Personality heterophily and friendship as drivers for successful cooperation.

Cooperation is widespread and arguably a pivotal evolutionary force in maintaining animal societies. Yet, proximately, what underlying motivators drive individuals to cooperate remains relatively unclear. Since 'free-riders' can exploit the benefits by cheating, selecting the right partner is paramount. Such decision rules need not be based on complex calculations and can be driven by cognitively less-demanding mechanisms, like social relationships (e.g. kinship, non-kin friendships, dyadic tolerance), social status (e.g. dominance hierarchies) and personalities (social and non-social traits); however, holistic evidence related to those mechanisms is scarce. Using the classical 'loose-string paradigm', we tested cooperative tendencies of a hierarchical primate, the long-tailed macaque (Macaca fascicularis). We studied three groups (n = 21) in their social settings, allowing partner choice. We supplemented cooperation with observational and experimental data on social relationships, dominance hierarchies and personality. Friendship and dissimilarities in non-social 'exploration' and 'activity-sociability' personality traits predicted the likelihood of cooperative dyad formation. Furthermore, the magnitude of cooperative success was positively associated with friendship, low rank-distance and dissimilarity in the activity-sociability trait. Kinship did not affect cooperation. While some findings align with prior studies, the evidence of (non-social) personality heterophily promoting cooperation may deepen our understanding of the proximate mechanisms and, broadly, the evolution of cooperation.

The ability to inhibit impulses is related to social behavior in long-tailed macaques.

Performance in cognitive tasks has been linked to differences in species' social organization, yet to understand its function its relationship to within-species variation in behavior should also be explored. One important cognitive capacity, the ability to inhibit impulses, is typically better in egalitarian than despotic primate species and in primate species with strong fission-fusion dynamics. A different line of research indicates that a high ability to inhibit impulses is related to less aggressive behavior and more socio-positive behavior. However, within species the relationship between performance on cognitive inhibition tasks and variation in social behavior remains to be explored. Here we investigate how performance in a typical inhibition task in cognitive research is related to aggressive and socio-positive behavior in despotic long-tailed macaques. Twenty individuals living in two naturalistic mixed-sex groups were tested with the Plexiglass Hole Task. Aggressive behavior and three types of socio-positive behavior (neutral/friendly approaches, socio-positive signaling, and grooming others) among group members were measured. Individuals differed in their ability to inhibit impulses. Individuals that were not good at inhibiting impulses showed higher rates of aggressive behavior, but also more socio-positive signals, whereas inhibition was not related to neutral/friendly approaches and grooming. These results confirm the positive link between impulsiveness and aggression. In addition, the results indicate that some social-positive behavior may be enhanced when inhibition is limited. In this species, benefits potentially derived from aggression and socio-positive signals match a low ability to inhibit impulses, suggesting that a low ability to inhibit impulses may actually be advantageous. To understand differences between species in cognitive skills, understanding the benefits of variation in a cognitive capacity within a species is crucial.

Food sharing with friends and acquaintances: A study in preschool boys and girls.

Introduction: The current study examined whether preschoolers in a (semi-)natural situation shared more food with friends or acquaintances, and whether this was different between boys and girls, older and younger children, and for preferred and non- preferred food. In order to do so, we replicated and extended the classical work of Birch and Billman in a Dutch sample. Methods: Participants included 91 children aged between 3 to 6 years (52.7% boys, 93.4% Western European) from a middle- to upper-middle-class neighborhood in the Netherlands. Results: The results revealed that children shared more non-preferred than preferred food with others. Girls gave more non-preferred food to acquaintances than to friends, whereas boys gave more to friends than to acquaintances. No effect of relationship was found for preferred food. Older children shared more food than younger children. Compared to acquaintances, friends made more active attempts to get food. Moreover, children who were not shared with were just as likely to share food as children who were shared with. Discussion: Overall, only a small degree of agreement with the original study was found: Some significant findings could not be replicated, and some unconfirmed hypotheses of the original study were supported. The results underscore both the need for replications and studying the effect of social-contextual factors in natural settings.

Does tolerance allow bonobos to outperform chimpanzees on a cooperative task? A conceptual replication of Hare et al., 2007.

Across various taxa, social tolerance is thought to facilitate cooperation, and many species are treated as having species-specific patterns of social tolerance. Yet studies that assess wild and captive bonobos and chimpanzees result in contrasting findings. By replicating a cornerstone experimental study on tolerance and cooperation in bonobos and chimpanzees (Hare et al. 2007 Cur. Biol. 17, 619-623 (doi:10.1016/j.cub.2007.02.040)), we aim to further our understanding of current discrepant findings. We tested bonobos and chimpanzees housed at the same facility in a co-feeding and cooperation task. Food was placed on dishes located on both ends or in the middle of a platform. In the co-feeding task, the tray was simply made available to the ape duos, whereas in the cooperation task the apes had to simultaneously pull at both ends of a rope attached to the platform to retrieve the food. By contrast to the published findings, bonobos and chimpanzees co-fed to a similar degree, indicating a similar level of tolerance. However, bonobos cooperated more than chimpanzees when the food was monopolizable, which replicates the original study. Our findings call into question the interpretation that at the species level bonobos cooperate to a higher degree because they are inherently more tolerant.

Individual behavioral correlates of tail biting in pre-finishing piglets.

Introduction: Tail biting is a widespread problem in pig production systems and has a negative impact on both animal welfare and farm income. This explorative study aims to validate how tail biting is related to general behaviors at the individual level and explore whether these behaviors are related to a particular type of tail biting: two-stage, sudden-forceful, obsessive, or epidemic. Methods: This research was conducted in a standard commercial setting where 89 tail-docked pre-finishing piglets divided into 8 groups were observed 4 days per week from 5 to 8 weeks of age. Each piglet was observed for a total of 160 min using continuous focal sampling. Ten individual behaviors were recorded based on the general behaviors expected to be linked to giving tail biting (PCA1), receiving tail biting (PCA2), and tail biting damage (PCA3). These PCAs were assembled and related to tail biting given, tail biting received, and tail biting lesions. Results: Tail biting did not lead to major damage on the piglets' tail at 8 weeks of age but was observed 420 times, where most of the individuals (72%) were categorized as "biters and victims." When relating PCA1 with tail biting given, piglets that gave more tail biting showed more "active exploration." When relating PCA2 with tail biting received, piglets receiving more tail biting were more "explored while active" and "attacked and explored." When relating PCA2 with tail biting lesions, piglets presenting lesions showed more "agonism." Surprisingly, tail biting lesions were not significantly related to PCA3. The relationship between explorative behaviors and tail biting indicates that the pre-damage stage of two-stage tail biting was the predominant tail biting type, while the damaging stage was likely incipient. The relationship between tail biting and aggression, as well as the minor tail lesions observed suggest that sudden-forceful tail biting was probably present even though it was rarely seen. Obsessive and epidemic tail biting were not observed. Discussion: This study demonstrates that studying tail biting at the individual level helps to identify the type of tail biting present. This gives directions to farmers for applying appropriate measures to prevent the development of tail biting behavior in piglets.

Multigenerational Social Housing and Group-Rearing Enhance Female Reproductive Success in Captive Rhesus Macaques (Macaca mulatta).

To optimize costs and reproductive success, rhesus macaques in biomedical primate research facilities are often peer-reared. Older, dependent infants are typically removed from their natal group to enhance female reproduction. The minimal husbandry age-norm of infant removal is ten months. These practices deviate from species-specific behavior and may reduce welfare, suggesting a trade-off between female reproduction and welfare. However, the effect of breeding group type and rearing history on female reproductive success (i.e., birth rate; inter-birth interval (IBI); offspring survival) is unclear. This retrospective study investigated whether group type (i.e., peer groups versus multigenerational groups) and rearing history (i.e., peer- or hand-reared; group-reared with peer- or hand-reared mother; group-reared) affected female reproductive success in captive rhesus macaques. Data on female reproduction between 1996 and 2019 were collected at the Biomedical Primate Research Centre, Rijswijk. Birth rates were higher in multigenerational breeding groups than in peer groups. Moreover, group-reared females had higher offspring survival than peer- or hand-reared females. IBI was not affected by breeding group type or female rearing history. However, females in both peer and multigenerational breeding groups typically conceived earlier after giving birth than the husbandry infant removal age-norm of ten months. Thus, infant removal at an age of ten months does not enhance a female's reproduction. Altogether, female reproduction and non-human primate welfare can simultaneously be optimized through multigenerational breeding groups and group-rearing.

The Older the Better: Infanticide Is Age-Related for Both Victims and Perpetrators in Captive Long-Tailed Macaques.

In wild primates, infanticide is a risk that is especially prevalent when a new male takes over the alpha position. Insight into risk factors related to infanticide may decrease the incidence of infanticide in captivity during male introductions. We investigated several risk factors of infanticide derived from hypotheses explaining infanticide in the wild and tested this in captive long-tailed macaques (Macaca fascicularis) using demographic data spanning a 25.5-year period. Factors that are related to infanticide in the wild explained a large proportion, but not all incidences, of infanticide in captivity. Consistent with the wild data, infants young enough to decrease the interbirth interval (<215 days) were at risk of being killed. In contrast to studies from the wild, infanticidal males were more than 2.5 years younger than non-infanticidal males. This indicates that captive settings can lead to new risks since relatively young males may gain the alpha position, promoting infanticide. Therefore, we propose the adolescent male risk hypothesis as a captive risk factor in which subadult males pose a risk of infanticide. In conclusion, the ages of both males and infants are related to infanticide in captivity and have to be taken into account during male introductions.

External environmental conditions impact nocturnal activity levels in proboscis monkeys (Nasalis larvatus) living in Sabah, Malaysia.

Recently, several diurnal nonhuman anthropoids have been identified displaying varying degrees of nocturnal activity, which can be influenced by activity "masking effects"-external events or conditions that suppress or trigger activity, temporarily altering normal activity patterns. Environmental masking characteristics include nocturnal temperature, rainfall, cloud cover, and moon brightness. Similarly, other ecological characteristics, including proximity to humans and predators and daytime activity, may also trigger or suppress nocturnal activity. Understanding the effects of external conditions on activity patterns is pertinent to effective species conservation. We investigated the presence of nocturnal activity and the influence of masking effects on the level of nocturnal activity displayed by wild proboscis monkeys (Nasalis larvatus) in Sabah, Malaysian Borneo. Dual-axis accelerometers were attached by collar to six male proboscis monkeys from different one-male, multi-female groups to record activity continuously (165-401 days each). We measured the monkeys' nocturnal and diurnal activity levels and investigated the effects of seven potential masking effects. Nocturnal activity was much lower than diurnal activity. Still, proboscis monkeys did display varying levels of nocturnal activity. Generalized linear mixed models identified higher nocturnal activity in the study individuals during nights with cooler temperatures, higher rainfall, and after higher diurnal activity. These three masking effects affected nocturnal activity levels during the observation period that informed our model, although they did not predict nocturnal activity outside of this period. While the generalizability of these results remains uncertain, this study highlights the utility of accelerometers in identifying activity patterns and masking effects that create variability in these patterns.

Overweight Management through Mild Caloric Restriction in Multigenerational Long-Tailed Macaque Breeding Groups.

Caloric restriction (CR) is an effective method to reduce overweight in captive non-human primates (NHPs). CR has been applied to individually- and pair-housed NHPs, but whether applying CR can be effective and safe in group-housed NHPs has not yet been assessed. This study investigates the effect of mild (20%) CR on adult overweight and biochemical parameters, immature growth, veterinary consultations, and reproductive success in multigenerational long-tailed macaque (Macaca fascicularis) breeding groups. Data were derived from anthropometric measurements and blood samples during yearly health checks, complemented with retrospective data on veterinary consultations and reproductive success. Adult body measures decreased after CR, with heavier individuals and females losing more weight compared to leaner individuals and males. CR lowered cholesterol levels in adults but had no overall effect on other biochemical parameters. Yet, biochemical parameters of individuals with high baseline values were reduced more compared to individuals with low baseline values. Immature growth, veterinary consultations and reproductive success were not influenced by CR. Thus, CR targeted the right individuals, i.e., overweight adults, and had no adverse effects on the variables examined in this study. This implies that mild CR can be a valuable overweight management strategy in group-housed NHPs.

Risso's dolphins perform spin dives to target deep-dwelling prey.

Foraging decisions of deep-diving cetaceans can provide fundamental insight into food web dynamics of the deep pelagic ocean. Cetacean optimal foraging entails a tight balance between oxygen-conserving dive strategies and access to deep-dwelling prey of sufficient energetic reward. Risso's dolphins (Grampus griseus) displayed a thus far unknown dive strategy, which we termed the spin dive. Dives started with intense stroking and right-sided lateral rotation. This remarkable behaviour resulted in a rapid descent. By tracking the fine-scale foraging behaviour of seven tagged individuals, matched with prey layer recordings, we tested the hypothesis that spin dives are foraging dives targeting deep-dwelling prey. Hunting depth traced the diel movement of the deep scattering layer, a dense aggregation of prey, that resides deep during the day and near-surface at night. Individuals shifted their foraging strategy from deep spin dives to shallow non-spin dives around dusk. Spin dives were significantly faster, steeper and deeper than non-spin dives, effectively minimizing transit time to bountiful mesopelagic prey, and were focused on periods when the migratory prey might be easier to catch. Hence, whereas Risso's dolphins were mostly shallow, nocturnal foragers, their spin dives enabled extended and rewarding diurnal foraging on deep-dwelling prey.

Retrospective Evaluation of a Minor Dietary Change in Non-Diabetic Group-Housed Long-Tailed Macaques (Macaca fascicularis).

Macaques in captivity are prone to becoming overweight and obese, which may cause several health problems. A diet that mimics the natural diet of macaques may prevent these problems and improve animal welfare. Adjusting captive diets towards a more natural composition may include increasing fiber content and lowering the glycemic index, i.e., reducing the impact on blood glucose levels. Such a dietary change was implemented in our long-tailed macaque (Macaca fascicularis) breeding colony. The basic diet of monkey chow pellets remained the same, while the supplementary provisioning of bread was replaced by grains and vegetables. This study is a retrospective evaluation, based on electronic health records, that investigated whether this minor dietary change had a beneficial effect on relative adiposity and overweight-related health parameters in 44 non-diabetic, group-housed, female long-tailed macaques. Relative adiposity was measured with a weight-for-height index and blood samples were collected during yearly health checks. Glycemic response and lipid metabolism were evaluated using several biochemical parameters. Relative adiposity and overweight status did not differ after dietary change. Yet, relatively heavy individuals generally lost body weight, while relatively lean individuals gained body weight, leading to a more balanced body weight dynamic. Dietary change did not affect HbA1c and triglyceride levels, while fructosamine and cholesterol levels were significantly reduced. Thus, the minor dietary change had no significant effect on overweight status, but some biochemical parameters related to the risk of diabetes and cardiovascular disease were positively affected. This study emphasizes the importance of evaluating husbandry changes and that critically reviewing husbandry practices can provide valuable insights to improve animal health and welfare.

Effect of Housing Conditions on Cortisol and Body Fat Levels in Female Rhesus Macaques.

Macaques are among the most commonly used non-human primates in biomedical research. They are highly social animals, yet biomedical studies often require group-living animals to be pair-housed in a controlled environment. A change in environment causes only short-term stress in adapting individuals, while non-adapting animals may experience long-term stress that can adversely affect study results. Individuals likely differ in their ability to adapt depending on individual characteristics. Changes in cortisol and body fat levels may reflect these different individual responses. Here, we investigate the long-term effect of a change from group- to pair-housing on cortisol and body fat levels in 32 female rhesus macaques, exploring whether age, dominance rank, original cortisol, and body fat levels are related to long-term stress in pair-housing. Hair samples were analyzed for cortisol levels, while anthropometric measurements and computed tomography were performed to quantify body fat. Monkeys served as their own control with a 7.5-month period between the measurements. Cortisol levels increased, while average body fat levels did not differ when individuals were moved from group- to pair-housing. Cortisol and body fat levels were not significantly correlated. Changes in cortisol were independent of age and dominance rank, whereas individual variation in body fat alterations was related to the group-housed body fat level and dominance rank. Although this study did not identify individual characteristics related to long-term stress in pair-housing, the individual variation confirms that some individuals are more resilient to change than others and provides possibilities for future refinement studies.

Emotional bookkeeping and differentiated affiliative relationships: Exploring the role of dynamics and speed in updating relationship quality in the EMO-model.

Emotional bookkeeping is the process by which primates integrate the emotional effects of social interactions to form internal representations of their affiliative relationships. The dynamics and speed of this process, which comprises the formation, maintenance and fading out of affiliative relationships, are not clear. Empirical data suggest that affiliative relationships are slowly formed and do not easily fade out. The EMO-model, an agent-based model designed to simulate the social life of primates capable of emotional bookkeeping, was used to explore the effects of different types of internal relationship dynamics and speeds of increase and decrease of relationship strength. In the original EMO-model the internal dynamics involves a fast built-up of a relationship independent of its current quality, alongside a relatively fast fading out of relationship quality. Here we explore the effect of this original dynamics and an alternative dynamics more in line with empirical data, in combination with different speeds of internal relationship quality increase and decrease, on the differentiation and stability of affiliative relationships. The alternative dynamics leads to more differentiated and stable affiliative relationships than the original dynamics, especially when the speed with which internal relationship quality increases is low and the speed with which it decreases is intermediate. Consequently, individuals can groom different group members with varying frequency and support a rich social life with stable preferred partners and attention to several others. In conclusion, differentiated and stable affiliative relationships are especially formed when friends are not made too quickly and not forgotten too easily.

A Stepwise Male Introduction Procedure to Prevent Inbreeding in Naturalistic Macaque Breeding Groups.

Male introductions into captive primate breeding groups can be risky and unsuccessful. However, they are necessary to prevent inbreeding in naturalistic breeding groups. The procedure used to introduce new individuals may affect the success and influence the risks associated with group introductions. At the Biomedical Primate Research Centre (BPRC) in Rijswijk, the Netherlands, male rhesus macaque (Macaca mulatta) introductions into naturalistic social groups with a matrilineal structure and without a breeding male achieve relatively high success rates. This paper describes the male introduction procedure used at the BPRC. Males are stepwise familiarized with and introduced to their new group, while all interactions between the new male and the resident females are closely monitored. Monitoring the behaviour of the resident females and their new male during all stages of the introduction provides crucial information as to whether or not it is safe to proceed. The BPRC introduction procedure is widely applicable and may improve the management of captive primate groups in any housing facility worldwide. Thus, the careful introduction management can minimize the risk associated with male introductions and enhance the welfare of captive primates.

Organized to learn: the influence of social structure on social learning opportunities in a group.

Social learning, which is a mechanism that allows an individual to acquire skills from other individuals, occurs in a social context. Therefore, factors that influence social context, like social structure, will impact social learning opportunities. This review explores how features of social structure affect social learning opportunities in primates, either through their relationship with social tolerance or through the number of social learning models. Features that are investigated in this review and that we hypothesize affect social learning opportunities are parental investment, dominance hierarchy, nepotism, social bonds, dispersal, group size, fission-fusion dynamics, and sex ratio. For most of these features we find evidence, but support varies. Of all primate species, only humans show all the requirements of an optimal social structure to promote social learning. Future research into social learning and culture should not overlook the social context in which it takes place.

How to Get the Biggest Slice of the Cake. A Comparative View of Social Behaviour and Resource Access in Human Children and Nonhuman Primates.

Social complexity results from engaging in different classes of social behaviour. The presence of different classes of social behaviour is reflected in multidimensional concepts of social asymmetry, found in both human and nonhuman primates. Based on an overview of such concepts, we propose that three classes of social behaviour are involved in having access to scarce and desired resources: next to aggressive and affiliative behaviour, also action indicating behaviour (i.e., inspire another individual to follow one's example or intentions) may lead to resource access. Studies with nonhuman primate and human children show that the contribution of aggression and affiliation to resource access has been widely documented and that there is initial support for action indicating behaviour. In addition, the studies show similarities and differences in conceptualization and approach that may inspire future research. Future research should address the (in)dependency of the behavioural dimensions, their relative importance, individual differences in combined expression and the type of resources accessed. Only a multi-dimensional view on behaviour leading to resource access will highlight the benefits of social complexity.

Tolerant and intolerant macaques show different levels of structural complexity in their vocal communication.

We tested the social complexity hypothesis which posits that animals living in complex social environments should use complex communication systems. We focused on two components of vocal complexity: diversity (number of categories of calls) and flexibility (degree of gradation between categories of calls). We compared the acoustic structure of vocal signals in groups of macaques belonging to four species with varying levels of uncertainty (i.e. complexity) in social tolerance (the higher the degree of tolerance, the higher the degree of uncertainty): two intolerant species, Japanese and rhesus macaques, and two tolerant species, Tonkean and crested macaques. We recorded the vocalizations emitted by adult females in affiliative, agonistic and neutral contexts. We analysed several acoustic variables: call duration, entropy, time and frequency energy quantiles. The results showed that tolerant macaques displayed higher levels of vocal diversity and flexibility than intolerant macaques in situations with a greater number of options and consequences, i.e. in agonistic and affiliative contexts. We found no significant differences between tolerant and intolerant macaques in the neutral context where individuals are not directly involved in social interaction. This shows that species experiencing more uncertain social interactions displayed greater vocal diversity and flexibility, which supports the social complexity hypothesis.

Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques.

Many animal species cooperate with conspecifics in various social contexts. While ultimate causes of cooperation are being studied extensively, its proximate causes, particularly endocrine mechanisms, have received comparatively little attention. Here, we present a study investigating the link between the hormone cortisol, cooperation and social bonds in long-tailed macaques (Macaca fascicularis). We tested 14 macaques in a dyadic cooperation task (loose-string paradigm), each with two partners of different social bond strength and measured their salivary cortisol before and after the task. We found no strong link between the macaques' cortisol level before the task and subsequent cooperative success. By contrast, we did find that the act of cooperating in itself led to a subsequent decrease in cortisol levels, but only when cooperating with closely bonded individuals. Two control conditions showed that this effect was not due to the mere presence of such an individual or the pulling task itself. Consequently, our study shows an intricate way in which the hypothalamic-pituitary-adrenal axis is involved in cooperation. Future studies should reveal whether and how our findings are driven by the anxiolytic effect of oxytocin, which has been associated with social bonding.

Low relationship quality predicts scratch contagion during tense situations in orangutans (Pongo pygmaeus).

Primates show various forms of behavioral contagion that are stronger between kin and friends. As a result, behavioral contagion is thought to promote group coordination, social cohesion, and possibly state matching. Aside from contagious yawning, little is known about the contagious effect of other behaviors. Scratching is commonly observed during arousal and as such may play a role within group dynamics. While the Bornean orangutan (Pongo pygmaeus) is commonly considered the least social great ape, orangutans do engage in social interactions. Therefore, their social organization makes them a suitable case for studying the social function of behavioral contagion. Through behavioral observations of captive orangutans, we recorded all yawn and scratch events together with the corresponding behavior of all bystander group-members. As yawning was rarely observed, no conclusions could be drawn regarding this behavior. Scratching was contagious and occurred within 90 s after the triggering scratch. Specifically, orangutans showed increased scratch contagion when they had seen a weakly bonded individual scratch during tense contexts. When the orangutan had not seen the triggering scratch, the contagiousness of scratching was not affected by context or relationship quality. Our results indicate that behavioral contagion is not simply higher between individuals with stronger social relationships, but that the contagiousness of behaviors may vary based on the context and on social factors. We discuss these findings in light of an adaptive function that may reduce aggression.

Emotional expressions in human and non-human great apes.

Humans and great apes are highly social species, and encounter conspecifics throughout their daily lives. During social interactions, they exchange information about their emotional states via expressions through different modalities including the face, body and voice. In this regard, their capacity to express emotions, intentionally or unintentionally, is crucial for them to successfully navigate their social worlds and to bond with group members. Darwin (1872) stressed similarities in how humans and other animals express their emotions, particularly with the great apes. Here, we show that emotional expressions have many conserved, yet also a number of divergent features. Some theorists consider emotional expressions as direct expressions of internal states, implying that they are involuntary, cannot be controlled and are inherently honest. Others see them as more intentional and/ or as indicators of the actor's future behavior. After reviewing the human and ape literature, we establish an integrative, evolutionary perspective and provide evidence showing that these different viewpoints are not mutually exclusive. Recent insights indicate that, in both apes and humans, some emotional expressions can be controlled or regulated voluntarily, including in the presence of audiences, suggesting modulation by cognitive processes. However, even non-intentional expressions such as pupil dilation can nevertheless inform others and influence future behavior. In sum, while showing deep evolutionary homologies across closely related species, emotional expressions show relevant species variation.