Manual preference, performance, and dexterity for bimanual grass-feeding behavior in wild geladas (Theropithecus gelada).

We assessed whether wild geladas, highly specialized terrestrial grass eaters, are lateralized for bimanual grass-plucking behavior. According to the literature, we expected that complex motor movements in grass feeding would favor the emergence of a population-level hand bias in these primates. In addition, we described geladas' manual behavior based on systematic observations of several individuals. Our study group included 28 individuals belonging to a population of free-ranging geladas frequenting the Kundi plateau, Ethiopia. We filmed monkeys while feeding on grass, and hand preference and performance were coded. Geladas performed more plucking movements per second with their left hand (LH) compared to the right one and preferred their LH both to start and finish collection bouts. Also, the rhythmic movements of each hand had a significant tendency toward isochrony. Finally, geladas used forceful pad-to-pad precision grips, in-hand movements, and compound grips to pluck and collect grass blades, considered the most advanced manual skills in primate species. The LH's leading role suggests an advantage of the right hemisphere in regulating geladas' bimanual grass-feeding behavior. The tactile input from the hands and/or rhythmic hand movements might contribute to explaining this pattern of laterality. Our findings highlighted the importance of adopting multiple laterality measures to investigate manual laterality. Moreover, the need to speed up the execution time of manual foraging might be a further important factor in studying the evolution of manual laterality and dexterity in primates.

Getting rid of blinkers: the case of mirror self-recognition in horses (Equus caballus).

The commentary by Gallup and Anderson (Anim Cogn https://doi.org/10.1007/s10071-021-01538-9 , 2021) on the original article by Baragli, Scopa, Maglieri, and Palagi (Anim Cogn https://doi.org/10.1007/s10071-021-01502-7 , 2021) raised some concerns about the methodological approach used by the authors to demonstrate Mirror Self-Recognition (MSR) in horses. The commentary does not take into account horse physiology and psychology, leading Gallup and Anderson to inappropriately discredit the findings obtained by Baragli et al. Anim Cogn 2021. In this reply, we underlined the importance of a blinker-free approach to understand the evolutionary processes at the basis of animal cognition.

If horses had toes: demonstrating mirror self recognition at group level in Equus caballus.

Mirror self-recognition (MSR), investigated in primates and recently in non-primate species, is considered a measure of self-awareness. Nowadays, the only reliable test for investigating MSR potential skills consists in the untrained response to a visual body mark detected using a reflective surface. Here, we report the first evidence of MSR at group level in horses, by facing the weaknesses of methodology present in a previous pilot study. Fourteen horses were used in a 4-phases mirror test (covered mirror, open mirror, invisible mark, visible colored mark). After engaging in a series of contingency behaviors (looking behind the mirror, peek-a-boo, head and tongue movements), our horses used the mirror surface to guide their movements towards their colored cheeks, thus showing that they can recognize themselves in a mirror. The analysis at the group level, which 'marks' a turning point in the analytical technique of MSR exploration in non-primate species, showed that horses spent a longer time in scratching their faces when marked with the visible mark compared to the non-visible mark. This finding indicates that horses did not see the non-visible mark and that they did not touch their own face guided by the tactile sensation, suggesting the presence of MSR in horses. Although a heated debate on the binary versus gradualist model in the MSR interpretation exists, recent empirical pieces of evidence, including ours, indicate that MSR is not an all-or-nothing phenomenon that appeared once in phylogeny and that a convergent evolution mechanism can be at the basis of its presence in phylogenetically distant taxa.

Not all yawns tell the same story: The case of Tonkean macaques.

Here we show for the first time that the plasticity in morphology and duration of yawning in Macaca tonkeana can be associated with different functional contexts. Macaca tonkeana is classified as a tolerant macaque species characterized by social interactions minimally constrained by dominance rank or kinship. Tonkean macaques, as other egalitarian species, rely on a complex facial communicative system. We found that the degree of mouth opening (ranging from covered to uncovered tooth yawns) and the duration of yawning were not strictly dependent. The shortest uncovered tooth yawns were associated with an intense locomotor/physical activity and peaked immediately after stressful social events thus indicating an increase in arousal. In contrast, longer yawns, independently from teeth exposure, were primarily associated with a relaxed state of the subject. In conclusion, our study suggests that to explore the potential different functions of yawning, it is necessary to focus on the variability of its expression both in terms of morphology and duration, because not all yawns tell the same story.

Earlier than previously thought: Yawn contagion in preschool children.

Yawning is a primitive and stereotyped motor action involving orofacial, laryngeal, pharyngeal, thoracic and abdominal muscles. Contagious yawning, an involuntarily action induced by viewing or listening to others' yawns, has been demonstrated in human and several non-human species. Previous studies with humans showed that infants and preschool children, socially separated during video experiments, were not infected by others' yawns. Here, we tested the occurrence of yawn contagion in 129 preschool children (ranging from 2.5 to 5.5 years) belonging to five different classes by video recording them in their classrooms during the ordinary school activities. As it occurs in adult humans, children of all ages were infected by others' yawns within the 2 min after the perception of the stimulus. The yawn contagion occurred earlier than previously thought. For children, it appears that the natural social setting is more conducive to yawn contagion than the inherently artificial experimental approach. Moreover, children's gender did not affect the level of contagious yawning. The neural, emotional and behavioural traits of preschool children are probably not sufficiently mature to express variability between boys and girls; nevertheless, children appeared to be already well equipped with the 'neural toolkit' necessary for expressing yawn contagion.

Sharing playful mood: rapid facial mimicry in Suricata suricatta.

One of the most productive behavioural domains to study visual communication in mammals is social play. The ability to manage play-fighting interactions can favour the development of communicative modules and their correct decoding. Due to their high levels of social cohesion and cooperation, slender-tailed meerkats (Suricata suricatta) are a very good model to test some hypotheses on the role of facial communication in synchronizing playful motor actions. We found that the relaxed open mouth (ROM), a playful facial expression conveying a positive mood in several social mammals, is also present in meerkats. ROM was mainly perceived during dyadic playful sessions compared to polyadic ones. We also found that meerkats mimic in a very rapid and automatic way the ROM emitted by playmates (Rapid Facial Mimicry, RFM). RFM was positively correlated with the relationship quality shared by subjects, thus suggesting that the mimicry phenomenon is socially modulated. Moreover, more than the mere presence of isolated ROMs, the presence of at RFM prolonged the duration of the play session. Through RFM animals can share the emotional mood, they are experiencing and this appears to be particularly adaptive in those species, whose relationships are not inhibited by rank rules and when animals build and maintain their bonds through social affiliation. The meerkat society is cohesive and cooperative. Such features could have, therefore, favoured the evolution of facial mimicry, a phenomenon linked to emotional contagion, one of the most basic forms of empathy.

Calming an aggressor through spontaneous post-conflict triadic contacts: Appeasement in Macaca tonkeana.

Peaceful third-party interventions usually occur after an aggressive encounter and can be directed toward the victim or the aggressor. Macaca tonkeana, a cercopithecine species characterized by high levels of tolerance, frequently engage in consolatory contacts, which both calm the victim and reduce the probability of further attacks against him/her. Other post-conflict affiliative interventions such as reconciliation and quadratic affiliation are also common in this species. However, little attention has been given to contacts directed toward the aggressor. Here, we explore the role of bystander affiliative interventions toward the aggressor in influencing the affective state of the aggressor and the consequences of triadic interventions at group level. We found that triadic post-conflict affiliation occurred independently from the intensity of the conflict and that it was more frequent in absence of the conciliatory contact between the opponents (reconciliation). Bystanders showed a higher amount of post-conflict affiliation toward low ranking aggressors. Post-conflict triadic affiliation functioned as a tension reduction mechanism by lowering the arousal of the aggressor, which less frequently engaged in renewed aggression. All these findings suggest that post-conflict triadic contacts in Tonkean macaques can be considered as a strategic mechanism to calm the aggressor and reduce the risk of retaliatory aggression.

Integrating Tinbergen's inquiries: Mimicry and play in humans and other social mammals.

Visual signals convey emotions and intentions between individuals. Darwin underlined that human facial expressions represent a shared heritage between our species and many other social mammals. Social play is a fertile field to examine the role and the potential communicative function of facial expressions. The relaxed open-mouth (or play face) is a context-specific playful expression, which is widespread in human and non-human mammals. Here, we focus on playful communication by applying Tinbergen's four areas of inquiry: proximate causation, ontogeny, function, and evolution. First of all we explore mimicry by focusing on its neural substrates and factors of modulation within playful and non-playful context (proximate causation). Play face is one of the earliest facial expressions to appear and be mimicked in neonates. The motor resonance between infants and their caregivers is essential later in life when individuals begin to engage in increasingly complex social interactions, including play (ontogeny). The success of a playful session can be evaluated by its duration in time. Mirroring facial expressions prolongs the session by favoring individuals to fine-tune their own motor sequences accordingly (function). Finally, through a comparative approach we also demonstrate that the elements constituting play communication and mimicry are sensitive to the quality of interindividual relationships of a species, thus reflecting the nature of its social network and style (evolution). In conclusion, our goal is to integrate Tinbergen's four areas of ethological inquiry to provide a broader framework regarding the importance of communication and mimicry in the play domain of humans and other social mammals.

Emotionality and intentionality in bonobo playful communication.

Great apes show very complex systems for communicating emotions and intentions. Whereas gestures are intentional signals, facial expressions can disclose both emotions and intentions. The playful context is a good field to explore the possible dichotomy between intentionally and emotionally driven signals as it has been suggested that one of its functions is to learn producing and decoding communicative patterns. To understand how signals are produced during play and how they are modified in the course of ontogeny, we investigated the use of playful facial expressions and gestures in bonobos (Pan paniscus), a tolerant species showing a high propensity to play even as adults. Our results showed that the use of play faces and gestures is strongly influenced by the characteristics of the play session. Both play faces and gestures were more often performed when social play involved physical contact and when the receiver was visually attending, thus suggesting that both signals can be strategically employed when communicating becomes more urgent. Compared to play faces, gestures were more frequent during dyadic than polyadic sessions, when a unique receiver was involved. Being gestures not context specific, they are probably used more selectively by the sender. On the contrary, play faces are context specific and transmit an unequivocal positive message that cannot be misconceived. These features legitimize a broad use of playful facial expressions, independently of the number of playmates. The similarities and differences in the production of these signals are probably linked to the different degree of emotionality and intentionality characterizing them.

Testing yawning hypotheses in wild populations of two strepsirrhine species: Propithecus verreauxi and Lemur catta.

Yawning, although easily recognized, is difficult to explain. Traditional explanations stressed physiological mechanisms, but more recently, behavioral processes have received increasing attention. This is the first study to test a range of hypotheses on yawning in wild primate populations. We studied two sympatric strepsirrhine species, Lemur catta, and Propithecus verreauxi, of the Ankoba forest (24.99°S, 46.29°E, Berenty reserve) in southern Madagascar. Sexual dimorphism is lacking in both species. However, their differences in ecological and behavioral characteristics facilitate comparative tests of hypotheses on yawning. Our results show that within each species males and females yawned with similar frequencies supporting the Dimorphism Hypothesis, which predicts that low sexual dimorphism leads to little inter-sexual differences in yawning. In support of the State Changing Hypothesis yawning frequencies was linked to the sleep-wake cycle and punctuated transitions from one behavior to another. Accordingly, yawning frequencies were significantly higher in L. catta than in P. verreauxi, because L. catta has a higher basal level of activity and consequently a higher number of behavioral transitions. In agreement with the Anxiety Hypothesis, yawning increased significantly in the 10 min following predatory attacks or aggression. Our findings provide the first empirical evidence of a direct connection between anxiety and yawning in lemurs. Our results show that yawning in these two strepsirrhines occurs in different contexts, but more research will be necessary to determine if yawns are a single, unitary behavior.

Being a victim or an aggressor: Different functions of triadic post-conflict interactions in wolves (Canis lupus lupus).

Animals adopt different behavioral strategies to cope with the conflict of interests coming from the competition over limited resources. Starting from the study on chimpanzees, post-conflict third-party affiliation (the affiliative contact provided by a third-party toward the victim--VTA--or the aggressor--ATA) was investigated mainly in primates. Later, this post-conflict mechanism has been demonstrated also in other mammals, such as wallabies, horses, dolphins, domestic dogs, and wolves. Here, we present data on triadic post-conflict affiliation in wolves (Canis lupus lupus) by exploring some of the hypotheses already proposed for primates and never tested before in other social mammals. In this carnivore species, the study of VTA and ATA revealed that these strategies cannot be considered as a unique behavioral category since they differ in many functional aspects. VTA serves to protect the victim by reducing the likelihood of reiterated attacks from the previous aggressor and to reinforce the relationship shared by the third-party and the victim. On the other hand, ATA has a role in bystander protection by limiting the renewed attacks of the previous aggressor toward uninvolved group-members (potential third-parties). In conclusion, exploring VTA and ATA gives the opportunity to concurrently demonstrate some functional differences in triadic post-conflict affiliation according to the different targets of bystanders (victims or aggressors). The data comparison between primates and other social mammals should permit to open new lines of research.

Play to learn, teach by play.

The synthesis provided by Kline in the target article is noteworthy, but ignores the inseparable role of play in the evolution of learning and teaching in both humans and other animals. Play is distinguished and advantaged by its positive feedback reinforcement through pleasure. Play, especially between adults and infants, is probably the platform from which human learning and teaching evolved.

Relaxed open mouth as a playful signal in wild ring-tailed lemurs.

Play signals are commonly used by animals to communicate their playful motivation and to limit the risk that rough acts are misunderstood by playmates. The relaxed open mouth is the most common facial expression performed during play in many mammals and represents the ritualized version of the movement anticipating a play bite. The signaling nature of this expression has been proven in many haplorrhine species but never demonstrated in strepsirrhines. Our purpose was assessing whether, also in strepsirrhines, the relaxed open mouth has an actual communicative function. We studied wild ring-tailed lemurs (Lemur catta), characterized by highly social habits including intense playful interactions. They largely use playful signals, mostly performed with the black and white tail. The signaling function of the tail (tail play) has been widely demonstrated. We analyzed both tail play and the relaxed open mouth to verify how their distribution is affected by different play variables (e.g., play session symmetry, number of play mates, previous use of the same pattern). Indeed, ring-tailed lemurs use the relaxed open mouth as a communicative signal during play. Relaxed open mouth was more frequent during unbalanced interactions showing the highest asymmetry in the patterns performed by the two players (offensive/neutral). Compared to tail play, relaxed open mouth was more frequent during dyadic than polyadic interactions and, as a highly directional signal, it was more frequently replicated by the play mate. Therefore, the relaxed open mouth needs to be performed face-to-face so that signal detection can be optimized. Similar to previous findings in monkeys and apes, the relaxed open mouth in lemurs seems to be a ritualized signal used to engage and, perhaps, sustain playful interaction.

The sound of yawns makes geladas yawn.

Yawning is undeniably contagious and hard to resist. Interestingly, in our species, even the mere sound of a yawn can trigger this contagious response, especially when the yawner is someone familiar. Together with humans, one other mammal species is known to produce loud and distinct vocalisations while yawning, Theropithecus gelada. Geladas are known for their complex social interactions and rich vocal communication, making them intriguing subjects for studying yawning behaviour. To explore the contagious effect of yawn sounds on geladas, we conducted playback experiments in a zoo-housed colony with animals living in two groups. We exposed them to yawn sounds (Test) or affiliative grunts (Control) produced by males from either their own group or the other one. The results were remarkable, as simply hearing yawn sounds led to yawn contagion in geladas, with multiple responses observed when the yawns came from members of their own group. This finding adds a significant contribution to the research on mimicry and behavioural contagion in primates. Moreover, it raises intriguing questions about the involvement of sensory modalities beyond visual perception in these phenomena.

More than a simple fixed action pattern: Yawning in drills.

In the last decade, increasing attention has been devoted to exploring some aspects of yawning in non-human animals. With their chin red mark, bony paranasal swellings, male large brains and long canines, drills (Mandrillus leucophaeus) offer a robust model for testing hypotheses on the phenomenon. We identified two yawn variants (covered, YCT and uncovered teeth, YUCT) which differ in terms of recruitment of muscular action units (AUs). We tested the effects of several variables (sex, dominance rank, context) on the duration of the yawn and the probability of YCT or YUCT occurrence. We found that males performed longer and more YUCT than females. These findings support the Brain Cooling Hypothesis suggesting that those species showing large brains tend to display larger and longer yawns. We also tested the State Changing Hypothesis predicting the presence of a temporal association of yawning and ongoing behavioral transitions. A sequential analysis revealed that after 30 s following a yawn, drills were significantly more likely to change their behavioral state. Through the observation of yawning, conspecifics might gain knowledge of impending state changes. Seeing other's yawns increased the probability of a similar response in the observers, thus suggesting the presence of yawn contagion in drills. Although the dataset needs to be expanded, our findings indicate that yawning is variable in drills, it can be associated with subjects' state changes, and the imminent shifts can be perceived/processed by conspecifics.

Animal play and evolution: Seven timely research issues about enigmatic phenomena.

The nature of play in animals has been long debated, but progress is being made in characterizing play and its variants, documenting its distribution across vertebrate and invertebrate taxa, describing its mechanisms and development, and proposing testable theories about its origins, evolution, and adaptive functions. To achieve a deeper understanding of the functions and evolution of play, integrative and conceptual advances are needed in neuroscience, computer modeling, phylogenetics, experimental techniques, behavior development, and inter- and intra-specific variation. The special issue contains papers documenting many of these advances. Here, we describe seven timely areas where further research is needed to understand this still enigmatic class of phenomena more fully. Growing empirical and theoretical evidence reveals that play has been crucial in the evolution of behavior and psychology but has been underestimated, if not ignored, in both empirical and theoretical areas of evolutionary biology and neuroscience. Play research has important ramifications for understanding the evolution of cognition, emotion, and culture, and research on animals can be both informative and transformative.

Adult play and the evolution of tolerant and cooperative societies.

Play is generally considered an immature affair. However, adult play is present in several mammal species living in complex social systems. Here, I hypothesize that adult social play is favored by natural selection in those species characterized by high level of social tolerance and/or by the need of others' cooperation to reach a goal (i.e., leverage). The integration and comparison of bio-behavioral data on non-human primates and wild social carnivores allows drawing a comprehensive picture on the importance of adult play in facing unpredictable, novel social situations and in overcoming stressful experiences. The ability to cope with potentially competitive interactions through play can favor the emergence of egalitarian societies. A further interesting and beneficial aspect of adult play is its role in synchronizing group activities and favoring collective decision making by renovating the motivation to cooperate in groupmates. As a last step, some considerations about the presence of adult play in the most egalitarian and cooperative human groups (e.g., hunter-gatherer societies) allows discussing the apparent dichotomy between cultural and biological evolution of certain behavioral traits, including social play in adulthood.

Record of thanatology and cannibalism in drills (Mandrillus leucophaeus).

Comparative thanatology includes the scientific study of death in non-human animals, which involves emotional, social, and exploratory responses of individuals and groups towards corpses. Stillborn babies and dead infants often elicit maternal and alloparental care that can persist for days, weeks, or even months, especially in primates. After this period, cannibalistic acts can occur not only by groupmates but also by the mother. Such cannibalism has been reported both in captive and wild primate groups, suggesting that the phenomenon is evolutionary adaptive. Here, we report a case in drills (Mandrillus leucophaeus), a largely unstudied monkey species. We collected data from the birth to the death of the infant on maternal and alloparental care towards the newborn across three phases: pre-mortem, post-mortem, and post-mortem cannibalism. The mother maintained high levels of grooming after the infant's death. Both the mother and other group members interacted with the dead baby by trying to engage its gaze. Two days after the death, the mother started to eat the corpse until it was almost completely consumed; there was no sharing with other group members. Although we cannot draw firm conclusions about potential benefits of the mother's behavior, this observation on drills adds a piece to the puzzle of thanatological behaviors and cannibalism in primates.

Don't stop me now, I'm having such a good time! Czechoslovakian wolfdogs renovate the motivation to play with a bow.

Dogs engage in play behavior at every age and the play bow is their most iconic playful posture. However, the function of this posture is still under debate. Here, we selected the Czechoslovakian Wolfdog (CWD) as a model breed to clarify the function of the play bow. We analyzed frame-by-frame 118 sessions of 24 subjects and recorded 76 play bow events. We found that all the play bows were performed in the visual field of the playmate suggesting that the sender takes into account the attentional state of the receiver when releasing the signal. By drawing survival curves and using log-rank test we found that play bow was mainly performed during a short pause in an ongoing session and that its performance triggered the playmate's reaction again. These findings show that play bow functions in restoring the partner motivation to play. Finally, by using a sequential analysis and a generalized mixed model, we found no evidence supporting the metacommunicative function of the play bow. The signal did not necessarily precede a contact offensive behavior (e.g., play biting and play pushing) and it was not affected by the level of asymmetry of the play session. In conclusion, in CWDs play bow can be considered a visual signal useful to maintain the motivation to play in the receiver. Therefore, we suggest that the mismatched number of play bows emitted by the 2 players in a given session can be predictive of their different motivations to play.