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Emotions are now largely recognised as a core element in animal welfare issues. However, convenient indicators to reliably infer emotions are still needed. As such, the availability of behavioural postures analogous to facial expressions in humans would be extremely valuable for animal studies of emotions. The purpose of this paper is to find out stable expressive postures in sheep and to relate these expressive postures with specific emotional contexts. In an initial experiment, we identified discrete ear postures from a comprehensive approach which integrates all theoretically distinguishable ear postures. Four main ear postures were identified: horizontal ears (P posture); ears risen up (R posture); ears pointed backward (B posture); and asymmetric posture (A posture). In a second experiment, we studied how these ear postures were affected by specific emotional states elicited by exposing sheep to experimental situations in which elementary characteristics (ie suddenness and unfamiliarity, negative contrast and controllability) were manipulated. We found that: i) the horizontal P posture corresponds to a neutral state; ii) sheep point their ears backward (B posture) when they face unfamiliar and unpleasant uncontrollable situations, hence likely to elicit fear; iii) they point their ears up (R posture) when facing similar negative situations but controllable, hence likely to elicit anger; and iv) they expressed the asymmetric A posture in very sudden situations, likely to elicit surprise. By cross-fostering psychological and ethological approaches, we are able to propose an interpretation of ear postures in sheep relative to their emotions.
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47
© 2011 Universities Federation for Animal Welfare
The Old School, Brewhouse Hill, Wheathampstead,
Hertfordshire AL4 8AN, UK
Animal Welfare 2011, 20: 47-56
ISSN 0962-7286
Cognitive sciences to relate ear postures to emotions in sheep
A Boissy*, A Aubert, L Désiré, L Greiveldinger§, E Delvaland I Veissier
INRA UR1213 Herbivores, Site de Theix, F-63122 Saint-Genès-Champanelle, France
Exploitation et Sécurité Routières, CETE Ouest, F-22015 St Brieuc Cedex, France
§UMR UJF CNRS 5525, Acquisition, Fusion d’Information et Réseaux pour la Médecine, Technopole du Biopark, F-74160 Archamps,
France
* Contact for correspondence and requests for reprints: alain.boissy@clermont.inra.fr
Abstract
Emotions are now largely recognised as a core element in animal welfare issues. However, convenient indicators to reliably infer
emotions are still needed. As such, the availability of behavioural postures analogous to facial expressions in humans would be
extremely valuable for animal studies of emotions. The purpose of this paper is to find out stable expressive postures in sheep
and to relate these expressive postures with specific emotional contexts. In an initial experiment, we identified discrete ear
postures from a comprehensive approach which integrates all theoretically distinguishable ear postures. Four main ear postures
were identified: horizontal ears (P posture); ears risen up (R posture); ears pointed backward (B posture); and asymmetric posture
(A posture). In a second experiment, we studied how these ear postures were affected by specific emotional states elicited by
exposing sheep to experimental situations in which elementary characteristics (ie suddenness and unfamiliarity, negative contrast
and controllability) were manipulated. We found that: i) the horizontal P posture corresponds to a neutral state; ii) sheep point
their ears backward (B posture) when they face unfamiliar and unpleasant uncontrollable situations, hence likely to elicit fear; iii)
they point their ears up (R posture) when facing similar negative situations but controllable, hence likely to elicit anger; and iv)
they expressed the asymmetric A posture in very sudden situations, likely to elicit surprise. By cross-fostering psychological and
ethological approaches, we are able to propose an interpretation of ear postures in sheep relative to their emotions.
Keywords:animal welfare, behaviour, cognition, ear postures, emotions, sheep
Introduction
The concern for animal welfare stems from the social and
legal acknowledgement that animals are sentient beings,
capable of feeling emotions. But, despite their central role in
welfare, there is still some reluctance to ascribe emotional
life to animals. However, basic (ie Darwinian) emotions, as
fundamental adaptive processes, have a long evolutionary
history and are shared by many species. Moreover, core
components of emotions — physiological, behavioural and
subjective components — have been clearly identified, and
the first two components can be readily measured objec-
tively in animal studies (Dantzer 1988). Finally, recent
development in the study of emotions in animals has bene-
fitted from merging theories and methods from psychology
and ethology (Dantzer 2002; Désiré et al 2002). Adding to
former biological theories of emotions, it is now acknowl-
edged, since the first studies in the field of cognitive-rela-
tional theories, that emotions are the consequence of an
appraisal and are therefore sustained by cognitive processes
(Scherer et al 2001). According to Scherer (1999), an
emotion results from the appraisal by the subject of a trig-
gering situation through the assessment of a limited number
of elementary characteristics (eg the suddenness, unfamil-
iarity and pleasantness of the situation, the ability for the
subject to predict and to control the situation, etc). Recently,
the behavioural and physiological responses of sheep to
controlled variations of the elementary characteristics of the
eliciting situation (eg suddenness, unfamiliarity, etc) were
described in order to set-up the ‘appraisal’ framework of
emotions to animals (Boissy et al 2007a). We showed that
sheep are responsive to most appraisal characteristics
defined in human studies, such as the suddenness and unfa-
miliarity of an event (Désiré et al 2004, 2006), the unpre-
dictability (Greiveldinger et al 2007) and the potential
control of the event (Greiveldinger et al 2009).
Physiological components commonly used to assess
emotions in animals generally provide a quantitative assess-
ment of the emotional activation (ie the arousal or the
intensity of the emotional response) without clearly defining
the exact nature of the emotion (eg the positive or negative
valence of the emotional experience). For example, plasma
concentrations of glucocorticoid can be increased in
Universities Federation for Animal Welfare Science in the Service of Animal Welfare
48 Boissy et al
response to both acute negative emotional stimuli (Mason
1971) or by the expectation of a positive situation, such as
the availability of a sex mate (Colborn et al 1991). The
mobilisation of energy that precedes these situations can lead
to a considerable overlap of responses to aversive and
pleasant stimuli (Dawkins 1983). Likewise, common behav-
ioural measures that generally consist of fixed action
postures, such as startle, offensive or defensive postures,
freezing, or approach, only provide information about the
intensity of the underlying emotion (for a review see Boissy
1998). Several indicators are generally required to differen-
tiate negative and positive emotional valence (Broom 1997;
Dawkins 2001; Désiré et al 2002), and further behavioural
indicators are nevertheless still needed to allow a convenient
and reliable assessment of emotion in sheep.
In humans, expression of emotions has been extensively
studied through changes in facial features. For example, one
of the most popular analysis systems of facial expression in
humans — the FACS (Facial Action Coding System; Ekman
et al 1972) — is based on the description of muscular
contractions (ie action units) of one’s face, the combination
of these action units forming a posture referring to a specific
emotion. Analogous expressive or postural indicators of
emotions in animals are unfortunately still missing
(Berridge 2000; Boissy et al 2007b) but they would be
highly beneficial both to scientific investigation of emotions
in animals and to welfare issues, by providing convenient
tools to understand and solve human-animal related
concerns, for example. So far, few germinal studies have
shown the availability of such parameters. For instance,
facial expressions relating to gustatory sensory pleasures
have been described in rats as in humans (Berridge 2003).
Moreover, it has been recently shown in farm mammals that
individual recognition is partly based on facial features
(cattle: Coulon et al 2009; sheep: Kendrick et al 2001). Such
findings call for further investigation of stable emotion-
specific facial postures in farm mammals. In order to find
out such facial expressions in farm animals, we focalised on
ears’ postures since they are essential for gathering informa-
tion from the environment (Manteuffel 2006).
By contrast with other mammals, such as primates, sheep
have a limited superficial facial muscles’ network and thus
do not appear to have a wide array of facial expressions.
Nevertheless, they are characterised by a high mobility
both of the neck — offering various global head
postures — and of the ears, due to several muscles for
rotating their ears (Nickel et al 1968). Do specific ear
movements occur in particular emotion-eliciting contexts?
Can measuring ear postures in sheep be used to accurately
infer their emotions? So far, very few studies have
measured the ear postures per se in farm mammals. Scarce
reports from the literature suggest that ear postures may be
useful in assessing emotional valence in farm animals. In
cattle, for example, a high occurrence of pendulous ear
postures was used as an indicator of the animals’ positive
rating of their favourite grooming sites (Schmied et al
2008). To our knowledge, only one study has been recently
carried on ear postures in sheep (Reefmann et al 2009). In
that experiment, ear postures were defined a priori and
sheep were exposed to complex situations likely to induce
states of emotions but it was not possible to characterise the
exact nature of the emotion induced.
The present paper focuses on the identification of ear
postures and their possible link with emotional states in
sheep. In an initial experiment, we identified discrete ear
postures from a comprehensive approach which distinguish
all theoretically measurable ear postures without a priori
interpretations. In a second phase, we ran three experiments
in order to explore the possible correspondence between
previously identified discrete ear postures and emotions.
According to the appraisal framework of emotions previ-
ously used in sheep (Désiré et al 2002; Boissy et al 2007a),
ewes were individually exposed to triggering situations
varying in their degree of either suddenness or unfamil-
iarity, and of negative contrast or controllability.
Materials and methods
An initial experiment was conducted to identify discrete
ear postures. In a second experiment, three groups of
sheep have been utilised separately to specifically assess
the relationship between the identified discrete ear
postures and three elementary components of emotions
corresponding to: (i) suddenness and familiarity of a
visual event (Study 1); (ii) negative contrast (ie, the drastic
reduction of a food reward (Study 2); and (iii) control (ie
control of the access to a food reward) (Study 3).
Animals and rearing
Ewes from the Romane breed, aged between six and ten
months, were used; ten for Experiment 1 and 78 for
Experiment 2 (32, 22, 24 in Studies 1, 2, 3). They had been
separated from their dam 24 to 48 h after birth and housed
with other animals of the same age. At the time of the exper-
iments, the ewes were reared in large pens (called home
pens, 3.8 m2per animal) with deep-litter straw bedding,
adjacent to an experimental chamber (Figure 1). They were
provided hay ad libitum and 400 g of food pellets composed
of barley, sugarbeet, wheat, maize, sunflower and soya
(Thivat Nutrition Animale, Cusset, France). The food was
distributed daily at 1700h in the home pen. When the
training procedure started (see below), the ewes received
food pellets during tests and were supplemented with pellets
in their home pen to reach a total provision of 400 g.
Experimental set-up
The experimental chamber was divided into three compart-
ments: a pre-test (1.5 m2), a test arena (3 m2) and a corridor
(1.8 m2). Each compartment was delineated by 1.8-m high
wooden partitions that prevented animals from seeing each
other (Figure 1). Sliding doors permitted access from one
compartment to the next. A device for delivering food
pellets was placed in the test arena at the opposite side to the
entrance. It consisted of a deck 30 cm above floor level with
a central aperture housing an adjustable 15-cm diameter
trough. Food pellets were delivered in the trough via an
© 2011 Universities Federation for Animal Welfare
Facial expressions of emotions in sheep 49
electronic system placed outside the arena and that could be
controlled by the experimenter.
Four video cameras (three Sony SPT-MC128CE and one
Sony DCR-TRV 320E Digital Handycam, Sony
Corporation, Tokyo, Japan) were used to record the behav-
ioural reactions and postures of the lambs around the trough
in the test arena. The cameras were connected to a video
recorder that simultaneously recorded the images from the
four cameras on the same tape (Sony SVT-1000P, Sony
Corporation, Tokyo, Japan) thanks to a quadravision system
(MV25 Multivision Processor, model MX25, Robot
Research, San Diego, California, USA). The cameras were
placed in such a way as to provide top, side and face-on
views of the ewes.
Procedures
The procedures to train and test the animals have already
been published (Désiré et al 2004, 2006; Greiveldinger et al
2007, 2009, 2010). We will only summarise them briefly in
the present paper.
General training procedure for ewes
To accustom the animals to the experimental chamber, they
were given free access to the chamber from their home pen
for one or two weeks; all access doors were opened and
food pellets were at their disposal in the test arena. Then,
once they accepted to feed in test arena, each ewe was indi-
vidually exposed to the chamber; the access doors were shut
when she moved from one compartment to the next one.
This was repeated on at least five sessions. After this
training phase, each ewe was exposed to test procedures
specific to each study.
Specific procedures for testing ewes
In Experiment 1, a rope-and-pulley device installed behind
the trough of the test arena was utilised to move a white
scarf (0.2 × 0.2 m; length × breadth) from a non-visible
location to 0.2 m above the trough in full sight of the
animal. While the ewe was eating, the scarf was moved by
the experimenter at a speed of 0.88 m s–1. The ewe was left
two minutes more in the arena. The test was repeated once
daily on three consecutive days.
In Experiment 2, Study 1, the rope-and-pulley device was
used, as in Experiment 1, with the exception that a second
object could be used (a flat square made of the same white
textile as the scarf). During training, half the ewes were
familiarised with the scarf and half with the flat square; these
objects always appeared slowly (0.06 cm s–1). The ewes were
trained once daily until they did not step back when object
appeared for three consecutive days. Then, during tests, only
the scarf was presented (it was thus familiar for certain ewes
and not so for others). It was moved down next to the trough
either slowly as previously (0.06 cm s–1) or rapidly
(0.88 m s–1) or. Four test sessions were run.
In Experiment 2, Study 2, the ewes were trained to perform an
operant task (to cross a beam with their muzzle) to get a large
food reward (50 g food pellets) or a small food reward (10 g
food pellets). The photobeam and two photoelectric cells were
placed in a 0.2 × 0.2 × 0.2 m (length × breadth × height) hole
Animal Welfare 2011, 20: 47-56
Figure 1
Experimental set-up (top) and the scarf (bottom) used for the
two experiments (except for Studies 2 and 3).
50 Boissy et al
placed in the partition, 1 m from the left-hand side of the trough.
Each ewe was subjected to one session a day and the session
was terminated when she had eaten four rewards, which took
between 2 and 4 min. After ten days of training the animals were
subjected to three test sessions with the same conditions then for
the next three sessions the ewes trained with a large reward and
received a small one (negative contrast), while the remaining
ewes continued to receive a small reward (no contrast).
In Experiment 2, Study 3, food was always present in the
trough of the test arena but the animals did not have free
access to it. From time-to-time during a session, an air
blower was turned on above the trough and a grid was
moved above the trough to prevent animals from eating.
Half the ewes were trained to perform the same operant task
as in Study 2 (crossing the photobeam) in order to resume
access to the food (air blower is turned off and the grid is
removed). The remaining ewes were yoked to the previous
ones: they received exactly the same access to the food but
without controlling it. Ewes that could control access to the
food and their yoked counterparts were further observed
during four test sessions, once the former had acquired the
operant task.
Identification and detection of ear postures
Video recordings were taken during the following sessions.
Experiment 1 — we selected a total of ten recordings that
allow full vision of the animals; these were taken during the
first, second, or third session where the scarf was presented
to animals and recordings from 30 s before to 30 s after the
appearance of the scarf were analysed.
Experiment 2, Study 1 — recordings from 30 s before to
30 s after the appearance of the scarf during the four test
sessions.
Experiment 2, Study 2 — recordings from 10 s before to
10 s after delivery of the food reward during the three test
sessions.
Experiment 2, Study 3 — recordings from 5 s before to 5 s
after the air blower was turned on during the four test
sessions.
Observer Video Pro (version 4.0.21, Noldus Information
Technology, the Netherlands) was used to record all ear
postures irrespective of the experiment. In Experiment 1,
two independent observers noted all changes in the
position of ears according to two criteria: the position of
the ear in regard to the frontal plane of the head, and the
visibility of the auricle. Within each criterion categories
were exclusive (see Figure 2):
• Position of the ear in the frontal plane — the ears can be
aligned with frontal plane, oriented forward (the top of the ear
is in front of the frontal plane), oriented backward (the top of
the ear is behind the frontal plane), or asymmetric (the two
ears differ in their position in regard to the frontal plane);
• Visibility of the auricle — the auricles can be flat (the
inner and outer sides are not visible, the inner side is
parallel to the floor, the observer can see the full ears),
open (the inner sides are visible by an observer placed in
front of the animal), closed (the inner sides are not visible,
the outer sides are visible at the root of the ear, the ears
cannot be fully seen by the observer), asymmetric (one
inner side visible, one not).
The positions of ears in the frontal plane of the head were
recorded separately from the positions of ears according to
the visibility of the auricle. Table 1 presents the 16 theoret-
ical combinations obtained from the crossing of the
4 × 4 framework (four in the frontal plane and four facial
views for the visibility of the auricle). From the 16 combina-
tions of position of the ears, we identified four discrete ear
postures (see results from Experiment 1). These defined
postures were further encoded in all studies of Experiment 2.
Statistical analysis
We used the software SAS (version 8.1, SAS Institute Inc,
Cary, NC, USA) for all analyses. In Experiment 1, each time
an observer noted a change in ear position, we checked the
position that the other observer noted. We calculated the
frequency and the duration of each of the 256 possible asso-
ciations between the 16 combinations of ear positions from
Observer 1 and those from Observer 2. The consistency
between the two observers encoding the ear postures was
assessed with Cronbach alpha index.
In Experiment 2, the duration of ear postures was
arcsine-transformed and compared between conditions
with a mixed model of variance analysis for repeated
measures. Repetitions were for session number and time
during a session (before vs after the event). The correla-
tion matrix was considered unstructured. The results are
expressed as mean (± SD). The limit of significance was
set at P< 0.05.
Results
Experiment 1 — Identification of discrete ear postures
The consistency between observers encoding the ear
postures was high (Cronbach’s alpha = 0.8645). The obser-
vations were then considered reliable. Figure 3 shows the
frequency and mean duration of the 16 theoretical combina-
tions of ear positions determined from the frontal plane and
visibility of the auricle. Certain combinations were never
observed (ie combinations 5, 9, 10, 12 and 13, such as ears
oriented forward and flat auricles). Some other combina-
tions (ie combinations 3, 4, 7, 8, 14, 15) were displayed for
very brief periods (mean duration<1s).
The remaining combinations were frequently expressed
(combinations 1, 2, 6, 11 and 16), with significant mean
durations (ie > confidence interval of mean). These combina-
tions were therefore considered as distinctive and meaningful
ear postures. In addition, it was decided to regroup postures
1 and 2 (the two ears are either ahead or in the frontal plane
with visible auricle) since they were closely associated during
the longest expressive episodes. Finally, four discrete ear
postures were considered for further analysis:
• ‘Raised ears’ posture (R posture), which correspond to
combinations 1 and 2. The two ears are in the same position
relative to the frontal plane (either ahead or aligned), and
auricles are visible from front view;
© 2011 Universities Federation for Animal Welfare
Facial expressions of emotions in sheep 51
• ‘Ears in the plane’ posture (P posture), which corresponds
to combination 6. The two ears are in the frontal plane and
auricles are concealed from front view’
• ‘Ears backward’ posture (B posture), which corresponds to
combination 11. The two ears are behind the frontal plane
and auricles are concealed from front view; and
• ‘Asymmetrical ears’ posture (A posture), which correspond
to combination 16. The two ears are in two distinct positions
relative to the frontal and visibility of auricles is asymmetrical.
Regarding the combinations displaying for very brief
periods, they could correspond to transitional postures
between two of these four ear postures. Each of the
transitional postures was then considered as belonging
to the same defined posture to which it was associated
most often: combination 3 was then regrouped with
posture R, combinations 4, 8 and 14 were regrouped
with posture A, and combinations 7 and 15 were
regrouped with posture B.
Animal Welfare 2011, 20: 47-56
Figure 2
Position of ears collected from ewes according to two criteria: position of the ears in relation to frontal plane of the head (top) and
orientation of the auricles observed in front of the animal (bottom).
Table 1 Labels of the 16 theoretical combinations between the position of the ears in the frontal plane of the head
and the orientation of the auricles observed in front of the animal.
Front view
pv1 pv2 pv3 pv4
View from above pr1 1, pr1pv1 5, pr1pv2 9, pr1pv3 13, pr1pv4
pr2 2, pr2pv1 6, pr2pv2 10, pr2pv3 14, pr2pv4
pr3 3, pr3pv1 7, pr3pv2 11, pr3pv3 15, pr3pv4
pr4 4, pr4pv1 8, pr2pv2 12, pr4pv3 16, pr4pv4
52 Boissy et al
Experiment 2 — Assessing stable relations between
ear postures and emotional contexts
Study 1 — Suddenness/unfamiliarity
Whatever the session, the ears were mainly in the plane
posture before the appearance of the scarf (21.2 [± 3.2] vs
2.4 [± 2.1] s, 0.7 [± 0.3] and 4.8 [± 4.3] s for ear in the
plane, raised ears, asymmetric ears and ears backward;
F= 18.4, P< 0.001).
The ear postures changed when the scarf appeared. The
change depended on the speed of the presentation and the
object used for training (Table 2). In response to the rapid
appearance of the scarf, the ewes spent more time in the
asymmetric ear posture. Although the time spent in this
posture decreased during subsequent sessions, it was always
significantly higher than the time spent in the other ear
postures, except the posture with the ears in the plane.
In response to the slow appearance of the scarf in the first
session, the ewes that had been trained with the square
spent more time with the ears raised or backward while
the time spent with the ears in the plane was decreased.
From the second to the fourth session, their time spent
with the ears raised decreased whereas their time with the
ears in the plane increased.
© 2011 Universities Federation for Animal Welfare
Table 2 Duration (s) spent in ears’ postures by the ewes exposed to a neutral, a sudden or an unfamiliar event
(Experiment 2, Study 1, n = 32).
Ears in the plane (P) Ears backward (B) Asymmetric ears (A) Ears raised (R) SEM F-value P-value
Session 1
Neutral 20.3a1.0c4.2b3.1bc 2.5 6.43 0.01
Sudden 16.8a1.2d8.1b4.5c2.8 5.23 0.01
Unfamiliar 8.3a5.3c5.0c12.2b1.7 3.52 0.05
Sessions 2-4
Neutral 24.5a0.8c2.1b3.1b3.2 5.56 0.01
Sudden 19.2a0.9d7.1b4.0bc 3.3 3.23 0.05
Unfamiliar 22.0a0.5c3.4b4.2b2.8 3.74 0.05
Figure 3
Distribution of frequency and mean duration of combinations observed for fear postures. Each label indicates a specific combination (cf
Table 1). Combinations that were never observed (ie 0 values) are combinations 5, 9, 10, 12 and 13.
Facial expressions of emotions in sheep 53
The ewes that had been trained with the scarf (ie same
object as for the test) did not show a change of ear posture
from before to after the slow appearance of the scarf. The
time spent with the ears in the plane was higher than the
time spent in the other ear postures (Table 2). This differ-
ence was still significant for the next three sessions.
With the exception of the first session, the ewes spent very
little time with their ears backward after the appearance of
the scarf and this did not vary with treatments.
Study 2 — Negative contrast
The ewes were particularly sensitive to the shift in the
size of the reward (Figure 4). Compared to ewes that had
always received a small reward, those that were shifted
from a large to a small reward (ie negative contrast)
spent more time with their ears asymmetric (F= 4.5;
P< 0.01) or oriented backward (F= 3.2; P< 0.05) at the
time when the reward was delivered. For the next two
sessions, the difference between the two treatments was
significant only regarding the posture with the ears
backward (F= 2.9; P< 0.05).
Study 3 — Control
When the ewes were eating, their ears were mainly in the
plane (10.5 [± 3.5], 1.3 [± 1.1], 2.7 [± 1.3] and 0.9 [± 0.6] s for
the time spent with ears in the plane, ears raised, asymmetric
ears, and ears backward; F= 8.3, P< 0.001). The possibility
to control the situation elicited different ear postures when the
air blow was initiated (Figure 5): the ewes that could interrupt
the air blow raised their ears for longer (F= 4.9; P< 0.01) and
oriented them backwards less often (F= 8.3; P< 0.001) than
the ewes that had no control over the situation.
Animal Welfare 2011, 20: 47-56
Figure 4
Time duration (s) spent in ears postures by the ewes exposed to a negative contrast during (a) the first session and (b) the following two sessions
(Experiment 2, Study 2, n = 22). Half of the ewes that were previously trained with a large reward of food received a small one (negative contrast)
while the other half continued to receive a small reward as during training (no contrast). Four main ear postures were identified: horizontal ears
(pattern P), ears pointed backward (pattern B), asymmetric posture (pattern A) and ears rose up (pattern R). * P< 0.05; ** P< 0.01.
54 Boissy et al
Discussion
The present study aimed to identify specific emotion-related
ear postures in sheep. First, we objectively identified four
discrete ear postures: ears in the plane (the two ears are in
the frontal plane and auricles are concealed from frontal
view), ears raised (the two ears are either ahead or aligned
and auricles are visible from front view), ears oriented
backward (the two ears are behind the frontal plane and
auricles are concealed from front view), and asymmetric
ears (the two ears are in two distinct positions relative to the
frontal and visibility of auricles is asymmetrical). From the
pool of putative combinations, some combinations were
never observed; this is easily understandable since they
represent anatomically irrelevant postures. For instance,
combination 5 would correspond to ear ahead in the frontal
plane but with auricles facing the ground. Then, we
analysed the occurrences of these four discrete postures in
relation to specific experimental situations defined
according to elementary appraisal components that were
previously shown as being relevant for eliciting emotional
responses in sheep: suddenness, unfamiliarity, negative
contrast, and uncontrollability. We observed that: i) the
posture with the ears in the plane was mainly associated
with neutral situations; ii) the backward posture was associ-
ated with unfamiliar and uncontrollable unpleasant situa-
tions; iii) the posture with raised ears was specifically
displayed in response to an unfamiliar, unpleasant but
controllable situation; and iv) the asymmetric posture is
mainly displayed in sheep exposed to sudden situations.
The two postures representing raised ears (ie forward ears)
and asymmetric ears have already been reported by
Reefmann et al (2009) as increasing during social contexts
eliciting negative emotions. Nevertheless, in our current
experiments, we could link these specific ear postures with
specific emotional experiences by exposing animals to
experimental situations defined according to the cognitive
components sheep use to evaluate their environment (Désiré
et al 2002; Boissy et al 2007a; Veissier et al 2009). In
addition, the comparison between our results and what was
found in humans can help the interpretation of sheep ear
postures. For instance, the facial expression of emotions
triggered by unfamiliarity in humans is described by
lowered eyebrows and raised eyelid (Kaiser & Wehrle
2001). Interestingly, the muscle network implied in
lowering eyebrows in humans would be evolutionarily
related to the muscles controlling the mobility of the ears in
animals (Fridlund 1994). The contraction of homologous
muscles could be therefore responsible for the lowering of
eyebrows in humans and raising of ears in animals. Since
eyebrows play a major role in expressing emotions in
humans (Ekman et al 1972), emotions in farm mammals
may be reflected in their ear postures.
Most of the results reported here were obtained in situations
with a negative valence for the animals. According to Fraser
and Duncan (1998), different evolutionary processes seem
to have selected negative from positive emotions. Negative
emotions are supposed to have evolved in ‘need situations’,
such as a threat to survival or reproductive success, whereas
positive emotions are supposed to have generally evolved in
‘opportunity situations’ where the resulting action may
enhance individual fitness without being essential for it
(Boissy et al 2007b). This may be the reason why positive
© 2011 Universities Federation for Animal Welfare
Figure 5
Time duration (s) spent in ears’ postures by the ewes controlling or not the access of food (Experiment 2, Study 3, n = 26). Ewes that
were previously trained to control throughout the experiment the interruption of air blow and the access of food are compared to
yoked ewes that had no possibility to control the accesses to food. Four main ear postures were identified: horizontal ears (pattern P),
ears pointed backward (pattern B), asymmetric posture (pattern A) and ears rose up (pattern R). ** P< 0.01; *** P < 0.001.
Facial expressions of emotions in sheep 55
emotions are more variable (either inter- or intra-individ-
uals) and versatile, hence more difficult to approach than
negative emotions. Relating to the homology between
muscles involved in lowering eyebrows in humans and in
animals’ ears raising (Fridlund 1994), the previous results
would indicate that some negative emotional experiences
involve rising ears up whereas positive emotional experi-
ences could coincide with non-erect ears (in our study the
plane ear posture). Further research is thus needed on the
positive side of the emotional scale to attempt to identify
specific facial expressions as it is known in humans. For
example, asymmetry of ear postures may differ between
negative and positive emotional states, due to lateralised
behaviour (Quaranta et al 2007) thought to result from
contra-lateral hemispheric brain activity (Wager et al 2003).
From our previous studies and according to the framework
used by Sander et al (2005), sheep appear to have the
potential to feel a wide range of emotions, including fear,
anger, rage and despair, because they use the same appraisal
components involved in such emotions as in humans (Boissy
et al 2007a; Veissier et al 2009). For instance, despair in
humans is triggered by situations which are evaluated as
sudden, unfamiliar, unpredictable, discrepant from expecta-
tions, and uncontrollable, whereas boredom results from an
overly predictable environment, and all these components
have been found to affect emotional responses in sheep.
Since it has been shown in the present study that ear postures
are related to specific appraisal components, these defined
ear postures could represent specific emotional signatures in
sheep. Thus, the backward posture that is associated with
unfamiliar and uncontrollable unpleasant situations would
express fear. The raised ear posture that is displayed in
response to an unfamiliar but controllable unpleasant
situation would characterise anger. Finally, the asymmetric
ear posture that is mainly displayed in response to sudden
situations in relation with a startle response would express
surprise. The assertions described in this study are not so far
from the intuitive knowledge of breeders or other people
who have close relations with animals (and sheep in this
case). The present paper gives support to this intuitive inter-
pretation of animal expressions.
Our interpretation of ear postures in sheep from a quantita-
tive ethogram-based approach could be reinforced by
analysing the concordance with the Qualitative Behaviour
Assessment (Wemesfelder 2001), that is a method based
upon the integration by observers of perceived animal
behaviour expression, using descriptors such as ‘calm’,
‘aggressive’, ‘sociable’ or ‘indifferent’. This method, based
on the body language of animals, has been recently
validated for sheep (Wickham et al 2009). Moreover, the
description of emotion-specific expressions in sheep
provides further information to better understand the social
function of emotions. Indeed, emotions are sustained by
three main processes: physiological (ie somatic and
visceral changes), subjective (ie the mental and representa-
tional content that can be verbally described in humans),
and expressive (ie the visible changes in behaviour,
postures, gestures and expressions). It has been shown that
the expressive component of emotions are fundamental for
many social processes. This has been demonstrated not
only in humans, but also in other primates (Dantzer 1988).
However, little work has been done on other animals, such
as farm species. It has been recently shown that such
animals (eg cattle or sheep) use facial information to
recognise specific individuals (Kendrick et al 2001;
Coulon et al 2009). Hence, such animals are sensitive not
only to the presence vs absence of conspecifics, but also to
subtle physical features of specific social partners. Our
study shows that sheep express specific stable changes in
their facial appearance (ie ear postures). These changes
could provide relevant information to conspecifics about
their environment. Further studies should be done to test
such a hypothesis, ie using conditioning procedures, and to
test whether animals are able not only to recognise
conspecifics’ identity but also to identify their emotional
state throughout their ear postures.
As we already claimed in previous papers, by applying
models developed for humans, we increase the knowledge
on how animals understand their environment and the
likely emotions they can feel. Moreover, such a non-
invasive and convenient method with freely moving
animals should help to better interpret what animals expe-
rience as unpleasant in their housing environments. It
should establish the basis for understanding and then
improving current housing and husbandry conditions from
an animal’s point of view. Such findings from sheep on
how to assess emotional states may be readily transferable
to closely related prey species at the very least.
In conclusion, this study provides some insight into
emotional expressions in sheep. This constitutes a first step
to characterise specific emotion-related facial expressions
in farm animals. Observations of ear postures are a reliable
non-invasive method for assessing the valence of emotional
states in sheep. We found that: i) sheep point their ears
backward when they face unfamiliar, unpleasant, and
uncontrollable situations, hence likely to elicit fear; ii) they
point their ears up when facing a similar negative situation
but controllable, hence likely to elicit anger or at least some
preparation of an active response; and iii) their ears are
more often asymmetric in very sudden situations, likely to
elicit surprise. These findings need to be confirmed in other
situations that might be appraised similarly by sheep but
using different stimuli. It is necessary to extend these first
four expressive postures characterising neutral or negative
emotions (ie fear, anger and surprise) to take into account
positive emotions in animals.
Animal welfare implications
The interpretation of ear postures could be used to assess
farming practices from the viewpoint of animals. It could also
help to understand what a given animal is feeling at a certain
time and the subsequent behaviour it is likely to adopt, eg
flight when the ears are oriented backward or attack when they
are raised up. These specific emotion-related facial expres-
sions could be easily used to enrich the behavioural measure-
ments for an overall assessment of welfare at farm level.
Animal Welfare 2011, 20: 47-56
56 Boissy et al
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... Studies in species including pigs have reported an increase in ears being held back during / following negative experiences (e.g. sheep (Bellegarde et al., 2017;Boissy et al., 2011;Guesgen et al., 2016), pigs (Reimert et al., 2013)), whereas ears forward has been shown to indicate heightened vigilance (e.g. sheep (Boissy et al., 2011;Reefmann et al., 2009), dogs (Racca et al., 2012)). ...
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... By contrast, changes in ear posture seem to be associated with increased negative emotions or decreased positive emotions in pigs (Reimert et al., 2013). The ear postures of sheep (Ovis arie) showed consistent changes in situations involving sudden changes, stimulus familiarity, and controllability (Boissy et al., 2011). Sheep maintained their ears in a horizontal posture in a neutral state, but they pointed their ears backward in unpleasant, uncontrollable, unfamiliar situations (fear-eliciting situations), upward in negative but controllable situations (anger-eliciting situations), and displayed asymmetric ear posture in situations involving unexpected, sudden changes (surprising situations). ...
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... Facial expressions have also been studied as potential indicators of other negative and positive affective states. Most studies compared changes in the face during or immediately after exposure to a presumably positive or negative stimulus to a presumably neutral control situation, focusing on either several parts of the face [e.g., (15,16)] or only aspects, for example, the ears [e.g., (17,18)] or eyes [e.g., (19,20)]. The identified facial expressions are supposed to reflect stimulus-specific short-term affective states, i.e., emotions. ...
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... Acute responses can be seen in attempts to escape from a situation, distress vocalisations, tachycardia and increased blood cortisol as observed when animals not used to handling are put in a holding cage [17]. More subtle signs can be seen in ear postures, with animals turning their ears back when exposed to a frightening stimulus [18]. When animals are submitted to prolonged stressful situations, their behavioural reactivity can be altered leading to hyperactivity or on the contrary to hyporeactivity (sometimes referred to as 'apathy') and the functioning of the corticotropic axis is modified [19]. ...
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