While spontaneous yawning is common across
all vertebrate classes, contagious yawning is
less common and has been observed only in a few
species of social animals. Interspecific
contagious yawning in response to yawning by
humans has been observed only by chimpanzees and
dogs. After confirming additional occurrences of
intraspecific contagious yawning in a group of
captive African elephants previously studied, we
further investigated the potential for the same
group of elephants to engage in interspecific
contagious yawning with familiar human handlers.
Ten captive African elephants, most of whom had
been previously studied, were observed over 13
nights for evidence of intraspecific contagious
yawning. Seven of these elephants were also
involved in trials where familiar handlers
performed staged yawns, as well as trials with
staged non-yawning gapes, or trials with no
yawns or gapes. Incorporating previously
collected contagious yawning data, we describe
nine instances of intraspecific contagious
yawning in the elephants. Three of the seven
elephants yawned contagiously in response to
humans during the interspecific yawning trials.
This is the first report of interspecific
contagious yawning by elephants in response to
yawns by familiar humans.
Bâillements
contagieux d'éléphants en
réponse à des bâillements
d'humains familiers
Alors que le bâillement
spontané s'observe dans toutes les
classes de vertébrés, le
bâillement contagieux est moins courant et
n'a été observé que chez
quelques espèces d'animaux sociaux. Le
bâillement contagieux
interspécifique en réponse au
bâillement par l'homme n'a
été observé que par les
chimpanzés et les chiens. Après
avoir confirmé des occurrences
supplémentaires de bâillements
contagieux intraspécifiques dans un
groupe d'éléphants africains
captifs précédemment
étudiés, nous avons approfondi la
possibilité pour le même groupe
d'éléphants de s'engager dans des
bâillements contagieux
interspécifiques avec des soigneurs
humains familiers.
Dix éléphants africains en
captivité, dont la plupart avaient
déjà été
étudiés, ont été
observés pendant 13 nuits pour visualiser
leurs bâillements contagieux
intraspécifiques. Sept de ces
éléphants ont également
participé à des essais où
des soigneurs familiers (ou cornacs)
effectuaient des bâillements
répétés, ainsi que des
essais avec des ouvertures de bouche banales, ou
des essais sans bâillements ni bouche
ouverte.
En incorporant les données de
bâillements contagieux
précédemment collectées,
nous décrivons neuf cas de
bâillements contagieux
intraspécifiques chez les
éléphants. Trois des sept
éléphants ont bâillé
de manière contagieuse en réponse
aux humains lors des essais de bâillements
interspécifiques. Il s'agit du premier
signalement de bâillements contagieux
interspécifiques
d'éléphants en réponse
à des bâillements d'humains
familiers.
Introduction
Spontaneous yawning is an ancestral trait
that has been identified in many species across
all classes of vertebrates (1). There are
several hypotheses relating to the function of
yawning, but it is generally accepted that
yawning relates to a state change and plays a
role in brain activation (1, 2). While
spontaneous yawning is an ancestral trait,
involving the older parts of the brain,
contagious yawning, in which an animal yawns
upon seeing another yawn, is thought to be
controlled by the neocortex which is essential
for complex social interactions (3). Contagious
yawning with conspecifics (intraspecific
contagious yawning) has been reported in several
species of social animals including humans,
chimpanzees, baboons, wolves, sheep, and
budgerigars (4&endash;9). These studies
generally show a positive relationship between
familiarity among the participants and
likelihood of yawning.
Contagious yawning between members of
different species (interspecific contagious
yawning) has been observed between humans and
chimpanzees as well as humans and dogs
(10&endash;13). Interestingly, yawn contagion
has been reported in different situations
between humans and dogs, but not between dogs.
In the studies of contagious yawning with humans
in both dogs and chimpanzees, there was no
evident difference in yawning responses to
familiar versus unfamiliar humans; this was also
the case in a study looking at contagious
yawning by chimpanzees in response to an android
(14).
Contagious yawning is, by nature, a social
behavior, but it is not entirely clear what
communicative function it serves. Several
investigators associate the phenomenon with
empathy (4&endash;8). Other investigators have
questioned the link to empathy (15). In humans,
a contagious yawn can be prompted not only by
seeing a yawn, but also by hearing or even
thinking about a yawn (16, 17).
Since African elephants have a highly
developed cognitive brain (18, 19), and are a
social mammal adapted for group living, it is
reasonable to expect that they would exhibit
contagious yawning with other familiar
elephants. Our previous study investigated
yawning behavior in captive African elephants at
the same study site as the present study,
reporting 6 instances of contagious yawning
(20), 4 of which were by standing
elephants.
As background information for the frequency
of yawning by standing elephants at night, in
the previous study, we accumulated 73.3 h of
observations in the nighttime enclosure; this
excluded all 2-min periods that were associated
with an elephant arousing. During these
non-arousing time periods, we observed only 4
spontaneous yawns by the standing elephants,
meaning that the rate of a standing elephant
spontaneously yawning apart from the 2-min
periods of an arousing elephant that might be
yawning was 0.055 yawns/h (4 yawns/73.3 h), or
one yawn in over 18 h. Spontaneous yawns by
standing elephants outside of arousal episodes
within the group thus were extremely rare. This
previous study, along with information about
elephant-initiated interactions with people at
the same study site (21), provided the context
for the current study.
One goal of the present study was to confirm
and expand upon our previous descriptions of
intraspecific contagious yawning among the same
group of elephants, at a different time and with
some changes in the group composition. The
second goal was to determine if the human
handlers that regularly interacted with the
elephants during the day would evoke yawning
from the elephants by yawning in a manner
similar to that used in the studies of humans
evoking yawns from dogs and captive chimpanzees.
These observations were conducted in the early
morning, outside the nighttime enclosure, a time
when spontaneous yawning would be highly
unlikely.
The setting of this study included
videorecording of the behavior of the elephants
freely moving at night; these recordings were
available for perusal later by an investigator.
The structured interactions of the handlers with
the elephants each morning were a daily routine.
As noted, the occurrence of contagious yawning
is rare compared with spontaneous yawning, so
the number of elephants exhibiting intraspecific
and/or interspecific contagious yawns by
elephants was expected to be small. With
elephants, where opportunities to record some
behaviors is limited, but the behaviors are
meaningful in understanding elephants'
comparative behavior, a documented occurrence in
just a few individuals is important. The
parameters used in designating a yawn as
contagious are presented in detail. Recent
examples of reports of just one or two instances
of elephant behavior, where details are given,
are of sleeping bouts in two wild African
elephants in nature (22) and self-identification
in a mirror by one elephant (23).
Discussion
Intraspecific Contagious Yawning
The results from our nighttime observations,
with three instances of contagious yawning
meeting the specific criteria, expand upon and
confirm our previous report of intraspecific
contagious yawning between elephants (20). There
were two instances where a standing elephant
yawned in response to an arousing elephant
yawning and one from a standing elephant yawning
in response to another standing elephant
yawning. This latter instance expands the
contexts in which contagious yawning in African
elephants may be expected to occur. The most
frequent context is that where a standing
elephant yawns in response to yawning by an
elephant arousing or just after arousing and
standing. The next most frequent context is an
arousing elephant yawning in response to yawning
by another arousing elephant. This was not seen
in this present study, but was seen in the
previous study. The third context is a standing
elephant yawning in response to yawning by
another standing elephant. To address the issue
of a spontaneous yawn occurring in a standing
elephant being mistaken for a contagious yawn,
we calculated the probability of a spontaneous
yawn by a standing elephant, being < 0.001.
Table 1 outlines the nine occurrences of
intraspecific contagious yawns seen in the two
studies. The varieties of contexts are mindful
of the different contexts of contagious yawning
in humans, ranging from directly looking at
another person, to just hearing someone talking
about yawning (4, 16).
Interspecific Contagious Yawning
Trials to test for interspecific yawning
were conducted early in the morning when the
elephants had just been taken from the nighttime
enclosure. This was a few hours after the time
when spontaneous yawning and contagious yawning
between elephants had been observed. As noted in
the introduction, spontaneous yawning was almost
always seen in association with arousal from
recumbent sleeping or resting bouts, and not at
other times. Thus, yawns that occurred during
these handler trials are unlikely to have been
spontaneous.
The testing protocol followed was similar to
that used in trials with dogs and chimpanzees to
observe for yawning by the animal in response to
yawning by the human that was facing the animal.
In trials on dogs and chimpanzees, the human
yawned several times before a yawn occurred by
the animal, if it occurred. The durations and
patterns of contagious yawning in handler trials
were typical of spontaneous yawns and of those
seen in the contagious yawns between elephants.
In contrast with prior studies investigating
interspecific contagious yawning, our study was
conducted using only familiar humans. We do not
know if elephants would respond contagiously to
the yawn of a strange human.
The observations of Keisha during yawning
trials, in which she initially yawned in
response to the handler's yawn and then yawned
several times during her control and gape
trials, and those of other elephants, provide
evidence for her yawns being provoked in ways
other than directly seeing a yawn. Given that
spontaneous yawning is infrequent during periods
of time not associated with arousal, it is
unlikely that Keisha's prevalent yawning was
occurring as spontaneous yawns. This yawning
behavior by Keisha seems analogous to
observations on human yawning being triggered by
thinking about a yawn (17), suggesting that
Keisha began to associate the trial context with
handlers yawning. An alternative explanation is
that the yawning was a reflection of the
positive reinforcement from the handler after
her initial contagious yawn, implying that she
then began yawning deliberately due to the
positive association of yawning with praise.
Both possibilities illustrate the involvement of
the neocortex in contagious yawning (discussed
in the introduction), as opposed to spontaneous
yawning.
Whether yawning, let alone contagious
yawning, occurs in wild free-ranging African
elephants has not been investigated at this
point. The study of two matriarchs in Botswana
from two herds of free-ranging wild elephants,
using a trunk-movement proxy for sleep, found
that the elephants slept about 2 h per night,
standing or in recumbency (22). There was no
video recording of the elephants, so it is
unknown whether or not contagious yawning, or
even spontaneous yawning, may have occurred.
Based on our studies, elephant yawns are rather
subtle. mostly occurring at night, and would
likely be missed by observers of wild
elephants.
Including the first interspecific yawn of
Keisha, we documented six interspecific yawns in
three elephants. While the number of yawns is
small, the observations meeting specific
criteria should be sufficient to establish that
elephants can, and do, display yawning in
response to seeing a familiar human yawning. As
mentioned above, at least two other notable
behaviors have been recently documented in
elephants based on just one or two individuals:
nighttime sleeping (22) and self-recognition in
a mirror (23).
A possible function of contagious yawning
among elephants living in nature, assuming it
occurs, and based on the presumed function of
yawning, is brain arousal and activation.
Yawning by an arousing elephant, leading to a
contagious yawn from elephants already awake, or
another simultaneously arousing elephant, could
facilitate a state of higher awareness and
arousal throughout the herd. Although our data
are on captive elephants, these elephants are a
well-integrated herd with group dynamics similar
to wild elephants where it would be advantageous
for an aroused state to quickly spread through a
herd in response to an external stimulus that
caused the arousal of some individuals.
The findings presented here with regard to
contagious yawning among a close group of
captive elephants, plus the occurrence of some
contagious yawning of the elephants in response
to staged human handler yawning, are consistent
with the perspective of the highly-developed
brain of elephants. Elephants have a larger
associative neural cortex than other mammals; a
neural cortex that is involved in
social-empathic responses (18, 19). As discussed
in the introduction, several studies associate
contagious yawning with empathic behavior. In
elephants, von Economo neurons (VENs) have
recently been discovered in the neocortex, and
are virtually identical to the VENs of humans
and chimpanzees (19, 24). These neurons subserve
the mental attributes of empathy and compassion
in humans. Although we cannot infer the emotions
or behavioral motivations of elephants, the
presence of VENs in elephants suggests that
elephants and humans share an important
mediating substrate for social-empathic
behaviors. While there is no currently proven
link between contagious yawning and empathy thus
far, the potential empathic aspect of contagious
yawning in elephants would be consistent with
the cytoarchitecture of the elephant brain.
