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.

A comparative study of mirror self-recognition in three corvid species.

Mirror self-recognition (MSR) assessed by the Mark Test has been the staple test for the study of animal self-awareness. When tested in this paradigm, corvid species return discrepant results, with only the Eurasian magpies and the Indian house crow successfully passing the test so far, whereas multiple other corvid species fail. The lack of replicability of these positive results and the large divergence in applied methodologies calls into question whether the observed differences are in fact phylogenetic or methodological, and, if so, which factors facilitate the expression of MSR in some corvids. In this study, we (1) present new results on the self-recognition abilities of common ravens, (2) replicate results of azure-winged magpies, and (3) compare the mirror responses and performances in the mark test of these two corvid species with a third corvid species: carrion crows, previously tested following the same experimental procedure. Our results show interspecies differences in the approach of and the response to the mirror during the mirror exposure phase of the experiment as well as in the subsequent mark test. However, the performances of these species in the Mark Test do not provide any evidence for their ability of self-recognition. Our results add to the ongoing discussion about the convergent evolution of MSR and we advocate for consistent methodologies and procedures in comparing this ability across species to advance this discussion.

Hand preference predicts behavioral responses to threats in Barbary macaques.

The structure and functioning of the brain are lateralized-the right hemisphere processes unexpected stimuli and controls spontaneous behavior, while the left deals with familiar stimuli and routine responses. Hemispheric dominance, the predisposition of an individual using one hemisphere over the other, may lead to behavioral differences; particularly, an individual may be programed to act in a certain way concerning hemispheric dominance. Hand preference is a robust estimator of hemispheric dominance in primates, as each hemisphere controls the opposing side of the body. Studies have found links between hand preference and the exhibition of behaviors in contexts such as exploring and manipulating objects. However, little is known whether hand preference predicts behavioral variations in other ecologically relevant contexts like predation. We investigated the relationship between hand preference and behavioral responses to two types of predator models in captive Barbary macaques (Macaca sylvanus) (n = 22). Besides, a nonpredator novel object was included as control. We found 91% of the macaques to be lateralized with no group-level bias. A higher rate of tension and focus (behavioral response) behavior was found in predator contexts than in the novel object condition. Unlike their right-hand counterparts, individuals with a strong left-hand preference elicited frequent focus and tension behavior toward the predator models. Additionally, the behavioral response varied with predator type. We also found an interaction effect between hand preference and predator type. Our study suggests that hand preference can reliably predict behavioral variations in the context of potential predation. While these results are consistent with lateralized brain function, indicating lateralization a neural mechanism of behavioral variation, the interaction effect between hand preference and predator type elucidates the importance of context-specificity when investigating laterality noninvasively. Future research on other nonhuman primates using the current framework may provide insights into the evolution of laterality and underlying behavioral predispositions.

A novel methodological approach for group classification during fission of a semi-free-ranging group of Japanese macaques (Macaca fuscata).

The self-initiated split of a social group, known as fission, is a challenge faced by many group-living animals. The study of group fission and the social restructuring process in real time provides insights into the mechanism of this biologically important process. Previous studies on fission in Japanese macaques (Macaca fuscata) assigned individuals to newly reorganized groups mainly using behavioral observations and group attendance records based on periods before or after fission itself. Here, we present a novel framework for group classification during the process of fission that uses quantifiable behavioral variables and statistical analyses. The framework was tested on a group fission process at Affenberg Landskron (Austria), a park that housed around 160 semi-free-ranging Japanese macaques. The behavioral data were collected for 26 days during fission. We analyzed three behavioral developments recurrent in fissions in Japanese macaques, that is, independence of behavior, participation in group movements, and separation of nomadic ranges. These analyses were combined to assign individuals to different groups. Our study resulted in one main group (N = 33), one subgroup (N = 36) and 56 individuals whose group membership was still undefined. The demographic characteristics of these newly formed groups were comparable with those of fissioned groups in wild populations. Furthermore, we found that these newly forming groups showed early social dynamics of fission five months before group level movements, that is: grouping based on spatial proximity and spatial withdrawal of the subgroup to the periphery. These results underline the validity of our novel framework to study social dynamics in Japanese macaques during the process of fission. It represents an important addition to existing methods, and we recommend testing its scope in other primate societies.

Measuring salivary mesotocin in birds - Seasonal differences in ravens' peripheral mesotocin levels.

Oxytocin is involved in a broad array of social behaviours. While saliva has been used regularly to investigate the role of oxytocin in social behaviour of mammal species, so far, to our knowledge, no-one has tried to measure its homolog, mesotocin, in birds' saliva. Therefore, in this study we measured salivary mesotocin in common ravens (Corvus corax), and subsequently explored its link to three aspects of raven sociality. We trained ravens (n = 13) to voluntarily provide saliva samples and analysed salivary mesotocin with a commercial oxytocin enzyme-immunoassay kit, also suitable for mesotocin. After testing parallelism and recovery, we investigated the effect of bonding status, sex and season on mesotocin levels. We found that mesotocin was significantly more likely to be detected in samples taken during the breeding season (spring) than during the mating season (winter). In those samples in which mesotocin was detected, concentrations were also significantly higher during the breeding than during the mating season. In contrast, bonding status and sex were not found to relate to mesotocin detectability and concentrations. The seasonal differences in mesotocin correspond to behavioral patterns known to be associated with mesotocin/oxytocin, with ravens showing much more aggression during the mating season while being more tolerant of conspecifics in the breeding season. We show for the first time that saliva samples can be useful for the non-invasive determination of hormone levels in birds. However, the rate of successfully analysed samples was very low, and collection and analysis methods will benefit from further improvements.

Temporal consistency and ecological validity of personality structure in common marmosets (Callithrix jacchus): A unifying field and laboratory approach.

Personality in animals has been extensively researched in recent decades. Temporal consistency of behaviors is almost always part of the personality definition and is usually explored in several different testing sessions or observation periods. However, it is still unclear whether the obtained personality constructs are stable across several years, which might be especially important for long-living animals, such as primates. Further, little is known on whether the personality structures obtained in the laboratory reflect the structures obtained under ecologically relevant conditions in the wild. Therefore, we conducted a battery of personality tests on common marmosets (Callithrix jacchus) (N = 27), compared it with a test battery conducted 4 years beforehand on a subset of animals in captivity (N = 13) and ran an adapted version under field conditions at Baracuhy Biological Field Station, Brazil (N = 18). Under captive conditions, we found a remarkably similar personality structure across 4 testing years. Further, we found high long-term temporal consistency in the first two personality components, Boldness and Exploration; however, monkeys that changed their social (i.e., breeding) status between the two testing periods showed a significant increase in Boldness scores. Under field conditions, we found a somewhat similar personality structure as compared to the laboratory, which to some extent corroborates ecological validity of our personality test design. Nevertheless, whether the structure in the wild is suppressed or expanded in comparison to captivity, and in which way the social setting influences personality structure, should be further explored. Taken together, our results contribute to the discussion about the reliability and ecological validity of personality structures in nonhuman primates.

Kea cooperate better with sharing affiliates.

Controlled studies that focus on intraspecific cooperation tasks have revealed striking similarities, but also differences, in abilities across taxa as diverse as primates, fish, and birds. Such comparisons may provide insight into the specific socio-ecological selection pressures that led to the evolution of cooperation. Unfortunately, however, compared to primates data on birds remain relatively scarce. We tested a New Zealand psittaciform, the kea, in a dyadic cooperation task using the loose-string design. During trials our subjects were in separate compartments, but obtained a common reward that could be divided multiple ways, allowing the examination of reward division effects. Ten individuals were tested twice in 44 combinations of partners. Dyads with a high affiliation score attempted to cooperate more often and were also more often successful in doing so. Furthermore, dyads that shared rewards more equally seemed to be more likely to attempt cooperation in the next trial. Like other bird and some monkey species, but unlike, for example, chimpanzees, kea did not spontaneously show understanding of either the role of the partner or the mechanism behind the cooperation task. This may point to true disparities between species, but may also be due to differences in task design and/or the amount of exposure to similar tasks and individual skills of the subjects.

Proactive prosociality in a cooperatively breeding corvid, the azure-winged magpie (Cyanopica cyana).

One of the contemporary hypotheses concerning the evolution of human altruism is the cooperative breeding hypothesis (CBH) which has recently been tested in non-human primates. Using a similar paradigm, we investigated prosociality in a cooperatively breeding corvid, the azure-winged magpie. We found that the magpies delivered food to their group members at high rates, and unlike other corvids, they did so without any cues provided by others. In two control conditions, the magpies stopped participating over time, indicating that they learned to discriminate prosocial tests from controls. Azure-winged magpies are thus the first birds that experimentally show proactive prosociality. Our findings are in line with the CBH; however, additional corvid species need to be tested in this promising paradigm.

Consistent inter-individual differences in common marmosets (Callithrix jacchus) in Boldness-Shyness, Stress-Activity, and Exploration-Avoidance.

The study of animal personality, defined as consistent inter-individual differences in correlated behavioral traits stable throughout time and/or contexts, has recently become one of the fastest growing areas in animal biology, with study species ranging from insects to non-human primates. The latter have, however, only occasionally been tested with standardized experiments. Instead their personality has usually been assessed using questionnaires. Therefore, this study aimed to test 21 common marmosets (Callithrix jacchus) living in three family groups, in five different experiments, and their corresponding controls. We found that behavioral differences between our animals were not only consistent over time, but also across different contexts. Moreover, the consistent behaviors formed a construct of four major non-social personality components: Boldness-Shyness in Foraging, Boldness-Shyness in Predation, Stress-Activity, and Exploration-Avoidance. We found no sex or age differences in these components, but our results did reveal differences in Exploration-Avoidance between the three family groups. As social environment can have a large influence on behavior of individuals, our results may suggest group-level similarity in personality (i.e., "group personality") in common marmosets, a species living in highly cohesive social groups. Am. J. Primatol. 78:961-973, 2016. © 2016 Wiley Periodicals, Inc.

Preliminary evidence that eye appearance in parrots (Psittaciformes) co-varies with latitude and altitude.

External eye appearance in avian taxa has been proposed to be driven by social and ecological functions. Recent research in primates suggests, instead, that, photoprotective functions are important drivers of external eye appearance. Using similar methods, we examined the variation in external eye appearance of 132 parrot species (Psittaciformes) in relation to their ecology and sociality. Breeding systems, flock size and sexual dimorphism, as well as species' latitude and maximum living altitude, and estimated UV-B incidence in species' ranges were used to explore the contribution of social and ecological factors in driving external eye appearance. We measured the hue and brightness of visible parts of the eye and the difference in measurements of brightness between adjacent parts of the eye. We found no link between social variables and our measurements. We did, however, find a negative association between the brightness of the inner part of the iris and latitude and altitude. Darker inner irises were more prevalent farther away from the equator and for those species living at higher altitudes. We found no link between UV-B and brightness measurements of the iris, or tissue surrounding the eye. We speculate that these results are consistent with an adaptation for visual functions. While preliminary, these results suggest that external eye appearance in parrots is influenced by ecological, but not social factors.

Investigating the effects of prenatal testosterone exposure (via 2D:4D) and socio-relational factors on 3-6-year-old preschoolers' prosocial choices.

BACKGROUND AND AIMS: Prosocial behavior such as helping and sharing develops early in childhood. Yet very few studies have investigated physiological and relational factors shaping prosociality among children. Here, we systematically examined the role of prenatal androgen exposure alongside prestige, dominance, and friendship in 3-6-year-old preschoolers' prosocial sharing with familiar peers. METHODS: We tested a sample of 65 children, predominately of European descent. We used a cost-free direct-interaction prosocial choice task to assess children's prosocial tendencies. Second-to-fourth digit ratio (2D:4D) was used as a retrospective biomarker for prenatal androgen exposure. Prestige was measured through behavioral observations of interaction partners and visual regard, dominance through teacher questionnaires, and friendship via peer preference assessments. RESULTS: We found that children acted prosocially when tested with a familiar peer. Children with lower 2D:4D (higher prenatal androgen exposure) behaved more prosocially. Further, there were marginal associations between the donors' prosocial tendencies and their visual regard as a proxy of their prestige (positive effect) and their teacher-rated dominance relative to the recipient (negative effect). Neither age, sex, nor friendship influenced prosocial choices. CONCLUSIONS: Prenatal androgen exposure, approximated via 2D:4D, was associated with prosocial behavior. In contrast to previous research in older children, higher exposure was related to stronger prosocial tendencies, which corresponds to earlier findings on fairness in adults. Our findings point towards a potential role of sex steroids in the early development of children's social behavior, but they have to be interpreted with caution due to the small sample size of the current study. Nevertheless, they underscore the importance of integrating biological and psychological perspectives, while also highlighting the significance of studying the development of prosocial behavior within peer groups.

Behavioral, physiological, and genetic drivers of coping in a non-human primate.

Animals experience stressful situations, from predation to social conflicts, but mostly deal with them successfully. This adaptive mechanism, coping, reduces the adverse effects of stressors, and its failure may result in reduced fitness. Substantial inter-individual variation in coping is observed, yet little is known about how behavioral, physiological and genetic drivers regulate coping holistically and contribute to such variations. We assessed behavioral coping styles (n=30), emotional arousal (n=12), and personalities (n=32) of long-tailed macaques (Macaca fascicularis) and also investigated the association of coping with a valine/methionine polymorphism encoded by a critical human stress regulatory gene, catechol-O-methyltransferase (COMT) (n=26). Personality and the human equivalent COMT Val/Met polymorphism were associated with "nonaggression-based" and "aggression-based" coping styles. Compared to nonaggression-based, aggression-based copers maintained higher average facial temperatures, indicating potentially lower emotional arousal, as measured using infrared thermography. These findings demonstrate a complex interplay of various proximate mechanisms governing coping in a non-human primate.

A behavioral view on chimpanzee personality: exploration tendency, persistence, boldness, and tool-orientation measured with group experiments.

Human and nonhuman animals show personality: temporal and contextual consistency in behavior patterns that vary among individuals. In contrast to most other species, personality of chimpanzees, Pan troglodytes, has mainly been studied with non-behavioral methods. We examined boldness, exploration tendency, persistence and tool-orientation in 29 captive chimpanzees using repeated experiments conducted in an ecologically valid social setting. High temporal repeatability and contextual consistency in all these traits indicated they reflected personality. In addition, Principal Component Analysis revealed two independent syndromes, labeled exploration-persistence and boldness. We found no sex or rank differences in the trait scores, but the scores declined with age. Nonetheless, there was considerable inter-individual variation within age-classes, suggesting that behavior was not merely determined by age but also by dispositional effects. In conclusion, our study complements earlier rating studies and adds new traits to the chimpanzee personality, thereby supporting the existence of multiple personality traits among chimpanzees. We stress the importance of ecologically valid behavioral research to assess multiple personality traits and their association, as it allows inclusion of ape studies in the comparison of personality structures across species studied behaviorally, and furthers our attempts to unravel the causes and consequences of animal personality.

Prosociality in a despotic society.

Prosociality is the intent to improve others' well-being. Existing hypotheses postulate that enhanced social tolerance and inter-individual dependence may facilitate prosocial preferences, which may favor the evolution of altruism. While most studies are restricted to "tolerant" (cooperatively breeding and self-domesticated) species, despotic societies provide an alternative opportunity to investigate prosociality due to nepotism and ample inter-individual dependencies. Japanese macaques live in hierarchical matrilineal societies, with strong kin bonds. Besides, tolerance among non-kin may persist through reciprocity. Using a group service food-provision paradigm, we found prosocial preferences in a semi free-ranging group of Japanese macaques. The extent of provisioning was at levels comparable to tolerant species. Dyadic tolerance predicted the likelihood and magnitude of provisioning, while kinship predicted the magnitude. We emphasize the role of a complex socio-ecology fostering individual prosocial tendencies through kinship and tolerance. These findings necessitate a framework including different forms of interdependence beyond the generally tolerant species.

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.

Personality and social environment predict cognitive performance in common marmosets (Callithrix jacchus).

Consistent inter-individual variation in cognition has been increasingly explored in recent years in terms of its patterns, causes and consequences. One of its possible causes are consistent inter-individual differences in behaviour, also referred to as animal personalities, which are shaped by both the physical and the social environment. The latter is particularly relevant for group-living species like common marmosets (Callithrix jacchus), apt learners that display substantial variation in both their personality and cognitive performance, yet no study to date has interlinked these with marmosets' social environment. Here we investigated (i) consistency of learning speed, and (ii) whether the PCA-derived personality traits Exploration-Avoidance and Boldness-Shyness as well as the social environment (i.e., family group membership) are linked with marmosets' speed of learning. We tested 22 individuals in series of personality and learning-focused cognitive tests, including simple motor tasks and discrimination learning tasks. We found that these marmosets showed significant inter-individual consistency in learning across the different tasks, and that females learned faster than males. Further, bolder individuals, and particularly those belonging to certain family groups, learned faster. These findings indicate that both personality and social environment affect learning speed in marmosets and could be important factors driving individual variation in cognition.

No Evidence for Contagious Yawning in Juvenile Ravens (Corvus corax): An Observational Study.

The overt and reflexive matching of behaviors among conspecifics has been observed in a growing number of social vertebrates, including avian species. In general, behavioral contagion-such as the spread of yawning-may serve important functions in group synchronization and vigilance behavior. Here, we performed an exploratory study to investigate yawn contagion among 10 captive juvenile ravens (Corvus corax), across two groups. Using observational methods, we also examined the contagiousness of three other distinct behaviors: stretching, scratching, and shaking. A total of 44 20 min observations were made across both groups, including 28 in the morning and 16 in the afternoon. The time and occurrence of all the behaviors from each bird were coded, and the temporal pattern of each behavior across both groups was then analyzed to assess the degree of social contagion. Overall, we found no evidence for contagious yawning, stretching, scratching, or shaking. However, yawns were relatively infrequent per observation (0.052 ± 0.076 yawns/bird) and thus experimental methods should be used to support this finding.

Personality as a Predictor of Time-Activity Budget in Lion-Tailed Macaques (Macaca silenus).

Time-activity budget, i.e., how a population or an individual divides their day into various behaviours and activities, is an important ecological aspect. Existing research primarily focused on group-level time-activity budgets, while individual variations have only been reported recently. However, little is known about how consistent inter-individual differences or personalities influence time-activity budgets. We examined the personalities of lion-tailed macaques (Macaca silenus) and investigated their influence on individual time-activity budgets. The resulting personality traits, namely persistence, sociability, affiliation, and anxiety, were used to predict the three broad categories of the time-activity budget-food-related, active, and resting behaviours. We found that persistence and sociability positively predicted the time spent being active. Food-related behaviours were positively predicted by persistence, while anxiety was found to influence them negatively. The time spent resting was negatively predicted by persistence. We did not find an effect of affiliation on the time-activity budgets. We discuss these findings in light of the ecology of lion-tailed macaques. Our study highlights the importance of a novel approach that uses animal personality traits as predictors of individual time-activity budgets and offers insights regarding the use of personality assessments in conservation and welfare activities.

My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals.

Do nonhuman animals (henceforth, animals) have emotions, and if so, are these similar to ours? This opinion piece aims to add to the recent debate about this question and provides a critical re-evaluation of what can be concluded about animal and human emotions. Emotions, and their cognitive interpretation, i.e., feelings, serve important survival functions. Emotions, we believe, can exist without feelings and are unconsciously influencing our behavior more than we think, and possibly more so than feelings do. Given that emotions are expressed in body and brain, they can be inferred from these measures. We view feelings primarily as private states, which may be similar across closely related species but remain mostly inaccessible to science. Still, combining data acquired through behavioral observation with data obtained from noninvasive techniques (e.g., eyetracking, thermography, hormonal samples) and from cognitive tasks (e.g., decision-making paradigms, cognitive bias, attentional bias) provides new information about the inner states of animals, and possibly about their feelings as well. Given that many other species show behavioral, neurophysiological, hormonal, and cognitive responses to valenced stimuli equivalent to human responses, it seems logical to speak of animal emotions and sometimes even of animal feelings. At the very least, the contemporary multi-method approach allows us to get closer than ever before. We conclude with recommendations on how the field should move forward.