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.

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.

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.

Enriching Zoo-Housed Ring-Tailed Lemurs (Lemur catta): Assessing the Influence of Three Types of Environmental Enrichment on Behavior.

Environmental enrichment is a management tool used to promote positive animal welfare by stimulating species-specific behaviors and providing animals with opportunities to exert choice and control over the environment. Our study aimed to evaluate the combined effect of three enrichment types and environmental/individual factors (i.e., individual age and rank position) on the behavior of six adult Lemur catta hosted at Pistoia Zoo (Italy). We collected data from June to September 2013 using a within-subject experimental design consisting of five conditions: Baseline, Food-based enrichment, Physical enrichment, Auditory enrichment and No enrichment provided. We conducted six 30-minute observation sessions per sampling day (total = 107 h). We recorded the animals' behavior via 2-minute focal animal sampling per individual per observation period and analyzed data with Generalized Linear Models. The study group only performed normal species-specific behaviors. Enrichments decreased stress-related behavioral patterns, whreas environmental and individual factors influenced the other recorded behaviors. Our study confirmed the usefulness of employing an integrated methodological approach to enrichment assessment for enhancing captive lemur care.

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.

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.

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.

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.

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.

Let's unite in play! Play modality and group membership in wild geladas.

Two of the main hypotheses put forth to explain the function of immature social play are the Social Skill Hypothesis and the Motor Training Hypothesis focussing on whether play can improve social competence to develop cooperative social networks or physical abilities to outcompete others, respectively. Here, we tested these hypotheses on a monkey species, the wild gelada (Theropithecus gelada) from the Kundi plateau, Ethiopia. This species is organized in bands divided in One-Male Units (OMUs), united only via social play. Immatures form 'play units' in which individuals from the same and different OMUs interact. We analysed the potential differences between inter- and intra-OMU play to verify which of the two hypotheses (Social Skill or Motor Training Hypothesis) best explains the function of play in geladas. We analysed 527 video-recorded social play sessions and found mixed support for both hypotheses. In agreement with the Social Skill Hypothesis, we found that play in geladas shows scarce social canalization being similarly distributed across age, sex and group membership. In line with the Motor Training Hypothesis, we detected higher levels of competition (shorter and more unbalanced sessions) in inter-OMU compared to intra-OMU play. Hence, in geladas play can be a tool for both the development of social relationships and the improvement of the physical skills necessary to cope with either future mates or competitors. In conclusion, neither hypothesis can be discarded and both hypotheses concur in explaining why immature geladas peculiarly form 'play units' embracing both ingroup and outgroup members.