C. L. Cheeseman

Positive and negative effects of widespread badger culling on tuberculosis in cattle.

Human and livestock diseases can be difficult to control where infection persists in wildlife populations. For three decades, European badgers (Meles meles) have been culled by the British government in a series of attempts to limit the spread of Mycobacterium bovis, the causative agent of bovine tuberculosis (TB), to cattle. Despite these efforts, the incidence of TB in cattle has risen consistently, re-emerging as a primary concern for Britains cattle industry. Recently, badger culling has attracted controversy because experimental studies have reached contrasting conclusions (albeit using different protocols), with culled areas showing either markedly reduced or increased incidence of TB in cattle. This has confused attempts to develop a science-based management policy. Here we use data from a large-scale, randomized field experiment to help resolve these apparent differences. We show that, as carried out in this experiment, culling reduces cattle TB incidence in the areas that are culled, but increases incidence in adjoining areas. These findings are biologically consistent with previous studies but will present challenges for policy development.

Culling and cattle controls influence tuberculosis risk for badgers

Human and livestock diseases can be difficult to control where infection persists in wildlife populations. In Britain, European badgers (Meles meles) are implicated in transmitting Mycobacterium bovis, the causative agent of bovine tuberculosis (TB), to cattle. Badger culling has therefore been a component of British TB control policy for many years. However, large-scale field trials have recently shown that badger culling has the capacity to cause both increases and decreases in cattle TB incidence. Here, we show that repeated badger culling in the same area is associated with increasing prevalence of M. bovis infection in badgers, especially where landscape features allow badgers from neighboring land to recolonize culled areas. This impact on prevalence in badgers might reduce the beneficial effects of culling on cattle TB incidence, and could contribute to the detrimental effects that have been observed. Additionally, we show that suspension of cattle TB controls during a nationwide epidemic of foot and mouth disease, which substantially delayed removal of TB-affected cattle, was associated with a widespread increase in the prevalence of M. bovis infection in badgers. This pattern suggests that infection may be transmitted from cattle to badgers, as well as vice versa. Clearly, disease control measures aimed at either host species may have unintended consequences for transmission, both within and between species. Our findings highlight the need for policymakers to consider multiple transmission routes when managing multihost pathogens.

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.

Mating system of the Eurasian badger, Meles meles, in a high density population

Badgers are facultatively social, forming large groups at high density. Group‐living appears to have high reproductive costs for females, and may lead to increased levels of inbreeding. The extent of female competition for reproduction has been estimated from field data, but knowledge of male reproductive success and the extent of extra‐group paternity remains limited. Combining field data with genetic data (16 microsatellite loci), we studied the mating system of 10 badger social groups across 14 years in a high‐density population. From 923 badgers, including 425 cubs, we were able to assign maternity to 307 cubs, with both parents assigned to 199 cubs (47%) with 80% confidence, and 14% with 95% confidence. Age had a significant effect on the probability of reproduction, seemingly as a result of a deficit of individuals aged two years and greater than eight years attaining parentage. We estimate that approximately 30% of the female population successfully reproduced in any given year, with a similar proportion of the male population gaining paternity across the same area. While it was known there was a cost to female reproduction in high density populations, it appears that males suffer similar, but not greater, costs. Roughly half of assigned paternity was attributed to extra‐group males, the majority of which were from neighbouring social groups. Few successful matings occurred between individuals born in the same social group (22%). The high rate of extra‐group mating, previously unquantified, may help reduce inbreeding, potentially making philopatry a less costly strategy.

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.

Perturbing implications of wildlife ecology for disease control

Britains 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.

Experimental evidence of competitive release in sympatric carnivores

Changes in the relative abundance of sympatric carnivores can have far-reaching ecological consequences, including the precipitation of trophic cascades and species declines. While such observations are compelling, experimental evaluations of interactions among carnivores remain scarce and are both logistically and ethically challenging. Carnivores are nonetheless a particular focus of management practices owing to their roles as predators of livestock and as vectors and reservoirs of zoonotic diseases. Here, we provide evidence from a replicated and controlled experiment that culling Eurasian badgers Meles meles for disease control was associated with increases in red fox Vulpes vulpes densities of 1.6–2.3 foxes km−2. This unique experiment demonstrates the importance of intraguild relations in determining species abundance and of assessing the wider consequences of intervention in predator populations.

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

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

BOVINE TUBERCULOSIS IN CATTLE AND BADGERS IN LOCALIZED CULLING AREAS

Bovine tuberculosis (TB) is a zoonotic disease that can have serious consequences for cattle farming and, potentially, for public health. In Britain, failure to control bovine TB has been linked to persistent infection of European badger (Meles meles) populations. However, culling of badgers in the vicinity of recent TB outbreaks in cattle has failed to reduce the overall incidence of cattle TB. Using data from a large-scale study conducted in 1998–2005, we show that badgers collected on such localized culls had elevated prevalence of Mycobacterium bovis, the causative agent of bovine TB, suggesting that infections in cattle and badgers were indeed associated. Moreover, there was a high degree of similarity in the M. bovis strain types isolated from cattle and associated badgers. This similarity between strain types appeared to be unaffected by time lags between the detection of infection in cattle and culling of badgers, or by the presence of purchased cattle that might have acquired infection elsewhere. However, localized culling appeared to prompt an increase in the prevalence of M. bovis infection in badgers, probably by disrupting ranging and territorial behavior and hence increasing intraspecific transmission rates. This elevated prevalence among badgers could offset the benefits, for cattle, of reduced badger densities and may help to explain the failure of localized culling to reduce cattle TB incidence.

Value of existing serological tests for identifying badgers that shed Mycobacterium bovis

In the UK there has been a sharp rise in the incidence of bovine tuberculosis since the early 1990s and the badger has been identified as an important wildlife reservoir for this infection. Infected badgers can excrete Mycobacterium bovis, putting other badgers and cattle at risk of becoming infected. Vaccination has been proposed as an approach to reducing the excretion of M. bovis by tuberculous badgers. In order to evaluate the efficacy of a badger vaccine it will be necessary to accurately determine the number of badgers excreting M. bovis without removing them for post-mortem evaluation. The existing live tests for tuberculosis in the badger (culture, indirect ELISA, Western blot) have not been assessed for their ability to detect badgers excreting M. bovis. Over the past 18 years, badgers from 31 social groups have been trapped and sampled in a study area of the Cotswold escarpment. We have examined the serological responses of 128 badgers trapped between 1985 and 1998 from social groups where M. bovis infection was endemic. These responses were compared with culture from faeces, urine, tracheal aspirates and bite wound swabs taken from these animals while alive. ELISA was found to be more sensitive than Western blot in detecting badgers excreting M. bovis. The majority of culture-positive badgers excreted M. bovis intermittently over the period of study. As a result, there was only a 27.5% chance of sampling a badger for culture when it was excreting M. bovis. In contrast, a positive ELISA result correctly predicted 68.2% of badgers with a history of excreting M. bovis. In the absence of alternative live tests for the badger, the Brock Test indirect ELISA appears to be more valuable than culture for measuring the effect of vaccination on reducing the number of badgers at risk of transmitting tuberculosis.