Disease In Wildlife Populations Research Articles

DNA Extraction Method Affects the Detection of a Fungal Pathogen in Formalin-Fixed Specimens Using qPCR.

Museum collections provide indispensable repositories for obtaining information about the historical presence of disease in wildlife populations. The pathogenic amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has played a significant role in global amphibian declines, and examining preserved specimens for Bd can improve our understanding of its emergence and spread. Quantitative PCR (qPCR) enables Bd detection with minimal disturbance to amphibian skin and is significantly more sensitive to detecting Bd than histology; therefore, developing effective qPCR methodologies for detecting Bd DNA in formalin-fixed specimens can provide an efficient and effective approach to examining historical Bd emergence and prevalence. Techniques for detecting Bd in museum specimens have not been evaluated for their effectiveness in control specimens that mimic the conditions of animals most likely to be encountered in museums, including those with low pathogen loads. We used American bullfrogs (Lithobates catesbeianus) of known infection status to evaluate the success of qPCR to detect Bd in formalin-fixed specimens after three years of ethanol storage. Our objectives were to compare the most commonly used DNA extraction method for Bd (PrepMan, PM) to Macherey-Nagel DNA FFPE (MN), test optimizations for Bd detection with PM, and provide recommendations for maximizing Bd detection. We found that successful detection is relatively high (80–90%) when Bd loads before formalin fixation are high, regardless of the extraction method used; however, at lower infection levels, detection probabilities were significantly reduced. The MN DNA extraction method increased Bd detection by as much as 50% at moderate infection levels. Our results indicate that, for animals characterized by lower pathogen loads (i.e., those most commonly encountered in museum collections), current methods may underestimate the proportion of Bd-infected amphibians. Those extracting DNA from archived museum specimens should ensure that the techniques they are using are known to provide high-quality throughput DNA for later analysis.

Effective Coordination and Management of Emerging Infectious Diseases in Wildlife Populations.

A transdisciplinary, One Health approach is proposed for the coordination of wildlife health diagnostics, research, and policy development. In some countries, considerable effort has been made to establish specific activities including surveillance and integration of wildlife health within diagnostic and research laboratories. We suggest that some of these activities can be improved and many countries still require national structures to deal with wildlife disease investigation and management. We also suggest that scientists in this field should actively engage with national and international organizations and conferences to influence the development of policy, diagnostics, research, and management of emerging wildlife diseases.

Serological profile of foot-and-mouth disease in wildlife populations of West and Central Africa with special reference to Syncerus caffer subspecies.

The role which West and Central African wildlife populations might play in the transmission dynamics of FMD is not known nor have studies been performed in order to assess the distribution and prevalence of FMD in wild animal species inhabiting those specific regions of Africa. This study reports the FMD serological profile extracted from samples (n = 696) collected from wildlife of West and Central Africa between 1999 and 2003. An overall prevalence of FMDV NSP reactive sera of 31.0% (216/696) was estimated, where a significant difference in seropositivity (p = 0.000) was reported for buffalo (64.8%) as opposed to other wild animal species tested (17.8%). Different levels of exposure to the FMDV resulted for each of the buffalo subspecies sampled (p = 0.031): 68.4%, 50.0% and 0% for Nile Buffalo, West African Buffalo and African Forest Buffalo, respectively. The characterisation of the FMDV serotypes tested for buffalo found presence of antibodies against all the six FMDV serotypes tested, although high estimates for type O and SAT 3 were reported for Central Africa. Different patterns of reaction to the six FMDV serotypes tested were recorded, from sera only positive for a single serotype to multiple reactivities. The results confirmed that FMDV circulates in wild ruminants populating both West and Central Africa rangelands and in particular in buffalo, also suggesting that multiple FMDV serotypes might be involved with type O, SAT 2 and SAT 1 being dominant. Differences in serotype and spill-over risk between wildlife and livestock likely reflect regional geography, historical circulation and differing trade and livestock systems.

Demographic processes drive increases in wildlife disease following population reduction.

Population reduction is often used as a control strategy when managing infectious diseases in wildlife populations in order to reduce host density below a critical threshold. However, population reduction can disrupt existing social and demographic structures leading to changes in observed host behaviour that may result in enhanced disease transmission. Such effects have been observed in several disease systems, notably badgers and bovine tuberculosis. Here we characterise the fundamental properties of disease systems for which such effects undermine the disease control benefits of population reduction.By quantifying the size of response to population reduction in terms of enhanced transmission within a generic non-spatial model, the properties of disease systems in which such effects reduce or even reverse the disease control benefits of population reduction are identified. If population reduction is not sufficiently severe, then enhanced transmission can lead to the counter intuitive perturbation effect, whereby disease levels increase or persist where they would otherwise die out. Perturbation effects are largest for systems with low levels of disease, e.g. low levels of endemicity or emerging disease.Analysis of a stochastic spatial meta-population model of demography and disease dynamics leads to qualitatively similar conclusions. Moreover, enhanced transmission itself is found to arise as an emergent property of density dependent dispersal in such systems. This spatial analysis also shows that, below some threshold, population reduction can rapidly increase the area affected by disease, potentially expanding risks to sympatric species.Our results suggest that the impact of population reduction on social and demographic structures is likely to undermine disease control in many systems, and in severe cases leads to the perturbation effect. Social and demographic mechanisms that enhance transmission following population reduction should therefore be routinely considered when designing control programmes.

Rinderpest: the veterinary perspective on eradication.

Rinderpest was a devastating disease of livestock responsible for continent-wide famine and poverty. Centuries of veterinary advances culminated in 2011 with the UN Food and Agriculture Organization and the World Organization for Animal Health declaring global eradication of rinderpest; only the second disease to be eradicated and the greatest veterinary achievement of our time. Conventional control measures, principally mass vaccination combined with zoosanitary procedures, led to substantial declines in the incidence of rinderpest. However, during the past decades, innovative strategies were deployed for the last mile to overcome diagnostic and surveillance challenges, unanticipated variations in virus pathogenicity, circulation of disease in wildlife populations and to service remote and nomadic communities in often-unstable states. This review provides an overview of these challenges, describes how they were overcome and identifies key factors for this success.

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.

Integrating Survey and Molecular Approaches to Better Understand Wildlife Disease Ecology

Infectious wildlife diseases have enormous global impacts, leading to human pandemics, global biodiversity declines and socio-economic hardship. Understanding how infection persists and is transmitted in wildlife is critical for managing diseases, but our understanding is limited. Our study aim was to better understand how infectious disease persists in wildlife populations by integrating genetics, ecology and epidemiology approaches. Specifically, we aimed to determine whether environmental or host factors were stronger drivers of Salmonella persistence or transmission within a remote and isolated wild pig (Sus scrofa) population. We determined the Salmonella infection status of wild pigs. Salmonella isolates were genotyped and a range of data was collected on putative risk factors for Salmonella transmission. We a priori identified several plausible biological hypotheses for Salmonella prevalence (cross sectional study design) versus transmission (molecular case series study design) and fit the data to these models. There were 543 wild pig Salmonella observations, sampled at 93 unique locations. Salmonella prevalence was 41% (95% confidence interval [CI]: 37–45%). The median Salmonella DICE coefficient (or Salmonella genetic similarity) was 52% (interquartile range [IQR]: 42–62%). Using the traditional cross sectional prevalence study design, the only supported model was based on the hypothesis that abundance of available ecological resources determines Salmonella prevalence in wild pigs. In the molecular study design, spatial proximity and herd membership as well as some individual risk factors (sex, condition score and relative density) determined transmission between pigs. Traditional cross sectional surveys and molecular epidemiological approaches are complementary and together can enhance understanding of disease ecology: abundance of ecological resources critical for wildlife influences Salmonella prevalence, whereas Salmonella transmission is driven by local spatial, social, density and individual factors, rather than resources. This enhanced understanding has implications for the control of diseases in wildlife populations. Attempts to manage wildlife disease using simplistic density approaches do not acknowledge the complexity of disease ecology.

Transmission of infectious diseases en route to habitat hotspots.

BackgroundThe spread of infectious diseases in wildlife populations is influenced by patterns of between-host contacts. Habitat “hotspots” - places attracting a large numbers of individuals or social groups - can significantly alter contact patterns and, hence, disease propagation. Research on the importance of habitat hotspots in wildlife epidemiology has primarily focused on how inter-individual contacts occurring at the hotspot itself increase disease transmission. However, in territorial animals, epidemiologically important contacts may primarily occur as animals cross through territories of conspecifics en route to habitat hotspots. So far, the phenomenon has received little attention. Here, we investigate the importance of these contacts in the case where infectious individuals keep visiting the hotspots and in the case where these individuals are not able to travel to the hotspot any more.Methodology and Principal FindingsWe developed a simulation epidemiological model to investigate both cases in a scenario when transmission at the hotspot does not occur. We find that (i) hotspots still exacerbate epidemics, (ii) when infectious individuals do not travel to the hotspot, the most vulnerable individuals are those residing at intermediate distances from the hotspot rather than nearby, and (iii) the epidemiological vulnerability of a population is the highest when the number of hotspots is intermediate.Conclusions and SignificanceBy altering animal movements in their vicinity, habitat hotspots can thus strongly increase the spread of infectious diseases, even when disease transmission does not occur at the hotspot itself. Interestingly, when animals only visit the nearest hotspot, creating additional artificial hotspots, rather than reducing their number, may be an efficient disease control measure.

Models predict that culling is not a feasible strategy to prevent extinction of Tasmanian devils from facial tumour disease

Summary1. Culling, either of all animals or infected animals only, is often suggested as a way of managing infectious diseases in wildlife populations. However, replicated experiments to investigate culling strategies are often impractical because of costs and ethical issues. Modelling therefore has an important role. Here, we describe a suite of models to investigate the culling of infected animals to control an infectious cancer in the Tasmanian devil Sarcophilus harrisii.2. The Tasmanian devil is threatened by an infectious cancer, Tasmanian devil facial tumour disease. We developed deterministic susceptible, exposed and infectious (SEI) models with differing ways of incorporating the time delays inherent in the system. We used these to investigate the effectiveness for disease suppression of various strategies for the removal of infected animals.3. The predictions of our models were consistent with empirical time series on host population dynamics and disease prevalence. This implies that they are capturing the essential dynamics of the system to a plausible extent.4. A previous empirical study has shown that removals every 3 months did not appear to be sufficient to suppress disease in a semi‐isolated infected population. Our models are in accordance with this observed result. The models further predict that while more frequent removals are more likely to be effective, the removal rate necessary to successfully eliminate disease may be too high to be achievable.5. Synthesis and applications.Our results, in association with a previous experimental study, show that culling is unlikely to be a feasible strategy for managing Tasmanian devil facial tumour disease. Similar conclusions have been reached in studies of other wildlife diseases. We conclude that culling is rarely appropriate for controlling wildlife diseases and should only be attempted if models predict that it will be effective.

The status of tuberculosis in European wild mammals

ABSTRACT Tuberculosis (TB) is a chronic disease caused by Mycobacterium bovis and related members of the Mycobacterium tuberculosis complex. Infection affects not only cattle but also other livestock species, companion animals and wild mammals. Humans are also susceptible; hence, zoonotic infection is a driver for disease control in animal hosts. As bovine TB prevalence has been reduced in livestock, the relative epidemiological and socio‐economic importance of wildlife reservoirs has increased, and there is a need for disease management strategies. We review the current status of TB in European wild mammals, identifying epidemiological trends and areas for future research and management. TB has a complex epidemiology, which may involve multiple hosts, and is influenced by climate and habitat. Consequently, the role of wild and domestic hosts in the epidemiology of TB varies among regions. In Europe, there are three regional examples of M. bovis maintenance hosts: the Eurasian badger Meles meles in Great Britain and Ireland, the Eurasian wild boar Sus scrofa in the Iberian Peninsula and deer belonging to the subfamily Cervinae in several European regions. In other parts of Europe, these species are currently regarded as spillover hosts, although in time their status may change depending on local or regional risk factors. Nevertheless, in most situations, the relative contribution of wild mammals to M. bovis infection in cattle is still a matter of debate. Also, the outcome of management interventions to control disease in wildlife populations may be complex and counter‐intuitive. As our knowledge of disease dynamics in wild mammals improves, options for disease control in wildlife reservoirs, such as vaccination, improved biosecurity and population management, are likely to broaden. In order to evaluate our existing control options, we must monitor the effects of interventions on TB occurrence in the affected regions of Europe and share our collective experiences.

An agent-based model of red colobus resources and disease dynamics implicates key resource sites as hot spots of disease transmission

The effect of anthropogenic landscape change on disease in wildlife populations represents a growing conservation and public health concern. Red colobus monkeys ( Procolobus rufomitratus), an endangered primate species, are particularly susceptible to habitat alteration and have been the focus of a great deal of disease and ecological research as a result. To infer how landscape changes can affect host and parasite dynamics, a spatially explicit agent-based model is created to simulate movement and foraging of this primate, based on a resource landscape estimated from extensive plot-derived tree population data from Kibale National Park, Uganda. Changes to this resource landscape are used to simulate effects of anthropogenic forest change. With each change in the landscape, disease outcomes within the simulated red colobus population are monitored using a hypothetical microparasite with a directly transmitted life cycle. The model predicts an optimal distribution of resources which facilitates the spread of an infectious agent through the simulated population. The density of resource rich sites and the overall heterogeneity of the landscape are important factors contributing to this spread. The characteristics of this optimal distribution are similar to those of logged sections of forest adjacent to our study area.

BOVINE TUBERCULOSIS IN ETHIOPIAN WILDLIFE

Bovine tuberculosis (BTB) is endemic in Ethiopian cattle. However, the status of the disease in wildlife populations that often share habitat with livestock is unknown. We screened for BTB in wildlife in five regions in Ethiopia. Blood and tissue samples from 133 mammals of 28 species were collected from 2006 to 2008. We used a rapid serology test (RT) based on lateral flow technology, and performed culture of lymph node specimens inoculated onto Lowenstein-Jensen and Middlebrook 7H11 media. Acid-fast colonies were further analyzed by molecular typing. Sera from 20 of 87 animals (23%) were positive for BTB by RT; acid-fast bacilli were cultured from 29 of 89 animals (32.5%). None of the positive cultures yielded mycobacteria from the Mycobacterium tuberculosis complex but many environmental mycobacteria were isolated. Among these, Mycobacterium terrae was the most common. We demonstrated a high prevalence of environmental mycobacteria in wildlife, the role of which is unknown. Flagship rare endemic species such as the mountain nyala (Tragelaphus buxtoni) and the Ethiopian wolf (Canis simensis) may be at risk for BTB. We also assessed the utility of RT for field purposes.

Amphibian Chemical Defense: Antifungal Metabolites of the Microsymbiont Janthinobacterium lividum on the Salamander Plethodon cinereus

Disease has spurred declines in global amphibian populations. In particular, the fungal pathogen Batrachochytrium dendrobatidis has decimated amphibian diversity in some areas unaffected by habitat loss. However, there is little evidence to explain how some amphibian species persist despite infection or even clear the pathogen beyond detection. One hypothesis is that certain bacterial symbionts on the skin of amphibians inhibit the growth of the pathogen. An antifungal strain of Janthinobacterium lividum, isolated from the skin of the red-backed salamander Plethodon cinereus, produces antifungal metabolites at concentrations lethal to B. dendrobatidis. Antifungal metabolites were identified by using reversed phase high performance liquid chromatography, high resolution mass spectrometry, nuclear magnetic resonance, and UV-Vis spectroscopy and tested for efficacy of inhibiting the pathogen. Two metabolites, indole-3-carboxaldehyde and violacein, inhibited the pathogen's growth at relatively low concentrations (68.9 and 1.82 microM, respectively). Analysis of fresh salamander skin confirmed the presence of J. lividum and its metabolites on the skin of host salamanders in concentrations high enough to hinder or kill the pathogen (51 and 207 microM, respectively). These results support the hypothesis that cutaneous, mutualistic bacteria play a role in amphibian resistance to fungal disease. Exploitation of this biological process may provide long-term resistance to B. dendrobatidis for vulnerable amphibians and serve as a model for managing future emerging diseases in wildlife populations.

Spatial Epidemiology and GIS in Marine Mammal Conservation Medicine and Disease Research

The use of spatial epidemiology and geographical information systems (GIS) facilitates the incorporation of spatial relationships into epidemiological investigations of marine mammal diseases and conservation medicine. Spatial epidemiology is the study of the spatial variation in disease risk or incidence and explicitly addresses spatial structures and functions that factor into disease. The GIS consists of input, management, analysis, and presentation of spatial disease data and can act as an integrative tool so that a range of varied data sources can be combined to describe different environmental aspects of wild animals and their diseases. The use of modern spatial analyses and GIS is becoming well developed in the field of marine mammal ecology and biology, but has just recently started to gain more use in disease research. The use of GIS methodology and spatial analysis in nondisease marine mammal studies is briefly discussed, while examples of the specific uses of these tools in mapping, surveillance and monitoring, disease cluster detection, identification of environmental predictors of disease in wildlife populations, risk assessment, and modeling of diseases, is presented. Marine mammal disease investigations present challenges, such as less consistent access to animals for sampling, fewer baseline data on diseases in wild populations, and less robust epidemiologic study designs, but several recommendations for future research are suggested. Since location is an integral part of investigating disease, spatial epidemiology and GIS should be incorporated as a data management and analysis tool in the study of marine mammal diseases and conservation medicine.

Wildlife disease can put conservation at risk

conservation at risk SIR — In their Letter ‘Global trends in emerging infectious diseases’ (Nature 451, 990–993; 2008), Kate Jones and colleagues reveal that emerging human infectious diseases are becoming globally more prevalent, particularly those originating from wildlife. Even when cases of all other transmission types started to decrease during 1990–2000 compared with previous decades, cases of wildlife-associated human diseases continued their upward trend. The authors highlight the implications for conservation, advocating more monitoring and preservation of areas rich in biodiversity to counter it. They do not mention the social and psychological effect this proliferation of wildlife-associated zoonoses could have. Such diseases are widely perceived as a threat to humans (see, for example, W. D. Newmark et al. Biol. Conserv. 63, 177–183; 1993). Negative interactions with wildlife tend to stifle support for conservation policies and initiatives. The increasing prevalence of such diseases could stand in the way of the very conservation initiatives that Jones and colleagues are recommending to protect human health. Widespread disease in wildlife populations could encourage humans to view wild animals as pests, instead of as resources to be protected and enjoyed. Risk-perception research on wildlife-associated zoonoses would confirm the extent to which this shift has occurred. Such research would also identify gaps between the public’s attitudes and epidemiological assessments, and would help to gauge the extent of public support for different proactive management plans. This would enable wildlife managers to decide which plans would be the most politically and socially viable, as well as the best ways to inform the public about them. Darrick T. Evensen Department of Natural Resources, Cornell University, Ithaca, New York 14853, USA

Vaccinating badgers ( Meles meles) against Mycobacterium bovis: the ecological considerations

Bovine tuberculosis (TB) is a serious zoonotic disease, which despite a largely successful test and slaughter programme has persisted in cattle herds in parts of the UK. The badger ( Meles meles) is widely considered to represent a significant wildlife reservoir for the transmission of Mycobacterium bovis to cattle, and has been the subject of a variety of culling strategies since the mid 1970s. Nevertheless, the incidence of herd breakdowns has continued to rise, and the efficacy of culling is currently the subject of a large-scale field trial. One potential alternative tool for the management of disease in wildlife populations is vaccination. However, the successful development of an effective vaccine and a strategy for its delivery will require careful consideration of the practical constraints imposed by ecological factors. In the current paper, we discuss relevant ecological and epidemiological characteristics of badger populations and practical aspects of vaccine delivery in the field.

A mathematical model for the control of diseases in wildlife populations: culling, vaccination and fertility control

Recent advances have permitted the red fox ( Vulpes vulpes) to be vaccinated against rabies in order to control the European epidemic. Vaccination is also the preferred long-term strategy for controlling bovine tuberculosis ( Mycobacterium bovis) (TB) in the European badger ( Meles meles) in England. We discuss a model to compare the efficacy of various disease control strategies, including temporary and permanent sterilisation. By using rabies and TB as examples of acute and chronic diseases, the model shows that lethal control can be more effective at disease eradication in an isolated population than vaccination. This is due to the birth of larger numbers of susceptible individuals during a vaccination campaign, which makes it harder to keep the population below the critical threshold density. This difference was very marked for the progressive disease of tuberculosis. The inclusion of an abortifacient increased the chances of disease control to levels close to that of lethal control. If the abortifacient is replaced by a permanent contraceptive then the chances of disease eradication and population extinction were very similar to that of lethal control, since the birth of susceptibles is now much reduced. These results are also of relevance in the control of wildlife diseases in threatened populations or species.

Mange epizootic in white-nosed coatis in western Mexico.

From November of 1994 to June of 1996 an epizootic of mange, probably caused by the mite Notoedres cati, occurred in white-nosed coatis (Nasua narica) in the tropical dry forests of the Chamela-Cuixmala Biosphere Reserve in western Mexico. A monitoring scheme to determine the extent and severity of the epizootic within coatis was implemented. Trapping periods and transects were conducted for 2 yr. To control the spread of the disease, all captured infected coatis were either euthanized or treated with acaricides such as Butox and Ivomec-F, depending on the severity of their infection. Four other species of wild mammals and feral cats had skin conditions resembling mange. A more severe problem with the disease was predicted and later confirmed in the less isolated areas of the reserve, with a higher density of coatis. Our results indicate that epizootics may be more prone to occur in areas with greater fragmentation and less isolation from anthropogenic influence. Interestingly, although there was an apparently severe impact of the mange epizootic in the coati population, the long-term impact of the disease is unknown but appears to be negligible. So in order to understand the role of diseases in wildlife populations, long-term experimental studies are required.

Environmentally driven epizootics

Environmental conditions can be the driving force behind an epizootic. Environmental changes may favor growth of a particular species, which results in increased contact rates and spread of a disease. We examine this particular phenomenon in SI and SIS models and use it to explain the possible disease outbreaks in nature. Either infected individuals recover from the disease ( SIS model) or suffer disease fatalities ( SI model). Epizootic models for a single population are examined where contact rate depends on population size. A reproductive number R is defined that depends on environmental carrying capacity. The single-population models are coupled to form three different two-species models with intra- and interspecies contact rates that depend on the population sizes of both populations. The stability results show that it is possible for the disease to drive one of the populations to extinction, the one with disease fatalities. The surviving species serves as a reservoir for the disease. Single- and two-species epizootic models are examined in a particular case where the contact rates are assumed to be constant. This leads to a new definition for the contact rate. A complete global analysis is possible in these latter cases. The results are compared and contrasted with the models with variable contact rates. The prototype for the models is the spread of disease in wildlife populations, which includes such diseases as plague or Lyme disease.