Behaviour of badgers (Meles meles) in farm buildings: Opportunities for the transmission of Mycobacterium bovis to cattle?

Applied Animal Behaviour Science 117 (2009) 103–113

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Behaviour of badgers (Meles meles) in farm buildings: Opportunities for the transmission of Mycobacterium bovis to cattle? Bryony A. Tolhurst a,*, Richard J. Delahay b, Neil J. Walker b, Alastair I. Ward b, Timothy J. Roper a a b

Department of Biology and Environmental Science, University of Sussex, Brighton BN1 9QG, UK Central Science Laboratory, Sand Hutton, York YO41 1LZ, UK

A R T I C L E I N F O

A B S T R A C T

Article history: Accepted 23 October 2008 Available online 30 December 2008

Eurasian badgers (Meles meles) are implicated in the transmission of bovine tuberculosis (Mycobacterium bovis) to cattle. Here we investigate potential spatio-temporal foci of opportunities for contact between badgers and cattle in farm buildings. We discuss the relative occurrence of different badger behaviours and their potential for facilitating disease transmission, and examine correlates of building use by badgers including availability of specific farm-based resources, badger demography, and environmental variables. In addition, we investigate seasonal variation in home range structure with respect to farm building use. Badger activity and ranging behaviour were monitored intensively on six cattle farms throughout the year between July 2003 and June 2005 using remote surveillance, radio-tracking and faecal analysis. Badgers foraged in buildings, exhibited close, investigative ‘nose-to-nose’ contact with housed cattle and excreted/scent marked on and around feed. A negative correlation was observed between frequency of visits and 24 h rainfall and a positive correlation with minimum temperature. Badgers visited feed stores most intensively and selected cattle ‘cake’ over other available food types. A peak in visits was detected in spring and summer, and male badgers were more likely to visit buildings than females. Management prescriptions for disease prevention centre on reducing opportunities for direct or indirect contact between badgers and housed cattle. It is thus recommended that effort to exclude badgers from buildings should focus on feed stores and cattle housing during spring and summer in warm, dry weather. ß 2008 Elsevier B.V. All rights reserved.

Keywords: Badger Farm buildings Foraging behaviour Ranging behaviour Bovine tuberculosis Disease transmission

1. Introduction Bovine tuberculosis (bTB) in cattle, caused by the bacterium Mycobacterium bovis is regarded as one of the UK’s most serious animal health problems (House of Commons, 2008). The Eurasian badger (Meles meles L.) is susceptible to bTB infection and is a wildlife reservoir of M. bovis. There is compelling evidence to suggest that

* Corresponding author. Present address: School of Pharmacy and Biomolecular Sciences, University of Brighton, Cockcroft Building, Lewes Road, Brighton BN2 4GJ, Sussex, UK. Tel.: +44 1273 644 794; fax: +44 1273 679 333. E-mail address: [email protected] (B.A. Tolhurst). 0168-1591/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2008.10.009

transmission occurs between badgers and cattle (Krebs et al., 1997; Donnelly et al., 2006) but the precise mechanism remains unknown. Infection may occur via direct contact or indirectly when cattle graze on grass contaminated by badger urine or faeces (e.g., Benham and Broom, 1989, 1991; Brown et al., 1993; Hutchings and Harris, 1999) or investigate contaminated land in the vicinity of badger setts (e.g., Sleeman and Mulcahy, 1993; Courtenay et al., 2006). Transmission as a result of direct contact has received relatively little attention in the scientific literature because field observations suggest that badgers avoid grazing cattle (Benham and Broom, 1989; Benham, 1993). Anecdotal observations (Muirhead et al., 1974; Cheeseman and Mallinson, 1981; Sleeman and

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Mulcahy, 1993) and systematic evidence (Garnett et al., 2002a, 2002b; Roper et al., 2003; Tolhurst, 2006) suggest that badgers regularly forage in farm buildings such as feed stores and cattle sheds, where they consume and contaminate feed and may come into direct contact with cattle. Consideration of these possibilities is embodied in recent recommendations as to the role that farm bio-security measures can play as part of the UK’s bTB control strategy (Independent Scientific Group, 2007; Department for Environment Food and Rural Affairs, 2007). Detailed information on the behaviour of badgers in relation to farm buildings may help in the development of farm husbandry practices that minimise disease transmission risks. Garnett et al. (2002a, b) demonstrated that badger foraging activity in buildings peaked in July and was negatively correlated with total rainfall in the preceding 24 h. However the study was conducted at two farms only and data were collected solely during part of the year (March to October). Hence, the extent to which such activity is representative of cattle farms in the region, and the degree to which badgers visit farm buildings in the winter, remain unknown. Seasonal shifts in badger home ranges in relation to farm use were not quantified. Moreover, direct information on the frequency of occurrence of different farm foods in badger diet and the relative frequency of potentially high-risk behaviours in a range of building types, was absent. The current study aims to further quantify badger behaviour in farm buildings and investigate environmental correlates of farm visits, in order to identify spatiotemporal foci of bTB infection risk. The objectives were: (a) to test for year-round weather-related and seasonal variation in the intensity of badger use of farm buildings; (b) to test for variation in badger home range structure over time in relation to use of buildings; (c) to investigate differences in the frequency of badger visits to different farm building types; (d) to explore differences in the exploitation of different types of food; (e) to quantify behaviours considered to potentially incur infection risk; and (f) to examine demographic correlates of building use by badgers, such as sex-related differences. 2. Materials and methods 2.1. Study sites The study area comprised six farms in the south-west of England where badger population density and the incidence of bovine tuberculosis in cattle were high. The habitat consisted of a mixture of deciduous woodland, permanent pasture, farm buildings, houses and gardens, and pockets of arable land, including maize and cabbage fields. The farms were situated between 800 m and 48 km apart and were divided equally into beef and dairy herds. Some variation in cattle husbandry was observed, for example what cattle were fed, where they were kept, and when. At all three dairy farms, and one beef farm, cattle were fed in buildings throughout the year, and additionally some cattle, such as bulls and very young or sick calves, were housed during all seasons. At one of the remaining beef farms, cattle were permanently at pasture from April to September, with the occasional exception of young calves or sick animals and at the other, a bull was housed throughout the summer. The farms exhibited consistently poor bio-security measures with one exception, where some systematic procedures were put in place to exclude wildlife (for a full description of husbandry practices see Tolhurst, 2006; see below for details of cattle feed types available). At each farm, the study site was designated as the farm buildings plus surrounding farmland extending to a distance of 500 m in every direction,

creating a circle with an area slightly smaller than 100 ha (1 km2). This is broadly consistent with the size of the largest reported badger territory in the south-west of England (Krebs et al., 1997) and was consequently considered to be likely to encompass the home ranges of all badgers potentially visiting each farm. 2.2. Territory delineation and live-trapping of badgers The extent to which badger social group territories overlapped with farm buildings was identified at each study site using bait marking (Delahay et al., 2000). A mixture of peanuts conspicuously coloured indigestible plastic pellets and golden syrup was fed, once a day, at potential main setts within the 500 m circle at all study sites. The mix was deposited in up to 10 different ‘bait points’ around and within 15 m of the outer holes, created by making a small depression in the ground with the heel of the foot and covered with stones to prevent non-target uptake. This process was undertaken during spring 2003 for 10 consecutive days. During feeding and for a three-week period thereafter, all latrines were searched for ‘returns’ (scats containing beads) in a systematic survey radiating from each baited sett following badger paths. Returns recovered in farm buildings and yards were traced back to the sett at which the colour had been fed, and were assumed to be within the territory of the corresponding social group. Cage traps baited with peanuts (see Cheeseman and Mallinson, 1979) were then used to capture badgers at the main setts of social groups whose territories included farm buildings. Trapping occurred approximately four times per year, from June 2003 to June 2005, with a closed season between early February and mid May each year to avoid catching females with dependant cubs. Captured badgers were transferred under Home Office licence to a sampling facility, where they were anaesthetised using a mixture of ketamine hydrochloride, butorphanol tartrate and medetomedine (De Leeuw et al., 2004). Each individual was tattooed at first capture for identification, sexed and weighed (Clifton-Hadley et al., 1993). All badgers, except for cubs weighing less than 2 kg, were fur-clipped (Stewart and Macdonald, 1997) to provide a unique mark that would allow identification by remote surveillance and direct observation. A total of 50 badgers was captured from six different social groups, of which 39 were fur-clipped, and 17 (comprising 11 females and 6 males), fitted with split rawhide leather radio-collars (Cheeseman and Mallinson, 1979). Each collar weighed <1.5% of the average adult badger body weight, which is considerably less than the stipulated welfare criterion of 3% (Brander and Cochran, 1971; Cochran, 1980). Initial selection of individuals for radio-collaring was based on acquiring equal numbers of each sex, however low capture success in the second year of the study resulted in all adults being collared, excluding those with neck injuries or abnormalities. Exact numbers of animals in each social group were unknown, however badger social groups at nearby locations have been recorded to reach 30 individuals, and average 12 (Tuyttens et al., 2000). Based on these figures and the number of individuals fur-clipped (Table 1), it is estimated that a mean% of 54  8.5 badgers per social group were individually marked in this way. 2.3. Weather and season Site-specific daily rainfall data (mm) were collected using rain gauges (Wirefree Rain Monitor, Alana Ecology, Shropshire, UK) downloaded weekly, and temperature (8C) dataloggers (Tinytag Plus, Alana Ecology, Shropshire, UK) downloaded every three months. These data were validated by hourly weather data: rainfall (mm) and maximum and minimum temperature (8C) provided by a local weather station (Nailsworth Weather Station, Nailsworth, Gloucestershire, UK). Based on changes in photoperiod, the seasons were defined as winter (January, February and March), spring (April, May and June), summer (July, August and September), and autumn (October, November and December). 2.4. Remote surveillance Video surveillance equipment and still cameras with motion sensors were deployed at the six farms between October 2003 and June 2005 for 10 nights per month, in order to record badger visits to farm buildings. Video ‘installations’ (Highview Electronics, Mitcheldean, Gloucestershire, UK) consisted of a watertight plastic case containing a time-lapse Sony VCR, timer, compartment and terminals for one 12 V dry fit lead acid battery, and a video camera mounted with an infrared LED array. Still cameras (TRAILMASTER, Goodson and Associates, Inc., 10614 Widmer,

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Table 1 Number of fur-clipped and radio-collared badgers per social group, percentage of fur-clips detected by remote surveillance, and number of times detected throughout the study. Number of radio-tracked badgers

Number of fur-clips detected by remote surveillance

Percentage of fur-clips detected by remote surveillance

Social group

Number of fur-clipped badgers

1 2 3 4 5 6

12 4 12 4 5 2

4 1 7 2 3 0

2 1 4 2 2 0

17 25 33 50 40 0

39

17

11

28  7*

Total * **

Number of repeat visits by fur-clipped individuals 11, 6 19 1, 6, 2, 3 1, 1 2, 5 0 5  2**

Denotes mean (S.E.) percentage of fur-clipped badgers detected (‘total’ percentage being redundant in this context). Denotes mean (S.E.) number of repeat visits by individuals.

Lenexa, Kansas, 66215, USA) were triggered by both active infrared (AIR) sensors (two aligned units emit a beam of infrared light which is triggered when an object crosses) and passive infrared (PIR) sensors (one unit detects changes in infrared light emitted by animate moving objects). A total of 12 video installations and 13 still cameras were deployed, rotated between the six farms to obtain equal coverage of a sample of each type of facility during each season. Video cameras were positioned at the entrance of facilities to record the entire inside of feed stores, silage clamps and cattle housing. Footage of farmyards was recorded incidentally, as views of the entire inside of a building, and deployment of cameras out-of-reach of cattle often necessitated installation of a camera to simultaneously record a section of surrounding farmyard. Where badgers were detected in the farmyard but were not observed to enter the building, farmyard use was recorded. Still cameras were positioned to capture images of the entrance to facilities only, as we were not able to observe badger resource use using this method, moreover the range of view was restricted comparative to video, and entrances generally small enough to adequately monitor. Each remote surveillance sampling session, recorded concurrently at different facilities on the same night, was termed a ‘camera night’. Remote installations were programmed to record between sunset and sunrise throughout the year and settings were adjusted to incorporate changes in hours of daylight. Unforeseen circumstances (for example loss of battery power or disturbance caused by cattle chewing cables or knocking over tripods) occasionally reduced the number of hours recorded to less than the entire night. Hence length of camera night was noted throughout the study period and was observed to vary between 3 and 14 h. Feed types available within the facilities were noted immediately prior to each camera night. Video footage was analysed in terms of when individual badgers entered and exited a building; designated a ‘visit’, and what they were doing. Image clarity permitted behavioural observations, including what resources, if any were exploited, even if there were several different food types visible within the view. Numbers of badger ‘visits’, badgers visiting and duration of visits were analysed as three separate response variables: (i) total frequency of visits by badgers per camera night (potentially including repeat visits by the same individuals; (ii) mean duration of badger visits (in minutes) per

camera night and; (iii) maximum number of badgers in view per camera night (the maximum number of badgers visible for the duration of each visit). The latter variable was used as a proxy because accurate calculation of number of individual badgers visiting per camera night was prevented by a low rate of detection of fur-clips on the video footage (mean% 28  7; Table 1). Possible explanations include rapid fur re-growth, and few badgers captured proportional to group size. At least one repeat visit was recorded for all 11 fur-clipped individuals that were detected (Table 1), suggesting that exploitation of farm resources represents habitual rather than occasional behaviour. Seasonal effects were investigated using Generalized Linear Modelling (GLM) where all three response variables were modelled with a Poisson distribution and regressed against the categorical variable ‘season’ (GenStat for Windows Edition 8.1.0.152, VSN International Ltd., Hemel Hempstead, UK). Any effect of year and differences between individual farms were controlled for via inclusion in the model. The relationship between rainfall, temperature and response variable (i) (number of visits by badgers per camera night) was investigated using Generalized Linear Modelling (GLM) where the response was modelled with a negative binomial distribution. Maximum temperature was removed from the analysis on the basis of collinearity with minimum temperature, the latter being considered more biologically relevant because badgers are nocturnal and the lowest temperatures tend to occur at night. To standardise interpretation of the rate of badger visits across camera nights of varying length, the variable ‘number of hours per camera night’ was entered into the model as a log-transformed offset. In analyses where over-dispersion was present in the response (taken to be when residual mean deviance >2) inference was based on an F-test with residual mean deviance used as the denominator. Otherwise, change in deviance was used, referenced against a chi-squared distribution on the corresponding number of degrees of freedom. Relative frequencies of badger behaviours and visits to different farm facilities and feed types were compared using one-way ANOVA (Minitab 15 Statistical Software) after the response variables were converted to proportions and arcsine transformed. An ethogram was constructed (Table 2) from which five types of behaviour were selected for analysis:

Table 2 Ethogram of behaviours exhibited by badgers from video footage. Activity

Code

Description

Feeding (farm food) Foraging

1 2

Excreting or scent-marking Moving through Auto-grooming Intra-specific aggressive behaviour

3 4 5 6

Interacting with cattle

7

Interacting with cattle; nose-to-nose contact

8

Farm foods seen going in mouth/chewing observed. Sniffing the air or substrate/moving around in exploratory manner, searching ground, etc. Can include scent communication. Seen lifting tail and squatting onto substrate. Passes through facility or enters and exits view without exhibiting any other behaviour Application of tongue or paws to parts of body in repetitive movements. Shakes body. Conspecifics chasing/squaring up to each other and ruffling up fur. Engaging in aggressive physical contact such as biting of other animals rump and neck. Interactions characterized by investigative exploration by either species of the other, whereby animals came within 2 m of each other. Interactions characterized by investigative exploration by either species of the other, whereby the noses of both animals came within 10 cm (termed ‘nose-to-nose’ contact)

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Dietary components were quantified using the frequency of occurrence method (Skoog, 1970), expressed as a percentage of the total number of samples (Zabala and Zuberogoitia, 2003). Farm-derived foods were identified using a feeding trial reference collection (see Tolhurst, 2006) consisting of samples collected from the three study farms, and food availability information provided from study-site surveys (see below). Frequency of occurrence of different types of farm-derived food was compared using one-way ANOVA (Minitab 15 Statistical Software) after the response variable was converted to proportions and arcsine transformed

feeding, foraging, interacting with cattle, interacting with cattle (nose-tonose contact) and excreting/scent marking (it was not always possible to distinguish between defaecating, urinating and caudal or anal scent gland marking). The selection was based on the high frequency of occurrence of the former two behaviours and the high potential relative risk of bTB cross-infection associated with the latter three. 2.5. Radio-tracking A total of seventeen adult badgers were radio-tracked between July 2003 and June 2005. Ten of these were tracked for up to one year each for eight nights per month in repeated sequences of half-night sessions, in order to monitor their movement patterns and behaviour, and a further seven were tracked throughout spring 2005 to supplement data for this season. Triangulated radio-fixes were obtained from two vantage points and, where possible, badgers were located visually using a generation 2+ night-vision monocular. A minimum inter-fix interval of 30 min was chosen, because all study animals at one site could be located easily and each could comfortably traverse an average home range within this time, thus reducing the extent to which the data were temporally autocorrelated (Doncaster and Macdonald, 1997; Salvatori et al., 1999). Logistic regression was used to investigate differences in the frequency of radio-fixes located in buildings according to season and sex of badgers. A binomially distributed response variable (fix in buildings = 1, fix elsewhere = 0) was regressed against the categorical variables ‘season’, and ‘sex’ (GenStat for Windows Edition 8.1.0.152, VSN International Ltd., Hemel Hempstead, UK). Home ranges encompassing 95% of radio-fixes (considered to represent the outer home range boundary, excluding outlying locations: Kenward, 1987) and core activity areas were generated for each of the 11 female and 6 male badgers, for each season using minimum convex polygons (MCP) and kernel estimators (ArcView GIS 3.2, ESRI, Redlands, California and Ranges6 1.2, Anatrack Ltd., Wareham, Dorset, UK). Both techniques were used so as to allow comparison with other studies whilst accurately quantifying the internal structure of badger home ranges. Fixed kernels and a smoothing factor (h) selected by visual assessment were used for each of the 17 animals based on the raw distribution of fixes (e.g., Pope et al., 2004). The analysis was standardised by using the median value of h for every animal (Kenward, 2001). Utilization plots were generated to identify the percentage of fixes that defined the core area, using an inflection point determined by eye (Harris et al., 1990; Kenward and Hodder, 1996). Linear regression was used to investigate seasonal variation in home range and core area size overlapping the farm buildings at each site.

2.7. Study-site surveys A survey of each study site was carried out by one observer once per season, between July 2003 and June 2005, where anthropogenic food resources potentially available to badgers were recorded. In addition, the potential accessibility of stored feed to badgers was assessed using ranked scores from 1 to 5 as follows: 1 = inaccessible; 2 = fairly inaccessible; 3 = moderately accessible; 4 = little effort needed to gain access; and 5 = freely accessible.

3. Results 3.1. Study-site surveys: resource availability in farm buildings and surrounding land Food available on the study farms included standing crops, cereals in pheasant feeders and troughs on pasture, and stored cattle feed in buildings and yards. Five broad classes of stored feed were identified: silage, cereal grains, concentrated feeds (cattle ‘cake’ and ‘concentrates’), ‘straights’ (un-combined feeds), and hay and straw. Farm-building facilities were broadly divided into four categories: feed stores, cattle housing, farmyards and silage clamps. There was little seasonal or inter-annual variation in perceived accessibility to badgers of these facility types (see Table 3). 3.2. Weather-related variation

2.6. Dietary analysis

A negative association was found between rainfall in the 24 h preceding each period of remote surveillance and the frequency of badger visits to farm buildings and yards (GLM, F1,317 = 5.62, p < 0.05), and a positive association between minimum temperature and frequency of visits (GLM, F1,317 = 25.33, p < 0.001). An interaction between 24 h rainfall and minimum temperature (GLM, F1,316 = 28.16, p < 0.001 indicated that the effect of rainfall on badger visits to farms varied according to temperature.

Dietary investigation of scats to determine the relative frequency with which badgers exploited the different types of feed derived from farm buildings was carried out at a sub-sample of three of the study farms; time and labour constraints preventing scat collection and analysis at all sites. The three farms were selected on the basis of the consistent availability of the same feed types throughout the year. Feed types included maize and grass silage, cattle ‘cake’ (a pelleted meal consisting of items such as wheat, palm kernel, maize gluten, rapeseed extract, sunflower extract, molasses and vegetable oils) and ‘concentrates’, containing similar ingredients to cake but excluding molasses and vegetable oils as binding agents. A sample of 20 scats was collected from each of the three sites once per season, between July 2003 and June 2005, at latrines within 5 m of each badger sett and, where present, inside farm buildings. Scats were stored frozen and subsequently defrosted in 70% alcohol and separated into fractions using graded sieves. Each macro-fraction was then placed in a petri dish and viewed under 10 magnification using a binocular light microscope, in order to separate and identify food items.

3.3. Seasonal variation Remote surveillance showed seasonal variation in the frequency of badger visits to farm buildings and yards (GLM, change in deviance = 72.37, d.f. = 3, p < 0.001), the

Table 3 Modes of accessibility scores for each facility type at different times of year. W = winter; SP = spring; SU = summer; AU = autumn. Facility type

Mode of scores

Accessibility

W

SP

SU

AU

Feed store Cattle housing Farmyard Silage clamp

2 3 5 3

2 4 5 3

2 4 5 3

2 3 5 3

Fairly inaccessible Access possible with effort/little effort needed to gain access Freely accessible Access possible with effort

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Fig. 1. (a) Mean number of badger visits to farms during each season; (b) mean maximum number of badgers in view during each season; and (c) mean duration, in minutes, of badger visits per season. All data  S.E. and pooled across farms and years. Bars with a different letter denote seasons that were significantly different from each other (GLM, z tests, p < 0.05).

maximum number of badgers present during each visit (GLM, change in deviance = 44.21, d.f. = 3, p < 0.001) and the duration of visits (GLM, F3,939 = 14.20, p < 0.001). A peak in the former two variables was detected during spring (April, May and June) and in the latter during summer (July, August and September)(see Fig. 1). Between-farm (GLM, change in deviance = 40.43, d.f. = 3, p < 0.001) and annual (GLM, change in deviance = 54.57, d.f. = 3, p < 0.001) variation was also detected. An inter-

action between season and farm (GLM, change in deviance = 5.67, d.f. = 15, p < 0.001) suggested that seasonal differences were not consistent across farms. The frequency of badger radio-fixes located in farm buildings differed between seasons (GLM, change in deviance = 16.38, d.f. = 3, p < 0.001). Badgers were more frequently located in buildings during spring than in all other seasons and more in summer than in autumn or winter (Table 4). In addition, there was seasonal variation

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Table 4 Comparison of means tests for GLM analysis of radio-tracking data. The parameter estimate (Est.), z-statistic and p-value are shown for each combination of explanatory levels, indicating the direction of the relationship between the 1st season and the 2nd on each row. Season

Frequency of radio-fixes in farm buildings

Overlap between core areas and farm buildings

Est.

z

p

Est.

z

p

Spring v summer Spring v autumn Spring v winter Summer v autumn Summer v winter

1.140 2.796 3.220 1.656 2.080

2.22 3.59 3.14 2.06 2.86

<0.05 <0.001 <0.05 <0.05 <0.05

1.230 3.420 2.830 1.670 1.520

1.16 2.28 2.02 1.25 1.12

NS <0.05 <0.05 NS NS

Fig. 2. (a) 95% kernel isopleth and (b) 100% minimum convex polygon home ranges for a male badger during autumn (dark grey), winter (black), spring (light grey) and summer (black and white hatched). The extent of the farm-building complex (LH bottom corner) is denoted by a black border and the position of the main sett by a black asterisk.

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in the overlap between badger home ranges and farm buildings and yards (GLM, change in deviance = 3.06, d.f. = 3, p < 0.05) (Fig. 2). Badger core areas were more likely to overlap with farm buildings during spring than during autumn or winter (see Table 4). 3.4. Frequency of badger visits to different farm facility types Badgers visited all four types of facility and variation was detected in the frequency of visits to each (one-way ANOVA, F3,16 = 3.47, p < 0.05). Visits to feed stores were more frequent than to any other facility type, followed (in descending order) by cattle housing, farmyards and silage clamps (Fig. 3). 3.5. Food types exploited Five different types of farm-derived food were observed in badger scats: cattle ‘cake’ or concentrated feed (it was

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not possible to distinguish between these two), rolled barley grains, wheat grains, wheat silage and maize silage. Variation was detected in the frequency of occurrence of the five food types (one-way ANOVA, F4,15 = 19.47, p < 0.001), with greater numbers of scats containing cattle ‘cake’ or concentrates than all others, followed in descending order by barley, wheat, maize silage and wheat silage (Fig. 4). Remote surveillance revealed badger visits to facilities containing five different types of farmderived food: cattle ‘cake’, maize silage, wheat grains, cattle ‘cake’ mixed with maize silage, and grass silage mixed with maize silage. Variation that approached significance was detected in the frequency with which badgers visited facilities containing the different food types (one-way ANOVA, F4,15 = 3.06, p = 0.05), with more frequent visits to those containing cattle ‘cake’ than all other types of farm-derived food (one-way ANOVA, comparisons of means tests, p always <0.05), followed by (in descending order) cattle ‘cake’ mixed with maize

Fig. 3. Proportions of badger visits to different farm facilities  S.E. (data pooled across farms and years) expressed as percentages. Bars with a different letter denote facility types that were significantly different from each other (p < 0.05) (one-way ANOVA, comparisons of means tests).

Fig. 4. Proportions of different food types in badger scats containing farm-derived foods  S.E. (data pooled across farms, seasons and years) expressed as percentages. Bars with a different letter denote proportions of food types that were significantly different from each other (p < 0.05) (one-way ANOVA, comparisons of means tests).

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Fig. 5. Proportions of different behaviours recorded during badger visits to farm buildings  S.E. (data pooled across farms and years) expressed as percentages. Bars with a different letter denote behaviours that were significantly different from each other (p < 0.05) (one-way ANOVA, comparisons of means tests).

silage, maize silage, wheat/maize silage mixed with grass silage, and hay. 3.6. Badger behaviour The frequency of occurrence of the five behaviours varied (one-way ANOVA, F4,15 = 6.23, p < 0.05) with feeding occurring more frequently than all other behaviours (Fig. 5). All of the observed ‘nose-to-nose’ contacts (N = 31) occurred in cattle housing, whereas 69.2 % of badger excretions/scent markings (N = 17) occurred in feed stores and 15.4% occurred in each of silage clamps and cattle housing. A sex difference was demonstrated in the frequency of radio-locations in buildings (GLM, change in deviance = 18.01, d.f. = 1, p < 0.001) and in the overlap between core activity areas and farm buildings (GLM, change in deviance = 3.98, d.f. = 1, p < 0.05). Male badgers were located in buildings more frequently than females (comparison of means tests, parameter estimate = 3.790, z = 3.30, p < 0.001) and their core areas were more likely to contain farm buildings (comparison of means tests, parameter estimate = 3.220, z = 2.54, p < 0.05). 4. Discussion Our results, taken from a larger sample of farms, and incorporating year-round effects, confirm the findings of Garnett et al. (2002a, b) in that frequency of badger visits to farms was negatively correlated with 24 h rainfall. We investigated this relationship in more detail and found an interaction between rainfall and minimum temperature, which suggests that increasing temperature may result in a corresponding increase in badger visits to farms, provided that rainfall is low. Anecdotal observations during radiotracking sessions were consistent with this hypothesis: badgers were observed to forage on pasture on warm, rainy nights and in farm buildings and yards on warm dry nights. Earthworms dominate the diet of badgers in Britain (Kruuk et al., 1979; Kruuk and Parish, 1981) and the species favoured by badgers (Lumbricus terrestris and rubellus) are

most commonly found under pasture where they forage on the surface at temperatures above 2 8C following recent rainfall (Satchell, 1967). Conversely, when the weather is dry or very cold, worms retreat deep underground and are not accessible to badgers, forcing them to seek alternative food sources. Badgers may be more active at higher temperatures per se, but it is likely that rainfall influences the direction of activity, i.e., towards buildings or to other parts of the home range. In our study the frequency of visits and number of badgers visiting peaked in spring, but visits lasted longer in summer and were also more likely to occur in summer than in winter or autumn. Such seasonal variation was unlikely to have been driven by changes in the availability of farm-derived foods, which was shown to vary little throughout the year. It is more likely that differential use of farm buildings at different times of year reflects changes in badger body weight, energy requirements and activity levels. Seasonal fluctuations in badger body weight have been noted by several authors (Neal, 1977; Kruuk, 1989; Rogers et al., 1997) and linked to both nutritive status (Hanks, 1981) and other factors such as day-length and temperature (Kruuk and Parish, 1983). Given the predominance of earthworms in badger diet (Kruuk and Parish, 1981) and the positive correlation between earthworm biomass and both badger body weight (Kruuk and Parish, 1985) and population size (Kruuk and Parish, 1982), seasonal fluctuations in rainfall might be expected to influence nutritive status, through effects on earthworm availability. Hence the availability of farm-derived foods during periods when earthworms are scarce may provide badgers with an important alternative source of nutrition. Most visits to farm buildings by badgers were recorded in feed stores, which reflects the main purpose of the visits, i.e., to obtain food (Garnett et al., 2002a, 2002b). Resources are likely to be more accessible and more attractive to badgers when taken from feed stores, partly because of the absence of cattle, although studies documenting the response of badgers to cattle (on pasture) are equivocal and report both habituation (Kruuk, 1989; Brown et al.,

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1993) and avoidance (Benham and Broom, 1989; Sleeman and Mulcahy, 1993). The high frequency of occurrence of cattle cake/ concentrates and barley in badger scats relative to forage feeds is consistent with the findings of Benham (1985, 1993), who detected a preference by badgers for cattle cake and barley in feed choice experiments, and Garnett et al. (2002a, b) who identified cattle cake to be the targeted resource in over 55% of badger visits to farm buildings. Evidence from remote surveillance from the present study also indicated disproportionate selection of facilities containing cattle ‘cake’ mixed with maize silage. This finding is potentially important, given that this combination is likely to be available only in cattle housing where risks of contact between badgers and cattle may be high. The higher frequency of farm visits by male badgers in the present study could potentially be linked to social dominance or differences in energy requirements or home range size. There is no evidence of interference competition based on a sex-related linear dominance hierarchy in the Eurasian badger (Macdonald et al., 2002) and only minimal aggression was observed between feeding individuals in the present study (aggressive behaviour was recorded from less than 3% of badger visits to buildings). Males might however visit buildings more frequently as a direct consequence of their home ranges encompassing a larger area (Neal and Cheeseman, 1996), but in our study this explanation is unlikely given that at all study sites main setts were present within four hundred metres of the farm buildings, which would have been incorporated in the home ranges of both sexes. Hence, the most plausible hypothesis explaining the observed sex-related variation in visits to farm buildings may relate to differences in energy budgets, although no data currently exists to support this. Transmission of bovine tuberculosis during badger foraging visits to farm buildings and yards could potentially occur through the respiratory route as a consequence of the ‘nose-to-nose’ contact described. Aerosol infection is more likely to occur in buildings than on pasture (Ministry of Agriculture, Fisheries and Food, 2000) and the survival of airborne microorganisms is aided by the dark, humid conditions of cattle housing, particularly if intensivelystocked and poorly ventilated (Robertson, 2000). In addition, in the present study, farm workers were observed to collect feed from feed stores and silage clamps at least twice a day, all of which was mixed and fed immediately to housed cattle. Hence, any badger excreta deposited in feed stores and silage clamps was likely to be transferred to troughs or the floor of cattle housing within 24 h of being deposited. Any remaining excreta, particularly if incorporated into feed, could remain infective for long periods, given that M. bovis persists in conditions of limited exposure to ultraviolet light (Wray, 1975; Wilesmith, 1991; King, 1997). Subsequent transmission of infection to cattle could potentially occur by ingestion during unselective feeding (Central Science Laboratory, 2006), by eructation and inhalation into the lungs, or inhaled directly into the respiratory system via the explosive snorting associated with cattle exploratory behaviour of novel food items.

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Knowledge gaps emerging from this study include a lack of empirical data on the likelihood of transmission per given contact between badgers and cattle, and the persistence of M. bovis in different types of excreta in buildings. Furthermore, annual and between-farm variation in badger use of buildings indicates that management advice for preventing access to farms by badgers may be most effective if ‘‘tailor-made’’ for individual farms rather than broad-based prescriptions. Differing husbandry practices between farms, individual differences in badger behaviour and yearly changes in rainfall are potential sources of variation. Potential measures to exclude badgers from housing and feed stores range from exclusion methods such as electric fencing (see Tolhurst et al., 2008) and simple procedures such as closing the doors of feed sheds at night (Department for Environment Food and Rural Affairs, 2007), to improved ‘‘housekeeping’’, for example clearing away spilled cattle cake from beneath silo bins. The extent to which the six farms represent the situation throughout bovine tuberculosis ‘‘hotspots’’ however, is unknown. 5. Conclusion In this study we identify spatio-temporal foci of potential bTB transmission arising from the habitual use of farm buildings by badgers. Badgers were most likely to visit feed stores containing cattle cake in spring and summer on warm, dry nights, and to exhibit ‘nose-to-nose’ contact with cattle in housing. Common-sense measures to prevent contact between badgers and cattle are recommended. Acknowledgements This study forms part of a DPhil project by the first author, funded by DEFRA (Division of Animal Health), under contract SE3029. We thank the farmers and landowners; Irvine Carter, John Jones, Martin Wooldridge, Jan Rowe, Alan Smith, and Burt Mayo for their cooperation and assistance. We are also indebted to Ivan Judd at the Nailsworth weather station for supplying rainfall and temperature data. Finally, we are especially grateful to the field staff at the Central Science Laboratory research station, Woodchester Park, for their expertise in trapping and handling badgers, in particular Paul Spyvee, Sarah Boxall and Chris Hanks, without whom the study would not have been possible. References Benham, P.F.J., 1985. A study of cattle and badger behaviour and farm husbandry practices relevant to the transmission of bovine tuberculosis (Mycobacterium bovis). Ph.D. thesis, The University of Reading, UK. Benham, P.F.J., 1993. In: Hayden, T.J. (Ed.), The Badger. The Interactive Behaviour of Cattle and Badgers with Reference to Transmission of Bovine Tuberculosis. Royal Irish Academy, Dublin, Eire, pp. 189–195. Benham, P.F.J., Broom, D.M., 1989. Interactions between cattle and badgers at pasture with reference to bovine tuberculosis transmission. Br. Vet. J. 145, 226–241.

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