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.

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.

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.

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.

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.

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.

Social Isolation Affects the Mimicry Response in the Use of Smartphones : An Ethological Experiment during the COVID-19 Pandemic.

Humans are social animals that rely on different ways to interact with each other. The COVID-19 pandemic strongly changed our communication strategies. Because of the importance of direct contact for our species, we predict that immediately after the forced social isolation, people were more prone to engage in direct rather than in virtual interactions, thus showing a lower mimicry response in the use of smartphones. In a non-longitudinal study, we collected behavioral data under naturalistic contexts and directly compared the data of the mimicry response gathered immediately following the Italian lockdown (May-September 2020) with those gathered one year later (May-October 2021). Contrary to our expectations, the mimicry response in the use of smartphones was higher immediately after the lockdown than a year later. Probably the large use of these devices during the lockdown translated into a greater sensitivity to be affected by others' smartphone manipulation. Indeed, social isolation modified, at least in the short term, the ways we interact with others by making us more prone to engage in "virtual" social interactions. The bright side of the coin unveiled by our findings is that the effect seems to diminish over time. The large behavioral dataset analyzed here (1,608 events; 248 people) also revealed that the mimicry response in the use of smartphones was higher between familiar subjects than between strangers. In this view, mimicry in manipulating smartphones can be considered an example of joint action that fosters behavioral synchrony between individuals that, in the long-term, can translate into the formation of social bonding.

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females.

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas (Theropithecus gelada). Because females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls, thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.

Playing together, laughing together: rapid facial mimicry and social sensitivity in lowland gorillas.

In nonhuman animals, the phenomenon of rapid facial mimicry (RFM)-the automatic, involuntary, and rapid (<1 s) replication of others' facial expressions-has been mainly investigated in the playful domain. In immature lowland gorillas Gorilla gorilla gorilla both play face (PF) and full PF (FPF) are rapidly mimicked between the players. This makes the species suitable to test hypotheses on the factors influencing RFM during play. The observations on 3 captive groups of lowland gorillas (N = 27) revealed that contrary to expectations, the closeness of social bond negatively influenced the occurrence of RFM but it did not affect either RFM latency or its overlapping index (OVERLAP). RFM was affected by the degree of symmetry of play fighting: the more balanced the session, the higher the occurrence of RFM. Players of the same sex class responded faster than players of different sex. These findings suggest that RFM may help synchronizing behaviors of playmates matching in size (same-sex) and promote symmetric playful interactions. "Laughing together" (measured by the RFM OVERLAP) lasted longer when the responder perfectly mirrored the partner expression (PF→PF; FPF→FPF). If PF and FPF convey information on the different play roughness degree, through "laughing together" the players could coordinate their actions and share positive moods and playful intensity. If the perfect congruency in the motor resonance, also known as social sensitivity, can foster a possible emotional dialogue between gorillas remains to be investigated.

Laughter, play faces and mimicry in animals: evolution and social functions.

Human laughter and laugh faces show similarities in morphology and function with animal playful expressions. To better understand primordial uses and effects of human laughter and laugh faces, it is important to examine these positive expressions in animals from both homologous and analogous systems. Phylogenetic research on hominids provided empirical evidence on shared ancestry across these emotional expressions, including human laughter and laugh faces. In addition, playful expressions of animals, in general, arguably have a key role in the development of social cognitive skills, a role that may help explain their polyphyletic history. The present work examines the evolution and function of playful expressions in primates and other animals. As part of this effort, we also coded for muscle activations of six carnivore taxa with regard to their open-mouth faces of play; our findings provide evidence that these carnivore expressions are homologues of primate open-mouth faces of play. Furthermore, our work discusses how the expressions of animal play may communicate positive emotions to conspecifics and how the motor resonance of these expressions increases affiliation and bonding between the subjects, resembling in a number of ways the important social-emotional effects that laughter and laugh faces have in humans. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

The naturalistic approach to laughter in humans and other animals: towards a unified theory.

This opinion piece aims to tackle the biological, psychological, neural and cultural underpinnings of laughter from a naturalistic and evolutionary perspective. A naturalistic account of laughter requires the revaluation of two dogmas of a longstanding philosophical tradition, that is, the quintessential link between laughter and humour, and the uniquely human nature of this behaviour. In the spirit of Provine's and Panksepp's seminal studies, who firstly argued against the anti-naturalistic dogmas, here we review compelling evidence that (i) laughter is first and foremost a social behaviour aimed at regulating social relationships, easing social tensions and establishing social bonds, and that (ii) homologue and homoplasic behaviours of laughter exist in primates and rodents, who also share with humans the same underpinning neural circuitry. We make a case for the hypothesis that the contagiousness of laughter and its pervasive social infectiousness in everyday social interactions is mediated by a specific mirror mechanism. Finally, we argue that a naturalistic account of laughter should not be intended as an outright rejection of classic theories; rather, in the last part of the piece we argue that our perspective is potentially able to integrate previous viewpoints-including classic philosophical theories-ultimately providing a unified evolutionary explanation of laughter. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

Visual communication in social play of a hierarchical carnivore species: the case of wild spotted hyenas.

Communication relies on signals that can be produced via different sensory modalities to modify receivers' behavior. During social interactions, the possibility to perceive subtle visual cues enhances the use of facial expressions to exchange information. One of the most appropriate fields to explore the specific design features of visual signals is play fighting. Here, we explored the production and potential role of Relaxed Open Mouth (ROM) and Head Bobbing (HB) in regulating play fighting of wild spotted hyenas Crocuta crocuta, a highly hierarchical carnivore species. In accordance with the assumptions of the signal optimization theory, wild hyenas produced ROM and HB almost exclusively when the sender was in direct visual contact with the receiver thus suggesting that senders were attentive to the playmates' face. Contrary to HB, the sequential analysis revealed that ROM often anticipated offensive patterns such as play biting thus supporting the hypothesis that ROM, but not HB, is a metacomunicative signal. Moreover, when the offensive patterns were biased toward one of the 2 players, the session was punctuated by a higher number of ROMs. Our findings support the general hypothesis that these 2 visual signals can play different roles in the management of play fighting in this carnivore species. The complementary use of ROM and HB would suggest that spotted hyenas are highly competent and fast in processing facial displays of different nature to correctly "read others' intentions" and respond with appropriate motor actions to avoid misunderstanding during one of the most multifaceted and risky social interaction.

Familiarity modulates both intra- and interspecific yawn contagion in red-capped mangabeys.

Yawn contagion (YC) is, compared to spontaneous yawning, an evolutionary recent phenomenon probably linked to behavioral synchronization in highly social species that is more likely when it involves familiar subjects. Here, we investigate for the first time in monkeys which factors modulate intra- and interspecific YC. Through an experimental approach, we exposed 17 red-capped mangabeys to video stimuli (Yawn vs Control) depicting familiar/unfamiliar red-capped mangabeys and humans, and unfamiliar hamadryas. We found that mangabeys yawned more often in response to Yawn than Control videos independently from the species depicted, demonstrating both intra- and interspecific YC in the tested species. Moreover, both mangabey and human familiar yawning stimuli evoked a stronger yawning response in the subjects compared to the unfamiliar counterparts. Neither the amount of time spent looking frontally at the screen (probability of stimulus perception) nor the levels of self-directed behaviors (a proxy of anxiety) accounted for the results. In conclusion, we provide the first evidence that in non-human primate familiarity modulates both intra- and inter-specific YC. Stimuli emitted by familiar faces somehow ease the mechanisms underlying YC, and this modulation can also apply to heterospecific subjects when previous shared experiences provide the prerequisites for the development of social bonds.

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.

Bridging Captive and Wild Studies: Behavioral Plasticity and Social Complexity in Theropithecus gelada.

Cognitive ethology explores the ability of animals to flexibly adapt their behavior to rapid physical and social environment fluctuations. Although there is a historical dichotomy between field and captive studies, recently, a growing interest in questions that sit at the intersection of cognitive and adaptive perspectives has helped bridge this divide. By focusing on Theropithecus gelada, we discuss the three main reasons why this hybrid approach is extremely successful. First, captive and wild studies provide data at different social, spatial, and temporal scales that can be synthesized to give a fuller picture of the behavior. Secondly, apparently conflicting results from captive and wild settings are powerful tools to explore behavioral flexibility and latent behavioral tendencies. Third, the different settings provide ways of validating and exploring behaviors that are noticed in the other setting. Although we were able to bring together our captive and wild research to demonstrate these ideas, we could have obtained a more integrated vision on the proximate and ultimate gelada behavioral and cognitive strategies if we had considered this hybrid approach from the beginning. We hope that this manuscript stimulates scholars in designing their studies by taking into account the incredible potential of a complementary captive-wild research approach.