Wolverine behavior varies spatially with anthropogenic footprint: implications for conservation and inferences about declines

Abstract

Understanding a species’ behavioral response to rapid environmental change is an ongoing challenge in modern conservation. Anthropogenic landscape modification, or “human footprint,” is well documented as a central cause of large mammal decline and range contractions where the proximal mechanisms of decline are often contentious. Direct mortality is an obvious cause; alternatively, human-modified landscapes perceived as unsuitable by some species may contribute to shifts in space use through preferential habitat selection. A useful approach to tease these effects apart is to determine whether behaviors potentially associated with risk vary with human footprint. We hypothesized wolverine (Gulo gulo) behaviors vary with different degrees of human footprint. We quantified metrics of behavior, which we assumed to indicate risk perception, from photographic images from a large existing camera-trapping dataset collected to understand wolverine distribution in the Rocky Mountains of Alberta, Canada. We systematically deployed 164 camera sites across three study areas covering approximately 24,000 km², sampled monthly between December and April (2007–2013). Wolverine behavior varied markedly across the study areas. Variation in behavior decreased with increasing human footprint. Increasing human footprint may constrain potential variation in behavior, through either restricting behavioral plasticity or individual variation in areas of high human impact. We hypothesize that behavioral constraints may indicate an increase in perceived risk in human-modified landscapes. Although survival is obviously a key contributor to species population decline and range loss, behavior may also make a significant contribution.

References Abrams, P. A. 2000. The impact of habitat selection on the spatial heterogeneity of resources in varying environments. Ecology 81:2902–2913. Amarasekare, P. 2003. Competitive coexistence in spatially structured environments: a synthesis. Ecol. Lett. 6:1109–1122. Baker, M. A., and J. Brown. 2010. Islands of fear: effects of wooded patches on habitat suitability of the striped mouse in a South African grassland. Funct. Ecol. 24:1313–1322. Banci, V. A. 1994. Wolverine  . pp. 29–127 in L. F. Ruggiero, K. B. Aubry, S. W. Buskirk, L. J. Lyon and W. J. Zielinski, edS. Ministry of environment, lands and parks, chapter 5 (Holbrow 1976). USDA Forest Service Rocky Mountain Forest and Range Experiment Station. Fort Collins, Colorado, USA. Bates, D. M. and J. M. Chambers. 1992. Nonlinear Models. Pp. 421–453 in J. M. Chambers, and T.J. Hastie, eds. Statistical Models In S. CRC Press, Boca Raton, Florida. Béchet, A., J. F. Giroux, and G. Gauthier. 2004. The effects of disturbance on behaviour, habitat use and energy of spring staging snow geese. J. Appl. Ecol. 41:689–700. Brodie, J. F., and E. Post. 2009. Nonlinear responses of wolverine populations to declining winter snowpack. Popul. Ecol. 52:279–287. Burnham, K. P., and D. R. Anderson. 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33:261–304. Burton, A. C., E. Neilsoń, D. Moreirá, A. Ladle, R. Steenweg, J. T. Fisher, et al. 2015. Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes. J. Appl. Ecol. 52:675–685. Butchart, S. H., M. Walpole, B. Collen, A. Van Strien, J. P. Scharlemann, R. E. Almond, et al. 2010. Global biodiversity: indicators of recent declines. Science 328:1164–1168. Caraco, T., S. Martindale, and H. R. Pulliam. 1980. Avian flocking in the presence of a predator. Nature 285:400–401. Caroll, C., R. F. Noss, P. C. Paquet, and N. H. Schumaker. 2004. Extinction debt of protected areas in developing landscapes. Conserv. Biol. 18:1110–1120. Childress, M. J., and M. A. Lung. 2003. Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics? Anim. Behav. 66:389–398. Ciuti, S., T. B. Muhly, D. G. Paton, A. D. McDevitt, M. Musiani, and M. S. Boyce. 2012a. Human selection of elk behavioural traits in a landscape of fear. Proc. Biol. Sci. 279:4407–4416. Ciuti, S., et al. 2012b. Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of fear. PLoS One 7:e50611. Clevenger, A., and M. Baruetto. 2014. Trans-Canada highway wildlife and monitoring research, final report. Part B: Research. Report to Parks Canada Agency, Radium Hot Springs, British Columbia, Canada. Copeland, J. P., K. S. McKelvey, K. B. Aubry, A. Landa, J. Persson, R. M. Inman, et al. 2010. The bioclimatic envelope of the wolverine (Gulo gulo): do climatic constraints limit its geographic distribution? Can. J. Zool. 88:233–246. COSEWIC. 2014. COSEWIC Annual Report. Presented to the Minister of Environment and the Canadian Endangered Species Conservation Council. Ottawa. 42 pp. Crawley, M. J. 2007. The R book. Wiley, Chichester, U.K. Cumming, G. S. 2007. Global biodiversity scenarios and landscape ecology. Landscape Ecol. 22:671–685. Dantzer, B., S. Boutin, M. M. Humpheries, and A. G. McAdam. 2012. Behavioral responses of territorial red squirrels to natural and experimental variation in population density. Behav. Ecol. Sociobiol. 66:865–878. Darimont, C. T., S. M. Carlson, M. T. Kinnison, P. C. Paquet, T. E. Reimchen, and C. C. Wilmers. 2009. Human predators outpace other agents of trait change in the wild. Proc. Natl Acad. Sci. USA 106:952–954. Fahrig, L. 1997. Relative effects of habitat loss and fragmentation on population extinction. J. Wildl. Manag. 61:603–610. Fahrig, L. 2001. How much habitat is enough? Biol. Conserv. 100:65–74. Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34:487–515. Fisher, J. T., and S. Bradbury. 2014. A multi-method hierarchical modeling approach to quantifying bias in occupancy from noninvasive genetic tagging studies. J. Wildl. Manag. 78:1087–1095. Fisher, J. T., B. Anholt, and J. Volpe. 2011. Body mass explains characteristic scales of habitat selection in terrestrial mammals. Ecol. Evol. 1:517–528. Fisher, J. T., S. Bradbury, B. Anholt, L. Nolan, L. Roy, J. P. Volpe, et al. 2013. Wolverines (Gulo gulo luscus) on the Rocky Mountain slopes: natural heterogeneity and landscape alteration as predictors of distribution. Can. J. Zool. 91:706–716. Ford, A. T., J. R. Goheen, T. O. Otieno, L. Bidner, L. A. Isbell, T. M. Palmer, et al. 2014. Large carnivores make savanna tree communities less thorny. Science 346:346–349. Fox, J., and S. Weisber. 2014. An R companion to applied regression, 2nd ed. Sage 2011, Thousand Oaks, California. R package version 2.0-25. Frid, A., and L. M. Dill. 2002. Human-caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 6:11. Heim, N. A. 2015. Complex effects of human-impacted landscapes on the spatial patterns of mammalian carnivores. M.Sc. thesis. University of Victoria. Heinemeyer, K., and J. R. Squires. 2013. Wolverine -The Winter Recreation Project: Investigating the interactions between wolverines and winter recreation. www.wolverinefoundation.org. Accessed November 15, 2014. Hollén, L. I., M. B. V. Bell, H. M. Wade, R. Rose, A. Russell, F. Niven, et al. 2011. Ecological conditions influence sentinel decisions. Anim. Behav. 82:1435–1441. Inman, R. M., A. J. Magoun, J. Persson, and J. Mattisson. 2012. The wolverine's niche: linking reproductive chronology, caching, competition, and climate. J. Mammal. 93:634–644. Komers, P. E. 1997. Behavioural plasticity in variable environments. Can. J. Zool. 75:161–169. Krebs, J. R. 1978. Optimal foraging: decision rules for predators. Pp. 23–63 in J. R. Krebs, N. B. Davies, eds. Behavioural ecology: an evolutionary approach. Blackwell, Oxford. Krebs, J. R., E. Lofroth, J. Copeland, V. Banci, D. Cooley, H. Golden, et al. 2004. Synthesis of survival rates and causes of mortality in North American wolverines. J. Wildl. Manag. 68:493–502. Krebs, J. R., E. C. Lofroth, and I. A. N. Parfitt. 2007. Multiscale habitat use by wolverines in British Columbia, Canada. J. Wildl. Manag. 71:2180. Laliberte, A. S., and W. J. Ripple. 2004. Range contractions of North American carnivores and ungluates. Bioscience 54:123–128. Laundre, H., L. Hernández, P. L. Medina, A. Campanella, J. López-Portillo, A. González-Romero, et al. 2014. The landscape of fear: the missing link to understand top-down and bottom-up control of prey abundance? Ecology 95:1141–1152. Laundré, J. W., L. Hernández, and W. J. Ripple. 2010. The landscape of fear: ecological implications of being afraid. Open Ecol. J. 3:1–7. Levene, H. 1960. Robust tests for equality of variances. Pp. 278–292 in I. Olkin, ed. Contributions to probability and statistics: essays in Honor of Harold Hoteling. Stanford Univ. Press, Stanford, CA. Lima, S. L., and P. A. Bednekoff. 2014. Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis. Am. Nat. 153:649–659. Lima, S. L., and L. M. Dill. 1990. Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68:619–640. Lima, S. L., and P. A. Zollner. 1996. Towards a behavioural ecology of ecological landscapes. Trends Ecol. Evol. 11:131–135. Lofroth, E. C., and P. K. Ott. 2007. Assessment of the sustainability of wolverine harvest in British Columbia, Canada. J. Wildl. Manag. 71:2193. Long, R. A., T. M. Donovan, P. Mackay, W. J. Zielinsky, and J. S. Buzas. 2007. Comparing scat detection dogs, cameras, and hair snares for surveying carnivores. J. Wildl. Manag. 71:2018–2025. MacKenzie, D. I. 2006. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press, Academic Press, Burlington, MA. Magoun, A. J., and J. P. Copeland. 1998. Characteristics of wolverine reproductive den sites. J. Wildl. Manag. 62:1313–1320. Magoun, A. J., C. D. Long, M. K. Schwartz, K. L. Pilgrim, R. E. Lowell, and P. Valkenburg. 2011. Integrating motion-detection cameras and hair snags for wolverine identification. J. Wildl. Manag. 75:731–739. Matassa, C. M., and G. C. Trussell. 2011. Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266. Mattisson, J., H. Andren, J. Persson, and P. Segerstrom. 2011. Influence of intraguild interactions on resource use by wolverines and Eurasian lynx. J. Mammal. 92:1321–1330. McKelvey, K. S., J. P. Copeland, M. K. Schwartz, J. S. Littell, K. B. Aubry, J. R. Squires, et al. 2011. Climate change predicted to shift wolverine distributions, connectivity, and dispersal corridors. Ecol. Appl. 21:2882–2897. Morrison, E. B. 2011. Vigilance behavior of a tropical bird in response to indirect and direct cues of predation risk. Behaviour 148:1067–1085. Murphy, K. M., G. S. Felzien, M. G. Hornocker, and T. K. Ruth. 1995. Encounter competition between bears and cougars: some ecological implications. Ursus 10:55–60. Petit, L. J., and D. R. Petit. 1996. Factors governing habitat selection by prothonotary warblers: field tests of the Fretwell-Lucas models. Ecol. Monogr. 66:367–387. Pinheiro, J., B. Douglas, D. Saikat, S. Deepayan, and R Core Team. “nlme: Linear and Nonlinear Mixed Effects Models, 2012.” R package version 3:1-78. http://cran.r-project.org/web/packages/nlme/index.html Pyke, G. H., H. R. Pulliam, and E. L. Charnov. 1977. Optimal foraging: a selective review of theory and tests. Q. Rev. Biol. 00:137–154. R Foundation for Statistical Computing. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Real, D., S. M. Reader, D. Sol, P. T. McDougall, and N. J. Dingemanse. 2007. Integrating animal temperament within ecology and evolution. Biol. Rev. 82:291–318. Ripple, W. J., and R. L. Beschta. 2006. Linking wolves to willows via risk-sensitive foraging by ungulates in the northern Yellowstone ecosystem. For. Ecol. Manage. 230:96–106. Rosenzweig, M. L. 1981. A Theory of Habitat Selection. Ecology 62:327–335. Rowland, M. M., M. J. Wisdom, D. H. Johnson, B. C. Wales, J. P. Copeland, and F. B. Edelmann. 2003. Evaluation of landscape models for wolverines in the interior northwest, United States of America. J. Mammal. 84:92–105. Sheriff, M. J., C. J. Krebs, and R. Boonstra. 2009. The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J. Anim. Ecol. 78:1249–1258. Sih, A. 1984. Optimal behaviour and density-dependent predation. Am. Nat. 123:314–326. Sih, A., P. Crowley, M. McPeek, J. Petranka, and K. Strohmeier. 1985. Predation, competition, and prey communities: a review of field experiments. Annu. Rev. Ecol. Syst. 16:269–311. Sih, A., A. Bell, and J. C. Johnson. 2004a. Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19:372–378. Sih, A., A. M. Bell, J. C. Johnson, and R. E. Ziemba. 2004b. Behavioural syndromes: an integrative overview. Q. Rev. Biol. 79:241–277. Sonderegger, D. 2015. SiZer: significant zero crossings. R package verison 0.1-4. Available at: www.r-project.org. Toms, J. D., and M. L. Lesperance. 2003. Piecewise regression: a tool for identifying ecological thresholds. Ecology 84:2034–2041. Vitousek, P. M., H. A. Mooney, J. Lubchenko, and J. M. Melillo. 1997. Human domination of earth's ecosystems. Science 277:494–499. Waits, L. P., and D. Paetkau. 2005. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J. Wildl. Manag. 69:1419–1433. Wang, Z., Z. Li, G. Beauchamp, and Z. Jiang. 2011. Flock size and human disturbance affect vigilance of endangered red-crowned cranes (Grus japonensis). Biol. Conserv. 144:101–105. Wolff, J. O., and T. Van Horn. 2003. Vigilance and foraging patterns of American elk during the rut in habitats with and without predators. Can. J. Zool. 81:266–271. Woodroffe, R. 2000. Predators and people: using human densities to interpret declines of large carnivores. Anim. Conserv. 3:165–173. Woodroffe, R., S. Thirgood, and A. Rabinowitz. 2005. The future of coexistence: Resolving human-wildlife conflict in a changing world. Pp. 370–474 in S. Thirgood and A. Rabinowitz, eds. People and wildlife, conflict or coexistence? Cambridge Univ. Press, Nature. Zuur, A., E. N. Ieno, N. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R. Chapter 4. Springer Science & Business Media, New York.