Genetic evidence that culling increases badger movement: implications for the spread of bovine tuberculosis

The Eurasian badger (Meles meles) has been implicated in the transmission of bovine tuberculosis (TB, caused by Mycobacterium bovis) to cattle. However, evidence suggests that attempts to reduce the spread of TB among cattle in Britain by culling badgers have mixed effects. A large-scale field experiment (the randomized badger culling trial, RBCT) showed that widespread proactive badger culling reduced the incidence of TB in cattle within culled areas but that TB incidence increased in adjoining areas. Additionally, localized reactive badger culling increased the incidence of TB in cattle. It has been suggested that culling-induced perturbation of badger social structure may increase individual movements and elevate the risk of disease transmission between badgers and cattle. Field studies support this hypothesis, by demonstrating increases in badger group ranges and the prevalence of TB infection in badgers following culling. However, more evidence on the effect of culling on badger movements is needed in order to predict the epidemiological consequences of this control strategy. Here, analysis of the genetic signatures of badger populations in the RBCT revealed increased dispersal following culling. While standard tests provided evidence for greater dispersal after culling, a novel method indicated that this was due to medium- and long-distance dispersal, in addition to previously reported increases in home-range size. Our results also indicated that, on average, badgers infected with M. bovis moved significantly farther than did uninfected badgers. A disease control strategy that included culling would need to take account of the potentially negative epidemiological consequences of increased badger dispersal.     

Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis

In the UK, attempts since the 1970s to control the incidence of bovine tuberculosis (bTB) in cattle by culling a wildlife host, the European badger (Meles meles), have produced equivocal results. Culling-induced social perturbation of badger populations may lead to unexpected outcomes. We test predictions from the 'perturbation hypothesis', determining the impact of culling operations on badger populations, movement of surviving individuals and the influence on the epidemiology of bTB in badgers using data dervied from two study areas within the UK Government's Randomised Badger Culling Trial (RBCT). Culling operations did not remove all individuals from setts, with between 34-43% of badgers removed from targeted social groups. After culling, bTB prevalence increased in badger social groups neighbouring removals, particularly amongst cubs. Seventy individual adult badgers were fitted with radio-collars, yielding 8,311 locational fixes from both sites between November 2001 and December 2003. Home range areas of animals surviving within removed groups increased by 43.5% in response to culling. Overlap between summer ranges of individuals from Neighbouring social groups in the treatment population increased by 73.3% in response to culling. The movement rate of individuals between social groups was low, but increased after culling, in Removed and Neighbouring social groups. Increased bTB prevalence in Neighbouring groups was associated with badger movements both into and out of these groups, although none of the moving individuals themselves tested positive for bTB. Significant increases in both the frequency of individual badger movements between groups and the emergence of bTB were observed in response to culling. However, no direct evidence was found to link the two phenomena. We hypothesise that the social disruption caused by culling may not only increase direct contact and thus disease transmission between surviving badgers, but may also increase social stress within the surviving population, causing immunosuppression and enhancing the expression of disease.     

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.     

The Duration of the Effects of Repeated Widespread Badger Culling on Cattle Tuberculosis Following the Cessation of Culling

Background

In the British Isles, control of cattle tuberculosis (TB) is hindered by persistent infection of wild badger (Meles meles) populations. A large-scale field trial—the Randomised Badger Culling Trial (RBCT)—previously showed that widespread badger culling produced modest reductions in cattle TB incidence during culling, which were offset by elevated TB risks for cattle on adjoining lands. Once culling was halted, beneficial effects inside culling areas increased, while detrimental effects on adjoining lands disappeared. However, a full assessment of the utility of badger culling requires information on the duration of culling effects.

Methodology/Principal Findings

We monitored cattle TB incidence in and around RBCT areas after culling ended. We found that benefits inside culled areas declined over time, and were no longer detectable by three years post-culling. On adjoining lands, a trend suggesting beneficial effects immediately after the end of culling was insignificant, and disappeared after 18 months post-culling. From completion of the first cull to the loss of detectable effects (an average five-year culling period plus 2.5 years post-culling), cattle TB incidence was 28.7% lower (95% confidence interval [CI] 20.7 to 35.8% lower) inside ten 100 km² culled areas than inside ten matched no-culling areas, and comparable (11.7% higher, 95% CI: 13.0% lower to 43.4% higher, p  =  0.39) on lands ≤2 km outside culled and no-culling areas. The financial costs of culling an idealized 150 km² area would exceed the savings achieved through reduced cattle TB, by factors of 2 to 3.5.

Conclusions/Significance

Our findings show that the reductions in cattle TB incidence achieved by repeated badger culling were not sustained in the long term after culling ended and did not offset the financial costs of culling. These results, combined with evaluation of alternative culling methods, suggest that badger culling is unlikely to contribute effectively to the control of cattle TB in Britain.     

Comparing badger (Meles meles) management strategies for reducing tuberculosis incidence in cattle

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 km(2) and were evaluated over the whole of a 300 km(2) 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 km(2) 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.     

Spatial Targeting for Bovine Tuberculosis Control: Can the Locations of Infected Cattle Be Used to Find Infected Badgers?

Bovine tuberculosis is a disease of historical importance to human health in the UK that remains a major animal health and economic issue. Control of the disease in cattle is complicated by the presence of a reservoir species, the Eurasian badger. In spite of uncertainty in the degree to which cattle disease results from transmission from badgers, and opposition from environmental groups, culling of badgers has been licenced in two large areas in England. Methods to limit culls to smaller areas that target badgers infected with TB whilst minimising the number of uninfected badgers culled is therefore of considerable interest. Here, we use historical data from a large-scale field trial of badger culling to assess two alternative hypothetical methods of targeting TB-infected badgers based on the distribution of cattle TB incidents: (i) a simple circular ‘ring cull’; and (ii) geographic profiling, a novel technique for spatial targeting of infectious disease control that predicts the locations of sources of infection based on the distribution of linked cases. Our results showed that both methods required coverage of very large areas to ensure a substantial proportion of infected badgers were removed, and would result in many uninfected badgers being culled. Geographic profiling, which accounts for clustering of infections in badger and cattle populations, produced a small but non-significant increase in the proportion of setts with TB-infected compared to uninfected badgers included in a cull. It also provided no overall improvement at targeting setts with infected badgers compared to the ring cull. Cattle TB incidents in this study were therefore insufficiently clustered around TB-infected badger setts to design an efficient spatially targeted cull; and this analysis provided no evidence to support a move towards spatially targeted badger culling policies for bovine TB control.     

Localized reactive badger culling increases risk of bovine tuberculosis in nearby cattle herds

Human and livestock diseases can be difficult to control where infection persists in wildlife populations. Control of bovine tuberculosis (bTB) in British cattle is complicated by the maintenance of Mycobacterium bovis (the causative agent of bTB) in badgers, acting as reservoirs of infection. Although over 20 000 badgers were culled to control bTB between 1975 and 1997, the incidence of bTB in cattle has substantially increased in parts of Great Britain in recent decades. Our case-control study, involving 1208 cattle herds, provides further evidence of the detrimental effect of localized reactive badger culling in response to the disclosure of a confirmed bTB herd breakdown in cattle. The presence of any reactive badger culling activity and increased numbers of badgers culled in the vicinity of a herd were associated with significantly increased bTB risk, even after adjusting for other important local risk factors. Such findings may partly explain why some earlier localized approaches to bTB control were ineffective.     

Impact of culling on relative abundance of the European badger (Meles meles) in Ireland

The European Badger (Meles meles) has been implicated in the epidemiology of bovine tuberculosis in cattle populations in the Republic of Ireland. Badger populations have been subject to a culling regime in areas with chronic histories of bTB cattle herd breakdowns. Removal data from 2004 to 2010 were used to model the impact of culling on populations in areas under capture. Additionally, changes in field signs of badger activity were used as an index of abundance to support, or otherwise, the outcomes of the removal models. Significant reductions in standardised badger captures over time were found across three large study areas (total area, 1,355 km²). Assuming that all inactive setts were vacant, an overall linear trend model suggested that badger captures had decreased by 78 % for setts with 6 years of repeated capturing operations. Given the uncertainty associated with the relationship between sett activity and badger presence, we repeated the linear modelling using two ‘what if’ scenarios. Assuming that individual badgers were missed on 10 % or 20 % of occasions at inactive setts, the estimated decline over 6 years is lowered to 71 % or 64 %, respectively. The decline profile consisted of a steep initial decrease in captures within the first 2 years, followed by a more gradual decrease thereafter. The number of active openings at setts (burrows) declined significantly in all three areas; but the magnitude of this decline varied significantly amongst study areas (41–82 %). There was a significant increase in the probability of setts becoming dormant with time. The removal programme was more intense (mean, 0.45 badgers culled km^?2 year^?1) than previous experimental badger removals in Ireland but some captures may be attributed to immigrant badgers as no attempt was made to limit inward dispersal from areas not under management. Results from this study suggest that significant reductions in badger density occurred in the areas where management had taken place. Since other non-culled badger populations in Northern Ireland and Britain exhibited stable population trends, we attribute the reduction in relative abundance to the culling regime. Further studies of the dynamics of this reduction are required to quantify how it is counteracted by immigration from populations outside of culled areas.     

Reports on badgers Meles meles in Dutch newspapers 1900–2013: same animals,different framings?

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Distribution of badger latrines in a high-density population: habitat selection and implications for the transmission of bovine tuberculosis to cattle

Eurasian badgers Meles meles habitually deposit droppings and other scent marks at latrines, which may be associated with territorial defence, and communicate information related to group and individual identity and status, and food resources. Understanding patterns of latrine distribution contributes to our understanding of badger social behaviour, and may be relevant to managing the risks of transmission of bovine tuberculosis from badgers to cattle. We investigated the distribution of badger latrines relative to habitat composition in a high-density badger population occupying a 7 km² area of diverse landscape in south-west England. Results indicated that the frequency and density of badger latrines varied according to land use, with woodland and linear landscape features (particularly hedges and stone walls) being positively selected. The number of latrines decreased significantly with distance from linear features. Grassland was negatively selected given its availability, but contained the highest number of latrines. The tendency for latrines to be associated with particular habitat types covaried spatially across the study area. We present a habitat selection probability function, based on the output of our analyses, to allow comparison of observed versus expected latrine counts per habitat type at different sites. Habitat manipulation on farmland may offer opportunities to manage exposure of cattle to badger latrines. However, our analyses indicate that other factors (perhaps demographic or environmental) may also exert a substantial local influence on latrine location.     

Perturbing implications of wildlife ecology for disease control

Britain's Randomised Badger Culling Trial provides robust evidence of the role badgers have in transmission of Mycobacterium bovis to cattle. Culling badgers perturbed their social structure, and brought positive and negative effects for bovine tuberculosis incidence in cattle, leading to the conclusion that culling could not make a meaningful contribution to disease control. The RBCT highlights the complexities of disease transmission in social animals and the importance of host ecology for controlling wildlife diseases.     

Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badger Meles meles population

1. The culling of European badgers Meles meles has been a central part of attempts to control bovine tuberculosis (TB) in British cattle for many years. Recent results, however, indicate that this approach could in practice enhance disease spread. 2. This paper looks at the relationship between TB incidence and badger ecology in a high-density population in south-west England, which has been the subject of a long-term intensive study. The principal aims were to relate the probability of TB incidence, as detected by culture of clinical samples (i.e. excretion of bacilli), at the level of the individual and of the social group to demographic processes, movement, social organization and disease dynamics. 3. The probability of an individual being an incident case was greater in groups where TB was already present, although this was less influential in groups that were subject to some instability in numbers. Both individuals and groups were more likely to be incident cases where the social group was diminishing in size, although no relationship was observed with group size itself. This suggests that the process of group size reduction rather than group size per se has most influence on disease dynamics. The likelihood that either an individual or a group was an incident case was positively correlated with both individual and group-level movement. When the proportion of females in a social group was high, the positive association between movement and incidence was found to be more pronounced and there was a significantly higher probability of incident cases among males. 4. These relationships highlight the importance of social structure in driving TB transmission dynamics in this stable, high-density badger population. The results support the idea that a stable social structure mitigates against new incident cases of disease, and are consistent with the contention that badger culling may create the social circumstances for enhanced transmission of TB.     

Local cattle and badger populations affect the risk of confirmed tuberculosis in British cattle herds

Background

The control of bovine tuberculosis (bTB) remains a priority on the public health agenda in Great Britain, after launching in 1998 the Randomised Badger Culling Trial (RBCT) to evaluate the effectiveness of badger (Meles meles) culling as a control strategy. Our study complements previous analyses of the RBCT data (focusing on treatment effects) by presenting analyses of herd-level risks factors associated with the probability of a confirmed bTB breakdown in herds within each treatment: repeated widespread proactive culling, localized reactive culling and no culling (survey-only).

Methodology/Principal Findings

New cases of bTB breakdowns were monitored inside the RBCT areas from the end of the first proactive badger cull to one year after the last proactive cull. The risk of a herd bTB breakdown was modeled using logistic regression and proportional hazard models adjusting for local farm-level risk factors. Inside survey-only and reactive areas, increased numbers of active badger setts and cattle herds within 1500 m of a farm were associated with an increased bTB risk. Inside proactive areas, the number of M. bovis positive badgers initially culled within 1500 m of a farm was the strongest predictor of the risk of a confirmed bTB breakdown.

Conclusions/Significance

The use of herd-based models provide insights into how local cattle and badger populations affect the bTB breakdown risks of individual cattle herds in the absence of and in the presence of badger culling. These measures of local bTB risks could be integrated into a risk-based herd testing programme to improve the targeting of interventions aimed at reducing the risks of bTB transmission.     

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.     

Interspecific visitation of cattle and badgers to fomites: A transmission risk for bovine tuberculosis?

In Great Britain and Ireland, badgers (Meles meles) are a wildlife reservoir of Mycobacterium bovis and implicated in bovine tuberculosis transmission to domestic cattle. The route of disease transmission is unknown with direct, so‐called “nose‐to‐nose,” contact between hosts being extremely rare. Camera traps were deployed for 64,464 hr on 34 farms to quantify cattle and badger visitation rates in space and time at six farm locations. Badger presence never coincided with cattle presence at the same time, with badger and cattle detection at the same location but at different times being negatively correlated. Badgers were never recorded within farmyards during the present study. Badgers utilized cattle water troughs in fields, but detections were infrequent (equivalent to one badger observed drinking every 87 days). Cattle presence at badger‐associated locations, for example, setts and latrines, were three times more frequent than badger presence at cattle‐associated locations, for example, water troughs. Preventing cattle access to badger setts and latrines and restricting badger access to cattle water troughs may potentially reduce interspecific bTB transmission through reduced indirect contact.     

Eliminating bovine tuberculosis in cattle and badgers: insight from a dynamic model

Bovine tuberculosis (BTB) is a multi-species infection that commonly affects cattle and badgers in Great Britain. Despite years of study, the impact of badgers on BTB incidence in cattle is poorly understood. Using a two-host transmission model of BTB in cattle and badgers, we find that published data and parameter estimates are most consistent with a system at the threshold of control. The most consistent explanation for data obtained from cattle and badger populations includes within-host reproduction numbers close to 1 and between-host reproduction numbers of approximately 0.05. In terms of controlling infection in cattle, reducing cattle-to-cattle transmission is essential. In some regions, even large reductions in badger prevalence can have a modest impact on cattle infection and a multi-stranded approach is necessary that also targets badger-to-cattle transmission directly. The new perspective highlighted by this two-host approach provides insight into the control of BTB in Great Britain.     

Control of bovine tuberculosis in British livestock: there is no 'silver bullet'

Bovine tuberculosis (bTB; Mycobacterium bovis) is a bacterial infection of cattle that also affects certain wildlife species. Culling badgers (Meles meles), the principal wildlife host, results in perturbation of the badger population and an increased level of disease in cattle. Therefore, the priority for future management must be to minimize the risk of disease transmission by finding new ways to reduce the contact rate among the host community. At the farm level, targeting those individuals that represent an elevated risk of transmission might prove to be effective. At the landscape level, risk mapping can provide the basis for targeted surveillance of the host community. Here, we review the current evidence for bTB persistence in Britain and make recommendations for future management and research.     

Changes in the prevalence of badger persecution in Northern Ireland

Animal populations generally increase after release from hunting pressure and/or cessation of illegal persecution. Implementation of full legislative protection of the Eurasian badger Meles meles in Great Britain is thought to have led to increases in badger abundance due to reduced levels of persecution. Conversely, prevalence of badger persecution in Northern Ireland was historically much higher than in Great Britain, and badger abundance remained stable over time despite similar legislative protection. We examined temporal changes in the prevalence of badger sett disturbance in Northern Ireland from 1990/1993 to 2007/2008 in relation to population status. A total of 56 (12.6%) of 445 setts surveyed during 1990/1993 had been disturbed compared to 29 (4.4%) of 653 setts during 2007/2008. This was a significant decline (−65%) in the incidence of sett disturbance over the 14–18-year period. Most notably, the incidence of digging at badger setts, indicative of local badger baiting activity, declined from 50% to 3.5% of disturbed setts. Signs of recent disturbance were significantly more frequent at disused setts suggesting that once disturbed, badgers may vacate a sett. The number of badger social groups in Northern Ireland did not differ between the two study periods, suggesting that previously high levels of badger persecution did not limit the number of badger social groups. The stability of the badger population in Northern Ireland compared to the growing population in Great Britain cannot be attributed to changes in the prevalence of persecution. Differences in the trajectories of both populations could be due to a range of factors including climate, habitat composition and structure, farming practices or food availability. More work is needed to determine how such factors influence badger population dynamics.     

Weather influences trapping success for tuberculosis management in European badgers (<Emphasis Type="Italic">Meles meles</Emphasis>)

European badgers (Meles meles) in Ireland and the UK are a reservoir for Mycobacterium bovis, the causative agent of bovine tuberculosis (TB). A number of interventions have been evaluated in attempts to control bovine TB within badger populations, and many of which rely on the capture of badgers. One strategy being implemented within Ireland is intramuscular vaccination using Bacillus Calmette-Guérin (BCG), as an alternative to badger culling. The success of vaccination as a disease control strategy depends on the ability to capture badgers and administer vaccines; thus, trapping success is crucial to effectively vaccinate the population (maximize vaccine coverage). A field vaccine trial was conducted in County Kilkenny, Ireland, from 2010–2013. We used data from this trial to evaluate the association between weather (precipitation and temperature data), badger sett characteristics, and badger trapping success. Approximately 10% of capture efforts resulted in a badger capture. Our results indicate that badger captures were the highest in drizzle, rain, and heavy rain weather conditions, and when minimum temperatures ranged from 3–8 °C. Badger captures were the highest at main setts (large burrow systems), and when sett activity scores were high (qualitative classes 4 or 5). Using local precipitation and temperature data in conjunction with observed sett characteristics provides wildlife managers with guidelines to optimize trapping success. Implementing capture operations under optimal conditions should increase the trapping success of badgers and allow for increased delivery of vaccines to manage bovine TB.