Management of large carnivores is among the most controversial topics in natural resource administration. Regulated hunting is a centrepiece of many carnivore management programmes and, although a number of hunting effects on population dynamics, body-size distributions and life history in other wildlife have been observed, its effects on life history and demography of large carnivores remain poorly documented. We report results from a 30-year study of brown bears (Ursus arctos) analysed using an integrated hierarchical approach. Our study revealed that regulated hunting has severely disrupted the interplay between age-specific survival and environmental factors, altered the consequences of reproductive strategies, and changed reproductive values and life expectancy in a population of the world’s largest terrestrial carnivore. Protection and sustainable management have led to numerical recovery of several populations of large carnivores, but managers and policymakers should be aware of the extent to which regulated hunting may be influencing vital rates, thereby reshaping the life history of apex predators.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Steffen, W., Crutzen, P. J. & McNeill, J. R. The Anthropocene: are humans now overwhelming the great forces of nature. Ambio 36, 614–621 (2007).

  2. 2.

    Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).

  3. 3.

    Ripple, W. J. et al. Status and ecological effects of the world’s largest carnivores. Science 343, 1241484 (2014).

  4. 4.

    Ray, J. C., Redford, K. H., Steneck, R. & Berger, J. Large Carnivores and the Conservation of Biodiversity (Island, Washington, 2005).

  5. 5.

    Barthold, J. A., Loveridge, A. J., Macdonald, D. W., Packer, C. & Colchero, F. Bayesian estimates of male and female African lion mortality for future use in population management. J. Appl. Ecol. 53, 295–304 (2016).

  6. 6.

    Karanth, K. U. et al. Counting India’s wild tigers reliably. Science 332, 791–791 (2011).

  7. 7.

    Mattson, D. J. & Merrill, T. Extirpations of grizzly bears in the contiguous United States, 1850–2000. Conserv. Biol. 16, 1123–1136 (2002).

  8. 8.

    Breitenmoser, U. Large predators in the Alps: the fall and rise of man’s competitors. Biol. Conserv. 83, 279–289 (1998).

  9. 9.

    Swenson, J. E. et al. The near extinction and recovery of brown bears in Scandinavia in relation to the bear management policies of Norway and Sweden. Wildlife Biol. 1, 11–25 (1995).

  10. 10.

    Chapron, G. et al. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346, 1517–1519 (2014).

  11. 11.

    Swenson, J. E. et al. Challenges of managing a European brown bear population; lessons from Sweden, 1943–2013. Wildlife Biol. https://doi.org/10.2981/wlb.00251 (2017).

  12. 12.

    Milleret, C. et al. Let’s stay together? Intrinsic and extrinsic factors involved in pair bond dissolution in a recolonizing wolf population. J. Anim. Ecol. 86, 43–54 (2017).

  13. 13.

    Coulson, T. et al. Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292, 1528–1531 (2001).

  14. 14.

    Kuijper, D. P. J. et al. Paws without claws? Ecological effects of large carnivores in anthropogenic landscapes. Proc. R. Soc. B 283, 20161625 (2016).

  15. 15.

    Coulson, T. et al. Modeling effects of environmental change on wolf population dynamics, trait evolution, and life history. Science 334, 1275–1278 (2011).

  16. 16.

    Smith, J. E., Lehmann, K. D. S., Montgomery, T. M., Strauss, E. D. & Holekamp, K. E. Insights from long‐term field studies of mammalian carnivores. J. Mammal. 98, 631–641 (2017).

  17. 17.

    Wielgus, R. B., Morrison, D. E., Cooley, H. S. & Maletzke, B. Effects of male trophy hunting on female carnivore population growth and persistence. Biol. Conserv. 167, 69–75 (2013).

  18. 18.

    Garel, M. et al. Selective harvesting and habitat loss produce long-term life history changes in a mouflon population. Ecol. Appl. 17, 1607–1618 (2007).

  19. 19.

    Coltman, D. W. et al. Undesirable evolutionary consequences of trophy hunting. Nature 426, 655–658 (2003).

  20. 20.

    Coulson, T., Guinness, F., Pemberton, J. & Clutton-Brock, T. The demographic consequences of releasing a population of red deer from culling. Ecology 85, 411–422 (2004).

  21. 21.

    Traill, L. W., Schindler, S. & Coulson, T. Demography, not inheritance, drives phenotypic change in hunted bighorn sheep. Proc. Natl Acad. Sci. USA 111, 13223–13228 (2014).

  22. 22.

    Schindler, S., Festa-Bianchet, M., Hogg, J. T. & Pelletier, F. Hunting, age structure, and horn size distribution in bighorn sheep. J. Wildlife Manage. 81, 792–799 (2017).

  23. 23.

    Swenson, J. E., Dahle, B. & Sandegren, F. Intraspecific predation in Scandinavian brown bears older than cubs-of-the-year. Ursus 12, 81–92 (2001).

  24. 24.

    Amstrup, S. C., Stirling, I., Smith, T. S., Perham, C. & Thiemann, G. W. Recent observations of intraspecific predation and cannibalism among polar bears in the southern Beaufort Sea. Polar Biol. 29, 997 (2006).

  25. 25.

    Galentine, S. P. & Swift, P. K. Intraspecific killing among mountain lions (Puma concolor). Southwest. Natural. 52, 161–164 (2007).

  26. 26.

    Bischof, R. et al. Implementation uncertainty when using recreational hunting to manage carnivores. J. Appl. Ecol. 49, 824–832 (2012).

  27. 27.

    Chapron, G. & Treves, A. Blood does not buy goodwill: allowing culling increases poaching of a large carnivore. Proc. R. Soc. B 283, 20152939 (2016).

  28. 28.

    Bischof, R., Swenson, J. E., Yoccoz, N. G., Mysterud, A. & Gimenez, O. The magnitude and selectivity of natural and multiple anthropogenic mortality causes in hunted brown bears. J. Anim. Ecol. 78, 656–665 (2009).

  29. 29.

    Swenson, J. E. et al. Infanticide caused by hunting of male bears. Nature 386, 450–451 (1997).

  30. 30.

    Promislow, D. E. L. & Harvey, P. H. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. 220, 417–437 (1990).

  31. 31.

    Milner, J. M., Nilsen, E. B. & Reassen, H. P. Demographic side effects of selective hunting in ungulates and carnivores. Conserv. Biol. 21, 36–47 (2007).

  32. 32.

    Treves, A. Hunting for large carnivore conservation. J. Appl. Ecol. 46, 1350–1356 (2009).

  33. 33.

    Packer, C. et al. Ecological change, group territoriality, and population dynamics in Serengeti lions. Science 307, 390–393 (2005).

  34. 34.

    Sahlén, V., Friebe, A., Sæbø, S., Swenson, J. E. & Støen, O.-G. Den entry behavior in Scandinavian brown bears: implications for preventing human injuries. J. Wildlife Manage. 79, 274–287 (2015).

  35. 35.

    Manchi, S. & Swenson, J. E. Denning behaviour of Scandinavian brown bears Ursus arctos. Wildlife Biol. 11, 123–132 (2005).

  36. 36.

    Bieber, C., Lebl, K., Stalder, G., Geiser, F. & Ruf, T. Body mass dependent use of hibernation: why not prolong the active season, if they can? Funct. Ecol. 28, 167–177 (2014).

  37. 37.

    Friebe, A. et al. Factors affecting date of implantation, parturition, and den entry estimated from activity and body temperature in free-ranging brown bears. PLoS ONE 9, 0101410 (2014).

  38. 38.

    Sahlén, E., Støen, O.-G. & Swenson, J. E. Brown bear den site concealment in relation to human activity in Sweden. Ursus 22, 152–158 (2011).

  39. 39.

    Elfström, M., Swenson, J. E. & Ball, J. P. Selection of denning habitats by Scandinavian brown bears Ursus arctos. Wildlife Biol. 14, 176–187 (2008).

  40. 40.

    Goldstein, M. I., Poe, A. J., Suring, L. H., Nielson, R. M. & McDonald, T. L. Brown bear den habitat and winter recreation in south-central Alaska. J. Wildlife Manage. 74, 35–42 (2010).

  41. 41.

    IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) (Cambridge Univ. Press, Cambridge, 2014).

  42. 42.

    Knight, R. R. & Eberhardt, L. L. Population dynamics of Yellowstone grizzly bears. Ecology 66, 323–334 (1985).

  43. 43.

    Zedrosser, A., Steyaert, S. M. J. G., Gossow, H. & Swenson, J. E. Brown bear conservation and the ghost of persecution past. Biol. Conserv. 144, 2163–2170 (2011).

  44. 44.

    Miller, S. D., McLellan, B. N. & Derocher, A. E. Conservation and management of large carnivores in North America. Int. J. Environ. Stud. 70, 383–398 (2013).

  45. 45.

    Ordiz, A., Bischof, R. & Swenson, J. E. Saving large carnivores, but losing the apex predator? Biol. Conserv. 168, 128–133 (2013).

  46. 46.

    Zedrosser, A., Dahle, B. & Swenson, J. E. Population density and food conditions determine adult female body size in brown bears. J. Mammal. 87, 510–518 (2006).

  47. 47.

    Moen, A. Nasjonalatlas for Norge: Vegetasjon (Statens Kartverk, Hønefoss, 1998).

  48. 48.

    Lundqvist, R. Fulufjället. Nationalpark i Dalafjällen (Naturvårdsverket, Stockholm, 2002).

  49. 49.

    Martin, J. et al. Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos). Canadian J. Zool. 88, 875–883 (2010).

  50. 50.

    Arnemo, J. M., Evans, A. & Fahlman, Å. Biomedical Protocols for Free-Ranging Brown Bears, Wolves, Wolverines and Lynx (Norwegian Directorate for Nature Management, Trondheim, 2011).

  51. 51.

    Steyaert, S. M. J. G., Swenson, J. E., Kindberg, J., Brunberg, S. & Zedrosser, A. Male reproductive strategy explains spatiotemporal segregation in brown bears. J. Anim. Ecol. 82, 836–845 (2013).

  52. 52.

    Matson, G. M. et al. A Laboratory Manual for Cementum Age Determination of Alaskan Brown Bear First Premolar Teeth (Matson’s Laboratory, Manhattan, 1993).

  53. 53.

    Bischof, R., Zedrosser, A., Brunberg, S. & Swenson, J. E. A note on opportunism and parsimony in data collection. J. Wildlife Manage. 73, 10–21 (2009).

  54. 54.

    Zedrosser, A., Bellemain, E., Taberlet, P. & Swenson, J. E. Genetic estimates of annual reproductive success in male brown bears: the effects of body size, age, internal relatedness and population density. J. Anim. Ecol. 76, 368–375 (2007).

  55. 55.

    Finley, A. O. & Banerjee, S. MBA: Multilevel B-Spline Approximation. R package version 0.0-8 (R Foundation for Statistical Computing, Vienna, 2014).

  56. 56.

    Rixen, C., Dawes, M. A., Wipf, S. & Hagedorn, F. Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming. Oikos 121, 1532–1543 (2012).

  57. 57.

    Kindberg, J., Ericsson, G. & Swenson, J. E. Monitoring rare or elusive large mammals using effort-corrected voluntary observers. Biol. Conserv. 142, 159–165 (2009).

  58. 58.

    Dahle, B. & Swenson, J. E. Home ranges in adult Scandinavian brown bears (Ursus arctos): effect of mass, sex, reproductive category, population density and habitat type. J. Zool. 260, 329–335 (2003).

  59. 59.

    Zedrosser, A., Pelletier, F., Bischof, R., Festa-Bianchet, M. & Swenson, J. E. Determinants of lifetime reproduction in female brown bears: early body mass, longevity, and hunting regulations. Ecology 94, 231–240 (2013).

  60. 60.

    Kuo, L. & Mallick, B. Variable selection for regression models. Indian J. Stat. B 60, 65–81 (1998).

  61. 61.

    O’Hara, R. B. & Sillanpaa, M. J. A review of Bayesian variable selection methods: what, how and which. Bayesian Anal. 4, 85–117 (2009).

  62. 62.

    Kéry, M. & Schaub, M. Bayesian Population Analysis Using WinBUGS: A Hierarchical Perspective (Academic, Waltham, 2012).

  63. 63.

    Liberg, O. et al. Shoot, shovel and shut up: cryptic poaching slows restoration of a large carnivore in Europe. Proc. R. Soc. B 279, 910–915 (2011).

  64. 64.

    Treves, A., Artelle, K. A., Darimont, C. T. & Parsons, D. R. Mismeasured mortality: correcting estimates of wolf poaching in the United States. J. Mammal. 98, 1256–1264 (2017).

  65. 65.

    Plummer, M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In Proc. 3rd International Workshop on Distributed Statistical Computing (DSC2003) Article 1 (Technische Universität Wien, Vienna, 2003).

  66. 66.

    Su, Y. & Yajima, M. R2jags: Using R to Run 'JAGS'. R package version 0.5-7 (R Foundation for Statistical Computing, Vienna, 2015).

  67. 67.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2017). 

  68. 68.

    Gelman, A. in Markov Chain Monte Carlo in Practice (eds Gilks, W. R., Richardson, S. & Spiegelhalter, D. J.) 131–143 (Chapman and Hall, New York, 1996).

  69. 69.

    Caswell, H. Matrix Population Models: Construction, Analysis, and Interpretation (Sinauer Associates, Sunderland, 2001).

  70. 70.

    Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 23 (2007).

  71. 71.

    Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).

Download references


We are grateful for the support of the Center for Advanced Study in Oslo, Norway, that funded and hosted our research project ‘Climate effects on harvested large mammal populations’ during the academic year of 2015–2016. R.B. and J.S. received additional funding from the Polish-Norwegian Research Program (GLOBE No POL-NOR/198352/85/2013). This research was supported in part by the computing cluster of the Pôle Bioinformatique Lyonnais. We thank S. Frank and A. Hertel for preparation of select environmental data, A. Ordiz, J. Kindberg, and V. Vazquez for constructive comments on the manuscript, and the Swedish Association for Hunting and Wildlife Management for the Large Carnivore Observation Index (LCOI), which was used to derive the density index. This is scientific paper 244 of the Scandinavian Brown Bear Research Project.

Author information


  1. Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway

    • Richard Bischof
    • , Andrea Friebe
    •  & Jon E. Swenson
  2. Université de Lyon, F-69000, CNRS, UMR, 5558, Laboratoire de Biométrie et Biologie Évolutive, Villeurbanne, France

    • Christophe Bonenfant
  3. Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo, Norway

    • Inger Maren Rivrud
    •  & Atle Mysterud
  4. Department of Natural Sciences and Environmental Health, University College of Southeast Norway, Bø, Norway

    • Andreas Zedrosser
  5. Institute of Wildlife Biology and Game Management, University of Natural Resources and Life Sciences, Vienna, Austria

    • Andreas Zedrosser
  6. Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK

    • Tim Coulson
  7. Norwegian Institute for Nature Research, Trondheim, Norway

    • Jon E. Swenson


  1. Search for Richard Bischof in:

  2. Search for Christophe Bonenfant in:

  3. Search for Inger Maren Rivrud in:

  4. Search for Andreas Zedrosser in:

  5. Search for Andrea Friebe in:

  6. Search for Tim Coulson in:

  7. Search for Atle Mysterud in:

  8. Search for Jon E. Swenson in:


R.B. and C.B. conceived the study with J.E.S., A.M. and T.C. J.E.S., A.Z. and A.F. coordinated collection and compilation of field data. R.B., I.M.R. and A.Z. extracted and formatted intrinsic and extrinsic covariates. R.B. and C.B. developed, implemented and analysed the model. R.B. wrote the first draft of the paper; all authors contributed to subsequent versions.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Richard Bischof.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–3, Supplementary Tables 1–9; Supplementary reference; description of Supplementary data files

  2. Life Sciences Reporting Summary

  3. Supplementary Data Set 1

    Data for Figure 1

  4. Supplementary Data Set 2

    Data for Figure 3

  5. Supplementary Data Set 3

    Data for Figure 4

  6. Supplementary Data Set 4

    Multistate model for JAGS

  7. Supplementary Data Set 5

    Data for Supplementary Figure 2

  8. Supplementary Data Set 6

    Data for Supplementary Figure 3

About this article

Publication history