Abstract
The ecology of wildlife living in proximity to humans often differs from that in more natural places. Animals may perceive anthropogenic features and people as threats, exhibiting avoidance behavior, or may acclimate to human activities. As development expands globally, changes in the ecology of species in response to human phenomena may determine whether animals persist in these changing environments. We hypothesize that American black bears (Ursus americanus) persist within developed areas by effectively avoiding risky landscape features. We test this by quantifying changes in the movements of adult females from a population living within exurban and suburban development. We collected hourly GPS data from 23 individuals from 2012 to 2014 and used step-selection functions to estimate selection for anthropogenic features. Females were more avoidant of roads and highways when with cubs than without and were more responsive to increased traffic volume. As bears occupied greater housing densities, selection for housing increased, while avoidance of roads and responsiveness to traffic increased. Behavioral flexibility allowed bears in highly developed areas to alter selection and avoidance for anthropogenic features seasonally. These findings support the hypothesis that black bears perceive human activity as risky, and effectively avoid these risks while inhabiting developed areas. We document a high amount of individual variation in selection of anthropogenic features within the study population. Our findings suggest that initially, wildlife can successfully inhabit developed landscapes by effectively avoiding human activity. However, variation among individuals provides the capacity for population-level shifts in behavior over time.
Similar content being viewed by others
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Animal Care and Use Committee (1998) Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J Mammal 79:1416–1431
Anthony LL, Blumstein DT (2000) Integrating behaviour into wildlife conservation: the multiple ways that behaviour can reduce Ne. Biol Conserv 95:303–315
Baker PJ, Dowding CV, Molony SE, White PC, Harris S (2007) Activity patterns of urban red foxes (vulpes vulpes) reduce the risk of traffic-induced mortality. Behav Ecol 18:716–724
Barber JR, Crooks KR, Fristrup KM (2010) The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol 25:180–189
Baruch-Mordo S, Wilson KR, Lewis DL, Broderick J, Mao JS, Breck SW (2014) Stochasticity in natural forage production affects use of urban areas by black bears: implications to management of human-bear conflicts. PLoS One 9:e85122
Bateman P, Fleming P (2012) Big city life: carnivores in urban environments. J Zool 287:1–23
Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R Package Version 1:1–12
Beckmann JP, Berger J (2003a) Using black bears to test ideal-free distribution models experimentally. J Mammal 84:594–606
Beckmann JP, Berger J (2003b) Rapid ecological and behavioral changes in carnivores: the response of black bears to (Ursus americanus) to altered food. J Zool 261:207–212
Beyer HL (2014) Geospatial modeling environment. http://www.spatialecology.com/gme. Accessed May 2015
Chapron G, Lopez-Bao JV (2014) Conserving carnivores: politics in play. Science 343:1199–1200
Clark JD, Eastridge R (2006) Growth and sustainability of black bears at white river national wildlife refuge, Arkansas. J Wildl Manag 70:1094–1101
Coulon A, Morellet N, Goulard M, Cargnelutti B, Angibault J, Hewison AJM (2008) Inferring the effects of landscape structure on roe deer movements using a step selection function. Landsc Ecol 23:603–614
Dahle B, Swenson JE (2003) Seasonal range size in relation to reproductive strategies in brown bears Ursus arctos. J Anim Ecol 72:660–667
Dall SR (2004) Behavioural biology: fortune favours bold and shy personalities. Curr Biol 14:470–472
Darrow PA, Shivik JA (2009) Bold, shy, and persistent: variable coyote response to light and sound stimuli. Appl Anim Behav Sci 116:82–87
Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 158:277–285
DeStefano S, DeGraaf RM (2003) Exploring the ecology of suburban wildlife. Front Ecol Environ 1:95–101
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12
Eiler JH, Wathen WG, Pelton MR (1989) Reproduction in black bears in the southern Appalachian Mountains. J Wildl Manag 53:353–360
Elfstrom M, Zedrosser A, Stoen O-G, Swenson JE (2012) Ultimate and proximate mechanisms underlying the occurrence of bears close to human settlements: review and management implications. Mamm Rev 44:5–18
Evans MJ, Hawley JE, Rego PW, Rittenhouse TAG (2017) Black bear recolonization patterns on human-dominated landscapes vary based on housing: new insights from spatially explicit density models. Landsc Urban Plan 162:13–24
Fortin D, Boyce MS, Merrill EH, Fryxell JM (2004) Foraging costs of vigilance in large mammalian herbivores. Oikos 107:172–180
Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330
Francis CD, Barber JR (2013) A framework for understanding noise impacts on wildlife: an urgent conservation priority. Front Ecol Environ 11:305–313
Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11
Fry JA, Xian G, Jin S, Dewitz JA, Homer CG, Yang L, Barnes CA, Herold ND, Wickham JD (2011) Completion of the 2006 national land cover database for the conterminous united states. Photogramm Eng Remote Sens 77(9):858–864
Garshelis DL, Noyce KV, Ditmer MA (2012) Ecology and population dynamics of black bears in Minnesota. In: Cornicelli L, Carstensen M, Grund MD, Larson MA, Lawrence JS (eds) Summaries of wildlife research findings 2012. Minnesota DNR, St. Paul, pp 13–27
Gehrt SD, Brown JL, Anchor C (2011) Is the urban coyote a misanthropic synanthrope? The case from Chicago. Cities Environ 4:3
Groffman PM, Baron JS, Blett T, Gold AJ, Goodman I, Gunderson LH, Levinson BM, Palmer MA, Paerl HW, Peterson GD (2006) Ecological thresholds: the key to successful environmental management or an important concept with no practical application? Ecosystems 9:1–13
Hopkins JB (2013) Use of genetics to investigate socially learned foraging behavior in free-ranging black bears. J Mammal 94:1214–1222
Hosmer DW, Leeshow S (2000) Applied logistic regression. Wiley Inc., New York
Hristienko H, McDonald JE Jr (2007) Going into the 21st century: a perspective on trends and controversies in the management of the American black bear. Ursus 18:72–88
Hulbert IA, French J (2001) The accuracy of GPS for wildlife telemetry and habitat mapping. J Appl Ecol 38:869–878
Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71
Johnson HE, Breck SW, Baruch-Mordo S, Lewis DL, Lackey CW, Wilson KR, Broderick J, Mao JS, Beckmann JP (2015) Shifting perceptions of risk and reward: dynamic selection for human development by black bears in the western United States. Biol Conserv 187:164–172
Kertson BN, Spencer RD, Marzluff JM, Hepinstall-Cymerman J, Grue CE (2011) Cougar space use and movements in the wildland–urban landscape of western Washington. Ecol Appl 21:2866–2881
Knopff AA, Knopff KH, Boyce MA, St Clair CC (2014) Flexible habitat selection by cougars in response to anthropogenic development. Biol Conserv 178:136–145
Kohl MT, Stahler DR, Metz MC, Forester JD, Kauffman MJ, Varley N, White PJ, Smith DW, MacNulty DR (2018) Diel predator activity drives a dynamic landscape of fear. Ecol Monogr 88(4):638–652
Koops MA, Abrahams MV (1998) Life history and the fitness consequences of imperfect information. Evol Ecol 12:601–613
Lele SR, Merrill EH, Keim J, Boyce MS (2013) Selection, use, choice and occupancy: clarifying concepts in resource selection studies. J Anim Ecol 82:1183–1191
Lewis D, Breck S, Wilson K, Webb C (2014) Modeling black bear population dynamics in a human-dominated stochastic environment. Ecol Model 294:51–58
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
Linnell JD, Swenson JE, Anderson R (2001) Predators and people: conservation of large carnivores is possible at high human densities if management policy is favourable. Anim Conserv 4:345–349
Lowry H, Lill A, Wong B (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549
Lukacs PM, Burnham KP, Anderson DR (2009) Model selection bias and Freedman’s paradox. Ann Inst Stat Math 62:117–125
Martin JG, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318
Matthiopoulos J, Hebblewhite M, Aarts G, Fieberg J (2011) Generalized functional responses for species distributions. Ecology 92:583–589
Mazur R, Seher V (2008) Socially learned foraging behavior in wild black bears, Ursus americanus. Anim Behav 75:1503–1508
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260
Merkle JA, Robinson HS, Krausman PR, Alaback P (2013) Food availability and foraging near human developments by black bears. J Mammal 94:378–385
Messmer TA (2009) Human–wildlife conflicts: emerging challenges and opportunities. Hum Wildl Confl 3:10–17
Naves J, Wiegand T, Revilla E, Delibes M (2003) Endangered species constrained by natural and human factors: the case of brown bears in northern Spain. Conserv Biol 17:1276–1289
Nellemann C, Støen O, Kindberg J, Swenson JE, Vistnes I, Ericsson G, Katajisto J, Kaltenborn BP, Martin J, Ordiz A (2007) Terrain use by an expanding brown bear population in relation to age, recreational resorts and human settlements. Biol Conserv 138:157–165
Ordiz A, Støen O, Delibes M, Swenson JE (2011) Predators or prey? Spatio-temporal discrimination of human-derived risk by brown bears. Oecologia 166:59–67
Powell RA, Zimmerman JW, Seaman DE, Gilliam JF (1996) Demographic analyses of a hunted black bear population with access to a refuge. Conserv Biol 10:224–234
Powell RA, Zimmerman JW, Seaman DE (1997) Ecology and behaviour of North American black bears: home ranges, habitat, and social organization. Springer, New York
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed Sept 2016
Remeš V (2000) How can maladaptive habitat choice generate source-sink population dynamics? Oikos 91:579–582
Riley SPD, Sauvajot RM, Fuller TK, York EC, Kamradt DA, Bromley C, Wayne RK (2003) Effects of urbanization and habitat fragmentation on bobcats and coyotes in southern California. Conserv Biol 17:566–576
Robertson BA, Rehage JS, Sih A (2013) Ecological novelty and the emergence of evolutionary traps. Trends Ecol Evol 28:552–560
Rode KD, Farley SD, Robbins CT (2006) Sexual dimorphism, reproductive strategy, and human activities determine resource use by brown bears. Ecology 87:2636–2646
Rodriguez-Prieto I, Fernández-Juricic E, Martín J, Regis Y (2009) Antipredator behavior in blackbirds: habituation complements risk allocation. Behav Ecol 20:371–377
Roever CL, Boyce MS, Stenhouse GB (2010) Grizzly bear movements relative to roads: application of step selection functions. Ecography 33:1113–1122
Rogers LL, Allen W (1987) Habitat suitability index models: black bear upper great lakes region. U.S. Fish Wildlife Service Biology Report 82(10.144)
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480
Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
Slater P (1981) Individual differences in animal behavior. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology. Springer, New York, pp 35–49
Spencer RD, Beausoleil RA, Martorello DA (2007) How agencies respond to human-black bear conflicts: a survey of wildlife agencies in North America. Ursus 18:217–229
Steyaert SMJG, Zedrosser A, Elfstrom M, Ordiz A, Leclerc M, Frank SC, Kindberg J, Stoen O-G, Brunberg S, Swenson JE (2016) Ecological implications from spatial patterns in human-caused brown bear mortality. Wildl Biol 22(4):144–152
Therneau T (2015) A package for survival analysis in S v 2.38
Thurfjell H, Ciuti S, Boyce M (2014) Applications of step-selection functions in ecology and conservation. Mov Ecol 2:4
Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev 86:640–657
Van Horne B (1983) Density as a misleading indicator of habitat quality. J Wildl Manag 47:893–901
Acknowledgements
We thank L. S. Eggert for help with manuscript preparation. Funding provided by Federal Aid in Wildlife Restoration Act under Project W-49-R “Wildlife Investigations” administered by the Connecticut Department of Energy and Environmental Protection, Wildlife Division.
Author information
Authors and Affiliations
Contributions
MJE conceived the study; JEH and PWR designed data collection and conducted fieldwork; and MJE designed and conducted analyses and led the writing of the manuscript, with contributions and supervision from TAGR.
Corresponding author
Additional information
Communicated by Andreas Zedrosser.
This work quantifies habitat selection during movements of a large carnivore through human development, including neighborhoods with different housing densities. The movement strategies we identify indicate how wildlife live within and may adapt to human development.
Electronic supplementary material
Below is the link to the electronic supplementary material.
442_2018_4307_MOESM1_ESM.pdf
Changes in model-averaged selection parameter estimates (βω) and standard errors (SEω) of the relationship between anthropogenic variables and log odds of black bear steps estimated by step selection functions using increasing numbers of simulated steps. Different symbols correspond to different individual bears, selected at random from the study population. (PDF 235 kb)
Rights and permissions
About this article
Cite this article
Evans, M.J., Hawley, J.E., Rego, P.W. et al. Hourly movement decisions indicate how a large carnivore inhabits developed landscapes. Oecologia 190, 11–23 (2019). https://doi.org/10.1007/s00442-018-4307-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4307-z