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No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria

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Three hypotheses have attempted to explain the phenomenon of contagious yawning. It has been hypothesized that it is a fixed action pattern for which the releasing stimulus is the observation of another yawn, that it is the result of non-conscious mimicry emerging through close links between perception and action or that it is the result of empathy, involving the ability to engage in mental state attribution. This set of experiments sought to distinguish between these hypotheses by examining contagious yawning in a species that is unlikely to show nonconscious mimicry and empathy but does respond to social stimuli: the red-footed tortoise Geochelone carbonaria. A demonstrator tortoise was conditioned to yawn when presented with a red square-shaped stimulus. Observer tortoises were exposed to three conditions: observation of conditioned yawn, non demonstration control, and stimulus only control. We measured the number of yawns for each observer animal in each condition. There was no difference between conditions. Experiment 2 therefore increased the number of conditioned yawns presented. Again, there was no significant difference between conditions. It seemed plausible that the tortoises did not view the conditioned yawn as a real yawn and therefore a final experiment was run using video recorded stimuli. The observer tortoises were presented with three conditions: real yawn, conditioned yawns and empty background. Again there was no significant difference between conditions. We therefore conclude that the red-footed tortoise does not yawn in response to observing a conspecific yawn. This suggests that contagious yawning is not the result of a fixed action pattern but may involve more complex social processes.
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WILKINSON A. et al.: No contagious yawning in tortoises
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UNCORRECTED PROOF
No evidence of contagious yawning in the red-footed tortoise
Geochelone carbonaria
Anna WILKINSON1, 2, Natalie SEBANZ3, Isabella MANDl1, Ludwig HUBER1
1 Department of Cognitive Biology, University of Vienna, Althanstrasse 14, Vienna, 1090, Austria
2 Department of Biological Sciences, University of Lincoln, Lincoln, LN2 2LG, UK
3 Donders Institute for Brain, Cognition and Behavior, Centre for Cognition, Radboud, University Nijmegen, P.O. Box 9104, 6500 HE
Nijmegen, The Netherlands
Abstract Three hypotheses have attempted to explain the phenomenon of contagious yawning. It has been hypothesized that it is a fixed
action pattern for which the releasing stimulus is the observation of another yawn, that it is the result of non-conscious mimicry emerging
through close links between perception and action or that it is the result of empathy, involving the ability to engage in mental state attribution.
This set of experiments sought to distinguish between these hypotheses by examining contagious yawning in a species that is unlikely to
show nonconscious mimicry and empathy but does respond to social stimuli: the red-footed tortoise Geochelone carbonaria. A demonstrator
tortoise was conditioned to yawn when presented with a red square-shaped stimulus. Observer tortoises were exposed to three conditions:
observation of conditioned yawn, non demonstration control, and stimulus only control. We measured the number of yawns for each
observer animal in each condition. There was no difference between conditions. Experiment 2 therefore increased the number of conditioned
yawns presented. Again, there was no significant difference between conditions. It seemed plausible that the tortoises did not view the
conditioned yawn as a real yawn and therefore a final experiment was run using video recorded stimuli. The observer tortoises were
presented with three conditions: real yawn, conditioned yawns and empty background. Again there was no significant difference between
conditions. We therefore conclude that the red-footed tortoise does not yawn in response to observing a conspecific yawn. This suggests that
contagious yawning is not the result of a fixed action pattern but may involve more complex social processes [Current Zoology 57 (4): –,
2011].
Keywords Reptile, Contagious yawn, Empathy, Nonconscious mimicry, Fixed action pattern
Contagious yawning is well documented in humans, however, little is known about its function and prevalence in
the animal kingdom or the brain mechanisms underlying it. The function of yawning itself is also poorly understood.
Yawning has been observed in a number of vertebrate taxa and, though it is likely that such a prominent and widespread
behaviour serves a biological function, the nature of this function remains unclear (Guggisberg et al., 2007). It has been
suggested that yawning may cause an increase in arousal which will reduce the probability of sleep. This is something
which is likely to be important for vigilance in all animal species (Walusinski and Deputte, 2004, cited by Guggisberg
et al., 2007). Another hypothesis suggests that yawning is a form of communication used to synchronize group behavior
(Daquin et al., 2001) this could be for a variety of reasons, those postulated have included communicating drowsiness,

Received Dec. 21, 2010; accepted Mar. 08, 2011
Corresponding Author. E-mail:awilkinson@lincoln.ac.uk
© 2011 Current Zoology
WILKINSON A. et al.: No contagious yawning in tortoises
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social stress or even boredom (Guggisberg et al., 2007). This would potentially serve an important social function and it
is possible that contagious yawning may have evolved as a result of this.
Experimental analysis of contagious yawning in humans has revealed that it occurs in 40%60% of participants
when they see (videos of) a yawning person (Platek et al., 2005). However, the mechanisms underlying contagious
yawning remain poorly understood (Nahab et al., 2009). A number of hypotheses have been proposed to account for the
occurrence of contagious yawning and current evidence to support or refute them is equivocal at best. It has been
suggested that contagious yawning may simply be the result of a fixed action pattern for which the releaser stimulus is
the observation of another yawn (Provine, 1986; Yoon and Tennie, 2010). Evidence to support this hypothesis comes
from the fact that yawns follow a highly stereotyped pattern (Provine, 1986). Further, yawning in humans can be
triggered by observing a yawn, hearing a yawn (Arnott et al., 2009) or even thinking about yawning (Provine, 1986).
This hypothesis predicts that contagious yawning may be observed in all vertebrates that exhibit yawning behavior.
A second hypothesis suggests that nonconscious social mimicry, the tendency to adopt postures, gestures and
mannerisms of an interaction partner (also known as the chameleon effect; Chartrand and Bargh, 1999) may control
contagious yawning behavior (Yoon and Tennie, 2010). Non-conscious mimicry is assumed to reflect close links
between perception and action. Many studies in macaque monkeys and humans have shown that when an individual
observes another perform a particular action, corresponding action representations in the observer’s action repertoire are
activated (Rizzolatti and Sinigaglia, 2010). Nonconscious mimicry may occur when inhibitory processes that normally
keep us from executing observed actions (Brass et al., 2005) are overridden. It has been shown to be modulated by
specific social motivations e.g. the desire to affiliate with the social partner. This is well documented in humans and
there is some evidence of this phenomenon in primates (Rizzolatti and Sinigaglia, 2010) but no research has directly
examined this in terms of contagious yawning. This hypothesis would predict the presence of contagious yawning in
species in which perception and action rely on common neural representations and social relations are of import.
The majority of recent research has attempted to explain the phenomenon of contagious yawning in terms of mental
state attribution and, in particular, empathy (e.g. Platek et al., 2005). There are many different definitions of empathy
(Vignemont and Singer, 2006), but in this context empathy is considered to be the understanding of another’s feelings
based on the capacity to infer others’ mental states (Baron-Cohen et al., 2005). According to this view contagious
yawning should only be observed in those species that possess mental state attribution, and thus we would expect to see
little evidence of contagious yawning outside the higher primates.
Contagious yawning has been observed in non-human primates (chimpanzees Pan troglodytes, Anderson et al.,
2004; stump-tailed macaques Macaca arctoides, Paukner and Anderson, 2006; gelada baboons Theropithecus gelada,
Palagi et al., 2009) and dogs (Canis familiaris, Joly-Mascheroni et al., 2008, but see Harr et al., 2009). These studies
interpret their data in terms of empathy. However the data presented in these papers do not allow the other hypotheses
to be dismissed (see Yoon and Tennie, 2010 for further details) as the studies have focused on those species that may
possess the ability to engage in some aspects of mental state attribution or fit the criteria for nononscious mimicry.
This study aimed to discriminate between the possible mechanisms controlling contagious yawning by asking
whether contagious yawning is present in a species that is unlikely to show empathy or nonconscious mimicry: the red-
footed tortoise Geochelone carbonaria. To our knowledge there is no evidence of social mimicry, mental state
attribution or empathy in this species. Though naturally solitary there is evidence that this species possesses a sensitivity
to visual social cues (Auffenberg, 1965), that it can follow the gaze direction of a conspecific (Wilkinson et al., 2010a)
and can learn to access an otherwise inaccessible goal by observing the behavior of a conspecific (Wilkinson et al.,
WILKINSON A. et al.: No contagious yawning in tortoises
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2010b). Further, research suggests that this species is highly visual and when available will use visual cues over both
olfactory cues (Wilkinson et al., 2007) and over a highly successful response based behavior (Wilkinson et al., 2009).
Taken together this makes them ideal subjects for examining this question. If contagious yawning is simply the result of
a fixed action pattern for which the releaser stimulus is the observation of another yawn, then we would expect to
observe it in this species; however, if it is controlled through social processes such as nonconscious mimicry or empathy
then we would expect it to be absent.
1 Materials and Methods
1.1 Experiment 1
1.1.1 Subjects Seven captive-bred, red-footed tortoises Geochelone carbonaria participated in this study. The tortoises
were housed in two groups in a heated (29±4 ) and humidified room. They were group housed for at least 6 months
prior to the onset of the experiment. Though this species is naturally solitary they adapt well to group living and are
frequently kept in groups in captivity. The exact age of the tortoises was unknown; however all were juvenile or
subadult with plastron (the lower part of the shell) lengths measuring 10.5 cm 17 cm at the start of the experiment (see
Table 1 for individual sizes). The sex of some of our subjects was unknown as this species does not develop
unambiguous sexually dimorphic traits until around the age of 5. However, Alexandra, the demonstrator, was female;
two of the observers (Wilhelmina and Moses) were also female and another observer, Aldous, was male (see Table 1 for
further details). None of the tortoises were experimentally naïve (e.g. Wilkinson et al., 2007; Wilkinson et al., 2009;
Wilkinson et al., 2010a; Wilkinson et al., 2010b), but they had never previously been involved in a contagious yawning
task or any similar experiment. Two of the tortoises (Wilhelmina and Aldous) lived in a group with the demonstrator.
1.1.2 Apparatus The study was run in a tank measuring 80cm × 40cm × 40cm in a heated room, maintained at
approximately 29oC. The testing tank was separated by a screen; the lower part was made of metal fencing (40 cm ×
17.5 cm) that the tortoises could see through. The upper part consisted of an opaque screen (40 cm × 22.5 cm; see Fig.
1).
1.1.3 Pretraining Prior to the onset of the study the demonstrator was trained to yawn when presented with a 2 cm × 2
cm red square shaped stimulus. The technique used for training was that of successive approximation. Initially
whenever the demonstrator opened her mouth slightly in the presence of the red stimulus she was rewarded with a
favored food. Once she started to readily open her mouth when presented with the stimulus she was then only rewarded
when she opened it wide. Once she readily performed the gape like response she was rewarded for tilting her head back
whilst her mouth was open. The resulting behavior appeared highly similar to a naturally occurring tortoise yawn. This
training took 6 months.
1.1.4 Procedure The goal of this study was to test whether tortoises show contagious yawning. To do so, we used a
demonstrator tortoise that was conditioned to yawn when presented with a red square-shaped stimulus. Observer
tortoises were exposed to three conditions: A yawning condition in which they observed a single conditioned yawn; a
control condition in which a conspecific was present but did not yawn; and a second control condition in which the red
square-shaped stimulus was presented without the presence of the demonstrator. We measured the number of yawns for
each observer animal in each condition.
WILKINSON A. et al.: No contagious yawning in tortoises
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The experiment was run between 19th August and 1st September 2009; trials took place in early afternoon. All
tortoises were habituated to the apparatus before testing began. The observer tortoises received one trial a day and three
trials for each condition. This resulted in each observer animal receiving nine trials. In general these studies present
only one trial per condition, however, we wanted to examine behavior over time. Further, the number of trials was
identical to that used in a recent (successful) study which investigated gaze following behavior in this species
(Wilkinson et al., 2010a). The order of presentation was counterbalanced across subjects. At the onset of each trial the
demonstrator was placed in the left hand side of the tank, after this one observer tortoise was placed in the right-hand
side and allowed to observe the demonstrator. Each trial lasted 5 minutes and 30 seconds. After the trial was completed
the tortoise was removed. Observer tortoises only received one trial per day to ensure that the demonstrator’s
conditioned yawn did not extinguish. Throughout the entire experiment an experimenter (IM) observed and documented
the observer tortoises’ behavior. Any yawn that occurred within the trial time was recorded.
Experimental condition: The conditioned stimulus was presented to the demonstrator tortoise. This resulted in the
demonstrator performing a single conditioned yawn in each experimental trial. The tortoise yawn is characterized by the
extension of the neck, the head being tilted back and the mouth opening in a large gape. The yawn is extremely clear
and cannot be mistaken for another behavior. The tortoise does not open its mouth in this way in any other circumstance.
When eating the mouth is less open and head position and body posture are quite different from that observed in a yawn.
A trial only counted if the demonstrator performed the yawn whilst the observer was watching (judged as facing
towards the demonstrator). If the observer was not watching then the trial was stopped, the observer removed and the
trial re-run later. An observer yawn was counted if the observer tortoise yawned within 5 minutes and 30 seconds of
observing the demonstrator yawn. This was based on the trial times used in previous contagious yawning experiments
with animals.
No yawn control: To rule out the possibility that the presence of another animal caused the subject to yawn, we included
a control condition in which the demonstrator was present, but the stimulus was not presented. This was identical to the
experimental condition except that the stimulus was not presented and thus the demonstrator did not perform a
conditioned yawn. On the rare occasion that the demonstrator happened to yawn, the trial was aborted and excluded
from analysis. This only occurred once. The trial started after the observer tortoise was placed in the apparatus and had
turned to face the demonstrator tortoise. Each trial lasted 5 minutes and 30 second and we recorded all yawns.
No demonstrator control: We included a control condition in which this stimulus was presented, but the demonstrator
was absent, to rule out the possibility that the subject responded to the red-square shaped stimulus. This was identical to
the experimental condition except that the demonstrator compartment was empty. For this control we analyzed whether
the subject yawned in the 5 minutes and 30 seconds following the presentation of the stimulus.
1.1.5 Data analysis The percentage of trials in which a tortoise yawned was calculated for each individual for each
condition on the basis of the total number of yawns divided by the total of possible yawns multiplied by 100. The
figures display an average of this across individuals. Given the small sample size non-parametric statistics were used
for analysis. A Friedman’s was used to analyze the number of yawns across conditions.
1.2 Experiment 2
Experiment 2 examined the hypothesis that contagious yawning would occur if the subject were presented with
multiple yawns. Thus the tortoises were presented with yawns for the first minute of the trial (2–3 yawns) in the
experimental condition. Further, observation of the tortoises’ behavior in the different conditions of Experiment 1
WILKINSON A. et al.: No contagious yawning in tortoises
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revealed that they yawned slightly earlier in the experimental condition than in the control conditions. It is possible that,
in the control condition, when no other tortoise was present the observer tortoises settled down to rest. Therefore the
trial time was reduced to 3 minutes for Experiment 2.
1.2.1 Subjects, Apparatus, and Procedure
The tortoises in Experiment 1 participated in Experiment 2. The Apparatus was the same as that used in Experiment
1. The experiment was run between 10th December 2009 and 18th December 2009; trials took place in the early
afternoon. The procedure was identical to that used in Experiment 1 except that in the experimental condition the
demonstrator tortoises performed conditioned yawns for the first minute of the trial. This resulted in 2–3 conditioned
yawns per trial (resulting in 6–9 in total per animal). To reduce the possibility that the tortoises yawned as the result of
resting in the tank the total trial time was reduced to 3 minutes (including the demonstration phase) for each condition.
1.3 Experiment 3
1.3.1 Subjects, Apparatus, and Procedure
We examined the possibility that the lack of differential responding observed in the first two experiments was
because the conditioned yawn did not appear as a yawn to the tortoises. It is possible that some element of a real yawn
was not reflected in the conditioned behavior of the demonstrator. We therefore presented the observer tortoises with
video stimuli which displayed a real yawn, a fake yawn or an empty background. A Sony Vaio laptop (VGN-CR31S)
was placed in the demonstrator side of the tank. The screen was 14.1-in and the resolution set at 1280 × 800 pixels. The
video stimuli were presented silently via this laptop. Three clips of Alexandra performing real yawns and conditioned
yawns were recorded. In addition three clips containing only empty background were also recorded. The clips were
edited and sequenced to produce three different videos. Each video contained six 10 second clips (each clip was
presented twice within a video) of real yawns, conditioned yawns or background. Each clip was preceded by a 5 second
white screen and matched for total length. This resulted in a stimulus presentation time of 1 minute 30 seconds. A
further 30 seconds of white screen was presented after the stimulus presentation had finished. This resulted in each
video being 2 minutes in length. The video length made up the total trial time for each observer tortoise for each
condition, the trial time was therefore 2 minutes for each condition.
The tortoises in Experiment 1 and 2 participated in Experiment 3. The testing tank was the same as that used in
Experiment 1 and 2. Each animal received three trials per condition. The experiment was run between 15th February
2010 and 17th March 2010; trials took place in the early afternoon. The procedure was identical to that used in
Experiment 2 except that the stimuli were presented via laptop. The laptop was placed on the left-hand side of the
experimental tank (where the demonstrator had been in previous experiments). It was turned on and displayed a white
screen before the start of each trial. The observer tortoise was then placed on the right-hand side of the experimental
tank. When the tortoise was looking at the screen the experimenter started the video sequence. In all other respects the
procedure was identical that used in Experiment 2.
2 Results
2.1 Experimental 1
WILKINSON A. et al.: No contagious yawning in tortoises
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Fig. 2 presents the percentage of yawns observed in each condition. A Friedman’s test revealed that there was no
difference in the tortoises behavior across conditions (χ2 = 3.82, df = 2, P = 0.15). Table 1 shows the number of
responses in each condition for each animal. Overall response rate was poor with three of the six tortoises not
responding in any of the conditions. However, of the three that did respond two responded more in the conditioned
yawn condition than in the control conditions.
2.2 Experiment 2
Fig. 3 presents the percentage of yawns observed in each condition. A Friedman’s test revealed no difference in the
tortoises behavior across condition (χ2 = 3.00, df = 2, P = 0.22). Examination of the individual data revealed that only
two tortoises (Wilhelmina and Aldous) yawned in this experiment. Wilhelmina yawned in all conditions (conditioned
yawn = 2, no demonstration = 1, stimulus only = 2) whereas Aldous only yawned once (in the stimulus only condition).
2.3 Experiment 3
Fig. 4 presents the percentage of yawns observed in each condition. A Friedman’s test revealed that there was no
difference in the tortoises behavior between conditions (χ2= 0.55, df = 2, P = 0.78). Examination of the individual data
(Table 2) revealed that four of the six tortoises responded in this experiment, however, not a single animal responded
more in the real yawn condition than in the two control conditions.
3 Discussion
The results of the three experiments presented in this paper suggest that the red-footed tortoise does not yawn in
response to observing a conspecific yawn. Experiment 1 examined whether tortoises would yawn more when observing
a conspecific perform a conditioned yawn than in other control conditions. They did not. The results revealed that there
was no overall difference in responding across conditions suggesting that tortoises do not possess the ability to yawn
contagiously. This suggests that contagious yawning may not be the result of a fixed action pattern for which the
releaser stimulus is a yawn (Provine, 1986; Yoon and Tennie, 2010) but rather supports the idea that higher level
mechanisms such as nonconscious mimicry (Yoon and Tennie 2010) or empathy (Anderson et al., 2004; Paukner and
Anderson, 2006; Palagi et al., 2009; Joly-Mascheroni et al., 2008) may control this behavior. However, examination of
the individual data revealed an overall low level of responding. Interestingly, of the three animals that did respond two
responded more in the yawn condition than in the control conditions. This suggests that the tortoises may have the
ability to yawn when they observe a conspecific yawning but it is possible that a single conditioned yawn per trial was
not enough to evoke convincing evidence of contagious yawning in this species. The majority of research in this area
has used multiple yawns (up to 19, Jolie-Mascheroni et al., 2008) as stimuli. It is therefore plausible that, under
experimental conditions, multiple yawns are necessary for contagious yawning to occur.
Experiment 2 thus examined whether contagious yawning would be observed if the demonstrator performed multiple
conditioned yawns. The results revealed that this was not the case. The tortoises were equally as likely to respond in the
control conditions as they were in the experimental conditions. The combined results of Experiment 1 and 2 suggest that
the tortoises do not yawn after observing a conspecific yawn. Again, the data contradict the hypothesis that contagious
yawning is the result of a fixed action pattern (Provine, 1986; Yoon and Tennie, 2010) and suggests that higher
processes such as empathy may be involved (Anderson et al., 2004; Anderson and Matsuzawa, 2006; Paukner and
Anderson, 2006; Palagi et al., 2009; Joly-Mascheroni et al., 2008) or nonconscious mimicry (Yoon and Tennie 2010).
WILKINSON A. et al.: No contagious yawning in tortoises
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Experiment 3 examined the possibility that the lack of differential responding observed in the first two experiments
was because the conditioned yawn did not appear as a yawn to the tortoises. The results revealed that the animals
appeared to respond more in both the yawn and the conditioned yawn conditions than when they were presented with
the background control. However, this apparent difference was not close to reaching statistical significance. Thus, the
findings of Experiment 3 support those of Experiments 1 and 2 which together reveal that the red-footed tortoise does
not yawn in response to observing a conspecific yawn. It is possible that the tortoises did not perceive the video stimuli
as a real tortoise and that the experimental stimulus (the conditioned yawn) with which the tortoises were presented may
have lacked some elements which, though not apparent to humans, were essential for contagious yawning to take place.
For example, the demonstrator was trained to express a simulated yawn by opening its mouth wide and turning its head
up. However, a yawn also involves the movement of air and this is something which was not simulated in either our
conditioned yawn experiments or in the video playback. It is possible that a real yawn is necessary to stimulate the
observer tortoise. Yet, video stimuli have successfully stimulated yawns in a variety of species (Anderson et al., 2004;
Paukner and Anderson, 2006) and video stimuli have produced appropriate responses to social stimuli in the red-footed
tortoise (Wilkinson et al., unpublished data). However, the use of video stimuli to elicit behavior in animals is
controversial because it is not clear what the animals perceive on the screen. This may account for the differences seen
between Joly-Macheroni et al.’s (2008) study in which dogs observed a real-life human demonstrator yawning and that
of Harr et al. (2009) in which the yawns were presented as video stimuli. Little work has directly investigated picture-
object recognition in reptiles. However, there is evidence that reptiles, including the red-footed tortoise, respond to
video stimuli of conspecifics as if they were the real animals (e.g. Ord and Evans, 2002; Ord et al., 2002; Van Dyk and
Evans, 2008; Wilkinson et al., unpublished data).
Overall, our findings are more consistent with the suggestion that tortoises do not yawn in a contagious manner and
that thus suggest that contagious yawning is not simply the result of a fixed action pattern and releaser stimulus, as if
this mechanism controlled the behavior it would be predicted that contagious yawning would be present in all
vertebrates that yawn. We suggest that contagious yawning may be controlled through social processes such as
nonconscious mimicry or empathy, neither of which would have predicted the presence of contagious yawning in the
red-footed tortoise. This finding indirectly suggests that, rather than increasing arousal, yawning may be a form of
communication that evolved to synchronize group behavior (Daquin et al., 2001). However, the type of information that
it might communicate or behavior that it might promote remains unclear. Numerous researchers have suggested that
contagious yawning may be an indicator of empathy; however, results in experiments with humans have been equivocal
(Platek et al., 2003; Schurmann et al., 2005). The findings of this study suggest that contagious yawning may be
controlled by higher level social processes as it is believed that tortoises do not possess nonconscious mimicry or
empathy. However, the current data do not allow us to determine whether contagious yawning is a result of
nonconscious mimicry or empathy. The nonconscious mimicry hypothesis predicts the presence of contagious yawning
in species in which perception and action rely on common neural representations we therefore might expect to observe
it in animals living in complex social groups. The empathy hypothesis predicts that we would expect to see little
evidence of contagious yawning outside the higher primates and (possibly) domesticated dogs, species believed to be
capable of empathy (Joly-Mascheroni et al., 2008). Further research is needed to determine which of these social
processes may be involved in controlling yawning.
WILKINSON A. et al.: No contagious yawning in tortoises
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Acknowledgements The authors would like to thank the cold-blooded cognition group at the University of Vienna for their helpful
comments. We are also indebted to Wolfgang Berger for making the setup and Michael Pollirer for providing the experimental tank.
This work was supported by funding from the Austrian Science Fund (to L.H.) contract number P19574.
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WILKINSON A. et al.: No contagious yawning in tortoises
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Table 1 The size, sex and the number of trials in which each tortoise yawned in each condition of Experiment 1
Tortoise Size (cm) Sex Experimental
Condition No Yawn Control No Demonstrator
Control
Moses 14 Female 0 0 0
Aldous 17 Male 1 0 2
Wilhelmina 16.2 Female 3 1 2
Quinn 10.5 Unknown 1 0 0
Esme 11 Unknown 0 0 0
Molly 11 Unknown 0 0 0
Table 2 The number of trials in which each tortoise yawned in each condition of Experiment 3
Tortoise Real Yawn Conditioned Yawn Background
Moses 0 1 1
Aldous 2 2 0
Wilhelmina 0 0 0
Quinn 0 0 0
Esme 0 0 1
Molly 2 2 0
WILKINSON A. et al.: No contagious yawning in tortoises
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Fig. 1 A diagram of the experimental setup in Experiment 1 and 2
WILKINSON A. et al.: No contagious yawning in tortoises
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Fig. 2 Experiment 1. The total percentage of yawns of all subjects in (bar a) the experimental condition in which the tortoises
observed the demonstrator perform a single conditioned yawn (bar b) the no yawn control condition in which the
demonstrator was present but did not perform the conditioned yawn and (bar c) the no demonstrator control condition in
which the stimulus was presented but the demonstrator was not there. The whiskers on all bars represent standard error.
WILKINSON A. et al.: No contagious yawning in tortoises
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Fig. 3 Experiment 2. The total percentage of yawns of all subjects in (bar a) the experimental condition in which the tortoises
observed the demonstrator perform six to nine conditioned yawns per animal conditioned yawns (bar b) the no yawn control
condition in which the demonstrator was present but did not perform the conditioned yawn and (bar c) the no demonstrator
control condition in which the stimulus was presented but the demonstrator was not there. The whiskers on all bars represent
standard error.
WILKINSON A. et al.: No contagious yawning in tortoises
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Fig. 4 Experiment 3. The total percentage of yawns of all subjects in (bar a) The experimental condition in which the
tortoises observed a video containing six real yawns (bar b) the conditioned yawn control condition in which the tortoises
watched video containing six conditioned yawns and (bar c) the background control condition in which the video background
from each of the clips was played. The whiskers on all bars represent standard error.
... A report of no evidence of contagious yawning in red-footed tortoises (Wilkinson et al. 2011) led to the award of an Ig Nobel prize. Two types of yawn stimuli were presented to observer tortoises: from live demonstrators that had been trained to yawn, and from video clips of demonstrators yawning spontaneously; both types gave negative results. ...
... Two types of yawn stimuli were presented to observer tortoises: from live demonstrators that had been trained to yawn, and from video clips of demonstrators yawning spontaneously; both types gave negative results. As well as showing that tortoises appear to lack mechanisms that underly contagious yawning in other species, Wilkinson et al. (2011) succeeded in using successive approximation and positive reinforcement to shape yawns or yawn-like responses in a reptile. ...
... In particular, the reflexive tendency to yawn following the detection of yawns in others, i.e., contagious yawning, is a well-documented phenomenon that may serve to enhance vigilance and synchronization in groups [19]. Distinct from physiologically triggered yawns, which are ubiquitous in vertebrates, there is a great deal of variation across species when it comes to the tendency to yawn contagiously [20][21][22][23]. ...
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Contagious yawning, or the reflexive tendency to yawn following the detection of yawning in others, is well-documented among humans and a growing number of social vertebrates. While the most common form of yawn contagion occurs between conspecifics, some non-human animals in captivity have been reported to yawn in response to yawns from human handlers/caregivers. The current research sought to provide the first formal investigation of whether people yawn contagiously in response to yawns from non-human animals. In addition, this study aimed to test whether this response was modulated by phylogenetic relatedness and domestication/social closeness. A total of 296 participants from Amazon Mechanical Turk self-reported on their yawning behavior following exposure to a (1) control (non-yawning) condition or a compilation of yawning stimuli either from (2) fish, (3) amphibians, (4) reptiles, (5) birds, (6) non-primate mammals, (7) apes, or (8) domesticated cats and dogs. The results provide strong support for interspecific yawn contagion. However, neither the propensity to yawn (binary) nor total yawn frequency varied significantly across interspecific conditions. Overall, these findings suggest that the mechanisms governing yawn contagion can be activated by varied forms of yawning stimuli, including those from distantly related and unfamiliar species.
... No formal investigations have been performed on amphibians or fish, although Baenninger (1987) assessed the temporal expression of yawn-like behaviours in Siamese fighting fish, Betta splendens, and found no evidence for contagion. In the only study on reptiles, the responses of red-footed tortoises, Geochelone carbonaria, were observed following the observation of conditioned yawn-like behaviour in a conspecific (Wilkinson et al., 2011). No increase in tortoise yawning occurred when compared to control conditions. ...
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Yawning is a stereotyped action pattern that is prevalent across vertebrates. While there is growing consensus on the physiological functions of spontaneous yawning in neurovascular circulation and brain cooling, far less is known about how the act of yawning alters the cognition and behaviour of observers. By bridging and synthesizing a wide range of literature, this review attempts to provide a unifying framework for understanding the evolution and elaboration of derived features of yawning in social vertebrates. Recent studies in animal behaviour, psychology and neuroscience now provide evidence that yawns serve as a cue that improves the vigilance of observers, and that contagious yawning functions to synchronize and/or coordinate group activity patterns. These social responses to yawning align with research on the physiological significance of this behaviour, as well as the ubiquitous temporal and contextual variation in yawn frequency across mammals and birds. In addition, these changes in mental processing and behaviour resulting from the detection of yawning in others are consistent with variability in the expression of yawn contagion based on affinity and social status in primates. Topics for further research in these areas are discussed.
... Research on animal personality has focused on mammalian species, particularly in the families of Primates [4,7,8], Suidae [9], Canidae [10,11] and Felidae [12,13], though also in fish [14]. Personality research has value in helping animal keepers to better understand the compatibility of animals in breeding programs, in applied research on the evolutionary development of personality [15,16], and in predicting conservation translocation success [17][18][19][20]. ...
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Human–animal interaction (HAI) can be valuable for captive animals, and many zoo-housed species benefit from interactions with their keepers. There is also an increasing body of evidence that some animal species possess personalities that are temporally consistent. However, the majority of zoo research, particularly on personality and HAI, traditionally has focused on mammals, and there are comparatively fewer studies on reptiles. Research was undertaken at the Faunistic Park Le Cornelle, Italy, to investigate the effects of approach tests and food interaction events on 5 male and 5 female Aldabra tortoise (Aldrabrachelys gigantea) behavior. During human–tortoise interactions, continuous focal sampling of behavior took place. The behavioral differences between individual tortoises, interaction type (approach or training) and person involved in the interaction (keeper, vet, or observer) were analysed using general linear mixed-effects models. The personality components of the tortoises were also quantified using principal component analysis. Overall, the study revealed that individuals acted significantly differently to one another, and that while females initially appeared to display a greater number of shy behaviors, this was not consistent across the group. PCA revealed two personality dimensions in the tortoises: boldness and avoidance. Overall, the study revealed that the tortoises possessed personalities that were independent of sex or scenario. The study also revealed that many tortoises chose to interact with their keepers during training and approach tests: this suggests that human–tortoise interactions may have some enrichment value. Future research could quantify tortoise personality in other scenarios such as in social interactions with other tortoises.
... Perhaps unsurprisingly, Wilkinson et al. (2011) found no evidence of contagious yawning in the red-footed tortoise, although it was not for lack of trying. Over 6 months, a demonstrator tortoise was trained to yawn when presented with a red stimulus. ...
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This is the fourth in a series of papers celebrating some of the weird and wonderful research findings hidden amongst the scientific literature. It aims to ensure that we remember the funnier side of science and provides answers to questions we may have been too afraid to ask. Here, we examine selected research focussing on animal mapping, behaviour, ecology and conservation. Ecology is the study of the relationships living organisms have with respect to each other and their natural environment.
... Thus far, contagious yawning is observed in several primate species, including chimpanzees (Pan troglodytes; Anderson, Myowa-Yamakoshi, & Matsuzawa, 2004;Campbell & de Waal, 2011;Campbell, Carter, Proctor, Eisenberg, & de Waal, 2009;Massen et al., 2012), bonobos (P. paniscus; Demuru & Palagi, 2012;Palagi et al., 2014) (Harr, Gilbert, & Phillips, 2009), and red-footed tortoises (Geochelone carbonaria; Wilkinson, Sebanz, Mandl, & Huber, 2011). This illustrates the ongoing debate on the possible mechanism underlying contagious yawning. ...
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Primates show various forms of behavioral contagion that are stronger between kin and friends. As a result, behavioral contagion is thought to promote group coordination, social cohesion, and possibly state matching. Aside from contagious yawning, little is known about the contagious effect of other behaviors. Scratching is commonly observed during arousal and as such may play a role within group dynamics. While the Bornean orangutan (Pongo pygmaeus) is commonly considered the least social great ape, orangutans do engage in social interactions. Therefore, their social organization makes them a suitable case for studying the social function of behavioral contagion. Through behavioral observations of captive orangutans, we recorded all yawn and scratch events together with the corresponding behavior of all bystander group‐members. As yawning was rarely observed, no conclusions could be drawn regarding this behavior. Scratching was contagious and occurred within 90 s after the triggering scratch. Specifically, orangutans showed increased scratch contagion when they had seen a weakly bonded individual scratch during tense contexts. When the orangutan had not seen the triggering scratch, the contagiousness of scratching was not affected by context or relationship quality. Our results indicate that behavioral contagion is not simply higher between individuals with stronger social relationships, but that the contagiousness of behaviors may vary based on the context and on social factors. We discuss these findings in light of an adaptive function that may reduce aggression. Research Highlights • Bornean orangutans show scratch contagion. • Seen scratches are more contagious during tense context between nonkin/friends.
... Additionally, an important next step is to consider evidence of contagious yawning outside of mammals. While there has been some work looking at contagious yawning in budgerigars [86,90] and tortoises [91], research has otherwise been sparse outside of the mammalian class. ...
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Contagious yawning has been suggested to be a potential signal of empathy in non-human animals. However, few studies have been able to robustly test this claim. Here, we ran a Bayesian multilevel reanalysis of six studies of contagious yawning in dogs. This provided robust support for claims that contagious yawning is present in dogs, but found no evidence that dogs display either a familiarity or gender bias in contagious yawning, two predictions made by the contagious yawning-empathy hypothesis. Furthermore, in an experiment testing the prosociality bias, a novel prediction of the contagious yawning-empathy hypothesis, dogs did not yawn more in response to a pro-social demonstrator than to an antisocial demonstrator. As such, these strands of evidence suggest that contagious yawning, although present in dogs, is not mediated by empathetic mechanisms. This calls into question claims that contagious yawning is a signal of empathy in mammals.
... Some studies on dogs (Canis lupus familiaris) have found evidence of contagious yawning while others have not, which may stem from the different methods used [20][21][22][23][24][25][26] . Lastly, two species of lemur (Lemur catta and Varecia variegata) 27 , lowland gorillas (Gorilla gorilla) 12,28 , orangutans (Pongo abelii) 12 , and red-footed tortoises (Geochelone carbonaria) 29 did not show evidence of contagion in experimental settings, although the sample size issues mentioned for the bonobo studies also pertain to the orangutans and tortoises. ...
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There is robust experimental evidence for contagious yawning, yet observational studies of naturalistic behavior have been fewer. Without data from real-world behavior, researchers have questioned the existence of contagious yawning and made assumptions about some parameters (e.g., the duration of the effect). We observed contagious yawning in chimpanzees to confirm/disconfirm its existence in the behavioral repertoire of this species, and if present, provide some of the missing descriptives. We recorded yawns on an all-occurrence basis from 18 captive-reared chimpanzees at the Los Angeles Zoo. We recorded identity, time, and individuals who could have been affected. We calculated a threshold for contagion by taking the mean and adding 1.96 standard deviations, constructing a response curve. Across multiple measures we see a consistent pattern in which there is a strong effect of contagion for 1.5 minutes, a less strong but still significant effect lasting up to 3.5 minutes in some measures, and no evidence of contagion beyond 3.5 minutes. From the time stamp on each yawn we were able to rule out temporal synchrony as an alternative hypothesis. thus, contagious yawning appears to be a natural phenomenon in chimpanzees lending support to the myriad experimental and observational studies to date.
... Reptiles were long considered to be sluggish and unintelligent; however, when tested under appropriate experimental conditions, they exhibit an impressive array of cognitive abilities (for example, red-footed tortoise, Chelonoidis carbonaria, and bearded dragon, Pogona vitticeps; Kis, Huber, & Wilkinson, 2015;Mueller-Paul et al., 2014;reviewed by Matsubara, Deeming, & Wilkinson, 2017;Wilkinson & Glass, 2018). Work has recently shown that these two species are able to perceive similarities between pictures and the objects that they represent (Wilkinson, Mueller-Paul, & Huber, 2013), respond to video stimuli (Siviter, Deeming, van Giezen, & Wilkinson, 2018;Wilkinson, Sebanz, Mandl, & Huber, 2011), and, crucially for this experiment, discriminate between different quantities of food reward (and remember this association for 18 months; Soldati, Burman, John, Pike, & Wilkinson, 2017). This ability was also found in another reptile species, the Italian wall lizard, Podarcis sicula (Miletto Petrazzini, Fraccaroli, et al., 2017). ...
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