Comparative study on the consequences of culling badgers (Meles meles) on biometrics, population dynamics and movement

1.  Capture–mark–recapture data were used to describe the process of recovery from a typical badger removal operation (BRO) at North Nibley, Gloucestershire, UK, which was carried out as part of the government's strategy to control bovine tuberculosis. Data on biometrics, demographics and movement from this low-density disturbed population were compared with those of two nearby high-density undisturbed populations (Wytham Woods and Woodchester Park, UK) in order to study fundamental principles of population dynamics and density-dependence.
2.  Badgers moved more between social groups at North Nibley than in the other study areas, particularly in the immediate aftermath of the removal operation.
3.  Recolonization of the vacated habitat occurred in the first instance by young females.
4.  Although in the first year after the BRO no cubs had been reared in any of the culled groups, and although the shortage of sexually mature boars may have limited the reproductive output of sows in the following year, the population took only 3 years to recover to its (already lowered) preremoval density.
5.  Losses from the adult (and cub) population due to mortality or emigration were smaller at North Nibley than at the other sites.
6.  There was much evidence that during 1995 and 1996 density-dependent effects constrained the reproductive output of the high-density populations, and some support for the hypothesis that badgers exhibit the non-linear 'large mammal' type of functional response to density.
7.  Badgers at North Nibley were younger, heavier and in better condition than badgers at Wytham Woods and Woodchester Park.
8.  We argue that the disease dynamics are likely to be different in disturbed compared with undisturbed badger populations, and that this could affect the effectiveness of BROs.     

Dispersal patterns in a medium‐density Irish badger population: Implications for understanding the dynamics of tuberculosis transmission

European badgers (Meles meles) are group‐living mustelids implicated in the spread of bovine tuberculosis (TB) to cattle and act as a wildlife reservoir for the disease. In badgers, only a minority of individuals disperse from their natal social group. However, dispersal may be extremely important for the spread of TB, as dispersers could act as hubs for disease transmission. We monitored a population of 139 wild badgers over 7 years in a medium‐density population (1.8 individuals/km²). GPS tracking collars were applied to 80 different individuals. Of these, we identified 25 dispersers, 14 of which were wearing collars as they dispersed. This allowed us to record the process of dispersal in much greater detail than ever before. We show that dispersal is an extremely complex process, and measurements of straight‐line distance between old and new social groups can severely underestimate how far dispersers travel. Assumptions of straight‐line travel can also underestimate direct and indirect interactions and the potential for disease transmission. For example, one female disperser which eventually settled 1.5 km from her natal territory traveled 308 km and passed through 22 different territories during dispersal. Knowledge of badgers' ranging behavior during dispersal is crucial to understanding the dynamics of TB transmission, and for designing appropriate interventions, such as vaccination.     

Bovine tuberculosis in “Eurasian” badgers (Meles meles) in France

In France, several surveillance programmes have been carried out to monitor the presence of bovine tuberculosis (bTB) in badgers in regions where cattle or wildlife show high bTB prevalence (Seine-Maritime, Côte d’Or, Dordogne/Charente). Diagnostic methods include post-mortem examination, polymerase chain reaction (PCR) and/or microbiological culture. The frequency of visible lesions was significantly higher in Dordogne/Charente (14/283, 4.9 %) than in Côte d’Or (19/1146, 1.7 %) and Seine-Maritime (2/160, 1.25 %) (Fisher’s exact test, p?<?0.001). Lesions were mainly located in cephalic and thoracic lymph nodes with one badger showing generalised tuberculosis. Near infected cattle farms or pastures, Mycobacterium bovis was detected using the culture method in roughly 1 % (1/103) of the badgers sampled in Seine-Maritime and in 5.6 % (49/878) of the badgers sampled in Côte d’Or. In Dordogne/Charente, the prevalence determined by PCR was 13.3 % (29/218). M. bovis was not found in badgers trapped in areas where there are no infected cattle. Spoligotyping and multiple locus variable number tandem repeat analysis showed that all M. bovis strains isolated from badgers were of the same genotype as those isolated from cattle in the vicinity, demonstrating an epidemiological link between both species. These are the first cases of bTB in badgers reported in France. Further surveys and research are needed to investigate the role badgers play in the epidemiology of bTB.     

Antibodies to Mycobacterium bovis in wild carnivores from Doñana National Park (Spain)

We conducted a retrospective serologic survey for antibodies against the MPB70 protein of Mycobacterium bovis in wild carnivores from Do?ana National Park (southwestern Spain). Serum samples from 118 red foxes (Vulpes vulpes), 39 Iberian lynx (Lynx pardinus), 31 Eurasian badgers (Meles meles), five Egyptian mongoose (Herpestes ichneumon), four European genet (Genetta genetta), and one Eurasian otter (Lutra lutra) were analyzed using an indirect competitive enzyme-linked immunoassay. Antibodies against the MPB70 protein of M. bovis were detected in seven badgers, five foxes, and one lynx. The frequency of positive animals was significantly higher in badger (23%) than in lynx (3%) and fox (4%). Antibodies were not detected in other species. Annual antibody frequency peaked at 38% in badgers and 11% for red fox. These species may contribute to persistence of bovine tuberculosis in Do?ana.     

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.     

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.     

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.     

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.     

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.     

Movements of European bison (Bison bonasus) beyond the Białowieża Forest (NE Poland): range expansion or partial migrations?

The European bison is the largest terrestrial mammal in Europe. After extinction in the wild at the beginning of the twentieth century, it was re-introduced to Bia?owie?a Forest and other woodlands in Eastern Europe. In this paper, we analysed the movements of European bison beyond the continuous woodlands of the Bia?owie?a Forest (NE Poland) between 1964 and 2010. In total, 1,117 direct observations of bison were collected. The number of males moving out of the forest fluctuated during the study period, whilst the number of females steadily increased. The number of male observations outside of the forest per annum was dependent on the population size and snow depth, whilst the number of cows in mixed groups moving outside of the forest was correlated with the population size only. Males were observed mainly alone (50 % of observations) or in small groups of two to three individuals (25 %); however, distribution of group size differed from those observed in the population. There was a significant difference between the direction of movement of males and females out of the forest—males moved mainly west and southwest, whilst females moved to the north. This was also significantly different from the expected movement direction. The mean distance of bison observations from the forest border was 1.8?±?0.13 km and did not differ significantly between sexes. After 1990, males were observed significantly farther away from the forest (2.2 km) than in the previous years (0.9 km). Most observations (94 % of bulls and 93 % of cows) were up to 5 km from the forest edge. The range of bison in the vicinity of the Bia?owie?a Forest was strictly seasonal. Most observations (78 % in males and 88 % in females) were recorded from November to April. Increasing utilisation of areas beyond the forest habitats may be driven by different factors but most probably it is related to range expansion and the bison's preference for open habitats. The strong seasonal pattern of bison movements indicate that the partial seasonal migrations were initiated in the Bia?owie?a population.     

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.     

Increasing frequency of bite wounds with increasing population density in Eurasian badgers, Meles meles

Eurasian badgers sometimes live in territorial, mixed-sex groups; the adaptive significance of this is not understood, but members generally interact amicably. None the less, badgers occasionally fight and inflict sometimes severe wounds on one another. Based on 498 badger life histories, from first emergence as a cub until death, documented during a 10-year trapping study at Wytham Woods, Oxfordshire, U.K., the patterns and rates of bite wounding and consequential scarring were examined. Male badgers received more wounds and more severe wounds than did females. Wounding rates for both sexes increased significantly with age, and there was evidence that heavier individuals received most wounds. No seasonal pattern in wounding rates was apparent. During the study, the badger population size increased three-fold and wounding rates, particularly in males, showed a density-dependent increase. The rate of bite wounding increased with group size, and this increase was more marked among males than among females. Among males, but not females, the rate of bite wounding also increased with the number of badgers living in adjoining territories.     

Inferring Mycobacterium bovis transmission between cattle and badgers using isolates from the Randomised Badger Culling Trial

Mycobacterium bovis (M. bovis) is a causative agent of bovine tuberculosis, a significant source of morbidity and mortality in the global cattle industry. The Randomised Badger Culling Trial was a field experiment carried out between 1998 and 2005 in the South West of England. As part of this trial, M. bovis isolates were collected from contemporaneous and overlapping populations of badgers and cattle within ten defined trial areas. We combined whole genome sequences from 1,442 isolates with location and cattle movement data, identifying transmission clusters and inferred rates and routes of transmission of M. bovis. Most trial areas contained a single transmission cluster that had been established shortly before sampling, often contemporaneous with the expansion of bovine tuberculosis in the 1980s. The estimated rate of transmission from badger to cattle was approximately two times higher than from cattle to badger, and the rate of within-species transmission considerably exceeded these for both species. We identified long distance transmission events linked to cattle movement, recurrence of herd breakdown by infection within the same transmission clusters and superspreader events driven by cattle but not badgers. Overall, our data suggests that the transmission clusters in different parts of South West England that are still evident today were established by long-distance seeding events involving cattle movement, not by recrudescence from a long-established wildlife reservoir. Clusters are maintained primarily by within-species transmission, with less frequent spill-over both from badger to cattle and cattle to badger.     

Patterns of den occupation by the spotted hyaena (Crocuta crocuta)

Spotted hyaenas utilize isolated natal dens (NDs) and communal dens (CDs) for rearing their cubs. Here we describe patterns of natal and CD occupation by hyaenas belonging to one well‐studied clan in the Maasai Mara National Reserve during a 10‐year period. Locations of 98 den sites that were used as natal or CDs by hyaenas in the study clan were digitized in a Geographic Information System, and the duration of use of each den site, frequency of re‐use, and distances involved in den moves were quantified. Hyaenas moved their CD monthly on average. Most CD sites were occupied only once during the study, but several sites were used repeatedly. On rare occasions, the movement of hyaenas to a new den site could be attributed to a disturbance event at the CD, but factors regularly prompting hyaenas to move to new CD sites were unclear. High‐ranking female hyaenas were more likely to rear their cubs from birth in a CD than low‐ranking females. Low‐ranking females almost always utilized isolated NDs for the first few weeks of a litter's development, and low‐ranking females transferred their cubs over longer distances than did high‐ranking females.     

Sex-biased dispersal and growth in sablefish (Anoplopoma fimbria) in the northeastern Pacific Ocean

To examine the potential linkage between sex-biased growth and dispersal in demersal fish, we studied the movement distance and growth of tag-recaptured sablefish (Anoplopoma fimbria). Tagging was conducted by teams from Japan and the United States. From 1980 to 1984, 58,918 sablefish were captured by Japanese vessels and tagged with anchor tags, and between 1980 and 2007, 3319 sablefish were recaptured in the Bering Sea and northeastern Pacific. Of these 3319 fish, we analyzed data on 659 individuals for which we have reliable data on recapture location, sex and fork length at the time of release and recapture, and elapsed time longer than 10?days. Annual growth increments (mean±S.D.) were 2.5?±?6.5?cm (males) and 3.5?±?8.6?cm (females), and the movement distances (assumed to be straight) were 712?±?800?km (males) and 877?±?920?km (females). Females grew larger and moved longer distances than males. We calculated the growth increment deviation that accounted for the effects of elapsed time, curvilinear growth, and initial fork length at release using a von Bertalanffy growth model. The growth increment deviation increased significantly with the distance moved over elapsed time. In addition, the relationship between distance moved over elapsed time and the growth deviation differed significantly between sexes; females grew faster than males at a given movement distance. We suggest that female-biased dispersal is a factor generating female-biased growth in sablefish.     

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.     

Modeling intra-sexual competition in a sex pheromone system: how much can female movement affect female mating success?

Mating disruption theory predicts that high concentrations of female pheromone, and/or large numbers of release sites, should confuse males orienting to "calling" females, reduce the number of successful matings, and decrease the reproductive potential of the population. In this scenario, females are regarded as stationary point sources of pheromone. Past behavioral observations, however, have shown virgin female grape root borers, Vitacea polistiformis Harris, significantly alter their behavior in mating disruption treatments. Treated females call at different heights, move less before call initiation, and move more after call initiation than control females. Pheromone gland dragging and wing fanning also increase significantly during pheromone treatments. These behavioral differences are significant only if they alter the mating success of females. Because long-term field studies are impractical, we used known behavior of male and female GRB to build a Fortran language time step model, adding the effects of female movement to past models of male pheromone plume following. Females were distributed randomly, and then assigned a conditional movement strategy. If females were within the competitive portion of another female's plume, the downwind female moved. Except in the lowest population density tested, females moving upwind and crosswind when in a competing female's pheromone plume mated significantly more often than females remaining stationary. In all population simulations, mating success was significantly reduced when females moved downwind. These field and simulation studies provide strong evidence for female movement as a previously overlooked potential mechanism for resistance to mating disruption treatments, as well as a shaping behavior in the evolution of pheromone communication systems.     

Restricted ranging behaviour in a high-density population of urban badgers

By studying the responses of different species to urbanization, it is possible to understand the impact of this type of habitat modification and to explore, more generally, the link between variations in the environment and changes in behaviour. We radio collared 17 badgers Meles meles from six social groups in a 1 km² urban study area in Brighton, UK, where local badger population density was high, and collected data on their ranging behaviour between 2005 and 2007. We aimed to determine how badgers adapt their behaviour to an urban environment and to assess the generality of previously reported differences in the ranging and territorial behaviour of urban and rural badgers. Analysis of habitat preferences and movement patterns suggested that garden habitat was principally used for foraging, while scrub and allotment habitats were important in allowing animals to travel from one part of their range to another. Group and individual home ranges were the smallest so far recorded for badgers (mean 100% minimum convex polygons=9.26 and 4.91 ha, respectively). Individual range size was negatively correlated with the availability of garden habitat, suggesting that the rich food resources provided by gardens enabled ranges to be small. Group ranges were mostly non-contiguous and there was no evidence of territorial scent marking; rather, activity was mainly restricted to areas in the vicinity of main setts. It is clear that badgers can adapt successfully to urban habitats and that this process affects various aspects of their behaviour. However, our high-density population of urban badgers displayed patterns of behaviour that differed not only from those of typical rural badgers, but also in some respects from those of a previously studied low-density urban population. We conclude that generalizations about the effects of urbanization must be made with caution.     

Ecology and Translocation-Aided Recovery of an Endangered Badger Population

Abstract Southern British Columbia, Canada, is the northwestern range limit of the American badger (Taxidea taxus) and supports a nationally endangered subspecies. We initially investigated space-use, diet, and demography in southeastern British Columbia to characterize range-limit ecology. Resident badgers in the northern part (NP) of our study area were extirpated or nearly so during our study (λ = 0.7), whereas the southern (SP) badger population remained viable (λ = 1.2). This apparent difference in viability between NP and SP may have been confounded by timing because research occurred later in SP; litter size, number of Columbian ground squirrels (Spermophilus columbianus) consumed, and home range size were each correlated nearly equally to latitude and date of research, and survivorship was greater later in the study for both the NP and SP. Collectively, these factors indicated temporal, not just spatial, variability. Therefore, we translocated badgers into the NP to 1) determine whether the NP had lost its capacity to support badgers or had merely experienced the variability expected at a range limit and, if the latter, 2) initiate recovery. Translocated animals and their offspring had kit production equivalent to that of SP residents, adult survivorship intermediate between the NP and SP residents, and no confirmed kit mortality, with population growth projected (λ = 1.3). Diet of translocated individuals was similar to that of residents. Home ranges of translocated females were intermediate between the 2 resident groups, and home ranges of translocated males were not different than either resident group. Juvenile dispersal dates and distances were similar to those of residents for each sex. Our results were consistent with the extirpation of the NP being driven by temporally variable conditions or the effect of random events expected at range limits. The extirpation of NP did not appear to have been primarily due to any permanent loss of the NP's capacity to support badgers. At 3.5 years after starting translocations, badgers remained in the NP within an apparently growing population. We found translocation to be a useful diagnostic and conservation tool for badgers at their northern limit. Its utility may extend to countering the fluctuations typical of other rare, range-limit species.