Play contagion in African elephants: The closest, the better.

Behavioural contagion is an automatic process through which a behaviour performed by an individual (trigger) is reproduced by an observer (responder) without necessarily replicating the exact motor sequence. It has been linked to inter-individual synchronisation and possibly emotional contagion. Play can convey emotions and enhance social bonding, although its contagiousness is understudied. To verify social play contagion presence and modulating factors, we gathered audio-video data on social play, distance and affiliation on a group of savannah African elephants (15 individuals) at Parque de la Naturaleza de Cabarceno (Cantabria, Spain). Social play was contagious as it was more likely started by uninvolved elephants (within 3-min) in Post-Play Condition (PP) - after that other elephants had started playing - than in Matched-control Condition (MC; no previous play). Social play contagion mostly occurred within 30 m - probably due to elephants' limited visual acuity - and it was highest between individuals that affiliated the most, with the distance-affiliation interaction having no effect. The most prominent individuals in the social play network were also the most influential in the play contagion network (Eigenvector-centrality measure). Play contagion was socially modulated, thus suggesting it may extend from motor replication to the replication of the underlying affective state.

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.

Witness for resolution: post-conflict quadratic affiliation in semi-free ranging pigs.

In social mammals, post-conflict resolution can involve the reunion of former opponents (reconciliation), spontaneous/solicited post-conflict affiliation of a third party with either opponent (triadic contacts), and affiliation between other individuals (hereafter bystanders; quadratic contacts). Quadratic contacts-possibly informing complex cognitive abilities-have been neglected in post-conflict studies. We investigated quadratic affiliation in semi-free ranging pigs Sus scrofa, at the ethical farm Parva-Domus (Cavagnolo, Italy). Kinship was known. We collected behavioral data on adult pigs (n = 104) via video recordings (43 h) followed by video analyses. Affiliative and anxiety behaviors between bystanders were collected under post-conflict (PC; following a conflict between non-bystanders) and matched-control (MC; no conflict) conditions. Quadratic affiliation was present in pigs, as bystanders affiliated more in PC than MC, and such affiliation was followed by a decrease in the anxiety behaviors of both the interacting bystanders. Thus, quadratic contacts may be partly aimed at reducing one's own anxiety (intrinsic regulation). Quadratic affiliation was highest between closely related bystanders, which suggests that such affiliation may be most effective when close kin is involved. Quadratic affiliation was lowest after reconciliation and spontaneous triadic contacts. This suggests that direct peacemaking between opponents and spontaneous triadic contacts with close kin may most likely replace quadratic affiliation. Hence, pigs can be influenced by the negative events that affect other pigs-but not themselves-and their response may be modulated by social factors. Such non-random quadratic affiliation may point toward the presence of elements of social appraisal abilities in pigs.

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.

Rapid facial mimicry in Platyrrhini: Play face replication in spider monkeys (Ateles fusciceps, Ateles hybridus, and Ateles paniscus).

Rapid facial mimicry (RFM), the rapid and automatic replication of facial expression perceived, is considered a basic form of empathy and was investigated mainly during play. RFM occurs in Catarrhini (Old World primates), but it is not still demonstrated in Platyrrhini (New World primates). For this reason, we collected video data on playful interactions (Nplay_interactions = 149) in three species of spider monkeys (Ateles fusciceps-N = 11, Ateles hybridus-N = 14, and Ateles paniscus-N = 6) housed at La Vallée des Singes and the ZooParc de Beauval (France). For the first time, we demonstrated the occurrence of RFM in Platyrrhini (analyzing 175 events). Players' sex, age, species, relationship quality, and kinship did not modulate RFM probably due to the species' complex fission-fusion dynamics and flexible interindividual social relationships. Compared to the absence of any playful expressions or the presence of only not replicated play face, RFM prolonged the session duration and was sequentially associated with more types of more intense offensive playful patterns (patterns aimed at attacking/pursuing the playmate). We proposed that RFM may favor synchronization and context sharing between players, thus decreasing the risk of behavior misinterpretation while simultaneously fostering a more competitive nature of play. In conclusion, this study stimulates additional research on the evolutionary origins of motor mimicry in primates, possibly dating back to before the divergence of New and Old World monkeys. Furthermore, it also points toward the possibility that RFM may not always lead to cooperation but also to competition, depending on the context and species' social and cognitive features.

Is it for real? Structural differences between play and real fighting in adult chimpanzees (Pan troglodytes).

In primates, as well as in other mammals, play fighting (PF) is a complex form of playful activity that is structurally similar to real fighting (RF) and may also be used in a competitive way. Here, we verify the structural key differences that can distinguish PF from RF in adult chimpanzees (Pan troglodytes). We collected 962 h of video recording on 30 adult individuals belonging to four chimpanzee groups (Mona Chimpanzee Sanctuary, Spain; La Vallée des Singes and ZooParc de Beauval, France). We applied different indices-two of which were borrowed from the ecological measures of biodiversity-to test for structural differences between PF (345 sessions) and RF (461 sessions) in the levels of behavior repetition (Repeatability of Same Behavior Index, RSBI), distribution uniformity (Pielou Index, J), variability (Shannon Index, H') and, symmetry (i.e., reciprocal exchange of offensive/defensive behaviors; Asymmetry Index, AI). Moreover, we compared the session duration between PF and RF. We found that duration and RSBI were higher in PF than RF while AI was higher in RF than PF. No difference was found between J and H'. Interestingly, both females and males maintained similar ranking positions (determined via Normalized David's scores) in RF and PF. Our study indicates that session duration, behavior repetition, and symmetry can be distinctive structural key features of PF whereas dominance role-reversal, behavior variability, and distribution uniformity were not. PF in adult chimpanzees may have elements of serious contexts (e.g., absence of role-reversal as in RF) which is in line with the view that play is a blended, multifunctional behavior deriving from the re-combination of different behavioral systems. Our findings highlight the need to investigate play structure and manifestation in a nuanced way to better understand the actual motivation that underlies what appears to be play.

Sows' Responses to Piglets in Distress: An Experimental Investigation in a Natural Setting.

Domestic pigs (Sus scrofa) possess complex socio-cognitive skills, and sows show high inter-individual variability in maternal behaviour. To evaluate how females-reared under natural conditions-react to the isolation calls of their own piglets or those of other females, we conducted observations and experimental trials. In January-February 2021, we conducted all-occurrences sampling on affiliation, aggression, and lactation (daily, 7:30-16:30 h) on six lactating and four non-lactating females at the ethical farm Parva Domus (Turin, Italy). The trials (30 s each, n = 37/sow) consisted of briefly catching and restraining a piglet. We recorded the sow response (none/reactive/proactive movement towards the piglet; self-directed anxiety behaviours such as body shaking) before and during the trial and under control conditions. Increased levels of anxiety behaviour in sows were accompanied by an increased frequency of responses. Less aggressive sows and lactating sows showed the highest frequencies of response. Finally, the isolation calls' maximum intensity had an influence on the type of response observed, with higher proactive response frequencies following lower intensity isolation calls. Our results suggest that being under lactation could play a key role in increasing sow response levels and that specific acoustic features may influence the response.

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.

Domestic pigs (Sus scrofa) engage in non-random post-conflict affiliation with third parties: cognitive and functional implications.

In social mammals, conflict resolution involves the reunion of former opponents (aggressor and victim) after an aggressive event (reconciliation) or post-conflict triadic contacts with a third party, started by either opponent (solicited-TSC) or spontaneously offered by the third party (unsolicited-TUC). These post-conflict strategies can serve different functions, including consolation (specifically when TUCs reduce the victim's anxiety). We investigated the possible presence and modulating factors of such strategies on semi-free ranging pigs (Sus scrofa; N = 104), housed at the ethical farm Parva Domus (Cavagnolo, Italy). Kinship was known. Reconciliation was present and mainly occurred between weakly related pigs to possibly improve tolerant cohabitation. Triadic contacts (all present except aggressor TSCs) mostly occurred between close kin. TSCs enacted by victims reduced neither their post-conflict anxiety behaviors nor further attacks by the previous aggressor, possibly because TSCs remained largely unreciprocated. TUCs towards aggressors did not reduce aggressor post-conflict anxiety but limited aggression redirection towards third parties. TUCs towards the victim reduced the victim but not the third-party's anxiety. However, TUCs may also provide inclusive fitness benefits to third parties by benefiting close kin. In sum, pigs engaged in non-random solicited/unsolicited triadic contacts, which suggests that pigs might possess socio-emotional regulation abilities to change their own or others' experience and elements of social appraisal, necessary to detect the emotional arousal of relevant others and (in case of TUCs) take the agency to restore homeostasis.

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.

Play fighting versus real fighting in piglets (Sus scrofa): Similar patterns, different structure.

When animals engage in 'non-serious' fighting (play-fighting) they 'borrow' motor patterns especially from the aggressive context. It may be difficult to distinguish play- and real-fighting. This is particularly true for piglets (Sus scrofa), which can use play-fighting as a substitute for aggression. To check for the structural differences between play- and real-fighting in piglets, we: i) video recorded 496 interactions from three litters (at Parva-Domus extensive ethical farm; Turin, Italy); ii) extracted (by video analyses) duration, patterns, and data on involved individuals; iii) calculated session structural/ecological indices; and iv) compared the indices (play- vs real-fighting). Compared to real-fighting - play-fighting was longer (informing its rewarding nature), more symmetrical (lower asymmetry index) and variable (higher Shannon index). Moreover, play-fighting showed less pattern repetition (lower Repetition Index) and was not more polyadic and evenly distributed (comparable polyadic and Pielou indices). By being longer, and more variable and symmetrical than real-fighting, play-fighting could serve some of its functions such as motor training, social assessment and training for the unexpected. However, play-fighting in piglets did not comply with all the expected play features, possibly because play is a fluid behavioural system that under certain circumstances may escalate into or replace aggression.

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.

Does the Domestication Syndrome Apply to the Domestic Pig? Not Completely.

The 'domestication syndrome' defines a suite of features that domesticated animals possess as the result of the artificial selection operated by Homo sapiens since the Neolithic. An interesting anthropological question is whether such features, including increased tameness and reduced aggression, apply to all domesticated forms. We investigated this issue in the domestic pig (Sus scrofa). We video-recorded and analysed aggression and social play (mostly play-fighting) sessions from piglets (three litters; n = 24) and wild boar hybrids (domestic pig mother x wild boar father; three litters; n = 27) from 6-50 days of age, raised in the same woodland/grassland habitat and extensive farming management (ethical farm 'Parva Domus', Cavagnolo, Torino). Play and aggression session structure was assessed via Asymmetry (AI; offensive/defensive pattern balance), Shannon (H'; pattern variability), and Pielou (J; pattern evenness) indices. We found that piglets played more (especially after the 20th day of life) and engaged in less variable and uniform sessions than wild boar hybrids. Compared to hybrids, piglets showed less variable but more frequent (especially when approaching weaning) and asymmetrical aggressive events. Thus, the domestication syndrome does not seem to fully apply to either social play or aggression, possibly because artificial selection has produced greater tameness of pigs towards humans than towards conspecifics.

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.

First evidence of yawn contagion in a wild monkey species.

Yawn contagion occurs when individuals yawn in response to the yawn of others (triggers). This is the first account of yawn contagion in wild geladas (Theropithecus gelada), a monkey species that shows yawn contagion in captivity and is organized in core units (one-male/bachelor groups) forming multilevel associations. In a population of geladas from the Kundi plateau (Ethiopia) we found that the yawning response was highest when geladas could perceive a triggering yawn, which confirms that yawn contagion is present in the wild. Yawn duration, mouth-opening degree and presence/absence of vocalisation (possibly modulating yawn detectability) did not affect the likelihood of contagion. Males and females, known to be both implicated in movement initiation within groups, were similarly powerful as yawn triggers. Instead, group membership and responder sex had a significant role in shaping the phenomenon. Yawn contagion was highest between individuals belonging to different core units and males were most likely to respond to others' yawns. Because males have a non-negligible role in inter-group coordination, our results suggest that yawn contagion may have a communicative function that goes beyond the basic unit level.

Infant handling increases grooming towards mothers in wild geladas (Theropithecus gelada).

Infant handling - involving affiliative behavior from non-mothers to infants - is a phenomenon that is variably present in Old World monkeys and can be granted by mothers to obtain social services, such as grooming. Here we investigated for the first time whether infant handling could influence grooming exchange in wild geladas. We gathered data on the population of Kundi highland (Ethiopia) in 2019/2020. Via sampling on 15 focal mothers from eight different One-Male Units, we video-recorded 55 grooming sessions between focal mothers and non-focal females (mothers or non-mothers). We also recorded the possible occurrence of infant handling performed by non-focal females. We found that grooming sessions were longer between mother and non-mothers and in the presence than in the absence of infant handling. Hence, our results show that infant handling can influence the grooming exchange between wild gelada females. Because grooming is used to establish and reinforce social bonds in primates, infant handling may act as a 'social bridge' in a female bonded society. From an evolutionary perspective, infant handling strategies might represent the stepping stone to more complex forms of infant care, such as allomaternal care and cooperative breeding.

Yawning Is More Contagious in Pregnant Than Nulliparous Women : Naturalistic and Experimental Evidence.

Contrary to spontaneous yawning, which is widespread in vertebrates and probably evolutionary ancient, contagious yawning-yawning triggered by others' yawns-is considered an evolutionarily recent phenomenon, found in species characterized by complex sociality. Whether the social asymmetry observed in the occurrence of contagious yawning is related to social and emotional attachment and may therefore reflect emotional contagion is a subject of debate. In this study we assessed whether yawn contagion was enhanced in pregnant women, a cohort of subjects who develop prenatal emotional attachment in preparation for parental care, via hormonal and neurobiological changes. We predicted that if yawn contagion underlies social and emotional attachment, pregnant women would be more likely to contagiously yawn than nonpregnant, nulliparous women of reproductive age. We gathered data in two different settings. In the experimental setting, 49 women were exposed to video stimuli of newborns either yawning or moving their mouth (control) and we video-recorded the women during repeated trials to measure their yawning response. In the naturalistic setting, 131 women were observed in a social environment and their yawning response was recorded. We tested the factors influencing the yawning response, including the reproductive status (pregnant vs. not pregnant). In both settings, yawn contagion occurred significantly more in pregnant than nonpregnant women. By showing that pregnant women were most likely to respond to others' yawns, our results support the hypothesis that the social variation observed in yawn contagion may be influenced by emotional attachment and that yawning in highly social species might have been coopted for emotional contagion during evolution.

Wild geladas (Theropithecus gelada) in crops-more than in pasture areas-reduce aggression and affiliation.

Human-primate interfaces are expanding and, despite recent studies on primates from peri-urban environments, little research exists on the impact of agriculture and/or pasture areas on primate social behavior and health. We assessed how crop/pasture areas potentially alter social behavior and health of wild geladas (Theropithecus gelada) frequenting the unprotected area of Kundi (Ethiopia). We predicted that compared to pasture areas, crop areas (i) would be more challenging for geladas (prediction 1) and (ii) would have a greater impact on both aggressive and affiliative behavior, by reducing grooming time and enhancing competition (prediction 2). During January-May 2019 and December 2019-February 2020, we collected data (via scan, focal animal sampling, and video analyses) on direct human disturbance, external signs of pathologies and social behavior of 140 individuals from 14 one-male units and two all-male units. Animals experienced the highest level of human disturbance in crop areas (in line with prediction 1). Individuals from the groups preferentially frequenting crop areas showed the highest prevalence of external signs of pathologies consistent with chemical and biological contamination (alopecia/abnormally swollen parts). We collected 48 fecal samples. Samples from frequent crop users contained the highest rates of parasitic elements/gram (egg/larva/oocyst/cyst) from Entamoeba histolytica/dispar, a parasite common in human settlements of the Amhara region. In crop areas, subjects spent less time grooming but engaged in lower rates of intense aggression (in partial agreement with prediction 2). We speculate that the reduction in social behavior may be a tactic adopted by geladas to minimize the likelihood of detection and maximize food intake while foraging in crops.