ABSTRACT: Six adult female
chimpanzees were shown video scenes of
chimpanzees repeatedly yawning or of chimpanzees
showing open-mouth facial expressions that were
not yawns. Two out of the six females showed
significantly higher frequencies of yawning in
response to yawn videos; no chimpanzees showed
the inverse. Three infant chimpanzees that
accompanied their mothers did not yawn at all.
These data are highly reminiscent of the
contagious yawning effects reported for humans.
Contagious yawning is thought to be based on the
capacity for empathy. Contagious yawning in
chimpanzees provides further evidence that these
apes may possess advanced self-awareness and
empathic abilities.
Experimental evidence supports the common
observation that seeing other people yawn can
induce yawning (Provine 1986, 1989; Platek et
al. 2003). Studies have shown that between 42%
and 55% of human adults will yawn during, or
shortly after, seeing a videotape of repeated
yawns of other humans. The only systematic study
to our knowledge of children, however, found
that children aged younger than 5 years do not
show this contagious yawning effect (Anderson
& Meno 2003).
Although yawning is widespread among
vertebrate species, contagious yawning has been
reported only in humans (Lehmann 1979;
Baenninger 1987; Smith 1999). It has been
suggested that contagious yawning reflects a
basic capacity for empathy (Lehmann 1979), and a
recent study linked human individual differences
in susceptibility to contagious yawning to
differences in empathic tendencies,
self-recognition ability and theory of mind
(Platek et al. 2003). We assessed whether
chimpanzeesÑhumans' nearest phylogenetic
neighboursÑare prone to contagious
yawning when exposed to videotapes showing
yawning of conspecifics. Evidence of contagious
yawning would provide further evidence of
similarities in the evolution of selfand
other-awareness between great apes and
humans.
A yawn response during presentation
of a yawn videotape. Ai watches a yawn on the
screen (top left), starts to yawn as the
stimulus yawn ends (top right), continues to
yawn (bottom left), and completes the yawn while
the screen is blank (bottom right) See
the video
MATERIAL AND METHODS
(a) Subjects :We
tested six socially reared, group-living adult
female chimpanzees (Pan troglodytes) living at
the Primate Research Institute of Kyoto
University. They were individually invited to
leave their outdoor enclosure and enter a
familiar test booth; three of them brought their
3-year-old dependent infants with them. The
chimpanzees had extensive experience with
experiments on learning and cognition (Matsuzawa
1985, 2003; Kawai & Matsuzawa 2000; Morimura
& Matsuzawa 2001), but none had previously
observed video stimuli of the type used here.
This experimental work complied with the Guide
for the Care and Use of Laboratory Primates,
Primate Research Institute, Kyoto
University.
(b) Experimental apparatus
:We prepared two 'yawn' and two
'open-mouthed' videotapes. Yawn videos contained
10 naturally occurring yawns by chimpanzees,
each separated by 6Ð10 s of a blue, blank
screen (see figure 1 or an example).
Open-mouthed videos were equated for total
duration, and showed chimpanzees displaying
eight or ten openmouthed faces but not yawning
(for example, while pant-hooting or
grinning), again separated by a blank
screen. The videos displayed chimpanzees in
various postures and orientations, the most
salient feature being the yawns or open-mouthed
expressions. One yawn video presented yawns by
familiar chimpanzees from the subjects' own
group, and the other presented yawns by
unfamiliar chimpanzees in the wild. The videos
were shown silently on a 35 cm monitor
(Panasonic TH-14RF2) positioned on a small table
30 cm high and ca. 8 cm from the front of the
glass-walled booth.
(c) Experimental procedure
:Two videotapes were shown in
each session. Five minutes after the chimpanzee
entered the booth, the monitor was switched on
and the first video ran until completion of the
last yawn or open-mouth (3 min). The monitor was
then switched off and the chimpanzee was
observed for 3 min. A 5-min distraction period
then followed, after which the second video was
shown (3 min), followed by another 3- min
observation period. Each chimpanzee was tested
during four sessions, with the following order
of video combinations presented in each session:
(i) familiar yawn, unfamiliar open-mouth; (ii)
unfamiliar open-mouth, familiar yawn; (iii)
familiar open-mouth, unfamiliar yawn; (iv)
unfamiliar yawn, familiar open-mouth. All
sessions were videotaped through the glass walls
of the booth, using three fixedposition cameras,
two of which were operated manually. The three
authors were present but remained passive
throughout, except that T.M. occasionally
encouraged the chimpanzee to watch the monitor
if her attention appeared to wane. All yawns by
the subject chimpanzees were scored in real time
and then verified by subsequent video analysis;
agreement between the three authors was
100%.
RESULTS
The adult chimpanzees yawned, on average,
4.7 times during and after the open-mouth
videos, and this rose to 10 yawns during and
after the yawn videos. The data were analysed
both at the group level and individual level.
There were no significant effects at group
level, as assessed by
paired t-tests. However, two chimpanzees
(Ai, Mari) showed significantly higher
frequencies of yawning during or shortly after
exposure to yawn videos (totals: 24 and 25) than
to open-mouth videos (2 and 9; both p 0.01,
binomial tests). Figure 1 shows a chimpanzee
yawning during
exposure to a yawn video, and figure 2
presents the data for all of the adult
chimpanzees. Social familiarity of the
chimpanzees in the videos did not affect yawning
frequency. No chimpanzee showed significantly
more yawning in response to the open-mouth
videos, and open-mouth videos did not elicit
facial expressions. None of the three infant
chimpanzees yawned at any time during the
tests.
DISCUSSION
Higher frequencies of yawning in response to
yawn stimuli compared with the open-mouth
control stimuli indicate a contagion effect in
33% of the adult chimpanzees. This percentage is
only slightly lower than the percentages
reported for adult humans exposed to visual
yawn stimuli (Provine 1986; Platek et al.
2003). It can be argued that the percentage of
chimpanzees showing contagious yawning is even
more impressive, given that adult human
participants are usually aware of the phenomenon
being studied, and simply thinking about yawning
may induce yawns (Provine 1989). The chimpanzees
had no knowledge of what the experimenters were
interested in, and had no idea of what was
expected of them. Unlike Old World monkeys
(Deputte 1994), chimpanzees do not appear to
show a sex difference in their frequency of
yawning. None of the infant chimpanzees that
accompanied their mothers showed any yawning,
even though they watched the videos and saw
their mothers yawning. This absence of
contagious yawning in infant chimpanzees recalls
the absence of contagious yawning in human
toddlers reported by Anderson & Meno (2003).
Further work on the young chimpanzees will
clarify the extent to which contagious yawning
in chimpanzees resembles the same behaviour in
humans. Chimpanzees display self-recognition in
mirrors (Gallup 1970; Povinelli et al. 1997), a
sign of objective self-awareness that has been
linked with the capacity for empathy (Gallup
1982). Monkeys do not show self-recognition
(Anderson 1994), and observations of social
behaviour reveal much more convincing evidence
of empathy in chimpanzees than in monkeys (de
Waal 1996). Observational studies of spontaneous
yawning in monkeys indicate that it is not
contagious (Baenninger 1987; Deputte 1994).
Given the distribution of self-recognition and
social cognitive abilities among primates, we
predict that susceptibility to contagious
yawning will be found in other great apes, but
not monkeys, and that individual differences in
susceptibility to contagious yawning may be
related to differences in self-recognition and
empathy.
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