Beware! Different methods lead to divergent results on yawn contagion modulation in bonobos.

Contagious yawning (CY)-linked to physiological synchronization and possibly emotional contagion-occurs when one individual's yawn induces yawning in others. CY was investigated over different time windows (minutes from the triggering stimulus) via naturalistic or experimental studies (using real and video yawns, respectively) with contrasting results, especially in bonobos. We verified whether in bonobos result divergences may derive from different methods. We gathered yawning data on 13 bonobos at Twycross Zoo (UK) via a naturalistic (all-occurrences observations) and experimental approach (by showing yawn/control video stimuli). Based on literature, we used 1- and 3-min windows to detect CY. Due to fission-fusion management, individuals could form permanent or non-permanent associations (more/less familiar subjects under naturalistic setting). Video yawn stimuli may come from group mates/stranger models (more/less familiar subjects under the experimental setting). Stimulus type and time window affected CY modulating factors but not CY detection. Familiarity and age effect on CY showed opposite trends in 3-min trials and 1-min observations. CY was highest in oldest, non-permanently (rather than permanently) associated subjects in the naturalistic setting, but in the youngest subjects and with ingroup (rather than outgroup) models in trials. The age effect differences on CY might be due to decontextualized yawns and immature subject curiosity toward videos. The reversed familiarity effect suggests CY's context-dependent function in promoting social synchronization with socially distant group mates, as failing to coordinate as a group may lead to social disruption. Complementary methods are needed to fully understand motor replication phenomena.

More Than Just Kibbles: Keeper Familiarity and Food Can Affect Bonobo Behavior.

The welfare of captive animals relies on numerous factors. Keepers can affect animals' welfare and this could especially apply to emotionally and cognitively complex species, such as great apes. We collected video data over three months on 17 bonobos (La Vallée des Singes, France) and extracted five behaviours (play, aggression, anxiety, gestures, sociosexual interactions) -during two-minute slots-under three conditions: keeper-present/food-unavailable; keeper-present/food-available; keeper-absent/food-unavailable. We ran generalized linear models to investigate whether behavioral frequencies were affected by food presence/quality and keeper familiarity. Anxiety-related behaviors increased when the keeper was present and in absence of food, due to food expectation. Sociosexual interactions increased in presence of more familiar keepers and in absence of food, maybe to decrease the tension around food. Gestures increased in presence of more familiar keepers and with low-quality food, which was provided in large 'catchable' pieces. Aggression levels increased with high-quality food with no effect of keeper. Play behavior was not affected by any variable. Hence, bonobos were affected not just by food but also by keeper features. Considering multiple variables in the 'welfare equation' can improve captive management and increase the well-being of bonobos, a species that is much closer to humans than to other non-human animals.

Female bonobos show social swelling by synchronizing their maximum swelling and increasing bonding.

Different Old World primates show conspicuous anogenital swelling, with the Maximum Swelling Phase (MSP) signaling the ovulatory phase. MSP synchronization between females has been linked to social dynamics. In bonobos, characterized by female dominance, MSP is not a fully reliable signal of fertility because it may cover anovulatory periods. We investigated whether bonobo females synchronized their MSP and whether this phenomenon was modulated by social factors. Data were collected at La Vallée des Singes (France). In the period 2009-2022, swelling cycles data were collected daily on bonobo females (N = 9). In the period 2018-2022, ethological data (aggression/affiliation/socio-sexual behaviors) were also collected. We found that: (i) females synchronized their MSP and most likely experienced MSP onset following the MSP onset in other females; (ii) synchronization increased as the years spent together by females increased; (iii) synchronization preferentially occurred between females that affiliated less; (iv) synchronization on the MSP was linked to increased female-female socio-sexual contacts, which probably favored MSP synchronization maintenance. Hence, in bonobos MSP can be modulated by social factors and its synchronization, possibly underlying autonomic contagion, might have been positively selected during evolution in relation to the benefits females obtain in terms of intra-group cohesion.

Adult-adult play in captive lowland gorillas (Gorilla gorilla gorilla).

Among African great apes, play is virtually absent between adult lowland gorillas (Gorilla gorilla gorilla). Here, we report an extremely rare case of adult-adult play observed in the lowland gorilla group housed at La Vallée de Singes (France). We recorded three playful interactions between the silverback and an adult lactating female. Given the diverse causal and functional nature of play, different factors may join in promoting this behaviour. In our group, contrary to what has been shown by previous studies in wild and captive gorillas, adult females spent more time in spatial proximity with the silverback than with other females. Hence, the probability of social interaction (including play) between silverback and adult females was enhanced. Moreover, the motivation of the lactating female to play might be an effect of oxytocin, a hormone that reaches high concentration levels during lactation and that promotes social affiliation. The fact that play invitations were always performed by the female might support this hypothesis. Certainly, we cannot exclude the possibility that the play event is a group idiosyncrasy or an artefact of captivity, even though the subjects never showed abnormal behaviour. Structurally, play sessions showed a suitable degree of pattern variability and switching frequency from one pattern to another. The proportion of offensive patterns was higher in the female during play and in the male during aggression, which conforms to the role reversal play phenomenon. In conclusion, this report confirms that the absence of evidence is not the evidence of absence. It is likely that under particular physiological or socio-ecological conditions, adult-adult play may be manifested as an "unconventional" part of gorilla social behaviour.

Yawn contagion in bonobos: Another group, another story.

In primates, yawn contagion (the yawning response elicited by others' yawn) is variably influenced by individual (e.g., sex, age) and social factors (e.g., familiarity) and possibly linked to interindividual synchronization, coordination, and emotional contagion. Two out of three studies on yawn contagion in bonobos (Pan paniscus), found the presence of the phenomenon with mixed results concerning the effect of familiarity and no replication on its modulating factors. To address this puzzling issue, we recorded all occurrences data on yawn contagion in a captive bonobo group (March-June 2021; 18 individuals; La Vallée des Singes, France). Contrary to chimpanzees and humans, the number of triggering yawns increased contagion, possibly owing to a higher stimulus threshold. This aspect may explain the interindividual variability observed in yawn contagion rates. In subjects under weaning, we did not detect yawn contagion and, as it occurs in certain human cohorts, yawn contagion declined with age, possibly due to reduced sensitivity to others. Females responded more than males and elicited more responses from females when showing sexual swelling. As reproductive females are central in bonobo society, our results support the hypothesis that-as in other Hominini-the most influential sex can influence yawn contagion. The relationship quality (measured via grooming/play) did not affect yawn contagion, possibly due to bonobos' xenophilic nature. Overall, this study confirms the presence of yawn contagion in bonobos and introduces new elements on its modulating factors, pointing toward the necessity of cross-group studies.

Sex and grooming as exchange commodities in female bonobos' daily biological market.

The Biological Market Theory (BMT) posits that cooperation between non-human animals can be seen as a mutually beneficial exchange of commodities similarly to what observed in human economic markets. Positive social interactions are commodities in non-human animals, and mutual exchanges fulfilling the criteria of the BMT have been shown in several species. However, the study of biological markets suffers from methodological limitations that are mainly linked to the difficulty of clearly identifying the currencies and their exchanges in the short-term. Here, we test whether bonobo females are more attractive during their maximum swelling phase, whether they exchange grooming and Genito-Genital Rubbing (GGR) on a daily level of analysis, and whether these daily exchanges fulfil the BMT criteria. Females engaged more in GGR when their sexual swelling was in the maximum phase. Moreover, they exchanged grooming and sex according to the daily "market fluctuations" associated with swelling status. Females in the minimum phase (low-value) increased their probability to engage in GGR with females in the maximum phase (high-value) by grooming them preferentially. In line with the supply/demand law, the female grooming strategy varied depending on the daily number of swollen females present: the higher the number of swollen females, the lower the individual grooming preference. As a whole, our study confirms BMT as a valid model to explain daily commodity exchanges as a function of the temporary value of traders, and underlines the importance of a day-by-day approach to unveil the presence of a biological market when the value of traders frequently changes.

Foraging postures are a potential communicative signal in female bonobos.

Body postures are essential in animal behavioural repertoires and their communicative role has been assessed in a wide array of taxa and contexts. Some body postures function as amplifiers, a class of signals that increase the detection likelihood of other signals. While foraging on the ground, bonobos (Pan paniscus) can adopt different crouching postures exposing more or less of their genital area. To our knowledge, their potential functional role in the sociosexual life of bonobos has not been assessed yet. Here we show, by analysing more than 2,400 foraging events in 21 captive bonobos, that mature females adopt a rear-exposing posture (forelimb-crouch) and do so significantly more often when their anogenital region is swollen than during the non-swollen phase. In contrast, mature males almost completely avoid this posture. Moreover, this strong difference results from a diverging ontogeny between males and females since immature males and females adopt the forelimb-crouch at similar frequencies. Our findings suggest that the forelimb-crouch posture may play a communicative role of amplification by enhancing the visibility of female sexual swellings, a conspicuous signal that is very attractive for both males and females. Given the high social relevance of this sexual signal, our study emphasizes that postural signalling in primates probably deserves more attention, even outside of reproductive contexts.

High-Ranking Geladas Protect and Comfort Others After Conflicts.

Post-conflict affiliation is a mechanism favored by natural selection to manage conflicts in animal groups thus avoiding group disruption. Triadic affiliation towards the victim can reduce the likelihood of redirection (benefits to third-parties) and protect and provide comfort to the victim by reducing its post-conflict anxiety (benefits to victims). Here, we test specific hypotheses on the potential functions of triadic affiliation in Theropithecus gelada, a primate species living in complex multi-level societies. Our results show that higher-ranking geladas provided more spontaneous triadic affiliation than lower-ranking subjects and that these contacts significantly reduced the likelihood of further aggression on the victim. Spontaneous triadic affiliation significantly reduced the victim's anxiety (measured by scratching), although it was not biased towards kin or friends. In conclusion, triadic affiliation in geladas seems to be a strategy available to high-ranking subjects to reduce the social tension generated by a conflict. Although this interpretation is the most parsimonious one, it cannot be totally excluded that third parties could also be affected by the negative emotional state of the victim thus increasing a third party's motivation to provide comfort. Therefore, the debate on the linkage between third-party affiliation and emotional contagion in monkeys remains to be resolved.

Are horses capable of mirror self-recognition? A pilot study.

Mirror Self-Recognition (MSR) unveils complex cognitive, social and emotional skills and it has been found only in humans and few other species, such as great apes, dolphins, elephants and magpies. In this pilot study, we tested if horses show the capacity of MSR. Four subjects living socially under naturalistic conditions were selected for the experiment. We adopted the classical mark test, which consists in placing a coloured mark on an out-of-view body part, visible only through mirror inspection. If the animal considers the image as its own, it will use its reflection to detect the mark and will try to explore it. We enhanced the classical paradigm by introducing a double-check control. Only in the presence of the reflecting surface, animals performed tactile and olfactory exploration of the mirror and looked behind it. These behaviors suggest that subjects were trying to associate multiple sensory cues (visual, tactile and olfactory) to the image in the mirror. The lack of correspondence between the collected stimuli in front of the mirror and the response to the colored mark lead us to affirm that horses are able to perceive that the reflected image is incongruent when compared with the memorized information of a real horse. However, without replication of data, the self-directed behavior towards the colored marks showed by our horses cannot be sufficient per se to affirm that horses are capable of self-recognition.

She more than he: gender bias supports the empathic nature of yawn contagion in Homo sapiens.

Psychological, clinical and neurobiological findings endorse that empathic abilities are more developed in women than in men. Because there is growing evidence that yawn contagion is an empathy-based phenomenon, we expect that the female bias in the empathic abilities reflects on a gender skew in the responsiveness to others' yawns. We verified this assumption by applying a linear model on a dataset gathered during a 5 year period of naturalistic observations on humans. Gender, age and social bond were included in the analysis as fixed factors. The social bond and the receiver's gender remained in the best model. The rates of contagion were significantly lower between acquaintances than between friends and family members, and significantly higher in women than in men. These results not only confirm that yawn contagion is sensitive to social closeness, but also that the phenomenon is affected by the same gender bias affecting empathy. The sex skew, also found in other non-human species, fits with the female social roles which are likely to require higher empathic abilities (e.g. parental care, group cohesion maintenance, social mediation). The fact that female influence in social dynamics also relies on face-to-face emotional exchange raises concerns on the negative repercussions of having women's facial expressions forcibly concealed.

Ultrasonographic Investigation of Human Fetus Responses to Maternal Communicative and Non-communicative Stimuli.

During pregnancy fetuses are responsive to the external environment, specifically to maternal stimulation. During this period, brain circuits develop to prepare neonates to respond appropriately. The detailed behavioral analysis of fetus' mouth movements in response to mothers' speech may reveal important aspects of their sensorimotor and affective skills; however, to date, no studies have investigated this response. Given that newborns at birth are capable of responding with matched behaviors to the social signals emitted by the caregiver, we hypothesize that such precocious responses could emerge in the prenatal period by exploiting infants' sensitivity to their mother's voice. By means of a two-dimensional (2D) ultrasonography, we assessed whether fetuses at 25 weeks of gestation, showed a congruent mouthmotor response to maternal acoustic stimulation. Mothers were asked to provide different stimuli, each characterized by a different acoustic output (e.g., chewing, yawning, nursery rhymes, etc.) and we recorded the behavioral responses of 29 fetuses. We found that, when mothers sang the syllable LA in a nursery rhyme, fetuses significantly increased mouth openings. Other stimuli provided by the mother did not produce other significant changes in fetus' behavior. This finding suggests that fetuses are sensitive only to specific maternal vocalizations (LA) and that fetal matched responses are rudimentary signs of early mirroring behaviors that become functional in the postnatal period. In conclusion, fetuses seem to be predisposed to respond selectively to specific maternal stimuli. We propose that such responses may play a role in the development of behavioral and emotional attunement with their mothers long before birth.

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.

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.

Yawn contagion in humans and bonobos: emotional affinity matters more than species.

In humans and apes, yawn contagion echoes emotional contagion, the basal layer of empathy. Hence, yawn contagion is a unique tool to compare empathy across species. If humans are the most empathic animal species, they should show the highest empathic response also at the level of emotional contagion. We gathered data on yawn contagion in humans (Homo sapiens) and bonobos (Pan paniscus) by applying the same observational paradigm and identical operational definitions. We selected a naturalistic approach because experimental management practices can produce different psychological and behavioural biases in the two species, and differential attention to artificial stimuli. Within species, yawn contagion was highest between strongly bonded subjects. Between species, sensitivity to others' yawns was higher in humans than in bonobos when involving kin and friends but was similar when considering weakly-bonded subjects. Thus, emotional contagion is not always highest in humans. The cognitive components concur in empowering emotional affinity between individuals. Yet, when they are not in play, humans climb down from the empathic podium to return to the "understory", which our species shares with apes.

In bonobos yawn contagion is higher among kin and friends.

In humans, the distribution of yawn contagion is shaped by social closeness with strongly bonded pairs showing higher levels of contagion than weakly bonded pairs. This ethological finding led the authors to hypothesize that the phenomenon of yawn contagion may be the result of certain empathic abilities, although in their most basal form. Here, for the first time, we show the capacity of bonobos (Pan paniscus) to respond to yawns of conspecifics. Bonobos spontaneously yawned more frequently during resting/relaxing compared to social tension periods. The results show that yawn contagion was context independent suggesting that the probability of yawning after observing others' yawns is not affected by the propensity to engage in spontaneous yawns. As it occurs in humans, in bonobos the yawing response mostly occurred within the first minute after the perception of the stimulus. Finally, via a Linear Mixed Model we tested the effect of different variables (e.g., sex, rank, relationship quality) on yawn contagion, which increased when subjects were strongly bonded and when the triggering subject was a female. The importance of social bonding in shaping yawn contagion in bonobos, as it occurs in humans, is consistent with the hypothesis that empathy may play a role in the modulation of this phenomenon in both species. The higher frequency of yawn contagion in presence of a female as a triggering subject supports the hypothesis that adult females not only represent the relational and decisional nucleus of the bonobo society, but also that they play a key role in affecting the emotional states of others.