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The causes and consequences of yawning in animal groups



Yawning is a stereotyped action pattern that is prevalent across vertebrates. While there is growing consensus on the physiological functions of spontaneous yawning in neurovascular circulation and brain cooling, far less is known about how the act of yawning alters the cognition and behaviour of observers. By bridging and synthesizing a wide range of literature, this review attempts to provide a unifying framework for understanding the evolution and elaboration of derived features of yawning in social vertebrates. Recent studies in animal behaviour, psychology and neuroscience now provide evidence that yawns serve as a cue that improves the vigilance of observers, and that contagious yawning functions to synchronize and/or coordinate group activity patterns. These social responses to yawning align with research on the physiological significance of this behaviour, as well as the ubiquitous temporal and contextual variation in yawn frequency across mammals and birds. In addition, these changes in mental processing and behaviour resulting from the detection of yawning in others are consistent with variability in the expression of yawn contagion based on affinity and social status in primates. Topics for further research in these areas are discussed.
The causes and consequences of yawning in animal groups
Andrew C. Gallup
Psychology and Evolutionary Behavioral Sciences Programs, SUNY Polytechnic Institute, Utica, NY, U.S.A.
Department of Biological Sciences, Nova Southeastern University, Ft Lauderdale, FL, U.S.A.
article info
Article history:
Received 28 September 2021
Initial acceptance 29 October 2021
Final acceptance 10 January 2022
MS. number: ARV-21-00575R
circadian rhythms
collective behaviour
motor synchrony
state change
Yawning is a stereotyped action pattern that is prevalent across vertebrates. While there is growing
consensus on the physiological functions of spontaneous yawning in neurovascular circulation and brain
cooling, far less is known about how the act of yawning alters the cognition and behaviour of observers.
By bridging and synthesizing a wide range of literature, this review attempts to provide a unifying
framework for understanding the evolution and elaboration of derived features of yawning in social
vertebrates. Recent studies in animal behaviour, psychology and neuroscience now provide evidence that
yawns serve as a cue that improves the vigilance of observers, and that contagious yawning functions to
synchronize and/or coordinate group activity patterns. These social responses to yawning align with
research on the physiological signicance of this behaviour, as well as the ubiquitous temporal and
contextual variation in yawn frequency across mammals and birds. In addition, these changes in mental
processing and behaviour resulting from the detection of yawning in others are consistent with vari-
ability in the expression of yawn contagion based on afnity and social status in primates. Topics for
further research in these areas are discussed.
©2022 The Author(s). Published by Elsevier Ltd on behalf of The Association for the Study of Animal
Behaviour. This is an open access article under the CC BY-NC-ND license (
Yawning is considered a stereotyped or xed action pattern and
appears to have similar within-species duration, interval and
variability (Provine, 1986). Characterized by a three-phase
response, yawns are dened by an involuntary and powerful
gaping of the jaw, a temporary period of peak muscularcontraction
with head titling and eye closure and a passive closure of the jaw
(Barbizet, 1958). Among terrestrial vertebrates, the rst two phases
of this response often include a deep inhalation of air, while the
third phase is accompanied by a shorter expiration. Yawning and
similar yawn-like gaping behaviours are conspicuous in nature and
have been documented within all classes of vertebrates (e.g.
Baenninger, 1987;Craemer, 1924;Luttenberger, 1975;Rasa, 1971;
Sauer &Sauer, 1967). The omnipresence of this behaviour across
diverse species and lineages suggests that it is phylogenetically old
and likely evolved with the emergence of jawed shes.
The widespread nature of spontaneous, or nonsocial, yawning
suggests it is an adaptation that holds important functionality. In
fact, Charles Darwin even contemplated the conserved nature of
yawning among humans and nonhuman animals in formulating his
theory of natural selection (Darwin, 1987). Yet, clearly the mere
pervasiveness of a trait both within and across species does not
imply functional signicance, since it could represent a by-product
or spandrel (Gould &Lewontin, 1979). For yawning, however, the
case for adaptation becomes stronger when considering its hedo-
nistic properties (Provine,1986), the risks for subluxation of the jaw
(Tesfaye &Lal, 1990) and associated costs of drawing unwanted
attention, momentarily decreasing alertness and/or conicting
with immediate antipredatory behaviours (Miller et al., 2010).
Moreover, recent neurological studies provide further support for
an adaptive signicance to this behaviour (Gallup, Church, &
Pelegrino, 2016). In particular, recent phylogenetically controlled
analyses from >100 species of birds and mammals revealed robust
positive correlations between yawn duration and brain mass and
overall and cortical/pallium neuron totals (Massen et al., 2021).
These ndings demonstrate a link between yawn duration and
brain size and complexity that cannot be explained by allometry
alone, indicating yawns likely serve an important neurophysiologic
function that has been conserved across amniote evolution.
Studies examining the ultimate mechanisms of yawning typi-
cally focus on roles either in physiology or in social behaviour
(Guggisberg et al., 2010). Instead of one or the other, however,
emerging research indicates that yawning holds both physiological
and social functionality. That said, the ubiquity of yawning across
lineages, within nonsocial animals and during periods of seclusion
leads to the conclusion that the primitive feature of this behaviour
is physiologic. Accordingly, any social roles of yawning in gregar-
ious species would represent a more recently derived feature of this
trait, built upon the original neurophysiological function(s) shared
across vertebrates (Gallup, 2011). This perspective can be further
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Animal Behaviour 187 (2022) 209e219
illustrated when comparing spontaneous yawns, which are
generated by internal changes in physiology, with contagious
yawns, which are triggered socially by sensing the yawns of others.
By denition, every contagious yawn can be traced back to an
original spontaneous yawn, and thus contagious yawning must
have evolved more recently in time. Further lines of evidence also
lead to the same conclusion. Spontaneous yawning is ubiquitous
among vertebrates (Baenninger,1987;Massen et al., 2021), appears
to be a universal act within a given species (Walusinski, 2018) and
begins early on during embryological development (de Vries et al.,
1982). These features all indicate that spontaneous yawning holds
basic and important functionality that is not social. Conversely,
contagious yawning has only been documented in social species
(Massen &Gallup, 2017;Palagi et al., 2020), shows individual
variability in expression (humans, Homo sapiens:Provine, 1986;
chimpanzees, Pan troglodytes:Anderson et al., 2004) and does not
develop until after infancy (humans: Cordoni et al., 2021;Millen &
Anderson, 2011; chimpanzees: Madsen et al., 2013; domesticated
dogs, Canis lupus familiaris:Madsen &Persson, 2013). Collectively,
these lines of evidence suggest a more recent phylogenetic origin
for yawn contagion.
This review will highlight the current scientic understanding
of the ways in which yawns alter the cognition of observers and
facilitate changes in group dynamics across diverse species, as well
as offer suggestions for future investigation in these areas. In
particular, various lines of research will be presented that reveal
adaptive outcomes to (1) the mere detection of yawns as well as (2)
subsequent yawn contagion. In both cases, it is essential to un-
derstand the underlying physiological causes and consequences of
spontaneous yawning. First, when it comes to yawn detection, the
internal changes that initiate this behaviour in the actor are what
determines the information that is transmitted to receivers. In
other words, the way yawns change the behaviour of observers
hinges upon what they reveal about the internal state of the
yawner. Second, when it comes to contagious yawns, an under-
standing of the biological signicance of this motor action pattern is
essential to appreciate how its propagation via contagion may then
go on to alter subsequent behaviour of the collective. Not only do
spontaneous and contagious yawns share a similar morphology (i.e.
they appear indistinguishable from one another), but based on the
cumulative properties of evolution, we should expect that they also
share similar fundamental mechanistic and perhaps functional
properties. Accordingly, the factors known to trigger spontaneous
yawns should have a similar effect on yawn contagion. This view is
supported by psychological research showing that the expression
of contagious yawning can be effectively modulated by the same
physiological variables known to modulate spontaneous yawning.
These include circadian factors (Gallup et al., 2021;Giganti &Zilli,
2011), cooling and warming of the brain via temperature manipu-
lations to the neck and skull (Gallup &Gallup, 2007;Ramirez et al.,
2019), ambient temperature variation (e.g. Eldakar et al., 2015;
Massen et al., 2014) and stressful situations (Eldakar et al., 2017).
Therefore, prior to focusing on the social nature of yawning, I
discuss the literature on the physiology, contexts and environ-
mental triggers of spontaneous yawning.
Numerous hypotheses have been proposed to explain the
physiological signicance of yawning (e.g. Smith, 1999), but most
lack empirical support or have been falsied. This includes the
common, but incorrect, assertion that yawning functions to equil-
ibrate blood oxygen levels. Through a series of elegant experiments
on human subjects, Provine, Tate, et al. (1987) demonstrated that
yawn frequency is not altered by breathing enhanced or decreased
levels of O
or CO
, and physical exercise sufcient to double
breathing rates had no effect on yawning. It has therefore been
concluded that yawning and breathing are controlled by different
mechanisms, and it is now widely accepted in the scientic liter-
ature that respiration is not a necessary component of yawning
(Corey et al., 2012;Guggisberg et al., 2010). These conclusions also
align with recent research showing that yawn-like behaviour of
common bottlenose dolphins, Tursiops truncatus, occurs in the
absence of breathing (Enokizu et al., 2021).
Instead, studies suggest that yawning functions to facilitate state
change (Provine, 1986,2005) and increase arousal (Greco &
Baenninger, 1991;Matikainen &Elo, 2008;Walusinski, 2006).
The state change hypothesis has shown to be a powerful framework
for understanding this behaviour, as yawns are by far most frequent
during changes in state associated with behavioural transitions,
such as from sleeping to waking, fromwaking to sleeping and from
uctuations of attentiveness and boredom, and even sexual arousal
(Provine, 2005). Related to the switching of activity patterns, yawns
commonly occur in anticipation of important events and tend to be
followed by an arousing effect both behaviourally and physiologi-
cally (reviewed by Baenninger, 1997). In addition, laboratory
studies have shown that electrical and chemical stimulation of the
paraventricular nucleus of the hypothalamus, the brain area that
controls yawning (Argiolas &Melis, 1998;Melis et al., 1987), evokes
both yawning and cortical arousal in Wistar rats (Sato-Suzuki et al.,
1998;Seki et al., 2002). Mechanistically, state change and arousal
could be achieved through the acceleration of heart rate, intracra-
nial circulation and cerebrospinal uid ow produced by the deep
inhalation and powerful stretching of the jaw during yawning
(Askenasy, 1989;Matikainen &Elo, 2008;Schroth &Klose, 1992;
Walusinski, 2014).
Given the rise in yawn frequency prior to sleep onset (e.g.
Provine, Hamernik, et al., 1987;Zilli et al., 2007), however, it be-
comes clear that not all yawns result in increased arousal. Although
yawning consistently precedes initial increases in motor activity
(Baenninger et al., 1996) and skin conductance (Greco &
Baenninger, 1991), subsequent changes in arousal and alertness
from this behaviour may be governed by circadian factors. This
perspective can potentially explain differences in the neurological
effects documented after yawns in humans as measured by elec-
troencephalography. For example, during the intravenous induc-
tion of general anaesthesia, which produces a controlled loss of
awareness during an otherwise active state, yawns are frequently
observed and induce counteracting spikes in arousal (Kasuya et al.,
2005). Among individuals experiencing excessive sleepiness,
however, yawns occur during periods of progressive drowsiness
and sleep pressure but fail to produce increases in arousal
(Guggisberg et al., 2007). Therefore, while yawning is consistently
triggered during low vigilance, it may be that increases in arousal
from this action pattern occur primarily during waking and active
states rather than during periods of sleepiness/fatigue prior to
resting or sleep onset.
More recent research provides evidence for a thermoregulatory
function to yawning in homeotherms (Gallup &Gallup, 2007,
2008). This hypothesis proposes that yawns function to cool the
brain, which in turn could improve alertness and mental processing
efciency of the yawner. Accordingly, yawns should be triggered by
initial rises in brain temperature and the action pattern of yawning
should function as a compensatory brain cooling mechanism by
promoting increased cerebral blood ow, ventilation of the sinus
system and countercurrent heat exchange with the ambient air
(reviewed by Gallup &Eldakar, 2013). Consistent with these pre-
dictions, laboratory studies on humans, rodents and birds show
that yawns are preceded by rises in brain/skull temperature and
that, following the execution of this behaviour, temperatures
A. C. Gallup / Animal Behaviour 187 (2022) 209e219210
decrease signicantly (Eguibar et al., 2017;Gallup &Gallup, 2010;
Gallup et al., 2017;Shoup-Knox et al., 2010). Moreover, the
manipulation of brain temperature in humans has recently been
shown to produce predicted changes in yawn frequency (Ramirez
et al., 2019). In addition, consistent with the view that yawning
evolved a brain cooling function, comparative studies on humans
(Massen et al., 2014), nonhuman primates (Macaca fascicularis:
Deputte, 1994;Cebus capucinus: Campos &Fedigan, 2009), rats
(Rattus norvegicus:Gallup et al., 2011) and birds (Melopsittacus
undulatus:Gallup et al., 2009,2010) all show that yawn frequency
can be reliably manipulated by changes in ambient temperature.
Consistent with the aforementioned physiological signicance
of yawning, a large number of comparative studies have revealed
similar contexts and behavioural changes that accompany yawns
across diverse species that relate to state change, arousal and
thermoregulation. In particular, this includes the close temporal
connection between sleeping and waking, activity patterns and
Circadian Variation and Behavioural Transitions
The most well-documented feature of yawning across different
species is its link to circadian changes in sleep and activity. Studies
in humans consistently show a bimodal distribution in yawn fre-
quency during the day, with an initial rise in the rate of yawning
shortly after waking in the morning and a larger increase in yawn
frequency in the evening prior to sleep onset (Baenninger et al.,
1996;Giganti et al., 2010;Provine, Hamernik, et al., 1987;Giganti
&Zilli, 2011;Zilli et al., 2007,2008). Consistent with links to
drowsiness, human yawns are also more common during periods of
boredom and/or low levels of stimulation (Provine &Hamernik,
1986). In addition to showing clear connections to state change
and modied arousal, changes in yawn frequency before and after
sleeping correlate strongly with circadian uctuations in brain/
body temperature (Landolt et al., 1995).
Similar temporal patterns of yawning are observed in wild
nonhuman primates, including grey-cheeked mangabeys, Lopho-
cebus albigena, and crab-eating macaques, M. fascicularis, where
pre- and post-sleep yawning peaks occur throughout the day
(Deputte, 1994). Analogous patterns are also observed in Sprague
Dawley rats in the laboratory, whereby yawns occur with greatest
frequency during transitional sleep/wake phases (Anias et al.,
1984). In captive chimpanzees, one study found that nearly all in-
stances of yawning (98.2%) occurred during periods of rest while
sitting and lying down (Vick &Paukner, 2010). Yawning also
commonly occurs under similar contexts in sea lions (Otaria a-
vescens)(Palagi, Guill
en-Salazar, et al., 2019) and has been linked
with sleep or recumbency periods in African elephants, Loxodonta
africana (Rossman et al., 2017).
Yawning appears to be driven by similar circadian factors in
birds as well. In the South African ostrich, Struthio camelus australis,
for example, it is noted that yawning occurs just prior to sleeping/
resting and again when a rest has been interrupted (Sauer &Sauer,
1967). In captive budgerigars, M. undulatus, the temporal variation
in yawning also varies across the day and is frequent in the evening
prior to sleep onset (Miller, Gallup, Vogel, Vicario, et al., 2012).
Based on the circadian factors that inuence yawning and the
purported arousing function of yawns (Baenninger, 1997), this
behaviour has also been noted to precede increases in activity
levels across taxa. In preterm human infants, yawns appear to in-
crease behavioural arousal and predict higher motoric activation
(Giganti et al., 2002). Similarly, among young adults (e.g. college
students), instances of yawning seem to be unvaryingly followed by
an increase in activity (as measured by wrist movement)
(Baenninger et al., 1996). Likewise, an increase in locomotion
within the rst few minutes after yawning has been documented in
both captive chimpanzees (Vick &Paukner, 2010) and bottlenose
dolphins (Enokizu et al., 2021). Yawning is also common during
varied behavioural transitions in wild populations of ringtailed le-
murs, Lemur catta, and white sifaka, Propithecus verreauxi (Zannella
et al., 2015). Analogously, yawns occur primarily upon arousal from
recumbency in African elephants (Rossman et al., 2017) and
alongside new phases in activity among South African ostriches
(Sauer &Sauer, 1967).
Stress and Anxiety
Yawning also tends to increase during and following periods of
stress across diverse species. Stressful situations naturally elicit
changes in mental state and arousal, and among varied physio-
logical effects, stress produces rises in bodily temperature (i.e.
stress-induced hyperthermia: Olivier et al., 2003;Zethof et al.,
1994). In humans, increases in yawning have been observed lead-
ing up to stressful and anxiety-provoking events, such as in para-
troopers prior to their rst free-fall, musicians waiting to perform
and Olympic athletes prior to competition (Provine, 2005). Among
nonhuman primates, yawning and other self-directed behaviours
(e.g. scratching, self-grooming) are considered an indicator of
psychosocial stress and anxiety (Maestripieri et al., 1992). In female
olive baboons, Papio anubus, for example, self-directed behaviours
like yawning increase substantially when the closest neighbour is
dominant compared to subordinate (Castles et al., 1999). For wild
chimpanzees, yawning has been noted to increase in the presence
of humans (Goodall, 1968) as well as following vocalizations from
neighbouring groups of conspecics (Baker &Aureli, 1997). Simi-
larly, a positive correlation has been observed between yawn fre-
quency and aggressive behaviour in Przewalski horses, Equus ferus
przewalskii (G
orecka-Bruzda et al., 2016). Yawning also increases
following nonsocial stressors. In strepsirrhine primates, yawns in-
crease following alarm calls or after predator attacks (Zannella
et al., 2015), and fear conditioning trials have been shown to
induce yawning in Wistar rats (Kubota et al., 2014).
A combination of experimental and observational studies across
a diverse array of mammals and birds have revealed a distinct
temporal relationship between the onset of stress and the associ-
ated yawning response (Demuru &Palagi, 2012;Eldakar et al.,
2017;Fenner et al., 2016;Liang et al., 2015;Miller et al., 2010;
Miller, Gallup, Vogel, &Clark, 2012;Moyaho &Valencia, 2002). For
example, in a study of captive budgerigars, yawns were measured
over a 1 h period following handling restraint (Miller et al., 2010). In
the rst 20 min following this encounter, yawning was relatively
infrequent (~1.5 M yawns/h), but in the next 20 min, yawn fre-
quency more than tripled (>5 yawns/h). Moreover, yawn latency
was negatively correlated with body temperature increases due to
handling, i.e. birds that were more hyperthermic yawned sooner. In
a separate study on wild Nadza boobies, Sula granti, yawning was
measured in adult birds during and after a comparable human
capture-restraint stressor (Liang et al., 2015). Similar to budgeri-
gars, booby yawns were absent during the stressor itself and
remained at low frequency from 0 to 30 min following release
(median ¼0) before increasing signicantly 30e60 min thereafter
(median ¼2). Lastly, in a study on humans, Eldakar et al. (2017)
examined the impact of an acute physical stressor (cold pressor
test) on contagiously triggered yawning. Analogous to the avian
research, yawns were infrequent immediately following the
stressor, but 20 min thereafter both the overall frequency of
yawning and the number of participants that yawned at least once
A. C. Gallup / Animal Behaviour 187 (2022) 209e219 211
during testing doubled. Taken together, these ndings appear to
reveal a homologous temporal effect regarding the relationship
between yawning and acute physical stress in birds and mammals,
whereby yawning is inhibited during stressors, but then becomes
potentiated thereafter.
Atop the physiological signicance of yawning, researchers have
long posited additional social functions to this behaviour (Deputte,
1994;Leone et al., 2014;Moyaho et al., 2017;Sauer &Sauer, 1967).
In particular, it was initially suggested that, among primates, yawns
preceded by a social interaction could provide a communicative
function to conspecics (Bolwig, 1959). In order to function in this
capacity, however, yawns must be detected and distinguished from
background noise by receivers (Wiley, 2006). In support of this
view, recent neurological research shows that human infants as
young as 5 months old can discriminate yawning from other types
of mouth movements (Tsurumi et al., 2019). Using functional near-
infrared spectroscopy, the presentation of yawning stimuli pro-
duced a signicantly increased haemodynamic response at the
superior temporal sulcus, as measured by the concentration of
oxyhaemoglobin. This work indicates that the neural mechanism
underlying the processing of yawning movements develops very
early on in humans eat about the same time infants begin to
discriminate emotional facial expressions (Kotsoni et al., 2001;
LaBarbera et al., 1976)esuggesting that the detection of yawns in
conspecics is biologically important.
Given the close relation to sleeping, it has been proposed that
yawns serve as a paralingual signal for drowsiness in humans
(Provine, Hamernik, et al., 1987). As yawns are also noted during
states of hunger and psychological stress in nonhuman primates,
Deputte (1994) suggested that yawning could be viewed as an in-
dicator of uneasinesssimilar to other self-directed behaviours.
More recently, in an attempt to account for the varied contexts and
situations in which yawning is elicited, Guggisberg et al. (2010)
proposed that yawns function in communicating mild to moder-
ately unpleasant, but not immediately threatening, states to other
members of a group. However, this appears overly general and
nonspecic. In order for traits to evolve a signalling function as
stated, the information transmitted by the sender must be reliable
and easily interpreted (Searcy &Nowicki, 2010).
One potentially unifying feature of spontaneous yawns is that
they reect a current state of low arousal and vigilance and rising
brain temperature. Therefore, the act of yawning could provide
meaningful information to conspecics. Recently, following the
observation that yawning is absent during physical stressors but
then potentiated thereafter in Nazca boobies, Liang et al. (2015)
introduced the arousal reduction hypothesis, which predicts that
yawns signal to others that the individual is experiencing a down
regulation of arousal and vigilance. This hypothesis is consistent
with psychological studies showing yawns increase in frequency
during sleepiness and fatigue (Giganti et al., 2010;Provine,
Hamernik, et al., 1987;Zilli et al., 2008) and periods of boredom
(Provine &Hamernik, 1986), as well as neurological studies
demonstrating that brain markers of decreased vigilance precede
the act of yawning (Guggisberg et al., 2007;Kasuya et al., 2005).
However, this hypothesis falls short in a number of important areas.
At its basis, signals are traits that evolved to alter the behaviour of
another organism (Maynard Smith &Harper, 2003), and the
receiver must benet from the information being transmitted
(Searcy &Nowicki, 2010). As stated, the arousal reduction hy-
pothesis is functionally unclear and fails to stipulate the benets of
yawning and who receives such benets. In addition, this
hypothesis is inconsistent with evidence for a clear arousing effect
to some yawns (for a commentary, see Gallup &Clark, 2015).
To date, the view that yawning evolved as a signal has not been
empirically supported. That is, there are no studies showing that
spontaneous yawns are elicited in ways or contexts that serve to
intentionally convey information and alter the behaviour and/or
mental processing of recipients. An exception to this would be a
distinct pattern of yawn-like behaviours within sexually dimorphic
nonhuman primates. In particular, modied mouth-gaping actions
from males, which are referred to as tension or aggression yawns,
are known to play a role in threat displays (Altmann, 1967;
Bertrand, 1969). This was in fact rst described by Charles Darwin
in The Expression of the Emotions in Man and Animals (Darwin, 1872).
In such cases, a dominant male will gape his mouth open while
xing his eyes on a target individual (a subordinate) and displaying
his canines. These yawn-like displays have been documented dur-
ing antagonist interactions and hostile social situations across
different old world monkeys (Macaca nigra:Hadidian, 1980;
M. fascicularis and Macaca fuscata:Troisi et al., 1990;Cercocebus
albigena and M. fascicularis:Deputte, 1994;Theropithacus gelada:
Leone et al., 2014). Unlike true yawns (see denition above),
however, which typically include the tilting of the head and closure
of the eyes (Deputte, 1994), the display yawner xes their attention
on the target during the episode to monitor the effect of the threat.
These tension/aggression yawns also vary in other morphological
characteristics, whereby the yawner uncovers their gums to more
clearly expose their canines (Leone et al., 2014;Zannella et al.,
2017), which is consistent with the view that these yawns are
most common in species with sexual dimorphism in canine size.
Therefore, while these threat displays indeed appear to hold a
communicative function, they are distinct from the more ubiqui-
tous forms of yawning related to sleeping, arousal and thermo-
regulation in other animals.
Yawning as a Cue
Yawns could still alter the behaviour of conspecics without
evolving a specic communicative function. Building from ideas
presented in the arousal reduction hypothesis (Liang et al., 2015),
and linking directly to known physiological function(s) and con-
texts of spontaneous yawns, Gallup and Meyers (2021) recently
proposed specic yawn-induced changes in mental processing that
should follow the observation of yawns in others. In particular, it
was predicted that seeing others perform this action pattern would
enhance the vigilance of observers as a means of compensating for
the diminished arousal and vigilance experienced by the yawner.
Independent of the resultant changes to the mental state of the
yawner, which are likely tied to circadian factors (as discussed
above), yawns are consistently triggered during states of low
arousal and vigilance (Guggisberg et al., 2007;Kasuya et al., 2005)
and rising brain temperature (Shoup-Knox et al., 2010). Although
initially described as a signal, in this case yawns likely serve as a cue
whereby the detection of this behaviour provides information
about the current (reduced) alertness of the yawner, which in turn
induces neurological changes to enhance the vigilance of observers.
This was termed the group vigilance hypothesis.
In support of this hypothesis, neuroimaging studies on humans
show distinct patterns of brain activation following exposure to
yawning stimuli that are indicative of improved threat detection.
For example, merely seeing and hearing other people yawn acti-
vates regions of the prefrontal cortex (Arnott et al., 2009;Nahab
et al., 2009) and the superior temporal sulcus (Schürmann et al.,
2005;Tsurumi et al., 2019). These brain regions are known to be
involved in attentional allocation to visual search (Bichot et al.,
2015;Ellison et al., 2004), the detection of biologically relevant
A. C. Gallup / Animal Behaviour 187 (2022) 209e219212
and threatening stimuli (Dinh et al., 2018;Mobbs et al., 2007) and
vigilance (Nelson et al., 2014;Parasuraman et al., 1998).
As a direct test of the group vigilance hypothesis, Gallup and
Meyers (2021) had 38 human subjects complete a series of visual
search tasks for detecting snakes and frogs (repeated measures
design). Snakes represented a recurrent evolutionary threat to
humans (Headland &Greene, 2011;Isbell, 2006;Kasturiratne et al.,
2008), while frogs served as a control stimulus. Participants were
displayed eight-image arrays, where a single snake or single frog
was presented among seven distractor images. During each trial,
participants were tasked with locating the single target image (a
frog or snake) as quickly as possible. A series of snake-target and
frog-target searches were performed both after viewing videos of
people yawning and after viewing the same people display neutral
behaviour with nonyawning mouth movements. Eye tracking was
used to measure the latency to xate on target images across trials.
As predicted by the group vigilance hypothesis, vigilance was
selectively enhanced after viewing videos of other people yawning.
That is, participants detected snakes more rapidly after seeing other
people yawn, while this manipulation had no effect on the detec-
tion of frogs. The results from Gallup and Meyers (2021) are
consistent with studies on the physiological signicance and con-
texts of spontaneous yawning and represent the rst experimental
evidence for changes in cognitive performance induced merely by
the observation of yawns in others.
The detection of yawns from conspecics is also known to elicit
more overt behavioural changes, such as yawn contagion, whereby
the yawns of others can trigger the reexive matching of this action
pattern in observers. Studies show that contagious yawning can be
triggered through visual and/or auditory cues (Massen et al., 2015;
Norscia et al., 2020;Palagi et al., 2009;Silva et al., 2012), and in
humans can even be induced in solitude by thinking or reading
about the act of yawning (Greco &Baenninger, 1991;Provine, 1986,
2005). The neural mechanisms governing contagious yawning are
not well known, but perhaps involve mirror neurons (Haker et al.,
2013). Comparatively, there is a growing number of species with
documented evidence for yawn contagion, with the phylogeny of
this behaviour possibly reecting the conservation of a homologous
trait in great apes and convergent evolution in other lineages.
Among the great apes, experimental evidence for contagious
yawning is present in humans (Platek et al., 2003), chimpanzees
(Anderson et al., 2004;Campbell et al., 2009), bonobos, Pan pan-
iscus (Tan et al., 2017), and orang-utans, Pongo pygmaeus (van Berlo
et al., 2020). Chimpanzees also yawn contagiously in response to
human yawners (e.g. Campbell &de Waal, 2014). However, there is
no evidence for yawn contagion among gorillas, Gorilla gorilla
(Amici et al., 2014;Palagi, Norscia, et al., 2019). In other primates,
the evidence for contagious yawning is limited. However, obser-
vations of gelada baboons indicate yawn contagion in both captive
and wild populations (Gallo et al., 2021;Palagi et al., 2009). There is
also a report of video-induced yawning in stump-tailed macaques,
Macaca arctoides (Paukner &Anderson, 2006), but this response
has been interpreted as a sign of stress and anxiety rather than
contagion since the yawning stimuli also produced an increase in
other self-directed behaviours (i.e. scratching). Other studies show
no evidence for contagious yawning in crab-eating macaques and
grey-cheeked mangabeys (Deputte, 1978), common marmosets,
Callithrix jacchus (Massen et al., 2016), or in either ringtailed le-
murs, L. catta, or red-ruffed lemurs, Varecia variegata rubra (Reddy
et al., 2016).
Across other mammals, experimental evidence for contagious
yawning has been documented in domesticated dogs in response to
human yawns (Joly-Mascheroni et al., 2008;Romero et al., 2013;
Silva et al., 2012) but not in response to conspecics (Harr et al.,
2009), which could reect selection on the emphasis of attending
to human cues during domestication. There is also experimental
evidence for contagious yawning in a subline of SpragueeDawley
rats (Moyaho et al., 2015). Observational evidence for contagious
yawning is present in captive wolves (Canis lupus lupus)(Romero
et al., 2014), and most recently, domesticated pigs, Sus scrofa
(Norscia, Coco, et al., 2021), and African lions, Pantheo leo (Cassetta
et al., 2021). Other mammalian species with limited evidence of
yawn contagion, thus requiring further investigation, include
sheep, Ovis aries (Yonezawa et al., 2017), African elephants
(Rossman et al., 2020), and southern elephant seals, Mirounga le-
onine (Wojczulanis-Jakubas et al., 2019). One study on horses, Equus
caballus, provided no evidence for yawn contagion (Malavasi,
Only a few studies have investigated contagious yawning among
nonmammalian species. No formal investigations have been per-
formed on amphibians or sh, although Baenninger (1987)
assessed the temporal expression of yawn-like behaviours in Sia-
mese ghting sh, Betta splendens, and found no evidence for
contagion. In the only study on reptiles, the responses of red-footed
tortoises, Geochelone carbonaria, were observed following the
observation of conditioned yawn-like behaviour in a conspecic
(Wilkinson et al., 2011). No increase in tortoise yawning occurred
when compared to control conditions. To date, the only evidence
for yawn contagion in a nonmammalian species comes from
studies on captive budgerigars, whereby yawns appear temporally
clustered within ocks under seminatural conditions (Miller,
Gallup, Vogel, Vicario, et al., 2012) and can be experimentally
triggered following exposure to both live and videorecorded yawns
from conspecics (Gallup et al., 2015). In the only other study on
yawn contagion among birds, observations of captive ravens,
Corvus corax, found no evidence for this effect (Gallup et al., 2014).
Comparative studies of contagious yawning have thus far been
relatively limited, so there are bound to be other species that show
this behaviour. However, it is worth noting that there are a number
of methodological challenges to the study of yawn contagion
(Campbell &Cox, 2019;Campbell &de Waal, 2010). Experimental
studies offer the most robust test, whereby explicit yawn versus
control comparisons can be made, but experiments are often
limited to animals in captivity. In addition, many experiments
designed to elicit yawn contagion use video stimuli with repeated
clips of yawning, which could inadvertently produce a supernormal
stimulus (Anderson, 2010). Moreover, video stimuli might not be
optimal for all species (D'Eath, 1998). As an alternative experi-
mental approach, live animals can be paired together both with and
without visual and/or auditory access, and the temporal association
of yawning between individuals can be assessed across conditions
(e.g. Gallup et al., 2015).
Observational studies offer a more naturalistic depiction of
yawn contagion, but these also present methodological challenges.
Such studies often classify yawns as contagious when they occur
within predetermined time periods (i.e. 3 min or 5 min) following
the observation of a yawn from another individual (e.g. Demuru &
Palagi, 2012;Palagi et al., 2009). However, the clustering of yawns
within groups could also result from the individuals sharing com-
mon circadian rhythms or activity patterns and have nothing to do
with contagion. In addition, the time frames used are often arbi-
trary, and different species could have longer or shorter contagion
latencies (Campbell &Cox, 2019). As a solution to these problems,
A. C. Gallup / Animal Behaviour 187 (2022) 209e219 213
observational studies can examine the temporal distribution of
yawning across recording sessions to rule out circadian effects
(Miller, Gallup, Vogel, Vicario, et al., 2012), as well as develop
response curves, whereby the rate of yawning signicantly above
the baseline would be evidence of yawn contagion (Campbell &
Cox, 2019).
Function(s) of Contagious Yawning
While numerous studies have examined individual differences
and social-psychological correlates of yawn contagion in different
species (reviewed by Massen &Gallup, 2017;Neilands et al., 2020;
Palagi et al., 2020), only limited research has attempted to uncover
its functional signicance. That said, it has long been speculated
that the spreading of yawns across groups may function to syn-
chronize and/or coordinate group behaviour (e.g. Baenninger et al.,
1996;de Waal &Preston, 2017;Deputte, 1994;Guggisberg et al.,
2010;Massen et al., 2012;Miller, Gallup, Vogel, &Clark, 2012;
Prochazkova &Kret, 2017;Provine, Hamernik, et al., 1987;Sauer &
Sauer, 1967;Vick &Paukner, 2010), which could provide survival
benets to group members (Duranton &Gaunet, 2016). This hy-
pothesis is consistent with the large and aforementioned literature
connecting yawns to circadian rhythms and behavioural transi-
tions. For example, given that the neurovascular consequences of
yawning produce changes in state (Provine, 1986) and initiate
behavioural transitions and increased movement (Baenninger et al.,
1996;Vick &Paukner, 2010), contagion could generate coordinated
or synchronized group activity. In line with this view, ethological
studies of wild animals show that yawns are naturally clustered
within groups during collective transitions in behaviour (Deputte,
1994;Sauer &Sauer, 1967). However, these studies fail to take
into account that the individuals within these groups are under-
going similar circadian and physiologic changes that may lead to a
nonrandom distribution of yawns and a synchronization of activity
that is independent of social inuence or function (see Campbell &
Cox, 2019;Miller, Gallup, Vogel, Vicario, et al., 2012).
To date, only one study has systematically examined the role of
contagious yawning on behavioural synchronization. In an obser-
vational study of wild African lions, Casetta et al. (2021) marked the
occurrence of all yawns from 19 individuals across two social
groups in order to classify the connection between yawn contagion
and motor synchrony. Yawn contagion was dened by a yawn that
followed a yawn from another lion within a 3 min window when
there were no visual obstructions between the individuals. Motor
synchrony was dened by the collective switching of behaviour
status by either transitioning from moving to resting or resting to
moving, also within a 3 min window. It was found that motor
synchrony between lions increased by a factor of 11 when one
yawned contagiously in response to the other, which was signi-
cantly higher than situations without contagion or when there
were no yawns observed. In particular, the results showed that
yawn contagion increased the likelihood that observers would
replicate the motor patterns of actors. These ndings from Casetta
et al. (2021) are notable in providing the rst direct evidence for a
potential function to contagious yawning, which will most surely
lead to follow-up research examining the role of yawn contagion in
motor synchrony across different species.
A separate, but not mutually exclusive, adaptive hypothesis for
yawn contagion stems from the purported brain cooling function of
yawning. In particular, Gallup and Gallup (2007) proposed that
contagious yawns may have evolved to promote overall group
vigilance. Accordingly, if yawns serve to counteract rising brain
temperature and reduced alertness and mental processing, the
transfer of this behaviour to nearby conspecics could then in-
crease their vigilance as well. This hypothesis is consistent with
interdisciplinary lines of research suggesting that yawns are trig-
gered to counteract decrements in alertness and arousal
(Baenninger, 1997;Kasuya et al., 2005;Walusinski, 2006). Yet, to
date, the vigilance hypothesis has not been directly tested. One
study showed that auditory disturbances, which elicit startle re-
sponses and vigilance behaviour, also enhance yawn contagion in
budgerigars (Miller, Gallup, Vogel, &Clark, 2012). However, this
work did not examine whether contagious yawning produced a
change in vigilance thereafter. As previously discussed, recent
research on humans has also shown that merely witnessing others
yawn improves individual threat detection (Gallup &Meyers,
2021). The small number of participants that yawned conta-
giously (N¼5) in this study did not permit statistical comparisons,
but the results were highly similar for yawners and nonyawners.
Even if vigilance is not improved further among contagious
yawners ewhich remains an empirical question ethe spreading of
this cue across the group via contagion should enhance collective
vigilance under natural conditions.
In addition to extending upon existing functional hypotheses of
spontaneous yawning, and accounting for the contexts and
behavioural activities in which nonsocial yawns are most common,
the synchronization and vigilance hypotheses are consistent with
studies documenting how various social factors modulate yawn
contagion among primates: i.e. social status and afliation. For
example, within dominance hierarchies, patterns of vigilance
contagion and synchronized movement are most often initiated by
high-ranking individuals (Iki &Kutsukake, 2021), and research on
chimpanzees and bonobos shows that yawn contagion most often
stems from the yawns of dominant group members (male chim-
panzees: Massen et al., 2012; female bonobos: Demuru &Palagi,
2012). Similarly, within freely moving groups, individuals with
greater contact and afliation are more likely to display coordi-
nated movement (Farine et al., 2016), and a number of studies have
reported biases in yawn contagion based on social closeness or
afliation. This includes naturalistic observations of humans,
bonobos and gelada baboons (Demuru &Palagi, 2012;Gallo et al.,
2021;Palagi et al., 2009,2014;Norscia &Palagi, 2011;Norscia
et al., 2020; but see Massen et al., 2015) as well as video-induced
experiments on captive chimpanzees (Campbell &de Waal, 2011;
Madsen et al., 2013). As a general rule, it seems that attention drives
yawn contagion (Gallup, 2021;Massen &Gallup, 2017). Among
chimpanzees and bonobos, attention is disproportionately directed
towards individuals that are familiar and of the dominant sex
(Lewis et al., 2021). Biased attention towards higher-ranking in-
dividuals is also present in other primates, such as Angolan talapoin
monkeys, Miopithecus talapoin (Keverne et al., 1978), and rhesus
macaques, Macaca mulatta (Shepherd et al., 2006). Similarly, pri-
mates tend to stay in close proximity to genetic relatives and so-
cially bonded individuals (Macaca maurus:Matsumura &Okamoto,
1997;C. capucinus:Perry et al., 2008; chimpanzees: Langergraber
et al., 2009), increasing the chances of detecting and responding
to the yawns from these group members (Gallo et al., 2021). From
an evolutionary perspective, biases in yawn contagion based on
genetic relatedness (as has been shown in humans; Norscia &
Palagi, 2011;Norscia et al., 2020) may hold tness benets by
facilitating greater social cohesion and protection among kin.
Moreover, these hypotheses offer further explanatory power for
observed differences in yawn contagion based on reproductive
status in humans. For example, during pregnancy, women appear
more susceptible to contagious yawning (Norscia, Agostini, et al.,
2021). Given that pregnant women also have increased reactions
A. C. Gallup / Animal Behaviour 187 (2022) 209e219214
to threatening stimuli (Roos et al., 2012), heightened yawn conta-
gion could improve vigilance and group synchronization during a
period of increased danger sensitivity. Therefore, the synchroni-
zation and vigilance hypotheses offer fruitful avenues for further
Yawning is a neurophysiological adaptation that is omnipresent
across vertebrates (Massen et al., 2021), and the detection of this
action pattern in others appears to be biologically important among
social species (Tsurumi et al., 2019). Moreover, recent studies
indicate that yawning serves as a cue that enhances individual
vigilance and promotes motor synchrony through contagion (see
Fig. 1 for a graphic illustration of these processes). However, addi-
tional research is needed to replicate and further examine the na-
ture of these effects, as well as investigate potential comparative
differences in these responses based by on ecological factors and
evolutionary history. In particular, future studies could examine
how exposure to yawns alters the detection of threatening stimuli
across different species, as well as how experimentally induced
yawn contagion inuences different patterns of motor synchrony
and group coordination among human and nonhuman animals in
the laboratory. In addition, naturalistic studies could investigate
how the detection of yawning alters scanning rates and vigilance
monitoring in free-moving groups, as well as how yawning and
other patterns of behavioural contagion inuence collective
movement across different species. For example, among many
species, yawning and stretching tend to co-occur, and both be-
haviours have been found to be contagious in budgerigars (Gallup
et al., 2017;Miller, Gallup, Vogel, Vicario, et al., 2012). Since yawn
and stretch contagion could have similar functions among animal
groups in initiating collective action, future research could assess
whether behavioural contagion in general is a key feature in initi-
ating synchrony.
The current evidence suggests that yawning serves as a cue
rather than as a signal, but future studies could further examine
whether spontaneous yawns evolved specically to communicate
internal states and/or alter the behaviour of observers in some
species. For example, studies could investigate whether yawning
occurs more readily in the presence of others and in contexts in
which synchrony and/or vigilance would be most advantageous to
the group. In addition, researchers could examine patterns in the
variability of yawn expression. A recent study on macaques (Macaca
tonkeana and M. fuscata) suggests differences in the morphology and
duration of yawning are predictive of the contexts in which this
behaviour arises (Zannella et al., 2021), so follow-up studies could
also assess how different types of yawns differentially impact the
Actor: yawns
Actor: yawns
Observer: yawns
Observer: no yawn
Possible cause(s):
• Rising brain temperature
• Diminishing arousal
• Changing state
• Increased stress/anxiety
Possible cause(s):
• Rising brain temperature
• Diminishing arousal
• Changing state
• Increased stress/anxiety
Potential factors*:
• Elevated brain temperature
• Low levels of arousal
• About to change states
• Prior exposure to stressor
Social outcomes:
• Increased vigilance for observer
• Increased motor synchrony
Potential factors*:
• Thermal homeostasis
• Sufficient arousal
• Maintaining current state
• Absence of stress
Social outcomes:
• Increased vigilance for observer
• No change in motor synchrony
Figure 1. Factors known to contribute to spontaneous and contagious yawning, and graphic illustrations of the social effects resulting from the observation of yawns in others both
in the (a) absence and (b) presence of yawn contagion. *Note: potential factors explaining variability in yawn contagion are for species that show this capacity. Other variables like
status and afliation, as well as individual differences and personality factors related to social attention and biobehavioral synchrony (Gallup et al., 2021;Helt et al., 2021), are also
known to inuence this response.
A. C. Gallup / Animal Behaviour 187 (2022) 209e219 215
subsequent vigilance behaviour and synchronization of observers.
Similarly, researchers could assess differences in yawn-induced
changes in behaviour based on the presence or absence of audi-
tory cues. Vocal components to yawning appear to be common
among humans and nonprimates (e.g. Massen et al., 2015;Palagi
et al., 2009), yet seem unnecessary for the physiological func-
tion(s) of this action pattern. Thus, studies could investigate the
factors that contribute to variation in vocal yawning and how the
social outcomes of yawning vary based on visual and/or auditory
Further examination of yawning in animals could provide
important insights into the social role of this behaviour and its
function in altering group dynamics, which could in turn offer
applications for improving performance in surveillance settings
and organized group activities in our own species. Based on what is
already known about the social nature of yawning, it appears time
to systemically examine some of the more overt social features of
this behaviour in humans. This includes the stigmatization of
yawning in some cultures (Schiller, 2002), which leads to the active
concealment (Schino &Aureli, 1989) and/or inhibition of yawning
when in the presence of others (Gallup, Church, Miller, et al., 2016;
Gallup et al., 2019). For example, further research is needed to fully
understand and disentangle the potential physiologic and social
causes and consequences of inhibiting spontaneous and contagious
yawning in groups. In line with the comparative perspective
highlighted throughout this review, the bridging of both human
and nonhuman animal research will provide the most compre-
hensive understanding of this evolutionarily conserved behaviour.
Author Contributions
A.C.G. is the sole contributor to this manuscript.
I am grateful to Omar Tonsi Eldakar for providing feedback on
aspects of this manuscript. I am also grateful to the two anonymous
referees for signicantly improving this article.
Altmann, J. (1967). The structure of primate social organization. In S. A. Altamann
(Ed.), Social communication among primates (pp. 325e362). The University of
Chicago Press.
Amici, F., Aureli, F., & Call, J. (2014). Response facilitation in the four great apes: Is
there a role for empathy? Primates, 55(1), 113e118 .
Anderson, J. R. (2010). Non-human primates: A comparative developmental
perspective on yawning. In O. Walusinski (Ed.), Mystery of yawning in physiology
and disease (Vol. 28, pp. 63e76). Basel: Karger.
Anderson, J. R., Myowa-Yamakoshi, M., & Matsuzawa, T. (2004). Contagious yawning
in chimpanzees. Proceedings of the Royal Society B: Biological Sciences,
271(Suppl. 6), S468eS470.
Anias, J., Holmgren, B., Holmgren, R. U., & Eguibar, J. R. (1984). Circadian variation of
yawning behavior. Acta Neurobiologiae Experimentalis, 44,179e18 6.
Argiolas, A., & Melis, M. R. (1998). The neuropharmacology of yawning. European
Journal of Pharmacology, 343(1), 1e16 .
Arnott, S. R., Singhal, A., & Goodale, M. A. (2009). An investigation of auditory
contagious yawning. Cognitive, Affective, &Behavioral Neuroscience, 9(3),
Askenasy, J. J. M. (1989). Is yawning an arousal defense reex? Journal of Psychology,
123(6), 609e621.
Baenninger, R. (1987). Some comparative aspects of yawning in Betta splendens,
Homo sapiens, Panthera leo, and Papio sphinx.Journal of Comparative Psychology,
101(4), 349e354.
Baenninger, R. (1997). On yawning and its functions. Psychonomic Bulletin &Review,
4(2), 198e207.
Baenninger, R., Binkley, S., & Baenninger, M. (1996). Field observations of yawning
and activity in humans. Physiology &Behavior, 59(3), 421e425.
Baker, K. C., & Aureli, F. (1997). Behavioural indicators of anxiety: An empirical test
in chimpanzees. Behaviour, 134(13), 1031e1050.
Barbizet, J. (1958). Yawning. Journal of Neurology, Neurosurgery, and Psychiatry, 21(3),
van Berlo, E., Díaz-Loyo, A. P., Ju
arez-Mora, O. E., Kret, M. E., & Massen, J. J. (2020).
Experimental evidence for yawn contagion in orangutans (Pongo pygmaeus).
Scientic Reports, 10(1), 1e11.
Bertrand, M. (1969). The behavioral repertoire of the stumptail macaque. Basel:
Bichot, N. P., Heard, M. T., DeGennaro, E. M., & Desimone, R. (2015). A source for
feature-based attention in the prefrontal cortex. Neuron, 88(4), 832e844.
Bolwig, N. (1959). A study of the behaviour of the chacma baboon, Papio ursinus.
Behaviour, 14,136e163.
Campbell, M. W., Carter, J. D., Proctor, D., Eisenberg, M. L., & de Waal, F. B. (2009).
Computer animations stimulate contagious yawning in chimpanzees. Pro-
ceedings of the Royal Society B: Biological Sciences, 276(1676), 4255e4259.
Campbell, M. W., & Cox, C. R. (2019). Observational data reveal evidence and pa-
rameters of contagious yawning in the behavioral repertoire of captive-reared
chimpanzees (Pan troglodytes). Scientic Reports, 9(1), 1e13.
Campbell, M. W., & de Waal, F. B. (2010). Methodological problems in the study of
contagious yawning. In O. Walusinski (Ed.), The mystery of yawning in physiology
and disease (Vol. 28, pp. 120e127). Basel: Karger.
Campbell, M. W., & de Waal, F. B. (2011). Ingroup-outgroup bias in contagious
yawning by chimpanzees supports link to empathy. PLoS One, 6(4), Article
Campbell, M. W., & de Waal, F. B. (2014). Chimpanzees empathize with group mates
and humans, but not with baboons or unfamiliar chimpanzees. Proceedings of
the Royal Society B: Biological Sciences, 281(1782), 20140013.
Campos, F. A., & Fedigan, L. M. (2009). Behavioral adaptations to heat stress and
water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa Na-
tional Park, Costa Rica. American Journal of Physical Anthropology, 138(1),
Casetta, G., Nolfo, A. P., & Palagi, E. (2021). Yawn contagion promotes motor syn-
chrony in wild lions, Panthera leo. Animal Behaviour, 174,149e159 .
Castles, D. L., Whiten, A., & Aureli, F. (1999). Social anxiety, relationships and self-
directed behaviour among wild female olive baboons. Animal Behaviour,
58(6), 1207e1215.
Cordoni, G., Favilli, E., & Palagi, E. (2021). Earlier than previously thought: Yawn
contagion in preschool children. Developmental Psychobiology, 63(5), 931e944.
Corey, T. P., Shoup-Knox, M. L., Gordis, E. B., & Gallup, G. G., Jr. (2012). Changes in
physiology before, during, and after yawning. Frontiers in Evolutionary Neuro-
science, 3,7.
Craemer, E. (1924). Uber Sodbrennen und Gahnen. Gastroenterologia Archiv ir
Verdauungskrankheiten, 33,149e162 .
D'Eath, R. B. (1998). Can video images imitate real stimuli in animal behaviour
experiments? Biological Reviews, 73(3), 267e292.
Darwin, C. R. (1872). The expression of the emotions in man and animals. London:
John Murray.
Darwin, C. R. (1987). Notebook M (1838). In P. H. Barrett, P. J. Gantrey, S. Herbert,
D. Kohn, & S. Smith (Eds.), Charles Darwin's notebooks, 1836e1844 (pp.
517e562). Ithaca, NY: Cornell University Press.
Demuru, E., & Palagi, E. (2012). In bonobos yawn contagion is higher among kin and
friends. PLoS One, 7(11), Article e49613.
Deputte, B. L. (1978). Study of yawning in two species of Cercopithecidae; Cercocebus
albigena Gray and Macaca fascicularis Rafes: Research on causal and functional
factors; a consideration of socio-bioenergetic factors (Masters dissertation).
Rennes, France: University of Rennes 1.
Deputte, B. L. (1994). Ethological study of yawning in primates. I. Quantitative
analysis and study of causation in two species of Old World monkeys (Cerco-
cebus albigena and Macaca fascicularis). Ethology, 98(3-4), 221e245.
Dinh, H. T., Nishimaru, H., Matsumoto, J., Takamura, Y., Le, Q. V., Hori, E., Maior, R. S.,
Tomaz, C., Tran, A. H., Ono, T., & Nishijo, H. (2018). Superior neuronal detection
of snakes and conspecic faces in the macaque medial prefrontal cortex. Ce-
rebral Cortex, 28(6), 2131e2145.
Duranton, C., & Gaunet, F. (2016). Behavioural synchronization from an ethological
perspective: Overview of its adaptive value. Adaptive Behavior, 24(3), 181e191.
Eguibar, J. R., Uribe, C. A., Cortes, C., Bautista, A., & Gallup, A. C. (2017). Yawning
reduces facial temperature in the high-yawning subline of SpragueeDawley
rats. BMC Neuroscience, 18(1), 1e8.
Eldakar, O. T., Dauzonne, M., Prilutzkaya, Y., Garcia, D., Thadal, C., & Gallup, A. C.
(2015). Temperature-dependent variation in self-reported contagious yawning.
Adaptive Human Behavior and Physiology, 1(4), 460e466.
Eldakar, O. T., Tartar, J. L., Garcia, D., Ramirez, V., Dauzonne, M., Armani, Y., &
Gallup, A. C. (2017). Acute physical stress modulates the temporal expression of
self-reported contagious yawning in humans. Adaptive Human Behavior and
Physiology, 3(2), 156e17 0 .
Ellison, A., Schindler, I., Pattison, L. L., & Milner, A. D. (2004). An exploration of the
role of the superior temporal gyrus in visual search and spatial perception using
TMS. Brain, 127(10), 2307e2315.
Enokizu, A., Morisaka, T., Murakami, K., Sakurai, N., Ueda, N., & Yoshioka, M. (2021).
Yawn-like behavior in captive common bottlenose dolphins (Tursiops trunca-
tus). Behavioural Processes, 189, 104444.
Farine, D. R., Strandburg-Peshkin, A., Berger-Wolf, T., Ziebart, B., Brugere, I., Li, J., &
Crofoot, M. C. (2016). Both nearest neighbours and long-term afliates predict
individual locations during collective movement in wild baboons. Scientic
Reports, 6(1), 1e10.
Fenner, K., Yoon, S., White, P., Starling, M., & McGreevy, P. (2016). The effect of
noseband tightening on horses' behavior, eye temperature, and cardiac re-
sponses. PLoS One, 11(5), Article e0154179.
A. C. Gallup / Animal Behaviour 187 (2022) 209e219216
Gallo, A., Zanoli, A., Caselli, M., Palagi, E., & Norscia, I. (2021). First evidence of yawn
contagion in a wild monkey species. Scientic Reports, 11, 17957.
Gallup, A. C. (2011). Why do we yawn? Primitive versus derived features. Neuro-
science &Biobehavioral Reviews, 35(3), 765e769.
Gallup, A. C. (2021). On the link between emotional contagion and contagious
yawning. Neuroscience &Biobehavioral Reviews, 121,18e19.
Gallup, A. C., Church, A. M., Miller, H., Risko, E. F., & Kingstone, A. (2016). Social
presence diminishes contagious yawning in the laboratory. Scientic Reports,
6(1), 1e5.
Gallup, A. C., Church, A. M., & Pelegrino, A. J. (2016). Yawn duration predicts brain
weight and cortical neuron number in mammals. Biology Letters, 12(10),
Gallup, A. C., & Clark, A. B. (2015). Commentary: Yawning, acute stressors, and
arousal reduction in Nazca booby adults and nestlings. Frontiers in Psychology, 6,
Gallup, A. C., & Eldakar, O. T. (2013). The thermoregulatory theory of yawning: What
we know from over 5 years of research. Frontiers in Neuroscience, 6,188.
Gallup, A. C., & Gallup, G. G. (2008). Yawning and thermoregulation. Physiology &
Behavior, 95(1e2), 10e16.
Gallup, G. G., & Gallup, A. C. (2010). Excessive yawning and thermoregulation: Two
case histories of chronic, debilitating bouts of yawning. Sleep and Breathing,
14(2), 157e159.
Gallup, A. C., & Gallup, G. G., Jr. (2007). Yawning as a brain cooling mechanism:
Nasal breathing and forehead cooling diminish the incidence of contagious
yawning. Evolutionary Psychology, 5(1), 92e101.
Gallup, A. C., Kret, M., Eldakar, O. T., Folz, J., & Massen, J. J. M. (2021). People that
score high on psychopathic traits are less likely to yawn contagiously. Scientic
Reports, 11(1), 1e11.
Gallup, A. C., & Meyers, K. (2021). Seeing others yawn selectively enhances vigi-
lance: An eye-tracking study of snake detection. Animal Cognition, 24(3),
Gallup, A. C., Militello, J., Swartwood, L., & Sackett, S. (2017). Experimental evidence
of contagious stretching and ingroup bias in budgerigars (Melopsittacus undu-
latus). Journal of Comparative Psychology, 131(1), 69e72.
Gallup, A. C., Miller, M. L., & Clark, A. B. (2009). Yawning and thermoregulation in
budgerigars, Melopsittacus undulatus.Animal Behaviour, 77(1), 109e113.
Gallup, A. C., Miller, M. L., & Clark, A. B. (2010). The direction and range of ambient
temperature change inuences yawning in budgerigars (Melopsittacus undu-
latus). Journal of Comparative Psychology, 124(2), 133e138 .
Gallup, A. C., Miller, R. R., & Clark, A. B. (2011). Changes in ambient temperature
trigger yawning but not stretching in rats. Ethology, 117(2), 145e153.
Gallup, A. C., Schild, A. B., Ühlein, M. A., & Massen, J. J. M. (2014). An observational
study of behavioral contagion in ravens (Corvus corax). In Paper presented at the
51st Annual Meeting of the Animal Behavior Society Conference, Princeton Uni-
versity, Princeton, NJ.
Gallup, A. C., Swartwood, L., Militello, J., & Sackett, S. (2015). Experimental evidence
of contagious yawning in budgerigars (Melopsittacus undulatus). Animal
Cognition, 18(5), 1051e1058.
Gallup, A. C., Vasilyev, D., Anderson, N., & Kingstone, A. (2019). Contagious yawning
in virtual reality is affected by actual, but not simulated, social presence. Sci-
entic Reports, 9(1), 1e10.
Giganti, F., Hayes, M. J., Akilesh, M. R., & Salzarulo, P. (2002). Yawning and behavioral
states in premature infants. Developmental Psychobiology, 41(3), 289e296.
Giganti, F., & Zilli, I. (2011). The daily time course of contagious and spontaneous
yawning among humans. Journal of Ethology, 29(2), 215e219.
Giganti, F., Zilli, I., Aboudan, S., & Salzarulo, P. (2010). Sleep, sleepiness and yawning.
In O. Walusinski (Ed.), The mystery of yawning in physiology and disease (Vol. 28,
pp. 42e46). Basel: Karger.
Goodall, J. (1968). A preliminary report on expressive movements and commu-
nication in the Gombe stream chimpanzees. In P. C. Jay (Ed.), Primates: Stud ies
in adaptation and variability (pp. 313e374). New York: Holt Rinehart &
orecka-Bruzda, A., Fureix, C., Ouvrard, A., Bourjade, M., & Hausberger, M. (2016).
Investigating determinants of yawning in the domestic (Equus caballus) and
Przewalski (Equus ferus przewalskii) horses. Science of Nature, 103(9), 1e10.
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the
Panglossian paradigm: A critique of the adaptationist programme. Proceedings
of the Royal Society B: Biological Sciences, 205(1161), 581e598.
Greco, M., & Baenninger, R. (1991). Effects of yawning and related activities on skin
conductance and heart rate. Physiology &Behavior, 50(5), 1067e1069.
Guggisberg, A. G., Mathis, J., Herrmann, U. S., & Hess, C. W. (2007). The functional
relationship between yawning and vigilance. Behavioural Brain Research, 179(1),
Guggisberg, A. G., Mathis, J., Schnider, A., & Hess, C. W. (2010). Why do we yawn?
Neuroscience &Biobehavioral Reviews, 34(8), 1267e1276.
Hadidian, J. (1980). Yawning in an old world monkey, Macaca nigra (Primates:
Cercopithecidae). Behaviour,133e147.
Haker, H., Kawohl, W., Herwig, U., & R
ossler, W. (2013). Mirror neuron activity
during contagious yawning eAn fMRI study. Brain Imaging and Behavior, 7(1),
Harr, A. L., Gilbert, V. R., & Phillips, K. A. (2009). Do dogs (Canis familiaris) show
contagious yawning? Animal Cognition, 12,833e837.
Headland, T. N., & Greene, H. W. (2011). Hunteregatherers and other primates as
prey, predators, and competitors of snakes. Proceedings of the National Academy
of Sciences of the United States of America, 108(52), E1470eE1474.
Helt, M. S., Sorensen, T. M., Scheub, R. J., Nakhle, M. B., & Luddy, A. C. (2021). Patterns
of contagious yawning and itching differ amongst adults with autistic traits vs.
psychopathic traits. Frontiers in Psychology, 12, 645310.
Iki, S., & Kutsukake, N. (2021). Social bias affects vigilance contagion in Japanese
macaques. Animal Behaviour, 178,67e76.
Isbell, L. A. (2006). Snakes as agents of evolutionary change in primate brains.
Journal of Human Evolution, 51(1), 1e35.
Joly-Mascheroni, R. M., Senju, A., & Shepherd, A. J. (20 08). Dogs catch human yawns.
Biology Letters, 4(5), 446e448.
Kasturiratne, A., Wickremasinghe, A. R., de Silva, N., Gunawardena, N. K.,
Pathmeswaran, A., Premaratna, R., Savioli, L., Lalloo, D. G., & de Silva, H. J.
(2008). The global burden of snakebite: A literature analysis and modelling
based on regional estimates of envenoming and deaths. PLoS Medicine, 5(11),
Kasuya, Y., Murakami, T., Oshima, T., & Dohi, S. (2005). Does yawning represent a
transient arousal-shift during intravenous induction of general anesthesia?
Anesthesia &Analgesia, 101(2), 382e384.
Keverne, E. B., Leonard, R. A., Scruton, D. M., & Young, S. K. (1978). Visual monitoring
in social groups of talapoin monkeys (Miopithecus talapoin). Animal Behaviour,
26, 933e944.
Kotsoni, E., De Haan, M., & Johnson, M. H. (2001). Categorical perception of facial
expressions by 7-month-old infants. Perception, 30(9), 1115e112 5 .
Kubota, N., Amemiya, S., Yanagita, S., Nishijima, T., & Kita, I. (2014). Emotional stress
evoked by classical fear conditioning induces yawning behavior in rats.
Neuroscience Letters, 566,182e18 7.
LaBarbera, J., Izard, C., Vietze, P., & Parisi, S. (1976). Four- and six-month-old infants'
visual responses to joy, anger, and neutral expressions. Child Development, 47,
Landolt, H. P., Moser, S., Wiesen, H. G., Borbeley, A. A., & Dijk, D. J. (1995). Intra-
cranial temperature across 24 hour sleep wake cycles in humans. NeuroReport,
Langergraber, K., Mitani, J., & Vigilant, L. (2009). Kinship and social bonds in female
chimpanzees (Pan troglodytes). American Journal of Primatology, 71(10),
Leone, A., Ferrari, P. F., & Palagi, E. (2014). Different yawns, different functions?
Testing social hypotheses on spontaneous yawning in Theropithecus gelada.
Scientic Reports, 4(1), 1e9.
Lewis, L. S., Kano, F., Stevens, J. M., DuBois, J. G., Call, J., & Krupenye, C. (2021).
Bonobos and chimpanzees preferentially attend to familiar members of the
dominant sex. Animal Behaviour, 177,193e206.
Liang, A. C., Grace, J. K., Tompkins, E. M., & Anderson, D. J. (2015). Yawning, acute
stressors, and arousal reduction in Nazca booby adults and nestlings. Physiology
&Behavior, 140,38e43.
Luttenberger, E. (1975). On yawning in reptiles. Zeitschrift für Tierpsychologie, 37,
113 e137.
Madsen, E. A., & Persson, T. (2013). Contagious yawning in domestic dog puppies
(Canis lupus familiaris): The effect of ontogeny and emotional closeness on low-
level imitation in dogs. Animal Cognition, 16(2), 233e240.
Madsen, E. A., Persson, T., Sayehli, S., Lenninger, S., & Sonesson, G. (2013). Chim-
panzees show a developmental increase in susceptibility to contagious
yawning: A test of the effect of ontogeny and emotional closeness on yawn
contagion. PLoS One, 8(10), Article e76266.
Maestripieri, D., Schino, G., Aureli, F., & Troisi, A. (1992). A modest proposal:
Displacement activities as an indicator of emotions in primates. Animal
Behaviour, 44(5), 967e979.
Malavasi, R. (2014). Social modulation of yawning behavior in the domestic horse e
an exploratory analysis. In I. Estevez, X. Manteca, R. H. Marin, & X. Aver
os (Eds.),
Proceedings of the 48th International Conference of the International Society for
Applied Ethology, 29 July e2 August 2014, Vitoria-Gasteiz, Spain: Moving on (p.
240). Wageningen Academic.
Massen, J. J. M., Church, A. M., & Gallup, A. C. (2015). Auditory contagious yawning in
humans: An investigation into afliation and status effects. Frontiers in Psy-
chology, 6, 1735.
Massen, J. J. M., Dusch, K., Eldakar, O. T., & Gallup, A. C. (2014). A thermal window for
yawning in humans: Yawning as a brain cooling mechanism. Physiology &
Behavior, 130 ,145e14 8.
Massen, J. J. M., & Gallup, A. C. (2017). Why contagious yawning does not (yet)
equate to empathy. Neuroscience &Biobehavioral Reviews, 80,573e585.
Massen, J. J. M., Hartlieb, M., Martin, J. S., Leitgeb, E., Bugnyar, T., Hockl, J.,
Kocourek, M., Olkowicz, S., Osadnik, C., Verkleij, J. W., Zhang, Y., N
emec, P., &
Gallup, A. C. (2021). Brain size and neuron numbers drive differences in yawn
duration across mammals and birds. Communications Biology, 4(1), 1e10.
Massen, J. J. M., Maylor, E., Moulson, J. M., Muncer, A.-M., Taylor, L. A., Massen, J. J.,
Vermunt, D. A., & Sterck, E. H. (2012). Male yawning is more contagious than
female yawning among chimpanzees (Pan troglodytes). PLoS One, 7(7), Article
Massen, J. J. M.,
Slipogor, V., & Gallup, A. C. (2016). An observational investigation of
behavioral contagion in common marmosets (Callithrix jacchus): Indications for
contagious scent-marking. Frontiers in Psychology, 7,1190.
Matikainen, J., & Elo, H. (2008). Does yawning increase arousal through mechanical
stimulation of the carotid body? Medical Hypotheses, 70(3), 488e492.
Matsumura, S., & Okamoto, K. (1997). Factors affecting proximity among members
of a wild group of moor macaques during feeding, moving, and resting. Inter-
national Journal of Primatology, 18(6), 929e940.
Maynard Smith, J., & Harper, D. (2003). Animal signals. Oxford University Press.
A. C. Gallup / Animal Behaviour 187 (2022) 209e219 217
Melis, M. R., Argiolas, A., & Gessa, G. L. (1987). Apomorphine-induced penile erec-
tion and yawning: Site of action in brain. Brain Research, 415(1), 98e10 4.
Millen, A., & Anderson, J. R. (2011). Neither infants nor toddlers catch yawns from
their mothers. Biology Letters, 7(3), 440e442.
Miller, M. L., Gallup, A. C., Vogel, A. R., & Clark, A. B. (2010). Handling stress initially
inhibits, but then potentiates yawning in budgerigars (Melopsittacus undulatus).
Animal Behaviour, 80(4), 615e619.
Miller, M. L., Gallup, A. C., Vogel, A. R., & Clark, A. B. (2012). Auditory disturbances
promote temporal clustering of yawning and stretching in small groups of
budgerigars (Melopsittacus undulatus). Journal of Comparative Psychology, 126(3),
Miller, M. L., Gallup, A. C., Vogel, A. R., Vicario, S. M., & Clark, A. B. (2012). Evidence
for contagious behaviors in budgerigars (Melopsittacus undulatus): An obser-
vational study of yawning and stretching. Behavioural Processes, 89(3),
Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B.,
Dolan, R. J., & Frith, C. D. (2007). When fear is near: Threat imminence elicits
prefrontal-periaqueductal gray shifts in humans. Science, 317(5841),
Moyaho, A., Rivas-Zamudio, X., Ugarte, A., Eguibar, J. R., & Valencia, J. (2015). Smell
facilitates auditory contagious yawning in stranger rats. Animal Cognition, 18(1),
Moyaho, A., Urbina, A. F., Guzm
an, E. M., & Walusinski, O. (2017). Yawning: A cue
and a signal. Heliyon, 3(11), Article e00437.
Moyaho, A., & Valencia, J. (2002). Grooming and yawning trace adjustment to un-
familiar environments in laboratory SpragueeDawley rats (Rattus norvegicus).
Journal of Comparative Psychology, 116(3), 263e269.
Nahab, F. B., Hattori, N., Saad, Z. S., & Hallett, M. (2009). Contagious yawning and the
frontal lobe: An fMRI study. Human Brain Mapping, 30(5), 1744e1751.
Neilands, P., Claessens, S., Ren, I., Hassall, R., Bastos, A. P., & Taylor, A. H. (2020).
Contagious yawning is not a signal of empathy: No evidence of familiarity,
gender or prosociality biases in dogs. Proceedings of the Royal Society B: Bio-
logical Sciences, 287(1920), 20192236.
Nelson, J. T., McKinley, R. A., Golob, E. J., Warm, J. S., & Parasuraman, R. (2014).
Enhancing vigilance in operators with prefrontal cortex transcranial direct
current stimulation (tDCS). NeuroImage, 85, 909e917.
Norscia, I., Agostini, L., Moroni, A., Caselli, M., Micheletti-Cremasco, M., Vard
e, C., &
Palagi, E. (2021). Yawning is more contagious in pregnant than nulliparous
women. Human Nature, 32,301e325.
Norscia, I., Coco, E., Robino, C., Chierto, E., & Cordoni, G. (2021). Yawn contagion in
domestic pigs (Sus scrofa). Scientic Reports, 11(1), 1e12.
Norscia, I., & Palagi, E. (2011). Yawn contagion and empathy in Homo sapiens.PLoS
One, 6(12), Article e28472.
Norscia, I., Zanoli, A., Gamba, M., & Palagi, E. (2020). Auditory contagious yawning is
highest between friends and family members: Support to the emotional bias
hypothesis. Frontiers in Psychology, 11,442.
Olivier, B., Zethof, T., Pattij, T., van Boogaert, M., van Oorschot, R., Leahy, C.,
Oosting, R., Bouwknecht, A., Veening, J., van der Gugten, J., & Groenink, L.
(2003). Stress-induced hyperthermia and anxiety: Pharmacological validation.
European Journal of Pharmacology, 463(1), 117e132.
Palagi, E., Celeghin, A., Tamietto, M., Winkielman, P., & Norscia, I. (2020). The
neuroethology of spontaneous mimicry and emotional contagion in human and
non-human animals. Neuroscience &Biobehavioral Reviews, 111,149e165.
Palagi, E., Guill
en-Salazar, F., & Llamazares-Martín, C. (2019). Spontaneous yawning
and its potential functions in South American sea lions (Otaria avescens).
Scientic Reports, 9(1), 1e8.
Palagi, E., Leone, A., Mancini, G., & Ferrari, P. F. (2009). Contagious yawning in gelada
baboons as a possible expression of empathy. Proceedings of the National
Academy of Sciences of the United States of America, 106(46), 19262e19267.
Palagi, E., Norscia, I., & Cordoni, G. (2019). Lowland gorillas (Gorilla gorilla gorilla)
failed to respond to others' yawn: Experimental and naturalistic evidence.
Journal of Comparative Psychology, 133(3), 406.
Palagi, E., Norscia, I., & Demuru, E. (2014). Yawn contagion in humans and bonobos:
Emotional afnity matters more than species. PeerJ, 2,e519.
Parasuraman, R., Warm, J. S., & See, J. E. (1998). Brain systems of vigilance. In
R. Parasuraman (Ed.), The attentive brain (pp. 221e256). Cambridge, MA: MIT
Paukner, A., & Anderson, J. R. (2006). Video-induced yawning in stumptail ma-
caques (Macaca arctoides). Biology Letters, 2(1), 36e38.
Perry, S., Manson, J. H., Muniz, L., Gros-Louis, J., & Vigilant, L. (2008). Kin-biased
social behaviour in wild adult female white-faced capuchins, Cebus capucinus.
Animal Behaviour, 76(1), 187e199.
Platek, S. M., Critton, S. R., Myers, T. E., & Gallup, G. G., Jr. (20 03). Contagious
yawning: The role of self-awareness and mental state attribution. Cognitive
Brain Research, 17(2), 223e227.
Prochazkova, E., & Kret, M. E. (2017). Connecting minds and sharing emotions
through mimicry: A neurocognitive model of emotional contagion. Neurosci-
ence &Biobehavioral Reviews, 80,99e114 .
Provine, R. R. (1986). Yawning as a stereotyped action pattern and releasing stim-
ulus. Ethology, 72(2), 109e12 2.
Provine, R. R. (2005). Yawning: The yawn is primal, unstoppable and contagious,
revealing the evolutionary and neural basis of empathy and unconscious
behavior. American Scientist, 93(6), 532e539.
Provine, R. R., & Hamernik, H. B. (1986). Yawning: Effects of stimulus interest.
Bulletin of the Psychonomic Society, 24(6), 437e438.
Provine, R. R., Hamernik, H. B., & Curchack, B. C. (1987). Yawning: Relation to
sleeping and stretching in humans. Ethology, 76(2), 152e160.
Provine, R. R., Tate, B. C., & Geldmacher, L. L. (1987). Yawning: No effect of 3e5%
CO2, 100% O2, and exercise. Behavioral and Neural Biology, 48(3), 382e393.
Ramirez, V., Ryan, C. P., Eldakar, O. T., & Gallup, A. C. (2019). Manipulating neck tem-
perature alters contagious yawningin humans. Physiology &Behavior, 207,86e89.
Rasa, O. A. (1971). The causal factors and functions of yawning in M. chrysurus
(Pisces: Pomacentridae). Behaviour, 39,39e57.
Reddy, R. B., Krupenye, C., MacLean, E. L., & Hare, B. (2016). No evidence for con-
tagious yawning in lemurs. Animal Cognition, 19(5), 889e898.
Romero, T., Ito, M., Saito, A., & Hasegawa, T. (2014). Social modulation of contagious
yawning in wolves. PLoS One, 9(8), Article e105963.
Romero, T., Konno, A., & Hasegawa, T. (2013). Familiarity bias and physiological
responses in contagious yawning by dogs support link to empathy. PLoS One, 8,
Article e71365.
Roos, A., Lochner, C., Kidd, M., van Honk, J., Vythilingum, B., & Stein, D. J. (2012).
Selective attention to fearful faces during pregnancy. Progress in Neuro-
Psychopharmacology and Biological Psychiatry, 37(1), 76e80.
Rossman,Z. T.,Hart,B. L., Greco,B.J.,Young,D.,Padeld,C., Weidner, L.,Gates,J.,& Hart,L.A.
(2017). When yawning occurs in elephants. Frontiers in Veterinary Science, 4,22.
Rossman, Z. T., Padeld, C., Young, D., Hart, B. L., & Hart, L. A. (2020). Contagious
yawning in African elephants (Loxodonta africana): Responses to other ele-
phants and familiar humans. Frontiers in Veterinary Science, 7, 252.
Sato-Suzuki, I., Kita, I., Oguri, M., & Arita, H. (1998). Stereotyped yawning responses
induced by electrical and chemical stimulation of paraventricular nucleus of the
rat. Journal of Neurophysiology, 80(5), 2765e2775.
Sauer, E. F., & Sauer, E. M. (1967). Yawning and other maintenance activities in the
South African ostrich. Auk, 84(4), 571e587.
Schiller, F.(2002). Yawning? Journal of the History of the Neurosciences, 11(4),392e401.
Schino, G., & Aureli, F. (1989). Do men yawn more than women? Ethology and So-
ciobiology, 10(5), 375e378.
Schroth, G., & Klose, U. (1992). Cerebrospinal uid ow. II. Physiology of respiration
related pulsations. Neuroradiology, 35,10e15.
Schürmann, M., Hesse, M. D., Stephan, K. E., Saarela, M., Zilles, K., Hari, R., &
Fink, G. R. (2005). Yearning to yawn: The neural basis of contagious yawning.
NeuroImage, 24(4), 1260e1264.
Searcy, W. A., & Nowicki, S. (2010). The evolution of animal communication. Princeton
University Press.
Seki, Y., Sato-Suzuki, I., Kita, I., Oguri, M., & Arita, H. (2002). Yawning/cortical acti-
vation induced by microinjection of histamine into the paraventricular nucleus
of the rat. Behavioural Brain Research, 134(1e2), 75e82.
Shepherd, S. V., Deaner, R. O., & Platt, M. L. (2006). Social status gates social
attention in monkeys. Trends in Cognitive Sciences, 4,138e147.
Shoup-Knox, M. L., Gallup, A. C., Gallup, G., & McNay, E. C. (2010). Yawning and
stretching predict brain temperature changes in rats: Support for the thermo-
regulatory hypothesis. Frontiers in Evolutionary Neuroscience, 2,108.
Silva, K., Bessa, J., & de Sousa, L. (2012). Auditory contagious yawning in domestic
dogs (Canis familiaris): First evidence for social modulation. Animal Cognition,
Smith, E. O. (1999). Yawning: An evolutionary perspective. Human Evolution, 14(3),
Tan, J., Ariely, D., & Hare, B. (2017). Bonobos respond prosocially toward members of
other groups. Scientic Reports, 7(1), 1e11.
Tesfaye, Y., & Lal, S. (1990). Hazard of yawning. Canadian Medical Association Journal,
142(6), 533be533.
Troisi, A., Aureli, F., Schino, G., Rinaldi, F., & de Angelis, N. (1990). The inuence of
age, sex, and rank on yawning behavior in two species of macaques (Macaca
fascicularis and M. fuscata). Ethology, 86(4), 303e310.
Tsurumi, S., Kanazawa, S., & Yamaguchi, M. K. (2019). Infant brain activity in
response to yawning using functional near-infrared spectroscopy. Scientic
Reports, 9(1), 1e9.
Vick, S. J., & Paukner, A. (2010). Variation and context of yawns in captive chim-
panzees (Pan troglodytes). American Journal of Primatology, 72(3), 262e269.
de Vries, J. I., Visser, G. H., & Prechtl, H. F. (1982). The emergence of fetal behaviour. I.
Qualitative aspects. Early Human Development, 7(4), 301e322.
de Waal, F. B., & Preston, S. D. (2017). Mammalian empathy: Behavioural manifes-
tations and neural basis. Nature Reviews Neuroscience, 18(8), 498e509.
Walusinski, O. (2006). Yawning: Unsuspected avenue for a better understanding of
arousal and interoception. Medical Hypotheses, 67(1), 6e14.
Walusinski, O. (2014). How yawning switches the default-mode network to the
attentional network by activating the cerebrospinal uid ow. Clinical Anatomy,
27(2), 201e209.
Walusinski, O. (2018). Pathological yawning, laughing and crying. In
J. Bogousslavsky (Ed.), Neurologic-psychiatric syndromes in focus - Part I (Vol. 41,
pp. 40e49). Basel: Karger.
Wiley, R. H. (2006). Signal detection and animal communication. Advances in the
Study of Behavior, 36,217e247.
Wilkinson, A., Sebanz, N., Mandl, I., & Huber, L. (2011). No evidence of contagious
yawning in the red-footed tortoise Geochelone carbonaria.Current Zoology,
57(4), 477e484.
Wojczulanis-Jakubas, K., Plenzler, J., & Jakubas, D. (2019). Indications of contagious
behaviours in the southern elephant seal: An observational study. Behaviour,
156(1), 59e77.
Yonezawa, T., Sato, K., Uchida, M., Matsuki, N., & Yamazaki, A. (2017). Presence of
contagious yawning in sheep. Animal Science Journal, 88(1), 195e200.
A. C. Gallup / Animal Behaviour 187 (2022) 209e219218
Zannella, A., Norscia, I., Stanyon, R., & Palagi, E. (2015). Testing yawning hypotheses
in wild populations of two strepsirrhine species: Propithecus verreauxi and
Lemur catta.American Journal of Primatology, 77(11), 1207e1215.
Zannella, A., Stanyon, R., Maglieri, V., & Palagi, E. (2021). Not all yawns tell the same
story: The case of Tonkean macaques. American Journal of Primatology, 83(7),
Article e23263.
Zannella, A., Stanyon, R., & Palagi, E. (2017). Yawning and social styles: Different
functions in tolerant and despotic macaques (Macaca tonkeana and Macaca
fuscata). Journal of Comparative Psychology, 131(3), 179e188.
Zethof, T. J., Van Der Heyden, J. A., Tolboom, J. T., & Olivier, B. (1994). Stress-induced
hyperthermia in mice: A methodological study. Physiology &Behavior, 55(1),
Zilli, I., Giganti, F., & Salzarulo, P. (2007). Yawning in morning and evening types.
Physiology &Behavior, 91(2e3), 218e222.
Zilli, I., Giganti, F., & Uga, V. (2008). Yawning and subjective sleepiness in the elderly.
Journal of Sleep Research, 17(3), 303e308.
A. C. Gallup / Animal Behaviour 187 (2022) 209e219 219
... Spontaneous yawning (or a yawning-like morphological pattern) appears to be phylogenetically widespread across vertebrates (Baenninger 1987) including humans (Homo sapiens) and non-human primates (Provine 1986(Provine , 2012Anderson 2020). Among other functions (brain cooling, arousal, neurovascular circulation and behavioural state change: Guggisberg et al. 2011;Massen et al. 2014;Gallup 2022), spontaneous yawning under relaxed conditions appears to be related to the sleep-wake cycle (Provine 1986;Leone et al. 2014;Zannella et al. 2015). Therefore, individuals that share similar circadian rhythms and activity budgets may show a peak in yawning within the same time slot (Giganti and Zilli 2011;Zannella et al. 2015). ...
... Because-among others-spontaneous yawning is associated with the sleep-wake cycle (Gallup 2022) and indris are diurnal with synchronous behavioural activities (Pollock 1975), we expected spontaneous yawns in indris to be grouped in time (i.e. synchronised during the day) and primarily concentrated in the morning (Prediction 1). ...
... Indeed, studies in the wild allow for the measurement of ecologically valid responses, whereas experimental studies can deal with a greater set of controlled variables. Concerning indris, being difficult to captive breed the species due to its ecological requirements, further investigation in the wild may indeed reveal whether the phenomenon of yawn contagion can enhance individual vigilance and motor synchrony among individuals (Casetta et al. 2021;Gallup 2022). ...
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Contrary to spontaneous yawning, yawn contagion occurs when yawning in a subject (responder) is elicited by the yawns of others (triggers). Yawn contagion has been associated with inter-individual synchronisation, activity coordination and possibly emotional contagion, based on the perception–action mechanism. We collected data on yawn contagion and grooming and verified—for the first time—yawn contagion presence and modulating factors in a wild strepsirhine. Specifically, we considered the diurnal lemur Indri indri (inhabiting Maromizaha rainforest, eastern Madagascar), which lives in socially cohesive family units. We recorded 613 yawning events involving 28 individuals and found that yawn contagion was present in the indris (with the best predictor for an individual to yawn at a given time of day was observing another group member yawning) and that it was positively influenced by grooming levels (but not by the spatial distance) between trigger and responder. Age and sex had no significant relationship with yawn contagion likelihood. Because yawn contagion has been found in different mammalian species regardless of their phylogenetic closeness, this study, reporting the phenomenon in a lemur species with highly cohesive behavioural pattern and able to emit coordinated vocal displays, adds a valuable piece to the investigation of the pressures that may have favoured yawning as a (possibly emotional) communicative cue during evolution. Significance statement Yawn contagion is associated with inter-individual synchronisation and activity coordination. While this behaviour is often investigated in apes, its presence in lemurs is debated. Here, we explored presence and modulating factors of yawn contagion in Indri indri, a critically endangered primate living in small family units where individuals show coordinated circadian rhythms and a highly cohesive behavioural pattern. We first demonstrated the presence of yawn contagion in wild indris where, in line with the high degree of behavioural synchrony showed by the individuals within a group, it may possibly indicate a transmission of physiological states. We also demonstrated the association of contagion with grooming rates, but not with the spatial proximity between triggers and responders, nor with their sex and age, pointing at social closeness as the most likely modulating factor.
... ostriches, Struthio camelus australis, Sauer and Sauer 1967;human, Provine 2005; red hill salamanders, Phaeognathus hubrichti, Bakkegard 2017; South American sea lions, Otaria flavescens, Palagi et al. 2019a; African lions, Panthera leo, Casetta et al. 2021;dugongs, Dugong dugon, Enokizu et al. 2022; bottlenose dolphins, Tursiops truncatus, Enokizu et al. 2021;non-human primates, Zannella et al. 2021). In this context, yawning increases alertness, thus making subjects able to adjust their behaviour in response to sudden and unexpected situations (Provine 2005;Gallup 2022). Spontaneous yawning also varies according to the stimuli the subject receives from its social environment (Greco et al. 1993;Deputte 1994;Baenninger 1997;Provine 1997;Guggisberg et al. 2010). ...
... In addition to the physiological functions, scholars have long hypothesised social functions for yawning (Deputte 1994;Guggisberg et al. 2010;Leone et al. 2014;Moyaho et al. 2017;Gallup 2022). The physiological underpinnings and the social aspects of the yawning phenomenon are often studied separately, even though they are strongly interconnected. ...
... Detecting yawns from conspecifics can elicit overt behavioural changes, such as yawn contagion, which is a reflexive matching action occurring when others' yawns trigger the same pattern in the observers (Provine 1986(Provine , 2005Palagi et al. 2009;Guggisberg et al. 2010). Being more evolutionary recent than spontaneous yawning, contagious yawning can be observed in those social species that show a high level of cohesion, social tolerance and cooperation (geladas, Theropithecus gelada; bonobos, Pan paniscus; lions, Panthera leo; see Palagi et al. 2020 andGallup 2022 for an extensive review). For example, yawn contagion has not been found in lowland gorillas (Gorilla gorilla gorilla), a social species whose group formation relies more on spatial proximity than on social affiliation (Palagi et al. 2019b). ...
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Yawning is a complex behaviour linked to several physiological (e.g. drowsiness, arousal, thermoregulation) and social phenomena (e.g. yawn contagion). Being yawning an evolutionary well-conserved, fixed action pattern widespread in vertebrates, it is a valuable candidate to test hypotheses on its potential functions across the different taxa. The spotted hyaena (Crocuta crocuta), the most social and cooperative species of the Hyaenidae family, is a good model to test hypotheses on yawning correlates and significances. Through an accurate sequential analysis performed on a group of wild hyaenas, we found that yawning mainly occurred during an imminent behavioural state changing in both juveniles and adults and that seeing others’ yawn elicited a mirror response in the receiver, thus demonstrating that yawn contagion is present in this species. These results taken together suggest that yawning is linked to a behavioural state change of the yawner and that such change is caught by the observers that engage in a motor resonance phenomenon, yawn contagion, possibly effective in anticipating yawners’ motor actions. Although additional data are necessary to verify whether yawn contagion translates into subsequent motor convergence and alignment, our data suggest that both spontaneous and contagious yawning can be fundamental building blocks on the basis of animal synchronisation in highly social and cooperative species. Significant statement Yawning is pervasive in many animal species, including humans. It is considered as a polyfunctional cue that has a role in regulating social interactions. While several studies focussed on yawning functions in primates, a little amount of effort was devoted to exploring this behaviour in social carnivores. We monitored a group of wild spotted hyaenas (Crocuta crocuta), which is one of the most cooperative carnivore species. In both immature and adult subjects, we found that a subject frequently changed its behavioural state after spontaneously yawning and that seeing others’ yawn elicited a mirror response in the observer. Although additional data are necessary to verify whether yawn contagion translates into subsequent motor convergence and alignment, our data suggest that both spontaneous and contagious yawning can be fundamental building blocks on the basis of animal synchronisation in highly social and cooperative species.
... Many expressions serve the particular situation in which they occur. For instance, one type of bird species yawns when in danger (Gallup, 2022). Because yawning cools down the brain and makes the bird more alert, this benefits all individuals in the group being in the same dangerous situation, so the overall yawning rate increases (Gallup, 2022). ...
... For instance, one type of bird species yawns when in danger (Gallup, 2022). Because yawning cools down the brain and makes the bird more alert, this benefits all individuals in the group being in the same dangerous situation, so the overall yawning rate increases (Gallup, 2022). Human research also shows that direct benefits may be at play. ...
In their "social contextual view" of emotional mimicry, authors Hess and Fischer (2022) put forward emotional mimicry as a social regulator, considering it a social act, bound to certain affiliative contexts or goals. In this commentary, we argue that the core function of mimicry is to ease predicting conspecifics' behaviours and the environment, and that as a consequence, this often smoothens social interactions. Accordingly, we make three main points. First, we argue that there is no good reason to believe that the mimicry of negative expressions is fundamentally different than the mimicry of positive or ambiguous or autonomic expressions. Second, we give examples of empirical evidence that mimicry is not always a social act. Third, we show that mimicry has primary benefits for the mimicker. As such, we will briefly summarise and elaborate on the relevant findings in these respects, and propose a comparative, multi-method and ecologically valid approach which can explain the multifaceted character of the phenomenon.
... Contagious yawning is shown to have a strong relationship with social stimuli, such as facial recognition, auditory senses, and empathy [5]; [6]; [7]. On the other hand, contagious yawning is also believed to share the same physiological effect as spontaneous yawning [8]. Thus, illuminating the functions of spontaneous yawning appears to be more essential than contagious yawning. ...
... The change in mental stress levels is indispensable with sleepiness and brain temperature change. Some scientists argue that stress is the expanding hypothesis of other hypotheses, such as brain cooling, and the evidence that supports the stress hypothesis will have similar effects on other hypotheses [8]. Yet, since all hypotheses could not eliminate the confounding factors, the important next step is to experimentally test which one is contributing the most to yawning. ...
Conference Paper
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... The overt and reflexive matching of behaviors among conspecifics, also referred to as behavioral contagion [1], is common among social species and could provide fitness advantages to group members [2]. In particular, contagious behaviors may serve important functions in synchronizing activity patterns and facilitating collective vigilance within groups [3][4][5]. Although the study of contagious behaviors has focused primarily on mammalian species [6][7][8][9][10], a number of studies have also found evidence for behavioral contagion among birds [11][12][13][14][15][16]. ...
... The absence of yawn and stretch contagion in ravens is also in contrast to observational and experimental studies in budgerigars [36,37]. However, potential comparative differences in these responses are to be expected, based on ecological factors and evolutionary history [5]. While ravens are highly gregarious and possess sophisticated social cognition [38,39,52], they live in much smaller groups composed of pair bonds and display less collective behavior in flocking, compared to budgerigars [71]. ...
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The overt and reflexive matching of behaviors among conspecifics has been observed in a growing number of social vertebrates, including avian species. In general, behavioral contagion—such as the spread of yawning—may serve important functions in group synchronization and vigilance behavior. Here, we performed an exploratory study to investigate yawn contagion among 10 captive juvenile ravens (Corvus corax), across two groups. Using observational methods, we also examined the contagiousness of three other distinct behaviors: stretching, scratching, and shaking. A total of 44 20 min observations were made across both groups, including 28 in the morning and 16 in the afternoon. The time and occurrence of all the behaviors from each bird were coded, and the temporal pattern of each behavior across both groups was then analyzed to assess the degree of social contagion. Overall, we found no evidence for contagious yawning, stretching, scratching, or shaking. However, yawns were relatively infrequent per observation (0.052 ± 0.076 yawns/bird) and thus experimental methods should be used to support this finding.
... Built atop these primitive functions, yawning has taken on derived social features [17,18]. In particular, the reflexive tendency to yawn following the detection of yawns in others, i.e., contagious yawning, is a well-documented phenomenon that may serve to enhance vigilance and synchronization in groups [19]. Distinct from physiologically triggered yawns, which are ubiquitous in vertebrates, there is a great deal of variation across species when it comes to the tendency to yawn contagiously [20][21][22][23]. ...
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Contagious yawning, or the reflexive tendency to yawn following the detection of yawning in others, is well-documented among humans and a growing number of social vertebrates. While the most common form of yawn contagion occurs between conspecifics, some non-human animals in captivity have been reported to yawn in response to yawns from human handlers/caregivers. The current research sought to provide the first formal investigation of whether people yawn contagiously in response to yawns from non-human animals. In addition, this study aimed to test whether this response was modulated by phylogenetic relatedness and domestication/social closeness. A total of 296 participants from Amazon Mechanical Turk self-reported on their yawning behavior following exposure to a (1) control (non-yawning) condition or a compilation of yawning stimuli either from (2) fish, (3) amphibians, (4) reptiles, (5) birds, (6) non-primate mammals, (7) apes, or (8) domesticated cats and dogs. The results provide strong support for interspecific yawn contagion. However, neither the propensity to yawn (binary) nor total yawn frequency varied significantly across interspecific conditions. Overall, these findings suggest that the mechanisms governing yawn contagion can be activated by varied forms of yawning stimuli, including those from distantly related and unfamiliar species.
... Although this behavior can be observed across the day, often in 6-s intervals, the majority of yawning events occur shortly after waking in the morning and prior to sleep onset in the evening (Baenninger et al., 1996;Gallup et al., 2016;Zilli et al., 2007). Yawning is therefore typically associated with sleepiness and fatigue (Provine et al., 1987) and appears to function in promoting state change, cortical arousal, and thermoregulation (Gallup, 2022). ...
Despite presenting several physiological and social benefits, yawning remains a highly stigmatized behavior across various cultures. Given evidence for an association between illness and the proclivity to yawn, it could be possible that yawning provides a heuristic cue to disease transmission between conspecifics. This aversion to yawning could thus serve as a disease avoidance strategy. The current study identified how individual differences in disease avoidance motivations could foster stigmatization of yawning. Participants completed personality inventories, including those related to disease avoidance and disgust, while indicating their attitudes toward various bodily functions. Individual differences in germ aversion and pathogen disgust were particularly associated with stigmatization of yawning, such that higher levels of these traits fostered greater aversion toward yawning. These data provide initial evidence for how fundamental social motives can facilitate reactions to involuntary behaviors.
... In particular, they suggest that, by repositioning the muscles around the airway, yawning evolved to secure long-term oxygenation. Given the growing appreciation for the evolutionary significance of yawning [2], research uncovering new potential function(s) of this motor action pattern is of clear importance. Doelman and Rijken indeed provide a nice overview, including very detailed and useful visualizations, of the physics of a yawn, and as such their paper could function as a reference work. ...