Infectious Diseases In Wildlife Research Articles

The Emerging Amphibian Fungal Disease, Chytridiomycosis: A Key Example of the Global Phenomenon of Wildlife Emerging Infectious Diseases.

The spread of amphibian chytrid fungus, Batrachochytrium dendrobatidis, is associated with the emerging infectious wildlife disease chytridiomycosis. This fungus poses an overwhelming threat to global amphibian biodiversity and is contributing toward population declines and extinctions worldwide. Extremely low host-species specificity potentially threatens thousands of the 7,000+ amphibian species with infection, and hosts in additional classes of organisms have now also been identified, including crayfish and nematode worms.Soon after the discovery of B. dendrobatidis in 1999, it became apparent that this pathogen was already pandemic; dozens of countries and hundreds of amphibian species had already been exposed. The timeline of B. dendrobatidis's global emergence still remains a mystery, as does its point of origin. The reason why B. dendrobatidis seems to have only recently increased in virulence to catalyze this global disease event remains unknown, and despite 15 years of investigation, this wildlife pandemic continues primarily uncontrolled. Some disease treatments are effective on animals held in captivity, but there is currently no proven method to eradicate B. dendrobatidis from an affected habitat, nor have we been able to protect new regions from exposure despite knowledge of an approaching "wave" of B. dendrobatidis and ensuing disease.International spread of B. dendrobatidis is largely facilitated by the commercial trade in live amphibians. Chytridiomycosis was recently listed as a globally notifiable disease by the World Organization for Animal Health, but few countries, if any, have formally adopted recommended measures to control its spread. Wildlife diseases continue to emerge as a consequence of globalization, and greater effort is urgently needed to protect global health.

Using "Omics" and Integrated Multi-Omics Approaches to Guide Probiotic Selection to Mitigate Chytridiomycosis and Other Emerging Infectious Diseases.

Emerging infectious diseases in wildlife are responsible for massive population declines. In amphibians, chytridiomycosis caused by Batrachochytrium dendrobatidis, Bd, has severely affected many amphibian populations and species around the world. One promising management strategy is probiotic bioaugmentation of antifungal bacteria on amphibian skin. In vivo experimental trials using bioaugmentation strategies have had mixed results, and therefore a more informed strategy is needed to select successful probiotic candidates. Metagenomic, transcriptomic, and metabolomic methods, colloquially called “omics,” are approaches that can better inform probiotic selection and optimize selection protocols. The integration of multiple omic data using bioinformatic and statistical tools and in silico models that link bacterial community structure with bacterial defensive function can allow the identification of species involved in pathogen inhibition. We recommend using 16S rRNA gene amplicon sequencing and methods such as indicator species analysis, the Kolmogorov–Smirnov Measure, and co-occurrence networks to identify bacteria that are associated with pathogen resistance in field surveys and experimental trials. In addition to 16S amplicon sequencing, we recommend approaches that give insight into symbiont function such as shotgun metagenomics, metatranscriptomics, or metabolomics to maximize the probability of finding effective probiotic candidates, which can then be isolated in culture and tested in persistence and clinical trials. An effective mitigation strategy to ameliorate chytridiomycosis and other emerging infectious diseases is necessary; the advancement of omic methods and the integration of multiple omic data provide a promising avenue toward conservation of imperiled species.

The relationship between physiological stress and wildlife disease: consequences for health and conservation

Wildlife populations are under increasing pressure from a variety of threatening processes, ranging from climate change to habitat loss, that can incite a physiological stress response. The stress response influences immune function, with potential consequences for patterns of infection and transmission of disease among and within wildlife, domesticated animals and humans. This is concerning because stress may exacerbate the impact of disease on species vulnerable to extinction, with consequences for biodiversity conservation globally. Furthermore, stress may shape the role of wildlife in the spread of emerging infectious diseases (EID) such as Hendra virus (HeV) and Ebola virus. However, we still have a limited understanding of the influence of physiological stress on infectious disease in wildlife. We highlight key reasons why an improved understanding of the relationship between stress and wildlife disease could benefit conservation, and animal and public health, and discuss approaches for future investigation. In particular, we recommend that increased attention be given to the influence of anthropogenic stressors including climate change, habitat loss and management interventions on disease dynamics in wildlife populations.

Estimating wildlife disease dynamics in complex systems using an Approximate Bayesian Computation framework.

Emerging infectious diseases of wildlife are of increasing concern to managers and conservation policy makers, but are often difficult to study and predict due to the complexity of host-disease systems and a paucity of empirical data. We demonstrate the use of an Approximate Bayesian Computation statistical framework to reconstruct the disease dynamics of bovine tuberculosis in Kruger National Park's lion population, despite limited empirical data on the disease's effects in lions. The modeling results suggest that, while a large proportion of the lion population will become infected with bovine tuberculosis, lions are a spillover host and long disease latency is common. In the absence of future aggravating factors, bovine tuberculosis is projected to cause a lion population decline of ~3% over the next 50 years, with the population stabilizing at this new equilibrium. The Approximate Bayesian Computation framework is a new tool for wildlife managers. It allows emerging infectious diseases to be modeled in complex systems by incorporating disparate knowledge about host demographics, behavior, and heterogeneous disease transmission, while allowing inference of unknown system parameters.

Successful elimination of a lethal wildlife infectious disease in nature.

Methods to mitigate the impacts of emerging infectious diseases affecting wildlife are urgently needed to combat loss of biodiversity. However, the successful mitigation of wildlife pathogens in situ has rarely occurred. Indeed, most strategies for combating wildlife diseases remain theoretical, despite the wealth of information available for combating infections in livestock and crops. Here, we report the outcome of a 5-year effort to eliminate infection with Batrachochytrium dendrobatidis affecting an island system with a single amphibian host. Our initial efforts to eliminate infection in the larval reservoir using a direct application of an antifungal were successful ex situ but infection returned to previous levels when tadpoles with cleared infections were returned to their natal sites. We subsequently combined antifungal treatment of tadpoles with environmental chemical disinfection. Infection at four of the five pools where infection had previously been recorded was eradicated, and remained so for 2 years post-application.

Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird.

Individual heterogeneity can influence the dynamics of infectious diseases in wildlife and humans alike. Thus, recent work has sought to identify behavioural characteristics that contribute disproportionately to individual variation in pathogen acquisition (super-receiving) or transmission (super-spreading). However, it remains unknown whether the same behaviours enhance both acquisition and transmission, a scenario likely to result in explosive epidemics. Here, we examined this possibility in an ecologically relevant host-pathogen system: house finches and their bacterial pathogen, Mycoplasma gallisepticum, which causes severe conjunctivitis. We examined behaviours likely to influence disease acquisition (feeder use, aggression, social network affiliations) in an observational field study, finding that the time an individual spends on bird feeders best predicted the risk of conjunctivitis. To test whether this behaviour also influences the likelihood of transmitting M. gallisepticum, we experimentally inoculated individuals based on feeding behaviour and tracked epidemics within captive flocks. As predicted, transmission was fastest when birds that spent the most time on feeders initiated the epidemic. Our results suggest that the same behaviour underlies both pathogen acquisition and transmission in this system and potentially others. Identifying individuals that exhibit such behaviours is critical for disease management.

Estimating wildlife disease dynamics in complex systems using an Approximate Bayesian Computation framework

Emerging infectious diseases of wildlife are of increasing concern to managers and conservation policy makers, but are often difficult to study and predict due to the complexity of host–disease systems and a paucity of empirical data. We demonstrate the use of an Approximate Bayesian Computation statistical framework to reconstruct the disease dynamics of bovine tuberculosis in Kruger National Park's lion population, despite limited empirical data on the disease's effects in lions. The modeling results suggest that, while a large proportion of the lion population will become infected with bovine tuberculosis, lions are a spillover host and long disease latency is common. In the absence of future aggravating factors, bovine tuberculosis is projected to cause a lion population decline of ~3% over the next 50 years, with the population stabilizing at this new equilibrium. The Approximate Bayesian Computation framework is a new tool for wildlife managers. It allows emerging infectious diseases to be modeled in complex systems by incorporating disparate knowledge about host demographics, behavior, and heterogeneous disease transmission, while allowing inference of unknown system parameters.

The alternate role of direct and environmental transmission in fungal infectious disease in wildlife: threats for biodiversity conservation.

Emerging fungal pathogens have substantial consequences for infected hosts, as revealed by the global decline of amphibian species from the chytrid fungus. According to the “curse of the Pharaoh” hypothesis, free-living infectious stages typical of fungal pathogens lengthen the timespan of transmission. Free-living infectious stages whose lifespan exceeds the infection time of their hosts are not constrained by virulence, enabling them to persist at high levels and continue transmitting to further sensitive hosts. Using the only Mesomycetozoea fungal species that can be cultured, Sphaerothecum destruens, we obtained tractable data on infectivity and pathogen life cycle for the first time. Here, based on the outcomes of a set of infectious trials and combined with an epidemiological model, we show a high level of dependence on direct transmission in crowded, confined environments and establish that incubation rate and length of infection dictate the epidemic dynamics of fungal disease. The spread of Mesomycetozoea in the wild raise ecological concerns for a range of susceptible species including birds, amphibians and mammals. Our results shed light on the risks associated with farming conditions and highlight the additional risk posed by invasive species that are highly abundant and can act as infectious reservoir hosts.

Constructing rigorous and broad biosurveillance networks for detecting emerging zoonotic outbreaks.

Determining optimal surveillance networks for an emerging pathogen is difficult since it is not known beforehand what the characteristics of a pathogen will be or where it will emerge. The resources for surveillance of infectious diseases in animals and wildlife are often limited and mathematical modeling can play a supporting role in examining a wide range of scenarios of pathogen spread. We demonstrate how a hierarchy of mathematical and statistical tools can be used in surveillance planning help guide successful surveillance and mitigation policies for a wide range of zoonotic pathogens. The model forecasts can help clarify the complexities of potential scenarios, and optimize biosurveillance programs for rapidly detecting infectious diseases. Using the highly pathogenic zoonotic H5N1 avian influenza 2006-2007 epidemic in Nigeria as an example, we determined the risk for infection for localized areas in an outbreak and designed biosurveillance stations that are effective for different pathogen strains and a range of possible outbreak locations. We created a general multi-scale, multi-host stochastic SEIR epidemiological network model, with both short and long-range movement, to simulate the spread of an infectious disease through Nigerian human, poultry, backyard duck, and wild bird populations. We chose parameter ranges specific to avian influenza (but not to a particular strain) and used a Latin hypercube sample experimental design to investigate epidemic predictions in a thousand simulations. We ranked the risk of local regions by the number of times they became infected in the ensemble of simulations. These spatial statistics were then complied into a potential risk map of infection. Finally, we validated the results with a known outbreak, using spatial analysis of all the simulation runs to show the progression matched closely with the observed location of the farms infected in the 2006-2007 epidemic.

Risk factors associated with prevalence of antibodies to Leptospira interrogans in a metapopulation of black-tailed prairie dogs in Mexico.

Interest in the study of infectious diseases of wildlife has grown in recent decades and now focuses on understanding host-parasite dynamics and factors involved in disease occurrence. The black-tailed prairie dog (Cynomys ludovicianus) is a useful species for this type of investigation because it lives in heterogeneous landscapes where human activities take place, and its populations are structured as a metapopulation. Our goal was to determine if colony area, density, and proximity to human settlements are associated with prevalence of antibodies to Leptospira interrogans in black-tailed prairie dogs of northwestern Chihuahua State, Mexico. We captured 266 prairie dogs in 11 colonies in 2009 and analyzed 248 serum samples with the microscopic agglutination test (MAT) for antibody to any of the 12 pathogenic serovars of L. interrogans. Serologically positive test results for only serovars Bratislava, Canicola, Celledoni, and Tarassovi were considered for statistical analysis. Almost 80% of sera were positive for at least one pathogenic serovar (MAT titer ≥1∶80). The highest recorded antibody prevalences were to serovars Bratislava and Canicola. Correlation analysis showed a negative relationship between L. interrogans antibody prevalence and colony area (r = -0.125, P<0.005), suggesting that animals living in larger colonies were at a lower risk than those in smaller colonies. The correlation between the serovar Canicola and distance was negative (r = -0.171, P<0.007), and this relationship may be explained by the presence of domestic dogs associated with human dwellings. This is the first study of Leptospira spp. antibody prevalence in prairie dogs, and it provides valuable insights into the dynamics of leptospirosis in threatened wildlife species. Further studies are needed to evaluate the impact of Leptospira serovars in metapopulations of prairie dogs and other domestic and wild mammals in grassland communities.

On Zoo Grounds; Monitoring of Infectious Diseases in Wildlife for Biosecurity Countermeasure and Health Management to Zoo Animals

On Zoo Grounds; Monitoring of Infectious Diseases in Wildlife for Biosecurity Countermeasure and Health Management to Zoo Animals

Wildlife Infectious Diseases and the Early Warning System Using Zoo Networks of the World

Wildlife Infectious Diseases and the Early Warning System Using Zoo Networks of the World

Wildlife health in a rapidly changing North: focus on avian disease.

Climate‐related environmental changes have increasingly been linked to emerging infectious diseases in wildlife. The Arctic is facing a major ecological transition that is expected to substantially affect animal and human health. Changes in phenology or environmental conditions that result from climate warming may promote novel species assemblages as host and pathogen ranges expand to previously unoccupied areas. Recent evidence from the Arctic and subarctic suggests an increase in the spread and prevalence of some wildlife diseases, but baseline data necessary to detect and verify such changes are still lacking. Wild birds are undergoing rapid shifts in distribution and have been implicated in the spread of wildlife and zoonotic diseases. Here, we review evidence of current and projected changes in the abundance and distribution of avian diseases and outline strategies for future research. We discuss relevant climatic and environmental factors, emerging host–pathogen contact zones, the relationship between host condition and immune function, and potential wildlife and human health outcomes in northern regions.

Surveillance, monitoring and surveys of wildlife diseases: a public health and conservation approach

During the past decades the interest in surveillance and monitoring of wildlife diseases has grown internationally. The main reasons could be the following: a) increased size of many wild populations that host pathogens affecting humans; b) the increased economic relevance of some wildlife disease; c) the role played by infections/diseases in the conservation of some wild endangered species. According to the above-described epidemiological situations there is an international need to develop appropriate strategies for the early detection, monitoring and surveys of infectious diseases in wildlife. The paper reviews the epidemiological assumptions on which disease surveillance, monitoring and survey are, or should be, based. The main conclusions are: 1) wildlife disease surveillance and monitoring are long lasting activities that should be implemented when legal bases are available; 2) a wildlife disease introduced in a free area is more likely to be early detected using passive rather than active surveillance; 3) the definition of the suspect largely affects the sensitivity of the whole passive surveillance; thus the suspected case definition should be modulated according to the level of risk; 4) in both active surveillance and monitoring, sampling plays an important role. The sensitivity of any active surveillance/monitoring system is highly dependent from the sampling unit that we define as: the host subpopulation, whose size can maintain the pathogen during a defined inter-sampling interval . Such definition merges the ecological, epidemiological and mathematical approaches aimed in controlling or eradicating infections in both domestic and wildlife; 5) When dealing with the conservation-disease interface, a standardized risk assessment procedure including risk mitigation has to become the rule. Download the complete issue.

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.

Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome

Pathogens can affect host behaviour in ways that influence disease transmission as well as survival and fitness for both host and pathogen. Hibernating bats with white-nose syndrome (WNS) show a number of unusual behaviours including increased frequency of arousal from torpor, altered roosting behaviour and premature emergence. However, mechanisms underlying these patterns are not understood, and the behaviour of bats with WNS has not been examined systematically. Three hypotheses could explain increased arousal frequency. Bats may arouse to (1) groom in response to skin infection, (2) drink to offset dehydration or (3) increase activity, possibly in an attempt to access resources, avoid a source of infection or limit the risk of infecting relatives. We tested these hypotheses with captive little brown bats, Myotis lucifugus, inoculated with Pseudogymnoascus destructans, the fungus that causes WNS. In contrast to predictions of all three hypotheses, bats inoculated with the fungus tended to be less active than controls during arousals from torpor and did not increase grooming or visits to the water source in their enclosures. However, bats showed a dramatic reduction in clustering behaviour as infection progressed. Reduced activity and clustering could represent adaptive, maladaptive or pathological responses. Reduced activity could be an energy-saving mechanism or a pathological consequence of infection while reduced clustering could have beneficial or detrimental consequences for transmission, energetics, water balance and survival. Our results highlight the need for studies of host behaviour to understand dynamics of wildlife infectious diseases.

Microscopic Aquatic Predators Strongly Affect Infection Dynamics of a Globally Emerged Pathogen

Research on emerging infectious wildlife diseases has placed particular emphasis on host-derived barriers to infection and disease. This focus neglects important extrinsic determinants of the host/pathogen dynamic, where all barriers to infection should be considered when ascertaining the determinants of infectivity and pathogenicity of wildlife pathogens. Those pathogens with free-living stages, such as fungi causing catastrophic wildlife declines on a global scale, must confront lengthy exposure to environmental barriers before contact with an uninfected host. Hostile environmental conditions therefore have the ability to decrease the density of infectious particles, reducing the force of infection and ameliorating the impact as well as the probability of establishing an infection. Here we show that, in nature, the risk of infection and infectious burden of amphibians infected by the chytrid fungus Batrachochytrium dendrobatidis (Bd) have a significant, site-specific component, and that these correlate with the microfauna present at a site. Experimental infections show that aquatic microfauna can rapidly lower the abundance and density of infectious stages by consuming Bd zoospores, resulting in a significantly reduced probability of infection in anuran tadpoles. Our findings offer new perspectives for explaining the divergent impacts of Bd infection in amphibian assemblages and contribute to our understanding of ecosystem resilience to colonization by novel pathogens.

Emerging Infectious Diseases of Wildlife and Species Conservation.

There has been an increase in the emergence and reemergence of human infectious diseases on a global scale, and zoonotic diseases in which wildlife serves as the reservoir are a large contributing factor. Faced with this situation, there is a necessity to create integrated prevention strategies and predictive models to determine the sites most vulnerable to the emergence of new zoonoses. Cases have been documented in which pathogens responsible for infectious diseases in wild species have been readily transmitted between hosts and have threatened vulnerable declining populations. Habitat destruction and man-made changes in the landscape together with the introduction of alien species are significant environmental variables that affect the ecology of infectious diseases. Thus, the loss of biodiversity is illustrated to be related to both the emergence of new or the exacerbation of existing vector-borne zoonotic diseases through mechanisms such as the loss of the dilution effect and ecological release and simplification. Hence, it is important to consider this factor when assessing disease risk and disease prevention in domestic animals and humans. Diseases like leptospirosis in which water plays an important role are ecosystem health diseases; in fact, the reported higher prevalence of Leptospira spp. in river otters in southern Chile compared with species less adapted to aquatic environments and with terrestrial domestic carnivores provides evidence that man-made landscape alterations, including the introduction of alien species, has exacerbated the transmission and prevalence of leptospirosis in wildlife and thus the risk of human infection.

TEMPORAL VARIATION IN BAT WING DAMAGE IN THE ABSENCE OF WHITE-NOSE SYNDROME

White-nose syndrome (WNS) is an emerging infectious wildlife disease that has killed more than 5 million bats in the eastern United States since its discovery in winter 2006. The disease is associated with a cold-adapted fungus that infects bats during winter hibernation. Wing damage has been documented in bats with WNS and could become a useful screening tool for determining whether samples should be submitted for testing. However, because there are no historic records, to our knowledge, of wing damage before the emergence of WNS, it is unknown what types of grossly observable wing damage, if any, are specific to WNS. To address this knowledge gap, we inspected the wings of 1,327 bat carcasses collected in Illinois from 2005 and 2008-2010, then used Akaike information criterion to evaluate generalized linear models of the frequencies of different categories of wing damage using age, sex, year, and season as predictors in big brown bats (Eptesicus fuscus). Wing discoloration was best predicted by year and season. There were no clear predictors for other categories of wing damage. We found that about one-fourth of big brown bats surveyed from this presumptive WNS-negative sample had moderate or severe wing damage. We encourage further studies of the relationship between WNS and wing damage to better understand which categories of damage are to be expected in the absence of WNS in susceptible species.

React or wait: which optimal culling strategy to control infectious diseases in wildlife

We applied optimal control theory to an SI epidemic model to identify optimal culling strategies for diseases management in wildlife. We focused on different forms of the objective function, including linear control, quadratic control, and control with limited amount of resources. Moreover, we identified optimal solutions under different assumptions on disease-free host dynamics, namely: self-regulating logistic growth, Malthusian growth, and the case of negligible demography. We showed that the correct characterization of the disease-free host growth is crucial for defining optimal disease control strategies. By analytical investigations of the model with negligible demography, we demonstrated that the optimal strategy for the linear control can be either to cull at the maximum rate at the very beginning of the epidemic (reactive culling) when the culling cost is low, or never to cull, when culling cost is high. On the other hand, in the cases of quadratic control or limited resources, we demonstrated that the optimal strategy is always reactive. Numerical analyses for hosts with logistic growth showed that, in the case of linear control, the optimal strategy is always reactive when culling cost is low. In contrast, if the culling cost is high, the optimal strategy is to delay control, i.e. not to cull at the onset of the epidemic. Finally, we showed that for diseases with the same basic reproduction number delayed control can be optimal for acute infections, i.e. characterized by high disease-induced mortality and fast dynamics, while reactive control can be optimal for chronic ones.