Ecological Applications, 13(6), 2003, pp. 1830–1834 q 2003 by the Ecological Society of America
IMPACT OF HUMAN NUISANCE DISTURBANCE ON VIGILANCE AND GROUP SIZE OF A SOCIAL UNGULATE REGEV MANOR1
AND
DAVID SALTZ
Mitrani Department of Desert Ecology, Blaustein Institute for Desert Research, Ben Gurion University, Sde Boker Campus 84990, Israel
Abstract. In social ungulates, the proportion of time devoted to vigilance is a function of group size (known as the group size effect). We studied how varying levels of human disturbance influence this function in the mountain gazelle ( Gazella gazella) along the southern coastal plain of Israel. Based on current theory, we predicted that changes in the slope of this function should be associated with changes in average group size. In heavily disturbed areas, individual vigilance levels increased in the bigger groups, causing the vigilance vs. group size curve to flatten, i.e., vigilance was high in all group sizes. Consequently, and in accordance with theory, we found a negative relationship between group size and human disturbance. Specifically, we found that in open areas with low disturbance levels, gazelles were in bigger groups than in open areas with high disturbance levels. In social species, the disruption of behavioral patterns by increased human presence can affect their social structure. Because social structure is a key component in the evolution and dynamics of social species, its disruption by human disturbance can have a considerable effect on population performance even if the disturbance does not directly impact survival and reproduction. Social disruption due to increased access to natural areas should be an important consideration in managing fragmented landscapes. Key words: accessibility; feral dogs; fragmentation; Gazella gazella; group size; human disturbance; Israel; mountain gazelle; nuisance disturbance; social structure; vigilance.
INTRODUCTION Increased fragmentation and accessibility to natural areas is bringing humans in closer contact with wild populations. Often, this contact is merely a nuisance disturbance and does not constitute a direct threat to the animals. However, such nuisance disturbances may force animals to devote more time to safety-related behaviors, such as increased levels of vigilance, which come at the expense of foraging activities (Houston et al. 1993). This trade-off between safety and obtaining resources ultimately affects population performance (McNamara and Houston 1987). Thus, it is important in conservation efforts to understand the impact of human nuisance disturbance on animal behavior (McLean 1997). In social ungulates, the trade-off between food and safety is more complex because group size and, ultimately, social structure are involved (Jarman 1974). Ungulates exhibit a reduction in vigilance with increased group size (Hunter and Skinner 1998) due to the ‘‘many eyes’’ or ‘‘dilution’’ effects (Roberts 1996). Generally, ungulates disturbed by humans are expected to increase their antipredator behavior (Paveri-Fontana and Focardi 1994). However, in areas where human presence is common but harassment by humans in scarce, habituation may occur. In terms of vigilance as Manuscript received 6 December 2001; revised 16 December 2002; accepted 14 January 2003; final version received 17 March 2003. Corresponding Editor: D. B. Lindenmayer. 1 E-mail:
[email protected]
a function of group size, these changes may be classified as one of four general response types. (Fig. 1). In Type I, the level of vigilance will increase equally for all group sizes, and the slope of vigilance against group size will not change but the intercept will increase. In Type II, habituation will occur and the level of vigilance will decrease equally for all group sizes, resulting in an unchanged slope of vigilance against group size but a lower intercept. For Type III, there will be a general increase in vigilance, but the response will be stronger in the larger group size because small groups are already near the maximum level of vigilance and the intercept will remain unchanged. For Type IV, there will be a general decrease in vigilance (habituation), but the response will be stronger in the smaller groups, in which case the slope of vigilance on group size will become more moderate and the intercept will decline. A change in the intercept or slope would, according to theory, be accompanied by a change in average group size (Paveri-Fontana and Focardi 1994). In reality, the change could be any combination of changes in intercept (Types I and II) and slope (Types III and IV). Here we report the results of a study on the effect of human disturbance and presence of predators (feral dogs) on the vigilance of mountain gazelles (Gazella gazella) in a heavily disturbed and fragmented area along the southern coastal plain on Israel. Human disturbance in this area consists mostly of hikers and offroad vehicles, which constitute a nuisance threat. Feral
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FIG. 1. Possible changes in the functional relationship between individual vigilance and group size (i.e., ‘‘the groups size effect’’; Roberts 1996) in response to increased threat/disturbance. If a Type I response occurs, group size is expected to increase. If any of the other responses shown here occurs, group size is expected to decrease or to show no change at all (depending on other factors). In order to identify the exact response, both intercept and slope values should be found. The actual response may be some combination of the four types.
dogs, on the other hand, pose a direct threat by preying on gazelle neonates (Manor 2001). Specifically, we studied how the function of vigilance vs. group size (i.e., ‘‘group size effect,’’ Roberts 1996) changes with increased disturbance, and we examined the impact of this change on average group size. METHODS We studied the gazelle population in a 120-km2 area along the southern Mediterranean coastal plain of Israel, south of the city of Ashdod (318409 N; 348309 E). Less than 60% of the area is natural sand dunes, most of them stable, dominated by the Artemisia monosperma–Retama raetam bush community. The remaining landscape is urban, agricultural, industrial, military, and transportation related. Based on the landscape, we divided the area into 13 subsections. In each subsection we selected a good observation site overlooking extensive areas of gazelle habitat. Each observation site was frequented 25–28 times during the period October 1998–February 2000 (weekends included). We conducted the observations with the aid of 7–21 3 40 binoculars and 15–45 3 60 spotting scope. Observations were made in five-hour blocks after sunrise, the time when gazelles are most active (Baharav 1981).
FIG. 2. Mean residual value of each of 13 subsections from the regression of vigilance on group size is positively related to human disturbance. The index of human disturbance was measured as the proportion of observation sessions in which hikers or off-road vehicles were sighted.
Each five-hour block was divided equally between three subsections, 1.5 hours in each. The order was regularly alternated. Many of the gazelles were individually recognizable and we recorded no movement between the subsections. In each site, we used the proportion of observation sessions in which pedestrians or off-road vehicles were sighted as an index of human disturbance. Feral dogs are common in the area and we used the proportion of the observations with feral dog sightings as an index of dog presence. We assessed habitat quality in each subsection based on perennial cover (Manor 2001) which, in these sand dunes, is positively correlated with the biomass of annuals and grasses, the main diet items of gazelles (Kaplan and Gutman 1989). Based on Baharav (1974), we classified sighted gazelles according to sex (only in adults) and age (young up to five months, or older). Also, we documented group size and composition (we distinguished among herds that contained only females with young, only males, and mixed herds). Focal samples (Altman 1974) were carried out to assess adult gazelle vigilance. Each focal sample lasted up to five minutes. Vigilance level was calculated as the proportion of time that a gazelle was standing with its head above shoulder level (FitzGibbon 1990) when
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REGEV MANOR AND DAVID SALTZ
FIG. 3. A negative relationship occurs between the regression coefficients of vigilance on group size and human disturbance level in the 13 subsections. As human disturbance increases, the group size effect almost disappears.
grazing. We excluded behavioral samples in which the gazelles stared at the observer or toward other specific disturbing factors. We terminated the focal sample before the 5-minute limit if the gazelle exited the field of vision or stayed with its head up .45 seconds. We assumed that gazelles that kept their head above shoulder level for such a long time had eaten enough, or were looking for new places to forage, or were staring at a disturbing factor that we could not see. We did not take more than one focal sample per individual per observation. We weighted each focal sample according to the time that it lasted. Vigilance level was arcsine and square-root transformed to obtain a normal distribution. To avoid pseudoreplication (caused by resampling the same individuals repeatedly in each subsections), we considered each subsection as our sampling unit. That is, to test the various factors affecting vigilance or group size, we used a single value per subsection for each of the dependent and predictor variables. We first tested what social factors affected vigilance by regressing vigilance level on group size, group composition, sex, and season (breeding or nonbreeding). After finding that only group size was significant, we tested the general effect of human disturbance, habitat quality, and presence of feral dogs on vigilance, car-
FIG. 4. There is no significant relationship between the y-intercepts of the regression of vigilance on group size and the index of human disturbance.
rying out a separate regression of vigilance on group size in each subsection. From these regressions, we derived the average residual value for each subsection and regressed them (weighted according to sample size in each subsection) on human disturbance, habitat quality, and indices of feral dog presence in each subsection. To see how the vigilance vs. group size slope changes between subsections and what factors affect it, we carried out separate regressions of vigilance on group size for each subsection. We then regressed the regressions coefficients and intercepts from these regressions on the factors found significant in the residual analysis. We calculated the intercept at the point where group size 5 1, as a group size of 0 is meaningless. We tested changes in group size by calculating the average group size of mixed (females and territorial male) and female-only groups in each subsection. Then we conducted a stepwise regression of average group size (weighted by the number of gazelles in each subsection) on the index of dog presence, the proportion of the area with low vegetation cover (habitat openness), human disturbance, and all possible interactions. RESULTS When data from all subsections were combined, vigilance was found to be negatively related to group size (n 5 457, R2 5 0.154, P , 0.001). In the regression of the mean residual value calculated for each subsection on human disturbance, habitat quality, and index of dog presence, only human disturbance was significant with a positive relationship (Fig. 2). Of the 13 slopes from the regression of vigilance on group size in each subsection, eight slopes were significantly negative and five were negative, but not significant (i.e., none of the regressions produced a positive slope). The coefficients from these regressions were negatively related to the human disturbance index (Fig. 3), but the y-intercept at the point where group size 5 1 varied little and was unaffected by the human disturbance index (Fig. 4). The average group size in the different subsections ranged from 2.3 to 3.5 and was, in fact, a function of
HUMAN IMPACT ON UNGULATE GROUP VIGILANCE
December 2003 TABLE 1.
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Factors affecting gazelle group size. Source
P
Coefficient
Low vegetation 3 human disturbance Low vegetation Presence of feral dogs
0.002 ,0.001 0.002
25.429 3.131 1.214
Note: Human disturbance by itself and all other possible interactions among the three factors were found to be insignificant.
various characteristics of the various subsections (Total GLM: F 5 27.529, df 5 3, 9, P , 0.001; R2 5 0.869). Three factors had a significant effect: the presence of feral dogs and the proportion of the area with low vegetation cover affected group size positively, and the interaction between the proportion of the area with low vegetation cover and human disturbance was negatively related to average group size (Table 1). The influence of human disturbance by itself and all other possible interactions among the three factors that were tested were insignificant. DISCUSSION In this study, we demonstrated a mechanism by which changes in individual animal behavior in response to human disturbance will ultimately affect the social structure, as manifested in the mean group size. Human presence was the overwhelming factor affecting gazelle vigilance in our study area. The amount of time that gazelles devoted to vigilance increased with human presence, but the change was dependent on group size. As human disturbance increased, the group size effect on vigilance decreased (i.e., the slope became less negative) and became negligible in places with high human disturbance. That is, in areas with high human presence, gazelles exhibited the same amount of vigilance no matter what their group size. The high and relatively unchanged intercept values also suggest that small groups are exhibiting the maximum or near-maximum level of vigilance even in the less disturbed areas. Thus, the decline in the steepness of the vigilance slope as a function of group size in areas with high human disturbance is due to increased vigilance in the larger groups, with little or no change in the smaller groups (i.e., a Type III response; Fig. 1b). Under the observed Type III response, the benefit derived from belonging to a larger group, in terms of reduction in the time allocated to vigilance by an individual, is expected to decline. Support for this prediction comes from the significant negative effect of the human disturbance 3 low vegetation interaction on group size. Namely, in open places with high human disturbance, gazelles tend to be in smaller groups than in open habitats with low human disturbance. Similar to other studies, habitat openness in itself and dog presence were associated with increased group size (Jarman 1974, Caraco et al. 1980, Lima 1998). The decrease of group size in response to human disturbance described in this study has not been doc-
umented previously in ungulates. In a single known study that attempted to evaluate how human disturbance affects group size, only the food distribution pattern was found to be a significant predictor of group size (Berger et al. 1983). The different responses of group size to human disturbance vs. feral dogs suggests that gazelles can distinguish between different types of threats (Mendelssohn 1974) and recognize human disturbance in our study area as a nuisance threat and not as a direct threat to survival, resulting in energy expenditure and vigilance. The response is in agreement with the model of Moody et al. (1996), which predicts that aggregation occurs only when it increases the fitness of the individual. As the landscape becomes more fragmented by human activities, the proximity and accessibility of humans to natural areas will increase and augment wildlife–human conflict. Such conflicts are often assessed in terms of the direct threats to the dynamics of the wild population (survival and reproductions), whereas behavioral changes are considered of lesser importance (Beissinger 1997, Clemmons and Buchholz 1997). However, disruption of behavioral patterns is linked to dynamics (McLellan and Shackleton 1989, Phillips and Alldredge 2000). Hence, in social animals, apparently benign human disturbances will impact the time budget of individuals, consequently affecting social structure and ultimately impacting population performance. ACKNOWLEDGMENTS Special thanks to M. Volchak and S. Cohen of the Israel Nature and Park Authority for technical support, to G. Borer for statistical advice, and to two anonymous reviewers. This is publication 376 of the Mitrani Department of Desert Ecology. LITERATURE CITED Altman, J. 1974. Observational studies of behaviour: sampling methods. Behaviour 49:227–265. Baharav, D. 1974. Notes on the population structure and biomass of the mountain gazelle, Gazella gazella gazella. Israel Journal of Zoology 23:39–44. Baharav, D. 1981. Food habits of the mountain gazelle in semi-arid habitats of eastern Galilee, Israel. Journal of Arid Environment, 4:63–69. Beissinger, S. R. 1997. Integrating behavior and conservation biology: potentials and limitations. Pages 3–22 in J. R. Clemmons and R. Buchholz, editors. Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, UK. Berger, J., D. Daneke, J. Johnson, and S. H. Berwick. 1983. Pronghorn foraging economy and predator avoidance in a desert ecosystem: implications for the conservation of large
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mammalian herbivores. Biological Conservation 25:193– 208. Caraco, T., S. Martindale, and H. R. Pulliam. 1980. Avian flocking in the presence of a predator. Nature 285:400– 401. Clemmons, J. R., and R. Buchholz. 1997. Linking conservation and behavior. Pages 1–3 in J. R. Clemmons, and R. Buchholz, editors. Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, UK. FitzGibbon, C. D. 1990. Anti-predator strategies of immature Thomson’s gazelles: hiding and the prone response. Animal Behavior 40:846–55. Houston, A. I., J. M. McNamara, and J. M. C. Hutchinson. 1993. General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society of London, Series B 341: 375–397. Hunter, L. T. B., and J. D. Skinner. 1998. Vigilance behavior in African ungulates: the role of predation pressure. Behaviour 135:195–211. Jarman, P. J. 1974. The social organization of antelope in relation to their ecology. Behaviour 48:215–267. Kaplan, D., and M. Gutman. 1989. Food composition of the mountain gazelle and cattle in the southern Golan, Israel. Israel Journal of Zoology 36:154. Lima, S. L. 1998. Stress and decision-making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27:215–290.
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Manor, R. 2001. Human impacts on mountain gazelle in a heavily disturbed and fragmented area of the southern coastal plain, Israel. Thesis. Ben-Gurion University, Sde Boker Campus, Israel. McLean, I. G. 1997. Conservation and the ontogeny of behavior. Pages 132–156 in J. R. Clemmons, and R. Buchholz, editors. Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, UK. McLellan, B. N., and D. M. Shackleton. 1989. Immediate reactions of grizzly bears to human activities. Wildlife Society Bulletin 17:269–274. McNamara, J. M., and A. I. Houston. 1987. Starvation and predation as factors limiting population size. Ecology 68: 1515–1519. Mendelssohn, H. 1974. The development of the populations of gazelles in Israel and their behavioral adaptations. Pages 722–743 in V. Geist and F. Walther, editors. The behaviour of ungulates and its relation to management. IUCN Publications Number 24. Morges, Switzerland. Moody, A. L., A. I. Houston, and J. M. McNamara. 1996. Ideal free distributions under predation risk. Behavioral Ecology and Sociobiology 38:131–143. Paveri-Fontana, S. L., and S. Focardi. 1994. A theoretical study of the sociobiology of ungulates. II. A dynamics programming study of the stochastic formulation. Theoretical Population Biology 46:279–299. Phillips, G. E., and A. W. Alldredge. 2000. Reproductive success of elk following disturbance by human during calving season. Journal of Wildlife Management 64:521–530. Roberts, G. 1996. Why individual vigilance declines as group size increases. Animal Behavior 51:1077–1086.
