Sociality in Callithrix penicillata: II. Individual Strategies During Intergroup Encounters

In social animals, intergroup interactions, whether through agonistic and competitive behaviors or affiliative ones, can influence important parameters such as home range, territory sizes, and access to resources, which may directly affect both female and male fitness. We studied the intergroup interaction patterns of a wild group of black-tufted-ear marmosets (Callithrix penicillata) in central Brazil. Agonistic interactions occurred at low frequencies during intergroup encounters. The marmosets directed agonistic interactions without physical aggression primarily against same-sex individuals, suggesting that male and female aggression patterns are shaped by their sexual interests. However, females of the focal group also directed agonistic behavior toward extragroup males that attempted copulation. The marmosets appeared to use intergroup encounters to gather information about possible partners and extragroup reproductive opportunities. Intergroup sexual interactions occurred mainly in the form of copulations or attempted copulations by all adults, with the exception of the dominant female. Our results suggest that a possible reproductive strategy used by males is to attempt fertilization of extragroup females. Adult males copulated with the same extragroup female during several opportunities, which suggests sperm competition or the establishment of social bonds with neighboring females.     

The behavioral context of visual displays in common marmosets (Callithrix jacchus)

Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays. Am. J. Primatol. 75:1084–1095, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Neighbor effect: evidence of affiliative and agonistic social contagion in captive chimpanzees (Pan troglodytes)

Previous studies of captive chimpanzees have demonstrated the "neighbor effect," or social contagion, with respect to agonistic vocalizations and behaviors. The present study considers whether there is a relationship between behavior patterns in focal animals and the auditory signals of neighboring social groups. Using focal-group sampling, we collected 172.5 hr of data on 51 subjects (25 females and 26 males) housed in 10 social groups. We performed two-tailed Wilcoxon matched-pairs signed-rank tests to determine whether the relative frequency of the vocalizations (high vs. low) affected the behaviors. In keeping with past research, we found that agonistic noises and vocalizations from neighboring social groups had a significant effect on the rates of focal-group bluff displays, pant-hoots, and aggression (P<0.05). In addition, we also found significant relationships between grooming behavior and vocalizations in focal groups, and grooming vocalizations from neighboring groups (P<0.05). The results suggest that social contagion is not limited to aggressive behaviors, but also occurs for affiliative behavior patterns.     

Role of loud calls in brown howlers,Alouatta fusca

The loud calls of brown howler monkeys were studied during a year at the Santa Genebra Reserve, in southeastern Brazil. The study group emitted roars and barks on a total of 47 occasions, the majority of which (92%) were restricted to intergroup visual encounters. Loud calls were also elicited by the roars of distant groups (6%) and during intragroup agonistic interactions (2%). Intergroup visual encounters (n = 42) occurred predominantly in seldom used quadrats of the study group home range. In these instances, the loud calls were produced chiefly by the adult male alone (69% of cases), while the study group's two adult females joined the male in the remaining cases. Intergroup physical aggression, such as chase and displacement, was observed during 15 encounters (35% of cases). A dawn chorus does not occur in Santa Genebra—the loud calls were heard most frequently in mid-morning and again during mid-afternoon—and they were more abundant during the dry season, when the availability of food (new leaves) in the forest was lower. The data presented here provide some support for the hypothesis that roars of howler adult males are used in assessment of opponents, providing an alternative to energetically expensive chases and fights. However, given the relatively high rate of physical aggression observed during intergroup encounters, a result probably related to the high density of howlers and the consequent high frequency of intergroup encounters observed in this forest (0.7/day), ritualized aggression, in the form of loud calling, is apparently often insufficient to settle disputes. © 1995 Wiley-Liss, Inc.     

Feeding Competition and Agonistic Relationships Among Bwindi <Emphasis Type="Italic">Gorilla beringei</Emphasis>

Testing predictions of socioecological models, specifically that the types of feeding competition and social relationships female primates exhibit are strongly influenced by the distribution, density, and quality of food resources, requires studies of closely related populations of subjects living under different ecological conditions. I examined feeding competition and the resulting female social relationships in mountain gorillas (Gorilla beringei beringei) of Bwindi Impenetrable National Park, Uganda, which has ecological conditions distinctive from those where other gorilla populations live. I observed 1 group of gorillas for 29 mo to examine the proportion of time spent foraging on fruit, the relationship between patch size and occupancy patterns of fruit trees, and agonistic interactions. Patch occupancy time while foraging in fruit trees decreased with increasing number of gorillas in a tree and decreasing tree size, suggesting that fruit trees represent limiting patches and can lead to intragroup scramble competition. Gorillas exhibited higher levels of aggression while feeding on fruit versus other food resources, which indicates intragroup contest competition. I observed a linear dominance hierarchy with no bidirectionality via displacements, and a similar hierarchy via aggression, though a notable proportion of the dyads contained 2-way interactions. However, most aggression was of low intensity (vocalizations) and the recipient typically ignored it. Despite differences in ecological conditions and diet between the Virunga Volcanoes and Bwindi, agonistic relationships among females are largely similar in the 2 populations and are best characterized as dispersal individualistic.     

Sociality in <Emphasis Type="Italic">Callithrix penicillata</Emphasis>: I. Intragroup Male Profile

We analyzed the social interactions and behavior of adult males from a group of black-tufted-ear marmosets (Callithrix penicillata) to determine their roles and hierarchy in the group and how their behavior fits within the predictions of monogamic or polyandric mating systems in callitrichines. We monitored 1 group of marmosets from February to October 2005 in central Brazil. We conducted focal subject samples with 20 predetermined behaviors for adult and subadult males and registered all occurrences of agonistic behavior, affiliative behavior, copulations, and alarm vocalizations. Moreover, we recorded the height in the vegetation and proximity to other individuals by the focal subject. Males exhibited no clear dominance hierarchy based on either behavioral data or patterns of scent marking. Copulation and grooming patterns showed a social bond between 1 of the males and the dominant female, suggesting him as the group’s putative breeding male, with no apparent competition for the position. There was no difference regarding other behaviors— alarm vocalization, infant carrying, and play—or the use of different vegetation strata among the males, and no indication of a specific role by the putative breeding male or any other male in the group. The presence of multiple males in marmoset groups and the behavioral profile generated in the current study suggest a mating system compatible with monogamy with helpers-at-the-nest structure.     

Importance of cooperation and affiliation in the evolution of primate sociality

The idea that competition and aggression are central to an understanding of the origins of group‐living and sociality among human and nonhuman primates is the dominant theory in primatology today. Using this paradigm, researchers have focused their attention on competitive and aggressive behaviors, and have tended to overlook the importance of cooperative and affiliative behaviors. However, cooperative and affiliative behaviors are considerably more common than agonistic behaviors in all primate species. The current paradigm often fails to explain the context, function, and social tactics underlying affiliative and agonistic behavior. Here, we present data on a basic question of primate sociality: how much time do diurnal, group‐living primates spend in social behavior, and how much of this time is affiliative and agonistic? These data are derived from a survey of 81 studies, including 28 genera and 60 species. We find that group‐living prosimians, New World monkeys, Old World monkeys, and apes usually devote less than 10% of their activity budget to active social interactions. Further, rates of agonistic behaviors are extremely low, normally less than 1% of the activity budget. If the cost to the actors of affiliative behavior is low even if the rewards are low or extremely variable, we should expect affiliation and cooperation to be frequent. This is especially true under conditions in which individuals benefit from the collective environment of living in stable social groups. Am J Phys Anthropol 128:84–97, 2005. © 2005 Wiley‐Liss, Inc.     

The neighbor effect: Other groups influence intragroup agonistic behavior in captive chimpanzees

While intercommunity interactions are well documented in wild chimpanzees, the influence of neighboring captive groups on social behavior has not been investigated. This study examined the influence of vocalizations and noisy displays produced in neighboring groups (i.e., “neighbor vocalization”) on intragroup hooting, bluff displays, and agonistic behavior. Chimpanzees from two broadly differing housing conditions were selected in order to examine the effect of neighboring groups: “Wing Groups” (those living in indoor/outdoor pens with auditory access to large number of neighboring individuals) and “Building Groups” (those housed in one indoor building, able to hear the calls and noisy displays produced by a small number of neighboring individuals occupying the building). Data were collected on 58 adult and juvenile subjects living in social groups varying in size from two to 14 individuals. Observation sessions were divided into two categories depending on the level of neighbor vocalization. Wing Groups showed higher rates of hooting, bluff displays, and agonistic behavior against other group members when levels of neighbor vocalization were high. Building Groups showed the same pattern, with results for bluff displays reaching statistical significance. This effect was also found through an analysis of the time periods immediately surrounding incidents of neighbor vocalization: Hooting and bluff displays were significantly more common after than before neighbor vocalizations. In spite of variation between the two housing conditions with respect to overall levels of neighbor vocalization, degree of differences between the high and low vocalization levels, and methods of data collection, a consistent neighbor effect was detected. This effect is congruous with behavioral patterns observed in the wild, and is therefore considered an expression of species-typical behavior as opposed to an artifact of captivity. These results are relevant to captive management, and bear on the influence of housing condition on psychological well-being. © 1996 Wiley-Liss, Inc.     

Aggression and Reconciliation in Cebus capucinus

Most data relating to aggressive and conciliatory behaviors are from Old World primates. We recorded agonistic interactions and post-conflict behaviors in a group of 12 white-faced capuchins (Cebus capucinus). After a conflict, we followed the aggressee as the focal individual during a 10-min postconflict period. We also conducted matched-control observations on the same individual. Conflicts involving physical contact were significantly bidirectional, and conflicts without physical contact were preferably unidirectional. Reconciliation was not be demonstrated at the group level. However, reconciliation occurred in kin and non-kin male/female dyads: their conciliatory tendencies were 48.1% and 21.2%, respectively. White-faced capuchins reconciled mainly during the first minutes after the end of the conflict. In kin and non-kin male/female dyads, selective attraction occurred, and aggressors were more likely to initiate affiliative contacts than aggressees. Hold-bottom and mount while emitting loud vocalizations were the most characteristic behaviors of reconciliation. Possible links may exist between aggressive and conciliatory patterns and other social variables.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Intragroup and Intergroup Social Interactions in White-Handed Gibbons

One of the least studied aspects of the Hylobatidae is their social behavior. In the past, researchers have attributed this to a general lack of affiliative social interactions due to small group size and the hostile nature of intergroup encounters. Data collected on white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand, indicate that gibbons engage in higher rates of social behavior than had previously been appreciated. In addition to relatively high rates of intragroup social contact, gibbons engaged in social behavior, including play and grooming, with members of neighboring groups. These findings obligate a renewed consideration of the nature and function of territoriality in primates.     

Duration and outcome of intergroup conflict influences intragroup affiliative behaviour

Theoreticians have long suggested that the amount of intergroup conflict in which a group is involved could influence the level of cooperation or affiliation displayed by its members. Despite the prevalence of intergroup conflicts in many social animal species, however, few empirical studies have investigated this potential link. Here, I show that intragroup allopreening rates are highest in green woodhoopoe (Phoeniculus purpureus) groups that have the greatest involvement in intergroup conflict. One reason for this relationship is a post-conflict increase in allopreening, and I demonstrate for the first time that both conflict duration and outcome influence subsequent allopreening rates: group members allopreened more following long conflicts and those they lost compared with short conflicts and those they won, perhaps because the former are more stressful. The increase in affiliative behaviour was the result of more allopreening of subordinate helpers by the dominant breeding pair, which may be because the breeders are trying to encourage helpers to participate in future conflicts; relative group size influences conflict outcome and helpers contribute more to conflicts than do the breeding pair. These results emphasize that our understanding of cooperation and group dynamics can be enhanced by investigations of how intergroup interactions affect intragroup processes.     

Sibling Age and Intragroup Aggression in Captive Saguinus midas midas

Different species of Callitrichidae show a consistent pattern in intragroup aggression. Aggression is more frequent between same-sex individuals, with males and older siblings being more aggressive. These findings have been associated with reproductive competition and dispersal events. However, the few studies dealing with intragroup aggression have not fully explored the effects of food availability on aggression or the relationship between age and aggression. I observed 3 family groups of Saguinus midas for 50 weeks and recorded all occurrences of aggression. A total of 138 agonistic events occurred at an average of 1.16 aggressive acts/hour per group, and 52.2% of aggressive acts occurred during a food shortage condition, which accounted for about 12% of all meals in the groups. During the food shortage, aggression was significantly higher, which suggests that food competition promoted an increase in aggression levels. Aggression amongst siblings accounted for 65.2% of all aggressive acts. Aggression from brothers to sisters was significantly more frequent than aggression between brothers. Aggression rates were significantly different between age classes. Young siblings were significantly more aggressive toward old ones than the reverse. Age and aggression received followed a linear relationship, while age and aggression initiated tended to follow a curvilinear relationship. Higher rates of aggression in young siblings probably were prompted by puberty and associated hormonal changes.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Preparing for battle? Potential intergroup conflict promotes current intragroup affiliation

Groups of human soldiers increase their affiliative behaviour when moving into combat zones. Despite numerous other species also competing as groups, little is known about how potential intergroup conflict might influence current intragroup affiliative behaviour in non-human animals. Here, I show that allopreening (when one individual preens another) increases in groups of cooperatively breeding green woodhoopoes (Phoeniculus purpureus) when they enter areas where conflicts with neighbours are more likely. Self-preening, which is an indicator of stress in other species, did not increase in conflict areas, suggesting that the change in affiliative behaviour is not the simple consequence of greater stress. Instead, because it is the dominant breeding pair that increase their preening of subordinate helpers, it is possible that current affiliative behaviour is being exchanged for agonistic support in any intergroup conflicts that might ensue. These results are important for our understanding of group dynamics, cooperation and the evolution of sociality, but also bring to mind the intriguing possibilities of social contracts and future planning in birds.     

Aggression and social support predict long‐term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella)

Many nonhuman primates live in complex social groups in which they regularly encounter both social stressors such as aggression and social support such as that provided by long‐term affiliative relationships. Repeated exposure to social stressors may result in chronically elevated cortisol levels that can have deleterious physical effects such as impaired immune function, cardiovascular disease, and reduced brain function. In contrast, affiliative social relationships may act as a buffer, dampening the release of cortisol in response to acute and chronic stressors. Understanding how social stressors and social support predict cortisol levels is therefore essential to understanding how social situations relate to health and welfare. We studied this relationship in 16 socially housed captive brown capuchin monkeys (Cebus [Sapajus] apella) by comparing long‐term hair cortisol levels with behavioral measures of social stress (dominance rank, rank certainty, and amount of aggression received) and social support (amount of affiliation and centrality in the affiliative social network of the group). Dominance rank, rank certainty, amount of affiliation, and age were not significant predictors of long‐term cortisol levels in this population. Instead, long‐term cortisol levels were positively related to the amount of aggression received and negatively related to centrality in the affiliative social network of the group. This pattern may be attributed to the species’ socially tolerant dominance system and to the availability of social support across the dominance hierarchy.     

Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses

Marmosets, as do many other primates, live in forest environments, are group living and constantly at risk of predation. Retaining contact with one another is therefore a matter of survival. We ask here whether their contact calls (phee and twitter vocalizations) are in some way ordered acoustically by sex or age and whether the calls of older marmosets elicit different responses than those of younger marmosets. In our study, marmosets (2–14 years) were visually isolated from conspecifics and the vocal responses to each isolated caller by other marmosets in the colony were recorded. Vocal responses to phee calls largely consisted of phee calls and, less commonly, twitter calls. No differences between the responses to calls by males and females were apparent. However, we found a strong positive and significant correlation between the caller's age and the percentage of its phee calls receiving a phee response, and a significant negative correlation between the caller's age and the percentage of its phee calls receiving a twitter response. The older the marmoset, the more antiphonal calling occurred. Two‐syllable phee calls were emitted more often by older marmosets (10–14 years) than by younger ones (2–6 years). Hence, we have found age‐dependent differences in phee‐call production and a consistent change in the response received across the adult life‐span. This age‐dependent effect was independent of kinship relations. This is the first evidence that marmosets distinguish age by vocal parameters alone and make social decisions based on age. Am. J. Primatol. 71:165–170, 2009. © 2008 Wiley‐Liss, Inc.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

The Pair-Bond Formation and Its Role in the Stimulation of Reproductive Function in Female Common Marmosets (Callithrix jacchus)

The sociosexual relationship between male and female common marmosets (Callithrix jacchus) is characterized by pair-bond formation, which includes sexual and social interactions such as contact, huddling and allogrooming. The formation of heterosexual pairs in captivity sometimes is unsuccessful in terms of reproduction. We investigated the existence of a correlation between characteristics of sociosexual interaction of marmoset pairs and its role in stimulating reproductive function in females. We studied pair-bond formation during the first 10 weeks of pairing in eight unrelated heterosexual pairs of common marmosets (Callithrix jacchus) without prior sexual experience. In three of them, pregnancy occurred during the study period (group SR), and we compared the profile of their sociosexual interactions with that of the five other couples in which pregnancy was not registered (group NS) during that period. The results show differences between the two groups, related mainly to affiliative responses between male and female, with significantly higher levels of allogrooming and simultaneous piloerection in the SR group. Although we did not find significant differences in the frequency of mounting behavior between groups, their reproductive success was different, suggesting that some behavioral patterns related to cooperative interactions between the male and female could be expressing the pair-bond. These behaviors may be influencing the females' physiology and consequently successful reproduction in the species.