different ecological conditions. We assessed the infection prevalence in the vector and in the wildlife reservoir species that play a central role in the persistence of these infections, ie the small mammals A. flavicollis and C. glareolus. We also considered the double effect of roe deer (Capreolus capreolus) which act as reservoir for A. phagocytophila but is an incompetent host for B. burgdorferi and TBE virus, thus reducing the infection prevalence in ticks of these last two pathogens. Infection prevalence with B. burgdorferi and A. phagocytophila in the vector was assessed by PCR screening 1212 I. ricinus nymphs collected by dragging in six main study areas during 2002. The mean infection prevalence recorded was 1.32% for B. burgdorferi s.l. and 9.84% for A. phagocytophila. Infection prevalence in nymphs with TBE virus, as assessed in a previous study was 0.03%. Infection prevalence in rodents was assessed by screening (with ELISA and PCR) tissues and blood samples collected from 367 rodent individuals trapped extensively during 2002 within 6 main study areas. A. flavicollis (N=238) was found to be infected with all three pathogens investigated, with infection prevalence ranging from 3.3% for TBE virus to 11.7% for A. phagocytophila, and 16.6% with B. burgdorferi s.l. C. glareolus (N=108) showed an infection prevalence of 6.5% with A. phagocytophila and 12.7% with B. burgdorferi s.l., while no individuals were infected with TBE virus. We also screened 98 spleen samples collected from roe deer with PCR, resulting in a mean prevalence of infection with A. phagocytophila of 19.8%. Using a deterministic model we explored the condition for diseases persistence under different rodent and roe deer densities. R0 values resulted largely above 1 for B. burgdorferi s.l. in the vast majority of the areas classified as suitable for I. ricinus occurrence in Trentino, while the condition for TBE persistence appeared to be more restricted by a combination of climatic condition and host densities.     

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.     

Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii

Recent outbreaks of new diseases in many ecosystems are caused by novel pathogens, impaired host immunity, or changing environmental conditions. Identifying the source of emergent pathogens is critical for mitigating the impacts of diseases, and understanding the cause of their recent appearances. One ecosystem suffering outbreaks of disease in the past decades is coral reefs, where pathogens such as the fungus Aspergillus sydowii have caused catastrophic population declines in their hosts. Aspergillosis is one of the best-characterized coral diseases, yet the origin of this typically terrestrial fungus in marine systems remains unknown. We examined the genetic structure of a global sample of A. sydowii, including isolates from diseased corals, diseased humans, and environmental sources. Twelve microsatellite markers reveal a pattern of global panmixia among the fungal isolates. A single origin of the pathogen into marine systems seems unlikely given the lack of isolation by distance and lack of evidence for a recent bottleneck. A neighbour-joining phylogeny shows that sea fan isolates are interspersed with environmental isolates, suggesting there have been multiple introductions from land into the ocean. Overall, our results underscore that A. sydowii is a true opportunist, with a diversity of nonrelated isolates able to cause disease in corals. This study highlights the challenge in distinguishing between the role of environment in allowing opportunistic pathogens to increase and actual introductions of new pathogenic microorganisms for coral diseases.     

How do pathogen evolution and host heterogeneity interact in disease emergence?

Heterogeneity in the parameters governing the spread of infectious diseases is a common feature of real-world epidemics. It has been suggested that for pathogens with basic reproductive number R(0)>1, increasing heterogeneity makes extinction of disease more likely during the early rounds of transmission. The basic reproductive number R(0) of the introduced pathogen may, however, be less than 1 after the introduction, and evolutionary changes are then required for R(0) to increase to above 1 and the pathogen to emerge. In this paper, we consider how host heterogeneity influences the emergence of both non-evolving pathogens and those that must undergo adaptive changes to spread in the host population. In contrast to previous results, we find that heterogeneity does not always make extinction more likely and that if adaptation is required for emergence, the effect of host heterogeneity is relatively small. We discuss the application of these ideas to vaccination strategies.     

A Review of Zoonotic Infection Risks Associated with the Wild Meat Trade in Malaysia

The overhunting of wildlife for food and commercial gain presents a major threat to biodiversity in tropical forests and poses health risks to humans from contact with wild animals. Using a recent survey of wildlife offered at wild meat markets in Malaysia as a basis, we review the literature to determine the potential zoonotic infection risks from hunting, butchering and consuming the species offered. We also determine which taxa potentially host the highest number of pathogens and discuss the significant disease risks from traded wildlife, considering how cultural practices influence zoonotic transmission. We identify 51 zoonotic pathogens (16 viruses, 19 bacteria and 16 parasites) potentially hosted by wildlife and describe the human health risks. The Suidae and the Cervidae families potentially host the highest number of pathogens. We conclude that there are substantial gaps in our knowledge of zoonotic pathogens and recommend performing microbial food safety risk assessments to assess the hazards of wild meat consumption. Overall, there may be considerable zoonotic risks to people involved in the hunting, butchering or consumption of wild meat in Southeast Asia, and these should be considered in public health strategies.     

Body-size scaling in an SEI model of wildlife diseases

A number of wildlife pathogens are generalist and can affect different host species characterized by a wide range of body sizes. In this work we analyze the role of allometric scaling of host vital and epidemiological rates in a Susceptible-Exposed-Infected (SEI) model. Our analysis shows that the transmission coefficient threshold for the disease to establish in the population scales allometrically (exponent = 0.45) with host size as well as the threshold at which limit cycles occur. In contrast, the threshold of the basic reproduction number for sustained oscillations to occur is independent of the host size and is always greater than 5. In the case of rabies, we show that the oscillation periods predicted by the model match those observed in the field for a wide range of host sizes.The population dynamics of the SEI model is also analyzed in the case of pathogens affecting multiple coexisting hosts with different body sizes. Our analyses show that the basic reproduction number for limit cycles to occur depends on the ratio between host sizes, that the oscillation period in a multihost community is set by the smaller species dynamics, and that intermediate interspecific disease transmission can stabilize the epidemic occurrence in wildlife communities.     

Genetic resistance to bovine tuberculosis in the Iberian wild boar

Bovine tuberculosis (bTB) is an important re-emerging zoonotic disease, causing major economic losses and constraining international trade of animals and their products. Despite eradication programmes, some countries continue to encounter outbreaks, mainly due to wildlife acting as primary hosts or reservoirs. While the genetic component of tuberculosis in humans and cattle is well documented, the role of genetic factors as modulators of bTB resistance remains unclear for natural populations. To address this issue, we investigated the relative contribution of host genetic variability to susceptibility to bTB infection and disease progression in wild boars from southern Spain. We found that genetic heterozygosity is an important predictor of bTB, not only modulating resistance to infection but also influencing containment of disease progression in infected individuals. Our results provide further evidence that host genetic variability plays a central role in natural populations. Testing each marker separately reveals evidence of both general and single-locus associative effects on bTB and several loci reveal high homology to regions of the genome with known immune function. Our results may prove to be crucial for understanding outbreaks of bTB in wildlife that could potentially affect domestic livestock and humans.     

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

Many generalist pathogens are influenced by the spatial distributions and relative abundances of susceptible host species. The spatial structure of host populations can influence patterns of infection incidence (or disease outbreaks), and the effects of a generalist pathogen on host community dynamics in a spatially heterogeneous community may differ from predictions derived via simple models. In this paper, we model the transmission of a generalist pathogen within a patch framework that incorporates the movement of vectors between discrete host patches to investigate the effects of local host community composition and vector movement rates on disease dynamics.     

Substrate-Specific Gene Expression in Batrachochytrium dendrobatidis,the Chytrid Pathogen of Amphibians

Determining the mechanisms of host-pathogen interaction is critical for understanding and mitigating infectious disease. Mechanisms of fungal pathogenicity are of particular interest given the recent outbreaks of fungal diseases in wildlife populations. Our study focuses on Batrachochytrium dendrobatidis (Bd), the chytrid pathogen responsible for amphibian declines around the world. Previous studies have hypothesized a role for several specific families of secreted proteases as pathogenicity factors in Bd, but the expression of these genes has only been evaluated in laboratory growth conditions. Here we conduct a genome-wide study of Bd gene expression under two different nutrient conditions. We compare Bd gene expression profiles in standard laboratory growth media and in pulverized host tissue (i.e., frog skin). A large proportion of genes in the Bd genome show increased expression when grown in host tissue, indicating the importance of studying pathogens on host substrate. A number of gene classes show particularly high levels of expression in host tissue, including three families of secreted proteases (metallo-, serine- and aspartyl-proteases), adhesion genes, lipase-3 encoding genes, and a group of phylogenetically unusual crinkler-like effectors. We discuss the roles of these different genes as putative pathogenicity factors and discuss what they can teach us about Bd’s metabolic targets, host invasion, and pathogenesis.     

Epidemiology and disease-control under gene-for-gene plant-pathogen interaction

An introduction of disease-resistant variety of a crop plant often leads to the development of a virulent race in pathogen species that restores the pathogenicity to the resistant crop. This often makes disease control of crop plants extremely difficult. In this paper, we theoretically explore the optimal 'multiline' control, which makes use of several different resistant varieties, that minimizes the expected degree of crop damages caused by epidemic outbreaks of the pathogen. We examine both single-locus and two-locus gene-for-gene (GFG) systems for the compatibility relationship between host genotypes and pathogen genotypes, in which host haplotype has either susceptible or resistant allele in each resistance locus, and the pathogen haplotype has either avirulent or virulent allele in the corresponding virulence locus. We then study the optimal planting strategy of host resistant genotypes based on standard epidemiological dynamics with pathogen spore stages. The most striking result of our single-locus GFG model is that there exists an intermediate optimum mixing ratio for the susceptible and resistant crops that maximizes the final yield, in spite of the fact that the susceptible crop has no use to fight against either avirulent or virulent race of the pathogen. The intermediate mixture is optimum except when the initial pathogen spore population in the season consists exclusively of the virulent race. The optimal proportion of resistant crops is approximately 1/R(0), where R(0) is the basic reproductive ratio of pathogen--the rest (the vast majority if R(0) is large) of crops should be the susceptible genotype. By mixing susceptible and resistant crops, we can force the pathogen races to compete with each other for their available hosts. This competition between avirulent and virulent races prevents the fatal outbreak of the virulent race (the super-race) that can infect all the host genotypes. In the two-locus GFG control, there again exists the optimal mixing ratio for the fraction of universally susceptible genotype and the total fraction of various resistant genotypes, with the ratio close to 1/R(0).     

Mortality Rates Differ Among Amphibian Populations Exposed to Three Strains of a Lethal Ranavirus

Infectious diseases are a growing threat to biodiversity, in many cases because of synergistic effects with habitat loss, environmental contamination, and climate change. Emergence of pathogens as new threats to host populations can also arise when novel combinations of hosts and pathogens are unintentionally brought together, for example, via commercial trade or wildlife relocations and reintroductions. Chytrid fungus (Batrachochytrium dendrobatidis) and amphibian ranaviruses (family Iridoviridae) are pathogens implicated in global amphibian declines. The emergence of disease associated with these pathogens appears to be at least partly related to recent translocations over large geographic distances. We experimentally examined the outcomes of novel combinations of host populations and pathogen strains using the amphibian ranavirus Ambystoma tigrinum virus (ATV) and barred tiger salamanders (Ambystoma mavortium, formerly considered part of the Ambystoma tigrinum complex). One salamander population was highly resistant to lethal infections by all ATV strains, including its own strain, and mortality rates differed among ATV strains according to salamander population. Mortality rates in novel pairings of salamander population and ATV strain were not predictable based on knowledge of mortality rates when salamander populations were exposed to their own ATV strain. The underlying cause(s) for the differences in mortality rates are unknown, but local selection pressures on salamanders, viruses, or both, across the range of this widespread host–pathogen system are a plausible hypothesis. Our study highlights the need to minimize translocations of amphibian ranaviruses, even among conspecifc host populations, and the importance of considering intraspecific variation in endeavors to manage wildlife diseases.     

Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994–2014

We propose ‘the moving target hypothesis’ to describe the aetiology of a contemporary coral disease that differs from that of its historical disease state. Hitting the target with coral disease aetiology is a complex pursuit that requires understanding of host and environment, and may lack a single pathogen solution. White pox disease (WPX) affects the Caribbean coral Acropora palmata. Acroporid serratiosis is a form of WPX for which the bacterial pathogen (Serratia marcescens) has been established. We used long-term (1994–2014) photographic monitoring to evaluate historical and contemporary epizootiology and aetiology of WPX affecting A. palmata at eight reefs in the Florida Keys. Ranges of WPX prevalence over time (0–71.4%) were comparable for the duration of the 20-year study. Whole colony mortality and disease severity were high in historical (1994–2004), and low in contemporary (2008–2014), outbreaks of WPX. Acroporid serratiosis was diagnosed for some historical (1999, 2003) and contemporary (2012, 2013) outbreaks, but this form of WPX was not confirmed for all WPX cases. Our results serve as a context for considering aetiology as a moving target for WPX and other coral diseases for which pathogens are established and/or candidate pathogens are identified. Coral aetiology investigations completed to date suggest that changes in pathogen, host and/or environment alter the disease state and complicate diagnosis.     

Elasticity analysis in epidemiology: an application to tick-borne infections

The application of projection matrices in population biology to plant and animal populations has a parallel in infectious disease ecology when next-generation matrices (NGMs) are used to characterize growth in numbers of infected hosts ( R ₀). The NGM is appropriate for multi-host pathogens, where each matrix element represents the number of cases of one type of host arising from a single infected individual of another type. For projection matrices, calculations of the sensitivity and elasticity of the population growth rate to changes in the matrix elements has generated insight into plant and animal populations. These same perturbation analyses can be used for infectious disease systems. To illustrate this in detail we parameterized an NGM for seven tick-borne zoonoses and compared them in terms of the contributions to R ₀ from three different routes of transmission between ticks, and between ticks and vertebrate hosts. The definition of host type may be the species of the host or the route of infection, or, as was the case for the set of tick-borne pathogens, a combination of species and the life stage at infection. This freedom means that there is a broad range of disease systems and questions for which the methodology is appropriate.     

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.     

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.     

Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta‐analysis

Urbanisation and agriculture cause declines for many wildlife, but some species benefit from novel resources, especially food, provided in human‐dominated habitats. Resulting shifts in wildlife ecology can alter infectious disease dynamics and create opportunities for cross‐species transmission, yet predicting host–pathogen responses to resource provisioning is challenging. Factors enhancing transmission, such as increased aggregation, could be offset by better host immunity due to improved nutrition. Here, we conduct a review and meta‐analysis to show that food provisioning results in highly heterogeneous infection outcomes that depend on pathogen type and anthropogenic food source. We also find empirical support for behavioural and immune mechanisms through which human‐provided resources alter host exposure and tolerance to pathogens. A review of recent theoretical models of resource provisioning and infection dynamics shows that changes in host contact rates and immunity produce strong non‐linear responses in pathogen invasion and prevalence. By integrating results of our meta‐analysis back into a theoretical framework, we find provisioning amplifies pathogen invasion under increased host aggregation and tolerance, but reduces transmission if provisioned food decreases dietary exposure to parasites. These results carry implications for wildlife disease management and highlight areas for future work, such as how resource shifts might affect virulence evolution.