Yawning is an involuntary action that begins
with a slow opening of the mouth with
inhalation, followed by a maximum gaping phase,
and ends with a short exhalation and the closing
of the mouth. A wide variety of vertebrate
species, including humans, yawn. Here, we report
underwater yawn-like behavior in three captive
common bottlenose dolphins, inferred from 119-h
of observations. Five cases of yawn-like
behavior were selected out of 2045 open-mouth
behaviors, after removing intentional open-mouth
behaviors. Yawn-like behaviors were chosen that
had a mouth open-close duration ratio of ² 1
(duration of Phase 3, the period of mouth
closing after maximum opening, divided by the
duration of Phase 1, the period of mouth opening
from start to maximum opening). Naïve human
evaluators selected "yawn-like" behaviors. All
five cases of yawn-like behavior occurred during
inactive periods, similar to human yawns. In
three of the five cases, inactivity levels
significantly decreased within 4 min after the
yawn-like behavior; therefore, yawn-like
behavior in dolphins may increase their arousal
level in drowsy states. Thus, the yawn-like
behavior of dolphins, without breathing, is
similar to yawning in terrestrial animals,
including humans.
Résumé
Le bâillement est une action
involontaire qui commence par une lente
ouverture de la bouche avec inspiration, suivie
d'une phase de béance maximale, et se
termine par une courte expiration et la
fermeture de la bouche. Une grande
variété d'espèces de
vertébrés, y compris les humains,
bâillent. Ici, nous rapportons un
comportement de type bâillement sous-marin
chez trois grands dauphins communs en
captivité, déduit de 119 heures
d'observations. Cinq cas de comportement
ressemblant à un bâillement ont
été sélectionnés sur
2045 comportements bouche ouverte, après
avoir supprimé les comportements bouche
ouverte intentionnelle. Des comportements de
type bâillement ont été
choisis avec un rapport de durée
d'ouverture-fermeture de la bouche 1
(durée de la phase 3, la période
de fermeture de la bouche après
l'ouverture maximale, divisée par la
durée de la phase 1, la période
d'ouverture de la bouche du début au
maximum ouverture). Des évaluateurs
humains naïfs ont sélectionné
des comportements « semblables à des
bâillements ». Les cinq cas de
comportement ressemblant à un
bâillement se sont produits pendant des
périodes d'inactivité, similaires
aux bâillements humains. Dans trois des
cinq cas, les niveaux d'inactivité ont
diminué de manière significative
dans les 4 minutes suivant le comportement
semblable à un bâillement ; par
conséquent, un comportement semblable
à un bâillement chez les dauphins
peut augmenter leur niveau d'excitation dans les
états de somnolence. Ainsi, le
comportement semblable au bâillement des
dauphins, sans respirer, est similaire au
bâillement des animaux terrestres, y
compris les humains.
To the best of our knowledge, this is the
first study to examine un- derwater open-mouth
behaviors that might be classified as yawning in
dolphins. The yawning action of the mouth has
been widely identified among various vertebrates
(e.g., Sauer and Sauer, 1967; Luttenberger,
1973; Baenninger, 1987; Miller et al., 2010;
Bakkegard, 2017) but has yet to be confirmed in
a fully aquatic mammal.
Do dolphins really yawn?
Yawning is characterized by a wide, open
mouth, accompanied by deep inhalation, with a
three-phase structure. Yawning in animals,
including humans, is generally subjectively
judged by a researcher, based on the appearance
of the behavior (e.g., Gallup, 2011), but an
OCDR ² 1 is one of the quantitative
characteristics of yawning (Reiss- land et al.,
2012). The yawn-like behaviors observed in these
common bottlenose dolphin are similar to yawning
in animals in terms of their behavioral
structure (three phases with OCDR ² 1 and
maximum gape). Additionally, these yawn-like
behaviors occur during resting states, and
possibly function in awakening from drowsy
states, which seems to be similar to the arousal
hypothesis for the function of yawning (Guggis-
berg et al., 2010; Walusinski, 2006). These
results imply that the yawn-like behavior
observed in these common bottlenose dolphin is
yawning.
The three-phase structures with OCDR ² 1 of
the yawn-like behavior in dolphins are quite
similar to yawning in human fetuses (Reissland
et al., 2012) and other animals [e.g.,
old-world monkeys, South Amer- ican sea lions
(Otaria flavescens), and Red Hills
salamanders] (Deputte, 1994; Bakkegard,
2017; Palagi et al., 2019). Traditionally,
yawning in animals has been extracted as
yawn-like open-mouth behavior using only the
visual impression of a researcher (on-site or
recorded video) (e. g., on-site: Deputte, 1994,
recorded video: Palagi et al., 2019). Our method
here was conservatively double-checked; first,
the first author extracted the yawn-like
behaviors by visual inspection, and then 10
nai_ve evaluators selected the yawn-like
behaviors from open-mouth behaviors with similar
durations and OCDR ² 1. This double-checked
inspection resulted in five agreements and two
disagreements in yawn-like behaviors between the
first author's selection and the selection of
the 10 evaluators. The maximum gape should be
added to quantitatively select yawn-like
behaviors because, in the two disagreements, the
first-author-selected "yawn-like" behaviors that
both had "medium" gapes instead of "large"
gapes.
Several mammals (e.g., primates, lions, and
South American sea lions), including humans,
yawn frequently in drowsy states (Deputte, 1994;
Baenninger, 1987; Palagi et al., 2019). The
yawn-like behaviors observed in these common
bottlenose dolphin also occurred when in a
resting state, or during sleepy or drowsy states
which required arousal. Further research is
needed to investigate whether these yawn-like
behaviors are affected by circadian rhythms,
like human yawns (Zilli et al., 2007).
Inactivity levels decreased within a few
minutes of yawn-like behavior in these common
bottlenose dolphin, after which they stabilized
in a resting state. Yawn-like behavior in
dolphins seemed to trigger arousal and change
the state of inactivity. This observation fits
the arousal hypothesis of human yawning, in
which yawning is thought to induce arousal.
Moreover, in previous studies yawning in other
mammals, including long-tailed macaques (Macaca
fascicularis), gray-cheeked mangabeys
(Lophocebus albigena), and African elephants
(Lox- odonta africana), has been shown to
function in arousal (Deputte, 1994; Rossman et
al., 2017).
The existence of yawning without breathing
in cetaceans as well as in human and rat fetuses
requires the definition of yawning (a wide, open
mouth with deep inhalation) to be broadened. We
propose the definition of animal yawning be
amended as follows: "Yawning is an involuntary
action that starts with slow mouth opening,
followed by a maximum gaping phase, and ends
with rapid closing of the mouth."
Categorizing open-mouth behaviors in
dolphins We propose the following steps to
distinguish yawning from other open-mouth
behaviors in fully aquatic mammals: 1) record
all open- mouth behaviors, 2) select open-mouth
behaviors with sufficiently long durations to
classify the three phases (0.3 s for the common
bottlenose dolphin) and without obvious purpose,
and 3) select open- mouth behaviors with three
clear phases, an OCDR ² 1, and with maximum
mouth size during Phase 2. After these steps
have been completed, the remaining open-mouth
behaviors could be classified as yawning in
fully aquatic mammals.
Yawning frequency across taxa
Yawning in these common bottlenose dolphin
and other mammals, including humans, differs in
the frequency of occurrence. The common
bottlenose dolphins in the present study yawned
only five times, for a total of 9 s, over 119 h
of observation (conservative values) (averaging
0.03 yawns/ind./h). Other mammals yawn more
often, for example, lion: 1.2 yawns/ind./h
(Baenninger, 1987); mandrill: 0.78 yawn-
s/ind./h (Baenninger, 1987); Przewalski's horse
(Equus ferus prze- walskii): 0.94 ± 0.89
yawns/ind./h (Gorecka-Bruzda et al., 2016); and
the domestic horse (E. caballus): 0.68 ±
0.86 yawns/ind./h (Goreck a-Bruzda et al.,
2016). Yawning in the common bottlenose dolphin
thus seems to be a rare behavior compared to
other mammals. This difference could be related
to their fully aquatic adaptations and/or other
unknown reasons. Further studies are required to
clarify why dolphins rarely yawn. Yawning
studies on other fully aquatic mammals, such as
sirenians, may reveal the effects aquatic
adaptations on the frequency of yawning.
We did not investigate the relationships
between yawn-like behaviors and feeding, or
yawn-like behaviors in a socially stressful
context. Previous studies have tested whether
yawning increases with fixed feeding time in
domestic horses (Fureix et al., 2011), lions,
and mandrills (Baenninger, 1987), and indicates
that yawning before a fixed feeding time might
be food-anticipatory yawning (Holmgren et al.,
1991). Our subject dolphins, however, did not
have fixed feeding times, and the interval
between feeding times varied daily, ranging from
2 to 7 h. It was thus difficult to test whether
dolphin yawn-like behavior was food-anticipatory
yawning. In addition, aggressive behaviors
(socially stressful conditions) occurred only
once during our observations, which made it
impossible to investigate the relationship
between yawn-like behaviors and socially
stressful conditions. Further research is needed
to investigate whether yawn-like behaviors in
dolphins are related to feeding or aggressive
behaviors.
The function of yawning in animals varies,
including social reactions when encountering
another individual (Siamese fighting fish:
Baenninger, 1987), starvation or preparation for
feeding (Herman's tortoises and European pond
turtles: Luttenberger, 1973, Red Hills
salamanders: Bakkegard, 2017, and lions and
mandrills: Baenninger, 1987); stress reactions
from being handled by a researcher or
encountering a predator (budgerigars: Miller et
al., 2010); and resting (ostrich: Sauer and
Sauer, 1967, this study). Although the contexts
of yawning are different, the behavioral form of
yawning (slow gaping and quick closure) is
similar among various vertebrates, suggesting a
stereotyped action pattern (Gallup et al.,
2016). Gallup et al. (2016) showed that yawn
duration is correlated with brain weight and
cortical neuron number in various terrestrial
mammals. Further studies on aquatic mammals, as
well as other terrestrial animals, will further
reveal the evolutionary pathway and function of
yawning in animals.
