Chimpanzees Show a Developmental Increase in Susceptibility to Contagious Yawning: A Test of the Effect of Ontogeny and Emotional Closeness on Yawn Contagion

Contagious yawning has been reported for humans, dogs and several non-human primate species, and associated with empathy in humans and other primates. Still, the function, development and underlying mechanisms of contagious yawning remain unclear. Humans and dogs show a developmental increase in susceptibility to yawn contagion, with children showing an increase around the age of four, when also empathy-related behaviours and accurate identification of others’ emotions begin to clearly evince. Explicit tests of yawn contagion in non-human apes have only involved adult individuals and examined the existence of conspecific yawn contagion. Here we report the first study of heterospecific contagious yawning in primates, and the ontogeny of susceptibility thereto in chimpanzees, Pan troglodytes verus. We examined whether emotional closeness, defined as attachment history with the yawning model, affected the strength of contagion, and compared the contagiousness of yawning to nose-wiping. Thirty-three orphaned chimpanzees observed an unfamiliar and familiar human (their surrogate human mother) yawn, gape and nose-wipe. Yawning, but not nose-wiping, was contagious for juvenile chimpanzees, while infants were immune to contagion. Like humans and dogs, chimpanzees are subject to a developmental trend in susceptibility to contagious yawning, and respond to heterospecific yawn stimuli. Emotional closeness with the model did not affect contagion. The familiarity-biased social modulatory effect on yawn contagion previously found among some adult primates, seem to only emerge later in development, or be limited to interactions with conspecifics. The influence of the ‘chameleon effect’, targeted vs. generalised empathy, perspective-taking and visual attention on contagious yawning is discussed.     

Familiarity Bias and Physiological Responses in Contagious Yawning by Dogs Support Link to Empathy

In humans, the susceptibility to yawn contagion has been theoretically and empirically related to our capacity for empathy. Because of its relevance to evolutionary biology, this phenomenon has been the focus of recent investigations in non-human species. In line with the empathic hypothesis, contagious yawning has been shown to correlate with the level of social attachment in several primate species. Domestic dogs (Canis familiaris) have also shown the ability to yawn contagiously. To date, however, the social modulation of dog contagious yawning has received contradictory support and alternative explanations (i.e., yawn as a mild distress response) could explain positive evidence. The present study aims to replicate contagious yawning in dogs and to discriminate between the two possible mediating mechanisms (i.e., empathic vs. distress related response). Twenty-five dogs observed familiar (dog’s owner) and unfamiliar human models (experimenter) acting out a yawn or control mouth movements. Concurrent physiological measures (heart rate) were additionally monitored for twenty-one of the subjects. The occurrence of yawn contagion was significantly higher during the yawning condition than during the control mouth movements. Furthermore, the dogs yawned more frequently when watching the familiar model than the unfamiliar one demonstrating that the contagiousness of yawning in dogs correlated with the level of emotional proximity. Moreover, subjects’ heart rate did not differ among conditions suggesting that the phenomenon of contagious yawning in dogs is unrelated to stressful events. Our findings are consistent with the view that contagious yawning is modulated by affective components of the behavior and may indicate that rudimentary forms of empathy could be present in domesticated dogs.     

Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes)

Yawn contagion is not restricted to humans and has also been reported for several non-human animal species, including chimpanzees (Pan troglodytes). Contagious yawning may lead to synchronisation of behaviour. However, the function of contagious yawning is relatively understudied. In this study, we investigated the function of contagious yawning by focusing on two types of signal providers: close social associates and leaders. We provided a captive chimpanzee colony with videos of all individuals of their own group that were either yawning, or at rest. Consistent with other studies, we demonstrated that yawning is contagious for chimpanzees, yet we did not find any effect of relationship quality on yawn contagion. However, we show that yawn contagion is significantly higher when the video model is a yawning male than when the video model was a yawning female, and that this effect is most apparent among males. As males are dominant in chimpanzee societies, male signals may be more relevant to the rest of the group than female signals. Moreover, since chimpanzees form male-bonded societies, male signals are especially relevant for other males. Therefore, we suggest that the sex-differences of yawning contagion among chimpanzees reflect the function of yawning in the synchronisation of behaviour.     

Dogs catch human yawns

This study is the first to demonstrate that human yawns are possibly contagious to domestic dogs (Canis familiaris). Twenty-nine dogs observed a human yawning or making control mouth movements. Twenty-one dogs yawned when they observed a human yawning, but control mouth movements did not elicit yawning from any of them. The presence of contagious yawning in dogs suggests that this phenomenon is not specific to primate species and may indicate that dogs possess the capacity for a rudimentary form of empathy. Since yawning is known to modulate the levels of arousal, yawn contagion may help coordinate dog-human interaction and communication. Understanding the mechanism as well as the function of contagious yawning between humans and dogs requires more detailed investigation.     

Social Modulation of Contagious Yawning in Wolves

On the basis of observational and experimental evidence, several authors have proposed that contagious yawn is linked to our capacity for empathy, thus presenting a powerful tool to explore the root of empathy in animal evolution. The evidence for the occurrence of contagious yawning and its link to empathy, however, is meagre outside primates and only recently domestic dogs have demonstrated this ability when exposed to human yawns. Since dogs are unusually skilful at reading human communicative behaviors, it is unclear whether this phenomenon is deeply rooted in the evolutionary history of mammals or evolved de novo in dogs as a result of domestication. Here we show that wolves are capable of yawn contagion, suggesting that such ability is a common ancestral trait shared by other mammalian taxa. Furthermore, the strength of the social bond between the model and the subject positively affected the frequency of contagious yawning, suggesting that in wolves the susceptibility of yawn contagion correlates with the level of emotional proximity. Moreover, female wolves showed a shorter reaction time than males when observing yawns of close associates, suggesting that females are more responsive to their social stimuli. These results are consistent with the claim that the mechanism underlying contagious yawning relates to the capacity for empathy and suggests that basic building blocks of empathy might be present in a wide range of species.     

Contagion of Cooperation in Static and Fluid Social Networks

Cooperation is essential for successful human societies. Thus, understanding how cooperative and selfish behaviors spread from person to person is a topic of theoretical and practical importance. Previous laboratory experiments provide clear evidence of social contagion in the domain of cooperation, both in fixed networks and in randomly shuffled networks, but leave open the possibility of asymmetries in the spread of cooperative and selfish behaviors. Additionally, many real human interaction structures are dynamic: we often have control over whom we interact with. Dynamic networks may differ importantly in the goals and strategic considerations they promote, and thus the question of how cooperative and selfish behaviors spread in dynamic networks remains open. Here, we address these questions with data from a social dilemma laboratory experiment. We measure the contagion of both cooperative and selfish behavior over time across three different network structures that vary in the extent to which they afford individuals control over their network ties. We find that in relatively fixed networks, both cooperative and selfish behaviors are contagious. In contrast, in more dynamic networks, selfish behavior is contagious, but cooperative behavior is not: subjects are fairly likely to switch to cooperation regardless of the behavior of their neighbors. We hypothesize that this insensitivity to the behavior of neighbors in dynamic networks is the result of subjects’ desire to attract new cooperative partners: even if many of one’s current neighbors are defectors, it may still make sense to switch to cooperation. We further hypothesize that selfishness remains contagious in dynamic networks because of the well-documented willingness of cooperators to retaliate against selfishness, even when doing so is costly. These results shed light on the contagion of cooperative behavior in fixed and fluid networks, and have implications for influence-based interventions aiming at increasing cooperative behavior.     

Yawning: An evolutionary perspective

Yawning is a ubiquitous activity among humans, nonhuman primates, mammals, birds and other vertebrates. Comparative analysis suggests that yawning has two major features: (1) communication — whereby the behavior of other individuals is affected, and (2) direct physiological benefit — whereby the organism is receiving some direct physiological benefit from yawning. Various functional hypotheses used to explain yawning in an evolutionary context are reviewed. The contagious nature in humans and the manifest lack of contagion in other species suggests that yawning in humans has a different and as yet poorly understood evolutionary history.     

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.     

Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy

Humans favor others seen as similar to themselves (ingroup) over people seen as different (outgroup), even without explicitly stated bias. Ingroup-outgroup bias extends to involuntary responses, such as empathy for pain. However, empathy biases have not been tested in our close primate relatives. Contagious yawning has been theoretically and empirically linked to empathy. If empathy underlies contagious yawning, we predict that subjects should show an ingroup-outgroup bias by yawning more in response to watching ingroup members yawn than outgroup. Twenty-three chimpanzees (Pan troglodytes) from two separate groups watched videos of familiar and unfamiliar individuals yawning or at rest (control). The chimpanzees yawned more when watching the familiar yawns than the familiar control or the unfamiliar yawns, demonstrating an ingroup-outgroup bias in contagious yawning. These results provide further empirical support that contagious yawning is a measure of empathy, which may be useful for evolutionary biology and mental health.     

Forest Structure and Support Availability Influence Orangutan Locomotion in Sumatra and Borneo

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites—two on Sumatra (Pongo abelii) in the dry‐lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau—to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age‐sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

Orangutans (Pongo pygmaeus) Remember Old Acquaintances

Many social animals can discriminate between familiar and unfamiliar faces. Orangutans, however, lead a semi-solitary life and spend much of the day alone. As such, they may be less adept at recognizing conspecifics and are a good model for determining how social structure influences the evolution of social cognition such as facial recognition. The present study is the first report of whether orangutans can distinguish among individual faces. We adopted a preferential looking method and found that orangutans used facial discrimination to identify known conspecifics. This suggests that frequent and intense social interaction is not necessary for facial discrimination, although our findings were limited by the small number of stimuli and the unequal numbers of male and female orangutans depicted in the stimuli.     

Response facilitation in the four great apes: is there a role for empathy?

Contagious yawning is a form of response facilitation found in humans and other primates in which observing a model yawning enhances the chance that the observer will also yawn. Because contagious yawning seems to be more easily triggered when models are conspecifics or have a strong social bond with the observer, it has been proposed that contagious yawning is linked to empathy. A possible way to test this hypothesis is to analyze whether individuals’ responses differ when they observe models yawning or performing different involuntary (i.e., nose wiping, scratching) and voluntary (i.e., hand closing, wrist shaking) actions that are not linked to empathy. In this study, we tested the four great ape species with two different setups by exposing them to a human experimenter repeatedly performing these actions online, and video-recorded conspecifics repeatedly performing these actions on a screen. We examined which behaviors were subject to response facilitation, whether response facilitation was triggered by both human models and video-recorded conspecifics, and whether all species showed evidence of response facilitation. Our results showed that chimpanzees yawned significantly more when and shortly after watching videos of conspecifics (but not humans) yawning than in control conditions, and they did not do so as a response to increased levels of anxiety. For all other behaviors, no species produced more target actions when being exposed to either model than under control conditions. Moreover, the individuals that were more “reactive” when watching yawning videos were not more reactive when exposed to other actions. Since, at least in chimpanzees, (1) subjects only showed response facilitation when they were exposed to yawning and (2) only if models were conspecifics, it appears that contagious yawning is triggered by unique mechanisms and might be linked to empathy.     

Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo

Orangutans are amongst the most craniometrically variable of the extant great apes, yet there has been no attempt to explicitly link this morphological variation with observed differences in behavioral ecology. This study explores the relationship between feeding behavior, diet, and mandibular morphology in orangutans. All orangutans prefer ripe, pulpy fruit when available. However, some populations of Bornean orangutans (Pongo pygmaeus morio and P. p. wurmbii) rely more heavily on bark and relatively tough vegetation during periods of low fruit yield than do Sumatran orangutans (Pongo abelii). I tested the hypothesis that Bornean orangutans exhibit structural features of the mandible that provide greater load resistance abilities to masticatory and incisal forces. Compared to P. abelii, P. p. morio exhibits greater load resistance abilities as reflected in a relatively deeper mandibular corpus, deeper and wider mandibular symphysis, and relatively greater condylar area. P. p. wurmbii exhibits most of these same morphologies, and in all comparisons is either comparable in jaw proportions to P. p. morio, or intermediate between P. p. morio and P. abelii. These data indicate that P. p. morio and P. p. wurmbii are better suited to resisting large and/or frequent jaw loads than P. abelii. Using these results, I evaluated mandibular morphology in P. p. pygmaeus, a Bornean orangutan population whose behavioral ecology is poorly known. Pongo p. pygmaeus generally exhibits relatively greater load resistance capabilities than P. abelii, but less than P. p. morio. These results suggest that P. p. pygmaeus may consume greater amounts of tougher and/or more obdurate foods than P. abelii, and that consumption of such foods may intensify amongst Bornean orangutan populations. Finally, data from this study are used to evaluate variation in craniomandibular morphology in Khoratpithecus piriyai, possibly the earliest relative of Pongo from the late Miocene of Thailand, and the late Pleistocene Hoa Binh subfossil orangutan recovered from Vietnam. With the exception of a relatively thicker M(3) mandibular corpus, K. piriyai has jaw proportions that would be expected for an extant orangutan of comparable jaw size. Likewise, the Hoa Binh subfossil does not differ in skull proportions from extant Pongo, independent of the effects of increase in jaw size. These results indicate that differences in skull and mandibular proportions between these fossil and subfossil orangutans and extant Pongo are allometric. Furthermore, the ability of K. piriyai to resist jaw loads appears to have been comparable to that of extant orangutans. However, the similarity in jaw proportions between P. abelii and K. piriyai suggest the latter may have been dietarily more similar to Sumatran orangutans.     

Social behavior of captive,group-living Orangutans

The behavior of orang-utans (Pongo pygmaeus)was observed in two captive groups (one adult group, one juvenile group). Activity profiles,animal interactions, and compartmental spatial use for both adult-group and juvenile-group individuals were recorded over a 9-month period. Behavioral repertoires for both groups included large amounts of social activity. Equivalent amounts of social activity were found for each group. The social behavior of juvenile animals involved more active behavior such as play. The social behavior of the adult animals was more subtle, involving social monitoring and allogrooming. These results indicate that orangutans, at least when group-living in captivity, exhibit the potential to display social behavior which is apparently of greater frequency and complexity than that which has been observed in the wild. These findings suggest that the solitary behavior of wild orangutans is not a necessary characteristic of orangutan behavior. Under different environmental conditions orangutans appear to readily adapt socially, and, like other nonhuman primates,they have the capacity to exhibit complex and subtle social behavior. This report is based on part of a senior thesis submitted by Sara D. Edwards     

Culture and geographic variation in orangutan behavior

Although geographic variation in an organism's traits is often seen as a consequence of selection on locally adaptive genotypes accompanied by canalized development [1], developmental plasticity may also play a role [2, 3], especially in behavior [4]. Behavioral plasticity includes both individual learning and social learning of local innovations ("culture"). Cultural plasticity is the undisputed and dominant explanation for geographic variation in human behavior. It has recently also been suggested to hold for various primates and birds [5], but this proposition has been met with widespread skepticism [6-8]. Here, we analyze parallel long-term studies documenting extensive geographic variation in behavioral ecology, social organization, and putative culture of orangutans [9] (genus Pongo). We show that genetic differences among orangutan populations explain only very little of the geographic variation in behavior, whereas environmental differences explain much more, highlighting the importance of developmental plasticity. Moreover, variation in putative cultural variants is explained by neither genetic nor environmental differences, corroborating the cultural interpretation. Thus, individual and cultural plasticity provide a plausible pathway toward local adaptation in long-lived organisms such as great apes and formed the evolutionary foundation upon which human culture was built.     

Human–Ape Interactions in a Zoo Setting: Gorillas and Orangutans Modify Their Behavior Depending upon Human Familiarity

Understanding how human presence influences animal behavior, specifically the behavior of nonhuman primates, has important implications for methodology in cognitive and behavioral studies, for our understanding of human–animal relationships and for animal welfare in captive settings. Conducted in the San Diego Zoo, this study partially replicates an existing study on human–animal relationships, which focused on familiarity effects on the human-directed behavior of great apes residing in the Toronto Zoo. Such a replication in a new location and with different individuals is necessary to expand sample size and to better understand how ontogeny and living environment influence human-directed ape behavior. All-occurrence sampling of human-directed behavior was used to gather data on two gorilla groups and one orangutan group, all housed at the San Diego Zoo. The aim was to compare ape-initiated behaviors toward zoo staff with apeinitiated visitor-directed behavior, in accordance with predictions of the Human–Animal Relationship (HAR) model. Overall, human-directed behaviors were more frequent toward visitors than toward staff, mainly caused by increased visitor-directed visual behavior, specifically brief glances. Given that visual monitoring has been seen as fearful behavior, potentially related to predator monitoring, this would confirm the expectation that lack of familiarity will lead to increased visual vigilance. However, the visitor-directed visual behaviors may not be antagonistic or fearful. Considering the specific behaviors and exhibit designs, curiosity may be an equally likely explanation in this context. Aiming to also understand whether these groups exhibited species differences in human-directed behavior, it was found that orangutans engaged in more affiliative behavior overall than gorillas. Comparing our results with the previous study, we conclude that while effects of familiarity are present, those effects are modulated by both individual ontogeny and exhibit design. While the HAR model is partially supported, additional factors may need to be included to fully interpret the observed behavior. Additional research is needed to further understand the effects of species, sex, and ontogeny on the predictions of the HAR model.     

Yawning: Relation to Sleeping and Stretching in Humans

The temporal relations among yawning, sleeping, and stretching were investigated by having undergraduate college students record the occurrences of these behaviors during a one-week period. Yawning was most frequent during the hour before sleeping and after waking. In contrast, stretching was common only during the hour after waking. Concurrent yawning and stretching were common but stretching was accompanied more often by yawning than vice-versa. The temporal proximity of yawning to sleep and waking times is probably the basis for yawning as a paralinguistic signal for drowsiness. The role of contagious yawning in synchronizing the behavior and physiological state of a group is considered.     

Nonaggressive interventions by third parties in conflicts among captive Bornean orangutans (<Emphasis Type="Italic">Pongo pygmaeus</Emphasis>)

Whereas orangutans are regarded as semisolitary animals in the wild, several studies have reported frequent social interactions, including aggression, among orangutans in captivity. As yet, there is a lack of knowledge about how they cope with aggression. In this report, we provide a number of new observations of interventions by third parties in aggressive interactions within a captive group of Bornean orangutans (Pongo pygmaeus) in the Tama Zoological Park, Japan. We observed that an adult female and a juvenile male orangutan intervened in aggressive interactions. The victim was a newly introduced juvenile female who was unrelated to anyone in the zoo. The ways in which the orangutans intervened were not aggressive, as the interveners simply aimed to separate the opponents, and these interventions did not lead to further aggression in almost every case. Our observations suggest that third parties can play an important role in managing aggressive conflicts among captive orangutans and, under conditions in which orangutans share limited space, nonaggressive interventions by third parties for settling conflicts appear. It is possible that orangutans may actively promote the peaceful coexistence of other individuals.     

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

To understand the development and evolution of cognition of our closest relatives, we need to investigate their learning behavior during every-day life. This study finds that wild orangutan males and females differ in their social learning strategies and subsequent learning outcomes from an early age, underlining the general importance of, and the effects of sex on, social learning in non-human great apes.