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1.  Demographic variation in the U.K. serotine bat: filling gaps in knowledge for management 
Ecology and Evolution  2014;4(19):3820-3829.
Species of conservation concern, or those in conflict with man, are most efficiently managed with an understanding of their population dynamics. European bats exemplify the need for successful and cost-effective management for both reasons, often simultaneously. Across Europe, bats are protected, and the concept of Favourable Conservation Status (FCS) is used as a key tool for the assessment and licensing of disruptive actions to populations. However, for efficient decision-making, this assessment requires knowledge on the demographic rates and long-term dynamics of populations. We used capture–mark–recapture to describe demographic rates for the Serotine bat (Eptesicus serotinus) at two sites in England and investigate the transition rates between three stages: juveniles, immatures, and breeders. We then use these rates in an individual-based population dynamics model to investigate the expected trajectories for both populations. Our results demonstrate for the first time the presence and scale of temporal variation in this species' demography. We describe the lengthy prereproductive period (3.5 years) that female Serotines experience. Finally, we show how site-specific variation in demographic rates can produce divergent population trajectories. Effective management of European bat populations can be achieved through the understanding of life histories, and local demographic rates and population dynamics, in order to anticipate the presence of source and sink sites in the landscape. Using the Serotine bat in England, we show that these can be obtained from rigorous and systematic studies of long-term demographic datasets.
doi:10.1002/ece3.1174
PMCID: PMC4301045  PMID: 25614796
Eptesicus serotinus; Favourable Conservation Status; prereproductive delay; reproduction; survival; temporal variation
2.  Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife–disease interactions 
In animal populations, males are commonly more susceptible to disease-induced mortality than females. However, three competing mechanisms can cause this sex bias: weak males may simultaneously be more prone to exposure to infection and mortality; being ‘male’ may be an imperfect proxy for the underlying driver of disease-induced mortality; or males may experience increased severity of disease-induced effects compared with females. Here, we infer the drivers of sex-specific epidemiology by decomposing fixed mortality rates into mortality trajectories and comparing their parameters. We applied Bayesian survival trajectory analysis to a 22-year longitudinal study of a population of badgers (Meles meles) naturally infected with bovine tuberculosis (bTB). At the point of infection, infected male and female badgers had equal mortality risk, refuting the hypothesis that acquisition of infection occurs in males with coincidentally high mortality. Males and females exhibited similar levels of heterogeneity in mortality risk, refuting the hypothesis that maleness is only a proxy for disease susceptibility. Instead, sex differences were caused by a more rapid increase in male mortality rates following infection. Males are indeed more susceptible to bTB, probably due to immunological differences between the sexes. We recommend this mortality trajectory approach for the study of infection in animal populations.
doi:10.1098/rspb.2014.0526
PMCID: PMC4123697  PMID: 25056621
sex differences; disease; Bayesian; survival analysis; badgers; tuberculosis
3.  Changes in the Distribution of Red Foxes (Vulpes vulpes) in Urban Areas in Great Britain: Findings and Limitations of a Media-Driven Nationwide Survey 
PLoS ONE  2014;9(6):e99059.
Urbanization is one of the major forms of habitat alteration occurring at the present time. Although this is typically deleterious to biodiversity, some species flourish within these human-modified landscapes, potentially leading to negative and/or positive interactions between people and wildlife. Hence, up-to-date assessment of urban wildlife populations is important for developing appropriate management strategies. Surveying urban wildlife is limited by land partition and private ownership, rendering many common survey techniques difficult. Garnering public involvement is one solution, but this method is constrained by the inherent biases of non-standardised survey effort associated with voluntary participation. We used a television-led media approach to solicit national participation in an online sightings survey to investigate changes in the distribution of urban foxes in Great Britain and to explore relationships between urban features and fox occurrence and sightings density. Our results show that media-based approaches can generate a large national database on the current distribution of a recognisable species. Fox distribution in England and Wales has changed markedly within the last 25 years, with sightings submitted from 91% of urban areas previously predicted to support few or no foxes. Data were highly skewed with 90% of urban areas having <30 fox sightings per 1000 people km−2. The extent of total urban area was the only variable with a significant impact on both fox occurrence and sightings density in urban areas; longitude and percentage of public green urban space were respectively, significantly positively and negatively associated with sightings density only. Latitude, and distance to nearest neighbouring conurbation had no impact on either occurrence or sightings density. Given the limitations associated with this method, further investigations are needed to determine the association between sightings density and actual fox density, and variability of fox density within and between urban areas in Britain.
doi:10.1371/journal.pone.0099059
PMCID: PMC4053368  PMID: 24919063
4.  BCG Vaccination Reduces Risk of Tuberculosis Infection in Vaccinated Badgers and Unvaccinated Badger Cubs 
PLoS ONE  2012;7(12):e49833.
Wildlife is a global source of endemic and emerging infectious diseases. The control of tuberculosis (TB) in cattle in Britain and Ireland is hindered by persistent infection in wild badgers (Meles meles). Vaccination with Bacillus Calmette-Guérin (BCG) has been shown to reduce the severity and progression of experimentally induced TB in captive badgers. Analysis of data from a four-year clinical field study, conducted at the social group level, suggested a similar, direct protective effect of BCG in a wild badger population. Here we present new evidence from the same study identifying both a direct beneficial effect of vaccination in individual badgers and an indirect protective effect in unvaccinated cubs. We show that intramuscular injection of BCG reduced by 76% (Odds ratio = 0.24, 95% confidence interval (CI) 0.11–0.52) the risk of free-living vaccinated individuals testing positive to a diagnostic test combination to detect progressive infection. A more sensitive panel of tests for the detection of infection per se identified a reduction of 54% (Odds ratio = 0.46, 95% CI 0.26–0.88) in the risk of a positive result following vaccination. In addition, we show the risk of unvaccinated badger cubs, but not adults, testing positive to an even more sensitive panel of diagnostic tests decreased significantly as the proportion of vaccinated individuals in their social group increased (Odds ratio = 0.08, 95% CI 0.01–0.76; P = 0.03). When more than a third of their social group had been vaccinated, the risk to unvaccinated cubs was reduced by 79% (Odds ratio = 0.21, 95% CI 0.05–0.81; P = 0.02).
doi:10.1371/journal.pone.0049833
PMCID: PMC3521029  PMID: 23251352
5.  Comparing Badger (Meles meles) Management Strategies for Reducing Tuberculosis Incidence in Cattle 
PLoS ONE  2012;7(6):e39250.
Bovine tuberculosis (bTB), caused by Mycobacterium bovis, continues to be a serious economic problem for the British cattle industry. The Eurasian badger (Meles meles) is partly responsible for maintenance of the disease and its transmission to cattle. Previous attempts to manage the disease by culling badgers have been hampered by social perturbation, which in some situations is associated with increases in the cattle herd incidence of bTB. Following the licensing of an injectable vaccine, we consider the relative merits of management strategies to reduce bTB in badgers, and thereby reduce cattle herd incidence. We used an established simulation model of the badger-cattle-TB system and investigated four proposed strategies: business as usual with no badger management, large-scale proactive badger culling, badger vaccination, and culling with a ring of vaccination around it. For ease of comparison with empirical data, model treatments were applied over 150 km2 and were evaluated over the whole of a 300 km2 area, comprising the core treatment area and a ring of approximately 2 km. The effects of treatment were evaluated over a 10-year period comprising treatment for five years and the subsequent five year period without treatment. Against a background of existing disease control measures, where 144 cattle herd incidents might be expected over 10 years, badger culling prevented 26 cattle herd incidents while vaccination prevented 16. Culling in the core 150 km2 plus vaccination in a ring around it prevented about 40 cattle herd breakdowns by partly mitigating the negative effects of culling, although this approach clearly required greater effort. While model outcomes were robust to uncertainty in parameter estimates, the outcomes of culling were sensitive to low rates of land access for culling, low culling efficacy, and the early cessation of a culling strategy, all of which were likely to lead to an overall increase in cattle disease.
doi:10.1371/journal.pone.0039250
PMCID: PMC3384660  PMID: 22761746
6.  Bacillus Calmette-Guérin vaccination reduces the severity and progression of tuberculosis in badgers 
Control of bovine tuberculosis (TB) in cattle has proven particularly challenging where reservoirs of infection exist in wildlife populations. In Britain and Ireland, control is hampered by a reservoir of infection in Eurasian badgers (Meles meles). Badger culling has positive and negative effects on bovine TB in cattle and is difficult, costly and controversial. Here we show that Bacillus Calmette-Guérin (BCG) vaccination of captive badgers reduced the progression, severity and excretion of Mycobacterium bovis infection after experimental challenge. In a clinical field study, BCG vaccination of free-living badgers reduced the incidence of positive serological test results by 73.8 per cent. In common with other species, BCG did not appear to prevent infection of badgers subjected to experimental challenge, but did significantly reduce the overall disease burden. BCG vaccination of badgers could comprise an important component of a comprehensive programme of measures to control bovine TB in cattle.
doi:10.1098/rspb.2010.1953
PMCID: PMC3097825  PMID: 21123260
bovine tuberculosis; vaccination; badger; wildlife; Bacillus Calmette-Guérin
7.  Emergency rabies control in a community of two high-density hosts 
Background
Rabies is a fatal viral disease that potentially can affect all mammals. Terrestrial rabies is not present in the United Kingdom and has been eliminated from Western Europe. Nevertheless the possibility remains that rabies could be introduced to England, where it would find two potentially suitable hosts, red foxes and badgers. With the aim to analyse the spread and emergency control of rabies in this two species host community, a simulation model was constructed. Different control strategies involving anti-rabies vaccination and population culling were developed, considering control application rates, spatial extent and timing. These strategies were evaluated for efficacy and feasibility to control rabies in hypothetical rural areas in the South of England immediately after a disease outbreak.
Results
The model confirmed that both fox and badger populations, separately, were competent hosts for the spread of rabies. Realistic vaccination levels were not sufficient to control rabies in high-density badger populations. The combined species community was a very strong rabies host. However, disease spread within species appeared to be more important than cross-species infection. Thus, the drivers of epidemiology depend on the potential of separate host species to sustain the disease. To control a rabies outbreak in the two species, both species had to be targeted. Realistic and robust control strategies involved vaccination of foxes and badgers, but also required badger culling. Although fox and badger populations in the UK are exceptionally dense, an outbreak of rabies can be controlled with a higher than 90% chance, if control response is quick and follows a strict regime. This requires surveillance and forceful and repeated control campaigns. In contrast, an uncontrolled rabies outbreak in the South of England would quickly develop into a strong epizootic involving tens of thousands of rabid foxes and badgers.
Conclusions
If populations of both host species are sufficiently large, epizootics are driven by within-species transmission, while cross-species-infection appears to be of minor importance. Thus, the disease control strategy has to target both host populations.
doi:10.1186/1746-6148-8-79
PMCID: PMC3492034  PMID: 22709848
Badger; Cross species infection; Epidemiology; Exotic disease; Fox; Model; Multi-host disease; Population control; Simulation; Vaccination
8.  Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology 
The Eurasian badger (Meles meles) is implicated in the transmission of bovine tuberculosis (TB) to cattle in the UK and Republic of Ireland. Badger culling has been employed for the control of TB in cattle in both countries, with varying results. Social perturbation of badger populations following culling has been proposed as an explanation for the failure of culling to consistently demonstrate significant reductions in cattle TB. Field studies indicate that culling badgers may result in increased immigration into culled areas, disruption of territoriality, increased ranging and mixing between social groups. Our analysis shows that some measures of sociality may remain significantly disrupted for up to 8 years after culling. This may have epidemiological consequences because previous research has shown that even in a relatively undisturbed badger population, movements between groups are associated with increases in the incidence of Mycobacterium bovis infection. This is consistent with the results from a large-scale field trial, which demonstrated decreased benefits of culling at the edges of culled areas, and an increase in herd breakdown rates in neighbouring cattle.
doi:10.1098/rspb.2007.0998
PMCID: PMC2279223  PMID: 17725974
behaviour; disease control; movement; social organization; wildlife disease reservoir
9.  Landscape as a Model: The Importance of Geometry 
PLoS Computational Biology  2007;3(10):e200.
In all models, but especially in those used to predict uncertain processes (e.g., climate change and nonnative species establishment), it is important to identify and remove any sources of bias that may confound results. This is critical in models designed to help support decisionmaking. The geometry used to represent virtual landscapes in spatially explicit models is a potential source of bias. The majority of spatial models use regular square geometry, although regular hexagonal landscapes have also been used. However, there are other ways in which space can be represented in spatially explicit models. For the first time, we explicitly compare the range of alternative geometries available to the modeller, and present a mechanism by which uncertainty in the representation of landscapes can be incorporated. We test how geometry can affect cell-to-cell movement across homogeneous virtual landscapes and compare regular geometries with a suite of irregular mosaics. We show that regular geometries have the potential to systematically bias the direction and distance of movement, whereas even individual instances of landscapes with irregular geometry do not. We also examine how geometry can affect the gross representation of real-world landscapes, and again show that individual instances of regular geometries will always create qualitative and quantitative errors. These can be reduced by the use of multiple randomized instances, though this still creates scale-dependent biases. In contrast, virtual landscapes formed using irregular geometries can represent complex real-world landscapes without error. We found that the potential for bias caused by regular geometries can be effectively eliminated by subdividing virtual landscapes using irregular geometry. The use of irregular geometry appears to offer spatial modellers other potential advantages, which are as yet underdeveloped. We recommend their use in all spatially explicit models, but especially for predictive models that are used in decisionmaking.
Author Summary
Many different areas of science try to simulate and predict (model) how processes act across virtual landscapes. Sometimes these models are abstract, but often they are based on real-world landscapes and are used to make real-world planning or management decisions. We considered two separate issues: how movement occurs across landscapes and how uncertainty in spatial data can be represented in the model. Most studies represent the landscape using regular geometries (e.g., squares and hexagons), but we generated landscapes of irregular shapes. We tested and compared how the shapes that make up a landscape affected cell-to-cell movement across it. All of the virtual landscapes formed with regular geometries had the potential to bias the direction and distance of movement. Those formed with irregular geometry did not. We have also shown that describing whole real-world landscapes with regular geometries will lead to errors and bias, whereas virtual landscapes formed with irregular geometries are free from both. We recommend the use of multiple versions of virtual landscapes formed using irregular geometries for all spatially explicit models as a way of minimizing this source of bias and error; this is especially relevant in predictive models (e.g., climate change) that are difficult to test and are designed to help make decisions.
doi:10.1371/journal.pcbi.0030200
PMCID: PMC2041976  PMID: 17967050
10.  European Bat Lyssavirus in Scottish Bats 
Emerging Infectious Diseases  2005;11(4):572-578.
Daubenton bats may roost infrequently in human dwellings, so risk for human contact is low.
We report the first seroprevalence study of the occurrence of specific antibodies to European bat lyssavirus type 2 (EBLV-2) in Daubenton's bats. Bats were captured from 19 sites across eastern and southern Scotland. Samples from 198 Daubenton's bats, 20 Natterer's bats, and 6 Pipistrelle's bats were tested for EBLV-2. Blood samples (N = 94) were subjected to a modified fluorescent antibody virus neutralization test to determine antibody titer. From 0.05% to 3.8% (95% confidence interval) of Daubenton's bats were seropositive. Antibodies to EBLV-2 were not detected in the 2 other species tested. Mouth swabs (N = 218) were obtained, and RNA was extracted for a reverse transcription–polymerase chain reaction (RT-PCR). The RT-PCR included pan lyssavirus-primers (N gene) and internal PCR control primers for ribosomal RNA. EBLV-2 RNA was not detected in any of the saliva samples tested, and live virus was not detected in virus isolation tests.
doi:10.3201/eid1104.040920
PMCID: PMC3320325  PMID: 15829196
Lyssavirus; EBLV-2; seroprevalence; Daubenton bats; Scotland; research

Results 1-10 (10)