2008 NORTHEASTERN NATURALIST 15(4):619–625 Behavioral Responses of Eastern Gray Squirrels in Suburban Habitats Differing in Human Activity Levels Christopher A. Cooper1, Allison J. Neff 1, David P. Poon1, and Geoffrey R. Smith1,* Abstract - We observed the alert responses of Sciurus carolinensis (Eastern Gray Squirrel) to two different approach stimuli (human only and human with a leashed dog) in two suburban habitats differing in the level of human activity. Alert distance in the habitat with higher levels of human activity was significantly shorter than the alert distance in the habitat with lower levels of human activity. Overall, the alert distance did not differ between the approach by a human alone and the approach by a human with a dog; however, in the high human activity sites (but not the low human activity sites), the presence of the dog increased alert distance in the squirrels. In addition, squirrels tended to initially respond by running more in the high human activity sites, but the presence of the dog increased the number of squirrels whose initial responses were to not run. Our results suggest that Eastern Gray Squirrel antipredator behavior, at least in response to humans and human-associated animals, is influenced by the level of human activity in the surrounding habitat. Introduction As natural habitats have become reduced and fragmented as a result of human development, many animals are being confronted with increased interactions with humans. In some instances, animals alter their behavior in the presence of humans, and these alterations in behavior can have consequences for other aspects of the animals’ ecology (e.g., Ditchkoff et al. 2006, George and Crooks 2006). Indeed, disturbance by humans has been equated to a form of predation risk (e.g., Beale and Monaghan 2004a, Frid and Dill 2002). Thus, it would be expected that animals should respond to human disturbance (i.e., the approach of humans) in a manner similar to how they respond to the approach of a predator (see Frid and Dill 2002). Animals living in areas with high levels of human visitation typically reduce their “antipredator” responses towards humans (e.g., lizards [Labra and Leonard 1999], mammals [Magle et al. 2005, Neuhaus and Mainini 1998], and birds [Walker et al. 2006]). However, the manner by which humans approach can also affect the behavioral response of animals (see Stankowich and Blumstein 2005 for a review of flight responses of animals). For example, the presence of a leashed dog (e.g., Banks and Bryant 2007, Burger et al. 2007, Miller et al. 2001) or the approach of humans off hiking trails, or on snowmobiles or other vehicles (e.g., Freddy et al. 1986, Papouchis et al. 2001, Taylor and Knight 2003a) can increase the antipredator response of animals to the presence of humans. 1Department of Biology, Denison University, Granville, OH 43023. *Corresponding author - smithg@denison.edu. 620 Northeastern Naturalist Vol. 15, No. 4 One species that is potentially affected by increased human presence is Sciurus carolinensis Gmelin (Eastern Gray Squirrel). Eastern Gray Squirrels are known to alter their behavior (e.g., patch use, flight-initiation distance) in response to perceived predation risk (Dill and Houtman 1989, Newman et al. 1988). We examined the behavioral responses of Eastern Gray Squirrels to the approach of humans in sites differing in the level of human activity. We predicted that Eastern Gray Squirrels would allow a closer approach in areas with higher levels of human activity. We also examined the response of Eastern Gray Squirrels to the approach of humans alone or with a leashed dog. Dogs are potential urban and suburban predators on Eastern Gray Squirrels (Van Der Merwe et al. 2005). We predicted that Eastern Gray Squirrels would respond to the approach of a human with a dog more readily than they would respond to the approach of only a human. Methods We conducted our study on and around the Denison University campus in Granville, Licking County, OH. We identified several sites with low levels of human activity and sites with high levels of human activity. The low human-activity level sites were more wooded sites with numerous trees and vegetation and low levels of human activity (i.e., no sidewalks or open areas for human traffic). The high human-activity level sites were more open with fewer trees, had sidewalks, and thus had higher levels of human traffic. Two different approach stimuli were used to elicit responses from gray squirrels. Either a human walking a six-month-old Golden Retriever on a leash or a human walking alone would approach an undisturbed squirrel. All approaches with or without the dog followed the same pattern: upon sighting an apparently undisturbed squirrel, the experimenter approached the squirrel directly. The distance at which the approach began was therefore variable, but not recorded. When the squirrel exhibited an initial response behavior (see below), the researcher stopped and marked his/her location and the location of the squirrel. The distance between the approaching researcher and the squirrel was then measured using a meter tape to the nearest cm (this value is the alert distance; see Taylor and Knight 2003b). Any approaches that were interrupted by external factors (e.g., approach by pedestrians, interactions with other squirrels) or in which the dog barked were excluded from our analyses. Approximately 17 trials were completed with each approach stimulus at each of the two types of locations (Total n = 71 approaches). In addition to recording the alert distance, we also categorized the initial behavioral response of the squirrels into either run (ran, ran up tree) or no run (froze, tail up, or flickered tail) responses. Efforts were made to minimize the possibility that individual squirrels were approached more than once by not conducting trials in the same local vicinity more than once, which would also reduce the likelihood of habituation of squirrels used in later trials to the presence of the researcher and dog. Two-way ANOVAs were used to compare alert distances between approach stimuli and sites with differing levels of human activity. Given the 2008 C.A. Cooper, A.J. Neff, D.P. Poon, and G.R. Smith 621 relatively low power of this ANOVA to detect approach stimulus effects (Power = 0.076), and the interaction of approach stimulus and site (Power = 0.318), we also ran separate ANOVAs comparing approach stimuli in each site type. Chi-square tests were used to compare the initial response behaviors between approach stimuli and sites with differing levels of human activity. Means are given ± 1 SE. Results The mean alert distance for squirrels from sites with low levels of human activity (10.44 ± 6.65 m, n = 32) was greater than the mean alert distance for squirrels from sites with high levels of human activity (5.33 ± 2.70 m, n = 39, F1,67 = 19.58, P < 0.0001). There was no difference in the mean alert distance for squirrels approached by human alone (6.94 ± 1.17 m, n = 33) and by a human with a dog on a leash (8.24 ± 0.67 m, n = 38, F1,67 = 0.23, P = 0.63). The interaction between approach stimuli and site was not signifi- cant (F1,67 = 2.27, P = 0.14; Fig. 1). However, when analyzed for each site separately, the presence of the dog significantly increased the alert distance in the high human-activity sites (F1,37 = 8.67, P = 0.006; Fig. 1), but had no effect on the low human-activity sites (F1,30 = 0.25, P = 0.62; Fig. 1). The most frequent initial responses were run responses (e.g., running, or running up a tree, Table 1). Approach stimuli and site together influenced the Table 1. Initial behavioral responses of Eastern Gray Squirrels (Sciurus carolinensis) upon the approach of a human alone (No dog) or a human with a dog on a leash (Dog), and from low human-activity sites and high human-activity sites. Total number of observations for each initial response is given in parentheses. Low human activity High human activity Initial response No dog Dog No dog Dog Run (46) 8 8 18 12 No run (25) 5 11 2 7 Figure 1. Interaction of site and approach stimulus for alert distances of Eastern Gray Squirrels (Sciurus carolinensis). Means are given ± 1 SE. 622 Northeastern Naturalist Vol. 15, No. 4 initial behavioral response of the squirrels (χ2 3 = 9.94, P = 0.019; Table 1). More squirrels in the high human-activity sites responded by running than did squirrels in the low human-activity sites. The presence of the dog tended to increase the number of non-running responses in both sites. Discussion Squirrels allowed closer approaches and also ran more as an initial response in the sites with higher levels of human activity than in the sites with lower levels of human activity. The high human-activity sites in our study also had a lower density of trees, thus if Eastern Gray Squirrels increase alert distance with distance to refuge (Dill and Houtman 1989), we would have expected alert distance to be greater in the high human-activity sites. This is the opposite of what we observed. It may be that the presence of shrubs in the low human-activity sites contributed obstructive cover rather than protective cover (see Lazarus and Symonds 1992). In such a case, one would predict the squirrels to show greater alert distances in the area with greater obstructive cover (e.g., Lazarus and Symonds 1992, Lima 1987, Metcalfe 1984). Such a pattern fits our observations; however, the amount of shrub cover appeared to be minimally obstructive to visibility, so while we cannot preclude its effect, we suggest other factors may also be playing as great or greater roles in determining the pattern of alert distances we observed. For example, if the sites differ in resources, one might expect differences in the responses to the approach by humans or humans and dogs. Beale and Monaghan (2004b) found that birds in better condition responded at further distances to human disturbance than did birds in poorer condition. Thus, the differences between the two sets of sites in the squirrels’ behavioral responses may result from differences in resource availability or squirrel condition. We suggest a more likely explanation for the difference in alert distance between the high and low human-activity sites is the habituation of Eastern Gray Squirrels to humans (e.g., Magle et al. 2005, Neuhaus and Mainini 1998). Several other studies on mammals also suggest that they generally tend to allow closer approaches by humans in areas with higher levels of human activity (e.g., Marmota marmota Blumenbach [Alpine Marmot] [Neuhaus and Mainini 1998], Marmota olympus Merriam [Olympic Marmot] [Griffin et al. 2007], Cynomys ludovicianus Ord [Black-tailed Prairie Dog] [Magle et al. 2005], and Odocoileus hemionus Rafinesque [Mule Deer] [Stankowich and Coss 2007]). Thus, mammals appear able to habituate to the presence of humans, recognizing the relatively low threat they pose. Alternatively, the reduced alert distances in the high human-activity sites are consistent with the risk-allocation hypothesis (Lima and Bednekoff 1999). The risk-allocation hypothesis argues that there is a trade-off between engaging in antipredator behavior and engaging in other behaviors and activities (e.g., foraging, courtship, etc.; see also Lima and Dill 1990). The risk-allocation hypothesis predicts that time spent in antipredator behavior will actually decrease in some situations of high predation risk or frequency because the continual allocation to antipredator behavior bears too great a 2008 C.A. Cooper, A.J. Neff, D.P. Poon, and G.R. Smith 623 cost and so one can sometimes see counterintuitive results upon presentation of “predation risk” (see Lima and Bednekoff 1999). Our results are consistent with this explanation. We can therefore not differentiate between these hypotheses; however, our results do confirm that the presence of human disturbance does alter the behavior of gray squirrels, and that further study would be useful in differentiating between these two hypotheses. Our initial overall analysis suggested that Eastern Gray Squirrels made no distinction between the human only and human with a dog approaches in our study. However, when we considered each site type separately, we found that the presence of a dog on a leash increased the alert distance of squirrels in the high human activity sites, but not the low human activity sites. In addition, the presence of the leashed dog also appeared to alter the initial response of the squirrels, increasing the proportion of squirrels that responded by not running. These responses are consistent with previous observations on the effects of dogs on other mammals. Gustafson and Van Druff (1990) observed greater alert distances when gray squirrels were approached by a free-ranging dog than when approached by a human alone. Other studies of mammal responses to dogs on leashes suggest that, in general, mammals perceive humans with dogs on a leash as greater threats than humans alone (e.g., Mainini et al. 1993, Martinetto and Cugnasse 2001, Miller et al. 2001). It is not clear why there is a difference among sites with different levels of human activity, but our results suggest that this may be a worthwhile subject of future research. Our results suggest that Eastern Gray Squirrels may adjust their behavioral responses to humans to minimize the effects of disturbance by nonpredatory organisms. Thus, Eastern Gray Squirrels appear to be able to cope, at least behaviorally, with regular interactions with humans. Acknowledgments We thank C. Kight and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. Literature Cited Banks, P.B., and J.V. Bryant. 2007. Four-legged friend or foe? Dog walking displaces native birds from natural areas. Biology Letters 3:611–613. Beale, C.M., and P. Monaghan. 2004a. Human disturbance: People as predation-free predators? Journal of Applied Ecology 41:335–343. Beale, C.M., and P. Monaghan. 2004b. Behavioural responses to human disturbance: A matter of choice? Animal Behaviour 68:1065–1069. Burger, J., S.A. Carlucci, C.W. Jeitner, and L. Niles. 2007. Habitat choice, disturbance, and management of foraging shorebirds and gulls at a migratory stopover. Journal of Coastal Research 23:1159–1166. Dill, L.M., and R. Houtman. 1989. The influence of distance to refuge on flightinitiation distance in the gray squirrel (Sciurus carolinensis). Canadian Journal of Zoology 67:233–235. Ditchkoff, S.S., S.T. Saalfeld, and C.J. Gibson. 2006. Animal behavior in urban ecosystems: Modifications due to human-induced stress. Urban Ecosystems 9:5–12. 624 Northeastern Naturalist Vol. 15, No. 4 Freddy, D.J., W.M. Bronaugh, and M.C. Fowler. 1986. Responses of Mule Deer to disturbance by persons afoot and snowmobiles. Wildlife Society Bulletin 14:63–68. Frid, A., and L. Dill. 2002. Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6(1):11. George, S.L., and K.R. Crooks. 2006. Recreation and large mammal activity in an urban nature reserve. Biological Conservation 133:107–117. Griffin, S.C., J. Valois, M.L. Taper, and L.S. Mills. 2007. Effects of tourists on behavior and demography of Olympic Marmots. Conservation Biology 21:1070– 1081. Gustafson, E.J., and L.W. Van Druff. 1990. Behavior of black and gray morphs of Sciurus carolinensis in an urban environment. American Midland Naturalist 123:186–192. Labra, A., and F. Leonard. 1999. Intraspecific variation in antipredator responses of three species of lizards (Liolaemus): Possible effects of human presence. Journal of Herpetology 33:441–448. Lazarus, J., and M. Symonds. 1992. Contrasting effects of protective and obstructive cover on avian vigilance. Animal Behaviour 43:519–521. Lima, S.L. 1987. Distance to cover, visual obstructions, and vigilance in house sparrows. Behaviour 102:231–238. Lima, S.L., and P.A. Bednekoff. 1999. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. American Naturalist 153:649–659. Lima, S.L., and L.M. Dill. 1990. Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68:619–640. Magle, S., J. Zhu, and K.R. Crooks. 2005. Behavioral responses to repeated human intrusion by Black-tailed Prairie Dogs (Cynomys ludovicianus). Journal of Mammalogy 86:524–530. Mainini, B., P. Neuhaus, and P. Ingold. 1993. Behaviour of marmots Marmota marmota under the influence of different hiking activities. Biological Conservation 64:161–164. Martinetto, K., and J.M. Cugnasse. 2001. Reaction distance in Mediterranean Mouflon (Ovis gmelini musimon x Ovis sp.) in the presence of hikers with a dog on the Caroux plateau (Herault, France). Revue d’Ecologie – La Terre et la Vie 56:231–242. Metcalfe, N.B. 1984. The effects of habitat on the vigilance of shorebirds: Is visibility important? Animal Behaviour 32:981–985. Miller, S.G., R.L. Knight, and C.K. Miller. 2001. Wildlife responses to pedestrians and dogs. Wildlife Society Bulletin 29:124–132. Neuhaus, P., and B. Mainini. 1998. Reactions and adjustment of adult and young Alpine Marmots, Marmota marmota, to intense hiking activities. Wildlife Biology 4:119–123. Newman, J.A., G.M. Recer, S.M. Zwicker, and T. Caraco. 1988. Effects of predation hazard on foraging “constraints:” Patch-use strategies in grey squirrels. Oikos 53:93–97. Papouchis, C.M., F.J. Singer, and W.B. Sloan. 2001. Responses of Desert Bighorn Sheep to increased human recreation. Journal of Wildlife Management 65:573– 582. Stankowich, T., and D.T. Blumstein. 2005. Fear in animals: A meta-analysis and review of risk assessment. Proceedings of the Royal Society of London 272B:2627–2634. 2008 C.A. Cooper, A.J. Neff, D.P. Poon, and G.R. Smith 625 Stankowich, T., and R.G. Coss. 2007. Effects of risk assessment, predator behavior, and habitat on escape on escape behavior in Columbian Black-tailed Deer. Behavioral Ecology 18:358–367. Taylor, A.R., and R.L. Knight. 2003a. Wildlife responses to recreation and associated visitor perceptions. Ecological Applications 13:951–963. Taylor, A.R., and R.L. Knight. 2003b. Behavioral responses of wildlife to human activity: Terminology and methods. Wildlife Society Bulletin 31:1263–1271. Van der Merwe, M., J.S. Brown, and W.M. Jackson. 2005. The coexistence of Fox (Sciurus niger) and Gray (S. carolinensis) Squirrels in the Chicago metropolitan area. Urban Ecosystems 8:335–347. Walker, B.G., P.D. Boersma, and J.C. Wingfield. 2006. Habituation of adult Magellanic Penguins to human visitation as expressed through behavior and corticosterone secretion. Conservation Biology 20:146–154.