Contagious Yawning in Gelada Baboons As a Possible Expression of Empathy

Contagious yawning in gelada baboons as a possible expression of empathy

E. Palagia,1, A. Leonea,b, G. Mancinia,b, and P. F. Ferrarib,c

aCentro Interdipartimentale Museo di Storia Naturale e del Territorio, Universita`di Pisa, 56011 Pisa, Italy; and Dipartimento di bBiologia Evolutiva e Funzionale and cNeuroscienze, Universita`di Parma, 43100 Parma, Italy

Communicated by Frans B. M. de Waal, Emory University, Atlanta, GA, September 29, 2009 (received for review May 9, 2009) Yawn contagion in humans has been proposed to be related to our scratching, perhaps indicative of increased anxiety (15). Al- capacity for empathy. It is presently unclear whether this capacity though those are the first attempts to investigate the phenom- is uniquely human or shared with other primates, especially mon- enon of contagious yawning in nonhuman primates, the evidence keys. Here, we show that in gelada baboons (Theropithecus remains meager, at least in monkeys, and more data are needed gelada) yawning is contagious between individuals, especially to better understand the natural or naturalistic conditions under those that are socially close, i.e., the contagiousness of yawning which yawning can be elicited and the possible social functions correlated with the level of grooming contact between individuals. of yawn contagion. This correlation persisted after controlling for the effect of spatial The infectiousness of yawning and the difficulty to suppress it association. Thus, emotional proximity rather than spatial proxim- when we observe someone else yawning are clear signs of a ity best predicts yawn contagion. Adult females showed precise connection present between two or more individuals and suggest matching of different yawning types, which suggests a mirroring that this phenomenon might involve not only purely motor mechanism that activates shared representations. The present aspects of the behavior but also more subtle emotional channels. study also suggests that females have an enhanced sensitivity and These observations have led some researchers to hypothesize a emotional tuning toward companions. These ﬁndings are consis- link between contagious yawning and empathy (16–19). In tent with the view that contagious yawning reveals an emotional humans, it has been reported that subjects showing higher levels connection between individuals. This phenomenon, here demon- of contagion to yawn stimuli also score higher in questionnaires strated in monkeys, could be a building block for full-blown evaluating empathy and mental state attribution (18). Although empathy. debated, there is no consensus about the possibility that nonhuman primates are capable of empathizing with others. How- emotional contagion ͉ matching behavior ͉ mirror neurons ͉ ever, there is a range of phenomena, from sensitivity to others’ social bonding ͉ Theropithecus gelada distress to reassuring behaviors from both experimental and observational studies, which suggest some level of empathy in awning is a common phenomenon in vertebrates, and in nonhuman primates (20–23). Moreover, in both humans and Yprimates it is present since birth (1). From an ethological animals empathy is biased toward individuals who are more point of view, yawning is one of the best examples of a fixed similar, familiar, or socially closer (24). It is assumed that shared action pattern. Once started, a yawn is unstoppable and uncon- representations are more easily activated the more two individ- tainable. Motor patterns of yawning are stereotyped and occur uals have in common. Because empathy is biased toward such in essentially the same form in different contexts, from resting to individuals, we expect that contagious yawning, if empathy- social interactions (2, 3). Yawning may also be a stress indicator based, should be similarly biased. Although the hypothetical link between contagious yawning and empathy is appealing, it has and a sign of neurological pathologies (4). From a physiological never been empirically tested in any species, including humans. perspective, it has been proposed that yawning maintains mental Here, we report that yawning is contagious in a nonhuman efficiency by regulating brain temperature through a cooling primate, the gelada baboon, and that this response seems mechanism (5, 6). unrelated to external stressful events. Moreover, our data dem- There are several theories about the possible function of onstrate that yawn contagion is more common between individ- yawning (7, 8). Communication theories propose yawning as a uals with higher levels of affiliation, thus suggesting that the way animals synchronize group behaviors during rest–activity roots of empathy could may be present in nonhuman primates. cycles or communicate drowsiness or stress. Arousal theories propose, instead, that yawning should help subjects maintain Results their attention levels and that it may have evolved to promote We recorded 3,229 yawns by means of all-occurrences sampling maintenance of vigilance and/or shared alertness (2, 9). (403 h). Geladas performed three different yawning displays (see In humans yawning is demonstrably contagious as it is easily Fig. 1) with the following hourly frequencies: (i) covered teeth triggered by seeing, hearing, reading, or simply thinking about (CT), individual mean 0.120 Ϯ 0.022 SE; (ii) uncovered teeth another individual yawning (3, 10). More than 50% of human (UT), individual mean 0.115 Ϯ 0.018 SE; and (iii) uncovered subjects yawned within a few minutes after having watched a gums (UG), individual mean 0.219 Ϯ 0.144 SE. Males and video of a yawning person (10). The power of contagious females did not differ in their baseline levels of CT and UT (CT: yawning is suggested by interspecific effects (11), even though Exact Mann–Whitney U ϭ 22, Nm ϭ 5, Nf ϭ 9, P ϭ 0.947; UT: this phenomenon is still under debate (12). exact Mann–Whitney U ϭ 21, Nm ϭ 5, Nf ϭ 9, P ϭ 0.841); In chimpanzees (Pan troglodytes), yawning can be induced by however, sex difference was found for UG (males Ͼ females: observing a video of a conspecific yawn (13), even though in that study the contagious response was limited to a few of the tested individuals. Recently, however, Campbell et al. (14) demon- Author contributions: E.P. and P.F.F. designed research; A.L. and G.M. performed research; strated at the population level that chimpanzees show contagious E.P., A.L., and G.M. analyzed data; and E.P. and P.F.F. wrote the paper. yawning in response to 3D-animated chimpanzee yawns, thus The authors declare no conﬂict of interest. confirming the results obtained in previous studies. In macaques 1To whom correspondence should be addressed. E-mail: [email protected] . (Macaca spp.), yawning responses elicited by the video of This article contains supporting information online at www.pnas.org/cgi/content/full/ unfamiliar monkeys yawning were accompanied by self- 0910891106/DCSupplemental.

19262–19267 ͉ PNAS ͉ November 17, 2009 ͉ vol. 106 ͉ no. 46 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0910891106 Downloaded by guest on September 28, 2021 Fig. 1. Three different yawning displays performed by geladas. (A) A CT yawning. (B) An UT-yawning. (C) An UG-yawning.

ϭ ϭ ϭ ϭ ␹2 ϭ ϭ ϭ exact Mann–Whitney U 6.5, Nmales 5, Nfemales 9, P 0.021; condition CT: exact Friedman test r 4.07, df 2, n 0.031). 9, P ϭ 0.139) (Fig. 4A). The Dunnett test (posthoc test) revealed The concurrent presence of three observers over the whole a trend for a matching response in the UT condition (UT-UT Ͼ period of observation permitted us to record the identity of each UT-UG: Dunnett’s q ϭ 1.83, 0.05 Ͻ P Ͻ 0.1). More interestingly, group member that was in visual and/or auditory contact with we obtained even more significant results when we restricted the the yawner and, consequently, to assess which individuals very analysis to the response displayed by females only. In this case likely were not able to perceive the presence of the yawn. To the matching response was present for CT and UT (condition evaluate the presence of contagion, we compared the experi- UG: exact Friedman test ␹2 ϭ 0.00, df ϭ 2, n ϭ 9, P ϭ 1.00; mental condition, defined as how often an individual X (re- r ceiver) yawns after the first individual Y (stimulus) yawned, with the baseline condition, defined as how often individual X yawns when individual Y is nearby (within Ϸ10 m) but does not yawn. A If the receiver yawned within the time window of 5 min after the yawning of the stimulus individual, the receiver response was considered as affected by the previous stimulus. Following the procedure used in previous experiments on yawning contagion in nonhuman primates (13, 15), if an individual yawned outside the time window of 5 min after the previous yawning, the yawning event was not considered as affected by the previous stimulus and was included in the baseline condition. In geladas, each kind of yawning display can be accompanied by a loud precall and/or a long-distance vocalization (25). To evaluate the effect of such acoustic components in yawning contagion, we analyzed responses according to different sensory modalities characterizing the stimulus: (i) visual and acoustic (VϩA), and (ii) acoustic alone (A). In adults and subadults we found that receivers’ yawning responses were significantly more frequent when the stimulus individual performed a yawn than when it engaged in any other B behaviors except yawning (VϩA: exact Wilcoxon’s T ϭ 0, n ϭ 14, P ϭ 0.0001; A: exact Wilcoxon’s T ϭ 2, n ϭ 14, P ϭ 0.005) (Fig. 2). Contagion was also present when the analysis was limited to females (VϩA: exact Wilcoxon’s T ϭ 0; n ϭ 9; P ϭ 0.002; A: exact Wilcoxon’s T ϭ 4, n ϭ 9, P ϭ 0.008). In contrast, no statistical difference was found for the immature subjects (exact Wilcoxon’s T ϭ 13, n ϭ 7, P ϭ 0.547). For immature animals it was not possible to analyze separately the two sensory modalities characterizing the stimulus because of the extremely low frequency of response events. We calculated the individual frequency of yawning contagion during each min of observation (for 5 min after the yawn of the stimulus individual), and we found that contagion was more ␹2 ϭ frequent during the second min (exact Friedman test r 10.303, df ϭ 4, n ϭ 14, P ϭ 0.029) (Fig. 3). As far as the matching response is concerned (i.e., if the stimulus individual performed a CT yawn, the receiver responded with a CT yawn), we included in the analysis only those Fig. 2. Frequency of yawning. (A) Frequency of yawning performed in the contagion events based on visual cues. We found that when the presence and absence of the visual stimulus is shown. We considered only nonvocalized yawning as stimulus; however, we cannot exclude the inﬂuence stimulus was a female, the response matched the type of yawn of audible respiratory movements. (B) Frequency of yawning performed in the (CT, UT, and UG) displayed by the stimulus individual (condi- presence and absence of the acoustic stimulus (vocalized yawning) is shown. ␹2 ϭ ϭ ϭ ϭ tion UG: exact Friedman test r 5.20, df 2, n 9, P 0.123; In this case the receiver was not able to see the ﬁrst yawner so the visual cue ANTHROPOLOGY ␹2 ϭ ϭ ϭ ϭ condition UT: exact Friedman test r 7.52, df 2, n 9, P can be excluded.

Palagi et al. PNAS ͉ November 17, 2009 ͉ vol. 106 ͉ no. 46 ͉ 19263 Downloaded by guest on September 28, 2021 Fig. 3. Frequency of contagion distribution as a function of the minutes of observation is shown. Fig. 5. Grooming and contagion. The scatter-plot shows the correlation between the frequency of grooming interchange (y axis) and the level of contagion (x axis). ␹2 ϭ ϭ ϭ ϭ condition UT: exact Friedman test r 14.00, df 2, n 9, P 0.0001; condition CT: exact Friedman test ␹2 ϭ 10.67, df ϭ 2, n ϭ r ␹2 ϭ ϭ ϭ ϭ 9, P ϭ 0.0017). For the CT and UT conditions the Dunnett test UT: exact Friedman test r 1.63, df 2, n 9, P 0.58; ␹2 ϭ ϭ ϭ ϭ (posthoc test) gave the following results: condition CT (CT-CT condition CT: exact Friedman test r 1.73, df 2, n 9, P vs. CT-UT: Dunnett’s q ϭ 2.6, P Ͻ 0.01; CT-CT vs. CT-UG: 0.53) (Fig. 4B), even when we restricted the analysis to the Dunnett’s q ϭ 1.96, P Ͻ 0.05) and condition UT (UT-UT vs. response displayed by males only (condition UG: exact Friedman test ␹2 ϭ 3.18, df ϭ 2, n ϭ 9, P ϭ 0.20; condition UT: exact UT-CT: Dunnett’s q ϭ 3.52, P Ͻ 0.01; UT-UT vs. UT-UG: r Friedman test ␹2 ϭ 2.60, df ϭ 2, n ϭ 9, P ϭ 0.44; condition CT: Dunnett’s q ϭ 2.84, P Ͻ 0.01). r exact Friedman test ␹2 ϭ 0.20, df ϭ 2, n ϭ 9, P ϭ 1.00). On the contrary, we did not find any statistical evidence for a r To calculate the level of reciprocal contagion for each dyad we matching response when the stimulus was a male (condition UG: ␹2 ϭ ϭ ϭ ϭ divided the number of XY contagion events plus number of YX exact Friedman test r 1.33, df 2, n 9, P 0.60; condition contagion event per the number of opportunities in which Y perceived X’s yawns plus number of opportunities in which X perceived Y’s yawns. A Last, we found a positive correlation between hourly grooming frequency and yawning contagion based on visual contact, so that we were confident that the receiver was aware of the stimulus’ identity [row-wise permutation test Kr ϭ 57, Taurw ϭ 0.18, n ϭ 10 individuals (45 dyads), P ϭ 0.02] (Fig. 5). However no correlation was found between yawning contagion and interindividual spatial association (proximity plus contact sitting frequency) [row-wise permutation test Kr ϭϪ1, Taurw ϭ Ϫ0.0033, n ϭ 10 individuals (45 dyads), P ϭ 0.50]. This analysis was performed on the unit A (n ϭ 10) because there was not any grooming exchange between the individuals of the two units. We did not perform the same analysis on the unit B because of the low sample size (n ϭ 4) and the absence of grooming interactions B in two dyads. In other words, the more two individuals groomed each other, the more they responded with a yawn to the other’s yawn. One could argue that individuals groom each other more when they are in proximity, and that proximity exposes them more toward the other’s yawning. However, the correlation between the frequency of grooming and yawning contagion remained significant even after controlling for interindividual spatial association (proximity plus contact sitting frequency) not involving grooming interactions [partial row-wise matrix permutation TauKr ϭ 0.19, n ϭ 10 individuals (45 dyads), P ϭ 0.03]. Thus, proximity does not seem to explain the level of yawning contagion. We obtained even a higher level of significance when Fig. 4. Matching response. (A) Type of yawning response as a function of we limited the analyses to the females [grooming frequency and type of previous yawning when the ﬁrst yawner (stimulus) was a female is yawning contagion: row-wise permutation test Kr ϭ 40, Taurw ϭ shown. A matching response is present only for CT and UT. (B) Type of yawning ϭ ϭ response as a function of type of previous yawning when the ﬁrst yawner 0.48, n 7 individuals (21 dyads), P 0.001; proximity plus (stimulus) was a male is shown. There is no matching response for any of the contact sitting frequency and yawning contagion: row-wise three types of yawning. permutation test Kr ϭ 18, Taurw ϭ 0.21, n ϭ 7 individuals (21

19264 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0910891106 Palagi et al. Downloaded by guest on September 28, 2021 dyads), P ϭ 0.106; grooming and yawning frequency controlled neurons. However, a more recent study (34) found that the for proximity plus contact sitting: partial row-wise matrix per- observation of yawning in humans activates these specific areas. mutation TauKr ϭ 0.42, n ϭ 7 (21 dyads), P ϭ 0.005]. This More data are clearly needed, but overall it seems imitation and analysis was restricted to the females of the unit A only (n ϭ 7) contagion are different types of phenomena, even though they because of the absence of grooming exchange between the may share some neural mechanisms (34–36). members of the two units. The same analysis could not be In the gelada baboons, yawn contagion was particularly evi- performed on males because of the low sample size (males of the dent when the analysis was limited to adult females, which also unit A ϭ 3; males of the unit B ϭ 2). showed an additional feature: they tended to match the type of yawn. This finding further supports the notion that a neural Discussion mechanism involved in behavioral matching is probably involved The present findings indicate that yawning in gelada baboons is in this phenomenon. If mirror neurons are involved in contagion contagious and can be elicited via both visual and acoustic they very likely can act, through an indirect pathway (32), on modalities. This latter result is in line with previous data (4) on limbic structures and subcortical areas that are involved in the contagious yawning by blind human subjects, thus suggesting the generation and control of the yawning motor patterns. importance of multimodal perception in yawn triggering. Fur- From a social perspective, the matching responsiveness shown thermore, activation of matched motor programs via different by gelada females may be interpreted in light of the female social sensory modalities has been shown in monkeys. For example, network characteristic of this species. The relationships within pig-tailed macaques (Macaca nemestrina) increased feeding be- the typical gelada one-male unit (OMU) revolve around adult havior, even though they were fully satiated, after just hearing females, who form the core of the cohesion and stability typical another monkey eat without visual input (26). Motor facilitation of OMUs (37). In some cases, the strength of female bonds to specific acoustic stimuli has also been demonstrated in the suffices to maintain OMU integrity despite the absence of the macaque motor cortex, suggesting that motor output may be male (25). Thus, the matching response recorded between facilitated by multiple sensory modalities (27). females probably reflects the need and ability of females to stay The contagion effect of yawning may be interpreted as a type in tune with each others’ behavioral activities and to form of response occurring in highly social animals that need to coalitions and alliances based on a precise reading of others’ synchronize behavioral activities (20). Coordinating activities behavior. An important implication of the present findings is among group members has an undoubted advantage because it that the contagion effect triggered by yawning has not only a promotes social cohesiveness. In fact, we observed such coor- main consequence to synchronize two individuals but it seems dination in the social context of our baboons, when they were also to influence affective components of the behavior. Through awake and relaxed, often coinciding with grooming sessions or the involuntary reenactment of an observed behavior, emotional with transitions from rest to activity, or vice versa. states related to the behavior may be arise in the observer. This Yawn contagion was present only in adults. The absence in idea has been theorized by Preston and de Waal (24) and likely infants and juveniles has also been reported for humans, in which involves neural mechanisms that, during the perception of an children aged younger than 5 years do not show this contagion action or of a facial expression, activate shared representations (28). The relative insensitivity of immature subjects to yawning (31, 38). may reflect a developmental immaturity of their social cognitive Recently, this hypothesis has been tested in tufted capuchin skills and/or brain structures involved in processing social information. In most social animals, including primates, adults have monkeys (Cebus apella). When monkeys were being imitated by the main role in group decision-making and regulating the group a human experimenter they increased their liking and interac- daily activities, whereas the young tend to passively follow adults, tions toward the imitator compared with a nonimitator (39). It especially the mother (29). Thus, synchronizing and coordinating has been proposed that in a highly social species, such as the one’s own behavior with that of conspecifics could be less capuchin monkey, activities are highly synchronized and this relevant for young individuals, which are rather more sensitive might provide a sufficient degree of behavioral matching to to maintain proximity with their mothers in their first years of life promote affiliative behaviors between individuals. Similar ef- before weaning (30). fects may be produced by yawn contagion. Even though our study The criteria we adopted for the analysis of contagion allowed could not disentangle the cause–effect relationship between us to exclude that yawning responses were elicited by any kind yawn contagion and affiliation, the correlation between the level of stressful event. In fact, we excluded all yawning events of contagion and the rate of grooming suggests that yawn associated with behavior indicative of stressful conditions (e.g., contagion is facilitated by an emotional connection between raised eye browse, self-scratching, self-grooming, body shaking, stimulus animals and receivers. lip flip, urination, defecation, gravel digging, etc.). An alternative explanation, however, is that individuals who Even though yawn contagion requires the reenactment of a often groom each other have more opportunities to observe and behavior, it cannot be considered an imitative or mimicry catch the yawns of the other. However, reduced interindividual process because of the reflexive and stereotypical nature of this distances (measured by proximity and contact sitting) did not chain reaction. However, this phenomenon could be compatible correlate with yawn contagion and the correlation between with the idea of a common mechanism active during the grooming and yawn contagiousness persisted after statistically perception and reenactment of yawning. The discovery of mirror controlling for spatial association. Thus, social closeness seems neurons in macaques has prompted the idea that an action– to predict yawn contagiousness, which is consistent with the idea perception mechanism could be responsible for important cog- that yawn contagion is mediated by empathy (24). nitive functions such as action understanding, response facilita- Another hypothesis, not necessarily mutually exclusive with tion, and other behavioral matching (31, 32). A human mirror the emotional connection hypothesis, is that yawn contagion in mechanism for action understanding and imitation homologous geladas can be a sign of mood convergence. Because gelada to that of the macaque has been supported by several neuro- baboons are highly social animals, which behave in a highly physiological and brain imaging studies (33). Only recently, synchronized and cohesive way, the capacity to communicate a however, has the hypothesis that a similar mechanism may sleepy mood may result in a better coordinated group activity for account for contagious yawning been empirically investigated in sleeping or waking. However, this hypothesis cannot explain the

humans. The findings obtained so far failed to find activation in results presented here because the data were cleaned from the ANTHROPOLOGY the traditional parietal-premotor areas populated by mirror resting–activity transition phases (mainly morning and evening)

Palagi et al. PNAS ͉ November 17, 2009 ͉ vol. 106 ͉ no. 46 ͉ 19265 Downloaded by guest on September 28, 2021 and included events that did not necessarily follow sleep-resting The analysis of contagion in presence of the visual cue has been performed activities. according to the following criteria: (i) absence of external stimuli (including Yawning has been conserved in its stereotypic forms through- visitors) alerting the attention of the first yawner (stimulus) and the receiver (at out mammals and other vertebrate taxa, demonstrating its least from the observer perspective); and (ii) the stimulus yawner had to maintain its gaze toward the target of its activity/behavior (without shifting its gaze important basic physiological function. In primates, its function toward other stimuli). Obviously, in this analysis the acoustic component caused has been extended to the social domain. The demand for by audible respiratory movements could not be completely excluded. synchronizing activities in highly social species requires that The analysis of contagion in the presence of acoustic cues (and in absence individuals read each others’ behaviors and match it accurately. of visual cues) has been performed according to the following criteria: (i) Matching one’s own behavior with that of others, independently absence of visual contact between the first yawner (stimulus) and the poten- on whether this occurs consciously or not, has recently been tial receiver (presence of visual barriers); (ii) a vocalized yawn (recorded by shown to promote affiliation between individuals through an observer 1 was considered ‘‘not perceived,’’ when observer 2, which followed empathic connection (39). The presence of yawn contagion in the potential receiver, did not hear any vocalization. Moreover, both the analyses were performed according to the following criteria: (i) the yawn gelada baboons and its relation with the degree of bonding sequence had to be not accompanied or associated with signs of stress or between individuals suggests that in this species are probably arousal such as raised eye brows, scratching, self-grooming, body shake, lip present the basic components of the multilayered empathy well flip, urination, defecation, gravel digging, and copulation and (ii) the whole known of humans and, at least in part, of the great apes. yawn sequence had to occur when the animals involved in the observation were awake and relaxed (i.e., not engaged in feeding activities or in agonistic, Methods sexual, and play encounters). Subjects and Housing. The colony of gelada baboons (T. gelada) housed at the By focal animal sampling (30 h of observation per subject), we were able to NaturZoo (Rheine, Germany) was made up of two OMUs, which comprised record all of the proximity and grooming sessions performed by each focal two adult males, eight adult females, three subadult males, one subadult animal with any other group member. Each subject was followed every day female, three immature males, and four immature females) (Table S1). The and at different times to obtain data covering the entire day in balanced two OMUs were housed in the same enclosure with both an indoor (a room proportions as much as possible. Ϸ36 m2) and outdoor facility (an island of Ϸ2,700 m2 surrounded by a boundary ditch). The animals of the two OMUs could interact freely with one Data Analysis and Statistics. When the analyses were carried out at the another. The size of the island allowed the scattering of geladas and, conse- individual level, we used nonparametric statistical approach (42). The Wil- quently, the formation of small groups of animals that frequently changed. coxon matched pairs sign rank test was applied to compare the frequency of This situation, together with the good observability conditions, allowed us to yawns performed after a previous yawn (experimental condition) and those easily define the stimulus animal (the first yawner) and the potential receivers. performed without the presence of any previous yawn (baseline condition). The enclosures were equipped with everything necessary to allow the Friedman’s two-way ANOVA was used to test for differences in the latency of geladas to move freely in all three dimensions. Specifically, the outside en- yawning response within a 5-min time window and evaluate whether a closure was located in an open naturally hilly area equipped with trees, matching response in the type of yawn (CT, UT, and UG) between the stimulus branches, ropes, and dens (Fig. S1). yawner and the receiver was present. In the case of a significant main effect, The animals were fed with grass, vegetables, and pellets, which were scattered we used the Dunnett multiple comparison test (post hoc test) to determine on the ground three times a day (9:30 AM, 11 AM, 2:30 PM). Water was available which responses were significantly different (42). ad libitum. No stereotypic or aberrant behaviors characterized the study group. We used exact tests according to the threshold values suggested by Mundry The research complied with current laws of Germany and Italy. and Fischer (43). Statistical analyses were performed by using Microsoft Excel and SPSS 12.0. Data Collection. We collected behavioral data during 4 months of observation To control for the possible correlation between the level of affinitive (June to October 2007) on all of the subjects of the colony. We concurrently relationships and the yawning contagion we applied the row-wise matrix used two methods of observation: all-occurrences sampling and focal-animal permutation test. In interaction matrices data are not independent because sampling (40). During all-occurrences sampling (a total of 403 h of observa- observations concerning the same individual recur. This results in dependency within and between rows and columns of the same individual. The row-wise tion) we recorded all of the yawns performed by each subject. Data were matrix correlation compares only the values within the same row, overcoming collected vocally through a voice recorder, and the records were later the problem of the interdependency of the data. The K row-wise matrix computer-transcribed. Before starting systematic data collection, the three r correlation coefficient is based on a weighted sum of the correlation between observers underwent a training period (Ϸ90 h). all dyads of corresponding rows of the two matrices and it is defined by using During the training phase (the trainer was E.P.), the same focal animal was Kendall’s rank order correlation coefficient (44). This method, applied to followed by the observers simultaneously, and the data were then compared. square matrices, can be used with small sample sizes because no assumptions Training was over when the observations matched in 95% of cases [␬ for are made about the underlying distribution (the smallest sample size for interobserver reliability according to Martin and Bateson (41)]. The observa- square matrices that can acquire a probability value Ͻ5% is four). The matrices tions took place daily over 6-hr periods that spanned morning (from 6 AM) and were permutated 10,000 times. Each analysis was carried out with the soft- evening (until 10 PM). ware MatMan 1.0. During each yawning occurrence we recorded the exact time of the yawn, As a second step, we used the Tau K matrix partial correlation (44) to test the posture assumed by the yawner (defined as sitting, standing, and lying), r the null hypothesis that the potential correlation between the levels of the identity of the yawner, the presence of vocalization, the level of mouth grooming and contagion was unaffected by the reduced interindividual opening (CT, UT, UG) (Fig. 1). Each type of yawn (CT, UT, UG) could be spatial distribution. For this test we constructed a third matrix of the associ- accompanied by a vocalization (precall and/or yawning vocalizations) (25). ation frequency measured by proximity plus contact sitting levels shown by Moreover, we sampled the behavioral item occurring during the 10 s before each dyadic pair. and 10 s after the yawn (7) that included further ethogram items. Specifically, we recorded a series of state of activity and behaviors classified into social and ACKNOWLEDGMENTS. We thank Johann Achim, the Director of the Rheine- nonsocial. Resting, sleeping, walking, standing, grooming, feeding, contact Zoo, for permission to work at the zoo; Annika Paukner for the accurate sitting, and proximity were scored as states. Other behavioral items, such as revision of a previous version of the manuscript; Han de Vries and Flavia raised eye brows, scratching, self-grooming, body shake, lip flip, urination, Chiarotti for statistical advice; and Mariangela Mia Ferrero for help with data defecation, gravel digging, and copulation were scored as events. For each collection. This work was supported by Ministero dell’Universita` e della behavioral item we recorded the identity of the actor and the receiver. Ricerca Grants 2004057380 and 2006052343.

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