Impact of internal and external factors on prosocial choices in rhesus macaques

While traditional economic models assume that agents are self-interested, humans and most non-human primates are social species. Therefore, many of decisions they make require the integration of information about other social agents. This study asks to what extent information about social status and the social context in which decisions are taken impact on reward-guided decisions in rhesus macaques. We tested 12 monkeys of varying dominance status in several experimental versions of a two-choice task in which reward could be delivered to self only, only another monkey, both the self and another monkey, or neither. Results showed dominant animals were more prone to make prosocial choices than subordinates, but only when the decision was between a reward for self only and a reward for both self and other. If the choice was between a reward for self only and a reward for other only, no animal expressed altruistic behaviour. Finally, prosocial choices were true social decisions as they were strikingly reduced when the social partner was replaced by a non-social object. These results showed that as in humans, rhesus macaques'' social decisions are adaptive and modulated by social status and the cost associated with being prosocial.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Social and environmental influences on self-aggression in monkeys

Three studies of stumptailed macaques examined the occurrence of self-aggression (SA) under different housing conditions. In group tests those environmental manipulations which increased social aggression decreased SA, but similar environmental conditions were found to increase SA in monkeys when tested in individual cages. SA increased in a group of monkeys in response to a temporarily impoverished environment. Like stereotyped movements reported for other species, SA may increase sensory input in poor environments, but this is probably not true for group-living monkeys, in which SA appears to be primarily a form of redirected social aggression. This research partially supported by SRC grant B/RG-98910 to A.S.C. Both J.R.A. and V.J.N. were partly supported by SRC studentships.     

Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta)

Due to primate adaptations for sociality, captive rhesus macaques have optimal welfare and utility as a biomedical model when they can be maintained in outdoor social groups. As a despotic species; however, aggression can result in costly injuries and may result in temporary or permanent removal of specific individuals from social housing. Enrichment items, such as toys, climbing structures, and foraging material, are employed to keep captive animals occupied. We hypothesized that produce enrichment that requires more processing to extract may reduce socially‐derived injuries by keeping animals occupied. We tested the effects of additional weekly produce (corn‐in‐husk, whole melon, or whole squash) on trauma incidence in an outdoor social group of rhesus macaques across two distinct seasons (mating and birthing seasons) at the California National Primate Research Center. Aggression and status behavioral data, food resource use and proximity, and trauma incidence were collected over two 16‐week periods, with eight control and treatment conditions alternating biweekly. Mixed‐effects regression modeling was used to determine the best predictors of trauma risk and severe aggression at the group level and at an individual level. We found that food resource use was an important predictor of trauma risk at both group and individual levels; greater use of food resources reduced trauma risk. Produce enrichment did not; however, reduce severe aggression. We suggest that other captive social groups of rhesus macaques with high levels of trauma may benefit from supplemental produce enrichment that increases animal engagement with food resources.     

Evidence that emotion mediates social attention in rhesus macaques

Background

Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual’s emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species.

Methodology

We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state.

Principle Findings

The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces.

Conclusions/Significance

These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.     

A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys

Social grooming in primates is a complex behavior in which monkeys stroke, pick, or otherwise manipulate a companion’s body surface. While grooming has been associated with important social functions, researchers who have examined its physical characteristics, such as body site preferences, have focused on its role in skin care and ectoparasite removal. Whether the form of social grooming is constrained primarily by utilitarian or social functions was empirically tested by directly comparing this behavior with self-grooming, which was assumed to have primarily utilitarian functions. Predictions made concerning social grooming, based on a comparison with self-grooming, were tested by examining site preferences, duration of grooming (overall and to specific body sites), and method of grooming (stroking, picking, or a combination of the two) in rhesus monkeys. None of these predictions was verified. The physical characteristics of social grooming could not be predicted from the way an animal groomed itself. There was no relationship between site preferences in these two types of grooming. Animals groomed others for longer periods of time than they groomed themselves, both overall and when grooming specific sites. The methods these animals used differed markedly in self-and social grooming: they primarily picked at their own hair or skin but, when grooming others, varied their technique across sites, stroking the hair where it was thickest and picking where the hair was sparse. These results suggest that utilitarian functions are not the most important factors constraining the form of social grooming.     

Tonkean Macaques Orient Their Food Search From Olfactory Cues Conveyed by Conspecifics

We investigated the ability of monkeys to use referential information about environmental resources from cues passively transmitted by conspecifics. The subjects and their companions were four young males belonging to a group of semifree‐ranging Tonkean macaques (Macaca tonkeana) raised in a 2‐acre wooded park. In a first experiment, a subject had to orient its search strategy from the information obtained from a conspecific. It first had to smell the mouth of a companion having just eaten a food item, and then search for same quality food in the field. The results showed that subjects adjusted their foraging speed according to the value of the reward to be found. They were able to recognize the food resource on the basis of the item previously eaten by their companion. In a second experiment, we asked whether the subjects could anticipate a given food quantity from smelling a companion associated with that given food quantity. When testing whether subjects oriented their search strategy on the basis of companion's identity, they did not appear to use it as a referential cue to food quantity. They nonetheless adapted their foraging speed according to food value. Both experiments indicated that macaques are liable to assess and select food from information extracted from conspecifics, and hence avoid some costs associated with individual food searching.     

A Longitudinal Test of the Belief that Companion Animal Ownership Can Help Reduce Loneliness

ABSTRACT

The widely held belief that companion animal ownership can help to reduce loneliness was tested using a quasi-experimental longitudinal design. Over a six-month period, 59 participants completed the UCLA-Loneliness Scale when they were seeking to acquire a companion animal. Participants' loneliness was measured again six-months after their initial recruitment, by which time 35 of the 59 participants had acquired a new companion animal. There was no evidence that companion animal acquisition helped to reduce levels of loneliness, irrespective of whether participants already owned a companion animal at the time of seeking to acquire a new companion animal, or the type of companion animal that was acquired. There was no evidence that participants who ultimately acquired a new companion animal differed from participants who did not, suggesting that the findings were not a consequence of a self-selection bias. The perseverance and apparent strength of the belief that companion animal ownership can alleviate loneliness is discussed in relation to the current findings.     

Serotonin Transporter Genotype Modulates Social Reward and Punishment in Rhesus Macaques

Background

Serotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans.

Methodology/Principal Findings

In contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a “pay-per-view” task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos.

Conclusions/Significance

These data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.     

Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Hierarchical organization of femaleMacaca radiata in captivity

Females of several species of macaques form cohesive matrilineal units in which all members share a collective status. The relationship between rank and kinship inMacaca radiata has not previously been studied. Analysis of observations of social interactions in a large and stable captive group ofM. radiata and longitudinal study of kinship and reproductive success indicate that with few exceptions a matrilineal dominance hierarchy exists in that group. Four young, upwardly mobile females are responsible for the exceptions. Contrary to the pattern noted in other species of macaques, several adult females outrank their daughters. Old age and deteriorating physical condition of mothers appear to be associated with mother-daughter rank reversals. The age and lineage size of females when they entered the group have had a lasting impact. Females who entered the group as adults have achieved higher rank and greater reproductive success than females who entered the group as juveniles without relatives. This research was conducted at the California Primate Research Center in Davis, supported by USPHS grant RR00169.     

The Social Facilitation of Drinking: What is Facilitated,and Who is Affected?

The effect of a drinking companion on conspecifics was investigated using domestic hens (Callus gallus domesticus). The two aims of the investigation were firstly to see whether drinking is sensitive to social facilitation, and if so, to see whether it follows the same pattern as that of feeding, i.e. whether it acts primarily on the drinking behaviour rather than the amount ingested. The second aim was to see whether differences in how influenced the birds were by a drinking companion correlated with one or more social or non-social traits. Social facilitation was measured by comparing the intake and number of ‘head-ups’ (i.e. swallowing) of an individual in the presence of a thirsty or non-thirsty companion. The traits measured were as follows: the rank within each pair, social dependence/fear, reaction to a novel object, reaction in a feeding-inhibition test, and finally weight (as a possible index of the overall rank of the birds in the group). Social facilitation of drinking occurs but acts primarily on drinking behaviour (number of ‘head ups’); birds do not swallow as much per ‘head up’ as when they themselves are thirsty. The lightest (possibly most subdominant) birds were also the ones most influenced by the drinking conspecific. Furthermore, the heaviest (possibly most dominant) individuals were the ones with the shortest social distance and the longest latency in approaching a novel object. This meant that the birds that were most influenced by a drinking companion were also the individuals that were least fearful and showed the highest degree of exploration.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Inequity aversion in relation to effort and relationship quality in long-tailed Macaques (Macaca fascicularis)

Social animals may employ evolved implicit rules to maintain a balance between cooperation and competition. Inequity aversion (IA), the aversive reaction to an unequal distribution of resources, is considered such a rule to avoid exploitation between cooperating individuals. Recent studies have revealed the presence of IA in several nonhuman species. In addition, it has been shown that an effort is crucial for this behavior to occur in animals. Moreover, IA may well depend on the partner's identity. Although dominant individuals typically monopolize food, subordinate individuals obtain less preferred food and usually do not protest. Furthermore, "friends" may pay less attention to equity than "nonfriends." We tested whether long-tailed macaques show IA with different cost-benefit ratios. In addition, we determined whether IA depends on relationship quality (RQ). Dominant subjects expressed IA only when a small effort was required. At a very large effort, however, long-tailed macaques did not show IA, possibly owing to bottom effects on the number of rewards they aim to receive. Moreover, and contrary to our predictions, an individual's inequity response was similar when tested with a "friend" or a "nonfriend." Therefore, we conclude that long-tailed macaques show IA only in conditions of moderate effort, yet that IA seems independent of RQ. Furthermore, IA may not be domain specific. Altogether, IA may be a trait present in all species that habitually cooperate, independent of their social organization.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Stability of social status rankings of female cynomolgus monkeys,of varying reproductive condition,in different social groups

In order test the hypothesis that adult female macaques display a tendency to attain a certain level of social status independent of the social situation, the social status rankings of 41 wild-caught adult female Macaca fascicularis were determined in different social groups. About one-third of the females were intact and housed with vasectomized males. About one-third of the females were ovariectomized and housed with intact males, and the remaining females were intact and housed with intact males in order to allow pregnancy to occur. Within each of these experimental groups, females were housed in social groups of 4–6 females and 1 male, and the constituency of these groups was changed every 3 months for 22 months. Thus, females lived in eight different social groups. The correlations between the social status rankings of individual females while living in different social groups were positive and significant. The majority of the females were either stable dominants or stable subordinates in 75% of the groups in which they lived, which was a significant proportion of the study population. The stability of social status rankings was higher in the ovariectomized than in the pregnant and intact groups; however, this was not a significant difference. In the context of the results of previous studies, these findings suggest that the social status of an individual is the result of both the immediate social environment and some inherent characteristic(s) of the individual that promotes the likelihood that under most social circumstances an individual will display a predictable level of social status.     

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

Social grooming in Tonkean macaques (Macaca tonkeana)

The distribution, form, and contexts of occurrence of social grooming were studied in two captive groups of Tonkean macaques (Macaca tonkeana), using interaction-dependent sampling. The social events surrounding grooming had little influence on its form, the participants' behavior being shaped mainly by physical constraints. Adult females were most often involved in grooming interactions. Grooming between adult females appeared more intimate than that between adult males and females. Kinship and dominance had no effect on the form or distribution of social grooming among adult females. It is concluded that social systems that are characterized by mild dominance relations allow individuals the freedom to interact in the way and with whom they wish.     

Coordination and consensus:the role of compromisers in Tibetan macaques

Coordination and consensus in collective behavior have attracted a lot of research interest. Although previous studies have investigated the role of compromisers in group consensus, they provide little insight into why compromisers would allow such social arrangements to persist. In this study, the potential relationship between group movements and conflict management in Tibetan macaques in Anhui province, China, was investigated using hierarchical cluster analyses. Some members with higher social centrality or social rank often formed a front-runner cluster during group movements. They had higher leadership success than individuals outside the front-runner cluster. Other members with lower social centrality or social rank often followed the group movements initiated by the front-runner cluster, and thus formed the compromiser cluster. Compromisers’ proximity relations with front-runners increased with their following scores to front-runners. Compromisers had fewer events of being attacked when they followed group movements initiated by the front-runners. The compromising process made compromisers lose the choice of direction preference, but it could increase their individual safeties. This trade-off suggests that compromisers play a role of decision-maker in coordination and consensus scenarios among social animals.     

A Neural Circuit Covarying with Social Hierarchy in Macaques

Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals'' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals'' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.