Inter-individual relationships in proboscis monkeys: a preliminary comparison with other non-human primates

This is the first report on inter-individual relationships within a one-male group of proboscis monkeys (Nasalis larvatus) based on detailed identification of individuals. From May 2005 to 2006, focal and ad libitum data of agonistic and grooming behaviour were collected in a forest along the Menanggul River, Sabah, Malaysia. During the study period, we collected over 1,968 h of focal data on the adult male and 1,539 h of focal data on the six females. Their social interactions, including agonistic and grooming behaviour, appeared to follow typical patterns reported for other colobines: the incidence of social interaction within groups is low. Of 39 agonistic events, 26 were displacement from sleeping places along the river, 6 were the α male threatening other monkeys to mediate quarrels between females and between females and juveniles, and 7 were displacement from feeding places. Although the agonistic behaviour matrix based on the 33 intra-group agonistic events (excluding events between adults and juveniles and between adults and infants) was indicative of non-significant linearity, there were some specific dominated individuals within the group of proboscis monkeys. Nonetheless, grooming behaviour among adult females within a group were not affected by the dominance hierarchy. This study also conducted initial comparisons of grooming patterns among proboscis monkeys and other primate species. On the basis of comparison of their grooming networks, similar grooming patterns among both-sex-disperse and male-philopatric/female-disperse species were detected. Because adult females in these species migrate to groups repeatedly, it may be difficult to establish the firm grooming exchange relationship for particular individuals within groups, unlike in female-philopatric/male-disperse species. However, grooming distribution patterns within groups among primate species were difficult to explain solely on the basis of their dispersal patterns. Newly immigrated females in some species including proboscis monkeys are eager to have social interactions with senior group members to improve their social position.     

Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis

The majority of studies of social learning in primates have tested subjects in isolation and investigated the effects of learning over very short periods of time. We aimed to test for social learning in two social groups of colobus monkeys, Colobus guereza kikuyuensis. Subjects were shown video footage of familiar monkeys either pushing or pulling a plastic flap to obtain a food reward, while they were given simultaneous access to the same apparatus. Action frequencies showed a significant difference between the two groups, with the pull group performing a higher proportion of pulls to pushes, compared with the push group. Copying persisted even in later sessions during which the demonstration footage was not being shown. We conclude that we successfully generated two contrasting behavioural traditions in these groups of monkeys. We do not know how long this contrast in behaviour would have persisted had we been able to continue testing for an even longer period of time, but further studies using similar designs and even longer test periods would have the power to confirm whether stable behavioural variation can be sustained between groups of monkeys, supported by social transmission.     

Sociability in Old Female Japanese Monkeys: Human versus Nonhuman Primate Aging

Over a period of 20 months, 18 aged and 22 non-aged semi-free ranging female Japanese monkeys were observed, and a total of 440 hours of focal animal data were collected. The goal of the study was to investigate the reported pattern of disengagement in old female monkeys. For each subject female, two sociability scores were calculated: the total number of other animals with whom time was spent in affiliative social interaction, and the total amount of time spent in affiliative social interaction. These data were analyzed in order to determine any change in sociability based on age. No relationship was found between age and sociability. The absence of a pattern of decreased social interaction with advancing age in these monkeys is discussed in terms of the methodological differences with earlier studies. It is suggested that the life of nonhuman primates may be essentially continuous from the attainment of adulthood to death, with no recognizable social stage for the elderly, at least in terms of sociability and isolation. Menopause, awareness of mortality, and interindividual dependence are three elements of the human life course that appear to be absent in this troop of Japanese monkeys, and these are discussed as key elements that may render the later portion of the human life course to be very different from that of monkeys, and possibly from that of all other primates.     

Familial interactions of male rhesus monkeys in a semi-free-ranging troop

Although the central and stable position of female rhesus monkeys in semi-free-ranging bands has been observed and described, the position of the developing male in the social group is not as well delineated. The present study is an attempt to describe interactions of 18 males with members of their families. Quantitative observations were made on one band (E) of rhesus monkeys on Cayo Santiago. Incidences of behavior recorded were joining, grooming, and threatening. The resulting data were analyzed by comparing the behavior of the males studied toward members of their genealogy as well as unrelated members of the social group. Behavior of family and non-relatives toward the males was also revealed. Statistical analysis revealed that the male subjects engaged in more positive social interactions within the matrifocal family than with other members of the genealogy, and in turn, more such behavior was observed within the genealogy than with unrelated monkeys. Threatening behavior within the genealogies was infrequent. Age effects were noted in that family members directed more interactions toward younger males and as males matured, they groomed more but joined family members less frequently. These data suggest mechanisms of socialization within the genealogy that may be different from those employed within the unrelated social group.     

Infant Development and Parental Care in Free-Ranging <Emphasis Type="Italic">Aotus azarai azarai</Emphasis> in Argentina

Studies of infant development and parental behavior in free-ranging owl monkeys have been constrained by their nocturnal habits. Taking advantage of the cathemeral activity pattern of Aotus azarai azarai in the Argentinean Chaco, we describe the development of a cohort of free-ranging infants born in an owl monkey population in Formosa Province. We observed 7 infants, whose birth dates are known to the nearest week, to record details of their development and care between October 1999 and March 2000. We collected 92 h of behavioral data in 76 sessions. The infants were almost never off the parents during the first 4 wk of life, and we observed no infant being transported by a nonadult. The parent carrying the infant traveled most frequently in the middle of the group, sometimes first, but rarely last. The mean duration of 33 nursing episodes is 69 sec. After nursing, the infant was more likely to return to the nonnursing adult than to remain with the mother suggesting that in owl monkeys the infant may be primarily attached to the adult male in the group. Infants began to explore, to manipulate and to consume solid foods during the second month. Our observations are comparable to ones on captive breeding groups of Colombian owl monkeys (Aotus lemurinus) and Bolivian owl monkeys (A. azarai boliviensis) under controlled conditions of temperature, illumination and food availability.     

Dihydrotestosterone propionate effects on dominance and sexual behaviors in gonadectomized male and female rhesus monkeys.

One triad of male and two triads of female gonadectomized rhesus monkeys were observed as social groups assembled for repeated hour-long sessions. Social relationships were measured in terms of aggressive behavior between the members of each group in order to determine the dominance hierarchical order. Sexual performance was assessed for each male, before and after castration, in tests with an estrogen-stimulated ovariectomized female. Similar measures were made when the same female was periodically introduced to the all-male triad. When dihydrotestosterone propionate (DHTP) was administered for a period of 6 weeks to the middle-ranking member of each group, social status changes occurred in two groups, one male and one female, resulting in the elevation of the treated monkeys to the highest rank in the dominance hierarchy. In the other female group, aggressive behavior was increased with DHTP treatment of the middle-ranking female. Somatic effects, particularly a gain in body weight, occurred in all treated animals. Yawning behavior also increased significantly in those animals receiving DHTP. The latter two effects returned toward pretreatment levels following the cessation of hormone injection; however, changes in dominance hierarchy persisted to the end of the experiment, 6 weeks following the last DHTP treatment.     

Rank,relationships, and responses to intruders among adult male vervet monkeys

We examined the influences of dyadic relationships among captive adult male vervet monkeys (Cercopithecus aethiops sabaeus) on behavior directed toward caged “intruder” males placed inside subjects' enclosures. Subjects were all 9 adult male residents from three stable social groups, each of which contained 3 adult males, at least 3 adult females, and their immature offspring. Every male was observed in two 3-hour sessions, each time with one of the 2 other adult males from his group. Observation sessions consisted of six consecutive 30-min stages in which group composition and the presence of the intruder were manipulated. All groups exhibited a stable, linear male dominance hierarchy prior to and throughout the study. In each group, there was one pair of males, when together, in which each member exhibited higher rates of intruder-directed approach and aggressive behaviors than when either animal was paired with the third male of his social group. Such pairs were also distinguished by high levels of within-pair agonistic interactions. The higher-ranking member of each dyad was the most aggressive male toward the intruder in his social group, although only one of these animals was the dominant male of his group. Mutual facilitation of aggression against intruding males is interpreted as cooperative behavior benefitting both males by increasing the likelihood of repelling a potential competitor for resident females. Such cooperation provides further evidence in nonhuman primates for cohesive male-male dyads between animals whose social interactions are characterized by agonism. © 1993 Wiley-Liss, Inc.     

A social developmental study of young monkeys (Callithrix jacchus) within a captive family group

Quantitative data were collected on the behaviour of one captive family group of common marmoset monkeys over some six months, which included a period immediately before the birth of a third set of twins, and up to the birth of the fourth set. Data were consistently collected on marking, auto and social grooming, as well as on three general categories of play behaviour. In addition, observations were recorded on the carrying of infants by other members of their family, until the end of the fourth week after the birth. The study demonstrated quantitative changes in the behaviour of juvenile and adult members of the family, and indicated the time scale of increasing involvement of the youngest monkeys in some of the major patterns of behaviour in the life of a family social unit.     

Grooming,kinship, and co‐feeding in captive spider monkeys (Ateles geoffroyi)

Allo‐grooming is perhaps the most powerful affiliative behavior observed in non‐human primates. However, the functional significance of grooming in New World monkeys has not yet been fully understood, perhaps because grooming is less frequently observed in platyrrhines. To differentiate the potential role of affiliative investment and/or kinship on sharing access to food (co‐feeding) in spider monkeys, behavioral data on grooming, embracing, and feeding were collected from two different groups of captive study subjects: a familiar/kin group and a non‐familiar/non‐kin group. The results of this study suggest that family‐related spider monkeys that engage in grooming tend to share access to food resources more than unfamiliar conspecifics that do not groom. One explanation for this difference is that the unfamiliar study subjects had not yet invested in the affiliative social network, were not reciprocating their affiliative investments and hence, had a higher tendency toward single animal monopolizing resources. Degree of relatedness alone was not found to be a determinant for sharing the access to food, suggesting that familiarity in spider monkeys is based on the extent to which animals invest in affiliative relationships. In this study, only animals that had engaged in long‐term grooming and recognized each other as familiar shared the access to food. Therefore, it might be likely that in spider monkeys, long‐term grooming of high intensity has to be developed for co‐feeding to occur. Zoo Biol 20:293–303, 2001. © 2001 Wiley‐Liss, Inc.     

Activity budgets in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve, China

We examined time allocation by Sichuan snub-nosed monkeys Rhinopithecus roxellana in the montane,temperate and highly seasonal forests of the Shennongjia Nature Reserve in China,in order to improve our understanding of the ecological and social influences on monkey behavior.We collected data on activity budgets in relation to food availability in a group of monkeys from July 2003 to September 2004(except February 2004),using instantaneous scan samples.The monkeys spent 36.21% of daytime moving(n=21,269 reco...     

Changes in the structure of group behavior in callosotomized rhesus monkeys

The studies were performed on 4 intact and 3 callosotomized adult male rhesus monkeys that comprised one social group. Group behaviour of all the monkeys was investigated by the frequency method of social contacts registration. Both aggressive and friendly contacts were registered. The results obtained have shown a considerable decrease in social contacts of callosotomized rhesus monkeys, as compared to normal animals. The aggressive contacts prevailed in the behaviour of the operated monkeys. The data suggest that callosotomy does not only significantly decrease the frequency, but also alters the structure of social contacts in the rhesus monkeys.     

Extinction deficits in male rhesus macaques with a history of self-injurious behavior

Self-injurious behavior (SIB) occurs in both human and nonhuman primate populations. Despite the potential for harm, SIB may persist in part because of an inability to inhibit behavior that results in wounding. A lever-pressing task was used to test the prediction that monkeys with SIB would show greater persistence in lever-pressing on extinction trials than monkeys without the disorder. The subjects were 15 individually-housed adult male rhesus macaques, 10 of which (the SIB group) had a veterinary record of self-inflicted wounding. All of the monkeys were trained to lever-press for food rewards to a criterion of 400 total responses. The test procedures consisted of five daily 30-min sessions divided into six 5-min intervals. On day 1, the subjects received continuous reinforcement. On days 2-4, testing consisted of alternating reinforced/unreinforced 5-min intervals, beginning with reinforcement. Reinforced intervals were cued with a buzzer. On day 5, the subjects received no reinforcement. The number of lever-presses and behavioral responses were recorded during each session. Saliva samples were collected for cortisol measurement before and after test sessions on days 1, 2, and 5. As predicted, monkeys with SIB lever-pressed more than controls during extinction intervals on days 2-4. There was no difference on day 1 or day 5. The frequency of scratching, yawning, and abnormal behavior increased when reinforcement was intermittent (days 2-4) or absent (day 5). Cortisol levels were highest with continuous reinforcement (day 1), and may reflect differential levels of food intake rather than stress. The presence of extinction deficits suggests that SIB may persist in some monkeys because they lack the ability to regulate the intensity of their biting behavior.     

The effects of data collection and observation methods on uncertainty of social networks in wild primates

In social species, network centralities of group members shape social transmission and other social phenomena. Different factors have been found to influence the measurement of social networks, such as data collection and observation methods. In this study, we collected data on adults and juveniles and examined the effect of data collection method (ad libitum sampling vs. focal animal sampling) and observation method (interaction—grooming; play—vs. association—arm-length; 2 m; 5 m proximities—) on social networks in wild vervet monkeys. First, we showed using a bootstrapping method, that uncertainty of ad libitum grooming and play matrices were lesser than uncertainty of focal matrices. Nevertheless, grooming and play networks constructed from ad libitum and focal animal sampling were very similar and highly correlated. We improved the certainty of both grooming and play networks by pooling focal and ad libitum matrices. Second, we reported a high correlation between the proximity arm-length network and the focal grooming one making an arm-length proximity network a reasonable proxy for a grooming one in vervet monkeys. However, we did not find such a correlation between proximity networks and the play one. Studying the effects of methodological issues as data collection and observation methods can help improve understanding of what shapes social networks and which data collection method to choose to study sociality.     

Social organization of captive monandrous squirrel monkey groups (Saimiri sciureus).

1 adult male and 4 adult female squirrel monkeys were observed together as a group, isolated from all other monkeys. 3 of the 4 females were deafened for a previous experiment. Deafening, however, had no apparent, permanent effect on social behavior. Social dominance hierarchy was evaluated in a variety of situations. The results were compared with those of a similar set of observations on the females prior to the introduction of the male. Before the male was introduced, the dyadic interactions involving food stealing, body grasping, and sexual behaviors were indicative of a female linear rank order. After the male was introduced, the rank order among the females generally remained intact, with the male becoming the highest ranking member in the group. The noteworthy exception to the stability involved the highest ranking female, whose position in the hierarchy was threatened. Heterosexual interactions predominated. Homosexual behavior was also observed, although appreciably reduced in frequency as compared to the all-female group situation. A similar rank order hierarchy was observed in a second group of squirrel monkeys comprised of 1 adult male and 4 adult females. None of these monkeys was deaf.     

Social after-effects of fur rubbing in tufted capuchin monkeys (Cebus apella): increased antagonism and reduced affiliation

Fur rubbing is widely believed to have a social bonding function in capuchin monkeys, yet a recent study of tufted capuchins revealed increased levels of aggression and reduced levels of affiliation after fur-rubbing bouts. This observed decrease in group cohesion may be attributable to increased intragroup competition for fur-rub material rather than being a direct effect of fur rubbing itself. To test this hypothesis, we separated individual tufted monkeys (Cebus apella) from their social group and provided them with fur-rub material or control material, thereby avoiding intragroup competition. After engagement with materials, we released subjects back into their social group and observed their subsequent interactions with group members. We found that subjects were more likely to encounter aggression and less likely to receive affiliation from others in the fur-rub condition than in the control condition. These results support the idea that fur rubbing carries social after-effects for capuchin monkeys. The precise mechanisms of the observed effects remain to be clarified in future studies.     

Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi's monkeys (Callimico goeldii)

Neophobia, defined as showing caution toward novel features of the environment, is widespread in birds and mammals; it can be affected by ecology, early experience, and social context. In this study, we aimed to (i) investigate the response to novel food in adult common marmosets and Goeldi's monkeys and (ii) assess the role of social influences. We used an experimental paradigm employed previously with capuchin monkeys and children, in which a subject (observer) was presented with a novel food under three conditions: (i) Presence: group members did not have food; (ii) Different color: group members received familiar food whose color differed from that of the observer's novel food; (iii) Same color: group members received familiar food of the same color as the observer's novel food. Although most common marmosets tasted and/or ate the novel food, none of the Goeldi's monkeys ate it and only two sampled it. Differences in home range size and early social experience might explain the divergent behavior of the two species. Observers of both species similarly attended to group members and their visual attention increased with the number of group members eating, especially when the observer's and group members' foods were perceptually similar. However, we observed social influences on explorative behavior in Goeldi's monkeys but not on explorative or eating behavior in common marmosets. This result might be explained by the different pattern of response to novel food observed in the two species. Moreover, social influences on Goeldi's monkeys' behavior were nonspecific, i.e. they were not based on an appreciation that the food is safe because eaten by group members.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

The effects of fur rubbing on the social behavior of tufted capuchin monkeys

Fur rubbing has often been attributed as a social as well as a medicinal function in capuchin monkeys, yet to date there have been no studies investigating the effects of fur rubbing on subsequent group dynamics. Here, we report for the first time how social group cohesion is affected by fur rubbing in tufted capuchin monkeys. Fifteen captive capuchins were each observed six times for 45 min, three times following the provision of materials typically used for fur rubbing (onion) and three times following control food items (apple). When compared with the apple condition, monkeys significantly increased proximity to one another in the first 15 min of the onion condition, which is when most fur rubbing took place. Moreover, monkeys were more likely to spend time in groups when fur rubbing but less likely to spend time in groups when manipulating the onion in other ways. In subsequent periods monkeys were less likely to be in proximity to one another in the onion condition compared with the apple condition. Aggression between group members was elevated whereas affiliation was decreased throughout the onion condition. In short, capuchins spent more time further apart and engaged in more aggressive acts and shorter affiliative acts following fur-rubbing bouts. It is possible that these differences in behavior could be owing to differences in how the monkeys competed for and interacted with the items presented in each condition rather than due to fur rubbing as such. Alternatively, fur rubbing with pungent materials might interfere with olfactory cues used to regulate social interactions within a group and thereby cause increased levels of aggression.     

Context affects the numerical semantic congruity effect in rhesus monkeys (Macaca mulatta)

Do monkeys anchor their numerical judgments based on the context in which their choices are presented? We addressed this question by varying the numerical range across sessions while macaque monkeys made ordinal judgments. Monkeys were trained to make a conditional discrimination whereby they were reinforced for ordering arrays of dots in ascending or descending numerical order, dependent on a color cue. Monkeys were tested using two ranges of numerosities that converged on a single pair. Similar to the findings of Cantlon and Brannon (2005), we found a semantic congruity effect whereby decision time was systematically influenced by the congruity between the cue (ascending or descending) and the relative Numerical Magnitude of the stimuli within each range. Furthermore, monkeys showed a context effect, such that decision time for a given pair was dependent on whether it was a relatively small or large set of values compared to the other values presented in that session. This finding suggests that, similar to humans, the semantic congruity effect observed in monkeys is anchored by the context. Thus our data provide further evidence for the existence of a shared numerical comparison process in monkeys and humans.