Effectiveness of biosecurity measures in preventing badger visits to farm buildings

Background

Bovine tuberculosis caused by Mycobacterium bovis is a serious and economically important disease of cattle. Badgers have been implicated in the transmission and maintenance of the disease in the UK since the 1970s. Recent studies have provided substantial evidence of widespread and frequent visits by badgers to farm buildings during which there is the potential for close direct contact with cattle and contamination of cattle feed.

Methodology

Here we evaluated the effectiveness of simple exclusion measures in improving farm biosecurity and preventing badger visits to farm buildings. In the first phase of the study, 32 farms were surveyed using motion-triggered infrared cameras on potential entrances to farm buildings to determine the background level of badger visits experienced by each farm. In the second phase, they were divided into four treatment groups; “Control”, “Feed Storage”, “Cattle Housing” and “Both”, whereby no exclusion measures were installed, exclusion measures were installed on feed storage areas only, cattle housing only or both feed storage and cattle housing, respectively. Badger exclusion measures included sheet metal gates, adjustable metal panels for gates, sheet metal fencing, feed bins and electric fencing. Cameras were deployed for at least 365 nights in each phase on each farm.

Results

Badger visits to farm buildings occurred on 19 of the 32 farms in phase one. In phase two, the simple exclusion measures were 100% effective in preventing badger entry into farm buildings, as long as they were appropriately deployed. Furthermore, the installation of exclusion measures also reduced the level of badger visits to the rest of the farmyard. The findings of the present study clearly demonstrate how relatively simple practical measures can substantially reduce the likelihood of badger visits to buildings and reduce some of the potential for contact and disease transmission between badgers and cattle.     

Use of cattle farm resources by badgers (Meles meles) and risk of bovine tuberculosis (Mycobacterium bovis) transmission to cattle

Nocturnal observations, radio telemetry and time-lapse camera surveillance were used to investigate visits by badgers (Meles meles L.) to two cattle farms. During 59 half-nights (ca. 295 h) of observation and 17 nights (ca. 154 h) of camera surveillance, 139 separate visits to farm buildings, by at least 26 individually identifiable badgers from two social groups, were recorded. The badgers, which included three individuals infected with bovine tuberculosis (Mycobacterium bovis), used cowsheds, feedsheds, barns, haystacks, slurry pits, cattle troughs and farmyards to exploit a range of food resources, including cattle feed and silage. Cattle feed was contaminated with badger faeces and badgers also came into close contact with cattle. The minimum number of badgers visiting farm buildings per night was negatively correlated with local 24 h rainfall. We conclude that exploitation by badgers of resources provided by cattle farms constitutes a potentially important mechanism for tuberculosis transmission from badgers to cattle.     

Badgers prefer cattle pasture but avoid cattle: implications for bovine tuberculosis control

Effective management of infectious disease relies upon understanding mechanisms of pathogen transmission. In particular, while models of disease dynamics usually assume transmission through direct contact, transmission through environmental contamination can cause different dynamics. We used Global Positioning System (GPS) collars and proximity‐sensing contact‐collars to explore opportunities for transmission of Mycobacterium bovis [causal agent of bovine tuberculosis] between cattle and badgers (Meles meles). Cattle pasture was badgers’ most preferred habitat. Nevertheless, although collared cattle spent 2914 collar‐nights in the home ranges of contact‐collared badgers, and 5380 collar‐nights in the home ranges of GPS‐collared badgers, we detected no direct contacts between the two species. Simultaneous GPS‐tracking revealed that badgers preferred land > 50 m from cattle. Very infrequent direct contact indicates that badger‐to‐cattle and cattle‐to‐badger M. bovis transmission may typically occur through contamination of the two species’ shared environment. This information should help to inform tuberculosis control by guiding both modelling and farm management.     

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.     

How many Eurasian badgers <Emphasis Type="Italic">Meles meles</Emphasis> L. are there in the Republic of Ireland?

In Ireland, the badger Meles meles L is a reservoir species for Mycobacterium bovis and, as such, contributes to the maintenance of bovine tuberculosis in cattle. A previous estimate of the badger population in the Republic was 200,000 badgers. In the current study, we obtained data on badger numbers from a large-scale badger removal project (the Four-Area project). The removal areas of the Four-Area Project were surrounded by barriers (either water or buffer areas where removals were also conducted) to prevent badger immigration. Within these areas, a grid of 0.25 km² was created within which we knew the badger numbers and habitat types (based on Corine data). Associations between badger numbers and habitat type were investigated using negative binomial modeling. Extrapolations from the model yielded an estimated badger population in the Republic of approximately 84,000 badgers. The implications of these findings are discussed.     

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

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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.     

Population ecology and prevalence of tuberculosis in Badgers in an area of Staffordshire

Forty-five badgers representing five social groups were removed from an area in Staffordshire where tuberculosis had occurred in cattle. Prior to removal, the tuberculosis status of the badger population was investigated by screening faeces samples, collected at fortnightly intervals, and badger social-group territories were determined by bait-marking. Samples for cultural and biological examination were taken from the live badgers before euthanasia and detailed post-mortem examination. The adult badger population density was 6-2/km2 and Mycobacterium bovis was isolated from samples taken post mortem from eight (17-8%) badgers. The results are reviewed in relation to previous findings.     

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.     

Effects of culling on badger abundance: implications for tuberculosis control

Culling is often considered as a tool for controlling wildlife diseases that can also infect people or livestock. Culling European badgers Meles meles can cause both positive and negative effects on the incidence of bovine tuberculosis (TB) in cattle. One factor likely to influence the outcome of different badger-culling strategies for cattle TB is the reduction in badger population density achieved. However, this reduction is difficult to measure because badgers, being nocturnal and fossorial, are difficult to count. Here, we use indices of badger abundance to measure the population impacts of two culling strategies tested in Britain. The densities of badger setts and latrines recorded before culling were correlated with the densities of badgers captured on initial culls, suggesting that both were indices of actual badger abundance. Widespread 'proactive' culling was associated with a 73% reduction in the density of badger latrines, a 69% reduction in the density of active burrows and a 73% reduction in the density of road-killed badgers. This population reduction was achieved by a coordinated effort entailing widespread and repeated trapping over several years. However, this strategy caused only modest reductions in cattle TB incidence in culled areas and elevated incidence in neighbouring unculled areas. Localized 'reactive' culling caused a 26% reduction in latrine density, a 32% reduction in active burrow density and a 10% reduction in the density of road-killed badgers, but apparently increased the incidence of cattle TB. These results indicate that the relationship between badger population reduction and TB transmission to cattle is strongly non-linear, probably because culling prompts changes in badger behaviour that influence transmission rates. These findings raise serious questions about the capacity of badger culling to contribute to the control of cattle TB in Britain.     

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.     

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.     

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.     

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.     

Environmental determinants of the <Emphasis Type="Italic">Mycobacterium bovis</Emphasis> concomitant infection in cattle and badgers in France

Landscape epidemiology analyses how environmental characteristics influence pathogen transmission between hosts of one or several species, by inducing constraints on space use by hosts, and/or on pathogen survival in the environment. Here, we analysed how environmental variables could be associated with the Mycobacterium bovis concomitant infection in both cattle and badgers, in an area of south-western France. We defined circular spatial units (500 and 1000 m radiuses) centred on 113 setts of trapped badgers and including cattle pastures. The characteristics of spatial units where only one species had been found infected were compared with the ones where both cattle and badgers had been found infected. A multivariate logistic model was used to analyse the association between concomitant infection in both species and three groups of variables describing landscape, animal population and terrain features of spatial units. The terrain ruggedness index of pastures and the percentage of sand in their soil were positively associated with the odds of concomitant infection in cattle and badgers in the spatial units. The number of neighbouring badger groups was negatively associated with the odds of concomitant infection (spatial units of 1000 m radius), whereas the number of crop parcels was positively associated with the odds of concomitant infection (spatial units of 500 m radius). These results suggest that terrain features, badger population structure and food availability may influence the spread of M. bovis infection between badgers and cattle, leading to concomitant infection of both species.     

Resource dispersion and badger population density in Mediterranean woodlands: is food,water or geology the limiting factor?

Eurasian badgers, Meles meles, in Mediterranean cork‐oak woodlands live in small groups within territories that embrace a mosaic of habitats where several setts (dens) are scattered. Assuming that their population density was related to home range sizes and that this in turn was influenced by food and water availability and the existence of substrate suitable for sett construction, we explored the relationship between these parameters. Two biotopes were predominantly important in providing food security to badgers in the ‘Grândola’ mountain study area: olive groves and orchards or vegetable gardens. Analysis of the mean total area of these two habitats in the ranges of radio‐tracked badgers permitted us to extrapolate to an estimate that the 66 km² encompassed eleven areas with the capacity to support badger groups each composed by 6–8 individuals. Since only three groups populated the area we concluded that food availability was not limiting badger density. Sites with surface water in summer (the dry season) seem sufficient to support more badger groups than existed, leading us to believe that this factor was also not limiting badger density. Simultaneously, using a logistic regression model and the biophysical characteristics of sett sites as explanatory variables, four predictor variables determined sett location: the existence of a geological fault/discontinuity, ridges, valleys and the distance to abandoned farm houses, of which the former had the higher odds ratio, being thus the best sett location predictor. Indeed, 56% of the areas predicted with >80% confidence to contain a badger sett were encompassed within a known home range. Therefore, our results suggest that, in Mediterranean cork oak woodlands in SW Portugal, the main factor limiting badger's density is the availability of suitable sites for setts. However, in areas where suitable sites for burrows existed, but food patches were absent, badgers were not found. This could indicate that the presence of both factors was necessary for badgers, although in this area sites suitable for digging setts appeared to be the primary limiting factor.     

A new phylodynamic model of Mycobacterium bovis transmission in a multi-host system uncovers the role of the unobserved reservoir

Multi-host pathogens are particularly difficult to control, especially when at least one of the hosts acts as a hidden reservoir. Deep sequencing of densely sampled pathogens has the potential to transform this understanding, but requires analytical approaches that jointly consider epidemiological and genetic data to best address this problem. While there has been considerable success in analyses of single species systems, the hidden reservoir problem is relatively under-studied. A well-known exemplar of this problem is bovine Tuberculosis, a disease found in British and Irish cattle caused by Mycobacterium bovis, where the Eurasian badger has long been believed to act as a reservoir but remains of poorly quantified importance except in very specific locations. As a result, the effort that should be directed at controlling disease in badgers is unclear. Here, we analyse densely collected epidemiological and genetic data from a cattle population but do not explicitly consider any data from badgers. We use a simulation modelling approach to show that, in our system, a model that exploits available cattle demographic and herd-to-herd movement data, but only considers the ability of a hidden reservoir to generate pathogen diversity, can be used to choose between different epidemiological scenarios. In our analysis, a model where the reservoir does not generate any diversity but contributes to new infections at a local farm scale are significantly preferred over models which generate diversity and/or spread disease at broader spatial scales. While we cannot directly attribute the role of the reservoir to badgers based on this analysis alone, the result supports the hypothesis that under current cattle control regimes, infected cattle alone cannot sustain M. bovis circulation. Given the observed close phylogenetic relationship for the bacteria taken from cattle and badgers sampled near to each other, the most parsimonious hypothesis is that the reservoir is the infected badger population. More broadly, our approach demonstrates that carefully constructed bespoke models can exploit the combination of genetic and epidemiological data to overcome issues of extreme data bias, and uncover important general characteristics of transmission in multi-host pathogen systems.     

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.     

Defecation and urination patterns of badgersMeles meles at low density in south west England

The spatial distribution of urine and faecal scent marks of badgersMeles meles (Linnaeus, 1758) at low population density (mean±SE across 4 social groups was 5.73±0.735 badgers/km2) in south-western England were quantified. Eighteen badger latrines (greater than one dung pit containing faeces), 74 single defecations not in pits and 21 faeces in single pits were located in spring when badgers were defending well-defined territories. Woodland was selected, and arable land avoided, for latrine sites. Pasture and built-up land was selected for single defecations not in pits whereas faeces in single pits were distributed randomly across habitat types. Faecal scent marks were strongly associated with the edge of pastoral fields rather than the middle. Forty-six and 51 urinations were located in spring and summer, respectively. Urine was deposited randomly across habitat types but was concentrated at the linear features surrounding the main setts. This is the first reported use of high levels of single defecations and urinations in badger scent marking strategies in the UK. These results are discussed in relation to the potential for transmission of bovine tuberculosisMycobacterium bovis from badger excreta to cattle.     

狗獾夜间活动节律是受人类活动影响而形成的吗?基于青海湖地区的研究实例

青海湖地区是目前已知的狗獾分布海拔最高点。为了解狗獾在青藏高原严酷生态环境下的生活史特点, 并验证是否人类干扰造成了狗獾夜行性的假说, 我们利用红外相机技术, 结合无线电遥测和野外调查研究了青海湖湖东地区亚洲狗獾(Meles leucurus)的种群密度、洞穴口的行为及活动节律。结果表明: (1)研究地区狗獾的平均种群密度为1.2 ± 0.6只/km², 其分布受食物丰富度的影响; (2)狗獾基本在夜间活动, 出洞时间集中在20:00-23:00之间, 而回洞时间则集中在清晨4:00-7:00之间, 23:00-4:00之间是狗獾的活动高峰; (3)狗獾离洞前行为主要是警戒行为, 回洞穴时的行为主要是嬉戏行为, 其他行为较少见, 表达具有特定的时间性; (4)人类活动对于狗獾活动没有显著性影响(P < 0.05)。