Reconciliation in captive Guyanese squirrel monkeys (Saimiri sciureus)

The tendency for agonistic interaction to increase the probability of friendly interaction between social partners has been demonstrated across a range of Old World primates. While research on such post-conflict behavior proceeds into an hypothesis-testing phase, new comparative information must accumulate to provide full phylogenetic perspective on primate social behavior. Data from New World and prosimian primates are yet extremely limited. We studied captive squirrel monkeys (Saimiri sciureus) via post-conflict (PC) and matched control (MC) observations and analyzed results using both the PC-MC and time-rule methods. Former opponents maintaining affiliative relationships soon engaged in friendly interaction following large proportions of agonistic interactions, whereas non-affiliated individuals, including virtually all male-female pairs, reconciled conflicts rarely. Close-proximity approaching and huddling contact constituted the principal modes of post-conflict amicability. Agonistic interactions of relatively high intensity were most likely to be reconciled and most likely to be reconciled via physical contact. High vulnerability of Saimiri to predation may have favored this species' strong inclination to reconcile soon after agonistic interaction. Research on free-living populations of this and other primate species is needed to illuminate similarities and differences across taxa.     

Neighbor effects in marmosets: social contagion of agonism and affiliation in captive Callithrix jacchus

Researchers have demonstrated the neighbor effect for affiliative and agonistic neighbor vocalizations in captive chimpanzees. We extend the investigation of the neighbor effect to New World monkeys, Callithrix jacchus. We collected data on vocalizations and behaviors of 31 focal individuals and concurrent neighbor vocalization within three behavioral categories: intragroup and intergroup aggression and intragroup affiliation. We investigated whether there was an influence of neighbor vocalizations on focal behavior within the same behavioral category. For data analysis we used approximate randomization of paired‐sample t‐tests. We found that marmosets performed intergroup aggressive behavior (bristle, anogenital present for neighbor loud shrill only) for significantly longer, and emitted significantly more intergroup agonistic vocalizations (twitter, loud shrill), at a high frequency of intergroup agonistic neighbor vocalizations (twitter, loud shrill) than at low. The marmosets were also significantly more likely to engage in bristle behavior immediately after hearing a neighbor intergroup aggressive call (twitter, loud shrill) than directly beforehand. High neighbor intragroup agonistic calls (chatter) were associated with significantly longer spent in related behavior (composite of: attack, chase, steal food). Affiliative behaviors (share food, grooming invite) were engaged in by marmosets for significantly longer at higher frequencies of affiliative neighbor chirp calls than at low. Marmosets were also significantly more likely to perform food sharing and active affiliative contact immediately after rather than before hearing a neighbor chirp call. Our findings suggest that neighbor vocalizations influence marmoset behavior through social contagion and indicate that the neighbor effect for affiliation and aggression generalizes to the marmoset. Am. J. Primatol. 72:549–558, 2010. © 2010 Wiley‐Liss, Inc.     

Social interaction analysis in captive orcas (Orcinus orca)

The management of socially complex species in captivity is challenging. Research on their social behavior improves our understanding of interactions in captive animals and captive‐group management. We conducted a detailed analysis of social relationships shown by the orcas kept at Loro Parque zoo and their tendency to reconcile after aggressive episodes. Affiliative interactions were the most frequent social activities compared to agonistic or sexual interactions. Within affiliative behaviors, we documented the pattern “gentle tongue bite”, where an animal touches the other's tongue with his teeth but does not bite it. Affiliative interactions between a specific pair of orcas occurred significantly more often than expected by chance, and together with low levels of agonistic interactions, indicated particular affinity between some individuals. The most frequently observed low‐level agonistic relationship was that of the two older males (Tekoa–Keto); however, they also showed frequent sexual and affiliative interactions. Sexual‐like behaviors (pursuit, mount, and penis between males) were found in both sexes. Finally, the observed corrected conciliatory tendency (31.57%) was within the range described for other primate and cetacean species. This study provides a systematic way to assess social interactions as well as conflict management strategies in cetaceans housed in zoos and zoo‐like facilities and may help to improve animal welfare and management of animals in controlled environments.     

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.     

人工投食行为对非人灵长类社会生态的影响

近年来,国内开展了对几种非人灵长类投食群的研究。借鉴日本猴(Macaca fuscata)、恒河猴(M.mulatta)和黑猩猩(Pan troglodytes)长期积累的研究经验,有利于我们减少人工投食对非人灵长类带来的不利影响,也有利于推动国内非人灵长类社会生态学的深入研究。本文通过比较这三种灵长类野生群和投食群之间的差异,量化地分析了人工投食对灵长类动物社会生态学方面的影响。结果表明在社会行为方面,人工投食会导致灵长类动物的聚集、增加争斗频率、改变个体间等级关系、延缓分群现象、影响活动域和增加新兴行为。在种群数量方面,人工投食会缩短雌性性成熟时间、增加出生率和婴猴存活率、减少成年猴死亡率。而人工投食对雄性性成熟、出生间隔等方面的影响仍需要进一步考证。最后我们讨论了人工投食行为的利弊,并建议应谨慎和妥善地实施人工投食,和对非人灵长类投食群进行合理的监管。     

Developmental changes in responsiveness to parents and unfamiliar adults in a monogamous monkey (Callicebus moloch)

Titi monkeys (Callicebus moloch) are monogamous New World primates that are characteristically found in family-type groups consisting of a mated adult pair and one or two young. The factors maintaining the small size of these groups are not known. Based on observations of free-ranging and captive families, parental aggression toward older offspring seems unlikely to play a significant role. Maturing individuals themselves, however, could undergo behavioral changes that weaken ties to their natal group. These might include waning of affiliative relations with parents, or subtle forms of aversion. Independent of such changes, increasing interest in unfamiliar conspecifics could be a factor. We examined these possibilities in the present study by assessing changes in social behavior and social preferences from initial ambulatory independence (6 months) through reproductive maturity (24 months) in a combined cross-sectional/longitudinal study of 21 captive titi monkeys living with their parents. Responses to both parents and to an unfamiliar adult heterosexual pair, a single unfamiliar adult male, and a single unfamiliar adult female were observed when subjects were given a choice between parents and strangers presented simultaneously or as the only social incentive. Social stimuli were at opposite ends of a 16.8-m-long test corridor. Subjects could move freely about the corridor for 5 min with each configuration of social stimuli. They stayed closer to parents than to strangers at all ages. Responsiveness to strangers increased with age and suggested growing ambivalence, particularly toward the male stranger. As they approached 24 months of age, male subjects showed a dramatic increase in the frequency and intensity of agonistic behaviors toward male strangers, behaviors that were rarely directed toward female strangers or parents. Waning of attraction to parents may be less important in dispersal from the natal group than changing reactions to strangers.     

The effect of social and ecological factors on the time budget of wild vervet monkeys

Animals often have a limited time to perform different fitness‐enhancing activities, such as the trade‐off between socializing versus foraging in group‐living species. Many previous studies have focused on how ecological and social factors influence activity budget at the individual or group level in various species. However, few primate studies have focused on multiple study groups living within a similar habitat. Here, we analyse group, season and sex effects on the individual activity budget of wild vervet monkeys (Chlorocebus pygerythrus) living in four groups with overlapping home ranges. Generally, our findings support previous studies on primates. Our results indicate that intragroup competition may force larger groups to spend more time feeding and less time resting. We also found that seasonal variation, and therefore food availability, has a strong influence on the monkeys’ activity budget. Females, which are the philopatric sex in vervet monkeys, spent more time socializing while, in general, males spent more time resting. However, we did not find any difference on the time spent socializing between groups. Since there is evidence that not only time constraints and habitat quality but also group size influence individual behaviours and ultimately group living, we advise that future studies should focus on multiple groups of the same species living in the same habitat in order to better understand how all these variables are interlinked.     

Postconflict behavior among female Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in the Qinling Mountains, China

For group-living primates, the information on postconflict management is crucial for understanding primate competition and cooperation. However, such information is poorly known for snub-nosed monkeys, especially for wild populations. In this study, from September 2007 to June 2008, we investigated postconflict behavior among adult females Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in a wild, provisioned group in the Qinling Mountains of China by means of the time-rule method and the PC-MC method. We obtained a total of 81 PC-MC pairs and each individual was involved in only 0.004 aggressive behavior per observation hour. The first affiliative behavior was more likely to occur within the first minute after a conflict. The postconflict affiliative behaviors most often seen were contact-sit, embrace and grooming. The affiliative contacts between adult females occur due to selective attraction, I.e. Reconciliation. The pattern of postconflict affiliation demonstrates that the R. Roxellana belongs to a tolerant species.     

Visitors excite primates in zoos

Fifteen species of primate were observed to assess the effects of zoo visitors on their social behavior. When visitors were present primates were less affiliative, more active, but more aggressive. These changes were particularly marked in arboreal monkeys, especially in smaller species, and were reduced by 50% by lowering the height of spectators. Detailed observations of a group of mandrills indicated that with increasing numbers of visitors the monkeys showed a linear increase in attention to visitors, in activity, and in stereotyped behavior. All of these effects are consistent with an interpretation that visitors are a source of stressful excitement rather than of enrichment.     

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.     

Influence of kinship and spatial density on reconciliation and grooming in rhesus monkeys

Some cercopithecine primates direct disproportionate amounts of grooming, huddling, and agonistic support toward maternal kin. Disproportionate amounts of aggression are also directed toward maternal kin, however, suggesting that mechanisms that restore relationships damaged by aggression, such as reconciliation, might be biased toward these preferred social partners. Studies investigating kinship effects and reconciliation are inconsistent, however, perhaps because of differences in the environmental conditions under which behavior was observed. In order to test the effects of kinship and spatial density on affiliative and reconciliation behavior, we conducted focal and scan sampling on a group of rhesus monkeys (Macaca mulatta) living in an outdoor corral under low spatial density conditions. We then compared this data to previously published data on a group of the same species living under higher spatial density conditions. Neither overall grooming nor reconciliation were affected by spatial density once correction procedures were applied. Grooming was kin biased at both study sites, whereas reconciliation was kin biased only in the low-density group. Although data failed to support a Coping Model according to which grooming and reconciliation should go up under higher densities, we suggest that coping may be reflected not so much in overall rates of behavior but in strategic partner choices, such as the increased importance monkeys under crowded conditions appear to attach to nonkin partners. © 1996 Wiley-Liss, Inc.     

Male chimpanzee behavior in relation to female ano-genital swelling

This study examined the relationships between male agonistic, affiliative, and sexual behaviors and female estrus condition in captive adolescent and young-adult chimpanzees (Pan troglodytes). Data on agonistic, affiliative, and sexual behaviors of 11 males living in three social groups were collected during daily 45 minute observations over a 5 month period. Female estrus condition was assessed daily using the relative size of the female's ano-genital swelling. It was hypothesized that the presence of maximally tumescent females would generate conflicts between males, so an increase in inter-male agonism was predicted. Males exhibited higher rates of agonism toward other males when at least one female in the group was maximally tumescent. Male affiliative behavior directed toward other males and social play with males were affected by the presence and number of maximally tumescent females. Male sexual behavior increased when maximally tumescent females were present.     

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.     

Examining deep litter as environmental enrichment for a family group of wolf's guenons,Cercopithecus wolfi

Manipulable substrates promote species‐typical behavior and decrease abnormal behavior in a variety of primate species. However, the effects of providing litter to arboreal primates are not as well studied, and there is little information specifically concerning enrichment for guenons. To inform the captive management of an under‐studied species, we evaluated deep litter substrate as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi. We expected it to promote species‐typical behavior and to act as an intervention by reducing aggressive behaviors targeted toward a juvenile group member by his parents. We compared the guenons' behavior during baseline periods in which normal husbandry routines were followed to periods when the entire floor of their enclosure was covered with 30 cm of straw or wood wool. We then evaluated the group's preference between litters by comparing their relative use. The guenons spent more time feeding and were more active during both litter conditions, but relative to their respective baselines, they spent more time examining straw and less time examining wood wool. Straw, but not wood wool, promoted some affiliative behavior as well as greater tolerance of the juvenile's social proximity to others. However, the addition of deep litter did not ameliorate patterns of agonistic behavior among our subjects. Our results suggest that straw conferred greater behavioral benefits than wood wool as a deep litter substrate for this guenon group and may constitute a form of environmental enrichment for this species. Zoo Biol 29:626–632, 2010. © 2009 Wiley‐Liss, Inc.     

Primate sociality in evolutionary context

Much work has been done to further our understanding of the mechanisms that underlie the diversity of primate social organizations, but none has addressed the limits to that diversity or the question of what causes species to either form or not form social networks. The fact that all living primates typically live in social networks makes it highly likely that the last common ancestor of living primates already lived in social networks, and that sociality formed an integral part of the adaptive nature of primate origins. A characterization of primate sociality within the wider mammalian context is therefore essential to further our understanding of the adaptive nature of primate origins. Here we determine correlates of sociality and nonsociality in rodents as a model to infer causes of sociality in primates. We found sociality to be most strongly associated with large-bodied arboreal species that include a significant portion of fruit in their diet. Fruits and other plant products, such as flowers, seeds, and young leaves, are patchily distributed in time and space and are therefore difficult to find. These food resources are, however, predictable and dependable when their location is known. Hence, membership in a social unit can maximize food exploitation if information on feeding sites is shared. Whether sociality evolved in the primate stem lineage or whether it was already present earlier in the evolution of Euarchontoglires remains uncertain, although tentative evidence points to the former scenario. In either case, frugivory is likely to have played an important role in maintaining the presence of a social lifestyle throughout primate evolution.     

Managing the socialization of an adult male gorilla (Gorilla gorilla gorilla) with a history of social deprivation

Most non‐human primates exhibit aggression during changes in social group composition. In zoological parks, group membership changes are necessary for optimal population management, but can elicit problematic aggression. Furthermore, some primates with a long history of social deprivation are hyperaggressive when introduced to conspecifics. In this study of one male gorilla with a 30‐year history of social deprivation, we assessed the rate of aggression quantitatively during a four‐step socialization procedure. We hypothesized that 1) the frequency of agonistic/display behaviors would increase markedly at the beginning of each phase of the socialization, then decline to baseline levels over time in each phase and 2) the frequency of affiliative behaviors would not vary systematically within or between phases of socialization. Our results largely supported these predictions, and we found the four‐step socialization process effective in managing aggression in this case. In addition to documenting the successful socialization of a socially deprived adult male gorilla, we believe that the empirical process used in this case argues for scientific management of other introductions. Zoo Biol 20:347–358, 2001. © 2001 Wiley‐Liss, Inc.     

Social lives of adult Mysore slender lorises (Loris lydekkerianus lydekkerianus)

Despite the persistent use of the word "solitary" to describe nocturnal primate social behavior, increasing numbers of studies are revealing sophisticated levels of social interactions among nocturnal primates. This study explores the relationships among 11 adult Mysore slender lorises (Loris lydekkerianus lydekkerianus) studied over 10(1/2) months in Tamil Nadu, India. When all observations regarding dependent offspring are excluded, the animals spent on average 38% of their activity in various forms of neutral, affiliative, and agonistic behaviors. Affiliative behaviors were the most common type of social interaction, and males in general were more social than females. Low values for Cole's index (CI) of association emphasize that females rarely interacted with same-sex conspecifics, but commonly interacted with males. In turn, males also formed strong affiliative relationships with other adult males. This index also indicates that levels of affiliation are strongest among animals that share sleeping sites. The Hinde index (HI) suggests that males control proximity to females more than the reverse. A female's tolerance of multiple males in her home range and at a sleeping site may be related to high spatial variability of food resources. Such resources may constrain females with costly reproductive strategies (up to two sets of twins per annum) to a small home range. With their larger home ranges, males may be able to monopolize females by initiating social interactions, and also provide a benefit to females by contributing to parental care.     

The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae)

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Sex differences in adolescent rhesus monkey (Macaca mulatta) Behavior

Sex differences in the behavior of 2.5- to 4.5-year-old rhesus monkeys, living in two social groups approximating natural compositions, were studied over a period of 3 years. Both sexes interacted significantly more often with members of their own sex in agonistic and affiliative interactions even when total rates and durations for male and female subjects did not differ. Strong sexual segregation was also seen in proximity, nonspecific contact, and huddling partners. Males were more involved in play and sex than were females and engaged in these activities primarily with other males. Females did more grooming than males, but groomed both male and female partners. Females also appeared to interact with a wider age range of partners than did males. Although total participation in aggressive interactions did not differ between the two sexes, females used more active forms of agonistic expression than did males. These differences in the behavior of adolescent rhesus are hypothesized to lead to social bonding among adolescent males, while females remain bonded to their matri-lines, including younger males and some fully adult males associated with matrilineal relatives. Adolescent males emigrate from their natal groups but retain sociality and bond to males and females in new groups as they become adult. © 1993 Wiley-Liss, Inc.