Contagious yawning is triggered by others
yawning, and it has previously been reported in
humans, primates and several experimental and
companion mammals. Whereas it might be a
response to an innate releasing mechanism,
contagious yawning is also considered to involve
emotional contagion. Here, we demonstrate that
sheep, the animal model of livestock animals,
also experience contagious yawning. Twelve adult
castrated Corriedale sheep were used in this
study. Pairs of sheep were adjacently restrained
with or without a wooden divider panel to shield
them from viewing the other. Their behaviors
were video-recorded for 3_days in each
condition. Sheep yawned 2.0_±_1.1 and
1.2_±_1.1 times/day/head in the unshielded
and shielded conditions, respectively.
Unshielded restrained sheep yawned within 1_min
after the other one 11.1% of the time, while
shielded pairs did not exhibit contagious
yawning. Rumination was also highly synchronized
under the unshielded condition. These data
reveal that contagious yawning and behavioral
synchronicity occur in ruminants like sheep,
making them a suitable animal model to
investigate contagious yawning and the
underlying mechanism.
Contagious yawning is a well-known
phenomenon where yawning is triggered by another
individual yawning. It has been described in
many mammalian species such as humans (Provin
1986; Senju et al. 2007; Norscia & Palagi
2011), chimpanzees (Anderson et al. 2004;
Campbell & de Waal 2011), gelada baboons
(Palagi et al. 2009), bonobos (Demuru &
Palagi 2012) macaque monkeys (Paukner &
Anderson 2006), wolves (Romero et al. 2014),
domestic dogs (Joly-Mascheroni et al. 2008;
Romero et al. 2013), rats (Moyaho et al. 2014)
and budgerigars (Miller et al. 2012).
While spontaneous yawning is common among
vertebrate species (Baenninger 1987; Heusner
1946), it is unknown whether more species could
yawn contagiously or not. Contagious yawning is
reported to be a response to an innate releasing
mechanism (Provine 1986; Bartholomew &
Cirulli 2014), and it is considered to be based
on the organism's capacity for empathy or
emotional contagion (Amici et al. 2014; Madsen
et al. 2013).
Emotional contagion is the perception of
expressive behaviour to transfer emotional
states from one individual to another (Blakemore
& Decety 2001). Indeed, contagious yawning
is not observed in young children (Anderson
& Meno 2003; Millen & Anderson 2011) or
patients with autism spectrum disorders (Senju
et al. 2007) although spontaneous yawning is
observed even in foetuses (Sherer et al. 1991).
Thus, contagious yawning could be a good tool to
assess the levels of emotional contagion.
The empathetic behaviours appear to emerge
developmentally and phylogenetically (Gallup
1998; Provinelli et al. 1994; Premack &
Woodruff 1978). Since there is convincing
evidence for self-other recognition and empathy
in primates (Gallup 1970; Bard et al. 2006),
these behaviours are mainly investigated using
humans and primates. Although some researchers
recently reported emotional contagion,
particularly related to contagious yawning in
other species such as domestic dogs
(Joly-Mascheroni et al. 2008; Romero et al.
2013), rats (Moyaho et al. 2014) and budgerigars
(Miller et al. 2012), there is still no report
in ungulate species to our knowledge.
Among those species, sheep are good
experimental animals because they have stable
genetic background and they are easily supplied,
and it is known to have social facilitation and
concurrent behaviours (Rook & Penning 1991;
Michelena et al. 2006; Gautrais et al. 2007;
Clayton 1978). It is reported that ruminating,
resting, grazing, and walking are synchronised
within its familiar herds of sheep (Rook &
Penning 1991; Michelena et al. 2006; Gautrais et
al. 2007). Sheep are also reported to have
developed social recognition skills using visual
facial cues (Kendrick 2004; Broad et al. 2000;
Peirce & Kendrick 2002). These reports lead
us to the hypothesis that sheep also experience
contagious yawning.
This study examined whether contagious
yawning occurs in sheep. In the experiments, a
pair of sheep was video recorded while they were
adjacently restrained with or without a wooden
divider panel that shielded them from their
stall mate's behaviour. Ruminating, resting, and
barking behaviours were also observed. To
clarify whether yawning contagion could be
derived from visual stimuli, their behaviours
were also observed while they were restrained
next to a television monitor showing a video
clip of a sheep that was yawning or
ruminating.
DISCUSSION
Our findings revealed that contagious
yawning occurs even in quadrupedal animals such
as sheep. In this study, unshielded restrained
sheep yawned within 1 minute after the other one
11.1% of the time, while shielded pairs never
exhibited contagious yawning. Moreover, the
number of contagious yawns in the unshielded
condition was significantly higher than that of
the randomised data, while there was no
significance in the shielded condition. These
data reveal that contagious yawning occurs in
ruminants like sheep, also indicating that sheep
is one of suitable animal models to investigate
contagious yawning and the underlying mechanism.
Since primates and dogs are not so suitable as
experimental animas because of animal facility
limitations and ethical problems, sheep could be
a useful model for basic research into
contagious yawning.
Stress is reported to change animal
behaviours in the most situations. Generally,
rumination are mostly observed when the animals
are relaxed (Provine 1986; Bartholomew &
Cirulli 2014; Gautrais 2007). Restraint is
well-known as one of stressors and reported to
induce the plasma cortisol level in sheep
(Matthews & Parrott 1991). Therefore, the
restraint stress might not have some effects on
all the results. On the other hand, sheep are
also prone to isolation stress (da Costa et al.
2004). In this study, the total numbers of
rumination and yawning were significantly larger
under the unshielded condition in comparison
with the shielded condition. Since sheep were
only isolated under the shielded condition,
their behaviours would be affected by
unignorable isolation stress. However, the
relationship between stress and yawning is still
under controversy. While yawning occurs
frequently when the human are under stress or
tired (Thompson 2011), the stress-induced yawn
is not so reproduced in dogs (Silva et al.
2013). In this study, the total number of
yawning was larger under the unshielded
condition. It is implied that yawning occurs
infrequently under the isolation stress in
sheep, which could be opposite from other
species. In any case, our data could suggest
that contagious yawning occurs in sheep because
the accuracy of contagious yawning was higher
than the randomized data only under the
unshielded condition.
The yawn contagion prevalence was 11.1% in
this study. In the previous report, the rates
are 45-55% in humans (Provin 1986; Senju et al.
2007; Norscia & Palagi 2011), and 33% in
chimpanzees chimpanzees (Anderson et al. 2004; 1
Campbell & de Waal 2011). Since these
results are derived from different conditions
and statistical tests, they cannot be compared
directly. Nevertheless, it is likely that the
ratio of contagious yawning in sheep is lower
than others. At least several reasons are
considered as follows.
Sheep could not yawn during rumination. When
the yawns that occurred during the other's
ruminating were excluded, 30.8% of yawns were
synchronised (8/26 yawns), which is subtle
nearer to other data.
They were examined under the restraint
stress. Although dogs did not change contagious
yawning frequency under the stress in the
previous report (Silva et al. 2013), the
different type of stress or species might have
some effect of stress on contagious yawning
occurrence.
Sheep brain might have more primitive or
simple yawning contagion mechanism than
primates. Further research is needed which
reason is more affirmative.
Previous report about social dynamics
indicates that activity synchronicity is
considered to be necessary for social cohesion
in gregarious species (Clayton 1978). It has
been reported that ruminating, resting, grazing,
and walking are synchronised in sheep herds
(Rook & Penning 1991; Michelena et al. 2006;
Gautrais et al. 2007). Indeed, it was observed
that the other behaviours than yawning such as
ruminating were also synchronised in this study.
The relationship of mechanism between social
dynamics and contagious yawning remains
unknown.
As there are many reports about social
dynamics in sheep, further study in sheep can
reveal difference or commonality of them. The
present results do not clarify which factor(s)
triggered contagious yawning. It could be
induced by viewing others' yawns (Provine 1986;
Senju et al. 2007) and/or hearing yawning sounds
(Arnott et al. 2009). Even video images or
computer animations of yawning induce contagious
yawning in human and primates (Senju et al.
2007; Paukner & Anderson 2006; Campbell et
al. 2009). The wooden board placed between the
partnered sheep in this study visually shielded
the neighbour's behaviour and partially blocked
aural information. To clarify the effect of
visual stimuli on contagious yawning, the sheep
were shown a muted video clip of another sheep
yawning or ruminating as a control.
Unfortunately, there were no significant
differences between video contents. Although
sheep are reported to have social recognition
skills involving the use of visual cues from
others' faces (Kendrick 2004; Broad et al. 2000;
Peirce & Kendrick 2002), no relevant studies
have employed a video-based approach. It is
suggested that sheep could not just recognise a
face in the video clips under our experiment
condition or visual effects are not sufficient
to induce contagious yawning in sheep. Further
studies are needed to clarify the mechanism of
contagious yawning.
In conclusion, our findings suggest that
contagious yawning occurs in sheep. Therefore,
sheep could be a good animal model to
investigate contagious yawning and collect
important information for animal welfare and
livestock management.
