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Spontaneous yawning is a widespread
behaviour in vertebrates. However, data on
marine mammals are scarce. In this study, we
tested some hypotheses on the functions of
yawning in a captive group of South American sea
lions (Otaria flavescens). According to the
Dimorphism Hypothesis, species showing low
levels of sexual dimorphism in canine size do
not show sex differences in yawning
distribution; this was supported by our
findings, since yawning did not differ between
the sexes.
Yawning was more frequently performed during
resting/sleeping contexts, thus supporting the
Drowsiness Hypothesis. Yawning and
self-scratching are considered reliable
indicators of short-term anxiety in sea lions,
since they immediately increased after conflicts
both in aggressors and victims (Social Distress
Hypothesis supported). In the long-term, yawning
was not correlated with individuals' dominance
status, thus showing that anxiety is similarly
experienced by dominants and subordinates.
The last two findings can be explained by
the social competition of this species, that
involves individuals independently from their
sex, age or ranking status. Therefore, the
exposure to frequent stressful events can induce
similar levels of anxiety in all the subjects
(Resource Inequity Hypothesis supported). In
conclusion, spontaneous yawning in sea lions
seems to share similar functions with other
social mammals, suggesting that this behaviour
is a possible plesiomorphic trait.
Résumé
Le bâillement spontané est un
comportement répandu chez les
vertébrés. Cependant, les
données sur les mammifères marins
sont rares. Dans cette étude, les auteurs
ont testé certaines hypothèses sur
les fonctions du bâillement dans un groupe
captif d'otaries du Sud (Otaria
flavescens).
Selon l'hypothèse du dimorphisme, les
espèces présentant de faibles
niveaux de dimorphisme sexuel, en taille de
leurs canines, ne montrent pas de
différence liée au sexe dans leurs
différents bâillements. Leurs
conclusions corroborent ces données,
puisque les bâillements ne
diffèrent pas entre les sexes.
Les bâillements sont plus
fréquents lors des transitions repos /
sommeil, corroborant ainsi l'hypothèse
d'un lien avec la somnolence.
Le bâillement et l'auto-grattage sont
considérés comme des indicateurs
fiables d'une anxiété
récente chez les lions de mer, puisqu'ils
augmentent aussitôt après les
conflits, tant chez les agresseurs que chez les
victimes (hypothèse de détresse
sociale soutenue).
À long terme, le bâillement
n'est pas corrélé au statut de
dominance des individus, ce qui montre que
l'anxiété est vécue de la
même manière par les dominants et
leurs subordonnés. Les deux
dernières conclusions peuvent être
expliquées par la compétition
sociale de cette espèce, qui implique des
individus indépendamment de leur sexe, de
leur âge ou de leur statut
hiérarchique. Par conséquent,
l'exposition à des
événements stressants
fréquents peut induire des niveaux
d'anxiété similaires chez tous les
sujets (hypothèse d'injustice relative
aux ressources appuyée).
En conclusion, le bâillement
spontané chez les lions de mer semble
partager des fonctions similaires avec d'autres
mammifères sociaux, ce qui suggère
que ce comportement est un trait
plésiomorphique possible.
Introduction
Yawning is a ubiquitous behaviour present in
all classes of vertebrates. It is a stereotyped
behaviour that once triggered, is uncontainable
and unstoppable. In air-breathing animal
species, the first phase of a yawning event is
characterized by a slow and wide opening of the
animal's mouth and is accompanied by a deep
inhalation. The second phase includes a quick
closure of the mouth and a short exhalation.
Depending on the species, yawning may be also
accompanied by eye closing, vocalizations, body
stretching, pandiculation and even tongue
protrusion.
Many hypotheses regarding the potential
functions of spontaneous yawning have been
proposed. These hypotheses can be classified
into two groups, the physiological and social
hypotheses. In the former group, yawning is
posited to act as a homeostatic restoring
mechanism, and, with the intensification of the
studies, some of these hypotheses such as brain
cooling, anxiety and drowsiness hypothesis have
found an increasing support.In the latter group,
the performance of yawning is posited to express
the emotional state of the yawner as a
communicative tool (e.g., threat yawns), since
other members of the group would be able to
associate it with certain contexts or behaviours
and so could act accordingly. Moreover, yawning
has been proven to have an infectious nature
(contagious yawning), suggesting that it may be
a primitive form of emotional contagion.
Spontaneous yawning is mainly displayed
during resting contexts characterized by the
absence of changes in social and environmental
stimuli. The effect of yawning can be linked to
a state of drowsiness in which animals may
change from an awake to a sleep phase and vice
versa1. It has been proposed that the role of
yawning in such situations is to increase the
alertness state, thus making animals able to
respond effectively to sudden and urgent
situations.
Spontaneous yawning can also be affected by
social stimuli and conditions. For example, in
birds, rats, lemurs and monkeys, yawning
increases after an anxiogenic event which can
affect the homeostasis of the subject. In the
wild, Goodall observed that chimpanzees yawned
more frequently in the presence of human
observers and, in captivity, the presence of
humans in front of animal facilities produced an
increase of yawning in monkeys (lion-tailed
macaques, Macaca silenus). For this reason,
along with self-directed behaviours such as
self-grooming and self-scratching, yawning can
be considered an indicator of anxiety. For
example, in chimpanzees, Baker and Aureli showed
that individuals tended to yawn and self-scratch
more frequently during high social tension
conditions that provoked an increase of anxiety
and arousal in the subjects. Recent findings
suggest a possible effect of yawning as a
stress-releaser, which helps restoring
physiological/emotional homeostasis.
In species showing an evident sexual
dimorphism in their canine size, yawning is more
frequent in males than in females. The
development of canines in males is a secondary
sexual characteristic that provides them
advantages both in intra- and inter-sexual
competition. The canine exposure during a
yawning event may convey information about the
transitional phase experienced by the yawner
that can pass from a relaxed to a tense
emotional state or vice versa. Hence, yawning
can anticipate a forthcoming aggressive
behaviour ("threat displays") or a reduction of
the levels of anxiety in the yawner.
In-group conflicts are undoubtedly a source
of social tension for both aggressors and
victims, which often increase self-directed
behaviours in the immediate period after an
agonistic event. This is also true for yawning,
which shows a peak in the minutes after the end
of an agonistic contact (Nazca booby, Sula
granti; ring-tailed lemur, Lemur catta and
Verreaux's sifaka, Propithecus verreauxi;
macaques, Macaca tonkeana).
This wide array of results strongly suggests
the multifunctional nature of this behaviour,
which has been widely studied in primates and
rodents, but has often been neglected in other
species such as marine mammals. Here, we test
some hypotheses, not necessarily mutually
exclusive, on spontaneous yawning in South
American sea lions, a species living in harems
and characterized by high levels of competition.
Sea lions show a strong sexual dimorphism in
body size and morphology (males possess a mane
around their heads), but show a reduced sexual
dimorphism in canine length. The Sexual
Dimorphism Hypothesis predicts that yawning is
more frequent in males when the species presents
evident sexual differences in canine size. We
thus predict that males and females of South
American sea lions do not necessarily differ in
the performance of yawning (Prediction 1).
In species showing an unequal distribution
of social power, subordinates experience greater
levels of anxiety in the long-term. Within
social groups, hierarchy affects stress levels,
which can be evident from the baseline frequency
of self-directed behaviours (e.g., with the
dominants scratching more than subordinates or
vice versa). The self-scratching trend across
hierarchy depends on social organization in
different species or populations, with
subordinates showing the highest long-term
stress levels in hierarchically stable social
groups of despotic species. According to the
Resource Inequity Hypothesis, since yawning is a
reliable indicator of stress, it will be more
frequently displayed by subordinate than by
dominant individuals, reflecting a baseline
anxiety in these kinds of social groups. For
example, in species such as Japanese macaques
(Macaca fuscata) that are characterized by
strong power asymmetry, yawning reflects a
baseline anxiety state in subordinate
individuals that show higher yawning frequencies
than in dominant individuals, particularly
during periods of social stability. Although
South American sea lions establish dominance
hierarchies between group members, a strong
competition over resources is present at all
ages and in both sexes (e.g., females, shade
areas for nursing or water access for
thermoregulation), thus reducing the
monopolization of resources by high ranking
individuals. For this reason, we expect that
yawning does not strictly follow a dominance
gradient in this species (Prediction 2).
If yawning and self-scratching are
behavioural responses linked to an anxiety state
of South American sea lions in response of an
immediate perturbing event (the Social Distress
Hypothesis), we expect that after an agonistic
event, these two behavioural patterns will
increase by following a similar trend in both
the aggressor and the victim (Prediction
3).
Finally, if yawning, as it occurs in other
mammal species, is a mechanism linked to the
alertness state of subjects (the Drowsiness
Hypothesis), we expect it to be concentrated
during periods of inactivity characterized by an
alternation of resting and sleeping phases
(Prediction 4).
Discussion
The aim of this study was to test, for the
first time, hypotheses on the potential
functions of the spontaneous yawning in a marine
mammal species, the South American sea lion
(Otaria flavescens). We have to note that the
hypotheses tested here are not necessarily
mutually exclusive due to the multifunctional
nature of yawning.
The LMMs revealed that the variable
'context' strongly affected the distribution of
yawning frequency but did not have a strong
effect on its mean duration. Yawning was mainly
performed in the resting/sleeping context, when
sea lions were lay on the platforms maintaining
their eyes closed without engaging in any social
behaviour with conspecifics (inactive state).
They sometimes opened their eyes and, from time
to time, moved their body parts. More rarely,
their state of alertness was increased and they
could interrupt the inactive phase by socially
interacting with other sea lions nearby. Despite
our difficulty in determining whether animals
were actually sleeping, the sea lions often
alternated long periods of total inactivity
(eyes closed) with short periods of low activity
(eyes opened). Our findings are consistent with
the association of yawning with drowsiness
already found in human and non-human primates.
These studies also reported that yawn
distribution changed according to the sleep-wake
rhythms of the different subjects with peaks of
yawning during the transitional phases between
the two states.
Sex does not seem to have a strong effect on
either the frequency or duration of yawning,
thus supporting the Dimorphism Hypothesis. In
agreement with our results, in ring-tailed
lemurs and Verreaux's sifaka - two prosimian
species showing monomorphism in canine and body
size - yawning distribution did not
significantly differ between sexes. Although our
results support the Dimorphism Hypothesis of
yawning, due to the small number of males
present in our study group, this support must be
taken with caution. Due to the social structure
of the species (one-male group or harem), the
exploration of the Dimorphism Hypothesis of
yawning in sea lions would need several data
collections in different captive and wild groups
to control for the possible male individual
variability in yawning propensity and canine
size.
Neither the frequency nor duration of
yawning was influenced by the NDS values of the
subjects (a quantitative measure of hierarchical
dominance) thus confirming that in our species,
dominants and subordinates do not show a strong
bias in the levels of baseline anxiety as a
function of a different inequity power
distribution (Resource Inequity Hypothesis
supported).To explain this finding the social
features of South American sea lions have to be
discussed. All the subjects of a colony strongly
compete for shaded areas for thermoregulation,
access to the sea for foraging, mating partners
and for enough safe places for
lactating/nursing49. Therefore, aggressive
interactions are not limited to adults, as
female aggression towards pups and infanticide
attempts by sub-adult males have also been
reported. Therefore, the aggressive propensity
characterizing the species can make each animal,
independent of the role it takes in an agonistic
encounter or its individual features (age, sex
or rank), uncertain about the probability of
being the recipient of aggression. This is in
line with the findings on the distribution of
self-scratching and yawning immediately after
agonistic interactions. Self-scratching has been
proven to be a reliable indicator of anxiety in
human and non-human primates, since it has been
described in a wide range of stressful
situations (e.g., crowded conditions, unfamiliar
encounters, proximity of high-dominant
individuals or post-conflicts). As for
self-scratching, yawning has also been
associated with the presence of environmental
and social stressful stimuli. In our study, we
found that yawning and self-scratching
significantly increased immediately after
conflict for both the aggressor and the victim.
This clearly indicates that both of these
behavioural patterns are sensitive to social
stressors and may have a similar function in
restoring the homeostasis of the subjects
independent of the role they play during the
conflict.
In conclusion, our findings reveal that
yawning is a multifunctional behaviour also seen
in the South American sea lion. Spontaneous
yawning seems to serve similar functions in
different mammals living in well-structured
social groups (e.g., primates, rodents and
pinnipeds), independent of their phylogenetic
distance and terrestrial/aquatic habits, thus
suggesting that this behaviour may be a
plesiomorphic trait.
