Squirrel monkey dominance and social behavior as related to group size and group structure

Adult male and female squirrel monkeys were tested in nonsocial adaptation and pairwise and triad social situations differing in sex composition. Social behaviors, nonsocial behaviors, and dominance hierarchies were observed during social testing. Dominance hierarchies were similar in groups differing in size and social structure. Nonsocial behaviors decreased in females and submissive animals paired with males or dominant monkeys. Aggressiveness between females decreased and the beginnings of coalitions between females were observed in the presence of a male. The social behavior patterns, but not dominance hierarchies, are consistent with behaviors observed in larger groups of squirrel monkeys.     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

Aggression with mixed age-sex groups of bolivian squirrel monkeys following single animal introductions and new group formations

The social organization of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is thought to be sexually segregated, with males and females forming separate social groups during the nonbreeding season. To investigate the influence of this social order on patterns of aggression, controlled single animal introductions within established groups and establishment of new groups were studied in a systematic manner. Behavioral observations were made using an all-occurrences technique to sample all agonistic interactions. In study I, 4 animals of each age-sex class (adult males and females, juvenile males and females) were introduced one at a time into 4 different social groups composed of 1 adult male and 8 to 10 adult females. Behavioral observations were made prior to and after the introductions. Newly introduced adult males received significantly more contact aggression than other age classes. Only the adult females increased aggression after the introduction of new animals. In study II, new social groups were formed and behavioral observations were made following formation. One group was formed from 7 pairs of familiar females and an unfamiliar adult male. This group had a high frequency of aggression during the first half hour, with contact aggression rising to peaks at 3 and 5 h. The second group consisted of 10 familiar females, 2 pairs of familiar females and an unfamiliar male. There was a significant peak in contact aggression 3 h into the observation.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

Proboscis monkey (Nasalis larvatus) social organization: Group structure

Proboscis monkey (Nasalis larvatus) social organization was studied at the Tanjung Puting National Park in Kalimantan Tengah, Indonesia, for 12 months. Data were collected on one-male groups and all-male groups by using scan sampling and event sampling while following groups. Evening census surveys were also conducted. Proboscis monkeys were found to follow the typical Asian colobine pattern of one-male social groups, with extra-group males forming all-male groups. These groups appear stable, with few changes in membership. One-male groups appear to be “female bonded”; adult females direct affiliative behaviors towards their offspring and other adult females, not towards the male. Nearest-neighbor data indicate some peripheralization of juvenile animals.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

Age related variation in male–male relationships in wild spider monkeys (Ateles geoffroyi yucatanensis)

In social organizations characterized by male philopatry, social relationships between males are argued to be the strongest. Little is known about the social relationships of philopatric male spider monkeys. To address this limitation, we investigated social relationships among individually recognized wild adult male spider monkeys from two well-habituated communities in the Yucatan Peninsula, Mexico, focusing on affiliative behaviors important in regulating male social relationships, including grooming, embracing, arm-wrapping, and grappling. We examined whether behaviors were reciprocated between male partners and whether age was a factor in how the behaviors were distributed or reciprocated, by examining differences between younger adult males (<10 years) and older adult males (≥14 years). Although we found evidence that affiliative behaviors were overall reciprocated between spider monkey adult males, there were pronounced differences in the interactions depending on their relative age. Reciprocation in grooming and embraces between same-age males suggests their relationships are valuable to both partners. Among different-age dyads, younger males gave more embraces than they received, were the initiators of grappling and arm-wrapped more often than with same-age males, suggesting relationships between younger and older males are more risky. This confirms that younger males are attracted to older males, probably because they value relationships with older males more than the reverse, but they are also at risk.     

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.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

Social compatibility in a newly formed all‐male group of white crowned mangabeys (Cercocebus atys lunulatus)

Surplus males in primate captive populations are a common problem for zoos. Some captive breeding programs promote all‐male groups as an adequate option to house surplus males, but there have been few attempts to assess the feasibility of this management technique across primate species. The present study provides preliminary data regarding social compatibility within a newly formed all‐male group of four white crowned mangabeys (Cercocebus atys lunulatus). The study was conducted at the Valencia Zoo (Spain), where data on social behavior were collected over 6 months using continuous focal animal sampling for a total of 87 hr of observation. Results show that low intensity aggressive behaviors (facial threats) were expressed at high rates, whereas physical aggression (fights) rarely occurred. Aggression was more frequent among individuals belonging to the same age–gender class. Regarding affiliative behaviors, every individual actively sought proximity to all other group members through positive approaches, and although not all males carried out social grooming, every male was groomed by at least one group member. Our results suggest that the group was compatible socially because social relationships among the individuals were not neutral, and physical aggression occurred at low rates. The present study provides preliminary data supporting the feasibility of all‐male groups as a management option for surplus males in captive populations of white crowned mangabeys. Nevertheless, further studies are needed to be able to generalize both within and across species. Zoo Biol 0:1–7, 2007. © 2006 Wiley‐Liss, Inc.     

Resting cortisol levels and the emergence of dominant status among male vervet monkeys

Resting serum cortisol was measured in adult male vervet monkeys (Cercopithicus aethiops sabaeus) in four different conditions: (1) among groups with unaltered group membership and established dominance hierarchies; (2) among groups from which the original dominant male had been removed and in which the remaining males competed for dominant status; (3) among newly formed groups of three unfamiliar males each of which had been the dominant male in his previous group; and (4) among groups from which a dominant male was temporarily separated and returned. In Condition 1, cortisol concentrations did not differ between dominant and subordinate males. The second condition showed that cortisol levels were highest among males who eventually emerged as the dominant male. In the third condition, however, cortisol levels did not differentiate eventually dominant from eventually subordinate males. In the last condition, cortisol levels were highest in the animals that became or remained dominant following reintroduction. These data indicate that cortisol concentration does not differ between dominant and subordinate males in stable groups and that cortisol rises during competition for dominance among familiar males.     

Social organization and social behavior in two subspecies of squirrel monkeys (Saimiri sciureus).

Social organization and social behavior were examined in two subspecies of squirrel monkeys which differ markedly in the degree of sexual dimorphism. The Bolivian squirrel monkeys, the subspecies with greater sexual dimorphism, manifested a sexually segregated form of social organization, while the social organization of the Guyanese monkeys was sexually integrated. Dominance relationships were found to reflect these patterns of sexual segregation or integration; in the Bolivian social groups separate linear dominance hierarchies were established within each sex while the Guyanese monkeys established a single linear hierarchy which included both males and females. Relationships between males and females in the two subspecies appear to be regulated by two distinct mechanisms, dominance in the Guyanese monkeys and sexual segregation in the Bolivians.     

Female social relationships in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli)

A study group of Campbell's monkeys (Cercopithecus c. campbelli) provided data on affiliative and agonistic relationships between females. Over a period of two years (involving 111 hr), we conducted observations of a captive group which had a composition similar to wild groups. We were able to identify a monitor-adjust social system with frequent affiliative interactions, directed gazing and avoidances rather than aggressive acts. We described long-term differentiated affiliative bonds: adult females interacting more often with some group mates than others, especially if they were relatives. Interactions between matrilines concerned essentially play and young adult females. We found a significant linear hierarchy of dominance with rare reversals and a stable intermatriline dominance. In contrast to other single-male groups, our adult male was socially integrated into the group although this may have been because of the housing conditions. Comparisons with the social organization of other captive and wild guenon groups are discussed.     

Group composition effects on social behaviour of captive squirrel monkeys (Saimiri sciureus)

Feral and semi-feral squirrel monkeys form sexually segregated subgroups. Observation of social interaction among laboratory animals revealed significant differences in social behaviour as a function of group composition. Females were more active in Unisexual groups. They engaged in more affiliative behaviour and were less often the target of agonistic attack. Adult females with young avoided adult males. ‘Aunts’ and Nulliparous females initially avoided these same males, but later spent over 50% of their time in close proximity to them. Results are discussed in terms of squirrel monkey social ecology, and successful child-rearing.     

Social behavior in fission–fusion groups of red uakari monkeys (Cacajao calvus ucayalii)

Primates living in large groups that divide to forage must have social systems compatible with this mode of living. Uakari monkeys (Cacajao spp.) live in large groups and exhibit a form of fission–fusion grouping, but their social organization is poorly understood. We present some of the first data on social behavior for this genus based on a study on Cacajao calvus ucayalii. They traveled in multimale multifemale groups of highly variable sizes, with bachelor units on the periphery. Adult males were affiliative, and adult females associated with more than one adult male. Adult females typically traveled with their dependent offspring and an older juvenile within the group. In parties of two or more males, individuals engaged in previously unreported display behaviors and acted together to aggressively chase other males. Breeding was seasonal, and mating occurred away from other group members. We speculate on the social organization of C. calvus ucayalii, in which dispersal may be bisexual and peripheral males are affiliative with one another. Affiliated males appear to cooperate in fighting and displaying to other males for access to females during the breeding season. Am. J. Primatol. 71:976–987, 2009. © 2009 Wiley‐Liss, Inc.     

Reactions of adult and immature squirrel monkeys to intergroup exposure

Initial encounters between unfamiliar animals raise the practical problem of controlling aggression and provide the opportunity to examine changes in social structure that may occur as groups merge. Social interactions and spatial grouping patterns were examined in newly formed squirrel monkey groups, in which a subgroup of familiar adults was introduced to a subgroup of familiar immature squirrel monkeys. Yearlings (10–11 months) and subadults (20–50 months) generally remained spatially distinct from adults, and intergroup interactions often consisted of adult-initiated antagonism. Adults exhibited sexual segregation in their spatial grouping patterns and interactions, whereas yearlings and subadults generally showed sexual integration. These data suggest that there is considerable adult resistance to integration of unfamiliar immatures into established adult social groups. Zoo Biol 17:519–524, 1998. © 1998 Wiley-Liss, Inc.     

Differences in Titi Monkey (Callicebus cupreus) Social Bonds Affect Arousal,Affiliation, and Response to Reward

Titi monkeys (Callicebus cupreus) are a monogamous, New World primate. Adult pair‐mates form a bidirectional social bond and offspring form a selective unidirectional bond to their father. Some of the neurobiology involved in social bonds and maternal behavior is similar to the neural circuitry involved in nonsocial reward. Due to these overlapping mechanisms, social states may affect responses to external rewarding stimuli. We sought to determine whether having a social attachment, and/or being in the presence of that attachment figure, can affect an individual's response to a rewarding stimulus. In addition, we compared affiliative bonds between pair‐mates to those between offspring and fathers. Eighteen adult male titi monkeys were either living alone (Lone), with a female pair‐mate (Paired), or with the natal group (Natal; N = 6/condition). Each individual went through eight 30‐min preference tests for a sweet substance, Tang. For Paired and Natal males, half of the test sessions were with their attachment figure and half were alone. Lone males were always tested alone. Preference scores for Tang, time spent drinking, affiliative, and arousal behaviors were measured. Paired and Natal males emitted significantly more isolation peeps and locomoted more when tested alone compared to when tested with their attachment figure, and paired males engaged in more affiliative behavior than Natal males. Lone males engaged in significantly more behaviors indicative of behavioral arousal such as locomotion and piloerection compared to Paired and Natal males. Finally, Paired males drank significantly more Tang and had a significantly greater preference for Tang compared to Lone and Natal males. These results indicate that offspring undergo a behavioral separation response upon separation from their father that persists into adulthood, Lone males are more behaviorally reactive, and that living with an attachment figure and the type of attachment relationship result in different responses to a rewarding sweet stimulus. Am. J. Primatol. 74:758‐769, 2012. © 2012 Wiley Periodicals, Inc.     

Sociophysiology of squirrel monkeys

Primate sociophysiology is an emerging discipline concerned with understanding the proximate mechanisms that contribute to the generation and maintenance of species-typical social systems. Studies of squirrel monkeys illustrate that sociophysiological processes are more varied than is commonly assumed with respect to both the effective social dimensions that influence physiological function and the nature of concomitant physiological effects. For adult squirrel monkeys, a major consequence of social stimulation is altered regulation of pituitary-adrenal, pituitary-gonadal, and autonomic function. In females, socially-induced physiological changes appear to be independent of specific interindividual relationships with other adults, whereas in males, many sociophysiological effects can be understood only when specific relational attributes are considered. In all instances, adult relationships are associated with distinctly different sociophysiological profiles than have been found for the mother-infant relationship and do not conform to the stress/buffering model within which they are often interpreted.     

Social organization of a stable natal group of captive Guyanese squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus sciureus</Emphasis>)

Socioecological models suggest competition for food, foraging efficiency, predation, infanticide risk, and the costs of dispersal regulate primate social structure and organization. Wild populations of squirrel monkeys (Saimiri spp.) appear to conform to the predictions of the predation/competition socioecological model (Sterck et al. in Behav Ecol Sociobiol 41:291–309, 1997) and the dispersal/foraging efficiency model (Isbell in Kinship and behavior in primates. Oxford University, New York, pp 71–108, 2004). However, squirrel monkeys in captivity are reported to maintain patterns of social behavior observed in their wild conspecifics despite different food distribution, predation risk, and dispersal options. This behavioral similarity suggests squirrel monkeys’ social behavior has limited flexibility to respond to environmental changes. In this study, we experimentally evaluated the flexibility of social behavior within a captive group of S. sciureus. First, we determined whether dominance and affiliative relationships observed under normal laboratory conditions (with abundant, widely distributed, food; no dispersal option; and no predators) better matched published reports of relationships among wild conspecifics or the predictions of the predation/competition model. Second, we made preferred food items defensible to determine whether dominance interactions would become more frequent and linear, as predicted by the model. The model correctly predicted rates of dominance behavior in both conditions and a linear hierarchy in the defensible food condition but did not predict the consistent affiliative relationships and linear dominance hierarchy observed in normal lab conditions. Although hierarchies were linear and male dominant, manipulating food distribution changed the dominant individual within each sex. Our findings suggest interaction rates adapt more rapidly than social structure to environmental changes in Saimiri and recommend caution in interpreting tests of socioecological models.