- -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
- - 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;131(3):179-188
- -Zannella A,
Stanyon R, Maglieri V, Palagi E. Not all
yawns tell the same story: The case of Tonkean
macaques. Am J Primatol. 2021;83(7):e23263.
- Abstract
- Here the authors show for the first time
that the plasticity in morphology and duration
of yawning in Macaca tonkeana can be associated
with different functional contexts. Macaca
tonkeana is classified as a tolerant macaque
species characterized by social interactions
minimally constrained by dominance rank or
kinship. Tonkean macaques, as other egalitarian
species, rely on a complex facial communicative
system. They found that the degree of mouth
opening (ranging from covered to uncovered tooth
yawns) and the duration of yawning were not
strictly dependent. The shortest uncovered tooth
yawns were associated with an intense
locomotor/physical activity and peaked
immediately after stressful social events thus
indicating an increase in arousal. In contrast,
longer yawns, independently from teeth exposure,
were primarily associated with a relaxed state
of the subject. In conclusion, this study
suggests that to explore the potential different
functions of yawning, it is necessary to focus
on the variability of its expression both in
terms of morphology and duration, because not
all yawns tell the same story.
-
- Résumé
- Les auteurs montrent pour la première
fois que la plasticité de la morphologie
et de la durée des bâillements chez
Macaca tonkeana peut être associée
à différents contextes
fonctionnels. Macaca tonkeana est classé
parmi les espèces de macaques
tolérantes, caractérisées
par des interactions sociales peu contraintes
par le rang de dominance ou la parenté.
Les macaques tonkéens, comme d'autres
espèces égalitaires, s'appuient
sur un système complexe de communication
faciale. Ils ont constaté que le
degré d'ouverture de la bouche (allant
des bâillements de dents couvertes aux
bâillements de dents non couvertes) et la
durée du bâillement
n'étaient pas strictement
dépendants. Les bâillements les
plus courts des dents non couvertes
étaient associés à une
activité locomotrice/physique intense et
atteignaient leur maximum immédiatement
après des événements
sociaux stressants, indiquant ainsi une
augmentation de l'excitation. En revanche, les
bâillements plus longs,
indépendamment de l'exposition des dents,
étaient principalement associés
à un état de relaxation du sujet.
En conclusion, cette étude suggère
que pour explorer les différentes
fonctions potentielles du bâillement, il
est nécessaire de se concentrer sur la
variabilité de son expression à la
fois en termes de morphologie et de
durée, car tous les bâillements ne
racontent pas la même histoire.
-
-
- 1. INTRODUCTION
- In 1872, Darwin defined yawning in humans as
"[...] a deep inspiration, followed by a
long and forcible expiration; and at the same
time almost all the muscles of the body are
strongly contracted, including those round the
eyes. During this act tears are often secreted,
and I have seen them even rolling down the
cheeks [...]" (Darwin, 1872, p. 164).
Yet, although spontaneous yawning is a
well-known and long discussed behavior, its
functions have not been fully elucidated.
Several authors have suggested that yawning is
driven by physiological factors, such as
respiration, circulation, and brain cooling
(Gallup & Eldakar, 2013; Guggisberg et al.,
2010). Oxygenation was also considered to be one
of the physiological triggers for yawning, but
in humans yawning frequency is not increased by
COz, inhibited by 02 blood concentrations or
influenced by physical exercise (Provine et al.,
1987a).
-
- Once elicited, yawning cannot be completely
suppressed and, for this reason, it has been
categorized as a stereotyped or reflex-like
pattern (Lehmann, 1979; Provine, 1986). However,
its morphological variability suggests that
yawning can be more than a simple reflex (Massen
& Gallup, 2017; Provine, 2012). It can vary
in duration, frequency, and mouth-opening degree
(Deputte, 1994; Gallup et al., 2016; Leone et
al., 2014). Such variability may be associated
with different social contexts (Vick &
Paukner, 2010).
- Therefore, yawning is considered as a
behavioral pattern that can have different
functions in different circumstances
(Baenninger, 1997; Górecka-Bruzda et al.,
2016; Guggisberg et al., 2010; Leone et al.,
2014; Zannella et al., 2015, 2017).
-
- It is commonly reported that yawning
punctuates the sleep-awake cycle (monkeys,
Deputte, 1994; monkeys, fish, big cats,
Baenninger, 1997). Endogenous rhythms induce
changes in brain activity that can trigger
yawning (humans, Zilli et al., 200Z). According
to the State Change Hypothesis formulated by
Provine et al. (1987b), human yawns are often
associated with sleepiness and boredom (Provine
& Hamernik, 1986). The temporal association
between yawns and behavioral transitions could
be coopted in social species where yawns can
represent a communicative social tool to
synchronize group activity (Pan troglodytes,
Vick & Paukner, 2010). For example, the
susceptibility to yawn in response to others'
yawns (yawn contagion), has been extensively
documented in human and nonhuman animals
(humans, Norscia & Palagi, 2011, Norscia et
al., 2020; Provine, 1986; monkeys, Palagi et
al., 2009; great apes, Campbell & Cox, 2019;
Demuru & Palagi, 2012; canids, Neilands et
al., 2020; Romero et al., 2014).
-
- External variables such as stressful events
can also activate the neurological circuit of
yawning (Rattus norvegicus, Moyaho &
Valencia, 2002). Liang et al., 2015) found that
in birds (Sula granti) the administration of
acute stressors initially inhibited and later
increased the occurrence of yawning. The authors
monitored variations in arousal by measuring
plasmatic corticosterone and found that yawning
increased during the arousal reduction phase.
These findings led the authors to formulate the
Arousal Reduction Hypothesis for yawning in
birds. However, Liang et al.,2015) did not focus
on possible differences in the duration and
morphology (degree of mouth opening) of each
yawning event in response to stressful
stimuli.
-
- Giving that yawning appears to be a sort of
'halfway between a reflex and an expressive
movement' (sensu Barbizet, 1958, p. 203), its
variability linked to duration and morphology
(Anderson & Wunderlich, 1988; Deputte, 1994;
Schino & Aureli, 1989) is an important key
for understanding the specific functions of
yawning. The duration of a yawn depends on the
intensity of the inhalation phase (Barbizet,
1958; Deputte, 1994). During the resting period,
when locomotor activity level and respiratory
frequency are both low, individuals perform long
yawns (Deputte, 1994). During intense locomotor
activity yawns are shorter, but not more
frequent (Provine et al., 1987a) due to the more
rapid breathing (Cercocebus albigena and Macaca
fascicularis; Deputte, 1994). Focusing on yawn
morphology in primates, it is possible to
associate the motor pattern with different
mouth-opening degrees, such as covered and
uncovered tooth yawning. In different species,
covered and uncovered tooth yawning can be
triggered by various affective states deriving
from diverse social contexts. In chimpanzees
(Pan troglodytes), covered tooth yawns are
associated with anxiety, measured by the
variation in the scratching levels (Vick &
Paukner, 2010). In contrast, in some monkeys,
the covered tooth yawn is apparently a relaxed
pattern (Leone et al., 2014); whereas the
uncovered tooth yawn is associated with tense
situations (Theropithecus gelada, Leone et al.,
2014; Palagi et al., 2009; Macaca tonkeana,
Zannella et al., 2017). This variability in yawn
morphology and affective states deserves further
research to understand if and how yawn
variability is predictive of emotional states in
primates, including humans.
-
- In 1994, Deputte described the motor
components of a yawning event by using
Cercocebus albigena and Macaca fascicularis as
model species. According to Deputte (1994),
yawns are characterized by a sequence of
movements during which three phases can be
distinguished on the basis of peculiar
morphological markers. During Phase 1 the head
is lifted upward, the mouth is slowly opened,
reaching an oval shape while teeth remained
covered. In Phase 2 the head continues to move
upward until maximum gaping is reached revealing
both teeth and gums. The eyes are often totally
closed. During Phase 3 the head is lowered, lips
rapidly cover the teeth and the mouth is snapped
shut (Figure 1, Figure S1). During the Phase 2
of a yawning event, animals expose their
canines, which are more evident in males of
primate species with marked sexual dimorphism in
canine size. The presence/absence of these
phases define the different types of yawn
morphology (Y1 includes Phases 1 and 3; Y2
includes Phases 1-3; Y3 includes Phases 2 and 3)
(Figure 1).
-
-
- Auditory cues often help to maximize the
effect of these impressive visual displays
especially in males of dimorphic species. A
yawn, therefore, can become a multimodal signal
if associated with the emission of vocalizations
(auditory component) (Theropithecus gelada
males, Leone et al., 2014; Cercocebus albigena,
Deputte, 1994). A yawn can be also accompanied
by an active production of sounds obtained by
specific behaviors (for the different species of
Sulawesi macaques see Dixson, 1977; Hadidian,
1980; Lindsay, 1976; Nickelson & Lockard,
1978; Reed et al., 1997; Thierry et al., 2000a).
By stamping on the ground and shaking objects,
animals express their arousal and enrich the
visual stimulus to attract the attention of the
potential receivers (i.e., attention getting
behaviors; Hostetter et al., 2007; Leavens et
al., 2004; Tomasello et al., 1994). To increase
signal detectability, animals can also emit the
stimulus in association with specific body
postures and location of performance. This
tactic generally reduces the reaction time of
receivers, making the signal (e.g., expressing
an emotional state) even more effective (see
Hebets & Papaj, 2005 for an extensive
review).
-
- Communicative complexity seems to covariate
with the high levels of social tolerance
characterizing certain primate species (Scopa
& Palagi, 2016), which tend to have more
complex and larger communicative repertoires
than despotic species (Dobson, 2012; Rebout et
al., 2020; Roberts & Roberts, 2020).
Tolerant interactions are less affected by rank
or kinship and rely more on the quality of
relationships shared by subjects (Maestripieri,
1995; Thierry et al., 2000b). Apparently,
yawning variability is linked to the high level
of tolerance of some primate species, such as
geladas (Theropithecus gelada, Leone et al.,
2014; Palagi et al., 2009) and Sulawesi macaques
(Dobson, 2012; Maestripieri, 1999). Here, for
the first time, we explore the different roles
of yawning depending on the variability in
morphology (degree of mouth opening) and the
variability in its duration. We selected Macaca
tonkeana as a model species due to its tolerant
social style (Butovskaya, 2004; Thierry et al.,
2000b) and its variable yawning repertoire
(Anderson & Wunderlich, 1988; Thierry et
al., 2000a; Zannella et al., 2017). We
hypothesize that yawns which differ in
morphology and duration are linked to different
individual contexts and possibly to the sex of
the yawner. Specifically, we expect that longer
yawns, independently of their morphology, are
associated with low level of locomotor activity
characteristic of resting/relaxing periods
(e.g., laying down, relaxed social interactions)
(Prediction 1) especially in females (see Leone
et al., 2014). Conversely, we predict that
short-yawns, associated with canine exposure,
are linked to (i) an intense locomotor activity
(e.g., standing/walking) and ii) arousal of
subjects (e.g., shaking objects, slapping on the
ground) as it occurs immediately after the
perception of a stressful stimulus (e.g.,
aggression) (Prediction 2).
-
- 4. DISCUSSION
- Understanding yawning has proved
challenging. Various authors have previously
suggested that yawning may have communicative
functions (see Guggisberg et al., 2010 for an
extensive review). In particular, several
studies showed that different morphologies of
yawning can be associated with different social
contexts (Theropithecus gelada, Leone et al.,
2014; Pan troglodytes, Vick & Paukner, 2010;
Macaca tonkeana, Zannella et al., 2017). For
example, in Old World monkeys, males have longer
canines than females and have been observed
yawning in tense and agonistic contexts
(Hadidian, 1980; Redican, 1975). The exposure of
canines, the directionality and the occurrence
during tense social situations led several
authors to conclude that in these circumstances,
yawning is a pattern possibly conveying
threat/arousal messages (Altmann, 1967; Deputte,
1994). This hypothesis is supported by
experimental findings suggesting that intense
male yawns induce in the observer specific
saccades directed to the canines (Gothard et
al., 2004).
-
- Yawning can be characterized by different
degrees of mouth opening and durations. To our
knowledge, previous literature focused on the
different morphologies of yawning without taking
into account the duration of the motor pattern.
We found that the longest yawns were mainly
performed by Tonkean macaques during periods of
relaxation/ social affiliation (Figure 2c) and
during sitting/laying down postures (Figure 2b)
(Prediction 1 supported). Moreover, males
performed shorter yawns compared to females thus
probably indicating a higher involvement of
males in arousal contexts. These findings
indirectly support the hypothesis formulated by
Deputte (1994) on the linkage between the low
level of locomotor activity and the extension of
the inhalation phase which translates into an
increase of yawn duration. The indirect linkage
between yawn duration and the activity level of
subjects was also observed in Macaca
fascicularis and Cercocebus albigena (Deputte,
1994), although Deputte's study was not focused
on the social interactions or contexts during
which the subject engaged in a yawning event. We
found that the duration of Y1 (covered teeth
including the preparatory phase, Phase 1) did
not differ from that of Y2 (uncovered teeth
including the preparatory phase, Phase 1) and Y3
(uncovered teeth not including the preparatory
phase) (Figure 1). Conversely, despite their
morphological similarity (uncovered teeth
display), Y2 and Y3 significantly differed in
their duration, with Y3 being shorter than Y2
(Figure 2d). Overall, these results suggest that
in Macaca tonkeana yawn durations are not
necessarily dependent on the mouth-opening
degree and canine exposure.
-
- Focusing on the two forms of yawning that
significantly differed in their duration (Y2 and
Y3), we found that the arousal state provoked by
previous aggression significantly affected the
morphology of the yawn performed. Specifically,
only the occurrence of Y3 (lacking the slow
preparatory phase and showing canines), was
positively influenced by the arousal state of
the yawner (Figure 3b) and its standing/walking
posture (Figure 3a). Y2 occurred more frequently
when animals were involved in low locomotor
activities (sitting/laying down) (Figure 3a)
under relaxed contexts (Figure 3b). In Tonkean
macaques, after an agonistic event, individuals
tend to increase self-directed behaviors, such
as self-scratching, selfgrooming and attention
getting patterns (shaking objects and ground
slapping) thus indicating that in this species
aggression induce an arousal state in the
subjects (Palagi et al., 2014; Pallante et al.,
2018; Zannella et al., 2017).
-
- Our data provide quantitative support to
previous observations on Old World monkeys in
which it was anecdotally reported that yawning
was often performed immediately after
producing-sound behaviors such as object shaking
or stamping (Deputte, 1994; Hadidian, 1980;
Thierry et al., 2000a). In Theropithecus gelada,
another tolerant monkey species (Pallante et
al., 2016), yawns are also variable in their
morphology (Palagi et al., 2009), but an
assessment of duration variability was lacking.
Leone et al., (2014) found that yawns
characterized by different mouth opening degrees
were predictive of different emotional states.
For example, the widest forms of yawing
(uncovered teeth and gums), typical of males,
occurred during highly tense situations.
Moreover, such types of yawns were often
accompanied by a loud call (preceding the yawn
performance) and/or a long-distance
vocalization, thus making yawning easily
detectable also in absence of physical proximity
between the yawner and the receiver. In Tonkean
macaques, yawns are completely silent but the
strict temporal association existing between Y3
and the active production of sounds might
optimize the communicative function of this type
of yawning by increasing its detectability.
-
- A relationship between yawn morphology and
the arousal state of the subject was also
reported in the great apes (Vick & Paukner,
2010). By applying the facial action coding
system analysis, these authors demonstrated that
chimpanzees show different types of yawn
characterized by different degrees of mouth
opening (full yawns = not modified yawns;
nonfull yawns = modified yawns). Modified yawns,
but not full yawns, were found to be associated
to subjects' arousal state that was measured via
scratching rates. Unfortunately, in this study
no data on the duration of yawns are reported in
association to morphology.
-
- In many primate species, being involved in
or witnessing a conflict can induce arousal
(Aureli, 1997). One of the most iconic
self-directed behaviors used to quantify the
arousal state of a subject is self-scratching
(Schino et al., 1990; Troisi et al., 1991) which
has been demonstrated to increase in the
post-conflict in primate species (Eulemur
fulvus, Palagi & Norscia, 2011; Papio
hamadryas, Judge & Mullen, 2005; Macaca
tonkeana, Palagi et al., 2014; Pallante et al.,
2018; Zannella et al., 2017). Focusing on the
exact minutes following an agonistic
interaction, we found that both the opponents
(Figure 4a) and bystanders (Figure 4b) showed a
peak of Y3 during the first minute of
post-conflict observations, when the level of
arousal experienced by the subjects was
presumably still high (Macaca tonkeana, Palagi
et al., 2014; Pallante et al., 2018). Following,
from the 2nd to the 3rd minute after the
conflict, the frequency of Y3 returned to
baseline levels. The peak of Y3 in the first
minute could indicate that yawning is an
immediate arousal response after the
administration of the stressful stimulus in
contrast to scratching in which the frequency
tends to remain above the baseline levels during
the PC 5-min block. Although this finding
suggests a possible link between Y3 and
post-conflict arousal, this aspect merits
further investigation considering that, to our
knowledge, a minute-by-minute analysis of
yawning in the postconflict period is lacking in
the literature.
-
- The frequency of Y2 (yawns characterized by
the preparatory phase and uncovered teeth,
Figure 1) did not show any variation in the
post-conflict compared to the matched-control
period either in opponents or bystanders.
According to previous literature, the uncovered
tooth yawns are the most impressive visual
displays making teeth completely visible and
occurring preferentially during tense situations
("threat yawns" sensu Altmann, 1967). However,
we showed that Y2 and Y3, two forms of yawning
both characterized by teeth exposure but
different durations, follow a different pattern
of distribution in the post-conflict
periods.
-
- In conclusion, our study suggests
that to explore the potential different
functions of yawning, it is necessary to focus
on the variability of its expression, not only
in terms of morphology, but also in terms of
duration. A possible next step would be to
investigate yawn contagion as a function of the
duration and morphology of triggering yawns. The
possible response to others' yawns could shed
light on the different communicative valences
expressed by the different types of yawning
stimuli.
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