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.

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.

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.

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.

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.

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.

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.

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.

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 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.

Dominance in a socially dynamic setting: hierarchical structure and conflict dynamics in ravens' foraging groups.

Dominance hierarchies typically emerge in systems where group members regularly encounter and compete for resources. In birds, the 'open' and dynamic structure of foraging groups may prevent the emergence of structured hierarchies, although this assumption have hardly been tested. We report on agonistic data for ravens Corvus corax, collected over two 18-month periods for 183 marked individuals of a wild (fluid) population and 51 birds from six captive (stable) groups. We show that the dominance structure (steep and transitive) in wild foraging groups is strikingly similar to that found in captivity. In the wild, we found that higher ranks are mainly occupied by males, older and more aggressive individuals that also tend to receive fewer aggressions. Exploring the mechanisms sustaining the wild dominance structure, we confirmed that males are more aggressive than females and, with age, tend to receive fewer aggressions than females. Males that are about to leave the foraging groups for some months are less aggressive than newcomers or locals, while newcomers are specifically targeted by aggressions in their first year (as juveniles). Taken together, our results indicate that the socially dynamic conditions ravens face during foraging do not hinder, but provide opportunities for, using (advanced) social cognition. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Socio-ecological correlates of neophobia in corvids.

Behavioral responses to novelty, including fear and subsequent avoidance of novel stimuli, i.e., neophobia, determine how animals interact with their environment. Neophobia aids in navigating risk and impacts on adaptability and survival. There is variation within and between individuals and species; however, lack of large-scale, comparative studies critically limits investigation of the socio-ecological drivers of neophobia. In this study, we tested responses to novel objects and food (alongside familiar food) versus a baseline (familiar food alone) in 10 corvid species (241 subjects) across 10 labs worldwide. There were species differences in the latency to touch familiar food in the novel object and novel food conditions relative to the baseline. Four of seven socio-ecological factors influenced object neophobia: (1) use of urban habitat (versus not), (2) territorial pair versus family group sociality, (3) large versus small maximum flock size, and (4) moderate versus specialized caching (whereas range, hunting live animals, and genus did not), while only maximum flock size influenced food neophobia. We found that, overall, individuals were temporally and contextually repeatable (i.e., consistent) in their novelty responses in all conditions, indicating neophobia is a stable behavioral trait. With this study, we have established a network of corvid researchers, demonstrating potential for further collaboration to explore the evolution of cognition in corvids and other bird species. These novel findings enable us, for the first time in corvids, to identify the socio-ecological correlates of neophobia and grant insight into specific elements that drive higher neophobic responses in this avian family group. VIDEO ABSTRACT.

People that score high on psychopathic traits are less likely to yawn contagiously.

Considerable variation exists in the contagiousness of yawning, and numerous studies have been conducted to investigate the proximate mechanisms involved in this response. Yet, findings within the psychological literature are mixed, with many studies conducted on relatively small and homogeneous samples. Here, we aimed to replicate and extend upon research suggesting a negative relationship between psychopathic traits and yawn contagion in community samples. In the largest study of contagious yawning to date (N = 458), which included both university students and community members from across 50 nationalities, participants completed an online study in which they self-reported on their yawn contagion to a video stimulus and completed four measures of psychopathy: the primary and secondary psychopathy scales from the Levenson Self-Report Psychopathy Scale (LSRPS), the psychopathy construct from the Dirty Dozen, and the Psychopathic Personality Traits Scale (PPTS). Results support previous findings in that participants that yawned contagiously tended to score lower on the combined and primary measures of psychopathy. That said, tiredness was the strongest predictor across all models. These findings align with functional accounts of spontaneous and contagious yawning and a generalized impairment in overall patterns of behavioral contagion and biobehavioral synchrony among people high in psychopathic traits.

Exploring the Cognitive Capacities of Japanese Macaques in a Cooperation Game.

Cooperation occurs amongst individuals embedded in a social environment. Consequently, cooperative interactions involve a variety of persistent social influences such as the dynamics of partner choice and reward division. To test for the effects of such dynamics, we conducted cooperation experiments in a captive population of Japanese macaques (Macaca fuscata, N = 164) using a modified version of the loose-string paradigm in an open-experiment design. We show that in addition to becoming more proficient cooperators over the course of the experiments, some of the macaques showed sensitivity to the presence of potential partners and adjusted their behavior accordingly. Furthermore, following an unequal reward division, individuals receiving a lesser reward were more likely to display aggressive and stress-related behaviors. Our experiments demonstrate that Japanese macaques have some understanding of the contingencies involved in cooperation as well as a sensitivity to the subsequent reward division suggestive of an aversion to inequity.

Carrion Crows and Azure-Winged Magpies Show No Prosocial Tendencies When Tested in a Token Transfer Paradigm.

To study the evolution of humans' cooperative nature, researchers have recently sought comparisons with other species. Studies investigating corvids, for example, showed that carrion crows and azure-winged magpies delivered food to group members when tested in naturalistic or simple experimental paradigms. Here, we investigated whether we could replicate these positive findings when testing the same two species in a token transfer paradigm. After training the birds to exchange tokens with an experimenter for food rewards, we tested whether they would also transfer tokens to other birds, when they did not have the opportunity to exchange the tokens themselves. To control for the effects of motivation, and of social or stimulus enhancement, we tested each individual in three additional control conditions. We witnessed very few attempts and/or successful token transfers, and those few instances did not occur more frequently in the test condition than in the controls, which would suggest that the birds lack prosocial tendencies. Alternatively, we propose that this absence of prosociality may stem from the artificial nature and cognitive complexity of the token transfer task. Consequently, our findings highlight the strong impact of methodology on animals' capability to exhibit prosocial tendencies and stress the importance of comparing multiple experimental paradigms.

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.

Brain size and neuron numbers drive differences in yawn duration across mammals and birds.

Recent studies indicate that yawning evolved as a brain cooling mechanism. Given that larger brains have greater thermolytic needs and brain temperature is determined in part by heat production from neuronal activity, it was hypothesized that animals with larger brains and more neurons would yawn longer to produce comparable cooling effects. To test this, we performed the largest study on yawning ever conducted, analyzing 1291 yawns from 101 species (55 mammals; 46 birds). Phylogenetically controlled analyses revealed robust positive correlations between yawn duration and (1) brain mass, (2) total neuron number, and (3) cortical/pallial neuron number in both mammals and birds, which cannot be attributed solely to allometric scaling rules. These relationships were similar across clades, though mammals exhibited considerably longer yawns than birds of comparable brain and body mass. These findings provide further evidence suggesting that yawning is a thermoregulatory adaptation that has been conserved across amniote evolution.

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.

Experimental evidence for yawn contagion in orangutans (Pongo pygmaeus).

Yawning is highly contagious, yet both its proximate mechanism(s) and its ultimate causation remain poorly understood. Scholars have suggested a link between contagious yawning (CY) and sociality due to its appearance in mostly social species. Nevertheless, as findings are inconsistent, CY's function and evolution remains heavily debated. One way to understand the evolution of CY is by studying it in hominids. Although CY has been found in chimpanzees and bonobos, but is absent in gorillas, data on orangutans are missing despite them being the least social hominid. Orangutans are thus interesting for understanding CY's phylogeny. Here, we experimentally tested whether orangutans yawn contagiously in response to videos of conspecifics yawning. Furthermore, we investigated whether CY was affected by familiarity with the yawning individual (i.e. a familiar or unfamiliar conspecific and a 3D orangutan avatar). In 700 trials across 8 individuals, we found that orangutans are more likely to yawn in response to yawn videos compared to control videos of conspecifics, but not to yawn videos of the avatar. Interestingly, CY occurred regardless of whether a conspecific was familiar or unfamiliar. We conclude that CY was likely already present in the last common ancestor of humans and great apes, though more converging evidence is needed.