Benefits and costs of resident males to females in white-faced capuchins Cebus capucinus.код для вставкиСкачать
American Journal of Primatology 32235-248 (1994) RESEARCH ARTICLES Benefits and Costs of Resident Males to Females in White- Faced Capuchins, Cebus capucinus LISA M. ROSE Department of Anthropology, University of Alberta, Edmonton, Alberta, Canada Some benefits and costs of resident males to females are examined in white-faced capuchins (Cebus capucinus) at Santa Rosa National Park, Costa Rica. A total of 380 hours of focal data were collected on adults in two groups, between January and July 1991. The results of this study suggest that for females, males provide some greater benefits, and impose some higher costs than do other females. Males are more vigilant than females, and are somewhat more successful in detecting predators. To the extent that predator protection is a major benefit of group living, this benefit seems to derive more from males than from females. Increased contest competition is the major cost of group living, and the study suggests that females bear a higher proportion of this cost than males. More foraging related agonism occurs between males and females than between females, more aggression occurs between than within sexes, and female foraging success is negatively associated with agonistic interactions involving males. However, female foraging success is negatively affected by the proximity of other females, and not by the proximity of males. Differences in the distribution of male benefits and costs according to female dominance rank are suggested. o 1994 Wiley-Liss, Inc. Key words: Cebus capucinus, sex differences, vigilance, competition INTRODUCTION Female reproductive strategies are considered to be the predominant factor shaping primate social systems, since male strategies depend largely on the distribution and behavior of females [Emlen & Oring, 1977; Wrangham, 1980; Mitchell et al., 19911. However, the presence of resident males within a social group provides several benefits for females. These include male participation in group defense against predators, which decreases the probability of mortality for females and infants, and the exclusion of non-group conspecifics, which contributes indirectly to female reproductive success by maintaining or increasing a group’s access to resources [Robinson, 1988; van Schaik, 1989; O’Brien, 19911. In addition, male Received for publication July 2, 1993; revision accepted October 18, 1993. Address reprint requests to Lisa M. Rose, Department of Anthropology,WashingtonUniversity, Campus Box 1114, One Brookings Drive, St. Louis, MO 63130-4899. 0 1994 Wiley-Liss, Inc. 236 I Rose vigilance may provide protection for females and their infants, allowing them more time for foraging and social activity. Males also may contribute to infant care by carrying, grooming, or “babysitting” infants, and providing protection from conspecifics [Altmann, 1980; Izawa, 19801. Concomitantly, the addition of males to a group imposes costs on females, primarily by increasing feeding competition. Individual success in contest competition is strongly influenced by social factors, especially dominance rank and aggressive behavior [Janson, 1985; 1990al. In many primate species, males are dominant over females, and ma.y obtain a disproportionate share of food resources through their greater success in contest competition. This study examines particular short-term benefits and costs of resident males to females in two groups of white-faced capuchins, Cebus capucinus. These arboreal neotropical primates live in multi-male, multi-female groups averaging about 15 individuals [Fedigan et al., 1985; Massey, 19871. Most groups have well-defined home ranges, and while overlaps do occur, a t least some boundaries are defended [Oppenheimer, 1982; Buckley, 19831. Females generally remain and breed in their natal groups, whereas most males migrate to other groups prior to maturity [Robinson & Janson, 19871. Males are 25-35% larger than females and are individually dominant over them, although the alpha female ranks immediately below the alpha male in some groups [Fedigan, 19931. HYPOTHESES AND PREDICTIONS I: For females, the benefits made available by males within a group exceed the benefits made available by existing female group members. In this section, I compare the extent to which males and females respectively provide particular benefits for the females within a social group. Predictions associated with this hypothesis are: 1)Males are more vigilant than females, thereby relieving requirements for female vigilance and increasing the likelihood of predator or conspecific group detection. 2) Males are more active than females in detecting and confronting predators, thereby playing a greater role than females in predator protection. 3) Males are more active and aggressive than females in intergroup encounters, thereby playing a greater role in intergroup competition. II: For females, the costs imposed by males within a group exceed the costs imposed by existing female group members. In this section, I compare the extent to which males and females respectively impose particular costs on females within a social group. Predictions associated with this hypothesis are: 1) Females engage in more agonistic interactions with males than with other females, especially in a foraging context, suggesting greater contest competition between females and males. A counter-prediction is that agonism reflects patterns of proximity between and within the sexes. 2) Males tend to direct aggression toward females, while females direct submissive signals toward males, suggesting that females are disadvantaged in agonistic interaction with males. 3) Female foraging is more often interrupted by males than by females. 4) Female foraging success decreases with increased time spent in proximity to males, suggesting that the presence of males has a negative impact on female foraging. A counter prediction is that foraging success is similarly reduced by proximity to others in all sex combinations. 5) Female foraging success decreases with increased agonism involving males, suggesting that male agonism has a negative impact on female foraging. A counter-prediction is that foraging success is similarly reduced by agonism in all sex combinations. The two hypotheses are not mutually exclusive, and may be independently accepted or rejected. Benefits and Costs of Males I 237 METHODS Study Site and Groups Santa Rosa National Park is situated near the Pacific coast of Costa Rica, about 35 km northwest of Liberia, Guanacaste. Santa Rosa covers approximately 10,800 ha of dry tropical forest, semi-evergreen forest, and reclaimed pasture in varying stages of secondary succession. Potential predators on capuchins at Santa Rosa include constricting snakes, felids, tayras, and raptors [Freese, 1983; Chapman, 19861. The study focused on two white-faced capuchin groups occupying nonoverlapping home ranges. Group Los Valles (LV) included 3-4 adult males, 4-5 adult females, 2-4 immatures, and 4-6 infants. Group Cerco de Pietra (CP) included 1-3 adult males, 4 adult females, 4 immatures, and 3-4 infants. Both groups were habituated to human observers. Visibility varied throughout the two ranges, but observation distances of five to ten metres were common. Individuals were identified by size, variation in brow color and length, and facial characteristics. Dominance hierarchies were constructed for each sex from the direction of aggression and submission within dyads. Data Collection and Analysis Preliminary observations for this study were made in May-July 1990 and January 1991. Intensive behavioral sampling of adults was conducted from February to July 1991. I collected 380 hours of focal data in the form of ten-minute continuous-time sessions [Altmann, 19741, and additional ad libitum data on comparatively rare events such as predator mobbing and intergroup encounters. Data were collected in alternating ten-day blocks for each group. Given the difficulty of locating particular group members in this arboreal species, it was not practical to follow a rigid sampling regime. I attempted t o sample each focal subject within a group before beginning a new round of observations, and kept a continuous record of the number of samples obtained for each individual to ensure that sampling was evenly distributed. If a focal subject was lost from view for more than 90 seconds, the session was ended and the data discarded. The nearest three neighbors within ten metres of the focal animal were noted immediately before and after each session. Agonistic behaviors were scored as “directed” or “received,” and other participants noted. Most behavioral categories were standard ethogram units [see Rose, 1992 for full description]. Vigilance behavior (SCAN) occurred when an animal remained stationary and alert, gazing beyond the immediate vegetation. ALARM calls [GYRRAHS; Boinski, 19931 were included in the analyses only if a potential predator was subsequently seen by the observer, or if the call elicited a response from other group members. MOBBINGS involved all or most group members gathering near and repeatedly threatening a potential predator, typically with repeated barking vocalizations, branch shaking and breaking, and openmouthed threats [Oppenheimer, 19681. AVOID was scored if an individual clearly moved away from an approaching group member, and was typically preceded by slight body tension and rapid glances toward the approaching individual. Since an AVOID was only recorded if I was able to see the associated approach, this category may be somewhat under-represented in the data. Vigilance behavior was expressed as a proportion of observation time for each focal subject. The proportions were transformed using the arcsine method, and tested for sex and group differences using a two-way analysis of variance. Significance was set at the P < 0.05 level. Hourly rates of agonism involving males and females respectively, were calculated for each individual, and divided by the num- 238 I Rose ber of potential partners available. Since some males were not present for the entire study period, the number of potential partners in male-female and malemale interactions reflected the proportion of focal samples for which each male was available. Hourly rates of directed aggression and submission were similarly calculated for all sex combinations. A Wilcoxon-Mann-Whitney test [Siegel & Castellan, 19881 was used to examine the adjusted agonism rates for intergroup differences. Wilcoxon matched-pairs signed-rank tests [Siegel & Castellan, 19881 were used to compare respective interaction rates with males and females for each sex (female interactions with males versus females; male interactions with males versus females). Wilcoxon-Mann-Whitney tests were used to compare male-male and female-female interaction rates, and male-female versus female-male rates of aggression and submission. Individual mean hourly rates of foraging interruptions were calculated from frequencies of supplantation and avoidance during feeding, and subjected to Wilcoxon tests (interrupts by males and females respectively). Foraging success was expressed as the percentage of foraging time spent feeding [Janson, 1990bl. Rates of male and female proximity were calculated from scans made at the start and end of each focal session. Female proximity was calculated as the total score for females observed within ten metres of the focal animal, divided by the number of samples obtained for the focal animal and by the number of possible female interactants. Male proximity was similarly calculated, allowing for the factor of male availability. A Spearman’s rank order correlation test [Siegel & Castellan, 19881was used to test the relationships between proximity, agonism, and foraging success. RESULTS I: Male Benefits to Females 1. Vigilance behavior. As predicted, males were more vigilant than females. On average, males devoted 8.0% (SE 0.80) of their time to vigilance behavior (SCAN), significantly more than the 3.2%(SE 0.17) spent by females (F = 42.47, P < =0.001). No significant intergroup difference was detected (F = 1.87, P = 0.199). The alpha male was the most vigilant individual in each group. 2. Predator detection and encounters. Males tended to give more confirmed predator alarms than females per sample period (Table I), but there were insufficient data for statistical analysis. I was able to discern the initial caller in two mobbing situations; in both cases, the CP alpha male gave the initial alarm. I observed a total of six confirmed snake mobbings (three involving boa constrictors) and several mobbings in which I was unable to confirm the target’s identity. Typically, the entire group participated in mobbings. Adult males typically approached the predator most closely, and were more boisterous and more persistent in threatening and following the predator than females. 3. Intergroup encounters. Males were involved in slightly more agonistic intergroup encounters than females. However, I observed only six cases, all involving the LV group and a small neighboring group in areas of range overlap. Three episodes involved only males, one primarily females, and two included both sexes. Contrary to what was predicted, females involved in intergroup encounters appeared to be more aggressive than males. I observed several females fighting, whereas male encounters mainly consisted of prolonged threats and chases. However, males were more persistent than females, and tended to patrol the area, scanning intently, for up to 30 min following an actual encounter. Aggression during intergroup encounters occurred almost exclusively within sex classes. Benefits and Costs of Males I 239 TABLE I. Confirmed Predator Alarms by Males and Females in Each Group, Including Focal and ad lib Observations Snake Raptor Coyote Unknown Total Per Capita" 2 1 - 1 4 1.14 1 2 - - 3 0.75 4 2 - 1 7 4.22 1 1 3 2 7 1.75 6 3 0 2 11 2.15 2 3 3 3 10 1.25 LV males (n = 4) LV females (n = 4) CP males (n = 3) CP females (n = 4) Total males (n = 7) Total females (n = 8) "Total alarms by each sex divided by number of individuals of that sex. For males, reflects percentage of total observation time that each male was present in group. 11: Male Costs to Females 1. Agonism between and within sexes. As predicted, females were involved in more agonistic interactions with males than with other females, both in total (Wilcoxon T + = 34, n = 8, P = 0.012) and during foraging (T+ = 36, n = 8, P = 0.004). Males tended t o have more agonistic interactions with females than with other males, but the difference was not significant for either total agonism (T = 21, n = 7, P = 0.148) or foraging-related agonism (T+ = 17.5, n = 7, P = 0.344). More agonism occurred in group CP than in group LV (Wilcoxon-Mann-Whitney Wx = 40, m = 7, n = 8, P = 0.0361, but the pattern of greater agonism between sexes is consistent in both groups (Fig. la,b). Patterns of agonism did not reflect patterns of proximity in either group (Fig. 2). In both groups, females had other females in proximity more often than males (Wilcoxon T + = 31, n = 8, P = 0.039).However, males had females in proximity more often than other males (T+ = 26, n = 7, P = 0.0231, and I therefore examined the relationship between individual proximity and agonism rates. Correlations were non-significant for both males (proximity of females and female agonism: rho = -0.500; proximity of males and male agonism, rho = 0.696) and females (proximity of females and female agonism: rho = -0.258; proximity of males and male agonism: rho = 0.09). 2. Direction of aggressive and submissive signals. There was a tendency for males to direct more aggression toward females than females directed toward males in group LV (Fig. 3a), but male to female aggression did not significantly exceed female to male aggression in either group (LV: Wilcoxon-Mann-Whitney Wx = 15, m = 4, n = 4, P = 0.243; CP: Wx = 11, m = 3, n = 4, P = 0.314). The greater proportion of female to male aggression in group CP was primarily due to frequent aggression by one female. Aggression between males was more common than aggression between females in group LV (Wx = 11, m = 4, n = 4, P = 0.0291, but not in group CP (Wx = 9, m = 3, n = 4, P = 0.200). The greater proportion of female-female aggression in group CP was again largely due to one female, and the absence of any aggressive interactions between two LV females. In both + 240 I Rose 0.30 5 0.25 '0 L b s E .E 0.20 0.15 0 P -5 2. 0.10 r 0 4 E 0.05 0.00 Group LV Group CP (b) 0.20 a Female-male Fern-fern s 2 0.15 fl Male-male .-E 0 P 2 0.10 a T z 5 P 0.05 0.00 Group LV Group CP Fig. 1. Distribution of (a) agonism and (b)foraging-related agonism between and within sex classes, expressed as mean hourly rate (and SE)per dyad. Rates adjusted to reflect partner availability. LV: n = 4 females, 4 males; CP: n = 4 females, 3 males. groups, more aggression occurred between sexes than within sexes (Fig. 3a). Females directed more aggression to males than to females (Wilcoxon T + = 27, n = 8, P = 0.016),and males directed more aggression to females than to males (T+ = 33, n = 7 P = 0.02). Males rarely injured females, but a male in group CP killed a two-day-old infant shortly after rising from beta to alpha position in the male dominance hierarchy. In both groups, females directed more submissive signals to males than males directed to females (Fig. 3b; Wilcoxon-Mann-Whitney Wx = 28, m = 7, n = 8, P = 0.002). The few submissive signals directed by males to females (n = 5) were from low ranking males toward an alpha female. All females directed more sub- Benefits and Costs of Males / 241 0.30 - Male-Female FernaleFernale P 0” 0.25 k - T Male-Male T 0.00 Group LV Group CP Fig. 2. Proximity between and within sex classes, expressed a s mean rate (and SE)per sample per dyad. Rates adjusted to reflect partner availability. LV n = 4 females, 4 males; CP: n = 4 females, 3 males. missive signals toward males than toward other females (Wilcoxon T + = 36, n = 8, P = 0.004). Submissive signals within sexes occurred too rarely to permit statistical analysis, but the number of submissive signals between females (n = 17) exceeded those between males (n = 3). All observed cases were directed by low ranking individuals to high ranking individuals. 3. Foraging interruptions. As predicted, female foraging bouts were more often interrupted by males than by other females (T+ = 36, n = 8, P = 0.004). Interruptions by males were broadly distributed, with the alpha female in each group having the fewest interruptions. Only low ranking females had their foraging interrupted by other females. Interruptions to male foraging bouts were too few (n = 7) to permit statistical analysis. In three cases, low ranking males were interrupted by a higher ranking male, in three cases, low ranking males were interrupted by an alpha female, and in one case, a male was supplanted from a small fruit tree by two mid-ranking females. 4. Proximity of others and foraging success. Contrary to what was predicted, there was no significant relationship between female foraging success and male proximity (rho = -0.167). However, female foraging success was negatively correlated with female proximity (rho = -0.762, n = 8, P < 0.05, two-tailed). There was also a tendency for male foraging success to decline with increased proximity of females, but this did not reach statistical significance (rho = -0.678). There was no significant relationship between male foraging success and proximity of other males (rho = 0.143). 5. Agonism involving males and female foraging success. As predicted, female foraging success decreased with increased foraging-related agonism involving males (Fig. 4; rho = -0.714, n = 8, P < 0.10, two-tailed). Female foraging success was not significantly correlated with foraging-related agonism involving other females (rho = -0.077). Male foraging success was not significantly correlated with agonism involving either females (rho = 0.473) or other males (rho = -0.571). The females with the highest foraging success were the highest and lowest ranked female in each group (Fig. 4). 242 I Rose (a) 0.20 MaletoFern 0.15 c 0" sm E .El -2 . M 2 .f 0.10 J=M 0.05 0.00 Group LV (b) 0 0.20 - Group CP FerntoMale MaletoFern Fern to Fern 0" sg E .a -h m ' 0.15 0 8 .$ 5g J = M 5 0.10 M 0.05 0.00 Group LV Group CP Fig. 3. Distribution of (a) aggressive and (b)submissive signals directed between and within sex classes, expressed as mean hourly rate (and SE) per dyad. Rates adjusted to reflect partner availability. LV: n = 4 females, 4 males. CP: n = 4 females, 3 males. DISCUSSION Male Benefits to Females This study suggests that males afford greater benefits to females than do other females in the form of vigilant behavior, with qualitative trends toward greater predator detection and defense. Since predation risk may be the primary pressure selecting for group living in primates [van Schaik, 1983; Terborgh & Janson, 1986; Mitchell et al., 19911, these results suggest that for C. capucinus females, a major benefit of group living derives largely from resident males. Comparatively greater vigilance by males has been reported for capuchins and other primate species [Fedigan, 1993; Fragaszy, 1986,1990; de Ruiter, 1986; Robinson, 1988; van Schaik & van Noordwijk, 1989; Gautier-Hion, 1980; Cheney & Seyfarth, 1981; Boinski, 1988aI. It cannot be assumed that male vigilance is directed solely (or even pri- Benefits and Costs of Males I 243 0 LVFemales CPfemales m 2 03 0 2 4 0 0. 1 1 72 74 76 78 80 Female Foraging success (% of foraging time spent feeding) 82 Fig. 4. Relationship between foraging-related agonism (hourly rate per female-male dyad, adjusted for partner availability) and female foraging success. n = 8 females; numbers indicate female dominance rank. Rho = -0.714, P < 0.05, two-tailed test. marily) toward predator detection, since vigilance can also serve a social function [Caine & Marra, 19881 or be directed toward conspecific groups [Baldellou & Henzi, 19921. The high level of vigilance by alpha males, and the tendency for males to focus on extragroup males during intergroup encounters suggest that male-male competition is a significant factor influencing male vigilance in the study groups. The object of male vigilance in Santa Rosa capuchins is currently under investigation [Rose & Fedigan, in press]. However, as Baldellou and Henzi  have noted, the intent of male vigilance is irrelevant from a female’s perspective, provided that it results in her receiving warning of potential dangers. Since the samples of predator and intergroup encounters are small and data are primarily qualitative, the findings in the following sections are tentative. However, the tendency for more vigilant individuals to be more successful in detecting predators is consistent with previous findings for other capuchin species [van Schaik & van Noordwijk, 19891. Males, particularly the CP alpha male, performed better than females in detecting snakes. Since males spend considerably more time than females on and near the ground [Gebo, 1992; Rose, 19941, their success in snake detection may reflect differential substrate use as well as higher levels of vigilance. Constricting snakes are a confirmed predator on young capuchins at the study site [Chapman, 19861, and the contribution of males in detecting them is thus likely to be significant. The persistence of males in pursuing and harassing large snakes may provide additional warning and protection for females and their infants. Male white-faced capuchins have been reported to kill a venomous snake by throwing branches at it [Boinski, 1988bl. Few intergroup encounters were observed during the study period, and the tendency for males to be more active than females is only weakly and qualitatively supported. The rate of aggressive intergroup encounters was unusually low for this particular site, perhaps in part because the alpha (and only) male in the nearest group overlapping the LV range had previously been an LV group member. In 244 I Rose previous years, such encounters have been recorded far more often, and primarily involved the males of each group forming opposing lines and repeatedly “bluff charging” toward each other, until one group retreated and was routed (L.M. Fedigan, pers. comm.). Long-term data suggest that females may benefit from exclusion of unfamiliar males by resident males. A number of females and infants have disappeared following incursions by immigrant males, and one female and three infant deaths were confirmed during a male takeover of CP group in 1993 (L.M. Fedigan & K. MacKinnon, pers. comm.). Male Costs to Females The results of this study suggest that resident males impose a greater cost on females than do other females in the form of agonistic interactions. Rates of agonism in both study groups were low (334 behaviors in 377 h), but over 70% of adult agonistic interactions were between males and females. Aggressive signals were more common than submissive signals because aggressive signals frequently elicited an aggressive response, especially between high ranking or mid-ranking individuals. Most agonistic exchanges consisted of open-mouthed threats. More aggression occurred between sexes than within sexes, but aggression was not unidirectional, suggesting that females are able to successfully counter male aggression in many cases, particularly if a female has a high rank. However, submission was predominantly directed by females toward males, suggesting that females are disadvantaged in agonistic interactions. Almost 75% of adult agonism occurred in a foraging context. Agonism between males and females occurred three times more often during foraging than at other times, whereas agonism among females was equally as likely to occur during foraging as at other times. This suggests that agonism between the sexes was primarily associated with feeding competition. Agonistic interactions with males adversely affected female foraging success. One finding was that females often avoided males during foraging, such that an agonistic signal but no aggression was recorded. Supplantations were less common than avoidance, especially between males and low ranking females, suggesting that these females may reduce the risk of aggression from a male by removing themselves from his vicinity. As avoidance and supplantation result in similar loss of feeding time and access to feeding sites, it is more appropriate to consider foraging success in terms of total agonistic interaction, rather than simply aggression received. Janson 11985, 1990al identified aggression received from the alpha male as the most significant factor reducing female foraging success in Cebus apella. However, in these C. capucinus groups, the alpha male was not notably more aggressive toward females than other males. Individual differences in behavior did affect patterns of aggression within the two groups. For example, the aggressive behavior of the beta female inflated both female-male and female-female aggression rates in group CP. However, the higher overall rate of agonism in group CP may have been more broadly associated with a smaller range and reduced food abundance compared with group LV [Rose, 19941, resulting in increased feeding competition. Feeding competition is recognized as the primary cost of group living [Janson & van Schaik, 19881. This study suggests that females bear a higher proportion of this cost than males, since female foraging success is negatively affected by agonistic interaction with males, while male foraging success is not. Agonistic interactions with females did not significantly affect female or male foraging success. However, female foraging success (and, to some extent, male foraging success) was negatively affected by the proximity of other females. This suggests that nonagonstic factors also affect foraging success in C. capucinus social groups, and that Benefits and Costs of Males / 245 these factors are predominantly associated with females. Subtle effects of female dominance, greater vigilance by males in proximity to females, and the effect of infants on adult foraging behavior are among the possible factors that warrant further investigation. Males in both study groups were typically tolerant and protective of infants, and considerable infant care by C . capucinus males has been observed at other study sites ( S . Perry, pers. comm.). However, the killing of an infant by a male during this study confirms that infanticide occurs in this species, and thus represents a potential cost associated with male group members. The infanticide occurred shortly after a change in male dominance ranks, but the relationship of the male to the infant (born to the lowest-ranked female) was unknown. A similar incident has been reported in Cebus olivaceus [Valderrama et al., 1990, case #2]. O’Brien  suggests that Cebus olivaceus females preferentially associate and mate with the alpha male as a strategy to reduce the risk of infanticide, and that high ranking females receive greater benefits than low ranking females by “monopolizing” the alpha male. Distribution of Benefits and Costs Among Females There was some evidence that the benefits and costs considered in this study were not equally distributed among the females within each group. High-ranking females were less likely to avoid or to be supplanted by other individuals than low-ranking females. As the alpha female in each group ranked immediately below the alpha male and above other males, she was probably less disadvantaged than other females in agonistic interactions with males. On the few occasions that a male avoided a female, the response was directed toward an alpha female. The alpha female in each group had a strong alliance with the alpha male, and was able to enlist his support during agonistic interactions and group movement [Rose, 19921. Female success in leading group movement was positively correlated with dominance rank [Boinksi, 19931. Within each group, the females with highest foraging success were the highest and lowest ranked. High ranking females tended to have high proximity to both females and males, while low ranking females were more peripheral [Rose, 19921. The highest and lowest-ranked females shared the lowest rate of agonistic interactions with males, suggesting that there may be two strategies through which a female can improve her foraging success: i) attain high dominance rank and form strong male bonds, or ii) remain low-ranking and avoid agonistic encounters with males. However, it is possible that by foraging in less central areas in the group, low ranking females may forfeit much of the benefit of male vigilance. High ranking females who forage nearer to males, especially the highly vigilant alpha male, may benefit more from male vigilance and predator detection. Balance of Male Benefits and Costs Primate social systems are often portrayed as a balance between conflict and cooperation [e.g., Walters & Seyfarth, 1987; O’Brien, 19911. But is the balance an equal one, or are the options for females more constrained than the options for males? For example, if the costs of resident males outweigh the benefits that they provide, could females choose to exclude males from social groups? In this study, females occasionally formed successful coalitions against a single male, but repeated confrontations would be energetically costly and physically risky as males are larger and stronger than females, and have larger canines. Continual vigilance against invading males would also be costly in terms of energy expenditure and lost foraging or rest time. Thus, excluding males may not be a viable option for C. 246 I Rose capucinus females, and a mixed-sex social system may persist even if there are some disadvantages for females. Females may compromise by following strategies that provide the best balance between the costs of male success in feeding competition and the benefits of male predator protection, in accordance with their rank in the female dominance hierarchy. CONCLUSIONS 1. Male white-faced capuchins are more vigilant than females, and somewhat more successful in detecting potential predators. 2. Both males and females are active in intergroup encounters with aggression occurring almost exclusively within sexes. 3. More agonism occurs between than within sexes, especially while foraging, and female foraging is interrupted more often by males than by females. 4. Female foraging success is negatively correlated with proximity to other females, but not with proximity to males. 5. Female foraging success is negatively correlated with agonism involving males, but not with agonism involving other females. 6. Males afford some greater benefits for females than do other females, but also impose some greater costs. ACKNOWLEDGMENTS I thank Linda Marie Fedigan for her support and advice throughout this project, and the Area de Conservacion Guanacaste for permission to work a t Santa Rosa. I am grateful to Sue Boinski for sharing her knowledge and observations of vocalizations, spatial position, and group movement. Marc Koehn gave generously of his time and expertise in writing the computer programme PRIMA 1.1 for data entry, and Chuck Humphries assisted with statistical advice. Sue Boinski, Linda Fedigan, Nancy Lovell, Rick Martin, Jan Murie, and three anonymous reviewers provided helpful comments on the manuscript. My research was funded by a postmaduate scholarshir, from the Natural Sciences and Engineering Research Council of Canada (NSERCC). REFERENCES Altmann, J. 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