When is a yawn just a yawn? When is a yawn more than a yawn? Contagious yawning - the increase in likelihood that you will yawn after watching or hearing someone else yawn - has been of particular interest to researchers in fields as varied as primatology, developmental psychology, and psychopathology.

At first, scientists thought that yawning was a mechanism designed to keep the brain cool. However, it turns out that there is a correlation between the susceptibility for contagious yawning and self-reported empathy. Humans who performed better at theory of mind tasks (a cognitive building block required for empathy) also yawn contagiously more often (PDF). And two conditions that have been associated with poorer performance on theory of mind tasks are also associated with reduced or absent contagious yawning: schizotypy and autism.

In 2008, psychologist Ramiro Joly-Mascheroni and colleagues from the University of London showed, for the first time, that human yawns are contagious for domestic dogs. Dogs' unique social skills in interacting with humans is probably the result of selection pressures during the domestication process. Therefore, they reasoned, it is possible that as a result of that process, dogs may have developed the capacity of empathy towards humans. And if so, it is further possible that they may yawn when they see and hear humans yawn.

In one condition, the experimenter, who was a stranger to the dogs, attracted the dogs' attention and then initiated a genuine yawn. The yawn was repeated for five minutes after re-establishing eye contact with the dog, which meant that the number of yawns varied between ten and nineteen per individual. In the control condition, the experimenter displayed a fake yawn, which mimicked the mouth opening and closing actions, but not the vocalization or other subtle muscular changes.

The yawning condition made 21 out of 29 dogs, seventy-two percent, yawn in response. None of the dogs yawned in the control condition. Amazingly, this is even higher than rates of contagious yawning that have been reported for humans, which range from 45-60%. With this experiment, membership in the group of species that exhibit contagious yawning became slightly less exclusive: dogs were added to a small list that had contained humans, chimpanzees, stumptail macaques, and gelada baboons. Despite this new evidence, however, there was still no consensus on the function of contagious yawning. Even if correlated with empathy, why would empathy lead to yawning?

Chimps Yawn When Their Friends Yawn

Then, in 2011, Matthew Campbell and Frans de Waal of Yerkes National Primate Research Center at Emory University proposed a more nuanced view of contagious yawning. They wondered if social group membership could affect the transmission of a contagious yawn. After all, if empathy is indeed the thing underlying contagious yawning, then contagious yawning should show many of the same behavioral signatures that empathy itself does. For example, it is known that certain parts of the brain (the anterior cingulate and the anterior insula) activate both when people experience pain as well as when another person experiences pain (other parts of the brain only activate in response to personal pain, not to others' pain). From this data, researchers suggested that humans are able to share the emotional aspects of pain, but not the physical aspects of pain, with others. This, of course, is the basis for empathy.

And additional fMRI studies have further refined these findings: activity in the anterior cingulate is greater in response to watching an in-group member experience pain than in response to the pain of an out-group member. So if contagious yawning reflects empathy, and empathy varies on the basis of social status, then it is possible that contagious yawning will vary on the basis of social status as well.

Since chimpanzees are highly territorial and overtly aggressive towards other groups, it is certain that members of the same social group are considered part of the in-group, and strangers are automatically outsiders.

Campbell and de Waal recorded videos of chimpanzees while they were yawning to use as experimental stimuli. The videos were edited down to just nine seconds each and were shown to the chimps on an iPod touch. It was expected that they would yawn more when shown videos of group members yawning than when shown videos of strangers yawning. They were also shown videos of chimpanzees doing other things, as a control condition. In this video, Tara, an adult female, yawns while watching a video of another chimp from her social group yawning on the iPod touch.

The chimpanzees did yawn more often after watching videos of a familiar chimp yawning compared with the videos of ingroup members doing other things. Consistent with the researchers' expectations, they yawned more after watching a familiar chimp yawning than after watching an unfamiliar chimp yawning. And there were no gender differences: males yawned in response to ingroup yawn videos as often as the females did. Importantly, these results could not have been due to differences in attention, since the chimps actually paid more attention when viewing videos of unfamiliar chimpanzees than familiar ones.

Taken together, this provided strong evidence that empathy indeed underlies contagious yawning, and that contagious yawning is dependent on social group membership. Given that, it is therefore unclear why humans do yawn after watching strangers or outgroup members yawn. Since all members of a chimpanzee community know eachother, not only are they members of the same group, but they are all familiar with eachother.

Campbell and de Waal speculated that humans, at some point in our evolution, may have evolved the ability to consider strangers, despite their unfamiliarity, as ingroup members. If this was the case, then strangers would not automatically be considered outgroup members, as they are with chimpanzees.

Conflicting Results

In order to serve as successful pets, domesticated dogs must also be able to comfortably interact with human strangers as well as with other dogs. It is possible that the selection process of domestication has allowed dogs the possibility of dissociating familiarity from group membership, as have humans. After all, in the Joly-Mascheroni study, seventy-two percent of dogs tested yawned after watching an unfamiliar human yawn.

However, a 2009 study by Aimee Harr and colleagues was unable to replicate Joly-Mascheroni's findings, and a 2010 study by Sean O’Hara and Amy Reeve found only weak evidence for contagious yawning in dogs - considerably more limited than suggested by Joly-Mascheroni. The O'Hara and Reeve study was the first explicit attempt to assess whether contagious yawning in dogs might have a basis in empathy. To the extent that dogs did display the yawn contagion, they found no evidence that dogs would be more likely to yawn in response to familiar, rather than unfamiliar, humans.

Taking stock of the extant literature on contagious yawning, Jennifer Yoon of Stanford University and Claudio Tennie from the Max Planck Institute for Evolutionary Anthropology argued in a theoretical paper that if cross-species contagious yawning does exist between dogs and humans, then it may not necessarily be necessarily related to empathy, per se. In animal cognition research, it is usually prudent to explain animal behavior in accordance with the lowest-level cognitive processes possible.

It is possible, they wrote, that contagious yawning could be explained more simply by non-conscious mimicry, or the "chameleon effect." This is a well-documented phenomenon in humans, and refers to the tendency of an individual to unintentionally imitate a social partner's behaviors. If contagious yawning is the result of non-conscious mimicry, then it could be explained by the desire to bond with a social partner. This sort of mimicry has been shown experimentally to increase subjective liking among two individuals.

An even simpler explanation is that that contagious yawning is the result of a releasing mechanism - in other words, seeing someone yawn flips the yawning-switch in the brain, and that makes you yawn. This is called a fixed action pattern. And the input required to flip that switch may be much less elaborate that actually watching someone yawn. "In humans," Yoon and Tennie note, "yawns are triggered just as frequently by a video of another person yawning as after reading written descriptions of yawning."

Searching For Empathy

The latest salvo in the epidemic of contagious yawning studies comes in a paper published last week in the journal Animal Cognition by Karine Silva and colleagues from the Universidade do Porto in Portugal. Taking a cue from Yoon and Tennie, Silva conducted an experiment that was designed to determine which was the better explanation for human-dog contagious yawning: empathy, non-conscious mimicry, or fixed action patterns.

Twenty-nine dogs were played audio recordings of familiar yawns (recorded by their owners) and unfamiliar yawns (recorded by an experimenter). The researchers also reversed each of those sounds to create control sounds. In this way, the control sounds were identical to the yawns in terms of variables like amplitude and frequency content, but were perceptually different, and did not sound like yawns. Altogether, each dog heard each of the four different types of audio recordings. Critically, the individual who provided the audio recording of the familiar yawn was not in the room with the dog during testing.

The first finding was that dogs yawned more frequently in response to either type of yawn (familiar or unfamiliar) than after hearing control sounds. More importantly, hearing familiar yawns resulted in significantly more yawn than the sounds of unfamiliar yawns, just like in chimpanzees! In fact, the dogs were four times more likely to yawn after hearing the familiar yawn than the unfamiliar yawn. Minimally, this evidence rejects the simplest explanation for contagious yawning: the fixed action pattern. Since contagious yawning in dogs is modulated by a social variable, it necessarily requires more complex cognitive mechanisms than simple imitation.

A Methodological Mess

Still, it is unclear whether human-dog contagious yawning is the result of a complex process like empathy or a simpler process like social mimicry. Differences in experimental methodologies makes it particularly hard to make much sense of the differing findings. O'Hara and Reeve found no evidence for a social bias in contagious yawning, but they used video recordings of human yawns, not just the audio recordings, as Silva did.

In an attempt to reconcile the two findings, Silva writes, "It is known that dogs can actively generate an internal representation of the owner’s face when they hear the owner’s voice. Therefore, if one considers that it may be the perceptual image of yawn that triggers yawning, then the explanation for the social bias observed here could be differences in the capacity to form mental representations from familiar and unfamiliar auditory input." In other words, the social bias seen in Silva's study could be an artifact, or an accidental outcome of the particular methodology used. If it is actually the visual representation of a yawn that triggers the contagious yawn, then dogs could be more likely to yawn when hearing a familiar human yawn simply because it is easier for them to create a mental image of their owner than a stranger.

"Clearly," Silva concludes, as most scientists do at the end of their papers, "there is a need for future research to focus on the key variables in the presentation of yawns, as this will facilitate comparisons across studies." If contagious yawning in dogs is indeed related to empathy, then it could be a useful tool for selecting dogs to use in service-related activities, such as animal-assisted therapy. In addition, a more coherent explanation for contagious yawning could also help to explain why some dogs do not have contagious yawning. Understanding why some dogs lack contagious yawning could possibly serve as a model for better understanding human disorders that are associated with reduced contagious yawning. But scientists won't be able to move forward until there are increased efforts towards replicating the methods rather than just the findings. This is especially the case for cross-species comparisons. For research in contagious yawning to move forward effectively, the methodology must be contagious as well.

Joly-Mascheroni, R., Senju, A., & Shepherd, A. (2008). Dogs catch human yawns Biology Letters, 4 (5), 446-448. DOI: 10.1098/rsbl.2008.0333

Matthew W. Campbell, & Frans B. M. de Waal (2011). Ingroup-Outgroup Bias in Contagious Yawning by Chimpanzees Supports Link to Empathy PLoS ONE, 6 (4) : 10.1371/journal.pone.0018283

Harr, A., Gilbert, V., & Phillips, K. (2009). Do dogs (Canis familiaris) show contagious yawning? Animal Cognition, 12 (6), 833-837 DOI: 10.1007/s10071-009-0233-0

O’Hara, S., & Reeve, A. (2011). A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris Animal Behaviour, 81 (1), 335-340 DOI: 10.1016/j.anbehav.2010.11.005

Yoon, J., & Tennie, C. (2010). Contagious yawning: a reflection of empathy, mimicry, or contagion? Animal Behaviour, 79 (5) DOI: 10.1016/j.anbehav.2010.02.011

Silva, K., Bessa, J., & de Sousa, L. (2012). Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation Animal Cognition DOI: 10.1007/s10071-012-0473-2

Chimp yawn via Flickr/Pelican; Baby yawning via Flickr/fumanch00. Dog photo copyright the author.