Yawning is a curious behavioural phenomenon
that at times may be described as 'contagious',
appearing to spread from one individual to
another. Contagious yawning is seen in several
primate species, including humans (Provine 1986;
Baenninger 1997; Campbell et al. 2009; Palagi et
al. 2009). Here we argue that contagious
yawning, particularly the newly documented
phenomenon of cross-species contagious yawning
(Joly- Mascheroni et al. 2008), is an important
avenue of research. In the discussion that
follows, we hope to encourage further
experimentation to identify the possible
functions of and mechanisms underlying
contagious yawning.
Yawning has several convenient properties
that make it ideal for cross-species research.
First, it is already in the behavioural
repertoire of a broad spectrum of vertebrates,
from fish to birds to mammals (Baenninger 1997;
Gallup et al. 2009). Thus, cross-species
comparisons do not hinge on complex and
error-prone training protocols. Because it
occurs spontaneously at low frequency,
crossindividual yawning in a temporally
correlated but asynchronous way is easy to
detect and difficult to explain as chance. Our
principal interest in cross-species contagious
yawning is its potential link with social
cognitive capacities. As described in a recent
report by Joly-Mascheroni et al. (2008), 21 of
29 pet dogs, Canis familiaris, tested yawned
after seeing human yawns while none yawned after
seeing silent mouth openings. A prominently
raised hypothesis in Joly-Mascheroni et al.
(2008, page 447) is that 'contagious yawning of
dogs may relate to their capacity for empathy'.
This intriguing hypothesis is also proposed in
findings of contagious yawning in nonhuman
primates (Palagi et al. 2009) and as explaining
the relative lack of contagious yawning in
autistic children (Senju et al. 2007). Empathy
is notoriously difficult to define (Preston
& de Waal 2002).
While empathy is not defined in
Joly-Mascheroni et al. or Palagi et al., and can
be construed in many ways, a related letter
(Senju et al. 2007) cites two references that
both offer high-level definitions for the term.
One refers to empathy as 'the capacity to
predict and to respond to the behavior of agents
(.) by inferring their mental states'
(Baron-Cohen et al. 2005, page 819), and the
other refers to contagious yawning as 'a
consequence of a theory of mind' (Platek et al.
2003, page 233), a representational system for
mental state attribution and reasoning. Yet,
contagious yawning may be related to empathy in
the 'theory of mind' sense only in that they
co-occur; one may simply be a good predictor of
the other. The relationship may also be causal,
with the representational capacities thought to
comprise 'theory of mind' (e.g. conceiving of
humans as agents with mental states, capacity
for false beliefs, etc.) being necessary in some
way for an individual to 'catch' yawns. Here, we
consider two more parsimonious accounts that do
not imply empathy in the 'theory of mind' sense:
nonconscious mimicry and contagion. We further
discuss empirical predictions that distinguish
these alternatives from one another. Thus, we
are in step with empirically based projects to
distinguish empathy from related but distinct
behaviours that may be considered by some to be
part of a broader unified phenomenon (see
'perception action model', Preston & de Waal
2002).
Nonconscious mimicry ('chameleon effect') is
well documented in humans and refers to an
individual's tendency to imitate a social
partner's behaviours without either party's
awareness or intent (Chartrand & Bargh
1999). Chartrand and colleagues have shown
nonconscious mimicry in humans is modulated by
specific social motivations including the desire
to affiliate or bond with the mimicker's social
partner. Conversely, nonconscious mimicry can
also increase liking and a sense of interaction
smoothness on the part of the mimicked
individual (e.g. Lakin & Chartrand 2003). A
cross-species chameleon effect was recently
demonstrated by Paukner et al. (2009), who
showed that capuchin monkeys, Cebus apella,
affiliated more with humans who had previously
mimicked their behaviours. Finding cross-species
chameleon effects like these has important
implications for animal cognition research. For
example, dogehuman nonconscious mimicry may have
important implications for understanding canine
domestication. If dogs' tendency to catch human
yawns is driven by dogs' underlying desire to
affiliate with humans, then perhaps an
affiliative motivation facilitated early
humanecanid interactions. If, furthermore, dogs'
tendency to engage in nonconscious mimicry
increased their affective or social value to
humans, we can speculate that early humans might
have promoted this trait through selective
breeding. Together, the effects of nonconscious
mimicry throughout canine domestication may have
contributed not only to modern dogs' tendency to
attend to and look at humans more than do
humanreared wolves, Canis lupus (Miklósi
et al. 2003) but also to their remarkable skill
in interpreting human social cues (Hare &
Tomasello 2005).
Apart from nonconscious mimicry, an even
lower-level mechanism underlying contagious
yawning is entirely possible. Referring to the
spread of yawning from one individual to another
as 'contagious' has an everyday meaning but also
a specialized meaning in the animal cognition
literature. 'Contagion' describes a short-term
spread of a behaviour (Thorpe 1963) in which a
special stimulus 'serves as a releaser to the
unlearned behaviour of others' (Zentall 2001).
According to the contagion hypothesis,
therefore, contagious yawning could be built
upon a specific behavioural fixed action pattern
(see Provine 1986) that is hard-wired and simply
needs a certain releasing stimulus (Tinbergen
1951). This releasing stimulus may be much less
elaborate than the full live-action yawning
event included in the Joly-Mascheroni et al.
procedure (e.g. mere sounds of a yawn). Control
experiments with more minimal yawning cues can
help to address these possibilities and may
yield different results for different species.
For example, in a recent experiment in which
dogs were shown silent videotaped yawns, the
vast majority of dogs did not show contagious
yawning (Harr et al. 2009).
In contrast, in chimpanzees, Pan
troglodytes, contagious yawning generalizes from
videos of real conspecifics to 'cartoonized'
computer animated conspecifics (Campbell et al.
2009). In humans, yawns are triggered just as
frequently by a video of another person yawning
as after reading written descriptions of yawning
(Provine 1986). Recently, data on contagious
yawning in gelada baboons, Theropithecus gelada,
seemingly refuted the contagion hypothesis,
since 'emotional proximity' rather than 'spatial
proximity' lead to contagious yawns (Palagi et
al. 2009); however, in our reading it could
equally have been the case that observer baboons
merely paid closer attention to those subjects
that were their affiliates. Thus, attention
differences (cf. Preston & de Waal 2002)
with subsequent differences in levels of
contagion, rather than empathy differences,
could have been responsible for the yawning
pattern observed.
We can empirically distinguish between the
nonconscious mimicry and contagion hypotheses of
contagious yawning. For example, the 'contagion
only' hypothesis predicts that the range of
possible contagious behaviours between
individuals should be limited to a small number
of unlearned behaviours. Also, we should be able
to identify the releasing stimulus that triggers
a contagious behaviour, like a yawn (or the
sound of it), and to show that an isolated
presentation of this stimulus is sufficient to
induce yawning in an encapsulated way that is
unmodulated by social contextual factors.
In its strong form, the nonconscious mimicry
hypothesis predicts that individuals mimic a
greater array of behavioural mannerisms. This
prediction can be tested in Joly-Mascheroni et
al.'s existing data set if both yawning and
nonyawning mouth movements are coded. In the
yawning condition, dogs' nonconscious mimicry
would take the form of yawning as measured and
reported by the authors. In the control
condition, the human experimenter silently and
repeatedly opened his mouth. Nonconscious
mimicry predicts that dogs would display more
nonyawning mouth movements in the control
condition than in the experimental condition.
This prediction is also somewhat supported by
Palagi et al.'s results, where female baboons
were found to mimic yawning mannerisms (e.g.
yawning with covered teeth, with uncovered teeth
and with uncovered gums) depending on the manner
of the first yawn.
Further predictions of the nonconscious
mimicry hypothesis include modulation of
nonconscious mimicry in a social context and
affiliation goal, and consequences for perceived
interaction quality and interindividual
valuation ('liking'). To test for these latter
predictions one could design interactions that
modulate an individual's motives to affiliate
with a social partner (competition/cooperation,
reward/punishment), then look for modulation in
their mimicking of incidental behaviours. If the
social partner is human, as in Joly-Mascheroni
et al. (2008) and Campbell et al. (2009), one
could also assess modulation in humans' liking
of the nonhuman partner and perception of
interaction smoothness. That contagious yawning
in monkeys was more frequent between highly
affiliated individuals that frequently groomed
each other further supports the nonconscious
mimicry hypothesis (Palagi et al. 2009; but see
also above for an alternative explanation). We
hope that laying out predictions made by the
contagion and nonconscious mimicry hypotheses
will guide future work to determine which of
these (or other) hypotheses best explains this
intriguing phenomenon of cross-species yawning
in a variety of vertebrate animals.
References
Baron-Cohen, S., Knickmeyer, R. C. &
Belmonte, M. K. 2005. Sex differences in the
brain: implications for explaining autism.
Science, 310, 819-823.
Baenninger,
R. 1997. On yawning and its functions.
Psychonomic Bulletin and Review, 4,
198-207.
Campbell,
M. W., Carter, J. D., Proctor, D.,
Eisenberg, M. L. & de Waal, F. B. M.
2009. Computer animations stimulate
contagious yawning in chimpanzees.
Proceedings of the Royal Society B, 276,
4255-4259,
Chartrand, T. L. & Bargh, J. A. 1999.
The chameleon effect: the perceptione
behavior
link and social interaction. Journal of
Personality and Social Psychology, 76,
893-910.
