Author Name: Simon Parkinson; BSc (Hons) Bioveterinary Science
Bovine tuberculosis (TB) is an infectious disease of cattle that is widespread across Great Britain. Large numbers of cattle are culled every year as a result of TB infection. Bovine TB. although mainly affecting cattle, can infect a range of wildlife such as badgers and deer as well as humans. It is widely believed that the spread of bovine TB is caused by transmission from badgers to cattle through contamination of grazing pastures. As a result, a number of culling trials have been implemented to assess the efficacy of badger culls in reducing the occurrence of bovine TB. One of the main issues believed to prevent significant reductions in TB in cattle is the perturbation of badgers, which is the social disruption and increased movement of badgers as a result of culling. A number of studies have drawn conclusions about the occurrence of perturbation as a result of culling however many factors have affected the reliability of the data produced in these studies. These factors include trapping methods, selection of culling and control sites, TB diagnostic techniques and methods of calculating the home ranges of badgers. Overall, more research is needed to enable accurate and reliable conclusions to be drawn as to whether perturbation of badgers as a result of culling is a significant factor in the failure to reduce the incidence of TB in cattle.
Bovine tuberculosis (TB) is a widespread issue affecting the farming industry throughout the UK, with the problem being endemic in certain areas (Lawes et al. 2016). It has been widely concluded that one of the main routes of transmission of TB in cattle is via infection from badgers through contamination of pastures with urine and faeces (Hutchings and Harris, 1997). As a result of this, a governmental action plan was set up to combat the spread of TB in the UK. Methods employed include the development of vaccines, monitoring of herd health and improving biosecurity and husbandry on farms (Jenkins, Woodroffe and Donnelly, 2008). Additionally, there has been implementation of widespread badger cull trials across the UK, resulting in both positive and negative changes in the incidence of bovine TB in cattle in areas of culling. One of the main issues believed to prevent the effective reduction of cases of bovine TB in cattle by culling is the perturbation of badgers (Rogers et al. 1998). Perturbation is the disruption to the social organisation and behaviour patterns of individuals in a population, causing animals to leave their natural ranges (McDonald et al. 2008). McDonald et al. (2008) outlines that increased ranging behaviour can be seen in badgers in areas of culling. A range of studies have concluded that perturbation of badgers is a significant factor in reducing the success of badger culls and may even lead to increased incidence of bovine TB in cattle. However, the findings of other studies suggest that culling has not resulted in the perturbation of badgers.
2.0 Literature Review
2.1 The Randomised Badger Culling Trial
The Randomised Badger Culling Trial (RBCT) is the largest culling field trial in the UK with culling implemented in 30 studied zones (DEFRA, 2007). This study found that there was a 23% reduction of TB in cattle within the culling areas. However in a 2km area surrounding the culling sites, an average 25% increase in cases of TB in cattle was observed. DEFRA (2007) concluded that where culling was implemented the badgers’ home ranges were significantly larger and overlapped with neighbouring territories. This is believed to increase the spread of TB as infected badgers contaminate wider areas of land and come into contact with other groups of badgers and cattle herds (Cox et al. 2005). DEFRA (2007) used the bait marking method to estimate the home ranges for the studied badgers to analyse whether culling affected their movement. Bait marking involves the feeding of indigestible pellets to badgers which are later identified in faeces, indicating the movement of badgers from their sets (Delahay et al. 2000). In another study by Woodroffe et al. (2006) where culling in 13 sites was implemented, bait marking was also used to calculate home ranges. Woodroffe et al. (2006) concluded that spatial organisation of badgers is influenced by culling. Bait marking was found to be an effective way of estimating home ranges in a study by Carter et al. (2007), however they stated that bait marking may underestimate home ranges of badgers in areas where culling is in place due to low numbers of bait returns. Furthermore a study by De Solla, Bonduriansky and Brooks (1999) states that the intervals that faeces are recorded, type of bait and error in identification of bait-markers in faeces are all factors that reduce the accuracy of the bait-marking method. Underestimation of the normal ranges of badgers in the study by DEFRA (2007) and Woodroffe et al. (2006) could mean that the movement observed may have been normal and not as a result of perturbation due to culling. In a study by Tuyttens et al. (2000) badger culls were put in place surrounding a farm in North Nibley in Gloucestershire following the identification of several TB positive cattle. Tuyttens et al. (2000) concluded that increased movement and overlap of group ranges occurred as a result of culling, and was subsequently followed by increasing incidence of TB in the area. Similarly to the DEFRA (2007) study, bait marking was used to calculate home ranges of badgers in the study area, however to eliminate the underestimation of the natural home ranges which may have occurred in the DEFRA (2007) and Woodroffe et al. (2006) studies, the mean distance between a badger set and the bait returns was calculated. This is believed to provide a more reliable representation of the home ranges of badgers (De Solla, Bonduriansky and Brooks, 1999). Furthermore in this study, radio tracking was also used alongside bait marking. This involved tracking of badgers fitted with radio collars both at night and during the day, to create data on the movement and ranges travelled by badgers from the studied sets. Huck, Davison and Roper (2008) concluded that radio-tracking can effectively calculate the home range sizes of badgers. This suggests that the home range sizes for badgers calculated in the study by Tuyttens et al. (2000) are more accurate than those collected by DEFRA (2007) and Woodroffe et al. (2006) due to the utilisation of both bait marking and radio-tracking. In a study by Balestrieri et al. (2016), it was found that using camera-traps was a reliable method for predicting home ranges of badgers. This study successfully identified 19 sets and the home ranges of theses badgers in Northern Italy. Implementation of this method in the badger cull trials may have produced more accurate estimations of the home ranges of the studied badgers, allowing more accurate conclusions of the perturbation that occurs as a result of culling.
2.2 The Four Areas Trial
The Four Areas trial conducted in the Republic of Ireland was put in place between 1997 and 2002 by Griffin et al. (2005). This trial involved the implementation of badger culls across four counties in Ireland. The Four Areas trial successfully reduced the occurrence of TB in cattle in the study areas as a result of culling and concluded that culling can be an effective strategy in controlling bovine TB. The Four Areas trial had a smaller sample population of badgers than in the DEFRA (2007) study. Badger density in the trial areas was found to be only around 40% of that studied by DEFRA (2007), and the total badgers captured and culled were 2360 in the Four Areas trial compared to over 8900 by DEFRA (2007). Woodroffe et al. (2009) outlines that badger population density has a direct correlation with the prevalence of TB in the badgers. Therefore, data collected from the Griffin et al. (2005) study may be less accurate in showing the effects of culling and the spread of TB than that of the DEFRA (2007) study due to a smaller sample population and lower badger population densities. In comparison to other badger culling studies this however is a large sample population, with the Tuyttens et al. (2000) study only looking at 22 groups of badgers and only culling 27 badgers and the Woodroffe et al. (2006) study using only 13 culling sites (compared to 30 in the study by DEFRA (2007). Smaller populations of badgers studied, lower badger population densities and smaller study areas reduce the reliability of the data collected.
2.3 Methods of capturing badgers for culling
Methods of capturing badgers for culling varies between the studies with cage traps being used in the DEFRA (2007) and Tuyttens et al. (2000) studies, whereas Griffin et al. (2006) used snares. Munoz-Igualada et al. (2008) state that using snares is a more effective method of trapping badgers than cage traps. Furthermore Griffin et al. (2006) performed culling two or three times per year compared to only once a year in the DEFRA (2007) and Tuyttens et al. (2000) studies. During the study by DEFRA (2007) badgers were only trapped on land inside areas where cull consent had been given by landowners, meaning that there were areas of inaccessible land (Donnelly et al. 2007). Donnelly et al. (2007) state that within these inaccessible areas 28% fewer badgers were captured per km2. This suggests that the capture of badgers in the study by Griffin et al. (2006) was more successful than in the other studies, resulting in a greater capture success. Unsuccessful trapping of badgers may be a possible reason for why perturbation of badgers was observed by DEFRA (2007) and Tuyttens et al. (2000) (Woodroffe et al. 2005). This may indicate that if culling and trapping is performed more successfully via methods such as snaring then perturbation may not occur.
2.4 Selection of Trial Sites
The trial sites in the studies by DEFRA (2007) and Tuyttens et al. (2000) were selected so that they had neighbouring farmland. These boundaries easily allowed badgers to move between areas in response to the culls. This observed perturbation was found to vastly increase the spread of TB as a result in both studies (Wilson, Carter and Delahay, 2011). This can similarly be seen in a study by Vincente et al. (2007) where culling procedures were put in place in an area of the Cotswolds and they observed increased social disturbance as a result of culling. This study used a study site surrounded by agricultural land, which allows the movement of badgers out of the area. This makes the data produced widely applicable to farmland across the UK, the majority of which would have similar boundaries to the trial sites used (O’Connor, Haydon and Kao, 2012). The Griffin et al. (2006) study selected trial sites that were located so that a large proportion of their boundaries were natural barriers to the movement of badgers such as coastlines and rivers (Wilson, Carter and Delahay, 2011). This would have significantly reduced the occurrence of perturbation as the badgers are contained within the study area, preventing movement and resultant spread of infection outside the culling sites (Wilkinson et al. 2009). This prevention of perturbation was also seen in the badger cull trial in Thornbury in 1975 (Clifton-Hadley et al. 1995). The site of this trial was contained by rivers on two sides and motorways on the other two sides. Although this study, along with the Griffin et al. (2006) study, successfully eradicated TB in cattle in the area suggesting that culling could be an effective method of reducing TB, by preventing the free movement of badgers this does not enable analysis of the impacts of perturbation on the success of culling on a wider scale (O’Connor, Haydon and Kao, 2012).
2.5 Control Sites
A control population is used for comparison with the culling sites to allow analysis of the effects of culling. In the DEFRA (2007) study the control sites that were used as comparison were adjacent areas of land to that where culling was implemented. This enabled accurate comparison of the two areas as conditions, such as physical barriers, which can impact on the response badgers have to culling, are the same at both locations (Pope et al. 2007). DEFRA (2007) further ensured the reliability of the comparison between the culling sites and the control sites by using a 2km buffer around each site. This was implemented to ensure that the sites were sufficiently separated so that badgers would not easily move between the sites. The study by Griffin et al. (2006) similarly used a 3km buffer around each study site, although the control sites were selected by matching criteria such as badger density, livestock density and geographical features. This method analyses the chosen sites to ensure that they are statistically similar (Griffin et al. 2005). By ensuring a valid comparison between the culling sites and the control sites it ensures that the observed effects are as a result of culling and not by chance. In the studies by Tuyttens et al. (2000) and Vincente et al. (2007), control sites were not used as the studies analysed the TB incidence before and after culling at one specific location. This is a less reliable way of assessing the impacts of the culls as any observed effects may have occurred by chance and not as a result of culling, but without a control site this cannot be determined.
2.6 Tuberculin Skin Test
In the study by DEFRA (2007) the tuberculin skin test was used to diagnose cases of TB in cattle in the study areas. The tuberculin skin test is commonly used in diagnostics of TB in cattle in the UK however it is believed that a range of factors can reduce the sensitivity and specificity of this test (de la Rua-Domenech et al. 2006). Monaghan et al. (1994) state that the sensitivity of tuberculin skin tests can be as low as 68% depending on factors such as the dose and potency of the tuberculin administered. This may have led to inaccurate data regarding the cases of TB in cattle in the studied areas which would mean any conclusions produced may be inaccurate. Moreover due to the large scale and wide study area used in the DEFRA (2007) study, diagnostics were conducted by a range of people, whereas in the study by Griffin et al. (2006) the same individuals were used to perform each diagnosis. This will minimise the potential for measurement bias and increase the likelihood of the data being accurate (Griffin et al. 2006). The studies by Griffin et al. (2006) and Tuyttens et al. (2000) used a combination of diagnostic methods including veterinary post-mortem and the Interferon gamma assay. Vordermeier et al. (2006) state that the Interferon gamma assay has increased sensitivity compared to the tuberculin skin test, making it a more reliable diagnostic method. Post-mortem was used in these studies alongside the use of the interferon gamma assay. These studies only recorded a positive TB result if tuberculous lesions were found at post-mortem, however Schiller et al. (2010) state that the sensitivity of post-mortem diagnosis of TB in cattle may be as low as 28.5%. This may have led to incorrect data regarding the incidence of TB in cattle in the studies. The study by Clifton-Hadley et al. (1995) used a combination of the tuberculin skin test and post-mortem diagnostics as the methods of diagnosing TB. Both these methods have been shown to be unreliable and have low sensitivity compared to methods such as the interferon gamma assay, meaning the data collected in the study regarding the incidence of TB in cattle in the study area is unreliable and may be incorrect.
2.7 General concerns
In a review of the data collected in the DEFRA (2007) study, DEFRA (2011) outlined that 3.8% of all traps laid were interfered with or stolen. This means that data collected may not provide a valid and reliable representation of the effects of culling in that area as trapping of badgers was not completed. Furthermore, on average 6.1% of deployed traps were interfered with by the capture of wildlife other than badgers. This may have affected the capture success of the badgers in this study which may have been a cause for the observed perturbation. In addition, the study by Vincente et al. (2007) outlines that the study was funded by DEFRA. Although a governmental body ,this may have induced bias into the study to corroborate findings with the large scale DEFRA (2007) study. Furthermore the studies outlined in this review are quite dated and due to the age of the data collected may be unreliable when applying this to situations in the modern day. More current studies evaluating the effect of badger culls on their perturbation are needed to produce accurate conclusions.
In conclusion, this review suggests that the data relating the perturbation of badgers as a result of culling to the failure to produce significant reductions in TB in cattle is not reliable enough to draw a valid conclusion. Studies such as DEFRA (2007), using large sample sites and large badger populations, concluded that perturbation was observed as a result of culling. This large sample improves the reliability of the study, however factors such as ineffective trapping methods and unreliable TB diagnostic techniques means that data collected may not provide reliable conclusions. The study by Griffin et al. (2006) produced evidence against the perturbation theory, also using a large sample population and more effective badger capturing techniques than in the DEFRA (2007) study, however does not provide reliable conclusions on the effects of perturbation due to its selected study site. Other studies looking into the effect of perturbation as a result of culling use much smaller badger populations and therefore provide less reliable conclusions about perturbation. Overall, in order to produce an accurate conclusion, more research is needed to eliminate these errors that reduce the reliability of prior badger cull trials.
Balestrieri, A., Cardarelli, E., Pandini, M., Remonti, L., Saino, N. and Prigioni, C. (2016) Spatial organisation of european badger (Meles meles) in northern Italy as assessed by camera-trapping. European Journal of Wildlife Research. 62 (2), pp. 219-226.
Carter, S.P., Delahay, R.J., Smith, G.C., Macdonald, D.W., Riordan, P., Etherington, T.R., Pimley, E.R., Walker, N.J. and Cheeseman, C.L. (2007) Culling-induced social perturbation in eurasion badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology. Proceedings of the Royal Society of Biological Sciences. 274 (1626)
Clifton-Hadley, R.S., Wilesmith, J.W., Richards, M.S., Upton, P. and Johnston, S. (1995) The occurrence of mycobacterium bovis infection in cattle in and around an area subject to extensive badger (Meles meles) control. Epidemiology and Infection. 114, pp. 179-193.
Cox, D.R., Donnelly, C.A., Bourne, F.J., Gettinby, G., McInerney, J.P., Morrison, W.I. and Woodroffe, R. (2005) Simple Model For Tuberculosis in Cattle and Badgers. Proceedings of the National Academy of Sciences Usa. 102, pp. 17588-17593.
De La Rua-Domench, R., Goodchild, A.T., Vordermeier, H.M., Hewinson, R.G., Christiansen, K.H. and Clifton-Hadley, R.S. (2006) Ante mortem diagnosis of tuberculosis in cattle: a review of tuberculin tests, y-interferon assay and other ancillary diagnostic techniques. Research in Veterinary Science. 81 (2), pp. 190-210.
De Solla, S.R., Bonduriansky, R. and Brooks, R.J. (1999) Eliminating Autocorrelation reduces biological relevance of home range estimates. Journal of Animal Ecology. 68 (2), pp. 221-234.
DEFRA. (2007) Bovine TB: The Scientific Evidence. Available from: http://webarchive.nationalarchives.gov.uk/20090330154646/www.defra.gov.uk/animalh/tb/isg/pdf/final_report.pdf [Accessed 25.10.16]
DEFRA. (2011) Request for information: Number of traps sited, interfered with and removed during the Randomised Badger Culling Trial (RBCT). Available from: http://www.bovinetb.info/docs/rbct-number-of-traps-interfered-with-and-removed-each-year.pdf [Accessed 25.10.16]
Delahay, R.J., Brown, J.A., Mallinson, P.J., Spyvee, P.D., Handoll, D., Rogers, L.M. and Cheeseman, C.L. (2000) The Use of Marked Bait in Studies of the Territorial Organization of the European Badger (Meles meles). Mammal Review. 30 (2), pp. 73-87.
Donnelly, C., Wei, G., Johnston, T., Cox, D.R., Woodroffe, R., Bourne, J., Cheesman, C.L., Clifton-Hadley, R.S., Gettinby, G., Gilks, P., Jenkins, H.E., Le Fevre, A.M., McInerney, J.P. and Morrison, I. (2007) Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. International Journal of Infectious Diseases. 11 (4), pp. 300-308.
Gallagher, J. and Clifton-Hadley, R.S. (2001) Tuberculosis in badgers; a review of the disease and its significance for other animals. Available from: http://www.bovinetb.info/docs/johngallt_b_review9-04.pdf [Accessed 26.10.16]
Griffin, J.M., More, S.J., Clegg, T.A., Collins, J.D., O’Boyle, I., Williams, D.H., Kelly, G.E., Costello, E., Sleeman, D.P., O’Shea, F., Duggan, M., Murphy, J. and Lavin, D.P.T. (2006) Tuberculosis in cattle: the results of the four-area project. Irish Veterinary Journal. 58 (11), pp. 629-636.
Griffin, J.M., Williams, D.H., Kelly, G.E., Clegg, T.A., O’Boyle, I., Collins, J.D. and More, S.J. (2005) The impact of badger removal on the control of tuberculosis in cattle herds in Ireland. Preventative Veterinary Medicine. 67 (4), pp. 237-266.
Jenkins, H.E., Woodroffe, R. and Donnelly, C.A. (2008) The effects of annual widespread badger culls on cattle tuberculosis following the cessation of culling. International Journal of Infectious Diseases. 12 (15), pp. 457-465.
Lawes, J.R., Harris, K.A., Brouwer, A., Broughan, J.M, Smith, N.H. and Upton, P.A. (2016) Bovine TB Surveillance in Great Britain in 2014. The Veterinary Record. 178 (13), pp. 310-315.
McDonald, R.A., Delahay, R.J., Carter, S.P., Smith, G.C. and Cheeseman, C.L. (2008) Perturbing Implications of Wildlife Ecology For Disease Control. Trends in Ecology and Evolution. 23 (2), pp. 53-56.
Monaghan, M.L., Doherty, M.L., Collins, J.D., Kazda, J.F. and Quinn, P.J. (1994) The tuberculin tests. Veterinary Microbiology. 40 (2), pp. 111-124.
Munoz-igualada, J., Shivik, J.A., Dominguez, F.G., Lara, J. and Gonzalez, L.M. (2008) Evaluation of Cage-traps and Cable Restraint Devices to Capture Red Foxes in Spain. Journal of Wildlife Management. 72 (3), pp. 830-836.
O’Connor, C.M., Haydon, D.T. and Kao, R.R. (2012) An Ecological and Comparative Perspective on the Control of Bovine Tuberculosis in Great Britain and the Republic of Ireland. Preventative Veterinary Medicine. 104 (3), pp. 185-197.
Pope, L.C., Butlin, R.K., Wilson, G.J., Woodroffe, R., Erven, K., Conyers, C.M, Franklin, T., Delahay, R.J., Cheeseman, C.L. and Burke, T. (2007) Genetic Evidence That Culling Increases Badger Movement: Implications For the Spread of Bovine Tuberculosis. Molecular Ecology. 16 (23), pp. 4919-4929.
Rogers, L.M., Delahay, R., Cheeseman, C.L., Langton, S., Smith, G.C. and Clifton-Hadley, R.S. (1998) Movement of badgers (Meles meles) in a high density population: individual, population and disease effects. Proceedings of the Royal Society of Biological Sciences. 265 (1403), pp. 1269-1276.
Schiller, I., Oesch, B., Vordermeier, H.M., Palmer, M.V., Harris, B.N., Orloski, K.A., Buddle, B.M., Thacker, T.C., Lyashchenkon, K.P. and Waters, W.R. (2010) Bovine Tuberculosis: A Review of Current and Emerging Diagnostic Techniques in View of their Relevance for Disease Control and Eradication. Transboundary and Emerging Diseases. 57 (4), pp. 205-220.
Tuyttens, F.A.M., Delahay, R.J., Macdonald, D.W., Cheeseman, C.L., Long, B. and Donnelly, C.A. (2000) Spatial perturbation caused by a badger (Meles meles) culling operation: implications for the function of territoriality and the control of bovine tuberculosis (mycobacterium bovis). Journal of Animal Ecology. 69 (5), pp. 815-828.
Vicente, J., Delahay, R.J., Walker, N.J. and Cheeseman, C.L. (2007) Social Organization and Movement Influence the Incidence of Bovine Tuberculosis in an Undisturbed High-density Badger Meles meles Population. Journal of Animal Ecology. 76 (2), pp. 348-360.
Vordermeier, H.M., Whelan, A., Ewer, K., Goodchild, T., Clifton-Hadley, R., Williams, J. and Hewinson, R.G. (2006) The BOVIGAM® assay as ancillary test to the tuberculin skin test. Government Veterinary Journal. 16, pp. 72-80.
Wilkinson, D., Bennet, R., McFarlane, I., Rushton, S., Shirley, M. and Smith, G.C. (2009) Cost-benefit Analysis Model of Badger (Meles meles) Culling to Reduce Cattle Herd Tuberculosis Breakdowns in Britain, with Particular Reference to Badger Perturbation. Journal of Wildlife Diseases. 45 (4), pp. 1062-1088.
Wilson, G.J., Carter, S.P. and Delahay, R.J. (2011) Advances and Prospects For Management of Tb Transmission Between Badgers and Cattle. Veterinary Microbiology. 151 (1), pp. 43-50.
Woodroffe, R., Bourne, F.J., Cheeseman, C.L., Cox, D.R., Donnely, C.A., Gettinby, G., McInerney, J.P. and Morrison, W.I. (2005) Welfare of Badgers (Meles meles) Subjected to Culling: Patterns of Trap-related Injury. Animal Welfare. 14 (1), pp. 11-17.
Woodroffe, R., Donnelly, C.A., Wei, G., Cox, D.R., Bourne, F.J., Burke, T., Butlin, R.K., Cheeseman, C.L., Gettinby, G., Gilks, P., Hedges, S., Jenkins, H.E., Johnston, W.T., McInerney, J.P., Morrison, W.I. and Pope, L.C. (2009) Social Group Size Affects Mycobacterium Bovis Infection in European Badgers. Journal of Animal Ecology. 78 (4), pp. 818-827.
Woodroffe, R., Donnely, C.A., Cox, D.R., Bourne, F.J., Cheeseman, C.L., Delahay, R.J., Gettinby, G., McInerney, P. and Morrsion, I. (2006) Effects of Culling on Badger (Meles meles) Spatial Organization: Implications For the Control of Bovine Tuberculosis. Journal of Applied Ecology. 43 (1), pp. 1-10