References
Altmann J. (1974). Observational study of behavior: sampling methods.Behav. 49(3–4), 227–66.
Arroyo, B, Mougeot, F, & Bretagnolle, V. (2017). Individual variation
in behavioural responsiveness to humans leads to differences in breeding
success and long‐term population phenotypic changes. Eco
Lett , 20(3), 317-325.
Ayon RE, Putman BJ, Clark RW. (2017). Recent encounters with
rattlesnakes enhance ground squirrel responsiveness to predator cues.Behav Ecol Sociobiol , 71(10), 1-10.
Bertram BCR. (1978). Living in groups: predators and prey . Krebs
JR, Davies NB. Behavioural ecology: an evolutionary approach. Blackwell
Scientific, Oxford, pp 64–96
Biro PA. (2012). Are most samples of animals systematically biased?
Consistent individual trait differences bias samples despite random
sampling. Oecologia , 171(2), 339–45.
Biro PA, Dingemanse NJ. (2009). Sampling bias resulting from animal
personality. Trends Ecol Evol , 24(2), 66–7.
Bjørvik LM, Dale S, Hermansen GH, Munishi PKT, Moe SR. (2014). Bird
flight initiation distances in relation to distance from human
settlements in a Tanzanian floodplain habitat. J Ornithol ,
156(1), 239–46.
Blumstein DT. (2016). Habituation and sensitization: new thoughts about
old ideas. Anim Behav , 120, 255–62.
Bonenfant M, Kramer DL. (1996). The influence of distance to burrow on
flight initiation distance in the woodchuck, Marmota monax .Behav Ecol , 7(3), 299–303.
Breck SW, Poessel SA, Mahoney P, Young JK. (2019). The intrepid urban
coyote: a comparison of bold and exploratory behavior in coyotes from
urban and rural environments. Sci Rep . 9(1), 1-11.
Brehm AM, Mortelliti A. (2018). Mind the trap: large-scale field
experiment shows that trappability is not a proxy for personality.Anim Behav , 142, 101–12.
Brown, J. S., & Kotler, B. P. (2004). Hazardous duty pay and the
foraging cost of predation. Eco lett , 7(10), 999-1014.
Bürkner P-C. (2017). brms: an R package for bayesian multilevel models
using stan. J Stat Soft. 80(1), 1-28.
Cabrera D, Andres D, McLoughlin PD, Debeffe L, Medill SA, Wilson AJ, et
al. (2017). Island tameness and the repeatability of flight initiation
distance in a large herbivore. Can J Zool , 95(10), 771–8.
Carrete M, Tella JL. (2009). Individual consistency in flight initiation
distances in burrowing owls: a new hypothesis on disturbance-induced
habitat selection. Biol Lett. 6(2), 167–70.
Clinchy M, Zanette LY, Roberts D, Suraci JP, Buesching CD, Newman C, et
al. (2016). Fear of the human “super predator” far exceeds the fear of
large carnivores in a model mesocarnivore. Behav Ecol , 27(6),
1826-1832.
Cooper WE JR, Frederick WG. (2007). Optimal time to emerge from refuge.Biol J Linn Soc , 91(3), 375–82.
Cooper, WE, & Sherbrooke, WC. (2015). FEAR and DREAD: starting
distance, escape decisions and time hiding in
refuge. Behaviour , 152(10), 1371-1389.
Corsini M, Marrot P, Szulkin M. (2019). Quantifying human presence in a
heterogeneous urban landscape. Behav Ecol , 30(6), 1632–41.
Creel, S., & Christianson, D. (2008). Relationships between direct
predation and risk effects. Trends Ecol Evol , 23(4), 194-201.
Engelhardt SC, Weladji RB. (2011). Effects of levels of human exposure
on flight initiation distance and distance to refuge in foraging eastern
gray squirrels (Sciurus carolinensis ). Can J Zool , 89(9),
823–30.
Garvey PM, Banks PB, Suraci JP, Bodey TW, Glen AS, Jones CJ, et al.
(2020). Leveraging motivations, personality, and sensory cues for
vertebrate pest management. Trends Ecol Evol , 35(11), 990–1000.
Geffroy B, Samia DSM, Bessa E, Blumstein DT. (2015). How nature-based
tourism might increase prey vulnerability to predators. Trends
Ecol Evol, 30(12), 755–65.
Gonson C, Pelletier D, Gamp E, Preuss B, Jollit I, Ferraris J. (2016).
Decadal increase in the number of recreational users is concentrated in
no-take marine reserves. Mar Pollut Bull , 107(1), 144–54.
Guiden PW, Bartel SL, Byer NW, Shipley AA, Orrock JL. (2019).
Predator–prey interactions in the Anthropocene: reconciling multiple
aspects of novelty. Trends Ecol Evol , 34(7), 616–27.
Hammond TT, Vo M, Burton CT, Surber LL, Lacey EA, Smith JE. (2019).
Physiological and behavioral responses to anthropogenic stressors in a
human-tolerant mammal. J Mammal , 100(6), 1928–40.
Hanson MT, Coss RG. (1997). Age differences in the response of
California ground squirrels (Spermophilus beecheyi ) to avian and
mammalian predators. J Comp Psychol , 111(2), 174–84.
Heithaus, M. R., Wirsing, A. J., Burkholder, D., Thomson, J., & Dill,
L. M. (2009). Towards a predictive framework for predator risk effects:
the interaction of landscape features and prey escape tactics. J
Anim Eco , 78(3), 556-562.
Holding ML, Putman BJ, Kong LM, Smith JE, Clark RW. 2020. Physiological
stress integrates resistance to rattlesnake venom and the onset of risky
foraging in California ground squirrels. Toxins , 12(10), 617.
Lapiedra O, Chejanovski Z, Kolbe JJ. (2016). Urbanization and biological
invasion shape animal personalities. Glob Change Biol , 23(2),
592–603.
Leger DW, Owings DH, Coss RG. (1983). Behavioral ecology of time
allocation in California ground squirrels (Spermophilus
beecheyi): microhabitat effects. J Comp Psychol , 97(4), 283–91.
Lima, S. L. (1998). Nonlethal effects in the ecology of predator-prey
interactions.
Bioscience, 48(1), 25-34.
Lima SL, Dill LM. (1990). Behavioral decisions made under the risk of
predation: a review and prospectus. Can J Zool, 68, 619–640.
Lowry H, Lill A, Wong BBM. (2012). Behavioural responses of wildlife to
urban environments. Biol Rev , 88(3), 537–49.
Michelangeli M, Wong BBM, Chapple DG. (2015). It’s a trap: sampling bias
due to animal personality is not always inevitable. Behav Ecol ,
27(1), 62–7.
Miranda AC, Schielzeth H, Sonntag T, Partecke J. (2013). Urbanization
and its effects on personality traits: a result of microevolution or
phenotypic plasticity? Glob Change Biol , 19(9), 2634–44.
Morelli F, Benedetti Y, Díaz M, Grim T, Ibáñez‐Álamo JD, Jokimäki J, et
al. (2019). Contagious fear: escape behavior increases with flock size
in European gregarious birds. Ecol Evol , 9(10), 6096–104.
Moller AP, Rubolini D, Lehikoinen E. (2008). Populations of migratory
bird species that did not show a phenological response to climate change
are declining. PNAS , 105(42), 16195–200.
Møller AP, Tryjanowski P. (2014). Direction of approach by predators and
flight initiation distance of urban and rural populations of birds.Behav Ecol , 25(4), 960–6.
Møller AndersP, Kwiecinski Z, Tryjanowski P. (2016). Prey reduce
risk-taking and abundance in the proximity of predators. Curr
Zool , 63(6), 591-598.
Nakagawa S, Johnson PCD, Schielzeth H. (2017). The coefficient of
determination R 2 and intra-class correlation coefficient from
generalized linear mixed-effects models revisited and expanded. J
R Soc Interface , 14(134), 20170213.
Oriol-Cotterill A, Valeix M, Frank LG, Riginos C, Macdonald DW. (2015).
Landscapes of coexistence for terrestrial carnivores: the ecological
consequences of being downgraded from ultimate to penultimate predator
by humans. Oikos , 124(10), 1263–73.
Ortiz CA, Pendleton EL, Newcomb KL, Smith JE. (2019). Conspecific
presence and microhabitat features influence foraging decisions across
ontogeny in a facultatively social mammal. Behav Ecol Sociobiol ,
73(4), 1-14.
Owings DH, Coss RG. (1977). Snake mobbing by California ground
squirrels: adaptive variation and ontogeny. Behav , 62(1–2),
50–68.
Owings DH, Leger DW. (2010). Chatter vocalizations of California ground
squirrels: predator- and social-role specificity. Zeitschrift für
Tierpsychologie , 54(2), 163–84.
Peacor, S. D., Barton, B. T., Kimbro, D. L., Sih, A., & Sheriff, M. J.
(2020). A framework and standardized terminology to facilitate the study
of predation‐risk effects.
Ecology, 101(12), e03152.
Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT. (2013).
Development of boldness and docility in yellow-bellied marmots.Anim Behav , 86(6), 1147–54.
Preisser, E. L., Bolnick, D. I., & Benard, M. F. (2005). Scared to
death? The effects of intimidation and consumption in predator–prey
interactions. Ecolog y, 86(2), 501-509.
Pulliam HR. (1973). On the advantages of flocking. J Theor Biol ,
38(2), 419–22.
Putman, B. J., Coss, R. G., & Clark, R. W. (2015). The ontogeny of
antipredator behavior: age differences in California ground squirrels
(Otospermophilus beecheyi ) at multiple stages of rattlesnake
encounters. Behav Ecol and Sociobiol , 69(9), 1447-1457.
R Core Team (2020). R: A language and environment for statistical
computing. R Foundation\ for Statistical Computing,
Vienna, Austria. https://www.R-project.org/.
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. (2007).
Integrating animal temperament within ecology and evolution. Biol
Rev , 82(2), 291–318.
Rodriguez-Prieto I, Fernández-Juricic E, Martín J, Regis Y. (2008).
Antipredator behavior in blackbirds: habituation complements risk
allocation. Behav Ecol , 20(2), 371–7.
Runyan AM, Blumstein DT. (2004). Do individual differences influence
flight initiation distance? J Wildl Manage , 68(4), 1124–9.
Sih A. (1992). Prey uncertainty and the balancing of antipredator and
feeding needs. Am Nat , 139(5), 1052–69.
Sih A, Bell AM, Johnson JC, Ziemba RE. (2004). Behavioral syndromes: an
integrative overview. Q Rev Biol , 79(3), 241–77.
Sih A, Bell A, Johnson JC. (2004). Behavioral syndromes: an ecological
and evolutionary overview. Trends Ecol Evol , 19(7), 372–8.
Sih A, Ferrari MCO, Harris DJ. (2011). Evolution and behavioural
responses to human-induced rapid environmental change. Evol Appl ,
4(2), 367–87.
Sih A, Cote J, Evans M, Fogarty S, Pruitt J. (2012). Ecological
implications of behavioural syndromes. Eco Lett ,15(3), 278–89.
Smith JE, Long DJ, Russell ID, Newcomb KL, Muñoz VD. (2016).Otospermophilus beecheyi (Rodentia: Sciuridae). Mammal
Species , 48(939), 91–108.
Smith, JE, Gamboa, DA, Spencer, JM, Travenick, SJ, Ortiz, CA, Hunter,
RD, & Sih, A. (2018). Split between two worlds: automated sensing
reveals links between above-and belowground social networks in a
free-living mammal. Proc R Soc B , 373(1753), 20170249.
Smith JE, Smith IB, Working CL, Russell ID, Krout SA, Singh KS, et al.
(2021). Host traits, identity, and ecological conditions predict
consistent flea abundance and prevalence on free-living California
ground squirrels. Int J Parasitol .
Stan Development Team. (2015). “RStan: the R interface to Stan.” R
package version 2.21. 2, http://mc-stan.org/
Stankowich T, Blumstein DT. (2005). Fear in animals: a meta-analysis and
review of risk assessment. Proc R Soc B , 272(1581), 2627–34.
Strasser EH, Heath JA. (2013). Reproductive failure of a human-tolerant
species, the American kestrel, is associated with stress and human
disturbance. J Appl Ecol , 50(4), 912–9.
Suraci JP, Clinchy M, Zanette LY, Wilmers CC. (2019). Fear of humans as
apex predators has landscape‐scale impacts from mountain lions to mice.Ecol Lett , 22(10), 1578–86.
Tätte K, Møller AP, Mänd R. (2018). Towards an integrated view of escape
decisions in birds: relation between flight initiation distance and
distance fled. Anim Behav , 136, 75–86.
Trimmer PC, Ehlman SM, Sih A. (2017). Predicting behavioural responses
to novel organisms: state-dependent detection theory. Proc R Soc
B , 284(1847), 20162108.
Trouilloud, W, Delisle, A, & Kramer, DL. (2004). Head raising during
foraging and pausing during intermittent locomotion as components of
antipredator vigilance in chipmunks. Anim Behav , 67(4), 789-797.
Uchida, K., & Blumstein, D. T. (2021). Habituation or sensitization?
Long-term responses of yellow-bellied marmots to human
disturbance. Behav Ecol.
Uchida K, Suzuki K, Shimamoto T, Yanagawa H, Koizumi I. (2015). Seasonal
variation of flight initiation distance in Eurasian red squirrels in
urban versus rural habitat. J Zool , 298(3), 225–31.
Uchida K, Suzuki KK, Shimamoto T, Yanagawa H, Koizumi I. (2019).
Decreased vigilance or habituation to humans? Mechanisms on increased
boldness in urban animals. Behav Ecol , 30(6), 1583–90.
van der Marel A, López-Darias M, Waterman JM. (2019). Group-enhanced
predator detection and quality of vigilance in a social ground squirrel.Anim Behav , 151, 43–52.
Vincze E, Papp S, Preiszner B, Seress G, Bókony V, Liker A. (2016).
Habituation to human disturbance is faster in urban than rural house
sparrows. Behav Ecol , 27(5), 1304–13.
Watson JEM, Shanahan DF, Di Marco M, Allan J, Laurance WF, Sanderson EW,
et al. (2016). Catastrophic declines in wilderness areas undermine
global environment targets. Curr Biol , 26(21), 2929–34.
Wilson, D. S., Clark, A. B., Coleman, K., & Dearstyne, T. (1994).
Shyness and boldness in humans and other animals. Trends Ecol
Evol , 9(11), 442-446.
Wilson MW, Ridlon AD, Gaynor KM, Gaines SD, Stier AC, Halpern BS.
(2020). Ecological impacts of human‐induced animal behaviour change.Ecol Lett , 23(10), 1522–36.
Wirsing, AJ, Heithaus, MR, Brown, JS, Kotler, BP, & Schmitz, OJ.
(2021). The context dependence of non‐consumptive predator
effects. Eco Lett , 24(1), 113-129.
Ydenberg RC, Dill LM. (1986). The economics of fleeing from predators.Adv Study Behav , 16, 229–49.
Table 1. Predictor effects on squirrel flight initiation
distance (FID). Values include posterior mean estimates ± standard error
(SE) with the 95% credible intervals (CIs). Significant predictors are
shown in bold.
Figure 1. Graphic depicting multiple components of the
antipredator response.
Figure 2. Model predicted relationship between FID andA) average level of human activity at home site, B)trappability, and C) foraging group size. Shaded regions in A
and B represent 95% credible intervals. For panel C , the
middle quartile (dark line) represents the median; the box edges are the
upper and lower quartiles; the whiskers are 50% from the median, and
the closed circles correspond to the outliers, calculated as the values
smaller or larger than 1.5 times the box length (i.e., upper—lower
quantile).
Figure 3. Model predicted relationship between emergence time
and A ) human activity and B ) trappability. Shaded
regions represent 95% credible intervals.
Figure 4. Among-individual correlation between FID andA ) emergence time and B ) stop look distance. BLUPs
(best linear unbiased predictors) represent posterior means of
individual random intercepts extracted from the multivariate models.
Table 1. Predictor effects on squirrel flight initiation
distance (FID). Values include posterior mean estimates ± standard error
(SE) with the 95% credible intervals (CIs). Significant predictors are
shown in bold.