-
- Abstract
- A high proportion of pet dogs show
fear-related behavioural problems, with noise
fears being most prevalent. Nonetheless, few
studies have objectively evaluated fear
expression in this species. Using owner-provided
video recordings, we coded behavioural
expressions of pet dogs during a real-life
firework situation at New Year's Eve and
compared them to behaviour of the same dogs on a
different evening without fireworks (control
condition), using Wilcoxon signed ranks tests. A
backwards-directed ear position, measured at the
base of the ear, was most strongly associated
with the fireworks condition (effect size:
Cohen's d_=_0.69). Durations of locomotion
(d_=_0.54) and panting (d_=_0.45) were also
higher during fireworks than during the control
condition. Vocalisations (d_=_0.40), blinking
(d_=_0.37), and hiding (d_=_0.37) were increased
during fireworks, but this was not significant
after sequential Bonferroni correction. This
could possibly be attributed to the high
inter-individual variability in the frequency of
blinking and the majority of subjects not
vocalising or hiding at all. Thus, individual
differences must be taken into account when
aiming to assess an individual's level of fear,
as relevant measures may not be the same for all
individuals. Firework exposure was not
associated with an elevated rate of other
so-called 'stress signals', lip licking and
yawning.
-
- Résumé
- Une forte proportion de chiens de compagnie
présente des problèmes de
comportement liés à la peur, la
peur du bruit étant la plus
répandue. Néanmoins, peu
d'études ont évalué
objectivement l'expression de la peur chez cette
espèce. À l'aide d'enregistrements
vidéo fournis par le propriétaire,
nous avons codé les expressions
comportementales de chiens de compagnie lors
d'une situation de feu d'artifice réelle
à la veille du Nouvel An et les avons
comparées au comportement des mêmes
chiens un soir différent sans feux
d'artifice (condition de contrôle), en
utilisant des tests de classement signés
par Wilcoxon.
-
- Une position de l'oreille dirigée
vers l'arrière, mesurée à
la base de l'oreille, était le plus
fortement associée à la condition
des feux d'artifice (taille de l'effet : d de
Cohen = 0,69). Les durées de locomotion
(d = 0,54) et de halètement (d = 0,45)
étaient également plus
élevées pendant les feux
d'artifice que pendant les conditions de
contrôle. Les vocalisations (d = 0,40), le
clignotement (d = 0,37) et la dissimulation (d =
0,37) ont augmenté pendant les feux
d'artifice, mais cela n'était pas
significatif après la correction
séquentielle de Bonferroni.
-
- Cela pourrait être attribué
à la forte variabilité
interindividuelle de la fréquence des
clignements des yeux et à la
majorité des sujets ne vocalisant pas ou
ne se cachant pas du tout. Ainsi, les
différences individuelles doivent
être prises en compte lorsque l'on cherche
à évaluer le niveau de peur d'un
individu, car les mesures pertinentes peuvent ne
pas être les mêmes pour tous.
L'exposition aux feux d'artifice n'était
pas associée à un taux
élevé d'autres soi-disant
«signaux de stress», de léchage
de lèvres et de bâillement.
-
-
- Introduction
- Emotions are short-term affective states
that are elicited by internal or external events
and comprise changes in several components,
including neuro-physiological, cognitive
(appraisal), motivational and expression
components, as well as the subjective
experience, or feeling1,2. As nonhuman animals
cannot report on what they are feeling, we can
attempt to infer the emotion that is likely
being experienced based on changes in these
emotion components (e.g. physiological stress
responses, behavioural expression and
behavioural choices) and the circumstances in
which these are occurring1,3. For instance,
behaviour and expressions during exposure to
potential threats can be assumed to be
fear-related while those in response to denial
of access to a desirable stimulus can be
interpreted as frustration (c.f.4,5).
-
- Identifying indicators of emotions in
nonhuman animals is important for assessing
their welfare state as well as to improve our
ability to predict subsequent behavioural
responses. This is particularly relevant in
domestic dogs, which live more closely with us
than any other species and do not only play a
role as social partners6,7, but also as therapy
dogs8, assistance dogs9,10 or working dogs with
functions ranging from search and rescue11 to
police work12. Nonetheless, problems due to
fear-related behaviour are often reported in
both pet and working dogs (e.g.13; reviewed
in14), and owners may even underestimate fear in
their dogs when not questioned about the
specific signs exhibited15.
-
- Fear is a key emotion that is highly
adaptive by prompting animals to react
adequately to threat16. When an environmental
threat (i.e. a stressor) is perceived, the
brain's fear system is activated, initiating
behavioural and physiological stress
responses17. Neuroscientists have identified
distinctions between 'fear' (an adaptive
response to a stimulus considered to be
potentially dangerous) and 'anxiety'
(anticipation of a negative outcome, lacking a
specific eliciting stimulus)18,19. However, in
practice it is often not easy to distinguish
between the two concepts behaviourally,
especially considering that anxiety promotes
fear and vice versa18,20. Hereafter, we shall
use the term 'fear' to denote both fear and
anxiety responses in dogs, since they have in
common that they are aversive emotional states
due to a (perceived) threat that are associated
with intense negative emotions and physiological
changes21, and sufficient criteria to
distinguish between the different concepts in
dogs have yet to be established (c.f.22).
-
- In response to fear, animals may respond by
freezing, hiding or fleeing, depending on the
distance of the threat and the perceived
likelihood of success23. Congruent with the
internal state, animals may also show specific
expressions; for example, a backward position of
the ears has been associated with fear in a
variety of mammalian species including sheep24,
goats25, pigs26, horses27,28 and cats29. Despite
the fear response being evolutionarily adaptive,
fear may often be elicited in situations that do
not pose real threats, as a 'false negative' may
entail high fitness costs (risk of death)
compared to a 'false positive' (an over-reaction
to an actually harmless stimulus)30. Being
associated with a negative affective state, fear
responses to stimuli in a human-dominated
environment may have detrimental effects on
animals' welfare, without serving a function in
aiding survival. For example, a fear of loud
noises is innate in many animals20, and noise
fears are among the most common fears affecting
pet dogs15,31,32. It is important to recognise
these negative affective states, to address them
and to use the right measures to evaluate
treatment progress.
-
- Surprisingly, there is a relative lack of
studies objectively evaluating the expression of
emotions in dogs. A few controlled studies have
measured behaviour and expression in dogs when
exposed to putatively fear-inducing stimuli
(note that the terminology used was variable,
with some authors referring to discrete emotions
such as fear33,34, others to stress more
generally35,36,37). Classic studies by Beerda et
al.36,37 in which dogs were exposed to various
potentially threatening stimuli, indicated that
a lowered posture (including the ears, tail and
body position) constitutes the most consistent
indicator of stress (no reference to emotions
was made) of both high and moderate intensity in
dogs. Furthermore, Beerda et al.36 suggested
that oral behaviours (such as frequency of
tongue protrusions and snout licking), yawning,
body shaking and crouching are indicative of
acute stress in dogs. However, as the severity
(as judged by the authors) of stressors was
confounded with the type of stressor
(social/non-social)36, no clear conclusions
could be drawn whether different observed
behaviours were associated with the severity of
the stressor or with the social vs non-social
context.
-
- More recently, Stellato34 confirmed that
fear in dogs towards both a social stimulus
(sudden appearance of a masked stranger) and a
non-social stimulus (sudden appearance of a
garbage bag) appears to be associated with
avoidance and/or a reduced body posture, whereas
effects on more subtle behaviours (such as body
shaking, barking, whining, lip licking, yawning,
tail wagging and paw lifting) were more
inconsistent34. Another controlled study on
puppies aged under six months inferred potential
fear indicators based on their association with
avoidance of different non-social stimuli
considered to induce mild to moderate fear33. On
this basis, a lowered posture, a lowered tail,
freezing, retreating, flinching, paw lifting and
barking were identified as the most reliable
fear indicators, while there was no association
of avoidance with ear position, tail-wagging and
lip licking33.
-
- Although noise fears represent the most
common fears in dogs15,32,38, only few studies
have been aimed to objectively quantify
fear-related behaviours in dogs during noise
events, and all of these used audio recordings.
Dreschel and Granger39 described excessive
salivation, vocalisations, hiding, pacing,
panting, remaining near the owner, and trembling
in dogs exposed to a thunderstorm recording at
the clinic, though they did not assess to which
extent these behaviours differed from a baseline
condition.
-
- De Souza et al.40 found that dogs both
classified as 'sound sensitive' and as 'not
sound sensitive' (categorisations based on
owners' description of the severity of signs)
reacted to recordings of a firework by
increasing alertness and attention, panting,
searching for the sound, startling, trembling,
hiding and running away, with 'sound sensitive'
dogs showing a greater intensity of reaction for
alertness and attention, searching the sound,
trembling, hiding and running away, as well as
showing less resting and winking/sleeping. No
significant effects were reported for variables
related to the posture and tail, lip licking,
yawning, vocalisations, elimination, and
destruction40.
-
- Some experimental studies yielded
conflicting behavioural results, reporting
either a reduction in activity41,42 or an
increase in activity43,44,45 in response to
audio recordings of thunderstorms or fireworks.
These different findings could potentially be
explained by different coping strategies of dogs
when exposed to fear-inducing noises, an active
and a passive response: Landsberg et al.45 used
separate scores for active (including aimless,
repetitive or stereotypic pacing, running or
circling; retreating to a hide, digging,
climbing, jumping or barking) and passive
(encompassing decreased activity, freezing
against a wall, staying close to the door,
crouching, tail between legs, ears back,
panting, trembling, being alert/tense/vigilant,
salivating, yawning, lip licking, lifting a
foreleg and whining) responses to audio
stimulation. Both active and passive scores were
increased in beagle dogs during noise exposure
compared to before and after stimulation,
indicating validity of the scores. However,
individual behavioural parameters were not
analysed45.
-
- While the standardisation of noise exposure
in studies using laboratory settings has many
advantages, it is not clear to what extent the
findings can be transferred to dogs' fear
responses in a home setting. For example, with
regard to noise fears, some discrepancies
between owner-reported improvements in
fearfulness and dogs' behaviour when exposed to
a noise recording in a clinic setting have been
reported46,47. Recordings cannot fully represent
the characteristics of real noises and the range
of stimuli (e.g. atmospheric changes associated
with thunder or lights accompanying fireworks)
(c.f.48,49), and some dogs do not respond to
these simulations even under optimal
conditions49.
-
- Here we aimed to identify fear indicators in
pet dogs in a real-life situation, during New
Year's eve fireworks, by comparing dogs'
behavioural expression during firework exposure
to a control night with no fireworks present. By
taking advantage of situations in which dogs are
exposed unavoidably to these stimuli, i.e. at
New Year's Eve, it was possible to study dogs'
fear reactions without ethical concerns due to
an artificial induction of fears. Hereafter we
refer to dogs' expressions during fireworks as
'fear' expressions, being aware that we can only
infer the underlying affective state.
-
- Predictions
- Based on the literature, we predicted that
dogs show the following behavioural expressions
during fireworks compared to the control
condition: a lowered posture (c.f.33,34,35,36),
a lowered tail position (c.f.33,45), a more
backwards-directed ear position (c.f.45,50), an
increased frequency of vocalisations
(c.f.15,39), an increased duration of panting
(c.f.22,39,51), an increased frequency of
blinking (c.f.52), an increased frequency of lip
licking and yawning (c.f.36,37), a change in
activity (time moving, c.f.43,45) and an
increased time hiding (c.f.40).
-
- To test these predictions, we performed a
citizen science study, asking volunteer dog
owners to film their dogs for five minutes (1)
during fireworks on New Year's Eve (firework
video) and (2) again several days later at a
similar time in the evening (control video),
when they considered their dog's behaviour to
have normalised. Videos of 36 dogs were coded
based on an ethogram (Table 1), and expressions
and behaviours during firework and control
videos were compared using Wilcoxon signed ranks
tests. In an accompanying questionnaire, owners
rated on a scale from 1 to 5 how much their
dogs' welfare was impaired by fireworks
('Welfare Impaired score', c.f.32). Only dogs
with scores of 2 and above were considered in
the current study (Supplementary Table S1).
Although we excluded dogs receiving medication,
and thus potentially the most fearful subjects,
the median 'Welfare Impaired score' of the 36
dogs included was still high at 4 (IQR
2.75&endash;5).
-
- Discussion
- In the current study, a backwards directed
ear position was the indicator most strongly
associated with the firework condition, and
presumably a fearful state in dogs, perhaps
because tail position and body posture could not
be evaluated. Although "ears back" or "flattened
ears" are often used to assess fearfulness in
dogs (e.g.43,45,48), the scientific data to
validate this expression as an indicator of fear
is surprisingly thin. In studies by Beerda et
al.36,37, a 'posture score' comprising ear
position along with tail position and breed
specific posture was one of the best indicators
of both "moderate and severe stress"36,37;
however, even if the individual components of
this score, body position, tail position and ear
position often co-vary, it is important to have
more detailed measures available and to take
into account evidence from individual
variables.
-
- Flint et al.33 differentiated between a
lowered posture, a lowered tail and "ears back"
in their study on fear expression in puppies,
but while their study confirmed both a reduced
posture and a lowered tail to be indicative of
fear in dogs, they found no relationship between
puppies' avoidance behaviour (used as proxy to
infer fearfulness) and whether they had their
ears back. This could simply be explained by the
low video quality, as suggested by Flint et
al.33, but another possible explanation could be
the confounding effects of alertness. In the
firework videos in the current study, dogs often
appeared to be vigilant and may thus have been
holding the ears up. However, when looking at
the base of the ears (as per our definition), it
was discernible that the ears were turned
backwards relative to the position judged to be
neutral by the raters.
-
- Our data thus suggest that a
backwards-directed ear position, judged at the
base of the ears, is a valid indicator of a
fearful state in dogs. In the Dog Facial Action
Coding System (DogFACS53), a system for
objectively analysing facial movements in dogs,
a differentiation is made between several ear
position changes including the ears flattener,
the ears rotator and ears downwards. While the
ears flattener and the ears rotator can only be
distinguished in dog with upright ears but not
those with floppy ears43, it is a possibility
that it is the backwards rotation of the ears
that is most consistently associated with
non-social fear at least in dogs with erect
ears. Nonetheless, while fear of fireworks
appears to be reliably associated with
backwards-directed ears (as measured at the base
of the ears), this is only one of several
contexts where this expression may be observed;
for example, backwards-directed ears are also
shown during frustration5, as well as in
affiliative greeting situations during active
submission54. Future studies could investigate
subtle differences in ear position and
associated contexts in more detail.
-
- Locomotion was significantly elevated during
fireworks compared to the control night. While
this finding per se does not necessarily signify
fear, as dogs might have adapted their own
activity to the heightened activity in the
household at a time of day where they were
usually sleeping, pacing has previously been
described as a behavioural expression of noise
fears in dogs22,39. Our definition did not allow
to differentiate between pacing and locomotion,
but personal observations indicated that besides
pacing, an increase in locomotion appeared to be
due to an inability to settle (attempting to lie
down in one locations, then changing to a new
location shortly thereafter) in some dogs in the
current study. Thus it might reflect fear or
anticipatory anxiety awaiting the next bang.
Previous studies indicated that some dogs react
to loud noise by decreasing activity, others
with an increase in activity45. Besides the
possible difference in active vs passive coping
styles45, the diverging results of previous
studies regarding changes in activity when dogs
were exposed to noise recordings could possibly
be explained by the novelty of the environment:
In a novel environment (such as during open
field tests42,43), exploration would be expected
in the beginning of the test. Consequentially,
startling stimuli could be expected to inhibit
exploration, and thus activity. On the other
hand, after animals have habituated to the
surroundings or if they are familiar with the
environment such as in the present study, they
might be more likely to spend the time resting,
and so an increase in activity, as in the
current study, might be noted as a result of
fear-inducing events.
-
- Panting was significantly associated with
the fireworks condition in the current study,
with eight of the nine dogs who panted doing so
only during the fireworks. We consider panting
in this situation to be fear-related, as the
increased locomotion observed at the group level
during fireworks cannot account for the high
amount of time panting in the eight dogs that
panted: four of these dogs remained stationary
throughout the video, and only two were moving
for more than ten percent of the time.
Similarly, in a previous study, panting and
pacing constituted differing coping strategies
employed by different dogs22.
-
- While the primary function of panting lies
in thermoregulation55, panting is commonly
regarded as an indicator of short-term stress,
fear or anxiety in dogs37,39,56,57. One possible
explanation for the mechanism underlying this
association might be the need to dissipate heat,
since stress leads to an increase in core body
temperature, as commonly reported in dogs58 and
other mammalian species (reviewed in59). Panting
has been described as a consequence of the rapid
activation of the autonomic nervous system,
along with piloerection and trembling60 and may
be a response associated with physiological
arousal due to perceived external stimuli in
dogs56. As in the current study, only a subset
of dogs have been observed to pant during
stressful situations, one contributing factor
being dog size. Pastore et al.56 found a higher
incidence of panting in female and larger dogs
during a high-arousal situation, the latter
being consistent with panting as a
thermoregulatory response due to stress-induced
hyperthermia, given that smaller dogs will
dissipate relatively more heat from their bodies
than bigger dogs due to their larger
surface/volume ratio (c.f.61).
-
- However, some contradictory results
regarding panting in dogs in relation to
stressful situations have been found. Although
panting is often increased in fear-inducing
situations22,39,51, panting in young dogs_<_6
months was reduced during exposure to
fear-inducing stimuli relative to control
trials33, and dogs that were separated from
their owner showed an increased frequency of
panting upon reunion with their owner62. Panting
might thus be indicative of both positive and
negative arousal (c.f. 56). These behavioural
signs thus need to be interpreted in the context
in which they are occurring and in conjunction
with other indicators.
-
- The frequency of vocalisations was higher
during the fireworks than during the control
night (after correction for multiple testing,
this was only a trend), but as with panting,
this effect was driven by just nine individuals
&endash; the majority of subjects did not
vocalise at all during either condition. Like
panting, vocalisations can occur in contexts
unrelated to fear, such as during greeting, play
initiation, submission, defence, threatening
behaviour, contact seeking, pain, or loneliness
(reviewed in63). Thus, while panting and
vocalising in a putatively fear-inducing
situations may signify fear (e.g.43,45,46,52),
they can also be shown for various other
reasons. Conversely, we cannot draw the
conclusion that there is no fear in the absence
of these signs. For example, Overall et al.22
reported that dogs of different breeds may
respond differently to loud noises (e.g. German
shepherds often reacted by pacing, while Border
collies and Australian shepherds showed a high
rate of hiding and panting). Also individuals
within a single breed may adopt different coping
strategies associated with either active or
passive (and more subtle) coping
behaviours43,44.
-
- Taken together, both the sensitivity and the
specificity of vocalisations and of panting as
fear indicators are low; i.e. not all fearful
dogs vocalise or pant, and not all dogs that
vocalise or pant are fearful. It is important to
take such individual behavioural differences
into account when making an assessment of an
individual's level of fear. Therefore, since
relevant measures may not be the same for all
individuals, it is likely that the assessment of
the animal's putative emotional state can be
improved by considering evidence from several
different indicators as well as the context
(c.f.3).
-
- In line with the suggestion by Mills52 that
an elevated blinking rate may be associated with
fear in dogs, blinking tended to be higher
during the fireworks night compared to the
control night (not significant after correction
for multiple testing). In view of large
inter-individual baseline differences in this
measure and the need to correct for multiple
testing, our study may have been underpowered
for detecting a significant effect &endash; the
effect size was moderate at Cohen's d_=_0.38.
Blinking constitutes a component of the startle
reflex64, which could potentially explain the
higher rate of blinking during fireworks.
However, it has also been considered as an
indicator of stress and/or anxiety per se in
humans (e.g.64,65,66,67,68). Moreover, in dogs,
Bremhorst et al.5 found an increase in blinking
frequency when dogs were frustrated. This might
indicate that an elevated blinking rate may
constitute a sign of stress in dogs, rather than
being specific to the emotions of either fear or
frustration. Perhaps one difficulty of using
this indicator in an applied setting lies in the
fact that blinking is also a normal mammalian
behaviour necessary to prevent dry eyes69, and
so it would be necessary to identify deviations
from baseline rates in order to draw conclusions
about possible underlying affective states.
Notably, the inter-individual variation in
blinking rate also during the control condition
was very high in our study (mean: 3.83/min, SD
4.07).
-
- Dogs tended to hide more during the
fireworks night than during the control night
(non-significant after correction for multiple
testing). Other studies similarly reported
hiding in dogs that were exposed to loud noises,
but as in our study there appeared to be much
variation in whether dogs adopted this coping
strategy22,39,40. A convenience sample was used
in the current study. While the dogs in the
current study were rated as mostly fearful by
their owners (see Methods), in a study on dogs
that were diagnosed with noise phobia,
proportions of dogs showing hiding (85%) and
panting (67%, as reported by the dogs' owners)
were higher than in the current study. Since our
analysis was based on just three minutes of
video material, it is possible that these
behaviours, if they occurred, were not captured
in the videos analysed, or they might be
characteristic of more severe fear responses, as
also indicated by de Souza et al.40. In
contrast, more subtle indicators such as ears
back might be more ubiquitously shown in fearful
situations.
-
- Our data show that even very strong
fear-inducing non-social stimuli, fireworks, are
not associated with an elevation in the rate of
the so-called 'stress signals' lip licking or
yawning in dogs. Similarly, de Souza et al.40
did not find an increase in lip licking and
yawning in dogs exposed to recordings of a
thunderstorm. Also, less severe fear-inducing
non-social stimuli were unrelated to rates of
lip licking33,34 or yawning33. In Stellato et
al.34, subtle behaviours, including lip licking
and yawning, were not affected by a non-social
stimulus, but moderate correlations were found
with the level of avoidance shown by dogs upon
appearance of a masked stranger and when
approaching the stranger. However, evidence was
not conclusive, as there was much individual
variation in these behavioural signs, the
frequency per individual was low, and not all
dogs rated as fearful based on gross behavioural
measures showed these subtle behaviours at
all34. Our results affirm the conclusion by
Stellato et al.34 that these expressions do not
represent good measures of fear in dogs, at
least not with regard to non-social stimuli.
Alternatively, they might play a role in social
communication. Lip licking and yawning have been
considered to function as appeasement signals
both inter54- and intraspecifically70, and lip
licking appears to be shown in situations of
mild social threat (but less so during severe
threats)54, as well as in greeting
situations54,71,72.
-
- Conclusions
- To our knowledge, this is the first study
objectively measuring behavioural expression of
pet dogs in their home settings during exposure
to real-life fireworks, an approach which has
advantages and drawbacks. Thus, due to using a
citizen science approach, it was not possible to
achieve complete standardisation and control,
such as regarding firework intensity, owner
behaviour and possible variation besides
fireworks between the firework and the control
situation. We made the decision not to restrict
owners' behaviour for ethical reasons to avoid
imposing additional fear on dogs that might
normally gain comfort from their owners, but
also in view of having a real-life scenario, the
latter being an advantage of the current study.
Despite the fact that the study was not
perfectly controlled, we are confident that the
fireworks were the most salient arousing
stimulus during the firework videos, as we
discerned no presence of guests or unusual
behaviours by the participating owners.
Importantly, the observed behavioural
differences shown during fireworks as compared
to the control night are consistent with
behavioural signs reported previously for noise
fears in dogs, providing external validation to
scales to assess noise fears in dogs where these
behavioural signs are included (e.g.73) and
strengthening the assumption that the measured
behaviours are indeed fear-related.
-
- Nonetheless it has to be acknowledged that
identifying behavioural indicators of emotions
in dog is challenging, as on the one hand,
domestic dogs have a very rich behavioural
repertoire, on the other hand, similar
expressions may be shown in different contexts,
and different individuals may react differently
to fear-inducing situations, as indicated in
this and previous studies. Based on the
component process model of emotions, inferences
about the probable emotion experienced by
nonhuman animals can be made based on the
combined analysis of the appraisal component
(presence of stimuli that may be emotionally
relevant for the animal), the arousal component
(e.g. heart rate), action tendency, and finally
behavioural expression3. Thus, in future
studies, the identification of behavioural
emotion indicators could be strengthened further
by including an objective measurement of the
arousal component, such as via heart rate or
cortisol measurements. While it may often not be
feasible in clinical practice to obtain
physiological measurements to gauge dogs'
arousal associated with fear reactions in their
home environment, collecting as much information
as possible regarding the appraisal component
(emotional relevance of the situation; in this
case firework noises, which are perceived as
threatening by many dogs), action tendency (e.g.
escape attempts), and a variety of different
expressive behaviours, may constitute the best
method to infer the likely underlying emotion
experienced by nonhuman animals.
-
|
