The overt and reflexive matching of
behaviors among conspecifics has been observed
in a growing number of social vertebrates,
including avian species. In general, behavioral
contagion&emdash;such as the spread of
yawning&emdash;may serve important functions in
group synchronization and vigilance behavior.
Here, we performed an exploratory study to
investigate yawn contagion among 10 captive
juvenile ravens (Corvus corax), across two
groups. Using observational methods, we also
examined the contagiousness of three other
distinct behaviors: stretching, scratching, and
shaking. A total of 44 20 min observations were
made across both groups, including 28 in the
morning and 16 in the afternoon. The time and
occurrence of all the behaviors from each bird
were coded, and the temporal pattern of each
behavior across both groups was then analyzed to
assess the degree of social contagion. Overall,
we found no evidence for contagious yawning,
stretching, scratching, or shaking. However,
yawns were relatively infrequent per observation
(0.052 ± 0.076 yawns/bird) and thus
experimental methods should be used to support
this finding.
La correspondance manifeste et
réflexive des comportements entre
congénères a été
observée chez un nombre croissant de
vertébrés sociaux, y compris chez
les espèces aviaires. En
général, la contagion
comportementale - telle que la propagation des
bâillements - peut remplir des fonctions
importantes dans la synchronisation des groupes
et le comportement de vigilance. Ici, nous avons
réalisé une étude
exploratoire pour étudier la contagion
des bâillements chez 10 corbeaux
juvéniles en captivité (Corvus
corax), dans deux groupes. En utilisant des
méthodes d'observation, nous avons
également examiné la
contagiosité de trois autres
comportements distincts : l'étirement, le
grattage et le tremblement. Un total de 44
observations de 20 minutes a été
réalisé dans les deux groupes,
dont 28 le matin et 16 l'après-midi.
L'heure et l'occurrence de tous les
comportements de chaque oiseau ont
été codées, et le
schéma temporel de chaque comportement
dans les deux groupes a ensuite
été analysé pour
évaluer le degré de contagion
sociale. Globalement, nous n'avons trouvé
aucune preuve de contagion des
bâillements, des étirements, des
grattages ou des secousses. Cependant, les
bâillements étaient relativement
peu fréquents par observation (0,052
± 0,076 bâillements/oiseau) et des
méthodes expérimentales devraient
donc être utilisées pour
étayer cette constatation.
Introduction
The overt and reflexive matching of
behaviors among conspecifics, also referred to
as behavioral contagion [1], is common
among social species and could provide fitness
advantages to group members [2]. In
particular, contagious behaviors may serve
important functions in synchronizing activity
patterns and facilitating collective vigilance
within groups [3,4,5]. Although the
study of contagious behaviors has focused
primarily on mammalian species
[6,7,8,9,10], a number of studies have
also found evidence for behavioral contagion
among birds [11,12,13,14,15,16].
Perhaps the exemplar of contagious behavior
is yawning. In humans, seeing, hearing, or even
thinking about others yawning triggers contagion
[17,18,19]. Among non-human primates,
experimental evidence for contagious yawning has
been documented in chimpanzees
[6,20,21], bonobos [22], and
orangutans [23]. Experimental studies
have also shown evidence for yawn contagion in a
subline of high-yawning Sprague Dawley rats
[24] as well in as domesticated dogs in
response to human yawns [25], but not to
conspecifics [26]. Yawn contagion has
been further reported within observational
studies of gelada baboons [27], captive
wolves [28], domesticated pigs
[29], and African lions [3].
Limited evidence for contagious yawning has also
been documented in African elephants
[30], southern elephant seals
[31], and domesticated sheep
[32]. Some other mammalian species that
have been studied for yawn contagion, but have
revealed no evidence for this effect, include
common marmosets, ring-tailed and ruffed lemurs,
as well as lowland gorillas
[33,34,35].
To date, the only evidence for contagious
yawning in a non-mammalian species is in
budgerigars (Melopsittacus undulatus). An
initial observational study found that yawns
were temporally clustered in a captive flock,
and that the clumping of yawns could not be
explained by circadian factors [36]. A
subsequent study confirmed the presence of yawn
contagion in this species, using experimental
manipulations which included both live
interactions and video recordings of
conspecifics [37]. To our knowledge, no
other species of bird has been tested for
contagious yawning; thus, it remains likely that
yawn contagion is also prevalent within this
taxon.
One avian species that has been of
particular interest in behavioral research is
common ravens (Corvus corax). Ravens are a
moderately social species, with non-breeders
regularly forming groups during foraging and
roosting [38,39]. These birds remain
keenly attuned to the behaviors of group members
[40], and previous studies have shown
that they display collective behaviors in flock
formation [41] and feeding recruitment
[42], can cooperate extensively
[43], and are able to coordinate the
necessary actions for cooperation [44].
Moreover, recent studies have shown that ravens
synchronize their play behavior [45] and
display contagious allopreening [46].
However, some of the more prototypical
contagious behaviors, such as yawning, have yet
to be examined in this species. Ravens represent
a good candidate for the study of contagious
yawning, given that this response has been
linked with empathy and emotional contagion
[7,8,47,48], and recent studies have
shown that these birds display both positive and
negative forms of emotional contagion
[49,50]. Similarly, ravens show complex
social cognition [38,40,51,52], and some
of their socio-cognitive skills, such as
consolation and emotional contagion
[49,53], seem to be linked to empathy,
to some degree [28,54].
Therefore, the current study sought to
investigate the presence of contagious yawning
in captive groups of juvenile common ravens.
Raven juveniles spend the first years of their
lives in flocks, before they might establish a
pair bond and acquire a territory. The juvenile
period is, in fact, the most social period for
ravens [39], and in these flocks, they
form multiple differential social bonds. Thus,
during this developmental stage, these birds
would specifically benefit from any advantages
related to behavioral contagion, making the
animals selected for this study the best sample
for examining contagion.
In addition to yawning, the contagiousness
of the following three behaviors was also
examined: stretching, scratching, and shaking.
Stretching is often associated with yawning
across species [55,56] and, in birds,
may function in promoting preparation for
flight. In addition, similar to yawning,
stretching has previously been shown to be
contagious among budgerigars [36,57,58].
Scratching is another behavior known to be
contagious both in humans [59] and other
mammalian species [31,60,61] but, to
date, has not been examined among birds. Similar
to stretching, contagious scratching has
previously been studied alongside yawn contagion
[62]. In addition, mirror neurons have
also been implicated in both responses
[63,64]. Lastly, shaking behavior,
representing a conspicuous shuttering of the
feathers, was examined, due to its common
occurrence and potential links to arousal and
group activity [65].
Using observational methods from previous
studies of behavioral contagion in budgerigars
[36] and marmosets [33], we
examined the temporal distribution of each of
these four behaviors to test for the presence of
non-random clustering or clumping through
behavioral runs that would be indicative of
contagion. In addition to assessing the social
influence on these responses, the naturalistic
frequency and circadian variation of these four
behaviors was examined for the first time.
Discussion
This study represents the second attempt to
measure contagious yawning and stretching, and
the first attempt to measure contagious
scratching and shaking, in a species of bird.
Despite prior studies reporting various forms of
behavioral contagion among ravens
[45,46], the current study did not find
evidence for contagious yawning, stretching,
scratching, or shaking in this species. While
each behavior was significantly clustered in
time for at least one of the observations,
combined probability analyses (taking into
account the probability values from across all
observations) definitively revealed no overall
effect of contagion. This was true when
examining both the distribution at 30 s and at
the less conservative 60 s bins (see
Supplementary Materials).
In addition to addressing behavioral
contagion, the current findings also provide the
first account of the naturalistic frequency of
these behaviors in this species, albeit among
small groups in captivity. The observational
data collected here suggest that in each hour,
ravens yawn 1.6 times, stretch 10.7 times,
scratch 12.2 times, and shake 20.3 times, on
average. However, there was large individual
variability in the expression of these behaviors
(Table 2). Yawning and stretching occurred with
relatively equal frequency in both the morning
and afternoon hours, while scratching and
shaking were both more common in the afternoon.
In comparison to the budgerigar, in which there
is comparable avian data for the relative
frequencies of yawning and stretching
[36], the rate of stretching for ravens
was highly similar, while yawns were only about
half as frequent. In fact, the majority of the
birds (6/10) in the current study did not yawn a
single time across the 44 observations.
Additionally, budgerigars displayed an increase
in yawn frequency as the day progressed
[36], while there was no difference in
the frequency of yawning among ravens between
the morning and afternoon observations. Whether
ravens truly deviate from the pattern observed
in budgerigars would require a better
investigation of ravens' activity patterns,
particularly since the current study did not
encompass many observations in the afternoon, or
any between 11:30 and 15:00.
The absence of yawn and stretch contagion in
ravens is also in contrast to observational and
experimental studies in budgerigars
[36,37]. However, potential comparative
differences in these responses are to be
expected, based on ecological factors and
evolutionary history [5]. While ravens
are highly gregarious and possess sophisticated
social cognition [38,39,52], they live
in much smaller groups composed of pair bonds
and display less collective behavior in
flocking, compared to budgerigars [71].
Given that contagious yawning and stretching are
thought to promote motor synchrony [3]
and collective vigilance [57,58], this
could explain the difference between the two
species. Nevertheless, ravens do tend to
cooperate in these small parties when scavenging
on large prey that is monopolized by pair-bonded
individuals or large predators [72],
which does require coordination and vigilance
that may be enhanced by contagious yawning.
Additionally, the social structure of ravens,
with their fission&endash;fusion spatial and
temporal dynamics [39,73], does resemble
that of chimpanzees [74], which do show
contagious yawning [8,20,21].
Together, these conflicting comparative
findings cast doubt on the purported link
between contagious yawning and emotional
contagion [8] and suggest that these
processes are independent. While some
experimental studies have reported emotional
contagion among ravens [49,50], to date,
there is no evidence for this capacity among
budgerigars. Instead, contagious yawning may be
tied to bodily synchrony only [75],
which budgerigars display when interacting with
conspecifics [76].
Given the inherent limitations of
observation research, experimental methods
should be performed in the future to support the
null findings for contagion effects. In
particular, the overall occurrence of yawning
was quite low, limiting the ability to
effectively analyze the social influence of this
response. Generally, we cannot rule out that our
sample size, though large by the standards of
ravens in captivity, was too small to detect a
significant effect. To a lesser extent, the same
issue could have applied to all the other
behaviors as well (though the frequencies for
these were much higher). Future experimental
research could also examine different time
scales at which subsequent behaviors should be
considered contagious. Due to the outdoor
aviary, there were influential factors to be
considered: throughout the observational study,
the temperature was not constant, and this is
known to influence yawning in birds
[77,78]. Parasite load could also have
had an influence on scratching levels.
Furthermore, the two compartments of the aviary
were not completely visually nor acoustically
separated; therefore, it is possible that
adjacent behaviors between the groups could have
occurred and gone unnoticed during the
experimental sessions. These factors, however,
were not likely to obfuscate our results
significantly, since the ravens' visual access
between compartments was still largely
obscured.
Conclusions
Overall, this study represents the second
attempt to measure contagious yawning in birds.
The temporal analyses presented here do not
suggest the presence of contagious yawning, nor
any of the other behaviors measured. Given the
low frequency of yawning and the limitations of
observation research, experimental setups are
needed to confirm and clarify these findings,
i.e., by using live birds or video recordings as
a target stimulus. Nonetheless, this study
revealed novel effects with respect to the
naturalistic frequency and circadian variation
of some everyday behaviors in juvenile common
ravens.
