Intergroup Encounters in Grey-Cheeked Mangabeys (Lophocebus albigena) and Redtail Monkeys (Cercopithecus ascanius): Form and Function Michelle Brown Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Graduate School of Arts and Sciences COLUMBIA UNIVERSITY 2011 © 2011 Michelle Brown All rights reserved ABSTRACT Intergroup Encounters in Grey-Cheeked Mangabeys (Lophocebus albigena) and Redtail Monkeys (Cercopithecus ascanius): Form and Function Michelle Brown Across species and populations, encounters between neighboring social groups take a variety of forms. In particular, intergroup encounters (IGEs) may or may not be aggressive and may include the participation of males and/or females. The proximate causes of aggressive participation by each sex, particularly among primates, is generally thought to be the availability of mates and food. However, existing hypotheses of resource defense have rarely been explicitly tested through identification of the proximate causes of male and female aggression. In this dissertation, I sought to test the existing hypotheses by determining whether female food defense, male food defense, and male mate defense occur in grey-cheeked mangabeys (Lophocebus albigena) and redtail monkeys (Cercopithecus ascanius). With a team of field assistants, I observed six mangabey groups for 15 months and four redtail groups for 12 months at the Ngogo site in Kibale National Park, Uganda. We observed naturally-occurring IGEs in both species, simulated IGEs among mangabey groups using playback experiments, and measured the availability of food resources in botanical plots. I evaluated multiple aspects of intergroup relations, including initiation of encounters, occurrence of intense aggression, encounter outcomes, overall encounter rates, and the effect of neighbors’ long-distance calls on group movements. For each IGE aspect, I determined the effects of group size and resource value. I found strong evidence for female food defense by redtails and male food defense by both species, weak evidence of male mate defense by redtails and no evidence for mangabeys, and no evidence of female food defense by mangabeys. In addition, the specific conditions under which food defense is expected to occur in primates were appropriate for male mangabeys, but not for female or male redtails. This pattern of results indicates that existing hypotheses cannot accurately predict which populations will exhibit food or mate defense by males or females, or the specific social and ecological conditions that elicit defense. I also found that mangabeys exhibited two types of IGE: whole group encounters, where the majority of two groups were in visual contact, and subgroup encounters, where one or a few individuals left their group and interacted aggressively with a neighboring group. Whereas whole group IGEs appeared to function as defense of specific feeding sites, subgroup IGEs did not; instead, they appeared to be a means of defending the core of the home range. Compared to earlier studies, the mangabey groups in this study exhibited higher encounter rates and more pronounced aggression. Higher group densities and more intense feeding competition have given rise to a dramatically different pattern of mangabey intergroup relations. This study demonstrates the importance of considering multiple IGE aspects, hypotheses, and food characteristics when evaluating the role of intergroup relations in the lives of social animals. TABLE OF CONTENTS List of Tables and Figures vi Acknowledgements xiii Dedication xviii Preface xix Chapter 1: Intergroup Encounters in Group-Living Birds and Mammals, with a Focus on Non-Human Primates Introduction 1 I. Defining intergroup encounters 5 II. General principles 7 II. A. Functions 7 II. B. Behaviors 10 II. C. Determinants of success 26 II. D. Spatial patterns 30 II. E. Factors modifying spacing systems 31 III. Differences among primates, other mammals, and birds 35 IV. A model of primate intergroup encounters 37 IV. A. Hypotheses 37 IV. B. Evaluating the model 44 Future directions 48 References 49 Tables and figures 63 i Chapter 2: Approach and avoidance among grey-cheeked mangabey (Lophocebus albigena) groups Abstract 72 Introduction 73 Methods 78 Data collection 78 Data analysis: long-range encounters 85 Data analysis: short-range encounters 91 Results 95 Habitat quality 95 Long-range encounters 95 Short-range encounters 98 Discussion 104 Long-range encounters 105 Short-range encounters 109 General conclusions 117 References 119 Tables and figures 125 ii Chapter 3: Proximate causes of male and female aggression during intergroup encounters in grey-cheeked mangabeys (Lophocebus albigena) and redtail monkeys (Cercopithecus ascanius) Abstract 167 Introduction 168 Methods 172 Results 184 Discussion 191 References 204 Tables and figures 211 Chapter 4: The effects of between-group contest competition on grey-cheeked mangabeys (Lophocebus albigena) and redtail monkeys (Cercopithecus ascanius) Abstract 232 Introduction 233 Methods 237 Results 245 Discussion 249 References 256 Tables and figures 261 iii Chapter 5: Intergroup encounter rates in redtail monkeys (Cercopithecus ascanius) and grey- cheeked mangabeys (Lophocebus albigena) Abstract 274 Introduction 275 Methods 279 Results 286 Discussion 290 References 297 Tables and figures 301 Chapter 6: An integrated approach to intergroup encounters Introduction 319 Review of results 321 Mangabey patterns 322 Redtail patterns 328 Future directions for research on between-group contests 329 Economics of food defense 329 Evolutionary game theory 333 Generalizability of the results 335 Conclusions 337 References 339 Tables and figures 344 iv Appendix 1: Top 20 diet species for three Kibale mangabey studies: (A) 348 this study, (B) Barrett (1995), and (C) Waser (1977). Appendix 2: Cumulative home range area for each study group, 351 calculated using the “data area curve” function in Biotas. Appendix 3: Spearman rank correlations among food-related variables. 357 Appendix 4: Measuring food abundance: the disconnect between 361 phenology census results and primate feeding behavior. Appendix 5: Frequencies of female and male participation in aggressive 373 intergroup encounters in relation to home range defendability. Appendix 6: Maps of four redtail and seven mangabey ranges, as well as 384 encounter outcomes. v LIST OF TABLES AND FIGURES CHAPTER 1 Figure 1. The components of intergroup encounters. 63 Figure 2. A hypothetical relationship between energetic balance and the 64 frequency of aggressive intergroup encounters. Figure 3. A spectrum of spacing behaviors, ranging from site-independent to 65 -dependent dominance. Figure 4. A spectrum of spacing behaviors in relation to population density. 66 Table 1. Combinations of variable states necessary for each function of IGE 67 participation. Table 2. Predicted and observed sex-specific functions of participation in 68 IGEs for some group-living primates. CHAPTER 2 Table 1. The observation period and hours per group and the composition 125 of each group. Table 2. Second generation models considered in the selection process, 126 each of which includes the best control variables. Table 3. Comparison of the mangabey population density, number of food 127 tree stems, and food basal area in three mangabey studies in Kibale National Park, Uganda. Table 4. Number of whoop gobble bouts recorded in each home range 128 zone. Figure 1. Change in group movement at different intergroup distances after 129 a neighbor’s long-distance call. Figure 2. Change in group movement within core/exclusive and 130 periphery/shared areas after a neighbor’s long-distance call. Table 5. Pearson χ2 tests of the frequency of withdrawal across core 131 (exclusive) and periphery (shared) areas, per study group. vi Figure 3. Group movements in response to neighbors’ whoop-gobbles by six 132 Ngogo study groups in a high density population. Table 6. The number (and percentage) of post-call travel direction 133 responses, sorted by pre-call travel direction. Table 7. The best model of listener deflection angles (when the pre-call 134 travel direction was ‘toward’ the caller). Figure 4. Listener’s deflection angle as a function of the degree of intrusion 135 by the calling group into the listener’s home range. Figure 5. Listener’s deflection angle as a function of the number of adult 136 males in the group . Figure 6. Listener’s deflection angle as a function of the short term feeding 137 value of its location at the time of the call. Table 8. Control variables assessed during the first step of the model 138 selection process. Table 9. Models consisting of different combinations of important control 139 variables. Table 10. Models assessed during the final step of the model selection 140 process, containing the best control model and different food- related independent variables Table 11. The number of experimental playback trials conducted per group, 141 per condition. Table 12. The number of experimental playback trials per condition, pooled 142 across groups. Table 13. The number of IGEs per group, per condition. 143 Table 14. The number of IGEs per condition, pooled across groups. 144 Table 15. Wilcoxon-Mann-Whitney tests of the differences in the conditions 145 associated with naturally-occurring intergroup encounters (IGEs) and experimental playback trials (PBs). Table 16. Differences in social and ecological predictors (median and 146 interquartile range) across group movement responses in experimental