- I expect many people to yawn as they read
this editorial. Not because they are bored
(although some might be), but because even just
reading about the topic I am going to discuss,
yawning, can often cause us to yawn. Many people
also yawn when they see somebody else yawning
(so-called contagious yawning), sometimes even
if that "somebody" belongs to another species.
Many primatologists working in laboratories and
the Þeld have described yawning in their
study groups, along with associated activities
and contexts, but fewer have explicitly
addressed possible functions of this behaviour
or its underlying mechanisms and development.
Here, I review some of the experimental and
observational research that has been done on
yawning and contagious yawning in primates,
human and nonhuman, and to a lesser extent in
other species. I also present a detailed case
study of yawning in one primate individual:
myself.
-
-Anderson JR,
Wunderlich D Food-reinforced yawning in
Macaca tonkeana American Journal of Primatology
1988;16:165-169
- -Anderson
JR, Myowa-Yamakoshi M, Matsuzawa T.
Contagious yawning in chimpanzees The Royal
Society Biology Proc R Soc Lond B Biol Sci
2004;271 Suppl 6:S468-470
- -Anderson
JR et al Psychological influences on yawning
in children Current
Psychology Letters Behaviour, brain,
cognition 2003;2(11)
- -Anderson JR,
Matsuzawa T Yawning, an opening into empathy
in Cognitive Development in Chimpanzees.
Springer 2006:233-245
- First, a few introductory comments about
yawning, a ubiquitous behaviour among
vertebrates, recorded in many aquatic,
terrestrial and avian species (Baenninger 1987,
1997; Walusinski 2010a). Almost everyone can
recognize the act of yawning: a typical human
yawn starts with the mouth opening and a deep
inhalation that can last several seconds; if the
yawner is sitting, the neck may stretch and the
head tilt back with the mouth opening widely
until the end of the inhalation (the acme of the
yawn); the head then returns to its normal
position during a shorter exhalation and the
mouth closes. Some people vocalize during the
exhalation phase. The average yawn lasts around
6 s (Provine 1986).
-
-
- Although most people might notice changes in
inner ear pressure and their eyes watering when
they yawn, most are unaware of the myriad
neurological, physiological, and neurochemical
changes that accompany yawning, a_ecting the
cardiovascular and pulmonary systems, the brain,
and eye pressure, among others (Corey et al.
2012; Krestel et al. 2018). Many people might
also be surprised at the overall lack of
consensus among scientists about why yawning
originally evolved and what its primary
function(s) might be. Research on yawning often
throws up unexpected Þndings, such as
yawning being largely una_ected by elevated CO2
or low levels of O2 when concentrations of these
gases were experimentally manipulated (Provine
et al. 1987a, b). This Þnding, along with
fetuses yawning despite being in a
þuid-Þlled environment, rules out
any simple relationship between oxygenation and
yawning (Walusinski 2010b). One recent
hypothesis that has been gathering empirical
support focuses on the thermoregulatory e_ects
of yawning; more speciÞcally: yawning can
reduce cortical brain temperature (Gallup and
Gallup 2007; Gallup and Eldakar 2013; Massen et
al. 2014; Eguibar et al. 2017). The literature
on the ontogeny and phylogeny of yawning leaves
open the possibility of di_erent functions at
di_erent life stages or in di_erent species.
Some examples of this literature are described
below.
-
-
- From seeing yawns to counting
yawns
-
- One morning in the mid 1980s, as I walked
toward the captive group of capuchin monkeys
that I was then studying, I noticed a young
adult male Tonkean macaque in a nearby
enclosure. He was yawning frequently and looking
toward a large outdoor park about 25 m away. I
knew that this male should be in the park, in
the group in which he was born and grew up, but
earlier that morning he had escaped, yet again.
A caretaker had lured him with fruit into the
enclosure where he now was and where he would
stay until it was decided what to do with him.
The young male's rapid rate of yawning is what
had especially caught my attention. So, in an
example of cross-species gaze following (before
it became a research topic), I turned around to
see what he was looking at. There it was: the
dominant adult male of the group, in a tree in
the park, yawning back at the escapee. Those
þashes of long, white canine teeth (Fig.
1) as the two males yawned back and forth at
each other impressed me. They clearly also
impress monkeys: the visual scanpaths of rhesus
monkeys presented with pictures of adult males
either yawning or open-mouth threatening
revealed frequent Þrst saccades to the
canines in the yawning pictures; open-mouth
threats elicited less speciÞc saccades to
the mouth area (Gothard et al. 2004).
-
- It proved surprisingly easy to increase
these monkeys' rates of yawning with positive
reinforcement (Louboungou and Anderson 1987); by
contrast, another natural behaviour, namely the
"protruded lips" facial expression, proved
extremely resistant to conditioning in the same
study. In baseline sessions each male yawned
fewer than 20 times, but in reinforcement
sessions this rose to 60-70 and 80-150 times,
and during extinction sessions their yawning
rates fell back to baseline levels. The yawns
they produced during reinforcement sessions
appeared to be authentic, full yawns, including
eyes closed and head tilted head back during the
climactic phase (or acme). Furthermore, the
males tried to make themselves yawn as humans
sometimes do, by opening the mouth and inhaling
deeply; sometimes this triggered a yawn,
sometimes the attempt was abandoned. A follow-up
study with two male Tonkean macaques (one was
the escapee at the origin of the project)
conÞrmed the conditionability of yawning.
After establishing increased yawning rates with
continuous reinforcement as before, we
introduced a Þxed ratio 3 schedule in
which a reward was given only after three yawns
were produced; these Þxed ratio 3 schedule
sessions produced peak yawn rates in both males
(Anderson and Wunderlich 1988). Finally, the
Tonkean macaque males also showed clear examples
of spontaneous recovery: short-lived resurgences
of yawning at the start of each new extinction
session.
-
- Together, these experiments indicated that
adult male macaques have some degree of
voluntary control of their yawning, which can be
a_ected by reinforcement schedules similar to
many other behaviors. These findings nicely
complemented other descriptions in the
literature that suggested purposeful expression
and withholding of yawning in some primates; for
example, in wild baboons: "males with the best
canines displayed them most often to other
males" (Packer 1979, p. 42). Similar to another
phylogenetically old behaviour that originally
evolved for a di_erent function, namely
self-scratching (Diezinger and Anderson 1986),
in some primate species the physiological
reþex of yawning appears to have been
coopted into the communicatory repertoire, with
a role for learning as well as physiological
triggers. Because they have some degree of
control over the production of yawns, adult
males can conceivably use their yawning
facultatively, depending on their social status,
physical condition, and the context.
-
 -
- Contagious yawning in human
children
-
- At around the same time as we were trying to
condition natural behaviors (facial expressions,
scratching, yawning) in various primate species
[see references above, Anderson et al.
(1990) and Mitchell and Anderson (1993)],
Robert Provine's (1986,1989)
experimental-ethological approach to yawning in
humans brought another perspective and fresh
ideas. His use of videos of yawns to investigate
releasing stimuli and mechanisms of contagious
yawning stimulated new questions:
- 1. Why had contagious yawning never been
reported in any nonhuman primates? (Does it
exist in them or, as
- was widely held, is it a uniquely human
phenomenon?)
- 2. Why not try to use video stimuli to
investigate contagious yawning in nonhuman
primates, and possibly
- other species?
-
- As I scoured the human and animal literature
in search of relevant information, another issue
became apparent: the absence of any quantitative
information or controlled studies about
contagious yawning in human infants and young
children. Based on observations of his own
children, Piaget (1951) had suggested that
infants in their second year of life might yawn
if they saw somebody else yawn, but I could
Þnd no systematic studies or normative
data on the development of contagious yawning.
So, inspired by Provine (1986,1989), to
investigate the development of this behaviour we
ran the following study. We showed 87 children
aged between 2 and 11 years a video of an adult
chatting and looking toward the camera, and
stopping to yawn approximately every 10 s. As a
control we used an identical video except that
smiles replaced the yawns. An observer
unobtrusively recorded any yawns by the children
as they watched the videos and for 5 min after
they returned to their playgroup or
classroom.
-
- What we found was an unexpected yawning gap
in development (Anderson and Meno 2003). No
child below the age of 5 years yawned during the
yawn video or afterwards, whereas children in
each age group from 5 to 11 years yawned at
least once, with 50% or more of children aged 9,
10, and 11 years doing so. In another phase of
the study, children either listened to
(preschoolers and young school- children) or
read (older children) a story during which "Mr.
Lazy" yawned 10 times, and another story in
which "Mr. Happy" smiled 10 times. The yawning
story elicited no yawns in preschoolers or 5
years old, and in only a few 6 years old,
whereas most children aged 7 years or more
yawned at least once while reading the story or
shortly after- wards. In summary, this study
showed the e_ectiveness of yawn videos for
eliciting contagious yawning in older children,
along with reading or thinking about yawning
(Provine 1986,1989; Baenninger and Greco 1991).
It also established that children reached
adult-like susceptibility to contagious yawning
by 9&endash;11 years of age. Most striking,
however, was the discovery that children younger
than 5 years appeared largely immune to the
contagious e_ects of yawning, despite the
occurrence of spontaneous yawns in toddlers,
infants, newborns, and even fetuses (Giganti and
Salzarulo 2010; Walusinski 2010b).
-
- In a second study in young children (Millen
and Anderson 2011), we focused on the identity
of the yawning model. Our reasoning was that the
unfamiliarity of the model in the videos used by
Anderson and Meno (2003) might have somehow
inhibited yawning in younger children, and that
perhaps yawns by mothers, who are highly
familiar to and socially bonded with their
infants, would be more e_ective yawn- releasing
stimuli. First, we asked a small group of
mothers to keep a log of the occurrence, time
and context every time they saw their infant
yawn (the infants' ages ranged from 6 to 34
months), for a 1-week period. Although we made
no speciÞc request, we expected the
mothers to report any occurrences of contagious
yawning. But none of them did; their data
indicated infant yawning peaks in the morning
and during daytime nap periods, especially after
waking up and around mealtimes, but zero
instances of contagious yawning, either from
mother to infant or vice versa.
-
- The second part of the study by Millen and
Anderson (2011) consisted of a video
presentation experiment. Each infant (n = 22;
mean age, 23.7 months) sat on their mother's lap
and watched as still images of babies and
animals yawning were projected onto a
þat-screen color monitor. At random
intervals during the presentation a silent,
color video clip of the mother yawning appeared;
this happened Þve times during each
presentation. A control stimulus set consisting
of baby smile and animal "smile" pictures
interspersed with videos of the mother smiling
was also presented. Each child was observed for
5 min before, during, and 5 min after each
presentation. We found that no children yawned
during the smile presentation, and only two did
so afterwards. More importantly, although 77% of
adults who watched one of the yawn presentations
yawned during or within 5 min of watching it,
only three of the 23 children did so: two during
the presentation (each to an animal picture),
and one post-presentation. These data reinforced
our earlier conclusion that, compared to older
children and adults, infants and preschool
children are markedly less susceptible to
contagious yawning; they do not even catch yawns
from their mothers.
-
- Contagious yawning has recently become quite
a popular research topic in developmental
psychology. The literature features studies that
compare susceptibility in typically developing
children and children with autistic spectrum
disorder (e.g., Senju et al. 2007; Mariscal et
al. 2019), and attempts to facilitate contagious
yawning in younger children, for example, by
using live models instead of video (Helt et al.
2010) or by ensuring that children pay su_cient
attention to the model's eyes (Senju et al.
2009; Hoogenhout et al. 2013; Usui et al. 2013).
A recent study using preferential looking and
functional near-infrared spectroscopy found that
infants as young as 3 months, who do not show
contagious yawning, clearly distinguished
between yawn and non-yawn videos (Tsurumi et al.
2019). This suggests that, in human infants, the
neural requisites for detecting yawns are
already in place, ahead of the emergence of
contagious yawning. Why this should be, and
other unknowns about the development of this
behaviour, may become less puzzling as research
continues in what is currently a vibrant
Þeld.
-
 -
- Experimental studies of contagious
yawning in chimpanzees and other
primates
-
- Returning to those earlier questions about
why nobody had ever described contagious yawning
in any nonhuman species and whether video
stimuli could be used to investigate this
phenomenon in primates, Kyoto University's
Primate Research Institute was an ideal place to
try to answer at least the second one. There,
chimpanzees living in a large and complex,
semi-naturalistic environment could be invited
to temporarily leave their group and come into a
familiar laboratory where they could be tested
in a relaxed atmosphere (Matsuzawa 2020). For
our study (Anderson et al. 2004), "being tested"
simply meant being given the opportunity to
watch video clips of chimpanzees. On o_er were
four videos showing several examples of either
familiar or unfamiliar chimpanzees yawning, or
moving their mouths but not yawning. Six adult
females of the group participated (three with
their 3-year-old infants), and they watched each
video four times (each lasted 3 min)
interspersed with 5-min distraction periods
between each video. Our question was simple:
would yawn videos elicit yawns in the chimpanzee
observers? (Fig. 2).
-
- Counts of the adult chimpanzees' rates of
yawning during the test sessions showed an
average of 4.7 yawns during and after the
control videos, compared to 10 during and after
the yawn videos, with no e_ect of familiarity of
the models. Although the di_erence was not
signiÞcant at the group level, it was
highly signiÞcant for two of the females.
We also noted that, despite exposure to yawns by
their mothers and the videos, none of the three
infants yawned during any of the sessions. This
study thus revealed that our nearest
evolutionary neighbors are susceptible to
contagious yawning, and that video is an
e_ective tool for comparative studies of the
phenomenon. Furthermore, young chimpanzees
appeared to resemble young humans in their
apparent immunity to the contagion e_ect.
Linking our Þndings to the literature, we
speculated that individual and species
differences in contagious yawning might be
related to other socio-cognitive and
socio-emotional capacities, including
self-recognition and empathy [see Anderson
and Matsuzawa (2006) for additional analyses and
discussion of this study].
-
- Studies of contagious yawning in chimpanzees
and other primates have þourished since
Anderson et al. (2004). Several authors have
reported induced yawning in chimpanzees and
bonobos in response to videos of yawning, with
manipulations of video content used to
investigate possible sex di_erences and
psychological factors, including a_liation and
empathy (Amici et al. 2014; Campbell and de Waal
2011, 2014; Massen et al. 2012; Tan et al.
2017); chimpanzees were even shown to catch
yawns from computer- animated chimpanzees
(Campbell et al. 2009). Two studies have
reported no contagious yawning in response to
conspeciÞc yawn videos in gorillas (Amici
et al. 2014; Palagi et al. 2019), which is
interesting in view of the more limited evidence
for mirror self-recognition in gorillas compared
to chimpanzees (Anderson and Gallup 2015). One
study that focused on young chimpanzees
corroborated our original observation that
3-year-old chimpanzees did not yawn when exposed
to yawns. Madsen et al. (2013) presented
orphaned, sanctuary-housed chimpanzees with a
live human model yawning; the chimpanzees were
divided into infants (mean age 2.8 years) and
juveniles (mean age 7.0 years). Only the older
group showed increased yawning after seeing the
human yawn, and they did not imitate simple
opening and closing of the mouth. The authors
concluded that the infant chimpanzees [like
those in Anderson et al. (2004)] appeared
immune to the contagiousness of yawning.
-
- To my knowledge, there is only one study of
video-inþuenced yawning in monkeys.
Paukner and Anderson (2006) reported that a
group of stump-tailed macaques yawned more
frequently during and after presentation of a
video of conspeciÞc yawns than a video of
non-yawn mouth movements (e.g., chewing).
Unfortunately, however, six of the 10 yawns on
video were by an adult male. As the monkeys also
showed increased self-scratching in response to
the yawn video, it seems likely that their
anxiety levels were raised by the sight of an
adult male yawning; yawning itself can also be
elicited by nervousness or anxiety. Although
some authors cite Paukner and Anderson (2006) as
evidence of contagious yawning in stump-tailed
macaques, we in fact cautioned against drawing
such a conclusion; the question should be
revisited.
-
- One video study has been done with lemurs.
After conÞrming that both ring-tailed and
ru_ed lemurs responded di_erently to videos
showing a positive scene (a familiar caretaker
presenting food) and a negative scene (a
potential predator walking), Reddy et al. (2016)
presented videos of conspeciÞcs yawning
and control videos to individual lemurs, and
later to four groups of lemurs. Most of the
lemurs did not yawn at all during the video
sessions, regardless of whether the lemur in the
video was familiar to them or a stranger. The
authors discussed possible scenarios for the
emergence of contagious yawning in primate
evolution, but also pointed out that visual
stimulation on its own (as in their videos)
might not be salient enough to trigger any e_ect
in the prosimians. By contrast, a reliable
trigger for one captive 3-year-old male
ring-tailed lemur was a human opening his mouth
wide and slowly tilting his head back (as if
yawning), whereas the same head movement by the
human but without him opening his mouth did not
elicit a response from the lemur (Roeder et al.
1994). The authors emphasized that the lemur
never received rewards for yawning and in fact
appeared to have little control over his
elicited yawns; the human's simulated yawns
acted like a supernormal stimulus. The same
authors also described more yawning by female
ring-tailed lemurs than males during
presentations of an unfamiliar adult female to a
small group, and related this observation to
female dominance in these prosimians.
-
- Contagious yawning in other
species?
-
- A report of no evidence of contagious
yawning in red-footed tortoises (Wilkinson et
al. 2011) led to the award of an Ig Nobel prize.
Two types of yawn stimuli were presented to
observer tortoises: from live demonstrators that
had been trained to yawn, and from video clips
of demonstrators yawning spontaneously; both
types gave negative results. As well as showing
that tortoises appear to lack mechanisms that
underly contagious yawning in other species,
Wilkinson et al. (2011) succeeded in using
successive approximation and positive
reinforcement to shape yawns or yawn-like
responses in a reptile.
-
- The Þrst evidence for contagious
yawning in an avian species came from
observations of a captive þock of
budgerigars (Miller et al. 2011). The overall
frequency of yawning was low (1-3 yawns/bird per
observation hour), but a yawn by one bird was
likely to be followed within 40 s by another
bird yawning, sometimes leading to "a cascade of
yawns among the others" (Miller et al. 2011, p.
269). This phenomenon was conÞrmed
experimentally by Gallup et al. (2015).
Individual birds were removed from their group
and placed in a cage adjacent to another cage
containing a familiar or an unfamiliar bird,
sometimes with an opaque visual barrier
separating the two cages. SigniÞcantly
more yawns occurred within 5 min of yawns by the
adjacent bird when it was visible than in the
control condition, with no e_ect of familiarity.
In a second experiment, a video of a single
conspeciÞc yawning elicited yawning by
observer budgerigars without also eliciting
signs of anxiety [remember that this was a
confounding factor in the study of stump-tailed
macaques by Paukner and Anderson (2006)
discussed above]. For Gallup et al. (2015),
the large size of natural þocks of
budgerigars might be a reason for the lack of
any e_ect of familiarity on contagious yawning,
in contrast to the ingroup e_ect reported in
chimpanzees, for example (Campbell and de Waal
2011). Further observational and experimental
studies on avian species should be worth waiting
for.
-
- A line of laboratory rats has been bred for
high spontaneous yawning rates, and they have
been shown to respond with contagious yawning
especially to auditory cues of yawning
associated with olfactory cues from strangers
(Moyaho et al. 2015). Auditory cues are known to
sometimes trigger contagious yawning in humans
(Massen et al. 2015), but unlike in the rats
studied by Moyaho et al. (2015), in primates
(including humans, see below), social closeness
is often reported to facilitate contagious
yawning. This study in rodents highlights the
likelihood of di_erent underlying mechanisms and
functions of yawning and contagious yawning
across species.
-
- In view of their multiple synchronized
activities within herds and their facial
recognition abilities, sheep were tested for
contagious yawning by Yonezawa et al. (2017).
Twelve castrated sheep were individually
separated from their herd and observed with a
familiar herd-mate in an adjacent stall, with
and without an opaque divider between them.
Eight of 72 yawns recorded for the subjects when
the adjacent sheep's face was visible occurred
within 1 min of the latter yawning, compared to
none of 42 yawns when the latter was shielded
from the subjects' view. However, six sheep
exposed to a video of a sheep yawning showed no
contagious yawning. The authors suggested that
research along these lines might be valuable for
animal welfare practices. Recent studies of
other mammals have presented data on social
correlates of yawning, but with no mention of
contagion [horses (Górecka-Bruzda et
al. 2016); sea lions (Palagi et al.
2019)].
-
- Several studies have been published on
yawning and contagious yawning in dogs.
Joly-Mascheroni et al. (2008) reported that 21
of 29 domestic dogs yawned when an unfamiliar
human sitting in front of them repeatedly yawned
(or more accurately, simulated yawns), but not
when the human made non-yawn mouth movements.
Subsequent studies a_rming contagious yawning in
dogs have examined the e_ectiveness of auditory
cues only and familiarity [yawns sounds were
e_ective, especially if the yawner was the dog's
owner (Silva et al. 2012)], ontogeny
[puppies younger than 7 months did not show
the behaviour (Madsen and Pearson 2013)],
and have used physiological measures to try to
clarify links between contagious yawning,
empathy, and arousal (Romero et al. 2013;
Buttner and Strasser 2014). However, both Harr
et al. (2009) and O'Hara and Reeve (2011)
reported no convincing evidence of contagious
yawning in dogs, and a recent study that set out
to investigate whether oxytocin might a_ect
contagious yawning in dogs also found no
convincing evidence for the phenomenon (Kis et
al. 2020). A reanalysis of results from some of
the earlier dog studies led to the conclusion
that contagious yawning is indeed present but
that no link with empathy has been established
(Nielands et al. 2020). This latter conclusion
was supported by an experiment in which dogs
were no more likely to catch yawns from a human
who had just behaved prosocially towards them
than from an antisocial human. Clearly, more
research is required to resolve various issues
surrounding contagious yawning in dogs. Finally,
in another canid, wolves, an observational study
of a captive pack revealed evidence of
contagious yawning (i.e., yawns occurring within
3 min of a Þrst wolf yawning), especially
between close social partners (Romero et al.
2014). This Þnding was taken as further
support of a relationship between contagious
yawning and empathy. [See Massen and Gallup
(2017) for a critical discussion of
empathy-related accounts of contagious
yawning.]
-
- The Þnal example of research with
non-primate mammals comes from two reports on
elephants. Rossman et al. (2017) described a
small percentage of yawns in a group of nine
semi-tame African elephants as possible
contagious yawns. Five of the six instances were
by elephants arousing from recumbent postures at
nighttime and seeing another arousing elephant
yawning. A more recent study on the same group
(with some di_erent members) yielded similar
data, along with data suggesting that some
elephants yawned contagiously after seeing
simulated yawns by their human handler (Rossman
et al. 2020). The authors called for more
observations of yawning in free-ranging
elephants.
-
-
- Natural yawning and contagious yawning in
primates
-
- Back to primates, and the question of why
contagious yawning has never been reported in
many thousands of hours of observations on
captive and free-ranging groups. Two possible
reasons for this are that it does not exist, or
that it does exist but has been consistently
missed by observers. One observational study of
a captive group of chimpanzees focused on
di_erent yawn types (identiÞed through
video microanalysis) but did not report any
contagious yawning (Vick and Paukner 2010). The
authors suggested that the phenomenon might
depend on the kind of yawns involved. They also
found no sex di_erence in overall frequency of
yawning. Comparative studies of macaque species
have revealed commonalities and divergences in
aspects of yawning. For example, in captive
Japanese macaques males yawned more than females
from a young age, whereas in long-tailed
macaques this difference emerged only after
puberty (Troisi et al. 1990). Furthermore,
yawning frequency correlated with dominance in
adult male long-tailed but not Japanese
macaques. The authors pointed out that di_erent
motivational states (e.g., aggression and
anxiety or tension) could result in males of
di_erent social rank yawn- ing at similar rates.
No examples of possible contagious yawning were
reported. As a "despotic" species, Japanese
macaques in a zoo were compared with a zoo group
of a "tolerant" species, namely Tonkean macaques
(Zanella et al. 2017). Both species displayed
two types of yawns, "covered teeth" and
"uncovered gums", with the latter being more
frequent in males of both species. However,
uncovered gums yawns were generally more
frequent in Tonkean macaques, and were expressed
especially in tense situations such as feeding
competition. Again, contagious yawning did not
feature in the results. In a rare example of a
study of yawning in wild prosimians, Zannella et
al. (2015) reported no sex di_erences in
frequency of yawning in ring-tailed lemurs or
Verreaux's sifakas. This Þnding supported
the sexual dimorphism hypothesis, which states
that a sex di_erence is less likely in
low-dimorphic species. Links between yawning and
behavioral transitions, and between yawning and
anxiety-evoking events such as predatory attacks
and aggression, were consistent with the
state-changing and anxiety hypotheses of
yawning, respectively.
-
- Interestingly, the Þrst observational
evidence for naturalistic (as opposed to
experimentally elicited) contagious yawning in
primates came from a study not of chimpanzees,
but of monkeys. Palagi et al. (2009) analyzed
over 3000 yawns in a zoo-housed group of
geladas. With contagion- induced yawns
deÞned as occurring within 5 min of a
witnessed yawn, the authors concluded that
female geladas showed contagious yawning, with
most such responses occurring during the second
minute after the Þrst individual yawned.
Furthermore, the e_ect was especially strong
between close grooming partners (suggesting a
link with empathy), and it concerned not just
yawns in general, but involved matching three
di_erent forms of yawning (covered teeth,
uncovered teeth, uncovered gums); the Þrst
two types are associated with friendly
interactions, and the third with agonistic and
tense contexts [based on almost 6000 yawns
(Leone et al. 2014)].
-
- Contagious yawning, reported in female
geladas by Palagi et al. (2009), has not yet
been reported in other groups of that species or
in other monkeys. To clarify the generality of
this phenomenon, attempts to Þnd it should
be extended to other female-bonded monkey
species such as macaques (Fig. 3). Naturally
occurring contagious yawning has been shown in
captive groups of chimpanzees (Campbell and Cox
2019) and bonobos (Demeru and Palagi 2012;
Palagi et al. 2014), notably between strongly
a_liated individuals in the latter species, but
not yet in the former. Again, the analytical
techniques that revealed contagious yawning in
captive geladas and great apes should be applied
to more groups and species, in captive as well
as natural settings.
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- One thousand yawns
-
- Scientific studies of people's natural
yawning typically involve self-reports: people
are asked to keep a log of their yawns (e.g.,
times of occurrence, contexts), sometimes
supplemented by data from portable activity
recorders (Baenninger et al. 1996; Greco et al.
1993; Provine et al. 1987a, b; Zilli et al.
2007). However, data derived from such self-
reports are vulnerable to several sources of
error, including variability in compliance with
instructions, accuracy of recalled events, and
the brevity of the period of record keeping
(typically a few days, rarely more than 1 week).
Furthermore, details of some important
contextual information may be ignored, including
contagion e_ects; for example, contagious
yawning appears not to have been mentioned at
all by students who kept personal logs of their
yawning for 1 week (Greco et al. 1993). For
these reasons, almost 25 years ago I decided to
keep a record of my own yawns and other yawns
that I saw. I aimed to do this accurately (for
example, recording on the spot rather than from
memory), with careful attention to contextual
details, and regardless of when, where, or in
whose company I was when a yawn event occurred.
What started out as a week-long exercise ended
up lasting for 10 weeks, the time it required
for me to record 1000 of my own yawns. Below, I
give more details and present some of my
Þndings, relating them to the literature
on human yawning.
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- I was 40 years old at the time, weighed
around 60 kg, and cohabited with a similar-aged
female ("partner"). Both in full-time
employment, we were non-smokers, on no
prescribed medication, and used no recreational
drugs other than alcohol (5&endash;10 units/week
each). On most days I walked around 1.5 km each
way to and from work, and I played 1-2 h of
sport (badminton) two to three times per week.
This general routine was subject to minor
variations such as short work-related trips away
from home, occasional journeys by car (always as
a passenger) or public transport, and more
leisure activities at weekends. One trip abroad
(from Scotland to the USA) meant that the last
28 yawns were recorded in a di_erent time
zone.
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- To record yawn data I carried a pen and a
small notebook (7.5 _ 13 cm). For 3 days before
starting formal data collection I practiced
recording yawns while attempting to maintain my
natural yawning rhythm. I made a point of
yawning naturally, without covering my mouth,
and without any obvious stretching or
vocalizations. Yawns performed when I was alone
were logged as soon as possible, usually
immediately. In company other than my partner,
who was aware of the study, I waited for
1&endash;2 min after yawning or seeing a yawn
before recording it. There were two reasons for
this short wait: to allow adequate time for any
valid second yawn to be recorded as
"contagious," which applied only if the second
yawner was potentially able to see or hear the
Þrst yawn; to ensure that no one else
would become aware of the study, which was
important because simply knowing that yawning is
being observed can inþuence its
occurrence, and often inhibits it (Baenninger
and Greco 1991; Gallup et al. 2019). The
e_ectiveness of this delay was conÞrmed:
when I asked colleagues and family members
shortly after the study ended, they replied that
they sometimes noticed me writing in the
notebook, but all were oblivious to any link
with yawning. For all my yawns, and as many of
other people's yawns as possible, I noted the
time, place, and general activity and posture
for everyone present. "Present" was deÞned
as within normal speaking distance; if nobody
was present, I was "alone." At night I kept the
diary, pen and a small þashlight under my
pillow. If I yawned while my partner was asleep,
it was recorded as an "alone" yawn.
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- To the Þndings: over the 71 days of
record keeping I yawned on average 14 times per
day (median, 13; range, 1&endash;31) (Fig. 4).
Yawning clearly peaked in the morning (shortly
after I awoke), with a 2-h lag at weekends (when
later bedtimes were usually followed by waking
up later the following morning) (Fig. 5).
Another, less pronounced increase occurred at
around 2200 hours, before I went to bed, and
another small peak at around 0200 hours at
weekends, which probably reþected
tiredness due to being up late. During weekdays
yawning also increased slightly between 1500
hours and 1600 hours, the time of a co_ee break
at work when colleagues gathered in a common
room to sit and chat. Fifty-seven percent of my
yawns occurred while I was sitting down, 23.2%
while lying down (mostly in bed in the morning)
and 19.8% while I was standing up and
stationary; only 0.7% (3.5% of yawns while
upright) happened while I was walking.
-
- Almost half of (48%) of my yawns occurred
when I was alone. I caught yawns from others
infrequently: only 60 (6%) of all my yawns
occurred within 2 min of seeing someone else
yawn (Fig. 6); of 427 yawns by other people that
might have caused me to yawn, 14% did so. Eighty
of my 1,000 yawns (8%) were contagious for
somebody else: 17% of 467 occasions when such an
e_ect was possible. To look for an association
between social closeness and contagious yawning,
I categorized my relationships with other people
as "close" (partner, immediate kin), "familiar"
(colleague, friend), or "unfamiliar" (stranger).
Table 1 shows that 90% of yawns that I caught
were from someone with whom I had a socially
close relationship (i.e., 54 of my 60 socially
induced yawns). By contrast, I yawned only
Þve times after seeing a familiar person
yawn, and only once after a stranger yawned (_
2= 13.7, df = 2, p = 0.001). Table 1 also shows
how often other people caught my yawns. Again,
when my yawns were contagious it was especially
for people with whom I shared a strong
relationship (_ 2= 25.23, df = 2, p < 0.001).
The percentage of yawns by strangers that caused
me to yawn (2%) was notably lower than the
percentage of my yawns that caused strangers to
yawn (25%).
-
- How do my yawn data relate to the literature
on yawning in humans? First, my average daily
yawn frequency fell within the (rather wide)
normal range of between Þve and 30. At 14
yawns/day it was close to the 13.5/day reported
by students who logged their yawns between 0800
and 2400 hours each day for 1 week (Giganti and
Zilli 2011), but higher than the 7&endash;8
yawns/day reported by volunteers in another
short-duration, self-monitoring study
(Baenninger et al. 1996). However, for reasons
already mentioned, in these studies some yawns
might have gone unreported. Also, in Baenninger
et al. (1996) three of the six volunteers were
over 45 years old, and research has shown that
yawning decreases with ageing (Zilli et al.
2008). Second, my overall yawn proÞle
suggests that I was a "morning type," preferring
to get up early and struggling to stay awake
beyond normal bedtime; by contrast "evening
types" prefer to go to bed later and report
di_culty in wakening in the morning [mean
daily yawn frequencies for these groups are 11
and 23, respectively (Zilli et al. 2007)].
Third, over 80% of my yawns occurred when I was
sitting or lying down, as predicted by the
association between yawning and boredom,
sleepiness, and attempts to increase vigilance
or arousal (Provine et al. 1987a, b; Dacquin et
al. 2001). Most yawns reported by a group of
students who kept records of their yawns for 1
week were also associated with sedentary
activities such as driving, studying or reading,
and watching television (Greco et al.
1993).
-
- The fact that almost half of my 1000 yawns
occurred in the absence of anyone else
challenges ideas that a major function of
yawning is communication. Although yawning can
explicitly signal that one is tired, bored,
nervous, or perhaps even sexually aroused (see
Barbizet 1958; Guggisberg et al. 2010; Seuntjens
2010), the communicatory aspect of yawning in
humans appears likely to be secondary to more
fundamental functions. Finally, although my
contagious yawning data predate the emergence of
the modern social closeness hypothesis, they
accord with reports that contagious yawns are
especially likely between people with strong
emotional ties to each other, such as kin and
close friends (Norscia and Palagi 2011; Palagi
et al. 2014); this even appears to be the case
for yawns that are heard but not seen (Norscia
et al. 2020). Kapitány and Nielsen (2017)
discuss methodological issues in the study of
contagious yawning in humans.
-
- Concluding comments
-
- The list of hypotheses that have been
proposed about the functions of yawning and
contagious yawning is too long to be presented
here (see, e.g., Smith 1999; Walusinski 2010a;
Gallup 2011; Krestel et al. 2018). These
behaviors continue to attract research attention
in a wide range of disciplines including
neurological, neuropharmacological,
physiological and medical sciences, and in
perceptual, social, developmental and
comparative psychology. I hope that this
editorial might stimulate further interest in
the ethology and psychology of yawning. Although
it may never become a major, stand-alone
research issue, as I have tried to show, yawning
can be relevant to several "bigger" topics, and
useful data can often be obtained with little
more than careful observation, patience, and if
possible, a video camera. Researchable questions
about yawning and its functions touch on
development, learning, communication, arousal
and stress, social affiliation, and more. When
does yawning occur in a given species, and in
what speciÞc contexts? How do age and sex
affect frequency and form of yawning? How does
yawning vary with species' sexual dimorphism and
social organization? What other factors might
contribute to individual variability in yawning?
How general is the ability to learn to control
aspects of yawning, which has been studied so
far only in adult male macaques? We still have
much to learn about this ubiquitous, quite
banal, yet mysterious behaviour in our own and
in other species.
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