Testing
social hypotheses on spontaneous yawning in
Theropithecus gelada.
Leone A, Ferrari PF, Palagi E
Dipartimento di
Neuroscienze, Università di Parma, Parma,
Italy
Centro Ateneo Museo di
Storia Naturale, Calci, Università di
Pisa, Pisa, Italy
Unità di Primatologia
Cognitiva, Istituto di Scienze e Tecnologie
della Cognizione, Consiglio Nazionale delle
Ricerche, Roma, Italy
Here, we tested hypotheses about the
potential functions of yawning based on its
intensity and social contexts. Due to their
spectrum intensity of yawns (covered teeth/YW1;
uncovered teeth/YW2; uncovered gums/YW3),
geladas are a good model species for this
purpose. We suggest that yawns of different
intensity can bear different information
according to the performer, the context and the
behavioural pattern temporally associated to the
yawn event. YW3, mainly performed by high
ranking males during periods of high social
tension, was frequently associated with an
auditory component and often accompanied by
scratching (a measure of anxiety). YW1 and YW2,
preferentially performed by females, were
frequently associated to lip smacking, an
affiliative display. In conclusion, even though
a clear-cut functional distinction of geladas'
yawn intensity is difficult, YW1 and YW2 seem to
be more linked to affiliative social
interactions; whereas, YW3 seems to be more
linked to agonistic and tension situations.
-Demuru
E, Palagi E. In Bonobos Yawn Contagion Is
Higher among Kin and Friends. PLoS One. 2012;
7(11): e49613
-Leone A,
Mignini M, Mancini G, Palagi E. Aggression
does not increase friendly contacts among
bystanders in geladas (Theropithecus gelada)
Primates. 2010;51(4):299-305
-Leone A,
Ferrari PF, Palagi E. Different yawns,
different functions? Testing social hypotheses
on spontaneous yawning in Theropithecus gelada.
Scientific Reports 2014;4;4010
-Norscia
I, Palagi E. Yawn Contagion and Empathy in
Homo sapiens. PLoS ONE. 2011;6(12): e28472
-Norscia
I, Demuru E, Palagi E. She more than he:
gender bias supports the empathic nature of yawn
contagion in Homo sapiens. R. Soc. open sci.
2016:3:150459.
http://dx.doi.org/10.1098/rsos.150459
-Palagi
E, Leone A, Mancini G, Ferrari PF.
Contagious yawning in gelada baboons as a
possible expression of empathy. Proc Natl Acad
Sci USA. 2009;106(46):19262-19267
-Palagi
E, Norscia I, Demuru E. Yawn contagion in
humans and bonobos: emotional affinity matters
more than species PeerJ 2:e519
-Zannella
A, Stanyon R, Palagi E. Yawning and Social
Styles: Different Functions in Tolerant and
Despotic Macaques (Macaca tonkeana and Macaca
fuscata). J Comp Psychol. 2017
-Zannella A,
Norscia I, Stanyon R, Palagi E. Testing
Yawning Hypotheses in Wild Populations of Two
Strepsirrhine Species: Propithecus Verreauxi and
Lemur Catta. Am J Primatol.
2015;77(11):1207-1215
Introduction
Yawning is an involuntary and stereotyped
behaviour observed in most vertebrate species
(including humans) from foetal stages to
adulthood1. In mammals, the yawning patterns
include mouth opening, deep inspiration, brief
apnea, and slow expiration2. Due to the old
phylogenetic origins of this behaviour3, it has
been proposed that it is adaptive and provides
some evolutionary advantages. Recently,
Guggisberg et al.2 suggested that due to its
ubiquity across different taxa and occurrence
under a number of different physiological states
and social contexts, yawning may serve more than
one function. For example, yawning may be
involved in homeostatic processes1, 3, 4, 5, and
it may be linked to changes of environmental
conditions6, 7, 8, 9, or even to social contexts
(e.g. signal of aggressiveness, hierarchical
dominance, frustration, sexual excitement, or a
means of synchronising activities within the
group)2, 10, 11, 12, 13, 14, 15, 16.
In human and nonhuman primates, two
different types of yawn are generally
distinguished according to the physiological
state and social context: true/rest yawns17 and
tension/aggressive yawns18. True yawns are
typically associated with states of drowsiness
and relaxation (sleepiness7, 9 or boredom19). On
the other hand, tension or aggressive yawns
occur in conflict situations and may indicate
arousal10, 11, 20, 21, 22. In contrast to this
dichotomous view, Altmann23 suggested that both
types of yawns may indicate levels of
physiological arousal and, therefore, it is
extremely difficult to disentangle the two based
on the stimuli/context triggering them. For
example, macaques are known to exhibit 'emotion
yawns' or 'social yawns' during antagonistic
social encounters10, 24, 25. Among the great
apes, chimpanzees yawn mostly in response to
human proximity26 and during conditions of
social tension27. Other researchers have also
proposed that in primates spontaneous yawning is
a form of self-directed behaviour associated to
anxiety states21, 28, 29.
Several of the reports here described seem
to support the hypothesis that one of the
functions of yawn is that of stimulating or
facilitating arousal during state changes1, 17,
30, 31. Although the concluding evidence
supporting such hypothesis still requires
further investigation, there is a general
consensus on that fact that yawning is often
anticipatory of important events and is
associated to behavioural transitions, including
sleep/awake cycles18, 32, 33, 34, 35.
One of the most intriguing issue related to
the yawning phenomenon concerns the analysis of
its behavioural patterns, which could be
potentially provide critical information in
order to understand its functional roles.
Recently, Vick and Paukner14, based on a
detailed behavioural analysis, identified in
chimpanzees two distinct forms of yawn, a full
yawn and a yawn in which the mouth is
half-closed. This finding has been interpreted
within the context of the possible underlying
neurological mechanism. In fact, the possibility
to partially regulate its expression suggests
that there is a voluntary control, or at least
in part, over oro-facial movements accompanying
the yawn. Moreover, it is possible that these
two different forms of yawn reflect different
functions.
Geladas, an Old World monkey species,
perform yawning at three different levels of
intensity that have been recently categorized on
the basis of the degree of mouth opening and the
possible co-presence of vocalizations: yawn with
covered teeth (YW1), yawn with uncovered teeth
(YW2), and yawn with uncovered gums and head
movements (YW3)13. Moreover, vocalizations can
be associated to yawns both before and during
the performance13. The variability in the
expression of this behaviour in geladas, makes
this species suitable to investigate in details
the possible functional role of yawning. We
therefore focussed our investigation on this
species and tested specific social hypotheses
(not mutually exclusive) on the function of
yawning according to its intensity and contexts.
The gelada is a good model species also because
it has a strong sexual dimorphism28, a clear-cut
linear hierarchy36, high social cohesiveness37
and fine-tuning towards companions38. Moreover,
yawn contagion has been recently demonstrated in
this species, thus suggesting its key role in
social behaviour13. In the present study we will
test three social hypotheses.
Hypothesis 1 (sleep-awake
transition)
Yawning is often associated with particular
patterns of rest-activity, indicating the
possibility of an endogenous temporal rhythm1,
8, 10. These internal rhythms allow individuals
to anticipate and to prepare them to the
environmental transitions, as well as to trigger
behavioural and physiological changes in
accordance to such transitions39. In laboratory
rats, a light-to-dark transition was found to be
associated with daily peaks of yawning40, thus
suggesting the presence of a circadian rhythm.
In humans, both the transition from
light-to-dark and dark-to-light are associated
with peak frequencies of yawn6, 7, even though
it seems to be more frequent after waking than
before sleeping7. Up to now, no study explored
the daily variation of the different types of
yawns performed13. If yawning in geladas is
linked to sleep/awake transition, we expect to
find peak levels of this behaviour in the early
morning and late evening (Prediction 1). If the
yawns of different intensity respond differently
to this transition we will be able to
distinguish what in literature are described as
true yawns from other types of yawn10, 11, 14,
17, 23.
Hypothesis 2 (social display)
Threat yawns have been described in some
primate species41, 42, but if canine displays
during yawning can be considered as an
aggressive signal, remains still
controversial10, 43. Furthermore, "threat yawns"
are fundamentally different from other types of
yawns (true/relax) in that they are assumed to
occur in specific social contexts (i.e. during
conflicts) and to be displayed by specific
subjects, such as high rank individuals44
directing their aggressive towards lower-rank
individuals. Moreover, in highly dimorphic
species (Cercocebus albigena and Macaca
fascicularis10; M. nigra11; M. fuscata12), it is
expected that it is displayed mostly by males
due to their active role in territorial defence
and females' control28. This sex difference in
yawn frequency seems, in fact, to disappear in
species not characterized by a pronounced
dimorphism in canine size, such as humans45 and
lemurs (Lemur catta, Propithecus verreauxi,
Palagi unpublished data).
If yawning in geladas, especially in its
more intense version (YW3), has a role in
threatening, we expect that sex and rank has an
influence on the yawning frequency (Prediction
2a). More specifically, we expect YW3 to be more
frequently displayed during contexts of high
social tension, such as during agonistic and
competitive interactions (Prediction 2b), which
in geladas are mainly up to alpha males.
Moreover, we expect that YW3 is frequently
enriched by an auditory component (multimodal
signal) which makes the behaviour less ambiguous
and more easily detectable by all group members
and potential rivals belonging to other OMUs
(Prediction 2c). Conversely, if YW1 and YW2 are
linked to a relaxed predisposition to interact
socially and positively as suggested in recent
reports13, we expect that these two patterns of
yawns are mainly performed by high ranking
subjects, both males and females, as a form of
appeasement (Prediction 2d), and that they are
temporally associated to reassuring signals such
as lip smacking, which is frequently performed
along with affiliative and parental care
behaviours (e.g., grooming, body contact, play,
lactating)36, 46, 47, 48 (Prediction 2e).
Hypothesis 3 (general arousal)
As self-scratching is a reliable indicator
of arousal in primates21, 27, 29, 49, 50, the
association between higher rates of scratching
and yawns may be indicative of increased
physiological arousal14, 27, 51. If yawning in
geladas is linked to a change in motivational
internal state of the performer we expect an
increase in scratching levels immediately after
a yawning event. More specifically, if the three
types of yawn are characterized by differences
in intensity and not in quality, we expect that
YW3 (full yawn) is indicative of a higher
variation in arousal compared to the other types
(YW1 and YW2). Moreover, we expect that
scratching frequency is maximum following YW3
(Prediction 3).
.......
Discussion
In this study we found that yawns of
different intensity performed by geladas follow
a different distribution in frequency depending
on the performer, the context, and the
behavioural pattern temporally associated to the
yawn event.
We investigated the role of social factors
on yawn distribution, and what clearly emerged
from our data is the relationship between male
dominance rank and yawns of higher intensity
level (YW3) (Prediction 2a supported; Figure 2),
being YW1 and YW2 not affected by the gender of
the performer but only by its rank. During YW3
the canine teeth are highly visible and their
whitish colour strongly contrasts with the
reddish one of the gums and of the internal part
of the mouth. This pattern is an evident visual
display, which can be easily detected at long
distances. Such type of yawn is often
accompanied by a loud call preceding the yawn,
and/or a long-distance vocalization, thus making
it a potential communicative signal easily to be
detected at distances that do not require
physical proximity. Compared to other baboon
species, geladas have larger vocal repertoires.
Gustison et al.52 found that gelada derived
vocalizations are generally used by alpha males
while interacting affiliatively with adult
females and immediately after intra-OMU fights.
The additional auditory component accompanying
the most intense form of yawing gives relevance
to the visual cue itself (Prediction 2c
supported), thus making YW3 a multimodal pattern
well perceived by members of the same or
different OMUs. Interestingly, male YW3 is
frequently displayed during post-conflict and
potential competitive periods such as those
preceding food distribution (Prediction 2b
supported) while, in similar contexts, females
showed high levels of YW1 and YW2. This suggests
that either YW3 has different functions in males
and females or that it is so rare in females
that it can be considered primarily a male
signal. Moreover, it is worth noting that a
vocalized yawn performed by the alpha male of
one of the two OMUs often elicited the same
response in the alpha male of the other OMU,
thus indicating a potential function of
inter-group communication between males that are
potential rivals. Based on our findings, we
hypothesize that YW3 can be used by high ranking
males as a multimodal display with the function
of intimidating conspecifics especially during
situations characterized by high levels of
social tension (Figure 3). Even though, to fully
understand the communicative function of a
behaviour, the response of potential receivers
has to be investigated before a display could be
labelled as a signal.
Yet, the hypothesis of the threatening
function of YW3 in geladas finds support in the
literature. In some nonhuman primates with
evident sexual dimorphism, males yawn
considerably more frequently than females do10,
11, 20, 41, 53, even though no distinction has
been made between different types of yawn
patterns. Moreover, in long-tailed macaque males
Chambers and Phoenix54 found a positive
correlation between testosterone levels and
rates of spontaneous yawning, which was mainly
associated with inter-male threats12. The
display function of yawning in dimorphic species
is also supported by the absence of sex
difference in yawn frequency in those primate
species characterized by a low level of sexual
dimorphism in canine size, such as humans (Homo
sapiens7, 45), chimpanzees (Pan troglodytes14),
and lemurs (Lemur catta and Propithecus
verrauxi, Palagi et al. unpublished data). Even
though some social factors appear to modulate
the use of yawn as a threatening signal in
geladas, it could be interesting to investigate
the potential link between the different types
of yawning and androgen hormone concentration
(e.g. testosterone).
Even though LMM revealed that YW1 and YW2
were only influenced by dominance rank
(Prediction 2d supported), females
preferentially performed YW1 and YW2 in each of
the contexts considered for the analyses (Figure
4). The association of lip-smacking (LS) with
YW1 and YW2 did not reach the baseline level of
LS (measured by the association of LS with the
main affiliative interactions36, 55). Yet, YW1
and YW2 were more frequently associated with LS
compared to YW3. It seems that, contrary to YW3,
the less intense forms of yawning are more
linked to positive social contexts thus adding a
further element of dichotomy between the
different yawn intensities considered
(Prediction 2e supported). Hence, compared to
YW3, YW1 and YW2 can be read as an expression of
benign intent by high ranking individuals
towards other group members, especially females.
Along with previous findings on yawn contagion
in this species13, these data suggest that YW1
and YW2 are commonly used by gelada females as
part of a complex communicative system among
individuals that often engage in affiliative
interactions and that are emotionally connected.
In fact, the relationships within the typical
gelada one-male unit (OMU) revolve around adult
females, who form the core of the cohesion and
stability typical of OMUs56. In some cases, the
strength of female bonds suffices to maintain
OMU integrity despite the absence of the male28.
It is worth noting that between gelada females
only YW1 and YW2 elicited a precise mirroring
during yawn contagion13 thus suggesting the
importance of these two types of yawn as strong
stimuli in triggering a matched response
(YW1/YW1 and YW2/YW2). The high frequency and
accuracy of contagiousness elicited by YW1 and
YW2 can have not only important implication in
synchronizing the activity between individuals,
but it may also strengthen their bonds and, at
the same time, signal their relationship
quality13.
The arousal hypothesis of yawning predicts
that it can be considered as a displacement
behaviour associated with neural mechanisms
lowering the arousal level in the subject
(humans12; mangabeys and macaques10; macaques21,
57; hamadryads56). In the first gelada's
ethogramm, yawning - similarly to scratching -
was described as a self-directed behaviour
indicating anxiety28. Our data show that
scratching increased after each yawning type,
even though animals tended to scratch themselves
more after yawning of higher intensity level
(YW3), thus suggesting that YW3 could indicate
an even higher level of arousal (Figure 5).
As it occurs in other primate species, in
which yawning shows predictable daily
variations1, 7, 8, 10, 18, 28, 58, in geladas we
found that animals yawned preferentially in the
phase of sleep/awake transition, especially in
the early mornings (Prediction 3 partially
supported). Yet, we detected a difference in the
yawn temporal distribution according to the
spectrum intensity of yawns considered. In early
morning, the first type of yawn to increase was
YW1, which peaked from 07.00 to 09.00 am. During
this time window the subjects alternated short
periods of sleeping and waking, being social
activities (e.g. grooming, care giving) not
already begun. YW2 and YW3 peaked an hour later,
from 08.00 to 09.00 am. During this period
animals were completely awake and all engaged in
their usual social activities. We could
tentatively consider the early morning YW1 (the
yawn of the lowest intensity) as a form of yawn
which, by promoting full vigilance and
awakening, favours the beginning of
group-coordinated activities (e.g. feeding,
grooming). To date, there are no studies
investigating the relation between the daily
distribution of yawning and its different
intensity or duration in time. Hence, it is not
yet possible to compare our findings with other
reports and, therefore, our hypothesis remains
speculative and needs further
investigation.
The only type of yawn showing a second peak
along the day was YW3, which was particularly
frequent from 02.00 to 03.00 pm. This time
window included the afternoon pre-feeding, a
period characterized by high levels of anxiety
and aggressive events. As already stated,
compared to YW1 and YW2, YW3 was more frequently
associated with social tension situations and,
under such circumstances, it was mainly used by
males as a threatening signal. Baenninger4
reported that lions (Panthera leo) and mandrills
(Papio sphinx) yawned more frequently just
before feeding time, a finding that was
replicated by Holmgren et al.59 in laboratory
rats, even though no distinction in the
morphology of the yawn was reported.
In conclusion, even though the functional
distinction of the different intensities of
gelada yawns is not so clear-cut, our data seem
to indicate that yawns of different intensity
have multiple communicative functions (e.g.,
synchronization of group activity, emotional
connection, inter-group communication and
threatening). Our findings also suggest that in
geladas the spectrum of yawn intensity varies
according to the sex of the yawner, with a
strong dimorphism which can reflect, at least in
part, on the potential communicative functions
of yawning. Methods
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