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Climate change increases predation risk for a keystone species of the boreal forest

Abstract

Canada lynx (Lynx canadensis) and snowshoe hares (Lepus americanus) form a keystone predator–prey cycle that has large impacts on the North American boreal forest vertebrate community. Snowshoe hares and lynx are both well-suited for snowy winters, but climate change-associated shifts in snow conditions could lower hare survival and alter cyclic dynamics. Using detailed monitoring of snowshoe hare cause-specific mortality, behaviour and prevailing weather, we demonstrate that hare mortality risk is strongly influenced by variation in snow conditions. Although predation risk from lynx was largely unaffected by snow conditions, coyote (Canis latrans) predation increased in shallow snow. Maximum snow depth in our study area has decreased 33% over the last two decades and predictions based on prolonged shallow snow indicate that future hare survival could resemble that seen during population declines. Our results indicate that climate change could disrupt cyclic dynamics in the boreal forest.

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Fig. 1: Predicted effect of climate on monthly hare survival.
Fig. 2: Snow depth change over the last two decades.
Fig. 3: Relationship between cause-specific mortality and climate.
Fig. 4: Effect of climate on age-specific mortality risk and foraging behaviour.

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Data availability

Data available from the Dryad Digital Repository https://doi.org/10.5061/dryad.bzkh1896b.

Code availability

The R code used to analyse the data and produce figures is available in the Dryad Digital Repository https://doi.org/10.5061/dryad.bzkh1896b.

References

  1. Romero, G. Q. et al. Global predation pressure redistribution under future climate change. Nat. Clim. Change 8, 1087–1091 (2018).

    Article  Google Scholar 

  2. Ims, R. A. et al. Arctic greening and bird nest predation risk across tundra ecotones. Nat. Clim. Change 9, 607–610 (2019).

    Article  Google Scholar 

  3. Stenseth, N. et al. Snow conditions may create an invisible barrier for lynx. Proc. Natl Acad. Sci. USA 101, 10632–10634 (2004).

    Article  CAS  Google Scholar 

  4. Zimova, M., Mills, L. S. & Nowak, J. J. High fitness costs of climate change induced camouflage mismatch in a seasonally colour moulting mammal. Ecol. Lett. 19, 299–307 (2016).

    Article  Google Scholar 

  5. Post, E., Peterson, R. O., Stenseth, N. C. & McLaren, B. E. Ecosystem consequences of wolf behavioural response to climate. Nature 401, 905–907 (1999).

    Article  CAS  Google Scholar 

  6. Iles, D. T., Rockwell, R. F. & Koons, D. N. Shifting vital rate correlations alter predicted population responses to increasingly variable environments. Am. Nat. 193, E57–E64 (2019).

    Article  Google Scholar 

  7. Fisher, J. T. & Burton, A. C. Wildlife winners and losers in an oil sands landscape. Front. Ecol. Environ. 16, 323–328 (2018).

    Article  Google Scholar 

  8. Myers, J. H. Population cycles: generalities, exceptions and remaining mysteries. Proc. R. Soc. B 285, 20172841 (2018).

    Article  Google Scholar 

  9. Boutin, S. et al. Population changes of the vertebrate community during a snowshoe hare cycle in Canada’s boreal forest. Oikos 74, 69–80 (1995).

    Article  Google Scholar 

  10. Murray, D. L. & Boutin, S. The influence of snow on lynx and coyote movements: does morphology affect behavior? Oecologia 88, 463–469 (1991).

    Article  Google Scholar 

  11. Penczykowski, R. M., Connolly, B. M. & Barton, B. T. Winter is changing: trophic interactions under altered snow regimes. Food Webs 13, 80–91 (2017).

    Article  Google Scholar 

  12. Cornulier, T. et al. Europe-wide dampening of population cycles in keystone herbivores. Science 340, 63–66 (2013).

    Article  CAS  Google Scholar 

  13. Kausrud, K. L. et al. Linking climate change to lemming cycles. Nature 456, 93–97 (2008).

    Article  CAS  Google Scholar 

  14. Ims, R. A., Henden, J.-A. & Killengreen, S. T. Collapsing population cycles. Trends Ecol. Evol. 23, 79–86 (2008).

    Article  Google Scholar 

  15. Hodges, K. et al. in Ecosystem Dynamics of the Boreal Forest (eds Krebs, C. et al.) 141–178 (Oxford Univ. Press, 2001).

  16. Oli, M. K. et al. Demography of snowshoe hare population cycles. Ecology 101, e02969 (2020).

    Article  Google Scholar 

  17. Peacock, S. Projected twenty-first-century changes in temperature, precipitation, and snow cover over North America in CCSM4. J. Clim. 25, 4405–4429 (2012).

    Article  Google Scholar 

  18. Krebs, C. J. et al. What factors determine cyclic amplitude in the snowshoe hare (Lepus americanus) cycle? Can. J. Zool. 92, 1039–1048 (2014).

    Article  Google Scholar 

  19. Yan, C., Stenseth, N. C., Krebs, C. J. & Zhang, Z. Linking climate change to population cycles of hares and lynx. Glob. Change Biol. 19, 3263–3271 (2013).

    Google Scholar 

  20. Studd, E. K. et al. Use of acceleration and acoustics to classify behavior, generate time budgets, and evaluate responses to moonlight in free-ranging snowshoe hares. Front. Ecol. Evol. 7, e154 (2019).

    Article  Google Scholar 

  21. Mills, L. et al. Camouflage mismatch in seasonal coat color due to decreased snow duration. Proc. Natl Acad. Sci. USA 110, 7360–7365 (2013).

    Article  CAS  Google Scholar 

  22. Wilson, E. C., Shipley, A. A., Zuckerberg, B., Peery, M. Z. & Pauli, J. N. An experimental translocation identifies habitat features that buffer camouflage mismatch in snowshoe hares. Conserv. Lett. 12, e12614 (2019).

    Article  Google Scholar 

  23. Guillaumet, A., Bowman, J., Thornton, D. & Murray, D. L. The influence of coyote on Canada lynx populations assessed at two different spatial scales. Community Ecol. 16, 135–146 (2015).

    Article  Google Scholar 

  24. Peers, M. J. L., Thornton, D. H. & Murray, D. L. Reconsidering the specialist–generalist paradigm in niche breadth dynamics: resource gradient selection by Canada lynx and bobcat. PLoS ONE 7, e51488 (2012).

    Article  CAS  Google Scholar 

  25. Bowler, B., Krebs, C., O’Donoghue, M. & Hone, J. Climatic amplification of the numerical response of a predator population to its prey. Ecology 95, 1153–1161 (2014).

    Article  Google Scholar 

  26. Krebs, C. J., Boutin, S. & Boonstra, R. (eds) Ecosystem Dynamics of the Boreal Forest (Oxford Univ. Press, 2001).

  27. O’Donoghue, M., Boutin, S., Krebs, C. & Hofer, E. Numerical responses of coyotes and lynx to the snowshoe hare cycle. Oikos 80, 150–162 (1997).

    Article  Google Scholar 

  28. Hodges, K. in Ecology and Conservation of Lynx in the United States (eds Ruggiero, L. F. et al.) 117–161 (Univ. Press of Colorado, 2000).

  29. Brown, R. D. & Mote, P. W. The response of Northern Hemisphere snow cover to a changing climate. J. Clim. 22, 2124–2145 (2009).

    Article  Google Scholar 

  30. Korpela, K. et al. Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles. Glob. Change Biol. 19, 697–710 (2013).

    Article  Google Scholar 

  31. Kielland, K., Olson, K. & Euskirchen, E. Demography of snowshoe hares in relation to regional climate variability during a 10-year population cycle in interior Alaska. Can. J. Res. 40, 1265–1272 (2010).

    Article  Google Scholar 

  32. Humphries, M. M., Studd, E. K., Menzies, A. K. & Boutin, S. To everything there is a season: summer-to-winter food webs and the functional traits of keystone species. Integr. Comp. Biol. 57, 961–976 (2017).

    Article  Google Scholar 

  33. Peers, M. J. L. et al. Prey availability and ambient temperature influence carrion persistence in the boreal forest. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13275 (2020).

  34. Krebs, C. J., Boonstra, R. & Boutin, S. Using experimentation to understand the 10-year snowshoe hare cycle in the boreal forest of North America. J. Anim. Ecol. 87, 87–100 (2018).

    Article  Google Scholar 

  35. Krebs, C. J. et al. The Community Ecological Monitoring Program Annual Data Report (Univ. of British Columbia, 2018).

  36. Zeileis, A., Grothendieck, G., Ryan, J., Ulrich, J. & Andrews, F. zoo: S3 infrastructure for regular and irregular time series (Z’s ordered observations). R package version 1.8-8 (2019).

  37. Fieberg, J. & Delgiudice, G. D. What time is it? Choice of time origin and scale in extended proportional hazards models. Ecology 90, 1687–1697 (2009).

    Article  Google Scholar 

  38. Murray, D. L. et al. Death from anthropogenic causes is partially compensatory in recovering wolf populations. Biol. Conserv. 143, 2514–2524 (2010).

    Article  Google Scholar 

  39. Murray, D. & Bastille-Rousseau, G. in Population Ecology in Practice (eds Murray, D. L. & Sandercock, B.) 123–156 (Wiley-Blackwell, 2020).

  40. Burnham, K. & Anderson, D. Model Selection and Multimodel Inference (Springer, 2002).

  41. Graham, M. H. Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815 (2003).

    Article  Google Scholar 

  42. McLellan, B. N. Some mechanisms underlying variation in vital rates of grizzly bears on a multiple use landscape. J. Wildl. Manag. 79, 749–765 (2015).

    Article  Google Scholar 

  43. Lunn, M. & McNeil, D. Applying Cox regression to competing risks. Biometrics 51, 524–532 (1995).

    Article  CAS  Google Scholar 

  44. Bastille-Rousseau, G. et al. Phase-dependent climate–predator interactions explain three decades of variation in neonatal caribou survival. J. Anim. Ecol. 85, 445–456 (2016).

    Article  Google Scholar 

  45. Murray, D. L., Bastille-Rousseau, G., Hornseth, M., Row, J. & Thornton, D. H. in Population Ecology in Practice (eds Murray, D. L. & Sandercock, B.) 17–46 (Wiley-Blackwell, 2020).

  46. Hodges, K. E., Krebs, C. J. & Sinclair, A. R. E. Snowshoe hare demography during a cyclic population low. J. Anim. Ecol. 68, 581–594 (1999).

    Article  Google Scholar 

  47. Boutin, S., Gilbert, B. S., Krebs, C. J., Sinclair, A. R. E. & Smith, J. N. M. The role of dispersal in the population dynamics of snowshoe hares. Can. J. Zool. 63, 106–115 (1984).

    Article  Google Scholar 

  48. Gillis, E. A. Survival of juvenile hares during a cyclic population increase. Can. J. Zool. 76, 1949–1956 (1998).

    Article  Google Scholar 

  49. Graf, P. M., Wilson, R. P., Qasem, L., Hackländer, K. & Rosell, F. The use of acceleration to code for animal behaviours; a case study in free-ranging Eurasian beavers Castor fiber. PLoS ONE 10, 1–17 (2015).

    Google Scholar 

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Acknowledgements

We thank the numerous field technicians who monitored hare survival and snow conditions throughout the study, as well as members of the Boutin Lab for comments on earlier versions of this manuscript. We also thank A. MacDonald and her family for long-term access to her trapline. We thank the Champagne and Aishihik, and Kluane First Nations, for supporting our work within their traditional territory. This work was supported by the Natural Sciences and Engineering Research Council of Canada, Northern Studies Training Programme, the University of Alberta Northern Research Award programme, the Association of Canadian Universities for Northern Studies, the Wildlife Conservation Society Canada, the W. Garfield Weston Foundation, the Killam Laureates programme, Government of Yukon and Earth Rangers.

Author information

Authors and Affiliations

Authors

Contributions

M.J.L.P. and S.B. designed the study. M.J.L.P., Y.N.M., A.K.M. and E.K.S. led data collection. Primary logistic support was provided by S.B. with assistance by M.H., T.S.J., A.J.K., C.J.K., D.L.M. and R.B. M.J.L.P. and G.B-R. performed the analysis. M.J.L.P. drafted the manuscript with input from all authors.

Corresponding author

Correspondence to Michael J. L. Peers.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Magnus Magnusson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Snowshoe hare density in our study region.

Spring snowshoe hare density (± 95% Confidence Intervals) in the Kluane Lake region, Yukon over the last cycle. Hare density estimates are determined through mark-recapture as part of the Community Ecological Monitoring Project (CEMP; https://www.zoology.ubc.ca/~krebs/kluane.html), and densities displayed here come from trapping area 2 (blue) in the study area map (Supplementary Fig. 1). Shaded area represents the years where we monitored detailed survival and weather data throughout the entire winter (that is Dec-Mar).

Extended Data Fig. 2 Over-winter survival of snowshoe hares.

Kaplan-Meier four-month survival curves (± 95% Confidence Intervals) for snowshoe hares in the Kluane Lake region, Yukon, across the three winters in which we monitored survival from December until March.

Extended Data Fig. 3 Relationship between snow depth and mortality risk.

Modelled effect of snow depth (cm) on mortality risk in snowshoe hares. Mortality risk is based on coefficients from the best supported Cox-proportional hazards model, and shaded areas represent predicted response standard errors. The dotted line represents baseline risk for hares.

Extended Data Fig. 4 Snow conditions at snowshoe hare kill sites.

Difference in a) snow depth (cm), and b) sinking depth of the penetrometer (cm) at kill site locations for each predator species compared to the daily snow measurements taken on the date of the mortality.

Extended Data Fig 5 Over-winter survival between age classes.

Kaplan-Meier four-month survival curves (± 95% Confidence Intervals) for sub-adult (red) and adult (blue) snowshoe hares during the winter of a) 2015–16, b) 2016–17, c) 2017–18, and d) all years combined.

Extended Data Fig 6 Effect of snow conditions on age-specific mortality risk and foraging behaviour.

Modelled effect of the sinking depth of the penetrometer (cm) on mortality risk and daily foraging time for sub-adult (a, b) and adult (c, d) snowshoe hare at two different snow depths. Shaded areas represent predicted response standard errors and the dotted line represents baseline mortality risk (a, c) or the average time spent foraging per day in hours across the winter for sub-adults (b) and adults (d).

Extended Data Fig 7 Predator density in our study region.

Canada lynx (blue, solid) and coyote (red, dashed) density in the Kluane lake region, Yukon, for each winter over the last snowshoe hare cycle. Densities in the region are determined each year based on track transects as part of the Community Ecological Monitoring Program (CEMP; https://www.zoology.ubc.ca/~krebs/kluane.html), where tracks are counted along a 25-km transect that traversed our study area, on days after fresh snowfalls while tracks were distinguishable (see Krebs et al. 26). Shaded area represents the years where we monitored detailed hare survival and weather data throughout the winter (that is Dec-Mar).

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Peers, M.J.L., Majchrzak, Y.N., Menzies, A.K. et al. Climate change increases predation risk for a keystone species of the boreal forest. Nat. Clim. Chang. 10, 1149–1153 (2020). https://doi.org/10.1038/s41558-020-00908-4

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