- This study reports the first experimental
exploration of possible contagious yawning in
monkeys. Twenty-two stumptail macaques (Macaca
arctoidas) were presented with video clips of
either yawns or control mouth movements by
conspecifics. At a group level, monkeys yawned
significantly more often during and just after
the yawn tape than the control tape.
Supplementary analysis revealed that the yawn
tape also elicited significantly more
self-directed scratching responses than the
control tape, which suggests that yawning might
have been caused by tension arising from viewing
the yawn tape. Understanding to what extent the
observed effect resembles contagious yawning as
found in humans and chimpanzees requires more
detailed experimentation.
-
- 1. INTRODUCTION
-
- Observational studies of yawning in monkeys
have provided no evidence that the behaviour is
contagious, which is in contrast to the picture
in humans (Baenninger 1987; Troisi et al. 1990;
Deputte 1994). Yawning is considered to be
contagious only in humans by some authors
(Lehmann 1979; Walusinski 2004), but this view
was recently challenged by a study on
chimpanzees (Anderson et al. 2004). The latter
study used an experimental video-based approach
similar to that used for studying contagious
yawning in humans (e.g. Provine 1986; Platek e:
al. 2003). individually tested adult female
chimpanzees watched on a television monitor a
series of yawns or a series of non-yawn facial
expressions by chimpanzees. Two of the six
subjects showed a significantly greater
frequency of yawning in response to the yawn
stimulus tapes compared to the non-yawn tapes.
The reported contagion effect in 33% of adult
chimpanzees compares with 45-60% typically
reported for humans.
-
- Some authors consider contagious yawning to
be a response to an innate releasing mechanism
(e.g. Provine 1986). Another hypothesis about
contagious yawning in humans is that it is based
on empathy (Lehmann 1979). In other words,
seeing another individual yawn makes one think
about oneself yawning, which elicits the
response. The likelihood of yawning in response
to video images of yawning is positively
correlated with measures of empathy and visual
self-recognition (Platek et al. 2003). Recent
studies investigating the neural correlates of
contagious yawning also support the empathy
hypothesis in that activation was found in areas
related to selfprocessing when viewing someone
yawn (Platek et al. 2005), but not in the human
mirror neuron system, which suggests that
yawning is not a truly imitative act (SchUrmann
et al. 2005). Since there is convincing evidence
for both self-recognition and empathy in
chimpanzees but not in monkeys (De Waal 1996;
Anderson & Gallup 1999), it may be predicted
that, unlike chimpanzees and humans, monkeys do
not show contagious yawning.
-
- Like other macaque species (Hadidian 1980;
Deputte 1994), stumptail macaques (Macaca
arctoides) yawn when waking up and occasionally
throughout the day. Also, especially in adult
males, 'tension yawns' may occur during
potential or actual agonistic situations
(Bertand 1969). Yawning occurs frequently during
staged male-male encounters, with the dominant
individual producing more yawns than the
subordinate (Adams & Schoel 1982). There is
no suggestion in the literature that stumptail
macaques are prone to contagious yawning;
however, no relevant study in any monkey species
has used a video-based approach of the type that
has been used with humans and chimpanzees. Here,
we report the first such attempt. Based on the
emerging view that contagious yawning is
associated with self-recognition and empathic
abilities, we predicted that there would be no
evidence of yawning elicited by video images of
yawning in stumptail macaques.
 - 2. MATERIAL AND METHODS
-
- (a) Subjects
-
- Twenty-two stumptail macaques (Macaca
anroides) were tested, 18 females (16 adult, 2
sub-adult) and 4 males (2 adult, 1 sub-adult, 1
infant), all captive-born and group-reared (mean
age: 13 years, range 1-23 years). They were
housed in five social groups of 2, 3, 3, 5 and 9
individuals in large indoor enclosures (2.7X2.8X
4.8m), famished with wooden logs, metal shelves,
ropes and ladders. The monkeys also had access
to a cage system in the adjacent room via slide
doors. They were fed once a day with fresh fruit
and vegetables, monkey pellets, dried fruits,
seeds and nuts, and given scatter-feeds (seeds)
in the late afternoon. Water was available ad
libitwn.
-
-
- (b) Apparatus
-
- The largest group of monkeys was filmed on
two separate days, and clips were edited into
one yawn tape and one control tape. The yawn
tape contained 10 naturally occurring yawns by
adult male, adult female and juvenile monkeys
(captured in relaxed contexts, not tension
yawns; see figure la), separated by 5 s of
black, blank screen. Each yawn was on average
4.5 s long. The control tape consisted of 10
non-yawn facial movements by adult male, adult
female and juvenile monkeys, and contained
scenes such as teeth chattering, vocalizations,
or chewing (no foods visible; see figure lb).
These clips were also separated by 5 s of black,
blank screen and were matched for total length
(1 min 30 s) with the yawn clips. A 17" TFT
Colour LCD monitor (S76OA) was used to present
these videos to the monkeys.
-
-
- (e) Procedure
-
- Monkeys were tested twice daily, once in the
morning and once in the afternoon ca 2 h after
their daily feed at lunchtime. They were only
tested when they appeared to have finished
eating and foraging. The video stimuli were
presented through a viewing window (IX 0.88 m)
at the front of the rooms which allowed
unobstructed visual access to the entire room.
Doors to the adjacent cage area remained open
throughout the experiment. This arrangement
meant that some monkeys missed part or whole of
the video presentation, and these individuals
were excluded from data collection for those
sessions. Monkeys were presented with either the
yawn video or the control video, with order of
presentation counterbalanced between groups,
followed by 3 min of blank screen. An
experimenter positioned at the viewing
window
 - 3. RESULTS
-
- No direct social responses were elicited by
any of the video clips. With the exception of
one adult female, all monkeys yawned at least
once during at least one test session. All
observed yawns were judged to be 'natural' yawns
by the experimenter. No 'threat yawns'
(associated with agonistic behaviours) were
observed. On average, each monkey yawned 2.4
times during or in the 3 min following the
control video, compared to 4.3 times for the
yawn video, which constitutes a significant
difference between conditions (Wilcoxon: z=
-2.33, p=0.02; figure 2). Overall, 13 monkeys
yawned more when presented with the yawn tape, 5
monkeys yawned more when presented with the
control tape and 4 monkeys showed the same
number of yawns in the two conditions. There was
no significant correlation between the number of
yawns and either age or dominance rank of the
monkeys. Sex of subject and familiarity with the
models also failed to significantly impact on
yawn frequency (all p>0.05).
-
- In the final six test sessions, the latency
of first yawn, the social context of yawns and
the number of self-scratching bouts were also
recorded for both conditions. These data
revealed that on average, the first yawn
occurred 2 min 26s into the yawn condition and 2
min 29s into the control condition. Further
yawns occurred on average every 49 s in the yawn
condition and every 67 s in the control
condition. Yawning monkeys always appeared
relaxed or resting, either sitting or lying down
alone, or huddling/being groomed by others.
There was a significant difference between
conditions in the frequency of self-directed
scratching, with the yawn condition (average
12.3 bouts) generating significantly more bouts
of scratching than the control condition
(average 9.1 bouts; Wilcoxon: z= - 1.97,
p=0.049). Fourteen monkeys scratched more in
yawn sessions, five scratched more in control
sessions, and three scratched equally often in
yawn and control sessions. However, there were
no correlations between the number of scratching
bouts and the number of yawns in the yawn
condition (Pearson: r=0.249, p>0.05) or the
control condition (Pearson: r=-0.013,
p>0.05).
-
- 4. DISCUSSION
-
- This is the first experimental demonstration
of yawning induced by video images of yawning
conspecifics in monkeys. Although there were no
significain differences between conditions for
any individual subject, there was a clear
increase in yawning in the yawn video condition
compared to the control video condition at group
level. This finding contradicts our prediction
of no effect. Also, although it is possible that
the monkeys were influenced by seeing yawning by
group members, any such effect is unlikely to
explain the difference between conditions.
-
- It is not clear from the present results
that a contagious yawning effect occurs as has
been observed in humans, and possibly
chimpanzees, as there was also a significant
increase in self-directed scratching in the yawn
sessions. Self-directed behaviours, including
scratching and yawning, are considered to be
indicators of tension or anxiety (Maestripieri
et al. 1992). The question then arises, why did
the monkeys show more self-directed behaviours
in the yawn condition than the control
condition? One possible reason is that the yawn
videotape contained more images of yawning by an
adult male (a total of six yawns) than the
control tape which contained images of an adult
male engaging in other acts (one non-yawn facial
movement). Yawning is a way of displaying the
canine teeth, and some yawns by adult males are
considered threat signals (Hall & DeVore
1965; Bertrand 1969). Conceivably, therefore,
increased yawning accompanied by scratching
during the yawn video might have been due to
greater uneasiness arising from seeing an adult
male yawning repeatedly. There is a clear need
for further experimentation on this issue, for
example presenting stimulus videotapes that
feature only one age-sex category (infants,
adult males, adult females) yawning or showing
other activities. Indeed, similar systematically
controlled experimentation on great apes would
clarify the extent to which these primates are
also prone to human-like contagious
yawning.
-
- The existence of a 'possible facilitative'
effect of seeing another individual yawn has
been alluded to in macaques (Hadidian 1980).
However, with the exception of tense male-male
situations (Darwin 1872/1999; Adams & Schoel
1982) in which yawning may be triggered as a
'canine contest', until now there has been no
evidence for the experimental elicitation of
yawning by visual conspeciflc stimuli in non-ape
primates. The subject clearly merits further
research, not only with the aim of clarifying
the psychological mechanisms underlying the
expression of yawning, but also because of its
implications for our understanding of the
emergence of empathic abilities in primates.
-
- Adams, D. B. & Schoel, W. M. 1982 A
statistical analysis of the social behavior of
the male stumptail macaque (Macaca arcwides).
Am. J. Primatol. 2, 249-273.
-
- Anderson, J. R & Gallup Jr, G. G. 1999
Self-recognition in primates: past and future
challenges. In Animal models of human emotion
and cognition (ed. M. Haug & R E. Whalen),
pp. 175-194. Washington, DC: American
Psychological Association.
-
- Anderson, J.
R, Myowa-Yamakoshi, M. & Matsuzawa, T.
2004 Contagious yawning in chimpanzees. Proc. R.
Soc. B 271(Suppl. 6), S468-S470. The Royal
Society Biology Letters may 2004
-
- Anderson
JR; Wunderlich D Food-reinforced yawning in
Macaca tonkeana American Journal of Primatology
1988; 16; 165-169
-
- Anderson JR
et al Psychological influences on yawning in
children Current
Psychology Letters Behaviour, brain,
cognition 2003; 2; 11
-
- Baenninger,
R. 1987 Some comparative aspects of yawning
in Betta splendens, Homo sapiens, Panthera leo,
and Papio sphinx. J. Comp. Psychol. 101,
349-354.
-
- Bertrand, M. 1969 The behavioral repertoire
of the stumptail macaque. Basel: Karger.
-
- Darwin,
C. 1872/1999 The expression of the emotions
in man and animals. London: HarperCollins.
-
- Deputte, B.
L. 1994 Ethological study of yawning in
primates. I. Quantitative analysis and study of
causation in two species of Old World monkeys
(Cercocebus albigena and Macacafascicularis).
Ethology 98, 221-245.
-
- De Waal, F. 1996 Good natured: the origins
of right and wrong in humans and other animals.
Cambridge, MA: Harvard University Press.
-
- Hadidian, J.
1980 Yawning in an Old World monkey, Macaca
nigra (Primates: Cercopithecidae). Behaviour 75,
133-147.
-
- Hall, K. R. L. & DeVore, I. 1965 Baboon
social behavior. In Primate behavior (ed. I.
DeVore), pp. 53-110. New York: Holt, Rinehart
& Winston.
-
- Lehmann, H. E.
1979 Yawning: a homeostatic reflex and its
psychological significance. Bull. Meninger Clin.
43, 123-136.
-
- Maestripieri,
D., Schino, G., Aureli, F. & Troisi, A.
1992 A modest proposal: displacement activities
as an indicator of emotions in primates. Anim.
Behav. 44, 967-979.
-
- Platek,
S. M., Critton, S. R., Myers, T. E. & Gallup
Jr. G. G. 2003 Contagious yawning: the role
of self-awareness and mental state attribution.
Cogn. Brain Res. 17, 223-227.
-
- Platek, S. M.,
Mohamed, F. & Gallup Jr, G. G. 2005
Contagious yawning and the brain. Cogn. Brain
Res. 2-3, 448-452.
-
- Provine, R
R. 1986 Yawning as a stereotyped action
pattern and releasing stimulus. Ethology 72,
448-455.
-
- Schürmann,
M., Hesse, M. D., Stephan, K. E., Saarela, M.,
Zilles, K, Han, R & Fink, G. R 2005
Yearning to yawn: the neural basis of contagious
yawning. Neuroimage 24, 1260-1264.
-
- Troisi, A.,
Aureli, F., Schino, G., Rinaldi, F. & de
Angelis, N. 1990 The influence of age, sex,
and rank on yawning behavior in two species of
macaques (Macaca fascicularis and M. fiiscata).
Ethology 86, 303-3 10.
-
- Walusinski,
O. 2004 Bâillements et pandiculations.
Brou (France): Oscitatio.
-
- -Arnott
SR et al. An investigation of auditory
contagious yawning Cognitive, Affective,
Behavioral Neurosci 2009;9(3):335-342
- -Anderson
JR et al Contagious yawning in chimpanzees
The Royal Society Biology Proc R Soc Lond B Biol
Sci 2004; 271 Suppl 6; S468-470
- -Anderson
JR et al Psychological influences on yawning
in children Current Psychology Letters
Behaviour, Brain, Cognition 2003;2:11
- -Anderson
JR, Matsuzawa T. Yawning: An Opening into
Empathy? Cognitive Development in Chimpanzees. T
Matsuzawa, M Tomonaga, M Tanaka Editors.
Springer 2006
- -Caswell
TA, The effects of status on yawning
behavior. Thesis 1991
- -Cialdini
RB, McPeek RW. Yawning, Yielding, and
Yearning to Yawn 1974 (non published)
- -Campbell
MW et al. Do chimpanzees yawn
contagiously in response
to 3d computer animations? 2008
- -Cooper NR,
Puzzo I, Pawley A Contagious yawning: the
mirror neuron system may be a candidate
physiological mechanism Medical Hyportheses
2008;71(6):975-976
- -Cooper NR,
Puzzo I, et al. Bridging a yawning chasm:
EEG investigations into the debate concerning
the role of the human mirror neuron system in
contagious yawning.Cogn Affect Behav Neurosci.
2012;12(2):393-405
- -Demuru E,
Palagi E. In Bonobos Yawn Contagion Is
Higher among Kin and Friends. PLoS One. 2012;
7(11): e49613
- -Dijksterhuis
A, Bargh JA The perception-behavior
expressway:automatic effects of social
perception on social behavior Advances in
Experimental Social Psychology
2001;33:1-40.
- -Estow,
S Jamieson JP, Yates JR Self-monitoring and
mimicry of positive and negative social
behaviors Journal of Research in Personality
2007;41(2):425-433
- -Gallagher
HL, Frith CD Functional imaging of theory of
mind Trends in Cognitive Scie.
2003;7(2):77-83
- -Giganti
F, Ziello ME Contagious and spontaneous
yawning in autistic and typically developing
children CPL 2009
- -Giganti
F, Zilli I. The daily time course of
contagious and spontaneous yawning among humans.
J Ethol 2011;29(2):215-216
- -Haker H, Kawohl W,
Herwig U, Rössler W. Mirror neuron
activity during contagious yawning-an fMRI
study. Brain Imaging Behav. 2012
- -Harr AL, Gilbert
VR Do dogs show contagious yawning ? Anim
Cogn. 2009;12(6):833-837
- -Helt MS, Eigsti
IM, Snyder PJ, Fein DA. Contagious yawning
in autistic and typical development. Child Dev.
2010;81(5):1620-1631
- -Iacoboni
M, G Rizzolatti Cortical mechanisms of human
imitation Science 24/12/99; 286
- -Joly-Mascheroni
RM, Senju A, Sheperd AJ Dogs catch human
yawns Biology letters Animal Behaviour
2008;4(5):446-448
- -Lindsay
SR Coping with fear and stress: licking and
yawning. Handbook of applied dog behavior and
training 2000
- -Madsen EA,
Persson T. Contagious yawning in domestic
dog puppies (Canis lupus familiaris): the effect
of ontogeny and emotional closeness on low-level
imitation in dogs. Anim Cogn. 2012
- -Massen
JJ, Vermunt DA, Sterck EH. Male Yawning Is
More Contagious than Female Yawning among
Chimpanzees (Pan troglodytes). PLoS One.
2012;7(7):e40697.
- -Nahab FB, Hattori
N, Saad ZS, Hallett M Contagious yawning and
the frontal lobe: An fMRI study Human Brain
Mapping 2009;30:1744-1751
- -Norscia I,
Palagi E. Yawn Contagion and Empathy in Homo
sapiens. PLoS ONE. 2011;6(12): e28472
- -O'Hara SJ, Reeve
AV A test of the yawning contagion and
emotional connectedness hypothesis in dogs,
Canis familiaris. Animal Behaviour
2011;81:335-340
- -Palagi E,
Leone A, Mancini G, Ferrari PF. Contagious
yawning in gelada baboons as a possible
expression of empathy. Proc Natl Acad Sci USA.
2009;106(46):19262-19567
- -Paukner
A, Anderson JR
Video-induced yawning in stumptail
macaques (Macaca
arctoides) Biol Lett 2006;2(1):36-38
- -Perkins
JR Teaching Dogs to Yawn, Sneeze, and
Implications for Preparedness Theory and
Observational Learning.
In: Kusonose, Ryo and Sato, Shusuke 39th
Congress of the International Society for
Applied Ethology, Kanagawa, Japan. 20-24 August,
2005
- -Platek
SM, SR Critton, et al Contagious yawning:
the role of self-awareness and mental state
attribution Cogn Brain Res
2003;17(2):223-227
- -Platek S et
al. Neural correlates of self-face
recognition 2008 Brain Res;1232:173-184
- -Platek S,
Mohamed F, Gallup G Contagious yawning and
the brain Cognitive Brain Research,
2005;23:448-452
- -Schurmann
M, Hari R et al Yearning to yawn: the neural
basis of contagious yawning NeuroImage
2005;24(4):1260-1264
- -Senju A, Maeda
M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H
Absence of contagious yawning in children with
autism spectrum disorder. Biology Letters
2007;3:706-708
- -Senju A,
Kikuchi Y, Akechi H et al. Does eye contact
induce contagious yawning in children with
autism spectrum disorder? J of Autism and
Developmental Disorders.
2009;39(11):1598-1602
- -Silva K, Bessa J, de
Sousa L. Auditory contagious yawning in
domestic dogs (Canis familiaris): first evidence
for social modulation. Anim Cogn. 2012.
- -Yoon JMD, Tennie C
Contagious yawning: a reflection of empathy,
mimicry, or contagion. Anim Behav
2010;79:e1-e3
- -Walusinski
O Echokinetic yawning, theory of mind, and
empathy
|
