Richard J. Delahay

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.

Crossing the Interspecies Barrier: Opening the Door to Zoonotic Pathogens

This research was funded by EU FP7 grant ANTIGONE (#278976). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Is Mycobacterium bovis in the environment important for the persistence of bovine tuberculosis

Mycobacterium bovis is the causative agent of bovine tuberculosis (bTB) in cattle and wildlife. Direct aerosol contact is thought to be the primary route of infection between conspecifics, whereas indirect transmission via an environmental reservoir of M. bovis is generally perceived not to be a significant source for infection. Here, we report on the application of molecular technology (PCR) to quantify the prevalence of M. bovis in the environment and to explore its epidemiological significance. We show that the detectability of viable M. bovis at badger setts and latrines is strongly linked to the frequency of M. bovis excretion by infected badgers, and that putative M. bovis in the environment is prevalent on a large proportion of endemic cattle farms in Britain. These results raise important questions about the role of an environmental reservoir in bTB persistence.

Badger social networks correlate with tuberculosis infection

Although disease hosts are classically assumed to interact randomly [1], infection is likely to spread across structured and dynamic contact networks [2]. We used social network analyses to investigate contact patterns of group-living European badgers, Meles meles, which are an important wildlife reservoir of bovine tuberculosis (TB). We found that TB test-positive badgers were socially isolated from their own groups but were more important for flow, potentially of infection, between social groups. The distinctive social position of infected badgers may help explain how social stability mitigates, and social perturbation increases, the spread of infection in badgers.

BCG vaccination reduces risk of tuberculosis infection in vaccinated badgers and unvaccinated badger cubs.

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 ratiou200a=u200a0.24, 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 ratiou200a=u200a0.46, 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 ratiou200a=u200a0.08, 95% CI 0.01–0.76; Pu200a=u200a0.03). When more than a third of their social group had been vaccinated, the risk to unvaccinated cubs was reduced by 79% (Odds ratiou200a=u200a0.21, 95% CI 0.05–0.81; Pu200a=u200a0.02).

Wildlife Population Structure and Parasite Transmission: Implications for Disease Management

The beginning stages of research often involve describing patterns (e.g. males tend to more heavily parasitized than females for a given subset of species). From those initial patterns, researchers then test hypothesised mechanisms that may create those patterns. As an emerging discipline, much of wildlife disease management is about detecting trends and associations, and currently there are few guiding principles that both explain the trends and are applicable across a broad range hosts and parasites. This chapter focuses on the associations between prevalence/transmission and host social structure, where host social structure includes within group factors (eg. sex, age, dominance) and among group factors (eg. group size and movement among groups). Although there are few general theories of how host social structure affects disease dynamics it is clear that a narrow focus on either the host or the pathogen is not as productive as a integrated approach that considers the host-parasite interaction, which is itself affected by the abiotic and biotic factors in the surrounding environment.

Performance of Proximity Loggers in Recording Intra and Inter-Species Interactions: A Laboratory and Field- Based Validation Study

Knowledge of the way in which animals interact through social networks can help to address questions surrounding the ecological and evolutionary consequences of social organisation, and to understand and manage the spread of infectious diseases. Automated proximity loggers are increasingly being used to record interactions between animals, but the accuracy and reliability of the collected data remain largely un-assessed. Here we use laboratory and observational field data to assess the performance of these devices fitted to a herd of 32 beef cattle (Bos taurus) and nine groups of badgers (Meles meles, n u200a=u200a77) living in the surrounding woods. The distances at which loggers detected each other were found to decrease over time, potentially related to diminishing battery power that may be a function of temperature. Loggers were highly accurate in recording the identification of contacted conspecifics, but less reliable at determining contact duration. There was a tendency for extended interactions to be recorded as a series of shorter contacts. We show how data can be manipulated to correct this discrepancy and accurately reflect observed interaction patterns by combining records between any two loggers that occur within a 1 to 2 minute amalgamation window, and then removing any remaining 1 second records. We make universally applicable recommendations for the effective use of proximity loggers, to improve the validity of data arising from future studies.

Advances and prospects for management of TB transmission between badgers and cattle

Bovine tuberculosis (bTB) is the most serious endemic disease facing the livestock industry in the United Kingdom (UK) and Republic of Ireland (RoI), where its management has been confounded by the presence of persistent infection in the Eurasian badger (Meles meles). Field evidence suggests that the social structure of badger populations can have an important influence on disease dynamics, and on the outcome of management interventions. Recent, large-scale badger culling experiments in the UK and RoI had complex epidemiological outcomes. In the UK, proactive culling led to reduced bTB incidence in cattle herds inside culled areas, but a temporary increase in adjacent areas. Reactive culling in response to herd breakdowns was associated with an increase in the incidence of bTB in cattle. In contrast, badger culling in RoI was reported to have only beneficial effects on bTB incidence in cattle. The reasons for these differences are not clear. The complexity of the evidence base for culling is highlighted by the different management approaches currently being adopted by the different authorities of the UK and RoI. It is generally accepted that a holistic approach to bTB management, which targets both cattle and wildlife, is necessary. Consequently recent research activities have also focussed on cattle and badger vaccines, and biosecurity on farms. This paper describes recent advances in our understanding of the epidemiology of bTB in badgers and the consequences of culling, and current research to develop approaches for the vaccination of badgers, and methods of managing the risks of contact between badgers and cattle in farm buildings.

Farm husbandry and badger behaviour: Opportunities to manage badger to cattle transmission of Mycobacterium bovis?

Bovine tuberculosis (bTB) is a serious disease of cattle in the UK in terms of the economic impact on the farming industry. The disease has proven difficult to control in the cattle population and the Eurasian badger (Meles meles) is a source of infection. In recent years, there has been growing interest in the potential to employ farm husbandry and biosecurity practices to reduce bTB transmission risks. Here we review the potential routes of bTB transmission between badgers and cattle and explore the options for managing cattle and badger behaviour with a view to reducing the risks of inter-species transmission at pasture and within farm buildings. We discuss the relative merits of different cattle grazing regimes, habitat manipulations and badger latrine management in reducing the potential for badger-cattle contact at pasture. The physical exclusion of badgers from farm buildings is suggested as the simplest, and potentially most effective, method of reducing contact and opportunities for disease transmission between badgers and cattle. However, more research is required on the effectiveness, practicalities and costs of implementing such measures before specific guidance can be developed.

Diagnostic Accuracy and Optimal Use of Three Tests for Tuberculosis in Live Badgers

Background Accurate diagnosis of tuberculosis (TB) due to infection with Mycobacterium bovis is notoriously difficult in live animals, yet important if we are to understand the epidemiology of TB and devise effective strategies to limit its spread. Currently available tests for diagnosing TB in live Eurasian badgers (Meles meles) remain unvalidated against a reliable gold standard. The aim of the present study was to evaluate the diagnostic accuracy and optimal use of three tests for TB in badgers in the absence of a gold standard. Methodology/Principal Findings A Bayesian approach was used to evaluate the diagnostic accuracy and optimal use of mycobacterial culture, gamma-interferon assay and a commercially available serological test using multiple samples collected from 305 live wild badgers. Although no single test was judged to be sufficiently sensitive and specific to be used as a sole diagnostic method, selective combined use of the three tests allowed guidelines to be formulated that allow a diagnosis to be made for individual animals with an estimated overall accuracy of 93% (range: 75% to 97%). Employing this approach in the study population of badgers resulted in approximately 13 out of 14 animals having their true infection status correctly classified from samples collected on a single capture. Conclusions/Significance This method of interpretation represents a marked improvement on the current procedure for diagnosing M. bovis infection in live badgers. The results should be of use to inform future test and intervention strategies with the aim of reducing the incidence of TB in free-living wild badger populations.