Chimpanzees yawn when observing an android yawn

Participants Participants were 14 adult chimpanzees (Pan troglodytes spp.) aged 10 to 33 years (\(\bar{X}\) = 22.57, SD = 8.06), including 10 males and 4 females (see Table 1). The chimpanzees had lived at the Fundació Mona (Spain) for between 1 and 12 years (\(\bar{X}\) = 7.36, SD = 4.34), after being confiscated or rescued from the pet and entertainment industry to be permanently housed at the centre. All chimpanzees were socially housed in two stable groups within a naturalistic enclosure designed to promote species-typical behaviours. The groups had access to both indoor and outdoor areas and were provided with daily environmental enrichment. No individuals were housed in isolation. Although some chimpanzees initially exhibited abnormal and anxiety-like behaviours, such as stereotypies or overgrooming, previous studies on their rehabilitation process83 have shown that desirable behaviours and welfare indices increased over time, while undesirable behaviours decreased. Table 1 Biographical information on the chimpanzees at time of participation in the study. Full size table Ethical considerations All experimental procedures were non-invasive and complied with the ethical guidelines of the Animal Behaviour Society, which establish the standard and safe Guidelines for the Use of Animals in Research. The study was reviewed and approved by the Ethics Board of Fundació Mona and the Psychology Department Research Ethics Committee of City St. George’s University of London (SREC 14–15 01 CA 16 06 2015). Design and stimuli The study used a within-subjects design, with an independent variable of exposure to an android performing one of three facial expressions: Yawning, Gaping, or a neutral expression (closed mouth) (see Fig. 1a). A human-like android was designed with realistic biological features and motion dynamics. The android measured 45 cm in height, 20 cm in width, and weighed 3.8 kg. Thirty three servo motors were integrated to generate controlled facial movements. When powered on, the android’s neutral expression corresponded to the Close condition (mouth closed, no movement). All programmed facial movements lasted 10 s from onset to offset. To ensure precise and consistent movement, the servos were programmed as follows: (1) Close condition (neutral expression), nine servos maintained the neutral face, ensuring that no unintentional expressive movement occurred; (2) Gape condition (Non-yawning mouth opening). Twelve servos (two on each side above the mouth and two on each side on the lower part of the mouth) controlled the mouth movement, opening it to a maximum of 1.5 cm, sustaining the expression for 6 to 8 s, and then closing the mouth. The remaining active servos acted as support for the rest of the face to remain static. The entire cycle lasted 10 s. Eight mini servos around the eyebrow regions were designed to exemplify the corrugator muscle movement, which forms part of the yawning expression. Finally, the (3) Yawn condition required 6 mini servos to create the internal space necessary for the movement command. These “space facilitator servos”, were placed in the back of the cheek area to maintain the facial structure in the same position and therefore prevent the portrayal of more than one expression at the same time. The android’s mouth opened to a maximum of 5.5 cm, mimicking air intake, while the eyes closed and reopened as the mouth closed. All motion parameters (e.g., time, speed, trajectory, velocity, and muscle simulation motion pattern) were programmed and automatically adjusted using C/C++, Python, Java, and MATLAB. The movements were designed to replicate human facial biological motion, maintaining smooth, human-like transitions while ensuring that each action adhered to the 10-second duration limit. Although the android’s silicone facial layers closely resembled human skin, some inherent textural differences remained. Nevertheless, a transparent rear panel revealed its internal mechanical components (See Fig. 1a), making its artificial nature explicit, despite its otherwise realistic human-like appearance when viewed frontally. During the Close condition, the android remained expressionless with its mouth closed and lips sealed for the entire 5-minute presentation phase. In the Gape condition, the model performed non-yawning mouth openings at regular intervals. In the Yawn condition, the model displayed full yawns as described above. During all conditions, the android was positioned within the chimpanzee’s “full visual field” (approximately 0–45°) or “peripheral visual field” (45–110°) relative to the sagittal plane of the participant’s eyes. The actions were repeated for 5 min, occurring a minimum of 15 times and a maximum of 20 times per condition. The experimenter, hidden behind a screen, remotely controlled the android’s actions via a button-operated remote panel (Fig. 2). Fig. 2 Trial structure of three exposure conditions and an initial baseline measurement. All sessions started with a five-minute baseline phase followed by a five-minute exposure condition (A) Close, (B) Gape, (C) Yawn and a five-minute post-stimulus observation phase (Post-Close, Post-Gape, Post-Yawn). Photos RMJM. Full size image Procedure and data collection Behavioural data was collected during an initial, 5-minute baseline period, during which the box containing the android was covered with a black cloth. This phase served as reference for each participant’s typical daily behaviour (Fig. 2). Each chimpanzee completed four 15-minute sessions, structured into three consecutive 5-minute phases: baseline, stimulus exposure (Yawn, Gape, or Close condition), and post-stimulus (Post-Yawn, Post-Gape, Post-Close), during which the android’s box was covered again. One keeper and one experimenter were present throughout all the sessions but remained behind a panel, to prevent any influence on the chimpanzees’ behaviour. The android was only visible within a 45° angle. As the chimpanzees could move freely within their enclosure, they might not have always had a direct view of the android. To account for this, the experimenter recorded in real time the duration (in seconds) that each chimpanzee spent looking at the android in each condition. The behaviour was scored by the experimenter with the use of a monitor behind the panel; the particular behaviours were corroborated from the additional cameras and later coded from video by the naïve coders. Each condition aimed to expose participants to between 15 and 20 instances of the android’s facial expressions. Furthermore, if a yawn or gape occurred outside the participant’s visual field, the expression was repeated while the chimpanzee was facing the android, ensuring visibility, without exceeding 20 presentations per condition. Individual sessions were separated by a minimum of 5 min and a maximum of 15 days (for 50% of the sessions, there were more than 12 h between sessions). To minimise interference with the centre’s daily routines, sessions conducted on the same day were separated by an average of 30 min. All conditions (except for the baseline phase) were counterbalanced across participants using a Latin Square design. The chimpanzees were tested individually between 09:30 and 18:00, in a familiar enclosure. All sessions were recorded with two Canon Legria HF G25, one at each side of the android, a Sony HDR-305 CX740VE above the android, and a Panasonic Lumix DMC-FZ200 directly below the android, all facing towards the enclosure to capture the chimpanzee positioned directly in front of the android. Additionally, two GoPro HERO + LCD cameras recorded supplementary angles: one inside the android’s transparent protective cube to document its facial movements and another on a tripod to capture areas outside the android’s 45º field of view. Behaviours such as Yawn, Gape and Close were previously defined in the literature, see Campbell, Provine, Madsen13,15,39. The chimpanzees’ behaviours were scored from video recordings using a focal continuous timed-event sampling77, focusing on the duration and frequencies of behaviours displayed. Analysis Two coders naïve to the purpose of the study, independently analysed all the videos and rated the number of chimpanzee yawns and gapes in the 5-minute baseline, stimulus (Yawn, Gape and Close) and post-stimulus phases (Post-Yawn, Post-Gape, Post-Close). Coder inter-rater reliability frequency of chimpanzee yawns was extremely high (agreement = 99%, Cohen’s Kappa = 0.99, 100% of sessions scored). Observers also coded lying-down behaviour and duration of looking at the stimuli. Lying down was defined as the whole body in a horizontal position, either on the ground or in a suspended hammock, with at least one shoulder in contact with the floor or the hammock. Inter-rater reliability for duration of lying down was perfect (agreement 100%, 100% of sessions scored). Inspection of raw data and Shapiro-Wilks tests of normality showed that all variables, except for Time spent Looking (TL) were significantly different from normality (p < 0.05). Therefore, non-parametric tests were used for analyses. Friedman test was used to analyse if the number of observed behaviours (yawns, gapes) varied across the different conditions. Wilcoxon tests were used for paired-wise comparisons. Values are reported as frequency of yawns and gapes per session, their mean and SEM per experimental condition, and the total number of yawns and gapes across all conditions. A secondary analysis was performed on the combined experimental and post experimental phases (10-min period, i.e., Yawn + Post-Yawn). All tests were two-tailed unless specified, and significance levels set at 0.05. Data were analysed using SPSS Statistics 25 for Windows (IBM Inc.).