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Research Article

Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis

Jon Bielby, Christl A. Donnelly, Lisa C. Pope, Terry Burke, and Rosie Woodroffe
  1. aInstitute of Zoology, Regent’s Park, London NW1 4RY, United Kingdom;
  2. bMedical Research Council Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Imperial College London, London W2 1PG, United Kingdom; and
  3. cDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom

See allHide authors and affiliations

PNAS June 24, 2014 111 (25) 9193-9198; first published June 9, 2014; https://doi.org/10.1073/pnas.1401503111
Jon Bielby
aInstitute of Zoology, Regent’s Park, London NW1 4RY, United Kingdom;
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Christl A. Donnelly
bMedical Research Council Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Imperial College London, London W2 1PG, United Kingdom; and
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Lisa C. Pope
cDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom
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Terry Burke
cDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom
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Rosie Woodroffe
aInstitute of Zoology, Regent’s Park, London NW1 4RY, United Kingdom;
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  • For correspondence: rosie.woodroffe@ioz.ac.uk
  1. Edited* by Robert M. May, University of Oxford, Oxford, United Kingdom, and approved April 24, 2014 (received for review January 28, 2014)

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Significance

Bovine tuberculosis (TB) killed 1,500 people annually in 1930s Britain. TB control efforts still entail slaughtering many thousands of cattle annually, costing British farmers and taxpayers millions of dollars. Transmission from wild badgers impedes control of cattle TB, but nonselective badger culls confer limited benefits because culling changes badger behavior in ways that increase disease spread. A new plan to cull only test-positive badgers, and vaccinate test-negative badgers [termed test–vaccinate/remove (TVR)], is probably more publicly acceptable, and might be more effective if culling small numbers of badgers prompts no behavioral change. Unfortunately, this study shows that small-scale culling (such as TVR) changes badgers’ behavior in ways that risk increasing TB transmission among badgers and exacerbating cattle TB incidence rather than reducing it.

Abstract

Where wildlife disease requires management, culling is frequently considered but not always effective. In the British Isles, control of cattle tuberculosis (TB) is hindered by infection in wild badger (Meles meles) populations. Large-scale badger culling can reduce the incidence of confirmed cattle TB, but these benefits are undermined by culling-induced changes in badger behavior (termed perturbation), which can increase transmission among badgers and from badgers to cattle. Test–vaccinate/remove (TVR) is a novel approach that entails testing individual badgers for infection, vaccinating test-negative animals, and killing test-positive animals. Imperfect capture success, diagnostic sensitivity, and vaccine effectiveness mean that TVR would be expected to leave some infected and some susceptible badgers in the population. Existing simulation models predict that TVR could reduce cattle TB if such small-scale culling causes no perturbation, but could increase cattle TB if considerable perturbation occurs. Using data from a long-term study, we show that past small-scale culling was significantly associated with four metrics of perturbation in badgers: expanded ranging, more frequent immigration, lower genetic relatedness, and elevated prevalence of Mycobacterium bovis, the causative agent of TB. Though we could not reject the hypothesis that culling up to three badgers per social group might avoid perturbation, we also could not reject the hypothesis that killing a single badger prompted detectable perturbation. When considered alongside existing model predictions, our findings suggest that implementation of TVR, scheduled for 2014, risks exacerbating the TB problem rather than controlling it. Ongoing illegal badger culling is likewise expected to increase cattle TB risks.

  • zoonotic disease
  • epidemiology
  • Bacillus Calmette-Guérin
  • wildlife management

Footnotes

  • ↵1Present address: The School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia.

  • ↵2To whom correspondence should be addressed. E-mail: rosie.woodroffe{at}ioz.ac.uk.
  • Author contributions: J.B., C.A.D., and R.W. designed research; J.B., C.A.D., and R.W. performed research; L.C.P. and T.B. contributed new reagents/analytic tools; L.C.P. and T.B. contributed data; J.B., C.A.D., and R.W. analyzed data; and J.B., C.A.D., L.C.P., T.B., and R.W. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1401503111/-/DCSupplemental.

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Small-scale badger culling for TB control
Jon Bielby, Christl A. Donnelly, Lisa C. Pope, Terry Burke, Rosie Woodroffe
Proceedings of the National Academy of Sciences Jun 2014, 111 (25) 9193-9198; DOI: 10.1073/pnas.1401503111

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Small-scale badger culling for TB control
Jon Bielby, Christl A. Donnelly, Lisa C. Pope, Terry Burke, Rosie Woodroffe
Proceedings of the National Academy of Sciences Jun 2014, 111 (25) 9193-9198; DOI: 10.1073/pnas.1401503111
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Proceedings of the National Academy of Sciences: 111 (25)
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