Among some haplorhine primates, including
humans, relaxed yawns spread contagiously. Such
contagious yawning has been linked to social
bonds and empathy in some species. However, no
studies have investigated contagious yawning in
strepsirhines. We conducted an experimental
study of contagious yawning in strepsirhines,
testing ring-tailed and ruffed lemurs (n = 24)
in a paradigm similar to one that has induced
contagious yawning in haplorhines. First, in a
control experiment, we investigated whether
lemurs responded to projected video content in
general (experiment 1). We showed them two
videos to which we expected differential
responses: one featured a terrestrial predator
and the other a caretaker holding food. Next, to
test for yawn contagion, we showed individual
lemurs life-size video projections of groupmates
and con- specific strangers yawning, and control
footage of the same individuals at rest
(experiment 2). Then, to examine whe- ther a
group context might enhance or allow for
contagion, we exposed subjects to the same
videos in a group setting (experiment 3). Lemurs
produced alarm vocalizations and moved upward
while viewing the predator, but not the
caretaker, demonstrating that they do perceive
video content meaningfully. However, lemurs did
not yawn in response to yawning stimuli when
tested alone, or with their groupmates. This
study provides preliminary evidence that lemurs
do not respond to yawning stimuli similarly to
haplorhines, and suggests that this behavior may
have evolved or become more exaggerated in
haplorhines after the two major primate lineages
split.
Introduction
Yawning is an activity common to most
vertebrates (Baenninger 1997; Smith 1999; Gallup
2011) yet its physiological and social functions
are still debated. For instance, yawning is
purported to prevent respiratory infections and
to increase oxygen levels in the blood and brain
(Baenninger 1997; Smith 1999; Gallup 2011). In
some species, yawns also convey important social
or emotional information. A yawn might be given,
for example, by a male baboon (Papio
cynocephalus) during a threatening dominance
display (Altmann 1967), by a captive chimpanzee
who has just heard social commotion among her
neighbors (Baker and Aureli 1997) or by a pet
dog who is anxious when separated from his owner
(Lund and Jørgensen 1999).
Animals may also produce different types of
yawns in different contexts. For example, after
social conflicts, gelada monkey males often
vocalize and then yawn, showing their canines,
while female geladas yawn when affiliatively
lip-smacking and grooming others (Leone et al.
2014). Sometimes, however, yawns appear to serve
no clear physiological or social function. In
these cases, for many species, including those
described above, yawns that occur in a relaxed
context spread contagiously from individual to
individual (Palagi et al. 2009).
In humans, yawn contagion is so powerful
that people yawn when watching videos of others
yawning, when reading about yawning, or when
being instructed to think about yawning (Provine
1986). Such non-conscious contagion has been
linked to a basic level of empathy (de Waal
2008). The connection to empathy is supported by
evidence in humans: subjects who yawn in
response to videos of others yawning have fewer
schizotypical personality traits and exhibit
better perspective-taking skills (Platek et al.
2003). In addition, contagious effects are more
powerful among individuals who share social
bonds. For instance, humans are more likely to
yawn in response to the yawns of friends and
family than acquaintances (Norscia and Palagi
2011). Given its connection to empathy and
sociality, comparative data on contagious
yawning may yield insights into social and
cognitive evolution.
It is important to note that while species
from birds, to fish, to snakes produce long,
gaping mouth movements that we identify as
yawns, it is unclear whether those movements
represent the same physiological processes
across taxa (Baenninger 1997; Smith 1999). For
instance, among mammals, carnivores seem to yawn
more frequently than herbivores (Baenninger
1997). Although yawning may serve different
functions across species, contagious yawning is
nevertheless found in a wide range of
species.
Observational studies have found contagious
yawning in taxa as diverse as birds and bonobos.
In captivity, budgerigars, which form cohesive
flocks in the wild, are observed to yawn and
stretch after conspecifics have yawned and
stretched (Miller et al. 2012). Wolves also
contagiously yawn, doing so more often if they
share a close social bond with the initial
yawner (Romero et al. 2014). Among primates,
captive bonobos and geladas are more likely to
yawn after conspecifics do, particularly if
those conspecifics are kin or preferred social
partners (Palagi et al. 2009, 2014; Demuru and
Palagi 2012).
Contagious yawning can also be induced
experimentally. Both chimpanzees and stumptail
macaques yawn when shown videos of yawning
conspecifics (Anderson et al. 2004; Paukner and
Anderson 2006; Amici et al. 2014). Importantly,
authors noted that these stumptail macaques also
displayed nervous behaviors while yawning,
suggesting that yawns produced could have been
motivated by social stress, so it is unclear
whether these yawns were induced by empathy-like
capacities (Paukner and Anderson 2006). In a
similar video playback experiment, chim- panzees
were more likely to yawn after watching footage
of a yawning groupmate than a yawning stranger
(Camp- bell and de Waal 2011).
Contagious yawning is not only induced by
conspecifics. Captive chimpanzees with human
caretakers are more likely to yawn in response
to a familiar chimpanzee or human than to an
unfamiliar chimpanzee (Campbell and de Waal
2014). Dogs may yawn when watching a human
experimenter yawn in person (Joly-Mascheroni et
al. 2008) and do so more often when the human is
familiar (Romero et al. 2013: although see Harr
et al. 2009a, b; O'Hara and Reeve 2011). These
interspecific results further emphasize the
possibility that emotional bonds influence
contagious behavior since dogs may be closely
bonded to their human owners and captive apes to
their human caretakers.
Understanding how and when such rudimentary
empathetic capabilities evolved is key to
understanding the evolution of complex social
cognition, as both empathy and cognition are
entwined with the evolution of sociality
(Seyfarth and Cheney 2013). The comparative
method affords a powerful approach for answering
questions about how, when, and why particular
cognitive capabilities have evolved (MacLean et
al. 2012a, b, 2014). This approach requires data
from broad phylogenetic samples in order to
estimate the evolutionary origins of particular
traits. Among our closest relatives, nonhuman
primates, only haplorhines have been the focus
of research on contagious yawning. No study has
examined whether contagious yawning occurs in
strepsirhines&emdash;the other major primate
lineage including lemurs, lorises, galagos, and
pottos. Therefore, comparative data from
strepsirhines will bear importantly on whether
contagious yawning is common to all primates or
unique to the haplorhine lineage.
Compared to haplorhines, little is known
about yawning behavior in general in
strepsirhine primates.
However, a recent study closely examined the
context of yawns that occurred among wild
ring-tailed lemurs (Lemur catta) and Verreaux's
sifakas (Propithecus verreauxi) (Zannella et al.
2015). Like many animals described above, lemurs
of both species yawned after events expected to
produce anxiety, such as within-group aggressive
incidents, encounters with unfamiliar stimuli,
or attacks by predators (Zannella et al. 2015).
These recent findings corroborate previous
reports that ring-tailed lemurs occasionally
yawn during intergroup encounters (Pereira and
Kappeler 1997; Nunn and Deaner 2004). In
addition to yawning when anxious, both ring-
tailed lemurs and sifakas, like other animal
species, yawned when they changed behavioral
state in relaxed contexts, such as rising from
rest to walk to a nearby place (Zannella et al.
2015).
Here, we used a video playback experiment
comparable to those used in haplorhines to
determine whether conta- gious yawning occurs in
free-ranging, captive ring-tailed lemurs and
ruffed lemurs (Varecia variegata) in relaxed
settings. Ring-tailed lemurs form large,
hierarchical, cohesive social groups (Sauther et
al. 1999), while ruffed
lemurs live in fission fusion communities
(Vasey 2007). Given their complex social
systems, these two species are ideal candidates
to test whether contagious yawning occurs in
strepsirhines.
The evidence for contagious yawning in
haplorhines as well as several diverse
non-primate species suggests that the phenomenon
is evolutionarily ancient and would thus appear
in strepsirhine as well as haplorhine primates.
Furthermore, lemurs show evidence of social
learning (Stoinski et al. 2011; Kendal et al.
2010) and other forms of complex social
cognition (Sandel et al. 2011; MacLean et al.
2012a, b; Bray et al. 2014), suggesting that
they likely possess basic empathetic processes.
Thus, we expected that both ring-tailed lemurs
and ruffed lemurs would demonstrate contagious
yawning.
Discussion
Lemurs did not yawn contagiously in response
to videos of yawning groupmates or strangers.
Our findings are consistent across individual
and group contexts, with large samples, and
between two of the most socially complex
strepsirhine species. However, lemurs did
demonstrate that they respond meaningfully to
video footage in general; they moved upward and
made alarm calls while viewing footage of a
predator but not a caretaker. This study pro-
vides the first evidence that lemurs do not
respond to yawning video stimuli in the same way
as haplorhine primates, and suggests the
possibility that strepsirhines do not yawn
contagiously.
Given that many social animals, including
wolves and budgerigars in addition to haplorhine
primates, yawn contagiously with conspecifics,
it seems surprising that lemurs did not do so.
However, several aspects of interindividual
social relationships in lemurs differ in
relevant ways from those of haplorhines and
other social mammals.
First, even lemurs species that live in
large social groups appear to engage in fewer
cooperative activities than haplorhines and are
characterized by more within-group competition
(for review, see: Fichtel and Kappeler 2010).
For example, ring-tailed lemurs form matrilineal
groups where females, like female Old World
monkeys, affiliate most often with kin, grooming
with them and maintaining close spatial
proximity to them frequently. Despite the
similarities of these affiliative kin behaviors,
ring-tailed lemurs, unlike Old World monkeys,
rarely recruit or assist others in coalitionary
aggression. Ring-tailed lemur mothers rarely
support even their daughters in fights (5 % of
the time, Nakamichi and Koyama 1997).
Consequently, ring-tailed lemur daughters,
unlike Old World monkey daughters, do not always
rank immediately below their mothers (Nakamichi
and Koyama 1997). The absence of such alliances
in lemurs contrasts not only to certain Old
World monkeys, but to many social mammals who
form coalitions against others, including
chimpanzees and wolves discussed above (for
review, see: Harcourt and De Waal 1992).
In addition to a lack of alliances, lemurs
show minimal post-conflict affiliation with
other individuals (Fichtel and
Kappeler 2010). After aggressive conflicts,
individuals of a wide range of species show
increased affiliation with their former
opponents or with other groupmates, including
baboons (Castles and Whiten 1998), long-tailed
macaques (Aureli and van Schaik 1991),
chimpanzees (De Waal and van Roosmalen 1979),
dolphins (Tamaki et al. 2006), rooks (Seed et
al. 2007), domestic horses (Cozzi et al. 2010),
goats (Schino 1998), hyenas (Hofer and East
2000), dogs (Cools et al. 2008), and wolves
(Cordoni and Palagi 2008). This affiliation is
thought to reduce anxiety and future aggression
(e.g., Castles and Whiten 1998) and has
implications for group cohesion.
Several captive studies have examined
post-conflict affiliation in ring-tailed lemurs
specifically. One study found no evidence for
affiliation in the 10 min following a conflict,
a typical time length examined in species above
(Kappeler 1993), but a follow-up study on the
same group observed opponents for 70 min
post-conflict and found that more affiliation
occurred in post-conflict periods compared to
control periods (Rolland and Roeder 2000). A
later study reexamined post-conflict association
in ring-tailed lemurs at the dyadic level with a
larger sample size and found that breeding
seasonality may influence the behavior: pairs of
ring-tailed lemurs showed increased affiliation
after a conflict in the social group with
breeding females but not in the social group
with lactating females who are less likely to be
tolerant of males (Palagi et al. 2005). Other
lemur species, including redfronted brown lemurs
and Verreaux's sifakas, do show some
post-conflict affiliation (Kappeler 1993; Palagi
et al. 2008). Post-conflict association has not
to our knowledge been studied in ruffed lemurs,
but like ring-tailed lemurs, this species also
experiences seasonal shifts in social behavior
(Vasey 2007).
Given these peculiarities of lemur social
relationships, one interpretation of our main
result is that contagious yawning capabilities
evolved in haplorhine primates after the lineage
split from strepsirhines and that the phenomenon
seen in other distantly related vertebrates like
budgies and wolves is the result of convergent
evolution linked to the social relationships
between individuals in these species;
budgerigars form cohesive flocks and wolves are
obligate carnivores that acquire food by hunting
cooperatively with groupmates (Wyndham 1980;
Peterson and Ciucci 2003). Another possibility
is that contagious yawning occurred at very low
levels in a primate ancestor and became
exaggerated as the result of selection in some
social species and not others. In our study,
yawns occurred infrequently, but importantly,
they occurred exclusively in conditions where
lemurs watched yawning stimuli. Although this
evidence certainly does not suggest that
contagious yawning is a strong phenomenon in
lemurs, it is consistent with the possibility
that contagious yawning is evolutionarily
ancient but has evolved to be more prevalent and
easily elicited in haplorhines and other social
species, but not in ring-tailed or ruffed
lemurs.
An alternative explanation for our results
is that lemurs do yawn contagiously but that
visual stimuli alone are not sufficient to
induce such behavior. Some research suggests
that this is the case for pet dogs.
Joly-Mascheroni et al. (2008) found that 72 % of
dogs tested yawned contagiously in response to a
live human who yawned, but in a later study Harr
et al. (2009a, b) showed 15 dogs video footage
of unfamiliar dogs and humans yawning and only
one subject yawned contagiously. Video was
insufficient to produce contagious yawning in
dogs. Yet, dogs, like lemurs in this study, do
produce responses to video in other contexts.
For instance, dogs pay attention to a familiar
human's communicative cues that occur onscreen
(Pongracz et al. 2003). This suggests that dogs
can perceive and respond to the content of
videos, but that a contagious yawning response
requires additional cues. For instance, Silva et
al. (2012) found that auditory cues were
integral to the contagious yawning response in
dogs; auditory play-backs of humans yawning
alone caused dogs to contagiously yawn.
Like pet dogs, lemurs may produce some but
not all natural behaviors in response to video
alone, but require other cues, not conveyed in
video, to yawn contagiously. Our videos did not
include sounds and it is possible that auditory
cues are important for contagious yawning in
lemurs. However, unlike dog yawns, lemur yawns
are silent to human observers and solely visual
playbacks did induce yawning in apes and in
stumptail macaques (e.g., Anderson et al. 2004;
Paukner and Anderson 2006), though visual
stimuli are perhaps relatively more salient to
haplorhine compared to strepsirhine primates who
use olfaction to communicate important social
information (e.g., Drea and Scordato 2008).
Olfactory cues can induce yawning in rodents
(Moyaho et al. 2015) and lemurs sometimes yawn
when presented with sticks scent-marked by other
lemurs (Sandel, pers. comm.), though,
importantly, these yawn responses do not occur
in response to the yawns of groupmates and
likely represent phenomena different than
empathy-related contagious yawning investigated
here. Issues of the importance of auditory,
olfactory, and other cues in potentially
inducing contagious yawning in lemurs could be
informed through an observational study of
yawning in lemur social groups.
We hope this study will be the first of many
that explore across a range of species the
distribution of contagious yawning in order to
understand its phylogenetic origin and ultimate
function (MacLean et al. 2012a, b).
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