Chimpanzees
empathize with group mates and humans, but not
with baboons or unfamiliar
chimpanzees
Matthew Campbell, Frans de Waal
Human empathy can extend to strangers and
even other species, but it is unknown whether
non-humans are similarly broad in their empathic
responses. We explored the breadth and
flexibility of empathy in chimpanzees, a close
relative of humans. We used contagious yawning
to measure involuntary empathy and showed
chimpanzees videos of familiar humans,
unfamiliar humans and gelada baboons (an
unfamiliar species). We tested whether each
class of stimuli elicited contagion by comparing
the effect of yawn and control videos. After
including previous data on the response to
ingroup and outgroup chimpanzees, we found that
familiar and unfamiliar humans elicited
contagion equal to that of ingroup chimpanzees.
Gelada baboons did not elicit contagion, and the
response to them was equal to that of outgroup
chimpanzees. However, the chimpanzees watched
the outgroup chimpanzee videos more than any
other. The combination of high interest and low
contagion may stem from hostility towards
unfamiliar chimpanzees, which may interfere with
an empathic response. Overall, chimpanzees
showed flexibility in that they formed an
empathic connection with a different species,
including unknown members of that species. These
results imply that human empathic flexibility is
shared with related species.
-Campbell M et
al. Computer animations stimulate contagious
yawning in chimpanzees
Proceed Royal Soc Biol
2009:276(1676):4255-4259
-Campbell
MW, de Waal F. Ingroup-Outgroup Bias in
Contagious Yawning by Chimpanzees Supports Link
to Empathy. Plos One. 2011;6(4):1-4
-Campbell
M, de Waal F. Methodological Problems in the
Study of Contagious Yawning; In Walusinski O
(ed): The Mystery of Yawning in Physiology and
Disease. Front Neurol Neurosci. Basel, Karger,
2010, vol 28, pp 120&endash;127
-Campbell M,
de Waal F. Chimpanzees empathize with group
mates and humans, but not with baboons or
unfamiliar chimpanzees. Proc. R. Soc. B 281:
20140013
The concept of empathy is increasingly
applied to explain animal sensitivity to the
emotional states of others. Without necessarily
implying the cognitively advanced forms found in
human adults (e.g. theory of mind), it takes as
its basis bodily connections and involuntary
mimicry, also known as the perception&endash;
action core of empathic processing
[1].There are now studies of empathy in
mammals, from mice (Mus musculus) [2],
rats (Rattus norvegicus) [3] and dogs
(Canis lupus familiaris) [4] to
elephants (Loxodonta africana) [5], and
also in birds [6,7].
One common behavioural measure is
contagious yawning (CY), which appears to
fit the empathy framework because of four key
findings: (i) human adults high on other
measures of empathy show more CY [8];
(ii) humans with developmental and personality
disorders in which empathy is impaired show
diminished CY [8&endash;11]; (iii) CY is
positively biased by familiarity in humans (Homo
sapiens) [12], chimpanzees (Pan
troglodytes) [13], bonobos (Pan
paniscus) [14], gelada baboons
(Theropithecus gelada) [15] and dogs
[16&endash;18], as is typical of other
measures of empathy; and (iv) presented with a
variety of body movements apes exclusively
increase yawning in response to observed
yawning, suggesting CY's high specificity
[19,20].
Aiding this specificity, brain areas
associated with the human mirror neuron system
activate in humans viewing yawns
[21&endash;23], withmirror neurons
having been implied as a proximate neural
mechanism for empathy [24,25]. Thus, CY
fits better with an empathy framework than with
explanations in terms of imitation or
behavioural facilitation. Human empathic
functioning, although biased towards similar and
familiar individuals, is flexible enough to
include empathy for strangers and even other
species [26&endash;28]. Is an empathy
response flexible enough to include strangers
uniquely human, related to our well-developed
capacity to cooperate with outsiders
[29]? Empirical studies with non-humans
show both the importance of familiarity in
forming empathic connections and potential for
moving beyond it. Mice showed heightened pain
responses after viewing cage-mates in pain, but
not after viewing strangers in pain [2].
Chimpanzees made a similar distinction, showing
CY in response to familiar individuals but not
unfamiliar individuals [13]. Rats,
however, would help unfamiliar individuals, but
only if the strain of rat was familiar
[30]. Domestic dogs show empathy-related
responses to unfamiliar humans [4,17,31]
(although there are conflicting results with CY
[32,33]), but with this species it is
unclear whether this ability stems from natural
or artificial selection. Young orphaned
chimpanzees showed a CY response to an
unfamiliar human [20], but positive
interactions between the two may have influenced
the response. A similar population of
chimpanzees also showed helping behaviour
towards an unfamiliar human [34].
When combined with anecdotes of
inter-species helping behaviour [35], a
pattern emerges that non-humans may indeed share
some of the human's empathic flexibility. To
explore the origins of flexible empathy in
humans, we studied the responses of one of our
closest living relatives, the chimpanzee, in
which CY is well established
[13,19,20,36&endash;38]. Chimpanzees
live in fission&endash;fusion communities, which
often compete [39,40]. Female migration
at sexual maturity is the only movement of
individuals between groups. In chimpanzee
society, all known individuals are members of
the community, and unknown individuals belong
per definition to a different community. Using
the contagiousness of yawning as a measure of
involuntary body synchronization and empathy, we
previously showed an ingroup&endash;outgroup
bias: chimpanzees were affected by the yawns of
known individuals, but not unknown individuals
of their species [13].
However, having an existing positive
relationship with an individual is not a
prerequisite for contagion, as chimpanzees have
also shown CY in response to computer-generated
animations [37]. Is motor mirroring in
chimpanzees flexible enough to induce yawns in
response to species different from themselves?
And would chimpanzees distinguish between known
and unknown individuals from other species?
Captive-reared chimpanzees interact daily with
humans, so we wanted to know whether chimpanzees
would express an empathic connection with humans
in CY. However, chimpanzees may respond to known
and unknown humans differently.
The research and animal care staff at the
Yerkes National Primate Research Center Field
Station use positive reinforcement when working
with the chimpanzees. Hence, the chimpanzees
have an established history of positive
interactions with these specific individuals.
Potentially, known humans may be categorized as
something approaching an ingroup and unknown
humans as something approaching an outgroup,
with the latter potentially limiting the
strength of a contagious response. To control
for species familiarity,we also showed
chimpanzees yawns from gelada baboons, a species
they have never seen before. Videos of gelada
baboons yawning were available from a previous
study by Palagi et al. [15]. Comparing
the response to humans and gelada baboons
allowed us to test whether a familiar,
meaningful species is necessary for crossspecies
contagion, or whether cross-species contagion
could be elicited via similarities in motor
muscle activation alone. We employed the same
experimental methods as in our previous study
[13], which allowed us to compare the
results directly as a gauge of how chimpanzees
view familiar humans, unfamiliar humans and
gelada baboons compared with their own species.
This way, we could ask chimpanzees about how our
species fits into their social world.
4. Discussion
The chimpanzees yawned significantly more
when viewing the familiar human yawn video than
the control. This result demonstrates that
familiar humans did stimulate CY; however, we
did not find that familiarity with the humans in
the video was required. Unfamiliar humans
stimulated the same yawn contagion, and the yawn
rates were not significantly different from
those for familiar humans. The third species
tested, the gelada baboon, failed to elicit the
same yawn contagion, however. Our interpretation
is that chimpanzees do not need to know each
yawning individual to show contagion, but the
individuals do need to belong to a species with
which the chimpanzees have a history of positive
social interactions. We found a difference in
the yawning rate between stimuli that did and
those that did not elicit contagion (figure 2).
Among the three stimuli that elicited contagion
(i.e. ingroup chimpanzees, familiar humans and
unfamiliar humans), the yawning rates were
similar and none of these stimuli was more
potent than another. Thus, we did not observe
different magnitudes of CY, in contrast to human
studies in which the degree of contagion follows
a continuum based on social closeness
[12]. Either humans are more
discriminating in their CY responses, or we have
not yet designed the experiment in the right way
for chimpanzees.
Human stimuli elicited a similar level of
contagion as the chimpanzees' friends and kin,
and significantly higher than strange
chimpanzees. For our subjects, a different
species (but one they have a history of positive
experiences with) was more potent at eliciting
empathy-based contagion than outsiders of their
own species. Many of our chimpanzees have not
seen or interacted with strangers of their own
species since the groups were assembled decades
ago, while others were born into the group and
may never even have seen a chimpanzee stranger.
While it is possible that the arousal of seeing
strange chimpanzees may have suppressed the
physiological yawn response [45]
irrespective of an empathic connection,
increased yawning is also a possible outcome of
high arousal [46], including in a CY
context [47]. Rather, given the
pervasive xenophobia among wild chimpanzees, in
which strangers are invariably treated with
hostility [40], we think that it is more
likely that antagonism inhibited yawn contagion
to the unfamiliar chimpanzee stimuli. Subjects
may never have reached the positive engagement
needed for an empathy-based response.
The human stimuli, on the other hand, are
not expected to arouse the same hostility as our
subjects are used to new people. Students come,
complete their studies and leave, and care staff
gain and lose members in the normal course of
people changing jobs. The chimpanzees may have
been conditioned to take a positive view of
humans in general, not just the ones that they
know. This is not to preclude that the
chimpanzees do not make distinctions between
familiar and unfamiliar humans, only that this
distinction was not detected by our behavioural
measure. How do the chimpanzees view gelada
baboons? The rate of yawning was the same as
that for outgroup chimpanzees (i.e. an absence
of any significant contagion). Does this mean
that chimpanzees responded with hostility to
gelada baboons as well? This possibility cannot
be excluded, yet given chimpanzee natural
history it seems unlikely. At Gombe National
Park, where chimpanzees interact freely with
baboons (Papio anubis), affiliative interactions
are common and competition between both species
is limited [48].
Our data rather suggest a different
possibility. The chimpanzees spent significantly
more time looking at the outgroup chimpanzee
videos than at gelada baboons or any other
stimulus class (figure 3). Our subjects thus
seemed far more interested in outgroup
chimpanzees than gelada baboons, yet they showed
a similar, minimal yawn response to both.
Outgroup chimpanzees possibly elicited a hostile
response, which interfered with empathybased
engagement [49], whereas the gelada
baboons were viewed as a socially meaningless
stimulus. If true, we could say that CY with
strange chimpanzees was actively thwarted,
whereas with geladas it was not there to begin
with. The different responses to the different
stimuli further support the idea that CY is
socially modulated, and thus serves as a measure
of empathic engagement with the stimulus. As
outgroup chimpanzees and gelada baboons did not
stimulate significant rates of yawning, CY does
not seem to be a simple fixed-action pattern for
which any yawn may serve as a releaser. As for
why humans but not gelada baboons stimulated
contagion, physical resemblance or lack thereof
probably does not alone account for the
differences as outgroup chimpanzees did not
stimulate CY. Rather, social experience probably
plays a role.Would mere exposure to gelada
baboons make them more familiar and lead to
contagion? Or is mere exposure not enough and CY
requires a history of positive social
interactions, such as the chimpanzees have with
most humans?
Most interestingly, could experience change
the way chimpanzees respond to outgroup
chimpanzees? These are unanswered questions. By
forming measurable empathy-based contagion with
unfamiliar humans, chimpanzees showed that the
ability to connect with unfamiliar individuals
is not unique to humans. Conditions within the
human evolutionary lineage may have altered the
expression of this ability, but flexible social
engagementwas probably already present in the
most recent common ancestor with chimpanzees.
This flexibility opens a door to examining how
we can modify who chimpanzees will form an
empathy-based connection with and how strongly.
Understanding this flexibility in social
engagement may help explain the proximate
mechanisms that allow for switching between
cooperation and competition within chimpanzee
and human societies [50].
